Diverse substrate recognition and hydrolysis mechanisms of human NUDT5

Nucleic Acids Research

Volumn 39, Issue 20, 2011, Pages 8972-8983

  Arimori, Takao ^a,b   Tamaoki, Haruhiko ^c   Nakamura, Teruya ^a   Kamiya, Hiroyuki ^d   Ikemizu, Shinji ^a   Takagi, Yasumitsu ^e   Ishibashi, Toru ^e   Harashima, Hideyoshi ^f   Sekiguchi, Mutsuo ^e   Yamagata, Yuriko ^a  

^a KUMAMOTO UNIVERSITY   (Japan)

^b JAPAN ATOMIC ENERGY AGENCY   (Japan)

^c KUMAMOTO UNIVERSITY   (Japan)

^d EHIME UNIVERSITY   (Japan)

^e FUKUOKA DENTAL COLLEGE   (Japan)

^f HOKKAIDO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

8 HYDROXYGUANINE; 8 HYDROXYGUANINE ADENOSINE DIPHOSPHATE; 8 HYDROXYGUANINE GUANOSINE DIPHOSPHATE; NUDT5 PROTEIN; PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ENZYME SPECIFICITY; ENZYME SUBSTRATE; ENZYME SUBSTRATE COMPLEX; HUMAN; HYDROLYSIS; ISOTOPE LABELING; MOLECULAR RECOGNITION; NONHUMAN; NUCLEOPHILICITY; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; SEQUENCE ALIGNMENT; STRUCTURE ANALYSIS;

5'-GUANYLIC ACID; ADENOSINE DIPHOSPHATE RIBOSE; BIOCATALYSIS; CRYSTALLOGRAPHY, X-RAY; DEOXYGUANINE NUCLEOTIDES; ESCHERICHIA COLI PROTEINS; HUMANS; HYDROLYSIS; MODELS, MOLECULAR; PROTEIN BINDING; PYROPHOSPHATASES; SUBSTRATE SPECIFICITY;

EID: 80455178769     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr575     Document Type: Article

References (50)

1. Kuchino, Y., Mori, F., Kasai, H., Inoue, H., Iwai, S., Miura, K., Ohtsuka, E. and Nishimura, S. (1987) Misreading of DNA templates containing 8-hydroxydeoxyguanosine at the modified base and at adjacent residues. Nature, 327, 77-79.
2. Moriya, M., Ou, C., Bodepudi, V., Johnson, F., Takeshita, M. and Grollman, A. (1991) Site-specific mutagenesis using a gapped duplex vector: a study of translesion synthesis past 8-oxodeoxyguanosine in E. coli. Mutat. Res., 254, 281-288.
3. Shibutani, S., Takeshita, M. and Grollman, A. (1991) Insertion of specific bases during DNA synthesis past the oxidation-damaged base 8-oxodG. Nature, 349, 431-434.
4. Maki, H. and Sekiguchi, M. (1992) MutT protein specifically hydrolyses a potent mutagenic substrate for DNA synthesis. Nature, 355, 273-275.
5. Satou, K., Kawai, K., Kasai, H., Harashima, H. and Kamiya, H. (2007) Mutagenic effects of 8-hydroxy-dGTP in live mammalian cells. Free Radic. Biol. Med., 42, 1552-1560.
6. Satou, K., Hori, M., Kawai, K., Kasai, H., Harashima, H. and Kamiya, H. (2009) Involvement of specialized DNA polymerases in mutagenesis by 8-hydroxy-dGTP in human cells. DNA Repair, 8, 637-642.
7. Hayakawa, H., Taketomi, A., Sakumi, K., Kuwano, M. and Sekiguchi, M. (1995) Generation and elimination of 8-oxo-7, 8-dihydro-2′-deoxyguanosine 5′-triphosphate, a mutagenic substrate for DNA synthesis, in human cells. Biochemistry, 34, 89-95.
8. Ito, R., Hayakawa, H., Sekiguchi, M. and Ishibashi, T. (2005) Multiple enzyme activities of Escherichia coli MutT protein for sanitization of DNA and RNA precursor pools. Biochemistry, 44, 6670-6674.
9. Taddei, F., Hayakawa, H., Bouton, M., Cirinesi, A., Matic, I., Sekiguchi, M. and Radman, M. (1997) Counteraction by MutT protein of transcriptional errors caused by oxidative damage. Science, 278, 128-130.
10. Nakamura, T., Doi, T., Sekiguchi, M. and Yamagata, Y. (2004) Crystallization and preliminary X-ray analysis of Escherichia coli MutT in binary and ternary complex forms. Acta. Crystallogr. D Biol. Crystallogr., 60, 1641-1643.
11. Nakamura, T., Meshitsuka, S., Kitagawa, S., Abe, N., Yamada, J., Ishino, T., Nakano, H., Tsuzuki, T., Doi, T., Kobayashi, Y. et al. (2010) Structural and dynamic features of the MutT protein in the recognition of nucleotides with the mutagenic 8-oxoguanine base. J. Biol. Chem., 285, 444-452.
12. Fujikawa, K., Kamiya, H., Yakushiji, H., Fujii, Y., Nakabeppu, Y. and Kasai, H. (1999) The oxidized forms of dATP are substrates for the human MutT homologue, the hMTH1 protein. J. Biol. Chem., 274, 18201-18205.
13. Fujikawa, K., Kamiya, H., Yakushiji, H., Nakabeppu, Y. and Kasai, H. (2001) Human MTH1 protein hydrolyzes the oxidized ribonucleotide, 2-hydroxy-ATP. Nucleic Acids Res., 29, 449-454.
14. Mo, J., Maki, H. and Sekiguchi, M. (1992) Hydrolytic elimination of a mutagenic nucleotide, 8-oxodGTP, by human 18-kilodalton protein: sanitization of nucleotide pool. Proc. Natl Acad. Sci. USA, 89, 11021-11025.
15. Ishibashi, T., Hayakawa, H. and Sekiguchi, M. (2003) A novel mechanism for preventing mutations caused by oxidation of guanine nucleotides. EMBO Rep., 4, 479-483.
16. Ishibashi, T., Hayakawa, H., Ito, R., Miyazawa, M., Yamagata, Y. and Sekiguchi, M. (2005) Mammalian enzymes for preventing transcriptional errors caused by oxidative damage. Nucleic Acids Res., 33, 3779-3784.
17. Kamiya, H., Hori, M., Arimori, T., Sekiguchi, M., Yamagata, Y. and Harashima, H. (2009) NUDT5 hydrolyzes oxidized deoxyribonucleoside diphosphates with broad substrate specificity. DNA Repair, 8, 1250-1254.
18. Bialkowski, K. and Kasprzak, K. (1998) A novel assay of 8-oxo- 20-deoxyguanosine 5'-triphosphate pyrophosphohydrolase (8-oxo-dGTPase) activity in cultured cells and its use for evaluation of cadmium(II) inhibition of this activity. Nucleic Acids Res., 26, 3194-3201.
19. Hori, M., Satou, K., Harashima, H. and Kamiya, H. (2010) Suppression of mutagenesis by 8-hydroxy-20-deoxyguanosine 50-triphosphate (7, 8-dihydro-8-oxo-20-deoxyguanosine 50-triphosphate) by human MTH1, MTH2, and NUDT5. Free Radic. Biol. Med., 48, 1197-1201.
20. Hassa, P., Haenni, S., Elser, M. and Hottiger, M. (2006) Nuclear ADP-ribosylation reactions in mammalian cells: where are we today and where are we going? Microbiol. Mol. Biol. Rev., 70, 789-829.
21. Jacobson, E., Cervantes-Laurean, D. and Jacobson, M. (1994) Glycation of proteins by ADP-ribose. Mol. Cell Biochem., 138, 207-212.
22. Gasmi, L., Cartwright, J. and McLennan, A. (1999) Cloning, expression and characterization of YSA1H, a human adenosine 50-diphosphosugar pyrophosphatase possessing a MutT motif. Biochem. J., 344, 331-337.
23. Yang, H., Slupska, M., Wei, Y., Tai, J., Luther, W., Xia, Y., Shih, D., Chiang, J., Baikalov, C., Fitz-Gibbon, S. et al. (2000) Cloning and characterization of a new member of the Nudix hydrolases from human and mouse. J. Biol. Chem., 275, 8844-8853.
24. Zha, M., Zhong, C., Peng, Y., Hu, H. and Ding, J. (2006) Crystal structures of human NUDT5 reveal insights into the structural basis of the substrate specificity. J. Mol. Biol., 364, 1021-1033.
25. Zha, M., Guo, Q., Zhang, Y., Yu, B., Ou, Y., Zhong, C. and Ding, J. (2008) Molecular mechanism of ADP-ribose hydrolysis by human NUDT5 from structural and kinetic studies. J. Mol. Biol., 379, 568-578.
26. Bessman, M., Frick, D. and O'Handley, S. (1996) The MutT proteins or "Nudix" hydrolases, a family of versatile, widely distributed, "housecleaning" enzymes. J. Biol. Chem., 271, 25059-25062.
27. Wang, S., Mura, C., Sawaya, M., Cascio, D. and Eisenberg, D. (2002) Structure of a Nudix protein from Pyrobaculum aerophilum reveals a dimer with two intersubunit beta-sheets. Acta. Crystallogr. D Biol. Crystallogr., 58, 571-578.
28. Coseno, M., Martin, G., Berger, C., Gilmartin, G., Keller, W. and Doublie, S. (2008) Crystal structure of the 25 kDa subunit of human cleavage factor Im. Nucleic Acids Res., 36, 3474-3483.
29. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol., 276, 307-326.
30. Brunger, A., Adams, P., Clore, G., DeLano, W., Gros, P., Grosse- Kunstleve, R., Jiang, J., Kuszewski, J., Nilges, M., Pannu, N. et al. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta. Crystallogr. D Biol. Crystallogr., 54, 905-921.
31. Adams, P., Gopal, K., Grosse-Kunstleve, R., Hung, L., Ioerger, T., McCoy, A., Moriarty, N., Pai, R., Read, R., Romo, T. et al. (2004) Recent developments in the PHENIX software for automated crystallographic structure determination. J. Synchrotron. Radiat., 11, 53-55.
32. Murshudov, G., Vagin, A. and Dodson, E. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta. Crystallogr. D Biol. Crystallogr., 53, 240-255.
33. Storoni, L., McCoy, A. and Read, R. (2004) Likelihood-enhanced fast rotation functions. Acta. Crystallogr. D Biol. Crystallogr., 60, 432-438.
34. Laskowski, R.A., MacArthur, M.W., Moss, D.S. and Thornton, J.M. (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr., 26, 283-291.
35. Kabsch, W. (1976) A solution for the best rotation to relate two sets of vectors. Acta. Crystallogr. A, 32, 922-923.
36. Ooga, T., Yoshiba, S., Nakagawa, N., Kuramitsu, S. and Masui, R. (2005) Molecular mechanism of the Thermus thermophilus ADP-ribose pyrophosphatase from mutational and kinetic studies. Biochemistry, 44, 9320-9329.
37. Doublie, S., Tabor, S., Long, A., Richardson, C. and Ellenberger, T. (1998) Crystal structure of a bacteriophage T7 DNA replication complex at 2.2 A resolution. Nature, 391, 251-258.
38. Gabelli, S., Bianchet, M., Bessman, M. and Amzel, L. (2001) The structure of ADP-ribose pyrophosphatase reveals the structural basis for the versatility of the Nudix family. Nat. Struct. Biol., 8, 467-472.
39. Gabelli, S., Bianchet, M., Ohnishi, Y., Ichikawa, Y., Bessman, M. and Amzel, L. (2002) Mechanism of the Escherichia coli ADP-ribose pyrophosphatase, a Nudix hydrolase. Biochemistry, 41, 9279-9285.
40. Kang, L., Gabelli, S., Cunningham, J., O'Handley, S. and Amzel, L. (2003) Structure and mechanism of MT-ADPRase, a nudix hydrolase from Mycobacterium tuberculosis. Structure, 11, 1015-1023.
41. Wakamatsu, T., Nakagawa, N., Kuramitsu, S. and Masui, R. (2008) Structural basis for different substrate specificities of two ADP-ribose pyrophosphatases from Thermus thermophilus HB8. J. Bacteriol., 190, 1108-1117.
42. Yoshiba, S., Ooga, T., Nakagawa, N., Shibata, T., Inoue, Y., Yokoyama, S., Kuramitsu, S. and Masui, R. (2004) Structural insights into the Thermus thermophilus ADP-ribose pyrophosphatase mechanism via crystal structures with the bound substrate and metal. J. Biol. Chem., 279, 37163-37174.
43. Cohn, M. and Hu, A. (1978) Isotopic (18O) shift in 31P nuclear magnetic resonance applied to a study of enzyme-catalyzed phosphate-phosphate exchange and phosphate (oxygen)-water exchange reactions. Proc. Natl Acad. Sci. USA, 75, 200-203.
44. Weber, D., Bhatnagar, S., Bullions, L., Bessman, M. and Mildvan, A. (1992) NMR and isotopic exchange studies of the site of bond cleavage in the MutT reaction. J. Biol. Chem., 267, 16939-16942.
45. Mishima, M., Sakai, Y., Itoh, N., Kamiya, H., Furuichi, M., Takahashi, M., Yamagata, Y., Iwai, S., Nakabeppu, Y. and Shirakawa, M. (2004) Structure of human MTH1, a Nudix family hydrolase that selectively degrades oxidized purine nucleoside triphosphates. J. Biol. Chem., 279, 33806-33815.
46. Ito, R., Sekiguchi, M., Setoyama, D., Nakatsu, Y., Yamagata, Y. and Hayakawa, H. (2011) Cleavage of oxidized guanine nucleotide and ADP-ribose by human NUDT5 protein. J. Biochem., 149, 731-738.
47. Uesugi, S. and Ikehara, M. (1977) Carbon-13 magnetic resonance spectra of 8-substituted purine nucleosides. Characteristic shifts for the syn conformation. J. Am. Chem. Soc., 99, 3250-3253.
48. Fromme, J., Banerjee, A., Huang, S. and Verdine, G. (2004) Structural basis for removal of adenine mispaired with 8-oxoguanine by MutY adenine DNA glycosylase. Nature, 427, 652-656.
49. Thompson, J., Higgins, D. and Gibson, T. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res., 22, 4673-4680.
50. Kawabata, T. (2003) MATRAS: a program for protein 3D structure comparison. Nucleic Acids Res., 31, 3367-3369.