Display options
Cite
Uppala R, Tsoi LC, Harms PW, et al. "Autoinflammatory psoriasis"-genetics and biology of pustular psoriasis. Cell Mol Immunol. 2020;18(2):307-317doi: 10.1038/s41423-020-0519-3.
Uppala, R., Tsoi, L. C., Harms, P. W., Wang, B., Billi, A. C., Maverakis, E., Michelle Kahlenberg, J., Ward, N. L., & Gudjonsson, J. E. (2021). "Autoinflammatory psoriasis"-genetics and biology of pustular psoriasis. Cellular & molecular immunology, 18(2), 307-317. https://doi.org/10.1038/s41423-020-0519-3
Uppala, Ranjitha, et al. ""Autoinflammatory psoriasis"-genetics and biology of pustular psoriasis." Cellular & molecular immunology vol. 18,2 (2021): 307-317. doi: https://doi.org/10.1038/s41423-020-0519-3
Uppala R, Tsoi LC, Harms PW, Wang B, Billi AC, Maverakis E, Michelle Kahlenberg J, Ward NL, Gudjonsson JE. "Autoinflammatory psoriasis"-genetics and biology of pustular psoriasis. Cell Mol Immunol. 2021 Feb;18(2):307-317. doi: 10.1038/s41423-020-0519-3. Epub 2020 Aug 19. PMID: 32814870; PMCID: PMC8027616.
Copy Download .nbib Format: NLM
Share it on

Cell Mol Immunol. 2021 Feb;18(2):307-317. doi: 10.1038/s41423-020-0519-3. Epub 2020 Aug 19.

"Autoinflammatory psoriasis"-genetics and biology of pustular psoriasis.

Cellular & molecular immunology

Ranjitha Uppala, Lam C Tsoi, Paul W Harms, Bo Wang, Allison C Billi, Emanual Maverakis, J Michelle Kahlenberg, Nicole L Ward, Johann E Gudjonsson

Affiliations

  1. Graduate Program in Immunology, University of Michigan, Ann Arbor, MI, USA.
  2. Department of Dermatology, University of Michigan, Ann Arbor, MI, USA.
  3. Department of Pathology, University of Michigan, Ann Arbor, MI, USA.
  4. Department of Dermatology, University of California, Davis, Sacramento, CA, USA.
  5. Division of Rheumatology, Department of Internal Medicine, University of Michigan, Ann Arbor, MI, USA.
  6. A. Alfred Taubman Medical Research Institute, Ann Arbor, MI, USA.
  7. Departments of Nutrition and Dermatology, Case Western Reserve University, Cleveland, OH, USA.
  8. Department of Dermatology, University of Michigan, Ann Arbor, MI, USA. [email protected].
  9. A. Alfred Taubman Medical Research Institute, Ann Arbor, MI, USA. [email protected].

PMID: 32814870 PMCID: PMC8027616 DOI: 10.1038/s41423-020-0519-3

Abstract

Psoriasis is a chronic inflammatory skin condition that has a fairly wide range of clinical presentations. Plaque psoriasis, which is the most common manifestation of psoriasis, is located on one end of the spectrum, dominated by adaptive immune responses, whereas the rarer pustular psoriasis lies on the opposite end, dominated by innate and autoinflammatory immune responses. In recent years, genetic studies have identified six genetic variants that predispose to pustular psoriasis, and these have highlighted the role of IL-36 cytokines as central to pustular psoriasis pathogenesis. In this review, we discuss the presentation and clinical subtypes of pustular psoriasis, contribution of genetic predisposing variants, critical role of the IL-36 family of cytokines in disease pathophysiology, and treatment perspectives for pustular psoriasis. We further outline the application of appropriate mouse models for the study of pustular psoriasis and address the outstanding questions and issues related to our understanding of the mechanisms involved in pustular psoriasis.

Keywords: Autoinflammation; Clinical features; Genetics; Histology; IL-36; Pustular psoriasis

References

  1. Sarac, G., Koca, T. T. & Baglan, T. A brief summary of clinical types of psoriasis. North Clin. Istanb. 3, 79–82 (2016). - PubMed
  2. Rendon, A. & Schakel, K. Psoriasis pathogenesis and treatment. Int. J. Mol. Sci. 20, 1475 (2019). - PubMed
  3. Nestle, F. O., Kaplan, D. H. & Barker, J. Psoriasis. N. Engl. J. Med. 361, 496–509 (2009). - PubMed
  4. Gudjonsson, J. E. & Elder, J. T. Psoriasis: epidemiology. Clin. Dermatol. 25, 535–546 (2007). - PubMed
  5. Gooderham, M. J., Van Voorhees, A. S. & Lebwohl, M. G. An update on generalized pustular psoriasis. Expert Rev. Clin. Immunol. 15, 907–919 (2019). - PubMed
  6. Bissonnette, R. et al. Palmoplantar pustular psoriasis (PPPP) is characterized by activation of the IL-17A pathway. J. Dermatol. Sci. 85, 20–26 (2017). - PubMed
  7. Twelves, S. et al. Clinical and genetic differences between pustular psoriasis subtypes. J. Allergy Clin. Immunol. 143, 1021–1026 (2019). - PubMed
  8. Bangale-Daflapurkar, S. & Danve, A. Pustular psoriasis of pregnancy successfully treated with cyclosporine. Am. J. Ther. 23, e1250–e1252 (2016). - PubMed
  9. Owczarczyk-Saczonek, A., Znajewska-Pander, A., Owczarek, W., Maciejewska-Radomska, A. & Placek, W. Clinicopathologic retrospective analysis of annular pustular psoriasis. Acta Dermatovenerol. Alp. Pannonica Adriat. 27, 215–219 (2018). - PubMed
  10. Huang, Y. W. & Tsai, T. F. Juvenile-onset pustular psoriasis: case series and literature review. Br. J. Dermatol. 182, 816–817 (2020). - PubMed
  11. Sanchez, N. P., Perry, H. O., Muller, S. A. & Winkelmann, R. K. Subcorneal pustular dermatosis and pustular psoriasis. A clinicopathologic correlation. Arch. Dermatol. 119, 715–721 (1983). - PubMed
  12. Zhu, T., Jin, H., Shu, D., Li, F. & Wu, C. Association of IL36RN mutations with clinical features, therapeutic response to acitretin, and frequency of recurrence in patients with generalized pustular psoriasis. Eur. J. Dermatol. 28, 217–224 (2018). - PubMed
  13. Choon, S. E. et al. Clinical profile, morbidity, and outcome of adult-onset generalized pustular psoriasis: analysis of 102 cases seen in a tertiary hospital in Johor, Malaysia. Int J. Dermatol. 53, 676–684 (2014). - PubMed
  14. Navarini, A. A. et al. European consensus statement on phenotypes of pustular psoriasis. J. Eur. Acad. Dermatol. Venereol. 31, 1792–1799 (2017). - PubMed
  15. Johnston, A. et al. IL-1 and IL-36 are dominant cytokines in generalized pustular psoriasis. J. Allergy Clin. Immunol. 140, 109–120 (2017). - PubMed
  16. Liang, Y., Sarkar, M. K., Tsoi, L. C. & Gudjonsson, J. E. Psoriasis: a mixed autoimmune and autoinflammatory disease. Curr. Opin. Immunol. 49, 1–8 (2017). - PubMed
  17. Griffiths, C. E. & Barker, J. N. Pathogenesis and clinical features of psoriasis. Lancet 370, 263–271 (2007). - PubMed
  18. Li, M. et al. Prevalent and rare mutations in IL-36RN gene in Chinese patients with generalized pustular psoriasis and psoriasis vulgaris. J. Invest. Dermatol. 133, 2637–2639 (2013). - PubMed
  19. Lohr, S. et al. Association analysis of psoriasis vulgaris and psoriatic arthritis with loss-of-function mutations in IL36RN in German patients. Br. J. Dermatol. 175, 639–641 (2016). - PubMed
  20. Asumalahti, K. et al. Genetic analysis of PSORS1 distinguishes guttate psoriasis and palmoplantar pustulosis. J. Invest. Dermatol. 120, 627–632 (2003). - PubMed
  21. Borges-Costa, J. et al. Clinical and laboratory features in acute generalized pustular psoriasis: a retrospective study of 34 patients. Am. J. Clin. Dermatol. 12, 271–276 (2011). - PubMed
  22. Griffiths, C., Barker, J., Chalmers, R., Bleiker, T. & Creamer, D. Rook’s Textbook of Dermatology (John Wiley & Sons, Incorporated, Hoboken, 2016). - PubMed
  23. Feldmeyer, L., Heidemeyer, K. & Yawalkar, N. Acute generalized exanthematous pustulosis: pathogenesis, genetic background, clinical variants and therapy. Int. J. Mol. Sci. 17, 1214 (2016). - PubMed
  24. Baker, H. & Ryan, T. J. Generalized pustular psoriasis. A clinical and epidemiological study of 104 cases. Br. J. Dermatol. 80, 771–793 (1968). - PubMed
  25. Ryan, T. J. & Baker, H. The prognosis of generalized pustular psoriasis. Br. J. Dermatol. 85, 407–411 (1971). - PubMed
  26. Zelickson, B. D. & Muller, S. A. Generalized pustular psoriasis. A review of 63 cases. Arch. Dermatol. 127, 1339–1345 (1991). - PubMed
  27. Armstrong, A. W. Psoriasis. JAMA Dermatol. 153, 956 (2017). - PubMed
  28. Jin, H. et al. Clinical features and course of generalized pustular psoriasis in Korea. J. Dermatol. 42, 674–678 (2015). - PubMed
  29. Larsabal M. et al. GENIPSO: a French prospective study assessing instantaneous prevalence, clinical features and impact on quality of life of genital psoriasis among patients consulting for psoriasis. Br. J. Dermatol. 180, 647–656 (2019). - PubMed
  30. Yan, D., Afifi, L., Jeon, C., Cordoro, K. M. & Liao, W. A cross-sectional study of the distribution of psoriasis subtypes in different ethno-racial groups. Dermatol. Online J. 24, 4 (2018). - PubMed
  31. Ohkawara, A. et al. Generalized pustular psoriasis in Japan: two distinct groups formed by differences in symptoms and genetic background. Acta Derm. Venereol. 76, 68–71 (1996). - PubMed
  32. Augey, F., Renaudier, P. & Nicolas, J. F. Generalized pustular psoriasis (Zumbusch): a French epidemiological survey. Eur. J. Dermatol. 16, 669–673 (2006). - PubMed
  33. Kharawala, S., Golembesky, A. K., Bohn, R. L. & Esser, D. The clinical, humanistic, and economic burden of generalized pustular psoriasis: a structured review. Expert Rev. Clin. Immunol. 16, 239–252 (2020). - PubMed
  34. Trattner, H. et al. Quality of life and comorbidities in palmoplantar pustulosis—a cross-sectional study on 102 patients. J. Eur. Acad. Dermatol. Venereol. 31, 1681–1685 (2017). - PubMed
  35. Kozlowska, D. et al. Serum sphingolipid level in psoriatic patients with obesity. Postepy Dermatol. Alergol. 36, 714–721 (2019). - PubMed
  36. Goolam Mahyoodeen, N., Crowther, N. J., Snyman, T., Pillay, L. & Tikly, M. High burden of the metabolic syndrome and its component disorders in South Africans with psoriasis. Int J. Dermatol. 58, 557–562 (2019). - PubMed
  37. Namiki, K. et al. Thyroid dysfunction in patients with psoriasis: higher prevalence of thyroid dysfunction in patients with generalized pustular psoriasis. J. Dermatol. 47, 133–139 (2020). - PubMed
  38. Xu, W., Li, C. & Zhang, W. The coexistence of SAPHO syndrome and rheumatoid arthritis: a case report. Medicine 96, e5724 (2017). - PubMed
  39. Rozin, A. P. & Nahir, A. M. Is SAPHO syndrome a target for antibiotic therapy? Clin. Rheumatol. 26, 817–820 (2007). - PubMed
  40. Ozturk, G. et al. Generalized pustular eruptions due to terbinafine. Cutan. Ocul. Toxicol. 31, 81–84 (2012). - PubMed
  41. Gammoudi, R. et al. Acute generalized exanthematous pustulosis induced by oxacillin confirmed by patch testing. Contact Dermat. 79, 108–110 (2018). - PubMed
  42. Webster, G. F. Pustular drug reactions. Clin. Dermatol. 11, 541–543 (1993). - PubMed
  43. Saeki, H. et al. Juvenile pustular psoriasis associated with steroid withdrawal syndrome due to topical corticosteroid. J. Dermatol. 35, 601–603 (2008). - PubMed
  44. Vasconcellos, J. B. et al. Paradoxical psoriasis after the use of anti-TNF in a patient with rheumatoid arthritis. Bras. Dermatol. 91, 137–139 (2016). - PubMed
  45. Jiyad, Z., Moriarty, B., Creamer, D. & Higgins, E. Generalized pustular psoriasis associated with Epstein-Barr virus. Clin. Exp. Dermatol. 40, 146–148 (2015). - PubMed
  46. Yoneda, K., Matsuoka-Shirahige, Y., Demitsu, T. & Kubota, Y. Pustular psoriasis precipitated by cytomegalovirus infection. Br. J. Dermatol. 167, 1186–1189 (2012). - PubMed
  47. Pouessel, G. et al. Childhood pustular psoriasis associated with Panton-Valentine leukocidin-producing Staphylococcus aureus. Pediatr. Dermatol. 24, 401–404 (2007). - PubMed
  48. Miot, H. A., Miot, L. D., Lopes, P. S., Haddad, G. R. & Marques, S. A. Association between palmoplantar pustulosis and cigarette smoking in Brazil: a case-control study. J. Eur. Acad. Dermatol. Venereol. 23, 1173–1177 (2009). - PubMed
  49. Wilsmann-Theis, D. et al. Palmoplantar pustulosis—a cross-sectional analysis in Germany. Dermatol. Online J. 23 (2017). - PubMed
  50. Michaelsson, G., Gustafsson, K. & Hagforsen, E. The psoriasis variant palmoplantar pustulosis can be improved after cessation of smoking. J. Am. Acad. Dermatol. 54, 737–738 (2006). - PubMed
  51. Onoufriadis, A. et al. Mutations in IL36RN/IL1F5 are associated with the severe episodic inflammatory skin disease known as generalized pustular psoriasis. Am. J. Hum. Genet. 89, 432–437 (2011). - PubMed
  52. Boutet, M. A. et al. Distinct expression of interleukin (IL)-36alpha, beta and gamma, their antagonist IL-36Ra and IL-38 in psoriasis, rheumatoid arthritis and Crohn’s disease. Clin. Exp. Immunol. 184, 159–173 (2016). - PubMed
  53. Aksentijevich, I. et al. An autoinflammatory disease with deficiency of the interleukin-1-receptor antagonist. N. Engl. J. Med. 360, 2426–2437 (2009). - PubMed
  54. Bachelez, H. et al. Inhibition of the interleukin-36 pathway for the treatment of generalized pustular psoriasis. N. Engl. J. Med. 380, 981–983 (2019). - PubMed
  55. McDermott, M. F. et al. Germline mutations in the extracellular domains of the 55 kDa TNF receptor, TNFR1, define a family of dominantly inherited autoinflammatory syndromes. Cell 97, 133–144 (1999). - PubMed
  56. Brydges, S. & Kastner, D. L. The systemic autoinflammatory diseases: inborn errors of the innate immune system. Curr. Top. Microbiol. Immunol. 305, 127–160 (2006). - PubMed
  57. Jesus, A. A. et al. A novel mutation of IL1RN in the deficiency of interleukin-1 receptor antagonist syndrome: description of two unrelated cases from Brazil. Arthritis Rheumatol. 63, 4007–4017 (2011). - PubMed
  58. Minkis, K. et al. Interleukin 1 receptor antagonist deficiency presenting as infantile pustulosis mimicking infantile pustular psoriasis. Arch. Dermatol. 148, 747–752 (2012). - PubMed
  59. Marrakchi, S. et al. Interleukin-36-receptor antagonist deficiency and generalized pustular psoriasis. N. Engl. J. Med. 365, 620–628 (2011). - PubMed
  60. Tauber, M. et al. IL36RN mutations affect protein expression and function: a basis for genotype-phenotype correlation in pustular diseases. J. Invest. Dermatol. 136, 1811–1819 (2016). - PubMed
  61. Setta-Kaffetzi, N. et al. Rare pathogenic variants in IL36RN underlie a spectrum of psoriasis-associated pustular phenotypes. J. Invest. Dermatol. 133, 1366–1369 (2013). - PubMed
  62. Mossner, R. et al. Palmoplantar pustular psoriasis is associated with missense variants in CARD14, but not with loss-of-function mutations in IL36RN in European patients. J. Invest. Dermatol. 135, 2538–2541 (2015). - PubMed
  63. Takahashi, T., Fujimoto, N., Kabuto, M., Nakanishi, T. & Tanaka, T. Mutation analysis of IL36RN gene in Japanese patients with palmoplantar pustulosis. J. Dermatol. 44, 80–83 (2017). - PubMed
  64. Xiaoling, Y., Dan, S. & Hongzhong, J. Lack of association between mutation in IL36RN and palmoplantar pustular psoriasis in Chinese patients. Bras. Dermatol 94, 658–663 (2019). - PubMed
  65. Capon, F. IL36RN mutations in generalized pustular psoriasis: just the tip of the iceberg? J. Invest. Dermatol. 133, 2503–2504 (2013). - PubMed
  66. Traks, T. et al. Polymorphisms in IL36G gene are associated with plaque psoriasis. BMC Med. Genet. 20, 10 (2019). - PubMed
  67. Jordan, C. T. et al. PSORS2 is due to mutations in CARD14. Am. J. Hum. Genet. 90, 784–795 (2012). - PubMed
  68. Tomfohrde, J. et al. Gene for familial psoriasis susceptibility mapped to the distal end of human chromosome 17q. Science 264, 1141–1145 (1994). - PubMed
  69. Blonska, M. & Lin, X. CARMA1-mediated NF-kappaB and JNK activation in lymphocytes. Immunol. Rev. 228, 199–211 (2009). - PubMed
  70. Howes, A. et al. Psoriasis mutations disrupt CARD14 autoinhibition promoting BCL10-MALT1-dependent NF-kappaB activation. Biochem J. 473, 1759–1768 (2016). - PubMed
  71. Jordan, C. T. et al. Rare and common variants in CARD14, encoding an epidermal regulator of NF-kappaB, in psoriasis. Am. J. Hum. Genet. 90, 796–808 (2012). - PubMed
  72. Wang, M. et al. Gain-of-function mutation of Card14 leads to spontaneous psoriasis-like skin inflammation through enhanced keratinocyte response to IL-17A. Immunity 49, 66–79 (2018). - PubMed
  73. Fu, F. et al. Rare CARD14 missense variants associated with palmoplantar pustulosis (PPP) in the Chinese Han population. Eur. J. Dermatol. 29, 99–100 (2019). - PubMed
  74. Tsoi, L. C. et al. Identification of 15 new psoriasis susceptibility loci highlights the role of innate immunity. Nat. Genet. 44, 1341–1348 (2012). - PubMed
  75. Setta-Kaffetzi, N. et al. AP1S3 mutations are associated with pustular psoriasis and impaired toll-like receptor 3 trafficking. Am. J. Hum. Genet. 94, 790–797 (2014). - PubMed
  76. Robinson, M. S. Adaptable adaptors for coated vesicles. Trends Cell Biol. 14, 167–174 (2004). - PubMed
  77. Alexopoulou, L., Holt, A. C., Medzhitov, R. & Flavell, R. A. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 413, 732–738 (2001). - PubMed
  78. Mahil, S. K. et al. AP1S3 mutations cause skin autoinflammation by disrupting keratinocyte autophagy and up-regulating IL-36 production. J. Invest. Dermatol. 136, 2251–2259 (2016). - PubMed
  79. Frey, S. et al. Rare loss-of-function mutation in SERPINA3 in generalized pustular psoriasis. J. Invest. Dermatol. 140, 1451–1455 (2020). - PubMed
  80. Beatty, K., Bieth, J. & Travis, J. Kinetics of association of serine proteinases with native and oxidized alpha-1-proteinase inhibitor and alpha-1-antichymotrypsin. J. Biol. Chem. 255, 3931–3934 (1980). - PubMed
  81. Henry, C. M. et al. Neutrophil-derived proteases escalate inflammation through activation of IL-36 family cytokines. Cell Rep. 14, 708–722 (2016). - PubMed
  82. Zhang, Z. & Xu, J. H. Investigation of psoriasis susceptibility loci in psoriatic arthritis and a generalized pustular psoriasis cohort. J. Investig. Dermatol. Symp. Proc. 19, S83–S85 (2018). - PubMed
  83. Heyninck, K., Kreike, M. M. & Beyaert, R. Structure-function analysis of the A20-binding inhibitor of NF-kappa B activation, ABIN-1. FEBS Lett. 536, 135–140 (2003). - PubMed
  84. Han, J. W. et al. Tumor necrosis factor-alpha induced protein 3 interacting protein 1 gene polymorphisms and pustular psoriasis in Chinese Han population. Chin. Med. J. 129, 1519–1524 (2016). - PubMed
  85. Nograles, K. E. et al. Th17 cytokines interleukin (IL)-17 and IL-22 modulate distinct inflammatory and keratinocyte-response pathways. Br. J. Dermatol. 159, 1092–1102 (2008). - PubMed
  86. Huffmeier, U., Watzold, M., Mohr, J., Schon, M. P. & Mossner, R. Successful therapy with anakinra in a patient with generalized pustular psoriasis carrying IL36RN mutations. Br. J. Dermatol. 170, 202–204 (2014). - PubMed
  87. Towne, J. E. et al. Interleukin-36 (IL-36) ligands require processing for full agonist (IL-36alpha, IL-36beta, and IL-36gamma) or antagonist (IL-36Ra) activity. J. Biol. Chem. 286, 42594–42602 (2011). - PubMed
  88. Debets, R. et al. Two novel IL-1 family members, IL-1 delta and IL-1 epsilon, function as an antagonist and agonist of NF-kappa B activation through the orphan IL-1 receptor-related protein 2. J. Immunol. 167, 1440–1446 (2001). - PubMed
  89. He, Y., Hara, H. & Nunez, G. Mechanism and regulation of NLRP3 inflammasome activation. Trends Biochem. Sci. 41, 1012–1021 (2016). - PubMed
  90. Johnston, A. et al. IL-1F5, -F6, -F8, and -F9: a novel IL-1 family signaling system that is active in psoriasis and promotes keratinocyte antimicrobial peptide expression. J. Immunol. 186, 2613–2622 (2011). - PubMed
  91. Ainscough, J. S. et al. Cathepsin S is the major activator of the psoriasis-associated proinflammatory cytokine IL-36gamma. Proc. Natl Acad. Sci. USA 114, E2748–E2757 (2017). - PubMed
  92. Clancy, D. M., Henry, C. M., Sullivan, G. P. & Martin, S. J. Neutrophil extracellular traps can serve as platforms for processing and activation of IL-1 family cytokines. FEBS J. 284, 1712–1725 (2017). - PubMed
  93. Liang, Y. et al. Six-transmembrane epithelial antigens of the prostate comprise a novel inflammatory nexus in patients with pustular skin disorders. J. Allergy Clin. Immunol. 139, 1217–1227 (2017). - PubMed
  94. Vigne, S. et al. IL-36R ligands are potent regulators of dendritic and T cells. Blood 118, 5813–5823 (2011). - PubMed
  95. Mutamba, S., Allison, A., Mahida, Y., Barrow, P. & Foster, N. Expression of IL-1Rrp2 by human myelomonocytic cells is unique to DCs and facilitates DC maturation by IL-1F8 and IL-1F9. Eur. J. Immunol. 42, 607–617 (2012). - PubMed
  96. Arakawa, A. et al. Unopposed IL-36 activity promotes clonal CD4(+) T-cell responses with IL-17A production in generalized pustular psoriasis. J. Invest. Dermatol. 138, 1338–1347 (2018). - PubMed
  97. Benoit, S., Toksoy, A., Brocker, E. B., Gillitzer, R. & Goebeler, M. Treatment of recalcitrant pustular psoriasis with infliximab: effective reduction of chemokine expression. Br. J. Dermatol. 150, 1009–1012 (2004). - PubMed
  98. Imafuku, S. et al. Efficacy and safety of secukinumab in patients with generalized pustular psoriasis: a 52-week analysis from phase III open-label multicenter Japanese study. J. Dermatol. 43, 1011–1017 (2016). - PubMed
  99. Blumberg, H. et al. Opposing activities of two novel members of the IL-1 ligand family regulate skin inflammation. J. Exp. Med. 204, 2603–2614 (2007). - PubMed
  100. Carrier, Y. et al. Inter-regulation of Th17 cytokines and the IL-36 cytokines in vitro and in vivo: implications in psoriasis pathogenesis. J. Invest. Dermatol. 131, 2428–2437 (2011). - PubMed
  101. Robinson, A. et al. Treatment of pustular psoriasis: from the Medical Board of the National Psoriasis Foundation. J. Am. Acad. Dermatol. 67, 279–288 (2012). - PubMed
  102. Torii, H., Nakagawa, H. & Japanese Infliximab Study Investigators. Long-term study of infliximab in Japanese patients with plaque psoriasis, psoriatic arthritis, pustular psoriasis and psoriatic erythroderma. J. Dermatol. 38, 321–334 (2011). - PubMed
  103. Kimura, U. et al. Generalized pustular psoriasis-like eruptions induced after the first use of adalimumab in the treatment of psoriatic arthritis. J. Dermatol. 39, 286–287 (2012). - PubMed
  104. Wendling, D. et al. Onset or exacerbation of cutaneous psoriasis during TNFalpha antagonist therapy. Jt. Bone Spine 75, 315–318 (2008). - PubMed
  105. Arakawa, A., Ruzicka, T. & Prinz, J. C. Therapeutic efficacy of interleukin 12/interleukin 23 blockade in generalized pustular psoriasis regardless of IL36RN mutation status. JAMA Dermatol. 152, 825–828 (2016). - PubMed
  106. Bissonnette, R. et al. Increased expression of IL-17A and limited involvement of IL-23 in patients with palmo-plantar (PP) pustular psoriasis or PP pustulosis; results from a randomised controlled trial. J. Eur. Acad. Dermatol. Venereol. 28, 1298–1305 (2014). - PubMed
  107. Husson, B. et al. Efficacy and safety of TNF blockers and of ustekinumab in palmoplantar pustulosis and in acrodermatitis continua of Hallopeau. J. Eur. Acad. Dermatol. Venereol. https://doi.org/10.1111/jdv.16265 (2020). - PubMed
  108. Mrowietz, U. et al. Secukinumab for moderate-to-severe palmoplantar pustular psoriasis: results of the 2PRECISE study. J. Am. Acad. Dermatol. 80, 1344–1352 (2019). - PubMed
  109. Mansouri, B., Richards, L. & Menter, A. Treatment of two patients with generalized pustular psoriasis with the interleukin-1beta inhibitor gevokizumab. Br. J. Dermatol. 173, 239–241 (2015). - PubMed
  110. Skendros, P. et al. Successful response in a case of severe pustular psoriasis after interleukin-1beta inhibition. Br. J. Dermatol. 176, 212–215 (2017). - PubMed
  111. Mansouri, B., Kivelevitch, D., Campa, M. & Menter, A. Palmoplantar pustular psoriasis unresponsive to the interleukin-1beta antagonist canakinumab. Clin. Exp. Dermatol. 41, 324–326 (2016). - PubMed
  112. Gudjonsson, J. E., Johnston, A., Dyson, M., Valdimarsson, H. & Elder, J. T. Mouse models of psoriasis. J. Invest. Dermatol. 127, 1292–1308 (2007). - PubMed
  113. Campbell, J. J. et al. Efficacy of chemokine receptor inhibition in treating IL-36alpha-induced psoriasiform inflammation. J. Immunol. 202, 1687–1692 (2019). - PubMed
  114. Foster, A. M. et al. IL-36 promotes myeloid cell infiltration, activation, and inflammatory activity in skin. J. Immunol. 192, 6053–6061 (2014). - PubMed
  115. Hawkes, J. E., Gudjonsson, J. E. & Ward, N. L. The snowballing literature on imiquimod-induced skin inflammation in mice: a critical appraisal. J. Invest. Dermatol. 137, 546–549 (2017). - PubMed
  116. Alvarez, P. & Jensen, L. E. Imiquimod treatment causes systemic disease in mice resembling generalized pustular psoriasis in an IL-1 and IL-36 dependent manner. Mediators Inflamm. 2016, 6756138 (2016). - PubMed
  117. Shao, S. et al. Neutrophil extracellular traps promote inflammatory responses in psoriasis via activating epidermal TLR4/IL-36R crosstalk. Front. Immunol. 10, 746 (2019). - PubMed
  118. Sundberg, J. P. et al. Gain of function p.E138A alteration in Card14 leads to psoriasiform skin inflammation and implicates genetic modifiers in disease severity. Exp. Mol. Pathol. 110, 104286 (2019). - PubMed
  119. Swindell, W. R. et al. RNA-Seq Analysis of IL-1B and IL-36 responses in epidermal keratinocytes identifies a shared MyD88-dependent gene signature. Front. Immunol. 9, 80 (2018). - PubMed
  120. Trivedi, M. K., Vaughn, A. R. & Murase, J. E. Pustular psoriasis of pregnancy: current perspectives. Int J. Women’s Health 10, 109–115 (2018). - PubMed
  121. Ross, M. G., Tucker, D. C. & Hayashi, R. H. Impetigo herpetiformis as a cause of postpartum fever. Obstet. Gynecol. 64, 49S–51S (1984). - PubMed
  122. Yamashita, T. et al. An effective and promising treatment with adalimumab for impetigo herpetiformis with postpartum flare-up. Int J. Dermatol. 58, 350–353 (2019). - PubMed
  123. Tay, Y. K. & Tham, S. N. The profile and outcome of pustular psoriasis in Singapore: a report of 28 cases. Int J. Dermatol. 36, 266–271 (1997). - PubMed
  124. Xiao, T., Li, B., He, C. D. & Chen, H. D. Juvenile generalized pustular psoriasis. J. Dermatol. 34, 573–576 (2007). - PubMed
  125. Wang, Q., Liu, W. & Zhang, L. Clinical features of von Zumbusch type of generalized pustular psoriasis in children: a retrospective study of 26 patients in southwestern China. Bras. Dermatol. 92, 319–322 (2017). - PubMed
  126. de Oliveira, S. T., Maragno, L., Arnone, M., Fonseca Takahashi, M. D. & Romiti, R. Generalized pustular psoriasis in childhood. Pediatr. Dermatol. 27, 349–354 (2010). - PubMed
  127. Korber, A. et al. Mutations in IL36RN in patients with generalized pustular psoriasis. J. Invest. Dermatol. 133, 2634–2637 (2013). - PubMed
  128. Sugiura, K. et al. A novel IL36RN/IL1F5 homozygous nonsense mutation, p.Arg10X, in a Japanese patient with adult-onset generalized pustular psoriasis. Br. J. Dermatol. 167, 699–701 (2012). - PubMed
  129. Farooq, M. et al. Mutation analysis of the IL36RN gene in 14 Japanese patients with generalized pustular psoriasis. Hum. Mutat. 34, 176–183 (2013). - PubMed
  130. Li, M. et al. IL36RN gene mutations are not associated with sporadic generalized pustular psoriasis in Chinese patients. Br. J. Dermatol. 168, 452–455 (2013). - PubMed
  131. Hussain, S. et al. IL36RN mutations define a severe autoinflammatory phenotype of generalized pustular psoriasis. J. Allergy Clin. Immunol. 135, 1067–1070. e1069 (2015). - PubMed
  132. Ammar, M. et al. CARD14 alterations in Tunisian patients with psoriasis and further characterization in European cohorts. Br. J. Dermatol. 174, 330–337 (2016). - PubMed
  133. Mossner, R. et al. The genetic basis for most patients with pustular skin disease remains elusive. Br. J. Dermatol. 178, 740–748 (2018). - PubMed
  134. Sugiura, K., Muto, M. & Akiyama, M. CARD14 c.526G>C (p.Asp176His) is a significant risk factor for generalized pustular psoriasis with psoriasis vulgaris in the Japanese cohort. J. Invest. Dermatol. 134, 1755–1757 (2014). - PubMed
  135. Tobita, R. et al. A novel CARD14 variant, homozygous c.526G>C (p.Asp176His), in an adolescent Japanese patient with palmoplantar pustulosis. Clin. Exp. Dermatol. 44, 694–696 (2019). - PubMed
  136. Qin, P. et al. Variant analysis of CARD14 in a Chinese Han population with psoriasis vulgaris and generalized pustular psoriasis. J. Invest. Dermatol. 134, 2994–2996 (2014). - PubMed
  137. Tauber, M. et al. Partial clinical response to anakinra in severe palmoplantar pustular psoriasis. Br. J. Dermatol. 171, 646–649 (2014). - PubMed
  138. ClinicalTrialNCT03886246. A 5-year study to test BI 655130 in patients with generalized pustular psoriasis who took part in previous studies with BI 655130. Clinical Trial. https://clinicaltrials.gov/ct2/show/NCT03886246 (2019). - PubMed
  139. ClinicalTrialNCT03135548. Initial dosing of BI 655130 in palmoplantar pustulosis patients. Clinical Trial. https://clinicaltrials.gov/ct2/show/NCT03135548 (2019). - PubMed
  140. ClinicalTrialNCT03619902. A study to evaluate the efficacy and safety of ANB019 in subjects with generalized pustular psoriasis (GPP). Clinical Trial. https://clinicaltrials.gov/ct2/show/NCT03619902 (2019). - PubMed
  141. ClinicalTrialNCT03633396. A study to evaluate the efficacy and safety of ANB019 in subjects with palmoplantar pustulosis (PPP). Clinical Trial. https://clinicaltrials.gov/ct2/show/NCT03633396 (2019). - PubMed

Publication Types

Grant support