Reperfusion does not induce oxidative stress but sustained endoplasmic reticulum stress in livers of rats subjected to traumatic-hemorrhagic shock

Shock

Volumn 33, Issue 3, 2010, Pages 289-298

  Duvigneau, Johanna Catharina ^a   Kozlov, Andrey V ^b   Zifko, Clara ^b   Postl, Astrid ^b   Hartl, Romana T ^a   Miller, Ingrid ^a   Gille, Lars ^a   Staniek, Katrin ^a   Moldzio, Rudolf ^a   Gregor, Wolfgang ^a   Haindl, Susanne ^b   Behling, Tricia ^b   Redl, Heinz ^b   Bahrami, Soheyl ^b  

^a UNIVERSITY OF VETERINARY MEDICINE   (Austria)

^b LUDWIG BOLTZMANN INSTITUTE FOR EXPERIMENTAL AND CLINICAL TRAUMATOLOGY   (Austria)

Author keywords

Antioxidants; Apoptosis; GRP78; Mitochondrial function; RONS; XBP 1

Indexed keywords

3 NITROTYROSINE; ALANINE AMINOTRANSFERASE; ALPHA TOCOPHEROL; ALPHA TOCOPHERYLQUINONE; ANTIOXIDANT; CYCLOPHILIN A; CYTOCHROME P450 1A1; GLUCOSE REGULATED PROTEIN 78; MESSENGER RNA; PROTEIN BAX; PROTEIN BCL XL; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE; X BOX BINDING PROTEIN 1;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CELL FRACTIONATION; CONTROLLED STUDY; ELECTRON SPIN RESONANCE; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION; HEMORRHAGIC SHOCK; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HISTOLOGY; LIPID PEROXIDATION; LIVER; LIVER CELL; LIVER FUNCTION; LIVER MITOCHONDRION; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; RAT; REPERFUSION INJURY; WESTERN BLOTTING;

ACUTE LUNG INJURY; ANIMALS; APOPTOSIS; DNA-BINDING PROTEINS; ENDOPLASMIC RETICULUM; HEAT-SHOCK PROTEINS; MALE; MITOCHONDRIA, LIVER; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE NITROGEN SPECIES; REPERFUSION; RESUSCITATION; SHOCK, HEMORRHAGIC; SHOCK, TRAUMATIC; TRANSCRIPTION FACTORS;

EID: 77149150929     PISSN: 10732322     EISSN: None     Source Type: Journal    
DOI: 10.1097/SHK.0b013e3181aef322     Document Type: Article

References (56)

1. Piskernik C, Haindl S, Behling T, Gerald Z, Kehrer I, Redl H, Kozlov AV: Antimycin A and lipopolysaccharide cause the leakage of superoxide radicals from rat liver mitochondria. Biochim Biophys Acta 1782:280-285, 2008.
2. Hsu YC, Chou TY, Chen CF, Wang D, Su CL, Hu RT: Rat liver ischemia/ reperfusion induced proinflammatory mediator and antioxidant expressions analyzed by gene chips and real-time polymerase chain reactions. Transplant Proc 40:2156-2158, 2008.
3. Miller I, Gemeiner M, Gesslbauer B, Kungl A, Piskernik C, Haindl S, Nurnberger S, Bahrami S, Redl H, Kozlov AV: Proteome analysis of rat liver mitochondria reveals a possible compensatory response to endotoxic shock. FEBS Lett 580:1257-1262, 2006.
4. Mela L: Altered mitochondrial metabolism in circulatory shock. Adv Exp Med Biol 78:371-373, 1977.
5. Sharma P, Walsh KT, Kerr-Knott KA, Karaian JE, Mongan PD: Pyruvate modulates hepatic mitochondrial functions and reduces apoptosis indicators during hemorrhagic shock in rats. Anesthesiology 103:65-73, 2005.
6. Brown GC: Nitric oxide and mitochondria. Front Biosci 12:1024-1033, 2007.
7. Bayir H, Kagan VE: Bench-to-bedside review: mitochondrial injury, oxidative stress and apoptosisVthere is nothing more practical than a good theory. Crit Care 12:206, 2008.
8. Hubbard WJ, Bland KI, Chaudry IH: The role of the mitochondrion in trauma and shock. Shock 22:395-402, 2004.
9. Harbrecht BG, Frye RF, Zenati MS, Branch RA, Peitzman AB: Cytochrome P-450 activity is differentially altered in severely injured patients. Crit Care Med 33:541-546, 2005.
10. Kozlov AV, Gille L, Miller I, Piskernik C, Haindl S, Staniek K, Nohl H, Bahrami S, Ohlinger W, Gemeiner M, et al.: Opposite effects of endotoxin on mitochondrial and endoplasmic reticulum functions. Biochem Biophys Res Commun 352:91-96, 2007.
11. van der Vlies D, Makkinje M, Jansens A, Braakman I, Verkleij AJ, Wirtz KW, Post JA: Oxidation of ER resident proteins upon oxidative stress: effects of altering cellular redox/antioxidant status and implications for protein maturation. Antioxid Redox Signal 5:381-387, 2003.
12. Zhang K, Kaufman RJ: The unfolded protein response: a stress signaling pathway critical for health and disease. Neurology 66:S102-S109, 2006.
13. Kaufman RJ: Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev 13:1211-1233, 1999.
14. 2+ homeostasis and apoptosis. EMBO J 23:1207-1216, 2004.
15. Hetz CA: ER stress signaling and the BCL-2 family of proteins: from adaptation to irreversible cellular damage. Antioxid Redox Signal 9:2345-2355, 2007.
16. 2+: a control point for apoptosis. Science 300:135-139, 2003.
17. Emadali A, Nguyen DT, Rochon C, Tzimas GN, Metrakos PP, Chevet E: Distinct endoplasmic reticulum stress responses are triggered during human liver transplantation. J Pathol 207:111-118, 2005.
18. Jian B, Hsieh CH, Chen J, Choudhry M, Bland K, Chaudry I, Raju R: Activation of endoplasmic reticulum stress response following trauma-hemorrhage. Biochim Biophys Acta 1782:621-626, 2008.
19. Bahrami S, Zimmermann K, Szelenyi Z, Hamar J, Scheiflinger F, Redl H, Junger WG: Small-volume fluid resuscitation with hypertonic saline prevents inflammation but not mortality in a rat model of hemorrhagic shock. Shock 25:283-289, 2006.
20. Kozlov AV, Szalay L, Umar F, Fink B, Kropik K, Nohl H, Redl H, Bahrami S: EPR analysis reveals three tissues responding to endotoxin by increased formation of reactive oxygen and nitrogen species. Free Radic Biol Med 34:1555-1562, 2003.
21. Tang PH, Miles MV, Miles L, Quinlan J, Wong B, Wenisch A, Bove K: Measurement of reduced and oxidized coenzyme Q9 and coenzyme Q10 levels in mouse tissues by HPLC with coulometric detection. Clin Chim Acta 341:173-184, 2004.
22. Leclercq I, Desager JP, Vandenplas C, Horsmans Y: Fast determination of low-level cytochrome P-450 1A1 activity by high-performance liquid chro-matography with fluorescence or visible absorbance detection. J Chromatogr B Biomed Appl 681:227-232, 1996.
23. Yagi K: Simple assay for the level of total lipid peroxides in serum or plasma. Methods Mol Biol 108:101-106, 1998.
24. Fitzal F, Redl H, Strohmaier W, Werner ER, Bahrami S: A 4-amino analogue of tetrahydrobiopterin attenuates endotoxin-induced hemodynamic alterations and organ injury in rats. Shock 18:158-162, 2002.
25. Kobelt F, Schreck U, Henrich HA: Involvement of liver in the decompensation of hemorrhagic shock. Shock 2:281-288, 1994.
26. Yokouchi M, Hiramatsu N, Hayakawa K, Okamura M, Du S, Kasai A, Takano Y, Shitamura A, Shimada T, Yao J, et al.: Involvement of selective reactive oxygen species upstream of proapoptotic branches of unfolded protein response. J Biol Chem 283:4252-4260, 2008.
27. Staniek K, Rosenau T, Gregor W, Nohl H, Gille L: The protection of bio-energetic functions in mitochondria by new synthetic chromanols. Biochem Pharmacol 70:1361-1370, 2005.
28. Nagel E, Meyer zu Vilsendorf A, Bartels M, Pichlmayr R: Antioxidative vitamins in prevention of ischemia/reperfusion injury. Int J Vitam Nutr Res 67:298-306, 1997.
29. Glantzounis GK, Salacinski HJ, Yang W, Davidson BR, Seifalian AM: The contemporary role of antioxidant therapy in attenuating liver ischemia-reperfusion injury: a review. Liver Transplant 11:1031-1047, 2005.
30. Ozaki M, Fuchinoue S, Teraoka S, Ota K: Mobilization of low-molecular-weight iron and peroxidative damage during ischemia and reoxygenation of the rat liver. Transplant Proc 26:918-921, 1994.
31. Kan WH, Hsu JT, Schwacha MG, Choudhry MA, Raju R, Bland KI, Chaudry IH: Selective inhibition of iNOS attenuates trauma-hemorrhage/ resuscitation-induced hepatic injury. J Appl Physiol 105:1076-1082, 2008.
32. Abdelrahman M, Mazzon E, Bauer M, Bauer I, Delbosc S, Cristol JP, Patel NS, Cuzzocrea S, Thiemermann C: Inhibitors of NADPH oxidase reduce the organ injury in hemorrhagic shock. Shock 23:107-114, 2005.
33. Izumi M, McDonald MC, Sharpe MA, Chatterjee PK, Thiemermann C: Superoxide dismutase mimetics with catalase activity reduce the organ injury in hemorrhagic shock. Shock 18:230-235, 2002.
34. Kentner R, Safar P, Behringer W, Wu X, Kagan VE, Tyurina YY, Henchir J, Ma L, Hsia CJ, Tisherman SA: Early antioxidant therapy with tempol during hemorrhagic shock increases survival in rats. J Trauma 53:968-977, 2002.
35. Mota-Filipe H, McDonald MC, Cuzzocrea S, Thiemermann C: A membrane-permeable radical scavenger reduces the organ injury in hemorrhagic shock. Shock 12:255-261, 1999.
36. Chandel NS, Trzyna WC, McClintock DS, Schumacker PT: Role of oxidants in NF-kappa B activation and TNF-alpha gene transcription induced by hypoxia and endotoxin. J Immunol 165:1013-1021, 2000.
37. Rensing H, Bauer I, Datene V, Patau C, Pannen BH, Bauer M: Differential expression pattern of heme oxygenase-1/heat shock protein 32 and nitric oxide synthase-II and their impact on liver injury in a rat model of hemorrhage and resuscitation. Crit Care Med 27:2766-2775, 1999.
38. Hoetzel A, Vagts DA, Loop T, Humar M, Bauer M, Pahl HL, Geiger KK, Pannen BH: Effect of nitric oxide on shock-induced hepatic heme oxygenase-1 expression in the rat. Hepatology 33:925-937, 2001.
39. Chandel NS, Maltepe E, Goldwasser E, Mathieu CE, Simon MC, Schumacker PT: Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc Natl Acad Sci USA 95:11715-11720, 1998.
40. Kentner R, Safar P, Behringer W, Wu X, Henchir J, Ma L, Hsia CJ, Tisherman SA: Small volume resuscitation with tempol is detrimental during uncontrolled hemorrhagic shock in rats. Resuscitation 72:295-305, 2007.
41. Douzinas EE, Andrianakis I, Livaditi O, Paneris P, Tasoulis M, Pelekanou A, Betrosian A, Giamarellos-Bourboulis EJ: The level of hypotension during hemorrhagic shock is a major determinant of the post-resuscitation systemic inflammatory response: an experimental study. BMC Physiol 8:15, 2008.
42. Fels DR, Koumenis C: The PERK/eIF2alpha/ATF4 module of the UPR in hypoxia resistance and tumor growth. Cancer Biol Ther 5:723-728, 2006.
43. Hanada S, Harada M, Kumemura H, Bishr OM, Koga H, Kawaguchi T, Taniguchi E, Yoshida T, Hisamoto T, Yanagimoto C, et al.: Oxidative stress induces the endoplasmic reticulum stress and facilitates inclusion formation in cultured cells. J Hepatol 47:93-102, 2007.
44. Kan WH, Hsieh CH, Schwacha MG, Choudhry MA, Raju R, Bland KI, Chaudry IH: Flutamide protects against trauma-hemorrhage-induced liver injury via attenuation of the inflammatory response, oxidative stress, and apopotosis. J Appl Physiol 105:595-602, 2008.
45. Yoshida H, Matsui T, Yamamoto A, Okada T, Mori K: XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107:881-891, 2001.
46. Lee AS: The ER chaperone and signaling regulator GRP78/BiP as a monitor of endoplasmic reticulum stress. Methods 35:373-381, 2005.
47. Xu C, Bailly-Maitre B, Reed JC: Endoplasmic reticulum stress: cell life and death decisions. J Clin Invest 115:2656-2664, 2005.
48. Zong WX, Li C, Hatzivassiliou G, Lindsten T, Yu QC, Yuan J, Thompson CB: Bax and Bak can localize to the endoplasmic reticulum to initiate apoptosis. J Cell Biol 162:59-69, 2003.
49. Schendel SL, Montal M, Reed JC: Bcl-2 family proteins as ion-channels. Cell Death Differ 5:372-380, 1998.
50. Reeve JL, Szegezdi E, Logue SE, Chonghaile TN, O'Brien T, Ritter T, Samali A: Distinct mechanisms of cardiomyocyte apoptosis induced by doxo-rubicin and hypoxia converge on mitochondria and are inhibited by Bcl-xL. J Cell Mol Med 11:509-520, 2007.
51. Vander Heiden MG, Chandel NS, Schumacker PT, Thompson CB: Bcl-xL prevents cell death following growth factor withdrawal by facilitating mito-chondrial ATP/ADP exchange. Mol Cell 3:159-167, 1999.
52. Gross A, McDonnell JM, Korsmeyer SJ: BCL-2 family members and the mitochondria in apoptosis. Genes Dev 13:1899-1911, 1999.
53. Carlson DE, Nguyen PX, Soane L, Fiedler SM, Fiskum G, Chiu WC, Scalea TM: Hypotensive hemorrhage increases calcium uptake capacity and Bcl-XL content of liver mitochondria. Shock 27:192-198, 2007.
54. Oyadomari S, Mori M: Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ 11:381-389, 2004.
55. McCullough KD, Martindale JL, Klotz LO, Aw TY, Holbrook NJ: Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol Cell Biol 21:1249-1259, 2001.
56. Kozlov AV, Duvigneau JC, Miller I, Nurnberger S, Gesslbauer B, Kungl A, Ohlinger W, Hartl RT, Gille L, Staniek K, et al.: Endotoxin causes functional endoplasmic reticulum failure, possibly mediated by mitochondria. Biochim Biophys Acta 1792(6):521-530, 2009.