Distribution and lateral mobility of voltage-dependent sodium channels in neurons [published erratum appears in J Cell Biol 1989 May;108(5):preceding 2001]

Voltage-dependent sodium channels are distributed nonuniformly over the surface of nerve cells and are localized to morphologically distinct regions. Fluorescent neurotoxin probes specific for the voltage- dependent sodium channel stain the axon hillock 5-10 times more intensely than the cell body and show punctate fluorescence confined to the axon hillock which can be compared with the more diffuse and uniform labeling in the cell body. Using fluorescence photobleaching recovery (FPR) we measured the lateral mobility of voltage-dependent sodium channels over specific regions of the neuron. Nearly all sodium channels labeled with specific neurotoxins are free to diffuse within the cell body with lateral diffusion coefficients on the order of 10(- 9) cm2/s. In contrast, lateral diffusion of sodium channels in the axon hillock is restricted, apparently in two different ways. Not only do sodium channels in these regions diffuse more slowly (10(-10)-10(-11) cm2/s), but also they are prevented from diffusing between axon hillock and cell body. No regionalization or differential mobilities were observed, however, for either tetramethylrhodamine- phosphatidylethanolamine, a probe of lipid diffusion, or FITC-succinyl concanavalin A, a probe for glycoproteins. During the maturation of the neuron, the plasma membrane differentiates and segregates voltage- dependent sodium channels into local compartments and maintains this localization perhaps either by direct cytoskeletal attachments or by a selective barrier to channel diffusion.

[1]  A. Lander,et al.  Laminin is associated with the "neurite outgrowth-promoting factors" found in conditioned media. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[2]  W. Catterall,et al.  The sodium channel from rat brain. Purification and subunit composition. , 1984, The Journal of biological chemistry.

[3]  K. Angelides,et al.  Mapping the molecular structure of the voltage-dependent sodium channel. Distances between the tetrodotoxin and Leiurus quinquestriatus quinquestriatus scorpion toxin receptors. , 1983, Journal of Biological Chemistry.

[4]  R. Small,et al.  Components of the plasma membrane of growing axons. I. Size and distribution of intramembrane particles , 1984, The Journal of cell biology.

[5]  R. Cherry,et al.  Rotational and lateral diffusion of membrane proteins. , 1979, Biochimica et biophysica acta.

[6]  K. Angelides,et al.  A comparative analysis of glial and neuronal markers in the retina of fish: Variable character of horizontal cells , 1985, The Journal of comparative neurology.

[7]  K. Angelides,et al.  Fluorescence resonance energy transfer on the voltage-dependent sodium channel. Spatial relationship and site coupling between the batrachotoxin and Leiurus quinquestriatus quinquestriatus alpha-scorpion toxin receptors. , 1984, Journal of Biological Chemistry.

[8]  E. Nigg,et al.  Anchorage of a band 3 population at the erythrocyte cytoplasmic membrane surface: protein rotational diffusion measurements. , 1980, Proceedings of the National Academy of Sciences of the United States of America.

[9]  M H Ellisman,et al.  Immunocytochemical localization of sodium channel distributions in the excitable membranes of Electrophorus electricus. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[10]  P G Nelson,et al.  Mouse spinal cord in cell culture. I. Morphology and intrinsic neuronal electrophysiologic properties. , 1977, Journal of neurophysiology.

[11]  M. Sheetz,et al.  Matrix control of protein diffusion in biological membranes. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[12]  T. Kasamatsu,et al.  Segregation of two spectrin forms in the chicken optic system: A mechanism for establishing restricted membrane-cytoskeletal domains in neurons , 1984, Cell.

[13]  M. Edidin,et al.  Lateral diffusion of wild-type and mutant Ld antigens in L cells , 1984, The Journal of cell biology.

[14]  T. Jovin,et al.  Distribution and mobility of murine histocompatibility H-2Kk antigen in the cytoplasmic membrane. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[15]  Mu-ming Poo,et al.  Lateral diffusion of rhodopsin in the photoreceptor membrane , 1974, Nature.

[16]  J. Miller,et al.  Principal glycopeptide of the tetrodotoxin/saxitoxin binding protein from Electrophorus electricus: isolation and partial chemical and physical characterization. , 1983, Biochemistry.

[17]  R. Klausner,et al.  Lipid domains in membranes. Evidence derived from structural perturbations induced by free fatty acids and lifetime heterogeneity analysis. , 1980, The Journal of biological chemistry.

[18]  K. Angelides,et al.  Characterization of mammalian neurofilament triplet proteins. Subunit stoichiometry and morphology of native and reconstituted filaments. , 1985, The Journal of biological chemistry.

[19]  K. Angelides,et al.  Preparation and characterization of fluorescent scorpion toxins from Leiurus quinquestriatus quinquestriatus as probes of the sodium channel of excitable cells. , 1983, The Journal of biological chemistry.

[20]  D W Tank,et al.  Enhanced molecular diffusibility in muscle membrane blebs: release of lateral constraints , 1982, The Journal of cell biology.

[21]  K. Akert,et al.  Intramembranous particles at the nodes of Ranvier of the cat spinal cord: A morphometric study , 1978, Brain Research.

[22]  E. Elson,et al.  Inhibition of the mobility of mouse lymphocyte surface immunoglobulins by locally bound concanavalin A. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[23]  M H Ellisman,et al.  Rows of dimeric-particles within the axolemma and juxtaposed particles within glia, incorporated into a new model for the paranodal glial- axonal junction at the node of Ranvier , 1980, The Journal of cell biology.

[24]  J. Eccles,et al.  The electrical properties of the motoneurone membrane , 1955, The Journal of physiology.

[25]  G. Strichartz,et al.  Components of the plasma membrane of growing axons. III. Saxitoxin binding to sodium channels , 1984, The Journal of cell biology.

[26]  M. Edidin,et al.  Effects of cell density and extracellular matrix on the lateral diffusion of major histocompatibility antigens in cultured fibroblasts , 1986, The Journal of cell biology.

[27]  R. Ghez,et al.  Components of the plasma membrane of growing axons. II. Diffusion of membrane protein complexes , 1984, The Journal of cell biology.

[28]  G. Shaw,et al.  The distribution of the neurofilament triplet proteins within individual neurones. , 1981, Experimental cell research.

[29]  J. M. Ritchie,et al.  Density of sodium channels in mammalian myelinated nerve fibers and nature of the axonal membrane under the myelin sheath. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[30]  K. Angelides,et al.  Physicochemical characterization of the alpha-peptide of the sodium channel from rat brain. , 1985, Biochemistry.

[31]  D. DeRosier,et al.  The Cytoskeleton , 1984, Springer US.

[32]  W. Catterall,et al.  Glycosylation is required for maintenance of functional sodium channels in neuroblastoma cells. , 1983, The Journal of biological chemistry.

[33]  E. Elson,et al.  Analysis of cell surface interactions by measurements of lateral mobility. , 1979, Journal of supramolecular structure.

[34]  D. Koppel,et al.  A localized surface protein of guinea pig sperm exhibits free diffusion in its domain , 1984, The Journal of cell biology.

[35]  S. Waxman.  Cytochemical heterogeneity of the axon membrane , 1981, Trends in Neurosciences.

[36]  M H Ellisman,et al.  Microtrabecular structure of the axoplasmic matrix: visualization of cross-linking structures and their distribution , 1980, The Journal of cell biology.

[37]  K. Angelides,et al.  Molecular and cellular mapping of the voltage-dependent na channel. , 1984, Biophysical journal.

[38]  R. Barchi.  Protein Components of the Purified Sodium Channel from Rat Skeletal Muscle Sarcolemma , 1983, Journal of neurochemistry.

[39]  M H Ellisman,et al.  Molecular specializations of the axon membrane at nodes of Ranvier are not dependent upon myelination , 1979, Journal of neurocytology.

[40]  M. Poo.  Rapid lateral diffusion of functional ACh receptors in embryonic muscle cell membrane , 1982, Nature.

[41]  J. Levine,et al.  Fodrin: axonally transported polypeptides associated with the internal periphery of many cells , 1981, The Journal of cell biology.

[42]  M. Poo,et al.  Redistribution of cell surface receptors induced by cell-cell contact , 1982, The Journal of cell biology.

[43]  J. Caldwell,et al.  Na channels in skeletal muscle concentrated near the neuromuscular junction , 1985, Nature.

[44]  H. Lecar,et al.  Electrical development in spinal cord cell culture , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[45]  K. Angelides.  Fluorescently labelled Na+ channels are localized and immobilized to synapses of innervated muscle fibres , 1986, Nature.

[46]  W. Webb,et al.  Diffusion, patching, and capping of stearoylated dextrans on 3T3 cell plasma membranes. , 1980, Biochemistry.

[47]  P. Saffman,et al.  Brownian motion in biological membranes. , 1975, Proceedings of the National Academy of Sciences of the United States of America.

[48]  P. Wood,et al.  Neuron-Schwann cell interaction in basal lamina formation. , 1982, Developmental biology.

[49]  E. Elson,et al.  5. Fluorescence Methods for Studying Membrane Dynamics , 1982 .

[50]  K. Angelides.  Fluorescent and photoactivatable fluorescent derivatives of tetrodotoxin to probe the sodium channel of excitable membranes. , 1981, Biochemistry.

[51]  K. Angelides,et al.  Structural mapping of the voltage-dependent sodium channel. Distance between the tetrodotoxin and Centruroides suffusus suffusus II beta-scorpion toxin receptors. , 1984, The Journal of biological chemistry.

[52]  M H Ellisman,et al.  Development of axonal membrane specializations defines nodes of Ranvier and precedes Schwann cell myelin elaboration. , 1980, Developmental biology.

[53]  J. Rosenbluth,et al.  Intramembranous particle distribution at the node of Ranvier and adjacent axolemma in myelinated axons of the frog brain , 1976, Journal of neurocytology.

[54]  W. Almers,et al.  Photobleaching through glass micropipettes: sodium channels without lateral mobility in the sarcolemma of frog skeletal muscle. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[55]  W. Webb,et al.  Mobility measurement by analysis of fluorescence photobleaching recovery kinetics. , 1976, Biophysical journal.