Gap junctions in olfactory neurons modulate olfactory sensitivity

BMC Neuroscience

Volumn 11, Issue , 2010, Pages

  Zhang, Chunbo ^a  

^a Illinois Institute of Technology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDASE; CONNEXIN 43; MESSENGER RNA; PROTEIN C FOS; CALCIUM; ELONGATION FACTOR 1; GAP JUNCTION PROTEIN;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GAP JUNCTION; JUXTAGLOMERULAR CELL; MOUSE; NONHUMAN; OLFACTORY BULB; OLFACTORY DISCRIMINATION; OLFACTORY NERVE; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; STIMULUS RESPONSE; TRANSGENIC MOUSE; WILD TYPE; ANIMAL; BIOSYNTHESIS; BRAIN MAPPING; C57BL MOUSE; CELL JUNCTION; CELL MEMBRANE; ELECTROPHYSIOLOGY; GENETICS; HUMAN; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; METABOLISM; ODOR; OLFACTORY EPITHELIUM; OLFACTORY RECEPTOR; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANIMALS; BETA-GALACTOSIDASE; BLOTTING, WESTERN; BRAIN MAPPING; CALCIUM; CELL MEMBRANE; CONNEXIN 43; CONNEXINS; ELECTROPHYSIOLOGY; GAP JUNCTIONS; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; ODORS; OLFACTORY MUCOSA; OLFACTORY RECEPTOR NEURONS; PEPTIDE ELONGATION FACTOR 1; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SMELL;

EID: 77957106734     PISSN: None     EISSN: 14712202     Source Type: Journal    
DOI: 10.1186/1471-2202-11-108     Document Type: Article

References (92)

1. Buck LB. The molecular architecture of odor and pheromone sensing in mammals. Cell 2000, 100:611-618. 10.1016/S0092-8674(00)80698-4, 10761927.
2. Mombaerts P. Molecular biology of odorant receptors in vertebrates. Annual Review of Neuroscience 1999, 22:487-509. 10.1146/annurev.neuro.22.1.487, 10202546.
3. Wachowiak M, Cohen LB. Representation of odorants by receptor neuron input to the mouse olfactory bulb. Neuron 2001, 32:723-735. 10.1016/S0896-6273(01)00506-2, 11719211.
4. Bozza T, McGann JP, Mombaerts P, Wachowiak M. In vivo imaging of neuronal activity by targeted expression of a genetically encoded probe in the mouse. Neuron 2004, 42:9-21. 10.1016/S0896-6273(04)00144-8, 15066261.
5. Spors H, Wachowiak M, Cohen LB, Friedrich RW. Temporal dynamics and latency patterns of receptor neuron input to the olfactory bulb. J Neurosci 2006, 26:1247-1259. 10.1523/JNEUROSCI.3100-05.2006, 16436612.
6. De Saint JD, Westbrook GL. Disynaptic amplification of metabotropic glutamate receptor 1 responses in the olfactory bulb. J Neurosci 2007, 27:132-140. 10.1523/JNEUROSCI.2439-06.2007, 17202480.
7. Firestein S, Picco C, Menini A. The relation between stimulus and response in olfactory receptor cells of the tiger salamander. J Physiol (Lond) 1993, 468:1-10. 1143811, 8254501.
8. Reisert J, Matthews HR. Response properties of isolated mouse olfactory receptor cells. J Physiol 2001, 530:113-122. 10.1111/j.1469-7793.2001.0113m.x, 2278387, 11136863.
9. Ma M, Chen WR, Shepherd GM. Electrophysiological characterization of rat and mouse olfactory receptor neurons from an intact epithelial preparation. J Neurosci Methods 1999, 92:31-40. 10.1016/S0165-0270(99)00089-8, 10595701.
10. Grosmaitre X, Vassalli A, Mombaerts P, Shepherd GM, Ma M. Odorant responses of olfactory sensory neurons expressing the odorant receptor MOR23: a patch clamp analysis in gene-targeted mice. Proc Natl Acad Sci USA 2006, 103:1970-1975. 10.1073/pnas.0508491103, 1413638, 16446455.
11. Duchamp-Viret P, Duchamp A, Chaput MA. Peripheral odor coding in the rat and frog: Quality and intensity specification. J Neurosci 2000, 20:2383-2390.
12. Dermietzel R. Gap junction wiring: a 'new' principle in cell-to-cell communication in the nervous system?. Brain Res Brain Res Rev 1998, 26:176-183. 10.1016/S0165-0173(97)00031-3, 9651521.
13. Lynch JW, Barry PH. Action potentials initiated by single channels opening in a small neuron (rat olfactory receptor). Biophys J 1989, 55:755-768. 10.1016/S0006-3495(89)82874-7, 1330559, 2470428.
14. Maue RA, Dionne VE. Patch-clamp studies of isolated mouse olfactory receptor neurons. J Gen Physiol 1987, 90:95-125. 10.1085/jgp.90.1.95, 2228861, 2442298.
15. Spray DC. Physiological properties of gap junction channels in the nervous system. Gap Junction in the Nervous System 1996, 39-58. R. G. Landes Company, Spray DC, Dermietzel R.
16. Maxeiner S, Dedek K, Janssen-Bienhold U, Ammermuller J, Brune H, Kirsch T, Pieper M, Degen J, Kruger O, Willecke K, et al. Deletion of connexin45 in mouse retinal neurons disrupts the rod/cone signaling pathway between AII amacrine and ON cone bipolar cells and leads to impaired visual transmission. J Neurosci 2005, 25:566-576. 10.1523/JNEUROSCI.3232-04.2005, 15659592.
17. Deans MR, Volgyi B, Goodenough DA, Bloomfield SA, Paul DL. Connexin36 is essential for transmission of rod-mediated visual signals in the mammalian retina. Neuron 2002, 36:703-712. 10.1016/S0896-6273(02)01046-2, 2834592, 12441058.
18. Shelley J, Dedek K, Schubert T, Feigenspan A, Schultz K, Hombach S, Willecke K, Weiler R. Horizontal cell receptive fields are reduced in connexin57-deficient mice. Eur J Neurosci 2006, 23:3176-3186. 10.1111/j.1460-9568.2006.04848.x, 16820008.
19. Schubert T, Maxeiner S, Kruger O, Willecke K, Weiler R. Connexin45 mediates gap junctional coupling of bistratified ganglion cells in the mouse retina. J Comp Neurol 2005, 490:29-39. 10.1002/cne.20621, 16041717.
20. Christie JM, Westbrook GL. Lateral excitation within the olfactory bulb. J Neurosci 2006, 26:2269-2277. 10.1523/JNEUROSCI.4791-05.2006, 16495454.
21. Christie JM, Bark C, Hormuzdi SG, Helbig I, Monyer H, Westbrook GL. Connexin36 mediates spike synchrony in olfactory bulb glomeruli. Neuron 2005, 46:761-772. 10.1016/j.neuron.2005.04.030, 15924862.
22. Schoppa NE, Westbrook GL. AMPA autoreceptors drive correlated spiking in olfactory bulb glomeruli. Nat Neurosci 2002, 5:1194-1202. 10.1038/nn953, 12379859.
23. Zhang C, Finger TE, Restrepo D. Mature olfactory receptor neurons express connexin 43. J Comp Neurol 2000, 426:1-12. 10.1002/1096-9861(20001009)426:1<1::AID-CNE1>3.0.CO;2-Y, 10980480.
24. Zhang C, Restrepo D. Heterogeneous expression of connexin 36 in the olfactory epithelium and glomerular layer of the olfactory bulb. J Comp Neurol 2003, 459:426-439. 10.1002/cne.10617, 12687708.
25. Zhang C. Expression of connexin 57 in the olfactory system in mice [abstract]. Chem Senses 2008, 33:S60.
26. Zhang C, Restrepo D. Expression of connexin 45 in the olfactory system. Brain Res 2002, 929:37-47. 10.1016/S0006-8993(01)03372-8, 11852029.
27. Rash JE, Davidson KG, Kamasawa N, Yasumura T, Kamasawa M, Zhang C, Michaels R, Restrepo D, Ottersen OP, Olson CO, et al. Ultrastructural localization of connexins (Cx36, Cx43, Cx45), glutamate receptors and aquaporin-4 in rodent olfactory mucosa, olfactory nerve and olfactory bulb. J Neurocytol 2005, 34:307-341. 10.1007/s11068-005-8360-2, 1525003, 16841170.
28. Sullivan R, Huang GY, Meyer RA, Wessels A, Linask KK, Lo CW. Heart malformations in transgenic mice exhibiting dominant negative inhibition of gap junctional communication in neural crest cells. Dev Biol 1998, 204:224-234. 10.1006/dbio.1998.9089, 9851855.
29. Sullivan R, Lo CW. Expression of a connexin 43/beta-galactosidase fusion protein inhibits gap junctional communication in NIH3T3 cells. J Cell Biol 1995, 130:419-429. 10.1083/jcb.130.2.419, 2199931, 7542247.
30. Das Sarma J, Lo CW, Koval M. Cx43/beta-gal inhibits Cx43 transport in the Golgi apparatus. Cell Adhes Commun 2001, 8:249-252.
31. Das Sarma J, Meyer RA, Wang F, Abraham V, Lo CW, Koval M. Multimeric connexin interactions prior to the trans-Golgi network. J Cell Sci 2001, 114:4013-4024.
32. Graziadei PP, Graziadei GA. Neurogenesis and neuron regeneration in the olfactory system of mammals. I. Morphological aspects of differentiation and structural organization of the olfactory sensory neurons. J Neurocytol 1979, 8:1-18. 10.1007/BF01206454, 438867.
33. Gonzales F, Farbman AI, Gesteland RC. Cell and explant culture of olfactory chemoreceptor cells. J Neurosci Methods 1985, 14:77-90. 10.1016/0165-0270(85)90118-9, 3897728.
34. Margolis FL. A marker protein for the olfactory chemoreceptor neuron. Proteins of the Nervous System 1980, 59-84. New York: Raven Press, Bradshaw RA, Schneider DM.
35. Su T, Ding X. Regulation of the cytochrome P450 2A genes. Toxicol Appl Pharmacol 2004, 199:285-294. 10.1016/j.taap.2003.11.029, 15364544.
36. Piras E, Franzen A, Fernandez EL, Bergstrom U, Raffalli-Mathieu F, Lang M, Brittebo EB. Cell-specific expression of CYP2A5 in the mouse respiratory tract: effects of olfactory toxicants. J Histochem Cytochem 2003, 51:1545-1555.
37. Margolis FL, Verhaagen J, Biffo S, Huang FL, Grillo M. Regulation of gene expression in the olfactory neuroepithelium: a neurogenetic matrix. Prog Brain Res 1991, 89:97-122. full_text, 1839074.
38. Ebrahimi FA, Chess A. Olfactory G proteins: Simple and complex signal transduction. Current Biology 1998, 8:R431-R433. 10.1016/S0960-9822(98)70271-4, 9637917.
39. Jones DT, Reed RR. Golf:an olfactory neuron specific-G protein involved in odorant signal transduction. Science 1989, 244:790-795. 10.1126/science.2499043, 2499043.
40. Araneda RC, Kini AD, Firestein S. The molecular receptive range of an odorant receptor. Nat Neurosci 2000, 3:1248-1255. 10.1038/81774, 11100145.
41. Bozza T, Feinstein P, Zheng C, Mombaerts P. Odorant receptor expression defines functional units in the mouse olfactory system. J Neurosci 2002, 22:3033-3043.
42. Kwak BR, Pepper MS, Gros DB, Meda P. Inhibition of endothelial wound repair by dominant negative connexin inhibitors. Mol Biol Cell 2001, 12:831-845. 32270, 11294890.
43. Getchell TV. Electrogenic sources of slow voltage transients recorded from frog olfactory epithelium. J Neurophysiol 1974, 37:1115-1130.
44. Scott JW, Brierley T, Schmidt FH. Chemical determinants of the rat electro-olfactogram. J Neurosci 2000, 20:4721-4731.
45. Curran-Everett D. Multiple comparisons: philosophies and illustrations. Am J Physiol Regul Integr Comp Physiol 2000, 279:R1-R8.
46. Davidson JS, Baumgarten IM, Harley EH. Reversible inhibition of intercellular junctional communication by glycyrrhetinic acid. Biochem Biophys Res Commun 1986, 134:29-36. 10.1016/0006-291X(86)90522-X, 3947327.
47. Venance L, Premont J, Glowinski J, Giaume C. Gap junctional communication and pahrmacological heterogeneity in astrocytes cultured from the rat striatum. J Physiol 1998, 510:429-440. 10.1111/j.1469-7793.1998.429bk.x, 2231053, 9705994.
48. Salcedo E, Zhang C, Kronberg E, Restrepo D. Analysis of training-induced changes in ethyl acetate odor maps using a new computational tool to map the glomerular layer of the olfactory bulb. Chem Senses 2005, 30:615-626. 10.1093/chemse/bji055, 16141292.
49. Schaefer ML, Young DA, Restrepo D. Olfactory fingerprints for major histocompatibility complex-determined body odors. J Neurosci 2001, 21:2481-2487.
50. White TW, Paul DL. Genetic diseases and gene knockouts reveal diverse connexin functions. Annu Rev Physiol 1999, 61:283-310. 10.1146/annurev.physiol.61.1.283, 10099690.
51. Dobrowolski R, Willecke K. Connexin-caused genetic diseases and corresponding mouse models. Antioxid Redox Signal 2009, 11:283-295. 10.1089/ars.2008.2128, 18831677.
52. Desplantez T, Halliday D, Dupont E, Weingart R. Cardiac connexins Cx43 and Cx45: formation of diverse gap junction channels with diverse electrical properties. Pflugers Arch 2004, 448:363-375. 10.1007/s00424-004-1250-0, 15048573.
53. Elenes S, Martinez AD, Delmar M, Beyer EC, Moreno AP. Heterotypic docking of Cx43 and Cx45 connexons blocks fast voltage gating of Cx43. Biophys J 2001, 81:1406-1418. 10.1016/S0006-3495(01)75796-7, 1301620, 11509355.
54. Gong X, Li E, Klier G, Huang Q, Wu Y, Lei H, Kumar NM, Horwitz J, Gilula NB. Disruption of alpha3 connexin gene leads to proteolysis and cataractogenesis in mice. Cell 1997, 91:833-843. 10.1016/S0092-8674(00)80471-7, 9413992.
55. Miragall F, Hwang TK, Traub O, Hertzberg EL, Dermietzel R. Expression of connexins in the developing olfactory system of the mouse. J Comp Neurol 1992, 325:359-378. 10.1002/cne.903250304, 1332989.
56. Delay RJ, Dionne VE. Coupling between Sensory Neurons in the Olfactory Epithelium. Chem Senses 2003, 28:807-815. 10.1093/chemse/bjg074, 14654449.
57. Deans MR, Gibson JR, Sellitto C, Connors BW, Paul DL. Synchronous activity of inhibitory networks in neocortex requires electrical synapses containing connexin36. Neuron 2001, 31:477-485. 10.1016/S0896-6273(01)00373-7, 11516403.
58. Buntinas L, Zhang C, Restrepo D. Biophysical model of olfactory receptor neuron pairs reveals mechanism for gap junction mediated synchronized firing at threshold odor concentrations [abstract]. Chem Senses 2005, 30:A83-A84.
59. Alexander DB, Goldberg GS. Transfer of biologically important molecules between cells through gap junction channels. Curr Med Chem 2003, 10:2045-2058. 10.2174/0929867033456927, 12871102.
60. Veenstra RD, Wang HZ, Beblo DA, Chilton MG, Harris AL, Beyer EC, Brink PR. Selectivity of connexin-specific gap junctions does not correlate with channel conductance. Circ Res 1995, 77:1156-1165.
61. Harris AL. Connexin channel permeability to cytoplasmic molecules. Prog Biophys Mol Biol 2007, 94:120-143. 10.1016/j.pbiomolbio.2007.03.011, 1995164, 17470375.
62. Goldberg GS, Valiunas V, Brink PR. Selective permeability of gap junction channels. Biochim Biophys Acta 2004, 1662:96-101. 10.1016/j.bbamem.2003.11.022, 15033581.
63. Spray DC, Ye ZC, Ransom BR. Functional connexin "hemichannels": a critical appraisal. Glia 2006, 54:758-773. 10.1002/glia.20429, 17006904.
64. Bargiotas P, Monyer H, Schwaninger M. Hemichannels in cerebral ischemia. Curr Mol Med 2009, 9:186-194. 10.2174/156652409787581646, 19275626.
65. Orellana JA, Saez PJ, Shoji KF, Schalper KA, Palacios-Prado N, Velarde V, Giaume C, Bennett MV, Saez JC. Modulation of brain hemichannels and gap junction channels by pro-inflammatory agents and their possible role in neurodegeneration. Antioxid Redox Signal 2009, 11:369-399. 10.1089/ars.2008.2130, 2713807, 18816186.
66. Gaietta G, Deerinck TJ, Adams SR, Bouwer J, Tour O, Laird DW, Sosinsky GE, Tsien RY, Ellisman MH. Multicolor and electron microscopic imaging of connexin trafficking. Science 2002, 296:503-507. 10.1126/science.1068793, 11964472.
67. Valiunas V, Bukauskas FF, Weingart R. Conductances and selective permeability of connexin43 gap junction channels examined in neonatal rat heart cells. Circ Res 1997, 80:708-719.
68. Burra S, Jiang JX. Connexin 43 hemichannel opening associated with Prostaglandin E(2) release is adaptively regulated by mechanical stimulation. Commun Integr Biol 2009, 2:239-240. 10.4161/cib.2.3.8154, 2717532, 19641742.
69. Siller-Jackson AJ, Burra S, Gu S, Xia X, Bonewald LF, Sprague E, Jiang JX. Adaptation of connexin 43-hemichannel prostaglandin release to mechanical loading. J Biol Chem 2008, 283:26374-26382. 10.1074/jbc.M803136200, 2546557, 18676366.
70. Hawat G, Baroudi G. Differential modulation of unapposed connexin 43 hemichannel electrical conductance by protein kinase C isoforms. Pflugers Arch 2008, 456:519-527. 10.1007/s00424-007-0426-9, 18172602.
71. Ramachandran S, Xie LH, John SA, Subramaniam S, Lal R. A novel role for connexin hemichannel in oxidative stress and smoking-induced cell injury. PLoS One 2007, 2:e712. 10.1371/journal.pone.0000712, 1933596, 17684558.
72. DeVries SH, Schwartz EA. Hemi-gap-junction channels in solitary horizontal cells of the catfish retina. J Physiol 1992, 445:201-230. 1179978, 1380084.
73. Fahrenfort I, Steijaert M, Sjoerdsma T, Vickers E, Ripps H, van AJ, Endeman D, Klooster J, Numan R, ten EH, et al. Hemichannel-mediated and pH-based feedback from horizontal cells to cones in the vertebrate retina. PLoS One 2009, 4:e6090. 10.1371/journal.pone.0006090, 2699542, 19564917.
74. Kamermans M, Fahrenfort I, Schultz K, Janssen-Bienhold U, Sjoerdsma T, Weiler R. Hemichannel-mediated inhibition in the outer retina. Science 2001, 292:1178-1180. 10.1126/science.1060101, 11349152.
75. Dando R, Roper SD. Cell-to-cell communication in taste buds through ATP signaling from pannexin 1 gap junction hemichannels. J Physiol 2009, 587:5899-5906.
76. Huang YJ, Maruyama Y, Dvoryanchikov G, Pereira E, Chaudhari N, Roper SD. The role of pannexin 1 hemichannels in ATP release and cell-cell communication in mouse taste buds. Proc Natl Acad Sci USA 2007, 104:6436-6441. 10.1073/pnas.0611280104, 1851090, 17389364.
77. Hegg CC, Greenwood D, Huang W, Han P, Lucero MT. Activation of purinergic receptor subtypes modulates odor sensitivity. J Neurosci 2003, 23:8291-8301.
78. Simoes-de-Souza FM, Roque AC. A biophysical model of vertebrate olfactory epithelium and bulb exhibiting gap junction dependent odor-evoked spatiotemporal patterns of activity. BioSystems 2004, 73:25-43. 10.1016/j.biosystems.2003.08.002, 14729280.
79. Nagao H, Yamaguchi M, Takahash Y, Mori K. Grouping and representation of odorant receptors in domains of the olfactory bulb sensory map. Microsc Res Tech 2002, 58:168-175. 10.1002/jemt.10146, 12203695.
80. Rubin BD, Katz LC. Optical imaging of odorant representations in the mammalian olfactory bulb. Neuron 1999, 23:499-511. 10.1016/S0896-6273(00)80803-X, 10433262.
81. Johnson BA, Leon M. Chemotopic odorant coding in a mammalian olfactory system. J Comp Neurol 2007, 503:1-34. 10.1002/cne.21396, 2213457, 17480025.
82. Leon M, Johnson BA. Olfactory coding in the mammalian olfactory bulb. Brain Res Brain Res Rev 2003, 42:23-32. 10.1016/S0165-0173(03)00142-5, 12668289.
83. Xu FQ, Greer CA, Shepherd GM. Odor maps in the olfactory bulb. J Comp Neurol 2000, 422:489-495. 10.1002/1096-9861(20000710)422:4<489::AID-CNE1>3.0.CO;2-#, 10861521.
84. Friedrich RW. Real time odor representations. Trends Neurosci 2002, 25:487-489. 10.1016/S0166-2236(02)02256-7, 12220868.
85. Laurent G. Olfactory network dynamics and the coding of multidimensional signals. Nat Rev Neurosci 2002, 3:884-895. 10.1038/nrn964, 12415296.
86. Walters E, Grillo M, Tarozzo G, Stein-Izsak C, Corbin J, Bocchiaro C, Margolis FL. Proximal regions of the olfactory marker protein gene promoter direct olfactory neuron-specific expression in transgenic mice. J Neurosci Res 1996, 43:146-160. 10.1002/(SICI)1097-4547(19960115)43:2<146::AID-JNR3>3.0.CO;2-G, 8820963.
87. Danciger E, Mettling C, Vidal M, Morris R, Margolis F. Olfactory marker protein gene: its structure and olfactory neuron-specific expression in transgenic mice. Proc Natl Acad Sci USA 1989, 86:8565-8569. 10.1073/pnas.86.21.8565, 298323, 2701951.
88. Largent BL, Sosnowski RG, Reed RR. Directed expression of an oncogene to the olfactory neuronal lineage in transgenic mice. J Neurosci 1993, 13:300-312.
89. Sambrook J, Fritsch EF, Maniatis T. Molecular cloning. A laboratory manual 1989, New York: Cold Spring Harbor Laboratory Press.
90. Chen S, Lane AP, Bock R, Leinders-Zufall T, Zufall F. Blocking adenylyl cyclase inhibits olfactory generator currents induced by "IP3-odors". J Neurophysiol 2000, 84:575-580.
91. Restrepo D, Zviman MM, Rawson NE. Imaging of intracellular calcium in chemosensory receptor cells. Experimental Cell Biology of Taste and Olfaction 1995, 387-398. Boca Raton: CRC Press, Spielman AI, Brand JG.
92. Schaefer ML, Finger TE, Restrepo D. Variability of position of the P2 glomerulus within a map of the mouse olfactory bulb. J Comp Neurol 2001, 436:351-362. 10.1002/cne.1072, 11438935.