Increased fibroblast growth factor 21 expression in high-fat diet-sensitive non-human primates (Macaca mulatta)

International Journal of Obesity

Volumn 38, Issue 2, 2014, Pages 183-191

  Nygaard, E B ^a,b   Moller C L ^a   Kievit, P ^c   Grove, K L ^c   Andersen, B ^b  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b NOVO NORDISK A S   (Denmark)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

klotho; diet induced obesity; FGF21 resistance; FGFR1; high fat diet; rhesus macaque

Indexed keywords

CHOLESTEROL; FIBROBLAST GROWTH FACTOR 21; GLUCOSE; TRIACYLGLYCEROL;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CHOLESTEROL BLOOD LEVEL; COHORT ANALYSIS; CONTROLLED STUDY; DIABETES MELLITUS; DOWN REGULATION; GLUCOSE STIMULATED INSULIN SECRETION; GLUCOSE TOLERANCE; INSULIN RELEASE; INSULIN SENSITIVITY; INTRAVENOUS GLUCOSE TOLERANCE TEST; LIPID BLOOD LEVEL; LIPID DIET; LIVER; MALE; NONHUMAN; OBESITY; PANCREAS; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; RHESUS MONKEY; SKELETAL MUSCLE; WHITE ADIPOSE TISSUE;

ANIMALIA; MACACA MULATTA; PRIMATES; RODENTIA;

ADIPOSE TISSUE, WHITE; ANIMALS; BLOOD GLUCOSE; BODY WEIGHT; CHOLESTEROL; DIET, HIGH-FAT; DYSLIPIDEMIAS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FIBROBLAST GROWTH FACTORS; GENE EXPRESSION REGULATION; GLUCOSE TOLERANCE TEST; HYPERGLYCEMIA; INSULIN RESISTANCE; LIVER; MACACA MULATTA; MALE; MICE; MICE, INBRED NOD; MUSCLE, SKELETAL; OBESITY; PROMOTER REGIONS, GENETIC; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER; TRIGLYCERIDES;

EID: 84896740306     PISSN: 03070565     EISSN: 14765497     Source Type: Journal    
DOI: 10.1038/ijo.2013.79     Document Type: Article

References (54)

1. Badman MK, Pissios P, Kennedy AR, Koukos G, Flier JS, Maratos-Flier E. Hepatic fibroblast growth factor 21 is regulated by PPARalpha and is a key mediator of hepatic lipid metabolism in ketotic states. Cell Metab 2007; 5: 426-437
2. Badman MK, Koester A, Flier JS, Kharitonenkov A, Maratos-Flier E. Fibroblast growth factor 21-deficient mice demonstrate impaired adaptation to ketosis. Endocrinology 2009; 150: 4931-4940
3. Inagaki T, Dutchak P, Zhao G, Ding X, Gautron L, Parameswara V et al. Endocrine regulation of the fasting response by PPARalpha-mediated induction of fibroblast growth factor 21. Cell Metab 2007; 5: 415-425
4. Kharitonenkov A, Shiyanova TL, Koester A, Ford AM, Micanovic R, Galbreath EJ et al. FGF-21 as a novel metabolic regulator. J Clin Invest 2005; 115: 1627-1635
5. Wente W, Efanov AM, Brenner M, Kharitonenkov A, Koster A, Sandusky GE et al. Fibroblast growth factor-21 improves pancreatic beta-cell function and survival by activation of extracellular signal-regulated kinase 1/2 and Akt signaling pathways. Diabetes 2006; 55: 2470-2478
6. Goetz R, Beenken A, Ibrahimi OA, Kalinina J, Olsen SK, Eliseenkova AV et al. Molecular insights into the klotho-dependent, endocrine mode of action of fibroblast growth factor 19 subfamily members. Mol Cell Biol 2007; 27: 3417-3428
7. Itoh N, Ornitz DM. Functional evolutionary history of the mouse Fgf gene family. Dev Dyn 2008; 237: 18-27
8. Fon TK, Bookout AL, Ding X, Kurosu H, John GB, Wang L et al. Research resource: Comprehensive expression atlas of the fibroblast growth factor system in adult mouse. Mol Endocrinol 2010; 24: 2050-2064
9. Nishimura T, Nakatake Y, Konishi M, Itoh N. Identification of a novel FGF, FGF-21, preferentially expressed in the liver. Biochimica et Biophysica Acta (BBA)-Gene Structure and Expression 2000; 1492: 203-206
10. Hojman P, Pedersen M, Nielsen AR, Krogh-Madsen R, Yfanti C, Akerstrom T et al. Fibroblast growth factor-21 is induced in human skeletal muscles by hyperinsulinemia. Diabetes 2009; 58: 2797-2801
11. Izumiya Y, Bina HA, Ouchi N, Akasaki Y, Kharitonenkov A, Walsh K. FGF21 is an Aktregulated myokine. FEBS Lett 2008; 582: 3805-3810
12. Mraz M, Bartlova M, Lacinova Z, Michalsky D, Kasalicky M, Haluzikova D et al. Serum concentrations and tissue expression of a novel endocrine regulator fibroblast growth factor-21 in patients with type 2 diabetes and obesity. Clin Endocrinol 2009; 71: 369-375
13. Muise ES, Azzolina B, Kuo DW, El-Sherbeini M, Tan Y, Yuan X et al. Adipose fibroblast growth factor 21 is up-regulated by peroxisome proliferator-Activated receptor gamma and altered metabolic states. Mol Pharmacol 2008; 74: 403-412
14. Wang H, Qiang L, Farmer SR. Identification of a domain within peroxisome proliferator-Activated receptor gamma regulating expression of a group of genes containing fibroblast growth factor 21 that are selectively repressed by SIRT1 in adipocytes. Mol Cell Biol 2008; 28: 188-200
15. Zhang X, Yeung DC, Karpisek M, Stejskal D, Zhou ZG, Liu F et al. Serum FGF21 levels are increased in obesity and are independently associated with the metabolic syndrome in humans. Diabetes 2008; 57: 1246-1253
16. Gupte J, Yang L, Wu X, Weiszmann J, Hecht R, Lemon B et al. The FGFR D3 domain determines receptor selectivity for fibroblast growth factor 21. J Mol Biol 2011; 408: 491-502
17. Kurosu H, Choi M, Ogawa Y, Dickson AS, Goetz R, Eliseenkova AV et al. Tissuespecific expression of betaKlotho and fibroblast growth factor (FGF) receptor isoforms determines metabolic activity of FGF19 and FGF21. J Biol Chem 2007; 282: 26687-26695
18. Ogawa Y, Kurosu H, Yamamoto M, Nandi A, Rosenblatt KP, Goetz R et al. BetaKlotho is required for metabolic activity of fibroblast growth factor 21. Proc Natl Acad Sci USA 2007; 104: 7432-7437
19. Suzuki M, Uehara Y, Motomura-Matsuzaka K, Oki J, Koyama Y, Kimura M et al. BetaKlotho is required for fibroblast growth factor (FGF) 21 signaling through FGF receptor (FGFR) 1c and FGFR3c. Mol Endocrinol 2008; 22: 1006-1014
20. Ge H, Baribault H, Vonderfecht S, Lemon B, Weiszmann J, Gardner J et al. Characterization of a FGF19 variant with altered receptor specificity revealed a central role for FGFR1c in the regulation of glucose metabolism. PLoS One 2012; 7: E33603
21. Yang C, Jin C, Li X, Wang F, McKeehan WL, Luo Y. Differential specificity of endocrine FGF19 and FGF21 to FGFR1 and FGFR4 in complex with KLB. PLoS One 2012; 7: E33870
22. Yie J,WangW, Deng L, Tam LT, Stevens J, Chen MM et al. Understanding the physical interactions in the FGF21/FGFR/beta-klotho complex: Structural requirements and implications in FGF21 signaling. Chem Biol Drug Design 2012; 79: 398-410
23. Lundasen T, Hunt MC, Nilsson LM, Sanyal S, Angelin B, Alexson SE et al. PPARalpha is a key regulator of hepatic FGF21. Biochem Biophys Res Commun 2007; 360: 437-440
24. Galman C, Lundasen T, Kharitonenkov A, Bina HA, Eriksson M, Hafstrom I et al. The circulating metabolic regulator FGF21 is induced by prolonged fasting and PPARalpha activation in man. Cell Metab 2008; 8: 169-174
25. Potthoff MJ, Inagaki T, Satapati S, Ding X, He T, Goetz R et al. FGF21 induces PGC-1alpha and regulates carbohydrate and fatty acid metabolism during the adaptive starvation response. Proc Natl Acad Sci USA 2009; 106: 10853-10858
26. Dutchak PA, Katafuchi T, Bookout AL, Choi JH, Yu RT, Mangelsdorf DJ et al. Fibroblast growth factor-21 regulates PPARgamma activity and the antidiabetic actions of thiazolidinediones. Cell 2012; 148: 556-567
27. Oishi K, Konishi M, Murata Y, Itoh N. Time-imposed daily restricted feeding induces rhythmic expression of Fgf21 in white adipose tissue of mice. Biochem Biophys Res Commun 2011; 412: 396-400
28. Uebanso T, Taketani Y, Yamamoto H, Amo K, Ominami H, Arai H et al. Paradoxical regulation of human FGF21 by both fasting and feeding signals: Is FGF21 a nutritional adaptation factor? PLoS One 2011; 6: E22976
29. Vienberg SG, Brons C, Nilsson E, Astrup A, Vaag A, Andersen B. Impact of shortterm high-fat feeding and insulin-stimulated FGF21 levels in subjects with low birth weight and controls. Eur J Endocrinol 2012; 167: 49-57
30. Coskun T, Bina HA, Schneider MA, Dunbar JD, Hu CC, Chen Y et al. Fibroblast growth factor 21 corrects obesity in mice. Endocrinology 2008; 149: 6018-6027
31. Xu J, Lloyd DJ, Hale C, Stanislaus S, Chen M, Sivits G et al. Fibroblast growth factor 21 reverses hepatic steatosis, increases energy expenditure, and improves insulin sensitivity in diet-induced obese mice. Diabetes 2009; 58: 250-259
32. Xu J, Stanislaus S, Chinookoswong N, Lau YY, Hager T, Patel J et al. Acute glucoselowering and insulin-sensitizing action of FGF21 in insulin-resistant mouse models-Association with liver and adipose tissue effects. Am J Physiol Endocrinol Metab 2009; 297: E1105-E1114
33. Kharitonenkov A, Wroblewski VJ, Koester A, Chen YF, Clutinger CK, Tigno XT et al. The metabolic state of diabetic monkeys is regulated by fibroblast growth factor-21. Endocrinology 2007; 148: 774-781
34. Vé niant MM, Komorowski R, Chen P, Stanislaus S, Winters K, Hager T et al. Long-Acting FGF21 has enhanced efficacy in diet-induced obese mice and in obese rhesus monkeys. Endocrinology 2012; 153: 4192-4203
35. Adams AC, Yang C, Coskun T, Cheng CC, Gimeno RE, Luo Y et al. The breadth of FGF21's metabolic actions are governed by FGFR1 in adipose tissue. Mol Metab 2013; 2: 31-37
36. Ding X, Boney-Montoya J, Owen BM, Bookout AL, Coate KC, Mangelsdorf DJ et al. Beta-klotho is required for fibroblast growth factor 21 effects on growth and metabolism. Cell Metab 2012; 16: 387-393
37. Badman MK, Kennedy AR, Adams AC, Pissios P, Maratos-Flier E. A very low carbohydrate ketogenic diet improves glucose tolerance in ob/ob mice independently of weight loss. Am J Physiol Endocrinol Metab 2009; 297: E1197-E1204
38. Chen WW, Li L, Yang GY, Li K, Qi XY, Zhu W et al. Circulating FGF-21 levels in normal subjects and in newly diagnose patients with type 2 diabetes mellitus. Exp Clin Endocrinol Diabetes 2008; 116: 65-68
39. Dushay J, Chui PC, Gopalakrishnan GS, Varela-Rey M, Crawley M, Fisher FM et al. Increased fibroblast growth factor 21 in obesity and nonalcoholic fatty liver disease. Gastroenterology 2010; 139: 456-463
40. Li H, Bao Y, Xu A, Pan X, Lu J, Wu H et al. Serum fibroblast growth factor 21 is associated with adverse lipid profiles and gamma- glutamyltransferase but not insulin sensitivity in chinese subjects. J Clin Endocrinol Metab 2009; 94: 2151-2156
41. Li L, Yang G, Ning H, Yang M, Liu H, Chen W. Plasma FGF-21 levels in type 2 diabetic patients with ketosis. Diabetes Res Clin Pract 2008; 82: 209-213
42. Fisher FM, Chui PC, Antonellis PJ, Bina HA, Kharitonenkov A, Flier JS et al. Obesity is a fibroblast growth factor 21 (FGF21)-resistant state. Diabetes 2010; 59: 2781-2789
43. Hale C, Chen MM, Stanislaus S, Chinookoswong N, Hager T, Wang M et al. Lack of overt FGF21 resistance in two mouse models of obesity and insulin resistance. Endocrinology 2012; 153: 69-80
44. Hansen BC. Primates in the experimental pharmacology of obesity. In: Lockwood Dean H and Heffner Thomas C (eds). Obesity: Pathology and therapy; Springer: Berlin, Heidelberg, 2000, pp 461-489
45. Schäfer SA, Hansen BC, Völkl A, Fahimi HD, Pill J. Biochemical and morphological effects of K-111, a peroxisome proliferator-Activated receptor (PPAR)alpha activator, in non-human primates. Biochem Pharmacol 2004; 68: 239-251
46. Winegar DA, Brown PJ, Wilkison WO, Lewis MC, Ott RJ, Tong WQ et al. Effects of fenofibrate on lipid parameters in obese rhesus monkeys. J Lipid Res 2001; 42: 1543-1551
47. Rozen S, Skaletsky H. Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 2000; 132: 365-386
48. Johnson CL, Weston JY, Chadi SA, Fazio EN, Huff MW, Kharitonenkov A et al. Fibroblast growth factor 21 reduces the severity of cerulein-induced pancreatitis in mice. Gastroenterology 2009; 137: 1795-1804
49. Fon Tacer K, Bookout AL, Ding X, Kurosu H, John GB, Wang L et al. Research resource: Comprehensive expression atlas of the fibroblast growth factor system in adult mouse. Mol Endocrinol 2010; 24: 2050-2064
50. Hondares E, Iglesias R, Giralt A, Gonzalez FJ, Giralt M, Mampel T et al. Thermogenic activation induces FGF21 expression and release in Brown adipose tissue. J Biol Chem 2011; 286: 12983-12990
51. Vienberg SG, Brøns C, Nilsson E, Astrup AV, Vaag A, Andersen B. Impact of short term high fat feeding and insulin stimulated FGF21 levels in subjects with low birth weight and controls. Eu J Endocrinol 2012; 167: 49-57
52. Fisher fM, Kleiner S, Douris N, Fox EC, Mepani RJ, Verdeguer F et al. FGF21 regulates PGC-1alpha and browning of white adipose tissues in adaptive thermogenesis. Genes Dev 2012; 26: 271-281
53. Tontonoz P, Spiegelman BM. Fat and beyond: The diverse biology of PPARgamma. Annu Rev Biochem 2008; 77: 289-312
54. Mashili FL, Austin RL, Deshmukh AS, Fritz T, Caidahl K, Bergdahl K et al. Direct effects of FGF21 on glucose uptake in human skeletal muscle: Implications for type 2 diabetes and obesity. Diabetes Metab Res Rev 2011; 27: 286-297