Plasma FGF21 is elevated by the intense lipid mobilization of lactation

Endocrinology

Volumn 152, Issue 12, 2011, Pages 4652-4661

  Schoenberg, Katie M ^a   Giesy, Sarah L ^a   Harvatine, Kevin J ^b   Waldron, Matthew R ^a   Cheng, Christine ^c   Kharitonenkov, Alexei ^c   Boisclair, Yves R ^a  

^a Department of Molecular Biology and Genetics   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c ELI LILLY AND COMPANY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA KLOTHO PROTEIN; FIBROBLAST GROWTH FACTOR 21; FIBROBLAST GROWTH FACTOR RECEPTOR; GLUCOSE; INSULIN; KLOTHO PROTEIN; SOMATOMEDIN C; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIRTH; CONTROLLED STUDY; CYTOKINE PRODUCTION; DAIRY CATTLE; ENERGY CONSUMPTION; ENERGY EXPENDITURE; FEMALE; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; INSULIN BLOOD LEVEL; LACTATION; LIPID METABOLISM; LIPID STORAGE; LIVER; MAMMARY GLAND; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; SKELETAL MUSCLE; THIRD TRIMESTER PREGNANCY; WHITE ADIPOSE TISSUE;

ADIPOSE TISSUE, WHITE; ANIMALS; CATTLE; FEMALE; FIBROBLAST GROWTH FACTORS; LACTATION; LIPID MOBILIZATION; LIVER; MEMBRANE PROTEINS; PREGNANCY; TISSUE DISTRIBUTION;

EID: 82355188226     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2011-1425     Document Type: Article

References (53)

1. Vernon RG, Denis RG, Sorensen A, Williams G 2002 Leptin and the adaptations of lactation in rodents and ruminants. Horm Metab Res 34:678-685 (Pubitemid 36398707)
2. Vernon RG 2005 Lipid metabolism during lactation: a review of adipose tissue-liver interactions and the development of fatty liver. J Dairy Res 72:460-469 (Pubitemid 41570083)
3. Drackley JK, Overton TR, Douglas GN 2001 Adaptations of glucose and long-chain fatty acid metabolism in liver of dairy cows during the periparturient period. J Dairy Sci 84:E100-E112
4. Bell AW 1995 Regulation of organic nutrient metabolism during transition from late pregnancy to early lactation. J Anim Sci 73:2804-2819
5. Desvergne B, Michalik L, WahliW2006 Transcriptional regulation of metabolism. Physiol Rev 86:465-514
6. Loor JJ, DannHM,Everts RE, Oliveira R, Green CA, Guretzky NA, Rodriguez-Zas SL, Lewin HA, Drackley JK 2005 Temporal gene expression profiling of liver from periparturient dairy cows reveals complex adaptive mechanisms in hepatic function. Physiol Genomics 23:217-226 (Pubitemid 44437980)
7. Wolfrum C, Asilmaz E, Luca E, Friedman JM, Stoffel M 2004 Foxa2 regulates lipid metabolism and ketogenesis in the liver during fasting and in diabetes. Nature 432:1027-1032 (Pubitemid 40052233)
8. Bobe G, Young JW, Beitz DC 2004 Invited review: pathology, etiology, prevention, and treatment of fatty liver in dairy cows. J Dairy Sci 87:3105-3124 (Pubitemid 39408446)
9. Goff JP 2006 Major advances in our understanding of nutritional influences on bovine health. J Dairy Sci 89:1292-1301 (Pubitemid 44365892)
10. Domouzoglou EM, Maratos-Flier E 2011 Fibroblast growth factor 21 is a metabolic regulator that plays a role in the adaptation to ketosis. Am J Clin Nutr 93:901S-905S
11. Kliewer SA, Mangelsdorf DJ 2010 Fibroblast growth factor 21: from pharmacology to physiology. Am J Clin Nutr 91:254S-257S
12. Kharitonenkov A, Shiyanova TL, Koester A, Ford AM, Micanovic R, Galbreath EJ, Sandusky GE, Hammond LJ, Moyers JS, Owens RA, Gromada J, Brozinick JT, Hawkins ED, Wroblewski VJ, Li DS, Mehrbod F, Jaskunas SR, Shanafelt AB 2005 FGF-21 as a novel metabolic regulator. J Clin Invest 115:1627-1635 (Pubitemid 40814671)
13. Kharitonenkov A, Larsen P 2011 FGF21 reloaded: challenges of a rapidly growing field. Trends Endocrinol Metab 22:81-86
14. Rydén M 2009 Fibroblast growth factor 21: an overview from a clinical perspective. Cell Mol Life Sci 66:2067-2073
15. Long YC, Kharitonenkov A 2011 Hormone-like fibroblast growth factors and metabolic regulation. Biochim Biophys Acta 1812:791-795
16. Itoh N 2010 Hormone-like (endocrine) Fgfs: their evolutionary history and roles in development, metabolism, and disease. Cell Tissue Res 342:1-11
17. Badman MK, Pissios P, Kennedy AR, Koukos G, Flier JS, Maratos-Flier E 2007 Hepatic fibroblast growth factor 21 is regulated by PPARα and is a key mediator of hepatic lipid metabolism in ketotic states. Cell Metab 5:426-437 (Pubitemid 46825495)
18. Inagaki T, Dutchak P, Zhao G, Ding X, Gautron L, Parameswara V, Li Y, Goetz R, Mohammadi M, Esser V, Elmquist JK, Gerard RD, Burgess SC, Hammer RE, Mangelsdorf DJ, Kliewer SA 2007 Endocrine regulation of the fasting response by PPARα-mediated induction of fibroblast growth factor 21. Cell Metab 5:415-425 (Pubitemid 46825496)
19. OgawaY, Kurosu H,YamamotoM,Nandi A, Rosenblatt KP, Goetz R, Eliseenkova AV, Mohammadi M, Kuro-o M 2007 β-Klotho is required for metabolic activity of fibroblast growth factor 21. Proc Natl Acad Sci USA 104:7432-7437 (Pubitemid 47185923)
20. Kharitonenkov A, Dunbar JD, Bina HA, Bright S, Moyers JS, Zhang C, Ding L, Micanovic R, Mehrbod SF, Knierman MD, Hale JE, Coskun T, Shanafelt AB 2008 FGF-21/FGF-21 receptor interaction and activation is determined by β-Klotho. J Cell Physiol 215:1-7 (Pubitemid 351363185)
21. Kurosu H, Choi M, Ogawa Y, Dickson AS, Goetz R, Eliseenkova AV, Mohammadi M, Rosenblatt KP, Kliewer SA, Kuro-o M 2007 Tissue-specific expression of β-Klotho and fibroblast growth factor (FGF) receptor isoforms determines metabolic activity of FGF19 and FGF21. J Biol Chem 282:26687-26695 (Pubitemid 47501965)
22. Badman MK, Koester A, Flier JS, Kharitonenkov A, Maratos-Flier E 2009 Fibroblast growth factor 21-deficient mice demonstrate impaired adaptation to ketosis. Endocrinology 150:4931-4940
23. Hotta Y, Nakamura H, Konishi M, Murata Y, Takagi H, Matsumura S, Inoue K, Fushiki T, Itoh N 2009 Fibroblast growth factor 21 regulates lipolysis in white adipose tissue but is not required for ketogenesis and triglyceride clearance in liver. Endocrinology 150:4625-4633
24. Tyynismaa H, Carroll CJ, Raimundo N, Ahola-Erkkil äS, Wenz T, Ruhanen H, Guse K, Hemminki A, Peltola-Mjosund KE, Tulkki V, Oresic M, Moraes CT, Pietiläinen K, Hovatta I, Suomalainen A 2010 Mitochondrial myopathy induces a starvation-like response. Hum Mol Genet 19:3948-3958
25. Izumiya Y, Bina HA, Ouchi N, Akasaki Y, Kharitonenkov A, Walsh K 2008 FGF21 is an Akt-regulated myokine. FEBS Lett 582:3805-3810
26. Muise ES, Azzolina B, Kuo DW, El-Sherbeini M, Tan Y, Yuan X, Mu J, Thompson JR, Berger JP, Wong KK 2008 Adipose fibroblast growth factor 21 is up-regulated by peroxisome proliferator-activated receptor γ and altered metabolic states. Mol Pharmacol 74:403-412
27. Zhang X, Yeung DC, Karpisek M, Stejskal D, Zhou ZG, Liu F, Wong RL, Chow WS, Tso AW, Lam KS, Xu A 2008 Serum FGF21 levels are increased in obesity and are independently associated with the metabolic syndrome in humans. Diabetes 57:1246-1253
28. National Research Council 2001 Nutrient requirements of dairy cattle. 7th revised ed. Washington, DC: National Academy Press
29. Block SS, Butler WR, Ehrhardt RA, Bell AW, Van Amburgh ME, Boisclair YR 2001 Decreased concentration of plasma leptin in periparturient dairy cows is caused by negative energy balance. J Endocrinol 171:339-348 (Pubitemid 33061711)
30. Bernal-Santos G, Perfield 2nd JW, Barbano DM, Bauman DE, Overton TR 2003 Production responses of dairy cows to dietary supplementation with conjugated linoleic acid (CLA) during the transition period and early lactation. J Dairy Sci 86:3218-3228 (Pubitemid 38995027)
31. Thorn SR, Ehrhardt RA, Butler WR, Quirk SM, Boisclair YR 2008 Insulin regulates hepatic leptin receptor expression in early lactating dairy cows. Am J Physiol Regul Integr Comp Physiol 295:R1455-R1462
32. Soberon F, Lukas JL, Van Amburgh ME, Capuco AV, Galton DM, Overton TR 2010 Effects of increased milking frequency on metabolism and mammary cell proliferation in Holstein dairy cows. J Dairy Sci 93:565-573
33. Rhoads RP, Kim JW, Van Amburgh ME, Ehrhardt RA, Frank SJ, Boisclair YR 2007 Effect of nutrition on the GH responsiveness of liver and adipose tissue in dairy cows. J Endocrinol 195:49-58 (Pubitemid 350055998)
34. Butte NF, Hopkinson JM, Mehta N, Moon JK, Smith EO 1999 Adjustments in energy expenditure and substrate utilization during late pregnancy and lactation. Am J Clin Nutr 69:299-307 (Pubitemid 29065555)
35. Gälman C, Lundåsen T, Kharitonenkov A, Bina HA, Eriksson M, Hafström I, Dahlin M, Amark P, Angelin B, Rudling M 2008 The circulating metabolic regulator FGF21 is induced by prolonged fasting and PPARα activation in man. Cell Metab 8:169-174
36. Fon Tacer K, Bookout AL, Ding X, Kurosu H, John GB, Wang L, Goetz R, Mohammadi M, Kuro-o M, Mangelsdorf DJ, Kliewer SA 2010 Research resource: comprehensive expression atlas of the fibroblast growth factor system in adult mouse. Mol Endocrinol 24:2050-2064
37. Hondares E, Rosell M, Gonzalez FJ, Giralt M, Iglesias R, Villarroya F 2010 Hepatic FGF21 expression is induced at birth via PPARα in response to milk intake and contributes to thermogenic activation of neonatal brown fat. Cell Metab 11:206-212
38. Yu H, Xia F, Lam KS, Wang Y, Bao Y, Zhang J, Gu Y, Zhou P, Lu J, Jia W, Xu A 2011 Circadian rhythm of circulating fibroblast growth factor 21 (FGF21) is related to the diurnal changes in fatty acids in humans. Clin Chem 57:691-700
39. Li H, Fang Q, Gao F, Fan J, Zhou J, Wang X, Zhang H, Pan X, Bao Y, Xiang K, Xu A, Jia W 2010 Fibroblast growth factor 21 levels are increased in nonalcoholic fatty liver disease patients and are correlated with hepatic triglyceride. J Hepatol 53:934-940
40. Nielsen NI, Ingvartsen KL, Larsen T 2003 Diurnal variation and the effect of feed restriction on plasma and milk metabolites in TMR-fed dairy cows. J Vet Med A Physiol Pathol Clin Med 50:88-97 (Pubitemid 41749401)
41. Lundåsen T, Hunt MC, Nilsson LM, Sanyal S, Angelin B, Alexson SE, Rudling M 2007 PPARα is a key regulator of hepatic FGF21. Biochem Biophys Res Commun 360:437-440 (Pubitemid 47039157)
42. Mai K, Bobbert T, Groth C, Assmann A, Meinus S, Kraatz J, Andres J, Arafat AM, Pfeiffer AF, Möhlig M, Spranger J 2010 Physiological modulation of circulating FGF21: relevance of free fatty acids and insulin. Am J Physiol Endocrinol Metab 299:E126-E130
43. Mai K, Andres J, Biedasek K, Weicht J, Bobbert T, Sabath M, Meinus S, Reinecke F, Möhlig M, Weickert MO, Clemenz M, Pfeiffer AF, Kintscher U, Spuler S, Spranger J 2009 Free fatty acids link metabolism and regulation of the insulin-sensitizing fibroblast growth factor-21. Diabetes 58:1532-1538
44. Bergen WG, Mersmann HJ 2005 Comparative aspects of lipid metabolism: impact on contemporary research and use of animal models. J Nutr 135:2499-2502 (Pubitemid 43156585)
45. Tyynismaa H, Raivio T, Hakkarainen A, Ortega-Alonso A, Lundbom N, Kaprio J, Rissanen A, Suomalainen A, Pietiläinen KH 2011 Liver fat but not other adiposity measures influence circulating FGF21 levels in healthy young adult twins. J Clin Endocrinol Metab 96:E351-E355
46. Dushay J, Chui PC, Gopalakrishnan GS, Varela-Rey M, Crawley M, Fisher FM, Badman MK, Martinez-Chantar ML, Maratos-Flier E 2010 Increased fibroblast growth factor 21 in obesity and nonalcoholic fatty liver disease. Gastroenterology 139:456-463
47. Carriquiry M, Weber WJ, Fahrenkrug SC, Crooker BA 2009 Hepatic gene expression in multiparous Holstein cows treated with bovine somatotropin and fed n-3 fatty acids in early lactation. J Dairy Sci 92:4889-4900
48. Mraz M, Bartlova M, Lacinova Z, Michalsky D, Kasalicky M, Haluzikova D, Matoulek M, Dostalova I, Humenanska V, Haluzik M 2009 Serum concentrations and tissue expression of a novel endocrine regulator fibroblast growth factor-21 in patients with type 2 diabetes and obesity. Clin Endocrinol (Oxf) 71:369-375
49. Hojman P, Pedersen M, Nielsen AR, Krogh-Madsen R, Yfanti C, Akerstrom T, Nielsen S, Pedersen BK 2009 Fibroblast growth factor-21 is induced in human skeletal muscles by hyperinsulinemia. Diabetes 58:2797-2801
50. Ito S, Kinoshita S, Shiraishi N, Nakagawa S, Sekine S, Fujimori T, Nabeshima YI 2000 Molecular cloning and expression analyses of mouse β-klotho, which encodes a novel Klotho family protein. Mech Dev 98:115-119
51. Zhao FQ, Moseley WM, Tucker HA, Kennelly JJ 1996 Regulation of glucose transporter gene expression in mammary gland, muscle, and fat of lactating cows by administration of bovine growth hormone and bovine growth hormone-releasing factor. J Anim Sci 74:183-189 (Pubitemid 126436703)
52. Suzuki M, Uehara Y, Motomura-Matsuzaka K, Oki J, Koyama Y, Kimura M, Asada M, Komi-Kuramochi A, Oka S, Imamura T 2008 β-Klotho is required for fibroblast growth factor (FGF) 21 signaling through FGF receptor (FGFR) 1c and FGFR3c. Mol Endocrinol 22:1006-1014 (Pubitemid 351482834)
53. Fisher FM, Chui PC, Antonellis PJ, Bina HA, Kharitonenkov A, Flier JS, Maratos-Flier E 2010 Obesity is a fibroblast growth factor 21 (FGF21)-resistant state. Diabetes 59:2781-2789