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Influences on neural lineage and mode of division in the zebrafish retina in vivo.

Poggi L, Vitorino M, Masai I, Harris WA - J. Cell Biol. (2005)

Bottom Line: Proc.Natl.This study provides the first insight into reproducible lineage patterns of retinal progenitors in vivo and the first evidence that environmental signals influence the orientation of cell division and the lineage of neural progenitors.

View Article: PubMed Central - PubMed

Affiliation: Department of Anatomy, University of Cambridge, Cambridge CB2 3DY, United Kingdom.

ABSTRACT
Cell determination in the retina has been under intense investigation since the discovery that retinal progenitors generate clones of apparently random composition (Price, J., D. Turner, and C. Cepko. 1987. Proc. Natl. Acad. Sci. USA. 84:156-160; Holt, C.E., T.W. Bertsch, H.M. Ellis, and W.A. Harris. 1988. Neuron. 1:15-26; Wetts, R., and S.E. Fraser. 1988. Science. 239:1142-1145). Examination of fixed tissue, however, sheds little light on lineage patterns or on the relationship between the orientation of division and cell fate. In this study, three-dimensional time-lapse analyses were used to trace lineages of retinal progenitors expressing green fluorescent protein under the control of the ath5 promoter. Surprisingly, these cells divide just once along the circumferential axis to produce two postmitotic daughters, one of which becomes a retinal ganglion cell (RGC). Interestingly, when these same progenitors are transplanted into a mutant environment lacking RGCs, they often divide along the central-peripheral axis and produce two RGCs. This study provides the first insight into reproducible lineage patterns of retinal progenitors in vivo and the first evidence that environmental signals influence the orientation of cell division and the lineage of neural progenitors.

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ath5:GFP cells become RGCs and other cell types in the zebrafish retina. (A–C) Sections through the central retina of a 5-d ath5:GFP transgenic embryo. (A) The three retinal cell layers are separated by a white dashed line. (B) Retinal ganglion cell (RGC) ath5:GFP progenitors in the ganglion cell layer (GCL) are zn-5+. The white box in B indicates the area shown in C. Some ath5:GFP progenitors (C) become photoreceptors (Ph), amacrines (Am), and horizontal (Ho) cells. (D–F) Sections of 4-d ath5:GFP transgenic embryos immunostained with zpr-1 (D), PKCβ1 (E), and calretinin (F; arrows). White dashed lines separate the three retinal cell layers. ath5:GFP cells colabel with zpr-1 in the outer nuclear layer (ONL) and with calretinin in the inner nuclear layer (INL). ath5:GFP cells in the INL do not colabel with PKCβ1.
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fig2: ath5:GFP cells become RGCs and other cell types in the zebrafish retina. (A–C) Sections through the central retina of a 5-d ath5:GFP transgenic embryo. (A) The three retinal cell layers are separated by a white dashed line. (B) Retinal ganglion cell (RGC) ath5:GFP progenitors in the ganglion cell layer (GCL) are zn-5+. The white box in B indicates the area shown in C. Some ath5:GFP progenitors (C) become photoreceptors (Ph), amacrines (Am), and horizontal (Ho) cells. (D–F) Sections of 4-d ath5:GFP transgenic embryos immunostained with zpr-1 (D), PKCβ1 (E), and calretinin (F; arrows). White dashed lines separate the three retinal cell layers. ath5:GFP cells colabel with zpr-1 in the outer nuclear layer (ONL) and with calretinin in the inner nuclear layer (INL). ath5:GFP cells in the INL do not colabel with PKCβ1.

Mentions: ath5 mRNA is rapidly lost from differentiating progenitors and is not visible even in mature RGCs. However, the persistence of stable GFP protein in transgenic zebrafish allowed us to track the fate of ath5:GFP-positive cells to later stages. Therefore, we analyzed the distribution of positive cells in 5-d postfertilization retinas, when all retinal cell layers are differentiated and distinguishable. Histological sections through the central retina showed GFP-positive cells in the ganglion cell layer (GCL) as expected. These cells colabeled with the RGC-specific antibody zn-5. There were also many GFP-positive cells in the inner nuclear layer (INL) and outer nuclear layer (ONL; Fig. 2, A–C). GFP-positive INL cells could often be identified by their morphologies and positions as either horizontal or amacrine cells (Fig. 2 C). Interestingly, we found that the INL GFP-positive cells do not colabel with the bipolar marker PKCβ1; on the other hand, some colabel with the amacrine-specific marker calretinin (Fig. 2, E and F), further suggesting that at least a number of these INL cells are amacrines. The GFP-positive cells in the ONL had the morphology of photoreceptors and expressed the photoreceptor-specific marker zpr-1 (Fig. 2 D). These results show that RGCs are not the exclusive fate choice of ath5-expressing retinal progenitors in the zebrafish retina.


Influences on neural lineage and mode of division in the zebrafish retina in vivo.

Poggi L, Vitorino M, Masai I, Harris WA - J. Cell Biol. (2005)

ath5:GFP cells become RGCs and other cell types in the zebrafish retina. (A–C) Sections through the central retina of a 5-d ath5:GFP transgenic embryo. (A) The three retinal cell layers are separated by a white dashed line. (B) Retinal ganglion cell (RGC) ath5:GFP progenitors in the ganglion cell layer (GCL) are zn-5+. The white box in B indicates the area shown in C. Some ath5:GFP progenitors (C) become photoreceptors (Ph), amacrines (Am), and horizontal (Ho) cells. (D–F) Sections of 4-d ath5:GFP transgenic embryos immunostained with zpr-1 (D), PKCβ1 (E), and calretinin (F; arrows). White dashed lines separate the three retinal cell layers. ath5:GFP cells colabel with zpr-1 in the outer nuclear layer (ONL) and with calretinin in the inner nuclear layer (INL). ath5:GFP cells in the INL do not colabel with PKCβ1.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2171316&req=5

fig2: ath5:GFP cells become RGCs and other cell types in the zebrafish retina. (A–C) Sections through the central retina of a 5-d ath5:GFP transgenic embryo. (A) The three retinal cell layers are separated by a white dashed line. (B) Retinal ganglion cell (RGC) ath5:GFP progenitors in the ganglion cell layer (GCL) are zn-5+. The white box in B indicates the area shown in C. Some ath5:GFP progenitors (C) become photoreceptors (Ph), amacrines (Am), and horizontal (Ho) cells. (D–F) Sections of 4-d ath5:GFP transgenic embryos immunostained with zpr-1 (D), PKCβ1 (E), and calretinin (F; arrows). White dashed lines separate the three retinal cell layers. ath5:GFP cells colabel with zpr-1 in the outer nuclear layer (ONL) and with calretinin in the inner nuclear layer (INL). ath5:GFP cells in the INL do not colabel with PKCβ1.
Mentions: ath5 mRNA is rapidly lost from differentiating progenitors and is not visible even in mature RGCs. However, the persistence of stable GFP protein in transgenic zebrafish allowed us to track the fate of ath5:GFP-positive cells to later stages. Therefore, we analyzed the distribution of positive cells in 5-d postfertilization retinas, when all retinal cell layers are differentiated and distinguishable. Histological sections through the central retina showed GFP-positive cells in the ganglion cell layer (GCL) as expected. These cells colabeled with the RGC-specific antibody zn-5. There were also many GFP-positive cells in the inner nuclear layer (INL) and outer nuclear layer (ONL; Fig. 2, A–C). GFP-positive INL cells could often be identified by their morphologies and positions as either horizontal or amacrine cells (Fig. 2 C). Interestingly, we found that the INL GFP-positive cells do not colabel with the bipolar marker PKCβ1; on the other hand, some colabel with the amacrine-specific marker calretinin (Fig. 2, E and F), further suggesting that at least a number of these INL cells are amacrines. The GFP-positive cells in the ONL had the morphology of photoreceptors and expressed the photoreceptor-specific marker zpr-1 (Fig. 2 D). These results show that RGCs are not the exclusive fate choice of ath5-expressing retinal progenitors in the zebrafish retina.

Bottom Line: Proc.Natl.This study provides the first insight into reproducible lineage patterns of retinal progenitors in vivo and the first evidence that environmental signals influence the orientation of cell division and the lineage of neural progenitors.

View Article: PubMed Central - PubMed

Affiliation: Department of Anatomy, University of Cambridge, Cambridge CB2 3DY, United Kingdom.

ABSTRACT
Cell determination in the retina has been under intense investigation since the discovery that retinal progenitors generate clones of apparently random composition (Price, J., D. Turner, and C. Cepko. 1987. Proc. Natl. Acad. Sci. USA. 84:156-160; Holt, C.E., T.W. Bertsch, H.M. Ellis, and W.A. Harris. 1988. Neuron. 1:15-26; Wetts, R., and S.E. Fraser. 1988. Science. 239:1142-1145). Examination of fixed tissue, however, sheds little light on lineage patterns or on the relationship between the orientation of division and cell fate. In this study, three-dimensional time-lapse analyses were used to trace lineages of retinal progenitors expressing green fluorescent protein under the control of the ath5 promoter. Surprisingly, these cells divide just once along the circumferential axis to produce two postmitotic daughters, one of which becomes a retinal ganglion cell (RGC). Interestingly, when these same progenitors are transplanted into a mutant environment lacking RGCs, they often divide along the central-peripheral axis and produce two RGCs. This study provides the first insight into reproducible lineage patterns of retinal progenitors in vivo and the first evidence that environmental signals influence the orientation of cell division and the lineage of neural progenitors.

Show MeSH
Related in: MedlinePlus