Skip to main content
SpringerLink
Log in

DNA damage in nucleosomes

  • Reviews
  • Special Issue: Dedicated to the 100th Anniversary of Nankai University
  • Published:
Science China Chemistry Aims and scope Submit manuscript

Abstract

Eukaryotic genomic DNA is packed into chromatin, whose fundamental structural unit is the nucleosome. As DNA-histone protein complexes, nucleosomes show different properties toward exogenous and endogenous DNA-damaging agents. This review summarizes nucleosome DNA damage due to different sources, including alkylating agents, radicals, UV radiation and reactive DNA damage intermediates. In most cases, the histone core protects the associated DNA against damage via its structure and/or scavenging of damaging agents. In contrast, histones react with damaged DNA and, in some instances, catalyze DNA damage in the nucleosome. The biological consequence of nucleosome DNA damage and future prospects in this field are briefly discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Gates KS. Chem Res Toxicol, 2009, 22: 1747–1760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Cadet J, Wagner JR. Cold Spring Harbor Perspect Biol, 2013, 5: a012559

    Google Scholar 

  3. Drabløs F, Feyzi E, Aas PA, Vaagbø CB, Kavli B, Bratlie MS, Peña-Diaz J, Otterlei M, Slupphaug G, Krokan HE. DNA Repair, 2004, 3: 1389–1407

    Article  CAS  PubMed  Google Scholar 

  4. Poirier MC. Nat Rev Cancer, 2004, 4: 630–637

    Article  CAS  PubMed  Google Scholar 

  5. Sinha RP, Häder DP. Photochem Photobiol Sci, 2002, 1: 225–236

    Article  CAS  PubMed  Google Scholar 

  6. Lindahl T. Nature, 1993, 362: 709–715

    Article  CAS  PubMed  Google Scholar 

  7. Schärer OD. Angew Chem Int Ed, 2003, 42: 2946–2974

    Article  CAS  Google Scholar 

  8. Lindahl T. Science, 1999, 286: 1897–1905

    Article  CAS  PubMed  Google Scholar 

  9. Sancar A, Lindsey-Boltz LA, Ünsal-Kaçmaz K, Linn S. Annu Rev Biochem, 2004, 73: 39–85

    Article  CAS  PubMed  Google Scholar 

  10. Cooke MS, Evans MD, Dizdaroglu M, Lunec J. FASEB J, 2003, 17: 1195–1214

    Article  CAS  PubMed  Google Scholar 

  11. Hurley LH. Nat Rev Cancer, 2002, 2: 188–200

    Article  CAS  PubMed  Google Scholar 

  12. Greenberg MM. Org Biomol Chem, 2007, 5: 18–30

    Article  CAS  PubMed  Google Scholar 

  13. Luger K, Mäder AW, Richmond RK, Sargent DF, Richmond TJ. Nature, 1997, 389: 251–260

    Article  CAS  PubMed  Google Scholar 

  14. Song F, Chen P, Sun D, Wang M, Dong L, Liang D, Xu RM, Zhu P, Li G. Science, 2014, 344: 376–380

    Article  CAS  PubMed  Google Scholar 

  15. Taylor JS. DNA Repair, 2015, 36: 59–67

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Olins DE, Olins AL. Nat Rev Mol Cell Biol, 2003, 4: 809–814

    Article  CAS  PubMed  Google Scholar 

  17. Szerlong HJ, Hansen JC. Biochem Cell Biol, 2011, 89: 24–34

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Ljungman M, Hanawalt PC. Mol Carcinog, 1992, 5: 264–269

    Article  CAS  PubMed  Google Scholar 

  19. Mao P, Wyrick JJ, Roberts SA, Smerdon MJ. Photochem Photobiol, 2017, 93: 216–228

    Article  CAS  PubMed  Google Scholar 

  20. Zou T, Kizaki S, Sugiyama H. Chembiochem, 2018, 19: 664–668

    Article  CAS  PubMed  Google Scholar 

  21. Hauer MH, Gasser SM. Genes Dev, 2017, 31: 2204–2221

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Liang Q, Dedon PC. Chem Res Toxicol, 2001, 14: 416–422

    Article  CAS  PubMed  Google Scholar 

  23. Sczepanski JT, Wong RS, McKnight JN, Bowman GD, Greenberg MM. Proc Natl Acad Sci USA, 2010, 107: 22475–22480

    Article  PubMed  PubMed Central  Google Scholar 

  24. Povirk LF, Shuker DE. Mutat Res/Rev Genet Toxicol, 1994, 318: 205–226

    Article  CAS  Google Scholar 

  25. Wang D, Lippard SJ. Nat Rev Drug Discov, 2005, 4: 307–320

    Article  CAS  PubMed  Google Scholar 

  26. Palermo G, Magistrato A, Riedel T, von Erlach T, Davey CA, Dyson PJ, Rothlisberger U. Chemmedchem, 2016, 11: 1199–1210

    Article  CAS  PubMed  Google Scholar 

  27. McGhee JD, Felsenfeld G. Proc Natl Acad Sci USA, 1979, 76: 2133–2137

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Moyer R, Mariën K, van Holde K, Bailey G. J Biol Chem, 1989, 264: 12226–12231

    CAS  PubMed  Google Scholar 

  29. Mirzabekov AD, San’ko DF, Kolchinsky AM, Melnikova AF. Eur J Biochem, 1977, 75: 379–389

    Article  CAS  PubMed  Google Scholar 

  30. Galea AM, Murray V. Chem Biol Drug Des, 2010, 75: 578–589

    Article  CAS  PubMed  Google Scholar 

  31. Millard JT, Wilkes EE. Biochemistry, 2000, 39: 16046–16055

    Article  CAS  PubMed  Google Scholar 

  32. Chua EYD, Davey GE, Chin CF, Dröge P, Ang WH, Davey CA. Nucleic Acids Res, 2015, 43: 5284–5296

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Wu B, Dröge P, Davey CA. Nat Chem Biol, 2008, 4: 110–112

    Article  CAS  PubMed  Google Scholar 

  34. Smith BL, Bauer GB, Povirk LF. J Biol Chem, 1994, 269: 30587–30594

    CAS  PubMed  Google Scholar 

  35. Thrall BD, Mann DB, Smerdon MJ, Springer DL. Biochemistry, 1994, 33: 2210–2216

    Article  CAS  PubMed  Google Scholar 

  36. Millard JT, Spencer RJ, Hopkins PB. Biochemistry, 1998, 37: 5211–5219

    Article  CAS  PubMed  Google Scholar 

  37. Zou T, Kizaki S, Pandian GN, Sugiyama H. Chem Eur J, 2016, 22: 8756–8758

    Article  CAS  PubMed  Google Scholar 

  38. Trzupek JD, Gottesfeld JM, Boger DL. Nat Chem Biol, 2006, 2: 79–82

    Article  CAS  PubMed  Google Scholar 

  39. Dizdaroglu M, Jaruga P. Free Radical Res, 2012, 46: 382–419

    Article  CAS  Google Scholar 

  40. Kabel AM. World J Nutr Health, 2014, 2: 35–38

    Google Scholar 

  41. Tullius TD, Dombroski BA. Proc Natl Acad Sci USA, 1986, 83: 5469–5473

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Hayes JJ, Tullius TD, Wolffe AP. Proc Natl Acad Sci USA, 1990, 87: 7405–7409

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Gajewski E, Rao G, Nackerdien Z, Dizdaroglu M. Biochemistry, 1990, 29: 7876–7882

    Article  CAS  PubMed  Google Scholar 

  44. Enright H, Miller WJ, Hays R, Floyd RA, Hebbel RP. Carcinogenesis, 1996, 17: 1175–1177

    Article  CAS  PubMed  Google Scholar 

  45. Toyokuni S, Mori T, Hiai H, Dizdaroglu M. Int J Cancer, 1995, 62: 309–313

    Article  CAS  PubMed  Google Scholar 

  46. Nackerdien Z, Rao G, Cacciuttolo MA, Gajewski E, Dizdaroglu M. Biochemistry, 1991, 30: 4873–4879

    Article  CAS  PubMed  Google Scholar 

  47. Olinski R, Nackerdien Z, Dizdaroglu M. Archives Biochem Biophys, 1992, 297: 139–143

    Article  CAS  Google Scholar 

  48. Zhou C, Greenberg MM. J Am Chem Soc, 2014, 136: 6562–6565

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Steighner RJ, Povirk LF. Proc Natl Acad Sci USA, 1990, 87: 8350–8354

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Povirk LF, Houlgrave CW. Biochemistry, 1988, 27: 3850–3857

    Article  CAS  PubMed  Google Scholar 

  51. Galm U, Hager MH, van Lanen SG, Ju J, Thorson JS, Shen B. Chem Rev, 2005, 105: 739–758

    Article  CAS  PubMed  Google Scholar 

  52. Smith AL, Nicolaou KC. J Med Chem, 1996, 39: 2103–2117

    Article  CAS  PubMed  Google Scholar 

  53. Yu L, Goldberg IH, Dedon PC. J Biol Chem, 1994, 269: 4144–4151

    CAS  PubMed  Google Scholar 

  54. Ikemoto N, Kumar RA, Dedon PC, Danishefsky SJ, Patel DJ. J Am Chem Soc, 1994, 116: 9387–9388

    Article  CAS  Google Scholar 

  55. Povirk LF, Goldberg IH. Biochemistry, 1980, 19: 4773–4780

    Article  CAS  PubMed  Google Scholar 

  56. Kuduvalli PN, Townsend CA, Tullius TD. Biochemistry, 1995, 34: 3899–3906

    Article  CAS  PubMed  Google Scholar 

  57. Xu J, Wu J, Dedon PC. Biochemistry, 1998, 37: 1890–1897

    Article  CAS  PubMed  Google Scholar 

  58. Liang Q, Choi DJ, Dedon PC. Biochemistry, 1997, 36: 12653–12659

    Article  CAS  PubMed  Google Scholar 

  59. Genereux JC, Barton JK. Chem Rev, 2010, 110: 1642–1662

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Nguyen KL, Steryo M, Kurbanyan K, Nowitzki KM, Butterfield SM, Ward SR, Stemp EDA. J Am Chem Soc, 2000, 122: 3585–3594

    Article  CAS  Google Scholar 

  61. Núñez ME, Noyes KT, Barton JK. Chem Biol, 2002, 9: 403–415

    Article  PubMed  Google Scholar 

  62. Bjorklund CC, Davis WB. Nucleic Acids Res, 2006, 34: 1836–1846

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Liu Y, Liu Z, Geacintov NE, Shafirovich V. Phys Chem Chem Phys, 2012, 14: 7400–7410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Lowary PT, Widom J. J Mol Biol, 1998, 276: 19–42

    Article  CAS  PubMed  Google Scholar 

  65. Vasudevan D, Chua EYD, Davey CA. J Mol Biol, 2010, 403: 1–10

    Article  CAS  PubMed  Google Scholar 

  66. Davis WB, Bjorklund CC, Deline M. Biochemistry, 2012, 51: 3129–3142

    Article  CAS  PubMed  Google Scholar 

  67. Bjorklund CC, Davis WB. Biochemistry, 2007, 46: 10745–10755

    Article  CAS  PubMed  Google Scholar 

  68. Cadet J, Sage E, Douki T. Mutat Res Fund Mol Mech Mut, 2005, 571: 3–17

    Article  CAS  Google Scholar 

  69. Mitchell DL, Nguyen TD, Cleaver JE. J Biol Chem, 1990, 265: 5353–5356

    CAS  PubMed  Google Scholar 

  70. Gale JM, Nissen KA, Smerdon MJ. Proc Natl Acad Sci USA, 1987, 84: 6644–6648

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Gale JM, Smerdon MJ. Photochem Photobiol, 1990, 51: 411–417

    Article  CAS  PubMed  Google Scholar 

  72. Brown DW, Libertini LJ, Suquet C, Small EW, Smerdon MJ. Biochemistry, 1993, 32: 10527–10531

    Article  CAS  PubMed  Google Scholar 

  73. Gale JM, Smerdon MJ. J Mol Biol, 1988, 204: 949–958

    Article  CAS  PubMed  Google Scholar 

  74. Mao P, Smerdon MJ, Roberts SA, Wyrick JJ. Proc Natl Acad Sci USA, 2016, 113: 9057–9062

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Wang K, Taylor JSA. Nucleic Acids Res, 2017, 45: 7031–7041

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Song Q, Cannistraro VJ, Taylor JS. Nucleic Acids Res, 2014, 42: 13122–13133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Cannistraro VJ, Pondugula S, Song Q, Taylor JS. J Biol Chem, 2015, 290: 26597–26609

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Greenberg MM. Acc Chem Res, 2014, 47: 646–655

    Article  CAS  PubMed  Google Scholar 

  79. Pogozelski WK, Tullius TD. Chem Rev, 1998, 98: 1089–1108

    Article  CAS  PubMed  Google Scholar 

  80. Burrows CJ, Muller JG. Chem Rev, 1998, 98: 1109–1152

    Article  CAS  PubMed  Google Scholar 

  81. David SS, Williams SD. Chem Rev, 1998, 98: 1221–1262

    Article  CAS  PubMed  Google Scholar 

  82. Catalano MJ, Liu S, Andersen N, Yang Z, Johnson KM, Price NE, Wang Y, Gates KS. J Am Chem Soc, 2015, 137: 3933–3945

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Yang Z, Price NE, Johnson KM, Wang Y, Gates KS. Nucleic Acids Res, 2017, 45: 6275–6283

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Sczepanski JT, Jacobs AC, Greenberg MM. J Am Chem Soc, 2008, 130: 9646–9647

    Article  CAS  PubMed  Google Scholar 

  85. Guan L, Greenberg MM. J Am Chem Soc, 2009, 131: 15225–15231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Sczepanski JT, Jacobs AC, Majumdar A, Greenberg MM. J Am Chem Soc, 2009, 131: 11132–11139

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Zhou C, Sczepanski JT, Greenberg MM. J Am Chem Soc, 2012, 134: 16734–16741

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Sczepanski JT, Zhou C, Greenberg MM. Biochemistry, 2013, 52: 2157–2164

    Article  CAS  PubMed  Google Scholar 

  89. Wang R, Yang K, Banerjee S, Greenberg MM. Biochemistry, 2018, 57: 3945–3952

    Article  CAS  PubMed  Google Scholar 

  90. Banerjee S, Chakraborty S, Jacinto MP, Paul MD, Balster MV, Greenberg MM. Biochemistry, 2017, 56: 14–21

    Article  CAS  PubMed  Google Scholar 

  91. Zhou C, Sczepanski JT, Greenberg MM. J Am Chem Soc, 2013, 135: 5274–5277

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Aso M, Kondo M, Suemune H, Hecht SM. J Am Chem Soc, 1999, 121: 9023–9033

    Article  CAS  Google Scholar 

  93. Jacobs AC, Kreller CR, Greenberg MM. Biochemistry, 2011, 50: 136–143

    Article  CAS  PubMed  Google Scholar 

  94. Jacinto MP, Pichling P, Greenberg MM. Org Lett, 2018, 20: 4885–4887

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Zhang Y, Zhou X, Xie Y, Greenberg MM, Xi Z, Zhou C. J Am Chem Soc, 2017, 139: 6146–6151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Weng L, Greenberg MM. J Am Chem Soc, 2015, 137: 11022–11031

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Zhou C, Greenberg MM. J Am Chem Soc, 2012, 134: 8090–8093

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Barker S, Weinfeld M, Murray D. Mutat Res/Rev Mutat Res, 2005, 589: 111–135

    Article  CAS  Google Scholar 

  99. Weng L, Zhou C, Greenberg MM. ACS Chem Biol, 2015, 10: 622–630

    Article  CAS  PubMed  Google Scholar 

  100. Bachman M, Uribe-Lewis S, Yang X, Burgess HE, Iurlaro M, Reik W, Murrell A, Balasubramanian S. Nat Chem Biol, 2015, 11: 555–557

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Su M, Kirchner A, Stazzoni S, Müller M, Wagner M, Schröder A, Carell T. Angew Chem Int Ed, 2016, 55: 11797–11800

    Article  CAS  Google Scholar 

  102. Xia B, Han D, Lu X, Sun Z, Zhou A, Yin Q, Zeng H, Liu M, Jiang X, Xie W, He C, Yi C. Nat Methods, 2015, 12: 1047–1050

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Guo P, Yan S, Hu J, Xing X, Wang C, Xu X, Qiu X, Ma W, Lu C, Weng X, Zhou X. Org Lett, 2013, 15: 3266–3269

    Article  CAS  PubMed  Google Scholar 

  104. Li F, Zhang Y, Bai J, Greenberg MM, Xi Z, Zhou C. J Am Chem Soc, 2017, 139: 10617–10620

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Ji S, Shao H, Han Q, Seiler CL, Tretyakova NY. Angew Chem Int Ed, 2017, 56: 14130–14134

    Article  CAS  Google Scholar 

  106. Ji S, Fu I, Naldiga S, Shao H, Basu AK, Broyde S, Tretyakova NY. Nucleic Acids Res, 2018: gky444

    Google Scholar 

  107. Raiber E-A, Portella G, Martínez Cuesta S, Hardisty R, Murat P, Li Z, Iurlaro M, Dean W, Spindel J, Beraldi D, Liu Z, Dawson MA, Reik W, Balasubramanian S. Nat Chem, 2018, 10: 1258–1266

    Article  CAS  PubMed  Google Scholar 

  108. Yang K, Park D, Tretyakova NY, Greenberg MM. Proc Natl Acad Sci USA, 2018, 115: E11212–E11220

    Google Scholar 

  109. Pratviel G, Meunier B. Chem Eur J, 2006, 12: 6018–6030

    Article  CAS  PubMed  Google Scholar 

  110. Xu X, Muller JG, Ye Y, Burrows CJ. J Am Chem Soc, 2008, 130: 703–709

    Article  CAS  PubMed  Google Scholar 

  111. Bai J, Zhang Y, Xi Z, Greenberg MM, Zhou C. Chem Res Toxicol, 2018, 31: 1364–1372

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Mangerich A, Knutson CG, Parry NM, Muthupalani S, Ye W, Prestwich E, Cui L, McFaline JL, Mobley M, Ge Z, Taghizadeh K, Wishnok JS, Wogan GN, Fox JG, Tannenbaum SR, Dedon PC. Proc Natl Acad Sci USA, 2012, 109: E1820–E1829

    Google Scholar 

  113. Mann DB, Springer DL, Smerdon MJ. Proc Natl Acad Sci USA, 1997, 94: 2215–2220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Duan MR, Smerdon MJ. J Biol Chem, 2010, 285: 26295–26303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Wu B, Davey CA. Chem Biol, 2008, 15: 1023–1028

    Article  CAS  PubMed  Google Scholar 

  116. Todd RC, Lippard SJ. Chem Biol, 2010, 17: 1334–1343

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Zhu G, Song L, Lippard SJ. Cancer Res, 2013, 73: 4451–4460

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Hinz JM, Rodriguez Y, Smerdon MJ. Proc Natl Acad Sci USA, 2010, 107: 4646–4651

    Article  PubMed  PubMed Central  Google Scholar 

  119. Menoni H, Shukla MS, Gerson V, Dimitrov S, Angelov D. Nucleic Acids Res, 2012, 40: 692–700

    Article  CAS  PubMed  Google Scholar 

  120. Maher RL, Prasad A, Rizvanova O, Wallace SS, Pederson DS. DNA Repair, 2013, 12: 964–971

    Article  CAS  PubMed  Google Scholar 

  121. Banerjee DR, Deckard Iii CE, Elinski MB, Buzbee ML, Wang WW, Batteas JD, Sczepanski JT. J Am Chem Soc, 2018, 140: 8260–8267

    Article  CAS  PubMed  Google Scholar 

  122. Odell ID, Wallace SS, Pederson DS. J Cell Physiol, 2013, 228: 258–266

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank Professor Marc M. Greenberg for carefully reading the manuscript and for helpful suggestions. This work was supported by the National Natural Science Foundation of China (21572109, 21877064, 21740002) and the National Key R&D Program of China (2017YFD0200501).

Author information

Author notes

  1. These authors contributed equally to this work.

Authors and Affiliations

  1. State Key Laboratory of Elemento-Organic Chemistry and Department of Chemical Biology, College of Chemistry, Nankai University, Tianjin, 300071, China

    Mengtian Ren, Jing Bai, Zhen Xi & Chuanzheng Zhou

Authors
  1. Mengtian Ren
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jing Bai
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zhen Xi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chuanzheng Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Chuanzheng Zhou.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ren, M., Bai, J., Xi, Z. et al. DNA damage in nucleosomes. Sci. China Chem. 62, 561–570 (2019). https://doi.org/10.1007/s11426-018-9421-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11426-018-9421-5

Keywords

Search

Navigation