Neonatal exendin-4 treatment reduces oxidative stress and prevents hepatic insulin resistance in intrauterine growth-retarded rats

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 297, Issue 6, 2009, Pages

  Raab, Elisabeth L ^a   Vuguin, Patricia M ^b   Stoffers, Doris A ^c   Simmons, Rebecca A ^c  

^a CHILDREN S HOSPITAL LOS ANGELES   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Diabetes; Insulin resistance; Intrauterine growth retardation; Liver

Indexed keywords

EXENDIN 4; GLUCOKINASE; GLUCOSE; GLUCOSE 6 PHOSPHATASE; GLUTATHIONE; GLUTATHIONE DISULFIDE; INSULIN; INSULIN RECEPTOR SUBSTRATE 2; MESSENGER RNA; PHOSPHOPYRUVATE CARBOXYLASE; PROTEIN KINASE B BETA; THIOBARBITURIC ACID REACTIVE SUBSTANCE; TRIACYLGLYCEROL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CALORIC INTAKE; CHEMOPROPHYLAXIS; CONTROLLED STUDY; ENZYME ACTIVITY; FAT CONTENT; FOOD INTAKE; GLUCONEOGENESIS; IN VITRO STUDY; IN VIVO STUDY; INSULIN RESISTANCE; INTRAUTERINE GROWTH RETARDATION; LIVER CELL; LIVER LEVEL; LIVER METABOLISM; MALE; NEWBORN; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; WEIGHT REDUCTION;

AGE FACTORS; AGING; ANIMALS; ANIMALS, NEWBORN; BIOLOGICAL MARKERS; BLOOD GLUCOSE; BODY COMPOSITION; BODY WEIGHT; CELLS, CULTURED; DIABETES MELLITUS, TYPE 2; DISEASE MODELS, ANIMAL; DRUG ADMINISTRATION SCHEDULE; FEMALE; FETAL GROWTH RETARDATION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLUCOKINASE; GLUCOSE-6-PHOSPHATASE; HYPOGLYCEMIC AGENTS; INJECTIONS, SUBCUTANEOUS; INSULIN; INSULIN RESISTANCE; LIVER; OXIDATIVE STRESS; PEPTIDES; PHOSPHOENOLPYRUVATE CARBOXYKINASE (GTP); PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; SIGNAL TRANSDUCTION; VENOMS;

EID: 72449182146     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00519.2009     Document Type: Article

References (66)

1. Ahren B, Larsson H, Holst JJ. Effects of glucagon-like peptide-1 on islet function and insulin sensitivity in noninsulin-dependent diabetes mellitus. J Clin Endocrinol Metab 82: 473-478, 1997. (Pubitemid 27068614)
2. Ahren B, Pacini G. Dose-related effects of GLP-1 on insulin secretion, insulin sensitivity, and glucose effectiveness in mice. Am J Physiol Endocrinol Metab 277: E996-E1004, 1999. (Pubitemid 30045992)
3. Aviv V, Meivar-Levy I, Rachmut IH, Rubinek T, Mor E, Ferber S. Exendin-4 promotes liver cell proliferation and enhances PDX-1-induced liver to pancreas differentiation. J Biol Chem. In Press.
4. Ayala JE, Bracy DP, James FD, Julien BM, Wasserman DH, Drucker DJ. The glucagon-like peptide-1 receptor regulates endogenous glucose production and muscle glucose uptake independent of its incretin action. Endocrinology 150:1155-1164, 2009.
5. Balkan B, Li X. Portal GLP-1 administration in rats augments the insulin response to glucose via neuronal mechanisms. Am J Physiol Regul Integr Comp Physiol 279: R1449-R1454, 2000. (Pubitemid 30953783)
6. Bizeau ME, Chort C, Thresher JS, Commerfored SR, Willis WT, Pagliassotti MJ. Increased pyruvate flux capacities account for diet-induced increases in gluconeogenesis in vitro. Am J Physiol Regul Integr Comp Physiol 281: R427-R433, 2001. (Pubitemid 32756134)
7. Blazquez E, Alvarez E, Navarro M, Roncero I, Rodriguez-Fonseca F, Chowen JA, Zueco JA. Glucagon-like peptide-1 (7-36) amide as a novel neuropeptide. Mol Neurobiol 18:157-173, 1998. (Pubitemid 29083007)
8. Bontemps F, Hue L, Hers HG. Phosphorylation of glucose in isolated rat hepatocytes. Sigmoidal kinetics explained by the activity of glucokinase alone. Biochem J 174: 603-611, 1978. (Pubitemid 8403670)
9. Bullock BP, Heller RS, Habener JF. Tissue distribution of messenger ribonucleic acid encoding the rat glucoagon-like peptide-1 receptor. Endocrinology 137: 2968-2978, 1996. (Pubitemid 26192194)
10. Burcelin R, Da Costa A, Drucker D, Thorens B. Glucose competence of the hepatoportal vein sensor requires the presence of an activated glucagon-like peptide-1 receptor. Diabetes 50: 1720-1728, 2001. (Pubitemid 33641588)
11. Burgess SC, He T, Yan Z, Lindner J, Sherry AD, Malloy CR, Browning JD, Magnuson MA. Cytosolic phosphoenolpyruvate carboxykinase does not solely control the rate of hepatic gluconeogenesis in the intact mouse liver. Cell Metab 5: 313-320, 2007. (Pubitemid 46477858)
12. Campos RV, Lee YC, Drucker DJ. Divergent tissue-specific and developmental expression of receptors for glucagon and glucagon-like peptide-1 in the mouse. Endocrinology 134: 2156-2164, 1994.
13. Curran TR Jr, Bahner RI Jr, Oh W, Gruppuso PA. Mitogen-independent DNA synthesis by fetal rat hepatocytes in primary culture. Exp Cell Res 209: 53-57, 1993. (Pubitemid 23344275)
14. Daniel EE, Anvari M, Fox-Threlkeld JE, McDonald TJ. Local, exendin-(9-39)-insensitive, site of action of GLP-1 in canine ileum. Am J Physiol Gastrointest Liver Physiol 283: G595-G602, 2002. (Pubitemid 34920346)
15. Davis, HR Jr, Mullins DE, Pines JM, Hoos LM, France CF, Compton DS, Graziano MP, Sybertz EJ, Strader CD, Van Heek M. Effect of chronic central administration of glucagon-like peptide-1 (7-36) amide on food consumption and body weight in normal and obese rats. Obes Res 6: 147-156, 1998. (Pubitemid 128679656)
16. Dillon JS, Tanizawa Y, Wheeler MB, Leng XH, Ligon BB, Rabin DU, Yoo-Warren H, Permutt MA, Boyd AE. Cloning and functional expression of the human glucagon-like peptide-1 (GLP-1) receptor. Endocrinology 133: 1907-1910, 1993.
17. Dunphy JL, Taylor RG, Fuller PJ. Tissue distribution of rat glucagon receptor and GLP-1 receptor gene expression. Mol Cell Endocrinol 141: 179-186, 1998. (Pubitemid 28393391)
18. Dupré J, Behme MT, McDonald TJ. Exendin-4 normalized postcibal glycemic excursions in type 1 diabetes. J Clin Endocrinol Metab 89: 3469-3473, 2004. (Pubitemid 38951922)
19. Eng J, Kleinman WA, Singh L, Singh G, Raufman JP. Isolation and characterization of exendin-4, an exendin-3 analogue, from Heloderma suspectum venom. Further evidence for an exendin receptor on dispersed acini from guinea pig pancreas. J Biol Chem 267: 7402-7405, 1992.
20. Esposito LA, Melov S, Panov A, Cottrell BA, Wallace DC. Mitochondrial disease in mouse results in increased oxidative stress. Proc Natl Acad Sci USA 96: 4820-4825, 1999. (Pubitemid 29214495)
21. Galera C, Clemente F, Alcantara A, Trapote MA, Perea A, Lopez-Delgado MI, Villanueva-Penacarrillo ML, Valverde I. Inositolphosphoglycans and diacyglycerol are possible mediators in the glycogenic effect of GLP-1(7-36)amide in BC3H-1 myocytes. Cell Biochem Funct 14: 43-48, 1996. (Pubitemid 26055415)
22. Gedulin BR, Nikoulina SE, Smith PA, Gedulin G, Nielsen LL, Baron AD, Parkes DG, Young AA. Exenatide (Exendin-4) improves insulin sensitivity, and β-cell mass in insulin-resistant obese fa/fa Zucker rats independent of glycemia and body weight. Endocrinology 146: 2069-2076, 2005. (Pubitemid 40396918)
23. Goke R, Fehmann HC, Linn T, Schmidt H, Krause M, Eng J, Goke B. Exendin-4 is a high potency agonist and truncated exendin-(9-39)-amide an antagonist at the glucagon-like peptide 1-(7-36)-amide receptor of insulin-secreting beta cells. J Biol Chem 268: 19650-19655, 1993. (Pubitemid 23270754)
24. Greig NH, Holloway HW, De Ore KA, Jani D, Wang Y, Zhou J, Garant MJ, Egan JM. Once daily injection of exendin-4 to diabetic mice achieves long-term beneficial effects on blood glucose concentrations. Diabetologia 42: 45-50, 1999. (Pubitemid 29039736)
25. Groen AK, van Roermund CW, Vervoorn RC, Tager JM. Control of gluconeogenesis in rat liver cells. Flux control coefficients of the enzymes in the gluconeogenic pathway in the absence and presence of glucagon. Biochem J 237: 329-389, 1986.
26. Gulpinar MA, Bozkurt A, Coskun T, Ulusoy NB, Yegen BC. Glucagon-like peptide (GLP-1) is involved in the central modulation of fecal output in rats. Am J Physiol Gastrointest Liver Physiol 278: G924-G929, 2000. (Pubitemid 30439171)
27. Idris I, Patiag D, Gray S, Donnelly R. Exendin-4 increases insulin sensitivity via a PI-3-kinase-dependent mechanism: contrasting effects of GLP-1. Biochem Pharmacol 63: 993-996, 2002. (Pubitemid 34243013)
28. Ikezawa Y, Yamatani K, Ohnuma H, Daimon M, Manaka H, Sasaki. Glucagon-like peptide 1 inhibits glucagon-induced glycogenolysis in perivenous hepatocytes specifically. Regul Pept 111: 207-210, 2003. (Pubitemid 36254769)
29. Ionut V, Zheng D, Stefanovski D, Bergman RN. Exenatide can reduce glucose independent of islet hormones or gastric emptying. Am J Physiol Endocrinol Metab 295: E269-E277, 2008.
30. Kimura K, Tawara S, Igarashi K, Takenaka A. Effect of various radical generators on insulin-dependent regulation of hepatic gene expression. Biosci Biotechnol Biochem 71: 16-22, 2007. (Pubitemid 46155141)
31. Knauf C, Cani PD, Kim DH, Iglesias MA, Chabo C, Waget A, Colom A, Rastrelli S, Delzenne NM, Crucker DJ, Seeley RJ, Burcelin R. Role of central nervous system glucagon-like peptide-1 receptors in enteric glucose sensing. Diabetes 57: 2603-2612, 2008.
32. Kolterman OG, Buse JB, Fineman MS, Gaines E, Heintz S, Bicsak TA, Taylor K, Kim D, Aisporna M, Wang Y, Baron AD. Synthetic exendin-4 (exenatide) significantly reduces postprandial and fasting plasma glucose in subjects with type 2 diabetes. J Clin Endocrinol Metab 88: 3082-3089, 2003. (Pubitemid 36877476)
33. Marquez L, Trapote MA, Luque MA, Valverde I, Villanueva-Penacarrillo ML. Inositolphosphoglycans possibly mediate the effects of glucagon-like peptide-1(7-36)amide on rat liver and adipose tissue. Cell Biochem Funct 16: 51-56, 1998. (Pubitemid 28098176)
34. 2 induce caspase-3-independent degradation of Akt/Protein kinase B. J Biol Chem 277: 42943-42952, 2002.
35. Meeran K, O'Shea D, Edwards CM, Turton MD, Heath MM, Gunn I, Abusnana S, Rossi M, Small CJ, Goldstone AP, Taylor GM, Sunter D, Steere J, Choi SJ, Ghatei MA, Bloom SR. Repeated intracerebroventricular administration of glucagon-like peptide-1-(7-36) amide or exendin-(9-39) alters body weight in the rat. Endocrinology 140: 244-250, 1999. (Pubitemid 29011165)
36. Murata H, Ihara Y, Nakamura H, Yodoi J, Sumikawa K, Kondo T. Glutaredoxin exerts an antiapoptotic effect by regulating the redox state of Akt. J Biol Chem 278: 50226-50233, 2003. (Pubitemid 37548863)
37. Navarro M, Rodriquez de Fonseca F, Alvarez E, Chowen JA, Zueco JA, Gomez R, Eng J, Blazquez E. Colocalization of glucagon-like peptide-1 (GLP-1) receptors, glucose transporter GLUT-2, and glucokinase mRNAs in rat hypothalamic cells: evidence for a role of GLP-1 receptor agonists as an inhibitory signal for food and water intake. J Neurochem 67: 1982-1991, 1996.
38. Nielsen LL, Baron AD. Pharmacology of exenatide (synthetic exendin-4) for the treatment of type 2 diabetes. Curr Opin Investig Drugs 4: 401-405, 2003. (Pubitemid 36686678)
39. Nishizawa M, Moore MC, Shiota M, Gustavson SM, Snead WL, Neal DW, Cherrington AD. Effect of intraportal glucagon-like peptide-1 on glucose metabolism in conscious dogs. Am J Physiol Endocrinol Metab 284: E1027-E1036, 2003. (Pubitemid 36444040)
40. Nishizawa M, Nakabayashi H, Kawai K, Ito T, Kawakami S, Nakagawa A, Niijima A, Uchida K. The hepatic vagal reception of intraportal GLP-1 is via receptor different from the pancreatic GLP-1 receptor. J Auton Nerv Syst 80: 14-21, 2000. (Pubitemid 30160722)
41. Ogata E, Bussey M, Finley S. Altered gas exchange, limited glucose, branched chain amino acids, and hypoinsulinism retard fetal growth in the rat. Metabolism 35: 970-977, 1986. (Pubitemid 17184368)
42. Orskov L, Holst JJ, Moller J, Orskov C, Moller N, Alberti KG, Schmitz O. GLP-1 does not acutely affect insulin sensitivity in healthy man. Diabetologia 39: 1227-1232, 1996. (Pubitemid 26319947)
43. Parkes DG, Pittner R, Jodka C, Smith P, Young A. Insulinotropic actions of exendin-4 and glucagon-like peptide-1 in vivo and in vitro. Metabolism 50: 583-589, 2001. (Pubitemid 32433049)
44. Peterside IE, Selak MA, Simmons RA. Impaired oxidative phosphorylation in hepatic mitochondria of growth retarded rats alters glucose metabolism. Am J Physiol Endocrinol Metab 285: E1258-E1264, 2003.
45. Preitner F, Ibberson M, Franklin I, Binnert C, Pende M, Gjinovci A, Hansotia T, Drucker DJ, Wollheim C, Burcelin R, Thorens B. Glucoincretins control insulin secretion at multiple levels as revealed in mice lacking GLP-1 and GIP receptors. J Clin Invest 113: 635-645, 2004. (Pubitemid 38542513)
46. Ryan AS, Egan JM, Habener JF, Elahi D. Insulinotropic hormone glucagon-like peptide-1-(7-37) appears not to augment insulin-mediated glucose uptake in young men during euglycemia. J Clin Endocrinol Metab 83: 2399-2404, 1998. (Pubitemid 28503037)
47. Selak MA, Storey BT, Peterside IE, Simmons R. Impaired oxidative phosphorylation in skeletal mscle cntributes to insulin resistance and hyperglycemia. Am J Physiol Endocrinol Metab 285: E130-E137, 2003.
48. Simmons RA, Gounis A, Bangalore S, Ogata E. Intrauterine growth retardation: Fetal glucose transport is diminished in lung but spared in brain. Pediatr Res 31: 59-63, 1992.
49. Simmons RA, Suponitsky-Kroyter I, Selak MA. Progressive accumulation of MtDNA mutations, and decline of mitochondrial function lead to β-cell failure. J Biol Chem 280: 28785-28791, 2005. (Pubitemid 41105780)
50. Simmons RA, Templeton L, Gertz SI. Intrauterine growth retardation leads to the development of type 2 diabetes in the rat. Diabetes 50: 2279-2286, 2001. (Pubitemid 33641912)
51. Stoffers DA, Desai BM, Ng DD, Simmons RA. Neonatal Ex-4 prevents the development of diabetes mellitus in the intrauterine growth retarded rat. Diabetes 52: 734-740, 2003.
52. Sun Y, Liu S, Ferguson S, Wang L, Klepcyk P, Yun JS, Friedman JE. Phosphoenolpyruvate carboxykinase overexpression selectively attenuates insulin signaling and hepatic insulin sensitivity in transgenic mice. J Biol Chem 277: 23301-23307, 2002. (Pubitemid 34952159)
53. Szayna M, Doyle ME, Betkey JA, Holloway HW, Spencer RGS, Greig NH, Egan JM. Exendin-4 decelerates food intake, weight gain, and fat deposition in Zucker rats. Endocrinology 141: 1936-1941, 2000.
54. Tews D, Lehr S, Hartwig S, Osmers A, PaBlack W, Eckel J. Antiapoptotic action of Exendin-4 in INS-1 beta-cells: comparative protein pattern analysis of isolated mitochondria. Horm Metab Res 41: 294-301, 2009.
55. Thorens B, Porret A, Buhler L, Deng SP, Morel P, Widmann C. Cloning and functional expression of the human islet GLP-1 receptor. Demonstration that Ex-4 is an agonist and exendin-(9-39) an antagonist of the receptor. Diabetes 42: 1678-1682, 1993. (Pubitemid 23318127)
56. Toft-Nielson M, Madsbad S, Holst JJ. The effect of glucagon-like peptide I (GLP-I) on glucose elimination in healthy subjects depends on the pancreatic glucoregulatory hormones. Diabetes 45: 552-556, 1996. (Pubitemid 26140536)
57. Trapote MA, Clemente F, Galera C, Morales M, Alcantara AI, Lopez-Delgado MI, Villanueva-Penacarrillo ML, Valverde I. Inositolphosphoglycans are possible mediators of the glucagon-like peptide 1 (7-36) amide action in the liver. J Endocrinol Invest 19: 114-118, 1996. (Pubitemid 26107181)
58. Vahl TP, Tauchi M, Durler TS, Elfers EE, Fernandes TM, Bitner RD, Ellis KS, Woods SC, Seeley RJ, Herman JP, D'Alessio DA. Glucagon-like peptide-1 (GLP-1) receptors expressed on nerve terminals in the portal vein mediate the effects of endogenous GLP-1 on glucose tolerance in rats. Endocrinology 148: 4965-4973, 2007. (Pubitemid 47481523)
59. Valera A, Pujol A, Pelegrin M, Bosch F. Transgenic mice overexpressing phosphoenolpyruvate carboxykinase develop non-insulin-dependent diabetes mellitus. Proc Natl Acad Sci USA 91: 151-9154, 1994.
60. Valverde I, Morales M, Clemente F, Lopex-Delgado MI, Delgado E, Perea A, Villanueva-Penacarrillo ML. Glucagon-like peptide 1: a potent glycogenic hormone. FEBS Lett 349: 13-316, 1994.
61. Vella A, Shah P, Basu R, Basu A, Holst JJ, Rizza RA. Effect of glucagon-like peptide 1(7-36) amide on glucose effectiveness and insulin action in people with type 2 diabetes. Diabetes 49: 611-617, 2000. (Pubitemid 30183750)
62. Vella A, Shah P, Reed AS, Adkins AS, Basu R, Rizza RA. Lack of effect of exendin-4 and glucagon-like peptide-1-(7,36)-amide on insulin action in non-diabetic humans. Diabetologia 45: 1410-1415, 2002. (Pubitemid 35244894)
63. Vuguin P, Raab E, Liu B, Barzilai N, Simmons RA. Hepatic insulin resistance precedes the development of diabetes in a model of intrauterine growth retardation. Diabetes 53: 2617-2622, 2004. (Pubitemid 39299270)
64. Wheeler MB, Lu M, Dilon JS, Leng XH, Chen C, Boyd AE. Functional expression of the rat glucagon-like receptor, evidence for coupling to both adenyl cyclase and phospholipase-C. Endocrinology 133: 57-62, 1993. (Pubitemid 23206374)
65. Yamato E, Ikegami H, Takekawa K, Fujisawa T, Nakagawa Y, Hamada Y, Ueda H, Ogihara T. Tissue-specific and glucose-dependent expression of receptor genes for glucagon and glucagon-like peptide-1 (GLP-1). Horm Metab Res 29: 56-59, 1997. (Pubitemid 27170091)
66. Young AA, Gedulin BR, Bhavzar S, Bodkin N, Jodka C, Hansen B, Denaro M. Glucose lowering and insulin-sensitizing actions of exendin-4: studies in obese diabetic (ob/ob, db/db) mice, diabetic fatty Zucker rats, and diabetic rhesus monkeys (Macaca mulatta). Diabetes 48: 1026-1034, 1999. (Pubitemid 29226349)