The C. elegans H3K27 demethylase UTX-1 is essential for normal development, independent of its enzymatic activity

PLoS Genetics

Volumn 8, Issue 5, 2012, Pages

  Vandamme, Julien ^a,b   Lettier, Gaëlle ^a   Sidoli, Simone ^c   Di Schiavi, Elia ^d   Nørregaard Jensen, Ole ^c   Salcini, Anna Elisabetta ^a,b  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^d INSTITUTE OF GENETICS AND BIOPHYSICS ADRIANO BUZZATI TRAVERSO   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE DEMETHYLASE; MIXED LINEAGE LEUKEMIA PROTEIN; CAENORHABDITIS ELEGANS PROTEIN; HISTONE; UTX 1 PROTEIN, C ELEGANS; UTX-1 PROTEIN, C ELEGANS;

ARTICLE; BIOCATALYSIS; BIOCHEMICAL COMPOSITION; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; DEVELOPMENTAL GENE; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; GENE; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE IDENTIFICATION; GENE LOSS; GENE SILENCING; GENETIC VARIABILITY; HISTONE METHYLATION; NONHUMAN; PROTEIN FUNCTION; SEQUENCE HOMOLOGY; SET 16 GENE; UTX 1 GENE; ANIMAL; CELL DIFFERENTIATION; FERTILITY; GENETIC EPIGENESIS; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; METHYLATION; RNA INTERFERENCE;

CAENORHABDITIS ELEGANS; MAMMALIA;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL DIFFERENTIATION; EMBRYONIC DEVELOPMENT; EPIGENESIS, GENETIC; FERTILITY; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HISTONE DEMETHYLASES; HISTONES; JUMONJI DOMAIN-CONTAINING HISTONE DEMETHYLASES; METHYLATION; RNA INTERFERENCE;

EID: 84863671360     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002647     Document Type: Article

References (48)

1. Strahl BD, Allis CD, (2000) The language of covalent histone modifications. Nature 403: 41-45.
2. Kouzarides T, (2007) Chromatin modifications and their function. Cell 128: 693-705.
3. Berger SL, (2007) The complex language of chromatin regulation during transcription. Nature 447: 407-412.
4. Tsukada Y, Fang J, Erdjument-Bromage H, Warren ME, Borchers CH, et al. (2006) Histone demethylation by a family of JmjC domain-containing proteins. Nature 439: 811-816.
5. Cloos PA, Christensen J, Agger K, Helin K, (2008) Erasing the methyl mark: histone demethylases at the center of cellular differentiation and disease. Genes Dev 22: 1115-1140.
6. Agger K, Cloos PA, Christensen J, Pasini D, Rose S, et al. (2007) UTX and JMJD3 are histone H3K27 demethylases involved in HOX gene regulation and development. Nature 449: 731-734.
7. Lee MG, Villa R, Trojer P, Norman J, Yan KP, et al. (2007) Demethylation of H3K27 Regulates Polycomb Recruitment and H2A Ubiquitination. Science 318: 447-450.
8. Smith ER, Lee MG, Winter B, Droz NM, Eissenberg JC, et al. (2007) Drosophila UTX is a histone H3 Lys27 demethylase that colocalizes with the elongating form of RNA polymerase II. Mol Cell Biol 28: 1041-1046.
9. Lan F, Bayliss PE, Rinn JL, Whetstine JR, Wang JK, et al. (2007) A histone H3 lysine 27 demethylase regulates animal posterior development. Nature 449: 689-694.
10. De Santa F, Totaro MG, Prosperini E, Notarbartolo S, Testa G, et al. (2007) The Histone H3 Lysine-27 Demethylase Jmjd3 Links Inflammation to Inhibition of Polycomb-Mediated Gene Silencing. Cell 130: 1083-1094.
11. Hong S, Cho YW, Yu LR, Yu H, Veenstra TD, et al. (2007) Identification of JmjC domain-containing UTX and JMJD3 as histone H3 lysine 27 demethylases. Proc Natl Acad Sci USA 104: 18439-18444.
12. Fisher K, Southall SM, Wilson JR, Poulin GB, (2010) Methylation and demethylation activities of a C. elegans MLL-like complex attenuate RAS signalling. Developmental biology 341: 142-153.
13. Maures TJ, Greer EL, Hauswirth AG, Brunet A, (2011) The H3K27 demethylase UTX-1 regulates C. elegans lifespan in a germline-independent, insulin-dependent manner. Aging cell 10: 980-990.
14. Jin C, Li J, Green CD, Yu X, Tang X, et al. (2011) Histone demethylase UTX-1 regulates C. elegans life span by targeting the insulin/IGF-1 signaling pathway. Cell metabolism 14: 161-172.
15. Mohler WA, Simske JS, Williams-Masson EM, Hardin JD, White JG, (1998) Dynamics and ultrastructure of developmental cell fusions in the Caenorhabditis elegans hypodermis. Current biology: CB 8: 1087-1090.
16. Henderson ST, Gao D, Lambie EJ, Kimble J, (1994) lag-2 may encode a signaling ligand for the GLP-1 and LIN-12 receptors of C. elegans. Development 120: 2913-2924.
17. Swigut T, Wysocka J, (2007) H3K27 demethylases, at long last. Cell 131: 29-32.
18. Jin C, Li J, Green CD, Yu X, Tang X, et al. (2011) Histone Demethylase UTX-1 Regulates C. elegans Life Span by Targeting the Insulin/IGF-1 Signaling Pathway. Cell metabolism 14: 161-172.
19. Cloos PA, Christensen J, Agger K, Maiolica A, Rappsilber J, et al. (2006) The putative oncogene GASC1 demethylates tri- and dimethylated lysine 9 on histone H3. Nature 442: 307-311.
20. Klose RJ, Yamane K, Bae Y, Zhang D, Erdjument-Bromage H, et al. (2006) The transcriptional repressor JHDM3A demethylates trimethyl histone H3 lysine 9 and lysine 36. Nature 442: 312-316.
21. Chang B, Chen Y, Zhao Y, Bruick RK, (2007) JMJD6 is a histone arginine demethylase. Science 318: 444-447.
22. Issaeva I, Zonis Y, Rozovskaia T, Orlovsky K, Croce CM, et al. (2007) Knockdown of ALR (MLL2) reveals ALR target genes and leads to alterations in cell adhesion and growth. Mol Cell Biol 27: 1889-1903.
23. Cho YW, Hong T, Hong S, Guo H, Yu H, et al. (2007) PTIP associates with MLL3- and MLL4-containing histone H3 lysine 4 methyltransferase complex. J Biol Chem 282: 20395-20406.
24. Patel SR, Kim D, Levitan I, Dressler GR, (2007) The BRCT-domain containing protein PTIP links PAX2 to a histone H3, lysine 4 methyltransferase complex. Dev Cell 13: 580-592.
25. Shilatifard A, (2008) Molecular implementation and physiological roles for histone H3 lysine 4 (H3K4) methylation. Current opinion in cell biology 20: 341-348.
26. Simonet T, Dulermo R, Schott S, Palladino F, (2007) Antagonistic functions of SET-2/SET1 and HPL/HP1 proteins in C. elegans development. Developmental biology 312: 367-383.
27. Andersen EC, Horvitz HR, (2007) Two C. elegans histone methyltransferases repress lin-3 EGF transcription to inhibit vulval development. Development 134: 2991-2999.
28. Seenundun S, Rampalli S, Liu QC, Aziz A, Palii C, et al. (2010) UTX mediates demethylation of H3K27me3 at muscle-specific genes during myogenesis. The EMBO journal 29: 1401-1411.
29. Agger K, Cloos PA, Rudkjaer L, Williams K, Andersen G, et al. (2009) The H3K27me3 demethylase JMJD3 contributes to the activation of the INK4A-ARF locus in response to oncogene- and stress-induced senescence. Genes Dev 23: 1171-1176.
30. Miller SA, Mohn SE, Weinmann AS, (2010) Jmjd3 and UTX play a demethylase-independent role in chromatin remodeling to regulate T-box family member-dependent gene expression. Molecular cell 40: 594-605.
31. Greer EL, Maures TJ, Hauswirth AG, Green EM, Leeman DS, et al. (2010) Members of the H3K4 trimethylation complex regulate lifespan in a germline-dependent manner in C. elegans. Nature 466: 383-387.
32. Xiao Y, Bedet C, Robert VJ, Simonet T, Dunkelbarger S, et al. (2011) Caenorhabditis elegans chromatin-associated proteins SET-2 and ASH-2 are differentially required for histone H3 Lys 4 methylation in embryos and adult germ cells. Proceedings of the National Academy of Sciences of the United States of America 108: 8305-8310.
33. Solari F, Ahringer J, (2000) NURD-complex genes antagonise Ras-induced vulval development in Caenorhabditis elegans. Current biology: CB 10: 223-226.
34. 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: 265-277.
35. Wang JK, Tsai MC, Poulin G, Adler AS, Chen S, et al. (2010) The histone demethylase UTX enables RB-dependent cell fate control. Genes & development 24: 327-332.
36. Li T, Kelly WG, (2011) A role for Set1/MLL-related components in epigenetic regulation of the Caenorhabditis elegans germ line. PLoS Genet 7: e1001349 doi:10.1371/journal.pgen.1001349.
37. Capowski EE, Martin P, Garvin C, Strome S, (1991) Identification of grandchildless loci whose products are required for normal germ-line development in the nematode Caenorhabditis elegans. Genetics 129: 1061-1072.
38. Paulsen JE, Capowski EE, Strome S, (1995) Phenotypic and molecular analysis of mes-3, a maternal-effect gene required for proliferation and viability of the germ line in C. elegans. Genetics 141: 1383-1398.
39. Kelly WG, Fire A, (1998) Chromatin silencing and the maintenance of a functional germline in Caenorhabditis elegans. Development 125: 2451-2456.
40. Holdeman R, Nehrt S, Strome S, (1998) MES-2, a maternal protein essential for viability of the germline in Caenorhabditis elegans, is homologous to a Drosophila Polycomb group protein. Development 125: 2457-2467.
41. Korf I, Fan Y, Strome S, (1998) The Polycomb group in Caenorhabditis elegans and maternal control of germline development. Development 125: 2469-2478.
42. Bender LB, Cao R, Zhang Y, Strome S, (2004) The MES-2/MES-3/MES-6 complex and regulation of histone H3 methylation in C. elegans. Curr Biol 14: 1639-1643.
43. Bender LB, Suh J, Carroll CR, Fong Y, Fingerman IM, et al. (2006) MES-4: an autosome-associated histone methyltransferase that participates in silencing the X chromosomes in the C. elegans germ line. Development 133: 3907-3917.
44. Brenner S, (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
45. Timmons L, Court DL, Fire A, (2001) Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene 263: 103-112.
46. Krag C, Malmberg EK, Salcini AE, (2010) PI3KC2alpha, a class II PI3K, is required for dynamin-independent internalization pathways. Journal of cell science 123: 4240-4250.
47. Finney M, Ruvkun G, (1990) The unc-86 gene product couples cell lineage and cell identity in C. elegans. Cell 63: 895-905.
48. Vandamme J, Volkel P, Rosnoblet C, Le Faou P, Angrand PO, (2011) Interaction proteomics analysis of polycomb proteins defines distinct PRC1 complexes in mammalian cells. Molecular & cellular proteomics: MCP 10: M110 002642.