The cyclic nucleotide-gated ion channel CNGA3 contributes to coolness-induced responses of Grueneberg ganglion neurons

Cellular and Molecular Life Sciences

Volumn 67, Issue 11, 2010, Pages 1859-1869

  Mamasuew, Katharina ^a   Michalakis, Stylianos ^b   Breer, Heinz ^a   Biel, Martin ^b   Fleischer, Joerg ^a  

^a UNIVERSITY OF HOHENHEIM   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

Author keywords

C Fos; cGMP; Olfaction; Thermosensory; Transmembrane guanylyl cyclase

Indexed keywords

CYCLIC GMP; CYCLIC NUCLEOTIDE GATED CHANNEL; PROTEIN CNGA3; UNCLASSIFIED DRUG; CNGA3 PROTEIN, MOUSE; OLFACTORY MARKER PROTEIN; OMP PROTEIN, MOUSE; PRIMER DNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENVIRONMENTAL TEMPERATURE; ENZYME ACTIVATION; MOUSE; MOUSE STRAIN; NERVE CELL MEMBRANE POTENTIAL; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; TEMPERATURE; THERMOREGULATION; WILD TYPE; ANIMAL; C57BL MOUSE; COLD; CYTOLOGY; GENETICS; IN SITU HYBRIDIZATION; METABOLISM; MOUSE MUTANT; OLFACTORY RECEPTOR; OLFACTORY SYSTEM; SENSORY GANGLION; SIGNAL TRANSDUCTION;

CAENORHABDITIS ELEGANS; MUS;

ANIMALS; BASE SEQUENCE; COLD TEMPERATURE; CYCLIC NUCLEOTIDE-GATED CATION CHANNELS; DNA PRIMERS; GANGLIA, SENSORY; IN SITU HYBRIDIZATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OLFACTORY MARKER PROTEIN; OLFACTORY PATHWAYS; OLFACTORY RECEPTOR NEURONS; SIGNAL TRANSDUCTION;

EID: 77952562660     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-010-0296-8     Document Type: Article

References (45)

1. H Breer J Fleischer J Strotmann 2006 The sense of smell: multiple olfactory subsystems Cell Mol Life Sci 63 1465 1475 10.1007/s00018-006-6108-5 1:CAS:528:DC%2BD28XnvFWmsLw%3D 16732429 (Pubitemid 44156743)
2. M Ma 2007 Encoding olfactory signals via multiple chemosensory systems Crit Rev Biochem Mol Biol 42 463 480 10.1080/10409230701693359 1:CAS:528:DC%2BD2sXhsVSgsbjI 18066954 (Pubitemid 350232896)
3. SD Munger T Leinders-Zufall F Zufall 2009 Subsystem organization of the mammalian sense of smell Annu Rev Physiol 71 115 140 10.1146/annurev.physiol.70. 113006.100608 1:CAS:528:DC%2BD1MXjsValsLk%3D 18808328
4. SH Fuss M Omura P Mombaerts 2005 The Grueneberg ganglion of the mouse projects axons to glomeruli in the olfactory bulb Eur J Neurosci 22 2649 2664 10.1111/j.1460-9568.2005.04468.x 16307607 (Pubitemid 41759007)
5. DS Koos SE Fraser 2005 The Grueneberg ganglion projects to the olfactory bulb Neuroreport 16 1929 1932 10.1097/01.wnr.0000186597.72081.10 16272881 (Pubitemid 41653516)
6. J Fleischer N Hass K Schwarzenbacher S Besser H Breer 2006 A novel population of neuronal cells expressing the olfactory marker protein (OMP) in the anterior/dorsal region of the nasal cavity Histochem Cell Biol 125 337 349 10.1007/s00418-005-0077-x 1:CAS:528:DC%2BD28Xit1Kqs7Y%3D 16273384 (Pubitemid 43376199)
7. D Roppolo V Ribaud VP Jungo C Lüscher I Rodriguez 2006 Projection of the Gruneberg ganglion to the mouse olfactory bulb Eur J Neurosci 23 2887 2894 10.1111/j.1460-9568.2006.04818.x 16819977 (Pubitemid 43882867)
8. MJ Storan B Key 2006 Septal organ of Gruneberg is part of the olfactory system J Comp Neurol 494 834 844 10.1002/cne.20858 16374816 (Pubitemid 43054229)
9. J Fleischer K Schwarzenbacher S Besser N Hass H Breer 2006 Olfactory receptors and signalling elements in the Grueneberg ganglion J Neurochem 98 543 554 10.1111/j.1471-4159.2006.03894.x 1:CAS:528:DC%2BD28Xot1OmsLk%3D 16805845 (Pubitemid 44133157)
10. J Fleischer K Schwarzenbacher H Breer 2007 Expression of trace amine-associated receptors in the Grueneberg ganglion Chem Senses 32 623 631 10.1093/chemse/bjm032 1:CAS:528:DC%2BD2sXptlKitro%3D 17556730 (Pubitemid 47261079)
11. J Brechbühl M Klaey MC Broillet 2008 Grueneberg ganglion cells mediate alarm pheromone detection in mice Science 321 1092 1095 10.1126/science.1160770 18719286
12. K Mamasuew H Breer J Fleischer 2008 Grueneberg ganglion neurons respond to cool ambient temperatures Eur J Neurosci 28 1775 1785 10.1111/j.1460-9568. 2008.06465.x 18973593
13. H Hensel 1981 Thermoreception and temperature regulation Monogr Physiol Soc 38 1 321 1:STN:280:DyaL3s3ksVKrtA%3D%3D 6820811
14. A Patapoutian AM Peier GM Story V Viswanath 2003 ThermoTRP channels and beyond: mechanisms of temperature sensation Nat Rev Neurosci 4 529 539 10.1038/nrn1141 1:CAS:528:DC%2BD3sXltVWmtro%3D 12838328 (Pubitemid 37271364)
15. M Tominaga MJ Caterina 2004 Thermosensation and pain J Neurobiol 61 3 12 10.1002/neu.20079 15362149 (Pubitemid 39302620)
16. H Wang CJ Woolf 2005 Pain TRPs Neuron 46 9 12 10.1016/j.neuron.2005.03. 011 1:CAS:528:DC%2BD2MXjslSgs7c%3D 15820689 (Pubitemid 40488307)
17. DD McKemy WM Neuhausser D Julius 2002 Identification of a cold receptor reveals a general role for TRP channels in thermosensation Nature 416 52 58 10.1038/nature719 1:CAS:528:DC%2BD38XitlSitrc%3D 11882888 (Pubitemid 34215395)
18. AM Peier A Moqrich AC Hergarden AJ Reeve DA Andersson GM Story TJ Earley I Dragoni P McIntyre S Bevan A Patapoutian 2002 A TRP channel that senses cold stimuli and menthol Cell 108 705 715 10.1016/S0092-8674(02)00652-9 1:CAS:528:DC%2BD38XisFOhtLg%3D 11893340 (Pubitemid 34241429)
19. DM Bautista J Siemens JM Glazer PR Tsuruda AI Basbaum CL Stucky SE Jordt D Julius 2007 The menthol receptor TRPM8 is the principal detector of environmental cold Nature 448 204 208 10.1038/nature05910 1:CAS:528: DC%2BD2sXnsFeisLg%3D 17538622 (Pubitemid 47067367)
20. RW Colburn ML Lubin DJ Stone Jr Y Wang D Lawrence MR D'Andrea MR Brandt Y Liu CM Flores N Qin 2007 Attenuated cold sensitivity in TRPM8 null mice Neuron 54 379 386 10.1016/j.neuron.2007.04.017 1:CAS:528:DC%2BD2sXmtVOjsrY%3D 17481392 (Pubitemid 46671410)
21. A Dhaka AN Murray J Mathur TJ Earley MJ Petrus A Patapoutian 2007 TRPM8 is required for cold sensation in mice Neuron 54 371 378 10.1016/j.neuron.2007. 02.024 1:CAS:528:DC%2BD2sXmtVOjsrk%3D 17481391 (Pubitemid 46659806)
22. J Fleischer K Mamasuew H Breer 2009 Expression of cGMP signaling elements in the Grueneberg ganglion Histochem Cell Biol 131 75 88 10.1007/s00418-008- 0514-8 1:CAS:528:DC%2BD1cXhsFamsLnP 18830617
23. CM Coburn CI Bargmann 1996 A putative cyclic nucleotide-gated channel is required for sensory development and function in C. elegans Neuron 17 695 706 10.1016/S0896-6273(00)80201-9 1:CAS:528:DyaK28Xms1aisr0%3D 8893026 (Pubitemid 26365348)
24. H Komatsu I Mori JS Rhee N Akaike Y Ohshima 1996 Mutations in a cyclic nucleotide-gated channel lead to abnormal thermosensation and chemosensation in C. elegans Neuron 17 707 718 10.1016/S0896-6273(00)80202-0 1:CAS:528: DyaK28Xms1aisro%3D 8893027 (Pubitemid 26365349)
25. H Inada H Ito J Satterlee P Sengupta K Matsumoto I Mori 2006 Identification of guanylyl cyclases that function in thermosensory neurons of Caenorhabditis elegans Genetics 172 2239 2252 10.1534/genetics.105.050013 1:CAS:528:DC%2BD28XkvFOgsbY%3D 16415369
26. CY Liu SE Fraser DS Koos 2009 Grueneberg ganglion olfactory subsystem employs a cGMP signaling pathway J Comp Neurol 516 36 48 10.1002/cne.22096 1:CAS:528:DC%2BD1MXhtVSntbnE 19565523
27. UB Kaupp R Seifert 2002 Cyclic nucleotide-gated ion channels Physiol Rev 82 769 824 1:CAS:528:DC%2BD38XlslCmt70%3D 12087135
28. M Biel M Seeliger A Pfeifer K Kohler A Gerstner A Ludwig G Jaissle S Fauser E Zrenner F Hofmann 1999 Selective loss of cone function in mice lacking the cyclic nucleotide-gated channel CNG3 Proc Natl Acad Sci USA 96 7553 7557 10.1073/pnas.96.13.7553 1:CAS:528:DyaK1MXltVOqsb8%3D 10377453 (Pubitemid 29299700)
29. M Biel 2009 Cyclic nucleotide-regulated cation channels J Biol Chem 284 9017 9021 10.1074/jbc.R800075200 1:CAS:528:DC%2BD1MXjs1ynur8%3D 19054768
30. RS Dhallan KW Yau KA Schrader RR Reed 1990 Primary structure and functional expression of a cyclic nucleotide-activated channel from olfactory neurons Nature 347 184 187 10.1038/347184a0 1:CAS:528:DyaK3MXhsF2hsrk%3D 1697649 (Pubitemid 20315877)
31. J Ludwig T Margalit E Eismann D Lancet UB Kaupp 1990 Primary structure of cAMP-gated channel from bovine olfactory epithelium FEBS Lett 270 24 29 10.1016/0014-5793(90)81226-E 1:CAS:528:DyaK3MXhvVSntrs%3D 1699793 (Pubitemid 20288560)
32. ER Liman LB Buck 1994 A second subunit of the olfactory cyclic nucleotide-gated channel confers high sensitivity to cAMP Neuron 13 611 621 10.1016/0896-6273(94)90029-9 1:CAS:528:DyaK2MXhtVaksbw%3D 7522482 (Pubitemid 24300166)
33. A Kuhara M Okumura T Kimata Y Tanizawa R Takano KD Kimura H Inada K Matsumoto I Mori 2008 Temperature sensing by an olfactory neuron in a circuit controlling behavior of C. elegans Science 320 803 807 10.1126/science.1148922 1:CAS:528:DC%2BD1cXlsVGltrY%3D 18403676 (Pubitemid 351929631)
34. S Pifferi A Boccaccio A Menini 2006 Cyclic nucleotide-gated ion channels in sensory transduction FEBS Lett 580 2853 2859 10.1016/j.febslet.2006.03.086 1:CAS:528:DC%2BD28XltVKnt7w%3D 16631748 (Pubitemid 43729158)
35. W Bönigk W Altenhofen F Müller A Dose M Illing RS Molday UB Kaupp 1993 Rod and cone photoreceptor cells express distinct genes for cGMP-gated channels Neuron 10 865 877 10.1016/0896-6273(93)90202-3 7684234 (Pubitemid 23152042)
36. I Weyand M Godde S Frings J Weiner F Müller W Altenhofen H Hatt UB Kaupp 1994 Cloning and functional expression of a cyclic-nucleotide-gated channel from mammalian sperm Nature 368 859 863 10.1038/368859a0 1:CAS:528:DyaK2cXksFalsL0%3D 7512693 (Pubitemid 24137751)
37. SW Cho KY Choi CS Park 2004 A new putative cyclic nucleotide-gated channel gene, cng-3, is critical for thermotolerance in Caenorhabditis elegans Biochem Biophys Res Commun 325 525 531 10.1016/j.bbrc.2004.10.060 1:CAS:528:DC%2BD2cXpsVOlsLw%3D 15530424 (Pubitemid 39458026)
38. MR Meyer A Angele E Kremmer UB Kaupp F Muller 2000 A cGMP-signaling pathway in a subset of olfactory sensory neurons Proc Natl Acad Sci USA 97 10595 10600 10.1073/pnas.97.19.10595 1:CAS:528:DC%2BD3cXms1Crt7c%3D 10984544
39. J Hu C Zhong C Ding Q Chi A Walz P Mombaerts H Matsunami M Luo 2007 Detection of near-atmospheric concentrations of CO2 by an olfactory subsystem in the mouse Science 317 953 957 10.1126/science.1144233 1:CAS:528: DC%2BD2sXptVaisr4%3D 17702944 (Pubitemid 47301324)
40. T Leinders-Zufall RE Cockerham S Michalakis M Biel DL Garbers RR Reed F Zufall SD Munger 2007 Contribution of the receptor guanylyl cyclase GC-D to chemosensory function in the olfactory epithelium Proc Natl Acad Sci USA 104 14507 14512 10.1073/pnas.0704965104 1:CAS:528:DC%2BD2sXhtVGmur3I 17724338 (Pubitemid 350003291)
41. DM Juilfs HJ Fülle AZ Zhao MD Houslay DL Garbers JA Beavo 1997 A subset of olfactory neurons that selectively express cGMP-stimulated phosphodiesterase (PDE2) and guanylyl cyclase-D define a unique olfactory signal transduction pathway Proc Natl Acad Sci USA 94 3388 3395 10.1073/pnas.94.7.3388 1:CAS:528:DyaK2sXisVKns78%3D 9096404 (Pubitemid 27157322)
42. C Zheng P Feinstein T Bozza I Rodriguez P Mombaerts 2000 Peripheral olfactory projections are differentially affected in mice deficient in a cyclic nucleotide-gated channel subunit Neuron 26 81 91 10.1016/S0896-6273(00)81140-X 1:CAS:528:DC%2BD3cXjtFSktrs%3D 10798394
43. S Serizawa K Miyamichi H Takeuchi Y Yamagishi M Suzuki H Sakano 2006 A neuronal identity code for the odorant receptor-specific and activity-dependent axon sorting Cell 127 1057 1069 10.1016/j.cell.2006.10.031 1:CAS:528: DC%2BD28XhtlWktrzI 17129788 (Pubitemid 44792252)
44. CM Coburn I Mori Y Ohshima CI Bargmann 1998 A cyclic nucleotide-gated channel inhibits sensory axon outgrowth in larval and adult Caenorhabditis elegans: a distinct pathway for maintenance of sensory axon structure Development 125 249 258 1:CAS:528:DyaK1cXhtlGgtb8%3D 9486798
45. K Togashi MJ von Schimmelmann M Nishiyama CS Lim N Yoshida B Yun RS Molday Y Goshima K Hong 2008 Cyclic GMP-gated CNG channels function in Sema3A-induced growth cone repulsion Neuron 58 694 707 10.1016/j.neuron.2008.03. 017 1:CAS:528:DC%2BD1cXnvVSqsbc%3D 18549782 (Pubitemid 351778462)