Effects of calcium channel blockers on cellular apoptosis: Implications for carcinogenic potential

Cancer

Volumn 85, Issue 10, 1999, Pages 2093-2102

  Mason, R Preston ^a  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

Apoptosis; Calcium channel blockers; Carcinogenic potential

Indexed keywords

CALCIUM CHANNEL BLOCKING AGENT; CALCIUM ION; MAGNESIUM;

APOPTOSIS; CALCIUM ANTAGONISM; CANCER RISK; CARCINOGENICITY; HUMAN; HUMAN CELL; HYPERTENSION; HYPOTHESIS; PRIORITY JOURNAL; REVIEW; RISK ASSESSMENT; TUMOR PROMOTION;

APOPTOSIS; CALCIUM CHANNEL BLOCKERS; CELL TRANSFORMATION, NEOPLASTIC; HUMANS; HYPERTENSION; NEOPLASMS; RISK ASSESSMENT;

EID: 0000143718     PISSN: 0008543X     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-0142(19990515)85:10<2093::AID-CNCR1>3.0.CO;2-E     Document Type: Review

References (90)

1. Pahor M, Guralnik JM, Salive ME, Corti MC, Carbonin P, Havlik RJ. Do calcium channel blockers increase the risk of cancer? Am J Hypertens 1996;9:695-9.
2. Pahor M, Guralnik JM, Ferrucci L, Corti MC, Salive ME, Cerhan JR, et al. Calcium-channel blockade and incidence of cancer in aged populations. Lancet 1996;348:493-7.
3. Fitzpatrick AL, Daling JR, Furberg CD, Kronmal RA, Weissfeld JL. Use of calcium channel blockers and breast carcinoma risk in postmenopausal women. Cancer 1997; 80:1438-47.
4. Daling JR. Calcium channel blockers and cancer: is an association biologically plausible? Am J Hypertens 1996;9: 713-4.
5. Weinmann S, Glass AG, Weiss NS, Psaty BM, Siscovick DS, White E. Use of diuretics and other antihypertensive medications in relation to the risk of renal cell cancer. Am J Epidemiol 1994;140:792-804.
6. Chow WH, McLaughlin JK, Mandel JS, Wacholder S, Niwa S, Fraumeni JF Jr. Risk of renal cell cancer in relation to diuretics, antihypertensive drugs, and hypertension. Cancer Epidemiol Biomarkers Prev 1995;4:327-31.
7. Mellemgaard A, Moller H, Olsen JH. Diuretics may increase risk of renal cell carcinoma. Cancer Causes Control 1992;3: 309-12.
8. Mellemgaard A, Niwa S, Mehl ES, Engholm G, McLaughlin JK, Olsen JH. Risk factors for renal cell carcinoma in Denmark: role of medication and medical history. Int J Epidemiol 1994;23:923-30.
9. McLaughlin JK, Chow WH, Mandel JS, Mellemgaard A, McCredie M, Lindblad P, et al. International renal-cell cancer study. VIII. Role of diuretics, other antihypertensive medications and hypertension. Int J Cancer 1995;63: 216-21.
10. Finkle WD, McLaughlin JK, Rasgon SA, Yeoh HH, Low JE. Increased risk of renal cell cancer among women using diuretics in the United States. Cancer Causes Control 1993; 4:555-8.
11. Hiatt RA, Tolan K, Quesenberry CPJ. Renal cell carcinoma and thiazide use: a historical case-control study (California, USA). Cancer Causes Control 1994;5:319-25.
12. Hole DJ, Hawthorne VM, Isles CG, McGhee SM, Robertson JW, Gillis CR, et al. Incidence of and mortality from cancer in hypertensive patients. BMJ 1993;306:609-11.
13. Hamet P. Cancer and hypertension: an unresolved issue. Hypertension 1996;28:321-4.
14. 2+ channels exposed to serum from patients with type I diabetes. Science 1993;261:86-90.
15. Li LH, Wine RN, Miller DS, Reece JM, Smith M, Chapin RE. Protection against methoxyacetic-acid-induced spermatocyte apoptosis with calcium channel blockers in cultured rat seminiferous tubules: possible mechanisms. Toxicol Appl Pharmacol 1997;144:105-19.
16. Connor J, Sawczuk IS, Benson MC, Tomashefsky P, O'Toole KM, Olsson CA, et al. Calcium channel antagonists delay regression of androgen-dependent tissues and suppress gene activity associated with cell-death. Prostate 1988;13: 119-30.
17. 2+-dependent endonuclease as an early event in castration-induced prostatic cell death. Prostate 1988;13: 103-17.
18. el-Azzouzi B, Tsangaris GT, Pellegrini O, Manuel Y, Benveniste J, Thomas Y. Cadmium induces apoptosis in a human T cell line. Toxicology 1994;88:127-39.
19. Escargueil-Blanc I, Meilhac O, Pieraggi MT, Arnal JF, Salvayre R, Negre-Salvayre A. Oxidized LDLs induce massive apoptosis of cultured human endothelial cells through a calcium-dependent pathway: prevention by aurintricarboxylic acid. Arterioscler Thromb Vasc Biol 1997; 17:331-9.
20. Leszczynski D, Zhao Y, Luokkamaki M, Foegh ML. Apoptosis of vascular smooth muscle cells: protein kinase C and oncoprotein Bcl-2 are involved in regulation of apoptosis in non-transformed rat vascular smooth muscle cells. Am J Pathol 1994;145:1265-70.
21. Balakumaran A, Campbell GA, Moslen MT. Calcium channel blockers induce thymic apoptosis in vivo in rats. Toxicol Appl Pharmacol 1996;139:122-7.
22. Galli C, Meucci O, Scorziello A, Werge TM, Calissano P, Schettini G. Apoptosis in cerebellar granule cells is blocked by high KCl, forskolin and IGF-1 through distinct mechanisms of action: the involvement of intracellular calcium and RNA synthesis. J Neurosci 1995;15:1172-9.
23. 2+ determine nerve growth factor dependence of sympathetic ganglion cells. Proc Natl Acad Sci U S A 1989;86:6421-5.
24. Shchepotin IB, Soldatenkov V, Buras RR, Nauta RJ, Shabahang M, Evans SR. Apoptosis of human primary and metastatic colon adenocarcinoma cell lines in vitro induced by 5-fluorouacil, verapamil, and hyperthermia. Anticancer Res 1994;14:1027-31.
25. Shamash J, Davies DC, Lister TA. Apoptosis and cell proliferation control induced by pulsed calcium channel blockade in a low grade lymphoma cell line expressing BCL-2. Blood 1994;84:448A.
26. Kondo S, Yin D, Morimura T, Takeuchi J. Combination therapy with cisplatin and nifedipine inducing apoptosis in multidrug-resistant human glioblastoma cells. J Neurosurg 1995;82:469-74.
27. Uehara H, Nakaizumi A, Baba M, Iishi H, Tatsuta M. Inhibition by Verapamil of hepatocarcinogenesis induced by N-nitrosomorpholine in Sprague-Dawley rats. Br J Cancer 1993;68:37-40.
28. Bertrand V, Bastle MJ, Vaysse N, Pradayrol L. Inhibition of gastrin-induced proliferation of AR4-2J cells by calcium channel antagonists. Int J Cancer 1994;56:427-32.
29. Tsuruo T, Iida H, Makishima F, Yamori T, Kawabata H, Tsukagoshi S, et al. Inhibition of spontaneous and experimental tumor metastasis by the calcium antagonist verapamil. Cancer Chemother Pharmacol 1985;14:30-3.
30. Juraskova V, Sladek T. Antimetastatic action of diltiazem on LS/BL tumor cells in liver tumor-colony assay. Neoplasma 1990;37:343-8.
31. Batra S, Popper LD, Hartley-Asp B. Effect of calcium and calcium antagonists on 45Ca influx and cellular growth of human prostatic tumor cells. Prostate 1991;19:299-311.
32. Sato K, Ishizuka J, Cooper CW, Chung DH, Tsuchiya T, Uchida T, et al. Inhibitory effect of calcium channel blockers on growth of pancreatic cancer cells. Pancreas 1994;9:193-202.
33. 2+-channel blocker verapamil on human lung cancer cell lines. Carcinogenesis 1991;12:2301-3.
34. Taylor JM, Simpson RU. Inhibition of cancer cell growth by calcium channel antagonists in the athymic mouse. Cancer Res 1992;52:2413-8.
35. Anundi I. Calcium antagonists and cancer: what do studies of animals used in experiments show? Information from the Swedish Drug Administration 1997;8:1-4.
36. Ahr HJ, Bomhard E, Mager H, Schluter G. Calcium channel blockers and cancer is there preclinical evidence for an association? Cardiology 1997;88(Suppl 3):68-72.
37. Borhani NO, Mercuri M, Borhani PA, Buckalew VM, Canossa-Terris M, Carr AA, et al. Final outcome results of the Multicenter Isradipine Diuretic Atherosclerosis Study (MIDAS): a randomized controlled trial. JAMA 1996;276:785-91.
38. Gong L, Zhang W, Zhu Y, Zhu J, Kong D, Page V, et al. Shanghai trial of nifedipine in the elderly (STONE). J Hypertens 1996;14:1237-45.
39. Jonas M, Goldbourt U, Boyko V, Mandelzweig L, Behar S, Reicher-Reiss H. Nifedipine and cancer mortality: Ten year mortality follow-up of 4808 patients after acute myocardial infarction. Cardiovasc. Drugs Ther. 1998;12:177-81.
40. Rosenberg L, Sowmya-Rao R, Palmer JR, Strom BL, Stolley PD, Zauber AG, et al. Calcium channel blockers and the risk of cancer. JAMA 1998;279:1000-4.
41. Lever AF, Hole D, McKinnin P, Gillis C, McInnes GT, Meredith PA, et al. Cancer risk is not increased in Glasgow patients taking calcium channel blockers. Cardiovascular Centres of Excellence Meeting, 1997.
42. Husten L. Calcium antagonists found "not guilty." Lancet 1997;349:1818.
43. Olsen JH, Toft-Sorensen HT, Friis S, McLaughlin JK, Steffensen FH, Nielsen GL, et al. Cancer risk in users of calcium channel blockers. Hypertension 1997;29:1091-4.
44. Michels KB, Rosner BA, Walker AM, Stampfer MJ, Manson JE, Colditz GA, et al. Calcium channel blockers, cancer incidence, and cancer mortality in a cohort of U.S. women. Cancer 1998;83:2003-7.
45. Staessen JA, Fagard R, Thijs L, Celis H, Arabidze GG, Birkenhager WH, et al. Randomised double-blind comparison of placebo and active treatment for older patients with isolated systolic hypertension. Lancet 1997;350:757-64.
46. Trenkwalder P, Hendricks P, Hense H-W. Treatment with calcium antagonists does not increase the risk of fatal or non-fatal cancer in an elderly mid-European population: Results from STEPHY II. J. Hypertens. 1998;16:1113-6.
47. Mason RP. Calcium channel blockers and cancer: a biological link remains elusive [letter]. Am J Hypertens 1996;9: 1047-9.
48. Wyllie AH, Kerr JF, Currie AR. Cell death: the significance of apoptosis. Int Rev Cytol 1980;68:251-306.
49. Margolis RL, Chuang DM, Post RM. Programmed cell death: implications for neuropsychiatric disorders. Biol Psychiatry 1994;35:946-56.
50. Olivetti G, Abbi R, Quaini F, Kajstura J, Cheng W, Nitahara JA, et al. Apoptosis in the failing human heart. N Engl J Med 1997;336:1131-41.
51. Goodman Y, Bruce AJ, Cheng B, Mattson MP. Estrogens attenuate and corticosterone exacerbates exitotoxicity, oxidative injury, and amyloid b-peptide toxicity in hippocampal neurons. J Neurochem 1996;66:1836-44.
52. Misao J, Hayakawa Y, Ohno M, Kato S, Fujiwara T, Fujiwara H. Expression of bcl-2 protein, an inhibitor of apoptosis, and Bax, an accelerator of apoptosis, in ventricular myocytes of human hearts with myocardial infarction. Circulation 1996; 94:1506-12.
53. deBlois D, Tea BS, Than VD, Tremblay J, Hamet P. Smooth muscle apoptosis during vascular regression in spontaneously hypertensive rats. Hypertension 1997;29:340-9.
54. Narula J, Haider N, Virmani R, DiSalvo TG, Kolodgie FD, Hajjar RJ, et al. Apoptosis in myocytes in end-stage heart failure. N Engl J Med 1996;335:1182-9.
55. Mallat Z, Tedgui A, Fontaliran F, Frank R, Durigon M, Fontaine G. Evidence of apoptosis in arrhythmogenic right ventricular dysplasia. N Engl J Med 1996;335:1190-6.
56. Gottlieb RA, Burleson KO, Kloner RA, Babior BM, Engler RL. Reperfusion injury induces apoptosis in rabbit cardiomyocytes. J Clin Invest 1994;94:1621-8.
57. Liu Y, Cigola E, Cheng W, Kajstura J, Olivetti G, Hintze TH, et al. Myocyte nuclear mitotic division and programmed myocyte cell death characterize the cardiac myopathy induced by rapid ventricular pacing in dogs. Lab Invest 1995; 73:771-87.
58. Hamet P, Richard L, Dam TV, Teiger E, Orlov SN, Gaboury L, et al. Apoptosis in target organs of hypertension. Hypertension 1995;26:642-8.
59. Sharov VG, Sabbah HN, Shimoyama H, Goussev AV, Lesch M, Goldstein S. Evidence of cardiocyte apoptosis in myocardium of dogs with chronic heart failure. Am J Pathol 1996;148:141-9.
60. Teiger E, Than VD, Richard L, Wisnewsky C, Tea BS, Gaboury L, et al. Apoptosis in pressure overload-induced heart hypertrophy in the rat. J Clin Invest 1996;97:2891-7.
61. Trump BF, Berezesky IK. Calcium-mediated cell injury and cell death. FASEB J 1995;9:219-28.
62. Kluck RM, McDougall CA, Harmon BV, Halliday JW. Calcium chelators induce apoptosis: evidence that raised intracellular ionised calcium is not essential for apoptosis. Biochim Biophys Acta 1994;1223:247-54.
63. Zhu W-H, Loh T-T. Roles of calcium in the regulation of apoptosis in HL-60 promyelocytic leukemia cells. Life Sci 1995;57:2091-9.
64. Rodriguez-Tarduchy G, Malde P, Lopez-Rivas A, Collins MK. Inhibition of apoptosis by calcium ionophores in IL-3-dependent bone marrow cells is dependent upon production of IL-4+. J Immunol 1992;148:1416-22.
65. Nicotera P, Zhivotovsky B, Orrenius S. Nuclear calcium transport and the role of calcium in apoptosis. Cell Calcium 1994;16:279-88.
66. Martikainen P, Isaacs J. Role of calcium in the programmed death of rat prostatic glandular cells. Prostate 1990;17:175-87.
67. Yoshino N, Takizawa M, Akiba H, Okumura H, Tashiro F, Honda M, et al. Transient elevation of intracellular calcium ion levels as an early event in T-2 toxin-induced apoptosis in human promyelotic cell line HL-60. Nat Toxins 1996;4:234-41.
68. Whitfield JF. Calcium signals and cancer. Crit Rev Oncog 1992;3:55-90.
69. 2+ are not required to trigger apoptosis in human leukaemia cells. Clin Exp Immunol 1992;87:465-71.
70. Reynolds JE, Li J, Craig RW, Eastman A. BCL-2 and MCL-1 expression in Chinese hamster ovary cells inhibits intracellular acidification and apoptosis induced by staurosporine. Exp Cell Res 1996;225:430-6.
71. Wright SC, Zhong J, Zheng H, Larrick JW. Nicotine inhibition of apoptosis suggests a role in tumor progression. FASEB J 1993;7:1045-51.
72. Yonish-Rouach E, Resnitzky D, Lotem J, Sachs L, Kimchi A, Oren M. Wild-type p53 induces apoptosis of myeloid leukaemic cells that is inhibited by interleukin-6. Nature 1991; 352:345-7.
73. Driscoll M, Chalfie M. Developmental and abnormal cell death in C elegans. Trends Neurosci. 1992;15:15-9.
74. Correale P, Tagliaferri P, Celio L, Genua G, Montagnani S, Bianco AR. Verapamil up-regulates sensitivity of human colon and breast cancer cells to LAK cytotoxicity in vitro. Eur J Cancer 1991;27:1393-5.
75. Tatsuta M, Iishi H, Baba M, Nakaizumi A, Uehara H, Taniguchi H. Effect of calcium channel blockers on gastric carcinogenesis and caerulein enhancement of gastric carcinogenesis induced by N-methyl-N′-nitro-N-nitrosoguanidine in Wistar rats. Cancer Res 1990;50:2095-8.
76. Battalora MS, Johnston DA, DiGiovanni J. The effects of calcium antagonists on anthrone skin tumor promotion and promoter-related effects in SENCAR mice. Cancer Lett 1995; 98:19-25.
77. Helson L. Calcium channel blocker enhancement of anticancer drug cytotoxicity: a review. Cancer Drug Deliv 1984; 1:353-61.
78. Cano-Gauci DF, Riordan JR. Action of calcium antagonists on multidrug resistant cells: specific cytotoxicity independent of increased cancer drug accumulation. Biochem Pharmacol 1987;36:2115-23.
79. Cornwell MM, Pastan I, Gottesman MM. Certain calcium channel blockers bind specifically to multidrug-resistant human KB carcinoma membrane vesicles and inhibit drug binding to P-glycoprotein. J Biol Chem 1987;262: 2166-70.
80. Hargrave RM, Davey MW, Davey RA, Kidman AD. Development of drug resistance is reduced with idarubicin relative to other anthracyclines. Anticancer Drugs 1995;6:432-7.
81. Chauffert B, Pelletier H, Corda C, Solary E, Bedenne L, Caillot D, et al. Potential usefulness of quinine to circumvent the anthracycline resistance in clinical practice. Br J Cancer 1990;62:395-7.
82. Timcheva CV, Todorov DK. Does verapamil help overcome multidrug resistance in tumor cell lines and cancer patients? J Chemother 1996;8:295-9.
83. Yeh GC, Lopaczynska J, Poore CM, Phang JM. A new functional role for P-glycoprotein: efflux pump for benzo(alpha) pyrene in human breast cancer MCF-7 cells. Cancer Res 1992;52:6692-5.
84. Phang JM, Poore CM, Lopaczynska J, Yeh GC. Flavonol-stimulated efflux of 7,12-dimethylbenz(a)anthracene in multidrug-resistant breast cancer cells. Cancer Res 1993;53: 5977-81.
85. 2+ channels. Kidney Int 1996;49:868-79.
86. Smith BM, Gindhart TD, Colburn NH. Extracellular calcium requirement for promotion of transformation in JB6 cells. Cancer Res 1986;46:701-6.
87. Braun S, Boyko V, Behar S, Reicher-Reiss H, Laniado S, Kaplinsky E, et al. Calcium channel blockers and cancer-related mortality in patients with coronary artery disease: a cohort study of 11575 patients. J Am Coll Cardiol 1998;31: 804-8.
88. Jick H, Jick S, Derby LE, et al. Calcium-channel blockers and risk of cancer. Lancet 1997;349:525-8.
89. Messerli FH, Grossman E. Do calcium antagonists increase the risk for malignancies? J. Am. Coll. Cardiol. 1998;31:809-10.
90. Dong EW, Connelly JE, Borden SP, Yorzyk W, Passov DG, Kupelnick B, Luo D, Ross SD. A systematic review and meta-analysis of the incidence of cancer in randomized, controlled trials of verapamil. Pharmacotherapy 1997;17: 1210-9.