Bruton's Kinase Inhibitors for the Treatment of Immunological Diseases: Current Status and Perspectives

Ewa Robak, Tadeusz Robak, Ewa Robak, Tadeusz Robak

Abstract

The use of Bruton's tyrosine kinase (BTK) inhibitors has changed the management of patients with B-cell lymphoid malignancies. BTK is an important molecule that interconnects B-cell antigen receptor (BCR) signaling. BTK inhibitors (BTKis) are classified into three categories, namely covalent irreversible inhibitors, covalent reversible inhibitors, and non-covalent reversible inhibitors. Ibrutinib is the first covalent, irreversible BTK inhibitor approved in 2013 as a breakthrough therapy for chronic lymphocytic leukemia patients. Subsequently, two other covalent, irreversible, second-generation BTKis, acalabrutinib and zanubrutinib, have been developed for lymphoid malignancies to reduce the ibrutinib-mediated adverse effects. More recently, irreversible and reversible BTKis have been under development for immune-mediated diseases, including autoimmune hemolytic anemia, immune thrombocytopenia, multiple sclerosis, pemphigus vulgaris, atopic dermatitis, rheumatoid arthritis, systemic lupus erythematosus, Sjögren's disease, and chronic spontaneous urticaria, among others. This review article summarizes the preclinical and clinical evidence supporting the role of BTKis in various autoimmune, allergic, and inflammatory conditions.

Keywords: AIHA; BTK inhibitor; ITP; IgG4-related disease; atopic dermatitis; chronic spontaneous urticaria; multiple sclerosis; pemphigus vulgaris; rheumatoid arthritis; systemic lupus erythematosus.

Conflict of interest statement

The authors declare no conflict of interest. Writing assistance was not utilized in the production of this manuscript.

References

    1. Bruton O.C. Agammaglobulinemia. Pediatrics. 1952;9:722–728. doi: 10.1542/peds.9.6.722.
    1. Conley M.E., Brown P., Pickard A.R., Buckley R.H., Miller D.S., Raskind W.H., Singer J.W., Fialkow P.J. Expression of the gene defect in X-linked agammaglobulinemia. N. Engl. J. Med. 1986;315:564–567. doi: 10.1056/NEJM198608283150907.
    1. Vetrie D., Vořechovský I., Sideras P., Holland J., Davies A., Flinter F., Hammarström L., Kinnon C., Levinsky R., Bobrow M., et al. The gene involved in X-linked agammaglobulinaemia is a member of the src family of protein-tyrosine kinases. Nature. 1993;361:226–233. doi: 10.1038/361226a0.
    1. Satterthwaite A.B., Witte O.N. The role of Bruton’s Tyrosine Kinase in B-cell development and function: A genetic perspective. Immunol. Rev. 2000;175:120–127. doi: 10.1111/j.1600-065X.2000.imr017504.x.
    1. Brullo C., Villa C., Tasso B., Russo E., Spallarossa A. Btk inhibitors: A medicinal chemistry and drug delivery perspective. Int. J. Mol. Sci. 2021;22:7641. doi: 10.3390/ijms22147641.
    1. Robak T., Witkowska M., Smolewski P. The role of Bruton’s kinase inhibitors in chronic lymphocytic leukemia: Current status and future directions. Cancers. 2022;14:771. doi: 10.3390/cancers14030771.
    1. Corneth O.B.J., Wolterink R.G.J.K., Hendriks R.W. BTK signaling in B cell differentiation and autoimmunity. B Cell Recept. Signal. 2016;393:67–105.
    1. Zarrin A.A., Bao K., Lupardus P., Vucic D. Kinase inhibition in autoimmunity and inflammation. Nat. Rev. Drug Discov. 2021;20:39–63. doi: 10.1038/s41573-020-0082-8.
    1. Ringheim G.E., Wampole M., Oberoi K. Bruton’s Tyrosine Kinase (BTK) inhibitors and autoimmune diseases: Making sense of BTK inhibitor specificity profiles and recent clinical trial successes and failures. Front. Immunol. 2021;12:662223. doi: 10.3389/fimmu.2021.662223.
    1. McDonald C., Xanthopoulos C., Kostareli E. The role of Bruton’s Tyrosine Kinase in the immune system and disease. Immunology. 2021;164:722–736. doi: 10.1111/imm.13416.
    1. Liubchenko G., Appleberry H.C., Striebich C.C., Franklin K.E., Derber L.A., Holers V.M., Lyubchenko T. Rheumatoid arthritis is associated with signaling alterations in naturally occurring autoreactive B-lymphocytes. J. Autoimmun. 2013;40:111–121. doi: 10.1016/j.jaut.2012.09.001.
    1. Iwata S., Tanaka Y. B-cell subsets, signaling and their roles in secretion of autoantibodies. Lupus. 2016;25:850–856. doi: 10.1177/0961203316643172.
    1. Zain R., Vihinen M. Structure-function relationships of covalent and non-covalent BTK inhibitors. Front. Immunol. 2021;12:2675. doi: 10.3389/fimmu.2021.694853.
    1. Robak P., Robak T. Novel synthetic drugs currently in clinical development for chronic lymphocytic leukemia. Expert Opin. Investig. Drugs. 2017;26:1249–1265. doi: 10.1080/13543784.2017.1384814.
    1. Honigberg L.A., Smith A.M., Sirisawad M., Verner E., Loury D., Chang B., Li S., Pan Z., Thamm D.H., Miller M.A., 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. USA. 2010;107:13075–13080. doi: 10.1073/pnas.1004594107.
    1. de Bruin G., Demont D., de Zwart E., Verkaik S., Hoogenboom N., van de Kar B., van Lith B., Emmelot-van Hoek M., Gulrajani M., Demont D., et al. Potency and selectivity of BTK inhibitors in clinical development for B-cell malignancies. Blood. 2018;132:1871.
    1. Wolska-Washer A., Robak T. Acalabrutinib: A Bruton tyrosine kinase inhibitor for the treatment of chronic lymphocytic leukemia. Expert Rev. Hematol. 2022;15:183–194. doi: 10.1080/17474086.2022.2054800.
    1. Tasso B., Spallarossa A., Russo E., Brullo C. The development of BTK inhibitors: A five-year update. Molecules. 2021;26:7411. doi: 10.3390/molecules26237411.
    1. McMullen J.R., Boey E.J., Ooi J.Y., Seymour J.F., Keating M.J., Tam C.S. Ibrutinib increases the risk of atrial fibrillation, potentially through inhibition of cardiac PI3K-Akt signaling. Blood. 2014;124:3829–3830. doi: 10.1182/blood-2014-10-604272.
    1. Barf T., Covey T., Izumi R., Van De Kar B., Gulrajani M., Van Lith B., Van Hoek M., De Zwart E., Mittag D., Demont D., et al. Acalabrutinib (ACP-196): A covalent Bruton tyrosine kinase inhibitor with a differentiated selectivity and in vivo potency profile. J. Pharmacol. Exp. Ther. 2017;363:240–252. doi: 10.1124/jpet.117.242909.
    1. von Hundelshausen P., Siess W. Bleeding by Bruton Tyrosine Kinase-inhibitors: Dependency on drug type and disease. Cancers. 2021;13:1103. doi: 10.3390/cancers13051103.
    1. Lynch T.J., Kim E.S., Eaby B., Garey J., West D.P., Lacouture M.E. Epidermal growth factor receptor inhibitor-associated cutaneous toxicities: An evolving paradigm in clinical management. Oncologist. 2007;12:610–621. doi: 10.1634/theoncologist.12-5-610.
    1. Alsadhan A., Cheung J., Gulrajani M., Gaglione E.M., Nierman P., Hamdy A., Izumi R., Bibikova E., Patel P., Sun C., et al. Pharmacodynamic analysis of BTK inhibition in patients with chronic lymphocytic leukemia treated with acalabrutinib. Clin. Cancer Res. 2020;26:2800–2809. doi: 10.1158/1078-0432.CCR-19-3505.
    1. Byrd J.C., Hillmen P., Ghia P., Kater A.P., Chanan-Khan A., Furman R.R., O’Brien S., Yenerel M.N., Illés A., Kay N., et al. Acalabrutinib versus ibrutinib in previously treated chronic lymphocytic leukemia: Results of the first randomized phase III trial. J. Clin. Oncol. 2021;39:3441–3452. doi: 10.1200/JCO.21.01210.
    1. Guo Y., Liu Y., Hu N., Yu D., Zhou C., Shi G., Zhang B., Wei M., Liu J., Luo L., et al. Discovery of zanubrutinib (BGB-3111), a novel, potent, and selective covalent inhibitor of Bruton’s Tyrosine Kinase. J. Med. Chem. 2019;62:7923–7940. doi: 10.1021/acs.jmedchem.9b00687.
    1. Hillmen P., Eichhorst B., Brown J.R., Lamanna N., O’Brien S., Tam C.S., Qiu L., Kazmierczak M., Zhou K., Šimkovič M., et al. First interim analysis of alpine study: Results of a phase 3 randomized study of zanubrutinibvs ibrutinib in patients with relapsed/refractory chroniclymphocytic leukemia/small lymphocytic lymphoma; Proceedings of the 2021 European Hematology Association Virtual Congress; Online. 9–17 June 2021.
    1. Evans E.K., Tester R., Aslanian S., Karp R., Sheets M., Labenski M.T., Witowski S.R., Lounsbury H., Chaturvedi P., Mazdiyasni H., et al. Inhibition of BTK with CC-292 provides early pharmacodynamic assessment of activity in mice and humans. J. Pharmacol. Exp. Ther. 2013;346:219–228. doi: 10.1124/jpet.113.203489.
    1. Schafer P.H., Kivitz A.J., Ma J., Korish S., Sutherland D., Li L., Azaryan A., Kosek J., Adams M., Capone L., et al. Spebrutinib (CC-292) affects markers of B cell activation, chemotaxis, and osteoclasts in patients with rheumatoid arthritis: Results from a mechanistic study. Rheumatol. Ther. 2020;7:101–119. doi: 10.1007/s40744-019-00182-7.
    1. Haselmayer P., Camps M., Liu-Bujalski L., Nguyen N., Morandi F., Head J., O’Mahony A., Zimmerli S.C., Bruns L., Bender A.T., et al. Efficacy and pharmacodynamic modeling of the BTK inhibitor evobrutinib in autoimmune disease models. J. Immunol. 2019;202:2888–2906. doi: 10.4049/jimmunol.1800583.
    1. Montalban X., Gold R., Thompson A.J., Otero-Romero S., Amato M.P., Chandraratna D., Clanet M., Comi G., Derfuss T., Fazekas F., et al. ECTRIMS/EAN guideline on the pharmacological treatment of people with multiple sclerosis. Mult. Scler. J. 2018;24:96–120. doi: 10.1177/1352458517751049.
    1. Angst D., Gessier F., Janser P., Vulpetti A., Wälchli R., Beerli C., Littlewood-Evans A., Dawson J., Nuesslein-Hildesheim B., Wieczorek G., et al. Discovery of LOU064 (Remibrutinib), a potent and highly selective covalent inhibitor of Bruton’s Ty-rosine Kinase. J. Med. Chem. 2020;63:5102–5118. doi: 10.1021/acs.jmedchem.9b01916.
    1. Duan R., Goldmann L., Brandl R., Spannagl M., Weber C., Siess W., von Hundelshausen P. Effects of the BTK-Inhibitors remibrutinib (LOU064) and rilzabrutinib (PRN1008) with varying BTK selectivity over Tec on platelet aggregation and in vitro bleeding time. Front. Cardiovasc. Med. 2021;8:1195. doi: 10.3389/fcvm.2021.749022.
    1. Kaul M., End P., Cabanski M., Schuhler C., Jakab A., Kistowska M., Kinhikar A., Maiolica A., Sinn A., Fuhr R., et al. Remibrutinib (LOU064): A selective potent oral BTK inhibitor with promising clinical safety and pharmacodynamics in a randomized phase I trial. Clin. Transl. Sci. 2021;14:1756–1768. doi: 10.1111/cts.13005.
    1. Liclican A., Serafini L., Xing W., Czerwieniec G., Steiner B., Wang T., Brendza K.M., Lutz J.D., Keegan K.S., Ray A.S., et al. Bio-chemical characterization of tirabrutinib and other irreversible inhibitors of Bruton’s Tyrosine Kinase reveals differences in on- and off-target inhibition. Biochim. Biophys. Acta Gen. Subj. 2020;1864:129531. doi: 10.1016/j.bbagen.2020.129531.
    1. Munakata W., Tobinai K. Tirabrutinib hydrochloride for B-cell lymphomas. Drugs Today. 2021;57:277–289. doi: 10.1358/dot.2021.57.4.3264113.
    1. Ariza Y., Murata M., Ueda Y., Yoshizawa T. Bruton’s Tyrosine Kinase (BTK) inhibitor tirabrutinib suppresses osteoclastic bone resorption. Bone Rep. 2019;10:100201. doi: 10.1016/j.bonr.2019.100201.
    1. Dhillon S. Tirabrutinib: First approval. Drugs. 2020;80:835–840. doi: 10.1007/s40265-020-01318-8.
    1. Goess C., Harris C.M., Murdock S., McCarthy R.W., Sampson E., Twomey R., Mathieu S., Mario R., Perham M., Goedken E.R., et al. ABBV-105, a selective and irreversible inhibitor of Bruton’s Tyrosine Kinase, is efficacious in multiple preclinical models of inflammation. Mod. Rheumatol. 2019;29:510–522. doi: 10.1080/14397595.2018.1484269.
    1. Leproult E., Barluenga S., Moras D., Wurtz J.-M., Winssinger N. Cysteine mapping in conformationally distinct kinase nu-cleotide binding sites: Application to the design of selective covalent inhibitors. J. Med. Chem. 2011;54:1347–1355. doi: 10.1021/jm101396q.
    1. Owens T.D., Smith P.F., Redfern A., Xing Y., Shu J., Karr D.E., Hartmann S., Francesco M.R., Langrish C.L., Nunn P.A., et al. Phase 1 clinical trial evaluating safety, exposure and pharmacodynamics of BTK inhibitor tolebrutinib (PRN2246, SAR442168) Clin. Transl. Sci. 2022;15:442–450. doi: 10.1111/cts.13162.
    1. Zhang B., Zhao R., Liang R., Gao Y., Liu R., Chen X., Wang Z., Yu L., Shakib Z., Cui J. Orelabrutinib, a potent and selective Bruton’s Tyrosine Kinase inhibitor with superior safety profile and excellent PK/PD properties. Cancer Res. 2020;80:CT132.
    1. Watterson S.H., Liu Q., Beaudoin Bertrand M., Batt D.G., Li L., Pattoli M.A., Skala S., Cheng L., Obermeier M.T., Moore R., et al. Discovery of branebrutinib (BMS-986195): A strategy for identifying a highly potent and selective covalent inhibitor providing rapid in vivo inactivation of Bruton’s Tyrosine Kinase (BTK) J. Med. Chem. 2019;62:3228–3250. doi: 10.1021/acs.jmedchem.9b00167.
    1. Catlett I.M., Nowak M., Kundu S., Zheng N., Liu A., He B., Girgis I.G., Grasela D.M. Safety, pharmacokinetics and pharma-codynamics of branebrutinib (BMS-986195), a covalent, irreversible inhibitor of Bruton’s tyrosine kinase: Randomised phase I, placebo-controlled trial in healthy participants. Br. J. Clin. Pharmacol. 2020;86:1849–1859. doi: 10.1111/bcp.14290.
    1. Park J.K., Byun J.Y., Park J.A., Kim Y.Y., Lee Y.J., Oh J.I., Jang S.Y., Kim Y.H., Song Y.W., Son J., et al. HM71224, a novel Bruton’s Tyrosine Kinase inhibitor, suppresses B cell and monocyte activation and ameliorates arthritis in a mouse model: A potential drug for rheumatoid arthritis. Arthritis Res. Ther. 2016;18:91. doi: 10.1186/s13075-016-0988-z.
    1. Kim Y.Y., Park K.T., Jang S.Y., Lee K.H., Byun J.Y., Suh K.H., Lee Y.M., Kim Y.H., Hwang K.W. HM71224, a selective Bruton’s Tyrosine Kinase inhibitor, attenuates the development of murine lupus. Arthritis Res. Ther. 2017;19:211. doi: 10.1186/s13075-017-1402-1.
    1. Byun J.Y., Koh Y.T., Jang S.Y., Witcher J.W., Chan J.R., Pustilnik A., Daniels M.J., Kim Y.H., Suh K.H., Linnik M.D., et al. Target modulation and pharmacokinetics/pharmacodynamics translation of the BTK inhibitor poseltinib for model-informed phase II dose selection. Sci. Rep. 2021;11:18671. doi: 10.1038/s41598-021-98255-7.
    1. Normant E., Gorelik L., Shmeis R., Le H., Nisch R., Miskin H.P., Sportelli P., Weiss M.S. TG-1701 a novel, orally available, and covalently-bound BTK inhibitor. HemaSphere. 2018;2:215080.
    1. Ribeiro M.L., Reyes-Garau D., Vinyoles M., Pelejà N.P., Santos J.C., Armengol M., Fernández-Serrano M., Mor A.S., Bech-Serra J.J., Blecua P., et al. Antitumor activity of the novel BTK inhibitor TG-1701 is associated with disruption of Ikaros signaling in patients with B-cell non–Hodgkin lymphoma. Clin. Cancer Res. 2021;27:6591–6601. doi: 10.1158/1078-0432.CCR-21-1067.
    1. Hosoi F., Iguchi S., Yoshiga Y., Kaneko R., Nakachi Y., Akasaka D., Yonekura K., Iwasawa Y., Sasaki E., Utsugi T. TAS5315, a novel Bruton’s Tyrosine Kinase (BTK) inhibitor, demonstrates potent efficacy in mouse collagen-induced arthritis model. Ann. Rheumatol. Dis. 2015;74:OP0075. doi: 10.1136/annrheumdis-2015-eular.3864.
    1. Noma N., Hosoi F., Iguchi S., Kaneko R., Yoshiga Y., Arima Y., Tanaka K., Saito A., Utsugi T., Ikizawa K. SAT0056 TAS5315, a novel Bruton’s Tyrosine Kinase inhibitor, demonstrates potent efficacy against bone destruction in an animal model for rheumatoid arthritis. Ann. Rheumatol. Dis. 2019;78:1092.
    1. Pan Z., Scheerens H., Li S.-J., Schultz B.E., Sprengeler P.A., Burrill L.C., Mendonca R.V., Sweeney M.D., Scott K.C.K., Grothaus P.G., et al. Discovery of selective irreversible inhibitors for Bruton’s Tyrosine Kinase. ChemMedChem. 2007;2:58–61. doi: 10.1002/cmdc.200600221.
    1. Aguilar C. Ibrutinib-related bleeding: Pathogenesis, clinical implications and management. Blood Coagul. Fibrinolysis. 2018;29:481–487. doi: 10.1097/MBC.0000000000000749.
    1. Scheible H., Dyroff M., Seithel-Keuth A., Harrison-Moench E., Mammasse N., Port A., Bachmann A., Dong J., van Lier J.J., Tracewell W., et al. Evobrutinib, a covalent Bruton’s Tyrosine Kinase inhibitor: Mass balance, elimination route, and metabolism in healthy participants. Clin. Transl. Sci. 2021;14:2420–2430. doi: 10.1111/cts.13108.
    1. Zhang D., Gong H., Meng F. Recent advances in BTK inhibitors for the treatment of inflammatory and autoimmune diseases. Molecules. 2021;26:4907. doi: 10.3390/molecules26164907.
    1. Becker A., Martin E.C., Mitchell D.Y., Grenningloh R., Bender A.T., Laurent J., Mackenzie H., Johne A. Safety, tolerability, pharmacokinetics, target occupancy, and concentration—QT analysis of the novel BTK inhibitor evobrutinib in healthy volunteers. Clin. Transl. Sci. 2020;13:325–336. doi: 10.1111/cts.12713.
    1. Dhillon S. Orelabrutinib: First approval. Drugs. 2021;81:503–507. doi: 10.1007/s40265-021-01482-5.
    1. Lewis K.L., Cheah C.Y. Non-covalent BTK inhibitors-the new BTKids on the block for B-bell malignancies. J. Pers. Med. 2021;11:764. doi: 10.3390/jpm11080764.
    1. Ran F., Liu Y., Wang C., Xu Z., Zhang Y., Liu Y., Zhao G., Ling Y. Review of the development of BTK inhibitors in overcoming the clinical limitations of ibrutinib. Eur. J. Med. Chem. 2022;229:114009. doi: 10.1016/j.ejmech.2021.114009.
    1. Crawford J.J., Johnson A.R., Misner D.L., Belmont L.D., Castanedo G., Choy R., Coraggio M., Dong L., Eigenbrot C., Erickson R., et al. Discovery of GDC-0853: A potent, selective, and noncovalent Bruton’s Tyrosine Kinase inhibitor in early clinical development. J. Med. Chem. 2018;61:2227–2245. doi: 10.1021/acs.jmedchem.7b01712.
    1. Herman A.E., Chinn L.W., Kotwal S.G., Murray E.R., Zhao R., Florero M., Lin A., Moein A., Wang R., Bremer M., et al. Safety, pharmacokinetics, and pharmacodynamics in healthy volunteers treated with GDC-0853, a selective reversible Bruton’s Tyrosine Kinase inhibitor. Clin. Pharmacol. Ther. 2018;103:1020–1028. doi: 10.1002/cpt.1056.
    1. Cohen S., Tuckwell K., Katsumoto T.R., Zhao R., Galanter J., Lee C.K., Rae J., Toth B., Ramamoorthi N., Hackney J.A., et al. Fenebrutinib versus placebo or adalimumab in rheumatoid arthritis: A randomized, double-blind, phase II trial (ANDES study) Arthritis Rheumatol. 2020;72:1435–1446. doi: 10.1002/art.41275.
    1. Isenberg D., Furie R., Jones N.S., Guibord P., Galanter J., Lee C., McGregor A., Toth B., Rae J., Hwang O., et al. Efficacy, safety, and pharmacodynamic effects of the Bruton’s Tyrosine Kinase inhibitor fenebrutinib (GDC-0853) in systemic lupus erythematosus: Results of a phase II, randomized, double-blind, placebo-controlled trial. Arthritis Rheumatol. 2021;73:1835–1846. doi: 10.1002/art.41811.
    1. Neys S.F.H., Rip J., Hendriks R.W., Corneth O.B.J. Bruton’s Tyrosine Kinase inhibition as an emerging therapy in systemic autoimmune disease. Drugs. 2021;81:1605–1626. doi: 10.1007/s40265-021-01592-0.
    1. Metz M., Sussman G., Gagnon R., Staubach P., Tanus T., Yang W.H., Lim J.J., Clarke H.J., Galanter J., Chinn L.W., et al. Fenebrutinib in H1 antihistamine-refractory chronic spontaneous urticaria: A randomized phase 2 trial. Nat. Med. 2021;27:1961–1969. doi: 10.1038/s41591-021-01537-w.
    1. Langrish C.L., Bradshaw J.M., Francesco M.R., Owens T.D., Xing Y., Shu J., LaStant J., Bisconte A., Outerbridge C., White S.D., et al. Preclinical efficacy and anti-inflammatory mechanisms of action of the Bruton Tyrosine Kinase inhibitor Rilzabrutinib for immune-mediated disease. J. Immunol. 2021;206:1454–1468. doi: 10.4049/jimmunol.2001130.
    1. Smith P.F., Krishnarajah J., Nunn P.A., Hill R.J., Karr D., Tam D., Masjedizadeh M., Funk J.O., Gourlay S.G. A phase I trial of PRN1008, a novel reversible covalent inhibitor of Bruton’s Tyrosine Kinase, in healthy volunteers. Br. J. Clin. Pharmacol. 2017;83:2367–2376. doi: 10.1111/bcp.13351.
    1. Murrell D., Patsatsi A., Stavropoulos P., Baum S., Zeeli T., Kern J., Roussaki-Schulze A., Sinclair R., Bassukas I., Thomas D., et al. Proof of concept for the clinical effects of oral rilzabrutinib, the first Bruton tyrosine kinase inhibitor for pemphigus vulgaris: The phase II BELIEVE study. Br. J. Dermatol. 2021;185:745–755. doi: 10.1111/bjd.20431.
    1. Kuter D.J., Boccia R.V., Lee E.-J., Efraim M., Tzvetkov N., Mayer J., Trněný M., Kostal M., Hajek R., McDonald V., et al. Phase I/II, open-label, adaptive study of oral Bruton Tyrosine Kinase inhibitor PRN1008 in patients with relapsed/refractory primary or secondary immune thrombocytopenia. Blood. 2019;134:87. doi: 10.1182/blood-2019-122336.
    1. Shirley M. Bruton tyrosine kinase inhibitors in B-cell malignancies: Their use and differential features. Target Oncol. 2022;17:69–84. doi: 10.1007/s11523-021-00857-8.
    1. Reiff S.D., Mantel R., Smith L.L., Greene J., Muhowski E.M., Fabian C.A., Goettl V.M., Tran M., Harrington B.K., Rogers K.A., et al. The BTK inhibitor ARQ 531 targets ibrutinib-resistant CLL and Richter transformation. Cancer Discov. 2018;8:1300–1315. doi: 10.1158/-17-1409.
    1. Xing Y., Chu K.A., Wadhwa J., Chen W., Zhu J., Bradshaw J.M., Shu J., Foulke M.C., Loewenstein N., Nunn P., et al. Preclinical mechanisms of topical PRN473, a Bruton Tyrosine Kinase inhibitor, in immune-mediated skin disease models. ImmunoHorizons. 2021;5:581–589. doi: 10.4049/immunohorizons.2100063.
    1. Goodale E.C., Varjonen K.E., Outerbridge C.A., Bizikova P., Borjesson D., Murrell D.F., Bisconte A., Francesco M., Hill R.J., Masjedizadeh M., et al. Efficacy of a Bruton’s Tyrosine Kinase inhibitor (PRN-473) in the treatment of canine pemphigus foliaceus. Vet. Dermatol. 2020;31:291. doi: 10.1111/vde.12841.
    1. Gillooly K.M., Pulicicchio C., Pattoli M.A., Cheng L., Skala S., Heimrich E.M., McIntyre K.W., Taylor T.L., Kukral D.W., Dudhgaonkar S., et al. Bruton’s Tyrosine Kinase inhibitor BMS986142 in experimental models of rheumatoid arthritis enhances efficacy of agents representing clinical standard-of-care. PLoS ONE. 2017;12:e0181782. doi: 10.1371/journal.pone.0181782.
    1. Michot J.-M., Ribrag V. Pirtobrutinib shows evidence to inaugurate a third generation of BTK inhibitors. Lancet. 2021;397:855–857. doi: 10.1016/S0140-6736(21)00235-X.
    1. Kumagai Y., Tanaka Y., Murata M., Takeuchi T. A phase 1, single and multiple ascending dose study of TAS5315—A novel highly selective inhibitor of Bruton’s Tyrosine Kinase in healthy male volunteers. Ann. Rheumatol. Dis. 2019;78:750.
    1. Yoshiga Y., Hosoi F., Iguchi S., Kaneko R., Nakachi Y., Akasaka D., Tanaka K., Yonekura K., Utsugi T., Sasaki E., et al. TAS5315, a novel Bruton’s Tyrosine Kinase inhibitor, ameliorates inflammation and bone erosion in murine model for rheumatoid arthritis. Arthritis Rheumatol. 2017;69:1320.
    1. Young W.B., Barbosa J., Blomgren P., Bremer M.C., Crawford J.J., Dambach D., Gallion S., Hymowitz S.G., Kropf J.E., Lee S.H., et al. Potent and selective Bruton’s Tyrosine Kinase inhibitors: Discovery of GDC-0834. Bioorg. Med. Chem. Lett. 2015;25:1333–1337. doi: 10.1016/j.bmcl.2015.01.032.
    1. Liu L., Di Paolo 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;338:154–163. doi: 10.1124/jpet.111.181545.
    1. Di Paolo J.A., Huang T., Balazs M., Barbosa J., Barck K.H., Bravo B.J., Carano R.A., Darrow J., Davies D.R., DeForge L.E., et al. Specific BTK inhibition suppresses B cell- and myeloid cell-mediated arthritis. Nat. Chem. Biol. 2011;7:41–50. doi: 10.1038/nchembio.481.
    1. Akinleye A., Chen Y., Mukhi N., Song Y., Liu D. Ibrutinib and novel BTK inhibitors in clinical development. J. Hematol. Oncol. 2013;6:59. doi: 10.1186/1756-8722-6-59.
    1. Ma B., Bohnert T., Otipoby K.L., Tien E., Arefayene M., Bai J., Bajrami B., Bame E., Chan T.R., Humora M., et al. Discovery of BIIB068: A selective, potent, reversible Bruton’s Tyrosine Kinase inhibitor as an orally efficacious agent for autoimmune diseases. J. Med. Chem. 2020;63:12526–12541. doi: 10.1021/acs.jmedchem.0c00702.
    1. Xu D., Kim Y., Postelnek J., Vu M.D., Hu D.-Q., Liao C., Bradshaw M., Hsu J., Zhang J., Pashine A., et al. RN486, a selective Bruton’s Tyrosine Kinase inhibitor, abrogates immune hypersensitivity responses and arthritis in rodents. J. Pharmacol. Exp. Ther. 2012;341:90–103. doi: 10.1124/jpet.111.187740.
    1. Hartkamp L.M., Fine J.S., van Es I.E., Tang M.W., Smith M., Woods J., Narula S., DeMartino J., Tak P.P., Reedquist K.A. BTK inhibition suppresses agonist-induced human macrophage activation and inflammatory gene expression in RA synovial tissue explants. Ann. Rheumatol. Dis. 2015;74:1603–1611. doi: 10.1136/annrheumdis-2013-204143.
    1. Mina-Osorio P., LaStant J., Keirstead N., Whittard T., Ayala J., Stefanova S., Garrido R., Dimaano N., Hilton H., Giron M., et al. Suppression of glomerulonephritis in lupus-prone NZB × NZW mice by RN486, a selective inhibitor of Bruton’s Tyrosine Kinase. Arthritis Rheumatol. 2013;65:2380–2391. doi: 10.1002/art.38047.
    1. Autore F., Pasquale R., Innocenti I., Fresa A., Sora F., Laurenti L. Autoimmune hemolytic anemia in chronic lymphocytic leukemia: A comprehensive review. Cancers. 2021;13:5804. doi: 10.3390/cancers13225804.
    1. Hill Q.A., Stamps R., Massey E., Grainger J., Provan D., Hill A., Haematology T.B.S.F. The diagnosis and management of primary autoimmune haemolytic anaemia. Br. J. Haematol. 2017;176:395–411. doi: 10.1111/bjh.14478.
    1. Noto A., Cassin R., Mattiello V., Reda G. The role of novel agents in treating CLL-associated autoimmune hemolytic anemia. J. Clin. Med. 2021;10:2064. doi: 10.3390/jcm10102064.
    1. Montillo M., O’Brien S., Tedeschi A., Byrd J.C., Dearden C., Gill D., Brown J.R., Barrientos J.C., Mulligan S.P., Furman R.R., et al. Ibrutinib in previously treated chronic lymphocytic leukemia patients with autoimmune cytopenias in the RESONATE study. Blood Cancer J. 2017;7:e524. doi: 10.1038/bcj.2017.5.
    1. Rogers K.A., Ruppert A.S., Bingman A., Andritsos L.A., Awan F.T., Blum K.A., Flynn J.M., Jaglowski S.M., Lozanski G., Maddocks K.J., et al. Incidence and description of autoimmune cytopenias during treatment with ibrutinib for chronic lymphocytic leukemia. Leukemia. 2016;30:346–350. doi: 10.1038/leu.2015.273.
    1. Manda S., Dunbar N., Marx-Wood C.R., Danilov A.V. Ibrutinib is an effective treatment of autoimmune haemolytic anaemia in chronic lymphocytic leukaemia. Br. J. Haematol. 2015;170:734–736. doi: 10.1111/bjh.13328.
    1. Galinier A., Delwail V., Puyade M. Ibrutinib is effective in the treatment of autoimmune haemolytic anaemia in mantle cell lymphoma. Case Rep. Oncol. 2017;10:127–129. doi: 10.1159/000456002.
    1. Molica S., Polliack A. Autoimmune Hemolytic Anemia (AIHA) associated with chronic lymphocytic leukemia in the current era of targeted therapy. Leuk. Res. 2016;50:31–36. doi: 10.1016/j.leukres.2016.09.002.
    1. Rider T.G., Grace R.J., Newman J.A. Autoimmune haemolytic anaemia occurring during ibrutinib therapy for chronic lympho-cytic leukaemia. Br. J. Haematol. 2016;173:326–327. doi: 10.1111/bjh.13602.
    1. Suzuki T., Miyakoshi S., Nanba A., Uchiyama T., Kawamoto K., Aoki S. A case of chronic lymphocytic leukemia complicated by autoimmune hemolytic anemia due to ibrutinib treatment. J. Clin. Exp. Hematop. 2018;58:136–140. doi: 10.3960/jslrt.18012.
    1. Hampel P.J., Larson M.C., Kabat B., Call T.G., Ding W., Kenderian S.S., Bowen D., Boysen J., Schwager S.M., Leis J.F., et al. Autoimmune cytopenias in patients with chronic lymphocytic leukaemia treated with ibrutinib in routine clinical practice at an academic medical centre. Br. J. Haematol. 2018;183:421–427. doi: 10.1111/bjh.15545.
    1. Jalink M., Berentsen S., Castillo J.J., Treon S.P., Cruijsen M., Fattizzo B., Cassin R., Fotiou D., Kastritis E., De Haas M., et al. Effect of ibrutinib treatment on hemolytic anemia and acrocyanosis in cold agglutinin disease/cold agglutinin syndrome. Blood. 2021;138:2002–2005. doi: 10.1182/blood.2021012039.
    1. Byrd J.C., Wierda W.G., Schuh A., Devereux S., Chaves J.M., Brown J.R., Hillmen P., Martin P., Awan F.T., Stephens D.M., et al. Acalabrutinib monotherapy in patients with relapsed/refractory chronic lymphocytic leukemia: Updated phase 2 results. Blood. 2020;135:1204–1213. doi: 10.1182/blood.2018884940.
    1. Witkowski M., Witkowska M., Robak T. Autoimmune thrombocytopenia: Current treatment options in adults with a focus on novel drugs. Eur. J. Haematol. 2019;103:531–541. doi: 10.1111/ejh.13319.
    1. Dobie G., Kuriri F.A., Omar M.M.A., Alanazi F., Gazwani A.M., Tang C.P.S., Sze D.M., Handunnetti S.M., Tam C., Jackson D.E. Ibrutinib, but not zanubrutinib, induces platelet receptor shedding of GPIb-IX-V complex and integrin αIIbβ3 in mice and humans. Blood Adv. 2019;3:4298–4311. doi: 10.1182/bloodadvances.2019000640.
    1. Langrish C.L., Bradshaw J.M., Owens T.D., Campbell R.L., Francesco M.R., Karr D.E., Murray S., Quesenberry R., Smith P., Taylor M., et al. PRN1008, a reversible covalent BTK inhibitor in clinical development for immune thrombocytopenic purpura. Blood. 2017;130:1052.
    1. Kuter J., Efraim M., Mayer J., McDonald V., Bird R., Regenbogen T., Garg M., Kaplan Z., Bandman O., Burns R., et al. Oral rilzabrutinib, a Bruton tyrosine kinase inhibitor, showed clinically active and durable platelet responses and was well-tolerated in patients with heavily pretreated immune thrombocytopenia. Blood. 2020;136:13–14. doi: 10.1182/blood-2020-134932.
    1. Kuter D.J., Bussel J.B., Cooper N., Gernsheimer T., Lambert M.P., Liebman H., Tarantino M.D., Bandman O., Arora P., Neale A., et al. LUNA3 phase III multicenter, double-blind, randomized, placebo-controlled trial of the oral BTK inhibitor rilzabrutinib in adults and adolescents with persistent or chronic immune thrombocytopenia. Blood. 2021;138:1010. doi: 10.1182/blood-2021-144504.
    1. You T., Wang L., Ni X., Hou Y., Liu X., Hou M. Orelabrutinib, a selective Bruton’s Tyrosine Kinase (BTK) inhibitor in the treatment of primary immune thrombocytopenia (ITP) Blood. 2021;138:3172. doi: 10.1182/blood-2021-144691.
    1. Arneson L.C., Carroll K.J., Ruderman E.M. Bruton’s Tyrosine Kinase inhibition for the treatment of rheumatoid arthritis. ImmunoTargets Ther. 2021;10:333–342. doi: 10.2147/ITT.S288550.
    1. Liu Y.-T., Ding H.-H., Lin Z.-M., Wang Q., Chen L., Liu S.-S., Yang X.-Q., Zhu F.-H., Huang Y.-T., Cao S.-Q., et al. A novel tricyclic BTK inhibitor suppresses B cell responses and osteoclastic bone erosion in rheumatoid arthritis. Acta Pharmacol. Sin. 2021;42:1653–1664. doi: 10.1038/s41401-020-00578-0.
    1. Hill R.J., Smith P., Krishnarajah J., Bradshaw J.M., Masjedizadeh M., Bisconte A., Karr D., Owens T.D., Brameld K., Funk J., et al. Discovery of PRN1008, a novel, reversible covalent BTK Inhibitor in clinical development for rheumatoid arthritis. Arthritis Rheumatol. 2015;67:11.
    1. Blaess J., Walther J., Petitdemange A., Gottenberg J.-E., Sibilia J., Arnaud L., Felten R. Immunosuppressive agents for rheumatoid arthritis: A systematic review of clinical trials and their current development stage. Ther. Adv. Musculoskelet. Dis. 2020;12:1759720X20959971. doi: 10.1177/1759720X20959971.
    1. Abdelhameed A.S., Attwa M.W., Al-Shaklia N.S., Kadi A. A highly sensitive LC-MS/MS method to determine novel Bruton’s Tyrosine Kinase inhibitor spebrutinib: Application to metabolic stability evaluation. R. Soc. Open Sci. 2019;6:190434. doi: 10.1098/rsos.190434.
    1. Genovese M.C., Spindler A., Sagawa A., Park W., Dudek A., Kivitz A., Chao J., Chan L.S.M., Witcher J., Barchuk W., et al. Safety and efficacy of poseltinib, Bruton’s Tyrosine Kinase inhibitor, in patients with rheumatoid arthritis: A randomized, double-blind, placebo-controlled, 2-part phase II study. J. Rheumatol. 2021;48:969–976. doi: 10.3899/jrheum.200893.
    1. Ali M., Firoz C.K., Jabir N.R., Rehan M., Khan M.S., Tabrez S. An insight on the pathogenesis and treatment of systemic lupus erythematosus. Endocr. Metab. Immune Disord. Drug Targets. 2018;18:110–123. doi: 10.2174/1871530318666171207145003.
    1. Chalmers S.A., Glynn E., Garcia S.J., Panzenbeck M., Pelletier J., Dimock J., Seccareccia E., Bosanac T., Khalil S., Harcken C., et al. BTK inhibition ameliorates kidney disease in spontaneous lupus nephritis. Clin. Immunol. 2018;197:205–218. doi: 10.1016/j.clim.2018.10.008.
    1. Katewa A., Wang Y., Hackney J.A., Huang T., Suto E., Ramamoorthi N., Austin C.D., Bremer M., Chen J.Z., Crawford J.J., et al. BTK-specific inhibition blocks pathogenic plasma cell signatures and myeloid cell–associated damage in IFNα-driven lupus nephritis. JCI Insight. 2017;2:e90111. doi: 10.1172/jci.insight.90111.
    1. Chalmers S.A., Wen J., Doerner J., Stock A., Cuda C.M., Makinde H.M., Perlman H., Bosanac T., Webb D., Nabozny G., et al. Highly selective inhibition of Bruton’s Tyrosine Kinase attenuates skin and brain disease in murine lupus. Arthritis Res. Ther. 2018;20:10. doi: 10.1186/s13075-017-1500-0.
    1. Bender A.T., Pereira A., Fu K., Samy E., Wu Y., Liu-Bujalski L., Caldwell R., Chen Y.-Y., Tian H., Morandi F., et al. BTK inhibition treats TLR7/IFN driven murine lupus. Clin. Immunol. 2016;164:65–77. doi: 10.1016/j.clim.2016.01.012.
    1. Kil L.P., de Bruijn M.J.W., van Nimwegen M., Corneth O.B.J., van Hamburg J.P., Dingjan G.M., Thaiss F., Rimmelzwaan G.F., Elewaut D., Delsing D., 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. doi: 10.1182/blood-2011-12-397919.
    1. Corneth O.B.J., Verstappen G.M.P., Paulissen S.M.J., de Bruijn M.J.W., Rip J., Lukkes M., van Hamburg J.P., Lubberts E., Bootsma H., Kroese F.G.M., et al. Enhanced Bruton’s Tyrosine Kinase activity in peripheral blood B lymphocytes from patients with autoimmune disease. Arthritis Rheumatol. 2017;69:1313–1324. doi: 10.1002/art.40059.
    1. Einhaus J., Pecher A.C., Asteriti E., Schmid H., Secker K.A., Duerr-Stoerzer S., Keppeler H., Klein R., Schneidawind C., Henes J., et al. Inhibition of effector B cells by ibrutinib in systemic sclerosis. Arthritis Res. Ther. 2020;22:66. doi: 10.1186/s13075-020-02153-8.
    1. García-Merino A. Bruton’s Tyrosine Kinase inhibitors: A new generation of promising agents for multiple sclerosis therapy. Cells. 2021;10:2560. doi: 10.3390/cells10102560.
    1. Li R., Tang H., Burns J.C., Hopkins B.T., Le Coz C., Zhang B., de Barcelos I.P., Romberg N., Goldstein A.C., Banwell B.L., et al. BTK inhibition limits B-cell–T-cell interaction through modulation of B-cell metabolism: Implications for multiple sclerosis therapy. Acta Neuropathol. 2022;143:505–521. doi: 10.1007/s00401-022-02411-w.
    1. Steinmaurer A., Wimmer I., Berger T., Rommer P.S., Sellner J. Bruton’s Tyrosine Kinase inhibition in the treatment of preclinical models and multiple sclerosis. Curr. Pharm. Des. 2022;28:437–444. doi: 10.2174/1381612827666210701152934.
    1. Correale J. BTK inhibitors as potential therapies for multiple sclerosis. Lancet Neurol. 2021;20:689–691. doi: 10.1016/S1474-4422(21)00250-7.
    1. Dolgin E. BTK blockers make headway in multiple sclerosis. Nat. Biotechnol. 2021;39:3–5. doi: 10.1038/s41587-020-00790-7.
    1. Torke S., Pretzsch R., Häusler D., Haselmayer P., Grenningloh R., Boschert U., Brück W., Weber M.S. Inhibition of Bruton’s Tyrosine Kinase interferes with pathogenic B-cell development in inflammatory CNS demyelinating disease. Acta Neuropathol. 2020;140:535–548. doi: 10.1007/s00401-020-02204-z.
    1. Montalban X., Arnold D.L., Weber M.S., Staikov I., Piasecka-Stryczynska K., Willmer J., Martin E.C., Dangond F., Syed S., Wolinsky J.S., et al. Placebo-controlled trial of an oral BTK inhibitor in multiple sclerosis. N. Engl. J. Med. 2019;380:2406–2417. doi: 10.1056/NEJMoa1901981.
    1. Reich D.S., Arnold D.L., Vermersch P., Bar-Or A., Fox R.J., Matta A., Turner T., Wallström E., Zhang X., Mareš M., et al. Safety and efficacy of tolebrutinib, an oral brain-penetrant BTK inhibitor, in relapsing multiple sclerosis: A phase 2b, randomised, double-blind, placebo-controlled trial. Lancet Neurol. 2021;20:729–738. doi: 10.1016/S1474-4422(21)00237-4.
    1. Arnold D., Elliott C., Montalban X., Martin E., Hyvert Y., Tomic D. Effects of evobrutinib, a Bruton’s Tyrosine Kinase inhibitor, on slowly expanding lesions: An emerging imaging marker of chronic tissue loss in multiple sclerosis. Multipl. Scler. J. 2021;27:69.
    1. Patsatsi A., Murrell D.F. Bruton Tyrosine Kinase inhibition and its role as an emerging treatment in Pemphigus. Front. Med. 2021;8:1314. doi: 10.3389/fmed.2021.708071.
    1. Goodale E.C., White S.D., Bizikova P., Borjesson D., Murrell D.F., Bisconte A., Francesco M., Hill R.J., Masjedizadeh M., Nunn P., et al. Open trial of Bruton’s Tyrosine Kinase inhibitor (PRN1008) in the treatment of canine pemphigus foliaceus. Vet. Dermatol. 2020;31:410-e110. doi: 10.1111/vde.12878.
    1. Dispenza M.C., Pongracic J.A., Singh A.M., Bochner B.S. Short-term ibrutinib therapy suppresses skin test responses and eliminates IgE-mediated basophil activation in adults with peanut or tree nut allergy. J. Allergy Clin. Immunol. 2018;141:1914–1916.e7. doi: 10.1016/j.jaci.2017.12.987.
    1. Dispenza M.C. The use of Bruton’s Tyrosine Kinase inhibitors to Treat allergic disorders. Curr. Treat. Options Allergy. 2021;8:261–273. doi: 10.1007/s40521-021-00286-y.
    1. Chovatiya R., Silverberg J. The heterogeneity of atopic dermatitis. J. Drugs Dermatol. 2022;21:172–176. doi: 10.36849/JDD.6408.
    1. Nadeem A., Ahmad S.F., Al-Harbi N.O., Ibrahim K.E., Siddiqui N., Al-Harbi M.M., Attia S.M., Bakheet S.A. Inhibition of Bruton’s Tyrosine Kinase and IL-2 inducible T-cell kinase suppresses both neutrophilic and eosinophilic airway inflammation in a cockroach allergen extract-induced mixed granulocytic mouse model of asthma using preventative and therapeutic strategy. Pharmacol. Res. 2019;148:104441. doi: 10.1016/j.phrs.2019.104441.
    1. Regan J.A., Cao Y., Dispenza M.C., Ma S., Gordon L.I., Petrich A.M., Bochner B.S. Ibrutinib, a Bruton’s Tyrosine Kinase inhibitor used for treatment of lymphoproliferative disorders, eliminates both aeroallergen skin test and basophil activation test reactivity. J. Allergy Clin. Immunol. 2017;140:875–879. doi: 10.1016/j.jaci.2017.03.013.
    1. Vestergaard C., Deleuran M. Chronic spontaneous urticaria: Latest developments in aetiology, diagnosis and therapy. Ther. Adv. Chronic Dis. 2015;6:304–313. doi: 10.1177/2040622315603951.
    1. Maurer M. The Bruton’s Tyrosine Kinase inhibitor remibrutinib (LOU064) in chronic spontaneous urticaria: Top-line results of a phase 2b dose-finding study; Proceedings of the 30th EADV’s Anniversary Congress; Online. 29 September–2 October 2021.
    1. Stone J.H., Zen Y., Deshpande V. IgG4-related disease. N. Engl. J. Med. 2012;366:539–551. doi: 10.1056/NEJMra1104650.
    1. Omar D., Chen Y., Cong Y., Dong L. Glucocorticoids and steroid sparing medications monotherapies or in combination for IgG4-RD: A systematic review and network meta-analysis. Rheumatology. 2020;59:718–726. doi: 10.1093/rheumatology/kez380.
    1. Yamamoto M. B cell targeted therapy for immunoglobulin G4-related disease. Immunol. Med. 2021;44:216–222. doi: 10.1080/25785826.2021.1886630.
    1. Braun L.M., Zeiser R. Kinase inhibition as treatment for acute and chronic graft-versus-host disease. Front. Immunol. 2021;12:760199. doi: 10.3389/fimmu.2021.760199.
    1. Schutt S.D., Fu J., Nguyen H., Bastian D., Heinrichs J., Wu Y., Liu C., McDonald D.G., Pidala J., Yu X.-Z. Inhibition of BTK and ITK with ibrutinib is effective in the prevention of chronic graft-versus-host disease in mice. PLoS ONE. 2015;10:e0137641. doi: 10.1371/journal.pone.0137641.
    1. Miklos D., Cutler C.S., Arora M., Waller E.K., Jagasia M., Pusic I., Flowers M.E., Logan A.C., Nakamura R., Blazar B.R., et al. Ibrutinib for chronic graft-versus-host disease after failure of prior therapy. Blood. 2017;130:2243–2250. doi: 10.1182/blood-2017-07-793786.
    1. Jaglowski S.M., Blazar B.R. How ibrutinib, a B-cell malignancy drug, became an FDA-approved second-line therapy for steroid-resistant chronic GVHD. Blood Adv. 2018;2:2012–2019. doi: 10.1182/bloodadvances.2018013060.
    1. Lipsky A., Lamanna N. Managing toxicities of Bruton tyrosine kinase inhibitors. Hematology. 2020;2020:336–345. doi: 10.1182/hematology.2020000118.
    1. Pleyer C., Sun C., Desai S., Ahn I.E., Tian X., Nierman P., Soto S., Superata J., Valdez J., Lotter J., et al. Reconstitution of humoral immunity and decreased risk of infections in patients with chronic lymphocytic leukemia treated with Bruton Tyrosine Kinase inhibitors. Leuk. Lymphoma. 2020;61:2375–2382. doi: 10.1080/10428194.2020.1772477.
    1. Xiang Z., Kuranda K., Quinn W., Chekaoui A., Ambrose R., Hasanpourghadi M., Novikov M., Newman M.D., Cole M.C., Zhou X., et al. The effect of rapamycin and ibrutinib on antibody responses to adeno-associated virus vector-mediated gene transfer. Hum. Gene Ther. 2022 doi: 10.1089/hum.2021.258. ahead of print.
    1. Weber M.S., Nicholas J.A., Yeaman M.R. Balancing potential benefits and risks of Bruton Tyrosine Kinase inhibitor therapies in multiple sclerosis during the COVID-19 pandemic. Neurol. Neuroimmunol. Neuroinflamm. 2021;8:e1067. doi: 10.1212/NXI.0000000000001067.
    1. Treon S.P., Castillo J.J., Skarbnik A.P., Soumerai J.D., Ghobrial I.M., Guerrera M.L., Meid K., Yang G. The BTK inhibitor ibrutinib may protect against pulmonary injury in COVID-19 infected patients. Blood. 2020;135:1912–1915. doi: 10.1182/blood.2020006288.
    1. Chong E.A., Roeker L.E., Shadman M., Davids M.S., Schuster S.J., Mato A.R. BTK inhibitors in cancer patients with COVID-19: “The winner will be the one who controls that chaos” (Napoleon Bonaparte) Clin. Cancer Res. 2020;26:3514–3516. doi: 10.1158/1078-0432.CCR-20-1427.
    1. Brunner C., Müller B., Wirth T. Bruton’s Tyrosine Kinase is involved in innate and adaptive immunity. Histol. Histopathol. 2005;20:945–955.
    1. Parry H., McIlroy G., Bruton R., Ali M., Stephens C., Damery S., Otter A., McSkeane T., Rolfe H., Faustini S., et al. Antibody responses after first and second COVID-19 vaccination in patients with chronic lymphocytic leukaemia. Blood Cancer J. 2021;11:136. doi: 10.1038/s41408-021-00528-x.

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