Cell-free synthesis and assembly of connexins into functional gap junction membrane channels

EMBO Journal

Volumn 16, Issue 10, 1997, Pages 2703-2716

  Falk, Matthias M ^a   Buehler, Lukas K ^a   Kumar, Nalin M ^a   Gilula, Norton B ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Cell free translation; Connexons; Gap junction channels; Protein oligomerization; Selective subunit assembly

Indexed keywords

GAP JUNCTION PROTEIN; ISOPROTEIN; MEMBRANE PROTEIN; PROTEIN SUBUNIT;

AMINO TERMINAL SEQUENCE; ARTICLE; BIOCHEMISTRY; BIOPHYSICS; CELL FREE SYSTEM; CELL JUNCTION; HYDRODYNAMICS; LIPID BILAYER; MEMBRANE CHANNEL; MEMBRANE VESICLE; MICROSOME MEMBRANE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN SYNTHESIS;

CELL-FREE SYSTEM; CONNEXINS; GAP JUNCTIONS; ION CHANNELS; LIPID BILAYERS; MEMBRANE FUSION; MICROSOMES; MUTATION; PATCH-CLAMP TECHNIQUES; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; PROTEIN PROCESSING, POST-TRANSLATIONAL; SEQUENCE DELETION;

EID: 0031001091     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.10.2703     Document Type: Article

References (54)

1. Anderson, D.J. and Blobel, G. (1981) In vitro synthesis, glycosylation, and membrane insertion of the four subunits of Torpedo acetylcholine receptor. Proc. Natl Acad. Sci. USA, 78, 5598-5602.
2. Babila, T., Moscucci, A., Wang, H., Weaver, F.E. and Koren, G. (1994) Assembly of mammalian voltage-gated potassium channels: evidence for an important role of the first transmembrane segment. Neuron, 12, 615-626.
3. Bai, L., Fushimi, F., Sasaki, S. and Marumo, F. (1996) Structure of aquaporin-2 vasopressin water channel. J. Biol. Chem., 271, 5171-5176.
4. Blount, P. and Merlie, J.P. (1988) Native folding of an acetylcholine receptor α subunit expressed in the absence of other receptor subunits. J. Biol. Chem., 263, 1072-1080.
5. Bruzzone, R., White, T.W. and Goodenough, D.A. (1996) The cellular internet: on-line with connexins. BioEssays, 18, 709-718.
6. 2 gap junction connexons reconstituted into planar lipid bilayers. Biophys. J., 68, 1767-1775.
7. Cascio, M., Kumar, N.M., Safarik, R. and Gilula, N.B. (1995) Physical characterization of gap junction membrane connexons (hemi-channels) isolated from rat liver. J. Biol. Chem., 270, 18643-18648.
8. Dahl, G., Miller, T., Paul, D., Voellmy, R. and Werner, R. (1987) Expression of functional cell-cell channels from cloned rat liver gap junction complementary DNA. Science, 236, 1290-1293.
9. Deal, K.K., Lovinger, D.M. and Tamkun, M.M. (1994) The brain Kv1.1 potassium channel: in vitro and in vivo studies on subunit assembly and post-translational processing. J. Neurosci., 14, 1666-1676.
10. Elfgang, C., Eckert, R., Lichtenberg-Fraté, H., Butterweck, A., Traub, O., Klein, R.A., Hülser, D.F. and Willecke, K. (1995) Specific permeability and selective formation of gap junction channels in connexin-transfected HeLa cells. J. Cell Biol., 129, 805-817.
11. Falk, M.M., Sobrino, F. and Beck, E. (1992) VPg gene amplification correlates with infective particle formation in foot-and-mouth disease virus. J. Virol., 66, 2251-2260.
12. Falk, M.M., Kumar, N.M. and Gilula, N.B. (1994) Membrane insertion of gap junction connexins: polytopic channel forming membrane proteins. J. Cell Biol., 127, 343-355.
13. Goodenough, D.A., Paul, D.L. and Jesaitis, L. (1988) Topological distribution of two connexin32 antigenic sites in intact and split rodent hepatocyte gap junctions. J. Cell Biol., 107, 1817-1824.
14. Goodenough, D.A, Goliger, J.A. and Paul, D.L. (1996) Connexins, connexons, and intercellular communication. Annu. Rev. Biochem., 65, 475-502.
15. Green, W.N. and Millar, N.S. (1995) Ion-channel assembly. Trends Neurosci., 18, 280-287.
16. Hart, G.W., Brew, K., Grant, G.A., Bradshaw, R.A. and Lennarz, W.J. (1978) Primary structural requirements for the enzymatic formation of the N-glycosidic bond in glycoproteins. J. Biol. Chem., 254, 9747-9753.
17. Hurtley, S.M. and Helenius, A. (1989) Protein oligomerization in the endoplasmic reticulum. Annu. Rev. Cell Biol. 5, 277-307.
18. Jiang, J.X. and Goodenough, D.A. (1996) Heteromeric connexons in lens gap junction channels. Proc. Natl Acad. Sci. USA. 93, 1287-1291.
19. Kistler, J., Goldie, K., Donaldson, P. and Engel, A. (1994) Reconstitution of native-type noncrystalline lens fiber gap junctions from isolated hemichannels. J. Cell Biol., 126, 1047-1058.
20. König, N. and Zampighi, G.A. (1995) Purification of bovine cell-to-cell channels composed of connexin44 and connexin50. J. Cell Sci., 108, 3091-3098.
21. Krieg, P.A. and Melton, D.A. (1984) Functional messenger RNAs are produced by SP6 in vitro transcription of cloned cDNAs. Nucleic Acids Res., 12, 7057-7070.
22. Kumar, N.M. and Gilula, N.M. (1996) The gap junction communication channel. Cell, 84, 381-388.
23. 1 cDNA. J. Cell Sci., 108, 3725-3734.
24. Kvist, S., Wiman, K., Claesson, L., Peterson, P.A. and Dobberstein, B. (1982) Membrane insertion and oligomeric assembly of HLA-DR histocompatibility antigens. Cell, 29, 61-69.
25. Li, M., Jan, Y.N. and Jan, L.Y. (1992) Specification of subunit assembly by the hydrophilic amino-terminal domain of the Shaker potassium channel. Science, 257, 1225-1230.
26. Marquardt, T., Hebert, D.N. and Helenius, A. (1993) Post-translational folding of influenza hemagglutinin in isolated endoplasmic reticulum-derived microsomes. J. Biol. Chem., 268, 19618-19625.
27. 3. J. Biol. Chem., 271, 30544-30547.
28. Mignery, G.A., Newton, C.L., Archer, B.T. and Südhof, T.C. (1990) Structure and expression of the rat inositol 1,4,5-triphosphate receptor. J. Biol. Chem., 265, 12679-12685.
29. Musil, L.S. and Goodenough, D.A. (1993) Multisubunit assembly of an integral plasma membrane channel protein, gap junction connexin43, occurs after exit from the ER. Cell, 74, 1065-1077.
30. Nicholson, B., Dermietzel, R., Teplow, D., Traub, O., Willecke, K. and Revel, J.-P. (1987) Two homologous protein components of hepatic gap junctions. Nature, 329, 732-734.
31. Peterson, O.H. and Findlay, I. (1987) Electrophysiology of the pancreas. Physiol. Rev., 67, 1054-1116.
32. Qu, D. and Green, M. (1995) Folding and assembly of a human MHC class II molecule in a cell-free system. DNA Cell Biol., 14, 741-751.
33. Rhee, S.K., Bevans, C.G. and Harris, A.L. (1996) Channel-forming activity of immunoaffinity-purified connexin32 in single phospholipid membranes. Biochemistry, 35, 9212-9223.
34. Risek, B.F. Klier, G. and Gilula, N.B. (1994) Developmental regulation and structural organization of connexins in epidermal gap junctions. Dev. Biol., 164, 183-196.
35. Rosenberg, R.L. and East, J.E. (1992) Cell-free expression of functional Shaker potassium channels. Nature, 360, 166-169.
36. Sawyer, J.T. and Doyle, D. (1990) Assembly of a heterooligomeric asialoglycoprotein receptor complex during cell-free translation. Proc. Natl Acad. Sci. USA, 87, 4854-4858.
37. + channel assembly. Neuron, 11, 67-77.
38. Smith, M.M., Schlesinger, S., Lindstrom, J. and Merlie, J.P. (1986) The effects of inhibiting oligosaccharide trimming by 1-deoxynojirimycin on the nicotinic acetylcholine receptor. J. Biol. Chem., 261, 14825-14832.
39. Sosinsky, G. (1995) Mixing of connexins in gap junction membrane channels. Proc. Natl Acad. Sci. USA, 92, 9210-9214.
40. 2-connexin (connexin-26) can form heteromeric hemichannels. J. Biol. Chem., 270, 6768-6772.
41. Stauffer, K.A., Kumar, N.M., Gilula, N.B. and Unwin, N. (1991) Isolation and purification of gap junction channels. J. Cell Biol., 115, 141-150.
42. Suarez-Isla, B.A., Wan, K., Lindstrom, J. and Montal, M. (1983) Single channel recordings from purified acetylcholine receptors reconstituted in bilayers formed at the tip of patch pipettes. Biochemistry, 22, 2319-2323.
43. 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, 145-156.
44. +)-ATPase of chick sensory neurons. J. Biol. Chem., 261, 1009-1019.
45. Thomas, L., Hartung, K., Langosch, D., Rehm, H., Bamberg, E., Franke, W.W. and Betz, H. (1988) Identification of synaptophysin as a hexameric channel protein of the synaptic vesicle membrane. Science, 242, 1050-1053.
46. Unger, V.M., Kumar, N.M., Gilula, N.B. and Yeager, M. (1997) Projection structure of a gap junction membrane channel at 7 Å resolution. Nature Struct. Biol., 4, 39-43.
47. Unwin, P.N.T. and Zampighi, G. (1980) Structure of the junction between communicating cells. Nature, 283, 545-549.
48. van Koppen, C.J. and Nathanson, N.M. (1990) Site-directed mutagenesis of the m2 muscarinic acetylcholine receptor. Analysis of the role of N-glycosylation in receptor expression and function. J. Biol. Chem., 265, 20887-20892.
49. Walter, P. and Blobel, G. (1983) Preparation of microsomal membranes for cotranslational protein translocation. Methods Enzymol., 96, 84-93.
50. Werner, R., Miller, T., Azarnia, R. and Dahl, G. (1985) Translation and functional expression of cell-cell channel mRNA in Xenopus oocytes. J. Membr. Biol., 87, 253-268.
51. Yeager, M. (1995) Electron microscopic image analysis of cardiac gap junction membrane crystals. Microsc. Res. Technol., 31, 452-466.
52. Yeager, M. and Nicholson, B.J. (1996) Structure of gap junction intercellular channels. Curr. Opin. Struct. Biol., 6, 183-192.
53. Yilla, M., Doyle, D. and Sawyer, J.T. (1992) Early disulfide bond formation prevents heterotypic aggregation of membrane proteins in a cell-free translation system. J. Cell Biol. 188, 245-252.
54. Zhang, J.-T., Chen, M., Foote, C.I. and Nicholson, B.J. (1996) Membrane integration of in vitro-translated gap junctional proteins: co- and post-translational mechanisms. Mol. Biol. Cell, 7, 471-482.