1,25-Dihydroxyvitamin D Alone Improves Skeletal Growth, Microarchitecture, and Strength in a Murine Model of XLH, Despite Enhanced FGF23 Expression

Journal of Bone and Mineral Research

Volumn 31, Issue 5, 2016, Pages 929-939

  Liu, Eva S ^a,b,c   Martins, Janaina S ^b,c,d   Raimann, Adalbert ^b,c,e   Chae, Byongsoo Timothy ^b   Brooks, Daniel J ^b,f   Jorgetti, Vanda ^d   Bouxsein, Mary L ^b,c,f   Demay, Marie B ^b,c  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF SÃO PAULO   (Brazil)

^e UNIV KLIN KINDER JUGENDHEILKUNDE   (Austria)

^f BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

BIOMECHANICS; BONE QCT CT; GENETIC MOUSE MODELS; GROWTH PLATE; PTH VIT D FGF23

Indexed keywords

ALPHA KLOTHO PROTEIN; CALCITRIOL; CALCIUM; FIBROBLAST GROWTH FACTOR 23; FIBROBLAST GROWTH FACTOR 23 ANTIBODY; KLOTHO PROTEIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PARATHYROID HORMONE; PHOSPHATE; PROTEIN ANTIBODY; SODIUM PHOSPHATE COTRANSPORTER 2A; UNCLASSIFIED DRUG; FIBROBLAST GROWTH FACTOR; SLC34A1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOMECHANICS; BONE GROWTH; BONE MICROARCHITECTURE; BONE STRENGTH; BONE STRUCTURE; CALCIUM BLOOD LEVEL; CONTROLLED STUDY; DRUG DOSE REGIMEN; DRUG EFFECT; DRUG EFFICACY; DRUG MEGADOSE; GROWTH PLATE; IMMUNOHISTOCHEMISTRY; MALE; METAPHYSIS; MONOTHERAPY; MOUSE; MOUSE MODEL; NONHUMAN; PARATHYROID HORMONE BLOOD LEVEL; PHOSPHATE BLOOD LEVEL; PHOSPHATE URINE LEVEL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; SUPPLEMENTATION; TRABECULAR BONE; X LINKED HYPOPHOSPHATEMIC RICKETS; ANIMAL; BONE DENSITY; DISEASE MODEL; DRUG EFFECTS; FAMILIAL HYPOPHOSPHATEMIC RICKETS; GENETICS; HUMAN; MAPK SIGNALING; METABOLISM; PATHOLOGY; SKELETON;

ANIMALS; BONE DENSITY; CALCITRIOL; DISEASE MODELS, ANIMAL; FAMILIAL HYPOPHOSPHATEMIC RICKETS; FIBROBLAST GROWTH FACTORS; HUMANS; MAP KINASE SIGNALING SYSTEM; MICE; MITOGEN-ACTIVATED PROTEIN KINASE 3; SKELETON; SODIUM-PHOSPHATE COTRANSPORTER PROTEINS, TYPE IIA;

EID: 84968880437     PISSN: 08840431     EISSN: 15234681     Source Type: Journal    
DOI: 10.1002/jbmr.2783     Document Type: Article

References (45)

1. Carpenter TO, Imel EA, Holm IA, Jan de Beur SM, Insogna KL,. A clinician's guide to X-linked hypophosphatemia. J Bone Miner Res. 2011; 26 (7): 1381-8.
2. Friedman NE, Lobaugh B, Drezner MK., Effects of calcitriol and phosphorus therapy on the growth of patients with X-linked hypophosphatemia. J Clin Endocrinol Metab. 1993; 76 (4): 839-44.
3. Liu S, Zhou J, Tang W, et al., Pathogenic role of Fgf23 in Hyp mice. Am J Physiol Endocrinol Metab. 2006; 291 (1): E38-49.
4. A gene (PEX) with homologies to endopeptidases is mutated in patients with X-linked hypophosphatemic rickets. The HYP Consortium. Nat Genet. 1995; 11 (2): 130-6.
5. Miedlich SU, Zalutskaya A, Zhu ED, Demay MB., Phosphate-induced apoptosis of hypertrophic chondrocytes is associated with a decrease in mitochondrial membrane potential and is dependent upon ERK1/2 phosphorylation. J Biol Chem. 2010; 285: 18270-5.
6. Sabbagh Y, Carpenter TO, Demay M., Hypophosphatemia leads to rickets by impairing caspase-mediated apoptosis of hypertrophic chondrocytes. Proc Natl Acad Sci USA. 2005; 102: 9637-42.
7. Miedlich SU, Zhu ED, Sabbagh Y, Demay MB., The receptor-dependent actions of 1,25-dihydroxyvitamin D are required for normal growth plate maturation in NPt2a knockout mice. Endocrinology. 2010; 151 (10): 4607-12.
8. Marie PJ, Travers R, Glorieux FH., Bone response to phosphate and vitamin D metabolites in the hypophosphatemic male mouse. Calcif Tissue Int. 1982; 34 (2): 158-64.
9. Verge CF, Lam A, Simpson JM, Cowell CT, Howard NJ, Silink M., Effects of therapy in X-linked hypophosphatemic rickets. N Engl J Med. 1991; 325 (26): 1843-8.
10. Marie PJ, Travers R, Glorieux FH., Healing of bone lesions with 1,25-dihydroxyvitamin D3 in the young X-linked hypophosphatemic male mouse. Endocrinology. 1982; 111 (3): 904-11.
11. Harrell RM, Lyles KW, Harrelson JM, Friedman NE, Drezner MK., Healing of bone disease in X-linked hypophosphatemic rickets/osteomalacia. Induction and maintenance with phosphorus and calcitriol. J Clin Invest. 1985; 75 (6): 1858-68.
12. Aono Y, Yamazaki Y, Yasutake J, et al., Therapeutic effects of anti-FGF23 antibodies in hypophosphatemic rickets/osteomalacia. J Bone Miner Res. 2009; 24 (11): 1879-88.
13. Carpenter TO, Imel EA, Ruppe MD, et al., Randomized trial of the anti-FGF23 antibody KRN23 in X-linked hypophosphatemia. J Clin Invest. 2014; 124 (4): 1587-97.
14. Imel EA, Zhang X, Ruppe MD, et al., Prolonged correction of serum phosphorus in adults with X-linked hypophosphatemia using monthly doses of KRN23. J Clin Endocrinol Metab. 2015; 100 (7): 2565-73.
15. Wohrle S, Henninger C, Bonny O, et al., Pharmacological inhibition of fibroblast growth factor (FGF) receptor signaling ameliorates FGF23-mediated hypophosphatemic rickets. J Bone Miner Res. 2013; 28 (4): 899-911.
16. Zhang MY, Ranch D, Pereira RC, Armbrecht HJ, Portale AA, Perwad F., Chronic inhibition of ERK1/2 signaling improves disordered bone and mineral metabolism in hypophosphatemic (Hyp) mice. Endocrinology. 2012; 153 (4): 1806-16.
17. Xiao Z, Huang J, Cao L, Liang Y, Han X, Quarles LD., Osteocyte-specific deletion of Fgfr1 suppresses FGF23. PloS One. 2014; 9 (8): e104154.
18. Li H, Martin A, David V, Quarles LD., Compound deletion of Fgfr3 and Fgfr4 partially rescues the Hyp mouse phenotype. Am J Physiol Endocrinol Metab. 2011; 300 (3): E508-17.
19. Brownstein CA, Zhang J, Stillman A, et al., Increased bone volume and correction of HYP mouse hypophosphatemia in the Klotho/HYP mouse. Endocrinology. 2010; 151 (2): 492-501.
20. Liu ES, Zalutskaya A, Chae BT, Zhu ED, Gori F, Demay MB., Phosphate interacts with PTHrP to regulate endochondral bone formation. Endocrinology. 2014; 155 (10): 3750-6.
21. Zhu ED, Louis L, Brooks DJ, Bouxsein ML, Demay MB., Effect of bisphosphonates on the rapidly growing male murine skeleton. Endocrinology. 2014; 155 (4): 1188-96.
22. Dempster DW, Compston JE, Drezner MK, et al., Standardized nomenclature, symbols, and units for bone histomorphometry: a 2012 update of the report of the ASBMR Histomorphometry Nomenclature Committee. J Bone Miner Res. 2013; 28 (1): 2-17.
23. Martin A, Liu S, David V, et al., Bone proteins PHEX and DMP1 regulate fibroblastic growth factor Fgf23 expression in osteocytes through a common pathway involving FGF receptor (FGFR) signaling. FASEB J. 2011; 25 (8): 2551-62.
24. Wang X, Wang S, Li C, et al., Inactivation of a novel FGF23 regulator, FAM20C, leads to hypophosphatemic rickets in mice. PLoS Genet. 2012; 8 (5): e1002708.
25. Feng JQ, Ward LM, Liu S, et al., Loss of DMP1 causes rickets and osteomalacia and identifies a role for osteocytes in mineral metabolism. Nat Genet. 2006; 38 (11): 1310-5.
26. Lorenz-Depiereux B, Schnabel D, Tiosano D, Hausler G, Strom TM., Loss-of-function ENPP1 mutations cause both generalized arterial calcification of infancy and autosomal-recessive hypophosphatemic rickets. Am J Hum Genet. 2010; 86 (2): 267-72.
27. Ichikawa S, Sorenson AH, Austin AM, et al., Ablation of the Galnt3 gene leads to low-circulating intact fibroblast growth factor 23 (Fgf23) concentrations and hyperphosphatemia despite increased Fgf23 expression. Endocrinology. 2009; 150 (6): 2543-50.
28. Lee K, Lanske B, Karaplis AC, et al., Parathyroid hormone-related peptide delays terminal differentiation of chondrocytes during endochondral bone development. Endocrinology. 1996; 137 (11): 5109-18.
29. Roberts S, Narisawa S, Harmey D, Millan JL, Farquharson C., Functional involvement of PHOSPHO1 in matrix vesicle-mediated skeletal mineralization. J Bone Miner Res. 2007; 22 (4): 617-27.
30. Wang W, Xu J, Du B, Kirsch T., Role of the progressive ankylosis gene (ank) in cartilage mineralization. Mol Cell Biol. 2005; 25 (1): 312-23.
31. Wennberg C, Hessle L, Lundberg P, et al., Functional characterization of osteoblasts and osteoclasts from alkaline phosphatase knockout mice. J Bone Miner Res. 2000; 15 (10): 1879-88.
32. Murshed M, Schinke T, McKee MD, Karsenty G., Extracellular matrix mineralization is regulated locally; different roles of two gla-containing proteins. J Cell Biol. 2004; 165 (5): 625-30.
33. Kogawa M, Wijenayaka AR, Ormsby RT, et al., Sclerostin regulates release of bone mineral by osteocytes by induction of carbonic anhydrase 2. J Bone Miner Res. 2013; 28 (12): 2436-48.
34. Wijenayaka AR, Yang D, Prideaux M, et al., 1alpha,25-dihydroxyvitamin D3 stimulates human SOST gene expression and sclerostin secretion. Mol Cell Endocrinol. 2015; 413: 157-67.
35. Glorieux FH, Marie PJ, Pettifor JM, Delvin EE., Bone response to phosphate salts, ergocalciferol, and calcitriol in hypophosphatemic vitamin D-resistant rickets. N Engl J Med. 1980; 303 (18): 1023-31.
36. Marie PJ, Travers R, Glorieux FH., Healing of rickets with phosphate supplementation in the hypophosphatemic male mouse. J Clin Invest. 1981; 67 (3): 911-4.
37. Meyer RA Jr, Meyer MH, Morgan PL., Effects of altered diet on serum levels of 1,25-dihydroxyvitamin D and parathyroid hormone in X-linked hypophosphatemic (Hyp and Gy) mice. Bone. 1996; 18 (1): 23-8.
38. Tagliabracci VS, Engel JL, Wiley SE, et al., Dynamic regulation of FGF23 by Fam20C phosphorylation, GalNAc-T3 glycosylation, and furin proteolysis. Proc Natl Acad Sci USA. 2014; 111 (15): 5520-5.
39. Goetz R, Nakada Y, Hu MC, et al., Isolated C-terminal tail of FGF23 alleviates hypophosphatemia by inhibiting FGF23-FGFR-Klotho complex formation. Proc Natl Acad Sci USA. 2010; 107 (1): 407-12.
40. Ecarot B, Glorieux F, Desbarats M, Travers R, Labelle L., Defective bone formation by Hyp mouse bone cells transplanted into normal mice: evidence in favor of an intrinsic osteoblast defect. J Bone Miner Res. 1992; 7: 215-20.
41. Miao D, Bai X, Panda D, McKee M, Karaplis A, Goltzman D., Osteomalacia in Hyp mice is associated with abnormal Phex expression and with altered bone matrix protein expression and deposition. Endocrinology. 2001; 142: 926-39.
42. Liu S, Tang W, Zhou J, Vierthaler L, Quarles LD., Distinct roles for intrinsic osteocyte abnormalities and systemic factors in regulation of FGF23 and bone mineralization in Hyp mice. Am J Physiol Endocrinol Metab. 2007; 293 (6): E1636-44.
43. Sitara D, Kim S, Razzaque MS, et al., Genetic evidence of serum phosphate-independent functions of FGF-23 on bone. PLoS Genet. 2008; 4 (8): e1000154.
44. Bresler D, Bruder J, Mohnike K, Fraser WD, Rowe PS., Serum MEPE-ASARM-peptides are elevated in X-linked rickets (HYP): implications for phosphaturia and rickets. J Endocrinol. 2004; 183 (3): R1-9.
45. Sullivan W, Carpenter T, Glorieux F, Travers R, Insogna K,. A prospective trial of phosphate and 1, 25-dihydroxyvitamin D3 therapy in symptomatic adults with X-linked hypophosphatemic rickets. J Clin Endocrinol Metab. 1992; 75 (3): 879-85.