S100Z is expressed in a lateral subpopulation of olfactory receptor neurons in the main olfactory system of Xenopus laevis.

amphibian calcium-binding protein frog larval olfaction tadpole vomeronasal organ

Journal

Developmental neurobiology
ISSN: 1932-846X
Titre abrégé: Dev Neurobiol
Pays: United States
ID NLM: 101300215

Informations de publication

Date de publication:
04 Mar 2024
Historique:
revised: 07 02 2024
received: 20 12 2023
accepted: 15 02 2024
medline: 5 3 2024
pubmed: 5 3 2024
entrez: 5 3 2024
Statut: aheadofprint

Résumé

In contrast to other S100 protein members, the function of S100 calcium-binding protein Z (S100Z) remains largely uncharacterized. It is expressed in the olfactory epithelium of fish, and it is closely associated with the vomeronasal organ (VNO) in mammals. In this study, we analyzed the expression pattern of S100Z in the olfactory system of the anuran amphibian Xenopus laevis. Using immunohistochemistry in whole mount and slice preparations of the larval olfactory system, we found exclusive S100Z expression in a subpopulation of olfactory receptor neurons (ORNs) of the main olfactory epithelium (MOE). S100Z expression was not co-localized with TP63 and cytokeratin type II, ruling out basal cell and supporting cell identity. The distribution of S100Z-expressing ORNs was laterally biased, and their average number was significantly increased in the lateral half of the olfactory epithelium. The axons of S100Z-positive neurons projected exclusively into the lateral and intermediate glomerular clusters of the main olfactory bulb (OB). Even after metamorphic restructuring of the olfactory system, S100Z expression was restricted to a neuronal subpopulation of the MOE, which was then located in the newly formed middle cavity. An axonal projection into the ventro-lateral OB persisted also in postmetamorphic frogs. In summary, S100Z is exclusively associated with the main olfactory system in the amphibian Xenopus and not with the VNO as in mammals, despite the presence of a separate accessory olfactory system in both classes.

Identifiants

pubmed: 38439531
doi: 10.1002/dneu.22935
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Deutsche Forschungsgemeinschaft
ID : 4113/4-1

Informations de copyright

© 2024 The Authors. Developmental Neurobiology published by Wiley Periodicals LLC.

Références

Ahuja, G., Ivandić, I., Saltürk, M., Oka, Y., Nadler, W., & Korsching, S. I. (2013). Zebrafish crypt neurons project to a single, identified mediodorsal glomerulus. Scientific Reports, 3, 2063. https://doi.org/10.1038/srep02063
Bear, D. M., Lassance, J.-M., Hoekstra, H. E., & Datta, S. R. (2016). The evolving neural and genetic architecture of vertebrate olfaction. Current Biology, 26, R1039-R1049. https://doi.org/10.1016/j.cub.2016.09.011
Berridge, M. J., Bootman, M. D., & Roderick, H. L. (2003). Calcium signalling: Dynamics, homeostasis and remodelling. Nature Reviews Molecular Cell Biology, 4, 517-529. https://doi.org/10.1038/nrm1155
Berridge, M. J., Lipp, P., & Bootman, M. D. (2000). The versatility and universality of calcium signalling. Nature Reviews Molecular Cell Biology, 1, 11-21. https://doi.org/10.1038/35036035
Bettini, S., Milani, L., Lazzari, M., Maurizii, M. G., & Franceschini, V. (2017). Crypt cell markers in the olfactory organ of Poecilia reticulata: Analysis and comparison with the fish model Danio rerio. Brain Structure and Function, 222, 3063-3074. https://doi.org/10.1007/s00429-017-1386-2
Biechl, D., Tietje, K., Ryu, S., Grothe, B., Gerlach, G., & Wullimann, M. F. (2017). Identification of accessory olfactory system and medial amygdala in the zebrafish. Scientific Reports, 7, 44295. https://doi.org/10.1038/srep44295
Braubach, O. R., Fine, A., & Croll, R. P. (2012). Distribution and functional organization of glomeruli in the olfactory bulbs of zebrafish (Danio rerio). Journal of Comparative Neurology, 520, 2317-2339. https://doi.org/10.1002/cne.23075
Burguera, D., Dionigi, F., Kverková, K., Winkler, S., Brown, T., Pippel, M., Zhang, Y., Shafer, M., Nichols, A. L. A., Myers, E., Němec, P., & Musilova, Z. (2023). Expanded olfactory system in ray-finned fishes capable of terrestrial exploration. BMC Biology, 21, 163. https://doi.org/10.1186/s12915-023-01661-8
Capsoni, S., Iseppe, A. F., Casciano, F., & Pignatelli, A. (2021). Unraveling the role of dopaminergic and calretinin interneurons in the olfactory bulb. Frontiers in Neural Circuits, 15, 718221. https://doi.org/10.3389/fncir.2021.718221
Carafoli, E., Santella, L., Branca, D., & Brini, M. (2001). Generation, control, and processing of cellular calcium signals. Critical Reviews in Biochemistry and Molecular Biology, 36, 107-260. https://doi.org/10.1080/20014091074183
Cervino, A. S., Paz, D. A., & Frontera, J. L. (2017). Neuronal degeneration and regeneration induced by axotomy in the olfactory epithelium of Xenopus laevis. Developmental Neurobiology, 77, 1308-1320. https://doi.org/10.1002/dneu.22513
Date-Ito, A., Ohara, H., Ichikawa, M., Mori, Y., & Hagino-Yamagishi, K. (2008). Xenopus V1R vomeronasal receptor family is expressed in the main olfactory system. Chemical Senses, 33, 339-346. https://doi.org/10.1093/chemse/bjm090
Daume, D., Offner, T., Hassenklöver, T., & Manzini, I. (2022). Patterns of tubb2b promoter-driven fluorescence in the forebrain of larval Xenopus laevis. Frontiers in Neuroanatomy, 16, 914281. https://doi.org/10.3389/fnana.2022.914281
DeMaria, S., Berke, A. P., Name, E. V., Heravian, A., Ferreira, T., & Ngai, J. (2013). Role of a ubiquitously expressed receptor in the vertebrate olfactory system. Journal of Neuroscience, 33, 15235-15247. https://doi.org/10.1523/jneurosci.2339-13.2013
Dieris, M., Kowatschew, D., & Korsching, S. I. (2021). Olfactory function in the trace amine-associated receptor family (TAARs) evolved twice independently. Scientific Reports, 11, 7807. https://doi.org/10.1038/s41598-021-87236-5
Donato, R. (2003). Intracellular and extracellular roles of S100 proteins. Microscopy Research and Technique, 60, 540-551. https://doi.org/10.1002/jemt.10296
Elíes, J., Yáñez, M., Pereira, T. M. C., Gil-Longo, J., MacDougall, D. A., & Campos-Toimil, M. (2019). An update to calcium binding proteins. In M. Islam (Ed.), Advances in experimental medicine and biology. (pp. 183-213). Springer International Publishing. https://doi.org/10.1007/978-3-030-12457-1_8
Gayoso, J., Castro, A., Anadón, R., & Manso, M. J. (2012). Crypt cells of the zebrafish Danio rerio mainly project to the dorsomedial glomerular field of the olfactory bulb. Chemical Senses, 37, 357-369. https://doi.org/10.1093/chemse/bjr109
Germanà, A., Montalbano, G., Laurà, R., Ciriaco, E., del Valle, M. E., & Vega, J. A. (2004). S100 protein-like immunoreactivity in the crypt olfactory neurons of the adult zebrafish. Neuroscience Letters, 371, 196-198. https://doi.org/10.1016/j.neulet.2004.08.077
Germanà, A., Paruta, S., Germanà, G. P., Ochoa-Erena, F. J., Montalbano, G., Cobo, J., & Vega, J. A. (2007). Differential distribution of S100 protein and calretinin in mechanosensory and chemosensory cells of adult zebrafish (Danio rerio). Brain Research, 1162, 48-55. https://doi.org/10.1016/j.brainres.2007.05.070
Gliem, S., Syed, A. S., Sansone, A., Kludt, E., Tantalaki, E., Hassenklöver, T., Korsching, S. I., & Manzini, I. (2013). Bimodal processing of olfactory information in an amphibian nose: Odor responses segregate into a medial and a lateral stream. Cellular and Molecular Life Sciences, 70, 1965-1984. https://doi.org/10.1007/s00018-012-1226-8
Gonzalez, L. L., Garrie, K., & Turner, M. D. (2020). Role of S100 proteins in health and disease. Biochimica et Biophysica Acta (BBA)-Molecular Cell Research, 1867, 118677. https://doi.org/10.1016/j.bbamcr.2020.118677
Hansen, A., Anderson, K. T., & Finger, T. E. (2004). Differential distribution of olfactory receptor neurons in goldfish: Structural and molecular correlates. Journal of Comparative Neurology, 477, 347-359. https://doi.org/10.1002/cne.20202
Hansen, A., Reiss, J. O., Gentry, C. L., & Burd, G. D. (1998). Ultrastructure of the olfactory organ in the clawed frog, Xenopus laevis, during larval development and metamorphosis. Journal of Comparative Neurology, 398, 273-288. https://doi.org/10.1002/(SICI)1096-9861(19980824)398:2<273::AID-CNE8>3.0.CO;2-Y
Hecker, N., Lächele, U., Stuckas, H., Giere, P., & Hiller, M. (2019). Convergent vomeronasal system reduction in mammals coincides with convergent losses of calcium signalling and odorant-degrading genes. Molecular Ecology, 28, 3656-3668. https://doi.org/10.1111/mec.15180
Hermann, A., Donato, R., Weiger, T. M., & Chazin, W. J. (2012). S100 calcium binding proteins and ion channels. Frontiers in Pharmacology, 3, 67. https://doi.org/10.3389/fphar.2012.00067
Kerschbaum, H. H., & Hermann, A. (1992). Calcium-binding proteins in chemoreceptors of Xenopus laevis. Tissue & Cell, 24, 719-724. https://doi.org/10.1016/0040-8166(92)90043-7
Kishida, T. (2021). Olfaction of aquatic amniotes. Cell and Tissue Research, 383, 353-365. https://doi.org/10.1007/s00441-020-03382-8
Kishida, T., Thewissen, J., Hayakawa, T., Imai, H., & Agata, K. (2015). Aquatic adaptation and the evolution of smell and taste in whales. Zoological Letters, 1, 9. https://doi.org/10.1186/s40851-014-0002-z
Koide, T., Miyasaka, N., Morimoto, K., Asakawa, K., Urasaki, A., Kawakami, K., & Yoshihara, Y. (2009). Olfactory neural circuitry for attraction to amino acids revealed by transposon-mediated gene trap approach in zebrafish. Proceedings of the National Academy of Sciences, 106, 9884-9889. https://doi.org/10.1073/pnas.0900470106
Kraemer, A. M., Saraiva, L. R., & Korsching, S. I. (2008). Structural and functional diversification in the teleost S100 family of calcium-binding proteins. BMC Evolutionary Biology, 8, 48. https://doi.org/10.1186/1471-2148-8-48
Kress, S., Biechl, D., & Wullimann, M. F. (2015). Combinatorial analysis of calcium-binding proteins in larval and adult zebrafish primary olfactory system identifies differential olfactory bulb glomerular projection fields. Brain Structure and Function, 220, 1951-1970. https://doi.org/10.1007/s00429-014-0765-1
Miwa, N., & Kawamura, S. (2003). Frog p26olf, a molecule with two S100-like regions in a single peptide. Microscopy Research and Technique, 60, 593-599. https://doi.org/10.1002/jemt.10301
Mohrhardt, J., Nagel, M., Fleck, D., Ben-Shaul, Y., & Spehr, M. (2018). Signal detection and coding in the accessory olfactory system. Chemical Senses, 43, 667-695. https://doi.org/10.1093/chemse/bjy061
Moreno, N., Rétaux, S., & González, A. (2008). Spatio-temporal expression of Pax6 in Xenopus forebrain. Brain Research, 1239, 92-99. https://doi.org/10.1016/j.brainres.2008.08.052
Morona, R., & González, A. (2013). Pattern of calbindin-D28k and calretinin immunoreactivity in the brain of Xenopus laevis during embryonic and larval development. Journal of Comparative Neurology, 521, 79-108. https://doi.org/10.1002/cne.23163
Nieuwkoop, P. D., & Faber, J. (Eds.). (1994). Normal table of Xenopus laevis (Daudin). Garland Science.
Offner, T., Weiss, L., Daume, D., Berk, A., Inderthal, T. J., Manzini, I., & Hassenklöver, T. (2023). Functional odor map heterogeneity is based on multifaceted glomerular connectivity in larval Xenopus olfactory bulb. iScience, 26, 107518. https://doi.org/10.1016/j.isci.2023.107518
Oka, Y., Saraiva, L. R., & Korsching, S. I. (2012). Crypt neurons express a single v1r-related ora gene. Chemical Senses, 37, 219-227. https://doi.org/10.1093/chemse/bjr095
Preibisch, S., Saalfeld, S., & Tomancak, P. (2009). Globally optimal stitching of tiled 3D microscopic image acquisitions. Bioinformatics, 25, 1463-1465. https://doi.org/10.1093/bioinformatics/btp184
Qi, Y., Cheng, H., Wang, Y., & Chen, Z. (2022). Revealing the precise role of calretinin neurons in epilepsy: We are on the way. Neuroscience Bulletin, 38, 209-222. https://doi.org/10.1007/s12264-021-00753-1
Sansone, A., Hassenklöver, T., Syed, A. S., Korsching, S. I., & Manzini, I. (2014). Phospholipase C and diacylglycerol mediate olfactory responses to amino acids in the main olfactory epithelium of an amphibian. PLoS ONE, 9, e87721. https://doi.org/10.1371/journal.pone.0087721
Sansone, A., Syed, A. S., Tantalaki, E., Korsching, S. I., & Manzini, I. (2014). Trpc2 is expressed in two olfactory subsystems, the main and the vomeronasal system of larval Xenopus laevis. Journal of Experimental Biology, 217, 2235-2238. https://doi.org/10.1242/jeb.103465
Santamaria-Kisiel, L., Rintala-Dempsey, A. C., & Shaw, G. S. (2006). Calcium-dependent and -independent interactions of the S100 protein family. Biochemical Journal, 396, 201-214. https://doi.org/10.1042/bj20060195
Sato, Y., Miyasaka, N., & Yoshihara, Y. (2005). Mutually exclusive glomerular innervation by two distinct types of olfactory sensory neurons revealed in transgenic zebrafish. Journal of Neuroscience, 25, 4889-4897. https://doi.org/10.1523/jneurosci.0679-05.2005
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., Tinevez, J. Y., White, D. J., Hartenstein, V., Eliceiri, K., Tomancak, P., & Cardona, A. (2012). Fiji: An open-source platform for biological-image analysis. Nature Methods, 9, 676-682. https://doi.org/10.1038/nmeth.2019
Schnittke, N., Herrick, D. B., Lin, B., Peterson, J., Coleman, J. H., Packard, A. I., Jang, W., & Schwob, J. E. (2015). Transcription factor p63 controls the reserve status but not the stemness of horizontal basal cells in the olfactory epithelium. Proceedings of the National Academy of Sciences of the United States of America, 112(36), E5068-E5077. https://doi.org/10.1073/pnas.1512272112
Schwaller, B. (2020). Cytosolic Ca2+ buffers are inherently Ca2+ signal modulators. Cold Spring Harbor perspectives in biology, 12, a035543. https://doi.org/10.1101/cshperspect.a035543
Singh, P., & Ali, S. A (2022). Multifunctional role of S100 protein family in the immune system: An update. Cells, 11, 2274. https://doi.org/10.3390/cells11152274
Stoykova, A., & Gruss, P. (1994). Roles of Pax-genes in developing and adult brain as suggested by expression patterns. Journal of Neuroscience, 14, 1395-1412. https://doi.org/10.1523/jneurosci.14-03-01395.1994
Syed, A. S., Sansone, A., Hassenklöver, T., Manzini, I., & Korsching, S. I. (2017). Coordinated shift of olfactory amino acid responses and V2R expression to an amphibian water nose during metamorphosis. Cellular and Molecular Life Sciences, 74, 1711-1719. https://doi.org/10.1007/s00018-016-2437-1
Syed, A. S., Sansone, A., Nadler, W., Manzini, I., & Korsching, S. I. (2013). Ancestral amphibian v2rs are expressed in the main olfactory epithelium. Proceedings of the National Academy of Sciences, 110, 7714-7719. https://doi.org/10.1073/pnas.1302088110
Syed, A. S., Sharma, K., Policarpo, M., Ferrando, S., Casane, D., & Korsching, S. I. (2023). Ancient and nonuniform loss of olfactory receptor expression renders the shark nose a de facto vomeronasal organ. Molecular Biology and Evolution, 40, msad076. https://doi.org/10.1093/molbev/msad076
Taniguchi, K., & Taniguchi, K. (2014). Phylogenic studies on the olfactory system in vertebrates. Journal of Veterinary Medical Science, 76, 781-788. https://doi.org/10.1292/jvms.13-0650
Wei, H., Lang, M.-F., & Jiang, X. (2013). Calretinin is expressed in the intermediate cells during olfactory receptor neuron development. Neuroscience Letters, 542, 42-46. https://doi.org/10.1016/j.neulet.2013.03.022
Weiss, L., Manzini, I., & Hassenklöver, T. (2021). Olfaction across the water-air interface in anuran amphibians. Cell and Tissue Research, 383, 301-325. https://doi.org/10.1007/s00441-020-03377-5
Yáñez, M., Gil-Longo, J., & Campos-Toimil, M. (2012). Calcium binding proteins. In Calcium Signaling (pp. 461-482). Springer Netherlands. https://doi.org/10.1007/978-94-007-2888-2_19

Auteurs

Melina Kahl (M)

Institute of Animal Physiology, Department of Animal Physiology and Molecular Biomedicine, Justus-Liebig-University Giessen, Giessen, Germany.

Thomas Offner (T)

Institute of Animal Physiology, Department of Animal Physiology and Molecular Biomedicine, Justus-Liebig-University Giessen, Giessen, Germany.

Alena Trendel (A)

Institute of Animal Physiology, Department of Animal Physiology and Molecular Biomedicine, Justus-Liebig-University Giessen, Giessen, Germany.

Lukas Weiss (L)

Institute of Animal Physiology, Department of Animal Physiology and Molecular Biomedicine, Justus-Liebig-University Giessen, Giessen, Germany.

Ivan Manzini (I)

Institute of Animal Physiology, Department of Animal Physiology and Molecular Biomedicine, Justus-Liebig-University Giessen, Giessen, Germany.

Thomas Hassenklöver (T)

Institute of Animal Physiology, Department of Animal Physiology and Molecular Biomedicine, Justus-Liebig-University Giessen, Giessen, Germany.

Classifications MeSH