Skip to main content
SpringerLink
Log in

Development of human olfactory bulbs in prenatal ontogenesis: An immunochistochemical study with markers of presynaptic terminals (anti-SNAP-25, synapsin-I, and synaptophysin)

  • Developmental Biology of Mammals
  • Published:
Russian Journal of Developmental Biology Aims and scope Submit manuscript

Abstract

Data on olfactory bulb (OB) development in human fetuses in the stages from the 8th week to birth is provided. Immunohistochemical markers of presynaptic terminals (anti-SNAP-25, synapsin-I, and synaptophysin) were used to evaluate the maturation of the OB. Differentiation of the OB layers begins from the periphery, which indirectly confirms that growth of the olfactory nerve fibers induces not only the anatomical differentiation of the OB but also the differentiation of its functional layers. The sites of the developing glomeruli are revealed using the immunohistochemical procedure prior to the stage in which distinct glomeruli can be identified using a common histological procedure. The OB conductive system demonstrates immunoreactivity with the antibodies to presynaptic proteins at all stages starting with the 10th–11th weeks of fetal development. Four stages of OB development are described. All functional layers of the OB are mature at the 22nd week stage. Further differentiation of the neuroblasts in the OB, including lamina formation of the internal granular layer and the glomerular layer development, and the growth of the OB continue after the 20th–22nd week stage until 38th–40th weeks of fetal development. Patterns of the immunoreactivity with antibodies to SNAP-25, synapsin-I, and synaptophysin at the 38th-40th weeks of prenatal development are fully consistent with those of the adult OB. Complete maturity of the human OB is reached at the 38th–40th week of prenatal development.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Biranowska, J., Dziewiatkowski, J., Ludkiewicz, B., and Morys, J., Developmental changes of synaptic proteins expression within the hippocampal formation of the rat, J. Anat. Embryol., (Berlin), 2002, vol. 206, nos. 1–2, pp. 85–96.

    Article  CAS  Google Scholar 

  • Bossy, J., Development of olfactory and related structures in staged human embryos, Anat. Embryol., 1980, vol. 161, pp. 225–236.

    Article  CAS  PubMed  Google Scholar 

  • Catsicas, S., Larhammar, D., Blomqvist, A., Sanna, P.P., Milner, R.J., and Wilson, M.C., Expression of a conserved cell-type-specific protein in nerve terminals coincides with synaptogenesis, Proc. Natl. Acad. Sci. U.S.A., 1991, vol. 88, no. 3, pp. 785–789.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chuah, M.I. and Zheng, D.R., Olfactory marker protein is present in olfactory receptor cells of human fetuses, Neuroscience, 1987, vol. 23, pp. 263–370.

    Article  Google Scholar 

  • Chuah, M.I. and Zheng, D.R., The human primary olfactory pathway: fine structural and cytochemical aspects during development and in adults, Microsc. Res. Tech., 1992, vol. 23, no. 1, pp. 76–85.

    Article  CAS  PubMed  Google Scholar 

  • DeCamilli, P., Cameron, R., and Greengard, P., Synapsin I (protein I), a nerve terminal-specific phosphoprotein. I. Its general distribution in synapses of the central and peripheral nervous system demonstrated by immunofluorescence in frozen and plastic sections, J. Cell Biol., 1983, vol. 96, no. 5, pp. 1337–1354.

    Article  CAS  Google Scholar 

  • Doty, R.L., Olfaction in Parkinson’s disease and related disorders, Neurobiol. Dis., 2012, vol. 46, no. 3, pp. 527–552.

    Article  PubMed Central  PubMed  Google Scholar 

  • Duc, C. and Catsicas, S., Ultrastructural localization of SNAP-25 within the rat spinal cord and peripheral nervous system, J. Comp. Neurol., 1995, vol. 356, no. 1, pp. 152–163.

    Article  CAS  PubMed  Google Scholar 

  • Fletcher, T.L., Cameron, P., DeCamilli, P., and Banker, G., The distribution of synapsin I and synaptophysin in hippocampal neurons developing in culture, J. Neurosci., 1991, vol. 11, pp. 1617–1626.

    CAS  PubMed  Google Scholar 

  • Fornasiero, E.F., Bonanomi, D., Benfenati, F., and Valtorta, F., The role of synapsins in neuronal development, Cell. Mol. Life. Sci., 2010, vol. 67, no. 9, pp. 1383–1396.

    Article  CAS  PubMed  Google Scholar 

  • Goutan, E., Martí, E., and Ferrer, I., Expression of synaptic proteins in the developing rat cerebellum following ionizing radiation, Int. J. Dev. Neurosci., 1999, vol. 17, no. 4, pp. 275–283.

    Article  CAS  PubMed  Google Scholar 

  • Greenlee, M.H., Roosevelt, C.B., and Sakaguchi, D.S., Differential localization of SNARE complex proteins SNAP-25, syntaxin, and VAMP during development of the mammalian retina, J. Comp. Neurol., 2001, vol. 430, no. 3, pp. 306–320.

    Article  CAS  PubMed  Google Scholar 

  • Grubb, M.S., Nissant, A., Murray, K., and Lledo, P.M., Functional maturation of the first synapse in olfaction: development and adult neurogenesis, J. Neurosci., 2008, vol. 28, no. 11, pp. 2919–2932.

    Article  CAS  PubMed  Google Scholar 

  • Hepp, R. and Langley, K., SNAREs during development, Cell. Tissue Res., 2001, vol. 305, pp. 247–253.

    Article  CAS  PubMed  Google Scholar 

  • Huart, C., Rombaux, P., and Hummel, T., Plasticity of the human olfactory system: the olfactory bulb, Molecules, 2013, vol. 18, no. 9, pp. 11586–11600.

    Article  CAS  PubMed  Google Scholar 

  • Humphrey, T., The development of the olfactory and accessory olfactory formations in human embryos and fetuses, J. Comp. Neurol., 1940, vol. 73, pp. 431–468.

    Article  Google Scholar 

  • Ichikawa, M., Kimura-Kuroda, J., Yasui, K., and Kuroda, Y., Expression of synaptophysin during synapse formation between dissociated cortical neurons, Neurosci. Res., 1991, vol. 12, no. 3, pp. 452–458.

    Article  CAS  PubMed  Google Scholar 

  • Kimura, M., Umehara, T., Udagawa, J., Kawauchi, H., and Otani, H., Development of olfactory epithelium in the human fetus: scanning electron microscopic observations, Congenit. Anom. (Kyoto), 2009, vol. 49, no. 3, pp. 102–107.

    Article  Google Scholar 

  • Knaus, P., Betz, H., and Rehm, H., Expression of synaptophysin during postnatal development of the mouse brain, J. Neurochem., 1986, vol. 47, no. 4, pp. 1302–1304.

    Article  CAS  PubMed  Google Scholar 

  • Kulakovskaya, V.S., Observations on the sense of taste and smell in newborns, Zhur. Izuch. Ran. Det. Vozr., 1929, vol. 9, no. 1, pp. 15–20.

    Google Scholar 

  • Leclerc, N., Beesley, P.W., Brown, I., Colonnier, M., Gurd, J.W., Paladino, T., and Hawkes, R., Synaptophysin expression during synaptogenesis in the rat cerebellar cortex, J. Comp. Neurol., 1989, vol. 280, no. 2, pp. 197–212.

    Article  CAS  PubMed  Google Scholar 

  • Lin, D.M. and Ngai, J., Development of the vertebrate main olfactory system, Curr. Opin. Neurobiol., 1999, vol. 9, pp. 74–78.

    Article  CAS  PubMed  Google Scholar 

  • Mason, C.A., Axon development in mouse cerebellum: embryonic axon forms and the expression of synapsin I, Neuroscience, 1987, vol. 19, pp. 1319–1333.

    Article  Google Scholar 

  • Mennella, J.A., Jagnow, C.P., and Beauchamp, G.K., Prenatal and postnatal flavor learning by human infants, Pediatrics, 2001, vol. 107, no. 6, p. E88.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Moran, DT., Rowley, J.C. 3rd, Jafek, B.W., and Lovell, M.A., The fine structure of the olfactory mucosa in man, J. Neurocytol., 1982, vol. 11, no. 5, pp. 721–746.

    Article  CAS  PubMed  Google Scholar 

  • Muller, F. and O’Rahilly, R., Olfactory structures in staged human embryos, Cells Tissues Organs, 2004, vol. 178, pp. 93–116.

    Article  CAS  PubMed  Google Scholar 

  • Nadarajah, B. and Parnavelas, J.G., Mode of neuronal migration in the developing cerebral cortex, Nat. Rev. Neurosci., 2002, vol. 3, pp. 423–443.

    Article  CAS  PubMed  Google Scholar 

  • Nieuwenhuys, R., The Central Nervous System of Vertebrates, Berlin: Springer-Verlag, 1998, vol. 3.

    Book  Google Scholar 

  • Oyler, G.A., Polli, J.W., Wilson, M.C., and Billingsley, M.L., Developmental expression of the 25-kDa synaptosomal-associated protein (SNAP-25) in rat brain, Proc. Natl. Acad. Sci USA, 1991, vol. 88, no. 12, pp. 5247–5251.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pearson, A.A., The development of the olfactory nerve in man, J. Comp. Neurol., 1941, vol. 75, pp. 199–217.

    Article  Google Scholar 

  • Pearson, A.A., The development of the olfactory nerve, the nervus terminalis, and the vomeronasal nerve in man, Ann. Otol. Rhinol. Laryngol., 1942, vol. 51, no. 2, pp. 317–332.

    Article  Google Scholar 

  • Petten, B.M., Embriologiya cheloveka (Human Embryology), Moscow: Medgiz, 1959.

    Google Scholar 

  • Pyatkina, G.A., The development of human olfactory receptors, Tsitologiya, 1982, vol. 24, no. 1, pp. 11–16.

    Google Scholar 

  • Rakic, P., Mode of cell migration to the superficial layers of fetal monkey neocortex, J. Comp. Neur., 1972, vol. 145, no. 1, pp. 61–84.

    Article  CAS  PubMed  Google Scholar 

  • Salasar, I., Quintiero, P.S., Lombardero, M., Aleman, N., and Fernandez de Troconiz, P., The prenatal maturity of the accessory olfactory bulb in pigs, Chem. Senses, 2004, vol. 29, no. 1, pp. 3–11.

    Article  Google Scholar 

  • Schaal, B., Marlier, L., and Soussignan, R., Human foetuses learn odours from their pregnant mother’s diet, Chem. Senses, 2000, vol. 25, pp. 729–737.

    Article  CAS  PubMed  Google Scholar 

  • Sidor-Kaczmarek, J., Labuda, C., Litwinowicz, B., Spodnik, J.H., Kowian-ski, P., Dziewiatkowski, J., and Moryś, J., Developmental expression of SNAP-25 protein in the rat striatum and cerebral cortex, Folia Morphol. (Warsz), 2004, vol. 63, no. 3, pp. 285–288.

    Google Scholar 

  • Sollner, T., Bennett, M.K., Whiteheart, S.W., Scheller, R.H., and Rothman, J.E., A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation, and fusion, Cell, 1993, vol. 75, no. 3, pp. 409–418.

    Article  CAS  PubMed  Google Scholar 

  • Takahashi, S., Iwanaga, T., Takahashi, Y., Nakano, Y., and Fujita, T., Neuron-specific enolase, neurofilament protein and S-100 protein in the olfactory mucosa of human fetuses. An immunohistochemical study, Cell. Tissue. Res., 1984, vol. 238, no. 2, pp. 231–234.

    Article  CAS  PubMed  Google Scholar 

  • Tao-Cheng, J.H., Du, J., and McBain, C.J., SNAP-25 is polarized to axons and abundant along the axolemma: an immunogold study of intact neurons, J. Neurocytol., 2000, vol. 29, no. 1, pp. 67–77.

    Article  CAS  PubMed  Google Scholar 

  • Valverde, F., Santacana, M., and Heredia, M., Formation of an olfactory glomerulus: morphological aspects of development and organization, Neuroscience, 1992, vol. 49, pp. 255–275.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratory of Nervous System Development, Research Institute of Human Morphology, Russian Academy of Medical Sciences, ul. Tsyurupy 3, Moscow, 117418, Russia

    A. S. Kharlamova, V. M. Barabanov & S. V. Saveliev

Authors
  1. A. S. Kharlamova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. V. M. Barabanov
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. V. Saveliev
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. S. Kharlamova.

Additional information

Original Russian Text © A.S. Kharlamova, V.M. Barabanov, S.V. Saveliev, 2015, published in Ontogenez, 2015, Vol. 46, No. 3, pp. 174–185.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kharlamova, A.S., Barabanov, V.M. & Saveliev, S.V. Development of human olfactory bulbs in prenatal ontogenesis: An immunochistochemical study with markers of presynaptic terminals (anti-SNAP-25, synapsin-I, and synaptophysin). Russ J Dev Biol 46, 137–147 (2015). https://doi.org/10.1134/S1062360415030054

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1062360415030054

Keywords

Search

Navigation