106
Views
1
CrossRef citations to date
0
Altmetric
Review

Bruton’s tyrosine kinase in chronic inflammation: from pathophysiology to therapy

, &
Pages 27-34 | Published online: 18 Sep 2015

References

  • Schmidt U, Boucheron N, Unger B, Ellmeier W. The role of Tec family kinases in myeloid cells. Int Arch Allergy Immunol. 2004;134(1):65–78.
  • Smith CI, Islam TC, Mattsson PT, Mohamed AJ, Nore BF, Vihinen M. The Tec family of cytoplasmic tyrosine kinases: mammalian Btk, Bmx, Itk, Tec, Txk and homologs in other species. Bioessays. 2001;23(5):436–446.
  • Takesono A, Finkelstein LD, Schwartzberg PL. Beyond calcium: new signaling pathways for Tec family kinases. J Cell Sci. 2002;115(Pt 15):3039–3048.
  • Mohamed AJ, Vargas L, Nore BF, Backesjo CM, Christensson B, Smith CI. Nucleocytoplasmic shuttling of Bruton’s tyrosine kinase. J Biol Chem. 2000;275(51):40614–40619.
  • Brunner C, Avots A, Kreth HW, Serfling E, Schuster V. Bruton’s tyrosine kinase is activated upon CD40 stimulation in human B lymphocytes. Immunobiology. 2002;206(4):432–440.
  • Jefferies CA, Doyle S, Brunner C, et al. Bruton’s tyrosine kinase is a Toll/interleukin-1 receptor domain-binding protein that participates in nuclear factor kappaB activation by Toll-like receptor 4. J Biol Chem. 2003;278(28):26258–26264.
  • Wang J, Lau KY, Jung J, Ravindran P, Barrat FJ. Bruton’s tyrosine kinase regulates TLR9 but not TLR7 signaling in human plasmacytoid dendritic cells. Eur J Immunol. 2014;44(4):1130–1136.
  • Jefferies CA, O’Neill LA. Bruton’s tyrosine kinase (Btk)-the critical tyrosine kinase in LPS signalling? Immunol Lett. 2004;92(1–2):15–22.
  • Herbst S, Shah A, Mazon MM, et al. Phagocytosis-dependent activation of a TLR9-BTK-calcineurin-NFAT pathway co-ordinates innate immunity to Aspergillus fumigatus. EMBO Mol Med. 2015;7(3):240–258.
  • Liljeroos M, Vuolteenaho R, Morath S, Hartung T, Hallman M, Ojaniemi M. Bruton’s tyrosine kinase together with PI 3-kinase are part of Toll-like receptor 2 multiprotein complex and mediate LTA induced Toll-like receptor 2 responses in macrophages. Cell Signal. 2007;19(3):625–633.
  • Lee KG, Xu S, Kang ZH, et al. Bruton’s tyrosine kinase phosphorylates Toll-like receptor 3 to initiate antiviral response. Proc Natl Acad Sci U S A. 2012;109(15):5791–5796.
  • Li YF, Lee KG, Ou X, Lam KP. Bruton’s tyrosine kinase and protein kinase C micro are required for TLR7/9-induced IKKalpha and IRF-1 activation and interferon-beta production in conventional dendritic cells. PLoS One. 2014;9(8):e105420.
  • Lougaris V, Baronio M, Vitali M, et al. Bruton tyrosine kinase mediates TLR9-dependent human dendritic cell activation. J Allergy Clin Immunol. 2014;133(6):1644–1650.
  • Kubo T, Uchida Y, Watanabe Y, et al. Augmented TLR9-induced Btk activation in PIR-B-deficient B-1 cells provokes excessive autoantibody production and autoimmunity. J Exp Med. 2009;206(9):1971–1982.
  • Kenny EF, Quinn SR, Doyle SL, Vink PM, van EH, O’Neill LA. Bruton’s tyrosine kinase mediates the synergistic signalling between TLR9 and the B cell receptor by regulating calcium and calmodulin. PLoS One. 2013;8(8):e74103.
  • Di Paolo JA, Huang T, Balazs M, et al. Specific Btk inhibition suppresses B cell- and myeloid cell-mediated arthritis. Nat Chem Biol. 2011;7(1):41–50.
  • Ellmeier W, Abramova A, Schebesta A. Tec family kinases: regulation of FcepsilonRI-mediated mast-cell activation. FEBS J. 2011;278(12):1990–2000.
  • 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.
  • Ni Gabhann J, Spence S, Wynne C, et al. Defects in acute responses to TLR4 in Btk-deficient mice result in impaired dendritic cell-induced IFN-gamma production by natural killer cells. Clin Immunol. 2012;142(3):373–382.
  • Horwood NJ, Urbaniak AM, Danks L. Tec family kinases in inflammation and disease. Int Rev Immunol. 2012;31(2):87–103.
  • Hartkamp LM, Fine JS, van Es IE, et al. Btk inhibition suppresses agonist-induced human macrophage activation and inflammatory gene expression in RA synovial tissue explants. Ann Rheum Dis. Epub April 24, 2014.
  • Horwood NJ, Mahon T, McDaid JP, et al. Bruton’s tyrosine kinase is required for lipopolysaccharide-induced tumor necrosis factor alpha production. J Exp Med. 2003;197(12):1603–1611.
  • Horwood NJ, Page TH, McDaid JP, et al. Bruton’s tyrosine kinase is required for TLR2 and TLR4-induced TNF, but not IL-6, production. J Immunol. 2006;176(6):3635–3641.
  • Hsu J, Gu Y, Tan SL, Narula S, DeMartino JA, Liao C. Bruton’s Tyrosine Kinase mediates platelet receptor-induced generation of microparticles: a potential mechanism for amplification of inflammatory responses in rheumatoid arthritis synovial joints. Immunol Lett. 2013;150(1–2):97–104.
  • Xu D, Kim Y, Postelnek J, et al. RN486, a selective Bruton’s tyrosine kinase inhibitor, abrogates immune hypersensitivity responses and arthritis in rodents. J Pharmacol Exp Ther. 2012;341(1):90–103.
  • Mangla A, Khare A, Vineeth V, et al. Pleiotropic consequences of Bruton tyrosine kinase deficiency in myeloid lineages lead to poor inflammatory responses. Blood. 2004;104(4):1191–1197.
  • Mohamed AJ, Yu L, Backesjo CM, et al. Bruton’s tyrosine kinase (Btk): function, regulation, and transformation with special emphasis on the PH domain. Immunol Rev. 2009;228(1):58–73.
  • Melcher M, Unger B, Schmidt U, Rajantie IA, Alitalo K, Ellmeier W. Essential roles for the Tec family kinases Tec and Btk in M-CSF receptor signaling pathways that regulate macrophage survival. J Immunol. 2008;180(12):8048–8056.
  • Quek LS, Bolen J, Watson SP. A role for Bruton’s tyrosine kinase (Btk) in platelet activation by collagen. Curr Biol. 1998;8(20):1137–1140.
  • Atkinson BT, Ellmeier W, Watson SP. Tec regulates platelet activation by GPVI in the absence of Btk. Blood. 2003;102(10):3592–3599.
  • Shinohara M, Koga T, Okamoto K, et al. Tyrosine kinases Btk and Tec regulate osteoclast differentiation by linking RANK and ITAM signals. Cell. 2008;132(5):794–806.
  • Setoguchi R, Kinashi T, Sagara H, Hirosawa K, Takatsu K. Defective degranulation and calcium mobilization of bone-marrow derived mast cells from Xid and Btk-deficient mice. Immunol Lett. 1998;64(2–3):109–118.
  • Buckley CD, Filer A, Haworth O, Parsonage G, Salmon M. Defining a role for fibroblasts in the persistence of chronic inflammatory joint disease. Ann Rheum Dis. 2004;63(Suppl 2):ii92–ii95.
  • van de Sande MG, de Hair MJ, van der Leij C, et al. Different stages of rheumatoid arthritis: features of the synovium in the preclinical phase. Ann Rheum Dis. 2011;70(3):772–777.
  • McInnes IB, Schett G. The pathogenesis of rheumatoid arthritis. N Engl J Med. 2011;365(23):2205–2219.
  • Jansson L, Holmdahl R. Genes on the X chromosome affect development of collagen-induced arthritis in mice. Clin Exp Immunol. 1993; 94(3):459–465.
  • Vargas L, Hamasy A, Nore BF, Smith CI. Inhibitors of BTK and ITK: state of the new drugs for cancer, autoimmunity and inflammatory diseases. Scand J Immunol. 2013;78(2):130–139.
  • Burger JA. Bruton’s tyrosine kinase (BTK) inhibitors in clinical trials. Curr Hematol Malig Rep. 2014;9(1):44–49.
  • Uckun FM. Clinical potential of targeting Bruton’s tyrosine kinase. Int Rev Immunol. 2008;27(1–2):43–69.
  • Lou Y, Owens TD, Kuglstatter A, Kondru RK, Goldstein DM. Bruton’s tyrosine kinase inhibitors: approaches to potent and selective inhibition, preclinical and clinical evaluation for inflammatory diseases and B cell malignancies. J Med Chem. 2012;55:4539–4550.
  • Hutchinson CV, Dyer MJ. Breaking good: the inexorable rise of BTK inhibitors in the treatment of chronic lymphocytic leukaemia. Br J Haematol. 2014;166(1):12–22.
  • Spaargaren M, de Rooij MF, Kater AP, Eldering E. BTK inhibitors in chronic lymphocytic leukemia: a glimpse to the future. Oncogene. 2015;34(19):2426–2436.
  • Honigberg LA, Smith AM, Sirisawad M, et al. The Bruton tyrosine kinase inhibitor PCI-32765 blocks B-cell activation and is efficacious in models of autoimmune disease and B-cell malignancy. Proc Natl Acad Sci U S A. 2010;107(29):13075–13080.
  • Chang BY, Huang MM, Francesco M, et al. The Bruton tyrosine kinase inhibitor PCI-32765 ameliorates autoimmune arthritis by inhibition of multiple effector cells. Arthritis Res Ther. 2011;13(4):R115.
  • Shinohara M, Chang BY, Buggy JJ, et al. The orally available Btk inhibitor ibrutinib (PCI-32765) protects against osteoclast-mediated bone loss. Bone. 2014;60:8–15.
  • Yoshizawa T, Ariza Y, Ueda Y, Hotta S, Narita M, Kawabata K. Development of a Bruton’s tyrosine kinase (Btk) inhibitor, ONO-4059: efficacy in a collagen induced arthritis (CIA) model indicates potential treatment for rheumatoid arthritis (RA). Arthritis Rheum. 2012;64:S709.
  • Akinleye A, Chen Y, Mukhi N, Song Y, Liu D. Ibrutinib and novel BTK inhibitors in clinical development. J Hematol Oncol. 2013;6:59.
  • Evans EK, Tester R, Aslanian S, et al. Inhibition of Btk with CC-292 provides early pharmacodynamic assessment of activity in mice and humans. J Pharmacol Exp Ther. 2013;346(2):219–228.
  • Whang JA, Chang BY. Bruton’s tyrosine kinase inhibitors for the treatment of rheumatoid arthritis. Drug Discov Today. 2014;19(8):1200–1204.
  • Liu L, Di Paulo J, Barbosa J, Rong H, Reif K, Wong H. Antiarthritis effect of a novel Bruton’s tyrosine kinase (BTK) inhibitor in rat collagen-induced arthritis and mechanism-based pharmacokinetic/pharmacodynamic modeling: relationships between inhibition of BTK phosphorylation and efficacy. J Pharmacol Exp Ther. 2011;338(1):154–163.
  • Liu L, Halladay JS, Shin Y, et al. Significant species difference in amide hydrolysis of GDC-0834, a novel potent and selective Bruton’s tyrosine kinase inhibitor. Drug Metab Dispos. 2011;39(10):1840–1849.
  • Yoon YK, Hadi S, Iersel TV, et al. Safety, pharmacokinetics, pharmacodynamics and food effect of an oral Bruton’s tyrosine kinase inhibitor HM71224 in healthy subjects. Ann Rheum Dis. 2014;73(Suppl 2):231.
  • Park JK, Park JA, Lee YJ, et al. HM71224, a novel oral Btk inhibitor, inhibits human immune cell activation: new drug candidate to treat B-cell associated autoimmune diseases. Ann Rheum Dis. 2014;73(Suppl 2):355–356. doi: 10.1136/annrheumdis-2014-eular.2783.
  • Mok CC, Lau CS. Pathogenesis of systemic lupus erythematosus. J Clin Pathol. 2003;56(7):481–490.
  • Pathak S, Mohan C. Cellular and molecular pathogenesis of systemic lupus erythematosus: lessons from animal models. Arthritis Res Ther. 2011(5);13:241.
  • Halcomb KE, Musuka S, Gutierrez T, Wright HL, Satterthwaite AB. Btk regulates localization, in vivo activation, and class switching of anti-DNA B cells. Mol Immunol. 2008;46(2):233–241.
  • Whyburn LR, Halcomb KE, Contreras CM, Lowell CA, Witte ON, Satterthwaite AB. Reduced dosage of Bruton’s tyrosine kinase uncouples B cell hyperresponsiveness from autoimmunity in lyn-/- mice. J Immunol. 2003;171(4):1850–1858.
  • Mina-Osorio P, LaStant J, Keirstead N, et al. Suppression of glomerulonephritis in lupus-prone NZB x NZW mice by RN486, a selective inhibitor of Bruton’s tyrosine kinase. Arthritis Rheum. 2013;65(9):2380–2391.
  • Rankin AL, Seth N, Keegan S, et al. Selective inhibition of BTK prevents murine lupus and antibody-mediated glomerulonephritis. J Immunol. 2013;191(9):4540–4550.
  • Hutcheson J, Vanarsa K, Bashmakov A, et al. Modulating proximal cell signaling by targeting Btk ameliorates humoral autoimmunity and end-organ disease in murine lupus. Arthritis Res Ther. 2012;14(6):R243.
  • Ciccarelli O, Barkhof F, Bodini B, et al. Pathogenesis of multiple sclerosis: insights from molecular and metabolic imaging. Lancet Neurol. 2014;13(8):807–822.
  • Nylander A, Hafler DA. Multiple sclerosis. J Clin Invest. 2012;122(4):1180–1188.
  • Lassmann H. Multiple sclerosis: lessons from molecular neuropathology. Exp Neurol. 2014;262 Pt A:2–7.
  • Kruglov AA, Lampropoulou V, Fillatreau S, Nedospasov SA. Pathogenic and protective functions of TNF in neuroinflammation are defined by its expression in T lymphocytes and myeloid cells. J Immunol. 2011; 187(11):5660–5670.
  • Dendrou CA, Bell JI, Fugger L. A clinical conundrum: the detrimental effect of TNF antagonists in multiple sclerosis. Pharmacogenomics. 2013;14(12):1397–1404.
  • Trinchieri G. Type I interferon: friend or foe? J Exp Med. 2010;207(10):2053–2063.
  • Verweij CL, Vosslamber S. Relevance of the type I interferon signature in multiple sclerosis towards a personalized medicine approach for interferon-beta therapy. Discov Med. 2013;15(80):51–60.
  • Atkinson MA. The pathogenesis and natural history of type 1 diabetes. Cold Spring Harb Perspect Med. 2012;2(11):pii:a007641.
  • Gillespie KM. Type 1 diabetes: pathogenesis and prevention. CMAJ. 2006;175(2):165–170.
  • Li M, Song LJ, Qin XY. Advances in the cellular immunological pathogenesis of type 1 diabetes. J Cell Mol Med. 2014;18(5):749–758.
  • Luo X, Herold KC, Miller SD. Immunotherapy of type 1 diabetes: where are we and where should we be going? Immunity. 2010;32(4):488–499.
  • Bonami RH, Sullivan AM, Case JB, et al. Bruton’s tyrosine kinase promotes persistence of mature anti-insulin B cells. J Immunol. 2014; 192(4):1459–1470.
  • Kendall PL, Moore DJ, Hulbert C, Hoek KL, Khan WN, Thomas JW. Reduced diabetes in btk-deficient nonobese diabetic mice and restoration of diabetes with provision of an anti-insulin IgH chain transgene. J Immunol. 2009;183(10):6403–6412.
  • Martin S, Wolf-Eichbaum D, Duinkerken G, et al. Development of type 1 diabetes despite severe hereditary B-lymphocyte deficiency. N Engl J Med. 2001;345(14):1036–1040.
  • van Bon L, Cossu M, Radstake TR. An update on an immune system that goes awry in systemic sclerosis. Curr Opin Rheumatol. 2011;23(6):505–510.
  • van Bon L, Affandi AJ, Broen J, et al. Proteome-wide analysis and CXCL4 as a biomarker in systemic sclerosis. N Engl J Med. 2014; 370(5):433–443.
  • Avouac J, Elhai M, Allanore Y. Experimental models of dermal fibrosis and systemic sclerosis. Joint Bone Spine. 2013;80(1):23–28.
  • Katsumoto TR, Whitfield ML, Connolly MK. The pathogenesis of systemic sclerosis. Annu Rev Pathol. 2011;6:509–537.
  • O’Reilly S, Hugle T, van Laar JM. T cells in systemic sclerosis: a reappraisal. Rheumatology (Oxford) 2012;51(9):1540–1549.
  • Cornec D, Devauchelle-Pensec V, Tobon GJ, Pers JO, Jousse-Joulin S, Saraux A. B cells in Sjogren’s syndrome: from pathophysiology to diagnosis and treatment. J Autoimmun. 2012;39(3):161–167.
  • Delaleu N, Nguyen CQ, Peck AB, Jonsson R. Sjogren’s syndrome: studying the disease in mice. Arthritis Res Ther. 2011;13(3):217.
  • Hillen MR, Ververs FA, Kruize AA, Van Roon JA. Dendritic cells, T-cells and epithelial cells: a crucial interplay in immunopathology of primary Sjogren’s syndrome. Expert Rev Clin Immunol. 2014;10(4):521–531.
  • Huang YF, Cheng Q, Jiang CM, et al. The immune factors involved in the pathogenesis, diagnosis, and treatment of Sjogren’s syndrome. Clin Dev Immunol. 2013;2013:160491.
  • Nocturne G, Mariette X. Advances in understanding the pathogenesis of primary Sjogren’s syndrome. Nat Rev Rheumatol. 2013;9(9):544–556.