Selectively targeting Mcl-1 for the treatment of acute myelogenous leukemia and solid tumors

Genes and Development

Volumn 26, Issue 4, 2012, Pages 305-311

  Gores, Gregory J ^a   Kaufmann, Scott H ^a,b  

^a MAYO CLINIC   (United States)

^b MAYO GRADUATE SCHOOL   (United States)

Author keywords

Acute myeloid leukemia; Apoptosis; Bcl x L; Mcl 1

Indexed keywords

ANTILEUKEMIC AGENT; CASPASE 9; CRE RECOMBINASE; FLAVOPIRIDOL; GLYCOGEN SYNTHASE KINASE 3; N [5 (5 TERT BUTYL 2 OXAZOLYLMETHYLTHIO) 2 THIAZOLYL]ISONIPECOTAMIDE; NAVITOCLAX; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN BID; PROTEIN MCL 1; PROTEIN NOXA; SORAFENIB; STAT3 PROTEIN; UNCLASSIFIED DRUG; WP 1130;

ACUTE GRANULOCYTIC LEUKEMIA; APOPTOSIS; ARTICLE; CANCER SURVIVAL; CHRONIC MYELOID LEUKEMIA; DEPHOSPHORYLATION; DOWN REGULATION; HALF LIFE TIME; HEMATOPOIETIC CELL; HUMAN; KIDNEY CARCINOMA; LEUKEMIA CELL; LIVER CELL CARCINOMA; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; RISK BENEFIT ANALYSIS; SEQUENCE HOMOLOGY; SOLID TUMOR; SOMATIC CELL; STRUCTURE ACTIVITY RELATION; UPREGULATION;

ANIMALS; HUMANS; LEUKEMIA, MYELOID, ACUTE; PROTO-ONCOGENE PROTEINS C-BCL-2;

EID: 84857168377     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.186189.111     Document Type: Article

References (46)

1. Alavian KN, Li H, Collis L, Bonanni L, Zeng L, Sacchetti S, Lazrove E, Nabili P, Flaherty B, Graham M, et al. 2011. Bcl-xL regulates metabolic efficiency of neurons through interaction with the mitochondrial F1FO ATP synthase. Nat Cell Biol 13: 1224-1233.
2. Beroukhim R, Mermel CH, Porter D, Wei G, Raychaudhuri S, Donovan J, Barretina J, Boehm JS, Dobson J, Urashima M, et al. 2010. The landscape of somatic copy-number alteration across human cancers. Nature 463: 899-905.
3. Cheng EH, Wei MC, Weiler S, Flavell RA, Mak TW, Lindsten T, Korsmeyer SJ. 2001. BCL-2, BCL-X(L) sequester BH3 domain-only molecules preventing BAX- and BAK-mediated mito-chondrial apoptosis. Mol Cell 8: 705-711.
4. Craig RW. 2002. MCL1 provides a window on the role of the BCL2 family in cell proliferation, differentiation and tumor-igenesis. Leukemia 16: 444-454.
5. Dai Y, Grant S. 2007. Targeting multiple arms of the apoptotic regulatory machinery. Cancer Res 67: 2908-2911.
6. Dai H, Smith A, Meng XW, Schneider PA, Pang Y-P, Kaufmann SH. 2011. Transient binding of an activator BH3 domain to the Bak BH3-binding groove initiates Bak oligomerization. J Cell Biol 194: 39-48.
7. De Biasio A, Vrana JA, Zhou P, Qian L, Bieszczad CK, Braley KE, Domina AM, Weintraub SJ, Neveu JM, Lane WS, et al. 2007. N-terminal truncation of antiapoptotic MCL1, but not G2/ M-induced phosphorylation, is associated with stabilization and abundant expression in tumor cells. J Biol Chem 282: 23919-23936.
8. Dewson G, Kratina T, Sim HW, Puthalakath H, Adams JM, Colman PM, Kluck RM. 2008. To trigger apoptosis, Bak exposes its BH3 domain and homodimerizes via BH3:groove interactions. Mol Cell 30: 369-380.
9. Ding Q, He X, Hsu JM, Xia W, Chen CT, Li LY, Lee DF, Liu JC, Zhong Q, Wang X, et al. 2007. Degradation of Mcl-1 by b-TrCP mediates glycogen synthase kinase 3-induced tumor suppression and chemosensitization. Mol Cell Biol 27: 4006-4017.
10. Fritsch RM, Schneider G, Saur D, Scheibel M, Schmid RM. 2007. Translational repression of MCL-1 couples stress-induced eIF2a phosphorylation to mitochondrial apoptosis initiation. J Biol Chem 282: 22551-22562.
11. Fröhling S, Scholl C, Gilliland DG, Levine RL. 2005. Genetics of myeloid malignancies: Pathogenetic and clinical implications. J Clin Oncol 23: 6285-6295.
12. Garzon R, Heaphy CE, Havelange V, Fabbri M, Volinia S, Tsao T, Zanesi N, Kornblau SM, Marcucci G, Calin GA, et al. 2009. MicroRNA 29b functions in acute myeloid leukemia. Blood 114: 5331-5341.
13. Gavathiotis E, Reyna DE, Davis ML, Bird GH, Walensky LD. 2010. BH3-triggered structural reorganization drives the activation of proapoptotic BAX. Mol Cell 40: 481-492.
14. Glaser SP, Lee EF, Trounson E, Bouillet P, Wei A, Fairlie WD, Izon DJ, Zuber J, Rappaport AR, Herold MJ, et al. 2012. Anti-apoptotic Mcl-1 is essential for the development and sustained growth of acute myeloid leukemia. Genes Dev 26: 120-125.
15. Huang CR, Yang-Yen HF. 2010. The fast-mobility isoform of mouse Mcl-1 is a mitochondrial matrix-localized protein with attenuated anti-apoptotic activity. FEBS Lett 584: 3323-3330.
16. Karp JE, Bauer KS, Passaniti A, Goji I, Kaufmann SH, Bible K, Greer J, Briel J, Tidwell ML, Ross DD, et al. 2005. Phase I study of timed sequential therapy of relapsed and refractory adult acute leukemias with flavopiridol followed by Ara-C and mitoxantrone. Clin Cancer Res 11: 8403-8412.
17. Karp JE, Smith BD, Resar LS, Greer JM, Blackford A, Zhao M, Moton-Nelson D, Alino K, Levis MJ, Gore SD, et al. 2011. Phase 1 and pharmacokinetic study of bolus-infusion flavo-piridol followed by cytosine arabinoside and mitoxantrone for acute leukemias. Blood 117: 3302-3310.
18. Kaufmann SH, Karp JE, Svingen PA, Krajewski S, Burke PJ, Gore SD. 1998. Elevated expression of the apoptotic regulator Mcl-1 at the time of leukemic relapse. Blood 91: 991-1000.
19. Kozopas KM, Yang T, Buchan HL, Zhou P, Craig RW. 1993. MCL1, a gene expressed in programmed myeloid cell differentiation, has sequence similarity to BCL-2. Proc Natl Acad Sci 90: 3516-3520.
20. Kvinlaug BT, Chan WI, Bullinger L, Ramaswami M, Sears C, Foster D, Lazic SE, Okabe R, Benner A, Lee BH, et al. 2011. Common and overlapping oncogenic pathways contribute to the evolution of acute myeloid leukemias. Cancer Res 71: 4117-4129.
21. Lee YK, Isham CR, Kaufmann SH, Bible KC. 2006. Flavopiridol disrupts STAT3/DNA interactions, attenuates STAT3-di-rected transcription and combines with the Jak kinase inhibitor AG490 to achieve cytotoxic synergy. Mol Cancer Ther 5: 138-148.
22. Liu H, Cheng EH, Hsieh JJ. 2009. MLL fusions: Pathways to leukemia. Cancer Biol Ther 8: 1204-1211.
23. Llambi F, Moldoveanu T, Tait SW, Bouchier-Hayes L, Temirov J, McCormick LL, Dillon CP, Green DR. 2011. A unified model of mammalian BCL-2 protein family interactions at the mitochondria. Mol Cell 44: 517-531.
24. Martinou JC, Youle RJ. 2011. Mitochondria in apoptosis: Bcl-2 family members and mitochondrial dynamics. Dev Cell 21: 92-101.
25. Mills JR, Hippo Y, Robert F, Chen SM, Malina A, Lin CJ, Trojahn U, Wendel HG, Charest A, Bronson RT, et al. 2008. Mtorc1 promotes survival through translational control of Mcl-1. Proc Natl Acad Sci 105: 10853-10858.
26. Mott JL, Kobayashi S, Bronk SF, Gores GJ. 2007. Mir-29 regulates Mcl-1 protein expression and apoptosis. Oncogene 26: 6133-6140.
27. Nguyen M, Marcellus RC, Roulston A, Watson M, Serfass L, Murthy Madiraju SR, Goulet D, Viallet J, Belec L, Billot X, et al. 2007. Small molecule obatoclax (GX15-070) antagonizes MCL-1 and overcomes MCL-1-mediated resistance to apoptosis. Proc Natl Acad Sci 104: 19512-19517.
28. Opferman JT. 2007. Life and death during hematopoietic differentiation. Curr Opin Immunol 19: 497-502.
29. Opferman JT, Iwasaki H, Ong CC, Suh H, Mizuno S, Akashi K, Korsmeyer SJ. 2005. Obligate role of anti-apoptotic MCL-1 in the survival of hematopoietic stem cells. Science 307: 1101- 1104.
30. Placzek WJ, Wei J, Kitada S, Zhai D, Reed JC, Pellecchia M. 2010. A survey of the anti-apoptotic Bcl-2 subfamily expression in cancer types provides a platform to predict the efficacy of Bcl-2 antagonists in cancer therapy. Cell Death Dis 1: e40. doi: 10.1038/cddis.2010.18.
31. Pratz KW, Cho E, Levis MJ, Karp JE, Gore SD, McDevitt M, Stine A, Zhao M, Baker SD, Carducci MA, et al. 2010. A pharmacodynamic study of sorafenib in patients with relapsed and refractory acute leukemias. Leukemia 24: 1437-1444.
32. Quinn BA, Dash R, Azab B, Sarkar S, Das SK, Kumar S, Oyesanya RA, Dasgupta S, Dent P, Grant S, et al. 2011. Targeting Mcl-1 for the therapy of cancer. Expert Opin Investig Drugs 20: 1397-1411.
33. Ravandi F, Cortes JE, Jones D, Faderl S, Garcia-Manero G, Konopleva MY, O'Brien S, Estrov Z, Borthakur G, Thomas D, et al. 2010. Phase I/II study of combination therapy with sorafenib, idarubicin, and cytarabine in younger patients with acute myeloid leukemia. J Clin Oncol 28: 1856-1862.
34. Schimmer AD, Pedersen IM, Kitada S, Eksioglu-Demiralp E, Minden MD, Pinto R, Mah K, Andreeff M, Kim Y, Suh WS, et al. 2003. Functional blocks in caspase activation pathways are common in leukemia and predict patient response to induction chemotherapy. Cancer Res 63: 1242-1248.
35. Schwickart M, Huang X, Lill JR, Liu J, Ferrando R, French DM, Maecker H, O'Rourke K, Bazan F, Eastham-Anderson J, et al. 2010. Deubiquitinase USP9X stabilizes MCL1 and promotes tumour cell survival. Nature 463: 103-107.
36. Stewart ML, Fire E, Keating AE, Walensky LD. 2010. The MCL-1 BH3 helix is an exclusive MCL-1 inhibitor and apoptosis sensitizer. Nat Chem Biol 6: 595-601.
37. Strasser A, Cory S, Adams JM. 2011. Deciphering the rules of programmed cell death to improve therapy of cancer and other diseases. EMBO J 30: 3667-3683.
38. Sun H, Kapuria V, Peterson LF, Fang D, Bornmann WG, Bartholomeusz G, Talpaz M, Donato NJ. 2011. Bcr-Abl ubiquitination and Usp9x inhibition block kinase signaling and promote CML cell apoptosis. Blood 117: 3151-3162.
39. Taniai M, Grambihler A, Higuchi H, Werneburg N, Bronk SF, Farrugia DJ, Kaufmann SH, Gores GJ. 2004. Mcl-1 mediates tumor necrosis factor-related apoptosis-inducing ligand resistance in human cholangiocarcinoma cells. Cancer Res 64: 3517-3524.
40. Vaux DL, Cory S, Adams JM. 1988. Bcl-2 gene promotes haemo-poietic cell survival and cooperates with c-myc to immortalize pre-B cells. Nature 335: 440-442.
41. Walensky LD. 2011. From mitochondrial biology to magic bullet: Navitoclax disarms BCL-2 in chronic lymphocytic leukemia. J Clin Oncol doi: 10.1200/JCO.2011.37.9339.
42. Warr MR, Shore GC. 2008. Unique biology of Mcl-1: Therapeutic opportunities in cancer. Curr Mol Med 8: 138-147.
43. Warr MR, Mills JR, Nguyen M, Lemaire-Ewing S, Baardsnes J, Sun KL, Malina A, Young JC, Jeyaraju DV, O'Connor-McCourt M, et al. 2011. Mitochondrion-dependent N-termi-nal processing of outer membrane Mcl-1 protein removes an essential Mule/Lasu1 protein-binding site. J Biol Chem 286: 25098-25107.
44. Wertz IE, Kusam S, Lam C, Okamoto T, Sandoval W, Anderson DJ, Helgason E, Ernst JA, Eby M, Liu J, et al. 2011. Sensitivity to antitubulin chemotherapeutics is regulated by MCL1 and FBW7. Nature 471: 110-114.
45. Yan N, Shi Y. 2005. Mechanisms of apoptosis through structural biology. Annu Rev Cell Dev Biol 21: 35-56.
46. Zhong Q, Gao W, Du F, Wang X. 2005. Mule/ARF-BP1, a BH3-only E3 ubiquitin ligase, catalyzes the polyubiquitination of Mcl-1 and regulates apoptosis. Cell 121: 1085-1095.