Expression, two-dimensional crystallization, and electron cryo- crystallography of recombinant gap junction membrane channels

Journal of Structural Biology

Volumn 128, Issue 1, 1999, Pages 98-105

  Unger, Vinzenz M ^a   Kumar, Nalin M ^a   Gilula, Norton B ^a   Yeager, Mark ^a,b  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b SCRIPPS CLINIC   (United States)

Author keywords

Connexin43; Electron cryo microscopy; Gap junctions; Image analysis; Integral membrane proteins; Intercellular communication; 1 Connexin

Indexed keywords

GAP JUNCTION PROTEIN; MEMBRANE PROTEIN;

ALPHA HELIX; ARTICLE; CRYOELECTRON MICROSCOPY; CRYSTALLIZATION; CRYSTALLOGRAPHY; GAP JUNCTION; MEMBRANE CHANNEL; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN STRUCTURE;

CRICETINAE; PHOCIDAE;

EID: 0033386437     PISSN: 10478477     EISSN: None     Source Type: Journal    
DOI: 10.1006/jsbi.1999.4184     Document Type: Article

References (71)

1. Beblo D. A., Wang H.-Z., Beyer E. C., Westphale E. M., Veenstra R. D. Unique conductance, gating, and selective permeability properties of gap junction channels formed by connexin40. Circ. Res. 77:1995;813-822.
2. Beyer E. C., Paul D. L., Goodenough D. A. Connexin family of gap junction proteins. J. Membr. Biol. 116:1990;187-194.
3. Brink P. R., Cronin K., Banach K., Peterson E., Westphale E. M., Seul K. H., Ramanan S. V., Beyer E. C. Evidence for heteromeric gap junction channels formed from rat connexin43 and human connexin37. Am. J. Physiol. 273:1997;C1386-C1396.
4. Brissette J. L., Kumar N. M., Gilula N. B., Hall J. E., Dotto G. P. Switch in gap junction protein expression is associated with selective changes in junctional permeability during keratinocyte differentiation. Proc. Natl. Acad. Sci. USA. 91:1994;6453-6457.
5. Bruzzone R., White T. W., Paul D. L. Connections with connexins: The molecular basis of direct intercellular signalling. Eur. J. Biochem. 238:1996;1-27.
6. Calero G., Kanemitsu M., Taffet S. M., Lau A. F., Delmar M. A 17mer peptide interferes with acidification-induced uncoupling of connexin43. Circ. Res. 82:1998;929-935.
7. Cao F., Eckert R., Elfgang C., Nitsche J. M., Snyder S. A., Hülser D. F., Willecke K., Nicholson B. J. A quantitative analysis of connexin-specific permeability differences of gap junctions expressed in HeLa transfectants and Xenopus oocytes. J. Cell Sci. 111:1998;31-43.
8. Cheng A., van Hoek A. N., Yeager M., Verkman A. S., Mitra A. K. Three-dimensional organization of a human water channel. Nature. 387:1997;627-630.
9. Crowther R. A., Henderson R., Smith J. M. MRC image processing programs. J. Struct. Biol. 116:1996;9-16.
10. Dahl G., Miller T., Paul D., Voellmy R., Werner R. Expression of functional cell-cell channels from cloned rat liver gap junction complementary DNA. Science. 236:1987;1290-1293.
11. Eghbali B., Kessler J. A., Spray D. C. Expression of gap junction channels in communication-incompetent cells after stable transfection with cDNA encoding connexin 32. Proc. Natl. Acad. Sci. USA. 87:1990;1328-1331.
12. Elfgang C., Eckert R., Lichtenberg-Fraté H., Butterweck A., Traub O., Klein R. A., Hülser D. F., Willecke K. Specific permeability and selective formation of gap junction channels in connexin-transfected HeLa cells. J. Cell Biol. 129:1995;805-817.
13. Engel A., Hoenger A., Hefti A., Henn C., Ford R. C., Kistler J., Zulauf M. Assembly of 2-D membrane protein crystals: Dynamics, crystal order, and fidelity of structure analysis by electron microscopy. J. Struct. Biol. 109:1992;219-234.
14. Fishman G. I., Moreno A. P., Spray D. C., Leinwand L. A. Functional analysis of human cardiac gap junction channel mutants. Proc. Natl. Acad. Sci. USA. 88:1991;3525-3529.
15. Fishman G. I., Spray D. C., Leinwand L. A. Molecular characterization and functional expression of the human cardiac gap junction channel. J. Cell Biol. 111:1990;589-598.
16. Foote C. I., Zhou L., Zhu X., Nicholson B. J. The pattern of disulfide linkages in the extracellular loop regions of connexin 32 suggests a model for the docking interface of gap junctions. J. Cell Biol. 140:1998;1187-1197.
17. Gogol E., Unwin N. Organization of connexons in isolated rat liver gap junctions. Biophys. J. 54:1988;105-112.
18. Goodenough D. A., Goliger J. A., Paul D. L. Connexins, connexons, and intercellular communication. Annu. Rev. Biochem. 65:1996;475-502.
19. Guan X., Cravatt B. F., Ehring G. R., Hall J. E., Boger D. L., Lerner R. A., Gilula N. B. The sleep-inducing lipid oleamide deconvolutes gap junction communication and calcium wave transmission in glial cells. J. Cell Biol. 139:1997;1785-1792.
20. Havelka W. A., Henderson R., Heymann J. A. W., Oesterhelt D. Projection structure of halorhodopsin from Halobacterium halobium at 6Å resolution obtained by electron cryo-microscopy. J. Mol. Biol. 234:1993;837-846.
21. 12 two-dimensional crystals. J. Mol. Biol. 271:1997;751-758.
22. Henderson R., Baldwin J. M., Downing K. H., Lepault J., Zemlin F. Structure of purple membrane from Halobacterium halobium: Recording, measurement and evaluation of electron micrographs at 3.5Å resolution. Ultramicroscopy. 19:1986;147-178.
23. Henderson R., Baldwin J. M., Ceska T. A., Zemlin F., Beckmann E., Downing K. H. Model for the structure of bacteriorhodopsin based on high-resolution electron cryo-microscopy. J. Mol. Biol. 213:1990;899-929.
24. Homma N., Alvarado J. L., Coombs W., Stergiopoulos K., Taffet S. M., Lau A. F., Delmar M. A particle-receptor model for the insulin-induced closure of connexin43 channels. Circ. Res. 83:1998;27-32.
25. 2O-channel, AQP-CHIP, in projection at 3.5Å resolution. J. Mol. Biol. 251:1995;413-420.
26. Jap B. K., Zulauf M., Scheybani T., Hefti A., Baumeister W., Aebi U., Engel A. 2D crystallization: From art to science. Ultramicroscopy. 46:1992;45-84.
27. Kanter H. L., Saffitz J. E., Beyer E. C. Cardiac myocytes express multiple gap junction proteins. Circ. Res. 70:1992;438-444.
28. Karrasch S., Bullough P. A., Ghosh R. The 8.5Å projection map of the light-harvesting complex I from Rhodospirillum rubrum reveals a ring composed of 16 subunits. EMBO J. 14:1995;631-638.
29. Kühlbrandt W. Two-dimensional crystallization of membrane proteins. Q. Rev. Biophys. 25:1992;1-49.
30. Kühlbrandt W., Downing K. H. Two-dimensional structure of plant light-harvesting complex at 3.7Å resolution by electron crystallography. J. Mol. Biol. 207:1989;823-828.
31. 1 cDNA. J. Cell Sci. 108:1995;3725-3734.
32. Kumar N. M., Gilula N. B. Molecular biology and genetics of gap junction channels. Semin. Cell Biol. 3:1992;3-16.
33. Kumar N. M., Gilula N. B. The gap junction communication channel. Cell. 84:1996;381-388.
34. Lampe P. D., Kistler J., Hefti A., Bond J., Müller S., Johnson R. G., Engel A. In vitro assembly of gap junctions. J. Struct. Biol. 107:1991;281-290.
35. Liu S., Taffet S., Stoner L., Delmar M., Vallano M. L., Jalife J. A structural basis for the unequal sensitivity of the major cardiac and liver gap junctions to intracellular acidification: The carboxyl tail length. Biophys. J. 64:1993;1422-1433.
36. Loewenstein W. R. Junctional intercellular communication: The cell-to-cell membrane channel. Physiol. Rev. 61:1981;829-913.
37. Makowski L., Caspar D. L. D., Phillips W. C., Goodenough D. A. Gap junction structures. II. Analysis of the X-ray diffraction data. J. Cell Biol. 74:1977;629-645.
38. Manjunath C. K., Goings G. E., Page E. Proteolysis of cardiac gap junctions during their isolation from rat hearts. J. Membr. Biol. 85:1985;159-168.
39. Mitra A. K., van Hoek A. N., Wiener M. C., Verkman A. S., Yeager M. The CHIP28 water channel visualized in ice by electron crystallography. Nat. Struct. Biol. 2:1995;726-729.
40. Moreno A. P., Eghbali B., Spray D. C. Connexin32 gap junction channels in stably transfected cells: Unitary conductance. Biophys. J. 60:1991a;1254-1266.
41. Moreno A. P., Eghbali B., Spray D. C. Connexin32 gap junction channels in stably transfected cells. Equilibrium and kinetic properties. Biophys. J. 60:1991b;1267-1277.
42. Morley G. E., Taffet S. M., Delmar M. Intramolecular interactions mediate pH regulation of connexin43 channels. Biophys. J. 70:1996;1294-1302.
43. Nicholson B., Dermietzel R., Teplow D., Traub O., Willecke K., Revel J.-P. Two homologous protein components of hepatic gap junctions. Nature. 329:1987;732-734.
44. Oh S., Ri Y., Bennett M. V. L., Trexler E. B., Verselis V. K., Bargiello T. A. Changes in permeability caused by connexin 32 mutations underlie X-linked Charcot-Marie-Tooth disease. Neuron. 19:1997;927-938.
45. Palmiter R. D., Behringer R. R., Quaife C. J., Maxwell F., Maxwell I. H., Brinster R. L. Cell lineage ablation in transgenic mice by cell-specific expression of a toxic gene. Cell. 50:1987;435-443.
46. Perkins G. A., Goodenough D. A., Sosinsky G. E. Formation of the gap junction intercellular channel requires a 30° rotation for interdigitating two apposing connexons. J. Mol. Biol. 277:1998;171-177.
47. Rubin J. B., Verselis V. K., Bennett M. V. L., Bargiello T. A. A domain substitution procedure and its use to analyze voltage dependence of homotypic gap junctions formed by connexins 26 and 32. Proc. Natl. Acad. Sci. USA. 89:1992;3820-3824.
48. Schertler G. F. X., Villa C., Henderson R. Projection structure of rhodopsin. Nature. 362:1993;770-772.
49. Schertler G. F. X., Hargrave P. A. Projection structure of frog rhodopsin in two crystal forms. Proc. Natl. Acad. Sci. USA. 92:1995;11578-11582.
50. Sikerwar S. S., Unwin N. Three-dimensional structure of gap junctions in fragmented plasma membranes from rat liver. Biophys. J. 54:1988;113-119.
51. Simonsen C. C., Levinson A. D. Isolation and expression of an altered mouse dihydrofolate reductase cDNA. Proc. Natl. Acad. Sci. USA. 80:1983;2495-2499.
52. Stauffer K. A., Kumar N. M., Gilula N. B., Unwin N. Isolation and purification of gap junction channels. J. Cell Biol. 115:1991;141-150.
53. Suchyna T. M., Xu L. X., Gao F., Fourtner C. R., Nicholson B. J. Identification of a proline residue as a transduction element involved in voltage gating of gap junctions. Nature. 365:1993;847-849.
54. Swenson K. I., Jordan J. R., Beyer E. C., Paul D. L. Formation of gap junctions by expression of connexins in Xenopus oocyte pairs. Cell. 57:1989;145-155.
55. Traub O., Eckert R., Lichtenberg-Fraté H., Elfgang C., Bastide B., Scheidtmann K. H., Hülser D. F., Willecke K. Immunochemical and electrophysiological characterization of murine connexin40 and -43 in mouse tissues and transfected human cells. Eur. J. Cell Biol. 64:1994;101-112.
56. Unger V. M., Kumar N. M., Gilula N. B., Yeager M. Projection structure of a gap junction membrane channel at 7Å resolution. Nat. Struct. Biol. 4:1997;39-43.
57. Unger V. M., Kumar N. M., Gilula N. B., Yeager M. Three-dimensional structure of a recombinant gap junction membrane channel. Science. 283:1999;1176-1180.
58. Unwin P. N. T., Ennis P. D. Two configurations of a channel-forming membrane protein. Nature. 307:1984;609-613.
59. Unwin P. N. T., Henderson R. Molecular structure determination by electron microscopy of unstained crystalline specimens. J. Mol. Biol. 94:1975;425-440.
60. Veenstra R. D., Wang H.-Z., Beyer E. C., Brink P. R. Selective dye and ionic permeability of gap junction channels formed by connexin45. Circ. Res. 75:1994;483-490.
61. Veenstra R. D., Wang H.-Z., Beblo D. A., Chilton M. G., Harris A. L., Beyer E. C., Brink P. R. Selectivity of connexin-specific gap junctions does not correlate with channel conductance. Circ. Res. 77:1995;1156-1165.
62. Verselis V. K., Ginter C. S., Bargiello T. A. Opposite voltage gating polarities of two closely related connexins. Nature. 368:1994;348-354.
63. Walz T., Typke D., Smith B. L., Agre P., Engel A. Projection map of aquaporin-1 determined by electron crystallography. Nat. Struct. Biol. 2:1995;730-732.
64. White T. W., Paul D. L., Goodenough D. A., Bruzzone R. Functional analysis of selective interactions among rodent connexins. Mol. Biol. Cell. 6:1995;459-470.
65. Willecke K., Hennemann H., Dahl E., Jungbluth S., Heynkes R. The diversity of connexin genes encoding gap junctional proteins. Eur. J. Cell Biol. 56:1991;1-7.
66. Yeager M. In situ two-dimensional crystallization of a polytopic membrane protein: The cardiac gap junction channel. Acta. Crystallogr. Sect. D. 50:1994;632-638.
67. Yeager M. Structure of cardiac gap junction intercellular channels. J. Struct. Biol. 121:1998;231-245.
68. Yeager M., Gilula N. B. Membrane topology and quaternary structure of cardiac gap junction ion channels. J. Mol. Biol. 223:1992;929-948.
69. Yeager M., Nicholson B. J. Structure of gap junction intercellular channels. Curr. Opin. Struct. Biol. 6:1996;183-192.
70. Yeager M., Unger V. M., Mitra A. K. Three-dimensional structure of membrane proteins determined by two-dimensional crystallization, electron cryomicroscopy, and image analysis. Methods Enzymol. 294:1999;135-180.
71. Zampighi G., Unwin P. N. T. Two forms of isolated gap junctions. J. Mol. Biol. 135:1979;451-464.