Origin, function and role in the development of skin diseases CLA+T-lymphocytes

Cover Page


Cite item

Full Text

Abstract

The idea of CLA+T-lymphocytes, which are a special subpopulation of cells with a tropic to the skin, is given. The issues of maturation, migration and functional features of CLA+T-cells are considered. Special attention is paid to the different phenotype of memory T-cells. Modern data concerning the role of CLA+T-cells in the pathogenesis of autoimmune and allergic dermatoses, as well as malignant skin tumors are also presented. The conclusion about the necessity of further study of CLA +T-lymphocytes for detailed understanding of pathogenesis and search of variants of targeted therapy in psoriasis, atopic dermatitis, skin lymphomas and other skin diseases is made.

About the authors

A. V. Patrushev

S. M. Kirov Militar y Medical Academy of the Ministr y of Defence of the Russian Federation

Author for correspondence.
Email: alexpat2@yandex.ru

Aleksandr V. Patrushev — Cand. Sci. (Medicine), Research Assistant, Department of Skin and Sexually Transmitted Diseases

Academician Lebedev str., 6, Saint Petersburg, 194044

Россия

A. V. Samtsov

S. M. Kirov Militar y Medical Academy of the Ministr y of Defence of the Russian Federation

Email: avsamtsov@mail.ru

Aleksey V. Samtsov — Dr. Sci. (Medicine), Prof., Departmental Head, Department of Skin and Sexually Transmitted Diseases

Academician Lebedev str., 6, Saint Petersburg, 194044

Россия

V. Yu. Nikitin

S. M. Kirov Militar y Medical Academy of the Ministr y of Defence of the Russian Federation

Email: vladimiryn@mail.ru

Vladimir Yu. Nikitin — Dr. Sci. (Medicine), Head of the Immunological Laboratory, Centre for Clinical Laboratory Diagnostics

Academician Lebedev str., 6, Saint Petersburg, 194044

Россия

A. М. Ivanov

S. M. Kirov Militar y Medical Academy of the Ministr y of Defence of the Russian Federation

Email: iamvma@mail.ru

Andrey M. Ivanov — Dr. Sci. (Medicine), Corresponding Member of the Russian Academy of Sciences, Prof., Head of the Department of Clinical Biochemistry and Laboratory Diagnostics, S. M. Kirov Military Medical Academy of the Ministry of Defence of the Russian Federation

Academician Lebedev str., 6, Saint Petersburg, 194044


Россия

O. Р. Gumilevskaya

S. M. Kirov Militar y Medical Academy of the Ministr y of Defence of the Russian Federation

Email: ogum@mail.ru

Oksana P. Gumilevskaya — Dr. Sci. (Medicine), Ass. Prof., Head of the Centre for Clinical Laboratory Diagnostics

Academician Lebedev str., 6, Saint Petersburg, 194044

Россия

A. V. Sukharev

S. M. Kirov Militar y Medical Academy of the Ministr y of Defence of the Russian Federation

Email: asoukharev@mail.ru

Aleksey V. Sukharev — Dr. Sci. (Medicine), Prof., Department of Skin and Sexually Transmitted Diseases

Academician Lebedev str., 6, Saint Petersburg, 194044

Россия

I. A. Sukhina

S. M. Kirov Militar y Medical Academy of the Ministr y of Defence of the Russian Federation

Email: kinya2000@mail.ru

Irina A. Sukhina — Cand. Sci. (Biology), Lecturer, Department of Clinical Biochemistry and Laboratory Diagnostics

Academician Lebedev str., 6, Saint Petersburg, 194044

Россия

References

  1. Hunger R. E., Yawalkar N., Braathen L. R., et al. The HECA-452 epitope is highly expressed on lymph cells derived from human skin. Br J Dermatol. 1999;141(3):565–569.
  2. Fuhlbrigge R. C., Kieffer J. D., Armerding D., et al. Cutaneous lymphocyte antigen is a specialized form of PSGL-1 expressed on skin-homing Tcells. Nature. 1997;389(6654):978–981.
  3. Picker L. J., Michie S. A., Rott L. S., et al. A Unique Phenotype of Skin-associated Lymphocytes in Humans. Am J Pathol. 1990;136(5):1053–1068.
  4. Rossiter H., van Reijsen F., Mudde G. C., et al. Skin disease-related T cells bind to endothelial selectins: expression of cutaneous lymphocyte antigen (CLA) predicts E-selectin but not P-selectin binding. Eur J Immunol. 1994;24(1):205–210.
  5. Santamaria Babi L. F., Perez Soler M. T., Hauser C., et al. Skin-homing T cells in human cutaneous allergic inflammation. Immunol Res. 1995;14(4):317–324.
  6. Pitzalis C., Cauli A., Pipitone N., et al. Cutaneous lymphocyte antigenpositive T lymphocytes preferentially migrate to the skin but not to the joint in psoriatic arthritis. Arthritis Rheum. 1996;39(1):137–145.
  7. Модлин Р. Л., Ким Д., Маурер Д. и др. Врожденный и адаптивный иммунитет кожи. В: Дерматология Фицпатрика в клинической практике: в 3 т. Пер. с англ.; общ. ред. акад. А. А. Кубановой. М.: Издательство Панфилова; БИНОМ. Лаборатория знаний, 2012;I:99–120.
  8. McEver R. P., Cummings R. D. Role of PSGL-1 Binding to Selectins in Leukocyte Recruitment. J Clin Invest. 1997;100(3):485–492.
  9. Borges E., Pendl G., Eytner R., et al. The binding of T cell-expressed P-selectin glycoprotein ligand-1 to Eand P-selectin is differentially regulated. J Biol Chem. 1997;272(45):28786–28792.
  10. Lo C. Y., Antonopoulos A., Gupta R. et al. Competition between core-2 GlcNAc-transferase and ST6GalNAc-transferase regulates the synthesis of the leukocyte selectin ligand on human P-selectin glycoprotein ligand1. J Biol Chem. 2013;288(20):13974–13987.
  11. Robert C. Fuhlbrigge, Sandra L. King, Robert Sackstein, et al. CD43 is a ligand for E-selectin on CLA+ human T cells. Blood. 2006;107(4):1421–1426.
  12. Santamaria Babi L. F., Moser R., Perez Soler M. T., et al. Migration of skin-homing T cells across cytokine-activated human endothelial cell layers involves interaction of the cutaneous lymphocyte-associated antigen (CLA), the very late antigen-4 (VLA-4), and the lymphocyte function-associated antigen-1 (LFA-1). J Immunol. 1995;154(4):1543–1550.
  13. Picker L. J., Kishimoto T. K., Smith C. W., et al. ELAM-1 is an adhesion molecule for skin-homing T cells. Nature. 1991;349:796–799.
  14. Sackstein R. The lymphocyte homing receptors: gatekeepers of the multistep paradigm. Curr Opin Hematol. 2005;12(6):444–450.
  15. Picker L. J., Treer J. R., Ferguson-Darnell B., et al. Control of lymphocyte recirculation in man. II. Differential regulation of the cutaneous lymphocyte-associated antigen, a tissue-selective homing receptor for skin-homing T cells. J. Immunol. 1993;150:1122–1136.
  16. Picker L. J., Martin R. J., Trumble A., et al. Differential expression of lymphocyte homing receptors by human memory/effector T cells in pulmonary versus cutaneous immune effector sites. Eur J Immunol. 1994;24(6):1269–1277.
  17. Schaerli P., Moser B. Chemokines: control of primary and memory T-cell traffic. Immunol Res. 2005;31(1):57–74.
  18. Butcher E.C., Picker L.J. Lymphocyte homing and homeostasis. Science. 1996;272(5258):60–66.
  19. Robert C., Kupper T. S. Inflammatory skin diseases, T cells, and immune surveillance. The New England Journal of Medicine. 1999;341(24):1817–1828.
  20. Mora J. R., von Andrian U. H. T-cell homing specificity and plasticity: new concepts and future challenges. Trends Immunol. 2006;3:235–243.
  21. Hudak S., Hagen M., Liu Y., et al. Immune Surveillance and Effector Functions of CCR10+ Skin Homing T Cells. J Immunol August. 2002;169 (3):1189–1196.
  22. Bromley S. K., Yan S., Tomura M., et al. Recirculating memory T cells are a unique subset of CD4+ T cells with a distinct phenotype and migratory pattern. J Immunol. 2013;190(3):970–976.
  23. Sallusto F., Lenig D., Forster R., et al. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature. 1999;401(6754):708–712.
  24. Janine Morales, Bernhard Homey, Alain P. Vicari, et al. CTACK, a skin-associated chemokine that preferentially attracts skin-homing memory T cells. Proc Natl Acad Sci U S A. 1999;96(25):14470–14475.
  25. Homey B., Alenius, H., Muller A., et al. CCL27-CCR10 interactions regulate T cell-mediated skin inflammation. Nat Med. 2002;8:157–165.
  26. Kagami S., Sugaya M., Minatani Y., et al. Elevated serum CTACK/ CCL27 levels in CTCL. J Invest Dermatol. 2006;126:1189–1191.
  27. Петзельбауэр П., Пенг Л., Робер Д. С. Эндотелий при воспалении и ангиогенез. В: Дерматология Фицпатрика в клинической практике: в 3 т. Пер. с англ.; общ. ред. акад. А. А. Кубановой. М.: Издательство Панфилова; БИНОМ. Лаборатория знаний, 2012;II:1729–1743.
  28. Gaide O. Skin memory: the clinical implications. Rev Med Suisse. 2016;12(512):631–634.
  29. Mueller S. N., Mackay L. K. Tissue-resident memory T cells: local specialists in immune defence. Nat Rev Immunol. 2016;16:79–89.
  30. Zaid A., Hor J. L., Christo S. N., et al. Chemokine Receptor-Dependent Control of Skin Tissue–Resident Memory T Cell Formation. J Immunol. 2017, published online. http://www.jimmunol.org/content/suppl/2017/08/30/jimmunol.170057 (accessed February 28, 2018).
  31. Griffith J. W., Sokol C. L., Luster A. D. Chemokines and Chemokine Receptors: Positioning Cells for Host Defense and Immunity. Annu. Rev. Immunol. 2014;32:659–702.
  32. Schenkel J. M., Fraser K. A., Vezys V., et al. Sensing and alarm function of resident memory CD8+ T cells. Nat Immunol. 2013;14:509–513.
  33. Ariotti S., Hogenbirk M. A., Dijkgraaf F. E., et al. T cell memory. Skin-resident memory CD8+ T cells trigger a state of tissue-wide pathogen alert. Science. 2014;346:101–105.
  34. Boyman O., Hefti H. P., Conrad C., et al. Spontaneous development of psoriasis in a new animal model shows an essential role for resident T cells and tumor necrosis factor-α. J Exp Med. 2004;199:731–736.
  35. Khairutdinov V. R., Mikhailichenko A. F., Belousova I. E., et al. The role of intradermal proliferation of T-cells in the pathogenesis of psoriasis. An Bras Dermatol. 2017;92(1):41–44.
  36. Matos T. R., Rie M. A. Discovery of skin lymphocytes was a game changer in experimental dermatology. Exp Dermatol. 2017;26(8):683–684.
  37. Kunstfeld R., Lechleitner S., Groger M., et al. HECA-452+ T cells migrate through superficial vascular plexus but not through deep vascularplexus endothelium. J Invest Dermatol. 1997;108(3):343–348.
  38. Bos J. D., Kapsenberg M. L. The skin immune system: progress in cutaneous biology. Immunol Today. 1993;2:75–78.
  39. Teraki Y., Picker L. J. Independent regulation of cutaneous lymphocyte-associated antigen expression and cytokine synthesis phenotype during human CD4+ memory T cell differentiation. J. Immunol. 1997;159:6018–6029.
  40. Lellem A., Colantonio L., D’Ambrosio D. Skin-versus gutskewed homing receptor expression and intrinsic CCR4 expression on human peripheral blood CD4+CD25+ suppressor T cells. Eur J Immunol. 2003;33:1488–1496.
  41. Davis R. E., Smoller B. R. T lymphocytes expressing HECA-452 epitope are present in cutaneous acute graft-versus-host disease and erythema multiforme, but not in acute graft-versus-host disease in gut organs. Am J Pathol. 1992;141:691–698.
  42. Ellis C. N., Fradin M. S., Messana J. M., et al. Cyclosporine for plaque-type psoriasis: results of a multidose, double-blind trial. N Engl J Med. 1991;324:277–84.
  43. Gottlieb S. L., Gilleaudeau P., Johnson R., et al. Response of psoriasis to a lymphocyte-selective toxin (DAB389IL-2) suggests a primary immune but not keratinocyte, pathogenic basis. Nat Med. 1995;1:442–447.
  44. Bowcock A. M., Krueger J. G. Getting under the skin: the immunogenetics of psoriasis. Nat Rev Immunol. 2005;5(9):699–711.
  45. Schlaak J. F., Buslau M., Jochum W., et al. T cells involved in psoriasis vulgaris belong to the Th1 subset. J Invest Dermatol. 1994;102:145–149.
  46. Chang J. C., Smith L. R., Froning K. J. et al. 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 USA. 1994;91:9282–9286.
  47. Myskowski P. L., Ahkami R. Dermatologic complications of HIV infection. Med Clin North Am. 1996;80:1415–1435.
  48. Davison S. C., Ballsdon A., Allen M. H., et al. Early migration of cutaneous lymphocyte-associated antigen (CLA) positive T cells into evolving psoriatic plaques. Exp Dermatol. 2001;10:280–285.
  49. Nestle F. O., Kaplan D. H., Barker J. Psoriasis. N Engl J Med. 2009;361:496–509.
  50. Valdimarsson H., Thorleifsdottir R. H., Sigurdardottir S.L., et al. Psoriasis — as an autoimmune disease caused by molecular mimicry. Trends Immunol. 2009;30:494–501.
  51. Weitz M., Kiessling C., Friedrich M., et al. Exp Dermatol. 2011;20:561–567.
  52. Diluvio L., Vollmer S., Besgen P. et al. Identical TCR beta-chain rearrangements in streptococcal angina and skin lesions of patients with psoriasis vulgaris. J Immunol. 2006:176:7104–7111.
  53. Thorleifsdottir R. H., Sigurdardottir S. L., Sigurgeirsson B., et al. Improvement of psoriasis after tonsillectomy is associated with a decrease in the frequency of circulating T cells that recognize streptococcal determinants and homologous skin determinants. J Immunol. 2012;188:5160–5165.
  54. Singh T. P., Schon M. P., Wallbrecht K., et al. 8-Methoxypsoralen plus UVA treatment increases the proportion of CLA+ CD25+CD4+ T cells in lymph nodes of K5.hTGFβ1 transgenic mice. Exp Dermatol. 2012;21:228–230.
  55. Hollo P., Marschalko M., Temesvari E., et al. Follow-up analysis of circulating mononuclear cell CLA expression in patients with psoriasis. J Dermatol Sci. 2005;39:131–133.
  56. Jokai H., Szakonyi J., Kontar O., et al. Cutaneous lymphocyte-associated antigen as a novel predictive marker of TNF-alpha inhibitor biological therapy in psoriasis. Exp Dermatol. 2013;22:221–223.
  57. Robert C., Kupper T. S. Inflammatory skin diseases, T cells, and immune surveillance. N Engl J Med. 1999;341(24):1817–1828.
  58. Santamaria-Babi L. F. Skin-Homing T Cells in Cutaneous Allergic Inflammation. Chem Immunol Allergy. 2006;91:87–97.
  59. Ferran M., Santamaria-Babi L. F. Pathological Mechanisms of Skin Homing T Cells in Atopic Dermatitis. World Allergy Organ J. 2010;3:44–47.
  60. Leung D. Y, Gately M., Trumble A. et al. 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;3:747–753.
  61. Akdis M., Akdis C. A., Weigl L., et al. Skin-homing, CLA+ memory T cells are activated in atopic dermatitis and regulate IgE by an IL-13-dominated cytokine pattern: IgG4 counter-regulation by CLA-memory T cells. J Immunol. 1997;159(9):4611–5619.
  62. Ferran M., Romeu E. R., Rincon C., et al. Circulating CLA+ T lymphocytes as peripheral cell biomarkers in T-cell-mediated skin diseases. Exp Dermatol. 2013;22(7):439–442.
  63. Santamaria Babi L. F., Picker L. J., Perez Soler M. T., et al. Circulating allergen-reactive T cells from patients with atopic dermatitis and allergic contact dermatitis express the skin-selective homing receptor, the cutaneous lymphocyte-associated antigen. J Exp Med. 1995;3:1935–1940.
  64. Reefer A. J., Satinover S. M., Solga M. D., et al. Analysis of CD25hiCD4+ “regulatory” T-cell subtypes in atopic dermatitis reveals a novel T(H)2-like population. J Allergy Clin Immunol. 2008;3:415–422.
  65. Harpers E. G., Simpson E. L., Takiguchi R. H., et al. Efalizumab therapy for atopic dermatitis causes marked increases in circulating effector memory CD4+ T cells that express cutaneous lymphocyte antigen. J Invest Dermatol. 2008;3:1173–1181.
  66. Antunez C., Torres M. J., Lopez S., et al. Calcitonin gene-related peptide modulates interleukin-13 in circulating cutaneous lymphocyte-associated antigen-positive T cells in patients with atopic dermatitis. Br J Dermatol. 2009;161:547–553.
  67. Schmid-Ott G., Jaeger B., Meyer S., et al. Different expression of cytokine and membrane molecules by circulating lymphocytes on acute mental stress in patients with atopic dermatitis in comparison with healthy controls. J Allergy Clin Immunol. 2001;3:455–462.
  68. Dillon S., Sprecher C., Hammond A., et al. Interleukin 31, a cytokine produced by activated T cells, induces dermatitis in mice. Nat Immunol. 2004;3:752–760.
  69. Sonkoly E., Muller A., Lauerma A. I., et al. IL-31: a new link between T cells and pruritus in atopic skin inflammation. J Allergy Clin Immunol. 2006;3:411–417.
  70. Gober M. D., Gaspari A. A. Allergic contact dermatitis. Curr Dir Autoimmun. 2008;10:1–26.
  71. Cavani A. Immune regulatory mechanisms in allergic contact dermatitis and contact sensitization. Chem Immunol Allergy. 2008;94:93–100.
  72. Cavani A., Nasorri F., Ottaviani C., et al. Human CD25+ regulatory T cells maintain immune tolerance to nickel in healthy, nonallergic individuals. J Immunol. 2003;171(11):5760–5768.
  73. Bangert C., Friedl J., Stary G., et al. Immunopathologic Features of Allergic Contact Dermatitis in Humans: Participation of Plasmacytoid Dendritic Cells in the Pathogenesis of the Disease? J Invest Dermatol. 2003;121(6):1409–1418.
  74. Dyring-Andersen B., Skov L., Lovendorf M. B., et al. CD4(+) T cells producing interleukin (IL)-17, IL-22 and interferon-γ are major effector T cells in nickel allergy. Contact Dermatitis. 2013;68(6):339–347.
  75. Ferrara J. L., Deeg H. J. Graft-versus-host disease. N Engl J Med. 1991;324: 667–674.
  76. Криволапова А. Ю., Белоусова И. Э., Смирнова И. О. и соавт. Патоморфологическая диагностика кожных проявлений реакции «трансплантат против хозяина». Архив патологии. 2014;(4):24–28.
  77. Davis R. E., Smoller B. R. T lymphocytes expressing HECA-452 epitope are present in cutaneous acute graft-versus-host disease and erythema multiforme, but not in acute graft-versus-host disease in gut organs. Am J Pathol. 1992;141:691–698.
  78. Engelhardt B. G., Sengsayadeth S. M., Jagasia M., et al. Tissuespecific regulatory T cells: biomarker for acute graft-vs-host disease and survival. Exp Hematol. 2012;40:974–982.
  79. Engelhardt B. G., Jagasia M., Savani B. N., et al. Regulatory T cell expression of CLA or α(4)β(7) and skin or gut acute GVHD outcomes. Bone Marrow Transplant. 2011;46:436–442.
  80. Fuschiotti P., Larregina A. T., Ho J., et al. Interleukin-13-producing CD8+ T cells mediate dermal fibrosis in patients with systemic sclerosis. Arthritis Rheum. 2012;65:236–246.
  81. Blanca M., Leyva L., Torres M. J., et al. Memory to the hapten in non-immediate cutaneous allergic reactions to betalactams resides in a lymphocyte subpopulation expressing both CD45RO and CLA markers. Blood Cells Mol Dis. 2003;31:75–79.
  82. Blanca M., Posadas S., Torres M. J., et al. Expression of the skin-homing receptor in peripheral blood lymphocytes from subjects with nonimmediate cutaneous allergic drug reactions. Allergy. 2000;55:998–1004.
  83. Gelb A. B., Smoller B. R., Warnke R. A., et al. Lymphocytes infiltrating primary cutaneous neoplasms selectively express the cutaneous lymphocyteassociated antigen (CLA). Am J Pathol. 1993;142(5):1556–1564.
  84. Weishaupt C., Munoz K. N., Buzney E., et al. T-cell distribution and adhesion receptor expression in metastatic melanoma. Clin Cancer Res. 2007;13:2549–2556.
  85. Clark R. A., Huang S. J., Murphy G. F., et al. Human squamous cell carcinomas evade the immune response by down-regulation of vascular E-selectin and recruitment of regulatory T cells. J Exp Med. 2008;205:2221–2234.
  86. Girardi M., Heald P. W., Wilson L. D. The pathogenesis of mycosis fungoides. N Engl J Med. 2004;350:1978–88.
  87. Jawed S. I., Myskowski P. L., Horwitz S., et al. Primary cutaneous T-cell lymphoma (mycosis fungoides and Sezary syndrome). Part I. Diagnosis: Clinical and histopathologic features and new molecular and biologic markers. J Am Acad Dermatol. 2014;70(2):205.e1–16.
  88. Campbell J. J., Clark R. A., Watanabe R., et al. Sezary syndrome and mycosis fungoides arise from distinct T-cell subsets: a biologic rationale for their distinct clinical behaviors. Blood. 2010;116(5):767–771.
  89. Nicolay J. P., Felcht M., Schledzewski K., et al. Sezary syndrome: old enigmas, new targets. J Dtsch Dermatol Ges. 2016;14(3):256–264.

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2018 Patrushev A.V., Samtsov A.V., Nikitin V.Y., Ivanov A.М., Gumilevskaya O.Р., Sukharev A.V., Sukhina I.A.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.
СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ПИ № ФС 77 - 60448 от 30.12.2014.


This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies