The structure of Resuscitation promoting factor B from M. tuberculosis reveals unexpected ubiquitin-like domains

Biochimica et Biophysica Acta - General Subjects

Volumn 1860, Issue 2, 2016, Pages 445-451

  Ruggiero, Alessia ^a   Squeglia, Flavia ^a   Romano, Maria ^a   Vitagliano, Luigi ^a   De Simone, Alfonso ^b   Berisio, Rita ^a  

^a CNR   (Italy)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Cell wall; Crystal structure; Peptidoglycan; Tuberculosis

Indexed keywords

BACTERIAL PROTEIN; PROTEIN RPFB; UNCLASSIFIED DRUG; SOLUTION AND SOLUBILITY; UBIQUITIN;

ARTICLE; BACTERIAL GROWTH; CATALYSIS; CIRCULAR DICHROISM; CONTROLLED STUDY; CRYSTALLOGRAPHY; GENETIC CONSERVATION; GENETIC VARIABILITY; LIGHT SCATTERING; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN STRUCTURE; SEQUENCE ALIGNMENT; SIZE EXCLUSION CHROMATOGRAPHY; STRUCTURE ANALYSIS; UBIQUITINATION; CHEMISTRY; CRYSTALLIZATION; PROTEIN TERTIARY STRUCTURE; SOLUTION AND SOLUBILITY;

BACTERIAL PROTEINS; CRYSTALLIZATION; MYCOBACTERIUM TUBERCULOSIS; PROTEIN STRUCTURE, TERTIARY; SOLUTIONS; UBIQUITIN;

EID: 84949508499     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2015.11.001     Document Type: Article

References (49)

1. H. Esmail, C.E. Barry 3rd, D.B. Young, and R.J. Wilkinson The ongoing challenge of latent tuberculosis Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 369 2014 20130437
2. V. Gupta, N. Sugg, M. Butners, G. Allen-White, and A. Molnar Tuberculosis among the homeless - preventing another outbreak through community action N. Engl. J. Med. 372 2015 1483 1485
3. A. Ruggiero, P. De Simone, G. Smaldone, F. Squeglia, and R. Berisio Bacterial cell division regulation by Ser/Thr kinases: a structural perspective Curr. Protein Pept. Sci. 13 2012 756 766
4. F. Squeglia, R. Marchetti, A. Ruggiero, R. Lanzetta, D. Marasco, J. Dworkin, M. Petoukhov, A. Molinaro, R. Berisio, and A. Silipo Chemical basis of peptidoglycan discrimination by PrkC, a key kinase involved in bacterial resuscitation from dormancy J. Am. Chem. Soc. 133 2011 20676 20679
5. A. Ruggiero, F. Squeglia, D. Marasco, R. Marchetti, A. Molinaro, and R. Berisio X-ray structural studies of the entire extracellular region of the serine/threonine kinase PrkC from Staphylococcus aureus Biochem. J. 435 2011 33 41
6. I.M. Shah, M.H. Laaberki, D.L. Popham, and J. Dworkin A eukaryotic-like Ser/Thr kinase signals bacteria to exit dormancy in response to peptidoglycan fragments Cell 135 2008 486 496
7. E.C. Hett, M.C. Chao, and E.J. Rubin Interaction and modulation of two antagonistic cell wall enzymes of mycobacteria PLoS Pathog. 6 2010 e1001020
8. F. Squeglia, A. Ruggiero, and R. Berisio Exit from mycobacterial dormancy: a structural perspective Curr. Med. Chem. 22 2015 1698 1709
9. F. Squeglia, A. Ruggiero, M. Romano, L. Vitagliano, and R. Berisio Mutational and structural study of RipA, a key enzyme in Mycobacterium tuberculosis cell division: evidence for the L-to-D inversion of configuration of the catalytic cysteine Acta Crystallogr. Sect. D: Biol. Crystallogr. 70 2014 2295 2300
10. S. Correale, A. Ruggiero, R. Capparelli, E. Pedone, and R. Berisio Structures of free and inhibited forms of the L,D-transpeptidase LdtMt1 from Mycobacterium tuberculosis Acta Crystallogr. Sect. D: Biol. Crystallogr. 69 2013 1697 1706
11. S.O. Meroueh, K.Z. Bencze, D. Hesek, M. Lee, J.F. Fisher, T.L. Stemmler, and S. Mobashery Three-dimensional structure of the bacterial cell wall peptidoglycan Proc. Natl. Acad. Sci. U. S. A. 103 2006 4404 4409
12. B.D. Kana, and V. Mizrahi Resuscitation-promoting factors as lytic enzymes for bacterial growth and signaling FEMS Immunol. Med. Microbiol. 58 2010 39 50
13. G.V. Mukamolova, N.D. Yanopolskaya, D.B. Kell, and A.S. Kaprelyants On resuscitation from the dormant state of Micrococcus luteus Antonie Van Leeuwenhoek 73 1998 237 243
14. G.V. Mukamolova, A.S. Kaprelyants, D.I. Young, M. Young, and D.B. Kell A bacterial cytokine Proc. Natl. Acad. Sci. U. S. A. 95 1998 8916 8921
15. V.D. Nikitushkin, G.R. Demina, M.O. Shleeva, S.V. Guryanova, A. Ruggiero, R. Berisio, and A.S. Kaprelyants A Product of RpfB and RipA Joint Enzymatic Action Promotes the Resuscitation of Dormant Mycobacteria 2015 Febs J
16. G.V. Mukamolova, O.A. Turapov, D.I. Young, A.S. Kaprelyants, D.B. Kell, and M. Young A family of autocrine growth factors in Mycobacterium tuberculosis Mol. Microbiol. 46 2002 623 635
17. A.P. Davies, A.P. Dhillon, M. Young, B. Henderson, T.D. McHugh, and S.H. Gillespie Resuscitation-promoting factors are expressed in Mycobacterium tuberculosis-infected human tissue Tuberculosis (Edinb.) 88 2008 462 468
18. B.D. Kana, B.G. Gordhan, K.J. Downing, N. Sung, G. Vostroktunova, E.E. Machowski, L. Tsenova, M. Young, A. Kaprelyants, G. Kaplan, and V. Mizrahi The resuscitation-promoting factors of Mycobacterium tuberculosis are required for virulence and resuscitation from dormancy but are collectively dispensable for growth in vitro Mol. Microbiol. 67 2008 672 684
19. X. Wu, Y. Yang, Y. Han, J. Zhang, Y. Liang, H. Li, B. Li, and L. Wang Effect of recombinant Rv1009 protein on promoting the growth of Mycobacterium tuberculosis J. Appl. Microbiol. 105 2008 1121 1127
20. E. Russell-Goldman, J. Xu, X. Wang, J. Chan, and J.M. Tufariello A Mycobacterium tuberculosis Rpf double-knockout strain exhibits profound defects in reactivation from chronic tuberculosis and innate immunity phenotypes Infect. Immun. 76 2008 4269 4281
21. B.D. Kana, B.G. Gordhan, K.J. Downing, N. Sung, G. Vostroktunova, E.E. Machowski, L. Tsenova, M. Young, A. Kaprelyants, G. Kaplan, and V. Mizrahi The resuscitation-promoting factors of Mycobacterium tuberculosis are required for virulence and resuscitation from dormancy but are collectively dispensable for growth in vitro Mol. Microbiol. 67 2008 672 684
22. J.M. Tufariello, K. Mi, J. Xu, Y.C. Manabe, A.K. Kesavan, J. Drumm, K. Tanaka, W.R. Jacobs Jr., and J. Chan Deletion of the Mycobacterium tuberculosis resuscitation-promoting factor Rv1009 gene results in delayed reactivation from chronic tuberculosis Infect. Immun. 74 2006 2985 2995
23. A. Ruggiero, B. Tizzano, E. Pedone, C. Pedone, M. Wilmanns, and R. Berisio Crystal structure of the resuscitation-promoting factor (DeltaDUF)RpfB from M. tuberculosis J. Mol. Biol. 385 2009 153 162
24. F. Squeglia, M. Romano, A. Ruggiero, L. Vitagliano, A. De Simone, and R. Berisio Carbohydrate recognition by RpfB from Mycobacterium tuberculosis unveiled by crystallographic and molecular dynamics analyses Biophys. J. 104 2013 2530 2539
25. A. Ruggiero, J. Marchant, F. Squeglia, V. Makarov, A. De Simone, and R. Berisio Molecular determinants of inactivation of the resuscitation promoting factor B from Mycobacterium tuberculosis J. Biomol. Struct. Dyn. 31 2013 195 205
26. M. Cohen-Gonsaud, P. Barthe, C. Bagneris, B. Henderson, J. Ward, C. Roumestand, and N.H. Keep The structure of a resuscitation-promoting factor domain from Mycobacterium tuberculosis shows homology to lysozymes Nat. Struct. Mol. Biol. 12 2005 270 273
27. J.S. Richardson, and D.C. Richardson Natural beta-sheet proteins use negative design to avoid edge-to-edge aggregation Proc. Natl. Acad. Sci. U. S. A. 99 2002 2754 2759
28. R.D. Finn, J. Tate, J. Mistry, P.C. Coggill, S.J. Sammut, H.R. Hotz, G. Ceric, K. Forslund, S.R. Eddy, E.L. Sonnhammer, and A. Bateman The Pfam protein families database Nucleic Acids Res. 36 2008 D281 D288
29. O. Goldenberg, E. Erez, G. Nimrod, and N. Ben-Tal The ConSurf-DB: pre-calculated evolutionary conservation profiles of protein structures Nucleic Acids Res. 37 2009 D323 D327
30. A. Ruggiero, F. Squeglia, L. Pirone, S. Correale, and R. Berisio Expression, purification, crystallization and preliminary X-ray crystallographic analysis of a major fragment of the resuscitation-promoting factor RpfB from Mycobacterium tuberculosis Acta Crystallogr. Sect. F: Struct. Biol. Cryst. Commun. 67 2011 164 168
31. S. Panjikar, V. Parthasarathy, V.S. Lamzin, M.S. Weiss, and P.A. Tucker Auto-Rickshaw: an automated crystal structure determination platform as an efficient tool for the validation of an X-ray diffraction experiment Acta Crystallogr. D Biol. Crystallogr. 61 2005 449 457
32. T.R. Schneider, and G.M. Sheldrick Substructure solution with SHELXD Acta Crystallogr. D Biol. Crystallogr. 58 2002 1772 1779
33. T.C. Terwilliger SOLVE and RESOLVE: automated structure solution and density modification Methods Enzymol. 374 2003 22 37
34. E. Potterton, P. Briggs, M. Turkenburg, and E. Dodson A graphical user interface to the CCP4 program suite Acta Crystallogr. D Biol. Crystallogr. 59 2003 1131 1137
35. R.A. Laskowski, J.A. Rullmannn, M.W. MacArthur, R. Kaptein, and J.M. Thornton AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR J. Biomol. NMR 8 1996 477 486
36. P.A. Karplus Experimentally observed conformation-dependent geometry and hidden strain in proteins Protein Sci.: Publication Protein Soc. 5 1996 1406 1420
37. L. Esposito, N. Balasco, A. De Simone, R. Berisio, and L. Vitagliano Interplay between peptide bond geometrical parameters in nonglobular structural contexts Biomed. Res. Int. 2013 2013 326914
38. L. Esposito, A. De Simone, A. Zagari, and L. Vitagliano Correlation between omega and psi dihedral angles in protein structures J. Mol. Biol. 347 2005 483 487
39. R. Improta, L. Vitagliano, and L. Esposito Peptide bond distortions from planarity: new insights from quantum mechanical calculations and peptide/protein crystal structures PLoS One 6 2011 e24533
40. A. Ruggiero, J.D. Dattelbaum, M. Staiano, R. Berisio, S. D'Auria, and L. Vitagliano A loose domain swapping organization confers a remarkable stability to the dimeric structure of the arginine binding protein from Thermotoga maritima PLoS One 9 2014 e96560
41. A. Micsonai, F. Wien, L. Kernya, Y.H. Lee, Y. Goto, M. Refregiers, and J. Kardos Accurate secondary structure prediction and fold recognition for circular dichroism spectroscopy Proc. Natl. Acad. Sci. U. S. A. 112 2015 E3095 E3103
42. M.D. Winn, C.C. Ballard, K.D. Cowtan, E.J. Dodson, P. Emsley, P.R. Evans, R.M. Keegan, E.B. Krissinel, A.G. Leslie, A. McCoy, S.J. McNicholas, G.N. Murshudov, N.S. Pannu, E.A. Potterton, H.R. Powell, R.J. Read, A. Vagin, and K.S. Wilson Overview of the CCP4 suite and current developments Acta Crystallogr. Sect. D: Biol. Crystallogr. 67 2011 235 242
43. L. Holm, and P. Rosenstrom Dali server: conservation mapping in 3D Nucleic Acids Res. 38 2010 W545 W549
44. M.J. Rudolph, M.M. Wuebbens, K.V. Rajagopalan, and H. Schindelin Crystal structure of molybdopterin synthase and its evolutionary relationship to ubiquitin activation Nat. Struct. Biol. 8 2001 42 46
45. S. Vijay-Kumar, C.E. Bugg, and W.J. Cook Structure of ubiquitin refined at 1.8 A resolution J. Mol. Biol. 194 1987 531 544
46. D. Finley, H.D. Ulrich, T. Sommer, and P. Kaiser The ubiquitin-proteasome system of Saccharomyces cerevisiae Genetics 192 2012 319 360
47. P.J. Kraulis Similarity of protein G and ubiquitin Science 254 1991 581 582
48. A.M. Burroughs, L.M. Iyer, and L. Aravind Structure and evolution of ubiquitin and ubiquitin-related domains Methods Mol. Biol. 832 2012 15 63
49. B. Schuster-Bockler, J. Schultz, and S. Rahmann HMM logos for visualization of protein families BMC Biochem. 5 2004 7