Innexins ogre and inx2 are required in glial cells for normal postembryonic development of the drosophila central nervous system

Journal of Cell Science

Volumn 126, Issue 17, 2013, Pages 3823-3834

  Holcroft, Catherine E ^a   Jackson, William D ^a   Lin, Wei Hsiang ^b   Bassiri, Kayleigh ^a   Baines, Richard A ^b   Phelan, Pauline ^a  

^a UNIVERSITY OF KENT   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Connexin; Drosophila; Gap junction; Glia; Innexin; Nervous system

Indexed keywords

GAP JUNCTION PROTEIN; INNEXIN 2; OPTIC GANGLION REDUCED INNEXIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BEHAVIOR DISORDER; CELL PROLIFERATION; CENTRAL NERVOUS SYSTEM; CHANNEL GATING; CONTROLLED STUDY; DOWN REGULATION; DROSOPHILA; EMBRYO DEVELOPMENT; FEMALE; GAP JUNCTION; GENE TARGETING; GLIA CELL; HETEROLOGOUS EXPRESSION; LARVA; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROEPITHELIUM; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RNA INTERFERENCE; SURVIVOR; TRANSGENE; XENOPUS LAEVIS;

CONNEXIN; DROSOPHILA; GAP JUNCTION; GLIA; INNEXIN; NERVOUS SYSTEM;

ANIMALS; BASE SEQUENCE; CENTRAL NERVOUS SYSTEM; CONNEXINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GAP JUNCTIONS; ION CHANNELS; MEMBRANE PROTEINS; NERVE TISSUE PROTEINS; NEUROGLIA; OOCYTES; RNA INTERFERENCE; RNA, SMALL INTERFERING; XENOPUS LAEVIS;

EID: 84883301354     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.117994     Document Type: Article

References (57)

1. Awasaki, T., Lai, S.-L., Ito, K. and Lee, T. (2008). Organization and postembryonic development of glial cells in the adult central brain of Drosophila. J. Neurosci. 28, 13742-13753.
2. Awasaki, T., Huang, Y., O'Connor, M. B. and Lee, T. (2011). Glia instruct developmental neuronal remodeling through TGF-b signaling. Nat. Neurosci. 14, 821-823.
3. Bauer, R., Lehmann, C., Fuss, B., Eckardt, F. and Hoch, M. (2002). The Drosophila gap junction channel gene innexin 2 controls foregut development in response to Wingless signalling. J. Cell Sci. 115, 1859-1867.
4. Bauer, R., Lehmann, C., Martini, J., Eckardt, F. and Hoch, M. (2004). Gap junction channel protein innexin 2 is essential for epithelial morphogenesis in the Drosophila embryo. Mol. Biol. Cell 15, 2992-3004.
5. Beckervordersandforth, R. M., Rickert, C., Altenhein, B. and Technau, G. M. (2008). Subtypes of glial cells in the Drosophila embryonic ventral nerve cord as related to lineage and gene expression. Mech. Dev. 125, 542-557.
6. Bruzzone, R., Hormuzdi, S. G., Barbe, M. T., Herb, A. and Monyer, H. (2003). Pannexins, a family of gap junction proteins expressed in brain. Proc. Natl. Acad. Sci. USA 100, 13644-13649.
7. Caldwell, M. C. and Datta, S. (1998). Expression of cyclin E or DP/E2F rescues the G1 arrest of trol mutant neuroblasts in the Drosophila larval central nervous system. Mech. Dev. 79, 121-130.
8. Colman, A. (1984). Expression of exogenous RNA in Xenopus oocytes. In: Transcription and Translation-a Practical Approach (ed. B. D. Hames and S. J. Higgins), pp. 271- 302. Oxford: IRL Press.
9. Connell-Crowley, L., Vo, D., Luke, L. and Giniger, E. (2007). Drosophila lacking the Cdk5 activator, p35, display defective axon guidance, age-dependent behavioral deficits and reduced lifespan. Mech. Dev. 124, 341-349.
10. Curtin, K. D., Zhang, Z. and 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.
11. Dawkins, R. and Dawkins, M. (1976). Hierarchical organization and postural facilitation: rules for grooming in flies. Anim. Behav. 24, 739-755.
12. DePriest, A., Phelan, P. and Skerrett, I. M. (2011). Tryptophan scanning mutagenesis of the first transmembrane domain of the innexin Shaking-B(Lethal). Biophys. J. 101, 2408-2416.
13. Dietzl, G., Chen, D., Schnorrer, F., Su, K.-C., Barinova, Y., Fellner, M., Gasser, B., Kinsey, K., Oppel, S., Scheiblauer, S. et al. (2007). A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448, 151-156.
14. Dumstrei, K., Wang, F. and Hartenstein, V. (2003). Role of DE-cadherin in neuroblast proliferation, neural morphogenesis, and axon tract formation in Drosophila larval brain development. J. Neurosci. 23, 3325-3335.
15. Ebens, A. J., Garren, H., Cheyette, B. N. and Zipursky, S. L. (1993). The Drosophila anachronism locus: a glycoprotein secreted by glia inhibits neuroblast proliferation. Cell 74, 15-27.
16. Eberl, D. F., Duyk, G. M. and Perrimon, N. (1997). A genetic screen for mutations that disrupt an auditory response in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 94, 14837-14842.
17. Egger, B., Boone, J. Q., Stevens, N. R., Brand, A. H. and Doe, C. Q. (2007). Regulation of spindle orientation and neural stem cell fate in the Drosophila optic lobe. Neural Dev. 2, 1.
18. Elias, L. A. B., Wang, D. D. and Kriegstein, A. R. (2007). Gap junction adhesion is necessary for radial migration in the neocortex. Nature 448, 901-907.
19. Goodenough, D. A. and Paul, D. L. (2003). Beyond the gap: functions of unpaired connexon channels. Nat. Rev. Mol. Cell Biol. 4, 285-294.
20. Halter, D. A., Urban, J., Rickert, C., Ner, S. S., Ito, K., Travers, A. A. and Technau, G. M. (1995). The homeobox gene repo is required for the differentiation and maintenance of glia function in the embryonic nervous system of Drosophila melanogaster. Development 121, 317-332.
21. Hartenstein, V., Nassif, C. and Lekven, A. (1998). Embryonic development of the Drosophila brain. II. Pattern of glial cells. J. Comp. Neurol. 402, 32-47.
22. Hofbauer, A. and Campos-Ortega, J. A. (1990). Proliferation pattern and early differentiation of the optic lobes in Drosophila melanogaster. Rouxs Arch. Dev. Biol. 198, 264-274.
23. Huang, Y. J., Maruyama, Y., Dvoryanchikov, G., Pereira, E., Chaudhari, N. and Roper, S. D. (2007). The role of pannexin 1 hemichannels in ATP release and cellcell communication in mouse taste buds. Proc. Natl. Acad. Sci. USA 104, 6436-6441.
24. Ito, K., Urban, J. and Technau, G. M. (1995). Distribution, classification, and development of Drosophila glial cells in the late embryonic and early larval ventral nerve cord. Rouxs Arch. Dev. Biol. 204, 284-307.
25. Landesman, Y., White, T. W., Starich, T. A., Shaw, J. E., Goodenough, D. A. and Paul, D. L. (1999). Innexin-3 forms connexin-like intercellular channels. J. Cell Sci. 112, 2391-2396.
26. Lehmann, C., Lechner, H., Löer, B., Knieps, M., Herrmann, S., Famulok, M., Bauer, R. and Hoch, M. (2006). Heteromerization of innexin gap junction proteins regulates epithelial tissue organization in Drosophila. Mol. Biol. Cell 17, 1676-1685.
27. Li, Q., Lau, A., Morris, T. J., Guo, L., Fordyce, C. B. and Stanley, E. F. (2004). A syntaxin 1, Galpha(o), and N-type calcium channel complex at a presynaptic nerve terminal: analysis by quantitative immunocolocalization. J. Neurosci. 24, 4070-4081.
28. Lipshitz, H. D. and Kankel, D. R. (1985). Specificity of gene action during central nervous system development in Drosophila melanogaster: analysis of the lethal (1) optic ganglion reduced locus. Dev. Biol. 108, 56-77.
29. Marziano, N. K., Hasegawa, D. K., Phelan, P. and Turnbull, M. W. (2011). Functional interactions between polydnavirus and host cellular innexins. J. Virol. 85, 10222-10229.
30. Ostrowski, K., Bauer, R. and Hoch, M. (2008). The Drosophila innexin 7 gap junction protein is required for development of the embryonic nervous system. Cell Commun. Adhes. 15, 155-167.
31. Panchin, Y., Kelmanson, I., Matz, M., Lukyanov, K., Usman, N. and Lukyanov, S. (2000). A ubiquitous family of putative gap junction molecules. Curr. Biol. 10, R473-R474.
32. Park, Y., Fujioka, M., Kobayashi, M., Jaynes, J. B. and Datta, S. (2001). even skipped is required to produce a trans-acting signal for larval neuroblast proliferation that can be mimicked by ecdysone. Development 128, 1899-1909.
33. Phelan, P. (2005). Innexins: members of an evolutionarily conserved family of gapjunction proteins. Biochim. Biophys. Acta 1711, 225-245.
34. Phelan, P., Nakagawa, M., Wilkin, M. B., Moffat, K. G., O'Kane, C. J., Davies, J. A. and Bacon, J. P. (1996). Mutations in shaking-B prevent electrical synapse formation in the Drosophila giant fiber system. J. Neurosci. 16, 1101-1113.
35. Phelan, P., Stebbings, L. A., Baines, R. A., Bacon, J. P., Davies, J. A. and Ford, C. (1998). Drosophila Shaking-B protein forms gap junctions in paired Xenopus oocytes. Nature 391, 181-184.
36. Phelan, P., Goulding, L. A., Tam, J. L. Y., Allen, M. J., Dawber, R. J., Davies, J. A. and Bacon, J. P. (2008). Molecular mechanism of rectification at identified electrical synapses in the Drosophila giant fiber system. Curr. Biol. 18, 1955-1960.
37. Phillis, R. W., Bramlage, A. T., Wotus, C., Whittaker, A., Gramates, L. S., Seppala, D., Farahanchi, F., Caruccio, P. and Murphey, R. K. (1993). Isolation of mutations affecting neural circuitry required for grooming behavior in Drosophila melanogaster. Genetics 133, 581-592.
38. Rath, A. and Deber, C. M. (2013). Correction factors for membrane protein molecular weight readouts on sodium dodecyl sulfate-polyacrylamide gel electrophoresis. Anal. Biochem. 434, 67-72.
39. Samuels, S. E., Lipitz, J. B., Dahl, G. and Muller, K. J. (2010). Neuroglial ATP release through innexin channels controls microglial cell movement to a nerve injury. J. Gen. Physiol. 136, 425-442.
40. Singh, R. N., Singh, K. and Kankel, D. R. (1989). Development and fine structure of the nervous system of lethal(1)optic ganglion reduced visual mutants of Drosophila melanogaster. In Neurobiology of Sensory Systems (ed. R. N. Singh and N. J. Strausfeld), pp. 203-218. New York, NY: Plenum Press.
41. Spray, D. C., Harris, A. L. and Bennett, M. V. L. (1981). Equilibrium properties of a voltage-dependent junctional conductance. J. Gen. Physiol. 77, 77-93.
42. Spray, D. C., Ye, Z.-C. and Ransom, B. R. (2006). Functional connexin 'hemichannels': a critical appraisal. Glia 54, 758-773.
43. Starich, T. A., Miller, A., Nguyen, R. L., Hall, D. H. and Shaw, J. E. (2003). The Caenorhabditis elegans innexin INX-3 is localized to gap junctions and is essential for embryonic development. Dev. Biol. 256, 403-417.
44. Stebbings, L. A., Todman, M. G., Phelan, P., Bacon, J. P. and Davies, J. A. (2000). Two Drosophila innexins are expressed in overlapping domains and cooperate to form gap-junction channels. Mol. Biol. Cell 11, 2459-2470.
45. Stebbings, L. A., Todman, M. G., Phillips, R., Greer, C. E., Tam, J., Phelan, P., Jacobs, K., Bacon, J. P. and Davies, J. A. (2002). Gap junctions in Drosophila: developmental expression of the entire innexin gene family. Mech. Dev. 113, 197- 205.
46. Stork, T., Bernardos, R. and Freeman, M. R. (2012). Analysis of glial cell development and function in Drosophila. Cold Spring Harb. Protoc. 2012, 1-17.
47. Swenson, K. I., Jordan, J. R., Beyer, E. C. and Paul, D. L. (1989). Formation of gap junctions by expression of connexins in Xenopus oocyte pairs. Cell 57, 145-155.
48. Tazuke, S. I., Schulz, C., Gilboa, L., Fogarty, M., Mahowald, A. P., Guichet, A., Ephrussi, A., Wood, C. G., Lehmann, R. and Fuller, M. T. (2002). A germlinespecific gap junction protein required for survival of differentiating early germ cells. Development 129, 2529-2539.
49. Thompson, R. J., Jackson, M. F., Olah, M. E., Rungta, R. L., Hines, D. J., Beazely, M. A., MacDonald, J. F. and MacVicar, B. A. (2008). Activation of pannexin-1 hemichannels augments aberrant bursting in the hippocampus. Science 322, 1555- 1559.
50. Trimarchi, J. R. and Murphey, R. K. (1997). The shaking-B2 mutation disrupts electrical synapses in a flight circuit in adult Drosophila. J. Neurosci. 17, 4700-4710.
51. Voigt, A., Pflanz, R., Schäfer, U. and Jäckle, H. (2002). Perlecan participates in proliferation activation of quiescent Drosophila neuroblasts. Dev. Dyn. 224, 403-412.
52. Watanabe, T. and Kankel, D. R. (1992). The l(1)ogre gene of Drosophila melanogaster is expressed in postembryonic neuroblasts. Dev. Biol. 152, 172-183.
53. Wei, C.-J., Xu, X. and Lo, C. W. (2004). Connexins and cell signaling in development and disease. Annu. Rev. Cell Dev. Biol. 20, 811-838.
54. White, T. W. and Paul, D. L. (1999). Genetic diseases and gene knockouts reveal diverse connexin functions. Annu. Rev. Physiol. 61, 283-310.
55. Wu, C.-L., Shih, M.-F. M., Lai, J. S.-Y., Yang, H.-T., Turner, G. C., Chen, L. and Chiang, A.-S. (2011). Heterotypic gap junctions between two neurons in the Drosophila brain are critical for memory. Curr. Biol. 21, 848-854.
56. Yen, M. R. and Saier, M. H., Jr (2007). Gap junctional proteins of animals: the innexin/pannexin superfamily. Prog. Biophys. Mol. Biol. 94, 5-14.
57. Younossi-Hartenstein A., Salvaterra, P. M. and Hartenstein, V. (2003). Early development of the Drosophila brain: IV. Larval neuropile compartments defined by glial septa. J. Comp. Neurol. 455, 435-450.