In vivo altered unfolded protein response and apoptosis in livers from lipopolysaccharide-challenged cirrhotic rats

Journal of Hepatology

Volumn 46, Issue 6, 2007, Pages 1075-1088

  Tazi, Khalid A ^a,b   Bièche, Ivan ^c   Paradis, Valérie ^d,e   Guichard, Cécile ^f   Laurendeau, Ingrid ^c   Dargère, Delphine ^e   Legrand, Agnès ^c   Fay, Michèle ^a,b   Pedruzzi, Eric ^a,b   Robin, Marie Anne ^a,b   Cazals Hatem, Dominique ^d   Tellier, Zéra ^g   Bernuau, Dominique ^c   Feldmann, Gérard ^a,b   Vidaud, Michel ^c   Lebrec, Didier ^a,b   Ogier Denis, Eric ^a,b   Moreau, Richard ^a,b  

^a CENTRE DE RECHERCHE BIOMÉDICALE BICHAT BEAUJON CRB3   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c INSERM   (France)

^d BEAUJON HOSPITAL   (France)

^e CNRS   (France)

^f UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

^g Laboratoire Francais du Fractionnement et des Biotechnologies   (France)

Author keywords

ATF6; Cirrhosis; Endoplasmic reticulum; IRE1; LPS; PERK; Programmed cell death

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; CASPASE 12; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INITIATION FACTOR 2ALPHA; LIPOPOLYSACCHARIDE; PENTOXIFYLLINE; PROTEIN IRE1; PROTEIN KINASE; PROTEIN KINASE LIKE ENDOPLASMIC RETICULUM KINASE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; IN VIVO STUDY; LIVER CIRRHOSIS; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; RAT;

ANIMALS; APOPTOSIS; CASPASE 3; ENDOPLASMIC RETICULUM; EUKARYOTIC INITIATION FACTOR-2; FIBROSIS; LIPOPOLYSACCHARIDES; LIVER; MALE; PROTEIN DENATURATION; PROTEIN FOLDING; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 34247585054     PISSN: 01688278     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jhep.2007.01.034     Document Type: Article

References (60)

1. Schroder M., and Kaufman R.J. The mammalian unfolded protein response. Annu Rev Biochem 74 (2005) 739-789
2. Harding H.P., Zhang Y., and Ron D. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397 (1999) 271-274
3. Yoshida H., Matsui T., Yamamoto A., Okada T., and 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 (2001) 881-891
4. Scheuner D., Mierde D.V., Song B., Flamez D., Creemers J.W., Tsukamoto K., et al. Control of mRNA translation preserves endoplasmic reticulum function in beta cells and maintains glucose homeostasis. Nat Med 11 (2005) 757-764
5. Novoa I., Zeng H., Harding H.P., and Ron D. Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2alpha. J Cell Biol 153 (2001) 1011-1022
6. Novoa I., Zhang Y., Zeng H., Jungreis R., Harding H.P., and Ron D. Stress-induced gene expression requires programmed recovery from translational repression. EMBO J 22 (2003) 1180-1187
7. Boyce M., Bryant K.F., Jousse C., Long K., Harding H.P., Scheuner D., et al. A selective inhibitor of eIF2alpha dephosphorylation protects cells from ER stress. Science 307 (2005) 935-939
8. Scheu S., Stetson D.B., Reinhardt R.L., Leber J.H., Mohrs M., and Locksley R.M. Activation of the integrated stress response during T helper cell differentiation. Nat Immunol 7 (2006) 644-651
9. Marciniak S.J., Yun C.Y., Oyadomari S., Novoa I., Zhang Y., Jungreis R., et al. CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum. Genes Dev 18 (2004) 3066-3077
10. Shen J., and Prywes R. ER stress signaling by regulated proteolysis of ATF6. Methods 35 (2005) 382-389
11. Ye J., Rawson R.B., Komuro R., Chen X., Dave U.P., Prywes R., et al. ER stress induces cleavage of membrane-bound ATF6 by the same proteases that process SREBPs. Mol Cell 6 (2000) 1355-1364
12. Back S.H., Schroder M., Lee K., Zhang K., and Kaufman R.J. ER stress signaling by regulated splicing: IRE1/HAC1/XBP1. Methods 35 (2005) 395-416
13. Reimold A.M., Etkin A., Clauss I., Perkins A., Friend D.S., Zhang J., et al. Genes Dev 14 (2000) 152-157
14. Pahl H.L., and Baeuerle P.A. The ER-overload response: activation of NF-kappa B. Trends Biochem Sci 22 (1997) 63-67
15. Urano F., Wang X., Bertolotti A., Zhang Y., Chung P., Harding H.P., et al. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287 (2000) 664-666
16. Pedruzzi E., Guichard C., Ollivier V., Driss F., Fay M., Prunet C., et al. NAD(P)H oxidase Nox-4 mediates 7-ketocholesterol-induced endoplasmic reticulum stress and apoptosis in human aortic smooth muscle cells. Mol Cell Biol 24 (2004) 10703-10717
17. Guichard C., Pedruzzi E., Fay M., Marie J.C., Braut-Boucher F., Daniel F., et al. Dihydroxyphenylethanol induces apoptosis by activating serine/threonine protein phosphatase PP2A and promotes the endoplasmic reticulum stress response in human colon carcinoma cells. Carcinogenesis 27 (2006) 1812-1827
18. Nakagawa T., Zhu H., Morishima N., Li E., Xu J., Yankner B.A., et al. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 403 (2000) 98-103
19. Zhang K., Shen X., Wu J., Sakaki K., Saunders T., Rutkowski D.T., et al. Endoplasmic reticulum stress activates cleavage of CREBH to induce a systemic inflammatory response. Cell 124 (2006) 587-599
20. Harding H.P., Novoa I., Zhang Y., Zeng H., Wek R., Schapira M., et al. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol Cell 6 (2000) 1099-1108
21. Calfon M., Zeng H., Urano F., Till J.H., Hubbard S.R., Harding H.P., et al. IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415 (2002) 92-96
22. Lee A.H., Iwakoshi N.N., and Glimcher L.H. XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol Cell Biol 23 (2003) 7448-7459
23. Xue X., Piao J.H., Nakajima A., Sakon-Komazawa S., Kojima Y., Mori K., et al. Tumor necrosis factor alpha (TNFalpha) induces the unfolded protein response (UPR) in a reactive oxygen species (ROS)-dependent fashion, and the UPR counteracts ROS accumulation by TNFalpha. J Biol Chem 280 (2005) 33917-33925
24. Grivennikov S.I., Tumanov A.V., Liepinsh D.J., Kruglov A.A., Marakusha B.I., Shakhov A.N., et al. Distinct and nonredundant in vivo functions of TNF produced by T cells and macrophages/neutrophils: protective and deleterious effects. Immunity 22 (2005) 93-104
25. Wong F., Bernardi M., Balk R., Christman B., Moreau R., Garcia-Tsao G., et al. Sepsis in cirrhosis: report on the 7th meeting of the International Ascites Club. Gut 54 (2005) 718-725
26. Heller J., Sogni P., Barriere E., Tazi K.A., Chauvelot-Moachon L., Guimont M.C., et al. Effects of lipopolysaccharide on TNF-alpha production, hepatic NOS2 activity, and hepatic toxicity in rats with cirrhosis. J Hepatol 33 (2000) 376-381
27. Tazi K.A., Quioc J.J., Saada V., Bezeaud A., Lebrec D., and Moreau R. Upregulation of TNF-alpha production signaling pathways in monocytes from patients with advanced cirrhosis: Possible role of Akt and IRAK-M. J Hepatol 45 (2006) 280-289
28. Moreau R., Tazi K.A., Paradis V., Bieche I., Laurendeau I., Dargere D., et al. Lipopolysaccharide (LPS)-induced in vivo hepatocyte apoptosis due to posttranscriptional inhibition of nuclear factor-KappaB (NF-KappaB)-dependent survival proteins in rats with cirrhosis. Hepatology 38 Suppl.1 (2004) 264A
29. Scheuner D., Patel R., Wang F., Lee K., Kumar K., Wu J., et al. dsRNA-dependent protein kinase phosphorylation of the alpha subunit of eukaryotic translation initiation factor 2 mediates apoptosis. J Biol Chem 281 (2006) 21458-21468
30. Hu P., Han Z., Couvillon A.D., Kaufman R.J., and Exton J.H. Autocrine tumor necrosis factor alpha links endoplasmic reticulum stress to the membrane death receptor pathway through IRE1alpha-mediated NF-kappaB activation and down-regulation of TRAF2 expression. Mol Cell Biol 26 (2006) 3071-3084
31. Karin M., and Lin A. NF-kappaB at the crossroads of life and death. Nat Immunol 3 (2002) 221-227
32. Kreuz S., Siegmund D., Scheurich P., and Wajant H. NF-kappaB inducers upregulate cFLIP, a cycloheximide-sensitive inhibitor of death receptor signaling. Mol Cell Biol 21 (2001) 3964-3973
33. Tang G., Minemoto Y., Dibling B., Purcell N.H., Li Z., Karin M., et al. Inhibition of JNK activation through NF-kappaB target genes. Nature 414 (2001) 313-317
34. De Smaele E., Zazzeroni F., Papa S., Nguyen D.U., Jin R., Jones J., et al. Induction of gadd45beta by NF-kappaB downregulates pro-apoptotic JNK signalling. Nature 414 (2001) 308-313
35. Chaisson M.L., Brooling J.T., Ladiges W., Tsai S., and Fausto N. Hepatocyte-specific inhibition of NF-kappaB leads to apoptosis after TNF treatment, but not after partial hepatectomy. J Clin Invest 110 (2002) 193-202
36. Pham C.G., Bubici C., Zazzeroni F., Papa S., Jones J., Alvarez K., et al. Ferritin heavy chain upregulation by NF-kappaB inhibits TNFalpha-induced apoptosis by suppressing reactive oxygen species. Cell 119 (2004) 529-542
37. Kamata H., Honda S., Maeda S., Chang L., Hirata H., and Karin M. Reactive oxygen species promote TNFalpha-induced death and sustained JNK activation by inhibiting MAP kinase phosphatases. Cell 120 (2005) 649-661
38. Harry D., Anand R., Holt S., Davies S., Marley R., Fernando B., et al. Increased sensitivity to endotoxemia in the bile duct-ligated cirrhotic rat. Hepatology 30 (1999) 1198-1205
39. Moreau R., Barriere E., Tazi K.A., Lardeux B., Dargere D., Urbanowicz W., et al. Terlipressin inhibits in vivo aortic iNOS expression induced by lipopolysaccharide in rats with biliary cirrhosis. Hepatology 36 (2002) 1070-1078
40. Urbanowicz W., Sogni P., Moreau R., Tazi K.A., Barriere E., Poirel O., et al. Tezosentan, an endothelin receptor antagonist, limits liver injury in endotoxin challenged cirrhotic rats. Gut 53 (2004) 1844-1849
41. Robin M.A., Demeilliers C., Sutton A., Paradis V., Maisonneuve C., Dubois S., et al. Alcohol increases tumor necrosis factor alpha and decreases nuclear factor-kappab to activate hepatic apoptosis in genetically obese mice. Hepatology 42 (2005) 1280-1290
42. Bieche I., Parfait B., Le Doussal V., Olivi M., Rio M.C., Lidereau R., et al. Identification of CGA as a novel estrogen receptor-responsive gene in breast cancer: an outstanding candidate marker to predict the response to endocrine therapy. Cancer Res 61 (2001) 1652-1658
43. Liu P., Kimmoun E., Legrand A., Sauvanet A., Degott C., Lardeux B., et al. Activation of NF-kappaB, AP-1 and STAT transcription factors is a frequent and early event in human hepatocellular carcinomas. J Hepatol 37 (2002) 63-71
44. Nowak M., Gaines G.C., Rosenberg J., Minter R., Bahjat F.R., Rectenwald J., et al. LPS-induced liver injury in D-galactosamine-sensitized mice requires secreted TNF-alpha and the TNF-p55 receptor. Am J Physiol 278 (2000) R1202-R1209
45. Maeda S., Chang L., Li Z.W., Luo J.L., Leffert H., and Karin M. IKKbeta is required for prevention of apoptosis mediated by cell-bound but not by circulating TNFalpha. Immunity 19 (2003) 725-737
46. Zabel P., Schade F.U., and Schlaak M. Inhibition of endogenous TNF formation by pentoxifylline. Immunobiology 187 (1993) 447-463
47. Dever T.E. Gene-specific regulation by general translation factors. Cell 108 (2002) 545-556
48. Holcik M., and Sonenberg N. Translational control in stress and apoptosis. Nat Rev Mol Cell Biol 6 (2005) 318-327
49. Haze K., Okada T., Yoshida H., Yanagi H., Yura T., Negishi M., et al. Identification of the G13 (cAMP-response-element-binding protein-related protein) gene product related to activating transcription factor 6 as a transcriptional activator of the mammalian unfolded protein response. Biochem J 355 (2001) 19-28
50. Hsu L.C., Park J.M., Zhang K., Luo J.L., Maeda S., Kaufman R.J., et al. The protein kinase PKR is required for macrophage apoptosis after activation of Toll-like receptor 4. Nature 428 (2004) 341-345
51. Pikarsky E., Porat R.M., Stein I., Abramovitch R., Amit S., Kasem S., et al. NF-kappaB functions as a tumour promoter in inflammation-associated cancer. Nature 431 (2004) 461-466
52. Hamasaki A., Sendo F., Nakayama K., Ishida N., Negishi I., Nakayama K., et al. Accelerated neutrophil apoptosis in mice lacking A1-a, a subtype of the bcl-2-related A1 gene. J Exp Med 188 (1998) 1985-1992
53. Chang L., Kamata H., Solinas G., Luo J.L., Maeda S., Venuprasad K., et al. The E3 ubiquitin ligase itch couples JNK activation to TNFalpha-induced cell death by inducing c-FLIP(L) turnover. Cell 124 (2006) 601-613
54. Yeh W.C., Shahinian A., Speiser D., Kraunus J., Billia F., Wakeham A., et al. Early lethality, functional NF-kappaB activation, and increased sensitivity to TNF-induced cell death in TRAF2-deficient mice. Immunity 7 (1997) 715-725
55. Wang C.Y., Mayo M.W., Korneluk R.G., Goeddel D.V., and Baldwin Jr. A.S. NF-kappaB antiapoptosis: induction of TRAF1 and TRAF2 and c-IAP1 and c-IAP2 to suppress caspase-8 activation. Science 281 (1998) 1680-1683
56. Koritzinsky M., Seigneuric R., Magagnin M.G., van den Beucken T., Lambin P., and Wouters B.G. The hypoxic proteome is influenced by gene-specific changes in mRNA translation. Radiother Oncol 76 (2005) 177-186
57. Koumenis C., Naczki C., Koritzinsky M., Rastani S., Diehl A., Sonenberg N., et al. Regulation of protein synthesis by hypoxia via activation of the endoplasmic reticulum kinase PERK and phosphorylation of the translation initiation factor eIF2alpha. Mol Cell Biol 22 (2002) 7405-7416
58. Blais J.D., Filipenko V., Bi M., Harding H.P., Ron D., Koumenis C., et al. Activating transcription factor 4 is translationally regulated by hypoxic stress. Mol Cell Biol 24 (2004) 7469-7482
59. Martindale J.J., Fernandez R., Thuerauf D., Whittaker R., Gude N., Sussman M.A., et al. Endoplasmic reticulum stress gene induction and protection from ischemia/reperfusion injury in the hearts of transgenic mice with a tamoxifen-regulated form of ATF6. Circ Res 98 (2006) 1186-1193
60. Corpechot C., Barbu V., Wendum D., Chignard N., Housset C., Poupon R., et al. Hepatocyte growth factor and c-Met inhibition by hepatic cell hypoxia: a potential mechanism for liver regeneration failure in experimental cirrhosis. Am J Pathol 160 (2002) 613-620