Ca


Journal

Proceedings of the National Academy of Sciences of the United States of America
ISSN: 1091-6490
Titre abrégé: Proc Natl Acad Sci U S A
Pays: United States
ID NLM: 7505876

Informations de publication

Date de publication:
15 01 2019
Historique:
pubmed: 2 1 2019
medline: 13 3 2019
entrez: 2 1 2019
Statut: ppublish

Résumé

Activation of most primary sensory neurons results in transduction currents that are carried by cations. One notable exception is the vertebrate olfactory receptor neuron (ORN), where the transduction current is carried largely by the anion [Formula: see text] However, it remains unclear why ORNs use an anionic current for signal amplification. We have sought to provide clarification on this topic by studying the so far neglected dynamics of [Formula: see text], [Formula: see text], [Formula: see text], and [Formula: see text] in the small space of olfactory cilia during an odorant response. Using computational modeling and simulations we compared the outcomes of signal amplification based on either [Formula: see text] or [Formula: see text] currents. We found that amplification produced by [Formula: see text] influx instead of a [Formula: see text] efflux is problematic for several reasons: First, the [Formula: see text] current amplitude varies greatly, depending on mucosal ion concentration changes. Second, a [Formula: see text] current leads to a large increase in the ciliary [Formula: see text] concentration during an odorant response. This increase inhibits and even reverses [Formula: see text] clearance by [Formula: see text] exchange, which is essential for response termination. Finally, a [Formula: see text] current increases the ciliary osmotic pressure, which could cause swelling to damage the cilia. By contrast, a transduction pathway based on [Formula: see text] efflux circumvents these problems and renders the odorant response robust and reliable.

Identifiants

pubmed: 30598447
pii: 1816371116
doi: 10.1073/pnas.1816371116
pmc: PMC6338846
doi:

Substances chimiques

Chloride Channels 0
Receptors, Odorant 0
Sodium 9NEZ333N27
Potassium RWP5GA015D
Calcium SY7Q814VUP

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1053-1058

Subventions

Organisme : NIDCD NIH HHS
ID : R01 DC016647
Pays : United States

Déclaration de conflit d'intérêts

The authors declare no conflict of interest.

Références

Nature. 1987 Jan 29-Feb 4;325(6103):442-4
pubmed: 3027574
J Neurosci. 1991 Nov;11(11):3565-72
pubmed: 1719165
Nat Neurosci. 2011 Jun;14(6):763-9
pubmed: 21516098
Proc Natl Acad Sci U S A. 2005 Jul 26;102(30):10415-20
pubmed: 16027364
Curr Biol. 1994 Mar 1;4(3):256-8
pubmed: 7922331
Biophys J. 2001 Apr;80(4):1712-21
pubmed: 11259285
Curr Opin Neurobiol. 1998 Jun;8(3):321-9
pubmed: 9687354
J Gen Physiol. 2011 Sep;138(3):303-10
pubmed: 21875979
Proc Natl Acad Sci U S A. 2009 Jul 14;106(28):11776-81
pubmed: 19561302
Neurosci Lett. 1987 Dec 4;82(3):321-6
pubmed: 3501083
J Gen Physiol. 2006 Aug;128(2):171-84
pubmed: 16880265
J Physiol. 1991 Oct;442:147-68
pubmed: 1798028
Chem Senses. 2010 Mar;35(3):239-45
pubmed: 20100788
Neuron. 1993 Jul;11(1):123-32
pubmed: 8393322
Biophys J. 2012 Jun 20;102(12):2677-86
pubmed: 22735517
Proc Natl Acad Sci U S A. 2016 Oct 4;113(40):11063-11065
pubmed: 27660238
J Gen Physiol. 2016 Oct;148(4):293-311
pubmed: 27619419
Nat Neurosci. 2011 Nov 06;15(1):131-7
pubmed: 22057188
Chem Senses. 2008 Nov;33(9):839-59
pubmed: 18703537
J Neurosci. 1998 Sep 1;18(17):6623-30
pubmed: 9712634
Neuron. 2005 Feb 17;45(4):553-61
pubmed: 15721241
Proc Natl Acad Sci U S A. 2016 Oct 4;113(40):11078-11087
pubmed: 27647918
Biophys J. 2006 Feb 15;90(4):1147-55
pubmed: 16326896
Annu Rev Physiol. 1989;51:385-99
pubmed: 2653189
J Vis Exp. 2012 Apr 05;(62):e3862
pubmed: 22508037
J Physiol. 1986 Dec;381:263-78
pubmed: 2442351
Physiol Rep. 2017 Aug;5(15):
pubmed: 28784854
J Neurosci. 1991 Nov;11(11):3624-9
pubmed: 1941099
Chem Senses. 2002 Nov;27(9):789-801
pubmed: 12438204
J Gen Physiol. 2003 Sep;122(3):349-63
pubmed: 12939394
Ups J Med Sci. 2006;111(1):137-53
pubmed: 16553253
Pflugers Arch. 2009 Oct;458(6):1023-38
pubmed: 19475416
Nature. 1993 Nov 18;366(6452):283-6
pubmed: 8232590
Channels (Austin). 2017 Sep 3;11(5):399-414
pubmed: 28301269
Nature. 1993 May 6;363(6424):71-4
pubmed: 7683113
Proc Natl Acad Sci U S A. 2018 May 22;115(21):5570-5575
pubmed: 29735665
Nat Neurosci. 2009 Apr;12(4):454-62
pubmed: 19305400
J Neurosci. 2004 Sep 8;24(36):7931-8
pubmed: 15356206

Auteurs

Johannes Reisert (J)

Monell Chemical Senses Center, Philadelphia, PA 19104; reingrub@ens.fr jreisert@monell.org.

Jürgen Reingruber (J)

INSERM UMR 1024-IBENS (Institute of Biology of Ecole Normale Supérieure), Group of Applied Mathematics and Computational Biology, 75005 Paris, France reingrub@ens.fr jreisert@monell.org.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH