Insights into RNA binding by the anticancer drug cisplatin from the crystal structure of cisplatin-modified ribosome

Nucleic Acids Research

Volumn 44, Issue 10, 2016, Pages 4978-4987

  Melnikov, Sergey V ^a   Söll, Dieter ^a   Steitz, Thomas A ^a   Polikanov, Yury S ^b  

^a YALE UNIVERSITY   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CISPLATIN; MESSENGER RNA; RIBOSOME RNA; ADENINE; AMICOUMACIN A; ANTIINFECTIVE AGENT; ANTINEOPLASTIC AGENT; COUMARIN DERIVATIVE; GUANINE; NUCLEIC ACID SYNTHESIS INHIBITOR;

ARTICLE; BINDING SITE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DRUG BINDING; DRUG TARGETING; INTERCALATION COMPLEX; MOLECULAR MODEL; NONHUMAN; PREDICTION; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RIBOSOME; RNA BINDING; RNA TRANSPORT; CHEMISTRY; METABOLISM; X RAY CRYSTALLOGRAPHY;

ADENINE; ANTI-BACTERIAL AGENTS; ANTINEOPLASTIC AGENTS; BINDING SITES; CISPLATIN; COUMARINS; CRYSTALLOGRAPHY, X-RAY; GUANINE; MODELS, MOLECULAR; NUCLEIC ACID SYNTHESIS INHIBITORS; RIBOSOMES; RNA, RIBOSOMAL;

EID: 84973332930     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkw246     Document Type: Article

References (44)

1. Rosenberg, B., Vancamp, L., Krigas, T. (1965) Inhibition of cell division in Escherichia coli by electrolysis products from a platinum electrode. Nature, 205, 698-699.
2. Rosenberg, B., VanCamp, L., Trosko, J.E., Mansour, V.H. (1969) Platinum compounds: a new class of potent antitumour agents. Nature, 222, 385-386.
3. Rosenberg, B. (1979) Anticancer activity of cis-dichlorodiammineplatinum(II) and some relevant chemistry. Cancer Treat. Rep., 63, 1433-1438.
4. Kelland, L. (2007) The resurgence of platinum-based cancer chemotherapy. Nat. Rev. Cancer, 7, 573-584.
5. Wheate, N.J., Walker, S., Craig, G.E., Oun, R. (2010) The status of platinum anticancer drugs in the clinic and in clinical trials. Dalton Trans., 39, 8113-8127.
6. Sava, G., Bergamo, A., Dyson, P.J. (2011) Metal-based antitumour drugs in the post-genomic era: what comes next? Dalton Trans., 40, 9069-9075.
7. Siddik, Z.H. (2003) Cisplatin: mode of cytotoxic action and molecular basis of resistance. Oncogene, 22, 7265-7279.
8. Wang, Guo, Z. (2007) The role of sulfur in platinum anticancer chemotherapy. Anticancer Agents Med. Chem., 7, 19-34.
9. Basu, A., Krishnamurthy, S. (2010) Cellular responses to cisplatin-induced DNA damage. J. Nucleic Acids, 2010, 1-16.
10. Wang, D., Lippard, S.J. (2005) Cellular processing of platinum anticancer drugs. Nat. Rev. Drug. Discov., 4, 307-320.
11. Chapman, E.G., Hostetter, A.A., Osborn, M.F., Miller, A.L., DeRose, V.J. (2011) Binding of kinetically inert metal ions to RNA: the case of platinum(II). Met. Ions Life Sci., 9, 347-377.
12. Rosenberg, J.M., Sato, P.H. (1988) Messenger RNA loses the ability to direct in vitro peptide synthesis following incubation with cisplatin. Mol. Pharmacol., 33, 611-616.
13. Hostetter, A.A., Chapman, E.G., DeRose, V.J. (2009) Rapid cross-linking of an RNA internal loop by the anticancer drug cisplatin. J. Am. Chem. Soc., 131, 9250-9257.
14. Chapman, E.G., DeRose, V.J. (2012) Site-specific platinum(II) cross-linking in a ribozyme active site. J. Am. Chem. Soc., 134, 256-262.
15. Becker, J.P., Weiss, J., Theile, D. (2014) Cisplatin, oxaliplatin, carboplatin unequally inhibit in vitro mRNA translation. Toxicol. Lett., 225, 43-47.
16. Burger, A.M., Double, J.A., Newell, D.R. (1997) Inhibition of telomerase activity by cisplatin in human testicular cancer cells. Eur. J. Cancer, 33, 638-644.
17. Colangelo, D., Ghiglia, A.L., Viano, I., Cavigiolio, G., Osella, D. (2003) Cis-[Pt(Cl)2(pyridine)(5-SO3H-isoquinoline)] complex, a selective inhibitor of telomerase enzyme. Biometals, 16, 553-560.
18. Rhodes, D., Piper, P.W., Clark, B.F. (1974) Location of a platinum binding site in the structure of yeast phenylalanine transfer RNA. J. Mol. Biol., 89, 469-475.
19. Sundaralingam, M., Rubin, J.R., Rao, S.T. (1985) X-ray studies on the interaction of the anticancer agent cis-[Pt(NH3)2cl2] to tRNAphe. A mechanism for the formation of the intrastrand cross-link to adjacent guanines in DNA. Prog. Clin. Biol. Res., 172, 175-184.
20. Polikanov, Y.S., Osterman, I.A., Szal, T., Tashlitsky, V.N., Serebryakova, M.V., Kusochek, P., Bulkley, D., Malanicheva, I.A., Efimenko, T.A., Efremenkova, O.V. et al. (2014) Amicoumacin A inhibits translation by stabilizing mRNA interaction with the ribosome. Mol. Cell, 56, 531-540.
21. Polikanov, Y.S., Steitz, T.A., Innis, C.A. (2014) A proton wire to couple aminoacyl-tRNA accommodation and peptide-bond formation on the ribosome. Nat. Struct. Mol. Biol., 21, 787-993.
22. Kabsch, W. (2010) XDS. Acta Cryst. Sect. D Biol. Cryst., 66, 125-132.
23. Polikanov, Y.S., Melnikov, S.V., Soll, D., Steitz, T.A. (2015) Structural insights into the role of rRNA modifications in protein synthesis and ribosome assembly. Nat. Struct. Mol. Biol., 22, 342-344.
24. Emsley, P., Lohkamp, B., Scott, W.G., Cowtan, K. (2010) Features and development of Coot. Acta Cryst. Sect. D Biol. Cryst., 66, 486-501.
25. Adams, P.D., Afonine, P.V., Bunkoczi, G., Chen, V.B., Davis, I.W., Echols, N., Headd, J.J., Hung, L.W., Kapral, G.J., Grosse-Kunstleve, R.W. et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Cryst. Sect. D Biol. Cryst., 66, 213-221.
26. Papsai, P., Aldag, J., Persson, T., Elmroth, S.K. (2006) Kinetic preference for interaction of cisplatin with the G-C-rich wobble basepair region in both tRNAAla and MhAla. Dalton Trans., 2006, 3515-3517.
27. Hagerlof, M., Papsai, P., Hedman, H.K., Jungwirth, U., Jenei, V., Elmroth, S.K. (2008) Cisplatin and siRNA interference with structure and function of Wnt-5a mRNA: design and in vitro evaluation of targeting AU-rich elements in the 3-UTR. J. Biol. Inorg. Chem., 13, 385-399.
28. Heminger, K.A., Hartson, S.D., Rogers, J., Matts, R.L. (1997) Cisplatin inhibits protein synthesis in rabbit reticulocyte lysate by causing an arrest in elongation. Arch. Biochem. Biophys., 344, 200-207.
29. Rosenberg, J.M., Sato, P.H. (1993) Cisplatin inhibits in vitro translation by preventing the formation of complete initiation complex. Mol. Pharmacol., 43, 491-497.
30. Szer, W., Kurylo-Borowska, Z. (1970) Effect of edeine on aminoacyl-tRNA binding to ribosomes and its relationship to ribosomal binding sites. Biochim. Biophys. Acta, 224, 477-486.
31. Kurylo-Borowska, Z. (1975) Edeines. In: John, WCaF and Hahn, E (eds). Mechanism of Action of Antimicrobial and Antitumor Agents. Springer, NY, Vol. 3, pp. 129-140.
32. Contreras, A., Carrasco, L. (1979) Selective inhibition of protein synthesis in virus-infected mammalian cells. J. Virol., 29, 114-122.
33. Pioletti, M., Schlunzen, F., Harms, J., Zarivach, R., Gluhmann, M., Avila, H., Bashan, A., Bartels, H., Auerbach, T., Jacobi, C. et al. (2001) Crystal structures of complexes of the small ribosomal subunit with tetracycline, edeine and IF3. EMBO J., 20, 1829-1839.
34. Dedduwa-Mudalige, G.N., Chow, C.S. (2015) Cisplatin targeting of bacterial ribosomal RNA hairpins. Int. J. Mol. Sci., 16, 21392-21409.
35. Osborn, M.F., White, J.D., Haley, M.M., DeRose, V.J. (2014) Platinum-RNA modifications following drug treatment in S. cerevisiae identified by click chemistry and enzymatic mapping. ACS Chem. Biol., 9, 2404-2411.
36. Hostetter, A.A., Osborn, M.F., DeRose, V.J. (2012) RNA-Pt adducts following cisplatin treatment of Saccharomyces cerevisiae. ACS Chem. Biol., 7, 218-225.
37. Durlach, J., Bara, M., Guiet-Bara, A., Collery, P. (1986) Relationship between magnesium, cancer and carcinogenic or anticancer metals. Anticancer Res., 6, 1353-1361.
38. Svidritskiy, E., Ling, C., Ermolenko, D.N., Korostelev, A.A. (2013) Blasticidin S inhibits translation by trapping deformed tRNA on the ribosome. Proc. Natl. Acad. Sci. U.S.A., 110, 12283-12288.
39. Polikanov, Y.S., Szal, T., Jiang, F., Gupta, P., Matsuda, R., Shiozuka, M., Steitz, T.A., Vazquez-Laslop, N., Mankin, A.S. (2014) Negamycin interferes with decoding and translocation by simultaneous interaction with rRNA and tRNA. Mol. Cell, 56, 541-550.
40. Olivier, N.B., Altman, R.B., Noeske, J., Basarab, G.S., Code, E., Ferguson, A.D., Gao, N., Huang, J., Juette, M.F., Livchak, S. et al. (2014) Negamycin induces translational stalling and miscoding by binding to the small subunit head domain of the Escherichia coli ribosome. Proc. Natl. Acad. Sci. U.S.A., 111, 16274-16279.
41. Polikanov, Y.S., Starosta, A.L., Juette, M.F., Altman, R.B., Terry, D.S., Lu, W., Burnett, B.J., Dinos, G., Reynolds, K.A., Blanchard, S.C. et al. (2015) Distinct tRNA accommodation intermediates observed on the ribosome with the antibiotics hygromycin A and A201A. Mol. Cell, 58, 832-844.
42. Kaminishi, T., Schedlbauer, A., Fabbretti, A., Brandi, L., Ochoa-Lizarralde, B., He, C.G., Milon, P., Connell, S.R., Gualerzi, C.O., Fucini, P. (2015) Crystallographic characterization of the ribosomal binding site and molecular mechanism of action of Hygromycin A. Nucleic Acids Res., 43, 10015-10025.
43. Anger, A.M., Armache, J.P., Berninghausen, O., Habeck, M., Subklewe, M., Wilson, D.N., Beckmann, R. (2013) Structures of the human and Drosophila 80S ribosome. Nature, 497, 80-85.
44. Gao, Y.G., Selmer, M., Dunham, C.M., Weixlbaumer, A., Kelley, A.C., Ramakrishnan, V. (2009) The structure of the ribosome with elongation factor G trapped in the posttranslocational state. Science, 326, 694-699.