Universality in RNA and DNA deformations induced by salt, temperature change, stretching force, and protein binding

被引:17
作者
Tian, Fu-Jia [1 ,2 ,3 ]
Zhang, Chen [1 ]
Zhou, Erchi [1 ]
Dong, Hai-Long
Tan, Zhi-Jie [4 ]
Zhang, Xing-Hua [1 ]
Dai, Liang [2 ,3 ]
Ha, Taekjip
机构
[1] Wuhan Univ, Renmin Hosp, Coll Life Sci, Hubei Key Lab Cell Homeostasis, Wuhan 430072, Peoples R China
[2] City Univ Hong Kong, Dept Phys, Hong Kong 999077, Peoples R China
[3] City Univ Hong Kong, Shenzhen Res Inst, Shenzhen 518057, Peoples R China
[4] Wuhan Univ, Sch Phys & Technol, Wuhan 430072, Peoples R China
基金
中国国家自然科学基金;
关键词
DOUBLE-STRANDED-RNA; SHAPE; MECHANISMS; DYNAMICS; RECOGNITION; DEPENDENCE; INSIGHTS;
D O I
10.1073/pnas.2218425120
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
Nucleic acid deformations play important roles in many biological processes. The physical understanding of nucleic acid deformation by environmental stimuli is limited due to the challenge in the precise measurement ofRNAandDNAdeformations and the complexity of interactions in RNA and DNA. Magnetic tweezers experiments provide an excellent opportunity to precisely measure DNA and RNA twist changes induced by environmental stimuli. In this work, we applied magnetic tweezers to measure doublestranded RNA twist changes induced by salt and temperature changes. We observed RNA unwinds when lowering salt concentration, or increasing temperature. Our molecular dynamics simulations revealed the mechanism: lowering salt concentration or increasing temperature enlarges RNA major groove width, which causes twist decrease through twist-groove coupling. Combining these results with previous results, we found some universality in RNA and DNA deformations induced by three different stimuli: salt change, temperature, and stretching force. For RNA, these stimuli first modify the major groove width, which is transduced into twist change through twistgroove coupling. For DNA, these stimuli first modify diameter, which is transduced into twist change through twist-diameter coupling. Twist-groove coupling and twistdiameter coupling appear to be utilized by protein binding to reduce DNA and RNA deformation energy cost upon protein binding. Copyright © 2023 the Author(s).
引用
收藏
页数:9
相关论文
共 50 条
  • [1] Development of RNA Stiffness Parameters and Analysis on Protein-RNA Binding Specificity: Comparison with DNA
    Gromiha, M. Michael
    CURRENT BIOINFORMATICS, 2012, 7 (02) : 173 - 179
  • [2] Experimental maps of DNA structure at nucleotide resolution distinguish intrinsic from protein-induced DNA deformations
    Azad, Robert N.
    Zafiropoulos, Dana
    Ober, Douglas
    Jiang, Yining
    Chiu, Tsu-Pei
    Sagendorf, Jared M.
    Rohs, Remo
    Tullius, Thomas D.
    NUCLEIC ACIDS RESEARCH, 2018, 46 (05) : 2636 - 2647
  • [3] Temperature and salt concentration alter base-sequence selectivity of a duplex DNA-binding protein
    Nagatoishi, Satoru
    Tanaka, Yoshikazu
    Kudou, Motonori
    Tsumoto, Kouhei
    MOLECULAR BIOSYSTEMS, 2010, 6 (01) : 98 - 101
  • [4] Accumulation and Stretching of DNA Molecules in Temperature-Induced Concentration Gradients
    Simon, David J.
    Thalheim, Tobias
    Cichos, Frank
    JOURNAL OF PHYSICAL CHEMISTRY B, 2023, 127 (50) : 10861 - 10870
  • [5] Biochemical and biophysical characterization of the nucleic acid binding properties of the RNA/DNA binding protein EWS
    Selig, Emily E.
    Bhura, Roohi
    White, Matthew R.
    Akula, Shivani
    Hoffman, Renee D.
    Tovar, Carmel N.
    Xu, Xiaoping
    Booth, Rachell E.
    Libich, David S.
    BIOPOLYMERS, 2023, 114 (05)
  • [6] Understanding protein diffusion on force-induced stretched DNA conformation
    Mondal, Anupam
    Bhattacherjee, Arnab
    FRONTIERS IN MOLECULAR BIOSCIENCES, 2022, 9
  • [7] Different thermodynamic signatures for DNA minor groove binding with changes in salt concentration and temperature
    Wang, Shuo
    Kumar, Arvind
    Aston, Karl
    Binh Nguyen
    Bashkin, James K.
    Boykin, David W.
    Wilson, W. David
    CHEMICAL COMMUNICATIONS, 2013, 49 (76) : 8543 - 8545
  • [8] High-affinity RNA binding by a hyperthermophilic single-stranded DNA-binding protein
    Morten, Michael J.
    Gamsjaeger, Roland
    Cubeddu, Liza
    Kariawasam, Ruvini
    Peregrina, Jose
    Penedo, J. Carlos
    White, Malcolm F.
    EXTREMOPHILES, 2017, 21 (02) : 369 - 379
  • [9] DNA Binding in High Salt: Analysing the Salt Dependence of Replication Protein A3 from the Halophile Haloferax volcanii
    Winter, Jody A.
    Patoli, Bushra
    Bunting, Karen A.
    ARCHAEA-AN INTERNATIONAL MICROBIOLOGICAL JOURNAL, 2012, 2012
  • [10] Phage anti-CRISPR control by an RNA- and DNA-binding helix-turn-helix protein
    Birkholz, Nils
    Kamata, Kotaro
    Feussner, Maximilian
    Wilkinson, Max E.
    Samaniego, Christian Cuba
    Migur, Angela
    Kimanius, Dari
    Ceelen, Marijn
    Went, Sam C.
    Usher, Ben
    Blower, Tim R.
    Brown, Chris M.
    Beisel, Chase L.
    Weinberg, Zasha
    Fagerlund, Robert D.
    Jackson, Simon A.
    Fineran, Peter C.
    NATURE, 2024, : 670 - 677