Apoptosis and the dilemma of cancer chemotherapy

Blood

Volumn 89, Issue 6, 1997, Pages 1845-1853

  Hannun, Yusuf A ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMSACRINE; ANTINEOPLASTIC AGENT; AZACITIDINE; BLEOMYCIN; CAMPTOTHECIN; CARMUSTINE; CHLORMETHINE; CISPLATIN; CYCLOPHOSPHAMIDE; CYTARABINE; DACTINOMYCIN; DEXAMETHASONE; DOXORUBICIN; ETOPOSIDE; FLOXURIDINE; FLUOROURACIL; HYDROXYUREA; MELPHALAN; METHOTREXATE; PACLITAXEL; TENIPOSIDE; VINCRISTINE;

APOPTOSIS; CANCER; CANCER CHEMOTHERAPY; CANCER RESISTANCE; CELL DAMAGE; DRUG MECHANISM; ETIOLOGY; HUMAN; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION;

EID: 0030999750     PISSN: 00064971     EISSN: None     Source Type: Journal    
DOI: 10.1182/blood.v89.6.1845     Document Type: Review

References (95)

1. Clarke PGH, Clarke S: Nineteenth century research on naturally occurring cell death and related phenomena. Anat Embryol 193:81, 1996
2. Kerr JFR, Harmon BV: Definition and incidence of apoptosis: An historical perspective, in Tomei LD, Cope FO (eds): Apoptosis: The Molecular Basis of Cell Death. Cold Spring Harbor, NY, Cold Spring Harbor Laboratory, 1991, p 5
3. Wyllie AH, Kerr JFR, Currie AR: Cell death: The significance of apoptosis. Int Rev Cytol 68:251, 1992
4. Smith CA, Farrah T, Goodwin RG: The TNF receptor super-family of cellular and viral proteins: Activation, costimulation, and death. Cell 76:959, 1994
5. Nagata S: Apoptosis regulated by a death factor and its receptor: Fas ligand and Fas. Phil Trans R Soc Lond Biol 345:281, 1994
6. Gerschenson LE, Rotello RJ: Apoptosis: A different type of cell death. FASEB J 6:2450, 1992
7. Michaelson J: The significance of cell death, in Tomei LD, Cope FO (eds): Apoptosis: The Molecular Basis of Cell Death. Cold Spring Harbor, NY, Cold Spring Harbor Laboratory, 1991, p 31
8. Carson DA, Ribeiro JM: Apoptosis and disease. Lancet 341:1251, 1993
9. Kerr JFR, Winterford CM, Harmon BV: Apoptosis: Its significance in cancer and cancer therapy. Cancer 73:2013, 1994
10. Williams GT: Programmed cell death: Apoptosis and oncogenesis. Cell 65:1097, 1991
11. Vogelstein B, Kinzler KW: p53 function and dysfunction. Cell 70:523, 1992
12. Oren M: p53: The ultimate tumor suppressor gene? FASEB J 6:3169, 1992
13. Lane DP: p53, guardian of the genome. Nature 358:15, 1992
14. Reed JC: BCL-2: Prevention of apoptosis as a mechanism of drug resistance. Hematol Oncol Clin North Am 9:451, 1995
15. Korsmeyer SJ, Yin X-M, Oltvai ZN, Veis-Novack DJ, Linette GP: Reactive oxygen species and the regulation of cell death by the Bcl-2 gene family. Biochim Biophys Acta Mol Basis Dis 1271:63, 1995
16. L and Bcl-2, displaces Bax and promotes cell death. Cell 80:285, 1995
17. Wang HG, Takayama S, Rapp UR, Reed JC: Bcl-2 interacting protein, BAG-1, binds to and activates the kinase Raf-1. Proc Natl Acad Sci USA 93:7063, 1996
18. Yuan J, Shaham S, Ledoux S, Ellis HM, Horvitz HR: The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1β-converting enzyme. Cell 75:641, 1993
19. Hedgecock EM, Salston JE, Thomson JN: Mutations affecting programmed cell death in the nematode Caenorhabditis elegans. Science 220:1277, 1983
20. McCohkey DJ, Orrenius S: Signal transduction pathways to apoptosis. Trends Cell Biol 4:370, 1994
21. Fesus L, Davies PJA, Piacentini M: Apoptosis: Molecular mechanisms in programmed cell death. Eur J Cell Biol 56:170, 1991
22. Bursch W, Kleine L, Tenniswood M: The biochemistry of cell death by apoptosis. Biochem Cell Biol 68:1071, 1990
23. Jacobson MD, Evan GI: Apoptosis: Breaking the ICE. Curr Biol 4:337, 1994
24. Hannun YA, Obeid LM: Ceramide: An intracellular signal for apoptosis. Trends Biochem Sci 20:73, 1995
25. Martin SJ, Green DR: Protease activation during apoptosis: Death by a thousand cuts? Cell 82:349, 1995
26. Lu W, Andrieu J-M: Apoptosis and HIV disease. Nat Med 1:386, 1995
27. Cohen JJ, Al-Rubeai M: Apoptosis-targeted therapies: The 'next big thing' in biotechnology? Trends Biotechnol 13:281, 1995
28. Jacobson MD: Reactive oxygen species and programmed cell death. Trends Biochem Sci 21:83, 1996
29. Chinnaiyan AM, Tepper CG, Seldin MF, O'Rourke K, Kischkel FC, Hellbardt S, Krammer PH, Peter ME, Dixit VM: FADD/MORT1 is a common mediator of CD95 (Fas/APO-1) and tumor necrosis factor receptor-induced apoptosis. J Biol Chem 271:4961, 1996
30. Hsu H, Xiong J, Goeddel DV: The TNF receptor 1-associated protein TRADD signals cell death and NF-kappaB activation. Cell 81:495, 1995
31. 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 85:803, 1996
32. 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 CD 95 (Fas/APO-1) death-inducing signaling complex. Cell 85:817, 1996
33. Obeid LM, Linardic CM, Karolak LA, Hannun YA: Programmed cell death induced by ceramide. Science 259:1769, 1993
34. Obeid LM, Hannun YA: Ceramide: A stress signal and mediator of growth suppression and apoptosis. J Cell Biochem 58:191, 1995
35. Smyth MJ, Perry DK, Zhang J, Poirier GG, Hannun YA, Obeid LM: prICE: A downstream target for ceramide-induced apoptosis and for the inhibitory action of bcl-2. Biochem J 316:25, 1996
36. L function upstream of the CED-3-like apoptotic proteases. J Biol Chem 271:4573, 1996
37. Kaufmann S: Induction of endonucleolytic DNA cleavage in human acute myelogenous leukemia cells by etoposide, camptothecin, and other cytotoxic anticancer drugs: A cautionary note. Cancer Res 49:5870, 1989
38. Walker PR, Smith C, Youdale T, Leblanc J, Whitfield JF, Sikorska M: Topoisomerase II-reactive chemotherapeutic drugs induce apoptosis in thymocytes. Cancer Res 51:1078, 1991
39. Shinomiya N, Shinomiya M, Wakiyama H, Katsura Y, Rokutanda M: Enhancement of CDDP cytotoxicity by caffeine is characterized by apoptotic cell death. Exp Cell Res 210:236, 1994
40. Havrilesky LJ, Elbendary A, Hurteau JA, Whitaker RS, Rodriguez GC, Berchuck A: Chemotherapy-induced apoptosis in epithelial ovarian cancers. Obstet Gynecol 85:1007, 1995
41. Huschtscha LI, Bartier WA, Ross CEA, Tattersall MHN: Characteristics of cancer cell death after exposure to cytotoxic drugs in vitro. Br J Cancer 73:54, 1996
42. Tomei LD, Kanter P, Werner CE: Inhibition of radiation-induced apoptosis in vitro by tumor promoters. Biochem Biophys Res Commun 155:324, 1988
43. Yao K-S, Clayton M, O'Dwyer PJ: Apoptosis in human adenocarcinoma HT29 cells induced by exposure to hypoxia. J Natl Cancer Inst 87:117, 1995
44. Haimovitz-Friedman A, Kan C-C, Ehleiter D, Persaud RS, McLoughlin M, Fuks Z, Kolesnick RN: Ionizing radiation acts on cellular membranes to generate ceramide and initiate apoptosis. J Exp Med 180:525, 1994
45. Harmon BV, Takano YS, Winterford CM, Bove GC: The role of apoptosis in the response of cells and tumours to mild hyperthermia. Int J Radiat Biol 59:489, 1991
46. Kyprianou N, English HF, Davidson NE, Isaacs JT: Programmed cell death during regression of the MCF-7 human breast cancer following estrogen ablation. Cancer Res 51:162, 1991
47. Redding TW, Schally AV, Radulovic S, Milovanovic S, Szepeshazi K, Isaacs JT: Sustained release formulations of luteinizing hormone-releasing hormone antangonist SB-75 inhibit proliferation and enhance apoptotic cell death of human prostate carcinoma (PC-82) in male nude mice. Cancer Res 52:2538, 1992
48. D'Amico AV, McKenna WG: Apoptosis and a re-investigation of the biologic basis for cancer therapy. Radiother Oncol 33:3, 1994
49. Sen S, D'Incalci M: Apoptosis: Biochemical events and relevance to cancer chemotherapy. FEBS Lett 307:122, 1992
50. Dive C, Evans CA, Whetton AD: Induction of apoptosis-new targets for cancer chemotherapy. Cancer Biol 3:417, 1992
51. Su I-J, Cheng A-L, Tsai T-F, Lay J-D: Retinoic acid-induced apoptosis and regression of a refractory Epstein-Barr virus-containing T cell lymphoma expressing multidrug-resistance phenotypes. Br J Haematol 85:826, 1993
52. Moreira LF, Naomoto Y, Hamada M, Kamikawa Y, Orita K: Assessment of apoptosis in oesophageal cancinoma preoperatively treated by chemotherapy and radiotherapy. Anticancer Res 15:639, 1995
53. Meyn RE, Stephens LC, Hunter NR, Milas L: Apoptosis in murine tumors treated with chemotherapy agents. Anticancer Drugs 6:443, 1995
54. Meyn RE, Stephens C, Hunter NR, Milas L: Induction of apoptosis in murine tumors by cyclophosphamide. Cancer Chemother Pharmacol 33:410, 1994
55. Gorczyca W, Bigman K, Mittelman A, Ahmed T, Gong J, Melamed MR, Darzynkiewicz Z: Induction of DNA strand breaks associated with apoptosis during treatment of leukemias. Leukemia 7:659, 1993
56. Kaufmann SH, Desnoyers S, Ottaviano Y, Davidson NE, Poirier GG: Specific proteolytic cleavage of poly(ADP-ribose) polymerase: An early marker of chemotherapy-induced apoptosis. Cancer Res 53:3976, 1993
57. Lazebnik YA, Kaufmann SH, Desnoyers S, Poirier GG, Earnshaw WC: Cleavage of poly(ADP-ribose) polymerase by a proteinase with properties like ICE. Nature 371:346, 1994
58. Fernandes-Alnemri T, Litwack G, Alnemri ES: CPP32, a novel human apoptotic protein with homology to Caenorhabditis elegans cell death protein Ced-3 and mammalian interleukin-1β-converting enzyme. J Biol Chem 269:30761, 1994
59. Tewari M, Quan LT, O'Rourke K, Desnoyers S, Zeng Z, Beidler DR, Poirier GG, Salvesen GS, Dixit VM: Yama/CPP32b, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase. Cell 81:1, 1995
60. 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 376:37, 1995
61. Miyashita T, Reed JC: Bcl-2 oncoprotein blocks chemotherapy-induced apoptosis in a human leukemia cell line. Blood 81:151, 1993
62. Kamesaki S, Kamesaki H, Jorgensen TJ, Tanizawa A, Pommier Y, Cossman J: Bcl-2 protein inhibits etoposide-induced apoptosis through its effects on events subsequent to topoisomerase II-induced DNA strand breaks and their repair. Cancer Res 53:4251, 1993
63. Fairgairn LJ, Cowling GJ, Dexter TM, Rafferty JA, Margison GP, Reipert B: bcl-2 delay of alkylating agent-induced apoptotic death in a murine hemopoietic stem cell line. Mol Carcinogen 11:49, 1994
64. Lotem J, Sachs L: Control of sensitivity to induction of apoptosis in myeloid leukemic cells by differentiation and bcl-2 dependent and independent pathways. Cell Growth Diff 5:321, 1994
65. Kondo S, Yin D, Takeuchi J, Morimura T, Oda Y, Kikuchi H: bcl-2 gene enables rescue from in vitro myelosuppression (bone marrow cell death) induced by chemotherapy. Br J Cancer 70:421, 1994
66. Keith FJ, Bradbury DA, Zhu Y-M, Russell NH: Inhibition of bcl-2 with antisense oligonucleotides induces apoptosis and increases the sensitivity of AML blasts to Ara-C. Leukemia 9:131, 1995
67. Weller M, Malipiero U, Aguzzi A, Reed JC, Fontana A: Protooncogene bcl-2 gene transfer abrogates Fas/APO-1 antibody-mediated apoptosis of human malignant glioma cells and confers resistance to chemotherapeutic drugs and therapeutic irradiation. J Clin Invest 95:2633, 1995
68. Hermine O, Haioun C, Lepage E, d'Agay M-F, Briere J, Lavignac C, Fillet G, Salles G, Marolleau J-P, Diebold J, Reyes F, Gaulard P: Prognostic significance of bcl-2 protein expression in aggressive non-Hodgkin's lymphoma. Blood 87:265, 1996
69. Coustan-Smith E, Kitanaka A, Pui C-H, McNinch L, Evans WE, Raimondi SC, Behm FG, Arico M, Campana D: Clinical relevance of Bcl-2 overexpression in clinical childhood acute lympho-blastic leukemia. Blood 87:1140, 1996
70. Krajewski S, Blomqvist C, Franssila K, Krajewska M, Wasenius V-M, Niskanen E, Nordling S, Reed JC: Reduced expression of proapoptotic gene Bax is associated with poor response rates to combination chemotherapy and shorter survival in women with metastatic breast adenocarcinoma. Cancer Res 55:4471, 1995
71. Strum JC, Small GW, Pauig SB, Daniel LW: 1-β-D-arabinofuranosylcytosine stimulates ceramide and diglyceride formation in HL-60 cells. J Biol Chem 269:15493, 1994
72. Zhang J, Alter N, Reed JC, Borner C, Obeid LM, Hannun YA: Bcl-2 interrupts the ceramide-mediated pathway of cell death. Proc Natl Acad Sci USA 93:5325, 1996
73. Bose R, Verheij M, Haimovitz-Friedman A, Scotto K, Fuks Z, Kolesnick R: Ceramide synthase mediates daunorubicin-induced apoptosis: An alternative mechanism for generating death signals. Cell 82:405, 1995
74. Jaffrézou J-P, Levade T, Bettaieb A, Andrieu N, Bezombes C, Maestre N, Vermeersch S, Rousse A, Laurent G: Daunorubucin induced apoptosis: Triggering of ceramide generation through sphingomyelin hydrolysis. EMBO J 15:2417, 1996
75. Santana P, Pena LA, Haimovitz-Friedman A, Martin S, Green D, McLoughlin M, Cordon-Cardo C, Schuchman EH, Fuks Z, Kolesnick R: Acid sphingomyelinase-deficient human lymphoblasts and mice are defective in radiation-induced apoptosis. Cell 86:189, 1996
76. Lotem J, Sachs L: Hematopoietic cytokines inhibit apoptosis induced by transforming growth factor β1 and cancer chemotherapy compounds in myeloid leukemic cells. Blood 80:1750, 1992
77. Fan S, Smith ML, Rivet DJ II, Duba D, Zhan Q, Kohn KW, Fornace AJ Jr, O'Connor PM: Disruption of p53 function sensitizes breast cancer MCF-7 cells to cisplatin and pentoxifylline. Cancer Res 55:1649, 1995
78. Eliopoulos AG, Derr DJ, Herod J, Hodgkins L, Krajewski S, Reed JC, Young LS: The control of apoptosis and drug resistance in ovarian cancer: Influence of p53 and Bcl-2. Oncogene 11:1217, 1995
79. Fuchs EJ, Bedi A, Jones RJ, Hess AD: Cytotoxic T cells overcome BCR-ABL-mediated resistance to apoptosis. Cancer Res 55:463, 1995
80. Cleary ML, Smith SD, Sklar J: Cloning and structural analysis of cDNAs for bcl-2 and a hybrid bcl-2/immunoglobulin transcript resulting from the t(14; 18) translocation. Cell 47:19, 1986
81. Henderson S, Huen D, Rowe M, Dawson C, Johnson G, Rickinson A: Epstein-Barr virus-coded BHRF1 protein, a viral homologue of Bcl-2, protects human B cells from programmed cell death. Proc Natl Acad Sci USA 90:8479, 1993
82. Tarodi B, Subramanian T, Chinnadurai G: Epstein-Barr virus BHRF1 protein protects against cell death by DNA-damaging agents and heterologous viral infection. Virology 201:404, 1994
83. L is expressed in neuroblastoma cells and modulates chemotherapy-induced apoptosis. Cancer Res 55:2576, 1995
84. s sensitizes MCF-7 cells to chemotherapy-induced apoptosis. Cancer Res 55:2507, 1995
85. L can confer a multidrug resistance phenotype. Blood 86:1903, 1995
86. Nooter K, Boersma AWM, Oostrum RG, Burger H, Jochemsen AG, Stoter G: Constitutive expression of the c-H-ras oncogene inhibits doxorubicin-induced apoptosis and promotes cell survival in a rhabdomyosarcoma cell line. Br J Cancer 71:556, 1995
87. Kondo S, Barnett GH, Hara H, Morimura T, Takeuchi J: MDM2 protein confers the resistance of a human glioblastoma cell line to cisplatin-induced apoptosis. Oncogene 10:2001, 1995
88. Schwartz GK, Haimovitz-Friedman A, Dhupar SK, Ehleiter D, Maslak P, Lai L, Loganzo F Jr, Kelsen DP, Fuks Z, Albino AP: Potentiation of apoptosis by treatment with the protein kinase C-specific inhibitor Safingol in Mitomycin C-treated gastric cancer cells. J Natl Cancer Inst 87:1394, 1995
89. Yuan Z-M, Huang Y, Whang Y, Sawyers C, Weichselbaum R, Kharbanda S, Kufe D: Role for c-Abl tyrosine kinase in growth arrest response to DNA damage. Nature 382:272, 1996
90. Friesen C, Herr I, Krammer PH, Debatin KM: Involvement of the CD95 (APO-1/Fas) receptor/ligand system in drug-induced apoptosis in leukemia cells. Nat Med 2:574, 1996
91. Yuan Z-M, Huang Y, Whang Y. Sawyers C, Weichselbaum R, Kharbanda S, Kufe D: Role for c-Abl tyrosine kinase in growth arrest response to DNA damage. Nature 382:272, 1996
92. Lowe SW, Ruley HE, Jacks T, Housman DE: p53-dependent apoptosis modulates the cytotoxicity of anticancer agents. Cell 74:957, 1993
93. Kitada S, Takayama S, De Riel K, Tanaka S, Reed JC: Reversal of chemoresistance of lymphoma cells by antisense-mediated reduction of bcl-2 gene expression. Antisense Res Dev 4:71, 1994
94. Tian QS, Taupin JL, Elledge S, Robertson M, Anderson P: Fas-activated serine threonine kinase (FAST) phosphorylates TIA-1 during Fas-mediated apoptosis. J Exp Med 182:865, 1995
95. Bischoff JR, Kim DH, Williams A, Heise C, Horn S, Muna M, Ng L, Nye JA, Sampson-Johannes A, Fattaey A, McCormick F: An adenovirus mutant that replicates selectively in p53-deficient human tumor cells. Science 274:373, 1996