Skip to main content
SpringerLink
Log in

Apoptosis and differentiation in presumptive neural retina and presumptive retinal pigmented epithelium during early eye development in toad, Bufo raddei strauch

  • Mechanisms of Cell Proliferation and Differentiation
  • Published:
Russian Journal of Developmental Biology Aims and scope Submit manuscript

Abstract

Apoptosis and differentiation in presumptive neural retina (PNR) and presumptive retinal pigmented epithelium (PRPE) were investigated during early retina development of toad, Bufo raddei Strauch. TUNEL staining was used to evaluate apoptotic cells and the immunohistochemistry was used to assess the expression levels of glial fibrillary acidic protein (GFAP), RT97 and tyrosinase (Tyr) during early eye development respectively. The density of apoptotic cells and protein expression were quantitated with Image-Pro Plus 6.0. Apoptosis was found in both PNR and PRPE and the density of apoptotic profiles in PRPE was higher than that in PNR (most P < 0.01) at the same stage during early eye development. The expression levels of GFAP and RT97 changed from low to high in PNR, but from high to low in PRPE, whereas the expression level of Tyr, was contrary to those of GFAP and RT97 in both PNR and PRPE. The point of intersection of these, increase and decrease respectively was found at 5–6 h after formation of optic vesicle (FOV). PRPE becomes thinner than PNR, one of the reasons might be due to higher density of apoptosis in PRPE than that in PNR during early eye development. Molecular differentiation, however, occurred after the contact of the optic vesicle outer wall with the overlying ectoderm which promotes the expression of specific molecules and inhibits the expression of non-specific molecules in PNR and PRPE respectively.

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

  • Adler, R. and Canto-Soler, M.V., Molecular Mechanisms of Optic Vesicle Development: Complexities, Ambiguities and Controversies, Dev. Biol., 2007, vol. 305, pp. 1–13.

    Article  PubMed  CAS  Google Scholar 

  • Basu, P.K., Sarkar, P., Menon, I., et al., Bovine Retinal Pigment Epithelial Cells Cultured in vitro: Growth Characteristics, Morphology, Chromosomes, Phagocytosis Ability, Tyrosinase Activity and Effect of Freezing, Exp. Eye Res., 1983, vol. 36, pp. 671–683.

    Article  PubMed  CAS  Google Scholar 

  • Bharti, K., Nguyen, M.T.T., Skuntz, S., et al., The Other Pigment Cell: Specification and Development of the Pigmented Epithelium of the Vertebrate Eye, Pigm. Cell Res., 2006, vol. 19, pp. 380–394.

    Article  Google Scholar 

  • Bignami, A., Eng, L.F., Dahl, D., et al., Localization of the Glial Fibrillary Acidic Protein in Astrocytes by Immunofluorescence, Brain Res., 1972, vol. 43, pp. 429–435.

    Article  PubMed  CAS  Google Scholar 

  • Barnstable C.J., A Molecular View of Vertebrate Retinal Development, Mol. Neurobiol., 1987, vol. 11, pp. 9–46.

    Article  Google Scholar 

  • Canto-Soler, M.V. and Adler, R., Optic Cup and Lens Development Requires Pax6 Expression in the Early Optic Vesicle during a Narrow Time Window, Dev. Biol., 2006, vol. 294, pp. 119–132.

    Article  PubMed  CAS  Google Scholar 

  • Coughlin, M.D., Boyer, D.M. and Black, I.B., Embryologic Development of a Mouse Sympathetic Ganglion in vivo and in vitro, Proc. Natl. Acad. Sci. USA, 1977, vol. 74, pp. 3438–3442.

    Article  PubMed  CAS  Google Scholar 

  • Cronin, C.A., Ryan, A.B., Talley, E.M., et al., Tyrosinase Expression during Neuroblast Divisions Affects Later Pathfinding by Retinal Ganglion Cells, J. Neurosc., 2003, vol. 23, pp. 11692–11697.

    CAS  Google Scholar 

  • Cuadros, M.A., García-Martín, M., Martin, C., et al., Haemopoietic Phagocytes in the Early Differentiating Avian Retina, J. Anat., 1991, vol. 177, pp. 145–158.

    PubMed  CAS  Google Scholar 

  • Dowling, J.E., The Retina, Cambridge, MA: Belknap Press, 1987.

    Google Scholar 

  • Eng, L.F., The Glial Fibrillary Acidic Protein: The Major Protein Constituent of Glial Filaments, Scand. J. Immunol., 1982, vol. 15, pp. 41–51.

    Article  Google Scholar 

  • Ezeonu, I., Smith, S. and Dutt, K., Differentiation in a Human Retinal Precursor Cell Line: Limitation to Multipotency, In vitro Cell Dev. Biol.-An., 1999, vol. 35, pp. 435–440.

    Article  CAS  Google Scholar 

  • Feng, B.S., Ge, R.C., and Tong, Y.X., Studies on Morphogenesis of Bufo raddei Eye, Acta Herpetol. Sin., 1984, vol. 3, pp. 5–10.

    Google Scholar 

  • Francisco-Morcillo, J., Hidalgo-Sánchez, M., and Martín-Partido, G., Spatial and Temporal Patterns of Apoptosis during Differentiation of the Retina in the Turtle, Anat. Embryol., 2004, vol. 208, pp. 289–299.

    Article  PubMed  CAS  Google Scholar 

  • Francisco-Morcillo, J., Hidalgo-Sánchez, M., and Martín-Partido, G., Spatial and Temporal Patterns of Proliferation and Differentiation in the Developing Turtle Eye, Brain Res., 2006, vol. 1103, pp. 32–48.

    Article  PubMed  CAS  Google Scholar 

  • Ge, R.C., Feng, B.S., and Tong, Y.X., The Early Embryonic Development and Stages of the Toad, Bufo raddei Strauch, J. Lanzhou Univ. (Nature Sci. Ed.), 1982, vol. 18, pp. 125–136.

    Google Scholar 

  • Gilbert, S.F., Developmental Biology, Sunderland, MA: Sinauer, 2003.

    Google Scholar 

  • Harris W.A. and Perron M., Molecular Recapitulation: The Growth of the Vertebrate Retina, Int. J. Dev. Biol., 1998, vol. 42, pp. 299–304.

    PubMed  CAS  Google Scholar 

  • Holt, C.E., A Single-Cell Analysis of Early Retinal Ganglion Cell Differentiation in Xenopus: From Soma to Axon Tip, J. Neurosci., 1989, vol. 9, pp. 3123–3145.

    PubMed  CAS  Google Scholar 

  • Hyer, J., Mima, T., and Mikawa, T., FGF1 Patterns the Optic Vesicle by Directing the Placement of the Neural Retina Domain, Development, 1998, vol. 125, pp. 869–877.

    PubMed  CAS  Google Scholar 

  • Jacobson, A.G., Inductive Processes in Embryonic Development, Science, 1966, vol. 152, pp. 25–34.

    Article  PubMed  CAS  Google Scholar 

  • Julien, S., Kociok, N., Kreppel, F., et al., Tyrosinase Biosynthesis and Trafficking in Adult Human Retinal Pigment Epithelial Cells, Graef. Arch. Clin. Exp., 2007, vol. 245, pp. 1495–1505.

    Article  CAS  Google Scholar 

  • Kumasaka, M., Sato, S., Yajima, I., et al., Isolation and Developmental Expression of Tyrosinase Family Genes in Xenopus laevis, Pigm. Cell Res., 2003, vol. 16, pp. 455–462.

    Article  CAS  Google Scholar 

  • Lee, C.S., May, N.R., and Fan, C.M., Transdifferentiation of the Ventral Retinal Pigmented Epithelium to Neural Retina in the growth arrest specific gene 1 Mutant, Dev. Biol., 2001, vol. 236, pp. 17–29.

    Article  PubMed  CAS  Google Scholar 

  • Li, M. and Sakaguchi, D.S., Expression Patterns of Focal Adhesion Associated Proteins in the Developing Retina, Dev. Dynam., 2002, vol. 225, pp. 544–553.

    Article  CAS  Google Scholar 

  • Li, Z., Hu, M., Ochocinska, M.J., et al., Modulation of Cell Proliferation in the Embryonic Retina of Zebrafish (Danio rerio), Dev. Dynam., 2000, vol. 219, pp. 391–401.

    Article  CAS  Google Scholar 

  • Lopashov, G.V., Developmental Mechanisms of Vertebrate Eye Rudiment, Oxford, 1963.

  • Lopashov, G.V. and Stroeva, O.G., Morphogenesis of the Vertebrate Eye, Adv. Morphol., 1961, vol. 1, pp. 331–370.

    Google Scholar 

  • Lopashov, G.V. and Stroeva, O.G., Development of the Eye: Experimental Studies, Jerusalem, 1964.

  • Martín-Partido, G., Rodríguez-Gallardo, L., álvarez, I.S., et al., Cell Death in the Ventral Region of the Neural Retina during the Early Development of the Chick Embryo Eye, Anat. Rec., 1988, vol. 222, pp. 272–281.

    Article  PubMed  Google Scholar 

  • Messenger, N.J. and Warner, A.E., The Appearance of Neural and Glial Cell Markers during Early Development of the Nervous System in the Amphibian Embryo, Development, 1989, vol. 107, pp. 43–54.

    PubMed  CAS  Google Scholar 

  • Newton, J.M., Cohen-Barak, O., Hagiwara, N., et al., Mutations in the Human Orthologue of the Mouse underwhite Gene (uw) Underlie a New Form of Oculocutaneous Albinism, OCA4, Am. J. Hum. Genet., 2001, vol. 69, pp. 981–988.

    Article  PubMed  CAS  Google Scholar 

  • Norkute, A., Kipp, M., Dang, J., et al., Early Formation of a GFAP-Positive Cell Population in the Ventricular Zone during Chicken Brain Development, Cells Tissues Organs, 2010, vol. 191, pp. 57–65.

    Article  PubMed  Google Scholar 

  • Rodríguez-Gallardo, L., Lineros-Domínguez, M.D.C., Francisco-Morcillo, J., et al., Macrophages during Retina and Optic Nerve Development in the Mouse Embryo: Relationship to Cell Death and Optic Fibres, Anat. Embryol., 2005, vol. 210, pp. 303–316.

    Article  PubMed  Google Scholar 

  • Schnitzer, J., Distribution and Immunoreactivity of Glia in the Retina of the Rabbit, J. Comp. Neurol., 1985, vol. 240, pp. 128–142.

    Article  PubMed  CAS  Google Scholar 

  • Sharma, S., Sharma, M.C., Gupta, D.K., et al., Angiogenic Patterns and Their Quantitation in High Grade Astrocytic Tumors, J. Neuro-Oncol., 2006, vol. 79, pp. 19–30.

    Article  Google Scholar 

  • Shin, D.H., Lee, K.S., Lee, E., et al., The Correspondence between the Labeling Patterns of Antibody RT97, Neurofilaments, Microtubule Associated Protein 1B and tau Varies with Cell Types and Development Stages of Chicken Retina, Neurosci. Lett., 2003, vol. 342, pp. 167–170.

    Article  PubMed  CAS  Google Scholar 

  • Turner, D.L. and Cepko, C.L., A Common Progenitor for Neurons and Glia Persists in Rat Retina Late in Development, Nature, 1987, vol. 328, pp. 131–136.

    Article  PubMed  CAS  Google Scholar 

  • Velasco, A., Bragado, M.J., Jimeno, D., et al., Growing and Regenerating Axons in the Visual System of Teleosts Are Recognized with the Antibody RT97, Brain Res., 2000, vol. 883, pp. 98–106.

    Article  PubMed  CAS  Google Scholar 

  • Wang, F.C., Liu, Z.H., Si, K.Y., et al., Immunohistochemical Localization of the Medium and High-Weight Neurofilament in the Visual Nervous System of Carassius auratus, J. Northwest Norm. Univ. (Nat. Sci.), 2006, vol. 42, pp. 74–77.

    CAS  Google Scholar 

  • Xavier, L.L., Viola, G.G., Ferraz, A.C., et al., A Simple and Fast Densitometric Method for the Analysis of Tyrosine Hydroxylase Immunoreactivity in the Substantia Nigra Pars Compacta and in the Ventral Tegmental Area, Brain Res., 2005, vol. 16, pp. 58–64.

    CAS  Google Scholar 

  • Zhang, S.S., Fu X.Y., and Barnstable, C.J., Molecular Aspects of Vertebrate Retinal Development, Mol. Neurobiol., 2002, vol. 26, nos. 2–3, pp. 137–152.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Developmental Biology, School of Life Sciences, Lanzhou University, Lanzhou, 730000, P.R. China

    W. Han, Y. -P. Han & Z. -R. Wang

  2. Collage of Life Scienes and Techenology, Longdong University, Qingyang, 745000, P.R. China

    Y. -P. Han

Authors
  1. W. Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Y. -P. Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Z. -R. Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Z. -R. Wang.

Additional information

Published in Russian in Ontogenez, 2012, Vol. 43, No. 6, pp. 436–446.

The article is published in the original.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Han, W., Han, Y.P. & Wang, Z.R. Apoptosis and differentiation in presumptive neural retina and presumptive retinal pigmented epithelium during early eye development in toad, Bufo raddei strauch. Russ J Dev Biol 43, 362–371 (2012). https://doi.org/10.1134/S1062360412060033

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1062360412060033

Keywords

Search

Navigation