Histone H2A Monoubiquitination Represses Transcription by Inhibiting RNA Polymerase II Transcriptional Elongation

Molecular Cell

Volumn 29, Issue 1, 2008, Pages 69-80

  Zhou, Wenlai ^a,b   Zhu, Ping ^a,b   Wang, Jianxun ^a,b   Pascual, Gabriel ^c   Ohgi, Kenneth A ^a,b   Lozach, Jean ^c   Glass, Christopher K ^c   Rosenfeld, Michael G ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

DNA; PROTEINS

Indexed keywords

HISTONE H2A; RING FINGER PROTEIN; RNA POLYMERASE II; TOLL LIKE RECEPTOR; UBIQUITIN PROTEIN LIGASE;

ARTICLE; GENE CONTROL; GENE EXPRESSION; NUCLEOTIDE SEQUENCE; PROMOTER REGION; PROTEIN DOMAIN; PROTEIN FUNCTION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; UBIQUITINATION;

AMINO ACID SEQUENCE; ANIMALS; CELL LINE; CHEMOKINES; DNA-BINDING PROTEINS; HIGH MOBILITY GROUP PROTEINS; HISTONE DEACETYLASES; HISTONES; HUMANS; LIGASES; MACROPHAGES; MICE; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PEPTIDE CHAIN ELONGATION, TRANSLATIONAL; PROTEIN PROCESSING, POST-TRANSLATIONAL; REPRESSOR PROTEINS; RING FINGER DOMAINS; RNA POLYMERASE II; RNA-BINDING PROTEINS; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ELONGATION FACTORS; UBIQUITIN; UBIQUITINATION;

EUKARYOTA;

EID: 38149098408     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2007.11.002     Document Type: Article

References (64)

1. Amendt B.A., Sutherland L.B., Semina E.V., and Russo A.F. The molecular basis of Rieger syndrome. Analysis of Pitx2 homeodomain protein activities. J. Biol. Chem. 273 (1998) 20066-20072
2. Baek S.H., Kioussi C., Briata P., Wang D., Nguyen H.D., Ohgi K.A., Glass C.K., Wynshaw-Boris A., Rose D.W., and Rosenfeld M.G. Regulated subset of G1 growth-control genes in response to derepression by the Wnt pathway. Proc. Natl. Acad. Sci. USA 100 (2003) 3245-3250
3. Bondarenko V.A., Steele L.M., Ujvari A., Gaykalova D.A., Kulaeva O.I., Polikanov Y.S., Luse D.S., and Studitsky V.M. Nucleosomes can form a polar barrier to transcript elongation by RNA polymerase II. Mol. Cell 24 (2006) 469-479
4. Borden K.L. RING domains: master builders of molecular scaffolds?. J. Mol. Biol. 295 (2000) 1103-1112
5. Breiling A., Turner B.M., Bianchi M.E., and Orlando V. General transcription factors bind promoters repressed by Polycomb group proteins. Nature 412 (2001) 651-655
6. Cao R., Tsukada Y., and Zhang Y. Role of Bmi-1 and Ring1A in H2A ubiquitylation and Hox gene silencing. Mol. Cell 20 (2005) 845-854
7. Dawson B.A., Herman T., Haas A.L., and Lough J. Affinity isolation of active murine erythroleukemia cell chromatin: uniform distribution of ubiquitinated histone H2A between active and inactive fractions. J. Cell. Biochem. 46 (1991) 166-173
8. Dellino G.I., Schwartz Y.B., Farkas G., McCabe D., Elgin S.C., and Pirrotta V. Polycomb silencing blocks transcription initiation. Mol. Cell 13 (2004) 887-893
9. de Napoles M., Mermoud J.E., Wakao R., Tang Y.A., Endoh M., Appanah R., Nesterova T.B., Silva J., Otte A.P., Vidal M., et al. Polycomb group proteins Ring1A/B link ubiquitylation of histone H2A to heritable gene silencing and X inactivation. Dev. Cell 7 (2004) 663-676
10. Doyle S., Vaidya S., O'Connell R., Dadgostar H., Dempsey P., Wu T., Rao G., Sun R., Haberland M., Modlin R., et al. IRF3 mediates a TLR3/TLR4-specific antiviral gene program. Immunity 17 (2002) 251-263
11. Eissenberg J.C., and Shilatifard A. Leaving a mark: the many footprints of the elongating RNA polymerase II. Curr. Opin. Genet. Dev. 16 (2006) 184-190
12. Fang J., Chen T., Chadwick B., Li E., and Zhang Y. Ring1b-mediated H2A ubiquitination associates with inactive X chromosomes and is involved in initiation of X inactivation. J. Biol. Chem. 279 (2004) 52812-52815
13. Fischle W., Wang Y., and Allis C.D. Binary switches and modification cassettes in histone biology and beyond. Nature 425 (2003) 475-479
14. Gearhart M.D., Corcoran C.M., Wamstad J.A., and Bardwell V.J. Polycomb group and SCF ubiquitin ligases are found in a novel BCOR complex that is recruited to BCL6 targets. Mol. Cell. Biol. 26 (2006) 6880-6889
15. Goldknopf I.L., Taylor C.W., Baum R.M., Yeoman L.C., Olson M.O., Prestayko A.W., and Busch H. Isolation and characterization of protein A24, a "histone-like" non-histone chromosomal protein. J. Biol. Chem. 250 (1975) 7182-7187
16. Henry K.W., Wyce A., Lo W.S., Duggan L.J., Emre N.C., Kao C.F., Pillus L., Shilatifard A., Osley M.A., and Berger S.L. Transcriptional activation via sequential histone H2B ubiquitylation and deubiquitylation, mediated by SAGA-associated Ubp8. Genes Dev. 17 (2003) 2648-2663
17. Huang S.Y., Barnard M.B., Xu M., Matsui S., Rose S.M., and Garrard W.T. The active immunoglobulin kappa chain gene is packaged by non-ubiquitin-conjugated nucleosomes. Proc. Natl. Acad. Sci. USA 83 (1986) 3738-3742
18. Hwang W.W., Venkatasubrahmanyam S., Ianculescu A.G., Tong A., Boone C., and Madhani H.D. A conserved RING finger protein required for histone H2B monoubiquitination and cell size control. Mol. Cell 11 (2003) 261-266
19. Jenuwein T., and Allis C.D. Translating the histone code. Science 293 (2001) 1074-1080
20. Kao C.F., Hillyer C., Tsukuda T., Henry K., Berger S., and Osley M.A. Rad6 plays a role in transcriptional activation through ubiquitylation of histone H2B. Genes Dev. 18 (2004) 184-195
21. Kim J., Hake S.B., and Roeder R.G. The human homolog of yeast BRE1 functions as a transcriptional coactivator through direct activator interactions. Mol. Cell 20 (2005) 759-770
22. Kim T.H., Barrera L.O., Zheng M., Qu C., Singer M.A., Richmond T.A., Wu Y., Green R.D., and Ren B. A high-resolution map of active promoters in the human genome. Nature 436 (2005) 876-880
23. Kioussi C., Briata P., Baek S.H., Rose D.W., Hamblet N.S., Herman T., Ohgi K.A., Lin C., Gleiberman A., Wang J., et al. Identification of a Wnt/Dvl/β-catenin→Pitx2 pathway mediating cell-type-specific proliferation during development. Cell 111 (2002) 673-685
24. Kireeva M.L., Hancock B., Cremona G.H., Walter W., Studitsky V.M., and Kashlev M. Nature of the nucleosomal barrier to RNA polymerase II. Mol. Cell 18 (2005) 97-108
25. Klose R.J., Yamane K., Bae Y., Zhang D., Erdjument-Bromage H., Tempst P., Wong J., and Zhang Y. The transcriptional repressor JHDM3A demethylates trimethyl histone H3 lysine 9 and lysine 36. Nature 442 (2006) 312-316
26. Komarnitsky P., Cho E.J., and Buratowski S. Different phosphorylated forms of RNA polymerase II and associated mRNA processing factors during transcription. Genes Dev. 14 (2000) 2452-2460
27. Kreft S.G., and Nassal M. hRUL138, a novel human RNA-binding RING-H2 ubiquitin-protein ligase. J. Cell Sci. 116 (2003) 605-616
28. Levinger L., and Varshavsky A. Selective arrangement of ubiquitinated and D1 protein-containing nucleosomes within the Drosophila genome. Cell 28 (1982) 375-385
29. Li J., Wang J., Wang J., Nawaz Z., Liu J.M., Qin J., and Wong J. Both corepressor proteins SMRT and N-CoR exist in large protein complexes containing HDAC3. EMBO J. 19 (2000) 4342-4350
30. Li B., Carey M., and Workman J.L. The role of chromatin during transcription. Cell 128 (2007) 707-719
31. Lu M.F., Pressman C., Dyer R., Johnson R.L., and Martin J.F. Function of Rieger syndrome gene in left-right asymmetry and craniofacial development. Nature 401 (1999) 276-278
32. Margueron R., Trojer P., and Reinberg D. The key to development: interpreting the histone code?. Curr. Opin. Genet. Dev. 15 (2005) 163-176
33. Minsky N., and Oren M. The RING domain of Mdm2 mediates histone ubiquitylation and transcriptional repression. Mol. Cell 16 (2004) 631-639
34. Nickel B.E., and Davie J.R. Structure of polyubiquitinated histone H2A. Biochemistry 28 (1989) 964-968
35. Nickel B.E., Allis C.D., and Davie J.R. Ubiquitinated histone H2B is preferentially located in transcriptionally active chromatin. Biochemistry 28 (1989) 958-963
36. Ogawa S., Lozach J., Jepsen K., Sawka-Verhelle D., Perissi V., Sasik R., Rose D.W., Johnson R.S., Rosenfeld M.G., and Glass C.K. A nuclear receptor corepressor transcriptional checkpoint controlling activator protein 1-dependent gene networks required for macrophage activation. Proc. Natl. Acad. Sci. USA 101 (2004) 14461-14466
37. Orphanides G., LeRoy G., Chang C.H., Luse D.S., and Reinberg D. FACT, a factor that facilitates transcript elongation through nucleosomes. Cell 92 (1998) 105-116
38. Orphanides G., Wu W.H., Lane W.S., Hampsey M., and Reinberg D. The chromatin-specific transcription elongation factor FACT comprises human SPT16 and SSRP1 proteins. Nature 400 (1999) 284-288
39. Osley M.A. H2B ubiquitylation: the end is in sight. Biochim. Biophys. Acta 1677 (2004) 74-78
40. Parlow M.H., Haas A.L., and Lough J. Enrichment of ubiquitinated histone H2A in a low salt extract of micrococcal nuclease-digested myotube nuclei. J. Biol. Chem. 265 (1990) 7507-7512
41. Pascual G., Fong A.L., Ogawa S., Gamliel A., Li A.C., Perissi V., Rose D.W., Willson T.M., Rosenfeld M.G., and Glass C.K. A SUMOylation-dependent pathway mediates transrepression of inflammatory response genes by PPAR-gamma. Nature 437 (2005) 759-763
42. Pavri R., Zhu B., Li G., Trojer P., Mandal S., Shilatifard A., and Reinberg D. Histone H2B monoubiquitination functions cooperatively with FACT to regulate elongation by RNA polymerase II. Cell 125 (2006) 703-717
43. Perissi V., Aggarwal A., Glass C.K., Rose D.W., and Rosenfeld M.G. A corepressor/coactivator exchange complex required for transcriptional activation by nuclear receptors and other regulated transcription factors. Cell 116 (2004) 511-526
44. Peterlin B.M., and Price D.H. Controlling the elongation phase of transcription with P-TEFb. Mol. Cell 23 (2006) 297-305
45. Peterson C.L., and Laniel M.A. Histones and histone modifications. Curr. Biol. 14 (2004) R546-R551
46. Reinberg D., and Sims III R.J. de FACTo nucleosome dynamics. J. Biol. Chem. 281 (2006) 23297-23301
47. Robzyk K., Recht J., and Osley M.A. Rad6-dependent ubiquitination of histone H2B in yeast. Science 287 (2000) 501-504
48. Rollins B.J. Chemokines. Blood 90 (1997) 909-928
49. Saunders A., Core L.J., and Lis J.T. Breaking barriers to transcription elongation. Nat. Rev. Mol. Cell Biol. 7 (2006) 557-567
50. Saurin A.J., Shao Z., Erdjument-Bromage H., Tempst P., and Kingston R.E. A Drosophila Polycomb group complex includes Zeste and dTAFII proteins. Nature 412 (2001) 655-660
51. Srinivasan S., Armstrong J.A., Deuring R., Dahlsveen I.K., McNeill H., and Tamkun J.W. The Drosophila trithorax group protein Kismet facilitates an early step in transcriptional elongation by RNA polymerase II. Development 132 (2005) 1623-1635
52. Strahl B.D., and Allis C.D. The language of covalent histone modifications. Nature 403 (2000) 41-45
53. Sun Z.W., and Allis C.D. Ubiquitination of histone H2B regulates H3 methylation and gene silencing in yeast. Nature 418 (2002) 104-108
54. Tanny J.C., Erdjument-Bromage H., Tempst P., and Allis C.D. Ubiquitylation of histone H2B controls RNA polymerase II transcription elongation independently of histone H3 methylation. Genes Dev. 21 (2007) 835-847
55. Thorne A.W., Sautiere P., Briand G., and Crane-Robinson C. The structure of ubiquitinated histone H2B. EMBO J. 6 (1987) 1005-1010
56. Wang H., Wang L., Erdjument-Bromage H., Vidal M., Tempst P., Jones R.S., and Zhang Y. Role of histone H2A ubiquitination in Polycomb silencing. Nature 431 (2004) 873-878
57. Whetstine J.R., Nottke A., Lan F., Huarte M., Smolikov S., Chen Z., Spooner E., Li E., Zhang G., Colaiacovo M., et al. Reversal of histone lysine trimethylation by the JMJD2 family of histone demethylases. Cell 125 (2006) 467-481
58. Wood A., Krogan N.J., Dover J., Schneider J., Heidt J., Boateng M.A., Dean K., Golshani A., Zhang Y., Greenblatt J.F., et al. Bre1, an E3 ubiquitin ligase required for recruitment and substrate selection of Rad6 at a promoter. Mol. Cell 11 (2003) 267-274
59. Zhang Y. Transcriptional regulation by histone ubiquitination and deubiquitination. Genes Dev. 17 (2003) 2733-2740
60. Zhang J., Kalkum M., Chait B.T., and Roeder R.G. The N-CoR-HDAC3 nuclear receptor corepressor complex inhibits the JNK pathway through the integral subunit GPS2. Mol. Cell 9 (2002) 611-623
61. Zhang D., Yoon H.G., and Wong J. JMJD2A is a novel N-CoR-interacting protein and is involved in repression of the human transcription factor achaete scute-like homologue 2 (ASCL2/Hash2). Mol. Cell. Biol. 25 (2005) 6404-6414
62. Zhu B., Zheng Y., Pham A.D., Mandal S.S., Erdjument-Bromage H., Tempst P., and Reinberg D. Monoubiquitination of human histone H2B: the factors involved and their roles in HOX gene regulation. Mol. Cell 20 (2005) 601-611
63. Zhu P., Zhou W., Wang J., Puc J., Ohgi K.A., Erdjument-Bromage H., Tempst P., Glass C.K., and Rosenfeld M.G. A histone H2A deubiquitinase complex coordinating histone acetylation and H1 dissociation in transcriptional regulation. Mol. Cell 27 (2007) 609-621
64. Zlotnik A., and Yoshie O. Chemokines: a new classification system and their role in immunity. Immunity 12 (2000) 121-127