Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Abbreviations
- AGO:
-
Argonaute
- ATM:
-
Ataxia telangiectasia mutated
- ChIP-seq:
-
Chromatin immunoprecipitation sequencing
- CTD:
-
C-terminal domain
- DDR:
-
DNA damage response
- DNA-PK:
-
DNA-dependent protein kinase
- DSB:
-
DNA double strand break
- DSIF:
-
DRB sensitivity-inducing factor
- FACT:
-
Facilitates chromatin transcription
- H3K4me3:
-
H3 trimethylated at lysine 4
- HSE:
-
Heat shock element
- HSF1:
-
Heat shock factor 1
- HSP:
-
Heat shock protein
- m7G:
-
7-methyl guanosine
- NELF:
-
Negative elongation factor
- NTP:
-
Nucleoside triphosphate
- NURF:
-
Nucleosome remodeling factor
- PARP:
-
Poly(ADP)-ribose polymerase
- PI3:
-
Phosphoinositide-3
- Pol II:
-
RNA polymerase II
- P-TEFb:
-
Positive transcription elongation factor b
- RNA-seq:
-
RNA sequencing
- SWI/SNF:
-
Switch/Sucrose non-fermentable
- TBP:
-
TATA box binding protein
- TOP2B:
-
Topoisomerase IIβ
- TRIM28:
-
Tripartite motif-containing 28
- Trl:
-
Trithorax-like
- TSS:
-
Transcription start site
References
Bunch H (2017) RNA polymerase II pausing and transcriptional regulation of the HSP70 expression. Eur J Cell Biol 96:739–745
Roeder RG (2019) 50+ years of eukaryotic transcription: an expanding universe of factors and mechanisms. Nat Struct Mol Biol 26:783–791
Bunch H (2018) Gene regulation of mammalian long non-coding RNA. Mol Gen Genet 293:1–15
Cramer P (2004) Structure and function of RNA polymerase II. Adv Protein Chem 67:1–42
Hahn S (2004) Structure and mechanism of the RNA polymerase II transcription machinery. Nat Struct Mol Biol 11:394–403
Phatnani HP, Greenleaf AL (2006) Phosphorylation and functions of the RNA polymerase II CTD. Genes Dev 20:2922–2936
Buratowski S (2003) The CTD code. Nat Struct Biol 10:679–680
Itzen F, Greifenberg AK, Bosken CA, Geyer M (2014) Brd4 activates P-TEFb for RNA polymerase II CTD phosphorylation. Nucleic Acids Res 42:7577–7590
Sawadogo M, Roeder RG (1985) Interaction of a gene-specific transcription factor with the adenovirus major late promoter upstream of the TATA box region. Cell 43:165–175
Bunch H et al (2014) TRIM28 regulates RNA polymerase II promoter-proximal pausing and pause release. Nat Struct Mol Biol 21:876–883
Ebmeier CC, Taatjes DJ (2010) Activator-mediator binding regulates mediator-cofactor interactions. Proc Natl Acad Sci U S A 107:11283–11288
Poss ZC, Ebmeier CC, Taatjes DJ (2013) The mediator complex and transcription regulation. Crit Rev Biochem Mol Biol 48:575–608
Shandilya J, Roberts SG (2012) The transcription cycle in eukaryotes: from productive initiation to RNA polymerase II recycling. Biochim Biophys Acta 1819:391–400
Rasmussen EB, Lis JT (1993) In vivo transcriptional pausing and cap formation on three Drosophila heat shock genes. Proc Natl Acad Sci U S A 90:7923–7927
Rahl PB et al (2010) c-Myc regulates transcriptional pause release. Cell 141:432–445
McClure WR (1980) Rate-limiting steps in RNA chain initiation. Proc Natl Acad Sci U S A 77:5634–5638
Henderson KL et al (2017) Mechanism of transcription initiation and promoter escape by E. coli RNA polymerase. Proc Natl Acad Sci U S A 114:E3032–E3040
Nechaev S et al (2010) Global analysis of short RNAs reveals widespread promoter-proximal stalling and arrest of Pol II in Drosophila. Science 327:335–338
Lee C et al (2008) NELF and GAGA factor are linked to promoter-proximal pausing at many genes in Drosophila. Mol Cell Biol 28:3290–3300
Gilmour DS (2009) Promoter proximal pausing on genes in metazoans. Chromosoma 118:1–10
Rougvie AE, Lis JT (1988) The RNA polymerase II molecule at the 5′ end of the uninduced hsp70 gene of D. melanogaster is transcriptionally engaged. Cell 54:795–804
Gilmour DS, Lis JT (1986) RNA polymerase II interacts with the promoter region of the noninduced hsp70 gene in Drosophila melanogaster cells. Mol Cell Biol 6:3984–3989
Gilchrist DA et al (2008) NELF-mediated stalling of Pol II can enhance gene expression by blocking promoter-proximal nucleosome assembly. Genes Dev 22:1921–1933
Wu CH et al (2003) NELF and DSIF cause promoter proximal pausing on the hsp70 promoter in Drosophila. Genes Dev 17:1402–1414
Yamaguchi Y et al (1999) NELF, a multisubunit complex containing RD, cooperates with DSIF to repress RNA polymerase II elongation. Cell 97:41–51
Vos SM, Farnung L, Urlaub H, Cramer P (2018) Structure of paused transcription complex Pol II-DSIF-NELF. Nature 560:601–606
Wada T et al (1998) DSIF, a novel transcription elongation factor that regulates RNA polymerase II processivity, is composed of human Spt4 and Spt5 homologs. Genes Dev 12:343–356
Szlachta K et al (2018) Alternative DNA secondary structure formation affects RNA polymerase II promoter-proximal pausing in human. Genome Biol 19:89
Jishage M et al (2012) Transcriptional regulation by Pol II(G) involving mediator and competitive interactions of Gdown1 and TFIIF with Pol II. Mol Cell 45:51–63
Ma J, Bai L, Wang MD (2013) Transcription under torsion. Science 340:1580–1583
Ma J et al (2019) Transcription factor regulation of RNA polymerase’s torque generation capacity. Proc Natl Acad Sci U S A 116:2583–2588
Liu X, Kraus WL, Bai X (2015) Ready, pause, go: regulation of RNA polymerase II pausing and release by cellular signaling pathways. Trends Biochem Sci 40:516–525
Bunch H et al (2015) Transcriptional elongation requires DNA break-induced signalling. Nat Commun 6:10191
Adelman K, Lis JT (2012) Promoter-proximal pausing of RNA polymerase II: emerging roles in metazoans. Nat Rev Genet 13:720–731
Core L, Adelman K (2019) Promoter-proximal pausing of RNA polymerase II: a nexus of gene regulation. Genes Dev 33:960–982
Nilson KA et al (2015) THZ1 reveals roles for Cdk7 in co-transcriptional capping and pausing. Mol Cell 59:576–587
Ebmeier CC et al (2017) Human TFIIH kinase CDK7 regulates transcription-associated chromatin modifications. Cell Rep 20:1173–1186
Sun J, Li R (2010) Human negative elongation factor activates transcription and regulates alternative transcription initiation. J Biol Chem 285:6443–6452
Bunch H (2016) Role of genome guardian proteins in transcriptional elongation. FEBS Lett 590:1064–1075
Madabhushi R et al (2015) Activity-induced DNA breaks govern the expression of neuronal early-response genes. Cell 161:1592–1605
Bunch H et al (2016) RNA polymerase II promoter-proximal pausing in mammalian long non-coding genes. Genomics 108:64–77
Kainz M, Roberts JW (1995) Kinetics of RNA polymerase initiation and pausing at the lambda late gene promoter in vivo. J Mol Biol 254:808–814
Liu X, Jiang H, Gu Z, Roberts JW (2013) High-resolution view of bacteriophage lambda gene expression by ribosome profiling. Proc Natl Acad Sci U S A 110:11928–11933
Petushkov I, Esyunina D, Kulbachinskiy A (2017) Possible roles of sigma-dependent RNA polymerase pausing in transcription regulation. RNA Biol 14:1678–1682
Grayhack EJ, Yang XJ, Lau LF, Roberts JW (1985) Phage lambda gene Q antiterminator recognizes RNA polymerase near the promoter and accelerates it through a pause site. Cell 42:259–269
Zhu J, Liu M, Liu X, Dong Z (2018) RNA polymerase II activity revealed by GRO-seq and pNET-seq in Arabidopsis. Nature plants 4:1112–1123
Hetzel J, Duttke SH, Benner C, Chory J (2016) Nascent RNA sequencing reveals distinct features in plant transcription. Proc Natl Acad Sci U S A 113:12316–12321
Yu X, Martin PGP, Michaels SD (2019) BORDER proteins protect expression of neighboring genes by promoting 3’ Pol II pausing in plants. Nat Commun 10:4359
Peterlin BM, Price DH (2006) Controlling the elongation phase of transcription with P-TEFb. Mol Cell 23:297–305
Yamada T et al (2006) P-TEFb-mediated phosphorylation of hSpt5 C-terminal repeats is critical for processive transcription elongation. Mol Cell 21:227–237
Fujinaga K et al (2004) Dynamics of human immunodeficiency virus transcription: P-TEFb phosphorylates RD and dissociates negative effectors from the transactivation response element. Mol Cell Biol 24:787–795
Byun JS et al (2012) ELL facilitates RNA polymerase II pause site entry and release. Nat Commun 3:633
Liang K et al (2018) Targeting Processive transcription elongation via SEC disruption for MYC-induced Cancer therapy. Cell 175:766–779 e717
Bunch H, Calderwood SK (2015) TRIM28 as a novel transcriptional elongation factor. BMC Mol Biol 16:14
Benjamin LR, Gilmour DS (1998) Nucleosomes are not necessary for promoter-proximal pausing in vitro on the Drosophila hsp70 promoter. Nucleic Acids Res 26:1051–1055
Petesch SJ, Lis JT (2008) Rapid, transcription-independent loss of nucleosomes over a large chromatin domain at Hsp70 loci. Cell 134:74–84
Zobeck KL, Buckley MS, Zipfel WR, Lis JT (2010) Recruitment timing and dynamics of transcription factors at the Hsp70 loci in living cells. Mol Cell 40:965–975
Corey LL, Weirich CS, Benjamin IJ, Kingston RE (2003) Localized recruitment of a chromatin-remodeling activity by an activator in vivo drives transcriptional elongation. Genes Dev 17:1392–1401
de La Serna IL et al (2000) Mammalian SWI-SNF complexes contribute to activation of the hsp70 gene. Mol Cell Biol 20:2839–2851
Chen B, Retzlaff M, Roos T, Frydman J (2011) Cellular strategies of protein quality control. Cold Spring Harb Perspect Biol 3:a004374
Hammerer-Lercher A et al (2001) Hypoxia induces heat shock protein expression in human coronary artery bypass grafts. Cardiovasc Res 50:115–124
Hentze N, Le Breton L, Wiesner J, Kempf G, Mayer MP (2016) Molecular mechanism of thermosensory function of human heat shock transcription factor Hsf1. elife 5:e11576
Vihervaara A, Sistonen L (2014) HSF1 at a glance. J Cell Sci 127:261–266
Ritossa F (1962) A new puffing pattern induced by temperature shock and DNP in drosophila. Experientia 18:571–573
Lis JT, Neckameyer W, Dubensky R, Costlow N (1981) Cloning and characterization of nine heat-shock-induced mRNAs of Drosophila melanogaster. Gene 15:67–80
Moran L et al (1979) Physical map of two D. melanogaster DNA segments containing sequences coding for the 70,000 dalton heat shock protein. Cell 17:1–8
Werner F, Grohmann D (2011) Evolution of multisubunit RNA polymerases in the three domains of life. Nat Rev Microbiol 9:85–98
Kapanidis AN et al (2006) Initial transcription by RNA polymerase proceeds through a DNA-scrunching mechanism. Science 314:1144–1147
Winkelman JT, Gourse RL (2017) Open complex DNA scrunching: a key to transcription start site selection and promoter escape. BioEssays News Rev Mol Cell Dev Biol 39:1600193
Porrua O, Libri D (2015) Transcription termination and the control of the transcriptome: why, where and how to stop. Nat Rev Mol Cell Biol 16:190–202
Proudfoot NJ (2016) Transcriptional termination in mammals: stopping the RNA polymerase II juggernaut. Science 352:aad9926
Larochelle M et al (2018) Common mechanism of transcription termination at coding and noncoding RNA genes in fission yeast. Nat Commun 9:4364
Ping YH, Rana TM (2001) DSIF and NELF interact with RNA polymerase II elongation complex and HIV-1 Tat stimulates P-TEFb-mediated phosphorylation of RNA polymerase II and DSIF during transcription elongation. J Biol Chem 276:12951–12958
Li J et al (2013) Kinetic competition between elongation rate and binding of NELF controls promoter-proximal pausing. Mol Cell 50:711–722
Muse GW et al (2007) RNA polymerase is poised for activation across the genome. Nat Genet 39:1507–1511
Gressel S, Schwalb B, Cramer P (2019) The pause-initiation limit restricts transcription activation in human cells. Nat Commun 10:3603
Samarakkody A et al (2015) RNA polymerase II pausing can be retained or acquired during activation of genes involved in the epithelial to mesenchymal transition. Nucleic Acids Res 43:3938–3949
Bunch H, Calderwood SK (2015) TRIM28 as a novel transcriptional elongation factor. BMC Mol Biol 16:14
Jimeno-Gonzalez S, Ceballos-Chavez M, Reyes JC (2015) A positioned +1 nucleosome enhances promoter-proximal pausing. Nucleic Acids Res 43:3068–3078
Petesch SJ, Lis JT (2012) Overcoming the nucleosome barrier during transcript elongation. Trends Genet 28:285–294
Teves SS, Henikoff S (2011) Heat shock reduces stalled RNA polymerase II and nucleosome turnover genome-wide. Genes Dev 25:2387–2397
Tettey TT et al (2019) A role for FACT in RNA polymerase II promoter-proximal pausing. Cell Rep 27:3770–3779 e3777
Levine M (2011) Paused RNA polymerase II as a developmental checkpoint. Cell 145:502–511
Ohtsuki S, Levine M (1998) GAGA mediates the enhancer blocking activity of the eve promoter in the Drosophila embryo. Genes Dev 12:3325–3330
Tsai SY, Chang YL, Swamy KB, Chiang RL, Huang DH (2016) GAGA factor, a positive regulator of global gene expression, modulates transcriptional pausing and organization of upstream nucleosomes. Epigenetics Chromatin 9:32
Kusch T, Mei A, Nguyen C (2014) Histone H3 lysine 4 trimethylation regulates cotranscriptional H2A variant exchange by Tip60 complexes to maximize gene expression. Proc Natl Acad Sci U S A 111:4850–4855
Cernilogar FM et al (2011) Chromatin-associated RNA interference components contribute to transcriptional regulation in Drosophila. Nature 480:391–395
Buckley MS, Kwak H, Zipfel WR, Lis JT (2014) Kinetics of promoter Pol II on Hsp70 reveal stable pausing and key insights into its regulation. Genes Dev 28:14–19
Calderwood SK, Murshid A (2017) Molecular chaperone accumulation in cancer and decrease in Alzheimer’s disease: the potential roles of HSF1. Front Neurosci 11:192
Witkin SS, Kanninen TT, Sisti G (2017) The role of Hsp70 in the regulation of autophagy in gametogenesis, pregnancy, and parturition. Adv Anat Embryol Cell Biol 222:117–127
Zou J, Guo Y, Guettouche T, Smith DF, Voellmy R (1998) Repression of heat shock transcription factor HSF1 activation by HSP90 (HSP90 complex) that forms a stress-sensitive complex with HSF1. Cell 94:471–480
Lis JT, Mason P, Peng J, Price DH, Werner J (2000) P-TEFb kinase recruitment and function at heat shock loci. Genes Dev 14:792–803
Yoon YJ et al (2011) KRIBB11 inhibits HSP70 synthesis through inhibition of heat shock factor 1 function by impairing the recruitment of positive transcription elongation factor b to the hsp70 promoter. J Biol Chem 286:1737–1747
Yuan CX, Gurley WB (2000) Potential targets for HSF1 within the preinitiation complex. Cell Stress Chaperones 5:229–242
Sullivan EK, Weirich CS, Guyon JR, Sif S, Kingston RE (2001) Transcriptional activation domains of human heat shock factor 1 recruit human SWI/SNF. Mol Cell Biol 21:5826–5837
Fujimoto M et al (2017) The HSF1-PARP13-PARP1 complex facilitates DNA repair and promotes mammary tumorigenesis. Nat Commun 8:1638
Stephanou A, Latchman DS (2011) Transcriptional modulation of heat-shock protein gene expression. Biochem Res Int 2011:238601
Mazina MY, Nikolenko YV, Krasnov AN, Vorobyeva NE (2016) SWI/SNF protein complexes participate in the initiation and elongation stages of drosophila hsp70 gene transcription. Genetika 52:164–169
Murawska M, Hassler M, Renkawitz-Pohl R, Ladurner A, Brehm A (2011) Stress-induced PARP activation mediates recruitment of Drosophila Mi-2 to promote heat shock gene expression. PLoS Genet 7:e1002206
Pinnola A, Naumova N, Shah M, Tulin AV (2007) Nucleosomal core histones mediate dynamic regulation of poly(ADP-ribose) polymerase 1 protein binding to chromatin and induction of its enzymatic activity. J Biol Chem 282:32511–32519
Thomas C et al (2019) Hit and run versus long-term activation of PARP-1 by its different domains fine-tunes nuclear processes. Proc Natl Acad Sci U S A 116:9941–9946
Haffner MC et al (2010) Androgen-induced TOP2B-mediated double-strand breaks and prostate cancer gene rearrangements. Nat Genet 42:668–675
Ju BG et al (2006) A topoisomerase IIbeta-mediated dsDNA break required for regulated transcription. Science 312:1798–1802
Williamson LM, Lees-Miller SP (2011) Estrogen receptor alpha-mediated transcription induces cell cycle-dependent DNA double-strand breaks. Carcinogenesis 32:279–285
Pommier Y, Sun Y, Huang SN, Nitiss JL (2016) Roles of eukaryotic topoisomerases in transcription, replication and genomic stability. Nat Rev Mol Cell Biol 17:703–721
White D et al (2012) The ATM substrate KAP1 controls DNA repair in heterochromatin: regulation by HP1 proteins and serine 473/824 phosphorylation. Mol Cancer Res 10:401–414
Mondal N et al (2003) Elongation by RNA polymerase II on chromatin templates requires topoisomerase activity. Nucleic Acids Res 31:5016–5024
Liu LF, Wang JC (1987) Supercoiling of the DNA template during transcription. Proc Natl Acad Sci U S A 84:7024–7027
Crisona NJ, Strick TR, Bensimon D, Croquette V, Cozzarelli NR (2000) Preferential relaxation of positively supercoiled DNA by E. coli topoisomerase IV in single-molecule and ensemble measurements. Genes Dev 14:2881–2892
Dellino GI et al (2019) Release of paused RNA polymerase II at specific loci favors DNA double-strand-break formation and promotes cancer translocations. Nat Genet 51:1011–1023
Nitiss JL (2009) DNA topoisomerase II and its growing repertoire of biological functions. Nat Rev Cancer 9:327–337
McKinnon PJ (2016) Topoisomerases and the regulation of neural function. Nat Rev Neurosci 17:673–679
Morimoto S et al (2019) Type II DNA topoisomerases cause spontaneous double-strand breaks in genomic DNA. Genes 10:868
Sasanuma H et al (2018) BRCA1 ensures genome integrity by eliminating estrogen-induced pathological topoisomerase II-DNA complexes. Proc Natl Acad Sci U S A 115:E10642–E10651
Brown SA, Imbalzano AN, Kingston RE (1996) Activator-dependent regulation of transcriptional pausing on nucleosomal templates. Genes Dev 10:1479–1490
Gilchrist DA et al (2010) Pausing of RNA polymerase II disrupts DNA-specified nucleosome organization to enable precise gene regulation. Cell 143:540–551
Pan XY et al (2016) Heat shock factor 1 mediates latent HIV reactivation. Sci Rep 6:26294
Kim S, Gross DS (2013) Mediator recruitment to heat shock genes requires dual Hsf1 activation domains and mediator tail subunits Med15 and Med16. J Biol Chem 288:12197–12213
Allen BL, Taatjes DJ (2015) The mediator complex: a central integrator of transcription. Nat Rev Mol Cell Biol 16:155–166
Takahashi H et al (2011) Human mediator subunit MED26 functions as a docking site for transcription elongation factors. Cell 146:92–104
Yang Z et al (2005) Recruitment of P-TEFb for stimulation of transcriptional elongation by the bromodomain protein Brd4. Mol Cell 19:535–545
Badenhorst P, Voas M, Rebay I, Wu C (2002) Biological functions of the ISWI chromatin remodeling complex NURF. Genes Dev 16:3186–3198
Chen M, Beck WT (1995) DNA topoisomerase II expression, stability, and phosphorylation in two VM-26-resistant human leukemic CEM sublines. Oncol Res 7:103–111
Kondapi AK, Padmaja G, Satyanarayana N, Mukhopadyaya R, Reitz MS (2005) A biochemical analysis of topoisomerase II alpha and beta kinase activity found in HIV-1 infected cells and virus. Arch Biochem Biophys 441:41–55
Kimura K, Nozaki N, Enomoto T, Tanaka M, Kikuchi A (1996) Analysis of M phase-specific phosphorylation of DNA topoisomerase II. J Biol Chem 271:21439–21445
Nakazawa N, Arakawa O, Ebe M, Yanagida M (2019) Casein kinase II-dependent phosphorylation of DNA topoisomerase II suppresses the effect of a catalytic topo II inhibitor, ICRF-193, in fission yeast. J Biol Chem 294:3772–3782
Ackerman P, Glover CV, Osheroff N (1985) Phosphorylation of DNA topoisomerase II by casein kinase II: modulation of eukaryotic topoisomerase II activity in vitro. Proc Natl Acad Sci U S A 82:3164–3168
Sahyoun N et al (1986) Protein kinase C phosphorylates topoisomerase II: topoisomerase activation and its possible role in phorbol ester-induced differentiation of HL-60 cells. Proc Natl Acad Sci U S A 83:1603–1607
Acknowledgements
I appreciate S.K. Calderwood at Beth Israel Deaconess Medical Center and D.J. Taatjes at the University of Colorado for their support to study the transcriptional regulation at HSP70. I thank previous and current Bunch lab members in the School of Applied Biosciences at Kyungpook National University (KNU), J. Christ, John, and D.Y. Bunch for their support and loving encouragement. I also thank International Edit for the help with proofreading manuscript. This study was supported by a grant from Korea National Foundation (NRF) (NRF-2017R1D1A1B03030548 and NRF-2020R1F1A1060996) to H.B.
Disclosure of Interest
There is no conflict of interest for the enclosed review article.
Ethical Approval for Studies Involving Humans
This article does not contain any studies with human participants performed by any of the authors.
Ethical Approval for Studies Involving Animals
This article does not contain any studies with animals performed by any of the authors.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2021 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Bunch, H. (2021). HSF1 in RNA Polymerase II Promoter-Proximal Pausing and HSP70 Transcription. In: Asea, A.A.A., Kaur, P. (eds) Heat Shock Proteins in Inflammatory Diseases. Heat Shock Proteins, vol 22. Springer, Cham. https://doi.org/10.1007/7515_2021_38
Download citation
DOI: https://doi.org/10.1007/7515_2021_38
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-85167-5
Online ISBN: 978-3-030-85168-2
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)