Home LiteratureArticle Details
PMID: 17267604 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Olfactory neurons expressing transient receptor potential channel M5 (TRPM5) are involved in sensing semiochemicals.

Lin W, Margolskee R, Donnert G, Hell SW, Restrepo D

Abstract

Olfactory sensory neurons (OSNs) in the main olfactory epithelium respond to environmental odorants. Recent studies reveal that these OSNs also respond to semiochemicals such as pheromones and that main olfactory input modulates animal reproduction, but the transduction mechanism for these chemosignals is not fully understood. Previously, we determined that responses to putative pheromones in the main olfactory system were reduced but not eliminated in mice defective for the canonical cAMP transduction pathway, and we suggested, on the basis of pharmacology, an involvement of phospholipase C. In the present study, we find that a downstream signaling component of the phospholipase C pathway, the transient receptor potential channel M5 (TRPM5), is coexpressed with the cyclic nucleotide-gated channel subunit A2 in a subset of mature OSNs. These neurons project axons primarily to the ventral olfactory bulb, where information from urine and other socially relevant signals is processed. We find that these chemosignals activate a subset of glomeruli targeted by TRPM5-expressing OSNs. Our data indicate that TRPM5-expressing OSNs that project axons to glomeruli in the ventral area of the main olfactory bulb are involved in processing of information from semiochemicals.

MeSH Terms
Animals Axons Cyclic Nucleotide-Gated Cation Channels Ion Channels/analysis Mice Mice, Transgenic Olfactory Bulb/physiology Olfactory Receptor Neurons/chemistry,physiology Pheromones/physiology Signal Transduction TRPM Cation Channels/analysis,physiology Transient Receptor Potential Channels Type C Phospholipases/metabolism
Chemicals
Cnga2 protein, mouse Cyclic Nucleotide-Gated Cation Channels Ion Channels Pheromones TRPM Cation Channels Transient Receptor Potential Channels Trpm5 protein, mouse Type C Phospholipases
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Lin Weihong
Department of Biological Sciences, University of Maryland Baltimore County, Baltimore, MD 21250, USA.
Margolskee Robert
Donnert Gerald
Hell Stefan W
Restrepo Diego
References (50)
50 references, click to expand
  1. Neuronal inositol 1,4,5-trisphosphate receptor localized to the plasma membrane of olfactory cilia.
    Neuroscience. 1993 Nov;57(2):339-52 PMID: 8115043
  2. Olfactory inputs to hypothalamic neurons controlling reproduction and fertility.
    Cell. 2005 Nov 18;123(4):669-82 PMID: 16290037
  3. Olfactory fingerprints for major histocompatibility complex-determined body odors II: relationship among odor maps, genetics, odor composition, and behavior.
    J Neurosci. 2002 Nov 1;22(21):9513-21 PMID: 12417675
  4. Encoding social signals in the mouse main olfactory bulb.
    Nature. 2005 Mar 24;434(7032):470-7 PMID: 15724148
  5. Odors detected by mice deficient in cyclic nucleotide-gated channel subunit A2 stimulate the main olfactory system.
    J Neurosci. 2004 Apr 7;24(14):3703-10 PMID: 15071119
  6. Controversial issues in vertebrate olfactory transduction.
    Annu Rev Physiol. 1999;61:857-71 PMID: 10099713
  7. Structure and function of the vomeronasal system: an update.
    Prog Neurobiol. 2003 Jun;70(3):245-318 PMID: 12951145
  8. Behaviour: smells, brains and hormones.
    Nature. 2006 Jan 12;439(7073):149-51 PMID: 16407941
  9. Intracellular Ca2+ and the phospholipid PIP2 regulate the taste transduction ion channel TRPM5.
    Proc Natl Acad Sci U S A. 2003 Dec 9;100(25):15160-5 PMID: 14657398
  10. Deficits in sexual and aggressive behaviors in Cnga2 mutant mice.
    Nat Neurosci. 2005 Dec;8(12):1660-2 PMID: 16261133
  11. Is the vomeronasal system really specialized for detecting pheromones?
    Trends Neurosci. 2006 Jan;29(1):1-7 PMID: 16271402
  12. Essential role of the main olfactory system in social recognition of major histocompatibility complex peptide ligands.
    J Neurosci. 2006 Feb 15;26(7):1961-70 PMID: 16481428
  13. Genetic analysis of brain circuits underlying pheromone signaling.
    Annu Rev Genet. 2006;40:449-67 PMID: 16953793
  14. Mice deficient in G(olf) are anosmic.
    Neuron. 1998 Jan;20(1):69-81 PMID: 9459443
  15. Ggamma13 colocalizes with gustducin in taste receptor cells and mediates IP3 responses to bitter denatonium.
    Nat Neurosci. 1999 Dec;2(12):1055-62 PMID: 10570481
  16. Macromolecular-scale resolution in biological fluorescence microscopy.
    Proc Natl Acad Sci U S A. 2006 Aug 1;103(31):11440-5 PMID: 16864773
  17. Molecular detection of pheromone signals in mammals: from genes to behaviour.
    Nat Rev Neurosci. 2003 Jul;4(7):551-62 PMID: 12838330
  18. Odortypes and MHC peptides: Complementary chemosignals of MHC haplotype?
    Trends Neurosci. 2006 Nov;29(11):604-9 PMID: 16904761
  19. MHC peptides and the sensory evaluation of genotype.
    Trends Neurosci. 2006 Feb;29(2):100-7 PMID: 16337283
  20. TRPM5 is a transient Ca2+-activated cation channel responding to rapid changes in [Ca2+]i.
    Proc Natl Acad Sci U S A. 2003 Dec 9;100(25):15166-71 PMID: 14634208
  21. Simultaneous activation of mouse main and accessory olfactory bulbs by odors or pheromones.
    J Comp Neurol. 2005 Sep 5;489(4):491-500 PMID: 16025460
  22. TRP channels in C. elegans.
    Annu Rev Physiol. 2006;68:719-36 PMID: 16460289
  23. Disruption of the type III adenylyl cyclase gene leads to peripheral and behavioral anosmia in transgenic mice.
    Neuron. 2000 Sep;27(3):487-97 PMID: 11055432
  24. The olfactory bulb: coding and processing of odor molecule information.
    Science. 1999 Oct 22;286(5440):711-5 PMID: 10531048
  25. Feedback loops link odor and pheromone signaling with reproduction.
    Cell. 2005 Nov 18;123(4):683-95 PMID: 16290036
  26. Phosphatidyl-inositide signalling proteins in a novel class of sensory cells in the mammalian olfactory epithelium.
    Eur J Neurosci. 2005 May;21(10):2692-700 PMID: 15926917
  27. Profoundly different calcium permeation and blockage determine the specific function of distinct cyclic nucleotide-gated channels.
    Neuron. 1995 Jul;15(1):169-79 PMID: 7542461
  28. Novel microglomerular structures in the olfactory bulb of mice.
    J Neurosci. 2002 Feb 1;22(3):766-74 PMID: 11826106
  29. Pheromones, binding proteins and receptor responses in rodents.
    Biochem Soc Trans. 2003 Feb;31(Pt 1):117-22 PMID: 12546667
  30. Olfactory fingerprints for major histocompatibility complex-determined body odors.
    J Neurosci. 2001 Apr 1;21(7):2481-7 PMID: 11264322
  31. General anosmia caused by a targeted disruption of the mouse olfactory cyclic nucleotide-gated cation channel.
    Neuron. 1996 Oct;17(4):681-93 PMID: 8893025
  32. Pharmacological properties and functional role of a TRP-related ion channel in lobster olfactory receptor neurons.
    J Neurophysiol. 2005 Mar;93(3):1372-80 PMID: 15525800
  33. Coding of sweet, bitter, and umami tastes: different receptor cells sharing similar signaling pathways.
    Cell. 2003 Feb 7;112(3):293-301 PMID: 12581520
  34. Olfaction: diverse species, conserved principles.
    Neuron. 2005 Nov 3;48(3):417-30 PMID: 16269360
  35. Pheromonal communication in vertebrates.
    Nature. 2006 Nov 16;444(7117):308-15 PMID: 17108955
  36. Primary structure and functional expression of a cyclic nucleotide-activated channel from olfactory neurons.
    Nature. 1990 Sep 13;347(6289):184-7 PMID: 1697649
  37. Breaking the diffraction resolution limit by stimulated emission: stimulated-emission-depletion fluorescence microscopy.
    Opt Lett. 1994 Jun 1;19(11):780-2 PMID: 19844443
  38. 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 Sep;30(7):615-26 PMID: 16141292
  39. A second class of chemosensory receptors in the olfactory epithelium.
    Nature. 2006 Aug 10;442(7103):645-50 PMID: 16878137
  40. Emerging views on the distinct but related roles of the main and accessory olfactory systems in responsiveness to chemosensory signals in mice.
    Horm Behav. 2004 Sep;46(3):247-56 PMID: 15325226
  41. Transduction mechanisms in vertebrate olfactory receptor cells.
    Physiol Rev. 1998 Apr;78(2):429-66 PMID: 9562035
  42. Making sense with TRP channels: store-operated calcium entry and the ion channel Trpm5 in taste receptor cells.
    Cell Calcium. 2003 May-Jun;33(5-6):541-9 PMID: 12765699
  43. Mouse taste cells with G protein-coupled taste receptors lack voltage-gated calcium channels and SNAP-25.
    BMC Biol. 2006;4:7 PMID: 16573824
  44. Localization of the olfactory cyclic nucleotide-gated channel subunit 1 in normal, embryonic and regenerating olfactory epithelium.
    Neuroscience. 1999;94(1):131-40 PMID: 10613503
  45. Trpm5 null mice respond to bitter, sweet, and umami compounds.
    Chem Senses. 2006 Mar;31(3):253-64 PMID: 16436689
  46. The expression of the growth associated protein B50/GAP43 in the olfactory system of neonatal and adult rats.
    J Neurosci. 1989 Feb;9(2):683-91 PMID: 2918383
  47. A transient receptor potential channel expressed in taste receptor cells.
    Nat Neurosci. 2002 Nov;5(11):1169-76 PMID: 12368808
  48. Variability of position of the P2 glomerulus within a map of the mouse olfactory bulb.
    J Comp Neurol. 2001 Jul 30;436(3):351-62 PMID: 11438935
  49. Pheromone detection in male mice depends on signaling through the type 3 adenylyl cyclase in the main olfactory epithelium.
    J Neurosci. 2006 Jul 12;26(28):7375-9 PMID: 16837584
  50. International Union of Pharmacology. XLIX. Nomenclature and structure-function relationships of transient receptor potential channels.
    Pharmacol Rev. 2005 Dec;57(4):427-50 PMID: 16382100
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2007-02-13
Epub
2007-00-31
Pages
2471-6
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC1892929
Subset
IM
Grants
NIDCD NIH HHS · P30 DC004657 · United States
NIDCD NIH HHS · DC006828 · United States
NIDCD NIH HHS · R03 DC006828 · United States
NIDCD NIH HHS · DC004657 · United States
NIDCD NIH HHS · R01 DC003055 · United States
NIDCD NIH HHS · DC006070 · United States
NIDCD NIH HHS · R01 DC003155 · United States
NIDCD NIH HHS · R03 DC006828-02 · United States
NIDCD NIH HHS · DC03155 · United States
NIDCD NIH HHS · DC00566 · United States
NIDCD NIH HHS · R01 DC000566 · United States
NIDCD NIH HHS · DC03055 · United States
NIDCD NIH HHS · R01 DC006070 · United States
NIDCD NIH HHS · R01 DC009269 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com