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Expression and function of Slc34 sodium–phosphate co-transporters in skeleton and teeth

  • Laurent Beck
Invited Review
  • 42 Downloads

Abstract

Under normal physiological condition, the biomineralization process is limited to skeletal tissues and teeth and occurs throughout the individual’s life. Biomineralization is an actively regulated process involving the progressive mineralization of the extracellular matrix secreted by osteoblasts in bone or odontoblasts and ameloblasts in tooth. Although the detailed molecular mechanisms underlying the formation of calcium–phosphate apatite crystals are still debated, it is suggested that calcium and phosphate may need to be transported across the membrane of the mineralizing cell, suggesting a pivotal role of phosphate transporters in bone and tooth mineralization. In this context, this short review describes the current knowledge on the role of Slc34 Na+–phosphate transporters in skeletal and tooth mineralization.

Keywords

NaPi-II Biomineralization Bone Cartilage Tooth Matrix vesicles 

Notes

Acknowledgments

I would like to acknowledge Céline Gaucher (Université Paris Descartes) and Laure Merametdjian (Université de Nantes) for their work on phosphate transporters in the tooth and Sarah Beck-Cormier, Annabelle Bourgine, Sophie Sourice, and Nina Bon (Université de Nantes) and Greig Couasnay (Baylor College of Medicine) for their work on Slc20a1 and Slc20a2 phosphate transporters in the skeleton.

Funding information

This work was supported by grants from Institut National de la Santé et de la Recherche Médicale (INSERM), Région des Pays de la Loire (grants “Nouvelle Equipe/Nouvelle Thématique”, “Senseo,” and “Adipos”), and Institut Français sur la Recherche en Odontologie (IFRO).

References

  1. 1.
    Adams C, Mansfield K, Perlot R, Shapiro I (2001) Matrix regulation of skeletal cell apoptosis. Role of calcium and phosphate ions. J Biol Chem 276:20316–20322.  https://doi.org/10.1074/jbc.M006492200 CrossRefPubMedGoogle Scholar
  2. 2.
    Albano G, Moor M, Dolder S, Siegrist M, Wagner CA, Biber J, Hernando N, Hofstetter W, Bonny O, Fuster DG (2015) Sodium-dependent phosphate transporters in osteoclast differentiation and function. PLoS One 10:e0125104.  https://doi.org/10.1371/journal.pone.0125104.g006 CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Althoff J, Quint P, Krefting ER, Höhling HJ (1982) Morphological studies on the epiphyseal growth plate combined with biochemical and X-ray microprobe analyses. Histochemistry 74:541–552CrossRefPubMedGoogle Scholar
  4. 4.
    An YH, Martin KL (2003) Handbook of histology methods for bone and cartilage. Springer Science & Business MediaGoogle Scholar
  5. 5.
    Arispe N, Rojas E, Genge BR, Wu LN, Wuthier RE (1996) Similarity in calcium channel activity of annexin V and matrix vesicles in planar lipid bilayers. Biophysj 71:1764–1775.  https://doi.org/10.1016/S0006-3495(96)79377-3 CrossRefGoogle Scholar
  6. 6.
    Beck L, Karaplis AC, Amizuka N, Hewson AS, Ozawa H, Tenenhouse HS (1998) Targeted inactivation of Npt2 in mice leads to severe renal phosphate wasting, hypercalciuria, and skeletal abnormalities. Proc Natl Acad Sci U S A 95:5372–5377.  https://doi.org/10.1073/pnas.95.9.5372 CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Bergwitz C, Jüppner H (2010) Regulation of phosphate homeostasis by PTH, vitamin D, and FGF23. Annu Rev Med 61:91–104.  https://doi.org/10.1146/annurev.med.051308.111339 CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Bergwitz C, Roslin NM, Tieder M, Loredo-Osti JC, Bastepe M, Abu-Zahra H, Frappier D, Burkett K, Carpenter TO, Anderson D (2006) SLC34A3 mutations in patients with hereditary hypophosphatemic rickets with hypercalciuria predict a key role for the sodium-phosphate cotransporter NaP i-IIc in maintaining phosphate homeostasis. Am J Hum Genet 78:179–192.  https://doi.org/10.1086/499409 CrossRefPubMedGoogle Scholar
  9. 9.
    Berner YN, Shike M (1988) Consequences of phosphate imbalance. Annu Rev Nutr 8:121–148.  https://doi.org/10.1146/annurev.nu.08.070188.001005 CrossRefPubMedGoogle Scholar
  10. 10.
    Bindels RJ, van den Broek LA, van Os CH (1987) Effect of pH on the kinetics of Na+-dependent phosphate transport in rat renal brush-border membranes. Biochim Biophys Acta 897:83–92.  https://doi.org/10.1016/0005-2736(87)90317-8 CrossRefPubMedGoogle Scholar
  11. 11.
    Bockman RS (2010) First it’s rickets, then it’s not the sodium-phosphate transporter 2a knockout mystery. Endocrinology 151:4599–4601.  https://doi.org/10.1210/en.2010-0818 CrossRefPubMedGoogle Scholar
  12. 12.
    Bolean M, Simão AMS, Barioni MB, Favarin BZ, Sebinelli HG, Veschi EA, Janku TAB, Bottini M, Hoylaerts MF, Itri R, Millán JL, Pietro Ciancaglini (2017) Biophysical aspects of biomineralization. 1–14.  https://doi.org/10.1007/s12551-017-0315-1 CrossRefGoogle Scholar
  13. 13.
    Bonewald LF (2010) The amazing osteocyte. J Bone Miner Res 26:229–238.  https://doi.org/10.1002/jbmr.320 CrossRefPubMedCentralGoogle Scholar
  14. 14.
    Boonrungsiman S, Gentleman E, Carzaniga R, Evans ND, McComb DW, Porter AE, Stevens MM (2012) The role of intracellular calcium phosphate in osteoblast-mediated bone apatite formation. Proc Natl Acad Sci U S A 109:14170–14175.  https://doi.org/10.1073/pnas.1208916109 CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Bottini M, Mebarek S, Anderson KL, Strzelecka-Kiliszek A, Bozycki L, Simão AMS, Bolean M, Pietro Ciancaglini, Pikula JB, Pikula S, Magne D, Volkmann N, Hanein D, Millán JL, Buchet R (2017) Accepted manuscript. 1–50.  https://doi.org/10.1016/j.bbagen.2017.11.005
  16. 16.
    Bourgine A, Beck L, Khoshniat S, Wauquier F, Oliver L, Hue E, Alliot-Licht B, Weiss P, Guicheux J, Wittrant Y (2010) Inorganic phosphate stimulates apoptosis in murine MO6-G3 odontoblast-like cells. Arch Oral Biol 56:977–983.  https://doi.org/10.1016/j.archoralbio.2011.03.001 CrossRefGoogle Scholar
  17. 17.
    Bourgine A, Pilet P, Diouani S, Sourice S, Lesoeur J, Beck-Cormier S, Khoshniat S, Weiss P, Friedlander G, Guicheux J, Beck L (2013) Mice with hypomorphic expression of the sodium-phosphate cotransporter PiT1/Slc20a1 have an unexpected normal bone mineralization. PLoS One 8:e65979.  https://doi.org/10.1371/journal.pone.0065979 CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Boyde A, Shapiro IM (1980) Energy dispersive X-ray elemental analysis of isolated epiphyseal growth plate chondrocyte fragments. Histochemistry 69:85–94CrossRefPubMedGoogle Scholar
  19. 19.
    Bronckers ALJJ, Lyaruu D, Jalali R, Medina JF, Zandieh-Doulabi B, DenBesten PK (2015) Ameloblast modulation and transport of Cl−, Na+, and K+ during amelogenesis. J Dent Res 94:1740–1747.  https://doi.org/10.1177/0022034514556708 CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Corut A, Senyigit A, Ugur SA, Altin S, Ozcelik U, Calisir H, Yildirim Z, Gocmen A, Tolun A (2006) Mutations in SLC34A2 cause pulmonary alveolar microlithiasis and are possibly associated with testicular microlithiasis. Am J Hum Genet 79:650–656.  https://doi.org/10.1086/508263 CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Couasnay G, Bon N, Devignes C-S, Sourice S, Bianchi A, Véziers J, Weiss P, Elefteriou F, Provot S, Guicheux J, Beck-Cormier S, Beck L (2018) PiT1/Slc20a1 is required for endoplasmic reticulum homeostasis, chondrocyte survival and skeletal development. J Bone Miner Res.  https://doi.org/10.1002/jbmr.3609
  22. 22.
    Demir K, Yildiz M, Bahat H, Goldman M, Hassan N, Tzur S, Ofir A, Magen D (2017) Clinical heterogeneity and phenotypic expansion of NaPi-IIa-associated disease. J Clin Endocrinol Metab 102:4604–4614.  https://doi.org/10.1210/jc.2017-01592 CrossRefPubMedGoogle Scholar
  23. 23.
    Diez-Roux G, Banfi S, Sultan M, Geffers L, Anand S, Rozado D, Magen A, Canidio E, Pagani M, Peluso I, Lin-Marq N, Koch M, Bilio M, Cantiello I, Verde R, De Masi C, Bianchi SA, Cicchini J, Perroud E, Mehmeti S, Dagand E, Schrinner S, Nürnberger A, Schmidt K, Metz K, Zwingmann C, Brieske N, Springer C, Hernandez AM, Herzog S, Grabbe F, Sieverding C, Fischer B, Schrader K, Brockmeyer M, Dettmer S, Helbig C, Alunni V, Battaini M-A, Mura C, Henrichsen CN, Garcia-Lopez R, Echevarria D, Puelles E, Garcia-Calero E, Kruse S, Uhr M, Kauck C, Feng G, Milyaev N, Ong CK, Kumar L, Lam M, Semple CA, Gyenesei A, Mundlos S, Radelof U, Lehrach H, Sarmientos P, Reymond A, Davidson DR, Dollé P, Antonarakis SE, Yaspo M-L, Martinez S, Baldock RA, Eichele G, Ballabio A (2011) A high-resolution anatomical atlas of the transcriptome in the mouse embryo. PLoS Biol 9:e1000582.  https://doi.org/10.1371/journal.pbio.1000582.s018 CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Dinour D, Davidovits M, Ganon L, Ruminska J, Forster IC, Hernando N, Eyal E, Holtzman EJ, Wagner CA (2016) Loss of function of NaPiIIa causes nephrocalcinosis and possibly kidney insufficiency. Pediatr Nephrol 31:1–9.  https://doi.org/10.1007/s00467-016-3443-0 CrossRefGoogle Scholar
  25. 25.
    Fearn A, Allison B, Rice SJ, Edwards N, Halbritter J, Bourgeois S, Pastor-Arroyo EM, Hildebrandt F, Tasic V, Wagner CA, Hernando N, Sayer JA, Werner A (2018) Clinical, biochemical, and pathophysiological analysis of SLC34A1mutations. Physiol Rep 6:e13715.  https://doi.org/10.1016/j.ajhg.2012.10.015 CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Feild JA, Zhang L, Brun KA, Brooks DP, Edwards RM (1999) Cloning and functional characterization of a sodium-dependent phosphate transporter expressed in human lung and small intestine. Biochem Biophys Res Commun 258:578–582.  https://doi.org/10.1006/bbrc.1999.0666 CrossRefPubMedGoogle Scholar
  27. 27.
    Frei P, Gao B, Hagenbuch B, Mate A, Biber J, Murer H, Meier PJ, Stieger B (2005) Identification and localization of sodium-phosphate cotransporters in hepatocytes and cholangiocytes of rat liver. Am J Physiol Gastrointest Liver Physiol 288:G771–G778.  https://doi.org/10.1152/ajpgi.00272.2004 CrossRefPubMedGoogle Scholar
  28. 28.
    Glimcher MJ (1984) Recent studies of the mineral phase in bone and its possible linkage to the organic matrix by protein-bound phosphate bonds. Philos Trans R Soc Lond Ser B Biol Sci 304:479–508CrossRefGoogle Scholar
  29. 29.
    Gupta A, Miyauchi A, Fujimori A, Hruska KA (1996) Phosphate transport in osteoclasts: a functional and immunochemical characterization. Kidney Int 49:968–974CrossRefPubMedGoogle Scholar
  30. 30.
    Gupta A, Guo XL, Alvarez UM, Hruska KA (1997) Regulation of sodium-dependent phosphate transport in osteoclasts. J Clin Invest 100:538–549.  https://doi.org/10.1172/JCI119563 CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Gupta A, Tenenhouse HS, Hoag HM, Wang D, Khadeer MA, Namba N, Feng X, Hruska KA (2001) Identification of the type II Na(+)-Pi cotransporter (Npt2) in the osteoclast and the skeletal phenotype of Npt2−/− mice. Bone 29:467–476CrossRefPubMedGoogle Scholar
  32. 32.
    Hilfiker H, Hattenhauer O, Traebert M, Forster I, Murer H, Biber J (1998) Characterization of a murine type II sodium-phosphate cotransporter expressed in mammalian small intestine. Proc Natl Acad Sci U S A 95:14564–14569.  https://doi.org/10.1073/pnas.95.24.14564 CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Huqun IS, Miyazawa H, Ishii K, Uchiyama B, Ishida T, Tanaka S, Tazawa R, Fukuyama S, Tanaka T, Nagai Y, Yokote A, Takahashi H, Fukushima T, Kobayashi K, Chiba H, Nagata M, Sakamoto S, Nakata K, Takebayashi Y, Shimizu Y, Kaneko K, Shimizu M, Kanazawa M, Abe S, Inoue Y, Takenoshita S, Yoshimura K, Kudo K, Tachibana T, Nukiwa T, Hagiwara K (2006) Mutations in the SLC34A2 gene are associated with pulmonary alveolar Microlithiasis. Am J Respir Crit Care Med 175:263–268.  https://doi.org/10.1164/rccm.200609-1274OC CrossRefPubMedGoogle Scholar
  34. 34.
    Ichikawa S, Sorenson AH, Imel EA, Friedman NE, Gertner JM, Econs MJ (2006) Intronic deletions in the SLC34A3 gene cause hereditary hypophosphatemic rickets with hypercalciuria. J Clin Endocrinol Metab 91:4022–4027.  https://doi.org/10.1210/jc.2005-2840 CrossRefPubMedGoogle Scholar
  35. 35.
    Ito M, Matsuka N, Izuka M, Haito S, Sakai Y, Nakamura R, Segawa H, Kuwahata M, Yamamoto H, Pike WJ, Miyamoto K-I (2005) Characterization of inorganic phosphate transport in osteoclast-like cells. Am J Physiol Cell Physiol 288:C921–C931.  https://doi.org/10.1152/ajpcell.00412.2004 CrossRefPubMedGoogle Scholar
  36. 36.
    Kakuta S, Golub E (1985) Morphochemical analysis of phosphorus pools in calcifying cartilage. Calcif Tissue Int 37:293–299CrossRefPubMedGoogle Scholar
  37. 37.
    Kenny J, Lees MM, Drury S, Barnicoat A, Van’t Hoff W, Palmer R, Morrogh D, Waters JJ, Lench NJ, Bockenhauer D (2011) Sotos syndrome, infantile hypercalcemia, and nephrocalcinosis: a contiguous gene syndrome. Pediatr Nephrol 26:1331–1334.  https://doi.org/10.1007/s00467-011-1884-z CrossRefPubMedGoogle Scholar
  38. 38.
    Khadeer MA, Tang Z, Tenenhouse HS, Eiden MV, Murer H, Hernando N, Weinman EJ, Chellaiah MA, Gupta A (2003) Na+-dependent phosphate transporters in the murine osteoclast: cellular distribution and protein interactions. Am J Physiol Cell Physiol 284:C1633–C1644.  https://doi.org/10.1152/ajpcell.00580.2002 CrossRefPubMedGoogle Scholar
  39. 39.
    Kirsch T (2012) Biomineralization—an active or passive process? Connect Tissue Res 53:438–445.  https://doi.org/10.3109/03008207.2012.730081 CrossRefPubMedGoogle Scholar
  40. 40.
    Kirsch T, Nah HD, Shapiro IM, Pacifici M (1997) Regulated production of mineralization-competent matrix vesicles in hypertrophic chondrocytes. J Cell Biol 137:1149–1160.  https://doi.org/10.1083/jcb.137.5.1149 CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Kirsch T, Harrison G, Golub EE, Nah HD (2000) The roles of annexins and types II and X collagen in matrix vesicle-mediated mineralization of growth plate cartilage. J Biol Chem 275:35577–35583.  https://doi.org/10.1074/jbc.M005648200 CrossRefPubMedGoogle Scholar
  42. 42.
    Ko FC, Martins JS, Reddy P, Bragdon B, Hussein AI, Gerstenfeld LC, Demay MB (2016) Acute phosphate restriction impairs bone formation and increases marrow adipose tissue in growing mice. J Bone Miner Res 31:2204–2214.  https://doi.org/10.1002/jbmr.275 CrossRefPubMedGoogle Scholar
  43. 43.
    Lacruz RS (2017) Enamel: molecular identity of its transepithelial ion transport system. Cell Calcium 65:1–7.  https://doi.org/10.1016/j.ceca.2017.03.006
  44. 44.
    Lacruz RS, Smith CE, Bringas P Jr, Chen Y-B, Smith SM, Snead ML, Kurtz I, Hacia JG, Hubbard MJ, Paine ML (2012) Identification of novel candidate genes involved in mineralization of dental enamel by genome-wide transcript profiling. J Cell Physiol 227:2264–2275.  https://doi.org/10.1177/0022034511398273 CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Lapointe J-Y, Tessier J, Paquette Y, Wallendorff B, Coady MJ, Pichette V, Bonnardeaux A (2006) NPT2a gene variation in calcium nephrolithiasis with renal phosphate leak. Kidney Int 69:2261–2267.  https://doi.org/10.1038/sj.ki.5000437 CrossRefPubMedGoogle Scholar
  46. 46.
    Lederer E, Miyamoto K-I (2012) Clinical consequences of mutations in sodium phosphate cotransporters. Clin J Am Soc Nephrol 7:1179–1187.  https://doi.org/10.2215/CJN.09090911 CrossRefPubMedGoogle Scholar
  47. 47.
    Lorenz-Depiereux B, Benet-Pagès A, Eckstein G, Tenenbaum-Rakover Y, Wagenstaller J, Tiosano D, Gershoni-Baruch R, Albers N, Lichtner P, Schnabel D, Hochberg Z, Strom TM (2006) Hereditary hypophosphatemic rickets with hypercalciuria is caused by mutations in the sodium-phosphate cotransporter gene SLC34A3. Am J Hum Genet 78:193–201.  https://doi.org/10.1086/499410 CrossRefPubMedGoogle Scholar
  48. 48.
    Lundquist P, Ritchie HH, Moore K, Lundgren T, Linde A (2002) Phosphate and calcium uptake by rat odontoblast-like MRPC-1 cells concomitant with mineralization. J Bone Miner Res 17:1801–1813.  https://doi.org/10.1359/jbmr.2002.17.10.1801 CrossRefPubMedGoogle Scholar
  49. 49.
    Lundquist P, Murer H, Biber J (2007) Type II Na+-Pi cotransporters in osteoblast mineral formation: regulation by inorganic phosphate. Cell Physiol Biochem 19:43–56.  https://doi.org/10.1159/000099191 CrossRefPubMedGoogle Scholar
  50. 50.
    Mackie EJ, Ahmed YA, Tatarczuch L, Chen KS, Mirams M (2008) Endochondral ossification: how cartilage is converted into bone in the developing skeleton. Int J Biochem Cell Biol 40:46–62.  https://doi.org/10.1016/j.biocel.2007.06.009 CrossRefPubMedGoogle Scholar
  51. 51.
    Magen D, Berger L, Coady MJ, Ilivitzki A, Militianu D, Tieder M, Selig S, Lapointe JY, Zelikovic I, Skorecki K (2010) A loss-of-function mutation in NaPi-IIa and renal Fanconi’s syndrome. N Engl J Med 362:1102–1109.  https://doi.org/10.1056/NEJMoa0905647 CrossRefPubMedGoogle Scholar
  52. 52.
    Magen D, Zelikovic I, Skorecki K (2010) Genetic disorders of renal phosphate transport. N Engl J Med 363:1774; author reply 1774–5–1775.  https://doi.org/10.1056/NEJMc1008407 CrossRefPubMedGoogle Scholar
  53. 53.
    Mahamid J, Sharir A, Addadi L, Weiner S (2008) Amorphous calcium phosphate is a major component of the forming fin bones of zebrafish: indications for an amorphous precursor phase. Proc Natl Acad Sci U S A 105:12748–12753.  https://doi.org/10.1073/pnas.0803354105 CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Mahamid J, Addadi L, Weiner S (2011) Crystallization pathways in bone. Cells Tissues Organs 194:92–97.  https://doi.org/10.1159/000324229 CrossRefPubMedGoogle Scholar
  55. 55.
    Mansfield K, Teixeira CC, Adams CS, Shapiro IM (2001) Phosphate ions mediate chondrocyte apoptosis through a plasma membrane transporter mechanism. Bone 28:1–8.  https://doi.org/10.1016/S8756-3282(00)00409-9 CrossRefPubMedGoogle Scholar
  56. 56.
    Merametdjian L, David A, Bon N, Couasnay G, Guicheux J, Gaucher C, Beck-Cormier S, Beck L (2016) Expression of phosphate transporters in optimized cell culture models for dental cells biomineralization. Bull Group Int Rech Sci Stomatol Odontol 53:e16PubMedGoogle Scholar
  57. 57.
    Merametdjian L, Beck-Cormier S, Bon N, Couasnay G, Sourice S, Guicheux J, Gaucher C, Beck L (2017) Expression of phosphate transporters during dental mineralization. J Dent Res 22034517729811:209–217.  https://doi.org/10.1177/0022034517729811 CrossRefGoogle Scholar
  58. 58.
    Millán JL (2013) The role of phosphatases in the initiation of skeletal mineralization. Calcif Tissue Int 93:299–306.  https://doi.org/10.1007/s00223-012-9672-8 CrossRefPubMedGoogle Scholar
  59. 59.
    Olsen BR, Reginato AM, Wang W (2000) Bone development. Annu Rev Cell Dev Biol 16:191–220.  https://doi.org/10.1146/annurev.cellbio.16.1.191 CrossRefPubMedGoogle Scholar
  60. 60.
    Onishi T, Okawa R, Ogawa T, Shintani S, Ooshima T (2007) Phex mutation causes the reduction of Npt2b mRNA in teeth. J Dent Res 86:158–162.  https://doi.org/10.1177/154405910708600210 CrossRefPubMedGoogle Scholar
  61. 61.
    Palmer G, Zhao J, Bonjour J, Hofstetter W, Caverzasio J (1999) In vivo expression of transcripts encoding the Glvr-1 phosphate transporter/retrovirus receptor during bone development. Bone 24:1–7CrossRefPubMedGoogle Scholar
  62. 62.
    Prié D, Huart V, Bakouh N, Planelles G, Dellis O, Gérard B, Hulin P, Benqué-Blanchet F, Silve C, Grandchamp B, Friedlander G (2002) Nephrolithiasis and osteoporosis associated with hypophosphatemia caused by mutations in the type 2a sodium–phosphate cotransporter. N Engl J Med 347:983–991.  https://doi.org/10.1056/NEJMoa020028 CrossRefPubMedGoogle Scholar
  63. 63.
    Quamme GA (1990) Effect of pH on Na(+)-dependent phosphate transport in renal outer cortical and outer medullary BBMV. Am J Phys 258:F356–F363.  https://doi.org/10.1152/ajprenal.1990.258.2.F356 CrossRefGoogle Scholar
  64. 64.
    Sabbagh Y, Carpenter TO, Demay MB (2005) Hypophosphatemia leads to rickets by impairing caspase-mediated apoptosis of hypertrophic chondrocytes. Proc Natl Acad Sci U S A 102:9637–9642.  https://doi.org/10.1073/pnas.0502249102 CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Sabbagh Y, O'Brien SP, Song W, Boulanger JH, Stockmann A, Arbeeny C, Schiavi SC (2009) Intestinal npt2b plays a major role in phosphate absorption and homeostasis. J Am Soc Nephrol 20:2348–2358.  https://doi.org/10.1681/ASN.2009050559 CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Sapir-Koren R, Livshits G (2011) Bone mineralization and regulation of phosphate homeostasis. IBMS BoneKEy 8:286–300.  https://doi.org/10.1138/20110516 CrossRefGoogle Scholar
  67. 67.
    Schlingmann KP, Ruminska J, Kaufmann M, Dursun I, Patti M, Kranz B, Pronicka E, Ciara E, Akcay T, Bulus D, Cornelissen EAM, Gawlik A, Sikora P, Patzer L, Galiano M, Boyadzhiev V, Dumic M, Vivante A, Kleta R, Dekel B, Levtchenko E, Bindels RJ, Rust S, Forster IC, Hernando N, Jones G, Wagner CA, Konrad M (2016) Autosomal-recessive mutations in SLC34A1 encoding sodium-phosphate cotransporter 2A cause idiopathic infantile hypercalcemia. J Am Soc Nephrol 27:604–614.  https://doi.org/10.1681/ASN.2014101025 CrossRefPubMedGoogle Scholar
  68. 68.
    Schmitz N, Laverty S, Kraus VB, Aigner T (2010) Basic methods in histopathology of joint tissues. Osteoarthr Cartil 18:S113–S116.  https://doi.org/10.1016/j.joca.2010.05.026 CrossRefPubMedGoogle Scholar
  69. 69.
    Segawa H, Aranami F, Kaneko I, Tomoe Y, Miyamoto K (2009) The roles of Na/Pi-II transporters in phosphate metabolism. Bone 45(Suppl 1):S2–S7.  https://doi.org/10.1016/j.bone.2009.02.003 CrossRefPubMedGoogle Scholar
  70. 70.
    Segawa H, Onitsuka A, Furutani J, Kaneko I, Aranami F, Matsumoto N, Tomoe Y, Kuwahata M, Ito M, Matsumoto M, Li M, Amizuka N, Miyamoto K-I (2009) Npt2a and Npt2c in mice play distinct and synergistic roles in inorganic phosphate metabolism and skeletal development. Am J Physiol Renal Physiol 297:F671–F678.  https://doi.org/10.1152/ajprenal.00156.2009 CrossRefPubMedGoogle Scholar
  71. 71.
    Segawa H, Onitsuka A, Kuwahata M, Hanabusa E, Furutani J, Kaneko I, Tomoe Y, Aranami F, Matsumoto N, Ito M, Matsumoto M, Li M, Amizuka N, Miyamoto K-I (2009) Type IIc sodium-dependent phosphate transporter regulates calcium metabolism. J Am Soc Nephrol 20:104–113.  https://doi.org/10.1681/ASN.2008020177 CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Segawa H, Shiozaki Y, Kaneko I, Miyamoto K-I (2015) The role of sodium-dependent phosphate transporter in phosphate homeostasis. J Nutr Sci Vitaminol 61(Suppl):S119–S121.  https://doi.org/10.3177/jnsv.61.S119 CrossRefPubMedGoogle Scholar
  73. 73.
    Shibasaki Y, Etoh N, Hayasaka M, Takahashi M-O, Kakitani M, Yamashita T, Tomizuka K, Hanaoka K (2009) Targeted deletion of the tybe IIb Na(+)-dependent Pi-co-transporter, NaPi-IIb, results in early embryonic lethality. Biochem Biophys Res Commun 381:482–486.  https://doi.org/10.1016/j.bbrc.2009.02.067 CrossRefPubMedGoogle Scholar
  74. 74.
    Simmer JP, Richardson AS, Hu Y-Y, Smith CE, Ching-Chun Hu J (2012) A post-classical theory of enamel biomineralization… and why we need one. Int J Oral Sci 4:129–134.  https://doi.org/10.1038/ijos.2012.59 CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Suzuki A, Ammann P, Nishiwaki-Yasuda K, Sekiguchi S, Asano S, Nagao S, Kaneko R, Hirabayashi M, Oiso Y, Itoh M, Caverzasio J (2010) Effects of transgenic Pit-1 overexpression on calcium phosphate and bone metabolism. J Bone Miner Metab 28:139–148.  https://doi.org/10.1007/s00774-009-0121-3 CrossRefPubMedGoogle Scholar
  76. 76.
    Tada H, Nemoto E, Foster BL, Somerman MJ, Shimauchi H (2011) Phosphate increases bone morphogenetic protein-2 expression through cAMP-dependent protein kinase and ERK1/2 pathways in human dental pulp cells. Bone 48:1409–1416.  https://doi.org/10.1016/j.bone.2011.03.675 CrossRefPubMedGoogle Scholar
  77. 77.
    Tenenhouse HS (1997) Cellular and molecular mechanisms of renal phosphate transport. J Bone Miner Res 12:159–164.  https://doi.org/10.1359/jbmr.1997.12.2.159 CrossRefPubMedGoogle Scholar
  78. 78.
    Tenenhouse HS, Klugerman AH, Neal JL (1989) Effect of phosphonoformic acid, dietary phosphate and the Hyp mutation on kinetically distinct phosphate transport processes in mouse kidney. Biochim Biophys Acta 984:207–213CrossRefPubMedGoogle Scholar
  79. 79.
    Tiosano D, Hochberg Z (2009) Hypophosphatemia: the common denominator of all rickets. J Bone Miner Metab 27:392–401.  https://doi.org/10.1007/s00774-009-0079-1 CrossRefPubMedGoogle Scholar
  80. 80.
    Traebert M, Lötscher M, Aschwanden R, Ritthaler T, Biber J, Murer H, Kaissling B (1999) Distribution of the sodium/phosphate transporter during postnatal ontogeny of the rat kidney. J Am Soc Nephrol 10:1407–1415PubMedGoogle Scholar
  81. 81.
    Veis A, Dorvee JR (2013) Biomineralization mechanisms: a new paradigm for crystal nucleation in organic matrices. Calcif Tissue Int 93:307–315.  https://doi.org/10.1007/s00223-012-9678-2 CrossRefPubMedGoogle Scholar
  82. 82.
    Virkki LV, Forster IC, Hernando N, Biber J, Murer H (2003) Functional characterization of two naturally occurring mutations in the human sodium-phosphate cotransporter type IIa. J Bone Miner Res 18:2135–2141.  https://doi.org/10.1359/jbmr.2003.18.12.2135 CrossRefPubMedGoogle Scholar
  83. 83.
    Wagner CA, Hernando N, Forster IC, Biber J (2013) The SLC34 family of sodium-dependent phosphate transporters. Pflugers Arch 466:139–153.  https://doi.org/10.2152/jmi.60.27 CrossRefPubMedGoogle Scholar
  84. 84.
    Wagner CA, Rubio-Aliaga I, Hernando N (2017) Renal phosphate handling and inherited disorders of phosphate reabsorption: an update 1–11.  https://doi.org/10.1007/s00467-017-3873-3
  85. 85.
    Walker JJ, Yan TS, Quamme GA (1987) Presence of multiple sodium-dependent phosphate transport processes in proximal brush-border membrane. Am J Phys 252:F226–F231.  https://doi.org/10.1152/ajprenal.1987.252.2.F226 CrossRefGoogle Scholar
  86. 86.
    Weiner S, Addadi L (2011) Crystallization pathways in biomineralization. Annu Rev Mater Res 41:21–40.  https://doi.org/10.1146/annurev-matsci-062910-095803 CrossRefGoogle Scholar
  87. 87.
    White KE, Hum JM, Econs MJ (2014) Hypophosphatemic rickets: revealing novel control points for phosphate homeostasis. Curr Osteoporos Rep 12:252–262.  https://doi.org/10.1172/JCI72829 CrossRefPubMedPubMedCentralGoogle Scholar
  88. 88.
    Wittrant Y, Bourgine A, Khoshniat S, Alliot-Licht B, Masson M, Gatius M, Rouillon T, Weiss P, Beck L, Guicheux J (2009) Inorganic phosphate regulates Glvr-1 and -2 expression: role of calcium and ERK1/2. Biochem Biophys Res Commun 381:259–263.  https://doi.org/10.1016/j.bbrc.2009.02.034 CrossRefPubMedGoogle Scholar
  89. 89.
    Wuthier RE (2011) Matrix vesicles: structure, composition, formation and function in calcification. Front Biosci (Landmark Ed) 16:2812–2902CrossRefGoogle Scholar
  90. 90.
    Xu H, Bai L, Collins JF, Ghishan FK (1999) Molecular cloning, functional characterization, tissue distribution, and chromosomal localization of a human, small intestinal sodium-phosphate (Na+-Pi) transporter (SLC34A2). Genomics 62:281–284.  https://doi.org/10.1006/geno.1999.6009 CrossRefPubMedGoogle Scholar
  91. 91.
    Yadav MC, Bottini M, Cory E, Bhattacharya K, Kuss P, Narisawa S, Sah RL, Beck L, Fadeel B, Farquharson C, Millán JL (2017) Skeletal mineralization deficits and impaired biogenesis and function of chondrocyte-derived matrix vesicles in Phospho1(−/−) and Phospho1/Pi t1 double-knockout mice. J Bone Miner Res 231:1275–1286.  https://doi.org/10.1002/jbmr.2790 CrossRefGoogle Scholar
  92. 92.
    Yamada S, Wallingford MC, Borgeia S, Cox TC, Giachelli CM (2018) Loss of PiT-2 results in abnormal bone development and decreased bone mineral density and length in mice. Biochem Biophys Res Commun 495:553–559.  https://doi.org/10.1016/j.bbrc.2017.11.071 CrossRefPubMedGoogle Scholar
  93. 93.
    Yin K, Hacia JG, Zhong Z, Paine ML (2014) Genome-wide analysis of miRNA and mRNA transcriptomes during amelogenesis. BMC Genomics 15:998–767.  https://doi.org/10.1016/j.molcel.2007.05.018 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.INSERM, UMR 1229, RMeS, Regenerative Medicine and Skeleton, Faculté de Chirurgie Dentaire, Université de NantesONIRISNantesFrance
  2. 2.Université de Nantes, UFR OdontologieNantesFrance

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