Enhanced expression of p53 and apoptosis induced by blockade of the vacuolar proton ATPase in cardiomyocytes

Journal of Clinical Investigation

Volumn 101, Issue 6, 1998, Pages 1453-1461

  Long, Xilin ^a   Crow, Michael T ^a   Sollott, Steven J ^a   O'Neill, Lydia ^a   Menees, Daniel S ^a   Hipolito, Maria De Lourdes ^a   Boluyt, Marvin O ^a   Asai, Toshinobu ^a   Lakatta, Edward G ^a  

^a NATIONAL INSTITUTE ON AGING   (United States)

Author keywords

Apoptosis; Bafilomycin A1; Cardiac myocyte; Vacuolar proton ATPase

Indexed keywords

BAFILOMYCIN; CYCLINE; DNA; ENZYME INHIBITOR; MESSENGER RNA; PHOSPHOTRANSFERASE; PROTEIN P53; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL VACUOLE; ENZYME INHIBITION; HEART MUSCLE CELL; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

EID: 0032520924     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI345     Document Type: Article

References (41)

1. Arends, M.J., and A.H. Wyllie. 1991. Apoptosis: mechanisms and roles in pathology, Int. Rev. Exp. Pathol. 32:223-254.
2. Ucker, D.S. 1991. Death by suicide; one way to go in mammalian cellular development? New Biol. 3:103-109.
3. Arends, M.J., R.G. Morris, and A.M. Wyllie. 1990. Apoptosis: the role of the endonuclease. Am. J. Pathol. 136:593-608.
4. Bursch, W., L. Kleine, and M. Tenniswood. 1990. The biochemistry of cell death by apoptosis. Biochem. Cell. Biol. 68:1071-1074.
5. Tanaka, M., H. Ito, S. Adachi, H. Akimoto, T. Nishikawa, T. Kasajima, F. Marumo, and M. Hiroe. 1994. Hypoxia induces apoptosis with enhanced expression of Fas antigen messenger RNA in cultured neonatal rat cardiomyocytes. Circ. Res. 75:426-433.
6. Gottleib. R.A., K.O. Burleson, R.A. Kloner, B.M. Babior, and R.L. Engler. 1994. Reperfusion injury induces apoptosis in rabbit cardiomyocytes. J. Clin. Invest. 94:1621-1628.
7. Kajstura, J., W. Cheng, and K. Reiss. 1996. Apoptotic and necrotic myocyte cell deaths are independent contributing variables of infarct size in rats. Lab. Invest. 74:86-107.
8. Cheng, W., B. Li, and J. Kajstura. 1995. Stretch-induced programmed myocyte cell death. J. Clin. Invest. 96:2247-2259.
9. Teiger, E., V.D. Than, and L. Richard. 1996. Apoptosis in pressure overload-induced heart hypertrophy in the rat. J. Clin. Invest. 97:2891-2897.
10. Li, Z., O.H.L. Bing, X. Long, K.G. Robinson, and E.G. Lakatta, 1997. Increased cardiomyocyte apoptosis during the transition from hypertrophy to heart failure in the spontaneously hypertensive rat. Am. J. Physiol. 272: H2313-2319.
11. Narula, J., N. Haider, R. Virmani, T.G. DiSalvo, F.D. Kolodgie, R.J. Haijjar, U. Schmidt, M.J. Semigran, G.W. Dec, and B.A. Khaw. 1996. Apoptosis in myocytes in end-stage heart failure. N. Engl. J. Med. 335:1182-1189.
12. Forgac, M. 1989. Structure and function of vacuolar class of ATP-driven proton pumps. Physiol. Rev. 69:765-796.
13. Peng. S.-B., B.P. Crider, X.-S. Xie, and D.K. Stone. 1994. Alternative mRNA splicing generates tissue-specific isoforms of 116-kD polypeptide of vacuolur proton pump. J. Biol. Chem. 269:17262-17266.
14. + -channel of vacuolar proton pumps. J. Biol. Chem. 269: 17379-17381.
15. Long, X., M.O. Boluyt, J.-S. Zheng, L. O'Neill, C. Cirelli, E.G. Lakatta, and M.T. Crow. 1997. p53 and the hypoxia-induced apoptosis of cultured neonatal rat cardiac myocytes. J. Clin. Invest. 99:2635-2643.
16. Bronk, S.F., and G.J. Gores. 1991. Efflux of protons from acidic vesicles contributes to cytosolic acidification of hepatocytes during ATP depletion. Hepatology. 14:626-633.
17. +-ATPase. Proc. Natl. Acad. Sci. USA. 92:5965-5968.
18. Gottlieb, R.A., D.L. Gruol. J.Y. Zhu, and R.L. Engler. 1996. Preconditioning in rabbit cardiomyocytes: role of pH, vacuolar proton ATPase, and apoptosis. J. Clin. Invest. 97:2391-2398.
19. +-ATPases induce apoptosis. Biochem. Biophys. Res. Comm. 212:255-262.
20. Simpson, P., and S. Savion. 1982. Differentiation of rat myocytes in single cell cultures with and without proliferating nonmyocardial cells: cross-striations, ultrastructure, and chronotropic response to isoproterenol. Circ. Res. 50: 101-116.
21. Prigent, P., C. Planpied, J. Aten, and F. Hirsch. 1993. A safe and rapid method for analyzing apoptosis-induced fragmentation of DNA extracted from tissue or cultured cells. J. Immunol. Methods. 160:139-140.
22. Blank, P.S., H.S. Silverman, O.Y. Chung, B.A. Hogue, M.D. Stern, R.G. Hansford, E.G. Lakatta, and M.C. Capogrossi. 1992. Cytosolic pH measurements in single cardiac myocytes using carboxy-seminaphthorhodafluor-1. Am. J. Physiol. 263:H276-H284.
23. Chirgwin, J.M., A.E. Prizybyla, R.J. MacDonald, and W.J. Rutter. 1979. Isolation of biological active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 18:5294-5299.
24. Church, G.M., and W. Gilbert. 1984. Genomic sequencing. Proc: Natl. Acad. Sci. USA. 81:1991-1995.
25. Soussi, T., C. Caron de Fromentel, C. Breugnot, and E. May. 1988. Nucleotide sequence of a cDNA encoding the rat p53 nuclear oncoprotein. Nucleic Acids Res. 16:11384.
26. Xu, H., J. Miller, and B.T. Liang. 1992. High-efficiency gene transfer into cardiac myocytes. Nucleic Acids Res. 20:6425-6426.
27. Meisenholder, G.W., S.J. Martin, D.R. Green, J. Nordberg, B.M. Babior, and R.A. Gottlieb. 1996. Events in apoptosis: acidification is downstream of protease activation and bcl-2 protection. J. Biol. Chem. 271:16260-16262.
28. Gottlieb, R.A., J. Nordberg, E. Skowronski, and B.M. Babior. 1995. Apoptosis induced in Jurkat cells by several agents is preceded by intracellular acidification. Proc. Natl. Acad. Sci. USA. 93:654-658.
29. Li, J., and E. Eastman. 1995. Apoptosis in an interleukin-2-dependent cytotoxic T lymphocyte cell line is associated with intracellular acidification. J. Biol. Chem. 270:3203-3211.
30. Perez-Sala, D., D. Collado-Escobar, and F. Mollinedo. 1995. Intracellular alkalinization supresses lovastatin-induced apoptosis in HL-60 cells through the inactivation of a pH-dependent endonuclease. J. Biol. Chem. 270:6235-6242.
31. Barry, M.A., J.E. Reynolds, and A. Eastman. 1993. Etoposide-induced apoptosis in HL-60 cells is associated with intracellular acidification. Cancer Res. 53:2349-2357.
32. Rebollo, A., J. Gomez, A. Martinez-de Aragon, P. Lastres, A. Silva, and D. Prerez-Sala. 1995. Apoptosis induced by IL-2 withdrawal is associated with an intracellular acidification. Exp. Cell Res. 218:581-585.
33. Rajotte D., P. Haddad, A. Haman, E.J. Cragoe, Jr., and T. Hoang. 1992. Role of protein kinase C and the Na+/H+ antiporter in suppression of apoptosis by granulocyte macrophage colony-stimulating factor. J. Biol. Chem. 267: 9980-9987.
34. Gottlieb, R.A., H.A. Giesing, R.L. Engler, and B.M. Babior. 1995. The acid deoxyribonuclease of neutrophils: a possible participant in apoptosis-associated genome destruction. Blood. 86:2414-2418.
35. Russo, C.A., T.K. Weber, C.M. Volpe, D.L. Stoler, N.J. Petrelli, M. Rodriguez-Bigas, W.C. Burhans, and G.R. Anderson. 1995. An anoxia inducible endonuclease and enhanced DNA breakage as contributors to genomic instability in cancer. Cancer Res. 55:1122-1128.
36. Ko, L.J., and C. Prives. 1996. p53: puzzle and paradigm. Genes Dev. 10: 1054-1072.
37. Baker, S.J., S. Markowitz, E.R. Fearon, J.K.V. Willson, and B. Volgelstein. 1990. Suppression of human colorectal carcinoma cell growth by wildtype p53. Science. 249:912-915.
38. Fearon E.R., and B. Volgelstein. 1990. A genetic model for colorectal tumorigenesis. Cell. 61:759-767.
39. Kastan, M.B. 1993. p53: evolutionally conserved and constantly evolving. J. NIH Res. 5:53-57.
40. Lowe, S.W., E.M. Schmiit, S.W. Smith, B.A. Osborne, and T. Jacks. 1993. p53 is required for radiation-induced apoptosis in mouse thymocytes. Nature. 362:847-849.
41. Fisher, D.E. 1994. Apoptosis in cancer therapy: crossing the threshold. Cell. 78:539-542.