Role of nav1.9 in activity-dependent axon growth in motoneurons

Human Molecular Genetics

Volumn 21, Issue 16, 2012, Pages 3655-3667

  Subramanian, Narayan ^a,c   Wetzel, Andrea ^a   Dombert, Benjamin ^a   Yadav, Preeti ^a   Havlicek, Steven ^a,d   Jablonka, Sibylle ^a   Nassar, Mohammed A ^b,e   Blum, Robert ^a   Sendtner, Michael ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^d UNIVERSITY HOSPITAL ERLANGEN   (Germany)

^e UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

SAXITOXIN; SODIUM CHANNEL NAV1.9; TETRODOTOXIN; VOLTAGE GATED CALCIUM CHANNEL;

ANIMAL CELL; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; EMBRYO; MOTONEURON; MOUSE; NERVE CELL CULTURE; NERVE ENDING; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SPINAL CORD;

ANIMALS; AXONS; CALCIUM; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; GROWTH CONES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOTOR NEURONS; MUSCULAR ATROPHY, SPINAL; NAV1.9 VOLTAGE-GATED SODIUM CHANNEL; RABBITS; SAXITOXIN; SODIUM CHANNEL BLOCKERS; SPINAL CORD; TETRODOTOXIN; VOLTAGE-GATED SODIUM CHANNELS;

EID: 84865092307     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/dds195     Document Type: Article

References (66)

1. Sanes, J.R. and Lichtman, J.W. (1999) Development of the vertebrate neuromuscular junction. Annu. Rev. Neurosci., 22, 389-442.
2. Hamburger, V. (1934) The effects of wing bud extirpation on the development of the central nervous system in chick embryos. J. Exp. Zool., 68, 449-494.
3. Hamburger, V. (1975) Cell death in the development of the lateral motor column of the chick embryo. J. Comp. Neurol., 160, 535-546.
4. Thoenen, H., Hughes, R.A. and Sendtner, M. (1993) Trophic support of motoneurons: physiological, pathophysiological, and therapeutic implications. Exp. Neurol., 124, 47-55.
5. Arakawa, Y., Sendtner, M. and Thoenen, H. (1990) Survival effect of ciliary neurotrophic factor (CNTF) on chick embryonic motoneurons in culture: comparison with other neurotrophic factors and cytokines. J. Neurosci., 10, 3507-3515.
6. Calof, A.L. and Reichardt, L.F. (1984) Motoneurons purified by cell sorting respond to two distinct activities in myotube-conditioned medium. Dev. Biol., 106, 194-210.
7. Sendtner, M., Pei, G., Beck, M., Schweizer, U. and Wiese, S. (2000) Developmental motoneuron cell death and neurotrophic factors. Cell Tissue Res., 301, 71-84.
8. Hanson, M.G. and Landmesser, L.T. (2003) Characterization of the circuits that generate spontaneous episodes of activity in the early embryonic mouse spinal cord. J. Neurosci., 23, 587-600.
9. Nishimaru, H., Iizuka, M., Ozaki, S. and Kudo, N. (1996) Spontaneous motoneuronal activity mediated by glycine and GABA in the spinal cord of rat fetuses in vitro. J. Physiol., 497(Pt 1), 131-143.
10. O'Donovan, M.J. and Landmesser, L. (1987) The development of hindlimb motor activity studied in the isolated spinal cord of the chick embryo. J. Neurosci., 7, 3256-3264.
11. Spitzer, N.C. (2006) Electrical activity in early neuronal development. Nature, 444, 707-712.
12. Ciccolini, F., Collins, T.J., Sudhoelter, J., Lipp, P., Berridge, M.J. and Bootman, M.D. (2003) Local and global spontaneous calcium events regulate neurite outgrowth and onset of GABAergic phenotype during neural precursor differentiation. J. Neurosci., 23, 103-111.
13. Wang, S., Polo-Parada, L. and Landmesser, L.T. (2009) Characterization of rhythmic Ca2+ transients in early embryonic chick motoneurons: Ca2+ sources and effects of altered activation of transmitter receptors. J. Neurosci., 29, 15232-15244.
14. Spitzer, N.C., Lautermilch, N.J., Smith, R.D. and Gomez, T.M. (2000) Coding of neuronal differentiation by calcium transients. Bioessays, 22, 811-817.
15. Gu, X. and Spitzer, N.C. (1995) Distinct aspects of neuronal differentiation encoded by frequency of spontaneous Ca2+ transients. Nature, 375, 784-787.
16. Hanson, M.G. and Landmesser, L.T. (2004) Normal patterns of spontaneous activity are required for correct motor axon guidance and the expression of specific guidance molecules. Neuron, 43, 687-701.
17. Jablonka, S., Beck, M., Lechner, B.D., Mayer, C. and Sendtner, M. (2007) Defective Ca2+ channel clustering in axon terminals disturbs excitability in motoneurons in spinal muscular atrophy. J. Cell Biol., 179, 139-149.
18. Chan, Y.B., Miguel-Aliaga, I., Franks, C., Thomas, N., Trulzsch, B., Sattelle, D.B., Davies, K.E. and van den Heuvel, M. (2003) Neuromuscular defects in a Drosophila survival motor neuron gene mutant. Hum. Mol. Genet., 12, 1367-1376.
19. Kong, L., Wang, X., Choe, D.W., Polley, M., Burnett, B.G., Bosch-Marce, M., Griffin, J.W., Rich, M.M. and Sumner, C.J. (2009) Impaired synaptic vesicle release and immaturity of neuromuscular junctions in spinal muscular atrophy mice. J. Neurosci., 29, 842-851.
20. Ruiz, R., Casanas, J.J., Torres-Benito, L., Cano, R. and Tabares, L. (2010) Altered intracellular Ca2+ homeostasis in nerve terminals of severe spinal muscular atrophy mice. J Neurosci, 30, 849-857.
21. Porter, B.E., Weis, J. and Sanes, J.R. (1995) A motoneuron-selective stop signal in the synaptic protein S-laminin. Neuron, 14, 549-559.
22. Nishimune, H., Sanes, J.R. and Carlson, S.S. (2004) A synaptic laminin-calcium channel interaction organizes active zones in motor nerve terminals. Nature, 432, 580-587.
23. Catterall, W.A. (2000) From ionic currents to molecular mechanisms: the structure and function of voltage-gated sodium channels. Neuron, 26, 13-25.
24. Catterall, W.A., Goldin, A.L. and Waxman, S.G. (2005) International Union of Pharmacology. XLVII. Nomenclature and structure-function relationships of voltage-gated sodium channels. Pharmacol. Rev., 57, 397-409.
25. Penzotti, J.L., Fozzard, H.A., Lipkind, G.M. and Dudley Jr S.C. (1998) Differences in saxitoxin and tetrodotoxin binding revealed by mutagenesis of the Na+ channel outer vestibule. Biophys. J., 75, 2647-2657.
26. Wiese, S., Herrmann, T., Drepper, C., Jablonka, S., Funk, N., Klausmeyer, A., Rogers, M.L., Rush, R. and Sendtner, M. (2010) Isolation and enrichment of embryonic mouse motoneurons from the lumbar spinal cord of individual mouse embryos. Nat. Protoc., 5, 31-38.
27. Gu, X., Olson, E.C. and Spitzer, N.C. (1994) Spontaneous neuronal calcium spikes and waves during early differentiation. J. Neurosci., 14, 6325-6335.
28. Feng, Z.P., Doering, C.J., Winkfein, R.J., Beedle, A.M., Spafford, J.D. and Zamponi, G.W. (2003) Determinants of inhibition of transiently expressed voltage-gated calcium channels by omega-conotoxins GVIA and MVIIA. J. Biol. Chem., 278, 20171-20178.
29. Cummins, T.R., Dib-Hajj, S.D., Black, J.A., Akopian, A.N., Wood, J.N. and Waxman, S.G. (1999) A novel persistent tetrodotoxin-resistant sodium current in SNS-null and wild-type small primary sensory neurons. J. Neurosci., 19, RC43.
30. Herzog, R.I., Cummins, T.R. and Waxman, S.G. (2001) Persistent TTX-resistant Na(+) current affects resting potential and response to depolarization in simulated spinal sensory neurons. J. Neurophysiol., 86, 1351-1364.
31. Östman, J.A., Nassar, M.A., Wood, J.N. and Baker, M.D. (2008) GTP up-regulated persistent Na + current and enhanced nociceptor excitability require NaV1.9. J. Physiol., 586, 1077-1087.
32. Rugiero, F., Mistry, M., Sage, D., Black, J.A., Waxman, S.G., Crest, M., Clerc, N., Delmas, P. and Gola, M. (2003) Selective expression of a persistent tetrodotoxin-resistant Na+ current and NaV1.9 subunit in myenteric sensory neurons. J. Neurosci., 23, 2715-2725.
33. Blum, R., Kafitz, K.W. and Konnerth, A. (2002) Neurotrophin-evoked depolarization requires the sodium channel Nav1.9. Nature, 419, 687-693.
34. Milner, L.D. and Landmesser, L.T. (1999) Cholinergic and GABAergic inputs drive patterned spontaneous motoneuron activity before target contact. J. Neurosci., 19, 3007-3022.
35. Zhou, F.Q. and Snider, W.D. (2006) Intracellular control of developmental and regenerative axon growth. Philos. Trans. R. Soc. Lond. B Biol. Sci, 361, 1575-1592.
36. Baker, M.D., Chandra, S.Y., Ding, Y., Waxman, S.G. and Wood, J.N. (2003) GTP-induced tetrodotoxin-resistant Na + current regulates excitability in mouse and rat small diameter sensory neurones. J. Physiol., 548, 373-382.
37. Coste, B., Osorio, N., Padilla, F., Crest, M. and Delmas, P. (2004) Gating and modulation of presumptive NaV1.9 channels in enteric and spinal sensory neurons. Mol. Cell Neurosci., 26, 123-134.
38. Kastanenka, K.V. and Landmesser, L.T. (2010) In vivo activation of channelrhodopsin-2 reveals that normal patterns of spontaneous activity are required for motoneuron guidance and maintenance of guidance molecules. J. Neurosci., 30, 10575-10585.
39. Kafitz, K.W., Rose, C.R., Thoenen, H. and Konnerth, A. (1999) Neurotrophin-evoked rapid excitation through TrkB receptors. Nature, 401, 918-921.
40. Lang, S.B., Stein, V., Bonhoeffer, T. and Lohmann, C. (2007) Endogenous brain-derived neurotrophic factor triggers fast calcium transients at synapses in developing dendrites. J. Neurosci., 27, 1097-1105.
41. Minichiello, L. (2009) TrkB signalling pathways in LTP and learning. Nat. Rev. Neurosci., 10, 850-860.
42. Brigadski, T., Hartmann, M. and Lessmann, V. (2005) Differential vesicular targeting and time course of synaptic secretion of the mammalian neurotrophins. J. Neurosci., 25, 7601-7614.
43. Blum, R. and Konnerth, A. (2005) Neurotrophin-mediated rapid signaling in the central nervous system: mechanisms and functions. Physiology (Bethesda), 20, 70-78.
44. Wiese, S., Jablonka, S., Holtmann, B., Orel, N., Rajagopal, R., Chao, M.V. and Sendtner, M. (2007) Adenosine receptor A2A-R contributes to motoneuron survival by transactivating the tyrosine kinase receptor TrkB. Proc. Natl. Acad. Sci. USA, 104, 17210-17215.
45. Rush, A.M. and Waxman, S.G. (2004) PGE2 increases the tetrodotoxin-resistant Nav1.9 sodium current in mouse DRG neurons via G-proteins. Brain Res., 1023, 264-271.
46. Leo, S., D'Hooge, R. and Meert, T. (2010) Exploring the role of nociceptor-specific sodium channels in pain transmission using Nav1.8 and Nav1.9 knockout mice. Behav. Brain Res., 208, 149-157.
47. Priest, B.T., Murphy, B.A., Lindia, J.A., Diaz, C., Abbadie, C., Ritter, A.M., Liberator, P., Iyer, L.M., Kash, S.F., Kohler, M.G. et al. (2005) Contribution of the tetrodotoxin-resistant voltage-gated sodium channel NaV1.9 to sensory transmission and nociceptive behavior. Proc. Natl Acad. Sci. USA, 102, 9382-9387.
48. Monani, U.R., Sendtner, M., Coovert, D.D., Parsons, D.W., Andreassi, C., Le, T.T., Jablonka, S., Schrank, B., Rossoll, W., Prior, T.W. et al. (2000) The human centromeric survival motor neuron gene (SMN2) rescues embryonic lethality in Smn(2/2) mice and results in a mouse with spinal muscular atrophy. Hum. Mol. Genet., 9, 333-339.
49. McGovern, V.L., Gavrilina, T.O., Beattie, C.E. and Burghes, A.H. (2008) Embryonic motor axon development in the severe SMA mouse. Hum. Mol. Genet., 17, 2900-2909.
50. Murray, L.M., Lee, S., Bäumer, D., Parson, S.H., Talbot, K. and Gillingwater, T.H. (2010) Pre-symptomatic development of lower motor neuron connectivity in a mouse model of severe spinal muscular atrophy. Hum. Mol. Genet., 19, 420-433.
51. McWhorter, M.L., Monani, U.R., Burghes, A.H. and Beattie, C.E. (2003) Knockdown of the survival motor neuron (Smn) protein in zebrafish causes defects in motor axon outgrowth and pathfinding. J. Cell Biol., 162, 919-931.
52. Glinka, M., Herrmann, T., Funk, N., Havlicek, S., Rossoll, W., Winkler, C. and Sendtner, M. (2010) The heterogeneous nuclear ribonucleoprotein-R is necessary for axonal beta-actin mRNA translocation in spinal motor neurons. Hum. Mol. Genet., 19, 1951-1966.
53. Rossoll, W., Jablonka, S., Andreassi, C., Kroning, A.K., Karle, K., Monani, U.R. and Sendtner, M. (2003) Smn, the spinal muscular atrophy-determining gene product, modulates axon growth and localization of beta-actin mRNA in growth cones of motoneurons. J. Cell Biol., 163, 801-812.
54. Götz, R., Wiese, S., Takayama, S., Camarero, G.C., Rossoll, W., Schweizer, U., Troppmair, J., Jablonka, S., Holtmann, B., Reed, J.C. et al. (2005) Bag1 is essential for differentiation and survival of hematopoietic and neuronal cells. Nat. Neurosci., 8, 1169-1178.
55. Durand, G.M., Marandi, N., Herberger, S.D., Blum, R. and Konnerth, A. (2006) Quantitative single-cell RT-PCR and Ca2+ imaging in brain slices. Pflugers Arch., 451, 716-726.
56. Hartmann, J., Blum, R., Kovalchuk, Y., Adelsberger, H., Kuner, R., Durand, G.M., Miyata, M., Kano, M., Offermanns, S. and Konnerth, A. (2004) Distinct roles of Galpha(q) and Galpha11 for Purkinje cell signaling and motor behavior. J. Neurosci., 24, 5119-5130.
57. Rose, C.R., Blum, R., Pichler, B., Lepier, A., Kafitz, K.W. and Konnerth, A. (2003) Truncated TrkB-T1 mediates neurotrophin-evoked calcium signalling in glia cells. Nature, 426, 74-78.
58. Rasmussen, R. (2001) Quantification on the LightCycler. In: Meurer, S., Wittwer, C. and Nakawara, K. (eds), Rapid Cycle Real-Time PCR, Methods and Applications. Springer, Berlin, Heidelberg, pp. 21-34.
59. Liss, B. (2002) Improved quantitative real-time RT-PCR for expression profiling of individual cells. Nucleic Acids Res., 30, e89.
60. Elbashir, S.M., Harborth, J., Lendeckel, W., Yalcin, A., Weber, K. and Tuschl, T. (2001) Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature, 411, 494-498.
61. Rubinson, D.A., Dillon, C.P., Kwiatkowski, A.V., Sievers, C., Yang, L., Kopinja, J., Rooney, D.L., Zhang, M., Ihrig, M.M., McManus, M.T. et al. (2003) A lentivirus-based system to functionally silence genes in primary mammalian cells, stem cells and transgenic mice by RNA interference. Nat. Genet., 33, 401-406.
62. Shaner, N.C., Campbell, R.E., Steinbach, P.A., Giepmans, B.N., Palmer, A.E. and Tsien, R.Y. (2004) Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat. Biotechnol., 22, 1567-1572.
63. Zufferey, R., Nagy, D., Mandel, R.J., Naldini, L. and Trono, D. (1997) Multiply attenuated lentiviral vector achieves efficient gene delivery in vivo. Nat. Biotechnol., 15, 871-875.
64. Rehberg, M., Lepier, A., Solchenberger, B., Osten, P. and Blum, R. (2008) A new non-disruptive strategy to target calcium indicator dyes to the endoplasmic reticulum. Cell Calcium, 44, 386-399.
65. Dull, T., Zufferey, R., Kelly, M., Mandel, R.J., Nguyen, M., Trono, D. and Naldini, L. (1998) A third-generation lentivirus vector with a conditional packaging system. J. Virol., 72, 8463-8471.
66. Naldini, L., Blomer, U., Gallay, P., Ory, D., Mulligan, R., Gage, F.H., Verma, I.M. and Trono, D. (1996) In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science, 272, 263-267.