The effect of iNOS deletion on hepatic gluconeogenesis in hyperdynamic murine septic shock

Intensive Care Medicine

Volumn 33, Issue 6, 2007, Pages 1094-1101

  Albuszies, Gerd ^a   Vogt, Josef ^a   Wachter, Ulrich ^a   Thiemermann, Christoph ^b   Leverve, Xavier M ^c   Weber, Sandra ^a   Georgieff, Michael ^a   Radermacher, Peter ^a   Barth, Eberhard ^a  

^a UNIVERSITY HOSPITAL ULM   (Germany)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^c UNIV GRENOBLE ALPES   (France)

Author keywords

Glucose 6 phosphatase; Laser Doppler flowmetry; Phosphoenolpyruvate carboxykinase; Remission spectrophotometry; Stable isotope; Tracer dilution modeling

Indexed keywords

CARBON 13; GLUCOSE; HEMOGLOBIN; HETASTARCH; INDUCIBLE NITRIC OXIDE SYNTHASE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE INHIBITOR; NORADRENALIN; OXYGEN; PHOSPHOENOLPYRUVATE CARBOXYKINASE (GTP); S [2 (1 IMINOETHYLAMINO)ETHYL]HOMOCYSTEINE;

ANESTHESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ARTIFICIAL VENTILATION; C57BL 6 MOUSE; CAPILLARY; CECUM; CONTINUOUS INFUSION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME REGULATION; GAS CHROMATOGRAPHY; GENE DELETION; GLUCONEOGENESIS; HEMODYNAMICS; ISOTOPE ANALYSIS; KNOCKOUT MOUSE; LASER DOPPLER FLOWMETRY; LIGATION; LIVER CIRCULATION; LIVER METABOLISM; LIVER PERFUSION; MALE; MASS SPECTROMETRY; MICROCIRCULATION; MOUSE; NONHUMAN; OXYGEN SATURATION; PROSPECTIVE STUDY; PROTEIN FUNCTION; PUNCTURE; RANDOMIZATION; RESUSCITATION; SEPTIC SHOCK; SPECTROPHOTOMETRY; WILD TYPE;

EID: 34249696885     PISSN: 03424642     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00134-007-0638-7     Document Type: Article

References (64)

1. L'Her E, Sebert P (2001) A global approach to energy metabolism in an experimental model of sepsis. Am J Respir Crit Care Med 164:1444-1447
2. Tu W, Satoi S, Zhang Z, Kitade H, Okumura T, Kwon AH, Kamiyama Y (2003) Hepatocellular dysfunction induced by nitric oxide production in hepatocytes isolated from rats with sepsis. Shock 19:373-377
3. Brealey D, Karyampudi S, Jacques TS, Novelli M, Stidwill R, Taylor V, Smolenski RT, Singer M (2004) Mitochondrial dysfunction in a long-term rodent model of sepsis and organ failure. Am J Physiol Regul Integr Comp Physiol 286:R491-R497
4. Porta F, Takala J, Weikert C, Bracht H, Kolarova A, Lauterburg BH, Borotto E, Jakob SM (2006) Effects of prolonged endotoxemia on liver, skeletal muscle and kidney mitochondrial function. Crit Care 10:R118
5. King CJ, Tytgat S, Delude RL, Fink MP (1999) Ileal mucosal oxygen consumption is decreased in endotoxemic rats but is restored toward normal by treatment with aminoguanidine. Crit Care Med 27:2518-2524
6. Brealey D, Brand M, Hargreaves I, Heales S, Land J, Smolenski R, Davies NA, Cooper CE, Singer M (2002) Association between mitochondrial dysfunction and severity and outcome of septic shock. Lancet 360:219-223
7. Boulos M, Astiz ME, Barua RS, Osman M (2003) Impaired mitochondrial function induced by serum from septic shock patients is attenuated by inhibition of nitric oxide synthase and poly(ADP-ribose) synthase. Crit Care Med 31:353-358
8. Albuszies G, Radermacher P, Vogt J, Wachter U, Weber S, Schoaff M, Georgieff M, Barth E (2005) Effect of increased cardiac output on hepatic and intestinal microcirculatory blood flow, oxygenation, and metabolism in hyperdynamic murine septic shock. Crit Care Med 33:2332-2338
9. Horton RA, Ceppi ED, Knowles RG, Titheradge MA (1994) Inhibition of hepatic gluconeogenesis by nitric oxide: a comparison with endotoxic shock. Biochem J 299:735-739
10. Stadler J, Barton D, Beil-Moeller H, Diekmann S, Hierholzer C, Erhard W, Heidecke CD (1995) Hepatocyte nitric oxide biosynthesis inhibits glucose output and competes with urea synthesis for L-arginine. Am J Physiol 268:G183-G188
11. Sprangers F, Sauerwein HP, Romijn JA, van Woerkom GM, Meijer AJ (1998) Nitric oxide inhibits glycogen synthesis in isolated rat hepatocytes. Biochem J 330:1045-1049
12. Andrejko KM, Deutschman CS (1997) Altered hepatic gene expression in fecal peritonitis: changes in transcription of gluconeogenic, beta-oxidative, and ureagenic genes. Shock 7:164-169
13. Deutschman CS, Andrejko KM, Haber BA, Bellin L, Elenko E, Harrison R, Taub R (1997) Sepsis-induced depression of rat glucose-6-phosphatase gene expression and activity. Am J Physiol 273:R1709-R1718
14. Ceppi ED, Smith FS, Titheradge MA (1996) Effect of multiple cytokines plus bacterial endotoxin on glucose and nitric oxide production by cultured hepatocytes. Biochem J 317:503-507
15. Ou J, Molina L, Kim YM, Billiar TR (1996) Excessive NO production dose not account for the inhibition of hepatic gluconeogenesis in endotoxemia. Am J Physiol 271:G621-G628
16. Villa P, Demitri MT, Meazza C, Sironi M, Gnocchi P, Ghezzi P (1996) Effects of methyl palmitate on cytokine release, liver injury and survival in mice with sepsis. Eur Cytokine Netw 7:765-769
17. 2 exchange and energy balance. Am J Respir Crit Care Med 159:1758-1765
18. 2-exchange and energy metabolism during hyperdynamic porcine endotoxemia. Shock 16:203-210
19. Moeniralam HS, Sprangers F, Endert E, Ackermans MT, Van Lanschot JJ, Sauerwein HP, Romijn JA (2001) Role of nitric oxide in the regulation of glucose kinetics in response to endotoxin in dogs. J Appl Physiol 91:130-136
20. Strunk V, Hahnenkamp K, Schneuing M, Fischer LG, Rich GF (2001) Selective iNOS inhibition prevents hypotension in septic rats while preserving endothelium-dependent vasodilation. Anesth Analg 92:681-687
21. Barth E, Radermacher P, Thiemermann C, Weber S, Georgieff M, Albuszies G (2006) Role of inducible nitric oxide synthase in the reduced responsiveness of the myocardium to catecholamines in a hyperdynamic, murine model of septic shock. Crit Care Med 34:307-313
22. Alderton WK, Angell ADR, Craig C, Dawson J, Garvey EP, Moncada S, Monkhouse J, Rees D, Russell LJ, Schwartz S, Waslidge N, Knowles RG (2005) GW274150 and GW273629 are potent and highly selective inhibitors of inducible nitric oxide (iNOS) in vitro and in vivo. Br J Pharmacol 145:310-312
23. Cobelli C, Toffolo G, Ferrannini E (1984) A model of glucose kinetics and their control by insulin, compartmental and noncompartmental approaches. Math Biosci 72:291-316
24. Bier DM, Leake RD, Haymond MW, Arnold KJ, Gruenke LD, Sperling MA, Kipnis DM (1977) Measurement of "true" glucose production rates in infancy and childhood with 6,6-dideuteroglucose. Diabetes 26:1016-1023
25. Goswami C, Datta S, Biswas K, Saha N (2004) Cell volume changes affect gluconeogenesis in the perfused liver of the catfish Clarias batrachus. J Biosci 29:337-347
26. Hansen RJ, Hinze H, Holzer H (1976) Assay of phosphoenolpyruvate carboxykinase in crude yeast extracts. Anal Biochem 74:576-584
27. Nüssler AK, Brückner UB, Vogt J, Radermacher P (2002) Measuring end products of nitric oxide in vivo. Methods Enzymol 359:75-83
28. Connolly CC, Steiner KE, Stevenson RW, Neal DW, Williams PE, Alberti KG, Cherrington AD (1991) Regulation of glucose metabolism by norepinephrine in conscious dogs. Am J Physiol 261:E764-E772
29. Chu CA, Galassetti P, Igawa K, Sindelar DK, Neal DW, Burish M, Cherrington AD (2003) Interaction of free fatty acids and epinephrine in regulating hepatic glucose production in conscious dogs. Am J Physiol Endocrinol Metab 284:E291-E301
30. Bearn AG, Billing B, Sherlock S (1951) The effect of adrenaline and noradrenaline on hepatic blood flow and splanchnic carbohydrate metabolism in man. J Physiol 115:430-441
31. Ensinger H, Geisser W, Brinkmann A, Wachter U, Vogt J, Radermacher P, Georgieff M, Träger K (2002) Metabolic effects of norepinephrine and dobutamine in healthy volunteers. Shock 18:495-500
32. Wang P, Tait SM, Chaudry IH (2000) Sustained elevation of norepinephrine depresses hepatocellular function. Biochim Biophys Acta 1535:36-44
33. Yang S, Koo DJ, Zhou M, Chaudry IH, Wang P (2000) Gut-derived norepinephrine plays a critical role in producing hepatocellular dysfunction during early sepsis. Am J Physiol Gastrointest Liver Physiol 279:G1274-G1281
34. Yang S, Zhou M, Chaudry IH, Wang P (2001) Norepinephrine-induced hepatocellular dysfunction in early sepsis is mediated by activation of alpha2-adrenoceptors. Am J Physiol Gastrointest Liver Physiol 281:G1014-G1021
35. Gumucio JJ (1989) Hepatocyte heterogeneity: the coming of age from the description of a biological curiosity to a partial understanding of its physiological meaning and regulation. Hepatology 9:154-160
36. Dahn MS, Mitchell RA, Lange MP, Smith S, Jacobs LA (1995) Hepatic metabolic response to injury and sepsis. Surgery 117:520-530
37. Reinelt H, Radermacher P, Kiefer P, Fischer G, Wachter U, Vogt J, Georgieff M (1999) Impact of exogenous beta-adrenergic receptor stimulation on hepatosplanchnic oxygen kinetics and metabolic activity in septic shock. Crit Care Med 27:325-331
38. Wilmore DW (1977) Impaired gluconeogenesis in extensively injured patients with gram-negative bacteremia. Am J Clin Nutr 30:1355-1356
39. Wilmore DW, Goodwin CW, Aulick LH, Powanda MC, Mason AD Jr, Pruitt BA Jr (1980) Effect of injury and infection on visceral metabolism and circulation. Ann Surg 192:491-504
40. Maitra SR, Homan CS, Beuhler MC, Thode HC Jr, Henry M (1999) Alterations in hepatic gluconeogenesis, prostanoid, and intracellular calcium during sepsis. Acad Emerg Med 6:588-595
41. Matejovic M, Krouzecky A, Martinkova V, Rokyta R, Kralova H, Treska V, Radermacher P, Novak I (2004) Selective inducible nitric oxide synthase inhibition during long-term hyperdynamic porcine bacteremia. Shock 21:458-465
42. 2 balance during endotoxemia in pigs. Intensive Care Med 31:985-992
43. Pullamsetti SS, Maring D, Ghofrani HA, Mayer K, Weissmann N, Rosengarten B, Lehner M, Schudt C, Boer R, Grimminger F, Seeger W, Schermuly RT (2006) Effect of nitric oxide synthase (NOS) inhibition on macro- and microcirculation in a model of rat endotoxic shock. Thromb Haemost 95:720-727
44. Ince C, Sinaasappel M (1999) Microcirculatory oxygenation and shunting in sepsis and shock. Crit Care Med 27:1369-1377
45. Ceppi ED, Titheradge MA (1998) The importance of nitric oxide in the cytokine-induced inhibition of glucose formation by cultured hepatocytes incubated with insulin, dexamethasone, and glucagon. Arch Biochem Biophys 349:167-174
46. Rognstad R (1979) Rate-limiting steps in metabolic pathways. J Biol Chem 254:1875-1878
47. Ochs RS, Lardy HA (1983) Catecholamine stimulation of hepatic gluconeogenesis at the site between pyruvate and phosphoenolpyruvate. J Biol Chem 258:9956-9962
48. Horton RA, Knowles RG, Titheradge MA (1994) Endotoxin causes reciprocal changes in hepatic nitric oxide synthesis, gluconeogenesis, and flux through phosphoenolpyruvate carboxykinase. Biochem Biophys Res Commun 204:659-665
49. Pilkis SJ, Granner DK (1992) Molecular physiology of the regulation of hepatic gluconeogenesis and glycolysis. Annu Rev Physiol 54:885-909
50. Pison CM, Chauvin C, Fontaine E, Catelloni F, Keriel C, Paramelle B, Leverve XM (1995) Mechanism of gluconeogenesis inhibition in rat hepatocytes isolated after in vivo hypoxia. Am J Physiol 268:E965-E973
51. Deutschman CS, De Maio A, Buchman TG, Clemens MG (1993) Sepsis-induced alterations in phosphoenolpyruvate carboxykinase expression: the role of insulin and glucagon. Circ Shock 40:295-302
52. Chang CK, Moskal SF, Srivenugopal KS, Schumer W (1993) Altered levels of mRNA encoding enzymes of hepatic glucose metabolism in septic rats. Circ Shock 41:35-39
53. Yamauchi K, Nakajima K, Ikeo S, Nishimura Y, Komatsu M, Aizawa T, Hashizume K (2001) Effects of nipradilol, a nitric oxide-releasing beta-adrenoceptor blocking agent, on phosphoenolpyruvate carboxykinase gene transcription in a rat hepatoma cell line. Jpn J Pharmacol 87:83-85
54. Hellerstein MK (2004) New stable isotope-mass spectrometric techniques for measuring fluxes through intact metabolic pathways in mammalian systems: introduction of moving pictures into functional genomics and biochemical phenotyping. Metab Eng 6:85-100
55. van Dijk TH, Boer TS, Havinga R, Stellaard F, Kuipers F, Reijngoud DJ (2003) Quantification of hepatic carbohydrate metabolism in conscious mice using serial blood and urine spots. Anal Biochem 322:1-13
56. 13C-labeled lactate. J Biol Chem 268:25509-25521
57. 13C]glucose in rats. J Biol Chem 264:12994-13004
58. Van den Berghe G (2004) How does blood glucose control with insulin save lives in intensive care? J Clin Invest 114:1187-1195
59. Chauhan SD, Seggara G, Vo PA, MacAllister RJ, Hobbs AJ, Ahluwalia A (2003) Protection against lipolysaccharide-induced endothelial dysfunction in resistance and conduit vasculature of iNOS knockout mice. FASEB J 17:773-775
60. Connelly L, Madhani M, Hobbs AJ (2005) Resistance to endotoxic shock in endothelial nitric-oxide synthase (eNOS) knockout mice. J Biol Chem 280:10040-10046
61. Liaudet L, Mabley JG, Soriano FG, Pacher P, Marton A, Haskó G, Szabó C (2001) Inosine reduces systemic inflammation and improves survivla in septic shock induced by cecal ligation and puncture. Am J Respir Crit Care Med 164:1213-1220
62. Soriano FG, Liaudet L, Szabó E, Virág L, Mabley JG, Pacher P, Szabó C (2002) Resistance to acute septic peritonitis in poly(ADp-ribose) polymerase-1 deficient mice. Shock 17:286-292
63. Wu F, Wilson JX, Tyml K (2003) Ascorbate inhibits iNOS expression and preserves vasoconstrictor responsiveness in skeletal muscle of septic mice. Am J Physiol Regul Integrative Comp Physiol 285:50-56
64. Alves-Filho JC, de Freitas A, Russo M, Cunha F (2006) Toll-like receptor 4 signaling leads to neutrophil migration impairment in polymicrobial sepsis. Crit Care Med 34:461-470