The basic keratin 10-binding domain of the virulence-associated pneumococcal serine-rich protein PsrP adopts a novel MSCRAMM fold

Open Biology

Volumn 4, Issue JAN, 2014, Pages

  Schulte, Tim ^a   Löfling, Jonas ^b,c   Mikaelsson, Cecilia ^a   Kikhney, Alexey ^d   Hentrich, Karina ^b,c   Diamante, Aurora ^a   Ebel, Christine ^e   Normark, Staffan ^b,c   Svergun, Dmitri ^d   Henriques Normark, Birgitta ^b,c   Achour, Adnane ^a  

^a SCIENCE FOR LIFE LABORATORY   (Sweden)

^b KAROLINSKA INSTITUTE   (Sweden)

^c KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^d EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^e CEA GRENOBLE   (France)

Author keywords

Adhesion; Bacterial virulence factor; Keratin 10; MSCRAMM; PsrP; Streptococcus pneumoniae

Indexed keywords

BACTERIA (MICROORGANISMS); STREPTOCOCCUS PNEUMONIAE;

ADHESIN; ALANINE; BACTERIAL PROTEIN; CYTOKERATIN 10; VIRULENCE FACTOR;

ADHESION; AMINO ACID SUBSTITUTION; ARTICLE; BACTERIAL VIRULENCE FACTOR; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; HUMAN; METABOLISM; MSCRAMM; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; PSRP; STATIC ELECTRICITY; STREPTOCOCCUS PNEUMONIAE; X RAY CRYSTALLOGRAPHY;

ADHESION; BACTERIAL VIRULENCE FACTOR; KERATIN-10; MSCRAMM; PSRP; STREPTOCOCCUS PNEUMONIAE;

ADHESINS, BACTERIAL; ALANINE; AMINO ACID SUBSTITUTION; BACTERIAL PROTEINS; CRYSTALLOGRAPHY, X-RAY; HUMANS; KERATIN-10; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; STATIC ELECTRICITY; STREPTOCOCCUS PNEUMONIAE; VIRULENCE FACTORS;

EID: 84901036159     PISSN: None     EISSN: 20462441     Source Type: Journal    
DOI: 10.1098/rsob.130090     Document Type: Article

References (50)

1. Van der Poll T, Opal SM. 2009 Pathogenesis, treatment, and prevention of pneumococcal pneumonia. Lancet 374, 1543-1556. (doi: 10.1016/S0140-6736(09) 61114-4)
2. Muñoz-Almagro C, Selva L, Sanchez CJ, Esteva C, de Sevilla MF, Pallares R, Orihuela CJ. 2010 PsrP, a protective pneumococcal antigen, is highly prevalent in children with pneumonia and is strongly associated with clonal type. Clin. Vaccine Immunol. 17, 1672-1678. (doi: 10.1128/CVI.00271-10)
3. Gamez G, Hammerschmidt S. 2012 Combat pneumococcal infections: adhesins as candidates for protein-based vaccine development. Curr. Drug Targets 13, 323-337. (doi: 10.2174/138945012799424697)
4. Spirig T, Weiner EM, Clubb RT. 2011 Sortase enzymes in Gram-positive bacteria. Mol. Microbiol. 82, 1044-1059. (doi: 10.1111/j.1365-2958.2011.07887.x)
5. Lizcano A, Sanchez CJ, Orihuela CJ. 2012 A role for glycosylated serine-rich repeat proteins in Grampositive bacterial pathogenesis. Mol. Oral Microbiol. 27, 257-269. (doi: 10.1111/j.2041-1014.2012.00653.x)
6. Ramboarina S et al. 2010 Structural insights into serine-rich fimbriae from gram-positive bacteria. J. Biol. Chem. 285, 32446-32457. (doi: 10.1074/jbc.M110.128165)
7. Sanchez CJ, Shivshankar P, Stol K, Trakhtenbroit S, Sullam PM, Sauer K, Hermans PWM, Orihuela CJ. 2010 The pneumococcal serine-rich repeat protein is an intra-species bacterial adhesin that promotes bacterial aggregation in vivo and in biofilms. PLoS Pathog. 6, e1001044. (doi: 10.1371/journal.ppat.1001044)
8. Pyburn TM et al. 2011 A structural model for binding of the serine-rich repeat adhesin GspB to host carbohydrate receptors. PLoS Pathog. 7, e1002112. (doi: 10.1371/journal.ppat.1002112)
9. Shivshankar P, Sanchez C, Rose LF, Orihuela CJ. 2009 The Streptococcus pneumoniae adhesin PsrP binds to keratin 10 on lung cells. Mol. Microbiol 73, 663-679. (doi: 10.1111/j.1365-2958.2009.06796.x)
10. Parry DAD, Steinert PM. 1999 Intermediate filaments: molecular architecture, assembly, dynamics and polymorphism. Q. Rev. Biophys. 32, 99-187. (doi: 10.1017/S0033583500003516) (Pubitemid 30303680)
11. Moll R, Divo M, Langbein L. 2008 The human keratins: biology and pathology. Histochem. Cell Biol. 129, 705-733. (doi: 10.1007/s00418-008-0435-6)
12. Lee C-H, Kim M-S, Chung BM, Leahy DJ, Coulombe PA. 2012 Structural basis for heteromeric assembly and perinuclear organization of keratin filaments. Nat. Struct. Mol. Biol. 19, 707. (doi: 10.1038/nsmb.2330)
13. O'Brien LM, Walsh EJ, Massey RC, Peacock SJ, Foster TJ. 2002 Staphylococcus aureus clumping factor B (ClfB) promotes adherence to human type I cytokeratin 10: implications for nasal colonization. Cell. Microbiol. 4, 759-770. (doi: 10.1046/j.1462-5822.2002.00231.x) (Pubitemid 35378715)
14. Haim M, Trost A, Maier CJ, Achatz G, Feichtner S, Hintner H, Bauer JW, Önder K. 2010 Cytokeratin 8 interacts with clumping factor B: a new possible virulence factor target. Microbiology 156, 3710-3721. (doi: 10.1099/mic.0.034413-0)
15. Samen U, Eikmanns BJ, Reinscheid DJ, Borges F. 2007 The surface protein Srr-1 of Streptococcus agalactiae binds human keratin 4 and promotes adherence to epithelial HEp-2 cells. Infect. Immun. 75, 5405-5414. (doi: 10.1128/IAI.00717-07) (Pubitemid 350033629)
16. Ganesh VK et al. 2011 Structural and biochemical characterization of Staphylococcus aureus clumping factor B/ligand interactions. J. Biol. Chem. 286, 25963-25972. (doi: 10.1074/jbc.M110.217414)
17. Xiang H, Feng Y, Wang J, Liu B, Chen Y, Liu L, Deng X, Yang M. 2012 Crystal structures reveal the multi-ligand binding mechanism of Staphylococcus aureus ClfB. PLoS Pathog. 8, e1002751. (doi: 10.1371/journal.ppat.1002751)
18. Symersky J et al. 1997 Structure of the collagen-binding domain from a Staphylococcus aureus adhesin. Nat. Struct. Mol. Biol. 4, 833-838. (doi: 10.1038/nsb1097-833) (Pubitemid 27435349)
19. Deivanayagam CCS, Wann ER, Chen W, Carson M, Rajashankar KR, Hook M, Narayana SVL 2002 A novel variant of the immunoglobulin fold in surface adhesins of Staphylococcus aureus: crystal structure of the fibrinogen-binding MSCRAMM, clumping factor A. EMBO J. 21, 6660-6672. (doi: 10.1093/emboj/cdf619) (Pubitemid 36014538)
20. Sheldrick GM 2010 Experimental phasing with SHELXC/D/E: combining chain tracing with density modification. Acta Crystallogr. D, Biol. Crystallogr. 66, 479-485. (doi: 10.1107/S0907444909038360)
21. Bork P, Holm L, Sander C. 1994 The immunoglobulin fold: structural classification, sequence patterns and common core. J. Mol. Biol. 242, 309-320. (doi: 10.1006/jmbi.1994.1582)
22. Vengadesan K, Narayana SVL 2011 Structural biology of Gram-positive bacterial adhesins. Protein Sci. 20, 759-772. (doi: 10.1002/pro.613)
23. Holm L, Kääriäinen S, Rosenström P, Schenkel A. 2008 Searching protein structure databases with DaliLite v. 3. Bioinformatics 24, 2780-2781. (doi: 10.1093/bioinformatics/btn507) (Pubitemid 352722625)
24. Mészáros B, Tompa P, Simon I, Dosztányi Z. 2007 Molecular principles of the interactions of disordered proteins. J. Mol. Biol. 372, 549-561. (doi: 10.1016/j.jmb.2007.07.004) (Pubitemid 47267965)
25. Schreiber G, Haran G, Zhou H-X. 2009 Fundamental aspects of protein2protein association kinetics. Chem. Rev. 109, 839-860. (doi: 10.1021/cr800373w)
26. Mack JW, Torchia DA, Steinert PM. 1988 Solid-state NMR studies of the dynamics and structure of mouse keratin intermediate filaments. Biochemistry 27, 5418-5426. (doi: 10.1021/bi00415a006)
27. Steinert PM, Mack JW, Korge BP, Gan SQ, Haynes SR, Steven AC. 1991 Glycine loops in proteins: their occurrence in certain intermediate filament chains, loricrins and single-stranded RNA binding proteins. Int. J. Biol. Macromol. 13, 130-139. (doi: 10.1016/0141-8130(91)90037-U)
28. Strnad P, Usachov V, Debes C, Gräter F, Parry DAD, Omary MB. 2011 Unique amino acid signatures that are evolutionarily conserved distinguish simple-type, epidermal and hair keratins. J. Cell. Sci. 124, 4221-4232. (doi: 10.1242/jcs.089516)
29. Petsalaki E, Stark A, García-Urdiales E, Russell RB. 2009 Accurate prediction of peptide binding sites on protein surfaces. PLoS Comput. Biol. 5, e1000335. (doi: 10.1371/journal.pcbi.1000335)
30. Li C, Wen A, Shen B, Lu J, Huang Y, Chang Y. 2011 FastCloning: a highly simplified, purification-free, sequence- and ligation-independent PCR cloning method. BMC Biotechnol. 11, 92. (doi: 10.1186/1472-6750-11-92)
31. Mellroth P, Daniels R, Eberhardt A, Rönnlund D, Blom H, Widengren J, Normark S, Henriques-Normark B. 2012 LytA, major autolysin of Streptococcus pneumoniae, requires access to nascent peptidoglycan. J. Biol. Chem. 287, 11018-11029. (doi: 10.1074/jbc.M111.318584)
32. Li J, Li C, Xiao W, Yuan D, Wan G, Ma L. 2008 Site-directed mutagenesis by combination of homologous recombination and DpnI digestion of the plasmid template in Escherichia coli. Anal. Biochem. 373, 389-391. (doi: 10.1016/j.ab.2007.10.034)
33. Cormier CY et al. 2010 Protein structure initiative material repository: an open shared public resource of structural genomics plasmids for the biological community. Nucleic Acids Res. 38, D743-D749. (doi: 10.1093/nar/gkp999)
34. Koth CM, Orlicky SM, Larson SM, Edwards AM. 2003 Use of limited proteolysis to identify protein domains suitable for structural analysis. In Macromolecular crystallography, part C (eds CW Carter Jr, RM Sweet), pp. 77-84. San Diego, CA: Academic Press. (Pubitemid 37498343)
35. Hatzfeld M, Weber K. 1990 Tailless keratins assemble into regular intermediate filaments in vitro. J. Cell. Sci. 97, 317-324. (Pubitemid 20361411)
36. Kabsch W. 1993 Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Crystallogr. 26, 795-800. (doi: 10.1107/S0021889893005588)
37. Panjikar S, Parthasarathy V, Lamzin VS, Weiss MS, Tucker PA. 2005 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, 449-457. (doi: 10.1107/S0907444905001307) (Pubitemid 43934605)
38. CCP4. 1994 The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D, Biol. Crystallogr. 50, 760-763. (doi: 10.1107/S0907444994003112)
39. Emsley P, Cowtan K. 2004 Coot: model-building tools for molecular graphics. Acta Crystallogr. D, Biol. Crystallogr. 60, 2126-2132. (doi: 10.1107/S0907444904019158) (Pubitemid 41742764)
40. McCoy AJ 2007 Solving structures of protein complexes by molecular replacement with Phaser. Acta Crystallogr. D, Biol. Crystallogr. 63, 32-41. (doi: 10.1107/S0907444906045975)
41. Adams PD et al. 2002 PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. D, Biol. Crystallogr. 58, 1948-1954. (doi: 10.1107/S0907444902016657) (Pubitemid 35337293)
42. Steinkellner G, Rader R, Thallinger GG, Kratky C, Gruber K. 2009 VASCo: computation and visualization of annotated protein surface contacts. BMC Bioinformatics 10, 32. (doi: 10.1186/1471-2105-10-32)
43. Dolinsky TJ, Nielsen JE, McCammon JA, Baker NA. 2004 PDB2PQR: an automated pipeline for the setup of Poisson-Boltzmann electrostatics calculations. Nucleic Acids Res. 32, W665-W667. (doi: 10.1093/nar/gkh381) (Pubitemid 38997419)
44. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA. 2001 Electrostatics of nanosystems: application to microtubules and the ribosome. Proc. Natl Acad. Sci. USA 98, 10037-10041. (doi: 10.1073/pnas.181342398) (Pubitemid 32802969)
45. Schrödinger L. 2010 PyMOL molecular graphics system. See http://www.pymol.org.
46. García De La Torre J, Huertas ML, Carrasco B. 2000 Calculation of hydrodynamic properties of globular proteins from their atomic-level structure. Biophys. J. 78, 719-730. (doi: 10.1016/S0006-3495(00)76630-6) (Pubitemid 30211830)
47. Blanchet CE et al. 2012 Instrumental setup for high-throughput small- and wide-angle solution scattering at the X33 beamline of EMBL Hamburg. J. Appl. Crystallogr. 45, 489-495. (doi: 10.1107/S0021889812013490)
48. Franke D, Kikhney AG, Svergun DI. 2012 Automated acquisition and analysis of small angle X-ray scattering data. Nucl. Instrum. Methods Phys. Res. A 689, 52-59. (doi: 10.1016/j.nima.2012.06.008)
49. Petoukhov MV et al. 2012 New developments in the ATSAS program package for small-angle scattering data analysis. J. Appl. Crystallogr. 45, 342-350. (doi: 10.1107/S0021889812007662)
50. Bernadó P, Mylonas E, Petoukhov MV, Blackledge M, Svergun DI. 2007 Structural characterization of flexible proteins using small-angle X-ray scattering. J. Am. Chem. Soc. 129, 5656-5664. (doi: 10.1021/ja069124n) (Pubitemid 46697655)