Skip to main content
Log in

Synapsin-like immunoreactivity is present in hair cells and efferent terminals of the toadfish crista ampullaris

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

The synapsins are presynaptic membrane-associated proteins involved in neurotransmitter release. They are differentially expressed in tissues and cells of the central and peripheral nervous system. In vestibular end organs of mammals, synapsin I-like immunoreactivity has been reported in efferent and afferent terminals and in afferent nerve calyces surrounding type I hair cells. In addition, synapsin I has recently been described in several non-neural cell lines. The present study was conducted to locate synapsin-like immunoreactivity in the neuronal and non-neuronal cells of the fish crista ampullaris, to examine the possibility that the non-neuronal sensory receptor cells express synapsins in vivo. Synapsin-like immunostaining was visualized by immunofluorescence detection in wholemounts of the toadfish crista ampullaris using multiphoton laser scanning microscopy and by electron microscopic visualization of post-embedding immunogold labeling. The results demonstrate that synapsin-like immunoreactivity is present in vestibular hair cells and efferent boutons of the toadfish crista ampullaris. Afferent endings are not labeled. Staining in hair cells is not associated with the synaptic ribbons, suggesting that there is an additional, non-synaptic role for the synapsins in some non-neuronal cells of vertebrates. Moreover, while the cristae of amniote and anamniote species share many functional attributes, differences in their synaptic vesicle-associated protein profiles appear to reflect their disparate hair cell populations.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2A–F
Fig. 3
Fig. 4A–C

Similar content being viewed by others

References

  • Bhangu PS, Genever PG, Spencer GJ, Grewal TS, Skerry TM (2001) Evidence for targeted vesicular glutamate exocytosis in osteoblasts. Bone 29:16–23

    CAS  PubMed  Google Scholar 

  • Bustos R, Kolen ER, Braiterman L, Baines AJ, Gorelick FS, Hubbard AL (2001) Synapsin I is expressed in epithelial cells: localization to a unique trans-Golgi compartment. J. Cell Sci. 114:3695–3704

    Google Scholar 

  • Ceccaldi PE, Benfenati F, Chieregatti E, Greengard P, Valtorta F (1993) Rapid binding of synapsin I to F- and G-actin. A study using fluorescence resonance energy transfer. FEBS Lett 329:301–305

    CAS  PubMed  Google Scholar 

  • De Camilli P, Camergon R, Greengard P (1983) 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 96:1355–1373

    PubMed  Google Scholar 

  • Dechesne CJ, Kauff C, Stettler O, Tavitian B (1997) Rab3A immunolocalization in the mammalian vestibular end-organs during development and comparison with synaptophysin expression. Dev Brain Res 99:103–111

    CAS  Google Scholar 

  • Farrell KP, Keates RA (1990) Synapsin-1 is found in a microtubule-associated complex of proteins isolated from bovine brain. Biochem Cell Biol 68:1256–1261

    CAS  PubMed  Google Scholar 

  • Favre D, Scarfone E, DiGioia G, DeCamilli P, Dememes D (1986) Presence of synapsin I in afferent and efferent nerve endings of the vestibular sensory epithelia. Brain Res 384:379–382

    CAS  PubMed  Google Scholar 

  • Fried G, Nestler EJ, De Camilli P, Stjarne L, Olson L, Lundberg JM, Hökfelt T, Ouimet CC, Greengard P (1982) Cellular and subcellular localization of protein I in the peripheral nervous system. Proc Natl Acad Sci USA 79:2717–2721

    CAS  PubMed  Google Scholar 

  • Holstein GR, Martinelli GP, Boyle R, Rabbitt RD, Highstein SM (2004a) Ultrastructural observations of efferent terminals in the crista ampullaris of the toadfish, Opsanus tau. Exp Brain Res 155:265–273

    CAS  PubMed  Google Scholar 

  • Holstein GR, Martinelli GP, Henderson SC, Friedrich VLJ, Rabbitt RD, Highstein SM (2004b) Gamma-aminobutyric acid is present in a spatially discrete subpopulation of hair cells in the crista ampullaris of the toadfish, Opsanus tau. J Comp Neurol 471:1–10

    CAS  PubMed  Google Scholar 

  • Hosaka M, Hammer RE, Südhof TC (1999) A phospho-switch controls the dynamic association of synapsins with synaptic vesicles. Neuron 24:377–387

    CAS  PubMed  Google Scholar 

  • Hosaka M, Südhof TC (1998) Synapsins I and II are ATP-binding proteins with differential Ca2+ regulation. J Biol Chem 273:1425–1429

    CAS  PubMed  Google Scholar 

  • Hurley SL, Brown DL, Cheetham JJ (2004) Cytoskeletal interactions of synapsin I in non-neuronal cells. Biochem Biophys Res Commun 317:16–23

    CAS  PubMed  Google Scholar 

  • Huttner WB, Schiebler W, Greengard P, De Camilli P (1983) Synapsin I (protein I), a nerve terminal-specific phosphoprotein. III. Its association with synaptic vesicles studies in a highly purified synaptic vesicle preparation. J Cell Biol 96:1374–1388

    CAS  PubMed  Google Scholar 

  • Kao H-T, Porton B, Czernik AJ, Feng J, Yiu G, Haring M, Benfenati F, Greengard P (1998) A third member of the synapsin gene family. Proc Natl Acad Sci USA 95:4667–4672

    CAS  PubMed  Google Scholar 

  • Matovcik LM, Karapetian O, Czernik AJ, Marino CR, Kinder BK, Gorelick FS (1994) Antibodies to an epitope on synapsin I detect a protein associated with the endocytic compartment in non-neuronal cells. Eur J Cell Biol 65:327–340

    CAS  PubMed  Google Scholar 

  • Petralia RS, Wenthold RJ (1999) Immunocytochemistry of NMDA receptors. Methods Mol Biol 128:73–92

    CAS  PubMed  Google Scholar 

  • Pieribone VA, Porton B, Rendon B, Feng J, Greengard P, Kao H-T (2002) Expression of synapsin III in nerve terminals and neurogenic regions of the adult brain. J Comp Neurol 454:105–114

    CAS  PubMed  Google Scholar 

  • Pieribone VA, Shupliakov O, Brodin L, Hilfiker-Rothenfluh S, Czernik AJ, Greengard P (1995) Distinct pools of synaptic vesicles in neurotransmitter release. Nature 375:493–497

    CAS  PubMed  Google Scholar 

  • Rosahl TW, Spillane D, Missler M, Herz J, Selig DK, Wolff JR, Hammer RE, Malenka RC, Südhof TC (1995) Essential functions of synapsins I and II in synaptic vesicle regulation. Nature 375:488–493

    CAS  PubMed  Google Scholar 

  • Safieddine S, Wenthold RJ (1997) The glutamate receptor subunit delta-1 is highly expressed in hair cells of the auditory and vestibular systems. J Neurosci 17:7523–7531

    CAS  PubMed  Google Scholar 

  • Safieddine S, Wenthold RJ (1999) SNARE complex at the ribbon synapses of cochlear hair cells: analysis of synaptic vesicle- and synaptic membrane-associated proteins. Eur J Neurosci 11:803–812

    CAS  PubMed  Google Scholar 

  • Scarfone E, Dememes D, Jahn R, DeCamilli P, Sans A (1988) Secretory function of the vestibular nerve calyx suggested by present of vesicles, synapsin I, and synaptophysin. J Neurosci 8:4640–4645

    CAS  PubMed  Google Scholar 

  • Scarfone E, Dememes D, Sans A (1991) Synapsin I and synaptophysin expression during ontogenesis of the mouse peripheral vestibular system. J Neurosci 11:1173–1181

    CAS  PubMed  Google Scholar 

  • Südhof TC, Czernik AJ, Kao HT, Takei K, Johnston PA, Horiuchi A, Kanazir SD, Wagner MA, Perin MS, DeCamilli P, Greengard P (1989) Synapsins: mosaics of shared and individual domains in a family of synaptic vesicles. Phosphoprotein Sci 245:1474–1480

    Google Scholar 

Download references

Acknowledgements

The authors are grateful to Dr Scott Henderson, for assistance with multiphoton microscopy, and to Dr Ewa Kukielka and Rosemary Lang for technical assistance. Research was supported by NIDCD grant DC01837. Multi-photon laser scanning microscopy was performed at the Mount Sinai School of Medicine Microscopy Shared Resource Facility, supported in part with a Howard Hughes Medical Institute–Biomedical Research Support Program award to Mount Sinai School of Medicine and an NIH-NCI shared resources grant 1 R24 CA095823-01.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to G. R. Holstein.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Holstein, G.R., Martinelli, G.P., Nicolae, R.A. et al. Synapsin-like immunoreactivity is present in hair cells and efferent terminals of the toadfish crista ampullaris. Exp Brain Res 162, 287–292 (2005). https://doi.org/10.1007/s00221-004-2194-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-004-2194-5

Keywords

Navigation