Importance of the bioenergetic reserve capacity in response to cardiomyocyte stress induced by 4-hydroxynonenal

Biochemical Journal

Volumn 424, Issue 1, 2009, Pages 99-107

  Hill, Bradford G ^a   Dranka, Brian P ^a   Zou, Luyon ^b   Chatham, John C ^b   Darley Usmar, Victor M ^a  

^a University of Alabama at Birmingham   (United States)

^b University of Alabama at Birmingham   (United States)

Author keywords

Cardiomyocyte; Extracellular flux; Glycolysis; Heart; Lipid peroxidation; Mitochondrion; Oxidative stress

Indexed keywords

CARDIOMYOCYTE; EXTRACELLULAR FLUX; GLYCOLYSIS; HEART; LIPID PEROXIDATION;

CELL DEATH; DETOXIFICATION; MITOCHONDRIA; OXIDATION; OXIDATIVE STRESS; OXYGEN; PATHOLOGY; REPAIR;

ENZYME ACTIVITY;

4 HYDROXYNONENAL;

ANIMAL CELL; ARTICLE; BIOENERGY; CELL DAMAGE; CELL DEATH; CELL ENERGY; CELL METABOLISM; CELLULAR STRESS RESPONSE; CONCENTRATION PROCESS; CONTROLLED STUDY; EXHAUSTION; HEART MUSCLE CELL; HEART VENTRICLE; MITOCHONDRIAL RESPIRATION; NEWBORN; NONHUMAN; OXYGEN CONSUMPTION; PRIORITY JOURNAL; PROTEIN MODIFICATION; RAT;

ALDEHYDES; ANIMALS; ANIMALS, NEWBORN; CELL SURVIVAL; CELLS, CULTURED; CYSTEINE PROTEINASE INHIBITORS; GLYCOLYSIS; LIPID PEROXIDATION; MITOCHONDRIA; MYOCYTES, CARDIAC; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY;

RATTUS;

EID: 70350694223     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20090934     Document Type: Article

References (57)

1. 31P-NMR measurement of mitochondrial uncoupling in isolated rat hearts. J. Biol. Chem. 265, 1545-1550
2. Gong, G., Liu, J., Liang, P., Guo, T., Hu, Q., Ochiai, K., Hou, M., Ye, Y., Wu, X., Mansoor, A. et al. (2003) Oxidative capacity in failing hearts. Am. J. Physiol. Heart Circ. Physiol. 285, H541-H548
3. Lucas, D. T. and Szweda, L. I. (1999) Declines in mitochondrial respiration during cardiac reperfusion: age-dependent inactivation of alpha-ketoglutarate dehydrogenase. Proc. Natl. Acad. Sci. U.S.A. 96, 6689-6693
4. Almsherqi, Z. A., McLachlan, C. S., Slocinska, M. B., Sluse, F. E., Navet, R., Kocherginsky, N., Kostetski, I., Shi, D. Y., Liu, S. L., Mossop, P. and Deng, Y. (2006) Reduced cardiac output is associated with decreased mitochondrial efficiency in the non-ischemic ventricular wall of the acute myocardial-infarcted dog. Cell Res. 16, 297-305
5. Petrosillo, G., Ruggiero, F. M., Di Venosa, N. and Paradies, G. (2003) Decreased complex III activity in mitochondria isolated from rat heart subjected to ischemia and reperfusion: role of reactive oxygen species and cardiolipin. FASEB J. 17, 714-716
6. Paradies, G., Petrosillo, G., Pistolese, M., Di Venosa, N., Federici, A. and Ruggiero, F. M. (2004) Decrease in mitochondrial complex I activity in ischemic/reperfused rat heart: involvement of reactive oxygen species and cardiolipin. Circ. Res. 94, 53-59
7. Chen, Z., Siu, B., Ho, Y. S., Vincent, R., Chua, C. C., Hamdy, R. C. and Chua, B. H. (1998) Overexpression of MnSOD protects against myocardial ischemia/reperfusion injury in transgenic mice. J. Mol. Cell. Cardiol. 30, 2281-2289
8. Li, G., Chen, Y., Saari, J. T. and Kang, Y. J. (1997) Catalase-overexpressing transgenic mouse heart is resistant to ischemia-reperfusion injury. Am. J. Physiol. 273, H1090-H1095
9. Chen, E. P., Bittner, H. B., Davis, R. D., Folz, R. J. and Van Trigt, P. (1996) Extracellular superoxide dismutase transgene overexpression preserves postischemic myocardial function in isolated murine hearts. Circulation 94, II412-II417
10. Yoshida, T., Watanabe, M., Engelman, D. T., Engelman, R. M., Schley, J. A., Maulik, N., Ho, Y. S., Oberley, T. D. and Das, D. K. (1996) Transgenic mice overexpressing glutathione peroxidase are resistant to myocardial ischemia reperfusion injury. J. Mol. Cell. Cardiol. 28, 1759-1767
11. +/- mouse hearts. Circulation 105, 981-986
12. Yoshida, T., Maulik, N., Engelman, R. M., Ho, Y. S., Magnenat, J. L., Rousou, J. A., Flack, III, J. E., Deaton, D. and Das, D. K. (1997) Glutathione peroxidase knockout mice are susceptible to myocardial ischemia reperfusion injury. Circulation 96 (Suppl. 9), II-216-II-220
13. Yoshida, T., Maulik, N., Engelman, R. M., Ho, Y. S. and Das, D. K. (2000) Targeted disruption of the mouse Sod I gene makes the hearts vulnerable to ischemic reperfusion injury. Circ. Res. 86, 264-269
14. Strauer, B. E. (1987) Cardiac energetics in clinical heart disease. Basic Res. Cardiol. 82 (Suppl. 2), 389-402
15. Gunning, J. F. and Coleman, 3rd, H. N. (1973) Myocardial oxygen consumption during experimental hypertrophy and congestive heart failure. J. Mol. Cell Cardiol. 5, 25-38
16. Gunning, J. F., Cooper, G. T., Harrison, C. E. and Coleman, 3rd, H. N. (1973) Myocardial oxygen consumption in experimental hypertrophy and congestive heart failure due to pressure overload. Am. J. Cardiol. 32, 427-436
17. Smith, D. R., Stone, D. and Darley-Usmar, V. M. (1996) Stimulation of mitochondrial oxygen consumption in isolated cardiomyocytes after hypoxia-reoxygenation. Free Radical Res. 24, 159-166
18. 31P NMR. J. Biol. Chem. 263, 10600-10607
19. Hill, B. G., Awe, S. O., Vladykovskaya, E., Ahmed, Y., Liu, S. Q., Bhatnagar, A. and Srivastava, S. (2009) Myocardial ischaemia inhibits mitochondrial metabolism of 4-hydroxy-trans-2-nonenal. Biochem. J. 417, 513-524
20. Eaton, P., Li, J. M., Hearse, D. J. and Shattock, M. J. (1999) Formation of 4-hydroxy-2-nonenal-modified proteins in ischemic rat heart. Am. J. Physiol. 276, H935-H943
21. Nakamura, K., Kusano, K., Nakamura, Y., Kakishita, M., Ohta, K., Nagase, S., Yamamoto, M., Miyaji, K., Saito, H., Morita, H. et al. (2002) Carvedilol decreases elevated oxidative stress in human failing myocardium. Circulation 105, 2867-2871
22. Srivastava, S., Chandrasekar, B., Bhatnagar, A. and Prabhu, S. D. (2002) Lipid peroxidation-derived aldehydes and oxidative stress in the failing heart: role of aldose reductase. Am. J. Physiol. Heart Circ. Physiol. 283, H2612-H2619
23. Esterbauer, H., Schaur, R. J. and Zollner, H. (1991) Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radical Biol. Med. 11, 81-128
24. Echtay, K. S., Esteves, T. C., Pakay, J. L., Jekabsons, M. B., Lambert, A. J., Portero-Otin, M., Pamplona, R., Vidal-Puig, A. J., Wang, S., Roebuck, S. J. and Brand, M. D. (2003) A signalling role for 4-hydroxy-2-nonenal in regulation of mitochondrial uncoupling. EMBO J. 22, 4103-4110
25. Humphries, K. M., Yoo, Y. and Szweda, L. I. (1998) Inhibition of NADH-linked mitochondrial respiration by 4-hydroxy-2-nonenal. Biochemistry 37, 552-557
26. Humphries, K. M. and Szweda, L. I. (1998) Selective inactivation of alpha-ketoglutarate dehydrogenase and pyruvate dehydrogenase: reaction of lipoic acid with 4-hydroxy-2-nonenal. Biochemistry 37, 15835-15841
27. Lashin, O. M., Szweda, P. A., Szweda, L. I. and Romani, A. M. (2006) Decreased complex II respiration and HNE-modified SDH subunit in diabetic heart. Free Radical Biol. Med. 40, 886-896
28. +-isocitrate dehydrogenase is inactivated through 4-hydroxynonenal adduct formation: an event that precedes hypertrophy development. J. Biol. Chem. 278, 45154-45159
29. Choksi, K. B., Boylston, W. H., Rabek, J. P., Widger, W. R. and Papaconstantinou, J. (2004) Oxidatively damaged proteins of heart mitochondrial electron transport complexes. Biochim. Biophys. Acta. 1688, 95-101
30. Chen, J., Henderson, G. I. and Freeman, G. L. (2001) Role of 4-hydroxynonenal in modification of cytochrome c oxidase in ischemia/ reperfused rat heart. J. Mol. Cell. Cardiol. 33, 1919-1927
31. Ji, C., Amarnath, V., Pietenpol, J. A. and Marnett, L. J. (2001) 4-Hydroxynonenal induces apoptosis via caspase-3 activation and cytochrome c release. Chem. Res. Toxicol. 14, 1090-1096
32. Vieira, H. L., Belzacq, A. S., Haouzi, D., Bernassola, F., Cohen, I., Jacotot, E., Ferri, K. F., El Hamel, C., Bartle, L. M., Melino, G. et al. (2001) The adenine nucleotide translocator: a target of nitric oxide, peroxynitrite, and 4-hydroxynonenal. Oncogene 20, 4305-4316
33. Chen, C. H., Budas, G. R., Churchill, E. N., Disatnik, M. H., Hurley, T. D. and Mochly-Rosen, D. (2008) Activation of aldehyde dehydrogenase-2 reduces ischemic damage to the heart. Science 321, 1493-1495
34. Churchill, E. N., Disatnik, M. H. and Mochly-Rosen, D. (2009) Time-dependent and ethanol-induced cardiac protection from ischemia mediated by mitochondrial translocation of iPKC and activation of aldehyde dehydrogenase 2. J. Mol. Cell. Cardiol. 46, 278-284
35. Champattanachai, V., Marchase, R. B. and Chatham, J. C. (2008) Glucosamine protects neonatal cardiomyocytes from ischemia-reperfusion injury via increased protein O-GlcNAc and increased mitochondrial Bcl-2. Am. J. Physiol. Cell Physiol. 294, C1509-C1520
36. Ferrick, D. A., Neilson, A. and Beeson, C. (2008) Advances in measuring cellular bioenergetics using extracellular flux. Drug Discov. Today 13, 268-274
37. Hill, B. G., Haberzettl, P., Ahmed, Y., Srivastava, S. and Bhatnagar, A. (2008) Unsaturated lipid peroxidation-derived aldehydes activate autophagy in vascular smooth-muscle cells. Biochem. J. 410, 525-534
38. 2 adduct formation with Keap1 over time: effects on potency for intracellular antioxidant defence induction. Biochem. J. 411, 297-306
39. Mosmann, T. (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65, 55-63
40. Nakamura, K., Kusano, K. F., Matsubara, H., Nakamura, Y., Miura, A., Nishii, N., Banba, K., Nagase, S., Miyaji, K., Morita, H. et al. (2005) Relationship between oxidative stress and systolic dysfunction in patients with hypertrophic cardiomyopathy. J. Card. Failure 11, 117-123
41. Mak, S., Lehotay, D. C., Yazdanpanah, M., Azevedo, E. R., Liu, P. P. and Newton, G. E. (2000) Unsaturated aldehydes including 4-OH-nonenal are elevated in patients with congestive heart failure. J. Card. Failure 6, 108-114
42. Srivastava, S., Chandra, A., Wang, L. F., Seifert, Jr, W. E., DaGue, B. B., Ansari, N. H., Srivastava, S. K. and Bhatnagar, A. (1998) Metabolism of the lipid peroxidation product, 4-hydroxy-trans-2-nonenal, in isolated perfused rat heart. J. Biol. Chem. 273, 10893-10900
43. Wu, M., Neilson, A., Swift, A. L., Moran, R., Tamagnine, J., Parslow, D., Armistead, S., Lemire, K., Orrell, J., Teich, J. et al. (2007) Multiparameter metabolic analysis reveals a close link between attenuated mitochondrial bioenergetic function and enhanced glycolysis dependency in human tumor cells. Am. J. Physiol. Cell Physiol. 292, C125-C136
44. David, H., Meyer, R., Marx, I., Guski, H. and Wenzelides, K. (1979) Morphometric characterization of left ventricular myocardial cells of male rats during postnatal development. J. Mol. Cell. Cardiol. 11, 631-638
45. Schaper, J., Meiser, E. and Stammler, G. (1985) Ultrastructural morphometric analysis of myocardium from dogs, rats, hamsters, mice, and from human hearts. Circ. Res. 56, 377-391
46. Giordano, F. J. (2005) Oxygen, oxidative stress, hypoxia, and heart failure. J. Clin. Invest. 115, 500-508
47. Katz, A. M. (1989) Changing strategies in the management of heart failure. J. Am. Coll. Cardiol. 13, 513-523
48. Boudina, S., Sena, S., O'Neill, B. T., Tathireddy, P., Young, M. E. and Abel, E. D. (2005) Reduced mitochondrial oxidative capacity and increased mitochondrial uncoupling impair myocardial energetics in obesity. Circulation 112, 2686-2695
49. Veronneau, M., Comte, B. and Des, R. C. (2002) Quantitative gas chromatographic-mass spectrometric assay of 4-hydroxynonenal bound to thiol proteins in ischemic/reperfused rat hearts. Free Radical Biol. Med. 33, 1380-1388
50. Fiorillo, C., Nediani, C., Ponziani, V., Giannini, L., Celli, A., Nassi, N., Formigli, L., Perna, A. M. and Nassi, P. (2005) Cardiac volume overload rapidly induces oxidative stress-mediated myocyte apoptosis and hypertrophy. Biochim. Biophys. Acta 1741, 173-182
51. Srivastava, S., Chandrasekar, B., Gu, Y., Luo, J., Hamid, T., Hill, B. G. and Prabhu, S. D. (2007) Downregulation of CuZn-superoxide dismutase contributes to β-adrenergic receptor-mediated oxidative stress in the heart. Cardiovasc. Res. 74, 445-455
52. Luo, J., Hill, B. G., Gu, Y., Cai, J., Srivastava, S., Bhatnagar, A. and Prabhu, S. D. (2007) Mechanisms of acrolein-induced myocardial dysfunction: implications for environmental and endogenous aldehyde exposure. Am. J. Physiol. Heart Circ. Physiol. 293, H3673-H3684
53. Irwin, W. A., Gaspers, L. D. and Thomas, J. A. (2002) Inhibition of the mitochondrial permeability transition by aldehydes. Biochem. Biophys. Res. Commun. 291, 215-219
54. Parker, N., Vidal-Puig, A. and Brand, M. D. (2008) Stimulation of mitochondrial proton conductance by hydroxynonenal requires a high membrane potential. Biosci. Rep. 28, 83-88
55. Nicholls, D. G., Johnson-Cadwell, L., Vesce, S., Jekabsons, M. and Yadava, N. (2007) Bioenergetics of mitochondria in cultured neurons and their role in glutamate excitotoxicity. J. Neurosci. Res. 85, 3206-3212
56. Yadava, N. and Nicholls, D. G. (2007) Spare respiratory capacity rather than oxidative stress regulates glutamate excitotoxicity after partial respiratory inhibition of mitochondrial complex I with rotenone. J. Neurosci. 27, 7310-7317
57. Choi, S. W., Gerencser, A. A. and Nicholls, D. G. (2009) Bioenergetic analysis of isolated cerebrocortical nerve terminals on a microgram scale: spare respiratory capacity and stochastic mitochondrial failure. J. Neurochem. 109, 1179-1191