Eviction of linker histone H1 by NAP-family histone chaperones enhances activated transcription

Epigenetics & Chromatin

Jennifer K. Nyborg²  Marisa K. Isaacson¹  Holli A. Giebler²  Qian Zhang² 

[1] Pace University, 1 Pace Plaza, New York 10038, NY, USA;Department of Biochemistry and Molecular Biology, Colorado State University, Fort Collins 80523-1870, CO, USA

关键词: Transcription activation;    Chromatin;    SET/Taf1β;    Histone chaperone;    H1;    Linker histone;   

Others  :  1226105
DOI  :  10.1186/s13072-015-0022-8

 received in 2015-06-08, accepted in 2015-08-13,  发布年份 2015

【 摘 要 】

Background

In the Metazoan nucleus, core histones assemble the genomic DNA to form nucleosome arrays, which are further compacted into dense chromatin structures by the linker histone H1. The extraordinary density of chromatin creates an obstacle for accessing the genetic information. Regulation of chromatin dynamics is therefore critical to cellular homeostasis, and histone chaperones serve as prominent players in these processes. In the current study, we examined the role of specific histone chaperones in negotiating the inherently repressive chromatin structure during transcriptional activation.

Results

Using a model promoter, we demonstrate that the human nucleosome assembly protein family members hNap1 and SET/Taf1β stimulate transcription in vitro during pre-initiation complex formation, prior to elongation. This stimulatory effect is dependent upon the presence of activators, p300, and Acetyl-CoA. We show that transcription from our chromatin template is strongly repressed by H1, and that both histone chaperones enhance RNA synthesis by overcoming H1-induced repression. Importantly, both hNap1 and SET/Taf1β directly bind H1, and function to enhance transcription by evicting the linker histone from chromatin reconstituted with H1. In vivo studies demonstrate that SET/Taf1β, but not hNap1, strongly stimulates activated transcription from the chromosomally-integrated model promoter, consistent with the observation that SET/Taf1β is nuclear, whereas hNap1 is primarily cytoplasmic. Together, these observations indicate that SET/Taf1β may serve as a critical regulator of H1 dynamics and gene activation in vivo.

Conclusions

These studies uncover a novel function for SET that mechanistically couples transcriptional derepression with H1 dynamics. Furthermore, they underscore the significance of chaperone-dependent H1 displacement as an essential early step in the transition of a promoter from a dense chromatin state into one that is permissive to transcription factor binding and robust activation.

【 授权许可】

   
2015 Zhang et al.

【 图 表 】

Fig.1.

Fig.2.

Fig.3.

Fig.4.

Fig.5.

【 参考文献 】

• [1]Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ. Crystal structure of the nucleosome core particle at 2.8 a resolution. Nature. 1997; 389(6648):251-260.
• [2]Woodcock CL, Ghosh RP. Chromatin higher-order structure and dynamics. Cold Spring Harb Perspect Biol. 2010; 2(5):a000596.
• [3]Happel N, Doenecke D. Histone h1 and its isoforms: contribution to chromatin structure and function. Gene. 2009; 431(1–2):1-12.
• [4]Bustin M, Catez F, Lim JH. The dynamics of histone H1 function in chromatin. Mol Cell. 2005; 17(5):617-620.
• [5]Zhou BR, Feng H, Kato H, Dai L, Yang Y, Zhou Y et al.. Structural insights into the histone H1-nucleosome complex. Proc Natl Acad Sci USA. 2013; 110(48):19390-19395.
• [6]Heintzman ND, Stuart RK, Hon G, Fu Y, Ching CW, Hawkins RD et al.. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat Genet. 2007; 39(3):311-318.
• [7]Izzo A, Kamieniarz-Gdula K, Ramirez F, Noureen N, Kind J, Manke T et al.. The genomic landscape of the somatic linker histone subtypes h1.1 to h1.5 in human cells. Cell Rep. 2013; 3(6):2142-2154.
• [8]Cao K, Lailler N, Zhang Y, Kumar A, Uppal K, Liu Z et al.. High-resolution mapping of H1 linker histone variants in embryonic stem cells. PLoS Genet. 2013; 9(4):e1003417.
• [9]Millan-Arino L, Islam AB, Izquierdo-Bouldstridge A, Mayor R, Terme JM, Luque N et al.. Mapping of six somatic linker histone H1 variants in human breast cancer cells uncovers specific features of H1.2. Nucleic Acids Res. 2014; 42(7):4474-4493.
• [10]Hansen JC, Nyborg JK, Luger K, Stargell LA. Histone chaperones, histone acetylation, and the fluidity of the chromogenome. J Cell Physiol. 2010; 224(2):289-299.
• [11]Das C, Tyler JK, Churchill ME. The histone shuffle: histone chaperones in an energetic dance. Trends Biochem Sci. 2010; 35(9):476-489.
• [12]Park YJ, Luger K. Structure and function of nucleosome assembly proteins. Biochem Cell Biol. 2006; 84(4):549-558.
• [13]Lorch Y, Maier-Davis B, Kornberg RD. Chromatin remodeling by nucleosome disassembly in vitro. Proc Natl Acad Sci USA. 2006; 103(9):3090-3093.
• [14]Park YJ, Chodaparambil JV, Bao Y, McBryant SJ, Luger K. Nucleosome assembly protein 1 exchanges histone H2A-H2B dimers and assists nucleosome sliding. J Biol Chem. 2005; 280(3):1817-1825.
• [15]Andrews AJ, Chen X, Zevin A, Stargell LA, Luger K. The histone chaperone NAP1 promotes nucleosome assembly by eliminating nonnucleosomal histone DNA interactions. Mol Cell. 2010; 37(6):834-842.
• [16]Ito T, Ikehara T, Nakagawa T, Kraus WL, Muramatsu M. P300-mediated acetylation facilitates the transfer of histone H2A-H2B dimers from nucleosomes to a histone chaperone. Genes Dev. 2000; 14(15):1899-1907.
• [17]Sharma N, Nyborg JK. The coactivators CBP/p300 and the histone chaperone nap1 promote transcription-independent nucleosome eviction at the HTLV-1 promoter. Proc Natl Acad Sci USA. 2008; 105(23):7959-7963.
• [18]Luebben WR, Sharma N, Nyborg JK. Nucleosome eviction and activated transcription require p300 acetylation of histone H3 lysine 14. Proc Natl Acad Sci USA. 2010; 107(45):19254-19259.
• [19]Attia M, Rachez C, Avner P, Rogner UC. Nucleosome assembly proteins and their interacting proteins in neuronal differentiation. Arch Biochem Biophys. 2013; 534(1–2):20-26.
• [20]Attia M, Rachez C, De Pauw A, Avner P, Rogner UC. Nap1l2 promotes histone acetylation activity during neuronal differentiation. Mol Cell Biol. 2007; 27(17):6093-6102.
• [21]Okuwaki M, Kato K, Nagata K. Functional characterization of human nucleosome assembly protein 1-like proteins as histone chaperones. Genes Cells. 2010; 15(1):13-27.
• [22]Muto S, Senda M, Akai Y, Sato L, Suzuki T, Nagai R et al.. Relationship between the structure of SET/TAF-Iβ/INHAT and its histone chaperone activity. Proc Natl Acad Sci USA. 2007; 104:4285-4290.
• [23]Li M, Guo H, Damuni Z. Purification and characterization of two potent heat-stable protein inhibitors of protein phosphatase 2a from bovine kidney. Biochemistry. 1995; 34(6):1988-1996.
• [24]Li M, Makkinje A, Damuni Z. The myeloid leukemia-associated protein set is a potent inhibitor of protein phosphatase 2a. J Biol Chem. 1996; 271(19):11059-11062.
• [25]von Lindern M, van Baal S, Wiegant J, Raap A, Hagemeijer A, Grosveld G. Can, a putative oncogene associated with myeloid leukemogenesis, may be activated by fusion of its 3′ half to different genes: characterization of the set gene. Mol Cell Biol. 1992; 12(8):3346-3355.
• [26]Adachi Y, Pavlakis GN, Copeland TD. Identification and characterization of set, a nuclear phosphoprotein encoded by the translocation break point in acute undifferentiated leukemia. J Biol Chem. 1994; 269(3):2258-2262.
• [27]Rosati R, La Starza R, Barba G, Gorello P, Pierini V, Matteucci C et al.. Cryptic chromosome 9q34 deletion generates TAF-1alpha/can and TAF-1beta/can fusion transcripts in acute myeloid leukemia. Haematologica. 2007; 92(2):232-235.
• [28]Saito S, Miyaji-Yamaguchi M, Nagata K. Aberrant intracellular localization of set-can fusion protein, associated with a leukemia, disorganizes nuclear export. Int J Cancer. 2004; 111(4):501-507.
• [29]Van Vlierberghe P, van Grotel M, Tchinda J, Lee C, Beverloo HB, van der Spek PJ et al.. The recurrent set-nup214 fusion as a new hoxa activation mechanism in pediatric T-cell acute lymphoblastic leukemia. Blood. 2008; 111(9):4668-4680.
• [30]Dong L, Zhu J, Wen X, Jiang T, Chen Y. Involvement of set in the wnt signaling pathway and the development of human colorectal cancer. Oncology letters. 2014; 7(4):1203-1208.
• [31]Nowak SJ, Pai CY, Corces VG. Protein phosphatase 2a activity affects histone H3 phosphorylation and transcription in drosophila melanogaster. Mol Cell Biol. 2003; 23(17):6129-6138.
• [32]Chambon JP, Touati SA, Berneau S, Cladiere D, Hebras C, Groeme R et al.. The pp2a inhibitor i2 pp2a is essential for sister chromatid segregation in oocyte meiosis II. Curr Biol. 2013; 23(6):485-490.
• [33]Qi ST, Wang ZB, Ouyang YC, Zhang QH, Hu MW, Huang X et al.. Overexpression of setbeta, a protein localizing to centromeres, causes precocious separation of chromatids during the first meiosis of mouse oocytes. J Cell Sci. 2013; 126(Pt 7):1595-1603.
• [34]Okuwaki M, Nagata K. Template activating factor-i remodels the chromatin structure and stimulates transcription from the chromatin template. J Biol Chem. 1998; 273(51):34511-34518.
• [35]Gamble MJ, Erdjument-Bromage H, Tempst P, Freedman LP, Fisher RP. The histone chaperone taf-i/set/inhat is required for transcription in vitro of chromatin templates. Mol Cell Biol. 2005; 25(2):797-807.
• [36]Gamble MJ, Fisher RP. Set and parp1 remove dek from chromatin to permit access by the transcription machinery. Nat Struct Mol Biol. 2007; 14(6):548-555.
• [37]Mansouri S, Wang S, Frappier L. A role for the nucleosome assembly proteins taf-ibeta and nap1 in the activation of bzlf1 expression and Epstein–Barr virus reactivation. PLoS One. 2013; 8(5):e63802.
• [38]Seo SB, McNamara P, Heo S, Turner A, Lane WS, Chakravarti D. Regulation of histone acetylation and transcription by inhat, a human cellular complex containing the set oncoprotein. Cell. 2001; 104(1):119-130.
• [39]Loven MA, Muster N, Yates JR, Nardulli AM. A novel estrogen receptor alpha-associated protein, template-activating factor ibeta, inhibits acetylation and transactivation. Mol Endocrinol. 2003; 17(1):67-78.
• [40]Schneider R, Bannister AJ, Weise C, Kouzarides T. Direct binding of inhat to H3 tails disrupted by modifications. J Biol Chem. 2004; 279(23):23859-23862.
• [41]Macfarlan T, Parker JB, Nagata K, Chakravarti D. Thanatos-associated protein 7 associates with template activating factor-ibeta and inhibits histone acetylation to repress transcription. Mol Endocrinol. 2006; 20(2):335-347.
• [42]Ichijo T, Chrousos GP, Kino T. Activated glucocorticoid receptor interacts with the inhat component SET/TAF-1beta and releases it from a glucocorticoid-responsive gene promoter, relieving repression: implications for the pathogenesis of glucocorticoid resistance in acute undifferentiated leukemia with set-can translocation. Mol Cell Endocrinol. 2008; 283(1–2):19-31.
• [43]Kepert JF, Mazurkiewicz J, Heuvelman GL, Toth KF, Rippe K. Nap1 modulates binding of linker histone H1 to chromatin and induces an extended chromatin fiber conformation. J Biol Chem. 2005; 280(40):34063-34072.
• [44]Shintomi K, Iwabuchi M, Saeki H, Ura K, Kishimoto T, Ohsumi K. Nucleosome assembly protein-1 is a linker histone chaperone in xenopus eggs. Proc Natl Acad Sci USA. 2005; 102(23):8210-8215.
• [45]Kato K, Okuwaki M, Nagata K. Role of template activating factor-I as a chaperone in linker histone dynamics. J Cell Sci. 2011; 124(Pt 19):3254-3265.
• [46]Georges SA, Kraus WL, Luger K, Nyborg JK, Laybourn PJ. p300-mediated tax transactivation from recombinant chromatin: histone tail deletion mimics coactivator function. Mol Cell Biol. 2002; 22(1):127-137.
• [47]Georges SA, Giebler HA, Cole PA, Luger K, Laybourn PJ, Nyborg JK. Tax recruitment of CBP/p300, via the KIX domain, reveals a potent requirement for acetyltransferase activity that is chromatin dependent and histone tail independent. Mol Cell Biol. 2003; 23(10):3392-3404.
• [48]Geiger TR, Sharma N, Kim YM, Nyborg JK. The human T-cell leukemia virus type 1 Tax protein confers CBP/p300 recruitment and transcriptional activation properties to phosphorylated CREB. Mol Cell Biol. 2008; 28(4):1383-1392.
• [49]Kim YM, Ramirez JA, Mick JE, Giebler HA, Yan JP, Nyborg JK. Molecular characterization of the tax-containing HTLV-1 enhancer complex reveals a prominent role for CREB phosphorylation in Tax transactivation. J Biol Chem. 2007; 282(26):18750-18757.
• [50]Van Orden K, Nyborg JK. Insight into the tumor suppressor function of CBP through the viral oncoprotein Tax. Gene Expr. 2000; 9(1–2):29-36.
• [51]Laybourn PJ, Kadonaga JT. Role of nucleosomal cores and histone H1 in regulation of transcription by RNA polymerase II. Science. 1991; 254(5029):238-245.
• [52]Croston GE, Laybourn PJ, Paranjape SM, Kadonaga JT. Mechanism of transcriptional antirepression by gal4-vp16. Genes Dev. 1992; 6(12A):2270-2281.
• [53]Croston GE, Kerrigan LA, Lira LM, Marshak DR, Kadonaga JT. Sequence-specific antirepression of histone H1-mediated inhibition of basal RNA polymerase II transcription. Science. 1991; 251(4994):643-649.
• [54]Schwarz PM, Hansen JC. Formation and stability of higher order chromatin structures. Contributions of the histone octamer. J Biol Chem. 1994; 269(23):16284-16289.
• [55]Marheineke K, Krude T. Nucleosome assembly activity and intracellular localization of human caf-1 changes during the cell division cycle. J Biol Chem. 1998; 273(24):15279-15286.
• [56]Dong A, Liu Z, Zhu Y, Yu F, Li Z, Cao K et al.. Interacting proteins and differences in nuclear transport reveal specific functions for the NAP1 family proteins in plants. Plant Physiol. 2005; 138(3):1446-1456.
• [57]Nagata K, Saito S, Okuwaki M, Kawase H, Furuya A, Kusano A et al.. Cellular localization and expression of template-activating factor I in different cell types. Exp Cell Res. 1998; 240(2):274-281.
• [58]Leung JW, Leitch A, Wood JL, Shaw-Smith C, Metcalfe K, Bicknell LS et al.. Set nuclear oncogene associates with microcephalin/mcph1 and regulates chromosome condensation. J Biol Chem. 2011; 286(24):21393-21400.
• [59]Kadota S, Nagata K. Silencing of ifn-stimulated gene transcription is regulated by histone h1 and its chaperone TAF-I. Nucleic Acids Res. 2014.
• [60]Kato K, Miyaji-Yamaguchi M, Okuwaki M, Nagata K. Histone acetylation-independent transcription stimulation by a histone chaperone. Nucleic Acids Res. 2007; 35(3):705-715.
• [61]Karetsou Z, Martic G, Sflomos G, Papamarcaki T. The histone chaperone set/taf-ibeta interacts functionally with the CREB-binding protein. Biochem Biophys Res Commun. 2005; 335(2):322-327.
• [62]Shikama N, Chan HM, Krstic-Demonacos M, Smith L, Lee CW, Cairns W et al.. Functional interaction between nucleosome assembly proteins and p300/CREB-binding protein family coactivators. Mol Cell Biol. 2000; 20(23):8933-8943.
• [63]Okada M, Jeang KT. Differential requirements for activation of integrated and transiently transfected human T-cell leukemia virus type 1 long terminal repeat. J Virol. 2002; 76(24):12564-12573.
• [64]Lemasson I, Polakowski NJ, Laybourn PJ, Nyborg JK. Tax-dependent displacement of nucleosomes during transcriptional activation of human T-cell leukemia virus type 1. J Biol Chem. 2006; 281(19):13075-13082.
• [65]Hebbar PB, Archer TK. Altered histone h1 stoichiometry and an absence of nucleosome positioning on transfected DNA. J Biol Chem. 2008; 283(8):4595-4601.
• [66]Keck KM, Pemberton LF. Histone chaperones link histone nuclear import and chromatin assembly. Biochim Biophys Acta. 2013; 1819(3–4):277-289.
• [67]Sandaltzopoulos R, Blank T, Becker PB. Transcriptional repression by nucleosomes but not H1 in reconstituted preblastoderm drosophila chromatin. EMBO J. 1994; 13(2):373-379.
• [68]Telese F, Bruni P, Donizetti A, Gianni D, D’Ambrosio C, Scaloni A et al.. Transcription regulation by the adaptor protein fe65 and the nucleosome assembly factor set. EMBO Rep. 2005; 6(1):77-82.
• [69]Matsumoto K, Nagata K, Miyaji-Yamaguchi M, Kikuchi A, Tsujimoto M. Sperm chromatin decondensation by template activating factor i through direct interaction with basic proteins. Mol Cell Biol. 1999; 19(10):6940-6952.
• [70]Karetsou Z, Martic G, Tavoulari S, Christoforidis S, Wilm M, Gruss C et al.. Prothymosin alpha associates with the oncoprotein set and is involved in chromatin decondensation. FEBS Lett. 2004; 577(3):496-500.
• [71]Kibler KV, Jeang KT. CREB/ATF-dependent repression of cyclin a by human T-cell leukemia virus type 1 Tax protein. J Virol. 2001; 75(5):2161-2173.
• [72]Rousset R, Desbois C, Bantignies F, Jalinot P. Effects on NF-kappa B/p105 processing of the interaction between the HTLV-1 transactivator tax and the proteasome. Nature. 1996; 381(6580):328-331.
• [73]Rehtanz M, Schmidt HM, Warthorst U, Steger G. Direct interaction between nucleosome assembly protein 1 and the papillomavirus e2 proteins involved in activation of transcription. Mol Cell Biol. 2004; 24(5):2153-2168.
• [74]Wang S, Frappier L. Nucleosome assembly proteins bind to Epstein–Barr virus nuclear antigen 1 and affect its functions in DNA replication and transcriptional activation. J Virol. 2009; 83(22):11704-11714.
• [75]Zhao LJ, Giam CZ. Interaction of the human t-cell lymphotrophic virus type 1 (HTLV-1) transcriptional activator Tax with cellular factors that bind specifically to the 21-base-pair repeats in the HTLV-1 enhancer. Proc Natl Acad Sci USA. 1991; 88(24):11445-11449.
• [76]Lopez DI, Mick JE, Nyborg JK. Purification of creb to apparent homogeneity: removal of truncation products and contaminating nucleic acid. Protein Expr Purif. 2007; 55(2):406-418.
• [77]Franklin AA, Kubik MF, Uittenbogaard MN, Brauweiler A, Utaisincharoen P, Matthews MA et al.. Transactivation by the human t-cell leukemia virus tax protein is mediated through enhanced binding of activating transcription factor-2 (ATF-2) and cAMP element-binding protein (CREB). J Biol Chem. 1993; 268(28):21225-21231.
• [78]Fyodorov DV, Kadonaga JT. Chromatin assembly in vitro with purified recombinant ACF and NAP-1. Methods Enzymol. 2003; 371:499-515.
• [79]Lu X, Hansen JC. Identification of specific functional subdomains within the linker histone H10 C-terminal domain. J Biol Chem. 2004; 279(10):8701-8707.
• [80]Hieb AR, D’Arcy S, Kramer MA, White AE, Luger K. Fluorescence strategies for high-throughput quantification of protein interactions. Nucleic Acids Res. 2012; 40(5):e33.
• [81]Luger K, Rechsteiner TJ, Flaus AJ, Waye MM, Richmond TJ. Characterization of nucleosome core particles containing histone proteins made in bacteria. J Mol Biol. 1997; 272(3):301-311.
• [82]Dynan WS. DNAse I footprinting as an assay for mammalian gene regulatory proteins. Genet Eng. 1987; 9:75-87.
• [83]Lal A, Navarro F, Maher CA, Maliszewski LE, Yan N, O’Day E et al.. Mir-24 inhibits cell proliferation by targeting e2f2, myc, and other cell-cycle genes via binding to “seedless” 3′utr microrna recognition elements. Mol Cell. 2009; 35(5):610-625.
• [84]Carruthers LM, Bednar J, Woodcock CL, Hansen JC. Linker histones stabilize the intrinsic salt-dependent folding of nucleosomal arrays: mechanistic ramifications for higher-order chromatin folding. Biochemistry. 1998; 37(42):14776-14787.
• [85]Luger K, Rechsteiner TJ, Richmond TJ. Preparation of nucleosome core particle from recombinant histones. Methods Enzymol. 1999; 304:3-19.
• [86]Scoggin KE, Ulloa A, Nyborg JK. The oncoprotein Tax binds the SRC-1-interacting domain of CBP/p300 to mediate transcriptional activation. Mol Cell Biol. 2001; 21(16):5520-5530.
• [87]Giebler HA, Loring JE, van Orden K, Colgin MA, Garrus JE, Escudero KW et al.. Anchoring of CREB binding protein to the human T-cell leukemia virus type 1 promoter: a molecular mechanism of tax transactivation. Mol Cell Biol. 1997; 17(9):5156-5164.