Rotation manipulation of single-molecule magnetic trapping and gene transcription regulation dynamics

Zhang Zhi-Peng; Liu Shuai; Zhang Yu-Qiong; Xiong Ying; Han Wei-Jing; Chen Tong-Sheng; Wang Shuang

doi:10.7498/aps.72.20231089

Abstract

Gene transcription regulation is a key step for gene expression in all organisms and responsible for the transmission of genetic information and genome integrity. As one of the most important mechanisms in gene transcription, an RNA polymerase (RNAP) specifically interacts with and unwinds genome DNA to form a transcription bubble where a nascent RNA transcript is polymerized, taking one of the unwound DNA strands as its template. The RNAP translocates along the DNA to transcribe the whole gene by carrying the transcription bubble. In such a way, an RNAP completes its biological task of gene expression by physically acting as a molecular machinery. Thus, an RNAP molecule can be considered as a research object for physicists who are willing to uncover the mechanisms of life processes in a physical view. To achieve this, single-molecule method has been invented and used widely. As one of these methods, single-molecule magnetic trapping manipulates biological molecules by applying extension force or torque to the magnetic beads tethered through biological molecule to pre-coated glass surfaces by manipulating the position or rotation of a pair of magnets. A linear DNA molecule can be manipulated in such a way to generate plectonemes, i.e. DNA supercoils, under an extension force of 0.3 pN (1 pN = 10^–12 N), possessing the feature that the number of unwound base pairs of a supercoiled DNA can be observed by the changes in the number of supercoils reflected by the DNA extension changes. Thus, the DNA unwound by RNAP, i.e. the transcription bubble, during transcription can be observed in this way. By monitoring the kinetics of the transcription bubble in real time, this method thus allows single-molecule detection with single-base resolution and a high-throughput data collection fashion in the kinetic studies of transcription. Owing to the advantages of the manipulation of DNA supercoils with single-molecule magnetic trapping, one can mimic the mechanistic feature of DNAs in vivo and characterize the kinetics of transcription under such conditions. This method can also be combined with single-molecule fluorescence method which can be applied to studying the mechanism of transcription regulation while monitoring the behaviors of fluorescently labeled biological molecules that interact with functional RNAP molecules, providing examples for studying the mechanisms of transcription regulations in more complex systems.

Keywords:

Authors and contacts

1.
College of Biophotonics, South China Normal University, Guangzhou 510631, China
2.
Songshan Lake Materials Laboratory, Dongguan 523808, China
3.
Institute of Physics, Chinese Academy of Sciences, Beijing 100190, China

Corresponding author: Wang Shuang, shuangwang@iphy.ac.cn

Funds: Project supported by the National Natural Science Foundation of China (Grant Nos. 12004420, 32071228, 12004271, 12274308, 62135003), the Strategic Priority Research Program (B) of the Chinese Academy of Sciences, China (Grant No. XDB37000000), the Youth Innovation Promotion Association of Chinese Academy of Sciences, China (Grant No. 2021009), the Key-Area Research and Development Program of Guangdong Province, China (Grant Nos. 21202107221900001, 2022B0303040003), the Basic and Applied Basic Research Foundation of Guangdong Province, China (Grant No. 2019A1515110186).

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References

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Cited By

图 1 单分子磁镊操控技术示意图

Figure 1. Schematic for single-molecule magnetic trap.

DownLoad: Full-Size Img PowerPoint

图 2 单分子磁镊旋转操控DNA超螺旋

Figure 2. Manipulation of DNA supercoils via single-molecule magnetic trap.

DownLoad: Full-Size Img PowerPoint

图 3 单分子磁镊旋转操控方法研究转录动力学　(a) 研究方法示意图; (b) 典型转录曲线(起始(RPitc)、延伸(RDe)和终止)

Figure 3. Transcription kinetics characterized via single-molecule magnetic trap: (a) Schematic of the methodology; (b) a typical transcription trajectory showing initiation (RPitc), elongation (RDe) and termination.

DownLoad: Full-Size Img PowerPoint

图 4 单分子磁镊操控技术和单分子荧光成像技术联用方案　(a)方案示意图; (b)磁镊监测转录动力学过程; (c)单分子荧光方法同步观测RNAP、Mfd和RNA的时空分布^[68]

Figure 4. Schematic for combination of single-molecule magnetic trap and single-molecule fluorescence imaging: (a) Schematic of the assay; (b) transcription kinetics characterized via single-molecule magnetic trap; (c) simultaneous detection of RNAP, Mfd and RNA via single-molecule fluorescence assay^[68].

DownLoad: Full-Size Img PowerPoint

[1]	Watson J D, Crick F H C 1953 Nature 171 737 Google Scholar
[2]	Watson J D, Crick F H C 1953 Nature 171 964 Google Scholar
[3]	Crick F 1970 Nature 227 561 Google Scholar
[4]	Monod J, Changeux J P, Jacob F 1963 J. Mol. Biol. 6 306 Google Scholar
[5]	Monod J, Wyman J, Changeux J P 1965 J. Mol. Biol. 12 88 Google Scholar
[6]	Zhang G, Campbell E A, Minakhin L, Richter C, Severinov K, Darst S A 1999 Cell 98 811 Google Scholar
[7]	Gnatt A L, Cramer P, Fu J, Bushnell D A, Kornberg R D 2001 Science 292 1876 Google Scholar
[8]	Chen X, Yin X, Li J, Wu Z, Qi Y, Wang X, Liu W, Xu Y 2021 Science 372 eabg0635 Google Scholar
[9]	Chen X, Qi Y, Wu Z, et al. 2021 Science 372 eaba8490 Google Scholar
[10]	Huang K, Wu X X, Fang C L, et al. 2021 Science 374 1579 Google Scholar
[11]	Komissarova N, Becker J, Solter S, Kireeva M, Kashlev M 2002 Mol. Cell 10 1151 Google Scholar
[12]	Skourti-Stathaki K, Proudfoot N J, Gromak N 2011 Mol. Cell 42 794 Google Scholar
[13]	Hazelbaker D Z, Marquardt S, Wlotzka W, Buratowski S 2013 Mol. Cell 49 55 Google Scholar
[14]	Kim S, Beltran B, Irnov I, Jacobs-Wagner C 2019 Cell 179 106 Google Scholar
[15]	Abbondanzieri E A, Greenleaf W J, Shaevitz J W, Landick R, Block S M 2005 Nature 438 460 Google Scholar
[16]	Chakraborty A, Wang D, Ebright Y W, et al. 2012 Science 337 591 Google Scholar
[17]	Howan K, Smith A J, Westblade L F, Joly N, Grange W, Zorman S, Darst S A, Savery N J, Strick T R 2012 Nature 490 431 Google Scholar
[18]	Ma J, Bai L, Wang M D 2013 Science 340 1580 Google Scholar
[19]	Koh H R, Roy R, Sorokina M, Tang G Q, Nandakumar D, Patel S S, Ha T 2018 Mol. Cell 70 695 Google Scholar
[20]	Rosen G A, Baek I, Friedman L J, Joo Y J, Buratowski S, Gelles J 2020 Proc. Natl. Acad. Sci. 117 32348 Google Scholar
[21]	Neuman K C, Nagy A 2008 Nat. Methods 5 491 Google Scholar
[22]	Roy R, Hohng S, Ha T J 2008 Nat. Methods 5 507 Google Scholar
[23]	Gosse C, Croquette V 2002 Biophys. J. 82 3314 Google Scholar
[24]	Cnossen J P, Dulin D, Dekker N H 2014 Rev. Sci. Instrum. 85 103712 Google Scholar
[25]	Huhle A, Klaue D, Brutzer H, Daldrop P, Joo S, Otto O, Keyser U F, Seidel R 2015 Nat. Commun. 6 5885 Google Scholar
[26]	Ashkin A, Dziedzic J M, Bjorkholm J E, Chu S 1986 Opt. Lett. 11 288 Google Scholar
[27]	Ashkin A, Dziedzic J M 1987 Science 235 1517 Google Scholar
[28]	Neuman K C, Block S M 2004 Rev. Sci. Instrum. 75 2787 Google Scholar
[29]	Rief M, Gautel M, Oesterhelt F, Femandez J M, Gaub H E 1997 Science 276 1109 Google Scholar
[30]	Yu H, Siewny M G W, Edwards D T, Sanders A W, Perkins T T 2017 Science 355 945 Google Scholar
[31]	Jiao F, Cannon K S, Lin Y C, Gladfelter A S, Scheuring S 2020 Nat. Commu. 11 5062 Google Scholar
[32]	Ha T, Enderle T, Ogletree D F, Chemla D S, Selvin P R, Weiss S 1996 Proc. Natl. Acad. Sci. 93 6264 Google Scholar
[33]	Weiss S 1999 Science 283 1676 Google Scholar
[34]	Lerner E, Cordes T, Ingargiola A, Alhadid Y, Chung S, Michalet X, Weiss S 2018 Science 359 eaan1133 Google Scholar
[35]	Friedman L J, Chung J, Gelles J 2006 Biophys. J. 91 1023 Google Scholar
[36]	Friedman L J, Gelles J 2015 Methods 86 27 Google Scholar
[37]	Thompson M A, Lew M D, Moerner W 2012 Annu. Rev. Bioph. Biom. 41 321 Google Scholar
[38]	Betzig E, Patterson G H, Sougrat R, Lindwasser O W, Olenych S, Bonifacino J S, Davidson M W, Lippincott-Schwartz J, Hess H F 2006 Science 313 1642 Google Scholar
[39]	Bates M, Huang B, Dempsey G T, Zhuang X 2007 Science 317 1749 Google Scholar
[40]	Seol Y, Neuman K C 2017 Combined Magnetic Tweezers, Micro-mirror Total Internal Reflection Fluorescence Microscope for Single-molecule Manipulation and Visualization Single Molecule Analysis (New York: Springer) pp297–316
[41]	Fan J, Leroux-Coyau M, Savery N J, Strick T R 2016 Nature 536 234 Google Scholar
[42]	Comstock M J, Whitley K D, Jia H, Sokoloski J, Lohman T M, Ha T, Chemla Y R 2015 Science 348 352 Google Scholar
[43]	Lionnet T, Allemand J F, Revyakin A, Strick T R, Saleh O A, Bensimon D, Croquette V 2011 Cold Spring Harb. Protoc. 2012 133 Google Scholar
[44]	Smith S B, Finzi L, Bustamante C 1992 Science 258 1122 Google Scholar
[45]	Strick T R, Allemand J F, Bensimon D, Bensimon A, Croquette V 1996 Science 271 1835 Google Scholar
[46]	Chen H, Yuan G, Winardhi R S, Yao M, Popa I, Fernandez J M, Yan J 2015 J. Am. Chem. Soc. 137 3540 Google Scholar
[47]	Guo Z, Hong H, Yuan G, Qian H, Li B, Cao Y, Wang W, Wu C X, Chen H 2020 Phys. Rev. Lett. 125 198101 Google Scholar
[48]	Strick T, Allemand J F, Bensimon D, Croquette V 1998 Biophys. J. 74 2016 Google Scholar
[49]	Revyakin A, Ebright R H, Strick T R 2004 Proc. Natl. Acad. Sci. U. S. A. 101 4776 Google Scholar
[50]	Revyakin A, Ebright R H, Strick T R 2005 Nat. Methods 2 127 Google Scholar
[51]	Yu L, Winkelman J T, Pukhrambam C, Strick T R, Nickels B E, Ebright R H 2017 eLife 6 e32038 Google Scholar
[52]	Smith S B, Cui Y, Bustamante C 1996 Science 271 795 Google Scholar
[53]	Roeder R G 2019 Nat Struct. Mol. Biol. 26 783 Google Scholar
[54]	Pomerantz R T, O’Donnell M 2010 Science 327 590 Google Scholar
[55]	Merrikh H, Machón C, Grainger W H, Grossman A D, Soultanas P 2011 Nature 470 554 Google Scholar
[56]	Tomko E J, Fishburn J, Hahn S, Galburt E A 2017 Nat Struct. Mol. Biol. 24 1139 Google Scholar
[57]	Revyakin A, Liu C, Ebright R H, Strick T R 2006 Science 314 1139 Google Scholar
[58]	Kapanidis A N, Margeat E, Ho S O, Kortkhonjia E, Weiss S, Ebright R H 2006 Science 314 1144 Google Scholar
[59]	Lerner E, Chung S, Allen B L, et al. 2016 Proc. Natl. Acad. Sci. U. S. A. 113 6562 Google Scholar
[60]	Wang D, Bushnell D A, Huang X, Westover K D, Levitt M, Kornberg R D 2009 Science 324 1203 Google Scholar
[61]	Zhang Y, Han W, Wang L, Wang H, Jia Q, Chen T, Wang S, Li M 2023 J. Phys. Chem. B 127 2909 Google Scholar
[62]	Zhu C, Guo X, Dumas P, Takacs M, Abdelkareem M, Broeck A V, Saint-André C, Papai G, Crucifix C, Ortiz J, Weixlbaumer A 2022 Nat. Commun. 13 1546 Google Scholar
[63]	Ray-Soni A, Bellecourt M J, Landick R 2016 Annu. Rev. Biochem. 85 319 Google Scholar
[64]	Kim M, Vasiljeva L, Rando O J, Zhelkovsky A, Moore C, Buratowski S 2006 Mol. Cell 24 723 Google Scholar
[65]	Arndt K M, Reines D 2015 Annu. Rev. Biochem. 84 381 Google Scholar
[66]	Fazal F M, Meng C A, Murakami K, Kornberg R D, Block S M 2015 Nature 525 274 Google Scholar
[67]	Wang S, Han Z, Libri D, Porrua O, Strick T R 2019 Nat. Commun. 10 1545 Google Scholar
[68]	Klein H L, Ang K K, Arkin M R, et al. 2019 Microbial. Cell 6 65 Google Scholar
[69]	王爽, 郑海子, 赵振业, 陆越, 徐春华 2013 物理学报 62 168703 Google Scholar Wang S, Zheng H Z, Zhao Z Y, Lu Y, Xu C H 2013 Acta Phys. Sin. 62 168703 Google Scholar
[70]	Graves E T, Duboc C, Fan J, Stransky F, Leroux-Coyau M, Strick T R 2015 Nat. Struct. Mol. Biol. 22 452 Google Scholar

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