Cargando…

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

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 of RNA and DNA deformations and the complexity of interactions in RNA and DNA. Magne...

Descripción completa

Detalles Bibliográficos
Autores principales: Tian, Fu-Jia, Zhang, Chen, Zhou, Erchi, Dong, Hai-Long, Tan, Zhi-Jie, Zhang, Xing-Hua, Dai, Liang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10193934/
https://www.ncbi.nlm.nih.gov/pubmed/37155848
http://dx.doi.org/10.1073/pnas.2218425120
_version_ 1785043914643734528
author Tian, Fu-Jia
Zhang, Chen
Zhou, Erchi
Dong, Hai-Long
Tan, Zhi-Jie
Zhang, Xing-Hua
Dai, Liang
author_facet Tian, Fu-Jia
Zhang, Chen
Zhou, Erchi
Dong, Hai-Long
Tan, Zhi-Jie
Zhang, Xing-Hua
Dai, Liang
author_sort Tian, Fu-Jia
collection PubMed
description 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 of RNA and DNA deformations 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 double-stranded 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 twist-groove coupling. For DNA, these stimuli first modify diameter, which is transduced into twist change through twist-diameter coupling. Twist-groove coupling and twist-diameter coupling appear to be utilized by protein binding to reduce DNA and RNA deformation energy cost upon protein binding.
format Online
Article
Text
id pubmed-10193934
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher National Academy of Sciences
record_format MEDLINE/PubMed
spelling pubmed-101939342023-05-19 Universality in RNA and DNA deformations induced by salt, temperature change, stretching force, and protein binding Tian, Fu-Jia Zhang, Chen Zhou, Erchi Dong, Hai-Long Tan, Zhi-Jie Zhang, Xing-Hua Dai, Liang Proc Natl Acad Sci U S A Biological Sciences 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 of RNA and DNA deformations 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 double-stranded 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 twist-groove coupling. For DNA, these stimuli first modify diameter, which is transduced into twist change through twist-diameter coupling. Twist-groove coupling and twist-diameter coupling appear to be utilized by protein binding to reduce DNA and RNA deformation energy cost upon protein binding. National Academy of Sciences 2023-05-08 2023-05-16 /pmc/articles/PMC10193934/ /pubmed/37155848 http://dx.doi.org/10.1073/pnas.2218425120 Text en Copyright © 2023 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by/4.0/This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY) (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Biological Sciences
Tian, Fu-Jia
Zhang, Chen
Zhou, Erchi
Dong, Hai-Long
Tan, Zhi-Jie
Zhang, Xing-Hua
Dai, Liang
Universality in RNA and DNA deformations induced by salt, temperature change, stretching force, and protein binding
title Universality in RNA and DNA deformations induced by salt, temperature change, stretching force, and protein binding
title_full Universality in RNA and DNA deformations induced by salt, temperature change, stretching force, and protein binding
title_fullStr Universality in RNA and DNA deformations induced by salt, temperature change, stretching force, and protein binding
title_full_unstemmed Universality in RNA and DNA deformations induced by salt, temperature change, stretching force, and protein binding
title_short Universality in RNA and DNA deformations induced by salt, temperature change, stretching force, and protein binding
title_sort universality in rna and dna deformations induced by salt, temperature change, stretching force, and protein binding
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10193934/
https://www.ncbi.nlm.nih.gov/pubmed/37155848
http://dx.doi.org/10.1073/pnas.2218425120
work_keys_str_mv AT tianfujia universalityinrnaanddnadeformationsinducedbysalttemperaturechangestretchingforceandproteinbinding
AT zhangchen universalityinrnaanddnadeformationsinducedbysalttemperaturechangestretchingforceandproteinbinding
AT zhouerchi universalityinrnaanddnadeformationsinducedbysalttemperaturechangestretchingforceandproteinbinding
AT donghailong universalityinrnaanddnadeformationsinducedbysalttemperaturechangestretchingforceandproteinbinding
AT tanzhijie universalityinrnaanddnadeformationsinducedbysalttemperaturechangestretchingforceandproteinbinding
AT zhangxinghua universalityinrnaanddnadeformationsinducedbysalttemperaturechangestretchingforceandproteinbinding
AT dailiang universalityinrnaanddnadeformationsinducedbysalttemperaturechangestretchingforceandproteinbinding