MCL-1 is a key determinant of breast cancer cell survival: Validation of MCL-1 dependency utilizing a highly selective small molecule inhibitor

Molecular Cancer Therapeutics

Volumn 14, Issue 8, 2015, Pages 1837-1847

  Xiao, Yu ^a   Nimmer, Paul ^a   Sheppard, George S ^a   Bruncko, Milan ^a   Hessler, Paul ^a   Lu, Xin ^a   Roberts Rapp, Lisa ^a   Pappano, William N ^a   Elmore, Steven W ^a   Souers, Andrew J ^a   Leverson, Joel D ^a   Phillips, Darren C ^a  

^a ABBVIE INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

A 1210477; BIM PROTEIN; FLAVOPIRIDOL; NAVITOCLAX; PROTEIN BAK; PROTEIN BCL XL; PROTEIN INHIBITOR; PROTEIN MCL 1; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; ANILINE DERIVATIVE; ANTINEOPLASTIC AGENT; PROTEIN BCL 2; PROTEIN BCL X; SULFONAMIDE;

APOPTOSIS; ARTICLE; BREAST CANCER CELL LINE; CANCER SURVIVAL; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; MICROARRAY ANALYSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA ISOLATION; WESTERN BLOTTING; ANTAGONISTS AND INHIBITORS; BREAST TUMOR; DRUG EFFECTS; FEMALE; GENE EXPRESSION; GENETICS; HUMAN; METABOLISM; RNA INTERFERENCE; TUMOR CELL LINE;

ANILINE COMPOUNDS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BCL-2 HOMOLOGOUS ANTAGONIST-KILLER PROTEIN; BCL-X PROTEIN; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL SURVIVAL; FEMALE; GENE EXPRESSION; HUMANS; MYELOID CELL LEUKEMIA SEQUENCE 1 PROTEIN; PROTO-ONCOGENE PROTEINS C-BCL-2; RNA INTERFERENCE; RNA, SMALL INTERFERING; SULFONAMIDES;

EID: 84942103252     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-14-0928     Document Type: Article

References (47)

1. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011;144:646-74.
2. Strasser A, Cory S, Adams JM. Deciphering the rules of programmed cell death to improve therapy of cancer and other diseases. EMBO J 2011;30:3667-83.
3. Phillips DC, Dias HK, KitasGD, Griffiths HR. Aberrant reactive oxygen and nitrogen species generation in rheumatoid arthritis (RA): causes and consequences for immune function, cell survival, and therapeutic intervention. Antioxid Redox Signal 2010;12:743-85.
4. Chipuk JE, Moldoveanu T, Llambi F, Parsons MJ, Green DR. The BCL-2 family reunion. Mol Cell 2010;37:299-310.
5. Llambi F, Moldoveanu T, Tait SW, Bouchier-Hayes L, Temirov J, McCormick LL, et al. A unified model of mammalian BCL-2 protein family interactions at the mitochondria. Mol Cell 2011;44:517-31.
6. Leber B, Lin J, Andrews DW. Embedded together: the life and death consequences of interaction of the Bcl-2 family with membranes. Apoptosis 2007;12:897-911.
7. Shamas-Din A, Kale J, Leber B, Andrews DW. Mechanisms of action of Bcl-2 family proteins. Cold Spring Harb Perspect Biol 2013;5:a008714.
8. Wei MC, Zong WX, Cheng EH, Lindsten T, Panoutsakopoulou V, Ross AJ, et al. Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 2001;292:727-30.
9. Lindsten T, Ross AJ, King A, Zong WX, Rathmell JC, Shiels HA, et al. The combined functions of proapoptotic Bcl-2 family members bak and bax are essential for normal development of multiple tissues. Mol Cell 2000;6:1389-99.
10. Vaux DL, Cory S, Adams JM. Bcl-2 gene promotes haemopoietic cell survival and cooperates with c-myc to immortalize pre-B cells. Nature 1988;335:440-2.
11. Strasser A, Harris AW, Bath ML, Cory S. Novel primitive lymphoid tumours induced in transgenic mice by cooperation between myc and bcl-2. Nature 1990;348:331-3.
12. Zhou P, Levy NB, Xie H, Qian L, Lee CY, Gascoyne RD, et al. MCL1 transgenic mice exhibit a high incidence of B-cell lymphoma manifested as a spectrum of histologic subtypes. Blood 2001;97:3902-9.
13. Campbell KJ, Bath ML, Turner ML, Vandenberg CJ, Bouillet P, Metcalf D, et al. Elevated Mcl-1 perturbs lymphopoiesis, promotes transformation of hematopoietic stem/progenitor cells, and enhances drug resistance. Blood 2010;116:3197-207.
14. Certo M, Del Gaizo Moore V, Nishino M, Wei G, Korsmeyer S, Armstrong SA, et al. Mitochondria primed by death signals determine cellular addiction to antiapoptotic BCL-2 family members. Cancer Cell 2006;9:351-65.
15. Deng J, Carlson N, Takeyama K, Dal Cin P, Shipp M, Letai A. BH3 profiling identifies three distinct classes of apoptotic blocks to predict response to ABT-737 andconventional chemotherapeutic agents. Cancer Cell2007;12:171-85.
16. Weinstein IB. Cancer. Addiction to oncogenes-the Achilles heal of cancer. Science 2002;297:63-4.
17. Tse C, Shoemaker AR, Adickes J, Anderson MG, Chen J, Jin S, et al. ABT-263: a potent and orally bioavailable Bcl-2 family inhibitor. Cancer Res 2008;68:3421-8.
18. Shoemaker AR, Mitten MJ, Adickes J, Ackler S, Refici M, Ferguson D, et al. Activity of the Bcl-2 family inhibitor ABT-263 in a panel of small cell lung cancer xenograft models. Clin Cancer Res 2008;14:3268-77.
19. Tahir SK, Wass J, Joseph MK, Devanarayan V, Hessler P, Zhang H, et al. Identification of expression signatures predictive of sensitivity to the Bcl-2 family member inhibitor ABT-263 in small cell lung carcinoma and leukemia/lymphoma cell lines. Mol Cancer Ther 2010;9:545-57.
20. Roberts AW, Seymour JF, Brown JR, Wierda WG, Kipps TJ, Khaw SL, et al. Substantial susceptibility of chronic lymphocytic leukemia to BCL2 inhibition: results of a phase I study of navitoclax in patients with relapsed or refractory disease. J Clin Oncol 2012;30:488-96.
21. Rudin CM, Hann CL, Garon EB, Ribeiro de Oliveira M, Bonomi PD, Camidge DR, et al. Phase II study of single-agent navitoclax (ABT-263) and biomarker correlates in patients with relapsed small cell lung cancer. Clin Cancer Res 2012;18:3163-9.
22. Tahir SK, Yang X, Anderson MG, Morgan-Lappe SE, Sarthy AV, Chen J, et al. Influence of Bcl-2 family members on the cellular response of small-cell lung cancer cell lines to ABT-737. Cancer Res 2007;67:1176-83.
23. van Delft MF, Wei AH, Mason KD, Vandenberg CJ, Chen L, Czabotar PE, et al. The BH3 mimetic ABT-737 targets selective Bcl-2 proteins and efficiently induces apoptosis via Bak/Bax if Mcl-1 is neutralized. Cancer Cell 2006;10:389-99.
24. Wertz IE, Kusam S, Lam C, Okamoto T, Sandoval W, Anderson DJ, et al. Sensitivity to antitubulin chemotherapeutics is regulated by MCL1 and FBW7. Nature 2011;471:110-4.
25. Kim SH, Ricci MS, El-Deiry WS. Mcl-1: a gateway to TRAIL sensitization. Cancer Res 2008;68:2062-4.
26. Beroukhim R, Mermel CH, Porter D, Wei G, Raychaudhuri S, Donovan J, et al. The landscape of somatic copy-number alteration across human cancers. Nature 2010;463:899-905.
27. Ding Q, He X, Xia W, Hsu JM, Chen CT, Li LY, et al. Myeloid cell leukemia-1 inversely correlates with glycogen synthase kinase-3beta activity and associates with poor prognosis in human breast cancer. Cancer Res 2007;67:4564-71.
28. Bruncko M, Wang L, Sheppard G, Petros A, Zhang H, Nimmer P, et al. Structure-guided design of a series of high affinity and selective MCL-1 inhibitors. J Med Chem 2015;58:2180-94.
29. Park CM, Bruncko M, Adickes J, Bauch J, Ding H, Kunzer A, et al. Discovery of an orally bioavailable small molecule inhibitor of prosurvival B-cell lymphoma 2 proteins. J Med Chem 2008;51:6902-15.
30. Verbrugge I, de Vries E, Tait SW, Wissink EH, Walczak H, Verheij M, et al. Ionizing radiation modulates the TRAIL death-inducing signaling complex, allowing bypass of the mitochondrial apoptosis pathway. Oncogene 2008;27:574-84.
31. Huang DC, Cory S, Strasser A. Bcl-2, Bcl-XL and adenovirus protein E1B19kD are functionally equivalent in their ability to inhibit cell death. Oncogene 1997;14:405-14.
32. Phillips DC, Garrison SP, Jeffers JR, Zambetti GP. Assays to measure p53-dependent and -independent apoptosis. Methods Mol Biol 2009;559:143-59.
33. Phillips DC, Martin S, Doyle BT, Houghton JA. Sphingosine-induced apoptosis in rhabdomyosarcoma cell lines is dependent on pre-mitochondrial Bax activation and post-mitochondrial caspases. Cancer Res 2007;67:756-64.
34. Borisy AA, Elliott PJ, Hurst NW, Lee MS, Lehar J, Price ER, et al. Systematic discovery of multicomponent therapeutics. Proc Natl Acad Sci U S A 2003;100:7977-82.
35. Chen R, Keating MJ, Gandhi V, Plunkett W. Transcription inhibition by flavopiridol: mechanism of chronic lymphocytic leukemia cell death. Blood 2005;106:2513-9.
36. Gojo I, Zhang B, Fenton RG. The cyclin-dependent kinase inhibitor flavopiridol induces apoptosis in multiple myeloma cells through transcriptional repression and down-regulation of Mcl-1. Clin Cancer Res 2002;8:3527-38.
37. Tsujimoto Y, Finger LR, Yunis J, Nowell PC, Croce CM. Cloning of the chromosome breakpoint of neoplastic B cells with the t(14;18) chromosome translocation. Science 1984;226:1097-9.
38. Galteland E, Sivertsen EA, Svendsrud DH, Smedshammer L, Kresse SH, Meza-Zepeda LA, et al. Translocation t(14;18) and gain of chromosome 18/BCL2: effects on BCL2 expression and apoptosis in B-cell non-Hodgkin's lymphomas. Leukemia 2005;19:2313-23.
39. Zhang H, Guttikonda S, Roberts L, Uziel T, Semizarov D, Elmore SW, et al. Mcl-1 is critical for survival in a subgroup of non-small-cell lung cancer cell lines. Oncogene 2011;30:1963-8.
40. Cuconati A, Mukherjee C, Perez D, White E. DNA damage response and MCL-1 destruction initiate apoptosis in adenovirus-infected cells. Genes Dev 2003;17:2922-32.
41. Leu JI, Dumont P, Hafey M, Murphy ME, George DL. Mitochondrial p53 activates Bak and causes disruption of a Bak-Mcl1 complex. Nat Cell Biol 2004;6:443-50.
42. Willis SN, Chen L, Dewson G, Wei A, Naik E, Fletcher JI, et al. Proapoptotic Bak is sequestered by Mcl-1 and Bcl-xL, but not Bcl-2, until displaced by BH3-only proteins. Genes Dev 2005;19:1294-305.
43. Dunkle A, Dzhagalov I, He YW. Mcl-1 promotes survival of thymocytes by inhibition of Bak in a pathway separate from Bcl-2. Cell Death Differ 2010;17:994-1002.
44. Farrow SN, White JH, Martinou I, Raven T, Pun KT, Grinham CJ, et al. Cloning of a bcl-2 homologue by interaction with adenovirus E1B 19K. Nature 1995;374:731-3.
45. Zhai D, Jin C, Huang Z, Satterthwait AC, Reed JC. Differential regulation of Bax and Bak by anti-apoptotic Bcl-2 family proteins Bcl-B and Mcl-1. J Biol Chem 2008;283:9580-6.
46. Souers AJ, Leverson JD, Boghaert ER, Ackler SL, Catron ND, Chen J, et al. ABT-199, a potent and selective BCL-2 inhibitor, achieves antitumor activity while sparing platelets. Nat Med 2013;19:202-8.
47. Tao ZF, Hasvold L, Wang L, Wang X, Petros AM, Park CH, et al. Discovery of a potent and selective BCL-XL inhibitor with in vivo activity. ACS Med Chem Lett 2014;5:1088-93.