Asymmetric inheritance of the apical domain and self-renewal of retinal ganglion cell progenitors depend on Anillin function

Alessio Paolini, Anne-Laure Duchemin, Shahad Albadri, Eva Patzel, Dorothee Bornhorst, Paula Gonzalez Avalos, Steffen Lemke, Anja Machate, Michael Brand, Saadettin Sel, Vincenzo Di Donato, Filippo Del Bene, Flavio R Zolessi, Mirana Soa Manarivo Ramialison, Lucia Poggi

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9 Citations (Scopus)

Abstract

Divisions that generate one neuronal lineage-committed and one self-renewing cell maintain the balance of proliferation and differentiation for the generation of neuronal diversity. The asymmetric inheritance of apical domains and components of the cell division machinery has been implicated in this process, and might involve interactions with cell fate determinants in regulatory feedback loops of an as yet unknown nature. Here, we report the dynamics of Anillin - an essential F-actin regulator and furrow component - and its contribution to progenitor cell divisions in the developing zebrafish retina. We find that asymmetrically dividing retinal ganglion cell progenitors position the Anillin-rich midbody at the apical domain of the differentiating daughter. anillin hypomorphic conditions disrupt asymmetric apical domain inheritance and affect daughter cell fate. Consequently, the retinal cell type composition is profoundly affected, such that the ganglion cell layer is dramatically expanded. This study provides the first in vivo evidence for the requirement of Anillin during asymmetric neurogenic divisions. It also provides insights into a reciprocal regulation between Anillin and the ganglion cell fate determinant Ath5, suggesting a mechanism whereby the balance of proliferation and differentiation is accomplished during progenitor cell divisions in vivo.
Original languageEnglish
Pages (from-to)832 - 839
Number of pages8
JournalDevelopment
Volume142
Issue number5
DOIs
Publication statusPublished - 2015

Cite this

Paolini, A., Duchemin, A-L., Albadri, S., Patzel, E., Bornhorst, D., Gonzalez Avalos, P., ... Poggi, L. (2015). Asymmetric inheritance of the apical domain and self-renewal of retinal ganglion cell progenitors depend on Anillin function. Development, 142(5), 832 - 839. https://doi.org/10.1242/dev.118612
Paolini, Alessio ; Duchemin, Anne-Laure ; Albadri, Shahad ; Patzel, Eva ; Bornhorst, Dorothee ; Gonzalez Avalos, Paula ; Lemke, Steffen ; Machate, Anja ; Brand, Michael ; Sel, Saadettin ; Di Donato, Vincenzo ; Del Bene, Filippo ; Zolessi, Flavio R ; Ramialison, Mirana Soa Manarivo ; Poggi, Lucia. / Asymmetric inheritance of the apical domain and self-renewal of retinal ganglion cell progenitors depend on Anillin function. In: Development. 2015 ; Vol. 142, No. 5. pp. 832 - 839.
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title = "Asymmetric inheritance of the apical domain and self-renewal of retinal ganglion cell progenitors depend on Anillin function",
abstract = "Divisions that generate one neuronal lineage-committed and one self-renewing cell maintain the balance of proliferation and differentiation for the generation of neuronal diversity. The asymmetric inheritance of apical domains and components of the cell division machinery has been implicated in this process, and might involve interactions with cell fate determinants in regulatory feedback loops of an as yet unknown nature. Here, we report the dynamics of Anillin - an essential F-actin regulator and furrow component - and its contribution to progenitor cell divisions in the developing zebrafish retina. We find that asymmetrically dividing retinal ganglion cell progenitors position the Anillin-rich midbody at the apical domain of the differentiating daughter. anillin hypomorphic conditions disrupt asymmetric apical domain inheritance and affect daughter cell fate. Consequently, the retinal cell type composition is profoundly affected, such that the ganglion cell layer is dramatically expanded. This study provides the first in vivo evidence for the requirement of Anillin during asymmetric neurogenic divisions. It also provides insights into a reciprocal regulation between Anillin and the ganglion cell fate determinant Ath5, suggesting a mechanism whereby the balance of proliferation and differentiation is accomplished during progenitor cell divisions in vivo.",
author = "Alessio Paolini and Anne-Laure Duchemin and Shahad Albadri and Eva Patzel and Dorothee Bornhorst and {Gonzalez Avalos}, Paula and Steffen Lemke and Anja Machate and Michael Brand and Saadettin Sel and {Di Donato}, Vincenzo and {Del Bene}, Filippo and Zolessi, {Flavio R} and Ramialison, {Mirana Soa Manarivo} and Lucia Poggi",
year = "2015",
doi = "10.1242/dev.118612",
language = "English",
volume = "142",
pages = "832 -- 839",
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Paolini, A, Duchemin, A-L, Albadri, S, Patzel, E, Bornhorst, D, Gonzalez Avalos, P, Lemke, S, Machate, A, Brand, M, Sel, S, Di Donato, V, Del Bene, F, Zolessi, FR, Ramialison, MSM & Poggi, L 2015, 'Asymmetric inheritance of the apical domain and self-renewal of retinal ganglion cell progenitors depend on Anillin function', Development, vol. 142, no. 5, pp. 832 - 839. https://doi.org/10.1242/dev.118612

Asymmetric inheritance of the apical domain and self-renewal of retinal ganglion cell progenitors depend on Anillin function. / Paolini, Alessio; Duchemin, Anne-Laure; Albadri, Shahad; Patzel, Eva; Bornhorst, Dorothee; Gonzalez Avalos, Paula; Lemke, Steffen; Machate, Anja; Brand, Michael; Sel, Saadettin; Di Donato, Vincenzo; Del Bene, Filippo; Zolessi, Flavio R; Ramialison, Mirana Soa Manarivo; Poggi, Lucia.

In: Development, Vol. 142, No. 5, 2015, p. 832 - 839.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - Asymmetric inheritance of the apical domain and self-renewal of retinal ganglion cell progenitors depend on Anillin function

AU - Paolini, Alessio

AU - Duchemin, Anne-Laure

AU - Albadri, Shahad

AU - Patzel, Eva

AU - Bornhorst, Dorothee

AU - Gonzalez Avalos, Paula

AU - Lemke, Steffen

AU - Machate, Anja

AU - Brand, Michael

AU - Sel, Saadettin

AU - Di Donato, Vincenzo

AU - Del Bene, Filippo

AU - Zolessi, Flavio R

AU - Ramialison, Mirana Soa Manarivo

AU - Poggi, Lucia

PY - 2015

Y1 - 2015

N2 - Divisions that generate one neuronal lineage-committed and one self-renewing cell maintain the balance of proliferation and differentiation for the generation of neuronal diversity. The asymmetric inheritance of apical domains and components of the cell division machinery has been implicated in this process, and might involve interactions with cell fate determinants in regulatory feedback loops of an as yet unknown nature. Here, we report the dynamics of Anillin - an essential F-actin regulator and furrow component - and its contribution to progenitor cell divisions in the developing zebrafish retina. We find that asymmetrically dividing retinal ganglion cell progenitors position the Anillin-rich midbody at the apical domain of the differentiating daughter. anillin hypomorphic conditions disrupt asymmetric apical domain inheritance and affect daughter cell fate. Consequently, the retinal cell type composition is profoundly affected, such that the ganglion cell layer is dramatically expanded. This study provides the first in vivo evidence for the requirement of Anillin during asymmetric neurogenic divisions. It also provides insights into a reciprocal regulation between Anillin and the ganglion cell fate determinant Ath5, suggesting a mechanism whereby the balance of proliferation and differentiation is accomplished during progenitor cell divisions in vivo.

AB - Divisions that generate one neuronal lineage-committed and one self-renewing cell maintain the balance of proliferation and differentiation for the generation of neuronal diversity. The asymmetric inheritance of apical domains and components of the cell division machinery has been implicated in this process, and might involve interactions with cell fate determinants in regulatory feedback loops of an as yet unknown nature. Here, we report the dynamics of Anillin - an essential F-actin regulator and furrow component - and its contribution to progenitor cell divisions in the developing zebrafish retina. We find that asymmetrically dividing retinal ganglion cell progenitors position the Anillin-rich midbody at the apical domain of the differentiating daughter. anillin hypomorphic conditions disrupt asymmetric apical domain inheritance and affect daughter cell fate. Consequently, the retinal cell type composition is profoundly affected, such that the ganglion cell layer is dramatically expanded. This study provides the first in vivo evidence for the requirement of Anillin during asymmetric neurogenic divisions. It also provides insights into a reciprocal regulation between Anillin and the ganglion cell fate determinant Ath5, suggesting a mechanism whereby the balance of proliferation and differentiation is accomplished during progenitor cell divisions in vivo.

UR - http://dev.biologists.org/content/142/5/832.full.pdf+html

U2 - 10.1242/dev.118612

DO - 10.1242/dev.118612

M3 - Article

VL - 142

SP - 832

EP - 839

JO - Development

JF - Development

SN - 0950-1991

IS - 5

ER -