Centriole movements in mammalian epithelial cells during cytokinesis

Asta B. Jonsdottir; Roeland W. Dirks; Johannes Vrolijk; Helga M. Ögmundsdottir; Hans J. Tanke; Jorunn E. Eyfjörd; Karoly Szuhai

doi:10.1186/1471-2121-11-34

Centriole movements in mammalian epithelial cells during cytokinesis

Asta B. Jonsdottir, Roeland W. Dirks, Johannes Vrolijk, Helga M. Ögmundsdottir, Hans J. Tanke, Jorunn E. Eyfjörd, Karoly Szuhai

Faculty of Medicine

University of Iceland

Research output: Contribution to journal › Article › peer-review

Abstract

Background: In cytokinesis, when the cleavage furrow has been formed, the two centrioles in each daughter cell separate. It has been suggested that the centrioles facilitate and regulate cytokinesis to some extent. It has been postulated that termination of cytokinesis (abscission) depends on the migration of a centriole to the intercellular bridge and then back to the cell center. To investigate the involvement of centrioles in cytokinesis, we monitored the movements of centrioles in three mammalian epithelial cell lines, HeLa, MCF 10A, and the p53-deficient mouse mammary tumor cell line KP-7.7, by time-lapse imaging. Centrin1-EGFP and α-Tubulin-mCherry were co-expressed in the cells to visualize respectively the centrioles and microtubules.Results: Here we report that separated centrioles that migrate from the cell pole are very mobile during cytokinesis and their movements can be characterized as 1) along the nuclear envelope, 2) irregular, and 3) along microtubules forming the spindle axis. Centriole movement towards the intercellular bridge was only seen occasionally and was highly cell-line dependent.Conclusions: These findings show that centrioles are highly mobile during cytokinesis and suggest that the repositioning of a centriole to the intercellular bridge is not essential for controlling abscission. We suggest that centriole movements are microtubule dependent and that abscission is more dependent on other mechanisms than positioning of centrioles.

Original language	English
Article number	34
Journal	BMC Cell Biology
Volume	11
DOIs	https://doi.org/10.1186/1471-2121-11-34
Publication status	Published - 21 May 2010

Bibliographical note

Funding Information: Prof. Michel Bornens, Institute Curie, Paris, France, for centrin1-EGFP expression construct and Dr. Matthieu Piel, Institute Curie, Paris, France for stable centrin1-EGFP HeLa cell line and their helpful discussion and comments during the preparation of this manuscript. We thank Dr. Jan Ellenberg, EMBL, Heidelberg, Germany and Prof. Roger Tsien, Howard Hughes Medical Institute, University of California, San Diego, USA, for providing expression constructs. Dr. Jos Jonkers and Dr. Bastiaan Evers, The Netherlands Cancer Institute, Amsterdam, The Netherlands and Dr. Fanni Gergely, Cancer Research UK Cambridge Research Institute, Cambridge, England, for collaboration and Dr. Jos Jonkers for reviewing the manuscript. Willem Sloos, Leiden University Medical Centre, Leiden, The Netherlands for technical assistance. Prof. Gunnar Stefansson and Johanna Sigmundsdottir, Statistics Centre, University of Iceland, Reykjavik, Iceland, for assistance with statistical analysis. This work is funded by the University of Iceland Research Fund (ABJ), Soroptimist International of Europe (ABJ) and Gongum Saman (ABJ).

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@article{a04becd507d64a5ea2450084da0181d9,

title = "Centriole movements in mammalian epithelial cells during cytokinesis",

abstract = "Background: In cytokinesis, when the cleavage furrow has been formed, the two centrioles in each daughter cell separate. It has been suggested that the centrioles facilitate and regulate cytokinesis to some extent. It has been postulated that termination of cytokinesis (abscission) depends on the migration of a centriole to the intercellular bridge and then back to the cell center. To investigate the involvement of centrioles in cytokinesis, we monitored the movements of centrioles in three mammalian epithelial cell lines, HeLa, MCF 10A, and the p53-deficient mouse mammary tumor cell line KP-7.7, by time-lapse imaging. Centrin1-EGFP and α-Tubulin-mCherry were co-expressed in the cells to visualize respectively the centrioles and microtubules.Results: Here we report that separated centrioles that migrate from the cell pole are very mobile during cytokinesis and their movements can be characterized as 1) along the nuclear envelope, 2) irregular, and 3) along microtubules forming the spindle axis. Centriole movement towards the intercellular bridge was only seen occasionally and was highly cell-line dependent.Conclusions: These findings show that centrioles are highly mobile during cytokinesis and suggest that the repositioning of a centriole to the intercellular bridge is not essential for controlling abscission. We suggest that centriole movements are microtubule dependent and that abscission is more dependent on other mechanisms than positioning of centrioles.",

author = "Jonsdottir, \{Asta B.\} and Dirks, \{Roeland W.\} and Johannes Vrolijk and {\"O}gmundsdottir, \{Helga M.\} and Tanke, \{Hans J.\} and Eyfj{\"o}rd, \{Jorunn E.\} and Karoly Szuhai",

note = "Funding Information: Prof. Michel Bornens, Institute Curie, Paris, France, for centrin1-EGFP expression construct and Dr. Matthieu Piel, Institute Curie, Paris, France for stable centrin1-EGFP HeLa cell line and their helpful discussion and comments during the preparation of this manuscript. We thank Dr. Jan Ellenberg, EMBL, Heidelberg, Germany and Prof. Roger Tsien, Howard Hughes Medical Institute, University of California, San Diego, USA, for providing expression constructs. Dr. Jos Jonkers and Dr. Bastiaan Evers, The Netherlands Cancer Institute, Amsterdam, The Netherlands and Dr. Fanni Gergely, Cancer Research UK Cambridge Research Institute, Cambridge, England, for collaboration and Dr. Jos Jonkers for reviewing the manuscript. Willem Sloos, Leiden University Medical Centre, Leiden, The Netherlands for technical assistance. Prof. Gunnar Stefansson and Johanna Sigmundsdottir, Statistics Centre, University of Iceland, Reykjavik, Iceland, for assistance with statistical analysis. This work is funded by the University of Iceland Research Fund (ABJ), Soroptimist International of Europe (ABJ) and Gongum Saman (ABJ).",

year = "2010",

month = may,

day = "21",

doi = "10.1186/1471-2121-11-34",

language = "English",

volume = "11",

journal = "BMC Cell Biology",

issn = "1471-2121",

publisher = "BioMed Central Ltd.",

}

TY - JOUR

T1 - Centriole movements in mammalian epithelial cells during cytokinesis

AU - Jonsdottir, Asta B.

AU - Dirks, Roeland W.

AU - Vrolijk, Johannes

AU - Ögmundsdottir, Helga M.

AU - Tanke, Hans J.

AU - Eyfjörd, Jorunn E.

AU - Szuhai, Karoly

N1 - Funding Information: Prof. Michel Bornens, Institute Curie, Paris, France, for centrin1-EGFP expression construct and Dr. Matthieu Piel, Institute Curie, Paris, France for stable centrin1-EGFP HeLa cell line and their helpful discussion and comments during the preparation of this manuscript. We thank Dr. Jan Ellenberg, EMBL, Heidelberg, Germany and Prof. Roger Tsien, Howard Hughes Medical Institute, University of California, San Diego, USA, for providing expression constructs. Dr. Jos Jonkers and Dr. Bastiaan Evers, The Netherlands Cancer Institute, Amsterdam, The Netherlands and Dr. Fanni Gergely, Cancer Research UK Cambridge Research Institute, Cambridge, England, for collaboration and Dr. Jos Jonkers for reviewing the manuscript. Willem Sloos, Leiden University Medical Centre, Leiden, The Netherlands for technical assistance. Prof. Gunnar Stefansson and Johanna Sigmundsdottir, Statistics Centre, University of Iceland, Reykjavik, Iceland, for assistance with statistical analysis. This work is funded by the University of Iceland Research Fund (ABJ), Soroptimist International of Europe (ABJ) and Gongum Saman (ABJ).

PY - 2010/5/21

Y1 - 2010/5/21

N2 - Background: In cytokinesis, when the cleavage furrow has been formed, the two centrioles in each daughter cell separate. It has been suggested that the centrioles facilitate and regulate cytokinesis to some extent. It has been postulated that termination of cytokinesis (abscission) depends on the migration of a centriole to the intercellular bridge and then back to the cell center. To investigate the involvement of centrioles in cytokinesis, we monitored the movements of centrioles in three mammalian epithelial cell lines, HeLa, MCF 10A, and the p53-deficient mouse mammary tumor cell line KP-7.7, by time-lapse imaging. Centrin1-EGFP and α-Tubulin-mCherry were co-expressed in the cells to visualize respectively the centrioles and microtubules.Results: Here we report that separated centrioles that migrate from the cell pole are very mobile during cytokinesis and their movements can be characterized as 1) along the nuclear envelope, 2) irregular, and 3) along microtubules forming the spindle axis. Centriole movement towards the intercellular bridge was only seen occasionally and was highly cell-line dependent.Conclusions: These findings show that centrioles are highly mobile during cytokinesis and suggest that the repositioning of a centriole to the intercellular bridge is not essential for controlling abscission. We suggest that centriole movements are microtubule dependent and that abscission is more dependent on other mechanisms than positioning of centrioles.

AB - Background: In cytokinesis, when the cleavage furrow has been formed, the two centrioles in each daughter cell separate. It has been suggested that the centrioles facilitate and regulate cytokinesis to some extent. It has been postulated that termination of cytokinesis (abscission) depends on the migration of a centriole to the intercellular bridge and then back to the cell center. To investigate the involvement of centrioles in cytokinesis, we monitored the movements of centrioles in three mammalian epithelial cell lines, HeLa, MCF 10A, and the p53-deficient mouse mammary tumor cell line KP-7.7, by time-lapse imaging. Centrin1-EGFP and α-Tubulin-mCherry were co-expressed in the cells to visualize respectively the centrioles and microtubules.Results: Here we report that separated centrioles that migrate from the cell pole are very mobile during cytokinesis and their movements can be characterized as 1) along the nuclear envelope, 2) irregular, and 3) along microtubules forming the spindle axis. Centriole movement towards the intercellular bridge was only seen occasionally and was highly cell-line dependent.Conclusions: These findings show that centrioles are highly mobile during cytokinesis and suggest that the repositioning of a centriole to the intercellular bridge is not essential for controlling abscission. We suggest that centriole movements are microtubule dependent and that abscission is more dependent on other mechanisms than positioning of centrioles.

UR - https://www.scopus.com/pages/publications/77952453712

U2 - 10.1186/1471-2121-11-34

DO - 10.1186/1471-2121-11-34

M3 - Article

C2 - 20492670

SN - 1471-2121

VL - 11

JO - BMC Cell Biology

JF - BMC Cell Biology

M1 - 34

ER -

Centriole movements in mammalian epithelial cells during cytokinesis

Abstract

Bibliographical note

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