Transcription apparatus: A dancer on a rope

Wang Yaolai; Liu Feng

doi:10.7498/aps.69.20201631

Abstract

Laws of physics govern all forms of matter movement. However, lives, which are composed of chemical elements which everyone is familiar with, are largely beyond physical description available. This is because the construction of life is not the same as that of general matters, rendering it unknown how physics laws are utilized. In this paper, we present our thinking on the transcriptional apparatus (TA). The TA is a huge molecular machine acting to sense regulatory signals and initiate transcripts at right time and with right rate. The operation of the TA is fundamental to almost all forms of lives. Although great progress has been made in recent years, one often has to face contradictory conclusions from different studies. Additionally, the studies of transcription are divided into several fields, and different fields are increasingly separate and independent. Focusing on eukaryotic transcription, in this review we briefly describe major advances in various fields and present new conflicting view points. Although the structural studies have revealed the main components and architecture of the TA, it is still unclear how the Mediator complex transmits signals from activators to the core transcriptional machinery at the promoter. It is believed that the Mediator functions to recruit RNA polymerase II onto the promoter and promote the entry into transcriptional elongation, which fails to explain how the signal transduction is achieved. On the other hand, the allostery effect of the Mediator allows for signal transmission but is not supported by structural study. It is reported that enhancers, especially supper enhancers, act to recruit activators via forming a so-called liquid drop and phase separation. By contrast, it is suggested that enhancers should cooperate delicately to orchestrate transcription. Results on the kinetics of protein-promoter interaction also contrast with each other, leading to a paradox called “transcriptional clock”. It is then concluded that proteins interact frequently and transiently with promoters and different proteins interact with the promoter at different stages of transcriptional progression. The phenomenon of transcriptional burst questions how the cellular signaling is achieved through such a noisy manner. While the burst frequency or size, or both are potentially modulated by transcriptional activators, more evidence supports the mode of frequency modulation. The technical difficulties in investigating the mechanism of transcription include 1) structural characterization of flexible and/or unstable proteins or protein complexes, 2) measurement of intermolecular kinetics, 3) tracking of single molecule movement, and 4) lack of methodology in theoretical research. We further propose a research strategy based on the ensemble statistical method, and introduce a model for how the TA dynamically operates. The model may act as a benchmark for further investigations. The operating mechanism of the TA should reflect an optimal use of physics laws as a result of long-term biological evolution.

Keywords:

Authors and contacts

Wang Yaolai¹,
Liu Feng²

1.
School of Science, Jiangnan University, Wuxi 214122, China
2.
Department of Physics, Nanjing University, Nanjing 210093, China

Corresponding author: Wang Yaolai, yaolaiwang@jiangnan.edu.cn ; Liu Feng, fliu@nju.edu.cn

Funds: Project supported by the National Natural Science Foundation of China (Grant Nos. 11804123, 11831015, 11874209)

FullText HTML : translate this paragraph

References

[1]	Brivanlou A H, Darnell Jr J E 2002 Science 295 813 Google Scholar
[2]	Blake W J, Kaern M, Cantor C R, Collins J J 2003 Nature 422 633 Google Scholar
[3]	Gregor T, Tank D W, Wieschaus E F, Bialek W 2007 Cell 130 153 Google Scholar
[4]	Weake V M, Workman J L 2010 Nat. Rev. Genet. 11 426 Google Scholar
[5]	Fuda N J, Ardehali M B, Lis J T 2009 Nature 461 186 Google Scholar
[6]	Senecal A, Munsky B, Proux F, Ly N, Braye F E, Zimmer C, Mueller F, Darzacq X 2014 Cell Rep. 8 75 Google Scholar
[7]	Koonin E V 2015 Biol. Direct. 10 52 Google Scholar
[8]	Bussard A E 2005 EMBO Rep. 6 691 Google Scholar
[9]	Crick F 1970 Nature 227 561 Google Scholar
[10]	Crick F H 1958 Symp. Soc. Exp. Biol. 12 138
[11]	Hurwitz J 2005 J. Biol. Chem. 280 42477 Google Scholar
[12]	Young R A 1991 Annu. Rev. Biochem. 60 689 Google Scholar
[13]	Lis J T 2019 Nat. Struct. Mol. Biol. 26 777 Google Scholar
[14]	Krishnamurthy S, Hampsey M 2009 Curr. Biol. 19 R153 Google Scholar
[15]	Kornberg R D 2007 Proc. Natl. Acad. Sci. U.S.A. 104 12955 Google Scholar
[16]	Wang D, Bushnell D A, Westover K D, Kaplan C D, Kornberg R D 2006 Cell 127 941 Google Scholar
[17]	Westover K D, Bushnell D A, Kornberg R D 2004 Science 303 1014 Google Scholar
[18]	Hahn S 2004 Nat. Struct. Mol. Biol. 11 394 Google Scholar
[19]	Thomas M C, Chiang C M 2006 Crit. Rev. Biochem. Mol. Biol. 41 105 Google Scholar
[20]	Cramer P, Bushnell D A, Kornberg R D 2001 Science 292 1863 Google Scholar
[21]	Cramer P, Bushnell D A, Fu J, Gnatt A L, Maier-Davis B, Thompson N E, Burgess R R, Edwards A M, David P R, Kornberg R D 2000 Science 288 640 Google Scholar
[22]	Fu J, Gnatt A L, Bushnell D A, Jensen G J, Thompson N E, Burgess R R, David P R, Kornberg R D 1999 Cell 98 799 Google Scholar
[23]	Meredith G D, Chang W H, Li Y, Bushnell D A, Darst S A, Kornberg R D 1996 J. Mol. Biol. 258 413 Google Scholar
[24]	Murakami K, Tsai K L, Kalisman N, Bushnell D A, Asturias F J, Kornberg R D 2015 Proc. Natl. Acad. Sci. U.S.A. 112 13543 Google Scholar
[25]	Fazal F M, Meng C A, Murakami K, Kornberg R D, Block S M 2015 Nature 525 274 Google Scholar
[26]	Schweikhard V, Meng C, Murakami K, Kaplan C D, Kornberg R D, Block S M 2014 Proc. Natl. Acad. Sci. U.S.A. 111 6642 Google Scholar
[27]	Murakami K, Elmlund H, Kalisman N, Bushnell D A, Adams C M, Azubel M, Elmlund D, Levi-Kalisman Y, Liu X, Gibbons B J, Levitt M, Kornberg R D 2013 Science 342 1238724 Google Scholar
[28]	Liu X, Bushnell D A, Kornberg R D 2013 Biochim. Biophys. Acta. 1829 2 Google Scholar
[29]	Liu X, Bushnell D A, Wang D, Calero G, Kornberg R D 2010 Science 327 206 Google Scholar
[30]	Kelleher R J, 3 rd, Flanagan P M, Kornberg R D 1990 Cell 61 1209 Google Scholar
[31]	Flanagan P M, Kelleher R J, 3 rd, Sayre M H, Tschochner H, Kornberg R D 1991 Nature 350 436 Google Scholar
[32]	Kim Y J, Bjorklund S, Li Y, Sayre M H, Kornberg R D 1994 Cell 77 599 Google Scholar
[33]	Kim T K, Shiekhattar R 2015 Cell 162 948 Google Scholar
[34]	Haberle V, Lenhard B 2016 Semin. Cell Dev. Biol. 57 11 Google Scholar
[35]	Robinson P J, Trnka M J, Bushnell D A, Davis R E, Mattei P J, Burlingame A L, Kornberg R D 2016 Cell 166 1411 Google Scholar
[36]	Robinson P J, Trnka M J, Pellarin R, Greenberg C H, Bushnell D A, Davis R, Burlingame A L, Sali A, Kornberg R D 2015 eLife 4 e08719 Google Scholar
[37]	Plaschka C, Lariviere L, Wenzeck L, Seizl M, Hemann M, Tegunov D, Petrotchenko E V, Borchers C H, Baumeister W, Herzog F, Villa E, Cramer P 2015 Nature 518 376 Google Scholar
[38]	Poss Z C, Ebmeier C C, Taatjes D J 2013 Crit. Rev. Biochem. Mol. Biol. 48 575 Google Scholar
[39]	Casamassimi A, Napoli C 2007 Biochimie 89 1439 Google Scholar
[40]	Takagi Y, Kornberg R D 2006 J. Biol. Chem. 281 80 Google Scholar
[41]	Kornberg R D 2005 Trends Biochem. Sci. 30 235 Google Scholar
[42]	Kornberg R D 2005 Trends Biochem. Sci. 30 221 Google Scholar
[43]	Guo Y E, Manteiga J C, Henninger J E, Sabari B R, Dall’Agnese A, Hannett N M, Spille J H, Afeyan L K, Zamudio A V, Shrinivas K, Abraham B J, Boija A, Decker T M, Rimel J K, Fant C B, Lee T I, Cisse I I, Sharp P A, Taatjes D J, Young R A 2019 Nature 572 543 Google Scholar
[44]	Wang Y, Liu F, Wang W 2012 Sci. Rep. 2 422 Google Scholar
[45]	Meyer K D, Lin S C, Bernecky C, Gao Y, Taatjes D J 2010 Nat. Struct. Mol. Biol. 17 753 Google Scholar
[46]	Natoli G, Saccani S, Bosisio D, Marazzi I 2005 Nat. Immunol. 6 439 Google Scholar
[47]	Levine M, Cattoglio C, Tjian R 2014 Cell 157 13 Google Scholar
[48]	Wang Y M, Austin R H, Cox E C 2006 Phys. Rev. Lett. 97 048302 Google Scholar
[49]	Elf J, Li G W, Xie X S 2007 Science 316 1191 Google Scholar
[50]	Whyte W A, Orlando D A, Hnisz D, Abraham B J, Lin C Y, Kagey M H, Rahl P B, Lee T I, Young R A 2013 Cell 153 307 Google Scholar
[51]	Spitz F, Furlong E E M 2012 Nat. Rev. Genet. 13 613 Google Scholar
[52]	Hahn S 2018 Cell 175 1723 Google Scholar
[53]	Boija A, Klein I A, Sabari B R, Dall’Agnese A, Coffey E L, Zamudio A V, Li C H, Shrinivas K, Manteiga J C, Hannett N M, Abraham B J, Afeyan L K, Guo Y E, Rimel J K, Fant C B, Schuijers J, Lee T I, Taatjes D J, Young R A 2018 Cell 175 1842 Google Scholar
[54]	Sabari B R, Dall’Agnese A, Boija A, Klein I A, Coffey E L, Shrinivas K, Abraham B J, Hannett N M, Zamudio A V, Manteiga J C, Li C H, Guo Y E, Day D S, Schuijers J, Vasile E, Malik S, Hnisz D, Lee T I, Cisse I I, Roeder R G, Sharp P A, Chakraborty A K, Young R A 2018 Science 361 eaar3958 Google Scholar
[55]	Rippe K 2000 Biochemistry 39 2131 Google Scholar
[56]	Atkinson M R, Pattaramanon N, Ninfa A J 2002 Mol. Microbiol. 46 1247 Google Scholar
[57]	Lilja A E, Jenssen J R, Kahn J D 2004 J. Mol. Biol. 342 467 Google Scholar
[58]	Huo Y X, Tian Z X, Rappas M, Wen J, Chen Y C, You C H, Zhang X, Buck M, Wang Y P, Kolb A 2006 Mol. Microbiol. 59 168 Google Scholar
[59]	Wang Y, Liu F, Wang W 2016 Nucleic Acids Res. 44 10530 Google Scholar
[60]	Elison G L, Xue Y, Song R, Acar M 2018 Cell Rep. 25 737 Google Scholar
[61]	Donovan B T, Huynh A, Ball D A, Patel H P, Poirier M G, Larson D R, Ferguson M L, Lenstra T L 2019 EMBO J. 38 e100809 Google Scholar
[62]	Karpova T S, Kim M J, Spriet C, Nalley K, Stasevich T J, Kherrouche Z, Heliot L, McNally J G 2008 Science 319 466 Google Scholar
[63]	Métivier R, Reid G, Gannon F 2006 EMBO Rep. 7 161 Google Scholar
[64]	Métivier R, Penot G, Hubner M R, Reid G, Brand H, Kos M, Gannon F 2003 Cell 115 751 Google Scholar
[65]	Kang Z, Pirskanen A, Janne O A, Palvimo J J 2002 J. Biol. Chem. 277 48366 Google Scholar
[66]	Liu Y, Xia X, Fondell J D, Yen P M 2006 Mol. Endocrinol. 20 483 Google Scholar
[67]	Shang Y, Hu X, DiRenzo J, Lazar M A, Brown M 2000 Cell 103 843 Google Scholar
[68]	Becker M, Baumann C, John S, Walker D A, Vigneron M, McNally J G, Hager G L 2002 EMBO Rep. 3 1188 Google Scholar
[69]	Darzacq X, Shav-Tal Y, de Turris V, Brody Y, Shenoy S M, Phair R D, Singer R H 2007 Nat. Struct. Mol. Biol. 14 796 Google Scholar
[70]	Johnson T A, Elbi C, Parekh B S, Hager G L, John S 2008 Mol. Biol. Cell 19 3308 Google Scholar
[71]	Catez F, Ueda T, Bustin M 2006 Nat. Struct. Mol. Biol. 13 305 Google Scholar
[72]	Bosisio D, Marazzi I, Agresti A, Shimizu N, Bianchi M E, Natoli G 2006 EMBO J. 25 798 Google Scholar
[73]	Reid G, Hubner M R, Métivier R, Brand H, Denger S, Manu D, Beaudouin J, Ellenberg J, Gannon F 2003 Mol. Cell 11 695 Google Scholar
[74]	Hager G L, McNally J G, Misteli T 2009 Mol. Cell 35 741 Google Scholar
[75]	Reid G, Gallais R, Métivier R 2009 Int. J. Biochem. Cell Biol. 41 155 Google Scholar
[76]	Wang Y, Liu F, Li J, Wang W 2014 J. R. Soc. Interface 11 20140253 Google Scholar
[77]	Lemaire V, Lee C F, Lei J, Métivier R, Glass L 2006 Phys. Rev. Lett. 96 198102 Google Scholar
[78]	Krasnov A N, Mazina M Y, Nikolenko J V, Vorobyeva N E 2016 Cell Biosci. 6 15 Google Scholar
[79]	Gourse R L, Landick R 2012 Cell 148 635 Google Scholar
[80]	Lenstra T L, Rodriguez J, Chen H, Larson D R 2016 Annu. Rev. Biophys. 45 25 Google Scholar
[81]	Raj A, van Oudenaarden A 2008 Cell 135 216 Google Scholar
[82]	Hocine S, Raymond P, Zenklusen D, Chao J A, Singer R H 2013 Nat. Methods 10 119 Google Scholar
[83]	Lim F, Peabody D S 2002 Nucleic Acids Res. 30 4138 Google Scholar
[84]	Chubb J R, Trcek T, Shenoy S M, Singer R H 2006 Curr. Biol. 16 1018 Google Scholar
[85]	Bertrand E, Chartrand P, Schaefer M, Shenoy S M, Singer R H, Long R M 1998 Mol. Cell 2 437 Google Scholar
[86]	Tantale K, Mueller F, Kozulic-Pirher A, Lesne A, Victor J M, Robert M C, Capozi S, Chouaib R, Backer V, Mateos-Langerak J, Darzacq X, Zimmer C, Basyuk E, Bertrand E 2016 Nat. Commun. 7 12248 Google Scholar
[87]	Fukaya T, Lim B, Levine M 2016 Cell 166 358 Google Scholar
[88]	Corrigan A M, Tunnacliffe E, Cannon D, Chubb J R 2016 eLife 5 e13051 Google Scholar
[89]	Chong S, Chen C, Ge H, Xie X S 2014 Cell 158 314 Google Scholar
[90]	Suter D M, Molina N, Gatfield D, Schneider K, Schibler U, Naef F 2011 Science 332 472 Google Scholar
[91]	Tripathi T, Chowdhury D 2008 EPL 84 68004 Google Scholar
[92]	Golding I, Paulsson J, Zawilski S M, Cox E C 2005 Cell 123 1025 Google Scholar
[93]	Raj A, Peskin C S, Tranchina D, Vargas D Y, Tyagi S 2006 PLoS Biol. 4 e309 Google Scholar
[94]	Sanchez A, Golding I 2013 Science 342 1188 Google Scholar
[95]	Wang Y, Ni T, Wang W, Liu F 2019 Biol. Rev. 94 248 Google Scholar
[96]	Tunnacliffe E, Chubb J R 2020 Trends Genet. 36 288 Google Scholar
[97]	Yao J 2017 J. Mol. Biol. 429 14 Google Scholar
[98]	Nicolas D, Phillips N E, Naef F 2017 Mol. Biosyst. 13 1280 Google Scholar
[99]	Hnisz D, Shrinivas K, Young R A, Chakraborty A K, Sharp P A 2017 Cell 169 13 Google Scholar
[100]	Chubb J R 2017 Wiley Interdiscip. Rev.-Dev. Biol. 6 e284 Google Scholar
[101]	Bressloff P C 2017 J. Phys. A-Math. Theor. 50 133001 Google Scholar
[102]	Reinius B, Sandberg R 2015 Nat. Rev. Genet. 16 653 Google Scholar
[103]	Munsky B, Neuert G 2015 Phys. Biol. 12 045004 Google Scholar
[104]	Munsky B, Fox Z, Neuert G 2015 Methods 85 12 Google Scholar
[105]	Boeger H, Shelansky R, Patel H, Brown C R 2015 Genes 6 469 Google Scholar
[106]	Skupsky R, Burnett J C, Foley J E, Schaffer D V, Arkin A P 2010 PLoS Comput. Biol. 6 e1000952 Google Scholar
[107]	Dar R D, Razooky B S, Singh A, Trimeloni T V, McCollum J M, Cox C D, Simpson M L, Weinberger L S 2012 Proc. Natl. Acad. Sci. U.S.A. 109 17454 Google Scholar
[108]	Molina N, Suter D M, Cannavo R, Zoller B, Gotic I, Naef F 2013 Proc. Natl. Acad. Sci. U.S.A. 110 20563 Google Scholar
[109]	Corrigan A M, Chubb J R 2014 Curr. Biol. 24 205 Google Scholar
[110]	Giri R, Papadopoulos D K, Posadas D M, Potluri H K, Tomancak P, Mani M, Carthew R W 2020 eLife 9 e53638 Google Scholar
[111]	Lammers N C, Galstyan V, Reimer A, Medin S A, Wiggins C H, Garcia H G 2020 Proc. Natl. Acad. Sci. U.S.A. 117 836 Google Scholar
[112]	Tian X, Huang B, Zhang X P, Lu M, Liu F, Onuchic J N, Wang W 2017 Proc. Natl. Acad. Sci. U.S.A. 114 5337 Google Scholar
[113]	Ko M S 1992 Bioessays 14 341 Google Scholar
[114]	Sanchez A, Choubey S, Kondev J 2013 Methods 62 13 Google Scholar
[115]	Peccoud J, Ycart B 1995 Theor. Popul. 48 222 Google Scholar
[116]	Pedraza J M, Paulsson J 2008 Science 319 339 Google Scholar
[117]	Freeman B C, Yamamoto K R 2002 Science 296 2232 Google Scholar
[118]	Stavreva D A, Muller W G, Hager G L, Smith C L, McNally J G 2004 Mol. Cell. Biol. 24 2682 Google Scholar
[119]	Wang Y, Qi J, Shao J, Tang X Q 2020 Biology 9 339 Google Scholar

Cited By

图 1 转录机器的基本架构和信号转导

Figure 1. Configuration and signaling of the transcriptional apparatus.

DownLoad: Full-Size Img PowerPoint

图 2 媒介子工作原理的两大模型　(a) 相分离模型; (b) 变构模型

Figure 2. Two models of how the Mediator complex operates: (a) The Mediator acts to nucleate the flexible CTDs of Pol IIs, with the efficiency of Pol II assembly elevated; (b) an enhancer-bound activator induces allostery in the Mediator, resulting in a facilitated circumstance for transcription initiation.

DownLoad: Full-Size Img PowerPoint

图 3 增强子工作原理的两种模型　(a) 液滴模型; (b) 分工协作模型

Figure 3. Two models of how the enhancers function: (a) In the phase separation model, enhancers recruit transcriptional activators that further recruit various coactivators and the transcriptional apparatus via low-affinity disordered regions; (b) every enhancer plays a unique role and different enhancers cooperate to orchestrate transcription regulation. Shown is an example of regulatory mode at the glnAp2 promoter.

DownLoad: Full-Size Img PowerPoint

图 4 人pS 2基因启动子的“转录钟”

Figure 4. Transcriptional clock of the human pS 2 promoter.

DownLoad: Full-Size Img PowerPoint

图 5 转录爆发^[95]

Figure 5. Transcriptional burst^[95].

DownLoad: Full-Size Img PowerPoint

图 6 转录机器的理想化模型^[44]

Figure 6. Ideal model for how the transcriptional apparatus operates^[44].

DownLoad: Full-Size Img PowerPoint

[1]	Brivanlou A H, Darnell Jr J E 2002 Science 295 813 Google Scholar
[2]	Blake W J, Kaern M, Cantor C R, Collins J J 2003 Nature 422 633 Google Scholar
[3]	Gregor T, Tank D W, Wieschaus E F, Bialek W 2007 Cell 130 153 Google Scholar
[4]	Weake V M, Workman J L 2010 Nat. Rev. Genet. 11 426 Google Scholar
[5]	Fuda N J, Ardehali M B, Lis J T 2009 Nature 461 186 Google Scholar
[6]	Senecal A, Munsky B, Proux F, Ly N, Braye F E, Zimmer C, Mueller F, Darzacq X 2014 Cell Rep. 8 75 Google Scholar
[7]	Koonin E V 2015 Biol. Direct. 10 52 Google Scholar
[8]	Bussard A E 2005 EMBO Rep. 6 691 Google Scholar
[9]	Crick F 1970 Nature 227 561 Google Scholar
[10]	Crick F H 1958 Symp. Soc. Exp. Biol. 12 138
[11]	Hurwitz J 2005 J. Biol. Chem. 280 42477 Google Scholar
[12]	Young R A 1991 Annu. Rev. Biochem. 60 689 Google Scholar
[13]	Lis J T 2019 Nat. Struct. Mol. Biol. 26 777 Google Scholar
[14]	Krishnamurthy S, Hampsey M 2009 Curr. Biol. 19 R153 Google Scholar
[15]	Kornberg R D 2007 Proc. Natl. Acad. Sci. U.S.A. 104 12955 Google Scholar
[16]	Wang D, Bushnell D A, Westover K D, Kaplan C D, Kornberg R D 2006 Cell 127 941 Google Scholar
[17]	Westover K D, Bushnell D A, Kornberg R D 2004 Science 303 1014 Google Scholar
[18]	Hahn S 2004 Nat. Struct. Mol. Biol. 11 394 Google Scholar
[19]	Thomas M C, Chiang C M 2006 Crit. Rev. Biochem. Mol. Biol. 41 105 Google Scholar
[20]	Cramer P, Bushnell D A, Kornberg R D 2001 Science 292 1863 Google Scholar
[21]	Cramer P, Bushnell D A, Fu J, Gnatt A L, Maier-Davis B, Thompson N E, Burgess R R, Edwards A M, David P R, Kornberg R D 2000 Science 288 640 Google Scholar
[22]	Fu J, Gnatt A L, Bushnell D A, Jensen G J, Thompson N E, Burgess R R, David P R, Kornberg R D 1999 Cell 98 799 Google Scholar
[23]	Meredith G D, Chang W H, Li Y, Bushnell D A, Darst S A, Kornberg R D 1996 J. Mol. Biol. 258 413 Google Scholar
[24]	Murakami K, Tsai K L, Kalisman N, Bushnell D A, Asturias F J, Kornberg R D 2015 Proc. Natl. Acad. Sci. U.S.A. 112 13543 Google Scholar
[25]	Fazal F M, Meng C A, Murakami K, Kornberg R D, Block S M 2015 Nature 525 274 Google Scholar
[26]	Schweikhard V, Meng C, Murakami K, Kaplan C D, Kornberg R D, Block S M 2014 Proc. Natl. Acad. Sci. U.S.A. 111 6642 Google Scholar
[27]	Murakami K, Elmlund H, Kalisman N, Bushnell D A, Adams C M, Azubel M, Elmlund D, Levi-Kalisman Y, Liu X, Gibbons B J, Levitt M, Kornberg R D 2013 Science 342 1238724 Google Scholar
[28]	Liu X, Bushnell D A, Kornberg R D 2013 Biochim. Biophys. Acta. 1829 2 Google Scholar
[29]	Liu X, Bushnell D A, Wang D, Calero G, Kornberg R D 2010 Science 327 206 Google Scholar
[30]	Kelleher R J, 3 rd, Flanagan P M, Kornberg R D 1990 Cell 61 1209 Google Scholar
[31]	Flanagan P M, Kelleher R J, 3 rd, Sayre M H, Tschochner H, Kornberg R D 1991 Nature 350 436 Google Scholar
[32]	Kim Y J, Bjorklund S, Li Y, Sayre M H, Kornberg R D 1994 Cell 77 599 Google Scholar
[33]	Kim T K, Shiekhattar R 2015 Cell 162 948 Google Scholar
[34]	Haberle V, Lenhard B 2016 Semin. Cell Dev. Biol. 57 11 Google Scholar
[35]	Robinson P J, Trnka M J, Bushnell D A, Davis R E, Mattei P J, Burlingame A L, Kornberg R D 2016 Cell 166 1411 Google Scholar
[36]	Robinson P J, Trnka M J, Pellarin R, Greenberg C H, Bushnell D A, Davis R, Burlingame A L, Sali A, Kornberg R D 2015 eLife 4 e08719 Google Scholar
[37]	Plaschka C, Lariviere L, Wenzeck L, Seizl M, Hemann M, Tegunov D, Petrotchenko E V, Borchers C H, Baumeister W, Herzog F, Villa E, Cramer P 2015 Nature 518 376 Google Scholar
[38]	Poss Z C, Ebmeier C C, Taatjes D J 2013 Crit. Rev. Biochem. Mol. Biol. 48 575 Google Scholar
[39]	Casamassimi A, Napoli C 2007 Biochimie 89 1439 Google Scholar
[40]	Takagi Y, Kornberg R D 2006 J. Biol. Chem. 281 80 Google Scholar
[41]	Kornberg R D 2005 Trends Biochem. Sci. 30 235 Google Scholar
[42]	Kornberg R D 2005 Trends Biochem. Sci. 30 221 Google Scholar
[43]	Guo Y E, Manteiga J C, Henninger J E, Sabari B R, Dall’Agnese A, Hannett N M, Spille J H, Afeyan L K, Zamudio A V, Shrinivas K, Abraham B J, Boija A, Decker T M, Rimel J K, Fant C B, Lee T I, Cisse I I, Sharp P A, Taatjes D J, Young R A 2019 Nature 572 543 Google Scholar
[44]	Wang Y, Liu F, Wang W 2012 Sci. Rep. 2 422 Google Scholar
[45]	Meyer K D, Lin S C, Bernecky C, Gao Y, Taatjes D J 2010 Nat. Struct. Mol. Biol. 17 753 Google Scholar
[46]	Natoli G, Saccani S, Bosisio D, Marazzi I 2005 Nat. Immunol. 6 439 Google Scholar
[47]	Levine M, Cattoglio C, Tjian R 2014 Cell 157 13 Google Scholar
[48]	Wang Y M, Austin R H, Cox E C 2006 Phys. Rev. Lett. 97 048302 Google Scholar
[49]	Elf J, Li G W, Xie X S 2007 Science 316 1191 Google Scholar
[50]	Whyte W A, Orlando D A, Hnisz D, Abraham B J, Lin C Y, Kagey M H, Rahl P B, Lee T I, Young R A 2013 Cell 153 307 Google Scholar
[51]	Spitz F, Furlong E E M 2012 Nat. Rev. Genet. 13 613 Google Scholar
[52]	Hahn S 2018 Cell 175 1723 Google Scholar
[53]	Boija A, Klein I A, Sabari B R, Dall’Agnese A, Coffey E L, Zamudio A V, Li C H, Shrinivas K, Manteiga J C, Hannett N M, Abraham B J, Afeyan L K, Guo Y E, Rimel J K, Fant C B, Schuijers J, Lee T I, Taatjes D J, Young R A 2018 Cell 175 1842 Google Scholar
[54]	Sabari B R, Dall’Agnese A, Boija A, Klein I A, Coffey E L, Shrinivas K, Abraham B J, Hannett N M, Zamudio A V, Manteiga J C, Li C H, Guo Y E, Day D S, Schuijers J, Vasile E, Malik S, Hnisz D, Lee T I, Cisse I I, Roeder R G, Sharp P A, Chakraborty A K, Young R A 2018 Science 361 eaar3958 Google Scholar
[55]	Rippe K 2000 Biochemistry 39 2131 Google Scholar
[56]	Atkinson M R, Pattaramanon N, Ninfa A J 2002 Mol. Microbiol. 46 1247 Google Scholar
[57]	Lilja A E, Jenssen J R, Kahn J D 2004 J. Mol. Biol. 342 467 Google Scholar
[58]	Huo Y X, Tian Z X, Rappas M, Wen J, Chen Y C, You C H, Zhang X, Buck M, Wang Y P, Kolb A 2006 Mol. Microbiol. 59 168 Google Scholar
[59]	Wang Y, Liu F, Wang W 2016 Nucleic Acids Res. 44 10530 Google Scholar
[60]	Elison G L, Xue Y, Song R, Acar M 2018 Cell Rep. 25 737 Google Scholar
[61]	Donovan B T, Huynh A, Ball D A, Patel H P, Poirier M G, Larson D R, Ferguson M L, Lenstra T L 2019 EMBO J. 38 e100809 Google Scholar
[62]	Karpova T S, Kim M J, Spriet C, Nalley K, Stasevich T J, Kherrouche Z, Heliot L, McNally J G 2008 Science 319 466 Google Scholar
[63]	Métivier R, Reid G, Gannon F 2006 EMBO Rep. 7 161 Google Scholar
[64]	Métivier R, Penot G, Hubner M R, Reid G, Brand H, Kos M, Gannon F 2003 Cell 115 751 Google Scholar
[65]	Kang Z, Pirskanen A, Janne O A, Palvimo J J 2002 J. Biol. Chem. 277 48366 Google Scholar
[66]	Liu Y, Xia X, Fondell J D, Yen P M 2006 Mol. Endocrinol. 20 483 Google Scholar
[67]	Shang Y, Hu X, DiRenzo J, Lazar M A, Brown M 2000 Cell 103 843 Google Scholar
[68]	Becker M, Baumann C, John S, Walker D A, Vigneron M, McNally J G, Hager G L 2002 EMBO Rep. 3 1188 Google Scholar
[69]	Darzacq X, Shav-Tal Y, de Turris V, Brody Y, Shenoy S M, Phair R D, Singer R H 2007 Nat. Struct. Mol. Biol. 14 796 Google Scholar
[70]	Johnson T A, Elbi C, Parekh B S, Hager G L, John S 2008 Mol. Biol. Cell 19 3308 Google Scholar
[71]	Catez F, Ueda T, Bustin M 2006 Nat. Struct. Mol. Biol. 13 305 Google Scholar
[72]	Bosisio D, Marazzi I, Agresti A, Shimizu N, Bianchi M E, Natoli G 2006 EMBO J. 25 798 Google Scholar
[73]	Reid G, Hubner M R, Métivier R, Brand H, Denger S, Manu D, Beaudouin J, Ellenberg J, Gannon F 2003 Mol. Cell 11 695 Google Scholar
[74]	Hager G L, McNally J G, Misteli T 2009 Mol. Cell 35 741 Google Scholar
[75]	Reid G, Gallais R, Métivier R 2009 Int. J. Biochem. Cell Biol. 41 155 Google Scholar
[76]	Wang Y, Liu F, Li J, Wang W 2014 J. R. Soc. Interface 11 20140253 Google Scholar
[77]	Lemaire V, Lee C F, Lei J, Métivier R, Glass L 2006 Phys. Rev. Lett. 96 198102 Google Scholar
[78]	Krasnov A N, Mazina M Y, Nikolenko J V, Vorobyeva N E 2016 Cell Biosci. 6 15 Google Scholar
[79]	Gourse R L, Landick R 2012 Cell 148 635 Google Scholar
[80]	Lenstra T L, Rodriguez J, Chen H, Larson D R 2016 Annu. Rev. Biophys. 45 25 Google Scholar
[81]	Raj A, van Oudenaarden A 2008 Cell 135 216 Google Scholar
[82]	Hocine S, Raymond P, Zenklusen D, Chao J A, Singer R H 2013 Nat. Methods 10 119 Google Scholar
[83]	Lim F, Peabody D S 2002 Nucleic Acids Res. 30 4138 Google Scholar
[84]	Chubb J R, Trcek T, Shenoy S M, Singer R H 2006 Curr. Biol. 16 1018 Google Scholar
[85]	Bertrand E, Chartrand P, Schaefer M, Shenoy S M, Singer R H, Long R M 1998 Mol. Cell 2 437 Google Scholar
[86]	Tantale K, Mueller F, Kozulic-Pirher A, Lesne A, Victor J M, Robert M C, Capozi S, Chouaib R, Backer V, Mateos-Langerak J, Darzacq X, Zimmer C, Basyuk E, Bertrand E 2016 Nat. Commun. 7 12248 Google Scholar
[87]	Fukaya T, Lim B, Levine M 2016 Cell 166 358 Google Scholar
[88]	Corrigan A M, Tunnacliffe E, Cannon D, Chubb J R 2016 eLife 5 e13051 Google Scholar
[89]	Chong S, Chen C, Ge H, Xie X S 2014 Cell 158 314 Google Scholar
[90]	Suter D M, Molina N, Gatfield D, Schneider K, Schibler U, Naef F 2011 Science 332 472 Google Scholar
[91]	Tripathi T, Chowdhury D 2008 EPL 84 68004 Google Scholar
[92]	Golding I, Paulsson J, Zawilski S M, Cox E C 2005 Cell 123 1025 Google Scholar
[93]	Raj A, Peskin C S, Tranchina D, Vargas D Y, Tyagi S 2006 PLoS Biol. 4 e309 Google Scholar
[94]	Sanchez A, Golding I 2013 Science 342 1188 Google Scholar
[95]	Wang Y, Ni T, Wang W, Liu F 2019 Biol. Rev. 94 248 Google Scholar
[96]	Tunnacliffe E, Chubb J R 2020 Trends Genet. 36 288 Google Scholar
[97]	Yao J 2017 J. Mol. Biol. 429 14 Google Scholar
[98]	Nicolas D, Phillips N E, Naef F 2017 Mol. Biosyst. 13 1280 Google Scholar
[99]	Hnisz D, Shrinivas K, Young R A, Chakraborty A K, Sharp P A 2017 Cell 169 13 Google Scholar
[100]	Chubb J R 2017 Wiley Interdiscip. Rev.-Dev. Biol. 6 e284 Google Scholar
[101]	Bressloff P C 2017 J. Phys. A-Math. Theor. 50 133001 Google Scholar
[102]	Reinius B, Sandberg R 2015 Nat. Rev. Genet. 16 653 Google Scholar
[103]	Munsky B, Neuert G 2015 Phys. Biol. 12 045004 Google Scholar
[104]	Munsky B, Fox Z, Neuert G 2015 Methods 85 12 Google Scholar
[105]	Boeger H, Shelansky R, Patel H, Brown C R 2015 Genes 6 469 Google Scholar
[106]	Skupsky R, Burnett J C, Foley J E, Schaffer D V, Arkin A P 2010 PLoS Comput. Biol. 6 e1000952 Google Scholar
[107]	Dar R D, Razooky B S, Singh A, Trimeloni T V, McCollum J M, Cox C D, Simpson M L, Weinberger L S 2012 Proc. Natl. Acad. Sci. U.S.A. 109 17454 Google Scholar
[108]	Molina N, Suter D M, Cannavo R, Zoller B, Gotic I, Naef F 2013 Proc. Natl. Acad. Sci. U.S.A. 110 20563 Google Scholar
[109]	Corrigan A M, Chubb J R 2014 Curr. Biol. 24 205 Google Scholar
[110]	Giri R, Papadopoulos D K, Posadas D M, Potluri H K, Tomancak P, Mani M, Carthew R W 2020 eLife 9 e53638 Google Scholar
[111]	Lammers N C, Galstyan V, Reimer A, Medin S A, Wiggins C H, Garcia H G 2020 Proc. Natl. Acad. Sci. U.S.A. 117 836 Google Scholar
[112]	Tian X, Huang B, Zhang X P, Lu M, Liu F, Onuchic J N, Wang W 2017 Proc. Natl. Acad. Sci. U.S.A. 114 5337 Google Scholar
[113]	Ko M S 1992 Bioessays 14 341 Google Scholar
[114]	Sanchez A, Choubey S, Kondev J 2013 Methods 62 13 Google Scholar
[115]	Peccoud J, Ycart B 1995 Theor. Popul. 48 222 Google Scholar
[116]	Pedraza J M, Paulsson J 2008 Science 319 339 Google Scholar
[117]	Freeman B C, Yamamoto K R 2002 Science 296 2232 Google Scholar
[118]	Stavreva D A, Muller W G, Hager G L, Smith C L, McNally J G 2004 Mol. Cell. Biol. 24 2682 Google Scholar
[119]	Wang Y, Qi J, Shao J, Tang X Q 2020 Biology 9 339 Google Scholar

[1]	Li Duo-Duo, Zhang Song. Molecular structures in the non-adiabatic relaxaiton processes of excited states of pentafluoropyridine. Acta Physica Sinica, 2024, 73(4): 043101. doi: 10.7498/aps.73.20231570
[2]	Chen Hong-Mei, Li Shi-Wei, Li Kai-Jing, Zhang Zhi-Yong, Chen Hao, Wang Ting-Ting. Molecules structure and viscosity relationship of nematic liquid crystal and BPNN-QSAR model. Acta Physica Sinica, 2024, 73(6): 066101. doi: 10.7498/aps.73.20231763
[3]	Hao Dan-Hui, Kong Fan-Jie, Jiang Gang. Structure and potential energy function of PuNO molecules. Acta Physica Sinica, 2015, 64(15): 153103. doi: 10.7498/aps.64.153103
[4]	Jiao Shang-Bin, Ren Chao, Huang Wei-Chao, Liang Yan-Ming. Parameter-induced stochastic resonance in multi-frequency weak signal detection with stable noise. Acta Physica Sinica, 2013, 62(21): 210501. doi: 10.7498/aps.62.210501
[5]	Peng Hao, Zhong Su-Chuan, Tu Zhe, Ma Hong. Stochastic resonance of over-damped bistable system driven by chirp signal and Gaussian white noise. Acta Physica Sinica, 2013, 62(8): 080501. doi: 10.7498/aps.62.080501
[6]	Huang Duo-Hui, Wang Fan-Hou, Wan Ming-Jie, Jiang Gang. SnS molecular structure and properties under external electric field. Acta Physica Sinica, 2013, 62(1): 013104. doi: 10.7498/aps.62.013104
[7]	Xu Yong-Qiang, Peng Wei-Cheng, Wu Hua. Structures and potential energy functions of the ground states of YH,YD,YT molecules. Acta Physica Sinica, 2012, 61(4): 043105. doi: 10.7498/aps.61.043105
[8]	Zhang Mao-Ping, Zhong Wei-Rong, Ai Bao-Quan. Thermal rectification of asymmetric double-stranded molecular structure. Acta Physica Sinica, 2011, 60(6): 060511. doi: 10.7498/aps.60.060511
[9]	Chen Jun, Meng Da-Qiao, Du Ji-Guang, Jiang Gang, Gao Tao, Zhu Zheng-He. Molecular structures and molecular spectra for plutonium oxides. Acta Physica Sinica, 2010, 59(3): 1658-1664. doi: 10.7498/aps.59.1658
[10]	Han Xiao-Qin, Jiang Li-Juan, Liu Yu-Fang. Structure and potential energy function of MgB and MgB2(1A1). Acta Physica Sinica, 2010, 59(7): 4542-4546. doi: 10.7498/aps.59.4542
[11]	Zheng Yu-Jun, Zhang Zhao-Yu, Zhang Xi-Zhong. Similarity of high-order cumulants for single molecule kinetics. Acta Physica Sinica, 2009, 58(12): 8194-8198. doi: 10.7498/aps.58.8194
[12]	Yang Ze-Jin, Gao Qing-He, Guo Yun-Dong, Cheng Xin-Lu, Zhu Zheng-He, Yang Xiang-Dong. The structure and potential energy function of SiOH and HSiO. Acta Physica Sinica, 2008, 57(3): 1587-1591. doi: 10.7498/aps.57.1587
[13]	Yang Ze-Jin, Gao Qing-He, Guo Yun-Dong, Cheng Xin-Lu, Zhu Zheng-He, Yang Xiang-Dong. The structure and potential energy function of AlOH(CS，X1A′). Acta Physica Sinica, 2008, 57(3): 1582-1586. doi: 10.7498/aps.57.1582
[14]	Kong Fan-Jie, Du Ji-Guang, Jiang Gang. The structure and potential energy function of PdCO molecule. Acta Physica Sinica, 2008, 57(1): 149-154. doi: 10.7498/aps.57.149
[15]	Yang Ze-Jin, Gao Qing-He, Guo Yun-Dong, Cheng Xin-Lu, Zhu Zheng-He, Yang Xiang-Dong. The structure and potential energy function of LiO2(C2V，X2A2) molecule. Acta Physica Sinica, 2007, 56(10): 5723-5726. doi: 10.7498/aps.56.5723
[16]	Xu Mei, Wang Rong-Kai, Linghu Rong-Feng, Yang Xiang-Dong. Structures and potential energy functions of the ground states of BeH, BeD, BeT molecules. Acta Physica Sinica, 2007, 56(2): 769-773. doi: 10.7498/aps.56.769
[17]	Yan Shi-Ying. The molecular structure and potential energy function of the ground state of BH2 molecule. Acta Physica Sinica, 2006, 55(7): 3408-3412. doi: 10.7498/aps.55.3408
[18]	Xiong Bi-Tao, Meng Da-Qiao, Xue Wei-Dong, Zhu Zheng-He, Jiang Gang, Wang Hong-Yan. The thermodynamical calculations of uranium-water vapor system. Acta Physica Sinica, 2003, 52(7): 1617-1623. doi: 10.7498/aps.52.1617
[19]	Xue Wei-Dong, Wang Hong-Yan, Zhu Zheng-He, Zhang Guang-Feng, Zhou Le-Xi, Chen Chang-An, Sun Ying. . Acta Physica Sinica, 2002, 51(11): 2480-2484. doi: 10.7498/aps.51.2480
[20]	LUO DE-LI, SUN YING, LIU XIAO-YA, JIANG GANG, MENG DA-QIAO, ZHU ZHENG-HE. STRUCTURE AND POTENTIAL ENERGY FUNCTION INVESTIGATION ON UH AND UH2 MOLECULES. Acta Physica Sinica, 2001, 50(10): 1896-1901. doi: 10.7498/aps.50.1896

Catalog

Vol. 69, Issue 24 - 2020-12-20

Metrics

Abstract views: 6474
PDF Downloads: 181
Cited By: 0

姓名
邮箱
手机号码
标题
留言内容
验证码

Search

Article

留言板