Skip to main content
SpringerLink
Log in

Innate and Acquired Cellular Immune Responses in Psoriasis and Psoriatic Arthritis

  • Chapter
  • First Online:
Psoriatic Arthritis and Psoriasis

  • 1836 Accesses

Abstract

Concepts of psoriasis and psoriatic arthritis pathogenesis are changing due to new knowledge of their immunopathology. Originally considered a disease of abnormal keratinocyte function, psoriasis was then considered an autoimmune Th1 T cell mediated condition due to the large number of interferon-γ secreting T cells in the skin. Recent findings showing a key role for cytokines such as interleukin 17 (IL-17) and IL-23, produced by a variety of resident skin cells, has led to the current concept that psoriasis is due to dysregulated immune function. Findings in psoriatic arthritis have generated similar changes in thought. A key factor in this change was the increased number of cell types capable of producing IL-17 and IL-23. IL-17 was originally described as a CD4 T cell product, then found to define the Th17 specific CD4 lineage. Interleukin 23, an antigen presenting cell product, plays a central role in the differentiation and stabilisation of Th17 cells. Subsequently, IL-17 was found to be produced by many immune cells of both the adaptive and the innate immune systems, including CD8 T cells, NK and innate lymphoid cells, gamma-delta T cells and neutrophils. Innate immune cells respond to pathogen or cell damage signals, with immediate cytokine responses providing early defence. Innate cell interaction with the acquired or adaptive immune system links the responses. The skin as the primary interface with the external environment, provides the first line of host defence against injury and infection, and is rich in cells of both the innate and adaptive immune system. This chapter will review the current evidence of innate and adaptive immune function in psoriasis and psoriatic arthritis, with an emphasis on recent reports.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Lowes MA, Suárez-Fariñas M, Krueger JG. Immunology of psoriasis. Annu Rev Immunol. 2014;32:227–55.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  2. Boehncke WH, Schön MP. Psoriasis. Lancet. S0140-6736(14)61909-7. 2015;386:983–94.

    Google Scholar 

  3. Lowes MA, Russell CB, Martin DA, et al. The IL-23/T17 pathogenic axis in psoriasis is amplified by keratinocyte responses. Trends Immunol. 2013;34:174–81.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  4. Smith MD, Barg E, Weedon H, Papengelis V, Smeets T, Tak PP, Kraan M, Coleman M, Ahern MJ. Microarchitecture and protective mechanisms in synovial tissue from clinically and arthroscopically normal knee joints. Ann Rheum Dis. 2003;62:303–7.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  5. Celis R, Planell N, Fernandez-Sueiro JL, Sanmarti R, Ramirez J, Gonzalez-Alvaro I, et al. Synovial cytokine expression in psoriatic arthritis and associations with lymphoid neogenesis and clinical features. Arthritis Res Ther. 2012;14:R93.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  6. Van Landuyt KB, JonesE A, McGonagle D, Luyten FP, Lories RJ. Flow cytometric characterization of freshly isolated and culture expanded human synovial cell populations in patients with chronic arthritis. Arthritis Res Ther. 2010;12:R15.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. Veale D, Yanni G, Rogers S, Barnes L, Bresnihan B, Fitzgerald O. Reduced synovial membrane macrophage numbers, ELAM-1 expression, and lining layer hyperplasia in psoriatic arthritis as compared with rheumatoid arthritis. Arthritis Rheum. 1993;36:893–900.

    Article  PubMed  CAS  Google Scholar 

  8. Danning CL, Illei GG, Hitchon C, Greer MR, Boumpas DT, McInnes IB. Macrophage-derived cytokine and nuclear factor kappaB p65 expression in synovial membrane and skin of patients with psoriatic arthritis. Arthritis Rheum. 2000;43(6):1244–56.

    Article  PubMed  CAS  Google Scholar 

  9. Kruithof E, Baeten D, De RL, Vandooren B, Foell D, Roth J, et al. Synovial histopathology of psoriatic arthritis, both oligo- and polyarticular, resembles spondyloarthropathy more than it does rheumatoid arthritis. Arthritis Res Ther. 2005;7(3):R569–80.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. Costello P, Bresnihan B, O’Farrelly C, FitzGerald O. Predominance of CD8+ T lymphocytes in psoriatic arthritis. J Rheumatol. 1999;26:1117–24.

    PubMed  CAS  Google Scholar 

  11. van Kuijk AWR, Reinders-Blankert P, Smeets TJM, Dijkmans BAC, Tak PP. Detailed analysis of the cell infiltrate and the expression of mediators of synovial inflammation and joint destruction in the synovium of patients with psoriatic arthritis: implications for treatment. Ann Rheum Dis. 2006;65:1551–7.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  12. Baeten D, Kruithof E, De Rycke L, Boots AM, Mielants H, Veys EM, De Keyser F. Infiltration of the synovial membrane with macrophage subsets and polymorphonuclear cells reflects global disease activity in spondyloarthropathy. Arthritis Res Ther. 2005;7:R359–69.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Yeremenko N, Noordenbos T, Cantaert T, van Tok M, van de Sande M, Cañete JD, Tak PP, Baeten D. Disease-specific and inflammation-independent stromal alterations in spondylarthritis synovitis. Arthritis Rheum. 2013;65:174–85.

    Article  PubMed  CAS  Google Scholar 

  14. Mak RKH, Hundhausen C, Nestle FO. Progress in understanding the immunopathogenesis of psoriasis. Clinical subtypes, histological features and associated comorbidities. Actas Dermosifiliogr. 2009;100 Suppl 2:2–13.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Baeten D, Van Damme N, Van den Bosch F, Kruithof E, De Vos M, Mielants H, Veys EM, De Keyser F. Impaired Th1 cytokine production in spondyloarthropathy is restored by anti-TNFalpha. Ann Rheum Dis. 2001;60:750–5.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  16. Ambarus C, Yeremenko N, Tak PP, Baeten D. Pathogenesis of spondyloarthritis: autoimmune or autoinflammatory? Curr Opin Rheumatol. 2012;24:351–8.

    Article  PubMed  CAS  Google Scholar 

  17. Huffmeier U, Uebe S, Ekici AB, Bowes J, Giardina E, Korendowych E, et al. Common variants at TRAF3IP2 are associated with susceptibility to psoriatic arthritis and psoriasis. Nat Genet. 2010;42:996–9.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Apel M, Uebe S, Bowes J, Giardina E, Korendowych E, Juneblad K, et al. Variants in RUNX3 contribute to susceptibility to psoriatic arthritis, exhibiting further common ground with ankylosing spondylitis. Arthritis Rheum. 2013;65:1224–31.

    Article  PubMed  CAS  Google Scholar 

  19. McGonagle D, Lories RJ, Tan AL, Benjamin M. The concept of a “synovio-entheseal complex” and its implications for understanding joint inflammation and damage in psoriatic arthritis and beyond. Arthritis Rheum. 2007;56(8):2482–91.

    Article  PubMed  Google Scholar 

  20. McGonagle D, Benjamin M, Tan AL. The pathogenesis of psoriatic arthritis and associated nail disease: not autoimmune after all? Curr Opin Rheumatol. 2009;21(4):340–7.

    Article  PubMed  CAS  Google Scholar 

  21. Sherlock JP, Joyce-Shaikh B, Turner SP, et al. IL-23 induces spondyloarthropathy by acting on ROR-γt + CD3+ CD4–CD8– entheseal resident T cells. Nat Med. 2012;18:1069–76.

    Article  PubMed  CAS  Google Scholar 

  22. Kirkham BW, Kavanaugh A, Reich K. Interleukin-17A: a unique pathway in immune mediated diseases: psoriasis, psoriatic arthritis, and rheumatoid arthritis. Immunology. 2014;141:133–42.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Ferretti S, Bonneau O, Dubois GR, Jones CE, Trifilieff A. IL-17, produced by lymphocytes and neutrophils, is necessary for lipopolysaccharide induced airway neutrophilia: IL-15 as a possible trigger. J Immunol. 2003;170(4):2106–12.

    Article  PubMed  CAS  Google Scholar 

  24. Li L, Huang L, Vergis AL, Ye H, Bajwa A, Narayan V, Strieter RM, Rosin DL, Okusa MD. IL-17 produced by neutrophils regulates IFN-γ–mediated neutrophil migration in mouse kidney ischemia-reperfusion injury. J Clin Invest. 2010;120:331–42.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Reich K, Papp KA, Matheson RT, Tu JH, Bissonnette R, Bourcier M, Gratton D, Kunynetz RA, Poulin Y, Rosoph LA, Stingl G, Bauer WM, Salter JM, Falk TM, Blödorn-Schlicht NA, Hueber W, Sommer U, Schumacher MM, Peters T, Kriehuber E, Lee DM, Wieczorek GA, Kolbinger F, Bleul CC. Evidence that a neutrophil-keratinocyte crosstalk is an early target of IL-17A inhibition in psoriasis. Exp Dermatol. 2015;24(7):529–35. doi:10.1111/ exd.12710.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. Hueber AJ, Asquith DL, Miller AM, Reilly J, Kerr S, Leipe J, et al. Mast cells express IL-17A in rheumatoid arthritis synovium. J Immunol. 2010;184:3336–40.

    Article  PubMed  CAS  Google Scholar 

  27. Noordenbos T, Yeremenko N, Gofita I, van de Sande M, Tak PP, Canete JD, et al. Interleukin-17–positive mast cells contribute to synovial inflammation in spondylarthritis. Arthritis Rheum. 2012;64:99–109.

    Article  PubMed  CAS  Google Scholar 

  28. Appel H, Maier R, Wu P, Scheer R, Hempfing A, Kayser R, Thiel A, Radbruch A, Loddenkemper C, Sieper J. Analysis of IL-17+ cells in facet joints of patients with spondyloarthritis suggests that the innate immune pathway might be of greater relevance than the Th17-mediated adaptive immune response. Arthritis Res Ther. 2011;13:R95.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Mashiko S, Bouguermouh S, Rubio M, Baba N, Bissonnette R, Sarfati M. Human mast cells are major IL-22 producers in patients with psoriasis and atopic dermatitis. J Allergy Clin Immunol. pii: S0091-6749(15)00175-X. 2015;136:351–9.

    Google Scholar 

  30. Kryczek I, Bruce AT, Gudjonsson JE, Johnston A, Aphale A, Vatan L, et al. Induction of IL-17 + T cell trafficking and development by IFN-γ: mechanism and pathological relevance in psoriasis. J Immunol. 2008;181:4733–41.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  31. Ortega C, Fernandez AS, Carrillo JM, Romero P, Molina IJ, Moreno JC, et al. IL-17-producing CD8 T lymphocytes from psoriasis skin plaques are cytotoxic effector cells that secrete Th17-related cytokines. J Leukoc Biol. 2009;86:435–43.

    Article  PubMed  CAS  Google Scholar 

  32. Res PC, Piskin G, de Boer OJ, van der Loos CM, Teeling P, Bos JD, et al. Overrepresentation of IL-17A and IL-22 producing CD8 T cells in lesional skin suggests their involvement in the pathogenesis of psoriasis. PLoS One. 2010;5:e14108.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Andersson J, Samarina A, Fink J, Rahman S, Grundstrom S. Impaired expression of perforin and granulysin in CD8 + T cells at the site of infection in human chronic pulmonary tuberculosis. Infect Immun. 2007;75:5210–22.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. Huber M, Heink S, Grothe H, Guralnik A, Reinhard K, Elflein K, Hünig T, Mittrücker HW, Brüstle A, Kamradt T, Lohoff M. A Th17-like developmental process leads to CD8(+) Tc17 cells with reduced cytotoxic activity. Eur J Immunol. 2009;39:1716–25.

    Article  PubMed  CAS  Google Scholar 

  35. Menon B, Gullick NJ, Walter GJ, Rajasekhar M, Garrood T, Evans HG, Taams LS, Kirkham BW. Interleukin-17 + CD8 + T cells are enriched in the joints of patients with psoriatic arthritis and correlate with disease activity and joint damage progression. Arthritis Rheum. 2014;66:1272–81.

    Article  CAS  Google Scholar 

  36. Medzhitov R, Janeway Jr C. Innate immunity. N Engl J Med. 2000;343:338–44.

    Article  PubMed  CAS  Google Scholar 

  37. Isailovic N, Daigo K, Mantovani A, Selmi C. Interleukin-17 and innate immunity in infections and chronic inflammation. J Autoimmun. 2015;60:1–11.

    Article  PubMed  CAS  Google Scholar 

  38. Diani M, Altomare G, Reali E. T cell responses in psoriasis and psoriatic arthritis. Autoimmun Rev. 2015;14:286–92.

    Article  PubMed  CAS  Google Scholar 

  39. Al-Mossawi MH, Ridley A, Kiedel S, Bowness P. The role of natural killer cells, gamma delta T-cells and other innate immune cells in spondyloarthritis. Curr Opin Rheumatol. 2013;25:434–9.

    Article  PubMed  CAS  Google Scholar 

  40. Koyasu S, Moro K. Role of innate lymphocytes in infection and inflammation. Front Immunol. 2012;3:101.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Sutton CE, Mielke LA, Mills KHG. IL-17-producing γδ T cells and innate lymphoid cells. Eur J Immunol. 2012;42:2221–31.

    Article  PubMed  CAS  Google Scholar 

  42. Spits H, Cupedo T. Innate lymphoid cells: emerging insights in development, lineage relationships, and function. Annu Rev Immunol. 2012;30:647–75.

    Article  PubMed  CAS  Google Scholar 

  43. Bowness P, Ridley A, Shaw J, et al. Th17 cells expressing KIR3DL2þ and responsive to HLA-B27 homodimers are increased in ankylosing spondylitis. J Immunol. 2011;186:2672–80.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  44. FitzGerald O, Haroon M, Giles JT, Winchester R. Concepts of pathogenesis in psoriatic arthritis: genotype determines clinical phenotype. Arthritis Res Ther. 2015;17(1):115.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  45. McKenzie AN, Spits H, Eberl G. Innate lymphoid cells in inflammation and immunity. Immunity. 2014;41:366–74.

    Article  PubMed  CAS  Google Scholar 

  46. Montaldo E, Juelke K, Romagnani C. Group 3 innate lymphoid cells (ILC3s): origin, differentiation and plasticity in humans and mice. Eur J Immunol. 2015;45(8):2171–82. doi:10.1002/eji.201545598.

    Article  PubMed  CAS  Google Scholar 

  47. Gray EE, Suzuki K, Cyster JG. Cutting edge: identification of a motile IL-17-producing gammadelta T cell population in the dermis. J Immunol. 2011;186:6091–5.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  48. Annunziato F, Romagnani C, Romagnani S. The 3 major types of innate and adaptive cell-mediated effector immunity. J Allergy Clin Immunol. 2015;135:626–35.

    Article  PubMed  CAS  Google Scholar 

  49. Sumaria N, Roediger B, Ng LG, Qin J, Pinto R, Cavanagh LL, et al. Cutaneous immunosurveillance by self-renewing dermal gammadelta T cells. J Exp Med. 2011;208:505–18.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  50. Laggner U, Di Meglio P, Perera GK, Hundhausen C, Ke L, Niwa Ali N, Smith CH, Hayday AC, Nickoloff BJ, Nestle FO. Identification of a novel pro-inflammatory human skin-homing Vγ9Vδ2 T cell subset with a potential role in psoriasis. J Immunol. 2011;187:2783–93.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  51. Spadaro A, Scrivo R, Moretti T, Bernardini G, Riccieri V, Taccari E, Strom R, Valesini G. Natural killer cells and gamma/delta T cells in synovial fluid and in peripheral blood of patients with psoriatic arthritis. Clin Exp Rheumatol. 2004;22:389–94.

    PubMed  CAS  Google Scholar 

  52. Kenna TJ, Davidson SI, Duan R, Bradbury LA, McFarlane J, Smith M, Weedon H, Street S, Thomas R, Thomas GP, Brown MA. Enrichment of circulating interleukin-17–secreting interleukin-23 receptor–positive γδT cells in patients with active ankylosing spondylitis. Arthritis Rheum. 2012;64:1420–9.

    Article  PubMed  CAS  Google Scholar 

  53. Ottaviani C, Nasorri F, Bedini C, et al. CD56 (bright) CD16(-) NK cells accumulate in psoriatic skin in response to CXCL10 and CCL5 and exacerbate skin inflammation. Eur J Immunol. 2006;36:118–28.

    Article  PubMed  CAS  Google Scholar 

  54. Luci C, Gaudy-Marqueste C, Rouzaire P, Audonnet S, Cognet C, Hennino A, Nicolas JF, Grob JJ, Tomasello E. Peripheral natural killer cells exhibit qualitative and quantitative changes in patients with psoriasis and atopic dermatitis. Br J Dermatol. 2012;166:789–96.

    Article  PubMed  CAS  Google Scholar 

  55. Gilhar A, Ullmann Y, Kerner H, et al. Psoriasis is mediated by a cutaneous defect triggered by activated immunocytes: induction of psoriasis by cells with natural killer receptors. J Invest Dermatol. 2002;119:384–91.

    Article  PubMed  CAS  Google Scholar 

  56. Dalbeth N, Callan MFC. A subset of natural killer cells is greatly expanded within inflamed joints. Arthritis Rheum. 2002;46:1763–72.

    Article  PubMed  Google Scholar 

  57. Tang F, Sally B, Ciszewski C, Abadie V, Curran SA, Groh V, FitzGerald O, Winchester RJ, Jabri B. Interleukin 15 primes natural killer cells to kill via NKG2D and cPLA2 and this pathway is active in psoriatic arthritis. PLoS One. 2013;8(9):e76292.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  58. Villanova F, Flutter B, Tosi I, Grys K, Sreeneebus H, Perera GK, Chapman A, Smith CH, Di Meglio P, Nestle FO. Characterization of innate lymphoid cells (ILC) in human skin and blood demonstrates increase of NKp44+ ILC3 in psoriasis. J Invest Dermatol. 2014;134:984–91.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  59. Teunissen MBM, Munneke JM, Bernink JH, Spuls PI, Res PCM, te Velde A, Cheuk S, Brouwer MWD, Menting SP, Eidsmo L, Spits H, Hazenberg MD, Mjösberg J. Composition of innate lymphoid cell subsets in the human skin: enrichment of NCR+ ILC3 in lesional skin and blood of psoriasis patients. J Invest Dermatol. 2014. doi:10.1038/jid.2014.146.

    Google Scholar 

  60. Cowley SC. MAIT cells and pathogen defence. Cell Mol Life Sci. 2014;71:4831–40.

    Article  PubMed  CAS  Google Scholar 

  61. Dusseaux M, Martin E, Serriari N, Peguillet I, Premel V, Louis D, et al. Human MAIT cells are xenobiotic-resistant, tissue-targeted, CD161hi IL-17-secreting T cells. Blood. 2011;117:1250–9.

    Article  PubMed  CAS  Google Scholar 

  62. Johnston A, Gudjonsson JE. Psoriasis and the MAITing game: a role for IL-17A+ invariant TCR CD8+ T cells in psoriasis? J Invest Dermatol. 2014;134:2864–6.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  63. Merad M, Manz MG. Dendritic cell homeostasis. Blood. 2009;113:3418–27.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  64. Nestle FO, Di Meglio P, Qin J-Z, Nickoloff BJ. Skin immune sentinels in health and disease. Nat Rev Immunol. 2009;9:679–91.

    PubMed  PubMed Central  CAS  Google Scholar 

  65. Nestle FO, Zheng XG, Thompson CB, Turka LA, Nickoloff BJ. Characterization of dermal dendritic cells obtained from normal human skin reveals phenotypic and functionally distinctive subsets. J Immunol. 1993;151:6535–45.

    PubMed  CAS  Google Scholar 

  66. Zaba LC, Fuentes-Duculan J, Eungdamrong NJ, Abello MV, Novitskaya I, Pierson KC, et al. Psoriasis is characterized by accumulation of immunostimulatory and Th1/Th17 cell-polarizing myeloid dendritic cells. J Invest Dermatol. 2009;129:79–88.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  67. Klechevsky E, Morita R, Liu M, Cao Y, Coquery S, Thompson-Snipes L, Briere F, Chaussabel D, Zurawski G, Palucka AK, et al. Functional specializations of human epidermal Langerhans cells and CD14+ dermal dendritic cells. Immunity. 2008;29:497–510.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  68. Chu C-C, Ali N, Karagiannis P, Di Meglio P, Skowera A, Napolitano L, Barinaga G, Grys K, Sharif-Paghaleh E, Karagiannis SN, Peakman M, Lombardi G, Nestle FO. Resident CD141 (BDCA3) + dendritic cells in human skin produce IL-10 and induce regulatory T cells that suppress skin inflammation. J Exp Med. 2012;209:935–94.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  69. Jongbloed SL, Lebre MC, Fraser AR, Gracie JA, Sturrock RD, Tak PP, McInnes IB. Enumeration and phenotypical analysis of distinct dendritic cell subsets in psoriatic arthritis and rheumatoid arthritis. Arthritis Res Ther. 2006;8:R15.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  70. Gaston JS, Jarvis LB, Zhang L, Goodall JC. Dendritic cell: T-cell interactions in spondyloarthritis. Adv Exp Med Biol. 2009;649:263–76.

    Article  PubMed  CAS  Google Scholar 

  71. McGonagle D, Gibbon W, O’Connor P, et al. Characteristic magnetic resonance imaging entheseal changes in knee synovitis in spondylarthropathy. Arthritis Rheum. 1998;41:694–700.

    Article  PubMed  CAS  Google Scholar 

  72. Benjamin M, Mcgonagle D. Histopathologic changes at “synovio–entheseal complexes” suggesting a novel mechanism for synovitis in osteoarthritis and spondylarthritis. Arthritis Rheum. 2007;56:3601–9.

    Article  PubMed  Google Scholar 

  73. Cua DJ, Tato CM. Innate IL-17-producing cells: the sentinels of the immune system. Nat Rev Immunol. 2010;10:479–89.

    Article  PubMed  CAS  Google Scholar 

  74. Benjamin M, Mcgonagle D. The anatomical basis for disease localisation in seronegative spondyloarthropathy at entheses and related sites. J Anat. 2001;199:503–26.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  75. Laloux L, Voisin MC, Allain J, Martin N, Kerboull L, Chevalier X, Claudepierre P. Immunohistological study of entheses in spondyloarthropathies: comparison in rheumatoid arthritis and osteoarthritis. Ann Rheum Dis. 2001;60:316–21.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  76. McGonagle D, Marzo-Ortega H, O’Connor P, Gibbon W, Hawkey P, Henshaw K, Emery P. Histological assessment of the early enthesitis lesion in spondyloarthropathy. Ann Rheum Dis. 2002;61:534–7.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgements

Many thanks to my colleague Professor Leonie Taams, CMCBI, Kings College London, for critical review of this work.

Author information

Authors and Affiliations

  1. Department of Rheumatology, Guy’s & St Thomas’ NHS Foundation Trust, Guy’s Hospital, Great Maze Pond, London, SE1 9RT, UK

    Bruce Kirkham BA, MD, FRACP, FRCP

Authors
  1. Bruce Kirkham BA, MD, FRACP, FRCP
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bruce Kirkham BA, MD, FRACP, FRCP .

Editor information

Editors and Affiliations

  1. Faculty of Medicine, University of Sheffield, Sheffield, United Kingdom

    Adewale Adebajo

  2. Faculty of Medicine, University of Geneva, Geneva 14, Switzerland

    Wolf-Henning Boehncke

  3. Toronto Western Hospital, Toronto, Ontario, Canada

    Dafna D. Gladman

  4. Seattle Rheumatology Associates, Seattle, Washington, USA

    Philip J. Mease

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Kirkham, B. (2016). Innate and Acquired Cellular Immune Responses in Psoriasis and Psoriatic Arthritis. In: Adebajo, A., Boehncke, WH., Gladman, D., Mease, P. (eds) Psoriatic Arthritis and Psoriasis. Springer, Cham. https://doi.org/10.1007/978-3-319-19530-8_8

Download citation

  • DOI: https://doi.org/10.1007/978-3-319-19530-8_8

  • Published:

  • Publisher Name: Springer, Cham

  • Print ISBN: 978-3-319-19529-2

  • Online ISBN: 978-3-319-19530-8

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics

Search

Navigation