Animals; Gene Expression Regulation, Developmental; In Situ Hybridization; Kidney/embryology/metabolism; Organ Specificity; Organogenesis; Sodium-Phosphate Cotransporter Proteins, Type III/genetics; Xenopus Proteins/genetics; Xenopus laevis/embryology/genetics/metabolism; Zebrafish/embryology/genetics/metabolism; Zebrafish Proteins/genetics
Abstract :
[en] The embryonic pronephric kidneys of Xenopus and zebrafish serve as models to study vertebrate nephrogenesis. Recently, multiple subdomains within the Xenopus pronephros have been defined based on the expression of several transport proteins. In contrast, very few studies on the expression of renal transporters have been conducted in zebrafish. We have recently shown that the anterior and posterior segments of the zebrafish pronephric duct may correspond to the proximal tubule and distal tubule/duct compartments of the Xenopus and higher vertebrate pronephros, respectively. Here, we report the embryonic expression pattern of the Na(+)/PO(4) cotransporter SLC20A1 (PiT1/Glvr-1) gene encoding a type III sodium-dependent phosphate cotransporter in Xenopus and zebrafish. In Xenopus, SLC20A1 mRNA is expressed in the somitic mesoderm and lower level of expression is detected in the neural tube, eye, and neural crest cells. From stage 25, SLC20A1 is also detectable in the developing pronephros where expression is restricted to the late portion of the distal pronephric tubules. In zebrafish, SLC20A1 is transcribed from mid-somitogenesis in the anterior part of the pronephros where its expression corresponds to the rostral portion of the expression of other proximal tubule-specific markers. Outside the pronephros, lower level of SLC20A1 expression is also observed in the posterior cardinal and caudal veins. Based on the SLC20A1 expression domain and that of other transporters, four segments have been defined within the zebrafish pronephros. Together, our data reveal that the zebrafish and Xenopus pronephros have non-identical proximo-distal organizations.
Research Center/Unit :
Giga-Development and Stem Cells - ULiège
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Nichane, Massimo; Université Libre de Bruxelles - ULB > Institut de Biologie et de Médecine Moléculaires > Laboratoire d’Embryologie Moléculaire
Van Campenhout, Claude; Université Libre de Bruxelles - ULB > Institut de Biologie et de Médecine Moléculaires > Laboratoire d’Embryologie Moléculaire
Pendeville, Helene; Université de Liège - ULiège > Département des sciences de la vie > GIGA-R : Biologie et génétique moléculaire
Voz, Marianne ; Université de Liège - ULiège > Département des sciences de la vie > GIGA-R : Biologie et génétique moléculaire
Bellefroid, Eric J.; Université Libre de Bruxelles - ULB > Institut de Biologie et de Médecine Moléculaires > Laboratoire d’Embryologie Moléculaire
Language :
English
Title :
The Na+/PO4 cotransporter SLC20A1 gene labels distinct restricted subdomains of the developing pronephros in Xenopus and zebrafish embryos.
Biber J., Custer M., Werner A., Kaissling B., and Murer H. Localization of NaPi-1, a Na/Pi cotransporter, in rabbit kidney proximal tubules. II. Localization by immunohistochemistry. Plugers Arch. 424 (1993) 210-215
Broadbent J., and Read E.M. Wholemount in situ hybridization of Xenopus and zebrafish embryos. Methods Mol. Biol. 127 (1999) 57-67
Custer M., Lotscher M., Biber J., Murer H., and Kaissling B. Expression of Na-P(i) cotransport in rat kidney: localization by RT-PCR and immunohistochemistry. Am. J. Physiol. 266 (1994) 764-767
Drummond I.A. Making a zebrafish kidney: a tale of two tubes. Trends Cell Biol. 13 (2003) 357-365
Drummond I.A. Kidney development and disease in the zebrafish. J. Am. Soc. Nephrol. 16 (2005) 299-304
Elger M., Werner A., Herter P., Kohl B., Kinne R.K., and Hentschel H. Na-P(i) cotransport sites in proximal tubule and collecting tubule of winter flounder (Pleuronectes americanus). Am. J. Physiol. 274 (1998) 374-383
Harland R.M. In situ hybridization: an improved whole-mount method for Xenopus embryos. Methods Cell Biol. 36 (1991) 685-695
Hentschel H., Burckhardt B.C., Scholermann B., Kuhne L., Burckhardt G., and Steffgen J. Basolateral localization of flounder Na+-dicarboxylate cotransporter (fNaDC-3) in the kidney of Pleuronectes americanus. Pflugers Arch. 446 (2003) 578-584
Hyodo S., Katoh F., Kaneko T., and Takei Y. A facilitative urea transporter is localized in the renal collecting tubule of the dogfish Triakis scyllia. J. Exp. Biol. 207 (2004) 347-356
Johann S.V., Gibbons J.J., and O'Hara B. GLVR1, a receptor forgibbon ape leukemia virus, is homologous to a phosphate permease of Neurospora and is expressed at high levels in the brain and thymus. J. Virol. 66 (1992) 1635-1640
Jones E.A. Xenopus: a prince among models for pronephric kidney development. J. Am. Soc. Nephrol. 16 (2005) 313-321
Kavanaugh M.P., Miller D.G., Zhang W., Law W., Kozak S.L., Kabat D., and Miller A.D. Cell-surface receptors for gibbon ape leukemia virus and amphotropic murine retrovirus are inducible sodium-dependent phosphate symporters. Proc. Natl. Acad. Sci. USA 91 (1994) 7071-7075
Kavanaugh M.P., and Kabat D. Identification and characterization of a widely expressed phosphate transporter/retrovirus receptor family. Kidney Int. 49 (1996) 959-963
Leung JC., Barac-Nieto M., Hering-Smith K., and Silverstein DM. Expression of the rat renal PiT-2 phosphate transporter. Horm. Metab. Res. 37 (2005) 265-269
Madjdpour C., Bacic D., Kaissling B., Murer H., and Biber J. Segment-specific expression of sodium-phosphate cotransporters NaPi-IIa and -IIc and interacting proteins in mouse renal proximal tubules. Pflugers Arch. 448 (2004) 402-410
Magagnin S., Werner A., Markovich D., Sorribas V., Stange G., Biber J., and Murer H. Expression cloning of human and rat renal cortex Na/Pi cotransport. Proc. Natl. Acad. Sci. USA 90 (1993) 5979-5983
Majumdar A., Lun K., Brand M., and Drummond A. Zebrafish no isthmus reveals a role for pax2.1 in tubule diferentiation and patterning events in the pronephric primordia. Development 127 (2000) 2089-2098
Marcos-Gutiérrez C., Wilson S., Holder N., and Pachnis V. The zebrafish homologue of the ret receptor and its pattern of expression during embryogenesis. Oncogene 14 (1997) 879-889
Mavropoulos A., Devos N., Biemar F., Zecchin E., Argenton F., Edlund H., Motte P., Martial J.A., and Peers B. sox4b is a key player of pancreatic alpha cell differentiation in zebrafish. Dev Biol. 285 (2005) 211-223
Miyazaki H., Kaneko T., Uchida S., Sasaki S., and Takei Y. Kidney-specific chloride channel, OmCLC-K, predominantly expressed in the diluting segment of freshwater-adapted tilapia kidney. Proc. Natl. Acad. Sci. USA 99 (2002) 15782-15787
Nieuwkoop P.D., and Faber J. A Normal Table of Xenopus laevis (Daudin) (1997), North Holland, Amsterdam, The Netherlands
O'Hara B., Johann S.V., Klinger H.P., Blair D.G., Rubinson H., Dunn K.J., Sass P., Vitek S.M., and Robins T. Characterization of a human gene conferring sensitivity to infection by gibbon ape leukemia virus. Cell Growth Differ. 1 (1990) 119-127
Olah Z., Lehel C., Anderson W.B., Eiden M.V., and Wilson C.A. The cellular receptor for gibbon ape leukemia virus is a novel high affinity sodium-dependent phosphate transporter. J. Biol. Chem. 269 (1994) 25426-25431
Ryffel G.U. What can a frog tell us about kidney development. Nephron Exp. Nephrol. 94 (2003) 35-43
Tenenhouse H.S., Roy S., Martel J., and Gauthier C. Differential expression, abundance, and regulation of Na+-phosphate cotransporter genes in murine kidney. Am. J. Physiol. 275 (1998) 527-534
Thisse, B., Pflumio, S., Fürthauer, M., Loppin, B., Heyer, V., Degrave, A., Woehl, R., Lux, A., Steffan, T., Charbonnier, X.Q., Thisse, C., 2001. Expression of the zebrafish genome during embryogenesis (NIH R01 RR15402). ZFIN Direct Data Submission.
Vize P.D. The chloride conductance channel ClC-K is a specific marker for the Xenopus pronephric distal tubule and duct. Gene Expr. Patterns 3 (2003) 347-350
Werner A., Moore M.L., Mantei J., Biber G., Semenza G., and Murer H. Cloning and expression of cDNA for a Na/Pi cotransport system of kidney cortex. Proc. Natl. Acad. Sci. USA 88 (1991) 9608-9612
Zhou X., and Vize P.D. Proximo-distal specialization of epithelial transport processes within the Xenopus pronephric kidney tubules. Dev. Biol. 271 (2004) 322-338
Zhou X., and Vize P.D. Amino acid cotransporter SLC3A2 is selectively expressed in the early proximal segment of Xenopus pronephric kidney nephrons. Gene Expr. Patterns 5 (2005) 774-777
Zhou X., and Vize P.D. Pronephric regulation of acid-base balance; coexpression of carbonic anhydrase type 2 and sodium-bicarbonate cotransporter-1 in the late distal segment. Dev. Dyn. 233 (2005) 142-144