Identification of a group B streptococcal fibronectin binding protein, SfbA, that contributes to invasion of brain endothelium and development of meningitis

Infection and Immunity

Volumn 82, Issue 6, 2014, Pages 2276-2286

  Mu, Rong ^a   Kim, Brandon J ^a   Paco, Czarinah ^a   Del Rosario, Yvette ^a   Courtney, Harry S ^b   Doran, Kelly S ^a,c  

^a SAN DIEGO STATE UNIVERSITY   (United States)

^b UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGINYLGLYCYLASPARTIC ACID; BACTERIAL PROTEIN; CELL SURFACE PROTEIN; FIBRONECTIN BINDING PROTEIN; INTEGRIN; INTERLEUKIN 8; STREPTOCOCCAL FIBRONECTIN BINDING PROTEIN A; UNCLASSIFIED DRUG; ADHESIN; FIBRONECTIN-BINDING PROTEINS, BACTERIAL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL GROWTH; BACTERIAL LOAD; BLOOD BRAIN BARRIER; COLONY FORMING UNIT; CONTROLLED STUDY; GROUP B STREPTOCOCCAL MENINGITIS; HOST CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LACTOCOCCUS LACTIS; MICROVASCULAR ENDOTHELIAL CELL; MOUSE; MUTAGENESIS; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; SEROTYPE; ANIMAL; BACTERIAL COUNT; BACTERIUM ADHERENCE; BRAIN; CELL LINE; DISEASE MODEL; ENDOTHELIUM CELL; GENE EXPRESSION REGULATION; MENINGITIS, BACTERIAL; METABOLISM; MICROBIOLOGY; MUTATION; PATHOGENICITY; PATHOPHYSIOLOGY; PHYSIOLOGY; STREPTOCOCCUS AGALACTIAE; STREPTOCOCCUS INFECTION; VASCULAR ENDOTHELIUM;

ADHESINS, BACTERIAL; ANIMALS; BACTERIAL ADHESION; BRAIN; CELL LINE; COLONY COUNT, MICROBIAL; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; GENE EXPRESSION REGULATION, BACTERIAL; INTEGRINS; MENINGITIS, BACTERIAL; MICE; MUTATION; STREPTOCOCCAL INFECTIONS; STREPTOCOCCUS AGALACTIAE;

EID: 84900433355     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01559-13     Document Type: Article

References (71)

1. Maisey HC, Doran KS, Nizet V. 2008. Recent advances in understanding the molecular basis of group B Streptococcus virulence. Expert Rev. Mol. Med. 10:e27. http://dx.doi.org/10.1017/S1462399408000811.
2. Brouwer MC, Tunkel AR, van de Beek D. 2010. Epidemiology, diagnosis, and antimicrobial treatment of acute bacterial meningitis. Clin. Microbiol. Rev. 23:467-492. http://dx.doi.org/10.1128/CMR.00070-09.
3. Thigpen MC, Whitney CG, Messonnier NE, Zell ER, Lynfield R, Hadler JL, Harrison LH, Farley MM, Reingold A, Bennett NM, Craig AS, Schaffner W, Thomas A, Lewis MM, Scallan E, Schuchat A. 2011. Bacterial meningitis in the United States, 1998-2007. N. Engl. J. Med. 364:2016-2025. http://dx.doi.org/10.1056/NEJMoa1005384.
4. Betz AL. 1985. Epithelial properties of brain capillary endothelium. Fed. Proc. 44:2614-2615.
5. Betz AL. 1992. An overview of the multiple functions of the blood-brain barrier. NIDA Res. Monogr. 120:54-72.
6. Abbott NJ, Patabendige AA, Dolman DE, Yusof SR, Begley DJ. 2010. Structure and function of the blood-brain barrier. Neurobiol. Dis. 37:13-25. http://dx.doi.org/10.1016/j.nbd.2009.07.030.
7. van Sorge NM, Doran KS. 2012. Defense at the border: the blood-brain barrier versus bacterial foreigners. Future Microbiol. 7:383-394. http://dx.doi.org/10.2217/fmb.12.1.
8. Kim KS. 2006. Microbial translocation of the blood-brain barrier. Int. J. Parasitol. 36:607-614. http://dx.doi.org/10.1016/j.ijpara.2006.01.013.
9. Doran KS, Liu GY, Nizet V. 2003. Group B streptococcal betahemolysin/cytolysin activates neutrophil signaling pathways in brain en-dothelium and contributes to development of meningitis. J. Clin. Invest. 112:736-744. http://dx.doi.org/10.1172/JCI200317335.
10. Doran KS, Engelson EJ, Khosravi A, Maisey HC, Fedtke I, Equils O, Michelsen KS, Arditi M, Peschel A, Nizet V. 2005. Blood-brain barrier invasion by group B Streptococcus depends upon proper cell-surface anchoring of lipoteichoic acid. J. Clin. Invest. 115:2499-2507. http://dx.doi.org/10.1172/JCI23829.
11. Banerjee A, Kim BJ, Carmona EM, Cutting AS, Gurney MA, Carlos C, Feuer R, Prasadarao NV, Doran KS. 2011. Bacterial pili exploit integrin machinery to promote immune activation and efficient bloodbrain barrier penetration. Nat. Commun. 2:462. http://dx.doi.org/10.1038/ncomms1474.
12. Tazi A, Disson O, Bellais S, Bouaboud A, Dmytruk N, Dramsi S, Mistou MY, Khun H, Mechler C, Tardieux I, Trieu-Cuot P, Lecuit M, Poyart C. 2010. The surface protein HvgA mediates group B streptococcus hypervirulence and meningeal tropism in neonates. J. Exp. Med. 207: 2313-2322. http://dx.doi.org/10.1084/jem.20092594.
13. Seo HS, Mu R, Kim BJ, Doran KS, Sullam PM. 2012. Binding of glycoprotein Srr1 of Streptococcus agalactiae to fibrinogen promotes attachment to brain endothelium and the development of meningitis. PLoS Pathog. 8:e1002947. http://dx.doi.org/10.1371/journal.ppat.1002947.
14. van Sorge NM, Quach D, Gurney MA, Sullam PM, Nizet V, Doran KS. 2009. The group B streptococcal serine-rich repeat 1 glycoprotein mediates penetration of the blood-brain barrier. J. Infect. Dis. 199:1479-1487. http://dx.doi.org/10.1086/598217.
15. Chang YC, Wang Z, Flax LA, Xu D, Esko JD, Nizet V, Baron MJ. 2011. Glycosaminoglycan binding facilitates entry of a bacterial pathogen into central nervous systems. PLoS Pathog. 7:e1002082. http://dx.doi.org/10.1371/journal.ppat.1002082.
16. Ponnuraj K, Bowden MG, Davis S, Gurusiddappa S, Moore D, Choe D, Xu Y, Hook M, Narayana SV. 2003. A "dock, lock, and latch" structural model for a staphylococcal adhesin binding to fibrinogen. Cell 115:217-228. http://dx.doi.org/10.1016/S0092-8674(03)00809-2.
17. Seo HS, Misanov G, Seepersaud R, Doran KS, Dubrovska I, Shuvalova L, Anderson WF, Iverson TM, Sullam PM. 2013. Characterization of fibrinogen binding by glycoproteins Srr1 and Srr2 of Streptococcus agalactiae. J. Biol. Chem. 288:35982-35996. http://dx.doi.org/10.1074/jbc.M113.513358.
18. Schubert A, Zakikhany K, Pietrocola G, Meinke A, Speziale P, Eikmanns BJ, Reinscheid DJ. 2004. The fibrinogen receptor FbsA promotes adherence of Streptococcus agalactiae to human epithelial cells. Infect. Immun. 72:6197-6205. http://dx.doi.org/10.1128/IAI.72.11.6197-6205.2004.
19. Gutekunst H, Eikmanns BJ, Reinscheid DJ. 2004. The novel fibrinogenbinding protein FbsB promotes Streptococcus agalactiae invasion into epithelial cells. Infect. Immun. 72:3495-3504. http://dx.doi.org/10.1128/IAI.72.6.3495-3504.2004.
20. Tenenbaum T, Spellerberg B, Adam R, Vogel M, Kim KS, Schroten H. 2007. Streptococcus agalactiae invasion of human brain microvascular endothelial cells is promoted by the laminin-binding protein Lmb. Microbes Infect. 9:714-720. http://dx.doi.org/10.1016/j.micinf.2007.02.015.
21. Baeten KM, Akassoglou K. 2011. Extracellular matrix and matrix receptors in blood-brain barrier formation and stroke. Dev. Neurobiol. 71: 1018-1039. http://dx.doi.org/10.1002/dneu.20954.
22. Jones TR, Ruoslahti E, Schold SC, Bigner DD. 1982. Fibronectin and glial fibrillary acidic protein expression in normal human brain and anaplastic human gliomas. Cancer Res. 42:168-177.
23. Price J, Hynes RO. 1985. Astrocytes in culture synthesize and secrete a variant form of fibronectin. J. Neurosci. 5:2205-2211.
24. Peters JH, Sporn LA, Ginsberg MH, Wagner DD. 1990. Human endothelial cells synthesize, process, and secrete fibronectin molecules bearing an alternatively spliced type III homology (ED1). Blood 75:1801-1808.
25. Pankov R, Yamada KM. 2002. Fibronectin at a glance. J. Cell Sci. 115: 3861-3863. http://dx.doi.org/10.1242/jcs.00059.
26. Hynes RO. 2002. Integrins: bidirectional, allosteric signaling machines. Cell 110:673-687. http://dx.doi.org/10.1016/S0092-8674(02)00971-6.
27. Espersen F, Clemmensen I. 1982. Isolation of a fibronectin-binding protein from Staphylococcus aureus. Infect. Immun. 37:526-531.
28. Lindgren PE, Speziale P, McGavin M, Monstein HJ, Hook M, Visai L, Kostiainen T, Bozzini S, Lindberg M. 1992. Cloning and expression of two different genes from Streptococcus dysgalactiae encoding fibronectin receptors. J. Biol. Chem. 267:1924-1931.
29. Jeng A, Sakota V, Li Z, Datta V, Beall B, Nizet V. 2003. Molecular genetic analysis of a group A Streptococcus operon encoding serum opacity factor and a novel fibronectin-binding protein, SfbX. J. Bacteriol. 185: 1208-1217. http://dx.doi.org/10.1128/JB.185.4.1208-1217.2003.
30. Terao Y, Okamoto S, Kataoka K, Hamada S, Kawabata S. 2005. Protective immunity against Streptococcus pyogenes challenge in mice after immunization with fibronectin-binding protein. J. Infect. Dis. 192:2081-2091. http://dx.doi.org/10.1086/498162.
31. Terao Y, Kawabata S, Nakata M, Nakagawa I, Hamada S. 2002. Molecular characterization of a novel fibronectin-binding protein of Streptococcus pyogenes strains isolated from toxic shock-like syndrome patients. J. Biol. Chem. 277:47428-47435. http://dx.doi.org/10.1074/jbc.M209133200.
32. Kreikemeyer B, Oehmcke S, Nakata M, Hoffrogge R, Podbielski A. 2004. Streptococcus pyogenes fibronectin-binding protein F2: expression profile, binding characteristics, and impact on eukaryotic cell interactions. J. Biol. Chem. 279:15850-15859. http://dx.doi.org/10.1074/jbc.M313613200.
33. Hanski E, Caparon M. 1992. Protein F, a fibronectin-binding protein, is an adhesin of the group A streptococcus Streptococcus pyogenes. Proc. Natl. Acad. Sci. U. S. A. 89:6172-6176. http://dx.doi.org/10.1073/pnas.89.13.6172.
34. Holmes AR, McNab R, Millsap KW, Rohde M, Hammerschmidt S, Mawdsley JL, Jenkinson HF. 2001. The pavA gene of Streptococcus pneumoniae encodes a fibronectin-binding protein that is essential for virulence. Mol. Microbiol. 41:1395-1408. http://dx.doi.org/10.1046/j.1365-2958.2001.02610.x.
35. Torelli R, Serror P, Bugli F, Paroni Sterbini F, Florio AR, Stringaro A, Colone M, De Carolis E, Martini C, Giard JC, Sanguinetti M, Posteraro B. 2012. The PavA-like fibronectin-binding protein of Enterococcus faecalis, EfbA, is important for virulence in a mouse model of ascending urinary tract infection. J. Infect. Dis. 206:952-960. http://dx.doi.org/10.1093/infdis/jis440.
36. Courtney HS, Dale JB, Hasty DI. 1996. Differential effects of the streptococcal fibronectin-binding protein, FBP54, on adhesion of group A streptococci to human buccal cells and HEp-2 tissue culture cells. Infect. Immun. 64:2415-2419.
37. Christie J, McNab R, Jenkinson HF. 2002. Expression of fibronectinbinding protein FbpA modulates adhesion in Streptococcus gordonii. Microbiology 148:1615-1625.
38. Simon D, Ferretti JJ. 1991. Electrotransformation of Streptococcus pyogenes with plasmid and linear DNA. FEMS Microbiol. Lett. 66:219-224.
39. Kuipers OP, de Ruyter PGGA, Kleerebezem M, de Vos WM. 1998. Quorum sensing-controlled gene expression in lactic acid bacteria. J. Biotechnol. 64:15-21. http://dx.doi.org/10.1016/S0168-1656(98)00100-X.
40. Wilson CB, Weaver WM. 1985. Comparative susceptibility of group B streptococci and Staphylococcus aureus to killing by oxygen metabolites. J. Infect. Dis. 152:323-329. http://dx.doi.org/10.1093/infdis/152.2.323.
41. Maisey HC, Hensler M, Nizet V, Doran KS. 2007. Group B streptococcal pilus proteins contribute to adherence to and invasion of brain microvascular endothelial cells. J. Bacteriol. 189:1464-1467. http://dx.doi.org/10.1128/JB.01153-06.
42. Pritzlaff CA, Chang JC, Kuo SP, Tamura GS, Rubens CE, Nizet V. 2001. Genetic basis for the beta-haemolytic/cytolytic activity of group B Streptococcus. Mol. Microbiol. 39:236-247. http://dx.doi.org/10.1046/j.1365-2958.2001.02211.x.
43. Woodcock DM, Crowther PJ, Doherty J, Jefferson S, DeCruz E, Noyer-Weidner M, Smith SS, Michael MZ, Graham MW. 1989. Quantitative evaluation of Escherichia coli host strains for tolerance to cytosine methylation in plasmid and phage recombinants. Nucleic Acids Res. 17:3469-3478. http://dx.doi.org/10.1093/nar/17.9.3469.
44. Lancefield RC. 1938. Two serological types of group B hemolytic streptococci with related, but not identical, type-specific substances. J. Exp. Med. 67:25-40. http://dx.doi.org/10.1084/jem.67.1.25.
45. Wessels MR, Paoletti LC, Rodewald AK, Michon F, DiFabio J, Jennings HJ, Kasper DL. 1993. Stimulation of protective antibodies against type Ia and Ib group B streptococci by a type Ia polysaccharide-tetanus toxoid conjugate vaccine. Infect. Immun. 61:4760-4766.
46. Madoff LC, Michel JL, Kasper DL. 1991. A monoclonal antibody identifies a protective C-protein alpha-antigen epitope in group B streptococci. Infect. Immun. 59:204-210.
47. Glaser P, Rusniok C, Buchrieser C, Chevalier F, Frangeul L, Msadek T, Zouine M, Couve E, Lalioui L, Poyart C, Trieu-Cuot P, Kunst F. 2002. Genome sequence of Streptococcus agalactiae, a pathogen causing invasive neonatal disease. Mol. Microbiol. 45:1499-1513. http://dx.doi.org/10.1046/j.1365-2958.2002.03126.x.
48. Fichorova RN, Rheinwald JG, Anderson DJ. 1997. Generation of papillomavirus-immortalized cell lines from normal human ectocervical, endocervical, and vaginal epithelium that maintain expression of tissuespecific differentiation proteins. Biol. Reprod. 57:847-855. http://dx.doi.org/10.1095/biolreprod57.4.847.
49. Patras KA, Wang NY, Fletcher EM, Cavaco CK, Jimenez A, Garg M, Fierer J, Sheen TR, Rajagopal L, Doran KS. 2013. Group B Streptococcus CovR regulation modulates host immune signalling pathways to promote vaginal colonization. Cell. Microbiol. 15:1154-1167. http://dx.doi.org/10.1111/cmi.12105.
50. Courtney HS, Li Y, Dale JB, Hasty DL. 1994. Cloning, sequencing, and expression of a fibronectin/fibrinogen-binding protein from group A streptococci. Infect. Immun. 62:3937-3946.
51. Butler KM, Baker CJ, Edwards MS. 1987. Interaction of soluble fibronectin with group B streptococci. Infect. Immun. 55:2404-2408.
52. Tamura GS, Rubens CE. 1995. Group B streptococci adhere to a variant of fibronectin attached to a solid phase. Mol. Microbiol. 15:581-589. http://dx.doi.org/10.1111/j.1365-2958.1995.tb02271.x.
53. Lamy MC, Dramsi S, Billoet A, Reglier-Poupet H, Tazi A, Raymond J, Guerin F, Couve E, Kunst F, Glaser P, Trieu-Cuot P, Poyart C. 2006. Rapid detection of the "highly virulent" group B Streptococcus ST-17 clone. Microbes Infect. 8:1714-1722. http://dx.doi.org/10.1016/j.micinf.2006.02.008.
54. Terao Y, Kawabata S, Kunitomo E, Murakami J, Nakagawa I, Hamada S. 2001. Fba, a novel fibronectin-binding protein from Streptococcus pyogenes, promotes bacterial entry into epithelial cells, and the fba gene is positively transcribed under the Mga regulator. Mol. Microbiol. 42:75-86. http://dx.doi.org/10.1046/j.1365-2958.2001.02579.x.
55. Takagi J, Strokovich K, Springer TA, Walz T. 2003. Structure of integrin alpha5beta1 in complex with fibronectin. EMBO J. 22:4607-4615. http://dx.doi.org/10.1093/emboj/cdg445.
56. Pilorget A, Conesa M, Sarray S, Michaud-Levesque J, Daoud S, Kim KS, Demeule M, Marvaldi J, El Ayeb M, Marrakchi N, Beliveau R, Luis J. 2007. Lebectin, a Macrovipera lebetina venom-derived C-type lectin, inhibits angiogenesis both in vitro and in vivo. J. Cell. Physiol. 211:307-315. http://dx.doi.org/10.1002/jcp.20935.
57. Nizet V, Kim KS, Stins M, Jonas M, Chi EY, Nguyen D, Rubens CE. 1997. Invasion of brain microvascular endothelial cells by group B streptococci. Infect. Immun. 65:5074-5081.
58. Walia B, Castaneda FE, Wang L, Kolachala VL, Bajaj R, Roman J, Merlin D, Gewirtz AT, Sitaraman SV. 2004. Polarized fibronectin secretion induced by adenosine regulates bacterial-epithelial interaction in human intestinal epithelial cells. Biochem. J. 382:589-596. http://dx.doi.org/10.1042/BJ20040021.
59. Beckmann C, Waggoner JD, Harris TO, Tamura GS, Rubens CE. 2002. Identification of novel adhesins from Group B streptococci by use of phage display reveals that C5a peptidase mediates fibronectin binding. Infect. Immun. 70:2869-2876. http://dx.doi.org/10.1128/IAI.70.6.2869-2876.2002.
60. Lalioui L, Pellegrini E, Dramsi S, Baptista M, Bourgeois N, Doucet-Populaire F, Rusniok C, Zouine M, Glaser P, Kunst F, Poyart C, Trieu-Cuot P. 2005. The SrtA Sortase of Streptococcus agalactiae is required for cell wall anchoring of proteins containing the LPXTG motif, for adhesion to epithelial cells, and for colonization of the mouse intestine. Infect. Immun. 73:3342-3350. http://dx.doi.org/10.1128/IAI.73.6.3342-3350.2005.
61. Krishnan V, Dwivedi P, Kim BJ, Samal A, Macon K, Ma X, Mishra A, Doran KS, Ton-That H, Narayana SV. 2013. Structure of Streptococcus agalactiae tip pilin GBS104: a model for GBS pili assembly and host interactions. Acta crystallogr. Biol. Crystallogr. D 69:1073-1089. http://dx.doi.org/10.1107/S0907444913004642.
62. Henderson B, Nair S, Pallas J, Williams MA. 2011. Fibronectin: a multidomain host adhesin targeted by bacterial fibronectin-binding proteins. FEMS Microbiol. Rev. 35:147-200. http://dx.doi.org/10.1111/j.1574-6976.2010.00243.x.
63. Pracht D, Elm C, Gerber J, Bergmann S, Rohde M, Seiler M, Kim KS, Jenkinson HF, Nau R, Hammerschmidt S. 2005. PavA of Streptococcus pneumoniae modulates adherence, invasion, and meningeal inflammation. Infect. Immun. 73:2680-2689. http://dx.doi.org/10.1128/IAI.73.5.2680-2689.2005.
64. Whitnack E, Beachey EH. 1985. Inhibition of complement-mediated opsonization and phagocytosis of Streptococcus pyogenes byDfragments of fibrinogen and fibrin bound to cell surface M protein. J. Exp. Med. 162:1983-1997. http://dx.doi.org/10.1084/jem.162.6.1983.
65. Schubert A, Zakikhany K, Schreiner M, Frank R, Spellerberg B, Eikmanns BJ, Reinscheid DJ. 2002. A fibrinogen receptor from group B Streptococcus interacts with fibrinogen by repetitive units with novel ligand binding sites. Mol. Microbiol. 46:557-569. http://dx.doi.org/10.1046/j.1365-2958.2002.03177.x.
66. Sinha B, Francois PP, Nusse O, Foti M, Hartford OM, Vaudaux P, Foster TJ, Lew DP, Herrmann M, Krause KH. 1999. Fibronectinbinding protein acts as Staphylococcus aureus invasin via fibronectin bridging to integrin alpha5beta1. Cell. Microbiol. 1:101-117. http://dx.doi.org/10.1046/j.1462-5822.1999.00011.x.
67. Jett BD, Gilmore MS. 2002. Internalization of Staphylococcus aureus by human corneal epithelial cells: role of bacterial fibronectin-binding protein and host cell factors. Infect. Immun. 70:4697-4700. http://dx.doi.org/10.1128/IAI.70.8.4697-4700.2002.
68. Unkmeir A, Latsch K, Dietrich G, Wintermeyer E, Schinke B, Schwender S, Kim KS, Eigenthaler M, Frosch M. 2002. Fibronectin mediates Opc-dependent internalization of Neisseria meningitidis in human brain microvascular endothelial cells. Mol. Microbiol. 46:933-946. http://dx.doi.org/10.1046/j.1365-2958.2002.03222.x.
69. Hynes RO. 2007. Cell-matrix adhesion in vascular development. J. Thromb. Haemost. 5(Suppl 1):32-40. http://dx.doi.org/10.1111/j.1538-7836.2007.02569.x.
70. Hynes RO, Naba A. 2012. Overview of the matrisome-an inventory of extracellular matrix constituents and functions. Cold Spring Harb. Perspect. Biol. 4:a004903. http://dx.doi.org/10.1101/cshperspect.a004903.
71. Nizet VDK. 2013. Group B streptococcal meningitis, p 118-132. In Christodoulides M (ed), Meningitis: cellular and molecular basis. CABI, London, United Kingdom.