Looking to Psoriatic Arthritis History to Disrupt Current Thinking

Disclosures

Jose U. Scher, MD, received consulting fees from: Janssen, Novartis, Pfizer, Sanofi, UCB, Amgen and AbbVie; research funding from the National Institutes of Health, the National Psoriasis Foundation, Beatrice Snyder Foundation, Bloomberg Philanthropies, Janssen and Pfizer.

Rebecca H. Haberman, MD, received consulting fees from Janssen; research funding from the National Institutes of Health, the National Psoriasis Foundation, the Rheumatology Research Foundation, Beatrice Snyder Foundation, Bloomberg Philanthropies, Janssen and Pfizer.

References

1. Glickman FS. Lepra, psora, psoriasis. J Am Acad Dermatol. 1986 May;14(5 Pt 1):863–866.
2. Alibert J-L. Précis théorique et pratique sur les maladies de la peau … par M. Alibert. Paris: Caille et Ravier. 1822.
3. Bazin E, Sergent L. Leçons théoriques et cliniques sur les affections cutanées de nature arthritique et dartreuse considérées en ellesmême et dans leurs rapports avec les éruptions scrofuleuses, parasitaires et syphilitiques réd. et publ. par Lucien Sergent. Paris: A. Delahaye. 1860.
4. Li Q, Chandran V, Tsoi L, et al. Quantifying differences in heritability among psoriatic arthritis (PsA), cutaneous psoriasis (PsC) and psoriasis vulgaris (PsV). Sci Rep. 2020 Mar 18;10(1):4925.
5. Winchester R, Minevich G, Steshenko V, et al. HLA associations reveal genetic heterogeneity in psoriatic arthritis and in the psoriasis phenotype. Arthritis Rheum. 2012 Apr;64(4):1134–1344.
6. Lønnberg AS, Skov L, Skytthe A, et al. Heritability of psoriasis in a large twin sample. Br J Dermatol. 2013 Aug;169(2):412–416.
7. Grjibovski AM, Olsen AO, Magnus P, et al. Psoriasis in Norwegian twins: Contribution of genetic and environmental effects. J Eur Acad Dermatol Venereol. 2007 Nov;21(10):1337–1343.
8. Gervin K, Vigeland MD, Mattingsdal M, et al. DNA methylation and gene expression changes in monozygotic twins discordant for psoriasis: Identification of epigenetically dysregulated genes. PLoS Genet. 2012 Jan;8(1):e1002454.
9. Brodin P, Jojic V, Gao T, et al. Variation in the human immune system is largely driven by non-heritable influences. Cell. 2015 Jan;160(1–2):37–47.
10. Kobner H. Zur atiologie der psoriasis. Vjschr Dermatol. 1876;3:559.
11. Thorarensen SM, Lu N, Ogdie A, et al. Physical trauma recorded in primary care is associated with the onset of psoriatic arthritis among patients with psoriasis. Ann Rheum Dis. 2017 Mar;76(3):521–525.
12. Ritchlin CT, Colbert RA, Gladman DD. Psoriatic Arthritis. N Engl J Med. 2017 May 25;376(21):2095–2096.
13. Clemente JC, Manasson J, Scher JU. The role of the gut microbiome in systemic inflammatory disease. BMJ. 2018 Jan 8;360:j5145.
14. Scher JU, Ubeda C, Artacho A, et al. Decreased bacterial diversity characterizes the altered gut microbiota in patients with psoriatic arthritis, resembling dysbiosis in inflammatory bowel disease. Arthritis Rheumatol. 2015 Jan;67(1):128–139.
15. Manasson J, Blank RB, Scher JU. The microbiome in rheumatology: Where are we and where should we go? Ann Rheum Dis. 2020 Jun;79(6):727–733.
16. Taurog JD, Richardson JA, Croft JT, et al. The germfree state prevents development of gut and joint inflammatory disease in HLA-B27 transgenic rats. J Exp Med. 1994 Dec;180(6):2359–2364.
17. Rehaume LM, Matigian N, Ormerod K, et al. IL-23 promotes fecal microbiota dysbiosis associated with susceptibility to spondyloarthritis and ileitis in ZAP-70 mutant SKG mice [abstract 1576]. Arthritis Rheumatol. 2017;69(suppl 10).
18. Manasson J, Wallach DS, Guggino G, et al. Interleukin-17 inhibition in spondyloarthritis is associated with subclinical gut microbiome perturbations and a distinctive interleukin-25-driven intestinal inflammation. Arthritis Rheumatol. 2020 Apr;72(4):645–657.
19. Alekseyenko AV, Perez-Perez GI, De Souza A, et al. Community differentiation of the cutaneous microbiota in psoriasis. Microbiome. 2013 Dec 23;1(1):31.
20. Shapiro J, Cohen NA, Shalev V, et al. Psoriatic patients have a distinct structural and functional fecal microbiota compared with controls. J Dermatol. 2019 Jul;46(7):595–603.
21. Kragsnaes MS, Kjeldsen J, Horn HC, et al. Safety and efficacy of faecal microbiota transplantation for active peripheral psoriatic arthritis: An exploratory randomised placebo-controlled trial. Ann Rheum Dis. 2021 Sep;80(9):1158–1167.
22. Ciccia F, Bombardieri M, Principato A, et al. Overexpression of interleukin-23, but not interleukin-17, as an immunologic signature of subclinical intestinal inflammation in ankylosing spondylitis. Arthritis Rheum. 2009 Apr;60(4):955–965.
23. Kenna TJ, Davidson SI, Duan R, et al. Enrichment of circulating interleukin-17-secreting interleukin-23 receptor-positive gamma/delta T cells in patients with active ankylosing spondylitis. Arthritis Rheum. 2012 May;64(5):1420–1429.
24. Gracey E, Qaiyum Z, Almaghlouth I, et al. IL-7 primes IL-17 in mucosalassociated invariant T (MAIT) cells, which contribute to the Th17-axis in ankylosing spondylitis. Ann Rheum Dis. 2016 Dec;75(12):2124–2132.
25. Veale D, Farrell M, Fitzgerald O. Mechanism of joint sparing in a patient with unilateral psoriatic arthritis and a longstanding hemiplegia. Br J Rheumatol. 1993 May;32(5):413–416.
26. Wang TS, Tsai TF. Psoriasis sparing the lower limb with postpoliomyelitis residual paralysis. Br J Dermatol. 2014 Aug;171(2):429–431.\
27. Weiner SR, Bassett LW, Reichman RP. Protective effect of poliomyelitis on psoriatic arthritis. Arthritis Rheum. 1985 Jun;28(6):703–706.
28. Riol-Blanco L, Ordovas-Montanes J, Perro M, et al. Nociceptive sensory neurons drive interleukin-23-mediated psoriasiform skin inflammation. Nature. 2014 June 5;510(7503):157–161.
29. Bordon Y. Neuroimmunology: A sensational IL-23 response. Nat Rev Immunol. 2014 Jun;14(6):354.
30. Kane D, Lockhart JC, Balint PV, et al. Protective effect of sensory denervation in inflammatory arthritis (evidence of regulatory neuroimmune pathways in the arthritic joint). Ann Rheum Dis. 2005 Feb;64(2):325–327.
31. Marsal S, Corominas H, de Agustín JJ, et al. Non-invasive vagus nerve stimulation for rheumatoid arthritis: A proof-of-concept study. Lancet Rheumatol. 2021 Apr;3(4):e262–e69.
32. Basu N, Kaplan CM, Ichesco E, et al. Neurobiologic features of fibromyalgia are also present among rheumatoid arthritis patients. Arthritis Rheumatol. 2018 Jul;70(7):1000–1007.
33. Schrepf A, Kaplan CM, Ichesco E, et al. A multi-modal MRI study of the central response to inflammation in rheumatoid arthritis. Nat Commun. 2018 Jun 8;9(1):2243.
34. Kanamori H, Tanaka M, Kawaguchi H, et al. Resolution of psoriasis following allogeneic bone marrow transplantation for chronic myelogenous leukemia: Case report and review of the literature. Am J Hematol. 2002 Sep;71(1):41–44.
35. Hinterberger W, Hinterberger-Fischer M, Marmont A. Clinically demonstrable anti-autoimmunity mediated by allogeneic immune cells favorably affects outcome after stem cell transplantation in human autoimmune diseases. Bone Marrow Transplant. 2002 Dec;30(11):753–759.
36. Annunziato F, Cosmi L, Santarlasci V, et al. Phenotypic and functional features of human Th17 cells. J Exp Med. 2007 Aug 6;204(8):1849–1861.
37. Korn T, Bettelli E, Oukka M, et al. IL-17 and Th17 Cells. Annu Rev Immunol. 2009;27:485–517.
38. Leipe J, Grunke M, Dechant C, et al. Role of Th17 cells in human autoimmune arthritis. Arthritis Rheum. 2010 Oct;62(10):2876–2885.
39. Cauli A, Mathieu A. Th17 and interleukin 23 in the pathogenesis of psoriatic arthritis and spondyloarthritis. J Rheumatol Suppl. 2012 Jul;89:15–18.
40. Leonardi C, Matheson R, Zachariae C, et al. Anti-interleukin-17 monoclonal antibody ixekizumab in chronic plaque psoriasis. N Eng J Med. 2012 Mar 29;366(13):1190–1199.
41. McInnes IB, Mease PJ, Kirkham B, et al. Secukinumab, a human anti-interleukin-17A monoclonal antibody, in patients with psoriatic arthritis (FUTURE 2): A randomised, double-blind, placebocontrolled, phase 3 trial. Lancet. 2015 Sep 19;386(9999):1137–1146.
42. Sherlock JP, Joyce-Shaikh B, Turner SP, et al. IL-23 induces spondyloarthropathy by acting on ROR-gammat+ CD3+CD4-CD8-entheseal resident T cells. Nat Med. 2012 Jul 1;18(7):1069–1076.
43. Menon B, Gullick NJ, Walter GJ, et al. Interleukin-17+CD8+ T cells are enriched in the joints of patients with psoriatic arthritis and correlate with disease activity and joint damage progression. Arthritis Rheumatol. 2014 May;66(5):1272–1281.
44. Costello P, Bresnihan B, O’Farrelly C, et al. Predominance of CD8+ T lymphocytes in psoriatic arthritis. J Rheumatol. 1999 May;26(5):1117–1124.
45. Penkava F, Velasco-Herrera MDC, Young MD, et al. Single-cell sequencing reveals clonal expansions of pro-inflammatory synovial CD8 T cells expressing tissue-homing receptors in psoriatic arthritis. Nat Commun. 2020 Sep 21;11(1):4767.
46. Steel KJA, Srenathan U, Ridley M, et al. Polyfunctional, proinflammatory, tissue-resident memory phenotype and function of synovial interleukin-17A+CD8+ T cells in psoriatic arthritis. Arthritis Rheumatol. 2020 Mar;72(3):435–447.
47. Belasco J, Louie JS, Gulati N, et al. Comparative genomic profiling of synovium versus skin lesions in psoriatic arthritis. Arthritis Rheumatol. 2015 Apr;67(4):934–944.
48. Nerviani A, Boutet M-A, Tan WSG, et al. IL-23 skin and joint profiling in psoriatic arthritis: Novel perspectives in understanding clinical responses to IL-23 inhibitors. Ann Rheum Dis. 2021 May;80(5):591–597.
49. Ritchlin CT, Haas-Smith SA, Li P, et al. Mechanisms of TNF-alpha- and RANKL-mediated osteoclastogenesis and bone resorption in psoriatic arthritis. J Clin Invest. 2003 Mar;111(6):821–831.
50. Sato K, Suematsu A, Okamoto K, et al. Th17 functions as an osteoclastogenic helper T cell subset that links T cell activation and bone destruction. J Exp Med. 2006 Nov 27;203(12):2673–2682.
51. Scher JU. The 2018 landscape of RA, PsA, and SpA pathogenesis. Curr Opin Rheumatol. 2018 Jan;30(1):57–58.
52. Armstrong AW, Siegel MP, Bagel J, et al. From the Medical Board of the National Psoriasis Foundation: Treatment targets for plaque psoriasis. J Am Acad Dermatol. 2017 Feb;76(2):290–298.
53. Mease PJ, van der Heijde D, Ritchlin CT, et al. Ixekizumab, an interleukin-17A specific monoclonal antibody, for the treatment of biologic-naive patients with active psoriatic arthritis: results from the 24-week randomised, double-blind, placebo-controlled and active (adalimumab)-controlled period of the phase III trial SPIRIT-P1. Ann Rheum Dis. 2017 Jan;76(1):79–87.
54. Mease PJ, Gladman DD, Ritchlin CT, et al. Adalimumab for the treatment of patients with moderately to severely active psoriatic arthritis: results of a double-blind, randomized, placebo-controlled trial. Arthritis Rheum. 2005 Oct;52(10):3279–3289.
55. Ritchlin C, Scher JU. Strategies to improve outcomes in psoriatic arthritis. Curr Rheumatol Rep. 2019 Dec 7;21(12):72.
56. Haberman RH, Castillo R, Scher JU. Induction of remission in biologic-naive, severe psoriasis and PsA with dual anticytokine combination. Rheumatology (Oxford). 2021 Jul 1;60(7):e225–e226.
57. National Institutes of Health-Accelerating Medicines Partnership Autoimmune and Immune Mediated Diseases Program. https://www.niams.nih.gov/grants-funding/niams-supported-research-programs/accelerating-medicines-partnership-amp
58. Scher JU, Ogdie A, Merola JF, et al. Moving the goalpost toward remission: The case for combination immunomodulatory therapies in psoriatic arthritis. Arthritis Rheumatol. 2021 Sep;73(9):1574–1578.
59. Scher JU, Ogdie A, Merola JF, et al. Preventing psoriatic arthritis: Focusing on patients with psoriasis at increased risk of transition. Nat Rev Rheumatol. 2019 Mar;15(3):153–166.