The group B streptococcal serine-rich repeat 1 glycoprotein mediates penetration of the blood-brain barrier

Journal of Infectious Diseases

Volumn 199, Issue 10, 2009, Pages 1479-1487

  Sorge, Nina M Van ^a   Quach, Darin ^c   Gurney, Michael A ^c   Sullam, Paul M ^d,e   Nizet, Victor ^a,b   Doran, Kelly S ^a,c  

^a Department of Pediatrics ^*  (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c SAN DIEGO STATE UNIVERSITY   (United States)

^d VETERANS AFFAIRS MEDICAL CENTER   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; GLYCOPROTEIN; GROUP B STREPTOCOCCAL SERINE RICH REPEAT 1 GLYCOPROTEIN; GROUP B STREPTOCOCCAL SERINE RICH REPEAT 2 GLYCOPROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL SURVIVAL; BACTERIUM ADHERENCE; BACTERIUM ISOLATE; BACTERIUM MUTANT; BLOOD BRAIN BARRIER; CELL INVASION; CONTROLLED STUDY; ENDOTHELIUM CELL; EXPERIMENTAL MODEL; GROUP B STREPTOCOCCAL MENINGITIS; HUMAN; HUMAN CELL; INDEL MUTATION; MALE; MOLECULAR WEIGHT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SEROTYPE; STRAIN DIFFERENCE; STREPTOCOCCUS AGALACTIAE; VASCULAR ENDOTHELIUM; WILD TYPE;

ADHESINS, BACTERIAL; ANIMALS; BLINDNESS; BLOOD-BRAIN BARRIER; CEREBRAL PALSY; COGNITION DISORDERS; DEAFNESS; DISEASE MODELS, ANIMAL; DNA PRIMERS; HUMANS; INFANT, NEWBORN; MENINGITIS, BACTERIAL; MICE; MUTAGENESIS; POLYMERASE CHAIN REACTION; SEIZURES; SEROTYPING; STREPTOCOCCAL INFECTIONS; STREPTOCOCCUS AGALACTIAE; VIRULENCE;

EID: 65549095152     PISSN: 00221899     EISSN: None     Source Type: Journal    
DOI: 10.1086/598217     Document Type: Article

References (48)

1. Doran KS, Nizet V. Molecular pathogenesis of neonatal group B streptococcal infection: no longer in its infancy. Mol Microbiol 2004; 54:23-31.
2. Edwards MS, Rench MA, Haffar AA, Murphy MA, Desmond MM, Baker CJ. Long-term sequelae of group B streptococcal meningitis in infants. J Pediatr 1985; 106:717-22.
3. Stins MF, Prasadarao NV, Ibric L, Wass CA, Luckett P, Kim KS. Binding characteristics of S fimbriated Escherichia coli to isolated brain microvascular endothelial cells. Am J Pathol 1994; 145:1228-36.
4. Stins MF, Prasadarao NV, Zhou J, Arditi M, Kim KS. Bovine brain microvascular endothelial cells transfected with SV40-large T antigen: development of an immortalized cell line to study pathophysiology of CNS disease. In Vitro Cell Dev Biol Anim 1997; 33:243-7.
5. Doran KS, Engelson EJ, Khosravi A, et al. Blood-brain barrier invasion by group B Streptococcus depends upon proper cell-surface anchoring of lipoteichoic acid. J Clin Invest 2005; 115:2499-507.
6. Maisey HC, Hensler M, Nizet V, Doran KS. Group B streptococcal pilus proteins contribute to adherence to and invasion of brain microvascular endothelial cells. J Bacteriol 2007; 189:1464-7.
7. Prasadarao NV, Wass CA, Weiser JN, Stins MF, Huang SH, Kim KS. Outer membrane protein A of Escherichia coli contributes to invasion of brain microvascular endothelial cells. Infect Immun 1996; 64:146-53.
8. Ring A, Weiser JN, Tuomanen EI. Pneumococcal trafficking across the blood-brain barrier: molecular analysis of a novel bidirectional pathway. J Clin Invest 1998; 102:347-60.
9. Tenenbaum T, Spellerberg B, Adam R, Vogel M, Kim KS, Schroten H. Streptococcus agalactiae invasion of human brain microvascular endothelial cells is promoted by the laminin-binding protein Lmb. Microbes Infect 2007; 9:714-20.
10. Turner DP, Marietou AG, Johnston L, et al. Characterization of MspA, an immunogenic autotransporter protein that mediates adhesion to epithelial and endothelial cells in Neisseria meningitidis. Infect Immun 2006; 74:2957-64.
11. Nizet V, Kim KS, Stins M, et al. Invasion of brain microvascular endothelial cells by group B streptococci. Infect Immun 1997; 65:5074-81.
12. Doran KS, Liu GY, Nizet V. Group B streptococcal -hemolysin/cytolysin activates neutrophil signaling pathways in brain endothelium and contributes to development of meningitis. J Clin Invest 2003; 112:736-44.
13. Bensing BA, Takamatsu D, Sullam PM. Determinants of the streptococcal surface glycoprotein GspB that facilitate export by the accessory Sec system. Mol Microbiol 2005; 58:1468-81.
14. Samen U, Eikmanns BJ, Reinscheid DJ, Borges F. The surface protein Srr-1 of Streptococcus agalactiae binds human keratin 4 and promotes adherence to epithelial HEp-2 cells. Infect Immun 2007; 75:5405-14.
15. Siboo IR, Chambers HF, Sullam PM. Role of SraP, a serine-rich surface protein of Staphylococcus aureus, in binding to human platelets. Infect Immun 2005; 73:2273-80.
16. Stinson MW, Alder S, Kumar S. Invasion and killing of human endothelial cells by viridans group streptococci. Infect Immun 2003; 71:2365-72.
17. Seifert KN, Adderson EE, Whiting AA, Bohnsack JF, Crowley PJ, Brady LJ. A unique serine-rich repeat protein (Srr-2) and novel surface antigen (epsilon) associated with a virulent lineage of serotype III Streptococcus agalactiae. Microbiology 2006; 152:1029-40.
18. Phares CR, Lynfield R, Farley MM, et al. Epidemiology of invasive group B streptococcal disease in the United States, 1999-2005. JAMA 2008; 299:2056-65.
19. Wilkinson HW. Nontypable group B streptococci isolated from human sources. J Clin Microbiol 1977; 6:183-4.
20. Wilson CB, Weaver WM. Comparative susceptibility of group B streptococci and Staphylococcus aureus to killing by oxygen metabolites. J Infect Dis 1985; 152:323-9.
21. Wessels MR, Paoletti LC, Rodewald AK, et al. Stimulation of protective antibodies against type Ia and Ib group B streptococci by a type Ia polysaccharide-tetanus toxoid conjugate vaccine. Infect Immun 1993; 61:4760-6.
22. Lancefield RC, McCarty M, Everly WN. Multiple mouse-protective antibodies directed against group B streptococci: special reference to antibodies effective against protein antigens. J Exp Med 1975; 142:165-79.
23. Sullam PM, Valone FH, Mills J. Mechanisms of platelet aggregation by viridans group streptococci. Infect Immun 1987; 55:1743-50.
24. Kim KS. Escherichia coli translocation at the blood-brain barrier. Infect Immun 2001; 69:5217-22.
25. Pritzlaff CA, Chang JC, Kuo SP, Tamura GS, Rubens CE, Nizet V. Genetic basis for the beta-haemolytic/cytolytic activity of group B Streptococcus. Mol Microbiol 2001; 39:236-47.
26. Jeng A, Sakota V, Li Z, Datta V, Beall B, Nizet V. Molecular genetic analysis of a group A Streptococcus operon encoding serum opacity factor and a novel fibronectin-binding protein, SfbX. J Bacteriol 2003; 185: 1208-17.
27. Maguin E, Duwat P, Hege T, Ehrlich D, Gruss A. New thermosensitive plasmid for gram-positive bacteria. J Bacteriol 1992; 174:5633-8.
28. Bensing BA, Sullam PM. An accessory sec locus of Streptococcus gordonii is required for export of the surface protein GspB and for normal levels of binding to human platelets. Mol Microbiol 2002; 44:1081-94.
29. Takamatsu D, Bensing BA, Sullam PM. Four proteins encoded in the gspB-secY2A2 operon of Streptococcus gordonii mediate the intracellular glycosylation of the platelet-binding protein GspB. J Bacteriol 2004; 186: 7100-11.
30. Tettelin H, Masignani V, Cieslewicz MJ, et al. Complete genome sequence and comparative genomic analysis of an emerging human pathogen, serotype V Streptococcus agalactiae. Proc Natl Acad Sci U S A 2002; 99:12391-6.
31. Takamatsu D, Bensing BA, Sullam PM. Genes in the accessory sec locus of Streptococcus gordonii have three functionally distinct effects on the expression of the platelet-binding protein GspB. Mol Microbiol 2004; 52:189-203.
32. Obert C, Sublett J, Kaushal D, et al. Identification of a candidate Streptococcus pneumoniae core genome and regions of diversity correlated with invasive pneumococcal disease. Infect Immun 2006; 74:4766-77.
33. Wu H, Mintz KP, Ladha M. Fives-Taylor PM. Isolation and characterization of Fap1, a fimbriae-associated adhesin of Streptococcus parasanguis FW213. Mol Microbiol 1998; 28:487-500.
34. Bensing BA, Gibson BW, Sullam PM. The Streptococcus gordonii platelet binding protein GspB undergoes glycosylation independently of export. J Bacteriol 2004; 186:638-45.
35. Petersdorf RG, Swarner DR, Garcia M. Studies on the pathogenesis of meningitis. II. Development of meningitis during pneumococcal bacteremia. J Clin Invest 1962; 41:320-7.
36. Bell LM, Alpert G, Campos JM, Plotkin SA. Routine quantitative blood cultures in children with Haemophilus influenzae or Streptococcus pneumoniae bacteremia. Pediatrics 1985; 76:901-4.
37. Dietzman DE, Fischer GW, Schoenknecht FD. Neonatal Escherichia coli septicemia-bacterial counts in blood. J Pediatr 1974; 85:128-30.
38. Kim KS. Pathogenesis of bacterial meningitis: from bacteraemia to neuronal injury. Nat Rev Neurosci 2003; 4:376-85.
39. Tenenbaum T, Bloier C, Adam R, Reinscheid DJ, Schroten H. Adherence to and invasion of human brain microvascular endothelial cells are promoted by fibrinogen-binding protein FbsA of Streptococcus agalactiae. Infect Immun 2005; 73:4404-9.
40. Takahashi Y, Konishi K, Cisar JO, Yoshikawa M. Identification and characterization of hsa, the gene encoding the sialic acid-binding adhesin of Streptococcus gordonii DL1. Infect Immun 2002; 70:1209-18.
41. Chen Q, Wu H, Fives-Taylor PM. Investigating the role of secA2 in secretion and glycosylation of a fimbrial adhesin in Streptococcus parasanguis FW213. Mol Microbiol 2004; 53:843-56.
42. Bensing BA, Lopez JA, Sullam PM. The Streptococcus gordonii surface proteins GspB and Hsa mediate binding to sialylated carbohydrate epitopes on the platelet membrane glycoprotein Ibalpha. Infect Immun 2004; 72:6528-37.
43. Stephenson AE, Wu H, Novak J, Tomana M, Mintz K, Fives-Taylor P. The Fap1 fimbrial adhesin is a glycoprotein: antibodies specific for the glycan moiety block the adhesion of Streptococcus parasanguis in an in vitro tooth model. Mol Microbiol 2002; 43:147-57.
44. Takamatsu D, Bensing BA, Cheng H, et al. Binding of the Streptococcus gordonii surface glycoproteins GspB and Hsa to specific carbohydrate structures on platelet membrane glycoprotein Ibalpha. Mol Microbiol 2005; 58:380-92.
45. Rose L, Shivshankar P, Hinojosa E, Rodriguez A, Sanchez CJ, Orihuela CJ. Antibodies against PsrP, a novel Streptococcus pneumoniae adhesin, block adhesion and protect mice against pneumococcal challenge. J Infect Dis 2008; 198:375-83.
46. Winram SB, Jonas M, Chi E, Rubens CE. Characterization of group B streptococcal invasion of human chorion and amnion epithelial cells in vitro. Infect Immun 1998; 66:4932-41.
47. Doran KS, Chang JC, Benoit VM, Eckmann L, Nizet V. Group B streptococcal beta-hemolysin/cytolysin promotes invasion of human lung epithelial cells and the release of interleukin-8. J Infect Dis 2002; 185: 196-203.
48. Stins MF, Nemani PV, Wass C, Kim KS. Escherichia coli binding to and invasion of brain microvascular endothelial cells derived from humans and rats of different ages. Infect Immun 1999; 67:5522-5.