Effect of Remifentanil on Mitochondrial Oxygen Consumption of Cultured Human Hepatocytes

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Djafarzadeh, Siamak ^a   Vuda, Madhusudanarao ^a   Takala, Jukka ^a   Jakob, Stephan M ^a  

^a UNIVERSITY OF BERN   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CASPASE 3; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; NALOXONE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); REMIFENTANIL; TUMOR NECROSIS FACTOR ALPHA;

APOPTOSIS; ARTICLE; CELL ISOLATION; CELL PROTECTION; CONTROLLED STUDY; CYTOKINE RELEASE; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DRUG EFFECT; DRUG MECHANISM; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; HUMAN CELL; INCUBATION TIME; LIVER CELL CULTURE; LIVER MITOCHONDRION; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; OXIDATIVE PHOSPHORYLATION UNCOUPLING; OXYGEN CONSUMPTION; PROTEIN PHOSPHORYLATION; RESPIROMETRY; WESTERN BLOTTING;

ADENOSINE TRIPHOSPHATE; CASPASE 3; CELL RESPIRATION; ELECTRON TRANSPORT COMPLEX I; ELECTRON TRANSPORT COMPLEX II; ELECTRON TRANSPORT COMPLEX IV; HEP G2 CELLS; HEPATOCYTES; HUMANS; HYPNOTICS AND SEDATIVES; I-KAPPA B KINASE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; NALOXONE; NARCOTIC ANTAGONISTS; PHOSPHORYLATION; PIPERIDINES; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84866407407     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0045195     Document Type: Article

References (61)

1. Dombrovskiy VY, Martin AA, Sunderram J, Sunderram J, Paz HL, (2007) Rapid increase in hospitalization and mortality rates for severe sepsis in the United States: A trend analysis from 1993 to 2003. Crit Care Med 35: 1244-1250.
2. Weycker D, Akhras KS, Edelsberg J, Angus DC, Oster G, (2003) Long-term mortality and medical care charges in patients with severe sepsis. Crit Care Med 31: 2316-2323.
3. Abraham E, Singer M, (2007) Mechanisms of sepsis-induced organ dysfunction. Crit Care Med 35: 2408-2416.
4. Vincent JL, De Backer D, (2005) Microvascular dysfunction as a cause of organ dysfunction in severe sepsis. Crit Care 9Suppl 4: S9-12.
5. Russell JA, Singer J, Bernard GR, Wheeler A, Fulkerson W, et al. (2000) Changing pattern of organ dysfunction in early human sepsis is related to mortality. Crit Care Med 28: 3405-3411.
6. Vincent JL, Sakr Y, Sprung CL, Ranieri VM, Reinhart K, et al. (2006) Sepsis in European intensive care units: results of the SOAP study. Crit Care Med 34: 344-353.
7. Angus DC, Linde-Zwirble WT, Lidicker J, Clermont G, Carcillo J, et al. (2001) Epidemiology of severe sepsis in the United States: analysis of incidence, outcome, and associated costs of care. Crit Care Med 29: 1303-1310.
8. Aronsohn A, Jensen D, (2011) Hepatobiliary manifestations of critically ill and postoperative patients. Clin Liver Dis 15(1): 183-197.
9. Elbers PW, Ince C, (2006) Mechanisms of critical illness-classifying microcirculatory flow abnormalities in distributive shock. Crit Care 10: 221.
10. Abraham E, (2003) Neutrophils and acute lung injury. Crit Care Med 31: S195-199.
11. Brealey D, Brand M, Hargreaves I, Heales S, Land J, et al. (2002) Association between mitochondrial dysfunction and severity and outcome of septic shock. Lancet 360: 219-223.
12. Dahm CC, Moore K, Murphy MP, (2006) Persistent S-nitrosation of complex I and other mitochondrial membrane proteins by S-nitrosothiols but not nitric oxide or peroxynitrite: implications for the interaction of nitric oxide with mitochondria. J Biol Chem 281: 10056-10065.
13. Frost MT, Wang Q, Moncada S, Singer M, (2005) Hypoxia accelerates nitric oxide-dependent inhibition of mitochondrial complex I in activated macrophages. Am J Physiol Regul Integr Comp Physiol 288: R394-400.
14. Brealey D, Karyampudi S, Jacques TS, Novelli M, Stidwill R, et al. (2004) Mitochondrial dysfunction in a long-term rodent model of sepsis and organ failure. Am J Physiol Regul Integr Comp Physiol 286: R491-497.
15. Larche J, Lancel S, Hassoun SM, Favory R, Decoster B, et al. (2006) Inhibition of mitochondrial permeability transition prevents sepsis-induced myocardial dysfunction and mortality. J Am Coll Cardiol 48: 377-385.
16. Crouser ED, Julian MW, Huff JE, Joshi MS, Bauer JA, et al. (2004) Abnormal permeability of inner and outer mitochondrial membranes contributes independently to mitochondrial dysfunction in the liver during acute endotoxemia. Crit Care Med 32: 478-388.
17. Muravchick S, Levy RJ, (2006) Clinical implications of mitochondrial dysfunction. Anesthesiology 105: 819-837.
18. Marian M, Parrino C, Leo AM, Vincenti E, Bindoli A, et al. (1997) Effect of the intravenous anesthetic 2,6-diisopropylphenol on respiration and energy production by rat brain synaptosomes. Neurochem Res 22: 287-292.
19. Schenkman KA, Yan S, (2000) Propofol impairment of mitochondrial respiration in isolated perfused guinea pig hearts determined by reflectance spectroscopy. Crit Care Med 28: 172-177.
20. Hanley PJ, Ray J, Brandt U, Daut J, (2002) Halothane, isoflurane and sevoflurane inhibit NADH:ubiquinone oxidoreductase (complex I) of cardiac mitochondria. J Physiol 544: 687-693.
21. Novaes MA, Knobel E, Bork AM, Pavao OF, Noqueira-Martins LA, et al. (1999) Stressors in ICU. Perception of the patient, relatives and healthcare team. Intensive Care Med 25: 1421-1426.
22. Glass PS, Hardman D, Kamiyama Y, Quill TJ, Marton G, et al. (1993) Preliminary pharmacokinetics and pharmacodynamics of an ultra-short-acting opioid-remifentanil (G187084B). Anesth Analg 77: 1031-1040.
23. Hoke JF, Cunningham F, James MK, Muir KT, Hoffman WE, (1997) Comparative pharmacokinetics and pharmacodynamics of remifentanil, its principle metabolite (GR90291) and alfentanil in dogs. J Pharmacol Exp Ther 281: 226-232.
24. Duthe DJR, (1998) Remifentanil and tramadol. Br J Anaesth 81: 51-57.
25. Knowles BB, Howe CC, Aden DP, (1980) Human hepatocellular carcinoma cell lines secrete the major plasma proteins and hepatitis B surface antigen. Science 209: 497-499.
26. Cai SY, He H, Nguyen T, Mennone A, Boyer JL, (2010) Retinoic acid represses CYP7A1 expression in human hepatocytes and HepG2 cells by FXR/RXR-dependent and independent mechanisms. J Lipid Res 51: 2265-2274.
27. Liguori MJ, Blomme EA, Waring JF, (2008) Trovafloxacin-induced gene expression changes in liver-derived in vitro systems: comparison of primary human hepatocytes to HepG2 cells. Drug Metab Dispos 36: 223-233.
28. Westerink WM, Schoonen WG, (2007) Phase II enzyme levels in HepG2 cells and cryopreserved primary human hepatocytes and their induction in HepG2 cells. Toxicol In Vitro 21: 1592-1602.
29. Said HM, Nabokina SM, Balamurugan K, Mohammed ZM, Urbina C, et al. (2007) Mechanism of nicotinic acid transport in human liver cells: experiments with HepG2 cells and primary hepatocytes. Am J Physiol Cell Physiol 293: C1773-1778.
30. Gabay C, Porter B, Guenette D, Billir B, Arend WP, (1999) Interleukin-4 (IL-4) and IL-13 enhance the effect of IL-1beta on production of IL-1 receptor antagonist by human primary hepatocytes and hepatoma HepG2 cells: differential effect on C-reactive protein production. Blood 93: 1299-1307.
31. Regueira T, Lepper PM, Brandt S, Ochs M, Vuda M, et al. (2009) Hypoxia inducible factor-1 alpha induction by tumour necrosis factor-alpha, but not by toll-like receptor agonists, modulates cellular respiration in cultured human hepatocytes. Liver Int 29: 1582-1592.
32. Michelsen LG, Holford NHG, Lu W, Hoke JF, Hug CC, et al. (2001) The pharmacokinetics of remifentanil in patients undergoing coronary artery bypass grafting with cardiopulmonary bypass. Anesth Analg 93: 1100-1105.
33. Brown GC, Lakin-Thomas PL, Brand MD, (1990) Control of respiration and oxidative phosphorylation in isolated rat liver cells. Eur J Biochem 192: 355-362.
34. Das M, Parker JE, Halestrap AP, (2003) Matrix volume measurements challenge the existence of diazoxide/glibencamide-sensitive KATP channels in rat mitochondria. J Physiol 547(3): 893-902.
35. Debska G, Kicinska A, Skalska J, Szewczyk A, May R, et al. (2002) Opening of potassium channels modulates mitochondrial function in rat skeletal muscle. Biochim Biophys Acta 1556(2-3): 97-105.
36. O′Rourke B, (2000) Myocardial K(ATP) channels in preconditioning. Circ Res 87(10): 845-855.
37. Grover GJ, Garlid KD, (2000) ATP-Sensitive potassium channels: a review of their cardioprotective pharmacology. Mol Cell Cardiol 32(4): 677-695.
38. Liu Y, Sato T, O'Rourke B, Marban E, (1998) Mitochondrial ATP-dependent potassium channels: novel effectors of cardioprotection? Circulation 97: 2463-2469.
39. Kowaltowski AJ, Seetharaman S, Paucek P, Garlid KD, (2001) Bioenergetic consequences of opening the ATP-sensitive K+ channel of heart mitochondria. Am J Physiol Heart Circ Physiol 280: H649-657.
40. Holmuhamedov EL, Jovanovic S, Dzeja PP, Jovanovic A, Terzic A, (1998) Mitochondrial ATP-sensitive K+ channels modulate cardiac mitochondrial function. Am J Physiol Heart Circ Physiol 275: H1567-1576.
41. Chakass D, Philippe D, Erdual E, Dharancy S, Malapel M, et al. (2007) micro-Opioid receptor activation prevents acute hepatic inflammation and cell death. Gut 56: 974-981.
42. Hou YN, Vlaskovska M, Cebers G, Kasakov L, Liljequist S, et al. (1996) A mu-receptor opioid agonist induces AP-1 and NF-kappa B transcription factor activity in primary cultures of rat cortical neurons. Neuroscience Letters 212: 159-162.
43. Stevanato R, Morno F, Marian M, Rigobello MP, Bindoli A, et al. (2002) Effects of nitrosopropofol on mitochondrial energy-converting system. Biochem Pharmacol 64: 1133-1138.
44. Vilela SM, Santos DJ, Félix L, Almeida JM, Antunes L, et al. (2009) Are fentanyl and remifentanil safe opioids for rat brain mitochondrial bioenergetics? Mitochondrion 9: 247-253.
45. Scandurra FM, Gnaiger E, (2010) Cell respiration under hypoxia: facts and artefacts in mitochondrial oxygen kinetics. Adv Exp Med Biol 662: 7-25.
46. Mousa SA, Zhang Q, Sitte N, Ji R, Stein C, (2001) beta-Endorphin-containing memory-cells and mu-opioid receptors undergo transport to peripheral inflamed tissue. J Neuroimmunol 115: 71-78.
47. Stein C, Millan MJ, Shippenberg TS, Herz A, (1988) Peripheral effect of fentanyl upon nociception in inflamed tissue of the rat. Neurosci Lett 84: 225-228.
48. Bencsics A, Elenkov IJ, Vizi ES, (1997) Effect of morphine on lipopolysaccharide-induced tumor necrosis factor-alpha production in vivo: involvement of the sympathetic nervous system. J Neuroimmunol 73: 1-6.
49. Xi J, Tian W, Zhang L, Jin Y, Xu Z, (2010) Morphine prevents the mitochondrial permeability transition pore opening through NO/cGMP/PKG/Zn2+/GSK-3beta signal pathway in cardiomyocytes. Am J Physiol Heart Circ Physiol 298(2): H601-607.
50. Graeve L, Baumann M, Heinrich PC, (1993) Interleukin-6 in autoimmune disease. Role of IL-6 in physiology and pathology of the immune defense. Clin Investig 71: 664-671.
51. Hack CE, De Groot ER, Felt-Bersma RJ, Nuijens JH, Strack Van Schijndel RJ, et al. (1989) Increased plasma levels of interleukin-6 in sepsis. Blood 74: 1704-1710.
52. Waage A, Brandtzaeg P, Halstensen A, Kierulf P, Espevik T, (1989) The complex pattern of cytokines in serum from patients with meningococcal septic shock: association between interleukin 6, interleukin 1, and fatal outcome. J Exp Med 169: 333-338.
53. Shalaby MR, Waage A, Aarden L, Espevik T, (1989) Endotoxin, tumor necrosis factor-α and interleukin 1 induce interleukin 6 production in vivo. Clin Immunol Immunopathol 53(3): 488-498.
54. Sheron N, Lau JN, Hofmann J, Williams R, Alexander GJ, (1990) Dose-dependent increase in plasma interleukin-6 after recombinant tumour necrosis factor infusion in humans. Clin Exp Immunol 82(3): 427-428.
55. Wu Y, Wang Y, Zhan J, (2009) Effects of remifentanil and fentanyl on LPS-induced cytokine release in human whole blood in vitro. Mol Biol Rep 36(5): 1113-1117.
56. Pinti M, Troiano L, Nasi M, Ferraresi R, Dobrucki J, et al. (2003) Hepatoma HepG2 cells as a model for in vitro studies on mitochondrial toxicity of antiviral drugs: which correlation with the patient? J Biol Regul Homeost Agents 17: 166-171.
57. Grant MH, Duthie SJ, Gray AG, Burke MD, (1988) Mixed function oxidase and UDP-glucuronyltransferase activities in the human Hep G2 hepatoma cell line. Biochem Pharmacol 37: 4111-4116.
58. Dungel P, Haindl S, Behling T, Mayer B, Redl H, et al. (2011) Neither nitrite nor nitric oxide mediate toxic effects of nitroglycerin on mitochondria. J Biochem Mol Toxicol 25(5): 297-302.
59. Braun B, Eze P, Stephens BR, Hagobian TA, Sharoff CG, et al. (2008) Impact of metformin on peak aerobic capacity. Appl Physiol Nutr Metab 33(1): 61-67.
60. Porta F, Bracht H, Weikert C, Beck M, Takala J, et al. (2009) Effects of endotoxin and catecholamines on hepatic mitochondrial respiration. Inflammation 32(5): 315-321.
61. Gnaiger E, Rieger G, Kuznetsov A, Fuchs A, Stadlmann S, et al. (1997) Mitochondrial ischemia-reoxygenation injury and plasma membrane integrity in human endothelial cells. Transplant Proc 29: 3524-3526.