Defense at the border: The blood-brain barrier versus bacterial foreigners

Future Microbiology

Volumn 7, Issue 3, 2012, Pages 383-394

  Van Sorge, Nina M ^a,b   Doran, Kelly S ^b,c  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c SAN DIEGO STATE UNIVERSITY   (United States)

Author keywords

blood brain barrier; Escherichia coli K1; group B Streptococcus; Haemophilus influenzae type B; meningitis; Neisseria meningitidis; neutrophil; Streptococcus pneumoniae; tight adherens junction

Indexed keywords

CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1; INTERLEUKIN 6; INTERLEUKIN 8; LAMININ RECEPTOR; THROMBOCYTE ACTIVATING FACTOR RECEPTOR; TUMOR NECROSIS FACTOR ALPHA;

BACILLUS ANTHRACIS; BACTERIAL CLEARANCE; BACTERIAL MENINGITIS; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BLOOD BRAIN BARRIER; DISEASE COURSE; ESCHERICHIA COLI; GENE EXPRESSION; HAEMOPHILUS INFLUENZAE TYPE B; HOST PATHOGEN INTERACTION; HUMAN; KLEBSIELLA; LISTERIA MONOCYTOGENES; MEMBRANE PERMEABILITY; MICROVASCULAR ENDOTHELIAL CELL; MYCOBACTERIUM TUBERCULOSIS; NEISSERIA MENINGITIDIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS AGALACTIAE; STREPTOCOCCUS PNEUMONIAE; STREPTOCOCCUS SUIS;

ANIMALS; BACTERIA; BACTERIAL PHYSIOLOGICAL PHENOMENA; BLOOD-BRAIN BARRIER; HOST-PATHOGEN INTERACTIONS; HUMANS; MENINGITIS, BACTERIAL;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; HAEMOPHILUS INFLUENZAE SEROTYPE B; NEISSERIA MENINGITIDIS; STREPTOCOCCUS PNEUMONIAE; STREPTOCOCCUS SP. 'GROUP B';

EID: 84858060614     PISSN: 17460913     EISSN: 17460921     Source Type: Journal    
DOI: 10.2217/fmb.12.1     Document Type: Review

References (169)

1. Baraff LJ, Lee SI, Schriger DL. Outcomes of bacterial meningitis in children: a meta-analysis. Pediatr. Infect. Dis. J. 12(5), 389-394 (1993).
2. Grimwood K, Anderson P, Anderson V, Tan L, Nolan T. Twelve year outcomes following bacterial meningitis: further evidence for persisting effects. Arch. Dis. Child. 83(2), 111-116 (2000).
3. Eskola J, Peltola H, Takala AK et al. Efficacy of Haemophilus influenzae type b polysaccharide-diphtheria toxoid conjugate vaccine in infancy. N. Engl. J. Med. 317(12), 717-722 (1987).
4. Peltola H. Worldwide Haemophilus influenzae type b disease at the beginning of the 21st century: global analysis of the disease burden 25 years after the use of the polysaccharide vaccine and a decade after the advent of conjugates. Clin. Microbiol. Rev. 13(2), 302-317 (2000).
5. Watt JP, Wolfson LJ, O'Brien KL et al. Burden of disease caused by Haemophilus influenzae type b in children younger than 5 years: global estimates. Lancet 374(9693), 903-911 (2009).
6. O'Brien KL, Wolfson LJ, Watt JP et al. Burden of disease caused by Streptococcus pneumoniae in children younger than 5 years: global estimates. Lancet 374(9693), 893-902 (2009).
7. Thigpen MC, Whitney CG, Messonnier NE et al. Bacterial meningitis in the United States, 1998-2007. N. Engl. J. Med. 364(21), 2016-2025 (2011).
8. Kaplan SL, Mason EO Jr, Wald ER et al. Decrease of invasive pneumococcal infections in children among 8 children's hospitals in the United States after the introduction of the 7-valent pneumococcal conjugate vaccine. Pediatrics 113(3 Pt 1), 443-449 (2004).
9. Nakhla I, Frenck RW Jr, Teleb NA et al. The changing epidemiology of meningococcal meningitis after introduction of bivalent A/C polysaccharide vaccine into school-based vaccination programs in Egypt. Vaccine 23(25), 3288-3293 (2005).
10. Gray SJ, Trotter CL, Ramsay ME et al. Epidemiology of meningococcal disease in England and Wales 1993/94 to 2003/04: contribution and experiences of the Meningococcal Reference Unit. J. Med. Microbiol. 55(Pt 7), 887-896 (2006).
11. Molyneux EM, Mankhambo LA, Phiri A et al. The outcome of non-typhoidal Salmonella meningitis in Malawian children, 1997-2006. Ann. Trop. Paediatr. 29(1), 13-22 (2009).
12. Molyneux EM, Walsh AL, Malenga G, Rogerson S, Molyneux ME. Salmonella meningitis in children in Blantyre, Malawi, 1996-1999. Ann. Trop. Paediatr. 20(1), 41-44 (2000).
13. Vaagland H, Blomberg B, Kruger C, Naman N, Jureen R, Langeland N. Nosocomial outbreak of neonatal Salmonella enterica serotype Enteritidis meningitis in a rural hospital in northern Tanzania. BMC Infect. Dis. 4, 35 (2004).
14. Iriso R, Ocakacon R, Acayo JA, Mawanda MA, Kisayke A. Bacterial meningitis following introduction of Hib conjugate vaccine in northern Uganda. Ann. Trop. Paediatr. 28(3), 211-216 (2008).
15. Gordon MA, Graham SM, Walsh AL et al. Epidemics of invasive Salmonella enterica serovar enteritidis and S. enterica serovar Typhimurium infection associated with multidrug resistance among adults and children in Malawi. Clin. Infect. Dis. 46(7), 963-969 (2008).
16. Owusu-Ofori A, Scheld WM. Treatment of Salmonella meningitis: two case reports and a review of the literature. Int. J. Infect. Dis. 7(1), 53-60 (2003).
17. Brouwer MC, Tunkel AR, Van De Beek D. Epidemiology, diagnosis, and antimicrobial treatment of acute bacterial meningitis. Clin. Microbiol. Rev. 23(3), 467-492 (2010).
18. Dawson KG, Emerson JC, Burns JL. Fifteen years of experience with bacterial meningitis. Pediatr. Infect. Dis. J. 18(9), 816-822 (1999).
19. Nigrovic LE, Kuppermann N, Malley R. Children with bacterial meningitis presenting to the emergency department during the pneumococcal conjugate vaccine era. Acad. Emerg. Med. 15(6), 522-528 (2008).
20. Group TWYIS. Bacterial etiology of serious infections in young infants in developing countries: results of a multicenter study. Pediatr. Infect. Dis. J. 18(10 Suppl.), S17-S22 (1999).
21. Zaidi AK, Thaver D, Ali SA, Khan TA. Pathogens associated with sepsis in newborns and young infants in developing countries. Pediatr. Infect. Dis. J. 28(1 Suppl), S10-S18 (2009).
22. Phares CR, Lynfield R, Farley MM et al. Epidemiology of invasive group B streptococcal disease in the United States, 1999-2005. JAMA 299(17), 2056-2065 (2008).
23. Van Dyke MK, Phares CR, Lynfield R et al. Evaluation of universal antenatal screening for group B Streptococcus. N. Engl. J. Med. 360(25), 2626-2636 (2009).
24. Stoll BJ, Hansen N, Fanaroff AA et al. Changes in pathogens causing early-onset sepsis in very-low-birth-weight infants. N. Engl. J. Med. 347(4), 240-247 (2002).
25. Stoll BJ, Hansen NI, Sanchez PJ et al. Early onset neonatal sepsis: the burden of group B Streptococcal and E. coli disease continues. Pediatrics 127(5), 817-826 (2011).
26. Bekondi C, Bernede C, Passone N et al. Primary and opportunistic pathogens associated with meningitis in adults in Bangui, Central African Republic, in relation to human immunodeficiency virus serostatus. Int. J. Infect. Dis. 10(5), 387-395 (2006).
27. Swe KS, Nagel G, Van Der Westhuizen M, Hoosen AA. Salmonella Typhimurium meningitis in an adult patient with AIDS. J. Clin. Pathol. 61(1), 138-139 (2008).
28. Fernandez Guerrero ML, Ramos JM, Nunez A, De Gorgolas M. Focal infections due to non-typhi Salmonella in patients with AIDS: report of 10 cases and review. Clin. Infect. Dis. 25(3), 690-697 (1997).
29. Lun ZR, Wang QP, Chen XG, Li AX, Zhu XQ. Streptococcus suis: an emerging zoonotic pathogen. Lancet Infect. Dis. 7(3), 201-209 (2007).
30. Gottschalk M, Xu J, Calzas C, Segura M. Streptococcus suis: a new emerging or an old neglected zoonotic pathogen? Future Microbiol. 5(3), 371-391 (2010).
31. Aguilar J, Urday-Cornejo V, Donabedian S, Perri M, Tibbetts R, Zervos M. Staphylococcus aureus meningitis: case series and literature review. Medicine 89(2), 117-125 (2010).
32. Pintado V, Meseguer MA, Fortun J et al. Clinical study of 44 cases of Staphylococcus aureus meningitis. Eur. J. Clin. Microbiol. Infect. Dis. 21(12), 864-868 (2002).
33. Lerche A, Rasmussen N, Wandall JH, Bohr VA. Staphylococcus aureus meningitis: a review of 28 consecutive community-acquired cases. Scand. J. Infect. Dis. 27(6), 569-573 (1995).
34. Brouwer MC, Keizerweerd GD, De Gans J, Spanjaard L, Van De Beek D. Community acquired Staphylococcus aureus meningitis in adults. Scand. J. Infect. Dis. 41(5), 375-377 (2009).
35. Jernigan JA, Stephens DS, Ashford DA et al. Bioterrorism-related inhalational anthrax: the first 10 cases reported in the United States. Emerg. Infect. Dis. 7(6), 933-944 (2001).
36. Bales ME, Dannenberg AL, Brachman PS, Kaufmann AF, Klatsky PC, Ashford DA. Epidemiologic response to anthrax outbreaks: field investigations, 1950-2001. Emerg. Infect. Dis. 8(10), 1163-1174 (2002).
37. Ramsay CN, Stirling A, Smith J et al. An outbreak of infection with Bacillus anthracis in injecting drug users in Scotland. EuroSurveill. 15(2), (2010).
38. Lanska DJ. Anthrax meningoencephalitis. Neurology 59(3), 327-334 (2002).
39. Stephens DS. Uncloaking the meningococcus: dynamics of carriage and disease. Lancet 353(9157), 941-942 (1999).
40. Kim KS, Itabashi H, Gemski P, Sadoff J, Warren RL, Cross AS. The K1 capsule is the critical determinant in the development of Escherichia coli meningitis in the rat. J. Clin. Invest. 90(3), 897-905 (1992).
41. Moxon ER, Ostrow PT. Haemophilus influenzae meningitis in infant rats: role of bacteremia in pathogenesis of age-dependent inflammatory responses in cerebrospinal fluid. J. Infect. Dis. 135(2), 303-307 (1977).
42. La Scolea LJ Jr, Dryja D. Quantitation of bacteria in cerebrospinal fluid and blood of children with meningitis and its diagnostic significance. J. Clin. Microbiol. 19(2), 187-190 (1984).
43. Petersdorf RG, Swarner DR, Garcia M. Studies on the pathogenesis of meningitis. II. Development of meningitis during pneumococcal bacteremia. J. Clin. Invest. 41, 320-327 (1962).
44. Ferrieri P, Burke B, Nelson J. Production of bacteremia and meningitis in infant rats with group B streptococcal serotypes. Infect. Immun. 27(3), 1023-1032 (1980).
45. Bell LM, Alpert G, Campos JM, Plotkin SA. Routine quantitative blood cultures in children with Haemophilus influenzae or Streptococcus pneumoniae bacteremia. Pediatrics 76(6), 901-904 (1985).
46. Nakamura S, Shchepetov M, Dalia AB et al. Molecular basis of increased serum resistance among pulmonary isolates of non-typeable Haemophilus influenzae. PLoS Pathog. 7(1), E1001247 (2011).
47. Mereghetti L, Sitkiewicz I, Green NM, Musser JM. Extensive adaptive changes occur in the transcriptome of Streptococcus agalactiae (group B Streptococcus) in response to incubation with human blood. PLoS One 3(9), E3143 (2008).
48. Echenique-Rivera H, Muzzi A, Del Tordello E et al. Transcriptome analysis of Neisseria meningitidis in human whole blood and mutagenesis studies identify virulence factors involved in blood survival. PLoS Pathog. 7(5), E1002027 (2011).
49. Santi I, Scarselli M, Mariani M et al. BibA: a novel immunogenic bacterial adhesin contributing to group B Streptococcus survival in human blood. Mol. Microbiol. 63(3), 754-767 (2007).
50. Sukumaran SK, Shimada H, Prasadarao NV. Entry and intracellular replication of Escherichia coli K1 in macrophages require expression of outer membrane protein A. Infect. Immun. 71(10), 5951-5961 (2003).
51. Mittal R, Prasadarao NV. gp96 expression in neutrophils is critical for the onset of Escherichia coli K1 (RS218) meningitis. Nat. Commun. 2, 552 (2011). Demonstrates mechanisms that promote bacterial bloodstream survival and subsequent blood-brain barrier (BBB) penetration.
52. Mittal R, Sukumaran SK, Selvaraj SK et al. Fcgamma receptor I alpha chain (CD64) expression in macrophages is critical for the onset of meningitis by Escherichia coli K1. PLoS Pathog. 6(11), E1001203 (2010).
53. Mittal R, Krishnan S, Gonzalez-Gomez I, Prasadarao NV. Deciphering the roles of outer membrane protein A extracellular loops in the pathogenesis of Escherichia coli K1 meningitis. J. Biol. Chem. 286(3), 2183-2193 (2011).
54. Pfister HW, Borasio GD, Dirnagl U, Bauer M, Einhaupl KM. Cerebrovascular complications of bacterial meningitis in adults. Neurology 42(8), 1497-1504 (1992).
55. Koedel U, Frankenberg T, Kirschnek S et al. Apoptosis is essential for neutrophil functional shutdown and determines tissue damage in experimental pneumococcal meningitis. PLoS Pathog. 5(5), E1000461 (2009).
56. Banerjee A, Kim BJ, Carmona EM et al. Bacterial Pili exploit integrin machinery to promote immune activation and efficient blood-brain barrier penetration. Nat. Commun. 2, 462 (2011).
57. Nguyen TH, Tran TH, Thwaites G et al. Dexamethasone in Vietnamese adolescents and adults with bacterial meningitis. N. Engl. J. Med. 357(24), 2431-2440 (2007).
58. Peltola H, Roine I, Fernandez J et al. Adjuvant glycerol and/or dexamethasone to improve the outcomes of childhood bacterial meningitis: a prospective, randomized, double-blind, placebo-controlled trial. Clin. Infect. Dis. 45(10), 1277-1286 (2007).
59. Van De Beek D, Farrar JJ, De Gans J et al. Adjunctive dexamethasone in bacterial meningitis: a meta-analysis of individual patient data. Lancet Neurol. 9(3), 254-263 (2010).
60. Scarborough M, Gordon SB, Whitty CJ et al. Corticosteroids for bacterial meningitis in adults in sub-Saharan Africa. N. Engl. J. Med. 357(24), 2441-2450 (2007).
61. Brouwer MC, Mcintyre P, De Gans J, Prasad K, Van De Beek D. Corticosteroids for acute bacterial meningitis. Cochrane Database Syst. Rev. (9), CD004405 (2010).
62. Abbott NJ, Ronnback L, Hansson E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat. Rev. Neurosci. 7(1), 41-53 (2006).
63. Rubin LL, Staddon JM. The cell biology of the blood-brain barrier. Annu. Rev. Neurosci. 22, 11-28 (1999).
64. Pulzova L, Bhide MR, Andrej K. Pathogen translocation across the blood-brain barrier. FEMS Immunol. Med. Microbiol. 57(3), 203-213 (2009).
65. Dejana E, Corada M, Lampugnani MG. Endothelial cell-to-cell junctions. FASEB 9(10), 910-918 (1995).
66. Hawkins RA, O'Kane RL, Simpson IA, Vina JR. Structure of the blood-brain barrier and its role in the transport of amino acids. J. Nutr. 136(1 Suppl.), 218S-226S (2006).
67. Schulze C, Firth JA. Immunohistochemical localization of adherens junction components in blood-brain barrier microvessels of the rat. Cell Sci. 104 (Pt 3), 773-782 (1993).
68. Wolburg H, Lippoldt A. Tight junctions of the blood-brain barrier: development, composition and regulation. Vascul. Pharmacol. 38(6), 323-337 (2002).
69. Gumbiner BM. Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell 84(3), 345-357 (1996).
70. Furuse M, Itoh M, Hirase T, Nagafuchi A, Yonemura S, Tsukita S. Direct association of occludin with ZO-1 and its possible involvement in the localization of occludin at tight junctions. J. Cell. Biol. 127(6 Pt 1), 1617-1626 (1994).
71. Martin-Padura I, Lostaglio S, Schneemann M et al. Junctional adhesion molecule, a novel member of the immunoglobulin superfamily that distributes at intercellular junctions and modulates monocyte transmigration. J. Cell. Biol. 142(1), 117-127 (1998).
72. Braga VM. Cell-cell adhesion and signalling. Curr. Opin. Cell Biol. 14(5), 546-556 (2002).
73. Matter K, Balda MS. Signalling to and from tight junctions. Nat. Rev. Mol. Cell Biol. 4(3), 225-236 (2003).
74. Wheelock MJ, Johnson KR. Cadherin-mediated cellular signaling. Curr. Opin. Cell Biol. 15(5), 509-514 (2003).
75. Taddei A, Giampietro C, Conti A et al. Endothelial adherens junctions control tight junctions by VE-cadherin-mediated upregulation of claudin-5. Nat. Cell Biol. 10(8), 923-934 (2008).
76. 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. 145(5), 1228-1236 (1994). Pioneering study describing the development of the human brain microvascular cell line.
77. Weksler BB, Subileau EA, Perriere N et al. Blood-brain barrier-specific properties of a human adult brain endothelial cell line. FASEB 19(13), 1872-1874 (2005).
78. Greiffenberg L, Goebel W, Kim KS et al. Interaction of Listeria monocytogenes with human brain microvascular endothelial cells: InlB-dependent invasion, long-term intracellular growth, and spread from macrophages to endothelial cells. Infect. Immun. 66(11), 5260-5267 (1998).
79. Wickham ME, Brown NF, Provias J, Finlay BB, Coombes BK. Oral infection of mice with Salmonella enterica serovar Typhimurium causes meningitis and infection of the brain. BMC Infect. Dis. 7, 65 (2007).
80. Doran KS, Liu GY, Nizet V. Group B streptococcal beta-hemolysin/cytolysin activates neutrophil signaling pathways in brain endothelium and contributes to development of meningitis. J. Clin. Invest. 112(5), 736-744. (2003).
81. Smith AL, Smith DH, Averill DR Jr, Marino J, Moxon ER. Production of Haemophilus influenzae b meningitis in infant rats by intraperitoneal inoculation. Infect. Immun. 8(2), 278-290 (1973).
82. Uchiyama S, Carlin AF, Khosravi A et al. The surface-anchored NanA protein promotes pneumococcal brain endothelial cell invasion. J. Exp. Med. 206(9), 1845-1852 (2009).
83. Sheen TR, Ebrahimi CM, Hiemstra IH, Barlow SB, Peschel A, Doran KS. Penetration of the blood-brain barrier by Staphylococcus aureus: contribution of membrane-anchored lipoteichoic acid. J. Mol. Med. 88(6), 633-639 (2010).
84. Nizet V, Kim KS, Stins M et al. Invasion of brain microvascular endothelial cells by group B streptococci. Infect. Immun. 65(12), 5074-5081 (1997).
85. Stins MF, Badger J, Sik Kim K. Bacterial invasion and transcytosis in transfected human brain microvascular endothelial cells. Microb. Pathog. 30(1), 19-28 (2001).
86. Ring A, Weiser JN, Tuomanen EI. Pneumococcal trafficking across the blood-brain barrier. Molecular analysis of a novel bidirectional pathway. J. Clin. Invest. 102(2), 347-360 (1998).
87. Jain SK, Paul-Satyaseela M, Lamichhane G, Kim KS, Bishai WR. Mycobacterium tuberculosis invasion and traversal across an in vitro human blood-brain barrier as a pathogenic mechanism for central nervous system tuberculosis. J. Infect. Dis. 193(9), 1287-1295 (2006).
88. Nikulin J, Panzner U, Frosch M, Schubert-Unkmeir A. Intracellular survival and replication of Neisseria meningitidis in human brain microvascular endothelial cells. Int. J. Med. Microbiol. 296(8), 553-558 (2006).
89. Van Sorge NM, Zialcita PA, Browne SH, Quach D, Guiney DG, Doran KS. Penetration and activation of brain endothelium by Salmonella enterica serovar Typhimurium. J. Infect. Dis. 203(3), 401-405 (2011).
90. Prasadarao NV, Wass CA, Stins MF, Shimada H, Kim KS. Outer membrane protein A-promoted actin condensation of brain microvascular endothelial cells is required for Escherichia coli invasion. Infect. Immun. 67(11), 5775-5783 (1999).
91. Das A, Asatryan L, Reddy MA et al. Differential role of cytosolic phospholipase A2 in the invasion of brain microvascular endothelial cells by Escherichia coli and Listeria monocytogenes. J. Infect. Dis. 184(6), 732-737 (2001).
92. Kim KS. Mechanisms of microbial traversal of the blood-brain barrier. Nat. Rev. Microbiol. 6(8), 625-634 (2008). Excellent review of bacterial and host factors involved in BBB penetration and pathogenesis of meningitis.
93. Kim KS. Acute bacterial meningitis in infants and children. Lancet Infect. Dis. 10(1), 32-42 (2010). Excellent review on the pathogenesis of bacterial meningitis.
94. Badger JL, Wass CA, Weissman SJ, Kim KS. Application of signature-tagged mutagenesis for identification of Escherichia coli K1 genes that contribute to invasion of human brain microvascular endothelial cells. Infect. Immun. 68(9), 5056-5061 (2000).
95. 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. 115(9), 2499-2507. (2005).
96. Dietrich G, Kurz S, Hubner C et al. Transcriptome analysis of Neisseria meningitidis during infection. J. Bacteriol. 185(1), 155-164 (2003).
97. Teng CH, Cai M, Shin S et al. Escherichia coli K1 RS218 interacts with human brain microvascular endothelial cells via type 1 fimbria bacteria in the fimbriated state. Infect. Immun. 73(5), 2923-2931 (2005).
98. Badger JL, Wass CA, Kim KS. Identification of Escherichia coli K1 genes contributing to human brain microvascular endothelial cell invasion by differential fluorescence induction. Mol. Microbiol. 36(1), 174-182 (2000).
99. Tazi A, Disson O, Bellais S et al. The surface protein HvgA mediates group B Streptococcus hypervirulence and meningeal tropism in neonates. J. Exp. Med. 207(11), 2313-2322 (2010).
100. Mairey E, Genovesio A, Donnadieu E et al. Cerebral microcirculation shear stress levels determine Neisseria meningitidis attachment sites along the blood-brain barrier. J. Exp. Med. 203(8), 1939-1950 (2006).
101. 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. 189(4), 1464-1467 (2007).
102. Van Sorge NM, Quach D, Gurney MA, Sullam PM, Nizet V, Doran KS. The group B streptococcal serine-rich repeat 1 glycoprotein mediates penetration of the blood-brain barrier. J. Infect. Dis. 199(10), 1479-1487 (2009).
103. Kirchner M, Meyer TF. The PilC adhesin of the Neisseria type IV pilus-binding specificities and new insights into the nature of the host cell receptor. Mol. Microbiol. 56(4), 945-957 (2005).
104. Telford JL, Barocchi MA, Margarit I, Rappuoli R, Grandi G. Pili in Gram-positive pathogens. Nat. Rev. Microbiol. 4(7), 509-519 (2006).
105. Barocchi MA, Ries J, Zogaj X et al. A pneumococcal pilus influences virulence and host inflammatory responses. Proc. Natl Acad. Sci. USA 103(8), 2857-2862 (2006).
106. Bagnoli F, Moschioni M, Donati C et al. A second pilus type in Streptococcus pneumoniae is prevalent in emerging serotypes and mediates adhesion to host cells. J. Bacteriol. 190(15), 5480-5492 (2008).
107. St Geme JW 3rd, Cutter D. Influence of pili, fibrils, and capsule on in vitro adherence by Haemophilus influenzae type b. Mol. Microbiol. 21(1), 21-31 (1996).
108. St. Geme JW 3rd, Cutter D. Evidence that surface fibrils expressed by Haemophilus influenzae type b promote attachment to human epithelial cells. Mol. Microbiol. 15(1), 77-85 (1995).
109. Unkmeir A, Latsch K, Dietrich G et al. Fibronectin mediates Opc-dependent internalization of Neisseria meningitidis in human brain microvascular endothelial cells. Mol. Microbiol. 46(4), 933-946 (2002).
110. Kim KJ, Elliott SJ, Di Cello F, Stins MF, Kim KS. The K1 capsule modulates trafficking of E. coli-containing vacuoles and enhances intracellular bacterial survival in human brain microvascular endothelial cells. Cell. Microbiol. 5(4), 245-252 (2003).
111. St Geme JW 3rd, Falkow S. Loss of capsule expression by Haemophilus influenzae type b results in enhanced adherence to and invasion of human cells. Infect. Immun. 59(4), 1325-1333 (1991).
112. Hammerschmidt S, Muller A, Sillmann H et al. Capsule phase variation in Neisseria meningitidis serogroup B by slipped-strand mispairing in the polysialyltransferase gene (siaD): correlation with bacterial invasion and the outbreak of meningococcal disease. Mol. Microbiol. 20(6), 1211-1220 (1996).
113. Khan NA, Wang Y, Kim KJ, Chung JW, Wass CA, Kim KS. Cytotoxic necrotizing factor-1 contributes to Escherichia coli K1 invasion of the central nervous system. J. Biol. Chem. 277(18), 15607-15612 (2002).
114. Zysk G, Schneider-Wald BK, Hwang JH et al. Pneumolysin is the main inducer of cytotoxicity to brain microvascular endothelial cells caused by Streptococcus pneumoniae. Infect. Immun. 69(2), 845-852 (2001).
115. Patrick D, Betts J, Frey EA, Prameya R, Dorovini-Zis K, Finlay BB. Haemophilus influenzae lipopolysaccharide disrupts confluent monolayers of bovine brain endothelial cells via a serum-dependent cytotoxic pathway. J. Infect. Dis. 165(5), 865-872 (1992).
116. Wellmer A, Zysk G, Gerber J et al. Decreased virulence of a pneumolysin-deficient strain of Streptococcus pneumoniae in murine meningitis. Infect. Immun. 70(11), 6504-6508 (2002).
117. Orihuela CJ, Mahdavi J, Thornton J et al. Laminin receptor initiates bacterial contact with the blood brain barrier in experimental meningitis models. J. Clin. Invest. 119(6), 1638-1646 (2009). Demonstrates a host receptor that acts as a common portal of bacterial entry.
118. Swords WE, Ketterer MR, Shao J, Campbell CA, Weiser JN, Apicella MA. Binding of the non-typeable Haemophilus influenzae lipooligosaccharide to the PAF receptor initiates host cell signalling. Cell. Microbiol. 3(8), 525-536 (2001).
119. Virji M, Saunders JR, Sims G, Makepeace K, Maskell D, Ferguson DJ. Pilus-facilitated adherence of Neisseria meningitidis to human epithelial and endothelial cells: modulation of adherence phenotype occurs concurrently with changes in primary amino acid sequence and the glycosylation status of pilin. Mol. Microbiol. 10(5), 1013-1028 (1993).
120. Kim KJ, Chung JW, Kim KS. 67-kDa laminin receptor promotes internalization of cytotoxic necrotizing factor 1-expressing Escherichia coli K1 into human brain microvascular endothelial cells. J. Biol. Chem. 280(2), 1360-1368 (2005).
121. Chung JW, Hong SJ, Kim KJ et al. 37-kDa laminin receptor precursor modulates cytotoxic necrotizing factor 1-mediated RhoA activation and bacterial uptake. J. Biol. Chem. 278(19), 16857-16862 (2003).
122. Radin JN, Orihuela CJ, Murti G, Guglielmo C, Murray PJ, Tuomanen EI. Beta-Arrestin 1 participates in platelet-activating factor receptor-mediated endocytosis of Streptococcus pneumoniae. Infect. Immun. 73(12), 7827-7835 (2005).
123. Rijneveld AW, Weijer S, Florquin S et al. Improved host defense against pneumococcal pneumonia in platelet-activating factor receptor-deficient mice. J. Infect. Dis. 189(4), 711-716 (2004).
124. Kolberg J, Hoiby EA, Jantzen E. Detection of the phosphorylcholine epitope in Streptococci, Haemophilus and pathogenic Neisseriae by immunoblotting. Microb. Pathog. 22(6), 321-329 (1997).
125. Weiser JN, Pan N, McGowan KL, Musher D, Martin A, Richards J. Phosphorylcholine on the lipopolysaccharide of Haemophilus influenzae contributes to persistence in the respiratory tract and sensitivity to serum killing mediated by C-reactive protein. J. Exp. Med. 187(4), 631-640 (1998).
126. Swords WE, Buscher BA, Ver Steeg Ii K et al. Non-typeable Haemophilus influenzae adhere to and invade human bronchial epithelial cells via an interaction of lipooligosaccharide with the PAF receptor. Mol. Microbiol. 37(1), 13-27 (2000).
127. Kim SH, Turnbull J, Guimond S. Extracellular matrix and cell signalling: the dynamic cooperation of integrin, proteoglycan and growth factor receptor. J. Endocrinol. 209(2), 139-151 (2011).
128. Chang YC, Wang Z, Flax LA et al. Glycosaminoglycan binding facilitates entry of a bacterial pathogen into central nervous systems. PLoS Pathog. 7(6), e1002082 (2011).
129. Fida NM, Al-Mughales J, Farouq M. Interleukin-1alpha, interleukin-6 and tumor necrosis factor-alpha levels in children with sepsis and meningitis. Pediatr. Int. 48(2), 118-124 (2006).
130. Tang RB, Lee BH, Chung RL, Chen SJ, Wong TT. Interleukin-1beta and tumor necrosis factor-alpha in cerebrospinal fluid of children with bacterial meningitis. Childs Nerv. Syst. 17(8), 453-456 (2001).
131. Lehmann AK, Halstensen A, Sornes S, Rokke O, Waage A. High levels of interleukin 10 in serum are associated with fatality in meningococcal disease. Infect. Immun. 63(6), 2109-2112 (1995).
132. Leist TP, Frei K, Kam-Hansen S, Zinkernagel RM, Fontana A. Tumor necrosis factor alpha in cerebrospinal fluid during bacterial, but not viral, meningitis. Evaluation in murine model infections and in patients. J. Exp. Med. 167(5), 1743-1748 (1988).
133. Waage A, Brandtzaeg P, Halstensen A, Kierulf P, Espevik T. The complex pattern of cytokines in serum from patients with meningococcal septic shock. Association between interleukin 6, interleukin 1, and fatal outcome. J. Exp. Med. 169(1), 333-338 (1989).
134. Nagesh Babu G, Kumar A, Kalita J, Misra UK. Proinflammatory cytokine levels in the serum and cerebrospinal fluid of tuberculous meningitis patients. Neurosci. Lett. 436(1), 48-51 (2008).
135. Cundell DR, Gerard NP, Gerard C, Idanpaan-Heikkila I, Tuomanen EI. Streptococcus pneumoniae anchor to activated human cells by the receptor for platelet-activating factor. Nature 377(6548), 435-438 (1995).
136. Banerjee A, Van Sorge NM, Sheen TR, Uchiyama S, Mitchell TJ, Doran KS. Activation of brain endothelium by pneumococcal neuraminidase NanA promotes bacterial internalization. Cell. Microbiol. 12(11), 1576-1588 (2010).
137. Zhang WG, Khan AN, Kim KJ, Stins M, Kim KS. Transforming growth factor-beta increases Escherichia coli K1 adherence, invasion, and transcytosis in human brain microvascular endothelial cells. Cell. Tissue Res. 309(2), 281-286 (2002).
138. Lembo A, Gurney MA, Burnside K et al. Regulation of CovR expression in group B Streptococcus impacts blood-brain barrier penetration. Mol. Microbiol. 77(2), 431-443 (2010).
139. Sharief MK, Ciardi M, Thompson EJ. Blood-brain barrier damage in patients with bacterial meningitis: association with tumor necrosis factor-alpha but not interleukin-1 beta. J. Infect. Dis. 166(2), 350-358 (1992).
140. Barichello T, Pereira JS, Savi GD et al. A kinetic study of the cytokine/chemokines levels and disruption of blood-brain barrier in infant rats after pneumococcal meningitis. J. Neuroimmunol. 233(1-2), 12-17 (2011).
141. Kim KS, Wass CA, Cross AS. Blood-brain barrier permeability during the development of experimental bacterial meningitis in the rat. Exp. Neurol. 145(1), 253-257 (1997).
142. Mittal R, Prasadarao NV. Nitric oxide/cGMP signalling induces Escherichia coli K1 receptor expression and modulates the permeability in human brain endothelial cell monolayers during invasion. Cell Microbiol. 12(1), 67-83 (2010).
143. Winkler F, Koedel U, Kastenbauer S, Pfister HW. Differential expression of nitric oxide synthases in bacterial meningitis: role of the inducible isoform for blood-brain barrier breakdown. J. Infect. Dis. 183(12), 1749-1759 (2001).
144. Leib SL, Kim YS, Black SM, Tureen JH, Tauber MG. Inducible nitric oxide synthase and the effect of aminoguanidine in experimental neonatal meningitis. J. Infect. Dis. 177(3), 692-700 (1998).
145. Koedel U, Bernatowicz A, Paul R, Frei K, Fontana A, Pfister HW. Experimental pneumococcal meningitis: cerebrovascular alterations, brain edema, and meningeal inflammation are linked to the production of nitric oxide. Ann. Neurol. 37(3), 313-323 (1995).
146. Mittal R, Gonzalez-Gomez I, Goth KA, Prasadarao NV. Inhibition of inducible nitric oxide controls pathogen load and brain damage by enhancing phagocytosis of Escherichia coli K1 in neonatal meningitis. Am. J. Pathol. 176(3), 1292-1305 (2010).
147. Coureuil M, Lecuyer H, Scott MG et al. Meningococcus Hijacks a beta2-adrenoceptor/beta-Arrestin pathway to cross brain microvasculature endothelium. Cell 143(7), 1149-1160 (2010).
148. Coureuil M, Mikaty G, Miller F et al. Meningococcal type IV pili recruit the polarity complex to cross the brain endothelium. Science 325(5936), 83-87 (2009). Demonstrates paracellular transit at the BBB.
149. Schubert-Unkmeir A, Konrad C, Slanina H, Czapek F, Hebling S, Frosch M. Neisseria meningitidis induces brain microvascular endothelial cell detachment from the matrix and cleavage of occludin: a role for MMP-8. PLoS Pathog. 6(4), e1000874 (2010).
150. Sukumaran SK, Prasadarao NV. Escherichia coli K1 invasion increases human brain microvascular endothelial cell monolayer permeability by disassembling vascular-endothelial cadherins at tight junctions. J. Infect. Dis. 188(9), 1295-1309 (2003).
151. Ebrahimi CM, Kern JW, Sheen TR et al. Penetration of the blood-brain barrier by Bacillus anthracis requires the pXO1-encoded BslA protein. J. Bacteriol. 191(23), 7165-7173 (2009).
152. Ebrahimi CM, Sheen TR, Renken CW, Gottlieb RA, Doran KS. Contribution of lethal toxin and edema toxin to the pathogenesis of anthrax meningitis. Infect. Immun. 79(7), 2510-2518 (2011).
153. Mukherjee DV, Tonry JH, Kim KS et al. Bacillus anthracis protease InhA increases blood-brain barrier permeability and contributes to cerebral hemorrhages. PLoS One 6(3), E17921 (2011).
154. Guichard A, McGillivray SM, Cruz-Moreno B, Van Sorge NM, Nizet V, Bier E. Anthrax toxins cooperatively inhibit endocytic recycling by the Rab11/Sec15 exocyst. Nature 467(7317), 854-858 (2010).
155. Saez-Llorens X, Jafari HS, Severien C et al. Enhanced attenuation of meningeal inflammation and brain edema by concomitant administration of anti-CD18 monoclonal antibodies and dexamethasone in experimental Haemophilus meningitis. J. Clin. Invest. 88(6), 2003-2011 (1991).
156. Tuomanen EI, Saukkonen K, Sande S, Cioffe C, Wright SD. Reduction of inflammation, tissue damage, and mortality in bacterial meningitis in rabbits treated with monoclonal antibodies against adhesion-promoting receptors of leukocytes. J. Exp. Med. 170(3), 959-969 (1989).
157. Galanakis E, Di Cello F, Paul-Satyaseela M, Kim KS. Escherichia coli K1 induces IL-8 expression in human brain microvascular endothelial cells. Eur. Cytokine Netw. 17(4), 260-265 (2006).
158. Vadeboncoeur N, Segura M, Al-Numani D, Vanier G, Gottschalk M. Pro-inflammatory cytokine and chemokine release by human brain microvascular endothelial cells stimulated by Streptococcus suis serotype 2. FEMS Immunol. Med. Microbiol. 35(1), 49-58 (2003).
159. Wilson SL, Drevets DA. Listeria monocytogenes infection and activation of human brain microvascular endothelial cells. J. Infect. Dis. 178(6), 1658-1666 (1998).
160. Sokolova O, Heppel N, Jagerhuber R et al. Interaction of Neisseria meningitidis with human brain microvascular endothelial cells: role of MAP- and tyrosine kinases in invasion and inflammatory cytokine release. Cell. Microbiol. 6(12), 1153-1166. (2004).
161. Schubert-Unkmeir A, Sokolova O, Panzner U, Eigenthaler M, Frosch M. Gene expression pattern in human brain endothelial cells in response to Neisseria meningitidis. Infect. Immun. 75(2), 899-914. (2007).
162. Krishnan V, Gaspar AH, Ye N, Mandlik A, Ton-That H, Narayana SV. An IgG-like domain in the minor pilin GBS52 of Streptococcus agalactiae mediates lung epithelial cell adhesion. Structure 15(8), 893-903 (2007).
163. Van Sorge NM, Ebrahimi CM, McGillivray SM et al. Anthrax toxins inhibit neutrophil signaling pathways in brain endothelium and contribute to the pathogenesis of meningitis. PLoS One 3(8), e2964 (2008).
164. Reddy MA, Wass CA, Kim KS, Schlaepfer DD, Prasadarao NV. Involvement of focal adhesion kinase in Escherichia coli invasion of human brain microvascular endothelial cells. Infect. Immun. 68(11), 6423-6430 (2000).
165. Sukumaran SK, Prasadarao NV. Regulation of protein kinase C in Escherichia coli K1 invasion of human brain microvascular endothelial cells. J. Biol. Chem. 277(14), 12253-12262 (2002).
166. 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. 73(7), 4404-4409 (2005).
167. 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. 9(6), 714-720 (2007).
168. .WHO Health Report 2004. www.who.int/whr/2004/en/report04-en.pdf
169. .HiB Initiative. www.hibaction.orgReviewvan