The Drosophila Melanogaster Condensin Subunit Cap-G Interacts with the Centromere-specific Histone H3 Variant CID

Overview

Journal Chromosoma

Specialty Molecular Biology

Date 2004 Dec 14

PMID 15592865

Citations 31

Authors

Hubert Jager

Melanie Rauch

Stefan Heidmann

Affiliations

Soon will be listed here.

Abstract

The centromere-specific histone H3 variant CENP-A plays a crucial role in kinetochore specification and assembly. We chose a genetic approach to identify interactors of the Drosophila CENP-A homolog CID. Overexpression of cid in the proliferating eye imaginal disk results in a rough eye phenotype, which is dependent on the ability of the overexpressed protein to localize to the kinetochore. A screen for modifiers of the rough eye phenotype identified mutations in the Drosophila condensin subunit gene Cap-G as interactors. Yeast two-hybrid experiments also reveal an interaction between CID and Cap-G. While chromosome condensation in Cap-G mutant embryos appears largely unaffected, massive defects in sister chromatid segregation occur during mitosis. Taken together, our results suggest a link between the chromatin condensation machinery and kinetochore structure.

Citing Articles

Centromere structure and function: lessons from Drosophila.

Kyriacou E, Heun P Genetics. 2023; 225(4).

PMID: 37931172 PMC: 10697814. DOI: 10.1093/genetics/iyad170.

Bivalent individualization during chromosome territory formation in Drosophila spermatocytes by controlled condensin II protein activity and additional force generators.

Vernizzi L, Lehner C PLoS Genet. 2021; 17(10):e1009870.

PMID: 34669718 PMC: 8559962. DOI: 10.1371/journal.pgen.1009870.

Condensin I is required for faithful meiosis in Drosophila males.

Kleinschnitz K, Viessmann N, Jordan M, Heidmann S Chromosoma. 2020; 129(2):141-160.

PMID: 32314039 PMC: 7260282. DOI: 10.1007/s00412-020-00733-w.

Condensin I subunit Cap-G is essential for proper gene expression during the maturation of post-mitotic neurons.

Hassan A, Araguas Rodriguez P, Heidmann S, Walmsley E, Aughey G, Southall T Elife. 2020; 9.

PMID: 32255428 PMC: 7170655. DOI: 10.7554/eLife.55159.

Multiple Functions of the Essential Gene in Early Development.

Liu B, Sung H, Grosshans J G3 (Bethesda). 2019; 9(11):3583-3593.

PMID: 31484673 PMC: 6829155. DOI: 10.1534/g3.119.400662.

References

Henikoff S, Ahmad K, Platero J, van Steensel B . Heterochromatic deposition of centromeric histone H3-like proteins. Proc Natl Acad Sci U S A. 2000; 97(2):716-21. PMC: 15396. DOI: 10.1073/pnas.97.2.716. View

Sullivan B, Blower M, Karpen G . Determining centromere identity: cyclical stories and forking paths. Nat Rev Genet. 2001; 2(8):584-96. DOI: 10.1038/35084512. View

Jager H, Herzig A, Lehner C, Heidmann S . Drosophila separase is required for sister chromatid separation and binds to PIM and THR. Genes Dev. 2001; 15(19):2572-84. PMC: 312799. DOI: 10.1101/gad.207301. View

Bhat M, Philp A, Glover D, Bellen H . Chromatid segregation at anaphase requires the barren product, a novel chromosome-associated protein that interacts with Topoisomerase II. Cell. 1996; 87(6):1103-14. DOI: 10.1016/s0092-8674(00)81804-8. View

Brand A, Perrimon N . Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development. 1993; 118(2):401-15. DOI: 10.1242/dev.118.2.401. View

Howman E, Fowler K, Newson A, Redward S, Macdonald A, Kalitsis P . Early disruption of centromeric chromatin organization in centromere protein A (Cenpa) null mice. Proc Natl Acad Sci U S A. 2000; 97(3):1148-53. PMC: 15551. DOI: 10.1073/pnas.97.3.1148. View

Rorth P . Gal4 in the Drosophila female germline. Mech Dev. 1998; 78(1-2):113-8. DOI: 10.1016/s0925-4773(98)00157-9. View

Oegema K, Desai A, Rybina S, Kirkham M, Hyman A . Functional analysis of kinetochore assembly in Caenorhabditis elegans. J Cell Biol. 2001; 153(6):1209-26. PMC: 2192036. DOI: 10.1083/jcb.153.6.1209. View

Coelho P, Queiroz-Machado J, Sunkel C . Condensin-dependent localisation of topoisomerase II to an axial chromosomal structure is required for sister chromatid resolution during mitosis. J Cell Sci. 2003; 116(Pt 23):4763-76. DOI: 10.1242/jcs.00799. View

10.

Andrade M, Perez-Iratxeta C, Ponting C . Protein repeats: structures, functions, and evolution. J Struct Biol. 2001; 134(2-3):117-31. DOI: 10.1006/jsbi.2001.4392. View

11.

Wignall S, Deehan R, Maresca T, Heald R . The condensin complex is required for proper spindle assembly and chromosome segregation in Xenopus egg extracts. J Cell Biol. 2003; 161(6):1041-51. PMC: 2172990. DOI: 10.1083/jcb.200303185. View

12.

Hirano T, Kobayashi R, Hirano M . Condensins, chromosome condensation protein complexes containing XCAP-C, XCAP-E and a Xenopus homolog of the Drosophila Barren protein. Cell. 1997; 89(4):511-21. DOI: 10.1016/s0092-8674(00)80233-0. View

13.

Evan G, LEWIS G, Ramsay G, Bishop J . Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product. Mol Cell Biol. 1985; 5(12):3610-6. PMC: 369192. DOI: 10.1128/mcb.5.12.3610-3616.1985. View

14.

Westermann S, Cheeseman I, Anderson S, Yates 3rd J, Drubin D, Barnes G . Architecture of the budding yeast kinetochore reveals a conserved molecular core. J Cell Biol. 2003; 163(2):215-22. PMC: 2173538. DOI: 10.1083/jcb.200305100. View

15.

Neuwald A, Hirano T . HEAT repeats associated with condensins, cohesins, and other complexes involved in chromosome-related functions. Genome Res. 2000; 10(10):1445-52. PMC: 310966. DOI: 10.1101/gr.147400. View

16.

Steffensen S, Coelho P, Cobbe N, Vass S, Costa M, Hassan B . A role for Drosophila SMC4 in the resolution of sister chromatids in mitosis. Curr Biol. 2001; 11(5):295-307. DOI: 10.1016/s0960-9822(01)00096-3. View

17.

Hudson D, Vagnarelli P, Gassmann R, Earnshaw W . Condensin is required for nonhistone protein assembly and structural integrity of vertebrate mitotic chromosomes. Dev Cell. 2003; 5(2):323-36. DOI: 10.1016/s1534-5807(03)00199-0. View

18.

Leismann O, Herzig A, Heidmann S, Lehner C . Degradation of Drosophila PIM regulates sister chromatid separation during mitosis. Genes Dev. 2000; 14(17):2192-205. PMC: 316890. DOI: 10.1101/gad.176700. View

19.

Swedlow J, Hirano T . The making of the mitotic chromosome: modern insights into classical questions. Mol Cell. 2003; 11(3):557-69. DOI: 10.1016/s1097-2765(03)00103-5. View

20.

Jacobs H, Richter D, Venkatesh T, Lehner C . Completion of mitosis requires neither fzr/rap nor fzr2, a male germline-specific Drosophila Cdh1 homolog. Curr Biol. 2002; 12(16):1435-41. DOI: 10.1016/s0960-9822(02)01074-6. View