A unified model for bone-renal mineral and energy metabolism

Current Opinion in Pharmacology

Volumn 22, Issue , 2015, Pages 64-71

  Rowe, Peter S ^a  

^a UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; BONE SIALOPROTEIN; DENTIN MATRIX PROTEIN 1; FIBROBLAST GROWTH FACTOR 23; MATRIX EXTRACELLULAR PHOSPHOGLYCOPROTEIN; OSTEOPONTIN; PHOSPHATE REGULATING NEUTRAL ENDOPEPTIDASE; STATHERIN; VITRONECTIN RECEPTOR; GLYCOPROTEIN; MEPE PROTEIN, HUMAN; PHOSPHOPROTEIN; SCLEROPROTEIN;

ARTICLE; BONE MINERALIZATION; BONE TURNOVER; CELL SURFACE; ENERGY METABOLISM; GENE EXPRESSION; HUMAN; MINERAL METABOLISM; NONHUMAN; OSTEOCYTE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; ANIMAL; BONE; KIDNEY; METABOLISM; PHYSIOLOGY;

ANIMALS; BONE AND BONES; CALCIFICATION, PHYSIOLOGIC; ENERGY METABOLISM; EXTRACELLULAR MATRIX PROTEINS; GLYCOPROTEINS; HUMANS; KIDNEY; PHOSPHOPROTEINS;

EID: 84928550437     PISSN: 14714892     EISSN: 14714973     Source Type: Journal    
DOI: 10.1016/j.coph.2015.03.006     Document Type: Review

References (80)

1. L.F. Bonewald The amazing osteocyte J Bone Miner Res 26 2011 229 238
2. G. Karsenty, and M. Ferron The contribution of bone to whole-organism physiology Nature 481 2012 314 320
3. R.L. Jilka The relevance of mouse models for investigating age-related bone loss in humans J Gerontol A Biol Sci Med Sci 68 2013 1209 1217
4. P.S. Rowe The chicken or the egg: PHEX FGF23 and SIBLINGs unscrambled Cell Biochem Funct 30 2012 355 375
5. J.P. Machado, W.E. Johnson, S.J. O'Brien, V. Vasconcelos, and A. Antunes Adaptive evolution of the matrix extracellular phosphoglycoprotein in mammals BMC Evol Biol 11 2011 342
6. J.J. Grantham, and D.P. Wallace Return of the secretory kidney Am J Physiol Renal Physiol 282 2002 F1 F9
7. P.S. Rowe, P.A. de Zoysa, R. Dong, H.R. Wang, K.E. White, M.J. Econs, and C.L. Oudet MEPE, a new gene expressed in bone marrow and tumors causing osteomalacia Genomics 67 2000 54 68
8. V. David, A.C. Martin, A.M. Hedge, M.K. Drezner, and P.S. Rowe ASARM peptides: PHEX-dependent & independent regulation of serum phosphate Am J Physiol Renal Physiol 300 2011 F783 F791
9. V. David, A. Martin, A.M. Hedge, and P.S. Rowe Matrix extracellular phosphoglycoprotein (MEPE) is a new bone renal hormone and vascularization modulator Endocrinology 150 2009 4012 4023
10. A. Martin, V. David, J.S. Laurence, P.M. Schwarz, E.M. Lafer, A.M. Hedge, and P.S. Rowe Degradation of MEPE DMP1, and release of SIBLING ASARM-peptides (minhibins): ASARM-peptide(s) are directly responsible for defective mineralization in HYP Endocrinology 149 2008 1757 1772
11. W. Addison, D. Masica, J. Gray, and M.D. McKee Phosphorylation-dependent inhibition of mineralization by osteopontin ASARM peptides is regulated by PHEX cleavage J Bone Miner Res 25 2009 695 705
12. W. Addison, Y. Nakano, T. Loisel, P. Crine, and M. McKee MEPE-ASARM peptides control extracellular matrix mineralization by binding to hydroxyapatite - an inhibition regulated by PHEX cleavage of ASARM J Bone Miner Res 23 2008 1638 1649
13. L. Zelenchuk, A. Hedge, and P.S. Rowe SPR4-peptide alters bone metabolism of normal and HYP mice Bone 72 2015 23 33
14. L.V. Zelenchuk, A.M. Hedge, and P.S. Rowe PHEX mimetic (SPR4-peptide) corrects and improves HYP and wild type mice energy-metabolism PLoS One 9 2014 e97326
15. P.S. Rowe, N. Matsumoto, O.D. Jo, R.N. Shih, J. Oconnor, M.P. Roudier, S. Bain, S. Liu, J. Harrison, and N. Yanagawa Correction of the mineralization defect in hyp mice treated with protease inhibitors CA074 and pepstatin Bone 39 2006 773 786
16. D.G. Shirley, N.J. Faria, R.J. Unwin, and H. Dobbie Direct micropuncture evidence that matrix extracellular phosphoglycoprotein inhibits proximal tubular phosphate reabsorption Nephrol Dial Transplant 25 2010 3191 3195
17. J. Marks, L.J. Churchill, S.D. Edward, and R. Unwin The phosphatonin matrix extracellular phosphoglycoprotein (MEPE) inhibits renal intestinal phosphate transport in vivo J Am Soc Nephrol 19 2008 2313 2320
18. H. Dobbie, R.J. Unwin, N.J. Faria, and D.G. Shirley Matrix extracellular phosphoglycoprotein causes phosphaturia in rats by inhibiting tubular phosphate reabsorption Nephrol Dial Transplant 23 2008 730 733
19. K.A. Staines, N.C. Mackenzie, C.E. Clarkin, L. Zelenchuk, P.S. Rowe, V.E. MacRae, and C. Farquharson MEPE is a novel regulator of growth plate cartilage mineralization Bone 51 2012 418 430
20. N.M. Barros, B. Hoac, R.L. Neves, W.N. Addison, D.M. Assis, M. Murshed, A.K. Carmona, and M.D. McKee Proteolytic processing of osteopontin by PHEX and accumulation of osteopontin fragments in Hyp mouse bone, the murine model of X-linked hypophosphatemia J Bone Miner Res 28 2013 688 699
21. B. Salmon, C. Bardet, M. Khaddam, J. Naji, B.R. Coyac, B. Baroukh, F. Letourneur, J. Lesieur, F. Decup, and D. Le Denmat MEPE-derived ASARM peptide inhibits odontogenic differentiation of dental pulp stem cells and impairs mineralization in tooth models of X-linked hypophosphatemia PLoS One 8 2013 e56749
22. G.J. Atkins, P.S. Rowe, H.P. Lim, K.J. Welldon, R. Ormsby, A.R. Wijenayaka, L. Zelenchuk, A. Evdokiou, and D.M. Findlay Sclerostin is a locally acting regulator of late-osteoblast/pre-osteocyte differentiation and regulates mineralization through a MEPE-ASARM dependent mechanism J Bone Miner Res 26 2011 1425 1436
23. HYP-consortium F. Francis, S. Hennig, B. Korn, R. Reinhardt, D. de Jong, A. Poustka, H. Lehrach, P.S.N. Rowe, and J.N. Goulding A gene (PEX) with homologies to endopeptidases is mutated in patients with X-linked hypophosphatemic rickets. The HYP Consortium Nat Genet 11 1995 130 136
24. T.O. Carpenter The expanding family of hypophosphatemic syndromes J Bone Miner Metab 30 2012 1 9
25. P.S. Rowe Regulation of bone-renal mineral and energy metabolism: the PHEX, FGF23, DMP1 MEPE ASARM pathway Crit Rev Eukaryot Gene Expr 22 2012 61 86
26. E.A. Imel, L.A. DiMeglio, S.L. Hui, T.O. Carpenter, and M.J. Econs Treatment of X-linked hypophosphatemia with calcitriol and phosphate increases circulating fibroblast growth factor 23 concentrations J Clin Endocrinol Metab 95 2010 1846 1850
27. P.J. Marie, R. Travers, and F.H. Glorieux Healing of bone lesions with 1,25-dihydroxyvitamin D3 in the young X-linked hypophosphataemic male mouse Endocrinology 111 1982 904 911
28. P.J. Marie, R. Travers, and F.H. Glorieux Bone response to phosphate and vitamin D metabolites in the hypophosphatemic male mouse Calcif Tissue Int 34 1982 158 164
29. B. Yuan, J.Q. Feng, S. Bowman, Y. Liu, R.D. Blank, I. Lindberg, and M.K. Drezner Hexa-d-arginine treatment increases 7B2∗PC2 activity in hyp-mouse osteoblasts and rescues the HYP phenotype J Bone Miner Res 28 2013 56 72
30. A. Cameron, J. Appel, R.A. Houghten, and I. Lindberg Polyarginines are potent furin inhibitors J Biol Chem 275 2000 36741 36749
31. J.Q. Feng, E.L. Clinkenbeard, B. Yuan, K.E. White, and M.K. Drezner Osteocyte regulation of phosphate homeostasis and bone mineralization underlies the pathophysiology of the heritable disorders of rickets and osteomalacia Bone 54 2013 213 221
32. T.O. Carpenter, E.A. Imel, M.D. Ruppe, T.J. Weber, M.A. Klausner, M.M. Wooddell, T. Kawakami, T. Ito, X. Zhang, and J. Humphrey Randomized trial of the anti-FGF23 antibody KRN23 in X-linked hypophosphatemia J Clin Invest 124 2014 1587 1597
33. Y. Aono, Y. Yamazaki, J. Yasutake, T. Kawata, H. Hasegawa, I. Urakawa, T. Fujita, M. Wada, T. Yamashita, and S. Fukumoto Therapeutic effects of anti-FGF23 antibodies in hypophosphatemic rickets/osteomalacia J Bone Miner Res 24 2009 1879 1888
34. T. Shimada, and S. Fukumoto FGF23 as a novel therapeutic target Adv Exp Med Biol 728 2012 158 170
35. V. Shalhoub Chronic kidney disease: FGF23 neutralization associated with increased risk of death Nat Rev Nephrol 8 2012 492
36. V. Shalhoub, E.M. Shatzen, S.C. Ward, J. Davis, J. Stevens, V. Bi, L. Renshaw, N. Hawkins, W. Wang, and C. Chen FGF23 neutralization improves chronic kidney disease-associated hyperparathyroidism yet increases mortality J Clin Invest 122 2012 2543 2553
37. J.L. Millan The role of phosphatases in the initiation of skeletal mineralization Calcif Tissue Int 93 2013 299 306
38. M.D. McKee, M.C. Yadav, B.L. Foster, M.J. Somerman, C. Farquharson, and J.L. Millan Compounded PHOSPHO1/ALPL deficiencies reduce dentin mineralization J Dent Res 92 2013 721 727
39. T. Kiffer-Moreira, M.C. Yadav, D. Zhu, S. Narisawa, C. Sheen, B. Stec, N.D. Cosford, R. Dahl, C. Farquharson, and M.F. Hoylaerts Pharmacological inhibition of PHOSPHO1 suppresses vascular smooth muscle cell calcification J Bone Miner Res 28 2013 81 91
40. V.S. Tagliabracci, J.L. Engel, J. Wen, S.E. Wiley, C.A. Worby, L.N. Kinch, J. Xiao, N.V. Grishin, and J.E. Dixon Secreted kinase phosphorylates extracellular proteins that regulate biomineralization Science 336 2012 1150 1153
41. H.O. Ishikawa, A. Xu, E. Ogura, G. Manning, and K.D. Irvine The Raine syndrome protein FAM20C is a Golgi kinase that phosphorylates bio-mineralization proteins PLoS One 7 2012 e42988
42. Y. Kinoshita, M. Hori, M. Taguchi, and S. Fukumoto Functional analysis of mutant FAM20C in Raine syndrome with FGF23-related hypophosphatemia Bone 67 2014 145 151
43. A. Tagliabracci, J.L. Engel, S.E. Wiley, J. Xiao, D.J. Gonzalez, H.N. Appaiah, A. Koller, V. Nizet, K.E. White, and J.E. Dixon Dynamic regulation of FGF23 by Fam20C phosphorylation GalNAc-T3 glycosylation, and furin proteolysis Proc Natl Acad Sci U S A 111 2014 5520 5525
44. I. Lindberg, H.W. Pang, J.P. Stains, D. Clark, A.J. Yang, L. Bonewald, and K.Z. Li FGF23 is endogenously phosphorylated in bone cells J Bone Miner Res 30 2015 449 454
45. X. Wang, S. Wang, C. Li, T. Gao, Y. Liu, A. Rangiani, Y. Sun, J. Hao, A. George, and Y. Lu Inactivation of a novel FGF23 regulator FAM20C, leads to hypophosphatemic rickets in mice PLoS Genet 8 2012 e1002708
46. P. Vogel, G.M. Hansen, R.W. Read, R.B. Vance, M. Thiel, J. Liu, T.J. Wronski, D.D. Smith, S. Jeter-Jones, and R. Brommage Amelogenesis imperfecta and other biomineralization defects in Fam20a and Fam20c null mice Vet Pathol 49 2012 998 1017
47. S.H. Rafaelsen, H. Raeder, A.K. Fagerheim, P. Knappskog, T.O. Carpenter, S. Johansson, and R. Bjerknes Exome sequencing reveals FAM20c mutations associated with fibroblast growth factor 23-related hypophosphatemia, dental anomalies, and ectopic calcification J Bone Miner Res 28 2013 1378 1385
48. A. Yancovitch, D. Hershkovitz, M. Indelman, P. Galloway, M. Whiteford, E. Sprecher, and E. Kilic Novel mutations in GALNT3 causing hyperphosphatemic familial tumoral calcinosis J Bone Miner Metab 29 2011 621 625
49. C.B. Confavreux, R.L. Levine, and G. Karsenty A paradigm of integrative physiology, the crosstalk between bone and energy metabolisms Mol Cell Endocrinol 310 2009 21 29
50. V.K. Yadav, F. Oury, K. Tanaka, T. Thomas, Y. Wang, S. Cremers, R. Hen, A. Krust, P. Chambon, and G. Karsenty Leptin-dependent serotonin control of appetite: temporal specificity, transcriptional regulation, and therapeutic implications J Exp Med 208 2011 41 52
51. G. Karsenty, and M.D. Gershon The importance of the gastrointestinal tract in the control of bone mass accrual Gastroenterology 141 2011 439 442
52. V.K. Yadav, J.H. Ryu, N. Suda, K.F. Tanaka, J.A. Gingrich, G. Schutz, F.H. Glorieux, C.Y. Chiang, J.D. Zajac, and K.L. Insogna Lrp5 controls bone formation by inhibiting serotonin synthesis in the duodenum Cell 135 2008 825 837
53. R. Baron, and M. Kneissel WNT signaling in bone homeostasis and disease: from human mutations to treatments Nat Med 19 2013 179 192
54. A. Kode, A. Obri, R. Paone, S. Kousteni, P. Ducy, and G. Karsenty Lrp5 regulation of bone mass and serotonin synthesis in the gut Nat Med 20 2014 1228 1229
55. Y. Cui, P.J. Niziolek, B.T. MacDonald, N. Alenina, S. Matthes, C.M. Jacobsen, R.A. Conlon, R. Brommage, D.R. Powell, and X. He Reply to Lrp5 regulation of bone mass and gut serotonin synthesis Nat Med 20 2014 1229 1230
56. G.S. Lee, C. Simpson, B.H. Sun, C. Yao, D. Foer, B. Sullivan, S. Matthes, N. Alenina, J. Belsky, and M. Bader Measurement of plasma, serum, and platelet serotonin in individuals with high bone mass and mutations in LRP5 J Bone Miner Res 29 2013 976 981
57. D. Goltzman LRP5, serotonin and bone: complexity, contradictions and conundrums J Bone Miner Res 26 2011 2002 2011
58. Y. Cui, P.J. Niziolek, B.T. Macdonald, C.R. Zylstra, N. Alenina, D.R. Robinson, Z. Zhong, S. Matthes, C.M. Jacobsen, and R.A. Conlon Lrp5 functions in bone to regulate bone mass Nat Med 17 2011 684 691
59. M.S. Nanes Phosphate wasting and fibroblast growth factor-23 Curr Opin Endocrinol Diabetes Obes 20 2013 523 531
60. W. Xie, M.C. Mechin, S.G. Dubois, D. Lajeunesse, and G. van de Werve Up-regulation of liver glucose-6-phosphatase in x-linked hypophosphatemic mice Horm Metab Res 34 2002 288 292
61. M. Wojcik, K. Dolezal-Oltarzewska, D. Janus, D. Drozdz, K. Sztefko, and J.B. Starzyk FGF23 contributes to insulin sensitivity in obese adolescents - preliminary results Clin Endocrinol (Oxf) 77 2012 537 540
62. M. Wojcik, D. Janus, K. Dolezal-Oltarzewska, D. Drozdz, K. Sztefko, and J.B. Starzyk The association of FGF23 levels in obese adolescents with insulin sensitivity J Pediatr Endocrinol Metab 25 2012 687 690
63. L. Haglin Hypophosphataemia: cause of the disturbed metabolism in the metabolic syndrome Med Hypotheses 56 2001 657 663
64. E. Levi, G.Z. Fadda, C. Ozbasli, and S.G. Massry Evolution of metabolic and functional derangements of pancreatic islets in phosphate depletion Endocrinology 131 1992 2182 2188
65. S.F. Travis, H.J. Sugerman, R.L. Ruberg, S.J. Dudrick, M. Delivoria-Papadopoulos, L.D. Miller, and F.A. Oski Alterations of red-cell glycolytic intermediates and oxygen transport as a consequence of hypophosphatemia in patients receiving intravenous hyperalimentation N Engl J Med 285 1971 763 768
66. B.D. Hettleman, R.L. Sabina, M.K. Drezner, E.W. Holmes, and J.L. Swain Defective adenosine triphosphate synthesis. An explanation for skeletal muscle dysfunction in phosphate-deficient mice J Clin Invest 72 1983 582 589
67. R.L. Sabina, M.K. Drezner, and E.W. Holmes Reduced renal cortical ribonucleoside triphosphate pools in three different hypophosphatemic animal models Biochem Biophys Res Commun 109 1982 649 655
68. L.K. Vaughn, R.A. Meyer Jr., and M.H. Meyer Increased metabolic rate in X-linked hypophosphatemic mice Endocrinology 118 1986 441 445
69. M. Hirao, J. Hashimoto, N. Yamasaki, W. Ando, H. Tsuboi, A. Myoui, and H. Yoshikawa Oxygen tension is an important mediator of the transformation of osteoblasts to osteocytes J Bone Miner Metab 25 2007 266 276
70. L.F. Bonewald Osteocytes: a proposed multifunctional bone cell J Musculoskelet Neuronal Interact 2 2002 239 241
71. M. Ferron, J. Wei, T. Yoshizawa, A. Del Fattore, R.A. DePinho, A. Teti, P. Ducy, and G. Karsenty Insulin signaling in osteoblasts integrates bone remodeling and energy metabolism Cell 142 2010 296 308
72. N.K. Lee, H. Sowa, E. Hinoi, M. Ferron, J.D. Ahn, C. Confavreux, R. Dacquin, P.J. Mee, M.D. McKee, and D.Y. Jung Endocrine regulation of energy metabolism by the skeleton Cell 130 2007 456 469
73. C. de Lorenzo, A. Greco, T.V. Fiorentino, G.C. Mannino, and M.L. Hribal Variants of insulin-signaling inhibitor genes in type 2 diabetes and related metabolic abnormalities Int J Genomics 2013 2013 376454
74. B.A. Maddux, Y.N. Chang, D. Accili, O.P. McGuinness, J.F. Youngren, and I.D. Goldfine Overexpression of the insulin receptor inhibitor PC-1/ENPP1 induces insulin resistance and hyperglycemia Am J Physiol Endocrinol Metab 290 2006 E746 E749
75. Q. Li, H. Guo, D.W. Chou, A. Berndt, J.P. Sundberg, and J. Uitto Mutant Enpp1asj mice as a model for generalized arterial calcification of infancy Dis Model Mech 6 2013 1227 1235
76. N.C. Mackenzie, D. Zhu, E.M. Milne, R. van't Hof, A. Martin, L. Darryl Quarles, J.L. Millan, C. Farquharson, and V.E. MacRae Altered bone development and an increase in FGF-23 expression in Enpp1(-/-) mice PLoS One 7 2012 e32177
77. I.D. Goldfine, B.A. Maddux, J.F. Youngren, G. Reaven, D. Accili, V. Trischitta, R. Vigneri, and L. Frittitta The role of membrane glycoprotein plasma cell antigen 1/ectonucleotide pyrophosphatase phosphodiesterase 1 in the pathogenesis of insulin resistance and related abnormalities Endocr Rev 29 2008 62 75
78. J. Gattineni, and M. Baum Genetic disorders of phosphate regulation Pediatr Nephrol 27 2012 1477 1487
79. E.G. Farrow, E.A. Imel, and K.E. White Miscellaneous non-inflammatory musculoskeletal conditions. Hyperphosphatemic familial tumoral calcinosis (FGF23, GALNT3 and alphaKlotho) Best Pract Res Clin Rheumatol 25 2011 735 747
80. S. Opsahl Vital, C. Gaucher, C. Bardet, P.S. Rowe, A. George, A. Linglart, and C. Chaussain Tooth dentin defects reflect genetic disorders affecting bone mineralization Bone 50 2012 989 997