Biological agents targeting interleukin-13 for atopic dermatitis

References

• Odhiambo JA, Williams HC, Clayton TO, et al. Global variations in prevalence of eczema symptoms in children from ISAAC Phase Three. J Allergy Clin Immunol. 2009;124(6):1251–8 e23.
   PubMed Web of Science ®Google Scholar
• Amat F, Soria A, Tallon P, et al. New insights into the phenotypes of atopic dermatitis linked with allergies and asthma in children: an overview. Clin Exp Allergy. 2018;48(8):919–934.
   PubMed Web of Science ®Google Scholar
• Langan SM, Irvine AD, Weidinger S. Atopic dermatitis. Lancet. 2020;396(10247):345–360.
   PubMed Web of Science ®Google Scholar
• Cheng BT, Silverberg JI. Depression and psychological distress in US adults with atopic dermatitis. Ann Allergy Asthma Immunol. 2019;123(2):179–185.
   PubMed Web of Science ®Google Scholar
• Dubin C, Del Duca E, Guttman-Yassky E. The IL-4, IL-13 and IL-31 pathways in atopic dermatitis. Expert Rev Clin Immunol. 2021;17(8):835–852.
   PubMed Web of Science ®Google Scholar
• Boguniewicz M, Leung DYM. Recent insights into atopic dermatitis and implications for management of infectious complications. J Allergy Clin Immunol. 2010;125(1):4–13.
   PubMed Web of Science ®Google Scholar
• Pastore S, Mascia F, Girolomoni G. The contribution of keratinocytes to the pathogenesis of atopic dermatitis. Eur J Dermatol. 2006;16(2):125–131.
   PubMed Web of Science ®Google Scholar
• Kong HH, Oh J, Deming C, et al. Temporal shifts in the skin microbiome associated with disease flares and treatment in children with atopic dermatitis. Genome Res. 2012;22(5):850–859.
   PubMed Web of Science ®Google Scholar
• Tubau C, Puig L. Therapeutic targeting of the IL-13 pathway in skin inflammation. Expert Rev Clin Immunol. 2021;17(1):15–25.
   PubMed Web of Science ®Google Scholar
• Garcovich S, Maurelli M, Gisondi P, et al. Pruritus as a distinctive feature of type 2 inflammation. Vaccines (Basel). 2021;9(3):303.
   PubMed Web of Science ®Google Scholar
• Brunner PM, Guttman-Yassky E, Leung DY. The immunology of atopic dermatitis and its reversibility with broad-spectrum and targeted therapies. J Allergy Clin Immunol. 2017;139(4S):S65–S76.
   PubMed Web of Science ®Google Scholar
• Ungar B, Garcet S, Gonzalez J, et al. An integrated model of atopic dermatitis biomarkers highlights the systemic nature of the disease. J Invest Dermatol. 2017;137(3):603–613.
   PubMed Web of Science ®Google Scholar
• Brunner PM, Suárez-Fariñas M, He H, et al. The atopic dermatitis blood signature is characterized by increases in inflammatory and cardiovascular risk proteins. Sci Rep. 2017;7(1):8707. Erratum in: Sci Rep. 2018;8(1):8439.
   PubMed Web of Science ®Google Scholar
• Suárez-Fariñas M, Tintle SJ, Shemer A, et al. Nonlesional atopic dermatitis skin is characterized by broad terminal differentiation defects and variable immune abnormalities. J Allergy Clin Immunol. 127(4): 954–64.e1-4. 2011.
   PubMed Web of Science ®Google Scholar
• Gittler JK, Shemer A, Suárez-Fariñas M, et al. Progressive activation of T(H)2/T(H)22 cytokines and selective epidermal proteins characterizes acute and chronic atopic dermatitis. J Allergy Clin Immunol. 2012;130(6):1344–1354.
   PubMed Web of Science ®Google Scholar
• Koppes SA, Brans R, Ljubojevic Hadzavdic S, et al. Stratum corneum tape stripping: monitoring of inflammatory mediators in atopic dermatitis patients using topical therapy. Int Arch Allergy Immunol. 2016;170(3):187–193.
   PubMed Web of Science ®Google Scholar
• La Grutta S, Richiusa P, Pizzolanti G, et al. CD4(+)IL-13(+) cells in peripheral blood well correlates with the severity of atopic dermatitis in children. Allergy. 2005;60(3):391–395.
   PubMed Web of Science ®Google Scholar
• Hijnen D, Knol EF, Gent YY, et al. CD8(+) T cells in the lesional skin of atopic dermatitis and psoriasis patients are an important source of IFN-gamma, IL-13, IL-17, and IL-22. J Invest Dermatol. 2013;133(4):973–979.
   PubMed Web of Science ®Google Scholar
• Bangert C, Rindler K, Krausgruber T, et al. Persistence of mature dendritic cells, TH2A, and Tc2 cells characterize clinically resolved atopic dermatitis under IL-4Rα blockade. Sci Immunol. 2021;6(55):eabe2749.
   PubMed Web of Science ®Google Scholar
• Mashiko S, Mehta H, Bissonnette R, et al. Increased frequencies of basophils, type 2 innate lymphoid cells and Th2 cells in skin of patients with atopic dermatitis but not psoriasis. J Dermatol Sci. 2017;88(2):167–174.
   PubMed Web of Science ®Google Scholar
• Szegedi K, Lutter R, Res PC, et al. Cytokine profiles in interstitial fluid from chronic atopic dermatitis skin. J Eur Acad Dermatol Venereol. 2015;29(11):2136–2144.
   PubMed Web of Science ®Google Scholar
• Tsoi LC, Rodriguez E, Degenhardt F, et al. Atopic dermatitis is an IL-13-dominant disease with greater molecular heterogeneity compared to psoriasis. J Invest Dermatol. 2019;139(7):1480–1489.
   PubMed Web of Science ®Google Scholar
• Bieber T. Interleukin-13: targeting an underestimated cytokine in atopic dermatitis. Allergy. 2020;75(1):54–62.
   PubMed Web of Science ®Google Scholar
• Omori-Miyake M, Yamashita M, Tsunemi Y, et al. In vitro assessment of IL-4- or IL-13-mediated changes in the structural components of keratinocytes in mice and humans. J Invest Dermatol. 2014;134(5):1342–1350. Erratum in: J Invest Dermatol. 2018;138(2):472-473.
   PubMed Web of Science ®Google Scholar
• Howell MD, Kim BE, Gao P, et al. Cytokine modulation of atopic dermatitis filaggrin skin expression. J Allergy Clin Immunol. 2009;124:R7–R12.
   PubMed Web of Science ®Google Scholar
• Howell MD, Fairchild HR, Kim BE, et al. Th2 cytokines act on S100/A11 to downregulate keratinocyte differentiation. J Invest Dermatol. 2008;128(9):2248–2258.
   PubMed Web of Science ®Google Scholar
• Berdyshev E, Goleva E, Bronova I, et al. Lipid abnormalities in atopic skin are driven by type 2 cytokines. JCI Insight. 2018;3(4):4.
   Web of Science ®Google Scholar
• Agrawal R, Woodfolk JA. Skin barrier defects in atopic dermatitis. Curr Allergy Asthma Rep. 2014;14(5):433.
   PubMed Web of Science ®Google Scholar
• Nomura I, Goleva E, Howell MD, et al. Cytokine milieu of atopic dermatitis, as compared to psoriasis, skin prevents induction of innate immune response genes. J Immunol. 2003;171(6):3262–3269.
   PubMed Web of Science ®Google Scholar
• Nakatsuji T, Chen TH, Two AM, et al. Staphylococcus aureus exploits epidermal barrier defects in atopic dermatitis to trigger cytokine expression. J Invest Dermatol. 2016;136(11):2192–2200.
   PubMed Web of Science ®Google Scholar
• Nograles KE, Suárez-Fariñas M, Shemer A, et al. Atopic dermatitis keratinocytes exhibit normal T(H)17 cytokine responses. J Allergy Clin Immunol. 2010;125(3):744–6, 746.e1-746.e2.
   Web of Science ®Google Scholar
• Horie S, Okubo Y, Hossain M, et al. Interleukin-13 but not interleukin-4 prolongs eosinophil survival and induces eosinophil chemotaxis. Intern Med. 1997;36(3):179–185.
   PubMed Web of Science ®Google Scholar
• Fish SC, Donaldson DD, Goldman SJ, et al. IgE generation and mast cell effector function in mice deficient in IL-4 and IL-13. J Immunol. 2005;174(12):7716–7724.72.
   PubMed Web of Science ®Google Scholar
• Mayer JU, Hilligan KL, Chandler JS, et al. Homeostatic IL-13 in healthy skin directs dendritic cell differentiation to promote TH2 and inhibit TH17 cell polarization. Nat Immunol. 22(12): 1538–1550. 2021.
   PubMed Web of Science ®Google Scholar
• Purwar R, Werfel T, Wittmann M. IL-13-stimulated human keratinocytes preferentially attract CD4+CCR4+ T cells: possible role in atopic dermatitis. J Invest Dermatol. 2006;126(5):1043–1051.
   PubMed Web of Science ®Google Scholar
• Emson CL, Bell SE, Jones A, et al. Interleukin (IL)- 4-independent induction of immunoglobulin (Ig)E, and perturbation of T cell development in transgenic mice expressing IL-13. J Exp Med. 1998;188(2):399–404.
   PubMed Web of Science ®Google Scholar
• Moriya C, Jinnin M, Yamane K, et al. Expression of matrix metalloproteinase-13 is controlled by IL-13 via PI3K/Akt3 and PKC-δ in normal human dermal fibroblasts. J Invest Dermatol. 2011;131(3):655–661.
   PubMed Web of Science ®Google Scholar
• Oriente A, Fedarko NS, Pacocha SE, et al. Interleukin-13 modulates collagen homeostasis in human skin and keloid fibroblasts. J Pharmacol Exp Ther. 2000;292(3):988–994.100.
   PubMed Web of Science ®Google Scholar
• Bochner BS, Klunk DA, Sterbinsky SA, et al. IL-13 selectively induces vascular cell adhesion molecule-1 expression in human endothelial cells. J Immunol. 1995 Jan 15;154(2):799–803. PMID: 7529288.
   PubMed Web of Science ®Google Scholar
• Woltmann G, McNulty CA, Dewson G, et al. Interleukin-13 induces PSGL-1/P-selectin-dependent adhesion of eosinophils, but not neutrophils, to human umbilical vein endothelial cells under flow. Blood. 2000;95(10):3146–3152.
   PubMed Web of Science ®Google Scholar
• Oh M-H, Oh SY, Lu J, et al. TRPA1-dependent pruritus in IL-13–induced chronic atopic dermatitis. J Immunol. 2013;191(11):5371– 5382.
   PubMed Web of Science ®Google Scholar
• Zheng T, Oh MH, Oh SY, et al. Transgenic expression of interleukin-13 in the skin induces a pruritic dermatitis and skin remodeling. J Invest Dermatol. 2009;129(3):742–751.
   PubMed Web of Science ®Google Scholar
• Hoving JC, Nieuwenhuizen NE, Schäfer G, et al. IL-13 signals independent of IL-4 receptor-alpha chain to drive ovalbumin-induced dermatitis. J Invest Dermatol. 136(6): 1286–1290. 2016.
   PubMed Web of Science ®Google Scholar
• Xiao S, Lu Z, Steinhoff M, et al. Innate immune regulates cutaneous sensory IL-13 receptor alpha 2 to promote atopic dermatitis. Brain Behav Immun. 2021;98:28–39.
   PubMed Web of Science ®Google Scholar
• Blauvelt A, de Bruin-weller M, Gooderham M, et al. Long-term management of moderate-to-severe atopic dermatitis with dupilumab and concomitant topical corticosteroids (LIBERTY AD CHRONOS): a 1-year, randomised, double-blinded, placebo-controlled, phase 3 trial. Lancet. 2017;389(10086):2287–2303.
   PubMed Web of Science ®Google Scholar
• Nakashima C, Otsuka A, Kabashima K. Interleukin-31 and interleukin-31 receptor: new therapeutic targets for atopic dermatitis. Exp Dermatol. 2018;27(4):327–331.
   PubMed Web of Science ®Google Scholar
• Freitas E, Guttman-Yassky E, Torres T. Tralokinumab for the Treatment of Atopic Dermatitis. Am J Clin Dermatol. 2021;22(5):625–638.
   PubMed Web of Science ®Google Scholar
• Wollenberg A, Howell MD, Guttman-Yassky E, et al. Treatment of atopic dermatitis with tralokinumab, an anti-IL-13 mAb. J Allergy Clin Immunol. 2019;143(1):135–141.
   PubMed Web of Science ®Google Scholar
• Ungar B, Pavel AB, Li R, et al. Phase 2 randomized, double-blind study of IL-17 targeting with secukinumab in atopic dermatitis. J Allergy Clin Immunol. 2021;147(1):394–397.
   PubMed Web of Science ®Google Scholar
• Khattri S, Brunner PM, Garcet S, et al. Efficacy and safety of ustekinumab treatment in adults with moderate-to-severe atopic dermatitis. Exp Dermatol. 2017 Jan;26(1):28–35.
   PubMed Web of Science ®Google Scholar
• Simpson EL, Parnes JR, She D, et al. Tezepelumab, an anti–thymic stromal lymphopoietin monoclonal antibody, in the treatment of moderate to severe atopic dermatitis: a randomized phase 2a clinical trial. J Am Acad Dermatol. 2019;80(4):1013–1021.
   PubMed Web of Science ®Google Scholar
• Uppal SK, Kearns DG, Chat VS, et al. Review and analysis of biologic therapies currently in phase II and phase III clinical trials for atopic dermatitis. J Dermatol Treat. 2020;1–11. https://doi.org/10.1080/09546634.2020.1775775.
   Google Scholar
• Brunner PM, Pavel AB, Khattri S, et al. Baseline IL-22 expression in patients with atopic dermatitis stratifies tissue responses to fezakinumab. J Allergy Clin Immunol. 2019;143(1):142–154.
   PubMed Web of Science ®Google Scholar
• Guttman-Yassky E, Brunner PM, Neumann AU, et al. Efficacy and safety of fezakinumab (an IL-22 monoclonal antibody) in adults with moderate-to-severe atopic dermatitis inadequately controlled by conventional treatments: a randomized, double-blind, phase 2a trial. J Am Acad Dermatol. 2018;78(5):872–881.e6.
   PubMed Web of Science ®Google Scholar
• Antoniu SA. Pitrakinra, a dual IL-4/IL-13 antagonist for the potential treatment of asthma and eczema. Curr Opin Invest Drugs. 2010;11(11):1286–1294.
   PubMedGoogle Scholar
• May RD, Monk PD, Cohen ES, et al. Preclinical development of CAT-354, an IL-13 neutralizing antibody, for the treatment of severe uncontrolled asthma. Br J Pharmacol. 2012;166(1):177– 193.
   PubMed Web of Science ®Google Scholar
• Tollenaere MAX, Litman T, Moebus L, et al. Skin barrier and inflammation genes associated with atopic dermatitis are regulated by interleukin-13 and modulated by tralokinumab in vitro. Acta Derm Venereol. 2021;101(4):adv00447.
   PubMedGoogle Scholar
• Wollenberg A, Howell MD, Guttman-Yassky E, et al. Treatment of atopic dermatitis with tralokinumab, an anti-IL-13 mAb. J Allergy Clin Immunol. 2019;143(1):135–141.
   PubMed Web of Science ®Google Scholar
• Silverberg JI, Guttman-Yassky E, Gooderham M, et al. Health-related quality of life with tralokinumab in moderate-to-severe atopic dermatitis: a phase 2b randomized study. Ann Allergy Asthma Immunol. 2021;126(5):576–583.e4.
   PubMed Web of Science ®Google Scholar
• Wollenberg A, Blauvelt A, Guttman-Yassky E, et al. Tralokinumab for moderate-to-severe atopic dermatitis: results from two 52-week, randomized, double-blind, multicentre, placebo-controlled phase III trials (ECZTRA 1 and ECZTRA 2). Br J Dermatol. 184(3): 437–449. 2021.
   PubMed Web of Science ®Google Scholar
• Silverberg JI, Toth D, Bieber T, et al. Tralokinumab plus topical corticosteroids for the treatment of moderate-to-severe atopic dermatitis: results from the double-blind, randomized, multicentre, placebo-controlled phase III ECZTRA 3 trial. Br J Dermatol. 184(3): 450–463. 2021.
   PubMed Web of Science ®Google Scholar
• Alexis AF, Zirwas M, Pinter A, et al. Progressive and sustained improvements in the extent and severity of atopic dermatitis with tralokinumab in combination with topical corticosteroids as needed in moderate-to-severe atopic dermatitis. Abstract 384. 10 December 2020 Virtual Conference - RAD 2020 - International Symposium on Atopic Dermatitis.
   Google Scholar
• Simpson EL, Flohr C, Eichenfield LF, et al. Efficacy and safety of lebrikizumab (an anti-IL-13 monoclonal antibody) in adults with moderate-to-severe atopic dermatitis inadequately controlled by topical corticosteroids: a randomized, placebo-controlled phase II trial (TREBLE). J Am Acad Dermatol. 2018;78(5):863–871.e11.
   PubMed Web of Science ®Google Scholar
• Guttman-Yassky E, Blauvelt A, Eichenfield LF, et al. Efficacy and safety of lebrikizumab, a high-affinity interleukin 13 inhibitor, in adults with moderate to severe atopic dermatitis: a phase 2b randomized clinical trial. JAMA Dermatol. 156(4): 411–420. 2020.
   PubMed Web of Science ®Google Scholar
• Bieber T. Atopic dermatitis: an expanding therapeutic pipeline for a complex disease. Nat Rev Drug Discov. 2021;21:1–20.
   Web of Science ®Google Scholar
• Bieber T, Simpson EL, Silverberg JI, et al. Abrocitinib versus placebo or dupilumab for atopic dermatitis. N Engl J Med. 2021;384(12):1101–1112.
   PubMed Web of Science ®Google Scholar
• Blauvelt A, Teixeira HD, Simpson EL, et al. Efficacy and safety of upadacitinib vs dupilumab in adults with moderate-to-severe atopic dermatitis: a randomized clinical trial. JAMA Dermatol. 2021;157(9):1047–1055.
   PubMed Web of Science ®Google Scholar
• Guttman-Yassky E, Thaçi D, Pangan AL, et al. Upadacitinib in adults with moderate to severe atopic dermatitis: 16-week results from a randomized, placebo-controlled trial. J Allergy Clin Immunol. 2020;145(3):877–884.
   PubMed Web of Science ®Google Scholar
• Simpson EL, Sinclair R, Forman S, et al. Efficacy and safety of abrocitinib in adults and adolescents with moderate-to-severe atopic dermatitis (JADE MONO-1): a multicentre, double-blind, randomised, placebo-controlled, phase 3 trial. Lancet. 2020;396(10246):255–266.
   PubMed Web of Science ®Google Scholar
• https://clinicaltrials.gov/ct2/show/NCT04090229
   Google Scholar
• Akinlade B, Guttman-Yassky E, de Bruin-weller M, et al. Conjunctivitis in dupilumab clinical trials. Br J Dermatol. 2019;181(3):459–473.
   PubMed Web of Science ®Google Scholar
• Castro M, Corren J, Pavord ID, et al. Dupilumab efficacy and safety in moderate-to-severe uncontrolled asthma. N Engl J Med. 2018;378(26):2486–2496.
   PubMed Web of Science ®Google Scholar
• Bachert C, Han JK, Desrosiers M, et al. Efficacy and safety of dupilumab in patients with severe chronic rhinosinusitis with nasal polyps (LIBERTY NP SINUS-24 and LIBERTY NP SINUS-52): results from two multicentre, randomised, double-blind, placebo-controlled, parallel-group phase 3 trials. Lancet. 2019;394(10209):1638–1650. Erratum in: Lancet. 2019;394(10209):1618.
   PubMed Web of Science ®Google Scholar
• Apter AJ. The tralokinumab story: nothing is ever simple. J Allergy Clin Immunol. 2019;143(4):1336–1338.
   PubMed Web of Science ®Google Scholar
• Panettieri RA Jr, Sjobring U, Peterffy AM, et al. Tralokinumab for severe, uncontrolled asthma (STRATOS 1 and STRATOS 2): two randomised, double-blind, placebo-controlled, phase 3 clinical trials. Lancet Respir Med. 2018;6(7):511–525.
   PubMed Web of Science ®Google Scholar
• Russell RJ, Chachi L, FitzGerald JM, et al. Effect of tralokinumab, an interleukin-13 neutralising monoclonal antibody, on eosinophilic airway inflammation in uncontrolled moderate-to-severe asthma (MESOS): a multicentre, double-blind, randomised, placebo-controlled phase 2 trial. Lancet Respir Med. 2018;6(7):499–510.
   PubMed Web of Science ®Google Scholar
• Brightling CE, Chanez P, Leigh R, et al. Efficacy and safety of tralokinumab in patients with severe uncontrolled asthma: a randomised, double-blind, placebo-controlled, phase 2b trial. Lancet Respir Med. 2015;3(9):692–701.
   PubMed Web of Science ®Google Scholar
• Hanania NA, Noonan M, Corren J, et al. Lebrikizumab in moderate-to-severe asthma: pooled data from two randomised placebo-controlled studies. Thorax. 2015;70(8):748–756.
   PubMed Web of Science ®Google Scholar
• Hanania NA, Korenblat P, Chapman KR, et al. Efficacy and safety of lebrikizumab in patients with uncontrolled asthma (LAVOLTA I and LAVOLTA II): replicate, phase 3, randomised, doubleblind, placebo- controlled trials. Lancet Respir Med. 2016;4(10):781–796.
   PubMed Web of Science ®Google Scholar
• Merola JF, Bagel J, Almgren P, et al. Tralokinumab does not impact vaccine-induced immune responses: results from a 30-week, randomized, placebo-controlled trial in adults with moderate-to-severe atopic dermatitis. J Am Acad Dermatol. 2021;85(1):71–78.
   PubMed Web of Science ®Google Scholar