The RNase H-like superfamily: New members, comparative structural analysis and evolutionary classification

Nucleic Acids Research

Volumn 42, Issue 7, 2014, Pages 4160-4179

  Majorek, Karolina A ^a,b,c   Dunin Horkawicz, Stanislaw ^a   Steczkiewicz, Kamil ^d   Muszewska, Anna ^d,e   Nowotny, Marcin ^a   Ginalski, Krzysztof ^d   Bujnicki, Janusz M ^a,c  

^a INTERNATIONAL INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Poland)

^b UNIVERSITY OF VIRGINIA   (United States)

^c ADAM MICKIEWICZ UNIVERSITY   (Poland)

^d UNIVERSITY OF WARSAW   (Poland)

^e INSTITUTE OF BIOCHEMISTRY AND BIOPHYSICS   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; ENDONUCLEASE; EXONUCLEASE; INTEGRASE; RIBONUCLEASE H; RIBONUCLEASE H LIKE SUPERFAMILY; TRANSPOSASE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CLUSTER ANALYSIS; COMPARATIVE STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME STRUCTURE; FAMILY; MOLECULAR EVOLUTION; PHYLOGENY; PRIORITY JOURNAL; PROTEIN DATABASE; PROTEIN FOLDING; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; STRUCTURE ACTIVITY RELATION;

CLUSTER ANALYSIS; EVOLUTION, MOLECULAR; EXONUCLEASES; PHYLOGENY; PROTEIN STRUCTURE, TERTIARY; RIBONUCLEASE H; SEQUENCE ALIGNMENT;

EID: 84899011562     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt1414     Document Type: Article

References (59)

1. Katayanagi, K., Miyagawa, M., Matsushima, M., Ishikawa, M., Kanaya, S., Ikehara, M., Matsuzaki, T. and Morikawa, K. (1990) Three-dimensional structure of ribonuclease H from E coli. Nature, 347, 306-309.
2. Yang, W., Hendrickson, W.A., Crouch, R.J. and Satow, Y. (1990) Structure of ribonuclease H phased at 2 A resolution by MAD analysis of the selenomethionyl protein. Science, 249, 1398-1405.
3. Rice, P.A. and Baker, T.A. (2001) Comparative architecture of transposase and integrase complexes. Nat. Struct. Biol., 8, 302-307. (Pubitemid 32275012)
4. Ariyoshi, M., Vassylyev, D.G., Iwasaki, H., Nakamura, H., Shinagawa, H. and Morikawa, K. (1994) Atomic structure of the RuvC resolvase: a holliday junction-specific endonuclease from E coli. Cell, 78, 1063-1072. (Pubitemid 24292333)
5. Parker, J.S., Roe, S.M. and Barford, D. (2004) Crystal structure of a PIWI protein suggests mechanisms for siRNA recognition and slicer activity. EMBO J., 23, 4727-4737. (Pubitemid 40069703)
6. Song, J.J., Smith, S.K., Hannon, G.J. and Joshua-Tor, L. (2004) Crystal structure of Argonaute and its implications for RISC slicer activity. Science, 305, 1434-1437. (Pubitemid 39167656)
7. Zuo, Y. and Deutscher, M.P. (2001) Exoribonuclease superfamilies: structural analysis and phylogenetic distribution. Nucleic Acids Res., 29, 1017-1026. (Pubitemid 32186186)
8. Pena, V., Rozov, A., Fabrizio, P., Luhrmann, R. and Wahl, M. (2008) Structure and function of an RNase H domain at the heart of the spliceosome. EMBO J., 27, 2929-2940.
9. Ma, B.G., Chen, L., Ji, H.F., Chen, Z.H., Yang, F.R., Wang, L., Qu, G., Jiang, Y.Y., Ji, C. and Zhang, H.Y. (2008) Characters of very ancient proteins. Biochem. Biophys. Res. Commun., 366, 607-611.
10. Davies, J.F.n., Hostomska, Z., Hostomsky, Z., Jordan, S.R. and Matthews, D.A. (1991) Crystal structure of the ribonuclease H domain of HIV-1 reverse transcriptase. Science, 252, 88-95. (Pubitemid 21916941)
11. Yang, W., Lee, J.Y. and Nowotny, M. (2006) Making and breaking nucleic acids: two-Mg2+-ion catalysis and substrate specificity. Mol. Cell, 22, 5-13.
12. Maertens, G.N., Hare, S. and Cherepanov, P. (2010) The mechanism of retroviral integration from X-ray structures of its key intermediates. Nature, 468, 326-329.
13. Cherepanov, P., Maertens, G.N. and Hare, S. (2011) Structural insights into the retroviral DNA integration apparatus. Curr. Opin. Struct. Biol., 21, 249-256.
14. Nowotny, M. and Yang, W. (2006) Stepwise analyses of metal ions in RNase H catalysis from substrate destabilization to product release. EMBO J., 25, 1924-1933.
15. Andreeva, A., Howorth, D., Brenner, S.E., Hubbard, T.J., Chothia, C. and Murzin, A.G. (2004) SCOP database in 2004: refinements integrate structure and sequence family data. Nucleic Acids Res., 32, D226-D229. (Pubitemid 38081644)
16. Holm, L. and Sander, C. (1995) Dali: a network tool for protein structure comparison. Trends.Biochem. Sci., 20, 478-480.
17. Frickey, T. and Lupas, A. (2004) CLANS: a Java application for visualizing protein families based on pairwise similarity. Bioinformatics, 20, 3702-3704. (Pubitemid 40136822)
18. Tatusov, R.L., Fedorova, N.D., Jackson, J.D., Jacobs, A.R., Kiryutin, B., Koonin, E.V., Krylov, D.M., Mazumder, R., Mekhedov, S.L., Nikolskaya, A.N. et al. (2003) The COG database: an updated version includes eukaryotes. BMC Bioinformatics, 4, 41.
19. Bateman, A., Coin, L., Durbin, R., Finn, R.D., Hollich, V., Griffiths-Jones, S., Khanna, A., Marshall, M., Moxon, S., Sonnhammer, E.L. et al. (2004) The Pfam protein families database. Nucleic Acids Res., 32, D138-D141. (Pubitemid 38081623)
20. Soding, J., Biegert, A. and Lupas, A.N. (2005) The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res., 33, W244-W248. (Pubitemid 44529917)
21. Soding, J. (2005) Protein homology detection by HMM-HMM comparison. Bioinformatics, 21, 951-960. (Pubitemid 40467915)
22. Ginalski, K., von Grotthuss, M., Grishin, N.V. and Rychlewski, L. (2004) Detecting distant homology with Meta-BASIC. Nucleic Acids Res., 32, W576-W581. (Pubitemid 38997401)
23. Ginalski, K., Elofsson, A., Fischer, D. and Rychlewski, L. (2003) 3D-Jury: a simple approach to improve protein structure predictions. Bioinformatics, 19, 1015-1018. (Pubitemid 36675823)
24. Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res., 32, 1792-1797. (Pubitemid 38832724)
25. Li, W., Jaroszewski, L. and Godzik, A. (2001) Clustering of highly homologous sequences to reduce the size of large protein databases. Bioinformatics, 17, 282-283. (Pubitemid 32288218)
26. Guex, N. and Peitsch, M.C. (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis, 18, 2714-2723. (Pubitemid 28059943)
27. Kurowski, M.A. and Bujnicki, J.M. (2003) GeneSilico protein structure prediction meta-server. Nucleic Acids Res., 31, 3305-3307. (Pubitemid 37442145)
28. Holm, L. and Park, J. (2000) DaliLite workbench for protein structure comparison. Bioinformatics, 16, 566-567.
29. Wagner, R.A. and Lowrance, R. (1975) An extension of the string-to-string correction problem. J. ACM, 22, 177-183.
30. van Dongen, S. (2000) Graph clustering by flow simulation. Ph.D thesis. University of Utrecht.
31. Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Hohna, S., Larget, B., Liu, L., Suchard, M.A. and Huelsenbeck, J.P. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol., 61, 539-542.
32. Tkaczuk, K.L., Dunin-Horkawicz, S., Purta, E. and Bujnicki, J.M. (2007) Structural and evolutionary bioinformatics of the SPOUT superfamily of methyltransferases. BMC Bioinformatics, 8, 73.
33. Kuchta, K., Knizewski, L., Wyrwicz, L.S., Rychlewski, L. and Ginalski, K. (2009) Comprehensive classification of nucleotidyltransferase fold proteins: identification of novel families and their representatives in human. Nucleic Acids Res., 37, 7701-7714.
34. Steczkiewicz, K., Muszewska, A., Knizewski, L., Rychlewski, L. and Ginalski, K. (2012) Sequence, structure and functional diversity of PD-(D/E)XK phosphodiesterase superfamily. Nucleic Acids Res., 40, 7016-7045.
35. Yuan, Y.W. and Wessler, S.R. (2011) The catalytic domain of all eukaryotic cut-and-paste transposase superfamilies. Proc. Natl Acad. Sci. USA, 108, 7884-7889.
36. Rawlings, N.D., Barrett, A.J. and Bateman, A. (2012) MEROPS: the database of proteolytic enzymes, their substrates and inhibitors. Nucleic Acids Res., 40, D343-D350.
37. Feiss, M. and Rao, V.B. (2012) The bacteriophage DNA packaging machine. Adv. Exp. Med. Biol., 726, 489-509.
38. Capy, P., Langin, T., Higuet, D., Maurer, P. and Bazin, C. (1997) Do the integrases of LTR-retrotransposons and class II element transposases have a common ancestor? Genetica, 100, 63-72. (Pubitemid 28034753)
39. Iwahara, J., Kigawa, T., Kitagawa, K., Masumoto, H., Okazaki, T. and Yokoyama, S. (1998) A helix-turn-helix structure unit in human centromere protein B (CENP-B). EMBO J., 17, 827-837. (Pubitemid 28062061)
40. Knizewski, L. and Ginalski, K. (2005) Bacillus subtilis YkuK protein is distantly related to RNase H. FEMS Microbiol. Lett., 251, 341-346. (Pubitemid 41383888)
41. Cheng, Y. and Patel, D.J. (2004) Crystallographic structure of the nuclease domain of 3′hExo, a DEDDh family member, bound to rAMP. J. Mol. Biol., 343, 305-312. (Pubitemid 39296868)
42. Hsiao, Y.Y., Yang, C.C., Lin, C.L., Lin, J.L., Duh, Y. and Yuan, H.S. (2011) Structural basis for RNA trimming by RNase T in stable RNA 3′-end maturation. Nat. Chem. Biol., 7, 236-243.
43. Constantinesco, F., Forterre, P. and Elie, C. (2002) NurA, a novel 5′-3′ nuclease gene linked to rad50 and mre11 homologs of thermophilic Archaea. EMBO Rep., 3, 537-542. (Pubitemid 34752454)
44. Kamtekar, S., Berman, A.J., Wang, J., Lazaro, J.M., de Vega, M., Blanco, L., Salas, M. and Steitz, T.A. (2004) Insights into strand displacement and processivity from the crystal structure of the protein-primed DNA polymerase of bacteriophage phi29. Mol. Cell, 16, 609-618. (Pubitemid 39531883)
45. Liu, J., Carmell, M.A., Rivas, F.V., Marsden, C.G., Thomson, J.M., Song, J.J., Hammond, S.M., Joshua-Tor, L. and Hannon, G.J. (2004) Argonaute2 is the catalytic engine of mammalian RNAi. Science, 305, 1437-1441. (Pubitemid 39167657)
46. Rivas, F.V., Tolia, N.H., Song, J.J., Aragon, J.P., Liu, J., Hannon, G.J. and Joshua-Tor, L. (2005) Purified Argonaute2 and an siRNA form recombinant human RISC. Nat. Struct. Mol. Biol., 12, 340-349. (Pubitemid 43093089)
47. Elkayam, E., Kuhn, C.D., Tocilj, A., Haase, A.D., Greene, E.M., Hannon, G.J. and Joshua-Tor, L. (2012) The structure of human argonaute-2 in complex with miR-20a. Cell, 150, 100-110.
48. Aravind, L., Makarova, K.S. and Koonin, E.V. (2000) Holliday junction resolvases and related nucleases: identification of new families, phyletic distribution and evolutionary trajectories. Nucleic Acids Res., 28, 3417-3432.
49. Badger, J., Sauder, J.M., Adams, J.M., Antonysamy, S., Bain, K., Bergseid, M.G., Buchanan, S.G., Buchanan, M.D., Batiyenko, Y., Christopher, J.A. et al. (2005) Structural analysis of a set of proteins resulting from a bacterial genomics project. Proteins, 60, 787-796. (Pubitemid 41266436)
50. Johnson, S.J., Close, D., Robinson, H., Vallet-Gely, I., Dove, S.L. and Hill, C.P. (2008) Crystal structure and RNA binding of the Tex protein from Pseudomonas aeruginosa. J. Mol. Biol., 377, 1460-1473.
51. Iwamoto, A., Osawa, A., Kawai, M., Honda, H., Yoshida, S., Furuya, N. and Kato, J. (2012) Mutations in the essential Escherichia coli gene, yqgF, and their effects on transcription. J. Mol. Microbiol. Biotechnol., 22, 17-23.
52. Barnes, M.H., Spacciapoli, P., Li, D.H. and Brown, N.C. (1995) The 3′-5′ exonuclease site of DNA polymerase III from gram-positive bacteria: definition of a novel motif structure. Gene, 165, 45-50.
53. Zuo, Y. and Deutscher, M.P. (2002) Mechanism of action of RNase T.I. Identification of residues required for catalysis, substrate binding, and dimerization. J. Biol. Chem., 277, 50155-50159. (Pubitemid 36014469)
54. Zuo, Y., Zheng, H., Wang, Y., Chruszcz, M., Cymborowski, M., Skarina, T., Savchenko, A., Malhotra, A. and Minor, W. (2007) Crystal structure of RNase T, an exoribonuclease involved in tRNA maturation and end turnover. Structure, 15, 417-428. (Pubitemid 46551724)
55. Horio, T., Murai, M., Inoue, T., Hamasaki, T., Tanaka, T. and Ohgi, T. (2004) Crystal structure of human ISG20, an interferon-induced antiviral ribonuclease. FEBS Lett., 577, 111-116. (Pubitemid 39452369)
56. Su, J., Li, Y., Shaw, N., Zhou, W., Zhang, M., Xu, H., Wang, B.C. and Liu, Z.J. (2010) Crystal structure of a novel non-Pfam protein PF2046 solved using low resolution B-factor sharpening and multi-crystal averaging methods. Protein Cell, 1, 453-458.
57. Malik, H.S. (2005) Ribonuclease H evolution in retrotransposable elements. Cytogenet. Genome Res., 110, 392-401. (Pubitemid 41159916)
58. Majumdar, S., Singh, A. and Rio, D.C. (2013) The human THAP9 gene encodes an active P-element DNA transposase. Science, 339, 446-448.
59. Dunin-Horkawicz, S., Feder, M. and Bujnicki, J.M. (2006) Phylogenomic analysis of the GIY-YIG nuclease superfamily. BMC Genomics, 7, 98.