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Annual Review of Biophysics

Volume 43, 2014

Ångström-Precision Optical Traps and Applications*

Abstract

Single-molecule optical-trapping experiments are now resolving the smallest units of motion in biology, including 1-base-pair steps along DNA. This review initially concentrates on the experimental problems with achieving 1-Å instrumental stability and the technical advances necessary to overcome these issues. Instrumental advances are complemented by insights in optical-trapping geometry and single-molecule motility assay development to accommodate the elasticity of biological molecules. I then discuss general issues in applying this measurement capability in the context of precision measurements along DNA. Such enhanced optical-trapping assays are revealing the fundamental step sizes of increasingly complex enzymes, as well as informative pauses in enzymatic motion. This information in turn is providing mechanistic insight into kinetic pathways that are difficult to probe by traditional assays. I conclude with a brief discussion of emerging techniques and future directions.

Keyword(s): DNA, molecular motor, optical tweezers, RNA polymerase, single-molecule force spectroscopy
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2014-05-06
2024-04-20
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Literature Cited

  1. Abbondanzieri EA, Greenleaf WJ, Shaevitz JW, Landick R, Block SM. 1.  2005. Direct observation of base-pair stepping by RNA polymerase. Nature 438:460–65Resolves 1–base pair steps of RNA polymerase along DNA. [Google Scholar]
  2. Arunajadai SG, Cheng W. 2.  2013. Step detection in single-molecule real time trajectories embedded in correlated noise. PLoS ONE 8:e59279 [Google Scholar]
  3. Aubin-Tam ME, Olivares AO, Sauer RT, Baker TA, Lang MJ. 3.  2011. Single-molecule protein unfolding and translocation by an ATP-fueled proteolytic machine. Cell 145:257–67 [Google Scholar]
  4. Bai L, Santangelo TJ, Wang MD. 4.  2006. Single-molecule analysis of RNA polymerase transcription. Annu. Rev. Biophys. Biomol. Struct. 35:343–60 [Google Scholar]
  5. Berg JM, Tymoczhko JL, Stryer L. 5.  2010. Biochemistry New York: W. H. Freeman
  6. Bianco PR, Brewer LR, Corzett M, Balhorn R, Yeh Y. 6.  et al. 2001. Processive translocation and DNA unwinding by individual RecBCD enzyme molecules. Nature 409:374–78 [Google Scholar]
  7. Brau RR, Tarsa PB, Ferrer JM, Lee P, Lang MJ. 7.  2006. Interlaced optical force-fluorescence measurements for single molecule biophysics. Biophys. J. 91:1069–77Significantly improves the combination of optical traps and single-molecule fluorescence by high-frequency interlacing of the trapping and the illumination lasers. [Google Scholar]
  8. Bustamante C, Marko JF, Siggia ED, Smith SB. 8.  1994. Entropic elasticity of λ-phage DNA. Science 265:1599–600 [Google Scholar]
  9. Candelli A, Wuite GJL, Peterman EJG. 9.  2011. Combining optical trapping, fluorescence microscopy and micro-fluidics for single molecule studies of DNA-protein interactions. Phys. Chem. Chem. Phys. 13:7263–72 [Google Scholar]
  10. Carter AR, King GM, Perkins TT. 10.  2007. Back-scattered detection provides atomic-scale localization precision, stability, and registration in 3D. Opt. Express 15:13434–45 [Google Scholar]
  11. Carter AR, King GM, Ulrich TA, Halsey W, Alchenberger D, Perkins TT. 11.  2007. Stabilization of an optical microscope to 0.1 nm in three dimensions. Appl. Opt. 46:421–27 [Google Scholar]
  12. Carter AR, Seol Y, Perkins TT. 12.  2009. Precision surface-coupled optical-trapping assays with 1 base-pair resolution. Biophys. J. 96:2926–34 [Google Scholar]
  13. Carter BC, Vershinin M, Gross SP. 13.  2008. A comparison of step-detection methods: How well can you do?. Biophys. J. 94:306–19 [Google Scholar]
  14. Chemla YR. 14.  2010. Revealing the base pair stepping dynamics of nucleic acid motor proteins with optical traps. Phys. Chem. Chem. Phys. 12:3080–95 [Google Scholar]
  15. Chemla YR, Smith DE. 15.  2012. Single-molecule studies of viral DNA packaging. Adv. Exp. Med. Biol. 726:549–84 [Google Scholar]
  16. Cheng W, Arunajadai SG, Moffitt JR, Tinoco IJ, Bustamante C. 16.  2011. Single-base pair unwinding and asynchronous RNA release by the hepatitis C virus NS3 helicase. Science 333:1746–49 [Google Scholar]
  17. Cheng W, Hou X, Ye F. 17.  2010. Use of tapered amplifier diode laser for biological-friendly high-resolution optical trapping. Opt. Lett. 35:2988–90 [Google Scholar]
  18. Churnside AB, King GM, Carter AR, Perkins TT. 18.  2008. Improved performance of an ultrastable measurement platform using a field-programmable gate array for real-time deterministic control. Proc. SPIE 7042:704205 [Google Scholar]
  19. Cisse I, Mangeol P, Bockelmann U. 19.  2011. DNA unzipping and force measurements with a dual optical trap. Methods Mol. Biol. 783:45–61 [Google Scholar]
  20. Cluzel P, Lebrun A, Heller C, Lavery R, Viovy JL. 20.  et al. 1996. DNA: an extensible molecule. Science 271:792–94 [Google Scholar]
  21. Colquhoun D. 21.  1971. Lectures on Biostatistics; an Introduction to Statistics with Applications in Biology and Medicine Oxford: Clarendon
  22. Comstock MJ, Ha T, Chemla YR. 22.  2011. Ultrahigh-resolution optical trap with single-fluorophore sensitivity. Nat. Methods 8:335–40 [Google Scholar]
  23. Czerwinski F, Richardson AC, Oddershede LB. 23.  2009. Quantifying noise in optical tweezers by Allan variance. Opt. Express 17:13255–69 [Google Scholar]
  24. Dalal RV, Larson MH, Neuman KC, Gelles J, Landick R, Block SM. 24.  2006. Pulling on the nascent RNA during transcription does not alter kinetics of elongation or ubiquitous pausing. Mol. Cell 23:231–39 [Google Scholar]
  25. Denk W, Webb WW. 25.  1990. Optical measurement of picometer displacements of transparent microscopic objects. Appl. Opt. 29:2382–91 [Google Scholar]
  26. Dumont S, Cheng W, Serebrov V, Beran RK, Tinoco IJ. 26.  et al. 2006. RNA translocation and unwinding mechanism of HCV NS3 helicase and its coordination by ATP. Nature 439:105–8 [Google Scholar]
  27. Finer JT, Simmons RM, Spudich JA. 27.  1994. Single myosin molecule mechanics: piconewton forces and nanometre steps. Nature 368:113–19 [Google Scholar]
  28. Galburt EA, Grill SW, Wiedmann A, Lubkowska L, Choy J. 28.  et al. 2007. Backtracking determines the force sensitivity of RNAP II in a factor-dependent manner. Nature 446:820–23 [Google Scholar]
  29. Gelles J, Schnapp BJ, Sheetz MP. 29.  1988. Tracking kinesin-driven movements with nanometre-scale precision. Nature 331:450–53 [Google Scholar]
  30. Goel A, Astumian RD, Herschbach D. 30.  2003. Tuning and switching a DNA polymerase motor with mechanical tension. Proc. Natl. Acad. Sci. USA 100:9699–704 [Google Scholar]
  31. Greenleaf WJ, Woodside MT, Abbondanzieri EA, Block SM. 31.  2005. Passive all-optical force clamp for high-resolution laser trapping. Phys. Rev. Lett. 95:208102Demonstrates a new trapping geometry, the passive force clamp, that provides for improved force control. [Google Scholar]
  32. Greenleaf WJ, Woodside MT, Block SM. 32.  2007. High-resolution, single-molecule measurements of biomolecular motion. Annu. Rev. Biophys. Biomol. Struct. 36:171–90 [Google Scholar]
  33. Hagerman PJ. 33.  1988. Flexibility of DNA. Annu. Rev. Biophys. Biophys. Chem. 17:265–86 [Google Scholar]
  34. Hansen PM, Bhatia VK, Harrit N, Oddershede L. 34.  2005. Expanding the optical trapping range of gold nanoparticles. Nano Lett. 5:1937–42 [Google Scholar]
  35. Herbert KM, Greenleaf WJ, Block SM. 35.  2008. Single-molecule studies of RNA polymerase: motoring along. Annu. Rev. Biochem. 77:149–76 [Google Scholar]
  36. Herbert KM, La Porta A, Wong BJ, Mooney RA, Neuman KC. 36.  et al. 2006. Sequence-resolved detection of pausing by single RNA polymerase molecules. Cell 125:1083–94 [Google Scholar]
  37. Hoffmann A, Neupane K, Woodside MT. 37.  2013. Single-molecule assays for investigating protein misfolding and aggregation. Phys. Chem. Chem. Phys. 15:7934–48 [Google Scholar]
  38. Hohng S, Zhou R, Nahas MK, Yu J, Schulten K. 38.  et al. 2007. Fluorescence-force spectroscopy maps two-dimensional reaction landscape of the Holliday junction. Science 318:279–83 [Google Scholar]
  39. Jannasch A, Demirors AF, van Oostrum PDJ, van Blaaderen A, Schaffer E. 39.  2012. Nanonewton optical force trap employing anti-reflection coated, high-refractive-index titania microspheres. Nat. Photonics 6:469–73 [Google Scholar]
  40. Kalafut B, Visscher K. 40.  2008. An objective, model-independent method for detection of non-uniform steps in noisy signals. Comput. Phys. Commun. 179:716–23 [Google Scholar]
  41. Kauert DJ, Kurth T, Liedl T, Seidel R. 41.  2011. Direct mechanical measurements reveal the material properties of three-dimensional DNA origami. Nano Lett. 11:5558–63 [Google Scholar]
  42. Kerssemakers JW, Munteanu EL, Laan L, Noetzel TL, Janson ME, Dogterom M. 42.  2006. Assembly dynamics of microtubules at molecular resolution. Nature 442:709–12 [Google Scholar]
  43. King GM, Carter AR, Churnside AB, Eberle LS, Perkins TT. 43.  2009. Ultrastable atomic force microscopy: atomic-scale lateral stability and registration in ambient condition. Nano Lett. 9:1451–56Extends optical detection techniques of optical traps to enable an ultrastable atomic force microscope. [Google Scholar]
  44. Landick R. 44.  2006. The regulatory roles and mechanism of transcriptional pausing. Biochem. Soc. Trans. 34:1062–66 [Google Scholar]
  45. Lang MJ, Block SM. 45.  2003. Resource letter: LBOT-1: laser-based optical tweezers. Am. J. Phys. 71:201–15 [Google Scholar]
  46. Lang MJ, Fordyce PM, Engh AM, Neuman KC, Block SM. 46.  2004. Simultaneous, coincident optical trapping and single-molecule fluorescence. Nat. Methods 1:133–39 [Google Scholar]
  47. Larson MH, Landick R, Block SM. 47.  2011. Single-molecule studies of RNA polymerase: one singular sensation, every little step it takes. Mol. Cell 41:249–62 [Google Scholar]
  48. Liphardt J, Onoa B, Smith SB, Tinoco IJ, Bustamante C. 48.  2001. Reversible unfolding of single RNA molecules by mechanical force. Science 292:733–37 [Google Scholar]
  49. Maillard RA, Chistol G, Sen M, Righini M, Tan JY. 49.  et al. 2011. ClpX(P) generates mechanical force to unfold and translocate its protein substrates. Cell 145:459–69 [Google Scholar]
  50. Marko JF, Siggia ED. 50.  1995. Stretching DNA. Macromolecules 28:8759–70 [Google Scholar]
  51. McCann LI, Dykman M, Golding B. 51.  1999. Thermally activated transitions in a bistable three-dimensional optical trap. Nature 402:785–87 [Google Scholar]
  52. Moffitt JR, Chemla YR, Aathavan K, Grimes S, Jardine PJ. 52.  et al. 2009. Intersubunit coordination in a homomeric ring ATPase. Nature 457:446–50Demonstrates a pentameric molecular motor making a rapid series of four 2.5-base pair steps. [Google Scholar]
  53. Moffitt JR, Chemla YR, Izhaky D, Bustamante C. 53.  2006. Differential detection of dual traps improves the spatial resolution of optical tweezers. Proc. Natl. Acad. Sci. USA 103:9006–11 [Google Scholar]
  54. Moffitt JR, Chemla YR, Smith SB, Bustamante C. 54.  2008. Recent advances in optical tweezers. Annu. Rev. Biochem. 77:205–28 [Google Scholar]
  55. Molloy JE, Burns JE, Kendrick-Jones J, Tregear RT, White DCS. 55.  1995. Movement and force produced by a single myosin head. Nature 378:209–12 [Google Scholar]
  56. Morin JA, Cao FJ, Lazaro JM, Arias-Gonzalez JR, Valpuesta JM. 56.  et al. 2012. Active DNA unwinding dynamics during processive DNA replication. Proc. Natl. Acad. Sci. USA 109:8115–20 [Google Scholar]
  57. Myong S, Bruno MM, Pyle AM, Ha T. 57.  2007. Spring-loaded mechanism of DNA unwinding by hepatitis C virus NS3 helicase. Science 317:513–16 [Google Scholar]
  58. Neuman KC, Abbondanzieri EA, Landick R, Gelles J, Block SM. 58.  2003. Ubiquitous transcriptional pausing is independent of RNA polymerase backtracking. Cell 115:437–47 [Google Scholar]
  59. Neuman KC, Block SM. 59.  2004. Optical trapping. Rev. Sci. Instrum. 75:2787–809 [Google Scholar]
  60. Neuman KC, Nagy A. 60.  2008. Single-molecule force spectroscopy: optical tweezers, magnetic tweezers and atomic force microscopy. Nat. Methods 5:491–505 [Google Scholar]
  61. Nugent-Glandorf L, Perkins TT. 61.  2004. Measuring 0.1-nm motion in 1 ms in an optical microscope with differential back-focal-plane detection. Opt. Lett. 29:2611–13 [Google Scholar]
  62. Perkins TT. 62.  2009. Optical traps for single molecule biophysics: a primer. Laser Photonics Rev. 3:203–20 [Google Scholar]
  63. Perkins TT, Dalal RV, Mitsis PG, Block SM. 63.  2003. Sequence-dependent pausing of single lambda exonuclease molecules. Science 301:1914–18 [Google Scholar]
  64. Perkins TT, Li HW, Dalal RV, Gelles J, Block SM. 64.  2004. Forward and reverse motion of single RecBCD molecules on DNA. Biophys. J. 86:1640–48 [Google Scholar]
  65. Perkins TT, Quake SR, Smith DE, Chu S. 65.  1994. Relaxation of a single DNA molecule observed by optical microscopy. Science 264:822–26 [Google Scholar]
  66. Perkins TT, Smith DE, Chu S. 66.  1994. Direct observation of tube-like motion of a single polymer chain. Science 264:819–22 [Google Scholar]
  67. Quake SR, Babcock H, Chu S. 67.  1997. The dynamics of partially extended single molecules of DNA. Nature 388:151–54 [Google Scholar]
  68. Radmacher M, Fritz M, Hansma HG, Hansma PK. 68.  1994. Direct observation of enzyme activity with the atomic force microscope. Science 265:1577–79 [Google Scholar]
  69. Ribeck N, Kaplan DL, Bruck I, Saleh OA. 69.  2010. DnaB helicase activity is modulated by DNA geometry and force. Biophys. J. 99:2170–79 [Google Scholar]
  70. Ribezzi-Crivellari M, Huguet JM, Ritort F. 70.  2013. Counter-propagating dual-trap optical tweezers based on linear momentum conservation. Rev. Sci. Instrum. 84:043104 [Google Scholar]
  71. Roy R, Hohng S, Ha T. 71.  2008. A practical guide to single-molecule FRET. Nat. Methods 5:507–16 [Google Scholar]
  72. Schnitzer MJ, Block SM. 72.  1997. Kinesin hydrolyses one ATP per 8-nm step. Nature 388:386–90 [Google Scholar]
  73. Seol Y, Carpenter AE, Perkins TT. 73.  2006. Gold nanoparticles: enhanced optical trapping and sensitivity coupled with significant heating. Opt. Lett. 31:2429–31 [Google Scholar]
  74. Seol Y, Li J, Nelson PC, Perkins TT, Betterton MD. 74.  2007. Elasticity of short DNA molecules: theory and experiment for contour lengths of 0.6–7 μm. Biophys. J. 93:4360–73 [Google Scholar]
  75. Shaevitz JW, Abbondanzieri EA, Landick R, Block SM. 75.  2003. Backtracking by single RNA polymerase molecules observed at near-base-pair resolution. Nature 426:684–87Introduces the dual-trap assay for studying RNA polymerase with significantly enhanced long-term stability. [Google Scholar]
  76. Sirinakis G, Ren Y, Gao Y, Xi Z, Zhang Y. 76.  2012. Combined versatile high-resolution optical tweezers and single-molecule fluorescence microscopy. Rev. Sci. Instrum. 83:093708 [Google Scholar]
  77. Smith SB, Cui Y, Bustamante C. 77.  1996. Overstretching of B-DNA: the elastic response of individual double-stranded and single-stranded DNA molecules. Science 271:795–99 [Google Scholar]
  78. Stigler J, Ziegler F, Gieseke A, Gebhardt JCM, Rief M. 78.  2011. The complex folding network of single calmodulin molecules. Science 334:512–16Demonstrates the utility of a dual-beam optical trap for providing a highly detailed picture of a single calmodulin molecule folding and unfolding. [Google Scholar]
  79. Sullivan DB, Allan DW, Howe DA, Walls EL. 79.  1990. Characterization of Clocks and Oscillators Washington, DC: USGPO
  80. Svoboda K, Block SM. 80.  1994. Biological applications of optical forces. Annu. Rev. Biophys. Biomol. Struct. 23:247–85 [Google Scholar]
  81. Svoboda K, Block SM. 81.  1994. Force and velocity measured for single kinesin molecules. Cell 77:773–84 [Google Scholar]
  82. Svoboda K, Schmidt CF, Schnapp BJ, Block SM. 82.  1993. Direct observation of kinesin stepping by optical trapping interferometry. Nature 365:721–27 [Google Scholar]
  83. Syed S, Müllner FE, Selvin PR, Sigworth FJ. 83.  2010. Improved hidden Markov models for molecular motors, Part 2: extensions and application to experimental data. Biophys. J. 99:3696–703 [Google Scholar]
  84. Taylor MA, Knittel J, Bowen WP. 84.  2013. Optical lock-in particle tracking in optical tweezers. Opt. Express 21:8018–24 [Google Scholar]
  85. Tinoco I, Chen G, Qu X. 85.  2010. RNA reactions one molecule at a time. Cold Spring Harb. Perspect. Biol. 2:a003624 [Google Scholar]
  86. van Mameren J, Wuite GJ, Heller I. 86.  2011. Introduction to optical tweezers: background, system designs, and commercial solutions. Methods Mol. Biol. 783:1–20 [Google Scholar]
  87. van Oijen AM, Loparo JJ. 87.  2010. Single-molecule studies of the replisome. Annu. Rev. Biophys. 39:429–48 [Google Scholar]
  88. Visscher K, Gross SP, Block SM. 88.  1996. Construction of multiple-beam optical traps with nanometer-resolution position sensing. IEEE J. Sel. Top. Quant. Electron. 2:1066–76 [Google Scholar]
  89. Visscher K, Schnitzer MJ, Block SM. 89.  1999. Single kinesin molecules studied with a molecular force clamp. Nature 400:184–89Demonstrates the application of a force clamp to enable high-resolution studies of single molecules. [Google Scholar]
  90. Wallin AE, Ojala H, Haeggstrom E, Tuma R. 90.  2008. Stiffer optical tweezers through real-time feedback control. Appl. Phys. Lett. 92:224104 [Google Scholar]
  91. Wang MD, Schnitzer MJ, Yin H, Landick R, Gelles J, Block SM. 91.  1998. Force and velocity measured for single molecules of RNA polymerase. Science 282:902–7 [Google Scholar]
  92. Wang MD, Yin H, Landick R, Gelles J, Block SM. 92.  1997. Stretching DNA with optical tweezers. Biophys. J. 72:1335–46 [Google Scholar]
  93. Wen JD, Lancaster L, Hodges C, Zeri AC, Yoshimura SH. 93.  et al. 2008. Following translation by single ribosomes one codon at a time. Nature 452:598–603Observes 1-codon steps of an individual ribosome along RNA. [Google Scholar]
  94. Wuite GJL, Smith SB, Young M, Keller D, Bustamante C. 94.  2000. Single-molecule studies of the effect of template tension on T7 DNA polymerase activity. Nature 404:103–6 [Google Scholar]
  95. Yin H, Landick R, Gelles J. 95.  1994. Tethered particle motion method for studying transcript elongation by a single RNA polymerase molecule. Biophys. J. 67:2468–78 [Google Scholar]
  96. Yin H, Wang MD, Svoboda K, Landick R, Block SM, Gelles J. 96.  1995. Transcription against an applied force. Science 270:1653–57 [Google Scholar]
  97. Yodh JG, Schlierf M, Ha T. 97.  2010. Insight into helicase mechanism and function revealed through single-molecule approaches. Q. Rev. Biophys. 43:185–217 [Google Scholar]
  98. Yu H, Liu X, Neupane K, Gupta AN, Brigley AM. 98.  et al. 2012. Direct observation of multiple misfolding pathways in a single prion protein molecule. Proc. Natl. Acad. Sci. USA 109:5283–88 [Google Scholar]
  99. Zhou J, Ha KS, La Porta A, Landick R, Block SM. 99.  2011. Applied force provides insight into transcriptional pausing and its modulation by transcription factor NusA. Mol. Cell 44:635–46 [Google Scholar]
  100. Zhou J, Schweikhard V, Block SM. 100.  2013. Single-molecule studies of RNAPII elongation. Biochim. Biophys. Acta 1829:29–38 [Google Scholar]
/content/journals/10.1146/annurev-biophys-042910-155223
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Ångström-Precision Optical Traps and Applications*
Annual Review of Biophysics 43, 279 (2014); https://doi.org/10.1146/annurev-biophys-042910-155223
/content/journals/10.1146/annurev-biophys-042910-155223
/content/journals/10.1146/annurev-biophys-042910-155223
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