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Homer 1b/c expression correlates with zebrafish olfactory system development

  • Published:
Journal of Neurocytology

Abstract

The zebrafish, (Danio rerio) is an important model organism for the analysis of molecular mechanisms that govern neuronal circuit development. The neuronal circuitry that mediates olfaction is crucial for the development and survival of all teleost fishes. In concert with other sensory systems, olfaction is functional at early stages in zebrafish development and mediates important behavioral and survival strategies in the developing larva. Odorant cues are transduced by an array of signaling molecules from receptors in olfactory sensory neurons. The scaffolding protein family known as Homer is well placed to orchestrate this signaling cascade by interacting with and coupling membrane bound receptors to cytosolic signaling partners. To date, Homer has not been demonstrated in the zebrafish. Here we report that the Homer 1b/c isoform was prominent in the olfactory system from the earliest stages of differentiation. We describe the spatial and temporal distribution of Homer in the zebrafish olfactory system. At 24 hours post fertilization (hpf), Homer expression delineated the boundary of the presumptive olfactory placode. Subsequent expression steadily increased throughout the developing olfactory placode, with a prominent localization to the dendritic knobs of the olfactory sensory neurons. Homer expression in the developing olfactory bulb was punctate and prominent in the glomeruli, displaying an apparent synaptic localization. This work supports the hypothesis that Homer is an important molecule in neuronal circuit development, necessary for crucial behaviors required for development and survival.

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References

  • ANGO, F., PIN, J.-P., TU, J. C., XIAO, B., WORLEY, P. F., BOCKAERT, J. & FAGNI, L. (2000) Dendritic and axonal targeting of type 5 metabotropic glutamate receptor is regulated by Homer1 proteins and neuronal excitation. The Journal of Neuroscience 20, 8710–9716.

    CAS  PubMed  Google Scholar 

  • ANGO, F., ROBBE, D., TU, J. C., XIAO, B., WORLEY, P. F., PIN, J.-P., BOCKAERT, J. & FAGNI, L. (2002) Homer-dependent cell surface expression of metabotropic glutamate receptor Type 5 in neurons. Molecular and Cellular Neuroscience 20, 323–329.

    Article  CAS  PubMed  Google Scholar 

  • BAIER, H. & KORSCHING, S. (1994a) Olfactory glomeruli in the zebrafish form an invariant pattern and are identifiable across animals. The Journal of Neuroscience 14, 219–230.

    CAS  Google Scholar 

  • BAIER, H., ROTTER, S. & KORSCHING, S. (1994b) Connectional topography in the Zebrafish olfactory system: Random positions but regular spacing of sensory neurons projecting to an individual gomerulus. Proceedings of the National Academy of Sciences 91, 11646–11650.

  • BARTH, A., JUSTICE, N. & NGAI, J. (1996) Asynchronous onset of odorant receptor expression in the developing zebrafish olfactory system. Neuron 16, 23–34.

    Article  CAS  PubMed  Google Scholar 

  • BRAKEMAN, P. R., LANAHAN, A. A., O'BRIEN, R., ROCHE, K., BARNES, C. A., HUGANIR, R. L. & WORLEY, P. F. (1997) Homer: A protein that selectively binds metabotropic glutamate receptors. Nature 386, 284–288.

    Article  CAS  PubMed  Google Scholar 

  • BYRD, C. A. & BRUNJES, P. C. (1995) Organization of the olfactory system in the adult zebrafish - histological, immunohistochemical, and quantitative analysis. The Journal of Comparative Neurology 358, 247–259.

    Article  CAS  PubMed  Google Scholar 

  • BYRD, C. A. & BRUNJES, P. C. (2001) Neurogenesis in the olfactory bulb of adult zebrafish. Neuroscience 105, 793–801.

    Article  CAS  PubMed  Google Scholar 

  • CHENG, S., CHRISTIE, T. & VALDIMARSSON, G. (2003) Expression of Connexin48.5, Connexin44.1, and Connexin43 during zebrafish (danio rerio) lens development. Developmental Dynamics 228, 709–715.

    CAS  PubMed  Google Scholar 

  • CIRUELA, F., SOLOVIEV, M. M., CHAN, W.-Y. & MCILHINNEY, R. A. J. (2000) Homer-1c/vesl-1L modulates the cell surface targeting of metabotropic glutamate receptor type 1α: Evidence for an anchoring function. Molecular and Cellular Neuroscience 15, 36–50.

    Article  CAS  PubMed  Google Scholar 

  • DIAGANA, T. T., THOMAS, U., PROKOPENKO, S. N., XIOAO, B., WORLEY, P. F. & THOMAS, J. B. (2002) Mutation of drosophila Homer disrupts control of locomotor activity and behavioral plasticity. The Journal of Neuroscience 22, 428–436.

    CAS  PubMed  Google Scholar 

  • DYNES, J. L. & NGAI, J. (1998) Pathfinding of olfactory neuron axons to stereotyped glomerular targets revealed by dynamic imaging in living zebrafish embryos. Neuron 20, 1081–1091.

    Article  CAS  PubMed  Google Scholar 

  • EDWARDS, J. & MICHEL, W. (2002) Odor-stimulated glutamatergic neurotransmission in the zebrafish olfactory bulb. The Journal of Comparative Neurology 454, 294– 309.

    Article  CAS  PubMed  Google Scholar 

  • FOA, L., RAJAN, I., HASS, K., WU, G.-Y., BRAKEMAN, P., WORLEY, P. F. & CLINE, H. (2001) The scaffold protein, Homer1b/c, regulates axon pathfinding in the central nervous system in vivo. Nature Neuroscience 4, 499–506.

    CAS  PubMed  Google Scholar 

  • FOA, L., JENSEN, K., RAJAN, I., BRONSON, K., GASPERINI, R., WORLEY, P. F., TU, J. C. & CLINE, H. T. (2005) Homer expression in the Xenopus tadpole nervous system. The Journal of Comparative Neurology. (In Press).

  • HANSEN, A. & ZEISKE, E. (1993) Devlopment of the olfactory organ in the zebrafish, Brachydanio rerio. The Journal of Comparative Neurology 333, 289–300.

    Article  CAS  PubMed  Google Scholar 

  • HANSEN, A., ROLEN, S. H., ANDERSON, K., MORITA, Y., CAPRIO, J. & FINGER, T. E. (2003) Correlation between olfactory receptor cell type and function in the channel catfish. The Journal of Neuroscience 23, 9328–9339.

    CAS  PubMed  Google Scholar 

  • HANSEN, A., ANDERSON, K. T. & FINGER, T. E. (2004) Differential distribution of olfactory receptor neurons in goldfish: Structural and molecular correlates. The Journal of Comparative Neurology 477, 347–359.

    Article  CAS  PubMed  Google Scholar 

  • HANSEN, A., ROLEN, S. H., ANDERSON, K., MORITA, Y., CAPRIO, J. & FINGER, T. E. (2005) Olfactory receptor neurons in fish: Structural, molecular and functional correlates. Chemical Senses 30, 311.

    Article  Google Scholar 

  • KAMMERMEIER, P. J., XIAO, B., TU, J. C., WORLEY, P. F. & IKEDA, S. R. (2000) Homer proteins regulate coupling of group I metabotropic glutamate receptors to N-type calcium and M-type potassium channels. The Journal of Neuroscience 20, 7238–7245.

    CAS  PubMed  Google Scholar 

  • KATO, A., OZAWA, F., SAITOH, Y., HIRAI, K. & INOKUCHI, K. (1997) vesl, a gene encoding VASP/Ena family related protein, is upregulated during seizure, long-term potentiation and synaptogenesis. FEBS Letters 412, 183–189.

    Article  CAS  PubMed  Google Scholar 

  • KATO, A., OZAWA, F., SAITOH, Y., FUKAZAWA, Y., SUGIYAMA, H. & INOKUCHI, K. (1998) Novel members of the Vesl/Homer family of PDZ proteins that bind metabotropic glutamate receptors. The Journal of Biological Chemistry 273, 23969–23975.

    CAS  PubMed  Google Scholar 

  • KIMMEL, C., BALLARD, W., KIMMEL, S., ULLMANN, B. & SCHILLING, T. (1995) Stages of embryonic development of the zebrafish. Developmental Dynamics 203, 253–310.

    CAS  PubMed  Google Scholar 

  • LITTLE, E. E. (1983) Behavioral function of olfaction and taste in fish. In: Northcutt, R. & Davis, R. Fish Neurobiolgy. University of Michigan Press, Ann Arbor, MI, pp. 351–375.

    Google Scholar 

  • MENCO, B. P. & MORRISON, E. E. (2003) Morphology of the mammalian olfactory epithelium: Form, fine structure, function and pathology. In Handbook of Olfaction and Gustation (Doty, R. L.) pp. 17–49. New York: Marcel Dekker Inc.

    Google Scholar 

  • NEDIVI, E., HEVRONI, D., NAOT, D., ISRAELI, D. & CITRI, Y. (1993) Numerous candidate plasticity-related genes revealed by differential cDNA cloning. Nature 363, 718–722.

    Article  CAS  PubMed  Google Scholar 

  • RHEIN, L. D. & CAGAN, R. H. (1983) Biochemical studies of olfaction: Binding specificity of odorants to a cilia preparation from rainbow trout olfactory rosettes. The Journal of Neurochemistry 41, 569–577.

    CAS  Google Scholar 

  • ROCHE, K. W., TU, J. C., PETRALIA, R. S., XIAO, B., WENTHOLD, R. J. & WORLEY, P. F. (1999) Homer 1b regulates the trafficking of group I metabotropic glutamate receptors. The Journal of Biological Chemistry 274, 25953–25957.

    Article  CAS  PubMed  Google Scholar 

  • SALA, C., VALENTIN, P., WILSON, N. R., PASSAFARO, M., LIU, G. & SHENG, M. (2001) Regulation of dendritic spine morphology and synaptic function by Shank and Homer. Neuron 31, 115–130.

    Article  CAS  PubMed  Google Scholar 

  • SHIRAISHI, Y., MIZUTANI, A., BITO, H., FUJISAWA, K., NARUMIYA, S., MIKOSHIBA, K. & FURUICHI, T. (1999) Cupidin, an isoform of Homer/Vesl, interacts with the actin cytoskeleton and activated rho family small GTPases and is expressed in developing mouse cerebellar granule cells. The Journal of Neuroscience 19, 8389–8400.

    CAS  PubMed  Google Scholar 

  • SONG, H. J. & POO, M. M. (1999) Signal transduction underlying growth cone guidance by diffusible factors. Current Opinion in Neurobiology 9, 355–363.

    Article  CAS  PubMed  Google Scholar 

  • STABELL, O. B. (1984) Homing and olfaction in salmonids: A critical review with special reference to the atlantic salmon. Biological Reviews 59, 333–388.

    CAS  Google Scholar 

  • TADOKORO, S., TACHIBANA, T., IMANAKA, T., NISHIDA, W. & SOBUE, K. (1999) Involvement of unique leucine-zipper motif of PSD-Zip45 (Homer 1c/vesl-1L) in group 1 metabotropic glutamate receptor clustering. Proceedings of the National Academy of Sciences USA 96, 13801–13806.

  • TREVARROW, B., MARKS, K. & KIMMEL, C. (1990) Organization of hindbrain segments in the zebrafish embyo. Neuron 4, 669–679.

    Article  CAS  PubMed  Google Scholar 

  • TU, J. C., XIAO, B., YUAN, J. P., LANAHAN, A. A., LEOFFERT, K., LI, M., LINDEN, D. J. & WORLEY, P. F. (1998) Homer binds a novel proline-rich motif and links group 1 metabotropic glutamate receptors with IP3 receptors. Neuron 21, 717–726.

    Article  CAS  PubMed  Google Scholar 

  • TU, J. C., XIAO, B., NAISBITT, S., YUAN, J. P., PETRALIA, R. S., BRAKEMAN, P., DOAN, A., AAKALU, V. K., LANAHAN, A. A., SHENG, M. & WORLEY, P. F. (1999) Coupling of mGluR/Homer and PSD-95 complexes by the Shank family of postsynaptic density proteins. Neuron 23, 583–592.

    Article  CAS  PubMed  Google Scholar 

  • USUI, S., KONNO, D., HORI, K., MARUOKA, H., OKABE, S., FJIKADO, T., TANO, Y. & SOBUE, K. (2003) Synaptic targeting of PSD-Zip45 (Homer1c) and its involvement in the synaptic accumulation of F-actin. The Journal of Biological Chemistry 278, 10619– 10628.

    CAS  PubMed  Google Scholar 

  • WEBER, S. & ROSS, L. (2003) Gap junctional coupling in the olfactory organ of zebrafish embryos. Developmental Brain Research 143, 25–31.

    Article  CAS  PubMed  Google Scholar 

  • WESTERFIELD, M. (1995) The Zebrafish Book. Eugene: Univ. of Oregon Press.

    Google Scholar 

  • WHITLOCK, K. E. & WESTERFIELD, M. (1998) A transient population of neurons pioneers the olfactory pathway in the zebrafish. The Journal of Neuroscience 18, 8919– 8927.

    CAS  PubMed  Google Scholar 

  • XIAO, B., TU, J. C., PETRALIA, R. S., YUAN, J. P., DOAN, A., BREDER, C. D., RUGGIERO, A., LANAHAN, A. A., WENTHOLD, R. J. & WORLEY, P. F. (1998) Homer regulates the association of group 1 metabotropic glutamate receptors with multivalent complexes of homer-related, synaptic proteins. Neuron 21, 707–716.

    Article  CAS  PubMed  Google Scholar 

  • XIAO, B., TU, J. & WORLEY, P. (2000) Homer: A link between neural activity and glutamate receptor function. Current Opinion in Neurobiology 10, 370–374.

    Article  CAS  PubMed  Google Scholar 

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Correspondence to Lisa Foa.

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Gasperini, R., Foa, L. Homer 1b/c expression correlates with zebrafish olfactory system development. J Neurocytol 33, 671–680 (2004). https://doi.org/10.1007/s11068-005-3335-x

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  • DOI: https://doi.org/10.1007/s11068-005-3335-x

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