Patterns of heterogeneous expression of pannexin 1 and pannexin 2 transcripts in the olfactory epithelium and olfactory bulb

Journal of Molecular Histology

Volumn 43, Issue 6, 2012, Pages 651-660

  Zhang, Honghong ^a   Chen, Youting ^b   Zhang, Chunbo ^a  

^a Illinois Institute of Technology   (United States)

^b XUZHOU MEDICAL UNIVERSITY   (China)

Author keywords

Gap junction; In situ hybridization; Neuron; Olfactory bulb; Olfactory epithelium; Pannexin

Indexed keywords

GAP JUNCTION PROTEIN; MESSENGER RNA; PANNEXIN 1; PANNEXIN 2; UNCLASSIFIED DRUG; NERVE PROTEIN; PANX1 PROTEIN, MOUSE; PANX2 PROTEIN, MOUSE;

ADULT ANIMAL; ANIMAL TISSUE; ARTICLE; BASAL CELL; CONTROLLED STUDY; GENE EXPRESSION; GRANULE CELL; IN SITU HYBRIDIZATION; MALE; MITRAL CELL; MOUSE; NERVE CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; OLFACTORY BULB; OLFACTORY EPITHELIUM; PERIGLOMERULAR CELL; PRIORITY JOURNAL; TISSUE DISTRIBUTION; TUFTED CELL; ANIMAL; GENETICS; METABOLISM;

MUS;

ANIMALS; CONNEXINS; IN SITU HYBRIDIZATION; MALE; MICE; NERVE TISSUE PROTEINS; OLFACTORY BULB; OLFACTORY MUCOSA;

EID: 84877120228     PISSN: 15672379     EISSN: 15672387     Source Type: Journal    
DOI: 10.1007/s10735-012-9443-x     Document Type: Article

References (50)

1. 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
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. doi: 10.1016/j.ygeno.2003.09.025 (Pubitemid 38340811)
3. 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 (Pubitemid 43752506)
4. 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
5. 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 (Pubitemid 37444793)
6. 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 (Pubitemid 47100188)
7. Christie JM, Westbrook GL (2006) Lateral excitation within the olfactory bulb. J Neurosci 26:2269-2277. doi: 10.1523/JNEUROSCI.4791-05.2006 (Pubitemid 44699036)
8. 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 (Pubitemid 40733131)
9. 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 (Pubitemid 46089967)
10. 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
11. 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 (Pubitemid 41746346)
12. 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
13. 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 (Pubitemid 40104636)
14. 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 (Pubitemid 41292114)
15. Hegg CC, Greenwood D, Huang W, Han P, Lucero MT (2003) Activation of purinergic receptor subtypes modulates odor sensitivity. J Neurosci 23:8291-8301 (Pubitemid 37129646)
16. 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
17. 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 (Pubitemid 47186112)
18. 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 (Pubitemid 40799295)
19. 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
20. 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 (Pubitemid 47302430)
21. 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 (Pubitemid 46177288)
22. 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
23. 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
24. 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 (Pubitemid 28127830)
25. 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 (Pubitemid 41133380)
26. 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
27. 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
28. 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
29. Panchin YV (2005) Evolution of gap junction proteins - the pannexin alternative. J Exp Biol 208:1415-1419. doi: 10.1242/jeb.01547 (Pubitemid 40697529)
30. 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 (Pubitemid 30466927)
31. 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 (Pubitemid 350187359)
32. 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
33. 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
34. 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 (Pubitemid 44078241)
35. 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
36. 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
37. 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 (Pubitemid 351594228)
38. Schoppa NE, Westbrook GL (2002) AMPA autoreceptors drive correlated spiking in olfactory bulb glomeruli. Nat Neurosci 5:1194-1202. doi: 10.1038/nn953 (Pubitemid 35247179)
39. 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 (Pubitemid 38496536)
40. 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
41. 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 (Pubitemid 32695231)
42. 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 (Pubitemid 37244100)
43. 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
44. 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
45. 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 (Pubitemid 46782985)
46. Zhang C (2010) Gap junctions in olfactory neurons modulate olfactory sensitivity. BMC Neurosci 11:108. doi: 10.1186/1471-2202-11-108
47. 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
48. 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 (Pubitemid 34168195)
49. 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 (Pubitemid 36438289)
50. 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