Pannexin1 Channel Proteins in the Zebrafish Retina Have Shared and Unique Properties

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Kurtenbach, Sarah ^a,d   Prochnow, Nora ^a   Kurtenbach, Stefan ^d   Klooster, Jan ^b   Zoidl, Christiane ^a,d   Dermietzel, Rolf ^a   Kamermans, Maarten ^b,c   Zoidl, Georg ^a,d  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

^c ACADEMIC MEDICAL CENTER   (Netherlands)

^d YORK UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; PROTEIN DRPANX1A; PROTEIN DRPANX1B; UNCLASSIFIED DRUG; GAP JUNCTION PROTEIN; ISOPROTEIN; OLIGONUCLEOTIDE; PANX1 PROTEIN, ZEBRAFISH; ZEBRAFISH PROTEIN;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN; CHANNEL GATING; CONTROLLED STUDY; EVOLUTION; FEMALE; GENE DUPLICATION; MALE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN LOCALIZATION; RETINA; SEQUENCE HOMOLOGY; SPECIES DIFFERENCE; ZEBRA FISH; ANIMAL; CONFOCAL MICROSCOPY; DNA SEQUENCE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOHISTOCHEMISTRY; KINETICS; METABOLISM; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PATCH CLAMP TECHNIQUE; PHYLOGENY; REAL TIME POLYMERASE CHAIN REACTION; SITE DIRECTED MUTAGENESIS; WESTERN BLOTTING;

ANIMALS; BASE SEQUENCE; BLOTTING, WESTERN; CONNEXINS; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; KINETICS; MICROSCOPY, CONFOCAL; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; OLIGONUCLEOTIDES; PATCH-CLAMP TECHNIQUES; PHYLOGENY; PROTEIN ISOFORMS; REAL-TIME POLYMERASE CHAIN REACTION; RETINA; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84886061563     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0077722     Document Type: Article

References (53)

1. Sosinsky GE, Boassa D, Dermietzel R, Duffy HS, Laird DW, et al. (2011) Pannexin channels are not gap junction hemichannels. Channels (Austin, Tex) 5: 193-197. doi:10.4161/chan.5.3.15765.
2. Ray A, Zoidl G, Weickert S, Wahle P, Dermietzel R, (2005) Site-specific and developmental expression of pannexin1 in the mouse nervous system. Eur J Neurosci 21: 3277-3290. doi:10.1111/j.1460-9568.2005.04139.x. PubMed: 16026466.
3. Zoidl G, Petrasch-Parwez E, Ray A, Meier C, Bunse S, et al. (2007) Localization of the pannexin1 protein at postsynaptic sites in the cerebral cortex and hippocampus. Neuroscience 146: 9-16. doi:10.1016/j.neuroscience.2007.01.061. PubMed: 17379420.
4. Dvoriantchikova G, Ivanov D, Panchin Y, Shestopalov VI, (2006) Expression of pannexin family of proteins in the retina. FEBS Lett 580: 2178-2182. doi:10.1016/j.febslet.2006.03.026. PubMed: 16616526.
5. Pelegrin P, Surprenant A, (2006) Pannexin-1 mediates large pore formation and interleukin-1beta release by the ATP-gated P2X7 receptor. EMBO J 25: 5071-5082. doi:10.1038/sj.emboj.7601378. PubMed: 17036048.
6. 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. doi:10.1016/j.febslet.2005.12.004. PubMed: 16364313.
7. Wang J, Ma M, Locovei S, Keane RW, Dahl G, (2007) Modulation of membrane channel currents by gap junction protein mimetic peptides: size matters. Am J Physiol Cell Physiol 293: C1112-C1119. doi:10.1152/ajpcell.00097.2007. PubMed: 17652431.
8. Qiu F, Dahl G, (2009) A permeant regulating its permeation pore: inhibition of pannexin 1 channels by ATP. Am J Physiol Cell Physiol 296: C250-C255. doi:10.1152/ajpcell.00433.2008. PubMed: 18945939.
9. Zoidl G, Kremer M, Zoidl C, Bunse S, Dermietzel R, (2008) Molecular diversity of connexin and pannexin genes in the retina of the zebrafish Danio rerio. Cell Commun Adhes 15: 169-183. doi:10.1080/15419060802014081. PubMed: 18649188.
10. Prochnow N, Hoffmann S, Vroman R, Klooster J, Bunse S, et al. (2009) Pannexin1 in the outer retina of the zebrafish, Danio rerio. Neuroscience 162: 1039-1054. doi:10.1016/j.neuroscience.2009.04.064. PubMed: 19409451.
11. Prochnow N, Hoffmann S, Dermietzel R, Zoidl G, (2009) Replacement of a single cysteine in the fourth transmembrane region of zebrafish pannexin1 alters hemichannel gating behavior. Exp Brain Res 199: 255-264. doi:10.1007/s00221-009-1957-4. PubMed: 19701745.
12. Klaassen LJ, Sun Z, Steijaert MN, Bolte P, Fahrenfort I, et al. (2011) Synaptic Transmission from Horizontal Cells to Cones Is Impaired by Loss of Connexin Hemichannels. PLOS Biol 9: e1001107. doi:10.1371/journal.pbio.1001107. PubMed: 21811399.
13. Kranz K, Dorgau B, Pottek M, Herrling R, Schultz K, et al. (2013) Expression of Pannexin1 in the outer plexiform layer of the mouse retina and physiological impact of its knockout. J Comp Neurol 521: 1119-1135. doi:10.1002/cne.23223. PubMed: 22965528.
14. Bond SR, Wang N, Leybaert L, Naus CC, (2012) Pannexin 1 Ohnologs in the Teleost Lineage. J Membr Biol 245: 483-493. doi:10.1007/s00232-012-9497-4. PubMed: 22922822.
15. Olmsted JB, Carlson K, Klebe R, Ruddle F, Rosenbaum J, (1970) Isolation of microtubule protein from cultured mouse neuroblastoma cells. Proc Natl Acad Sci U S A 65: 129-136. doi:10.1073/pnas.65.1.129. PubMed: 5263744.
16. Shields CR, Klooster J, Claassen Y, Ul-Hussain M, Zoidl G, et al. (2007) Retinal horizontal cell-specific promoter activity and protein expression of zebrafish connexin 52.6 and connexin. p. 55.5. The Journal of comparative neurology 501: 765-779. doi:10.1002/cne.21282.
17. Grigoriev IV, Nordberg H, Shabalov I, Aerts A, Cantor M, et al. (2012) The genome portal of the Department of Energy Joint Genome Institute. Nucleic Acids Res 40: D26-D32. doi:10.1093/nar/gkr947. PubMed: 22110030.
18. Chapman Ja, Kirkness EF, Simakov O, Hampson SE, Mitros T, et al. (2010) The dynamic genome of Hydra. Nature 464: 592-596. doi:10.1038/nature08830. PubMed: 20228792.
19. Katoh K, Misawa K, Kuma K, Miyata T, (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30: 3059-3066. doi:10.1093/nar/gkf436. PubMed: 12136088.
20. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, et al. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML. Syst Biol 3.0: 59: 307-321. doi:10.1093/sysbio/syq010.
21. Abascal F, Zardoya R, Posada D, (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21: 2104-2105. doi:10.1093/bioinformatics/bti263. PubMed: 15647292.
22. Stamatakis A, (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics (Oxf, England) 22: 2688-2690. doi:10.1093/bioinformatics/btl446. PubMed: 16928733.
23. Miller Ma, Pfeiffer W, Schwartz T, (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. 2010 Gateway Computing Environments. Workshop (GCE): pp. 1-8. doi:10.1109/GCE.2010.5676129.
24. Boassa D, Ambrosi C, Qiu F, Dahl G, Gaietta G, et al. (2007) Pannexin1 channels contain a glycosylation site that targets the hexamer to the plasma membrane. J Biol Chem 282: 31733-31743. doi:10.1074/jbc.M702422200. PubMed: 17715132.
25. Penuela S, Bhalla R, Gong XQ, Cowan KN, Celetti SJ, et al. (2007) Pannexin 1 and pannexin 3 are glycoproteins that exhibit many distinct characteristics from the connexin family of gap junction proteins. J Cell Sci 120: 3772-3783. doi:10.1242/jcs.009514. PubMed: 17925379.
26. Boassa D, Qiu F, Dahl G, Sosinsky G, (2008) Trafficking dynamics of glycosylated pannexin 1 proteins. Cell Commun Adhes 15: 119-132. doi:10.1080/15419060802013885. PubMed: 18649184.
27. Penuela S, Bhalla R, Nag K, Laird DW, (2009) Glycosylation regulates pannexin intermixing and cellular localization. Mol Biol Cell 20: 4313-4323. doi:10.1091/mbc.E09-01-0067. PubMed: 19692571.
28. Fahrenfort I, Sjoerdsma T, Ripps H, Kamermans M, (2004) Cobalt ions inhibit negative feedback in the outer retina by blocking hemichannels on horizontal cells. Vis Neurosci 21: 501-511. doi:10.1017/S095252380421402X. PubMed: 15579217.
29. Contreras JE, Sánchez HA, Eugenin EA, Speidel D, Theis M, et al. (2002) Metabolic inhibition induces opening of unapposed connexin 43 gap junction hemichannels and reduces gap junctional communication in cortical astrocytes in culture. Proc Natl Acad Sci U S A 99: 495-500. doi:10.1073/pnas.012589799. PubMed: 11756680.
30. Trexler EB, Bukauskas FF, Bennett MV, Bargiello TA, Verselis VK, (1999) Rapid and direct effects of pH on connexins revealed by the connexin46 hemichannel preparation. J Gen Physiol 113: 721-742. doi:10.1085/jgp.113.5.721. PubMed: 10228184.
31. Ambrosi C, Gassmann O, Pranskevich JN, Boassa D, Smock A, et al. (2010) Pannexin1 and Pannexin2 channels show quaternary similarities to connexons and different oligomerization numbers from each other. J Biol Chem 285: 24420-24431. doi:10.1074/jbc.M110.115444. PubMed: 20516070.
32. Bao L, Locovei S, Dahl G, (2004) Pannexin membrane channels are mechanosensitive conduits for ATP. FEBS Lett 572: 65-68. doi:10.1016/j.febslet.2004.07.009. PubMed: 15304325.
33. Gründken C, Hanske J, Wengel S, Reuter W, Abdulazim A, et al. (2011) Unified patch clamp protocol for the characterization of Pannexin 1 channels in isolated cells and acute brain slices. J Neurosci Methods 199: 15-25. doi:10.1016/j.jneumeth.2011.04.016. PubMed: 21549752.
34. Vroman R, Klaassen L, Howlett M, Klooster J, Sjoerdsma T, et al. (2013) Extracellular ATP hydrolysis inhibits synaptic transmission by increasing pH buffering in the synaptic cleft. In press.
35. Laird DW, (2006) Life cycle of connexins in health and disease. Biochem J 394: 527-543. doi:10.1042/BJ20051922. PubMed: 16492141.
36. Martin PE, Blundell G, Ahmad S, Errington RJ, Evans WH, (2001) Multiple pathways in the trafficking and assembly of connexin 26, 32 and 43 into gap junction intercellular communication channels. J Cell Sci 114: 3845-3855. PubMed: 11719551.
37. Vanden Abeele F, Bidaux G, Gordienko D, Beck B, Panchin YV, et al. (2006) Functional implications of calcium permeability of the channel formed by pannexin 1. J Cell Biol 174: 535-546. doi:10.1083/jcb.200601115. PubMed: 16908669.
38. Kienitz MC, Bender K, Dermietzel R, Pott L, Zoidl G, (2011) Pannexin 1 constitutes the large conductance cation channel of cardiac myocytes. J Biol Chem 286: 290-298. doi:10.1074/jbc.M110.163477. PubMed: 21041301.
39. Locovei S, Bao L, Dahl G, (2006) Pannexin 1 in erythrocytes: function without a gap. Proc Natl Acad Sci U S A 103: 7655-7659. doi:10.1073/pnas.0601037103. PubMed: 16682648.
40. Huang YJ, Maruyama Y, Dvoryanchikov G, Pereira E, Chaudhari N, et al. (2007) 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: 6436-6441. doi:10.1073/pnas.0611280104. PubMed: 17389364.
41. Nottingham S, Leiter JC, Wages P, Buhay S, Erlichman JS, (2001) Developmental changes in intracellular pH regulation in medullary neurons of the rat. Am J Physiol Regul, Integr Comp Physiol 281: R1940-R1951. PubMed: 11705781.
42. Xiong ZQ, Stringer JL, (2000) Extracellular pH responses in CA1 and the dentate gyrus during electrical stimulation, seizure discharges, and spreading depression. J Neurophysiol 83: 3519-3524. PubMed: 10848567.
43. Bonnet U, Bingmann D, Wiemann M, (2000) Intracellular pH modulates spontaneous and epileptiform bioelectric activity of hippocampal CA3-neurones. Eur Neuropsychopharmacol 10: 97-103. doi:10.1016/S0924-977X(99)00063-2. PubMed: 10706990.
44. Hirasawa H, Kaneko A, (2003) pH changes in the invaginating synaptic cleft mediate feedback from horizontal cells to cone photoreceptors by modulating Ca2+ channels. J Gen Physiol 122: 657-671. doi:10.1085/jgp.200308863. PubMed: 14610018.
45. Fahrenfort I, Steijaert M, Sjoerdsma T, Vickers E, Ripps H, et al. (2009) Hemichannel-mediated and pH-based feedback from horizontal cells to cones in the vertebrate retina. PLOS ONE 4: e6090. doi:10.1371/journal.pone.0006090. PubMed: 19564917.
46. Dmitriev AV, Mangel SC, (2001) Circadian clock regulation of pH in the rabbit retina. J Neurosci 21: 2897-2902. PubMed: 11306641.
47. Inamura K, Smith ML, Hansen AJ, Siesjö BK, (1989) Seizure-induced damage to substantia nigra and globus pallidus is accompanied by pronounced intra- and extracellular acidosis. J Cereb Blood Flow Metab 9: 821-829. doi:10.1038/jcbfm.1989.116. PubMed: 2584276.
48. Thompson RJ, Jackson MF, Olah ME, Rungta RL, Hines DJ, et al. (2008) Activation of pannexin-1 hemichannels augments aberrant bursting in the hippocampus. Science (New York, NY) 322: 1555-1559. doi:10.1126/science.1165209. PubMed: 19056988.
49. Bargiotas P, Krenz A, Monyer H, Schwaninger M, (2012) Functional outcome of pannexin-deficient mice after cerebral ischemia. Channels (Austin, Tex) 6: 453-456. doi:10.4161/chan.22315. PubMed: 23111424.
50. Gulbransen BD, Bashashati M, Hirota SA, Gui X, Roberts JA, et al. (2012) Activation of neuronal P2X7 receptor-pannexin-1 mediates death of enteric neurons during colitis. Nat Med 18: 600-604. doi:10.1038/nm.2679. PubMed: 22426419.
51. Alberto AVP, Faria RX, Couto CGC, Ferreira LGB, Souza CAM, et al. (2013) Is pannexin the pore associated with the P2X7 receptor? Naunyn Schmiedebergs Arch Pharmacol, 386: 775-87. doi:10.1007/s00210-013-0868-x. PubMed: 23657251.
52. Qiu F, Wang J, Dahl G, (2012) Alanine substitution scanning of pannexin1 reveals amino acid residues mediating ATP sensitivity. Purinergic Signal 8: 81-90. doi:10.1007/s11302-011-9263-6. PubMed: 21987098.
53. Kraaij DA, Spekreijse H, Kamermans M, (2000) The nature of surround-induced depolarizing responses in goldfish cones. J Gen Physiol 115: 3-16. PubMed: 10613914.