Cytokine pathways and interactions in alopecia areata

European Journal of Dermatology

Volumn 23, Issue 3, 2013, Pages 308-318

  Giordano, Cerrene N ^a   Sinha, Animesh A ^a  

^a ROSWELL PARK CANCER INSTITUTE   (United States)

Author keywords

Alopecia; Autoantigens; Autoimmunity; Cytokines; Proinflammatory; T lymphocytes

Indexed keywords

CANAKINUMAB; CORTICOSTEROID; CYCLOSPORIN A; CYTOKINE; DIPHENCYPRONE; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 16; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 8; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; RANTES; RECOMBINANT INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR ALPHA INHIBITOR; USTEKINUMAB;

ALOPECIA; ALOPECIA AREATA; AUTOIMMUNE DISEASE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CYTOKINE PRODUCTION; DISEASE SEVERITY; GENETIC POLYMORPHISM; GOUT; HAIR GROWTH; HAIR LOSS; HUMAN; MULTIPLE SCLEROSIS; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PATHOGENESIS; PSORIASIS; PUVA; REGULATORY T LYMPHOCYTE; REVIEW; RHEUMATOID ARTHRITIS; SEPSIS; T LYMPHOCYTE ACTIVATION; TH1 CELL; TH17 CELL; TH2 CELL; ANIMAL; ANTAGONISTS AND INHIBITORS; FORECASTING; IMMUNOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

ALOPECIA AREATA; ANIMALS; CYTOKINES; FORECASTING; HUMANS; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 84880609284     PISSN: 11671122     EISSN: 19524013     Source Type: Journal    
DOI: 10.1684/ejd.2013.2042     Document Type: Review

References (83)

1. Gregoriou S, Papafragkaki D, Kontochristopoulos G, Rallis E, Kalogeromitros D, Rigopoulos D. Cytokines and other mediators in alopecia areata. Mediators Inflamm 2010; 2010: 928030.
2. Safavi KH, Muller SA, Suman VJ, Moshell AN, Melton LJ, 3rd. Incidence of alopecia areata in Olmsted County, Minnesota, 1975 through 1989. Mayo Clin Proc 1995; 70: 628-33.
3. Madani S, Shapiro J. Alopecia areata update. J Am Acad Dermatol 2000; 42: 549-66; quiz 67-70.
4. Hoffmann R. The potential role of cytokines and T cells in alopecia areata. J Investig Dermatol Symp Proc 1999; 4: 235-8.
5. Messenger AG, Slater DN, Bleehen SS. Alopecia areata: alterations in the hair growth cycle and correlation with the follicular pathology. Br J Dermatol 1986; 114: 337-47.
6. Alexis AF, Dudda-Subramanya R, Sinha AA. Alopecia areata: autoimmune basis of hair loss. Eur J Dermatol 2004; 14: 364-70.
7. McDonagh AJ, Messenger AG. The pathogenesis of alopecia areata. Dermatol Clin 1996; 14: 661-70.
8. McDonagh AJ, Messenger AG. Alopecia areata. Clin Dermatol 2001; 19: 141-7.
9. Hair Research. 3rd Annual meeting of the European Hair Research Society. Berlin, October 2-3, 1992. Skin Pharmacol 1994; 7: 1-108.
10. Whiting DA. Histopathology of alopecia areata in horizontal sections of scalp biopsies. J Invest Dermatol 1995; 104(5 Suppl): 26S-7S.
11. Cotsarelis G, Sun TT, Lavker RM. Label-retaining cells reside in the bulge area of pilosebaceous unit: implications for follicular stem cells, hair cycle, and skin carcinogenesis. Cell 1990; 61: 1329-37.
12. Paus R, Ito N, Takigawa M, Ito T. The hair follicle and immune privilege. J Investig Dermatol Symp Proc 2003; 8: 188-94.
13. Christoph T, Muller-Rover S, Audring H, et al. The human hair follicle immune system: cellular composition and immune privilege. Br J Dermatol 2000; 142: 862-73.
14. Brocker EB, Echternacht-Happle K, Hamm H, Happle R. Abnormal expression of class I and class II major histocompatibility antigens in alopecia areata: modulation by topical immunotherapy. J Invest Dermatol 1987; 88: 564-8.
15. Hamm H, Klemmer S, Kreuzer I, Steijlen PM, Happle R, Brocker EB. HLA-DR and HLA-DQ antigen expression of anagen and telogen hair bulbs in long-standing alopecia areata. Arch Dermatol Res 1988; 280: 179-81.
16. Khoury EL, Price VH, Greenspan JS. HLA-DR expression by hair follicle keratinocytes in alopecia areata: evidence that it is secondary to the lymphoid infiltration. J Invest Dermatol 1988; 90: 193-200.
17. Konig A, Happle R, Hoffmann R. IFN-gamma-induced HLA-DR but not ICAM-1 expression on cultured dermal papilla cells is downregulated by TNF-alpha. Arch Dermatol Res 1997; 289: 466-70.
18. Arca E, Musabak U, Akar A, Erbil AH, Tastan HB. Interferongamma in alopecia areata. Eur J Dermatol 2004; 14: 33-6.
19. Hoffmann R, Wenzel E, Huth A, et al. Cytokine mRNA levels in Alopecia areata before and after treatment with the contact allergen diphenylcyclopropenone. J Invest Dermatol 1994; 103: 530-3.
20. Gilhar A, Krueger GG. Hair growth in scalp grafts from patients with alopecia areata and alopecia universalis grafted onto nude mice. Arch Dermatol 1987; 123: 44-50.
21. Gilhar A, Ullmann Y, Berkutzki T, Assy B, Kalish RS. Autoimmune hair loss (alopecia areata) transferred by T lymphocytes to human scalp explants on SCID mice. J Clin Invest 1998; 101: 62-7.
22. Bodemer C, Peuchmaur M, Fraitaig S, Chatenoud L, Brousse N, De Prost Y. Role of cytotoxic T cells in chronic alopecia areata. J Invest Dermatol 2000; 114: 112-6.
23. Norris DA, Duke R, Whang K, Middleton M. Immunologic cytotoxicity in alopecia areata: apoptosis of dermal papilla cells in alopecia areata. J Invest Dermatol 1995; 104(5 Suppl): 8S-9S.
24. Weedon D, Strutton G. Apoptosis as the mechanism of the involution of hair follicles in catagen transformation. Acta Derm Venereol 1981; 61: 335-9.
25. Michie HJ, Jahoda CA, Oliver RF, Johnson BE. The DEBR rat: an animal model of human alopecia areata. Br J Dermatol 1991; 125: 94-100.
26. McElwee KJ, Spiers EM, Oliver RF. In vivo depletion of CD8+ T cells restores hair growth in the DEBR model for alopecia areata. Br J Dermatol 1996; 135: 211-7.
27. McElwee KJ, Boggess D, King LE, Jr, Sundberg JP. Experimental induction of alopecia areata-like hair loss in C3H/HeJ mice using fullthickness skin grafts. J Invest Dermatol 1998; 111: 797-803.
28. Sato-Kawamura M, Aiba S, Tagami H. Strong expression of CD40, CD54 and HLA-DR antigen and lack of evidence for direct cellular cytotoxicity are unique immunohistopathological features in alopecia areata. Arch Dermatol Res 2003; 294: 536-43.
29. Teraki Y, Imanishi K, Shiohara T. Cytokines in alopecia areata: contrasting cytokine profiles in localized form and extensive form (alopecia universalis). Acta Derm Venereol 1996; 76: 421-3.
30. Gilhar A, Landau M, Assy B, et al. Transfer of alopecia areata in the human scalp graft/Prkdc(scid) (SCID) mouse system is characterized by a TH1 response. Clin Immunol 2003; 106: 181-7.
31. Freyschmidt-Paul P, McElwee KJ, Hoffmann R, et al. Interferongamma-deficient mice are resistant to the development of alopecia areata. Br J Dermatol 2006; 155: 515-21.
32. Kasumagic-Halilovic E, Prohic A, Karamehic J. Serum concentrations of interferon-gamma (IFN-g) in patients with alopecia areata: correlation with clinical type and duration of the disease. Med Arh 2010; 64: 212-4.
33. Barahmani N, Lopez A, Babu D, Hernandez M, Donley SE, Duvic M. Serum T helper 1 cytokine levels are greater in patients with alopecia areata regardless of severity or atopy. Clin Exp Dermatol 2010; 35: 409-16.
34. Zoller M, McElwee KJ, Vitacolonna M, Hoffmann R. The progressive state, in contrast to the stable or regressive state of alopecia areata, is reflected in peripheral blood mononuclear cells. Exp Dermatol 2004; 13: 435-44.
35. Lee D, Hong SK, Park SW, et al. Serum levels of IL-18 and sIL-2R in patients with alopecia areata receiving combined therapy with oral cyclosporine and steroids. Exp Dermatol 2010; 19: 145-7.
36. McElwee KJ, Hoffmann R. Alopecia areata-animal models. Clin Exp Dermatol 2002; 27: 410-7.
37. Katagiri K, Arakawa S, Hatano Y. In vivo levels of IL-4, IL-10, TGF-beta1 and IFN-gamma mRNA of the peripheral blood mononuclear cells in patients with alopecia areata in comparison to those in patients with atopic dermatitis. Arch Dermatol Res 2007; 298: 397-401.
38. Shohat M, Mimouni D, Ben-Amitai D, et al. In vitro cytokine profile in childhood alopecia areata and the immunomodulatory effects of AS-101. Clin Exp Dermatol 2005; 30: 432-4.
39. Bettelli E, Carrier Y, Gao W, et al. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 2006; 441: 235-8.
40. Korn T, Bettelli E, Oukka M, Kuchroo VK. IL-17 and Th17 Cells. Annu Rev Immunol 2009; 27: 485-517.
41. Bettelli E, Oukka M, Kuchroo VK. T(H)-17 cells in the circle of immunity and autoimmunity. Nat Immunol 2007; 8: 345-50.
42. Mangan PR, Harrington LE, O'Quinn DB, et al. Transforming growth factor-beta induces development of the T(H)17 lineage. Nature 2006; 441: 231-4.
43. 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.
44. Coda AB, Qafalijaj Hysa V, Seiffert-Sinha K, Sinha AA. Peripheral blood gene expression in alopecia areata reveals molecular pathways distinguishing heritability, disease and severity. Genes Immun 2010; 11: 531-41.
45. Kryczek I, Wei S, Gong W, et al. Cutting edge: IFN-gamma enables APC to promote memory Th17 and abate Th1 cell development. J Immunol 2008; 181: 5842-6.
46. Kryczek I, Bruce AT, Gudjonsson JE, et al. Induction of IL-17+ T cell trafficking and development by IFN-gamma: mechanism and pathological relevance in psoriasis. J Immunol 2008; 181: 4733-41.
47. Arakawa M, Dainichi T, Yasumoto S, Hashimoto T. Lesional Th17 cells in pemphigus vulgaris and pemphigus foliaceus. J Dermatol Sci 2009; 53: 228-31.
48. Zoller M, McElwee KJ, Engel P, Hoffmann R. Transient CD44 variant isoform expression and reduction in CD4(+)/CD25(+) regulatory T cells in C3H/HeJ mice with alopecia areata. J Invest Dermatol 2002; 118: 983-92.
49. Philpott MP, Sanders DA, Bowen J, Kealey T. Effects of interleukins, colony-stimulating factor and tumour necrosis factor on human hair follicle growth in vitro: a possible role for interleukin-1 and tumour necrosis factor-alpha in alopecia areata. Br J Dermatol 1996; 135: 942-8.
50. Groves R.W. WIR, Sarkar S., Nakamura K., and Kupper T.S. Analysis of epidermal IL-1 family members in vivo using transgenic mouse models. Journal of Investigative Dermatology 1994; 102: 556.
51. Tarlow JK, Clay FE, Cork MJ, et al. Severity of alopecia areata is associated with a polymorphism in the interleukin-1 receptor antagonist gene. J Invest Dermatol 1994; 103: 387-90.
52. Ahini R.T. dGFS, and McDonagh A.J.G. Interleukin 1 composite genotypes as determinants for subtypes of alopecia areata. Journal of Investigative Dermatology Symposium Proceedings 1999; 4: 53.
53. Deeths MJ, Endrizzi BT, Irvin ML, Steiner LP, Ericson ME, Hordinsky MK. Phenotypic analysis of T-cells in extensive alopecia areata scalp suggests partial tolerance. J Invest Dermatol 2006; 126: 366-73.
54. Strober BE, Siu K, Alexis AF, et al. Etanercept does not effectively treat moderate to severe alopecia areata: an open-label study. J Am Acad Dermatol 2005; 52: 1082-4.
55. Abramovits W, Losornio M. Failure of two TNF-alpha blockers to influence the course of alopecia areata. Skinmed 2006; 5: 177-81.
56. Beccastrini E, Squatrito D, Emmi G, Fabbri P, Emmi L. Alopecia areata universalis during off-label treatment with Infliximab in a patient with Behcet disease. Dermatol Online J 2010; 16: 15.
57. Chaves Y, Duarte G, Ben-Said B, Tebib J, Berard F, Nicolas JF. Alopecia areata universalis during treatment of rheumatoid arthritis with anti-TNF-alpha antibody (adalimumab). Dermatology 2008; 217: 380.
58. Ferran M, Calvet J, Almirall M, Pujol RM, Maymo J. Alopecia areata as another immune-mediated disease developed in patients treated with tumour necrosis factor-alpha blocker agents: Report of five cases and review of the literature. J Eur Acad Dermatol Venereol 2011; 25: 479-84.
59. Hernandez MV, Nogues S, Ruiz-Esquide V, Alsina M, Canete JD, Sanmarti R. Development of alopecia areata after biological therapy with TNF-alpha Blockers: description of a case and review of the literature. Clin Exp Rheumatol 2009; 27: 892-3.
60. Kirshen C, Kanigsberg N. Alopecia areata following adalimumab. J Cutan Med Surg 2009; 13: 48-50.
61. Pan Y, Rao NA. Alopecia areata during etanercept therapy. Ocul Immunol Inflamm 2009; 17: 127-9.
62. Pelivani N, Hassan AS, Braathen LR, Hunger RE, Yawalkar N. Alopecia areata universalis elicited during treatment with adalimumab. Dermatology 2008; 216: 320-3.
63. Tanyasiri K, Hira K, Mitsuishi K, Ueki R, Sekigawa I, Ogawa H. Interleukin-16 in patients with alopecia areata. J Dermatol Sci 2005; 37: 55-7.
64. Kuwano Y, Fujimoto M, Watanabe R, et al. Serum chemokine profiles in patients with alopecia areata. Br J Dermatol 2007; 157: 466-73.
65. Shimizu T, Mizue Y, Abe R, Watanabe H, Shimizu H. Increased macrophage migration inhibitory factor (MIF) in the sera of patients with extensive alopecia areata. J Invest Dermatol 2002; 118: 555-7.
66. Galbraith GM, Palesch Y, Gore EA, Pandey JP. Contribution of interleukin 1beta and KM loci to alopecia areata. Hum Hered 1999; 49: 85-9.
67. McDonagh AJ, Snowden JA, Stierle C, Elliott K, Messenger AG. HLA and ICAM-1 expression in alopecia areata in vivo and in vitro: the role of cytokines. Br J Dermatol 1993; 129: 250-6.
68. Symington FW. Lymphotoxin, tumor necrosis factor, and gamma interferon are cytostatic for normal human keratinocytes. J Invest Dermatol 1989; 92: 798-805.
69. Korn T, Bettelli E, Gao W, et al. IL-21 initiates an alternative pathway to induce proinflammatory T(H)17 cells. Nature 2007; 448: 484-7.
70. Nurieva R, Yang XO, Martinez G, et al. Essential autocrine regulation by IL-21 in the generation of inflammatory T cells. Nature 2007; 448: 480-3.
71. Zhou L, Ivanov II, Spolski R, et al. IL-6 programs T(H)-17 cell differentiation by promoting sequential engagement of the IL-21 and IL-23 pathways. Nat Immunol 2007; 8: 967-74.
72. McGeachy MJ, Bak-Jensen KS, Chen Y, et al. TGF-beta and IL-6 drive the production of IL-17 and IL-10 by T cells and restrain T(H)-17 cell-mediated pathology. Nat Immunol 2007; 8: 1390-7.
73. Gupta P, Freyschmidt-Paul P, Vitacolonna M, et al. A chronic contact eczema impedes migration of antigen-presenting cells in alopecia areata. J Invest Dermatol 2006; 126: 1559-73.
74. Kalish RS, Gilhar A. Alopecia areata: autoimmunity-the evidence is compelling. J Investig Dermatol Symp Proc 2003; 8: 164-7.
75. Skurkovich B, Skurkovich S. Anti-interferon-gamma antibodies in the treatment of autoimmune diseases. Curr Opin Mol Ther 2003; 5: 52-7.
76. Ludwig RJ, Schmidt E. Cytokines in autoimmune bullous skin diseases. Epiphenomena or contribution to pathogenesis? G Ital Dermatol Venereol 2009; 144: 339-49.
77. Church LD, McDermott MF. Canakinumab, a fully-human mAb against IL-1beta for the potential treatment of inflammatory disorders. Curr Opin Mol Ther 2009; 11: 81-9.
78. Posten W, Swan J. Recurrence of alopecia areata in a patient receiving etanercept injections. Arch Dermatol 2005; 141: 759-60.
79. Doyle LA, Sperling LC, Baksh S, et al. Psoriatic alopecia/alopecia areata-like reactions secondary to anti-tumor necrosis factor-alpha therapy: a novel cause of noncicatricial alopecia. Am J Dermatopathol 2011; 33: 161-6.
80. Slowinska M, Kardynal A, Warszawik O, Czuwara J, Rudnicka L. Alopecia areata developing paralell to improvement of psoriasis during ustekinumab therapy. J Dermatol Case Rep 2010; 4: 15-7.
81. Ayroldi E, Bastianelli A, Cannarile L, Petrillo MG, Delfino DV, Fierabracci A. A Pathogenetic Approach to Autoimmune Skin Disease Therapy: Psoriasis and Biological Drugs, Unresolved Issues, and Future Directions. Curr Pharm Des 2011; 17: 3176-90.
82. Chen Y, Langrish CL, McKenzie B, et al. Anti-IL-23 therapy inhibits multiple inflammatory pathways and ameliorates autoimmune encephalomyelitis. J Clin Invest 2006; 116: 1317-26.
83. Kunz M, Ibrahim SM. Cytokines and cytokine profiles in human autoimmune diseases and animal models of autoimmunity. Mediators Inflamm 2009; 2009: 979258.