Different levels of epidermal growth factor signaling modifies the differentiation of specific cell types in mouse postnatal retina

Authors

  • Sanja Ivković Department for Neurobiology, Institute for Biological Research “Siniša Stanković” - National Institute of Republic of Serbia, University of Belgrade, Bulevar despota Stefana 142, 11060 Belgrade
  • Irena Jovanović Macura Department for Neurobiology, Institute for Biological Research “Siniša Stanković” - National Institute of Republic of Serbia, University of Belgrade, Bulevar despota Stefana 142, 11060 Belgrade
  • Tijana Antonijević Department for Neurobiology, Institute for Biological Research “Siniša Stanković” - National Institute of Republic of Serbia, University of Belgrade, Bulevar despota Stefana 142, 11060 Belgrade
  • Selma Kanazir Department for Neurobiology, Institute for Biological Research “Siniša Stanković” - National Institute of Republic of Serbia, University of Belgrade, Bulevar despota Stefana 142, 11060 Belgrade
  • Domingos Henrique Instituto de Medicina Molecular, Faculdade de Medicina da Universidade de Lisboa, Avenida Professor Egas Moniz, 1649-028 Lisbon

Keywords:

retina, EGFR, progenitors, differentiation, postnatal development

Abstract

Paper description:

  • Different levels of Epidermal Growth Factor (EGF) signaling can have different effects on progenitor’s destiny during the embryonic and postnatal retinal development.
  • The addition of EGF-receptor into postnatal retinal progenitors ensured the sustained signaling in the presence of the exogenous EGF ligand during the first postnatal week in the model system of the retinal explants (REs).
  • The continuous EGF signaling altered postnatal progenitors’ competence restrictions.
  • Better understanding of how different levels of EGF signaling can affect progenitor’s competence can elucidate the ways of interfering with the developmental programs and thus facilitate retinal regeneration.


Abstract: Epidermal growth factor (EGF) signaling has been implicated in the regulation of the differentiation and proliferation of retinal progenitors. We assessed how different levels of EGF signaling, achieved either by increasing receptor expression or via addition of the exogenous ligand, or an increase in both, can affect the differentiation of progenitors in the first week of postnatal retinal development in the model system of retinal explants (REs). Proliferating progenitor cells in REs were infected with either the control CLV3/ESR-related peptide family (CLE)-green fluorescent protein (GFP)- or with EGF receptor (EGFR)-GFP-expressing retrovirus, and grown in the control medium or in the presence of exogenous EGF (10 ng/mL). The differentiation of infected cells into Müller glia (Sox9+), rod photoreceptors (rhodopsin+) and horizontal cells (calbindin+) was analyzed. In all the examined conditions, infected cells differentiated into Müller glia and rod photoreceptors that normally develop postnatally. Horizontal cells finished their development during the embryonic stages and progenitors infected with control-GFP virus did not differentiate into GFP+/calbindin- in either control or EGF-supplemented medium, however, cells infected with EGFR-GFP differentiated into horizontal cells (GFP+/calbindin+) in both culture conditions. These results imply that altering the levels of EGFR and/or the amount of the EGF ligand can overcome progenitor competence restriction.

https://doi.org/10.2298/ABS190617054I

Received: June 17, 2019; Revised: August 22, 2019; Accepted: September 4, 2019; Published online: September 5, 2019

How to cite this article: Ivković S, Jovanović-Macura I, Antonijević T, Kanazir S, Henrique D. Different levels of epidermal growth factor signaling modifies the differentiation of specific cell types in mouse postnatal retina. Arch Biol Sci. 2019;71(4):711-9.

Downloads

Download data is not yet available.

References

Cepko CL, Austin CP, Yang X, Alexiades M, Ezzedine D. Cell fate determination in the vertebrate retina. Proc Natl Acad Sci U S A. 1996;93:589-95.

Livesey R, Cepko C. Vertebrate neural cell-fate determination: lessons from the retina. Nat. Rev. Neurosci. 2001;2:109-18.

Raz E, Shilo B-Z. Establishment of ventral cell fates in the Drosophila embryonic ectoderm requires DER, the EGF receptor homolog. Genes Dev. 1993;7:1937-48.

Diaz-Benjumea FJ, Hafen E. The sevenless signaling cassette mediates Drosophila EGF receptor function during epidermal development. Development. 1994;120:569-78.

Schweitzer R, Shaharabany M, Seger R, Shilo B-Z. Secreted Spitz triggers the DER signaling pathway and is a limiting component in embryonic ventral ectoderm determination. Genes Dev. 1995;9:1518-29.

Katz WS, Hill RJ, Clandinin TR, Sternberg PW. Different levels of the C. elegans growth factor LIN-3 promote distinct vulval precursor fates. Cell. 1995;82:297-307.

Lillien L, Cepko C. Control of proliferation in the retina: temporal changes in responsiveness to FGF and TGF alpha. Development. 1992;115:253-66.

Close JL, Liu J, Gumuscu B, Reh TA. Epidermal growth factor receptor expression regulates proliferation in the postnatal rat retina. Glia. 2006;54:94-104.

Traverse S, Seedorf K, Paterson H, Marshall CJ, Cohen P, Ullrich A. EGF triggers neuronal differentiation of PC12 cells that overexpresses the EGF receptor. Curr Biol. 1994;4:694-701.

Lillien L. Changes in retinal cell fate induced by overexpression of EGF receptor. Nature. 1995;377:158-62.

Neophytou C, Vernallis AB, Smith A, Raff MC. Müller-cell-derived leukaemia inhibitory factor arrests rod photoreceptor differentiation at a postmitotic pre-rod stage of development. Development. 1997;124:2345-54.

Rhee KD, Goureau O, Chen S, Yang X-J. Cytokine-induced activation of signal transducer and activator of transcription in photoreceptor precursors regulates rod differentiation in the developing mouse retina. J Neurosci. 2004;24:9779 -88.

Burrows RC, Wancio D, Levitt P, Lillien L. Response diversity and the timing of progenitor cell maturation are regulated by developmental changes in EGF-R expression in the cortex. Neuron. 1997;19:251-67.

Lillien L, Wancio D. Changes in epidermal growth factor receptor expression and competence to generate glia regulate timing and choice of differentiation in the retina. Mol Cell Neurosci. 1998;10:296-308.

Ivkovic S, Canoll P, Goldman JE. Constitutive EGFR signaling in oligodendrocyte progenitors leads to diffuse hyperplasia in postnatal white matter. J Neurosci. 2008;28:914-22.

Sun Y, Goderie SK, Temple S. Asymmetric distribution of EGFR receptor during mitosis generates diverse CNS progenitor cells. Neuron. 2005;45:873-86.

Gaiano N, Kohtz JD, Turnbull DH, Fishell G. A method for rapid gain-of-function studies in the mouse embryonic nervous system. Nature. 1999;2:812-9.

Kakita A, Goldman JE. Patterns and dynamics of SVZ cell migration

in the postnatal forebrain: monitoring living progenitors in slice preparations. Neuron. 1999;23:461-72.

Hatakeyama J, Kageyama R. Retrovirus-mediated gene transfer to retinal explants. Methods. 2002;28:387-95.

Young RW. Cell proliferation during postnatal development of the retina in the mouse. Brain Res. 1985;353:229-39.

Turner DL, Cepko CL. A common progenitor for neurons and glia persists in rat retina late in development. Nature. 1987;328:131-6.

Haverkamp S, Wassle H. Immunocytochemical analysis of the mouse retina. J Comp Neurol. 2000;424:1-23.

McAvoy JW, Chamberlin CG. Fibroblast growth factor induces different responses in lens epithelial cells depending on its concentration. Development. 1989;107:221-8.

Green JBA, Smith JC. Graded changes in dose of a Xenopus activin A homologue elicit stepwise transitions in embryonic cell fate. Nature. 1990;347:391-4.

Roelink H, Porter JA, Chiang C, Tanabe Y, Chang TJ, Beachy PA, Jessell TM. Floor plate and motor neuron induction by different concentrations of the amino-terminal cleavage product of sonic hedgehog autoproteolysis. Cell. 1995;81:445-55.

Johnson RL, Tabin C. The long and short of hedgehog signaling. Cell. 1995;81:313-6.

Hynes M, Porter JA, Chiang C, Chang D, Tessier-Lavigne M, Beachy PA, Rosenthal A. Induction of midbrain dopaminergic neurons by sonic hedgehog. Neuron. 1995;15:35-44.

Goentoro LA, Reeves GT, Kowal CP, Martinelli L, Schupbach T, Shvartsman SY. Quantifying the Gurken morphogen gradient in Drosophila oogenesis. Dev Cell. 2006;11:263-72.

Bergmann S, Sandler O, Sberro H, Shnider S, Schejter E, Shilo BZ, Barkai N. Pre-steady-state decoding of the Bicoid morphogen gradient. PLoS Biol.2007;5:e46.

Anchan RM, Reh TA, Angello J, Balliet A, Walker M. EGF and TGF-alpha stimulate retinal neuroepithelial cell proliferation in vitro. Neuron. 1991;6:923-36.

Anchan RM, Reh TA. Transforming growth factor-beta-3 is mitogenic for rat retinal progenitor cells in vitro. J Neurobiol. 1995;28:133-45.

Sidman RL, 1960. The structure of the eye. In: Smelser GK, editor. Seventh International Congress of Anatomists. New York: Academic Press; 1960. p. 487-505.

Poche RA, Resse BE. Retinal horizontal cells: challenging paradigms of neural development and cancer biology. Development. 2009;136:2141-51.

Ajioka I, Martins RA, Bayazitov IT, Donovan S, Johnson DA, Frase S, Cicero SA, Boyd K, Zakharenko SS, Dyer MA. Differentiated horizontal interneurons clonally expand to form metastatic retinoblastoma in mice. Cell. 2007;131:378-90.

Watanabe T, Raff MC. Rod photoreceptor development in vitro: intrinsic properties of proliferating neuroepithelial cells change as development proceeds in the rat retina. Neuron. 1990;4:461-7.

Sonntag S, Dedek K, Dorgau B, Schultz K, Schmidt K-F, Cimiotti K, Weiler R, Lowel S, Willecke K, Janssen-Bienhold U. Ablation of retinal horizontal cells from adult mice leads to rod degeneration and remodeling in the outer retina. J Neurosci. 2012; 32:10713-24.

Downloads

Published

2019-12-19

How to Cite

1.
Ivković S, Jovanović Macura I, Antonijević T, Kanazir S, Henrique D. Different levels of epidermal growth factor signaling modifies the differentiation of specific cell types in mouse postnatal retina. Arch Biol Sci [Internet]. 2019Dec.19 [cited 2024Nov.21];71(4):711-9. Available from: https://serbiosoc.org.rs/arch/index.php/abs/article/view/4389

Issue

Vol. 71 No. 4 (2019)

Section

Articles

License

Authors grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution 4.0 International License that allows others to share the work with an acknowledgment of the work’s authorship and initial publication in this journal.