Diabetes Research and Clinical Practice
Volume 75, Issue 1 , Pages 14-26 , January 2007

Regulation of hormone-sensitive lipase in islets

  • Wen-Jun Shen

      Affiliations

    • Department of Medicine, Stanford University, Stanford, CA 94305, United States
    • VA Palo Alto Health Care System, Palo Alto, CA 94304, United States
    • Corresponding Author InformationCorresponding author at: Division of Endocrinology S025, Department of Medicine, Stanford University, Stanford, CA 94305-5103, United States. Tel.: +1 650 493 5000x60351; fax: +1 650 849 0215.
  • ,
  • Yu Liang

      Affiliations

    • Department of Medicine, Stanford University, Stanford, CA 94305, United States
  • ,
  • Jenny Wang

      Affiliations

    • Department of Medicine, Stanford University, Stanford, CA 94305, United States
  • ,
  • Kenji Harada

      Affiliations

    • Department of Medicine, Stanford University, Stanford, CA 94305, United States
  • ,
  • Shailja Patel

      Affiliations

    • Department of Medicine, Stanford University, Stanford, CA 94305, United States
  • ,
  • Sara A. Michie

      Affiliations

    • Department of Pathology, Stanford University, United States
  • ,
  • Jun-Ichi Osuga

      Affiliations

    • Department of Metabolic Disease, University of Tokyo, Tokyo 113, Japan
  • ,
  • Shun Ishibashi

      Affiliations

    • Department of Internal Medicine, Jichi Medical School, Tochigi, Japan
  • ,
  • Fredric B. Kraemer

      Affiliations

    • Department of Medicine, Stanford University, Stanford, CA 94305, United States
    • VA Palo Alto Health Care System, Palo Alto, CA 94304, United States

Received 22 November 2005 ,Accepted 3 May 2006.

References 

  1. Kraemer F, Shen W-J. Hormone-sensitive lipase: control of intracellular tri-(di-)acylglycerol and cholesteryl ester hydrolysis. J. Lipid Res. 2002;43:1585–1594
  2. Corkey B, Glennon MC, Chen KS, Deeney JT, Matschinsky FM, Prentki M. A role for malonyl-CoA in glucose-stimulated insulin secretion from clonal pancreatic-beta cells. J. Biol. Chem. 1989;264:21608–21612
  3. 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. 1992;267:5802–5810
  4. Brun T, Roche E, Assimacopoulos-Jeannet F, Corkey BE, Kim KH, Prentki M. Evidence for an anaplerotic/malonyl-CoA pathway in pancreatic b-cell nutrient signaling. Diabetes. 1996;45:190–198
  5. Chen S, Ogawa A, Ohneda M, Unger RH, Foster DW, McGarry JD. More direct evidence for a malonyl-CoA–carnitine palmitoyltransferase I interaction as key event in pancreatic beta-cell signaling. Diabetes. 1994;43:878–883
  6. Deeney J, Gromada J, Hoy M, Olsen HL, Rhodes CJ, Prentki M, et al. Acute stimulation with long chain acyl-CoA enhances exocytosis in insulin-secreting cells (HIT T-15 and NMRI beta-cells). J. Biol. Chem. 2000;275:9363–9368
  7. Nishizuka Y. Protein kinase C and lipid signaling for sustained cellular responses. FASEB J. 1995;9:484–496
  8. Konrad RJ, Major CD, Wolf BA. Diacylglycerol hydrolysis to arachidonic acid is necessary for insulin secretion from isolated pancreatic islets: sequential actions of diacylglycerol and monoacylglycerol lipases. Biochemistry. 1994;33:13284–13294
  9. Sheu L, Pasyk EA, Ji J, Huang X, Gao X, Varoqueaux F, et al. Regulation of insulin exocytosis by Munc13-1. J. Biol. Chem. 2003;278:27556–27563
  10. Malaisse W, Dunlop ME, Mathias PC. Stimulation of protein kinase C and insulin release by 1-oleoyl-2-acetyl-glycerol. Eur. J. Biochem. 1985;149:23–27
  11. Peter-Riesch B, Fathi M, Schlegel W, Wollheim CB. Glucose and carbachol generate 1,2-diacylglycerols by different mechanisms in pancreatic islets. J. Clin. Invest. 1988;81:1154–1161
  12. Arkhammar P, Juntti-Berggren L, Larsson O, Welsh M, Nanberg E, Sjoholm A, et al. Protein kinase C modulates the insulin secretory process by maintaining a proper function of the beta-cell voltage-activated Ca2+ channels. J. Biol. Chem. 1994;269:2743–2749
  13. Mulder H, Holst LS, Svensson H, Degerman E, Sundler F, Ahren B, et al. Hormone-sensitive lipase, the rate-limiting enzyme in triglyceride hydrolysis, is expressed and active in beta-cells. Diabetes. 1999;48:228–232
  14. Winzell M, Svensson H, Arner P, Ahren B, Holm C. The expression of hormone-sensitive lipase in clonal β-cells and rat islets is induced by long-term exposure to high glucose. Diabetes. 2001;50:2225–2230
  15. Roduit R, Masiello P, Wang SP, Li H, Mitchell GA, Prentki M. A role for hormone-sensitive lipase in glucose-stimulated insulin secretion. Diabetes. 2001;50:1970–1975
  16. Mulder H, Sorhede-Winzell M, Contreras JA, Fex M, Strom K, Ploug T, et al. Hormone-sensitive lipase null mice exhibit signs of impaired insulin sensitivity whereas insulin secretion is intact. J. Biol. Chem. 2003;278:36380–36388
  17. Harada K, Shen W-J, Patel S, Natu V, Wang J, Osuga JI, et al. Resistance to high fat diet-induced obesity associated with altered expression of adipose specific genes in hormone-sensitive lipase deficient mice. Am. J. Physiol. Endocrinol. Metab. 2003;285:E1182
  18. Mulder H, Yang S, Winzell MS, Holm C, Ahrén B. Inhibition of lipase activity and lipolysis in rat islets reduces insulin secretion. Diabetes. 2004;53:122–128
  19. Peyot M, Nolan CJ, Soni K, Joly E, Lussier R, Corkey BE, et al. Hormone-sensitive lipase has a role in lipid signaling for insulin secretion but is non-essential for the incretin action of glucagon-like peptide 1. Diabetes. 2004;53:1733–1742
  20. Claus LD, Liang TH, Salhanick Y, Lubeski AI, Yang CK, Lemoine L, et al. Specific inhibition of hormone-sensitive lipase improves lipid profile while reducing plasma glucose. J. Pharmacol. Exp. Ther. 2005;14:(Epub ahead of print)
  21. Osuga J, Ishibashi S, Oka T, Yagyu H, Tozawa R, Fujimoto A, et al. Targeted disruption of hormone-sensitive lipase results in male sterility and adipocyte hypertrophy, but not in obesity. Proc. Natl. Acad. Sci. U.S.A. 2000;97:787–792
  22. Cousin S, Hügl SR, Wrede CE, Kajio H, Myers MG, Rhodes CJ. Free fatty acid-induced inhibition of glucose and insulin-like growth factor i-induced deoxyribonucleic acid synthesis in the pancreatic β-cell line INS-1. Endocrinology. 2001;142:229–240
  23. Xu B, Wagner N, Pham LN, Magno V, Shan Z, Butcher EC, et al. Lymphocyte homing to bronchus-associated lymphoid tissue (BALT) is mediated by L-selectin/PNAd, 4β1 integrin/VCAM-1, and LFA-1 adhesion pathways. J. Exp. Med. 2003;197:1255–1267
  24. Shen W-J, Patel S, Natu V, Kraemer FB. Mutational analysis of structural features of rat hormone-sensitive lipase. Biochemistry. 1998;37:8973–8979
  25. Kraemer F, Patel S, Singh-Bist A, Gholami S, Saedi M, Sztalryd C. Detection of hormone-sensitive lipase in various tissues. II. Regulation in the rat testis by human chorionic gonadotropin. J. Lipid Res. 1993;34:609–616
  26. Fex M, Olofsson CS, Fransson U, Bacos K, Lindvall H, Sorhede-Winzell M, et al. Hormone-sensitive lipase deficiency in mouse islets abolishes neutral cholesterol ester hydrolase activity but leaves lipolysis, acylglycerides, fat oxidation, and insulin secretion intact. Endocrinology. 2004;145:3746–3753
  27. Osuga J, Ishibashi S, Oka T, Yagyu H, Tozawa R, Fujimoto A, et al. Targeted disruption of hormone-sensitive lipase results in male sterility and adipocyte hypertrophy, but not in obesity. Proc. Natl. Acad. Sci. U.S.A. 2000;97:787–792
  28. Kraemer F, Shen WJ, Harada K, Patel S, Osuga J, Ishibashi S, et al. Hormone-sensitive lipase is required for high-density lipoprotein cholesteryl ester-supported adrenal steroidogenesis. Mol. Endocrinol. 2004;18:549–557
  29. Scearce LM, Brestelli JE, McWeeney SK, Lee CS, Mazzarelli J, Pinney DF, et al. Functional genomics of the endocrine pancreas: the pancreas clone set and PancChip, new resources for diabetes research. Diabetes. 2002;51:1997–2004
  30. Tusher V, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. U.S.A. 2001;97:5116–5121
  31. Liang Y, Zhu J, Lemoin L, Salhanick A, Lowe D, Clairmont KB. Inhibition of hormone-sensitive lipase (HSL) reduces GLP-1, CCK and acetylcholine stimulated insulin release from isolated rat pancreatic islets. Diabetes. 2002;51:A359
  32. Winzell MS, Holm C, Ahren B. Downregulation of islet hormone-sensitive lipase during long-term high-fat feeding. Biochem. Biophys. Res. Commun. 2003;304:273–278
  33. Listenberger L, Han X, Lewis SE, Cases S, Farese RV, Ory DS, et al. Triglyceride accumulation protects against fatty acid-induced lipotoxicity. Proc. Natl. Acad. Sci. U.S.A. 2003;100:3077–3082
  34. Jenkins-Kruchten AE, Bennaars-Eiden A, Ross JR, Shen W-J, Kraemer FB, Bernlohr DA. Fatty acid binding protein–hormone-sensitive lipase interaction; fatty acid dependence on binding. J. Biol. Chem. 2003;(Epub)
  35. Deng T, Shan S, Li PP, Shen ZF, Lu XP, Cheng J, et al. Peroxisome proliferator-activated receptor-gamma transcriptionally up-regulates hormone-sensitive lipase via the involvement of specificity protein-1. Endocrinology. 2006;147:875–884(Epub 2005, November 2003)
  36. Yaney G, Civelek VN, Richard AM, Dillon JS, Deeney JT, Hamilton JA, et al. Glucagon-like peptide 1 stimulates lipolysis in clonal pancreatic beta-cells (HIT). Diabetes. 2001;50:56–62
  37. MacDonald P, El-Kholy W, Riedel MJ, Salapatek AM, Light PE, Wheeler MB. The multiple actions of GLP-1 on the process of glucose-stimulated insulin secretion. Diabetes. 2002;51:S434–S442
  38. Wang M-Y, Lee Y, Unger RH. Novel form of lipolysis induced by leptin. J. Biol. Chem. 1999;274:17541–17544
  39. Widdup G, Bryson JM, Pawlak D, Phuyal JL, Denyer GS, Caterson ID. In vivo and in vitro suppression by leptin of glucose-stimulated insulin hypersecretion in high glucose-fed rats. Eur. J. Endocrinol. 2000;143:431–437
  40. Kawai T, Hirose H, Seto Y, Fujita H, Saruta T. Chronic effects of different fatty acids and leptin in INS-1 cells. Diabetes Res. Clin. Pract. 2001;51:1–8
  41. Rhodes CJ. Type 2 diabetes-a matter of β-cell life and death?. Science. 2005;307:380–384
  42. Louveau I, Gondret F. GH and insulin affect fatty acid synthase activity in isolated porcine adipocytes in culture without any modifications of sterol regulatory element binding protein-1 expression. J. Endocrinol. 2004;181:271–280
  43. Chan C, De-Leo D, Joseph JW, McQuaid TS, Ha XF, Xu F, et al. Increased uncoupling protein-2 levels in beta-cells are associated with impaired glucose-stimulated insulin secretion: mechanism of action. Diabetes. 2001;50:1302–1310
  44. Joseph J, Koshkin V, Zhang CY, Wang J, Lowell BB, Chan CB, et al. Uncoupling protein 2 knockout mice have enhanced insulin secretory capacity after a high-fat diet. Diabetes. 2002;51:3211–3219
  45. Li L, Skorpen F, Egeberg K, Jorgensen IH, Grill V. Induction of uncoupling protein 2 mRNA in beta-cells is stimulated by oxidation of fatty acids but not by nutrient oversupply. Endocrinology. 2002;143:1371–1377
  46. Medvedev A, Robidoux J, Bai X, Cao W, Floering LM, Daniel KW, et al. Regulation of the uncoupling protein-2 gene in INS-1 beta-cells by oleic acid. J. Biol. Chem. 2002;277:42639–42644
  47. Lupi R, Dotta F, Marselli L, Guerra SD, Masini M, Santangelo C, et al. Prolonged exposure to free fatty acids has cytostatic and pro-apoptotic effects on human pancreatic islets: evidence that beta-cell death is caspase mediated, partially dependent on ceramide pathway, and Bcl-2 regulated. Diabetes. 2002;51:1437–1442
  48. Lameloise N, Muzzin P, Prentki M, Assimacopoulos-Jeannet F. Uncoupling protein 2: a possible link between fatty acid excess and impaired glucose-induced insulin secretion?. Diabetes. 2001;50:803–809
  49. Armstrong M, Towel HC. Polyunsaturated fatty acids stimulate hepatic UCP-2 expression via a PPARalpha-mediated pathway. Am. J. Physiol. Endocrinol. Metab. 2001;281:E1197–E1204
  50. Darville M, Eizirik DL. Cytokine induction of Fas gene expression in insulin-producing cells requires the transcription factors NF-kappaB and C/EBP. Diabetes. 2001;50:1741–1748
  51. Prentki M, Wang SP, Raphael R, Li H, Mitchell G, Masiello P. Hormone-sensitive lipase is essential for glucose stimulated insulin secretion. Diabetes. 2001;50:A52
  52. Winzell MS, Svensson H, Enerback S, Ravnskjaer K, Mandrup S, Esser V, et al. Pancreatic β-cell lipotoxicity induced by overexpression of homrone-sensitive lipase. Diabetes. 2003;52:2057–2065

PII: S0168-8227(06)00175-6

doi: 10.1016/j.diabres.2006.05.001

Diabetes Research and Clinical Practice
Volume 75, Issue 1 , Pages 14-26 , January 2007