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Annual Review of Physical Chemistry

Volume 74, 2023

Studies of Local DNA Backbone Conformation and Conformational Disorder Using Site-Specific Exciton-Coupled Dimer Probe Spectroscopy

Abstract

The processes of genome expression, regulation, and repair require direct interactions between proteins and DNA at specific sites located at and near single-stranded–double-stranded DNA (ssDNA–dsDNA) junctions. Here, we review the application of recently developed spectroscopic methods and analyses that combine linear absorbance and circular dichroism spectroscopy with nonlinear 2D fluorescence spectroscopy to study the local conformations and conformational disorder of the sugar-phosphate backbones of ssDNA–dsDNA fork constructs that have been internally labeled with exciton-coupled cyanine (iCy3) dimer probes. With the application of these methods, the (iCy3) dimer can serve as a reliable probe of the mean local conformations and conformational distributions of the sugar-phosphate backbones of dsDNA at various critical positions. The results of our studies suggest a possible structural framework for understanding the roles of DNA breathing in driving the processes of protein–DNA complex assembly and function.

Keyword(s): 2D spectroscopy, DNA breathing, DNA replication, exciton-coupled dimers, protein–DNA interactions, site-specific fluorescence labeling
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/content/journals/10.1146/annurev-physchem-090419-041204
2023-04-24
2024-04-26
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Literature Cited

  1. 1.
    Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P. 2008. Molecular Biology of the Cell New York: Garland Science
  2. 2.
    Kuriyan J, Konfuri B, Wemmer D. 2013. The Molecules of Life New York: Garland Science
  3. 3.
    Phillips R, Kondev J, Theriot J, Garcia H. 2012. Physical Biology of the Cell New York: Garland Science
  4. 4.
    Benkovic SJ, Spiering MM. 2017. Understanding DNA replication by the bacteriophage T4 replisome. J. Biol. Chem. 292:18434–42
     [Google Scholar]
  5. 5.
    Lee W, Gillies JP, Jose D, von Hippel PH, Marcus AH. 2016. Single-molecule FRET studies of cooperative and non-cooperative binding kinetics of the bacteriophage T4 single-stranded DNA binding protein (gp32) to ssDNA lattices at replication fork junctions. Nucleic Acids Res. 44:10691–710
     [Google Scholar]
  6. 6.
    Alberts BM. 1987. Prokaryotic DNA replication mechanisms. Philos. Trans. R. Soc. B 317:395–420
     [Google Scholar]
  7. 7.
    Barry J, Wong ML, Alberts B. 2018. In vitro reconstitution of DNA replication initiated by genetic recombination: a T4 bacteriophage model for a type of DNA synthesis important for all cells. Mol. Biol. Cell 30:146–59
     [Google Scholar]
  8. 8.
    Sakabe K, Okazaki RA. 1966. A unique property of the replicating region of chromosomal DNA. Biochim. Biophys. Acta Nucl. Acids Protein Synth. 129:651–54
     [Google Scholar]
  9. 9.
    Kozlov AG, Shinn MK, Lohman TM. 2019. Regulation of nearest-neighbor cooperative binding of E. coli SSB protein to DNA. Biophys. J. 117:2120–40
     [Google Scholar]
  10. 10.
    von Hippel PH, Marcus AH. 2019. The many roles of binding cooperativity in the control of DNA replication. Biophys. J. 117:2143–46
     [Google Scholar]
  11. 11.
    von Hippel PH, Johnson NP, Marcus AH. 2013. 50 years of DNA ‘breathing’: reflections on old and new approaches. Biopolymers 99:923–54
     [Google Scholar]
  12. 12.
    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. PNAS 110:17320–25
     [Google Scholar]
  13. 13.
    Jordan SR, Pabo CO. 1988. Structure of lambda complex at 2.5 Å resolution: details of the repressor-operator interactions. Science 242:893–99
     [Google Scholar]
  14. 14.
    Kringle L, Sawaya N, Widom JR, Adams C, Raymer MG et al. 2018. Temperature-dependent conformations of exciton-coupled Cy3 dimers in double-stranded DNA. J. Chem. Phys. 148:085101
     [Google Scholar]
  15. 15.
    Heussman D, Kittell J, Kringle L, Tamimi A, von Hippel PH, Marcus AH. 2019. Measuring local conformations and conformational disorder of (Cy3)2 dimers labeled DNA fork junctions using absorbance, circular dichroism and two-dimensional fluorescence spectroscopy. Faraday Disc. 216:211–35
     [Google Scholar]
  16. 16.
    Heussman D, Kittell J, von Hippel PH, Marcus AH. 2022. Temperature-dependent local conformations and conformational distributions of cyanine dimer labeled single-stranded–double-stranded DNA junctions by 2D fluorescence spectroscopy. J. Chem. Phys. 156:045101–1-23
     [Google Scholar]
  17. 17.
    Levitus M, Ranjit S. 2011. Cyanine dyes in biophysical research: the photophysics of polymethine fluorescent dyes in biomolecular environments. Q. Rev. Biophys. 44:123–51
     [Google Scholar]
  18. 18.
    Murphy MC, Rasnik I, Cheng W, Lohman TM, Ha T. 2004. Probing single-stranded DNA conformational flexibility using fluorescence spectroscopy. Biophys. J. 86:2530–37
     [Google Scholar]
  19. 19.
    Lee W, von Hippel PH, Marcus AH. 2014. Internally labeled Cy3/Cy5 DNA constructs show greatly enhanced photostability in single-molecule FRET experiments. Nucleic Acids Res. 42:5967–77
     [Google Scholar]
  20. 20.
    Jia K, Wan Y, Xia A, Li S, Gong F, Yang G 2007. Characterization of photoinduced isomerization and intersystem crossing of the cyanine dye Cy3. J. Phys. Chem. A 111:1593–97
     [Google Scholar]
  21. 21.
    Fulton RL, Gouterman M. 1961. Vibronic coupling. I. Mathematical treatment for two electronic states. J. Chem. Phys. 35:1059–71
     [Google Scholar]
  22. 22.
    Zhao Z, Spano FC. 2007. Multiple mode exciton-phonon coupling: applications to photoluminescence in oligothiophene thin films. Phys J. Chem. C 111:6113–23
     [Google Scholar]
  23. 23.
    Sorour M, Marcus AH, Matsika S. 2022. Modeling the electronic absorption spectra of the indocarbocyanine Cy3. Molecules 27:134062
     [Google Scholar]
  24. 24.
    Hestand NJ, Spano FC. 2018. Expanded theory of H- and J-molecular aggregates: the effects of vibronic coupling and intermolecular charge transfer. Chem. Rev. 118:7069–163
     [Google Scholar]
  25. 25.
    Fulton RL, Gouterman M. 1964. Vibronic coupling. II. Spectra of dimers. J. Chem. Phys. 41:2280–86
     [Google Scholar]
  26. 26.
    Eisfeld A, Braun L, Stunz WT, Briggs JS, Engel V. 2005. Vibronic energies and spectra of molecular dimers. J. Chem. Phys. 122:134103–1-10
     [Google Scholar]
  27. 27.
    Kistler KA, Pochas CM, Yamagata H, Matsika S, Spano FC. 2011. Absorption, circular dichroism, and photoluminescence in perylene diimide bichromophores: polarization-dependent H- and J-aggregate behavior. J. Phys. Chem. B 116:77–86
     [Google Scholar]
  28. 28.
    Howard IA, Zutterman F, Deroover G, Lamoen D, Van Alsenoy C. 2004. Approaches to calculation of exciton interaction energies for a molecular dimer. J. Phys. Chem. B 108:19155–62
     [Google Scholar]
  29. 29.
    Czikklely VHDF, Kuhn H. 1970. Extended dipole model for aggregates of dye molecules. Chem. Phys. Lett. 6:207–10
     [Google Scholar]
  30. 30.
    Kistler KA, Spano FC, Matsika S. 2013. A benchmark of excitonic couplings derived from atomic transition charges. J. Phys. Chem. B 117:2032–44
     [Google Scholar]
  31. 31.
    Sorour MI, Kistler KA, Marcus AH, Matsika S. 2021. Accurate modeling of exciton coupling in cyanine dye Cy3. J. Phys. Chem. A 125:7852–66
     [Google Scholar]
  32. 32.
    Nordén B, Rodger A, Dafforn T. 2010. Linear Dichroism and Circular Dichroism: A Textbook on Polarized-Light Spectroscopy Cambridge, UK: RSC Publ.
  33. 33.
    Förster T. 1965. Delocalized excitation and excitation transfer Bull. 18. Div. Biol. Med., U.S. Atomic Energy Comm., Fla. State Univ. Tallahassee:
  34. 34.
    Harada N, Berova N 2012. Spectroscopic analysis: exciton circular dichroism for chiral analysis. Comprehensive Chirality EM Carreira, H Yamamoto 449–77. Amsterdam: Elsevier
     [Google Scholar]
  35. 35.
    Mukamel S, Abramavicius D, Yang L, Zhuang W, Schweigert IV, Voronine DV. 2009. Coherent multidimensional optical probes for electron correlations and exciton dynamics: from NMR to X-rays. Acc. Chem. Res. 42:553–62
     [Google Scholar]
  36. 36.
    Jonas DM. 2003. Optical analogs of 2D NMR. Science 300:1515–17
     [Google Scholar]
  37. 37.
    Reppert M, Tokmakoff A. 2016. Computational amide I 2D IR spectroscopy as a probe of protein structure and dynamics. Annu. Rev. Phys. Chem. 67:359–86
     [Google Scholar]
  38. 38.
    Ghosh A, Ostrander JS, Zanni MT. 2017. Watching proteins wiggle: mapping structures with two-dimensional infrared spectroscopy. Chem. Rev. 117:10726–59
     [Google Scholar]
  39. 39.
    Laage D, Elsaesser T, Hynes JT. 2017. Water dynamics in the hydration shells of biomolecules. Chem. Rev. 117:10694–725
     [Google Scholar]
  40. 40.
    Tian P, Keusters D, Suzaki Y, Warren WS. 2003. Femtosecond phase-coherent two-dimensional spectroscopy. Science 300:1553–55
     [Google Scholar]
  41. 41.
    Tekavec PF, Dyke TR, Marcus AH. 2006. Wave packet interferometry and quantum state reconstruction by acousto-optic phase modulation. J. Chem. Phys. 125:194303–1-19
     [Google Scholar]
  42. 42.
    Tekavec PF, Lott GA, Marcus AH. 2007. Fluorescence-detected two-dimensional electronic coherence spectroscopy by acousto-optic phase modulation. J. Chem. Phys. 127:214307
     [Google Scholar]
  43. 43.
    Nardin G, Autry TM, Silverman KL, Cundiff ST. 2013. Multidimensional coherent photocurrent spectroscopy of a semiconductor nanostructure. Opt. Express 21:28617–27
     [Google Scholar]
  44. 44.
    Karki KJ, Widom JR, Seibt J, Moody I, Lonergan MC et al. 2014. Coherent two-dimensional photocurrent spectroscopy in a PbS quantum dot photocell. Nat. Commun. 5:5869–1-7
     [Google Scholar]
  45. 45.
    De AK, Monahan D, Dawlaty JM, Fleming GR. 2014. Two-dimensional fluorescence-detected coherent spectroscopy with absolute phasing by confocal imaging of a dynamic grating and 27-step phase-cycling. J. Chem. Phys. 140:194201
     [Google Scholar]
  46. 46.
    Bruder L, Mudrich M, Stienkemeier F. 2015. Phase-modulated electronic wave packet interferometry reveals high resolution spectra of free Rb atoms and Rb*He molecules. Phys. Chem. Chem. Phys. 17:23877–85
     [Google Scholar]
  47. 47.
    Grégoire P, Kandada ARS, Vella E, Tao C, Leonelli R, Silva C. 2017. Incoherent population mixing of contributions to phase-modulated two-dimensional coherent excitation spectra. J. Chem. Phys. 147:114201
     [Google Scholar]
  48. 48.
    Tiwari V, Matutes YA, Konar A, Yu Z, Ptaszek M et al. 2018. Strongly coupled bacteriochlorin dyad studied using phase-modulated fluorescence-detected two-dimensional electronic spectroscopy. Opt. Express 28:22327–41
     [Google Scholar]
  49. 49.
    Lavoie JTL, Smith B, Marcus AH, Raymer MG. 2020. Phase-modulated interferometry, spectroscopy and refractometry using entangled photon-pairs. Adv. Quantum Tech. 3:1900114
     [Google Scholar]
  50. 50.
    Tamimi A, Landes T, Lavoie J, Raymer MG, Marcus AH. 2020. Fluorescence-detected Fourier transform electronic spectroscopy by phase-tagged photon counting. Opt. Express 28:25194–214
     [Google Scholar]
  51. 51.
    Fuller FD, Ogilvie JP. 2015. Experimental implementations of two-dimensional Fourier transform electronic spectroscopy. Annu. Rev. Phys. Chem. 66:667–90
     [Google Scholar]
  52. 52.
    Tiwari V. 2021. Multidimensional electronic spectroscopy in high-definition—combining spectral, temporal, and spatial resolutions. J. Chem. Phys. 154:230901–1-17
     [Google Scholar]
  53. 53.
    Siemens ME, Moody G, Li H, Bristow AD, Cundiff ST. 2010. Resonance lineshapes in two-dimensional Fourier transform spectroscopy. Opt. Express 18:17699–708
     [Google Scholar]
  54. 54.
    Israels B, Albrecht C, Dang A, Barney M, von Hippel PH, Marcus AH. 2021. Sub-millisecond conformational transitions of single-stranded DNA lattices by photon correlation single-molecule FRET. J. Phys. Chem. B 125:9426–40
     [Google Scholar]
  55. 55.
    Beyerle ER, Dinpahjooh M, Ji H, von Hippel PH, Marcus AH, Guenza MG 2021. Dinucleotides as simple models of the base stacking-unstacking component of DNA ‘breathing’ mechanisms. Nucleic Acids Res. 49:1872–85
     [Google Scholar]
  56. 56.
    Privalov PL, Griko YV, Venyaminov SY. 1986. Cold denaturation of myoglobin. J. Mol. Biol. 190:487–98
     [Google Scholar]
  57. 57.
    Mikulecky PJ, Feig AL. 2002. Cold denaturation of the hammerhead ribozyme. J. Am. Chem. Soc. 124:890–91
     [Google Scholar]
  58. 58.
    Mikulecky PJ, Feig AL. 2006. Heat capacity changes associated with nucleic acid folding. Biopolymers 82:38–58
     [Google Scholar]
  59. 59.
    Vaitiekunas P, Crane-Robinson C, Privalov PL. 2015. The energetic basis of the DNA double helix: a combined microcalorimetric approach. Nucleic Acids Res. 43:8577–89
     [Google Scholar]
  60. 60.
    Phelps C, Israels B, Jose D, Marsh MC, von Hippel PH, Marcus AH 2016. Using multi-order time correlation functions (TCFs) to elucidate biomolecular reaction pathways from microsecond single-molecule fluorescence experiments. J. Phys. Chem. B 120:13003–16
     [Google Scholar]
  61. 61.
    Phelps C, Israels B, Jose D, Marsh MC, von Hippel PH, Marcus AH 2017. Using microsecond single-molecule FRET to determine the assembly pathways of T4 ssDNA binding protein onto model DNA replication forks. PNAS 114:E3612–21
     [Google Scholar]
  62. 62.
    Widom JR, Johnson NP, von Hippel PH, Marcus AH. 2013. Solution conformation of 2-aminopurine (2-AP) dinucleotide by ultraviolet 2D fluorescence spectroscopy (UV-2D FS). New J. Phys. 15:025028–43
     [Google Scholar]
  63. 63.
    Datta K, Johnson NP, Villani G, Marcus AH, von Hippel PH. 2012. Characterization of the 6-methyl isoxanthopterin (6-MI) base analog dimer, a spectroscopic probe for monitoring guanine base conformations at specific sites in nucleic acids. Nucleic Acids Res. 40:1191–202
     [Google Scholar]
  64. 64.
    Ji H, Johnson NP, von Hippel PH, Marcus AH. 2019. Local DNA base conformation and ligand intercalation in DNA constructs containing optical probes. Biophys. J. 117:1101–15
     [Google Scholar]
  65. 65.
    Camel BR, Jose D, Meze K, Dang A, von Hippel PH. 2021. Mapping DNA conformations and interactions within the binding cleft of bacteriophage T4 single-stranded DNA binding protein (gp32) at single nucleotide resolution. Nucleic Acids Res. 49:916–27
     [Google Scholar]
  66. 66.
    Whaley-Mayda L, Guha A, Tokmakoff A. 2022. Resonance conditions, detection quality, and single-molecule sensitivity in fluorescence-encoded infrared vibrational spectroscopy. J. Chem. Phys. 156:174202-1-15
     [Google Scholar]
  67. 67.
    Raymer MG, Landes T, Marcus AH. 2021. Entangled two-photon absorption by atoms and molecules: a quantum optics tutorial. J. Chem. Phys. 155:081501-1–25
     [Google Scholar]
  68. 68.
    Landes T, Raymer MG, Allgaier M, Merkouche S, Smith BJ, Marcus AH. 2021. Quantifying the enhancement of two-photon absorption due to spectral-temporal entanglement. Optics Express 29:20022–33
     [Google Scholar]
  69. 69.
    Landes T, Merkouche S, Allgaier M, Smith BJ, Marcus AH, Raymer MG. 2021. Experimental feasibility of molecular two-photon absorption with isolated time-frequency-entangled photon pairs. Phys. Rev. Res. 3:033154–1-9
     [Google Scholar]
/content/journals/10.1146/annurev-physchem-090419-041204
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Studies of Local DNA Backbone Conformation and Conformational Disorder Using Site-Specific Exciton-Coupled Dimer Probe Spectroscopy
Annual Review of Physical Chemistry 74, 245 (2023); https://doi.org/10.1146/annurev-physchem-090419-041204
/content/journals/10.1146/annurev-physchem-090419-041204
/content/journals/10.1146/annurev-physchem-090419-041204
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