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Kinetics of olfactory responses might largely depend on the odorant–receptor interaction and the odorant deactivation postulated for flux detectors

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Abstract

Experimental data together with modeling of pheromone perireceptor and receptor events in moths (Bombyx mori, Antheraea polyphemus) suggest that the kinetics of olfactory receptor potentials largely depend on the association of the odorant with the neuronal receptor molecules and the deactivation of the odorant accumulated around the receptor neuron. The first process could be responsible for the reaction times (mean about 400 ms) of the nerve impulses at threshold. The second process has been postulated for flux detectors such as olfactory sensilla of moths. The odorant deactivation could involve a modification of the pheromone-binding protein (PBP) that “locks” the pheromone inside the inner binding cavity of the protein. The model combines seemingly contradictory functions of the PBP such as pheromone transport, protection of the pheromone from enzymatic degradation, pheromone deactivation, and pheromone–receptor interaction. Model calculations reveal a density of at least 6,000 receptor molecules per µm2 of neuronal membrane. The volatile decanoyl-thio-1,1,1-trifluoropropanone specifically blocks pheromone receptor neurons, probably when bound to the PBP and by competitive binding to the receptor molecules. The shallow dose–response curve of the receptor potential and altered response properties observed with pheromone derivatives or after adaptation may indicate shortened opening of ion channels.

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Abbreviations

Ac1:

(E,Z)-6,11-hexadecadienyl acetate

ApolPBP:

Antheraea polyphemus pheromone-binding protein

bombykol:

(E,Z)-10,12-hexadecadien-1-ol

bombykal:

(E,Z)-10,12-hexadecadienal

BSA:

Bovine serum albumin

DEET:

N,N-diethyl-3-methylbenzamide

DTFP:

Decanoyl-thio-1,1,1-trifluoropropanone

EAG:

Electroantennogram

EC50 :

Effective concentration

ERP:

Elementary receptor potential

k i , k −i :

Rate constants of forward and backward reactions, respectively

model N:

Model with the hypothetical enzyme N for pheromone deactivation

ORCO:

Olfactory receptor co-receptor

PBP:

Pheromone-binding protein

SNMP:

Sensory neuron membrane protein

U :

Pheromone uptake (μM/s) related to the hair volume (2.6 pl)

U sat :

Pheromone uptake (μM/s) at which the postulated deactivation process is saturated

VUAA1:

2-(4-ethyl-5-(pyridin-3-yl)-4H-1,2,4-triazol-3-ylthio)-N-(4-ethylphenyl) acetamide

A:

A-form of PBP, with C-terminus in

B:

B-form of PBP, with C-terminus out

B′:

Scavenger form of PBP

E:

Pheromone-degrading enzyme

F:

Free pheromone

Fair :

Free pheromone in air

FA:

Pheromone–PBP A-form complex, able to bind R

FAR:

Pheromone–PBP–receptor complex

FAR′:

Activated pheromone–PBP–receptor complex

FB:

Pheromone–PBP B-form complex

FB′:

Pheromone–PBP B′-form complex, deactivated pheromone

M:

Pheromone metabolite

MB′:

Metabolite–PBP scavenger form complex

N:

Pheromone deactivating enzyme, hypothetical

R:

Pheromone receptor molecule, at the receptor neuron membrane

R′:

Activated receptor molecule

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Acknowledgments

The author is grateful for help by the librarian A. Krikellis and his team. He thanks J.-P. Rospars for stimulating discussions and constructive criticism, R. A. Steinbrecht, and two referees for valuable suggestions, and A. M. Biederman-Thorson for linguistic improvements of an earlier version of the manuscript. Finally, he thanks John G. Hildebrand for multi-decadic friendship and for carrying Manduca sexta to his lab. Last but not least he wishes to thank F. G. Barth for his careful editorial work.

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  1. Max-Planck-Institut fuer Verhaltensphysiologie/Ornithologie, Seewiesen, 82319, Starnberg, Germany

    Karl-Ernst Kaissling

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Kaissling, KE. Kinetics of olfactory responses might largely depend on the odorant–receptor interaction and the odorant deactivation postulated for flux detectors. J Comp Physiol A 199, 879–896 (2013). https://doi.org/10.1007/s00359-013-0812-z

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  • DOI: https://doi.org/10.1007/s00359-013-0812-z

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