The beneficial effects of melatonin against heart mitochondrial impairment during sepsis: Inhibition of i NOS and preservation of n NOS

Journal of Pineal Research

Volumn 56, Issue 1, 2014, Pages 71-81

  Ortiz, Francisco ^a,b   García, José A ^a,b   Acuña Castroviejo, Darío ^a,b,c   Doerrier, Carolina ^a,b   Lõpez, Ana ^a,b   Venegas, Carmen ^a,b   Volt, Huayqui ^a,b   Luna Sánchez, Marta ^a,b   Lõpez, Luis C ^a,b   Escames, Germaine ^a,b  

^a UNIVERSITY OF GRANADA   (Spain)

^b UNIVERSITY OF GRANADA   (Spain)

^c HOSPITAL UNIVERSITARIO SAN CECILIO   (Spain)

Author keywords

antioxidant; free radicals; heart; melatonin; mitochondria; nitric oxide; nitric oxide synthases

Indexed keywords

GLUTATHIONE DISULFIDE; GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE; INDUCIBLE NITRIC OXIDE SYNTHASE; MELATONIN; NEURONAL NITRIC OXIDE SYNTHASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUCCINATE DEHYDROGENASE (UBIQUINONE); UBIQUINOL CYTOCHROME C REDUCTASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOENERGY; CONTROLLED STUDY; CYTOSOL; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME ACTIVITY; HEART MITOCHONDRION; HOMEOSTASIS; LIPID PEROXIDATION; MOUSE; NITROSATIVE STRESS; NONHUMAN; OXIDATIVE STRESS; PROTEIN CONTENT; PROTEIN EXPRESSION; RESPIRATORY CHAIN; SEPSIS;

ANTIOXIDANT; FREE RADICALS; HEART; MELATONIN; MITOCHONDRIA; NITRIC OXIDE; NITRIC OXIDE SYNTHASES;

ANALYSIS OF VARIANCE; ANIMALS; ANTIOXIDANTS; CYTOSOL; DISEASE MODELS, ANIMAL; GLUTATHIONE; LIPID PEROXIDATION; MELATONIN; MICE; MICE, KNOCKOUT; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MYOCARDIUM; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE I; NITRIC OXIDE SYNTHASE TYPE II; OXIDATIVE STRESS; SEPSIS;

EID: 84890123744     PISSN: 07423098     EISSN: 1600079X     Source Type: Journal    
DOI: 10.1111/jpi.12099     Document Type: Article

References (79)

1. Blanco J, Muriel-Bombin A, Sagredo V, et al. Incidence, organ dysfunction and mortality in severe sepsis: a Spanish multicentre study. Crit Care 2008; 12: R158. doi: 10.1186/cc7157.
2. Levy RJ,. Mitochondrial dysfunction, bioenergetic impairment, and metabolic down-regulation in sepsis. Shock 2007; 28: 24-28.
3. 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.
4. Escames G, Leõn J, Macías M, et al. Melatonin counteracts lipopolysaccharide-induced expression and activity of mitochondrial nitric oxide synthase in rats. FASEB J 2003; 17: 932-934.
5. Escames G, Lõpez LC, Tapias V, et al. Melatonin counteracts inducible mitochondrial nitric oxide synthase-dependent mitochondrial dysfunction in skeletal muscle of septic mice. J Pineal Res 2006; 40: 71-78.
6. Escames G, Lõpez LC, Ortiz F, et al. Attenuation of cardiac mitochondrial dysfunction by melatonin in septic mice. FEBS J 2007; 274: 2137-2147.
7. Lõpez LC, Escames G, Tapias V, et al. 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.
8. Massion PB, Feron O, Dessy C, et al. Nitric oxide and cardiac function: ten years after, and continuing. Circ Res 2003; 93: 388-398.
9. Kingma JG Jr, Simard D, Rouleau JR,. Modulation of nitric oxide affects myocardial perfusion-contraction matching in anaesthetized dogs with recurrent no-flow ischaemia. Exp Physiol 2011; 96: 1293-1301.
10. Nisoli E, Clementi E, Paolucci C, et al. Mitochondrial biogenesis in mammals: the role of endogenous nitric oxide. Science 2003; 299: 896-899.
11. Brealey D, Brand M, Hargreaves I, et al. Association between mitochondrial dysfunction and severity and outcome of septic shock. Lancet 2002; 360: 219-223.
12. Brealey D, Karyampudi S, Jacques TS, et al. Mitochondrial dysfunction in a long-term rodent model of sepsis and organ failure. Am J Physiol Regul Integr Comp Physiol 2004; 286: R491-R497.
13. Lõpez LC, Escames G, Ortiz F, et al. Melatonin restores the mitochondrial production of ATP in septic mice. Neuro Endocrinol Lett 2006; 27: 623-630.
14. Escames G, Lõpez LC, Ortiz F, et al. Age-dependent lipopolysaccharide-induced iNOS expression and multiorgan failure in rats: effects of melatonin treatment. Exp Gerontol 2006; 41: 1165-1173.
15. Forstermann U, Boissel JP, Kleinert H,. Expressional control of the 'constitutive' isoforms of nitric oxide synthase (NOS I and NOS III). FASEB J 1998; 12: 773-790.
16. Macmicking J, Xie QW, Nathan C,. Nitric oxide and macrophage function. Annu Rev Immunol 1997; 15: 323-350.
17. Zaobornyj T, Ghafourifar P,. Strategic localization of heart mitochondrial NOS: a review of the evidence. Am J Physiol Heart Circ Physiol 2012; 303: H1283-H1293.
18. Brenman JE, Chao DS, Xia H, et al. Nitric oxide synthase complexed with dystrophin and absent from skeletal muscle sarcolemma in Duchenne muscular dystrophy. Cell 1995; 82: 743-752.
19. Andrew PJ, Mayer B,. Enzymatic function of nitric oxide synthases. Cardiovasc Res 1999; 43: 521-531.
20. Alderton WK, Cooper CE, Knowles RG,. Nitric oxide synthases: structure, function and inhibition. Biochem J 2001; 357: 593-615.
21. Sen S, Kawahara B, Chaudhuri G,. Mitochondrial-associated nitric oxide synthase activity inhibits cytochrome c oxidase: implications for breast cancer. Free Radic Biol Med 2013; 57: 210-220.
22. Leõn J, Acuña-Castroviejo D, Escames G, et al. Melatonin mitigates mitochondrial malfunction. J Pineal Res 2005; 38: 1-9.
23. Boveris A, Costa LE, Poderoso JJ, et al. Regulation of mitochondrial respiration by oxygen and nitric oxide. Ann N Y Acad Sci 2000; 899: 121-135.
24. Cadenas E, Poderoso JJ, Antunes F, et al. Analysis of the pathways of nitric oxide utilization in mitochondria. Free Radic Res 2000; 33: 747-756.
25. Poderoso JJ, Carreras MC, Lisdero C, et al. Nitric oxide inhibits electron transfer and increases superoxide radical production in rat heart mitochondria and submitochondrial particles. Arch Biochem Biophys 1996; 328: 85-92.
26. Quijano C, Romero N, Radi R,. Tyrosine nitration by superoxide and nitric oxide fluxes in biological systems: modeling the impact of superoxide dismutase and nitric oxide diffusion. Free Radic Biol Med 2005; 39: 728-741.
27. Riobo NA, Clementi E, Melani M, et al. Nitric oxide inhibits mitochondrial NADH:ubiquinone reductase activity through peroxynitrite formation. Biochem J 2001; 359: 139-145.
28. Boczkowski J, Lisdero CL, Lanone S, et al. Endogenous peroxynitrite mediates mitochondrial dysfunction in rat diaphragm during endotoxemia. FASEB J 1999; 13: 1637-1646.
29. Brown GC,. Regulation of mitochondrial respiration by nitric oxide inhibition of cytochrome c oxidase. Biochim Biophys Acta 2001; 1504: 46-57.
30. Leõn J, Escames G, Rodríguez MI, et al. Inhibition of neuronal nitric oxide synthase activity by N1-acetyl-5-methoxykynurenamine, a brain metabolite of melatonin. J Neurochem 2006; 98: 2023-2033.
31. Rodella LF, Filippini F, Bonomini F, et al. Beneficial effects of melatonin on nicotine-induced vasculopathy. J Pineal Res 2010; 48: 126-132.
32. Wichterman KA, Baue AE, Chaudry IH,. Sepsis and septic shock-a review of laboratory models and a proposal. J Surg Res 1980; 29: 189-201.
33. Tatoyan A, Giulivi C,. Purification and characterization of a nitric-oxide synthase from rat liver mitochondria. J Biol Chem 1998; 273: 11044-11048.
34. Lowry OH, Rosenbrough NJ, Farral AL, et al. Protein measurement with the Folin phenol reagent. J Biol Chem 1951; 193: 265-275.
35. Bredt DS, Snyder SH,. Nitric oxide mediates glutamate-linked enhancement of cGMP levels in the cerebellum. Proc Natl Acad Sci U S A 1989; 86: 9030-9033.
36. Green LC, Ruiz DE, Luzuriaga K., Nitrate biosynthesis in man. Proc Natl Acad Sci USA 1981; 78: 7764-7768.
37. Esterbauer H, Cheeseman KH,. Determination of aldehidic lipid peroxidation products: malonaldehide and 4-hydroxynonenal. Methods Enzymol 1990; 186: 407-421.
38. Levine RL, Garland D, Oliver CN, et al. Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol 1990; 186: 464-478.
39. Jaskot RH, Charlet EG, Grose EC, et al. An automated analysis of glutathione peroxidase, S-transferase, and reductase activity in animal tissue. J Anal Toxicol 1983; 7: 86-88.
40. Hissin PJ, Hilf R,. A fluorometric method for determination of oxidized and reduced glutathione in tissues. Anal Biochem 1976; 74: 214-226.
41. Barrientos A,. In vivo and in organello assessment of OXPHOS activities. Methods 2002; 26: 307-316.
42. Brusque AM, Borba RR, Schuck PF, et al. Inhibition of the mitochondrial respiratory chain complex activities in rat cerebral cortex by methylmalonic acid. Neurochem Int 2002; 40: 593-601.
43. Ghafourifar P, Richter C,. Nitric oxide synthase activity in mitochondria. FEBS Lett 1997; 418: 291-296.
44. Kanai AJ, Pearce LL, Clemens PR, et al. 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.
45. Brookes PS,. Mitochondrial nitric oxide synthase. Mitochondrion 2004; 3: 187-204.
46. Tay YM, Lim KS, Sheu FS, et al. Do mitochondria make nitric oxide? no? Free Radic Res 2004; 38: 591-599.
47. Elfering SL, Sarkela TM, Giulivi C,. Biochemistry of mitochondrial nitric-oxide synthase. J Biol Chem 2002; 277: 38079-38086.
48. Haynes V, Elfering S, Traaseth N, et al. Mitochondrial nitric-oxide synthase: enzyme expression, characterization, and regulation. J Bioenerg Biomembr 2004; 36: 341-346.
49. Acuña-Castroviejo D, Escames G, Lõpez LC, et al. Melatonin and nitric oxide: two required antagonists for mitochondrial homeostasis. Endocrine 2005; 27: 159-168.
50. Valdez LB, Zaobornyj T, Boveris A,. Functional activity of mitochondrial nitric oxide synthase. Methods Enzymol 2005; 396: 444-455.
51. Crouser ED, Julian MW, Huff JE, et al. Abnormal permeability of inner and outer mitochondrial membranes contributes independently to mitochondrial dysfunction in the liver during acute endotoxemia. Crit Care Med 2004; 32: 478-488.
52. Callahan LA, Supinski GS,. Downregulation of diaphragm electron transport chain and glycolytic enzyme gene expression in sepsis. J Appl Physiol 2005; 99: 1120-1126.
53. Prime TA, Blaikie FH, Evans C, et al. A mitochondria-targeted S-nitrosothiol modulates respiration, nitrosates thiols, and protects against ischemia-reperfusion injury. Proc Natl Acad Sci U S A 2009; 106: 10764-10769.
54. Chouchani ET, Hurd TR, Nadtochiy SM, et al. Identification of S-nitrosated mitochondrial proteins by S-nitrosothiol difference in gel electrophoresis (SNO-DIGE): implications for the regulation of mitochondrial function by reversible S-nitrosation. Biochem J 2010; 430: 49-59.
55. Poderoso JJ, Peralta JG, Lisdero CL, et al. Nitric oxide regulates oxygen uptake and hydrogen peroxide release by the isolated beating rat heart. Am J Physiol 1998; 274: C112-C119.
56. Valdez LB, Zaobornyj T, Alvarez S, et al. Heart mitochondrial nitric oxide synthase. Effects of hypoxia and aging. Mol Aspects Med 2004; 25: 49-59.
57. Carreras MC, Poderoso JJ,. Mitochondrial nitric oxide in the signaling of cell integrated responses. Am J Physiol Cell Physiol 2007; 292: C1569-C1580.
58. Brown GC, Borutaite V,. Inhibition of mitochondrial respiratory complex I by nitric oxide, peroxynitrite and S-nitrosothiols. Biochim Biophys Acta 2004; 1658: 44-49.
59. Callahan LA, Supinski GS,. Sepsis induces diaphragm electron transport chain dysfunction and protein depletion. Am J Respir Crit Care Med 2005; 172: 861-868.
60. Schreiber J, Jenner RG, Murray HL, et al. Coordinated binding of NF-kappaB family members in the response of human cells to lipopolysaccharide. Proc Natl Acad Sci USA 2006; 103: 5899-5904.
61. Anderson MF, Sims NR,. The effects of focal ischemia and reperfusion on the glutathione content of mitochondria from rat brain subregions. J Neurochem 2002; 81: 541-549.
62. Huang J, Philbert MA,. Cellular responses of cultured cerebellar astrocytes to ethacrynic acid-induced perturbation of subcellular glutathione homeostasis. Brain Res 1996; 711: 184-192.
63. Martin M, Macias M, Escames G, et al. Melatonin but not vitamins C and E maintains glutathione homeostasis in t-butyl hydroperoxide-induced mitochondrial oxidative stress. FASEB J 2000; 14: 1677-1679.
64. Crouser ED, Julian MW, Blaho DV, et al. Endotoxin-induced mitochondrial damage correlates with impaired respiratory activity. Crit Care Med 2002; 30: 276-284.
65. Acuña-Castroviejo D, Lõpez LC, Escames G, et al. Melatonin-mitochondria interplay in health and disease. Curr Top Med Chem 2011; 11: 221-240.
66. Mayo JC, Sainz RM, Tan DX, et al. Anti-inflammatory actions of melatonin and its metabolites, N1-acetyl-N2-formyl-5-methoxykynuramine (AFMK) and N1-acetyl-5-methoxykynuramine (AMK), in macrophages. J Neuroimmunol 2005; 165: 139-149.
67. Mauriz JL, Collado PS, Veneroso C, et al. A review of the molecular aspects of melatonin's anti-inflammatory actions: recent insights and new perspectives. J Pineal Res 2013; 54: 1-14.
68. Reiter RJ, Fuentes-Broto L, Tan DX,. Melatonin: a multitasking molecule. Prog Brain Res 2010; 181: 127-151.
69. Rodríguez MI, Escames G, Lõpez LC, et al. Melatonin administration prevents cardiac and diaphragmatic mitochondrial oxidative damage in senescence accelerated mice. J Endocrinol 2007; 194: 637-643.
70. Giacomo CG, Antonio M,. Melatonin in cardiac ischemia/reperfusion-induced mitochondrial adaptive changes. Cardiovasc Hematol Disord Drug Targets 2007; 7: 163-169.
71. Galano A, Tan DX, Reiter RJ,. On the free radical scavenging activities of melatonin's metabolites, AFMK and AMK. J Pineal Res 2013; 54: 245-257.
72. Zhang H, Liu D, Wang X, et al. Melatonin improved rat cardiac mitochondria and survival rate in septic heart injury. J Pineal Res 2013; 55: 1-6.
73. Rodriguez C, Mayo JC, Sainz RM, et al. Regulation of antioxidant enzymes: a significant role for melatonin. J Pineal Res 2004; 36: 1-9.
74. Fischer TW, Kleszczynski K, Hardkop LH, et al. Melatonin enhances antioxidative enzyme gene expression (CAT, GPx, SOD), prevents their UVR-induced depletion, and protects against the formation of DNA damage (8-hydroxy-2′-deoxyguanosine) in ex vivo human skin. J Pineal Res 2013; 54: 303-312.
75. Crespo E, Macías M, Pozo D, et al. Melatonin inhibits expression of the inducible NO synthase II in liver and lung and prevents endotoxemia in lipopolysaccharide-induced multiple organ dysfunction syndrome in rats. FASEB J 1999; 13: 1537-1546.
76. Acuña-Castroviejo D, Escames G, Rodríguez MI, et al. Melatonin role in the mitochondrial function. Front Biosci 2007; 12: 947-963.
77. Lõpez A, García JA, Escames G, et al. Melatonin protects the mitochondria from oxidative damage reducing oxygen consumption, membrane potential, and superoxide anion production. J Pineal Res 2009; 46: 188-198.
78. Brookes PS, Levonen AL, Shiva S, et al. Mitochondria: regulators of signal transduction by reactive oxygen and nitrogen species. Free Radic Biol Med 2002; 33: 755-764.
79. Gitto E, Karbownik M, Reiter RJ, et al. Effects of melatonin treatment in septic newborns. Pediatr Res 2001; 50: 756-760.