The crystal structure of the leptospiral hypothetical protein LIC12922 reveals homology with the periplasmic chaperone SurA

Journal of Structural Biology

Volumn 173, Issue 2, 2011, Pages 312-322

  Giuseppe, Priscila O ^a   Atzingen, Marina Von ^b   Nascimento, Ana Lúcia T O ^b,c   Zanchin, Nilson I T ^d   Guimarães, Beatriz G ^e  

^a BRAZILIAN CENTER FOR RESEARCH IN ENERGY AND MATERIALS CNPEM   (Brazil)

^b INSTITUTO BUTANTAN   (Brazil)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

^d UNIVERSITY OF CAMPINAS   (Brazil)

^e SYNCHROTRON SOLEIL   (France)

Author keywords

Chaperone; Crystal structure; LIC12922; Parvulin domain; SurA homology

Indexed keywords

BACTERIAL PROTEIN; CHAPERONE; CHAPERONE SURA; CIS TRANS ISOMERASE; OUTER MEMBRANE PROTEIN; PROTEIN LIC 12922; UNCLASSIFIED DRUG;

ARTICLE; BIOGENESIS; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ESCHERICHIA COLI; LEPTOSPIRA; LEPTOSPIRA INTERROGANS; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN STRUCTURE; STRUCTURAL HOMOLOGY; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; BACTERIAL OUTER MEMBRANE PROTEINS; LEPTOSPIRA; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PERIPLASM; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID;

ESCHERICHIA COLI; LEPTOSPIRA; LEPTOSPIRA INTERROGANS; SPIROCHAETES;

EID: 78751577599     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2010.10.009     Document Type: Article

References (71)

1. Abrahams J.P., Leslie A.G. Methods used in the structure determination of bovine mitochondrial F1 ATPase. Acta Crystallogr. D Biol. Crystallogr. 1996, 52:30-42.
2. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997, 25:3389-3402.
3. Atzingen M., Goncales A., Morais Z., Araujo E., De Brito T., Vasconcellos S., Nascimento A.L. Characterization of leptospiral proteins that afforded partial protection in hamsters against lethal challenge with Leptospira interrogans. J. Med. Microbiol. 2010.
4. Behrens S. Periplasmic chaperones-new structural and functional insights. Structure 2002, 10:1469-1471.
5. Behrens S., Maier R., de Cock H., Schmid F.X., Gross C.A. The SurA periplasmic PPIase lacking its parvulin domains functions in vivo and has chaperone activity. EMBO J. 2001, 20:285-294.
6. Behrens-Kneip S. The role of SurA factor in outer membrane protein transport and virulence. Int. J. Med. Microbiol 2010.
7. Behrsin C.D., Bailey M.L., Bateman K.S., Hamilton K.S., Wahl L.M., Brandl C.J., Shilton B.H., Litchfield D.W. Functionally important residues in the peptidyl-prolyl isomerase Pin1 revealed by unigenic evolution. J. Mol. Biol. 2007, 365:1143-1162.
8. Biertumpfel C., Basquin J., Suck D., Sauter C. Crystallization of biological macromolecules using agarose gel. Acta Crystallogr. D Biol. Crystallogr. 2002, 58:1657-1659.
9. Bitto E., McKay D.B. Crystallographic structure of SurA, a molecular chaperone that facilitates folding of outer membrane porins. Structure 2002, 10:1489-1498.
10. Bradford J.R., Westhead D.R. Improved prediction of protein-protein binding sites using a support vector machines approach. Bioinformatics 2005, 21:1487-1494.
11. Bricogne G., Vonrhein C., Flensburg C., Schiltz M., Paciorek W. Generation, representation and flow of phase information in structure determination: recent developments in and around SHARP 2.0. Acta Crystallogr. D Biol. Crystallogr 2003, 59:2023-2030.
12. Bricogne G., Blanc E., Brandl M., Flensburg C., Keller P., Paciorek W., Roversi P., Smart O.S., Vonrhein C., Womack T.O. BUSTER, version 2.9.1 2010, Global Phasing Ltd., Cambridge, United Kingdom.
13. Bryson K., McGuffin L.J., Marsden R.L., Ward J.J., Sodhi J.S., Jones D.T. Protein structure prediction servers at University College London. Nucleic Acids Res. 2005, 33:W36-W38.
14. Bulach D.M., Zuerner R.L., Wilson P., Seemann T., McGrath A., Cullen P.A., Davis J., Johnson M., Kuczek E., Alt D.P., Peterson-Burch B., Coppel R.L., Rood J.I., Davies J.K., Adler B. Genome reduction in Leptospira borgpetersenii reflects limited transmission potential. Proc. Natl. Acad. Sci. USA 2006, 103:14560-14565.
15. Buljan M., Bateman A. The evolution of protein domain families. Biochem. Soc. Trans. 2009, 37:751-755.
16. Ciccarelli F.D., Doerks T., von Mering C., Creevey C.J., Snel B., Bork P. Toward automatic reconstruction of a highly resolved tree of life. Science 2006, 311:1283-1287.
17. Cullen P.A., Haake D.A., Adler B. Outer membrane proteins of pathogenic spirochetes. FEMS Microbiol. Rev. 2004, 28:291-318.
18. Davis I.W., Leaver-Fay A., Chen V.B., Block J.N., Kapral G.J., Wang X., Murray L.W., Arendall W.B., Snoeyink J., Richardson J.S., Richardson D.C. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 2007, 35:W375-W383.
19. DeLano, W.L. 2002. The PyMOL Molecular Graphics System. DeLano Scientific, San Carlos, CA, USA. http://www.pymol.org.
20. Emanuelsson O., Brunak S., von Heijne G., Nielsen H. Locating proteins in the cell using TargetP, SignalP and related tools. Nat. Protoc. 2007, 2:953-971.
21. Emsley P., Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 2004, 60:2126-2132.
22. Evans G., Pettifer R.F. CHOOCH: a program for deriving anomalous-scattering factors from X-ray fluorescence spectra. J. Appl. Cryst. 2001, 34:82-86.
23. Faine S., Adler B., Bolin C., Perolat P. Leptospira and leptospirosis 1999, second ed. MediSci, Melbourne.
24. Felsenstein, J. 2009. PHYLIP (Phylogeny Inference Package), version 3.69, Distributed by the author. Department of Genome Sciences, University of Washington. Seattle, WA, USA, 2009. Available online: (accessed on 18 March 2010). http://evolution.genetics.washington.edu/phylip.html.
25. Ferbitz L., Maier T., Patzelt H., Bukau B., Deuerling E., Ban N. Trigger factor in complex with the ribosome forms a molecular cradle for nascent proteins. Nature 2004, 431:590-596.
26. Gemmill T.R., Wu X., Hanes S.D. Vanishingly low levels of Ess1 prolyl-isomerase activity are sufficient for growth in Saccharomyces cerevisiae. J. Biol. Chem. 2005, 280:15510-15517.
27. Gouet P., Courcelle E., Stuart D.I., Metoz F. ESPript: multiple sequence alignments in PostScript. Bioinformatics 1999, 15:305-308.
28. Gough J. The SUPERFAMILY database in structural genomics. Acta Crystallogr. D Biol. Crystallogr. 2002, 58:1897-1900.
29. Gough J., Karplus K., Hughey R., Chothia C. Assignment of homology to genome sequences using a library of hidden Markov models that represent all proteins of known structure. J. Mol. Biol. 2001, 313:903-919.
30. Heikkinen O., Seppala R., Tossavainen H., Heikkinen S., Koskela H., Permi P., Kilpelainen I. Solution structure of the parvulin-type PPIase domain of Staphylococcus aureus PrsA-implications for the catalytic mechanism of parvulins. BMC Struct. Biol. 2009, 9:17.
31. Hubbard T.J., Murzin A.G., Brenner S.E., Chothia C. SCOP: a structural classification of proteins database. Nucleic Acids Res. 1997, 25:236-239.
32. Inada R., Ido Y., Hoki R., Kaneko R., Ito H. The Etiology, Mode of Infection, and Specific Therapy of Weil's Disease (Spirochaetosis Icterohaemorrhagica). J. Exp. Med. 1916, 23:377-402.
33. Kabsch W. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Cryst. 1993, 26:795-800.
34. Ko A.I., Goarant C., Picardeau M. Leptospira: the dawn of the molecular genetics era for an emerging zoonotic pathogen. Nat. Rev. Microbiol. 2009, 7:736-747.
35. Kofron J.L., Kuzmic P., Kishore V., Colon-Bonilla E., Rich D.H. Determination of kinetic constants for peptidyl prolyl cis-trans isomerases by an improved spectrophotometric assay. Biochemistry 1991, 30:6127-6134.
36. Krissinel E., Henrick K. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr. D Biol. Crystallogr. 2004, 60:2256-2268.
37. Krissinel E., Henrick K. Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 2007, 372:774-797.
38. Lakshmipathy S.K., Tomic S., Kaiser C.M., Chang H.C., Genevaux P., Georgopoulos C., Barral J.M., Johnson A.E., Hartl F.U., Etchells S.A. Identification of nascent chain interaction sites on trigger factor. J. Biol. Chem. 2007, 282:12186-12193.
39. Laskowski R.A., MacArthur M.W., Moss D.S., Thornton J.M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Cryst. 1993, 26:283-291.
40. Lazar S.W., Kolter R. SurA assists the folding of Escherichia coli outer membrane proteins. J. Bacteriol. 1996, 178:1770-1773.
41. Levett P.N. Leptospirosis. Clin. Microbiol. Rev. 2001, 14:296-326.
42. Lo M., Cordwell S.J., Bulach D.M., Adler B. Comparative transcriptional and translational analysis of leptospiral outer membrane protein expression in response to temperature. PLoS Negl. Trop. Dis. 2009, 3:e560.
43. McBride A.J., Athanazio D.A., Reis M.G., Ko A.I. Leptospirosis. Curr. Opin. Infect. Dis. 2005, 18:376-386.
44. Merz F., Hoffmann A., Rutkowska A., Zachmann-Brand B., Bukau B., Deuerling E. The C-terminal domain of Escherichia coli trigger factor represents the central module of its chaperone activity. J. Biol. Chem. 2006, 281:31963-31971.
45. Merz F., Boehringer D., Schaffitzel C., Preissler S., Hoffmann A., Maier T., Rutkowska A., Lozza J., Ban N., Bukau B., Deuerling E. Molecular mechanism and structure of Trigger Factor bound to the translating ribosome. EMBO J. 2008, 27:1622-1632.
46. Moretti S., Armougom F., Wallace I.M., Higgins D.G., Jongeneel C.V., Notredame C. The M-Coffee web server: a meta-method for computing multiple sequence alignments by combining alternative alignment methods. Nucleic Acids Res. 2007, 35:W645-W648.
47. Muller M., Koch H.G., Beck K., Schafer U. Protein traffic in bacteria: multiple routes from the ribosome to and across the membrane. Prog. Nucleic Acid Res. Mol. Biol. 2001, 66:107-157.
48. 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.
49. Nakai K., Horton P. PSORT: a program for detecting sorting signals in proteins and predicting their subcellular localization. Trends Biochem. Sci. 1999, 24:34-36.
50. Nascimento A.L., Verjovski-Almeida S., Van Sluys M.A., Monteiro-Vitorello C.B., Camargo L.E., Digiampietri L.A., Harstkeerl R.A., Ho P.L., Marques M.V., Oliveira M.C., Setubal J.C., Haake D.A., Martins E.A. Genome features of Leptospira interrogans serovar Copenhageni. Braz. J. Med. Biol. Res. 2004, 37:459-477.
51. Page R.D. TreeView: an application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 1996, 12:357-358.
52. Picardeau M., Bulach D.M., Bouchier C., Zuerner R.L., Zidane N., Wilson P.J., Creno S., Kuczek E.S., Bommezzadri S., Davis J.C., McGrath A., Johnson M.J., Boursaux-Eude C., Seemann T., Rouy Z., Coppel R.L., Rood J.I., Lajus A., Davies J.K., Medigue C., Adler B. Genome sequence of the saprophyte Leptospira biflexa provides insights into the evolution of Leptospira and the pathogenesis of leptospirosis. PLoS ONE 2008, 3:e1607.
53. Qin, J.H., Sheng, Y.Y., Zhang, Z.M., Shi, Y.Z., He, P., Hu, B.Y., Yang, Y., Liu, S.G., Zhao, G.P., Guo, X.K., 2006. Genome-wide transcriptional analysis of temperature shift in L. interrogans serovar lai strain 56601. BMC Microbiol. 6, 51.
54. Ranganathan R., Lu K.P., Hunter T., Noel J.P. Structural and functional analysis of the mitotic rotamase Pin1 suggests substrate recognition is phosphorylation dependent. Cell 1997, 89:875-886.
55. Rouviere P.E., Gross C.A. SurA, a periplasmic protein with peptidyl-prolyl isomerase activity, participates in the assembly of outer membrane porins. Genes Dev. 1996, 10:3170-3182.
56. Sayers E.W., Barrett T., Benson D.A., Bryant S.H., Canese K., Chetvernin V., Church D.M., DiCuccio M., Edgar R., Federhen S., Feolo M., Geer L.Y., Helmberg W., Kapustin Y., Landsman D., Lipman D.J., Madden T.L., Maglott D.R., Miller V., Mizrachi I., Ostell J., Pruitt K.D., Schuler G.D., Sequeira E., Sherry S.T., Shumway M., Sirotkin K., Souvorov A., Starchenko G., Tatusova T.A., Wagner L., Yaschenko E., Ye J. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res. 2009, 37:D5-D15.
57. Schulze-Gahmen U., Aono S., Chen S., Yokota H., Kim R., Kim S.H. Structure of the hypothetical Mycoplasma protein MPN555 suggests a chaperone function. Acta Crystallogr. D Biol. Crystallogr. 2005, 61:1343-1347.
58. Sheldrick G.M. A short history of SHELX. Acta Crystallogr. A 2008, 64:112-122.
59. Sklar J.G., Wu T., Kahne D., Silhavy T.J. Defining the roles of the periplasmic chaperones SurA, Skp, and DegP in Escherichia coli. Genes Dev. 2007, 21:2473-2484.
60. Stura E.A., Wilson I.A. Seeding Techniques, Crystallization of Nucleic Acids and Proteins: A Practical Approach 1992, Oxford University Press, Oxford.
61. Terada T., Shirouzu M., Fukumori Y., Fujimori F., Ito Y., Kigawa T., Yokoyama S., Uchida T. Solution structure of the human parvulin-like peptidyl prolyl cis/trans isomerase, hPar14. J. Mol. Biol. 2001, 305:917-926.
62. Vagin A.A., Isupov M.N. Spherically averaged phased translation function and its application to the search for molecules and fragments in electron-density maps. Acta Crystallogr. D Biol. Crystallogr. 2001, 57:1451-1456.
63. Valent Q.A., Kendall D.A., High S., Kusters R., Oudega B., Luirink J. Early events in preprotein recognition in E. Coli: interaction of SRP and trigger factor with nascent polypeptides. EMBO J. 1995, 14:5494-5505.
64. Valent Q.A., Scotti P.A., High S., de Gier J.W., von Heijne G., Lentzen G., Wintermeyer W., Oudega B., Luirink J. The Escherichia coli SRP and SecB targeting pathways converge at the translocon. EMBO J. 1998, 17:2504-2512.
65. Van Duyne G.D., Standaert R.F., Karplus P.A., Schreiber S.L., Clardy J. Atomic structures of the human immunophilin FKBP-12 complexes with FK506 and rapamycin. J. Mol. Biol. 1993, 229:105-124.
66. Vieira M.L., Atzingen M.V., Oliveira T.R., Oliveira R., Andrade D.M., Vasconcellos S.A., Nascimento A.L. In vitro identification of novel plasminogen-binding receptors of the pathogen Leptospira interrogans. PLoS ONE 2010, 5:e11259.
67. Vitikainen M., Lappalainen I., Seppala R., Antelmann H., Boer H., Taira S., Savilahti H., Hecker M., Vihinen M., Sarvas M., Kontinen V.P. Structure-function analysis of PrsA reveals roles for the parvulin-like and flanking N- and C-terminal domains in protein folding and secretion in Bacillus subtilis. J. Biol. Chem. 2004, 279:19302-19314.
68. Weininger U., Jakob R.P., Kovermann M., Balbach J., Schmid F.X. The prolyl isomerase domain of PpiD from Escherichia coli shows a parvulin fold but is devoid of catalytic activity. Protein Sci. 2010, 19:6-18.
69. Wu X., Wilcox C.B., Devasahayam G., Hackett R.L., Arevalo-Rodriguez M., Cardenas M.E., Heitman J., Hanes S.D. The Ess1 prolyl isomerase is linked to chromatin remodeling complexes and the general transcription machinery. EMBO J. 2000, 19:3727-3738.
70. Xu X., Wang S., Hu Y.X., McKay D.B. The periplasmic bacterial molecular chaperone SurA adapts its structure to bind peptides in different conformations to assert a sequence preference for aromatic residues. J. Mol. Biol. 2007, 373:367-381.
71. Xue F., Yan J., Picardeau M. Evolution and pathogenesis of Leptospira spp.: lessons learned from the genomes. Microbes Infect. 2009, 11:328-333.