Adipose differentiation-related protein regulates lipids and insulin in pancreatic islets

American Journal of Physiology - Endocrinology and Metabolism

Volumn 299, Issue 2, 2010, Pages

  Faleck, D M ^a   Ali, K ^a   Roat, R ^a   Graham, M J ^b   Crooke, R M ^b   Battisti, R ^c   Garcia, E ^c   Ahima, R S ^a   Imai, Y ^a,c  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b ISIS PHARMACEUTICALS   (United States)

^c EASTERN VIRGINIA MEDICAL SCHOOL   (United States)

Author keywords

Fasting; High fat diet; MIN6 cells; Oleic acid; Palmitic acid

Indexed keywords

ADIPOPHILIN; DIACYLGLYCEROL ACYLTRANSFERASE 2; FATTY ACID; FATTY ACID SYNTHASE; INSULIN; LIPID; MESSENGER RNA; PALMITIC ACID; ADFP PROTEIN, MOUSE; MEMBRANE PROTEIN; RNA; TRIACYLGLYCEROL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIET RESTRICTION; DOWN REGULATION; FATTY ACID OXIDATION; FATTY ACID TRANSPORT; INSULIN RELEASE; LIPID DIET; LIPID METABOLISM; LIPOLYSIS; MALE; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; NUTRITIONAL STATUS; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL CULTURE; CYTOLOGY; FLUORESCENT ANTIBODY TECHNIQUE; GLUCOSE BLOOD LEVEL; HUMAN; IMMUNOHISTOCHEMISTRY; ISOLATION AND PURIFICATION; METABOLISM; NUTRITION; PANCREAS ISLET; PHYSIOLOGY; SECRETION; WESTERN BLOTTING;

ANIMALS; BLOOD GLUCOSE; BLOTTING, WESTERN; CELLS, CULTURED; DOWN-REGULATION; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNOHISTOCHEMISTRY; INSULIN; ISLETS OF LANGERHANS; LIPID METABOLISM; LIPOLYSIS; MALE; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; NUTRITIONAL PHYSIOLOGICAL PHENOMENA; RNA; TRIGLYCERIDES;

EID: 77954890412     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00646.2009     Document Type: Article

References (67)

1. Bell M, Wang H, Chen H, McLenithan JC, Gong DW, Yang RZ, Yu D, Fried SK, Quon MJ, Londos C, Sztalryd C. Consequences of lipid droplet coat protein downregulation in liver cells: abnormal lipid droplet metabolism and induction of insulin resistance. Diabetes 57: 2037-2045, 2008.
2. Borg J, Klint C, Wierup N, Strom K, Larsson S, Sundler F, Lupi R, Marchetti P, Xu G, Kimmel A, Londos C, Holm C. Perilipin is present in islets of Langerhans and protects against lipotoxicity when overexpressed in the beta-cell line INS-1. Endocrinology 150: 3049-3057, 2009.
3. Brasaemle DL, Barber T, Wolins NE, Serrero G, Blanchette-Mackie EJ, Londos C. Adipose differentiation-related protein is an ubiquitously expressed lipid storage droplet-associated protein. J Lipid Res 38: 2249-2263, 1997. (Pubitemid 27495384)
4. Briaud I, Harmon JS, Kelpe CL, Segu VB, Poitout V. Lipotoxicity of the pancreatic beta-cell is associated with glucose-dependent esterification of fatty acids into neutral lipids. Diabetes 50: 315-321, 2001.
5. Carlsson C, Borg LA, Welsh N. Sodium palmitate induces partial mitochondrial uncoupling and reactive oxygen species in rat pancreatic islets in vitro. Endocrinology 140: 3422-3428, 1999. (Pubitemid 30645397)
6. Chang BH, Chan L. Regulation of Triglyceride Metabolism. III. Emerging role of lipid droplet protein ADFP in health and disease. Am J Physiol Gastrointest Liver Physiol 292: G1465-G1468, 2007.
7. Chang BH, Li L, Paul A, Taniguchi S, Nannegari V, Heird WC, Chan L. Protection against fatty liver but normal adipogenesis in mice lacking adipose differentiation-related protein. Mol Cell Biol 26: 1063-1076, 2006.
8. 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 50: 1771-1777, 2001.
9. Dalen KT, Ulven SM, Arntsen BM, Solaas K, Nebb HI. PPARalpha activators and fasting induce the expression of adipose differentiation-related protein in liver. J Lipid Res 47: 931-943, 2006.
10. 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 47: 1613-1618, 1998.
11. El-Assaad W, Buteau J, Peyot ML, Nolan C, Roduit R, Hardy S, Joly E, Dbaibo G, Rosenberg L, Prentki M. Saturated fatty acids synergize with elevated glucose to cause pancreatic beta-cell death. Endocrinology 144: 4154-4163, 2003. (Pubitemid 37088771)
12. Fan B, Ikuyama S, Gu JQ, Wei P, Oyama J, Inoguchi T, Nishimura J. Oleic acid-induced ADRP expression requires both AP-1 and PPAR response elements, and is reduced by Pycnogenol through mRNA degradation in NMuLi liver cells. Am J Physiol Endocrinol Metab 297: E112-E123, 2009.
13. Folch J, Lees M, Sloane Stanley GH. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226: 497-509, 1957.
14. Fujimoto T, Ohsaki Y. Cytoplasmic lipid droplets: rediscovery of an old structure as a unique platform. Ann NY Acad Sci 1086: 104-115, 2006.
15. Gao J, Serrero G. Adipose differentiation related protein (ADRP) expressed in transfected COS-7 cells selectively stimulates long chain fatty acid uptake. J Biol Chem 274: 16825-16830, 1999.
16. Goh TT, Mason TM, Gupta N, So A, Lam TK, Lam L, Lewis GF, Mari A, Giacca A. Lipid-induced β-cell dysfunction in vivo in models of progressive β-cell failure. Am J Physiol Endocrinol Metab 292: E549-E560, 2007. (Pubitemid 46220580)
17. Gotoh M, Maki T, Kiyoizumi T, Satomi S, Monaco AP. An improved method for isolation of mouse pancreatic islets. Transplantation 40: 437-438, 1985.
18. Greenberg AS, Egan JJ, Wek SA, Garty NB, Blanchette-Mackie EJ, Londos C. Perilipin, a major hormonally regulated adipocyte-specific phosphoprotein associated with the periphery of lipid storage droplets. J Biol Chem 266: 11341-11346, 1991.
19. Gross DN, Miyoshi H, Hosaka T, Zhang HH, Pino EC, Souza S, Obin M, Greenberg AS, Pilch PF. Dynamics of lipid droplet-associated proteins during hormonally stimulated lipolysis in engineered adipocytes: stabilization and lipid droplet binding of adipocyte differentiation-related protein/adipophilin. Mol Endocrinol 20: 459-466, 2006.
20. Hall AM, Brunt EM, Chen Z, Viswakarma N, Reddy JK, Wolins NE, Finck BN. Dynamic and differential regulation of proteins that coat lipid droplets in fatty liver dystrophic mice. J Lipid Res 51: 554-563, 2010.
21. Heid HW, Moll R, Schwetlick I, Rackwitz HR, Keenan TW. Adipophilin is a specific marker of lipid accumulation in diverse cell types and diseases. Cell Tissue Res 294: 309-321, 1998. (Pubitemid 28486407)
22. Igal RA, Wang P, Coleman RA. Triacsin C blocks de novo synthesis of glycerolipids and cholesterol esters but not recycling of fatty acid into phospholipid: evidence for functionally separate pools of acyl-CoA. Biochem J 324: 529-534, 1997.
23. 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 148: 5716-5723, 2007.
24. Imai Y, Varela GM, Jackson MB, Graham MJ, Crooke RM, Ahima RS. Reduction of hepatosteatosis and lipid levels by an adipose differentiation- related protein antisense oligonucleotide. Gastroenterology 132: 1947-1954, 2007.
25. Itoh Y, Kawamata Y, Harada M, Kobayashi M, Fujii R, Fukusumi S, Ogi K, Hosoya M, Tanaka Y, Uejima H, Tanaka H, Maruyama M, Satoh R, Okubo S, Kizawa H, Komatsu H, Matsumura F, Noguchi Y, Shinohara T, Hinuma S, Fujisawa Y, Fujino M. Free fatty acids regulate insulin secretion from pancreatic beta cells through GPR40. Nature 422: 173-176, 2003.
26. Kersten S, Seydoux J, Peters JM, Gonzalez FJ, Desvergne B, Wahli W. Peroxisome proliferator-activated receptor alpha mediates the adaptive response to fasting. J Clin Invest 103: 1489-1498, 1999.
27. Lacy PE, Kostianovsky M. Method for the isolation of intact islets of Langerhans from the rat pancreas. Diabetes 16: 35-39, 1967.
28. Larigauderie G, Furman C, Jaye M, Lasselin C, Copin C, Fruchart JC, Castro G, Rouis M. Adipophilin enhances lipid accumulation and prevents lipid efflux from THP-1 macrophages: potential role in atherogenesis. Arterioscler Thromb Vasc Biol 24: 504-510, 2004. (Pubitemid 38326145)
29. Latour MG, Alquier T, Oseid E, Tremblay C, Jetton TL, Luo J, Lin DC, Poitout V. GPR40 is necessary but not sufficient for fatty acid stimulation of insulin secretion in vivo. Diabetes 56: 1087-1094, 2007.
30. Lee Y, Wang MY, Kakuma T, Wang ZW, Babcock E, McCorkle K, Higa M, Zhou YT, Unger RH. Liporegulation in diet-induced obesity. The antisteatotic role of hyperleptinemia. J Biol Chem 276: 5629-5635, 2001.
31. Listenberger LL, Ostermeyer-Fay AG, Goldberg EB, Brown WJ, Brown DA. Adipocyte differentiation-related protein reduces the lipid droplet association of adipose triglyceride lipase and slows triacylglycerol turnover. J Lipid Res 48: 2751-2761, 2007.
32. Londos C, Sztalryd C, Tansey JT, Kimmel AR. Role of PAT proteins in lipid metabolism. Biochimie 87: 45-49, 2005. (Pubitemid 40305232)
33. Magnusson B, Asp L, Bostrom P, Ruiz M, Stillemark-Billton P, Linden D, Boren J, Olofsson SO. Adipocyte differentiation-related protein promotes fatty acid storage in cytosolic triglycerides and inhibits secretion of very low-density lipoproteins. Arterioscler Thromb Vasc Biol 26: 1566-1571, 2006.
34. Malaisse WJ, Best L, Kawazu S, Malaisse-Lagae F, Sener A. The stimulus-secretion coupling of glucose-induced insulin release: fuel metabolism in islets deprived of exogenous nutrient. Arch Biochem Biophys 224: 102-110, 1983. (Pubitemid 13072634)
35. Martin S, Parton RG. Lipid droplets: a unified view of a dynamic organelle. Nat Rev Mol Cell Biol 7: 373-378, 2006.
36. Martinez-Botas J, Anderson JB, Tessier D, Lapillonne A, Chang BH, Quast MJ, Gorenstein D, Chen KH, Chan L. Absence of perilipin results in leanness and reverses obesity in Lepr(db/db) mice. Nat Genet 26: 474-479, 2000.
37. Masuda Y, Itabe H, Odaki M, Hama K, Fujimoto Y, Mori M, Sasabe N, Aoki J, Arai H, Takano T. ADRP/adipophilin is degraded through the proteasome-dependent pathway during regression of lipid-storing cells. J Lipid Res 47: 87-98, 2006.
38. Mokdad AH, Ford ES, Bowman BA, Dietz WH, Vinicor F, Bales VS, Marks JS. Prevalence of obesity, diabetes, and obesity-related health risk factors, 2001. JAMA 289: 76-79, 2003.
39. Moller L, Stodkilde-Jorgensen H, Jensen FT, Jorgensen JO. Fasting in healthy subjects is associated with intrahepatic accumulation of lipids as assessed by 1H-magnetic resonance spectroscopy. Clin Sci (Lond) 114: 547-552, 2008. (Pubitemid 351548762)
40. Motomura W, Inoue M, Ohtake T, Takahashi N, Nagamine M, Tanno S, Kohgo Y, Okumura T. Up-regulation of ADRP in fatty liver in human and liver steatosis in mice fed with high fat diet. Biochem Biophys Res Commun 340: 1111-1118, 2006.
41. Mulder H, Yang S, Winzell MS, Holm C, Ahren B. Inhibition of lipase activity and lipolysis in rat islets reduces insulin secretion. Diabetes 53: 122-128, 2004.
42. Murphy DJ, Vance J. Mechanisms of lipid-body formation. Trends Biochem Sci 24: 109-115, 1999.
43. Nolan CJ, Madiraju MS, Delghingaro-Augusto V, Peyot ML, Prentki M. Fatty acid signaling in the beta-cell and insulin secretion. Diabetes 55, Suppl 2: S16-S23, 2006.
44. Nunemaker CS, Chen M, Pei H, Kimble SD, Keller SR, Carter JD, Yang Z, Smith KM, Wu R, Bevard MH, Garmey JC, Nadler JL. 12-Lipoxygenase-knockout mice are resistant to inflammatory effects of obesity induced by western diet. Am J Physiol Endocrinol Metab 295: E1065-E1075, 2008.
45. Poitout V, Robertson RP. Minireview: Secondary beta-cell failure in type 2 diabetes - a convergence of glucotoxicity and lipotoxicity. Endocrinology 143: 339-342, 2002. (Pubitemid 34107184)
46. Prentki M, Madiraju SR. Glycerolipid metabolism and signaling in health and disease. Endocr Rev 29: 647-676, 2008.
47. Prentki M, Nolan CJ. Islet beta cell failure in type 2 diabetes. J Clin Invest 116: 1802-1812, 2006.
48. Prentki M, Vischer S, Glennon MC, Regazzi R, Deeney JT, Corkey BE. Malonyl-CoA and long chain acyl-CoA esters as metabolic coupling factors in nutrient-induced insulin secretion. J Biol Chem 267: 5802-5810, 1992.
49. Sakada M, Tanaka A, Ohta D, Takayanagi M, Kodama T, Suzuki K, Inoue K, Fujita Y, Maruyama M. Severe steatosis resulted from anorexia nervosa leading to fatal hepatic failure. J Gastroenterol 41: 714-715, 2006.
50. Sako Y, Grill VE. A 48-hour lipid infusion in the rat time-dependently inhibits glucose-induced insulin secretion and B cell oxidation through a process likely coupled to fatty acid oxidation. Endocrinology 127: 1580-1589, 1990.
51. Schmitz-Peiffer C, Laybutt DR, Burchfield JG, Gurisik E, Narasimhan S, Mitchell CJ, Pedersen DJ, Braun U, Cooney GJ, Leitges M, Biden TJ. Inhibition of PKCepsilon improves glucose-stimulated insulin secretion and reduces insulin clearance. Cell Metab 6: 320-328, 2007.
52. Shimabukuro M, Zhou YT, Levi M, Unger RH. Fatty acid-induced beta cell apoptosis: a link between obesity and diabetes. Proc Natl Acad Sci USA 95: 2498-2502, 1998.
53. Stein DT, Stevenson BE, Chester MW, Basit M, Daniels MB, Turley SD, McGarry JD. The insulinotropic potency of fatty acids is influenced profoundly by their chain length and degree of saturation. J Clin Invest 100: 398-403, 1997.
54. Tamarit-Rodriguez J, Vara E, Tamarit J. Starvation-induced changes of palmitate metabolism and insulin secretion in isolated rat islets stimulated by glucose. Biochem J 221: 317-324, 1984. (Pubitemid 14052328)
55. Tansey JT, Sztalryd C, Gruia-Gray J, Roush DL, Zee JV, Gavrilova O, Reitman ML, Deng CX, Li C, Kimmel AR, Londos C. Perilipin ablation results in a lean mouse with aberrant adipocyte lipolysis, enhanced leptin production, and resistance to diet-induced obesity. Proc Natl Acad Sci USA 98: 6494-6499, 2001.
56. Unger RH. Minireview: weapons of lean body mass destruction: the role of ectopic lipids in the metabolic syndrome. Endocrinology 144: 5159-5165, 2003.
57. Varela GM, Antwi DA, Dhir R, Yin X, Singhal NS, Graham MJ, Crooke RM, Ahima RS. Inhibition of ADRP prevents diet-induced insulin resistance. Am J Physiol Gastrointest Liver Physiol 295: G621-G628, 2008.
58. Wang H, Hu L, Dalen K, Dorward H, Marcinkiewicz A, Russell D, Gong D, Londos C, Yamaguchi T, Holm C, Rizzo MA, Brasaemle D, Sztalryd C. Activation of hormone-sensitive lipase requires two steps, protein phosphorylation and binding to the PAT-1 domain of lipid droplet coat proteins. J Biol Chem 284: 32116-32125, 2009.
59. Wang H, Maechler P, Antinozzi PA, Herrero L, Hagenfeldt-Johansson KA, Bjorklund A, Wollheim CB. The transcription factor SREBP-1c is instrumental in the development of beta-cell dysfunction. J Biol Chem 278: 16622-16629, 2003.
60. Wei P, Taniguchi S, Sakai Y, Imamura M, Inoguchi T, Nawata H, Oda S, Nakabeppu Y, Nishimura J, Ikuyama S. Expression of adipose differentiation- related protein (ADRP) is conjointly regulated by PU.1 and AP-1 in macrophages. J Biochem 138: 399-412, 2005.
61. Winzell MS, Holm C, Ahren B. Downregulation of islet hormone-sensitive lipase during long-term high-fat feeding. Biochem Biophys Res Commun 304: 273-278, 2003. (Pubitemid 36444566)
62. Wolins NE, Quaynor BK, Skinner JR, Schoenfish MJ, Tzekov A, Bickel PE. S3-12, Adipophilin, and TIP47 package lipid in adipocytes. J Biol Chem 280: 19146-19155, 2005.
63. Wolins NE, Quaynor BK, Skinner JR, Tzekov A, Croce MA, Gropler MC, Varma V, Yao-Borengasser A, Rasouli N, Kern PA, Finck BN, Bickel PE. OXPAT/PAT-1 is a PPAR-induced lipid droplet protein that promotes fatty acid utilization. Diabetes 55: 3418-3428, 2006.
64. Xu G, Sztalryd C, Lu X, Tansey JT, Gan J, Dorward H, Kimmel AR, Londos C. Post-translational regulation of adipose differentiation-related protein by the ubiquitin/proteasome pathway. J Biol Chem 280: 42841-42847, 2005.
65. Yaney GC, Corkey BE. Fatty acid metabolism and insulin secretion in pancreatic beta cells. Diabetologia 46: 1297-1312, 2003.
66. Yaney GC, Korchak HM, Corkey BE. Long-chain acyl CoA regulation of protein kinase C and fatty acid potentiation of glucose-stimulated insulin secretion in clonal beta-cells. Endocrinology 141: 1989-1998, 2000.
67. Zhou YP, Ling ZC, Grill VE. Inhibitory effects of fatty acids on glucose-regulated B-cell function: association with increased islet triglyceride stores and altered effect of fatty acid oxidation on glucose metabolism. Metabolism 45: 981-986, 1996.