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Type II Na+-phosphate Cotransporters and Phosphate Balance in Teleost Fish

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Abstract

Teleost fish are excellent models to study the phylogeny of the slc34 gene family, Slc34-mediated phosphate (Pi) transport and how Slc34 transporters contribute Pi homeostasis. Fish need to accumulate Pi from the diet to sustain growth. Much alike in mammals, intestinal uptake in fish is partly a paracellular and partly a Slc34-mediated transcellular process. Acute regulation of Pi balance is achieved in the kidney via a combination of Slc34-mediated secretion and/or reabsorption. A great plasticity is observed in how various species perform and combine the different processes of secretion and reabsorption. A reason for this diversity is found in one or two whole genome duplication events followed by potential gene loss; consequently, teleosts exhibit distinctly different repertoires of Slc34 transporters. Moreover, due to habitats with vastly different salinity, teleosts face the challenge of either preserving water in a hyperosmotic environment (seawater) or excreting water in hypoosmotic freshwater. An additional challenge in understanding teleost Pi homeostasis are the genome duplication and retention events that diversified peptide hormones such as parathyroid hormone and stanniocalcin. Dietary Pi and non-coding RNAs also regulate the expression of piscine Slc34 transporters. The adaptive responses of teleost Slc34 transporters to e.g. Pi diets and vitamin D are informative in the context of comparative physiology, but also relevant in applied physiology and aquaculture. In fact, Pi is essential for teleost fish growth but it also exerts significant adverse consequences if over-supplied. Thus, investigating Slc34 transporters helps tuning the physiology of commercially valuable teleost fish in a confined environment.

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References

  1. Abbink W, Flik G (2007) Parathyroid hormone-related protein in teleost fish. Gen Comp Endocrinol 152:243–251

    Article  CAS  PubMed  Google Scholar 

  2. Abbink W, Bevelander GS, Hang X, Lu W, Guerreiro PM, Spanings T, Canario AV, Flik G (2006) PTHrP regulation and calcium balance in sea bream (Sparus auratus L.) under calcium constraint. J Exp Biol 209:3550–3557

    Article  CAS  PubMed  Google Scholar 

  3. Amemiya Y, Marra LE, Reyhani N, Youson JH (2002) Stanniocalcin from an ancient teleost: a monomeric form of the hormone and a possible extracorpuscular distribution. Mol Cell Endocrinol 188:141–150

    Article  CAS  PubMed  Google Scholar 

  4. Apschner A, Huitema LF, Ponsioen B, Peterson-Maduro J, Schulte-Merker S (2014) Zebrafish enpp1 mutants exhibit pathological mineralization, mimicking features of generalized arterial calcification of infancy (GACI) and pseudoxanthoma elasticum (PXE). Dis Model Mech 7:811–822

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Avila EM, Basantes SP, Ferraris RP (1999) Cholecalciferol modulates plasma phosphate but not plasma vitamin D levels and intestinal phosphate absorption in rainbow trout (Oncorhynchus mykiss). Gen Comp Endocrinol 114:460–469

    Article  CAS  PubMed  Google Scholar 

  6. Avila EM, Tu H, Basantes S, Ferraris RP (2000) Dietary phosphorus regulates intestinal transport and plasma concentrations of phosphate in rainbow trout. J Comp Physiol B 170:201–209

    Article  CAS  PubMed  Google Scholar 

  7. Banerjee C, Goswami R, Datta S, Rajagopal R, Mazumder S (2011) Arsenic-induced alteration in intracellular calcium homeostasis induces head kidney macrophage apoptosis involving the activation of calpain-2 and ERK in Clarias batrachus. Toxicol Appl Pharmacol 256:44–51

    Article  CAS  PubMed  Google Scholar 

  8. Beene LC, Halluer J, Yoshinaga M, Hamdi M, Liu Z (2011) Pentavalent arsenate transport by zebrafish phosphate transporter NaPi-IIb1. Zebrafish 8:125–131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Berndt TJ, Knox FG (1984) Proximal tubule site of inhibition of phosphate reabsorption by calcitonin. Am J Physiol 246:F927–F930

    CAS  PubMed  Google Scholar 

  10. Berthelot C, Brunet F, Chalopin D, Juanchich A, Bernard M, Noel B, Bento P, Da Silva C, Labadie K, Alberti A, Aury JM, Louis A, Dehais P, Bardou P, Montfort J, Klopp C, Cabau C, Gaspin C, Thorgaard GH, Boussaha M, Quillet E, Guyomard R, Galiana D, Bobe J, Volff JN, Genet C, Wincker P, Jaillon O, Roest Crollius H, Guiguen Y (2014) The rainbow trout genome provides novel insights into evolution after whole-genome duplication in vertebrates. Nat Commun 5:3657

    Article  PubMed  PubMed Central  Google Scholar 

  11. Betancur RR, Wiley EO, Arratia G, Acero A, Bailly N, Miya M, Lecointre G, Orti G (2017) Phylogenetic classification of bony fishes. BMC Evol Biol 17:162

    Article  Google Scholar 

  12. Beyenbach KW (2004) Kidneys sans glomeruli. Am J Physiol Ren Physiol 286:F811–F827

    Article  CAS  Google Scholar 

  13. Bjornsson BT, Deftos LJ (1985) Plasma calcium and calcitonin in the marine teleost, Gadus morhua. Comp Biochem Physiol A Comp Physiol 81:593–596

    Article  CAS  PubMed  Google Scholar 

  14. Bonga SE, Lammers PI, Van der Meij JC (1983) Effects of 1,25- and 24,25-dihydroxyvitamin D3 on bone formation in the ciclid teleost Sarotherodon mossambicus. Cell Tissue Res 228:117–126

    Article  Google Scholar 

  15. Bouillon R, Suda T (2014) Vitamin D: calcium and bone homeostasis during evolution. Bonekey Rep 3:480

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Bourre JM, Paquotte P (2008) Seafood (wild and farmed) for the elderly: contribution to the dietary intakes of iodine, selenium, DHA and vitamins B12 and D. J Nutr Health Aging 12:186–192

    Article  CAS  PubMed  Google Scholar 

  17. Butkus A, Roche PJ, Fernley RT, Haralambidis J, Penschow JD, Ryan GB, Trahair JF, Tregear GW, Coghlan JP (1987) Purification and cloning of a corpuscles of Stannius protein from Anguilla australis. Mol Cell Endocrinol 54:123–133

    Article  CAS  PubMed  Google Scholar 

  18. Canario AV, Rotllant J, Fuentes J, Guerreiro PM, Rita Teodosio H, Power DM, Clark MS (2006) Novel bioactive parathyroid hormone and related peptides in teleost fish. FEBS Lett 580:291–299

    Article  CAS  PubMed  Google Scholar 

  19. Carlile M, Nalbant P, Preston-Fayers K, McHaffie GS, Werner A (2008) Processing of naturally occurring sense/antisense transcripts of the vertebrate Slc34a gene into short RNAs. Physiol Genomics 34:95–100

    Article  CAS  PubMed  Google Scholar 

  20. Chen P, Tang Q, Wang C (2016) Characterizing and evaluating the expression of the type IIb sodium-dependent phosphate cotransporter (slc34a2) gene and its potential influence on phosphorus utilization efficiency in yellow catfish (Pelteobagrus fulvidraco). Fish Physiol Biochem 42:51–64

    Article  CAS  PubMed  Google Scholar 

  21. Chen P, Huang Y, Bayir A, Wang C (2017) Characterization of the isoforms of type IIb sodium-dependent phosphate cotransporter (Slc34a2) in yellow catfish, Pelteobagrus fulvidraco, and their vitamin D3-regulated expression under low-phosphate conditions. Fish Physiol Biochem 43:229–244

    Article  CAS  PubMed  Google Scholar 

  22. Cheng CN, Wingert RA (2015) Nephron proximal tubule patterning and corpuscles of Stannius formation are regulated by the sim1a transcription factor and retinoic acid in zebrafish. Dev Biol 399:100–116

    Article  CAS  PubMed  Google Scholar 

  23. Chesnut CH 3rd, Azria M, Silverman S, Engelhardt M, Olson M, Mindeholm L (2008) Salmon calcitonin: a review of current and future therapeutic indications. Osteoporos Int 19:479–491

    Article  PubMed  Google Scholar 

  24. Cho CY, Bureau DP (2001) A review of diet formulation strategies and feeding systems to reduce excretory and feed wastes in aquaculture. Aquac Res 32:349–360

    CAS  Google Scholar 

  25. Chou MY, Lin CH, Chao PL, Hung JC, Cruz SA, Hwang PP (2015) Stanniocalcin-1 controls ion regulation functions of ion-transporting epithelium other than calcium balance. Int J Biol Sci 11:122–132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Costa JM, Sartori MMP, Nascimento NFD, Kadri SM, Ribolla PEM, Pinhal D, Pezzato LE (2018) Inadequate dietary phosphorus levels cause skeletal anomalies and alter osteocalcin gene expression in zebrafish. Int J Mol Sci 19:364

  27. Danks JA, Ho PM, Notini AJ, Katsis F, Hoffmann P, Kemp BE, Martin TJ, Zajac JD (2003) Identification of a parathyroid hormone in the fish Fugu rubripes. J Bone Miner Res 18:1326–1331

  28. Danks JA, D'Souza DG, Gunn HJ, Milley KM, Richardson SJ (2011) Evolution of the parathyroid hormone family and skeletal formation pathways. Gen Comp Endocrinol 170:79–91

    Article  CAS  PubMed  Google Scholar 

  29. Datta S, Saha DR, Ghosh D, Majumdar T, Bhattacharya S, Mazumder S (2007) Sub-lethal concentration of arsenic interferes with the proliferation of hepatocytes and induces in vivo apoptosis in Clarias batrachus L. Comp Biochem Physiol C Toxicol Pharmacol 145:339–349

    Article  CAS  PubMed  Google Scholar 

  30. Datta S, Mazumder S, Ghosh D, Dey S, Bhattacharya S (2009) Low concentration of arsenic could induce caspase-3 mediated head kidney macrophage apoptosis with JNK-p38 activation in Clarias batrachus. Toxicol Appl Pharmacol 241:329–338

    Article  CAS  PubMed  Google Scholar 

  31. Davidson WS, Koop BF, Jones SJ, Iturra P, Vidal R, Maass A, Jonassen I, Lien S, Omholt SW (2010) Sequencing the genome of the Atlantic salmon (Salmo salar). Genome Biol 11:403

    PubMed  PubMed Central  Google Scholar 

  32. Dean MN, Ekstrom L, Monsonego-Ornan E, Ballantyne J, Witten PE, Riley C, Habraken W, Omelon S (2015) Mineral homeostasis and regulation of mineralization processes in the skeletons of sharks, rays and relatives (Elasmobranchii). Semin Cell Dev Biol 46:51–67

    Article  CAS  PubMed  Google Scholar 

  33. Dickman KG, Renfro JL (1986) Primary culture of flounder renal tubule cells: transepithelial transport. Am J Physiol 251:F424–F432

    CAS  PubMed  Google Scholar 

  34. Dimitrov EL, Petrus E, Usdin TB (2010) Tuberoinfundibular peptide of 39 residues (TIP39) signaling modulates acute and tonic nociception. Exp Neurol 226:68–83

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Dimitrov EL, Kuo J, Kohno K, Usdin TB (2013) Neuropathic and inflammatory pain are modulated by tuberoinfundibular peptide of 39 residues. Proc Natl Acad Sci U S A 110:13156–13161

    Article  PubMed  PubMed Central  Google Scholar 

  36. Drummond BE, Li Y, Marra AN, Cheng CN, Wingert RA (2017) The tbx2a/b transcription factors direct pronephros segmentation and corpuscle of Stannius formation in zebrafish. Dev Biol 421:52–66

    Article  CAS  PubMed  Google Scholar 

  37. Elger M, Werner A, Herter P, Kohl B, Kinne RK, Hentschel H (1998) Na-P(i) cotransport sites in proximal tubule and collecting tubule of winter flounder (Pleuronectes americanus). Am J Physiol 274:F374–F383

    CAS  PubMed  Google Scholar 

  38. Elizondo MR, Budi EH, Parichy DM (2010) trpm7 regulation of in vivo cation homeostasis and kidney function involves stanniocalcin 1 and fgf23. Endocrinology 151:5700–5709

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Erickson RJ, Mount DR, Highland TL, Russell Hockett J, Jenson CT (2011) The relative importance of waterborne and dietborne arsenic exposure on survival and growth of juvenile rainbow trout. Aquat Toxicol 104:108–115

    Article  CAS  PubMed  Google Scholar 

  40. Evans DH (2008) Teleost fish osmoregulation: what have we learned since August Krogh, Homer Smith, and Ancel Keys. Am J Physiol Regul Integr Comp Physiol 295:R704–R713

    Article  CAS  PubMed  Google Scholar 

  41. Evans DH, Claiborne JB (2009) Osmotic and ionic regulation in fishes. In: Evans DH (ed) Osmotic and ionic regulation: cells and animals. CRC Press, Boca Raton

    Google Scholar 

  42. Fenwick JC, Lam TJ (1988) Effects of calcitonin on plasma calcium and phosphate in the mudskipper, Periophthalmodon schlosseri (Teleostei), in water and during exposure to air. Gen Comp Endocrinol 70:224–230

    Article  CAS  PubMed  Google Scholar 

  43. Fenwick JC, Vermette MG (1989) Vitamin D3 and the renal handling of phosphate in American eels. Fish Physiol Biochem 7:351–358

    Article  CAS  PubMed  Google Scholar 

  44. Fenwick JC, Smith K, Smith J, Flik G (1984) Effect of various vitamin D analogs on plasma calcium and phosphorus and intestinal calcium absorption in fed and unfed American eels, Anguilla rostrata. Gen Comp Endocrinol 55:398–404

    Article  CAS  PubMed  Google Scholar 

  45. Fenwick JC, Davison W, Forster ME (1994) In vivo calcitropic effect of some vitamin D compounds in the marine Antarctic teleost, Pagothenia bernacchii. Fish Physiol Biochem 12:479–484

    Article  CAS  PubMed  Google Scholar 

  46. Flanagan JA, Power DM, Bendell LA, Guerreiro PM, Fuentes J, Clark MS, Canario AV, Danks JA, Brown BL, Ingleton PM (2000) Cloning of the cDNA for sea bream (Sparus aurata) parathyroid hormone-related protein. Gen Comp Endocrinol 118:373–382

    Article  CAS  PubMed  Google Scholar 

  47. Fleming A, Sato M, Goldsmith P (2005) High-throughput in vivo screening for bone anabolic compounds with zebrafish. J Biomol Screen 10:823–831

    Article  CAS  PubMed  Google Scholar 

  48. Flik G, Labedz T, Neelissen JA, Hanssen RG, Bonga SE, Pang PK (1990) Rainbow trout corpuscles of Stannius: stanniocalcin synthesis in vitro. Am J Physiol 258:R1157–R1164

  49. Forster IC (2018) The molecular mechanism of SLC34 proteins: insights from two decades of transport assays and structure-function studies. Pflugers Arch - Eur J Physiol (in press)

  50. Fraser DR (2018) Evolutionary Biology. In: Evolutionary biology: mysteries of vitamin D in fish. Academic Press, San Diego

    Google Scholar 

  51. Fraser RA, Kaneko T, Pang PK, Harvey S (1991) Hypo- and hypercalcemic peptides in fish pituitary glands. Am J Physiol 260:R622–R626

    CAS  PubMed  Google Scholar 

  52. Fuentes J, Figueiredo J, Power DM, Canario AV (2006) Parathyroid hormone-related protein regulates intestinal calcium transport in sea bream (Sparus auratus). Am J Physiol Regul Integr Comp Physiol 291:R1499–R1506

    Article  CAS  PubMed  Google Scholar 

  53. Fuentes J, Power DM, Canario AV (2010) Parathyroid hormone-related protein-stanniocalcin antagonism in regulation of bicarbonate secretion and calcium precipitation in a marine fish intestine. Am J Physiol Regul Integr Comp Physiol 299:R150–R158

    Article  CAS  PubMed  Google Scholar 

  54. Gensure RC, Ponugoti B, Gunes Y, Papasani MR, Lanske B, Bastepe M, Rubin DA, Juppner H (2004) Identification and characterization of two parathyroid hormone-like molecules in zebrafish. Endocrinology 145:1634–1639

    Article  CAS  PubMed  Google Scholar 

  55. Gerritsen ME, Wagner GF (2005) Stanniocalcin: no longer just a fish tale. Vitam Horm 70:105–135

    Article  CAS  PubMed  Google Scholar 

  56. Giachelli CM (2008) Ectopic mineralization: new concepts in etiology and regulation. Weinheim, Wiley-VCH Verlag GmbH

    Google Scholar 

  57. Graham C, Nalbant P, Scholermann B, Hentschel H, Kinne RK, Werner A (2003) Characterization of a type IIb sodium-phosphate cotransporter from zebrafish (Danio rerio) kidney. Am J Physiol Regul Integr Comp Physiol 284:F727–F736

    Article  CAS  Google Scholar 

  58. Guerreiro PM, Fuentes J, Power DM, Ingleton PM, Flik G, Canario AV (2001) Parathyroid hormone-related protein: a calcium regulatory factor in sea bream (Sparus aurata L.) larvae. Am J Physiol Regul Integr Comp Physiol 281:R855–R860

    Article  CAS  PubMed  Google Scholar 

  59. Guerreiro PM, Renfro JL, Power DM, Canario AV (2007) The parathyroid hormone family of peptides: structure, tissue distribution, regulation, and potential functional roles in calcium and phosphate balance in fish. Am J Physiol Regul Integr Comp Physiol 292:R679–R696

    Article  CAS  PubMed  Google Scholar 

  60. Guerreiro PM, Canario AV, Power DM, Renfro JL (2010) Piscine PTHrP regulation of calcium and phosphate transport in winter flounder renal proximal tubule primary cultures. Am J Physiol Regul Integr Comp Physiol 299:R603–R611

    Article  CAS  PubMed  Google Scholar 

  61. Gupta A, Renfro JL (1989) Control of phosphate transport in flounder renal proximal tubule primary cultures. Am J Physiol 256:R850–R857

    CAS  PubMed  Google Scholar 

  62. Hallauer J, Geng X, Yang HC, Shen J, Tsai KJ, Liu Z (2016) The effect of chronic arsenic exposure in zebrafish. Zebrafish 13:405–412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Hamdi M, Sanchez MA, Beene LC, Liu Q, Landfear SM, Rosen BP, Liu Z (2009) Arsenic transport by zebrafish aquaglyceroporins. BMC Mol Biol 10:104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Hang X, Balment RJ (2005) Stanniocalcin in the euryhaline flounder (Platichthys flesus): primary structure, tissue distribution, and response to altered salinity. Gen Comp Endocrinol 144:188–195

    Article  CAS  PubMed  Google Scholar 

  65. Hansen JA, Lipton J, Welsh PG, Cacela D, MacConnell B (2004) Reduced growth of rainbow trout (Oncorhynchus mykiss) fed a live invertebrate diet pre-exposed to metal-contaminated sediments. Environ Toxicol Chem 23:1902–1911

    Article  CAS  PubMed  Google Scholar 

  66. Hanssen RG, Mayer-Gostan N, Flik G, Bonga SE (1992) Influence of ambient calcium levels on stanniocalcin secretion in the European eel (Anguilla anguilla). J Exp Biol 162:197–208

    CAS  Google Scholar 

  67. Hanssen RG, Mayer-Gostan N, Flik G, Bonga SE (1993) Stanniocalcin kinetics in freshwater and seawater european eel (Anguilla anguilla). Fish Physiol Biochem 10:491–496

    Article  CAS  PubMed  Google Scholar 

  68. Hong SH, Park SJ, Lee S, Kim S, Cho MH (2015) Biological effects of inorganic phosphate: potential signal of toxicity. J Toxicol Sci 40:55–69

    Article  CAS  PubMed  Google Scholar 

  69. Hori M, Shimizu Y, Fukumoto S (2011) Minireview: fibroblast growth factor 23 in phosphate homeostasis and bone metabolism. Endocrinology 152:4–10

    Article  CAS  PubMed  Google Scholar 

  70. Huitema LF, Apschner A, Logister I, Spoorendonk KM, Bussmann J, Hammond CL, Schulte-Merker S (2012) Entpd5 is essential for skeletal mineralization and regulates phosphate homeostasis in zebrafish. Proc Natl Acad Sci U S A 109:21372–21377

    Article  PubMed  PubMed Central  Google Scholar 

  71. Hulova I, Kawauchi H (1999) Assignment of disulfide linkages in chum salmon stanniocalcin. Biochem Biophys Res Commun 257:295–299

    Article  CAS  PubMed  Google Scholar 

  72. Juan D, Liptak P, Gray TK (1976) Absorption of inorganic phosphate in the human jejunum and its inhibition by salmon calcitonin. J Clin Endocrinol Metab 43:517–522

    Article  CAS  PubMed  Google Scholar 

  73. Juppner H (2011) Phosphate and FGF-23. Kidney Int 79121:S24–S27

    Article  CAS  PubMed  Google Scholar 

  74. Kassahn KS, Dang VT, Wilkins SJ, Perkins AC, Ragan MA (2009) Evolution of gene function and regulatory control after whole-genome duplication: comparative analyses in vertebrates. Genome Res 19:1404–1418

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Kaune R, Hentschel H (1987) Stimulation of renal phosphate secretion in the stenohaline freshwater teleost: Carassius auratus gibelio Bloch. Comp Biochem Physiol A Comp Physiol 87:359–362

    Article  CAS  PubMed  Google Scholar 

  76. Kawai M (2016) The FGF23/klotho axis in the regulation of mineral and metabolic homeostasis. Horm Mol Biol Clin Invest 28:55–67

    CAS  Google Scholar 

  77. Kawamura J, Daizyo K, Hosokawa S, Yoshida O (1978) Acute effects of salmon calcitonin on renal electrolyte excretion in intact, thyroparathyroidectomized and sulfacetylthiazole-induced uremic rats. Nephron 21:334–344

    Article  CAS  PubMed  Google Scholar 

  78. Ketola HG (1975) Requirement of Atlantic salmon for dietary phosphorus. Trans Am Fish Soc 87:548–551

    Article  Google Scholar 

  79. Kim E, Yoo S, Ro HY, Han HJ, Baek YW, Eom IC, Kim HM, Kim P, Choi K (2013) Aquatic toxicity assessment of phosphate compounds. Environ Health Toxicol 28:e2013002

    Article  PubMed  PubMed Central  Google Scholar 

  80. Kirchner S, McDaniel NK, Sugiura SH, Soteropoulos P, Tian B, Fletcher JW, Ferraris RP (2007) Salmonid microarrays identify intestinal genes that reliably monitor P deficiency in rainbow trout aquaculture. Anim Genet 38:319–331

    Article  CAS  PubMed  Google Scholar 

  81. Kirsch T (2012) Biomineralization—an active or passive process? Connect Tissue Res 53:438–445

    Article  CAS  PubMed  Google Scholar 

  82. Kohl B, Herter P, Hulseweh B, Elger M, Hentschel H, Kinne RK, Werner A (1996) Na-Pi cotransport in flounder: same transport system in kidney and intestine. Am J Physiol 270:F937–F944

    CAS  PubMed  Google Scholar 

  83. Koide Y, Kugai N, Yamashita K, Shimazawa E, Ogata E (1976) A transient increase in renal clearance of phosphate in response to continuous infusion of salmon calcitonin in rats. Endocrinol Jpn 23:295–304

    Article  CAS  PubMed  Google Scholar 

  84. Krishnamurthy VG (1976) Cytophysiology of corpuscles of Stannius. Int Rev Cytol 46:177–249

    Article  CAS  PubMed  Google Scholar 

  85. Kumari B, Kumar V, Sinha AK, Ahsan J, Ghosh AK, Wang H, DeBoeck G (2017) Toxicology of arsenic in fish and aquatic systems. Environ Chem Lett 15:43–64

    Article  CAS  Google Scholar 

  86. Lafeber FP, Hanssen RG, Choy YM, Flik G, Herrmann-Erlee MP, Pang PK, Bonga SE (1988) Identification of hypocalcin (teleocalcin) isolated from trout Stannius corpuscles. Gen Comp Endocrinol 69:19–30

    Article  CAS  PubMed  Google Scholar 

  87. Lake J, Gravel C, Koko GK, Robert C, Vandenberg GW (2010) Combining suppressive subtractive hybridization and cDNA microarrays to identify dietary phosphorus-responsive genes of the rainbow trout (Oncorhynchus mykiss) kidney. Comp Biochem physiology Part D Genomics Proteomics 5:24–35

    Article  CAS  Google Scholar 

  88. Lall SP (2002) Mineral nutrition. Academic Press, San Diego

    Google Scholar 

  89. Lall SP, Lewis-McCrea LM (2007) Role of nutrients in skeletal metabolism and pathology in fish—an overview. Aquaculture 267:3–19

    Article  CAS  Google Scholar 

  90. Lin CH, Hu HJ, Hwang PP (2017) Molecular physiology of the hypocalcemic action of fibroblast growth factor 23 in zebrafish (Danio rerio). Endocrinology 158:1347–1358

    Article  PubMed  Google Scholar 

  91. Lock EJ, Waagbø R, Bonga SE, Flik G (2010) The significance of vitamin D for fish: a review. Aquac Nutr 16:100–116

    Article  CAS  Google Scholar 

  92. Lopez E, Peignoux-Deville J, Lallier F, Colston KW, Macintyre I (1977) Responses of bone metabolism in the eel (Anguilla anguilla) to injections of 1,25-dihydroxyvitamin D3. Calcif Tissue Res 22 Suppl:19–23

    CAS  PubMed  Google Scholar 

  93. Lopez E, Mac Intyre I, Martelly E, Lallier F, Vidal B (1980) Paradoxical effect of 1,25 dihydroxycholecalciferol on osteoblastic and osteoclastic activity in the skeleton of the eel Anguilla anguilla L. Calcif Tissue Int 32:83–87

    Article  CAS  PubMed  Google Scholar 

  94. Lu M, Wagner GF, Renfro JL (1994) Stanniocalcin stimulates phosphate reabsorption by flounder renal proximal tubule in primary culture. Am J Physiol 267:R1356–R1362

    CAS  PubMed  Google Scholar 

  95. Lu M, Swanson P, Renfro JL (1995) Effect of somatolactin and related hormones on phosphate transport by flounder renal tubule primary cultures. Am J Physiol 268:R577–R582

    CAS  PubMed  Google Scholar 

  96. Luo CW, Pisarska MD, Hsueh AJ (2005) Identification of a stanniocalcin paralog, stanniocalcin-2, in fish and the paracrine actions of stanniocalcin-2 in the mammalian ovary. Endocrinology 146:469–476

    Article  CAS  PubMed  Google Scholar 

  97. Macqueen DJ, Johnston IA (2014) A well-constrained estimate for the timing of the salmonid whole genome duplication reveals major decoupling from species diversification. Proc Biol Sci 281:20132881

    Article  PubMed  PubMed Central  Google Scholar 

  98. Magagnin S, Werner A, Markovich D, Sorribas V, Stange G, Biber J, Murer H (1993) Expression cloning of human and rat renal cortex Na/Pi cotransport. Proc Natl Acad Sci U S A 90:5979–5983

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Mangos S, Amaral AP, Faul C, Juppner H, Reiser J, Wolf M (2012) Expression of fgf23 and alphaklotho in developing embryonic tissues and adult kidney of the zebrafish, Danio rerio. Nephrol Dial Transplant 27:4314–4322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Marshall EK, Grafflin AL (1933) Excretion of inorganic phosphate by the aglomerular kidney. Proc Soc Exp Biol Med 31:44–46

    Article  CAS  Google Scholar 

  101. Martin A, David V, Quarles LD (2012) Regulation and function of the FGF23/klotho endocrine pathways. Physiol Rev 92:131–155

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. McCauley LK, Martin TJ (2012) Twenty-five years of PTHrP progress: from cancer hormone to multifunctional cytokine. J Bone Miner Res 27:1231–1239

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. McCudden CR, Kogon MR, DiMattia GE, Wagner GF (2001) Novel expression of the stanniocalcin gene in fish. J Endocrinol 171:33–44

    Article  CAS  PubMed  Google Scholar 

  104. Murer H, Hernando N, Forster I, Biber J (2003) Regulation of Na/Pi transporter in the proximal tubule. Annu Rev Physiol 65:531–542

    Article  CAS  PubMed  Google Scholar 

  105. Nakamura Y, Hirano T (1986) Effect of hypophysectomy on absorption of inorganic phosphate by the eel intestine. Comp Biochem Physiol A Comp Physiol 84:595–599

    Article  CAS  PubMed  Google Scholar 

  106. Nalbant P, Boehmer C, Dehmelt L, Wehner F, Werner A (1999) Functional characterization of a Na+-phosphate cotransporter (NaPi-II) from zebrafish and identification of related transcripts. J Physiol 520:79–89

  107. Near TJ, Eytan RI, Dornburg A, Kuhn KL, Moore JA, Davis MP, Wainwright PC, Friedman M, Smith WL (2012) Resolution of ray-finned fish phylogeny and timing of diversification. Proc Natl Acad Sci U S A 109:13698–13703

    Article  PubMed  PubMed Central  Google Scholar 

  108. Nelson JS (2006) Fishes of the world. John Wiley and Sons, New York

    Google Scholar 

  109. Okabe M, Graham A (2004) The origin of the parathyroid gland. Proc Natl Acad Sci U S A 101:17716–17719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Olsen HS, Cepeda MA, Zhang QQ, Rosen CA, Vozzolo BL, Wagner GF (1996) Human stanniocalcin: a possible hormonal regulator of mineral metabolism. Proc Natl Acad Sci U S A 93:1792–1796

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Pang PK (1971) Calcitonin and ultimobranchial glands in fishes. J Exp Zool 178:89–99

    Article  CAS  PubMed  Google Scholar 

  112. Papasani MR, Gensure RC, Yan YL, Gunes Y, Postlethwait JH, Ponugoti B, John MR, Juppner H, Rubin DA (2004) Identification and characterization of the zebrafish and fugu genes encoding tuberoinfundibular peptide 39. Endocrinology 145:5294–5304

    Article  CAS  PubMed  Google Scholar 

  113. Pasquier J, Cabau C, Nguyen T, Jouanno E, Severac D, Braasch I, Journot L, Pontarotti P, Klopp C, Postlethwait JH, Guiguen Y, Bobe J (2016) Gene evolution and gene expression after whole genome duplication in fish: the PhyloFish database. BMC Genomics 17:368

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Pedlar RM, Klaverkamp JF (2002) Accumulation and distribution of dietary arsenic in lake whitefish (Coregonus clupeaformis). Aquat Toxicol 57:153–166

    Article  CAS  PubMed  Google Scholar 

  115. Pedlar RM, Ptashynski MD, Evans R, Klaverkamp JF (2002) Toxicological effects of dietary arsenic exposure in lake whitefish (Coregonus clupeaformis). Aquat Toxicol 57:167–189

    Article  CAS  PubMed  Google Scholar 

  116. Pedlar RM, Ptashynski MD, Wautier KG, Evans RE, Baron CL, Klaverkamp JF (2002) The accumulation, distribution, and toxicological effects of dietary arsenic exposure in lake whitefish (Coregonus clupeaformis) and lake trout (Salvelinus namaycush). Comp Biochem Physiol C Toxicol Pharmacol 131:73–91

    Article  CAS  PubMed  Google Scholar 

  117. Piatek MJ, Henderson V, Zynad HS, Werner A (2016) Natural antisense transcription from a comparative perspective. Genomics 108:56–63

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Piatek MJ, Henderson V, Fearn A, Chaudhry B, Werner A (2017) Ectopically expressed Slc34a2a sense-antisense transcripts cause a cerebellar phenotype in zebrafish embryos depending on RNA complementarity and dicer. PLoS One 12:e0178219

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Pierens SL, Fraser DR (2015) The origin and metabolism of vitamin D in rainbow trout. J Steroid Biochem Mol Biol 145:58–64

    Article  CAS  PubMed  Google Scholar 

  120. Potts JT (2005) Parathyroid hormone: past and present. J Endocrinol 187:311–325

    Article  CAS  PubMed  Google Scholar 

  121. Power DM, Ingleton PM, Flanagan J, Canario AV, Danks J, Elgar G, Clark MS (2000) Genomic structure and expression of parathyroid hormone-related protein gene (PTHrP) in a teleost, Fugu rubripes. Gene 250:67–76

    Article  CAS  PubMed  Google Scholar 

  122. Rao DS, Raghuramulu N (1999) Vitamin D3 and its metabolites have no role in calcium and phosphorus metabolism in Tilapia mossambica. J Nutr Sci Vitaminol 45:9–19

    Article  CAS  PubMed  Google Scholar 

  123. Ravi V, Venkatesh B (2008) Rapidly evolving fish genomes and teleost diversity. Curr Opin Genet Dev 18:544–550

    Article  CAS  PubMed  Google Scholar 

  124. Renfro JL (1997) Hormonal regulation of renal inorganic phosphate transport in the winter flounder, Pleuronectes americanus. Fish Physiol Biochem 17:377–383

    Article  CAS  Google Scholar 

  125. Richter B, Faul C (2018) FGF23 actions on target tissues-with and without klotho. Front Endocrinol 9:189

    Article  Google Scholar 

  126. Roach G, Heath Wallace R, Cameron A, Emrah Ozel R, Hongay CF, Baral R, Andreescu S, Wallace KN (2013) Loss of ascl1a prevents secretory cell differentiation within the zebrafish intestinal epithelium resulting in a loss of distal intestinal motility. Dev Biol 376:171–186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Roggenbeck BA, Banerjee M, Leslie EM (2016) Cellular arsenic transport pathways in mammals. J Environ Sci (China) 49:38–58

    Article  Google Scholar 

  128. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  129. Samy JKA, Mulugeta TD, Nome T, Sandve SR, Grammes F, Kent MP, Lien S, Vage DI (2017) SalmoBase: an integrated molecular data resource for Salmonid species. BMC Genomics 18:482

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Sasayama Y, Suzuki N, Oguro C, Takei Y, Takahashi A, Watanabe TX, Nakajima K, Sakakibara S (1992) Calcitonin of the stingray: comparison of the hypocalcemic activity with other calcitonins. Gen Comp Endocrinol 86:269–274

    Article  CAS  PubMed  Google Scholar 

  131. Sato Y, Hashiguchi Y, Nishida M (2009) Temporal pattern of loss/persistence of duplicate genes involved in signal transduction and metabolic pathways after teleost-specific genome duplication. BMC Evol Biol 9:127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Schein V, Cardoso JC, Pinto PI, Anjos L, Silva N, Power DM, Canario AV (2012) Four stanniocalcin genes in teleost fish: structure, phylogenetic analysis, tissue distribution and expression during hypercalcemic challenge. Gen Comp Endocrinol 175:344–356

    Article  CAS  PubMed  Google Scholar 

  133. Schmid A, Walther B (2013) Natural vitamin D content in animal products. Adv Nutr 4:453–462

  134. Shin J, Sohn YC (2009) cDNA cloning of Japanese flounder stanniocalcin 2 and its mRNA expression in a variety of tissues. Comp Biochem Physiol Part A Mol Integr Physiol 153:24–29

    Article  CAS  Google Scholar 

  135. Shin J, Oh D, Sohn YC (2006) Molecular characterization and expression analysis of stanniocalcin-1 in turbot (Scophthalmus maximus). Gen Comp Endocrinol 147:214–221

    Article  CAS  PubMed  Google Scholar 

  136. Shu Y, Lou Q, Dai Z, Dai X, He J, Hu W, Yin Z (2016) The basal function of teleost prolactin as a key regulator on ion uptake identified with zebrafish knockout models. Sci Rep 6:18597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Singh S, Srivastav AK (1993) Effects of calcitonin administration on serum calcium and inorganic phosphate levels of the fish, Heteropneustes fossilis, maintained either in artificial freshwater, calcium-rich freshwater, or calcium-deficient freshwater. J Exp Zool 265:35–39

    Article  CAS  Google Scholar 

  138. Smith WW (1939) The excretion of phosphate in the dogfish, Squalus acanthias. J Cell Comp Physiol 14:95–102

  139. Srivastav SK, Jaiswal R, Srivastav AK (1993) Response of serum calcium to administration of 1,25-dihydroxyvitamin D3 in the freshwater carp Cyprinus carpio maintained either in artificial freshwater, calcium-rich freshwater or calcium-deficient freshwater. Acta Physiol Hung 81:269–275

    CAS  PubMed  Google Scholar 

  140. Srivastav AK, Srivastav SK, Sasayama Y, Suzuki N, Norman AW (1997) Vitamin D metabolites affect serum calcium and phosphate in freshwater catfish (Heteropneustes fossilis). Zool Sci 14:95–102

    Article  Google Scholar 

  141. Srivastav AK, Tiwari PR, Srivastav SK, Sasayama Y, Suzuki N (1997) Vitamin D3-induced calcemic and phosphatemic responses in the freshwater mud eel Amphipnous cuchia maintained in different calcium environments. Braz J Med Biol Res 30:1343–1348

    Article  CAS  PubMed  Google Scholar 

  142. Srivastav AK, Srivastav SK, Sasayama Y, Suzuki N (1998) Salmon calcitonin induced hypocalcemia and hyperphosphatemia in an elasmobranch, Dasyatis akajei. Gen Comp Endocrinol 109:8–12

    Article  CAS  PubMed  Google Scholar 

  143. Stolte H, Galaske RG, Eisenbach GM, Lechene C, Schmidt-Nielson B, Boylan JW (1977) Renal tubule ion transport and collecting duct function in the elasmobranch little skate, Raja erinacea. J Exp Zool 199:403–410

    Article  CAS  PubMed  Google Scholar 

  144. Suarez-Bregua P, Cal L, Canestro C, Rotllant J (2017) PTH reloaded: a new evolutionary perspective. Front Physiol 8:776

    Article  PubMed  PubMed Central  Google Scholar 

  145. Suarez-Bregua P, Saxena A, Bronner ME, Rotllant J (2017) Targeted Pth4-expressing cell ablation impairs skeletal mineralization in zebrafish. PLoS One 12:e0186444

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Suarez-Bregua P, Torres-Nunez E, Saxena A, Guerreiro P, Braasch I, Prober DA, Moran P, Cerda-Reverter JM, Du SJ, Adrio F, Power DM, Canario AV, Postlethwait JH, Bronner ME, Canestro C, Rotllant J (2017) Pth4, an ancient parathyroid hormone lost in eutherian mammals, reveals a new brain-to-bone signaling pathway. FASEB J 31:569–583

    Article  CAS  PubMed  Google Scholar 

  147. Suarez-Bregua P, Cal L, Guerreiro PM, Rotllant J (2018) Novel aspects of phosphate endocrine control: a key element for the long-term sustainability of finfish aquaculture. In: Yúfera M (ed) Emerging issues in fish larvae research. Springer International Publishing, Cham, pp 253–273

    Chapter  Google Scholar 

  148. Sugiura SH (2009) Identification of intestinal phosphate transporters in fishes and shellfishes. Fish Sci 75:99–108

    Article  CAS  Google Scholar 

  149. Sugiura SH, Ferraris RP (2004) Contributions of different NaPi cotransporter isoforms to dietary regulation of P transport in the pyloric caeca and intestine of rainbow trout. J Exp Biol 207:2055–2064

    Article  CAS  PubMed  Google Scholar 

  150. Sugiura SH, Ferraris RP (2004) Dietary phosphorus-responsive genes in the intestine, pyloric ceca, and kidney of rainbow trout. Am J Physiol Regul Integr Comp Physiol 287:R541–R550

    Article  CAS  PubMed  Google Scholar 

  151. Sugiura SH, McDaniel NK, Ferraris RP (2003) In vivo fractional P(i) absorption and NaPi-II mRNA expression in rainbow trout are upregulated by dietary P restriction. Am J Physiol Regul Integr Comp Physiol 285:R770–R781

    Article  CAS  PubMed  Google Scholar 

  152. Sugiura SH, Hardy RW, Roberts RJ (2004) The pathology of phosphorus deficiency in fish—a review. J Fish Dis 27:255–265

    Article  CAS  PubMed  Google Scholar 

  153. Sugiura SH, Marchant DD, Kelsey K, Wiggins T, Ferraris RP (2006) Effluent profile of commercially used low-phosphorus fish feeds. Environ Pollut 140:95–101

    Article  CAS  PubMed  Google Scholar 

  154. Sugiura SH, Kelsey K, Ferraris RP (2007) Molecular and conventional responses of large rainbow trout to dietary phosphorus restriction. J Comp Physiol B 177:461–472

    Article  CAS  PubMed  Google Scholar 

  155. Sundell K, Bjornsson BT, Itoh H, Kawauchi H (1992) Chum salmon (Oncorhynchus keta) stanniocalcin inhibits in vitro intestinal calcium uptake in Atlantic cod (Gadus morhua). J Comp Physiol B 162:489–495

    Article  CAS  PubMed  Google Scholar 

  156. Suzuki N (2005) Physiological significance of calcitonin in fish. Clin Calcium 15:139–146

    PubMed  Google Scholar 

  157. Swarup K, Norman AW, Srivastav AK, Srivastav SP (1984) Dose-dependent vitamin D3 and 1,25-dihydroxyvitamin D3-induced hypercalcemia and hyperphosphatemia in male catfish Clarias batrachus. Comp Biochem Physiology B 78:553–555

    Article  Google Scholar 

  158. Swarup K, Pandey AK, Hasan N, Das VK (1992) Dose-dependent vitamin D3, 25-hydroxyvitamin D3 and 1,25-dihydroxyvitamin D3-induced hypercalcemia and hyperphosphatemia, and the correlative changes in the activity of ultimobranchial and parathyroid glands of the toad, Bufo andersoni Boulenger. Biol Struct Morphog 4:174–181

    CAS  PubMed  Google Scholar 

  159. Tan Q, He R, Xie S, Xie C, Zhang S (2007) Effect of dietary supplementation of vitamins a, D3, E, and C on yearling rice field eel, Monopterus albus: serum indices, gonad development, and metabolism of calcium and phosphorus. J World Aquacult Soc 38:146–153

    Article  Google Scholar 

  160. Tseng DY, Chou MY, Tseng YC, Hsiao CD, Huang CJ, Kaneko T, Hwang PP (2009) Effects of stanniocalcin 1 on calcium uptake in zebrafish (Danio rerio) embryo. Am J Physiol Regul Integr Comp Physiol 296:R549–R557

    Article  CAS  PubMed  Google Scholar 

  161. Urist MR (1976) Biogenesis of bone: calcium and phosphorus in the skeleton and blood in vertebrate evolution. Washington, American Physiological Society

    Google Scholar 

  162. Ventura-Lima J, Bogo MR, Monserrat JM (2011) Arsenic toxicity in mammals and aquatic animals: a comparative biochemical approach. Ecotoxicol Environ Saf 74:211–218

    Article  CAS  PubMed  Google Scholar 

  163. Verbost PM, Butkus A, Atsma W, Willems P, Flik G, Bonga SE (1993) Studies on stanniocalcin: characterization of bioactive and antigenic domains of the hormone. Mol Cell Endocrinol 93:11–16

    Article  CAS  PubMed  Google Scholar 

  164. Vielma J, Lall SP (1998) Phosphorus utilization by Atlantic salmon (Salmo salar) reared in freshwater is not influenced by higher dietary calcium intake. Aquaculture 160:117–128

    Article  CAS  Google Scholar 

  165. Volff JN (2005) Genome evolution and biodiversity in teleost fish. Heredity 94:280–294

    Article  CAS  PubMed  Google Scholar 

  166. Wagner GF, Dimattia GE (2006) The stanniocalcin family of proteins. J Exp Zool A Comp Exp Biol 305:769–780

    Article  CAS  PubMed  Google Scholar 

  167. Wagner GF, Hampong M, Park CM, Copp DH (1986) Purification, characterization, and bioassay of teleocalcin, a glycoprotein from salmon corpuscles of Stannius. Gen Comp Endocrinol 63:481–491

    Article  CAS  PubMed  Google Scholar 

  168. Wagner GF, Fenwick JC, Park CM, Milliken C, Copp DH, Friesen HG (1988) Comparative biochemistry and physiology of teleocalcin from sockeye and coho salmon. Gen Comp Endocrinol 72:237–246

    Article  CAS  PubMed  Google Scholar 

  169. Wagner GF, Dimattia GE, Davie JR, Copp DH, Friesen HG (1992) Molecular cloning and cDNA sequence analysis of coho salmon stanniocalcin. Mol Cell Endocrinol 90:7–15

    Article  CAS  PubMed  Google Scholar 

  170. Wagner GF, Fargher RC, Milliken C, McKeown BA, Copp DH (1993) The gill calcium transport cycle in rainbow trout is correlated with plasma levels of bioactive, not immunoreactive, stanniocalcin. Mol Cell Endocrinol 93:185–191

    Article  CAS  PubMed  Google Scholar 

  171. Wagner GF, Haddad M, Fargher RC, Milliken C, Copp DH (1998) Calcium is an equipotent stimulator of stanniocalcin secretion in freshwater and seawater salmon. Gen Comp Endocrinol 109:186–191

    Article  CAS  PubMed  Google Scholar 

  172. Wells G, Chernoff J, Gilligan JP, Krause DS (2016) Does salmon calcitonin cause cancer? A review and meta-analysis. Osteoporos Int 27:13–19

    Article  CAS  PubMed  Google Scholar 

  173. Werner A, Murer H, Kinne RK (1994) Cloning and expression of a renal Na-Pi cotransport system from flounder. Am J Physiol 267:F311–F317

    CAS  PubMed  Google Scholar 

  174. Werner A, Preston-Fayers K, Dehmelt L, Nalbant P (2002) Regulation of the NPT gene by a naturally occurring antisense transcript. Cell Biochem Biophys 36:241–252

    Article  CAS  PubMed  Google Scholar 

  175. Werner A, Patti M, Zinad HS, Fearn A, Laude A, Forster IC (2016) Molecular determinants of transport function in zebrafish Slc34a Na-phosphate transporters. Am J Physiol Regul Integr Comp Physiol 311:R1213–R1222

  176. Witten PE, Huysseune A (2009) A comparative view on mechanisms and functions of skeletal remodelling in teleost fish, with special emphasis on osteoclasts and their function. Biol Rev Camb Philos Soc 84:315–346

    Article  PubMed  Google Scholar 

  177. Wolbach RA (1970) Phlorizin and renal phosphate secretion in the spiny dogfish Squalus acanthias. Am J Physiol 219:886–888

    Article  CAS  PubMed  Google Scholar 

  178. Yamashita K, Koide Y, Itoh H, Kawada N, Kawauchi H (1995) The complete amino acid sequence of chum salmon stanniocalcin, a calcium-regulating hormone in teleosts. Mol Cell Endocrinol 112:159–167

    Article  CAS  PubMed  Google Scholar 

  179. Yan YL, Bhattacharya P, He XJ, Ponugoti B, Marquardt B, Layman J, Grunloh M, Postlethwait JH, Rubin DA (2012) Duplicated zebrafish co-orthologs of parathyroid hormone-related peptide (PTHrP, Pthlh) play different roles in craniofacial skeletogenesis. J Endocrinol 214:421–435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  180. Yang JH, Zhao ZH, Hou JF, Zhou ZL, Deng YF, Dai JJ (2013) Expression of TRPV6 and CaBP-D28k in the egg shell gland (uterus) during the oviposition cycle of the laying hen. Br Poult Sci 54:398–406

    CAS  PubMed  Google Scholar 

  181. Yeung BH, Law AY, Wong CK (2012) Evolution and roles of stanniocalcin. Mol Cell Endocrinol 349:272–280

    Article  CAS  PubMed  Google Scholar 

  182. Zhu Y, Qiu X, Ding QL, Duan MM, Wang CF (2014) Combined effects of dietary phytase and organic acid on growth and phosphorus utilization of juvenile yellow catfish Pelteobagrus fulvidraco. Aquaculture 430:1–8

    Article  CAS  Google Scholar 

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Funding

This work and experimental findings therein were funded by the Northern Counties Kidney Research Fund (to Andreas Werner).

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  1. Laboratory of General Physiology, Department of Biological and Environmental Sciences and Technologies, University of Salento, Lecce, Italy

    Tiziano Verri

  2. Epithelial Research Group, Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle upon Tyne, UK

    Andreas Werner

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This article is part of the special issue on Phosphate transport in Pflügers Archiv – European Journal of Physiology

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Verri, T., Werner, A. Type II Na+-phosphate Cotransporters and Phosphate Balance in Teleost Fish. Pflugers Arch - Eur J Physiol 471, 193–212 (2019). https://doi.org/10.1007/s00424-018-2239-4

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