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Lipid Metabolism in Rats is Modified by Nitric Oxide Availability Through a Ca++-Dependent Mechanism

  • Original Article
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Lipids

Abstract

We studied lipid metabolism and the antioxidant defense system in plasma and liver of rats fed diets supplemented with l ω-nitro-l-arginine methyl ester (l-NAME), isosorbide dinitrate (DIS), l-arginine (Arg), or the associations of these drugs. Liver hydroperoxide and thiobarbituric-acid-reactive substance (TBARS) levels were decreased by Arg and increased by l-NAME or DIS treatments. Oxidized glutathione and conjugated dienes were increased by DIS. Nitrate + nitrite levels and serum calcium ([Ca++]) were incremented by Arg or DIS and reduced by l-NAME. Superoxide dismutase and catalase activities decreased under Arg treatment, while l-NAME or DIS caused stimulation. Liver high-density lipoprotein (HDL) cholesterol was increased by DIS or NAME (alone or associated with Arg). Free fatty acids and neutral and polar lipids were increased by Arg, l-NAME, and DIS. However, predominating phospholipid synthesis increased the neutral/polar ratio. Decreased levels of nitric oxide (NO) (low [Ca++]) was directly associated with increased fatty acid synthetase, decreased phospholipase A2, carnitine-palmitoyl transferase, and fatty acid desaturase activities. Raised NO (high [Ca++]) inversely correlated with increased phospholipase-A2 and acyl-coenzyme A (CoA) synthetase and decreased fatty acid synthetase and β-oxidation rate. Arg or DIS produced changes that were partially reverted by association with l-NAME. Based on these observations, prolonged therapeutical approaches using drugs that modify NO availability should be carefully considered.

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Abbreviations

NO:

Nitric oxide

[Ca2+]:

Calcium concentration

[NOx]:

Nitrite plus nitrate concentration

Arg:

l-arginine

CAT:

Catalase

DIS:

Isosorbide dinitrate

FAS:

Fatty acid synthetase

GSHPx:

Glutathione peroxidase

GSHRd:

Glutathione reductase

GSHTr:

Glutathione transferase

LLC:

Low-level chemiluminescence

l-NAME:

lω-nitro-l-arginine methyl ester

NL:

Neutral lipids

PL:

Polar lipids (phospholipids)

PL-A2 :

Phospholipase A2

ROOHs:

Lipid hydroperoxides

SOD:

Superoxide dismutase

References

  1. Bobé P, Benihoud K, Grandjon D, Opolon P, Pritchard LL, Huchet R (1999) Nitric oxide mediation of active immunosuppression associated with graft-versus-host reaction. Blood 94:1028–1037

    PubMed  Google Scholar 

  2. Barron JT, Gu L, Parrillo E (2001) Endothelial- and nitric oxide-dependent effects on oxidative metabolism of intact artery. Biochim Biophys Acta 1506:204–211

    Article  PubMed  CAS  Google Scholar 

  3. Pavlick KP, Laroux FS, Fuseler J, Wolff RE, Gray L, Hoffman J, Grisham MB (2002) Role of reactive metabolites of oxygen and nitrogen in inflammatory bowel disease. Free Radic Biol Med 33:311–322

    Article  PubMed  CAS  Google Scholar 

  4. Sakuma S, Fujimoto Y, Katoh Y, Fujita T (2003) The effects of nitric oxide and peroxynitrite on the formation of prostaglandin and arachidonoyl-CoA formed from arachidonic acid in rabbit kidney medulla microsomes. Prostaglandins Leukot Essent Fatty Acids 68:343–349

    Article  PubMed  CAS  Google Scholar 

  5. Schopfer FJ, Baker PR, Freeman BA (2003) No-dependent protein nitration: a cell signaling event or an oxidative inflammatory response? Trends Biochem Sci 28:646–654

    Article  PubMed  CAS  Google Scholar 

  6. Clapp BR, Hingorani AD, Kharbanda RK, Mohamed-Ali V, Stephens JW, Vallance P, MacAllister RJ (2004) Inflammation-induced endothelial dysfunction involves reduced nitric oxide bioavailability and increased oxidant stress. Cardiovasc Res 64:172–178

    Article  PubMed  CAS  Google Scholar 

  7. Lipton SA, Nicotera P (1998) Calcium, free radicals and excitotoxins in neuronal apoptosis. Cell Calcium 23:165–171

    Article  PubMed  CAS  Google Scholar 

  8. Bonfoco E, Krainc D, Ankarcrona M, Nicotera P, Lipton SA (1995) Apoptosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N-methyl-d-aspartate or nitric oxide/superoxide in cortical cell cultures. Proc Natl Acad Sci USA 92:7162–7166

    Article  PubMed  CAS  Google Scholar 

  9. Heinloth A, Brüne B, Fischer B, Galle J (2002) Nitric oxide prevents oxidised LDL-induced p53 accumulation, cytochrome c translocation, and apoptosis in macrophages via guanylate cyclase stimulation. Atherosclerosis 162:93–101

    Article  PubMed  CAS  Google Scholar 

  10. Murphy MP (1999) Nitric oxide and cell death. Biochim Biophys Acta 1411:401–414

    Article  PubMed  CAS  Google Scholar 

  11. Leonard TO, Lydic R (1997) Pontine nitric oxide modulates acetylcholine release, rapid eye movement sleep generation, and respiratory rate. J Neurosci 17:774–785

    PubMed  CAS  Google Scholar 

  12. Kiss J, Zsilla G, Vizi ES (2004) Inhibitory effect of nitric oxide dopamine transporters: interneuronal communication without receptors. Neurochem Int 45:485–489

    Article  PubMed  CAS  Google Scholar 

  13. Brown GC (1999) Nitric oxide and mitochondrial respiration. Biochim Biophys Acta 1411:351–369

    Article  PubMed  CAS  Google Scholar 

  14. Valdez LB, Alvarez S, Arnaiz SL, Schópfer F, Carreras MC, Poderoso JJ, Boveris A (2000) Reactions of peroxynitrite in the mitochondrial matrix. Free Radic Biol Med 34:349–356

    Article  Google Scholar 

  15. Abeywardena MY, Head RJ (2001) Long chain n-3 polyunsaturated fatty acids and blood vessel function. Cardiovasc Res 52:361–371

    Article  PubMed  CAS  Google Scholar 

  16. Miatello R, Risler N, Castro C, González S, Rüttler M, Cruzado M (2001) Aortic smooth muscle cell proliferation and endothelial nitric oxide synthase activity in fructose-fed rats. Am J Hypertens 14:1135–1141

    Article  PubMed  CAS  Google Scholar 

  17. Bilsborough W, Green DJ, Mamotte CD, Van Bockxmeer FM, O´Driscoll GJ, Taylor RR (2003) Endothelial nitric oxide synthase gene polymorphism, homocysteine, cholesterol, and vascular endothelial function. Atherosclerosis 169:131–138

    Article  PubMed  CAS  Google Scholar 

  18. Stoclet JC, Chataigneau T, Ndiaye M, Oak MH, Bedoui JE, Chataigneau M, Schini-Kerth VB (2004) Vascular protection by dietary polyphenols. Eur J Pharmacol 500:299–313

    Article  PubMed  CAS  Google Scholar 

  19. Pereira AC, Sposito AC, Mota GF, Cunha RS, Herkenhoff FL, Mill JG, Krieger JE (2006) Endothelial nitric oxide synthase gene variant modulates the relationship between serum cholesterol levels and blood pressure in the general population: new evidence for a direct effect of lipids in arterial blood pressure. Atherosclerosis 18:193–200

    Article  CAS  Google Scholar 

  20. Mohr S, Stamler JS, Brune B (1994) Mechanism of covalent modification of glyceraldehydes-3-phosphate dehydrogenase at its active site thiol by nitric oxide, peroxynitrite and related nitrosating agents. FEBS Lett 348:223–227

    Article  PubMed  CAS  Google Scholar 

  21. Gross SS, Wolin MS (1995) Nitric oxide pathophysiological mechanisms. Annu Rev Physiol 57:737–769

    Article  PubMed  CAS  Google Scholar 

  22. Welsh N, Sandler S (1992) Interleukin-1β induces nitric oxide production and inhibits the activity of aconitase without decreasing glucose oxidation rates in isolated mouse pancreatic islets. Biochem Biophys Res Commun 182:333–340

    Article  PubMed  CAS  Google Scholar 

  23. Ginter E (1979) Chronic marginal vitamin C deficiency: biochemistry and pathophysiology. World Rev Nutr Diet 33:104–141

    PubMed  CAS  Google Scholar 

  24. Nambisan B, Kurup PA (1975) Ascorbic acid and glycosaminoglycan and lipid metabolism in guinea pigs fed normal and atherogenic diets. Atherosclerosis 22:447–461

    Article  PubMed  CAS  Google Scholar 

  25. Chupukdaroen N, Komaratat P, Wilairat P (1985) Effects of vitamin E deficiency on the distribution of cholesterol in plasma lipoproteins and the activity of cholesterol 7α-hydroxylase in rabbit liver. J Nutr 115:468–472

    Google Scholar 

  26. Stone WL, Scott RL, Stewart EM, Kheshti A (1994) Lipoprotein alterations in the spontaneously hypertensive rat fed diets deficient in selenium and vitamin E. Proc Soc Exp Biol Med 206:130–137

    PubMed  CAS  Google Scholar 

  27. Al-Othman AA, Rosenstein F, Lei KY (1993) Cooper deficiency increases in vivo hepatic synthesis of fatty acids, triacylglycerols, and phospholipids in rats. Proc Soc Exp Biol Med 204:97–103

    PubMed  CAS  Google Scholar 

  28. Scott RL, Kheshti A, Heimberg M, Wilcox HG, Stone WL (1991) The role of selenium in the secretion of very low density lipoprotein in the isolated perfused rat liver. Biochem J 279:741–745

    PubMed  CAS  Google Scholar 

  29. Khedara A, KawaI Y, Kayashita J, Kato N (1996) Feeding rats the nitric oxide synthase inhibitor, l-n ωnitroarginine, elevates serum triglyceride and cholesterol and lowers hepatic fatty acid oxidation. J Nutr 126:2563–2567

    PubMed  CAS  Google Scholar 

  30. Khedara A, Goto T, Morishima M, Kayashita J, Kato N (1999) Elevated body fat in rats by the dietary nitric oxide synthase inhibitor, l-N-omega-nitroarginine. Biosci Biotechnol Biochem 63:698–702

    Article  PubMed  CAS  Google Scholar 

  31. Patel RP, McAndrew J, Sellak H, White CR, Jo H, Freeman BA, Darley-Usmar VM (1999) Biological aspects of reactive nitrogen species. Biochim Biophys Acta 1411:385–400

    Article  PubMed  CAS  Google Scholar 

  32. Hogg N, Kalyanaraman B (1999) Nitric oxide and lipid peroxidation. Biochim Biophys Acta 1411:378–384

    Article  PubMed  CAS  Google Scholar 

  33. Reeves PG, Nielsen FH, Fahey GC Jr (1993) AIN-93 Purified Diets for Laboratory Rodents: Final Report of the American Institute of Nutrition ad hoc Writing Committee on the Reformulation of the AIN-76A Rodent Diet. J Nutr 123:1939–1951

    PubMed  CAS  Google Scholar 

  34. National Research Council, Guide for the Care and Use of Laboratory Animals (1985) Publication N° 85–23 (rev), National Institute of Health, Bethesda

  35. Marra CA, Alaniz MJT de, Brenner RR (1986) Modulation of Δ6 and Δ5 rat liver microsomal desaturase activities by dexamethasone-induced factor. Biochim Biophys Acta 879:388–393

    PubMed  CAS  Google Scholar 

  36. Kler RS, Jackson S, Barlett K, Bindoff LA, Eaton S, Pourfarzam M, Frerman FE, Goodman SI, Watmough NJ, Turnbull DM (1991) Quantitation of acyl-CoA and acylcarnitine esters accumulated during abnormal mitochondrial fatty acid oxidation. J Biol Chem 266:22932–22938

    PubMed  CAS  Google Scholar 

  37. Marra CA, Alaniz MJT de (2000) Calcium deficiency modifies polyunsaturated fatty acid metabolism in growing rats. Lipids 35:983–990

    Article  PubMed  CAS  Google Scholar 

  38. Marra CA, Alaniz MJT de (1999) Acyl-CoA synthetase activity in liver microsomes from calcium-deficient rats. Lipids 34:343–354

    Article  PubMed  CAS  Google Scholar 

  39. Tomlinson CW, Dhalla SN (1972) Myocardial contractility. II. Effect of changes in cardiac function on the subcellular distribution of calcium in the isolated perfused rat heart. Can J Physiol Pharmacol 50:853–859

    PubMed  CAS  Google Scholar 

  40. Verdon CP, Burton BA, Prior RL (1995) Sample pretreatment with nitrate reductase and glucose-6-phopshate dehydrogenase quantitatively reduces nitrate while avoiding interference by NADP+ when the Griess reaction is used to assay for nitrite. Anal Biochem 224:502–508

    Article  PubMed  CAS  Google Scholar 

  41. Dodge JT, Mitchell C, Hanahan DJ (1963) The preparation and chemical characteristics of hemoglobin-free ghosts of human erythrocytes. Arch Biochem Biophys 100:119–130

    Article  PubMed  CAS  Google Scholar 

  42. Berlin E, Bhathena SJ, Judd JT, Nair PP, Jones DY (1989) Taylor, P.R. dietary fat and hormonal effects on erythrocyte membrane fluidity and lipid composition in adult women. Metabolism 38:790–796

    Article  PubMed  CAS  Google Scholar 

  43. Yagi K (1976) A simple fluorometric assay for lipoperoxide in blood plasma. Biochem Med 15:212–216

    Article  PubMed  CAS  Google Scholar 

  44. Nourooz-Zadeh J, Tajaddini-Sarmandi J, McCarthy S, Betteridge DJ, Wolff SP (1995) Elevated levels of authentic plasma hydroperoxides in NIDDM. Diabetes 44:1054–1058

    Article  PubMed  CAS  Google Scholar 

  45. Asensi M, Sastre J, Pallardo FV, García de la Asunción J, Estrela JM, Vina JA (1994) High-performance liquid chromatography method for measurement of oxidized glutathion in biological samples. Anal Biochem 217:323–328

    Article  PubMed  CAS  Google Scholar 

  46. Brigelius R, Muckel C, Akerboom TP, Sies H (1983) Identification and quantitation of glutathione in hepatic protein mixed disulfides and its relationship to glutathione disulfide. Biochem Pharmacol 32:2529–2534

    Article  PubMed  CAS  Google Scholar 

  47. Buttriss JL, Diplock AT (1984) High-performance liquid chromatography methods for vitamin e in tissues. Methods Enzymol 105:131–138

    PubMed  CAS  Google Scholar 

  48. Bagnati M, Bordone R, Perugini C, Cau C, Albano E, Bellomo G (1998) Cu(I) availability paradoxically antagonizes antioxidant consumption and lipid peroxidation during the initiation phase of copper-induced LDL oxidation. Biochem Biophys Res Commun 253:235–240

    Article  PubMed  CAS  Google Scholar 

  49. Benzie IF (1996) An automated specific, spectrophotometric method for measuring ascorbic acid in plasma (EFTSA). Clin Biochem 29:111–116

    Article  PubMed  CAS  Google Scholar 

  50. Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126

    Article  PubMed  CAS  Google Scholar 

  51. Flohé L, Ötting F (1984) Superoxide dismutase assays. Methods Enzymol 105:93–104

    PubMed  Google Scholar 

  52. Wheeler MD, Nakagami M, Bradford BU, Uesugi T, Mason RP, Connor HD, Dikalova A, Kadiiska M, Thurman RG (2001) Overexpression of manganese superoxide dismutase prevents alcohol-induced liver injury in the rat. J Biol Chem 276:36664–36672

    Article  PubMed  CAS  Google Scholar 

  53. Habig WH, Pabst MJ, Jakoby WB (1984) Glutathione-S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139

    Google Scholar 

  54. Carlberg I, Mannervick B (1985) Glutathione reductase. Methods Enzymol 113:484–490

    PubMed  CAS  Google Scholar 

  55. Wright JR, Rumbaugh RC, Colby HD, Miles PR (1979) The relationship between chemiluminescence and lipid peroxidation in rat hepatic microsomes. Arch Biochem Biophys 192:344–351

    Article  PubMed  CAS  Google Scholar 

  56. Folch J, Lees M, Sloane GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509

    PubMed  CAS  Google Scholar 

  57. Hanahan DJ, Dittner JC, Warashina E (1957) A columm chromatographic separation of classes of phospholipides. J Biol Chem 228:685–690

    PubMed  CAS  Google Scholar 

  58. Malins DC, Mangold HK (1960) Analysis of complex lipid mixtures by thin layer chromatographic and complementary methods. J Am Oil Chem Soc 37:576–582

    CAS  Google Scholar 

  59. Neskovic NM, Kostic DM (1968) Quantitative analysis of rat liver phospholipids by a two-step thin-layer chromatographic procedure. J Chromatogr 35:297–300

    Article  PubMed  CAS  Google Scholar 

  60. Marra CA, Alaniz MJT de (1989) Influence of testosterone administration on the biosynthesis of unsaturated fatty acids in male and female rats. Lipids 24:1014–1019

    Article  PubMed  CAS  Google Scholar 

  61. Allain CC, Poon LS, Chan CS, Richmond W, Fu PC (1974) Enzymatic determination of total serum cholesterol. Clin Chem 20:470–475

    PubMed  CAS  Google Scholar 

  62. Marra CA, Alaniz MJT de (1990) Mineralocorticoids modify rat liver Δ6 desaturase activity and other parameters of lipid metabolism. Biochem Int 22:483–493

    PubMed  CAS  Google Scholar 

  63. Chen PS, Toribara TY, Warner H (1956) Microdetermination of phosphorus. Anal Chem 33:1405–1406

    Google Scholar 

  64. Hirata F, Schiffmann E, Venkatasubramanian K, Salomon D, Axelrod J (1980) A phospholipase A2 inhibitory protein in rabbit neutrophils induced by glucocorticoids. Proc Natl Acad Sci USA 77:2533–2536

    Article  PubMed  CAS  Google Scholar 

  65. Irazú CE, González-Rodríguez S, Brenner RR (1993) Δ5 Desaturase activity in rat kidney microsomes. Mol Cell Biochem 129:31–37

    Article  PubMed  Google Scholar 

  66. López Jiménez J, Bordoni A, Hrelia S, Rossi CA, Turchetto E, Zamora Navarro S, Biagi PL (1993) Evidence for a detectable delta-6-desaturase activity in rat heart microsomes: aging influence on enzyme activity. Biochem Biophys Res Commun 192:1037–1041

    Article  PubMed  Google Scholar 

  67. Tanaka T, Hosaka K, Hoshimaru M, Numa S (1979) Purification and properties of long-chain acyl-coenzyme-A synthetase from rat liver. Eur J Biochem 98:165–172

    Article  PubMed  CAS  Google Scholar 

  68. Horning MG, Martin DB, Karmen A, Vagelos PR (1961) Fatty acid synthesis in adipose tissue. II. Enzymatic synthesis of branched chain and odd-numbered fatty acids. J Biol Chem 236:669–672

    PubMed  CAS  Google Scholar 

  69. Bieber LL, Fiol C (1986) Purification and assay of carnitine acyltransferases. Methods Enzymol 123:276–284

    PubMed  CAS  Google Scholar 

  70. Laun RA, Rapsch B, Abel W, Schroder O, Roher HD, Ekkerkamp A, Schulte KM (2001) The determination of ketone bodies: preanalytical, analytical and physiological considerations. Clin Exp Med 1:201–209

    Article  PubMed  CAS  Google Scholar 

  71. Duncombe WG, Rising TJ (1973) Quantitative extraction and determination of non-esterified fatty acids in plasma. J Lipid Res 14:258–261

    PubMed  CAS  Google Scholar 

  72. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  73. Hogg N, Kalyanaraman B (1999) Nitric oxide and lipid peroxidation. Biochim Biophys Acta 141:378–384

    Google Scholar 

  74. Joshi MS, Ponthier JL, Lancaster JR Jr (1999) Cellular antioxidant and pro-oxidant actions of nitric oxide. Free Rad Biol Med 27:1357–1366

    Article  PubMed  CAS  Google Scholar 

  75. Moshage H (1997) Nitric oxide determinations: much ado about NO•-thing? Clin Chem 43:553–556

    PubMed  CAS  Google Scholar 

  76. Adams MR, Phu CV, Stocker R, Celermajer DS (1999) Lack of antioxidant activity of the antiatherogenic compound l-arginine. Atherosclerosis 146:329–335

    Article  PubMed  CAS  Google Scholar 

  77. Tapiero H, Mathé G, Couvreur P, Tew KD (2002) Free aminoacids in human health and pathologies. (I) Arginine. Biomed Pharmacother 56:439–445

    Article  PubMed  CAS  Google Scholar 

  78. George J, Shmuel SB, Roth A, Her I, Izraelov S, Deutsch V, Keren G, Miller H (2004) l-Arginine attenuates lymphocyte activation and anti-oxidized LDL antibody levels in patients undergoing angioplasty. Atherosclerosis 174:323–327

    PubMed  CAS  Google Scholar 

  79. Böger RH, Bode-Böger SM, Frölich JC (1996) The l-Arginine-nitric oxide pathway: role in atherosclerosis and therapeutic implications. Atherosclerosis 127:1–11

    Article  PubMed  Google Scholar 

  80. Slawinski M, Grodzinska L, Kostka-Trabka E, Bieron K, Goszcz A, Gryglewski RJ (1996) l-Arginine—substrate for NO synthesis—its beneficial effects in therapy of patients with peripheral arterial disease: comparison with placebo-preliminary results. Acta Physiol Hung 84:457–458

    PubMed  CAS  Google Scholar 

  81. Bult H, Herman AG, Matthys KE (1999) Antiatherosclerotic activity of drugs in relation to nitric oxide function. Eur J Pharmacol 375:157–176

    Article  PubMed  CAS  Google Scholar 

  82. Moore PK, Handy RL (1997) Selective inhibitors of neuronal nitric oxide synthase—is no NOS really good NOS for the nervous system? Trends Pharmacol Sci 18:204–211

    PubMed  CAS  Google Scholar 

  83. Ding-Zhou L, Marchand-Verrecchia C, Croci N, Plotkine M, Margaill I (2002) l-NAME reduces infarctation, neurological deficit and blood–brain barrier disruption following cerebral ischemia in mice. Eur J Pharmacol 457:137–146

    Article  PubMed  Google Scholar 

  84. Patel RP, Levonen AL, Crawford JH, Darley-Usmar VM (2000) Mechanisms of the pro- and anti-oxidant actions of nitric oxide in atherosclerosis. Cardiovasc Res 47:465–474

    Article  PubMed  CAS  Google Scholar 

  85. Willmott N, Sethi JK, Walseth TF, Lee HC, White AM, Galione A (1996) Nitric oxide-induced mobilization of intracellular calcium via the cyclic ADP-ribose signaling pathway. J Biol Chem 271:3699–3705

    Article  PubMed  CAS  Google Scholar 

  86. Guidarelli A, Sciorati C, Clementi E, Cantoni O (2006) Peroxynitrite mobilizes calcium ions from ryanodine-sensitive stores, a process associated with the mitochondrial accumulation of the cation and the enforced formation of species mediating cleavage of genomic DNA. Free Radic Biol Med 41:154–164

    Article  PubMed  CAS  Google Scholar 

  87. Szabó C, Salzman AL (1996) Inhibition of terminal calcium overload protects against peroxynitrite-induced cellular injury in macrophages. Immunol Lett 51:163–167

    Article  PubMed  Google Scholar 

  88. Zaidi A, Michaelis ML (1999) Effects of reactive oxygen species on brain synaptic plasma membrane Ca2+-ATPase. Free Radic Biol Med 27:810–821

    Article  PubMed  CAS  Google Scholar 

  89. Bapat S, Verkleij A, Post JA (2001) Peroxynitrite activates mitogen-activates protein kinase (MAPK) via a MEK-independent pathway: role for protein kinase C. FEBS Lett 499:21–26

    Article  PubMed  CAS  Google Scholar 

  90. Gutiérrez-Martín Y, Martín-Romero FJ, Henao F, Gutiérrez-Merino C (2002) Synaptosomal plasma membrane Ca2+ pump activity inhibition by repetitive micromolar ONOO− pulses. Free Rad Biol Med 32:46–55

    Article  PubMed  Google Scholar 

  91. Pan BX, Zhao GL, Huang XL, Zhao KS (2004) Calcium mobilization is required for peroxynitrite-mediated enhancement of spontaneous transient outward currents in arteriolar smooth muscle cells. Free Radic Biol Med 37:823–838

    Article  PubMed  CAS  Google Scholar 

  92. Vicente S, Figueroa S, Pérez-Rodríguez R, González MP, Oset-Gasque MJ (2005) Nitric oxide donors induce calcium mobilisation from internal stores but do not stimulate catecholamine secretion by bovine chromaffin cells in resting conditions. Cell Calcium 37:163–172

    Article  PubMed  CAS  Google Scholar 

  93. Redondo PC, Jardín I, Hernández-Cruz JM, Pariente JA, Salido GM, Rosado JA (2005) Hydrogen peroxide and peroxynitrite enhance Ca2+ mobilization and aggregation in platelets from Type 2 diabetic patients. Biochim Biophys Res Commun 333:794–802

    Article  CAS  Google Scholar 

  94. Berkels R, Dachs C, Roesen R, Klaus W (2000) Simultaneous measurement of intracellular Ca2+ and nitric oxide: a new method. Cell Calcium 27:281–286

    Article  PubMed  CAS  Google Scholar 

  95. Hsu HC, Lee YT, Chen MF (2001) Effects of Fisch oil and vitamin E on the antioxidant defense system in diet-induced hypercholesterolemic rabbits. Prostaglandins Other Lipid Mediat 66:99–108

    Article  PubMed  CAS  Google Scholar 

  96. Dringen R (2000) Metabolism and functions of glutathione in brain. Progr Neurobiol 62:649–671

    Article  CAS  Google Scholar 

  97. Muralikrishna Adibhatla R, Hatcher JF (2006) Phospholipase A2, reactive oxygen species, and lipid peroxidation in cerebral ischemia. Free Radic Biol Med 40:376–387

    Article  PubMed  CAS  Google Scholar 

  98. White BC, Sullivan JM, DeGracia DJ, O´Neil BJ, Neumar RW, Grossman LI, Rafols JA, Krause GS (2000) Brain ischemia and reperfusion: molecular mechanisms of neuronal injury. J Neurol Sci 179:1–33

    Article  PubMed  CAS  Google Scholar 

  99. Jensen B, Farach-Carson MC, Kenaley E, Akanbi KA (2004) High extracellular calcium attenuates adipogenesis in 3T3-L1 preadipocytes. Exp Cell Res 301:280–292

    Article  PubMed  CAS  Google Scholar 

  100. Schwartz RS, Abraham S (1982) Effect of dietary polyunsaturated fatty acids on the activity and content of fatty acid synthetase in mouse liver. Biochim Biophys Acta 711:316–326

    PubMed  CAS  Google Scholar 

  101. Ereciñska M, Silver IA (2001) Tissue oxygen tension and brain sensitivity to hypoxia. Respir Physiol 128:263–276

    Article  PubMed  Google Scholar 

  102. Brookes PS, Land JM, Clark JB, Heales SJR (1998) Peroxynitrite and brain mitochondria: evidence for increased proton leak. J Neurochem 70:2195–2202

    Article  PubMed  CAS  Google Scholar 

  103. Vatassery GT, Santa Cruz KS, DeMaster EG, Quach HT, Smith WE (2004) Oxidative stress and inhibition of oxidative phosphorylation induced by peroxynitrite and nitrite in rat brain subcellular fractions. Neurochem Int 45:963–970

    Article  PubMed  CAS  Google Scholar 

  104. Infante JP, Huszagh VA, (2000) Secondary carnitine deficiency and impaired docosahexaenoic (22:6 n-3) acid synthesis: a common denominator in the pathophysiology of diseases of oxidative phosphorylation and β-oxidation. FEBS Lett 468:1–5

    Article  PubMed  CAS  Google Scholar 

  105. Infante JP (1999) A function for the vitamin E metabolite alpha-tocopherol quinone as an essential enzyme cofactor for the mitochondrial fatty acid desaturases. FEBS Lett 446:1–5

    Article  PubMed  CAS  Google Scholar 

  106. James MJ, Gibson RA, Cleland LG (2000) Dietary polyunsaturated fatty acids and inflammatory mediator production. Am J Clin Nutr 71:343S–348S

    PubMed  CAS  Google Scholar 

  107. Elabbadi N, Day CP, Gamouh A, Zyad A, Yeaman SJ (2005) Relationship between the inhibition of phosphatidic acid phosphohydrolase-1 by oleate and oleoyl-CoA ester and its apparent translocation. Biochimie 87:437–443

    Article  PubMed  CAS  Google Scholar 

  108. Van Hove C, Carreer-Bruhwyler F, Géczy J, Herman AG (2005) Long-term treatment with the NO-donor molsidomine reduces circulating ICAM-1 levels in patients with stable angina. Atherosclerosis 180:399–405

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was partially supported by grants from CONICET and CIC, República Argentina. The authors are grateful for the excellent technical assistance of Norma Cristalli and Elsa Claverie.

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  1. INIBIOLP (Instituto de Investigaciones Bioquímicas de La Plata), CONICET-UNLP. Cátedra de Bioquímica, Facultad de Ciencias Médicas, Universidad Nacional de La Plata, Calles 60 y 120 (1900), La Plata, Argentina

    Carlos A. Marra, Julio Nella, Damián Manti & María J. T. de Alaniz

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  1. Carlos A. Marra
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  2. Julio Nella
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  3. Damián Manti
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  4. María J. T. de Alaniz
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Correspondence to Carlos A. Marra.

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Julio Nella author in memoriam.

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Marra, C.A., Nella, J., Manti, D. et al. Lipid Metabolism in Rats is Modified by Nitric Oxide Availability Through a Ca++-Dependent Mechanism. Lipids 42, 211–228 (2007). https://doi.org/10.1007/s11745-006-3004-6

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