Advertisement

Excited States in DNA Strands Investigated by Ultrafast Laser Spectroscopy

  • Jinquan Chen
  • Yuyuan Zhang
  • Bern KohlerEmail author
Chapter
Part of the Topics in Current Chemistry book series (TOPCURRCHEM, volume 356)

Abstract

Ultrafast laser experiments on carefully selected DNA model compounds probe the effects of base stacking, base pairing, and structural disorder on excited electronic states formed by UV absorption in single and double DNA strands. Direct π-orbital overlap between two stacked bases in a dinucleotide or in a longer single strand creates new excited states that decay orders of magnitude more slowly than the generally subpicosecond excited states of monomeric bases. Half or more of all excited states in single strands decay in this manner. Ultrafast mid-IR transient absorption experiments reveal that the long-lived excited states in a number of model compounds are charge transfer states formed by interbase electron transfer, which subsequently decay by charge recombination. The lifetimes of the charge transfer states are surprisingly independent of how the stacked bases are oriented, but disruption of π-stacking, either by elevating temperature or by adding a denaturing co-solvent, completely eliminates this decay channel. Time-resolved emission measurements support the conclusion that these states are populated very rapidly from initial excitons. These experiments also reveal the existence of populations of emissive excited states that decay on the nanosecond time scale. The quantum yield of these states is very small for UVB/UVC excitation, but increases at UVA wavelengths. In double strands, hydrogen bonding between bases perturbs, but does not quench, the long-lived excited states. Kinetic isotope effects on the excited-state dynamics suggest that intrastrand electron transfer may couple to interstrand proton transfer. By revealing how structure and non-covalent interactions affect excited-state dynamics, on-going experimental and theoretical studies of excited states in DNA strands can advance understanding of fundamental photophysics in other nanoscale systems.

Keywords

Base pairing Base stacking Charge transfer state DNA photophysics Excimer Excited-state dynamics Exciton Femtosecond transient absorption Proton-coupled electron transfer 

Abbreviations

2AP

2-Aminopurine

8-oxo-dGuo

8-Oxo-7,8-dihydro-2′-deoxyguanosine

A

Adenine

AMP

Adenosine 5′-monophosphate

ATP

Adenosine 5′-triphosphate

C

Cytosine

CASPT2

Complete active space with second-order perturbation theory

CD

Circular dichroism

CI

Conical intersection

CPD

Cyclobutane pyrimidine dimer

CR

Charge recombination

CT

Charge transfer

dAMP

2′-Deoxyadenosine 5′-monophosphate

DFT

Density functional theory

ECCD

Exciton-coupled circular dichroism

ESA

Excited-state absorption

ESPT

Excited-state proton transfer

ET

Electron transfer

FC

Franck–Condon

FTIR

Fourier-transformed infrared spectroscopy

FU

Fluorescence upconversion

G

Guanine

GSB

Ground-state bleaching

IC

Internal conversion

IET

Intermolecular energy transfer

KIE

Kinetic isotope effect

MCT

Mercury-cadmium-telluride

O

8-Oxo-7,8-dihydro-2′-deoxyguanosine (in a DNA sequence)

PCET

Proton-coupled electron transfer

PMT

Photomultiplier tube

PT

Proton transfer

QM/MM

Quantum mechanical/molecular mechanical

RI-ADC(2)

Algebraic diagrammatic construction to second-order with resolution of the identity

T

Thymine

TA

Transient absorption

TCSPC

Time-correlated single photon counting

TD-DFT

Time-dependent density functional theory

TRIR

Time-resolved infrared spectroscopy

U

Uracil

UV

Ultraviolet

VC

Vibrational cooling

VUV

Vacuum ultraviolet

WC

Watson–Crick

Notes

Acknowledgments

This work has been supported by grants from the Chemical Structure, Dynamics and Mechanisms Program of the National Science Foundation and from the NASA Astrobiology Program. Many current and former students, postdoctoral researchers, and collaborators have contributed to this work over the past 15 years. Their efforts, which are documented in the papers cited in this chapter, have been indispensible to the success of this work.

References

  1. 1.
    Kohler B (2010) J Phys Chem Lett 1:2047Google Scholar
  2. 2.
    Gustavsson T, Improta R, Markovitsi D (2010) J Phys Chem Lett 1:2025Google Scholar
  3. 3.
    Crespo-Hernández CE, Cohen B, Hare PM, Kohler B (2004) Chem Rev 104:1977Google Scholar
  4. 4.
    Middleton CT, de La Harpe K, Su C, Law YK, Crespo-Hernández CE, Kohler B (2009) Annu Rev Phys Chem 60:217Google Scholar
  5. 5.
    Kleinermanns K, Nachtigallova D, de Vries MS (2013) Int Rev Phys Chem 32:308Google Scholar
  6. 6.
    Takaya T, Su C, de La Harpe K, Crespo-Hernández CE, Kohler B (2008) Proc Natl Acad Sci USA 105:10285Google Scholar
  7. 7.
    Schreier WJ, Schrader TE, Koller FO, Gilch P, Crespo-Hernández CE, Swaminathan VN, Carell T, Zinth W, Kohler B (2007) Science 315:625Google Scholar
  8. 8.
    Schreier WJ, Kubon J, Regner N, Haiser K, Schrader TE, Zinth W, Clivio P, Gilch P (2009) J Am Chem Soc 131:5038Google Scholar
  9. 9.
    Su C, Middleton CT, Kohler B (2012) J Phys Chem B 116:10266Google Scholar
  10. 10.
    Ward DC, Reich E, Stryer L (1969) J Biol Chem 244:1228Google Scholar
  11. 11.
    Rist MJ, Marino JP (2002) Curr Org Chem 6:775Google Scholar
  12. 12.
    Thompson KC, Miyake N (2005) J Phys Chem B 109:6012Google Scholar
  13. 13.
    Crespo-Hernández CE, Cohen B, Kohler B (2005) Nature 436:1141Google Scholar
  14. 14.
    Kang H, Lee KT, Jung B, Ko YJ, Kim SK (2002) J Am Chem Soc 124:12958Google Scholar
  15. 15.
    Ullrich S, Schultz T, Zgierski MZ, Stolow A (2004) J Am Chem Soc 126:2262Google Scholar
  16. 16.
    Smith VR, Samoylova E, Ritze HH, Radloff W, Schultz T (2010) Phys Chem Chem Phys 12:9632Google Scholar
  17. 17.
    Banyasz A, Vayá I, Changenet-Barret P, Gustavsson T, Douki T, Markovitsi D (2011) J Am Chem Soc 133:5163Google Scholar
  18. 18.
    Towrie M, Grills DC, Dyer J, Weinstein JA, Matousek P, Barton R, Bailey PD, Subramaniam N, Kwok WM, Ma CS, Phillips D, Parker AW, George MW (2003) Appl Spectrosc 57:367Google Scholar
  19. 19.
    Towrie M, Doorley GW, George MW, Parker AW, Quinn SJ, Kelly JM (2009) Analyst 134:1265Google Scholar
  20. 20.
    Oliver TAA, Zhang Y, Ashfold MNR, Bradforth SE (2011) Faraday Discuss 150:439Google Scholar
  21. 21.
    Zhang Y, Chen J, Kohler B (2013) J Phys Chem A 117:6771Google Scholar
  22. 22.
    Chen J, Thazhathveetil AK, Lewis FD, Kohler B (2013) J Am Chem Soc 135:10290Google Scholar
  23. 23.
    Kwok W-M, Ma C, Phillips DL (2006) J Am Chem Soc 128:11894Google Scholar
  24. 24.
    Karunakaran V, Kleinermanns K, Improta R, Kovalenko SA (2009) J Am Chem Soc 131:5839Google Scholar
  25. 25.
    Pecourt J-ML, Peon J, Kohler B (2000) J Am Chem Soc 122:9348Google Scholar
  26. 26.
    Pecourt J-ML, Peon J, Kohler B (2001) J Am Chem Soc 123:10370Google Scholar
  27. 27.
    Crespo-Hernández CE, Kohler B (2004) J Phys Chem B 108:11182Google Scholar
  28. 28.
    Jou F-Y, Freeman GR (1979) J Phys Chem 83:2383Google Scholar
  29. 29.
    Hare PM, Crespo-Hernández CE, Kohler B (2007) Proc Natl Acad Sci U S A 104:435Google Scholar
  30. 30.
    Middleton CT, Cohen B, Kohler B (2007) J Phys Chem A 111:10460Google Scholar
  31. 31.
    Elles CG, Rivera CA, Zhang Y, Pieniazek PA, Bradforth SE (2009) J Chem Phys 130:13Google Scholar
  32. 32.
    Kovalenko SA, Dobryakov AL, Ruthmann J, Ernsting NP (1999) Phys Rev A 59:2369Google Scholar
  33. 33.
    Jailaubekov AE, Bradforth SE (2005) Appl Phys Lett 87Google Scholar
  34. 34.
    Tauber MJ, Mathies RA, Chen XY, Bradforth SE (2003) Rev Sci Instrum 74:4958Google Scholar
  35. 35.
    Zhang Y, Improta R, Kohler B (2014) Phys Chem Chem Phys 16:1487Google Scholar
  36. 36.
    Gustavsson T, Sharonov A, Markovitsi D (2002) Chem Phys Lett 351:195Google Scholar
  37. 37.
    Peon J, Zewail AH (2001) Chem Phys Lett 348:255Google Scholar
  38. 38.
    Gustavsson T, Sharonov A, Onidas D, Markovitsi D (2002) Chem Phys Lett 356:49Google Scholar
  39. 39.
    Pancur T, Schwalb NK, Renth F, Temps F (2005) Chem Phys 313:199Google Scholar
  40. 40.
    Markovitsi D, Gustavsson T, Talbot F (2007) Photochem Photobiol Sci 6:717Google Scholar
  41. 41.
    Markovitsi D, Onidas D, Talbot F, Marguet S, Gustavsson T, Lazzarotto E (2006) J Photochem Photobiol. A 183:1Google Scholar
  42. 42.
    Schweizer MP, Broom AD, Ts'o POP, Hollis DP (1968) J Am Chem Soc 90:1042Google Scholar
  43. 43.
    Broom AD, Schweizer MP, Ts’o POP (1967) J Am Chem Soc 89:3612Google Scholar
  44. 44.
    Valdes-Aguilera O, Neckers DC (1989) Acc Chem Res 22:171Google Scholar
  45. 45.
    Bloomfield VA, Crothers DM, Tinoco I Jr (1974) Physical chemistry of nucleic acids. Harper & Row, New YorkGoogle Scholar
  46. 46.
    Gray DM, Ratliff RL, Vaughan MR (1992) Methods Enzymol 211:389Google Scholar
  47. 47.
    Woody RW (1995) Biochem Spectroscopy 246:34Google Scholar
  48. 48.
    Berova N, Di Bari L, Pescitelli G (2007) Chem Soc Rev 36:914Google Scholar
  49. 49.
    Kypr J, Kejnovska I, Renciuk D, Vorlickova M (2009) Nucleic Acids Res 37:1713Google Scholar
  50. 50.
    Ke C, Humeniuk M, S-Gracz H, Marszalek PE (2007) Phys Rev Lett 99:018302Google Scholar
  51. 51.
    Seol Y, Skinner GM, Visscher K, Buhot A, Halperin A (2007) Phys Rev Lett 98:158103Google Scholar
  52. 52.
    Hatters DM, Wilson L, Atcliffe BW, Mulhern TD, Guzzo-Pernell N, Howlett GJ (2001) Biophys J 81:371Google Scholar
  53. 53.
    Mills JB, Vacano E, Hagerman PJ (1999) J Mol Biol 285:245Google Scholar
  54. 54.
    Banáš P, Mládek A, Otyepka M, Zgarbová M, Jurečka P, Svozil D, Lankaš F, Šponer J (2012) J Chem Theory Comput 8:2448Google Scholar
  55. 55.
    Chen AA, García AE (2013) Proc Natl Acad Sci U S A 110:16820Google Scholar
  56. 56.
    Olson WK, Bansal M, Burley SK, Dickerson RE, Gerstein M, Harvey SC, Heinemann U, Lu X-J, Neidle S, Shakked Z, Sklenar H, Suzuki M, Tung C-S, Westhof E, Wolberger C, Berman HM (2001) J Mol Biol 313:229Google Scholar
  57. 57.
    Rose IA, Hanson KR, Wilkinson KD, Wimmer MJ (1980) Proc Natl Acad Sci U S A 77:2439Google Scholar
  58. 58.
    Chen J, Kohler B (2014) J Am Chem Soc 136:6362Google Scholar
  59. 59.
    Olaso-González G, Merchán M, Serrano-Andrés L (2009) J Am Chem Soc 131:4368Google Scholar
  60. 60.
    Hunter RS, van Mourik T (2012) J Comput Chem 33:2161Google Scholar
  61. 61.
    Florián J, Šponer J, Warshel A (1999) J Phys Chem B 103:884Google Scholar
  62. 62.
    Jafilan S, Klein L, Hyun C, Florián J (2012) J Phys Chem B 116:3613Google Scholar
  63. 63.
    Šponer J, Leszczyński J, Hobza P (1996) J Phys Chem 100:5590Google Scholar
  64. 64.
    Šponer J, Šponer JE, Mládek A, Jurečka P, Bánaš P, Otyepka M (2013) Biopolymers 99:978Google Scholar
  65. 65.
    Ts'o POP, Melvin IS, Olson AC (1963) J Am Chem Soc 85:1289Google Scholar
  66. 66.
    Ts'o POP, Chan SI (1964) J Am Chem Soc 86:4176Google Scholar
  67. 67.
    Eimer W, Dorfmuller T (1992) J Phys Chem 96:6790Google Scholar
  68. 68.
    Hamlin RM Jr, Lord RC, Rich A (1965) Science (Washington, DC, USA) 148:1734Google Scholar
  69. 69.
    Kyogoku Y, Lord RC, Rich A (1967) J Am Chem Soc 89:496Google Scholar
  70. 70.
    Schwalb NK, Temps F (2007) J Am Chem Soc 129:9272Google Scholar
  71. 71.
    Schwalb NK, Michalak T, Temps F (2009) J Phys Chem B 113:16365Google Scholar
  72. 72.
    Plützer C, Hunig I, Kleinermanns K (2003) Phys Chem Chem Phys 5:1158Google Scholar
  73. 73.
    Asami H, Yagi K, Ohba M, Urashima S, Saigusa H (2013) Chem Phys 419:84Google Scholar
  74. 74.
    Šponer J, Jurečka P, Marchan I, Luque FJ, Orozco M, Hobza P (2006) Chem Eur J 12:2854Google Scholar
  75. 75.
    Lowe MJ, Schellman JA (1972) J Mol Biol 65:91Google Scholar
  76. 76.
    Brahms J, Michelson AM, van Holde KE (1966) J Mol Biol 15:467Google Scholar
  77. 77.
    Powell JT, Richards EG, Gratzer WB (1972) Biopolymers 11:235Google Scholar
  78. 78.
    Olsthoorn CSM, Bostelaar LJ, De Rooij JFM, Van Boom JH, Altona C (1981) Eur J Biochem 115:309Google Scholar
  79. 79.
    Buhot A, Halperin A (2004) Phys Rev E 70:020902Google Scholar
  80. 80.
    Donohue J, Trueblood KN (1960) J Mol Biol 2:363Google Scholar
  81. 81.
    Cohen B, Larson MH, Kohler B (2008) Chem Phys 350:165Google Scholar
  82. 82.
    Schwalb NK, Temps F (2009) J Photochem Photobiol. A 208:164Google Scholar
  83. 83.
    Miannay FA, Banyasz A, Gustavsson T, Markovitsi D (2009) J Phys Chem C 113:11760Google Scholar
  84. 84.
    Nguyen Thuan D, Haselsberger R, Michel-Beyerle M-E, Anh Tuan P (2013) ChemPhysChem 14:2667Google Scholar
  85. 85.
    Hunger K, Buschhaus L, Biemann L, Braun M, Kovalenko S, Improta R, Kleinermanns K (2013) Chem Eur J 19:5425Google Scholar
  86. 86.
    Changenet-Barret P, Hua Y, Markovitsi D (2014) Electronic excitations in guanine quadruplexes. Springer, Berlin Heidelberg, p 1Google Scholar
  87. 87.
    Schwalb NK, Temps F (2008) Science 322:243Google Scholar
  88. 88.
    Brahms J, Mommaerts WFH (1964) J Mol Biol 10:73Google Scholar
  89. 89.
    Cassani GR, Bollum FJ (1969) Biochemistry 8:3928Google Scholar
  90. 90.
    Ke CH, Loksztejn A, Jiang Y, Kim M, Humeniuk M, Rabbi M, Marszalek PE (2009) Biophys J 96:2918Google Scholar
  91. 91.
    Applequist J, Damle V (1966) J Am Chem Soc 88:3895Google Scholar
  92. 92.
    Luzzati V, Mathis A, Masson F, Witz J (1964) J Mol Biol 10:28Google Scholar
  93. 93.
    Nonin S, Leroy J-L, Gueron M (1995) Biochemistry 34:10652Google Scholar
  94. 94.
    Davis JT (2004) Angew Chem Int Ed 43:668Google Scholar
  95. 95.
    Gehring K, Leroy JL, Guéron M (1993) Nature 363:561Google Scholar
  96. 96.
    Leroy JL, Gueron M, Mergny JL, Helene C (1994) Nucleic Acids Res 22:1600Google Scholar
  97. 97.
    Holm AIS, Kohler B, Hoffmann SV, Nielsen SB (2010) Biopolymers 93:429Google Scholar
  98. 98.
    Plasser F, Lischka H (2012) J Chem Theory Comput 8:2777Google Scholar
  99. 99.
    Blancafort L, Voityuk AA (2014) J Chem Phys 140:8Google Scholar
  100. 100.
    Kasha M (1963) Radiat Res 20:55Google Scholar
  101. 101.
    Bouvier B, Gustavsson T, Markovitsi D, Millié P (2002) Chem Phys 275:75Google Scholar
  102. 102.
    Czader A, Bittner ER (2008) J Chem Phys 128:035101Google Scholar
  103. 103.
    Scholes GD, Ghiggino KP (1994) J Phys Chem 98:4580Google Scholar
  104. 104.
    Gould IR, Young RH, Mueller LJ, Albrecht AC, Farid S (1994) J Am Chem Soc 116:8188Google Scholar
  105. 105.
    Wang YS, Haze O, Dinnocenzo JP, Farid S, Farid RS, Gould IR (2007) J Org Chem 72:6970Google Scholar
  106. 106.
    Wang YS, Haze O, Dinnocenzo JP, Farid S, Farid RS, Gould IR (2008) J Phys Chem A 112:13088Google Scholar
  107. 107.
    Spata VA, Matsika S (2013) J Phys Chem A 117:8718Google Scholar
  108. 108.
    Improta R, Barone V (2011) Angew Chem Int Ed 50:12016Google Scholar
  109. 109.
    Voityuk AA (2013) Photochem Photobiol Sci 12:1303Google Scholar
  110. 110.
    Bouvier B, Dognon J-P, Lavery R, Markovitsi D, Millié P, Onidas D, Zakrzewska K (2003) J Phys Chem B 107:13512Google Scholar
  111. 111.
    Emanuele E, Markovitsi D, Millie P, Zakrzewska K (2005) ChemPhysChem 6:1387Google Scholar
  112. 112.
    Plasser F, Aquino AJA, Hase WL, Lischka H (2012) J Phys Chem A 116:11151Google Scholar
  113. 113.
    Mouret S, Philippe C, Gracia-Chantegrel J, Banyasz A, Karpati S, Markovitsi D, Douki T (2010) Org Biomol Chem 8:1706Google Scholar
  114. 114.
    Ritze HH, Hobza P, Nachtigallova D (2007) Phys Chem Chem Phys 9:1672Google Scholar
  115. 115.
    Santoro F, Barone V, Improta R (2009) J Am Chem Soc 131:15232Google Scholar
  116. 116.
    Conti I, Altoè P, Stenta M, Garavelli M, Orlandi G (2010) Phys Chem Chem Phys 12:5016Google Scholar
  117. 117.
    Santoro F, Barone V, Lami A, Improta R (2010) Phys Chem Chem Phys 12:4934Google Scholar
  118. 118.
    de La Harpe K, Kohler B (2011) J Phys Chem Lett 2:133Google Scholar
  119. 119.
    Zeleny T, Ruckenbauer M, Aquino AJA, Muller T, Lankas F, Drsata T, Hase WL, Nachtigallova D, Lischka H (2012) J Am Chem Soc 134:13662Google Scholar
  120. 120.
    Plasser F, Lischka H (2013) Photochem Photobiol Sci 12:1440Google Scholar
  121. 121.
    Banyasz A, Gustavsson T, Onidas D, Changenet-Barret P, Markovitsi D, Improta R (2013) Chem Eur J 19:3762Google Scholar
  122. 122.
    Stuhldreier MC, Temps F (2013) Faraday Discuss 163:173Google Scholar
  123. 123.
    Doorley GW, Wojdyla M, Watson GW, Towrie M, Parker AW, Kelly JM, Quinn SJ (2013) J Phys Chem Lett 4:2739Google Scholar
  124. 124.
    Markovitsi D, Gustavsson T, Vaya I (2010) J Phys Chem Lett 1:3271Google Scholar
  125. 125.
    Holcomb DN, Tinoco I Jr (1965) Biopolymers 3:121Google Scholar
  126. 126.
    Eisenberg H, Felsenfeld G (1967) J Mol Biol 30:17Google Scholar
  127. 127.
    Warshaw MM, Tinoco I Jr (1965) J Mol Biol 13:54Google Scholar
  128. 128.
    Ogasawara N, Inoue Y (1976) J Am Chem Soc 98:7048Google Scholar
  129. 129.
    Dolinnaya NG, Fresco JR (1992) Proc Natl Acad Sci USA 89:9242Google Scholar
  130. 130.
    Stuhldreier MC, Schüler C, Kleber J, Temps F (2011) In: Chergui M, Jonas D, Riedle E, Schoenlein R, Taylor A (eds) Ultrafast phenomena XVII proceedings of the 17th international conference, Snowmass, Colorado, USA, July 18–23, 2010 Oxford University Press, New York, p 553Google Scholar
  131. 131.
    Eisinger J, Guéron M, Shulman RG, Yamane T (1966) Proc Natl Acad Sci U S A 55:1015Google Scholar
  132. 132.
    Buchvarov I, Wang Q, Raytchev M, Trifonov A, Fiebig T (2007) Proc Natl Acad Sci U S A 104:4794Google Scholar
  133. 133.
    Lu Y, Lan ZG, Thiel W (2011) Angew Chem Int Ed 50:6864Google Scholar
  134. 134.
    Lu Y, Lan ZG, Thiel W (2012) J Comput Chem 33:1225Google Scholar
  135. 135.
    Onidas D, Gustavsson T, Lazzarotto E, Markovitsi D (2007) J Phys Chem B 111:9644Google Scholar
  136. 136.
    Bucher DB, Pilles BM, Carell T, Zinth W (2014) Proc Natl Acad Sci U S A 111:4369Google Scholar
  137. 137.
    Zhang Y, Dood J, Beckstead AA, Li X-B, Nguyen KV, Burrows CJ, Improta R, Kohler B (2014) Proc Natl Acad Sci U S A 111:11612Google Scholar
  138. 138.
    Nguyen KV, Burrows CJ (2011) J Am Chem Soc 133:14586Google Scholar
  139. 139.
    Zhang Y, Dood J, Beckstead A, Chen J, Li X-B, Burrows CJ, Lu Z, Matsika S, Kohler B (2013) J Phys Chem A 117:12851Google Scholar
  140. 140.
    Pan ZZ, Chen JQ, Schreier WJ, Kohler B, Lewis FD (2012) J Phys Chem B 116:698Google Scholar
  141. 141.
    Onidas D, Markovitsi D, Marguet S, Sharonov A, Gustavsson T (2002) J Phys Chem B 106:11367Google Scholar
  142. 142.
    Improta R, Santoro F, Barone V, Lami A (2009) J Phys Chem A 113:15346Google Scholar
  143. 143.
    Santoro F, Improta R, Avila F, Segado M, Lami A (2013) Photochem Photobiol Sci 12:1527Google Scholar
  144. 144.
    Dreuw A, Weisman JL, Head-Gordon M (2003) J Chem Phys 119:2943Google Scholar
  145. 145.
    Lange AW, Rohrdanz MA, Herbert JM (2008) J Phys Chem B 112:6304Google Scholar
  146. 146.
    Improta R (2008) Phys Chem Chem Phys 10:2656Google Scholar
  147. 147.
    Lange AW, Herbert JM (2009) J Am Chem Soc 131:3913Google Scholar
  148. 148.
    Szalay PG, Watson T, Perera A, Lotrich V, Bartlett RJ (2013) J Phys Chem A 117:3149Google Scholar
  149. 149.
    Markovitsi D, Talbot F, Gustavsson T, Onidas D, Lazzarotto E, Marguet S (2006) Nature 441:E7Google Scholar
  150. 150.
    Jimenez R, Fleming GR, Kumar PV, Maroncelli M (1994) Nature 369:471Google Scholar
  151. 151.
    Andreatta D, Lustres JLP, Kovalenko SA, Ernsting NP, Murphy CJ, Coleman RS, Berg MA (2005) J Am Chem Soc 127:7270Google Scholar
  152. 152.
    Furse KE, Corcelli SA (2010) J Phys Chem Lett 1:1813Google Scholar
  153. 153.
    Tazawa S, Tazawa I, Tso POP, Alderfer JL (1972) Biochemistry 11:3544Google Scholar
  154. 154.
    Guckian KM, Schweitzer BA, Ren RXF, Sheils CJ, Tahmassebi DC, Kool ET (2000) J Am Chem Soc 122:2213Google Scholar
  155. 155.
    Johnson WC Jr, Itzkowitz MS, Tinoco I Jr (1972) Biopolymers 11:225Google Scholar
  156. 156.
    Šponer J, Riley KE, Hobza P (2008) Phys Chem Chem Phys 10:2595Google Scholar
  157. 157.
    Norberg J, Nilsson L (1998) Biophys J 74:394Google Scholar
  158. 158.
    Murata K, Sugita Y, Okamoto Y (2004) Chem Phys Lett 385:1Google Scholar
  159. 159.
    Davis RC, Tinoco I Jr (1968) Biopolymers 6:223Google Scholar
  160. 160.
    Scott JF, Zamecnik PC (1969) Proc Natl Acad Sci U S A 64:1308Google Scholar
  161. 161.
    Stern N, Major DT, Gottlieb HE, Weizman D, Fischer B (2010) Org Biomol Chem 8:4637Google Scholar
  162. 162.
    Moser CC, Keske JM, Warncke K, Farid RS, Dutton PL (1992) Nature 355:796Google Scholar
  163. 163.
    Zhang WY, Yuan SA, Wang ZJ, Qi ZM, Zhao JS, Dou YS, Lo GV (2011) Chem Phys Lett 506:303Google Scholar
  164. 164.
    Dou YS, Liu ZC, Yuan S, Zhang WY, Tang H, Zhao JS, Fang WH, Lo GV (2013) Int J Biol Macromol 52:358Google Scholar
  165. 165.
    Markovitsi D, Onidas D, Gustavsson T, Talbot F, Lazzarotto E (2005) J Am Chem Soc 127:17130Google Scholar
  166. 166.
    Wilson RW, Callis PR (1976) J Phys Chem 80:2280Google Scholar
  167. 167.
    Nielsen LM, Hoffmann SV, Nielsen SB (2013) Photochem Photobiol Sci 12:1273Google Scholar
  168. 168.
    Tonzani S, Schatz GC (2008) J Am Chem Soc 130:7607Google Scholar
  169. 169.
    Shao F, Augustyn K, Barton JK (2005) J Am Chem Soc 127:17445Google Scholar
  170. 170.
    Simpkins H, Richards EG (1967) J Mol Biol 29:349Google Scholar
  171. 171.
    Löwdin PO (1963) Rev Mod Phys 35:724Google Scholar
  172. 172.
    Cohen B, Hare PM, Kohler B (2003) J Am Chem Soc 125:13594Google Scholar
  173. 173.
    Gustavsson T, Sarkar N, Lazzarotto E, Markovitsi D, Improta R (2006) Chem Phys Lett 429:551Google Scholar
  174. 174.
    Gustavsson T, Banyasz A, Sarkar N, Markovitsi D, Improta R (2008) Chem Phys 350:186Google Scholar
  175. 175.
    Sobolewski AL, Domcke W (2004) Phys Chem Chem Phys 6:2763Google Scholar
  176. 176.
    Perun S, Sobolewski AL, Domcke W (2006) J Phys Chem A 110:9031Google Scholar
  177. 177.
    Abo-Riziq A, Grace L, Nir E, Kabelac M, Hobza P, de Vries MS (2005) Proc Natl Acad Sci U S A 102:20Google Scholar
  178. 178.
    Biemann L, Kovalenko SA, Kleinermanns K, Mahrwald R, Markert M, Improta R (2011) J Am Chem Soc 133:19664Google Scholar
  179. 179.
    Roettger K, Soennichsen FD, Temps F (2013) Photochem Photobiol Sci 12:1466Google Scholar
  180. 180.
    Crespo-Hernández CE, de La Harpe K, Kohler B (2008) J Am Chem Soc 130:10844Google Scholar
  181. 181.
    Brazard J, Thazhathveetil AK, Vaya I, Lewis FD, Gustavsson T, Markovitsi D (2013) Photochem Photobiol Sci 12:1453Google Scholar
  182. 182.
    Santoro F, Barone V, Improta R (2007) Proc Natl Acad Sci U S A 104:9931Google Scholar
  183. 183.
    Improta R (2012) J Phys Chem B 116:14261Google Scholar
  184. 184.
    de La Harpe K, Crespo-Hernández CE, Kohler B (2009) ChemPhysChem 10:1421Google Scholar
  185. 185.
    Doorley GW, McGovern DA, George MW, Towrie M, Parker AW, Kelly JM, Quinn SJ (2009) Angew Chem Int Ed 48:123Google Scholar
  186. 186.
    Vayá I, Gustavsson T, Miannay FA, Douki T, Markovitsi D (2010) J Am Chem Soc 132:11834Google Scholar
  187. 187.
    de La Harpe K, Crespo-Hernández CE, Kohler B (2009) J Am Chem Soc 131:17557Google Scholar
  188. 188.
    Kumar A, Sevilla MD (2013) Photochem Photobiol Sci 12:1328Google Scholar
  189. 189.
    Colson AO, Besler B, Sevilla MD (1992) J Phys Chem 96:9787Google Scholar
  190. 190.
    Colson A-O, Besler B, Close DM, Sevilla MD (1992) J Phys Chem 96:661Google Scholar
  191. 191.
    Bertran J, Oliva A, Rodríguez-Santiago L, Sodupe M (1998) J Am Chem Soc 120:8159Google Scholar
  192. 192.
    Li X, Cai Z, Sevilla MD (2001) J Phys Chem B 105:10115Google Scholar
  193. 193.
    Kumar A, Sevilla MD (2010) Chem Rev 110:7002Google Scholar
  194. 194.
    Guallar V, Douhal A, Moreno M, Lluch JM (1999) J Phys Chem A 103:6251Google Scholar
  195. 195.
    Kumar A, Sevilla MD (2009) J Phys Chem B 113:11359Google Scholar
  196. 196.
    Ko C, Hammes-Schiffer S (2013) J Phys Chem Lett 4:2540Google Scholar
  197. 197.
    Chinnapen DJF, Sen D (2004) Proc Natl Acad Sci U S A 101:65Google Scholar
  198. 198.
    Holman MR, Ito T, Rokita SE (2007) J Am Chem Soc 129:6Google Scholar
  199. 199.
    Law YK, Forties RA, Liu X, Poirier MG, Kohler B (2013) Photochem Photobiol Sci 12:1431Google Scholar
  200. 200.
    Kao YT, Saxena C, Wang LJ, Sancar A, Zhong DP (2005) Proc Natl Acad Sci U S A 102:16128Google Scholar
  201. 201.
    Jorns MS (1987) J Am Chem Soc 109:3133Google Scholar
  202. 202.
    Shafirovich V, Dourandin A, Geacintov NE (2001) J Phys Chem B 105:8431Google Scholar
  203. 203.
    Shafirovich V, Dourandin A, Luneva NP, Geacintov NE (2000) J Phys Chem B 104:137Google Scholar
  204. 204.
    Shafirovich V, Dourandin A, Huang W, Luneva NP, Geacintov NE (1999) J Phys Chem B 103:10924Google Scholar
  205. 205.
    Shafirovich VY, Courtney SH, Ya N, Geacintov NE (1995) J Am Chem Soc 117:4920Google Scholar
  206. 206.
    Spoerlein S, Carstens H, Satzger H, Renner C, Behrendt R, Morader L, Tavan P, Zinth W, Wachtveitl J (2002) Proc Natl Acad Sci U S A 99:7998Google Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  1. 1.Department of Chemistry and BiochemistryMontana State UniversityBozemanUSA
  2. 2.Department of ChemistryEmory UniversityAtlantaUSA

Personalised recommendations