TRAIL-induced apoptosis is enhanced by heat shock protein 70 expression

Cell Stress and Chaperones

Volumn 11, Issue 4, 2006, Pages 343-355

  Clemons, N J ^a,c   Anderson, R L ^a,b  

^a PETER MACCALLUM CANCER CENTRE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c HUTCHISON MRC RESEARCH CENTRE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DEATH RECEPTOR; FAS LIGAND; HEAT SHOCK PROTEIN 70; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; CASPASE; HEAT SHOCK PROTEIN 72; MESSENGER RNA; PROTEIN P53; TNFRSF10B PROTEIN, HUMAN; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND RECEPTOR; UNCLASSIFIED DRUG;

ANALYTIC METHOD; APOPTOSIS; ARTICLE; CHROMATIN; CONTROLLED STUDY; FLOW CYTOMETRY; GENE; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TRAIL-R2 GENE; UPREGULATION; GENETIC TRANSFECTION; GENETICS; METABOLISM; PHYSIOLOGY; TUMOR CELL LINE;

APOPTOSIS; CASPASES; CELL LINE, TUMOR; HSP72 HEAT-SHOCK PROTEINS; HUMANS; RECEPTORS, TNF-RELATED APOPTOSIS-INDUCING LIGAND; RNA, MESSENGER; SIGNAL TRANSDUCTION; TNF-RELATED APOPTOSIS-INDUCING LIGAND; TRANSFECTION; TUMOR SUPPRESSOR PROTEIN P53; UP-REGULATION;

EID: 33947585134     PISSN: 13558145     EISSN: 14661268     Source Type: Journal    
DOI: 10.1379/CSC-206.1     Document Type: Article

References (87)

1. Almasan A, Ashkenazi A. 2003. Apo2L/TRAIL: apoptosis signaling, biology, and potential for cancer therapy. Cytokine Growth Factor Rev 14: 337-348.
2. Arizono Y, Yoshikawa H, Naganuma H, Hamada Y, Nakajima Y, Tasaka K. 2003. A mechanism of resistance to TRAIL/Apo2L-induced apoptosis of newly established glioma cell line and sensitisation to TRAIL by genotoxic agents. Br J Cancer 88: 298-306.
3. Ashkenazi A. 2002. Targeting death and decoy receptors of the tumour-necrosis factor superfamily. Nat Rev Cancer 2: 420-430.
4. Ashkenazi A, Pai RC, Fong S, et al. 1999. Safety and antitumor activity of recombinant soluble Apo2 ligand. J Clin Invest 104: 155-162.
5. Athanassiadou P, Petrakakou E, Sakelariou V, Zerva C, Liossi A, Michalas S, Athanassiades P. 1998. Expression of p53, bcl-2 and heat shock protein (hsp72) in malignant and benign ovarian tumours. Eur J Cancer Prev 7: 225-231.
6. Bartek J, Iggo R, Gannon J, Lane DP. 1990. Genetic and immunochemical analysis of mutant p53 in human breast cancer cell lines. Oncogene 5: 893-899.
7. Beere HM, Wolf BB, Cain K, et al. 2000. Heat-shock protein 70 inhibits apoptosis by preventing recruitment of procaspase-9 to the Apaf-1 apoptosome. Nat Cell Biol 2: 469-475.
8. Bonavida B, Ng CP, Jazirehi A, Schiller G, Mizutani Y. 1999. Selectivity of TRAIL-mediated apoptosis of cancer cells and synergy with drugs: the trail to non-toxic cancer therapeutics (review). Int J Oncol 15: 793-802.
9. Buzzard KA, Giaccia AJ, Killender M, Anderson RL. 1998. Heat shock protein 72 modulates pathways of stress-induced apoptosis. J Biol Chem 273: 17147-17153.
10. Chant ID, Rose PE, Morris AG. 1995. Analysis of heat-shock protein expression in myeloid leukaemia cells by flow cytometry. Br J Haematol 90: 163-168.
11. Cheng J, Haas M. 1990. Frequent mutations in the p53 tumor suppressor gene in human leukemia T-cell lines. Mol Cell Biol 10: 5502-5509.
12. Chinnaiyan AM, Prasad U, Shankar S, et al. 2000. Combined effect of tumor necrosis factor-related apoptosis-inducing ligand and ionizing radiation in breast cancer therapy. Proc Natl Acad Sci USA 97: 1754-1759.
13. Ciocca DR, Clark GM, Tandon AK, Fuqua SA, Welch WJ, McGuire WL. 1993. Heat shock protein hsp70 in patients with axillary lymph node-negative breast cancer: prognostic implications. J Natl Cancer Inst 85: 570-574.
14. Clemons NJ, Buzzard K, Steel R, Anderson RL. 2005. Hsp72 inhibits Fas-mediated apoptosis upstream of the mitochondria in type II cells. J Biol Chem 280: 9005-9012.
15. Creagh EM, Sheehan D, Cotter TG. 2000. Heat shock proteins - modulators of apoptosis in tumour cells. Leukemia 14: 1161-1173.
16. Eskes R, Desagher S, Antonsson B, Martinou JC. 2000. Bid induces the oligomerization and insertion of Bax into the outer mitochondrial membrane. Mol Cell Biol 20: 929-935.
17. Furth EE, Thilly WG, Penman BW, Liber HL, Rand WM. 1981. Quantitative assay for mutation in diploid human lymphoblasts using microtiter plates. Anal Biochem 110: 1-8.
18. Gabai VL, Meriin AB, Mosser DD, Caron AW, Rits S, Shifrin VI, Sherman MY. 1997. Hsp70 prevents activation of stress kinases. A novel pathway of cellular thermotolerance. J Biol Chem 272: 18033-18037.
19. Gannon JV, Greaves R, Iggo R, Lane DP. 1990. Activating mutations in p53 produce a common conformational effect. A monoclonal antibody specific for the mutant form. EMBO J 9: 1595-1602.
20. Giaccia AJ, Kastan MB. 1998. The complexity of p53 modulation: emerging patterns from divergent signals. Genes Dev 12: 2973-2983.
21. Gliniak B, Le T. 1999. Tumor necrosis factor-related apoptosis-inducing ligand's antitumor activity in vivo is enhanced by the chemotherapeutic agent CPT-11. Cancer Res 59: 6153-6158.
22. Gotoh T, Terada K, Oyadomari S, Mori M. 2004. hsp70-DnaJ chaperone pair prevents nitric oxide- and CHOP-induced apoptosis by inhibiting translocation of Bax to mitochondria. Cell Death Differ 11: 390-402.
23. Green DR, Evan GI. 2002. A matter of life and death. Cancer Cell 1: 19-30.
24. Griffith TS, Rauch CT, Smolak PJ, et al. 1999. Functional analysis of TRAIL receptors using monoclonal antibodies. J Immunol 162: 2597-2605.
25. Guan B, Yue P, Clayman GL, Sun SY. 2001. Evidence that the death receptor DR4 is a DNA damage-inducible, p53-regulated gene. J Cell Physiol 188: 98-105.
26. Guo F, Sigua C, Bali P, et al. 2005. Mechanistic role of heat shock protein 70 in Bcr-Abl-mediated resistance to apoptosis in human acute leukemia cells. Blood 105: 1246-1255.
27. Hanahan D, Weinberg RA. 2000. The hallmarks of cancer. Cell 100: 57-70.
28. Hollstein M, Rice K, Greenblatt MS, et al. 1994. Database of p53 gene somatic mutations in human tumors and cell lines. Nucleic Acids Res 22: 3551-3555.
29. Hollstein M, Sidransky D, Vogelstein B, Harris CC. 1991. p53 mutations in human cancers. Science 253: 49-53.
30. L. Proc Natl Acad Sci USA 96: 14871-14876.
31. Huang DC, Tschopp J, Strasser A. 2000. Bcl-2 does not inhibit cell death induced by the physiological Fas ligand: implications for the existence of type I and type II cells. Cell Death Differ 7: 754-755.
32. Hussain SP, Harris CC. 1998. Molecular epidemiology of human cancer: contribution of mutation spectra studies of tumor suppressor genes. Cancer Res 58: 4023-4037.
33. Jaattela M. 1999. Escaping cell death: survival proteins in cancer. Exp Cell Res 248: 30-43.
34. Jaattela M, Wissing D, Bauer PA, Li GC. 1992. Major heat shock protein hsp70 protects tumor cells from tumor necrosis factor cytotoxicity. EMBO J 11: 3507-3512.
35. Jaattela M, Wissing D, Kokholm K, Kallunki T, Egeblad M. 1998. Hsp70 exerts its anti-apoptotic function downstream of caspase-3-like proteases. EMBO J 17: 6124-6134.
36. Jolly C, Morimoto RI. 2000. Role of the heat shock response and molecular chaperones in oncogenesis and cell death. J Natl Cancer Inst 92: 1564-1572.
37. Kelley SK, Harris LA, Xie D, Deforge L, Totpal K, Bussiere J, Fox JA. 2001. Preclinical studies to predict the disposition of Apo2L/tumor necrosis factor-related apoptosis-inducing ligand in humans: characterization of in vivo efficacy, pharmacokinetics, and safety. J Pharmacol Exp Ther 299: 31-38.
38. Kischkel F, Hellbardt S, Behrmann I, Germer M, Pawlita M, Krammer P, Peter M. 1995. Cytotoxicity-dependent APO-1 (Fas/CD95)-associated proteins form a death-inducing signaling complex (DISC) with the receptor. EMBO J 14: 5579-5588.
39. Kischkel FC, Lawrence DA, Tinel A, et al. 2001. Death receptor recruitment of endogenous caspase-10 and apoptosis initiation in the absence of caspase-8. J Biol Chem 276: 46639-46646.
40. Krammer PH. 1999. CD95(APO-1/Fas)-mediated apoptosis: live and let die. Adv Immunol 71: 163-210.
41. Lawrence D, Shahrokh Z, Marsters S, et al. 2001. Differential hepatocyte toxicity of recombinant Apo2L/TRAIL versions. Nat Med 7: 383-385.
42. Lazaris A, Chatzigianni EB, Panoussopoulos D, Tzimas GN, Davaris PS, Golematis B. 1997. Proliferating cell nuclear antigen and heat shock protein 70 immunolocalization in invasive ductal breast cancer not otherwise specified. Breast Cancer Res Treat 43: 43-51.
43. Lazaris AC, Theodoropoulos GE, Davaris PS, Panoussopoulos D, Nakopoulou L, Kittas C, Golematis BC. 1995. Heat shock protein 70 and HLA-DR molecules tissue expression. Prognostic implications in colorectal cancer. Dis Colon Rectum 38: 739-745.
44. Levine AJ. 1992. The p53 tumor-suppressor gene. N Engl J Med 326: 1350-1352.
45. Li H, Zhu H, Xu CJ, Yuan J. 1998. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94: 491-501.
46. Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M, Alnemri ES, Wang X. 1997. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91: 479-489.
47. Lindquist S. 1986. The heat-shock response. Annu Rev Biochem 55: 1151-1191.
48. Luo X, Budihardjo I, Zou H, Slaughter C, Wang X. 1998. Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 94: 481-490.
49. Medema JP, Scaffidi C, Kischkel FC, Shevchenko A, Mann M, Krammer PH, Peter ME. 1997. FLICE is activated by association with the CD95 death-inducing signaling complex (DISC). EMBO J 16: 2794-2804.
50. Meek DW. 1999. Mechanisms of switching on p53: a role for covalent modification? Oncogene 18: 7666-7675.
51. Meng RD, McDonald III ER, Sheikh MS, Fornace Jr AJ, El-Deiry WS. 2000. The TRAIL decoy receptor TRUNDD (DcR2, TRAIL-R4) is induced by adenovirus-p53 overexpression and can delay TRAIL-, p53-, and KILLER/DR5-dependent colon cancer apoptosis. Mol Ther 1: 130-144.
52. Mosser DD, Caron AW, Bourget L, Denis-Larose C, Massie B. 1997. Role of the human heat shock protein hsp70 in protection against stress-induced apoptosis. Mol Cell Biol 17: 5317-5327.
53. Mosser DD, Caron AW, Bourget L, Meriin AB, Sherman MY, Morimoto RI, Massie B. 2000. The chaperone function of hsp70 is required for protection against stress-induced apoptosis. Mol Cell Biol 20: 7146-7159.
54. Mosser DD, Morimoto RI. 2004. Molecular chaperones and the stress of oncogenesis. Oncogene 23: 2907-2918.
55. Nagane M, Pan G, Weddle JJ, Dixit VM, Cavenee WK, Huang HJ. 2000. Increased death receptor 5 expression by chemotherapeutic agents in human gliomas causes synergistic cytotoxicity with tumor necrosis factor-related apoptosis-inducing ligand in vitro and in vivo. Cancer Res 60: 847-853.
56. Nigro JM, Baker SJ, Preisinger AC, et al. 1989. Mutations in the p53 gene occur in diverse human tumour types. Nature 342: 705-708.
57. Ozoren N, El-Deiry W. 2002. Heat shock protects HCT116 and H460 cells from TRAIL-induced apoptosis. Exp Cell Res 281: 175-181.
58. Park DJ, Nakamura H, Chumakov AM, Said JW, Miller CW, Chen DL, Koeffler HP. 1994. Transactivational and DNA binding abilities of endogenous p53 in p53 mutant cell lines. Oncogene 9: 1899-1906.
59. Pitti RM, Marsters SA, Ruppert S, Donahue CJ, Moore A, Ashkenazi A. 1996. Induction of apoptosis by Apo-2 ligand, a new member of the tumor necrosis factor cytokine family. J Biol Chem 271: 12687-12690.
60. Prives C, Hall PA. 1999. The p53 pathway. J Pathol 187: 112-126.
61. r 70,000 heat shock protein in normal, premalignant, and malignant human uterine cervix. Clin Cancer Res 1: 1217-1222.
62. Rodrigues NR, Rowan A, Smith ME, Kerr IB, Bodmer WF, Gannon JV, Lane DP. 1990. p53 mutations in colorectal cancer. Proc Natl Acad Sci USA 87: 7555-7559.
63. Ruiz de Almodovar C, Ruiz-Ruiz C, Rodriguez A, Ortiz-Ferron G, Redondo JM, Lopez-Rivas A. 2004. Tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) decoy receptor TRAIL-R3 is up-regulated by p53 in breast tumor cells through a mechanism involving an intronic p53-binding site. J Biol Chem 279: 4093-4101.
64. Saleh A, Srinivasula SM, Balkir L, Robbins PD, Alnemri ES. 2000. Negative regulation of the Apaf-1 apoptosome by Hsp70. Nat Cell Biol 2: 476-483.
65. Samali A, Cotter TG. 1996. Heat shock proteins increase resistance to apoptosis. Exp Cell Res 223: 163-170.
66. Scaffidi C, Fulda S, Srinivasan A, et al. 1998. Two CD95 (APO-1/Fas) signaling pathways. EMBO J 17: 1675-1687.
67. Schmitz I, Walczak H, Krammer PH, Peter ME. 1999. Differences between CD95 type I and II cells detected with the CD95 ligand. Cell Death Differ 6: 821-822.
68. Selivanova G, Kawasaki T, Ryabchenko L, Wiman KG. 1998. Reactivation of mutant p53: a new strategy for cancer therapy. Semin Cancer Biol 8: 369-378.
69. Sheikh MS, Burns TF, Huang Y, et al. 1998. p53-dependent and -independent regulation of the death receptor KILLER/DR5 gene expression in response to genotoxic stress and tumor necrosis factor-α. Cancer Res 58: 1593-1598.
70. Sheikh MS, Huang Y, Fernandez-Salas EA, et al. 1999. The anti-apoptotic decoy receptor TRID/TRAIL-R3 is a p53-regulated DNA damage-inducible gene that is overexpressed in primary tumors of the gastrointestinal tract. Oncogene 18: 4153-4159.
71. Stankiewicz AR, Lachapelle G, Foo CP, Radicioni SM, Mosser DD. 2005. Hsp70 inhibits heat-induced apoptosis upstream of mitochondria by preventing Bax translocation. J Biol Chem 280: 38729-38739.
72. Steel R, Doherty JP, Buzzard K, Clemons N, Hawkins CJ, Anderson RL. 2004. Hsp72 inhibits apoptosis upstream of the mitochon dria and not through interactions with Apaf-1. J Biol Chem 279: 51490-51499.
73. Subjeck JR, Sciandra JJ, Johnson RJ. 1982. Heat shock proteins and thermotolerance; a comparison of induction kinetics. Br J Radiol 55: 579-584.
74. Takimoto R, El-Deiry WS. 2000. Wild-type p53 transactivates the KILLER/DR5 gene through an intronic sequence-specific DNA-binding site. Oncogene 19: 1735-1743.
75. Thornberry NA, Lazebnik Y. 1998. Caspases: enemies within. Science 281: 1312-1316.
76. Vaux DL, Korsmeyer SJ. 1999. Cell death in development. Cell 96: 245-254.
77. Walczak H, Miller RE, Ariail K, et al. 1999. Tumoricidal activity of tumor necrosis factor-related apoptosis-inducing ligand in vivo. Nat Med 5: 157-163.
78. Wei MC, Lindsten T, Mootha VK, et al. 2000. tBID, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome c. Genes Dev 14: 2060-2071.
79. Wei MC, Zong WX, Cheng EH, et al. 2001. Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 292: 727-730.
80. Wiley SR, Schooley K, Smolak PJ, et al. 1995. Identification and characterization of a new member of the TNF family that induces apoptosis. Immunity 3: 673-682.
81. Wu GS, Kim K, el-Deiry WS. 2000. Killer/dr5, a novel DNA-damage inducible death receptor gene, links the p53-tumor suppressor to caspase activation and apoptotic death. Adv Exp Med Biol 465: 143-151.
82. Xu Y. 2003. Regulation of p53 responses by post-translational modifications. Cell Death Differ 10: 400-403.
83. Yoshida T, Maeda A, Tani N, Sakai T. 2001. Promoter structure and transcription initiation sites of the human death receptor 5/TRAIL-R2 gene. FEBS Lett 507: 381-385.
84. Zambetti GP, Levine AJ. 1993. A comparison of the biological activities of wild-type and mutant p53. FASEB J 7: 855-865.
85. Zhang XY, Zhang XD, Borrow JM, Nguyen T, Hersey P. 2004. Translational control of tumor necrosis factor-related apoptosis-inducing ligand death receptor expression in melanoma cells. J Biol Chem 279: 10606-10614.
86. Zou H, Henzel WJ, Liu X, Lutschg A, Wang X. 1997. Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell 90: 405-413.
87. Zylicz M, King FW, Wawrzynow A. 2001. Hsp70 interactions with the p53 tumour suppressor protein. EMBO J 20: 4634-4638.