Lipases in the pancreatic β-cell: Implications for insulin secretion

Biochemical Society Transactions

Volumn 36, Issue 5, 2008, Pages 885-890

  Fox, Malin ^a   Mulder, Hindrik ^a  

^a LUND UNIVERSITY DIABETES CENTRE   (Sweden)

Author keywords

Coupling signal; Fatty acid; Islet; Lipolysis; Orlistat; Triacylglycerol

Indexed keywords

ACYLGLYCEROL; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; CARBOXYLESTER LIPASE; ESTERASE; GLUCOSE; HORMONE SENSITIVE LIPASE; INSULIN; LIPOPROTEIN LIPASE; TETRAHYDROLIPSTATIN; TRIACYLGLYCEROL LIPASE; UNCLASSIFIED DRUG;

ADIPOCYTE; CELL METABOLISM; CELLULAR DISTRIBUTION; CONFERENCE PAPER; ENZYME ACTIVITY; ENZYME SPECIFICITY; GENE INACTIVATION; GENETIC SUSCEPTIBILITY; GLUCOSE HOMEOSTASIS; GLUCOSE INTOLERANCE; GLUCOSE OXIDATION; HYPERGLYCEMIA; INSULIN RELEASE; INSULIN SENSITIVITY; LIPID HYDROLYSIS; LIPID METABOLISM; LIPOLYSIS; NONHUMAN; PANCREAS ISLET BETA CELL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION;

ADIPOCYTES; ANIMALS; GLUCOSE; HOMEOSTASIS; INSULIN; INSULIN-SECRETING CELLS; LIPASE; LIPID METABOLISM; MICE; MICE, KNOCKOUT; PHENOTYPE; STEROL ESTERASE;

MUS; RODENTIA;

EID: 53849110273     PISSN: 03005127     EISSN: None     Source Type: Journal    
DOI: 10.1042/BST0360885     Document Type: Conference Paper

References (50)

1. Unger, R.H. (1995) Lipotoxicity in the pathogenesis of obesity-dependent NIDDM: genetic and clinical implications. Diabetes 44, 863-870
2. Koyama, K., Chen, G., Wang, M.Y., Lee, Y., Shimabukuro, M., Newgard, C.B. and Unger, R.H. (1997) β-Cell function in normal rats made chronically hyperleptinemic by adenovirus-leptin gene therapy. Diabetes 46, 1276-1280
3. Chen, G., Koyama, K., Yuan, X., Lee, Y., Zhou, Y.T., O'Doherty, R., Newgard, C.B. and Unger, R.H. (1996) Disappearance of body fat in normal rats induced by adenovirus-mediated leptin gene therapy. Proc. Natl. Acad. Sci. U.S.A. 93, 14795-14799
4. Stein, D.T., Esser, V., Stevenson, B.E., Lane, K.E., Whiteside, J.H., Daniels, M.B., Chen, S. and McGarry, J.D. (1996) Essentiality of circulating fatty acids for glucose-stimulated insulin secretion in the fasted rat. J. Clin. Invest. 97, 2728-2735
5. Dobbins, R.L., Chester, M.W., Daniels, M.B., McGarry, J.D. and Stein, D.T. (1998) Circulating fatty acids are essential for efficient glucose-stimulated insulin secretion after prolonged fasting in humans. Diabetes 47, 1613-1618
6. Prentki, M. and Corkey, B.E. (1996) Are the β-cell signaling molecules malonyl-CoA and cystolic long-chain acyl-CoA implicated in multiple tissue defects of obesity and NIDDM? Diabetes 45, 273-283
7. Corkey, B.E, Glennon, M.C., Chen, K.S., Deeney, J.T., Matschinsky, F.M. and Prentki, M. (1989) A role for malonyl-CoA in glucose-stimulated insulin secretion from clonal pancreatic β-cells. J. Biol. Chem. 264, 21608-21612
8. McGarry, J.D. and Brown, N.F. (1997) The mitochondrial carnitine palmitoyltransferase system: from concept to molecular analysis. Eur. J. Biochem. 244, 1-14
9. Lee, Y., Hirose, H., Ohneda, M., Johnson, J.H., McGarry, J.D. and Unger, R.H. (1994) β-Cell lipotoxicity in the pathogenesis of non-insulin-dependent diabetes mellitus of obese rats: impairment in adipocyte-β-cell relationships. Proc. Natl. Acad. Sci. U.S.A. 91, 10878-10882
10. Henquin, J.C. (2000) Triggering and amplifying pathways of regulation of insulin secretion by glucose. Diabetes 49, 1751-1760
11. Mulder, H., Yang, S., Sörhede Winzell, M., Holm, C. and Ahrén, B. (2004) Inhibition of lipase activity and lipolysis in rat islets reduces insulin secretion. Diabetes 53, 122-128
12. Smith, G.M., Garton, A.J., Aitken, A. and Yeaman, S.J. (1996) Evidence for a multi-domain structure for hormone-sensitive lipase. FEBS Lett. 396, 90-94
13. Ballinger, A. and Peikin, S.R. (2002) Orlistat: its current status as an anti-obesity drug. Eur. J. Pharmacol. 440, 109-117
14. Ko, J. and Small, D.M. (1997) Behavior of tetrahydrolipstatin in biological model membranes and emulsions. J. Lipid Res. 38, 1544-1552
15. Yaney, G.C., Civelek, V.N., Richard, A.M,, Dillon, J.S., Deeney, J.T., Hamilton, J.A., Korchak, H.M., Tornheim, K., Corkey, B.E. and Boyd, 3rd, A.E. (2001) Glucagon-like peptide 1 stimulates lipolysis in clonal pancreatic β-cells (HIT). Diabetes 50, 56-62
16. Cunningham, B.A., Richard, A.M., Dillon, J.S., Daley, J.T., Civelek, V.N., Deeney, J.T., Yaney, G.C., Corkey, B.E. and Tornheim, K. (2003) Glucagon-like peptide 1 and fatty acids amplify pulsatile insulin secretion from perifused rat islets. Biochem. J. 369, 173-178
17. Sörhede Winzell, M., Ström, K., Holm, C. and Ahrén, B. (2006) Glucose-stimulated insulin secretion correlates with β-cell lipolysis. Nutr. Metab. Cardiovasc. Dis. 16, (Suppl. 1), S11-S16
18. Peyot, M.L., Nolan, C.J., Soni, K., Joly, F., Lussier, R., Corkey, B.E., Wang, S.P., Mitchell, G.A. and Prentki, M. (2004) Hormone-sensitive lipase has a role in lipid signaling for insulin secretion but is nonessential for the incretin action of glucagon-like peptide 1. Diabetes 53, 1733-1742
19. Masiello, P., Novelli, M., Bombara, M., Fierabracci, V., Vittorini, S., Prentki, M. and Bergamini, F. (2002) The antilipolytic agent 3,5-dimethylpyrazole inhibits insulin release in response to both nutrient secretagogues and cyclic adenosine monophosphate agonists in isolated rat islets. Metabolism 51, 110-114
20. Claus, T.H., Lowe, D.B., Liang, Y., Salhanick, A.I., Lubeski, C.K., Yang, L., Lemoine, I., Zhu, J. and Clairmont, K.B. (2005) Specific inhibition of hormone-sensitive lipase improves lipid profile while reducing plasma glucose. J. Pharmacol. Exp. Ther. 315, 1396-1402
21. Berne, C. (1975) The metabolism of lipids in mouse pancreatic islets: the biosynthesis of triacylglycerols and phospholipids. Biochem. J. 152, 667-673
22. Malaisse, W.J., Malaisse-Lagae, F., Sener, A. and Hellerstrom, C. (1985) Participation of endogenous fatty acids in the secretory activity of the pancreatic β-cell. Biochem. J. 227, 995-1002
23. Mulder, H., Holst, L.S., Svensson, H., Degerman, F., Sundler, F., Ahren, B., Rorsman, P. and Holm, C. (1999) Hormone-sensitive lipase, the rate-limiting enzyme in triglyceride hydrolysis, is expressed and active in β-cells. Diabetes 48, 228-232
24. Lindvall, H., Nevsten, P., Ström, K., Wallenberg, R., Sundler, F., Langin, D., Sörhede Winzell, M. and Holm, C. (2004) A novel hormone-sensitive lipase isoform expressed in pancreatic β-cells. J. Biol. Chem. 279, 3828-3836
25. Sörhede-Winzell, S., Svensson, H., Arner, P., Ahrén, B. and Holm, C. (2001) The expression of hormone-sensitive lipase in clonal β-cells and rat islets is induced by long-term exposure to high glucose. Diabetes 50, 2225-2230
26. Sörhede Winzell, M., Holm, C. and Ahrén, B. (2003) Downregulation of islet hormone-sensitive lipase during long-term high-fat feeding. Biochem. Biophys. Res. Commun. 304, 273-278
27. Zimmermann, R., Strauss, J.G., Haemmerle, G., Schoiswohl, G., Birner-Gruenberger, R., Riederer, M., Lass, A., Neuberger, G., Eisenhaber, F., Hermetter, A. and Zechner, R. (2004) Fat mobilization in adipose tissue is promoted by adipose triglyceride lipase. Science 306, 1383-1386
28. Villena, J.A., Roy, S., Sarkadi-Nagy, E., Kim, K.H. and Sul, H.S. (2004) Desnutrin, an adipocyte gene encoding a novel patatin domain-containing protein, is induced by fasting and glucocorticoids: ectopic expression of desnutrin increases triglyceride hydrolysis. J. Biol. Chem. 279, 47066-47075
29. 2 family members possessing triacylglycerol lipase and acylglycerol transacylase activities. J. Biol. Chem. 279, 48968-48975
30. Fex, M., Lucas, S., Sörhede Winzell, M., Ahrén, B., Holm, C. and Mulder, H. (2006) β-Cell lipases and insulin secretion. Diabetes 55, S24-S31
31. Raeder, H., Johansson, S., Holm, P.I., Haldorsen, I.S., Mas, E., Sbarra, V., Nermoen, I., Eide, S.A., Grevle, L., Bjorkhaug, L. et al. (2006) Mutations in the CEL VNTR cause a syndrome of diabetes and pancreatic exocrine dysfunction. Nat. Genet. 38, 54-62
32. Vesterhus, M., Raeder, H., Johansson, S., Molven, A. and Njolstad, P.R. (2008) Pancreatic exocrine dysfunction in maturity-onset diabetes of the young type 3. Diabetes Care 31, 306-310
33. Weng, W., Li, L., van Bennekum, A.M., Potter, S.H., Harrison, E.H., Blaner, W.S., Breslow, J.L. and Fisher, E.A. (1999) Intestinal absorption of dietary cholesteryl ester is decreased but retinyl ester absorption is normal in carboxyl ester lipase knockout mice. Biochemistry 38, 4143-4149
34. Osuga, J.I., S. Oka, T., Yagyu, H., Tozawa, R., Fujimoto, A., Shionoiri, F., Yahagi, N., Kraemer, F.B., Tsutsumi, O. and Yamada, N. (2000) Targeted disruption of hormone-sensitive lipase results in male sterility and adipocyte hypertrophy, but not in obesity. Proc. Natl. Acad. Sci. U.S.A. 18, 787-792
35. Wang, S.P., Laurin, N., Himms-Hagen, J., Rudnicki, M.A., Levy, E., Robert, M.F., Pan, L., Oligny, L. and Mitchell, G.A. (2001) The adipose tissue phenotype of hormone-sensitive lipase deficiency in mice. Obes. Res. 9, 119-128
36. Haemmerle, G., Zimmermann, R., Hayn, M., Theussl, C., Waeg, G., Wagner, E., Sattler, W., Magin, T.M., Wagner, E.F. and Zechner, R. (2002) Hormone-sensitive lipase deficiency in mice causes diglyceride accumulation in adipose tissue, muscle, and testis. J. Biol. Chem. 277, 4806-4815
37. Mulder, H., Sörhede-Winzell, M., Contreras, J.-A., Fex, M., Ström, K., Ploug, T., Galbo, H., Arner, P., Lundberg, C., Sundler, F. et al. (2003) Hormone-sensitive lipase null mice exhibit signs of impaired insulin sensitivity whereas insulin secretion is intact. J. Biol. Chem. 278, 36380-36388
38. Chung, S., Wang, S.P., Pan, L., Mitchell, G., Trasler, J. and Hermo, L. (2001) Infertility and testicular defects in hormone-sensitive lipase-deficient mice. Endocrinology 142, 4272-4281
39. Wang, S.P., Chung, S., Soni, K., Bourdages, H., Hermo, L., Trasler, J. and Mitchell, G.A. (2004) Expression of human hormone-sensitive lipase (HSL) in postmeiotic germ cells confers normal fertility to HSL-deficient mice. Endocrinology 145, 5688-5693
40. Okazaki, H., Osuga, J., Tamura, Y., Yahagi, N., Tomita, S., Shionoiri, F., Iizuka, Y., Ohashi, K., Harada, K., Kimura, S. et al. (2002) Lipolysis in the absence of hormone-sensitive lipase: evidence for a common mechanism regulating distinct lipases. Diabetes 51, 3368-3375
41. Rydén, M., Jocken, J., van Harmelen, V., Dicker, A., Hoffstedt, J., Wirén, M., Blomqvist, L., Mairal, A., Langin, D., Blaak, E. and Arner, P. (2007) Comparative studies of the role of hormone-sensitive lipase and adipose triglyceride lipase in human fat cell lipolysis. Am. J. Physiol. Endocrinol. Metab. 292, E1847-E1855
42. Roduit, R., Masiello, P., Wang, S.P., Li, H., Mitchell, G.A. and Prentki, M. (2001) A role for hormone-sensitive lipase in glucose-stimulated insulin secretion: a study in hormone-sensitive lipase-deficient mice. Diabetes 50, 1970-1975
43. Voshol, P.J., Haemmerle, G., Ouwens, D.M., Zimmermann, R., Zechner, R., Teusink, B., Maassen, J.A., Havekes, L.M. and Romijn, J.A. (2003) Increased hepatic insulin sensitivity together with decreased hepatic triglyceride stores in hormone-sensitive lipase-deficient mice. Endocrinology 144, 3456-3462
44. Harada, K., Shen, W.-J., Patel, S., Natu, V., Wang, J., Osuga, J.-i., Ishibashi, S. and Kraemer, F.B. (2003) Resistance to high-fat diet-induced obesity and altered expression of adipose-specific genes in HSL-deficient mice. Am. J. Physiol. Endocrinol. Metab. 285, E1182-E1195
45. Park, S.Y., Kim, H.J., Wang, S., Higashimori, T., Dong, J., Kim, Y.J., Cline, G., Li, H., Prentki, M., Shulman, G.I. et al. (2005) Hormone-sensitive lipase knockout mice have increased hepatic insulin sensitivity and are protected from short-term diet-induced insulin resistance in skeletal muscle and heart. Am. J. Physiol. Endocrinol. Metab. 289, E30-E39
46. Fex, M., Olofsson, C.S., Fransson, U., Bacos, K., Lindvall, H., Sorhede-Winzell, M., Rorsman, P., Holm, C. and Mulder, H. (2004) Hormone-sensitive lipase deficiency in mouse islets abolishes neutral cholesterol ester hydrolase activity but leaves lipolysis, acylglycerides, fat oxidation, and insulin secretion intact. Endocrinology 145, 3746-3753
47. Kulkarni, R.N., Almind, K., Goren, H.J., Winnay, J.N., Ueki, K., Okada, T. and Kahn, C.R. (2003) Impact of genetic background on development of hyperinsulinemia and diabetes in insulin receptor/insulin receptor substrate-1 double heterozygous mice. Diabetes 52, 1528-1534
48. Gannon, M., Shiota, C., Postic, C., Wright, C.V. and Magnuson, M. (2000) Analysis of the Cre-mediated recombination driven by rat insulin promoter in embryonic and adult mouse pancreas. Genesis 26, 139-142
49. Lee, J.Y., Ristow, M., Lin, X., White, M.F., Magnuson, M.A. and Hennighausen, L. (2006) RIP-Cre revisited, evidence for impairments of pancreatic β-cell function. J. Biol. Chem. 281, 2649-2653
50. Fex, M., Wierup, N., Nitert, M.D., Ristow, M. and Mulder, H. (2007) Rat insulin promoter 2-Cre recombinase mice bred onto a pure C57BL/6J background exhibit unaltered glucose tolerance. J. Endocrinol. 194, 551-555