Anatomical and functional evidence for a role of arginine-vasopressin (AVP) in rat olfactory epithelium cells
Abstract
The olfactory epithelium (OE) is composed of olfactory sensory neurons (OSNs) and sustentacular cells; it lies in the nasal cavity where it is protected by a thin mucus layer. The finely regulated composition of this mucus provides OSN with a suitable ionic environment. To maintain the functional integrity of the epithelium despite permanent physical, chemical and microbial aggressions, both OSNs and surrounding sustentacular cells are continuously renewed from globose basal cells. Moreover, the sense of smell is involved in so numerous behaviours (feeding, reproduction, etc.) that it has to cross-talk with the endocrine and neuroendocrine systems. Thus, besides its sensory function, the olfactory epithelium is thought to undergo a lot of complex regulatory processes. We therefore studied the effects of various neuropeptides on primary cultures of Sprague-Dawley rat olfactory epithelium cells. We found that arginine-vasopressin (AVP) triggered a robust, dose-dependent calcium increase in these cells. The cell response was essentially ascribed to the V1a AVP receptor, whose presence was confirmed by RT-PCR and immunolabelling. In the culture, V1a but not V1b receptors were present, mainly localized in neurons. In the epithelium, both subtypes were found differentially distributed. V1a-R were localized mainly in globose basal cells and at the apical side of the epithelium, in the area of the dendritic knobs of OSNs. V1b-R were strongly associated with Bowman's gland cells and globose basal cells. These localizations suggested potential multifaceted roles of a hormone, AVP, in the olfactory epithelium.
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At moderately high concentrations, oxytocin activates V1 vasopressin receptors, which are present at many peripheral sites including the olfactory epithelium; the consequences of this activation are unknown.
“Finally, oxytocin at moderately high concentrations is an agonist at V1 vasopressin receptors, and these are expressed at many peripheral sites (including the olfactory epithelium (56); the consequences of activating these is not known).”
From Intranasal Oxytocin: Myths and Delusions (2016) · cites this paper as [56]
Cites
Single-Step Method of RNA Isolation by Acid Guanidinium Thiocyanate–Phenol–Chloroform Extraction
Chomczynski, P., & Sacchi, N. (1987) · Analytical Biochemistry · doi:10.1006/abio.1987.9999 · Cited by 65,240 · see citing works
Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction
Chomczyński, P., & Sacchi, N. (1987) · Analytical Biochemistry · doi:10.1016/0003-2697(87)90021-2 · Cited by 47,092 · see citing works
A new generation of Ca2+ indicators with greatly improved fluorescence properties.
Grynkiewicz, G., Poenie, M., & Tsien, R. Y. (1985) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)83641-4 · Cited by 21,722 · see citing works
The Neuron-Specific Protein PGP 9.5 Is a Ubiquitin Carboxyl-Terminal Hydrolase
Wilkinson, K. D., Lee, K., Deshpande, S. S., Duerksen-Hughes, P. J., Boss, J. M., & Pohl, J. (1989) · Science · doi:10.1126/science.2530630 · Cited by 871 · see citing works
Calof, A. L., & Chikaraishi, D. M. (1989) · Neuron · doi:10.1016/0896-6273(89)90120-7 · Cited by 363 · see citing works
Novel Ligand Specificity of Pituitary Vasopressin Receptors in the Rat
Antoni, F. A. (2008) · Neuroendocrinology · doi:10.1159/000123976 · Cited by 159 · see citing works
Progenitor cells of the olfactory receptor neuron lineage
Calof, A. L., Bonnin, A., Crocker, C. E., Kawauchi, S., Murray, R. C., Shou, J., & Wu, H. (2002) · Microscopy Research and Technique · doi:10.1002/jemt.10147 · Cited by 147 · see citing works
Activation of Purinergic Receptor Subtypes Modulates Odor Sensitivity
Hegg, C. C., Greenwood, D., Huang, W. C., Han, P., & Lucero, M. T. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-23-08291.2003 · Cited by 113 · see citing works
Adrenaline enhances odorant contrast by modulating signal encoding in olfactory receptor cells
Kawai, F., Kurahashi, T., & Kaneko, A. (1999) · Nature Neuroscience · doi:10.1038/5686 · Cited by 106 · see citing works
Biogenic Amines Modulate Olfactory Receptor Neurons Firing Activity in Mamestra brassicae
Grosmaître, X. (2001) · Chemical Senses · doi:10.1093/chemse/26.6.653 · Cited by 102 · see citing works
Hurbin, A., Boissin‐Agasse, L., Orcel, H., Rabié, A., Joux, N., Desarménien, M. G., Richard, P., & Moos, F. (1998) · Endocrinology · doi:10.1210/endo.139.11.6320 · Cited by 101 · see citing works
Olfactory receptor neurons express D2 dopamine receptors
Koster, N. L., Norman, A. B., Richtand, N. M., Nickell, W. T., Puché, A. C., Pixley, S. K., & Shipley, M. T. (1999) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19990906)411:4 · Cited by 95 · see citing works
Caillol, M., Aı̈oun, J., Baly, C., Persuy, M., & Salesse, R. (2003) · Brain Research · doi:10.1016/s0006-8993(02)03755-1 · Cited by 95 · see citing works
Self-citationSchofield, J. N., Day, I. N. M., Thompson, R. J., & Edwards, Y. H. (1995) · Developmental Brain Research · doi:10.1016/0165-3806(94)00217-n · Cited by 93 · see citing works
An Olfactory Sensory Neuron Line,Odora, Properly Targets Olfactory Proteins and Responds to Odorants
Murrell, J. R., & Hunter, D. D. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-19-08260.1999 · Cited by 83 · see citing works
Hurbin, A., Orcel, H., Alonso, G., Moos, F., & Rabié, A. (2002) · Endocrinology · doi:10.1210/endo.143.2.8643 · Cited by 80 · see citing works
Olfactory receptor cell function is affected by trigeminal nerve activity
Bouvet, J., Delaleu, J. C., & Holley, A. (1987) · Neuroscience Letters · doi:10.1016/0304-3940(87)90583-0 · Cited by 69 · see citing works
Freemark, M., Driscoll, P., Andrews, J. S., Kelly, P. A., & Royster, M. (1996) · Endocrinology · doi:10.1210/endo.137.3.8603606 · Cited by 67 · see citing works
Sabatier, N., Richard, P., & Dayanithi, G. (1997) · The Journal of Physiology · doi:10.1111/j.1469-7793.1997.253bh.x · Cited by 66 · see citing works
Gaillard, R.-C., Schoenenberg, P., Favrod-Coune, C. A., Muller, A. F., Marie, J., Bockaert, J., & Jard, S. (1984) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.81.9.2907 · Cited by 64 · see citing works
Coronas, V., Feron, F. P., Hen, R., Sicard, G., Jourdan, F., & Moyse, E. (1997) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1997.69051870.x · Cited by 61 · see citing works
Sabatier, N., Richard, P., & Dayanithi, G. (1998) · The Journal of Physiology · doi:10.1111/j.1469-7793.1998.699ba.x · Cited by 57 · see citing works
Gouzènes, L., Sabatier, N., Richard, P., Moos, F., & Dayanithi, G. (1999) · The Journal of Physiology · doi:10.1111/j.1469-7793.1999.0771s.x · Cited by 55 · see citing works
The activity of olfactory receptor cells is affected by acetylcholine and substance P
Bouvet, J., Delaleu, J.-C., & Holley, A. (1988) · Neuroscience Research · doi:10.1016/0168-0102(88)90050-8 · Cited by 54 · see citing works
Park, D., & Eisthen, H. L. (2003) · Journal of Neurophysiology · doi:10.1152/jn.01162.2002 · Cited by 49 · see citing works
Barni, T., Maggi, M., Fantoni, G., Granchi, S., Mancina, R., Gulisano, M., Marra, F., Macorsini, E., Luconi, M., Rotella, C. M., et al. (1999) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.84.11.6150 · Cited by 46 · see citing works
Cunningham, A. M., Manis, P. B., Reed, R. R., & Ronnett, G. V. (1999) · Neuroscience · doi:10.1016/s0306-4522(99)00193-1 · Cited by 39 · see citing works
Liu, X., Tribollet, E., Ogier, R., Barberis, C., & Raggenbass, M. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02625.x · Cited by 38 · see citing works
Alfaidy, N., Blot‐Chabaud, M., Bonvalet, J. P., & Farman, N. (1997) · Journal of Clinical Investigation · doi:10.1172/jci119785 · Cited by 37 · see citing works
Hegg, C. C., & Lucero, M. T. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00670.2003 · Cited by 33 · see citing works
Barni, T. (1999) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.84.11.4266 · Cited by 32 · see citing works
Fluorescent Pseudo-Peptide Linear Vasopressin Antagonists: Design, Synthesis, and Applications,
Durroux, T., Peter, M., Turcatti, G., Chollet, A., Balestre, M., Barberis, C., & Seyer, R. (1999) · Journal of Medicinal Chemistry · doi:10.1021/jm9804782 · Cited by 31 · see citing works
Manning, M., Bańkowski, K., Barberis, C., Jard, S., Elands, J., & Chan, W. Y. (1992) · International journal of peptide & protein research · doi:10.1111/j.1399-3011.1992.tb00300.x · Cited by 29 · see citing works
Coronas, V., Krantic, S. M., Jourdan, F., & Moyse, E. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00460-6 · Cited by 27 · see citing works
Rennick, R. E., Loesch, A., & Burnstock, G. (1992) · Thorax · doi:10.1136/thx.47.12.1044 · Cited by 27 · see citing works
Nishimura, T. (2002) · Chemical Senses · doi:10.1093/chemse/27.1.13 · Cited by 27 · see citing works
A Method for Maintaining Odor-responsive Adult Rat Olfactory Receptor Neurons in Short-term Culture
Vargas, G. (1999) · Chemical Senses · doi:10.1093/chemse/24.2.211 · Cited by 26 · see citing works
AVP Induces Myogenesis through the Transcriptional Activation of the Myocyte Enhancer Factor 2
Scicchitano, B. M., Spath, L., Musarò, A., Molinaro, M., Adamo, S., & Nervi, C. (2002) · Molecular Endocrinology · doi:10.1210/mend.16.6.0854 · Cited by 24 · see citing works
McEntire, J. (2000) · Chemical Senses · doi:10.1093/chemse/25.1.93 · Cited by 23 · see citing works
Rennick, R. E., Milner, P., & Burnstock, G. (1993) · European Journal of Pharmacology · doi:10.1016/0014-2999(93)90575-3 · Cited by 19 · see citing works
Naro, F., Arcangelis, V. D., Sette, C., Ambrosio, C., Komati, H., Molinaro, M., Adamo, S., & Némoz, G. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m306941200 · Cited by 17 · see citing works
Tamaoki, J., Kondo, M., Takeuchi, S., Takemura, H., & Nagai, A. (1998) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/ajrcmb.19.2.3134 · Cited by 14 · see citing works
Kern, R. C., & Pitovski, D. Z. (1997) · Acta Oto-Laryngologica · doi:10.3109/00016489709113470 · Cited by 14 · see citing works
Tran, D., Durroux, T., Stelly, N., Seyer, R., Tordjmann, T., Combettes, L., & Claret, M. (1999) · Journal of Histochemistry & Cytochemistry · doi:10.1177/002215549904700314 · Cited by 11 · see citing works
Mineralocorticoid Receptors in the Mammalian Olfactory Mucosa
Robinson, A. M., Kern, R. C., Krozowski, Z. S., Foster, J. D., & Pitovski, D. Z. (1999) · Annals of Otology Rhinology & Laryngology · doi:10.1177/000348949910801009 · Cited by 11 · see citing works
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- Authors
- Levasseur, G., Baly, C., Grébert, D., Durieux, D., Salesse, R., & Caillol, M.
- Affiliations
- Neurobiologie de l'Olfaction et Modélisation en Imagerie (FR)
- Corresponding author
- Caillol, Monique
- ORCID
- Baly, Christine
- Venue
- European Journal of Neuroscience
- Publisher
- Wiley
- Published
- 2004-07-15
- Volume
- 20
- Issue
- 3
- Pages
- 658-670
- ISSN
- 0953-816X (ISSN-L)
- 1460-9568
- OpenAlex
- W2099523247
- Cited by
- 28
- References
- 45
- Citations by year
- 2024: 1 · 2023: 2 · 2022: 1 · 2020: 2 · 2019: 2 · 2018: 2 · 2015: 2 · 2013: 3 · 2012: 2
- FWCI
- 0.43
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- European Journal of Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Funders
- Institut National de la Recherche Agronomique
- Topics
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Life Sciences › Neuroscience › Sensory Systems › Ion Channels and Receptors
- Keywords
- vasopressin, olfactory epithelium, V1a receptor, V1b receptor, olfactory sensory neurons, sustentacular cells, globose basal cells, Bowman's glands, calcium signaling, neuropeptides, receptor localization
- MeSH terms
- Animals, Animals, Newborn, Arginine Vasopressin, Boron Compounds, Calcium, Calcium Channel Blockers, Cells, Cultured, Chelating Agents, Dose-Response Relationship, Drug, Drug Interactions, Egtazic Acid, Enzyme Inhibitors, Estrenes, Extracellular Space, Immunohistochemistry, Male, Neurons, Olfactory Mucosa, Oxytocin, Pyrrolidinones, RNA, Messenger, Time Factors, Verapamil, Fura-2, Rats, Sprague-Dawley, Receptors, Vasopressin, Receptors, Oxytocin, Cadmium Chloride, Thapsigargin, Reverse Transcriptase Polymerase Chain Reaction, Rats
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