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

Volumn 110, Issue 40, 2013, Pages

  Pferdehirt, Rebecca R ^a,b   Meyer, Barbara J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b GENENTECH INC   (United States)

Author keywords

Chromatin; Epigenetics; Sexual dimorphism

Indexed keywords

CONDENSIN; SUMO PROTEIN;

ARTICLE; BINDING SITE; CAENORHABDITIS ELEGANS; CHROMOSOME SEGREGATION; CONTROLLED STUDY; GENE DELETION; GENE EXPRESSION REGULATION; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; SEX CHROMOSOME; SIGNAL TRANSDUCTION; SUMOYLATION;

CHROMATIN; EPIGENETICS; SEXUAL DIMORPHISM;

ADENOSINE TRIPHOSPHATASES; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CHROMATIN IMMUNOPRECIPITATION; DNA-BINDING PROTEINS; DOSAGE COMPENSATION, GENETIC; HERMAPHRODITIC ORGANISMS; MALE; MULTIPROTEIN COMPLEXES; PROTEIN ARRAY ANALYSIS; SEX CHARACTERISTICS; SUMOYLATION; X CHROMOSOME;

EID: 84884966441     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1315793110     Document Type: Article

References (36)

1. Conrad T, Akhtar A (2011) Dosage compensation in Drosophila melanogaster: Epigenetic fine-tuning of chromosome-wide transcription. Nat Rev Genet 13(2):123-134.
2. Meyer BJ (2010) Targeting X chromosomes for repression. Curr Opin Genet Dev 20(2): 179-189.
3. Disteche CM (2012) Dosage compensation of the sex chromosomes. Annu Rev Genet 46:537-560.
4. Gelbart ME, Kuroda MI (2009) Drosophila dosage compensation: A complex voyage to the X chromosome. Development 136(9):1399-1410.
5. Pferdehirt RR, Kruesi WS, Meyer BJ (2011) An MLL/COMPASS subunit functions in the C. elegans dosage compensation complex to target X chromosomes for transcriptional regulation of gene expression. Genes Dev 25(5):499-515.
6. Kruesi WS, Core LJ, Waters CT, Lis JT, Meyer BJ (2013) Condensin controls recruitment of RNA polymerase II to achieve nematode X-chromosome dosage compensation. eLife 2:e00808.
7. Deng X, et al. (2011) Evidence for compensatory upregulation of expressed X-linked genes in mammals, Caenorhabditis elegans and Drosophila melanogaster. Nat Genet 43(12):1179-1185.
8. Hirano T (2012) Condensins: Universal organizers of chromosomes with diverse functions. Genes Dev 26(15):1659-1678.
9. Chan RC, Severson AF, Meyer BJ (2004) Condensin restructures chromosomes in preparation for meiotic divisions. J Cell Biol 167(4):613-625.
10. Tsai CJ, et al. (2008) Meiotic crossover number and distribution are regulated by a dosage compensation protein that resembles a condensin subunit. Genes Dev 22(2):194-211.
11. Csankovszki G, et al. (2009) Three distinct condensin complexes control C. elegans chromosome dynamics. Curr Biol 19(1):9-19.
12. Mets DG, Meyer BJ (2009) Condensins regulate meiotic DNA break distribution, thus crossover frequency, by controlling chromosome structure. Cell 139(1):73-86.
13. Lieb JD, Albrecht MR, Chuang PT, Meyer BJ (1998) MIX-1: An essential component of the C. elegans mitotic machinery executes X chromosome dosage compensation. Cell 92(2):265-277.
14. Dawes HE, et al. (1999) Dosage compensation proteins targeted to X chromosomes by a determinant of hermaphrodite fate. Science 284(5421):1800-1804.
15. Nagy PL, Griesenbeck J, Kornberg RD, Cleary ML (2002) A trithorax-group complex purified from Saccharomyces cerevisiae is required for methylation of histone H3. Proc Natl Acad Sci USA 99(1):90-94.
16. McDonel P, Jans J, Peterson BK, Meyer BJ (2006) Clustered DNA motifs mark X chromosomes for repression by a dosage compensation complex. Nature 444(7119): 614-618.
17. Jans J, et al. (2009) A condensin-like dosage compensation complex acts at a distance to control expression throughout the genome. Genes Dev 23(5):602-618.
18. Ercan S, Dick LL, Lieb JD (2009) The C. elegans dosage compensation complex propagates dynamically and independently of X chromosome sequence. Curr Biol 19(21):1777-1787.
19. Lomelí H, Vázquez M (2011) Emerging roles of the SUMO pathway in development. Cell Mol Life Sci 68(24):4045-4064.
20. Gareau JR, Lima CD (2010) The SUMO pathway: Emerging mechanisms that shape specificity, conjugation and recognition. Nat Rev Mol Cell Biol 11(12):861-871.
21. Jones D, Crowe E, Stevens TA, Candido EP (2002) Functional and phylogenetic analysis of the ubiquitylation system in Caenorhabditis elegans: Ubiquitin-conjugating enzymes, ubiquitin-activating enzymes, and ubiquitin-like proteins. Genome Biol 3(1): RESEARCH0002.
22. Rodriguez MS, Dargemont C, Hay RT (2001) SUMO-1 conjugation in vivo requires both a consensus modification motif and nuclear targeting. J Biol Chem 276(16):12654-12659.
23. Song J, Durrin LK, Wilkinson TA, Krontiris TG, Chen Y (2004) Identification of a SUMObinding motif that recognizes SUMO-modified proteins. Proc Natl Acad Sci USA 101(40):14373-14378.
24. Hecker CM, RabillerM, Haglund K, Bayer P, Dikic I (2006) Specification of SUMO1-and SUMO2-interacting motifs. J Biol Chem 281(23):16117-16127.
25. Hickey CM, Wilson NR, Hochstrasser M (2012) Function and regulation of SUMO proteases. Nat Rev Mol Cell Biol 13(12):755-766.
26. Ouyang J, Gill G (2009) SUMO engages multiple corepressors to regulate chromatin structure and transcription. Epigenetics 4(7):440-444.
27. Johnson ES, Blobel G (1999) Cell cycle-regulated attachment of the ubiquitin-related protein SUMO to the yeast septins. J Cell Biol 147(5):981-994.
28. Dou H, Huang C, Van Nguyen T, Lu LS, Yeh ET (2011) SUMOylation and de-SUMOylation in response to DNA damage. FEBS Lett 585(18):2891-2896.
29. Psakhye I, Jentsch S (2012) Protein group modification and synergy in the SUMO pathway as exemplified in DNA repair. Cell 151(4):807-820.
30. Kaminsky R, et al. (2009) SUMO regulates the assembly and function of a cytoplasmic intermediate filament protein in C. elegans. Dev Cell 17(5):724-735.
31. D'Amours D, Amon A (2004) At the interface between signaling and executing anaphase-Cdc14 and the FEAR network. Genes Dev 18(21):2581-2595.
32. Zhang H, et al. (2004) SUMO modification is required for in vivo Hox gene regulation by the Caenorhabditis elegans Polycomb group protein SOP-2. Nat Genet 36(5): 507-511.
33. Huber P, et al. (2013) Function of the C. elegans T-box factor TBX-2 depends on SUMOylation. Cell Mol Life Sci, 10.1007/s00018-013-1336-y.
34. Poulin G, Dong Y, Fraser AG, Hopper NA, Ahringer J (2005) Chromatin regulation and sumoylation in the inhibition of Ras-induced vulval development in Caenorhabditis elegans. EMBO J 24(14):2613-2623.
35. Leight ER, Glossip D, Kornfeld K (2005) Sumoylation of LIN-1 promotes transcriptional repression and inhibition of vulval cell fates. Development 132(5):1047-1056.
36. Broday L, et al. (2004) The small ubiquitin-like modifier (SUMO) is required for gonadal and uterine-vulval morphogenesis in Caenorhabditis elegans. Genes Dev 18(19):2380-2391.