Heat shock proteins - Modulators of apoptosis in tumour cells

Leukemia

Volumn 14, Issue 7, 2000, Pages 1161-1173

  Creagh, E M ^a   Sheehan, D ^a   Cotter, T G ^a  

^a UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

Apoptosis; Hsp27; Hsp70; Leukemia

Indexed keywords

HEAT SHOCK PROTEIN;

APOPTOSIS; CARCINOGENESIS; CELL DESTRUCTION; DRUG RESISTANCE; LEUKEMIA CELL; MEDICAL RESEARCH; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATOR GENE; REVIEW; TUMOR CELL;

EID: 0033944777     PISSN: 08876924     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.leu.2401841     Document Type: Review

References (192)

1. Arends MJ, Wyllie AH. Apoptosis: mechanisms and roles in pathology. Int Rev Exp Pathol 1991; 32: 223-254.
2. Barr PJ, Tomei LD. Apoptosis and its role in human disease. Biotechnology (NY) 1994; 12: 487-493.
3. Thompson CB. Apoptosis in the pathogenesis and treatment of disease. Science 1995; 267: 1456-1462.
4. Haslett C. Resolution of acute inflammation and the role of apoptosis in the tissue fate of granulocytes (editorial). Clin Sci (Colch) 1992; 83: 639-648.
5. Wyllie AH, Kerr JF, Currie AR. Cell death: the significance of apoptosis. Int Rev Cytol 1980; 68: 251-306.
6. Searle J, Kerr JF, Bishop CJ. Necrosis and apoptosis: distinct modes of cell death with fundamentally different significance. Pathol Annu 1982; 17: 229-259.
7. Wyllie AH. Apoptosis and the regulation of cell numbers in normal and neoplastic tissues: an overview. Cancer Metastasis Rev 1992; 11: 95-103.
8. Hahn GM, Li GC. Thermotolerance, thermoresistance and thermosensitization. In: Morimoto RI, Tissieres A, Georgeopoulos C (eds). Stress Proteins in Biology and Medicine. Cold Spring Harbor Press: Cold Spring Harbor, NY, 1990, p 79.
9. Lindquist S, Craig EA. The heat-shock proteins. Annu Rev Genet 1988; 22: 631-677.
10. Kojika S, Sugita K, Inukai T, Saito M, Iijima K, Tezuka T, Goi K, Shiraishi K, Mori T, Okazaki T, Kagami K, Ohyama K, Nakazawa S. Mechanisms of glucocorticoid resistance in human leukemic cells: implication of abnormal 90 and 70 kDa heat shock proteins. Leukemia 1996; 10: 994-999.
11. Kim SH, Yeo GS, Lim YS, Kang CD, Kim CM, Chung BS. Suppression of multidrug resistance via inhibition of heat shock factor by quercetin in MDR cells. Exp Mol Med 1998; 30: 87-92.
12. Konno A, Sato N, Yagihashi A, Torigoe T, Cho JM, Torimoto K, Hara I, Wada Y, Okubo M, Takahashi N, Kikuchi K. Heat- or stress-inducible transformation-associated cell surface antigen on the activated H-ras oncogene-transfected rat fibroblast. Cancer Res 1989; 49: 6578-6582.
13. Mosser DD, Caron AW, Bourget L, Denis-Larose C, Massie B. Role of the human heat shock protein hsp70 in protection against stress-induced apoptosis. Mol Cell Biol 1997; 17: 5317-5327.
14. Mehlen P, Schulze-Osthotf K, Arrigo AP. Small stress proteins as novel regulators of apoptosis. Heat shock protein 27 blocks Fas/APO-1- and staurosporine-induced cell death. J Biol Chem 1996; 271: 16510-16514.
15. Garrido C, Ottavi P, Fromentin A, Hammann A, Arrigo AP, Chauffert B, Mehlen P. HSP27 as a mediator of confluence-dependent resistance to cell death induced by anticancer drugs. Cancer Res 1997; 57: 2661-2667.
16. Galea-Lauri J, Richardson AJ, Latchman DS, Katz DR. Increased heat shock protein 90 (hsp90) expression leads to increased apoptosis in the monoblastoid cell line U937 following induction with TNF-alpha and cycloheximide: a possible role in immunopathology. J Immunol 1996; 157: 4109-4118.
17. Liossis SN, Ding XZ, Kiang JG, Tsokos GC. Overexpression of the heat shock protein 70 enhances the TCR/CD3- and Fas/Apo-1/CD95-mediated apoptotic cell death in Jurkat T cells. J Immunol 1997; 158: 5668-5775.
18. Wang JH, Redmond HP, Watson RW, Bouchier-Hayes D. Induction of human endothelial cell apoptosis requires both heat shock and oxidative stress responses. Am J Physiol 1997; 272: C1543-C1551.
19. Ritossa F. A new puffing pattern induced by heat shock and DNP in Drosophila. Experientia 1952; 18: 571-573.
20. Tissieres A, Mitchell HK, Tracy UM. Protein synthesis in salivary glands of Drosophila melanogaster: relation to chromosome puffs. J Mol Biol 1974; 84: 389-398.
21. Lindquist S. Heat-shock proteins and stress tolerance in microorganisms. Curr Opin Genet Dev 1992; 2: 748-755.
22. Feige U, Polla BS. Hsp70 - a multi-gene, multi-structure, multi-function family with potential clinical applications. Experientia 1994; 50: 979-986.
23. Chretien P, Landry J. Enhanced constitutive expression of the 27-kDa heat shock proteins in heat-resistant variants from Chinese hamster cells. J Cell Physiol 1988; 137: 157-166.
24. Mehlen P, Preville X, Chareyron P, Briolay J, Klemenz R, Arrigo AP. Constitutive expression of human hsp27, Drosophila hsp27, or human alpha B-crystallin confers resistance to TNF- and oxidative stress-induced cytotoxicity in stably transfected murine L929 fibroblasts. J Immunol 1995; 154: 363-374.
25. Arrigo AP, Suhan JP, Welch WJ. Dynamic changes in the structure and intracellular locale of the mammalian low-molecular-weight heat shock protein. Mol Cell Biol 1988; 8: 5059-5071.
26. Benndorf R, Hayess K, Ryazantsev S, Wieske M, Behlke J, Lutsch G. Phosphorylation and supramolecular organization of murine small heat shock protein HSP25 abolish its actin polymerization-inhibiting activity. J Biol Chem 1994; 269: 20780-20784.
27. Hendrick JP, Hartl FU. Molecular chaperone functions of heat-shock proteins. Annu Rev Biochem 1993; 62: 349-384.
28. Li GC, Li L, Liu RY, Rehman M, Lee WM. Heat shock protein hsp70 protects cells from thermal stress even after deletion of its ATP-binding domain. Proc Natl Acad Sci USA 1992; 89: 2036-2040.
29. Sanchez Y, Lindquist SL. HSP104 required for induced thermotolerance. Science 1990; 248: 1112-1115.
30. Koyasu S, Nishida E, Kadowaki T, Matsuzaki F, Iida K, Harada F, Kasuga M, Sakai H, Yahara I. Two mammalian heat shock proteins, HSP90 and HSP100, are actin-binding proteins. Proc Natl Acad Sci USA 1986; 83: 8054-8058.
31. Wiech H, Buchner J, Zimmermann R, Jakob U. Hsp90 chaperones protein folding in vitro. Nature 1992; 358: 169-170.
32. Welch WJ. Mammalian stress response: cell physiology, structure/function of stress proteins, and implications for medicine and disease. Physiol Rev 1992; 72: 1063-1081.
33. Beckmann RP, Mizzen LE, Welch WJ. Interaction of Hsp 70 with newly synthesized proteins: implications for protein folding and assembly. Science 1990, 248: 850-854.
34. Angelidis CE, Lazaridis I, Pagoulatos GN. Constitutive expression of heat-shock protein 70 in mammalian cells confers thermoresistance. Eur J Biochem 1991; 199: 35-39.
35. Samali A, Cotter TG. Heat shock proteins increase resistance to apoptosis. Exp Cell Res 1996; 223: 163-170.
36. Frydman J, Hartl FU. Molecular chaperone functions of hsp70 and hsp60 in protein folding. In: Morimoto RI, Tissieres A, Georgopoulos C (eds). Heat Shock Proteins and Molecular Chaperones. Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY, 1994, p 251-283.
37. Samali A, Cai J, Zhivotovsky B, Jones DP, Orrenius S. Presence of a pre-apoptotic complex of pro-caspase-3, Hsp60 and Hsp10 in the mitochondrial fraction of jurkat cells. EMBO J 1999; 18: 2040-2048.
38. Xanthoudakis S, Roy S, Rasper D, Hennessey T, Aubin Y, Cassady R, Tawa P, Ruel R, Rosen A, Nicholson DW. Hsp60 accelerates the maturation of pro-caspase-3 by upstream activator proteases during apoptosis. EMBO J 1999; 18: 2049-2056.
39. Miron T, Vancompernolle K, Vandekerckhove J, Wilchek M, Geiger B. A 25-kD inhibitor of actin polymerization is a low molecular mass heat shock protein. J Cell Biol 1991; 114: 255-261.
40. Clechanover A. The ubiquitin-proteasome proteolytic pathway. Cell 1994; 79: 13-21.
41. Lindquist S. Translational efficiency of heat-induced messages in Drosophila melanogaster cells. J Mol Biol 1980; 137: 151-158.
42. Creagh EM, Cotter TG. Selective protection by hsp 70 against cytotoxic drug-, but not Fas-induced T-cell apoptosis. Immunology 1999; 97: 36-44.
43. Wu C. The 5′ ends of Drosophila heat shock genes in chromatin are hypersensitive to DNase I. Nature 1980; 286: 854-860.
44. Fernandes M, O'Brien T, Lis J. Structure and regulation of heat shock gene promoters. In: Morimoto RI, Tissieres A, Georgopoulos C (eds). The Biology of Heat Shock Proteins and Molecular Chaperones. Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY, 1994, p 375-393.
45. Morimoto RI, Kline MP, Bimston DN, Cotto JJ. The heat-shock response: regulation and function of heat-shock proteins and molecular chaperones. Essays Biochem 1997; 32: 17-29.
46. Wu C, Clos J, Giorgi G, Haroun RI. Structure and regulation of heat shock transcription factor. In: Morimoto RI, Tissieres A, Georgopoulos C (eds). The Biology of Heat Shock Proteins and Molecular Chaperones. Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY, 1994, pp 395-416.
47. Morimoto RI, Jurivich DA, Kroeger PE. Regulation of heat shock gene transcription by a family of heat shock factors. In: Morimoto RI, Tissieres A, Georgopoulos C (eds). The Biology of Heat Shock Proteins and Molecular Chaperones. Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY, 1994, pp 417-455.
48. Zou J, Guo 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.
49. Elia G, De Marco A, Rossi A, Santoro MG. Inhibition of HSP70 expression by calcium ionophore A23187 in human cells. An effect independent of the acquisition of DNA-binding activity by the heat shock transcription factor. J Biol Chem 1996; 271: 16111-16118.
50. Liu H, Lightfoot R, Stevens JL. Activation of heat shock factor by alkylating agents is triggered by glutathione depletion and oxidation of protein thiols. J Biol Chem 1996; 271: 4805-4812.
51. Nishizawa J, Nakai A, Matsuda K, Komeda M, Ban T, Nagata K. Reactive oxygen species play an important role in the activation of heat shock factor 1 in ischemic-reperfused heart. Circulation 1999; 99: 934-941.
52. Marini M, Frabetti F, Musiani D, Franceschi C. Oxygen radicals induce stress proteins and tolerance to oxidative stress in human lymphocytes. Int J Radiat Biol 1996; 70: 337-350.
53. Gorman AM, Heavey B, Creagh E, Cotter TG, Samali A. Antioxidant-mediated inhibition of the heat shock response leads to apoptosis. FEBS Lett 1999; 445: 98-102.
54. Pirkkala L, Alastalo TP, Nykanen P, Seppa L, Sistonen L. Differentiation lineage-specific expression of human heat shock transcription factor 2. FASEB J 1999; 13: 1089-1098.
55. Rougvie AE, Lis JT. The RNA polymerase II molecule at the 5′ end of the uninduced hsp70 gene of D. melanogaster is transcriptionally engaged. Cell 1980; 54: 795-804.
56. Yost HJ, Lindquist S. RNA splicing is interrupted by heat shock and is rescued by heat shock protein synthesis. Cell 1986; 45: 185-193.
57. Craig EA, Gross CA. Is hsp70 the cellular thermometer? Trends Biochem Sci 1991; 16: 135-140.
58. Hightower LE. Heat shock, stress proteins, chaperones, and proteotoxicity. Cell 1991; 66: 191-197.
59. Baler R, Welch WJ, Voellmy R. Heat shock gene regulation by nascent polypeptides and denatured proteins: hsp70 as a potential auroregulatory factor. J Cell Biol 1992; 117: 1151-1159.
60. Mosser DD, Duchaine J, Massie B. The DNA-binding activity of the human heat shock transcription factor is regulated in vivo by hsp70. Mol Cell Biol 1993; 13: 5427-5438.
61. Mifflin LC, Cohen RE. hsc70 moderates the heat shock (stress) response in Xenopus laevis oocytes and binds to denatured protein inducers. J Biol Chem 1994; 269: 15718-15723.
62. Kim HR, Kang HS, Kim HD. Geldanamycin induces heat shock protein expression through activation of HSF1 in K562 erythroleukemic cells. IUBMB Life 1999; 48: 429-433.
63. Suda T, Takahashi T, Golstein P, Nagata S. Molecular cloning and expression of the Fas ligand, a novel member of the tumor necrosis factor family. Cell 1993; 75: 1169-1178.
64. Kischkel FC, Hellbardt S, Behrmann I, Germer M, Pawlita M, Krammer PH, Peter ME. Cytotoxicity-dependent APO-1 (Fas/CD95)-associated proteins form a death-inducing signaling complex (DISC) with the receptor. EMBO J 1995; 14: 5579-5588.
65. Enari M, Talanian RV, Wong WW, Nagata S. Sequential activation of ICE-like and CPP32-like proteases during Fas-mediated apoptosis. Nature 1996; 380: 723-726.
66. Trauth BC, Klas C, Peters AM, Matzku S, Moller P, Falk W, Debatin KM, Krammer PH. Monoclonal antibody-mediated tumor regression by induction of apoptosis. Science 1989; 245: 301-305.
67. Debatin KM, Goldmann CK, Bamford R, Waldmann TA, Krammer PH. Monoclonal-antibody-mediated apoptosis in adult T-cell leukaemia. Lancet 1990; 335: 497-500.
68. Komada Y, Sakurai M. Fas receptor (CD95)-mediated apoptosis in leukemic cells. Leuk Lymphoma 1997; 25: 9-21.
69. Ogasawara J, Watanabe-Fukunaga R, Adachi M, Matsuzawa A, Kasugai T, Kitamura Y, Itoh N, Suda T, Nagata S. Lethal effect of the anti-Fas antibody in mice. Nature 1993; 364: 806-809.
70. Findley HW, Zhou M. The clinical significance of Fas expression in leukemia: questions and controversies. Leukemia 1999; 13: 147-149.
71. Jaattela M, Wissing D. Heat-shock proteins protect cells from monocyte cytotoxicity: possible mechanism of self-protection. J Exp Med 1993; 177: 231-236.
72. Richards EH, Hickey E, Weber L, Master JR. Effect of overexpression of the small heat shock protein HSP27 on the heat and drug sensitivities of human testis tumor cells. Cancer Res 1996; 56: 2446-2451.
73. Guenal I, Sidoti-de Fraisse C, Gaumer S, Mignotte B. Bcl-2 and Hsp27 act at different levels to suppress programmed cell death. Oncogene 1997; 15: 347-360.
74. Trautinger F, Kokesch C, Herbacek I, Knobler RM, Kindas-Mugge I. Overexpression of the small heat shock protein, hsp27, confers resistance to hyperthermia, but not to oxidative stress and UV-induced cell death, in a stably transfected squamous cell carcinoma cell line. J Photochem Photobiol B 1997; 39: 90-95.
75. Strahler JR, Kuick R, Eckerskorn C, Lottspeich F, Richardson BC, Fox DA, Stoolman LM, Hanson CA, Nichols D, Tueche HJ, Hanash SM. Identification of two related markers for common acute lymphoblastic leukemia as heat shock proteins. J Clin Invest 1990; 85: 200-207.
76. Arrigo AP. Small stress proteins: chaperones that act as regulators of intracellular redox state and programmed cell death. Biol Chem 1998; 379: 19-26.
77. Mehlen P, Kretz-Remy C, Preville X, Arrigo AP. Human hsp27, Drosophila hsp27 and human alphaB-crystallin expression-mediated increase in glutathione is essential for the protective activity of these proteins against TNFalpha-induced cell death. EMBO J 1996; 15: 2695-2706.
78. van den Dobbelsteen DJ, Nobel CSI, Schlegel J, Cotgreave IA, Orrenius S, Slater AF. Rapid and specific efflux of reduced glutathione during apoptosis induced by anti-Fas/APO-1 antibody. J Biol Chem 1996; 271: 15420-15427.
79. Bauer MKA, Vogt M, Los M, Siegel J, Wesselborg S, Schulze-Osthoff K. Role of reactive oxygen intermediates in activation-induced CD95 (APO- 1/Fas) ligand expression. J Biol Chem 1998; 273: 8048-8055.
80. Chant ID, Rose PE, Morris AG. Susceptibility of AML cells to in vitro apoptosis correlates with heat shock protein 70 (hsp 70) expression. Br J Haematol 1996; 93: 898-902.
81. Filippovich I, Sorokina N, Khanna KK, Lavin MF. Butyrate induced apoptosis in lymphoid cells preceded by transient overexpression of HSP70 mRNA. Biochem Biophys Res Commun 1994; 198: 257-265.
82. Murdoch WJ. Temporal relationships between stress protein induction, progesterone withdrawal, and apoptosis in corpora lutea of ewes treated with prostaglandin F2 alpha. J Anim Sci 1995; 73: 1789-1792.
83. Furlini G, Vignoli M, Re MC, Gibellini D, Ramazzotti E, Zauli G, La Placa M. Human immunodeficiency virus type 1 interaction with the membrane of CD4+ cells induces the synthesis and nuclear translocation of 70K heat shock protein. J Gen Virol 1994; 75: 193-199.
84. Finkel T. Oxygen radicals and signaling. Curr Opin Cell Biol 1998; 10: 248-253.
85. Floyd RA. Oxidative damage to behavior during aging. Science 1991; 254: 1597.
86. Carney JM, Starke-Reed PE, Oliver CN, Landum RW, Cheng MS, Wu JF, Floyd RA. Reversal of age-related increase in brain protein oxidation, decrease in enzyme activity, and loss in temporal and spatial memory by chronic administration of the spin-trapping compound N-tert-butyl-alpha-phenylnitrone. Proc Natl Acad Sci USA 1991; 88: 3633-3636.
87. 2 in the cellular stress. Free Radic Res Commun 1991; 12-13: 455-460.
88. Troll W. Prevention of canter by agents that suppress oxygen radical formation. Free Radic Res Commun 1991; 12-13: 751-757.
89. Lennon SV, Martin SJ, Cotter TG. Dose-dependent induction of apoptosis in human tumour cell lines by widely diverging stimuli. Cell Prolif 1991; 24: 203-214.
90. Albina JE, Cui S, Mateo RB, Reichner JS. Nitric oxide-mediated apoptosis in murine peritoneal macrophages. J Immunol 1993; 150: 5080-5085.
91. Escargueil I, Negre-Salvayre A, Pieraggi MT, Salvayre R. Oxidized low density lipoproteins elicit DNA fragmentation of cultured lymphoblastoid cells. FEBS Lett 1992; 305; 155-159.
92. McCowan AJ, Ruiz-Ruiz MC, Gorman AM, Lopez-Rivas A, Cotter TG. Reactive oxygen intermediate(s) (ROI): common mediator(s) of poly(ADP- ribose)polymerase (PARP) cleavage and apoptosis. FEBS Lett 1996; 392: 299-303.
93. Gorman A, McGowan A, Cotter TG. Role of peroxide and superoxide anion during tumour cell apoptosis. FEBS Lett 1997; 404: 27-33.
94. Li PF, Dietz R, von Harsdorf R. p53 regulates mitochondrial membrane potential through reactive oxygen species and induces cytochrome c-independent apoptosis blocked by Bcl-2. EMBO J 1999; 18: 6027-6036.
95. Slater AF, Nobel CS, Maellaro E, Bustamante J, Kimland M, Orrenius S. Nitrone spin traps and a nitroxide antioxidant inhibit a common pathway of thymocyte apoptosis. Biochem J 1995; 306: 771-778.
96. Hedley DW, McCulloch EA, Minden MD, Chow S, Curtis J. Anti-leukemic action of buthionine sulfoximine: evidence for an intrinsic death mechanism based on oxidative stress. Leukemia 1998; 12: 1545-1552.
97. Furuke K, Sasada T, Ueda-Taniguchi Y, Yamauchi A, Inamoto T, Yamaoka Y, Masutani H, Yodoi J. Role of intracellular redox status in apoptosis induction of human T-cell leukemia virus type I-infected lymphocytes by 13-cis-retinoic acid. Cancer Res 1997; 57: 4916-4923.
98. Lindquist S. The heat-shock response. Annu Rev Biochem 1986; 55: 1151-1191.
99. Jaattela M. Overexpression of major heat shock protein hsp70 inhibits tumor necrosis factor-induced activation of phospholipase A2. J Immunol 1993; 151: 4286-4294.
100. Simon MM, Reikerstorfer A, Schwarz A, Krone C, Luger TA, Jaattela M, Schwarz T. Heat shock protein 70 overexpression affects the response to ultraviolet light in murine fibroblasts. Evidence for increased cell viability and suppression of cytokine release. J Clin Invest 1995; 95: 926-933.
101. Halliwell B. Oxidants and human disease: some new concepts. FASEB J 1987; 1: 158-364.
102. Chant ID, Rose PE, Morris AG. Analysis of heat-shock protein expression in myeloid leukaemia cells by flow cytometry. Br J Haematol 1995; 90: 163-168.
103. Santarosa M, Favaro D, Quaia M, Galligioni E. Expression of heat shock protein 72 in renal cell carcinoma: possible role and prognostic implications in cancer patients. Eur J Cancer 1997; 33: 873-877.
104. Ralhan R, Kaur J. Differential expression of Mr 70,000 heat shock protein in normal, premalignant, and malignant human uterine cervix. Ciln Cancer Res 1995; 1: 1217-1222.
105. Richards FM, Watson A, Hickman JA. Investigation of the effects of heat shock and agents which induce a heat shock response on the induction of differentiation of HL-60 cells. Cancer Res 1988; 48: 6715-6720.
106. Sliutz G, Karlseder J, Tempfer C, Orel L, Holzer G, Simon MM. Drug resistance against gemcitabine and topotecan mediated by constitutive hsp70 overexpression in vitro: implication of quercetin as sensitiser in chemotherapy. Br J Cancer 1996; 74: 172-177.
107. Hug H, Enari M, Nagata S. No requirement of reactive oxygen intermediates in Fas-mediated apoptosis. FEBS Lett 1994; 351: 311-313.
108. Yu BP. Cellular defenses against damage from reactive oxygen species. Physiol Rev 1994; 74: 139-162.
109. Schulze-Osthoff K, Bakker AC, Vanhaesebroeck B, Beyaert R, Jacob WA, Fiers W. Cytotoxic activity of tumor necrosis factor is mediated by early damage of mitochondrial functions. Evidence for the involvement of mitochondrial radical generation. J Biol Chem 1992; 267: 5317-5323.
110. Buttke TM, Sandstrom PA. Oxidative stress as a mediator of apoptosis. Immunol Today 1994; 15: 7-10.
111. 2+ homeostasis, cell death, proliferation, and differentiation. Chem Biol Interact 1991; 77: 1-23.
112. Gabai VL, Meriin AB, Mosser DD, Caron AW, Rits S, Shifrin VI, Sherman MY. Hsp70 prevents activation of stress kinases. A novel pathway of cellular thermotoleranre. J Biol Chem 1997; 272: 18033-18037.
113. Buzzard KA, Giaccia AJ, Killender M, Anderson RL. Heat shock protein 72 modulates pathways of stress-induced apoptosis. J Biol Chem 1998; 273: 17147-17153.
114. 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.
115. Lee YJ, Corry PM. Metabolic oxidative stress-induced HSP70 gene expression is mediated through SAPK pathway. Role of Bcl-2 and c-Jun NH2-terminal kinase. J Biol Chem 1998; 273: 29857-29863.
116. 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.
117. Ichijo H, Nishida E, Irie K, ten Dijke P, Saitoh M, Moriguchi T, Takagi M, Matsumoto K, Miyazono K, Gotoh Y. Induction of apoptosis by ASK1, a mammalian MAPKKK that activates SAPK/JNK and p38 signaling pathways. Science 1997; 275: 90-94.
118. Hainaut P, Milner J. Interaction of heat-shock protein 70 with p.53 translated in vitro: evidence for interaction with dimeric p53 and for a role in the regulation of p53 conformation. EMBO J 1992; 11: 3513-3520.
119. Koskinen PJ, Sistonen L, Evan G, Morimoto R, Alitalo K. Nuclear colocalization of cellular and viral myc proteins with HSP70 in myc-overexpressing cells. J Virol 1991; 65: 842-851.
120. Jaattela M, Wissing D, Bauer PA, Li GC. Major heat shock protein hsp70 protects tumor cells from tumor necrosis factor cytotoxicity. EMBO J 1992; 11: 3507-3512.
121. Pratt WB. The role of the hsp90-based chaperone system in signal transduction by nuclear receptors and receptors signaling via MAP kinase. Annu Rev Pharmacol Toxicol 1997; 37: 297-326.
122. Scheibel T, Buchner J. The Hsp90 complex - a super-chaperone machine as a novel drug target. Biochem Pharmacol 1998; 56: 675-682.
123. Stebbins CE, Russo AA, Schneider C, Rosen N, Hartl FU, Pavletich NP. Crystal structure of an Hsp90-geldanamycin complex: targeting of a protein chaperone by an antitumor agent. Cell 1997; 89: 239-250.
124. Blagosklonny MV, Toretsky J, Bohen S, Neckers L. Mutant conformation of p53 translated in vitro or in vivo requires functional HSP90. Proc Natl Acad Sci USA 1996; 93: 8379-8383.
125. Schulte TW, Blagosklonny MV, Romanova L, Mushinski JF, Monia BP, Johnston JF, Nguyen P, Trepel J, Neckers LM. Destabilization of Raf-1 by geldanamycin leads to disruption of the Raf-1-MEK-mitogen-activated protein kinase signalling pathway. Mol Cell Biol 1996; 16: 5839-5845.
126. An WG, Schnur RC, Neckers L, Blagosklonny MV. Depletion of p185erbB2, Raf-1 and mutant p53 proteins by geldanamycin derivatives correlates with antiproliferative activity. Cancer Chemother Pharmacol 1997; 40: 60-64.
127. Thornberry NA, Lazebnik Y. Caspases: enemies within. Science 1998; 281: 1312-1316.
128. Gianni M, de The H. In acute promyelocytic leukemia NB4 cells, the synthetic retinoid CD437 induces contemporaneously apoptosis, a caspase-3-mediated degradation of PML/RARalpha protein and the PML retargeting on PML-nuclear bodies. Leukemia 1999: 13: 739-749.
129. Meinhardt G, Roth J, Totok G, Auner H, Emmerich B, Hass R. Signaling defect in the activation of caspase-3 and PKCdelta in human TUR leukemia cells is associated with resistance to apoptosis. Exp Cell Res 1999; 247: 534-542.
130. Rheaume E, Cohen LY, Uhlmann F, Lazure C, Alam A, Hurwitz J, Sekaly RP, Denis F. The large subunit of replication factor C is a substrate for caspase-3 in vitro and is cleaved by a caspase-3-like protease during Fas-mediated apoptosis. EMBO J 1997; 16: 6346-6354.
131. Song Q, Burrows SR, Smith C, Lees-Miller SP, Kumar S, Chan DW, Trapani JA, Alnemri E, Litwack G, Lu H, Moss DJ, Jackson S, Lavin MF. Interleukin-1 beta-converting enzyme-like protease cleaves DNA-dependent protein kinase in cytotoxic T cell killing. J Exp Med 1996; 184: 619-626.
132. Bokoch GM. Caspase-mediated activation of PAK2 during apoptosis: proteolytic kinase activation as a general mechanism of apoptotic signal transduction? Cell Death Differ 1998; 5: 637-645.
133. Cheng EH, Kirsch DG, Clem RJ, Ravi R, Kastan MB, Bedi A, Ueno K, Hardwick JM. Conversion of Bcl-2 to a Bax-like death effector by caspases. Science 1997; 278: 1966-1968.
134. Widmann C, Gibson S, Johnson GL. Caspase-dependent cleavage of signaling proteins during apoptosis. A turn-off mechanism for anti-apoptotic signals. J Biol Chem 1998; 273: 7141-7147.
135. Kumar S, Colussi PA. Prodomains-adaptors-oligomerization: the pursuit of caspase activation in apoptosis. Trends Biochem Sci 1999; 24: 1-4.
136. Cryns V, Yuan J. Proteases to die for. Genes Dey 1998; 12: 1551-1570.
137. Muzio M, Chinnaiyan AM, Kischkel FC, O'Rourke K, Shevchenko A, Ni J, Scaffidi C, Bretz JD, Zhang M, Gentz R, Mann M, Krammer PH, Peter ME, Dixit VM. FLICE, a novel FADD-homologous ICE/CED-3-like protease, is recruited to the CD95 (Fas/APO-1) death-inducing signaling complex. Cell 1996; 85: 817-827.
138. Boldin MP, Goncharov TM, Goltsev YV, Wallach D. Involvement of MACH, a novel MORT1/FADD-interacting protease, in Fas/APO-1- and TNF receptor-induced cell death. Cell 1996; 85: 803-815.
139. Ashkenazi A, Dixit VM. Death receptors: signaling and modulation. Science 1998; 281: 1305-1308.
140. Scaffidi C, Fulda S, Srinivasan A, Friesen C, Li F, Tomaselli KJ, Debatin KM, Krammer PH, Peter ME. Two CD95 (APO-1/Fas) signaling pathways. EMBO J 1998; 17: 1675-1687.
141. Zou H, Henzel WJ, Liu X, Lutschg A, Wang X. Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3 (see comments). Cell 1997; 90: 405-413.
142. Kluck RM, Bossy-Wetzel E, Green DR, Newmeyer DD. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 1997; 275: 1132-1136.
143. Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M, Alnemri ES, Wang X. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 1997; 91: 479-489.
144. Zou H, Li Y, Liu X, Wang X. An APAF-1 cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9. J Biol Chem 1999; 274: 11549-11556.
145. Garrido C, Bruey JM, Fromentin A, Hammann A, Arrigo AP, Solary E. HSP27 inhibits cytochrome c-dependent activation of procaspase-9. FASEB J 1999; 13: 2061-2070.
146. Green DR, Reed JC. Mitochondria and apoptosis. Science 1998; 281: 1309-1312.
147. Mancini M, Nicholson DW, Roy S, Thornberry NA, Peterson EP, Casciola-Rosen LA, Rosen A. The caspase-3 precursor has a cytosolic and mitochondrial distribution: implications for apoptotic signaling. J Cell Biol 1998; 140: 1485-1495.
148. McCarthy NJ, Whyte MK, Gilbert CS, Evan GI. Inhibition of Ced3/ICE-related proteases does not prevent cell death induced by oncogenes, DNA damage, or the Bcl-2 homologue Bak. J Cell Biol 1997; 136: 215-227.
149. Berndt C, Mopps B, Angermuller S, Gierschik P, Krammer PH. CXCR4 and CD4 mediate a rapid CD95-independent cell death in CD4(+) T cells. Proc Natl Acad Sci USA 1998; 95; 12556-12561.
150. Kawahara A, Ohsawa Y, Matsumura H, Uchiyama Y, Nagata S. Caspase-independent cell killing by Fas-associated protein with death domain. J Cell Biol 1998; 143; 1353-1360.
151. Lavoie JN, Nguyen M, Marcellus RC, Branton PE, Shore GC. E4orf4, a novel adenovirus death factor that induces p53-independent apoptosis by a pathway that is not inhibited by zVAD-fmk. J Cell Biol 1998; 140: 637-645.
152. Lesage S, Steff AM, Philippoussis F, Page M, Trop S, Mateo V, Hugo P. CD4+ CD8+ thymocytes are preferentially induced to die following CD45 cross-linking, through a novel apoptotic pathway. J Immunol 1997; 159: 4762-4771.
153. Sohn HW, Choi EY, Kim SH, Lee IS, Chung DH, Sung UA, Hwang DH, Cho SS, Jun BH, Jang JJ, Chi JG, Park SH. Engagement of CD99 induces apoptosis through a calcineurin-independent pathway in Ewing's sarcoma cells. Am J Pathol 1998; 153: 1937-1945.
154. Nicholson DW, Ali A, Thornberry NA, Vaillancourt JP, Ding CK, Gallant M, Gareau Y, Griffin PR, Labelle M, Lazebnik YA, Munday NA, Raju SM, Smulson ME, Yamin T-T, Yu VL, Miller DK. Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 1995; 376: 37-43.
155. Freeman BC, Myers MP, Schumacher R, Morimoto RI. Identification of a regulatory motif in Hsp70 that affects ATPase activity, substrate binding and interaction with HDJ-1. EMBO J 1995; 14: 2281-2292.
156. Clem RJ, Cheng EH, Karp CL, Kirsch DG, Ueno K, Takahashi A, Kastan MB, Griffin DE, Earnshaw WC, Veliuona MA, Hardwick JM. Modulation of cell death by Bcl-XL through caspase interaction. Proc Natl Acad Sci USA 1998; 95: 554-559.
157. Susin SA, Zamzami N, Castedo M, Hirsch T, Marchetti P, Macho A, Daugas E, Geuskens M, Kroemer G. Bcl-2 inhibits the mitochondrial release of an apoptogenic protease. J Exp Med 1996; 184: 1331-1341.
158. Susin SA, Lorenzo HK, Zamzami N, Marzo I, Brenner C, Larochette N, Prevost MC, Alzari PM, Kroemer G. Mitochondrial release of caspase-2 and -9 during the apoptotic process. J Exp Med 1999; 189: 381-394.
159. Kroemer G, Dallaporta B, Resche-Rigon M. The mitochondrial death/life regulator in apoptosis and necrosis. Annu Rev Physiol 1998; 60: 619-642.
160. Liu X, Kim CN, Yang J, Jemmerson R, Wang X. Induction of apoptotic program in cell-tree extracts: requirement for dATP and cytochrome c. Cell 1996; 86: 147-157.
161. Jurgensmeier JM, Xie Z, Deveraux Q, Ellerby L, Bredesen D, Reed JC. Bax directly induces release of cytochrome c from isolated mitochondria. Proc Natl Acad Sci USA 1998; 95: 4997-5002.
162. Susin SA, Lorenzo HK, Zamzami N, Marzo I, Snow BE, Brothers GM, Mangion J, Jacotot E, Costantini P, Loeffler M, Larochette N, Goodlett DR, Aebersold R, Siderovski DP, Penninger JM, Kroemer G. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 1999; 397: 441-446.
163. Lorenzo HK, Susin SA, Penninger J, Kroemer G. Apoptosis inducing factor (AIF): a phylogenetically old, caspase-independent effector of cell death. Cell Death Differ 1999; 6: 516-524.
164. Ichas F, Mazat IP. From calcium signaling to cell death: two conformations for the mitochondrial permeability transition pore. Switching from low- to high-conductance state. Biochim Biophys Acta 1998; 1366: 33-50.
165. Zamzami N, Susin SA, Marchetti P, Hirsch T, Gomez-Monterrey I, Castedo M, Kroemer G. Mitochondrial control of nuclear apoptosis. J Exp Med 1996; 183: 1533-1544.
166. Zhu L, Ling S, Yu XD, Venkatesh LK, Subramanian T, Chinnadurai G, Kuo TH. Modulation of Mitochondrial Ca(2+) Homeostasis by Bcl-2. J Biol Chem 1999; 274: 33267-33273.
167. Polla BS, Kantengwa S, Francois D, Salvioli S, Franceschi C, Marsac C, Cossarizza A. Mitochondria are selective targets for the protective effects of heat shock against oxidative injury. Proc Natl Acad Sci USA 1996; 93: 6458-6463.
168. Bossy-Wetzel E, Newmeyer DD, Green DR. Mitochondrial cytochrome c release in apoptosis occurs upstream of DEVD-specific caspase activation and independently of mitochondrial transmembrane depolarization. EMBO J 1998; 17: 37-49.
169. Hockenbery D, Nunez G, Milliman C, Schreiber RD, Korsmeyer SJ. Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death. Nature 1990; 348: 334-336.
170. Sentman CL, Shutter JR, Hockenbery D, Kanagawa O, Korsmeyer SJ. Bcl-2 inhibits multiple forms of apoptosis but not negative selection in thymocytes. Cell 1991; 67: 879-808.
171. Bissonnelle RP, Echeverri F, Mahboubi A, Green DR. Apoptotic cell death induced by c-myc is inhibited by bcl-2. Nature 1992; 359: 552-554.
172. Miyashita T, Reed JC. bcl-2 gene transfer increases relative resistance of S49.1 and WEHI7.2 lymphoid cells to cell death and DNA fragmentation induced by glucocorticoids and multiple chemotherapeutic drugs. Cancer Res 1992; 52: 5407-5411.
173. Vanhaesebroeck B, Reed JC, De Valck D, Grooten J, Miyashita T, Tanaka S, Beyaert R, Van Roy F, Fiers W. Effect of bcl-2 protooncogene expression on cellular sensitivity to tumor necrosis factor-mediated cytotoxicity. Oncogene 1993; 8: 1075-1081.
174. Itoh N, Tsujimoto Y, Nagata S. Effect of bcl-2 on Fas antigen-mediated cell death. J Immunol 1993; 151: 621-627.
175. Jaattela M, Benedict M, Tewari M, Shayman JA, Dixit VM. Bcl-x and Bcl-2 inhibit TNF and Fas-induced apoptosis and activation of phospholipase A2 in breast carcinoma cells. Oncogene 1995; 10: 2297-2305.
176. Robertson JD, Datta K, Kehrer JP. Bcl-xL overexpression restricts heat-induced apoptosis and influences hsp70, bcl-2, and Bax protein levels in FL5.12 cells. Biochem Biophys Res Commun 1997; 241: 164-168.
177. Foghsgaard L, Jaattela M. The ability of BHRF1 to inhibit apoptosis is dependent on stimulus and cell type. J Virol 1997; 71: 7509-7517.
178. Adams JM, Cory S. The Bcl-2 protein family: arbiters of cell survival. Science 1998; 281: 1322-1326.
179. Chao DT, Korsmeyer SJ. BCL-2 family: regulators of cell death. Annu Rev Immunol 1998; 16: 395-419.
180. Reed JC. Bcl-2 family proteins. Oncogene 1998; 17: 3225-3236.
181. Hill ME, MacLennan KA, Cunningham DC, Vaughan Hudson B, Burke M, Clarke P, Di Stefano F, Anderson L, Vaughan Hudson G, Mason D, Selby P, Linch DC. Prognostic significance or BCL-2 expression and bcl-2 major breakpoint region rearrangement in diffuse large cell non-Hodgkin's lymphoma: a British National Lymphoma Investigation Study. Blood 1996; 88: 1046-1051.
182. Campos L, Rouault JP, Sabido O, Oriol P, Roubi N, Vasselon C, Archimbaud E, Maraud JP, Guyotat D. High expression of bcl-2 protein in acute myeloid leukemia cells is associated with poor response to chemotherapy. Blood 1993; 81: 3091-3096.
183. Robertson LE, Plunkett W, McConnell K, Keating MJ, McDonnell TJ. Bcl-2 expression in chronic lymphocytic leukemia and its correlation with the induction of apoptosis and clinical outcome. Leukemia 1996; 10: 456-459.
184. Takayama S, Bimston DN, Matsuzawa S, Freeman BC, Aime-Sempe C, Xie Z, Morimoto RI, Reed JC. BAG-1 modulates the chaperone activity of Hsp70/Hsc70. EMBO J 1997; 16; 4887-4896.
185. Takayama S, Krajewski S, Krajewska M, Kitada S, Zapata JM, Kochel K, Knee D, Scudiero D, Tudor G, Miller GJ, Miyashita T, Yamada M, Reed JC. Expression and location of Hsp70/Hsc-binding anti-apoptotic protein BAG- 1 and its variants in normal tissues and tumor cell lines. Cancer Res 1998; 58: 3116-3131.
186. McKenna SL, Padua RA. Multidrug resistance in leukaemia. Br J Haematol 1997; 96: 659-674.
187. Zwelling LA. Topoisomerase II as a target of antileukemia drugs: a review of controversial areas. Hematol Pathol 1989; 3: 101-112.
188. Izquierdo MA, Shoemaker RH, Flens MJ, Scheffer GL, Wu L, Prather TR, Scheper RJ. Overlapping phenotypes of multidrug resistance among panels of human cancer-cell lines. Int J Cancer 1996; 65: 230-237.
189. Kasimir-Bauer S, Ottinger H, Meusers P, Beelen DW, Brittinger G, Seeber S, Scheulen ME. In acute myeloid leukemia, coexpression of at least two proteins, including P-glycoprotein, the multidrug resistance-related protein, bcl-2, mutant p53, and heat-shock protein 27, is predictive of the response to induction chemotherapy. Exp Hematol 1998; 26: 1111-1117.
190. Wei YQ, Zhao X, Kariya Y, Teshigawara K, Uchida A. Inhibition of proliferation and induction of apoptosis by abrogation of heat-shock protein (HSP) 70 expression in tumor cells. Cancer Immunol Immunother 1995; 40: 73-78.
191. Mairesse N, Horman S, Mosselmans R, Galand P. Antisense inhibition of the 27 kDa heat shock protein production affects growth rate and cytoskeletal organisation in MCF-7 cells. Cell Biol Int 1996; 20: 205-212.
192. Creagh EM, Carmody RJ, Cotter TG. HSP70 inhibits caspase-dependent and -independent apoptosis in Jurkat T cells. Exp Cell Res 2000 (in press).