Abstract
Pannexins form membrane channels that release biological signals to communicate with neighboring cells. Here, we report expression patterns of pannexin 1 (Panx1) and pannexin 2 (Panx2) in the olfactory epithelium and olfactory bulb of adult mice. In situ hybridization revealed that mRNAs for Panx1 and Panx2 were both expressed in the olfactory epithelium and olfactory bulb. Expression of Panx1 and Panx2 was mainly found in cell bodies below the sustentacular cell layer in the olfactory epithelium, indicating that Panx1 and Panx2 are expressed in mature and immature olfactory neurons, and basal cells. Expression of Panx2 was observed in sustentacular cells in a few locations of the olfactory epithelium. In the olfactory bulb, Panx1 and Panx2 were expressed in spatial patterns. Many mitral cells, tufted cells, periglomerular cells and granule cells were Panx1 and Panx2 positive. Mitral cells located at the dorsal and lateral portions of the olfactory bulb showed weak Panx1 expression compared with those in the medial side. However, the opposite was true for the distribution of Panx2 positive mitral cells. There were more Panx2 mRNA positive mitral cells and granule cells compared to those expressing Panx1. Our findings on pannexin expression in the olfactory system of adult mice raise the novel possibility that pannexins play a role in information processing in the olfactory system. Demonstration of expression patterns of pannexins in the olfactory system provides an anatomical basis for future functional studies.
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References
Ambrosi C, Gassmann O, Pranskevich JN, Boassa D, Smock A, Wang J, Dahl G, Steinem C, Sosinsky GE (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
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. doi:10.1016/j.ygeno.2003.09.025
Barbe MT, Monyer H, Bruzzone R (2006) Cell-cell communication beyond connexins: the pannexin channels. Physiology (Bethesda) 21:103–114. doi:10.1152/physiol.00048.2005
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
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. doi:10.1073/pnas.2233464100
Bush CF, Jones SV, Lyle AN, Minneman KP, Ressler KJ, Hall RA (2007) Specificity of olfactory receptor interactions with other G protein-coupled receptors. J Biol Chem 282:19042–19051. doi:10.1074/jbc.M610781200
Christie JM, Westbrook GL (2006) Lateral excitation within the olfactory bulb. J Neurosci 26:2269–2277. doi:10.1523/JNEUROSCI.4791-05.2006
Christie JM, Bark C, Hormuzdi SG, Helbig I, Monyer H, Westbrook GL (2005) Connexin36 mediates spike synchrony in olfactory bulb glomeruli. Neuron 46:761–772. doi:10.1016/j.neuron.2005.04.030
De Saint JD, Westbrook GL (2007) Disynaptic amplification of metabotropic glutamate receptor 1 responses in the olfactory bulb. J Neurosci 27:132–140. doi:10.1523/JNEUROSCI.2439-06.2007
D’hondt C, Ponsaerts R, De SH, Vinken M, De VE, De BM, Wang N, Rogiers V, Leybaert L, Himpens B, Bultynck G (2011) Pannexin channels in ATP release and beyond: an unexpected rendezvous at the endoplasmic reticulum. Cell Signal 23:305–316. doi:10.1016/j.cellsig.2010.07.018
Finger TE, Danilova V, Barrows J, Bartel DL, Vigers AJ, Stone L, Hellekant G, Kinnamon SC (2005) ATP signaling is crucial for communication from taste buds to gustatory nerves. Science 310:1495–1499. doi:10.1126/science.1118435
Fischer T, Rotermund N, Lohr C, Hirnet D (2012) P2Y(1) receptor activation by photolysis of caged ATP enhances neuronal network activity in the developing olfactory bulb. Purinergic Signal 8:191–198. doi:10.1007/s11302-011-9286-z
Gayle S, Burnstock G (2005) Immunolocalisation of P2X and P2Y nucleotide receptors in the rat nasal mucosa. Cell Tissue Res 319:27–36. doi:10.1007/s00441-004-0979-2
Hayar A, Shipley MT, Ennis M (2005) Olfactory bulb external tufted cells are synchronized by multiple intraglomerular mechanisms. J Neurosci 25:8197–8208. doi:10.1523/JNEUROSCI.2374-05.2005
Hegg CC, Greenwood D, Huang W, Han P, Lucero MT (2003) Activation of purinergic receptor subtypes modulates odor sensitivity. J Neurosci 23:8291–8301
Huang YA, Roper SD (2010) Intracellular Ca(2 +) and TRPM5-mediated membrane depolarization produce ATP secretion from taste receptor cells. J Physiol 588:2343–2350. doi:10.1113/jphysiol.2010.191106
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. doi:10.1073/pnas.0611280104
Jiang JX, Gu S (2005) Gap junction- and hemichannel-independent actions of connexins. Biochim Biophys Acta 1711:208–214. doi:10.1016/j.bbamem.2004.10.001
Kiyokage E, Pan YZ, Shao Z, Kobayashi K, Szabo G, Yanagawa Y, Obata K, Okano H, Toida K, Puche AC, Shipley MT (2010) Molecular identity of periglomerular and short axon cells. J Neurosci 30:1185–1196. doi:10.1523/JNEUROSCI.3479-09.2010
Kosaka K, Kosaka T (2007a) Chemical properties of type 1 and type 2 periglomerular cells in the mouse olfactory bulb are different from those in the rat olfactory bulb. Brain Res 1167:42–55. doi:10.1016/j.brainres.2007.04.087
Kosaka T, Kosaka K (2007b) Heterogeneity of nitric oxide synthase-containing neurons in the mouse main olfactory bulb. Neurosci Res 57:165–178. doi:10.1016/j.neures.2006.10.005
Kosaka T, Kosaka K (2008) Tyrosine hydroxylase-positive GABAergic juxtaglomerular neurons are the main source of the interglomerular connections in the mouse main olfactory bulb. Neurosci Res 60:349–354. doi:10.1016/j.neures.2007.11.012
Kosaka T, Kosaka K (2012) Further characterization of the juxtaglomerular neurons in the mouse main olfactory bulb by transcription factors, Sp8 and Tbx21. Neurosci Res 73:24–31. doi:10.1016/j.neures.2012.02.013
Kosaka K, Toida K, Aika Y, Kosaka T (1998) How simple is the organization of the olfactory glomerulus? the heterogeneity of so-called periglomerular cells. Neurosci Res 30:101–110. doi:10.1016/S0168-0102(98)00002-9
Kosaka T, Deans MR, Paul DL, Kosaka K (2005) Neuronal gap junctions in the mouse main olfactory bulb: morphological analyses on transgenic mice. Neuroscience 134:757–769. doi:10.1016/j.neuroscience.2005.04.057
Miragall F, Hwang TK, Traub O, Hertzberg EL, Dermietzel R (1992) Expression of connexins in the developing olfactory system of the mouse. J Comp Neurol 325:359–378
Miragall F, Traub O, Dermietzel R (1996) Gap junction expression in the olfactory system. In: Spray DC, Dermietzel R (eds) Gap junctions in the nervous system. R.G. Landes Co, New York, pp 243–260
Mulder J, Zilberter M, Spence L, Tortoriello G, Uhlen M, Yanagawa Y, Aujard F, Hokfelt T, Harkany T (2009) Secretagogin is a Ca2+-binding protein specifying subpopulations of telencephalic neurons. Proc Natl Acad Sci USA 106:22492–22497. doi:10.1073/pnas.0912484106
Panchin YV (2005) Evolution of gap junction proteins—the pannexin alternative. J Exp Biol 208:1415–1419. doi:10.1242/jeb.01547
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–R474. doi:10.1016/S0960-9822(00)00576-5
Penuela S, Bhalla R, Gong XQ, Cowan KN, Celetti SJ, Cowan BJ, Bai D, Shao Q, Laird DW (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
Penuela S, Celetti SJ, Bhalla R, Shao Q, Laird DW (2008) Diverse subcellular distribution profiles of pannexin 1 and pannexin 3. Cell Commun Adhes 15:133–142. doi:10.1080/15419060802014115
Plachez C, Puche AC (2012) Early specification of GAD67 subventricular derived olfactory interneurons. J Mol Histol 43:215–221. doi:10.1007/s10735-012-9394-2
Rash JE, Davidson KG, Kamasawa N, Yasumura T, Kamasawa M, Zhang C, Michaels R, Restrepo D, Ottersen OP, Olson CO, Nagy JI (2005) Ultrastructural localization of connexins (Cx36, Cx43, Cx45), glutamate receptors and aquaporin-4 in rodent olfactory mucosa, olfactory nerve and olfactory bulb. J Neurocytol 34:307–341. doi:10.1007/s11068-005-8360-2
Rela L, Bordey A, Greer CA (2010) Olfactory ensheathing cell membrane properties are shaped by connectivity. Glia 58:665–678. doi:10.1002/glia.20953
Romanov RA, Rogachevskaja OA, Bystrova MF, Jiang P, Margolskee RF, Kolesnikov SS (2007) Afferent neurotransmission mediated by hemichannels in mammalian taste cells. EMBO J 26:657–667. doi:10.1038/sj.emboj.7601526
Scemes E, Suadicani SO, Dahl G, Spray DC (2007) Connexin and pannexin mediated cell–cell communication. Neuron Glia Biol 3:199–208. doi:10.1017/S1740925X08000069
Schoppa NE, Westbrook GL (2002) AMPA autoreceptors drive correlated spiking in olfactory bulb glomeruli. Nat Neurosci 5:1194–1202. doi:10.1038/nn953
Sohl G, Willecke K (2004) Gap junctions and the connexin protein family. Cardiovasc Res 62:228–232. doi:10.1016/j.cardiores.2003.11.013
Sosinsky GE, Boassa D, Dermietzel R, Duffy HS, Laird DW, MacVicar B, Naus CC, Penuela S, Scemes E, Spray DC, Thompson RJ, Zhao HB, Dahl G (2011) Pannexin channels are not gap junction hemichannels. Channels (Austin) 5:193–197. doi:10.4161/chan.5.3.15765
Steward O, Schuman EM (2001) Protein synthesis at synaptic sites on dendrites. Annu Rev Neurosci 24:299–325. doi:10.1146/annurev.neuro.24.1.299
Steward O, Schuman EM (2003) Compartmentalized synthesis and degradation of proteins in neurons. Neuron 40:347–359. doi:10.1016/S0896-6273(03)00635-4
Swayne LA, Sorbara CD, Bennett SA (2010) Pannexin 2 is expressed by postnatal hippocampal neural progenitors and modulates neuronal commitment. J Biol Chem 285:24977–24986. doi:10.1074/jbc.M110.130054
Thompson RJ, MacVicar BA (2008) Connexin and pannexin hemichannels of neurons and astrocytes. Channels (Austin) 2:81–86. doi:10.4161/chan.2.2.6003
Yen MR, Saier MH Jr (2007) Gap junctional proteins of animals: the innexin/pannexin superfamily. Prog Biophys Mol Biol 94:5–14. doi:10.1016/j.pbiomolbio.2007.03.006
Zhang C (2010) Gap junctions in olfactory neurons modulate olfactory sensitivity. BMC Neurosci 11:108. doi:10.1186/1471-2202-11-108
Zhang C (2011) Expression of connexin 57 in the olfactory epithelium and olfactory bulb. Neurosci Res 71:226–234. doi:10.1016/j.neures.2011.07.1832
Zhang C, Restrepo D (2002) Expression of connexin 45 in the olfactory system. Brain Res 929:37–47. doi:10.1016/S0006-8993(01)03372-8
Zhang C, Restrepo D (2003) Heterogeneous expression of connexin 36 in the olfactory epithelium and glomerular layer of the olfactory bulb. J Comp Neurol 459:426–439. doi:10.1002/cne.10617
Zhang C, Finger TE, Restrepo D (2000) Mature olfactory receptor neurons express connexin 43. J Comp Neurol 426:1–12. doi:10.1002/1096-9861(20001009
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Zhang, H., Chen, Y. & Zhang, C. Patterns of heterogeneous expression of pannexin 1 and pannexin 2 transcripts in the olfactory epithelium and olfactory bulb. J Mol Hist 43, 651–660 (2012). https://doi.org/10.1007/s10735-012-9443-x
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DOI: https://doi.org/10.1007/s10735-012-9443-x