Unique subunit packing in mycobacterial nanoRNase leads to alternate substrate recognitions in DHH phosphodiesterases

Nucleic Acids Research

Volumn 42, Issue 12, 2014, Pages 7894-7910

  Srivastav, Rajpal ^a   Kumar, Dilip ^a   Grover, Amit ^a,c   Singh, Ajit ^a   Manjasetty, Babu A ^b   Sharma, Rakesh ^a   Taneja, Bhupesh ^a  

^a CSIR INSTITUTE OF GENOMICS AND INTEGRATIVE BIOLOGY   (India)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (France)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE; DHH PHOSPHODIESTERASE; DNA; NANORIBONUCLEASE; PHOSPHATASE; PHOSPHODIESTERASE; PHOSPHODIESTERASE I; RIBONUCLEASE; RNA; SINGLE STRANDED DNA; SPLEEN EXONUCLEASE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CLUSTER ANALYSIS; CONTROLLED STUDY; DNA DAMAGE; ENZYME ACTIVITY; ENZYME SUBSTRATE; GENE CLUSTER; GROWTH DISORDER; IN VITRO STUDY; IN VIVO STUDY; MICROBIAL GENOME; MOLECULAR RECOGNITION; MYCOBACTERIUM SMEGMATIS; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROTEIN QUATERNARY STRUCTURE; STRESS; TRANSCRIPTION INITIATION; TRANSLATION INITIATION;

BACTERIAL PROTEINS; CATALYTIC DOMAIN; EXONUCLEASES; MODELS, MOLECULAR; MUTATION; MYCOBACTERIUM SMEGMATIS; OPERON; PHOSPHORIC DIESTER HYDROLASES; PHOSPHORIC MONOESTER HYDROLASES; PHYLOGENY; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; RIBONUCLEASES; SEQUENCE ALIGNMENT;

EID: 84903979422     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku425     Document Type: Article

References (48)

1. Nickels, B.E., Dove, S.L. (2011) NanoRNAs: a class of small RNAs that can prime transcription initiation in bacteria. J. Mol. Biol., 412, 772-781.
2. Vvedenskaya, I.O., Sharp, J.S., Goldman, S.R., Kanabar, P.N., Livny, J., Dove, S.L., Nickels, B.E. (2012) Growth phase-dependent control of transcription start site selection and gene expression by nanoRNAs. Genes Dev., 26, 1498-1507.
3. Goldman, S.R., Sharp, J.S., Vvedenskaya, I.O., Livny, J., Dove, S.L., Nickels, B.E. (2011) NanoRNAs prime transcription initiation in vivo. Mol. Cell, 42, 817-825.
4. Zhang, X., Zhu, L., Deutscher, M.P. (1998) Oligoribonuclease is encoded by a highly conserved gene in the 3'-5' exonuclease superfamily. J. Bacteriol., 180, 2779-2781.
5. Mechold, U., Fang, G., Ngo, S., Ogryzko, V., Danchin, A. (2007) YtqI from Bacillus subtilis has both oligoribonuclease and pAp-phosphatase activity. Nucleic Acids Res., 35, 4552-4561.
6. Fang, M., Zeisberg, W.M., Condon, C., Ogryzko, V., Danchin, A., Mechold, U. (2009) Degradation of nanoRNA is performed by multiple redundant RNases in Bacillus subtilis. Nucleic Acids Res., 37, 5114-5125.
7. Liu, M.F., Cescau, S., Mechold, U., Wang, J., Cohen, D., Danchin, A., Boulouis, H.J., Biville, F. (2012) Identification of a novel nanoRNase in Bartonella. Microbiology, 158, 886-895.
8. Uemura, Y., Nakagawa, N., Wakamatsu, T., Kim, K., Montelione, G.T., Hunt, J.F., Kuramitsu, S., Masui, R. (2013) Crystal structure of the ligand-binding form of nanoRNase from Bacteroides fragilis, a member of the DHH/DHHA1 phosphoesterase family of proteins. FEBS Lett., 587, 2669-2674.
9. Chin, K.H., Yang, C.Y., Chou, C.C., Wang, A.H., Chou, S.H. (2006) The crystal structure of XC847 from Xanthomonas campestris: a 3'-5' oligoribonuclease of DnaQ fold family with a novel opposingly shifted helix. Proteins, 65, 1036-1040.
10. Postic, G., Danchin, A., Mechold, U. (2012) Characterization of NrnA homologs from Mycobacterium tuberculosis and Mycoplasma pneumoniae. RNA, 18, 155-165.
11. Kumar, A., Saigal, K., Malhotra, K., Sinha, K.M., Taneja, B. (2011) Structural and functional characterization of Rv2966c protein reveals an RsmD-like methyltransferase from Mycobacterium tuberculosis and the role of its N-terminal domain in target recognition. J. Biol. Chem., 286, 19652-19661.
12. Evans, G., Pettifer, R.F. (2001) CHOOCH: a program for deriving anomalous-scattering factors from X-ray fluorescence spectra. J. Appl. Cryst., 34, 82-86.
13. Leslie, A.G.W., Powell, H.R. (2007) Processing diffraction data with mosflm. In: Read, R.J., Sussman, J.L. (eds). Evolving Methods for Macromolecular Crystallography. Springer, Netherlands, Vol. 245, pp. 41-51.
14. Diederichs, K., Karplus, P. A. (1997) Improved R-factors for diffraction data analysis in macromolecular crystallography. Nat Struct. Biol., 4, 269-275.
15. Potterton, E., Briggs, P., Turkenburg, M., Dodson, E. (2003) A graphical user interface to the CCP4 program suite. Acta Cryst., D67, 1131-1137.
16. Winn, M.D., Ballard, C.C., Cowtan, K.D., Dodson, E.J., Emsley, P., Evans, P.R., Keegan, R.M., Krissinel, E.B., Leslie, A.G.W., McCoy, A. et al. (2011) Overview of the CCP4 suite and current developments. Acta Cryst., D67, 235-242.
17. Panjikar, S., Parthasarathy, V., Lamzin, V.S., Weiss, M.S., Tucker, P.A. (2009) On the combination of molecular replacement and single-wavelength anomalous diffraction phasing for automated structure determination. Acta Cryst., D65, 1089-1097.
18. Emsley, P., Lohkamp, B., Scott, W.G., Cowtan, K. (2010) Features and development of Coot. Acta Cryst., D66, 486-501.
19. Murshudov, G.N., Skubak, P., Lebedev, A.A., Pannu, N.S., Steiner, R.A., Nicholls, R. A., Winn, M. D., Long, F., Vagin, A.A. (2011) REFMAC5 for the refinement of macromolecular crystal structures. Acta Cryst., D67, 355-367.
20. Bricogne, G., Blanc, E., Brandl, M., Flensburg, C., Keller, P., Paciorek, W., Roversi, P., Sharff, A., Smart, O.S., Vonrhein, C. et al. (2011) BUSTER 2.10.0. Global Phasing Ltd, Cambridge.
21. Painter, J., Merritt, E.A. (2006) Optimal description of a protein structure in terms of multiple groups undergoing TLS motion. Acta Cryst., D62, 439-450.
22. Grover, A., Sharma, R. (2006) Identification and characterization of a major Zn(II) resistance determinant of Mycobacterium smegmatis. J. Bacteriol., 188, 7026-7032.
23. Gaora, P.O., Barnini, S., Hayward, C., Filley, E., Rook, G., Young, D., Thole, J. (1997) Mycobacteria as immunogens: development of expression vectors for use in multiple mycobacterial species. Med. Princ. Pract., 6, 91-96.
24. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol., 28, 2731-2739.
25. Mishra, M.N., Daniels, L. (2013) Characterization of the MSMEG 2631 gene (mmp) encoding a multidrug and toxic compound extrusion (MATE) family protein in Mycobacterium smegmatis and exploration of its polyspecific nature using biolog phenotype microarray. J. Bacteriol., 195, 1610-1621.
26. Sassetti, C.M., Boyd, D.H., Rubin, E.J. (2003) Genes required for mycobacterial growth defined by high density mutagenesis. Mol. Microbiol., 48, 77-84.
27. Griffin, J.E., Gawronski, J.D., Dejesus, M.A., Ioerger, T.R., Akerley, B.J., Sassetti, C.M. (2011) High-resolution phenotypic profiling defines genes essential for mycobacterial growth and cholesterol catabolism. PLoS Pathog., 7, e1002251.
28. Cox, J.D., Kim, N.N., Traish, A.M., Christianson, D.W. (1999) Arginase-boronic acid complex highlights a physiological role in erectile function.Nat. Struct. Biol., 6, 1043-1047.
29. Voegtli, W.C., White, D.J., Reiter, N.J., Rusnak, F., Rosenzweig, A.C. (2000) Structure of the bacteriophage lambda Ser/Thr protein phosphatase with sulfate ion bound in two coordination modes. Biochemistry, 39, 15365-15374.
30. Wakamatsu, T., Kitamura, Y., Kotera, Y., Nakagawa, N., Kuramitsu, S., Masui, R. (2010) Structure of RecJ exonuclease defines its specificity for single-stranded DNA. J. Biol. Chem., 285, 9762-9769.
31. Ahn, S., Milner, A.J., Futterer, K., Konopka, M., Ilias, M., Young, T.W., White, S.A. (2001) The "open" and "closed" structures of the type-C inorganic pyrophosphatases from Bacillus subtilis and Streptococcus gordonii. J. Mol. Biol., 313, 797-811.
32. Merckel, M.C., Fabrichniy, I.P., Salminen, A., Kalkkinen, N., Baykov, A.A., Lahti, R., Goldman, A. (2001) Crystal structure of Streptococcus mutans pyrophosphatase: a new fold for an old mechanism. Structure, 9, 289-297.
33. Fabrichniy, I.P., Lehtio, L., Tammenkoski, M., Zyryanov, A.B., Oksanen, E., Baykov, A.A., Lahti, R., Goldman, A. (2007) A trimetal site and substrate distortion in a family II inorganic pyrophosphatase. J. Biol. Chem., 282, 1422-1431.
34. Harding, M.M. (2001) Geometry of metal-ligand interactions in proteins. Acta Cryst., D57, 401-411.
35. Fabrichniy, I.P., Lehtio, L., Salminen, A., Zyryanov, A.B., Baykov, A.A., Lahti, R., Goldman, A. (2004) Structural studies of metal ions in family II pyrophosphatases: the requirement for a Janus ion. Biochemistry, 43, 14403-14411.
36. Holm, L., Rosenstrom, P. (2010) Dali server: conservation mapping in 3D. Nucleic Acids Res., 38, W545-W549.
37. Yamagata, A., Kakuta, Y., Masui, R., Fukuyama, K. (2002) The crystal structure of exonuclease RecJ bound to Mn2+ ion suggests how its characteristic motifs are involved in exonuclease activity. Proc. Natl. Acad. Sci. U.S.A., 99, 5908-5912.
38. Guo, M., Chong, Y.E., Beebe, K., Shapiro, R., Yang, X.L., Schimmel, P. (2009) The C-Ala domain brings together editing and aminoacylation functions on one tRNA. Science, 325, 744-747.
39. Sutera, V.A. Jr, Han, E.S., Rajman, L.A., Lovett, S.T. (1999) Mutational analysis of the RecJ exonuclease of Escherichia coli: identification of phosphoesterase motifs. J. Bacteriol., 181, 6098-6102.
40. Rao, F., See, R.Y., Zhang, D., Toh, D.C., Ji, Q., Liang, Z.X. (2010) YybT is a signaling protein that contains a cyclic dinucleotide phosphodiesterase domain and a GGDEF domain with ATPase activity. J. Biol. Chem., 285, 473-482.
41. Aravind, L., Koonin, E.V. (1998) The HD domain defines a new superfamily of metal-dependent phosphohydrolases. Trends Biochem. Sci., 23, 469-472.
42. Ugochukwu, E., Lovering, A.L., Mather, O.C., Young, T.W., White, S.A. (2007) The crystal structure of the cytosolic exopolyphosphatase from Saccharomyces cerevisiae reveals the basis for substrate specificity. J. Mol. Biol., 371, 1007-1021.
43. Hatzios, S.K., Iavarone, A.T., Bertozzi, C.R. (2008) Rv2131c from Mycobacterium tuberculosis is a CysQ 3'-phosphoadenosine-5'- phosphatase. Biochemistry, 47, 5823-5831.
44. Young, P.A., Elvin, C.M., Hamdan, S.M., Wood, R.J., Liyou, N.E., Hamwood, T.E., Jennings, P.A., Dixon, N.E. (2008) Hydrolysis of the 5'-p-nitrophenyl ester of TMP by oligoribonucleases (ORN) from Escherichia coli, Mycobacterium smegmatis, and human. Protein Expr. Purif., 57, 180-187.
45. Engelen, S., Vallenet, D., Médigue, C., Danchin, A. (2012) Distinct co-evolution patterns of genes associated to DNA polymerase III DnaE and PolC. BMC Genomics, 13, 69-83.
46. Oberai, A., Ihm, Y., Kim, S., Bowie, J.U. (2006) A limited universe of membrane protein families and folds. Protein Sci., 15, 1723-1734.
47. Wallace, A.C., Laskowski, R.A., Thornton, J.M. (1996) Derivation of 3D coordinate templates for searching structural databases: application to Ser-His-Asp catalytic triads in the serine proteinases and lipases. Protein Sci., 5, 1001-1013.
48. Cheng, C., Kussie, P., Pavletich, N., Shuman, S. (1998) Conservation of structure and mechanism between eukaryotic topoisomerase I and site-specific recombinases. Cell, 92, 841-850.