Seminars in Immunopathology

, Volume 38, Issue 1, pp 123–133 | Cite as

The continuing evolution of targeted therapy for inflammatory skin disease

Review
First Online:
Received:
Accepted:

Abstract

Treatment of inflammatory skin disease has evolved from non-specific suppression of immune cells to increasingly precise targeting and modulation of immune mechanisms at all levels. This has led to dramatic treatment successes and deepened understanding of the pathophysiology. The cycle of in vitro studies, animal models, clinical trials, and case series of non-primary indications is a feedback loop that informs and guides the design of ever better disease models and therapeutic targets. Not only are we constantly discovering new molecules driving skin inflammation, we have also found that psoriasis and other autoimmune conditions are driven by distinct mediators occurring in early and late phases, which could be an opportunity for phase-specific or multipronged interventions. The deeper our mechanistic understanding, the more likely we will be able to discover subtle strategies to reprogram each patients’ immune cells without having to dampen or eliminate their protective effects against pathogens and tumors. Lastly, ongoing genomic studies might soon confirm interesting genetic markers for predictive personalized medicine, the earliest currently being evaluated in psoriasis such as HLA-Cw6 and TNFAIP3. Taken together, the continued evolution of immune therapies in skin will potentially allow an unprecedented form of medicine that is not bent on silencing the pathogenic mechanism, but rather aims at using subtle interventions to shepherd the immune cell swarm back on the correct path.

Keywords

Biologics Inflammation Swarm Combined Phase-specific 
This is a preview of subscription content, log in to check access.

Notes

Financial Disclosure

None of the authors have relevant financial relationships to this manuscript.

References

  1. 1.
    Noda S, Krueger JG, Guttman-Yassky E (2015) The translational revolution and use of biologics in patients with inflammatory skin diseases. J Allergy Clin Immunol 135:324–336PubMedCrossRefGoogle Scholar
  2. 2.
    Bieber T (2008) Atopic dermatitis. N Engl J Med 358:1483–1494PubMedCrossRefGoogle Scholar
  3. 3.
    Nestle FO, Kaplan DH, Barker J (2009) Psoriasis. N Engl J Med 361:496–509PubMedCrossRefGoogle Scholar
  4. 4.
    Henseler T, Christophers E (1985) Psoriasis of early and late onset: characterization of two types of psoriasis vulgaris. J Am Acad Dermatol 13:450–456PubMedCrossRefGoogle Scholar
  5. 5.
    van Kempen TS, Wenink MH, Leijten EF, Radstake TR, Boes M. Perception of self: distinguishing autoimmunity from autoinflammation. Nat Rev Rheumatol 2015Google Scholar
  6. 6.
    Christophers E, Metzler G, Rocken M (2014) Bimodal immune activation in psoriasis. Br J Dermatol 170:59–65PubMedCrossRefGoogle Scholar
  7. 7.
    Kakeda M, Schlapbach C, Danelon G et al (2014) Innate immune cells express IL-17A/F in acute generalized exanthematous pustulosis and generalized pustular psoriasis. Arch Dermatol Res 306:933–938PubMedCrossRefGoogle Scholar
  8. 8.
    Nestle FO, Conrad C, Tun-Kyi A et al (2005) Plasmacytoid predendritic cells initiate psoriasis through interferon-alpha production. J Exp Med 202:135–143PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    Schubert C, Christophers E (1985) Mast cells and macrophages in early relapsing psoriasis. Arch Dermatol Res 277:352–358PubMedCrossRefGoogle Scholar
  10. 10.
    Biedermann T, Kneilling M, Mailhammer R et al (2000) Mast cells control neutrophil recruitment during T cell-mediated delayed-type hypersensitivity reactions through tumor necrosis factor and macrophage inflammatory protein 2. J Exp Med 192:1441–1452PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Tamagawa-Mineoka R, Okuzawa Y, Masuda K, Katoh N (2014) Increased serum levels of interleukin 33 in patients with atopic dermatitis. J Am Acad Dermatol 70:882–888PubMedCrossRefGoogle Scholar
  12. 12.
    Kim BS, Siracusa MC, Saenz SA et al (2013) TSLP elicits IL-33-independent innate lymphoid cell responses to promote skin inflammation. Sci Transl Med 5:170ra16PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Rank MA, Kobayashi T, Kozaki H, Bartemes KR, Squillace DL, Kita H (2009) IL-33-activated dendritic cells induce an atypical TH2-type response. J Allergy Clin Immunol 123:1047–1054PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    Maier E, Werner D, Duschl A, Bohle B, Horejs-Hoeck J (2014) Human Th2 but not Th9 cells release IL-31 in a STAT6/NF-kappaB-dependent way. J Immunol (Baltimore, Md : 1950) 193:645–654CrossRefGoogle Scholar
  15. 15.
    Bieber T (2010) Atopic dermatitis. Ann Dermatol 22:125–137PubMedPubMedCentralCrossRefGoogle Scholar
  16. 16.
    Eichenfield LF, Tom WL, Chamlin SL et al (2014) Guidelines of care for the management of atopic dermatitis: section 1. Diagnosis and assessment of atopic dermatitis. J Am Acad Dermatol 70:338–351PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Harden JL, Johnson-Huang LM, Chamian MF et al (2015) Humanized anti-IFN-gamma (HuZAF) in the treatment of psoriasis. J Allergy Clin Immunol 135:553–556PubMedCrossRefGoogle Scholar
  18. 18.
    Guttman-Yassky E, Lowes MA, Fuentes-Duculan J et al (2007) Major differences in inflammatory dendritic cells and their products distinguish atopic dermatitis from psoriasis. J Allergy Clin Immunol 119:1210–1217PubMedCrossRefGoogle Scholar
  19. 19.
    Lazarevic V, Glimcher LH (2011) T-bet in disease. Nat Immunol 12:597–606PubMedCrossRefGoogle Scholar
  20. 20.
    Johnson-Huang LM, Suarez-Farinas M, Pierson KC et al (2012) A single intradermal injection of IFN-gamma induces an inflammatory state in both non-lesional psoriatic and healthy skin. J Invest Dermatol 132:1177–1187PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    Conrad C, Boyman O, Tonel G et al (2007) Alpha1beta1 integrin is crucial for accumulation of epidermal T cells and the development of psoriasis. Nat Med 13:836–842PubMedCrossRefGoogle Scholar
  22. 22.
    Perera GK, Ainali C, Semenova E et al (2014) Integrative biology approach identifies cytokine targeting strategies for psoriasis. Sci Transl Med 6:223ra22PubMedCrossRefGoogle Scholar
  23. 23.
    Taylor PR, Roy S, Leal SM Jr et al (2014) Activation of neutrophils by autocrine IL-17A-IL-17RC interactions during fungal infection is regulated by IL-6, IL-23, RORgammat and dectin-2. Nat Immunol 15:143–151PubMedPubMedCentralCrossRefGoogle Scholar
  24. 24.
    Guttman-Yassky E, Nograles KE, Krueger JG (2011) Contrasting pathogenesis of atopic dermatitis and psoriasis—part II: immune cell subsets and therapeutic concepts. J Allergy Clin Immunol 127:1420–1432PubMedCrossRefGoogle Scholar
  25. 25.
    Mansouri B, Richards L, Menter A (2014) Treatment of two patients with generalized pustular psoriasis with the interleukin-1beta inhibitor gevokizumab. Br J DermatolGoogle Scholar
  26. 26.
    Saggini A, Chimenti S, Chiricozzi A (2014) IL-6 as a druggable target in psoriasis: focus on pustular variants. J Immunol Res 2014:964069PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Prat L, Bouaziz JD, Wallach D, Vignon-Pennamen MD, Bagot M (2014) Neutrophilic dermatoses as systemic diseases. Clin Dermatol 32:376–388PubMedCrossRefGoogle Scholar
  28. 28.
    Acosta-Rodriguez EV, Napolitani G, Lanzavecchia A, Sallusto F (2007) Interleukins 1beta and 6 but not transforming growth factor-beta are essential for the differentiation of interleukin 17-producing human T helper cells. Nat Immunol 8:942–949PubMedCrossRefGoogle Scholar
  29. 29.
    Oldhoff JM, Darsow U, Werfel T et al (2006) No effect of anti-interleukin-5 therapy (mepolizumab) on the atopy patch test in atopic dermatitis patients. Int Arch Allergy Immunol 141:290–294PubMedCrossRefGoogle Scholar
  30. 30.
    Oldhoff JM, Darsow U, Werfel T et al (2005) Anti-IL-5 recombinant humanized monoclonal antibody (mepolizumab) for the treatment of atopic dermatitis. Allergy 60:693–696PubMedCrossRefGoogle Scholar
  31. 31.
    Hamilton JD, Suarez-Farinas M, Dhingra N et al (2014) Dupilumab improves the molecular signature in skin of patients with moderate-to-severe atopic dermatitis. J Allergy Clin Immunol 134:1293–1300PubMedCrossRefGoogle Scholar
  32. 32.
    Beck LA, Thaci D, Hamilton JD et al (2014) Dupilumab treatment in adults with moderate-to-severe atopic dermatitis. N Engl J Med 371:130–139PubMedCrossRefGoogle Scholar
  33. 33.
    Simon D, Hosli S, Kostylina G, Yawalkar N, Simon HU (2008) Anti-CD20 (rituximab) treatment improves atopic eczema. J Allergy Clin Immunol 121:122–128PubMedCrossRefGoogle Scholar
  34. 34.
    Navarini AA, French LE, Hofbauer GF (2011) Interrupting IL-6-receptor signaling improves atopic dermatitis but associates with bacterial superinfection. J Allergy Clin Immunol 128:1128–1130PubMedCrossRefGoogle Scholar
  35. 35.
    Hunter CA, Jones SA (2015) IL-6 as a keystone cytokine in health and disease. Nat Immunol 16:448–457PubMedCrossRefGoogle Scholar
  36. 36.
    Schmitt E, Klein M, Bopp T (2014) Th9 cells, new players in adaptive immunity. Trends Immunol 35:61–68PubMedCrossRefGoogle Scholar
  37. 37.
    Licona-Limon P, Henao-Mejia J, Temann AU et al (2013) Th9 cells drive host immunity against gastrointestinal worm infection. Immunity 39:744–757PubMedCrossRefGoogle Scholar
  38. 38.
    Schlapbach C, Gehad A, Yang C et al (2014) Human TH9 cells are skin-tropic and have autocrine and paracrine proinflammatory capacity. Sci Transl Med 6:219ra8PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    Turner JE, Morrison PJ, Wilhelm C et al (2013) IL-9-mediated survival of type 2 innate lymphoid cells promotes damage control in helminth-induced lung inflammation. J Exp Med 210:2951–2965PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Wilhelm C, Hirota K, Stieglitz B et al (2011) An IL-9 fate reporter demonstrates the induction of an innate IL-9 response in lung inflammation. Nat Immunol 12:1071–1077PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    Oh CK, Leigh R, McLaurin KK, Kim K, Hultquist M, Molfino NA (2013) A randomized, controlled trial to evaluate the effect of an anti-interleukin-9 monoclonal antibody in adults with uncontrolled asthma. Respir Res 14:93PubMedPubMedCentralCrossRefGoogle Scholar
  42. 42.
    Ghoreschi K, Thomas P, Breit S et al (2003) Interleukin-4 therapy of psoriasis induces Th2 responses and improves human autoimmune disease. Nat Med 9:40–46PubMedCrossRefGoogle Scholar
  43. 43.
    Reich K, Garbe C, Blaschke V et al (2001) Response of psoriasis to interleukin-10 is associated with suppression of cutaneous type 1 inflammation, downregulation of the epidermal interleukin-8/CXCR2 pathway and normalization of keratinocyte maturation. J Invest Dermatol 116:319–329PubMedCrossRefGoogle Scholar
  44. 44.
    Trepicchio WL, Ozawa M, Walters IB et al (1999) Interleukin-11 therapy selectively downregulates type I cytokine proinflammatory pathways in psoriasis lesions. J Clin Invest 104:1527–1537PubMedPubMedCentralCrossRefGoogle Scholar
  45. 45.
    Guenova E, Skabytska Y, Hoetzenecker W et al (2015) IL-4 abrogates T(H)17 cell-mediated inflammation by selective silencing of IL-23 in antigen-presenting cells. Proc Natl Acad Sci U S A 112:2163–2168PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Lammermann T, Afonso PV, Angermann BR et al (2013) Neutrophil swarms require LTB4 and integrins at sites of cell death in vivo. Nature 498:371–375PubMedCrossRefGoogle Scholar
  47. 47.
    Clark RA (2011) Gone but not forgotten: lesional memory in psoriatic skin. J Invest Dermatol 131:283–285PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Eyerich S, Onken AT, Weidinger S et al (2011) Mutual antagonism of T cells causing psoriasis and atopic eczema. N Engl J Med 365:231–238PubMedCrossRefGoogle Scholar
  49. 49.
    Kroemer G, Galluzzi L (2015) Combinatorial immunotherapy with checkpoint blockers solves the problem of metastatic melanoma—an exclamation sign with a question mark. Oncoimmunology 4:e1058037PubMedCrossRefGoogle Scholar
  50. 50.
    Wolchok JD, Kluger H, Callahan MK et al (2013) Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med 369:122–133PubMedCrossRefGoogle Scholar
  51. 51.
    Chiricozzi A, Guttman-Yassky E, Suarez-Farinas M et al (2011) Integrative responses to IL-17 and TNF-alpha in human keratinocytes account for key inflammatory pathogenic circuits in psoriasis. J Invest Dermatol 131:677–687PubMedCrossRefGoogle Scholar
  52. 52.
    Sutton CE, Lalor SJ, Sweeney CM, Brereton CF, Lavelle EC, Mills KH (2009) Interleukin-1 and IL-23 induce innate IL-17 production from gammadelta T cells, amplifying Th17 responses and autoimmunity. Immunity 31:331–341PubMedCrossRefGoogle Scholar
  53. 53.
    Thaci D, Ortonne JP, Chimenti S et al (2010) A phase IIIb, multicentre, randomized, double-blind, vehicle-controlled study of the efficacy and safety of adalimumab with and without calcipotriol/betamethasone topical treatment in patients with moderate to severe psoriasis: the BELIEVE study. Br J Dermatol 163:402–411PubMedCrossRefGoogle Scholar
  54. 54.
    Tsapas A, Matthews DR (2009) Using N-of-1 trials in evidence-based clinical practice. JAMA 301:1022–1023, author reply 3 PubMedCrossRefGoogle Scholar
  55. 55.
    Clark RA, Watanabe R, Teague JE et al (2012) Skin effector memory T cells do not recirculate and provide immune protection in alemtuzumab-treated CTCL patients. Sci Transl Med 4:117ra7PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Hernandez MV, Nogues S, Ruiz-Esquide V, Alsina M, Canete JD, Sanmarti R (2009) Development of alopecia areata after biological therapy with TNF-alpha blockers: description of a case and review of the literature. Clin Exp Rheumatol 27:892–893PubMedGoogle Scholar
  57. 57.
    Tauber M, Beneton N, Reygagne P, Bachelez H, Viguier M (2013) Alopecia areata developing during ustekinumab therapy: report of two cases. Eur J Dermatol : EJD 23:912–913PubMedGoogle Scholar
  58. 58.
    Price VH, Hordinsky MK, Olsen EA et al (2008) Subcutaneous efalizumab is not effective in the treatment of alopecia areata. J Am Acad Dermatol 58:395–402PubMedCrossRefGoogle Scholar
  59. 59.
    Strober BE, Menon K, McMichael A et al (2009) Alefacept for severe alopecia areata: a randomized, double-blind, placebo-controlled study. Arch Dermatol 145:1262–1266PubMedCrossRefGoogle Scholar
  60. 60.
    Wright RC (2003) Atopic dermatitis-like eruption precipitated by infliximab. J Am Acad Dermatol 49:160–161PubMedCrossRefGoogle Scholar
  61. 61.
    Samorano LP, Hanifin JM, Simpson EL, Leshem YA (2014) Inadequate response to ustekinumab in atopic dermatitis—a report of two patients. J Eur Acad Dermatol Venereol : JEADVGoogle Scholar
  62. 62.
    Fernandez-Anton Martinez MC, Alfageme Roldan F, Ciudad Blanco C, Suarez FR (2014) Ustekinumab in the treatment of severe atopic dermatitis: a preliminary report of our experience with 4 patients. Actas Dermosifiliogr 105:312–313PubMedCrossRefGoogle Scholar
  63. 63.
    Sanchez-Ramon S, Eguiluz-Gracia I, Rodriguez-Mazariego ME et al (2013) Sequential combined therapy with omalizumab and rituximab: a new approach to severe atopic dermatitis. J Investig Allergol Clin Immunol 23:190–196PubMedGoogle Scholar
  64. 64.
    Ibler K, Dam TN, Gniadecki R, Kragballe K, Jemec GB, Agner T (2010) Efalizumab for severe refractory atopic eczema: retrospective study on 11 cases. J Eur Acad Dermatol Venereol : JEADV 24:837–839PubMedCrossRefGoogle Scholar
  65. 65.
    Moul DK, Routhouska SB, Robinson MR, Korman NJ (2008) Alefacept for moderate to severe atopic dermatitis: a pilot study in adults. J Am Acad Dermatol 58:984–989PubMedCrossRefGoogle Scholar
  66. 66.
    Cantarini L, Lopalco G, Caso F et al (2015) Effectiveness and tuberculosis-related safety profile of interleukin-1 blocking agents in the management of Behcet’s disease. Autoimmun Rev 14:1–9PubMedCrossRefGoogle Scholar
  67. 67.
    Addimanda O, Pipitone N, Pazzola G, Salvarani C (2015) Tocilizumab for severe refractory neuro-Behcet: three cases IL-6 blockade in neuro-Behcet. Semin Arthritis Rheum 44:472–475PubMedCrossRefGoogle Scholar
  68. 68.
    Vallet H, Riviere S, Sanna A et al (2015) Efficacy of anti-TNF alpha in severe and/or refractory Behcet’s disease: multicenter study of 124 patients. J Autoimmun 62:67–74PubMedCrossRefGoogle Scholar
  69. 69.
    Baerveldt EM, Kappen JH, Thio HB, van Laar JA, van Hagen PM, Prens EP (2013) Successful long-term triple disease control by ustekinumab in a patient with Behcet’s disease, psoriasis and hidradenitis suppurativa. Ann Rheum Dis 72:626–627PubMedCrossRefGoogle Scholar
  70. 70.
    Davatchi F, Shams H, Rezaipoor M et al (2010) Rituximab in intractable ocular lesions of Behcet’s disease; randomized single-blind control study (pilot study). Int J Rheum Dis 13:246–252PubMedCrossRefGoogle Scholar
  71. 71.
    Ricci M, Zauli S, Zelante A, Trevisani L, Virgili A, Bettoli V (2014) Bullous pemphigoid occurring under anti-tumor necrosis factor-alpha therapy. Int J Color Dis 29:1573–1574CrossRefGoogle Scholar
  72. 72.
    Nakayama C, Fujita Y, Watanabe M, Shimizu H (2015) Development of bullous pemphigoid during treatment of psoriatic onycho-pachydermo periostitis with ustekinumab. J DermatolGoogle Scholar
  73. 73.
    Majima Y, Yagi H, Tateishi C et al (2013) A successful treatment with ustekinumab in a case of antilaminin-gamma1 pemphigoid associated with psoriasis. Br J Dermatol 168:1367–1369PubMedCrossRefGoogle Scholar
  74. 74.
    Cho YT, Chu CY, Wang LF (2015) First-line combination therapy with rituximab and corticosteroids provides a high complete remission rate in moderate-to-severe bullous pemphigoid. Br J Dermatol 173:302–304PubMedCrossRefGoogle Scholar
  75. 75.
    Yu KK, Crew AB, Messingham KA, Fairley JA, Woodley DT (2014) Omalizumab therapy for bullous pemphigoid. J Am Acad Dermatol 71:468–474PubMedCrossRefGoogle Scholar
  76. 76.
    Monnier-Murina K, Du Thanh A, Merlet-Albran S, Guillot B, Dereure O (2009) Bullous pemphigoid occurring during efalizumab treatment for psoriasis: a paradoxical auto-immune reaction? Dermatology (Basel, Switzerland) 219:89–90CrossRefGoogle Scholar
  77. 77.
    Kondo M, Murakawa Y, Matsumura T et al (2014) A case of overlap syndrome successfully treated with tocilizumab: a hopeful treatment strategy for refractory dermatomyositis? Rheumatology (Oxford) 53:1907–1908CrossRefGoogle Scholar
  78. 78.
    Riley P, McCann LJ, Maillard SM, Woo P, Murray KJ, Pilkington CA (2008) Effectiveness of infliximab in the treatment of refractory juvenile dermatomyositis with calcinosis. Rheumatology (Oxford) 47:877–880CrossRefGoogle Scholar
  79. 79.
    Oddis CV, Reed AM, Aggarwal R et al (2013) Rituximab in the treatment of refractory adult and juvenile dermatomyositis and adult polymyositis: a randomized, placebo-phase trial. Arthritis Rheum 65:314–324PubMedPubMedCentralCrossRefGoogle Scholar
  80. 80.
    Huber A, Gaffal E, Bieber T, Tuting T, Wenzel J (2006) Treatment of recalcitrant dermatomyositis with efalizumab. Acta Derm Venereol 86:254–255PubMedCrossRefGoogle Scholar
  81. 81.
    Navarini AA, Trueb RM (2010) 3 cases of dissecting cellulitis of the scalp treated with adalimumab: control of inflammation within residual structural disease. Arch Dermatol 146:517–520PubMedGoogle Scholar
  82. 82.
    Amy de la Breteque M, Saussine A, Rybojad M, et al.(2014) Infliximab in recalcitrant granuloma annulare. Int J DermatolGoogle Scholar
  83. 83.
    Murdaca G, Colombo BM, Barabino G, Caiti M, Cagnati P, Puppo F (2010) Anti-tumor necrosis factor-alpha treatment with infliximab for disseminated granuloma annulare. Am J Clin Dermatol 11:437–439PubMedCrossRefGoogle Scholar
  84. 84.
    Shah BK, Hewett Y, Peterson A, Tretheway D (2014) Resolution of granuloma annulare following treatment with bendamustine and rituximab in a patient with follicular lymphoma: a serendipitous finding. J Postgrad Med 60:406–408PubMedCrossRefGoogle Scholar
  85. 85.
    Goffe BS (2004) Disseminated granuloma annulare resolved with the T-cell modulator efalizumab. Arch Dermatol 140:1287–1288PubMedCrossRefGoogle Scholar
  86. 86.
    Hellwig Y, Yoo YE, Ress ML, et al. (2015) Fulminant skin GvHD with a cytokine pattern resemblant of cytokine release syndrome successfully treated with multimodal immunosuppression including tocilizumab. Pediatr Blood CancerGoogle Scholar
  87. 87.
    Kennedy GA, Varelias A, Vuckovic S et al (2014) Addition of interleukin-6 inhibition with tocilizumab to standard graft-versus-host disease prophylaxis after allogeneic stem-cell transplantation: a phase 1/2 trial. Lancet Oncol 15:1451–1459PubMedCrossRefGoogle Scholar
  88. 88.
    Couriel DR, Saliba R, de Lima M et al (2009) A phase III study of infliximab and corticosteroids for the initial treatment of acute graft-versus-host disease. Biol Blood Marrow Transplant 15:1555–1562PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    Shapira MY, Resnick IB, Bitan M et al (2005) Rapid response to alefacept given to patients with steroid resistant or steroid dependent acute graft-versus-host disease: a preliminary report. Bone Marrow Transplant 36:1097–1101PubMedCrossRefGoogle Scholar
  90. 90.
    Hurd DS, Johnston C, Bevins A (2008) A case report of Hailey-Hailey disease treated with alefacept (Amevive). Br J Dermatol 158:399–401PubMedGoogle Scholar
  91. 91.
    Leslie KS, Tripathi SV, Nguyen TV, Pauli M, Rosenblum MD (2014) An open-label study of anakinra for the treatment of moderate to severe hidradenitis suppurativa. J Am Acad Dermatol 70:243–251PubMedCrossRefGoogle Scholar
  92. 92.
    Martin-Ezquerra G, Masferrer E, Masferrer-Niubo M et al (2015) Use of biological treatments in patients with hidradenitis suppurativa. J Eur Acad Dermatol Venereol : JEADV 29:56–60PubMedCrossRefGoogle Scholar
  93. 93.
    Strober BE, Kim C, Siu K (2007) Efalizumab for the treatment of refractory hidradenitis suppurativa. J Am Acad Dermatol 57:1090–1091PubMedCrossRefGoogle Scholar
  94. 94.
    Cohen PR, Kurzrock R (2014) Anakinra-responsive lichen planus in a woman with Erdheim-Chester disease: a therapeutic enigma. Dermatol Online J 20:21241PubMedGoogle Scholar
  95. 95.
    Asarch A, Gottlieb AB, Lee J et al (2009) Lichen planus-like eruptions: an emerging side effect of tumor necrosis factor-alpha antagonists. J Am Acad Dermatol 61:104–111PubMedCrossRefGoogle Scholar
  96. 96.
    Heelan K, McAleer MA, Roche L, McCreary C, Murphy M (2015) Intractable erosive lichen planus treated successfully with rituximab. Br J Dermatol 172:538–540PubMedCrossRefGoogle Scholar
  97. 97.
    Seeborg FO, Rihal PS, Czelusta A, Sanchez R, Hanson IC (2009) Lichen planus associated with omalizumab administration in an adult with allergic asthma. Ann Allergy Asthma Immunol 102:349–351PubMedCrossRefGoogle Scholar
  98. 98.
    Heffernan MP, Smith DI, Bentley D, Tabacchi M, Graves JE (2007) A single-center, open-label, prospective pilot study of subcutaneous efalizumab for oral erosive lichen planus. J Drugs Dermatol : JDD 6:310–314PubMedGoogle Scholar
  99. 99.
    Moosig F, Zeuner R, Renk C, Schroder JO (2004) IL-1RA in refractory systemic lupus erythematosus. Lupus 13:605–606PubMedCrossRefGoogle Scholar
  100. 100.
    Makol A, Gibson LE, Michet CJ (2012) Successful use of interleukin 6 antagonist tocilizumab in a patient with refractory cutaneous lupus and urticarial vasculitis. J Clin Rheumatol 18:92–95PubMedCrossRefGoogle Scholar
  101. 101.
    Subramanian S, Yajnik V, Sands BE, Cullen G, Korzenik JR (2011) Characterization of patients with infliximab-induced lupus erythematosus and outcomes after retreatment with a second anti-TNF agent. Inflamm Bowel Dis 17:99–104PubMedCrossRefGoogle Scholar
  102. 102.
    De Souza A, Ali-Shaw T, Strober BE, Franks AG Jr (2011) Successful treatment of subacute lupus erythematosus with ustekinumab. Arch Dermatol 147:896–898PubMedCrossRefGoogle Scholar
  103. 103.
    Navarini AA, Kerl K, French LE, Trueb RM (2010) Control of widespread hypertrophic lupus erythematosus with T-cell-directed biologic efalizumab. Dermatology (Basel, Switzerland) 220:249–253CrossRefGoogle Scholar
  104. 104.
    Berthelot C, Nash J, Duvic M (2007) Coexistent psoriasis and lupus erythematosus treated with alefacept. Am J Clin Dermatol 8:47–50PubMedCrossRefGoogle Scholar
  105. 105.
    Hertl MS, Haendle I, Schuler G, Hertl M (2005) Rapid improvement of recalcitrant disseminated granuloma annulare upon treatment with the tumour necrosis factor-alpha inhibitor, infliximab. Br J Dermatol 152:552–555PubMedCrossRefGoogle Scholar
  106. 106.
    Caso F, Iaccarino L, Bettio S et al (2013) Refractory pemphigus foliaceus and Behcet’s disease successfully treated with tocilizumab. Immunol Res 56:390–397PubMedCrossRefGoogle Scholar
  107. 107.
    Jacobi A, Shuler G, Hertl M (2005) Rapid control of therapy-refractory pemphigus vulgaris by treatment with the tumour necrosis factor-alpha inhibitor infliximab. Br J Dermatol 153:448–449PubMedCrossRefGoogle Scholar
  108. 108.
    Hall RP 3rd, Fairley J, Woodley D et al (2015) A multicentre randomized trial of the treatment of patients with pemphigus vulgaris with infliximab and prednisone compared with prednisone alone. Br J Dermatol 172:760–768PubMedCrossRefGoogle Scholar
  109. 109.
    Kanwar AJ, Vinay K, Sawatkar GU et al (2014) Clinical and immunological outcomes of high- and low-dose rituximab treatments in patients with pemphigus: a randomized, comparative, observer-blinded study. Br J Dermatol 170:1341–1349PubMedCrossRefGoogle Scholar
  110. 110.
    Santos-Juanes J, Coto-Segura P, Saavedra J, Laviano S, Galache C (2009) Development of familial benign chronic pemphigus in a patient undergoing treatment with efalizumab for psoriasis. J Eur Acad Dermatol Venereol : JEADV 23:605–606PubMedCrossRefGoogle Scholar
  111. 111.
    Adnot-Desanlis L, Antonicelli F, Tabary T, Bernard P, Reguiai Z (2013) Effectiveness of infliximab in pityriasis rubra pilaris is associated with pro-inflammatory cytokine inhibition. Dermatology (Basel, Switzerland) 226:41–46CrossRefGoogle Scholar
  112. 112.
    Wohlrab J, Kreft B (2010) Treatment of pityriasis rubra pilaris with ustekinumab. Br J Dermatol 163:655–656PubMedCrossRefGoogle Scholar
  113. 113.
    Klein A, Szeimies RM, Landthaler M, Karrer S (2007) Exacerbation of pityriasis rubra pilaris under efalizumab therapy. Dermatology (Basel, Switzerland) 215:72–75CrossRefGoogle Scholar
  114. 114.
    Gomez M, Ruelas ME, Welsh O, Arcaute HD, Ocampo-Candiani J (2007) Clinical improvement of pityriasis rubra pilaris with efalizumab in a pediatric patient. J Drugs Dermatol : JDD 6:337–339PubMedGoogle Scholar
  115. 115.
    Shima Y, Kuwahara Y, Murota H et al (2010) The skin of patients with systemic sclerosis softened during the treatment with anti-IL-6 receptor antibody tocilizumab. Rheumatology (Oxford) 49:2408–2412CrossRefGoogle Scholar
  116. 116.
    Elhai M, Meunier M, Matucci-Cerinic M et al (2013) Outcomes of patients with systemic sclerosis-associated polyarthritis and myopathy treated with tocilizumab or abatacept: a EUSTAR observational study. Ann Rheum Dis 72:1217–1220PubMedCrossRefGoogle Scholar
  117. 117.
    Phumethum V, Jamal S, Johnson SR (2011) Biologic therapy for systemic sclerosis: a systematic review. J Rheumatol 38:289–296PubMedCrossRefGoogle Scholar
  118. 118.
    Jordan S, Distler JH, Maurer B et al (2015) Effects and safety of rituximab in systemic sclerosis: an analysis from the European Scleroderma Trial and Research (EUSTAR) group. Ann Rheum Dis 74:1188–1194PubMedCrossRefGoogle Scholar
  119. 119.
    Chi GC, Hsu FS, Yang CC, Wei JC (2005) Scleroderma and failed response to alefacept. Rheumatology (Oxford) 44:1328–1330CrossRefGoogle Scholar
  120. 120.
    Gonzalez-Lopez MA, Martinez-Taboada VM, Gonzalez-Vela MC, Fernandez-Llaca H, Val-Bernal JF (2008) New-onset psoriasis following treatment with the interleukin-1 receptor antagonist anakinra. Br J Dermatol 158:1146–1148PubMedCrossRefGoogle Scholar
  121. 121.
    Palmou-Fontana N, Sanchez Gavino JA, McGonagle D, Garcia-Martinez E, Iniguezde Onzono Martin L (2014) Tocilizumab-induced psoriasiform rash in rheumatoid arthritis. Dermatology (Basel, Switzerland) 228:311–313CrossRefGoogle Scholar
  122. 122.
    Reich K, Nestle FO, Papp K et al (2005) Infliximab induction and maintenance therapy for moderate-to-severe psoriasis: a phase III, multicentre, double-blind trial. Lancet (London, England) 366:1367–1374CrossRefGoogle Scholar
  123. 123.
    Papp KA, Langley RG, Lebwohl M et al (2008) 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 (London, England) 371:1675–1684CrossRefGoogle Scholar
  124. 124.
    Langley RG, Elewski BE, Lebwohl M et al (2014) Secukinumab in plaque psoriasis—results of two phase 3 trials. N Engl J Med 371:326–338PubMedCrossRefGoogle Scholar
  125. 125.
    Toussirot E (2013) New onset of psoriasis in a patient with rheumatoid arthritis treated with rituximab. J Rheumatol 40:1230–1231PubMedCrossRefGoogle Scholar
  126. 126.
    Pariser DM, Gordon KB, Papp KA et al (2005) Clinical efficacy of efalizumab in patients with chronic plaque psoriasis: results from three randomized placebo-controlled phase III trials: part I. J Cutan Med Surg 9:303–312PubMedCrossRefGoogle Scholar
  127. 127.
    Ellis CN, Krueger GG (2001) Treatment of chronic plaque psoriasis by selective targeting of memory effector T lymphocytes. N Engl J Med 345:248–255PubMedCrossRefGoogle Scholar
  128. 128.
    Brenner M, Ruzicka T, Plewig G, Thomas P, Herzer P (2009) Targeted treatment of pyoderma gangrenosum in PAPA (pyogenic arthritis, pyoderma gangrenosum and acne) syndrome with the recombinant human interleukin-1 receptor antagonist anakinra. Br J Dermatol 161:1199–1201PubMedCrossRefGoogle Scholar
  129. 129.
    Acquitter M, Plantin P, Kupfer I, Auvinet H, Marhadour T (2015) Anakinra improves pyoderma gangrenosum in psoriatic arthritis: a case report. Ann Intern Med 163:70–71PubMedCrossRefGoogle Scholar
  130. 130.
    Brooklyn TN, Dunnill MG, Shetty A et al (2006) Infliximab for the treatment of pyoderma gangrenosum: a randomised, double blind, placebo controlled trial. Gut 55:505–509PubMedPubMedCentralCrossRefGoogle Scholar
  131. 131.
    Guenova E, Teske A, Fehrenbacher B et al (2011) Interleukin 23 expression in pyoderma gangrenosum and targeted therapy with ustekinumab. Arch Dermatol 147:1203–1205PubMedCrossRefGoogle Scholar
  132. 132.
    Kleinpenning MM, Langewouters AM, Van De Kerkhof PC, Greebe RJ (2011) Severe pyoderma gangrenosum unresponsive to etanercept and adalimumab. J Dermatolog Treat 22:261–265PubMedCrossRefGoogle Scholar
  133. 133.
    Selva-Nayagam P, Fischer G, Hamann I, Sobel J, James C (2015) Rituximab causing deep ulcerative suppurative vaginitis/pyoderma gangrenosum. Curr Infect Dis Rep 17:478PubMedCrossRefGoogle Scholar
  134. 134.
    Foss CE, Clark AR, Inabinet R, Camacho F, Jorizzo JL (2008) An open-label pilot study of alefacept for the treatment of pyoderma gangrenosum. J Eur Acad Dermatol Venereol : JEADV 22:943–949PubMedCrossRefGoogle Scholar
  135. 135.
    Nutz A, Pernet C, Combe B, Cohen JD (2013) Sarcoidosis induced by tocilizumab: a paradoxical event? J Rheumatol 40:1773–1774PubMedCrossRefGoogle Scholar
  136. 136.
    Rossman MD, Newman LS, Baughman RP et al (2006) A double-blinded, randomized, placebo-controlled trial of infliximab in subjects with active pulmonary sarcoidosis. Sarcoidosis Vasc Diffuse Lung Dis 23:201–208PubMedGoogle Scholar
  137. 137.
    Kaiser CA, Cozzio A, Hofbauer GF, Kamarashev J, French LE, Navarini AA (2011) Disfiguring annular sarcoidosis improved by adalimumab. Case Rep Dermatology 3:103–106CrossRefGoogle Scholar
  138. 138.
    Judson MA, Baughman RP, Costabel U et al (2014) Safety and efficacy of ustekinumab or golimumab in patients with chronic sarcoidosis. Eur Respir J 44:1296–1307PubMedCrossRefGoogle Scholar
  139. 139.
    Sweiss NJ, Lower EE, Mirsaeidi M et al (2014) Rituximab in the treatment of refractory pulmonary sarcoidosis. Eur Respir J 43:1525–1528PubMedPubMedCentralCrossRefGoogle Scholar
  140. 140.
    Garcia-Zuazaga J, Korman NJ (2006) Cutaneous sarcoidosis successfully treated with alefacept. J Cutan Med Surg 10:300–303PubMedCrossRefGoogle Scholar
  141. 141.
    Devauchelle-Pensec V, Mariette X, Jousse-Joulin S et al (2014) Treatment of primary Sjogren syndrome with rituximab: a randomized trial. Ann Intern Med 160:233–242PubMedCrossRefGoogle Scholar
  142. 142.
    Moutsopoulos NM, Katsifis GE, Angelov N et al (2008) Lack of efficacy of etanercept in Sjogren syndrome correlates with failed suppression of tumour necrosis factor alpha and systemic immune activation. Ann Rheum Dis 67:1437–1443PubMedCrossRefGoogle Scholar
  143. 143.
    Voigtlander C, Luftl M, Schuler G, Hertl M (2001) Infliximab (anti-tumor necrosis factor alpha antibody): a novel, highly effective treatment of recalcitrant subcorneal pustular dermatosis (Sneddon-Wilkinson disease). Arch Dermatol 137:1571–1574PubMedCrossRefGoogle Scholar
  144. 144.
    Sauder MB, Glassman SJ (2013) Palmoplantar subcorneal pustular dermatosis following adalimumab therapy for rheumatoid arthritis. Int J Dermatol 52:624–628PubMedCrossRefGoogle Scholar
  145. 145.
    Kluger N, Gil-Bistes D, Guillot B, Bessis D (2011) Efficacy of anti-interleukin-1 receptor antagonist anakinra (Kineret(R)) in a case of refractory Sweet’s syndrome. Dermatology (Basel, Switzerland) 222:123–127CrossRefGoogle Scholar
  146. 146.
    Foster EN, Nguyen KK, Sheikh RA, Prindiville TP (2005) Crohn’s disease associated with Sweet’s syndrome and Sjogren’s syndrome treated with infliximab. Clin Dev Immunol 12:145–149PubMedPubMedCentralCrossRefGoogle Scholar
  147. 147.
    Zarate-Correa LC, Carrillo-Gomez DC, Ramirez-Escobar AF, Serrano-Reyes C (2013) Toxic epidermal necrolysis successfully treated with infliximab. J Investig Allergol Clin Immunol 23:61–63PubMedGoogle Scholar
  148. 148.
    Lowndes S, Darby A, Mead G, Lister A (2002) Stevens-Johnson syndrome after treatment with rituximab. Ann Oncol 13:1948–1950PubMedCrossRefGoogle Scholar
  149. 149.
    (2005) Etanercept plus standard therapy for Wegener’s granulomatosis. N Engl J Med 352:351–61Google Scholar
  150. 150.
    Miloslavsky EM, Specks U, Merkel PA et al (2013) Clinical outcomes of remission induction therapy for severe antineutrophil cytoplasmic antibody-associated vasculitis. Arthritis Rheum 65:2441–2449PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Department of DermatologyUniversity of BernBernSwitzerland
  2. 2.Department of DermatologyUniversity Hospital of ZurichZurichSwitzerland

Personalised recommendations