Perilipin 5 regulates islet lipid metabolism and insulin secretion in a cAMP-dependent manner: Implication of its role in the postprandial insulin secretion

Diabetes

Volumn 64, Issue 4, 2015, Pages 1299-1310

  Trevino, Michelle B ^a   Machida, Yui ^a   Hallinger, Daniel R ^a   Garcia, Eden ^a   Christensen, Aaron ^a   Dutta, Sucharita ^a   Peake, David A ^b   Ikeda, Yasuhiro ^c   Imai, Yumi ^a  

^a EASTERN VIRGINIA MEDICAL SCHOOL   (United States)

^b Thermo Fisher Scientific   (United States)

^c MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

8 BROMO CYCLIC AMP; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; EXENDIN 4; FATTY ACID; G PROTEIN COUPLED RECEPTOR 40; INSULIN; PERILIPIN; PERILIPIN 5; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; G PROTEIN COUPLED RECEPTOR; GLUCOSE; GPR40 PROTEIN, MOUSE; LIPID STORAGE DROPLET PROTEIN 5, MOUSE; MEMBRANE PROTEIN; MUSCLE PROTEIN; PERILIPIN 2; SIGNAL PEPTIDE;

ADENO ASSOCIATED VIRUS 8; ANIMAL CELL; ARTICLE; DIET RESTRICTION; GENE EXPRESSION; GLUCOSE TOLERANCE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; INSULIN RELEASE; LIPID METABOLISM; LIPOLYSIS; MALE; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; POSTPRANDIAL STATE; PRIORITY JOURNAL; REFEEDING; SINGLE DRUG DOSE; ANIMAL; GENETICS; METABOLISM; PANCREAS ISLET; PHYSIOLOGY; SECRETION (PROCESS);

ANIMALS; CYCLIC AMP; FASTING; GLUCOSE; HUMANS; INSULIN; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; ISLETS OF LANGERHANS; LIPID METABOLISM; LIPOLYSIS; MALE; MEMBRANE PROTEINS; MICE; MUSCLE PROTEINS; POSTPRANDIAL PERIOD; RECEPTORS, G-PROTEIN-COUPLED;

EID: 84962020084     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db14-0559     Document Type: Article

References (50)

1. Weir GC, Bonner-Weir S. Islet β cell mass in diabetes and how it relates to function, birth, and death. Ann N Y Acad Sci 2013;1281: 92-105
2. Bonora E, Corrao G, Bagnardi V, et al. Prevalence and correlates of postprandial hyperglycaemia in a large sample of patients with type 2 diabetes mellitus. Diabetologia 2006;49: 846-854
3. Monnier L, Colette C, Dunseath GJ, Owens DR. The loss of postprandial glycemic control precedes stepwise deterioration of fasting with worsening diabetes. Diabetes Care 2007;30: 263-269
4. Shichiri M, Kishikawa H, Ohkubo Y, Wake N. Long-term results of the Kumamoto Study on optimal diabetes control in type 2 diabetic patients. Diabetes Care 2000;23(Suppl. 2): B21-B29
5. Warnotte C, Gilon P, Nenquin M, Henquin JC. Mechanisms of the stimulation of insulin release by saturated fatty acids. A study of palmitate effects in mouse beta-cells. Diabetes 1994;43: 703-711
6. Yaney GC, Corkey BE. Fatty acid metabolism and insulin secretion in pancreatic beta cells. Diabetologia 2003;46: 1297-1312
7. Latour MG, Alquier T, Oseid E, et al. GPR40 is necessary but not sufficient for fatty acid stimulation of insulin secretion in vivo. Diabetes 2007;56: 1087-1094
8. Prentki M, Matschinsky FM, Madiraju SR. Metabolic signaling in fuelinduced insulin secretion. Cell Metab 2013;18: 162-185
9. Dobbins RL, Chester MW, Daniels MB, McGarry JD, Stein DT. Circulating fatty acids are essential for efficient glucose-stimulated insulin secretion after prolonged fasting in humans. Diabetes 1998;47: 1613-1618
10. Malaisse WJ, Best L, Kawazu S, Malaisse-Lagae F, Sener A. The stimulussecretion coupling of glucose-induced insulin release: Fuel metabolism in islets deprived of exogenous nutrient. Arch Biochem Biophys 1983;224: 102-110
11. Brasaemle DL. Thematic review series: Adipocyte biology. The perilipin family of structural lipid droplet proteins: Stabilization of lipid droplets and control of lipolysis. J Lipid Res 2007;48: 2547-2559
12. Ducharme NA, Bickel PE. Lipid droplets in lipogenesis and lipolysis. Endocrinology 2008;149: 942-949
13. Greenberg AS, Coleman RA, Kraemer FB, et al. The role of lipid droplets in metabolic disease in rodents and humans. J Clin Invest 2011;121: 2102-2110
14. Faleck DM, Ali K, Roat R, et al. Adipose differentiation-related protein regulates lipids and insulin in pancreatic islets. Am J Physiol Endocrinol Metab 2010;299: E249-E257
15. Dalen KT, Dahl T, Holter E, et al. LSDP5 is a PAT protein specifically expressed in fatty acid oxidizing tissues. Biochim Biophys Acta 2007;1771: 210-227
16. Wolins NE, Quaynor BK, Skinner JR, et al. OXPAT/PAT-1 is a PPAR-induced lipid droplet protein that promotes fatty acid utilization. Diabetes 2006;55: 3418-3428
17. Yamaguchi T, Matsushita S, Motojima K, Hirose F, Osumi T. MLDP, a novel PAT family protein localized to lipid droplets and enriched in the heart, is regulated by peroxisome proliferator-activated receptor alpha. J Biol Chem 2006; 281: 14232-14240
18. Bosma M, Minnaard R, Sparks LM, et al. The lipid droplet coat protein perilipin 5 also localizes to muscle mitochondria. Histochem Cell Biol 2012;137: 205-216
19. Kimmel AR, Sztalryd C. Perilipin 5, a lipid droplet protein adapted to mitochondrial energy utilization. Curr Opin Lipidol 2014;25: 110-117
20. Kuramoto K, Okamura T, Yamaguchi T, et al. Perilipin 5, a lipid dropletbinding protein, protects heart from oxidative burden by sequestering fatty acid from excessive oxidation. J Biol Chem 2012;287: 23852-23863
21. Li H, Song Y, Zhang LJ, et al. LSDP5 enhances triglyceride storage in hepatocytes by influencing lipolysis and fatty acid b-oxidation of lipid droplets. PLoS One 2012;7: E36712
22. Wang H, Bell M, Sreenivasan U, et al. Unique regulation of adipose triglyceride lipase (ATGL) by perilipin 5, a lipid droplet-associated protein. J Biol Chem 2011;286: 15707-15715
23. Granneman JG, Moore HP, Mottillo EP, Zhu Z. Functional interactions between Mldp (LSDP5) and Abhd5 in the control of intracellular lipid accumulation. J Biol Chem 2009;284: 3049-3057
24. Granneman JG, Moore HP, Mottillo EP, Zhu Z, Zhou L. Interactions of perilipin-5 (Plin5) with adipose triglyceride lipase. J Biol Chem 2011;286: 5126-5135
25. Imai Y, Patel HR, Hawkins EJ, Doliba NM, Matschinsky FM, Ahima RS. Insulin secretion is increased in pancreatic islets of neuropeptide Y-deficient mice. Endocrinology 2007;148: 5716-5723
26. Bird SS, Marur VR, Sniatynski MJ, Greenberg HK, Kristal BS. Lipidomics profiling by high-resolution LC-MS and high-energy collisional dissociation fragmentation: Focus on characterization of mitochondrial cardiolipins and monolysocardiolipins. Anal Chem 2011;83: 940-949
27. Bird SS, Marur VR, Sniatynski MJ, Greenberg HK, Kristal BS. Serum lipidomics profiling using LC-MS and high-energy collisional dissociation fragmentation: Focus on triglyceride detection and characterization. Anal Chem 2011; 83: 6648-6657
28. Vernier S, Chiu A, Schober J, et al. β-cell metabolic alterations under chronic nutrient overload in rat and human islets. Islets 2012;4: 379-392
29. Hsieh K, Lee YK, Londos C, Raaka BM, Dalen KT, Kimmel AR. Perilipin family members preferentially sequester to either triacylglycerol-specific or cholesteryl-ester-specific intracellular lipid storage droplets. J Cell Sci 2012;125: 4067-4076
30. Borg J, Klint C, Wierup N, 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: 3049-3057
31. Thiam AR, Farese RV Jr, Walther TC. The biophysics and cell biology of lipid droplets. Nat Rev Mol Cell Biol 2013;14: 775-786
32. Masuda Y, Itabe H, Odaki M, et al. ADRP/adipophilin is degraded through the proteasome-dependent pathway during regression of lipid-storing cells. J Lipid Res 2006;47: 87-98
33. Xu G, Sztalryd C, Lu X, et al. Post-translational regulation of adipose differentiation-related protein by the ubiquitin/proteasome pathway. J Biol Chem 2005;280: 42841-42847
34. Lavine RL, Voyles N, Perrino PV, Recant L. The effect of fasting on tissue cyclic cAMP and plasma glucagon in the obese hyperglycemic mouse. Endocrinology 1975;97: 615-620
35. Tengholm A. Cyclic AMP dynamics in the pancreatic β-cell. Ups J Med Sci 2012;117: 355-369
36. 2+ channel and link to insulin release. Am J Physiol Endocrinol Metab 2005;289: E670-E677
37. Campbell JE, Drucker DJ. Pharmacology, physiology, and mechanisms of incretin hormone action. Cell Metab 2013;17: 819-837
38. Pollak NM, Schweiger M, Jaeger D, et al. Cardiac-specific overexpression of perilipin 5 provokes severe cardiac steatosis via the formation of a lipolytic barrier. J Lipid Res 2013;54: 1092-1102
39. Wang H, Sreenivasan U, Gong DW, et al. Cardiomyocyte-specific perilipin 5 overexpression leads to myocardial steatosis and modest cardiac dysfunction. J Lipid Res 2013;54: 953-965
40. Haemmerle G, Moustafa T, Woelkart G, et al. ATGL-mediated fat catabolism regulates cardiac mitochondrial function via PPAR-A and PGC-1. Nat Med 2011; 17: 1076-1085
41. Prentki M, Madiraju SR. Glycerolipid/free fatty acid cycle and islet β-cell function in health, obesity and diabetes. Mol Cell Endocrinol 2012;353: 88-100
42. Peyot ML, Guay C, Latour MG, et al. Adipose triglyceride lipase is implicated in fuel-and non-fuel-stimulated insulin secretion. J Biol Chem 2009;284: 16848-16859
43. Tang T, Abbott MJ, Ahmadian M, Lopes AB, Wang Y, Sul HS. Desnutrin/ ATGL activates PPARd to promote mitochondrial function for insulin secretion in islet β cells. Cell Metab 2013;18: 883-895
44. Zhao S, Mugabo Y, Iglesias J, et al. a/b-Hydrolase domain-6-accessible monoacylglycerol controls glucose-stimulated insulin secretion. Cell Metab 2014; 19: 993-1007
45. Burant CF. Activation of GPR40 as a therapeutic target for the treatment of type 2 diabetes. Diabetes Care 2013;36(Suppl. 2): S175-S179
46. Eichmann TO, Kumari M, Haas JT, et al. Studies on the substrate and stereo/regioselectivity of adipose triglyceride lipase, hormone-sensitive lipase, and diacylglycerol-O-acyltransferases. J Biol Chem 2012;287: 41446-41457
47. El-Azzouny M, Evans CR, Treutelaar MK, Kennedy RT, Burant CF. Increased glucose metabolism and glycerolipid formation by fatty acids and GPR40 receptor signaling underlies the fatty acid potentiation of insulin secretion. J Biol Chem 2014;289: 13575-13588
48. Kaihara KA, Dickson LM, Jacobson DA, et al. β-Cell-specific protein kinase A activation enhances the efficiency of glucose control by increasing acute-phase insulin secretion. Diabetes 2013;62: 1527-1536
49. Pearson GL, Mellett N, Chu KY, et al. Lysosomal acid lipase and lipophagy are constitutive negative regulators of glucose-stimulated insulin secretion from pancreatic beta cells. Diabetologia 2014;57: 129-139
50. Zhou L, Zhang L, Meng Q, et al. C/EBPa promotes transcription of the porcine perilipin5 gene. Mol Cell Endocrinol 2012;364: 28-35