Innexins in the lobster stomatogastric nervous system: Cloning, phylogenetic analysis, developmental changes and expression within adult identified dye and electrically coupled neurons

European Journal of Neuroscience

Volumn 24, Issue 11, 2006, Pages 3119-3133

  Ducret, E ^a   Alexopoulos, H ^b,c   Le Feuvre, Y ^a   Davies, J A ^b   Meyrand, P ^a   Bacon, J P ^b   Fenelon V S ^a  

^a UNIVERSITÉ DE BORDEAUX   (France)

^b UNIVERSITY OF SUSSEX   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Development; Gap junctions; Homarus gammarus; In situ hybridization; Stomatogastric ganglion

Indexed keywords

DYE; INNEXIN 1; INNEXIN 2; MESSENGER RNA; STRUCTURAL PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; COMPARATIVE STUDY; CRUSTACEA; DOWN REGULATION; EMBRYO DEVELOPMENT; GANGLION; GENE DUPLICATION; IN SITU HYBRIDIZATION; LOBSTER; MOLECULAR BIOLOGY; MOLECULAR CLONING; MOLECULAR PHYLOGENY; NERVE CELL; NERVE CELL NETWORK; NERVOUS SYSTEM; NERVOUS SYSTEM DEVELOPMENT; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; STATISTICAL SIGNIFICANCE; STOMACH INNERVATION;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CELL COMMUNICATION; CONNEXINS; DNA, COMPLEMENTARY; DROSOPHILA PROTEINS; EVOLUTION, MOLECULAR; FLUORESCENT DYES; GANGLIA, INVERTEBRATE; GAP JUNCTIONS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MEMBRANE POTENTIALS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; NEPHROPIDAE; NERVE TISSUE PROTEINS; NERVOUS SYSTEM; NEURONS; PHYLOGENY; SEQUENCE HOMOLOGY, AMINO ACID; SEQUENCE HOMOLOGY, NUCLEIC ACID;

EID: 33845665431     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2006.05209.x     Document Type: Article

References (51)

1. Adams, M.D., Celniker, S.E., Holt, R.A., Evans, C.A., Gocayne, J.D., Amanatides, P.G., Scherer, S.E., Li, P.W., Hoskins, R.A., Galle, R.F., George, R.A., Lewis, S.E., Richards, S., Ashburner, M., Henderson, S.N., Sutton, G.G., Wortman, J.R., Yandell, M.D., Zhang, Q., Chen, L.X., Brandon, R.C., Rogers, Y.H., Blazej, R.G., Champe, M., Pfeiffer, B.D., Wan, K.H., Doyle, C., Baxter, E.G., Helt, G., Nelson, C.R., Gabor, G.L., Abril, J.F., Agbayani, A., An, H.J., Andrews-Pfannkoch, C., Baldwin, D., Ballew, R.M., Basu, A., Baxendale, J., Bayraktaroglu, L., Beasley, E.M., Beeson, K.Y., Benos, P.V., Berman, B.P., Bhandari, D., Bolshakov, S., Borkova, D., Botchan, M.R., Bouck, J., Brokstein, P., Brottier, P., Burtis, K.C., Busam, D.A., Butler, H., Cadieu, E., Center, A., Chandra, I., Cherry, J.M., Cawley, S., Dahlke, C., Davenport, L.B., Davies, P., de Pablos, B., Delcher, A., Deng, Z., Mays, A.D., Dew, I., Dietz, S.M., Dodson, K., Doup, L.E., Downes, M., Dugan-Rocha, S., Dunkov, B.C., Dunn, P., Durbin, K.J., Evangelista, C.C., Ferraz, C., Ferriera, S., Fleischmann, W., Fosler, C., Gabrielian, A.E., Garg, N.S., Gelbart, W.M., Glasser, K., Glodek, A., Gong, F., Gorrell, J.H., Gu, Z., Guan, P., Harris, M., Harris, N.L., Harvey, D., Heiman, T.J., Hernandez, J.R., Houck, J., Hostin, D., Houston, K.A., Howland, T.J., Wei, M.H., Ibegwam, C (2000) The genome sequence of Drosophila melanogaster. Science, 287, 2185-2195.
2. Alexopoulos, H., Bottger, A., Fischer, S., Levin, A., Wolf, A., Fujisawa, T., Hayakawa, S., Gojobori, T., Davies, J.A., David, C.N. & Bacon, J.P. (2004) Evolution of gap junctions: the missing link? Curr. Biol., 14, R879-R880.
3. Alexopoulos, H., Dykes, I.M., Bacon, J.P. & Davies, J.A. (2000) Novel innexins in snails and leeches. Eur. J. Neurosci., 11, 15.
4. Baro, D.J., Cole, C.L., Zarrin, A.R., Hughes, S. & Harris-Warrick, R.M. (1994) Shab gene expression in identified neurons of the pyloric network in the lobster stomatogastric ganglion. Receptors Channels, 2, 193-205.
5. Bem, T., Le Feuvre, Y., Rinzel, J. & Meyrand, P. (2005) Electrical coupling induces bistability of rhythms in networks of inhibitory spiking neurons. Eur. J. Neurosci., 22, 2661-2668.
6. Bem, T., Le Feuvre, Y., Simmers, J. & Meyrand, P. (2002) Electrical coupling can prevent expression of adult-like properties in an embryonic neural circuit. J. Neurophysiol., 87, 538-547.
7. Bem, T. & Rinzel, J. (2004) Short duty cycle destabilizes a half-center oscillator, but gap junctions can restabilize the anti-phase pattern. J. Neurophysiol., 91, 693-703.
8. Bruzzone, R., Hormuzdi, S.G., Barbe, M.T., Herb, A. & Monyer, H. (2003) Pannexins, a family of gap junction proteins expressed in brain. Proc. Natl Acad. Sci. USA, 100, 13644-13649.
9. Casasnovas, B. & Meyrand, P. (1995) Functional differentiation of adult neural circuits from a single embryonic network. J. Neurosci., 15, 5703-5718.
10. Chang, Q., Gonzalez, M., Pinter, M.J. & Balice-Gordon, R.J. (1999) Gap junctional coupling and patterns of connexin expression among neonatal rat lumbar spinal motor neurons. J. Neurosci., 19, 10813-10828.
11. Combes, D., Meyrand, P. & Simmers, J. (1999) Motor pattern specification by dual descending pathways to a lobster rhythm-generating network. J. Neurosci., 19, 3610-3619.
12. Connors, B.W., Benardo, L.S. & Prince, D.A. (1983) Coupling between neurons of the developing rat neocortex. J. Neurosci., 3, 773-782.
13. Curtin, K.D., Zhang, Z. & Wyman, R.J. (2002) Gap junction proteins expressed during development are required for adult neural function in the Drosophila optic lamina. J. Neurosci., 22, 7088-7096.
14. Dehal, P., Satou, Y., Campbell, R.K., Chapman, J., Degnan, B., De Tomaso, A., Davidson, B., Di Gregorio, A., Gelpke, M., Goodstein, D.M., Harafuji, N., Hastings, K.E., Ho, I., Hotta, K., Huang, W., Kawashima, T., Lemaire, P., Martinez, D., Meinertzhagen, I.A., Necula, S., Nonaka, M., Putnam, N., Rash, S., Saiga, H., Satake, M., Terry, A., Yamada, L., Wang, H.G., Awazu, S., Azumi, K., Boore, J., Branno, M., Chin-Bow, S., DeSantis, R., Doyle, S., Francino, P., Keys, D.N., Haga, S., Hayashi, H., Hino, K., Imai, K.S., Inaba, K., Kano, S., Kobayashi, K., Kobayashi, M., Lee, B.I., Makabe, K.W., Manohar, C., Matassi, G., Medina, M., Mochizuki, Y., Mount, S., Morishita, T., Miura, S., Nakayama, A., Nishizaka, S., Nomoto, H., Ohta, F., Oishi, K., Rigoutsos, I., Sano, M., Sasaki, A., Sasakura, Y., Shoguchi, E., Shin-i, T., Spagnuolo, A., Stainier, D., Suzuki, M.M., Tassy, O., Takatori, N., Tokuoka, M., Yagi, K., Yoshizaki, F., Wada, S., Zhang, C., Hyatt, P.D., Larimer, F., Detter, C., Doggett, N., Glavina, T., Hawkins, T., Richardson, P., Lucas, S., Kohara, Y., Levine, M., Satoh, N. & Rokhsar, D.S. (2002) The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science, 298, 2157-2167.
15. Dermietzel, R., Traub, O., Hwang, T.K., Beyer, E., Bennett, M.V., Spray, D.C. & Willecke, K. (1989) Differential expression of three gap junction proteins in developing and mature brain tissues. Proc. Natl Acad. Sci. USA, 86, 10148-10152.
16. Draguhn, A., Traub, R.D., Schmitz, D. & Jefferys, J.G. (1998) Electrical coupling underlies high-frequency oscillations in the hippocampus in vitro. Nature, 394, 189-192.
17. Dykes, I.M., Freeman, F.M., Bacon, J.P. & Davies, J.A. (2004) Molecular basis of gap junctional communication in the CNS of the leech Hirudo medicinalis. J. Neurosci., 24, 886-894.
18. Felsenstein, J. (1989) Phylip - Phylogeny Inference Package Version 3.2., Cladistics, 5, 164-166.
19. Fenelon, V.S., Casasnovas, B., Faumont, S. & Meyrand, P. (1998) Ontogenetic alteration in peptidergic expression within a stable neuronal population in lobster stomatogastric nervous system. J. Comp. Neurol., 399, 289-305.
20. Jezzini, S.H., Bodnarova, M. & Moroz, L.L. (2005) Two-color in situ hybridization in the CNS of Aplysia californica. J. Neurosci. Meth., 149, 15-25.
21. Johnson, B.R. & Harris-Warrick, R.M. (1990) Aminergic modulation of graded synaptic transmission in the lobster stomatogastric ganglion. J. Neurosci., 10, 2066-2076.
22. Johnson, B.R., Peck, J.H. & Harris-Warrick, R.M. (1993) Amine modulation of electrical coupling in the pyloric network of the lobster stomatogastric ganglion. J. Comp. Physiol., 172, 715-732.
23. Le Feuvre, Y., Fenelon, V.S. & Meyrand, P. (2001) Ontogeny of modulatory inputs to motor networks: early established projection and progressive neurotransmitter acquisition. J. Neurosci., 21, 1313-1326.
24. Manor, Y., Rinzel, J., Segev, I. & Yarom, Y. (1997) Low-amplitude oscillations in the inferior olive: a model based on electrical coupling of neurons with heterogeneous channel densities. J. Neurophysiol., 77, 2736-2752.
25. Merriam, E.B., Netoff, T.I. & Banks, M.I. (2005) Bistable network behavior of layer I interneurons in auditory cortex. J. Neurosci., 25, 6175-6186.
26. Montoro, R.J. & Yuste, R. (2004) Gap junctions in developing neocortex: a review. Brain Res. Brain Res. Rev., 47, 216-226.
27. Nadarajah, B., Jones, A.M., Evans, W.H. & Parnavelas, J.G. (1997) Differential expression of connexins during neocortical development and neuronal circuit formation. J. Neurosci., 17, 3096-3111.
28. Nomura, M., Fukai, T. & Aoyagi, T. (2003) Synchrony of fast-spiking interneurons interconnected by GABAergic and electrical synapses. Neural Comput., 15, 2179-2198.
29. Panchin, Y., Kelmanson, I., Matz, M., Lukyanov, K., Usman, N. & Lukyanov, S. (2000) A ubiquitous family of putative gap junction molecules. Curr. Biol., 10, R473-R474.
30. Peinado, A., Yuste, R. & Katz, L.C. (1993a) Extensive dye coupling between rat neocortical neurons during the period of circuit formation. Neuron, 10, 103-114.
31. Peinado, A., Yuste, R. & Katz, L.C. (1993b) Gap junctional communication and the development of local circuits in neocortex. Cereb. Cortex, 3, 488-498.
32. Personius, K.E. & Balice-Gordon, R.J. (2001) Loss of correlated motor neuron activity during synaptic competition at developing neuromuscular synapses. Neuron, 31, 395-408.
33. Pfeuty, B., Mato, G., Golomb, D. & Hansel, D. (2005) The combined effects of inhibitory and electrical synapses in synchrony. Neural Comput., 17, 633-670.
34. Phelan, P., Bacon, J.P., Davies, J.A., Stebbings, L.A., Todman, M.G., Avery, L., Baines, R.A., Barnes, T.M., Ford, C., Hekimi, S., Lee, R., Shaw, J.E., Starich, T.A., Curtin, K.D., Sun, Y.A. & Wyman, R.J. (1998a) Innexins: a family of invertebrate gap-junction proteins. Trends Genet., 14, 348-349.
35. Phelan, P., Stebbings, L.A., Baines, R.A., Bacon, J.P., Davies, J.A. & Ford, C. (1998b) Drosophila Shaking-B protein forms gap junctions in paired Xenopus oocytes. Nature, 391, 181-184.
36. Potenza, N., del Gaudio, R., Rivieccio, L., Russo, G.M. & Geraci, G. (2002) Cloning and molecular characterization of the first innexin of the phylum annelida-expression of the gene during development. J. Mol. Evol., 54, 312-321.
37. Pradet-Balade, B., Boulme, F., Beug, H., Mullner, E.W. & Garcia-Sanz, J.A. (2001) Translation control: bridging the gap between genomics and proteomics? TIBS, 26, 225-229.
38. Rose, T.M., Schultz, E.R., Henikoff, J.G., Pietrokovski, S., McCallum, C.M. & Henikoff, S. (1998) Consensus-degenerate hybrid oligonucleotide primers for amplification of distantly related sequences. Nucl. Acids Res., 26, 1628-1635.
39. Sasakura, Y., Shoguchi, E., Takatori, N., Wada, S., Meinertzhagen, I.A., Satou, Y. & Satoh, N. (2003) A genomewide survey of developmentally relevant genes in Ciona intestinalis. X. Genes for cell junctions and extracellular matrix. Dev. Genes Evol., 213, 303-313.
40. Schulz, D.J., Goaillard, J.M. & Marder, E. (2006) Variable channel expression in identified single and electrically coupled neurons in different animals. Nature Neurosci., 9, 356-362.
41. Selverston, A. & Moulins, M. (1987) The Crustacean Stomatogastric System. Springer-Verlag, Berlin.
42. Sherman, A. & Rinzel, J. (1992) Rhythmogenic effects of weak electrotonic coupling in neuronal models. Proc. Natl Acad. Sci. USA, 89, 2471-2474.
43. Skinner, F.K., Zhang, L., Velazquez, J.L. & Carlen, P.L. (1999) Bursting in inhibitory interneuronal networks: a role for gap-junctional coupling. J. Neurophysiol., 81, 1274-1283.
44. Sohl, G., Degen, J., Teubner, B. & Willecke, K. (1998) The murine gap junction gene connexin36 is highly expressed in mouse retina and regulated during brain development. FEBS Lett., 428, 27-31.
45. Starich, T., Sheehan, M., Jadrich, J. & Shaw, J. (2001) Innexins in C. Elegans. Cell Commun. Adhes., 8, 311-314.
46. Stebbings, L.A., Todman, M.G., Phillips, R., Greer, C.E., Tam, J., Phelan, P., Jacobs, K., Bacon, J.P. & Davies, J.A. (2002) Gap junctions in Drosophila: developmental expression of the entire innexin gene family. Mech. Dev., 113, 197-205.
47. Sutor, B. (2002) Gap junctions and their implications for neurogenesis and maturation of synaptic circuitry in the developing neocortex. Results Probl. Cell Differ., 39, 53-73.
48. Thompson, J.D., Higgins, D.G. & Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl. Acids Res., 22, 4673-4680.
49. Traub, R.D. (1995) Model of synchronized population bursts in electrically coupled interneurons containing active dendritic conductances. J. Comput. Neurosci., 2, 283-289.
50. Vandecasteele, M., Glowinski, J. & Venance, L. (2005) Electrical synapses between dopaminergic neurons of the substantia nigra pars compacta. J. Neurosci., 25, 291-298.
51. Vaney, D.I. (1991) Many diverse types of retinal neurons show tracer coupling when injected with biocytin or Neurobiotin. Neurosci. Lett., 125, 187-190.