Mechanistic role of heat shock protein 70 in Bcr-Abl-mediated resistance to apoptosis in human acute leukemia cells

Blood

Volumn 105, Issue 3, 2005, Pages 1246-1255

  Guo, Fei ^a   Sigua, Celia ^a   Bali, Purva ^a   George, Prince ^a   Fiskus, Warren ^a   Scuto, Anna ^a   Annavarapu, Srinivas ^a   Mouttaki, Abdelmoughite ^a   Sondarva, Gautam ^a   Wei, Sheng ^a   Wu, Jie ^a   Djeu, Julie ^a   Bhalla, Kapil ^a  

^a H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BCR ABL PROTEIN; CASPASE 3; CASPASE 9; COMPLEMENTARY DNA; CYTARABINE; CYTOCHROME C; DEATH RECEPTOR 4; DEATH RECEPTOR 5; ETOPOSIDE; HEAT SHOCK PROTEIN 70; IMATINIB; PROTEIN BCL XL; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; SERINE PROTEINASE OMI; STAT5 PROTEIN; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

ACUTE GRANULOCYTIC LEUKEMIA; APOPTOSIS; ARTICLE; AUTOPHOSPHORYLATION; CHRONIC MYELOID LEUKEMIA; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DNA BINDING; DRUG INHIBITION; DRUG MECHANISM; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; LEUKEMIA CELL; MITOCHONDRION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN EXPRESSION; REGULATORY MECHANISM;

EID: 19944433616     PISSN: 00064971     EISSN: None     Source Type: Journal    
DOI: 10.1182/blood-2004-05-2041     Document Type: Article

References (64)

1. Thijsen SFT, Schuurhuis GJ, van Oostveen JW, Ossenkoppele GJ. Chronic myeloid leukemia from basic to bedside. Leukemia. 1999;13:1646-1674.
2. Deininger M, Goldman J, Melo J. The molecular biology of chronic myeloid leukemia. Blood. 2000;96:3343-3356.
3. Bedi A, Barber JP, Bedi GC, et al. BCR-ABL-mediated inhibition of apoptosis by delay of G2/M transition following DNA damage: a mechanism of resistance to multiple anticancer agents. Blood. 1995;86:1148-1158.
4. Amarante-Mendes G, Kim C, Liu L, et al. Bcr-Abl exerts its anti-apoptotic effect against diverse stimuli through blockage of mitochondrial release of cytochrome c and activation of caspase-3. Blood. 1998;91:1700-1705.
5. Ramadevi N, Porosnicu M, Nguyen D, et al. Co-treatment with STI-571 enhances TNFα related apoptosis inducing ligand (TRAIL or Apo-2L)-induced apoptosis of Bcr-Abl-positive human acute leukemia cells. Clin Cancer Res. 2001;7: 350-357.
6. Nimmanapalli R, Bhalla K. Mechanisms of resistance to imatinib mesylate (Gleevec) in Bcr-Abl positive leukemias. Curr Opin Oncol. 2002;6:616-620.
7. Sillaber C, Gesbert F, Frank D, Sattler M, Griffin J. STAT5 activation contributes to growth and viability in Bcr/Abl-transformed cells. Blood. 2000;95:2118-2125.
8. Gesbert F, Griffin JD. BCR-ABL activates transcription of the BCL-X gene through STAT5. Blood. 2000;96:2269-2276.
9. Fox CJ, Hammerman PS, Cinalli RM, Master SR, Chodosh LA, Thompson CB. The serine/threonine kinase Pim-2 is a transcriptionally regulated apoptotic inhibitor. Genes Dev. 2003;17:1841-1854.
10. Skorski T, Bellacosa A, Nieborowska-Skorska M, et al. Transformation of hematopoietic cells by BCR/ABL requires activation of a Pl-3k/Akt-dependent pathway. EMBO J. 1997;16:6151-6161.
11. Neshat M, Raitano A, Wang H, Reed J, Sawyers C. The survival function of the Bcr-Abl oncogene is mediated by Bad-dependent and -independent pathways: roles for phosphatidylinositol 3-kinase and Raf. Mol Cell Biol. 2000;20:1179-1186.
12. Datta SR, Brunet A, Greenberg ME. Cellular survival: a play of three Akts. Genes Dev. 1999;13:2905-2927.
13. Buchdunger E, Zimmermann J, Mett H, et al. Inhibition of the Abl protein-tyrosine kinase in vitro and in vivo by a 2-phenylaminopyrimidine derivative. Cancer Res. 1996;56:100-104.
14. Druker BJ, Tamura S, Buchdunger E, et al. Effects of a selective inhibitor of the Abl tyrosine kinase on the growth of Bcr-Abl-positive cells. Nat Med. 1996;2:561-566.
15. Deininger MWN, Goldman JM, Lydon N, Melo JV. The tyrosine kinase inhibitor CGP57148B selectively inhibits the growth of the BCR-ABL-positive cells. Blood. 1997;90:3691-3698.
16. Fang G, Kim C, Perkins C, et al. CGP57148 (STI-571) induces differentiation and apoptosis and sensitizes Bcr-Abl-positive human leukemia cells to apoptosis due to antileukemic drugs. Blood. 2000;96:2246-2256.
17. Thiesing J, Ohno-Jones S, Kolibaba K, Druker B. Efficacy of STI571, an Abl tyrosine kinase inhibitor, in conjunction with other antileukemic agents against Bcr-Abl-positive cells. Blood. 2000;96:3195-3199.
18. Kano Y, Akutsu M, Tsunoda S, et al. In vitro cytotoxic effects of a tyrosine kinase inhibitor STI571 in combination with commonly used antileukemic agents. Blood. 2001;97:1999-2007.
19. Druker BJ. Perspectives on the development of a molecularly targeted agent. Cancer Cell. 2002;1:31-36.
20. Savage DG, Antman KH. Imatinib mesylate - a new oral targeted therapy. N Engl J Med. 2002;28:689-6932.
21. Nimmanapalli R, O'Bryan E, Huang M. Molecular characterization and sensitivity of STI-571 (imatinib mesylate, Gleevec)-resistant, Bcr-Abl-positive, human acute leukemia cells retain sensitivity to SRC kinase inhibitor PD180970and 17-allylamino-17-demethoxy-geldanamycin (17-AAG). Cancer Res. 2002;62:5761-5769.
22. Wickner S, Maurizi MR, Gottesman S. Posttranslational quality control: folding, refolding, and degrading proteins. Science. 1999;286:1888-1893.
23. McClellan AJ, Frydman J. Molecular chaperones and the art of recognizing a lost cause. Nat Cell Biol. 2001;3:E1-E3.
24. Hartl FU, Hayer-Hartl M. Molecular chaperones in the cytosol: from nascent chain to folded protein. Science. 2002;295:1852-1858.
25. Volloch VZ, Sherman MY. Oncogenic potential of Hsp72. Oncogene. 1999;18:3648-3651.
26. Jaattela M. Over-expression of hsp70 confers tumorigenicity to mouse fibrosarcoma cells. Int J Cancer. 1995;60:689-693.
27. Seo JS, Park YM, Kim JI, et al. T cell lymphoma in transgenic mice expressing the human Hsp70 gene. Biochem Biophys Res Commun. 1996;218:582-587.
28. Creagh EM, Sheehan D, Cotter TG. Heat shock proteins - modulators of apoptosis in tumour cells. Leukemia. 2000;14:1161-1173.
29. Takayama S, Reed JC, Homma S. Heat-shock proteins as regulators of apoptosis. Oncogene. 2003;22:9041-9047.
30. Gabai VL, Mabuchi K, Mosser DD, Sherman MY. Hsp72 and stress kinase c-jun N-terminal kinase regulate the bid-dependent pathway in tumor necrosis factor-induced apoptosis. Mol Cell Biol. 2002;22:3415-3424.
31. Saleh A, Srinivasula SM, Balkir L, Robbins PD, Alnemri ES. Negative regulation of the Apaf-1 apoptosome by Hsp70. Nat Cell Biol. 2000;2:476-483.
32. Beere HM, Wolf BB, Cain K, et al. Heat-shock protein 70 inhibits apoptosis by preventing recruitment of procaspase-9 to the Apaf-1 apoptosome. Nat Cell Biol. 2000;2:469-475.
33. Jaattela M, Wissing D, Kokholm K, Kallunki T, Egeblad M. Hsp70 exerts its anti-apoptotic function downstream of caspase-3-like proteases. EMBO J. 1998;17:6124-6134.
34. Ravagnan L, Gurbuxani S, Susin SA, et al. Heatshock protein 70 antagonizes apoptosis-inducing factor. Nat Cell Biol. 2001;3:839-843.
35. Gurbuxani S, Schmitt E, Cande C, et al. Heat shock protein 70 binding inhibits the nuclear import of apoptosis-inducing factor. Oncogene. 2003;22:6669-6678.
36. Nylandsted J, Rohde M, Brand K, Bastholm L, Elling F, Jaattela M. Selective depletion of heat shock protein 70 (Hsp70) activates a tumor-specific death program that is independent of caspases and bypasses Bcl-2. Proc Natl Acad Sci U S A. 2000;97:7871-7876.
37. Nylandsted J, Wick W, Hirt UA, et al. Eradication of glioblastoma and breast and colon carcinoma xenografts by Hsp70 depletion. Cancer Res. 2002;62:7139-7142.
38. Guo F, Nimmanapalli R, Paranawithana S, et al. Ectopic overexpression of second mitochondrial-derived activator of caspases (Smac/DIABLO) or co-treatment with N-terminus of Smac peptide potentiates Epothilone derivative (BMS 247550) and Apo-2L/TRAIL-induced apoptosis. Blood. 2002;99:3419-3426.
39. Mukhopadhyay A, Shishodia S. Suttles J. et al. Ectopic expression of protein tyrosine kinase Bcr-Abl suppresses TNF-induced MF-kappa 8 activation and Ikappa Balpha phosphorylation: relationship with downregulation of TNF receptors. J Biol Chem. 2002;277:30622-30628.
40. Wittmann S, Bali P, Donapaty S, et al. Flavopiridol downregulates antiapoptotic proteins and sensitizes human breast cancer cells to epothilone B-induced apoptosis. Cancer Res. 2003;63:93-99.
41. Nimmanapalli R, Fuino L, Bali P, et al. Histone deacetylase inhibitor LAQ824 both lowers expression and promotes proteasomal degradation of Bcr-Abl and induces apoptosis of imatinib mesylate-sensitive or -refractory chronic myelogenous leukemia-blast crisis cells. Cancer Res. 2003;63:5126-5135.
42. Yamaguchi H, Paranawithana S, Lee M, Huang Z, Bhalla K, Wang HG. Epothilone B analogue (BMS247550)-mediated cytotoxicity through induction of Bax conformational change in human breast cancer cells. Cancer Res. 2002;62:466-471.
43. Guo F, Sigua C, Tao J, et al. Cotreatment with histone deacetylase inhibitor LAQ824 enhances Apo-2L/tumor necrosis factor-related apoptosis inducing ligand-induced death inducing signaling complex activity and apoptosis of human acute leukemia cells. Cancer Res. 2004;64:2580-2589.
44. Wei S, Gilvary DL, Corliss BC, et al. Direct tumor lysis by NK cells uses a Ras-independent mitogen-activated protein kinase signal pathway. J Immunol. 2000;165:3811-3819.
45. Takayama S, Sato T, Krajewski S, et al. Cloning and functional analysis of BAG-1: a novel Bcl-2-binding protein with anti-cell death activity. Cell. 1995;80:279-284.
46. Nollen EA, Kabakov AE, Brunsting JF, Kanon B. Hohfeld J, Kampinga HH. Modulation of in vivo HSP70 chaperone activity by Hip and Bag-1. J Biol Chem. 2001;276:4677-4682.
47. Zou J, Quo Y, Guettouche T, Smith DF, Voellmy R. Repression of heat shock transcription factor HSF1 activation by HSP90 (HSP90 complex) that forms a stress-sensitive complex with HSF1. Cell. 1998;94:471-480.
48. Morimoto RI. Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev. 1998;12:3788-3796.
49. Fox CJ, Hammerman PS, Cinalli RM, Master SR, Chodosh LA, Thompson CB. The serine/threonine kinase Pim-2 is a transcriptionally regulated apoptotic inhibitor. Genes Dev. 2003;17:1841-1854.
50. Gross A, McDonnell J, Korsmeyer S. Bcl-2 family members and the mitochondria in apoptosis. Genes Dev. 1999;13:1899-1911.
51. Wang X. The expanding role of mitochondria in apoptosis. Genes Dev. 2001;15:2922-2933.
52. Newmeyer DD, Ferguson-Miller S. Mitochondria: releasing power for life and unleashing the machineries of death. Cell. 2003;112:481-490.
53. Yamaguchi H, Bhalla K, Wang HG. Bax plays a pivotal role in thapsigargin-induced apoptosis of human colon cancer cells by controlling Smac/Diablo and Omi/HtrA2 release from mitochondria. Cancer Res. 2003;63:1483-1489.
54. Gotoh T, Terada K, Oyadomari S, Mori M. hsp70-DnaJ chaperone pair prevents nitric oxide- and CHOP-induced apoptosis by inhibiting translocation of Bax to mitochondria. Cell Death Differ. 2004;11:390-402.
55. Dorsey JF, Cunnick JM, Lanehart R, et al. Interleukin-3 protects Bcr-Abl-transformed hematopoietic progenitor cells from apoptosis induced by Bcr-Abl tyrosine kinase inhibitors. Leukemia. 2002;16:1589-1595.
56. Mizuki M, Schwäble J, Steur C, et al. Suppression of myeloid transcription factors and induction of STAT response genes by AML-specific Flt3 mutations. Blood. 2003;101:3164-3173.
57. Cotto JJ, Kline M, Morimoto RI. Activation of heat shock factor 1 DNA binding precedes stress-induced serine phosphorylation. J Biol Chem. 1996;271:3355-3358.
58. Wang S, El-Deiry WS. TRAIL and apoptosis induction by TNF-family death receptors. Oncogene. 2003;22:8628-8633.
59. Scaffidi C, Fulda S, Srinivasan A, et al. Two CD95 (Apo-1/Fas) signaling pathways. EMBO J. 1998;17:1675-1687.
60. Deng Y, Ren X, Yang L, Lin Y, Wu X. A JNK-dependent pathway is required for TNFalpha-induced apoptosis. Cell. 2003;115:61-70.
61. Park HS, Lee JS, Huh SH, Seo JS, Choi EJ. Hsp72 functions as a natural inhibitory protein of c-Jun N-terminal kinase. EMBO J. 2001;20:446-456.
62. Mosser DD, Caron AW, Bourget L, et al. The chaperone function of hsp70 is required for protection against stress-induced apoptosis. Mol Cell Biol. 2000;20:7146-7159.
63. Hatai T, Matsuzawa A, Inoshita S, et al. Execution of apoptosis signal-regulating kinase 1 (ASK1)-induced apoptosis by the mitochondria- dependent caspase activation. J Biol Chem. 2000;275: 26576-26581.
64. Park HS, Cho SG, Kim CK, et al. Heat shock protein hsp72 is a negative regulator of apoptosis signal-regulating kinase 1. Mol Cell Biol. 2002;22:7721-7730.