Chemical Senses Vol. 30 No. suppl 1 © Oxford University
Press 2005; all rights reserved
Olfactory Receptor Neurons in Fish: Structural, Molecular and Functional Correlates
1 Department of Cellular and Developmental Biology, University of Colorado Health Sciences Center at Fitzsimons, Aurora, CO 80045, USA, 2 Department of Biological Sciences, Louisiana State University, Baton Rouge, LA, USA and 3 Department of Anatomy and Physiology, Kagawa Prefecture College, Kagawa, Japan
Correspondence to be sent to: Anne Hansen, e-mail: anne.hansen{at}uchsc.edu
Key words: G-protein, in situ hybridization, OR, teleost, ultrastructure, V2R
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Introduction |
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 Top Introduction Materials and methodsResults and discussionAcknowledgementsReferences |
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In rodents, the olfactory system is segregated into the main olfactory epithelium (OE) and into the vomeronasal organ (VNO), the former populated by ciliated olfactory receptor neurons (ORNs) expressing the G-protein subunit G
olf and OR-type
odorant receptor molecules, the latter housing microvillous receptor neurons (VRNs)
expressing Go and Gi and V1R, V2R and V3R receptor
molecules. Projections of ORNs and VRNs target distinct areas in the olfactory bulb (OB)
and the accessory olfactory bulb (AOB), respectively.
Differing from the situation in rodents, the fish OE contains three different types
of ORNs: ciliated, microvillous and crypt cells. These three types of ORNs are
intermingled in one epithelium. Recently,
Nikonov and Caprio (2001
) showed that
in catfish responses to biologically relevant stimuli form a consistent map in the OB.
The present study asked whether a distinct function can be attributed to the different
types of ORNs; whether the different types of ORNs utilize different G-protein
-subunits and different OR or V2R receptor molecules; and whether the different
morphological types of ORNs are distributed homogeneously across the olfactory
lamellae.
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Materials and methods |
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TopIntroductionMaterials and methodsResults and discussionAcknowledgementsReferences |
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The study was carried out in the catfish (Ictalurus punctatus) and the goldfish (Carassius auratus). We injected the fluorescent tracer DiI into OBs to retrogradely label ORNs in the OE. Immunocytochemistry was used to examine the expression of G-protein subunits. Probes for OR-type and V2R-type receptors [courtesy of John Ngai, UC Berkeley (catfish OR probes), Michelle Rankin, NIH (catfish V2R probe) and Y. Cao and L. Stryer, UCSF (goldfish OR and V2R probes)] were used for in situ hybridization to visualize the expression of odorant receptor molecules. All three methods were carried out at the light microscopic and the electron microscopic level. All procedures were carried out with the approval of the Institutional Animal Care and Use Committees of the respective institutions.
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Results and discussion |
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TopIntroductionMaterials and methodsResults and discussionAcknowledgementsReferences |
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Our results as shown by DiI injections indicate that ciliated ORNs predominantly project to medial and ventral areas of the OB, areas for which Nikonov and Caprio (2001
) reported
responses to bile salts. DiI injections into the posterior dorsal areas labeled
microvillous ORNs in the OE. In the posterior dorsal areas of catfish
Nikonov and Caprio (2001) found
responses to nucleotides. DiI injections into anterior dorsal areas retrogradely labeled
microvillous ORNs while injections into anterior ventral areas labeled ciliated ORNs. For
both regions
Nikonov and Caprio (2001) reported
responses to amino acids. Crypt ORNs were labeled only by injections into two very small
distinct ventral areas. Interestingly, catfish and goldfish revealed differences in the
expression of G-protein subunits. Golf was expressed in ciliated ORNs
in both species, while Go was expressed in crypt ORNs in catfish and in
microvillous ORNs in goldfish. Conversely, Gq was expressed in
microvillous ORNs in catfish and Gq/11 in crypt cells of goldfish. In
addition, goldfish crypt ORNs expressed Go in their insunk
cilia—the only case where two different protein subunits were expressed in one cell
type (Hansen et al., 2003,
2004).
In both catfish and goldfish OR-type probes labeled ciliated ORNs while V2R-type
probes labeled microvillous ORNs. Neither set of probes available labeled crypt ORNs.
Based on the results of G-protein subunit immunoreactivity and in situ
hybridization in whole mount preparations of lamellae, the distribution of ciliated ORNs
is more or less homogeneous across the lamellae of goldfish but heterogeneous in catfish.
The distribution of microvillous and crypt type ORNs is heterogeneous in both catfish and
goldfish. ORNs in both catfish and goldfish never expressed more than one molecular
receptor per cell. In goldfish, V2R probes were co-expressed with Go
(Hansen et al., 2003, 2004).
In catfish, bile salts are detected by ciliated ORNs, nucleotides by microvillous ORNs
and amino acids by ciliated and microvillous ORNs. A recent study by
Sato and Suzuki (2001) reported a
similar scenario for trout. The function of crypt ORNs is unknown. We conclude that in
catfish, distinct types of ORNs project to defined areas in the olfactory bulb. G-protein
-subunits mediate the transduction pathways in catfish and goldfish, but different
subunits are expressed in different cell types. In both species OR-type receptor
molecules are expressed in ciliated ORNs, and V2R-like receptor molecules are expressed
in microvillous ORNs.
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Acknowledgements |
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TopIntroductionMaterials and methodsResults and discussionAcknowledgementsReferences |
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This study was supported by National Institute on Deafness and Other Communication Disorders Grants RO1 DC 03792 (J.C.) and P30 DC04657 (to Diego Restrepo, University of Colorado, CO).
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References |
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TopIntroductionMaterials and methodsResults and discussionAcknowledgementsReferences |
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Hansen, A., Rolen, S.H., Anderson, K., Morita, Y., Caprio, J. and Finger, T.E. (2003) Correlation between olfactory receptor cell type and function in the channel catfish. J. Neurosci., 23, 9328–9339.
Hansen, A., Anderson, K. and Finger, T.E. (2004) Differential distribution of olfactory receptor neurons in goldfish: structural and molecular correlates. J. Comp. Neurol., 477, 347–359.[CrossRef][ISI][Medline]
Nikonov, A.A. and Caprio, J. (2001) Electrophysiological evidence for a chemotopy of biologically relevant odors in the olfactory bulb of the channel catfish. J. Neurophysiol., 86, 1869–1876.
Sato, K. and Suzuki, N. (2001) Whole-cell response characteristics of ciliated and microvillous olfactory receptor neurons to amino acids, pheromone candidates and urine in rainbow trout. Chem. Senses, 26, 1145–1156.
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