Mitogen-inducible gene 6 triggers apoptosis and exacerbates ER stress-induced β-cell death

Molecular Endocrinology

Volumn 27, Issue 1, 2013, Pages 162-171

  Chen, Yi Chun ^a   Scott Colvin, E ^a   Maier, Bernhard F ^a   Mirmira, Raghavendra G ^a   Fueger, Patrick T ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; CASPASE 3; HEAT SHOCK PROTEIN; MITOGEN INDUCIBLE GENE 6; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL DEATH; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; GLUCOSE TOLERANCE; IN VITRO STUDY; MALE; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PANCREAS ISLET BETA CELL; POLYSOME; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; UPREGULATION; WILD TYPE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CASPASE 3; CELL LINE, TUMOR; CELL PROLIFERATION; DIABETES MELLITUS, TYPE 2; ENDOPLASMIC RETICULUM STRESS; INSULIN-SECRETING CELLS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PROTEIN BIOSYNTHESIS; RATS; TRANSCRIPTIONAL ACTIVATION;

MUS;

EID: 84871743227     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2012-1174     Document Type: Article

References (61)

1. Yach D, Stuckler D, Brownell KD 2006 Epidemiologic and economic consequences of the global epidemics of obesity and diabetes. Nat Med 12:62-66
2. Muoio DM, Newgard CB 2008 Mechanisms of disease: molecular and metabolic mechanisms of insulin resistance and β-cell failure in type 2 diabetes. Nat Rev Mol Cell Biol 9:193-205
3. Fonseca SG, Gromada J, Urano F 2011 Endoplasmic reticulum stress and pancreatic β-cell death. Trends Endocrinol Metab 22: 266-274
4. Walter P, Ron D 2011 The unfolded protein response: from stress pathway to homeostatic regulation. Science 334:1081-1086
5. Oyadomari S, Koizumi A, Takeda K, Gotoh T, Akira S, Araki E, Mori M 2002 Targeted disruption of the Chop gene delays endoplasmic reticulum stress-mediated diabetes. J Clin Invest 109:525-532
6. Zinszner H, Kuroda M, Wang X, Batchvarova N, Lightfoot RT, Remotti H, Stevens JL, Ron D 1998 CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev 12:982-995
7. Urano F, Wang X, Bertolotti A, Zhang Y, Chung P, Harding HP, Ron D 2000 Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287:664-666
8. Nicoletti-Carvalho JE, Nogueira TC, Gorjão R, Bromati CR, Ya- manaka TS, Boschero AC, Velloso LA, Curi R, Anhê GF, Bordin S 2010 UPR-mediated TRIB3 expression correlates with reduced AKT phosphorylation and inability of interleukin 6 to overcome palmitate-induced apoptosis in RINm5F cells. J Endocrinol 206:183-193
9. Qian B, Wang H, Men X, Zhang W, Cai H, Xu S, Xu Y, Ye L, Wollheim CB, Lou J 2008 TRIB3 [corrected] is implicated in glu- cotoxicity- and endoplasmic reticulum-stress-induced [corrected] β-cell apoptosis. J Endocrinol 199:407-416
10. Humphrey RK, Newcomb CJ, Yu SM, Hao E, Yu D, Krajewski S, Du K, Jhala US 2010 Mixed lineage kinase-3 stabilizes and functionally cooperates with TRIBBLES-3 to compromise mitochondrial integrity in cytokine-induced death of pancreatic /3 cells. J Biol Chem 285:22426-22436
11. Wick M, Bürger C, Funk M, Müller R 1995 Identification of a novel mitogen-inducible gene (mig-6): regulation during G1 progression and differentiation. Exp Cell Res 219:527-535
12. Anastasi S, Fiorentino L, Fiorini M, Fraioli R, Sala G, Castellani L, Alemà S, Alimandi M, Segatto O 2003 Feedback inhibition by RALT controls signal output by the ErbB network. Oncogene 22: 4221-4234
13. Zhang X, Pickin KA, Bose R, Jura N, Cole PA, Kuriyan J 2007 Inhibition of the EGF receptor by binding of MIG6 to an activating kinase domain interface. Nature 450:741-744
14. Ying H, Zheng H, Scott K, Wiedemeyer R, Yan H, Lim C, Huang J, Dhakal S, Ivanova E, Xiao Y, Zhang H, Hu J, Stommel JM, Lee MA, Chen AJ, Paik JH, Segatto O, Brennan C, Elferink LA, Wang YA, Chin L, DePinho RA2010 Mig-6 controls EGFR trafficking and suppresses gliomagenesis. Proc Natl Acad Sci USA 107:6912-6917
15. Frosi Y, Anastasi S, Ballarò C, Varsano G, Castellani L, Maspero E, Polo S, Alemà S, Segatto O 2010 A two-tiered mechanism of EGFR inhibition by RALT/MIG6 via kinase suppression and receptor degradation. J Cell Biol 189:557-571
16. Makkinje A, Quinn DA, Chen A, Cadilla CL, Force T, Bonventre JV, Kyriakis JM 2000 Gene 33/Mig-6, a transcriptionally inducible adapter protein that binds GTP-Cdc42 and activates SAPK/JNK-a potential marker transcript for chronic pathologic conditions, such as diabetic nephropathy. Possible role in the response to persistent stress. J Biol Chem 275:17838-17847
17. Zhang YW, Su Y, Lanning N, Swiatek PJ, Bronson RT, Sigler R, Martin RW, Vande Woude GF 2005 Targeted disruption of Mig-6 in the mouse genome leads to early onset degenerative joint disease. Proc Natl Acad Sci USA 102:11740-11745
18. Xu D, Patten RD, Force T, Kyriakis JM 2006 Gene 33/RALT is induced by hypoxia in cardiomyocytes, where it promotes cell death by suppressing phosphatidylinositol 3-kinase and extracellular signal-regulated kinase survival signaling. Mol Cell Biol 26:5043-5054
19. Ma SF, Grigoryev DN, Taylor AD, Nonas S, Sammani S, Ye SQ, Garcia JG 2005 Bioinformatic identification of novel early stress response genes in rodent models of lung injury. Am J Physiol Lung Cell Mol Physiol 289:L468-L477
20. Fiorini M, Ballarò C, Sala G, Falcone G, Alemà S, Segatto O 2002 Expression of RALT, a feedback inhibitor of ErbB receptors, is subjected to an integrated transcriptional and post-translational control. Oncogene 21:6530-6539
21. Wek RC, Jiang HY, Anthony TG 2006 Coping with stress: eIF2 kinases and translational control. Biochem Soc Trans 34:7-11
22. Thomas JD, Johannes GJ 2007 Identification of mRNAs that continue to associate with polysomes during hypoxia. RNA 13:1116-1131
23. Warnakulasuriyarachchi D, Cerquozzi S, Cheung HH, Holcík M 2004 Translational induction of the inhibitor of apoptosis protein HIAP2 during endoplasmic reticulum stress attenuates cell death and is mediated via an inducible internal ribosome entry site element. J Biol Chem 279:17148-17157
24. Gotoh M, Maki T, Kiyoizumi T, Satomi S, Monaco AP 1985 An improved method for isolation of mouse pancreatic islets. Transplantation 40:437-438
25. Milburn Jr JL, Hirose H, Lee YH, Nagasawa Y, Ogawa A, Ohneda M, BeltrandelRio H, Newgard CB, Johnson JH, Unger RH 1995 Pancreatic β-cells in obesity. Evidence for induction of functional, morphologic, and metabolic abnormalities by increased long chain fatty acids. J Biol Chem 270:1295-1299
26. Naber SP, McDonald JM, Jarett L, McDaniel ML, Ludvigsen CW, Lacy PE 1980 Preliminary characterization of calcium binding in islet-cell plasma membranes. Diabetologia 19:439-444
27. Schisler JC, Fueger PT, Babu DA, Hohmeier HE, Tessem JS, Lu D, Becker TC, Naziruddin B, Levy M, Mirmira RG, Newgard CB 2008 Stimulation of human and rat islet β-cell proliferation with retention of function by the homeodomain transcription factor Nkx6.1. Mol Cell Biol 28:3465-3476
28. Becker TC, Noel RJ, Coats WS, Gomez-Foix AM, Alam T, Gerard RD, Newgard CB 1994 Use of recombinant adenovirus for metabolic engineering of mammalian cells. Methods Cell Biol 43(Pt A): 161-189
29. Luo J, Deng ZL, Luo X, Tang N, Song WX, Chen J, Sharff KA, Luu HH, Haydon RC, Kinzler KW, Vogelstein B, He TC 2007 A protocol for rapid generation of recombinant adenoviruses using the AdEasy system. Nat Protoc 2:1236-1247
30. Xu D, Makkinje A, Kyriakis JM 2005 Gene 33 is an endogenous inhibitor of epidermal growth factor (EGF) receptor signaling and mediates dexamethasone-induced suppression of EGF function. J Biol Chem 280:2924-2933
31. Bain JR, Schisler JC, Takeuchi K, Newgard CB, Becker TC 2004 An adenovirus vector for efficient RNA interference-mediated suppression of target genes in insulinoma cells and pancreatic islets of langerhans. Diabetes 53:2190-2194
32. Elbashir SM, Harborth J, Lendeckel W, Yalcin A, Weber K, Tuschl T 2001 Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411:494-498
33. Palam LR, Baird TD, Wek RC 2011 Phosphorylation of eIF2 facilitates ribosomal bypass of an inhibitory upstream ORF to enhance CHOP translation. J Biol Chem 286:10939-10949
34. Tersey SA, Nishiki Y, Templin AT, Cabrera SM, Stull ND, Colvin SC, Evans-Molina C, Rickus JL, Maier B, Mrmira RG 2012 Islet β-cell endoplasmic reticulum stress precedes the onset of type 1 diabetes in the nonobese diabetic mouse model. Diabetes 61:818-827
35. Maier B, Ogihara T, Trace AP, Tersey SA, Robbins RD, Chakrabarti SK, Nunemaker CS, Stull ND, Taylor CA, Thompson JE, Dondero RS, Lewis EC, Dinarello CA, Nadler JL, Mrmira RG 2010 The unique hypusine modification of eIF5A promotes islet /3 cell inflammation and dysfunction in mice. J Clin Invest 120:2156-2170
36. Zhang YW, Staal B, Su Y, Swiatek P, Zhao P, Cao B, Resau J, Sigler R, Bronson R, Vande Woude GF 2007 Evidence that MIG-6 is a tumor-suppressor gene. Oncogene 26:269-276
37. Ferby I, Reschke M, Kudlacek O, Knyazev P, Pantè G, Amann K, Sommergruber W, Kraut N, Ullrich A, Fässler R, Klein R 2006 Mig6 is a negative regulator of EGF receptor-mediated skin morphogenesis and tumor formation. Nat Med 12:568-573
38. Butler AE, Janson J, Bonner-Weir S, Ritzel R, Rizza RA, Butler PC 2003 β-cell deficit and increased β-cell apoptosis in humans with type 2 diabetes. Diabetes 52:102-110
39. Back SH, Kaufman RJ 2012 Endoplasmic reticulum stress and type 2 diabetes. Annu Rev Biochem 81:767-793
40. Saarikoski ST, Rivera SP, Hankinson O 2002 Mitogen-inducible gene 6 (MIG-6), adipophilin and tuftelin are inducible by hypoxia. FEBS Lett 530:186-190
41. van Laar T, Schouten T, van der Eb AJ, Terleth C 2001 Induction of the SAPK activator MIG-6 by the alkylating agent methyl meth-anesulfonate. Mol Carcinog 31:63-67
42. Lee KL, Makkinje A, ChAng LY, Kenney FT 1989 Molecular cloning and analysis of full-length cDNAs cognate to a rat gene under multi-hormonal control. Arch Biochem Biophys 269:106-113
43. von Roretz C, Di Marco S, Mazroui R, Gallouzi IE 2011 Turnover of AU-rich-containing mRNAs during stress: a matter of survival. Wiley Interdiscip Rev RNA 2:336-347
44. Ron D 2002 Translational control in the endoplasmic reticulum stress response. J Clin Invest 110:1383-1388
45. Holcik M, Sonenberg N 2005 Translational control in stress and apoptosis. Nat Rev Mol Cell Biol 6:318-327
46. Harding HP, Novoa I, Zhang Y, Zeng H, Wek R, Schapira M, Ron D 2000 Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol Cell 6:1099-1108
47. Brewer JW, Diehl JA 2000 PERK mediates cell-cycle exit during the mammalian unfolded protein response. Proc Natl Acad Sci USA 97:12625-12630
48. Lee KL, Isham KR, Stringfellow L, Rothrock R, Kenney FT 1985 Molecular cloning of cDNAs cognate to genes sensitive to hormonal control in rat liver. J Biol Chem 260:16433-16438
49. Pante G, Thompson J, Lamballe F, Iwata T, Ferby I, Barr FA, Davies AM, Maina F, Klein R 2005 Mitogen-inducible gene 6 is an endogenous inhibitor of HGF/Met-induced cell migration and neu-rite growth. J Cell Biol 171:337-348
50. Nagashima T, Ushikoshi-Nakayama R, Suenaga A, Ide K, Yumoto N, Naruo Y, Takahashi K, Saeki Y, Taiji M, Tanaka H, Tsai SF, Hatakeyama M 2009 Mutation of epidermal growth factor receptor is associated with MIG6 expression. FEBS J 276:5239-5251
51. Fernandez J, Yaman I, Sarnow P, Snider MD, Hatzoglou M 2002 Regulation of internal ribosomal entry site-mediated translation by phosphorylation of the translation initiation factor eIF2a. J Biol Chem 277:19198-19205
52. Kim TH, Franco HL, Jung SY, Qin J, Broaddus RR, Lydon JP, Jeong JW 2010 The synergistic effect of Mig-6 and Pten ablation on endometrial cancer development and progression. Oncogene 29: 3770-3780
53. Anastasi S, Sala G, Huiping C, Caprini E, Russo G, Iacovelli S, Lucini F, Ingvarsson S, Segatto O 2005 Loss of RALT/MIG-6 expression in ERBB2-amplified breast carcinomas enhances ErbB-2 oncogenic potency and favors resistance to Herceptin. Oncogene 24:4540-4548
54. Reschke M, Ferby I, Stepniak E, Seitzer N, Horst D, Wagner EF, Ullrich A 2010 Mitogen-inducible gene-6 is a negative regulator of epidermal growth factor receptor signaling in hepatocytes and human hepatocellular carcinoma. Hepatology 51:1383-1390
55. Patil C, Walter P 2001 Intracellular signaling from the endoplasmic reticulum to the nucleus: the unfolded protein response in yeast and mammals. Curr Opin Cell Biol 13:349-355
56. Srinivasan S, Ohsugi M, Liu Z, Fatrai S, Bernal-Mizrachi E, Per-mutt MA 2005 Endoplasmic reticulum stress-induced apoptosis is partly mediated by reduced insulin signaling through phosphatidyl-inositol 3-kinase/Akt and increased glycogen synthase kinase-3/3 in mouse insulinoma cells. Diabetes 54:968-975
57. Hollien J, Lin JH, Li H, Stevens N, Walter P, Weissman JS 2009 Regulated Ire1-dependent decay of messenger RNAs in mammalian cells. J Cell Biol 186:323-331
58. Lipson KL, Ghosh R, Urano F 2008 The role of IRE1a in the degradation of insulin mRNA in pancreatic β-cells. PLoS One 3:e1648
59. Pirot P, Naamane N, Libert F, Magnusson NE, Ørntoft TF, Car-dozo AK, Eizirik DL 2007 Global profiling of genes modified by endoplasmic reticulum stress in pancreatic /3 cells reveals the early degradation of insulin mRNAs. Diabetologia 50:1006-1014
60. Harding HP, Zhang Y, Bertolotti A, Zeng H, Ron D 2000 Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol Cell 5:897-904
61. Vattem KM, Wek RC 2004 Reinitiation involving upstream ORFs regulates ATF4 mRNA translation in mammalian cells. Proc Natl Acad Sci USA 101:11269-11274