Autophagy is a major regulator of beta cell insulin homeostasis

Diabetologia

Volumn 59, Issue 7, 2016, Pages 1480-1491

  Riahi, Yael ^a   Wikstrom, Jakob D ^a,b   Bachar Wikstrom, Etty ^a   Polin, Nava ^a   Zucker, Hava ^a   Lee, Myung Shik ^c   Quan, Wenying ^d   Haataja, Leena ^e   Liu, Ming ^e   Arvan, Peter ^e   Cerasi, Erol ^a   Leibowitz, Gil ^a  

^a HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

^b KAROLINSKA INSTITUTE   (Sweden)

^c Yonsei University College of Medicine   (South Korea)

^d Sungkyunkwan University School of Medicine   (South Korea)

^e UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Autophagy; Beta cells; Insulin secretion; Lysosome; Proinsulin; Proteasome; Protein degradation

Indexed keywords

AUTOPHAGY RELATED PROTEIN; BAFILOMYCIN A1; CELL PROTEIN; CHROMOGRANIN A; GLUCOSE; HORMONE PRECURSOR; INSULIN; PROINSULIN; PROTEIN AGGREGATE; SQSTM1 PROTEIN; UNCLASSIFIED DRUG; ATG7 PROTEIN, MOUSE; AUTOPHAGY RELATED PROTEIN 7;

ANIMAL CELL; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENDOPLASMIC RETICULUM; ENZYME LINKED IMMUNOSORBENT ASSAY; HOMEOSTASIS; HORMONAL REGULATION; IN VIVO STUDY; INSULIN RELEASE; INSULIN SYNTHESIS; LYSOSOME; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FOLDING; RADIOIMMUNOASSAY; REGULATORY MECHANISM; STIMULUS RESPONSE; ANIMAL; C57BL MOUSE; CELL LINE; GENETICS; HUMAN; KNOCKOUT MOUSE; METABOLISM; OXYGEN CONSUMPTION; PHYSIOLOGY; RNA INTERFERENCE; WESTERN BLOTTING;

ANIMALS; AUTOPHAGY; AUTOPHAGY-RELATED PROTEIN 7; BLOTTING, WESTERN; CELL LINE; HOMEOSTASIS; HUMANS; INSULIN; INSULIN-SECRETING CELLS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROSCOPY, ELECTRON; OXYGEN CONSUMPTION; RNA INTERFERENCE;

EID: 84975175105     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-016-3868-9     Document Type: Article

References (34)

1. Orci L, Ravazzola M, Amherdt M et al (1984) Insulin, not C-peptide (proinsulin), is present in crinophagic bodies of the pancreatic B cell. J Cell Biol 98:222–228
2. Goginashvili A, Zhang Z, Erbs E et al (2015) Insulin granules. Insulin secretory granules control autophagy in pancreatic beta cells. Science 347:878–882
3. Schuit FC, In't Veld PA, Pipeleers DG (1988) Glucose stimulates proinsulin biosynthesis by a dose-dependent recruitment of pancreatic beta cells. Proc Natl Acad Sci U S A 85:3865–3869
4. Brodsky JL (2012) Cleaning up: ER-associated degradation to the rescue. Cell 151:1163–1167
5. Day KJ, Staehelin LA, Glick BS (2013) A three-stage model of Golgi structure and function. Histochem Cell Biol 140:239–249
6. Cecconi F, Levine B (2008) The role of autophagy in mammalian development: cell makeover rather than cell death. Dev Cell 15:344–357
7. Klionsky DJ (2007) Autophagy: from phenomenology to molecular understanding in less than a decade. Nat Rev Mol Cell Biol 8:931–937
8. Levine B, Mizushima N, Virgin HW (2011) Autophagy in immunity and inflammation. Nature 469:323–335
9. Green DR, Levine B (2014) To be or not to be? How selective autophagy and cell death govern cell fate. Cell 157:65–75
10. Ebato C, Uchida T, Arakawa M 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
11. Jung HS, Chung KW, Won Kim J et al (2008) Loss of autophagy diminishes pancreatic beta cell mass and function with resultant hyperglycemia. Cell Metab 8:318–324
12. Stienstra R, Haim Y, Riahi Y, Netea M, Rudich A, Leibowitz G (2014) Autophagy in adipose tissue and the beta cell: implications for obesity and diabetes. Diabetologia 57:1505–1516
13. Masini M, Bugliani M, Lupi R et al (2009) Autophagy in human type 2 diabetes pancreatic beta cells. Diabetologia 52:1083–1086
14. Quan W, Hur KY, Lim Y et al (2012) Autophagy deficiency in beta cells leads to compromised unfolded protein response and progression from obesity to diabetes in mice. Diabetologia 55:392–403
15. Shaked M, Ketzniel-Gilad M, Cerasi E et al (2011) AMP-activated protein kinase (AMPK) mediates nutrient regulation of thioredoxin-interacting protein (TXNIP) in pancreatic beta-cells. PLoS One 6:e28804
16. Stålberg P, Wang S, Larsson C et al (1999) Suppression of the neoplastic phenotype by transfection of phospholipase C β 3 to neuroendocrine tumor cells. FEBS Lett 450:210–216
17. Falcon-Perez JM, Nazarian R, Sabatti C, Dell'Angelica EC (2005) Distribution and dynamics of Lamp1-containing endocytic organelles in fibroblasts deficient in BLOC-3. J Cell Sci 118:5243–5255
18. Bjorkoy G, Lamark T, Brech A et al (2005) p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J Cell Biol 171:603–614
19. Goedhart J, von Stetten D, Noirclerc-Savoye M et al (2012) Structure-guided evolution of cyan fluorescent proteins towards a quantum yield of 93%. Nat Commun 3:751
20. Rajan S, Eames SC, Park SY et al (2010) In vitro processing and secretion of mutant insulin proteins that cause permanent neonatal diabetes. Am J Physiol Endocrinol Metab 298:E403–E410
21. Wright J, Wang X, Haataja L et al (2013) Dominant protein interactions that influence the pathogenesis of conformational diseases. J Clin Invest 123:3124–3134
22. Wikstrom JD, Sereda SB, Stiles L et al (2012) A novel high-throughput assay for islet respiration reveals uncoupling of rodent and human islets. PLoS ONE 7:e33023
23. Bachar-Wikstrom E, Wikstrom JD, Ariav Y et al (2013) Stimulation of autophagy improves endoplasmic reticulum stress-induced diabetes. Diabetes 62:1227–1237
24. Kienzle C, von Blume J (2014) Secretory cargo sorting at the trans-Golgi network. Trends Cell Biol 24:584–593
25. Winkler H, Fischer-Colbrie R (1992) The chromogranins A and B: the first 25 years and future perspectives. Neuroscience 49:497–528
26. Barbosa JA, Gill BM, Takiyyuddin MA, O'Connor DT (1991) Chromogranin A: posttranslational modifications in secretory granules. Endocrinology 128:174–190
27. Preston AM, Gurisik E, Bartley C, Laybutt DR, Biden TJ (2009) Reduced endoplasmic reticulum (ER)-to-Golgi protein trafficking contributes to ER stress in lipotoxic mouse beta cells by promoting protein overload. Diabetologia 52:2369–2373
28. Zhang X, Yuan Q, Tang W, Gu J, Osei K, Wang J (2011) Substrate-favored lysosomal and proteasomal pathways participate in the normal balance control of insulin precursor maturation and disposal in beta-cells. PLoS ONE 6:e27647
29. Pearson GL, Mellett N, Chu KY et al (2014) Lysosomal acid lipase and lipophagy are constitutive negative regulators of glucose-stimulated insulin secretion from pancreatic beta cells. Diabetologia 57:129–139
30. Liu M, Hodish I, Rhodes CJ, Arvan P (2007) Proinsulin maturation, misfolding, and proteotoxicity. Proc Natl Acad Sci U S A 104:15841–15846
31. Zuber C, Fan JY, Guhl B, Roth J (2004) Misfolded proinsulin accumulates in expanded pre-Golgi intermediates and endoplasmic reticulum subdomains in pancreatic beta cells of Akita mice. FASEB J 18:917–919
32. Rivera JF, Costes S, Gurlo T, Glabe CG, Butler PC (2014) Autophagy defends pancreatic beta cells from human islet amyloid polypeptide-induced toxicity. J Clin Invest 124:3489–3500
33. Shigihara N, Fukunaka A, Hara A et al (2014) Human IAPP-induced pancreatic beta cell toxicity and its regulation by autophagy. J Clin Invest 124:3634–3644
34. Kim J, Cheon H, Jeong YT et al (2014) Amyloidogenic peptide oligomer accumulation in autophagy-deficient beta cells induces diabetes. J Clin Invest 124:3311–3324