Skip to main content
SpringerLink
Log in

Differential expression of syntaxin-1 and synaptophysin in the developing and adult human retina

  • Published:
Journal of Biosciences Aims and scope Submit manuscript

Abstract

Synaptophysin and syntaxin-1 are membrane proteins that associate with synaptic vesicles and presynaptic active zones at nerve endings, respectively. The former is known to be a good marker of synaptogenesis; this aspect, however, is not clear with syntaxin-1. In this study, the expression of both proteins was examined in the developing human retina and compared with their distribution in postnatal to adult retinas, by immunohistochemistry. In the inner plexiform layer, both were expressed simultaneously at 11–12 weeks of gestation, when synaptogenesis reportedly begins in the central retina. In the outer plexiform layer, however, the immunoreactivities were prominent by 16 weeks of gestation. Their expression in both plexiform layers followed a centre-to-periphery gradient. The immunoreactivities for both proteins were found in the immature photoreceptor, amacrine and ganglion cells; however, synaptophysin was differentially localized in bipolar cells and their axons, and syntaxin was present in some horizontal cells. In postnatal-to-adult retinas, synaptophysin immunoreactivity was prominent in photoreceptor terminals lying in the outer plexiform layer; on the contrary, syntaxin-1 was present in a thin immunoreactive band in this layer. In the inner plexiform layer, however, both were homogeneously distributed. Our study suggests that (i) syntaxin-1 appears in parallel with synapse formation; (ii) synaptogenesis in the human retina might follow a centre-to-periphery gradient; (iii) syntaxin-1 is likely to be absent from ribbon synapses of the outer plexiform layer, but may occur at presynaptic terminals of photoreceptor and horizontal cells, as is apparent from its localization in these cells, which is hitherto unreported for any vertebrate retina.

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

Abbreviations

DPX:

Dibutylpthala polystyrene xylene

IPL:

inner plexiform layer

PBS:

phosphate buffer saline

PD:

postnatal day

OPL:

outer plexiform layer

References

  • Barnstable C, Hofstein R and Akagawa K 1985 A marker of early amacrine cell development in rat retina;Dev. Brain Res. 20 286–290

    Article  CAS  Google Scholar 

  • Bennett M K, Calakos N and Scheller R 1992 Syntaxin: A synaptic protein implicated in docking of synaptic vesicles at presynaptic active zones;Science 257 255–259

    Article  PubMed  CAS  Google Scholar 

  • Blasi J, Chapman E R, Ramasari S, Binz T, Niemann H and Jahn R 1993 Botulinum neurotoxin C1 blocks neurotransmitter release by clearing HPC-1 syntaxin;EMBO. J. 12 4821–4828

    PubMed  CAS  Google Scholar 

  • Brandstätter J H, Lohrke S, Morgans C W and Wessle H 1996 Distributions of two homologous synaptic vesicle proteins, synaptoporin and synaptophysin, in the mammalian retina;J. Comp. Neurol. 370 1–10

    Article  PubMed  Google Scholar 

  • Catsicas S, Catsicas M, Keyser K T, Karten H J, Wilson M C and Milner R J 1992 Differential expression of the presynaptic protein SNAP-25 in mammalian retina;J. Neurosci. Res. 33 1–9

    Article  PubMed  CAS  Google Scholar 

  • Chun J J M and Shatz C J 1983 Immunohistochemical localization of synaptic vesicle antigens in developing cat cortex;Soc. Neurosci. Abstr. 9 692

    Google Scholar 

  • DeCamilli P and Jahn R 1990 Pathways to regulated exocytosis in neurons;Annu. Rev. Physiol. 52 625–645

    Article  CAS  Google Scholar 

  • DeCamilli P, Cameron R and Greengard P 1983 Localization of protein I by immunofluorescence in the adult and developing nervous system;J. Cell Biol. 96 1337–1354

    Article  CAS  Google Scholar 

  • Devoto S H and Barnstable C J 1987 SVP 38: A synaptic vesicle protein whose appearance correlates closely with synaptogenesis in the rat nervous system;Ann. N.Y. Acad. Sci. 493 493–496

    Article  CAS  Google Scholar 

  • Dhingra N K, Ramamoham Y and Raju T R 1997 Developmental expression of synaptophysin, synapsin I and syntaxin in the rat retina;Dev. Brain Res. 102 267–273

    Article  CAS  Google Scholar 

  • Dowling J E 1987The retina: An approchable part of the brain (Cambridge: Harvard University Press)

    Google Scholar 

  • Haas C A, Degennaro L J, Muller M and Holländer H 1990 Synapsin I expression in the rat retina during postnatal development;Exp. Brain Res. 82 25–32

    Article  PubMed  CAS  Google Scholar 

  • Hamilton W J, Boyd J D and Mossman J W W 1972Human embryology 4th edition (Cambridge: W Heffer)

    Google Scholar 

  • Hendrickson A 1992 A morphological comparison of foveal development in man and monkey;Eye 6 136–144

    PubMed  Google Scholar 

  • Hollenberg M J and Spira A W 1972 Early development of the human retina;Can. J. Ophthalmol. 7 472–491

    PubMed  CAS  Google Scholar 

  • Hollenberg M J and Spira A W 1973 Human retinal development: Ultrastructure of the outer retina;Am. J. Anat. 137 357–386

    Article  PubMed  CAS  Google Scholar 

  • Horsburgh G M and Sefton J 1987 Cellular degenisin and synaptogenesis in the developing retina of the rat;J. Comp. Neurol. 263 553–566

    Article  PubMed  CAS  Google Scholar 

  • Jahn R and Sudhof T C 1994 Synaptic vesicles and exocytosis;Annu. Rev. Neurosci. 17 219–246

    Article  PubMed  CAS  Google Scholar 

  • Jahn R, Schiebler W, Quimet C and Greengard P 1985 A 38000-dalton membrane protein (p 38) present in synaptic vesicles;Proc. Natl. Acad. Sci. USA 82 4137–4141

    Article  PubMed  Google Scholar 

  • Kapfhammer J P, Christ F and Schwab M E 1994 The expression of GAP-43 and synaptophysin in the developing rat retina;Dev. Brain Res. 80 251–260

    Article  CAS  Google Scholar 

  • Kivelä T, Tarkkanen A and Virtanen I 1989 Synatophysin in the human retina and retinoblastoma;Invest. Ophthalmol. Vis. Sci. 30 212–219

    PubMed  Google Scholar 

  • Knaus P, Betz H and Rehm H 1986 Expression of synaptophysin during postnatal development of the mouse brain;J. Neurochem. 47 1302–1304

    Article  PubMed  CAS  Google Scholar 

  • Koh S, Yamamoto A, Inoue Y, Akagawa K, Kawamura Y, Kawamoto K and Tashiro Y 1993 Immunoelectron microscopic localization of HPC-1 antigen in rat cerebellum;J. Neurocytol. 22 995–1002

    Article  PubMed  CAS  Google Scholar 

  • Koontz M A and Hendrickson A E 1993 Comparison of immunolocalization patterns for the synaptic vesicle proteins p65 and synapsin I in Macaque monkey retina;Synapse 14 268–282

    Article  PubMed  CAS  Google Scholar 

  • Kretzschmar S, Volknandt W and Zimmermann H 1996 Colocalization on the same synaptic vesicles of syntaxin and SNAP-25 with synaptic vesicle proteins: a re-evaluation of functional model required;Neurosci. Res. 26 141–148

    Article  PubMed  CAS  Google Scholar 

  • Leclerc N, Beasley P W, Brown I, Colonnier M, Gurd J W, Paladino T and Hawkes R 1989 Synaptophysin expression during synaptogenesis in the rat cerebellar cortex;J. Comp. Neurol. 280 197–212

    Article  PubMed  CAS  Google Scholar 

  • Linberg K A and Fisher S K 1988 Ultrastuctural evidence that horizontal cell axon terminals are presynaptic in the human retina;J. Comp. Neurol. 268 281–297

    Article  PubMed  CAS  Google Scholar 

  • Linberg K A and Fisher S K 1990 A burst of differentiation in the outer posterior retina of the eleven-week human fetus: An ultrastructural study;Vis. Neurosci. 5 43–60

    PubMed  CAS  Google Scholar 

  • Mandell J W, Townes-Anderson E, Czernik A J, Cameron R, Greengard P and DeCamilli P 1990 Synapsins in the vertebrate retina: absence from ribbon synapses and heterogeneous distribution among conventional synapses;Neuron 5 19–33

    Article  PubMed  CAS  Google Scholar 

  • Mann I 1964The development of the human eye 3rd edition (New York: Grune and Stratton)

    Google Scholar 

  • Maslim J and Stone J 1986 Synaptogenesis in the retina of the cat;Brain Res. 373 35–48

    Article  PubMed  CAS  Google Scholar 

  • Maslin J and Stone J 1988 Time course of the stratification of the dendritic fields of ganglion cells in the retina of the cat;Dev. Brain Res. 44 87–93

    Article  Google Scholar 

  • Missotten L 1965The ultrastucture of the human retina (Brussels: Arscia)

    Google Scholar 

  • Morgans C W 2000 Presynaptic proteins of ribbon synapses in the retina;Microsc. Res. Tech. 50 141–150

    Article  PubMed  CAS  Google Scholar 

  • Morgans C W, Brandstätter J H, Kellerman J, Betz H and Wässle H 1996 A SNARE complex containing syntaxin 3 is present in ribbon synapses of the retina;J. Neurosci. 16 6713–6721

    PubMed  CAS  Google Scholar 

  • Nag T C and Wadhwa S 1996 Calbindin and parvalbumin immunoreactivity in the developing and adult human retina;Dev. Brain Res. 93 23–32

    Article  CAS  Google Scholar 

  • Nag T C and Wadhwa S 1999 Developmental expression of calretinin immunoreactivity in the human retina and a comparison with two other EF-hand calcium binding proteins;Neuroscience 91 41–55

    Article  PubMed  CAS  Google Scholar 

  • Narayanan K and Wadhwa S 1998 Photoreceptor morphogenesis in the human retina: A scanning electron microscopic study;Anat. Rec. 252 133–139

    Article  PubMed  CAS  Google Scholar 

  • Navone F, Jahn R, Di Gioin G, Stukenbrok H, Greengard P and DeCamilli P 1986 Protein 38: An integral membrane protein specific for small vesicles of neurons and neuroendocrine cells;J. CellBiol. 103 2511–2527

    Article  CAS  Google Scholar 

  • Nishimura Y and Rakic P 1985 Development of the rhesus monkey retina. I. Emergence of the inner plexiform layers and its synapses;J.Comp. Neurol. 241 420–434

    Article  PubMed  CAS  Google Scholar 

  • Nishimura Y and Rakic P 1987 Synaptogenesis in the primate retina proceeds from the ganglion cells towards the photoreceptors;Neurosci. Res. (Suppl.) 6 253–268

    Article  Google Scholar 

  • Okada M, Erickson A and Hendrickson A 1992 Synaptogenesis in primate retina;Invest. Ophthalmol. Vis. Sci. (Suppl.) 33 941

    Google Scholar 

  • Okada M, Erickson A and Hendrickson A 1994 Light and electron microscopic analysis of synaptic development in Macaca monkey retina as detected by immunocytochemical labeling for the synaptic vesicle protein SV2;J. Comp. Neurol. 339 535–558

    Article  PubMed  CAS  Google Scholar 

  • O'Rahilly R 1975 The prenatal development of the human eye;Exp.EyeRes. 21 93–112

    Article  Google Scholar 

  • Ovtscharoff W, Bergmann M, Marqueze-Pouey B, Knaus P, Betz H, Grabs D, Reisert I and Gratzl M 1993 Ontogeny of synaptophysin and synaptoporin in the central nervous system: differential expression in striatal neurons and their afferents during development;Dev. Brain Res. 72 219–225

    Article  CAS  Google Scholar 

  • Phelan P and Gordon-Weeks P R 1992 Widespread distribution of synaptophysin, a synaptic vesicle glycoprotein, in growing neurites and growth cones;Eur. J. Neurosci. 4 1180–1190

    Article  PubMed  Google Scholar 

  • Provis J M, Van Driel D, Billson F A and Russell P 1985 Development of the human retina: Pattern of cell distribution and redistribution in the ganglion cell layer;J. Comp. Neurol. 233 429–451

    Article  PubMed  CAS  Google Scholar 

  • Rapaport D H and Stone J 1982 The site of commencement of maturation in mammalian retina; Observations in the cat;Dev. Brain Res. 5 273–279

    Article  Google Scholar 

  • Rhodes R H 1979 A light microscopic study of the developing human neural retina;Am. J. Anat. 154 195–210

    Article  PubMed  CAS  Google Scholar 

  • Sarthy P V and Bacon W 1985 Developmental expression of a synaptic-vesicle specific protein in the rat retina;Dev. Biol. 112 284–291

    Article  PubMed  CAS  Google Scholar 

  • Sesack S R and Snyder C L 1995 Cellular and subcellular localization of syntaxin-like immunoreactivity in the rat striatum and cortex;Neuroscience 67 993–1007

    Article  PubMed  CAS  Google Scholar 

  • Seiler M and Aramant R B 1994 Photoreceptor and glial markers in human embryonic retina and in human embryonic retinal transplants to rat retina;Dev. Brain Res. 80 81–95

    Article  CAS  Google Scholar 

  • Sheedlo H J, Li L, Barnstable C J and Turner J E 1995 Synpatic and photoreceptor components in retinal pigment epithelial cell transplanted retinas of Royal college of surgeons dystrophic rats;J. Neurosci. Res. 36 423–431

    Article  Google Scholar 

  • Sollner T, Whiteheart S W, Brunner M, Erdjument-Bromage H, Geromanoz S, Tempst P and Rothman J E 1993 SNAP receptors implicated in vesicle targeting and fusion;Nature (London) 362 318–324

    Article  CAS  Google Scholar 

  • Spira A W and Hollenberg M J 1973 Human retinal development: Ultrastructure of the inner retinal layers;Dev. Biol. 1 1–21

    Article  Google Scholar 

  • Ullrich B and Sudhof T C 1994 Distribution of synaptic markers in the retina: Implications for synaptic vesicle traffic in ribbon synapses;J. Physiol. (Paris) 88 249–257

    Article  CAS  Google Scholar 

  • Van Driel D, Provis J M and Billson F A 1990 Early differentiation of ganglion, amacrine, bipolar and Muller cells in the developing fovea of human retina;J. Comp. Neurol. 291 203–219

    Article  PubMed  Google Scholar 

  • Voigt. T, Delima A D and Beckmann M 1993 Synaptophysin immunohistochemistry reveals inside-out pattern of early synaptogenesis in ferret cerebral cortex;J. Comp. Neurol. 330 48–64

    Article  PubMed  CAS  Google Scholar 

  • Wiedenmann B and Franke W W 1985 Identification and localization of synaptophysin, an integral membrane glycoprotein of Mr 38,000 characteristic of presynaptic vesicles;Cell 41 1017–1028

    Article  PubMed  CAS  Google Scholar 

  • Weidmann T A and Kuwabara T 1968 Postnatal development of the rat retina. An electron microscope study;Arch. Ophthalmol. 79 470–484

    Google Scholar 

  • Weidmann T A and Kuwabara T 1969 Development of the rat retina;Invest. Ophthalmol. 8 60–69

    Google Scholar 

  • Yoshida A, Oho C, Omori A, Kuwahara R, Ito T and Takahashi M 1992 HPC-1 is associated with synaptotagmin and W-Conotoxin receptor;J. Biol. Chem. 267 24925–24928

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anatomy, All India Institute of Medical Sciences, Ansari Nagar, 110 029, New Delhi, India

    T. C. Nag & Shashi Wadhwa

Authors
  1. T. C. Nag
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shashi Wadhwa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shashi Wadhwa.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nag, T.C., Wadhwa, S. Differential expression of syntaxin-1 and synaptophysin in the developing and adult human retina. J Biosci 26, 179–191 (2001). https://doi.org/10.1007/BF02703642

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02703642

Key words

Search

Navigation