The BH3-only protein Bim plays a critical role in leukemia cell death triggered by concomitant inhibition of the PI3K/Akt and MEK/ERK1/2 pathways

Blood

Volumn 114, Issue 20, 2009, Pages 4507-4516

  Rahmani, Mohamed ^a   Anderson, Anh ^a   Habibi, Joseph Reza ^a   Crabtree, Timothy Ryan ^a   Mayo, Mandy ^a   Harada, Hisashi ^a   Ferreira Gonzalez, Andrea ^b   Dent, Paul ^b   Grant, Steven ^a,b  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2 CHLORO 4 IODOANILINO) N CYCLOPROPYLMETHOXY 3,4 DIFLUOROBENZAMIDE; BH3 PROTEIN; BIM PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; PERIFOSINE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BAK; PROTEIN MCL 1; SMALL INTERFERING RNA; UO 126; APOPTOSIS REGULATORY PROTEIN; BAD PROTEIN, HUMAN; BCL 2 LIKE PROTEIN 11; BCL-2-LIKE PROTEIN 11; ENZYME INHIBITOR; MEMBRANE PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; MYELOID CELL LEUKEMIA SEQUENCE 1 PROTEIN; ONCOPROTEIN; PROTEIN BAD; PROTEIN BCL 2; PROTEIN KINASE B;

ACUTE MYELOBLASTIC LEUKEMIA; APOPTOSIS; ARTICLE; CD34 SELECTION; CELL DEATH; CONFORMATIONAL TRANSITION; DOWN REGULATION; HEMATOPOIETIC CELL; HUMAN; HUMAN CELL; LEUKEMIA CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UPREGULATION; DRUG EFFECT; IMMUNOBLOTTING; IMMUNOPRECIPITATION; LEUKEMIA; METABOLISM; NUCLEOTIDE SEQUENCE; PATHOLOGY; PHYSIOLOGY;

1-PHOSPHATIDYLINOSITOL 3-KINASE; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BCL-ASSOCIATED DEATH PROTEIN; DNA MUTATIONAL ANALYSIS; ENZYME INHIBITORS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; LEUKEMIA; MAP KINASE KINASE KINASES; MEMBRANE PROTEINS; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-BCL-2; SIGNAL TRANSDUCTION;

EID: 73349137309     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2008-09-177881     Document Type: Article

References (55)

1. Stommel JM, Kimmelman AC, Ying H, et al. Coactivation of receptor tyrosine kinases affects the response of tumor cells to targeted therapies. Science. 2007;318:287-290.
2. Marone R, Cmiljanovic V, Giese B, Wymann MP. Targeting phosphoinositide 3-kinase: moving towards therapy. Biochim Biophys Acta. 2008;1784: 159-185.
3. Schubbert S, Shannon K, Bollag G. Hyperactive Ras in developmental disorders and cancer. Nat Rev Cancer. 2007;7:295-308.
4. She QB, Solit DB, Ye Q, O'Reilly KE, Lobo J, Rosen N. The BAD protein integrates survival signaling by EGFR/MAPK and PI3K/Akt kinase pathways in PTEN-deficient tumor cells. Cancer Cell. 2005;8:287-297.
5. Lambert PJ, Shahrier AZ, Whitman AG, et al. Targeting the PI3K and MAPK pathways to treat Kaposi's-sarcoma-associated herpes virus infection and pathogenesis. Expert Opin Ther Targets. 2007;11:589-599.
6. McCubrey JA, Steelman LS, Abrams SL, et al. Roles of the RAF/MEK/ERK and PI3K/PTEN/AKT pathways in malignant transformation and drug resistance. Adv Enzyme Regul. 2006;46:249-279.
7. Xia Z, Dickens M, Raingeaud J, Davis RJ, Greenberg ME. Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science. 1995;270:1326-1331.
8. Tai YT, Fulciniti M, Hideshima T, et al. Targeting MEK induces myeloma-cell cytotoxicity and inhibits osteoclastogenesis. Blood. 2007;110:1656-1663.
9. Dijkers PF, Medema RH, Lammers JW, Koenderman L, Coffer PJ. Expression of the proapoptotic Bcl-2 family member Bim is regulated by the forkhead transcription factor FKHR-L1. Curr Biol. 2000;10:1201-1204.
10. Hilgard P, Klenner T, Stekar J, Nossner G, Kutscher B, Engel J. D-21266, a new heterocyclic alkylphospholipid with antitumor activity. Eur J Cancer. 1997;33:442-446.
11. Hideshima T, Catley L, Yasui H, et al. Perifosine, an oral bioactive novel alkylphospholipid, inhibits Akt and induces in vitro and in vivo cytotoxicity in human multiple myeloma cells. Blood. 2006;107: 4053-4062.
12. LoPiccolo J, Blumenthal GM, Bernstein WB, Dennis PA. Targeting the PI3K/Akt/mTOR pathway: effective combinations and clinical considerations. Drug Resist Updat. 2008;11:32-50.
13. Kondapaka SB, Singh SS, Dasmahapatra GP, Sausville EA, Roy KK. Perifosine, a novel alkylphospholipid, inhibits protein kinase B activation. Mol Cancer Ther. 2003;2:1093-1103.
14. Rahmani M, Reese E, Dai Y, et al. Coadministration of histone deacetylase inhibitors and perifosine synergistically induces apoptosis in human leukemia cells through Akt and ERK1/2 inactivation and the generation of ceramide and reactive oxygen species. Cancer Res. 2005;65:2422-2432.
15. Dong S, Kang S, Gu TL, et al. 14-3-3 Integrates prosurvival signals mediated by the AKT and MAPK pathways in ZNF198-FGFR1-transformed hematopoietic cells. Blood. 2007;110:360-369.
16. Rahmani M, Yu C, Reese E, et al. Inhibition of PI-3 kinase sensitizes human leukemic cells to histone deacetylase inhibitor-mediated apoptosis through p44/42 MAP kinase inactivation and abrogation of p21(CIP1/WAF1) induction rather than AKT inhibition. Oncogene. 2003;22:6231-6242.
17. Harada H, Quearry B, Ruiz-Vela A, Korsmeyer SJ. Survival factor-induced extracellular signal-regulated kinase phosphorylates BIM, inhibiting its association with BAX and proapoptotic activity. Proc Natl Acad Sci U S A. 2004;101:15313-15317.
18. Rahmani M, Davis EM, Bauer C, Dent P, Grant S. Apoptosis induced by the kinase inhibitor BAY 43-9006 in human leukemia cells involves down-regulation of Mcl-1 through inhibition of translation. J Biol Chem. 2005;280:35217-35227.
19. + human leukemia cells in association with signal transducer and activator of transcription 5 inhibition and myeloid cell leukemia-1 down-regulation. Mol Pharmacol. 2007;72:788-795.
20. Guzman ML, Li X, Corbett CA, et al. Rapid and selective death of leukemia stem and progenitor cells induced by the compound 4-benzyl, 2-methyl, 1,2,4-thiadiazolidine, 3,5 dione (TDZD-8). Blood. 2007;110:4436-4444.
21. Ogino S, Kawasaki T, Brahmandam M, et al. Sensitive sequencing method for KRAS mutation detection by Pyrosequencing. J Mol Diagn. 2005;7: 413-421.
22. Ogino S, Nosho K, Kirkner GJ, et al. PIK3CA mutation is associated with poor prognosis among patients with curatively resected colon cancer. J Clin Oncol. 2009;27:1477-1484.
23. Shoji K, Oda K, Nakagawa S, et al. The oncogenic mutation in the pleckstrin homology domain of AKT1 in endometrial carcinomas. Br J Cancer. 2009;101:145-148.
24. Geyer JT, López-García MA, Sánchez-Estevez C, et al. Pathogenetic pathways in ovarian endometrioid adenocarcinoma: a molecular study of 29 cases. Am J Surg Pathol. 2009;33:1157-1163.
25. Dai Y, Yu C, Singh V, et al. Pharmacological inhibitors of the mitogen-activated protein kinase (MAPK) kinase/MAPK cascade interact synergistically with UCN-01 to induce mitochondrial dysfunction and apoptosis in human leukemia cells. Cancer Res. 2001;61:5106-5115.
26. Rahmani M, Davis EM, Crabtree TR, et al. The kinase inhibitor sorafenib induces cell death through a process involving induction of endoplasmic reticulum stress. Mol Cell Biol. 2007;27: 5499-5513.
27. Rahmani M, Dai Y, Grant S. The histone deacetylase inhibitor sodium butyrate interacts synergistically with phorbol myristate acetate (PMA) to induce mitochondrial damage and apoptosis in human myeloid leukemia cells through a tumor necrosis factor-α-mediated process. Exp Cell Res. 2002;277:31-47.
28. Chou TC, Talalay P. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv Enzyme Regul. 1984;22:27-55.
29. De Siervi A, Marinissen M, Diggs J, Wang XF, Pages G, Senderowicz A. Transcriptional activation of p21(waf1/cip1) by alkylphospholipids: role of the mitogen-activated protein kinase pathway in the transactivation of the human p21(waf1/ cip1) promoter by Sp1. Cancer Res. 2004;64: 743-750.
30. Murphy KM, Streips UN, Lock RB. Bcl-2 inhibits a Fas-induced conformational change in the Bax N terminus and Bax mitochondrial translocation. J Biol Chem. 2000;275:17225-17228.
31. Wolter KG, Hsu YT, Smith CL, Nechushtan A, Xi XG, Youle RJ. Movement of Bax from the cytosol to mitochondria during apoptosis. J Cell Biol. 1997;139:1281-1292.
32. Derenne S, Monia B, Dean NM, et al. Antisense strategy shows that Mcl-1 rather than Bcl-2 or Bcl-xL is an essential survival protein of human myeloma cells. Blood. 2002;100:194-199.
33. Moulding DA, Giles RV, Spiller DG, White MR, Tidd DM, Edwards SW. Apoptosis is rapidly triggered by antisense depletion of MCL-1 in differentiating U937 cells. Blood. 2000;96:1756-1763.
34. Weng C, Li Y, Xu D, Shi Y, Tang H. Specific cleavage of Mcl-1 by caspase-3 in tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)-induced apoptosis in Jurkat leukemia T cells. J Biol Chem. 2005;280:10491-10500.
35. Carracedo A, Ma L, Teruya-Feldstein J, et al. Inhibition of mTORC1 leads to MAPK pathway activation through a PI3K-dependent feedback loop in human cancer. J Clin Invest. 2008;118:3065-3074.
36. Konopleva M, Contractor R, Tsao T, et al. Mechanisms of apoptosis sensitivity and resistance to the BH3 mimetic ABT-737 in acute myeloid leukemia. Cancer Cell. 2006;10:375-388.
37. Domina AM, Vrana JA, Gregory MA, Hann SR, Craig RW. MCL1 is phosphorylated in the PEST region and stabilized upon ERK activation in viable cells, and at additional sites with cytotoxic okadaic acid or taxol. Oncogene. 2004;23:5301-5315.
38. Maurer U, Charvet C, Wagman AS, Dejardin E, Green DR. Glycogen synthase kinase-3 regulates mitochondrial outer membrane permeabilization and apoptosis by destabilization of MCL-1. Mol Cell. 2006;21:749-760.
39. Nijhawan D, Fang M, Traer E, et al. Elimination of Mcl-1 is required for the initiation of apoptosis following ultraviolet irradiation. Genes Dev. 2003;17: 1475-1486.
40. Adams JM, Cory S. The Bcl-2 apoptotic switch in cancer development and therapy. Oncogene. 2007;26:1324-1337.
41. Gomez-Bougie P, Bataille R, Amiot M. Endogenous association of Bim BH3-only protein with Mcl-1, Bcl-xL and Bcl-2 on mitochondria in human B cells. Eur J Immunol. 2005;35:971-976.
42. Han J, Goldstein LA, Gastman BR, Froelich CJ, Yin XM, Rabinowich H. Degradation of Mcl-1 by granzyme B: implications for Bim-mediated mitochondrial apoptotic events. J Biol Chem. 2004; 279:22020-22029.
43. Shimazu T, Degenhardt K, Nur-E-Kamal, et al. NBK/BIK antagonizes MCL-1 and BCL-XL and activates BAK-mediated apoptosis in response to protein synthesis inhibition. Genes Dev. 2007;21: 929-941.
44. Reginato MJ, Mills KR, Paulus JK, et al. Integrins and EGFR coordinately regulate the pro-apoptotic protein Bim to prevent anoikis. Nat Cell Biol. 2003;5:733-740.
45. Weston CR, Balmanno K, Chalmers C, et al. Activation of ERK1/2 by Raf-1:ER* represses Bim expression independently of the JNK or PI3K pathways. Oncogene. 2003;22:1281-1293.
46. Ewings KE, Hadfield-Moorhouse K, Wiggins CM, et al. ERK1/2-dependent phosphorylation of BimEL promotes its rapid dissociation from Mcl-1 and Bcl-xL. EMBO J. 2007;26:2856-2867.
47. Qi XJ, Wildey GM, Howe PH. Evidence that Ser87 of BimEL is phosphorylated by Akt and regulates BimEL apoptotic function. J Biol Chem. 2006;281:813-823.
48. Willis SN, Fletcher JI, Kaufmann T, et al. Apoptosis initiated when BH3 ligands engage multiple Bcl-2 homologs, not Bax or Bak. Science. 2007; 315:856-859.
49. Chen L, Willis SN, Wei A, et al. Differential targeting of prosurvival Bcl-2 proteins by their BH3-only ligands allows complementary apoptotic function. Mol Cell. 2005;17:393-403.
50. Willis SN, Adams JM. Life in the balance: how BH3-only proteins induce apoptosis. Curr Opin Cell Biol. 2005;17:617-625.
51. Kuwana T, Bouchier-Hayes L, Chipuk JE, et al. BH3 domains of BH3-only proteins differentially regulate Bax-mediated mitochondrial membrane permeabilization both directly and indirectly. Mol Cell. 2005;17:525-535.
52. Kim H, Rafiuddin-Shah M, Tu HC, et al. Hierarchical regulation of mitochondrion-dependent apoptosis by BCL-2 subfamilies. Nat Cell Biol. 2006; 8:1348-1358.
53. Willis SN, Chen L, Dewson G, 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;19:1294-1305.
54. Birkenkamp KU, Geugien M, Schepers H, Westra J, Lemmink HH, Vellenga E. Constitutive NF-κB DNA-binding activity in AML is frequently mediated by a Ras/PI3-K/PKB-dependent pathway. Leukemia. 2004;18:103-112.
55. Xu Q, Simpson SE, Scialla TJ, Bagg A, Carroll M. Survival of acute myeloid leukemia cells requires PI3 kinase activation. Blood. 2003;102:972-980.