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Clinical Review

Th17 cells: A new paradigm for cutaneous inflammation

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Pages 259-266 | Received 23 Apr 2008, Accepted 24 Apr 2008, Published online: 12 Jul 2009

References

  • Steinman L. A brief history of T(H)17, the first major revision in the T(H)1/T(H)2 hypothesis of T cell‐mediated tissue damage. Nat Med 2007; 13: 139–45
  • Coffman R. L., Carty J. A T cell activity that enhances polyclonal IgE production and its inhibition by interferon‐gamma. J Immunol 1986; 136: 949–54
  • Mosmann T. R., Cherwinski H., Bond M. W., Giedlin M. A., Coffman R. L. Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. J Immunol 1986; 136: 2348–57
  • Stockinger B., Veldhoen M. Differentiation and function of Th17 T cells. Curr Opin Immunol 2007; 19: 281–6
  • Harrington L. E., Mangan P. R., Weaver C. T. Expanding the effector CD4 T‐cell repertoire: The Th17 lineage. Curr Opin Immunol 2006; 18: 349–56
  • Weaver C. T., Harrington L. E., Mangan P. R., Gavrieli M., Murphy K. M. Th17: An effector CD4 T cell lineage with regulatory T cell ties. Immunity 2006; 24: 677–88
  • Bettelli E., Carrier Y., Gao W., Korn T., Strom T. B., Oukka M., et al. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 2006; 441: 235–8
  • Oppmann B., Lesley R., Blom B., Timans J. C., Xu Y., Hunte B., et al. Novel p19 protein engages IL‐12p40 to form a cytokine, IL‐23, with biological activities similar as well as distinct from IL‐12. Immunity 2000; 13: 715–25
  • Parham C., Chirica M., Timans J., Vaisberg E., Travis M., Cheung J., et al. A receptor for the heterodimeric cytokine IL‐23 is composed of IL‐12Rbeta1 and a novel cytokine receptor subunit, IL‐23R. J Immunol 2002; 168: 5699–708
  • Murphy C. A., Langrish C. L., Chen Y., Blumenschein W., McClanahan T., Kastelein R. A., et al. Divergent pro‐ and antiinflammatory roles for IL‐23 and IL‐12 in joint autoimmune inflammation. J Exp Med 2003; 198: 1951–7
  • Langrish C. L., Chen Y., Blumenschein W. M., Mattson J., Basham B., Sedgwick J. D., et al. IL‐23 drives a pathogenic T cell population that induces autoimmune inflammation. J Exp Med 2005; 201: 233–40
  • Langrish C. L., McKenzie B. S., Wilson N. J., de Waal Malefyt R., Kastelein R. A., Cua D. J. IL‐12 and IL‐23: Master regulators of innate and adaptive immunity. Immunol Rev 2004; 202: 96–105
  • Chen Y., Langrish C. L., McKenzie B., Joyce‐Shaikh B., Stumhofer J. S., McClanahan T., et al. Anti‐IL‐23 therapy inhibits multiple inflammatory pathways and ameliorates autoimmune encephalomyelitis. J Clin Invest 2006; 116: 1317–26
  • Kastelein R. A., Hunter C. A., Cua D. J. Discovery and biology of IL‐23 and IL‐27: Related but functionally distinct regulators of inflammation. Ann Rev Immunol 2007; 25: 221–42
  • Park H., Li Z., Yang X. O., Chang S. H., Nurieva R., Wang Y‐H., et al. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol 2005; 6: 1133–41, [see comment]
  • Mangan P. R., Harrington L. E., O'Quinn D. B., Helms W. S., Bullard D. C., Elson C. O., et al. Transforming growth factor‐beta induces development of the T(H)17 lineage. Nature 2006; 441: 231–4, [see comment]
  • McKenzie B. S., Kastelein R. A., Cua D. J. Understanding the IL‐23‐IL‐17 immune pathway. Trends Immunol 2006; 27: 17–23
  • Sabat R., Philipp S., Hoflich C., Kreutzer S., Wallace E., Asadullah K., et al. Immunopathogenesis of psoriasis. Exp Dermatol 2007; 16: 779–98
  • Ghoreschi K., Weigert C., Rocken M. Immunopathogenesis and role of T cells in psoriasis. Clin Dermatol 2007; 25: 574–80
  • Fitch E., Harper E., Skorcheva I., Kurtz S. E., Blauvelt A. Pathophysiology of psoriasis: Recent advances on IL‐23 and Th17 cytokines. Curr Rheumatol Rep 2007; 9: 461–7
  • Zheng Y., Danilenko D. M., Valdez P., Kasman I., Eastham‐Anderson J., Wu J., et al. Interleukin‐22, a T(H)17 cytokine, mediates IL‐23‐induced dermal inflammation and acanthosis. Nature 2007; 445: 648–51
  • Veldhoen M., Hocking R. J., Atkins C. J., Locksley R. M., Stockinger B. TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL‐17‐producing T cells. Immunity 2006; 24: 179–89
  • Hoeve M. A., Savage N. D. L., de Boer T., Langenberg D. M. L., de Waal Malefyt R., Ottenhoff T. H. M., et al. Divergent effects of IL‐12 and IL‐23 on the production of IL‐17 by human T cells. Eur J Immunol 2006; 36: 661–70
  • Paradowska A., Maslinski W., Grzybowska‐Kowalczyk A., Lacki J. The function of interleukin 17 in the pathogenesis of rheumatoid arthritis. Arch Immunol Ther Exp (Warsz) 2007; 55: 329–34
  • Kikly K., Liu L., Na S., Sedgwick J. D. The IL‐23/Th(17) axis: Therapeutic targets for autoimmune inflammation. Curr Opin Immunol 2006; 18: 670–5
  • Zhang Z., Hinrichs D. J., Lu H., Chen H., Zhong W., Kolls J. K. After interleukin‐12p40, are interleukin‐23 and interleukin‐17 the next therapeutic targets for inflammatory bowel disease?. Int Immunopharmacol 2007; 7: 409–16
  • Matusevicius D., Kivisakk P., He B., Kostulas N., Ozenci V., Fredrikson S., et al. Interleukin‐17 mRNA expression in blood and CSF mononuclear cells is augmented in multiple sclerosis. Mult Scler 1999; 5: 101–4
  • Teunissen M. B., Koomen C. W., de Waal Malefyt R., Wierenga E. A., Bos J. D. Interleukin‐17 and interferon‐gamma synergize in the enhancement of proinflammatory cytokine production by human keratinocytes. J Invest Dermatol 1998; 111: 645–9
  • Van Beelen A. J., Teunissen M. B., Kapsenberg M. L., de Jong E. C. Interleukin‐17 in inflammatory skin disorders. Curr Opin Allergy Clin Immunol 2007; 7: 374–81
  • Liang S. C., Tan X‐Y., Luxenberg D. P., Karim R., Dunussi‐Joannopoulos K., Collins M., et al. Interleukin (IL)‐22 and IL‐17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides. J Exp Med 2006; 203: 2271–9
  • Ma H. L., Liang S., Li J., Napierata L., Brown T., Benoit S., et al. IL‐22 is required for Th17 cell‐mediated pathology in a mouse model of psoriasis‐like skin inflammation. J Clin Invest 2008; 118: 597–607
  • Krueger G. G., Langley R. G., Leonardi C., Yeilding N., Guzzo C., Wang Y., et al. A human interleukin‐12/23 monoclonal antibody for the treatment of psoriasis. N Engl J Med 2007; 356: 580–92
  • Toichi E., Torres G., McCormick T. S., Chang T., Mascelli M. A., Kauffman C. L., et al. An anti‐IL‐12p40 antibody down‐regulates type 1 cytokines, chemokines, and IL‐12/IL‐23 in psoriasis. J Immunol 2006; 177: 4917–26
  • Gottlieb A. B., Cooper K. D., McCormick T. S., Toichi E., Everitt D. E., Frederick B., et al. A phase 1, double‐blind, placebo‐controlled study evaluating single subcutaneous administrations of a human interleukin‐12/23 monoclonal antibody in subjects with plaque psoriasis. Curr Med Res Opin 2007; 23: 1081–92
  • Kimball A. B., Gordon K. B., Langley R. G., Menter A., Chartash E. K., Valdes J. Safety and efficacy of ABT‐874, a fully human interleukin 12/23 monoclonal antibody, in the treatment of moderate to severe chronic plaque psoriasis: Results of a randomized, placebo‐controlled, phase 2 trial. Arch Dermatol 2008; 144: 200–7
  • Papp K. A., Langley R. G., Lebwohl M., Krueger G. G., Szapary P., Yeilding N., et al. Efficacy and safety of ustekinumab, a human interleukin‐12/23 monoclonal antibody, in patients with psoriasis: 52‐week results from a randomised, double‐blind, placebo‐controlled trial (PHOENIX 2). Lancet. 2008; 371: 1675–84
  • Constantinescu C. S., Tani M., Ransohoff R. M., Wysocka M., Hilliard B., Fujioka T., et al. Astrocytes as antigen‐presenting cells: Expression of IL‐12/IL‐23. J Neurochem 2005; 95: 331–40
  • Thakker P., Leach M. W., Kuang W., Benoit S. E., Leonard J. P., Marusic S. IL‐23 is critical in the induction but not in the effector phase of experimental autoimmune encephalomyelitis. J Immunol 2007; 178: 2589–98
  • Deshpande P., King I. L., Segal B. M. Cutting edge: CNS CD11c+ cells from mice with encephalomyelitis polarize Th17 cells and support CD25+CD4+ T cell‐mediated immunosuppression, suggesting dual roles in the disease process. J Immunol 2007; 178: 6695–9
  • Wynn T. A. T(H)‐17: A giant step from T(H)1 and T(H)2 [comment]. Nat Immunol 2005; 6: 1069–70
  • Harrington L. E., Hatton R. D., Mangan P. R., Turner H., Murphy T. L., Murphy K. M., et al. Interleukin 17‐producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat Immunol 2005; 6: 1123–32
  • Weaver C. T., Hatton R. D., Mangan P. R., Harrington L. E. IL‐17 family cytokines and the expanding diversity of effector T cell lineages. Ann Rev Immunol 2007; 25: 821–52
  • Knauer J., Siegemund S., Muller U., Al‐Robaiy S., Kastelein R. A., Alber G., et al. Borrelia burgdorferi potently activates bone marrow‐derived conventional dendritic cells for production of IL‐23 required for IL‐17 release by T cells. FEMS Immunol Med Microbiol 2007; 49: 353–63
  • Burchill M. A., Nardelli D. T., England D. M., DeCoster D. J., Christopherson J. A., Callister S. M., et al. Inhibition of interleukin‐17 prevents the development of arthritis in vaccinated mice challenged with Borrelia burgdorferi. Infect Immun 2003; 71: 3437–42
  • Nakae S., Nambu A., Sudo K., Iwakura Y. Suppression of immune induction of collagen‐induced arthritis in IL‐17‐deficient mice. J Immunol 2003; 171: 6173–7
  • Bush K. A., Farmer K. M., Walker J. S., Kirkham B. W. Reduction of joint inflammation and bone erosion in rat adjuvant arthritis by treatment with interleukin‐17 receptor IgG1 Fc fusion protein. Arthritis Rheum 2002; 46: 802–5
  • Vaknin‐Dembinsky A., Balashov K., Weiner H. L. IL‐23 is increased in dendritic cells in multiple sclerosis and down‐regulation of IL‐23 by antisense oligos increases dendritic cell IL‐10 production. J Immunol 2006; 176: 7768–74, [erratum appears in J Immunol. 2006;177:2025]
  • McGovern D., Powrie F. The IL23 axis plays a key role in the pathogenesis of IBD. Gut 2007; 56: 1333–6
  • Wong C. K., Ho C. Y., Li E. K., Lam C. W. Elevation of proinflammatory cytokine (IL‐18, IL‐17, IL‐12) and Th2 cytokine (IL‐4) concentrations in patients with systemic lupus erythematosus. Lupus 2000; 9: 589–93
  • Siciliano N. A., Skinner J. A., Yuk M. H. Bordetella bronchiseptica modulates macrophage phenotype leading to the inhibition of CD4+ T cell proliferation and the initiation of a Th17 immune response. J Immunol 2006; 177: 7131–8
  • Bettelli E., Korn T., Kuchroo V. K. Th17: The third member of the effector T cell trilogy. Curr Opin Immunol 2007; 19: 652–7
  • McGeachy M. J., Cua D. J. T cells doing it for themselves: TGF‐beta regulation of Th1 and Th17 cells. Immunity 2007; 26: 547–9
  • Grossman R. M., Krueger J., Yourish D., Granelli‐Piperno A., Murphy D. P., May L. T., et al. Interleukin 6 is expressed in high levels in psoriatic skin and stimulates proliferation of cultured human keratinocytes. Proc Natl Acad Sci U S A 1989; 86: 6367–71
  • Miranda‐Carus M. E., Benito‐Miguel M., Llamas M. A., Balsa A., Martin‐Mola E. Human T cells constitutively express IL‐15 that promotes ex vivo T cell homeostatic proliferation through autocrine/juxtacrine loops. J Immunol 2005; 175: 3656–62
  • Zaba L. C., Cardinale I., Gilleaudeau P., Sullivan‐Whalen M., Suarez Farinas M., Fuentes‐Duculan J., et al. Amelioration of epidermal hyperplasia by TNF inhibition is associated with reduced Th17 responses. J Exp Med 2007; 204: 3183–94
  • Gottlieb A. B., Chamian F., Masud S., Cardinale I., Abello M. V., Lowes M. A., et al. TNF inhibition rapidly down‐regulates multiple proinflammatory pathways in psoriasis plaques. J Immunol 2005; 175: 2721–9
  • Jovanovic D. V., Di Battista J. A., Martel‐Pelletier J., Jolicoeur F. C., He Y., Zhang M., et al. IL‐17 stimulates the production and expression of proinflammatory cytokines, IL‐beta and TNF‐alpha, by human macrophages. J Immunol 1998; 160: 3513–21
  • Iwamoto S., Iwai S., Tsujiyama K., Kurahashi C., Takeshita K., Naoe M., et al. TNF‐alpha drives human CD14+ monocytes to differentiate into CD70+ dendritic cells evoking Th1 and Th17 responses. J Immunol 2007; 179: 1449–57
  • Sabat R., Sterry W., Philipp S., Wolk K. Three decades of psoriasis research: Where has it led us?. Clin Dermatol 2007; 25: 504–9
  • Wolk K., Kunz S., Witte E., Friedrich M., Asadullah K., Sabat R. IL‐22 increases the innate immunity of tissues. Immunity 2004; 21: 241–54
  • Chung Y., Yang X., Chang S. H., Ma L., Tian Q., Dong C. Expression and regulation of IL‐22 in the IL‐17‐producing CD4+ T lymphocytes. Cell Res 2006; 16: 902–7
  • Aggarwal S., Ghilardi N., Xie M‐H., de Sauvage F. J., Gurney A. L. Interleukin‐23 promotes a distinct CD4 T cell activation state characterized by the production of interleukin‐17. J Biol Chem 2003; 278: 1910–14
  • Wilson N. J., Boniface K., Chan J. R., McKenzie B. S., Blumenschein W. M., Mattson J. D., et al. Development, cytokine profile and function of human interleukin 17‐producing helper T cells. Nat Immunol 2007; 8: 950–7
  • Veldhoen M., Stockinger B. TGFbeta1, a ‘Jack of all trades’: The link with pro‐inflammatory IL‐17‐producing T cells. Trends Immunol 2006; 27: 358–61
  • Toda M., Leung D. Y., Molet S., Boguniewicz M., Taha R., Christodoulopoulos P., et al. Polarized in vivo expression of IL‐11 and IL‐17 between acute and chronic skin lesions. J Allergy Clin Immunol 2003; 111: 875–81
  • Li A. G., Wang D., Feng X. H., Wang X. J. Latent TGFbeta1 overexpression in keratinocytes results in a severe psoriasis‐like skin disorder. EMBO J 2004; 23: 1770–81
  • Baran W., Szepietowski J. C., Mazur G., Baran E. TGF‐beta(1) gene polymorphism in psoriasis vulgaris. Cytokine 2007; 38: 8–11
  • Nockowski P., Szepietowski J. C., Ziarkiewicz M., Baran E. Serum concentrations of transforming growth factor beta 1 in patients with psoriasis vulgaris. Acta Dermatovenerol Croat 2004; 12: 2–6
  • Engelhart K., El Hindi T., Biesalski H. K., Pfitzner I. In vitro reproduction of clinical hallmarks of eczematous dermatitis in organotypic skin models. Arch Dermatol Res 2005; 297: 1–9
  • Spiekstra S. W., Breetveld M., Rustemeyer T., Scheper R. J., Gibbs S. Wound‐healing factors secreted by epidermal keratinocytes and dermal fibroblasts in skin substitutes. Wound Repair Regen 2007; 15: 708–17
  • Elder J. T. IL‐15 and psoriasis: Another genetic link to Th17?. J Invest Dermatol 2007; 127: 2495–7
  • Zhang X. J., Yan K. L., Wang Z. M., Yang S., Zhang G. L., Fan X., et al. Polymorphisms in interleukin‐15 gene on chromosome 4q31.2 are associated with psoriasis vulgaris in Chinese population. J Invest Dermatol 2007; 127: 2544–51
  • Ong P. Y., Hamid Q. A., Travers J. B., Strickland I., Al Kerithy M., Boguniewicz M., et al. Decreased IL‐15 may contribute to elevated IgE and acute inflammation in atopic dermatitis. J Immunol 2002; 168: 505–10
  • Ruckert R., Brandt K., Bulanova E., Mirghomizadeh F., Paus R., Bulfone‐Paus S. Dendritic cell‐derived IL‐15 controls the induction of CD8 T cell immune responses. Eur J Immunol 2003; 33: 3493–503
  • Villadsen L. S., Schuurman J., Beurskens F., Dam T. N., Dagnaes‐Hansen F., Skov L., et al. Resolution of psoriasis upon blockade of IL‐15 biological activity in a xenograft mouse model. J Clin Invest 2003; 112: 1571–80
  • McInnes I. B. Cytokine targeting in psoriasis and psoriatic arthritis: Beyond TNFalpha. Ernst Schering Res Found Workshop 2006, 29–44
  • McInnes I. B., Gracie J. A. Interleukin‐15: A new cytokine target for the treatment of inflammatory diseases. Curr Opin Pharmacol 2004; 4: 392–7
  • Chan J. R., Blumenschein W., Murphy E., Diveu C., Wiekowski M., Abbondanzo S., et al. IL‐23 stimulates epidermal hyperplasia via TNF and IL‐20R2‐dependent mechanisms with implications for psoriasis pathogenesis. J Exp Med 2006; 203: 2577–87
  • Chen Z., Laurence A., O'Shea J. J. Signal transduction pathways and transcriptional regulation in the control of Th17 differentiation. Semin Immunol 2007; 19: 400–8
  • Kopp T., Lenz P., Bello‐Fernandez C., Kastelein R. A., Kupper T. S., Stingl G. IL‐23 production by cosecretion of endogenous p19 and transgenic p40 in keratin 14/p40 transgenic mice: Evidence for enhanced cutaneous immunity. J Immunol 2003; 170: 5438–44
  • Lee E., Trepicchio W. L., Oestreicher J. L., Pittman D., Wang F., Chamian F., et al. Increased expression of interleukin 23 p19 and p40 in lesional skin of patients with psoriasis vulgaris. J Exp Med 2004; 199: 125–30
  • Piskin G., Sylva‐Steenland R. M., Bos J. D., Teunissen M. B. In vitro and in situ expression of IL‐23 by keratinocytes in healthy skin and psoriasis lesions: Enhanced expression in psoriatic skin. J Immunol 2006; 176: 1908–15
  • Chen X., Tan Z., Yue Q., Liu H., Liu Z., Li J. The expression of interleukin‐23 (p19/p40) and inteleukin‐12 (p35/p40) in psoriasis skin. J Huazhong Univ Sci Technolog Med Sci 2006; 26: 750–2
  • Liang S. C., Tan X. Y., Luxenberg D. P., Karim R., Dunussi‐Joannopoulos K., Collins M., et al. Interleukin (IL)‐22 and IL‐17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides. J Exp Med 2006; 203: 2271–9
  • Wolk K., Witte E., Wallace E., Docke W‐D., Kunz S., Asadullah K., et al. IL‐22 regulates the expression of genes responsible for antimicrobial defense, cellular differentiation, and mobility in keratinocytes: A potential role in psoriasis. Eur J Immunol 2006; 36: 1309–23
  • Infante‐Duarte C., Horton H. F., Byrne M. C., Kamradt T. Microbial lipopeptides induce the production of IL‐17 in Th cells. J Immunol 2000; 165: 6107–15
  • Aggarwal S., Gurney A. L. IL‐17: Prototype member of an emerging cytokine family. J Leukoc Biol 2002; 71: 1–8
  • Albanesi C., Cavani A., Girolomoni G. IL‐17 is produced by nickel‐specific T lymphocytes and regulates ICAM‐1 expression and chemokine production in human keratinocytes: Synergistic or antagonist effects with IFN‐gamma and TNF‐alpha. J Immunol 1999; 162: 494–502
  • Albanesi C., Scarponi C., Cavani A., Federici M., Nasorri F., Girolomoni G. Interleukin‐17 is produced by both Th1 and Th2 lymphocytes, and modulates interferon‐gamma‐ and interleukin‐4‐induced activation of human keratinocytes. J Invest Dermatol 2000; 115: 81–7
  • Boniface K., Bernard F. X., Garcia M., Gurney A. L., Lecron J. C., Morel F. IL‐22 inhibits epidermal differentiation and induces proinflammatory gene expression and migration of human keratinocytes. J Immunol 2005; 174: 3695–702

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