Mechanistic studies on bleomycin-mediated DNA damage: Multiple binding modes can result in double-stranded DNA cleavage

Nucleic Acids Research

Volumn 36, Issue 11, 2008, Pages 3781-3790

  Chen, Jingyang ^a,b   Ghorai, Manas K ^a,c   Kenney, Grace ^a   Stubbe, JoAnne ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c INDIAN INSTITUTE OF TECHNOLOGY KANPUR   (India)

Author keywords

[No Author keywords available]

Indexed keywords

AMINE; BETA CYCLODEXTRIN; BLEOMYCIN; DOUBLE STRANDED DNA; PHOSPHORUS 32; PLASMID DNA;

ANIMAL TISSUE; ARTICLE; BINDING SITE; CATTLE; CHEMICAL REACTION; CONTROLLED STUDY; CYTOTOXICITY; DNA BINDING; DNA DAMAGE; DNA SEQUENCE; DRUG STRUCTURE; DRUG SYNTHESIS; INTERMETHOD COMPARISON; NONHUMAN; PRIORITY JOURNAL; THYMUS;

ANTIBIOTICS, ANTINEOPLASTIC; BASE SEQUENCE; BETA-CYCLODEXTRINS; BLEOMYCIN; DNA; DNA BREAKS, DOUBLE-STRANDED; DNA, SINGLE-STRANDED; DNA, SUPERHELICAL; INTERCALATING AGENTS; PLASMIDS;

EID: 46349109588     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkn302     Document Type: Article

References (51)

1. Umezawa,H., Maeda,K., Takeuchi,J. and Okami,Y. (1966) New antibiotics, bleomycin A and B. J. Antibiot., 19, 200-209.
2. Sikic,B.I., Rozencweig,M. and Carter,S.K. (1985) Bleomycin Chemotherapy. Academic Press, Orlando, Florida.
3. Einhorn,L.H. (2002) Curing metastatic testicular cancer. Proc. Natl Acad. Sci. USA, 99, 4592-4595.
4. Stubbe,J. and Kozarich,J.W. (1987) Mechanisms of bleomycin-induced DNA degradation. Chem. Rev., 87, 1107-1136.
5. Burger,R.M. (1998) Cleavage of nucleic acids by bleomycin. Chem. Rev. 98, 1153-1169.
6. Claussen,C.A. and Long,E.C. (1999) Nucleic acid recognition by metal complexes of bleomycin. Chem. Rev., 99, 2797-2816.
7. Chen,J. and Stubbe,J. (2004) Bleomycins: New methods will allow reinvestigation of old issues. Curr, Opin. Chem. Biol., 8, 175-181.
8. Povirk,L.F. (1996) DNA damage and mutagenesis by radiomimetic DNA-cleaving agents: Bleomycin, neocarzinostatin and other enediynes. Mutat. Res., 355, 71-89.
9. Chen,J. and Stubbe,J. (2005) Bleomycins: Towards better therapeutics. Nat. Rev. Cancer, 5, 102-112.
10. Povirk,L.F., Han,Y.H. and Steighner,R.J. (1989) Structure of bleomycin-induced DNA double-strand breaks: Predominance of blunt ends and single-base 5′ extensions. Biochemistry, 28, 5808-5814.
11. Povirk,L.F., Wübker,W., Köhnlein,W. and Hutchinson,F. (1977) DNA double-strand breaks and alkali-labile bonds produced by bleomycin. Nucleic Acids Res., 4, 3573-3580.
12. Steighner,R.J. and Povirk,L.F. (1990) Bleomycin-induced DNA lesions at mutational hot spots: Implications for the mechanism of double-strand cleavage. Proc. Natl Acad. Sci. USA, 87, 8350-8354.
13. Absalon,M.J., Kozatich,J.W. and Stubbe,J. (1995) Sequence-specific double-strand cleavage of DNA by Fe bleomycin. 1. The detection of sequence-specific double-strand breaks using hairpin oligonucleotides. Biochemistry, 34, 2065-2075.
14. Absalon,M.J., Wu,W., Kozurich,J.W. and Stubbe,J. (1995) Sequence-specific double-strand cleavage of DNA by Fe bleomycin.2. Mechanism and dynamics. Biochemistry, 34, 2076-2086.
15. 2: Recognition at the d(GpT) site and implications for double-stranded DNA cleavage. Chem. Biol., 4, 373-387.
16. 2: Evidence for intercalation using 2D NMR. J. Am. Chem. Soc., 116, 10843-10844.
17. Quada,J.C., Levy,M.J. and Hecht,S.M. (1993) Highly efficient DNA strand scission by photoactivated chlorobithiazoles. J. Am. Chem. Soc., 115, 12171-12172.
18. Zuber,G., Quada,J.C. and Hecht,S.M. (1998) Sequence selective cleavage of a DNA octanucleotide by chlorinated bithiazoles and bleomycins. J. Am. Chem. Soc., 120, 9368-9369.
19. Abraham,A.T., Zhou,X. and Hecht,S.M. (1999) DNA cleavage by Fe(II)-bleomycin conjugated to a solid support. J. Am. Chem. Soc., 121, 1892-1893.
20. Abraham,A.T., Zhou,X. and Hecht,S.M. (2001) Metallobleomycin-mediated cleavage of DNA not involving a threading-intercalation mechanism. J. Am. Chem. Soc., 123, 5167-5175.
21. Choudhury,A.K., Tao,Z.F. and Hecht,S.M. (2001) Synthesis and DNA cleavage activity of a novel bleomycin A(5) glycoconjugate. Org. Lett., 3, 1291-1294.
22. Schmidt,A.K., Cottaz,S., Driguez,H. and Schulz,G.E. (1998) Structure of cyclodextrin glycosyltransferase complexed with a derivative of its main product beta-cyclodextrin. Biochemistry, 37, 5909-5915.
23. Leroy,J.L., Kochoyan,M., Huynh-Dinh,T. and Gueron,M. (1988) Characterization of base-pair opening in deoxynucleotide duplexes using catalyzed exchange of the imino proton. J. Mol. Biol., 200, 223-238.
24. Sambrook,J., Fritsch,E.F. and Maniatis,T. (1989) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
25. Hamasaki,K., Ikeda,H., Nakamura,A., Ueno,A., Toda,F., Suzuki,I. and Osa,T. (1993) Fluorescent sensors of molecular recognition. Modified cyclodextrins capable of exhibiting guest-responsive twisted intramolecular charge transfer fluorescence. J. Am. Chem. Soc., 115, 5035-5040.
26. Huang,C.H., Mirabelli,C.K., Jan,Y. and Crooke,S.T. (1981) Single-strand and double-strand deoxyribonucleic acid breaks produced by several bleomycin analogues. Biochemistry, 20, 233-238.
27. Mirabelli,C.K., Huang,C.-H., Fenwick,R.G. and Crooke,S.T. (1985) Quantitative measurement of single- and double-strand breakage of DNA in Escherichia coli by the antitumor antibiotics bleomycin and talisomycin. Antimicrob. Agents Chemother., 27, 460-467.
28. Povirk,L.F. and Houlgrave,C.W. (1988) Effect of apurinic/apyrimidic endonucleases and polyamines on DNA treated with bleomycin and neocarzinostatin: Specific formation and cleavage of closely opposed lesions in complementary strands. Biochemistry, 27, 3850-3857.
29. Onfelt,B., Lincoln,P. and Norden,B. (1999) A molecular staple for DNA: threading bis-intercalating [Ru(phen)(2)dppzl(2+) dimer. J. Am. Chem. Soc., 121, 10846-10847.
30. Povirk,L.F., Hogan,M. and Dattagupta,N. (1979) Binding of bleomycin to DNA: Intercalation of the bithiazole rings. Biochemistry, 18 96-101.
31. Fox,K.R., Grigg,G.W. and Waring,M.J. (1987) Sequence-selective binding of phleomycin to DNA. Biochem. J., 243, 847-851.
32. Kross,J., Henner,D., Hecht,S.M. and Haseltine,W.A. (1982) Specificity of deoxyribonulceic acid cleavage by bleomycin, phleomycin, and tallysomycin. Biochemistry, 21, 4310-4318.
33. Hamamichi,N. and Hecht,S.M. (1993) Determination of the absolute-configuration of the thiazolinylthiazole moiety of phleomycin. J. Am. Chem. Soc., 115, 12605-12606.
34. 2: Evidence for binding by partial intercalation. Nucleic Acids Res., 30, 4881-4891.
35. Boger,D.L., Ramsey,T.M., Cai,H., Hoehn,S.T., Kozarich,J.W. and Stubbe,J. (1998) Assessment of the role of the bleomycin A2 pyrimidoblamic acid C4 amino group. J. Am. Chem: Soc., 120, 53-65.
36. Boger,D.L., Ramsey,T.M., Cai,H., Hoehn,S.T. and Stubbe,J.A. (1999) A systematic evaluation of the bleomycin A2 L-threonine side chain: Its role in preorganization of a compact conformation implicated in sequence-selective DNA cleavage. J. Am. Chem. Soc., 120, 9139-9148.
37. Hoehn,S.T., Junker,H.D., Bunt,R.C., Turner,C.J. and Stubbe,J. (2001) Solution structure of Co(III)-bleomycin-OOH bound to a phosphoglycolate lesion containing oligonucleotide: Implications for bleomycin-induced double-strand DNA cleavage. Biochemistry, 40, 5894-5905.
38. McGall,G.H., Rabow,L.E., Ashley,G.W., Wu,S.H., Kozarich,J.W. and Stubbe,J. (1992) New insight into the mechanism of base propenal formation during bleomycin-mediated DNA degradation. J. Am. Chem. Soc., 114, 4958-4967.
39. 2. J. Am. Chem. Soc., 109, 2836-2837.
40. Burger,R.M., Drlica,K. and Birdsall,B. (1994) The DNA cleavage pathway of iron bleomycin. J. Biol. Chem., 269, 25978-25985.
41. Palecek,E. (1991) Local supercoil-stabilized DNA structures. Crit. Rev. Biochem. Mol. Biol., 26, 151-226.
42. Carter,B.J., de Vroom,E., Long,E.C., van der Marel,G.A., van Boom,J.H. and Hecht,S.M. (1990) Site-specific cleavage of RNA by Fe(II)•bleomycin. Proc. Natl Acad. Sci. USA, 87, 9373-9377.
43. Holmes,C.E., Abraham,A.T., Hecht,S.M., Florentz,C. and Giege,R. (1996) Fe bleomycin as a probe of RNA conformation. Nucleic Acids Res., 24, 3399-3406.
44. Smith,B.L., Bauer,G.B. and Povirk,L.F. (1994) DNA damage induced by bleomycin, neocarzinostatin, and melphalan in a precisely positioned nucleosome. J. Biol. Chem., 269, 30597-30594.
45. Pron,G., Belehradek,J.,Jr and Mir,L.M. (1993) Identification of a plasma membrane protein that specifically binds bleomycin. Biochem. Biophys. Res. Commun., 194, 333-337.
46. Pron,G., Mahrour,N., Orlowski,S., Tounekti,O., Poddevin,B., Belehradek,J.,Jr and Mir,L.M. (1999) Internalisation of the bleomycin molecules responsible for bleomycin toxicity: A receptor-mediated endocytosis mechanism. Biochem. Pharmacol., 57, 45-56.
47. Aouida,M., Page,N., Leduc,A., Peter,M. and Ramotar,D. (2004) A genome-wide screen in Saccharomyces cerevisiae reveals altered transport as a mechanism of resistance to the anticancer drug bleomycin. Cancer Res., 64, 1102-1109.
48. Aouida,M., Tounekti,O., Leduc,A., Belhadj,O., Mir,L. and Ramotar,D. (2004) Isolation and characterization of Saccharomyces cerevisiae mutants with enhanced resistance to the anticancer drug bleomycin. Curr. Genet., 45, 265-272.
49. Roy,S.N. and Horwitz,S.B. (1984) Characterization of the association of radiolabeled bleomycin A2 with HeLa cells. Cancer Res., 44, 1541-1546.
50. Lyman,S., Ujjani,B., Renner,K., Antholine,W., Petering,D.H., Whetstone,J.W. and Knight,J.M. (1986) Properties of the initial reaction of bleomycin and several of its metal complexes with Ehrlich cells. Cancer Res., 46, 4472-4478.
51. Kenani,A., Bailly,C., Houssin,R. and Henichart,J.P. (1994) Comparative subcellular distribution of the copper complexes of bleomycin-A2 and deglycobleomycin-A2. Anticancer Drugs, 5, 199-201.