Single-molecular methodologies for the physical biology of protein machines

doi:10.1088/1674-1056/ac98a2

中国物理B ›› 2022, Vol. 31 ›› Issue (12): 128702-128702.doi: 10.1088/1674-1056/ac98a2

所属专题： TOPICAL REVIEW — Celebrating 30 Years of Chinese Physics B

Single-molecular methodologies for the physical biology of protein machines

Shuang Wang(王爽), Ying Lu(陆颖), and Ming Li(李明)^†

Beijing National Laboratory for Condensed Matter Physics, Institute of Physics, Chinese Academy of Sciences, Beijing 100190, China

收稿日期:2022-07-29 修回日期:2022-09-21 接受日期:2022-10-10 出版日期:2022-11-11 发布日期:2022-11-11
通讯作者: Ming Li E-mail:mingli@iphy.ac.cn
基金资助:
This work is supported by the National Key Research and Development Program of China (Grant No. 2019YFA0709304), the National Natural Science Foundation of China (Grant Nos. 12090051 and 12022409), the Strategic Priority Research Program of the Chinese Academy of Sciences (Grant No. XDB37000000), and the Youth Innovation Promotion Association of CAS (Grant Nos. 2021009 and Y2021003). We sincerely apologize to the authors whose work could not be included because of the scope of this review. We thank Prof. Wei Li (Institute of Physics, Chinese Academy of Sciences), Prof. Hui Li (Beijing Normal University), Dr. Jianbing Ma (Institute of Physics, Chinese Academy of Sciences) and Dr. Dongfei Ma (Songshan Lake Materials Laboratory) for their kind discussion and figure preparation.

Single-molecular methodologies for the physical biology of protein machines

Shuang Wang(王爽), Ying Lu(陆颖), and Ming Li(李明)^†

Beijing National Laboratory for Condensed Matter Physics, Institute of Physics, Chinese Academy of Sciences, Beijing 100190, China

Received:2022-07-29 Revised:2022-09-21 Accepted:2022-10-10 Online:2022-11-11 Published:2022-11-11
Contact: Ming Li E-mail:mingli@iphy.ac.cn
Supported by:
This work is supported by the National Key Research and Development Program of China (Grant No. 2019YFA0709304), the National Natural Science Foundation of China (Grant Nos. 12090051 and 12022409), the Strategic Priority Research Program of the Chinese Academy of Sciences (Grant No. XDB37000000), and the Youth Innovation Promotion Association of CAS (Grant Nos. 2021009 and Y2021003). We sincerely apologize to the authors whose work could not be included because of the scope of this review. We thank Prof. Wei Li (Institute of Physics, Chinese Academy of Sciences), Prof. Hui Li (Beijing Normal University), Dr. Jianbing Ma (Institute of Physics, Chinese Academy of Sciences) and Dr. Dongfei Ma (Songshan Lake Materials Laboratory) for their kind discussion and figure preparation.

摘要/Abstract

摘要： Physical biology is an interdisciplinary field that bridges biology with physical sciences and engineering. Single-molecule physical biology focuses on dynamics of individual biomolecules and complexes, aiming to answering basic questions about their functions and mechanisms. It takes advantages of physical methodologies to gain quantitative understanding of biological processes, often engaging precise physical measurements of reconstructed objects to avoid interference from unnecessary complications. In this review, we (i) briefly introduce concepts of single-molecule physical biology, (ii) describe extensively used single-molecule methodologies that have been developed to address key questions in two important objects of single-molecule physical biology, namely, nucleic acid-interacting proteins and membrane-interacting proteins, and (iii) show by a few successful examples how one may use single-molecule methods to deepen our understanding of protein machines.

关键词: physical biology, single-molecules, research object reconstruction, precise measurements

Abstract: Physical biology is an interdisciplinary field that bridges biology with physical sciences and engineering. Single-molecule physical biology focuses on dynamics of individual biomolecules and complexes, aiming to answering basic questions about their functions and mechanisms. It takes advantages of physical methodologies to gain quantitative understanding of biological processes, often engaging precise physical measurements of reconstructed objects to avoid interference from unnecessary complications. In this review, we (i) briefly introduce concepts of single-molecule physical biology, (ii) describe extensively used single-molecule methodologies that have been developed to address key questions in two important objects of single-molecule physical biology, namely, nucleic acid-interacting proteins and membrane-interacting proteins, and (iii) show by a few successful examples how one may use single-molecule methods to deepen our understanding of protein machines.

Key words: physical biology, single-molecules, research object reconstruction, precise measurements

中图分类号: (Single-molecule techniques)

87.80.Nj

87.14.gk (DNA) 87.64.kv (Fluorescence) 87.14.E- (Proteins)

Shuang Wang(王爽), Ying Lu(陆颖), and Ming Li(李明). Single-molecular methodologies for the physical biology of protein machines[J]. 中国物理B, 2022, 31(12): 128702-128702.

Shuang Wang(王爽), Ying Lu(陆颖), and Ming Li(李明). Single-molecular methodologies for the physical biology of protein machines[J]. Chin. Phys. B, 2022, 31(12): 128702-128702.

参考文献

[1] Finer J T, Simmons R M and Spudich J A 1994 Nature 368 113
[2] Yu H, Siewny M G W, Edwards D T, Sanders A W and Perkins T T 2017 Science 355 945
[3] Chen H, Zhu X, Cong P, Sheetz M P, Nakamura F and Yan J 2011 Biophys. J. 101 1231
[4] Chen H, Yuan G, Winardhi R S, Yao M, Popa I, Fernandez J M and Yan J 2015 J. Am. Chem. Soc. 137 3540
[5] Yuan G, Le S, Yao M, Qian H, Zhou X, Yan J and Chen H 2017 Angew. Chem. Int. Ed. 56 5490
[6] Guo Z, Hong H, Yuan G, Qian H, Li B, Cao Y, Wang W, Wu C X and Chen H 2020 Phys. Rev. Lett. 125 198101
[7] Li W, Chen P, Yu J, Dong L, Liang D, Feng J, Yan J, Wang P Y, Li Q, Zhang Z, Li M and Li G 2016 Mol. Cell 64 120
[8] Vassylyev D G, ichi Sekine S, Laptenko O, Lee J, Vassylyeva M N, Borukhov S and Yokoyama S 2002 Nature 417 712
[9] Song F, Chen P, Sun D, Wang M, Dong L, Liang D, Xu R M, Zhu P and Li G 2014 Science 344 376
[10] Osman S and Cramer P 2020 Annu. Rev. Cell Dev. Biol. 36 1
[11] Chen X, Yin X, Li J, Wu Z, Qi Y, Wang X, Liu W and Xu Y 2021 Science 372 eabg0635
[12] Kujirai T, Ehara H, Fujino Y, Shirouzu M, i Sekine S and Kurumizaka H 2018 Science 362 595
[13] Abbondanzieri E A, Greenleaf W J, Shaevitz J W, Landick R and Block S M 2005 Nature 438 460
[14] Hohlbein J and Kapanidis A 2016 Single-Molecule Enzymology: Fluorescence-Based and High-Throughput Methods (Elsevier) pp. 353-378
[15] Hud N V and Vilfan I D 2005 Annu. Rev. Biophys. Biomol. Struct. 34 295
[16] Pomerantz R T and O'Donnell M 2010 Science 327 590
[17] Merrikh H, Machón C, Grainger W H, Grossman A D and Soultanas P 2011 Nature 470 554
[18] Hohlbein J, Aigrain L, Craggs T D, Bermek O, Potapova O, Shoolizadeh P, Grindley N D F, Joyce C M and Kapanidis A N 2013 Nat. Commun. 4 2131
[19] Koster M J and Snel H T T 2015 Cell 161 724
[20] Bernardi G 2015 Cold Spring Harb. Symp. Quant. Biol. 80 83
[21] Landick R 2021 Annu. Rev. Microbiol. 75 291
[22] Förster T H 1965 in Modern quantum chemistry, istanbul lectures, Part III: Action of light and organic crystals pp. 93-137 (New York: Academic Press)
[23] Ha T, Enderle T, Ogletree D F, Chemla D S, Selvin P R and Weiss S 1996 Proc. Natl. Acad. Sci. USA 93 6264
[24] Weiss S 1999 Science 283 1676
[25] Lerner E, Cordes T, Ingargiola A, Alhadid Y, Chung S, Michalet X and Weiss S 2018 Science 359 eaan1133
[26] Lerner E, Barth A, Hendrix J, et al. 2021 eLife 10 e60416
[27] Ha T, Kaiser C, Myong S, Wu B and Xiao J 2022 Mol. Cell 82 304
[28] Ashkin A and Dziedzic J M 1987 Science 235 1517
[29] Neuman K C and Block S M 2004 Rev. Sci. Instrum. 75 2787
[30] Gosse C and Croquette V 2002 Biophys. J. 82 3314
[31] Strick T R, Allemand J F, Bensimon D, Bensimon A and Croquette V 1996 Science 271 1835
[32] Neuman K C and Nagy A 2008 Nat. Methods 5 491
[33] Lionnet T, Allemand J F, Revyakin A, Strick T R, Saleh O A, Bensimon D and Croquette V 2011 Cold Spring Harb. Protoc. 2012 133
[34] Klein H L, Ang K K, Arkin M R,et al. 2019 Microbial Cell 6 65
[35] Revyakin A, Ebright R H and Strick T R 2005 Nat. Methods 2 127
[36] Revyakin A, Ebright R H and Strick T R 2004 Proc. Natl. Acad. Sci. USA 101 4776
[37] Revyakin A, Liu C, Ebright R H and Strick T R 2006 Science 314 1139
[38] Lerner E, Chung S, Allen B L, Wang S, Lee J, Lu S W, Grimaud L W, Ingargiola A, Michalet X, Alhadid Y, Borukhov S, Strick T R, Taatjes D J and Weiss S 2016 Proc. Natl. Acad. Sci. USA 113 6562
[39] Wang S, Han Z, Libri D, Porrua O and Strick T R 2019 Nat. Commun. 10 1545
[40] Galburt E A, Grill S W, Wiedmann A, Lubkowska L, Choy J, Nogales E, Kashlev M and Bustamante C 2007 Nature 446 820
[41] Fazal F M, Meng C A, Murakami K, Kornberg R D and Block S M 2015 Nature 525 274
[42] Friedman L J and Gelles J 2015 Methods 86 27
[43] Tetone L E, Friedman L J, Osborne M L, Ravi H, Kyzer S, Stumper S K, Mooney R A, Landick R and Gelles J 2017 Proc. Natl. Acad. Sci. USA 114 E1081
[44] Rosen G A, Baek I, Friedman L J, Joo Y J, Buratowski S and Gelles J 2020 Proc. Natl. Acad. Sci. USA 117 32348
[45] Almén M S, Nordström K J, Fredriksson R and Schiöth H B 2009 BMC Biol. 7 50
[46] Lingwood D and Simons K 2010 Science 327 46
[47] Latorraca N R, Venkatakrishnan A J and Dror R O 2016 Chem. Rev. 117 139
[48] Bennett D L, Clark A J, Huang J, Waxman S G and Dib-Hajj S D 2019 Physiol. Rev. 99 1079
[49] James J R and Vale R D 2012 Nature 487 64
[50] Bhagwat A R, Sage V L, Nturibi E, Kulej K, Jones J, Guo M, Kim E T, Garcia B A, Weitzman M D, Shroff H and Lakdawala S S 2020 Nat. Commun. 11 23
[51] García-López V, Chen F, Nilewski L G, Duret G, Aliyan A, Kolomeisky A B, Robinson J T, Wang G, Pal R and Tour J M 2017 Nature 548 567
[52] Ritter A T, Asano Y, Stinchcombe J C, Dieckmann N, Chen B C, Gawden-Bone C, van Engelenburg S, Legant W, Gao L, Davidson M W, Betzig E, Lippincott-Schwartz J and Griffiths G M 2015 Immunity 42 864
[53] Jackson H J, Rafiq S and Brentjens R J 2016 Nat. Rev. Clin. Oncol. 13 370
[54] Fridman W H, Zitvogel L, Sautés-Fridman C and Kroemer G 2017 Nat. Rev. Clin. Oncol. 14 717
[55] Zhu C, Chen W, Lou J, Rittase W and Li K 2019 Nat. Immunol. 20 1269
[56] Hu W, Zhang Y, Fei P, Zhang T, Yao D, Gao Y, Liu J, Chen H, Lu Q, Mudianto T, Zhang X, Xiao C, Ye Y, Sun Q, Zhang J, Xie Q, Wang P H, Wang J, Li Z, Lou J and Chen W 2021 Cell Res. 31 1047
[57] Wu P, Zhang T, Liu B, Fei P, Cui L, Qin R, Zhu H, Yao D, Martinez R J, Hu W, An C, Zhang Y, Liu J, Shi J, Fan J, Yin W, Sun J, Zhou C, Zeng X, Xu C, Wang J, Evavold B D, Zhu C, Chen W and Lou J 2019 Mol. Cell 73 1015
[58] Liu Y, Blanchfield L, Ma V P Y, Andargachew R, Galior K, Liu Z, Evavold B and Salaita K 2016 Proc. Natl. Acad. Sci. USA 113 5610
[59] Kaback H R 1974 Science 186 882
[60] Discher D E and Eisenberg A 2002 Science 297 967
[61] Rogers M A and Aikawa E 2018 Nat. Rev. Cardiol. 16 261
[62] Wang Y, Gao J, Guo X, Tong T, Shi X, Li L, Qi M, Wang Y, Cai M, Jiang J, Xu C, Ji H and Wang H 2014 Cell Research 24 959
[63] Pan Y, Wang S, Shan Y, Zhang D, Gao J, Zhang M, Liu S, Cai M, Xu H, Li G, Qin Q and Wang H 2015 Small 11 2782
[64] Pan Y, Zhang F, Zhang L, Liu S, Cai M, Shan Y, Wang X, Wang H and Wang H 2017 Adv. Sci. 4 1600489
[65] Yan Q, Lu Y, Zhou L, Chen J, Xu H, Cai M, Shi Y, Jiang J, Xiong W, Gao J and Wang H 2018 Proc. Natl. Acad. Sci. USA 115 7033
[66] Garcá-Rendón A, Garibay-Escobar A, Guzmán R and Tejeda-Mansir A 2018 Lipid Nanocarriers for Drug Targeting (Elsevier) pp. 231-267
[67] Ma D F, Xu C H, Hou W Q, Zhao C Y, Ma J B, Huang X Y, Jia Q, Ma L, Diao J, Liu C, Li M and Lu Y 2019 Angew. Chem. Int. Ed. 58 5577
[68] Litschel T and Schwille P 2021 Annu. Rev. Bioph. Biom. 50 525
[69] Hou W, Ma D, He X, Han W, Ma J, Wang H, Xu C, Xie R, Fan Q, Ye F, Hu S, Li M and Lu Y 2020 Nano Lett. 21 485
[70] Balasubramanian G, Chan I Y, Kolesov R, Al-Hmoud M, Tisler J, Shin C, Kim C, Wojcik A, Hemmer P R, Krueger A, Hanke T, Leitenstorfer A, Bratschitsch R, Jelezko F and Wrachtrup J 2008 Nature 455 648
[71] Maze J R, Stanwix P L, Hodges J S, Hong S, Taylor J M, Cappellaro P, Jiang L, Dutt M V G, Togan E, Zibrov A S, Yacoby A, Walsworth R L and Lukin M D 2008 Nature 455 644
[72] Shi F, Zhang Q, Wang P, Sun H, Wang J, Rong X, Chen M, Ju C, Reinhard F, Chen H, Wrachtrup J, Wang J and Du J 2015 Science 347 1135
[73] Shi F, Kong F, Zhao P, Zhang X, Chen M, Chen S, Zhang Q, Wang M, Ye X, Wang Z, Qin Z, Rong X, Su J, Wang P, Qin P Z and Du J 2018 Nat. Methods 15 697
[74] Kasianowicz J, Brandin E, Branton D and Deamer D 1996 Proc. Natl. Acad. Sci. USA 93 13770
[75] Cao C, Ying Y L, Hu Z L, Liao D F, Tian H and Long Y T 2016 Nat. Nanotechnol. 11 713
[76] Cao J, Jia W, Zhang J, Xu X, Yan S, Wang Y, Zhang P, Chen H Y and Huang S 2019 Nat. Commun. 10 5668
[77] Huang S, Romero-Ruiz M, Castell O K, Bayley H and Wallace M I 2015 Nat. Nanotechnol 10 986
[78] Wang Y, Wang Y, Du X, Yan S, Zhang P, Chen H Y and Huang S 2019 Sci. Adv. 5 eaar3309
[79] Cao C, Li M Y, Cirauqui N, Wang Y Q, Peraro M D, Tian H and Long Y T 2018 Nat. Commun. 9 2823
[80] Santoso Y, Joyce C M, Potapova O, Reste L L, Hohlbein J, Torella J P, Grindley N D F and Kapanidis A N 2009 Proc. Natl. Acad. Sci. USA 107 715
[81] Roeder R G 2019 Nat. Struct. Mol. Biol. 26 783
[82] Murphy M, Rasnik I, Cheng W, Lohman T M and Ha T 2004 Biophys. J. 86 2530
[83] Lin W, Ma J, Nong D, Xu C, Zhang B, Li J, Jia Q, Dou S, Ye F, Xi X, Lu Y and Li M 2017 Phys. Rev. Lett. 119 138102
[84] Ma J B, Chen Z, Xu C H, Huang X Y, Jia Q, Zou Z Y, Mi C Y, Ma D F, Lu Y, Zhang H D and Li M 2020 Nucleic Acids Res. 48 3156
[85] Gu L, Sheng Y, Chen Y, Chang H, Zhang Y, Lv P, Ji W and Xu T 2014 Biophys. J. 106 2443
[86] Gu L, Li Y, Zhang S, Xue Y, Li W, Li D, Xu T and Ji W 2019 Nat. Methods 16 1193
[87] Gu L, Li Y, Zhang S, Zhou M, Xue Y, Li W, Xu T and Ji W 2021 Nat. Methods 18 369
[88] Yuan J W, Zhang Y N, Liu Y R, Li W, Dou S X, Wei Y, Wang P Y and Li H 2021 Small 18 2106498
[89] Li H, Dou S X, Liu Y R, Li W, Xie P, Wang W C and Wang P Y 2015 J. Am. Chem. Soc. 137 436
[90] Lidke D S, Nagy P, Heintzmann R, Arndt-Jovin D J, Post J N, Grecco H E, Jares-Erijman E A and Jovin T M 2004 Nat. Biotechnol. 22 198
[91] Cui B, Wu C, Chen L, Ramirez A, Bearer E L, Li W P, Mobley W C and Chu S 2007 Proc. Natl. Acad. Sci. USA 104 13666
[92] Li H, Duan Z W, Xie P, Liu Y R, Wang W C, Dou S X and Wang P Y 2012 PLoS ONE 7 e45465
[93] Li B, Dou S X, Yuan J W, Liu Y R, Li W, Ye F, Wang P Y and Li H 2018 Proc. Natl. Acad. Sci. USA 115 12118
[94] Jiang C, Li B, Dou S X, Wang P Y and Li H 2020 Chin. Phys. Lett. 37 078701
[95] Chen X 2020 Chin. Phys. Lett. 37 080103
[96] Jiang C, Yang M, Li W, Dou S X, Wang P Y and Li H 2022 iScience 25 104210
[97] Dongfei M, Wenqing H, Chenguang Y, Shuxin H, Weijing H, Ying L and and 2021 Biophysics Reports 7 490
[98] Petrie E J, Czabotar P E and Murphy J M 2019 Trends Biochem. Sci. 44 53
[99] Shuai J W and Jung P 2005 Phys. Rev. Lett. 95 114501
[100] Wu X X and Shuai J 2015 Phys. Rev. E 91 022712
[101] Chen Y, Qi H, Li X, Cai M, Chen X, Liu W and Shuai J 2016 Phys. Rev. E 94 022411
[102] Tian X, Huang B, Zhang X P, Lu M, Liu F, Onuchic J N and Wang W 2017 Proc. Natl. Acad. Sci. USA 114 5337
[103] Lv C, Li F, Li X, Tian Y, Zhang Y, Sheng X, Song Y, Meng Q, Yuan S, Luan L, Andl T, Feng X, Jiao B, Xu M, Plikus M V, Dai X, Lengner C, Cui W, Ren F, Shuai J, Millar S E and Yu Z 2017 Nat. Commun. 8 1036
[104] Li W, Wang J, Zhang J, Takada S and Wang W 2019 Phys. Rev. Lett. 122 238102

Single-molecular methodologies for the physical biology of protein machines

Single-molecular methodologies for the physical biology of protein machines

RichHTML

PDF (PC)

赞

可视化

摘要/Abstract

引用本文

使用本文

参考文献

相关文章 6

Metrics

本文评价

推荐阅读 0

[1]	Rokshana Parvin, Qi Jia(贾棋), Jianbing Ma(马建兵), Chunhua Xu(徐春华), Ying Lu(陆颖), Fangfu Ye(叶方富), and Ming Li(李明). New insight into the mechanism of DNA polymerase I revealed by single-molecule FRET studies of Klenow fragment[J]. 中国物理B, 2022, 31(8): 88701-088701.
[2]	童鑫, 胡蕊, 李晓晴, 赵清. Probing conformational change of T7 RNA polymerase and DNA complex by solid-state nanopores[J]. 中国物理B, 2018, 27(11): 118705-118705.
[3]	王一舟, 侯锡苗, 车海鹏, 肖雪, 奚绪光, 窦硕星, 王鹏业, 李伟. Interaction between human telomeric G-quadruplexes characterized by single molecule magnetic tweezers[J]. 中国物理B, 2018, 27(6): 68701-068701.
[4]	翟伟利, 袁国华, 刘超, 陈虎. Improved data analysis method of single-molecule experiments based on probability optimization[J]. 中国物理B, 2018, 27(1): 18703-018703.
[5]	马丽, 李颖, 李明, 胡书新. Protein-membrane interactions investigated with surface-induced fluorescence attenuation[J]. 中国物理B, 2017, 26(12): 128708-128708.
[6]	徐悦, 陈虎, 璩玉杰, 黎明, 欧阳钟灿, 刘冬生, 严洁. Mechano-chemical selections of two competitive unfolding pathways of a single DNA i-motif[J]. 中国物理B, 2014, 23(6): 68702-068702.