Death of tumor cells after intracellular acidification is dependent on stress-activated protein kinases (SAPK/JNK) pathway activation and cannot be inhibited by Bcl-2 expression or interleukin 1β-converting enzyme inhibition

Cancer Research

Volumn 58, Issue 13, 1998, Pages 2801-2808

  Zanke, Brent W ^a   Lee, Carol ^a   Arab, Sara ^a   Tannock, Ian F ^a  

^a PRINCESS MARGARET HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 1BETA CONVERTING ENZYME INHIBITOR; PROTEIN BAX; PROTEIN KINASE; SERINE PROTEINASE;

ACIDIFICATION; ANIMAL CELL; ARTICLE; CANCER CELL CULTURE; CELL CULTURE; CELL DAMAGE; CELL DEATH; CELL PH; CELL SURVIVAL; CELL VIABILITY; ENZYME ACTIVITY; ENZYME INHIBITION; GENE EXPRESSION; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTO ONCOGENE; SIGNAL TRANSDUCTION; TUMOR CELL;

ANIMALS; ANTI-BACTERIAL AGENTS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CASPASE 1; CELL DEATH; CELL LINE; CYSTEINE ENDOPEPTIDASES; HUMANS; HYDROGEN-ION CONCENTRATION; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MAP KINASE KINASE 4; MICE; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; MITOGEN-ACTIVATED PROTEIN KINASES; NIGERICIN; PROTEIN KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2;

EID: 0032126479     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (65)

1. Vaupel, P., Kallinowsky, F., and Okunieff, P. Blood flow, oxygen and nutrient supply, and metabolic microenvironment of human tumors: a review. Cancer Res., 49: 6449-6465, 1989.
2. Wike-Hooley, J. L., Haveman, J., and Reinhold, J. S. The relevance of tumor pH to the treatment of malignant disease. Radiother. Oncol., 2: 343-366, 1984.
3. Hochachka, P. W., and Mommsen, T. P. Protons and anaerobiosis. Science (Washington DC), 219: 1391-1397, 1983.
4. 2 gradients in solid tumors in vivo: high-resolution measurements reveal a lack of correlation. Nat. Med., 3: 177-182, 1997.
5. Daly, P. G., and Cohen, J. S. Magnetic resonance spectroscopy of tumors and potential in vivo clinical applications: a review. Cancer Res., 49: 770-779, 1989.
6. Maidorn, R. P., Cragoe, E. J., Jr., and Tannock, I. F. Therapeutic potential of analogues of amiloride: inhibition of the regulation of intracellular pH as a possible mechanism of tumour selective therapy. Br. J. Cancer, 67: 297-303, 1993.
7. Yamagata, M., and Tannock, I. F. The chronic administration of drugs that inhibit the regulation of intracellular pH: in vitro and anti-tumour effects. Br. J. Cancer, 73: 1328-1334, 1996.
8. Park, H. J., Makepeace, C. M., Lyons, J. C., and Song, C. W. Effect of intracellular acidity and ionomycin on apoptosis in HL-60 cells. Eur. J. Cancer, 32A: 540-546, 1996.
9. Barry, M. A., and Eastman, A. Identification of deoxyribonuclease II as an endonuclease involved in apoptosis. Arch. Biochem. Biophys., 300: 440-450, 1993.
10. 2+ and pH. Biochem. Biophys. Res. Commun., 186: 782-789, 1992.
11. Rebollo, A., Gomez, J., Martinez de Aragon, A., Lastres, P., Silva, A., and Perez-Sala, D. Apoptosis induced by IL-2 withdrawal is associated with an intracellular acidification. Exp. Cell Res., 218: 581-585, 1995.
12. + antiporter, glycoprotein of 110 kDa. Science (Washington DC), 247: 723-726, 1990.
13. + exchanger of sea urchin eggs by phorbol ester. Nature (Lond.), 314: 274-277, 1985.
14. Gottlieb, R. A., Nordberg, J., Skowronski, E., and Babior, B. M. Apoptosis induced in Jurkat cells by several agents is preceded by intracellular acidification. Proc. Natl. Acad. Sci. USA, 93: 654-658, 1996.
15. Kyriakis, J. M., Banerjee, P., Nikolakaki, E., Dai, T., Rubie, E. A., Ahmad, M. F., Avruch, J., and Woodgett, J. R. The stress-activated protein kinase subfamily of c-Jun kinases. Nature (Lond.), 369: 156-160, 1994.
16. Davis, R. J. MAPKs: new JNK expands the group. Trends Biochem. Sci., 19: 470-473, 1994.
17. Kharbanda, S., Ren, R., Pandey, P., Shafman, T. D., Feller, S. M., Weichselbaum, R. R., and Kufe, D. W. Activation of the c-Abl tyrosine kinase in the stress response to DNA-damaging agents. Nature (Lond.), 376: 785-788, 1995.
18. Lin, A., Minden, A., Martinetto, H., Claret, F., Lange-Carter, C., Mercurio, F., Johnson, G., and Karin, M. Identification of a dual specificity kinase that activates the jun kinases and p38-mpk2. Science (Washington DC), 268: 286-290, 1995.
19. Sanchez, I., Hughes, R. T., Mayer, B. J., Yee, K., Woodgett, J. R., Avruch, J., Kyriakis, J. M., and Zon, L. I. Role of SAPK/ERK kinase-1 in the stress-activated pathway regulating transcription factor c-Jun. Nature (Lond.), 372: 794-798, 1994.
20. Yan, M., Dai, T., Deak, J. C., Kyriakis, J. M., Zon, L. I., Woodgett, J. R., and Templeton, D. J. Activation of stress-activated protein kinase by MEKK1 phosphorylation of its activator SEK1. Nature (Lond.), 372: 798-800, 1994.
21. Yan, M., and Templeton, D. J. Identification of 2 serine residues of MEK-1 that are differentially phosphorylated during activation by raf and MEK kinase. J. Biol. Chem., 269: 19067-19073, 1994.
22. Zanke, B. W., Boudreau, K., Rubie, E., Winnett, E., Tibbles, L. A., Zon, L. I., Kyriakis, J. M., Liu, F-F., and Woodgett, J. R. The stress-activated protein kinase pathway mediates cell death following injury induced by cis-platinum, UV irradiation or heat. Curr. Biol., 6: 606-613, 1996.
23. Chen, Y. R., Wang, X., Templeton, D., Davis, R. J., and Tan, T. H. The role of c-Jun N-terminal kinase (JNK) in apoptosis induced by ultraviolet C and γ radiation. J. Biol. Chem., 271: 31929-31936, 1996.
24. Bossy-Wetzel, E., Bakiri, L., and Yaniv, M. Induction of apoptosis by the transcription factor c-Jun. EMBO J., 16: 1695-1709, 1997.
25. Xia, Z., Dickens, M., Raingeaud, J., Davis, R. J., and Greenberg, M. E. Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science (Washington DC), 270: 1326-1331, 1995.
26. Park, D. S., Stefanis, L., Yan, C. Y. I., Farinelli, S. E., and Greene, L. A. Ordering the cell death pathway. J. Biol. Chem., 271: 21898-21905, 1996.
27. 2-terminal kinasemediated activation of interleukin-1β-converting enzyme/CED-3-like protease during anticancer drug-induced apoptosis. J. Biol. Chem., 272: 4631-4636, 1997.
28. Cahill, M. A., Peter, M. E., Kischkel, F. C., Chinnaiyan, A. M., Dixit, V. M., Krammer, P. H., and Nordheim, A. CD95 (APO-1/Fas) induces activation of SAP kinases downstream of ICE-like proteases. Oncogene, 13: 2087-2096, 1996.
29. Enari, M., Hug, H., and Nagata, S. Involvement of an ICE-like protease in Fasmediated apoptosis. Nature (Lond.), 375: 78-81, 1995.
30. Los, M., Van de Craen, M., Penning, L. C., Schenk, H., Westendorp, M., Baeuerle, P. A., Droge, W., Krammer, P. H., Fiers, W., and Schulze-Osthoff, K. Requirement of an ICE/CED-3 protease for Fas/APO-1-mediated apoptosis. Nature (Lond.), 375: 81-83, 1995.
31. Marsters, S. A., Pitti, R. M., Donahue, C. J., Ruppert, S., Bauer, K. D., and Ashkenazi, A. Activation of apoptosis by Apo-2 ligand is independent of FADD but blocked by CrmA. Curr. Biol., 6: 750-752, 1996.
32. Bodmer, J. L., Burns, K., Schneider, P., Hofmann, K., Steiner, V., Thome, M., Bomand, T., Hahne, M., Schroter, M., Becker, K., Wilson, A., French, L. E., Browning, J. L., MacDonald, H. R., and Tschopp, J. TRAMP, a novel apoptosis-mediating receptor with sequence homology to tumor necrosis factor receptor 1 and Fas(Apo-1/CD95). Immunity, 6: 79-88, 1997.
33. Hartfield, P. J., Mayne, G. C., and Murray, A. W. Ceramide induces apoptosis in PC12 cells. FEES Lett., 401: 148-152, 1997.
34. Chen, Z., Naito, M., Mashima, T., and Tsuruo, T. Activation of actin-cleavable interleukin 1β-converting enzyme (ICE) family protease CPP-32 during chemotherapeutic agentinduced apoptosis in ovarian carcinoma cells. Cancer Res., 56: 5224-5229, 1996.
35. Iversen, P. O., Hercus, T. R., Zacharakis, B., Woodcock, J. M., Stomski, F. C., Kumar, S., Nelson, B. H., Miyajima, A., and Lopez, A. F. The apoptosis-inducing granulocyte macrophage colony-stimulating factor (GM-CSF) analog E21R functions through specific regions of the heterodimeric GM-CSF receptor and requires interleukin-1β-converting enzyme-like proteases. J. Biol. Chem., 272: 9877-9883, 1997.
36. Martin, S. J., Amarante-Mendes, G. P., Shi, L., Chuang, T. H., Casiano, C. A., O'Brien, G. A., Fitzgerald, P., Tan, E. M., Bokoch, G. M., Greenberg, A. H., and Green, D. R. The cytotoxic cell protease granzyme B initiates apoptosis in a cell-free system by proteolytic processing and activation of the ICE/CED-3 family protease, CPP32, via a novel two-step mechanism. EMBO J., 15: 2407-2416, 1996.
37. Varnes, M. E., Glazier, K. G., and Gray, C. pH-dependent effects of the ionophore nigericin on response of mammalian cells to radiation and heat treatment. Radiat. Res., 117: 282-292, 1989.
38. Boyer, M. J., Horn, I., Firestone, R. A., Steele-Norwood, D., and Tannock, I. F. pH dependent cytotoxicity of N-dodecylimidazole: a compound that acquires detergent properties under acidic conditions. Br. J. Cancer, 67: 81-87, 1993.
39. Wood, P. J., Sansom, J. M., Newell, K., Tannock, I. F., and Stratford, I.J. Reduction of tumour intracellular pH and enhancement of melphalan cytotoxicity by the ionophore nigericin. Int. J. Cancer, 60: 264-268, 1995.
40. Ambinder, R. F., and Griffin, C. A. Biology of the lymphomas: cytogenetics, molecular biology, and virology. Curr. Opin. Oncol., 3: 806-812, 1991.
41. May, W. S., Tyler, P. G., Ito, T., Armstrong, D. K., Qatsha, K. A., and Davidson, N. E. Interleukin-3 and bryostatin-1 mediate J. Biol. Chem., 269: 26865-26870, 1994.
42. Fairgairn, L. J., Cowling, G. J., Dexter, T. M., Rafferty, J. A., Margison, G. P., and Reipert, B. Bcl-2 delay of alkylating agent-induced apoptotic death in a murine hemopoietic stem cell line. Mol. Carcinog., 11: 49-55, 1994.
43. Dole, M., Nuñez, G., Merchant, A. K., Maybaum, J., Rode, C. K., Bloch, C. A., and Castle, V. P. Bcl-2 inhibits chemotherapy-induced apoptosis in neuroblastoma. Cancer Res., 54: 3253-3259, 1994.
44. Reed, J. C. BCL-2: prevention of apoptosis as a mechanism of drug resistance. Hematol. Oncol. Clin. N. Am., 9: 451-473, 1995.
45. Oltvai, Z. N., Milliman, C. L., and Korsmeyer, S. J. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell, 74: 609-619, 1993.
46. Salvesen, G. S., and Dixit, V. M. Caspases. Intracellular signaling by proteolysis. Cell, 91: 443-446, 1997.
47. Dolle, R. E., Singh, J., Rinker, J., Hoyer, D., Prasad, C. V., Graybill, T. L., Salvino, J. M., Helaszek, C. T., Miller, R. E., and Ator, M. A. Aspartyl α-((1-phenyl-3-(trifluororoethyl)-pyrazol-5-yl)oxy)methyl ketones as interleukin-1β-converting enzyme inhibitors. Significance of the P1 and P3 amido nitrogens for enzyme-peptide inhibitor binding. J. Med. Chem., 37: 3863-3866, 1994.
48. Loddick, S. A., MacKenzie, A., and Rothwell, N. J. An ICE inhibitor, z-VAD-DCB, attenuates ischaemic brain damage in the rat. Neuroreport, 7: 1465-1468, 1996.
49. Luo, J., and Tannock, I. F. Inhibition of the regulation of intracellular pH: potential of 5-(N,N-hexamethylene) amiloride in tumour-selective therapy. Br. J. Cancer, 70: 617-624, 1994.
50. Barry, M. A., Reynolds, J. E., and Eastman, A. Etoposide-induced apoptosis in human HL-60 cells is associated with intracellular acidification. Cancer Res., 53: 2349-2357, 1993.
51. Gottlieb, R. A., Nordberg, J., Skowronski, E., and Babior, B. M. Apoptosis induced in Jurkat cells by several agents is preceded by intracellular acidification. Proc. Natl. Acad. Sci. USA. 93: 654-658, 1996.
52. Perez-Sala, D., Collado-Escobar, D., and Mollinedo, F. Intracellular alkalinization suppresses lovastatin-induced apoptosis in HL-60 cells through the inactivation of a pH-dependent endonuclease. J. Biol. Chem., 270: 6235-6242, 1995.
53. Walton, M. I., Whysong, D., O'Connor, P. M., Hockenbery, D., Korsmeyer, S. J., and Kohn, K. W. Constitutive expression of human Bcl-2 modulates nitrogen mustard and camptothecin induced apoptosis. Cancer Res., 53: 1853-1861, 1993.
54. Fisher, T. C, Milner, A. E., Gregory, C. D., Jackman, A. L., Aherne, G. W., Hartley, J. A., Dive, C., and Hickman, J. A. bcl-2 modulation of apoptosis induced by anticancer drugs: resistance to thymidylate stress is independent of classical resistance pathways. Cancer Res., 53: 3321-3326, 1993.
55. Miyashita, T., and Reed, J. C. 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., 52: 5407-5411, 1992.
56. Hockenbery, D. M., Oltvai, Z. N., Yin, X-M., Milliman, C. L., and Korsmeyer, S. J. Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell, 75: 241-251, 1993.
57. Korsmeyer, S. J. Bcl-2 initiates a new category of oncogenes: Regulators of cell death. Blood, 80: 879-886, 1992.
58. L and Bcl-2, displaces Bax and promotes cell death. Cell, 80: 285-291, 1995.
59. Yin, X. M., Oltvai, Z. N., and Korsmeyer, S. J. BH1 and BH2 domains of Bcl-2 are required for inhibition of apoptosis and heterodimerization with Bax. Nature (Lond.), 369: 321-323, 1994.
60. Knudson, C. M., and Korsmeyer, S. J. Bcl-2 and Bax function independently to regulate cell death. Nat. Genet., 16: 358-363, 1997.
61. Yuan, J., Shaham, S., Ledoux, S., Ellis, H. M., and Horvitz, H. R. The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1β-converting enzyme. Cell, 75: 641-652, 1993.
62. Oltvai, Z. N., and Korsmeyer, S. J. Checkpoints of dueling dimers foil death wishes. Cell, 79: 189-192, 1994.
63. Nicholson, D. W., Ali, A., Thornberry, N. A., Vaillancourt, J. P., Ding, C. K., Gallant, M., Gareau, Y., Griffin, P. R., Labelle, M., and Lazebnik, Y. A. Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature (Lond.), 376: 37-43, 1995.
64. Weaver, D. T. What to do at an end: DNA double-strand-break repair. Trends Genet., 11: 388-392, 1995.
65. Schreiber, V., Hunting, D., Trucco, C., Gowans, B., Grunwald, D., De Murcia, G., and De Murcia, J. M. A dominant-negative mutant of human poly(ADP-ribose) polymerase affects cell recovery, apoptosis, and sister chromatid exchange following DNA damage. Proc. Natl. Acad. Sci. USA, 92: 4753-4757, 1995.