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Regenerating Heart Valves

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Regenerating the Heart

Part of the book series: Stem Cell Biology and Regenerative Medicine ((STEMCELL))

Abstract

Valvular heart disease is a significant cause of morbidity and mortality worldwide. Current options for surgical heart valve replacement are associated with several major disadvantages as clinically available valve prostheses represent nonviable structures and lack the potential to grow, repair, and remodel. Heart valve tissue engineering represents a promising scientific concept to overcome these limitations, aiming at the fabrication of living autologous heart valves with a thromboresistant surface and a viable interstitium with repair and remodeling capabilities. Following the in vitro tissue engineering concept, autologous cells are harvested and seeded onto three-dimensional matrices followed by biomimetic conditioning enabling the development of neo-heart valve tissue. Here, we review the concept of both in vitro and in vivo heart valve tissue engineering, focusing in particular on different synthetic scaffold materials and available cell sources for the fabrication of living autologous heart valve substitutes.

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Abbreviations

α-SMA:

α-Smooth muscle actin

BMSC:

Bone-marrow-derived stem cell

ECM:

Extracellular matrix

EPC:

Endothelial progenitor cell

MSC:

Marrow stromal cell

P4HB:

Poly(4-hydroxybutyrate)

PGA:

Polyglycolic acid

PHA:

Polyhydroxyalkanoate

PLA:

Polylactic acid

VEGF:

Vascular endothelial growth factor

WMF:

Myofibroblast derived from Wharton’s jelly

References

  1. Iung B, Vahanian A (2006) Valvular heart diseases in elderly people. Lancet 368(9540):969–71

    Article  PubMed  Google Scholar 

  2. Otto CM, Lind BK, Kitzman DW et al (1999) Association of aortic-valve sclerosis with cardiovascular mortality and morbidity in the elderly. N Engl J Med 341(3):142–7

    Article  PubMed  CAS  Google Scholar 

  3. Supino PG, Borer JS, Preibisz J (2006) The epidemiology of valvular heart disease: a growing public health problem. Heart Fail Clin 2:379–93

    Article  PubMed  Google Scholar 

  4. Yacoub MH, Cohn LH (2004) Novel approaches to cardiac valve repair: from structure to function: part I. Circulation 109:942–50

    Article  PubMed  Google Scholar 

  5. Mikos AG, Herring SW, Ochareon P et al (2006) Engineering complex tissues. Tissue Eng 12(12):3307–39

    Article  PubMed  CAS  Google Scholar 

  6. Yacoub MH, Takkenberg JJ (2005) Will heart valve tissue engineering change the world? Nat Clin Pract Cardiovasc Med 2:60–1

    Article  PubMed  CAS  Google Scholar 

  7. Nkomo VT, Gardin JM, Skelton TN et al (2006) Burden of valvular heart diseases: a population-based study. Lancet 368(9540):1005–11

    Article  PubMed  Google Scholar 

  8. Ruel J, Lachance G (2009) A new bioreactor for the development of tissue-engineered heart valves. Ann Biomed Eng 37(4):674–81

    Article  PubMed  Google Scholar 

  9. Yoganathan AP, He Z et al (2004) Fluid mechanics of heart valves. Annu Rev Biomed Eng 6:331–62

    Article  PubMed  CAS  Google Scholar 

  10. Dasi LP, Simon HA, Sucosky P et al (2009) Fluid mechanics of artificial heart valves. Clin Exp Pharmacol Physiol 36(2):225–37

    Article  PubMed  CAS  Google Scholar 

  11. Zilla P, Brink J, Human P et al (2008) Prosthetic heart valves: catering for the few. Biomaterials 29:385–406

    Article  PubMed  CAS  Google Scholar 

  12. Bonow RO, Carabello BA, Kanu C et al (2006) ACC/AHA 2006 guidelines for the management of patients with valvular heart disease: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines. Circulation 114(5):e84–231

    Article  PubMed  Google Scholar 

  13. Lee KY, Mooney DJ (2001) Hydrogels for tissue engineering. Chem Rev 101(7):1869–79

    Article  PubMed  CAS  Google Scholar 

  14. Senthilnathan V, Treasure T, Grunkemeier G et al (1999) Heart valves: which is the best choice? Cardiovasc Surg 7(4):393–7

    Article  PubMed  CAS  Google Scholar 

  15. Schoen FJ (2008) Evolving concepts of cardiac valve dynamics: the continuum of development, functional structure, pathobiology, and tissue engineering. Circulation 118:1864–80

    Article  PubMed  Google Scholar 

  16. Schoen JF (1997) Aortic valve structure–function correlations: role of elastic fibers no longer a stretch of imagination. J Heart Valve Dis 6:1–6

    PubMed  CAS  Google Scholar 

  17. Yacoub MH, Kilner PJ, Birks EJ, Misfeld M (1999) The aortic outflow and root: a tale of dynamism and crosstalk. Ann Thorac Surg 68(3 Suppl):S37–43

    Article  PubMed  CAS  Google Scholar 

  18. Simmons CA (2009) Aortic valve mechanics: an emerging role for the endothelium. J Am Coll Cardiol 53:1456–8

    Article  PubMed  Google Scholar 

  19. Misfeld M, Sievers HH (2007) Heart valve macro- and microstructure. Philos Trans R Soc Lond B Biol Sci 362(1484):1421–36

    Article  PubMed  Google Scholar 

  20. Butcher JT, Simmons CA, Warnock JN (2008) Mechanobiology of the aortic heart valve. Heart Valve Dis 17(1):62–73

    Google Scholar 

  21. Peskin CS, McQueen DM (1994) Mechanical equilibrium determines the fractal fiber architecture of aortic heart valve leaflets. Am J Physiol 266(1 Pt 2):H319–28

    PubMed  CAS  Google Scholar 

  22. Thubrikar MJ, Aouad J, Nolan SP (1986) Comparison of the in vivo and in vitro mechanical properties of aortic valve leaflets. J Thorac Cardiovasc Surg 92:29–36

    PubMed  CAS  Google Scholar 

  23. Schoen FJ, Levy RJ (1999) Tissue heart valves: current challenges and future research perspectives. Biomed Mater Res 47(4):439–65

    Article  CAS  Google Scholar 

  24. Scott M, Vesely I (1995) Aortic valve cusp microstructure: the role of elastin. Ann Thorac Surg 60(2 Suppl):S391–4

    Article  PubMed  CAS  Google Scholar 

  25. Scott MJ, Vesely I (1996) Morphology of porcine aortic valve cusp elastin. J Heart Valve Dis 5(5):464–71

    PubMed  CAS  Google Scholar 

  26. Bairati A Jr, De Biasi S, Pilotto F (1978) Smooth muscle cells in the cusps of the aortic valve of pigs. Experientia 34(12):1636–8

    Article  PubMed  Google Scholar 

  27. Bairati A, DeBiasi S (1981) Presence of a smooth muscle system in aortic valve leaflets. Anat Embryol (Berl) 161(3):329–40

    Article  CAS  Google Scholar 

  28. Roy A, Brand NJ, Yacoub MH (2000) Molecular characterization of interstitial cells isolated from human heart valves. J Heart Valve Dis 9(3):459–64; discussion 464–5

    PubMed  CAS  Google Scholar 

  29. Della Rocca F, Sartore S, Guidolin D et al (2000) Cell composition of the human pulmonary valve: a comparative study with the aortic valve – the VESALIO Project. Ann Thorac Surg 70(5):1594–600

    Article  PubMed  CAS  Google Scholar 

  30. Messier RH Jr, Bass BL, Aly HM et al (1994) Dual structural and functional phenotypes of the porcine aortic valve interstitial population: characteristics of the leaflet myofibroblast. J Surg Res 57(1):1–21

    Article  PubMed  Google Scholar 

  31. Langer R, Vacanti JP (1993) Tissue engineering. Science 260:920–6

    Article  PubMed  CAS  Google Scholar 

  32. Matheny RG, Hutchison ML, Dryden PE et al (2000) Porcine small intestine submucosa as a pulmonary valve leaflet substitute. J Heart Valve Dis 9:769–75

    PubMed  CAS  Google Scholar 

  33. Mol A, Bouten CV, Baaijens FP et al (2004) Review article: tissue engineering of semilunar heart valves: current status and future developments. J Heart Valve Dis 13(2):272–80

    PubMed  Google Scholar 

  34. Schmidt D, Stock UA, Hoerstrup SP (2007a) Tissue engineering of heart valves using decellularized xenogeneic or polymeric starter matrices. Philos Trans R Soc Lond B Biol Sci 362(1484):1505–12

    Article  PubMed  CAS  Google Scholar 

  35. Schmidt D, Mol A, Kelm JM et al (2007b) In vitro heart valve tissue engineering. Methods Mol Med 140:319–30

    Article  PubMed  CAS  Google Scholar 

  36. Schmidt D, Achermann J, Odermatt B et al (2007c) Prenatally fabricated autologous human living heart valves based on amniotic fluid derived progenitor cells as single cell source. Circulation 116:I64–70

    Article  PubMed  Google Scholar 

  37. Breuer CK, Mettler BA, Anthony T et al (2004) Application of tissue-engineering principles toward the development of a semilunar heart valve substitute. Tissue Eng 10(11–12):1725–36

    Article  PubMed  CAS  Google Scholar 

  38. Brody S, Pandit A (2007) Approaches to heart valve tissue engineering scaffold design. J Biomed Mater Res B Appl Biomater 83(1):16–43

    PubMed  Google Scholar 

  39. Sacks MS, Schoen FJ, Mayer JE (2009) Bioengineering challenges for heart valve tissue engineering. Annu Rev Biomed Eng 11:289–313

    Article  PubMed  CAS  Google Scholar 

  40. Lichtenberg A, Cebotari S, Tudorache I et al (2007) Biological scaffolds for heart valve tissue engineering. Methods Mol Med 140:309–17

    Article  PubMed  CAS  Google Scholar 

  41. Sales VL, Engelmayr GC Jr, Johnson JA Jr et al (2007) Protein precoating of elastomeric tissue-engineering scaffolds increased cellularity, enhanced extracellular matrix protein production, and differentially regulated the phenotypes of circulating endothelial progenitor cells. Circulation 116(11 Suppl):I55–63

    PubMed  CAS  Google Scholar 

  42. Affonso da Costa FD, Dohmen PM, Lopes SV et al (2004) Comparison of cryopreserved homografts and decellularized porcine heterografts implanted in sheep. Artif Organs 28:366–70

    Article  PubMed  Google Scholar 

  43. Allen BS, El-Zein C, Cuneo B et al (2002) Pericardial tissue valves and Gore-Tex conduits as an alternative for right ventricular outflow tract replacement in children. Ann Thorac Surg 74:771–77

    Article  PubMed  Google Scholar 

  44. Bielefeld MR, Bishop DA, Campbell DN et al (2001) Reoperative homograft right ventricular outflow tract reconstruction. Ann Thorac Surg 71:482–7; discussion 7–8

    Article  PubMed  CAS  Google Scholar 

  45. Carr-White GS, Glennan S, Edwards S et al (1999) Pulmonary autograft versus aortic homograft for rereplacement of the aortic valve: results from a subset of a prospective randomized trial. Circulation 100(19 Suppl):II103–6

    PubMed  CAS  Google Scholar 

  46. Grauss RW, Hazekamp MG, van Vliet S et al (2003) Decellularization of rat aortic valve allografts reduces leaflet destruction and extracellular matrix remodeling. J Thorac Cardiovasc Surg 126:2003–10

    Article  PubMed  CAS  Google Scholar 

  47. Hong H, Dong GN, Shi WJ et al (2008) Fabrication of biomatrix/polymer hybrid scaffold for heart valve tissue engineering in vitro. ASAIO J 54(6):627–32

    Article  PubMed  CAS  Google Scholar 

  48. Hong H, Dong N, Shi J et al (2009) Fabrication of a novel hybrid heart valve leaflet for tissue engineering: an in vitro study. Artif Organs 33(7):554–8

    Article  PubMed  Google Scholar 

  49. Neidert MR, Tranquillo RT (2006) Tissue-engineered valves with commissural alignment. Tissue Eng 12(4):891–903

    Article  PubMed  Google Scholar 

  50. Robinson PS, Johnson SL, Evans MC et al (2008) Functional tissue-engineered valves from cell-remodeled fibrin with commissural alignment of cell-produced collagen. Tissue Eng Part A 14:83–95

    Article  PubMed  CAS  Google Scholar 

  51. Syedain ZH, Weinberg JS, Tranquillo RT (2008) Cyclic distension of fibrin-based tissue constructs: evidence of adaptation during growth of engineered connective tissue. Proc Natl Acad Sci 105(18):6537–42

    Article  PubMed  CAS  Google Scholar 

  52. Williams C, Johnson SL, Robinson PS et al (2006) Cell sourcing and culture conditions for fibrin-based valve constructs. Tissue Eng 12:1489–502

    Article  PubMed  CAS  Google Scholar 

  53. Mol A, Smits AI, Bouten CV et al (2009) Tissue engineering of heart valves: advances and current challenges. Expert Rev Med Devices 6(3):259–75

    Article  PubMed  CAS  Google Scholar 

  54. Kasimir MT, Rieder E, Seebacher G et al (2003) Comparison of different decellularization procedures of porcine heart valves. Int J Artif Organs 26(5):421–7

    PubMed  CAS  Google Scholar 

  55. Leyh RG, Wilhelmi M, Rebe P et al (2003) In vivo repopulation of xenogeneic and allogeneic acellular valve matrix conduits in the pulmonary circulation. Ann Thorac Surg 75(5):1457–63; discussion 1463

    Article  PubMed  Google Scholar 

  56. Steinhoff G, Stock U, Karim N et al (2000) Tissue engineering of pulmonary heart valves on allogenic acellular matrix conduits: in vivo restoration of valve tissue. Circulation 102:50–5

    Google Scholar 

  57. Curtil A, Pegg DE, Wilson A (1997) Repopulation of freeze-dried porcine valves with human fibroblasts and endothelial cells. J Heart Valve Dis 6(3):296–306

    PubMed  CAS  Google Scholar 

  58. Wilson GJ, Courtman DW, Klement P et al (1995) Acellular matrix: a biomaterials approach for coronary artery bypass and heart valve replacement. Ann Thorac Surg 1995 60:353–8

    Article  Google Scholar 

  59. Bader A, Schilling T, Teebken OE et al (1998) Tissue engineering of heart valves – human endothelial cell seeding of detergent acellularized porcine valves. Eur J Cardiothorac Surg 14(3):279–84

    Article  PubMed  CAS  Google Scholar 

  60. Bertiplaglia B, Ortolani F, Petrelli L et al (2003) Cell characterization of porcine aortic valve and decellularized leaflets repopulated with aortic valve interstitial cells: the VESALIO project. Ann Thorac Surg 75:1274–82

    Article  Google Scholar 

  61. Booth C, Korossis SA, Wilcox HE et al (2002) Tissue engineering of cardiac valve prostheses I: development and histological characterization of an acellular porcine scaffold. J Heart Valve Dis 11(4):457–62

    PubMed  Google Scholar 

  62. Kim WG, Park JK, Lee WY (2002) Tissue-engineered heart valve leaflets: an effective method of obtaining acellularized valve xenografts. Int J Artif Organs 25(8):791–7

    PubMed  CAS  Google Scholar 

  63. Zeltinger J, Landeen LK, Alexander HG et al (2001) Development and characterization of tissue-engineered aortic valves. Tissue Eng 7:9–22

    Article  PubMed  CAS  Google Scholar 

  64. Rieder E, Kasimir MT, Silberhumer G et al (2004) Decellularization protocols of porcine heart valves differ importantly in efficiency of cell removal and susceptibility of the matrix to re-cellularization with human vascular cells. J Thorac Cardiovasc Surg 127(2):399–405

    Article  PubMed  Google Scholar 

  65. Tudorache I, Cebotari S, Sturz G et al (2007) Tissue engineering of heart valves: biomechanical and morphological properties of decellularized heart valves. J Heart Valve Dis 16:567–73

    PubMed  Google Scholar 

  66. Cushing MC, Jaeggli MP, Masters KS et al (2005) Serum deprivation improves seeding and repopulation of acellular matrices with valvular interstitial cells. J Biomed Mater Res A 75(1):232–41

    PubMed  Google Scholar 

  67. Knight RL, Booth C, Wilcox HE et al (2005) Tissue engineering of cardiac valves: re-seeding of acellular porcine aortic valve matrices with human mesenchymal progenitor cells. J Heart Valve Dis 14(6):806–13

    PubMed  Google Scholar 

  68. Schenke-Layland K, Opitz F, Gross M (2003) Complete dynamic repopulation of decellularized heart valves by application of defined physical signals – an in vitro study. Cardiovasc Res 60:497–509

    Article  PubMed  CAS  Google Scholar 

  69. Kim SS, Lim SH, Hong YS et al (2006) Tissue engineering of heart valves in vivo using bone marrow-derived cells. Artif Organs 30(7):554–7

    Article  PubMed  Google Scholar 

  70. Takeuchi Y (2000) Risk of zoonosis in xenotransplantation. Transplant Proc 32:2698–700

    Article  PubMed  CAS  Google Scholar 

  71. Weiss RA, Magre S, Takeuchi Y (2000) Infection hazards of xenotransplantation. J Infect 40:21–5

    Article  PubMed  CAS  Google Scholar 

  72. Martin U, Kiessig V, Blusch JH et al (1998) Expression of pig endogenous retrovirus by primary porcine endothelial cells and infection of human cells. Lancet 352:692–4

    Article  PubMed  CAS  Google Scholar 

  73. Martin U, Winkler ME, Id M et al (2000) Productive infection of primary human endothelial cells by pig endogenous retrovirus (PERV). Xenotransplantation 7(2):138–42

    Article  PubMed  CAS  Google Scholar 

  74. Moza AK, Mertsching H, Herden T et al (2001) Heart valves from pigs and the porcine endogenous retrovirus: experimental and clinical data to assess the probability of porcine endogenous retrovirus infection in human subjects. J Thorac Cardiovasc Surg 121:697–701

    Article  PubMed  CAS  Google Scholar 

  75. Patience C, Takeuchi Y, Weiss RA (1997) Infection of human cells by an endogenous retrovirus of pigs. Nat Med 3(3):282–6

    Article  PubMed  CAS  Google Scholar 

  76. Patience C, Switzer WM, Takeuchi Y et al (2001) Multiple groups of novel retroviral genomes in pigs and related species. J Virol 75:2771–5

    Article  PubMed  CAS  Google Scholar 

  77. Prabha S, Verghese S (2008) Existence of proviral porcine endogenous retrovirus in fresh and decellularised porcine tissues. Indian J Med Microbiol 26(3):228–32

    Article  PubMed  CAS  Google Scholar 

  78. Specke V, Rubant S, Denner J (2001) Productive infection of human primary cells and cell lines with porcine endogenous retroviruses. Virology 285:177–80

    Article  PubMed  CAS  Google Scholar 

  79. Wilson CA, Wong S, Muller J et al (1998) Type C retrovirus released from porcine primary peripheral blood mononuclear cells infects human cells. J Virol 72:3082–7

    PubMed  CAS  Google Scholar 

  80. Knight R, Brazier M, Collins SJ (2004) Human prion diseases: cause, clinical and diagnostic aspects. Contrib Microbiol 11:72–97

    Article  PubMed  Google Scholar 

  81. Knight R, Collins S (2001) Human prion diseases: cause, clinical and diagnostic aspects. Contrib Microbiol 7:68–92

    Article  PubMed  CAS  Google Scholar 

  82. Kallenbach K, Leyh RG, Lefik E et al (2004) Guided tissue regeneration: porcine matrix does not transmit PERV. Biomaterials 25(17):3613–20

    Article  PubMed  CAS  Google Scholar 

  83. Walles T, Lichtenberg A, Puschmann C (2003) In vivo model for cross-species porcine endogenous retrovirus transmission using tissue engineered pulmonary arteries. Eur J Cardiothorac Surg 24:358–63

    Article  PubMed  Google Scholar 

  84. Schmidt D, Mol A, Odermatt B et al (2006) Engineering of biologically active living heart valve leaflets using human umbilical cord-derived progenitor cells. Tissue Eng 12(11):3223–32

    Article  PubMed  CAS  Google Scholar 

  85. Schmidt D, Mol A, Breymann C et al (2006) Living autologous heart valves engineered from human prenatally harvested progenitors. Circulation 114(1 Suppl):I125–31

    PubMed  Google Scholar 

  86. Agrawal CM, Ray RB (2001) Biodegradable polymeric scaffolds for musculoskeletal tissue engineering. J Biomed Mater Res 55(2):141–50

    Article  PubMed  CAS  Google Scholar 

  87. Hutmacher DW, Goh JC, Teoh SH (2001) An introduction to biodegradable materials for tissue engineering applications. Ann Acad Med Singapore 30(2):183–91

    PubMed  CAS  Google Scholar 

  88. Hutmacher DW, Schantz T, Zein I et al (2001) Mechanical properties and cell cultural response of polycaprolactone scaffolds designed and fabricated via fused deposition modeling. J Biomed Mater Res 55(2):203–16

    Article  PubMed  CAS  Google Scholar 

  89. Kessler B, Witholt B (2001) Factors involved in the regulatory network of polyhydroxyalkanoate metabolism. J Biotechnol 86(2):97–104

    Article  PubMed  CAS  Google Scholar 

  90. Kidane AG, Burriesci G, Cornejo P et al (2009) Current developments and future prospects for heart valve replacement therapy. Biomed Mater Res B Appl Biomater 88(1):290–303

    Article  CAS  Google Scholar 

  91. Sodian R, Hoerstrup SP, Sperling JS et al (2000) Early in vivo experience with tissue-engineered trileaflet heart valves. Circulation 102:22–9

    Google Scholar 

  92. Sodian R, Hoerstrup SP, Sperling JS et al (2000) Evaluation of biodegradable, three-dimensional matrices for tissue engineering of heart valves. ASAIO J 46:107–10

    Article  PubMed  CAS  Google Scholar 

  93. Sodian R, Sperling JS, Martin DP et al (2000) Fabrication of a trileaflet heart valve scaffold from a polyhydroxyalkanoate biopolyester for use in tissue engineering. Tissue Eng 6:183–8

    Article  PubMed  CAS  Google Scholar 

  94. Schaefermeier PK, Szymanski D, Weiss F et al (2009) Design and fabrication of three-dimensional scaffolds for tissue engineering of human heart valves. Eur Surg Res 42(1):49–53

    Article  PubMed  CAS  Google Scholar 

  95. Sodian R, Loebe M, Hein A et al (2002) Application of stereolithography for scaffold fabrication for tissue engineered heart valves. ASAIO J 48:12–6

    Article  PubMed  Google Scholar 

  96. Hoerstrup SP, Sodian R, Daebritz S et al (2000) Functional living trileaflet heart valves grown in vitro. Circulation 102(19 Suppl 3):III44–9

    PubMed  CAS  Google Scholar 

  97. Rabkin E, Hoerstrup SP, Aikawa M et al (2002) Evolution of cell phenotype and extracellular matrix in tissue-engineered heart valves during in-vitro maturation and in-vivo remodeling. J Heart Valve Dis 11(3):308–14

    PubMed  Google Scholar 

  98. Stock UA, Nagashima M, Khalil PN (2000) Tissue-engineered valved conduits in the pulmonary circulation. J Thorac Cardiovasc Surg 119:732–40

    Article  PubMed  CAS  Google Scholar 

  99. Hoerstrup SP, Kadner A, Melnitchouk S et al (2002) Tissue engineering of functional trileaflet heart valves from human marrow stromal cells. Circulation 106(12 Suppl 1):I143–50

    PubMed  Google Scholar 

  100. Mol A, Rutten MC, Driessen NJ et al (2006) Autologous human tissue-engineered heart valves: prospects for systemic application. Circulation 114(1 Suppl):I152–8

    PubMed  Google Scholar 

  101. Grabow N, Schmohl K, Khosravi A et al (2004) Mechanical and structural properties of a novel hybrid heart valve scaffold for tissue engineering. Artif Organs 28(11):971–9

    Article  PubMed  CAS  Google Scholar 

  102. Stamm C, Khosravi A, Grabow N et al (2004) Biomatrix/polymer composite material for heart valve tissue engineering. Ann Thorac Surg 78:2084–92

    Article  PubMed  Google Scholar 

  103. Lutolf MP, Hubbell JA (2005) Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering. Nat Biotechnol 23(1):47–55

    Article  PubMed  CAS  Google Scholar 

  104. Tabata Y (2009) Biomaterial technology for tissue engineering applications. J R Soc Interface 6:311–24

    Article  CAS  Google Scholar 

  105. De Laporte L, Shea LD (2007) Matrices and scaffolds for DNA delivery in tissue engineering. Adv Drug Deliv Rev 59(4–5):292–307

    Article  PubMed  CAS  Google Scholar 

  106. Rothenburger M, Volker W, Vischer JP et al (2002) Tissue engineering of heart valves: formation of a three-dimensional tissue using porcine heart valve cells. ASAIO J 48(6):586–91

    Article  PubMed  CAS  Google Scholar 

  107. Rothenburger M, Völker W, Vischer P et al (2002) Ultrastructure of proteoglycans in tissue-engineered cardiovascular structures. Tissue Eng 8(6):1049–56

    Article  PubMed  CAS  Google Scholar 

  108. Butcher JT, Nerem RM (2004) Porcine aortic valve interstitial cells in three-dimensional culture: comparison of phenotype with aortic smooth muscle cells. J Heart Valve Dis 13(3):478–85; discussion 485–6

    PubMed  Google Scholar 

  109. Butcher JT, Nerem RM (2006) Valvular endothelial cells regulate the phenotype of interstitial cells in co-culture: effects of steady shear stress. Tissue Eng 12(4):905–15

    Article  PubMed  CAS  Google Scholar 

  110. Flanagan TC, Wilkins B, Black A et al (2006) A collagen-glycosaminoglycan co-culture model for heart valve tissue engineering applications. Biomaterials 27(10):2233–46

    Article  PubMed  CAS  Google Scholar 

  111. Taylor PM, Sachlos E, Dreger SA et al (2006) Interaction of human valve interstitial cells with collagen matrices manufactured using rapid prototyping. Biomaterials 27:2733–7

    Article  PubMed  CAS  Google Scholar 

  112. Tedder ME, Liao J, Weed B et al (2009) Stabilized collagen scaffolds for heart valve tissue engineering. Tissue Eng Part A 15:1257–68

    Article  PubMed  CAS  Google Scholar 

  113. Taylor PM, Allen SP, Dreger SA (2002) Human cardiac valve interstitial cells in collagen sponge: a biological three-dimensional matrix for tissue engineering. J Heart Valve Dis 11:298–306

    PubMed  Google Scholar 

  114. Rothenburger M, Vischer P, Völker W et al (2001) In vitro modelling of tissue using isolated vascular cells on a synthetic collagen matrix as a substitute for heart valves. Thorac Cardiovasc Surg 49(4):204–9

    Article  PubMed  CAS  Google Scholar 

  115. Shi Y, Ramamurthi A, Vesely I (2002) Towards tissue engineering of a composite aortic valve. Biomed Sci Instrum 38:35–40

    PubMed  CAS  Google Scholar 

  116. Mol A, van Lieshout MI, Dam-de Veen CG et al (2005) Fibrin as a cell carrier in cardiovascular tissue engineering applications. Biomaterials 26(16):3113–21

    Article  PubMed  CAS  Google Scholar 

  117. Ameer GA, Mahmood TA, Langer R (2002) A biodegradable composite scaffold for cell transplantation. J Orthop Res 20(1):16–9

    Article  PubMed  CAS  Google Scholar 

  118. Jockenhoevel S, Chalabi K, Sachweh JS et al (2001) Tissue engineering: complete autologous valve conduit – a new moulding technique. Thorac Cardiovasc Surg 49(5):287–90

    Article  PubMed  CAS  Google Scholar 

  119. Jockenhoevel S, Zund G, Hoerstrup SP et al (2001) Fibrin gel – advantages of a new scaffold in cardiovascular tissue engineering. Eur J Cardiothorac Surg 19(4):424–30

    Article  PubMed  CAS  Google Scholar 

  120. Ye Q, Zünd G, Benedikt P et al (2000) Fibrin gel as a three dimensional matrix in cardiovascular tissue engineering. Eur J Cardiothorac Surg 17:587–91

    Article  PubMed  CAS  Google Scholar 

  121. Schense JC, Hubbell JA (1999) Cross-linking exogenous bifunctional peptides into fibrin gels with factor XIIIa. Bioconjug Chem 10(1):75–81

    Article  PubMed  CAS  Google Scholar 

  122. Shin’oka T, Breuer CK, Tanel RE (1995) Tissue engineering heart valves: valve leaflet replacement study in a lamb model. Ann Thorac Surg 60(6):513–6

    Article  Google Scholar 

  123. Shin’oka T, Ma PX, Shum-Tim D et al (1996) Tissue-engineered heart valves. Autologous valve leaflet replacement study in a lamb model. Circulation 94:II164–8

    Google Scholar 

  124. Kim WG, Cho SK, Kang MC et al (2001) Tissue-engineered heart valve leaflets: an animal study. Int J Artif Organs 24(9):642–8

    PubMed  CAS  Google Scholar 

  125. Sutherland FW, Perry TE, Yu Y et al (2005) From stem cells to viable autologous semilunar heart valve. Circulation 111:2783–91

    Article  PubMed  Google Scholar 

  126. Hoerstrup SP, Cummings Mrcs I, Lachat M et al (2006) Functional growth in tissue-engineered living, vascular grafts: follow-up at 100 weeks in a large animal model. Circulation 114(1 Suppl):I159–66

    PubMed  Google Scholar 

  127. Matsumura G, Hibino N, Ikada Y et al (2003) Successful application of tissue engineered vascular autografts: clinical experience. Biomaterials 24(13):2303–8

    Article  PubMed  CAS  Google Scholar 

  128. Shin’oka T, Imai Y, Ikada Y (2001) Transplantation of a tissue-engineered pulmonary artery. N Engl J Med 344:532–3

    Article  PubMed  Google Scholar 

  129. Hoerstrup SP, Sodian R, Sperling JS et al (2000) New pulsatile bioreactor for in vitro formation of tissue engineered heart valves. Tissue Eng 6(1):75–9

    Article  PubMed  CAS  Google Scholar 

  130. Balguid A, Rubbens MP, Mol A et al (2007) The role of collagen cross-links in biomechanical behavior of human aortic heart valve leaflets – relevance for tissue engineering. Tissue Eng 13(7):1501–110

    Article  PubMed  CAS  Google Scholar 

  131. Huang SD, Liu XH, Bai CG et al (2007) Synergistic effect of fibronectin and hepatocyte growth factor on stable cell-matrix adhesion, re-endothelialization, and reconstitution in developing tissue-engineered heart valves. Heart Vessels 22(2):116–22

    Article  PubMed  Google Scholar 

  132. Rogers KA, Boughner D, Appleton CT et al (2009) Vascular smooth muscle cells as a valvular interstitial cell surrogate in heart valve tissue engineering. Tissue Eng Part A 15(12):3889–97

    Article  PubMed  Google Scholar 

  133. Stock UA, Vacanti JP, Mayer Jr JE (2002) Tissue engineering of heart valves – current aspects. Thorac Cardiovasc Surg 50:184–93

    Article  PubMed  CAS  Google Scholar 

  134. Isenberg BC, Tranquillo RT (2003) Long-term cyclic distention enhances the mechanical properties of collagen-based media-equivalents. Ann Biomed Eng 31(8):937–49

    Article  PubMed  Google Scholar 

  135. Mendelson K, Schoen FJ (2006) Heart valve tissue engineering: concepts, approaches, progress, and challenges. Ann Biomed Eng 34(12):1799–819

    Article  PubMed  Google Scholar 

  136. Mol A, Bouten CV, Zünd G et al (2003) The relevance of large strains in functional tissue engineering of heart valves. Thorac Cardiovasc Surg 51(2):78–83

    Article  PubMed  CAS  Google Scholar 

  137. Seliktar D, Nerem RM, Galis ZS et al (2003) Mechanical strain-stimulated remodeling of tissue-engineered blood vessel constructs. Tissue Eng 9(4):657–66

    Article  PubMed  CAS  Google Scholar 

  138. Hinz B, Gabbiani G (2003) Mechanisms of force generation and transmission by myofibroblasts. Curr Opin Biotechnol 14(5):538–46

    Article  PubMed  CAS  Google Scholar 

  139. Parizi M, Howard EW, Tomasek JJ (2000) Regulation of LPA-promoted myofibroblast contraction: role of Rho, myosin light chain kinase, and myosin light chain phosphatase. Exp Cell Res 254(2):210–20

    Article  PubMed  CAS  Google Scholar 

  140. Grenier G, Rémy-Zolghadri M, Larouche D et al (2005) Tissue reorganization in response to mechanical load increases functionality. Tissue Eng 11(1–2):90–100

    Article  PubMed  CAS  Google Scholar 

  141. Boerboom RA, Rubbens MP, Driessen NJ et al (2008) Effect of strain magnitude on the tissue properties of engineered cardiovascular constructs. Ann Biomed Eng 36(2):244–53

    Article  PubMed  Google Scholar 

  142. Rubbens MP, Mol A, van Marion MH et al (2009) Straining mode-dependent collagen remodeling in engineered cardiovascular tissue. Tissue Eng Part A 15(4):841–9

    Article  PubMed  CAS  Google Scholar 

  143. Rubbens MP, Mol A, Boerboom RA et al (2009) Intermittent straining accelerates the development of tissue properties in engineered heart valve tissue. Tissue Eng Part A 15(5):999–1008

    Article  PubMed  CAS  Google Scholar 

  144. Engelmayr GC Jr, Hildebrand DK, Sutherland FW et al (2003) A novel bioreactor for the dynamic flexural stimulation of tissue engineered heart valve biomaterials. Biomaterials 24(14):2523–32

    Article  PubMed  CAS  Google Scholar 

  145. Engelmayr GC Jr, Rabkin E, Sutherland FW et al (2005) The independent role of cyclic flexure in the early in vitro development of an engineered heart valve tissue. Biomaterials 26(2):175–87

    Article  PubMed  CAS  Google Scholar 

  146. Jockenhoevel S, Zund G, Hoerstrup SP et al (2002) Cardiovascular tissue engineering: a new laminar flow chamber for in vitro improvement of mechanical tissue properties. ASAIO J 48(1):8–11

    Article  PubMed  Google Scholar 

  147. Engelmayr GC Jr, Sales VL, Mayer JE Jr et al (2006) Cyclic flexure and laminar flow synergistically accelerate mesenchymal stem cell-mediated engineered tissue formation: implications for engineered heart valve tissues. Biomaterials 27(36):6083–95

    Article  PubMed  CAS  Google Scholar 

  148. Engelmayr GC Jr, Soletti L, Vigmostad SC et al (2008) A novel flex-stretch-flow bioreactor for the study of engineered heart valve tissue mechanobiology. Ann Biomed Eng 36(5):700–12

    Article  PubMed  Google Scholar 

  149. Balguid A, Mol A, van Vlimmeren MA et al (2009) Hypoxia induces near-native mechanical properties in engineered heart valve tissue. Circulation 119(2):290–7

    Article  PubMed  Google Scholar 

  150. Mertsching H, Hansmann J (2009) Bioreactor technology in cardiovascular tissue engineering. Adv Biochem 112:29–37

    CAS  Google Scholar 

  151. Stock UA, Wiederschain D, Kilroy SM et al (2001) Dynamics of extracellular matrix production and turnover in tissue engineered cardiovascular structures. J Cell Biochem 81:220–8

    Article  PubMed  CAS  Google Scholar 

  152. Sodian R, Lemke T, Loebe M et al (2001) New pulsatile bioreactor for fabrication of tissue-engineered patches. J Biomed Mater Res 58:401–5

    Article  PubMed  CAS  Google Scholar 

  153. Sodian R, Lemke T, Fritsche C et al (2002) Tissue-engineering bioreactors: a new combined cell-seeding and perfusion system for vascular tissue engineering. Tissue Eng 8:863–70

    Article  PubMed  CAS  Google Scholar 

  154. Narita Y, Hata K, Kagami H et al (2004) Novel pulse duplicating bioreactor system for tissue-engineered vascular construct. Tissue Eng 10(7–8):1224–33

    PubMed  CAS  Google Scholar 

  155. Williams C, Wick TM (2004) Perfusion bioreactor for small diameter tissue-engineered arteries. Tissue Eng 10:930–41

    Article  PubMed  CAS  Google Scholar 

  156. Mol A, Driessen NJ, Rutten MC et al (2005) Tissue engineering of human heart valve leaflets: a novel bioreactor for a strain-based conditioning approach. Ann Biomed Eng 33(12):1778–88

    Article  PubMed  Google Scholar 

  157. Niklason LE, Gao J, Abbott WM et al (1999) Functional arteries grown in vitro. Science 284(5413):489–93

    Article  PubMed  CAS  Google Scholar 

  158. Stegemann JP, Nerem RM (2003) Phenotype modulation in vascular tissue engineering using biochemical and mechanical stimulation. Ann Biomed Eng 31:391–402

    Article  PubMed  Google Scholar 

  159. Syedain ZH, Tranquillo RT (2009) Controlled cyclic stretch bioreactor for tissue-engineered heart valves. Biomaterials 30(25):4078–84

    Article  PubMed  CAS  Google Scholar 

  160. Lee DJ, Steen J, Jordan JE et al (2009) Endothelialization of heart valve matrix using a computer-assisted pulsatile bioreactor. Tissue Eng Part A 15(4):807–14

    Article  PubMed  CAS  Google Scholar 

  161. Schmidt D, Achermann J, Odermatt B (2008) Cryopreserved amniotic fluid-derived cells: a lifelong autologous fetal stem cell source for heart valve tissue engineering. J Heart Valve Dis 17(4):446–55

    PubMed  Google Scholar 

  162. Sodian R, Lueders C, Kraemer L et al (2006) Tissue engineering of autologous human heart valves using cryopreserved vascular umbilical cord cells. Ann Thorac Surg 81(6):2207–16

    Article  PubMed  Google Scholar 

  163. Hildebrand DK, Wu ZJ, Mayer JE Jr et al (2004) Design and hydrodynamic evaluation of a novel pulsatile bioreactor for biologically active heart valves. Ann Biomed Eng 32(8):1039–49

    Article  PubMed  Google Scholar 

  164. Kortsmit J, Driessen NJ, Rutten MC et al (2009) Nondestructive and noninvasive assessment of mechanical properties in heart valve tissue engineering. Tissue Eng Part A 15(4):797–806

    Article  PubMed  CAS  Google Scholar 

  165. Kortsmit J, Driessen NJ, Rutten MC et al (2009) Real time, non-invasive assessment of leaflet deformation in heart valve tissue engineering. Ann Biomed Eng 37(3):532–41

    Article  PubMed  CAS  Google Scholar 

  166. Vesely I (2005) Heart valve tissue engineering. Circ Res 97:743–55

    Article  PubMed  CAS  Google Scholar 

  167. Sievers HH (2007) In vivo tissue engineering an autologous semilunar biovalve: can we get what we want? J Thorac Cardiovasc Surg 134:20–2

    Article  PubMed  Google Scholar 

  168. Schleicher M, Wendel HP, Fritze O et al (2009) In vivo tissue engineering of heart valves: evolution of a novel concept. Regen Med 4(4):613–9

    Article  PubMed  CAS  Google Scholar 

  169. Dohmen PM, da Costa F, Holinski S et al (2006) Is there a possibility for a glutaraldehyde-free porcine heart valve to grow? Eur Surg Res 38(1):54–61

    Article  PubMed  CAS  Google Scholar 

  170. Elkins RC, Dawson PE, Goldstein S et al (2001) Decellularized human valve allografts. Ann Thorac Surg 71(5 Suppl):S428–32

    Article  PubMed  CAS  Google Scholar 

  171. Elkins RC, Goldstein S, Hewitt CW et al (2001) Recellularization of heart valve grafts by a process of adaptive remodeling. Semin Thorac Cardiovasc Surg 13(4 Suppl 1):87–92

    PubMed  CAS  Google Scholar 

  172. Erdbrügger W, Konertz W, Dohmen PM et al (2006) Decellularized xenogenic heart valves reveal remodeling and growth potential in vivo. Tissue Eng 12(8):2059–68

    Article  PubMed  Google Scholar 

  173. Goldstein S, Clarke DR, Walsh SP et al (2000) Transpecies heart valve transplant: advanced studies of a bioengineered xeno-autograft. Ann Thorac Surg 70(6):1962–9

    Article  PubMed  CAS  Google Scholar 

  174. Iwai S, Torikai K, Coppin CM et al (2007) Minimally immunogenic decellularized porcine valve provides in situ recellularization as a stentless bioprosthetic valve. J Artif Organs 10(1):29–35

    Article  PubMed  Google Scholar 

  175. Kim WG, Huh JH (2004) Time related histopathologic changes of acellularized xenogenic pulmonary valved conduits. ASAIO J 50(6):601–5

    Article  PubMed  Google Scholar 

  176. Leyh RG, Wilhelmi M, Walles T et al (2003) Acellularized porcine heart valve scaffolds for heart valve tissue engineering and the risk of cross-species transmission of porcine endogenous retrovirus. J Thorac Cardiovasc Surg 126(4):1000–4

    Article  PubMed  CAS  Google Scholar 

  177. Takagi K, Fukunaga S, Nishi A et al (2006) In vivo recellularization of plain decellularized xenografts with specific cell characterization in the systemic circulation: histological and immunohistochemical study. Artif Organs 30:233–41

    Article  PubMed  CAS  Google Scholar 

  178. Dohmen PM, Konertz W (2005) Results with decellularized xenografts. Circ Res 97(8):743–55

    Article  CAS  Google Scholar 

  179. Dohmen PM, Hauptmann S, Terytze A et al (2007) In-vivo repopularization of a tissue-engineered heart valve in a human subject. J Heart Valve Dis 16(4):447–9

    PubMed  Google Scholar 

  180. Simon P, Kasimir MT, Seebacher G (2003) Early failure of the tissue engineered porcine heart valve SYNERGRAFT in pediatric patients. Eur J Cardiothorac Surg 23:1002–6

    Article  PubMed  CAS  Google Scholar 

  181. Kasimir MT, Rieder E, Seebacher G et al (2006) Decellularization does not eliminate thrombogenicity and inflammatory stimulation in tissue-engineered porcine heart valves. J Heart Valve Dis 15(2):278–86

    PubMed  Google Scholar 

  182. Rieder E, Nigisch A, Dekan B et al (2006) Granulocyte-based immune response against decellularized or glutaraldehyde cross-linked vascular tissue. Biomaterials 27(33):5634–42

    Article  PubMed  CAS  Google Scholar 

  183. Bastian F, Stelzmüller ME, Kratochwill K et al (2008) IgG deposition and activation of the classical complement pathway involvement in the activation of human granulocytes by decellularized porcine heart valve tissue. Biomaterials 29(12):1824–32

    Article  PubMed  CAS  Google Scholar 

  184. Lichtenberg A, Cebotari S, Tudorache I et al (2006) Flow-dependent re-endothelialization of tissue-engineered heart valves. J Heart Valve Dis 15(2):287–93; discussion 293–4

    PubMed  Google Scholar 

  185. Lichtenberg A, Tudorache I, Cebotari S et al (2006) In vitro re-endothelialization of detergent decellularized heart valves under simulated physiological dynamic conditions. Biomaterials 27(23):4221–9

    Article  PubMed  CAS  Google Scholar 

  186. Stamm C, Steinhoff G (2006) When less is more: go slowly when repopulating a decellularized valve in vivo! J Thorac Cardiovasc Surg 131:843–52

    Article  CAS  Google Scholar 

  187. Stamm C, Kleine HD, Choi YH et al (2007) Intramyocardial delivery of CD133+ bone marrow cells and coronary artery bypass grafting for chronic ischemic heart disease: safety and efficacy studies. J Thorac Cardiovasc Surg 133:717–25

    Article  PubMed  Google Scholar 

  188. Rieder E, Seebacher G, Kasimir MT et al (2005) Tissue engineering of heart valves: decellularized porcine and human valve scaffolds differ importantly in residual potential to attract monocytic cells. Circulation 111(21):2712–4

    Article  Google Scholar 

  189. Sayk F, Bos I, Schubert U et al (2005) Histopathologic findings in a novel decellularized pulmonary homograft: an autopsy study. Ann Thorac Surg 79(5):1755–8

    Article  PubMed  Google Scholar 

  190. Miller DV, Edwards WD, Zehr KJ (2006) Endothelial and smooth muscle cell populations in a decellularized cryopreserved aortic homograft (SynerGraft) 2 years after implantation.J Thorac Cardiovasc Surg 132(1):175–6

    Article  PubMed  Google Scholar 

  191. Zehr KJ, Yagubyan M, Connolly HM et al (2005) Aortic root replacement with a novel decellularized cryopreserved aortic homograft: postoperative immunoreactivity and early results. J Thorac Cardiovasc Surg 130(4):1010–5

    Article  PubMed  Google Scholar 

  192. Bechtel JF, Müller-Steinhardt M, Schmidtke C et al (2003) Evaluation of the decellularized pulmonary valve homograft (SynerGraft). J Heart Valve Dis 12(6):734–9

    PubMed  Google Scholar 

  193. Bechtel JF, Stierle U, Sievers HH (2008) Fifty-two months’ mean follow up of decellularized SynerGraft-treated pulmonary valve allografts. J Heart Valve Dis 17(1):98–104

    PubMed  Google Scholar 

  194. Shin’oka T, Shum-Tim D, Ma PX et al (1998) Creation of viable pulmonary artery autografts through tissue engineering. J Thorac Cardiovasc Surg 115(3):536–45

    Article  Google Scholar 

  195. Iwai S, Sawa Y, Ichikawa H et al (2004) Biodegradable polymer with collagen microsponge serves as a new bioengineered cardiovascular prosthesis. J Thorac Cardiovasc Surg 128(3):472–9

    Article  PubMed  CAS  Google Scholar 

  196. Iwai S, Sawa Y, Taketani S et al (2005) Novel tissue-engineered biodegradable material for re-construction of vascular wall. Ann Thorac Surg 80(5):1828

    Article  Google Scholar 

  197. Torikai K, Ichikawa H, Hirakawa K et al (2008) A self-renewing, tissue-engineered vascular graft for arterial reconstruction. J Thorac Cardiovasc Surg 136:37–45

    Article  PubMed  Google Scholar 

  198. Yokota T, Ichikawa H, Matsumiya G et al (2008) In situ tissue regeneration using a novel tissue-engineered, small-caliber vascular graft without cell seeding. J Thorac Cardiovasc Surg 2008 136:900–7

    Article  PubMed  Google Scholar 

  199. Brennan MP, Dardik A, Hibino N et al (2008) Tissue-engineered vascular grafts demonstrate evidence of growth and development when implanted in a juvenile animal model. Ann Surg 248(3):370–7

    PubMed  Google Scholar 

  200. Hibino N, Shin’oka T, Matsumura G et al (2005) The tissue-engineered vascular graft using bone marrow without culture. J Thorac Cardiovasc Surg 129(5):1064–70

    Article  PubMed  Google Scholar 

  201. Matsumura G, Miyagawa-Tomita S, Shin’oka T et al (2003) First evidence that bone marrow cells contribute to the construction of tissue-engineered vascular autografts in vivo. Circulation 108(14):1729–34

    Article  PubMed  Google Scholar 

  202. Matsumura G, Ishihara Y, Miyagawa-Tomita S et al (2006) Evaluation of tissue-engineered vascular autografts. Tissue Eng 12(11):3075–83

    Article  PubMed  CAS  Google Scholar 

  203. Shin’oka T, Matsumura G, Hibino N et al (2005) Midterm clinical result of tissue-engineered vascular autografts seeded with autologous bone marrow cells. J Thorac Cardiovasc Surg 129(6):1330–8

    Article  PubMed  Google Scholar 

  204. De Visscher G, Vranken I, Lebacq A et al (2007) In vivo cellularization of a cross-linked matrix by intraperitoneal implantation: a new tool in heart valve tissue engineering. Eur Heart J 28(11):1389–96

    Article  PubMed  Google Scholar 

  205. De Visscher G, Blockx H, Meuris B et al (2008) Functional and biomechanical evaluation of a completely recellularized stentless pulmonary bioprosthesis in sheep. J Thorac Cardiovasc Surg 135(2):395–404

    Article  PubMed  Google Scholar 

  206. Hayashida K, Kanda K, Yaku H et al (2007) Development of an in vivo tissue-engineered, autologous heart valve (the biovalve): preparation of a prototype model. J Thorac Cardiovasc Surg 134(1):152–9

    Article  PubMed  Google Scholar 

  207. Nakayama Y, Yamanami M, Yahata Y et al (2009) Preparation of a completely autologous trileaflet valve-shaped construct by in-body tissue architecture technology. J Biomed Mater Res B Appl Biomater 91(2):813–8

    PubMed  Google Scholar 

  208. Vranken I, De Visscher G, Lebacq A et al (2008) The recruitment of primitive Lin(−) Sca-1(+), CD34(+), c-kit(+) and CD271(+) cells during the early intraperitoneal foreign body reaction. Biomaterials 29:797–808

    Article  PubMed  CAS  Google Scholar 

  209. Ruiz CE, Iemura M, Medie S et al (2005) Transcatheter placement of a low-profile biodegradable pulmonary valve made of small intestinal submucosa: a long-term study in a swine model. J Thorac Cardiovasc Surg 130(2):477–84

    Article  PubMed  Google Scholar 

  210. Stock UA, Schenke-Layland K (2006) Performance of decellularized xenogeneic tissue in heart valve replacement. Biomaterials 27:1–2

    Article  PubMed  CAS  Google Scholar 

  211. Schaefermeier PK, Cabeza N, Besser JC et al (2009) Potential cell sources for tissue engineering of heart valves in comparison with human pulmonary valve cells. ASAIO J 55(1):86–92

    Article  PubMed  CAS  Google Scholar 

  212. Schnell AM, Hoerstrup SP, Zund G et al (2001) Optimal cell source for cardiovascular tissue engineering: venous vs. aortic human myofibroblasts. Thorac Cardiovasc Surg 49(4):221–5

    Article  PubMed  CAS  Google Scholar 

  213. Shin’oka T, Shum-Tim D, Ma PX (1997) Tissue-engineered heart valve leaflets: does cell origin affect outcome? Circulation 96:II102–7

    Google Scholar 

  214. Zund G, Hoerstrup SP, Schoeberlein A et al (1998) Tissue engineering: a new approach in cardiovascular surgery: seeding of human fibroblasts followed by human endothelial cells on resorbable mesh. Eur J Cardiothorac Surg 13:160–4

    Article  PubMed  CAS  Google Scholar 

  215. Mol A, Hoerstrup SP (2004) Heart valve tissue engineering – where do we stand? IntJ Cardiol 95(1 Suppl):S57–8

    Article  PubMed  Google Scholar 

  216. Hoerstrup SP, Zund G, Schoeberlein A et al (1998) Fluorescence activated cell sorting: a reliable method in tissue engineering of a bioprosthetic heart valve. Ann Thorac Surg 66(5):1653–7

    Article  PubMed  CAS  Google Scholar 

  217. Schmidt D, Hoerstrup SP (2007) Tissue engineered heart valves based on human cells. Swiss Med Wkly 155:80–5

    Google Scholar 

  218. Ugurlucan M, Yerebakan C, Furlani D et al (2009) Cell sources for cardiovascular tissue regeneration and engineering. Thorac Cardiovasc Surg 57:63–73

    Article  PubMed  CAS  Google Scholar 

  219. Breuer CK, Shin’oka T, Tanel RE et al (1996) Tissue engineering lamb heart valve leaflets. Biotechnol Bioeng 50(5):562–7

    Article  PubMed  CAS  Google Scholar 

  220. Shin’oka T (2002) Tissue engineered heart valves: autologous cell seeding on biodegradable polymer scaffold. Artif Organs 26:402–6

    Article  Google Scholar 

  221. Kadner A, Zund G, Maurus C et al (2004) Human umbilical cord cells for cardiovascular tissue engineering: a comparative study. Eur J Cardiothorac Surg 25(4):635–41

    Article  PubMed  Google Scholar 

  222. Shum-Tim D, Stock U, Hrkach J (1999) Tissue engineering of autologous aorta using a new biodegradable polymer. Ann Thorac Surg 68:2298–304

    Article  PubMed  CAS  Google Scholar 

  223. De Vriese AS, Verbeuren TJ, Van de Voorde J et al (2000) Endothelial dysfunction in diabetes. Br J Pharmacol 130(5):963–74

    Article  PubMed  Google Scholar 

  224. Bonetti PO, Lerman LO, Lerman A (2003) Endothelial dysfunction: a marker of atherosclerotic risk. Arterioscler Thromb Vasc Biol 23(2):168–75

    Article  PubMed  CAS  Google Scholar 

  225. Kadner A, Hoerstrup SP, Zund G et al (2002) A new source for cardiovascular tissue engineering: human bone marrow stromal cells. Eur J Cardiothorac Surg 21(6):1055–60

    Article  PubMed  Google Scholar 

  226. Perry TE, Kaushal S, Sutherland FW et al (2003) Thoracic Surgery Directors Association Award. Bone marrow as a cell source for tissue engineering heart valves. Ann Thorac Surg 75(3):761–7

    Article  PubMed  Google Scholar 

  227. Prockop DJ (1997) Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 276(5309):71–4

    Article  PubMed  CAS  Google Scholar 

  228. Orlic D, Kajstura J, Chimenti S et al (2001) Bone marrow cells regenerate infarcted myocardium. Nature 410(6829):701–5

    Article  PubMed  CAS  Google Scholar 

  229. Sata M, Saiura A, Kunisato A et al (2002) Hematopoietic stem cells differentiate into vascular cells that participate in the pathogenesis of atherosclerosis. Nat Med 8(4):403–9

    Article  PubMed  CAS  Google Scholar 

  230. Taylor PM, Allen SP, Yacoub MH (2000) Phenotypic and functional characterization of interstitial cells from human heart valves, pericardium and skin. J Heart Valve Dis 9:150–8

    PubMed  CAS  Google Scholar 

  231. Oswald J, Boxberger S, Jorgensen B et al (2004) Mesenchymal stem cells can be differentiated into endothelial cells in vitro. Stem Cells 22(3):377–84

    Article  PubMed  Google Scholar 

  232. Huang CY, Hagar KL, Frost LE et al (2004) Effects of cyclic compressive loading on chondrogenesis of rabbit bone-marrow derived mesenchymal stem cells. Stem Cells 22(3):313–23

    Article  PubMed  CAS  Google Scholar 

  233. Liechty KW, MacKenzie TC, Shaaban AF et al (2000) Human mesenchymal stem cells engraft and demonstrate site-specific differentiation after in utero transplantation in sheep. Nat Med 6(11):1282–6

    Article  PubMed  CAS  Google Scholar 

  234. Xin Y, Wang YM, Zhang H et al (2009) Aging adversely impacts biological properties of human bone marrow-derived mesenchymal stem cells: implications for tissue engineering heart valve construction. Artif Organs 34(3):215–22

    Article  PubMed  Google Scholar 

  235. Tanaka KA, Key NS, Levy JH (2009) Blood coagulation: hemostasis and thrombin regulation. Anesth Analg 108:1433–46

    Article  PubMed  CAS  Google Scholar 

  236. El-Hamamsy I, Balachandran K, Yacoub MH et al (2009) Endothelium-dependent regulation of the mechanical properties of aortic valve cusps. J Am Coll Cardiol 53(16):1448–55

    Article  PubMed  CAS  Google Scholar 

  237. Kasimir MT, Weigel G, Sharma J et al (2005) The decellularized porcine heart valve matrix in tissue engineering: platelet adhesion and activation. Thromb Haemost 94(3):469–70

    Google Scholar 

  238. Alsberg E, von Recum HA, Mahoney MJ (2006) Environmental cues to guide stem cell fate decision for tissue engineering applications. Expert Opin Biol Ther 6:847–66

    Article  PubMed  CAS  Google Scholar 

  239. Aird WC (2007) Phenotypic heterogeneity of the endothelium: II. Representative vascular beds. Circ Res 100(2):174–90

    Article  PubMed  CAS  Google Scholar 

  240. Asahara T, Murohara T, Sullivan A et al (1997) Isolation of putative progenitor endothelial cells for angiogenesis. Science 275(5302):964–7

    Article  PubMed  CAS  Google Scholar 

  241. Kim S, von Recum HA (2008) Endothelial stem cells and precursors for tissue engineering: cell source, differentiation, selection, and application. Tissue Eng Part B Rev 14(1):133–47

    Article  PubMed  CAS  Google Scholar 

  242. Kim S, von Recum HA (2009) Endothelial progenitor populations in differentiating embryonic stem cells I: identification and differentiation kinetics. Tissue Eng Part A 15(12):3709–18

    Article  PubMed  CAS  Google Scholar 

  243. Urbich C, Dimmeler S (2004) Endothelial progenitor cells: characterization and role in vascular biology. Circ Res 95(4):343–53

    Article  PubMed  CAS  Google Scholar 

  244. Urbich C, Dimmeler S (2004) Endothelial progenitor cells functional characterization. Trends Cardiovasc Med 14:318–22

    Article  PubMed  CAS  Google Scholar 

  245. Kawamoto A, Losordo DW (2008) Endothelial progenitor cells for cardiovascular regeneration. Trends Cardiovasc Med 18(1):33–7

    Article  PubMed  CAS  Google Scholar 

  246. Hofmann M, Wollert KC, Meyer GP et al (2005) Monitoring of bone marrow cell homing into the infarcted human myocardium. Circulation 111:2198–202

    Article  PubMed  Google Scholar 

  247. Iwasaki H, Kawamoto A, Ishikawa M et al (2006) Dose-dependent contribution of CD34-positive cell transplantation to concurrent vasculogenesis and cardiomyogenesis for functional regenerative recovery after myocardial infarction. Circulation 113:1311–25

    Article  PubMed  CAS  Google Scholar 

  248. Kocher AA, Schuster MD, Szabolcs MJ et al (2001) Neovascularization of ischemic myocardium by human bone marrow-derived angioblasts prevents cardiomyocyte apoptosis, reduces remodeling and improves cardiac function. Nat Med 7:430–6

    Article  PubMed  CAS  Google Scholar 

  249. Martin-Rendon E, Brunskill S, Dorée C et al (2008) Stem cell treatment for acute myocardial infarction. Cochrane Database Syst Rev 8(4):CD006536

    Google Scholar 

  250. Pearson JD (2009) Endothelial progenitor cells – hype or hope? J Thromb Haemost 7(2):255–62

    Article  PubMed  CAS  Google Scholar 

  251. Shirota T, He H, Yasui H (2003) Human endothelial progenitor cell-seeded hybrid graft: proliferative and antithrombogenic potentials in vitro and fabrication processing. Tissue Eng 9:127–36

    Article  PubMed  CAS  Google Scholar 

  252. Kaushal S, Amiel GE, Guleserian KJ et al (2001) Functional small-diameter neovessels created using endothelial progenitor cells expanded ex vivo. Nat Med 7(9):1035–40

    Article  PubMed  CAS  Google Scholar 

  253. Shirota T, Yasui H, Shimokawa H et al (2003) Fabrication of endothelial progenitor cell (EPC)-seeded intravascular stent devices and in vitro endothelialization on hybrid vascular tissue. Biomaterials 24:2295–302

    Article  PubMed  CAS  Google Scholar 

  254. Schmidt D, Breymann C, Weber A et al (2004) Umbilical cord blood derived endothelial progenitor cells for tissue engineering of vascular grafts. Ann Thorac Surg 78(6):2094–8

    Article  PubMed  Google Scholar 

  255. Schmidt D, Mol A, Neuenschwander S et al (2005) Living patches engineered from human umbilical cord derived fibroblasts and endothelial progenitor cells. Eur J Cardiothorac Surg 27(5):795–800

    Article  PubMed  Google Scholar 

  256. Schmidt D, Asmis LM, Odermatt B (2006) Engineered living blood vessels: functional endothelia generated from human umbilical cord-derived progenitors. Ann Thorac Surg 82(4):1465–71

    Article  PubMed  Google Scholar 

  257. Fang NT, Xie SZ, Wang SM et al (2007) Construction of tissue-engineered heart valves by using decellularized scaffolds and endothelial progenitor cells. Chin Med J (Engl) 120(8):696–702

    CAS  Google Scholar 

  258. Dvorin EL, Wylie-Sears J, Kaushal S et al (2003) Quantitative evaluation of endothelial progenitors and cardiac valve endothelial cells: proliferation and differentiation on poly-glycolic acid/poly-4-hydroxybutyrate scaffold in response to vascular endothelial growth factor and transforming growth factor beta1. Tissue Eng 9(3):487–93

    Article  PubMed  CAS  Google Scholar 

  259. Sales VL, Engelmayr GC Jr, Mettler BA et al (2006) Transforming growth factor-beta1 modulates extracellular matrix production, proliferation, and apoptosis of endothelial progenitor cells in tissue-engineering scaffolds. Circulation 114(1 Suppl):I193–9

    PubMed  Google Scholar 

  260. Ferguson VL, Dodson RB (2009) Bioengineering aspects of the umbilical cord. Eur J Obstet Gynecol Reprod Biol 144(1):108–13

    Article  Google Scholar 

  261. Wang HS, Hung SC, Peng ST et al (2004) Mesenchymal stem cells in Wharton’s Jelly of the human umbilical cord. Stem Cells 22:1330–37

    Article  PubMed  Google Scholar 

  262. Kadner A, Hoerstrup SP, Tracy J et al (2002) Human umbilical cord cells: a new cell source for cardiovascular tissue engineering. Ann Thorac Surg 74(4):S1422–8

    Article  PubMed  Google Scholar 

  263. Kobayashi K, Kubota T, Aso T (1998) Study on myofibroblast differentiation in the stromal cells of Wharton’s jelly: expression and localization of alpha-smooth muscle actin. Early Hum Dev 51:223–33

    Article  PubMed  CAS  Google Scholar 

  264. Kogler G, Sensken S, Airey JA et al (2004) A new human somatic stem cell from placental cord blood with intrinsic pluripotent differentiation potential. J Exp Med 200:123–35

    Article  PubMed  Google Scholar 

  265. Lee OK, Kuo TK, Chen WM et al (2004) Isolation of multipotent mesenchymal stem cells from umbilical cord blood. Blood 103:1669–75

    Article  PubMed  CAS  Google Scholar 

  266. Sarugaser R, Lickorish D, Baksh D et al (2005) Human umbilical cord perivascular (HUCPV) cells: a source of mesenchymal progenitors. Stem Cells 23(2):220–9

    Article  PubMed  Google Scholar 

  267. Weiss ML, Medicetty S, Bledsoe AR et al (2006) Human umbilical cord matrix stem cells: preliminary characterization and effect of transplantation in a rodent model of Parkinson’s disease. Stem Cells 24:781–92

    Article  PubMed  CAS  Google Scholar 

  268. Weiss ML, Anderson C, Medicetty S et al (2008) Immune properties of human umbilical cord Wharton’s jelly-derived cells. Stem Cells 26:2865–74

    Article  PubMed  CAS  Google Scholar 

  269. Sipehia R, Martucci G, Lipscombe J (1996) Transplantation of human endothelial cell monolayer on artificial vascular prosthesis: the effect of growth-support surface chemistry, cell seeding density, ECM protein coating, and growth factors. Artif Cells Blood Substit Immobil Biotechnol 24:51–63

    Article  PubMed  CAS  Google Scholar 

  270. Hoerstrup SP, Kadner A, Breymann CI et al (2002) Living, autologous pulmonary artery conduits tissue engineered from human umbilical cord cells. Ann Thorac Surg 74:46–52

    Article  PubMed  Google Scholar 

  271. Koike N, Fukumura D, Gralla O et al (2004) Tissue engineering: creation of long-lasting blood vessels. Nature 428(6979):138–9

    Article  PubMed  CAS  Google Scholar 

  272. Breymann C, Schmidt D, Hoerstrup SP (2006) Umbilical cord cells as a source of cardiovascular tissue engineering. Stem Cell Rev 2(2):87–92

    Article  PubMed  Google Scholar 

  273. Armson BA, Maternal/Fetal Medicine Committee, Society of Obstetricians and Gynaecologists of Canada (2005) Umbilical cord blood banking: implications for perinatal care providers. J Obstet Gynaecol Can 27(3):263–90

    PubMed  Google Scholar 

  274. Ruhil S, Kumar V, Rathee P (2009) Umbilical cord stem cell: an overview. Curr Pharm Biotechnol 10(3):327–34

    Article  PubMed  CAS  Google Scholar 

  275. Pappa KI, Anagnou NP (2009) Novel sources of fetal stem cells: where do they fit on the developmental continuum? Regen Med 4(3):423–33

    Article  PubMed  Google Scholar 

  276. Zhang X, Mitsuru A, Igura K et al (2006) Mesenchymal progenitor cells derived from chorionic villi of human placenta for cartilage tissue engineering. Biochem Biophys Res Commun 340:944–52

    Article  PubMed  CAS  Google Scholar 

  277. Miki T, Strom SC (2006) Amnion-derived pluripotent/multipotent stem cells. Stem Cell Rev 2(2):133–42

    Article  PubMed  CAS  Google Scholar 

  278. Toda A, Okabe M, Yoshida T, Nikaido T (2007) The potential of amniotic membrane/amnion-derived cells for regeneration of various tissues. J Pharmacol Sci 105(3):215–28

    Article  PubMed  CAS  Google Scholar 

  279. Parolini O, Soncini M, Evangelista M et al (2009) Amniotic membrane and amniotic fluid-derived cells: potential tools for regenerative medicine? Regen Med 4(2):275–91

    Article  PubMed  CAS  Google Scholar 

  280. Kaviani A, Guleserian K, Perry TE et al (2003) Fetal tissue engineering from amniotic fluid. J Am Coll Surg 196(4):592–7

    Article  PubMed  Google Scholar 

  281. Kunisaki SM, Armant M, Kao GS et al (2007) Tissue engineering from human mesenchymal amniocytes: a prelude to clinical trials. J Pediatr Surg 42(6):974–9; discussion 979–80

    Article  PubMed  Google Scholar 

  282. Pansky A, Roitzheim B, Tobiasch E (2007) Differentiation potential of adult human mesenchymal stem cells. Clin Lab 53(1–2):81–4

    PubMed  CAS  Google Scholar 

  283. Tuan RS, Boland G, Tuli R (2003) Adult mesenchymal stem cells and cell-based tissue engineering. Arthritis Res Ther 5:32–45

    Article  PubMed  CAS  Google Scholar 

  284. Zuk PA, Zhu M, Mizuno H et al (2001) Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 7:211–28

    Article  PubMed  CAS  Google Scholar 

  285. Cao Y, Sun Z, Liao L et al (2005) Human adipose tissue-derived stem cells differentiate into endothelial cells in vitro and improve postnatal neovascularization in vivo. Biochem Biophys Res Commun 332(2):370–9

    Article  PubMed  CAS  Google Scholar 

  286. Miranville A, Heeschen C, Sengenès C et al (2004) Improvement of postnatal neovascularization by human adipose tissue-derived stem cells. Circulation 110(3):349–55

    Article  PubMed  CAS  Google Scholar 

  287. Planat-Benard V, Silvestre JS, Cousin B et al (2004) Plasticity of human adipose lineage cells toward endothelial cells: physiological and therapeutic perspectives. Circulation 109(5):656–63

    Article  PubMed  Google Scholar 

  288. Colazzo F, Sarathchandra P, Chester AH et al (2009) An evaluation of adipose-derived stem cells for heart valve tissue engineering. Paper presented at the 5th biennial meeting of the Society of Heart Valve Disease, Berlin, 28–30 June 2009

    Google Scholar 

  289. DiMuzio P, Tulenko T (2007) Tissue engineering applications to vascular bypass graft development: the use of adipose-derived stem cells. J Vasc Surg 45(Suppl A):A99–103

    Article  PubMed  Google Scholar 

  290. Okita K, Ichisaka T, Yamanaka S (2007) Generation of germline-competent induced pluripotent stem cells. Nature 448(7151):313–7

    Article  PubMed  CAS  Google Scholar 

  291. Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126(4):663–76

    Article  PubMed  CAS  Google Scholar 

  292. Wernig M, Meissner A, Foreman R (2007) In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state. Nature 448:318–24

    Article  PubMed  CAS  Google Scholar 

  293. Mauritz C, Schwanke K, Reppel M et al (2008) Generation of functional murine cardiac myocytes from induced pluripotent stem cells. Circulation 118(5):507–17

    Article  PubMed  Google Scholar 

  294. Zhang J, Wilson GF, Soerens AG (2009) Functional cardiomyocytes derived from human induced pluripotent stem cells. Circ Res 104:e30–41

    Article  PubMed  CAS  Google Scholar 

  295. Guan K, Nayernia K, Maier LS et al (2006) Pluripotency of spermatogonial stem cells from adult mouse testis. Nature 440(7088):1199–203

    Article  PubMed  CAS  Google Scholar 

  296. Seandel M, James D, Shmelkov SV et al (2007) Generation of functional multipotent adult stem cells from GPR125+ germline progenitors. Nature 449(7160):346–50

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Swiss Center for Regenerative Medicine, Department of Surgical Research and Center for Clinical Research, University of Hospital of Zurich, Zurich, Switzerland

    Simon P. Hoerstrup

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  1. Benedikt Weber
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  2. Simon P. Hoerstrup
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Correspondence to Simon P. Hoerstrup .

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  1. Health Sciences Center, Dept. Physiology & Biophysics, Stony Brook University, Stony Brook, 11794-8661, New York, USA

    Ira S. Cohen

  2. Worcester Polytechnic Institute, Institute Rd. 100, Worcester, 01609-2280, Massachusetts, USA

    Glenn R. Gaudette

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Weber, B., Hoerstrup, S.P. (2011). Regenerating Heart Valves. In: Cohen, I., Gaudette, G. (eds) Regenerating the Heart. Stem Cell Biology and Regenerative Medicine. Humana Press. https://doi.org/10.1007/978-1-61779-021-8_22

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