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PMID: 14678257 Published · ppublish English Journal Article Review

Immunopathogenic mechanisms in psoriasis.

Clinical and experimental immunology ·Vol. 135 ·No. 1 ·2004-01-00 ·Pages 1-8

Gudjonsson JE, Johnston A, Sigmundsdottir H, Valdimarsson H

Abstract

Psoriasis is a common autoimmune skin disease characterized by T cell-mediated hyperproliferation of keratinocytes. The disease has a strong but complex genetic background with a concordance of approximately 60% in monozygotic twins, and recent linkage and high resolution association studies indicate that HLA-Cw*0602 is itself a major susceptibility allele for psoriasis. Patients carrying this allele have been shown to have different clinical features and earlier age of disease onset, and patients homozygous for this allele have about 2.5 times higher disease risk than heterozygotes. Published data indicate that CD8+ T cells may play a major effector role in psoriasis. Epidermal infiltration of predominantly oligoclonal CD8+ T cells, and probably also of CD4+ T cells in the dermis, is a striking feature of chronic psoriasis lesions, indicating that these cells are responding to specific antigens. We argue that CD4+ T cells are essential for initiating and maintaining the pathogenic process of psoriasis but that cross-primed CD8+ T cells are the main effector cells responding to antigens in the HLA-Cw*0602 binding pocket of keratinocytes. It is further proposed that CD8+ T cells are involved in the control of the Th1 polarization, which is observed in psoriasis lesions, through a complex interplay between CD4+, CD8+ T cells and cross-presenting dendritic cells. It is also suggested that spontaneous remissions or fluctuations in disease activity may be determined by a balance within the lesions between effector and suppressor CD4+ and CD8+ T cells.

MeSH Terms
Autoimmune Diseases/immunology CD8-Positive T-Lymphocytes/immunology Cross-Priming/immunology Cytokines/immunology HLA-C Antigens/immunology Humans Psoriasis/immunology T-Lymphocyte Subsets/immunology Th1 Cells/immunology
Chemicals
Cytokines HLA-C Antigens HLA-C*06 antigen
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Gudjonsson J E
Department of Immunology, Landspitali University Hospital, University of Iceland, Reykjavik, Iceland.
Johnston A
Sigmundsdottir H
Valdimarsson H
References (102)
102 references, click to expand
  1. Interleukin 20: discovery, receptor identification, and role in epidermal function.
    Cell. 2001 Jan 12;104(1):9-19 PMID: 11163236
  2. Cross-priming for a secondary cytotoxic response to minor H antigens with H-2 congenic cells which do not cross-react in the cytotoxic assay.
    J Exp Med. 1976 May 1;143(5):1283-8 PMID: 1083422
  3. Keratinocytes derived from psoriatic plaques are resistant to apoptosis compared with normal skin.
    Am J Pathol. 1997 Nov;151(5):1321-9 PMID: 9358758
  4. Oligoclonal expansion of intraepidermal T cells in psoriasis skin lesions.
    J Invest Dermatol. 2001 Dec;117(6):1546-53 PMID: 11886521
  5. Cyclosporin A for psoriasis.
    N Engl J Med. 1979 Sep 6;301(10):555 PMID: 460314
  6. Psoriasis: maintenance of an intact monolayer basal cell differentiation compartment in spite of hyperproliferation.
    Br J Dermatol. 1985 Jul;113(1):53-64 PMID: 2410005
  7. Circulating T cells of patients with active psoriasis respond to streptococcal M-peptides sharing sequences with human epidermal keratins.
    Scand J Immunol. 1997 Jun;45(6):688-97 PMID: 9201310
  8. Interleukin (IL)-15 and IL-7 jointly regulate homeostatic proliferation of memory phenotype CD8+ cells but are not required for memory phenotype CD4+ cells.
    J Exp Med. 2002 Jun 17;195(12):1523-32 PMID: 12070280
  9. Immunocompetent cells in psoriasis. In situ immunophenotyping by monoclonal antibodies.
    Arch Dermatol Res. 1983;275(3):181-9 PMID: 6604503
  10. Clinical improvement of HIV-associated psoriasis parallels a reduction of HIV viral load induced by effective antiretroviral therapy.
    AIDS. 1999 Apr 1;13(5):628-9 PMID: 10203394
  11. IL-1 beta and IFN-gamma induce the regenerative epidermal phenotype of psoriasis in the transwell skin organ culture system. IFN-gamma up-regulates the expression of keratin 17 and keratinocyte transglutaminase via endogenous IL-1 production.
    J Pathol. 1999 Feb;187(3):358-64 PMID: 10398092
  12. Family-based analysis using a dense single-nucleotide polymorphism-based map defines genetic variation at PSORS1, the major psoriasis-susceptibility locus.
    Am J Hum Genet. 2002 Sep;71(3):554-64 PMID: 12148091
  13. Macrophages and dendritic cells use the cytosolic pathway to rapidly cross-present antigen from live, vaccinia-infected cells.
    J Immunol. 2002 Dec 15;169(12):6733-42 PMID: 12471104
  14. Epidermal T lymphocytes and dendritic cells in chronic plaque psoriasis: the effects of PUVA treatment.
    Clin Exp Immunol. 1985 Sep;61(3):526-34 PMID: 3878241
  15. The role of streptococcal infection in the initiation of guttate psoriasis.
    Arch Dermatol. 1992 Jan;128(1):39-42 PMID: 1739285
  16. Psoriasis in monozygotic twins: variations in expression in individuals with identical genetic constitution.
    Acta Derm Venereol. 1982;62(3):229-36 PMID: 6179364
  17. Epidermal CD8+ T cells reactive with group A streptococcal antigens in chronic plaque psoriasis.
    Exp Dermatol. 2002 Aug;11(4):357-64 PMID: 12190945
  18. Regulatory CD4+CD25+ T cells restrict memory CD8+ T cell responses.
    J Exp Med. 2002 Dec 16;196(12):1585-92 PMID: 12486101
  19. Blockade of T lymphocyte costimulation with cytotoxic T lymphocyte-associated antigen 4-immunoglobulin (CTLA4Ig) reverses the cellular pathology of psoriatic plaques, including the activation of keratinocytes, dendritic cells, and endothelial cells.
    J Exp Med. 2000 Sep 4;192(5):681-94 PMID: 10974034
  20. The development of manifest psoriatic lesions is linked with the invasion of CD8 + T cells and CD11c + macrophages into the epidermis.
    Arch Dermatol Res. 1992;284(7):375-9 PMID: 1363190
  21. Cytotoxic T lymphocytes show HLA-C-restricted recognition of EBV-bearing cells and allorecognition of HLA class I molecules presenting self-peptides.
    J Immunol. 1992 Oct 1;149(7):2406-14 PMID: 1326579
  22. Keratinocytes and cytokines.
    Vet Immunol Immunopathol. 2002 Sep 6;88(1-2):1-12 PMID: 12088639
  23. Psoriasis.
    Br J Dermatol. 1988 Oct;119(4):445-61 PMID: 3056491
  24. Cross-presentation: a general mechanism for CTL immunity and tolerance.
    Immunol Today. 1998 Aug;19(8):368-73 PMID: 9709505
  25. Overexpression of interleukin (IL)-7 leads to IL-15-independent generation of memory phenotype CD8+ T cells.
    J Exp Med. 2002 Jun 17;195(12):1533-9 PMID: 12070281
  26. Clearance of psoriasis with low dose cyclosporin.
    Br Med J (Clin Res Ed). 1986 Sep 20;293(6549):731-2 PMID: 3094629
  27. Tonsillitis and chronic psoriasis.
    Clin Otolaryngol Allied Sci. 1998 Feb;23(1):67-8 PMID: 9563669
  28. Linkage analysis of human leukocyte antigen (HLA) markers in familial psoriasis: strong disequilibrium effects provide evidence for a major determinant in the HLA-B/-C region.
    Am J Hum Genet. 1998 Jul;63(1):191-9 PMID: 9634500
  29. A role for tonsillectomy in the treatment of psoriasis?
    Ear Nose Throat J. 1999 Mar;78(3):155-8 PMID: 10188351
  30. [Efficacy of tonsillectomy on psoriasis and tonsil histology].
    Nihon Jibiinkoka Gakkai Kaiho. 2001 Nov;104(11):1065-70 PMID: 11766391
  31. Cytokines in skin lesions of psoriasis.
    Cytokine. 1990 Jan;2(1):68-75 PMID: 2104215
  32. Help for cytotoxic-T-cell responses is mediated by CD40 signalling.
    Nature. 1998 Jun 4;393(6684):478-80 PMID: 9624004
  33. Treatment of psoriasis with the chimeric monoclonal antibody against tumor necrosis factor alpha, infliximab.
    J Am Acad Dermatol. 2002 Jun;46(6):886-91 PMID: 12063486
  34. Psoriasis and human immunodeficiency virus infection.
    J Am Acad Dermatol. 1992 Nov;27(5 Pt 1):667-73 PMID: 1430384
  35. Clones of human cytotoxic T lymphocytes derived from an allosensitized individual: HLA specificity and cell surface markers.
    Scand J Immunol. 1981 Sep;14(3):213-24 PMID: 6173916
  36. Autologous cytolytic T lymphocytes recognize a MAGE-1 nonapeptide on melanomas expressing HLA-Cw*1601.
    Eur J Immunol. 1994 Sep;24(9):2134-40 PMID: 7522162
  37. Intracellular reservoir of Streptococcus pyogenes in vivo: a possible explanation for recurrent pharyngotonsillitis.
    Laryngoscope. 1997 May;107(5):640-7 PMID: 9149167
  38. Group A streptococci efficiently invade human respiratory epithelial cells.
    Proc Natl Acad Sci U S A. 1994 Dec 6;91(25):12115-9 PMID: 7991594
  39. Interleukin-17 and interferon-gamma synergize in the enhancement of proinflammatory cytokine production by human keratinocytes.
    J Invest Dermatol. 1998 Oct;111(4):645-9 PMID: 9764847
  40. On the existence of non-cycling germinative cells in human epidermis in vivo and cell cycle aspects of psoriasis.
    Cell Tissue Kinet. 1982 Jul;15(4):393-7 PMID: 7105130
  41. The wound repair-associated keratins 6, 16, and 17. Insights into the role of intermediate filaments in specifying keratinocyte cytoarchitecture.
    Subcell Biochem. 1998;31:173-204 PMID: 9932493
  42. Cross-reactivity between streptococcal M surface antigen and human skin.
    Br J Dermatol. 1991 Nov;125(5):443-7 PMID: 1721523
  43. A frameshift mutation in NOD2 associated with susceptibility to Crohn's disease.
    Nature. 2001 May 31;411(6837):603-6 PMID: 11385577
  44. CD8+ T cells in psoriatic lesions preferentially use T-cell receptor V beta 3 and/or V beta 13.1 genes.
    Proc Natl Acad Sci U S A. 1994 Sep 27;91(20):9282-6 PMID: 7937756
  45. Streptococcal throat infections and exacerbation of chronic plaque psoriasis: a prospective study.
    Br J Dermatol. 2003 Sep;149(3):530-4 PMID: 14510985
  46. Mechanisms for the induction of autoimmunity by infectious agents.
    J Clin Invest. 2001 Oct;108(8):1097-104 PMID: 11602615
  47. CD4(+) T cells are required for the development of cytotoxic CD8(+) T cells during Mycobacterium tuberculosis infection.
    J Immunol. 2001 Dec 15;167(12):6991-7000 PMID: 11739519
  48. Psoriasis regression in terminal AIDS.
    Lancet. 1992 May 2;339(8801):1110 PMID: 1349120
  49. Flow cytometric quantification of human epidermal cells expressing keratin 16 in vivo after standardized trauma.
    Arch Dermatol Res. 1990;282(2):126-30 PMID: 1693838
  50. T cell clones from psoriasis skin lesions can promote keratinocyte proliferation in vitro via secreted products.
    Eur J Immunol. 1994 Mar;24(3):593-8 PMID: 8125129
  51. HLA-G and NK receptor are expressed in psoriatic skin: a possible pathway for regulating infiltrating T cells?
    Am J Pathol. 2001 Jul;159(1):71-7 PMID: 11438456
  52. Localization of elevated transforming growth factor-alpha in psoriatic epidermis.
    J Invest Dermatol. 1990 Aug;95(2):229-32 PMID: 2380581
  53. Bacterial peptidoglycan and immune reactivity in the central nervous system in multiple sclerosis.
    Brain. 2001 Aug;124(Pt 8):1544-54 PMID: 11459746
  54. Psoriasis: a disease of abnormal Keratinocyte proliferation induced by T lymphocytes.
    Immunol Today. 1986 Sep;7(9):256-9 PMID: 25290627
  55. Intraepidermal lymphocytes in psoriatic lesions are activated GMP-17(TIA-1)+CD8+CD3+ CTLs as determined by phenotypic analysis.
    J Cutan Pathol. 1998 Feb;25(2):79-88 PMID: 9521496
  56. Role of NF-kappaB in the apoptotic-resistant phenotype of keratinocytes.
    J Biol Chem. 1999 Dec 31;274(53):37957-64 PMID: 10608863
  57. Dermatologic complications of HIV infection.
    Med Clin North Am. 1996 Nov;80(6):1415-35 PMID: 8941229
  58. The immunologic and genetic basis of psoriasis.
    Arch Dermatol. 1999 Sep;135(9):1104-10 PMID: 10490116
  59. Dendritic cells acquire antigens from live cells for cross-presentation to CTL.
    J Immunol. 2001 Mar 15;166(6):3717-23 PMID: 11238612
  60. Psoriasis: a T-cell-mediated autoimmune disease induced by streptococcal superantigens?
    Immunol Today. 1995 Mar;16(3):145-9 PMID: 7718088
  61. Cyclosporine improves psoriasis in a double-blind study.
    JAMA. 1986 Dec 12;256(22):3110-6 PMID: 3023712
  62. In vivo dynamics of T cell activation, proliferation, and death in HIV-1 infection: why are CD4+ but not CD8+ T cells depleted?
    Proc Natl Acad Sci U S A. 2002 Nov 26;99(24):15572-7 PMID: 12434018
  63. Anti-CD4 monoclonal antibody therapy in severe psoriasis.
    J Autoimmun. 1992 Aug;5(4):465-77 PMID: 1384529
  64. Constitutive class I-restricted exogenous presentation of self antigens in vivo.
    J Exp Med. 1996 Sep 1;184(3):923-30 PMID: 9064352
  65. HLA-Cw6-positive and HLA-Cw6-negative patients with Psoriasis vulgaris have distinct clinical features.
    J Invest Dermatol. 2002 Feb;118(2):362-5 PMID: 11841557
  66. HLA-C and guttate psoriasis.
    Br J Dermatol. 2000 Dec;143(6):1177-82 PMID: 11122018
  67. Cross-presentation, dendritic cells, tolerance and immunity.
    Annu Rev Immunol. 2001;19:47-64 PMID: 11244030
  68. Cell kinetic basis for pathophysiology of psoriasis.
    J Invest Dermatol. 1985 Dec;85(6):579-83 PMID: 4067329
  69. Complementary dendritic cell-activating function of CD8+ and CD4+ T cells: helper role of CD8+ T cells in the development of T helper type 1 responses.
    J Exp Med. 2002 Feb 18;195(4):473-83 PMID: 11854360
  70. Skin CD4+ T cells produce interferon-gamma in vitro in response to streptococcal antigens in chronic plaque psoriasis.
    J Invest Dermatol. 2000 Mar;114(3):576-80 PMID: 10692120
  71. Inhibition of keratinocyte apoptosis by IL-15: a new parameter in the pathogenesis of psoriasis?
    J Immunol. 2000 Aug 15;165(4):2240-50 PMID: 10925312
  72. Langerhans cells renew in the skin throughout life under steady-state conditions.
    Nat Immunol. 2002 Dec;3(12):1135-41 PMID: 12415265
  73. High-frequency intracellular invasion of epithelial cells by serotype M1 group A streptococci: M1 protein-mediated invasion and cytoskeletal rearrangements.
    Mol Microbiol. 1999 Feb;31(3):859-70 PMID: 10048029
  74. Efficiency of cross presentation of vaccinia virus-derived antigens by human dendritic cells.
    Eur J Immunol. 2001 Dec;31(12):3432-42 PMID: 11745362
  75. Effects of ultraviolet B radiation on human Langerhans cells: functional alteration of CD86 upregulation and induction of apoptotic cell death.
    J Invest Dermatol. 1998 Sep;111(3):373-9 PMID: 9740226
  76. Successful ultraviolet B treatment of psoriasis is accompanied by a reversal of keratinocyte pathology and by selective depletion of intraepidermal T cells.
    J Exp Med. 1995 Dec 1;182(6):2057-68 PMID: 7500051
  77. Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn's disease.
    Nature. 2001 May 31;411(6837):599-603 PMID: 11385576
  78. Autoreactive T cells in endocrine/organ-specific autoimmunity: why has progress been so slow?
    Springer Semin Immunopathol. 2002 Dec;24(3):261-71 PMID: 12503054
  79. Dermal injection of immunocytes induces psoriasis.
    J Clin Invest. 1996 Oct 15;98(8):1878-87 PMID: 8878440
  80. Expression of interleukin-12 is increased in psoriatic skin.
    J Invest Dermatol. 1998 Dec;111(6):1053-7 PMID: 9856816
  81. Psoriatic arthritis.
    Curr Opin Rheumatol. 1992 Aug;4(4):470-8 PMID: 1503870
  82. Keratins (K16 and K17) as markers of keratinocyte hyperproliferation in psoriasis in vivo and in vitro.
    Br J Dermatol. 1995 Oct;133(4):501-11 PMID: 7577575
  83. Epidermal T lymphocytes and HLA-DR expression in psoriasis.
    Br J Dermatol. 1984 May;110(5):555-64 PMID: 6232938
  84. Is an epitope on keratin 17 a major target for autoreactive T lymphocytes in psoriasis?
    Clin Exp Immunol. 1999 Sep;117(3):580-6 PMID: 10469066
  85. Injection of pre-psoriatic skin with CD4+ T cells induces psoriasis.
    Am J Pathol. 1999 Jul;155(1):145-58 PMID: 10393847
  86. Cross-presentation of Listeria monocytogenes-derived CD4 T cell epitopes.
    J Immunol. 2002 Aug 1;169(3):1410-8 PMID: 12133966
  87. Treatment of chronic plaque psoriasis by selective targeting of memory effector T lymphocytes.
    N Engl J Med. 2001 Jul 26;345(4):248-55 PMID: 11474662
  88. Immunology of the tonsils.
    Immunol Today. 1998 Sep;19(9):414-21 PMID: 9745205
  89. CD8+ T suppressor cells are back to the game: are they players in autoimmunity?
    Autoimmun Rev. 2002 Oct;1(5):279-83 PMID: 12848981
  90. Role of antigen-presenting cells in cross-priming of cytotoxic T lymphocytes by apoptotic cells.
    J Leukoc Biol. 1999 Aug;66(2):247-51 PMID: 10449162
  91. Interleukin-12 alone can not enhance the expression of the cutaneous lymphocyte associated antigen (CLA) by superantigen-stimulated T lymphocytes.
    Clin Exp Immunol. 2003 Jun;132(3):430-5 PMID: 12780689
  92. Antigen presentation to CD8+ T cells: cross-priming in infectious diseases.
    Curr Opin Immunol. 2001 Aug;13(4):437-41 PMID: 11498299
  93. Evidence that HLA-Cw6 determines early onset of psoriasis, obtained using sequence-specific primers (PCR-SSP).
    Acta Derm Venereol. 1997 Jul;77(4):273-6 PMID: 9228217
  94. Immunohistochemical studies of infiltrating cells in early and chronic lesions of psoriasis.
    J Dermatol. 1994 Apr;21(4):223-32 PMID: 7914525
  95. Bacterial superantigens induce T cell expression of the skin-selective homing receptor, the cutaneous lymphocyte-associated antigen, via stimulation of interleukin 12 production.
    J Exp Med. 1995 Feb 1;181(2):747-53 PMID: 7836926
  96. Response of psoriasis to a lymphocyte-selective toxin (DAB389IL-2) suggests a primary immune, but not keratinocyte, pathogenic basis.
    Nat Med. 1995 May;1(5):442-7 PMID: 7585092
  97. Psoriasis: the plot thickens....
    Nat Immunol. 2001 Feb;2(2):91 PMID: 11175798
  98. Psoriasis induced at the injection site of recombinant interferon gamma. Results of immunohistologic investigations.
    Arch Dermatol. 1990 Mar;126(3):351-5 PMID: 2106838
  99. Dominant lesional T cell receptor rearrangements persist in relapsing psoriasis but are absent from nonlesional skin: evidence for a stable antigen-specific pathogenic T cell response in psoriasis vulgaris.
    J Invest Dermatol. 2001 Nov;117(5):1296-301 PMID: 11710947
  100. HLA-C revisited. Ten years of change.
    Immunol Res. 1997;16(2):203-14 PMID: 9212365
  101. IL-12 synergizes with IL-18 or IL-1beta for IFN-gamma production from human T cells.
    Int Immunol. 2000 Feb;12(2):151-60 PMID: 10653850
  102. Psoriasis patients who are homozygous for the HLA-Cw*0602 allele have a 2.5-fold increased risk of developing psoriasis compared with Cw6 heterozygotes.
    Br J Dermatol. 2003 Feb;148(2):233-5 PMID: 12588373
Article Info
Journal
Clinical and experimental immunology
Abbr.
Clin Exp Immunol
ISSN
0009-9104
Published
2004-01-00
Pages
1-8
Language
English
Region
England
NLM ID
0057202
PMCID
PMC1808928
Subset
IM
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