Preconditioning in rabbit cardiomyocytes: Role of pH, vacuolar proton ATPase, and apoptosis

Journal of Clinical Investigation

Volumn 97, Issue 10, 1996, Pages 2391-2398

  Gottlieb, Roberta A ^a,b,c   Gruol, Donna L ^c   Zhu, Jessica Y ^a,b   Engler, Robert L ^a,b,d  

^a VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Bafilomycin; Ischemia; Reperfusion

Indexed keywords

BAFILOMYCIN; CYANIDE; DEOXYGLUCOSE; DNA; INTERLEUKIN 1BETA CONVERTING ENZYME; ION CHANNEL; PROTEIN KINASE C; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE;

ACIDIFICATION; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL PH; CELL VACUOLE; CONDITIONING; CONTROLLED STUDY; DNA NICK TRANSLATION; ENZYME ACTIVATION; ETIOLOGY; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; NONHUMAN; PRIORITY JOURNAL; PROTON SODIUM EXCHANGE; RABBIT; REPERFUSION INJURY;

ANIMALS; APOPTOSIS; FEMALE; HYDROGEN-ION CONCENTRATION; MALE; MYOCARDIAL ISCHEMIA; MYOCARDIUM; PROTEIN KINASE C; PROTON-TRANSLOCATING ATPASES; RABBITS; SODIUM-HYDROGEN ANTIPORTER; VACUOLES;

EID: 0029885316     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI118683     Document Type: Article

References (70)

1. Murry, C.E., V.J. Richard, K.A. Reimer, and R.B. Jennings. 1990. Ischemic preconditioning slows energy metabolism and delays ultrastructural damage during a sustained ischemic episode. Circ. Res. 66:913-931.
2. Ikonomidis, J.S., L.C. Tumiati, R.D. Weisel, D.A. G. Mickle, and R.-K. Li. 1994. Preconditioning human ventricular cardiomyocytes with brief periods of simulated ischaemia. Cardiovasc. Res. 28:1285-1291.
3. Yellon, D., A. Alkhulaifi, and W. Pugsley. 1993. Preconditioning the human myocardium. Lancet. 342:276-277.
4. Downey, J.M., G.S. Liu, and J.D. Thornton. 1993. Adenosine and the anti-infarct effects of preconditioning. Cardiovasc. Res. 27:3-8.
5. Liu, G.S., S.C. Richards, R.A. Olsson, K. Mullane, R.S. Walsh, and J.M. Downey. 1994. Evidence that the adenosine A3 receptor may mediate the protection afforded by preconditioning in the isolated rabbit heart. Cardiovasc. Res. 28:1057-1061.
6. Yao, Z., and G.J. Gross. 1993. Acetylcholine mimics ischemic preconditioning via a glibenclamide-sensitive mechanism in dogs. Am. J. Physiol. 264: H2221-H2225.
7. + channel in mediating the effects of acetylcholine to mimic preconditioning in dogs. Circ. Res. 73:1193-1201.
8. Kitakaze, M., M. Hori, and T. Kamada. 1993. Role of adenosine and its interaction with alpha adrenoreceptor activity in ischaemic and reperfusion injury of the myocardium. Cardiovasc. Res. 27:18-27.
9. Ytrehus, K., Y. Liu, and J.M. Downey. 1994. Preconditioning protects ischemic rabbit heart by protein kinase C activation. Am. J. Physiol. 35(34): H1145-H1152.
10. Asimakis, G.K., K. Inners-McBride, G. Medellin, and V.R. Conti. 1992. Ischemic preconditioning attenuates acidosis and postischemic dysfunction in isolated rat heart. Am. J. Physiol. 263:H887-H894.
11. Wolfe, C.L., R.E. Sievers, F.L.J. Visseren, and T.J. Donnelly. 1993. Loss of myocardial protection after preconditioning correlates with the time course of glycogen recovery within the preconditioned segment. Circulation. 87(3): 881-892.
12. Steenbergen, C., M.E. Perlman, R.E. London, and E. Murphy. 1993. Mechanism of preconditioning. Ionic alterations. Circ. Res. 72:112-125.
13. deAlbuquerque, C.P., G. Gerstenblith, and R.G. Weiss. 1994. Importance of metabolic inhibition and cellular pH in mediating preconditioning contractile and metabolic effects in rat hearts. Circ. Res. 74:139-150.
14. Vuorinen, K., K. Ylitalo, B.M, K. Peuhkurinen, P. Raatikainen, A. Ala-Rami, and I.E. Hassinen. 1995. Mechanisms of ischemic preconditioning in rat myocardium. Roles of adenosine, cellular energy state, and mitochondrial flfo-ATPase. Circulation. 91:2810-2818.
15. Gottlieb, R.A., H.A. Giesing, J.Y. Zhu, R.L. Engler, and B.M. Babior. 1995. Cell acidification in apoptosis: granulocyte colony-stimulating factor delays programed cell death in neutrophils by up-regulating the vacuolar H+-ATPase. Proc. Natl. Acad. Sci. USA. 92:5965-5968.
16. Rajotte, D., P. Haddad, A. Haman, E.J. Cragoe, J., 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.
17. Caceres-Cortes, J., D. Rajotte, J. Dumouchel, P. Haddad, and T. Hoang. 1994. Product of the Steel locus suppresses apoptosis in hemopoietic cells. Comparison with pathways activated by granulocyte macrophage colony-stimulating factor. J. Biol. Chem. 269:12084-12091.
18. Nordstrom, T., S. Grinstein, G.F. Brisseau, M.F. Manolson, and O.D. Rotstein. 1994. Protein kinase C activation accelerates proton extrusion by vacuolar-type H(+)-ATPases in murine peritoneal macrophages. FEBS Lett. 350: 82-86.
19. Nanda, A., A. Gukovskaya, J. Tseng, and S. Grinstein. 1992. Activation of vacuolar-type proton pumps by protein kinase C. Role in neutrophil pH regulation. J. Biol. Chem. 267:22740-22746.
20. Gottlieb, 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.
21. 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.
22. Meng, H., and G.N. Pierce. 1990. Protective effects of 5-(N,N-dimethyl) amiloride on ischemia-reperfusion injury in hearts. Am. J. Physiol. 27:H1615-H1619.
23. Murphy, E., M. Perlman, R.E. London, and C. Steenbergen. 1991. Amiloride delays the ischemia induced rise in cytosolic free calcium. Circ. Res. 68:1250-1258.
24. Haigney, M.C.P., H. Miyata, E.G. Lakatta, M.D. Stern, and H.S. Silverman. 1992. Dependence of hypoxic cellular calcium loading on sodium-calcium exchange. Circ. Res. 71:547-557.
25. Bond, J.M., E. Chacon, B. Herman, and J.J. Lemasters. 1993. Intracellular pH and Ca2+ homeostasis in the pH paradox of reperfusion injury to neonatal rat cardiac myocytes. Am. J. Physiol. 265:C129-C137.
26. Cornelis, V.H., V.J. A. Schouten, A. Muller, V.D. Meulen, E.T, and G. Elzinga. 1995. Exposure of energy-depleted rat trabeculae to low pH improves contractile recovery: role of calcium. Heart Circ. Physiol. 37:H1510-H1520.
27. Silverman, H.S., and M.D. Stern. 1994. Ionic basis of ischaemic cardiac injury: insights from cellular studies. Cardiovasc. Res. 28:581-597.
28. Atsma, D.E., E.M. LarsBatiaanse, A. Jerzewski, L. VanderValk, J.M, and A. VanderLaarse. 1995. Role of calcium-activated neutral protease (calpain) in cell death in cultured neonatal rat cardiomyocytes during metabolic inhibition. Circ. Res. 76:1071-1078.
29. Satoh, H., H. Hayashi, H. Katoh, H. Terada, and A. Kobayashi. 1995. Na+/H + and Na+/Ca2+ exchange in regulation of [Na+]i and [Ca2+]i during metabolic inhibition. Am. J. Physiol. 268:H1239-H1248.
30. Yasutake, M., C. Ibuki, D J. Hearse, and M. Avkiran. 1994. Na+/H+ exchange and reperfusion arrhythmias: protection by intracoronary infusion of a novel inhibitor. Am. J. Physiol. 36(4):H2430-H2440.
31. Meng, H.P., T.G. Maddaford, and G.N. Pierce. 1993. Effect of amiloride and selected analogues on postischemic recovery of cardiac contractile function. Am. J. Physiol. 264:H1831-H1835.
32. Bugge, E., and K. Ytrehus. 1995. Inhibition of sodium-hydrogen exchange reduces infarct size in the isolated rat heart: a protective additive to ischaemic preconditioning. Cardiovasc. Res. 29:269-274.
33. Scholz, W., U. Albus, L. Counillon, H. Gogelein, H.J. Lang, W. Linz, A. Weichert, and B.A. Scholkens. 1995. Protective effects of HOE642, a selective sodium-hydrogen exchange subtype 1 inhibitor, on cardiac ischaemia and reperfusion. Cardiovasc. Res. 29:260-268.
34. Navon, G., J.G. Werrmann, R. Maron, and S.M. Cohen. 1994. 31 P NMR and triple quantum filtered 23 Na NMR studies of the effects of inhibition of Na+/H+ exchange on intracellular sodium and pH in working and ischemic hearts. Magn. Reson. Med. 32:556-564.
35. Pike, M.M., C.S. Luo, M.D. Clark, K.K.A, M. Kitakaze, M.C. Madden, E.J. Cragoe, Jr., and G.M. Pohost. 1993. NMR measurements of Na+ and cellular energy in ischemic rats heart:role of Na(+)-H+exchange. Am. J. Physiol. 265:H2017-H2026.
36. Hendrikx, M., K. Mubagwa, F. Verdonck, K. Overloop, P. VanHecke, F. Vanstapel, A. VanLommel, E. Verbeken, J. Lauweryns, and W. Flameng. 1994. New Na(+)-H+-exchange inhibitor HOE 694 improves postischemic function and high-energy phosphate resynthesis and reduces Ca2+ overload in isolated perfused rabbit heart. Circulation. 89:2787-2798.
37. Imai, S., A.Y. Shi, T. Ishibashi, and M. Nakazawa. 1991. Na+/H+ exchange is not operative under low-flow ischemic conditions. J. Mol. Cell. Cardiol. 23:505-517.
38. Pierce, G.N., W.C. Cole, K. Liu, H. Massaaeli, T.G. Maddaford, Y.J. Chen, C.D. McPherson, S. Jain, and D. Sontag. 1993. Modulation of cardiac performance by amiloride and several selected derivatives of amiloride. J. Pharm. Exp. Ther. 265:1280-1291.
39. Drose, S., K.U. Bindseil, E.J. Bowman, S. Siebers, A. Zeeck, and K. Altendorf. 1993. Inhibitory effect of modified bafilomycins and concanamycins on P- and V-type adenosinetriphosphatases. Biochemistry 32:3902-9206.
40. 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.
41. Crider, B., X.S. Xie, and D.K. Stone. 1994. Bafilomycin inhibits proton flow through the H+ channel of vacuolar proton pumps. J. Biol. Chem. 269: 17379-17381.
42. Fearnhead, H.O., D. Dinsdale, and G.M. Cohen. 1995. An interleukin-1 beta-converting enzyme-like protease is a common mediator of apoptosis in thymocytes. FEBS Lett. 375:283-288.
43. 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.
44. Barry, M.A., J.E. Reynolds, and A. Eastman. 1993. Etoposide-induced apoptosis in human HL-60 cells is associated with intracellular acidification. Cancer Res 53:2349-2357.
45. 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.
46. Perez-Sala, D., D. Collado-Escobar, and F. Mollinedo. 1995. Intracellular alkalinization suppresses lovastatin-induced apoptosis in HL-60 cells through the inactivation of a pH-dependent endonuclease. J. Biol. Chem. 270: 6235-6242.
47. Rebollo, A., J. Gomez, A. Martinez-de Aragon, P. Lastres, A. Silva, and D. Perez-Sala. 1995. Apoptosis induced by IL-2 withdrawal is associated with an intracellular acidification. Exp. Cell Res. 218:581-585.
48. Nishihara, T., S. Akifusa, T. Koseki, S. Kato, M. Muro, and N. Hanada. 1995. Specific inhibitors of vacuolar type H(+)-ATPases induce apoptotic cell death. Biochem. Biophys. Res. Commun. 212:255-262.
49. Flesser, A., V. Marshansky, M. Duplain, J. Noel. A. Hoang, A. Tejedor, and P. Vinay. 1995. Cross-talk between the Na(+)-K(+)-ATPase and the H(+)-ATPase in proximal tubules in suspension. Renal Physiol. Biochem. 18: 140-152.
50. Bidani, A., S.E. Brown, and T.A. Heming. 1994. pHi regulation in alveolar macrophages: relative roles of Na(+)-H+ antiport and H(+)-ATPase. Am. J. Physiol. 266:L681-L688.
51. Lepier, A., M. Azuma, W.R. Harvey, and H. Wieczorek. 1994. K+/H+ antiport in the tobacco hornworm midgut: the K(+)-transporting component of the K+ pump. J. Exp. Biol. 196:361-373.
52. Hayashi, H., K. Arai, O. Sato, A. Shimaya, Y. Sai, and S. Ohkuma. 1992. Three types of membranous ATPase on rat liver lysosomes. Chem. Pharm. Bull. 40:2783-2786.
53. Mattsson, J.P., K. Vaananen, B. Wallmark, and P. Lorentzon. 1991. Omeparazole and bafilomycin, two proton pump inhibitors: differentiation of their effects on gastric, kidney and bone H(+) translocating ATPases. Biochim. Biophys. Acta. 1065:261-268.
54. Bidani, A., and S.E. Brown. 1990. ATP-dependent pHi recovery in lung macrophages: evidence for plasma membrane H(+)-ATPase. Am. J. Physiol. 259:C586-C598.
55. Swallow, C.J., S. Grinstein, R.A. Sudsbury, and O.D. Rotstein. 1993. Relative roles of Na+/H+ exchange and vacuolar-type H+ ATPases in regulating cytoplasmic pH and function in murine peritoneal macrophages. J. Cell Physiol. 157:453-460.
56. Martinez-Zaguilan, R., R.M. Lynch, G.M. Martinez, and R.J. Gillies. 1993. Vacuolar-type H(+)-ATPases are functionally expressed in plasma membranes of human tumor cells. Am. J. Physiol. 265:C1015-C1029.
57. Novotny, W.F., O. Chassande, M. Baker, M. Lazdunski, and P. Barbry. 1994. Diamine oxidase is the amiloride-binding protein and is inhibited by amiloride analogues. J. Biol. Chem. 269:9921-9925.
58. Presek, P., and C. Reuter. 1987. Amiloride inhibits the protein tyrosine kinases associated with the cellular and the transforming SRC-gene products. Biochem. Pharmacol. 36:2821-2826.
59. Vanhaesebroeck, B., E.J. Cragoe, Jr., J. Pouyssegur, R. Beyaert, F. Van-Roy, and W. Fiers. 1990. Cytotoxic activity of tumor necrosis factor is inhibited by amiloride derivatives without involvement of the Na+/H+ antiporter. FEBS Lett. 261:319-322.
60. Hori, M., M. Kitakaze, H. Sato, S. Takashima, K. Iwakura, M. Inoue, A. Kitabatake, and T. Kamada. 1991. Staged reperfusion attenuates myocardial stunning in dogs. Role of transient acidosis during early reperfusion. Circulation. 84(5):2135-2145.
61. Shanley, P.F., and G.C. Johnson. 1991. Calcium and acidosis in renal hypoxia. Lab. Invest. 65:298-305.
62. Kitakaze, M., M.L. Weisfeldt, and E. Marban. 1988. Acidosis during early reperfusion prevents myocardial stunning in perfused ferret hearts. J. Clin. Invest. 82:920-927.
63. Halestrap, A.P. 1991. Calcium-dependent opening of a non-specific pore in the mitochondrial inner membrane is inhibited at pH values below 7. Biochem. J. 278:715-719.
64. Nicholli, A., V. Petronilli, and P. Bernardi. 1993. Modulation of the mitochondrial cyclosporin A-sensitive permeability transition pore by matrix pH. Evidence that the pore open-closed probability is regulated by reversible histidine protonation. Biochemistry. 32:4461-4465.
65. Shen, H., J. Chan, I.S. Kass, and P.J. Bergold. 1995. Transient acidosis induces delayed neurotoxicity on cultured hippocampal slices. Neurosci. Lett. 185:115-118.
66. Gottlieb, R.A., H.A. Giesing, R.L. Engler, and B. Babior. 2414. The acid deoxyribonuclease of neutrophils: a possible participation in apoptosis-associated genome destruction. Blood. 86:2414-2418.
67. Barry, M. A., and A. Eastman. 1993. Identification of deoxyribonuclease 11 as an endonuclease involved in apoptosis. Arch. Biochem. Biophys. 300:440-448.
68. Kanfer, J.N., O.M. Young, D. Shapiro, and R.O. Brady. 1966. The metabolism of sphingomyelin I purification and properties of a sphingomyelin-cleaving enzyme from rat liver tissue. J. Biol. Chem. 241:1081-1084.
69. Folk, J.E., and P.W. Cole. 1966. Transglutaminase: mechanistic features of the active site as determined by kinetic and inhibitor studies. Biochim. Biophys. Acta. 122:244-264.
70. Lamb, J.A., P.G. Allen, B.Y. Tuan, and P.A. Janmey. 1993. Modulation of gelsolin function: activation at low pH overrides Ca2+ requirement. J. Biol. Chem. 268:8999-9004.