Endoplasmic reticulum stress is the crossroads of autophagy, inflammation, and apoptosis signaling pathways and participates in liver fibrosis

Inflammation Research

Volumn 64, Issue 1, 2015, Pages

  Li, Xiaohui ^a,b   Wang, Yarui ^b   Wang, Huan ^b   Huang, Cheng ^b   Huang, Yan ^b   Li, Jun ^b  

^a Department of Respiratory medicine   (China)

^b ANHUI MEDICAL UNIVERSITY   (China)

Author keywords

Apoptosis; Autophagy; Endoplasmic reticulum stress; Inflammation; Liver fibrosis

Indexed keywords

GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153;

ANIMAL; APOPTOSIS; AUTOPHAGY; CALCIUM SIGNALING; DISEASE COURSE; ENDOPLASMIC RETICULUM STRESS; HUMAN; INFLAMMATION; LIVER CELL; LIVER CIRRHOSIS; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; STELLATE CELL; UNFOLDED PROTEIN RESPONSE;

ANIMALS; APOPTOSIS; AUTOPHAGY; CALCIUM SIGNALING; DISEASE PROGRESSION; ENDOPLASMIC RETICULUM STRESS; HEPATIC STELLATE CELLS; HEPATOCYTES; HUMANS; INFLAMMATION; LIVER CIRRHOSIS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR CHOP; UNFOLDED PROTEIN RESPONSE;

EID: 84921938206     PISSN: 10233830     EISSN: 1420908X     Source Type: Journal    
DOI: 10.1007/s00011-014-0772-y     Document Type: Review

References (64)

1. Jiang JX, Torok NJ. Liver injury and the activation of the hepatic myofibroblasts. Curr Pathobiol Rep. 2013;1:215–23.
2. 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.
3. Friedman SL. Hepatic fibrosis—overview. Toxicology. 2008;254:120–9.
4. Wallace K, Burt AD, Wright MC. Liver fibrosis. Biochem J. 2008;411:1–18.
5. Atzori L, Poli G, Perra A. Hepatic stellate cell: a star cell in the liver. Int J Biochem Cell Biol. 2009;41:1639–42.
6. Wells RG. The role of matrix stiffness in hepatic stellate cell activation and liver fibrosis. J Clin Gastroenterol. 2005;39:S158–61.
7. Safadi R, Friedman SL. Hepatic fibrosis–role of hepatic stellate cell activation. Med General Med. 2002;4:27.
8. Kisseleva T, Brenner DA. Role of hepatic stellate cells in fibrogenesis and the reversal of fibrosis. J Gastroenterol Hepatol. 2007;22(Suppl 1):S73–8.
9. Schinoni MI, Parana R. Apoptosis and progression of hepatic fibrosis in liver diseases. Acta Gastroenterol Latinoam. 2006;36:211–7.
10. Kisseleva T, Brenner DA. Hepatic stellate cells and the reversal of fibrosis. J Gastroenterol Hepatol. 2006;21(Suppl 3):S84–7.
11. Leclercq IA, Da SMA, Schroyen B, Van Hul N, Geerts A. Insulin resistance in hepatocytes and sinusoidal liver cells: mechanisms and consequences. J Hepatol. 2007;47:142–56.
12. Mollica MP, Lionetti L, Putti R, Cavaliere G, Gaita M, Barletta A. From chronic overfeeding to hepatic injury: role of endoplasmic reticulum stress and inflammation. Nutr Metab Cardiovasc Dis. 2011;21:222–30.
13. Bravo R, Parra V, Gatica D, Rodriguez AE, Torrealba N, Paredes F, et al. Endoplasmic reticulum and the unfolded protein response: dynamics and metabolic integration. Int Rev Cell Mol Biol. 2013;301:215–90.
14. Engin F, Hotamisligil GS. Restoring endoplasmic reticulum function by chemical chaperones: an emerging therapeutic approach for metabolic diseases. Diabetes Obes Metab. 2010;12(Suppl 2):108–15.
15. Sovolyova N, Healy S, Samali A, Logue SE. Stressed to death—mechanisms of ER stress-induced cell death. Biol Chem. 2014;395:1–13.
16. Lenna S, Trojanowska M. The role of endoplasmic reticulum stress and the unfolded protein response in fibrosis. Curr Opin Rheumatol. 2012;24:663–8.
17. Gardner BM, Pincus D, Gotthardt K, Gallagher CM, Walter P. Endoplasmic reticulum stress sensing in the unfolded protein response. Cold Spring Harb Perspect Biol. 2013;5:a013169.
18. Malhotra JD, Kaufman RJ. ER stress and its functional link to mitochondria: role in cell survival and death. Cold Spring Harb Perspect Biol. 2011;3:a004424.
19. Rasheva VI, Domingos PM. Cellular responses to endoplasmic reticulum stress and apoptosis. Apoptosis. 2009;14:996–1007.
20. Sano R, Reed JC. ER stress-induced cell death mechanisms. Biochim Biophys Acta. 2013;1833(12):3460–70.
21. Hernandez-Gea V, Hilscher M, Rozenfeld R, Lim MP, Nieto N, Werner S, et al. Endoplasmic reticulum stress induces fibrogenic activity in hepatic stellate cells through autophagy. J Hepatol. 2013;59:98–104.
22. De Minicis S, Candelaresi C, Agostinelli L, Taffetani S, Saccomanno S, Rychlicki C, et al. Endoplasmic Reticulum stress induces hepatic stellate cell apoptosis and contributes to fibrosis resolution. Liver Int. 2012;32:1574–84.
23. Wang JQ, Chen X, Zhang C, Tao L, Zhang ZH, Liu XQ, et al. Phenylbutyric acid protects against carbon tetrachloride-induced hepatic fibrogenesis in mice. Toxicol Appl Pharmacol. 2013;266:307–16.
24. Foufelle F, Ferre P. Unfolded protein response: its role in physiology and physiopathology. Med Sci (Paris). 2007;23:291–6.
25. Hollien J. Evolution of the unfolded protein response. Biochim Biophys Acta. 2013;1833:2458–63.
26. Misra UK, Pizzo SV. Modulation of the unfolded protein response in prostate cancer cells by antibody-directed against the carboxyl-terminal domain of GRP78. Apoptosis. 2010;15:173–82.
27. Woehlbier U, Hetz C. Modulating stress responses by the UPRosome: a matter of life and death. Trends Biochem Sci. 2011;36:329–37.
28. Kim R, Emi M, Tanabe K, Murakami S. Role of the unfolded protein response in cell death. Apoptosis. 2006;11:5–13.
29. Feng LJ, Jiang TC, Zhou CY, Yu CL, Shen YJ, Li J, et al. Activated macrophage-like synoviocytes are resistant to endoplasmic reticulum stress-induced apoptosis in antigen-induced arthritis. Inflamm Res. 2014;63(5):335–46.
30. Shore GC, Papa FR, Oakes SA. Signaling cell death from the endoplasmic reticulum stress response. Curr Opin Cell Biol. 2011;23:143–9.
31. Prell T, Lautenschlager J, Grosskreutz J. Calcium-dependent protein folding in amyotrophic lateral sclerosis. Cell Calcium. 2013;54:132–43.
32. Nakagawa T, Zhu H, Morishima N, Li E, Xu J, Yankner BA, et al. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature. 2000;403:98–103.
33. Morishima N, Nakanishi K, Takenouchi H, Shibata T, Yasuhiko Y. An endoplasmic reticulum stress-specific caspase cascade in apoptosis. Cytochrome c-independent activation of caspase-9 by caspase-12. J Biol Chem. 2002;277:34287–94.
34. Xie Q, Khaoustov VI, Chung CC, Sohn J, Krishnan B, Lewis DE, et al. Effect of tauroursodeoxycholic acid on endoplasmic reticulum stress-induced caspase-12 activation. Hepatology. 2002;36:592–601.
35. Brostrom MA, Brostrom CO. Calcium dynamics and endoplasmic reticular function in the regulation of protein synthesis: implications for cell growth and adaptability. Cell Calcium. 2003;34:345–63.
36. Kooptiwut S, Mahawong P, Hanchang W, Semprasert N, Kaewin S, Limjindaporn T, et al. Estrogen reduces endoplasmic reticulum stress to protect against glucotoxicity induced-pancreatic beta-cell death. J Steroid Biochem Mol Biol. 2014;139:25–32.
37. Paredes RM, Bollo M, Holstein D, Lechleiter JD. Luminal Ca2+ depletion during the unfolded protein response in Xenopus oocytes: cause and consequence. Cell Calcium. 2013;53:286–96.
38. Anholt RR, Carbone MA. A molecular mechanism for glaucoma: endoplasmic reticulum stress and the unfolded protein response. Trends Mol Med. 2013;19:586–93.
39. Kapoor A, Sanyal AJ. Endoplasmic reticulum stress and the unfolded protein response. Clin Liver Dis. 2009;13:581–90.
40. Carpenter JE, Jackson W, Benetti L, Grose C. Autophagosome formation during varicella-zoster virus infection following endoplasmic reticulum stress and the unfolded protein response. J Virol. 2011;85:9414–24.
41. Nair S, Xu C, Shen G, Hebbar V, Gopalakrishnan A, Hu R, et al. Toxicogenomics of endoplasmic reticulum stress inducer tunicamycin in the small intestine and liver of Nrf2 knockout and C57BL/6J mice. Toxicol Lett. 2007;168:21–39.
42. Wu T, Zhao F, Gao B, Tan C, Yagishita N, Nakajima T, et al. Hrd1 suppresses Nrf2-mediated cellular protection during liver cirrhosis. Genes Dev. 2014;28:708–22.
43. Liu J, Wu KC, Lu YF, Ekuase E, Klaassen CD. Nrf2 protection against liver injury produced by various hepatotoxicants. Oxid Med Cell Longev. 2013;2013:305861.
44. Yang JJ, Tao H, Huang C, Li J. Nuclear erythroid 2-related factor 2: a novel potential therapeutic target for liver fibrosis. Food Chem Toxicol. 2013;59:421–7.
45. Lee BH, Hsu WH, Hsu YW, Pan TM. Suppression of dimerumic acid on hepatic fibrosis caused from carboxymethyl-lysine (CML) by attenuating oxidative stress depends on Nrf2 activation in hepatic stellate cells (HSCs). Food Chem Toxicol. 2013;62:413–9.
46. Reichard JF, Petersen DR. Hepatic stellate cells lack AP-1 responsiveness to electrophiles and phorbol 12-myristate-13-acetate. Biochem Biophys Res Commun. 2004;322:842–53.
47. Kohler UA, Kurinna S, Schwitter D, Marti A, Schafer M, Hellerbrand C, et al. Activated Nrf2 impairs liver regeneration in mice by activation of genes involved in cell-cycle control and apoptosis. Hepatology. 2014;60:670–8.
48. Tanjore H, Lawson WE, Blackwell TS. Endoplasmic reticulum stress as a pro-fibrotic stimulus. Biochim Biophys Acta. 2013;1832:940–7.
49. Brenner C, Galluzzi L, Kepp O, Kroemer G. Decoding cell death signals in liver inflammation. J Hepatol. 2013;59:583–94.
50. Duwaerts CC, Maher JJ. Mechanisms of liver injury in non-alcoholic steatohepatitis. Curr Hepatol Rep. 2014;13:119–29.
51. Zheng Z, Zhang C, Zhang K. Measurement of ER stress response and inflammation in the mouse model of nonalcoholic fatty liver disease. Methods Enzymol. 2011;489:329–48.
52. Wang CM, Li SJ, Wu CH, Hu CM, Cheng HW, Chang JS. Transient knock down of Grp78 reveals roles in serum ferritin mediated pro-inflammatory cytokine secretion in rat primary activated hepatic stellate cells. Asian Pac J Cancer Prev. 2014;15:605–10.
53. Cho HK, Cheong KJ, Kim HY, Cheong J. Endoplasmic reticulum stress induced by hepatitis B virus X protein enhances cyclo-oxygenase 2 expression via activating transcription factor 4. Biochem J. 2011;435:431–9.
54. Malhi H, Kaufman RJ. Endoplasmic reticulum stress in liver disease. J Hepatol. 2011;54:795–809.
55. Ji C. Dissection of endoplasmic reticulum stress signaling in alcoholic and non-alcoholic liver injury. J Gastroenterol Hepatol. 2008;23(Suppl 1):S16–24.
56. Jeschke MG, Gauglitz GG, Song J, Kulp GA, Finnerty CC, Cox RA, et al. Calcium and ER stress mediate hepatic apoptosis after burn injury. J Cell Mol Med. 2009;13:1857–65.
57. Zhang J, Li Y, Jiang S, Yu H, An W. Enhanced endoplasmic reticulum SERCA activity by overexpression of hepatic stimulator substance gene prevents hepatic cells from ER stress-induced apoptosis. Am J Physiol Cell Physiol. 2014;306:C279–90.
58. Gorman AM, Healy SJ, Jager R, Samali A. Stress management at the ER: regulators of ER stress-induced apoptosis. Pharmacol Ther. 2012;134:306–16.
59. Lai E, Teodoro T, Volchuk A. Endoplasmic reticulum stress: signaling the unfolded protein response. Physiology (Bethesda). 2007;22:193–201.
60. Tashiro K, Satoh A, Utsumi T, Chung C, Iwakiri Y. Absence of Nogo-B (reticulon 4B) facilitates hepatic stellate cell apoptosis and diminishes hepatic fibrosis in mice. Am J Pathol. 2013;182:786–95.
61. Lim MP, Devi LA, Rozenfeld R. Cannabidiol causes activated hepatic stellate cell death through a mechanism of endoplasmic reticulum stress-induced apoptosis. Cell Death Dis. 2011;2:e170.
62. Dolai S, Pal S, Yadav RK, Adak S. Endoplasmic reticulum stress-induced apoptosis in Leishmania through Ca2+-dependent and caspase-independent mechanism. J Biol Chem. 2011;286:13638–46.
63. Raimbourg Q, Perez J, Vandermeersch S, Prignon A, Hanouna G, Haymann JP, et al. The calpain/calpastatin system has opposing roles in growth and metastatic dissemination of melanoma. PLoS One. 2013;8:e60469.
64. Lin HJ, Tseng CP, Lin CF, Liao MH, Chen CM, Kao ST, et al. A Chinese herbal decoction, modified Yi Guan Jian, induces apoptosis in hepatic stellate cells through an ROS-mediated mitochondrial/caspase pathway. Evid Based Complement Alternat Med. 2011;2011:459531.