The biochemistry and function of pannexin channels

Biochimica et Biophysica Acta - Biomembranes

Volumn 1828, Issue 1, 2013, Pages 15-22

  Penuela, Silvia ^a   Gehi, Ruchi ^a   Laird, Dale W ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

Biochemistry; Pannexin; Panx1; Panx2; Panx3; Physiological function

Indexed keywords

ADENOSINE TRIPHOSPHATE; ANTIRETROVIRUS AGENT; CALCIUM; CD4 ANTIGEN; GLYCOPROTEIN; PANNEXIN 1; PANNEXIN 2; PANNEXIN 3; PURINERGIC P2X7 RECEPTOR; UNCLASSIFIED DRUG;

APOPTOSIS; BIOCHEMISTRY; BLOOD VESSEL TONE; CALCIUM SIGNALING; CANCER INHIBITION; CARCINOGENESIS; CARTILAGE CELL; CD4+ T LYMPHOCYTE; CELL DEATH; CELL DIFFERENTIATION; CELL MATURATION; CELLULAR IMMUNITY; DISEASE COURSE; EPILEPTIC STATE; EPILEPTOGENESIS; GENOMICS; GLIOMA; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; KERATINOCYTE; MALIGNANT TRANSFORMATION; MUCOCILIARY CLEARANCE; NERVE CELL DIFFERENTIATION; NONHUMAN; OSTEOBLAST; PARACRINE SIGNALING; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEFECT; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; REVIEW; SEIZURE; SPERMATOZOON MIGRATION; TASTE ACUITY; TASTE BUD; VASOCONSTRICTION; VASODILATATION;

ANIMALS; CONNEXINS; GENE EXPRESSION; GENE KNOCKOUT TECHNIQUES; HUMANS; PARACRINE COMMUNICATION; PROTEIN CONFORMATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STABILITY;

HUMAN IMMUNODEFICIENCY VIRUS 1; MAMMALIA;

EID: 84870054442     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2012.01.017     Document Type: Review

References (77)

1. Y. Panchin, I. Kelmanson, M. Matz, K. Lukyanov, N. Usman, and S. Lukyanov A ubiquitous family of putative gap junction molecules Curr. Biol. 10 2000 R473 R474
2. M.R. Yen, and M.H. Saier Jr. Gap junctional proteins of animals: the innexin/pannexin superfamily Prog. Biophys. Mol. Biol. 94 2007 5 14
3. A. Baranova, D. Ivanov, N. Petrash, A. Pestova, M. Skoblov, I. Kelmanson, D. Shagin, S. Nazarenko, E. Geraymovych, O. Litvin, A. Tiunova, T.L. Born, N. Usman, D. Staroverov, S. Lukyanov, and Y. Panchin The mammalian pannexin family is homologous to the invertebrate innexin gap junction proteins Genomics 83 2004 706 716
4. S. Penuela, R. Bhalla, X.Q. Gong, K.N. Cowan, S.J. Celetti, B.J. Cowan, D. Bai, Q. Shao, and D.W. Laird Pannexin 1 and pannexin 3 are glycoproteins that exhibit many distinct characteristics from the connexin family of gap junction proteins J. Cell Sci. 120 2007 3772 3783
5. R. Bauer, B. Loer, K. Ostrowski, J. Martini, A. Weimbs, H. Lechner, and M. Hoch Intercellular communication: the Drosophila innexin multiprotein family of gap junction proteins Chem. Biol. 12 2005 515 526
6. M.K. Iovine, A.M. Gumpert, M.M. Falk, and T.C. Mendelson Cx23, a connexin with only four extracellular-loop cysteines, forms functional gap junction channels and hemichannels FEBS Lett. 582 2008 165 170
7. C.I. Foote, L. Zhou, X. Zhu, and B.J. Nicholson The pattern of disulfide linkages in the extracellular loop regions of connexin 32 suggests a model for the docking interface of gap junctions J. Cell Biol. 140 1998 1187 1197
8. D. Boassa, C. Ambrosi, F. Qiu, G. Dahl, G. Gaietta, and G. Sosinsky Pannexin1 channels contain a glycosylation site that targets the hexamer to the plasma membrane J. Biol. Chem. 282 2007 31733 31743
9. C. Ambrosi, O. Gassmann, J.N. Pranskevich, D. Boassa, A. Smock, J. Wang, G. Dahl, C. Steinem, and G.E. Sosinsky Pannexin1 and Pannexin2 channels show quaternary similarities to connexons and different oligomerization numbers from each other J. Biol. Chem. 285 2010 24420 24431
10. J. Wang, and G. Dahl SCAM analysis of Panx1 suggests a peculiar pore structure J. Gen. Physiol. 136 2010 515 527
11. R. Bruzzone, T.W. White, and D.L. Paul Connections with connexins: the molecular basis of direct intercellular signaling [Review] [535 refs] Eur. J. Biochem. 238 1996 1 27
12. D.A. Goodenough, J.A. Goliger, and D.L. Paul Connexins, connexons, and intercellular communication Annu. Rev. Biochem. 65 1996 475 502
13. G.E. Sosinsky, D. Boassa, R. Dermietzel, H.S. Duffy, D.W. Laird, B. MacVicar, C.C. Naus, S. Penuela, E. Scemes, D.C. Spray, R.J. Thompson, H.B. Zhao, and G. Dahl Pannexin channels are not gap junction hemichannels Channels (Austin) 5 2011 193 197
14. D. Boassa, F. Qiu, G. Dahl, and G. Sosinsky Trafficking dynamics of glycosylated pannexin1 proteins Cell Commun. Adhes. 15 2008 119 132
15. S. Penuela, R. Bhalla, K. Nag, and D.W. Laird Glycosylation regulates pannexin intermixing and cellular localization Mol. Biol. Cell 20 2009 4313 4323
16. R. Bruzzone, S.G. Hormuzdi, M.T. Barbe, A. Herb, and H. Monyer Pannexins, a family of gap junction proteins expressed in brain Proc. Natl. Acad. Sci. U. S. A. 100 2003 13644 13649
17. G. Dvoriantchikova, D. Ivanov, Y. Panchin, and V.I. Shestopalov Expression of pannexin family of proteins in the retina FEBS Lett. 580 2006 2178 2182
18. G. Dvoriantchikova, D. Ivanov, A. Pestova, and V. Shestopalov Molecular characterization of pannexins in the lens Mol. Vis. 12 2006 1417 1426
19. A. Ray, G. Zoidl, P. Wahle, and R. Dermietzel Pannexin expression in the cerebellum Cerebellum 5 2006 189 192
20. A. Ray, G. Zoidl, S. Weickert, P. Wahle, and R. Dermietzel Site-specific and developmental expression of pannexin1 in the mouse nervous system Eur. J. Neurosci. 21 2005 3277 3290
21. V.I. Shestopalov, and Y. Panchin Pannexins and gap junction protein diversity Cell. Mol. Life Sci. 65 2008 376 394
22. G. Sohl, S. Maxeiner, and K. Willecke Expression and functions of neuronal gap junctions Nat. Rev. Neurosci. 6 2005 191 200
23. A. Vogt, S.G. Hormuzdi, and H. Monyer Pannexin1 and pannexin2 expression in the developing and mature rat brain Mol. Brain Res. 141 2005 113 120
24. S. Weickert, A. Ray, G. Zoidl, and R. Dermietzel Expression of neural connexins and pannexin1 in the hippocampus and inferior olive: a quantitative approach Mol. Brain Res. 133 2005 102 109
25. A. Zappala, D. Cicero, M.F. Serapide, C. Paz, M.V. Catania, M. Falchi, R. Parenti, M.R. Panto, F. La Delia, and F. Cicirata Expression of pannexin1 in the CNS of adult mouse: cellular localization and effect of 4-aminopyridine- induced seizures Neuroscience 141 2006 167 178
26. G. Zoidl, E. Petrasch-Parwez, A. Ray, C. Meier, S. Bunse, H.-W. Habbes, G. Dahl, and R. Dermietzel Localization of the pannexin1 protein at postsynaptic sites in the cerebral cortex and hippocampus Neuroscience 146 2007 9 16
27. X.H. Wang, M. Streeter, Y.P. Liu, and H.B. Zhao Identification and characterization of pannexin expression in the mammalian cochlea J. Comp. Neurol. 512 2009 336 346
28. M. Billaud, A.W. Lohman, A.C. Straub, R. Looft-Wilson, S.R. Johnstone, C.A. Araj, A.K. Best, F.B. Chekeni, K.S. Ravichandran, S. Penuela, D.W. Laird, and B.E. Isakson Pannexin1 regulates alpha1-adrenergic receptor-mediated vasoconstriction Circ. Res. 109 2011 80 85
29. P. Turmel, J. Dufresne, L. Hermo, C.E. Smith, S. Penuela, D.W. Laird, and D.G. Cyr Characterization of pannexin1 and pannexin3 and their regulation by androgens in the male reproductive tract of the adult rat Mol. Reprod. Dev. 78 2011 124 138
30. L.A. Swayne, C.D. Sorbara, and S.A. Bennett Pannexin 2 is expressed by postnatal hippocampal neural progenitors and modulates neuronal commitment J. Biol. Chem. 285 2010 24977 24986
31. T. Iwamoto, T. Nakamura, A. Doyle, M. Ishikawa, S. de Vega, S. Fukumoto, and Y. Yamada Pannexin 3 regulates intracellular ATP/cAMP levels and promotes chondrocyte differentiation J. Biol. Chem. 285 2010 18948 18958
32. S.R. Bond, A. Lau, S. Penuela, A.V. Sampaio, T.M. Underhill, D.W. Laird, and C.C. Naus Pannexin3 is a novel target for Runx2, expressed by osteoblasts and mature growth plate chondrocytes J. Bone Miner. Res. 26 2011 2911 2922
33. M. Ishikawa, T. Iwamoto, T. Nakamura, A. Doyle, S. Fukumoto, and Y. Yamada Pannexin 3 functions as an ER Ca(2 +) channel, hemichannel, and gap junction to promote osteoblast differentiation J. Cell Biol. 193 2011 1257 1274
34. S. Penuela, S.J. Celetti, R. Bhalla, Q. Shao, and D.W. Laird Diverse subcellular distribution profiles of pannexin 1 and pannexin 3 Cell Commun. Adhes. 15 2008 133 142
35. R. Bruzzone, M.T. Barbe, N.J. Jakob, and H. Monyer Pharmacological properties of homomeric and heteromeric pannexin hemichannels expressed in Xenopus oocytes J. Neurochem. 92 2005 1033 1043
36. R. Bhalla-Gehi, S. Penuela, J.M. Churko, Q. Shao, and D.W. Laird Pannexin1 and pannexin3 delivery, cell surface dynamics, and cytoskeletal interactions J. Biol. Chem. 285 2010 9147 9160
37. S. Bunse, A. Haghika, G. Zoidl, and R. Dermietzel Identification of a potential regulator of the gap junction protein pannexin1 Cell Commun. Adhes. 12 2005 231 236
38. S. Bunse, S. Locovei, M. Schmidt, F. Qiu, G. Zoidl, G. Dahl, and R. Dermietzel The potassium channel subunit Kvbeta3 interacts with pannexin 1 and attenuates its sensitivity to changes in redox potentials FEBS J. 276 2009 6258 6270
39. W.R. Silverman, J.P. De Rivero Vaccari, S. Locovei, F. Qiu, S.K. Carlsson, E. Scemes, R.W. Keane, and G. Dahl The pannexin 1 channel activates the inflammasome in neurons and astrocytes J. Biol. Chem. 284 2009 18143 18151
40. L. Bao, S. Locovei, and G. Dahl Pannexin membrane channels are mechanosensitive conduits for ATP FEBS Lett. 572 2004 65 68
41. J.C. Saez, M.A. Retamal, D. Basilio, F.F. Bukauskas, and M.V. Bennett Connexin-based gap junction hemichannels: gating mechanisms Biochim. Biophys. Acta 1711 2005 215 224
42. F.B. Chekeni, M.R. Elliott, J.K. Sandilos, S.F. Walk, J.M. Kinchen, E.R. Lazarowski, A.J. Armstrong, S. Penuela, D.W. Laird, G.S. Salvesen, B.E. Isakson, D.A. Bayliss, and K.S. Ravichandran Pannexin 1 channels mediate 'find-me' signal release and membrane permeability during apoptosis Nature 467 2010 863 867
43. S. Locovei, J. Wang, and G. Dahl Activation of pannexin 1 channels by ATP through P2Y receptors and by cytoplasmic calcium FEBS Lett. 580 2006 239 244
44. P. Pelegrin, and A. Surprenant Pannexin-1 mediates large pore formation and interleukin-1beta release by the ATP-gated P2X7 receptor EMBO J. 25 2006 5071 5082
45. D. Reigada, W. Lu, M. Zhang, and C.H. Mitchell Elevated pressure triggers a physiological release of ATP from the retina: possible role for pannexin hemichannels Neuroscience 157 2008 396 404
46. U. Schenk, A.M. Westendorf, E. Radaelli, A. Casati, M. Ferro, M. Fumagalli, C. Verderio, J. Buer, E. Scanziani, and F. Grassi Purinergic control of T cell activation by ATP released through pannexin-1 hemichannels Sci. Signal. 1 2008 ra6
47. F. Qiu, and G. Dahl A permeant regulating its permeation pore: inhibition of pannexin 1 channels by ATP Am. J. Physiol. Cell Physiol. 296 2009 C250 C255
48. J. Wang, M. Ma, S. Locovei, R.W. Keane, and G. Dahl Modulation of membrane channel currents by gap junction protein mimetic peptides: size matters Am. J. Physiol. Cell Physiol. 293 2007 C1112 C1119
49. M.T. Barbe, H. Monyer, and R. Bruzzone Cell-cell communication beyond connexins: the pannexin channels Physiology (Bethesda) 21 2006 103 114
50. R. Dando, and S.D. Roper Cell-to-cell communication in intact taste buds through ATP signalling from pannexin 1 gap junction hemichannels J. Physiol. 587 2009 5899 5906
51. G. Dahl, and S. Locovei Pannexin: to gap or not to gap, is that a question? IUBMB Life 58 2006 409 419
52. Y. Huang, J.B. Grinspan, C.K. Abrams, and S.S. Scherer Pannexin1 is expressed by neurons and glia but does not form functional gap junctions Glia 55 2007 46 56
53. R.J. Thompson, M.F. Jackson, M.E. Olah, R.L. Rungta, D.J. Hines, M.A. Beazely, J.F. MacDonald, and B.A. MacVicar Activation of pannexin-1 hemichannels augments aberrant bursting in the hippocampus Science 322 2008 1555 1559
54. S.J. Celetti, K.N. Cowan, S. Penuela, Q. Shao, J. Churko, and D.W. Laird Implications of pannexin 1 and pannexin 3 for keratinocyte differentiation J. Cell Sci. 123 2010 1363 1372
55. R. Bruzzone, and R. Dermietzel Structure and function of gap junctions in the developing brain Cell Tissue Res. 26 2006 239 248
56. C.P.K. Lai, J.F. Bechberger, R.J. Thompson, B.A. MacVicar, R. Bruzzone, and C.C. Naus Tumor-suppressive effects of pannexin 1 in C6 glioma cells Cancer Res. 67 2007 1545 1554
57. F. Vanden Abeele, G. Bidaux, D. Gordienko, B. Beck, Y.V. Panchin, A.V. Baranova, D.V. Ivanov, R. Skryma, and N. Prevarskaya Functional implications of calcium permeability of the channel formed by pannexin 1 J. Cell Biol. 174 2006 535 546
58. S. Locovei, L. Bao, and G. Dahl Pannexin 1 in erythrocytes: function without a gap Proc. Natl. Acad. Sci. U. S. A. 103 2006 7655 7659
59. M.V. Bennett, and R.S. Zukin Electrical coupling and neuronal synchronization in the mammalian brain Neuron 41 2004 495 511
60. M.J. Berridge, M.D. Bootman, and H.L. Roderick Calcium signalling: dynamics, homeostasis and remodelling Nat. Rev. Mol. Cell Biol. 4 2003 517 529
61. E. Scemes, D.C. Spray, and P. Meda Connexins, pannexins, innexins: novel roles of hemi-channels Pflugers Arch. 457 2009 1207 1226
62. S. Locovei, E. Scemes, F. Qiu, D.C. Spray, and G. Dahl Pannexin1 is part of the pore forming unit of the P2X7 receptor death complex FEBS Lett. 581 2007 483 488
63. M.F. Santiago, J. Veliskova, N.K. Patel, S.E. Lutz, D. Caille, A. Charollais, P. Meda, and E. Scemes Targeting pannexin1 improves seizure outcome PLoS One 6 2011 e25178
64. G.R. Bergfeld, and T. Forrester Release of ATP from human erythrocytes in response to a brief period of hypoxia and hypercapnia Cardiovasc. Res. 26 1992 40 47
65. Y.-J. Huang, Y. Maruyama, G. Dvoryanchikov, E. Pereira, N. Chaudhari, and S.D. Roper The role of pannexin 1 hemichannels in ATP release and cell-cell communication in mouse taste buds Proc. Natl. Acad. Sci. U. S. A. 104 2007 6436 6441
66. G.A. Ransford, N. Fregien, F. Qiu, G. Dahl, G.E. Conner, and M. Salathe Pannexin 1 contributes to ATP release in airway epithelia Am. J. Respir. Cell Mol. Biol. 41 2009 525 534
67. C. Seror, M.T. Melki, F. Subra, S.Q. Raza, M. Bras, H. Saidi, R. Nardacci, L. Voisin, A. Paoletti, F. Law, I. Martins, A. Amendola, A.A. Abdul-Sater, F. Ciccosanti, O. Delelis, F. Niedergang, S. Thierry, N. Said-Sadier, C. Lamaze, D. Metivier, J. Estaquier, G.M. Fimia, L. Falasca, R. Casetti, N. Modjtahedi, J. Kanellopoulos, J.F. Mouscadet, D.M. Ojcius, M. Piacentini, M.L. Gougeon, G. Kroemer, and J.L. Perfettini Extracellular ATP acts on P2Y2 purinergic receptors to facilitate HIV-1 infection J. Exp. Med. 208 2011 1823 1834
68. T.D. Kanneganti, M. Lamkanfi, Y.G. Kim, G. Chen, J.H. Park, L. Franchi, P. Vandenabeele, and G. Nunez Pannexin-1-mediated recognition of bacterial molecules activates the cryopyrin inflammasome independent of Toll-like receptor signaling Immunity 26 2007 433 443
69. Y. Qu, S. Misaghi, K. Newton, L.L. Gilmour, S. Louie, J.E. Cupp, G.R. Dubyak, D. Hackos, and V.M. Dixit Pannexin-1 is required for ATP release during apoptosis but not for inflammasome activation J. Immunol. 186 2011 6553 6561
70. C.P. Lai, J.F. Bechberger, and C.C. Naus Pannexin2 as a novel growth regulator in C6 glioma cells Oncogene 28 2009 4402 4408
71. R.J. Thompson, N. Zhou, and B.A. MacVicar Ischemia opens neuronal gap junction hemichannels Science 312 2006 924 927
72. 2 + signals across the inner ear Proc. Natl. Acad. Sci. U. S. A. 105 2008 18770 18775
73. L. Seminario-Vidal, S.F. Okada, J.I. Sesma, S.M. Kreda, C.A. van Heusden, Y. Zhu, L.C. Jones, W.K. O'Neal, S. Penuela, D.W. Laird, R.C. Boucher, and E.R. Lazarowski Rho signaling regulates pannexin 1-mediated ATP release from airway epithelia J. Biol. Chem. 286 2011 26277 26286
74. P. Bargiotas, A. Krenz, S.G. Hormuzdi, D.A. Ridder, A. Herb, W. Barakat, S. Penuela, J. von Engelhardt, H. Monyer, and M. Schwaninger Pannexins in ischemia-induced neurodegeneration Proc. Natl. Acad. Sci. U. S. A. 108 2011 20772 22077
75. E. Scemes, S.O. Suadicani, G. Dahl, and D.C. Spray Connexin and pannexin mediated cell-cell communication Neuron Glia Biol. 3 2007 199 208
76. S. Li, I. Bjelobaba, Z. Yan, M. Kucka, M. Tomic, and S.S. Stojilkovic Expression and roles of pannexins in ATP release in the pituitary gland Endocrinology 152 2011 2342 2352
77. W. Ma, H. Hui, P. Pelegrin, and A. Surprenant Pharmacological characterization of pannexin-1 currents expressed in mammalian cells J. Pharmacol. Exp. Ther. 328 2009 409 418