Membrane and integrative nuclear fibroblastic growth factor receptor (FGFR) regulation of FGF-23

Journal of Biological Chemistry

Volumn 290, Issue 16, 2015, Pages 10447-10459

  Han, Xiaobin ^a   Xiao, Zhousheng ^a   Quarles, L Darryl ^a  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANES; CELL SIGNALING; GENES; MOLECULAR WEIGHT; TRANSCRIPTION;

CAMP-RESPONSE ELEMENT-BINDING PROTEINS; CAMP-RESPONSE ELEMENTS; GENE TRANSCRIPTIONS; GROWTH FACTOR RECEPTORS; HIGH MOLECULAR WEIGHT; LOW MOLECULAR WEIGHT; PATHOLOGICAL CONDITIONS; PROMOTER ACTIVITIES;

BINDING SITES;

CALCINEURIN; CIS ACTING ELEMENT; CYCLIC AMP; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; FIBROBLAST GROWTH FACTOR 23; FIBROBLAST GROWTH FACTOR RECEPTOR; FIBROBLAST GROWTH FACTOR RECEPTOR 1; FIBROBLAST GROWTH FACTOR RECEPTOR 2; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHOLIPASE C GAMMA; TRANSCRIPTION FACTOR ETS 1; TRANSCRIPTION FACTOR NFAT; CREB1 PROTEIN, HUMAN; ETS1 PROTEIN, HUMAN; FGFR1 PROTEIN, HUMAN; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 2; ISOPROTEIN; PROTEIN BINDING;

ANIMAL CELL; ARTICLE; BINDING SITE; CELL STIMULATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; MC3T3 E1 CELL LINE; MOLECULAR WEIGHT; MOUSE; NONHUMAN; OSTEOBLAST; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; RECEPTOR UPREGULATION; SAOS 2 CELL LINE; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; CELL DIFFERENTIATION; CELL LINE; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM;

CALCINEURIN; CELL DIFFERENTIATION; CELL LINE; CYCLIC AMP; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTORS; GENE EXPRESSION REGULATION; HUMANS; MITOGEN-ACTIVATED PROTEIN KINASES; MOLECULAR WEIGHT; NFATC TRANSCRIPTION FACTORS; OSTEOBLASTS; PHOSPHOLIPASE C GAMMA; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN ISOFORMS; PROTO-ONCOGENE PROTEIN C-ETS-1; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 1; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

EID: 84927949848     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.609230     Document Type: Article

References (63)

1. Quarles, L. D. (2012) Skeletal secretion of FGF-23 regulates phosphate and vitamin D metabolism. Nat. Rev. Endocrinol. 8, 276-286
2. Liu, S., Zhou, J., Tang, W., Jiang, X., Rowe, D. W., and Quarles, L. D. (2006) Pathogenic role of Fgf23 in Hyp mice. Am. J. Physiol. Endocrinol. Metab. 291, E38-E49
3. 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
4. Shimada, T., Mizutani, S., Muto, T., Yoneya, T., Hino, R., Takeda, S., Takeuchi, Y., Fujita, T., Fukumoto, S., and Yamashita, T. (2001) Cloning and characterization of FGF23 as a causative factor of tumor-induced osteomalacia. Proc. Natl. Acad. Sci. U.S.A. 98, 6500-6505
5. 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
6. Shimada, T., Yamazaki, Y., Takahashi, M., Hasegawa, H., Urakawa, I., Oshima, T., Ono, K., Kakitani, M., Tomizuka, K., Fujita, T., Fukumoto, S., and Yamashita, T. (2005) Vitamin D receptor-independent FGF23 actions in regulating phosphate and vitamin D metabolism. Am. J. Physiol. Renal Physiol. 289, F1088-1095
7. Tomiyama, K., Maeda, R., Urakawa, I., Yamazaki, Y., Tanaka, T., Ito, S., Nabeshima, Y., Tomita, T., Odori, S., Hosoda, K., Nakao, K., and Imura, A. (2010) Relevant use of Klotho in FGF19 subfamily signaling system in vivo. Proc. Natl. Acad. Sci. U.S.A. 107, 1666-1671
8. Beckman, M. J., Tadikonda, P., Werner, E., Prahl, J., Yamada, S., and DeLuca, H. F. (1996) Human 25-hydroxyvitamin D3-24-hydroxylase, a multicatalytic enzyme. Biochemistry 35, 8465-8472
9. Hoenderop, J. G., Chon, H., Gkika, D., Bluyssen, H. A., Holstege, F. C., St-Arnaud, R., Braam, B., and Bindels, R. J. (2004) Regulation of gene expression by dietary Ca2+ in kidneys of 25-hydroxyvitamin D3-1 α-hydroxylase knockout mice. Kidney Int. 65, 531-539
10. Martin, A., Liu, S., David, V., Li, H., Karydis, A., Feng, J. Q., and Quarles, L. D. (2011) Bone proteins PHEX and DMP1 regulate fibroblastic growth factor Fgf23 expression in osteocytes through a common pathway involving FGF receptor (FGFR) signaling. FASEB J. 25, 2551-2562
11. David, V., Dai, B., Martin, A., Huang, J., Han, X., and Quarles, L. D. (2013) Calcium regulates FGF-23 expression in bone. Endocrinology 154, 4469-4482
12. Liu, S., Tang, W., Zhou, J., Stubbs, J. R., Luo, Q., Pi, M., and Quarles, L. D. (2006) Fibroblast growth factor 23 is a counter-regulatory phosphaturic hormone for vitamin D. J. Am. Soc. Nephrol. 17, 1305-1315
13. Kolek, O. I., Hines, E. R., Jones, M. D., LeSueur, L. K., Lipko, M. A., Kiela, P. R., Collins, J. F., Haussler, M. R., and Ghishan, F. K. (2005) 1α,25-Dihydroxyvitamin D3 upregulates FGF23 gene expression in bone: the final link in a renal-gastrointestinal-skeletal axis that controls phosphate transport. Am. J. Physiol. Gastrointest. Liver Physiol. 289, G1036-1042
14. Brown, W. W., Jüppner, H., Langman, C. B., Price, H., Farrow, E. G., White, K. E., and McCormick, K. L. (2009) Hypophosphatemia with elevations in serum fibroblast growth factor 23 in a child with Jansen's metaphyseal chondrodysplasia. J. Clin. Endocrinol. Metab. 94, 17-20
15. Kawata, T., Imanishi, Y., Kobayashi, K., Miki, T., Arnold, A., Inaba, M., and Nishizawa, Y. (2007) Parathyroid hormone regulates fibroblast growth factor-23 in a mouse model of primary hyperparathyroidism. J. Am. Soc. Nephrol. 18, 2683-2688
16. Lavi-Moshayoff, V., Wasserman, G., Meir, T., Silver, J., and Naveh-Many, T. (2010) PTH increases FGF23 gene expression and mediates the high-FGF23 levels of experimental kidney failure: a bone parathyroid feedback loop. Am. J. Physiol. Renal Physiol. 299, F882-889
17. Sato, T., Tominaga, Y., Ueki, T., Goto, N., Matsuoka, S., Katayama, A., Haba, T., Uchida, K., Nakanishi, S., Kazama, J. J., Gejyo, F., Yamashita, T., and Fukagawa, M. (2004) Total parathyroidectomy reduces elevated circulating fibroblast growth factor 23 in advanced secondary hyperparathyroidism. Am. J. Kidney Dis. 44, 481-487
18. 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
19. 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
20. Li, S. A., Watanabe, M., Yamada, H., Nagai, A., Kinuta, M., and Takei, K. (2004) Immunohistochemical localization of Klotho protein in brain, kidney, and reproductive organs of mice. Cell Struct. Funct. 29, 91-99
21. Samadfam, R., Richard, C., Nguyen-Yamamoto, L., Bolivar, I., and Goltzman, D. (2009) Bone formation regulates circulating concentrations of fibroblast growth factor 23. Endocrinology 150, 4835-4845
22. Ben-Dov, I. Z., Galitzer, H., Lavi-Moshayoff, V., Goetz, R., Kuro-o, M., Mohammadi, M., Sirkis, R., Naveh-Many, T., and Silver, J. (2007) The parathyroid is a target organ for FGF23 in rats. J. Clin. Invest. 117, 4003-4008
23. Martin, A., David, V., and Quarles, L. D. (2012) Regulation and Function of the FGF23/Klotho Endocrine Pathways. Physiol. Rev. 92, 131-155
24. White, K. E., Cabral, J. M., Davis, S. I., Fishburn, T., Evans, W. E., Ichikawa, S., Fields, J., Yu, X., Shaw, N. J., McLellan, N. J., McKeown, C., Fitzpatrick, D., Yu, K., Ornitz, D. M., and Econs, M. J. (2005) Mutations that cause osteoglophonic dysplasia define novel roles for FGFR1 in bone elongation. Am. J. Hum. Genet. 76, 361-367
25. Stevens, D. A., Harvey, C. B., Scott, A. J., O'Shea, P. J., Barnard, J. C., Williams, A. J., Brady, G., Samarut, J., Chassande, O., and Williams, G. R. (2003) Thyroid hormone activates fibroblast growth factor receptor-1 in bone. Mol. Endocrinol. 17, 1751-1766
26. Xiao, L., Naganawa, T., Lorenzo, J., Carpenter, T. O., Coffin, J. D., and Hurley, M. M. (2010) Nuclear isoforms of fibroblast growth factor 2 are novel inducers of hypophosphatemia via modulation of FGF23 and KLOTHO. J. Biol. Chem. 285, 2834-2846
27. Xiao, L., Esliger, A., and Hurley, M. M. (2013) Nuclear fibroblast growth factor 2 (FGF2) isoforms inhibit bone marrow stromal cell mineralization through FGF23/FGFR/MAPK in vitro. J. Bone Miner. Res. 28, 35-45
28. Liu, S., Tang, W., Fang, J., Ren, J., Li, H., Xiao, Z., and Quarles, L. D. (2009) Novel regulators of Fgf23 expression and mineralization in Hyp bone. Mol. Endocrinol. 23, 1505-1518
29. Wöhrle, S., Henninger, C., Bonny, O., Thuery, A., Beluch, N., Hynes, N. E., Guagnano, V., Sellers, W. R., Hofmann, F., Kneissel, M., and Graus Porta, D. (2013) Pharmacological inhibition of fibroblast growth factor (FGF) receptor signaling ameliorates FGF23-mediated hypophosphatemic rickets. J. Bone Miner. Res. 28, 899-911
30. Wöhrle, S., Bonny, O., Beluch, N., Gaulis, S., Stamm, C., Scheibler, M., Müller, M., Kinzel, B., Thuery, A., Brueggen, J., Hynes, N. E., Sellers, W. R., Hofmann, F., and Graus-Porta, D. (2011) FGF receptors control vitamin D and phosphate homeostasis by mediating renal FGF-23 signaling and regulating FGF-23 expression in bone. J. Bone Miner. Res. 26, 2486-2497
31. Wu, A. L., Feng, B., Chen, M. Z., Kolumam, G., Zavala-Solorio, J., Wyatt, S. K., Gandham, V. D., Carano, R. A., and Sonoda, J. (2013) Antibody-mediated activation of FGFR1 induces FGF23 production and hypophosphatemia. PloS One 8, e57322
32. Xiao, Z., Huang, J., Cao, L., Liang, Y., Han, X., and Quarles, L. D. (2014) Osteocyte-specific deletion of Fgfr1 suppresses FGF23. PloS One 9, e104154
33. Delrieu, I. (2000) The high molecular weight isoforms of basic fibroblast growth factor (FGF-2): an insight into an intracrine mechanism. FEBS Lett. 468, 6-10
34. Degnin, C. R., Laederich, M. B., and Horton, W. A. (2010) FGFs in endochondral skeletal development. J. Cell. Biochem. 110, 1046-1057
35. Eswarakumar, V. P., Lax, I., and Schlessinger, J. (2005) Cellular signaling by fibroblast growth factor receptors. Cytokine Growth Factor Rev. 16, 139-149
36. Stachowiak, M. K., Fang, X., Myers, J. M., Dunham, S. M., Berezney, R., Maher, P. A., and Stachowiak, E. K. (2003) Integrative nuclear FGFR1 signaling (INFS) as a part of a universal "feed-forward-and-gate" signaling module that controls cell growth and differentiation. J. Cell. Biochem. 90, 662-691
37. Itoh, N., and Ornitz, D. M. (2004) Evolution of the Fgf and Fgfr gene families. Trends Genet. 20, 563-569
38. Quarles, L. D., Yohay, D. A., Lever, L. W., Caton, R., and Wenstrup, R. J. (1992) Distinct proliferative and differentiated stages of murine MC3T3-E1 cells in culture: an in vitro model of osteoblast development. J. Bone Miner. Res. 7, 683-692
39. Shalhoub, V., Ward, S. C., Sun, B., Stevens, J., Renshaw, L., Hawkins, N., and Richards, W. G. (2011) Fibroblast growth factor 23 (FGF23) and α-klotho stimulate osteoblastic MC3T3.E1 cell proliferation and inhibit mineralization. Calcif. Tissue Int. 89, 140-150
40. Gee, K., Angel, J. B., Mishra, S., Blahoianu, M. A., and Kumar, A. (2007) IL-10 regulation by HIV-Tat in primary human monocytic cells: involvement of calmodulin/calmodulin-dependent protein kinase-activated p38 MAPK and Sp-1 and CREB-1 transcription factors. J. Immunol. 178, 798-807
41. Miraoui, H., and Marie, P. J. (2010) Fibroblast growth factor receptor signaling crosstalk in skeletogenesis. Sci. Signal. 3, re9
42. Crabtree, G. R., and Olson, E. N. (2002) NFAT signaling: choreographing the social lives of cells. Cell 109, S67-S79
43. Wasylyk, B., Hagman, J., and Gutierrez-Hartmann, A. (1998) Ets transcription factors: nuclear effectors of the Ras-MAP-kinase signaling pathway. Trends Biochem. Sci. 23, 213-216
44. Saini, R. K., Kaneko, I., Jurutka, P. W., Forster, R., Hsieh, A., Hsieh, J. C., Haussler, M. R., and Whitfield, G. K. (2013) 1,25-Dihydroxyvitamin D3regulation of fibroblast growth factor-23 expression in bone cells: evidence for primary and secondary mechanisms modulated by leptin and interleukin-6. Calcif. Tissue Int. 92, 339-353
45. Peng, H., Myers, J., Fang, X., Stachowiak, E. K., Maher, P. A., Martins, G. G., Popescu, G., Berezney, R., and Stachowiak, M. K. (2002) Integrative nuclear FGFR1 signaling (INFS) pathway mediates activation of the tyrosine hydroxylase gene by angiotensin II, depolarization and protein kinase C. J. Neurochem. 81, 506-524
46. Dunham-Ems, S. M., Lee, Y. W., Stachowiak, E. K., Pudavar, H., Claus, P., Prasad, P. N., and Stachowiak, M. K. (2009) Fibroblast growth factor receptor-1 (FGFR1) nuclear dynamics reveal a novel mechanism in transcription control. Mol. Biol. Cell 20, 2401-2412
47. Stachowiak, M. K., Birkaya, B., Aletta, J. M., Narla, S. T., Benson, C. A., Decker, B., and Stachowiak, E. K. (2015) "Nuclear FGF receptor-1 and CREB binding protein: an integrative signaling module." J. Cell. Physiol. 230, 989-1002
48. Homer-Bouthiette, C., Doetschman, T., Xiao, L., and Hurley, M. M. (2014) Knockout of nuclear high molecular weight FGF2 isoforms in mice modulates bone and phosphate homeostasis. J. Biol. Chem. 289, 36303-36314
49. Marie, P. J. (2012) Fibroblast growth factor signaling controlling bone formation: an update. Gene 498, 1-4
50. Du, X., Xie, Y., Xian, C. J., and Chen, L. (2012) Role of FGFs/FGFRs in skeletal development and bone regeneration. J. Cell. Physiol. 227, 3731-3743
51. Ornitz, D. M., and Marie, P. J. (2002) FGF signaling pathways in endochondral and intramembranous bone development and human genetic disease. Genes Dev. 16, 1446-1465
52. Wesseling-Perry, K., Pereira, R. C., Tsai, E., Ettenger, R., Jüppner, H., and Salusky, I. B. (2013) FGF23 and mineral metabolism in the early post-renal transplantation period. Pediat. Nephrol. 28, 2207-2215
53. Meir, T., Durlacher, K., Pan, Z., Amir, G., Richards, W. G., Silver, J., and Naveh-Many, T. (2014) Parathyroid hormone activates the orphan nuclear receptor Nurr1 to induce FGF23 transcription. Kidney Int. 86, 1106-1115
54. Baron, O., Förthmann, B., Lee, Y. W., Terranova, C., Ratzka, A., Stachowiak, E. K., Grothe, C., Claus, P., and Stachowiak, M. K. (2012) Cooperation of nuclear fibroblast growth factor receptor 1 and Nurr1 offers new interactive mechanism in postmitotic development of mesencephalic dopaminergic neurons. J. Biol. Chem. 287, 19827-19840
55. Nauman, E. A., Sakata, T., Keaveny, T. M., Halloran, B. P., and Bikle, D. D. (2003) bFGF administration lowers the phosphate threshold for mineralization in bone marrow stromal cells. Calcif. Tissue Int. 73, 147-152
56. Liang, H., Pun, S., and Wronski, T. J. (1999) Bone anabolic effects of basic fibroblast growth factor in ovariectomized rats. Endocrinology 140, 5780-5788
57. Munoz Mendoza, J., Isakova, T., Ricardo, A. C., Xie, H., Navaneethan, S. D., Anderson, A. H., Bazzano, L. A., Xie, D., Kretzler, M., Nessel, L., Hamm, L. L., Negrea, L., Leonard, M. B., Raj, D., Wolf, M., and Chronic Renal Insufficiency, C. (2012) Fibroblast growth factor 23 and inflammation in CKD. Clin. J. Am. Soc. Nephrol. 7, 1155-1162
58. Avitan-Hersh, E., Tatur, S., Indelman, M., Gepstein, V., Shreter, R., Hershkovitz, D., Brick, R., Bergman, R., and Tiosano, D. (2014) Postzygotic HRAS mutation causing both keratinocytic epidermal nevus and thymoma and associated with bone dysplasia and hypophosphatemia due to elevated FGF23. J. Clin. Endocrinol. Metab. 99, E132-E136
59. Farrow, E. G., Yu, X., Summers, L. J., Davis, S. I., Fleet, J. C., Allen, M. R., Robling, A. G., Stayrook, K. R., Jideonwo, V., Magers, M. J., Garringer, H. J., Vidal, R., Chan, R. J., Goodwin, C. B., Hui, S. L., Peacock, M., and White, K. E. (2011) Iron deficiency drives an autosomal dominant hypophosphatemic rickets (ADHR) phenotype in fibroblast growth factor-23 (Fgf23) knock-in mice. Proc. Natl. Acad. Sci. U.S.A. 108, E1146-E1155
60. Valtink, M., Knels, L., Stanke, N., Engelmann, K., Funk, R. H., and Lindemann, D. (2012) Overexpression of human HMW FGF-2 but not LMW FGF-2 reduces the cytotoxic effect of lentiviral gene transfer in human corneal endothelial cells. Invest. Ophthalmol. Vis. Sci. 53, 3207-3214
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. Yu, K., Xu, J., Liu, Z., Sosic, D., Shao, J., Olson, E. N., Towler, D. A., and Ornitz, D. M. (2003) Conditional inactivation of FGF receptor 2 reveals an essential role for FGF signaling in the regulation of osteoblast function and bone growth. Development 130, 3063-3074
63. Jacob, A. L., Smith, C., Partanen, J., and Ornitz, D. M. (2006) Fibroblast growth factor receptor 1 signaling in the osteo-chondrogenic cell lineage regulates sequential steps of osteoblast maturation. Dev. Biol. 296, 315-328