Phosphate-dependent FGF23 secretion is modulated by PiT2/Slc20a2

Molecular Metabolism

Volumn 11, Issue , 2018, Pages 197-204

  Bon, Nina ^a   Frangi, Giulia ^a   Sourice, Sophie ^a   Guicheux, Jérôme ^a,b   Beck Cormier, Sarah ^a   Beck, Laurent ^a  

^a UNIVERSITÉ DE NANTES   (France)

^b NANTES UNIVERSITY HOSPITAL   (France)

Author keywords

Bone; FGF23 secretion; Phosphate sensing; PiT1 Slc20a1; PiT2 Slc20a2

Indexed keywords

FIBROBLAST GROWTH FACTOR 23; KLOTHO PROTEIN; PHOSPHATE; PROTEIN PIT1; PROTEIN PIT2; SODIUM PHOSPHATE COTRANSPORTER; UNCLASSIFIED DRUG; DMP1 PROTEIN, MOUSE; FIBROBLAST GROWTH FACTOR; SCLEROPROTEIN; SLC20A1 PROTEIN, MOUSE; SODIUM PHOSPHATE COTRANSPORTER 3;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORTICAL BONE; DIET; EX VIVO STUDY; GENE DELETION; GENE EXPRESSION; IN VIVO STUDY; KIDNEY; MOUSE; NONHUMAN; OSTEOCYTE; PHOSPHATE BLOOD LEVEL; PIT1 GENE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN SECRETION; ANIMAL; BLOOD; C57BL MOUSE; GENETICS; METABOLISM; SIGNAL TRANSDUCTION;

ANIMALS; EXTRACELLULAR MATRIX PROTEINS; FIBROBLAST GROWTH FACTORS; KIDNEY; MICE; MICE, INBRED C57BL; OSTEOCYTES; PHOSPHATES; SIGNAL TRANSDUCTION; SODIUM-PHOSPHATE COTRANSPORTER PROTEINS, TYPE III;

EID: 85044943802     PISSN: None     EISSN: 22128778     Source Type: Journal    
DOI: 10.1016/j.molmet.2018.02.007     Document Type: Article

References (35)

1. Kawai, M., Kinoshita, S., Ozono, K., Michigami, T., Inorganic phosphate activates the AKT/mTORC1 pathway and shortens the life span of an α-klotho-deficient model. Journal of the American Society of Nephrology: JASN 27:9 (2016), 2810–2824, 10.1681/ASN.2015040446.
2. Erben, R.G., Update on FGF23 and Klotho signaling. Molecular and Cellular Endocrinology 432:C (2016), 56–65, 10.1016/j.mce.2016.05.008.
3. Razzaque, M.S., Phosphate toxicity: new insights into an old problem. Clinical Science (London, England: 1979) 120:3 (2011), 91–97, 10.1042/CS20100377.
4. Lau, W.L., Pai, A., Moe, S.M., Giachelli, C.M., Direct effects of phosphate on vascular cell function. Advances in Chronic Kidney Disease 18:2 (2011), 105–112, 10.1053/j.ackd.2010.12.002.
5. Martin, A., Liu, S., David, V., Li, H., Karydis, A., Feng, J.Q., et al. Bone proteins PHEX and DMP1 regulate fibroblastic growth factor Fgf23 expression in osteocytes through a common pathway involving FGF receptor (FGFR) signaling. The FASEB Journal 25:8 (2011), 2551–2562, 10.1096/fj.10-177816.
6. Christov, M., Jüppner, H., Insights from genetic disorders of phosphate homeostasis. Seminars in Nephrology 33:2 (2013), 143–157, 10.1016/j.semnephrol.2012.12.015.
7. Xiao, Z., Huang, J., Cao, L., Liang, Y., Han, X., Quarles, L.D., Osteocyte-specific deletion of Fgfr1 suppresses FGF23. PLoS One, 9(8), 2014, e104154, 10.1371/journal.pone.0104154.t003.
8. Wolf, M., White, K.E., Coupling fibroblast growth factor 23 production and cleavage. Current Opinion in Nephrology and Hypertension 23:4 (2014), 411–419, 10.1097/01.mnh.0000447020.74593.6f.
9. David, V., Martin, A., Isakova, T., Spaulding, C., Qi, L., Ramirez, V., et al. Inflammation and functional iron deficiency regulate fibroblast growth factor 23 production. Kidney International, 2015, 1–12, 10.1038/ki.2015.290.
10. Ito, N., Wijenayaka, A.R., Prideaux, M., Kogawa, M., Ormsby, R.T., Evdokiou, A., et al. Regulation of FGF23 expression in IDG-SW3 osteocytes and human bone by pro-inflammatory stimuli. Molecular and Cellular Endocrinology 399:C (2015), 208–218, 10.1016/j.mce.2014.10.007.
11. Tagliabracci, V.S., Engel, J.L., Wiley, S.E., Xiao, J., Gonzalez, D.J., Nidumanda Appaiah, H., et al. Dynamic regulation of FGF23 by Fam20C phosphorylation, GalNAc-T3 glycosylation, and furin proteolysis. Proceedings of the National Academy of Sciences of the United States of America 111:15 (2014), 5520–5525, 10.1073/pnas.1402218111.
12. Martin, A., David, V., Quarles, L.D., Regulation and function of the FGF23/klotho endocrine pathways. Physiological Reviews 92:1 (2012), 131–155, 10.1152/physrev.00002.2011.
13. Ferrari, S.L., Bonjour, J.P., Rizzoli, R., Fibroblast growth factor-23 relationship to dietary phosphate and renal phosphate handling in healthy young men. The Journal of Clinical Endocrinology and Metabolism 90:3 (2005), 1519–1524, 10.1210/jc.2004-1039.
14. Burnett, S.A.M., Gunawardene, S.C., Bringhurst, F.R., Jüppner, H., Lee, H., Finkelstein, J.S., Regulation of C-terminal and intact FGF-23 by dietary phosphate in men and women. Journal of Bone and Mineral Research 21:8 (2006), 1187–1196, 10.1359/jbmr.060507.
15. Scanni, R., vonRotz, M., Jehle, S., Hulter, H.N., Krapf, R., The human response to acute enteral and parenteral phosphate loads. Journal of the American Society of Nephrology: JASN 25:12 (2014), 2730–2739, 10.1681/ASN.2013101076.
16. Saito, H., Maeda, A., Ohtomo, S.I., Hirata, M., Kusano, K., Kato, S., et al. Circulating FGF-23 is regulated by 1alpha,25-dihydroxyvitamin D3 and phosphorus in vivo. The Journal of Biological Chemistry 280:4 (2005), 2543–2549, 10.1074/jbc.M408903200.
17. Perwad, F., Azam, N., Zhang, M.Y.H., Yamashita, T., Tenenhouse, H.S., Portale, A.A., Dietary and serum phosphorus regulate fibroblast growth factor 23 expression and 1,25-dihydroxyvitamin D metabolism in mice. Endocrinology 146:12 (2005), 5358–5364, 10.1210/en.2005-0777.
18. Khoshniat, S., Bourgine, A., Julien, M., Weiss, P., Guicheux, J., Beck, L., The emergence of phosphate as a specific signaling molecule in bone and other cell types in mammals. Cellular and Molecular Life Sciences: CMLS 68:2 (2011), 205–218, 10.1007/s00018-010-0527-z.
19. Michigami, T., Extracellular phosphate as a signaling molecule. Contributions to Nephrology 180 (2013), 14–24, 10.1159/000346776.
20. Bergwitz, C., Jüppner, H., Phosphate sensing. Advances in Chronic Kidney Disease 18:2 (2011), 132–144, 10.1053/j.ackd.2011.01.004.
21. Bon, N., Couasnay, G., Bourgine, A., Sourice, S., Beck-Cormier, S., Guicheux, J., et al. Phosphate (Pi)-regulated heterodimerization of the high-affinity sodium-dependent Pi transporters PiT1/Slc20a1 and PiT2/Slc20a2 underlies extracellular Pi sensing independently of Pi uptake. The Journal of Biological Chemistry, 2017, 10.1074/jbc.M117.807339.
22. Beck, L., Leroy, C., Beck-Cormier, S., Forand, A., Salaün, C., Paris, N., et al. The phosphate transporter PiT1 (Slc20a1) revealed as a new essential gene for mouse liver development. PLoS One, 5(2), 2010, e9148, 10.1371/journal.pone.0009148.
23. Lu, Y., Xie, Y., Zhang, S., Dusevich, V., Bonewald, L.F., Feng, J.Q., DMP1-targeted Cre expression in odontoblasts and osteocytes. Journal of Dental Research 86:4 (2007), 320–325.
24. Skarnes, W.C., Rosen, B., West, A.P., Koutsourakis, M., Bushell, W., Iyer, V., et al. A conditional knockout resource for the genome-wide study of mouse gene function. Nature 474:7351 (2011), 337–342, 10.1038/nature10163.
25. Pfaffl, M.W., A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research, 29(9), 2001, e45.
26. Giovannini, D., Touhami, J., Charnet, P., Sitbon, M., Battini, J.-L., Inorganic phosphate export by the retrovirus receptor XPR1 in metazoans. Cell Reports 3:6 (2013), 1866–1873, 10.1016/j.celrep.2013.05.035.
27. Nishida, Y., Taketani, Y., Yamanaka-Okumura, H., Imamura, F., Taniguchi, A., Sato, T., et al. Acute effect of oral phosphate loading on serum fibroblast growth factor 23 levels in healthy men. Kidney International 70:12 (2006), 2141–2147, 10.1038/sj.ki.5002000.
28. Lim, J., Burclaff, J., He, G., Mills, J.C., Long, F., Unintended targeting of Dmp1-Cre reveals a critical role for Bmpr1a signaling in the gastrointestinal mesenchyme of adult mice. Bone Research, 5, 2017, 16049, 10.1038/boneres.2016.49.
29. Smith, R.C., O'Bryan, L.M., Farrow, E.G., Summers, L.J., Clinkenbeard, E.L., Roberts, J.L., et al. Circulating αKlotho influences phosphate handling by controlling FGF23 production. Journal of Clinical Investigation 122:12 (2012), 4710–4715, 10.1172/JCI64986DS1.
30. Eren, M., Place, A.T., Thomas, P.M., Flevaris, P., Miyata, T., Vaughan, D.E., PAI-1 is a critical regulator of FGF23 homeostasis. Science Advances, 3(9), 2017, e1603259, 10.1126/sciadv.1603259.
31. Ma, X.-X., Li, X., Yi, P., Wang, C., Weng, J., Zhang, L., et al. PiT2 regulates neuronal outgrowththrough interaction withmicrotubule-associated protein 1B. Scientific Reports, 2017, 1–13, 10.1038/s41598-017-17953-3.
32. Forand, A., Koumakis, E., Rousseau, A., Sassier, Y., Journe, C., Merlin, J.-F., et al. Disruption of the phosphate transporter Pit1 in hepatocytes improves glucose metabolism and insulin signaling by modulating the USP7/IRS1 interaction. Cell Reports, 17(7), 2016, 1905, 10.1016/j.celrep.2016.10.039.
33. Isakova, T., Barchi-Chung, A., Enfield, G., Smith, K., Vargas, G., Houston, J., et al. Effects of dietary phosphate restriction and phosphate binders on FGF23 levels in CKD. Clinical Journal of the American Society of Nephrology 8:6 (2013), 1009–1018, 10.2215/CJN.09250912.
34. Block, G.A., Wheeler, D.C., Persky, M.S., Kestenbaum, B., Ketteler, M., Spiegel, D.M., et al. Effects of phosphate binders in moderate CKD. Journal of the American Society of Nephrology: JASN 23:8 (2012), 1407–1415, 10.1681/ASN.2012030223.
35. David, V., Francis, C., Babitt, J.L., Ironing out the cross talk between FGF23 and inflammation. AJP: Renal Physiology 312:1 (2017), F1–F8, 10.1152/ajprenal.00359.2016.