Skip to main content
Top
Published in: Calcified Tissue International 1/2015

01-07-2015 | Original Research

Biphasic Effects of Vitamin D and FGF23 on Human Osteoclast Biology

Authors: Lise Allard, Nathalie Demoncheaux, Irma Machuca-Gayet, Dan Georgess, Fabienne Coury-Lucas, Pierre Jurdic, Justine Bacchetta

Published in: Calcified Tissue International | Issue 1/2015

Login to get access

Abstract

Vitamin D and FGF23 play a major role in calcium/phosphate balance. Vitamin D may control bone resorption but the potential role of FGF23 has never been evaluated. The objective of this study was therefore to compare the effects of vitamin D and FGF23 on osteoclast differentiation and activity in human monocyte-derived osteoclasts. Human monocytes, purified from blood of healthy donors, were incubated with M-CSF and RANKL to obtain mature multinucleated osteoclasts (MNC). Experiments were carried out to assess the effects of FGF23 as compared to native vitamin D (25-D) and active vitamin D (1,25-D) on osteoclast differentiation and on bone-resorbing osteoclast activity. Additional experiments with the pan fibroblast growth factor receptor inhibitor (FGFR-i) were performed. Phosphorylation Akt and Erk pathways were analyzed by Western blot analyses. Both 1,25-D and FGF23, to a lesser extent, significantly inhibited osteoclastogenesis at early stages; when adding FGFR-i, osteoclast formation was restored. Biochemical experiments showed an activation of the Akt and Erk pathways under FGF23 treatment. In contrast, in terms of activity, 1,25-D had no effect on resorption, whereas FGF23 slightly but significantly increased bone resorption; 25-D had no effects on either differentiation or on activity. These data show that 1,25-D inhibits osteoclastogenesis without regulating osteoclast-mediated bone resorption activity; FGF23 has biphasic effects on osteoclast physiology, inhibiting osteoclast formation while stimulating slightly osteoclast activity. These results may be of importance and taken into account in chronic kidney disease when therapies modulating FGF23 are available.
Literature
1.
go back to reference Razzaque MS (2009) FGF23-mediated regulation of systemic phosphate homeostasis: is Klotho an essential player? Am J Physiol 296:470–476 Razzaque MS (2009) FGF23-mediated regulation of systemic phosphate homeostasis: is Klotho an essential player? Am J Physiol 296:470–476
2.
go back to reference Yamazaki Y, Tamada T, Kasai N et al (2008) Anti-FGF23 neutralizing antibodies show the physiological role and structural features of FGF23. J Bone Miner Res 23:1509–1518PubMedCrossRef Yamazaki Y, Tamada T, Kasai N et al (2008) Anti-FGF23 neutralizing antibodies show the physiological role and structural features of FGF23. J Bone Miner Res 23:1509–1518PubMedCrossRef
3.
go back to reference Ben-Dov IZ, Galitzer H, Lavi-Moshayoff V et al (2007) The parathyroid is a target organ for FGF23 in rats. J Clin Invest 117:4003–4008PubMedCentralPubMed Ben-Dov IZ, Galitzer H, Lavi-Moshayoff V et al (2007) The parathyroid is a target organ for FGF23 in rats. J Clin Invest 117:4003–4008PubMedCentralPubMed
4.
go back to reference Yoshiko Y, Wang H, Minamizaki T et al (2007) Mineralized tissue cells are a principal source of FGF23. Bone 40:1565–1573PubMedCrossRef Yoshiko Y, Wang H, Minamizaki T et al (2007) Mineralized tissue cells are a principal source of FGF23. Bone 40:1565–1573PubMedCrossRef
6.
go back to reference Bacchetta J, Sea JL, Chun RF et al (2013) Fibroblast growth factor 23 inhibits extrarenal synthesis of 1,25-dihydroxyvitamin D in human monocytes. J Bone Miner Res 28:46–55PubMedCentralPubMedCrossRef Bacchetta J, Sea JL, Chun RF et al (2013) Fibroblast growth factor 23 inhibits extrarenal synthesis of 1,25-dihydroxyvitamin D in human monocytes. J Bone Miner Res 28:46–55PubMedCentralPubMedCrossRef
7.
go back to reference Gattineni J, Alphonse P, Zhang Q, Mathews N, Bates CM, Baum M (2014) Regulation of renal phosphate transport by FGF23 is mediated by FGFR1 and FGFR4. Am J Physiol 306:351–358 Gattineni J, Alphonse P, Zhang Q, Mathews N, Bates CM, Baum M (2014) Regulation of renal phosphate transport by FGF23 is mediated by FGFR1 and FGFR4. Am J Physiol 306:351–358
8.
go back to reference Kurosu H, Kuro-O M (2009) The Klotho gene family as a regulator of endocrine fibroblast growth factors. Mol Cell Endocrinol 299:72–78PubMedCrossRef Kurosu H, Kuro-O M (2009) The Klotho gene family as a regulator of endocrine fibroblast growth factors. Mol Cell Endocrinol 299:72–78PubMedCrossRef
9.
go back to reference Farrow EG, Davis SI, Summers LJ, White KE (2009) Initial FGF23-mediated signaling occurs in the distal convoluted tubule. J Am Soc Nephrol 20:955–960PubMedCentralPubMedCrossRef Farrow EG, Davis SI, Summers LJ, White KE (2009) Initial FGF23-mediated signaling occurs in the distal convoluted tubule. J Am Soc Nephrol 20:955–960PubMedCentralPubMedCrossRef
10.
go back to reference Wang H, Yoshiko Y, Yamamoto R et al (2008) Overexpression of fibroblast growth factor 23 suppresses osteoblast differentiation and matrix mineralization in vitro. J Bone Miner Res 23:939–948PubMedCrossRef Wang H, Yoshiko Y, Yamamoto R et al (2008) Overexpression of fibroblast growth factor 23 suppresses osteoblast differentiation and matrix mineralization in vitro. J Bone Miner Res 23:939–948PubMedCrossRef
11.
12.
go back to reference Wesseling-Perry K, Pereira RC, Wang H et al (2009) Relationship between plasma fibroblast growth factor-23 concentration and bone mineralization in children with renal failure on peritoneal dialysis. J Clin Endocrinol Metab 94:511–517PubMedCentralPubMedCrossRef Wesseling-Perry K, Pereira RC, Wang H et al (2009) Relationship between plasma fibroblast growth factor-23 concentration and bone mineralization in children with renal failure on peritoneal dialysis. J Clin Endocrinol Metab 94:511–517PubMedCentralPubMedCrossRef
14.
go back to reference Cappariello A, Maurizi A, Veeriah V, Teti A (2014) The Great Beauty of the osteoclast. Arch Biochem Biophys 558:70–78PubMedCrossRef Cappariello A, Maurizi A, Veeriah V, Teti A (2014) The Great Beauty of the osteoclast. Arch Biochem Biophys 558:70–78PubMedCrossRef
15.
go back to reference Takasu H, Sugita A, Uchiyama Y et al (2006) c-Fos protein as a target of anti-osteoclastogenic action of vitamin D, and synthesis of new analogs. J Clin Invest 116:528–535PubMedCentralPubMedCrossRef Takasu H, Sugita A, Uchiyama Y et al (2006) c-Fos protein as a target of anti-osteoclastogenic action of vitamin D, and synthesis of new analogs. J Clin Invest 116:528–535PubMedCentralPubMedCrossRef
16.
go back to reference Sakai S, Takaishi H, Matsuzaki K et al (2009) 1-Alpha, 25-dihydroxy vitamin D3 inhibits osteoclastogenesis through IFN-beta-dependent NFATc1 suppression. J Bone Miner Metab 27:643–652PubMedCrossRef Sakai S, Takaishi H, Matsuzaki K et al (2009) 1-Alpha, 25-dihydroxy vitamin D3 inhibits osteoclastogenesis through IFN-beta-dependent NFATc1 suppression. J Bone Miner Metab 27:643–652PubMedCrossRef
17.
go back to reference Vincent C, Findlay DM, Welldon KJ et al (2009) Pro-inflammatory cytokines TNF-related weak inducer of apoptosis (TWEAK) and TNFalpha induce the mitogen-activated protein kinase (MAPK)-dependent expression of sclerostin in human osteoblasts. J Bone Miner Res 24:1434–1449PubMedCrossRef Vincent C, Findlay DM, Welldon KJ et al (2009) Pro-inflammatory cytokines TNF-related weak inducer of apoptosis (TWEAK) and TNFalpha induce the mitogen-activated protein kinase (MAPK)-dependent expression of sclerostin in human osteoblasts. J Bone Miner Res 24:1434–1449PubMedCrossRef
18.
go back to reference Kogawa M, Findlay DM, Anderson PH et al (2010) Osteoclastic metabolism of 25(OH)-vitamin D3: a potential mechanism for optimization of bone resorption. Endocrinology 151:4613–4625PubMedCrossRef Kogawa M, Findlay DM, Anderson PH et al (2010) Osteoclastic metabolism of 25(OH)-vitamin D3: a potential mechanism for optimization of bone resorption. Endocrinology 151:4613–4625PubMedCrossRef
19.
go back to reference Kogawa M, Anderson PH, Findlay DM, Morris HA, Atkins GJ (2010) The metabolism of 25-(OH)vitamin D3 by osteoclasts and their precursors regulates the differentiation of osteoclasts. J Steroid Biochem Mol Biol 121:277–280PubMedCrossRef Kogawa M, Anderson PH, Findlay DM, Morris HA, Atkins GJ (2010) The metabolism of 25-(OH)vitamin D3 by osteoclasts and their precursors regulates the differentiation of osteoclasts. J Steroid Biochem Mol Biol 121:277–280PubMedCrossRef
20.
go back to reference Itonaga I, Sabokbar A, Neale SD, Athanasou NA (1999) 1,25-Dihydroxyvitamin D(3) and prostaglandin E(2) act directly on circulating human osteoclast precursors. Biochem Biophys Res Commun 264:590–595PubMedCrossRef Itonaga I, Sabokbar A, Neale SD, Athanasou NA (1999) 1,25-Dihydroxyvitamin D(3) and prostaglandin E(2) act directly on circulating human osteoclast precursors. Biochem Biophys Res Commun 264:590–595PubMedCrossRef
21.
go back to reference Fugier-Vivier I, Servet-Delprat C, Rivailler P, Rissoan MC, Liu YJ, Rabourdin-Combe C (1997) Measles virus suppresses cell-mediated immunity by interfering with the survival and functions of dendritic and T cells. J Exp Med 186:813–823PubMedCentralPubMedCrossRef Fugier-Vivier I, Servet-Delprat C, Rivailler P, Rissoan MC, Liu YJ, Rabourdin-Combe C (1997) Measles virus suppresses cell-mediated immunity by interfering with the survival and functions of dendritic and T cells. J Exp Med 186:813–823PubMedCentralPubMedCrossRef
22.
go back to reference Rivollier A, Mazzorana M, Tebib J et al (2004) Immature dendritic cell transdifferentiation into osteoclasts: a novel pathway sustained by the rheumatoid arthritis microenvironment. Blood 104:4029–4037PubMedCrossRef Rivollier A, Mazzorana M, Tebib J et al (2004) Immature dendritic cell transdifferentiation into osteoclasts: a novel pathway sustained by the rheumatoid arthritis microenvironment. Blood 104:4029–4037PubMedCrossRef
23.
go back to reference Harre U, Georgess D, Bang H et al (2012) Induction of osteoclastogenesis and bone loss by human autoantibodies against citrullinated vimentin. J Clin Invest 122:1791–1802PubMedCentralPubMedCrossRef Harre U, Georgess D, Bang H et al (2012) Induction of osteoclastogenesis and bone loss by human autoantibodies against citrullinated vimentin. J Clin Invest 122:1791–1802PubMedCentralPubMedCrossRef
25.
go back to reference Hayashibara T, Hiraga T, Sugita A et al (2007) Regulation of osteoclast differentiation and function by phosphate: potential role of osteoclasts in the skeletal abnormalities in hypophosphatemic conditions. J Bone Miner Res 22:1743–1751PubMedCrossRef Hayashibara T, Hiraga T, Sugita A et al (2007) Regulation of osteoclast differentiation and function by phosphate: potential role of osteoclasts in the skeletal abnormalities in hypophosphatemic conditions. J Bone Miner Res 22:1743–1751PubMedCrossRef
26.
go back to reference Hollberg K, Marsell R, Norgård M, Larsson T, Jonsson KB, Andersson G (2008) Osteoclast polarization is not required for degradation of bone matrix in rachitic FGF23 transgenic mice. Bone 42:1111–1121PubMedCrossRef Hollberg K, Marsell R, Norgård M, Larsson T, Jonsson KB, Andersson G (2008) Osteoclast polarization is not required for degradation of bone matrix in rachitic FGF23 transgenic mice. Bone 42:1111–1121PubMedCrossRef
27.
go back to reference Chen IP, Wang L, Jiang X, Aguila HL, Reichenberger EJ (2011) A Phe377del mutation in ANK leads to impaired osteoblastogenesis and osteoclastogenesis in a mouse model for craniometaphyseal dysplasia (CMD). Hum Mol Genet 20:948–961PubMedCentralPubMedCrossRef Chen IP, Wang L, Jiang X, Aguila HL, Reichenberger EJ (2011) A Phe377del mutation in ANK leads to impaired osteoblastogenesis and osteoclastogenesis in a mouse model for craniometaphyseal dysplasia (CMD). Hum Mol Genet 20:948–961PubMedCentralPubMedCrossRef
28.
go back to reference Wang N, Robaye B, Gossiel F, Boeynaems JM, Gartland A (2014) The P2Y13 receptor regulates phosphate metabolism and FGF-23 secretion with effects on skeletal development. FASEB J 28:2249–2259PubMedCrossRef Wang N, Robaye B, Gossiel F, Boeynaems JM, Gartland A (2014) The P2Y13 receptor regulates phosphate metabolism and FGF-23 secretion with effects on skeletal development. FASEB J 28:2249–2259PubMedCrossRef
29.
go back to reference Hu L, Andersson G, Jonsson KB, Melhus H, Lind T (2013) Adamts1 is highly induced in rachitic bones of FGF23 transgenic mice and participates in degradation of non-mineralized bone matrix collagen. Biochem Biophys Res Commun 430:901–906PubMedCrossRef Hu L, Andersson G, Jonsson KB, Melhus H, Lind T (2013) Adamts1 is highly induced in rachitic bones of FGF23 transgenic mice and participates in degradation of non-mineralized bone matrix collagen. Biochem Biophys Res Commun 430:901–906PubMedCrossRef
30.
go back to reference Gutiérrez OM, Mannstadt M, Isakova T et al (2008) Fibroblast growth factor 23 and mortality among patients undergoing hemodialysis. N Engl J Med 359:584–592PubMedCentralPubMedCrossRef Gutiérrez OM, Mannstadt M, Isakova T et al (2008) Fibroblast growth factor 23 and mortality among patients undergoing hemodialysis. N Engl J Med 359:584–592PubMedCentralPubMedCrossRef
31.
go back to reference Wolf M, Molnar MZ, Amaral AP et al (2011) Elevated fibroblast growth factor 23 is a risk factor for kidney transplant loss and mortality. J Am Soc Nephrol 22:956–966PubMedCentralPubMedCrossRef Wolf M, Molnar MZ, Amaral AP et al (2011) Elevated fibroblast growth factor 23 is a risk factor for kidney transplant loss and mortality. J Am Soc Nephrol 22:956–966PubMedCentralPubMedCrossRef
32.
go back to reference Pereira RC, Juppner H, Azucena-Serrano CE, Yadin O, Salusky IB, Wesseling-Perry K (2009) Patterns of FGF-23, DMP1, and MEPE expression in patients with chronic kidney disease. Bone 45:1161–1168PubMedCentralPubMedCrossRef Pereira RC, Juppner H, Azucena-Serrano CE, Yadin O, Salusky IB, Wesseling-Perry K (2009) Patterns of FGF-23, DMP1, and MEPE expression in patients with chronic kidney disease. Bone 45:1161–1168PubMedCentralPubMedCrossRef
33.
go back to reference Shalhoub V, Shatzen EM, Ward SC et al (2012) FGF23 neutralization improves chronic kidney disease-associated hyperparathyroidism yet increases mortality. J Clin Invest 122:2543–2553PubMedCentralPubMedCrossRef Shalhoub V, Shatzen EM, Ward SC et al (2012) FGF23 neutralization improves chronic kidney disease-associated hyperparathyroidism yet increases mortality. J Clin Invest 122:2543–2553PubMedCentralPubMedCrossRef
Metadata
Title
Biphasic Effects of Vitamin D and FGF23 on Human Osteoclast Biology
Authors
Lise Allard
Nathalie Demoncheaux
Irma Machuca-Gayet
Dan Georgess
Fabienne Coury-Lucas
Pierre Jurdic
Justine Bacchetta
Publication date
01-07-2015
Publisher
Springer US
Published in
Calcified Tissue International / Issue 1/2015
Print ISSN: 0171-967X
Electronic ISSN: 1432-0827
DOI
https://doi.org/10.1007/s00223-015-0013-6

Other articles of this Issue 1/2015

Calcified Tissue International 1/2015 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.