Large pore ion and metabolite-permeable channel regulation of postnatal ventricular zone neural stem and progenitor cells: Interplay between aquaporins, connexins, and pannexins?

Stem Cells International

Volumn , Issue , 2012, Pages

  Wicki Stordeur, Leigh E ^a   Swayne, Leigh Anne ^a,b  

^a UNIVERSITY OF VICTORIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AQUAPORIN; AQUAPORIN 4; CONNEXIN 43; GAP JUNCTION PROTEIN; ION CHANNEL; NUCLEOTIDE; PANNEXIN 1; UNCLASSIFIED DRUG;

CELL PROLIFERATION; CYTOSKELETON; HUMAN; MEMBRANE TRANSPORT; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL PROGENITOR CELL; NEURAL STEM CELL; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; TELENCEPHALON; VENTRICULAR ZONE;

EID: 84863639126     PISSN: None     EISSN: 16879678     Source Type: Journal    
DOI: 10.1155/2012/454180     Document Type: Review

References (129)

1. Ming G. L., Song H., Adult neurogenesis in the mammalian brain: significant answers and significant questions Neuron 2011 70 4 687 702
2. Swayne L. A., Wicki-Stordeur L., Ion channels in postnatal neurogenesis: potential targets for brain repair Channels 2012 6 2
3. Yasuda T., Adams D. J., Physiological roles of ion channels in adult neural stem cells and their progeny Journal of Neurochemistry 2010 114 4 946 959
4. Ishibashi K., Hara S., Kondo S., Aquaporin water channels in mammals Clinical and Experimental Nephrology 2009 13 2 107 117
5. Rojek A., Praetorius J., Frkiaer J., Nielsen S., Fenton R. A., A current view of the mammalian aquaglyceroporins Annual Review of Physiology 2008 70 301 327 (Pubitemid 351738182)
6. Preston G. M., Agre P., Isolation of the cDNA for erythrocyte integral membrane protein of 28 kilodaltons: member of an ancient channel family Proceedings of the National Academy of Sciences of the United States of America 1991 88 24 11110 11114 (Pubitemid 21915989)
7. Preston G. M., Jung J. S., Guggino W. B., Agre P., Membrane topology of aquaporin CHIP. Analysis of functional epitope- scanning mutants by vectorial proteolysis The Journal of Biological Chemistry 1994 269 3 1668 1673
8. Gonen T., Walz T., The structure of aquaporins Quarterly Reviews of Biophysics 2006 39 4 361 396 (Pubitemid 44950380)
9. Smith B. L., Agre P., Erythrocyte M(r) 28,000 transmembrane protein exists as a multisubunit oligomer similar to channel proteins The Journal of Biological Chemistry 1991 266 10 6407 6415 (Pubitemid 21906233)
10. Jung J. S., Preston G. M., Smith B. L., Guggino W. B., Agre P., Molecular structure of the water channel through aquaporin CHIP. The hourglass model The Journal of Biological Chemistry 1994 269 20 14648 14654
11. Hasegawa H., Ma T., Skach W., Matthay M. A., Verkman A. S., Molecular cloning of a mercurial-insensitive water channel expressed in selected water-transporting tissues The Journal of Biological Chemistry 1994 269 8 5497 5500 (Pubitemid 24242908)
12. Nielsen S., Smith B. L., Christensen E. I., Agre P., Distribution of the aquaporin CHIP in secretory and resorptive epithelia and capillary endothelia Proceedings of the National Academy of Sciences of the United States of America 1993 90 15 7275 7279 (Pubitemid 23222432)
13. Mylonakou M. N., Petersen P. H., Rinvik E., Rojek A., Vladimarsdottir E., Zelenin S., Zeuthen T., Nielsen S., Ottersen O. P., Amiry-Moghaddam M., Analysis of mice with targeted deletion of AQP9 gene provides conclusive evidence for expression of AQP9 in neurons Journal of Neuroscience Research 2009 87 6 1310 1322
14. Jung J. S., Bhat R. V., Preston G. M., Guggino W. B., Baraban J. M., Agre P., Molecular characterization of an aquaporin cDNA from brain: candidate osmoreceptor and regulator of water balance Proceedings of the National Academy of Sciences of the United States of America 1994 91 26 13052 13056
15. Venero J. L., Vizuete M. L., Machado A., Cano J., Aquaporins in the central nervous system Progress in Neurobiology 2001 63 3 321 336
16. Tait M. J., Saadoun S., Bell B. A., Papadopoulos M. C., Water movements in the brain: role of aquaporins Trends in Neurosciences 2008 31 1 37 43
17. Cavazzin C., Ferrari D., Facchetti F., Russignan A., Vescovi A. L., La Porta C. A. M., Gritti A., Unique expression and localization of aquaporin-4 and aquaporin-9 in murine and human neural stem cells and in their glial progeny Glia 2006 53 2 167 181
18. La Porta C. A. M., Gena P., Gritti A., Fascio U., Svelto M., Calamita G., Adult murine CNS stem cells express aquaporin channels Biology of the Cell 2006 98 2 89 94 (Pubitemid 43230618)
19. Kong H., Fan Y., Xie J., Ding J., Sha L., Shi X., Sun X., Hu G., AQP4 knockout impairs proliferation, migration and neuronal differentiation of adult neural stem cells Journal of Cell Science 2008 121 24 4029 4036
20. Kong H., Sha L. L., Fan Y., Xiao M., Ding J. H., Wu J., Hu G., Requirement of AQP4 for antidepressive efficiency of fluoxetine: implication in adult hippocampal neurogenesis Neuropsychopharmacology 2009 34 5 1263 1276
21. Xie L. L., Sun X. L., Fan Y., Kong H., Ding J. H., Hu G., Aquaporin 4 knockout resists negative regulation of neural cell proliferation by cocaine in mouse hippocampus International Journal of Neuropsychopharmacology 2009 12 6 843 850
22. D'Ascenzo M., Piacentini R., Casalbore P., Budoni M., Pallini R., Azzena G. B., Grassi C., Role of L-type Ca 2+ channels in neural stem/progenitor cell differentiation European Journal of Neuroscience 2006 23 4 935 944 (Pubitemid 43344688)
23. Deisseroth K., Singla S., Toda H., Monje M., Palmer T. D., Malenka R. C., Excitation-neurogenesis coupling in adult neural stem/progenitor cells Neuron 2004 42 4 535 552 (Pubitemid 38639875)
24. Mishra S. K., Braun N., Shukla V., Fllgrabe M., Schomerus C., Korf H. W., Gachet C., Ikehara Y., Svigny J., Robson S. C., Zimmermann H., Extracelluar nucleotide signaling in adult neural stem cells: synergism with growth factor-mediated cellular proliferation Development 2006 133 4 675 684
25. Lin J. H. C., Takano T., Arcuino G., Wang X., Hu F., Darzynkiewicz Z., Nunes M., Goldman S. A., Nedergaard M., Purinergic signaling regulates neural progenitor cell expansion and neurogenesis Developmental Biology 2007 302 1 356 366 (Pubitemid 46096933)
26. Scemes E., Duval N., Meda P., Reduced expression of P2Y1 receptors in connexin43-null mice alters calcium signaling and migration of neural progenitor cells Journal of Neuroscience 2003 23 36 11444 11452 (Pubitemid 37549701)
27. Wicki-Stordeur L. E., Dzugalo A. D., Swansburg R. M., Suits J. M., Swayne L. A., Pannexin 1 regulates postnatal neural stem and progenitor cell proliferation Neural Development 2012 7 1, article 11
28. Goodenough D. A., The structure and permeability of isolated hepatocyte gap junctions Cold Spring Harbor Symposia on Quantitative Biology 1976 40 37 43 (Pubitemid 8020565)
29. Goldberg G. S., Moreno A. P., Lampe P. D., Gap junctions between cells expressing connexin 43 or 32 show inverse permselectivity to adenosine and ATP The Journal of Biological Chemistry 2002 277 39 36725 36730
30. Saez J. C., Connor J. A., Spray D. C., Bennett M. V. L., Hepatocyte gap junctions are permeable to the second messenger, inositol 1,4,5-trisphosphate, and to calcium ions Proceedings of the National Academy of Sciences of the United States of America 1989 86 8 2708 2712 (Pubitemid 19112612)
31. Alexander D. B., Goldberg G. S., Transfer of biologically important molecules between cells through gap junction channels Current Medicinal Chemistry 2003 10 19 2045 2058 (Pubitemid 37139061)
32. Dbouk H. A., Mroue R. M., El-Sabban M. E., Talhouk R. S., Connexins: a myriad of functions extending beyond assembly of gap junction channels Cell Communication and Signaling 2009 7, article 4
33. Spray D. C., Ye Z. C., Ransom B. R., Functional connexin hemichannels: a critical appraisal Glia 2006 54 7 758 773 (Pubitemid 44629638)
34. Jiang J. X., Gu S., Gap junction- and hemichannel-independent actions of connexins Biochimica et Biophysica Acta 2005 1711 2 208 214 (Pubitemid 40799295)
35. Giepmans B. N. G., Gap junctions and connexin-interacting proteins Cardiovascular Research 2004 62 2 233 245 (Pubitemid 38496537)
36. Kardami E., Dang X., Iacobas D. A., Nickel B. E., Jeyaraman M., Srisakuldee W., Makazan J., Tanguy S., Spray D. C., The role of connexins in controlling cell growth and gene expression Progress in Biophysics and Molecular Biology 2007 94 1-2 245 264 (Pubitemid 46782981)
37. Olk S., Turchinovich A., Grzendowski M., Sthler K., Meyer H. E., Zoidl G., Dermietzel R., Proteomic analysis of astroglial connexin43 silencing uncovers a cytoskeletal platform involved in process formation and migration Glia 2010 58 4 494 505
38. Iacobas D. A., Iacobas S., Urban-Maldonado M., Spray D. C., Sensitivity of the brain transcriptome to connexin ablation Biochimica et Biophysica Acta 2005 1711 2 183 196 (Pubitemid 40799293)
39. Stains J. P., Lecanda F., Screen J., Towler D. A., Civitelli R., Gap junctional communication modulates gene transcription by altering the recruitment of Sp1 and Sp3 to connexin-response elements in osteoblast promoters The Journal of Biological Chemistry 2003 278 27 24377 24387 (Pubitemid 37548589)
40. Stains J. P., Civitelli R., Gap junctions regulate extracellular signal-regulated kinase signaling to affect gene transcription Molecular Biology of the Cell 2005 16 1 64 72 (Pubitemid 40024291)
41. Shl G., Willecke K., An update on connexin genes and their nomenclature in mouse and man Cell Communication and Adhesion 2003 10 46 173 180 (Pubitemid 38081368)
42. Beyer E. C., Paul D. L., Goodenough D. A., Connexin43: a protein from rat heart homologous to a gap junction protein from liver Journal of Cell Biology 1987 105 6 2621 2629 (Pubitemid 18017692)
43. Leung D. S. Y., Unsicker K., Reuss B., Expression and developmental regulation of gap junction connexins cx26, cx32, cx43 and cx45 in the rat midbrain-floor International Journal of Developmental Neuroscience 2002 20 1 63 75 (Pubitemid 34465462)
44. Dermietzel R., Traub O., Hwang T. K., Beyer E., Bennett M. V. L., Spray D. C., Willecke K., Differential expression of three gap junction proteins in developing and mature brain tissues Proceedings of the National Academy of Sciences of the United States of America 1989 86 24 10148 10152 (Pubitemid 20030796)
45. Belliveau D. J., Naus C. C. G., Cellular localization of gap junction mRNAs in developing rat brain Developmental Neuroscience 1995 17 2 81 96
46. Rozental R., Morales M., Mehler M. F., Urban M., Kremer M., Dermietzel R., Kessler J. A., Spray D. C., Changes in the properties of gap junctions during neuronal differentiation of hippocampal progenitor cells Journal of Neuroscience 1998 18 5 1753 1762 (Pubitemid 28103083)
47. Duval N., Goms D., Calaora V., Calabrese A., Meda P., Bruzzone R., Cell coupling and Cx43 expression in embryonic mouse neural progenitor cells Journal of Cell Science 2002 115 16 3241 3251 (Pubitemid 34960177)
48. Bittman K. S., LoTurco J. J., Differential regulation of connexin 26 and 43 in murine neocortical precursors Cerebral Cortex 1999 9 2 188 195 (Pubitemid 29174200)
49. Nadarajah B., Jones A. M., Evans W. H., Parnavelas J. G., Differential expression of connexins during neocortical development and neuronal circuit formation Journal of Neuroscience 1997 17 9 3096 3111 (Pubitemid 27175822)
50. Cheng A., Tang H., Cai J., Zhu M., Zhang X., Rao M., Mattson M. P., Gap junctional communication is required to maintain mouse cortical neural progenitor cells in a proliferative state Developmental Biology 2004 272 1 203 216 (Pubitemid 38887295)
51. Santiago M. F., Alcami P., Striedinger K. M., Spray D. C., Scemes E., The carboxyl-terminal domain of Connexin43 is a negative modulator of neuronal differentiation The Journal of Biological Chemistry 2010 285 16 11836 11845
52. Elias L. A. B., Wang D. D., Kriegstein A. R., Gap junction adhesion is necessary for radial migration in the neocortex Nature 2007 448 7156 901 907 (Pubitemid 47312775)
53. Scemes E., Duval N., Meda P., Reduced Expression of P2Y1 Receptors in Connexin43-Null Mice Alters Calcium Signaling and Migration of Neural Progenitor Cells Journal of Neuroscience 2003 23 36 11444 11452 (Pubitemid 37549701)
54. Marins M., Xavier A. L. R., Viana N. B., Fortes F. S. A., Fres M. M., Menezes J. R. L., Gap junctions are involved in cell migration in the early postnatal subventricular zone Developmental Neurobiology 2009 69 11 715 730
55. Boyer L. A., Lee T. I., Cole M. F., Johnstone S. E., Levine S. S., Zucker J. P., Guenther M. G., Kumar R. M., Murray H. L., Jenner R. G., Gifford D. K., Melton D. A., Jaenisch R., Young R. A., Core transcriptional regulatory circuitry in human embryonic stem cells Cell 2005 122 6 947 956 (Pubitemid 41345211)
56. Parekkadan B., Berdichevsky Y., Irimia D., Leeder A., Yarmush G., Toner M., Levine J. B., Yarmush M. L., Cell-cell interaction modulates neuroectodermal specification of embryonic stem cells Neuroscience Letters 2008 438 2 190 195
57. Todorova M. G., Soria B., Quesada I., Gap junctional intercellular communication is required to maintain embryonic stem cells in a non-differentiated and proliferative state Journal of Cellular Physiology 2008 214 2 354 362 (Pubitemid 350308991)
58. Rash J. E., Yasumura T., Davidson K. G. V., Furman C. S., Dudek F. E., Nagy J. I., Identification of cells expressing Cx43, Cx30, Cx26, Cx32 and Cx36 in gap junctions of rat brain and spinal cord Cell Communication and Adhesion 2001 8 46 315 320
59. Theis M., Shl G., Speidel D., Khn R., Willecke K., Connexin43 is not expressed in principal cells of mouse cortex and hippocampus European Journal of Neuroscience 2003 18 2 267 274 (Pubitemid 36999931)
60. Micevych P. E., Abelson L., Distribution of mRNAs coding for liver and heart gap junction proteins in the rat central nervous system Journal of Comparative Neurology 1991 305 1 96 118
61. Nadarajah B., Thomaidou D., Evans W. H., Parnavelas J. G., Gap junctions in the adult cerebral cortex: regional differences in their distribution and cellular expression of connexins The Journal of Comparative Neurology 1996 376 2 326 342 (Pubitemid 26404603)
62. Lacar B., Young S. Z., Platel J. C., Bordey A., Gap junction-mediated calcium waves define communication networks among murine postnatal neural progenitor cells European Journal of Neuroscience 2011 34 12 1895 1905
63. Liu X., Bolteus A. J., Balkin D. M., Henschel O., Bordey A., GFAP-expressing cells in the postnatal subventricular zone display a unique glial phenotype intermediate between radial glia and astrocytes Glia 2006 54 5 394 410 (Pubitemid 44422941)
64. Mirzadeh Z., Merkle F. T., Soriano-Navarro M., Garcia-Verdugo J. M., Alvarez-Buylla A., Neural stem cells confer unique pinwheel architecture to the ventricular surface in neurogenic regions of the adult brain Cell Stem Cell 2008 3 3 265 278
65. Freitas A. S., Xavier A. L., Furtado C. M., Dye coupling and connexin expression by cortical radial glia in the early postnatal subventricular zone. Developmental Neurobiology. In press
66. Miragall F., Albiez P., Bartels H., De Vries U., Dermietzel R., Expression of the gap junction protein connexin43 in the subependymal layer and the rostral migratory stream of the mouse: evidence for an inverse correlation between intensity of connexin43 expression and cell proliferation activity Cell and Tissue Research 1997 287 2 243 253 (Pubitemid 27064884)
67. Liu X., Wang Q., Haydar T. F., Bordey A., Nonsynaptic GABA signaling in postnatal subventricular zone controls proliferation of GFAP-expressing progenitors Nature Neuroscience 2005 8 9 1179 1187 (Pubitemid 43348136)
68. Stout C. E., Costantin J. L., Naus C. C. G., Charles A. C., Intercellular calcium signaling in astrocytes via ATP release through connexin hemichannels The Journal of Biological Chemistry 2002 277 12 10482 10488 (Pubitemid 34968170)
69. Braet K., Aspeslagh S., Vandamme W., Willecke K., Martin P. E. M., Evans W. H., Leybaert L., Pharmacological sensitivity of ATP release triggered by photoliberation of inositol-1,4,5-trisphosphate and zero extracellular calcium in brain endothelial cells Journal of Cellular Physiology 2003 197 2 205 213 (Pubitemid 37485249)
70. Dale N., Dynamic ATP signalling and neural development Journal of Physiology 2008 586 10 2429 2436 (Pubitemid 351689802)
71. Weissman T. A., Riquelme P. A., Ivic L., Flint A. C., Kriegstein A. R., Calcium waves propagate through radial glial cells and modulate proliferation in the developing neocortex Neuron 2004 43 5 647 661 (Pubitemid 39179725)
72. Owens D. F., Kriegstein A. R., Patterns of intracellular calcium fluctuation in precursor cells of the neocortical ventricular zone Journal of Neuroscience 1998 18 14 5374 5388 (Pubitemid 28311954)
73. De Bock M., Wang N., Bol M., Connexin-43 hemichannels contribute to cytoplasmic Ca 2+ oscillations by providing a bimodal Ca 2+ -dependent Ca 2+ -entry pathway The Journal of Biological Chemistry 2012 287 15 12250 12266
74. De Vuyst E., Wang N., Decrock E., De Bock M., Vinken M., Van Moorhem M., Lai C., Culot M., Rogiers V., Cecchelli R., Naus C. C., Evans W. H., Leybaert L., Ca 2+ regulation of connexin 43 hemichannels in C6 glioma and glial cells Cell Calcium 2009 46 3 176 187
75. Reaume A. G., De Sousa P. A., Kulkarni S., Langille B. L., Zhu D., Davies T. C., Juneja S. C., Kidder G. M., Rossant J., Cardiac malformation in neonatal mice lacking connexin43 Science 1995 267 5205 1831 1834
76. Moorby C., Patel M., Dual functions for connexins: Cx43 regulates growth independently of gap junction formation Experimental Cell Research 2001 271 2 238 248 (Pubitemid 33141205)
77. Quist A. P., Rhee S. K., Lin H., Lal R., Physiological role of gap-junctional hemichannels: extracellular calcium-dependent isosmotic volume regulation Journal of Cell Biology 2000 148 5 1063 1074
78. Belliveau D. J., Bani-Yaghoub M., McGirr B., Naus C. C. G., Rushlow W. J., Enhanced neurite outgrowth in PC12 cells mediated by connexin hemichannels and ATP The Journal of Biological Chemistry 2006 281 30 20920 20931 (Pubitemid 44115433)
79. Bani-Yaghoub M., Underhill T. M., Naus C. C. G., Gap junction blockage interferes with neuronal and astroglial differentiation of mouse p19 embryonal carcinoma cells Developmental Genetics 1999 24 1-2 69 81 (Pubitemid 29115550)
80. Kunze A., Congreso M. R., Hartmann C., Wallraff-Beck A., Httmann K., Bedner P., Requardt R., Seifert G., Redecker C., Willecke K., Hofmann A., Pfeifer A., Theis M., Steinhuser C., Connexin expression by radial glia-like cells is required for neurogenesis in the adult dentate gyrus Proceedings of the National Academy of Sciences of the United States of America 2009 106 27 11336 11341
81. Panchina Y., Kelmanson I., Matz M., Lukyanov K., Usman N., Lukyanov S., A ubiquitous family of putative gap junction molecules Current Biology 2000 10 13 R473 R474
82. Sosinsky G. E., Boassa D., Dermietzel R., Duffy H. S., Laird D. W., MacVicar B. A., Naus C. C., Penuela S., Scemes E., Spray D. C., Thompson R. J., Zhao H. B., Dahl G., Pannexin channels are not gap junction hemichannels Channels 2011 5 3 193 197
83. MacVicar B. A., Thompson R. J., Non-junction functions of pannexin-1 channels Trends in Neurosciences 2010 33 2 93 102
84. Penuela S., Gehi R., Laird D. W., The biochemistry and function of pannexin channels. Biochimica et Biophysica Acta. In press
85. Ambrosi C., Gassmann O., Pranskevich J. N., Boassa D., Smock A., Wang J., Dahl G., Steinem C., Sosinsky G. E., Pannexin1 and pannexin2 channels show quaternary similarities to connexons and different oligomerization numbers from each other The Journal of Biological Chemistry 2010 285 32 24420 24431
86. Bruzzone R., Hormuzdi S. G., Barbe M. T., Herb A., Monyer H., Pannexins, a family of gap junction proteins expressed in brain Proceedings of the National Academy of Sciences of the United States of America 2003 100 23 13644 13649 (Pubitemid 37444793)
87. Ma W., Hui H., Pelegrin P., Surprenant A., Pharmacological characterization of pannexin-1 currents expressed in mammalian cells Journal of Pharmacology and Experimental Therapeutics 2009 328 2 409 418
88. Santiago M. F., Veliskova J., Patel N. K., Targeting pannexin1 improves seizure outcome PLoS ONE 2011 6 9, article e25178
89. Silverman W. R., de Rivero Vaccari J. P., Locovei S., Qiu F., Carlsson S. K., Scemes E., Keane R. W., Dahl G., The pannexin 1 channel activates the inflammasome in neurons and astrocytes The Journal of Biological Chemistry 2009 284 27 18143 18151
90. Bao L., Locovei S., Dahl G., Pannexin membrane channels are mechanosensitive conduits for ATP FEBS Letters 2004 572 13 65 68 (Pubitemid 39092514)
91. Thompson R. J., Jackson M. F., Olah M. E., Rungta R. L., Hines D. J., Beazely M. A., MacDonald J. F., MacVicar B. A., Activation of pannexin-1 hemichannels augments aberrant bursting in the hippocampus Science 2008 322 5907 1555 1559
92. Locovei S., Wang J., Dahl G., Activation of pannexin 1 channels by ATP through P2Y receptors and by cytoplasmic calcium FEBS Letters 2006 580 1 239 244 (Pubitemid 43005343)
93. Thompson R. J., Zhou N., MacVicar B. A., Ischemia opens neuronal gap junction hemichannels Science 2006 312 5775 924 927 (Pubitemid 43727327)
94. Bargiotas P., Krenz A., Hormuzdi S. G., Pannexins in ischemia-induced neurodegeneration Proceedings of the National Academy of Sciences of the United States of America 2011 108 51 20772 20777
95. Chekeni F. B., Elliott M. R., Sandilos J. K., Walk S. F., Kinchen J. M., Lazarowski E. R., Armstrong A. J., Penuela S., Laird D. W., Salvesen G. S., Isakson B. E., Bayliss D. A., Ravichandran K. S., Pannexin 1 channels mediate find-me signal release and membrane permeability during apoptosis Nature 2010 467 7317 863 867
96. Sandilos J. K., Chiu Y. H., Chekeni F. B., Pannexin 1, an ATP release channel, is activated by caspase cleavage of its pore-associated C terminal autoinhibitory region. The Journal of Biological Chemistry. In press
97. Qiu F., Dahl G., A permeant regulating its permeation pore: inhibition of pannexin 1 channels by ATP American Journal of Physiology 2009 296 2 C250 C255
98. Wang J., Ma M., Locovei S., Keane R. W., Dahl G., Modulation of membrane channel currents by gap junction protein mimetic peptides: size matters American Journal of Physiology 2007 293 3 C1112 C1119
99. Dando R., Roper S. D., Cell-to-cell communication in intact taste buds through ATP signalling from pannexin 1 gap junction hemichannels Journal of Physiology 2009 587 24 5899 5906
100. Barbe M. T., Monyer H., Bruzzone R., Cell-cell communication beyond connexins: the pannexin channels Physiology 2006 21 2 103 114 (Pubitemid 43752506)
101. Ma W., Compan V., Zheng W., Pannexin 1 forms an anion-selective channel Pflgers Archiv 2012 463 4 585 592
102. Vogt A., Hormuzdi S. G., Monyer H., Pannexin1 and Pannexin2 expression in the developing and mature rat brain Molecular Brain Research 2005 141 1 113 120 (Pubitemid 41566034)
103. Ray A., Zoidl G., Weickert S., Wahle P., Dermietzel R., Site-specific and developmental expression of pannexin1 in the mouse nervous system European Journal of Neuroscience 2005 21 12 3277 3290 (Pubitemid 40961423)
104. Bruzzone R., Barbe M. T., Jakob N. J., Monyer H., Pharmacological properties of homomeric and heteromeric pannexin hemichannels expressed in Xenopus oocytes Journal of Neurochemistry 2005 92 5 1033 1043 (Pubitemid 40344294)
105. Sez J. C., Berthoud V. M., Braes M. C., Martnez A. D., Beyer E. C., Plasma membrane channels formed by connexins: their regulation and functions Physiological Reviews 2003 83 4 1359 1400 (Pubitemid 37222275)
106. Yasuda T., Bartlett P. F., Adams D. J., Kir and Kv channels regulate electrical properties and proliferation of adult neural precursor cells Molecular and Cellular Neuroscience 2008 37 2 284 297 (Pubitemid 351173849)
107. Dubois J. M., Rouzaire-Dubois B., The influence of cell volume changes on tumour cell proliferation European Biophysics Journal 2004 33 3 227 232 (Pubitemid 39118299)
108. Rouzaire-Dubois B., Malo M., Milandri J. B., Dubois J. M., Cell size-proliferation relationship in rat glioma cells Glia 2004 45 3 249 257 (Pubitemid 38222253)
109. Nicchia G. P., Srinivas M., Li W., Brosnan C. F., Frigeri A., Spray D. C., New possible roles for aquaporin-4 in astrocytes: cell cytoskeleton and functional relationship with connexin43 FASEB Journal 2005 19 12 1674 1676 (Pubitemid 41429526)
110. Saha K., Keung A. J., Irwin E. F., Li Y., Little L., Schaffer D. V., Healy K. E., Substrate modulus directs neural stem cell behavior Biophysical Journal 2008 95 9 4426 4438
111. Keung A. J., de Juan-Pardo E. M., Schaffer D. V., Kumar S., Rho GTPases mediate the mechanosensitive lineage commitment of neural stem cells Stem Cells 2011 29 11 1886 1897
112. Imbeault S., Gauvin L. G., Toeg H. D., Pettit A., Sorbara C. D., Migahed L., DesRoches R., Menzies A. S., Nishii K., Paul D. L., Simon A. M., Bennett S. A. L., The extracellular matrix controls gap junction protein expression and function in postnatal hippocampal neural progenitor cells BMC Neuroscience 2009 10, article 13
113. Smyth J. W., Vogan J. M., Buch P. J., Actin cytoskeleton rest stops regulate anterograde traffic of connexin 43 vesicles to the plasma membrane Circulation Research 2012 110 7 978 989
114. Francis R., Xu X., Park H., Connexin43 modulates cell polarity and directional cell migration by regulating microtubule dynamics PLoS ONE 2011 6 10, article e26379
115. Crespin S., Bechberger J., Mesnil M., Naus C. C., Sin W. C., The carboxy-terminal tail of connexin43 gap junction protein is sufficient to mediate cytoskeleton changes in human glioma cells Journal of Cellular Biochemistry 2010 110 3 589 597
116. Toyofuku T., Yabuki M., Otsu K., Kuzuya T., Hori M., Tada M., Direct association of the gap junction protein connexin-43 with ZO-1 in cardiac myocytes The Journal of Biological Chemistry 1998 273 21 12725 12731 (Pubitemid 28246824)
117. Olk S., Zoidl G., Dermietzel R., Connexins, cell motility, and the cytoskeleton Cell Motility and the Cytoskeleton 2009 66 11 1000 1016
118. Ponsaerts R., Wang N., Himpens B., Leybaert L., Bultynck G., The contractile system as a negative regulator of the connexin 43 hemichannel. Biology of the Cell. In press
119. Bhalla-Gehi R., Penuela S., Churko J. M., Shao Q., Laird D. W., Pannexin1 and pannexin3 delivery, cell surface dynamics, and cytoskeletal interactions The Journal of Biological Chemistry 2010 285 12 9147 9160
120. Bao B. A., Lai C. P., Naus C. C., Morgan J. R., Pannexin1 drives multicellular aggregate compaction via a signaling cascade that remodels the actin cytoskeleton The Journal of Biological Chemistry 2012 287 11 8407 8416
121. Grimm I., Ullsperger S. N., Zimmermann H., Nucleotides and epidermal growth factor induce parallel cytoskeletal rearrangements and migration in cultured adult murine neural stem cells Acta Physiologica 2010 199 2 181 189
122. Benfenati V., Nicchia G. P., Svelto M., Rapisarda C., Frigeri A., Ferroni S., Functional down-regulation of volume-regulated anion channels in AQP4 knockdown cultured rat cortical astrocytes Journal of Neurochemistry 2007 100 1 87 104 (Pubitemid 46085841)
123. Ma W., Compan V., Zheng W., Pannexin 1 forms an anion-selective channel Pflgers Archiv 2012 463 4 585 592
124. Sabirov R. Z., Okada Y., The maxi-anion channel: a classical channel playing novel roles through an unidentified molecular entity Journal of Physiological Sciences 2009 59 1 3 21
125. Kang J., Kang N., Lovatt D., Torres A., Zhao Z., Lin J., Nedergaard M., Connexin 43 hemichannels are permeable to ATP Journal of Neuroscience 2008 28 18 4702 4711
126. Iglesias R., Dahl G., Qiu F., Spray D. C., Scemes E., Pannexin 1: the molecular substrate of astrocyte hemichannels Journal of Neuroscience 2009 29 21 7092 7097
127. Hoang Q. V., Qian H., Ripps H., Functional analysis of hemichannels and gap-junctional channels formed by connexins 43 and 46 Molecular Vision 2010 16 1343 1352
128. Ye Z. C., Oberheim N., Kettenmann H., Ransom B. R., Pharmacological cross-inhibition of connexin hemichannels and swelling activated anion channels Glia 2009 57 3 258 269
129. Sez J. C., Retamal M. A., Basilio D., Bukauskas F. F., Bennett M. V. L., Connexin-based gap junction hemichannels: gating mechanisms Biochimica et Biophysica Acta 2005 1711 2 215 224 (Pubitemid 40799296)