The identification and functional characterization of WxL proteins from Enterococcus faecium reveal surface proteins involved in extracellular matrix interactions

Journal of Bacteriology

Volumn 197, Issue 5, 2015, Pages 882-892

  Galloway Peña, Jessica R ^a,b,d   Liang, Xiaowen ^b   Singh, Kavindra V ^a,b   Yadav, Puja ^a,b   Chang, Chungyu ^a   La Rosa, Sabina Leanti ^c   Shelburne, Samuel ^d   Ton That, Hung ^a   Höök, Magnus ^b   Murray, Barbara E ^a,b  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF TEXAS   (United States)

^c NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^d UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; BACTERIAL PROTEIN; CELL SURFACE PROTEIN; COLLAGEN TYPE 1; FIBRONECTIN; LWPA PROTEIN; MEMBRANE PROTEIN; RECOMBINANT PROTEIN; SWPA PROTEIN; UNCLASSIFIED DRUG; WXL PROTEIN; PROTEIN BINDING;

AMINO ACID SEQUENCE; ANALYSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGENICITY; ARTICLE; ASSAY; BACTERIAL COLONIZATION; BACTERIAL ENDOCARDITIS; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; BACTERIUM MUTANT; BETA SHEET; BIACORE ANALYSIS; BILE SALT SURVIVAL ASSAY; CELL SURFACE; CLINICAL ARTICLE; COMMENSAL; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENTEROCOCCAL INFECTION; ENTEROCOCCUS FAECIUM; ENTEROCOCCUS FAECIUM INFECTION; ENZYME LINKED IMMUNOSORBENT ASSAY; EXTRACELLULAR MATRIX; GENE DELETION; GENE LOCUS; GENOMICS; GRAM POSITIVE BACTERIUM; HUMAN; IN VITRO STUDY; MICROBIAL DIVERSITY; NONHUMAN; OPERON; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STRESS; WESTERN BLOTTING; ANIMAL; CHEMISTRY; GENETICS; GRAM POSITIVE INFECTION; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; PATHOGENICITY; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SEQUENCE ALIGNMENT; SPRAGUE DAWLEY RAT; VIRULENCE;

ANIMALIA; BACTERIA (MICROORGANISMS); ENTEROCOCCUS FAECIUM; POSIBACTERIA;

AMINO ACID SEQUENCE; ANIMALS; BACTERIAL PROTEINS; ENTEROCOCCUS FAECIUM; EXTRACELLULAR MATRIX; GRAM-POSITIVE BACTERIAL INFECTIONS; HUMANS; MOLECULAR SEQUENCE DATA; OPERON; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RATS; RATS, SPRAGUE-DAWLEY; SEQUENCE ALIGNMENT; VIRULENCE;

EID: 84961289799     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.02288-14     Document Type: Article

References (62)

1. Rice LB. 2010. Progress and challenges in implementing the research on ESKAPE pathogens. Infect Control Hosp Epidemiol 31(Suppl 1):S7-S10. http://dx.doi.org/10.1086/655995.
2. Hendrickx AP, Willems RJ, Bonten MJ, van Schaik W. 2009. LPxTG surface proteins of enterococci. Trends Microbiol 17:423-430. http://dx .doi.org/10.1016/j.tim.2009.06.004.
3. Sillanpaa J, Nallapareddy SR, Prakash VP, Qin X, Hook M, Weinstock GM, Murray BE. 2008. Identification and phenotypic characterization of a second collagen adhesin, Scm, and genome-based identification and analysis of 13 other predicted MSCRAMMs, including four distinct pilus loci, in Enterococcus faecium. Microbiology 154:3199-3211. http://dx .doi.org/10.1099/mic.0.2008/017319-0.
4. Brinster S, Furlan S, Serror P. 2007. C-terminal WxL domain mediates cell wall binding in Enterococcus faecalis and other gram-positive bacteria. J Bacteriol 189:1244-1253. http://dx.doi.org/10.1128/JB.00773-06.
5. Chaillou S, Champomier-Verges MC, Cornet M, Crutz-Le Coq AM, Dudez AM, Martin V, Beaufils S, Darbon-Rongere E, Bossy R, Loux V, Zagorec M. 2005. The complete genome sequence of the meat-borne lactic acid bacterium Lactobacillus sakei 23K. Nat Biotechnol 23:1527-1533. http://dx.doi.org/10.1038/nbt1160.
6. Kleerebezem M, Boekhorst J, van Kranenburg R, Molenaar D, Kuipers OP, Leer R, Tarchini R, Peters SA, Sandbrink HM, Fiers MW, Stiekema W, Lankhorst RM, Bron PA, Hoffer SM, Groot MN, Kerkhoven R, de Vries M, Ursing B, de Vos WM, Siezen RJ. 2003. Complete genome sequence of Lactobacillus plantarum WCFS1. Proc Natl Acad Sci U S A 100:1990-1995. http://dx.doi.org/10.1073/pnas.0337704100.
7. Siezen R, Boekhorst J, Muscariello L, Molenaar D, Renckens B, Kleerebezem M. 2006. Lactobacillus plantarum gene clusters encoding putative cell-surface protein complexes for carbohydrate utilization are conserved in specific gram-positive bacteria. BMC Genomics 7:126. http://dx.doi .org/10.1186/1471-2164-7-126.
8. Schachtsiek M, Hammes WP, Hertel C. 2004. Characterization of Lactobacillus coryniformis DSM 20001T surface protein Cpf mediating coaggregation with and aggregation among pathogens. Appl Environ Microbiol 70: 7078-7085. http://dx.doi.org/10.1128/AEM.70.12.7078-7085.2004.
9. Brinster S, Posteraro B, Bierne H, Alberti A, Makhzami S, Sanguinetti M, Serror P. 2007. Enterococcal leucine-rich repeat-containing protein involved in virulence and host inflammatory response. Infect Immun 75: 4463-4471. http://dx.doi.org/10.1128/IAI.00279-07.
10. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Biol 215:403-410. http://dx.doi.org/10.1016 /S0022-2836(05)80360-2.
11. Gotoh O. 1995. A weighting system and algorithm for aligning many phylogenetically related sequences. Comput Appl Biosci 11:543-551.
12. Galloway-Pena J, Roh JH, Latorre M, Qin X, Murray BE. 2012. Genomic and SNP analyses demonstrate a distant separation of the hospital and community-associated clades of Enterococcus faecium. PLoS One 7:e30187. http://dx.doi.org/10.1371/journal.pone.0030187.
13. Lebreton F, van Schaik W, McGuire AM, Godfrey P, Griggs A, Mazumdar V, Corander J, Cheng L, Saif S, Young S, Zeng Q, Wortman J, Birren B, Willems RJ, Earl AM, Gilmore MS. 2013. Emergence of epidemic multidrug-resistant Enterococcus faecium from animal and commensal strains. mBio 4:e00534-13. http://dx.doi.org/10.1128/mBio .00534-13.
14. Nallapareddy SR, Singh KV, Murray BE. 2008. Contribution of the collagen adhesin Acm to pathogenesis of Enterococcus faecium in experimental endocarditis. Infect Immun 76:4120-4128. http://dx.doi.org/10 .1128/IAI.00376-08.
15. Palmer KL, Godfrey P, Griggs A, Kos VN, Zucker J, Desjardins C, Cerqueira G, Gevers D, Walker S, Wortman J, Feldgarden M, Haas B, Birren B, Gilmore MS. 2012. Comparative genomics of enterococci: variation in Enterococcus faecalis, clade structure in E. faecium, and defining characteristics of E. gallinarum and E. casseliflavus. mBio 3:e00318-00311. http://dx.doi.org/10.1128/mBio.00318-11.
16. Sillanpaa J, Nallapareddy SR, Singh KV, Prakash VP, Fothergill T, Ton-That H, Murray BE. 2010. Characterization of the ebp(fm) pilusencoding operon of Enterococcus faecium and its role in biofilm formation and virulence in a murine model of urinary tract infection. Virulence 1:236-246. http://dx.doi.org/10.4161/viru.1.4.11966.
17. Somarajan SR, Roh JH, Singh KV, Weinstock GM, Murray BE. 2014. CcpA is important for growth and virulence of Enterococcus faecium. Infect Immun 82:3580-3587. http://dx.doi.org/10.1128/IAI.01911-14.
18. Hunter S, Apweiler R, Attwood TK, Bairoch A, Bateman A, Binns D, Bork P, Das U, Daugherty L, Duquenne L, Finn RD, Gough J, Haft D, Hulo N, Kahn D, Kelly E, Laugraud A, Letunic I, Lonsdale D, Lopez R, Madera M, Maslen J, McAnulla C, McDowall J, Mistry J, Mitchell A, Mulder N, Natale D, Orengo C, Quinn AF, Selengut JD, Sigrist CJ, Thimma M, Thomas PD, Valentin F, Wilson D, Wu CH, Yeats C. 2009. InterPro: the integrative protein signature database. Nucleic Acids Res 37:D211-D215. http://dx.doi.org/10.1093/nar/gkn785.
19. Krogh A, Larsson B, von Heijne G, Sonnhammer EL. 2001. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567-580. http://dx.doi.org/10 .1006/jmbi.2000.4315.
20. Nielsen H, Brunak S, von Heijne G. 1999. Machine learning approaches for the prediction of signal peptides and other protein sorting signals. Protein Eng 12:3-9. http://dx.doi.org/10.1093/protein/12.1.3.
21. Solovyev V, Salamov A. 2011. Automatic annotation of microbial ge-nomes and metagenomic sequences, p 61-78. In LiRW(ed), Metagenomics and its applications in agriculture, biomedicine and environmental studies. Nova Science Publishers, Hauppage, NY.
22. Bennett-Lovsey RM, Herbert AD, Sternberg MJ, Kelley LA. 2008. Exploring the extremes of sequence/structure space with ensemble fold recognition in the program Phyre. Proteins 70:611-625. http://dx.doi.org/10 .1002/prot.21688.
23. Iakoucheva LM, Dunker AK. 2003. Order, disorder, and flexibility: prediction from protein sequence. Structure 11:1316-1317. http://dx.doi.org /10.1016/j.str.2003.10.009.
24. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A. 2012. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647-1649. http://dx.doi.org/10.1093 /bioinformatics/bts199.
25. Singh KV, Coque TM, Weinstock GM, Murray BE. 1998. In vivo testing of an Enterococcus faecalis efaA mutant and use of efaA homologs for species identification. FEMS Immunol Med Microbiol 21:323-331. http: //dx.doi.org/10.1016/S0928-8244(98)00087-X.
26. Barbu EM, Ganesh VK, Gurusiddappa S, Mackenzie RC, Foster TJ, Sudhof TC, Hook M. 2010. Beta-neurexin is a ligand for the Staphylococcus aureus MSCRAMM SdrC. PLoS Pathog 6:e1000726. http://dx.doi .org/10.1371/journal.ppat.1000726.
27. Wilkins MR, Gasteiger E, Bairoch A, Sanchez JC, Williams KL, Appel RD, Hochstrasser DF. 1999. Protein identification and analysis tools in the ExPASy server. Methods Mol Biol 112:531-552.
28. Singh KV, Nallapareddy SR, Sillanpaa J, Murray BE. 2010. Importance of the collagen adhesin ace in pathogenesis and protection against Enterococcus faecalis experimental endocarditis. PLoS Pathog 6:e1000716. http: //dx.doi.org/10.1371/journal.ppat.1000716.
29. Nallapareddy SR, Qin X, Weinstock GM, Hook M, Murray BE. 2000. Enterococcus faecalis adhesin, ace, mediates attachment to extracellular matrix proteins collagen type IV and laminin as well as collagen type I. Infect Immun 68:5218-5224. http://dx.doi.org/10.1128/IAI.68.9.5218 -5224.2000.
30. Gao P, Pinkston KL, Nallapareddy SR, van Hoof A, Murray BE, Harvey BR. 2010. Enterococcus faecalis rnjB is required for pilin gene expression and biofilm formation. J Bacteriol 192:5489-5498. http://dx.doi.org/10 .1128/JB.00725-10.
31. Mandlik A, Das A, Ton-That H. 2008. The molecular switch that activates the cell wall anchoring step of pilus assembly in gram-positive bacteria. Proc Natl Acad Sci U S A 105:14147-14152. http://dx.doi.org/10 .1073/pnas.0806350105.
32. Nallapareddy SR, Weinstock GM, Murray BE. 2003. Clinical isolates of Enterococcus faecium exhibit strain-specific collagen binding mediated by Acm, a new member of the MSCRAMM family. Mol Microbiol 47: 1733-1747. http://dx.doi.org/10.1046/j.1365-2958.2003.03417.x.
33. Nallapareddy SR, Singh KV, Okhuysen PC, Murray BE. 2008. A functional collagen adhesin gene, acm, in clinical isolates of Enterococcus faecium correlates with the recent success of this emerging nosocomial pathogen. Infect Immun 76:4110-4119. http://dx.doi.org/10.1128/IAI .00375-08.
34. Panesso D, Montealegre MC, Rincon S, Mojica MF, Rice LB, Singh KV, Murray BE, Arias CA. 2011. The hylEfm gene in pHylEfm of Enterococcus faecium is not required in pathogenesis of murine peritonitis. BMC Microbiol 11:20. http://dx.doi.org/10.1186/1471-2180-11-20.
35. Teng F, Nannini EC, Murray BE. 2005. Importance of gls24 in virulence and stress response of Enterococcus faecalis and use of the Gls24 protein as a possible immunotherapy target. J Infect Dis 191:472-480. http://dx.doi .org/10.1086/427191.
36. Dutka-Malen S, Evers S, Courvalin P. 1995. Detection of glycopeptide resistance genotypes and identification to the species level of clinically relevant enterococci by PCR. J Clin Microbiol 33:1434.
37. Qin X, Galloway-Pena JR, Sillanpaa J, Roh JH, Nallapareddy SR, Chowdhury S, Bourgogne A, Choudhury T, Muzny DM, Buhay CJ, Ding Y, Dugan-Rocha S, Liu W, Kovar C, Sodergren E, Highlander S, Petrosino JF, Worley KC, Gibbs RA, Weinstock GM, Murray BE. 2012. Complete genome sequence of Enterococcus faecium strain TX16 and comparative genomic analysis of Enterococcus faecium genomes. BMC Microbiol 12:135. http://dx.doi.org/10.1186/1471-2180-12-135.
38. Vahling CM, McIver KS. 2006. Domains required for transcriptional activation show conservation in the mga family of virulence gene regulators J Bacteriol 188:863-873. http://dx.doi.org/10.1128/JB.188.3.863-873 .2006.
39. Nikolskaya AN, Galperin MY. 2002. A novel type of conserved DNAbinding domain in the transcriptional regulators of the AlgR/AgrA/LytR family. Nucleic Acids Res 30:2453-2459. http://dx.doi.org/10.1093/nar/30 .11.2453.
40. Galloway-Pena JR, Rice LB, Murray BE. 2011. Analysis of PBP5 of early U.S. isolates of Enterococcus faecium: sequence variation alone does not explain increasing ampicillin resistance over time. Antimicrob Agents Chemother 55:3272-3277. http://dx.doi.org/10.1128/AAC.00099-11.
41. Sillanpaa J, Prakash VP, Nallapareddy SR, Murray BE. 2009. Distribution of genes encoding MSCRAMMs and pili in clinical and natural populations of Enterococcus faecium. J Clin Microbiol 47:896-901. http://dx .doi.org/10.1128/JCM.02283-08.
42. Foster TJ, Geoghegan JA, Ganesh VK, Hook M. 2014. Adhesion, invasion and evasion: the many functions of the surface proteins of Staphylococcus aureus. Nat Rev Microbiol 12:49-62. http://dx.doi.org/10.1038 /nrmicro3161.
43. Kim JH, Singvall J, Schwarz-Linek U, Johnson BJ, Potts JR, Hook M. 2004. BBK32, a fibronectin binding MSCRAMM from Borrelia burgdorferi, contains a disordered region that undergoes a conformational change on ligand binding. J Biol Chem 279:41706-41714. http://dx.doi.org/10.1074/jbc.M401691200.
44. Milani A, Vecchietti D, Rusmini R, Bertoni G. 2012. TgpA, a protein with a eukaryotic-like transglutaminase domain, plays a critical role in the viability of Pseudomonas aeruginosa. PLoS One 7:e50323. http://dx.doi .org/10.1371/journal.pone.0050323.
45. Crennell S, Garman E, Laver G, Vimr E, Taylor G. 1994. Crystal structure of Vibrio cholerae neuraminidase reveals dual lectin-like domains in addition to the catalytic domain. Structure 2:535-544. http://dx .doi.org/10.1016/S0969-2126(00)00053-8.
46. Wedekind JE, Trame CB, Dorywalska M, Koehl P, Raschke TM, McKee M, FitzGerald D, Collier RJ, McKay DB. 2001. Refined crystallographic structure of Pseudomonas aeruginosa exotoxin A and its implications for the molecular mechanism of toxicity. J Mol Biol 314:823-837. http://dx .doi.org/10.1006/jmbi.2001.5195.
47. Whitmore L, Wallace BA. 2008. Protein secondary structure analyses from circular dichroism spectroscopy: methods and reference databases. Biopolymers 89:392-400. http://dx.doi.org/10.1002/bip.20853.
48. Schwarz-Linek U, Pilka ES, Pickford AR, Kim JH, Hook M, Campbell ID, Potts JR. 2004. High affinity streptococcal binding to human fibronectin requires specific recognition of sequential F1 modules. J Biol Chem 279:39017-39025. http://dx.doi.org/10.1074/jbc.M405083200.
49. Sillanpaa J, Nallapareddy SR, Houston J, Ganesh VK, Bourgogne A, Singh KV, Murray BE, Hook M. 2009. A family of fibrinogen-binding MSCRAMMs from Enterococcus faecalis. Microbiology 155:2390-2400. http://dx.doi.org/10.1099/mic.0.027821-0.
50. Bron PA, Molenaar D, de Vos WM, Kleerebezem M. 2006. DNA micro-array-based identification of bile-responsive genes in Lactobacillus plantarum. J Appl Microbiol 100:728-738. http://dx.doi.org/10.1111/j .1365-2672.2006.02891.x.
51. Pieterse B, Leer RJ, Schuren FH, van der Werf MJ. 2005. Unravelling the multiple effects of lactic acid stress on Lactobacillus plantarum by transcription profiling. Microbiology 151:3881-3894. http://dx.doi.org/10 .1099/mic.0.28304-0.
52. Kielhofner MA, Hamill RJ. 1989. Role of adherence in infective endocarditis. Tex Heart Inst J 16:239-249.
53. Angrist AA, Oka M. 1963. Pathogenesis of bacterial endocarditis. JAMA 183:249-252.
54. Hamill RJ. 1987. Role of fibronectin in infective endocarditis. Rev Infect Dis 9(Suppl 4):S360-S371. http://dx.doi.org/10.1093/clinids/9.Supplement_4.S360.
55. Mostafavi-Pour Z, Askari JA, Whittard JD, Humphries MJ. 2001. Identification of a novel heparin-binding site in the alternatively spliced IIICS region of fibronectin: roles of integrins and proteoglycans in cell adhesion to fibronectin splice variants. Matrix Biol 20:63-73. http://dx.doi.org/10 .1016/S0945-053X(00)00131-1.
56. Foster TJ, Hook M. 1998. Surface protein adhesins of Staphylococcus aureus. Trends Microbiol 6:484-488. http://dx.doi.org/10.1016/S0966 -842X(98)01400-0.
57. Probert WS, Johnson BJ. 1998. Identification of a 47 kDa fibronectinbinding protein expressed by Borrelia burgdorferi isolate B31. Mol Microbiol 30:1003-1015. http://dx.doi.org/10.1046/j.1365-2958.1998.01127.x.
58. Schwarz-Linek U, Hook M, Potts JR. 2006. Fibronectin-binding proteins of gram-positive cocci. Microbes Infect 8:2291-2298. http://dx.doi.org/10 .1016/j.micinf.2006.03.011.
59. Dabo SM, Confer AW, Anderson BE, Gupta S. 2006. Bartonella henselae Pap31, an extracellular matrix adhesin, binds the fibronectin repeat III13 module. Infect Immun 74:2513-2521. http://dx.doi.org/10.1128/IAI.74.5 .2513-2521.2006.
60. Gaultney RA, Gonzalez T, Floden AM, Brissette CA. 2013. BB0347, from the Lyme disease spirochete Borrelia burgdorferi, is surface exposed and interacts with the CS1 heparin-binding domain of human fibronectin. PLoS One 8:e75643. http://dx.doi.org/10.1371/journal.pone.0075643.
61. Kingsley RA, Keestra AM, de Zoete MR, Baumler AJ. 2004. The ShdA adhesin binds to the cationic cradle of the fibronectin 13FnIII repeat module: evidence for molecular mimicry of heparin binding. Mol Microbiol 52:345-355. http://dx.doi.org/10.1111/j.1365-2958.2004.03995.x.
62. Kuo CJ, Bell H, Hsieh CL, Ptak CP, Chang YF. 2012. Novel mycobacteria antigen 85 complex binding motif on fibronectin. J Biol Chem 287: 1892-1902. http://dx.doi.org/10.1074/jbc.M111.298687.