Mechanism for modulation of gating of connexin26-containing channels by taurine

Journal of General Physiology

Volumn 138, Issue 3, 2011, Pages 321-339

  Locke, Darren ^a   Kieken, Fabien ^b   Tao, Liang ^c   Sorgen, Paul L ^b   Harris, Andrew L ^a  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^c SUN YAT SEN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

4 (2 HYDROXYETHYL) 1 PIPERAZINEETHANESULFONIC ACID; CONNEXIN 26; CONNEXIN 32; GAP JUNCTION PROTEIN; TAURINE;

ARTICLE; CELL JUNCTION; CHEMISTRY; CYTOPLASM; HELA CELL; HUMAN; METABOLISM; PH; PROTEIN MULTIMERIZATION;

CONNEXINS; CYTOPLASM; GAP JUNCTIONS; HELA CELLS; HEPES; HUMANS; HYDROGEN-ION CONCENTRATION; INTERCELLULAR JUNCTIONS; PROTEIN MULTIMERIZATION; TAURINE;

EID: 80054013332     PISSN: 00221295     EISSN: 15407748     Source Type: Journal    
DOI: 10.1085/jgp.201110634     Document Type: Article

References (79)

1. Allen, M.J., J. Gemel, E.C. Beyer, and R. Lal. 2011. Atomic force microscopy of connexin40 gap junction hemichannels reveals calcium-dependent three-dimensional molecular topography and open-closed conformations of both the extracellular and cytoplasmic faces. J. Biol. Chem. 286:22139-22146. doi:10.1074/jbc.M111.240002
2. Antoniadi, T., K. Grønskov, A. Sand, A. Pampanos, K. Brøndum-Nielsen, and M.B. Petersen. 2000. Mutation analysis of the GJB2 (connexin 26) gene by DGGE in Greek patients with sensorineural deafness. Hum. Mutat. 16:7-12. doi:10.1002/1098-1004(200007) 16:1<7::AID-HUMU2>3.0.CO;2-A
3. Ayad, W.A., D. Locke, I.V. Koreen, and A.L. Harris. 2006. Heteromeric, but not homomeric, connexin channels are selectively permeable to inositol phosphates. J. Biol. Chem. 281:16727-16739. doi:10.1074/jbc.M600136200
4. Bao, X., G.A. Altenberg, and L. Reuss. 2004. Mechanism of regulation of the gap junction protein connexin 43 by protein kinase Cmediated phosphorylation. Am. J. Physiol. Cell Physiol. 286:C647-C654. doi:10.1152/ajpcell.00295.2003
5. Beahm, D.L., and J.E. Hall. 2002. Hemichannel and junctional properties of connexin 50. Biophys. J. 82:2016-2031. doi:10.1016/S0006-3495(02)75550-1
6. Bevans, C.G., and A.L. Harris. 1999. Regulation of connexin channels by pH. Direct action of the protonated form of taurine and other aminosulfonates. J. Biol. Chem. 274:3711-3719. doi:10.1074/jbc.274.6.3711
7. Bevans, C.G., M. Kordel, S.K. Rhee, and A.L. Harris. 1998. Isoform composition of connexin channels determines selectivity among second messengers and uncharged molecules. J. Biol. Chem. 273:2808-2816. doi:10.1074/jbc.273.5.2808
8. Bukauskas, F.F., and V.K. Verselis. 2004. Gap junction channel gating. Biochim. Biophys. Acta. 1662:42-60. doi:10.1016/j.bbamem.2004.01.008
9. Chesler, M., and R.P. Kraig. 1989. Intracellular pH transients of mammalian astrocytes. J. Neurosci. 9:2011-2019.
10. Contreras, J.E., J.C. Sáez, F.F. Bukauskas, and M.V.L. Bennett. 2003. Gating and regulation of connexin 43 (Cx43) hemichannels. Proc. Natl. Acad. Sci. USA. 100:11388-11393. doi:10.1073/pnas.1434298100
11. D'Andrea, P., V. Veronesi, M. Bicego, S. Melchionda, L. Zelante, E. Di Iorio, R. Bruzzone, and P. Gasparini. 2002. Hearing loss: frequency and functional studies of the most common connexin26 alleles. Biochem. Biophys. Res. Commun. 296:685-691. doi:10.1016/S0006-291X(02)00891-4
12. Foos, T.M., and J.Y. Wu. 2002. The role of taurine in the central nervous system and the modulation of intracellular calcium homeostasis. Neurochem. Res. 27:21-26. doi:10.1023/A:1014890219513
13. Fort, A.G., and D.C. Spray. 2009. Trifluoroethanol reveals helical propensity at analogous positions in cytoplasmic domains of three connexins. Biopolymers. 92:173-182. doi:10.1002/bip.21166
14. Goldberg, G.S., J.F. Bechberger, and C.C.G. Naus. 1995. A preloading method of evaluating gap junctional communication by fluorescent dye transfer. Biotechniques. 18:490-497.
15. González-Nilo, F.D., H. Krautwurst, A. Yévenes, E. Cardemil, and R. Cachau. 2002. Saccharomyces cerevisiae phosphoenolpyruvate carboxykinase: theoretical and experimental study of the effect of glutamic acid 284 on the protonation state of lysine 213. Biochim. Biophys. Acta. 1599:65-71.
16. Good, N.E., G.D. Winget, W. Winter, T.N. Connolly, S. Izawa, and R.M. Singh. 1966. Hydrogen ion buffers for biological research. Biochemistry. 5:467-477. doi:10.1021/bi00866a011
17. Goodenough, D.A., and D.L. Paul. 2003. Beyond the gap: functions of unpaired connexon channels. Nat. Rev. Mol. Cell Biol. 4:285-294. doi:10.1038/nrm1072
18. Green, G.E., D.A. Scott, J.M. McDonald, G.G. Woodworth, V.C. Sheffield, and R.J.H. Smith. 1999. Carrier rates in the midwestern United States for GJB2 mutations causing inherited deafness. JAMA. 281:2211-2216. doi:10.1001/jama.281.23.2211
19. Halgren, T.A. 1996. Merck molecular force field. I. Basis, form, scope, parameterization, and performance of MMFF94. J. Comput. Chem. 17:490-519. doi:10.1002/(SICI)1096-987X(199604)17:5/6<490::AID-JCC1>3.0.CO;2-P
20. Han, X., A.B. Patters, D.P. Jones, I. Zelikovic, and R.W. Chesney. 2006. The taurine transporter: mechanisms of regulation. Acta Physiol. (Oxf.). 187:61-73. doi:10.1111/j.1748-1716.2006.01573.x
21. Hand, G.M., D.J. Müller, B.J. Nicholson, A. Engel, and G.E. Sosinsky. 2002. Isolation and characterization of gap junctions from tissue culture cells. J. Mol. Biol. 315:587-600. doi:10.1006/jmbi.2001.5262
22. Harris, A.L. 2001. Emerging issues of connexin channels: biophysics fills the gap. Q. Rev. Biophys. 34:325-472.
23. Harris, A.L. 2007. Connexin channel permeability to cytoplasmic molecules. Prog. Biophys. Mol. Biol. 94:120-143. doi:10.1016/j.pbiomolbio.2007.03.011
24. Harris, A.L., A. Walter, D.L. Paul, D.A. Goodenough, and J. Zimmerberg. 1992. Ion channels in single bilayers induced by rat connexin32. Brain Res. Mol. Brain Res. 15:269-280. doi:10.1016/0169-328X(92)90118-U
25. Harris, T.K., and G.J. Turner. 2002. Structural basis of perturbed pKa values of catalytic groups in enzyme active sites. IUBMB Life. 53:85-98. doi:10.1080/15216540211468
26. + channel. J. Gen. Physiol. 111:741-749.
27. Hehre, W. 1973. A Guide to Molecular Mechanics and Quantum Chemical Calculations. Wavefunction, Inc., Irvine, CA. 812 pp.
28. Hervé, J.C., and D. Sarrouilhe. 2005. Connexin-made channels as pharmacological targets. Curr. Pharm. Des. 11:1941-1958. doi:10.2174/1381612054021060
29. Hirst-Jensen, B.J., P. Sahoo, F. Kieken, M. Delmar, and P.L. Sorgen. 2007. Characterization of the pH-dependent interaction between the gap junction protein connexin43 carboxyl terminus and cytoplasmic loop domains. J. Biol. Chem. 282:5801-5813. doi:10.1074/jbc.M605233200
30. Homma, N., J.L. Alvarado, W. Coombs, K. Stergiopoulos, S.M. Taffet, A.F. Lau, and M. Delmar. 1998. A particle-receptor model for the insulin-induced closure of connexin43 channels. Circ. Res. 83:27-32.
31. Huxtable, R.J. 1992. Physiological actions of taurine. Physiol. Rev. 72:101-163.
32. Kelley, P.M., D.J. Harris, B.C. Comer, J.W. Askew, T. Fowler, S.D. Smith, and W.J. Kimberling. 1998. Novel mutations in the connexin 26 gene (GJB2) that cause autosomal recessive (DFNB1) hearing loss. Am. J. Hum. Genet. 62:792-799. doi:10.1086/301807
33. Kim, D.Y., Y. Kam, S.K. Koo, and C.O. Joe. 1999. Gating connexin 43 channels reconstituted in lipid vesicles by mitogen-activated protein kinase phosphorylation. J. Biol. Chem. 274:5581-5587. doi:10.1074/jbc.274.9.5581
34. Koreen, I.V., W.A. Elsayed, Y.J. Liu, and A.L. Harris. 2004. Tetracyclineregulated expression enables purification and functional analysis of recombinant connexin channels from mammalian cells. Biochem. J. 383:111-119. doi:10.1042/BJ20040806
35. Lambert, I.H. 2004. Regulation of the cellular content of the organic osmolyte taurine in mammalian cells. Neurochem. Res. 29:27-63. doi:10.1023/B:NERE.0000010433.08577.96
36. Lambert, I.H., E.K. Hoffmann, and S.F. Pedersen. 2008. Cell volume regulation: physiology and pathophysiology. Acta Physiol. (Oxf.). 194:255-282. doi:10.1111/j.1748-1716.2008.01910.x
37. Lampe, P.D., J. Kistler, A. Hefti, J. Bond, S. Müller, R.G. Johnson, and A. Engel. 1991. In vitro assembly of gap junctions. J. Struct. Biol. 107:281-290. doi:10.1016/1047-8477(91)90053-Y
38. Lee, J.R., and T.W. White. 2009. Connexin-26 mutations in deafness and skin disease. Expert Rev. Mol. Med. 11:e35. doi:10.1017/S1462399409001276
39. Li, H.Y., T.F. Liu, A. Lazrak, C. Peracchia, G.S. Goldberg, P.D. Lampe, and R.G. Johnson. 1996. Properties and regulation of gap junctional hemichannels in the plasma membranes of cultured cells. J. Cell Biol. 134:1019-1030. doi:10.1083/jcb.134.4.1019
40. Liu, F., F.T. Arce, S. Ramachandran, and R. Lal. 2006. Nanomechanics of hemichannel conformations: connexin flexibility underlying channel opening and closing. J. Biol. Chem. 281:23207-23217. doi:10.1074/jbc.M605048200
41. Locke, D., I.V. Koreen, J.Y. Liu, and A.L. Harris. 2004a. Reversible pore block of connexin channels by cyclodextrins. J. Biol. Chem. 279:22883-22892. doi:10.1074/jbc.M401980200
42. Locke, D., T. Stein, C. Davies, J. Morris, A.L. Harris, W.H. Evans, P. Monaghan, and B. Gusterson. 2004b. Altered permeability and modulatory character of connexin channels during mammary gland development. Exp. Cell Res. 298:643-660. doi:10.1016/j.yexcr.2004.05.003
43. Locke, D., J. Liu, and A.L. Harris. 2005. Lipid rafts prepared by different methods contain different connexin channels, but gap junctions are not lipid rafts. Biochemistry. 44:13027-13042. doi:10.1021/bi050495a
44. Locke, D., S. Bian, H. Li, and A.L. Harris. 2009. Post-translational modifications of connexin26 revealed by mass spectrometry. Biochem. J. 424:385-398. doi:10.1042/BJ20091140
45. Lurtz, M.M., and C.F. Louis. 2007. Intracellular calcium regulation of connexin43. Am. J. Physiol. Cell Physiol. 293:C1806-C1813. doi:10.1152/ajpcell.00630.2006
46. Maeda, S., S. Nakagawa, M. Suga, E. Yamashita, A. Oshima, Y. Fujiyoshi, and T. Tsukihara. 2009. Structure of the connexin 26 gap junction channel at 3.5 A resolution. Nature. 458:597-602. doi:10.1038/nature07869
47. Mani, R.S., A. Ganapathy, R. Jalvi, C.R. Srikumari Srisailapathy, V. Malhotra, S. Chadha, A. Agarwal, A. Ramesh, R.R. Rangasayee, and A. Anand. 2009. Functional consequences of novel connexin 26 mutations associated with hereditary hearing loss. Eur. J. Hum.Genet. 17:502-509. doi:10.1038/ejhg.2008.179
48. Mese, G., E. Londin, R. Mui, P.R. Brink, and T.W. White. 2004. Altered gating properties of functional Cx26 mutants associated with recessive non-syndromic hearing loss. Hum. Genet. 115:191-199. doi:10.1007/s00439-004-1142-6
49. Mukouyama, E.B., M. Oguchi, Y. Kodera, T. Maeda, and H. Suzuki. 2004. Low pKa lysine residues at the active site of sarcosine oxidase from Corynebacterium sp. U-96. Biochem. Biophys. Res.Commun. 320:846-851. doi:10.1016/j.bbrc.2004.05.219
50. Müller, D.J., G.M. Hand, A. Engel, and G.E. Sosinsky. 2002. Conformational changes in surface structures of isolated connexin 26 gap junctions. EMBO J. 21:3598-3607. doi:10.1093/emboj/cdf365
51. Nicholson, B.J. 2003. Gap junctions-from cell to molecule. J. Cell Sci. 116:4479-4481. doi:10.1242/jcs.00821
52. Palmada, M., K. Schmalisch, C. Böhmer, N. Schug, M. Pfister, F. Lang, and N. Blin. 2006. Loss of function mutations of the GJB2 gene detected in patients with DFNB1-associated hearing impairment. Neurobiol. Dis. 22:112-118. doi:10.1016/j.nbd.2005.10.005
53. Pan, C., G.S. Giraldo, H. Prentice, and J.Y. Wu. 2010. Taurine protection of PC12 cells against endoplasmic reticulum stress induced by oxidative stress. J. Biomed. Sci. 17:S17. doi:10.1186/1423-0127-17-S1-S17
54. Petegnief, V., P.L. Lleu, R.C. Gupta, J.J. Bourguignon, and G. Rebel. 1995. Taurine analog modulation of taurine uptake by two different mechanisms in cultured glial cells. Biochem. Pharmacol. 49:399-410. doi:10.1016/0006-2952(94)00390-8
55. Prasad, S., R.A. Cucci, G.E. Green, and R.J.H. Smith. 2000. Genetic testing for hereditary hearing loss: connexin 26 (GJB2) allele variants and two novel deafness-causing mutations (R32C and 645-648delTAGA). Hum. Mutat. 16:502-508. doi:10.1002/1098-1004(200012)16:6<502::AID-HUMU7>3.0.CO;2-4
56. Quist, A.P., S.K. Rhee, H. Lin, and R. Lal. 2000. Physiological role of gap-junctional hemichannels. Extracellular calcium-dependent isosmotic volume regulation. J. Cell Biol. 148:1063-1074. doi:10.1083/jcb.148.5.1063
57. Ramamoorthy, S., F.H. Leibach, V.B. Mahesh, H. Han, T. Yang-Feng, R.D. Blakely, and V. Ganapathy. 1994. Functional characterization and chromosomal localization of a cloned taurine transporter from human placenta. Biochem. J. 300:893-900.
58. Rhee, S.K., C.G. Bevans, and A.L. Harris. 1996. Channel-forming activity of immunoaffinity-purified connexin32 in single phospholipid membranes. Biochemistry. 35:9212-9223. doi:10.1021/bi960295m
59. Sáez, J.C., M.A. Retamal, D. Basilio, F.F. Bukauskas, and M.V. Bennett. 2005. Connexin-based gap junction hemichannels: gating mechanisms. Biochim. Biophys. Acta. 1711:215-224. doi:10.1016/j.bbamem.2005.01.014
60. Schaffer, S.W., J. Azuma, and M. Mozaffari. 2009. Role of antioxidant activity of taurine in diabetes. Can. J. Physiol. Pharmacol. 87:91-99.doi:10.1139/Y08-110
61. Schalper, K.A., J.A. Orellana, V.M. Berthoud, and J.C. Sáez. 2009. Dysfunctions of the diffusional membrane pathways mediated by hemichannels in inherited and acquired human diseases. Curr.Vasc. Pharmacol. 7:486-505. doi:10.2174/157016109789043937
62. Schulte, U., H. Hahn, M. Konrad, N. Jeck, C. Derst, K. Wild, S. Weidemann, J.P. Ruppersberg, B. Fakler, and J. Ludwig. 1999. pH gating of ROMK (K(ir)1.1) channels: control by an Arg-Lys-Arg triad disrupted in antenatal Bartter syndrome. Proc. Natl. Acad.Sci. USA. 96:15298-15303. doi:10.1073/pnas.96.26.15298
63. Seifert, R., E. Eismann, J. Ludwig, A. Baumann, and U.B. Kaupp. 1999. Molecular determinants of a Ca2+-binding site in the pore of cyclic nucleotide-gated channels: S5/S6 segments control affinity of intrapore glutamates. EMBO J. 18:119-130. doi:10.1093/emboj/18.1.119
64. Solan, J.L., and P.D. Lampe. 2009. Connexin43 phosphorylation: structural changes and biological effects. Biochem. J. 419:261-272. doi:10.1042/BJ20082319
65. Sorgen, P.L., H.S. Duffy, P. Sahoo, W. Coombs, M. Delmar, and D.C. Spray. 2004. Structural changes in the carboxyl terminus of the gap junction protein connexin43 indicates signaling between binding domains for c-Src and zonula occludens-1. J. Biol. Chem. 279:54695-54701. doi:10.1074/jbc.M409552200
66. Sosinsky, G.E., and B.J. Nicholson. 2005. Structural organization of gap junction channels. Biochim. Biophys. Acta. 1711:99-125.
67. Spray, D.C., Z.C. Ye, and B.R. Ransom. 2006. Functional connexin "hemichannels": a critical appraisal. Glia. 54:758-773. doi:10.1002/glia.20429
68. Srinivas, M., J. Kronengold, F.F. Bukauskas, T.A. Bargiello, and V.K. Verselis. 2005. Correlative studies of gating in Cx46 and Cx50 hemichannels and gap junction channels. Biophys. J. 88:1725-1739. doi:10.1529/biophysj.104.054023
69. Srinivas, M., D.P. Calderon, J. Kronengold, and V.K. Verselis. 2006. Regulation of connexin hemichannels by monovalent cations.J. Gen. Physiol. 127:67-75. doi:10.1085/jgp.200509397
70. Stergiopoulos, K., J.L. Alvarado, M. Mastroianni, J.F. Ek-Vitorin, S.M. Taffet, and M. Delmar. 1999. Hetero-domain interactions as a mechanism for the regulation of connexin channels. Circ. Res.84:1144-1155.
71. Tao, L., and A.L. Harris. 2004. Biochemical requirements for inhibition of connexin26-containing channels by natural and synthetic taurine analogs. J. Biol. Chem. 279:38544-38554. doi:10.1074/jbc.M405654200
72. Tao, L., and A.L. Harris. 2007. 2-aminoethoxydiphenyl borate directly inhibits channels composed of connexin26 and/orconnexin32. Mol. Pharmacol. 71:570-579. doi:10.1124/mol.106.027508
73. Tappaz, M.L. 2004. Taurine biosynthetic enzymes and taurine transporter:molecular identification and regulations. Neurochem. Res. 29:83-96. doi:10.1023/B:NERE.0000010436.44223.f8
74. 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. doi:10.1529/biophysj.103.036350
75. Willecke, K., J. Eiberger, J. Degen, D. Eckardt, A. Romualdi, M. Güldenagel, U. Deutsch, and G. Söhl. 2002. Structural and functional diversity of connexin genes in the mouse and human genome. Biol. Chem. 383:725-737. doi:10.1515/BC.2002.076
76. Wu, H., Y. Jin, J. Wei, H. Jin, D. Sha, and J.Y. Wu. 2005. Mode of action of taurine as a neuroprotector. Brain Res. 1038:123-131. doi:10.1016/j.brainres.2005.01.058
77. Yu, J., C.A. Bippes, G.M. Hand, D.J. Müller, and G.E. Sosinsky. 2007. Aminosulfonate modulated pH-induced conformational changes in connexin26 hemichannels. J. Biol. Chem. 282:8895-8904. doi:10.1074/jbc.M609317200
78. Zhang, J.T., and B.J. Nicholson. 1989. Sequence and tissue distribution of a second protein of hepatic gap junctions, Cx26, as deduced from its cDNA. J. Cell Biol. 109:3391-3401. doi:10.1083/jcb.109.6.3391
79. Zoidl, G., and R. Dermietzel. 2010. Gap junctions in inherited human disease. Pflugers Arch. 460:451-466. doi:10.1007/s00424-010-0789-1