Differential sensitivity to adrenergic stimulation underlies the sexual dimorphism in the development of diabetes caused by Irs-2 deficiency

Biochemical Pharmacology

Volumn 81, Issue 2, 2011, Pages 279-288

  Garcia Barrado, Maria Jose ^a   Iglesias Osma, Maria Carmen ^a   Moreno Viedma, Veronica ^c   Pastor Mansilla, Maria Francisca ^b   Gonzalez, Silvia Sanz ^c   Carretero, Jose ^a   Moratinos, Julio ^a   Burks, Deborah J ^c  

^a UNIVERSITY OF SALAMANCA   (Spain)

^b UNIVERSITY OF VALLADOLID   (Spain)

^c CENTRO DE INVESTIGACIÓN PRÍNCIPE FELIPE   (Spain)

Author keywords

Adrenergic receptors; cAMP; Diabetes; Insulin; Lipolysis

Indexed keywords

CATECHOLAMINE; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; INSULIN RECEPTOR SUBSTRATE 2; TRIACYLGLYCEROL LIPASE;

ADIPOSE TISSUE; ADRENERGIC STIMULATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CATABOLISM; DIABETES MELLITUS; FEMALE; INSULIN RELEASE; LIPOLYSIS; MALE; MOUSE; NONHUMAN; OBESITY; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; SEX DIFFERENCE;

ADENYLATE CYCLASE; ADIPOCYTES; ADRENERGIC ALPHA-2 RECEPTOR AGONISTS; ANIMALS; CELLS, CULTURED; CYCLIC AMP; DIABETES MELLITUS; FEMALE; FORSKOLIN; GENE EXPRESSION REGULATION; INSULIN; INSULIN RECEPTOR SUBSTRATE PROTEINS; ISLETS OF LANGERHANS; LIPOLYSIS; MALE; MICE; MICE, KNOCKOUT; RECEPTORS, ADRENERGIC, ALPHA-2; SEX CHARACTERISTICS; SIGNAL TRANSDUCTION; STEROL ESTERASE;

EID: 78650168896     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2010.10.008     Document Type: Article

References (56)

1. T. Kadowaki Insights into insulin resistance and type 2 diabetes from knockout mouse models J Clin Invest 106 2000 459 465 (Pubitemid 30666378)
2. R.C. Oriel, C.D. Wiley, M.J. Dewey, and P.B. Vrana Adaptive genetic variation, stress and glucose regulation Dis Model Mech 1 2008 255 263
3. D.J. Withers, J.S. Gutierrez, H. Towery, D.J. Burks, J.M. Ren, and S. Previs Disruption of IRS-2 causes type 2 diabetes in mice Nature 391 1998 900 904 (Pubitemid 28157668)
4. J.C. Wells Sexual dimorphism of body composition Best Pract Res Clin Endocrinol Metab 21 2007 415 430 (Pubitemid 47387103)
5. A. Amrani, S. Durant, M. Throsby, J. Coulaud, M. Dardenne, and F. Homo-Delarche Glucose homeostasis in the nonobese diabetic mouse at the prediabetic stage Endocrinology 139 1998 1115 1124 (Pubitemid 28510130)
6. H. Kikutani, and S. Makino The murine autoimmune diabetes model: NOD and related strains Adv Immunol 51 1992 285 322
7. B. Ahren Evidence that autonomic mechanisms contribute to the adaptive increase in insulin secretion during dexamethasone-induced insulin resistance in humans Diabetologia 51 2008 1018 1024
8. B. Ahren Autonomic regulation of islet hormone secretion - implications for health and disease Diabetologia 43 2000 393 410 (Pubitemid 30237947)
9. J.B. Redmon, H.C. Towle, and R.P. Robertson Regulation of human insulin gene transcription by glucose, epinephrine, and somatostatin Diabetes 43 1994 546 551 (Pubitemid 24096295)
10. R.P. Robertson, J.B. Halter, and D. Porte Jr. A role for alpha-adrenergic receptors in abnormal insulin secretion in diabetes mellitus J Clin Invest 57 1976 791 795
11. N.J. Christensen Catecholamines and diabetes mellitus Diabetologia 16 1979 211 224 (Pubitemid 9200652)
12. C.G. Isles, and J.K. Johnson Phaeochromocytoma and diabetes mellitus: further evidence that alpha 2 receptors inhibit insulin release in man Clin Endocrinol (Oxf) 18 1983 37 41 (Pubitemid 13203730)
13. G. Stenstrom, L. Sjostrom, and U. Smith Diabetes mellitus in phaeochromocytoma. Fasting blood glucose levels before and after surgery in 60 patients with phaeochromocytoma Acta Endocrinol (Copenh) 106 1984 511 515 (Pubitemid 14053024)
14. C.G. Ostenson, A.G. Cattaneo, J.C. Doxey, and S. Efendic Alpha-adrenoceptors and insulin release from pancreatic islets of normal and diabetic rats Am J Physiol 257 1989 E439 443
15. E. Guillot, A. Coste, and I. Angel Alpha 2-adrenoceptors and the regulation of glucose, insulin and amylin levels in diabetic rats Life Sci 57 1995 2081 2090
16. T. Nakaki, T. Nakadate, K. Ishii, and R. Kato Postsynaptic alpha-2 adrenergic receptors in isolated rat islets of Langerhans: inhibition of insulin release and cyclic 3′:5′-adenosine monophosphate accumulation J Pharmacol Exp Ther 216 1981 607 612 (Pubitemid 11143730)
17. G. Drews, A. Debuyser, M. Nenquin, and J.C. Henquin Galanin and epinephrine act on distinct receptors to inhibit insulin release by the same mechanisms including an increase in K+ permeability of the B-cell membrane Endocrinology 126 1990 1646 1653 (Pubitemid 20095775)
18. + channel in mouse pancreatic B cells Nature 349 1991 77 79 (Pubitemid 21912019)
19. 2+ concentration J Biol Chem 263 1988 1855 1860 (Pubitemid 18052140)
20. E. Savontaus, V. Fagerholm, O. Rahkonen, and M. Scheinin Reduced blood glucose levels, increased insulin levels and improved glucose tolerance in alpha2A-adrenoceptor knockout mice Eur J Pharmacol 578 2008 359 364
21. J.C. Devedjian, A. Pujol, C. Cayla, M. George, A. Casellas, and H. Paris Transgenic mice overexpressing alpha2A-adrenoceptors in pancreatic beta-cells show altered regulation of glucose homeostasis Diabetologia 43 2000 899 906 (Pubitemid 30463170)
22. A.H. Rosengren, R. Jokubka, D. Tojjar, C. Granhall, O. Hansson, and D.Q. Li Overexpression of alpha2A-adrenergic receptors contributes to type 2 diabetes Science 327 2010 217 220
23. J. Dupuis, C. Langenberg, I. Prokopenko, R. Saxena, N. Soranzo, and A.U. Jackson New genetic loci implicated in fasting glucose homeostasis and their impact on type 2 diabetes risk Nat Genet 42 2010 105 116
24. D. Langin Adipose tissue lipolysis as a metabolic pathway to define pharmacological strategies against obesity and the metabolic syndrome Pharmacol Res 53 2006 482 491 (Pubitemid 43767551)
25. S.P. Alexander, A. Mathie, and J.A. Peters Guide to receptors and channels (GRAC), 3rd edition Br J Pharmacol 153 2008 S1 S209
26. L. Fu, K. Isobe, Q. Zeng, K. Suzukawa, K. Takekoshi, and Y. Kawakami The effects of beta(3)-adrenoceptor agonist CL-316,243 on adiponectin, adiponectin receptors and tumor necrosis factor-alpha expressions in adipose tissues of obese diabetic KKAy mice Eur J Pharmacol 584 2008 202 206
27. J.N. Fain, and J.A. Garcija-Sainz Adrenergic regulation of adipocyte metabolism J Lipid Res 24 1983 945 966 (Pubitemid 13002334)
28. A.A. Butler, and R.D. Cone Knockout models resulting in the development of obesity Trends Genet 17 2001 S50 54
29. P. Arner Human fat cell lipolysis: biochemistry, regulation and clinical role Best Pract Res Clin Endocrinol Metab 19 2005 471 482 (Pubitemid 41819214)
30. L.J. Emorine, S. Marullo, M.M. Briend-Sutren, G. Patey, K. Tate, and C. Delavier-Klutchko Molecular characterization of the human beta 3-adrenergic receptor Science 245 1989 1118 1121 (Pubitemid 19231821)
31. T. Kitamura, C.R. Kahn, and D. Accili Insulin receptor knockout mice Annu Rev Physiol 65 2003 313 332 (Pubitemid 38249156)
32. D.J. Burks, and M.F. White IRS proteins and beta-cell function Diabetes 50 2001 S140 145
33. N. Kubota, K. Tobe, Y. Terauchi, K. Eto, T. Yamauchi, and R. Suzuki Disruption of insulin receptor substrate 2 causes type 2 diabetes because of liver insulin resistance and lack of compensatory beta-cell hyperplasia Diabetes 49 2000 1880 1889
34. H. Hashimoto, T. Arai, Y. Ohnishi, T. Eto, M. Ito, and K. Hioki Phenotypes of IRS-2 deficient mice produced by reproductive technology are stable Exp Anim 56 2007 149 154 (Pubitemid 46711799)
35. (-/-) mouse liver J Biol Chem 276 2001 38337 38340
36. D.J. Burks, J. Font de Mora, M. Schubert, D.J. Withers, M.G. Myers, and H.H. Towery IRS-2 pathways integrate female reproduction and energy homeostasis Nature 407 2000 377 382
37. M.C. Iglesias-Osma, M.J. Garcia-Barrado, V. Visentin, M.F. Pastor-Mansilla, S. Bour, and D. Prevot Benzylamine exhibits insulin-like effects on glucose disposal, glucose transport, and fat cell lipolysis in rabbits and diabetic mice J Pharmacol Exp Ther 309 2004 1020 1028 (Pubitemid 38669687)
38. M.J. Garcia-Barrado, M.A. Ravier, J.F. Rolland, P. Gilon, M. Nenquin, and J.C. Henquin Inhibition of protein synthesis sequentially impairs distinct steps of stimulus-secretion coupling in pancreatic beta cells Endocrinology 142 2001 299 307 (Pubitemid 32183691)
39. P. Detimary, J.C. Jonas, and J.C. Henquin Possible links between glucose-induced changes in the energy state of pancreatic B cells and insulin release. Unmasking by decreasing a stable pool of adenine nucleotides in mouse islets J Clin Invest 96 1995 1738 1745
40. N. Kubota, Y. Terauchi, K. Tobe, W. Yano, R. Suzuki, and K. Ueki Insulin receptor substrate 2 plays a crucial role in beta cells and the hypothalamus J Clin Invest 114 2004 917 927 (Pubitemid 39578719)
41. A.M. Valverde, D.J. Burks, I. Fabregat, T.L. Fisher, J. Carretero, and M.F. White Molecular mechanisms of insulin resistance in IRS-2-deficient hepatocytes Diabetes 52 2003 2239 2248 (Pubitemid 37059493)
42. N.A. Ducharme, and P.E. Bickel Lipid droplets in lipogenesis and lipolysis Endocrinology 149 2008 942 949
43. J.G. Granneman Delivery of DNA into adipocytes within adipose tissue Methods Mol Biol 423 2008 191 195
44. W.J. Shen, S. Patel, H. Miyoshi, A.S. Greenberg, and F.B. Kraemer Functional interaction of hormone-sensitive lipase and perilipin in lipolysis J Lipid Res 2009
45. V. Grill, and E. Cerasi Activation by glucose of adenyl cyclase in pancreatic islets of the rat FEBS Lett 33 1973 311 314
46. D. Delmeire, D. Flamez, S.A. Hinke, J.J. Cali, D. Pipeleers, and F. Schuit Type VIII adenylyl cyclase in rat beta cells: coincidence signal detector/generator for glucose and GLP-1 Diabetologia 46 2003 1383 1393 (Pubitemid 37297209)
47. A. Tengholm, and E. Gylfe Oscillatory control of insulin secretion Mol Cell Endocrinol 297 2009 58 72
48. L. Ste Marie, and R.D. Palmiter Norepinephrine and epinephrine-deficient mice are hyperinsulinemic and have lower blood glucose Endocrinology 144 2003 4427 4432 (Pubitemid 37204842)
49. Y. Tsuji, Y. Kaburagi, Y. Terauchi, S. Satoh, N. Kubota, and H. Tamemoto Subcellular localization of insulin receptor substrate family proteins associated with phosphatidylinositol 3-kinase activity and alterations in lipolysis in primary mouse adipocytes from IRS-1 null mice Diabetes 50 2001 1455 1463 (Pubitemid 32500180)
50. C. Selman, S. Lingard, A.I. Choudhury, R.L. Batterham, M. Claret, and M. Clements Evidence for lifespan extension and delayed age-related biomarkers in insulin receptor substrate 1 null mice FASEB J 22 2008 807 818 (Pubitemid 351348133)
51. V. Large, and P. Arner Regulation of lipolysis in humans. Pathophysiological modulation in obesity, diabetes, and hyperlipidaemia Diabetes Metab 24 1998 409 418 (Pubitemid 28564954)
52. M.J. Watt, A.L. Carey, E. Wolsk-Petersen, F.B. Kraemer, B.K. Pedersen, and M.A. Febbraio Hormone-sensitive lipase is reduced in the adipose tissue of patients with type 2 diabetes mellitus: influence of IL-6 infusion Diabetologia 48 2005 105 112 (Pubitemid 40174662)
53. G. Faulds, M. Ryden, I. Ek, H. Wahrenberg, and P. Arner Mechanisms behind lipolytic catecholamine resistance of subcutaneous fat cells in the polycystic ovarian syndrome J Clin Endocrinol Metab 88 2003 2269 2273 (Pubitemid 36549907)
54. I. Ek, P. Arner, A. Bergqvist, K. Carlstrom, and H. Wahrenberg Impaired adipocyte lipolysis in nonobese women with the polycystic ovary syndrome: a possible link to insulin resistance? J Clin Endocrinol Metab 82 1997 1147 1153 (Pubitemid 27166656)
55. I. Neganova, H. Al-Qassab, H. Heffron, C. Selman, A.I. Choudhury, and S.J. Lingard Role of central nervous system and ovarian insulin receptor substrate 2 signaling in female reproductive function in the mouse Biol Reprod 76 2007 1045 1053 (Pubitemid 46835013)
56. A. Nadal, P. Alonso-Magdalena, S. Soriano, A.B. Ropero, and I. Quesada The role of oestrogens in the adaptation of islets to insulin resistance J Physiol 587 2009 5031 5037