Alopecia areata profiling shows TH1, TH2, and IL-23 cytokine activation without parallel TH17/TH22 skewing

Journal of Allergy and Clinical Immunology

Volumn 136, Issue 5, 2015, Pages 1277-1287

  Suárez Fariñas, Mayte ^a,b   Ungar, Benjamin ^a,b   Noda, Shinji ^b   Shroff, Anjali ^a   Mansouri, Yasaman ^a   Fuentes Duculan, Judilyn ^b   Czernik, Annette ^a   Zheng, Xiuzhong ^b   Estrada, Yeriel D ^a   Xu, Hui ^a   Peng, Xiangyu ^a   Shemer, Avner ^c   Krueger, James G ^b   Lebwohl, Mark G ^a   Guttman Yassky, Emma ^a,b  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b ROCKEFELLER UNIVERSITY   (United States)

^c Rockefeller University ^*  (Israel)

Author keywords

Alopecia areata; atopic dermatitis; hair keratin; IL 23; T cell; TH1; TH2

Indexed keywords

BIOLOGICAL MARKER; CHEMOKINE; INTERLEUKIN 23; KERATIN; TRANSCRIPTOME;

ADULT; ALOPECIA AREATA; ATOPIC DERMATITIS; FEMALE; GENETICS; HUMAN; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; MALE; METABOLISM; MICROARRAY ANALYSIS; MIDDLE AGED; PSORIASIS; TH1 CELL; TH2 CELL; YOUNG ADULT;

ADULT; ALOPECIA AREATA; BIOMARKERS; CHEMOKINES; DERMATITIS, ATOPIC; FEMALE; HUMANS; INTERLEUKIN-23; KERATINS, HAIR-SPECIFIC; LYMPHOCYTE ACTIVATION; MALE; MICROARRAY ANALYSIS; MIDDLE AGED; PSORIASIS; TH1 CELLS; TH2 CELLS; TRANSCRIPTOME; YOUNG ADULT;

EID: 84953638491     PISSN: 00916749     EISSN: 10976825     Source Type: Journal    
DOI: 10.1016/j.jaci.2015.06.032     Document Type: Article

References (112)

1. Hordinsky MK. Overview of alopecia areata. J Investig Dermatol Symp Proc 2013;16:S13-5.
2. Huang KP, Mullangi S, Guo Y, Qureshi AA. Autoimmune, atopic, and mental health comorbid conditions associated with alopecia areata in the United States. JAMA Dermatol 2013;149:789-94.
3. Giordano CN, Sinha AA. Cytokine pathways and interactions in alopecia areata. Eur J Dermatol 2013;23:308-18.
4. Alkhalifah A. Alopecia areata update. Dermatol Clin 2013;31:93-108.
5. Hunt N, McHale S. The psychological impact of alopecia. BMJ 2005;331:951-3.
6. Karimkhani C, Boyers LN, Naghavi M, Coffeng LE, Lott JP, Wulf S, et al. The global burden of disease associated with alopecia areata. Br J Dermatol 2015;172: 1424-6.
7. Biran R, Zlotogorski A, Ramot Y. The genetics of alopecia areata: new approaches, new findings, new treatments. J Dermatol Sci 2015;78:11-20.
8. Madani S, Shapiro J. Alopecia areata update. J Am Acad Dermatol 2000;42: 549-70.
9. Seetharam KA. Alopecia areata: an update. Indian J Dermatol Venereol Leprol 2013;79:563-75.
10. Finner AM. Alopecia areata: Clinical presentation, diagnosis, and unusual cases. Dermatol Ther 2011;24:348-54.
11. Ito T. Advances in the management of alopecia areata. J Dermatol 2012;39:11-7.
12. Alkhalifah A, Alsantali A, Wang E, McElwee KJ, Shapiro J. Alopecia areata update: part II. Treatment. J Am Acad Dermatol 2010;62:191-204.
13. Alkhalifah A, Alsantali A, Wang E, McElwee KJ, Shapiro J. Alopecia areata update: part I. Clinical picture, histopathology, and pathogenesis. J Am Acad Dermatol 2010;62:177-90.
14. Luk NM, Chiu LS, Lee KC, Chau CT, Lee VW, Chang M, et al. Efficacy and safety of diphenylcyclopropenone among Chinese patients with steroid resistant and extensive alopecia areata. J Eur Acad Dermatol Venereol 2013;27:e400-5.
15. Aghaei S, Saki N, Daneshmand E, Kardeh B. Prevalence of psychological disorders in patients with alopecia areata in comparison with normal subjects. ISRN Dermatol 2014;2014:304370.
16. Kumaresan M. Intralesional steroids for alopecia areata. Int J Trichology 2010;2: 63-5.
17. Alkhalifah A. Topical and intralesional therapies for alopecia areata. Dermatol Ther 2011;24:355-63.
18. Durdu M, Ozcan D, Baba M, Seckin D. Efficacy and safety of diphenylcyclopropenone alone or in combination with anthralin in the treatment of chronic extensive alopecia areata: a retrospective case series. J Am Acad Dermatol 2015;72: 640-50.
19. El Khoury J, Abd-el-Baki J, Succariah F, Abbas O, Kibbi AG, Kurban M. Topical immunomodulation with diphenylcyclopropenone for alopecia areata: the Lebanese experience. Int J Dermatol 2013;52:1551-6.
20. Kim BJ, Min SU, Park KY, Choi JW, Park SW, Youn SW, et al. Combination therapy of cyclosporine and methylprednisolone on severe alopecia areata. J Dermatolog Treat 2008;19:216-20.
21. Park KY, Jang WS, Son IP, Choi SY, Lee MY, Kim BJ, et al. Combination therapy with cyclosporine and psoralen plus ultraviolet a in the patients with severe alopecia areata: a retrospective study with a self-controlled design. Ann Dermatol 2013;25:12-6.
22. Yang CC, Lee CT, Hsu CK, Lee YP, Wong TW, Chao SC, et al. Early intervention with high-dose steroid pulse therapy prolongs disease-free interval of severe alopecia areata: a retrospective study. Ann Dermatol 2013;25:471-4.
23. Whitmont KJ, Cooper AJ. PUVA treatment of alopecia areata totalis and universalis: a retrospective study. Australas J Dermatol 2003;44:106-9.
24. Xing L, Dai Z, Jabbari A, Cerise JE, Higgins CA, Gong W, et al. Alopecia areata is driven by cytotoxic T lymphocytes and is reversed by JAK inhibition. Nat Med 2014;20:1043-9.
25. Ito T, Tokura Y. The role of cytokines and chemokines in the T-cell-mediated autoimmune process in alopecia areata. Exp Dermatol 2014;23:787-91.
26. Gilhar A, Etzioni A, Paus R. Alopecia areata. N Engl J Med 2012;366: 1515-25.
27. McElwee KJ, Spiers EM, Oliver RF. In vivo depletion of CD81 T cells restores hair growth in the DEBR model for alopecia areata. Br J Dermatol 1996;135: 211-7.
28. McElwee KJ, Silva K, Boggess D, Bechtold L, King LE, Sundberg JP. Alopecia areata in C3H/HeJ mice involves leukocyte-mediated root sheath disruption in advance of overt hair loss. Vet Pathol 2003;40:643-50.
29. Gregoriou S, Papafragkaki D, Kontochristopoulos G, Rallis E, Kalogeromitros D, Rigopoulos D. Cytokines and other mediators in alopecia areata. Mediators Inflamm 2010;2010:928030.
30. McElwee KJ, Gilhar A, Tobin DJ, Ramot Y, Sundberg JP, Nakamura M, et al. What causes alopecia areata? Exp Dermatol 2013;22:609-26.
31. Hoffmann R. The potential role of cytokines and T cells in alopecia areata. J Investig Dermatol Symp Proc 1999;4:235-8.
32. Subramanya RD, Coda AB, Sinha AA. Transcriptional profiling in alopecia areata defines immune and cell cycle control related genes within disease-specific signatures. Genomics 2010;96:146-53.
33. 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.
34. Zhang X, Zhao Y, Ye Y, Li S, Qi S, Yang Y, et al. Lesional infiltration of mast cells, Langerhans cells, T cells and local cytokine profiles in alopecia areata. Arch Dermatol Res 2015;307:319-31.
35. Ito T, Hashizume H, Shimauchi T, Funakoshi A, Ito N, Fukamizu H, et al. CXCL10 produced from hair follicles induces Th1 and Tc1 cell infiltration in the acute phase of alopecia areata followed by sustained Tc1 accumulation in the chronic phase. J Dermatol Sci 2013;69:140-7.
36. Tembhre MK, Sharma VK. T-helper and regulatory T-cell cytokines in the peripheral blood of patients with active alopecia areata. Br J Dermatol 2013;169:543-8.
37. Bakry OA, El Shazly RM, Basha MA, Mostafa H. Total serum immunoglobulin E in patients with alopecia areata. Indian Dermatol Online J 2014;5:122-7.
38. Avitabile S, Sordi D, Garcovich S, Colonna L, De Luca A, Nasorri F, et al. Effective squaric acid dibutylester immunotherapy is associated with a reduction of skin infiltrating T-helper (Th)1 and Th17 cells in alopecia areata patients. J Dermatol 2015;42:98-9.
39. Tanemura A, Oiso N, Nakano M, Itoi S, Kawada A, Katayama I. Alopecia areata: infiltration of Th17 cells in the dermis, particularly around hair follicles. Dermatology 2013;226:333-6.
40. Khattri S, Shemer A, Rozenblit M, Dhingra N, Czarnowicki T, Finney R, et al. Cyclosporine in patients with atopic dermatitis modulates activated inflammatory pathways and reverses epidermal pathology. J Allergy Clin Immunol 2014;133: 1626-34.
41. Johnson-Huang LM, Suarez-Farinas M, Sullivan-Whalen M, Gilleaudeau P, Krueger JG, Lowes MA. Effective narrow-band UVB radiation therapy suppresses the IL-23/IL-17 axis in normalized psoriasis plaques. J Invest Dermatol 2010;130:2654-63.
42. Gittler JK, Shemer A, Suarez-Farinas M, Fuentes-Duculan J, Gulewicz KJ, Wang CQ, et al. Progressive activation of T(H)2/T(H)22 cytokines and selective epidermal proteins characterizes acute and chronic atopic dermatitis. J Allergy Clin Immunol 2012;130:1344-54.
43. Guttman-Yassky E, Lowes MA, Fuentes-Duculan J, Whynot J, Novitskaya I, Cardinale I, et al. Major differences in inflammatory dendritic cells and their products distinguish atopic dermatitis from psoriasis. J Allergy Clin Immunol 2007;119: 1210-7.
44. Guttman-Yassky E, Suarez-Farinas M, Chiricozzi A, Nograles KE, Shemer A, Fuentes-Duculan J, et al. Broad defects in epidermal cornification in atopic dermatitis identified through genomic analysis. J Allergy Clin Immunol 2009; 124:1235-44.e58.
45. Suarez-Farinas M, Dhingra N, Gittler J, Shemer A, Cardinale I, de Guzman Strong C, et al. Intrinsic atopic dermatitis shows similar TH2 and higher TH17 immune activation compared with extrinsic atopic dermatitis. J Allergy Clin Immunol 2013;132:361-70.
46. Suarez-Farinas M, Pellegrino M, Wittkowski KM, Magnasco MO. Harshlight: a "corrective make-up" program for microarray chips. BMC Bioinformatics 2005;6:294.
47. Wu Z, Irizarry R, Gentleman R, Martinez-Murillo F, Spencer F. A model-based background adjustment for oligonucleotide expression arrays. J Am Stat Assoc 2004;99:909-17.
48. Chen C, Grennan K, Badner J, Zhang D, Gershon E, Jin L, et al. Removing batch effects in analysis of expression microarray data: an evaluation of six batch adjustment methods. PLoS One 2011;6:e17238.
49. Johnson WE, Li C, Rabinovic A. Adjusting batch effects in microarray expression data using empirical Bayes methods. Biostatistics 2007;8:118-27.
50. Ohmatsu H, Humme D, Gulati N, Gonzalez J, Mobs M, Suarez-Farinas M, et al. IL32 is progressively expressed in mycosis fungoides independent of helper Tcell 2 and helper T-cell 9 polarization. Cancer Immunol Res 2014;2:890-900.
51. Shimomura Y, Ito M. Human hair keratin-associated proteins. J Investig Dermatol Symp Proc 2005;10:230-3.
52. Schweizer J, Langbein L, Rogers MA, Winter H. Hair follicle-specific keratins and their diseases. Exp Cell Res 2007;313:2010-20.
53. Krueger JG, Fretzin S, Suarez-Farinas M, Haslett PA, Phipps KM, Cameron GS, et al. IL-17A is essential for cell activation and inflammatory gene circuits in subjects with psoriasis. J Allergy Clin Immunol 2012;130:145-54.e9.
54. Price VH. Topical minoxidil (3%) in extensive alopecia areata, including longterm efficacy. J Am Acad Dermatol 1987;16:737-44.
55. Barahmani N, Schabath MB, Duvic M, Registry NAA. History of atopy or autoimmunity increases risk of alopecia areata. J Am Acad Dermatol 2009; 61:581-91.
56. Lee NR, Kim BK, Yoon NY, Lee SY, Ahn SY, Lee WS. Differences in comorbidity profiles between early-onset and late-onset alopecia areata patients: a retrospective study of 871 Korean patients. Ann Dermatol 2014;26:722-6.
57. Chu SY, Chen YJ, Tseng WC, Lin MW, Chen TJ, Hwang CY, et al. Comorbidity profiles among patients with alopecia areata: the importance of onset age, a nationwide population-based study. J Am Acad Dermatol 2011;65: 949-56.
58. Betz RC, Pforr J, Flaquer A, Redler S, Hanneken S, Eigelshoven S, et al. Loss-offunction mutations in the filaggrin gene and alopecia areata: strong risk factor for a severe course of disease in patients comorbid for atopic disease. J Invest Dermatol 2007;127:2539-43.
59. Richmond J, Tuzova M, Cruikshank W, Center D. Regulation of cellular processes by interleukin-16 in homeostasis and cancer. J Cell Physiol 2014;229: 139-47.
60. Lee S, Kaneko H, Sekigawa I, Tokano Y, Takasaki Y, Hashimoto H. Circulating interleukin-16 in systemic lupus erythematosus. Br J Rheumatol 1998;37:1334-7.
61. Lew BL, Chung JH, Sim WY. Association between IL16 gene polymorphisms and susceptibility to alopecia areata in the Korean population. Int J Dermatol 2014;53:319-22.
62. 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.
63. Schafer P. Apremilast mechanism of action and application to psoriasis and psoriatic arthritis. Biochem Pharmacol 2012;83:1583-90.
64. Busa S, Kavanaugh A. Drug safety evaluation of apremilast for treating psoriatic arthritis. Expert Opin Drug Saf 2015;14:979-85.
65. Samrao A, Berry TM, Goreshi R, Simpson EL. A pilot study of an oral phosphodiesterase inhibitor (apremilast) for atopic dermatitis in adults. Arch Dermatol 2012;148:890-7.
66. Keren A, Shemer A, Ullmann Y, Paus R, Gilhar A. The PDE4 inhibitor, apremilast, suppresses experimentally induced alopecia areata in human skin in vivo. J Dermatol Sci 2015;77:74-6.
67. Kanda N, Watanabe S. IL-12, IL-23, and IL-27 enhance human beta-defensin-2 production in human keratinocytes. Eur J Immunol 2008;38:1287-96.
68. Chan JR, 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.
69. Yu M, Kissling S, Freyschmidt-Paul P, Hoffmann R, Shapiro J, McElwee KJ. Interleukin-6 cytokine family member oncostatin M is a hair-follicle-expressed factor with hair growth inhibitory properties. Exp Dermatol 2008;17:12-9.
70. Philpott MP, Sanders DA, Bowen J, Kealey T. Effects of interleukins, colonystimulating 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.
71. Kim CD, Choe Y, Shim C, Kim K. Interferon Beta secreted from human hair dermal papilla cells inhibits the growth of outer root sheath cells cultured in vitro. Biochem Biophys Res Commun 2002;290:1133-8.
72. Ito T, Ito N, Saathoff M, Bettermann A, Takigawa M, Paus R. Interferon-gamma is a potent inducer of catagen-like changes in cultured human anagen hair follicles. Br J Dermatol 2005;152:623-31.
73. Tauber M, Buche S, Reygagne P, Berthelot JM, Aubin F, Ghislain PD, et al. Alopecia areata occurring during anti-TNF therapy: a national multicenter prospective study. J Am Acad Dermatol 2014;70:1146-9.
74. Howell MD, Kim BE, Gao P, Grant AV, Boguniewicz M, Debenedetto A, et al. Cytokine modulation of atopic dermatitis filaggrin skin expression. J Allergy Clin Immunol 2007;120:150-5.
75. Kim BE, Leung DY, Boguniewicz M, Howell MD. Loricrin and involucrin expression is down-regulated by Th2 cytokines through STAT-6. Clin Immunol 2008;126:332-7.
76. Omori-Miyake M, Yamashita M, Tsunemi Y, Kawashima M, Yagi J. In vitro assessment of IL-4-or IL-13-mediated changes in the structural components of keratinocytes in mice and humans. J Invest Dermatol 2014;134:1342-50.
77. 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.
78. 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.
79. 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.
80. Noda S, Krueger JG, Guttman-Yassky E. The translational revolution and use of biologics in patients with inflammatory skin diseases. J Allergy Clin Immunol 2015;135:324-36.
81. Suárez-Fariñas M, Ungar B, Correa da Rosa J, Ewald DA, Rozenblit M, Xu H, et al. RNA sequencing atopic dermatitis transcriptome profiling provides insights into novel disease mechanisms with potential therapeutic implications. J Allergy Clin Immunol 2015;135:1218-27.
82. Czarnowicki T, Krueger JG, Guttman-Yassky E. Skin barrier and immune dysregulation in atopic dermatitis: an evolving story with important clinical implications. J Allergy Clin Immunol Pract 2014;2:371-81.
83. Tintle S, Shemer A, Suárez-Fariñas M, Fujita H, Gilleaudeau P, Sullivan-Whalen M, et al. Reversal of atopic dermatitis with narrow-band UVB phototherapy and biomarkers for therapeutic response. J Allergy Clin Immunol 2011;128:583-93, e1-4.
84. Malajian D, Guttman-Yassky E. New pathogenic and therapeutic paradigms in atopic dermatitis. Cytokine 2015;73:311-8.
85. Hirota R, Tajima S, Yoneda Y, Tamayama T, Watanabe M, Ueda K, et al. Alopecia of IFN-gamma knockout mouse as a model for disturbance of the hair cycle: a unique arrest of the hair cycle at the anagen phase accompanied by mitosis. J Interferon Cytokine Res 2002;22:935-45.
86. Inui S, Noguchi F, Nakajima T, Itami S. Serum thymus and activation-regulated chemokine as disease activity and response biomarker in alopecia areata. J Dermatol 2013;40:881-5.
87. Coda AB, Sinha AA. Integration of genome-wide transcriptional and genetic profiles provides insights into disease development and clinical heterogeneity in alopecia areata. Genomics 2011;98:431-9.
88. Shohat M, Mimouni D, Ben-Amitai D, Sredni B, Sredni D, Shohat B, et al. In vitro cytokine profile in childhood alopecia areata and the immunomodulatory effects of AS-101. Clin Exp Dermatol 2005;30:432-4.
89. Jagielska D, Redler S, Brockschmidt FF, Herold C, Pasternack SM, Garcia Bartels N, et al. Follow-up study of the first genome-wide association scan in alopecia areata: IL13 and KIAA0350 as susceptibility loci supported with genome-wide significance. J Invest Dermatol 2012;132:2192-7.
90. Kalkan G, Karakus N, Bas Y, Takç Z, Ozuguz P, Ates O, et al. The association between Interleukin (IL)-4 gene intron 3 VNTR polymorphism and alopecia areata (AA) in Turkish population. Gene 2013;527:565-9.
91. Betz RC, Petukhova L, Ripke S, Huang H, Menelaou A, Redler S, et al. Genomewide meta-analysis in alopecia areata resolves HLA associations and reveals two new susceptibility loci. Nat Commun 2015;6:5966.
92. McPhee CG, Duncan FJ, Silva KA, King LE, Hogenesch H, Roopenian DC, et al. Increased expression of Cxcr3 and its ligands, Cxcl9 and Cxcl10, during the development of alopecia areata in the mouse. J Invest Dermatol 2012;132:1736-8.
93. Beck LA, Thaci D, Hamilton JD, Graham NM, Bieber T, Rocklin R, et al. Dupilumab treatment in adults with moderate-to-severe atopic dermatitis. N Engl J Med 2014;371:130-9.
94. Hamilton JD, Suarez-Farinas M, Dhingra N, Cardinale I, Li X, Kostic A, et al. Dupilumab improves the molecular signature in skin of patients with moderateto-severe atopic dermatitis. J Allergy Clin Immunol 2014;134:1293-300.
95. Haider AS, Lowes MA, Suarez-Farinas M, Zaba LC, Cardinale I, Khatcherian A, et al. Identification of cellular pathways of "type 1, " Th17 T cells, and TNF-and inducible nitric oxide synthase-producing dendritic cells in autoimmune inflammation through pharmacogenomic study of cyclosporine A in psoriasis. J Immunol 2008;180:1913-20.
96. Sofen H, Smith S, Matheson RT, Leonardi CL, Calderon C, Brodmerkel C, et al. Guselkumab (an IL-23-specific mAb) demonstrates clinical and molecular response in patients with moderate-to-severe psoriasis. J Allergy Clin Immunol 2014;133:1032-40.
97. Krueger JG, Ferris LK, Menter A, Wagner F, White A, Visvanathan S, et al. Anti-IL-23A mAb BI 655066 for treatment of moderate-to-severe psoriasis: Safety, efficacy, pharmacokinetics, and biomarker results of a single-risingdose, randomized, double-blind, placebo-controlled trial. J Allergy Clin Immunol 2015;136:116-24.e7.
98. Papp KA, Leonardi C, Menter A, Ortonne JP, Krueger JG, Kricorian G, et al. Brodalumab, an anti-interleukin-17-receptor antibody for psoriasis. N Engl J Med 2012;366:1181-9.
99. Harden J.L. Johnson-Huang L.M. Chamian M.F. Lee E. Pearce T. Leonardi C.L. et al., Humanized anti-IFN-g (HuZAF) in the treatment of psoriasis. J Allergy Clin Immunol. 2015;135:553-556.
100. Haan C, Rolvering C, Raulf F, Kapp M, Druckes P, Thoma G, et al. Jak1 has a dominant role over Jak3 in signal transduction through gc-containing cytokine receptors. Chem Biol 2011;18:314-23.
101. Bao L, Zhang H, Chan LS. The involvement of the JAK-STAT signaling pathway in chronic inflammatory skin disease atopic dermatitis. JAKSTAT 2013;2:e24137.
102. Fridman JS, Scherle PA, Collins R, Burn T, Neilan CL, Hertel D, et al. Preclinical evaluation of local JAK1 and JAK2 inhibition in cutaneous inflammation. J Invest Dermatol 2011;131:1838-44.
103. Craiglow BG, King BA. Killing two birds with one stone: oral tofacitinib reverses alopecia universalis in a patient with plaque psoriasis. J Invest Dermatol 2014; 134:2988-90.
104. Tojo G, Fujimura T, Kawano M, Ogasawara K, Kambayashi Y, Furudate S, et al. Comparison of interleukin-17-producing cells in different clinical types of alopecia areata. Dermatology 2013;227:78-82.
105. Mohan GC, Silverberg JI. Association of vitiligo and alopecia areata with atopic dermatitis: a systematic review and meta-analysis. JAMA Dermatol 2015;151: 522-8.
106. Yamakoshi T, Andoh T, Makino T, Kuraishi Y, Shimizu T. Clinical and histopathological features of itch in patients with alopecia areata. Acta Derm Venereol 2013;93:575-6.
107. Attia EA, El Shennawy D, Sefin A. Serum Interleukin-4 and total immunoglobulin E in nonatopic alopecia areata patients and HLA-DRB1 typing. Dermatol Res Pract 2010;2010:503587.
108. Kasumagic-Halilovic E, Prohic A. Serum levels of total immunoglobulin e in patients with alopecia areata: relationship with clinical type of the disease. Acta Dermatovenerol Croat 2006;14:149-52.
109. Zhang B, Zhao Y, Cai Z, Caulloo S, McElwee KJ, Li Y, et al. Early stage alopecia areata is associated with inflammation in the upper dermis and damage to the hair follicle infundibulum. Australas J Dermatol 2013;54:184-91.
110. Corren J, Lemanske RF, Hanania NA, Korenblat PE, Parsey MV, Arron JR, et al. Lebrikizumab treatment in adults with asthma. N Engl J Med 2011;365:1088-98.
111. Piper E, Brightling C, Niven R, Oh C, Faggioni R, Poon K, et al. A phase II placebo-controlled study of tralokinumab in moderate-to-severe asthma Eur Respir J 2013;41:330-8.
112. Andrisani G, Marzo M, Celleno L, Guidi L, Papa A, Gasbarrini A, et al. Development of psoriasis scalp with alopecia during treatment of Crohns disease with infliximab and rapid response to both diseases to ustekinumab. Eur Rev Med Pharmacol Sci 2013;17 2831-6.