Role of a tryptophan anchor in human topoisomerase I structure, function and inhibition

Biochemical Journal

Volumn 411, Issue 3, 2008, Pages 523-530

  Laco, Gary S ^a   Pommier, Yves ^b  

^a LAKE ERIE COLLEGE OF OSTEOPATHIC MEDICINE   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Camptothecin; Distributive relaxation; Interaction energy score; Processive relaxation; Topoisomerase I; Tryptophan anchor

Indexed keywords

AMINO ACIDS; AROMATIC COMPOUNDS; CELLS; DNA;

CAMPTOTHECIN; DISTRIBUTIVE RELAXATION; INTERACTION ENERGY SCORE; PROCESSIVE RELAXATION; TOPOISOMERASE I; TRYPTOPHAN ANCHOR;

ENZYMES;

ALANINE; CAMPTOTHECIN; DNA TOPOISOMERASE; TRYPTOPHAN; DNA;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; COMPUTER MODEL; ELECTRICITY; ENZYME INHIBITION; ENZYME STRUCTURE; IN VITRO STUDY; MUTANT; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; WILD TYPE; AMINO ACID SEQUENCE; ANIMAL; ARMYWORM; CELL LINE; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME ACTIVATION; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; PROTEIN BINDING; PROTEIN TERTIARY STRUCTURE; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; ANIMALS; CELL LINE; DNA; DNA TOPOISOMERASES, TYPE I; ELECTROSTATICS; ENZYME ACTIVATION; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; SPODOPTERA; TRYPTOPHAN;

EID: 42449119272     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20071436     Document Type: Article

References (44)

1. Champoux, J. J. and Dulbecco, R. (1972) An activity from mammalian cells that untwists superhelical DNA: a possible swivel for DNA replication (polyoma-ethidium bromide-mouse-embryo cells-dye binding assay). Proc. Natl. Acad. Sci. U.S.A. 69, 143-146
2. Champoux, J. J. (2001) DNA topoisomerases: structure, function, and mechanism. Annu. Rev. Biochem. 70, 369-413
3. Pommier, Y., Pourquier, P., Fan, Y. and Strumberg, D. (1998) Mechanism of action of eukaryotic DNA topoisomerase I and drugs targeted to the enzyme. Biochim. Biophys. Acta 1400, 83-105
4. Chen, A. Y. and Liu, L. F. (1994) DNA topoisomerases: essential enzymes and lethal targets. Annu. Rev. Pharmacol. Toxicol. 94, 194-218
5. Wang, J. C. (1996) DNA topoisomerases. Annu. Rev. Biochem. 65, 635-692
6. Champoux, J. J. (1998) Domains of human topoisomerase I and associated functions. Prog. Nucleic Acids Res. Mol. Biol. 60, 111-132
7. Redinbo, M. R., Stewart, L., Kuhn, P., Champoux, J. J. and Hol, W. G. (1998) Crystal structures of human topoisomerase I in covalent and noncovalent complexes with DNA. Science 279, 1504-1513
8. Pommier, Y., Laco, G. S., Kohlhagen, G., Sayer, J. M., Kroth, H. and Jerina, D. M. (2000) Position-specific trapping of topoisomerase I-DNA cleavage complexes by intercalated benzo[a]-pyrene diol epoxide adducts at the 6-amino group of adenine. Proc. Natl. Acad. Sci. U.S.A. 97, 10739-10744
9. Laco, G. S., Collins, J. R., Luke, B. T., Kroth, K., Sayer, J. M., Jerina, D. M. and Pommier, Y. (2002) Human topoisomerase I inhibition: docking camptothecin and derivatives into a structure-based active site model. Biochemistry 41, 1428-1435
10. Laco, G. S., Wu, D., Kohlhagen, G., Sayer, J. M., Jerina, D. M., Burke, T. G., Curran, D. P. and Pommier, Y. (2004) Analysis of human topoisomerase I inhibition and interaction with the cleavage site +1 deoxyguanosine, via in vitro experiments and molecular modeling studies. Bioorg. Med. Chem. 12, 5225-5235
11. D'Arpa, P., Machlin, P. S., Ratrie, 3rd, H., Rothfield, N. F., Cleveland, D. W. and Earnshaw, W. C. (1988) cDNA cloning of human DNA topoisomerase I: catalytic activity of a 67.7-kDa carboxyl-terminal fragment. Proc. Natl. Acad. Sci. U.S.A. 85, 2543-2547
12. Stewart, L., Ireton, G. C., Parker, L. H., Madden, K. R. and Champoux, J. J. (1996) Biochemical and biophysical analyses of recombinant forms of human topoisomerase I. J. Biol. Chem. 271, 7593-7601
13. Mo, Y. Y., Wang, C. and Beck, W. T. (2000) A novel nuclear localization signal in human DNA topoisomerase I. J. Biol. Chem. 275, 41107-41113
14. Redinbo, M. R., Stewart, L., Champoux, J. J. and Hol, W. G. (1999) Structural flexibility in human topoisomerase I revealed in multiple non-isomorphous crystal structures. J. Mol. Biol. 292, 685-696
15. Lesher, D. T., Pommier, Y., Stewart, L. and Redinbo, M. R. (2002) 8-Oxoguanine rearranges the active site of human topoisomerase I. Proc. Natl. Acad. Sci. U.S.A. 99, 12102-12107
16. Lisby, M., Olesen, J. R., Skouboe, C., Krogh, B. O., Straub, T., Boege, F., Velmurugan, S., Martensen, P. M., Andersen, A. H., Jayaram, M., Westergaard, O. and Knudsen, B. R. (2001) Residues within the N-terminal domain of human topoisomerase I play a direct role in relaxation. J. Biol. Chem. 276, 20220-20227
17. Christensen, M. O., Barthelmes, H. U., Boege, F. and Mielke, C. (2003) Residues 190-210 of human topoisomerase I are required for enzyme activity in vivo but not in vitro. Nucleic Acids Res. 31, 7255-7263
18. Alsner, J., Svejstrup, J. Q., Kjeldsen, E., Sorensen, B. S. and Westergaard, O. (1992) Identification of an N-terminal domain of eukaryotic DNA topoisomerase I dispensable for catalytic activity but essential for in vivo function. J. Biol. Chem. 267, 12408-12411
19. Stewart, L., Redinbo, M. R., Qiu, X., Hol, W. G. and Champoux, J. J. (1998) A model for the mechanism of human topoisomerase I. Science 279, 1534-1541
20. Prasad, G. S., Stura, E. A., McRee, D. E., Laco, G. S., Hasselkus-Light, C., Elder, J. H. and Stout, C. D. (1996) Crystal structure of dUTP pyrophosphatase from feline immunodeficiency virus. Protein Sci. 5, 2429-2437
21. Eaton, D., Rodriguez, H. and Vehar, G. A. (1986) Proteolytic processing of human Factor-VIII: correlation of specific cleavages by thrombin, Factor Xa, and activated protein-C with activation and inactivation of Factor-VIII coagulant activity. Biochemistry 25, 505-512
22. Bonven, B. J., Gocke, E. and Westergaard, O. (1985) A high affinity topoisomerase I binding sequence is clustered at DNAase I hypersensitive sites in Tetrahymena R-chromatin. Cell 41, 541-551
23. Staker, B. L., Hjerrild, K., Feese, M. D., Behnke, C. A., Burgin, Jr, A. B. and Stewart, L. (2002) The mechanism of topoisomerase I poisoning by a camptothecin analog, Proc. Natl. Acad. Sci. U.S.A. 99, 15387-15392
24. Laco, G. S., Kent, S. B. and Beachy, R. N. (1995) Analysis of the proteolytic processing and activation of the rice tungro bacilliform virus reverse transcriptase. Virology 208, 207-214
25. Frohlich, R. F., Andersen, F. F., Westergaard, O., Andersen, A. H. and Knudsen, B. R. (2004) Regions within the N-terminal domain of human topoisomerase I exert important functions during strand rotation and DNA binding. J. Mol. Biol. 336, 93-103
26. Tsai, J., Taylor, R., Chothis, C. and Gerstein, M. (1999) The packing density in proteins: standard radii and volumes. J. Mol. Biol. 290, 253-266
27. Frohlich, R. F., Veigaard, C., Andersen, F. F., McClendon, A. K., Gentry, A. C., Andersen, A. H., Osheroff, N., Stevnsner, T. and Knudsen, B. R. (2007) Tryptophan-205 of human topoisomerase I is essential for camptothecin inhibition of negative but not positive supercoil removal. Nucleic Acids Res. 35, 6170-6180
28. Sari, L. and Andricioaei, I. (2005) Rotation of DNA around intact strand in human topoisomerase I implies distinct mechanisms for positive and negative supercoil relaxation. Nucleic Acids Res. 33, 6621-6634
29. Bennion, B. J. and Daggett, V. (2003) The molecular basis for the chemical denaturation of proteins by urea. Proc. Natl. Acad. Sci. U.S.A. 100, 5142-5147
30. Laco, G. S., Fitzgerald, M. C., Morris, G. M., Olson, A. J., Kent, S. B. and Elder, J. H. (1997) Molecular analysis of the feline immunodeficiency virus protease: generation of a novel form of the protease by autoproteolysis and construction of cleavage-resistant proteases. J. Virol. 71, 5505-5511
31. Thrash, C., Bankier, A. T., Barrell, B. G. and Sternglanz, R. (1985) Cloning, characterization, and sequence of the yeast DNA topoisomerase I gene. Proc. Natl. Acad. Sci. U.S.A. 82, 4374-4378
32. Kieber, J. J., Tissier, A. F. and Signer, E. R. (1992) Cloning and characterization of an Arabidopsis thaliana topoisomerase I gene. Plant Physiol. 99, 1493-1501
33. Lima, C. D., Wang, J. C. and Mondragon, A. (1994) Three-dimensional structure of the 67K N-terminal fragment of E. coli DNA topoisomerase I. Nature 367, 138-146
34. Patel, A., Shuman, S. and Mondragon, A. (2006) Crystal structure of a bacterial type IB DNA topoisomerase reveals a preassembled active site in the absence of DNA. J. Biol. Chem. 281, 6030-6037
35. Krogh, B. O. and Shuman, S. (2002) A poxvirus-like type IB topoisomerase family in bacteria. Proc. Natl. Acad. Sci. U.S.A. 99, 1853-1858
36. Vogel, V. (2006) Mechanotransduction involving multimodular proteins: converting force into biochemical signals. Annu. Rev. Biophys. Biomol. Struct. 35, 459-488
37. Craig, D., Krammer, A., Schulten, K. and Vogel, V. (2001) Comparison of the early stages of forced unfolding for fibronectin type III modules. Proc. Natl. Acad. Sci. U.S.A. 98, 5590-5595
38. Krammer, A., Lu, H., Isralewitz, B., Schulten, K. and Vogel, V. (1999) Forced unfolding of the fibronectin type III module reveals a tensile molecular recognition switch. Proc. Natl. Acad. Sci. U.S.A. 96, 1351-1356
39. Cota, E., Hamill, S. J., Fowler, S. B. and Clarke, J. (2000) Two proteins with the same structure respond very differently to mutation: the role of plasticity in protein stability. J. Mol. Biol. 302, 713-725
40. Mo, Y. Y., Wang, P. and Beck, W. T. (2000) Functional expression of human DNA topoisomerase I and its subcellular localization in HeLa cells. Exp. Cell Res. 256, 480-490
41. Mao, Y., Mehl, I. R. and Muller, M. T. (2002) Subnuclear distribution of topoisomerase I is linked to ongoing transcription and p53 status. Proc. Natl. Acad. Sci. U.S.A. 99, 1235-1240
42. Edwards, T. K., Saleem, A., Shaman, J. A., Dennis, T., Gerigk, C., Oliveros, E., Gartenberg, M. R. and Rubin, E. H. (2000) Role for nucleolin/Nsr1 in the cellular localization of topoisomerase I. J. Biol. Chem. 275, 36181-36188
43. Christensen, M. O., Barthelmes, H. U., Boege, F. and Mielke, C. (2002) The N-terminal domain anchors human topoisomerase I at fibrillar centers of nucleoli and nucleolar organizer regions of mitotic chromosomes. J. Biol. Chem. 277, 35932-35938
44. Chillemi, G., Bruselles, A., Fiorani, P., Bueno, S. and Desideri, A. (2007) The open state of human topoisomerase I as probed by molecular dynamics simulation. Nucleic Acids Res. 35, 3032-3038