Autoinflammatory process in the pathogenesis of generalized pustular psoriasis and perspectives of its targeted therapy
Authors:
J. Javor; M. Buc; M. Bucová
Authors place of work:
Imunologický ústav, Lekárska fakulta Univerzity Komenského v Bratislave
Published in the journal:
Epidemiol. Mikrobiol. Imunol. 70, 2021, č. 3, s. 199-207
Category:
Review Article
Summary
The dysregulated inflammatory process not only plays an important role in the development of chronic plaque psoriasis but also is a major pathogenetic mechanism behind the generalized pustular psoriasis (GPP) and other rare pustular forms of the disease. The key players in this process are the cytokines interleukin (IL)-1β, IL-6, tumor necrosis factor (TNF), IL-12/23, IL-17A and especially IL-36. Their excessive activity or production in some GPP patients is due to mutations in genes that encode molecules involved in inhibiting the action of IL-36 (IL-36Ra) or in intracellular inflammatory signaling (CARD14, AP1S3). Knowledge about the pathological role of inflammatory cytokines in the development of pustular forms of psoriasis has also found application in their biological therapy with monoclonal antibodies that neutralize the action of IL-12/23, IL-17A, TNF or IL-1β. Other promising agents are monoclonal antibodies against the interleukin 36 receptor, which have already successfully gone through the first phases of clinical trials and are currently being tested for their long-term efficacy, safety and tolerability.
Keywords:
autoinflammatory disease – biological therapy – generalized pustular psoriasis – interleukin 36 – spesolimab
Zdroje
1. Hedrich CM. Shaping the spectrum – From autoinflammation to autoimmunity. Clin Immunol, 2016;165:21–28.
2. Liang Y, Sarkar MK, Tsoi LC et al. Psoriasis: a mixed autoimmune and autoinflammatory disease. Curr Opin Immunol, 2017;49:1–8.
3. Madonna S, Girolomoni G, Dinarello CA et al. The Significance of IL-36 Hyperactivation and IL-36R Targeting in Psoriasis. Int J Mol Sci, 2019;20(13):3318.
4. Akiyama M, Takeichi T, McGrath JA et al. Autoinflammatory keratinization diseases: An emerging concept encompassing various inflammatory keratinization disorders of the skin. J Dermatol Sci, 2018;90(2):105–111.
5. Boehncke WH, Schön MP. Psoriasis. Lancet, 2015;386(9997):983–994.
6. Lowes MA, Suárez-Fariñas M, Krueger JG. Immunology of Psoriasis. Annu Rev Immunol, 2014;32:227–255.
7. Hawkes JE, Chan TC, Krueger JG. Psoriasis pathogenesis and the development of novel targeted immune therapies. J Allergy Clin Immunol, 2017;140(3):645–653.
8. Furue K, Yamamura K, Tsuji G et al. Highlighting Interleukin-36 Signalling in Plaque Psoriasis and Pustular Psoriasis. Acta Derm Venereol, 2018;98(1):5–13.
9. Boehner A, Navarini AA, Eyerich K. Generalized pustular psoriasis - a model disease for specific targeted immunotherapy, systematic review. Exp Dermatol, 2018;27(10):1067–1077.
10. Benjegerdes KE, Hyde K, Kivelevitch D et al. Pustular psoriasis: pathophysiology and current treatment perspectives. Psoriasis (Auckl), 2016;6:131–144.
11. Navarini AA, Burden AD, Capon F et al. European consensus statement on phenotypes of pustular psoriasis. J Eur Acad Dermatol Venereol, 2017;31(11):1792–1799.
12. Hoegler KM, John AM, Handler MZ et al. Generalized pustular psoriasis: a review and update on treatment. J Eur Acad Dermatol Venereol, 2018;32(10):1645–1651.
13. Twelves S, Mostafa A, Dand N et al. Clinical and genetic differences between pustular psoriasis subtypes. J Allergy Clin Immunol, 2019;143(3):1021–1026.
14. Bachelez H. Pustular psoriasis and related pustular skin diseases. Br J Dermatol, 2018;178(3):614–618.
15. Ly K, Beck KM, Smith MP et al. Diagnosis and screening of patients with generalized pustular psoriasis. Psoriasis (Auckl), 2019;9:37–42.
16. Gooderham MJ, Van Voorhees AS, Lebwohl MG. An Update on Generalized Pustular Psoriasis. Expert Rev Clin Immunol, 2019;15(9):907–919.
17. Popadic S, Nikolic M. Pustular psoriasis in childhood and adolescence: a 20-year single-center experience. Pediatr Dermatol, 2014;31(5):575–579.
18. Trivedi MK, Vaughn AR, Murase JE. Pustular psoriasis of pregnancy: current perspectives. Int J Womens Health, 2018;10:109–115.
19. Sehgal VN, Verma P, Sharma S et al. Acrodermatitis continua of Hallopeau: evolution of treatment options. Int J Dermatol, 2011;50(10):1195–1211.
20. Misiak-Galazka M, Wolska H, Rudnicka L. What do we know about palmoplantar pustulosis? J Eur Acad Dermatol Venereol, 2017;31(1):38–44.
21. Chung J, Callis Duffin K, Takeshita J et al. Palmoplantar psoriasis is associated with greater impairment of health-related quality of life compared with moderate to severe plaque psoriasis. J Am Acad Dermatol, 2014;71(4):623–632.
22. Trattner H, Blüml S, Steiner I et al. Quality of life and comorbidities in palmoplantar pustulosis - a cross-sectional study on 102 patients. J Eur Acad Dermatol Venereol, 2017;31(10):1681–1685.
23. Fujita H, Terui T, Hayama K et al. Japanese guidelines for the management and treatment of generalized pustular psoriasis: The new pathogenesis and treatment of GPP. J Dermatol, 2018;45(11):1235–1270.
24. Choon SE, Lai NM, Mohammad NA 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, 2014;53(6):676–684.
25. Johnston A, Xing X, Wolterink L et al. IL-1 and IL-36 are dominant cytokines in generalized pustular psoriasis. J Allergy Clin Immunol, 2017;140(1):109–120.
26. Bassoy EY, Towne JE, Gabay C. Regulation and function of interleukin- 36 cytokines. Immunol Rev, 2018;281(1):169–178.
27. Buhl AL, Wenzel J. Interleukin-36 in Infectious and Inflammatory Skin Diseases. Front Immunol, 2019;10:1162.
28. Boutet MA, Nerviani A, Pitzalis C. IL-36, IL-37, and IL-38 Cytokines in Skin and Joint Inflammation: A Comprehensive Review of Their Therapeutic Potential. Int J Mol Sci, 2019;20(6):1257.
29. Walsh PT, Fallon PG. The emergence of the IL-36 cytokine family as novel targets for inflammatory diseases. Ann N Y Acad Sci, 2018;1417(1):23–34.
30. Towne JE, Renshaw BR, Douangpanya J et al. Interleukin-36 (IL-36) ligands require processing for full agonist (IL-36α, IL-36β, and IL-36γ) or antagonist (IL-36Ra) activity. J Biol Chem, 2011;286(49):42594–42602.
31. Clancy DM, Henry CM, Sullivan GP et al. Neutrophil extracellular traps can serve as platforms for processing and activation of IL-1 family cytokines. FEBS J, 2017;284(11):1712–1725.
32. Towne JE, Garka KE, Renshaw BR et al. Interleukin (IL)-1F6, IL-1F8, and IL-1F9 signal through IL-1Rrp2 and IL-1RAcP to activate the pathway leading to NF-kappaB and MAPKs. J Biol Chem, 2004;279(14):13677–13688.
33. Zhou L, Todorovic V, Kakavas S et al. Quantitative ligand and receptor binding studies reveal the mechanism of interleukin-36 (IL-36) pathway activation. J Biol Chem, 2018;293(2):403–411.
34. Dietrich D, Gabay C. Inflammation: IL-36 has proinflammatory effects in skin but not in joints. Nat Rev Rheumatol, 2014;10(11):639–640.
35. Dietrich D, Martin P, Flacher V et al. Interleukin-36 potently stimulates human M2 macrophages, Langerhans cells and keratinocytes to produce pro-inflammatory cytokines. Cytokine, 2016;84:88–98.
36. Kakeda M, Schlapbach C, Danelon G et al. Innate immune cells express IL-17A/F in acute generalized exanthematous pustulosis and generalized pustular psoriasis. Arch Dermatol Res, 2014;306(10):933–938.
37. Arakawa A, Vollmer S, Besgen P et al. Unopposed IL-36 Activity Promotes Clonal CD4+ T-Cell Responses with IL-17A Production in Generalized Pustular Psoriasis. J Invest Dermatol, 2018;138(6):1338–1347.
38. van de Veerdonk FL, Stoeckman AK, Wu G et al. IL-38 binds to the IL-36 receptor and has biological effects on immune cells similar to IL-36 receptor antagonist. Proc Natl Acad Sci U S A, 2012;109(8):3001–3005.
39. Marrakchi S, Guigue P, Renshaw BR et al. Interleukin-36-receptor antagonist deficiency and generalized pustular psoriasis. N Engl J Med, 2011;365(7):620–628.
40. Onoufriadis A, Simpson MA, Pink AE et al. Mutations in IL36RN/ IL1F5 are associated with the severe episodic inflammatory skin disease known as generalized pustular psoriasis. Am J Hum Genet, 2011;89(3):432–437.
41. Sugiura K. The genetic background of generalized pustular psoriasis: IL36RN mutations and CARD14 gain-of-function variants. J Dermatol Sci, 2014;74(3):187–192.
42. Hussain S, Berki DM, Choon SE et al. IL36RN mutations define a severe autoinflammatory phenotype of generalized pustular psoriasis. J Allergy Clin Immunol, 2015;135(4):1067–1070.e9.
43. Mössner R, Wilsmann-Theis D, Oji V et al. The genetic basis for most patients with pustular skin disease remains elusive. Br J Dermatol, 2018;178(3):740–748.
44. Hospach T, Glowatzki F, Blankenburg F et al. Scoping review of biological treatment of deficiency of interleukin-36 receptor antagonist (DITRA) in children and adolescents. Pediatr Rheumatol Online J, 2019;17(1):37.
45. Picard C, Bobby Gaspar H, Al-Herz W et al. International Union of Immunological Societies: 2017 Primary Immunodeficiency Diseases Committee Report on Inborn Errors of Immunity. J Clin Immunol, 2018;38(1):96–128.
46. Capon F. IL36RN mutations in generalized pustular psoriasis: just the tip of the iceberg? J Invest Dermatol, 2013;133(11):2503–2504.
47. Sugiura K, Takemoto A, Yamaguchi M et al. The majority of generalized pustular psoriasis without psoriasis vulgaris is caused by deficiency of interleukin-36 receptor antagonist. J Invest Dermatol, 2013;133(11):2514–2521.
48. Akiyama M. Early-onset generalized pustular psoriasis is representative of autoinflammatory keratinization diseases. J Allergy Clin Immunol, 2019;143(2):809–810.
49. Berki DM, Liu L, Choon SE et al. Activating CARD14 Mutations Are Associated with Generalized Pustular Psoriasis but Rarely Account for Familial Recurrence in Psoriasis Vulgaris. J Invest Dermatol, 2015;135(12):2964–2970.
50. Takeichi T, Akiyama M. Generalized Pustular Psoriasis: Clinical Management and Update on Autoinflammatory Aspects. Am J Clin Dermatol, 2020;21(2):227–236.
51. Setta-Kaffetzi N, Simpson MA, Navarini AA et al. AP1S3 mutations are associated with pustular psoriasis and impaired Toll-like receptor 3 trafficking. Am J Hum Genet, 2014;94(5):790–797.
52. Mahil SK, Twelves S, Farkas K et al. AP1S3 Mutations Cause Skin Autoinflammation by Disrupting Keratinocyte Autophagy and Up-Regulating IL-36 Production. J Invest Dermatol, 2016;136(11):2251–2259.
53. Robinson A, Van Voorhees AS, Hsu S et al. Treatment of pustular psoriasis: from the Medical Board of the National Psoriasis Foundation. J Am Acad Dermatol, 2012;67(2):279–288.
54. Morita A, Yamazaki F, Matsuyama T et al. Adalimumab treatment in Japanese patients with generalized pustular psoriasis: Results of an open-label phase 3 study. J Dermatol, 2018;45(12):1371– 1380.
55. Sano S, Kubo H, Morishima H et al. Guselkumab, a human interleukin- 23 monoclonal antibody in Japanese patients with generalized pustular psoriasis and erythrodermic psoriasis: Efficacy and safety analyses of a 52-week, phase 3, multicenter, open-label study. J Dermatol, 2018;45(5):529–539.
56. Imafuku S, Honma M, Okubo Y 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, 2016;43(9):1011–1017.
57. Saeki H, Nakagawa H, Nakajo K et al. Efficacy and safety of ixekizumab treatment for Japanese patients with moderate to severe plaque psoriasis, erythrodermic psoriasis and generalized pustular psoriasis: Results from a 52-week, open-label, phase 3 study (UNCOVER-J). J Dermatol, 2017;44(4):355–362.
58. Okubo Y, Mabuchi T, Iwatsuki K et al. Long-term efficacy and safety of ixekizumab in Japanese patients with erythrodermic or generalized pustular psoriasis: subgroup analyses of an open-label, phase 3 study (UNCOVER-J). J Eur Acad Dermatol Venereol, 2019;33(2):325–332.
59. Yamasaki K, Nakagawa H, Kubo Y et al. Efficacy and safety of brodalumab in patients with generalized pustular psoriasis and psoriatic erythroderma: results from a 52-week, open-label study. Br J Dermatol, 2017;176(3):741–751.
60. Bachelez H, Choon SE, Marrakchi S et al. Inhibition of the Interleukin- 36 Pathway for the Treatment of Generalized Pustular Psoriasis. N Engl J Med, 2019;380(10):981–983.
61. BI655130 Single Dose in Generalized Pustular Psoriasis [online]. 2018-01-17 [cit. 2020-07-03]. Dostupný na: https://clinicaltrials. gov/ct2/show/NCT02978690
62. A Study to Test BI 655130 in Patients With a Flare-up of a Skin Disease Called Generalized Pustular Psoriasis [online]. 2020-07-01 [cit. 2020-07-03]. Dostupný na: https://clinicaltrials.gov/ct2/show/ NCT03782792
63. A Study to Test Whether BI 655130 (Spesolimab) Prevents Flare-ups in Patients With Generalized Pustular Psoriasis [online]. 2020-07- 01 [cit. 2020-07-03]. Dostupný na: https://clinicaltrials.gov/ct2/ show/NCT04399837
64. A 5-year Study to Test BI 655130 in Patients With Generalized Pustular Psoriasis Who Took Part in Previous Studies With BI 655130 [online]. 2020-06-16 [cit. 2020-07-03]. Dostupný na: https://clinicaltrials. gov/ct2/show/NCT03886246
65. A Study to Test How Effective and Safe Different Doses of BI 655130 Are in Patients With a Moderate to Severe Form of the Skin Disease Palmoplantar Pustulosis [online]. 2020-07-02 [cit. 2020-07-03]. Dostupný na: https://clinicaltrials.gov/ct2/show/NCT04015518
66. Initial Dosing of BI 655130 in Palmoplantar Pustulosis Patients [online]. 2019-11-26 [cit. 2020-07-03]. Dostupný na: https://clinicaltrials. gov/ct2/show/NCT03135548
67. A Study to Evaluate the Efficacy and Safety of ANB019 in Subjects With Generalized Pustular Psoriasis (GPP) [online]. 2019-07-02 [cit. 2020-07-03]. Dostupný na: https://clinicaltrials.gov/ct2/ show/NCT03619902
68. A Study to Evaluate the Efficacy and Safety of ANB019 in Subjects With Palmoplantar Pustulosis (PPP) [online]. 2019-07-10 [cit. 2020-07-03]. Dostupný na: https://clinicaltrials.gov/ct2/show/NCT03633396
69. Sullivan GP, Henry CM, Clancy DM et al. Suppressing IL-36-driven inflammation using peptide pseudosubstrates for neutrophil proteases. Cell Death Dis, 2018;9(3):378.
70. Sullivan GP, Davidovich PB, Sura-Trueba S et al. Identification of small-molecule elastase inhibitors as antagonists of IL-36 cytokine activation. FEBS Open Bio, 2018;8(5):751–763.
Štítky
Hygiene and epidemiology Medical virology Clinical microbiologyČlánok vyšiel v časopise
Epidemiology, Microbiology, Immunology
2021 Číslo 3
Najčítanejšie v tomto čísle
- Epidemiology, risk factors and possibilities for the prevention of acute leukaemia
- What we know and still do not know about tick-borne encephalitis?
- If a vaccine against COVID-19 was available, would you like to be vaccinated? And are you vaccinated against flu and other diseases? A survey among university students during state of emergency
- Autoinflammatory process in the pathogenesis of generalized pustular psoriasis and perspectives of its targeted therapy