GLUT4 content decreases along with insulin resistance and high levels of inflammatory markers in rats with metabolic syndrome

Cardiovascular Diabetology

Volumn 11, Issue , 2012, Pages

  Leguisamo, Natalia M ^a   Lehnen, Alexandre M ^a   Machado, Ubiratan F ^b   Okamoto, Maristela M ^b   Markoski, Melissa M ^a   Pinto, Graziela H ^a   Schaan, Beatriz D ^a,c  

^a INSTITUTO DE CARDIOLOGIA DO RIO GRANDE DO SUL   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c HOSPITAL DE CLÍNICAS DE PORTO ALEGRE   (Brazil)

Author keywords

Glucose transporter 4; Monosodium glutamate; Spontaneously hypertensive rats

Indexed keywords

ADIPONECTIN; C REACTIVE PROTEIN; GLUCOSE TRANSPORTER 4; GLUTAMATE SODIUM; INTERLEUKIN 6; LIPID; SODIUM CHLORIDE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD PRESSURE; CONTROLLED STUDY; GASTROCNEMIUS MUSCLE; HEART; INFLAMMATION; INSULIN RESISTANCE; LIPID ANALYSIS; MALE; METABOLIC SYNDROME X; NEWBORN; NONHUMAN; PROTEIN ANALYSIS; RAT; SPONTANEOUSLY HYPERTENSIVE RAT; TREATMENT DURATION; WHITE ADIPOSE TISSUE; WISTAR KYOTO RAT;

ADIPONECTIN; ADIPOSE TISSUE, WHITE; ANIMALS; ANIMALS, NEWBORN; BIOLOGICAL MARKERS; BLOOD PRESSURE; C-REACTIVE PROTEIN; DISEASE MODELS, ANIMAL; DOWN-REGULATION; GLUCOSE TRANSPORTER TYPE 4; HYPERTENSION; INFLAMMATION MEDIATORS; INSULIN RESISTANCE; INTERLEUKIN-6; LIPIDS; MALE; METABOLIC SYNDROME X; MUSCLE, SKELETAL; MYOCARDIUM; RATS; RATS, INBRED SHR; RATS, INBRED WKY; SODIUM GLUTAMATE; TIME FACTORS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84864949747     PISSN: None     EISSN: 14752840     Source Type: Journal    
DOI: 10.1186/1475-2840-11-100     Document Type: Article

References (65)

1. Ford ES, Li C, Zhao G. Prevalence and correlates of metabolic syndrome based on a harmonious definition among adults in the US. J Diabetes 2010, 2:180-193. 10.1111/j.1753-0407.2010.00078.x, 20923483.
2. Wildman RP, McGinn AP, Lin J, Wang D, Muntner P, Cohen HW, Reynolds K, Fonseca V, Sowers MR. Cardiovascular disease risk of abdominal obesity vs. metabolic abnormalities. Obesity (Silver Spring) 2011, 19:853-860.
3. Aschner P. Metabolic syndrome as a risk factor for diabetes. Expert Rev Cardiovasc Ther 2010, 8:407-412. 10.1586/erc.10.13, 20222818.
4. Reaven GM. Banting lecture 1988. Role of insulin resistance in human disease. Diabetes 1988, 37:1595-1607. 10.2337/diabetes.37.12.1595, 3056758.
5. Choi KM, Ryu OH, Lee KW, Kim HY, Seo JA, Kim SG, Kim NH, Choi DS, Baik SH. Serum adiponectin, interleukin-10 levels and inflammatory markers in the metabolic syndrome. Diabetes Res Clin Pract 2007, 75:235-240. 10.1016/j.diabres.2006.06.019, 16872712.
6. Emanuela F, Grazia M, de Marco R, Maria Paola L, Giorgio F, Marco B. Inflammation as a link between obesity and metabolic syndrome. J Nutr Metab 2012, 2012:476380. 3317136, 22523672.
7. Hotamisligil GS, Arner P, Caro JF, Atkinson RL, Spiegelman BM. Increased adipose tissue expression of tumor necrosis factor-alpha in human obesity and insulin resistance. J Clin Invest 1995, 95:2409-2415. 10.1172/JCI117936, 295872, 7738205.
8. Rotter V, Nagaev I, Smith U. Interleukin-6 (IL-6) induces insulin resistance in 3T3-L1 adipocytes and is, like IL-8 and tumor necrosis factor-alpha, overexpressed in human fat cells from insulin-resistant subjects. J Biol Chem 2003, 278:45777-45784. 10.1074/jbc.M301977200, 12952969.
9. Stephens JM, Lee J, Pilch PF. Tumor necrosis factor-alpha-induced insulin resistance in 3T3-L1 adipocytes is accompanied by a loss of insulin receptor substrate-1 and GLUT4 expression without a loss of insulin receptor-mediated signal transduction. J Biol Chem 1997, 272:971-976. 10.1074/jbc.272.2.971, 8995390.
10. Shehata MF. Important genetic checkpoints for insulin resistance in salt-sensitive (S) Dahl rats. Cardiovasc Diabetol 2008, 7:19. 10.1186/1475-2840-7-19, 2459151, 18570670.
11. Pfeffer J, Pfeffer M, Fishbein M, Frohlich E. Cardiac function and morphology with aging in the spontaneously hypertensive rat. Am J Physiol 1979, 237:H461-H468.
12. Lehnen AM, Leguisamo NM, Pinto GH, Markoski MM, De Angelis K, Machado UF, Schaan B. The beneficial effects of exercise in rodents are preserved after detraining: a phenomenon unrelated to GLUT4 expression. Cardiovasc Diabetol 2010, 9:67. 10.1186/1475-2840-9-67, 2984487, 21029425.
13. Carvalho E, Kotani K, Peroni OD, Kahn BB. Adipose-specific overexpression of GLUT4 reverses insulin resistance and diabetes in mice lacking GLUT4 selectively in muscle. Am J Physiol Endocrinol Metab 2005, 289:E551-E561. 10.1152/ajpendo.00116.2005, 15928024.
14. Garvey W, Malanu L, Zhu J, Brechtel-Hook G, Wallace P, Baron A. Evidence of the defects in trafficking and translocation of GLUT4 glucose transporter in skeletal muscle as a cause of human insulin resistance. J Clin Invest 1998, 101:2377-2386. 10.1172/JCI1557, 508827, 9616209.
15. Razny U, Kiec-Wilk B, Wator L, Polus A, Dyduch G, Solnica B, Malecki M, Tomaszewska R, Cooke JP, Dembinska-Kiec A. Increased nitric oxide availability attenuates high fat diet metabolic alterations and gene expression associated with insulin resistance. Cardiovasc Diabetol 2011, 10:68. 10.1186/1475-2840-10-68, 3212914, 21781316.
16. Gray S, Feinberg MW, Hull S, Kuo CT, Watanabe M, Sen-Banerjee S, DePina A, Haspel R, Jain MK. The Kruppel-like factor KLF15 regulates the insulin-sensitive glucose transporter GLUT4. J Biol Chem 2002, 277:34322-34328. 10.1074/jbc.M201304200, 12097321.
17. Hirata AE, Andrade IS, Vaskevicius P, Dolnikoff MS. Monosodium glutamate (MSG)-obese rats develop glucose intolerance and insulin resistance to peripheral glucose uptake. Braz J Med Biol Res 1997, 30:671-674.
18. Papa PC, Seraphim PM, Machado UF. Loss of weight restores GLUT 4 content in insulin-sensitive tissues of monosodium glutamate-treated obese mice. Int J Obes Relat Metab Disord 1997, 21:1065-1070. 10.1038/sj.ijo.0800517, 9368832.
19. Nemeroff CB, Konkol RJ, Bissette G, Youngblood W, Martin JB, Brazeau P, Rone MS, Prange AJ, Breese GR, Kizer JS. Analysis of the disruption in hypothalamic-pituitary regulation in rats treated neonatally with monosodium L-glutamate (MSG): evidence for the involvement of tuberoinfundibular cholinergic and dopaminergic systems in neuroendocrine regulation. Endocrinology 1977, 101:613-622. 10.1210/endo-101-2-613, 407073.
20. Nemeroff CB, Grant LD, Bissette G, Ervin GN, Harrell LE, Prange AJ. Growth, endocrinological and behavioral deficits after monosodium L-glutamate in the neonatal rat: possible involvement of arcuate dopamine neuron damage. Psychoneuroendocrinology 1977, 2:179-196. 10.1016/0306-4530(77)90023-3, 601168.
21. Nemeroff CB, Lipton MA, Kizer JS. Models of neuroendocrine regulation: use of monosodium glutamate as an investigational tool. Dev Neurosci 1978, 1:102-109. 10.1159/000112561, 39735.
22. Kizer JS, Nemeroff CB, Youngblood WW. Neurotoxic amino acids and structurally related analogs. Pharmacol Rev 1977, 29:301-318.
23. Lorden JF, Caudle A. Behavioral and endocrinological effects of single injections of monosodium glutamate in the mouse. Neurobehav Toxicol Teratol 1986, 8:509-519.
24. Olney JW. Brain lesions, obesity, and other disturbances in mice treated with monosodium glutamate. Science 1969, 164:719-721. 10.1126/science.164.3880.719, 5778021.
25. Caputo FA, Scallet AC. Postnatal MSG treatment attenuates angiotensin II (AII) induced drinking in rats. Physiol Behav 1995, 58:25-29. 10.1016/0031-9384(95)00031-D, 7667423.
26. Djazayery A, Miller DS, Stock MJ. Energy balances in obese mice. Nutr Metab 1979, 23:357-367. 10.1159/000176281, 384301.
27. Duloo AG, Miller DS. Unimpaired thermogenic response to noradrenaline in genetic (ob/ob) and hypothalamic (MSG) obese mice. Biosci Rep 1984, 4:343-349. 10.1007/BF01140498, 6733259.
28. Yoshida T, Nishioka H, Nakamura Y, Kanatsuna T, Kondo M. Reduced norepinephrine turnover in brown adipose tissue of pre-obese mice treated with monosodium-L-glutamate. Life Sci 1985, 36:931-938. 10.1016/0024-3205(85)90388-1, 3974402.
29. Machado U, Shimizu I, Saito M. Reduced content and preserved translocation of glucose transporter (GLUT 4) in white adipose tissue of obese mice. Physiol Behav 1994, 55:621-625. 10.1016/0031-9384(94)90035-3, 8190786.
30. Machado U, Shimizu Y, Saito M. Decreased glucose transporter (GLUT 4) content in insulin-sensitive tissues of obese aurothioglucose- and monosodium glutamatetreated mice. Horm Metab Res 1993, 25:462-465. 10.1055/s-2007-1002149, 8225198.
31. Mori RC, Hirabara SM, Hirata AE, Okamoto MM, Machado UF. Glimepiride as insulin sensitizer: increased liver and muscle responses to insulin. Diabetes Obes Metab 2008, 10:596-600. 10.1111/j.1463-1326.2008.00870.x, 18355328.
32. van den Buuse M, Versteeg DH, de Jong W. Effects of neonatal treatment with monosodium-glutamate in spontaneously hypertensive rats. Brain Res 1985, 351:135-138.
33. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254. 10.1016/0003-2697(76)90527-3, 942051.
34. Ferguson RE, Carroll HP, Harris A, Maher ER, Selby PJ, Banks RE. Housekeeping proteins: a preliminary study illustrating some limitations as useful references in protein expression studies. Proteomics 2005, 5:566-571. 10.1002/pmic.200400941, 15627964.
35. Chung S, Park CW, Shin SJ, Lim JH, Chung HW, Youn DY, Kim HW, Kim BS, Lee JH, Kim GH, Chang YS. Tempol or candesartan prevents high-fat diet-induced hypertension and renal damage in spontaneously hypertensive rats. Nephrol Dial Transplant 2010, 25:389-399. 10.1093/ndt/gfp472, 19749146.
36. Murase T, Mizuno T, Omachi T, Onizawa K, Komine Y, Kondo H, Hase T, Tokimitsu I. Dietary diacylglycerol suppresses high fat and high sucrose diet-induced body fat accumulation in C57BL/6J mice. J Lipid Res 2001, 42:372-378.
37. Parekh PI, Petro AE, Tiller JM, Feinglos MN, Surwit RS. Reversal of diet-induced obesity and diabetes in C57BL/6J mice. Metabolism 1998, 47:1089-1096. 10.1016/S0026-0495(98)90283-9, 9751238.
38. Sampey BP, Vanhoose AM, Winfield HM, Freemerman AJ, Muehlbauer MJ, Fueger PT, Newgard CB, Makowski L. Cafeteria diet is a robust model of human metabolic syndrome with liver and adipose inflammation: comparison to high-fat diet. Obesity (Silver Spring) 2011, 19:1109-1117.
39. Iwase M, Yamamoto M, Iino K, Ichikawa K, Shinohara N, Yoshinari M, Fujishima M. Obesity induced by neonatal monosodium glutamate treatment in spontaneously hypertensive rats: an animal model of multiple risk factors. Hypertens Res 1998, 21:1-6. 10.1291/hypres.21.1, 9582101.
40. Gong SL, Xia FQ, Wei J, Li XY, Sun TH, Lu Z, Liu SZ. Harmful effects of MSG on function of hypothalamus-pituitary-target gland system. Biomed Environ Sci 1995, 8:310-317.
41. de Carvalho Papa P, Vargas AM, da Silva JL, Nunes MT, Machado UF. GLUT4 protein is differently modulated during development of obesity in monosodium glutamate-treated mice. Life Sci 2002, 71:1917-1928. 10.1016/S0024-3205(02)01948-3, 12175706.
42. Dolnikoff MS, Kater CE, Egami M, de Andrade IS, Marmo MR. Neonatal treatment with monosodium glutamate increases plasma corticosterone in the rat. Neuroendocrinology 1988, 48:645-649. 10.1159/000125076, 3251163.
43. Haber RS, Weinstein SP. Role of glucose transporters in glucocorticoid-induced insulin resistance. GLUT4 isoform in rat skeletal muscle is not decreased by dexamethasone. Diabetes 1992, 41:728-735. 10.2337/diabetes.41.6.728, 1587399.
44. Kondoh T, Torii K. MSG intake suppresses weight gain, fat deposition, and plasma leptin levels in male Sprague-Dawley rats. Physiol Behav 2008, 95:135-144. 10.1016/j.physbeh.2008.05.010, 18559279.
45. Lobato NS, Filgueira FP, Akamine EH, Davel AP, Rossoni LV, Tostes RC, Carvalho MH, Fortes ZB. Obesity induced by neonatal treatment with monosodium glutamate impairs microvascular reactivity in adult rats: role of NO and prostanoids. Nutr Metab Cardiovasc Dis 2011, 21:808-816. 10.1016/j.numecd.2010.02.006, 20554176.
46. Glazier AM, Scott J, Aitman TJ. Molecular basis of the Cd36 chromosomal deletion underlying SHR defects in insulin action and fatty acid metabolism. Mamm Genome 2002, 13:108-113. 10.1007/s00335-001-2132-9, 11889559.
47. Chiappe De Cingolani GE, Caldiz CI. Insulin resistance and GLUT-4 glucose transporter in adipocytes from hypertensive rats. Metabolism 2004, 53:382-387. 10.1016/j.metabol.2003.10.017, 15015152.
48. Han XX, Bonen A. Epinephrine translocates GLUT-4 but inhibits insulin-stimulated glucose transport in rat muscle. Am J Physiol 1998, 274:E700-E707.
49. Exton JH. Mechanisms of hormonal regulation of hepatic glucose metabolism. Diabetes Metab Rev 1987, 3:163-183. 10.1002/dmr.5610030108, 3032541.
50. Iwase M, Ichikawa K, Tashiro K, Iino K, Shinohara N, Ibayashi S, Yoshinari M, Fujishima M. Effects of monosodium glutamate-induced obesity in spontaneously hypertensive rats vs. Wistar Kyoto rats: serum leptin and blood flow to brown adipose tissue. Hypertens Res 2000, 23:503-510.
51. Dandona P, Aljada A, Mohanty P, Ghanim H, Hamouda W, Assian E, Ahmad S. Insulin inhibits intranuclear nuclear factor kappaB and stimulates IkappaB in mononuclear cells in obese subjects: evidence for an anti-inflammatory effect?. J Clin Endocrinol Metab 2001, 86:3257-3265. 10.1210/jc.86.7.3257, 11443198.
52. Furuya DT, Poletto AC, Favaro RR, Martins JO, Zorn TM, Machado UF. Anti-inflammatory effect of atorvastatin ameliorates insulin resistance in monosodium glutamate-treated obese mice. Metabolism 2010, 59:395-399. 10.1016/j.metabol.2009.08.011, 19800637.
53. Hontecillas R, O'Shea M, Einerhand A, Diguardo M, Bassaganya-Riera J. Activation of PPAR gamma and alpha by punicic acid ameliorates glucose tolerance and suppresses obesity-related inflammation. J Am Coll Nutr 2009, 28:184-195.
54. Gomez Rosso L, Merono T, Benitez MB, Lopez G, Giunta G, D'Ambrosio ML, Wikinski R, Cuniberti L, Brites F. Low adiponectin levels in primary hypertriglyceridemic male patients. Nutr Metab Cardiovasc Dis 2009, 19:135-139. 10.1016/j.numecd.2008.02.008, 18472252.
55. Cassidy A, Skidmore P, Rimm EB, Welch A, Fairweather-Tait S, Skinner J, Burling K, Richards JB, Spector TD, MacGregor AJ. Plasma adiponectin concentrations are associated with body composition and plant-based dietary factors in female twins. J Nutr 2009, 139:353-358.
56. Kouidhi S, Berrhouma R, Rouissi K, Jarboui S, Clerget-Froidevaux MS, Seugnet I, Bchir F, Demeneix B, Guissouma H, Elgaaied AB. Human subcutaneous adipose tissue Glut 4 mRNA expression in obesity and type 2 diabetes. Acta Diabetol 2011, Epub ahead of print.
57. Katayama S, Inaba M, Maruno Y, Morita T, Awata T, Oka Y. Glucose intolerance in spontaneously hypertensive and wistar-kyoto rats: enhanced gene expression and synthesis of skeletal muscle glucose transporter 4. Hypertens Res 1997, 20:279-286. 10.1291/hypres.20.279, 9453263.
58. Miyata T, Taguchi T, Uehara M, Isami S, Kishikawa H, Kaneko K, Araki E, Shichiri M. Bradykinin potentiates insulin-stimulated glucose uptake and enhances insulin signal through the bradykinin B2 receptor in dog skeletal muscle and rat L6 myoblasts. Eur J Endocrinol 1998, 138:344-352. 10.1530/eje.0.1380344, 9539311.
59. Carvalho CR, Thirone AC, Gontijo JA, Velloso LA, Saad MJ. Effect of captopril, losartan, and bradykinin on early steps of insulin action. Diabetes 1997, 46:1950-1957. 10.2337/diabetes.46.12.1950, 9392479.
60. Shepherd P, Kahn B. Glucose transporters and insulin action ¬ implications for insulin resistance and diabetes mellitus. N Engl J Med 1999, 341:248-257. 10.1056/NEJM199907223410406, 10413738.
61. Lopaschuk GD, Belke DD, Gamble J, Itoi T, Schonekess BO. Regulation of fatty acid oxidation in the mammalian heart in health and disease. Biochim Biophys Acta 1994, 1213:263-276. 10.1016/0005-2760(94)00082-4, 8049240.
62. Thackeray JT, Radziuk J, Harper ME, Suuronen EJ, Ascah KJ, Beanlands RS, Dasilva JN. Sympathetic nervous dysregulation in the absence of systolic left ventricular dysfunction in a rat model of insulin resistance with hyperglycemia. Cardiovasc Diabetol 2011, 10:75. 10.1186/1475-2840-10-75, 3170183, 21831292.
63. Luiken JJ, Coort SL, Koonen DP, Bonen A, Glatz JF. Signalling components involved in contraction-inducible substrate uptake into cardiac myocytes. Proc Nutr Soc 2004, 63:251-258. 10.1079/PNS2004333, 15294039.
64. Vettor R, Fabris R, Serra R, Lombardi AM, Tonello C, Granzotto M, Marzolo MO, Carruba MO, Ricquier D, Federspil G, Nisoli E. Changes in FAT/CD36, UCP2, UCP3 and GLUT4 gene expression during lipid infusion in rat skeletal and heart muscle. Int J Obes Relat Metab Disord 2002, 26:838-847.
65. Morel S, Berthonneche C, Tanguy S, Toufektsian MC, Perret P, Ghezzi C, de Leiris J, Boucher F. Early pre-diabetic state alters adaptation of myocardial glucose metabolism during ischemia in rats. Mol Cell Biochem 2005, 272:9-17. 10.1007/s11010-005-4778-1, 16010967.