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Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1992 Sep 15;89(18):8414–8418. doi: 10.1073/pnas.89.18.8414

Isoforms of the Na,K-ATPase are present in both axons and dendrites of hippocampal neurons in culture.

G Pietrini 1, M Matteoli 1, G Banker 1, M J Caplan 1
PMCID: PMC49930  PMID: 1326755

Abstract

The distributions of isoforms of the Na,K-ATPase alpha subunit were determined in mature cultured hippocampal neurons and in a polarized epithelial cell line. We find that hippocampal neurons express the alpha 1 and alpha 3 isoforms in the membranes of both axons and dendrites. In contrast the alpha 1 and alpha 3 proteins are exclusively basolateral when expressed endogenously or by stable transfection in renal epithelial cells. These data suggest that epithelial cells and hippocampal neurons localize these proteins by different mechanisms. These observations contrast with those made for the vesicular stomatitis virus and the influenza glycoproteins, which are polarized in both epithelial and neuronal cells.

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Selected References

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  1. Bayer S. A. Development of the hippocampal region in the rat. I. Neurogenesis examined with 3H-thymidine autoradiography. J Comp Neurol. 1980 Mar 1;190(1):87–114. doi: 10.1002/cne.901900107. [DOI] [PubMed] [Google Scholar]
  2. Brewer C. B., Roth M. G. A single amino acid change in the cytoplasmic domain alters the polarized delivery of influenza virus hemagglutinin. J Cell Biol. 1991 Aug;114(3):413–421. doi: 10.1083/jcb.114.3.413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Brines M. L., Gulanski B. I., Gilmore-Hebert M., Greene A. L., Benz E. J., Jr, Robbins R. J. Cytoarchitectural relationships between [3H]ouabain binding and mRNA for isoforms of the sodium pump catalytic subunit in rat brain. Brain Res Mol Brain Res. 1991 May;10(2):139–150. doi: 10.1016/0169-328x(91)90104-6. [DOI] [PubMed] [Google Scholar]
  4. Cameron P. L., Südhof T. C., Jahn R., De Camilli P. Colocalization of synaptophysin with transferrin receptors: implications for synaptic vesicle biogenesis. J Cell Biol. 1991 Oct;115(1):151–164. doi: 10.1083/jcb.115.1.151. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cáceres A., Banker G. A., Binder L. Immunocytochemical localization of tubulin and microtubule-associated protein 2 during the development of hippocampal neurons in culture. J Neurosci. 1986 Mar;6(3):714–722. doi: 10.1523/JNEUROSCI.06-03-00714.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. De Almeida J. B., Stow J. L. Disruption of microtubules alters polarity of basement membrane proteoglycan secretion in epithelial cells. Am J Physiol. 1991 Jul;261(1 Pt 1):C691–C700. doi: 10.1152/ajpcell.1991.261.1.C691. [DOI] [PubMed] [Google Scholar]
  7. De Camilli P., Miller P. E., Navone F., Theurkauf W. E., Vallee R. B. Distribution of microtubule-associated protein 2 in the nervous system of the rat studied by immunofluorescence. Neuroscience. 1984 Apr;11(4):817–846. [PubMed] [Google Scholar]
  8. Dotti C. G., Parton R. G., Simons K. Polarized sorting of glypiated proteins in hippocampal neurons. Nature. 1991 Jan 10;349(6305):158–161. doi: 10.1038/349158a0. [DOI] [PubMed] [Google Scholar]
  9. Dotti C. G., Simons K. Polarized sorting of viral glycoproteins to the axon and dendrites of hippocampal neurons in culture. Cell. 1990 Jul 13;62(1):63–72. doi: 10.1016/0092-8674(90)90240-f. [DOI] [PubMed] [Google Scholar]
  10. Geering K., Theulaz I., Verrey F., Häuptle M. T., Rossier B. C. A role for the beta-subunit in the expression of functional Na+-K+-ATPase in Xenopus oocytes. Am J Physiol. 1989 Nov;257(5 Pt 1):C851–C858. doi: 10.1152/ajpcell.1989.257.5.C851. [DOI] [PubMed] [Google Scholar]
  11. Gloor S., Antonicek H., Sweadner K. J., Pagliusi S., Frank R., Moos M., Schachner M. The adhesion molecule on glia (AMOG) is a homologue of the beta subunit of the Na,K-ATPase. J Cell Biol. 1990 Jan;110(1):165–174. doi: 10.1083/jcb.110.1.165. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Good P. J., Richter K., Dawid I. B. A nervous system-specific isotype of the beta subunit of Na+,K(+)-ATPase expressed during early development of Xenopus laevis. Proc Natl Acad Sci U S A. 1990 Dec;87(23):9088–9092. doi: 10.1073/pnas.87.23.9088. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Goslin K., Schreyer D. J., Skene J. H., Banker G. Changes in the distribution of GAP-43 during the development of neuronal polarity. J Neurosci. 1990 Feb;10(2):588–602. doi: 10.1523/JNEUROSCI.10-02-00588.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gundersen D., Orlowski J., Rodriguez-Boulan E. Apical polarity of Na,K-ATPase in retinal pigment epithelium is linked to a reversal of the ankyrin-fodrin submembrane cytoskeleton. J Cell Biol. 1991 Mar;112(5):863–872. doi: 10.1083/jcb.112.5.863. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hammerton R. W., Krzeminski K. A., Mays R. W., Ryan T. A., Wollner D. A., Nelson W. J. Mechanism for regulating cell surface distribution of Na+,K(+)-ATPase in polarized epithelial cells. Science. 1991 Nov 8;254(5033):847–850. doi: 10.1126/science.1658934. [DOI] [PubMed] [Google Scholar]
  16. Jewell E. A., Lingrel J. B. Comparison of the substrate dependence properties of the rat Na,K-ATPase alpha 1, alpha 2, and alpha 3 isoforms expressed in HeLa cells. J Biol Chem. 1991 Sep 5;266(25):16925–16930. [PubMed] [Google Scholar]
  17. Kashgarian M., Biemesderfer D., Caplan M., Forbush B., 3rd Monoclonal antibody to Na,K-ATPase: immunocytochemical localization along nephron segments. Kidney Int. 1985 Dec;28(6):899–913. doi: 10.1038/ki.1985.216. [DOI] [PubMed] [Google Scholar]
  18. Kordeli E., Bennett V. Distinct ankyrin isoforms at neuron cell bodies and nodes of Ranvier resolved using erythrocyte ankyrin-deficient mice. J Cell Biol. 1991 Sep;114(6):1243–1259. doi: 10.1083/jcb.114.6.1243. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kunimoto M., Otto E., Bennett V. A new 440-kD isoform is the major ankyrin in neonatal rat brain. J Cell Biol. 1991 Dec;115(5):1319–1331. doi: 10.1083/jcb.115.5.1319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lazarides E., Nelson W. J., Kasamatsu T. Segregation of two spectrin forms in the chicken optic system: a mechanism for establishing restricted membrane-cytoskeletal domains in neurons. Cell. 1984 Feb;36(2):269–278. doi: 10.1016/0092-8674(84)90220-4. [DOI] [PubMed] [Google Scholar]
  21. Lerner R. A., Green N., Alexander H., Liu F. T., Sutcliffe J. G., Shinnick T. M. Chemically synthesized peptides predicted from the nucleotide sequence of the hepatitis B virus genome elicit antibodies reactive with the native envelope protein of Dane particles. Proc Natl Acad Sci U S A. 1981 Jun;78(6):3403–3407. doi: 10.1073/pnas.78.6.3403. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lingrel J. B., Orlowski J., Shull M. M., Price E. M. Molecular genetics of Na,K-ATPase. Prog Nucleic Acid Res Mol Biol. 1990;38:37–89. doi: 10.1016/s0079-6603(08)60708-4. [DOI] [PubMed] [Google Scholar]
  23. Lisanti M. P., Le Bivic A., Saltiel A. R., Rodriguez-Boulan E. Preferred apical distribution of glycosyl-phosphatidylinositol (GPI) anchored proteins: a highly conserved feature of the polarized epithelial cell phenotype. J Membr Biol. 1990 Feb;113(2):155–167. doi: 10.1007/BF01872889. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. McGrail K. M., Phillips J. M., Sweadner K. J. Immunofluorescent localization of three Na,K-ATPase isozymes in the rat central nervous system: both neurons and glia can express more than one Na,K-ATPase. J Neurosci. 1991 Feb;11(2):381–391. doi: 10.1523/JNEUROSCI.11-02-00381.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Meldolesi J., Corte G., Pietrini G., Borgese N. Localization and biosynthesis of NADH-cytochrome b5 reductase, an integral membrane protein, in rat liver cells. II. Evidence that a single enzyme accounts for the activity in its various subcellular locations. J Cell Biol. 1980 Jun;85(3):516–526. doi: 10.1083/jcb.85.3.516. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Mercer R. W., Schneider J. W., Savitz A., Emanuel J., Benz E. J., Jr, Levenson R. Rat-brain Na,K-ATPase beta-chain gene: primary structure, tissue-specific expression, and amplification in ouabain-resistant HeLa C+ cells. Mol Cell Biol. 1986 Nov;6(11):3884–3890. doi: 10.1128/mcb.6.11.3884. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Morrow J. S., Cianci C. D., Ardito T., Mann A. S., Kashgarian M. Ankyrin links fodrin to the alpha subunit of Na,K-ATPase in Madin-Darby canine kidney cells and in intact renal tubule cells. J Cell Biol. 1989 Feb;108(2):455–465. doi: 10.1083/jcb.108.2.455. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Nelson W. J., Veshnock P. J. Ankyrin binding to (Na+ + K+)ATPase and implications for the organization of membrane domains in polarized cells. Nature. 1987 Aug 6;328(6130):533–536. doi: 10.1038/328533a0. [DOI] [PubMed] [Google Scholar]
  29. Puddington L., Woodgett C., Rose J. K. Replacement of the cytoplasmic domain alters sorting of a viral glycoprotein in polarized cells. Proc Natl Acad Sci U S A. 1987 May;84(9):2756–2760. doi: 10.1073/pnas.84.9.2756. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Schlessinger A. R., Cowan W. M., Swanson L. W. The time of origin of neurons in Ammon's horn and the associated retrohippocampal fields. Anat Embryol (Berl) 1978 Aug 18;154(2):153–173. doi: 10.1007/BF00304660. [DOI] [PubMed] [Google Scholar]
  31. Shull G. E., Greeb J., Lingrel J. B. Molecular cloning of three distinct forms of the Na+,K+-ATPase alpha-subunit from rat brain. Biochemistry. 1986 Dec 16;25(25):8125–8132. doi: 10.1021/bi00373a001. [DOI] [PubMed] [Google Scholar]
  32. Shyjan A. W., Gottardi C., Levenson R. The Na,K-ATPase beta 2 subunit is expressed in rat brain and copurifies with Na,K-ATPase activity. J Biol Chem. 1990 Mar 25;265(9):5166–5169. [PubMed] [Google Scholar]
  33. Sompayrac L. M., Danna K. J. Efficient infection of monkey cells with DNA of simian virus 40. Proc Natl Acad Sci U S A. 1981 Dec;78(12):7575–7578. doi: 10.1073/pnas.78.12.7575. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Sweadner K. J. Isozymes of the Na+/K+-ATPase. Biochim Biophys Acta. 1989 May 9;988(2):185–220. doi: 10.1016/0304-4157(89)90019-1. [DOI] [PubMed] [Google Scholar]
  35. Takeyasu K., Tamkun M. M., Renaud K. J., Fambrough D. M. Ouabain-sensitive (Na+ + K+)-ATPase activity expressed in mouse L cells by transfection with DNA encoding the alpha-subunit of an avian sodium pump. J Biol Chem. 1988 Mar 25;263(9):4347–4354. [PubMed] [Google Scholar]
  36. Tokuyasu K. T. Application of cryoultramicrotomy to immunocytochemistry. J Microsc. 1986 Aug;143(Pt 2):139–149. doi: 10.1111/j.1365-2818.1986.tb02772.x. [DOI] [PubMed] [Google Scholar]
  37. Tokuyasu K. T. Use of poly(vinylpyrrolidone) and poly(vinyl alcohol) for cryoultramicrotomy. Histochem J. 1989 Mar;21(3):163–171. doi: 10.1007/BF01007491. [DOI] [PubMed] [Google Scholar]

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