Abstract
High hydrostatic pressure affects the structure, dynamics, and the stability of biomolecular systems. Therefore, in order to describe the entire energy and conformational landscape and the set of parameters required for a comprehensive understanding of the general phase behavior of biomolecular systems, one needs to scan the full thermodynamic parameter space, including high pressure. In addition, high hydrostatic pressures are encountered in organisms living in the deep sea and in subseafloor ecosystems, which constitute a significant portion of the Earth’s biosphere and where pressures up to the 1000 bar level or more prevail. High pressure is also a key parameter in the context of exploring the origin and the physical limits of life on Earth or on other planets and moons. In this review, we lay out the conceptual framework for exploring conformational fluctuations, dynamical properties, and the activity of biomolecular systems using pressure perturbation, focusing in particular on non-canonical nucleic acid systems, such as DNA hairpins, G-quadruplexes and i-motifs, and their interactions. Moreover, the effects of cosolutes (salts, osmolytes), macromolecular crowding, and intrinsically disordered peptides on the conformational dynamics of non-canonical nucleic acid structures at ambient and high-pressure conditions will be discussed.
This is a preview of subscription content, log in via an institution to check access.
References
Akasaka K, Matsuki H (2015) High pressure bioscience. In: Akasaka K, Matsuki H (eds) Subcellular biochemistry, vol 72. Springer Netherlands, Dordrecht. https://doi.org/10.1007/978-94-017-9918-8
Arns L, Winter R (2019) Liquid-liquid phase separation rescues the conformational stability of a DNA hairpin from pressure-stress. Chem Commun 55(72):10673–10676. https://doi.org/10.1039/c9cc04967c
Arns L, Knop J-M, Patra S, Anders C, Winter R (2019) Single-molecule insights into the temperature and pressure dependent conformational dynamics of nucleic acids in the presence of crowders and osmolytes. Biophys Chem 251:106190. https://doi.org/10.1016/j.bpc.2019.106190
ATTO-TEC. https://www.atto-tec.com/product_info.php?info=p103_atto-550.html; https://www.atto-tec.com/product_info.php?info=p114_atto-647n.html; https://www.atto-tec.com/?cat=c45_R-0%2D%2DWerte%2D%2DFRET%2D%2Dr-0-werte-fret.html
Biffi G, Tannahill D, McCafferty J, Balasubramanian S (2013) Quantitative visualization of DNA G-quadruplex structures in human cells. Nat Chem 5(3):182–186. https://doi.org/10.1038/nchem.1548
Chaurasiya, KR, Dame, RT (2018) Single Molecule FRET Analysis of DNA Binding Proteins. In: Peterman, E (eds) Single Molecule Analysis. Methods in Molecular Biology, vol 1665. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-7271-5_12
Choi J, Kim S, Tachikawa T, Fujitsuka M, Majima T (2011) PH-induced intramolecular folding dynamics of i-motif DNA. J Am Chem Soc 133(40):16146–16153. https://doi.org/10.1021/ja2061984
Cui J, Waltman P, Le VH, Lewis EA (2013) The effect of molecular crowding on the stability of human C-MYC promoter sequence i-motif at neutral pH. Molecules 18(10):12751–12767. https://doi.org/10.3390/molecules181012751
Daniel I, Oger P, Winter R (2006) Origins of life and biochemistry under high-pressure conditions. Chem Soc Rev 35(10):858–875. https://doi.org/10.1039/b517766a
Davis JT (2004) G-quartets 40 years later: from 5′-GMP to molecular biology and supramolecular chemistry. Angew Chemie Int Ed 43(6):668–698. https://doi.org/10.1002/anie.200300589
del Villar-Guerra R, Trent JO, Chaires JB (2018) G-quadruplex secondary structure obtained from circular dichroism spectroscopy. Angew Chemie Int Ed 57(24):7171–7175. https://doi.org/10.1002/anie.201709184
Deniz AA, Mukhopadhyay S, Lemke EA (2008) Single-molecule biophysics: at the interface of biology, physics and chemistry. J R Soc Interface 5(18):15–45. https://doi.org/10.1098/rsif.2007.1021
Fan HY, Shek YL, Amiri A, Dubins DN, Heerklotz H, MacGregor RB, Chalikian TV (2011) Volumetric characterization of sodium-induced G-quadruplex formation. J Am Chem Soc 133(12):4518–4526. https://doi.org/10.1021/ja110495c
Fiore JL, Kraemer B, Koberling F, Edmann R, Nesbitt DJ (2009) Enthalpy-driven RNA folding: single-molecule thermodynamics of tetraloop-receptor tertiary interaction. Biochemistry 48(11):2550–2558. https://doi.org/10.1021/bi8019788
Garcia AE, Paschek D (2008) Simulation of the pressure and temperature folding/unfolding equilibrium of a small RNA hairpin. J Am Chem Soc 130(3):815–817. https://doi.org/10.1021/ja074191i
Girard E, Prange T, Dhaussy A-C, Migianu-Griffoni E, Lecouvey M, Chervin J-C, Mezouar M, Kahn R, Fourme R (2007) Adaptation of the base-paired double-helix molecular architecture to extreme pressure. Nucleic Acids Res 35(14):4800–4808. https://doi.org/10.1093/nar/gkm511
Ha T (2004) Structural dynamics and processing of nucleic acids revealed by single-molecule spectroscopy. Biochemistry 43(14):4055–4063. https://doi.org/10.1021/bi049973s
Ha T, Selvin PR (2008) The new era of biology in singulo. In: Single-molecule techniques: a laboratory manual. CSH Press, pp 1–36
Harish B, Wang J, Hayden EJ, Grabe B, Hiller W, Winter R, Royer CA (2022) Hidden intermediates in mango III RNA aptamer folding revealed by pressure perturbation. Biophys J 121(3):421–429. https://doi.org/10.1016/j.bpj.2021.12.037
Knop J-M, Patra S, Harish B, Royer CA, Winter R (2018) The deep sea osmolyte trimethylamine N -oxide and macromolecular crowders rescue the antiparallel conformation of the human telomeric G-quadruplex from urea and pressure stress. Chem A Eur J 24(54):14346–14351. https://doi.org/10.1002/chem.201802444
Knop J-M, Mukherjee SK, Oliva R, Möbitz S, Winter R (2020) Remodeling of the conformational dynamics of noncanonical DNA structures by monomeric and aggregated α-synuclein. J Am Chem Soc 142(43):18299–18303. https://doi.org/10.1021/jacs.0c07192
Krzyzaniak A, Sałański P, Jurczak J, Barciszewski J, Krzyźaniak A, Salański P, Jurczak J, Barciszewski J (1991) B-Z DNA reversible conformation changes effected by high pressure. FEBS Lett 279(1):1–4. https://doi.org/10.1016/0014-5793(91)80235-U
Lakowicz JR (2006) In: Lakowicz JR (ed) Principles of fluorescence spectroscopy. Springer US, Boston, MA. https://doi.org/10.1007/978-0-387-46312-4
Lee T (2009) Extracting kinetics information from single-molecule fluorescence resonance energy transfer data using hidden Markov models. J Phys Chem B 113(33):11535–11542. https://doi.org/10.1021/jp903831z
Lepper CP, Williams MAK, Edwards PJB, Filichev VV, Jameson GB (2019) Effects of pressure and pH on the physical stability of an i-motif DNA structure. ChemPhysChem 20(12):1567–1571. https://doi.org/10.1002/cphc.201900145
Lerner E, Barth A, Hendrix J, Ambrose B, Birkedal V, Blanchard SC, Börner R, Chung HS, Cordes T, Craggs TD, Deniz AA, Diao J, Fei J, Gonzalez RL, Gopich IV, Ha T, Hanke CA, Haran G, Hatzakis NS, Hohng S, Hong SC, Hugel T, Ingargiola A, Joo C, Kapanidis AN, Kim HD, Laurence T, Lee NK, Lee TH, Lemke EA, Margeat E, Michaelis J, Michalet X, Myong S, Nettels D, Peulen TO, Ploetz E, Razvag Y, Robb NC, Schuler B, Soleimaninejad H, Tang C, Vafabakhsh R, Lamb DC, Seidel CAM, Weiss S, Boudker O (2021) FRET-based dynamic structural biology: challenges, perspectives and an appeal for open-science practices. elife 10:e60416. https://doi.org/10.7554/eLife.60416
Lu HP (2005) Probing single-molecule protein conformational dynamics. Acc Chem Res 38(7):557–565. https://doi.org/10.1021/ar0401451
Macgregor RB (1998) Effect of hydrostatic pressure on nucleic acids. Biopolymers 48(4):253–263. https://doi.org/10.1002/(SICI)1097-0282(1998)48:4<253::AID-BIP5>3.0.CO;2-F
Macgregor RB (2002) The interactions of nucleic acids at elevated hydrostatic pressure. Biochim Biophys Acta Protein Struct Mol Enzymol 1595(1–2):266–276. https://doi.org/10.1016/S0167-4838(01)00349-1
McKinney SA, Joo C, Ha T (2006) Analysis of single-molecule FRET trajectories using hidden Markov modeling. Biophys J 91(5):1941–1951. https://doi.org/10.1529/biophysj.106.082487
Megalathan A, Cox BD, Wilkerson PD, Kaur A, Sapkota K, Reiner JE, Dhakal S (2019) Single-molecule analysis of i-motif within self-assembled DNA duplexes and nanocircles. Nucleic Acids Res 47(14):7199–7212. https://doi.org/10.1093/nar/gkz565
Merrin J, Kumar P, Libchaber A (2011) Effects of pressure and temperature on the binding of RecA protein to single-stranded DNA. Proc Natl Acad Sci U S A 108(50):19913–19918. https://doi.org/10.1073/pnas.1112646108
Miura T, Benevides JM, Thomas GJ (1995) A phase diagram for sodium and potassium ion control of polymorphism in telomeric DNA. J Mol Biol 248(2):233–238. https://doi.org/10.1016/s0022-2836(95)80046-8
Miyoshi D, Nakamura K, Tateishi-Karimata H, Ohmichi T, Sugimoto N (2009) Hydration of Watson Crick base pairs and dehydration of Hoogsteen base pairs inducing structural polymorphism under molecular crowding conditions. J Am Chem Soc 131(10):3522–3531. https://doi.org/10.1021/ja805972a
Mukherjee SK, Knop JM, Möbitz S, Winter RHA (2020) Alteration of the conformational dynamics of a DNA hairpin by α-synuclein in the presence of aqueous two-phase systems. Chem A Eur J 26(48):10987–10991. https://doi.org/10.1002/chem.202002119
Mukherjee SK, Knop J-M, Oliva R, Möbitz S, Winter R (2021) Untangling the interaction of α-synuclein with DNA i-motifs and hairpins by volume-sensitive single-molecule FRET spectroscopy. RSC Chem Biol 2(4):1196–1200. https://doi.org/10.1039/d1cb00108f
Myong S, Bruno MM, Pyle AM, Ha T (2007) Spring-loaded mechanism of DNA unwinding by hepatitis C virus NS3 helicase. Science 317(5837):513–516. https://doi.org/10.1126/science.1144130
Neidle S (2010) Human telomeric G-quadruplex: the current status of telomeric G-quadruplexes as therapeutic targets in human cancer. FEBS J 277(5):1118–1125. https://doi.org/10.1111/j.1742-4658.2009.07463.x
Olsen CM, Marky LA (2009) Energetic and hydration contributions of the removal of methyl groups from thymine to form uracil in G-quadruplexes. J Phys Chem B 113(1):9–11. https://doi.org/10.1021/jp808526d
Patra S, Anders C, Schummel PH, Winter R (2018) Antagonistic effects of natural osmolyte mixtures and hydrostatic pressure on the conformational dynamics of a DNA hairpin probed at the single-molecule level. Phys Chem Chem Phys 20(19):13159–13170. https://doi.org/10.1039/C8CP00907D
Patra S, Schuabb V, Kiesel I, Knop J-M, Oliva R, Winter R (2019) Exploring the effects of cosolutes and crowding on the volumetric and kinetic profile of the conformational dynamics of a poly DA loop DNA hairpin: a single-molecule FRET study. Nucleic Acids Res 47(2):981–996. https://doi.org/10.1093/nar/gky1122
Paul S, Hossain SS, Samanta A (2020) Insights into the folding pathway of a C-MYC-promoter-based i-motif DNA in crowded environments at the single-molecule level. J Phys Chem B 124(5):763–770. https://doi.org/10.1021/acs.jpcb.9b10633
Phelps C, Lee W, Jose D, Von Hippel PH, Marcus AH (2013) Single-molecule FRET and linear dichroism studies of DNA breathing and helicase binding at replication fork junctions. Proc Natl Acad Sci U S A 110(43):17320–17325. https://doi.org/10.1073/pnas.1314862110
Rajendran A, Nakano SI, Sugimoto N (2010) Molecular crowding of the cosolutes induces an intramolecular i-motif structure of triplet repeat DNA oligomers at neutral pH. Chem Commun 46(8):1299–1301. https://doi.org/10.1039/b922050j
Ren J, Qu X, Trent JO, Chaires JB (2002) Tiny telomere DNA. Nucleic Acids Res 30(11):2307–2315. https://doi.org/10.1093/nar/30.11.2307
Robinson CR, Sligar SG (1994) Hydrostatic pressure reverses osmotic pressure effects on the specificity of EcoRI-DNA interactions. Biochemistry 33(13):3787–3793. https://doi.org/10.1021/bi00179a001
Rohs R, West SM, Sosinsky A, Liu P, Mann RS, Honig B (2009) The role of DNA shape in protein-DNA recognition. Nature 461(7268):1248–1253. https://doi.org/10.1038/nature08473
Royer CA, Chakerian AE, Matthews KS (1990) Macromolecular binding equilibria in the lac repressor system: studies using high-pressure fluorescence spectroscopy. Biochemistry 29(20):4959–4966. https://doi.org/10.1021/bi00472a028
Rüttinger S, Macdonald R, Krämer B, Koberling F, Roos M, Hildt E (2006) Accurate single-pair Förster resonant energy transfer through combination of pulsed interleaved excitation, time correlated single-photon counting, and fluorescence correlation spectroscopy. J Biomed Opt 11(2):024012. https://doi.org/10.1117/1.2187425
Schärfen L, Schlierf M (2019) Real-time monitoring of protein-induced DNA conformational changes using single-molecule FRET. Methods 169:11–20. https://doi.org/10.1016/j.ymeth.2019.02.011
Senior MM, Jones RA, Breslauer KJ (1988) Influence of loop residues on the relative stabilities of DNA hairpin structures. Proc Natl Acad Sci U S A 85(17):6242–6246. https://doi.org/10.1073/pnas.85.17.6242
Silva JL, Oliveira AC, Gomes AMO, Lima LMTR, Mohana-Borges R, Pacheco ABF, Foguel D (2002) Pressure induces folding intermediates that are crucial for protein–DNA recognition and virus assembly. Biochim Biophys Acta Protein Struct Mol Enzymol 1595(1–2):250–265. https://doi.org/10.1016/S0167-4838(01)00348-X
Silva JL, Oliveira AC, Vieira TCRG, de Oliveira GAP, Suarez MC, Foguel D (2014) High-pressure chemical biology and biotechnology. Chem Rev 114:7239–7267. https://doi.org/10.1021/cr400204z
Sinden RR, Pearson CE, Potaman VN, Ussery DW (1998) DNA: structure and function. In: Advances in genome biology, vol 5, pp 1–141. https://doi.org/10.1016/S1067-5701(98)80019-3
Somkuti J, Molnár OR, Smeller L (2020) Revealing unfolding steps and volume changes of human telomeric i-motif DNA. Phys Chem Chem Phys 22(41):23816–23823. https://doi.org/10.1039/d0cp03894f
Son I, Shek YL, Dubins DN, Chalikian TV (2014) Hydration changes accompanying helix-to-coil DNA transitions. J Am Chem Soc 136(10):4040–4047. https://doi.org/10.1021/ja5004137
Sugimoto N (2021) In: Maiti D, Guin S (eds) Chemistry and biology of non-canonical nucleic acids, 1st ed. Wiley, Weinheim. https://doi.org/10.1002/9783527817856
Summers MF, Byrd RA, Gallo KA, Samson CJ, Zon G, Egan W (1985) Nuclear magnetic resonance and circular dichroism studies of a duplex – single-stranded hairpin loop equilibrium for the oligodeoxyribonucleotide sequence d(CGCGATTCGCG). Nucleic Acids Res 13(17):6375–6386. https://doi.org/10.1093/nar/13.17.6375
Sung HL, Nesbitt DJ (2020a) Single-molecule kinetic studies of DNA hybridization under extreme pressures. Phys Chem Chem Phys 22(41):23491–23501. https://doi.org/10.1039/d0cp04035e
Sung H-LL, Nesbitt DJ (2020b) DNA hairpin hybridization under extreme pressures: a single-molecule FRET study. J Phys Chem B 124(1):110–120. https://doi.org/10.1021/acs.jpcb.9b10131
Sung H-LL, Nesbitt DJ (2020c) High pressure single-molecule FRET studies of the lysine riboswitch: cationic and osmolytic effects on pressure induced denaturation. Phys Chem Chem Phys 22(28):15853–15866. https://doi.org/10.1039/D0CP01921F
Takahashi S, Sugimoto N (2013a) Effect of pressure on the stability of G-quadruplex DNA: thermodynamics under crowding conditions. Angew Chemie Int Ed 52(51):13774–13778. https://doi.org/10.1002/anie.201307714
Takahashi S, Sugimoto N (2013b) Effect of pressure on thermal stability of G-quadruplex DNA and double-stranded DNA structures. Molecules 18(11):13297–13319. https://doi.org/10.3390/molecules181113297
Takahashi S, Sugimoto N (2015) Pressure-dependent formation of i-motif and G-quadruplex DNA structures. Phys Chem Chem Phys 17(46):31004–31010. https://doi.org/10.1039/C5CP04727G
Tsukanov R, Tomov TE, Berger Y, Liber M, Nir E (2013) Conformational dynamics of DNA hairpins at millisecond resolution obtained from analysis of single-molecule FRET histograms. J Phys Chem B 117(50):16105–16109. https://doi.org/10.1021/jp411280n
Wahl M, Röhlicke T, Rahn H-J, Erdmann R, Kell G, Ahlrichs A, Kernbach M, Schell AW, Benson O (2013) Integrated multichannel photon timing instrument with very short dead time and high throughput. Rev Sci Instrum 84(4):043102. https://doi.org/10.1063/1.4795828
Wang L, Brown SJ (2006) BindN: a web-based tool for efficient prediction of DNA and RNA binding sites in amino acid sequences. Nucleic Acids Res 34(Web Server):W243–W248. https://doi.org/10.1093/nar/gkl298
Wang G, Vasquez KM (2014) Impact of alternative DNA structures on DNA damage, DNA repair, and genetic instability. DNA Repair 19(1):143–151. https://doi.org/10.1016/j.dnarep.2014.03.017
Wells RD (2009) Discovery of the role of non-B DNA structures in mutagenesis and human genomic disorders. J Biol Chem 284(14):8997–9009. https://doi.org/10.1074/jbc.X800010200
Winter R (2019) Interrogating the structural dynamics and energetics of biomolecular systems with pressure modulation. Annu Rev Biophys 48(1):441–463. https://doi.org/10.1146/annurev-biophys-052118-115601
Wright EP, Huppert JL, Waller ZAE (2017) Identification of multiple genomic DNA sequences which form i-motif structures at neutral pH. Nucleic Acids Res 45(6):2951–2959. https://doi.org/10.1093/nar/gkx090
Yancey PH, Blake WR, Conley J (2002) Unusual organic osmolytes in deep-sea animals: adaptations to hydrostatic pressure and other perturbants. Comp Biochem Physiol Part A Mol Integr Physiol 133(3):667–676. https://doi.org/10.1016/S1095-6433(02)00182-4
Ying L, Green JJ, Li H, Klenerman D, Balasubramanian S (2003) Studies on the structure and dynamics of the human telomeric G quadruplex by single-molecule fluorescence resonance energy transfer. Proc Natl Acad Sci 100(25):14629–14634. USA. https://doi.org/10.1073/pnas.2433350100
Yu H, Gu X, Nakano SI, Miyoshi D, Sugimoto N (2012) Beads-on-a-string structure of long telomeric DNAs under molecular crowding conditions. J Am Chem Soc 134(49):20060–20069. https://doi.org/10.1021/ja305384c
Zeraati M, Langley DB, Schofield P, Moye AL, Rouet R, Hughes WE, Bryan TM, Dinger ME, Christ D (2018) I-motif DNA structures are formed in the nuclei of human cells. Nat Chem 10(6):631–637. https://doi.org/10.1038/s41557-018-0046-3
Acknowledgments
This project received funding from the European Union’s Horizon 2020 research and innovation program under the Marie Skłodowska-Curie grant agreement No 801459 – FP-RESOMUS and was funded by the Deutsche Forschungsgemeinschaft (DFG) under Germany’s Excellence Strategy – EXC 2033 – 390677874 – RESOLV.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Section Editor information
Rights and permissions
Copyright information
© 2022 Springer Nature Singapore Pte Ltd.
About this entry
Cite this entry
Mukherjee, S.K., Knop, JM., Winter, R. (2022). High-Pressure Single-Molecule Studies on Non-canonical Nucleic Acids and Their Interactions. In: Sugimoto, N. (eds) Handbook of Chemical Biology of Nucleic Acids. Springer, Singapore. https://doi.org/10.1007/978-981-16-1313-5_1-1
Download citation
DOI: https://doi.org/10.1007/978-981-16-1313-5_1-1
Received:
Accepted:
Published:
Publisher Name: Springer, Singapore
Print ISBN: 978-981-16-1313-5
Online ISBN: 978-981-16-1313-5
eBook Packages: Springer Reference Chemistry and Mat. ScienceReference Module Physical and Materials ScienceReference Module Chemistry, Materials and Physics