Autophagy deficiency in beta cells leads to compromised unfolded protein response and progression from obesity to diabetes in mice

Diabetologia

Volumn 55, Issue 2, 2012, Pages 392-403

  Quan, W ^a   Hur, K Y ^a   Lim, Y ^a   Oh, S H ^a   Lee, J C ^a   Kim, K H ^a   Kim, G H ^b   Kim, S W ^b   Kim, H L ^c   Lee, M K ^a   Kim, K W ^a   Kim, J ^c   Komatsu, M ^d   Lee, M S ^a,e  

^a Sungkyunkwan University   (South Korea)

^b University of Ulsan College of Medicine   (South Korea)

^c The Catholic University of Korea   (South Korea)

^d TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

^e Samsung Medical Center   (South Korea)

Author keywords

Autophagy; Diabetes mellitus; Endoplasmic reticulum stress; Pancreatic beta cell; Unfolded protein response

Indexed keywords

PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN P85; PROTEIN P85 ALPHA; PROTEIN P85 BETA; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPHAGY; CELL DEATH; CONTROLLED STUDY; DIABETES MELLITUS; DISEASE COURSE; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION PROFILING; HYPERGLYCEMIA; IN VIVO STUDY; MOUSE; NONHUMAN; OBESITY; PANCREAS ISLET BETA CELL; PANCREAS ISLET CELL FUNCTION; PRIORITY JOURNAL; PROTEIN DEGRADATION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UNFOLDED PROTEIN RESPONSE;

ANIMALS; APOPTOSIS; AUTOPHAGY; CROSSES, GENETIC; DISEASE PROGRESSION; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOPLASMIC RETICULUM; GENETIC PREDISPOSITION TO DISEASE; GENOTYPE; INSULIN-SECRETING CELLS; LIPIDS; MICE; MICE, OBESE; MICROSCOPY, FLUORESCENCE; OBESITY; PHOSPHATIDYLINOSITOL 3-KINASES; RATS; UNFOLDED PROTEIN RESPONSE;

EID: 84856764175     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-011-2350-y     Document Type: Article

References (36)

1. DJ Klionsky SD Emr 2000 Autophagy as a regulated pathway of cellular degradation Science 290 1717 1721 11099404 10.1126/science.290.5497.1717 1:CAS:528:DC%2BD3cXovVOitbw%3D (Pubitemid 32004796)
2. M Komatsu S Waguri T Ueno, et al. 2005 Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice J Cell Biol 169 425 434 15866887 10.1083/jcb.200412022 1:CAS:528:DC%2BD2MXktFOjsLk%3D (Pubitemid 40686693)
3. K Matsunaga E Morita T Saitoh, et al. 2009 Autophagy requires endoplasmic reticulum targeting of the PI3-kinase complex via Atg14L J Cell Biol 190 511 521 10.1083/jcb.200911141
4. DC Rubinsztein 2006 The roles of intracellular protein-degradation pathways in neurodegeneration Nature 443 780 786 17051204 10.1038/nature05291 1:CAS:528:DC%2BD28XhtVyktbbN (Pubitemid 44622682)
5. Y Kouroku E Fujita I Tanida, et al. 2007 ER stress (PERK/eIF2alpha phosphorylation) mediates the polyglutamine-induced LC3 conversion, an essential step for autophagy formation Cell Death Differ 14 230 239 16794605 10.1038/sj.cdd.4401984 1:CAS:528:DC%2BD2sXkslCitw%3D%3D (Pubitemid 46092226)
6. M Ogata H S-i A Saito, et al. 2006 Autophagy is activated for cell survival after endoplasmic reticulum stress Mol Cell Biol 26 9220 9231 17030611 10.1128/MCB.01453-06 1:CAS:528:DC%2BD28XhtlemsLvI (Pubitemid 44904418)
7. T Yorimitsu U Nair Z Yang DJ Klionsky 2006 Endoplasmic reticulum stress triggers autophagy J Biol Chem 281 30299 30304 16901900 10.1074/jbc.M607007200 1:CAS:528:DC%2BD28XhtVahsbjE (Pubitemid 44537037)
8. D Scheuner D Vander Mierde B Song, et al. 2005 Control of mRNA translation preserves endoplasmic reticulum function in beta cells and maintains glucose homeostasis Nat Med 11 757 764 15980866 10.1038/nm1259 1:CAS:528:DC%2BD2MXmt1ajurw%3D (Pubitemid 41021208)
9. DR Laybutt AM Preston MC Akerfeldt, et al. 2007 Endoplasmic reticulum stress contributes to beta cell apoptosis in type 2 diabetes Diabetologia 50 752 763 17268797 10.1007/s00125-006-0590-z 1:CAS:528:DC%2BD2sXitlOntL0%3D (Pubitemid 46355827)
10. HS Jung KW Chung JW Kim, et al. 2008 Loss of autophagy diminishes pancreatic β-cell mass and function with resultant hyperglycemia Cell Metab 8 318 324 18840362 10.1016/j.cmet.2008.08.013 1:CAS:528:DC%2BD1cXht1Cit77O
11. M Masini M Bugliani R Lupi, et al. 2009 Autophagy in human type 2 diabetes pancreatic beta cells Diabetologia 52 1083 1086 19367387 10.1007/s00125-009-1347-2 1:CAS:528:DC%2BD1MXlt1GqtLc%3D
12. N Mizushima A Yamamoto M Matsui T Yoshimori Y Ohsumi 2004 In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker Mol Biol Cell 15 1101 1111 14699058 10.1091/mbc.E03-09-0704 1:CAS:528:DC%2BD2cXitlGhu7g%3D (Pubitemid 38316219)
13. SH Back D Scheuner J Han, et al. 2009 Translation attenuation through eIF2alpha phosphorylation prevents oxidative stress and maintains the differentiated state in beta cells Cell Metab 10 13 26 19583950 10.1016/j.cmet.2009.06.002 1:CAS:528:DC%2BD1MXhsVChsL3N
14. YH Kim S Kim KA Kim, et al. 1999 Apoptosis of pancreatic beta-cells detected in accelerated diabetes of NOD mice: no role of Fas-Fas ligand interaction in autoimmune diabetes Eur J Immunol 29 455 465 10064061 10.1002/(SICI)1521-4141(199902)29:02<455::AID-IMMU455>3.0.CO;2-A 1:CAS:528:DyaK1MXhsVanu7s%3D (Pubitemid 29078506)
15. I Chang N Cho S Kim, et al. 2004 Role of calcium in pancreatic islet cell death by IFN-gamma/TNF-alpha J Immunol 172 7008 7014 15153522 1:CAS:528:DC%2BD2cXktFSktbc%3D (Pubitemid 38669142)
16. MS Han SY Park K Shinzawa, et al. 2008 Lysophosphatidylcholine as a death effector in lipoapoptosis of hepatocytes J Lipid Res 49 84 97 17951222 10.1194/jlr.M700184-JLR200 1:CAS:528:DC%2BD1cXktVWqtQ%3D%3D
17. N Hosokawa Y Hara N Mizushima 2006 Generation of cell lines with tetracycline-regulated autophagy and a role for autophagy in controlling cell size FEBS Lett 580 2623 2629 16647067 10.1016/j.febslet.2006.04.008 1:CAS:528:DC%2BD28XksFaqsr4%3D
18. SW Park Y Zhou J Lee, et al. 2010 The regulatory subunits of PI3K, p85α and p85β, interact with XBP-1 and increase its nuclear translocation Nat Med 16 429 437 20348926 10.1038/nm.2099 1:CAS:528: DC%2BC3cXjvFWjs7c%3D
19. JN Winnay J Boucher MA Mori K Ueki CR Kahn 2010 A regulatory subunit of phosphoinositide 3-kinase increases the nuclear accumulation of X-box-binding protein-1 to modulate the unfolded protein response Nat Med 16 438 445 20348923 10.1038/nm.2121 1:CAS:528:DC%2BC3cXjvFWjs70%3D
20. PI Merksamer A Trusina FR Papa 2008 Real-time redox measurements during endoplasmic reticulum stress reveal interlinked protein folding functions Cell 135 933 947 19026441 10.1016/j.cell.2008.10.011 1:CAS:528:DC%2BD1cXhsV2jtrzN
21. 2+ depletion J Biol Chem 268 12003 12009 8505325 1:CAS:528:DyaK3sXltFSntrc%3D
22. DA Cunha P Hekerman L Ladrière, et al. 2008 Initiation and execution of lipotoxic ER stress in pancreatic beta-cells J Cell Sci 121 2308 2318 18559892 10.1242/jcs.026062 1:CAS:528:DC%2BD1cXpvVKqsbg%3D
23. JY Lee M Ristow X Lin MF White MA Magnuson L Hennighausen 2006 RIP-Cre revisited, evidence for impairments of pancreatic beta-cell function J Biol Chem 281 2649 2653 16326700 10.1074/jbc.M512373200 1:CAS:528:DC%2BD28XovVeitA%3D%3D (Pubitemid 43845726)
24. K Nakahira JA Haspel VAK Rathinam, et al. 2011 Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome Nat Immunol 12 222 231 21151103 10.1038/ni.1980 1:CAS:528:DC%2BC3cXhsFGgtrzE
25. DJ Klionsky H Abeliovich P Agostinis, et al. 2008 Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes Autophagy 4 151 175 18188003 1:CAS:528:DC%2BD1cXksFGrtLg%3D (Pubitemid 351231180)
26. R Singh S Kaushik Y Wang, et al. 2009 Autophagy regulates lipid metabolism Nature 458 1131 1135 19339967 10.1038/nature07976 1:CAS:528:DC%2BD1MXjvV2ks7s%3D
27. A Nakai O Yamaguchi T Takeda, et al. 2007 The role of autophagy in cardiomyocytes in the basal state and in response to hemodynamic stress Nat Med 13 619 624 17450150 10.1038/nm1574 1:CAS:528:DC%2BD2sXkvVOgsr4%3D (Pubitemid 46828485)
28. L Yang P Li S Fu ES Calay GS Hotamisligil 2010 Defective hepatic autophagy in obesity promotes ER stress and causes insulin resistance Cell Metab 11 467 478 20519119 10.1016/j.cmet.2010.04.005 1:CAS:528:DC%2BC3cXnsFyitrs%3D
29. E Gomez ML Powell A Bevington TP Herbert 2008 A decrease in cellular energy status stimulates PERK-dependent eIF2alpha phosphorylation and regulates protein synthesis in pancreatic beta-cells Biochem J 410 485 493 18052927 10.1042/BJ20071367 1:CAS:528:DC%2BD1cXisVWgtrc%3D (Pubitemid 351429019)
30. S Kim I Millet HS Kim, et al. 2007 NF-kappa B prevents beta cell death and autoimmune diabetes in NOD mice Proc Natl Acad Sci USA 104 1913 1918 17267600 10.1073/pnas.0610690104 1:CAS:528:DC%2BD2sXitVejs7s%3D (Pubitemid 46239878)
31. C Ebato T Uchida M Arakawa, et al. 2008 Autophagy is important in islet homeostasis and compensatory increase of beta cell mass in response to high-fat diet Cell Metab 8 325 332 18840363 10.1016/j.cmet.2008.08.009 1:CAS:528:DC%2BD1cXht1Cit77J
32. K Lemaire RF Moura M Granvik, et al. 2011 Ubiquitin fold modifier 1 (UFM1) and its target UFBP1 protect pancreatic beta cells from ER stress-induced apoptosis PLoS One 6 e18517 21494687 10.1371/journal.pone.0018517 1:CAS:528:DC%2BC3MXkvFKjtbw%3D
33. R Mathew CM Karp B Beaudoin, et al. 2009 Autophagy suppresses tumorigenesis through elimination of p62 Cell 137 1062 1075 19524509 10.1016/j.cell.2009.03.048 1:CAS:528:DC%2BD1MXps1eiu74%3D
34. H Koga S Kaushik AM Cuervo 2010 Altered lipid content inhibits autophagic vesicular fusion FASEB J 24 3052 3065 20375270 10.1096/fj.09-144519 1:CAS:528:DC%2BC3cXhtVeitr%2FE
35. M Shibata K Yoshimura H Tamura, et al. 2010 LC3, a microtubule-associated protein1A/B light chain3, is involved in cytoplasmic lipid droplet formation Biochem Biophys Res Commun 393 274 279 20132792 10.1016/j.bbrc.2010.01.121 1:CAS:528:DC%2BC3cXjtVClur0%3D
36. HM Ni A Bockus AL Wozniak, et al. 2011 Dissecting the dynamic turnover of GFP-LC3 in the autolysosome Autophagy 7 1 17 10.4161/auto.7.2.14181