Conversion of a paracrine fibroblast growth factor into an endocrine fibroblast growth factor

Journal of Biological Chemistry

Volumn 287, Issue 34, 2012, Pages 29134-29146

  Goetz, Regina ^a   Ohnishi, Mutsuko ^b   Kir, Serkan ^c   Kurosu, Hiroshi ^c   Wang, Lei ^c   Pastor, Johanne ^c   Ma, Jinghong ^a   Gai, Weiming ^a   Kuro o, Makoto ^c   Razzaque, Mohammed S ^b   Mohammadi, Moosa ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HARVARD SCHOOL OF DENTAL MEDICINE   (United States)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

C-TERMINAL TAIL; CELL SURFACES; FIBROBLAST GROWTH FACTOR; GLOBAL EPIDEMIC; HEPARAN SULFATES; LIPID METABOLISMS; METABOLIC PROCESS; NOVEL STRATEGIES; PARACRINE; PROOF OF CONCEPT; TARGET TISSUES;

BINDING ENERGY; CELL MEMBRANES; GLUCOSE; LIGANDS; METABOLISM; PHYSIOLOGY; TISSUE;

SULFUR COMPOUNDS;

FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 19; FIBROBLAST GROWTH FACTOR 23; HEPARAN SULFATE; KLOTHO CO RECEPTOR; KLOTHO PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING COMPETITION; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL SURFACE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DIMERIZATION; INTRACELLULAR SIGNALING; LIGAND BINDING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RAT; RECEPTOR AFFINITY; RECEPTOR BINDING; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION;

ANIMALS; CELL LINE, TUMOR; DIABETES MELLITUS, TYPE 2; ENDOCRINE SYSTEM; FIBROBLAST GROWTH FACTORS; HEPARITIN SULFATE; HUMANS; MICE; MICE, MUTANT STRAINS; MODELS, BIOLOGICAL; OBESITY; PARACRINE COMMUNICATION; SIGNAL TRANSDUCTION;

EID: 84865258676     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.342980     Document Type: Article

References (65)

1. Beenken, A., and Mohammadi, M. (2009) The FGF family. Biology, pathophysiology and therapy. Nat. Rev. Drug Discov. 8, 235-253
2. Itoh, N., and Ornitz, D. M. (2011) Fibroblast growth factors. From molecular evolution to roles in development, metabolism and disease. J. Biochem. 149, 121-130
3. Mohammadi, M., Olsen, S. K., and Ibrahimi, O. A. (2005) Structural basis for fibroblast growth factor receptor activation. Cytokine Growth Factor Rev. 16, 107-137
4. Itoh, N., and Ornitz, D. M. (2004) Evolution of the Fgf and Fgfr gene families. Trends Genet. 20, 563-569
5. Chellaiah, A. T., McEwen, D. G., Werner, S., Xu, J., and Ornitz, D. M. (1994) Fibroblast growth factor receptor (FGFR) 3. Alternative splicing in immunoglobulin-like domain III creates a receptor highly specific for acidic FGF/FGF-1. J. Biol. Chem. 269, 11620-11627
6. Johnson, D. E., Lu, J., Chen, H., Werner, S., and Williams, L. T. (1991) The human fibroblast growth factor receptor genes. A common structural arrangement underlies the mechanisms for generating receptor forms that differ in their third immunoglobulin domain. Mol. Cell. Biol. 11,4627-4634
7. Miki, T., Bottaro, D. P., Fleming, T. P., Smith, C. L., Burgess, W. H., Chan, A. M., and Aaronson, S. A. (1992) Determination of ligand-binding specificity by alternative splicing. Two distinct growth factor receptors encoded by a single gene. Proc. Natl. Acad. Sci. U.S.A. 89, 246-250
8. Olsen, S. K., Li, J. Y., Bromleigh, C., Eliseenkova, A. V., Ibrahimi, O. A., Lao, Z., Zhang, F., Linhardt, R. J., Joyner, A. L., and Mohammadi, M. (2006) Structural basis by which alternative splicing modulates the organizer activity of FGF8 in the brain. Genes Dev. 20, 185-198
9. Orr-Urtreger, A., Bedford, M. T., Burakova, T., Arman, E., Zimmer, Y., Yayon, A., Givol, D., and Lonai, P. (1993) Developmental localization of the splicing alternatives of fibroblast growth factor receptor-2 (FGFR2). Dev. Biol. 158, 475-486
10. Yeh, B. K., Igarashi, M., Eliseenkova, A. V., Plotnikov, A. N., Sher, I., Ron, D., Aaronson, S. A., and Mohammadi, M. (2003) Structural basis by which alternative splicing confers specificity in fibroblast growth factor receptors. Proc. Natl. Acad. Sci. U.S.A. 100, 2266-2271
11. Böttcher, R. T., and Niehrs, C. (2005) Fibroblast growth factor signaling during early vertebrate development. Endocr. Rev. 26, 63-77
12. Thisse, B., and Thisse, C. (2005) Functions and regulations of fibroblast growth factor signaling during embryonic development. Dev. Biol. 287,390-402
13. Hart, A. W., Baeza, N., Apelqvist, A., and Edlund, H. (2000) Attenuation of FGF signalling in mouse beta-cells leads to diabetes. Nature 408, 864-868
14. Jonker, J. W., Suh, J. M., Atkins, A. R., Ahmadian, M., Li, P., Whyte, J., He, M., Juguilon, H., Yin, Y. Q., Phillips, C. T., Yu, R. T., Olefsky, J. M., Henry, R. R., Downes, M., and Evans, R. M. (2012)APPARγ-FGF1 axis is required for adaptive adipose remodelling and metabolic homeostasis. Nature 485,391-394
15. Inagaki, T., Choi, M., Moschetta, A., Peng, L., Cummins, C. L., McDonald, J. G., Luo, G., Jones, S. A., Goodwin, B., Richardson, J. A., Gerard, R. D., Repa, J. J., Mangelsdorf, D. J., and Kliewer, S. A. (2005) Fibroblast growth factor 15 functions as an enterohepatic signal to regulate bile acid homeostasis. Cell Metab. 2, 217-225
16. Kir, S., Beddow, S. A., Samuel, V. T., Miller, P., Previs, S. F., Suino-Powell, K., Xu, H. E., Shulman, G. I., Kliewer, S. A., and Mangelsdorf, D. J. (2011) FGF19 as a postprandial, insulin-independent activator of hepatic protein and glycogen synthesis. Science 331, 1621-1624
17. Potthoff, M. J., Boney-Montoya, J., Choi, M., He, T., Sunny, N. E., Satapati, S., Suino-Powell, K., Xu, H. E., Gerard, R. D., Finck, B. N., Burgess, S. C., Mangelsdorf, D. J., and Kliewer, S. A. (2011) FGF15/19 regulates hepatic glucose metabolism by inhibiting the CREB-PGC-1α pathway. Cell Metab. 13, 729-738
18. Badman, M. K., Pissios, P., Kennedy, A. R., Koukos, G., Flier, J. S., and 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
19. 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 PPARα-mediated induction of fibroblast growth factor 21. Cell Metab. 5, 415-425
20. 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) FGF-21 as a novel metabolic regulator. J. Clin. Invest. 115, 1627-1635
21. Potthoff, M. J., Inagaki, T., Satapati, S., Ding, X., He, T., Goetz, R., Mohammadi, M., Finck, B. N., Mangelsdorf, D. J., Kliewer, S. A., and Burgess, S. C. (2009) FGF21 induces PGC-1α and regulates carbohydrate and fatty acid metabolism during the adaptive starvation response. Proc. Natl. Acad. Sci. U.S.A. 106, 10853-10858
22. White, K. E., Evans, W. E., O'Riordan, J. L., Speer, M. C., Econs, M. J., Lorenz-Depiereux, B., Grabowski, M., Meitinger, T., and Strom, T. M. (2000) Autosomal dominant hypophosphataemic rickets is associated with mutations in FGF23. Nat. Genet. 26, 345-348
23. Shimada, T., Kakitani, M., Yamazaki, Y., Hasegawa, H., Takeuchi, Y., Fujita, T., Fukumoto, S., Tomizuka, K., and Yamashita, T. (2004) Targeted ablation of Fgf23 demonstrates an essential physiological role of FGF23 in phosphate and vitamin D metabolism. J. Clin. Invest. 113, 561-568
24. Beenken, A., and Mohammadi, M. (2012) The structural biology of the FGF19 subfamily, in Endocrine FGFs and Klothos (Kuro-o, M., ed) pp. 1-24, Landes Bioscience, Austin, TX
25. Ago, H., Kitagawa, Y., Fujishima, A., Matsuura, Y., and Katsube, Y. (1991) Crystal structure of basic fibroblast growth factor at 1.6 A resolution. J. Biochem. 110, 360-363
26. Eriksson, A. E., Cousens, L. S., Weaver, L. H., and Matthews, B. W. (1991) Three-dimensional structure of human basic fibroblast growth factor. Proc. Natl. Acad. Sci. U.S.A. 88, 3441-3445
27. Zhang, J. D., Cousens, L. S., Barr, P. J., and Sprang, S. R. (1991) Three-dimensional structure of human basic fibroblast growth factor, a structural homolog of interleukin 1β. Proc. Natl. Acad. Sci. U.S.A. 88,3446-3450
28. Zhu, X., Komiya, H., Chirino, A., Faham, S., Fox, G. M., Arakawa, T., Hsu, B. T., and Rees, D. C. (1991) Three-dimensional structures of acidic and basic fibroblast growth factors. Science 251, 90-93
29. Goetz, R., Beenken, A., Ibrahimi, O. A., Kalinina, J., Olsen, S. K., Eliseenkova, A. V., Xu, C., Neubert, T. A., Zhang, F., Linhardt, R. J., Yu, X., White, K. E., Inagaki, T., Kliewer, S. A., Yamamoto, M., Kurosu, H., Ogawa, Y., Kuro-o, M., Lanske, B., Razzaque, M. S., and Mohammadi, M. (2007) Molecular insights into the Klotho-dependent, endocrine mode of action of fibroblast growth factor 19 subfamily members. Mol. Cell. Biol. 27,3417-3428
30. Asada, M., Shinomiya, M., Suzuki, M., Honda, E., Sugimoto, R., Ikekita, M., and Imamura, T. (2009) Glycosaminoglycan affinity of the complete fibroblast growth factor family. Biochim. Biophys. Acta 1790, 40-48
31. Schlessinger, J., Plotnikov, A. N., Ibrahimi, O. A., Eliseenkova, A. V., Yeh, B. K., Yayon, A., Linhardt, R. J., and Mohammadi, M. (2000) Crystal structure of a ternary FGF-FGFR-heparin complex reveals a dual role for heparin in FGFR binding and dimerization. Mol Cell 6, 743-750
32. Kalinina, J., Byron, S. A., Makarenkova, H. P., Olsen, S. K., Eliseenkova, A. V., Larochelle, W. J., Dhanabal, M., Blais, S., Ornitz, D. M., Day, L. A., Neubert, T. A., Pollock, P. M., and Mohammadi, M. (2009) Homodimerization controls the fibroblast growth factor 9 subfamily's receptor binding and heparan sulfate-dependent diffusion in the extracellular matrix. Mol. Cell. Biol. 29, 4663-4678
33. Makarenkova, H. P., Hoffman, M. P., Beenken, A., Eliseenkova, A. V., Meech, R., Tsau, C., Patel, V. N., Lang, R. A., and Mohammadi, M. (2009) Differential interactions of FGFs with heparan sulfate control gradient formation and branching morphogenesis. Sci. Signal. 2, ra55
34. Mohammadi, M., Olsen, S. K., and Goetz, R. (2005) A protein canyon in the FGF-FGF receptor dimer selects from an à la carte menu of heparan sulfate motifs. Curr. Opin. Struct. Biol. 15, 506-516
35. Kurosu, H., Choi, M., Ogawa, Y., Dickson, A. S., Goetz, R., Eliseenkova, A. V., Mohammadi, M., Rosenblatt, K. P., Kliewer, S. A., and Kuro-o, M. (2007) Tissue-specific expression of βKlotho and fibroblast growth factor(FGF) receptor isoforms determines metabolic activity of FGF19 and FGF21. J. Biol. Chem. 282, 26687-26695
36. Kurosu, H., Ogawa, Y., Miyoshi, M., Yamamoto, M., Nandi, A., Rosenblatt, K. P., Baum, M. G., Schiavi, S., Hu, M. C., Moe, O. W., and Kuro-o, M. (2006) Regulation of fibroblast growth factor-23 signaling by Klotho. J. Biol. Chem. 281, 6120-6123
37. Ogawa, Y., Kurosu, H., Yamamoto, M., Nandi, A., Rosenblatt, K. P., Goetz, R., Eliseenkova, A. V., Mohammadi, M., and Kuro-o, M. (2007) βKlotho isrequired for metabolic activity of fibroblast growth factor 21. Proc. Natl. Acad. Sci. U.S.A. 104, 7432-7437
38. Urakawa, I., Yamazaki, Y., Shimada, T., Iijima, K., Hasegawa, H., Okawa, K., Fujita, T., Fukumoto, S., and Yamashita, T. (2006) Klotho converts canonical FGF receptor into a specific receptor for FGF23. Nature 444,770-774
39. Ito, S., Kinoshita, S., Shiraishi, N., Nakagawa, S., Sekine, S., Fujimori, T., and Nabeshima, Y. I. (2000) Molecular cloning and expression analyses of mouse βKlotho, which encodes a novel Klotho family protein. Mech. Dev. 98, 115-119
40. Kuro-o, M., Matsumura, Y., Aizawa, H., Kawaguchi, H., Suga, T., Utsugi, T., Ohyama, Y., Kurabayashi, M., Kaname, T., Kume, E., Iwasaki, H., Iida, A., Shiraki-Iida, T., Nishikawa, S., Nagai, R., and Nabeshima, Y. I. (1997) Mutation of the mouse Klotho gene leads to a syndrome resembling ageing. Nature 390, 45-51
41. Goetz, R., Nakada, Y., Hu, M. C., Kurosu, H., Wang, L., Nakatani, T., Shi, M., Eliseenkova, A. V., Razzaque, M. S., Moe, O. W., Kuro-o, M., and Mohammadi, M. (2010) Isolated C-terminal tail of FGF23 alleviates hypophosphatemia by inhibiting FGF23-FGFR-Klotho complex formation. Proc. Natl. Acad. Sci. U.S.A. 107, 407-412
42. Micanovic, R., Raches, D. W., Dunbar, J. D., Driver, D. A., Bina, H. A., Dickinson, C. D., and Kharitonenkov, A. (2009) Different roles of N- and C-termini in the functional activity of FGF21. J. Cell. Physiol. 219,227-234
43. Wu, X., Lemon, B., Li, X., Gupte, J., Weiszmann, J., Stevens, J., Hawkins, N., Shen, W., Lindberg, R., Chen, J. L., Tian, H., and Li, Y. (2008) C-terminal tail of FGF19 determines its specificity toward Klotho co-receptors. J. Biol. Chem. 283, 33304-33309
44. Yie, J., Hecht, R., Patel, J., Stevens, J., Wang, W., Hawkins, N., Steavenson, S., Smith, S., Winters, D., Fisher, S., Cai, L., Belouski, E., Chen, C., Michaels, M. L., Li, Y. S., Lindberg, R., Wang, M., Véniant, M., and Xu, J. (2009) FGF21 N- and C-termini play different roles in receptor interaction and activation. FEBS Lett. 583, 19-24
45. Goetz, R., Ohnishi, M., Ding, X., Kurosu, H., Wang, L., Akiyoshi, J., Ma, J., Gai, W., Sidis, Y., Pitteloud, N., Kuro-O, M., Razzaque, M. S., and Mohammadi, M. (2012) Klotho coreceptors inhibit signaling by paracrine fibroblast growth factor 8 subfamily ligands. Mol. Cell. Biol. 32, 1944-1954
46. Suzuki, M., Uehara, Y., Motomura-Matsuzaka, K., Oki, J., Koyama, Y., Kimura, M., Asada, M., Komi-Kuramochi, A., Oka, S., and Imamura, T. (2008) βKlotho is required for fibroblast growth factor (FGF) 21 signalingthrough FGF receptor (FGFR) 1c and FGFR3c. Mol. Endocrinol. 22,1006-1014
47. Yu, X., Ibrahimi, O. A., Goetz, R., Zhang, F., Davis, S. I., Garringer, H. J., Linhardt, R. J., Ornitz, D. M., Mohammadi, M., and White, K. E. (2005) Analysis of the biochemical mechanisms for the endocrine actions of fibroblast growth factor-23. Endocrinology 146, 4647-4656
48. Zhang, X., Ibrahimi, O. A., Olsen, S. K., Umemori, H., Mohammadi, M., and Ornitz, D. M. (2006) Receptor specificity of the fibroblast growth factor family. The complete mammalian FGF family. J. Biol. Chem. 281,15694-15700
49. Ibrahimi, O. A., Zhang, F., Eliseenkova, A. V., Itoh, N., Linhardt, R. J., and Mohammadi, M. (2004) Biochemical analysis of pathogenic ligand-dependent FGFR2 mutations suggests distinct pathophysiological mechanisms for craniofacial and limb abnormalities. Hum. Mol. Genet. 13,2313-2324
50. Plotnikov, A. N., Hubbard, S. R., Schlessinger, J., and Mohammadi, M. (2000) Crystal structures of two FGF-FGFR complexes reveal the determinants of ligand-receptor specificity. Cell 101, 413-424
51. White, K. E., Carn, G., Lorenz-Depiereux, B., Benet-Pages, A., Strom, T. M., and Econs, M. J. (2001) Autosomal-dominant hypophosphatemic rickets (ADHR) mutations stabilize FGF-23. Kidney Int. 60, 2079-2086
52. Olsen, S. K., Garbi, M., Zampieri, N., Eliseenkova, A. V., Ornitz, D. M., Goldfarb, M., and Mohammadi, M. (2003) Fibroblast growth factor (FGF) homologous factors share structural but not functional homology with FGFs. J. Biol. Chem. 278, 34226-34236
53. Kurosu, H., Yamamoto, M., Clark, J. D., Pastor, J. V., Nandi, A., Gurnani, P., McGuinness, O. P., Chikuda, H., Yamaguchi, M., Kawaguchi, H., Shimomura, I., Takayama, Y., Herz, J., Kahn, C. R., Rosenblatt, K. P., and Kuro-o, M. (2005) Suppression of aging in mice by the hormone Klotho. Science 309, 1829-1833
54. Kato, Y., Arakawa, E., Kinoshita, S., Shirai, A., Furuya, A., Yamano, K., Nakamura, K., Iida, A., Anazawa, H., Koh, N., Iwano, A., Imura, A., Fujimori, T., Kuro-o, M., Hanai, N., Takeshige, K., and Nabeshima, Y. (2000) Establishment of the anti-Klotho monoclonal antibodies and detection of Klotho protein in kidneys. Biochem. Biophys. Res. Commun. 267, 597-602
55. Kim, I., Ahn, S. H., Inagaki, T., Choi, M., Ito, S., Guo, G. L., Kliewer, S. A., and Gonzalez, F. J. (2007) Differential regulation of bile acid homeostasis by the farnesoid X receptor in liver and intestine. J. Lipid Res. 48,2664-2672
56. Nakatani, T., Ohnishi, M., and Razzaque, M. S. (2009) Inactivation of Klotho function induces hyperphosphatemia even in presence of high serum fibroblast growth factor 23 levels in a genetically engineered hypophosphatemic (Hyp) mouse model. FASEB J. 23, 3702-3711
57. Ohnishi, M., Nakatani, T., Lanske, B., and Razzaque, M. S. (2009) Reversal of mineral ion homeostasis and soft-tissue calcification of Klotho knockout mice by deletion of vitamin D 1α-hydroxylase. Kidney Int. 75, 1166-1172
58. Ohnishi, M., Kato, S., Akiyoshi, J., Atfi, A., and Razzaque, M. S. (2011) Dietary and genetic evidence for enhancing glucose metabolism and reducing obesity by inhibiting Klotho functions. FASEB J. 25, 2031-2039
59. Russell, D. W. (2003) The enzymes, regulation, and genetics of bile acid synthesis. Annu. Rev. Biochem. 72, 137-174
60. Gattineni, J., Bates, C., Twombley, K., Dwarakanath, V., Robinson, M. L., Goetz, R., Mohammadi, M., and Baum, M. (2009) FGF23 decreases renal NaPi-2a and NaPi-2c expression and induces hypophosphatemia in vivo predominantly via FGF receptor 1. Am. J. Physiol. Renal Physiol 297,F282-F291
61. Liu, S., Vierthaler, L., Tang, W., Zhou, J., and Quarles, L. D. (2008) FGFR3 and FGFR4 do not mediate renal effects of FGF23. J. Am. Soc. Nephrol. 19,2342-2350
62. Pantoliano, M. W., Horlick, R. A., Springer, B. A., Van Dyk, D. E., Tobery, T., Wetmore, D. R., Lear, J. D., Nahapetian, A. T., Bradley, J. D., and Sisk, W. P. (1994) Multivalent ligand-receptor binding interactions in the fibroblast growth factor system produce a cooperative growth factor and heparin mechanism for receptor dimerization. Biochemistry 33, 10229-10248
63. Roghani, M., Mansukhani, A., Dell'Era, P., Bellosta, P., Basilico, C., Rifkin, D. B., and Moscatelli, D. (1994) Heparin increases the affinity of basic fibroblast growth factor for its receptor but is not required for binding. J. Biol. Chem. 269, 3976-3984
64. Onesti, S., Brick, P., and Blow, D. M. (1991) Crystal structure of a Kunitz-type trypsin inhibitor from Erythrina caffra seeds. J. Mol. Biol. 217,153-176
65. Finzel, B. C., Clancy, L. L., Holland, D. R., Muchmore, S. W., Watenpaugh, K. D., and Einspahr, H. M. (1989) Crystal structure of recombinant human interleukin-1β at 2.0 A resolution. J. Mol. Biol. 209, 779-791