GIP increases human adipocyte LPL expression through CREB and TORC2-mediated trans-activation of the LPL gene

Journal of Lipid Research

Volumn 51, Issue 11, 2010, Pages 3145-3157

  Kim, Su Jin ^a   Nian, Cuilan ^a   McIntosh, Christopher H S ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Adenosine 3 ,5 cyclic monophosphate; cAMP response element binding protein; cAMP responsive CREB coactivator 2; Glucose dependent insulinotropic polypeptide; Lipoprotein lipase

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSIVE CYCLIC AMP RESPONSIVE ELEMENT BINDING COACTIVATOR 2 PROTEIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DACTINOMYCIN; GASTRIC INHIBITORY POLYPEPTIDE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; INSULIN; LIPOPROTEIN LIPASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ADIPOCYTE; ADULT; ARTICLE; CELL NUCLEUS; CELL STRAIN HEK293; CONTROLLED STUDY; FEMALE; GENE CONTROL; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE LOCATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; NORMAL HUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RNA INTERFERENCE; TRANSACTIVATION; UPREGULATION;

ACTIVE TRANSPORT, CELL NUCLEUS; ADIPOCYTES; ADULT; AMP-ACTIVATED PROTEIN KINASES; CELL NUCLEUS; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; FEMALE; GASTRIC INHIBITORY POLYPEPTIDE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HEK293 CELLS; HUMANS; LIPOPROTEIN LIPASE; MIDDLE AGED; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHOPROTEINS; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS C-AKT; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION;

EID: 78149350158     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M006841     Document Type: Article

References (53)

1. Drucker, D. J., and M. A. Nauck. 2006. The incretin system: glucagon-like peptide-1 receptor agonists and dipeptidyl peptidase-4 inhibitors in type 2 diabetes. Lancet. 368: 1696-1705.
2. McIntosh, C. H. S., S. Widenmaier, and S. J. Kim. 2009. Glucose-dependent insulinotropic polypeptide (Gastric Inhibitory Polypeptide; GIP). Vitam. Horm. 80: 409-471.
3. Davidson, M. B., G. Bate, and P. Kirkpatrick. 2005. Exenatide. Nat. Rev. Drug Discov. 4: 713-714.
4. Harder, H., L. Nielsen, D. T. T. Tu, and A. Astrup. 2004. The effect of liraglutide, a long-acting glucagon-like peptide 1 derivative, on glycemic control, body composition, and 24-h energy expenditure in patients with type 2 diabetes. Diabetes Care. 27: 1915-1921. (Pubitemid 38989232)
5. DeFronzo, R. A., R. E. Ratner, J. Han, D. D. Kim, M. S. Fineman, and A. D. Baron. 2005. Effects of exenatide (exendin-4) on glycemic control and weight over 30 weeks in metformin-treated patients with type 2 diabetes. Diabetes Care. 28: 1092-1100.
6. Deacon, C. F. 2007. Dipeptidyl peptidase 4 inhibition with sitagliptin: a new therapy for type 2 diabetes. Expert Opin. Investig. Drugs. 16: 533-545.
7. Rosenstock, J., M. A. Baron, S. Dejager, D. Mills, and A. Schweizer. 2007. Comparison of vildagliptin and rosiglitazone monotherapy in patients with type 2 diabetes: a 24-week, double-blind, randomized trial. Diabetes Care. 30: 217-223. (Pubitemid 46198322)
8. McIntosh, C. H. S. 2008. Dipeptidyl peptidase IV inhibitors and diabetes therapy. Front. Biosci. 13: 1753-1773.
9. Brubaker, P. L., and D. J. Drucker. 2004. Minireview: Glucagon-like peptides regulate cell proliferation and apoptosis in the pancreas, gut, and central nervous system. Endocrinology. 145: 2653-2659.
10. Drucker, D. J. 2007. The role of gut hormones in glucose homeostasis. J. Clin. Invest. 117: 24-32.
11. Yusta, B., L. L. Baggio, J. L. Estall, J. A. Koehler, D. P. Holland, H. Li, D. Pipeleers, Z. Ling, and D. J. Drucker. 2006. GLP-1 receptor activation improves beta cell function and survival following induction of endoplasmic reticulum stress. Cell Metab. 4: 391-406.
12. Ehses, J. A., V. R. Casilla, T. Doty, J. A. Pospisilik, K. D. Winter, H. U. Demuth, R. A. Pederson, and C. H. S. McIntosh. 2003. Glucose-dependent insulinotropic polypeptide promotes beta-(INS-1) cell survival via cyclic adenosine monophosphate-mediated caspase-3 inhibition and regulation of p38 mitogen-activated protein kinase. Endocrinology. 144: 4433-4445.
13. Kim, S. J., K. Winter, C. Nian, M. Tsuneoka, Y. Koda, and C. H. S. McIntosh. 2005. Glucose-dependent insulinotropic polypeptide (GIP) stimulation of pancreatic beta-cell survival is dependent upon phosphatidylinositol 3-kinase (PI3K)/protein kinase B (PKB) signaling, inactivation of the forkhead transcription factor Foxo1, and down-regulation of bax expression. J. Biol. Chem. 280: 22297-22307.
14. Kim, S. J., C. Nian, S. Widenmaier, and C. H. S. McIntosh. 2008. Glucose-dependent insulinotropic polypeptide mediated up-regulation of β-cell anti-apoptotic Bcl-2 gene expression is coordinated by cAMP-response element binding protein (CREB) and cAMP-responsive CREB coactivator 2. Mol. Cell. Biol. 28: 1644-1656.
15. Widenmaier, S. B., Z. Ao, S. J. Kim, G. Warnock, and C. H. S. McIntosh. 2009. Suppression of p38 MAPK and JNK via Akt-mediated inhibition of apoptosis signal regulating kinase 1 constitutes a core component of the beta-cell pro-survival effects of glucose-dependent insulinotropic polypeptide. J. Biol. Chem. 284: 30372-30382.
16. Spiegelman, B. M., and J. S. Flier. 2001. Obesity and the regulation of energy balance. Cell. 104: 531-543.
17. MacDougald, O. A., and S. Mandrup. 2002. Adipogenesis: forces that tip the scales. Trends Endocrinol. Metab. 13: 5-11.
18. Attie, A. D., and P. E. Scherer. 2009. Adipocyte metabolism and obesity. J. Lipid Res. 50: S395-S399.
19. Pederson, R. A., H. E. Schubert, and J. C. Brown. 1975. Gastric inhibitory polypeptide. Its physiologic release and insulinotropic action in the dog. Diabetes. 24: 1050-1056.
20. Krarup, T. 1988. Immunoreactive gastric inhibitory polypeptide. Endocr. Rev. 9: 122-134.
21. Wasada, T., K. McCorkle, V. Harris, K. Kawai, B. Howard, and R. H. Unger. 1981. Effect of gastric inhibitory polypeptide on plasma levels of chylomicron triglycerides in dogs. J. Clin. Invest. 68: 1106-1107.
22. Ebert, R., M. Nauck, and W. Creutzfeldt. 1991. Effect of exogenous or endogenous gastric inhibitory polypeptide (GIP) on plasma triglyceride responses in rats. Horm. Metab. Res. 23: 517-521.
23. Jorde, R., J. E. Pettersen, and P. G. Burhol. 1984. Lack of effect of exogenous or endogenous gastric inhibitory polypeptide on the elimination rate of Intralipid in man. Acta Med. Scand. 216: 19-23.
24. Ohneda, A., T. Kobayashi, and J. Nihei. 1983. Effect of endogenous gastric inhibitory polypeptide (GIP) on the removal of triacylglycerol in dogs. Regul. Pept. 6: 25-32.
25. McIntosh, C. H. S., I. Bremsak, F. C. Lynn, R. Gill, S. A. Hinke, R. Gelling, C. Nian, G. McKnight, S. Jaspers, and R. A. Pederson. 1999. Glucose-dependent insulinotropic polypeptide stimulation of lipolysis in differentiated 3T3-L1 cells: wortmannin-sensitive inhibition by insulin. Endocrinology. 140: 398-404.
26. Yip, R. G., and M. M. Wolfe. 2000. GIP biology and fat metabolism. Life Sci. 66: 91-103.
27. Kim, S. J., C. Nian, and C. H. S. McIntosh. 2007. Activation of lipoprotein lipase by glucose- dependent insulinotropic polypeptide in adipocytes. A role for a protein kinase B, LKB1, and AMP-activated protein kinase cascade. J. Biol. Chem. 282: 8557-8567.
28. Kim, S. J., C. Nian, and C. H. S. McIntosh. 2007. Resistin is a key mediator of glucose-dependent insulinotropic polypeptide (GIP) stimulation of lipoprotein lipase (LPL) activity in adipocytes. J. Biol. Chem. 282: 34139-34147.
29. Eckel, R. H., W. Y. Fujimoto, and J. D. Brunzell. 1979. Gastric inhibitory polypeptide enhanced lipoprotein lipase activity in cultured preadipocytes. Diabetes. 28: 1141-1142.
30. Knapper, J. M., S. M. Puddicombe, L. M. Morgan, and J. M. Fletcher. 1995. Investigations into the actions of glucose-dependent insulinotropic polypeptide and glucagon-like peptide-1(7-36)amide on lipoprotein lipase activity in explants of rat adipose tissue. J. Nutr. 125: 183-188.
31. Schreiber, E., P. Matthias, M. M. Muller, and W. Schaffner. 1989. Rapid detection of octamer binding proteins with 'mini-extracts', prepared from a small number of cells. Nucleic Acids Res. 17: 6419.
32. Kim, S. J., W. S. Choi, J. S. Han, G. Warnock, D. Fedida, and C. H. S. McIntosh. 2005. A novel mechanism for the suppression of a voltage-gated potassium channel by glucose-dependent insulinotropic polypeptide: protein kinase A-dependent endocytosis. J. Biol. Chem. 280: 28692-28700.
33. Peinado-Onsurbe, J., B. Staels, S. Deeb, and J. Auwerx. 1992. Lipoprotein lipase expression in undifferentiated hepatoma cells is regulated by progesterone and protein kinase A. Biochemistry. 31: 10121-10128.
34. Staels, B., G. Martin, M. Martinez, C. Albert, J. Peinado-Onsurbe, R. Saladin, D. W. Hum, M. Reina, S. Vilaro, and J. Auwerx. 1996. Expression and regulation of the lipoprotein lipase gene in human adrenal cortex. J. Biol. Chem. 271: 17425-17432.
35. Merkel, M., R. H. Eckel, and R. H. Goldberg. 2002. Lipoprotein lipase: genetics, lipid uptake, and regulation. J. Lipid Res. 43: 1997-2006.
36. Vinson, C., M. Myakishev, A. Acharya, A. A. Mir, J. R. Moll, and M. Bonovich. 2002. Classification of human B-ZIP proteins based on dimerization properties. Mol. Cell. Biol. 22: 6321-6335.
37. Gonzalez, G. A., and M. R. Montminy. 1989. Cyclic AMP stimulates somatostatin gene transcription by phosphorylation of CREB at serine 133. Cell. 59: 675-680.
38. Du, K., H. Asahara, U. S. Jhala, B. L. Wagner, and M. Montminy. 2000. Characterization of a CREB gain-of-function mutant with constitutive transcriptional activity in vivo. Mol. Cell. Biol. 20: 4320-4327.
39. Conkright, M. D., G. Canettieri, R. Screaton, E. Guzman, L. Miraglia, J. B. Hogenesch, and M. Montminy. 2003. TORCs: transducers of regulated CREB activity. Mol. Cell. 12: 413-423.
40. Xu, W., L. H. Kasper, S. Lerach, T. Jeevan, and P. K. Brindle. 2007. Individual CREB-target genes dictate usage of distinct cAMP-responsive coactivation mechanisms. EMBO J. 26: 2890-2903.
41. Oben, J., L. Morgan, J. Fletcher, and V. Marks. 1991. Effect of the entero-pancreatic hormones, gastric inhibitory polypeptide and glucagon-like polypeptide-1(7-36) amide, on fatty acid synthesis in explants of rat adipose tissue. J. Endocrinol. 130: 267-272.
42. Beck, B., and J. P. Max. 1986. Direct metabolic effects of gastric inhibitory polypeptide (GIP): dissociation at physiological levels of effects on insulin-stimulated fatty acid and glucose incorporation in rat adipose tissue. Diabetologia. 29: 68.
43. Wang, H., and R. H. Eckel. 2009. Lipoprotein lipase: from gene to obesity. Am. J. Physiol. Endocrinol. Metab. 297: E271-E288.
44. Kirchgessner, T. G., J. C. Chuat, C. Heinzmann, J. Etienne, S. Guilhot, K. Svenson, D. Ameis, C. Pilon, L. D'Auriol, A. Andalibi, et al. 1989. Organization of the human lipoprotein lipase gene and evolution of the lipase gene family. Proc. Natl. Acad. Sci. USA 86: 9647-9651.
45. Bey, L., J. Etienne, C. Tse, D. Brault, L. Noe, A. Raisonnier, F. Arnault, M. T. Hamilton, and F. Galibert. 1998. Cloning, sequencing and structural analysis of 976 base pairs of the promoter sequence for the rat lipoprotein lipase gene. Comparison with the mouse and human sequences. Gene. 209: 31-38.
46. Du, K., and M. Montminy. 1998. CREB is a regulatory target for the protein kinase Akt/PKB. J. Biol. Chem. 273: 32377-32379.
47. Kato, S., J. Ding, and K. Du. 2007. Differential activation of CREB by Akt1 and Akt2. Biochem. Biophys. Res. Commun. 354: 1061-1066.
48. Song, D. H., L. Getty-Kaushik, E. Tseng, J. Simon, B. E. Corkey, and M. M. Wolfe. 2007. Glucose-dependent insulinotropic polypeptide enhances adipocyte development and glucose uptake in part through Akt activation. Gastroenterology. 133: 1796-1805.
49. Yip, R. G., M. O. Boylan, T. J. Kieffer, and M. M. Wolfe. 1998. Functional GIP receptors are present on adipocytes. Endocrinology. 139: 4004-4007.
50. Ebert, R., and W. Creutzfeldt. 1987. Metabolic effects of Gastric Inhibitory Polypeptide. Front. Horm. Res. 16: 175-185.
51. McTernan, P. G., C. M. Kusminski, and S. Kumar. 2006. Resistin. Curr. Opin. Lipidol. 17: 170-175.
52. Janke, J., S. Engeli, K. Gorzelniak, F. C. Luft, and A. M. Sharma. 2002. Resistin gene expression in human adipocytes is not related to insulin resistance. Obes. Res. 10: 1-5.
53. Savage, D. B., C. P. Sewter, E. S. Klenk, D. G. Segal, A. Vidal-Puig, R. V. Considine, and S. O'Rahilly. 2001. Resistin/Fizz3 Expression in relation to obesity and peroxisome proliferator-activated receptor-γ action in humans. Diabetes. 50: 2199-2202.