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SUMOylation is essential for sex-specific assembly and function of the Caenorhabditis elegans dosage compensation complex on X chromosomes.
Proc Natl Acad Sci U S A 2013; 110(40):E3810-9PN

Abstract

The essential process of dosage compensation equalizes X-chromosome gene expression between Caenorhabditis elegans XO males and XX hermaphrodites through a dosage compensation complex (DCC) that is homologous to condensin. The DCC binds to both X chromosomes of hermaphrodites to repress transcription by half. Here, we show that posttranslational modification by the SUMO (small ubiquitin-like modifier) conjugation pathway is essential for sex-specific assembly and function of the DCC on X. Depletion of SUMO in vivo severely disrupts binding of particular DCC subunits and causes changes in X-linked gene expression similar to those caused by deleting genes encoding DCC subunits. Three DCC subunits are SUMOylated, and SUMO depletion preferentially reduces their binding to X, suggesting that SUMOylation of DCC subunits is essential for robust association with X. DCC SUMOylation is triggered by the signal that initiates DCC assembly onto X. The initial step of assembly-binding of X-targeting factors to recruitment sites on X-is independent of SUMOylation, but robust binding of the complete complex requires SUMOylation. SUMOylated DCC subunits are enriched at recruitment sites, and SUMOylation likely enhances interactions between X-targeting factors and condensin subunits that facilitate DCC binding beyond the low level achieved without SUMOylation. DCC subunits also participate in condensin complexes essential for chromosome segregation, but their SUMOylation occurs only in the context of the DCC. Our results reinforce a newly emerging theme in which multiple proteins of a complex are collectively SUMOylated in response to a specific stimulus, leading to accelerated complex formation and enhanced function.

Authors+Show Affiliations

Howard Hughes Medical Institute and Department of Molecular and Cell Biology, University of California, Berkeley, CA 94720-3204.No affiliation info available

Pub Type(s)

Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

24043781

Citation

Pferdehirt, Rebecca R., and Barbara J. Meyer. "SUMOylation Is Essential for Sex-specific Assembly and Function of the Caenorhabditis Elegans Dosage Compensation Complex On X Chromosomes." Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 40, 2013, pp. E3810-9.
Pferdehirt RR, Meyer BJ. SUMOylation is essential for sex-specific assembly and function of the Caenorhabditis elegans dosage compensation complex on X chromosomes. Proc Natl Acad Sci USA. 2013;110(40):E3810-9.
Pferdehirt, R. R., & Meyer, B. J. (2013). SUMOylation is essential for sex-specific assembly and function of the Caenorhabditis elegans dosage compensation complex on X chromosomes. Proceedings of the National Academy of Sciences of the United States of America, 110(40), pp. E3810-9. doi:10.1073/pnas.1315793110.
Pferdehirt RR, Meyer BJ. SUMOylation Is Essential for Sex-specific Assembly and Function of the Caenorhabditis Elegans Dosage Compensation Complex On X Chromosomes. Proc Natl Acad Sci USA. 2013 Oct 1;110(40):E3810-9. PubMed PMID: 24043781.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - SUMOylation is essential for sex-specific assembly and function of the Caenorhabditis elegans dosage compensation complex on X chromosomes. AU - Pferdehirt,Rebecca R, AU - Meyer,Barbara J, Y1 - 2013/09/16/ PY - 2013/9/18/entrez PY - 2013/9/18/pubmed PY - 2013/12/16/medline KW - chromatin KW - epigenetics KW - sexual dimorphism SP - E3810 EP - 9 JF - Proceedings of the National Academy of Sciences of the United States of America JO - Proc. Natl. Acad. Sci. U.S.A. VL - 110 IS - 40 N2 - The essential process of dosage compensation equalizes X-chromosome gene expression between Caenorhabditis elegans XO males and XX hermaphrodites through a dosage compensation complex (DCC) that is homologous to condensin. The DCC binds to both X chromosomes of hermaphrodites to repress transcription by half. Here, we show that posttranslational modification by the SUMO (small ubiquitin-like modifier) conjugation pathway is essential for sex-specific assembly and function of the DCC on X. Depletion of SUMO in vivo severely disrupts binding of particular DCC subunits and causes changes in X-linked gene expression similar to those caused by deleting genes encoding DCC subunits. Three DCC subunits are SUMOylated, and SUMO depletion preferentially reduces their binding to X, suggesting that SUMOylation of DCC subunits is essential for robust association with X. DCC SUMOylation is triggered by the signal that initiates DCC assembly onto X. The initial step of assembly-binding of X-targeting factors to recruitment sites on X-is independent of SUMOylation, but robust binding of the complete complex requires SUMOylation. SUMOylated DCC subunits are enriched at recruitment sites, and SUMOylation likely enhances interactions between X-targeting factors and condensin subunits that facilitate DCC binding beyond the low level achieved without SUMOylation. DCC subunits also participate in condensin complexes essential for chromosome segregation, but their SUMOylation occurs only in the context of the DCC. Our results reinforce a newly emerging theme in which multiple proteins of a complex are collectively SUMOylated in response to a specific stimulus, leading to accelerated complex formation and enhanced function. SN - 1091-6490 UR - https://www.unboundmedicine.com/medline/citation/24043781/SUMOylation_is_essential_for_sex_specific_assembly_and_function_of_the_Caenorhabditis_elegans_dosage_compensation_complex_on_X_chromosomes_ L2 - http://www.pnas.org/cgi/pmidlookup?view=long&pmid=24043781 DB - PRIME DP - Unbound Medicine ER -