Structural basis of human DNA polymerase η-mediated chemoresistance to cisplatin

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 19, 2012, Pages 7269-7274

  Zhao, Ye ^a,b   Biertümpfel, Christian ^b,c   Gregory, Mark T ^b,d   Hua, Yue Jin ^a   Hanaoka, Fumio ^e,f   Yang, Wei ^b  

^a ZHEJIANG UNIVERSITY   (China)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^c MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^d JOHNS HOPKINS UNIVERSITY   (United States)

^e OSAKA UNIVERSITY   (Japan)

^f GAKUSHUIN UNIVERSITY   (Japan)

Author keywords

Chemotherapy; Inhibitor; Translesion DNA synthesis; Yeast polymerase

Indexed keywords

CISPLATIN; DEOXYCYTIDINE; DNA DIRECTED DNA POLYMERASE ETA;

ARTICLE; BINDING SITE; COMPLEX FORMATION; CRYSTAL STRUCTURE; DNA BINDING; HYDROPHOBICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN CROSS LINKING; YEAST;

ADENOSINE TRIPHOSPHATE; BASE SEQUENCE; BINDING SITES; CISPLATIN; CROSS-LINKING REAGENTS; CRYSTALLOGRAPHY, X-RAY; DNA; DNA-DIRECTED DNA POLYMERASE; DRUG RESISTANCE; HUMANS; KINETICS; MODELS, MOLECULAR; MOLECULAR STRUCTURE; MUTATION; NEOPLASMS; NUCLEIC ACID CONFORMATION; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; PYRIMIDINE DIMERS; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84860792390     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1202681109     Document Type: Article

References (45)

1. Rosenberg B, VanCamp L, Trosko JE, Mansour VH (1969) Platinum compounds: A new class of potent antitumour agents. Nature 222:385-386.
2. Wheate NJ, Walker S, Craig GE, Oun R (2010) The status of platinum anticancer drugs in the clinic and in clinical trials. Dalton Trans 39:8113-8127.
3. Jung Y, Lippard SJ (2007) Direct cellular responses to platinum-induced DNA damage. Chem Rev 107:1387-1407. (Pubitemid 46864967)
4. Cepeda V, et al. (2007) Biochemical mechanisms of cisplatin cytotoxicity. Anticancer Agents Med Chem 7:3-18. (Pubitemid 46062402)
5. Howell SB, Safaei R, Larson CA, Sailor MJ (2010) Copper transporters and the cellular pharmacology of the platinum-containing cancer drugs. Mol Pharmacol 77:887-894.
6. Reardon JT, Sancar A (2005) Nucleotide excision repair. Prog Nucleic Acid Res Mol Biol 79:183-235. (Pubitemid 43583902)
7. Hanawalt PC, Spivak G (2008) Transcription-coupled DNA repair: Two decades of progress and surprises. Nat Rev Mol Cell Biol 9:958-970.
8. Strauss BS (1985) Translesion DNA synthesis: Polymerase response to altered nucleotides. Cancer Surv 4:493-516.
9. Mamenta EL, et al. (1994) Enhanced replicative bypass of platinum-DNA adducts in cisplatin-resistant human ovarian carcinoma cell lines. Cancer Res 54:3500-3505. (Pubitemid 24225973)
10. Chaney SG, Campbell SL, Bassett E, Wu Y (2005) Recognition and processing of cisplatin- and oxaliplatin-DNA adducts. Crit Rev Oncol Hematol 53:3-11. (Pubitemid 39656106)
11. Xie K, Doles J, Hemann MT, Walker GC (2010) Error-prone translesion synthesis mediates acquired chemoresistance. Proc Natl Acad Sci USA 107:20792-20797.
12. Vaisman A, Masutani C, Hanaoka F, Chaney SG (2000) Efficient translesion replication past oxaliplatin and cisplatin GpG adducts by human DNA polymerase eta. Biochemistry 39:4575-4580. (Pubitemid 30225320)
13. Masutani C, Kusumoto R, Iwai S, Hanaoka F (2000) Mechanisms of accurate translesion synthesis by human DNA polymerase η. EMBO J 19:3100-3109. (Pubitemid 30386780)
14. Bassett E, et al. (2004) The role of DNA polymerase eta in translesion synthesis past platinum-DNA adducts in human fibroblasts. Cancer Res 64:6469-6475. (Pubitemid 39297902)
15. Masutani C, et al. (1999) The XPV (xeroderma pigmentosum variant) gene encodes human DNA polymerase η. Nature 399:700-704. (Pubitemid 29289067)
16. Johnson RE, Kondratick CM, Prakash S, Prakash L (1999) hRAD30 mutations in the variant form of xeroderma pigmentosum. Science 285:263-265. (Pubitemid 29330001)
17. Lehmann AR (2002) Replication of damaged DNA in mammalian cells: New solutions to an old problem. Mutat Res 509:23-34.
18. Albertella MR, Green CM, Lehmann AR, O'Connor MJ (2005) A role for polymerase eta in the cellular tolerance to cisplatin-induced damage. Cancer Res 65:9799-9806. (Pubitemid 41541457)
19. Chen YW, Cleaver JE, Hanaoka F, Chang CF, Chou KM (2006) A novel role of DNA polymerase eta in modulating cellular sensitivity to chemotherapeutic agents. Mol Cancer Res 4:257-265.
20. Ceppi P, et al. (2009) Polymerase eta mRNA expression predicts survival of non-small cell lung cancer patients treated with platinum-based chemotherapy. Clin Cancer Res 15:1039-1045.
21. Teng KY, et al. (2010) DNA polymerase η protein expression predicts treatment response and survival of metastatic gastric adenocarcinoma patients treated with oxaliplatin-based chemotherapy. J Transl Med 8:126.
22. Suo Z, Lippard SJ, Johnson KA (1999) Single d(GpG)/cis- diammineplatinum(II) adductinduced inhibition of DNA polymerization. Biochemistry 38:715-726.
23. Wong JH, et al. (2010) Structural insight into dynamic bypass of the major cisplatin- DNA adduct by Y-family polymerase Dpo4. EMBO J 29:2059-2069.
24. Brown JA, Newmister SA, Fiala KA, Suo Z (2008) Mechanism of double-base lesion bypass catalyzed by a Y-family DNA polymerase. Nucleic Acids Res 36:3867-3878. (Pubitemid 351984804)
25. Biertümpfel C, et al. (2010) Structure and mechanism of human DNA polymerase eta. Nature 465:1044-1048.
26. Silverstein TD, et al. (2010) Structural basis for the suppression of skin cancers by DNA polymerase eta. Nature 465:1039-1043.
27. Masutani C, et al. (1999) Xeroderma pigmentosum variant (XP-V) correcting protein from HeLa cells has a thymine dimer bypass DNA polymerase activity. EMBO J 18: 3491-3501. (Pubitemid 29276594)
28. Johnson RE, Prakash S, Prakash L (1999) Efficient bypass of a thymine-thymine dimer by yeast DNA polymerase, Poleta. Science 283:1001-1004.
29. McCulloch SD, et al. (2004) Preferential cis-syn thymine dimer bypass by DNA polymerase η occurs with biased fidelity. Nature 428:97-100. (Pubitemid 38332365)
30. Park H, et al. (2002) Crystal structure of a DNA decamer containing a cis-syn thymine dimer. Proc Natl Acad Sci USA 99:15965-15970. (Pubitemid 35462732)
31. Wu Y, et al. (2007) Solution structures of a DNA dodecamer duplex with and without a cisplatin 1,2-d(GG) intrastrand cross-link: Comparison with the same DNA duplex containing an oxaliplatin 1,2-d(GG) intrastrand cross-link. Biochemistry 46:6477-6487. (Pubitemid 46876489)
32. Takahara PM, Rosenzweig AC, Frederick CA, Lippard SJ (1995) Crystal structure of double-stranded DNA containing the major adduct of the anticancer drug cisplatin. Nature 377:649-652.
33. Alt A, et al. (2007) Bypass of DNA lesions generated during anticancer treatment with cisplatin by DNA polymerase eta. Science 318:967-970. (Pubitemid 350098991)
34. Kusumoto R, Masutani C, Iwai S, Hanaoka F (2002) Translesion synthesis by human DNA polymerase eta across thymine glycol lesions. Biochemistry 41:6090-6099. (Pubitemid 34498915)
35. Shachar S, et al. (2009) Two-polymerase mechanisms dictate error-free and errorprone translesion DNA synthesis in mammals. EMBO J 28:383-393.
36. Spingler B, Whittington DA, Lippard SJ (2001) 2.4 A crystal structure of an oxaliplatin 1,2-d(GpG) intrastrand cross-link in a DNA dodecamer duplex. Inorg Chem 40: 5596-5602. (Pubitemid 32999342)
37. Todd RC, Lippard SJ (2010) Structure of duplex DNA containing the cisplatin 1,2-Pt(NH3)22+-d(GpG) cross-link at 1.77 A resolution. J Inorg Biochem 104:902-908.
38. Glick E, Vigna KL, Loeb LA (2001) Mutations in human DNA polymerase eta motif II alter bypass of DNA lesions. EMBO J 20:7303-7312. (Pubitemid 34062321)
39. Vaisman A, Ling H, Woodgate R, YangW(2005) Fidelity of Dpo4: Effect of metal ions, nucleotide selection and pyrophosphorolysis. EMBO J 24:2957-2967. (Pubitemid 41486333)
40. Wilson RC, Pata JD (2008) Structural insights into the generation of single-base deletions by the Y family DNA polymerase dbh. Mol Cell 29:767-779. (Pubitemid 351400923)
41. Kirouac KN, Ling H (2009) Structural basis of error-prone replication and stalling at a thymine base by human DNA polymerase iota. EMBO J 28:1644-1654.
42. Livneh Z, Ziv O, Shachar S (2010) Multiple two-polymerase mechanisms in mammalian translesion DNA synthesis. Cell Cycle 9:729-735.
43. Hirota K, et al. (2010) Simultaneous disruption of two DNA polymerases, Polη and Polζ, in Avian DT40 cells unmasks the role of Polη in cellular response to various DNA lesions. PLoS Genet 6:e1001151.
44. Yang W (2006) Poor base stacking at DNA lesions may initiate recognition by many repair proteins. DNA Repair 5:654-666.
45. Wang F, Yang W (2009) Structural insight into translesion synthesis by DNA Pol II. Cell 139:1279-1289.