The aurora kinase AIR-2 functions in the release of chromosome cohesion in Caenorhabditis elegans meiosis

Eric Rogers, John D. Bishop, James A. Waddle, Jill M. Schumacher, Rueyling Lin

Research output: Contribution to journalArticle

144 Citations (Scopus)

Abstract

Accurate chromosome segregation during cell division requires not only the establishment, but also the precise, regulated release of chromosome cohesion. Chromosome dynamics during meiosis are more complicated, because homologues separate at anaphase I whereas sister chromatids remain attached until anaphase II. How the selective release of chromosome cohesion is regulated during meiosis remains unclear. We show that the aurora-B kinase AIR-2 regulates the selective release of chromosome cohesion during Caenorhabditis elegans meiosis. AIR-2 localizes to subchromosomal regions corresponding to last points of contact between homologues in metaphase I and between sister chromatids in metaphase II. Depletion of AIR-2 by RNA interference (RNAi) prevents chromosome separation at both anaphases, with concomitant prevention of meiotic cohesin REC-8 release from meiotic chromosomes. We show that AIR-2 phosphorylates REC-8 at a major amino acid in vitro. Interestingly, depletion of two PP1 phosphatases, CeGLC-7α and CeGLC-7β, abolishes the restricted localization pattern of AIR-2. In Ceglc-7α/β(RNAi) embryos, AIR-2 is detected on the entire bivalent. Concurrently, chromosomal REC-8 is dramatically reduced and sister chromatids are separated precociously at anaphase I in Ceglc-7α/β(RNAi) embryos. We propose that AIR-2 promotes the release of chromosome cohesion via phosphorylation of REC-8 at specific chromosomal locations and that CeGLC-7α/β, directly or indirectly, antagonize AIR-2 activity.

Original languageEnglish (US)
Pages (from-to)219-229
Number of pages11
JournalJournal of Cell Biology
Volume157
Issue number2
DOIs
StatePublished - Apr 15 2002

Fingerprint

Aurora Kinases
Caenorhabditis elegans
Meiosis
Chromosomes
Anaphase
Chromatids
RNA Interference
Metaphase
Embryonic Structures
Aurora Kinase B
Chromosome Segregation
Phosphoric Monoester Hydrolases
Cell Division
Phosphorylation
Amino Acids

Keywords

  • AIR-2
  • Aurora-B
  • C. elegans
  • Cohesion
  • Meiosis

ASJC Scopus subject areas

  • Cell Biology

Cite this

The aurora kinase AIR-2 functions in the release of chromosome cohesion in Caenorhabditis elegans meiosis. / Rogers, Eric; Bishop, John D.; Waddle, James A.; Schumacher, Jill M.; Lin, Rueyling.

In: Journal of Cell Biology, Vol. 157, No. 2, 15.04.2002, p. 219-229.

Research output: Contribution to journalArticle

Rogers, Eric ; Bishop, John D. ; Waddle, James A. ; Schumacher, Jill M. ; Lin, Rueyling. / The aurora kinase AIR-2 functions in the release of chromosome cohesion in Caenorhabditis elegans meiosis. In: Journal of Cell Biology. 2002 ; Vol. 157, No. 2. pp. 219-229.
@article{5af84fd3e47a45d882c06f19ee6c55f5,
title = "The aurora kinase AIR-2 functions in the release of chromosome cohesion in Caenorhabditis elegans meiosis",
abstract = "Accurate chromosome segregation during cell division requires not only the establishment, but also the precise, regulated release of chromosome cohesion. Chromosome dynamics during meiosis are more complicated, because homologues separate at anaphase I whereas sister chromatids remain attached until anaphase II. How the selective release of chromosome cohesion is regulated during meiosis remains unclear. We show that the aurora-B kinase AIR-2 regulates the selective release of chromosome cohesion during Caenorhabditis elegans meiosis. AIR-2 localizes to subchromosomal regions corresponding to last points of contact between homologues in metaphase I and between sister chromatids in metaphase II. Depletion of AIR-2 by RNA interference (RNAi) prevents chromosome separation at both anaphases, with concomitant prevention of meiotic cohesin REC-8 release from meiotic chromosomes. We show that AIR-2 phosphorylates REC-8 at a major amino acid in vitro. Interestingly, depletion of two PP1 phosphatases, CeGLC-7α and CeGLC-7β, abolishes the restricted localization pattern of AIR-2. In Ceglc-7α/β(RNAi) embryos, AIR-2 is detected on the entire bivalent. Concurrently, chromosomal REC-8 is dramatically reduced and sister chromatids are separated precociously at anaphase I in Ceglc-7α/β(RNAi) embryos. We propose that AIR-2 promotes the release of chromosome cohesion via phosphorylation of REC-8 at specific chromosomal locations and that CeGLC-7α/β, directly or indirectly, antagonize AIR-2 activity.",
keywords = "AIR-2, Aurora-B, C. elegans, Cohesion, Meiosis",
author = "Eric Rogers and Bishop, {John D.} and Waddle, {James A.} and Schumacher, {Jill M.} and Rueyling Lin",
year = "2002",
month = "4",
day = "15",
doi = "10.1083/jcb.200110045",
language = "English (US)",
volume = "157",
pages = "219--229",
journal = "Journal of Cell Biology",
issn = "0021-9525",
publisher = "Rockefeller University Press",
number = "2",

}

TY - JOUR

T1 - The aurora kinase AIR-2 functions in the release of chromosome cohesion in Caenorhabditis elegans meiosis

AU - Rogers, Eric

AU - Bishop, John D.

AU - Waddle, James A.

AU - Schumacher, Jill M.

AU - Lin, Rueyling

PY - 2002/4/15

Y1 - 2002/4/15

N2 - Accurate chromosome segregation during cell division requires not only the establishment, but also the precise, regulated release of chromosome cohesion. Chromosome dynamics during meiosis are more complicated, because homologues separate at anaphase I whereas sister chromatids remain attached until anaphase II. How the selective release of chromosome cohesion is regulated during meiosis remains unclear. We show that the aurora-B kinase AIR-2 regulates the selective release of chromosome cohesion during Caenorhabditis elegans meiosis. AIR-2 localizes to subchromosomal regions corresponding to last points of contact between homologues in metaphase I and between sister chromatids in metaphase II. Depletion of AIR-2 by RNA interference (RNAi) prevents chromosome separation at both anaphases, with concomitant prevention of meiotic cohesin REC-8 release from meiotic chromosomes. We show that AIR-2 phosphorylates REC-8 at a major amino acid in vitro. Interestingly, depletion of two PP1 phosphatases, CeGLC-7α and CeGLC-7β, abolishes the restricted localization pattern of AIR-2. In Ceglc-7α/β(RNAi) embryos, AIR-2 is detected on the entire bivalent. Concurrently, chromosomal REC-8 is dramatically reduced and sister chromatids are separated precociously at anaphase I in Ceglc-7α/β(RNAi) embryos. We propose that AIR-2 promotes the release of chromosome cohesion via phosphorylation of REC-8 at specific chromosomal locations and that CeGLC-7α/β, directly or indirectly, antagonize AIR-2 activity.

AB - Accurate chromosome segregation during cell division requires not only the establishment, but also the precise, regulated release of chromosome cohesion. Chromosome dynamics during meiosis are more complicated, because homologues separate at anaphase I whereas sister chromatids remain attached until anaphase II. How the selective release of chromosome cohesion is regulated during meiosis remains unclear. We show that the aurora-B kinase AIR-2 regulates the selective release of chromosome cohesion during Caenorhabditis elegans meiosis. AIR-2 localizes to subchromosomal regions corresponding to last points of contact between homologues in metaphase I and between sister chromatids in metaphase II. Depletion of AIR-2 by RNA interference (RNAi) prevents chromosome separation at both anaphases, with concomitant prevention of meiotic cohesin REC-8 release from meiotic chromosomes. We show that AIR-2 phosphorylates REC-8 at a major amino acid in vitro. Interestingly, depletion of two PP1 phosphatases, CeGLC-7α and CeGLC-7β, abolishes the restricted localization pattern of AIR-2. In Ceglc-7α/β(RNAi) embryos, AIR-2 is detected on the entire bivalent. Concurrently, chromosomal REC-8 is dramatically reduced and sister chromatids are separated precociously at anaphase I in Ceglc-7α/β(RNAi) embryos. We propose that AIR-2 promotes the release of chromosome cohesion via phosphorylation of REC-8 at specific chromosomal locations and that CeGLC-7α/β, directly or indirectly, antagonize AIR-2 activity.

KW - AIR-2

KW - Aurora-B

KW - C. elegans

KW - Cohesion

KW - Meiosis

UR - http://www.scopus.com/inward/record.url?scp=0037092044&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0037092044&partnerID=8YFLogxK

U2 - 10.1083/jcb.200110045

DO - 10.1083/jcb.200110045

M3 - Article

VL - 157

SP - 219

EP - 229

JO - Journal of Cell Biology

JF - Journal of Cell Biology

SN - 0021-9525

IS - 2

ER -