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Review

Pathogenesis-oriented therapy of psoriasis using biologics

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Pages 1463-1473 | Received 04 May 2022, Accepted 07 Jul 2022, Published online: 20 Jul 2022

References

  • Boehncke WH, Schon MP. Psoriasis. Lancet. 2015;386(9997):983–994.
  • Griffiths CEM, Armstrong AW, Gudjonsson JE, et al. Psoriasis. Lancet. 2021;397(10281):1301–1315.
  • Clark RA. Resident memory T cells in human health and disease. Sci Transl Med. 2015;7(269):269rv1.
  • Boehncke WH, Dressel D, Zollner TM, et al. Pulling the trigger on psoriasis. Nature. 1996;379(6568):777.
  • Lande R, Gregorio J, Facchinetti V, et al. Plasmacytoid dendritic cells sense self-DNA coupled with antimicrobial peptide. Nature. 2007;449(7162):564–569.
  • Veldhoen M, Hocking RJ, Atkins CJ, et al. TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity. 2006;24(2):179–189.
  • Brembilla NC, Senra L, Boehncke WH. The IL-17 family of cytokines in psoriasis: IL-17A and beyond. Front Immunol. 2018;9:1682.
  • Girolomoni G, Strohal R, Puig L, et al. The role of IL-23 and the IL-23/TH 17 immune axis in the pathogenesis and treatment of psoriasis. J Eur Acad Dermatol Venereol. 2017;31(10):1616–1626.
  • Ehst B, Wang Z, Leitenberger J, et al. Synergistic induction of IL-23 by TNFalpha, IL-17A, and EGF in keratinocytes. Cytokine. 2021;138:155357.
  • Cole S, Murray J, Simpson C, et al. Interleukin (IL)-12 and IL-18 synergize to promote MAIT cell IL-17A and IL-17F production independently of IL-23 signaling. Front Immunol. 2020;11:585134.
  • Uttarkar S, Brembilla NC, Boehncke WH. Regulatory cells in the skin: pathophysiologic role and potential targets for anti-inflammatory therapies. J Allergy Clin Immunol. 2019;143(4):1302–1310.
  • Boehncke WH, Ochsendorf FR, Noll S, et al. Efficacy of the fully human monoclonal antibody MOR102 (#5) against intercellular adhesion molecule 1 in the psoriasis-severe combined immunodeficient mouse model. Br J Dermatol. 2005;153(4):758–766.
  • Sobell JM, Kalb RE, Weinberg JM. Management of moderate to severe plaque psoriasis (part 2): clinical update on T-cell modulators and investigational agents. J Drugs Dermatol. 2009;8(3):230–238.
  • Boehncke WH, Schon MP, Girolomoni G, et al. Leukocyte extravasation as a target for anti-inflammatory therapy - which molecule to choose? Exp Dermatol. 2005;14(1):70–80.
  • Dostert C, Grusdat M, Letellier E, et al. The TNF family of ligands and receptors: communication modules in the immune system and beyond. Physiol Rev. 2019;99(1):115–160.
  • Ward-Kavanagh LK, Lin WW, Sedy JR, et al. The TNF receptor superfamily in co-stimulating and co-inhibitory responses. Immunity. 2016;44(5):1005–1019.
  • Pasparakis M, Alexopoulou L, Episkopou V, et al. Immune and inflammatory responses in TNF alpha-deficient mice: a critical requirement for TNF alpha in the formation of primary B cell follicles, follicular dendritic cell networks and germinal centers, and in the maturation of the humoral immune response. J Exp Med. 1996;184(4):1397–1411.
  • Parameswaran N, Patial S. Tumor necrosis factor-alpha signaling in macrophages. Crit Rev Eukaryot Gene Expr. 2010;20(2):87–103.
  • Bean AG, Roach DR, Briscoe H, et al. Structural deficiencies in granuloma formation in TNF gene-targeted mice underlie the heightened susceptibility to aerosol Mycobacterium tuberculosis infection, which is not compensated for by lymphotoxin. J Immunol. 1999;162(6):3504–3511.
  • Roach DR, Bean AG, Demangel C, et al. TNF regulates chemokine induction essential for cell recruitment, granuloma formation, and clearance of mycobacterial infection. J Immunol. 2002;168(9):4620–4627.
  • Sheng Y, Li F, Qin Z. TNF receptor 2 makes tumor necrosis factor a friend of tumors. Front Immunol. 2018;9:1170.
  • Kondo N, Kuroda T, Kobayashi D. Cytokine networks in the pathogenesis of rheumatoid arthritis. Int J Mol Sci. 2021;22(20):10922.
  • Ruder B, Atreya R, Becker C. Tumour necrosis factor alpha in intestinal homeostasis and gut related diseases. Int J Mol Sci. 2019;20(8):1887.
  • Neurath MF. Cytokines in inflammatory bowel disease. Nat Rev Immunol. 2014;14(5):329–342.
  • Holtmann MH, Douni E, Schutz M, et al. Tumor necrosis factor-receptor 2 is up-regulated on lamina propria T cells in Crohn’s disease and promotes experimental colitis in vivo. Eur J Immunol. 2002;32(11):3142–3151.
  • Perrier C, de Hertogh G, Cremer J, et al. Neutralization of membrane TNF, but not soluble TNF, is crucial for the treatment of experimental colitis. Inflamm Bowel Dis. 2013;19(2):246–253.
  • Urschel K, Cicha I. TNF-a in the cardiovascular system: from physiology to therapy. Int J Interferon Cytokine Mediat Res. 2015;7:9–25.
  • Probert L. TNF and its receptors in the CNS: the essential, the desirable and the deleterious effects. Neuroscience. 2015;302:2–22.
  • Papazian I, Tsoukala E, Boutou A, et al. Fundamentally different roles of neuronal TNF receptors in CNS pathology: TNFR1 and IKKbeta promote microglial responses and tissue injury in demyelination while TNFR2 protects against excitotoxicity in mice. J Neuroinflammation. 2021;18(1):222.
  • Tait Wojno ED, Hunter CA, Stumhofer JS. The immunobiology of the interleukin-12 family: room for discovery. Immunity. 2019;50(4):851–870.
  • Ullrich KA, Schulze LL, Paap EM, et al. Immunology of IL-12: an update on functional activities and implications for disease. EXCLI J. 2020;19:1563–1589.
  • Trinchieri G. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat Rev Immunol. 2003;3(2):133–146.
  • Hsieh CS, Macatonia SE, Tripp CS, et al. Development of TH1 CD4+ T cells through IL-12 produced by Listeria-induced macrophages. Science. 1993;260(5107):547–549.
  • Mirlekar B, Pylayeva-Gupta Y. IL-12 family cytokines in cancer and immunotherapy. Cancers (Basel). 2021;13(2):167.
  • Eftychi C, Schwarzer R, Vlantis K, et al. Temporally distinct functions of the cytokines IL-12 and IL-23 drive chronic colon inflammation in response to intestinal barrier impairment. Immunity. 2019;51(2):367–380 e4.
  • Hanauer SB, Sandborn WJ, Feagan BG, et al. IM-UNITI: three-year efficacy, safety, and immunogenicity of ustekinumab treatment of Crohn’s disease. J Crohns Colitis. 2020;14(1):23–32.
  • van der Heijden T, Bot I, Kuiper J. The IL-12 cytokine family in cardiovascular diseases. Cytokine. 2019;122:154188.
  • Grifka-Walk HM, Giles DA, Segal BM. IL-12-polarized Th1 cells produce GM-CSF and induce EAE independent of IL-23. Eur J Immunol. 2015;45(10):2780–2786.
  • Parham C, Chirica M, Timans J, et al. A receptor for the heterodimeric cytokine IL-23 is composed of IL-12Rbeta1 and a novel cytokine receptor subunit, IL-23R. J Immunol. 2002;168(11):5699–5708.
  • Gaffen SL, Jain R, Garg AV, et al. The IL-23-IL-17 immune axis: from mechanisms to therapeutic testing. Nat Rev Immunol. 2014;14(9):585–600.
  • Yan J, Smyth MJ, Teng MWL. Interleukin (IL)-12 and IL-23 and their conflicting roles in cancer. Cold Spring Harb Perspect Biol. 2018;10(7):a028530.
  • Cua DJ, Sherlock J, Chen Y, et al. Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature. 2003;421(6924):744–748.
  • Murphy CA, Langrish CL, Chen Y, et al. Divergent pro- and antiinflammatory roles for IL-23 and IL-12 in joint autoimmune inflammation. J Exp Med. 2003;198(12):1951–1957.
  • McGeachy MJ, Cua DJ, Gaffen SL. The IL-17 family of cytokines in health and disease. Immunity. 2019;50(4):892–906.
  • Zhao J, Chen X, Herjan T, et al. The role of interleukin-17 in tumor development and progression. J Exp Med. 2020;217(1).
  • Taams LS. Interleukin-17 in rheumatoid arthritis: trials and tribulations. J Exp Med. 2020;217(3).
  • Kirkham BW, Kavanaugh A, Reich K. Interleukin-17A: a unique pathway in immune-mediated diseases: psoriasis, psoriatic arthritis and rheumatoid arthritis. Immunology. 2014;141(2):133–142.
  • Maxwell JR, Zhang Y, Brown WA, et al. Differential roles for interleukin-23 and interleukin-17 in intestinal immunoregulation. Immunity. 2015;43(4):739–750.
  • Lee JS, Tato CM, Joyce-Shaikh B, et al. Interleukin-23-independent il-17 production regulates intestinal epithelial permeability. Immunity. 2015;43(4):727–738.
  • Gelderblom M, Weymar A, Bernreuther C, et al. Neutralization of the IL-17 axis diminishes neutrophil invasion and protects from ischemic stroke. Blood. 2012;120(18):3793–3802.
  • Kang Z, Wang C, Zepp J, et al. Act 1 mediates IL-17-induced EAE pathogenesis selectively in NG2+ glial cells. Nat Neurosci. 2013;16(10):1401–1408.
  • Robert M, Miossec P. Effects of Interleukin 17 on the cardiovascular system. Autoimmun Rev. 2017;16(9):984–991.
  • Swedik S, Madola A, Levine A. IL-17C in human mucosal immunity: more than just a middle child. Cytokine. 2021;146:155641.
  • Kleinschek MA, Owyang AM, Joyce-Shaikh B, et al. IL-25 regulates Th17 function in autoimmune inflammation. J Exp Med. 2007;204(1):161–170.
  • Deleuran M, Hvid M, Kemp K, et al. IL-25 induces both inflammation and skin barrier dysfunction in atopic dermatitis. Chem Immunol Allergy. 2012;96:45–49.
  • Senra L, Mylonas A, Kavanagh RD, et al. IL-17E (IL-25) enhances innate immune responses during skin inflammation. J Invest Dermatol. 2019;139(8):1732–1742 e17.
  • Senra L, Stalder R, Alvarez Martinez D, et al. Keratinocyte-derived IL-17E contributes to inflammation in psoriasis. J Invest Dermatol. 2016;136(10):1970–1980.
  • Suto H, Nambu A, Morita H, et al. IL-25 enhances TH17 cell-mediated contact dermatitis by promoting IL-1beta production by dermal dendritic cells. J Allergy Clin Immunol. 2018;142(5):1500–1509 e10.
  • Gottlieb SL, Gilleaudeau P, Johnson R, et al. Response of psoriasis to a lymphocyte-selective toxin (DAB389IL-2) suggests a primary immune, but not keratinocyte, pathogenic basis. Nat Med. 1995;1(5):442–447.
  • Saurat JH, Stingl G, Dubertret L, et al. Efficacy and safety results from the randomized controlled comparative study of Adalimumab vs. methotrexate vs. placebo in patients with psoriasis (CHAMPION). Br J Dermatol. 2008;158(3):558–566.
  • Nast A, Altenburg A, Augustin M, et al. German S3-Guideline on the treatment of Psoriasis vulgaris, adapted from EuroGuiDerm - Part 1: treatment goals and treatment recommendations. J Dtsch Dermatol Ges. 2021;19(6):934.
  • Gossec L, Baraliakos X, Kerschbaumer A, et al. EULAR recommendations for the management of psoriatic arthritis with pharmacological therapies: 2019 update. Ann Rheum Dis. 2020;79(6):700–712.
  • Nast A, Altenburg A, Augustin M, et al. German S3-Guideline on the treatment of Psoriasis vulgaris, adapted from EuroGuiDerm - Part 2: treatment monitoring and specific clinical or comorbid situations. J Dtsch Dermatol Ges. 2021;19(7):1092–1115.
  • Sbidian E, Chaimani A, Garcia-Doval I, et al. Systemic pharmacological treatments for chronic plaque psoriasis: a network meta-analysis. Cochrane Database Syst Rev. 2021;4:CD011535.
  • Strain J, Leis M, Lee KO, et al. Certolizumab pegol in plaque psoriasis: considerations for pregnancy. Skin Therapy Lett. 2021;26(2):1–5.
  • Mariette X, Forger F, Abraham B, et al. Lack of placental transfer of certolizumab pegol during pregnancy: results from CRIB, a prospective, postmarketing, pharmacokinetic study. Ann Rheum Dis. 2018;77(2):228–233.
  • Caminero A, Comabella M, Montalban X. Tumor necrosis factor alpha (TNF-alpha), anti-TNF-alpha and demyelination revisited: an ongoing story. J Neuroimmunol. 2011;234(1–2):1–6.
  • Bardazzi F, Odorici G, Virdi A, et al. Autoantibodies in psoriatic patients treated with anti-TNF-alpha therapy. J Dtsch Dermatol Ges. 2014;12(5):401–406.
  • Boehncke WH, Brembilla NC. Immunogenicity of biologic therapies: causes and consequences. Expert Rev Clin Immunol. 2018;14(6):513–523.
  • Boehncke WH, Boehncke S, Tobin AM, et al. The ‘psoriatic march’: a concept of how severe psoriasis may drive cardiovascular comorbidity. Exp Dermatol. 2011;20(4):303–307.
  • Boehncke S, Salgo R, Garbaraviciene J, et al. Effective continuous systemic therapy of severe plaque-type psoriasis is accompanied by amelioration of biomarkers of cardiovascular risk: results of a prospective longitudinal observational study. J Eur Acad Dermatol Venereol. 2011;25(10):1187–1193.
  • Wu JJ, Sundaram M, Cloutier M, et al. The risk of cardiovascular events in psoriasis patients treated with tumor necrosis factor-alpha inhibitors versus phototherapy: an observational cohort study. J Am Acad Dermatol. 2018;79(1):60–68.
  • Wegner J, Karbach S, Drosos I, et al. TNF-alpha blockade may lead to improvement of vascular function in psoriasis patients. Exp Dermatol. 2022;31(2):237–241.
  • Gooderham MJ, Papp KA, Lynde CW. Shifting the focus - the primary role of IL-23 in psoriasis and other inflammatory disorders. J Eur Acad Dermatol Venereol. 2018;32(7):1111–1119.
  • Griffiths CE, Strober BE, van de Kerkhof P, et al. Comparison of ustekinumab and etanercept for moderate-to-severe psoriasis. N Engl J Med. 2010;362(2):118–128.
  • Zhao Y, Liu Z, Qin L, et al. Insights into the mechanisms of Th17 differentiation and the Yin-Yang of Th17 cells in human diseases. Mol Immunol. 2021;134:109–117.
  • Mehta H, Mashiko S, Angsana J, et al. Differential changes in inflammatory mononuclear phagocyte and T-cell profiles within psoriatic skin during treatment with guselkumab vs. secukinumab. J Invest Dermatol. 2021;141(7):1707–1718 e9.
  • Brembilla NC, Stalder R, Senra L, et al. IL-17A localizes in the exocytic compartment of mast cells in psoriatic skin. Br J Dermatol. 2017;177(5):1458–1460.
  • Langley RG, Elewski BE, Lebwohl M, et al. Secukinumab in plaque psoriasis–results of two phase 3 trials. N Engl J Med. 2014;371(4):326–338.
  • Menter A, Warren RB, Langley RG, et al. Efficacy of ixekizumab compared to etanercept and placebo in patients with moderate-to-severe plaque psoriasis and non-pustular palmoplantar involvement: results from three phase 3 trials (UNCOVER-1, UNCOVER-2 and UNCOVER-3). J Eur Acad Dermatol Venereol. 2017;31(10):1686–1692.
  • Pappu R, Ramirez-Carrozzi V, Sambandam A. The interleukin-17 cytokine family: critical players in host defence and inflammatory diseases. Immunology. 2011;134(1):8–16.
  • Glatt S, Baeten D, Baker T, et al. Dual IL-17A and IL-17F neutralisation by bimekizumab in psoriatic arthritis: evidence from preclinical experiments and a randomised placebo-controlled clinical trial that IL-17F contributes to human chronic tissue inflammation. Ann Rheum Dis. 2018;77(4):523–532.
  • Borowczyk J, Shutova M, Brembilla NC, et al. IL-25 (IL-17E) in epithelial immunology and pathophysiology. J Allergy Clin Immunol. 2021;148(1):40–52.
  • Rodriguez-Cerdeira C, Gonzalez-Cespon JL, Martinez-Herrera E, et al. Candida infections in patients with psoriasis and psoriatic arthritis treated with interleukin-17 inhibitors and their practical management. Ital J Dermatol Venerol. 2021;156(5):545–557.
  • Nast A, Smith C, Spuls PI, et al. EuroGuiDerm guideline on the systemic treatment of Psoriasis vulgaris - Part 2: specific clinical and comorbid situations. J Eur Acad Dermatol Venereol. 2021;35(2):281–317.
  • Armstrong AW, Blauvelt A, Mrowietz U, et al. A practical guide to the management of oral candidiasis in patients with plaque psoriasis receiving treatments that target interleukin-17. Dermatol Ther. 2022;12(3):787–800.
  • Burisch J, Eigner W, Schreiber S, et al. Risk for development of inflammatory bowel disease under inhibition of interleukin 17: a systematic review and meta-analysis. PLoS One. 2020;15(5):e0233781.
  • Wack S, Patton T, Ferris LK. COVID-19 vaccine safety and efficacy in patients with immune-mediated inflammatory disease: review of available evidence. J Am Acad Dermatol. 2021;85(5):1274–1284.
  • Tang Z, Shen M, Chen X. Risk of herpes zoster among psoriasis patients taking biologics: a network meta-analysis of cohort studies. Front Med. 2021;8:665559.
  • Gordon KB, Blauvelt A, Papp KA, et al. Phase 3 trials of ixekizumab in moderate-to-severe plaque psoriasis. N Engl J Med. 2016;375(4):345–356.
  • Reich K, Warren RB, Lebwohl M, et al. Bimekizumab versus secukinumab in plaque psoriasis. N Engl J Med. 2021;385(2):142–152.
  • Warren RB, Blauvelt A, Poulin Y, et al. Efficacy and safety of risankizumab vs. secukinumab in patients with moderate-to-severe plaque psoriasis (IMMerge): results from a phase III, randomized, open-label, efficacy-assessor-blinded clinical trial. Br J Dermatol. 2021;184(1):50–59.
  • Reich K, Armstrong AW, Langley RG, et al. Guselkumab versus secukinumab for the treatment of moderate-to-severe psoriasis (ECLIPSE): results from a phase 3, randomised controlled trial. Lancet. 2019;394(10201):831–839.
  • Coates LC, Kavanaugh A, Mease PJ, et al. Group for research and assessment of psoriasis and psoriatic arthritis 2015 treatment recommendations for psoriatic arthritis. Arthritis Rheumatol. 2016;68(5):1060–1071.
  • Cushing K, Higgins PDR. Management of Crohn Disease: a Review. Jama. 2021;325(1):69–80.
  • Boehncke WH. Systemic inflammation and cardiovascular comorbidity in psoriasis patients: causes and consequences. Front Immunol. 2018;9:579.
  • Tseng WY, Huang YS, Lin HH, et al. TNFR signalling and its clinical implications. Cytokine. 2018;101:19–25.
  • von Stebut E, Boehncke WH, Ghoreschi K, et al. IL-17A in psoriasis and beyond: cardiovascular and metabolic implications. Front Immunol. 2019;10:3096.
  • Boehncke WH, Brembilla NC, Nissen MJ. Guselkumab: the first selective IL-23 inhibitor for active psoriatic arthritis in adults. Expert Rev Clin Immunol. 2021;17(1):5–13.
  • McInnes IB, Kavanaugh A, Gottlieb AB, et al. Efficacy and safety of ustekinumab in patients with active psoriatic arthritis: 1 year results of the phase 3, multicentre, double-blind, placebo-controlled PSUMMIT 1 trial. Lancet. 2013;382(9894):780–789.
  • Mease P, van den Bosch F. IL-23 and axial disease: do they come together? Rheumatology. 2021;60(Suppl 4):iv28–iv33.
  • Gilliet M. Targeted therapies and precision medicine for inflammatory skin diseases. Eur J Dermatol. 2019;29(S1):19–24.
  • Krishnan VS, Koks S. Transcriptional basis of psoriasis from large scale gene expression studies: the importance of moving towards a precision medicine approach. Int J Mol Sci. 2022;23(11):6130.

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