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Expression of the Skate (Raja erinacea) AE1 Osmolyte Channel in Xenopus laevis Oocytes: Monovalent Cation Permeability

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Abstract

The aim of this study was to express the cloned skate anion exchanger 1 (skAE1) in Xenopus oocytes and determine whether the differences in monovalent cation permeabilities in hypotonically stimulated skate and trout erythrocytes could be due to differences in the presence or absence of intracellular channel regulators between the two species or in the intrinsic permeability properties of the channels themselves. The expressed protein (skAE1) was inserted into the oocyte cell membrane and facilitated both Cl− exchange and taurine transport. Expression of skAE1 in oocytes showed similar monovalent cation permeabilities as previously reported for skate erythrocytes and different from both trout erythrocytes and trAE1 expressed in Xenopus oocytes. These results show that the skAE1 expressed in oocytes functions in a manner similar to that of the osmolyte channel in hypotonically activated skate erythrocytes and supports the hypothesis that differences in the monovalent cation permeabilities of the osmolyte channels in skate and trout RBCs resides in the differences in permeability properties of the channels between the two species.

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References

  1. E. Davis M. Musch L. Goldstein (2002) ArticleTitleTransfection of an inducible trout anion exchanger (AE1) into HEK-EcR cells J. Exp. Zool. 293 46–57 Occurrence Handle10.1002/jez.10111 Occurrence Handle12115918

    Article  PubMed  Google Scholar 

  2. E. Davis-Amaral M. Musch L. Goldstein (1996) ArticleTitleChloride and taurine effluxes occur by different pathways in skate erythrocytes Am. J. Physiol. 271 R1544–R1549 Occurrence Handle8997351

    PubMed  Google Scholar 

  3. B. Fievet N. Gabillat F. Borgese R. Motais (1995) ArticleTitleExpression of band 3 anion exchanger induces chloride current and taurine transport: structure-function analysis EMBO J. 14 5158–5169 Occurrence Handle7489705

    PubMed  Google Scholar 

  4. B. Fievet F. Perset N. Gabillat H. Guizouarn F. Borgese P. Ripoche R. Motais (1998) ArticleTitleTransport of uncharged organic solutes in Xenopus oocytes expressing red cell anion exchangers (AE1) Proc. Natl. Acad. Sci. USA 95 10996–11001 Occurrence Handle10.1073/pnas.95.18.10996 Occurrence Handle9724818

    Article  PubMed  Google Scholar 

  5. F. Garcia-Romeu A.R. Cossins R. Motais (1991) ArticleTitleCell volume regulation by trout erythrocytes: characteristics of the transport systems activated by hypotonic swelling J. Physiol. 440 547–567 Occurrence Handle1804976

    PubMed  Google Scholar 

  6. L. Goldstein S. Brill (1990) ArticleTitleIsosmotic swelling of skate (Raja erinacea) red blood cells causes a volume regulatory release of intracellular taurine J. Exp. Zool. 253 132–138 Occurrence Handle10.1002/jez.1402530203

    Article  Google Scholar 

  7. L. Goldstein D.L. Koomoa M.W. Musch (2003) ArticleTitleATP release from hypotonically stressed skate RBC: Potential role in osmolyte channel regulation J. Exp. Zool. 296 160–163 Occurrence Handle10.1002/jez.a.10228

    Article  Google Scholar 

  8. H. Guizouarn N. Gabillat R. Motais F. Borgese (2001) ArticleTitleMultiple transport functions of a red blood cell anion exchanger, tAE1: its role in cell volume regulation J. Physiol. 535 497–506 Occurrence Handle10.1111/j.1469-7793.2001.t01-1-00497.x Occurrence Handle11533139

    Article  PubMed  Google Scholar 

  9. H. Guizouarn M. Musch L. Goldstein (2003) ArticleTitleEvidence for the presence of three different anion exchangers in a red cell. Functional expression studies in Xenopus oocytes J. Membrane. Biol. 193 109–120 Occurrence Handle10.1007/s00232-002-2012-6

    Article  Google Scholar 

  10. J.K. Haynes L. Goldstein (1993) ArticleTitleVolume-regulatory amino acid transport in red blood cells of the little skate, Raja erinacea Am. J. Physiol. 265 R173–R179 Occurrence Handle8342684

    PubMed  Google Scholar 

  11. D.L. Koomoa M. Musch L. Goldstein (2002) ArticleTitleComparison of the osmolyte transport properties induced by trAE1 versus I clswell in Xenopus oocytes J. Membrane Biol. 185 57–63 Occurrence Handle10.1007/s00232-001-0109-y

    Article  Google Scholar 

  12. F. Lang M. Ritter H. Volki D. Haussinger (1993) ArticleTitleThe biological significance of cell volume Renal Physiol. Biochem. 16 48–65 Occurrence Handle7684146

    PubMed  Google Scholar 

  13. R. Motais H. Guizouarn F. Garcia-Romeu (1991) ArticleTitleRed cell volume regulation: The pivotal role of ionic strength in controlling swelling-dependent transport systems Biochim. Biophys. Acta 1075 169–180 Occurrence Handle1657175

    PubMed  Google Scholar 

  14. M. Musch E.M. Davis L. Goldstein (1994) ArticleTitleOligomeric forms of skate erythrocyte band 3 J. Biol. Chem. 269 19683–19686 Occurrence Handle8051044

    PubMed  Google Scholar 

  15. M. Musch E.M. Davis-Amaral L. Leibowitz L. Goldstein (1998) ArticleTitleHypotonic-stimulated taurine efflux in skate erythrocytes: regulation by tyrosine phosphatase activity Am. J. Physiol. 274 R1677–R1686 Occurrence Handle9608023

    PubMed  Google Scholar 

  16. Y. Okada (1997) ArticleTitleVolume expansion-sensing outward-rectifier Cl− channel: fresh start to the molecular identity and volume sensor Am. J. Physiol. 273 C755–C789 Occurrence Handle9316396

    PubMed  Google Scholar 

  17. D. Perlman L. Goldstein (1999) ArticleTitleOrganic osmolyte channels in cell volume regulation in vertebrates J. Exp. Zool. 283 725–733 Occurrence Handle10.1002/(SICI)1097-010X(19990601)283:7<725::AID-JEZ10>3.0.CO;2-# Occurrence Handle10222593

    Article  PubMed  Google Scholar 

  18. S. Schmieder S. Lindenthal U. Banderali J. Ehrenfeld (1998) ArticleTitleCharacterization of the putative chloride channel xClC-5 expressed in Xenopus laevis oocytes and comparison with endogenous chloride currents J. Physiol. 511 379–393 Occurrence Handle10.1111/j.1469-7793.1998.379bh.x Occurrence Handle9706017

    Article  PubMed  Google Scholar 

  19. K. Wittels E. Hubert M. Musch L. Goldstein (2000) ArticleTitleOsmolyte channel regulation by ionic strength in skate RBC Am. J. Physiol. 279 R69–R76

    Google Scholar 

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Acknowledgments

This work was supported by National Science Foundation Grant IBN-9974350 (to L.G.) and National Institutes of Health Grants DK-38510, DK-47722 and DK-42086 (to M.W.M.). We thank H. Guizouarn for generously donating the plasmid that was used to make the skAE1 cRNA (Laboratoire de Physiologie des Membranes Cellulaires).

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Authors and Affiliations

  1. Division of Biology and Medicine, Brown University, Providence, RI, 02912, USA

    D. -L. T. Koomoa, D. E. Myers & L. Goldstein

  2. Department of Medicine, Inflammatory Bowel Disease Research Center, University of Chicago, Chicago, Illinois, 60637, USA

    M. W. Musch

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  1. D. -L. T. Koomoa
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  2. M. W. Musch
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  3. D. E. Myers
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  4. L. Goldstein
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Correspondence to L. Goldstein.

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Koomoa, D.L.T., Musch, M.W., Myers, D.E. et al. Expression of the Skate (Raja erinacea) AE1 Osmolyte Channel in Xenopus laevis Oocytes: Monovalent Cation Permeability. J Membrane Biol 198, 23–29 (2004). https://doi.org/10.1007/s00232-004-0655-1

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  • DOI: https://doi.org/10.1007/s00232-004-0655-1

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