Pancreatic adaptive responses in alcohol abuse: Role of the unfolded protein response

Pancreatology

Volumn 15, Issue 4, 2015, Pages S1-S5

  Lugea, Aurelia ^a   Waldron, Richard T ^a   Pandol, Stephen J ^a  

^a VA GREATER LOS ANGELES HEALTHCARE SYSTEM   (United States)

Author keywords

Alcohol; Alcohol abuse; ER stress; Pancreas; Pancreatitis; Unfolded protein response

Indexed keywords

ALCOHOLISM; ANIMAL; COMPLICATION; ENDOPLASMIC RETICULUM STRESS; GENETICS; HUMAN; PANCREAS; PANCREATITIS, ALCOHOLIC; PATHOLOGY; UNFOLDED PROTEIN RESPONSE;

ALCOHOLISM; ANIMALS; ENDOPLASMIC RETICULUM STRESS; HUMANS; PANCREAS; PANCREATITIS, ALCOHOLIC; UNFOLDED PROTEIN RESPONSE;

EID: 84923532332     PISSN: 14243903     EISSN: 14243911     Source Type: Journal    
DOI: 10.1016/j.pan.2015.01.011     Document Type: Review

References (56)

1. Yadav, D., Eigenbrodt, M.L., Briggs, M.J., et al. Pancreatitis: prevalence and risk factors among male veterans in a detoxification program. Pancreas 34 (2007), 390–398.
2. Yadav, D., Lowenfels, A.B., The epidemiology of pancreatitis and pancreatic cancer. Gastroenterology 144 (2013), 1252–1261.
3. Sand, J., Lankisch, P.G., Nordback, I., Alcohol consumption in patients with acute or chronic pancreatitis. Pancreatology 7 (2007), 147–156.
4. Whitcomb, D.C., Genetics and alcohol: a lethal combination in pancreatic disease?. Alcohol Clin Exp Res 35 (2011), 838–842.
5. Anderson, M.A., Zolotarevsky, E., Cooper, K.L., Sherman, S., Shats, O., Whitcomb, D.C., et al. Alcohol and tobacco lower the age of presentation in sporadic pancreatic cancer in a dose-dependent manner: a multicenter study. Am J Gastroenterol 107 (2012), 1730–1739.
6. Whitcomb, D.C., LaRusch, J., Krasinskas, A.M., Klei, L., Smith, J.P., Brand, R.E., et al. Common genetic variants in the CLDN2 and PRSS1-PRSS2 loci alter risk for alcohol-related and sporadic pancreatitis. Nat Genet 44 (2012), 1349–1354.
7. Pandol, S.J., Periskic, S., Gukovsky, I., Zaninovic, V., Jung, Y., Zong, Y., et al. Ethanol diet increases the sensitivity of rats to pancreatitis induced by cholecystokinin octapeptide. Gastroenterology 117 (1999), 706–716.
8. Apte, M.V., Phillips, P.A., Fahmy, R.G., Darby, S.J., Rodgers, S.C., McCaughan, G.W., et al. Does alcohol directly stimulate pancreatic fibrogenesis? Studies with rat pancreatic stellate cells. Gastroenterology 118 (2000), 780–794.
9. Yadav, D., Whitcomb, D.C., The role of alcohol and smoking in pancreatitis. Nat Rev Gastroenterol Hepatol 7 (2010), 131–145.
10. Lugea, A., Waldron, R.T., French, S.W., et al. Drinking and driving pancreatitis: links between endoplasmic reticulum stress and autophagy. Autophagy 7 (2011), 783–785.
11. Direnzo, D., Hess, D.A., Damsz, B., Hallet, J.E., Marshall, B., Goswami, C., et al. Induced MIST1 expression promotes remodeling of mouse pancreatic acinar cells. Gastroenterology 143 (2012), 469–480.
12. Kim, I., Xu, W., Reed, J.C., Cell death and endoplasmic reticulum stress: disease relevance and therapeutic opportunities. Nat Rev Drug Discov 7 (2008), 1013–1030.
13. Mandl, J., Mészáros, T., Bánhegyi, G., et al. Minireview: endoplasmic reticulum stress: control in protein, lipid, and signal homeostasis. Mol Endocrinol 27 (2013), 384–393.
14. Han, J., Back, S.H., Hur, J., Lin, Y.H., Gildersleeve, R., Shan, J., et al. ER-stress-induced transcriptional regulation increases protein synthesis leading to cell death. Nat Cell Biol 15 (2013), 481–490.
15. Sutton, R., Petersen, O.H., Pandol, S.J., Pancreatitis and calcium signaling: report of an international workshop. Pancreas 36 (2008), e1–e14.
16. Mukherjee, R., Criddle, D.N., Gukovskaya, A., Gukvoskaya, A., Pandol, S., Petersen, O.H., et al. Mitochondrial injury in pancreatitis. Cell Calcium 44 (2008), 14–23.
17. Pandol, S.J., Saluja, A.K., Imrie, C.W., et al. Acute pancreatitis: bench to the bedside. Gastroenterology 132 (2007), 1127–1151.
18. Kim, M.S., Lee, K.P., Yang, D., Shin, D.M., Abramowitz, J., Kiyonaka, S., et al. Genetic and pharmacologic inhibition of the Ca2+ influx channel TRPC3 protects secretory epithelia from Ca2+-dependent toxicity. Gastroenterology 140 (2011), 2107–2115 2115 e1-4.
19. Ron, D., Walter, P., Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8 (2007), 519–529.
20. Rutkowski, D.T., Kaufman, R.J., That which does not kill me makes me stronger: adapting to chronic ER stress. Trends Biochem Sci 32 (2007), 469–476.
21. Marciniak, S.J., Garcia-Bonilla, L., Hu, J., et al. Activation-dependent substrate recruitment by the eukaryotic translation initiation factor 2 kinase PERK. J Cell Biol 172 (2006), 201–209.
22. Kaser, A., Lee, A.H., Franke, A., Glickman, J.N., Zeissig, S., Tilg, H., et al. XBP1 links ER stress to intestinal inflammation and confers genetic risk for human inflammatory bowel disease. Cell 134 (2008), 743–756.
23. Lin, J.H., Li, H., Yasumura, D., Cohen, H.R., Zhang, C., Panning, B., et al. IRE1 signaling affects cell fate during the unfolded protein response. Science 318 (2007), 944–949.
24. Chambers, J.E., Marciniak, S.J., Cellular mechanisms of endoplasmic reticulum stress signaling in health and disease. 2. Protein misfolding and ER stress. Am J Physiol Cell Physiol 307 (2014), C657–C670.
25. Lee, A.H., Chu, G.C., Iwakoshi, N.N., et al. XBP-1 is required for biogenesis of cellular secretory machinery of exocrine glands. EMBO J 24 (2005), 4368–4380.
26. 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.
27. Ghosh, R., Wang, L., Wang, E.S., Perera, B.G., Igbaria, A., Morita, S., et al. Allosteric inhibition of the IRE1alpha RNase preserves cell viability and function during endoplasmic reticulum stress. Cell 158 (2014), 534–548.
28. Hetz, C., Martinon, F., Rodriguez, D., et al. The unfolded protein response: integrating stress signals through the stress sensor IRE1alpha. Physiol Rev 91 (2011), 1219–1243.
29. Hetz, C., Bernasconi, P., Fisher, J., Lee, A.H., Bassik, M.C., Antonsson, B., et al. Proapoptotic BAX and BAK modulate the unfolded protein response by a direct interaction with IRE1alpha. Science 312 (2006), 572–576.
30. Lisbona, F., Rojas-Rivera, D., Thielen, P., Zamorano, S., Todd, D., Martinon, F., et al. BAX inhibitor-1 is a negative regulator of the ER stress sensor IRE1alpha. Mol Cell 33 (2009), 679–691.
31. Yalcin, A., Hotamisligil, G.S., Impact of ER protein homeostasis on metabolism. Diabetes 62 (2013), 691–693.
32. Johansson, B.B., Torsvik, J., Bjorkhaug, L., Vesterhus, M., Ragvin, A., Tjora, E., et al. Diabetes and pancreatic exocrine dysfunction due to mutations in the carboxyl ester lipase gene-maturity onset diabetes of the young (CEL-MODY): a protein misfolding disease. J Biol Chem 286 (2011), 34593–34605.
33. Xiao, X., Ferguson, M.R., Magee, K.E., et al. The Arg92Cys colipase polymorphism impairs function and secretion by increasing protein misfolding. J Lipid Res 54 (2013), 514–521.
34. Weiss, M.A., Diabetes mellitus due to the toxic misfolding of proinsulin variants. FEBS Lett 587 (2013), 1942–1950.
35. Young, J.C., The role of the cytosolic HSP70 chaperone system in diseases caused by misfolding and aberrant trafficking of ion channels. Dis Model Mech 7 (2014), 319–329.
36. Nemeth, B.C., Sahin-Toth, M., Human cationic trypsinogen (PRSS1) variants and chronic pancreatitis. Am J Physiol Gastrointest Liver Physiol 306 (2014), G466–G473.
37. Sans, M.D., Xie, Q., Williams, J.A., Regulation of translation elongation and phosphorylation of eEF2 in rat pancreatic acini. Biochem Biophys Res Commun 319 (2004), 144–151.
38. Uemura, A., Oku, M., Mori, K., et al. Unconventional splicing of XBP1 mRNA occurs in the cytoplasm during the mammalian unfolded protein response. J Cell Sci 122 (2009), 2877–2886.
39. Luo, X., Shin, D.M., Wang, X., et al. Aberrant localization of intracellular organelles, Ca2+ signaling, and exocytosis in Mist1 null mice. J Biol Chem 280 (2005), 12668–12675.
40. Lugea, A., Tischler, D., Nguyen, J., Gong, J., Gukovsky, I., French, S.W., et al. Adaptive unfolded protein response attenuates alcohol-induced pancreatic damage. Gastroenterology 140 (2011), 987–997.
41. Hess, D.A., Humphrey, S.E., Ishibashi, J., Damsz, B., Lee, A.H., Glimcher, L.H., et al. Extensive pancreas regeneration following acinar-specific disruption of Xbp1 in mice. Gastroenterology 141 (2011), 1463–1472.
42. Lee, K., Tirasophon, W., Shen, X., Michalak, M., Prywes, R., Okada, T., et al. IRE1-mediated unconventional mRNA splicing and S2P-mediated ATF6 cleavage merge to regulate XBP1 in signaling the unfolded protein response. Genes Dev 16 (2002), 452–466.
43. Blais, J.D., Chin, K.T., Zito, E., Zhang, Y., Heldman, N., Harding, H.P., et al. A small molecule inhibitor of endoplasmic reticulum oxidation 1 (ERO1) with selectively reversible thiol reactivity. J Biol Chem 285 (2010), 20993–21003.
44. 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.
45. Scheuner, D., Song, B., McEwen, E., Liu, C., Laybutt, R., Gillespie, P., et al. Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol Cell 7 (2001), 1165–1176.
46. Iida, K., Li, Y., McGrath, B.C., et al. PERK eIF2 alpha kinase is required to regulate the viability of the exocrine pancreas in mice. BMC Cell Biol, 8, 2007, 38.
47. Harding, H.P., Zhang, Y., Zeng, H., Novoa, I., Lu, P.D., Calfon, M., et al. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol Cell 11 (2003), 619–633.
48. Oyadomari, S., Mori, M., Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ 11 (2004), 381–389.
49. Goodall, J.C., Wu, C., Zhang, Y., McNeill, L., Ellis, L., Saudek, V., et al. Endoplasmic reticulum stress-induced transcription factor, CHOP, is crucial for dendritic cell IL-23 expression. Proc Natl Acad Sci U S A 107 (2010), 17698–17703.
50. Malhi, H., Kropp, E.M., Clavo, V.F., Kobrossi, C.R., Han, J., Mauer, A.S., et al. C/EBP homologous protein-induced macrophage apoptosis protects mice from steatohepatitis. J Biol Chem 288 (2013), 18624–18642.
51. Suyama, K., Ohmuraya, M., Hirota, M., Ozaki, N., Ida, S., Endo, M., Araki, K., et al. C/EBP homologous protein is crucial for the acceleration of experimental pancreatitis. Biochem Biophys Res Commun 367 (2008), 176–182.
52. Gukovsky, I., Lugea, A., Shahsahebi, M., Cheng, J.H., Hong, P.P., Jung, Y.J., et al. A rat model reproducing key pathological responses of alcoholic chronic pancreatitis. Am J Physiol Gastrointest Liver Physiol 294 (2008), G68–G79.
53. Lam, P.P., Cosen Binker, L.I., Lugea, A., et al. Alcohol redirects CCK-mediated apical exocytosis to the acinar basolateral membrane in alcoholic pancreatitis. Traffic 8 (2007), 605–617.
54. Vonlaufen, A., Phillips, P.A., Xu, Z., Zhang, X., Yang, L., Pirola, R.C., et al. Withdrawal of alcohol promotes regression while continued alcohol intake promotes persistence of LPS-induced pancreatic injury in alcohol-fed rats. Gut 60 (2011), 238–246.
55. Pandol, S.J., Gukovsky, I., Satoh, A., et al. Animal and in vitro models of alcoholic pancreatitis: role of cholecystokinin. Pancreas 27 (2003), 297–300.
56. Alahari, S., Mehmood, R., Johnson, C.L., et al. The absence of MIST1 leads to increased ethanol sensitivity and decreased activity of the unfolded protein response in mouse pancreatic acinar cells. PLoS One, 6, 2011, e28863.