Abstract
In this study, two isoforms slc34a2 genes (type IIb sodium-dependent phosphate cotransporter), slc34a2a2 and slc34a2b, were cloned from intestine and kidney of yellow catfish (Pelteobagrus fulvidraco), with rapid amplification of cDNA ends. The structure differences and the regulation effects of dietary VD3 under low phosphorus were compared among three isoforms of slc34a2 in yellow catfish. The predicted Slc34a2a2 and Slc34a2b proteins match 65 % and 53.8 % sequence identity, with Slc34a2a1, respectively. The membrane-spanning domains were different among these three isoforms. Intestinal Slc34a2a1 and Slc34a2a2 proteins had eight and eleven transmembrane domains, while renal Slc34a2b protein had nine. The tissue distribution study showed that same as slc34a2a1, slc34a2a2 mRNA was mainly distributed in intestine and slc34a2b mRNA in kidney. The effect of vitamin D3 (VD3) level on slc34a2 subfamily expression under low-phosphate conditions, induced by the addition of 0 (VD0), 324 (VD1), 1243 (VD2), 3621 (VD3), 8040 (VD4), or 22700 (VD5) IU VD3/kg feed, was assessed by qPCR. The dose-responsive expression of intestinal slc34a2a2 and high expression of intestinal slc34a2a2 in VD5 together with peak expression of kidney slc34a2b in VD3 coincided with the accumulation of body phosphate content. These data suggested that appropriate level of dietary VD3 up-regulated slc34a2a1, slc34a2a2, and slc34a2b mRNA levels, which increased phosphate retention. In conclusion, the current study provided another possible approach to improve dietary phosphate utilization by adding appropriate level of VD3 to a low-phosphate diet to regulate intestinal and renal slc34a2 gene expression and thus minimize the excretion of phosphorus in yellow catfish.
Similar content being viewed by others
References
Berndt T, Kumar R (2007) Phosphatonins and the regulation of phosphate homeostasis. Annu Rev Physiol 69:341–359
Cerri MF, de Rezende LCD, Paes MF, Silva IV, Rangel LBA, Rezende LC (2010) The cotransporter NaPi-IIb: characteristics, regulation and its role in carcinogenesis. Appl Cancer Res 30(1):197–203
Chen P, Tang Q, Wang C (2015) 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(1):51–64
Deer DM, Lampel KA, González-Escalona N (2010) A versatile internal control for use as DNA in real-time PCR and as RNA in real-time reverse transcription PCR assays. Lett Appl Microbial 50(4):366–372
Fanning AS, Anderson JM (1996) Protein-protein interactions: PDZ domain networks. Curr Biol 6:1385–1388
Fenwick JC, Vermette MG (1989) Vitamin D and renal handling of phosphate in American eels. Fish Physiol Biochem 7:351–358
Forster IC, Köhler K, Biber J, Murer H (2002) Forging the link between structure and function of electrogenic cotransporters: the renal type IIa Na/Pi cotransporter as a case study. Prog Biophys Mol Biol 80:69–108
Friedlaender MM, Wald H, Dranitzki-Elhalel M, Zajicek HK, Levi M, Popovtzer MM (2001) Vitamin D reduces renal NaPi-2 in PTH-infused rats: complexity of vitamin D action on renal Pi handling. Am J Physiol Ren 281:428–433
Gisler SM, Stagljar I, Traebert M, Bacic D, Biber J, Murer H (2001) Interaction of the type IIa Na/Pi cotransporter with PDZ proteins. J Biol Chem 276:9206–9213
Graham C, Nalbant P, Scholermann B, Hentschel H, Kinne RK, Werner A (2003) Characterization of a type IIb sodium-phosphate cotransporter from zebra fish (Danio rerio) kidney. Am J Physiol Ren 284:727–736
Haussler MR, Whitfield GK, Kaneko I, Haussler CA, Hsieh D, Hsieh JC, Jurutka PW (2013) Molecular mechanisms of vitamin D action. Calcif Tissue Int 92(2):77–98
Hayes G, Busch A, Lötscher M, Waldegger S, Lang F, Verrey F, Biber J, Murer H (1994) Role of N-linked glycosylation in rat renal Na/Pi cotransport. J Biol Chem 269:24143–24149
Katai K, Miyamoto K, Kishida S, Segawa H, Nii T, Tanaka H, Tani Y, Arai H, Tatsumi S, Morita K, Taketani Y, Takeda E (1999) Regulation of intestinal Na-dependent phosphate co-transporters by a low-phosphate diet and 1,25-dihydroxyvitamin D3. Biochem J 343:705–712
Kido S, Kaneko I, Tatsumi S, Segawa H, Miyamoto K (2013) Vitamin D and type II sodium-dependent phosphate cotransporters. Contrib Nephrol 180:86–97
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 Ren 270:937–944
Köhler K, Forster IC, Stange G, Biber J, Murer H (2002) Identification of functionally important sites in the first intracellular loop of the Na/Pi-IIa cotransporter. Am J Physiol 282:687–696
Kurnik BRC, Hruska KA (1984) Effects of 1,25-dihydroxycholecalciferol on phosphate transport in vitamin D-deprived rats. Am J Physiol 247:177–184
Kurnik BRC, Hruska KA (1985) Mechanism of stimulation of renal phosphate transport by 1,25-dihydroxycholecalciferol. Biochim Biophys Acta 817:42–50
Lambert G, Traebert M, Hernando N, Biber J, Murer H (1999) Studies on the topology of the renal type II NaPi-cotransporter. Eur J Physiol 437:972–978
Lee DBN, Walling MW, Brautbar N (1986) Intestinal phosphate absorption: influence of vitamin D and non-vitamin D factors. Am J Physiol 250:369–373
Lock EJ, Waagbø R, Wendelaar Bonga S, Flik G (2010) The significance of vitamin D for fish: a review. Aquac Nutr 16:100–116
Marks J, Debnam ES, Unwin RJ (2010) Phosphate homeostasis and the renal gastrointestinal axis. Am J Physiol Ren 299:285–296
Mchaffie GS, Graham C, Kohl B, Strunck-Warnecke U, Werner A (2007) The role of an intracellular cysteine stretch in the sorting of the type II Na/phosphate cotransporter. Biochim Biophys Acta 1768(9):2099–2106
Møbjerg N, Werner A, Hansen SM, Novak I (2007) Physiological and molecular mechanisms of inorganic phosphate handling in the toad Bufo bufo. Eur J Physiol 454:101–113
Mohammed A, Gibney MJ, Taylor TG (1991) The effects of dietary levels of inorganic phosphorus, calcium and cholecalciferol on the digestibility of phytate-P by the chick. Br J Nutr 66:251–259
Murer H, Hernando N, Forster I, Biber J (2001) Molecular mechanisms in proximal tubular and small intestinal phosphate reabsorption (plenary lecture). Mol Membr Biol 18(1):3–11
Murer H, Forster I, Biber J (2004) The sodium phosphate cotransporter family SLC34. Pflüg Arch 447(5):763–767
Nalbant P, Böhmer C, Dehmelt L, Wehner F, Werner A (1999) Functional characterization of a Na/P cotransporter (NaP-II) from zebra fish and identification of related transcripts. J Physiol 520:79–89
NRC (2011) Nutrient requirements of fish and shrimp. National Academies Press, Washington, pp 168–169
Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29(9):45
Radanovic T, Gisler SM, Biber J, Murer H (2006) Topology of the type IIa Na+/Pi cotransporter. J Membr Biol 212:41–49
Schultz AG, Guffey SC, Clifford AM, Goss GG (2014) Phosphate absorption across multiple epithelia in the pacific hagfish (Eptatretus stoutii). Am J Physiol Regul Integr Comp Physiol 307:R643–R652
Srivastav AK, Srivastav SK, Sasayama Y, Suzuki N, Norman AW (1997a) Vitamin D metabolites affect serum calcium and phosphate in freshwater catfish (Heteropneustes fossilis). Zool Sci 14:743–746
Srivastav AK, Tiwari PR, Srivastav SK, Sasayama Y, Suzuki N (1997b) Vitamin D3-induced calcemic and phosphatemic responses in the freshwater mud eel (Amphipnous cuchiamaintained) in different calcium environments. Braz J Med Biol Res 30:1343–1348
Sugiura SH (2009) Identification of intestinal phosphate transporters in fishes and shellfishes. Fish Sci 75:99–108
Sugiura SH, Ferraris RP (2004) Dietary phosphorus-responsive genes in the intestine, pyloric ceca, and kidney of rainbow trout. Am J Physiol Reg 287:541–550
Swarup K, Das VK, Norman AW (1991) Dose-dependent vitamin D3 and 1,25-dihydroxyvitamin D3-induced hypercalcemia and hyperphosphatemia in male cyprinoid (Cyprinus carpio). Comp Biochem Physiol 100A:445–447
Wagner CA, Hernando N, Forster IC, Biber J (2014) The SLC34 family of sodium-dependent phosphate transporters. Pflug Arch 466(1):139–153
Werner A, Kinne RK (2001) Evolution of the Na–P(i) cotransport systems. Am J Physiol Reg 280:301–312
Werner A, Murer H, Kinne RK (1994) Cloning and expression of a renal Na–Pi cotransport system from flounder. Am J Physiol 267:311–317
Werner A, Dehmelt L, Nalbant P (1998) Na+-dependent phosphate cotransporters: the NaPi protein families. J Exp Biol 201:3135–3142
Xu H, Bai L, Collins JF, Ghishan FK (2002) Age-dependent regulation of rat intestinal type IIb sodium-phosphate cotransporter by 1,25-(OH)(2) vitamin D(3). Am J Physiol Cell Physiol 282(3):487–493
Zhao Y, Gul Y, Li S, Wang W (2011) Cloning, identification and accurate normalization expression analysis of PPARα gene by GeNorm in Megalobrama amblycephala. Fish Shellfish Immunol 31:462–468
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
Acknowledgments
This research was funded by the National Natural Science Foundation of China (Project Nos. 31172421 and 31672667).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Chen, P., Huang, Y., Bayir, A. et al. 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 (2017). https://doi.org/10.1007/s10695-016-0282-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10695-016-0282-7