Free fatty acids block glucose-induced β-cell proliferation in mice by inducing cell cycle inhibitors p16 and p18

Diabetes

Volumn 61, Issue 3, 2012, Pages 632-641

  Pascoe, Jordan ^a   Hollern, Douglas ^a   Stamateris, Rachel ^a   Abbasi, Munira ^a   Romano, Lia C ^a   Zou, Baobo ^a   O'Donnell, Christopher P ^a   Garcia Ocana, Adolfo ^a   Alonso, Laura C ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE 4; FATTY ACID; GLUCOSE; LINOLEIC ACID; LIPOSYN II; PALMITIC ACID; PROTEIN P16; PROTEIN P18; SODIUM CHLORIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CELL CYCLE; CELL DEATH; CELL PROLIFERATION; CONTROLLED STUDY; GENE SILENCING; IN VITRO STUDY; IN VIVO CULTURE; IN VIVO STUDY; INSULIN RESISTANCE; INSULINOMA; LIPOTOXICITY; MALE; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; CELL PROLIFERATION; CYCLIN D2; CYCLIN-DEPENDENT KINASE INHIBITOR P16; CYCLIN-DEPENDENT KINASE INHIBITOR P18; EMULSIONS; FATTY ACIDS, NONESTERIFIED; GLUCOSE; INSULIN-SECRETING CELLS; MALE; MICE; MICE, INBRED C57BL; PHOSPHOLIPIDS; RATS; SAFFLOWER OIL; SOYBEAN OIL;

EID: 84857435669     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db11-0991     Document Type: Article

References (50)

1. Butler AE, Janson J, Bonner-Weir S, Ritzel R, Rizza RA, Butler PC. Betacell deficit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes 2003;52:102-110 (Pubitemid 36042113)
2. Lorenzo C, Wagenknecht LE, Rewers MJ, et al. Disposition index, glucose effectiveness, and conversion to type 2 diabetes: the Insulin Resistance Atherosclerosis Study (IRAS). Diabetes Care 2010;33:2098-2103
3. Ritzel RA, Butler AE, Rizza RA, Veldhuis JD, Butler PC. Relationship between beta-cell mass and fasting blood glucose concentration in humans. Diabetes Care 2006;29:717-718 (Pubitemid 44115384)
4. Sachdeva MM, Stoffers DA. Minireview: Meeting the demand for insulin: molecular mechanisms of adaptive postnatal beta-cell mass expansion. Mol Endocrinol 2009;23:747-758
5. Hosokawa H, Hosokawa YA, Leahy JL. Upregulated hexokinase activity in isolated islets from diabetic 90% pancreatectomized rats. Diabetes 1995;44: 1328-1333
6. Liu YQ, Han J, Epstein PN, Long YS. Enhanced rat beta-cell proliferation in 60% pancreatectomized islets by increased glucose metabolic flux through pyruvate carboxylase pathway. Am J Physiol Endocrinol Metab 2005;288: E471-E478 (Pubitemid 40250540)
7. Terauchi Y, Takamoto I, Kubota N, et al. Glucokinase and IRS-2 are required for compensatory beta cell hyperplasia in response to high-fat dietinduced insulin resistance. J Clin Invest 2007;117:246-257 (Pubitemid 46048470)
8. Porat S, Weinberg-Corem N, Tornovsky-Babaey S, et al. Control of pancreatic β cell regeneration by glucose metabolism. Cell Metab 2011;13:440-449
9. Weir GC, Bonner-Weir S. A dominant role for glucose in beta cell compensation of insulin resistance. J Clin Invest 2007;117:81-83 (Pubitemid 46048452)
10. Liu YQ, Jetton TL, Leahy JL. Beta-Cell adaptation to insulin resistance. Increased pyruvate carboxylase and malate-pyruvate shuttle activity in islets of nondiabetic Zucker fatty rats. J Biol Chem 2002;277:39163-39168 (Pubitemid 35190884)
11. Poitout V, Robertson RP. Glucolipotoxicity: fuel excess and beta-cell dysfunction. Endocr Rev 2008;29:351-366 (Pubitemid 351679704)
12. Charles MA, Eschwège E, Thibult N, et al. The role of non-esterified fatty acids in the deterioration of glucose tolerance in Caucasian subjects: results of the Paris Prospective Study. Diabetologia 1997;40:1101-1106 (Pubitemid 27381974)
13. Paolisso G, Tataranni PA, Foley JE, Bogardus C, Howard BV, Ravussin E. A high concentration of fasting plasma non-esterified fatty acids is a risk factor for the development of NIDDM. Diabetologia 1995;38:1213-1217
14. Milburn JL Jr, Hirose H, Lee YH, 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- 1299
15. Samuel VT, Petersen KF, Shulman GI. Lipid-induced insulin resistance: unravelling the mechanism. Lancet 2010;375:2267-2277
16. Prentki M, Madiraju SR. Glycerolipid metabolism and signaling in health and disease. Endocr Rev 2008;29:647-676
17. Rhodes CJ. IGF-I and GH post-receptor signaling mechanisms for pancreatic beta-cell replication. J Mol Endocrinol 2000;24:303-311 (Pubitemid 30415004)
18. Cousin SP, Hügl SR, Wrede CE, Kajio H, Myers MG Jr, Rhodes CJ. Free fatty acid-induced inhibition of glucose and insulin-like growth factor I-induced deoxyribonucleic acid synthesis in the pancreatic beta-cell line INS-1. Endocrinology 2001;142:229-240 (Pubitemid 32183685)
19. González-Pertusa JA, Dubé J, Valle SR, et al. Novel proapoptotic effect of hepatocyte growth factor: synergy with palmitate to cause pancreatic betacell apoptosis. Endocrinology 2010;151:1487-1498
20. Brelje TC, Bhagroo NV, Stout LE, Sorenson RL. Beneficial effects of lipids and prolactin on insulin secretion and beta-cell proliferation: a role for lipids in the adaptation of islets to pregnancy. J Endocrinol 2008;197:265-276 (Pubitemid 351696239)
21. Maedler K, Oberholzer J, Bucher P, Spinas GA, Donath MY. Monounsaturated fatty acids prevent the deleterious effects of palmitate and high glucose on human pancreatic beta-cell turnover and function. Diabetes 2003;52:726-733 (Pubitemid 36323580)
22. Delghingaro-Augusto V, Nolan CJ, Gupta D, 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;52:1122-1132
23. Fontés G, Zarrouki B, Hagman DK, et al. Glucolipotoxicity agedependently impairs beta cell function in rats despite a marked increase in beta cell mass. Diabetologia 2010;53:2369-2379
24. Steil GM, Trivedi N, Jonas JC, et al. Adaptation of beta-cell mass to substrate oversupply: enhanced function with normal gene expression. Am J Physiol Endocrinol Metab 2001;280:E788-E796
25. Hagman DK, Latour MG, Chakrabarti SK, et al. Cyclical and alternating infusions of glucose and intralipid in rats inhibit insulin gene expression and Pdx-1 binding in islets. Diabetes 2008;57:424-431
26. 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 (Pubitemid 19021816)
27. Topp BG, McArthur MD, Finegood DT. Metabolic adaptations to chronic glucose infusion in rats. Diabetologia 2004;47:1602-1610 (Pubitemid 39371643)
28. Alonso LC, Yokoe T, Zhang P, et al. Glucose infusion in mice: a new model to induce beta-cell replication. Diabetes 2007;56:1792-1801 (Pubitemid 47025447)
29. Levitt HE, Cyphert TJ, Pascoe JL, et al. Glucose stimulates human beta cell replication in islets transplanted into NOD-SCID mice. Diabetologia 2011; 54:572-582
30. Yokoe T, Alonso LC, Romano LC, et al. Intermittent hypoxia reverses the diurnal glucose rhythm and causes pancreatic beta-cell replication in mice. J Physiol 2008;586:899-911 (Pubitemid 351194126)
31. Fatrai S, Elghazi L, Balcazar N, et al. Akt induces beta-cell proliferation by regulating cyclin D1, cyclin D2, and p21 levels and cyclin-dependent kinase-4 activity. Diabetes 2006;55:318-325 (Pubitemid 43343259)
32. Georgia S, Bhushan A. Beta cell replication is the primary mechanism for maintaining postnatal beta cell mass. J Clin Invest 2004;114:963-968 (Pubitemid 39578724)
33. Kushner JA, CiemerychMA, Sicinska E, et al. Cyclins D2 and D1 are essential for postnatal pancreatic beta-cell growth. Mol Cell Biol 2005;25:3752-3762 (Pubitemid 40559580)
34. Peshavaria M, Larmie BL, Lausier J, et al. Regulation of pancreatic betacell regeneration in the normoglycemic 60% partial-pancreatectomy mouse. Diabetes 2006;55:3289-3298 (Pubitemid 44923585)
35. Georgia S, Hinault C, Kawamori D, et al. Cyclin D2 is essential for the compensatory beta-cell hyperplastic response to insulin resistance in rodents. Diabetes 2010;59:987-996
36. Cozar-Castellano I, Fiaschi-Taesch N, Bigatel TA, et al. Molecular control of cell cycle progression in the pancreatic beta-cell. Endocr Rev 2006;27:356-370 (Pubitemid 43848303)
37. Rane SG, Dubus P, Mettus RV, et al. Loss of Cdk4 expression causes insulin-deficient diabetes and Cdk4 activation results in beta-islet cell hyperplasia. Nat Genet 1999;22:44-52
38. Cozar-Castellano I, Weinstock M, Haught M, Velázquez-Garcia S, Sipula D, Stewart AF. Evaluation of beta-cell replication in mice transgenic for hepatocyte growth factor and placental lactogen: comprehensive characterization of the G1/S regulatory proteins reveals unique involvement of p21cip. Diabetes 2006;55:70-77 (Pubitemid 43343300)
39. Elghazi L, Balcazar N, Blandino-Rosano M, et al. Decreased IRS signaling impairs beta-cell cycle progression and survival in transgenic mice overexpressing S6K in beta-cells. Diabetes 2010;59:2390-2399
40. Uchida T, Nakamura T, Hashimoto N, et al. Deletion of Cdkn1b ameliorates hyperglycemia by maintaining compensatory hyperinsulinemia in diabetic mice. Nat Med 2005;11:175-182 (Pubitemid 40321353)
41. Chen H, Gu X, Su IH, et al. Polycomb protein Ezh2 regulates pancreatic beta-cell Ink4a/Arf expression and regeneration in diabetes mellitus. Genes Dev 2009;23:975-985
42. Dhawan S, Tschen SI, Bhushan A. Bmi-1 regulates the Ink4a/Arf locus to control pancreatic beta-cell proliferation. Genes Dev 2009;23:906-911
43. Krishnamurthy J, Ramsey MR, Ligon KL, et al. p16INK4a induces an agedependent decline in islet regenerative potential. Nature 2006;443:453-457 (Pubitemid 44477281)
44. Pappan KL, Pan Z, Kwon G, et al. Pancreatic beta-cell lipoprotein lipase independently regulates islet glucose metabolism and normal insulin secretion. J Biol Chem 2005;280:9023-9029 (Pubitemid 40409594)
45. Kim SP, Catalano KJ, Hsu IR, Chiu JD, Richey JM, Bergman RN. Nocturnal free fatty acids are uniquely elevated in the longitudinal development of diet-induced insulin resistance and hyperinsulinemia. Am J Physiol Endocrinol Metab 2007;292:E1590-E1598 (Pubitemid 47084693)
46. Duesing K, Fatemifar G, Charpentier G, et al. Strong association of common variants in the CDKN2A/CDKN2B region with type 2 diabetes in French Europids. Diabetologia 2008;51:821-826
47. Gizard F, Amant C, Barbier O, et al. PPAR alpha inhibits vascular smooth muscle cell proliferation underlying intimal hyperplasia by inducing the tumor suppressor p16INK4a. J Clin Invest 2005;115:3228-3238 (Pubitemid 41567587)
48. 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 (Pubitemid 40174657)
49. Tschen SI, Dhawan S, Gurlo T, Bhushan A. Age-dependent decline in betacell proliferation restricts the capacity of beta-cell regeneration in mice. Diabetes 2009;58:1312-1320
50. Ramsey MR, Krishnamurthy J, Pei XH, et al. Expression of p16Ink4a compensates for p18Ink4c loss in cyclin-dependent kinase 4/6-dependent tumors and tissues. Cancer Res 2007;67:4732-4741 (Pubitemid 46910180)