Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Light- and focus-dependent expression of the transcription factor ZENK in the chick retina

Nature Neuroscience volume 2, pages 706–712 (1999)Cite this article

Abstract

Ocular growth and refraction are regulated by visual processing in the retina. We identified candidate regulatory neurons by immunocytochemistry for immediate-early gene products, ZENK (zif268, Egr-1) and Fos, after appropriate visual stimulation. ZENK synthesis was enhanced by conditions that suppress ocular elongation (plus defocus, termination of form deprivation) and suppressed by conditions that enhance ocular elongation (minus defocus, form deprivation), particularly in glucagon-containing amacrine cells. Fos synthesis was enhanced by termination of visual deprivation, but not by defocus and not in glucagon-containing amacrine cells. We conclude that glucagon-containing amacrine cells respond differentially to the sign of defocus and may mediate lens-induced changes in ocular growth and refraction.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: ZENK expression in the chick retina through the light–dark cycle.
Figure 2: Effects of restored vision and form-deprivation lens-induced defocus on ZENK expression in the chick retina.
Figure 3: Effects of NMDA and MK-801 on ZENK expression in the chick retina.
Figure 4: Expression of ZENK, glucagon and PKCα in vertical sections of chick retina.
Figure 5: Quantification of vision-dependent expression of ZENK in the chick retina.
Figure 6: Vision-dependent expression of Fos.

Similar content being viewed by others

References

  1. Wallman, J. Retinal control of eye growth and refraction. Prog. Retinal Res. 12, 133–153 ( 1993).

    Article  Google Scholar 

  2. Fischer, A. J., Seltner, R. L. & Stell, W. K. NMDA-induced excitotoxicity causes myopia in post-hatch chicks. Can. J. Ophthalmol. 32, 373– 377 (1997).

    CAS  PubMed  Google Scholar 

  3. Fischer, A. J., Miethke, P., Morgan, I. G. & Stell, W. K. Cholinergic amacrine cells are not required for the progression and atropine-mediated suppression of form-deprivation myopia. Brain Res. 794, 48–60 (1998).

    Article  CAS  Google Scholar 

  4. Fischer, A. J., Seltner, R. L., Poon, J. & Stell, W. K. Immunocytochemical characterization of NMDA and QA-induced excitotoxicity in the retina of chicks. J. Comp. Neurol. 393, 1– 15 (1998).

    Article  CAS  Google Scholar 

  5. Fischer, A. J., Seltner, R. P. L. & Stell, W. K. Opiate and N-methyl-D-aspartate receptors in form-deprivation myopia. Vis. Neurosci. 15, 685– 693 (1998).

    Google Scholar 

  6. Fischer, A. J., Morgan, I. G. & Stell, W. K. Colchicine induces excessive ocular growth and myopia in chicks. Vision Res. 39, 685– 697 (1999).

    Article  CAS  Google Scholar 

  7. Wildsoet, C. & Pettigrew, J. D. Kainic acid-induced eye enlargement in chickens: Differential effect on anterior and posterior segments. Invest. Ophthal. Vis. Sci. 29, 311– 319 (1988).

    CAS  PubMed  Google Scholar 

  8. Curtin, B. J. The Myopias: Basic Science and Clinical Management (Harper & Row, Philadelphia, 1985).

    Google Scholar 

  9. Wallman, J. Nature and nurture of myopia. Nature 371, 201–202 (1994).

    Article  CAS  Google Scholar 

  10. Beckman, A. M. & Wilce, P. A. Egr transcription factors in the nervous system. Neurochem. Int. 31, 477–510 (1997).

    Article  Google Scholar 

  11. Chaudhuri, A. Neural activity mapping with inducible transcription factors. Neuroreport 8, iii–vii ( 1997).

    Article  CAS  Google Scholar 

  12. Long, K. D. & Salbaum, J. M. Evolutionary conservation of the immediate-early gene ZENK. Mol. Biol. Evol. 15, 284–292 (1998).

    Article  CAS  Google Scholar 

  13. Sukhatme, V. P. et al. A zinc finger-encoding gene coregulated with c-fos during growth and differentiation, and after cellular depolarization. Cell 53, 37–43 ( 1988).

    Article  CAS  Google Scholar 

  14. Lemaire, P., Revelant, O., Bravo, R. & Charnay, P. Two genes encoding potential transcription factors with identical DNA-binding domains are activated by growth factors in cultured cells. Proc. Natl. Acad. Sci. USA 85, 4691–4695 ( 1988).

    Article  CAS  Google Scholar 

  15. Milbrant, J. A nerve growth factor-induced gene encodes a possible transcriptional regulatory factor. Science 238, 797– 799 (1987).

    Article  Google Scholar 

  16. Dragunow, M. & Faull, R. The use of c-fos as a metabolic marker in neuronal pathway tracing. J. Neurosci. Methods 29 , 261–265 (1989).

    Article  CAS  Google Scholar 

  17. Gudehithlu, K. P., Neff, N. H. & Hadjiconstantinou, M. c-fos and NGFI-A mRNA of rat retina: evidence for light-induced augmentation and a role for cholinergic and glutamate receptors. Brain Res. 631, 77–82 ( 1993).

    Article  CAS  Google Scholar 

  18. Araki, C. M. & Hamassaki-Britto, D. E. Motion-sensitive neurons in the retina: a study using Fos immunohistochemistry. Brain Res. 794, 333–337 ( 1998).

    Article  CAS  Google Scholar 

  19. Masana, M. I., Benloucif, S. & Dubocovich, M. L. Light-induced c-fos mRNA expression in the suprachiasmatic nucleus and the retina of C3H/HeN mice. Mol. Brain Res. 42,193–201 (1996).

    Article  CAS  Google Scholar 

  20. Rohrer, B., Iuvone, P. M. & Stell, W. K. Stimulation of dopaminergic amacrine cells by stroboscopic illumination or fibroblast growth factor (bFGF, FGF-2) injections: possible roles in prevention of form-deprivation myopia in the chick. Brain Res. 686, 169–181 ( 1995).

    Article  CAS  Google Scholar 

  21. Sagar, S. M. & Sharp, F. R. Light induces a Fos-like nuclear antigen in retinal neurons. Mol. Brain Res. 7, 17–21 (1990).

    Article  CAS  Google Scholar 

  22. Yaqub, A., Guimaraes, M. & Eldred, W. D. Neurotransmitter modulation of Fos- and Jun-like proteins in the turtle retina. J. Comp. Neurol. 354 , 481–500 (1995).

    Article  CAS  Google Scholar 

  23. Yoshida, K., Kawamura, K. & Imaki, J. Differential expression of c-fos mRNA in rat retinal cells: Regulation by light/dark cycle. Neuron 10, 1049–1054 (1993).

    Article  CAS  Google Scholar 

  24. Koistinaho, J. & Sagar, S. M. Localization of protein kinase C subspecies in the rabbit retina. Neurosci. Lett. 177, 15–18 ( 1994).

    Article  CAS  Google Scholar 

  25. Kolb, H., Zhang, L. & DeKorver, L. Differential staining of neurons in the human retina with antibodies to protein kinase C isozymes. Vis. Neurosci. 10, 341–351 (1993).

    Article  CAS  Google Scholar 

  26. Ueda, Y., Iwakabe, H., Masu, M., Suzuki, M. & Nakanishi, S. The mGluR6 5´-upstream transgene sequence directs a cell-specific and developmentally regulated expression in retinal rod and ON-type cone bipolar cells. J. Neurosci. 17, 3014–3023 (1997).

    Article  CAS  Google Scholar 

  27. Kuwayama, Y. et al. Overall distribution of glucagon-like immunoreactivity in the chicken retina: an immunohistochemical study with flat mounts. Invest. Ophthal. Vis. Sci. 22, 681– 686 (1982).

    CAS  PubMed  Google Scholar 

  28. Schmid, K. L. & Wildsoet, C. F. Effects on the compensatory responses to positive and negative lenses of intermittent lens wear and ciliary nerve section in chicks. Vision Res. 36, 1023–1036 (1996).

    Article  CAS  Google Scholar 

  29. Schaeffel, F. & Diether, S. The growing eye—an autofocus system that works on very poor images. Vision Res. 39, 1585–1589 (1999).

    Article  CAS  Google Scholar 

  30. McBrien, N. A., Moghaddam, H. O., Cottriall, C. L., Leech, E. M. & Cornell, L. M. The effects of blockade of retinal cell action potentials on ocular growth, emmetropization and form deprivation myopia in young chicks. Vision Res. 35, 1141–1152 (1995) .

    Article  CAS  Google Scholar 

  31. Wildsoet, C. & Wallman, J. Choroidal and scleral mechanisms of compensation for spectacle lenses in chicks. Vision Res. 35, 1175–1194 (1995).

    Article  CAS  Google Scholar 

  32. Rohrer, B., Spira, A. W. & Stell, W. K. Apomorphine blocks form-deprivation myopia in chickens by a dopamine D2-receptor mechanism acting in retina or pigmented epithelium. Vis. Neurosci. 10, 447– 453 (1993).

    Article  CAS  Google Scholar 

  33. Owusu-Yaw, V., Kyle, A. L. & Stell, W. K. Effects of lesions of the optic nerve, optic tectum and nervus terminalis on rod precursor proliferation in the goldfish retina. Brain Res. 576, 220–230 (1992).

    Article  CAS  Google Scholar 

  34. Fischer, A. J. & Stell, W. K. Localization and identification of different isoforms of nitric oxide synthase in the chick eye. J. Comp. Neurol. 405, 1– 14 (1999).

    Article  CAS  Google Scholar 

  35. Ramon y Cajal, S. R. in The Structure of the Retina (eds. Thorpe, S. A. & Glickstein, M.) 76–92 (Thomas, Springfield, 1972).

    Google Scholar 

  36. Uchiyama, H. & Ito, H. Target cells for the isthmo-optic fibers in the retina of the Japanese quail. Neurosci. Lett. 154, 35–38 (1993).

    Article  CAS  Google Scholar 

  37. Crossland, W. J. & Hughes, C. P. Observations on the afferent and efferent connections of the avian isthmo-optic nucleus. Brain Res. 145, 239–256 (1978).

    Article  CAS  Google Scholar 

  38. de la Villa, P., Kurahashi, T. & Kaneko, A. L-glutamate-induced responses and cGMP-activated channels in three subtypes of retinal bipolar cells dissociated from the cat. J. Neurosci. 15, 3571–3582 (1995).

    Article  CAS  Google Scholar 

  39. Grünert, U., Martin, P. R. & Wässle, H. Immunocytochemical analysis of bipolar cells in the macaque monkey retina. J. Comp. Neurol. 348, 607–627 (1994).

    Article  Google Scholar 

  40. Brandstätter, J. H., Hartveit, E., Sassoë-Pognetto, M. & Wässle, H. Expression of NMDA and high-affinity kainate receptor subunit mRNAs in the adult rat retina. Eur. J. Neurosci. 6, 1100 –1112 (1994).

    Article  Google Scholar 

  41. Hartveit, E. et al. Localization and developmental expression of the NMDA receptor subunit NR2A in the mammalian retina. J. Comp. Neurol. 348, 570–582 (1994).

    Article  CAS  Google Scholar 

  42. Vaney, D. The mosaic of amacrine cells in the mammalian retina. Prog. Retinal Res. 9, 49–100 ( 1990).

    Article  CAS  Google Scholar 

  43. Vaney, D. I. Patterns of neuronal coupling in the retina. Prog. Retinal Res. 13, 301–355 ( 1993).

    Article  Google Scholar 

  44. Dowling, J. E. The Retina: An Approachable Part of the Brain (Belknap/Harvard, Cambridge, Massachusetts, 1987).

    Google Scholar 

Download references

Acknowledgements

This research was supported by a studentship from the Alberta Heritage Foundation for Medical Research and a University of Calgary Silver Anniversary Graduate Fellowship to A.J.F., grants from the Alberta Children's Hospital Foundation, the University of Calgary Research Grants Committee and the Marigold Foundation of Calgary to W.K.S. and the Max Planck Prize to F.S.

Author information

Author notes

  1. Andy J. Fischer

    Present address: Department of Biological Structure, University of Washington School of Medicine, Health Science Center, PO 357420, Seattle, Washington, 98195, USA

Authors and Affiliations

  1. Department of Anatomy and Cell Biology, Neuroscience Research Group, and the Lions' Sight Centre, University of Calgary Faculty of Medicine, 3330 Hospital Drive N.W., Calgary , T2N 4N1, Alberta, Canada

    Andy J. Fischer, Jennifer J. McGuire & William K. Stell

  2. Division of Experimental Ophthalmology, University Eye Hospital, Tübingen, Roentgenweg 11, Tübingen, 72076, Germany

    Frank Schaeffel

Authors
  1. Andy J. Fischer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jennifer J. McGuire
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Frank Schaeffel
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. William K. Stell
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andy J. Fischer.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fischer, A., McGuire, J., Schaeffel, F. et al. Light- and focus-dependent expression of the transcription factor ZENK in the chick retina. Nat Neurosci 2, 706–712 (1999). https://doi.org/10.1038/11167

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/11167

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing