Nitric oxide as a competitive inhibitor of oxygen consumption in the mitochondrial respiratory chain

Acta Physiologica Scandinavica

Volumn 168, Issue 4, 2000, Pages 667-674

  Brown, Guy C ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Mitochondria; Nitric oxide; Oxygen; Respiration

Indexed keywords

ADENOSINE TRIPHOSPHATE; BRADYKININ; CYTOCHROME C OXIDASE; CYTOKINE; ENDOTOXIN; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; OXYGEN;

AORTA; ASTROCYTE; CELL CULTURE; CELL LINE; CONCENTRATION (PARAMETERS); CONFERENCE PAPER; HUMAN; MACROPHAGE; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; NERVE ENDING; OXYGEN AFFINITY; OXYGEN CONSUMPTION; PRIORITY JOURNAL; TISSUE CULTURE; VASCULAR ENDOTHELIUM;

ANIMALS; HUMANS; MITOCHONDRIA; NITRIC OXIDE; OXYGEN CONSUMPTION;

EID: 0034036986     PISSN: 00016772     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-201X.2000.00718.x     Document Type: Conference Paper

References (63)

1. Babcock, G.T. & Wikstrom, M. 1992. Oxygen activation and the conservation of energy in cell respiration. Nature 356, 301-309.
2. Balligand, J.-L., Kelly, R.A., Marsden, P.A., Smith, T.W. & Michel, T. 1993. Control of cardiac-muscle cell function by an endogenous NO signalling system. Proc Natl Acad Sci USA 90, 347-351.
3. Bates, T.E., Loesch, A., Burnstock, G. & Clark, J.B. 1995. Immunological evidence for a mitochondrially located NO synthase in brain and liver. Biochem Biophys Res Commun 213, 869-900.
4. Bates, T.E., Locsch, A., Burnstock, G. & Clark, J.B. 1996. Mitochondrial NO synthase: A ubiquituous regulator of oxidative phosphorylation? Biochem Biophys Res Commun 218, 40-44.
5. Blackmore, R.S., Greenwood, C. & Gibson, Q.H. 1991. Studies of the primary oxygen intermediate in the reactions of fully reduced cytochrome c oxidase. J Biol Chem 266, 19245-19249.
6. Boelens, R., Wever, R., Van Gelder, B.F. & Rademaker, II, 1983. An electron-paramagnetic-res sudy of the photodissociation reactions of oxidised cytochrome c oxidase NO complex. Biochim Biophys Acta 724, 176-183.
7. Borutaite, V. & Brown, G.C. 1996. Rapid reduction of NO by mitochondria, and reversible inhibition of mitochondrail respiration by NO. Biochem J 315, 295-299.
8. Brady, A.J.B., Warren, J.B., Poole-Wilson, P.A., Williams, T.J. & Harding, S.E. 1993. NO attenuates cardiac myocyte contraction. Am J Physiol 265, H176-H182.
9. Brown, G.C. 1995. NO regulates mitochondrial respiration and cell functions by inhibiting cytochrome oxidase. FEBS Lett 369, 136-139.
10. Brown, G.C. 1999. NO and mitochondrial respiration. Biochim Biophys Acta 1411, 351-369.
11. Brown, G.C., Bolanos, J.P., Heales, S.J.R. & Clark, J.B. 1995. NO produced by activated astrocytes rapidly and reversibly inhibits cellular respiration. Neuroscience Lett 193, 1-4.
12. Brown, G.C. & Cooper, C.E. 1994. Nanomolar concentrations of NO reversibly inhibit synaptosomal respiration by competing with oxygen at cytochrome oxidase. FEBS Lett 356, 295-298.
13. Brown, G.C., Foxwell, N. & Moncada, S. 1998. Transcellular regulation of cell respiration by NO generated by activated macrophages. FEBS Lett 439, 321-324.
14. Brudvig, G.W., Stevens, T.H. & Chan, S.I. 1980. Reactions of NO with cytochrome c oxidase. Biochemistry 19, 5275-5285.
15. Cassina, A. & Radi, R. 1996. Different inhibitory actions of NO and peroxynitrite on mitochondrial electron transport. Arch Biophys Biochem 328, 309-316.
16. Cleeter, M.W.J., Cooper, J.M., Darley-Usmar, V.M., Moncada, S. & Schapira, A.H.V. 1994. Reversible inhibition of cytochrome oxidase, the terminal enzyme of the mitochondrial respiratory chain by NO. FEBS Lett 345, 50-54.
17. Clementi, E., Brown, G.C., Feelisch, M. & Moncada, S. 1998. Persistent inhibition of cell respiration by nitric oxide: crucial role of S-nitrosylation of mitochondrial complex I and protective role of glutathione. Proc Natl Acad Sci USA 95, 7631-7636.
18. Clementi, E., Brown, G.C., Foxwell, N. & Moncada, S. 1999. On the mechanisms by which vascular endothelial cells regulate their oxygen consumption. Proc Natl Acad Sci USA 96, 1559-1562.
19. Drapier, J.-C. & Hibbs, J.B. Jr 1988. Differentiation of murine macrophages to express non-specific cytotoxicity for tumour cells results in L-arginine-dependent inhibtion of mitochondrial iron-sulphur in the macrophage effector cells. J Immunol 140, 2829-2838.
20. Ghafourifar, P. & Richter, C. 1997. NO synthase activity in mitochondria. FEBS Lett 418, 291-296.
21. Giuffre, A., Sarti, P., D'Itri, E., Buse, G., Soulimane, T. & Brunori, M. 1996. On the mechanism of inhibition of cytochrome c oxidase by NO. J Biol Chem 271, 33404-33408.
22. Giulivi, C. 1998. Functional implications of NO produced by mitochondria in mitochondrial metabolism. Biochem J 332, 673-679.
23. Giulivi, C., Poderoso, J.J. & Boveris, A. 1998. Production of NO by mitochondria. J Biol Chem 273, 11038-11043.
24. Gnaiger, E., Steinlechner-Maran, R., Mendez, G., Eberl, T. & Margreiter, R. 1995. Control of mitochondrial and cellular respiration by oxygen. J Bioenerg Biomembr 27, 583-596.
25. Gong, G.X., Weiss, H.R., Tse, J. & Scholz, P.M. 1998. Exogenous NO reduces oxygen consumption of isolated ventricular myocytes less than other forms of guanylate cyclase stimulation. Eur J Pharmacol 344, 299-305.
26. Granger, D.L. & Lehninger, A.L. 1982. Sites of inhibition of mitochondrial electron transport in macrophage-injured neoplastic cells. J Cell Biol 95, 527-535.
27. Heales, J.R., Bolanos, J.P., Stewart, V.C., Brookes, P.S., Land, J.M. & Clark, J.B. 1999. NO, mitochondria and neurological disease. Biochim Biophys Acta 1410, 215-228.
28. Henry, Y., Lepoivre, M., Drapier, J.C., Ducrocq, C., Boucher, J.L. & Guissani, A. 1993. EPR characterisation of molecular targets for NO in mammalian cells and oraganelles. FASEB J 7, 1124-1134.
29. Hibbs, J.B. Jr, Taintor, R.R. & Vavrin, Z. 1987. Macrophage cytotoxicity - role of L-arginine deiminase and imino-nitrogen oxidation to nitrite. Science 235, 473-476.
30. Hibbs, J.B. Jr, Taintor, R.R., Vavrin, Z. & Rachlin, K.M. 1988. NO: A cytotoxic acivated-macrophage effector molecule. Biochem Biophys Res Commun 157, 87-94.
31. + channels, adenosine, and NO-mediated mechanisms account for coronary vasodilation during exercise. Circ Res 82, 346-359.
32. Jones, D.P. 1986. Intracellular diffusion gradients of oxygen and ATP. Am J Physiol 250, C663-C675.
33. King, C.E., Melinyshyn, M.J., Mewburn, J.D. et al. 1994. Canine hindlimb blood flow and oxygen uptake after inhibition of EDRF/NO synthesis. J Appl Physiol 76, 1166-1171.
34. Kobzik, L., Stringer, B., Balligand, J.-L., Reid, M.B. & Stamler, J.S. 1995. Endothelial type NO synthase in skeletal muscle fibres-mitochondrial relationships. Biochem Biophys Res Commun 211, 375-381.
35. Koivisto, A., Matthias, A., Bronnikov, G. & Nedergaard, J. 1997. Kinetics of inhibition of respiration by NO. FEBS Lett 417, 75-80.
36. Laffranchi, R., Gogvadze, V., Richter, C. & Spinas, G.A. 1996. NO stimulates insulin secretion by inducing calcium release from mitochondria. Biochem Biophys Res Commun 217, 584-591.
37. Laycock, S.V., Vogel, T., Forfia, P.R. et al. 1998. Role of NO in the control of renal oxygen consumption and the regulation of chemical work in the kidney. Circulation Res 82, 1263-1271.
38. Lizasoain, I., Moro, M.A., Knowles, R.G., Darley-Usmar, V. & Moncada, S. 1996. NO and peroxynitrite exert distinct effects on mitochondrial respiration which are differentially blocked by glutathione and glucose. Biochem J 314, 877-880.
39. Loke, K.E., McConnell, P.I., Tuzman, J.M. et al. 1999. Endogenous endothelial NO synthase-derived NO is a physiological regulator of myocardial oxygen consumption. Circ Res 84, 840-845.
40. Malinski, T. & Czuchajowski, L. 1996. NO measurement by electrochemical methods. In: M. Feelisch & J. Stamler (eds) Methods in Nitric Oxide Research, pp. 319-340. Wiley, Chichester.
41. McNaught, K.St.P. & Brown, G.C. 1998. NO causes glutamate release from brain synaptosomes. J Neurochem 70, 1541-1546.
42. Miles, P.R., Bowman, L. & Huffman, L. 1996. NO alters metabolism in isolated type II cells. Am J Physiol 271, L23-L30.
43. Nishikawa, N., Sato, E.F., Kuroki, T. & Inoue, M. 1997. Role of glutathione and NO in the energy metabolism of rat liver mitochondria. FEBS Lett 415, 341-345.
44. Nishikawa, M., Sato, E.F., Utsumi, K. & Inoue, M. 1996. Oxygen-dependent regulation of energy metabolism in ascites tumour cells by NO. Cancer Res 56, 4535-4540.
45. Poderoso, J.J., Carreras, M.C., Lisdero, C., Riobo, N., Schopfer, F. & Boveris, A. 1996. NO inhibits electron transfer and increases superoxide radical production in rat heart mitochondria and submitochondrial particles. Arch Biophys Biochem 328, 85-92.
46. Poderoso, J.P., Peralta, J.G., Lisdero, C.L. et al. 1998. NO regulates oxygen uptake and hydrogen peroxide release by the isolated beating rat heart. Am J Physiol 274, C112-C119.
47. Richter, C. 1997. Reactive oxygen and nitrogen species regulate mitochondrial calcium homeostasis and respiration. Biosci Reports 17, 53-66.
48. Richter, C., Gogvadze, V., Schlapbach, R., Schweizer, M. & Schlegel, J. 1994. NO kills hepatocytes by mobilizing mitochondrial calcium. Biochem Biophys Res Commun 205, 1143-1150.
49. Sarti, P., Lendaro, E., Ippoliti, R., Bellelli, A., Benedetti, P.A. & Brunori, M. 1999. Modulation of mitochondrial respiration by NO: investigation by single cell fluorescence microscopy. FASEB J 13, 191-197.
50. Schweizer, M. & Richter, C. 1994. NO potently and reversibly de-energizes mitochondria at low oxygen tension. Biochem Biophys Res Commun 204, 169-175.
51. Shen, W., Hintze, T.H. & Wolin, M.S. 1995. NO: An important signalling mechanism between vascular endothelium and parenchymal cells in the regulation of oxygen consumption. Circulation 92, 3505-3512.
52. Shen, W., Xu, X., Ochoa, M., Zhoa, G., Wolin, M.S. & Hintze, T.H. 1994. Role of NO in the regulation of oxygen consumption in conscious dogs. Circ Res 75, 1086-1095.
53. Stubauer, G., Giuffre, A., Brunori, M. & Sarti, P. 1998. Cytochrome c oxidase does not catalyze the anaerobic reduction of NO. Biochem Biophys Res Commun 245, 459-465.
54. Stuehr, D.J. & Nathan, C.F. 1989. NO: A macrophage product responsible for cytostasis and respiratory inhibition in tumour target cells. J Exp Med 169, 1543-1555.
55. Takehara, Y., Kanno, T., Yoshioka, T., Inoue, M. & Utsumi, K. 1995. Oxygen-dependent regulation of mitochondrial energy metabolism by NO. Arch Biophys Biochem 323, 27-32.
56. Tatoyan, A. & Giulivi, C. 1998. Purification and characterisation of a NO synthase from rat liver mitochondria. J Biol Chem 273, 11044-11048.
57. Torres, J., Cooper, C.E. & Wilson, M.T. 1998. A common mechanism for the interaction of NO with the oxidised binuclear centre and oxygen intermediates of cytochrome c oxidase. J Biol Chem 273, 8756-8766.
58. Torres, J., Darley-Usmar, V. & Wilson, M.T. 1995. Inhibition of cytochrome c oxidase in turnover by NO: Mechanisms and implications for control of respiration. Biochem J 312, 169-173.
59. Welter, R., Yu, L. & Yu, C.-A. 1996. The effects of NO on electron transport complexes. Arch Biophys Biochem 331, 9-14.
60. Xie, Y.-W., Shen, W., Zhao, G., Xu, X., Wolin, M.S. & Hintze, T.H. 1996. Role of endothelial derived NO in the modulation of canine myocardial mitochondrial respiration in vitro - implications for the development of heart failure. Circ Res 79, 381-387.
61. Young, M.E. & Leighton, B. 1998a. Evidence for altered sensitivity of the NO/cGMP signalling cascade insulin-resistant skeletal muscle. Biochem J 329, 73-79.
62. Young, M.E. & Leighton, B. 1998b. Fueloxidation in skeletal muscle is increased by NO/cGMP - evidence for involvement of cGMP-dependent protein kinase. FEBS Lett 424, 79-83.
63. Young, M.E., Radda, G.K. & Leighton, B. 1997. NO stimulates glucose transport and metabolism in rat skeletal muscle in vivo. Biochem J 322, 223-228.