Isolated C-terminal tail of FGF23 alleviates hypophosphatemia by inhibiting FGF23-FGFR-Klotho complex formation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 1, 2010, Pages 407-412

  Goetz, Regina ^a   Nakada, Yuji ^b   Hu, Ming Chang ^b   Kurosu, Hiroshi ^b   Wang, Lei ^b   Nakatani, Teruyo ^c   Shi, Mingjun ^b   Eliseenkova, Anna V ^a   Razzaque, Mohammed S ^c,d   Moe, Orson W ^b   Kuro o, Makoto ^b   Mohammadi, Moosa ^a  

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

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

^c HARVARD SCHOOL OF DENTAL MEDICINE   (United States)

^d Riyadh Armed Forces Hospital ^*  (Saudi Arabia)

Author keywords

Binary FGF receptor 1c klotho complex; Composite FGF receptor 1c klotho interface; Endogenous inhibitor of FGF23; FGF23 antagonist; FGF23 C terminal peptide

Indexed keywords

FIBROBLAST GROWTH FACTOR 23; FIBROBLAST GROWTH FACTOR RECEPTOR 1; KLOTHO PROTEIN; LIGAND; PHOSPHATE; TERNARY COMPLEX FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; HYPERPHOSPHATEMIA; HYPOPHOSPHATEMIA; MOUSE; NONHUMAN; OPOSSUM; PHOSPHATE BLOOD LEVEL; PHOSPHATE EXCRETION; PHOSPHATURIA; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN ISOLATION; RAT; SIGNAL TRANSDUCTION; URINARY EXCRETION;

ANIMALS; CELL LINE; FIBROBLAST GROWTH FACTORS; GLUCURONIDASE; HUMANS; HYPOPHOSPHATEMIA; KIDNEY TUBULES; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MITOGEN-ACTIVATED PROTEIN KINASES; MULTIPROTEIN COMPLEXES; OPOSSUMS; PEPTIDES; PROTEIN STRUCTURE, TERTIARY; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 1; SIGNAL TRANSDUCTION;

RATTUS;

EID: 76249084836     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0902006107     Document Type: Article

References (48)

1. Dwyer K, Barone JE, Rogers JF (1992) Severe hypophosphatemia in postoperative patients. Nutr Clin Pract 7:279-283.
2. Alon US, et al. (2008) Calcimimetics as an Adjuvant Treatment for Familial Hypophosphatemic Rickets. Clin J Am Soc Nephrol 3:658-664.
3. Gaasbeek A, Meinders AE (2005) Hypophosphatemia: an update on its etiology and treatment. Am J Med 118:1094-1101.
4. Brunelli SM, Goldfarb S (2007) Hypophosphatemia: clinical consequences and management. J Am Soc Nephrol 18:1999-2003.
5. Imel EA, Econs MJ (2005) Fibroblast growth factor 23: roles in health and disease. J Am Soc Nephrol 16:2565-2575.
6. Negri AL (2007) Hereditary hypophosphatemias: new genes in the bone-kidney axis. Nephrology 12:317-320.
7. Shiber JR, Mattu A (2002) Serum phosphate abnormalities in the emergency department. J Emerg Med 23:395-400.
8. Bohannon NJ (1989) Large phosphate shifts with treatment for hyperglycemia. Arch Intern Med 149:1423-1425.
9. Charron T, et al. (2003) Intravenous phosphate in the intensive care unit: more aggressive repletion regimens for moderate and severe hypophosphatemia. Intensive Care Med 29:1273-1278.
10. Rosen GH, Boullata JI, O'Rangers EA, Enow NB, Shin B (1995) Intravenous phosphate repletion regimen for critically ill patients with moderate hypophosphatemia. Crit Care Med 23:1204-1210.
11. Anonymous; ADHR Consortium (2000) Autosomal dominant hypophosphataemic rickets is associated with mutations in FGF23. Nat Genet 26:345-348.
12. White KE, et al. (2001) The autosomal dominant hypophosphatemic rickets (ADHR) gene is a secreted polypeptide overexpressed by tumors that cause phosphate wasting. J Clin Endocrinol Metab 86:497-500.
13. Shimada T, et al. (2001) Cloning and characterization of FGF23 as a causative factor of tumor-induced osteomalacia. Proc Natl Acad Sci USA 98:6500-6505.
14. Baum M, Schiavi S, Dwarakanath V, Quigley R (2005) Effect of fibroblast growth factor-23 on phosphate transport in proximal tubules. Kidney Int 68:1148-1153.
15. Perwad F, Zhang MY, Tenenhouse HS, Portale AA (2007) Fibroblast growth factor 23 impairs phosphorus and vitamin D metabolism in vivo and suppresses 25-hydroxyvitamin D-1alpha-hydroxylase expression in vitro. Am J Physiol Renal Physiol 293:F1577-F1583.
16. Larsson T, et al. (2004) Transgenic mice expressing fibroblast growth factor 23 under the control of the alpha1(I) collagen promoter exhibit growth retardation, osteomalacia, and disturbed phosphate homeostasis. Endocrinology 145:3087-3094.
17. Shimada T, et al. (2002) Mutant FGF-23 responsible for autosomal dominant hypophosphatemic rickets is resistant to proteolytic cleavage and causes hypophosphatemia in vivo. Endocrinology 143:3179-3182.
18. White KE, et al. (2001) Autosomal-dominant hypophosphatemic rickets (ADHR) mutations stabilize FGF-23. Kidney Int 60:2079-2086.
19. Goetz R, et al. (2007) Molecular insights into the klotho-dependent, endocrine mode of action of fibroblast growth factor 19 subfamily members. Mol Cell Biol 27:3417-3428.
20. Kurosu H, et al. (2006) Regulation of fibroblast growth factor-23 signaling by klotho. J Biol Chem 281:6120-6123.
21. Urakawa I, et al. (2006) Klotho converts canonical FGF receptor into a specific receptor for FGF23. Nature 444:770-774.
22. Kuro-o M, et al. (1997) Mutation of the mouse klotho gene leads to a syndrome resembling ageing. Nature 390:45-51.
23. Garringer HJ, et al. (2008) Molecular genetic and biochemical analyses of FGF23 mutations in familial tumoral calcinosis. Am J Physiol Endocrinol Metab 295:E929-E937.
24. Yamashita T, Konishi M, Miyake A, Inui K, Itoh N (2002) Fibroblast growth factor (FGF)-23 inhibits renal phosphate reabsorption by activation of the mitogen-activated protein kinase pathway. J Biol Chem 277:28265-28270.
25. Segawa H, et al. (2003) Effect of hydrolysis-resistant FGF23-R179Q on dietary phosphate regulation of the renal type-II Na/Pi transporter. Pflugers Arch 446:585-592.
26. Anonymous; The HYP Consortium (1995) A gene (PEX) with homologies to endopeptidases is mutated in patients with X-linked hypophosphatemic rickets. Nat Genet 11:130-136.
27. Beck L, et al. (1997) Pex/PEX tissue distribution and evidence for a deletion in the 3′ region of the Pex gene in X-linked hypophosphatemic mice. J Clin Invest 99:1200-1209.
28. Eicher EM, Southard JL, Scriver CR, Glorieux FH (1976) Hypophosphatemia: mouse model for human familial hypophosphatemic (vitamin D-resistant) rickets. Proc Natl Acad Sci USA 73:4667-4671.
29. Strom TM, et al. (1997) Pex gene deletions in Gy and Hyp mice provide mouse models for X-linked hypophosphatemia. Hum Mol Genet 6:165-171.
30. van Boekel G, et al. (2008) Tumor producing fibroblast growth factor 23 localized by two-staged venous sampling. Eur J Endocrinol 158:431-437.
31. Jan de Beur SM (2005) Tumor-induced osteomalacia. JAMA 294:1260-1267.
32. Yamazaki Y, et al. (2008) Anti-FGF23 neutralizing antibodies show the physiological role and structural features of FGF23. J Bone Miner Res 23:1509-1518.
33. Aono Y, et al. (2009) Therapeutic effects of anti-FGF23 antibodies in hypophosphatemic rickets/osteomalacia. J Bone Miner Res 24:1879-1888.
34. Nakatani T, Ohnishi M, Razzaque MS (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.
35. Schouten BJ, Hunt PJ, Livesey JH, Frampton CM, Soule SG (2009) FGF23 elevation and hypophosphatemia after intravenous iron polymaltose: a prospective study. J Clin Endocrinol Metab 94:2332-2337.
36. BhanI, et al. (2006)Post-transplanthypophosphatemia: tertiary 'hyper-phosphatoninism'? Kidney Int 70:1486-1494.
37. Larsson T, Nisbeth U, Ljunggren O, Jüppner H, Jonsson KB (2003) Circulating concentration of FGF-23 increases as renal function declines in patients with chronic kidney disease, but does not change in response to variation in phosphate intake in healthy volunteers. Kidney Int 64:2272-2279.
38. Fliser D, et al. (2007) Fibroblast growth factor 23 (FGF23) predicts progression of chronic kidney disease: the Mild to Moderate Kidney Disease (MMKD) Study. J Am Soc Nephrol 18:2600-2608.
39. Garringer HJ, et al. (2007) Two novel GALNT3 mutations in familial tumoral calcinosis. Am J Med Genet A 143A:2390-2396.
40. Araya K, et al. (2005) A novel mutation in fibroblast growth factor 23 gene as a cause of tumoral calcinosis. J Clin Endocrinol Metab 90:5523-5527.
41. Kato Y, et al. (2000) Establishment of the anti-Klotho monoclonal antibodies and detection of Klotho protein in kidneys. Biochem Biophys Res Commun 267:597-602.
42. Li SA, et al. (2004) Immunohistochemical localization of Klotho protein in brain, kidney, and reproductive organs of mice. Cell Struct Funct 29:91-99.
43. Tsujikawa H, Kurotaki Y, Fujimori T, Fukuda K, Nabeshima Y (2003) Klotho, a gene related to a syndrome resembling human premature aging, functions in a negative regulatory circuit of vitamin D endocrine system. Mol Endocrinol 17:2393-2403.
44. Farrow EG, Davis SI, Summers LJ, White KE (2009) Initial FGF23-mediated signaling occurs in the distal convoluted tubule. J Am Soc Nephrol 20:955-960.
45. Imura A, et al. (2004) Secreted Klotho protein in sera and CSF: implication for posttranslational cleavage in release of Klotho protein from cell membrane. FEBS Lett 565:143-147.
46. Kurosu H, et al. (2005) Suppression of aging in mice by the hormone Klotho. Science 309:1829-1833.
47. Matsumura Y, et al. (1998) Identification of the human klotho gene and its two transcripts encoding membrane and secreted klotho protein. Biochem Biophys Res Commun 242:626-630.
48. Shiraki-Iida T, et al. (1998) Structure of the mouse klotho gene and its two transcripts encoding membrane and secreted protein. FEBS Lett 424:6-10.