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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 progenitors generate two RGCs after division in the lakritz environment. (A) The two daughter cells have been highlighted in yellow or red. Time-lapse series showing an example of an ath5:GFP progenitor generating two RGCs in the lakritz environment. Imaging was started at 30–32 h after fertilization, and t = 0 corresponds to the time of appearance of ath5:GFP (4 h after the onset of the video recording). After 11 h, the red daughter cell starts migrating toward the apical surface. Once it has reached the apical surface (t = 15 h), it migrates back again toward the basal surface, where it differentiates in RGCs. The location of both daughter cells after 20 h is outlined by a white dotted line. Both cells were zn-5 positive after immunolabeling of the imaged retina. (B) An example of a time-lapse series showing an ath5:GFP progenitor that divides and generates another dividing progenitor. Imaging was started 30–32 h after fertilization, and t = 0 corresponds to the time of appearance of ath5:GFP (3 h after the onset of the video recording). At t = 9.40 h, the progenitor highlighted in red divides once more at the apical surface, generating one daughter cell (green) that lost its apical process and began to put out an axon and another daughter cell (red) that remained apical. White arrowheads point to the retracting apical process and the forming axon. AP, apical cell; RGC, retinal ganglion cell.
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fig5: ath5:GFP progenitors generate two RGCs after division in the lakritz environment. (A) The two daughter cells have been highlighted in yellow or red. Time-lapse series showing an example of an ath5:GFP progenitor generating two RGCs in the lakritz environment. Imaging was started at 30–32 h after fertilization, and t = 0 corresponds to the time of appearance of ath5:GFP (4 h after the onset of the video recording). After 11 h, the red daughter cell starts migrating toward the apical surface. Once it has reached the apical surface (t = 15 h), it migrates back again toward the basal surface, where it differentiates in RGCs. The location of both daughter cells after 20 h is outlined by a white dotted line. Both cells were zn-5 positive after immunolabeling of the imaged retina. (B) An example of a time-lapse series showing an ath5:GFP progenitor that divides and generates another dividing progenitor. Imaging was started 30–32 h after fertilization, and t = 0 corresponds to the time of appearance of ath5:GFP (3 h after the onset of the video recording). At t = 9.40 h, the progenitor highlighted in red divides once more at the apical surface, generating one daughter cell (green) that lost its apical process and began to put out an axon and another daughter cell (red) that remained apical. White arrowheads point to the retracting apical process and the forming axon. AP, apical cell; RGC, retinal ganglion cell.

Mentions: A likely explanation for the increase in the proportion of ath:GFP-positive RGCs in lakritz versus wild-type hosts is that the lineage of the ath5:GFP progenitors is changed in these circumstances. Therefore, we traced the lineages of a number of dividing ath5:GFP cells in lakritz hosts. Again, no cell deaths were observed in the transplanted population of ath5:GFP-positive cells, and progenitors displayed normal interkinetic nuclear movements. Strikingly, these dividing progenitors showed different lineage patterns in lakritz than in wild-type hosts. In many instances, both daughter cells began to differentiate as RGCs (Fig. 5 A and Video 5, available at http://www.jcb.org/cgi/content/full/jcb.200509098/DC1), and, in two cases, a progenitor divided twice, giving rise to one RGC with each division (Fig. 5 B and Video 6). A diagram comparison of the 14 lineages that we were able to follow in each of the two environments are shown in Fig. 6 A. Clearly, there is a striking difference between these two populations. Moreover, if it is the case that all RGCs normally arise from ath5-expressing progenitors, the changes in lineage programs represented in this study are enough to account for the increase in RGCs when ath5:GFP progenitors are transplanted into an environment lacking RGCs (Fig. 6 B).


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 progenitors generate two RGCs after division in the lakritz environment. (A) The two daughter cells have been highlighted in yellow or red. Time-lapse series showing an example of an ath5:GFP progenitor generating two RGCs in the lakritz environment. Imaging was started at 30–32 h after fertilization, and t = 0 corresponds to the time of appearance of ath5:GFP (4 h after the onset of the video recording). After 11 h, the red daughter cell starts migrating toward the apical surface. Once it has reached the apical surface (t = 15 h), it migrates back again toward the basal surface, where it differentiates in RGCs. The location of both daughter cells after 20 h is outlined by a white dotted line. Both cells were zn-5 positive after immunolabeling of the imaged retina. (B) An example of a time-lapse series showing an ath5:GFP progenitor that divides and generates another dividing progenitor. Imaging was started 30–32 h after fertilization, and t = 0 corresponds to the time of appearance of ath5:GFP (3 h after the onset of the video recording). At t = 9.40 h, the progenitor highlighted in red divides once more at the apical surface, generating one daughter cell (green) that lost its apical process and began to put out an axon and another daughter cell (red) that remained apical. White arrowheads point to the retracting apical process and the forming axon. AP, apical cell; RGC, retinal ganglion cell.
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Related In: Results  -  Collection

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fig5: ath5:GFP progenitors generate two RGCs after division in the lakritz environment. (A) The two daughter cells have been highlighted in yellow or red. Time-lapse series showing an example of an ath5:GFP progenitor generating two RGCs in the lakritz environment. Imaging was started at 30–32 h after fertilization, and t = 0 corresponds to the time of appearance of ath5:GFP (4 h after the onset of the video recording). After 11 h, the red daughter cell starts migrating toward the apical surface. Once it has reached the apical surface (t = 15 h), it migrates back again toward the basal surface, where it differentiates in RGCs. The location of both daughter cells after 20 h is outlined by a white dotted line. Both cells were zn-5 positive after immunolabeling of the imaged retina. (B) An example of a time-lapse series showing an ath5:GFP progenitor that divides and generates another dividing progenitor. Imaging was started 30–32 h after fertilization, and t = 0 corresponds to the time of appearance of ath5:GFP (3 h after the onset of the video recording). At t = 9.40 h, the progenitor highlighted in red divides once more at the apical surface, generating one daughter cell (green) that lost its apical process and began to put out an axon and another daughter cell (red) that remained apical. White arrowheads point to the retracting apical process and the forming axon. AP, apical cell; RGC, retinal ganglion cell.
Mentions: A likely explanation for the increase in the proportion of ath:GFP-positive RGCs in lakritz versus wild-type hosts is that the lineage of the ath5:GFP progenitors is changed in these circumstances. Therefore, we traced the lineages of a number of dividing ath5:GFP cells in lakritz hosts. Again, no cell deaths were observed in the transplanted population of ath5:GFP-positive cells, and progenitors displayed normal interkinetic nuclear movements. Strikingly, these dividing progenitors showed different lineage patterns in lakritz than in wild-type hosts. In many instances, both daughter cells began to differentiate as RGCs (Fig. 5 A and Video 5, available at http://www.jcb.org/cgi/content/full/jcb.200509098/DC1), and, in two cases, a progenitor divided twice, giving rise to one RGC with each division (Fig. 5 B and Video 6). A diagram comparison of the 14 lineages that we were able to follow in each of the two environments are shown in Fig. 6 A. Clearly, there is a striking difference between these two populations. Moreover, if it is the case that all RGCs normally arise from ath5-expressing progenitors, the changes in lineage programs represented in this study are enough to account for the increase in RGCs when ath5:GFP progenitors are transplanted into an environment lacking RGCs (Fig. 6 B).

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