Conservation and divergence of the histone H2B monoubiquitination pathway from yeast to humans and plants

Abstract

Histone ubiquitination plays a critical role in the regulation of transcription, and histone H2B monoubiquitination (H2Bub1) is mainly associated with transcriptional activation. Recent studies in yeast, humans, and BoldItalic have revealed the conservation of chromatin modification via H2Bub1 during evolution. Rad6-Bre1 and their homologs are responsible for H2B monoubiquitination in diverse eukaryotic organisms, and the PAF complex is required for H2Bub1 to proceed. H2Bub1 is involved in many developmental processes in yeast, humans, and BoldItalic, and it activates gene transcription by regulating the H3K4 methylation state. Notably, the level of H3K4 methylation is entirely dependent on H2Bub1 in yeast and humans, whereas the H3K4 methylation level of only a small number of genes in BoldItalic is dependent on H2Bub1. In this review, we summarize the enzymes involved in H2B monoubiquitination and deubiquitination, and discuss the biologic functions of H2Bub1 in different organisms. In addition, we focus on recent advances in our understanding of the molecular mechanisms that enable H2Bub1 to perform its function.

Keywords

H2B monoubiquitination / H2B deubiquitination / H3K4 methylation / PAF complex / transcriptional requlation

References

[1] Briggs S D, Xiao T, Sun Z W, Caldwell J A, Shabanowitz J, Hunt D F, Allis C D, Strahl B D (2002). Gene silencing: trans-histone regulatory pathway in chromatin. Nature, 418(6897): 498

[2] Cao Y, Dai Y, Cui S J, Ma L G (2008). Histone H2B monoubiquitination in the chromatin of FLOWERING LOCUS C regulates flowering time in Arabidopsis. Plant Cell, 20: 2586-2602

[3] Chandrasekharan M B, Huang F, Chen Y C, Sun Z W (2010b). Histone H2B C-terminal helix mediates trans-histone H3K4 methylation independent of H2B ubiquitination. Mol Cell Biol, 30(13): 3216-3232

[4] Chandrasekharan M B, Huang F, Sun Z W (2009). Ubiquitination of histone H2B regulates chromatin dynamics by enhancing nucleosome stability. Proc Natl Acad Sci USA, 106(39): 16686-16691

[5] Chandrasekharan M B, Huang F, Sun Z W (2010a). Histone H2B ubiquitination and beyond: Regulation of nucleosome stability, chromatin dynamics and the trans-histone H3 methylation. Epigenetics, 5(6): 460-468

[6] Daniel J A, Torok M S, Sun Z W, Schieltz D, Allis C D, Yates J R 3rd, Grant P A (2004). Deubiquitination of histone H2B by a yeast acetyltransferase complex regulates transcription. J Biol Chem, 279(3): 1867-1871

[7] Dhawan R, Luo H, Foerster A M, Abuqamar S, Du H N, Briggs S D, Scheid O M, Mengiste T (2009). HISTONE MONOUBIQUITINATION1 interacts with a subunit of the mediator complex and regulates defense against necrotrophic fungal pathogens in Arabidopsis. Plant Cell, 21(3): 1000-1019

[8] Dover J, Schneider J, Tawiah-Boateng M A, Wood A, Dean K, Johnston M, Shilatifard A (2002). Methylation of histone H3 by COMPASS requires ubiquitination of histone H2B by Rad6. J Biol Chem, 277(32): 28368-28371

[9] Emre N C, Ingvarsdottir K, Wyce A, Wood A, Krogan N J, Henry K W, Li K, Marmorstein R, Greenblatt J F, Shilatifard A, Berger S L (2005). Maintenance of low histone ubiquitylation by Ubp10 correlates with telomere-proximal Sir2 association and gene silencing. Mol Cell, 17(4): 585-594

[10] Espinosa J M (2008). Histone H2B ubiquitination: the cancer connection. Genes Dev, 22(20): 2743-2749

[11] Ezhkova E, Tansey W P (2004). Proteasomal ATPases link ubiquitylation of histone H2B to methylation of histone H3. Mol Cell, 13(3): 435-442

[12] Fleming A B, Kao C F, Hillyer C, Pikaart M, Osley M A (2008). H2B ubiquitylation plays a role in nucleosome dynamics during transcription elongation. Mol Cell, 31(1): 57-66

[13] Fleury D, Himanen K, Cnops G, Nelissen H, Boccardi T M, Maere S, Beemster G T S, Neyt P, Anami S, Robles P, Micol J L, Inzé D, Van Lijsebettens M (2007). The Arabidopsis thaliana homolog of yeast BRE1 has a function in cell cycle regulation during early leaf and root growth. Plant Cell, 19(2): 417-432

[14] Gardner R G, Nelson Z W, Gottschling D E (2005). Ubp10/Dot4p regulates the persistence of ubiquitinated histone H2B: distinct roles in telomeric silencing and general chromatin. Mol Cell Biol, 25(14): 6123-6139

[15] Goldknopf I L, Taylor C W, Baum R M, Yeoman L C, Olson M O, Prestayko A W, Busch H (1975). Isolation and characterization of protein A24, a “histone-like” non-histone chromosomal protein. J Biol Chem, 250(18): 7182-7187

[16] Gu X, Jiang D, Wang Y, Bachmair A, He Y (2009). Repression of the floral transition via histone H2B monoubiquitination. Plant J, 57(3): 522-533

[17] Hartzog G A, Quan T K (2008). Just the FACTs: histone H2B ubiquitylation and nucleosome dynamics. Mol Cell, 31(1): 2-4

[18] Henry K W, Wyce A, Lo W S, Duggan L J, Emre N C T, Kao C F, Pillus L, Shilatifard A, Osley M A, Berger S L (2003). Transcriptional activation via sequential histone H2B ubiquitylation and deubiquitylation, mediated by SAGA-associated Ubp8. Genes Dev, 17(21): 2648-2663

[19] Hwang W W, Venkatasubrahmanyam S, Ianculescu A G, Tong A, Boone C, Madhani H D (2003). A conserved RING finger protein required for histone H2B monoubiquitination and cell size control. Mol Cell, 11(1): 261-266

[20] Ingvarsdottir K, Krogan N J, Emre N C, Wyce A, Thompson N J, Emili A, Hughes T R, Greenblatt J F, Berger S L (2005). H2B ubiquitin protease Ubp8 and Sgf11 constitute a discrete functional module within the Saccharomyces cerevisiae SAGA complex. Mol Cell Biol, 25(3): 1162-1172

[21] Jenuwein T, Allis C D (2001). Translating the histone code. Science, 293(5532): 1074-1080

[22] Kao C F, Hillyer C, Tsukuda T, Henry K, Berger S, Osley M A (2004). Rad6 plays a role in transcriptional activation through ubiquitylation of histone H2B. Genes Dev, 18(2): 184-195

[23] Kim J, Guermah M, McGinty R K, Lee J S, Tang Z, Milne T A, Shilatifard A, Muir T W, Roeder R G (2009). RAD6-Mediated transcription-coupled H2B ubiquitylation directly stimulates H3K4 methylation in human cells. Cell, 137(3): 459-471

[24] Kim J, Hake S B, Roeder R G (2005). The human homolog of yeast BRE1 functions as a transcriptional coactivator through direct activator interactions. Mol Cell, 20(5): 759-770

[25] Kornberg R D, Lorch Y (1999). Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome. Cell, 98(3): 285-294

[26] Kouzarides T (2007). Chromatin modifications and their function. Cell, 128(4): 693-705

[27] Krogan N J, Dover J, Wood A, Schneider J, Heidt J, Boateng M A, Dean K, Ryan O W, Golshani A, Johnston M, Greenblatt J F, Shilatifard A (2003). The Paf1 complex is required for histone H3 methylation by COMPASS and Dot1p: linking transcriptional elongation to histone methylation. Mol Cell, 11(3): 721-729

[28] Laribee R N, Fuchs S M, Strahl B D (2007a). H2B ubiquitylation in transcriptional control: a FACT-finding mission. Genes Dev, 21(7): 737-743

[29] Laribee R N, Shibata Y, Mersman D P, Collins S R, Kemmeren P, Roguev A, Weissman J S, Briggs S D, Krogan N J, Strahl B D (2007b). CCR4/NOT complex associates with the proteasome and regulates histone methylation. Proc Natl Acad Sci USA, 104(14): 5836-5841

[30] Lee J S, Shukla A, Schneider J, Swanson S K, Washburn M P, Florens L, Bhaumik S R, Shilatifard A (2007). Histone crosstalk between H2B monoubiquitination and H3 methylation mediated by COMPASS. Cell, 131(6): 1084-1096

[31] Lee K K, Florens L, Swanson S K, Washburn M P, Workman J L (2005). The deubiquitylation activity of Ubp8 is dependent upon Sgf11 and its association with the SAGA complex. Mol Cell Biol, 25(3): 1173-1182

[32] Li B, Carey M, Workman J L (2007). The role of chromatin during transcription. Cell, 128(4): 707-719

[33] Liu Y, Koornneef M, Soppe W J J (2007). The absence of histone H2B monoubiquitination in the Arabidopsis hub1 (rdo4) mutant reveals a role for chromatin remodeling in seed dormancy. Plant Cell, 19(2): 433-444

[34] Lolas I B, Himanen K, Grønlund J T, Lynggaard C, Houben A, Melzer M, Van Lijsebettens M, Grasser K D (2010). The transcript elongation factor FACT affects Arabidopsis vegetative and reproductive development and genetically interacts with HUB1/2. Plant J, 61(4): 686-697

[35] Luger K, Mäder A W, Richmond R K, Sargent D F, Richmond T J (1997). Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature, 389(6648): 251-260

[36] Minsky N, Shema E, Field Y, Schuster M, Segal E, Oren M (2008). Monoubiquitinated H2B is associated with the transcribed region of highly expressed genes in human cells. Nat Cell Biol, 10(4): 483-488

[37] Nakanishi S, Lee J S, Gardner K E, Gardner J M, Takahashi Y H, Chandrasekharan M B, Sun Z W, Osley M A, Strahl B D, Jaspersen S L, Shilatifard A (2009). Histone H2BK123 monoubiquitination is the critical determinant for H3K4 and H3K79 trimethylation by COMPASS and Dot1. J Cell Biol, 186(3): 371-377

[38] Ng H H, Dole S, Struhl K (2003). The Rtf1 component of the Paf1 transcriptional elongation complex is required for ubiquitination of histone H2B. J Biol Chem, 278(36): 33625-33628

[39] Oh S, Zhang H, Ludwig P, van Nocker S (2004). A mechanism related to the yeast transcriptional regulator Paf1c is required for expression of the Arabidopsis FLC/MAF MADS box gene family. Plant Cell, 16(11): 2940-2953

[40] Osley M A (2004). H2B ubiquitylation: the end is in sight. Biochim Biophys Acta, 1677(1-3): 74-78

[41] Osley M A (2006). Regulation of histone H2A and H2B ubiquitylation. Brief Funct Genomics Proteomics, 5(3): 179-189

[42] Osley M A, Fleming A B, Kao C F (2006). Histone ubiquitylation and the regulation of transcription. Results Probl Cell Differ, 41: 47-75

[43] Pavri R, Zhu B, Li G, Trojer P, Mandal S, Shilatifard A, Reinberg D (2006). Histone H2B monoubiquitination functions cooperatively with FACT to regulate elongation by RNA polymerase II. Cell, 125(4): 703-717

[44] Pfluger J, Wagner D (2007). Histone modifications and dynamic regulation of genome accessibility in plants. Curr Opin Plant Biol, 10(6): 645-652

[45] Pirngruber J, Shchebet A, Schreiber L, Shema E, Minsky N, Chapman R D, Eick D, Aylon Y, Oren M, Johnsen S A (2009). CDK9 directs H2B monoubiquitination and controls replication-dependent histone mRNA 3¢-end processing. EMBO Rep, 10(8): 894-900PMID:19575011

[46] Robzyk K, Recht J, Osley M A (2000). Rad6-dependent ubiquitination of histone H2B in yeast. Science, 287(5452): 501-504

[47] Schmitz R J, Tamada Y, Doyle M R, Zhang X, Amasino R M (2009). Histone H2B deubiquitination is required for transcriptional activation of FLOWERING LOCUS C and for proper control of flowering in Arabidopsis. Plant Physiol, 149(2): 1196-1204

[48] Shema E, Tirosh I, Aylon Y, Huang J, Ye C, Moskovits N, Raver-Shapira N, Minsky N, Pirngruber J, Tarcic G, Hublarova P, Moyal L, Gana-Weisz M, Shiloh Y, Yarden Y, Johnsen S A, Vojtesek B, Berger S L, Oren M (2008). The histone H2B-specific ubiquitin ligase RNF20/hBRE1 acts as a putative tumor suppressor through selective regulation of gene expression. Genes Dev, 22(19): 2664-2676

[49] Shukla A, Bhaumik S R (2007). H2B-K123 ubiquitination stimulates RNAPII elongation independent of H3-K4 methylation. Biochem Biophys Res Commun, 359(2): 214-220

[50] Sridhar V V, Kapoor A, Zhang K, Zhu J, Zhou T, Hasegawa P M, Bressan R A, Zhu J K (2007). Control of DNA methylation and heterochromatic silencing by histone H2B deubiquitination. Nature, 447(7145): 735-738

[51] Sun Z W, Allis C D (2002). Ubiquitination of histone H2B regulates H3 methylation and gene silencing in yeast. Nature, 418(6893): 104-108

[52] Tanny J C, Erdjument-Bromage H, Tempst P, Allis C D (2007). Ubiquitylation of histone H2B controls RNA polymerase II transcription elongation independently of histone H3 methylation. Genes Dev, 21(7): 835-847

[53] Turner B M (2002). Cellular memory and the histone code. Cell, 111(3): 285-291

[54] Weake V M, Workman J L (2008). Histone ubiquitination: triggering gene activity. Mol Cell, 29(6): 653-663

[55] West M H, Bonner W M (1980). Histone 2B can be modified by the attachment of ubiquitin. Nucleic Acids Res, 8(20): 4671-4680

[56] Wood A, Krogan N J, Dover J, Schneider J, Heidt J, Boateng M A, Dean K, Golshani A, Zhang Y, Greenblatt J F, Johnston M, Shilatifard A (2003a). Bre1, an E3 ubiquitin ligase required for recruitment and substrate selection of Rad6 at a promoter. Mol Cell, 11(1): 267-274

[57] Wood A, Schneider J, Dover J, Johnston M, Shilatifard A (2003b). The Paf1 complex is essential for histone monoubiquitination by the Rad6-Bre1 complex, which signals for histone methylation by COMPASS and Dot1p. J Biol Chem, 278(37): 34739-34742

[58] Wyce A, Henry K W, Berger S L (2004). H2B ubiquitylation and de-ubiquitylation in gene activation. Novartis Found Symp, 259: 63-73, discussion 73-77, 163-169

[59] Wyce A, Xiao T, Whelan K A, Kosman C, Walter W, Eick D, Hughes T R, Krogan N J, Strahl B D, Berger S L (2007). H2B ubiquitylation acts as a barrier to Ctk1 nucleosomal recruitment prior to removal by Ubp8 within a SAGA-related complex. Mol Cell, 27(2): 275-288

[60] Xiao T, Kao C F, Krogan N J, Sun Z W, Greenblatt J F, Osley M A, Strahl B D (2005). Histone H2B ubiquitylation is associated with elongating RNA polymerase II. Mol Cell Biol, 25(2): 637-651

[61] Xu L, Ménard R, Berr A, Fuchs J, Cognat V, Meyer D, Shen W H (2009). The E2 ubiquitin-conjugating enzymes, AtUBC1 and AtUBC2, play redundant roles and are involved in activation of FLC expression and repression of flowering in Arabidopsis thaliana. Plant J, 57(2): 279-288

[62] Zhang X Y, Varthi M, Sykes S M, Phillips C, Warzecha C, Zhu W, Wyce A, Thorne A W, Berger S L, McMahon S B (2008). The putative cancer stem cell marker USP22 is a subunit of the human SAGA complex required for activated transcription and cell-cycle progression. Mol Cell, 29(1): 102-111

[63] Zhang Y (2003). Transcriptional regulation by histone ubiquitination and deubiquitination. Genes Dev, 17(22): 2733-2740

[64] Zhao Y, Lang G, Ito S, Bonnet J, Metzger E, Sawatsubashi S, Suzuki E, Le Guezennec X, Stunnenberg H G, Krasnov A, Georgieva S G, Schüle R, Takeyama K, Kato S, Tora L, Devys D (2008). A TFTC/STAGA module mediates histone H2A and H2B deubiquitination, coactivates nuclear receptors, and counteracts heterochromatin silencing. Mol Cell, 29(1): 92-101

[65] Zhu B, Mandal S S, Pham A D, Zheng Y, Erdjument-Bromage H, Batra S K, Tempst P, Reinberg D (2005a). The human PAF complex coordinates transcription with events downstream of RNA synthesis. Genes Dev, 19(14): 1668-1673

[66] Zhu B, Zheng Y, Pham A D, Mandal S S, Erdjument-Bromage H, Tempst P, Reinberg D (2005b). Monoubiquitination of human histone H2B: the factors involved and their roles in HOX gene regulation. Mol Cell, 20(4): 601-611

Acknowledgments

We thank Dr. Jessica Habashi for critical reading of the manuscript. This work was supported by grants from China MOST 863 project (L.M.), Hebei Province Key Laboratory Program (L.M.), National Science Foundation of China (Y.C.).

RIGHTS & PERMISSIONS

2014 Higher Education Press and Springer-Verlag Berlin Heidelberg