Theoretical models for single-molecule DNA and RNA experiments: from elasticity to unzipping

Simona Cocco; John F. Marko; Rémi Monasson

doi:10.1016/S1631-0705(02)01345-2

Biophysique à l'échelle de la molécule unique/Single molecule biophysics

Theoretical models for single-molecule DNA and RNA experiments: from elasticity to unzipping
[Modélisation théorique des expériences de molécules uniques sur l'ADN et l'ARN : de l'élasticité au dégraffage des bases]

Simona Cocco ¹ ; John F. Marko ² ; Rémi Monasson ³

¹ CNRS–Laboratoire de dynamique des fluides complexes, 3, rue de l'Université, 67000 Strasbourg, France
² Department of Physics, The University of Illinois at Chicago, 845 W. Taylor St., Chicago, IL 60607, USA
³ CNRS–Laboratoire de physique théorique de l'ENS, 24, rue Lhomond, 75005 Paris, France

Comptes Rendus. Physique, Volume 3 (2002) no. 5, pp. 569-584.

Résumé
Abstract

Les travaux théoriques portant sur les expériences sur molécules uniques sont ici passés en revue. Tout d'abord, nous introduisons les modèles simples de polymères élastiques. Ensuite, nous expliquons comment ces modèles peuvent être utilisés pour interpréter les mesures de force-extension effectuées sur une molécule unique d'ADN (simple brin ou double brin), mesures qui mettent en évidence tantôt le caractère élastique de cette molécule, tantôt des transitions structurelles brutales. Dans une troisième partie, nous montrons qu'en associant les propriétes élastiques des brins d'acides nucléiques à une description de leurs interactions d'appariement, l'essentiel de la phénomènologie et de la cinétique de dégraffage de l'ARN et l'ADN peut être expliqué.

We review statistical-mechanical theories of single-molecule micromanipulation experiments on nucleic acids. Firstly, models for describing polymer elasticity are introduced. We then review how these models are used to interpret single-molecule force-extension experiments on single-stranded and double-stranded DNA. Depending on the force and the molecules used, both smooth elastic behavior and abrupt structural transitions are observed. Thirdly, we show how combining the elasticity of two single nucleic acid strands with a description of the base-pairing interactions between them explains much of the phenomenology and kinetics of RNA and DNA ‘unzipping’ experiments.

Reçu le : 2002-03-28
Accepté le : 2002-05-15
Publié le : 2002-01-01

DOI : 10.1016/S1631-0705(02)01345-2

Keywords: micromanipulation, polymer elasticity, DNA, RNAs
Mot clés : micromanipulation, élasticité des polymères, ADN, ARNs

Affiliations des auteurs :

Simona Cocco ¹ ; John F. Marko ² ; Rémi Monasson ³

@article{CRPHYS_2002__3_5_569_0,
     author = {Simona Cocco and John F. Marko and R\'emi Monasson},
     title = {Theoretical models for single-molecule {DNA} and {RNA} experiments: from elasticity to unzipping},
     journal = {Comptes Rendus. Physique},
     pages = {569--584},
     publisher = {Elsevier},
     volume = {3},
     number = {5},
     year = {2002},
     doi = {10.1016/S1631-0705(02)01345-2},
     language = {en},
}

TY  - JOUR
AU  - Simona Cocco
AU  - John F. Marko
AU  - Rémi Monasson
TI  - Theoretical models for single-molecule DNA and RNA experiments: from elasticity to unzipping
JO  - Comptes Rendus. Physique
PY  - 2002
SP  - 569
EP  - 584
VL  - 3
IS  - 5
PB  - Elsevier
DO  - 10.1016/S1631-0705(02)01345-2
LA  - en
ID  - CRPHYS_2002__3_5_569_0
ER  -

%0 Journal Article
%A Simona Cocco
%A John F. Marko
%A Rémi Monasson
%T Theoretical models for single-molecule DNA and RNA experiments: from elasticity to unzipping
%J Comptes Rendus. Physique
%D 2002
%P 569-584
%V 3
%N 5
%I Elsevier
%R 10.1016/S1631-0705(02)01345-2
%G en
%F CRPHYS_2002__3_5_569_0

Simona Cocco; John F. Marko; Rémi Monasson. Theoretical models for single-molecule DNA and RNA experiments: from elasticity to unzipping. Comptes Rendus. Physique, Volume 3 (2002) no. 5, pp. 569-584. doi : 10.1016/S1631-0705(02)01345-2. https://comptes-rendus.academie-sciences.fr/physique/articles/10.1016/S1631-0705(02)01345-2/

Bibliographie
Cité par

[1] P.J. Flory Statistical Mechanics of Chain Molecules, Hanser, Munich, 1989

[2] M. Doy; S.F. Edwards The Theory of Polymer Dynamics, Oxford University Press, Oxford, 1986

[3] C. Bustamante; J.F. Marko; E.D. Siggia; S. Smith Entropic elasticity of lambda-phage DNA, Science, Volume 265 (1994), p. 1599

[4] J.F. Marko; E.D. Siggia Stretching DNA, Macromolecules, Volume 28 (1995), p. 209

[5] R.H. Austin; J.P. Brody; E.C. Cox; T. Duke; W. Volkmuth Stretch genes, Phys. Today, Volume 50 (1997), p. 32

[6] C. Bustamante; S.B. Smith; J. Liphardt; D. Smith Single-molecule studies of DNA mechanics, Curr. Opin. Struct. Biol., Volume 10 (2000), p. 279

[7] M.D. Wang; H. Yin; R. Landick; J. Gelles; S. Block Stretching DNA with optical tweezers, Biophys. J., Volume 72 (1997), p. 1335

[8] T. Strick; J.F. Allemand; V. Croquette; D. Bensimon Twisting and stretching single DNA molecules, Progr. Biophys. Mol. Biol., Volume 74 (2000), p. 115

[9] P. Cluzel; A. Lebrun; C. Heller; R. Lavery; J.L. Viovy; D. Chatenay; F. Caron DNA: An extensible molecule, Science, Volume 271 (1996), p. 792

[10] T.R. Strick; J.F. Allemand; D. Bensimon; V. Croquette Behavior of supercoiled DNA, Biophys. J., Volume 74 (1998), p. 2016

[11] C. Bouchiat; M.D. Wang; J.F. Allemand; T. Strick; S.M. Block; V. Croquette Estimating the persistence length of a worm-like chain molecule from force extension measurements, Biophys. J., Volume 76 (1999), p. 409

[12] S. Smith; Y. Cui; C. Bustamante Overstretching B-DNA: The elastic response of individual double-stranded and single-stranded DNA molecules, Science, Volume 271 (1996), p. 795

[13] J.L. Barrat; J.F. Joanny Persistence length of polyelectrolytes chains, Europhys. Lett., Volume 24 (1993), p. 333

[14] C.G. Baumann; S.B. Smith; V.A. Bloomfield; C. Bustamante Ionic effects on the elasticity of single DNA molecules, Proc. Natl. Acad. Sci. USA, Volume 94 (1997), p. 6185

[15] J. Marko, M. Feig, B.M. Pettitt, Unification of the microscopic atomic fluctuations with mesoscopic elasticity of the DNA double helix, preprint, 2001

[16] S. Cocco; R. Monasson Theoretical study of collective modes in DNA at ambient temperature, J. Chem. Phys., Volume 112 (2000), p. 10017

[17] S.B. Smith; L. Finzi; C. Bustamante Direct mechanical measurements of the elasticity of single DNA molecules by using magnetic beads, Science, Volume 258 (1992), p. 1122

[18] A. Lebrun; R. Lavery Modelling extreme deformations of DNA, Nucl. Acids Res., Volume 24 (1996), p. 2260

[19] P. Cizeau; J.L. Viovy Modelling extreme extension of DNA, Biopolymers, Volume 42 (1997), pp. 383-385

[20] T.L. Hill J. Chem. Phys., 30 (1959), p. 383

[21] B. Zimm; J. Bragg J. Chem. Phys., 31 (1959), p. 526

[22] Y. Kafri; D. Mukamel; L. Peliti Why is the DNA denaturation transition first order?, Phys. Rev. Lett., Volume 85 (2000), p. 4988

[23] I. Rouzina; V.A. Bloomfield Force-induced melting of the DNA double helix, Biophys. J., Volume 80 (2001), pp. 882-893

[24] J.F. Marko DNA under high tension: overstretching, undertwisting, and relaxation dynamics, Phys. Rev. E, Volume 57 (1998), p. 2134

[25] T.R. Strick; J.-F. Allemand; D. Bensimon; A. Bensimon; V. Croquette The elasticity of a single supercoiled DNA molecule, Science, Volume 271 (1996), p. 1835

[26] J.-F. Léger; G. Romano; A. Sarkar; J. Robert; L. Bourdieu; D. Chatenay; J.F. Marko Structural transitions of a twisted and stretched DNA molecule, Phys. Rev. Lett., Volume 83 (1999), p. 1066

[27] J.F. Allemand; D. Bensimon; R. Lavery; V. Croquette Stretched and overwound DNA forms a Pauling-like structure with exposed bases, Proc. Natl. Acad. Sci. USA, Volume 74 (1998), p. 2016

[28] J.F. Marko; E.D. Siggia Statistical mechanics of supercoiled DNA, Phys. Rev. E, Volume 52 (1995), p. 2912

[29] J.F. Marko Supercoiled and braided DNA under tension, Phys. Rev. E, Volume 55 (1997), p. 1758

[30] S. Cocco; R. Monasson Statistical mechanics of torque induced denaturation of DNA, Phys. Rev. Lett., Volume 83 (1999), p. 5178

[31] A. Sarkar; J.-F. Léger; D. Chatenay; J.F. Marko Structural transitions in DNA driven by external force and torque, Phys. Rev. E, Volume 63 (2001), p. 051903

[32] B. Fain; J. Rudnick; S. Ostlund Conformations of linear DNA, Phys. Rev. E, Volume 55 (1997), p. 7364

[33] J.D. Moroz; P. Nelson Torsional directed walks, entropic elasticity, and DNA twist stiffness, Proc. Natl. Acad. Sci. USA, Volume 94 (1997), p. 1441

[34] C. Bouchiat; M. Mézard Elasticity model of a supercoiled DNA molecule, Phys. Rev. Lett., Volume 80 (1998), p. 1556

[35] M.N. Dessinges, B. Maier, M. Peliti, D. Bensimon, V. Croquette, Stretching single stranded DNA, a real self avoiding and interacting heteropolymer, preprint, 2001

[36] Y. Zhang; H. Zhou; Z.C. Ou-Yang Stretching single-stranded DNA: interplay of electrostatic, base-pairing, and base-pair stacking interactions, Biophys. J., Volume 81 (2001), p. 1133

[37] S. Cocco, R. Monasson, J. Yan, A. Sarkar, J.F. Marko, Elastic response of folding polymers, preprint, 2002

[38] C. Bouchiat, Hartree–Fock computation of self avoiding flexible polymer elasticity, preprint, 2001

[39] B. Maier; D. Bensimon; V. Croquette Replication by a single DNA-polymerase of a stretched single strand DNA, Proc. Natl. Acad. Sci. USA, Volume 97 (2000), p. 12002

[40] A. Montanari; M. Mezard Hairpin formation and elongation of biomolecules, Phys. Rev. Lett., Volume 86 (2001), p. 2178

[41] R. Bundschuh; T. Hwa Statistical mechanics of secondary structures fromed by random RNA sequences, Phys. Rev. E, Volume 65 (2002), p. 031903

[42] A. Pagnani; G. Parisi; F. Ricci-Tersenghi Glassy transition in a disordered model for the RNA secondary structure, Phys. Rev. Lett., Volume 84 (2000), p. 2026

[43] H. Isambert; E.D. Siggia Modeling RNA folding paths with pseudoknots: Application to hepatitis delta virus ribozyme, Proc. Natl. Acad. Sci. USA, Volume 97 (2000), p. 6515

[44] Y. Cui; C. Bustamante Pulling a single chromatin fiber reveals the forces that maintain its higher-order structure, Proc. Natl. Acad. Sci. USA, Volume 97 (2000), pp. 127-132

[45] J.F. Marko; E.D. Siggia Driving proteins off DNA using applied tension, Biophys. J., Volume 73 (1997), p. 2173

[46] B. Essevaz-Roulet; U. Bockelmann; F. Heslot Mechanical separation of the complementary strands of DNA, Proc. Natl. Acad. Sci. USA, Volume 94 (1997), p. 11935

[47] K. Breslauer; R. Frank; H. Blocker; L.A. Marky Predicting DNA duplex stability from the base sequence, Proc. Natl. Acad. Sci. USA, Volume 83 (1986), p. 3746

[48] U. Bockelmann; P. Thomen; B. Essevaz-Roulet; V. Viasnoff; F. Heslot Unzipping DNA with optical tweezers: high sequence sensitivity and force flips, Biophys J., Volume 82 (2002), pp. 1537-1553

[49] M. Rief; H. Clausen-Schaumann; H.E. Gaub Sequence-dependent mechanics of single DNA molecules, Nat. Struct. Biol., Volume 6 (1999), p. 346

[50] D.K. Lubensky; D.R. Nelson Pulling pinned polymers and unzipping DNA, Phys. Rev. Lett., Volume 85 (2000), p. 1572

[51] D.K. Lubensky; D.R. Nelson Single molecule statistics and the polynucleotide unzipping transition, Phys. Rev. E, Volume 65 (2002), p. 031917

[52] S. Cocco; R. Monasson; J.F. Marko Force and kinetic barriers to unzipping of the DNA double helix, Proc. Natl. Aca. Sci. USA, Volume 98 (2001), pp. 8608-8613

[53] M. Zuker Calculating nucleic acid secondary structure, Curr. Opin. Struct. Biol., Volume 10 (2000), pp. 303-310

[54] J. Liphardt; B. Onoa; S.B. Smith; I. Tinoco; C. Bustamante Reversible unfolding of single RNA molecules by mechanical force, Science, Volume 292 (2001), pp. 733-737

[55] E.R. Thompson; E.D. Siggia Physical limits on the mechanical measurement of the secondary structure of bio-molecules, Europhys. Lett., Volume 31 (1995), pp. 335-340

[56] U. Bockelmann; B. Essevaz-Roulet; F. Heslot DNA strand separation studied by single molecule force measurements, Phys. Rev. E, Volume 58 (1998), p. 2386

[57] S. Cocco; R. Monasson; J.F. Marko Force and kinetic barriers to initiation of DNA unzipping, Phys. Rev. E, Volume 65 (2002), p. 041907

[58] J.S. Langer Statistical theory of the decay of metastable states, Ann. Phys. (NY), Volume 54 (1967), pp. 258-275

[59] E. Evans; K. Ritchie Dynamic strength of molecular adhesion bonds, Biophys. J., Volume 72 (1997), pp. 1541-1555

[60] S. Cocco, J.F. Marko, R. Monasson, Slow nucleic acid unzipping kinetics from sequence-defined barriers, preprint, 2002

Cité par Sources :

Commentaires - Politique

Ces articles pourraient vous intéresser

Tracking enzymatic steps of DNA topoisomerases using single-molecule micromanipulation

Terence R. Strick; Gilles Charvin; Nynke H. Dekker; ...

C. R. Phys (2002)

Mechanical opening of DNA by micro manipulation and force measurements

Ulrich Bockelmann; B. Essevaz-Roulet; Philippe Thomen; ...

C. R. Phys (2002)