Crystal structure of metagenome-derived LC11-RNase H1 in complex with RNA/DNA hybrid

Journal of Structural Biology

Volumn 182, Issue 2, 2013, Pages 144-154

  Nguyen, Tri Nhan ^a   You, Dong Ju ^a,b   Matsumoto, Hiroyuki ^a   Kanaya, Eiko ^a   Koga, Yuichi ^a   Kanaya, Shigenori ^a  

^a OSAKA UNIVERSITY   (Japan)

^b Korea Basic Science Institute (KBSI)   (South Korea)

Author keywords

Crystal structure; DNA binding site; Enzyme substrate complex; RNA DNA hybrid; RNase H1

Indexed keywords

DNA; DOUBLE STRANDED RNA; HYBRID PROTEIN; LC11 RNASE H1 PROTEIN; PHOSPHATE; RIBONUCLEASE; RNA; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS; BACILLUS HALODURANS; BINDING SITE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA BINDING; DNA RNA HYBRIDIZATION; ENZYME ACTIVE SITE; ENZYME LOCALIZATION; ENZYME SUBSTRATE COMPLEX; GENE MUTATION; METAGENOME; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN STRUCTURE; SULFOLOBUS TOKODAII; X RAY DIFFRACTION;

CRYSTALLIZATION; DNA, ARCHAEAL; METAGENOME; MODELS, MOLECULAR; PLASMIDS; PROTEIN CONFORMATION; RIBONUCLEASE H; RNA, ARCHAEAL; SULFOLOBUS; X-RAY DIFFRACTION;

BACILLUS HALODURANS; SULFOLOBUS TOKODAII;

EID: 84876718351     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2013.02.018     Document Type: Article

References (39)

1. Arudchandran A., Cerritelli S., Narimatsu S., Itaya M., Shin D.Y., et al. The absence of ribonuclease H1 or H2 alters the sensitivity of Saccharomyces cerevisiae to hydroxyurea, caffeine and ethyl methanesulphonate: implications for roles of RNases H in DNA replication and repair. Genes Cells 2000, 5:789-802.
2. Cerritelli S.M., Crouch R.J. Ribonuclase H: the enzymes in eukaryotes. FEBS J. 2009, 276:1494-1505.
3. Cerritelli S.M., Frolova E.G., Feng C., Grinberg A., Love P.E., et al. Failure to produce mitochondrial DNA results in embryonic lethality in Rnaseh1 null mice. Mol. Cell 2003, 11:807-815.
4. Crouch R.J., Dirksen M.-L. Ribonucleases H. Nuclease 1982, 211-241. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. S.M. Linn, R.J. Roberts (Eds.).
5. Crow Y.J., Leitch A., Hayward B.E., Garner A., Parmar R., et al. Mutations in genes encoding ribonuclease H2 subunits cause Aicardi-Goutieres syndrome and mimic congenital viral brain infection. Nat. Genet. 2006, 38:910-916.
6. Emsley P., Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 2004, 60:2126-2132.
7. Haruki M., Noguchi E., Kanaya S., Crouch R.J. Kinetic and stoichiometric analysis for the binding of Escherichia coli ribonuclease HI to RNA-DNA hybrids using surface plasmon resonance. J. Biol. Chem. 1997, 272:22015-22022.
8. Haruki M., Tsunaka Y., Morikawa M., Kanaya S. Cleavage of a DNA-RNA-DNA/DNA chimeric substrate containing a single ribonucleotide at the DNA-RNA junction with prokaryotic RNases HII. FEBS Lett. 2002, 531:204-208.
9. Itaya M., Omori A., Kanaya S., Crouch R.J., Tanaka T., et al. Isolation of RNase H genes that are essential for growth of Bacillus subtilis 168. J. Bacteriol. 1999, 181:2118-2123.
10. 2+-dependent activity. FEBS J. 2010, 277:4474-4489.
11. Kanaya S., Kohara A., Miura Y., Sekiguchi A., Iwai S., et al. Identification of the amino acid residues involved in an active site of Escherichia coli ribonuclease H by site-directed mutagenesis. J. Biol. Chem. 1990, 265:4615-4621.
12. Kanaya E., Sakabe T., Nguyen N.T., Koikeda S., Koga Y., et al. Cloning of the RNase H genes from a metagenomic DNA library: identification of a new type 1 RNase H without a typical active-site motif. J. Appl. Microbiol. 2010, 109:974-983.
13. Kogoma T., Foster P.L. Physiological functions of E. coli RNase HI. Ribonucleases H 1998, 39-66. INSERM, Paris. R.J. Crouch, J.J. Toulme (Eds.).
14. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T. Nature 1970, 227:680-685.
15. Langer G., Cohen S.X., Lamzin V.S., Perrakis A. Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7. Nat. Protoc. 2008, 3:1171-1179.
16. Lazzaro F., Novarina D., Amara F., Watt D.L., Stone J.E., et al. RNase H and postreplication repair protect cells from ribonucleotides incorporated in DNA. Mol. Cell 2012, 45:99-110.
17. Lima W.F., Wu H., Nichols J.G., Prakash T.P., Ravikumer V., et al. Human RNase H1 uses one tryptophan and two lysines to position the enzyme at the 3'-DNA/5'-RNA terminus of the heteroduplex substrate. J. Biol. Chem. 2003, 278:49860-49867.
18. Murshudov G.N., Vagin A.A., Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 1997, 53:240-255.
19. Nguyen T.N., Angkawidjaja C., Kanaya E., Koga Y., Takano K., et al. Activity, stability, and structure of metagenome-derived LC11-RNase H1, a homolog of Sulfolobus tokodaii RNase H1. Protein Sci. 2012, 21:553-561.
20. Nowotny M., Yang W. Stepwise analyses of metal ions in RNase H catalysis from substrate destabilization to product release. EMBO J. 2006, 25:1924-1933.
21. Nowotny M., Gaidamakov S.A., Crouch R.J., Yang W. Crystal structures of RNase H bound to an RNA/DNA hybrid: substrate specificity and metal-dependent catalysis. Cell 2005, 121:1005-1016.
22. Nowotny M., Gaidamakov S.A., Ghirlando R., Cerritelli S.M., Crouch R.J., et al. Structure of human RNase H1 complexed with an RNA/DNA hybrid: insight into HIV reverse transcription. Mol. Cell 2007, 28:264-276.
23. Nowotny M., Cerritelli S.M., Ghirlando R., Gaidamakov S.A., Crouch R.J., et al. Specific recognition of RNA/DNA hybrid and enhancement of human RNase H1 activity by HBD. EMBO J. 2008, 27:1172-1181.
24. Oda Y., Yoshida M., Kanaya S. Role of histidine 124 in the catalytic function of ribonuclease HI from Escherichia coli. J. Biol. Chem. 1993, 268:88-92.
25. Ohtani N., Haruki M., Morikawa M., Kanaya S. Molecular diversities of RNases H. J. Biosci. Bioeng. 1999, 88:12-19.
26. 2+-dependent RNase HIII from Bacillus subtilis: classification of RNases H into three families. Biochemistry 1999, 38:605-618.
27. Ohtani N., Haruki M., Muroya A., Morikawa M., Kanaya S. Characterization of ribonuclease HII from Escherichia coli overproduced in a soluble form. J. Biochem. 2000, 127:895-899.
28. Ohtani N., Yanagawa H., Tomita M., Itaya M. Cleavage of double-stranded RNA by RNase HI from a thermoacidophilic archaeon, Sulfolobus tokodaii 7. Nucleic Acids Res. 2004, 32:5809-5819.
29. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Macromol. Crystallogr. Part A 1997, 276:307-326.
30. Qiu J.Z., Qian Y., Frank P., Wintersberger U., Shen B.H. Saccharomyces cerevisiae RNase H(35) functions in RNA primer removal during lagging-strand DNA synthesis, most efficiently in cooperation with Rad27 nuclease. Mol. Cell Biol. 1999, 19:8361-8371.
31. Rychlik M.P., Chon H., Cerritelli S.M., Klimek P., Crouch R.J., et al. Crystal structures of RNase H2 in complex with nucleic acid reveal the mechanism of RNA-DNA junction recognition and cleavage. Mol. Cell 2010, 40:658-670.
32. Sparks J.L., Chon H., Cerritelli S.M., Kunkel T.A., Johansson E., et al. RNase H2-initiated ribonucleotide excision repair. Mol. Cell 2012, 47:980-986.
33. Tadokoro T., Kanaya S. Ribonuclease H: molecular diversities, substrate binding domains, and catalytic mechanism of the prokaryotic enzymes. FEBS J. 2009, 276:1482-1493.
34. Tramontano E., Di Santo R. HIV-1 RT-associated RNase H function inhibitors: recent advances in drug development. Curr. Med. Chem. 2010, 17:2837-2853.
35. 2+-dependent activity of E. coli ribonuclease HI. Biochemistry 2003, 42:3366-3374.
36. Vagin A., Teplyakov A. An approach to multi-copy search in molecular replacement. Acta Crystallogr. D Biol. Crystallogr. 2000, 56:1622-1624.
37. 2+-ion catalysis and substrate specificity. Mol. Cell 2006, 22:5-13.
38. You D.-J., Chon H., Koga Y., Takano K., Kanaya S. Crystallization and preliminary crystallographic analysis of type 1 RNase H from the hyperthermophilic archaeon Sulfolobus tokodaii 7. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 2006, 62:781-784.
39. You D.-J., Chon H., Koga Y., Takano K., Kanaya S. Crystal structure of type 1 Ribonuclease H from hyperthermophilic archaeon Sulfolobus tokodaii: role of Arg118 and C-terminal anchoring. Biochemistry 2007, 46:11494-11503.