Functional evidence for nitric oxide production by skeletal-muscle mitochondria from lipopolysaccharide-treated mice

Mitochondrion

Volumn 12, Issue 1, 2012, Pages 126-131

  Aguirre, Enara ^a   López Bernardo, Elia ^b   Cadenas, Susana ^a,b,c  

^a CENTRO NACIONAL DE INVESTIGACIONES CARDIOVASCULARES CNIC   (Spain)

^b Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas   (Spain)

^c UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

Mitochondrial NOS (mtNOS); Nitric oxide (NO); Oxygen consumption; Oxygen kinetics; Respiration; Skeletal muscle

Indexed keywords

ARGININE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; ESCHERICHIA COLI LIPOPOLYSACCHARIDE; INDUCIBLE NITRIC OXIDE SYNTHASE; N(G) METHYLARGININE; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; OXYGEN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BREATHING RATE; CONTROLLED STUDY; ENERGY METABOLISM; MITOCHONDRIAL RESPIRATION; MOUSE; MUSCLE METABOLISM; MUSCLE MITOCHONDRION; NONHUMAN; OXYGEN CONSUMPTION; PRIORITY JOURNAL; REGULATORY MECHANISM; RESPIROMETRY; SKELETAL MUSCLE;

ANIMALS; CELL RESPIRATION; ESCHERICHIA COLI; LIPOPOLYSACCHARIDES; MICE; MICE, INBRED C57BL; MITOCHONDRIA, MUSCLE; MUSCLE, SKELETAL; NITRIC OXIDE; OXYGEN;

ANIMALIA; ESCHERICHIA COLI; MUS;

EID: 84856558702     PISSN: 15677249     EISSN: 18728278     Source Type: Journal    
DOI: 10.1016/j.mito.2011.05.010     Document Type: Article

References (49)

1. Aguirre E., Cadenas S. GDP and carboxyatractylate inhibit 4-hydroxynonenal-activated proton conductance to differing degrees in mitochondria from skeletal muscle and heart. Biochim Biophys Acta 2010, 1797:1716-1726.
2. Aguirre E., Rodriguez-Juarez F., Bellelli A., Gnaiger E., Cadenas S. Kinetic model of the inhibition of respiration by endogenous nitric oxide in intact cells. Biochim Biophys Acta 2010, 1797:557-565.
3. Alderton W.K., Cooper C.E., Knowles R.G. Nitric oxide synthases: structure, function and inhibition. Biochem J 2001, 357:593-615.
4. Alvarez S., Boveris A. Mitochondrial nitric oxide metabolism in rat muscle during endotoxemia. Free Radic Biol Med 2004, 37:1472-1478.
5. Alvarez S., Valdez L.B., Zaobornyj T., Boveris A. Oxygen dependence of mitochondrial nitric oxide synthase activity. Biochem Biophys Res Commun 2003, 305:771-775.
6. Boveris A., Navarro A. Systemic and mitochondrial adaptive responses to moderate exercise in rodents. Free Radic Biol Med 2008, 44:224-229.
7. Boveris A., Alvarez S., Navarro A. The role of mitochondrial nitric oxide synthase in inflammation and septic shock. Free Radic Biol Med 2002, 33:1186-1193.
8. Boveris A., D'Amico G., Lores-Arnaiz S., Costa L.E. Enalapril increases mitochondrial nitric oxide synthase activity in heart and liver. Antioxid Redox Signal 2003, 5:691-697.
9. Boveris A., Valdez L.B., Alvarez S., Zaobornyj T., Boveris A.D., Navarro A. Kidney mitochondrial nitric oxide synthase. Antioxid Redox Signal 2003, 5:265-271.
10. Brookes P.S. Mitochondrial nitric oxide synthase. Mitochondrion 2004, 3:187-204.
11. Brown G.C. Nitric oxide regulates mitochondrial respiration and cell functions by inhibiting cytochrome oxidase. FEBS Lett 1995, 369:136-139.
12. Brunori M., Forte E., Arese M., Mastronicola D., Giuffre A., Sarti P. Nitric oxide and the respiratory enzyme. Biochim Biophys Acta 2006, 1757:1144-1154.
13. Bustamante J., Bersier G., Badin R.A., Cymeryng C., Parodi A., Boveris A. Sequential NO production by mitochondria and endoplasmic reticulum during induced apoptosis. Nitric Oxide 2002, 6:333-341.
14. Cadenas S., Brand M.D. Effects of magnesium and nucleotides on the proton conductance of rat skeletal-muscle mitochondria. Biochem J 2000, 348:209-213.
15. Cadenas S., Cadenas A.M. Fighting the stranger-antioxidant protection against endotoxin toxicity. Toxicology 2002, 180:45-63.
16. Carreras M.C., Peralta J.G., Converso D.P., Finocchietto P.V., Rebagliati I., Zaninovich A.A., Poderoso J.J. Modulation of liver mitochondrial NOS is implicated in thyroid-dependent regulation of O(2) uptake. Am J Physiol Heart Circ Physiol 2001, 281:H2282-H2288.
17. Costa L.E., La-Padula P., Lores-Arnaiz S., D'Amico G., Boveris A., Kurnjek M.L., Basso N. Long-term angiotensin II inhibition increases mitochondrial nitric oxide synthase and not antioxidant enzyme activities in rat heart. J Hypertens 2002, 20:2487-2494.
18. Csordas A., Pankotai E., Snipes J.A., Cselenyak A., Sarszegi Z., Cziraki A., Gaszner B., Papp L., Benko R., Kiss L., Kovacs E., Kollai M., Szabo C., Busija D.W., Lacza Z. Human heart mitochondria do not produce physiologically relevant quantities of nitric oxide. Life Sci 2007, 80:633-637.
19. Elfering S.L., Sarkela T.M., Giulivi C. Biochemistry of mitochondrial nitric-oxide synthase. J Biol Chem 2002, 277:38079-38086.
20. Erusalimsky J.D., Moncada S. Nitric oxide and mitochondrial signaling: from physiology to pathophysiology. Arterioscler Thromb Vasc Biol 2007, 27:2524-2531.
21. Escames G., Leon J., Macias M., Khaldy H., Acuna-Castroviejo D. Melatonin counteracts lipopolysaccharide-induced expression and activity of mitochondrial nitric oxide synthase in rats. FASEB J 2003, 17:932-934.
22. Escames G., Lopez L.C., Tapias V., Utrilla P., Reiter R.J., Hitos A.B., Leon J., Rodriguez M.I., Acuna-Castroviejo D. Melatonin counteracts inducible mitochondrial nitric oxide synthase-dependent mitochondrial dysfunction in skeletal muscle of septic mice. J Pineal Res 2006, 40:71-78.
23. Ghafourifar P., Richter C. Nitric oxide synthase activity in mitochondria. FEBS Lett 1997, 418:291-296.
24. Giulivi C. Functional implications of nitric oxide produced by mitochondria in mitochondrial metabolism. Biochem J 1998, 332:673-679.
25. Giulivi C. Characterization and function of mitochondrial nitric-oxide synthase. Free Radic Biol Med 2003, 34:397-408.
26. Giulivi C., Poderoso J.J., Boveris A. Production of nitric oxide by mitochondria. J Biol Chem 1998, 273:11038-11043.
27. Glancy B., Balaban R.S. Protein composition and function of red and white skeletal muscle mitochondria. Am J Physiol Cell Physiol. 2011, 300:C1280-C1290.
28. Gnaiger E. Bioenergetics at low oxygen: dependence of respiration and phosphorylation on oxygen and adenosine diphosphate supply. Respir Physiol 2001, 128:277-297.
29. Gnaiger E., Kuznetsov A.V. Mitochondrial respiration at low levels of oxygen and cytochrome c. Biochem Soc Trans 2002, 30:252-258.
30. Gnaiger E., Steinlechner-Maran R., Mendez G., Eberl T., Margreiter R. Control of mitochondrial and cellular respiration by oxygen. J Bioenerg Biomembr 1995, 27:583-596.
31. Gonzales G.F., Chung F.A., Miranda S., Valdez L.B., Zaobornyj T., Bustamante J., Boveris A. Heart mitochondrial nitric oxide synthase is upregulated in male rats exposed to high altitude (4,340m). Am J Physiol Heart Circ Physiol 2005, 288:H2568-H2573.
32. Hobbs A.J., Higgs A., Moncada S. Inhibition of nitric oxide synthase as a potential therapeutic target. Annu Rev Pharmacol Toxicol 1999, 39:191-220.
33. Kanai A.J., Pearce L.L., Clemens P.R., Birder L.A., VanBibber M.M., Choi S.Y., de Groat W.C., Peterson J. Identification of a neuronal nitric oxide synthase in isolated cardiac mitochondria using electrochemical detection. Proc Natl Acad Sci U S A 2001, 98:14126-14131.
34. Lacza Z., Puskar M., Figueroa J.P., Zhang J., Rajapakse N., Busija D.W. Mitochondrial nitric oxide synthase is constitutively active and is functionally upregulated in hypoxia. Free Radic Biol Med 2001, 31:1609-1615.
35. Lacza Z., Snipes J.A., Zhang J., Horvath E.M., Figueroa J.P., Szabo C., Busija D.W. Mitochondrial nitric oxide synthase is not eNOS, nNOS or iNOS. Free Radic Biol Med 2003, 35:1217-1228.
36. Lacza Z., Horn T.F., Snipes J.A., Zhang J., Roychowdhury S., Horvath E.M., Figueroa J.P., Kollai M., Szabo C., Busija D.W. Lack of mitochondrial nitric oxide production in the mouse brain. J Neurochem 2004, 90:942-951.
37. Lanone S., Mebazaa A., Heymes C., Henin D., Poderoso J.J., Panis Y., Zedda C., Billiar T., Payen D., Aubier M., Boczkowski J. Muscular contractile failure in septic patients: role of the inducible nitric oxide synthase pathway. Am J Respir Crit Care Med 2000, 162:2308-2315.
38. Lopez L.C., Escames G., Tapias V., Utrilla P., Leon J., Acuna-Castroviejo D. Identification of an inducible nitric oxide synthase in diaphragm mitochondria from septic mice: its relation with mitochondrial dysfunction and prevention by melatonin. Int J Biochem Cell Biol 2006, 38:267-278.
39. Mason M.G., Nicholls P., Wilson M.T., Cooper C.E. Nitric oxide inhibition of respiration involves both competitive (heme) and noncompetitive (copper) binding to cytochrome c oxidase. Proc Natl Acad Sci U S A 2006, 103:708-713.
40. Navarro A., Boveris A. Mitochondrial nitric oxide synthase, mitochondrial brain dysfunction in aging, and mitochondria-targeted antioxidants. Adv Drug Deliv Rev 2008, 60:1534-1544.
41. Navarro A., Lopez-Cepero J.M., Bandez M.J., Sanchez-Pino M.J., Gomez C., Cadenas E., Boveris A. Hippocampal mitochondrial dysfunction in rat aging. Am J Physiol Regul Integr Comp Physiol 2008, 294:R501-R509.
42. Pecina P., Gnaiger E., Zeman J., Pronicka E., Houstek J. Decreased affinity for oxygen of cytochrome-c oxidase in Leigh syndrome caused by SURF1 mutations. Am J Physiol Cell Physiol 2004, 287:C1384-C1388.
43. Peralta J.G., Finocchietto P.V., Converso D., Schopfer F., Carreras M.C., Poderoso J.J. Modulation of mitochondrial nitric oxide synthase and energy expenditure in rats during cold acclimation. Am J Physiol Heart Circ Physiol 2003, 284:H2375-H2383.
44. Quesada A., Sainz J., Wangensteen R., Rodriguez-Gomez I., Vargas F., Osuna A. Nitric oxide synthase activity in hyperthyroid and hypothyroid rats. Eur J Endocrinol 2002, 147:117-122.
45. Rey B., Roussel D., Teulier L., Eyenga P., Degletagne C., Belouze M., Duchamp C. Functional argument for the existence of an avian nitric oxide synthase in muscle mitochondria: effect of cold acclimation. FEBS Lett 2011, 585:173-177.
46. Riobo N.A., Melani M., Sanjuan N., Fiszman M.L., Gravielle M.C., Carreras M.C., Cadenas E., Poderoso J.J. The modulation of mitochondrial nitric-oxide synthase activity in rat brain development. J Biol Chem 2002, 277:42447-42455.
47. Rodriguez-Juarez F., Aguirre E., Cadenas S. Relative sensitivity of soluble guanylate cyclase and mitochondrial respiration to endogenous nitric oxide at physiological oxygen concentration. Biochem J 2007, 405:223-231.
48. Tay Y.M., Lim K.S., Sheu F.S., Jenner A., Whiteman M., Wong K.P., Halliwell B. Do mitochondria make nitric oxide? no?. Free Radic Res 2004, 38:591-599.
49. Venkatakrishnan P., Nakayasu E.S., Almeida I.C., Miller R.T. Absence of nitric-oxide synthase in sequentially purified rat liver mitochondria. J Biol Chem 2009, 284:19843-19855.