Increased expression of fibroblast growth factor 21 (FGF21) during chronic undernutrition causes growth hormone insensitivity in chondrocytes by inducing leptin receptor overlapping transcript (LEPROT) and leptin receptor overlapping transcript-like 1 (LEPROTL1) expression

Journal of Biological Chemistry

Volumn 288, Issue 38, 2013, Pages 27375-27383

  Wu, Shufang ^a,b   Grunwald, Tal ^a   Kharitonenkov, Alexei ^c   Dam, Julie ^d,e,f   Jockers, Ralf ^d,e,f   De Luca, Francesco ^a  

^a DREXEL UNIVERSITY   (United States)

^b XI'AN JIAOTONG UNIVERSITY   (China)

^c ELI LILLY AND COMPANY   (United States)

^d INSTITUT COCHIN   (France)

^e CNRS   (France)

^f UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CALORIE RESTRICTION; CELL SURFACE EXPRESSION; FIBROBLAST GROWTH FACTOR; FOOD RESTRICTIONS; GROWTH HORMONES; INTRACELLULAR PROTEINS; LEPTIN RECEPTORS; OVER-EXPRESSION;

COLLAGEN; HORMONES; MAMMALS;

BODY FLUIDS;

COLLAGEN TYPE 10; FIBROBLAST GROWTH FACTOR 21; GROWTH HORMONE; GROWTH HORMONE RECEPTOR; LEPTIN RECEPTOR OVERLAPPING TRANSCRIPT LIKE 1 PROTEIN; LEPTIN RECEPTOR OVERLAPPING TRANSCRIPT PROTEIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 3; RECOMBINANT CYTOKINE; RECOMBINANT FIBROBLAST GROWTH FACTOR 21; SMALL INTERFERING RNA; THYMIDINE; TRITIUM; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARTILAGE CELL; CELL STIMULATION; CELL SURFACE; CONTROLLED STUDY; DIET RESTRICTION; EMBRYO; GENE EXPRESSION; GENETIC TRANSFECTION; GROWTH PLATE; HORMONE BINDING; HORMONE INHIBITION; HORMONE RESISTANCE; KNOCKOUT MOUSE; LIVER PARENCHYMA; MALNUTRITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN TRANSPORT; TIBIA; WILD TYPE;

CHONDROCYTES; CHONDROGENESIS; FIBROBLAST GROWTH FACTOR (FGF); GROWTH HORMONE; GROWTH PLATE; NUTRITION;

ANIMALS; CARRIER PROTEINS; CELLS, CULTURED; CHONDROCYTES; CHRONIC DISEASE; FIBROBLAST GROWTH FACTORS; GENE EXPRESSION REGULATION; GROWTH HORMONE; HUMANS; INSULIN-LIKE GROWTH FACTOR I; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALNUTRITION; MICE; MICE, KNOCKOUT; MITOGEN-ACTIVATED PROTEIN KINASE 3; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 1; RNA, MESSENGER;

EID: 84884580553     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.462218     Document Type: Article

References (25)

1. Nishimura, T., Nakatake, Y., Konishi, M., and Itoh, N. (2000) Identification of a novel FGF. FGF21, preferentially expressed in the liver. Biochim. Biophys. Acta 1492, 203-206
2. Kharitonenkov, A., Shiyanova, T. L., Koester, A., Ford, A. M., Micanovic, R., Galbreath, E. J., Sandusky, G. E., Hammond, L. J., Moyers, J. S., Owens, R. A., Gromada, J., Brozinick, J. T., Hawkins, E. D., Wroblewski, V. J., Li, D. S., Mehrbod, F., Jaskunas, S. R., and Shanafelt, A. B. (2005) FGF21 as a novel metabolic regulator. J. Clin. Invest. 115, 1627-1635
3. Inagaki, T., Dutchak, P., Zhao, G., Ding, X., Gautron, L., Parameswara, V., Li, Y., Goetz, R., Mohammadi, M., Esser, V., Elmquist, J. K., Gerard, R. D., Burgess, S. C., Hammer, R. E., Mangelsdorf, D. J., and Kliewer, S. A. (2007) Endocrine regulation of the fasting response by PPARγ;-mediated induction of fibroblast growth factor 21. Cell Metab. 5, 415-425
4. Gälman, C., Lundåsen, T., Kharitonenkov, A., Bina, H. A., Eriksson, M., Hafström, I., Dahlin, M., Amark, P., Angelin, B., and Rudling, M. (2008) The circulating metabolic regulator FGF21 is induced by prolonged fasting and PPARγ; activation in man. Cell Metab. 8, 169-174
5. Reitman, M. L. (2007) FGF21. A missing link in the biology of fasting. Cell Metab. 5, 405-407
6. Inagaki, T., Lin, V. Y., Goetz, R., Mohammadi, M., Mangelsdorf, D. J., and Kliewer, S. A. (2008) Inhibition of growth hormone signaling by the fastinginduced hormone FGF21. Cell Metab. 8, 77-83
7. Tannenbaum, G. S., Rorstad, O., and Brazeau, P. (1979) Effects of prolonged food deprivation on the ultradian growth hormone rhythm and immunoreactive somatostatin tissue levels in the rats. Endocrinology 104, 1733-1738
8. Maes, M., Underwood, L. E., and Ketelslegers, J. M. (1983) Plasma somatomedin-C in fasted and refed rats. Close relationship with changes in somatogenic but not lactogenic binding sites. J. Endocrinol. 97, 243-252
9. Straus, D. S., and Takemoto, C. D. (1990) Effects of fasting on insulin-like growth factor-1 and growth hormone receptor mRNA levels and IGF-1 gene transcription in rat liver. Mol. Endocrinol. 4, 91-100
10. Bornfeldt, K. E., Arnqvist, H. J., Enberg, B., Mathews, L. S., and Norstedt, G. (1989) Regulation of insulin-like growth factor-1 and growth hormone receptor gene expression by diabetes and nutritional states in rat tissues. J. Endocrinol. 122, 651-656
11. Counts, D. R., Gwirtsman, H., Carlsson, L. M., Lesem, M., and Cutler, G. B. (1992) The effect of anorexia nervosa and refeeding on growth hormonebinding protein, the insulin-like growth factors (IGFs), and the IGF-binding proteins. J. Clin. Endocrinol. Metab. 75, 762-767
12. Ho, K. Y., Veldhuis, J. D., Johnson, M. L., Furlanetto, R., Evans, W. S., Alberti, K. G., and Thorner, M. O. (1988) Fasting enhances growth hormone secretion and amplifies the complex rhythms of growth hormone secretion in man. J. Clin. Invest. 81, 968-975
13. Bang, P., Brismar, K., Rosenfeld, R. G., and Hall, K. (1994) Fasting affects serum insulin-like growth factors (IGFs) and IGF-binding proteins differently in patients with non-insulin-dependent diabetes mellitus vs. healthy nonobese and obese subjects. J. Clin. Endocrinol. Metab. 78, 960-967
14. Breier, B. H., Bass, J. J., Butler, J. H., and Gluckman, P. D. (1986) The somatotrophic axis in young steers. Influence of nutritional status on pulsatile release of growth hormone and circulating concentrations of insulinlike growth factor-1. J. Endocrinol. 111, 209-215
15. Buonomo, F. C., and Baile, C. A. (1991) Influence of nutrition deprivation on insulin-like growth factor-1, somatotropin, and metabolic hormones in swine. J. Anim. Sci. 69, 755-760
16. Heinrichs, C., Colli, M., Yanovski, J. A., Laue, L., Gerstl, N. A., Kramer, A. D., Uyeda, J. A., and Baron, J. (1997) Effects of fasting on the growth plate. Systemic and local mechanisms. Endocrinology 138, 5359-5365
17. Kubicky, R. A., Wu, S., Kharitonenkov, A., and De Luca, F. (2012) Role of Fibroblast Growth Factor 21 (FGF21) in undernutrition-related attenuation of growth in mice. Endocrinology 153, 2287-2295
18. Wu, S., Levenson, A., Kharitonenkov, A., and De Luca, F. (2012) Fibroblast growth factor 21 (FGF21) inhibits chondrocyte function and growth hormone (GH) action directly at the growth plate. J. Biol. Chem. 287, 26060-26067
19. Touvier, T., Conte-Auriol, F., Briand, O., Cudejko, C., Paumelle, R., Caron, S., Baugé, E., Rouillé, Y., Salles, J. P., Staels, B., and Bailleul, B. (2009) LEPROT and LEPROTL1 cooperatively decrease hepatic growth hormone action in mice. J. Clin. Invest. 119, 3830-3838
20. Séron, K., Couturier, C., Belouzard, S., Bacart, J., Monté, D., Corset, L., Bocquet, O., Dam, J., Vauthier, V., Lecoeur, C., Bailleul, B., Hoflack, B., Froguel, P., Jockers, R., and Rouillé, Y. (2011) Endospanins regulate a postinternalization step of the leptin receptor endocytic pathway. J. Biol. Chem. 286, 17968-17981
21. Leung, K. C., Doyle, N., Ballesteros, M., Waters, M. J., and Ho, K. K. (2000) Insulin regulation of human hepatic growth hormone receptors. Divergent effects of biosynthesis and surface translocation. J. Clin. Endocrinol. Metab. 85, 4712-4720
22. Couturier, C., Sarkis, C., Séron, K., Belouzard, S., Chen, P., Lenain, A., Corset, L., Dam, J., Vauthier, V., Dubart, A., Mallet, J., Froguel, P., Rouillé, Y., and Jockers, R. (2007) Silencing of OB-RGRP in mouse hypothalamic arcuate nucleus increases leptin receptor signaling and prevents diet-induced obesity. Proc. Natl. Acad. Sci. U. S. A. 104, 19476-19481
23. Adams A. C., and Kharitonenkov, A. (2012) FGF21. The center of a transcriptional nexus in metabolic regulation. Curr. Diabetes Rev. 8, 285-293
24. Huang, Y., Ying, K., Xie, Y., Zhou, Z., Wang, W., Tang, R., Zhao, W., Zhao, S., Wu, H., Gu, S., and Mao, Y. (2001) Cloning and characterization of a novel human leptin receptor overlapping transcript-like 1 gene (LEPROTL1). Biochim. Biophys. Acta 1517, 327-331
25. Belgareh-Touzé, N., Avaro, S., Rouillé, Y., Hoflack, B., and Haguenauer-Tsapis, R. (2002) Yeast Vps55p, a functional homolog of human obesity receptor gene-related protein, is involved in late endosome to vacuole trafficking. Mol. Biol. Cell 13, 1694-1708