The Journal of Membrane Biology

, Volume 211, Issue 3, pp 151–161 | Cite as

Functional Links between Membrane Transport and the Spectrin Cytoskeleton

Topical Review

Abstract

Membrane transporters precisely regulate which molecules cross the plasma membrane and when they can cross. In many cases it is also important to regulate where substances can cross the plasma membrane. Consequently, cells have evolved mechanisms to confine and stabilize membrane transport proteins within specific subdomains of the plasma membrane. A number of different transporters (including ion pumps, channels and exchangers) are known to physically associate with the spectrin cytoskeleton, a submembrane complex of spectrin and ankyrin. These proteins form a protein scaffold that assembles within discrete subdomains of the plasma membrane in polarized cells. Recent genetic studies in humans and model organisms have provided the opportunity to test the hypothesis that the spectrin cytoskeleton has a direct role in restricting transporters to specialized domains. Remarkably, genetic defects in spectrin and ankyrin can produce effects on cell physiology that are comparable to knockouts of the transporters themselves.

Keywords

Spectrin Ankyrin Sodium channel Sodium pump Potassium channel Drosophila Genetics 

Notes

Acknowledgement

This work was supported by NIH GM49301.

References

  1. Banuelos S., M. Saraste, K.D. Carugo. 1998. Structural comparisons of calponin homology domains: implications for actin binding. Structure 6:1419–1431PubMedCrossRefGoogle Scholar
  2. Bennett V. 1989. The spectrin-actin junction of erythrocyte membrane skeletons. Biochim. Biophys. Acta 988:107–121PubMedGoogle Scholar
  3. Bennett V., A.J. Baines. 2001. Spectrin and ankyrin-based pathways: Metazoan inventions for integrating cells into tissues. Physiol. Rev. 81:1353–1388PubMedGoogle Scholar
  4. Bennett V., L. Chen. 2001. Ankyrins and cellular targeting of diverse membrane proteins to physiological sites. Curr. Op. Cell Biol. 13:61–67PubMedCrossRefGoogle Scholar
  5. Bennett V., Davis J., W.E. Fowler. 1982. Brain spectrin, a membrane-associated protein related in structure and function to human erythrocyte spectrin. Nature 299:126–131PubMedCrossRefGoogle Scholar
  6. Berghs S., D. Aggujaro, R. Dirkx, E. Maksimova, P. Stabach, J.-M. Mermel, M.-P. Zhang, W. Philbrick, V. Slepnev, T., Ort, M. Solimena. 2000. ΒIV spectrin, a new spectrin localized at axon initial segments and nodes of ranvier in the central and peripheral nervous system. J. Cell Biol. 151:985–1001PubMedCrossRefGoogle Scholar
  7. Bourguignon L.Y.W., H. Jin, N. Iida, N.R. Brandt, S.H. Zhang. 1993. The involvement of ankyrin in the regulation of inositol 1,4,5-triphosphate receptor-mediated internal Ca2+ release from Ca2+ storage vesicles in mouse T-lymphoma cells. J. Biol. Chem. 268:7290–7297PubMedGoogle Scholar
  8. Bretscher A., K. Edwards, R.G. Fehon. 2002. ERM proteins and merlin: integrators at the cell cortex. Nat Rev Mol Cell Biol. 3:586–599PubMedCrossRefGoogle Scholar
  9. Byers T.J., D. Branton. 1985. Visualization of the protein associations in the erythrocyte membrane skeleton. Proc. Natl. Acad. Sci. USA 82:6153–6157PubMedCrossRefGoogle Scholar
  10. Craig S.W., J.V. Pardo. 1983. Gamma actin, spectrin, and intermediate filament proteins colocalize with vinculin at costameres, myofibril-to-sarcolemma attachment sites. Cell Motil. 3:449–462PubMedCrossRefGoogle Scholar
  11. Chung H. J., Y. N. Jan, L.Y. Jan. 2006. Polarized axonal surface expression of neuronal KCNQ channels is mediated by multiple signals in the KCNQ2 and KCNQ3 C-erminal domains. Proc. Natl Acad. Sci. USA 103: 8870–8875PubMedCrossRefGoogle Scholar
  12. Das A., S. Srinivasan, C. Base, P. Ng, D. Pruden, R.R. Dubreuil (2003) Characterization of a new Drosophila anion exchanger (DAE) and its dependence on the spectrin cytoskeleton. Mol. Biol.Cell 14:194aGoogle Scholar
  13. Das, A., Base, C., Dhulipala, S., Dubreuil, R.R. 2006. Spectrin functions upstream of ankyrin in a spectrin cytoskeleton assembly pathway. J. Cell Biol., in pressGoogle Scholar
  14. Davis J., V. Bennett. 1984. Brain ankyrin. J. Biol. Chem. 259:13550–13559PubMedGoogle Scholar
  15. Davis J.Q., T. McLaughlin, V. Bennett. 1993. Ankyrin-binding proteins related to nervous system cell adhesion molecules: Candidates to provide transmembrane and intercellular connections in adult brain. J. Cell Biol. 121:121–133PubMedCrossRefGoogle Scholar
  16. Devarajan P., D.A. Scaramuzzino, J.S. Morrow. 1994. Ankyrin binds to two distinct cytoplasmic domains of Na,K-ATPase α subunit. Proc. Natl. Acad. Sci. USA. 91:2965–2969PubMedCrossRefGoogle Scholar
  17. Drenckhahn D., Schluter K., Allen D.P., V. Bennett. 1985. Colocalization of band 3 with ankyrin and spectrin at the basal membrane of intercalated cells in the rat kidney. Science. 230:1287–1289PubMedCrossRefGoogle Scholar
  18. Drubin D.G., W.J. Nelson. 1996. Origins of Cell Polarity. Cell. 84:335–344PubMedCrossRefGoogle Scholar
  19. Dubreuil R.R., Byers T.J., Stewart C.T., D.P. Kiehart. 1990. A β spectrin isoform from DrosophilaH) is similar in size to vertebrate dystrophin. J. Cell Biol. 111:1849–1858PubMedCrossRefGoogle Scholar
  20. Dubreuil R.R., G.R. MacVicar, S. Dissanayake, C. Liu, D. Homer, M. Hortsch. 1996. Neuroglian-mediated adhesion induces assembly of the membrane skeleton at cell contact sites. J. Cell Biol. 133:647–655PubMedCrossRefGoogle Scholar
  21. Dubreuil R.R., P. Wang, S.C. Dahl, J.K. Lee, L.S.B. Goldstein. 2000. Drosophila βspectrin functions independently of α spectrin to polarize the Na,K ATPase in epithelial cells. J. Cell Biol. 149:647–656PubMedCrossRefGoogle Scholar
  22. Dubreuil R.R., J. Yu. 1994. Ankyrin and β spectrin accumulate independently of α spectrin in Drosophila. Proc. Natl. Acad. Sci. USA. 91:10285–10289PubMedCrossRefGoogle Scholar
  23. Fowler V., D. Branton. 1977. Lateral mobility of human erythrocyte integral membrane proteins. Nature 268: 23–26PubMedCrossRefGoogle Scholar
  24. Funke L., S. Dakoji, D.S. Bredt. 2005. Membrane-associated guanylate kinases regulate adhesion and plasticity at cell junctions. Ann. Rev. Biochem. 74:219–245PubMedCrossRefGoogle Scholar
  25. Garrido J.J., P. Giraud, E. Carlier, F. Fernandes, A. Moussif, M.-P. Fache, D. Debanne, B. Dargent. 2003. A targeting motif involved in sodium channel clustering at the axonal initial segment. Science. 300:2091–2094PubMedCrossRefGoogle Scholar
  26. Garver T.D., Q. Ren, S. Tuvia, V. Bennett. 1997. Tyrosine phosphorylation at a site highly conserved in the L1 family of cell adhesion molecules abolishes ankyrin binding and increases lateral mobility of neurofascin. J. Cell Biol. 137:703–714PubMedCrossRefGoogle Scholar
  27. Glenney J.R., Glenney P., Osborn M., K. Weber. 1982. An F-actin and calmodulin-binding protein from isolated intestinal brush borders has a morphology related to spectrin. Cell. 28:843–854PubMedCrossRefGoogle Scholar
  28. Golan D. E., W. Veatch. 1980. Lateral mobility of band 3 in the human erythrocyte membrane studied by fluorescence photobleaching recovery: Evidence for control by cytoskeletal interactions. Proc. Natl Acad. Sci. USA 77: 2537–2541PubMedCrossRefGoogle Scholar
  29. Hanwell D., T. Ishikawa, R. Saleki, D. Rotin. 2002. Trafficking and cell surface stability of the epithelial Na+ channel expressed in epithelial madin-Darby canine kidney cells. J. Biol. Chem. 277:9772–9779PubMedCrossRefGoogle Scholar
  30. Harper S.L., G.E. Begg, D.W. Speicher. 2001. Role of terminal nonhomologous domains in initiation of human red cell spectrin dimerization. Biochemistry 40:9935–9943PubMedCrossRefGoogle Scholar
  31. Hortsch M., K.S. O’Shea, G. Zhao, F. Kim, Y. Vallejo, R.R. Dubreuil. 1998. A conserved role for L1 as a transmembrane link between neuronal adhesion and membrane cytoskleton assembly. Cell Adhesion & Communication. 5:61–73CrossRefGoogle Scholar
  32. Ikeda Y., K.A. Dick, M.R. Westherspoon, D. Gincel, et al. 2006. Spectrin mutations cause spinocerebellar ataxia type 5. Nat. Genetics. 38:184–190CrossRefGoogle Scholar
  33. Jackson M., W. Song, M.-Y. Liu, L. Jin, M. Dykes-Hoberg, C.-L.G. Lin, W.J. Bowers, H.J. Federoff, P.C. Sternweis, J.D. Rothstein. 2001. Modulation of the neuronal glutamate transporter EAAT4 by two interacting proteins. Nature. 410:89–93PubMedCrossRefGoogle Scholar
  34. Kalomiris E.L., L.Y.W. Bourguignon. 1988. Mouse T lymphoma cells contain a transmembrane glycoprotein (gp85) that binds ankyrin. J. Cell Biol. 106:319–327PubMedCrossRefGoogle Scholar
  35. Kennedy S.P., S.L. Warren, B.G. Forget, J.S. Morrow. 1991. Ankyrin binds to the 15th repetitive unit of erythroid and nonerythroid β spectrin. J. Cell Biol. 114:267–277CrossRefGoogle Scholar
  36. Kizhatil K., V. Bennett. 2004. Lateral membrane biogenesis in human bronchial epithelial cells requires 190-kDa ankyrin-G. J. Biol. Chem. 279:16706–16714PubMedCrossRefGoogle Scholar
  37. Komada M., P. Soriano. 2002. ΒIV-spectrin regulates sodium channel clustering through ankyrin-G at axon initial segments and nodes of Ranvier. J. Cell Biol. 156:337–348PubMedCrossRefGoogle Scholar
  38. Kordeli E., S. Lambert, V. Bennett. 1995. Ankyrin-G. J. Biol. Chem. 270:2352–2359PubMedCrossRefGoogle Scholar
  39. Lacas-Gervais S., J. Guo, N. Strenzke, E. Scarfone, M. Kolpe, M. Jahkel, P. DeCamilli, T. Moser, M.N. Rasband, M. Solimena. 2004. BIVE1 spectrin stabilizes the nodes of Ranvier and axon initial segments. J. Cell Biol. 166:983–990PubMedCrossRefGoogle Scholar
  40. Lazarides E., W.J. Nelson. 1983. Erythrocyte and brain forms of spectrin in cerebellum: Distinct membrane-cytoskeleton domains in neurons. Science 220:1295–1297PubMedCrossRefGoogle Scholar
  41. Lebovitz R.M., Takeyasu, K., D.M. Fambrough. 1989. Molecular characterization and expression of the (Na+ + K+)-ATPase α-subunit in Drosophila melanogaster. EMBO J. 8:193–202PubMedGoogle Scholar
  42. Lee J., R. Coyne, R.R. Dubreuil, L.S.B. Goldstein, D. Branton. 1993. Cell shape and interaction defects in α-spectrin mutants of Drosophila melanogaster. J. Cell Biol. 123:1797–1809PubMedCrossRefGoogle Scholar
  43. Lemaillet G., B. Walker, S. Lambert. 2003. Identification of a conserved ankyrin-binding motif in the family of sodium channel α subunits. J. Biol. Chem. 278:27333–27339PubMedCrossRefGoogle Scholar
  44. Levine J., M. Willard. 1981. Fodrin: Axonally transported polypeptides associated with the internal periphery of many cells. J. Cell Biol. 90:631–643PubMedCrossRefGoogle Scholar
  45. Li Z., E.P. Burke, J.S. Frank, V. Bennett, K.D. Phillipson. 1993. The cardiac Na+-Ca+ exchanger binds to the cytoskeletal protein ankyrin. J. Biol. Chem. 268:11489–11491PubMedGoogle Scholar
  46. Lopez C., S. Metral, D. Eladari, S. Drevensek, P. Gane, R. Chambrey, V. Bennett, J.-P. Cartron, C. LeVanKim, Y. Colin. 2005. The ammonium transporter RhBG. J. Biol. Chem. 280:8221–8228PubMedCrossRefGoogle Scholar
  47. Lux, S.E., J. Palek, 1995. Disorders of the Red Cell Membrane. In: Blood: Principles and practice of hematology. R.I. Handin, S.E. Lux, T.P. Stossel editors. J.B. Lippincott Co., Philadelphia. 1701–1818Google Scholar
  48. Matteis M.A.D., J.S. Morrow. 2000. Spectrin tethers and mesh in the biosynthetic pathway. J. Cell Sci. 113:2331–2343PubMedGoogle Scholar
  49. McKeown C., V. Praitis, J. Austin. 1998. sma-1 encodes a βH-spectrin homolog required for Caenorhabditis elegans morphogenesis. Development 125:2087–2098PubMedGoogle Scholar
  50. McNeill H., Ozawa M., Kemler R., W.J. Nelson. 1990. Novel function of the cell adhesion molecule uvomorulin as an inducer of cell surface polarity. Cell 62:309–316PubMedCrossRefGoogle Scholar
  51. Mercier F., Teggio H., Deviliers G., Bataille D., P. Mangeat. 1989. Membrane-cytoskeleton dynamics in rat parietal cells: Mobilization of actin and spectrin upon stimulation of gastric acid secretion. J. Cell Biol. 108:441–453PubMedCrossRefGoogle Scholar
  52. Mohler P.J., V. Bennett. 2005. Ankyrin-based cardiac arrhythmias: A new class of channelopathies due to loss of cellular targeting. Curr. Op. Cardiol. 20:189–193CrossRefGoogle Scholar
  53. Mohler P. J., J. Q. Davis, V. Bennett. 2005. Ankyrin-B coordinates the Na/K ATPase, Na/Ca exchanger, and InsP3 receptor in a cardiac T-tubule/SR microdomain. PloS Biology 3: e423PubMedCrossRefGoogle Scholar
  54. Mohler P.J., I. Rivolta, C. Napolitano, G. LeMaillet, S. Lambert, S.G. Priori, V. Bennett. 2004a. Nav1.5 E1053K mutation causing Brugada syndrome blocks binding to ankyrin-G and expression of nav1.5 on the surface of cardiomyocytes. Proc. Natl. Acad. Sci. USA 101:17533–17538CrossRefGoogle Scholar
  55. Mohler P.J., J.-J. Schott, A.O. Gramolini, K.W. Dilly, S. Guatimoisim, W.H. duBell, L.-S. Song, K. Haurogne, F. Kyndt, M.E. Ali, T.B. Rogers, W.J. Lederer, D. Escande, H.L. Marec, V. Bennett. 2003. Ankyrin-B mutations causes type 4 long-QT cardiac arrhythmia and sudden cardiac death. Nature 634–639Google Scholar
  56. Mohler P.J., W. Yoon, V. Bennett. 2004b. Ankyrin-B targets B2-spectrin to an intracellular compartment in neonatal cardiomyocytes. J. Biol. Chem. 279:40185–40193CrossRefGoogle Scholar
  57. Molday L.L., Cook M.J., Kaupp U.B., R.S. Molday. 1990. The cGMP-gated cation-channel of bovine rod photoreceptor cells is associated with a 240 kDa protein exhibiting immunochemical cross-reactivity with spectrin. J. Biol. Chem. 265:18690–18695PubMedGoogle Scholar
  58. Nelson W.J., R.W. Hammerton. 1989. A membrane-cytoskeletal complex containing Na+, K+-ATPase, ankyrin, and fodrin in Madin-Darby canine kidney (MDCK) cells: Implications for the biogenesis of epithelial cell polarity. J. Cell Biol. 108:893–902PubMedCrossRefGoogle Scholar
  59. Nelson W.J., P.J. Veshnock. 1986. Dynamics of membrane skeleton (fodrin) organization during development of polarity in Madin-Darby Canine Kidney epithelial cells. J. Cell Biol. 103:1751–1765PubMedCrossRefGoogle Scholar
  60. Nelson W.J., P.J. Veshnock. 1987a. Modulation of fodrin (membrane skeleton) stability by cell-cell contact in Madin-Darby Canine Kidney epithelial cells. J. Cell Biol. 104:1527–1537CrossRefGoogle Scholar
  61. Nelson W.J., P.J. Veshnock. 1987b. Ankyrin binding to (Na+ & K+) ATPase and implications for the organization of membrane domains in polarized cells. Nature. 328:533–536CrossRefGoogle Scholar
  62. Nicolas V., C.L.V. Kim, P. Gane, C. Birkenmeier, J.-P. Cartron, Y. Colin, I. Mouro-Chanteloup. 2003. Rh-RhAG/Ankyrin-R, a new interaction site between the membrane bilayer and the red cell skeleton, is impaired by Rhnull-associated mutation. J. Biol. Chem. 278:25526–25533PubMedCrossRefGoogle Scholar
  63. Nigg E. A., R. J. Cherry. 1980. Anchorage of a band 3 population at the erythrocyte cytoplasmic membrane surface: Protein rotational diffusion measurements. Proc. Natl Acad. Sci. USA 77: 4702–4706PubMedCrossRefGoogle Scholar
  64. Pan Z., T. Kao, Z. Horvath, J. Lemos, J.-Y. Sul, S.D. Cranstoun, V. Bennett, S.S. Scherer, E.C. Cooper. 2006. A common ankyrin-G-based mechanism retains KCNQ and Nav channels at electrically active domains of the axon. J. Neurosci. 26: 2599–2613PubMedCrossRefGoogle Scholar
  65. Parkinson N.J., C.L. Olsson, J.L. Hallows, J. McKee-Johnson, B.P. Keogh, K. Noben-Trauth, S.G. Kujawa, B.L. Tempel. 2001. Mutant β-spectrin 4 causes auditory and motor neuropathies in quivering mice. Nature Gen. 29:61–65CrossRefGoogle Scholar
  66. Peters L.L., C.S. Birkenmeier, R.T. Bronson, R.A. White, S.E. Lux, E. Otto V. Bennett, A. Higgins, J.E. Barker. 1991. Purkinje cell degeneration associated with erythroid ankyrin deficiency in nb/nb mice. J. Cell Biol. 114:1233–1241PubMedCrossRefGoogle Scholar
  67. Peters L.L., K.M. John, F.M. Lu, E.M. Eicher, A. Higgins, M. Yialamas, L.C. Turtzo, A.J. Otsuka, S.E. Lux. 1995. Ank3 (epithelial ankyrin), a widely distributed new member of the ankyrin gene family and the major ankyrin in kidney, is expressed in alternatively spliced forms, including forms that lack the repeat domain. J. Cell Biol. 130:313–330PubMedCrossRefGoogle Scholar
  68. Phillips M.D., G.H. Thomas. 2006. Brush border spectrin is required for early endosome recycling in Drosophila. J. Cell Sci. 119:1361–1370PubMedCrossRefGoogle Scholar
  69. Pradhan D., J.S. Morrow. 2002. The spectrin-ankyrin skeleton controls CD45 surface display and interleukin-2 production. Immunity 17:303–315PubMedCrossRefGoogle Scholar
  70. Pradhan D., K. Tseng, C.D. Cianci, J.S. Morrow. 2004. Antibodies to β a I E2 spectrin identify in-homogeneities in the erythrocyte membrane skeleton. Blood Cells, Molecules, & Diseases 32:408–410CrossRefGoogle Scholar
  71. Rotin D., D. Bar-Sagi, H. O’Brodovich, J. Merilainen, V.P. Lehto, C.M. Canessa, B.C. Rossier, G.P. Downey. 1994. An SH3 binding region in the epithelial Na+ channel (alpharENaC) mediates its localization at the apical membrane. EMBO J. 13:4440–4450PubMedGoogle Scholar
  72. Salomao M., X. An, X. Guo, W.B. Gratzer, N. Mohandas, A.J. Baines. 2006. Mammalian αI spectrin is a neofunctionalized polypeptide adapted to small highly deformable erythrocytes. Proc. Natl Acad. Sci. USA 103:643–648PubMedCrossRefGoogle Scholar
  73. Scotland P., D. Zhou, H. Benveniste, V. Bennett. 1998. Nervous system defects of ankyrin B (-/-) mice suggest functional overlap between the cell adhesion molecule L1 and 440 kD ankyrin B in premyelinated axons. J. Cell Biol. 143:1305–1315PubMedCrossRefGoogle Scholar
  74. Siddhanta A., A. Radulescu, M.C. Stankewich, J.S. Morrow, D. Shields. 2003. Fragmentation of the Golgi apparatus. J. Biol. Chem. 278:1957–1965PubMedCrossRefGoogle Scholar
  75. Speicher D.W., V.T. Marchesi. 1984. Erythrocyte spectrin is comprised of many homologous triple helical segments. Nature 311:177–180PubMedCrossRefGoogle Scholar
  76. Srinivasan Y., Elmer L., Davis J., Bennett V., K. Angelides. 1988. Ankyrin and spectrin associate with voltage-dependent sodium channels in brain. Nature 333:177–180PubMedCrossRefGoogle Scholar
  77. Stabach P.R., J.S. Morrow. 2000. Identification and characterization of βV spectrin, a mammalian ortholog of Drosophila βH spectrin. J. Biol. Chem. 275:21385–21395PubMedCrossRefGoogle Scholar
  78. Stankewich M.C., W.T. Tse, L.L. Peters, Y. Ch’ng, K.M. John, P.R. Stabach, P. Devarajan, J.S. Morrow, S.E. Lux. 1998. A widely expressed βIII spectrin associated with Golgi and cytoplasmic vesicles. Proc. Natl. Acad. Sci. USA 95:14158–14163PubMedCrossRefGoogle Scholar
  79. Tse W.T., Lecomte M.C., Costa F.F., Garbarz M., Feo C., Boivin P., Dhermy D., B.G. Forget. 1990. A point mutation in the β-spectrin gene associated with α-I/74 hereditary elliptocytosis - implications for the mechanism of spectrin dimer self association. J. Clin. Invest. 86:909–916PubMedCrossRefGoogle Scholar
  80. Tse W.T., S.E. Lux. 1999. Red Blood cell membrane disorders. Br. J. Hematol. 104:2–13CrossRefGoogle Scholar
  81. Tse W.T., J. Tang, O. Jin, C. Korsgren, K.M. John, A.L. Kung, B. Gwynn, L.L. Peters, S.E. Lux. 2001. A new spectrin β4, has a major truncated isoform that associates with promyelocytic leukemia protein nuclear bodies and the nuclear matrix. J. Biol. Chem. 276:23974–23985PubMedCrossRefGoogle Scholar
  82. Tuvia S., M. Buhusi, L. Davis, M. Reedy, V. Bennett. 1999. Ankyrin-B is required for intracellular sorting of structurally diverse Ca2+-homeostasis proteins. J. Cell Biol. 147:995–1007PubMedCrossRefGoogle Scholar
  83. Wasenius V.-M., Saraste M., Salven P., Eramaa M., Holm L., V.-P. Lehto. 1989. Primary structure of the brain -spectrin. J. Cell Biol. 108:79–93PubMedCrossRefGoogle Scholar
  84. Wechsler A., V.I. Teichberg. 1998. Brain spectrin binding to the NMDA receptor is regulated by phosphorylation, calcium and calmodulin. EMBO J. 17:3931–3939PubMedCrossRefGoogle Scholar
  85. Yan Y., E. Winograd, A. Viel, T. Cronin, S.C. Harrison, D. Branton. 1993. Crystal structure of the repetitive segments of spectrin. Science 262:2027–2030PubMedCrossRefGoogle Scholar
  86. Yang Y., S. Lacas-Gervais, D.K. Morest, M. Solimena, M.N. Rasband. 2004. ΒIV spectrins are essential for membrane stability and the molecular organization of nodes of Ranvier. J. Neurosci. 24:7230–7240PubMedCrossRefGoogle Scholar
  87. Zhang Z., P. Devarajan, A.L. Dorfman, J.S. Morrow. 1998. Structure of the ankyrin-binding domain of -Na,K-ATPase. J. Biol. Chem. 273:18681–18684PubMedCrossRefGoogle Scholar
  88. Zhou D., S. Lambert, P.L. Malen, S. Carpenter, L.M. Boland, V. Bennett. 1998. Ankyrin G is required for clustering of voltage-gated Na channels at axon initial segments and for normal action potential firing. J. Cell Biol. 143:1295–1304PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  1. 1.Dept. of Biological SciencesUniversity of Illinois at ChicagoChicagoUSA

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