In-depth characterization of the cisplatin mutational signature in human cell lines and in esophageal and liver tumors

Genome Research

Volumn 28, Issue 5, 2018, Pages 654-665

  Boot, Arnoud ^a   Huang, Mi Ni ^a   Ng, Alvin W T ^a,b   Ho, Szu Chi ^a   Lim, Jing Quan ^c   Kawakami, Yoshiiku ^d   Chayama, Kazuaki ^d   Teh, Bin Tean ^c   Nakagawa, Hidewaki ^e   Rozen, Steven G ^a  

^a DUKE NUS MEDICAL SCHOOL   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c DIVISION OF MEDICAL ONCOLOGY   (Singapore)

^d HIROSHIMA UNIVERSITY   (Japan)

^e Institute of Physical and Chemical Research   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; CISPLATIN; DNA; PURINE; ANTINEOPLASTIC AGENT;

ARTICLE; CROSS LINKING; ESOPHAGEAL ADENOCARCINOMA; HEP-G2 CELL LINE; HUMAN; HUMAN CELL; LIVER CELL CARCINOMA; MAJOR CLINICAL STUDY; MCF-10A CELL LINE; MOLECULAR CLONING; MUTAGENESIS; PRIORITY JOURNAL; SEQUENCE ANALYSIS; SINGLE NUCLEOTIDE POLYMORPHISM; WHOLE GENOME SEQUENCING; ADENOCARCINOMA; CELL LINE; DNA MUTATIONAL ANALYSIS; DRUG EFFECT; ESOPHAGUS TUMOR; GENETICS; HUMAN GENOME; LIVER TUMOR; MUTATION; PROCEDURES; WHOLE EXOME SEQUENCING;

ADENOCARCINOMA; ANTINEOPLASTIC AGENTS; CARCINOMA, HEPATOCELLULAR; CELL LINE; CISPLATIN; DNA MUTATIONAL ANALYSIS; ESOPHAGEAL NEOPLASMS; GENOME, HUMAN; HEP G2 CELLS; HUMANS; LIVER NEOPLASMS; MUTAGENESIS; MUTATION; WHOLE EXOME SEQUENCING;

EID: 85046630432     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.230219.117     Document Type: Article

References (55)

1. The 1000 Genomes Project Consortium. 2015. A global reference for human genetic variation. Nature 526: 68–74.
2. Alexandrov LB. 2014. “Signatures of mutational processes in human cancer.” PhD thesis, Darwin College, University of Cambridge, Cambridge, UK. ftp://ftp.sanger.ac.uk/pub/resources/theses/la2/alexandrov_ludmil_thesis.pdf.
3. Alexandrov LB, Nik-Zainal S, Wedge DC, Aparicio SA, Behjati S, Biankin AV, Bignell GR, Bolli N, Borg A, Borresen-Dale AL, et al. 2013a. Signatures of mutational processes in human cancer. Nature 500: 415–421.
4. Alexandrov LB, Nik-Zainal S, Wedge DC, Campbell PJ, Stratton MR. 2013b. Deciphering signatures of mutational processes operative in human cancer. Cell Rep 3: 246–259.
5. Alexandrov LB, Jones PH, Wedge DC, Sale JE, Campbell PJ, Nik-Zainal S, Stratton MR. 2015. Clock-like mutational processes in human somatic cells. Nat Genet 47: 1402–1407.
6. Andreassen PR, Ren K. 2009. Fanconi anemia proteins, DNA interstrand crosslink repair pathways, and cancer therapy. Curr Cancer Drug Targets 9: 101–117.
7. Baik MH, Friesner RA, Lippard SJ. 2003. Theoretical study of cisplatin binding to purine bases: Why does cisplatin prefer guanine over adenine? J Am Chem Soc 125: 14082–14092.
8. Behmand B, Marignier JL, Mostafavi M, Wagner JR, Hunting DJ, Sanche L. 2015. Radiosensitization of DNA by cisplatin adducts results from an increase in the rate constant for the reaction with hydrated electrons and formation of Pt(I). J Phys Chem B 119: 9496–9500.
9. Bernstein BE, Stamatoyannopoulos JA, Costello JF, Ren B, Milosavljevic A, Meissner A, Kellis M, Marra MA, Beaudet AL, Ecker JR, et al. 2010. The NIH Roadmap Epigenomics Mapping Consortium. Nat Biotechnol 28: 1045–1048.
10. Chen X, Schulz-Trieglaff O, Shaw R, Barnes B, Schlesinger F, Kallberg M, Cox AJ, Kruglyak S, Saunders CT. 2016. Manta: rapid detection of structural variants and indels for germline and cancer sequencing applications. Bioinformatics 32: 1220–1222.
11. Choi DK, Helenowski I, Hijiya N. 2014. Secondary malignancies in pediatric cancer survivors: perspectives and review of the literature. Int J Cancer 135: 1764–1773.
12. Conaway JW, Conaway RC. 1999. Transcription elongation and human disease. Annu Rev Biochem 68: 301–319.
13. Dasari S, Tchounwou PB. 2014. Cisplatin in cancer therapy: molecular mechanisms of action. Eur J Pharmacol 740: 364–378.
14. Dugbartey GJ, Peppone LJ, de Graaf IA. 2016. An integrative view of cisplatin-induced renal and cardiac toxicities: molecular mechanisms, current treatment challenges and potential protective measures. Toxicology 371: 58–66.
15. Eastman A. 1983. Characterization of the adducts produced in DNA by cis-diamminedichloroplatinum(II) and cis-dichloro(ethylenediamine)plat-inum(II). Biochemistry 22: 3927–3933.
16. Eilers PH, de Menezes RX. 2005. Quantile smoothing of array CGH data. Bioinformatics 21: 1146–1153.
17. Enoiu M, Jiricny J, Scharer OD. 2012. Repair of cisplatin-induced DNA interstrand crosslinks by a replication-independent pathway involving transcription-coupled repair and translesion synthesis. Nucleic Acids Res 40: 8953–8964.
18. Fichtinger-Schepman AM, Vendrik CP, van Dijk-Knijnenburg WC, de Jong WH, van der Minnen AC, Claessen AM, van der Velde-Visser SD, de Groot G, Wubs KL, Steerenberg PA, et al. 1989. Platinum concentrations and DNA adduct levels in tumors and organs of cisplatin-treated LOU/M rats inoculated with cisplatin-sensitive or -resistant immunoglobulin M immunocytoma. Cancer Res 49: 2862–2867.
19. Forbes SA, Beare D, Boutselakis H, Bamford S, Bindal N, Tate J, Cole CG, Ward S, Dawson E, Ponting L, et al. 2017. COSMIC: somatic cancer genetics at high-resolution. Nucleic Acids Res 45: D777–D783.
20. Fousteri M, Mullenders LH. 2008. Transcription-coupled nucleotide excision repair in mammalian cells: molecular mechanisms and biological effects. Cell Res 18: 73–84.
21. Fujimoto A, Furuta M, Totoki Y, Tsunoda T, Kato M, Shiraishi Y, Tanaka H, Taniguchi H, Kawakami Y, Ueno M, et al. 2016. Whole-genome mutational landscape and characterization of noncoding and structural mutations in liver cancer. Nat Genet 48: 500–509.
22. Garrison E, Marth G. 2012. Haplotype-based variant detection from short-read sequencing. arXiv:1207.3907 [q-bio.GN.
23. Harrington CF, Le Pla RC, Jones GD, Thomas AL, Farmer PB. 2010. Determination of cisplatin 1,2-intrastrand guanine–guanine DNA adducts in human leukocytes by high-performance liquid chromatography coupled to inductively coupled plasma mass spectrometry. Chem Res Toxicol 23: 1313–1321.
24. Hashimoto S, Anai H, Hanada K. 2016. Mechanisms of interstrand DNA crosslink repair and human disorders. Genes Environ 38: 9.
25. Hu J, Adar S, Selby CP, Lieb JD, Sancar A. 2015. Genome-wide analysis of human global and transcription-coupled excision repair of UV damage at single-nucleotide resolution. Genes Dev 29: 948–960.
26. Hu J, Lieb JD, Sancar A, Adar S. 2016. Cisplatin DNA damage and repair maps of the human genome at single-nucleotide resolution. Proc Natl Acad Sci 113: 11507–11512.
27. Huang MN, Yu W, Teoh WW, Ardin M, Jusakul A, Ng AWT, Boot A, Abedi-Ardekani B, Villar S, Myint SS, et al. 2017. Genome-scale mutational signatures of aflatoxin in cells, mice, and human tumors. Genome Res 27: 1475–1486.
28. Imielinski M, Berger AH, Hammerman PS, Hernandez B, Pugh TJ, Hodis E, Cho J, Suh J, Capelletti M, Sivachenko A, et al. 2012. Mapping the hallmarks of lung adenocarcinoma with massively parallel sequencing. Cell 150: 1107–1120.
29. Jamieson ER, Lippard SJ. 1999. Structure, recognition, and processing of cisplatin-DNA adducts. Chem Rev 99: 2467–2498.
30. Kaiser VB, Taylor MS, Semple CA. 2016. Mutational biases drive elevated rates of substitution at regulatory sites across cancer types. PLoS Genet 12: e1006207.
31. Kan Z, Zheng H, Liu X, Li S, Barber TD, Gong Z, Gao H, Hao K, Willard MD, Xu J, et al. 2013. Whole-genome sequencing identifies recurrent mutations in hepatocellular carcinoma. Genome Res 23: 1422–1433.
32. Kushner BH, Cheung NK, Kramer K, Heller G, Jhanwar SC. 1998. Neuroblastoma and treatment-related myelodysplasia/leukemia: the Memorial Sloan-Kettering experience and a literature review. J Clin Oncol 16: 3880–3889.
33. Liu F, Ren C, Li H, Zhou P, Bo X, Shu W. 2016. De novo identification of replication-timing domains in the human genome by deep learning. Bioinformatics 32: 641–649.
34. Masters JR, Koberle B. 2003. Curing metastatic cancer: lessons from testicular germ-cell tumours. Nat Rev Cancer 3: 517–525.
35. McCulloch SD, Kokoska RJ, Masutani C, Iwai S, Hanaoka F, Kunkel TA. 2004. Preferential cis-syn thymine dimer bypass by DNA polymerase eta occurs with biased fidelity. Nature 428: 97–100.
36. Meier B, Cooke SL, Weiss J, Bailly AP, Alexandrov LB, Marshall J, Raine K, Maddison M, Anderson E, Stratton MR, et al. 2014. C. elegans whole-genome sequencing reveals mutational signatures related to carcinogens and DNA repair deficiency. Genome Res 24: 1624–1636.
37. Ng AWT, Poon SL, Huang MN, Lim JQ, Boot A, Yu W, Suzuki Y, Thangaraju S, Ng CCY, Tan P, et al. 2017. Aristolochic acids and their derivatives are widely implicated in liver cancers in Taiwan and throughout Asia. Sci Transl Med 9: eaan6446.
38. Noorani A, Bornschein J, Lynch AG, Secrier M, Achilleos A, Eldridge M, Bower L, Weaver JMJ, Crawte J, Ong CA, et al. 2017. A comparative analysis of whole genome sequencing of esophageal adenocarcinoma pre- and post-chemotherapy. Genome Res 27: 902–912.
39. Olivier M, Weninger A, Ardin M, Huskova H, Castells X, Vallee MP, McKay J, Nedelko T, Muehlbauer KR, Marusawa H, et al. 2014. Modelling mutational landscapes of human cancers in vitro. Sci Rep 4: 4482.
40. Polak P, Karlic R, Koren A, Thurman R, Sandstrom R, Lawrence MS, Reynolds A, Rynes E, Vlahovicek K, Stamatoyannopoulos JA, et al. 2015. Cell-of-origin chromatin organization shapes the mutational landscape of cancer. Nature 518: 360–364.
41. Poon SL, Pang ST, McPherson JR, Yu W, Huang KK, Guan P, Weng WH, Siew EY, Liu Y, Heng HL, et al. 2013. Genome-wide mutational signatures of aristolochic acid and its application as a screening tool. Sci Transl Med 5: 197ra101.
42. Ratain MJ, Kaminer LS, Bitran JD, Larson RA, Le Beau MM, Skosey C, Purl S, Hoffman PC, Wade J, Vardiman JW, et al. 1987. Acute nonlymphocytic leukemia following etoposide and cisplatin combination chemotherapy for advanced non-small-cell carcinoma of the lung. Blood 70: 1412–1417.
43. Reardon JT, Vaisman A, Chaney SG, Sancar A. 1999. Efficient nucleotide excision repair of cisplatin, oxaliplatin, and Bis-aceto-ammine-dichloro-cyclohexylamine-platinum(IV) (JM216) platinum intrastrand DNA diad-ducts. Cancer Res 59: 3968–3971.
44. Roy U, Scharer OD. 2016. Involvement of translesion synthesis DNA polymerases in DNA interstrand crosslink repair. DNA Repair (Amst) 44: 33–41.
45. Saunders CT, Wong WS, Swamy S, Becq J, Murray LJ, Cheetham RK. 2012. Strelka: accurate somatic small-variant calling from sequenced tumor–normal sample pairs. Bioinformatics 28: 1811–1817.
46. Schmidt MN, Larsen J, Hsiao FT. 2007. Wind noise reduction using nonnegative sparse coding. In 2007 IEEE workshop on machine learning for signal processing, pp. 431–436, Thessaloniki, Greece. doi: 10.1109/MLSP.2007.4414345.
47. Seplyarskiy VB, Bazykin GA, Soldatov RA. 2015. Polymerase ζ activity is linked to replication timing in humans: evidence from mutational signatures. Mol Biol Evol 32: 3158–3172.
48. Szikriszt B, Poti A, Pipek O, Krzystanek M, Kanu N, Molnar J, Ribli D, Szeltner Z, Tusnady GE, Csabai I, et al. 2016. A comprehensive survey of the mutagenic impact of common cancer cytotoxics. Genome Biol 17: 99.
49. Tarasov A, Vilella AJ, Cuppen E, Nijman IJ, Prins P. 2015. Sambamba: fast processing of NGS alignment formats. Bioinformatics 31: 2032–2034.
50. Travis LB, Fossa SD, Schonfeld SJ, McMaster ML, Lynch CF, Storm H, Hall P, Holowaty E, Andersen A, Pukkala E, et al. 2005. Second cancers among 40,576 testicular cancer patients: focus on long-term survivors. J Natl Cancer Inst 97: 1354–1365.
51. Waseem M, Bhardwaj M, Tabassum H, Raisuddin S, Parvez S. 2015. Cisplatin hepatotoxicity mediated by mitochondrial stress. Drug Chem Toxicol 38: 452–459.
52. Zamble DB, Mu D, Reardon JT, Sancar A, Lippard SJ. 1996. Repair of cisplatin–DNA adducts by the mammalian excision nuclease. Biochemistry 35: 10004–10013.
53. Zen C, Zen Y, Mitry RR, Corbeil D, Karbanova J, O’Grady J, Karani J, Kane P, Heaton N, Portmann BC, et al. 2011. Mixed phenotype hepatocellular carcinoma after transarterial chemoembolization and liver transplantation. Liver Transpl 17: 943–954.
54. Zhang J, Baran J, Cros A, Guberman JM, Haider S, Hsu J, Liang Y, Rivkin E, Wang J, Whitty B, et al. 2011. International Cancer Genome Consortium Data Portal—a one-stop shop for cancer genomics data. Database (Oxford) 2011: bar026.
55. Zhivagui M, Ardin M, Ng AWT, Churchwell M, Pandey M, Villar S, Cahais V, Robitaille A, Bouaoun L, Heguy A, et al. 2018. Experimental analysis of exome-scale mutational signature of glycidamide, the reactive metabolite of acrylamide. bioRxiv doi: 10.1101/254664.