Pancreatic β-cells depend on basal expression of active ATF6 α-p50 for cell survival even under nonstress conditions

American Journal of Physiology - Cell Physiology

Volumn 302, Issue 7, 2012, Pages

  Teodoro, Tracy ^a,b   Odisho, Tanya ^a,b   Sidorova, Elena ^b   Volchuk, Allen ^a,b  

^a UNIVERSITY HEALTH NETWORK   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Activating transcription factor 6; Apoptosis; Endoplasmic reticulum chaperones; Endoplasmic reticulum stress; GRP78; Stress kinases

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; CHAPERONE; GLUCOSE REGULATED PROTEIN 78; PROTEIN P50; SMALL INTERFERING RNA; STRESS ACTIVATED PROTEIN KINASE; SYNAPTOPHYSIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL SURVIVAL; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; HOMEOSTASIS; INSULINOMA; MOLECULAR RECOGNITION; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; STEADY STATE; UNFOLDED PROTEIN RESPONSE;

ACTIVATING TRANSCRIPTION FACTOR 6; ANIMALS; APOPTOSIS; CELL LINE, TUMOR; CELL SURVIVAL; CELLS, CULTURED; EIF-2 KINASE; ENDOPLASMIC RETICULUM; GENE KNOCKDOWN TECHNIQUES; HEAT-SHOCK PROTEINS; HELA CELLS; HUMANS; INSULIN-SECRETING CELLS; INSULINOMA; ISLETS OF LANGERHANS; MAP KINASE KINASE 4; MEMBRANE PROTEINS; MICE; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS C-JUN; RATS; RNA, MESSENGER; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE;

RODENTIA;

EID: 84859477044     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00160.2011     Document Type: Article

References (50)

1. Adachi Y, Yamamoto K, Okada T, Yoshida H, Harada A, Mori K. ATF6 is a transcription factor specializing in the regulation of quality control proteins in the endoplasmic reticulum. Cell Struct Funct 33: 75-89, 2008.
2. Amyot J, Benterki I, Fontes G, Hagman DK, Ferdaoussi M, Teodoro T, Volchuk A, Joly E, Poitout V. Binding of activating transcription factor 6 to the A5/Core of the rat insulin II gene promoter does not mediate its transcriptional repression. J Mol Endocrinol 47: 273-283, 2011.
3. Asfari M, Janjic D, Meda P, Li G, Halban PA, Wolheim CB. Establishment of 2-mercaptoethanol-dependent differentiated insulin-secreting cell lines. Endocrinology 130: 167-178, 1992.
4. Bartz R, Sun LP, Bisel B, Wei JH, Seemann J. Spatial separation of Golgi and ER during mitosis protects SREBP from unregulated activation. EMBO J 27: 948-955, 2008.
5. Bennett BL, Sasaki DT, Murray BW, O'Leary EC, Sakata ST, Xu W, Leisten JC, Motiwala A, Pierce S, Satoh Y, Bhagwat SS, Manning AM, Anderson DW. SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proc Natl Acad Sci USA 98: 13681-13686, 2001.
6. Bridge AJ, Pebernard S, Ducraux A, Nicoulaz AL, Iggo R. Induction of an interferon response by RNAi vectors in mammalian cells. Nat Genet 34: 263-264, 2003.
7. Cai B, Chang SH, Becker EBE, Bonni A, Xia Z. p38 MAP kinase mediates apoptosis through phosphorylation of Bim(EL) at Ser-65. J Biol Chem 281: 25215-25222, 2006.
8. Chen X, Shen J, Prywes F. The luminal domain of ATF6 senses endoplasmic reticulum (ER) stress and causes translocation of ATF6 from the ER to the Golgi. J Biol Chem 277: 13045-13052, 2002.
9. Chevet E. From stress specificity to basal necessity: ATF6 uprising. Focus on "Pancreatic β-cells depend on basal expression of active ATF6α-p50 for cell survival even under nonstress conditions" Am J Physiol Cell Physiol (January 11, 2012). doi:10.1152/ajpcell.00001.2012.
10. Dudek J, Benedix J, Cappel G, Grenier M, Jalal C, Muller L, Zimmermann R. Functions and pathologies of BiP and its interaction partners. Cell Mol Life Sci 66: 1556-1569, 2009.
11. Eizirik DL, Cardozo AK, Cnop M. The role for endoplasmic reticulum stress in diabetes mellitus. Endocr Rev 29: 42-61, 2008.
12. Elouil H, Bensellam M, Guiot Y, Vander Mierde D, Pascal SM, Schuit FC, Jonas JC. Acute nutrient regulation of the unfolded protein response and integrated stress response in cultured rat pancreatic islets. Diabetologia 50: 1442-1452, 2007.
13. Fonseca SG, Ishigaki S, Oslowski CM, Lu S, Lipson KL, Ghosh R, Hayashi E, Ishihara J, Oka Y, Permutt MA, Urano F. Wolfram syndrome 1 gene negatively regulates ER stress signaling in rodent and human cells. J Clin Invest 120: 744-755, 2010.
14. Gorbatyuk MS, Knox T, LaVail MM, Gorbatyuk OS, Noorwez SM, Hauswirth WW, Lin JH, Muzyczka M, Lewin AS. Restoration of visual function in P23H rhodopsin transgenic rats by gene delivery of BiP/Grp78. Proc Natl Acad Sci USA 107: 5961-5966, 2010.
15. Gotoh T, Oyadomari S, Mori K, Mori M. Nitric oxide-induced apoptosis in RAW 264.7 macrophages is mediated by endoplasmic reticulum stress pathway involving ATF6 and CHOP. J Biol Chem 277: 12343-12350, 2002.
16. Harding HP, Calfon M, Urano F, Novoa I, Ron D. Transcriptional and translational control in the mammalian unfolded protein response. Annu Rev Cell Dev Biol 18: 575-599, 2002.
17. Haze K, Yoshida H, Yanagi H, Yura T, Mori K. Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress. Mol Biol Cell 10: 3787-3799, 1999.
18. + channel-dependent and -independent glucose-stimulated insulin secretion. Diabetes 49: 424-430, 2000.
19. Karaskov E, Scott C, Zhang L, Teodoro T, Ravazzola M, Volchuk A. Chronic palmitate but not oleate exposure induces endoplasmic reticulum stress, which may contribute to INS-1 pancreatic beta-cell apoptosis. Endocrinology 147: 3398-3407, 2006.
20. Keshet Y, Seger R. The MAP kinase signaling cascades: a system of hundreds of components regulates a diverse array of physiological functions. Methods Mol Biol 661: 3-38, 2010.
21. Kilkenny D, Rocheleau J. Fibroblast growth factor receptor-1 signaling in pancreatic islet beta-cells is modulated by the extracellular matrix. Mol Endocrinol 22: 196-205, 2008.
22. Kokame K, Kato H, Miyata T. Identification of ERSE-II, a new cisacting element responsible for the ATF6-dependent mammalian unfolded protein response. J Biol Chem 276: 9199-9205, 2001.
23. Lai E, Bikopoulos G, Wheeler MB, Rozakis-Adcock M, Volchuk A. Differential activation of ER stress and apoptosis in response to chronically elevated free fatty acids in pancreatic β-cells. Am J Physiol Endocrinol Metab 294: E540-E550, 2008.
24. Laybutt DR, Preston AM, Akerfeldt MC, Kench JG, Busch AK, Biandin AV, Biden TJ. Endoplasmic reticulum stress contributes to beta cell apoptosis in type 2 diabetes. Diabetologia 50: 752-763, 2007.
25. Lipson KL, Fonseca SG, Ishigaki S, Nguyen L, Foss E, Bortell R, Rossini A, Urano F. Regulation of insulin biosynthesis in pancreatic beta cells by an endoplasmic reticulum-resident protein kinase IRE1. Cell Metab 4: 245-254, 2006.
26. Marciniak SJ, Ron D. Endoplasmic reticulum stress signaling in disease. Physiol Rev 86: 1133-1149, 2006.
27. Nadanaka S, Yoshida H, Sato R, Mori K. Analysis of ATF6 activation in Site-2 protease-deficient Chinese hamster ovary cells. Cell Struct Funct 31: 109-116, 2006.
28. Nozaki J, Kubota H, Yoshida H, Naitoh M, Goji J, Yoshinaga T, Mori K, Koizumi A, Nagata K. The endoplasmic reticulum stress response is stimulated through the continuous activation of transcription factors ATF6 and XBP1 in Ins2 /Akita pancreatic beta cells. Genes Cells 9: 261-270, 2004.
29. Okada T, Yoshida H, Akazawa R, Neqishi M, Mori K. Distinct roles of activating transcription factor 6 (ATF6) and double-stranded RNA-activated protein kinase-like endoplasmic reticulum kinase (PERK) in transcription during the mammalian unfolded protein response. Biochem J 366: 585-594, 2002.
30. Oyadomari S, Araki E, Mori K. Endoplasmic reticulum stress-mediated apoptosis in pancreatic beta-cells. Apoptosis 7: 335-345, 2002.
31. Ron D, Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8: 519-529, 2007.
32. Schewe DM, Aguirre-Ghiso JA. ATF6alpha-Rheb-mTOR signaling promotes survival of dormant tumor cells in vivo. Proc Natl Acad Sci USA 105: 10519-10524, 2008.
33. Schindler AJ, Schedman R. In vitro reconstitution of ER-stress induced ATF6 transport in COPII vesicles. Proc Natl Acad Sci USA 106: 17775-17780, 2009.
34. Seo HY, Kim YD, Lee KM, Min AK, Kim MK, Kim HS, Won KC, Park JY, Lee KU, Choi HS, Park KG, Lee IK. Endoplasmic reticulum stress-induced activation of activating transcription factor 6 decreases insulin gene expression via up-regulation of orphan nuclear receptor small heterodimer partner. Endocrinology 149: 3832-3841, 2008.
35. Shen J, Chen X, Hendershot L, Prywes F. ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of Golgi localization signals. Dev Cell 3: 9901-9911, 2002.
36. Teodoro T, Zhang L, Alexander T, Yue J, Vranic M, Volchuk A. Oleanolic acid enhances insulin secretion in pancreatic beta-cells. FEBS Lett 582: 1375-1380, 2008.
37. Thuerauf DJ, Arnold ND, Zechner D, Hanford DS, DeMartin KM, McDonough PM, Prywes R, Glembotski CC. p38 Mitogen-activated protein kinase mediates the transcriptional induction of the atrial natriuretic factor gene through a serum response element. A potential role for the transcription factor ATF6. J Biol Chem 273: 20636-20643, 1998.
38. Thuerauf DJ, Morrison L, Glembotski CC. Opposing roles for ATF6alpha and ATF6beta in endoplasmic reticulum stress response gene induction. J Biol Chem 279: 21078-21084, 2004.
39. Tournier C, Hess P, Yang DD, Xu J, Turner TK, Nimnual A, Bar-Sagi D, Jones SN, Flavell RA, Davis RJ. Requirement of JNK for stressinduced activation of the cytocrome c-mediated death pathway. Science 288: 870-874, 2000.
40. Underwood DC, Osborn RR, Kotzer CJ, Adams JL, Lee JC, Webb EF, Carpenter DC, Bochnowicz S, Thomas HC, Hay DW, Griswold DE. SB 239063, a potent p38 MAP kinase inhibitor, reduces inflammatory cytokine production, airways eosinophil infiltration, and persistence. J Pharmacol Exp Ther 293: 281-288, 2000.
41. Urano F, Wang XZ, Bertolotti A, Zhang Y, Chung P, Harding HP, Ron D. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287: 664-666, 2000.
42. Van Anken E, Braakman I. Versatility of the endoplasmic reticulum protein folding factory. Crit Rev Biochem Mol Biol 40: 191-228, 2005.
43. Vellanki RN, Zhang L, Guney MA, Rocheleau J, Gannon M, Volchuk A. OASIS/CREB3L1 induces expression of genes involved in extracellular matrix production but not classical endoplasmic reticulum stress response genes in pancreatic beta-cells. Endocrinology 151: 4146-4157, 2010.
44. Wang H, Kouri G, Wolheim CB. ER stress and SREBP-1 activation are implicated in beta-cell glucolipotoxicity. J Cell Sci 118: 3905-3915, 2005.
45. Wu J, Ruas JL, Estall JL, Rasbach KA, Choi JH, Ye L, Bostrom P, Tyra HM, Crawford RW, Campbell KP, Rutkowski DT, Kaufman RJ, Spiegelman BM. The unfolded protein response mediates adaptation to exercise in skeletal muscle through a PGC-1 /ATF6 complex. Cell Metab 13: 160-169, 2011.
46. Wu J, Rutkowski DT, Dubois M, Swathirajan J, Saunders T, Wang J, Song B, Yau GD, Kaufman RJ. ATF6alpha optimizes long-term endoplasmic reticulum function to protect cells from chronic stress. Dev Cell 13: 351-364, 2007.
47. Yamamoto K, Sato T, Matsui T, Sato M, Okada T, Yoshida H, Harada A, Mori K. Transcriptional induction of mammalian ER quality control proteins is mediated by single or combined action of ATF6alpha and XBP1. Dev Cell 13: 365-376, 2007.
48. Ye J, Rawson RB, Komuro R, Chen X, Dave UP, Prywes F, Brown MS, Goldstein JL. ER stress induces cleavage of membrane-bound ATF6 by the same proteases that process SREBPs. Mol Cell 6: 1355-1364, 2000.
49. Yoshida H, Haze K, Yanagi H, Yura T, Mori K. Identification of the cis-acting endoplasmic reticulum stress response element responsible for transcriptional induction of mammalian glucose-regulated proteins. Involvement of basic leucine zipper transcription factors. J Biol Chem 273: 33741-33749, 1998.
50. Zhang L, Lai E, Teodoro T, Volchuk A. GRP78, but not proteindisulfide isomerase, partially reverses hyperglycemia-induced inhibition of insulin synthesis and secretion in pancreatic beta-cells. J Biol Chem 284: 5289-98, 2009.