Biopolym. Cell. 2024; 40(4):247-263.
Огляди
Протеїнкіназа ABL1 як перспективна молекулярна мішень для протиракових препаратів
- Київський академічний університет
бул. Вернадського, 36, Київ, Україна, 03142 - Інститут молекулярної біології і генетики НАН України
Вул. Академіка Заболотного, 150, Київ, Україна, 03143
Abstract
Тирозинкіназа ABL1 відіграє важливу роль у регуляції багатьох клітинних процесів, пов’язаних із ростом, проліферацією, диференціюванням, виживанням, апоптозом, рухливістю клітин, адгезією та ін. Однак, ця протеїнкіназа асоційована із розвитком низки онкологічних захворювань. В огляді зроблено спробу підсумувати літературні дані щодо структури, функцій, ролі ABL1 у розвитку раку та існуючих інгібіторів цієї протеїнкінази.
Keywords: протеїнкіназа ABL1, онкологічні захворювання, інгібітор
Повний текст: (PDF, англійською)
References
[1]
Ben-Neriah Y, Daley GQ, Mes-Masson AM, Witte ON, Baltimore D. The chronic myelogenous leukemia-specific P210 protein is the product of the bcr/abl hybrid gene. Science. 1986; 233(4760):212-4.
[2]
Hantschel O, Grebien F, Superti-Furga G. The growing arsenal of ATP-competitive and allosteric inhibitors of BCR-ABL. Cancer Res. 2012; 72(19):4890-5.
[3]
Schwartzberg PL, Stall AM, Hardin JD, Bowdish KS, Humaran T, Boast S, Harbison ML, Robertson EJ, Goff SP. Mice homozygous for the ablm1 mutation show poor viability and depletion of selected B and T cell populations. Cell. 1991; 65(7):1165-75.
[4]
Tybulewicz VL, Crawford CE, Jackson PK, Bronson RT, Mulligan RC. Neonatal lethality and lymphopenia in mice with a homozygous disruption of the c-abl proto-oncogene. Cell. 1991; 65(7):1153-63.
[5]
Hantschel O, Superti-Furga G. Regulation of the c-Abl and Bcr-Abl tyrosine kinases. Nat Rev Mol Cell Biol. 2004; 5(1):33-44.
[6]
ABL1 - Tyrosine-protein kinase ABL1 - Homo sapiens (Human)
[8]
Corbi-Verge C, Marinelli F, Zafra-Ruano A, Ruiz-Sanz J, Luque I, Faraldo-Gómez JD. Two-state dynamics of the SH3-SH2 tandem of Abl kinase and the allosteric role of the N-cap. Proc Natl Acad Sci U S A. 2013; 110(36):E3372-80.
[9]
Brasher BB, Van Etten RA. c-Abl has high intrinsic tyrosine kinase activity that is stimulated by mutation of the Src homology 3 domain and by autophosphorylation at two distinct regulatory tyrosines. J Biol Chem. 2000; 275(45):35631-7.
[10]
Dorey K, Engen JR, Kretzschmar J, Wilm M, Neubauer G, Schindler T, Superti-Furga G. Phosphorylation and structure-based functional studies reveal a positive and a negative role for the activation loop of the c-Abl tyrosine kinase. Oncogene. 2001; 20(56):8075-84.
[11]
Muller AJ, Pendergast AM, Parmar K, Havlik MH, Rosenberg N, Witte ON. En bloc substitution of the Src homology region 2 domain activates the transforming potential of the c-Abl protein tyrosine kinase. Proc Natl Acad Sci U S A. 1993; 90(8):3457-61.
[12]
Plattner R, Kadlec L, DeMali KA, Kazlauskas A, Pendergast AM. c-Abl is activated by growth factors and Src family kinases and has a role in the cellular response to PDGF. Genes Dev. 1999; 13(18):2400-11.
[13]
Woodring PJ, Hunter T, Wang JY. Inhibition of c-Abl tyrosine kinase activity by filamentous actin. J Biol Chem. 2001; 276(29):27104-10.
[14]
Guo XY, Balague C, Wang T, Randhawa G, Yuan Z, Bachier C, Greenberger J, Arlinghaus R, Kufe D, Deisseroth AB. The presence of the Rb c-box peptide in the cytoplasm inhibits p210bcr-abl transforming function. Oncogene. 1999; 18(8):1589-95.
[15]
Knudsen ES, Wang JY. Differential regulation of retinoblastoma protein function by specific Cdk phosphorylation sites. J Biol Chem. 1996; 271(14):8313-20.
[16]
Macdonald JI, Dick FA. Posttranslational modifications of the retinoblastoma tumor suppressor protein as determinants of function. Genes Cancer. 2012; 3(11-12):619-33.
[17]
Colicelli J. ABL tyrosine kinases: evolution of function, regulation, and specificity. Sci Signal. 2010; 3(139):re6.
[18]
McWhirter JR, Wang JY. Activation of tyrosinase kinase and microfilament-binding functions of c-abl by bcr sequences in bcr/abl fusion proteins. Mol Cell Biol. 1991; 11(3):1553-65.
[19]
Antonenko SV, Gurianov DS, Telegeev GD. Colocalization of USP1 and РН domain of Bcr-Abl oncoprotein in terms of chronic myeloid leukemia cell rearrangements. Cytol Genet. 2016; 50(5):352-6.
[20]
Antonenko S, Zavelevich M, Telegeev G. The role of USP1 deubiquitinase in the pathogenesis and therapy of cancer. Acta Biochim Pol. 2023; 70(2):219-31.
[21]
Wong S, Witte ON. The BCR-ABL story: bench to bedside and back. Annu Rev Immunol. 2004; 22:247-306.
[22]
Burmeister T, Schwartz S, Bartram CR, Gökbuget N, Hoelzer D, Thiel E; GMALL study group. Patients' age and BCR-ABL frequency in adult B-precursor ALL: a retrospective analysis from the GMALL study group. Blood. 2008; 112(3):918-9.
[23]
Pane F, Frigeri F, Sindona M, Luciano L, Ferrara F, Cimino R, Meloni G, Saglio G, Salvatore F, Rotoli B. Neutrophilic-chronic myeloid leukemia: a distinct disease with a specific molecular marker (BCR/ABL with C3/A2 junction). Blood. 1996; 88(7):2410-4.
[24]
Wilson G, Frost L, Goodeve A, Vandenberghe E, Peake I, Reilly J. BCR-ABL transcript with an e19a2 (c3a2) junction in classical chronic myeloid leukemia. Blood. 1997; 89(8):3064.
[25]
Hagemeijer A, Graux C. ABL1 rearrangements in T-cell acute lymphoblastic leukemia. Genes Chromosomes Cancer. 2010; 49(4):299-308.
[26]
De Braekeleer E, Douet-Guilbert N, Rowe D, Bown N, Morel F, Berthou C, Férec C, De Braekeleer M. ABL1 fusion genes in hematological malignancies: a review. Eur J Haematol. 2011; 86(5):361-71.
[27]
Ernst T, Score J, Deininger M, Hidalgo-Curtis C, Lackie P, Ershler WB, Goldman JM, Cross NC, Grand F. Identification of FOXP1 and SNX2 as novel ABL1 fusion partners in acute lymphoblastic leukaemia. Br J Haematol. 2011; 153(1):43-6.
[28]
Simpson L, He X, Pins M, Huang X, Campbell SC, Yang XJ, Perlman EJ, Bergan RC. Renal medullary carcinoma and ABL gene amplification. J Urol. 2005; 173(6):1883-8.
[29]
Lamballe F, Toscano S, Conti F, Arechederra M, Baeza N, Figarella-Branger D, Helmbacher F, Maina F. Coordination of signalling networks and tumorigenic properties by ABL in glioblastoma cells. Oncotarget. 2016; 7(46):74747-67.
[30]
Zhao H, Ou-Yang F, Chen IF, Hou MF, Yuan SS, Chang HL, Lee YC, Plattner R, Waltz SE, Ho SM, Sims J, Wang SC. Enhanced resistance to tamoxifen by the c-ABL proto-oncogene in breast cancer. Neoplasia. 2010; 12(3):214-23.
[31]
Craig VJ, Cogliatti SB, Rehrauer H, Wündisch T, Müller A. Epigenetic silencing of microRNA-203 dysregulates ABL1 expression and drives Helicobacter-associated gastric lymphomagenesis. Cancer Res. 2011; 71(10):3616-24.
[32]
Liu Y, Cao J, Zhu YN, Ma Y, Murtaza G, Li Y, Wang JH, Pu YS. C1222C Deletion in Exon 8 of ABL1 Is Involved in Carcinogenesis and Cell Cycle Control of Colorectal Cancer Through IRS1/PI3K/Akt Pathway. Front Oncol. 2020; 10:1385.
[33]
Vincent C, Groepper D, Mubayed L, Fleischer J. Broadening the phenotype of ABL1-associated disorder. GIM Open. 2023; 1(1):100370.
[34]
Wang X, Charng WL, Chen CA, Rosenfeld JA, Al Shamsi A, Al-Gazali L, McGuire M, Mew NA, Arnold GL, Qu C, Ding Y, Muzny DM, Gibbs RA, Eng CM, Walkiewicz M, Xia F, Plon SE, Lupski JR, Schaaf CP, Yang Y. Germline mutations in ABL1 cause an autosomal dominant syndrome characterized by congenital heart defects and skeletal malformations. Nat Genet. 2017; 49(4):613-7.
[35]
Chen CA, Crutcher E, Gill H, Nelson TN, Robak LA, Jongmans MCJ, Pfundt R, Prasad C, Berard RA, Fannemel M, Frengen E, Misceo D, Ramsey K, Yang Y, Schaaf CP, Wang X. The expanding clinical phenotype of germline ABL1-associated congenital heart defects and skeletal malformations syndrome. Hum Mutat. 2020; 41(10):1738-44.
[36]
Blakes AJM, Gaul E, Lam W, Shannon N, Knapp KM, Bicknell LS, Jackson MR, Wade EM, Robertson S, White SM, Heller R, Chase A, Baralle D, Douglas AGL. Pathogenic variants causing ABL1 malformation syndrome cluster in a myristoyl-binding pocket and increase tyrosine kinase activity. Eur J Hum Genet. 2021; 29(4):593-603.
[37]
O'Brien SG, Guilhot F, Larson RA, Gathmann I, Baccarani M, Cervantes F, Cornelissen JJ, Fischer T, Hochhaus A, Hughes T, Lechner K, Nielsen JL, Rousselot P, Reiffers J, Saglio G, Shepherd J, Simonsson B, Gratwohl A, Goldman JM, Kantarjian H, Taylor K, Verhoef G, Bolton AE, Capdeville R, Druker BJ; IRIS Investigators. Imatinib compared with interferon and low-dose cytarabine for newly diagnosed chronic-phase chronic myeloid leukemia. N Engl J Med. 2003; 348(11):994-1004.
[38]
Kimura S. Dasatinib, nilotinib, bosutinib, ponatinib, and other TKIs. In: Chemotherapy for leukemia.- Singapore: Springer Singapore, 2017.- 369p.
[39]
Reddy EP, Aggarwal AK. The ins and outs of bcr-abl inhibition. Genes Cancer. 2012; 3(5-6):447-54.
[40]
Rossari F, Minutolo F, Orciuolo E. Past, present, and future of Bcr-Abl inhibitors: from chemical development to clinical efficacy. J Hematol Oncol. 2018; 11(1):84.
[41]
Weisberg E, Manley PW, Breitenstein W, Brüggen J, Cowan-Jacob SW, Ray A, Huntly B, Fabbro D, Fendrich G, Hall-Meyers E, Kung AL, Mestan J, Daley GQ, Callahan L, Catley L, Cavazza C, Azam M, Neuberg D, Wright RD, Gilliland DG, Griffin JD. Characterization of AMN107, a selective inhibitor of native and mutant Bcr-Abl. Cancer Cell. 2005; 7(2):129-41.
[42]
Kantarjian HM, Shah NP, Cortes JE, Baccarani M, Agarwal MB, Undurraga MS, Wang J, Ipiña JJ, Kim DW, Ogura M, Pavlovsky C, Junghanss C, Milone JH, Nicolini FE, Robak T, Van Droogenbroeck J, Vellenga E, Bradley-Garelik MB, Zhu C, Hochhaus A. Dasatinib or imatinib in newly diagnosed chronic-phase chronic myeloid leukemia: 2-year follow-up from a randomized phase 3 trial (DASISION). Blood. 2012; 119(5):1123-9.
[43]
Cortes JE, Gambacorti-Passerini C, Deininger MW, Mauro MJ, Chuah C, Kim DW, Dyagil I, Glushko N, Milojkovic D, le Coutre P, Garcia-Gutierrez V, Reilly L, Jeynes-Ellis A, Leip E, Bardy-Bouxin N, Hochhaus A, Brümmendorf TH. Bosutinib Versus Imatinib for Newly Diagnosed Chronic Myeloid Leukemia: Results From the Randomized BFORE Trial. J Clin Oncol. 2018; 36(3):231-7.
[44]
Boschelli F, Arndt K, Gambacorti-Passerini C. Bosutinib: a review of preclinical studies in chronic myelogenous leukaemia. Eur J Cancer. 2010; 46(10):1781-9.
[45]
Hochhaus A, Saussele S, Rosti G, Mahon FX, Janssen JJWM, Hjorth-Hansen H, Richter J, Buske C; ESMO Guidelines Committee. Chronic myeloid leukaemia: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2018; 29(Suppl 4):iv261.
[46]
Qian H, Gang D, He X, Jiang S. A review of the therapeutic role of the new third-generation TKI olverembatinib in chronic myeloid leukemia. Front Oncol. 2022; 12:1036437.
[47]
Huang WS, Metcalf CA, Sundaramoorthi R, Wang Y, Zou D, Thomas RM, Zhu X, Cai L, Wen D, Liu S, Romero J, Qi J, Chen I, Banda G, Lentini SP, Das S, Xu Q, Keats J, Wang F, Wardwell S, Ning Y, Snodgrass JT, Broudy MI, Russian K, Zhou T, Commodore L, Narasimhan NI, Mohemmad QK, Iuliucci J, Rivera VM, Dalgarno DC, Sawyer TK, Clackson T, Shakespeare WC. Discovery of 3-[2-(imidazo[1,2-b]pyridazin-3-yl)ethynyl]-4-methyl-N-{4-[(4-methylpiperazin-1-yl)methyl]-3-(trifluoromethyl)phenyl}benzamide (AP24534), a potent, orally active pan-inhibitor of breakpoint cluster region-abelson (BCR-ABL) kinase including the T315I gatekeeper mutant. J Med Chem. 2010; 53(12):4701-19.
[48]
Cortes JE, Kantarjian H, Shah NP, Bixby D, Mauro MJ, Flinn I, O'Hare T, Hu S, Narasimhan NI, Rivera VM, Clackson T, Turner CD, Haluska FG, Druker BJ, Deininger MW, Talpaz M. Ponatinib in refractory Philadelphia chromosome-positive leukemias. N Engl J Med. 2012; 367(22):2075-88.
[49]
Hughes TP, Mauro MJ, Cortes JE, Minami H, Rea D, DeAngelo DJ, Breccia M, Goh YT, Talpaz M, Hochhaus A, le Coutre P, Ottmann O, Heinrich MC, Steegmann JL, Deininger MWN, Janssen JJWM, Mahon FX, Minami Y, Yeung D, Ross DM, Tallman MS, Park JH, Druker BJ, Hynds D, Duan Y, Meille C, Hourcade-Potelleret F, Vanasse KG, Lang F, Kim DW. Asciminib in Chronic Myeloid Leukemia after ABL Kinase Inhibitor Failure. N Engl J Med. 2019; 381(24):2315-23.
[50]
Kimura S, Naito H, Segawa H, Kuroda J, Yuasa T, Sato K, Yokota A, Kamitsuji Y, Kawata E, Ashihara E, Nakaya Y, Naruoka H, Wakayama T, Nasu K, Asaki T, Niwa T, Hirabayashi K, Maekawa T. NS-187, a potent and selective dual Bcr-Abl/Lyn tyrosine kinase inhibitor, is a novel agent for imatinib-resistant leukemia. Blood. 2005; 106(12):3948-54.
[51]
Rix U, Hantschel O, Dürnberger G, Remsing Rix LL, Planyavsky M, Fernbach NV, Kaupe I, Bennett KL, Valent P, Colinge J, Köcher T, Superti-Furga G. Chemical proteomic profiles of the BCR-ABL inhibitors imatinib, nilotinib, and dasatinib reveal novel kinase and nonkinase targets. Blood. 2007; 110(12):4055-63.
[52]
Lambert GK, Duhme-Klair AK, Morgan T, Ramjee MK. The background, discovery and clinical development of BCR-ABL inhibitors. Drug Discov Today. 2013; 18(19-20):992-1000.
[53]
Kantarjian H, le Coutre P, Cortes J, Pinilla-Ibarz J, Nagler A, Hochhaus A, Kimura S, Ottmann O. Phase 1 study of INNO-406, a dual Abl/Lyn kinase inhibitor, in Philadelphia chromosome-positive leukemias after imatinib resistance or intolerance. Cancer. 2010; 116(11):2665-72.
[54]
Eide CA, Adrian LT, Tyner JW, Mac Partlin M, Anderson DJ, Wise SC, Smith BD, Petillo PA, Flynn DL, Deininger MW, O'Hare T, Druker BJ. The ABL switch control inhibitor DCC-2036 is active against the chronic myeloid leukemia mutant BCR-ABLT315I and exhibits a narrow resistance profile. Cancer Res. 2011; 71(9):3189-95.
[55]
Chan WW, Wise SC, Kaufman MD, Ahn YM, Ensinger CL, Haack T, Hood MM, Jones J, Lord JW, Lu WP, Miller D, Patt WC, Smith BD, Petillo PA, Rutkoski TJ, Telikepalli H, Vogeti L, Yao T, Chun L, Clark R, Evangelista P, Gavrilescu LC, Lazarides K, Zaleskas VM, Stewart LJ, Van Etten RA, Flynn DL. Conformational control inhibition of the BCR-ABL1 tyrosine kinase, including the gatekeeper T315I mutant, by the switch-control inhibitor DCC-2036. Cancer Cell. 2011; 19(4):556-68.
[56]
Cortes J, Talpaz M, Smith HP, Snyder DS, Khoury J, Bhalla KN, Pinilla-Ibarz J, Larson R, Mitchell D, Wise SC, Rutkoski TJ, Smith BD, Flynn DL, Kantarjian HM, Rosen O, Van Etten RA. Phase 1 dose-finding study of rebastinib (DCC-2036) in patients with relapsed chronic myeloid leukemia and acute myeloid leukemia. Haematologica. 2017; 102(3):519-28.
[57]
Bebbington D, Binch H, Charrier JD, Everitt S, Fraysse D, Golec J, Kay D, Knegtel R, Mak C, Mazzei F, Miller A, Mortimore M, O'Donnell M, Patel S, Pierard F, Pinder J, Pollard J, Ramaya S, Robinson D, Rutherford A, Studley J, Westcott J. The discovery of the potent aurora inhibitor MK-0457 (VX-680). Bioorg Med Chem Lett. 2009; 19(13):3586-92.
[58]
Young MA, Shah NP, Chao LH, Seeliger M, Milanov ZV, Biggs WH 3rd, Treiber DK, Patel HK, Zarrinkar PP, Lockhart DJ, Sawyers CL, Kuriyan J. Structure of the kinase domain of an imatinib-resistant Abl mutant in complex with the Aurora kinase inhibitor VX-680. Cancer Res. 2006; 66(2):1007-14.
[59]
Giles FJ, Swords RT, Nagler A, Hochhaus A, Ottmann OG, Rizzieri DA, Talpaz M, Clark J, Watson P, Xiao A, Zhao B, Bergstrom D, Le Coutre PD, Freedman SJ, Cortes JE. MK-0457, an Aurora kinase and BCR-ABL inhibitor, is active in patients with BCR-ABL T315I leukemia. Leukemia. 2013; 27(1):113-7.
[60]
Borthakur G, Dombret H, Schafhausen P, Brummendorf TH, Boissel N, Jabbour E, Mariani M, Capolongo L, Carpinelli P, Davite C, Kantarjian H, Cortes JE. A phase I study of danusertib (PHA-739358) in adult patients with accelerated or blastic phase chronic myeloid leukemia and Philadelphia chromosome-positive acute lymphoblastic leukemia resistant or intolerant to imatinib and/or other second generation c-ABL therapy. Haematologica. 2015; 100(7):898-904.
[61]
Weisberg E, Choi HG, Ray A, Barrett R, Zhang J, Sim T, Zhou W, Seeliger M, Cameron M, Azam M, Fletcher JA, Debiec-Rychter M, Mayeda M, Moreno D, Kung AL, Janne PA, Khosravi-Far R, Melo JV, Manley PW, Adamia S, Wu C, Gray N, Griffin JD. Discovery of a small-molecule type II inhibitor of wild-type and gatekeeper mutants of BCR-ABL, PDGFRalpha, Kit, and Src kinases: novel type II inhibitor of gatekeeper mutants. Blood. 2010; 115(21):4206-16.
[62]
Karaman MW, Herrgard S, Treiber DK, Gallant P, Atteridge CE, Campbell BT, Chan KW, Ciceri P, Davis MI, Edeen PT, Faraoni R, Floyd M, Hunt JP, Lockhart DJ, Milanov ZV, Morrison MJ, Pallares G, Patel HK, Pritchard S, Wodicka LM, Zarrinkar PP. A quantitative analysis of kinase inhibitor selectivity. Nat Biotechnol. 2008; 26(1):127-32.
[63]
Soverini S, Mancini M, Bavaro L, Cavo M, Martinelli G. Chronic myeloid leukemia: the paradigm of targeting oncogenic tyrosine kinase signaling and counteracting resistance for successful cancer therapy. Mol Cancer. 2018; 17(1):49.