Inhibition of type IA topoisomerase by a monoclonal antibody through perturbation of DNA cleavage-religation equilibrium

FEBS Journal

Volumn 279, Issue 1, 2012, Pages 55-65

  Leelaram, Majety Naga ^a   Bhat, Anuradha Gopal ^a   Hegde, Shivanand Manjunath ^a   Manjunath, Ramanathapuram ^a   Nagaraja, Valakunja ^a,b  

^a INDIAN INSTITUTE OF SCIENCE   (India)

^b JAWAHARLAL NEHRU CENTRE FOR ADVANCED SCIENTIFIC RESEARCH   (India)

Author keywords

monoclonal antibody; mycobacteria; protein DNA complex; topoisomerase I; transesterification

Indexed keywords

DNA TOPOISOMERASE; DNA TOPOISOMERASE (ATP HYDROLYSING); IMMUNOGLOBULIN G2B; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 2F3G4; SINGLE STRANDED DNA; TYPE 1A DNA TOPOISOMERASE; UNCLASSIFIED DRUG;

ANTIBODY AFFINITY; ANTIBODY SPECIFICITY; ARTICLE; CHEMICAL MODIFICATION; CONTROLLED STUDY; COVALENT BOND; DNA CLEAVAGE; DNA CLEAVAGE RELIGATION; DNA STRAND BREAKAGE; ENZYME ACTIVITY; ENZYME BINDING; ENZYME INHIBITION; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME MECHANISM; ENZYME STRUCTURE; ENZYME SUBSTRATE; EPITOPE MAPPING; GENE TARGETING; IMMUNOBLOTTING; MOLECULAR BIOLOGY; MYCOBACTERIUM SMEGMATIS; NONHUMAN; PERTURBATION THEORY; PRIORITY JOURNAL; PROTEIN DNA BINDING; TRANSESTERIFICATION;

ANTIBODIES, MONOCLONAL; DNA ADDUCTS; DNA CLEAVAGE; DNA TOPOISOMERASES, TYPE I; DNA, BACTERIAL; DNA, SUPERHELICAL; KINETICS; MUTATION; MYCOBACTERIUM SMEGMATIS;

BACTERIA (MICROORGANISMS); CORYNEBACTERINEAE; MYCOBACTERIUM SMEGMATIS;

EID: 83655184731     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2011.08398.x     Document Type: Article

References (45)

1. Champoux JJ, (2001) DNA topoisomerases: structure, function, and mechanism. Annu Rev Biochem 70, 369-413. (Pubitemid 32662215)
2. Gellert M, (1981) DNA topoisomerases. Annu Rev Biochem 50, 879-910.
3. Corbett KD, &, Berger JM, (2004) Structure, molecular mechanisms, and evolutionary relationships in DNA topoisomerases. Annu Rev Biophys Biomol Struct 33, 95-118. (Pubitemid 38829953)
4. Dean FB, &, Cozzarelli NR, (1985) Mechanism of strand passage by Escherichia coli topoisomerase I. The role of the required nick in catenation and knotting of duplex DNA. J Biol Chem 260, 4984-4994. (Pubitemid 15038694)
5. Low RL, Kaguni JM, &, Kornberg A, (1984) Potent catenation of supercoiled and gapped DNA circles by topoisomerase I in the presence of a hydrophilic polymer. J Biol Chem 259, 4576-4581. (Pubitemid 14131364)
6. Tse Y, &, Wang JC, (1980) E. coli and M. luteus DNA topoisomerase I can catalyze catenation of decatenation of double-stranded DNA rings. Cell 22, 269-276. (Pubitemid 11226448)
7. Wang JC, (2002) Cellular roles of DNA topoisomerases: a molecular perspective. Nat Rev Mol Cell Biol 3, 430-440. (Pubitemid 34685700)
8. Liu LF, (1989) DNA topoisomerase poisons as antitumor drugs. Annu Rev Biochem 58, 351-375. (Pubitemid 19172974)
9. Chen AY, &, Liu LF, (1994) DNA topoisomerases: essential enzymes and lethal targets. Annu Rev Pharmacol Toxicol 34, 191-218.
10. Maxwell A, (1997) DNA gyrase as a drug target. Trends Microbiol 5, 102-109. (Pubitemid 27139470)
11. Hooper DC, &, Wolfson JS, (1991) Fluoroquinolone antimicrobial agents. N Engl J Med 324, 384-394.
12. Froelich-Ammon SJ, &, Osheroff N, (1995) Topoisomerase poisons: harnessing the dark side of enzyme mechanism. J Biol Chem 270, 21429-21432.
13. Drlica K, Malik M, Kerns RJ, &, Zhao X, (2008) Quinolone-mediated bacterial death. Antimicrob Agents Chemother 52, 385-392. (Pubitemid 351170804)
14. Nitiss JL, (2002) DNA topoisomerases in cancer chemotherapy: using enzymes to generate selective DNA damage. Curr Opin Investig Drugs 3, 1512-1516.
15. Zhu Q, Pongpech P, &, DiGate RJ, (2001) Type I topoisomerase activity is required for proper chromosomal segregation in Escherichia coli. Proc Natl Acad Sci USA 98, 9766-9771. (Pubitemid 32769378)
16. Fisher LM, Austin CA, Hopewell R, Margerrison EE, Oram M, Patel S, Plummer K, Sng JH, &, Sreedharan S, (1992) DNA supercoiling and relaxation by ATP-dependent DNA topoisomerases. Philos Trans R Soc Lond B Biol Sci 336, 83-91.
17. Bhat AG, Leelaram MN, Hegde SM, &, Nagaraja V, (2009) Deciphering the distinct role for the metal coordination motif in the catalytic activity of Mycobacterium smegmatis topoisomerase I. J Mol Biol 393, 788-802.
18. Cheng B, Annamalai T, Sorokin E, Abrenica M, Aedo S, &, Tse-Dinh YC, (2009) Asp-to-Asn substitution at the first position of the DxD TOPRIM motif of recombinant bacterial topoisomerase I is extremely lethal to E. coli. J Mol Biol 385, 558-567.
19. Cheng B, Sorokin EP, &, Tse-Dinh YC, (2008) Mutation adjacent to the active site tyrosine can enhance DNA cleavage and cell killing by the TOPRIM Gly to Ser mutant of bacterial topoisomerase I. Nucleic Acids Res 36, 1017-1025. (Pubitemid 351267255)
20. Corbett EL, Watt CJ, Walker N, Maher D, Williams BG, Raviglione MC, &, Dye C, (2003) The growing burden of tuberculosis: global trends and interactions with the HIV epidemic. Arch Intern Med 163, 1009-1021. (Pubitemid 36548927)
21. Kaufmann SH, &, van Embden JD, (1993) Tuberculosis: a neglected disease strikes back. Trends Microbiol 1, 2-5. (Pubitemid 23187151)
22. Sassetti CM, &, Rubin EJ, (2003) Genetic requirements for mycobacterial survival during infection. Proc Natl Acad Sci USA 100, 12989-12994. (Pubitemid 37340013)
23. Guilhot C, Otal I, Van Rompaey I, Martin C, &, Gicquel B, (1994) Efficient transposition in mycobacteria: construction of Mycobacterium smegmatis insertional mutant libraries. J Bacteriol 176, 535-539. (Pubitemid 24034077)
24. Bhaduri T, Bagui TK, Sikder D, &, Nagaraja V, (1998) DNA topoisomerase I from Mycobacterium smegmatis. An enzyme with distinct features. J Biol Chem 273, 13925-13932. (Pubitemid 28268447)
25. Nagaraja V, Sikder D, &, Jain P, (2002) DNA topoisomerase I from mycobacteria-a potential drug target. Curr Pharm Des 8, 1995-2007. (Pubitemid 34982166)
26. Leelaram MN, Bhat AG, Suneetha N, Nagaraja V, &, Manjunath R, (2009) Immunological cross-reactivity of mycobacterial topoisomerase I and divergence from other bacteria. Tuberculosis (Edinb) 89, 256-262.
27. Bhaduri T, Sikder D, &, Nagaraja V, (1998) Sequence specific interaction of Mycobacterium smegmatis topoisomerase I with duplex DNA. Nucleic Acids Res 26, 1668-1674. (Pubitemid 28291801)
28. Drlica K, &, Malik M, (2003) Fluoroquinolones: action and resistance. Curr Top Med Chem 3, 249-282.
29. Cheng B, Liu IF, &, Tse-Dinh YC, (2007) Compounds with antibacterial activity that enhance DNA cleavage by bacterial DNA topoisomerase I. J Antimicrob Chemother 59, 640-645. (Pubitemid 47073396)
30. Drlica K, &, Zhao X, (1997) DNA gyrase, topoisomerase IV, and the 4-quinolones. Microbiol Mol Biol Rev 61, 377-392. (Pubitemid 28090230)
31. Pohlhaus JR, &, Kreuzer KN, (2005) Norfloxacin-induced DNA gyrase cleavage complexes block Escherichia coli replication forks, causing double-stranded breaks in vivo. Mol Microbiol 56, 1416-1429. (Pubitemid 40780640)
32. Flatman RH, Howells AJ, Heide L, Fiedler HP, &, Maxwell A, (2005) Simocyclinone D8, an inhibitor of DNA gyrase with a novel mode of action. Antimicrob Agents Chemother 49, 1093-1100. (Pubitemid 40327729)
33. Roca J, Ishida R, Berger JM, Andoh T, &, Wang JC, (1994) Antitumor bisdioxopiperazines inhibit yeast DNA topoisomerase II by trapping the enzyme in the form of a closed protein clamp. Proc Natl Acad Sci USA 91, 1781-1785. (Pubitemid 24080289)
34. Classen S, Olland S, &, Berger JM, (2003) Structure of the topoisomerase II ATPase region and its mechanism of inhibition by the chemotherapeutic agent ICRF-187. Proc Natl Acad Sci USA 100, 10629-10634. (Pubitemid 37140080)
35. Bromberg KD, Burgin AB, &, Osheroff N, (2003) Quinolone action against human topoisomerase IIα: stimulation of enzyme-mediated double-stranded DNA cleavage. Biochemistry 42, 3393-3398. (Pubitemid 36368632)
36. Sengupta S, &, Nagaraja V, (2008) YacG from Escherichia coli is a specific endogenous inhibitor of DNA gyrase. Nucleic Acids Res 36, 4310-4316.
37. Sengupta S, Shah M, &, Nagaraja V, (2006) Glutamate racemase from Mycobacterium tuberculosis inhibits DNA gyrase by affecting its DNA-binding. Nucleic Acids Res 34, 5567-5576. (Pubitemid 44742444)
38. Changela A, DiGate RJ, &, Mondragon A, (2001) Crystal structure of a complex of a type IA DNA topoisomerase with a single-stranded DNA molecule. Nature 411, 1077-1081. (Pubitemid 32612335)
39. Manjunatha UH, Maxwell A, &, Nagaraja V, (2005) A monoclonal antibody that inhibits mycobacterial DNA gyrase by a novel mechanism. Nucleic Acids Res 33, 3085-3094. (Pubitemid 41194453)
40. Lima CD, Wang JC, &, Mondragon A, (1994) Three-dimensional structure of the 67K N-terminal fragment of E. coli DNA topoisomerase I. Nature 367, 138-146. (Pubitemid 24031694)
41. Changela A, DiGate RJ, &, Mondragon A, (2007) Structural studies of E. coli topoisomerase III-DNA complexes reveal a novel type IA topoisomerase-DNA conformational intermediate. J Mol Biol 368, 105-118. (Pubitemid 46441213)
42. Feinberg H, Lima CD, &, Mondragón A, (1999) Conformational changes in E. coli DNA topoisomerase I. Nat Struct Biol 6, 918-922. (Pubitemid 29463303)
43. Jain P, &, Nagaraja V, (2006) Indispensable, functionally complementing N and C-terminal domains constitute site-specific topoisomerase I. J Mol Biol 357, 1409-1421.
44. Leelaram MN, Suneetha N, Nagaraja V, &, Manjunath R, (2010) A new ELISA plate based microtiter well assay for mycobacterial topoisomerase I for the direct screening of enzyme inhibitory monoclonal antibody supernatants. J Immunol Methods 357, 26-32.
45. Bhaduri T, &, Nagaraja V, (1994) DNA topoisomerase I from Mycobacterium smegmatis. Indian J Biochem Biophys 31, 339-343.