Two Drosophila innexins are expressed in overlapping domains and cooperate to form gap-junction channels

Molecular Biology of the Cell

Volumn 11, Issue 7, 2000, Pages 2459-2470

  Stebbings, Lucy A ^a   Todman, Martin G ^a   Phelan, Pauline ^a,b   Bacon, Jonathan P ^a   Davies, Jane A ^a  

^a UNIVERSITY OF SUSSEX   (United Kingdom)

^b UNIVERSITY OF KENT   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

INNEXIN; INSECT PROTEIN; MESSENGER RNA; UNCLASSIFIED DRUG;

ARTICLE; CELL VIABILITY; DROSOPHILA; ELECTROPHYSIOLOGY; EMBRYO DEVELOPMENT; GAP JUNCTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION;

ANIMALIA; DROSOPHILA; HEXAPODA; INSECTA; INVERTEBRATA; VERTEBRATA;

EID: 0033916033     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.11.7.2459     Document Type: Article

References (59)

1. Avery, L. (1993). The genetics of feeding in Caenorhabditis elegans. Genetics 133, 897-917.
2. Barnes, T.M., and Hekimi, S. (1997). The Caenorhabditis elegans avermectin resistance and anesthetic response gene unc-9 encodes a member of a protein family implicated in electrical coupling of excitable cells. J. Neurochem. 69, 2251-2260.
3. Barrio, L.C., Suchyna, T., Bargiello, T., Xu, L.X., Roginski, R.S., Bennett, M.V.L., and Nicholson, B.J. (1991). Gap junctions formed by Connexin 26 and 32 alone and in combination are differently affected by applied voltage. Proc. Natl. Acad. Sci. USA 88, 8410-8414.
4. Bennett, M.V.L. (1997). Gap junctions as electrical synapses. J. Neurocytol. 26, 349-366.
5. Bevans, C.G., and Harris, A.L. (1999). Regulation of connexin channels by pH - Direct action of the protonated form of taurine and other aminosulfonates. J. Biol. Chem. 274, 3711-3719.
6. Blagburn, J.M., Alexopoulos, H., Davies, J.A., and Bacon, J.P. (1999). Null mutation in shaking-B eliminates electrical, but not chemical, synapses in the Drosophila giant fiber system: a structural study. J. Comp. Neurol. 404, 449-458.
7. Blennerhassett, M.G., and Caveney, S. (1984). Separation of developmental compartments by a cell type with reduced junctional permeability. Nature 309, 361-364.
8. Brand, A.H., and Perrimon, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415.
9. Bruzzone, R., White, T.W., Yoshizaki, G., Patino, R., and Paul, D.L. (1995). Intercellular channels in teleosts: functional characterization of two connexins from Atlantic croaker. FEBS Lett. 358, 301-304.
10. Bruzzone, R., White, T.W., and Paul, D.L. (1996). Connections with connexins: the molecular basis of direct intercellular signaling. Eur. J. Biochem. 238, 1-27.
11. Bukauskas, F.F., Kempf, C., and Weingart, R. (1992). Electrical coupling between cells of the insect Ades albopictus. J. Physiol. 448, 321-337.
12. Bukauskas, F.F., Vogel, R., and Weingart, R. (1997). Biophysical properties of heterotypic gap junctions newly formed between two types of insect cells. J. Physiol. 499, 701-713.
13. Chang, M., Werner, R., and Dahl, G. (1996). A role for an inhibitory connexin in testis? Dev. Biol. 175, 50-56.
14. Churchill, D., and Caveney, S. (1993). Double whole-cell patchclamp characterization of gap junctional channels in isolated insect epidermal cell pairs. J. Membrane Biol. 135, 165-180.
15. Colman, A. (1984). In: Transcription and Translation-A Practical Approach, ed. B.D. Hames and S.J. Higgins, Oxford, UK: IRL, 271-302.
16. Crompton, D., Todman, M., Wilkin, M., Ji, S., and Davies, J. (1995). Essential and neural transcripts from the Drosophila shaking-B locus are differentially expressed in the embryonic mesoderm and pupal nervous system. Dev. Biol. 170, 142-158.
17. Curtin, K.D., Zhang, Z., and Wyman, R.J. (1999). Drosophila has several genes for gap junction proteins. Gene 232, 191-201.
18. Ebihara, L., Xu, X., Oberti, C., Beyer, E.C., and Berthoud, V.M. (1999). Co-expression of lens fiber connexins modifies hemi-gapjunctional channel behavior. Biophys. J. 76, 198-206.
19. Falk, M.M., Buehler, L.K., Kumar, N.M., and Gilula, N.B. (1997). Cell-free synthesis and assembly of connexins into functional gap junction membrane channels. EMBO J. 16, 2703-2716.
20. Ganfornina, M.D., Sanchez, D., Herrera, M., and Bastiani, M.J. (1999). Developmental expression and molecular characterization of two gap junction channel proteins expressed during embryogenesis in the grasshopper Schistocerca americana. Dev. Genet. 24, 137-150.
21. Gho, M. (1994). Voltage-clamp analysis of gap junctions between embryonic muscles in Drosophila. J. Physiol. 481, 371-383.
22. Hartl, D.L., Nurminsky, D.I., Jones, R.W., and Lozovskaya, E.R. (1994). Genome structure and evolution in Drosophila: applications of the framework Pl map. Proc. Natl. Acad. Sci. USA 91, 6824-6829.
23. He, D.S., Jiang, J.X., Taffet, S.M., and Burt, J.M. (1999). Formation of heteromeric gap junction channels by connexins 40 and 43 in vascular smooth muscle cells. Proc. Natl. Acad. Sci. USA 96, 6495-6500.
24. Hennemann, H., Dahl, E., White, J.B., Schwarz, H.J., Lalley, P.A., Chang, S., Nicholson, B.J., and Willecke, K. (1992). Two gap junction genes, connexin 31.1 and 30.3, are closely linked on mouse chromosome 4 and preferentially expressed in skin. J. Biol. Chem. 267, 17225-17233.
25. Jiang, J.X., and Goodenough, D.A. (1996). Heteromeric connexons in lens gap junction channels. Proc. Natl. Acad. Sci. USA 93, 1287-1291.
26. Karess, R.E., and Rubin, G.M. (1984). Analysis of P transposable element functions in Drosophila. Cell 38, 135-146.
27. Krishnan, S.N., Frei, E., Swain, G.P., and Wyman, R.J. (1993). Passover: a gene required for synaptic connectivity in the giant fiber system of Drosophila. Cell 73, 967-977.
28. 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 channel. J. Cell. Sci. 112, 2391-2396.
29. Lee, M.-J., and Rhee, S.K. (1998). Heteromeric gap junction channels in rat hepatocytes in which the expression of connexin26 is induced. Molecules and Cells 8, 295-300.
30. Lehmann, R., and Tautz, D. (1994). In situ hybridization to RNA. Methods Cell. Biol. 44, 575-598.
31. Lennon, G., Auffray, C., Polymeropoulos, M., and Soares, M.B. (1996). The I.M.A.G.E. consortium: an integrated molecular analysis of genomes and their expression. Genomics 33, 151-152.
32. 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.
33. Manning, G., and Krasnow, M.G. (1993). Development of the Drosophila tracheal system. In: The Development of Drosophila melanogaster, vol. I, ed. M. Bate and A. Martinez-Arias, Cold Spring Harbor: Cold Spring Harbor Laboratory Press, 609-685.
34. Obaid, A.L., Socolar, S.J., and Rose, B. (1983). Cell-to-cell channels with two independently regulated gates in series: analysis of junctional conductance modulation by membrane-potential, calcium, and pH. J. Membrane Biol. 73, 69-89.
35. 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.
36. Phelan, P., Stebbings, L.A., Baines, R.A., Bacon, J.P., Davies, J.A., and Ford, C. (1998a). Drosophila Shaking-B protein forms gap junctions in paired Xenopus oocytes. Nature 391, 181-184.
37. Phelan, P., et al. (1998b). Innexins: a family of invertebrate gapjunction proteins. Trends. Genet. 14, 348-349.
38. Phelan, P. (2000). Gap junction communication in invertebrates: the innexin gene family. Curr. Top. Membranes 49, 389-422.
39. Ruangvoravat, C.P., and Lo, C.W. (1992). Restrictions in gap junctional communication in the Drosophila larval epidermis. Dev. Dynamics 193, 70-82.
40. Samakovlis, C., Hacohen, N., Manning, G., Sutherland, D.C., Guillemin, K., and Krasnow, M.A. (1996). Development of the Drosophila tracheal system occurs by a series of morphologically distinct but genetically coupled branching events. Development 122, 1395-1407.
41. Spradling, A.C., and Rubin, G.M. (1982). Transposition of cloned P elements into Drosophila germ line chromosomes. Science 218, 341-347.
42. 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.
43. Starich, T.A., Herman, R.K., and Shaw, J.E. (1993). Molecular and genetic analysis of unc-7, a Caenorhabditis elegans gene required for coordinated locomotion. Genetics 133, 527-541.
44. Starich, T.A., Lee, R.Y.N., Panzarella, C., Avery, L., and Shaw, J.E. (1996). eat-5 and unc-7 represent a multigene family in Caenorhabditis elegans involved in cell-cell coupling. J. Cell Biol. 134, 537-548.
45. Stauffer, K.A. (1995). The gap junction proteins betal connexin (connexin 32) and beta2 connexin (connexin 26) can form heteromeric hemi-channels. J. Biol. Chem. 270, 6768-6772.
46. Swenson, K.I., Jordan, J.R., Beyer, E.G., and Paul, D.L. (1989). Formation of gap junctions by expression of connexins in Xenopus oocyte pairs. Cell 57, 145-155.
47. Tepass, U., and Hartenstein, V. (1994). The development of cellular junctions in the Drosophila embryo. Dev. Biol. 161, 563-596.
48. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F., and Higgins, D.G. (1997). The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25, 4876-4882.
49. Todman, M.G., Baines, R.A., Stebbings, L.A., Davies, J.A., and Bacon, J.P. (1999). Gap-junctional communication between developing Drosophila muscles is essential for their normal development. Dev. Genet. 24, 57-68.
50. 2 mutation disrupts electrical synapses in a flight circuit in adult Drosophila. J. Neurosci. 17, 4700-4710.
51. Unger, V.M., Kumar, N.M., Gilula, N.B., and Yeager, M. (1999). Three-dimensional structure of a recombinant gap junction membrane channel. Science 283, 1176-1180.
52. Verselis, V.K., Bennett, M.V.L., and Bargiello, T.A. (1991). A voltage dependent gap junction in Drosophila melanogaster. Biophys. J. 59, 114-126.
53. Warner, A.E., and Lawrence, P.A. (1982). Permeability of gap junctions at the segmental border in insect epidermis. Cell 28, 243-252.
54. Watanabe, T., and Kankel, D.R. (1990). Molecular cloning and analysis of l(1)ogre, a locus of Drosophila melanogaster with prominent effects on the postembryonic development of the central nervous system. Genetics 126, 1033-1044.
55. Werner, R., Levine, E., Rabadan-Diehl, C., and Dahl, G. (1989). Formation of hybrid cell-cell channels. Proc. Natl. Acad. Sci. USA 86, 5380-5384.
56. Wilders, R., and Jongsma, H.J. (1992). Limitations of the dual voltage clamp method in assaying conductance and kinetics of gap junction channels. Biophys. J. 63, 942-953.
57. Wilson, R.K. (1999). How the worm was won - the C. elegans genome sequencing project. Trends Genet. 15, 51-58.
58. Yeager, M., and Nicholson, B.J. (1996). Structure of gap junction intercellular channels. Curr. Opin. Structural Biol. 6, 183-192.
59. Zhang, Z., Curtin, K.D., Sun, Y.-A., and Wyman, R.J. (1999). Nested transcripts of gap junction gene have distinct expression patterns. J. Neurobiol. 40, 288-301.