Dalrymple SA, Palmer JT (2006) Discovery of selective irreversible inhibitors for Bruton’s
tyrosine kinase. ChemMedChem 2:58–61. https://doi.org/10.1002/cmdc.200600221
73. Honigberg LA, Smith AM, Sirisawad M, Verner E, Loury D, Chang B, Li S, Pan Z, Thamm
DH, Miller RA, Buggy JJ (2010) The Bruton tyrosine kinase inhibitor PCI-32765 blocks
B-cell activation and is efficacious in models of autoimmune disease and B-cell malignancy.
PNAS 107:13075–13080. https://doi.org/10.1073/pnas.1004594107
74. Flanagan ME, Abramite JA, Anderson DP, Aulabaugh A, Dahal UP, Gilbert AM, Li C,
Montgomery J, Oppenheimer SR, Ryder T, Schuff BP, Uccello DP, Walker GS, Wu Y,
Brown MF, Chen JM, Hayward MM, Noe MC, Obach RS, Philippe L,
Shanmugasundaram V, Shapiro MJ, Starr J, Stroh J, Che Y (2014) Chemical and computational methods for the characterization of covalent reactive groups for the prospective design
of irreversible inhibitors. J Med Chem 57:10072–10079. https://doi.org/10.1021/jm501412a
75. Markham A, Dhillon S (2018) Acalabrutinib: first global approval. Drugs 78:139–145. https://
doi.org/10.1007/s40265-017-0852-8
76. Buhimschi AD, Armstrong HA, Toure M, Jaime-Figueroa S, Chen TL, Lehman AM, Woyach
JA, Johnson AJ, Byrd JC, Crews CM (2018) Targeting the C481S ibrutinib-resistance
mutation in Bruton’s tyrosine kinase using PROTAC-mediated degradation. Biochemistry
57:3564–3575. https://doi.org/10.1021/acs.biochem.8b00391
77. Wu H, Huang Q, Qi Z, Chen Y, Wang A, Chen C, Liang Q, Wang J, Chen W, Dong J, Yu K,
Hu C, Wang W, Liu X, Deng Y, Wang L, Wang B, Li X, Gray NS, Liu J, Wei W, Liu Q (2017)
Irreversible inhibition of BTK kinase by a novel highly selective inhibitor CHMFL-BTK-11
suppresses inflammatory response in rheumatoid arthritis model. Sci Rep 7:466. https://doi.
org/10.1038/s41598-017-00482-4
78. Watterson SH, Liu Q, Beaudoin Bertrand M, Batt DG, Li L, Pattoli MA, Skala S, Cheng L,
Obermeier MT, Moore R, Yang Z, Vickery R, Elzinga PA, Discenza L, D’Arienzo C, Gillooly
KM, Taylor TL, Pulicicchio C, Zhang Y, Heimrich E, McIntyre KW, Ruan Q, Westhouse RA,
Catlett IM, Zheng N, Chaudhry C, Dai J, Galella MA, Tebben AJ, Pokross M, Li J, Zhao R,
Smith D, Rampulla R, Allentoff A, Wallace MA, Mathur A, Salter-Cid L, Macor JE, Carter
PH, Fura A, Burke JR, Tino JA (2019) 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 62:3228–3250. https://doi.org/
10.1021/acs.jmedchem.9b00167
79. Park JK, Byun J-Y, Park JA, Kim Y-Y, Lee YJ, Oh JI, Jang SY, Kim YH, Song YW, Son J,
Suh KH, Lee Y-M, Lee EB (2016) 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 18:91. https://doi.org/10.1186/
s13075-016-0988-z
80. Smith PF, Krishnarajah J, Nunn PA, Hill RJ, Karr D, Tam D, Masjedizadeh M, Funk JO,
Gourlay SG (2017) A phase I trial of PRN1008, a novel reversible covalent inhibitor of
Bruton’s tyrosine kinase, in healthy volunteers. Br J Clin Pharmacol 83:2367–2376. https://
doi.org/10.1111/bcp.13351
81. Benson MJ, Rodriguez V, von Schack D, Keegan S, Cook TA, Edmonds J, Benoit S, Seth N,
Du S, Messing D, Nickerson-Nutter CL, Dunussi-Joannopoulos K, Rankin AL, Ruzek M,
Schnute ME, Douhan J (2014) Modeling the clinical phenotype of BTK inhibition in the
mature murine immune system. J Immunol 193:185. https://doi.org/10.4049/jimmunol.
1302570
82. Falgueyret J-P, Oballa RM, Okamoto O, Wesolowski G, Aubin Y, Rydzewski RM, Prasit P,
Riendeau D, Rodan SB, Percival MD (2001) Novel, nonpeptidic cyanamides as potent and
reversible inhibitors of human Cathepsins K and L. J Med Chem 44:94–104. https://doi.org/
10.1021/jm0003440
83. Lainé D, Palovich M, McCleland B, Petitjean E, Delhom I, Xie H, Deng J, Lin G, Davis R,
Jolit A, Nevins N, Zhao B, Villa J, Schneck J, McDevitt P, Midgett R, Kmett C, Umbrecht S,
Covalent Kinase Inhibitors: An Overview
89
tyrosine kinase. ChemMedChem 2:58–61. https://doi.org/10.1002/cmdc.200600221
73. Honigberg LA, Smith AM, Sirisawad M, Verner E, Loury D, Chang B, Li S, Pan Z, Thamm
DH, Miller RA, Buggy JJ (2010) The Bruton tyrosine kinase inhibitor PCI-32765 blocks
B-cell activation and is efficacious in models of autoimmune disease and B-cell malignancy.
PNAS 107:13075–13080. https://doi.org/10.1073/pnas.1004594107
74. Flanagan ME, Abramite JA, Anderson DP, Aulabaugh A, Dahal UP, Gilbert AM, Li C,
Montgomery J, Oppenheimer SR, Ryder T, Schuff BP, Uccello DP, Walker GS, Wu Y,
Brown MF, Chen JM, Hayward MM, Noe MC, Obach RS, Philippe L,
Shanmugasundaram V, Shapiro MJ, Starr J, Stroh J, Che Y (2014) Chemical and computational methods for the characterization of covalent reactive groups for the prospective design
of irreversible inhibitors. J Med Chem 57:10072–10079. https://doi.org/10.1021/jm501412a
75. Markham A, Dhillon S (2018) Acalabrutinib: first global approval. Drugs 78:139–145. https://
doi.org/10.1007/s40265-017-0852-8
76. Buhimschi AD, Armstrong HA, Toure M, Jaime-Figueroa S, Chen TL, Lehman AM, Woyach
JA, Johnson AJ, Byrd JC, Crews CM (2018) Targeting the C481S ibrutinib-resistance
mutation in Bruton’s tyrosine kinase using PROTAC-mediated degradation. Biochemistry
57:3564–3575. https://doi.org/10.1021/acs.biochem.8b00391
77. Wu H, Huang Q, Qi Z, Chen Y, Wang A, Chen C, Liang Q, Wang J, Chen W, Dong J, Yu K,
Hu C, Wang W, Liu X, Deng Y, Wang L, Wang B, Li X, Gray NS, Liu J, Wei W, Liu Q (2017)
Irreversible inhibition of BTK kinase by a novel highly selective inhibitor CHMFL-BTK-11
suppresses inflammatory response in rheumatoid arthritis model. Sci Rep 7:466. https://doi.
org/10.1038/s41598-017-00482-4
78. Watterson SH, Liu Q, Beaudoin Bertrand M, Batt DG, Li L, Pattoli MA, Skala S, Cheng L,
Obermeier MT, Moore R, Yang Z, Vickery R, Elzinga PA, Discenza L, D’Arienzo C, Gillooly
KM, Taylor TL, Pulicicchio C, Zhang Y, Heimrich E, McIntyre KW, Ruan Q, Westhouse RA,
Catlett IM, Zheng N, Chaudhry C, Dai J, Galella MA, Tebben AJ, Pokross M, Li J, Zhao R,
Smith D, Rampulla R, Allentoff A, Wallace MA, Mathur A, Salter-Cid L, Macor JE, Carter
PH, Fura A, Burke JR, Tino JA (2019) 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 62:3228–3250. https://doi.org/
10.1021/acs.jmedchem.9b00167
79. Park JK, Byun J-Y, Park JA, Kim Y-Y, Lee YJ, Oh JI, Jang SY, Kim YH, Song YW, Son J,
Suh KH, Lee Y-M, Lee EB (2016) 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 18:91. https://doi.org/10.1186/
s13075-016-0988-z
80. Smith PF, Krishnarajah J, Nunn PA, Hill RJ, Karr D, Tam D, Masjedizadeh M, Funk JO,
Gourlay SG (2017) A phase I trial of PRN1008, a novel reversible covalent inhibitor of
Bruton’s tyrosine kinase, in healthy volunteers. Br J Clin Pharmacol 83:2367–2376. https://
doi.org/10.1111/bcp.13351
81. Benson MJ, Rodriguez V, von Schack D, Keegan S, Cook TA, Edmonds J, Benoit S, Seth N,
Du S, Messing D, Nickerson-Nutter CL, Dunussi-Joannopoulos K, Rankin AL, Ruzek M,
Schnute ME, Douhan J (2014) Modeling the clinical phenotype of BTK inhibition in the
mature murine immune system. J Immunol 193:185. https://doi.org/10.4049/jimmunol.
1302570
82. Falgueyret J-P, Oballa RM, Okamoto O, Wesolowski G, Aubin Y, Rydzewski RM, Prasit P,
Riendeau D, Rodan SB, Percival MD (2001) Novel, nonpeptidic cyanamides as potent and
reversible inhibitors of human Cathepsins K and L. J Med Chem 44:94–104. https://doi.org/
10.1021/jm0003440
83. Lainé D, Palovich M, McCleland B, Petitjean E, Delhom I, Xie H, Deng J, Lin G, Davis R,
Jolit A, Nevins N, Zhao B, Villa J, Schneck J, McDevitt P, Midgett R, Kmett C, Umbrecht S,
Covalent Kinase Inhibitors: An Overview
89