Abstract
Syndecan-3 is a transmembrane proteoglycan, the largest of the four syndecan family members and the most mysterious. To date, the number of published studies involving syndecan-3 is only a small fraction of the number of studies involving the other subfamily member syndecan-1, yet, these few studies on syndecan-3 cover a whole range of biological functions and phenotypes suggesting that syndecan-3 might be the most eclectic and intereting of the four syndecans. In this review, we focus on what is currently known about the role of syndecan-3 in the musculoskeletal system, from development to aging, including regeneration and disease. We also briefly refer to known syndecan-3 functions in other tissues and systems in an attempt to summarize the most up-to-date knowledge while also instilling curiosity about this extraordinary biomolecule and, hopefully, inspiring more research into its biochemistry and biological functions.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Alini M, Roughley PJ (2001) Changes in leucine-rich repeat proteoglycans during maturation of the bovine growth plate. Matrix Biol 19:805–813
Asundi VK, Carey DJ (1995) Self-association of N-syndecan (syndecan-3) core protein is mediated by a novel structural motif in the transmembrane domain and ectodomain flanking region. J Biol Chem 270:26404–26410
Asundi VK, Carey DJ (1997) Phosphorylation of recombinant N-syndecan (syndecan 3) core protein. Biochem Biophys Res Commun 240:502–506
Asundi VK, Erdman R, Stahl RC, Carey DJ (2003) Matrix metalloproteinase-dependent shedding of syndecan-3, a transmembrane heparan sulfate proteoglycan, in Schwann cells. J Neurosci Res 73:593–602
Baietti MF, Zhang Z, Mortier E, Melchior A, Degeest G, Geeraerts A, Ivarsson Y, Depoortere F, Coomans C, Vermeiren E, Zimmermann P, David G (2012) Syndecan-syntenin-ALIX regulates the biogenesis of exosomes. Nat Cell Biol 14:677–685
Beauvais DM, Rapraeger AC (2003) Syndecan-1-mediated cell spreading requires signaling by alphavbeta3 integrins in human breast carcinoma cells. Exp Cell Res 286:219–232
Bentahir M, Nyabi O, Verhamme J, Tolia A, Horre K, Wiltfang J, Esselmann H, De Strooper B (2006) Presenilin clinical mutations can affect gamma-secretase activity by different mechanisms. J Neurochem 96:732–742
Berndt C, Casaroli-Marano RP, Vilaró S, Reina M (2001) Cloning and characterization of human syndecan-3. J Cell Biochem 82:246–259
Bernfield M, Kokenyesi R, Kato M, Hinkes M, Spring J, Gallo R, Lose E (1992) Biology of the syndecans: a family of transmembrane heparan sulfate proteoglycans. Annu Rev Cell Biol 8:365–393
Bernfield M, Gotte M, Park PW, Reizes O, Fitzgerald ML, Lincecum J, Zako M (1999) Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem 68:729–777
Bespalov MM, Sidorova YA, Tumova S, Ahonen-Bishopp A, Magalhães AC, Kulesskiy E, Paveliev M, Rivera C, Rauvala H, Saarma M (2011) Heparan sulfate proteoglycan syndecan-3 is a novel receptor for GDNF, neurturin, and artemin. J Cell Biol 192:153–169
Biressi S, Molinaro M, Cossu G (2007) Cellular heterogeneity during vertebrate skeletal muscle development. Dev Biol 308:281–293
Brandan E, Gutierrez J (2013) Role of skeletal muscle proteoglycans during myogenesis. Matrix Biol 32:289–297
Buckingham M (2007) Skeletal muscle progenitor cells and the role of Pax genes. C R Biol 330:530–533
Buckwalter JA, Mankin HJ (1998) Articular cartilage: degeneration and osteoarthritis, repair, regeneration, and transplantation. Instr Course Lect 47:487–504
Carey DJ, Evans DM, Stahl RC, Asundi VK, Conner KJ, Garbes P, Cizmeci-Smith G (1992) Molecular cloning and characterization of N-syndecan, a novel transmembrane heparan sulfate proteoglycan. J Cell Biol 117:191–201
Carey DJ, Conner K, Asundi VK, O’Mahony DJ, Stahl RC, Showalter L, Cizmeci-Smith G, Hartman J, Rothblum LI (1997) cDNA cloning, genomic organization, and in vivo expression of rat N-syndecan. J Biol Chem 272:2873–2879
Casar JC, Cabello-Verrugio C, Olguin H, Aldunate R, Inestrosa NC, Brandan E (2004) Heparan sulfate proteoglycans are increased during skeletal muscle regeneration: requirement of syndecan-3 for successful fiber formation. J Cell Sci 117:73–84
Chakravarti R, Adams JC (2006) Comparative genomics of the syndecans defines an ancestral genomic context associated with matrilins in vertebrates. BMC Genomics 7:83
Chakravarti R, Sapountzi V, Adams JC (2005) Functional role of syndecan-1 cytoplasmic V region in lamellipodial spreading, actin bundling, and cell migration. Mol Biol Cell 16:3678–3691
Chanalaris A, Clarke H, Guimond SE, Vincent TL, Turnbull JE, Troeberg L (2019) Heparan sulfate proteoglycan synthesis is dysregulated in human osteoarthritic cartilage. Am J Pathol 189:632–647
Chen E, Hermanson S, Ekker SC (2004) Syndecan-2 is essential for angiogenic sprouting during zebrafish development. Blood 103:1710–1719
Choi S, Lee H, Choi JR, Oh ES (2010) Shedding; towards a new paradigm of syndecan function in cancer. BMB Rep 43:305–310
Choi Y, Chung H, Jung H, Couchman JR, Oh ES (2011) Syndecans as cell surface receptors: Unique structure equates with functional diversity. Matrix Biol 30:93–99
Choi S, Kim JY, Park JH, Lee ST, Han IO, Oh ES (2012) The matrix metalloproteinase-7 regulates the extracellular shedding of syndecan-2 from colon cancer cells. Biochem Biophys Res Commun 417:1260–1264
Choi Y, Yun JH, Yoo J, Lee I, Kim H, Son HN, Kim IS, Yoon HS, Zimmermann P, Couchman JR, Cho HS, Oh ES, Lee W (2016) New structural insight of C-terminal region of Syntenin-1, enhancing the molecular dimerization and inhibitory function related on Syndecan-4 signaling. Sci Rep 6:36818
Christ B, Ordahl CP (1995) Early stages of chick somite development. Anat Embryol 191:381–396
Cornelison DD, Filla MS, Stanley HM, Rapraeger AC, Olwin BB (2001) Syndecan-3 and syndecan-4 specifically mark skeletal muscle satellite cells and are implicated in satellite cell maintenance and muscle regeneration. Dev Biol 239:79–94
Cornelison DDW, Wilcox-Adelman SA, Goetinck PF, Rauvala H, Rapraeger AC, Olwin BB (2004) Essential and separable roles for Syndecan-3 and Syndecan-4 in skeletal muscle development and regeneration. Genes Dev 18:2231–2236
Couchman JR (2003) Syndecans: proteoglycan regulators of cell-surface microdomains? Nat Rev Mol Cell Biol 4:926–937
Couchman JR (2010) Transmembrane signaling proteoglycans. Annu Rev Cell Dev Biol 26:89–114
David G, van der Schueren B, Marynen P, Cassiman JJ, van den Berghe H (1992) Molecular cloning of amphiglycan, a novel integral membrane heparan sulfate proteoglycan expressed by epithelial and fibroblastic cells. J Cell Biol 118:961–969
De Rossi G, Whiteford JR (2013) A novel role for syndecan-3 in angiogenesis. F1000Research 2:270
Dews IC, Mackenzie KR (2007) Transmembrane domains of the syndecan family of growth factor coreceptors display a hierarchy of homotypic and heterotypic interactions. Proc Natl Acad Sci U S A 104:20782–20787
Endo K, Takino T, Miyamori H, Kinsen H, Yoshizaki T, Furukawa M, Sato H (2003) Cleavage of syndecan-1 by membrane type matrix metalloproteinase-1 stimulates cell migration. J Biol Chem 278:40764–40770
Esko JD, Zhang L (1996) Influence of core protein sequence on glycosaminoglycan assembly. Curr Opin Struct Biol 6:663–670
Eustace AD, McNaughton EF, King S, Kehoe O, Kungl A, Mattey D, Nobbs AH, Williams N, Middleton J (2019) Soluble syndecan-3 binds chemokines, reduces leukocyte migration in vitro and ameliorates disease severity in models of rheumatoid arthritis. Arthritis Res Ther 21:172
Fisher MC, Li Y, Seghatoleslami MR, Dealy CN, Kosher RA (2006) Heparan sulfate proteoglycans including syndecan-3 modulate BMP activity during limb cartilage differentiation. Matrix Biol 25:27–39
Fitzgerald ML, Wang Z, Park PW, Murphy G, Bernfield M (2000) Shedding of syndecan-1 and -4 ectodomains is regulated by multiple signaling pathways and mediated by a TIMP-3-sensitive metalloproteinase. J Cell Biol 148:811–824
Fry CS, Lee JD, Mula J, Kirby TJ, Jackson JR, Liu F, Yang L, Mendias CL, Dupont-Versteegden EE, McCarthy JJ, Peterson CA (2015) Inducible depletion of satellite cells in adult, sedentary mice impairs muscle regenerative capacity without affecting sarcopenia. Nat Med 21:76–80
Fry CS, Kirby TJ, Kosmac K, McCarthy JJ, Peterson CA (2017) Myogenic progenitor cells control extracellular matrix production by fibroblasts during skeletal muscle hypertrophy. Cell Stem Cell 20:56–69
Gao Q, Chen CY, Zong C, Wang S, Ramiah A, Prabhakar P, Morris LC, Boons GJ, Moremen KW, Prestegard JH (2016) Structural aspects of heparan sulfate binding to Robo1-Ig1-2. ACS Chem Biol 11:3106–3113
Ghadiali RS, Guimond SE, Turnbull JE, Pisconti A (2017) Dynamic changes in heparan sulfate during muscle differentiation and ageing regulate myoblast cell fate and FGF2 signalling. Matrix Biol 59:54–68
Gould SE, Upholt WB, Kosher RA (1992) Syndecan 3: a member of the syndecan family of membrane-intercalated proteoglycans that is expressed in high amounts at the onset of chicken limb cartilage differentiation. Proc Natl Acad Sci U S A 89:3271–3275
Goulding M, Lumsden A, Paquette AJ (1994) Regulation of Pax-3 expression in the dermomyotome and its role in muscle development. Development 120:957–971
Granes F, Berndt C, Roy C, Mangeat P, Reina M, Vilaro S (2003) Identification of a novel Ezrin-binding site in syndecan-2 cytoplasmic domain. FEBS Lett 547:212–216
Guimond SE, Turnbull JE (1999) Fibroblast growth factor receptor signalling is dictated by specific heparan sulphate saccharides. Curr Biol 9:1343–1346
Handley CJ, Lowther DA (1979) Extracellular matrix metabolism by chondrocytes. 5. The proteoglycans and glycosaminoglycans synthesized by chondrocytes in high density cultures. Biochim Biophys Acta 582:234–245
Hayashida K, Chen Y, Bartlett AH, Park PW (2008a) Syndecan-1 is an in vivo suppressor of Gram-positive toxic shock. J Biol Chem 283:19895–19903
Hayashida K, Stahl PD, Park PW (2008b) Syndecan-1 ectodomain shedding is regulated by the small GTPase Rab5. J Biol Chem 283:35435–35444
Herndon ME, Stipp CS, Lander AD (1999) Interactions of neural glycosaminoglycans and proteoglycans with protein ligands: assessment of selectivity, heterogeneity and the participation of core proteins in binding. Glycobiology 9:143–155
Hienola A, Tumova S, Kulesskiy E, Rauvala H (2006) N-syndecan deficiency impairs neural migration in brain. J Cell Biol 174:569–580
Hooper NM, Karran EH, Turner AJ (1997) Membrane protein secretases. Biochem J 321(Pt 2):265–279
Horowitz A, Simons M (1998) Phosphorylation of the cytoplasmic tail of syndecan-4 regulates activation of protein kinase Calpha. J Biol Chem 273:25548–25551
Horowitz A, Murakami M, Gao Y, Simons M (1999) Phosphatidylinositol-4,5-bisphosphate mediates the interaction of syndecan-4 with protein kinase C. Biochemistry 38:15871–15877
Huang YZ, Wang Q, Zhang CL, Fang XT, Song EL, Chen H (2016) Genetic variants in SDC3 gene are significantly associated with growth traits in two Chinese beef cattle breeds. Anim Biotechnol 27:190–198
Imai S, Kaksonen M, Raulo E, Kinnunen T, Fages C, Meng X, Lakso M, Rauvala H (1998) Osteoblast recruitment and bone formation enhanced by cell matrix-associated heparin-binding growth-associated molecule (HB-GAM). J Cell Biol 143:1113–1128
Imai S, Heino TJ, Hienola A, Kurata K, Buki K, Matsusue Y, Vaananen HK, Rauvala H (2009) Osteocyte-derived HB-GAM (pleiotrophin) is associated with bone formation and mechanical loading. Bone 44:785–794
Jang B, Jung H, Choi S, Lee YH, Lee ST, Oh ES (2017) Syndecan-2 cytoplasmic domain up-regulates matrix metalloproteinase-7 expression via the protein kinase Cgamma-mediated FAK/ERK signaling pathway in colon cancer. J Biol Chem 292:16321–16332
Johnson de Sousa Brito FM, Butcher A, Pisconti A, Poulet B, Prior A, Charlesworth G, Sperinck C, Scotto di Mase M, Liu K, Bou-Gharios G, van’t Hof RJ, Daroszewska A (2021) Syndecan-3 enhances anabolic bone formation through WNT signaling. FASEB J 35:e21246. https://doi.org/10.1096/fj.202002024R
Jones FK, Hardman GE, Ferries S, Eyers CE, Pisconti A (2019) Myoblast phosphoproteomics as a tool to investigate global signaling events during myogenesis. Methods Mol Biol 1889:301–317
Jones FK, Stefan A, Kay AG, Hyland M, Morgan R, Forsyth NR, Pisconti A, Kehoe O (2020) Syndecan-3 regulates MSC adhesion, ERK and AKT signalling in vitro and its deletion enhances MSC efficacy in a model of inflammatory arthritis in vivo. Sci Rep 10(1):20487. https://doi.org/10.1038/s41598-020-77514-z
Jones FK, Phillips A, Jones AR, Pisconti A (2021) SDC3 acts as a timekeeper of myogenic differentiation by regulating the insulin/AKT/mTOR axis in muscle stem cell progeny. BioRxiv. https://doi.org/10.1101/2020.08.10.244152
Jung H, Han M, Jang B, Park E, Oh ES (2020) The oligomerization mediated by the alanine 397 residue in the transmembrane domain is crucial to sydecan-3 functions. Cell Signal 69:109544
Keefe AC, Lawson JA, Flygare SD, Fox ZD, Colasanto MP, Mathew SJ, Yandell M, Kardon G (2015) Muscle stem cells contribute to myofibres in sedentary adult mice. Nat Commun 6:7087
Kehoe O, Kalia N, King S, Eustace A, Boyes C, Reizes O, Williams A, Patterson A, Middleton J (2014) Syndecan-3 is selectively pro-inflammatory in the joint and contributes to antigen-induced arthritis in mice. Arthritis Res Ther 16:R148
Kim JM, Lee K, Kim MY, Shin HI, Jeong D (2018) Suppressive effect of syndecan ectodomains and N-desulfated heparins on osteoclastogenesis via direct binding to macrophage-colony stimulating factor. Cell Death Dis 9:1119
Kinnunen T, Kaksonen M, Saarinen J, Kalkkinen N, Peng HB, Rauvala H (1998) Cortactin-Src kinase signaling pathway is involved in N-syndecan-dependent neurite outgrowth. J Biol Chem 273:10702–10708
Kirsch T, Koyama E, Liu M, Golub EE, Pacifici M (2002) Syndecan-3 is a selective regulator of chondrocyte proliferation. J Biol Chem 277:42171–42177
Kosher RA (1998) Syndecan-3 in limb skeletal development. Microsc Res Tech 43:123–130
Koyama E, Shimazu A, Leatherman JL, Golden EB, Nah HD, Pacifici M (1996) Expression of syndecan-3 and tenascin-C: possible involvement in periosteum development. J Orthop Res 14:403–412
Lehmann W, Schinke T, Schilling AF, Catala-Lehnen P, Gebauer M, Pogoda P, Gerstenfeld LC, Rueger JM, Einhorn TA, Amling M (2004) Absence of mouse pleiotrophin does not affect bone formation in vivo. Bone 35:1247–1255
Leonova EI, Galzitskaya OV (2015) Cell communication using intrinsically disordered proteins: what can syndecans say? J Biomol Struct Dyn 33:1037–1050
Loeser RF, Goldring SR, Scanzello CR, Goldring MB (2012) Osteoarthritis: a disease of the joint as an organ. Arthritis Rheum 64:1697–1707
Mackie EJ, Ahmed YA, Tatarczuch L, Chen KS, Mirams M (2008) Endochondral ossification: how cartilage is converted into bone in the developing skeleton. Int J Biochem Cell Biol 40:46–62
Manon-Jensen T, Itoh Y, Couchman JR (2010) Proteoglycans in health and disease: the multiple roles of syndecan shedding. FEBS J 277:3876–3889
Manon-Jensen T, Multhaupt HA, Couchman JR (2013) Mapping of matrix metalloproteinase cleavage sites on syndecan-1 and syndecan-4 ectodomains. FEBS J 280:2320–2331
Marynen P, Zhang J, Cassiman JJ, Van den Berghe H, David G (1989) Partial primary structure of the 48- and 90-kilodalton core proteins of cell surface-associated heparan sulfate proteoglycans of lung fibroblasts. Prediction of an integral membrane domain and evidence for multiple distinct core proteins at the cell surface of human lung fibroblasts. J Biol Chem 264:7017–7024
Mashinchian O, Pisconti A, Le Moal E, Bentzinger CF (2018) The muscle stem cell niche in health and disease. Curr Top Dev Biol 126:23–65
Masuda H, Tsujimura A, Yoshioka M, Arai Y, Kuboki Y, Mukai T, Nakamura T, Tsuji H, Nakagawa M, Hashimoto-Gotoh T (1997) Bone mass loss due to estrogen deficiency is compensated in transgenic mice overexpressing human osteoblast stimulating factor-1. Biochem Biophys Res Commun 238:528–533
Mauro A (1961) Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9:493–495
McInnes IB, Schett G (2011) The pathogenesis of rheumatoid arthritis. N Engl J Med 365:2205–2219
Mitsiadis TA, Salmivirta M, Muramatsu T, Muramatsu H, Rauvala H, Lehtonen E, Jalkanen M, Thesleff I (1995) Expression of the heparin-binding cytokines, midkine (MK) and HB-GAM (pleiotrophin) is associated with epithelial-mesenchymal interactions during fetal development and organogenesis. Development 121:37–51
Molteni A, Modrowski D, Hott M, Marie PJ (1999) Differential expression of fibroblast growth factor receptor-1, -2, and -3 and syndecan-1, -2, and -4 in neonatal rat mandibular condyle and calvaria during osteogenic differentiation in vitro. Bone 24:337–347
Morgan MR, Humphries MJ, Bass MD (2007) Synergistic control of cell adhesion by integrins and syndecans. Nat Rev Mol Cell Biol 8:957–969
Noborn F, Gomez Toledo A, Green A, Nasir W, Sihlbom C, Nilsson J, Larson G (2016) Site-specific identification of heparan and chondroitin sulfate glycosaminoglycans in hybrid proteoglycans. Sci Rep 6:34537
O’Callaghan P, Sandwall E, Li JP, Yu H, Ravid R, Guan ZZ, van Kuppevelt TH, Nilsson LN, Ingelsson M, Hyman BT, Kalimo H, Lindahl U, Lannfelt L, Zhang X (2008) Heparan sulfate accumulation with Abeta deposits in Alzheimer’s disease and Tg2576 mice is contributed by glial cells. Brain Pathol 18:548–561
Oh ES, Couchman JR, Woods A (1997a) Serine phosphorylation of syndecan-2 proteoglycan cytoplasmic domain. Arch Biochem Biophys 344:67–74
Oh ES, Woods A, Couchman JR (1997b) Syndecan-4 proteoglycan regulates the distribution and activity of protein kinase C. J Biol Chem 272:8133–8136
Olguin H, Brandan E (2001) Expression and localization of proteoglycans during limb myogenic activation. Dev Dyn 221:106–115
OlguĂn HC, Pisconti A (2012) Marking the tempo for myogenesis: Pax7 and the regulation of muscle stem cell fate decisions. J Cell Mol Med 16:1013–1025
Ortega N, Behonick DJ, Werb Z (2004) Matrix remodeling during endochondral ossification. Trends Cell Biol 14:86–93
Ott VL, Rapraeger AC (1998) Tyrosine phosphorylation of syndecan-1 and -4 cytoplasmic domains in adherent B82 fibroblasts. J Biol Chem 273:35291–35298
Pacifici M, Shimo T, Gentili C, Kirsch T, Freeman TA, Enomoto-Iwamoto M, Iwamoto M, Koyama E (2005) Syndecan-3: a cell-surface heparan sulfate proteoglycan important for chondrocyte proliferation and function during limb skeletogenesis. J Bone Miner Metab 23:191–199
Pap T, Bertrand J (2013) Syndecans in cartilage breakdown and synovial inflammation. Nat Rev Rheumatol 9:43–55
Park H, Kim Y, Lim Y, Han I, Oh ES (2002) Syndecan-2 mediates adhesion and proliferation of colon carcinoma cells. J Biol Chem 277:29730–29736
Patterson AM, Gardner L, Shaw J, David G, Loreau E, Aguilar L, Ashton BA, Middleton J (2005) Induction of a CXCL8 binding site on endothelial syndecan-3 in rheumatoid synovium. Arthritis Rheum 52:2331–2342
Patterson AM, Cartwright A, David G, Fitzgerald O, Bresnihan B, Ashton BA, Middleton J (2008) Differential expression of syndecans and glypicans in chronically inflamed synovium. Ann Rheum Dis 67:592–601
Pawlikowski B, Pulliam C, Betta ND, Kardon G, Olwin BB (2015) Pervasive satellite cell contribution to uninjured adult muscle fibers. Skelet Muscle 5:42
Pfander D, Swoboda B, Kirsch T (2001) Expression of early and late differentiation markers (proliferating cell nuclear antigen, syndecan-3, annexin VI, and alkaline phosphatase) by human osteoarthritic chondrocytes. Am J Pathol 159:1777–1783
Pisconti A, Cornelison DDW, OlguĂn HC, Antwine TL, Olwin BB (2010) Syndecan-3 and Notch cooperate in regulating adult myogenesis. J Cell Biol 190:427–441
Pisconti A, Bernet JD, Olwin BB (2012) Syndecans in skeletal muscle development, regeneration and homeostasis. Muscles Ligaments Tendons J 2:1–9
Pisconti A, Banks GB, Babaeijandaghi F, Betta ND, Rossi FMV, Chamberlain JS, Olwin BB (2016) Loss of niche-satellite cell interactions in syndecan-3 null mice alters muscle progenitor cell homeostasis improving muscle regeneration. Skelet Muscle 6:34
Prasthofer T, Ek B, Ekman P, Owens R, Hook M, Johansson S (1995) Protein kinase C phosphorylates two of the four known syndecan cytoplasmic domains in vitro. Biochem Mol Biol Int 36:793–802
Pruessmeyer J, Martin C, Hess FM, Schwarz N, Schmidt S, Kogel T, Hoettecke N, Schmidt B, Sechi A, Uhlig S, Ludwig A (2010) A disintegrin and metalloproteinase 17 (ADAM17) mediates inflammation-induced shedding of syndecan-1 and -4 by lung epithelial cells. J Biol Chem 285:555–564
Rapraeger AC, Bernfield M (1983) Heparan sulfate proteoglycans from mouse mammary epithelial cells. A putative membrane proteoglycan associates quantitatively with lipid vesicles. J Biol Chem 258:3632–3636
Rapraeger A, Jalkanen M, Bernfield M (1986) Cell surface proteoglycan associates with the cytoskeleton at the basolateral cell surface of mouse mammary epithelial cells. J Cell Biol 103(6 Pt 2):2683–2696
Reiland J, Ott VL, Lebakken CS, Yeaman C, McCarthy J, Rapraeger AC (1996) Pervanadate activation of intracellular kinases leads to tyrosine phosphorylation and shedding of Syndecan-1. Biochem J 319:39–47
Reizes O, Benoit SC, Strader AD, Clegg DJ, Akunuru S, Seeley RJ (2003) Syndecan-3 modulates food intake by interacting with the melanocortin/AgRP pathway. Ann N Y Acad Sci 994:66–73
Relaix F, Zammit PS (2012) Satellite cells are essential for skeletal muscle regeneration: the cell on the edge returns centre stage. Development 139:2845–2856
Relaix F, Rocancourt D, Mansouri A, Buckingham M (2005) A Pax3/Pax7-dependent population of skeletal muscle progenitor cells. Nature 435:948–953
Rudd TR, Skidmore MA, Guerrini M, Hricovini M, Powell AK, Siligardi G, Yates EA (2010) The conformation and structure of GAGs: recent progress and perspectives. Curr Opin Struct Biol 20:567–574
Saunders S, Bernfield M (1988) Cell surface proteoglycan binds mouse mammary epithelial cells to fibronectin and behaves as a receptor for interstitial matrix. J Cell Biol 106:423–430
Saunders S, Jalkanen M, O’Farrell S, Bernfield M (1989) Molecular cloning of syndecan, an integral membrane proteoglycan. J Cell Biol 108:1547–1556
Schmidt M, Schuler SC, Huttner SS, von Eyss B, von Maltzahn J (2019) Adult stem cells at work: regenerating skeletal muscle. Cell Mol Life Sci 76:2559–2570
Scholefield Z, Yates EA, Wayne G, Amour A, McDowell W, Turnbull JE (2003) Heparan sulfate regulates amyloid precursor protein processing by BACE1, the Alzheimer’s beta-secretase. J Cell Biol 163:97–107
Schroeder TM, Jensen ED, Westendorf JJ (2005) Runx2: a master organizer of gene transcription in developing and maturing osteoblasts. Birth Defects Res C Embryo Today 75:213–225
Schulz JG, Annaert W, Vandekerckhove J, Zimmermann P, De Strooper B, David G (2003) Syndecan 3 intramembrane proteolysis is presenilin/gamma-secretase-dependent and modulates cytosolic signaling. J Biol Chem 278:48651–48657
Seghatoleslami MR, Kosher RA (1996) Inhibition of in vitro limb cartilage differentiation by syndecan-3 antibodies. Dev Dyn 207:114–119
Sherwood J (2019) Osteoarthritis year in review 2018: biology. Osteoarthr Cartil 27:365–370
Shimazu A, Nah HD, Kirsch T, Koyama E, Leatherman JL, Golden EB, Kosher RA, Pacifici M (1996) Syndecan-3 and the control of chondrocyte proliferation during endochondral ossification. Exp Cell Res 229:126–136
Shimo T, Gentili C, Iwamoto M, Wu C, Koyama E, Pacifici M (2004) Indian hedgehog and syndecans-3 coregulate chondrocyte proliferation and function during chick limb skeletogenesis. Dev Dyn 229:607–617
Shin J, Lee W, Lee D, Koo BK, Han I, Lim Y, Woods A, Couchman JR, Oh ES (2001) Solution structure of the dimeric cytoplasmic domain of syndecan-4. Biochemistry 40:8471–8478
Spring J, Paine-Saunders SE, Hynes RO, Bernfield M (1994) Drosophila syndecan: conservation of a cell-surface heparan sulfate proteoglycan. Proc Natl Acad Sci U S A 91:3334–3338
Steinfeld R, Van Den Berghe H, David G (1996) Stimulation of fibroblast growth factor receptor-1 occupancy and signaling by cell surface-associated syndecans and glypican. J Cell Biol 133:405–416
Szekanecz Z, Koch AE (2016) Successes and failures of chemokine-pathway targeting in rheumatoid arthritis. Nat Rev Rheumatol 12:5–13
Tanaka KK, Hall JK, Troy AA, Cornelison DDW, Majka SM, Olwin BB (2009) Syndecan-4-expressing muscle progenitor cells in the SP engraft as satellite cells during muscle regeneration. Cell Stem Cell 4:217–225
Tare RS, Oreffo RO, Clarke NM, Roach HI (2002a) Pleiotrophin/Osteoblast-stimulating factor 1: dissecting its diverse functions in bone formation. J Bone Miner Res 17:2009–2020
Tare RS, Oreffo RO, Sato K, Rauvala H, Clarke NM, Roach HI (2002b) Effects of targeted overexpression of pleiotrophin on postnatal bone development. Biochem Biophys Res Commun 298:324–332
Teplyuk NM, Haupt LM, Ling L, Dombrowski C, Mun FK, Nathan SS, Lian JB, Stein JL, Stein GS, Cool SM, van Wijnen AJ (2009) The osteogenic transcription factor Runx2 regulates components of the fibroblast growth factor/proteoglycan signaling axis in osteoblasts. J Cell Biochem 107:144–154
Tkachenko E, Rhodes JM, Simons M (2005) Syndecans: new kids on the signaling block. Circ Res 96:488–500
Tumova S, Woods A, Couchman JR (2000) Heparan sulfate chains from glypican and syndecans bind the Hep II domain of fibronectin similarly despite minor structural differences. J Biol Chem 275:9410–9417
Turnbull J, Powell A, Guimond S (2001) Heparan sulfate: decoding a dynamic multifunctional cell regulator. Trends Cell Biol 11:75–82
van Velthoven CTJ, de Morree A, Egner IM, Brett JO, Rando TA (2017) Transcriptional profiling of quiescent muscle stem cells in vivo. Cell Rep 21:1994–2004
Waggett AD, Ralphs JR, Kwan AP, Woodnutt D, Benjamin M (1998) Characterization of collagens and proteoglycans at the insertion of the human Achilles tendon. Matrix Biol 16:457–470
Whiteford JR, Couchman JR (2006) A conserved NXIP motif is required for cell adhesion properties of the syndecan-4 ectodomain. J Biol Chem 281:32156–32163
Whiteford JR, Behrends V, Kirby H, Kusche-Gullberg M, Muramatsu T, Couchman JR (2007) Syndecans promote integrin-mediated adhesion of mesenchymal cells in two distinct pathways. Exp Cell Res 313:3902–3913
Yanagishita M, Hascall VC (1984) Metabolism of proteoglycans in rat ovarian granulosa cell culture. Multiple intracellular degradative pathways and the effect of chloroquine. J Biol Chem 259:10270–10283
Zammit PS, Golding JP, Nagata Y, Hudon V, Partridge TA, Beauchamp JR (2004) Muscle satellite cells adopt divergent fates: a mechanism for self-renewal? J Cell Biol 166:347–357
Zhang Y, Wang Z, Liu J, Zhang Z, Chen Y (2016) Suppressing Syndecan-1 shedding ameliorates intestinal epithelial inflammation through inhibiting NF-kappaB pathway and TNF-alpha. Gastroenterol Res Pract 2016:6421351
Zhang Y, Wang Z, Liu J, Zhang S, Fei J, Li J, Zhang T, Wang J, Park PW, Chen Y (2017) Cell surface-anchored syndecan-1 ameliorates intestinal inflammation and neutrophil transmigration in ulcerative colitis. J Cell Mol Med 21:13–25
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2021 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Jones, F.K., Kehoe, O., Daroszewska, A., van’t Hof, R.J., Pisconti, A. (2021). Syndecan-3: A Signaling Conductor in the Musculoskeletal System. In: Götte, M., Forsberg-Nilsson, K. (eds) Proteoglycans in Stem Cells. Biology of Extracellular Matrix, vol 9. Springer, Cham. https://doi.org/10.1007/978-3-030-73453-4_7
Download citation
DOI: https://doi.org/10.1007/978-3-030-73453-4_7
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-73452-7
Online ISBN: 978-3-030-73453-4
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)