Hepatic FGF21 production is increased in late pregnancy in the mouse

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 307, Issue 3, 2014, Pages

  Cui, Yingjun ^a   Giesy, Sarah L ^b   Hassan, Mahmoud ^b   Davis, Kristen ^b   Zhao, Shuhong ^b   Boisclair, Yves R ^b  

^a NORTHEAST AGRICULTURAL UNIVERSITY   (China)

^b Department of Obstetrics Gynecology   (United States)

Author keywords

Energy; Lactation; Liver; Maternal metabolism; Reproduction

Indexed keywords

FIBROBLAST GROWTH FACTOR 21; FIBROBLAST GROWTH FACTOR RECEPTOR 1; FIBROBLAST GROWTH FACTOR RECEPTOR 1C; FIBROBLAST GROWTH FACTOR RECEPTOR 2; FIBROBLAST GROWTH FACTOR RECEPTOR 2C; KLOTHO PROTEIN; KLOTHO PROTEIN BETA; UNCLASSIFIED DRUG;

ADAPTATION; ADIPOSE TISSUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; BREAST EPITHELIUM; CONTROLLED STUDY; ENERGY METABOLISM; FATTY ACID BLOOD LEVEL; FEMALE; GENE EXPRESSION; LACTATION; LIPID LIVER LEVEL; LIVER; MALE; METABOLIC PARAMETERS; MOUSE; NONHUMAN; PANCREAS; PLACENTA DEVELOPMENT; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; THIRD TRIMESTER PREGNANCY;

ENERGY; LACTATION; LIVER; MATERNAL METABOLISM; REPRODUCTION;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ENERGY METABOLISM; FEMALE; FIBROBLAST GROWTH FACTORS; LIVER; MEMBRANE PROTEINS; MICE; MICE, INBRED STRAINS; MODELS, ANIMAL; PLACENTA; PREGNANCY; PREGNANCY, ANIMAL; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 1; UP-REGULATION;

EID: 84905271294     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00554.2013     Document Type: Article

References (53)

1. Adams AC, Coskun T, Cheng CC, LSOF, Dubois SL, Kharitonenkov A. Fibroblast growth factor 21 is not required for the antidiabetic actions of the thiazoladinediones. Mol Metab 2: 205-214, 2013.
2. Adams AC, Halstead CA, Hansen BC, Irizarry AR, Martin JA, Myers SR, Reynolds VL, Smith HW, Wroblewski VJ, Kharitonenkov A. LY2405319, an Engineered FGF21 Variant, Improves the Metabolic Status of Diabetic Monkeys. PLos One 8: e65763, 2013.
3. Adams AC, Yang C, Coskun T, Cheng CC, Gimeno RE, Luo Y, Kharitonenkov A. The breadth of FGF21's metabolic actions are governed by FGFR1 in adipose tissue. Mol Metab 2: 31-37, 2012.
4. Angelin B, Larsson TE, Rudling M. Circulating fibroblast growth factors as metabolic regulators-a critical appraisal. Cell Metab 16: 693-705, 2012.
5. Badman MK, Koester A, Flier JS, Kharitonenkov A, Maratos-Flier E. Fibroblast growth factor 21-deficient mice demonstrate impaired adaptation to ketosis. Endocrinology 150: 4931-4940, 2009.
6. 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 5: 426-437, 2007.
7. Bell AW. Regulation of organic nutrient metabolism during transition from late pregnancy to early lactation. J Anim Sci 73: 2804-2819, 1995.
8. Bell AW, Bauman DE. Adaptations of glucose metabolism during pregnancy and lactation. J Mammary Gland Biol Neoplasia 2: 265-278, 1997.
9. Butte NF, Hopkinson JM, Mehta N, Moon JK, O'Brian Smith E. Adjustments in energy expenditure and substrate utilization during late pregnancy and lactation. Am J Clin Nutr 69: 299-307, 1999.
10. De Sousa-Coelho AL, Marrero PF, Haro D. Activating transcription factor 4-dependent induction of FGF21 during amino acid deprivation. Biochem J 443: 165-171, 2012.
11. Dilworth MR, Sibley CP. Review: Transport across the placenta of mice and women. Placenta 34, Suppl: S34-S39, 2013.
12. Drackley JK. ADSA Foundation Scholar Award. Biology of dairy cows during the transition period: the final frontier? J Dairy Sci 82: 2259-2273, 1999.
13. Dutchak PA, Katafuchi T, Bookout AL, Choi JH, Yu RT, Mangelsdorf DJ, Kliewer SA. Fibroblast growth factor-21 regulates PPARgamma activity and the antidiabetic actions of thiazolidinediones. Cell 148: 556-567, 2012.
14. Fon Tacer K, Bookout A, Ding X, Kurosu H, John G, Wang L, Goetz R, Mohammadi M, Kuro-o M, Mangelsdorf D, Kliewer S. Research resource: Comprehensive expression atlas of the fibroblast growth factor system in adult mouse. Mol Endocrinol 24: 2050-2114, 2010.
15. Foote MR, Giesy SL, Bernal-Santos G, Bauman DE, Boisclair YR. t10, c12-CLA decreases adiposity in peripubertal mice without doserelated detrimental effects on mammary development, inflammation sta-tus, and metabolism. Am J Physiol Regul Integr Comp Physiol 299: R1521-R1528, 2010.
16. Gaich G, Chien JY, Fu H, Glass LC, Deeg MA, Holland WL, Kharitonenkov A, Bumol T, Schilske HK, Moller DE. The effects of LY2405319, an FGF21 analog, in obese human subjects with type 2 diabetes. Cell Metab 18: 333-340, 2013.
17. Holland WL, Adams AC, Brozinick JT, Bui HH, Miyauchi Y, Kusminski CM, Bauer SM, Wade M, Singhal E, Cheng CC, Volk K, Kuo MS, Gordillo R, Kharitonenkov A, Scherer PE. An FGF21-adiponectin-ceramide axis controls energy expenditure and insulin action in mice. Cell Metab 17: 790-797, 2013.
18. Hondares E, Iglesias R, Giralt A, Gonzalez FJ, Giralt M, Mampel T, Villarroya F. Thermogenic activation induces FGF21 expression and release in brown adipose tissue. J Biol Chem 286: 12983-12990, 2011.
19. Hondares E, Rosell M, Gonzalez FJ, Giralt M, Iglesias R, Villarroya F. Hepatic FGF21 expression is induced at birth via PPARalpha in response to milk intake and contributes to thermogenic activation of neonatal brown fat. Cell Metab 11: 206-212, 2010.
20. Hu D, Cross JC. Development and function of trophoblast giant cells in the rodent placenta. Int J Dev Biol 54: 341-354, 2010.
21. Huang C, Snider F, Cross JC. Prolactin receptor is required for normal glucose homeostasis and modulation of beta-cell mass during pregnancy. Endocrinology 150: 1618-1626, 2009.
22. 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. Endocrine regulation of the fasting response by PPARalpha-mediated induction of fibroblast growth factor 21. Cell Metab 5: 415-425, 2007.
23. Izumiya Y, Bina HA, Ouchi N, Akasaki Y, Kharitonenkov A, Walsh K. FGF21 is an Akt-regulated myokine. FEBS Lett 582: 3805-3810, 2008.
24. Karnik SK, Chen H, McLean GW, Heit JJ, Gu X, Zhang AY, Fontaine M, Yen MH, Kim SK. Menin controls growth of pancreatic beta-cells in pregnant mice and promotes gestational diabetes mellitus. Science 318: 806-809, 2007.
25. 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. FGF-21/FGF-21 receptor interaction and activation is determined by betaKlotho. J Cell Physiol 215: 1-7, 2008.
26. 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. FGF-21 as a novel metabolic regulator. J Clin Invest 115: 1627-1635, 2005.
27. Kim KH, Jeong YT, Kim SH, Jung HS, Park KS, Lee HY, Lee MS. Metformin-induced inhibition of the mitochondrial respiratory chain increases FGF21 expression via ATF4 activation. Biochem Biophys Res Commun 440: 76-81, 2013.
28. Kim KH, Jeong YT, Oh H, Kim SH, Cho JM, Kim YN, Kim SS, Kim do H, Hur KY, Kim HK, Ko T, Han J, Kim HL, Kim J, Back SH, Komatsu M, Chen H, Chan DC, Konishi M, Itoh N, Choi CS, Lee MS. Autophagy deficiency leads to protection from obesity and insulin resistance by inducing Fgf21 as a mitokine. Nat Med 19: 83-92, 2013.
29. Kurosu H, Choi M, Ogawa Y, Dickson AS, Goetz R, Eliseenkova AV, Mohammadi M, Rosenblatt KP, Kliewer SA, Kuro-o M. Tissuespecific expression of betaKlotho and fibroblast growth factor (FGF) receptor isoforms determines metabolic activity of FGF19 and FGF21. J Biol Chem 282: 26687-26695, 2007.
30. Lin Z, Tian H, Lam KS, Lin S, Hoo RC, Konishi M, Itoh N, Wang Y, Bornstein SR, Xu A, Li X. Adiponectin mediates the metabolic effects of FGF21 on glucose homeostasis and insulin sensitivity in mice. Cell Metab 17: 779-789, 2013.
31. Long YC, Kharitonenkov A. Hormone-like fibroblast growth factors and metabolic regulation. Biochim Biophys Acta 1812: 791-795, 2011.
32. Lundasen T, Hunt MC, Nilsson LM, Sanyal S, Angelin B, Alexson SE, Rudling M. PPARalpha is a key regulator of hepatic FGF21. Biochem Biophys Res Commun 360: 437-440, 2007.
33. Makarova EN, Yakovleva TV, Shevchenko AY, Bazhan NM. Pregnancy and lactation have anti-obesity and anti-diabetic effects in A(y)/a mice. Acta Physiol (Oxf) 198: 169-177, 2010.
34. Nishimura T, Nakatake Y, Konishi M, Itoh N. Identification of a novel FGF, FGF-21, preferentially expressed in the liver. Biochim Biophys Acta 1492: 203-206, 2000.
35. Oftedal OT. Milk composition, milk yield and energy output at peak lactation: a comparative review. Symp Zool Soc Lond 51: 33-85, 1984.
36. Potthoff MJ, Kliewer SA, Mangelsdorf DJ. Endocrine fibroblast growth factors 15/19 and 21: from feast to famine. Genes Dev 26: 312-324, 2012.
37. Prentice AM, Prentice A. Energy costs of lactation. Ann Rev Nutr 8: 63-79, 1988.
38. Rudolph MC, Wellberg EA, Anderson SM. Adipose-depleted mammary epithelial cells and organoids. J Mammary Gland Biol Neoplasia 14: 381-386, 2009.
39. Schaap FG, Kremer AE, Lamers WH, Jansen PL, Gaemers IC. Fibroblast growth factor 21 is induced by endoplasmic reticulum stress. Biochimie 95: 692-699, 2013.
40. Schoenberg KM, Giesy SL, Harvatine KJ, Waldron MR, Cheng C, Kharitonenkov A, Boisclair YR. Plasma FGF21 is elevated by the intense lipid mobilization of lactation. Endocrinology 152: 4652-4661, 2011.
41. Silva-del-Rio N, Fricke PM, and Grummer RR. Effects of twin pregnancy and dry period feeding strategy on milk production, energy balance, and metabolic profiles in dairy cows. J Anim Sci 88: 1048-1060, 2010.
42. Speakman JR. The physiological costs of reproduction in small mammals. Philos Trans R Soc Lond B Biol Sci 363: 375-398, 2008.
43. Stein S, Stepan H, Kratzsch J, Verlohren M, Verlohren HJ, Drynda K, Lossner U, Bluher M, Stumvoll M, Fasshauer M. Serum fibroblast growth factor 21 levels in gestational diabetes mellitus in relation to insulin resistance and dyslipidemia. Metabolism 59: 33-37, 2010.
44. Stepan H, Kley K, Hindricks J, Kralisch S, Jank A, Schaarschmidt W, Schrey S, Ebert T, Lossner U, Kratzsch J, Bluher M, Stumvoll M, Richter J, Fasshauer M. Serum levels of the adipokine fibroblast growth factor-21 are increased in preeclampsia. Cytokine 62: 322-326, 2013.
45. Tan BK, Sivakumar K, Bari MF, Vatish M, Randeva HS. Lower cerebrospinal fluid/plasma fibroblast growth factor 21 (FGF21) ratios and placental FGF21 production in gestational diabetes. PLos One 8: e65254, 2013.
46. Trayhurn P. Thermogenesis and the energetics of pregnancy and lactation. Can J Physiol Pharmacol 67: 370-375, 1989.
47. Tyynismaa H, Raivio T, Hakkarainen A, Ortega-Alonso A, Lundbom N, Kaprio J, Rissanen A, Suomalainen A, Pietilainen KH. Liver fat but not other adiposity measures influence circulating FGF21 levels in healthy young adult twins. J Clin Endocrinol Metab 96: E351-E355, 2011.
48. Wente W, Efanov AM, Brenner M, Kharitonenkov A, Koster A, Sandusky GE, Sewing S, Treinies I, Zitzer H, Gromada J. 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 55: 2470-2478, 2006.
49. Xu J, Lloyd DJ, Hale C, Stanislaus S, Chen M, Sivits G, Vonderfecht S, Hecht R, Li YS, Lindberg RA, Chen JL, Jung DY, Zhang Z, Ko HJ, Kim JK, Veniant MM. Fibroblast growth factor 21 reverses hepatic steatosis, increases energy expenditure, and improves insulin sensitivity in diet-induced obese mice. Diabetes 58: 250-259, 2009.
50. Yan H, Xia M, Chang X, Xu Q, Bian H, Zeng M, Rao S, Yao X, Tu Y, Jia W, Gao X. Circulating fibroblast growth factor 21 levels are closely associated with hepatic fat content: a cross-sectional study. PLos One 6: e24895, 2011.
51. Yu J, Zhao L, Wang A, Eleswarapu S, Ge X, Chen D, Jiang H. Growth hormone stimulates transcription of the fibroblast growth factor 21 gene in the liver through the signal transducer and activator of transcription 5. Endocrinology 153: 750-758, 2012.
52. Zhang J, Li Y. Fibroblast growth factor 21, the endocrine FGF pathway and novel treatments for metabolic syndrome. Drug Discov Today 2013.
53. Zhang X, Yeung DC, Karpisek M, Stejskal D, Zhou ZG, Liu F, Wong RL, Chow WS, Tso AW, Lam KS, Xu A. Serum FGF21 levels are increased in obesity and are independently associated with the metabolic syndrome in humans. Diabetes 57: 1246-1253, 2008.