Bruton’s tyrosine kinase inhibitors: a promising emerging treatment option for multiple sclerosis

References

• Reich DS, Lucchinetti CF, Calabresi PA. Multiple Sclerosis. N Engl J Med. 2018;378(2):169–180.
   PubMed Web of Science ®Google Scholar
• Jelcic I, Al Nimer F, Wang J, et al. Memory B cells activate brain-homing, autoreactive CD4(+) T cells in multiple sclerosis. Cell. 2018;175(1):85–100.
   PubMed Web of Science ®Google Scholar
• Neubauer H, Cumano A, Müller M, et al. Jak2 deficiency defines an essential developmental checkpoint in definitive hematopoiesis. Cell. 1998;93(3):397–409.
   PubMed Web of Science ®Google Scholar
• Ghoreschi K, Jesson MI, Li X, et al. Modulation of innate and adaptive immune responses by tofacitinib (CP-690,550). J Immunol. 2011;186(7):4234–4243.
   PubMed Web of Science ®Google Scholar
• Ferguson F, Gray N. Kinase inhibitors: the road ahead. Nat Rev Drug Discov. 2018;17:353–377.
   PubMed Web of Science ®Google Scholar
• Davis MI, Hunt JP, Herrgard S, et al. Comprehensive analysis of kinase inhibitor selectivity. Nat Biotechnol. 2011;29(11):1046–1051.
   PubMed Web of Science ®Google Scholar
• Byrd JC, Furman RR, Coutre SE, et al. Targeting BTK with ibrutinib in relapsed chronic lymphocytic leukemia [published correction appears in N Engl J Med. 2014 Feb 20;370(8):786]. N Engl J Med. 2013;369(1):32–42.
   PubMed Web of Science ®Google Scholar
• Liu X, Zhang J, Han W, et al. Inhibition of BTK protects lungs from trauma-hemorrhagic shock-induced injury in rats [published correction appears in Mol Med Rep. 2018 May;17(5):6926]. Mol Med Rep. 2017;16(1):192–200.
   PubMed Web of Science ®Google Scholar
• Kil LP, de Bruijn MJ, van Nimwegen M, et al. Btk levels set the threshold for B-cell activation and negative selection of autoreactive B cells in mice. Blood. 2012;119:3744–3756.
   PubMed Web of Science ®Google Scholar
• Liang C, Tian D, Ren X, et al. The development of Bruton’s tyrosine kinase (BTK) inhibitors from 2012-2017: A mini-review. Eur J Med Chem. 2018;151:315–326.
   PubMed Web of Science ®Google Scholar
• Jongstra-Bilen J, Puig Cano A, Hasija M, et al. Dual functions of Bruton’s tyrosine kinase and Tec kinase during Fcgamma receptor-induced signaling and phagocytosis. J Immunol. 2008;181(1):288–298.
   PubMed Web of Science ®Google Scholar
• Hata D, Kawakami Y, Inagaki N, et al. Involvement of Bruton’s tyrosine kinase in FcepsilonRI-dependent mast cell degranulation and cytokine production. J Exp Med. 1998;187(8):1235–1247.
   PubMed Web of Science ®Google Scholar
• Roskoski R Jr. Properties of FDA-approved small molecule protein kinase inhibitors: A 2020 update. Pharmacol Res. 2020;152:104609.
   PubMed Web of Science ®Google Scholar
• Feng Y, Duan W, Cu X, et al. Bruton’s tyrosine kinase (BTK) inhibitors in treating cancer: a patent review (2010-2018). Expert Opin Ther Pat. 2019;29(4):217–241.
   PubMed Web of Science ®Google Scholar
• Matsushita T, Yanaba K, Bouaziz JD, et al. Regulatory B cells inhibit EAE initiation in mice while other B cells promote disease progression. J Clin Invest. 2008;118(10):3420–3430.
   PubMed Web of Science ®Google Scholar
• Weber MS, Prod’homme T, Patarroyo JC, et al. B-cell activation influences T-cell polarization and outcome of anti-CD20 B-cell depletion in central nervous system autoimmunity. Ann Neurol. 2010;68(3):369–383. .
   PubMed Web of Science ®Google Scholar
• Lehmann-Horn K, Schleich E, Hertzenberg D, et al. Anti-CD20 B-cell depletion enhances monocyte reactivity in neuroimmunological disorders. J Neuroinflammation. 2011;8:146.
   PubMed Web of Science ®Google Scholar
• Monson NL, Cravens P, Hussain R, et al. Rituximab therapy reduces organ-specific T cell responses and ameliorates experimental autoimmune encephalomyelitis. PLoS One. 2011;6(2):e17103.
   PubMed Web of Science ®Google Scholar
• Anthony DC, Dickens AM, Seneca N, et al. Anti-CD20 inhibits T cell-mediated pathology and microgliosis in the rat brain. Ann Clin Transl Neurol. 2014;1(9):659–669.
   PubMed Web of Science ®Google Scholar
• Sefia E, Pryce G, Meier UC, et al. Depletion of CD20 B cells fails to inhibit relapsing mouse experimental autoimmune encephalomyelitis. Mult Scler Relat Disord. 2017;14:46–50.
   PubMed Web of Science ®Google Scholar
• Crespo O, Kang SC, Daneman R, et al. Tyrosine kinase inhibitors ameliorate autoimmune encephalomyelitis in a mouse model of multiple sclerosis. J Clin Immunol. 2011;31(6):1010–1020.
   PubMed Web of Science ®Google Scholar
• Menzfeld C, John M, van Rossum D, et al. Tyrphostin AG126 exerts neuroprotection in CNS inflammation by a dual mechanism. Glia. 2015;63(6):1083–1099.
   PubMed Web of Science ®Google Scholar
• Torke S, Pretzsch R, Häusler D, et al. Inhibition of Bruton’s tyrosine kinase interferes with pathogenic B-cell development in inflammatory CNS demyelinating disease [published online ahead of print, 2020 Aug 6]. Acta Neuropathol. 2020. DOI:10.1007/s00401-020-02204-z.
   PubMed Web of Science ®Google Scholar
• Smith PF, Owens TD, Langrish CL, et al. Phase 1 clinical trial of PRN2246 (SAR441268), a covalent BTK inhibitor demonstrates safety, CNS exposure and therapeutic levels of BTK occupancy. Mult Scler J. 2019;25(Suppl1):52.
   Google Scholar
• Montalban X, Arnold DL, Weber MS, et al. Placebo-controlled trial of an oral BTK inhibitor in multiple sclerosis. N Engl J Med. 2019;380(25): 2406–2417. .
   PubMed Web of Science ®Google Scholar
• Reich DS, Honeycutt WD, Laganke C, et al. Efficacy and safety outcomes in patients with relapsing forms of MS treated with the CNS-Penetrating BTK inhibitor SAR442168: results from the phase 2b trial. Eur J Neurol. 2020;27(Suppl. 1):1–102. O4010.
   Google Scholar
• Gruber RC, Chretien N, Dufault MR, et al. Central effects of BTK inhibition in neuroinflammation. Neurology. 2020 Apr;94(15 Supplement):808.
   Web of Science ®Google Scholar
• Scaramozza M, Arefayene X, Peng M, et al. A Phase 1 study of BIIB091, a Bruton’s tyrosine kinase (BTK) inhibitor, in healthy adult participants: preliminary results (ID 390). ECTRIMS/ACTRIMS: P0186.
   Google Scholar
• Colado A, Genoula M, Cougoule C, et al. Effect of the BTK inhibitor ibrutinib on macrophage- and γδ T cell-mediated response against Mycobacterium tuberculosis. Blood Cancer J. 2018;8(11):100.
   PubMedGoogle Scholar
• Liu X, Pichulik T, Wolz OO, et al. Human NACHT, LRR, and PYD domain-containing protein 3 (NLRP3) inflammasome activity is regulated by and potentially targetable through Bruton tyrosine kinase. J Allergy Clin Immunol. 2017;140(4):1054–1067.e10.
   PubMed Web of Science ®Google Scholar
• Köprülü AD, Kastner R, Wienerroither S, et al. The tyrosine kinase Btk regulates the macrophage response to Listeria monocytogenes infection. PLoS One. 2013;8(3):e60476.
   PubMed Web of Science ®Google Scholar
• de Porto AP, Liu Z, de Beer R, et al. Btk inhibitor ibrutinib reduces inflammatory myeloid cell responses in the lung during murine pneumococcal pneumonia. Mol Med. 2019;25(1):3.
   PubMedGoogle Scholar
• Douglas AP, Trubiano JA, Barr I, et al. Ibrutinib may impair serological responses to influenza vaccination. Haematologica. 2017;102(10):e397–e399.
   PubMed Web of Science ®Google Scholar
• Sun C, Gao J, Couzens L, et al. Seasonal influenza vaccination in patients with chronic lymphocytic leukemia treated with ibrutinib. JAMA Oncol. 2016;2(12):1656–1657.
   PubMed Web of Science ®Google Scholar
• Katayama R, Aoyama A, Yamori T, et al. Cytotoxic activity of tivantinib (ARQ 197) is not due solely to c-MET inhibition. Cancer Res. 2013;73(10):3087–3096.
   PubMed Web of Science ®Google Scholar
• Munshi N, Jeay S, Li Y, et al. ARQ 197, a novel and selective inhibitor of the human c-Met receptor tyrosine kinase with antitumor activity. Mol Cancer Ther. 2010;9(6):1544–1553.
   PubMed Web of Science ®Google Scholar