Home LiteratureArticle Details
PMID: 16824953 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

INCENP and Aurora B promote meiotic sister chromatid cohesion through localization of the Shugoshin MEI-S332 in Drosophila.

Developmental cell ·Vol. 11 ·No. 1 ·2006-07-00 ·Pages 57-68

Resnick TD, Satinover DL, MacIsaac F, Stukenberg PT, Earnshaw WC, Orr-Weaver TL, Carmena M

Abstract

The chromosomal passenger complex protein INCENP is required in mitosis for chromosome condensation, spindle attachment and function, and cytokinesis. Here, we show that INCENP has an essential function in the specialized behavior of centromeres in meiosis. Mutations affecting Drosophila incenp profoundly affect chromosome segregation in both meiosis I and II, due, at least in part, to premature sister chromatid separation in meiosis I. INCENP binds to the cohesion protector protein MEI-S332, which is also an excellent in vitro substrate for Aurora B kinase. A MEI-S332 mutant that is only poorly phosphorylated by Aurora B is defective in localization to centromeres. These results implicate the chromosomal passenger complex in directly regulating MEI-S332 localization and, therefore, the control of sister chromatid cohesion in meiosis.

MeSH Terms
Animals Aurora Kinases Cell Cycle Proteins/genetics,metabolism Centromere/genetics,metabolism Chromatids/genetics,metabolism Chromosomal Proteins, Non-Histone/genetics,metabolism Drosophila Proteins/genetics,metabolism Drosophila melanogaster/genetics,metabolism Female Genes, Insect In Vitro Techniques Infertility, Female/genetics Male Meiosis Mitosis Models, Biological Mutation Phenotype Phosphorylation Protein Serine-Threonine Kinases/metabolism Substrate Specificity
Chemicals
Cell Cycle Proteins Chromosomal Proteins, Non-Histone Drosophila Proteins mei-S332 protein, Drosophila Aurora Kinases Protein Serine-Threonine Kinases
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Resnick Tamar D
Whitehead Institute and Department of Biology, Massachusetts Institute of Technology, Nine Cambridge Center, Cambridge, Massachusetts 02142, USA.
Satinover David L
MacIsaac Fiona
Stukenberg P Todd
Earnshaw William C
Orr-Weaver Terry L
Carmena Mar
References (61)
61 references, click to expand
  1. The inner centromere protein (INCENP) antigens: movement from inner centromere to midbody during mitosis.
    J Cell Biol. 1987 Nov;105(5):2053-67 PMID: 3316246
  2. Regulation of HP1-chromatin binding by histone H3 methylation and phosphorylation.
    Nature. 2005 Dec 22;438(7071):1116-22 PMID: 16222246
  3. Exploring the functional interactions between Aurora B, INCENP, and survivin in mitosis.
    Mol Biol Cell. 2003 Aug;14(8):3325-41 PMID: 12925766
  4. Borealin: a novel chromosomal passenger required for stability of the bipolar mitotic spindle.
    J Cell Biol. 2004 Jul 19;166(2):179-91 PMID: 15249581
  5. Two fission yeast homologs of Drosophila Mei-S332 are required for chromosome segregation during meiosis I and II.
    Curr Biol. 2004 Feb 17;14(4):287-301 PMID: 14972679
  6. Survivin is required for stable checkpoint activation in taxol-treated HeLa cells.
    J Cell Sci. 2003 Jul 15;116(Pt 14):2987-98 PMID: 12783991
  7. Maintenance of cohesin at centromeres after meiosis I in budding yeast requires a kinetochore-associated protein related to MEI-S332.
    Curr Biol. 2004 Apr 6;14(7):560-72 PMID: 15062096
  8. The Synaptonemal complex component C(2)M regulates meiotic crossing over in Drosophila.
    Curr Biol. 2003 Feb 18;13(4):276-85 PMID: 12593793
  9. Female sterile mutations on the second chromosome of Drosophila melanogaster. I. Maternal effect mutations.
    Genetics. 1989 Jan;121(1):101-17 PMID: 2492966
  10. The cellular geography of aurora kinases.
    Nat Rev Mol Cell Biol. 2003 Nov;4(11):842-54 PMID: 14625535
  11. POLO kinase regulates the Drosophila centromere cohesion protein MEI-S332.
    Dev Cell. 2005 Jan;8(1):53-64 PMID: 15621529
  12. Survivin and the inner centromere protein INCENP show similar cell-cycle localization and gene knockout phenotype.
    Curr Biol. 2000 Nov 2;10(21):1319-28 PMID: 11084331
  13. Control of centromere localization of the MEI-S332 cohesion protection protein.
    Curr Biol. 2004 Jul 27;14(14):1277-83 PMID: 15268859
  14. Sister-chromatid cohesion via MEI-S332 and kinetochore assembly are separable functions of the Drosophila centromere.
    Curr Biol. 2000 Aug 24;10(16):997-1000 PMID: 10985388
  15. The role of Drosophila CID in kinetochore formation, cell-cycle progression and heterochromatin interactions.
    Nat Cell Biol. 2001 Aug;3(8):730-9 PMID: 11483958
  16. A genome-wide screen identifies genes required for centromeric cohesion.
    Science. 2004 Feb 27;303(5662):1367-70 PMID: 14752166
  17. Human survivin is a kinetochore-associated passenger protein.
    J Cell Biol. 2000 Dec 25;151(7):1575-82 PMID: 11134084
  18. Juxtaposition of C(2)M and the transverse filament protein C(3)G within the central region of Drosophila synaptonemal complex.
    Proc Natl Acad Sci U S A. 2005 Mar 22;102(12):4482-7 PMID: 15767569
  19. Regulation of sister chromatid cohesion between chromosome arms.
    Curr Biol. 2004 Jul 13;14(13):1187-93 PMID: 15242616
  20. Drosophila Incenp is required for cytokinesis and asymmetric cell division during development of the nervous system.
    J Cell Sci. 2006 Mar 15;119(Pt 6):1144-53 PMID: 16507586
  21. The aurora B kinase AIR-2 regulates kinetochores during mitosis and is required for separation of homologous Chromosomes during meiosis.
    Curr Biol. 2002 May 14;12(10):798-812 PMID: 12015116
  22. Mei-S332, a Drosophila protein required for sister-chromatid cohesion, can localize to meiotic centromere regions.
    Cell. 1995 Oct 20;83(2):247-56 PMID: 7585942
  23. Mapping of Drosophila mutations using site-specific male recombination.
    Genetics. 1998 May;149(1):157-63 PMID: 9584093
  24. Disjunction of homologous chromosomes in meiosis I depends on proteolytic cleavage of the meiotic cohesin Rec8 by separin.
    Cell. 2000 Oct 27;103(3):387-98 PMID: 11081626
  25. Dynamic relocalization of the chromosomal passenger complex proteins inner centromere protein (INCENP) and aurora-B kinase during male mouse meiosis.
    J Cell Sci. 2003 Mar 15;116(Pt 6):961-74 PMID: 12584241
  26. The mitotic centromeric protein MEI-S332 and its role in sister-chromatid cohesion.
    Chromosoma. 1999 Dec;108(7):401-11 PMID: 10654079
  27. Human INCENP colocalizes with the Aurora-B/AIRK2 kinase on chromosomes and is overexpressed in tumour cells.
    Chromosoma. 2001 May;110(2):65-74 PMID: 11453556
  28. AIM-1: a mammalian midbody-associated protein required for cytokinesis.
    EMBO J. 1998 Feb 2;17(3):667-76 PMID: 9450992
  29. A modular misexpression screen in Drosophila detecting tissue-specific phenotypes.
    Proc Natl Acad Sci U S A. 1996 Oct 29;93(22):12418-22 PMID: 8901596
  30. Sister-chromatid misbehavior in Drosophila ord mutants.
    Genetics. 1992 Dec;132(4):1047-61 PMID: 1459426
  31. Phosphorylation of the carboxyl terminus of inner centromere protein (INCENP) by the Aurora B Kinase stimulates Aurora B kinase activity.
    J Biol Chem. 2002 Aug 2;277(31):27577-80 PMID: 12048181
  32. Maintenance of sister-chromatid cohesion at the centromere by the Drosophila MEI-S332 protein.
    Genes Dev. 1998 Dec 15;12(24):3843-56 PMID: 9869638
  33. pavarotti encodes a kinesin-like protein required to organize the central spindle and contractile ring for cytokinesis.
    Genes Dev. 1998 May 15;12(10):1483-94 PMID: 9585508
  34. Roles and regulation of the Drosophila centromere cohesion protein MEI-S332 family.
    Philos Trans R Soc Lond B Biol Sci. 2005 Mar 29;360(1455):543-52 PMID: 15915585
  35. Recruitment of cohesin to heterochromatic regions by Swi6/HP1 in fission yeast.
    Nat Cell Biol. 2002 Jan;4(1):89-93 PMID: 11780129
  36. ISWI remodeling complexes in Xenopus egg extracts: identification as major chromosomal components that are regulated by INCENP-aurora B.
    Mol Biol Cell. 2002 Jan;13(1):25-39 PMID: 11809820
  37. Complex formation of Plk1 and INCENP required for metaphase-anaphase transition.
    Nat Cell Biol. 2006 Feb;8(2):180-7 PMID: 16378098
  38. AIR-2: An Aurora/Ipl1-related protein kinase associated with chromosomes and midbody microtubules is required for polar body extrusion and cytokinesis in Caenorhabditis elegans embryos.
    J Cell Biol. 1998 Dec 14;143(6):1635-46 PMID: 9852156
  39. Homologous pairing and chromosome dynamics in meiosis and mitosis.
    Biochim Biophys Acta. 2004 Mar 15;1677(1-3):165-80 PMID: 15020057
  40. The aurora kinase AIR-2 functions in the release of chromosome cohesion in Caenorhabditis elegans meiosis.
    J Cell Biol. 2002 Apr 15;157(2):219-29 PMID: 11940606
  41. Shugoshin prevents dissociation of cohesin from centromeres during mitosis in vertebrate cells.
    PLoS Biol. 2005 Mar;3(3):e86 PMID: 15737064
  42. INCENP centromere and spindle targeting: identification of essential conserved motifs and involvement of heterochromatin protein HP1.
    J Cell Biol. 1998 Dec 28;143(7):1763-74 PMID: 9864353
  43. Histone H3 serine 10 phosphorylation by Aurora B causes HP1 dissociation from heterochromatin.
    Nature. 2005 Dec 22;438(7071):1176-80 PMID: 16222244
  44. Separase regulates INCENP-Aurora B anaphase spindle function through Cdc14.
    Science. 2003 Dec 19;302(5653):2120-4 PMID: 14605209
  45. The Drosophila meiotic kleisin C(2)M functions before the meiotic divisions.
    Chromosoma. 2004 Oct;113(4):177-87 PMID: 15375666
  46. INCENP binds the Aurora-related kinase AIRK2 and is required to target it to chromosomes, the central spindle and cleavage furrow.
    Curr Biol. 2000 Sep 7;10(17):1075-8 PMID: 10996078
  47. Drosophila aurora B kinase is required for histone H3 phosphorylation and condensin recruitment during chromosome condensation and to organize the central spindle during cytokinesis.
    J Cell Biol. 2001 Feb 19;152(4):669-82 PMID: 11266459
  48. Meiosis in Drosophila melanogaster. IV. The conjunctive mechanism of the XY bivalent.
    Chromosoma. 1982;86(3):309-17 PMID: 6816529
  49. Requirement of heterochromatin for cohesion at centromeres.
    Science. 2001 Dec 21;294(5551):2539-42 PMID: 11598266
  50. Un ménage à quatre: the molecular biology of chromosome segregation in meiosis.
    Cell. 2003 Feb 21;112(4):423-40 PMID: 12600308
  51. The chromosomal passenger complex is required for chromatin-induced microtubule stabilization and spindle assembly.
    Cell. 2004 Jul 23;118(2):187-202 PMID: 15260989
  52. An overexpression screen in Drosophila for genes that restrict growth or cell-cycle progression in the developing eye.
    Genetics. 2002 Sep;162(1):229-43 PMID: 12242236
  53. Genetic interactions between mei-S332 and ord in the control of sister-chromatid cohesion.
    Genetics. 1998 Dec;150(4):1467-76 PMID: 9832524
  54. Cohesin release is required for sister chromatid resolution, but not for condensin-mediated compaction, at the onset of mitosis.
    Genes Dev. 2002 Dec 1;16(23):3004-16 PMID: 12464631
  55. Functional cooperation of Dam1, Ipl1, and the inner centromere protein (INCENP)-related protein Sli15 during chromosome segregation.
    J Cell Biol. 2001 Nov 26;155(5):763-74 PMID: 11724818
  56. The conserved kinetochore protein shugoshin protects centromeric cohesion during meiosis.
    Nature. 2004 Feb 5;427(6974):510-7 PMID: 14730319
  57. Pericentric heterochromatin becomes enriched with H2A.Z during early mammalian development.
    EMBO J. 2003 Apr 1;22(7):1599-607 PMID: 12660166
  58. Cleavage of cohesin by the CD clan protease separin triggers anaphase in yeast.
    Cell. 2000 Oct 27;103(3):375-86 PMID: 11081625
  59. INCENP binds directly to tubulin and requires dynamic microtubules to target to the cleavage furrow.
    Exp Cell Res. 2001 Jan 15;262(2):122-7 PMID: 11139336
  60. Essential roles of Drosophila inner centromere protein (INCENP) and aurora B in histone H3 phosphorylation, metaphase chromosome alignment, kinetochore disjunction, and chromosome segregation.
    J Cell Biol. 2001 May 14;153(4):865-80 PMID: 11352945
  61. Chromosomal passengers: the four-dimensional regulation of mitotic events.
    Chromosoma. 2004 Nov;113(5):211-22 PMID: 15351889
Article Info
Journal
Developmental cell
Abbr.
Dev Cell
ISSN
1534-5807
DOI
10.1016/j.devcel.2006.04.021
Published
2006-07-00
Pages
57-68
Language
English
Region
United States
NLM ID
101120028
PMCID
PMC7115953
Subset
IM
Grants
Wellcome Trust · 043189 · United Kingdom
NIGMS NIH HHS · R01 GM039341 · United States
NICHD NIH HHS · HD07528 · United States
NICHD NIH HHS · T32 HD007528 · United States
NIGMS NIH HHS · R01 GM063045 · United States
NIGMS NIH HHS · GM39341 · United States
NIGMS NIH HHS · GM63045 · United States
Wellcome Trust · United Kingdom
Wellcome Trust · 073915 · United Kingdom
External Links
PubMed source DOI: 10.1016/j.devcel.2006.04.021 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2