Resistance to the beneficial metabolic effects and hepatic antioxidant defense actions of fibroblast growth factor 21 treatment in growth hormone-overexpressing transgenic mice

International Journal of Endocrinology

Volumn 2015, Issue , 2015, Pages

  Boparai, Ravneet K ^a,b   Arum, Oge ^a   Miquet, Johanna G ^a,c   Masternak, Michal M ^a,d,e   Bartke, Andrzej ^a   Khardori, Romesh K ^a,f  

^a SOUTHERN ILLINOIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b PANJAB UNIVERSITY   (India)

^c UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^d UNIVERSITY OF CENTRAL FLORIDA COLLEGE OF MEDICINE   (United States)

^e GREATER POLAND CANCER CENTRE   (Poland)

^f EASTERN VIRGINIA MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYL COENZYME A CARBOXYLASE; ACYL COENZYME A OXIDASE; ACYL COENZYME A OXIDASE 1; AGOUTI RELATED PROTEIN; CARNITINE PALMITOYLTRANSFERASE 1ALPHA; CARNITINE PALMITOYLTRANSFERASE I; CATALASE; COCAINE AND AMPHETAMINE REGULATED TRANSCRIPT PEPTIDE; FATTY ACID SYNTHASE; FIBROBLAST GROWTH FACTOR 21; GLUCOSE 6 PHOSPHATASE; GLUTATHIONE PEROXIDASE 1; GROWTH HORMONE; HEPATOCYTE NUCLEAR FACTOR 1ALPHA; HEPATOCYTE NUCLEAR FACTOR 4ALPHA; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; INSULIN RECEPTOR; INSULIN RECEPTOR SUBSTRATE 1; INSULIN RECEPTOR SUBSTRATE 2; LEPTIN RECEPTOR; MANGANESE SUPEROXIDE DISMUTASE; MELANIN CONCENTRATING HORMONE; OREXIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PHOSPHOENOLPYRUVATE CARBOXYKINASE (GTP); PROOPIOMELANOCORTIN; SIRTUIN 1; TRANSCRIPTION FACTOR FKHRL1; UNCLASSIFIED DRUG; UNCOUPLING PROTEIN 2;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTINUOUS INFUSION; CONTROLLED STUDY; GENE EXPRESSION; HYPERINSULINEMIA; INTRACELLULAR SIGNALING; MOUSE; NONHUMAN; PRIORITY JOURNAL; TRANSGENIC MOUSE;

EID: 84930638386     PISSN: 16878337     EISSN: 16878345     Source Type: Journal    
DOI: 10.1155/2015/282375     Document Type: Article

References (54)

1. S. Wild, G. Roglic, A. Green, R. Sicree, and H. King, "Global prevalence of diabetes: estimates for the year 2000 and projections for 2030," Diabetes Care, vol. 27,no. 5, pp. 1047-1053, 2004.
2. A. Kharitonenkov, V. J. Wroblewski, A. Koester et al., "The metabolic state of diabetic monkeys is regulated by fibroblast growth factor-21," Endocrinology, vol. 148, no. 2, pp. 774-781, 2007.
3. W. Wente, A. M. Efanov, M. Brenner et al., "Fibroblast growth factor-21 improves pancreatic β-cell function and survival by activation of extracellular signal-regulated kinase 1/2 and Akt signaling pathways," Diabetes, vol. 55, no. 9, pp. 2470-2478, 2006.
4. J. Xu, D. J. Lloyd, C. Hale et al., "Fibroblast growth factor 21 reverses hepatic steatosis, increases energy expenditure, and improves insulin sensitivity in diet-induced obese mice," Diabetes, vol. 58, no. 1, pp. 250-259, 2009.
5. E. S. Muise, B. Azzolina, D. W. Kuo et al., "Adipose fibroblast growth factor 21 is up-regulated by peroxisome proliferatoractivated receptor γ and altered metabolic states," Molecular Pharmacology, vol. 74, no. 2, pp. 403-412, 2008.
6. T. Nishimura, Y. Nakatake, M. Konishi, and N. Itoh, "Identification of a novel FGF, FGF-21, preferentially expressed in the liver," Biochimica et Biophysica Acta: Gene Structure and Expression, vol. 1492, no. 1, pp. 203-206, 2000.
7. S. Ito, S. Kinoshita, N. Shiraishi et al., "Molecular cloning and expression analyses of mouse βklotho, which encodes a novel Klotho family protein," Mechanisms of Development, vol. 98, no. 1-2, pp. 115-119, 2000.
8. I.Dostálová,D.Haluzíková, andM.Haluzík, "Fibroblast growth gactor 21: a novelmetabolic regulator with potential therapeutic properties in obesity/type 2 diabetes mellitus," Physiological Research, vol. 58, no. 1, pp. 1-7, 2009.
9. A. Kharitonenkov, J. D. Dunbar, H. A. Bina et al., "FGF-21/ FGF-21 receptor interaction and activation is determined by βKlotho," Journal of Cellular Physiology, vol. 215, no. 1, pp. 1-7, 2008.
10. J. S. Moyers, T. L. Shiyanova, F. Mehrbod et al., "Molecular determinants of FGF-21 activity-synergy and cross-talk with PPARγ signaling," Journal of Cellular Physiology, vol. 210, no. 1, pp. 1-6, 2007.
11. T. Inagaki, V. Y. Lin, R. Goetz, M. Mohammadi, D. J. Mangelsdorf, and S. A. Kliewer, "Inhibition of growth hormone signaling by the fasting-induced hormone FGF21," Cell Metabolism, vol. 8, no. 1, pp. 77-83, 2008.
12. M. B. Davidson, "Effect of growth hormone on carbohydrate and lipid metabolism," Endocrine Reviews, vol. 8, no. 2, pp. 115-131, 1987.
13. F. P. Dominici, D. Cifone, A. Bartke, and D. Turyn, "Loss of sensitivity to insulin at early events of the insulin signaling pathway in the liver of growth hormone-transgenic mice," Journal of Endocrinology, vol. 161, no. 3, pp. 383-392, 1999.
14. C. J. Quaife, L. S. Mathews, C. A. Pinkert, R. E. Hammer, R. L. Brinster, and R. D. Palmiter, "Histopathology associated with elevated levels of growth hormone and insulin-like growth factor I in transgenic mice," Endocrinology, vol. 124, no. 1, pp. 40-48, 1989.
15. I. Hansen, E. Tsalikian, B. Beaufrere, J. Gerich, M. Haymond, and R. Rizza, "Insulin resistance in acromegaly: defects in both hepatic and extrahepatic insulin action," American Journal of Physiology: Endocrinology and Metabolism, vol. 250, no. 3, part 1, pp. E269-E273, 1986.
16. A. Valera, J. E. Rodriguez-Gil, J. S. Yun, M. M. Mcgrane, R. W. Hanson, and F. Bosch, "Glucose metabolism in transgenic mice containing a chimeric P-enolpyruvate carboxykinase/bovine growth hormone gene," FASEB Journal, vol. 7, no. 9,pp. 791-800, 1993.
17. R. K. Boparai, O. Arum, R. Khardori, and A. Bartke, "Glucose homeostasis and insulin sensitivity in growth hormonetransgenic mice: a cross-sectional analysis," Biological Chemistry, vol. 391, no. 10, pp. 1149-1155, 2010.
18. J. G. Miquet, A. I. Sotelo, A. Bartke, and D. Turyn, "Suppression of growth hormone (GH) Janus tyrosine kinase 2/signal transducer and activator of transcription 5 signaling pathway in transgenic mice overexpressing bovine GH," Endocrinology, vol. 145, no. 6, pp. 2824-2832, 2004.
19. T.Coskun,H.A.Bina,M. A. Schneider et al., "Fibroblast growth factor 21 corrects obesity in mice," Endocrinology, vol. 149, no. 12, pp. 6018-6027, 2008.
20. F. M. Fisher, P. C. Chui, P. J. Antonellis et al., "Obesity is a fibroblast growth factor 21 (FGF21)-resistant state," Diabetes, vol. 59, no. 11, pp. 2781-2789, 2010.
21. A. Kharitonenkov, T. L. Shiyanova, A. Koester et al., "FGF-21 as a novel metabolic regulator," Journal of Clinical Investigation, vol. 115, no. 6, pp. 1627-1635, 2005.
22. Z. Wang, M. M. Masternak, K. A. Al-Regaiey, and A. Bartke, "Adipocytokines and the regulation of lipid metabolism in growth hormone transgenic and calorie-restricted mice," Endocrinology, vol. 148, no. 6, pp. 2845-2853, 2007.
23. M.W. Schwartz, S. C. Woods,D. Porte Jr., R. J. Seeley, andD. G. Baskin, "Central nervous systemcontrol of food intake," Nature, vol. 404, no. 6778, pp. 661-671, 2000.
24. Y. Kobayashi, Y. Furukawa-Hibi, C. Chen et al., "SIRT1 is critical regulator of FOXO-mediated transcription in response to oxidative stress," International Journal ofMolecularMedicine, vol. 16, no. 2, pp. 237-243, 2005.
25. T. T. Tran, N. Gupta, T. Goh et al., "Direct measure of insulin sensitivity with the hyperinsulinemic-euglycemic clamp and surrogate measures of insulin sensitivity with the oral glucose tolerance test: correlations with aberrant crypt foci promotion in rats," Cancer Epidemiology, Biomarkers & Prevention, vol. 12, no. 1, pp. 47-56, 2003.
26. M. J. Potthoff, T. Inagaki, S. Satapati et al., "FGF21 induces PGC-1α and regulates carbohydrate and fatty acidmetabolism during the adaptive starvation response," Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 26, pp. 10853-10858, 2009.
27. M. K. Badman, P. Pissios, A. R. Kennedy, G. Koukos, J. S. Flier, and E. Maratos-Flier, "Hepatic fibroblast growth factor 21 is regulated by PPARα and is a key mediator of hepatic lipid metabolism in ketotic states," Cell Metabolism, vol. 5, no. 6, pp. 426-437, 2007.
28. J. G. Miquet, L. González, M. N. Matos et al., "Transgenic mice overexpressing GH exhibit hepatic upregulation of GHsignaling mediators involved in cell proliferation," Journal of Endocrinology, vol. 198, no. 2, pp. 317-330, 2008.
29. Y. Hotta, H. Nakamura, M. Konishi et al., "Fibroblast growth factor 21 regulates lipolysis in white adipose tissue but is not required for ketogenesis and triglyceride clearance in liver," Endocrinology, vol. 150, no. 10, pp. 4625-4633, 2009.
30. J. D. McGarry and N. F. Brown, "The mitochondrial carnitine palmitoyltransferase system. From concept to molecular analysis," European Journal of Biochemistry, vol. 244, no. 1, pp. 1-14, 1997.
31. B. Viollet, F. Andreelli, S. B. Jørgensen et al., "Physiological role of AMP-activated protein kinase (AMPK): insights from knockoutmousemodels," Biochemical Society Transactions, vol. 31, no. 1, pp. 216-219, 2003.
32. W. W. Winder and D. G. Hardie, "Inactivation of acetyl-CoA carboxylase and activation of AMP-activated protein kinase in muscle during exercise," American Journal of Physiology-Endocrinology and Metabolism, vol. 270, no. 2, pp. E299-E304, 1996.
33. F. M. Fisher, P. C. Chui, P. J. Antonellis et al., "Obesity is a fibroblast growth factor 21 (FGF21)-resistant state," Diabetes, vol. 59, no. 11, pp. 2781-2789, 2010.
34. D. E. Berryman, E. O. List, K. T. Coschigano, K. Behar, J. K. Kim, and J. J. Kopchick, "Comparing adiposity profiles in three mouse models with altered GH signaling," Growth Hormone & IGF Research, vol. 14, no. 4, pp. 309-318, 2004.
35. J. L. Evans, I. D. Goldfine, B. A. Maddux, and G. M. Grodsky, "Are oxidative stress-activated signaling pathways mediators of insulin resistance and β-cell dysfunction?" Diabetes, vol. 52, no. 1, pp. 1-8, 2003.
36. R. A. Simmons, "Developmental origins of diabetes: the role of oxidative stress," Free Radical Biology and Medicine, vol. 40, no. 6, pp. 917-922, 2006.
37. A. B. Salmon, A. Richardson, and V. I. Pérez, "Update on the oxidative stress theory of aging: does oxidative stress play a role in aging or healthy aging?" Free Radical Biology&Medicine, vol. 48, no. 5, pp. 642-655, 2010.
38. M. D. L. Chau, J. Gao, Q. Yang, Z. Wu, and J. Gromada, "Fibroblast growth factor 21 regulates energy metabolism by activating the AMPK-SIRT1-PGC-1α pathway," Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 28, pp. 12553-12558, 2010.
39. Z. Wu, P. Puigserver, U. Andersson et al., "Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1," Cell, vol. 98, no. 1, pp. 115-124, 1999.
40. Z. B. Andrews and T. L. Horvath, "Uncoupling protein-2 regulates lifespan in mice," American Journal of Physiology: Endocrinology and Metabolism, vol. 296, no. 4, pp. E621-E627, 2009.
41. C. Pecqueur, T. Bui, C. Gelly et al., "Uncoupling protein-2 controls proliferation by promoting fatty acid oxidation and limiting glycolysis-derived pyruvate utilization," The FASEB Journal, vol. 22, no. 1, pp. 9-18, 2008.
42. A. Brunet, L. B. Sweeney, J. F. Sturgill et al., "Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase," Science, vol. 303, no. 5666, pp. 2011-2015, 2004.
43. G. J. P. L. Kops, T. B. Dansen, P. E. Polderman et al., "Forkhead transcription factor FOXO3a protects quiescent cells from oxidative stress," Nature, vol. 419, no. 6904, pp. 316-321, 2002.
44. J.W. Eriksson, "Metabolic stress in insulin's target cells leads to ROS accumulation - a hypothetical common pathway causing insulin resistance," FEBS Letters, vol. 581, no. 19, pp. 3734-3742, 2007.
45. S. Kawahito, H. Kitahata, and S. Oshita, "Problems associated with glucose toxicity: role of hyperglycemia-induced oxidative stress," World Journal of Gastroenterology, vol. 15, no. 33, pp. 4137-4142, 2009.
46. R.Gredilla andG.Barja, "The role of oxidative stress in relation to caloric restriction and longevity," Endocrinology, vol. 146, no. 9, pp. 3713-3717, 2005.
47. Y. Zhang, Y. Xie, E.D. Berglund et al., "The starvation hormone, fibroblast growth factor-21, extends lifespan in mice," eLife, vol. 2012, no. 1, Article ID e00065, 2012.
48. C. Kenyon, "Longevity: could a hormone point the way to life extension?" Elife, vol. 1, Article IDe00286, 2012.
49. Y. Li, K.Wong, A. Giles et al., "Hepatic SIRT1 attenuates hepatic steatosis and controls energy balance in mice by inducing fibroblast growth factor 21," Gastroenterology, vol. 146, no. 2, pp. 539.e7-549.e7, 2014.
50. F.M.Fisher, J. L. Estall,A.C.Adams et al., "Integratedregulation of hepatic metabolism by fibroblast growth factor 21 (FGF21) in vivo," Endocrinology, vol. 152, no. 8, pp. 2996-3004, 2011.
51. Y. Zhou, B. C. Xu, H. G. Maheshwari et al., "A mammalian model for Laron syndrome produced by targeted disruption of themouse growth hormone receptor/binding protein gene (the Laron mouse)," Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 24, pp. 13215-13220, 1997.
52. M. M. McGrane, J. de Vente, J. Yun et al., "Tissue-specific expression and dietary regulation of a chimeric phosphoenolpyruvate carboxykinase/bovine growth hormone gene in transgenic mice," Journal of Biological Chemistry, vol. 263, no. 23, pp. 11443-11451, 1988.
53. C. Hale, M. M. Chen, S. Stanislaus et al., "Lack of overt FGF21 resistance in two mouse models of obesity and insulin resistance," Endocrinology, vol. 153, no. 1, pp. 69-80, 2012.
54. P. Chomczynski and N. Sacchi, "Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction," Analytical Biochemistry, vol. 162, no. 1, pp. 156-159, 1987.