Endoplasmic Reticulum stress induces hepatic stellate cell apoptosis and contributes to fibrosis resolution

Liver International

Volumn 32, Issue 10, 2012, Pages 1574-1584

  De Minicis, Samuele ^a   Candelaresi, Cinzia ^a   Agostinelli, Laura ^a   Taffetani, Silvia ^a   Saccomanno, Stefania ^a   Rychlicki, Chiara ^a   Trozzi, Luciano ^a   Marzioni, Marco ^a   Benedetti, Antonio ^a   Svegliati Baroni, Gianluca ^a  

^a UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

Author keywords

Apoptosis; ER stress; Extracellular matrix degradation; Hepatic stellate cells; Liver fibrosis

Indexed keywords

CALPAIN; CALPASTATIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; LIVER FIBROSIS; MALE; NONHUMAN; PROTEIN EXPRESSION; RAT; REMISSION; STELLATE CELL;

ANIMALS; APOPTOSIS; BILE DUCTS; BLOTTING, WESTERN; CALCIUM-BINDING PROTEINS; CALPAIN; CASPASE 8; ENDOPLASMIC RETICULUM STRESS; FIBROSIS; HEPATIC STELLATE CELLS; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; LIGATION; LIVER; RATS; RNA, SMALL INTERFERING; THAPSIGARGIN; TUNICAMYCIN;

EID: 84867102077     PISSN: 14783223     EISSN: 14783231     Source Type: Journal    
DOI: 10.1111/j.1478-3231.2012.02860.x     Document Type: Article

References (59)

1. Bataller R, Sancho-Bru P, Gines P, Brenner DA. Liver fibrogenesis: a new role for the renin-angiotensin system. Antioxid Redox Signal 2005; 7: 1346-55.
2. Friedman SL. Liver fibrosis - from bench to bedside. J Hepatol 2003; 38(Suppl 1): S38-53.
3. Friedman SL. Stellate cells: a moving target in hepatic fibrogenesis. Hepatology 2004; 40: 1041-3.
4. Reeves HL, Friedman SL. Activation of hepatic stellate cells-a key issue in liver fibrosis. Front Biosci 2002; 7: d808-26.
5. Svegliati-Baroni G, De Minicis S, Marzioni M. Hepatic fibrogenesis in response to chronic liver injury: novel insights on the role of cell-to-cell interaction and transition. Liver Int 2008; 28: 1052-64.
6. Wright MC, Issa R, Smart DE, et al. Gliotoxin stimulates the apoptosis of human and rat hepatic stellate cells and enhances the resolution of liver fibrosis in rats. Gastroenterology 2001; 121: 685-98.
7. Iredale JP, Benyon RC, Pickering J, et al. Mechanisms of spontaneous resolution of rat liver fibrosis. Hepatic stellate cell apoptosis and reduced hepatic expression of metalloproteinase inhibitors. J Clin Invest 1998; 102: 538-49.
8. Anan A, Baskin-Bey ES, Bronk SF, et al. Proteasome inhibition induces hepatic stellate cell apoptosis. Hepatology 2006; 43: 335-44.
9. Fulda S, Debatin KM. Extrinsic versus intrinsic apoptosis pathways in anticancer chemotherapy. Oncogene 2006; 25: 4798-811.
10. Khosravi-Far R, Esposti MD. Death receptor signals to mitochondria. Cancer Biol Ther 2004; 3: 1051-7.
11. Wajant H. The Fas signaling pathway: more than a paradigm. Science 2002; 296: 1635-6.
12. Malhi H, Kaufman RJ. Endoplasmic reticulum stress in liver disease. J Hepatol 2011; 54: 795-809.
13. Rasheva VI, Domingos PM. Cellular responses to endoplasmic reticulum stress and apoptosis. Apoptosis 2009; 14: 996-1007.
14. Kim R, Emi M, Tanabe K, Murakami S. Role of the unfolded protein response in cell death. Apoptosis 2006; 11: 5-13.
15. Ji C, Kaplowitz N. Hyperhomocysteinemia, endoplasmic reticulum stress, and alcoholic liver injury. World J Gastroenterol 2004; 10: 1699-708.
16. Novo E, Marra F, Zamara E, et al. Overexpression of Bcl-2 by activated human hepatic stellate cells: resistance to apoptosis as a mechanism of progressive hepatic fibrogenesis in humans. Gut 2006; 55: 1174-82.
17. Kawada N. Human hepatic stellate cells are resistant to apoptosis: implications for human fibrogenic liver disease. Gut 2006; 55: 1073-4.
18. Nakatsukasa K, Huyer G, Michaelis S, Brodsky JL. Dissecting the ER-associated degradation of a misfolded polytopic membrane protein. Cell 2008; 132: 101-12.
19. Hiller MM, Finger A, Schweiger M, Wolf DH. ER degradation of a misfolded luminal protein by the cytosolic ubiquitin-proteasome pathway. Science 1996; 273: 1725-8.
20. Malhotra JD, Kaufman RJ. The endoplasmic reticulum and the unfolded protein response. Semin Cell Dev Biol 2007; 18: 716-31.
21. van der Kallen CJ, van Greevenbroek MM, Stehouwer CD, Schalkwijk CG. Endoplasmic reticulum stress-induced apoptosis in the development of diabetes: is there a role for adipose tissue and liver? Apoptosis 2009; 14: 1424-34.
22. Szegezdi E, Logue SE, Gorman AM, Samali A. Mediators of endoplasmic reticulum stress-induced apoptosis. EMBO Rep 2006; 7: 880-5.
23. Marciniak SJ, Ron D. Endoplasmic reticulum stress signaling in disease. Physiol Rev 2006; 86: 1133-49.
24. Rao RV, Ellerby HM, Bredesen DE. Coupling endoplasmic reticulum stress to the cell death program. Cell Death Differ 2004; 11: 372-80.
25. Du Y, Wang K, Fang H, et al. Coordination of intrinsic, extrinsic, and endoplasmic reticulum-mediated apoptosis by imatinib mesylate combined with arsenic trioxide in chronic myeloid leukemia. Blood 2006; 107: 1582-90.
26. Liu Y, Borchert GL, Surazynski A, Hu CA, Phang JM. Proline oxidase activates both intrinsic and extrinsic pathways for apoptosis: the role of ROS/superoxides. NFAT and MEK/ERK signaling. Oncogene 2006; 25: 5640-7.
27. Shiraishi H, Okamoto H, Yoshimura A, Yoshida H. ER stress-induced apoptosis and caspase-12 activation occurs downstream of mitochondrial apoptosis involving Apaf-1. J Cell Sci 2006; 119: 3958-66.
28. Murakami Y, Aizu-Yokota E, Sonoda Y, Ohta S, Kasahara T. Suppression of endoplasmic reticulum stress-induced caspase activation and cell death by the overexpression of Bcl-xL or Bcl-2. J Biochem 2007; 141: 401-10.
29. Sanchez-Gomez MV, Alberdi E, Perez-Navarro E, Alberch J, Matute C. Bax and calpain mediate excitotoxic oligodendrocyte death induced by activation of both AMPA and kainate receptors. J Neurosci 2011; 31: 2996-3006.
30. De Minicis S, Seki E, Uchinami H, et al. Gene expression profiles during hepatic stellate cell activation in culture and in vivo. Gastroenterology 2007; 132: 1937-46.
31. Brafman DA, de Minicis S, Seki E, et al. Investigating the role of the extracellular environment in modulating hepatic stellate cell biology with arrayed combinatorial microenvironments. Integr Biol (Camb) 2009; 1: 513-24.
32. Di Sario A, Baroni GS, Bendia E, et al. Characterization of ion transport mechanisms regulating intracellular pH in hepatic stellate cells. Am J Physiol 1997; 273: G39-48.
33. Morishima N, Nakanishi K, Tsuchiya K, Shibata T, Seiwa E. Translocation of Bim to the endoplasmic reticulum (ER) mediates ER stress signaling for activation of caspase-12 during ER stress-induced apoptosis. J Biol Chem 2004; 279: 50375-81.
34. Di Sario A, Bendia E, Svegliati Baroni G, et al. Effect of pirfenidone on rat hepatic stellate cell proliferation and collagen production. J Hepatol 2002; 37: 584-91.
35. Marzioni M, Saccomanno S, Candelaresi C, et al. Pancreatic Duodenal Homeobox-1 de novo expression drives cholangiocyte neuroendocrine-like transdifferentiation. J Hepatol 2010; 53: 663-70.
36. Svegliati-Baroni G, Ghiselli R, Marzioni M, et al. Estrogens maintain bile duct mass and reduce apoptosis after biliodigestive anastomosis in bile duct ligated rats. J Hepatol 2006; 44: 1158-66.
37. Wang XZ, Kuroda M, Sok J, et al. Identification of novel stress-induced genes downstream of chop. EMBO J 1998; 17: 3619-30.
38. Guerra MT, Fonseca EA, Melo FM, et al. Mitochondrial calcium regulates rat liver regeneration through the modulation of apoptosis. Hepatology 2011; 54: 296-306.
39. Jung CR, Lim JH, Choi Y, et al. Enigma negatively regulates p53 through MDM2 and promotes tumor cell survival in mice. J Clin Invest 2010; 120: 4493-506.
40. Derdak Z, Lang CH, Villegas KA, et al. Activation of p53 enhances apoptosis and insulin resistance in a rat model of alcoholic liver disease. J Hepatol 2011; 54: 164-72.
41. Martin J, Romanque P, Maurhofer O, et al. Ablation of the tumor suppressor histidine triad nucleotide binding protein 1 is protective against hepatic ischemia/reperfusion injury. Hepatology 2011; 53: 243-52.
42. Zhang JQ, Li YM, Liu T, et al. Antitumor effect of matrine in human hepatoma G2 cells by inducing apoptosis and autophagy. World J Gastroenterol 2010; 16: 4281-90.
43. Schmich K, Schlatter R, Corazza N, et al. Tumor necrosis factor alpha sensitizes primary murine hepatocytes to Fas/CD95-induced apoptosis in a Bim- and Bid-dependent manner. Hepatology 2011; 53: 282-92.
44. Saile B, Matthes N, El Armouche H, Neubauer K, Ramadori G. The bcl, NFkappaB and p53/p21WAF1 systems are involved in spontaneous apoptosis and in the anti-apoptotic effect of TGF-beta or TNF-alpha on activated hepatic stellate cells. Eur J Cell Biol 2001; 80: 554-61.
45. Wang D, Wei Y, Schmoll D, Maclean KN, Pagliassotti MJ. Endoplasmic reticulum stress increases glucose-6-phosphatase and glucose cycling in liver cells. Endocrinology 2006; 147: 350-8.
46. Shuldiner AR, Yang R, Gong DW. Resistin, obesity and insulin resistance-the emerging role of the adipocyte as an endocrine organ. N Engl J Med 2001; 345: 1345-6.
47. Polotsky VY, Patil SP, Savransky V, et al. Obstructive sleep apnea, insulin resistance, and steatohepatitis in severe obesity. Am J Respir Crit Care Med 2009; 179: 228-34.
48. Kasuga M. Insulin resistance and pancreatic beta cell failure. J Clin Invest 2006; 116: 1756-60.
49. Boden G. Endoplasmic reticulum stress: another link between obesity and insulin resistance/inflammation? Diabetes 2009; 58: 518-9.
50. Shah PK. Innate immune pathway links obesity to insulin resistance. Circ Res 2007; 100: 1531-3.
51. Kuznetsov G, Nigam SK. Folding of secretory and membrane proteins. N Engl J Med 1998; 339: 1688-95.
52. Zhang K, Kaufman RJ. From endoplasmic-reticulum stress to the inflammatory response. Nature 2008; 454: 455-62.
53. Scheuner D, Kaufman RJ. The unfolded protein response: a pathway that links insulin demand with beta-cell failure and diabetes. Endocr Rev 2008; 29: 317-33.
54. Zhang K, Kaufman RJ. Protein folding in the endoplasmic reticulum and the unfolded protein response. Handb Exp Pharmacol 2006: 172; 69-91.
55. Wei Y, Wang D, Topczewski F, Pagliassotti MJ. Saturated fatty acids induce endoplasmic reticulum stress and apoptosis independently of ceramide in liver cells. Am J Physiol Endocrinol Metab 2006; 291: E275-81.
56. Zhang K. Integration of ER stress, oxidative stress and the inflammatory response in health and disease. Int J Clin Exp Med 2010; 3: 33-40.
57. Cullinan SB, Diehl JA. Coordination of ER and oxidative stress signaling: the PERK/Nrf2 signaling pathway. Int J Biochem Cell Biol 2006; 38: 317-32.
58. Boyce M, Yuan J. Cellular response to endoplasmic reticulum stress: a matter of life or death. Cell Death Differ 2006; 13: 363-73.
59. Hu P, Han Z, Couvillon AD, Exton JH. Critical role of endogenous Akt/IAPs and MEK1/ERK pathways in counteracting endoplasmic reticulum stress-induced cell death. J Biol Chem 2004; 279: 49420-9.