β-cell metabolic alterations under chronic nutrient overload in rat and human islets

Islets

Volumn 4, Issue 6, 2012, Pages 379-392

  Vernier, Stephanie ^a   Chiu, Angela ^a   Schober, Joseph ^a   Weber, Theresa ^a   Nguyen, Phuong ^a   Luer, Mark ^a   McPherson, Timothy ^a   Wanda, Paul E ^a   Marshall, Connie A ^b   Rohatgi, Nidhi ^b   McDaniel, Michael L ^b   Greenberg, Andrew S ^c   Kwon, Guim ^a  

^a SOUTHERN ILLINOIS UNIVERSITY EDWARDSVILLE   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c TUFTS UNIVERSITY   (United States)

Author keywords

ADRP; Human islets; Insulin; Lipid droplets; MTORC1; Nutrient overload; Rapamycin; Time lapse studies

Indexed keywords

ADIPOPHILIN; FAT DROPLET; GLUCOSE; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; OLEIC ACID; PALMITIC ACID; RAPAMYCIN; TRIACYLGLYCEROL;

ADULT; ANIMAL TISSUE; ARTICLE; CELL EXPANSION; CELL GROWTH; CULTURE MEDIUM; DNA SYNTHESIS; FEMALE; HUMAN; HUMAN TISSUE; INSULIN RELEASE; INSULIN SYNTHESIS; LIPID STORAGE; MALE; NONHUMAN; PANCREAS ISLET ALPHA CELL; PANCREAS ISLET BETA CELL; PROTEIN EXPRESSION; RAT; UPREGULATION;

ADRP; HUMAN ISLETS; INSULIN; LIPID DROPLETS; MTORC1; NUTRIENT OVERLOAD; RAPAMYCIN; TIME LAPSE STUDIES;

ANIMALS; BLOTTING, WESTERN; DIABETES MELLITUS, TYPE 2; FATTY ACIDS, NONESTERIFIED; GLUCOSE; HUMANS; IMMUNOHISTOCHEMISTRY; INSULIN-SECRETING CELLS; MALE; MEMBRANE PROTEINS; MICROSCOPY, PHASE-CONTRAST; PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; SIROLIMUS; TRIGLYCERIDES;

EID: 84876262194     PISSN: 19382014     EISSN: 19382022     Source Type: Journal    
DOI: 10.4161/isl.22720     Document Type: Article

References (42)

1. Unger RH, Zhou YT. Lipotoxicity of beta-cells in obesity and in other causes of fatty acid spillover. Diabetes 2001; 50(Suppl 1):S118-21; PMID:11272168; http://dx.doi.org/10.2337/diabetes.50.2007.S118
2. Unger RH. Minireview: weapons of lean body mass destruction: the role of ectopic lipids in the metabolic syndrome. Endocrinology 2003; 144:5159-65; PMID:12960011; http://dx.doi.org/10.1210/en.2003-0870
3. Raz I, Eldor R, Cernea S, Shafrir E. Diabetes: insulin resistance and derangements in lipid metabolism. Cure through intervention in fat transport and storage. Diabetes Metab Res Rev 2005; 21:3-14; PMID:15386813; http://dx.doi.org/10.1002/dmrr.493
4. Milburn JL Jr., Hirose H, Lee YH, Nagasawa Y, Ogawa A, Ohneda M, et al. Pancreatic beta-cells in obesity. Evidence for induction of functional, morphologic, and metabolic abnormalities by increased long chain fatty acids. J Biol Chem 1995; 270:1295-9; PMID:7836394
5. Sone H, Kagawa Y. Pancreatic beta cell senescence contributes to the pathogenesis of type 2 diabetes in high-fat diet-induced diabetic mice. Diabetologia 2005; 48:58-67; PMID:15624098; http://dx.doi.org/10.1007/s00125- 004-1605-2
6. Londos C, Brasaemle DL, Schultz CJ, Segrest JP, Kimmel AR. Perilipins, ADRP, and other proteins that associate with intracellular neutral lipid droplets in animal cells. Semin Cell Dev Biol 1999; 10:51-8; PMID:10355028; http://dx.doi.org/10.1006/scdb.1998.0275
7. Hickenbottom SJ, Kimmel AR, Londos C, Hurley JH. Structure of a lipid droplet protein; the PAT family member TIP47. Structure 2004; 12:1199-207; PMID:15242596; http://dx.doi.org/10.1016/j.str.2004.04.021
8. Londos C, Sztalryd C, Tansey JT, Kimmel AR. Role of PAT proteins in lipid metabolism. Biochimie 2005; 87:45-9; PMID:15733736; http://dx.doi.org/10.1016/ j.biochi.2004.12.010
9. Borg J, Klint C, Wierup N, Ström K, Larsson S, Sundler F, et al. Perilipin is present in islets of Langerhans and protects against lipotoxicity when overexpressed in the beta-cell line INS-1. Endocrinology 2009; 150:3049-57; PMID:19299455; http://dx.doi.org/10.1210/en.2008-0913
10. Faleck DM, Ali K, Roat R, Graham MJ, Crooke RM, Battisti R, et al. Adipose differentiation-related protein regulates lipids and insulin in pancreatic islets. Am J Physiol Endocrinol Metab 2010; 299:E249-57; PMID:20484013.
11. Coleman DL. Diabetes-obesity syndromes in mice. Diabetes 1982; 31(Suppl 1 Pt 2):1-6; PMID:7160533
12. Hull RL, Kodama K, Utzschneider KM, Carr DB, Prigeon RL, Kahn SE. Dietary-fat-induced obesity in mice results in beta cell hyperplasia but not increased insulin release: evidence for specificity of impaired beta cell adaptation. Diabetologia 2005; 48:1350-8; PMID:15937671; http://dx.doi.org/10. 1007/s00125-005-1772-9
13. Bonner-Weir S, Deery D, Leahy JL, Weir GC. Compensatory growth of pancreatic beta-cells in adult rats after short-Term glucose infusion. Diabetes 1989; 38:49-53; PMID:2642434; http://dx.doi.org/10.2337/diabetes.38.1.49
14. Steil GM, Trivedi N, Jonas JC, Hasenkamp WM, Sharma A, Bonner-Weir S, et al. Adaptation of beta-cell mass to substrate oversupply: enhanced function with normal gene expression. Am J Physiol Endocrinol Metab 2001; 280:E788-96; PMID:11287362
15. Fontés G, Zarrouki B, Hagman DK, Latour MG, Semache M, Roskens V, et al. Glucolipotoxicity age-dependently impairs beta cell function in rats despite a marked increase in beta cell mass. Diabetologia 2010; 53:2369-79; PMID:20628728; http://dx.doi.org/10.1007/s00125-010-1850-5
16. Delghingaro-Augusto V, Nolan CJ, Gupta D, Jetton TL, Latour MG, Peshavaria M, et al. Islet beta cell failure in the 60% pancreatectomised obese hyperlipidaemic Zucker fatty rat: severe dysfunction with altered glycerolipid metabolism without steatosis or a falling beta cell mass. Diabetologia 2009; 52:1122-32; PMID:19294363; http://dx.doi.org/10.1007/s00125-009-1317-8
17. Kargar C, Ktorza A. Anatomical versus functional beta-cell mass in experimental diabetes. Diabetes Obes Metab 2008; 10(Suppl 4):43-53; PMID:18834432; http://dx.doi.org/10.1111/j.1463-1326.2008.00940.x
18. McDaniel ML, Marshall CA, Pappan KL, Kwon G. Metabolic and autocrine regulation of the mammalian target of rapamycin by pancreatic beta-cells. Diabetes 2002; 51:2877-85; PMID:12351422; http://dx.doi.org/10.2337/diabetes.51. 10.2877
19. Harris TE, Lawrence JC, Jr. TOR signaling. Sci STKE 2003; 2003:re15
20. Hay N, Sonenberg N. Upstream and downstream of mTOR. Genes Dev 2004; 18:1926-45; PMID:15314020; http://dx.doi.org/10.1101/gad.1212704
21. Fingar DC, Blenis J. Target of rapamycin (TOR): an integrator of nutrient and growth factor signals and coordinator of cell growth and cell cycle progression. Oncogene 2004; 23:3151-71; PMID:15094765; http://dx.doi.org/10. 1038/sj.onc.1207542
22. Pende M, Kozma SC, Jaquet M, Oorschot V, Burcelin R, Le Marchand-Brustel Y, et al. Hypoinsulinaemia, glucose intolerance and diminished beta-cell size in S6K1-deficient mice. Nature 2000; 408:994-7; PMID:11140689; http://dx.doi.org/10.1038/35050135
23. Lee CH, Inoki K, Guan KL. mTOR pathway as a target in tissue hypertrophy. Annu Rev Pharmacol Toxicol 2007; 47:443-67; PMID:16968213; http://dx.doi.org/ 10.1146/annurev.pharmtox.47.120505.105359
24. Wang X, Beugnet A, Murakami M, Yamanaka S, Proud CG. Distinct signaling events downstream of mTOR cooperate to mediate the effects of amino acids and insulin on initiation factor 4E-binding proteins. Mol Cell Biol 2005; 25:2558-72; PMID:15767663; http://dx.doi.org/10.1128/MCB.25.7.2558-2572.2005
25. Um SH, D'Alessio D, Thomas G. Nutrient overload, insulin resistance, and ribosomal protein S6 kinase 1, S6K1. Cell Metab 2006; 3:393-402; PMID:16753575; http://dx.doi.org/10.1016/j.cmet.2006.05.003
26. Patti ME, Kahn BB. Nutrient sensor links obesity with diabetes risk. Nat Med 2004; 10:1049-50; PMID:15459705; http://dx.doi.org/10.1038/nm1004-1049
27. Liu H, Remedi MS, Pappan KL, Kwon G, Rohatgi N, Marshall CA, et al. Glycogen synthase kinase-3 and mammalian target of rapamycin pathways contribute to DNA synthesis, cell cycle progression, and proliferation in human islets. Diabetes 2009; 58:663-72; PMID:19073772; http://dx.doi.org/10.2337/db07-1208
28. Balcazar N, Sathyamurthy A, Elghazi L, Gould A, Weiss A, Shiojima I, et al. mTORC1 activation regulates beta-cell mass and proliferation by modulation of cyclin D2 synthesis and stability. J Biol Chem 2009; 284:7832-42; PMID:19144649; http://dx.doi.org/10.1074/jbc.M807458200
29. Fu A, Ng AC, Depatie C, Wijesekara N, He Y, Wang GS, et al. Loss of Lkb1 in adult beta cells increases beta cell mass and enhances glucose tolerance in mice. Cell Metab 2009; 10:285-95; PMID:19808021; http://dx.doi.org/10.1016/j. cmet.2009.08.008
30. Rachdi L, Balcazar N, Osorio-Duque F, Elghazi L, Weiss A, Gould A, et al. Disruption of Tsc2 in pancreatic beta cells induces beta cell mass expansion and improved glucose tolerance in a TORC1-dependent manner. Proc Natl Acad Sci U S A 2008; 105:9250-5; PMID:18587048; http://dx.doi.org/10.1073/pnas.0803047105
31. Yoon KH, Ko SH, Cho JH, Lee JM, Ahn YB, Song KH, et al. Selective beta-cell loss and alpha-cell expansion in patients with type 2 diabetes mellitus in Korea. J Clin Endocrinol Metab 2003; 88:2300-8; PMID:12727989; http://dx.doi.org/10.1210/jc.2002-020735
32. Gromada J, Franklin I, Wollheim CB. Alpha-cells of the endocrine pancreas: 35 years of research but the enigma remains. Endocr Rev 2007; 28:84-116; PMID:17261637; http://dx.doi.org/10.1210/er.2006-0007
33. Cnop M, Hannaert JC, Hoorens A, Eizirik DL, Pipeleers DG. Inverse relationship between cytotoxicity of free fatty acids in pancreatic islet cells and cellular triglyceride accumulation. Diabetes 2001; 50:1771-7; PMID:11473037; http://dx.doi.org/10.2337/diabetes.50.8.1771
34. Maedler K, Spinas GA, Dyntar D, Moritz W, Kaiser N, Donath MY. Distinct effects of saturated and monounsaturated fatty acids on beta-cell turnover and function. Diabetes 2001; 50:69-76; PMID:11147797; http://dx.doi.org/10.2337/ diabetes.50.1.69
35. Listenberger LL, Han X, Lewis SE, Cases S, Farese RV Jr., Ory DS, et al. Triglyceride accumulation protects against fatty acid-induced lipotoxicity. Proc Natl Acad Sci U S A 2003; 100:3077-82; PMID:12629214; http://dx.doi.org/10. 1073/pnas.0630588100
36. Cunha DA, Hekerman P, Ladrière L, Bazarra-Castro A, Ortis F, Wakeham MC, et al. Initiation and execution of lipotoxic ER stress in pancreatic beta-cells. J Cell Sci 2008; 121:2308-18; PMID:18559892; http://dx.doi.org/10. 1242/jcs.026062
37. Kwon G, Marshall CA, Liu H, Pappan KL, Remedi MS, McDaniel ML. Glucose-stimulated DNA synthesis through mammalian target of rapamycin (mTOR) is regulated by KATP channels: effects on cell cycle progression in rodent islets. J Biol Chem 2006; 281:3261-7; PMID:16344552; http://dx.doi.org/10.1074/jbc. M508821200
38. Koyanagi M, Asahara S, Matsuda T, Hashimoto N, Shigeyama Y, Shibutani Y, et al. Ablation of TSC2 enhances insulin secretion by increasing the number of mitochondria through activation of mTORC1. PLoS One 2011; 6:e23238; PMID:21886784; http://dx.doi.org/10.1371/journal.pone.0023238
39. Butler AE, Janson J, Bonner-Weir S, Ritzel R, Rizza RA, Butler PC. Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes 2003; 52:102-10; PMID:12502499; http://dx.doi.org/10.2337/ diabetes.52.1.102
40. Klöppel G, Löhr M, Habich K, Oberholzer M, Heitz PU. Islet pathology and the pathogenesis of type 1 and type 2 diabetes mellitus revisited. Surv Synth Pathol Res 1985; 4:110-25; PMID:3901180
41. Tomita T, Doull V, Pollock HG, Krizsan D. Pancreatic islets of obese hyperglycemic mice (ob/ob). Pancreas 1992; 7:367-75; PMID:1594559; http://dx.doi.org/10.1097/00006676-199205000-00015
42. Kwon G, Pappan KL, Marshall CA, Schaffer JE, McDaniel ML. cAMP Dose-dependently prevents palmitate-induced apoptosis by both protein kinase A-And cAMP-guanine nucleotide exchange factor-dependent pathways in beta-cells. J Biol Chem 2004; 279:8938-45; PMID:14688288; http://dx.doi.org/10.1074/jbc. M310330200