Selective defects in channel permeability associated with Cx32 mutations causing X-linked Charcot-Marie-Tooth disease

Neurobiology of Disease

Volumn 21, Issue 3, 2006, Pages 607-617

  Bicego, Massimiliano ^a   Morassutto, Sabina ^a   Hernandez, Victor H ^b   Morgutti, Marcello ^c   Mammano, Fabio ^b   D'Andrea, Paola ^a   Bruzzone, Roberto ^d  

^a UNIVERSITY OF TRIESTE   (Italy)

^b VENETIAN INSTITUTE OF MOLECULAR MEDICINE   (Italy)

^c INSTITUTE FOR MATERNAL AND CHILD HEALTH IRCCS BURLO GAROFOLO   (Italy)

^d INSTITUT PASTEUR   (France)

Author keywords

Connexin; Dye coupling; Gap junction; Genetic disease; Human; PNS

Indexed keywords

CONNEXIN 32; FLUORESCENT DYE; GAP JUNCTION PROTEIN; ION CHANNEL; TRACER;

ARTICLE; CHANNEL GATING; COMPARATIVE STUDY; CONTROLLED STUDY; FLUORESCENCE ANALYSIS; GENE MUTATION; GENETIC LINKAGE; HEREDITARY MOTOR SENSORY NEUROPATHY; HUMAN; HUMAN CELL; MOLECULAR PROBE; MOLECULAR WEIGHT; PATHOPHYSIOLOGY; PRIORITY JOURNAL; SURFACE CHARGE; WILD TYPE; X CHROMOSOME LINKED DISORDER;

BLOTTING, WESTERN; CHARCOT-MARIE-TOOTH DISEASE; CONNEXINS; GENETIC DISEASES, X-LINKED; HELA CELLS; HUMANS; ION CHANNELS; MICROSCOPY, FLUORESCENCE; MUTATION; PATCH-CLAMP TECHNIQUES; PERMEABILITY; TRANSFECTION;

EID: 33244478285     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2005.09.005     Document Type: Article

References (75)

1. C.K. Abrams, S. Oh, Y. Ri, and T.A. Bargiello Mutations in connexin 32: the molecular and biophysical bases for the X-linked form of Charcot-Marie-Tooth disease Brain Res. Brain Res. Rev. 32 2000 203 214
2. C.K. Abrams, M.M. Freidin, V.K. Verselis, M.V. Bennett, and T.A. Bargiello Functional alterations in gap junction channels formed by mutant forms of connexin 32: evidence for loss of function as a pathogenic mechanism in the X-linked form of Charcot-Marie-Tooth disease Brain Res. 900 2001 9 25
3. C.K. Abrams, M.V. Bennett, V.K. Verselis, and T.A. Bargiello Voltage opens unopposed gap junction hemichannels formed by a connexin 32 mutant associated with X-linked Charcot-Marie-Tooth disease Proc. Natl. Acad. Sci. U. S. A. 99 2002 3980 3984
4. B.M. Altevogt, K.A. Kleopa, F.R. Postma, S.S. Scherer, and D.L. Paul Connexin29 is uniquely distributed within myelinating glial cells of the central and peripheral nervous systems J. Neurosci. 22 2002 6458 6470
5. P. Anzini, D.H. Neuberg, M. Schachner, E. Nelles, K. Willecke, J. Zielasek, K.V. Toyka, U. Suter, and R. Martini Structural abnormalities and deficient maintenance of peripheral nerve myelin in mice lacking the gap junction protein connexin 32 J. Neurosci. 17 1997 4545 4551
6. R.J. Balice-Gordon, L.J. Bone, and S.S. Scherer Functional gap junctions in the Schwann cell myelin sheath J. Cell Biol. 142 1998 1095 1104
7. D.A. Beblo, and R.D. Veenstra Monovalent cation permeation through the connexin40 gap junction channel. Cs, Rb, K, Na, Li, TEA, TMA, TBA, and effects of anions Br, Cl, F, acetate, aspartate, glutamate, and NO3 J. Gen. Physiol. 109 1997 509 522
8. M. Beltramello, M. Bicego, V. Piazza, C.D. Ciubotaru, F. Mammano, and P. D'Andrea Permeability and gating properties of human connexins 26 and 30 expressed in HeLa cells Biochem. Biophys. Res. Commun. 305 2003 1024 1033
9. M. Beltramello, V. Piazza, F.F. Bukauskas, T. Pozzan, and F. Mammano Impaired permeability to Ins(1,4,5)P3 in a mutant connexin underlies recessive hereditary deafness Nat. Cell Biol. 7 2005 63 69
10. J. Bergoffen, S.S. Scherer, S. Wang, M.O. Scott, L.J. Bone, D.L. Paul, K. Chen, M.W. Lensch, P.F. Chance, and K.H. Fischbeck Connexin mutations in X-linked Charcot-Marie-Tooth disease Science 262 1993 2039 2042
11. C.G. Bevans, M. Kordel, S.K. Rhee, and A.L. Harris Isoform composition of connexin channels determines selectivity among second messengers and uncharged molecules J. Biol. Chem. 273 1998 2808 2816
12. L.J. Bone, S.M. Deschenes, R.J. Balice-Gordon, K.H. Fischbeck, and S.S. Scherer Connexin32 and X-linked Charcot-Marie-Tooth disease Neurobiol. Dis. 4 1997 221 230
13. J.L. Brissette, N.M. Kumar, N.B. Gilula, J.E. Hall, and G.P. Dotto Switch in gap junction protein expression is associated with selective changes in junctional permeability during keratinocyte differentiation Proc. Natl. Acad. Sci. U. S. A. 91 1994 6453 6457
14. R. Bruzzone, T.W. White, S.S. Scherer, K.H. Fischbeck, and D.L. Paul Null mutations of connexin32 in patients with X-linked Charcot-Marie-Tooth disease Neuron 13 1994 1253 1260
15. R. Bruzzone, T.W. White, and D.L. Paul Connections with connexins: the molecular basis of direct intercellular signaling Eur. J. Biochem. 238 1996 1 27
16. R. Bruzzone, V. Veronesi, D. Gomes, M. Bicego, N. Duval, S. Marlin, C. Petit, P. D'Andrea, and T.W. White Loss-of-function and residual channel activity of connexin26 mutations associated with non-syndromic deafness FEBS Lett. 533 2003 79 88
17. F. Cao, R. Eckert, C. Elfgang, J.M. Nitsche, S.A. Snyder, H.u. DF, K. Willecke, and B.J. Nicholson 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
18. C. Castro, J.M. Gomez-Hernandez, K. Silander, and L.C. Barrio Altered formation of hemichannels and gap junction channels caused by C-terminal connexin-32 mutations J. Neurosci. 19 1999 3752 3760
19. K.J. Chandross Nerve injury and inflammatory cytokines modulate gap junctions in the peripheral nervous system Glia 24 1998 21 31
20. K.J. Chandross, J.A. Kessler, R.I. Cohen, E. Simburger, D.C. Spray, P. Bieri, and R. Dermietzel Altered connexin expression after peripheral nerve injury Mol. Cell. Neurosci. 7 1996 501 518
21. M. Chanson, K.J. Chandross, M.B. Rook, J.A. Kessler, and D.C. Spray Gating characteristics of a steeply voltage-dependent gap junction channel in rat Schwann cells J. Gen. Physiol. 102 1993 925 946
22. P. D'Andrea, V. Veronesi, M. Bicego, S. Melchionda, L. Zelante, E. Di Iorio, R. Bruzzone, and P. Gasparini Hearing loss: frequency and functional studies of the most common connexin26 alleles Biochem. Biophys. Res. Commun. 296 2002 685 691
23. S.M. Deschenes, J.L. Walcott, T.L. Wexler, S.S. Scherer, and K.H. Fischbeck Altered trafficking of mutant connexin32 J. Neurosci. 17 1997 9077 9084
24. M. Dezawa, T. Mutoh, A. Dezawa, and E. Adachi-Usami Putative gap junctional communication between axon and regenerating Schwann cells during mammalian peripheral nerve regeneration Neuroscience 85 1998 663 667
25. C. Elfgang, R. Eckert, H. Lichtenberg-Frate, A. Butterweck, O. Traub, R.A. Klein, D.F. Hulser, and K. Willecke Specific permeability and selective formation of gap junction channels in connexin-transfected HeLa cells J. Cell Biol. 129 1995 805 817
26. J. Garcia de la Torre, S. Navarro, M.C. Lopez Martinez, F.G. Diaz, and J.J. Lopez Cascales HYDRO: a computer program for the prediction of hydrodynamic properties of macromolecules Biophys. J. 67 1994 530 531
27. D.A. Gerido, and T.W. White Connexin disorders of the ear, skin, and lens Biochim. Biophys. Acta 1662 2004 159 170
28. G.S. Goldberg, P.D. Lampe, and B.J. Nicholson Selective transfer of endogenous metabolites through gap junctions composed of different connexins Nat. Cell Biol. 1 1999 457 459
29. G.S. Goldberg, A.P. Moreno, and P.D. Lampe Gap junctions between cells expressing connexin 43 or 32 show inverse permselectivity to adenosine and ATP J. Biol. Chem. 277 2002 36725 36730
30. X.Q. Gong, and B.J. Nicholson Size selectivity between gap junction channels composed of different connexins Cell Commun. Adhes. 8 2001 187 192
31. A.L. Harris Emerging issues of connexin channels: biophysics fills the gap Q. Rev. Biophys. 34 2001 325 472
32. P.M. Kelley, D.J. Harris, B.C. Comer, J.W. Askew, T. Fowler, S.D. Smith, and W.J. Kimberling Novel mutations in the connexin 26 gene (GJB2) that cause autosomal recessive (DFNB1) hearing loss Am. J. Hum. Genet. 62 1998 792 799
33. D.P. Kelsell, J. Dunlop, and M.B. Hodgins Human diseases: clues to cracking the connexin code? Trends Cell Biol. 11 2001 2 6
34. M.A. Kenna, B.L. Wu, D.A. Cotanche, B.R. Korf, and H.L. Rehm Connexin 26 studies in patients with sensorineural hearing loss Arch. Otolaryngol., Head Neck Surg. 127 2001 1037 1042
35. W.R. Loewenstein Junctional intercellular communication: the cell-to-cell membrane channel Physiol. Rev. 61 1981 829 913
36. F.J. Martinez-Wittinghan, C. Sellitto, L. Li, X. Gong, P.R. Brink, R.T. Mathias, and T.W. White Dominant cataracts result from incongruous mixing of wild-type lens connexins J. Cell Biol. 161 2003 969 978
37. P. Meda Assaying the molecular permeability of connexin channels Methods Mol. Biol. 154 2001 201 224
38. C. Meier, R. Dermietzel, K.G. Davidson, T. Yasumura, and J.E. Rash Connexin32-containing gap junctions in Schwann cells at the internodal zone of partial myelin compaction and in Schmidt-Lanterman incisures J. Neurosci. 24 2004 3186 3198
39. M. Mesnil, V. Krutovskikh, C. Piccoli, C. Elfgang, O. Traub, K. Willecke, and H. Yamasaki Negative growth control of HeLa cells by connexin genes: connexin species specificity Cancer Res. 55 1995 629 639
40. G. Munhoz Essenfelder, R. Bruzzone, J. Lamartine, A. Charollais, C. Blanchet-Bardon, M.T. Barbe, P. Meda, and G. Waksman Connexin30 mutations responsible for hidrotic ectodermal dysplasia cause abnormal hemichannel activity Hum. Mol. Genet. 13 2004 1703 1714
41. B.J. Nicholson, P.A. Weber, F. Cao, H. Chang, P. Lampe, and G. Goldberg The molecular basis of selective permeability of connexins is complex and includes both size and charge Braz. J. Med. Biol. Res. 33 2000 369 378
42. H. Niessen, H. Harz, P. Bedner, K. Kramer, and K. Willecke Selective permeability of different connexin channels to the second messenger inositol 1,4,5-trisphosphate J. Cell Sci. 113 2000 1365 1372
43. S. Oh, Y. Ri, M.V. Bennett, E.B. Trexler, V.K. Verselis, and T.A. Bargiello Changes in permeability caused by connexin 32 mutations underlie X-linked Charcot-Marie-Tooth disease Neuron 19 1997 927 938
44. Y. Omori, M. Mesnil, and H. Yamasaki Connexin 32 mutations from X-linked Charcot-Marie-Tooth disease patients: functional defects and dominant negative effects Mol. Biol. Cell 7 1996 907 916
45. D.L. Paul New functions for gap junctions Curr. Opin. Cell Biol. 7 1995 665 672
46. W.A. Paznekas, S.A. Boyadjiev, R.E. Shapiro, O. Daniels, B. Wollnik, C.E. Keegan, J.W. Innis, M.B. Dinulos, C. Christian, M.C. Hannibal, and E.W. Jabs Connexin 43 (GJA1) mutations cause the pleiotropic phenotype of oculodentodigital dysplasia Am. J. Hum. Genet. 72 2003 408 418
47. C. Peracchia Chemical gating of gap junction channels; roles of calcium, pH and calmodulin Biochim. Biophys. Acta 1662 2004 61 80
48. C. Petit, J. Levilliers, and J.P. Hardelin Molecular genetics of hearing loss Annu. Rev. Genet. 35 2001 589 646
49. A. Plum, G. Hallas, T. Magin, F. Dombrowski, A. Hagendorff, B. Schumacher, C. Wolpert, J. Kim, W.H. Lamers, M. Evert, P. Meda, O. Traub, and K. Willecke Unique and shared functions of different connexins in mice Curr. Biol. 10 2000 1083 1091
50. C. Rabadan-Diehl, G. Dahl, and R. Werner A connexin-32 mutation associated with Charcot-Marie-Tooth disease does not affect channel formation in oocytes FEBS Lett. 351 1994 90 94
51. C. Ressot, and R. Bruzzone Connexin channels in Schwann cells and the development of the X-linked form of Charcot-Marie-Tooth disease Brain Res. Brain Res. Rev. 32 2000 192 202
52. C. Ressot, D. Gomes, A. Dautigny, D. Pham-Dinh, and R. Bruzzone Connexin32 mutations associated with X-linked Charcot-Marie-Tooth disease show two distinct behaviors: loss of function and altered gating properties J. Neurosci. 18 1998 4063 4075
53. G. Richard Human connexin disorders of the skin Cell Commun. Adhes. 8 2001 401 407
54. M. Romanello, and P. D'Andrea Dual mechanism of intercellular communication in HOBIT osteoblastic cells: a role for gap-junctional hemichannels J. Bone Miner. Res. 16 2001 1465 1476
55. J.C. Saez, J.A. Connor, D.C. Spray, and M.V. Bennett Hepatocyte gap junctions are permeable to the second messenger, inositol 1,4,5-trisphosphate, and to calcium ions Proc. Natl. Acad. Sci. U. S. A. 86 1989 2708 2712
56. J.C. Saez, V.M. Berthoud, M.C. Branes, A.D. Martinez, and E.C. Beyer Plasma membrane channels formed by connexins: their regulation and functions Physiol. Rev. 83 2003 1359 1400
57. C. Sandri, J.M. Van Buren, and K. Akert Membrane morphology of the vertebrate nervous system. A study with freeze-etch technique Prog. Brain Res. 46 1977 1 384
58. S.S. Scherer, S.M. Deschenes, Y.T. Xu, J.B. Grinspan, K.H. Fischbeck, and D.L. Paul Connexin32 is a myelin-related protein in the PNS and CNS J. Neurosci. 15 1995 8281 8294
59. S.S. Scherer, Y.T. Xu, E. Nelles, K. Fischbeck, K. Willecke, and L.J. Bone Connexin32-null mice develop demyelinating peripheral neuropathy Glia 24 1998 8 20
60. S.S. Scherer, Y.T. Xu, A. Messing, K. Willecke, K.H. Fischbeck, and L.J. Jeng Transgenic expression of human connexin32 in myelinating Schwann cells prevents demyelination in connexin32-null mice J. Neurosci. 25 2005 1550 1559
61. T.H. Steinberg, R. Civitelli, S.T. Geist, A.J. Robertson, E. Hick, R.D. Veenstra, H.Z. Wang, P.M. Warlow, E.M. Westphale, J.G. Laing, and E.C. Beyer Connexin43 and connexin45 form gap junctions with different molecular permeabilities in osteoblastic cells EMBO J. 13 1994 744 750
62. T.M. Suchyna, J.M. Nitsche, M. Chilton, A.L. Harris, R.D. Veenstra, and B.J. Nicholson Different ionic selectivities for connexins 26 and 32 produce rectifying gap junction channels Biophys. J. 77 1999 2968 2987
63. U. Suter, and S.S. Scherer Disease mechanisms in inherited neuropathies Nat. Rev., Neurosci. 4 2003 714 726
64. W. Tetzlaff Tight junction contact events and temporary gap junctions in the sciatic nerve fibres of the chicken during Wallerian degeneration and subsequent regeneration J. Neurocytol. 11 1982 839 858
65. V. Valiunas, E.C. Beyer, and P.R. Brink Cardiac gap junction channels show quantitative differences in selectivity Circ. Res. 91 2002 104 111
66. D.I. Vaney Many diverse types of retinal neurons show tracer coupling when injected with biocytin or neurobiotin Neurosci. Lett. 125 1991 187 190
67. J.K. VanSlyke, S.M. Deschenes, and L.S. Musil Intracellular transport, assembly, and degradation of wild-type and disease-linked mutant gap junction proteins Mol. Biol. Cell 11 2000 1933 1946
68. R.D. Veenstra Size and selectivity of gap junction channels formed from different connexins J. Bioenerg. Biomembr. 28 1996 327 337
69. H.Z. Wang, and R.D. Veenstra Monovalent ion selectivity sequences of the rat connexin43 gap junction channel J. Gen. Physiol. 109 1997 491 507
70. H.L. Wang, W.T. Chang, T.H. Yeh, T. Wu, M.S. Chen, and C.Y. Wu Functional analysis of connexin-32 mutants associated with X-linked dominant Charcot-Marie-Tooth disease Neurobiol. Dis. 15 2004 361 370
71. P.A. Weber, H.C. Chang, K.E. Spaeth, J.M. Nitsche, and B.J. Nicholson The permeability of gap junction channels to probes of different size is dependent on connexin composition and permeant-pore affinities Biophys. J. 87 2004 958 973
72. T.W. White Unique and redundant connexin contributions to lens development Science 295 2002 319 320
73. T.W. White, and R. Bruzzone Gap junctions: fates worse than death? Curr. Biol. 10 2000 R685 R688
74. T.W. White, and D.L. Paul Genetic diseases and gene knockouts reveal diverse connexin functions Annu. Rev. Physiol. 61 1999 283 310
75. S.W. Yum, K.A. Kleopa, S. Shumas, and S.S. Scherer Diverse trafficking abnormalities of connexin32 mutants causing CMTX Neurobiol. Dis. 11 2002 43 52