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Pannexin 1 forms an anion-selective channel

  • Ion Channels, Receptors and Transporters
  • Published:
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Abstract

Pannexin 1 (Panx1) is expressed in various mammalian tissues including the brain and immune cells. Here, we present evidence that Panx1 when expressed in mammalian cells, forms anion-selective channels, with a rank order of permeabilities: NO −3  > I− > Br− > Cl− > F− ≫ aspartate− ≈ glutamate− ≈ gluconate−. Single-channel Panx1-mediated currents have a unitary conductance around 68 pS. Our results show that Panx1 assembles into a membrane anion channel with a relatively low single-channel conductance.

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References

  1. Bao L, Locovei S, Dahl G (2004) Pannexin membrane channels are mechanosensitive conduits for ATP. FEBS Lett 572:65–68

    Article  PubMed  CAS  Google Scholar 

  2. Baranova A, Ivanov D, Petrash N, Pestova A, Skoblov M, Kelmanson I, Shagin D, Nazarenko S, Geraymovych E, Litvin O, Tiunova A, Born TL, Usman N, Staroverov D, Lukyanov S, Panchin Y (2004) The mammalian pannexin family is homologous to the invertebrate innexin gap junction proteins. Genomics 83:706–716

    Article  PubMed  CAS  Google Scholar 

  3. Boassa D, Ambrosi C, Qiu F, Dahl G, Gaietta G, Sosinsky G (2007) Pannexin1 channels contain a glycosylation site that targets the hexamer to the plasma membrane. J Biol Chem 282:31733–31743

    Article  PubMed  CAS  Google Scholar 

  4. Bruzzone R, Hormuzdi SG, Barbe MT, Herb A, Monyer H (2003) Pannexins, a family of gap junction proteins expressed in brain. Proc Natl Acad Sci USA 100:13644–13649

    Article  PubMed  CAS  Google Scholar 

  5. Bruzzone R, Barbe MT, Jakob NJ, Monyer H (2005) Pharmacological properties of homomeric and heteromeric pannexin hemichannels expressed in Xenopus oocytes. J Neurochem 92:1033–1043

    Article  PubMed  CAS  Google Scholar 

  6. Chekeni FB, Elliott MR, Sandilos JK, Walk SF, Kinchen JM, Lazarowski ER, Armstrong AJ, Penuela S, Laird DW, Salvesen GS, Isakson BE, Bayliss DA, Ravichandran KS (2010) Pannexin 1 channels mediate ‘find-me’ signal release and membrane permeability during apoptosis. Nature 467:863–867

    Article  PubMed  CAS  Google Scholar 

  7. Dando R, Roper SD (2009) Cell-to-cell communication in intact taste buds through ATP signalling from pannexin 1 gap junction hemichannels. J Physiol 587:5899–5906

    Article  PubMed  CAS  Google Scholar 

  8. Eghbali B, Kessler JA, Spray DC (1990) Expression of gap junction channels in communication-incompetent cells after stable transfection with cDNA encoding connexin 32. Proc Natl Acad Sci USA 87:1328–1331

    Article  PubMed  CAS  Google Scholar 

  9. Fields RD (2011) Nonsynaptic and nonvesicular ATP release from neurons and relevance to neuron-glia signaling. Semin Cell Dev Biol 22:214–219

    Article  PubMed  CAS  Google Scholar 

  10. Huang Y, Grinspan JB, Abrams CK, Scherer SS (2007) Pannexin1 is expressed by neurons and glia but does not form functional gap junctions. Glia 55:46–56

    Article  PubMed  Google Scholar 

  11. Huang YJ, Maruyama Y, Dvoryanchikov G, Pereira E, Chaudhari N, Roper SD (2007) The role of pannexin 1 hemichannels in ATP release and cell-cell communication in mouse taste buds. Proc Natl Acad Sci USA 104:6436–6441

    Article  PubMed  CAS  Google Scholar 

  12. Iglesias R, Dahl G, Qiu F, Spray DC, Scemes E (2009) Pannexin 1: the molecular substrate of astrocyte “hemichannels”. J Neurosci 29:7092–7097

    Article  PubMed  CAS  Google Scholar 

  13. Kawamura M Jr, Ruskin DN, Masino SA (2010) Metabolic autocrine regulation of neurons involves cooperation among pannexin hemichannels, adenosine receptors, and KATP channels. J Neurosci 30:3886–3895

    Article  PubMed  CAS  Google Scholar 

  14. Locovei S, Bao L, Dahl G (2006) Pannexin 1 in erythrocytes: function without a gap. Proc Natl Acad Sci USA 103:7655–7659

    Article  PubMed  CAS  Google Scholar 

  15. Locovei S, Wang J, Dahl G (2006) Activation of pannexin 1 channels by ATP through P2Y receptors and by cytoplasmic calcium. FEBS Lett 580:239–244

    Article  PubMed  CAS  Google Scholar 

  16. Ma W, Hui H, Pelegrin P, Surprenant A (2009) Pharmacological characterization of pannexin-1 currents expressed in mammalian cells. J Pharmacol Exp Ther 328:409–418

    Article  PubMed  CAS  Google Scholar 

  17. MacVicar BA, Thompson RJ (2010) Non-junction functions of pannexin-1 channels. Trends Neurosci 33:93–102

    Article  PubMed  CAS  Google Scholar 

  18. Moreno AP, Eghbali B, Spray DC (1991) Connexin32 gap junction channels in stably transfected cells: unitary conductance. Biophys J 60:1254–1266

    Article  PubMed  CAS  Google Scholar 

  19. Neussert R, Muller C, Milenkovic VM, Strauss O (2010) The presence of bestrophin-1 modulates the Ca2+ recruitment from Ca2+ stores in the ER. Pflugers Arch 460:163–175

    Article  PubMed  CAS  Google Scholar 

  20. Panchin YV (2005) Evolution of gap junction proteins—the pannexin alternative. J Exp Biol 208:1415–1419

    Article  PubMed  CAS  Google Scholar 

  21. Panchin Y, Kelmanson I, Matz M, Lukyanov K, Usman N, Lukyanov S (2000) A ubiquitous family of putative gap junction molecules. Curr Biol 10:R473–474

    Article  PubMed  CAS  Google Scholar 

  22. Pelegrin P, Surprenant A (2006) Pannexin-1 mediates large pore formation and interleukin-1β release by the ATP-gated P2X7 receptor. EMBO J 25:5071–5082

    Article  PubMed  CAS  Google Scholar 

  23. Pelegrin P, Barroso-Gutierrez C, Surprenant A (2008) P2X7 receptor differentially couples to distinct release pathways for IL-1β in mouse macrophage. J Immunol 180:7147–7157

    PubMed  CAS  Google Scholar 

  24. Ransford GA, Fregien N, Qiu F, Dahl G, Conner GE, Salathe M (2009) Pannexin 1 contributes to ATP release in airway epithelia. Am J Respir Cell Mol Biol 41:525–534

    Article  PubMed  CAS  Google Scholar 

  25. Reyes JP, Hernandez-Carballo CY, Perez-Flores G, Perez-Cornejo P, Arreola J (2009) Lack of coupling between membrane stretching and pannexin-1 hemichannels. Biochem Biophys Res Commun 380:50–53

    Article  PubMed  CAS  Google Scholar 

  26. Schalper KA, Palacios-Prado N, Retamal MA, Shoji KF, Martinez AD, Saez JC (2008) Connexin hemichannel composition determines the FGF-1-induced membrane permeability and free [Ca2+]i responses. Mol Biol Cell 19:3501–3513

    Article  PubMed  CAS  Google Scholar 

  27. Silverman WR, de Rivero Vaccari JP, Locovei S, Qiu F, Carlsson SK, Scemes E, Keane RW, Dahl G (2009) The pannexin 1 channel activates the inflammasome in neurons and astrocytes. J Biol Chem 284:18143–18151

    Article  PubMed  CAS  Google Scholar 

  28. Thompson RJ, Jackson MF, Olah ME, Rungta RL, Hines DJ, Beazely MA, MacDonald JF, MacVicar BA (2008) Activation of pannexin-1 hemichannels augments aberrant bursting in the hippocampus. Science 322:1555–1559

    Article  PubMed  CAS  Google Scholar 

  29. Wright EM, Diamond JM (1977) Anion selectivity in biological systems. Physiol Rev 57:109–156

    PubMed  CAS  Google Scholar 

  30. Yang YD, Cho H, Koo JY, Tak MH, Cho Y, Shim WS, Park SP, Lee J, Lee B, Kim BM, Raouf R, Shin YK, Oh U (2008) TMEM16A confers receptor-activated calcium-dependent chloride conductance. Nature 455:1210–1215

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

The authors would like to thank Austin Sitko and Rosemary Gaskell for cell culture assistance. This study was supported by the Biotechnology and Biological Sciences Research Council, UK.

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  1. Weihong Ma

    Present address: Manchester Medical School, Faculty of Medical and Human Sciences, The University of Manchester, Oxford Road, Manchester, M13 9PT, UK

Authors and Affiliations

  1. Faculty of Life Sciences, The University of Manchester, Smith Building, Oxford Road, Manchester, M13 9PT, UK

    Weihong Ma, Vincent Compan, Wenxuan Zheng, Elizabeth Martin, R. Alan North, Alexei Verkhratsky & Annmarie Surprenant

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  1. Weihong Ma
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  2. Vincent Compan
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  3. Wenxuan Zheng
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Corresponding author

Correspondence to Alexei Verkhratsky.

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Weihong Ma and Vincent Compan contributed equally to the study.

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Ma, W., Compan, V., Zheng, W. et al. Pannexin 1 forms an anion-selective channel. Pflugers Arch - Eur J Physiol 463, 585–592 (2012). https://doi.org/10.1007/s00424-012-1077-z

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  • DOI: https://doi.org/10.1007/s00424-012-1077-z

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