Sex steroids influence glucose oxidation through modulation of insulin receptor expression and IRS-1 serine phosphorylation in target tissues of adult male rat

Molecular and Cellular Biochemistry

Volumn 352, Issue 1-2, 2011, Pages 35-45

  Muthusamy, Thirupathi ^a,b   Murugesan, Palaniappan ^c   Srinivasan, Chinnapaiyan ^a   Balasubramanian, Karundevi ^a  

^a UNIVERSITY OF MADRAS   (India)

^b UNIVERSITY OF ILLINOIS   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Estradiol; Glucose oxidation; Insulin receptor; IRS 1; Orchidectomy; Testosterone

Indexed keywords

ESTRADIOL; GLUCOSE; INSULIN; INSULIN RECEPTOR; INSULIN RECEPTOR SUBSTRATE 1; MESSENGER RNA; TESTOSTERONE;

ADIPOSE TISSUE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GLUCOSE BLOOD LEVEL; GLUCOSE OXIDATION; HORMONAL REGULATION; INSULIN BLOOD LEVEL; LIVER; MALE; MUSCLE; NONHUMAN; NUCLEOTIDE SEQUENCE; ORCHIECTOMY; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; TARGET ORGAN; TISSUE LEVEL;

ANIMALS; BASE SEQUENCE; BLOOD GLUCOSE; DNA PRIMERS; ESTRADIOL; INSULIN; INSULIN RECEPTOR SUBSTRATE PROTEINS; MALE; ORCHIECTOMY; OXIDATION-REDUCTION; PHOSPHORYLATION; POLYMERASE CHAIN REACTION; RADIOIMMUNOASSAY; RATS; RATS, WISTAR; RECEPTOR, INSULIN; RNA, MESSENGER; SERINE; TESTOSTERONE;

RATTUS;

EID: 79959224996     PISSN: 03008177     EISSN: 15734919     Source Type: Journal    
DOI: 10.1007/s11010-011-0737-1     Document Type: Article

References (67)

1. Saad F, Gooren L (2009) The role of testosterone in the metabolic syndrome: a review. J Steroid Biochem Mol Biol 114:40-43
2. Grossmann M, Gianatti EJ, Zajac JD (2010) Testosterone and type 2 diabetes. Curr Opin Endocrinol Diabetes Obes 17:247-256
3. Kapoor D, Goodwin E, Channer KS, Jones TH (2006) Testosterone replacement therapy improves insulin resistance, glycaemic control, visceral adiposity and hypercholesterolaemia in hypogonadal men with type 2 diabetes. Eur J Endocrinol 154:899-906 (Pubitemid 43997730)
4. Yialamas MA, Dwyer AA, Hanley E, Lee H, Pitteloud N, Hayes FJ (2007) Acute sex steroid withdrawal reduces insulin sensitivity in healthy men with idiopathic hypogonadotropic hypogonadism. J Clin Endocrinol Metab 92:4254-4259 (Pubitemid 350074740)
5. Jones TH (2010) Testosterone deficiency: a risk factor for cardiovascular disease? Trends Endocrinol Metab 21:496-503
6. Holmang A, Bjorntorp P (1992) The effects of testosterone on insulin sensitivity in male rats. Acta Physiol Scand 146:505-510 (Pubitemid 23008349)
7. Morimoto S, Fernandez-Mejia C, Romero-Navarro G, Morales-Peza N, Diaz-Sanchez V (2001) Testosterone effect on insulin content, messenger ribonucleic acid levels, promoter activity, and secretion in the rat. Endocrinology 142:1442-1447 (Pubitemid 32299671)
8. Grillo ML, Jacobus AP, Scalco R, Amaral F, Rodrigues DO, Loss ES, Wassermann GF (2005) Testosterone rapidly stimulates insulin release from isolated pancreatic islets through a non-genomic dependent mechanism. Horm Metab Res 37:662-665 (Pubitemid 41810487)
9. Rizza RA (2000) Androgen effect on insulin action and glucose metabolism. Mayo Clin Proc 75:S61-S64
10. Livingstone C, Collison M (2002) Sex steroids and insulin resistance. Clin Sci 102:151-166 (Pubitemid 34185043)
11. Rochira V, Madeo B, Zirilli L, Caffagni G, Maffei L, Carani C (2007) Oestradiol replacement treatment and glucose homeostasis in two men with congenital aromatase deficiency: evidence for a role of oestradiol and sex steroids imbalance on insulin sensitivity in men. Diabet Med 24:1491-1495 (Pubitemid 350179451)
12. Barros RP, Gabbi C, Morani A, Warner M, Gustafsson JA (2009) Participation of ERalpha and ERbeta in glucose homeostasis in skeletal muscle and white adipose tissue. Am J Physiol Endocrinol Metab 297:E124-E133
13. Cohen JC, Hickman R (1987) Insulin resistance and diminished glucose tolerance in powerlifters ingesting anabolic steroids. J Clin Endocrinol Metab 64:960-963 (Pubitemid 17067428)
14. Marin P, Holmang S, Gustafsson C, Jonsson L, Kvist H, Elander A, Eldh J, Sjostrom L, Holm G, Bjorntorp P (1993) Androgen treatment of abdominally obese men. Obes Res 1:245-251
15. Heine PA, Taylor JA, Iwamoto GA, Lubahn DB, Cooke PS (2000) Increased adipose tissue in male and female estrogen receptor-alpha knockout mice. Proc Natl Acad Sci USA 97:12729-12734
16. Takeda K, Toda K, Saibara T, Nakagawa M, Saika K, Onishi T, Sugiura T, Shizuta Y (2003) Progressive development of insulin resistance phenotype in male mice with complete aromatase (CYP19) deficiency. J Endocrinol 176:237-246 (Pubitemid 36284816)
17. Muthusamy T, Dhevika S, Murugesan P, Balasubramanian K (2007) Testosterone deficiency impairs glucose oxidation through defective insulin and its receptor gene expression in target tissues of adult male rats. Life Sci 81:534-542 (Pubitemid 47212235)
18. Schinner S, Scherbaum WA, Bornstein SR, Barthel A (2005) Molecular mechanisms of insulin resistance. Diabet Med 22:674-682 (Pubitemid 40805885)
19. Sykiotis GP, Papavassiliou AG (2001) Serine phosphorylation of insulin receptor substrate-1: a novel target for the reversal of insulin resistance. Mol Endocrinol 15:1864-1869 (Pubitemid 33022527)
20. Bouzakri K, Roques M, Gual P, Espinosa S, Guebre-Egziabher F, Riou JP, Laville M, Le Marchand-Brustel Y, Tanti JF, Vidal H (2003) Reduced activation of phosphatidylinositol-3 kinase and increased serine 636 phosphorylation of insulin receptor substrate-1 in primary culture of skeletal muscle cells from patients with type 2 diabetes. Diabetes 52:1319-1325
21. Liu J, Tsang S, Wong TM (2006) Testosterone is required for delayed cardioprotection and enhanced heat shock protein 70 expression induced by preconditioning. Endocrinology 147:4569-4577 (Pubitemid 44402162)
22. Oparil S, Levine RL, Chen SJ, Durand J, Chen YF (1997) Sexually dimorphic response of the balloon-injured rat carotid artery to hormone treatment. Circulation 95:1301-1307 (Pubitemid 27097844)
23. Dickson RB, Aten RF, Eisenfeld AJ (1978) An unusual sex steroid- binding protein in mature male rat liver cytosol. Endocrinology 103:1636-1646 (Pubitemid 9051853)
24. Ariano MA, Armstrong RB, Edgerton VR (1973) Hindlimb muscle fiber populations of five mammals. J Histochem Cytochem 21:51-55
25. Collins S, Ahima RS, Kahn BB (2005) Biology of adipose tissue. In: Kahn CR, Weir GC, King GL, Jacobson AM, Moses AC, Smith RJ (eds) Joslin's diabetes mellitus. A Wolters Klunwer Company, Indian edition by BI publication, pp 207-226
26. Riley V (1960) Adaptation of orbital bleeding technic to rapid serial blood studies. Proc Soc Exp Biol Med 104:751-754
27. Johnson AD, Turner PC (1971) Epidydimal carbohydrate metabolism-I. Glucose-1-14C and Glucose-6-14C metabolism by mouse, rat and rabbit tissues. Comp Biochem Physiol 39:599-604
28. Kraft LA, Johnson AD (1972) Epididymal carbohydrate metabolism II. Substrates and pathway utilization of caput and cauda epididymal tissue from the rabbit, rat and mouse. Comp Biochem Physiol B 42:451-461
29. Yabe D, Komuro R, Liang G, Goldstein JL, Brown MS (2003) Liver-specific mRNA for Insig-2 down-regulated by insulin: implications for fatty acid synthesis. Proc Natl Acad Sci USA 100:3155-3160 (Pubitemid 36356555)
30. Peinnequin A, Mouret C, Birot O, Alonso A, Mathieu J, Clarencon D, Agay D, Chancerelle Y, Multon E (2004) Rat proinflammatory cytokine and cytokine related mRNA quantification by real-time polymerase chain reaction using SYBR green. BMC Immunol 5:3
31. Dombrowski L, Roy D, Marcotte B, Marette A (1996) A new procedure for the isolation of plasmamembranes,Ttubules, and internal membranes from skeletal muscle. Am J Physiol 270:E667-E676
32. Nevado C, Valverde AM, Benito M (2006) Role of insulin receptor in the regulation of glucose uptake in neonatal hepatocytes. Endocrinology 147:3709-3718 (Pubitemid 44079375)
33. Lowry OH, Rosenberg NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265-275
34. White MF (1997) The insulin signalling system and the IRS proteins. Diabetologia 40:S2-S17
35. Dominici FP, Hauck S, Argentino DP, Bartke A, Turyn D (2002) Increased insulin sensitivity and upregulation of insulin receptor, insulin receptor substrate (IRS)-1 and IRS-2 in liver of Ames dwarf mice. J Endocrinol 173:81-94 (Pubitemid 34428894)
36. Shinozaki S, Chiba T, Kokame K, Miyata T, Ai M, Kawakami A, Kaneko E, Yoshida M, Shimokado K (2007) Site-specific effect of estradiol on gene expression in the adipose tissue of ob/ob mice. Horm Metab Res 39:192-196 (Pubitemid 46580617)
37. Maffei L, Murata Y, Rochira V, Tubert G, Aranda C, Vazquez M, Clyne CD, Davis S, Simpson ER, Carani C (2004) Dysmetabolic syndrome in a man with a novel mutation of the aromatase gene: effects of testosterone, alendronate, and estradiol treatment. J Clin Endocrinol Metab 89:61-70 (Pubitemid 38183860)
38. Orphanides G, Reinberg D (2002) A unified theory of gene expression. Cell 108:439-451 (Pubitemid 34260870)
39. Cato AC, Peterziel H (1998) The androgen receptor as mediator of gene expression and signal transduction pathways. Trends Endocrinol Metab 9:150-154 (Pubitemid 28252607)
40. Lemoine S, Granier P, Tiffoche C, Berthon PM, Thieulant ML, Carre F, Delamarche P (2002) Effect of endurance training on oestrogen receptor alpha expression in different rat skeletal muscle type. Acta Physiol Scand 175:117-211
41. Mayes JS, Watson GH (2004) Direct effects of sex steroid hormones on adipose tissues and obesity. Obes Rev 5:197-216 (Pubitemid 39423001)
42. McEwan IJ, Gustafsson J (1997) Interaction of the human androgen receptor transactivation function with the general transcription factor TFIIF. Proc Natl Acad Sci USA 94:8485-8490
43. Yeh S, Chang C (1996) Cloning and characterization of a specific coactivator, ARA70, for the androgen receptor in human prostate cells. Proc Natl Acad Sci USA 93:5517-5521
44. Aarnisalo P, Palvimo JJ, Janne OA (1998) CREB-binding protein in androgen receptor mediated signaling. Proc Natl Acad Sci USA 95:2122-2127 (Pubitemid 28145905)
45. Fukuda H, Noguchi T, Iritani N (2001) Transcriptional regulation of insulin receptor gene promoter in rat hepatocytes. Biochem Biophys Res Commun 280:1274-1278 (Pubitemid 32917781)
46. Scheen AJ, Lefebvre PJ (1996) Insulin action in man. Diabetes Metab 22:105-110
47. Kahn CR, Saltiel AR (2005) The molecular mechanism of insulin action and regulation of glucose and lipid metabolism. In: Kahn CR, Weir GC, King GL, Jacobson AM, Moses AC, Smith RJ (eds) Joslin's diabetes mellitus. A Wolters Klunwer Company, Indian edition by BI publication, pp 145-169
48. Aguirre V, Werner ED, Giraud J, Lee YH, Shoelson SE, White MF (2002) Phosphorylation of Ser307 in insulin receptor substrate- 1 blocks interactions with the insulin receptor and inhibits insulin action. J Biol Chem 277:1531-1537 (Pubitemid 34968910)
49. Rui L, Aguirre V, Kim JK, Shulman GI, Lee A, Corbould A, Dunaif A, White MF (2001) Insulin/IGF-1 and TNF-α stimulate phosphorylation of IRS-1 at inhibitory Ser307 via distinct pathways. J Clin Invest 107:181-189 (Pubitemid 32096834)
50. Gual P, Gremeaux T, Gonzalez T, Le Marchand-Brustel Y, Tanti JF (2003) MAP kinases and mTOR mediate insulin-induced phosphorylation of insulin receptor substrate-1 on serine residues 307, 612, and 632. Diabetologia 46:1532-1542
51. Ohlson N, Bergh A, Persson ML, Wikström P (2006) Castration rapidly decreases local insulin-like growth factor-1 levels and inhibits its effects in the ventral prostate in mice. Prostate 66:1687-1697 (Pubitemid 44893895)
52. Allemand MC, Asmann Y, Klaus K, Tatpati L, Coddington CC, Nair KS (2006) O-202: An in vitro model for PCOS related insulin resistance: The effects of testosterone on phosphorylation of intracellular insulin signaling proteins in rat skeletal muscle primary culture. Fertil Steril (Suppl 1):S86-S87
53. Muthusamy T, Murugesan P, Balasubramanian K (2009) Sex steroids deficiency impairs glucose transporter 4 expression and its translocation through defective Akt phosphorylation in target tissues of adult male rat. Metabolism 58:1581-1592
54. Nagira K, Sasaoka T, Wada T, Fukui K, Ikubo M, Hori S, Tsuneki H, Saito S, Kobayashi M (2006) Altered subcellular distribution of estrogen receptor alpha is implicated in estradiol-induced dual regulation of insulin signaling in 3T3-L1 adipocytes. Endocrinology 147:1020-1028 (Pubitemid 43113022)
55. Hommelberg PP, Langen RC, Schols AM, Mensink RP, Plat J (2010) Inflammatory signaling in skeletal muscle insulin resistance: green signal for nutritional intervention? Curr Opin Clin Nutr Metab Care 13:647-655
56. Staab CA, Maser E (2010) 11beta-Hydroxysteroid dehydrogenase type 1 is an important regulator at the interface of obesity and inflammation. J Steroid Biochem Mol Biol 119:56-72
57. Ozes ON, Akca H, Mayo LD, Gustin JA, Maehama T, Dixon JE, Donner DB (2001) A phosphatidylinositol 3-kinase/Akt/mTOR pathway mediates and PTEN antagonizes tumor necrosis factor inhibition of insulin signaling through insulin receptor substrate-1. Proc Natl Acad Sci USA 98:4640-4645 (Pubitemid 32295029)
58. Gual P, Le Marchand-Brustel Y, Tanti JF (2005) Positive and negative regulation of insulin signaling through IRS-1 phosphorylation. Biochimie 87:99-109
59. Khamzina L, Veilleux A, Bergeron S, Marette A (2005) Increased activation of the mammalian target of rapamycin pathway in liver and skeletal muscle of obese rats: possible involvement in obesity-linked insulin resistance. Endocrinology 146:1473-1481 (Pubitemid 40289337)
60. Moretti C, Frajese GV, Guccione L, Wannenes F, De Martino MU, Fabbri A, Frajese G (2005) Androgens and body composition in the aging male. J Endocrinol Invest 28(3 Suppl):56-64
61. Jiao Q, Pruznak AM, Huber D, Vary TC, Lang CH (2009) Castration differentially alters basal and leucine-stimulated tissue protein synthesis in skeletal muscle and adipose tissue. Am J Physiol Endocrinol Metab 297:E1222-E1232
62. Yanase T, Fan W, Kyoya K, Min L, Takayanagi R, Kato S, Nawata H (2008) Androgens and metabolic syndrome: lessons from androgen receptor knock out (ARKO) mice. J Steroid Biochem Mol Biol 109:254-257
63. Lin HY, Yu IC, Wang RS, Chen YT, Liu NC, Altuwaijri S, Hsu CL, Ma WL, Jokinen J, Sparks JD, Yeh S, Chang C (2008) Increased hepatic steatosis and insulin resistance in mice lacking hepatic androgen receptor. Hepatology 47:1924-1935 (Pubitemid 351945560)
64. Traish AM, Saad F, Guay A (2009) The dark side of testosterone deficiency: II. Type 2 diabetes and insulin resistance. J Androl 30:23-32
65. Ramamani A, Aruldhas MM, Govindarajulu P (1999) Differential response of rat skeletal muscle glycogen metabolism to testosterone and estradiol. Can J Physiol Pharmacol 77:300-304 (Pubitemid 29447975)
66. Kahn CR, Goldfine ID, Neville DM Jr, De Meyts P (1978) Alterations in insulin binding induced by changes in vivo in the levels of glucocorticoids and growth hormone. Endocrinology 103:1054-1466
67. Buren J, Liu HX, Jensen J, Eriksson JW (2002) Dexamethasone impairs insulin signalling and glucose transport by depletion of insulin receptor substrate-1, phosphatidylinositol 3-kinase and protein kinase B in primary cultured rat adipocytes. Eur J Endocrinol 146:419-429 (Pubitemid 34257654)