Cosegregation of permeability and single-channel conductance in chimeric connexins

Biophysical Journal

Volumn 90, Issue 1, 2006, Pages 151-163

  Ma, Meiyun ^a   Dahl, Gerhard ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CELL SYNCHRONIZATION; CONDUCTANCE; ELECTRIC ACTIVITY; GAP JUNCTION; MEMBRANE POTENTIAL; METABOLITE; PERMEABILITY;

EID: 33646145304     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.105.066381     Document Type: Article

References (45)

1. Barr, L. 1963. Propagation in vertebrate visceral smooth muscle. J. Theor. Biol. 4:73-85.
2. Barr, L., and W. Berger. 1964. The role of current flow in the propagation of cardiac muscle action potentials. Pflugers Arch. 279:192-194.
3. Barr, L., W. Berger, and M. M. Dewey. 1968. Electrical transmission at the nexus between smooth muscle cells. J. Gen. Physiol. 51:347-368.
4. Furshpan, E. J., and D. D. Potter. 1959. Transmission of the giant motor synapses of the crayfish. J. Physiol. 145:289-325.
5. Loewenstein, W. R. 1981. Junctional intercellular communication: the cell-to-cell membrane channel. Physiol. Rev. 61:829-912.
6. Loewenstein, W. R. 1966. Permeability of membrane junctions. Ann. N. Y. Acad. Sci. 137:441-472.
7. Harris, A. L. 2001. Emerging issues of connexin channels: biophysics fills the gap. Q. Rev. Biophys. 34:325-472.
8. Sohl, G., and K. Willecke. 2004. Gap junctions and the connexin protein family. Cardiovasc. Res. 62:228-232.
9. Plum, A., G. Hallas, T. Magin, F. Dombrowski, A. Hagendorff, B. Schumacher, C. Wolpert, J. Kim, W. H. Lamers, M. Evert, P. Meda, O. Traub, et al. 2000. Unique and shared functions of different connexins in mice. Curr. Biol. 10:1083-1091.
10. Panchin, Y., I. Kelmanson, M. Matz, K. Lukyanov, N. Usman, and S. Lukyanov. 2000. A ubiquitous family of putative gap junction molecules. Curr. Biol. 10:R473-R474.
11. Bruzzone, R., S. G. Hormuzdi, M. T. Barbe, A. Herb, and H. Monyer. 2003. Pannexins, a family of gap junction proteins expressed in brain. Proc. Natl. Acad. Sci. USA. 100:13644-13649.
12. Bao, L., S. Locovei, and G. Dahl. 2004. Pannexin membrane channels are mechanosensitive conduits for ATP. FEBS Lett. 572:65-68.
13. Goldberg, G. S., V. Valiunas, and P. R. Brink. 2004. Selective permeability of gap junction channels. Biochim. Biophys. Acta. 1662:96-101.
14. Moreno, A. P. 2004. Biophysical properties of homomeric and heteromultimeric channels formed by cardiac connexins. Cardiovasc. Res. 62:276-286.
15. Valiunas, V. 2002. Biophysical properties of connexin-45 gap junction hemichannels studied in vertebrate cells. J. Gen. Physiol. 119:147-164.
16. Srinivas, M., R. Rozental, T. Kojima, R. Dermietzel, M. Mehler, D. F. Condorelli, J. A. Kessler, and D. C. Spray. 1999. Functional properties of channels formed by the neuronal gap junction protein connexin36. J. Neurosci. 19:9848-9855.
17. Veenstra, R. D., H. Z. Wang, E. C. Beyer, S. V. Ramanan, and P. R. Brink. 1994. Connexin37 forms high conductance gap junction channels with subconductance state activity and selective dye and ionic permeabilities. Biophys. J. 66:1915-1928.
18. Goldberg, G. S., P. D. Lampe, and B. J. Nicholson. 1999. Selective transfer of endogenous metabolites through gap junctions composed of different connexins. Nat. Cell Biol. 1:457-459.
19. Veenstra, R. D., H. Z. Wang, D. A. Beblo, M. G. Chilton, A. L. Harris, E. C. Beyer, and P. R. Brink. 1995. Selectivity of connexin-specific gap junctions does not correlate with channel conductance. Circ. Res. 77:1156-1165.
20. Elfgang, C., R. Eckert, H. Lichtenberg-Frate, A. Butterweck, O. Traub, R. A. Klein, D. F. Hulser, and K. Willecke. 1995. Specific permeability and selective formation of gap junction channels in connexin-transfected HeLa cells. J. Cell Biol. 129:805-817.
21. Gong, X. Q., and B. J. Nicholson. 2001. Size selectivity between gap junction channels composed of different connexins. Cell Commun. Adhes. 8:187-192.
22. Oh, S., J. B. Rubin, M. V. Bennett, V. K. Verselis, and T. A. Bargiello. 1999. Molecular determinants of electrical rectification of single channel conductance in gap junctions formed by connexins 26 and 32. J. Gen. Physiol. 114:339-364.
23. Trexler, E. B., F. F. Bukauskas, J. Kronengold, T. A. Bargiello, and V. K. Verselis. 2000. The first extracellular loop domain is a major determinant of charge selectivity in connexin46 channels. Biophys. J. 79:3036-3051.
24. Nicholson, B. J., P. A. Weber, F. Cao, H. Chang, P. Lampe, and G. Goldberg. 2000. The molecular basis of selective permeability of connexins is complex and includes both size and charge. Braz. J. Med. Biol. Res. 33:369-378.
25. Krasilnikov, O. V., R. Z. Sabirov, V. I. Ternovsky, P. G. Merzliak, and J. N. Muratkhodjaev. 1992. A simple method for the determination of the pore radius of ion channels in planar lipid bilayer membranes. FEMS Microbiol. Immunol. 5:93-100.
26. Bezrukov, S. M., and I. Vodyanoy. 1993. Probing alamethicin channels with water-soluble polymers. Effect on conductance of channel states. Biophys. J. 64:16-25.
27. Bezrukov, S. M., I. Vodyanoy, and V. A. Parsegian. 1994. Counting polymers moving through a single ion channel. Nature. 370:279-281.
28. Bezrukov, S. M., L. Kullman, and M. Winterhalter. 2000. Probing sugar translocation through maltoporin at the single channel level. FEBS Lett. 476:224-228.
29. Bezrukov, S. M. 2000. Ion channels as molecular coulter counters to probe metabolite transport. J. Membr. Biol. 174:1-13.
30. Merzlyak, P. G., L. N. Yuldasheva, C. G. Rodrigues, C. M. Carneiro, O. V. Krasilnikov, and S. M. Bezrukov. 1999. Polymeric nonelectrolytes to probe pore geometry: application to the alpha-toxin transmembrane channel. Biophys. J. 77:3023-3033.
31. Kullman, L., M. Winterhalter, and S. M. Bezrukov. 2002. Transport of maltodextrins through maltoporin: a single-channel study. Biophys. J. 82:803-812.
32. Oh, S., Y. Ri, M. V. Bennett, E. B. Trexler, V. K. Verselis, and T. A. Bargiello. 1997. Changes in permeability caused by connexin 32 mutations underlie X-linked Charcot-Marie-Tooth disease. Neuron. 19:927-938.
33. Qu, Y., and G. Dahl. 2004. Accessibility of Cx46 hemichannels for uncharged molecules and its modulation by voltage. Biophys. J. 86:1502-1509.
34. Locke, D., I. V. Koreen, J. Y. Liu, and A. L. Harris. 2004. Reversible pore block of connexin channels by cyclodextrins. J. Biol. Chem. 279:22883-22892.
35. Sabirov, R. Z., O. V. Krasilnikov, V. I. Ternovsky, and P. G. Merzliak. 1993. Relation between ionic channel conductance and conductivity of media containing different nonelectrolytes. A novel method of pore size determination. Gen. Physiol. Biophys. 12:95-111.
36. Krasilnikov, O. V., J. B. Da Cruz, L. N. Yuldasheva, W. A. Varanda, and R. A. Nogueira. 1998. A novel approach to study the geometry of the water lumen of ion channels: colicin Ia channels in planar lipid bilayers. J. Membr. Biol. 161:83-92.
37. Zhou, X. W., A. Pfahnl, R. Werner, A. Hudder, A. Llanes, A. Luebke, and G. Dahl. 1997. Identification of a pore lining segment in gap junction hemichannels. Biophys. J. 72:1946-1953.
38. Deleted in proof.
39. Nitsche, J. M., H. C. Chang, P. A. Weber, and B. J. Nicholson. 2004. A transient diffusion model yields unitary gap junctional permeabilities from images of cell-to-cell fluorescent dye transfer between Xenopus oocytes. Biophys. J. 86:2058-2077.
40. Weber, P. A., H. C. Chang, K. E. Spaeth, J. M. Nitsche, and B. J. Nicholson. 2004. The permeability of gap junction channels to probes of different size is dependent on connexin composition and permeant-pore affinities. Biophys. J. 87:958-973.
41. Skerrett, I. M., J. Aronowitz, J. H. Shin, G. Cymes, E. Kasperek, F. L. Cao, and B. J. Nicholson. 2002. Identification of amino acid residues lining the pore of a gap junction channel. J. Cell Biol. 159:349-360.
42. Fleishman, S. J., V. M. Unger, M. Yeager, and N. Ben-Tal. 2004. A Calpha model for the transmembrane alpha helices of gap junction intercellular channels. Mol. Cell. 15:879-888.
43. Kronengold, J., E. B. Trexler, F. F. Bukauskas, T. A. Bargiello, and V. K. Verselis. 2003. Single-channel SCAM identifies pore-lining residues in the first extracellular loop and first transmembrane domains of Cx46 hemichannels. J. Gen. Physiol. 122:389-405.
44. Pfahnl, A., and G. Dahl. 1998. Localization of a voltage gate in connexin46 gap junction hemichannels. Biophys. J. 75:2323-2331.
45. Brelidze, T. I., X. Niu, and K. L. Magleby. 2003. A ring of eight conserved negatively charged amino acids doubles the conductance of BK channels and prevents inward rectification. Proc. Natl. Acad. Sci. USA. 100:9017-9022.