Literature DB >> 22425160

A role for the centrosome and PAR-3 in the hand-off of MTOC function during epithelial polarization.

Jessica L Feldman1, James R Priess.   

Abstract

BACKGROUND: The centrosome is the major microtubule organizing center (MTOC) in dividing cells and in many postmitotic, differentiated cells. In other cell types, however, MTOC function is reassigned from the centrosome to noncentrosomal sites. Here, we analyze how MTOC function is reassigned to the apical membrane of C. elegans intestinal cells.
RESULTS: After the terminal intestinal cell division, the centrosomes and nuclei move near the future apical membranes, and the postmitotic centrosomes lose all, or nearly all, of their associated microtubules. We show that microtubule-nucleating proteins such as γ-tubulin and CeGrip-1 that are centrosome components in dividing cells become localized to the apical membrane, which becomes highly enriched in microtubules. Our results suggest that centrosomes are critical to specify the apical membrane as the new MTOC. First, γ-tubulin appears to redistribute directly from the migrating centrosome onto the lateral then apical membrane. Second, γ-tubulin fails to accumulate apically in wild-type cells following laser ablation of the centrosome. We show that centrosomes localize apically by first moving toward lateral foci of the conserved polarity proteins PAR-3 and PAR-6 and then move together with these foci toward the future apical surface. Embryos lacking PAR-3 fail to localize their centrosomes apically and have aberrant localization of γ-tubulin and CeGrip-1.
CONCLUSIONS: These data suggest that PAR proteins contribute to apical polarity in part by determining centrosome position and that the reassignment of MTOC function from centrosomes to the apical membrane is associated with a physical hand-off of nucleators of microtubule assembly.
Copyright © 2012 Elsevier Ltd. All rights reserved.

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Year:  2012        PMID: 22425160      PMCID: PMC3409831          DOI: 10.1016/j.cub.2012.02.044

Source DB:  PubMed          Journal:  Curr Biol        ISSN: 0960-9822            Impact factor:   10.834


  33 in total

1.  Organogenesis of the Caenorhabditis elegans intestine.

Authors:  B Leung; G J Hermann; J R Priess
Journal:  Dev Biol       Date:  1999-12-01       Impact factor: 3.582

2.  The aPKC-PAR-6-PAR-3 cell polarity complex localizes to the centrosome attracting body, a macroscopic cortical structure responsible for asymmetric divisions in the early ascidian embryo.

Authors:  Solenn Patalano; Gérard Prulière; François Prodon; Alexandre Paix; Philippe Dru; Christian Sardet; Janet Chenevert
Journal:  J Cell Sci       Date:  2006-03-28       Impact factor: 5.285

Review 3.  Generation of noncentrosomal microtubule arrays.

Authors:  Francesca Bartolini; Gregg G Gundersen
Journal:  J Cell Sci       Date:  2006-10-15       Impact factor: 5.285

4.  Shroom family proteins regulate gamma-tubulin distribution and microtubule architecture during epithelial cell shape change.

Authors:  Chanjae Lee; Heather M Scherr; John B Wallingford
Journal:  Development       Date:  2007-02-28       Impact factor: 6.868

5.  Centrosome maturation and mitotic spindle assembly in C. elegans require SPD-5, a protein with multiple coiled-coil domains.

Authors:  Danielle R Hamill; Aaron F Severson; J Clayton Carter; Bruce Bowerman
Journal:  Dev Cell       Date:  2002-11       Impact factor: 12.270

6.  PAR-6 is required for junction formation but not apicobasal polarization in C. elegans embryonic epithelial cells.

Authors:  Ronald Totong; Annita Achilleos; Jeremy Nance
Journal:  Development       Date:  2007-02-21       Impact factor: 6.868

7.  unc-83 encodes a novel component of the nuclear envelope and is essential for proper nuclear migration.

Authors:  D A Starr; G J Hermann; C J Malone; W Fixsen; J R Priess; H R Horvitz; M Han
Journal:  Development       Date:  2001-12       Impact factor: 6.868

8.  Identification and characterization of Caenorhabditis elegans gamma-tubulin in dividing cells and differentiated tissues.

Authors:  Y Bobinnec; M Fukuda; E Nishida
Journal:  J Cell Sci       Date:  2000-11       Impact factor: 5.285

9.  The kinetically dominant assembly pathway for centrosomal asters in Caenorhabditis elegans is gamma-tubulin dependent.

Authors:  Eva Hannak; Karen Oegema; Matthew Kirkham; Pierre Gönczy; Bianca Habermann; Anthony A Hyman
Journal:  J Cell Biol       Date:  2002-05-13       Impact factor: 10.539

10.  Aurora-A kinase is required for centrosome maturation in Caenorhabditis elegans.

Authors:  E Hannak; M Kirkham; A A Hyman; K Oegema
Journal:  J Cell Biol       Date:  2001-12-17       Impact factor: 10.539

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  60 in total

Review 1.  Centrosome function and assembly in animal cells.

Authors:  Paul T Conduit; Alan Wainman; Jordan W Raff
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2.  Flipping the switch: regulating MTOC location.

Authors:  Maria D Sallee; Jessica L Feldman
Journal:  Cell Cycle       Date:  2015       Impact factor: 4.534

Review 3.  Golgi as an MTOC: making microtubules for its own good.

Authors:  Xiaodong Zhu; Irina Kaverina
Journal:  Histochem Cell Biol       Date:  2013-07-03       Impact factor: 4.304

4.  Network analysis in aged C. elegans reveals candidate regulatory genes of ageing.

Authors:  Foteini Aktypi; Nikoletta Papaevgeniou; Konstantinos Voutetakis; Aristotelis Chatziioannou; Tilman Grune; Niki Chondrogianni
Journal:  Biogerontology       Date:  2021-04-19       Impact factor: 4.277

5.  A toolkit for GFP-mediated tissue-specific protein degradation in C. elegans.

Authors:  Shaohe Wang; Ngang Heok Tang; Pablo Lara-Gonzalez; Zhiling Zhao; Dhanya K Cheerambathur; Bram Prevo; Andrew D Chisholm; Arshad Desai; Karen Oegema
Journal:  Development       Date:  2017-06-15       Impact factor: 6.868

6.  Nuclei migrate through constricted spaces using microtubule motors and actin networks in C. elegans hypodermal cells.

Authors:  Courtney R Bone; Yu-Tai Chang; Natalie E Cain; Shaun P Murphy; Daniel A Starr
Journal:  Development       Date:  2016-10-03       Impact factor: 6.868

Review 7.  Centrosome positioning in vertebrate development.

Authors:  Nan Tang; Wallace F Marshall
Journal:  J Cell Sci       Date:  2012-11-01       Impact factor: 5.285

Review 8.  Microtubule-organizing centers: from the centrosome to non-centrosomal sites.

Authors:  Ariana D Sanchez; Jessica L Feldman
Journal:  Curr Opin Cell Biol       Date:  2016-09-22       Impact factor: 8.382

Review 9.  Centrosomes are multifunctional regulators of genome stability.

Authors:  Dorothy A Lerit; John S Poulton
Journal:  Chromosome Res       Date:  2016-01       Impact factor: 5.239

Review 10.  Oocyte Meiotic Spindle Assembly and Function.

Authors:  Aaron F Severson; George von Dassow; Bruce Bowerman
Journal:  Curr Top Dev Biol       Date:  2016-01-23       Impact factor: 4.897

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