Epidemiology and pathogenesis of Neisseria meningitidis

Microbes and Infection

Volumn 2, Issue 6, 2000, Pages 687-700

  Tzeng, Yih Ling ^a   Stephens, David S ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Epidemiology; Meningitis; Neisseria meningitidis; Pathogenesis; Virulence factors

Indexed keywords

MENINGOCOCCUS VACCINE;

BACTERIAL VIRULENCE; DISEASE PREDISPOSITION; HUMAN; INFECTION CONTROL; MENINGOCOCCOSIS; NEISSERIA MENINGITIDIS; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; VACCINATION;

BACTERIA (MICROORGANISMS); MENINGOCOCCUS; NEGIBACTERIA; NEISSERIA MENINGITIDIS;

EID: 0034051214     PISSN: 12864579     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1286-4579(00)00356-7     Document Type: Review

References (142)

1. Tikhomirov E., Santamaria M., Esteves K. Meningococcal disease: public health burden and control. Wld Hlth Statist. Quart. 166:1997.
2. Pinner R.W., Onyango F., Perkins B.A., Mirza N.B., Ngacha D.M., Reeves M., Dewitt W., Njeru E., Agata N.N., Broome C.V. Epidemic meningococcal disease in Nairobi, Kenya, 1988. The Kenya/Centers for Disease Control (CDC) Meningitis Study Group. J. Infect. Dis. 273:1992;359-364.
3. Jackson L.A., Schuchat A., Reeves M.W., Wenger J.D. Serogroup C meningococcal outbreaks in the United States. An emerging threat. JAMA. 83:1995;383-389.
4. Achtman M. Meningococcal disease. Cartwright K. 1995;159-175 John Wiley and Sons, Chichester, UK.
5. Rosenstein N., Pinner R.W., Stephens D.S. Infectious Diseases, Vol. Sect. 6. Armstrong D, Cohen J. 1999;201-204 Mosby, London.
6. Caugant D.A., Froholm L.O., Bovre K., Holten E., Frasch C.E., Mocca L.F., Zollinger W.D., Selander R.K. Intercontinental spread of a genetically distinctive complex of clones of Neisseria meningitidis causing epidemic disease. Proc. Natl. Acad. Sci. USA. 177:1986;4927-4931.
7. Martin D.R., Walker S.J., Baker M.G., Lennon D.R. New Zealand epidemic of meningococcal disease identified by a strain with phenotype B:4: P1. 4. J. Infect. Dis. 123:1998;497-500.
8. Perkins B.A., Pinner R.W., Stephens D.S. Medicine for the practicing physician. Hurst J.W. 1996;412-414 Appleton and Lange, Norwalk, CT.
9. Greenfield S., Sheehe P.R., Feldman H.A. Meningococcal carriage in a population of 'normal' families. J. Infect. Dis. 5:1971;67-73.
10. Peltola H. Meningococcal disease: still with us. Rev. Infect. Dis. 95:1983;71-91.
11. Maiden M.C., Bygraves J.A., Feil E., Morelli G., Russell J.E., Urwin R., Zhang Q., Zhou J., Zurth K., Caugant D.A., Feavers I.M., Achtman M., Spratt B.G. Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc. Natl. Acad. Sci. USA. 176:1998;3140-3145.
12. Raymond N.J., Reeves M., Ajello G., Baughman W., Gheesling L.L., Carlone G.M., Wenger J.D., Stephens D.S. Molecular epidemiology of sporadic (endemic) serogroup C meningococcal disease. J. Infect. Dis. 178:1997;1277-1284.
13. Jones G.R., Christodoulides M., Brooks J.L., Miller A.R., Cartwright K.A., Heckels J.E. Dynamics of carriage of Neisseria meningitidis in a group of military recruits: subtype stability and specificity of the immune response following colonization. J. Infect. Dis. 56:1998;451-459.
14. Caugant D.A., Kristiansen B.E., Froholm L.O., Bovre K., Selander R.K. Clonal diversity of Neisseria meningitidis from a population of asymptomatic carriers. Infect. Immun. 94:1988;2060-2068.
15. Swartley J.S., Marfin A.A., Edupuganti S., Liu L.J., Cieslak P., Perkins B., Wenger J.D., Stephens D.S. Capsule switching of Neisseria meningitidis. Proc. Natl. Acad. Sci. USA. 11:1997;271-276.
16. Achtman M. Clonal spread of serogroup A meningococci: a paradigm for the analysis of microevolution in bacteria. Mol. Microbiol. 33:1994;15-22.
17. Blondeau J.M., Ashton F.E., Isaacson M., Yaschuck Y., Anderson C., Ducasse G. Neisseria meningitidis with decreased susceptibility to penicillin in Saskatchewan, Canada. J. Clin. Microbiol. 13:1995;1784-1786.
18. Brandtzaeg P., Halstensen A., Kierulf P., Espevik T., Waage A. Molecular mechanisms in the compartmentalized inflammatory response presenting as meningococcal meningitis or septic shock. Microb. Pathog. 104:1992;423-431.
19. Blackwell C.C., Weir D.M., James V.S., Todd W.T., Banatvala N., Chaudhuri A.K., Gray H.G., Thomson E.J., Fallon R.J. Secretor status, smoking and carriage of Neisseria meningitidis. Epidemiol. Infect. 137:1990;203-209.
20. Gold R., Goldschneider I., Lepow M.L., Draper T.F., Randolph M. Carriage of Neisseria meningitidis and Neisseria lactamica in infants and children. J. Infect. Dis. 308:1978;112-121.
21. Ellison R.T.D., Kohler P.F., Curd J.G., Judson F.N., Reller L.B. Prevalence of congenital or acquired complement deficiency in patients with sporadic meningocococcal disease. New Engl. J. M. 129:1983;913-916.
22. Gotschlich E.C., Liu T.Y., Artenstein M.S. Human immunity to the meningococcus. 3. Preparation and immunochemical properties of the group A, group B, and group C meningococcal polysaccharides. J. Exp. M. 123:1969;1349-1365.
23. Stephens D.S., Hajjeh R.A., Baughman W.S., Harvey R.C., Wenger J.D., Farley M.M. Sporadic meningococcal disease in adults: results of a 5-year population-based study. Ann. Intern. M. 12:1995;937-940.
24. Figueroa J., Andreoni J., Densen P. Complement deficiency states and meningococcal disease. Immunol. Res. 114:1993;295-311.
25. Griffiss J.M. Bactericidal activity of meningococcal antisera. Blocking by IgA of lytic antibody in human convalescent sera. J. Immunol. 155:1975;1779-1784.
26. Ross S.C., Rosenthal P.J., Berberich H.M., Densen P. Killing of Neisseria meningitidis by human neutrophils: implications for normal and complement-deficient individuals. J. Infect. Dis. 170:1987;1266-1275.
27. Schlesinger M., Greenberg R., Levy J., Kayhty H., Levy R. Killing of meningococci by neutrophils: effect of vaccination on patients with complement deficiency. J. Infect. Dis. 61:1994;449-453.
28. Guttormsen H.K., Wetzler L.M., Naess A. Humoral immune response to the class 3 outer membrane protein during the course of meningococcal disease. Infect. Immun. 354:1993;4734-4742.
29. Westendorp R.G.J., Hottenga J.J., Slagboom P.E. Variation in plasminogen-activator-inhibitor-1 gene and risk of meningococcal septic shock. Lancet. 170:1999;561-563.
30. Bredius R.G., Derkx B.H., Fijen C.A., De Wit T.P., De Haas M., Weening R.S., Van De Winkel J.G., Out T.A. Fc gamma receptor IIa (CD32) polymorphism in fulminant meningococcal septic shock in children. J. Infect. Dis. 174:1994;848-853.
31. Nadel S., Newport M.J., Booy R., Levin M. Variation in the tumor necrosis factor-alpha gene promoter region may be associated with death from meningococcal disease. J. Infect. Dis. 2:1996;878-880.
32. Moore P.S., Reeves M.W., Schwartz B., Gellin B.G., Broome C.V. Intercontinental spread of an epidemic group A Neisseria meningitidis strain. Lancet. 1:1989;260-263.
33. Greenwood B.M., Blakebrough I.S., Bradley A.K., Wali S., Whittle H.C. Meningococcal disease and season in sub-Saharan Africa. Lancet. 89:1984;1339-1342.
34. Yusuf H.R., Rochat R.W., Baughman W.S., Gargiullo P.M., Perkins B.A., Brantley M.D., Stephens D.S. Maternal cigarette smoking and invasive meningococcal disease: a cohort study among young children in metropolitan Atlanta, 1989-1996. Am. J. Public Health. 16:1999;712-717.
35. Fischer M., Hedberg K., Cardosi P., Plikaytis B.D., Hoesly F.C., Steingart K.R., Bell T.A., Fleming D.W., Wenger J.D., Perkins B.A. Tobacco smoke as a risk factor for meningococcal disease. Pediatr. Infect. Dis. J. 2:1997;979-983.
36. Faur Y.C., Weisburd M.H., Wilson M.E. Isolation of Neisseria meningitidis from the genito-urinary tract and anal canal. J. Clin. Microbiol. 264:1975;178-182.
37. Moore P.S., Hierholzer J., Dewitt W., Gouan K., Djore D., Lippeveld T., Plikaytis B., Broome C.V. Respiratory viruses and mycoplasma as cofactors for epidemic group A meningococcal meningitis. JAMA. 2 Suppl:1990;1271-1275.
38. Stephens D.S. Gonococcal and meningococcal pathogenesis as defined by human cell, cell culture, and organ culture assays. Clin. Microbiol. Rev. 15:1989;S104-111.
39. Mackinnon F.G., Borrow R., Gorringe A.R., Fox A.J., Jones D.M., Robinson A. Demonstration of lipooligosaccharide immunotype and capsule as virulence factors for Neisseria meningitidis using an infant mouse intranasal infection model. Microb. Pathog. 148:1993;359-366.
40. Stephens D.S., Hoffman L.H., McGee Z.A. Interaction of Neisseria meningitidis with human nasopharyngeal mucosa: attachment and entry into columnar epithelial cells. J. Infect. Dis. 64:1983;369-376.
41. Read R.C., Zimmerli S., Broaddus C., Sanan D.A., Stephens D.S., Ernst J.D. The (α → 8)-linked polysialic acid capsule of group B Neisseria meningitidis modifies multiple steps during interaction with human macrophages. Infect. Immun. 170:1996;3210-3217.
42. Waage A., Halstensen A., Shalaby R., Brandtzaeg P., Kierulf P., Espevik T. Local production of tumor necrosis factor alpha, interleukin 1, and interleukin 6 in meningococcal meningitis. Relation to the inflammatory response. J. Exp. M. 93:1989;1859-1867.
43. Tinsley C.R., Nassif X. Analysis of the genetic differences between Neisseria meningitidis and Neisseria gonorrhoeae: two closely related bacteria expressing two different pathogenicities. Proc. Natl. Acad. Sci. USA. 250:1996;11109-11114.
44. Kupsch E.M., Aubel D., Gibbs C.P., Kahrs A.F., Rudel T., Meyer T.F. Construction of Hermes shuttle vectors: a versatile system useful for genetic complementation of transformable and non-transformable Neisseria mutants. Mol. Gen. Genet. 62:1996;558-569.
45. Stephens D.S., McAllister C.F., Zhou D., Lee F.K., Apicella M.A. Tn916-generated, lipooligosaccharide mutants of Neisseria meningitidis and Neisseria gonorrhoeae. Infect. Immun. 161:1994;2947-2952.
46. Stephens D.S., Whitney A.M., Rothbard J., Schoolnik G.K. Pili of Neisseria meningitidis. Analysis of structure and investigation of structural and antigenic relationships to gonococcal pili. J. Exp. M. 135:1985;1539-1553.
47. Virji M.H.J., Potts W.J., Hart C.A., Saunders J.R. Identification of epitopes recognized by monoclonal antibodies SM1 and SM2 which react with all pili of Neisseria gonorrhoeae but which differentiate between two structural classes of pili expressed by Neisseria meningitidis and the distribution of their encoding sequences in the genomes of Neisseria spp. J. Gen. Microbiol. 378:1989;3239-3251.
48. Parge H.E., Forest K.T., Hickey M.J., Christensen D.A., Getzoff E.D., Tainer J.A. Structure of the fibre-forming protein pilin at 2. 6 A resolution. Nature. 172:1995;32-38.
49. Seifert H.S., Ajioka R.S., Paruchuri D., Heffron F., So M. Shuttle mutagenesis of Neisseria gonorrhoeae: pilin null mutations lower DNA transformation competence. J. Bacteriol. 273:1990;40-46.
50. Kallstrom H., Islam M.S., Berggren P.O., Jonsson A.B. Cell signaling by the type IV pili of pathogenic Neisseria. J. Biol. Chem. 25:1998;21777-21782.
51. Kallstrom H., Liszewski M.K., Atkinson J.P., Jonsson A.B. Membrane cofactor protein (MCP or CD46) is a cellular pilus receptor for pathogenic Neisseria. Mol. Microbiol. 90:1997;639-647.
52. Strom M.S., Nunn D.N., Lory S. A single bifunctional enzyme, PilD, catalyzes cleavage and N-methylation of proteins belonging to the type IV pilin family. Proc. Natl. Acad. Sci. USA. 8:1993;2404-2408.
53. Nassif X., Lowy J., Stenberg P., O'Gaora P., Ganji A., So M. Antigenic variation of pilin regulates adhesion of Neisseria meningitidis to human epithelial cells. Mol. Microbiol. 338:1993;719-725.
54. Gibbs C.P., Reimann B.Y., Schultz E., Kaufmann A., Haas R., Meyer T.F. Reassortment of pilin genes in Neisseria gonorrhoeae occurs by two distinct mechanisms. Nature. 17:1989;651-652.
55. Stimson E., Virji M., Makepeace K., Dell A., Morris H.R., Payne G., Saunders J.R., Jennings M.P., Barker S., Panico M. Meningococcal pilin: a glycoprotein substituted with digalactosyl 2, 4-diacetamido-2, 4, 6-trideoxyhexose. Mol. Microbiol. 27:1995;1201-1214.
56. Marceau M., Forest K., Beretti J.L., Tainer J., Nassif X. Consequences of the loss of O-linked glycosylation of meningococcal type IV pilin on piliation and pilus-mediated adhesion. Mol. Microbiol. 66:1998;705-715.
57. Weiser J.N., Goldberg J.B., Pan N., Wilson L., Virji M. The phosphorylcholine epitope undergoes phase variation on a 43-kilodalton protein in Pseudomonas aeruginosa and on pili of Neisseria meningitidis and Neisseria gonorrhoeae. Infect. Immun. 31:1998;4263-4267.
58. Forest K.T., Dunham S.A., Koomey M., Tainer J.A. Crystallographic structure reveals phosphorylated pilin from Neisseria: phosphoserine sites modify type IV pilus surface chemistry and fibre morphology. Mol. Microbiol. 91:1999;743-752.
59. Nassif X., Beretti J.L., Lowy J., Stenberg P., O'Gaora P., Pfeifer J., Normark S., So M. Roles of pilin and PilC in adhesion of Neisseria meningitidis to human epithelial and endothelial cells. Proc. Natl. Acad. Sci. USA. 23:1994;3769-3773.
60. Ryll R.R., Rudel T., Scheuerpflug I., Barten R., Meyer T.F. PilC of Neisseria meningitidis is involved in class II pilus formation and restores pilus assembly, natural transformation competence and adherence to epithelial cells in PilC-deficient gonococci. Mol. Microbiol. 16:1997;879-892.
61. Virji M., Makepeace K., Peak I., Payne G., Saunders J.R., Ferguson D.J., Moxon E.R. Functional implications of the expression of PilC proteins in meningococci. Mol. Microbiol. 10:1995;1087-1097.
62. Jonsson A.B., Nyberg G., Normark S. Phase variation of gonococcal pili by frameshift mutation in pilC, a novel gene for pilus assembly. EMBO J. 28:1991;477-488.
63. Taha M.K., Morand P.C., Pereira Y., Eugene E., Giorgini D., Larribe M., Nassif X. Pilus-mediated adhesion of Neisseria meningitidis: the essential role of cell contact-dependent transcriptional upregulation of the PilC1 protein. Mol. Microbiol. 373:1998;1153-1163.
64. Rudel T., Scheurerpflug I., Meyer T.F. Neisseria PilC protein identified as type-4 pilus tip-located adhesin. Nature. 96:1995;357-359.
65. Pujol C., Eugene E., Marceau M., Nassif X. The meningococcal PilT protein is required for induction of intimate attachment to epithelial cells following pilus-mediated adhesion. Proc. Natl. Acad. Sci. USA. 95:1999;4017-4022.
66. Wolfgang M., Park H.S., Hayes S.F., Van Putten J.P., Koomey M. Suppression of an absolute defect in type IV pilus biogenesis by loss-of-function mutations in pilT, a twitching motility gene in Neisseria gonorrhoeae. Proc. Natl. Acad. Sci. USA. 16:1998;14973-14978.
67. Tonjum T., Freitag N.E., Namork E., Koomey M. Identification and characterization of pilG, a highly conserved pilus-assembly gene in pathogenic Neisseria. Mol. Microbiol. 29:1995;451-464.
68. Tonjum T., Caugant D.A., Dunham S.A., Koomey M. Structure and function of repetitive sequence elements associated with a highly polymorphic domain of the Neisseria meningitidis PilQ protein. Mol. Microbiol. 10:1998;111-124.
69. Griffiss J.M., Schneider H., Mandrell R.E., Yamasaki R., Jarvis G.A., Kim J.J., Gibson B.W., Hamadeh R., Apicella M.A. Lipooligosaccharides: the principal glycolipids of the neisserial outer membrane. Rev. Infect. Dis. 24:(Suppl. 2):1988;S287-295.
70. Kahler C.M., Stephens D.S. Genetic basis for biosynthesis, structure, and function of meningococcal lipooligosaccharide (endotoxin). Crit. Rev. Microbiol. 57:1998;281-334.
71. Verheul A.F., Snippe H., Poolman J.T. Meningococcal lipopolysaccharides: virulence factor and potential vaccine component. Microbiol. Rev. 269:1993;34-49.
72. Yamasaki R., Kerwood D.E., Schneider H., Quinn K.P., Griffiss J.M., Mandrell R.E. The structure of lipooligosaccharide produced by Neisseria gonorrhoeae, strain 15253, isolated from a patient with disseminated infection. Evidence for a new glycosylation pathway of the gonococcal lipooligosaccharide. J. Biol. Chem. 6:1994;30345-30351.
73. Wyckoff T.J., Raetz C.R., Jackman J.E. Antibacterial and anti-inflammatory agents that target endotoxin. Trends Microbiol. 174:1998;154-159.
74. Kulshin V.A., Zahringer U., Lindner B., Frasch C.E., Tsai C.M., Dmitriev B.A., Rietschel E.T. Structural characterization of the lipid A component of pathogenic Neisseria meningitidis. J. Bacteriol. 307:1992;1793-1800.
75. Rahman M.M., Stephens D.S., Kahler C.M., Glushka J., Carlson R.W. The lipooligosaccharide (LOS) of Neisseria meningitidis serogroup B strain NMB contains L2, L3, and novel oligosaccharides, and lacks the lipid-A 4'-phosphate substituent. Carbohydr. Res. 13:1998;311-324.
76. Jones D.M., Borrow R., Fox A.J., Gray S., Cartwright K.A., Poolman J.T. The lipooligosaccharide immunotype as a virulence determinant in Neisseria meningitidis. Microb. Pathog. 172:1992;219-224.
77. Schneider H., Cross A.S., Kuschner R.A., Taylor D.N., Sadoff J.C., Boslego J.W., Deal C.D. Experimental human gonococcal urethritis: 250 Neisseria gonorrhoeae MS11mkC are infective. J. Infect. Dis. 16:1995;180-185.
78. Moran A.P., Prendergast M.M., Appelmelk B.J. Molecular mimicry of host structures by bacterial lipopolysaccharides and its contribution to disease. FEMS Immunol. Med. Microbiol. 271:1996;105-115.
79. Gilbert M., Watson D.C., Cunningham A.M., Jennings M.P., Young N.M., Wakarchuk W.W. Cloning of the lipooligosaccharide alpha-2, 3-sialyltransferase from the bacterial pathogens Neisseria meningitidis and Neisseria gonorrhoeae. J. Biol. Chem. 185:1996;28271-28276.
80. Vogel U., Hammerschmidt S., Frosch M. Sialic acids of both the capsule and the sialylated lipooligosaccharide of Neisseria meningitis serogroup B are prerequisites for virulence of meningococci in the infant rat. Med. Microbiol. Immunol. (Berl). 167:1996;81-87.
81. Stephens D.S., Spellman P.A., Swartley J.S. Effect of the (α2→8)-linked polysialic acid capsule on adherence of Neisseria meningitidis to human mucosal cells. J. Infect. Dis. 54:1993;475-479.
82. Bhattacharjee A.K., Jennings H.J., Kenny C.P., Martin A., Smith I.C. Structural determination of the polysaccharide antigens of Neisseria meningitidis serogroups Y, W-135, and BO1. Can. J. Biochem. 246:1976;1-8.
83. Liu T.Y., Gotschlich E.C., Jonssen E.K., Wysocki J.R. Studies on the meningococcal polysaccharides. I. Composition and chemical properties of the group A polysaccharide. J. Biol. Chem. 246:1971;2849-2858.
84. Liu T.Y., Gotschlich E.C., Dunne F.T., Jonssen E.K. Studies on the meningococcal polysaccharides. II. Composition and chemical properties of the group B and group C polysaccharide. J. Biol. Chem. 86:1971;4703-4712.
85. Frosch M., Weisgerber C., Meyer T.F. Molecular characterization and expression in Escherichia coli of the gene complex encoding the polysaccharide capsule of Neisseria meningitidis group B. Proc. Natl. Acad. Sci. USA. 178:1989;1669-1673.
86. Swartley J.S., Ahn J.H., Liu L.J., Kahler C.M., Stephens D.S. Expression of sialic acid and polysialic acid in serogroup B Neisseria meningitidis: divergent transcription of biosynthesis and transport operons through a common promoter region. J. Bacteriol. 180:1996;4052-4059.
87. Swartley J.S., Liu L.J., Miller Y.K., Martin L.E., Edupuganti S., Stephens D.S. Characterization of the gene cassette required for biosynthesis of the (α1→6)-linked N-acetyl-D-mannosamine-1-phosphate capsule of serogroup A Neisseria meningitidis. J. Bacteriol. 20:1998;1533-1539.
88. Hammerschmidt S., Muller A., Sillmann H., Muhlenhoff M., Borrow R., Fox A., Van Putten J., Zollinger W.D., Gerardy-Schahn R., Frosch M. 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. 15:1996;1211-1220.
89. Hammerschmidt S., Hilse R., Van Putten J.P., Gerardy-Schahn R., Unkmeir A., Frosch M. Modulation of cell surface sialic acid expression in Neisseria meningitidis via a transposable genetic element. EMBO J. 154:1996;192-198.
90. Masson L., Holbein B.E. Physiology of sialic acid capsular polysaccharide synthesis in serogroup B Neisseria meningitidis. J. Bacteriol. 99:1983;728-736.
91. Cartwright K.A., Stuart J.M., Jones D.M., Noah N.D. The Stonehouse survey: nasopharyngeal carriage of meningococci and Neisseria lactamica. Epidemiol. Infect. 66:1987;591-601.
92. Kahler C.M., Martin L.E., Shih G.C., Rahman M.M., Carlson R.W., Stephens D.S. The (α2→8)-linked polysialic acid capsule and lipooligosaccharide structure both contribute to the ability of serogroup B Neisseria meningitidis to resist the bactericidal activity of normal human serum. Infect. Immun. 27:1998;5939-5947.
93. De Vries F.P., Cole R., Dankert J., Frosch M., Van Putten J.P. Neisseria meningitidis producing the Opc adhesin binds epithelial cell proteoglycan receptors. Mol. Microbiol. 67:1998;1203-1212.
94. Lehmann A.K., Halstensen A., Aaberge I.S., Holst J., Michaelsen T.E., Sornes S., Wetzler L.M., Guttormsen H. Human opsonins induced during meningococcal disease recognize outer membrane proteins PorA and PorB. Infect. Immun. 65:1999;2552-2560.
95. Snapper C.M., Rosas F.R., Kehry M.R., Mond J.J., Wetzler L.M. Neisserial porins may provide critical second signals to polysaccharide-activated murine B cells for induction of immunoglobulin secretion. Infect. Immun. 67:1997;3203-3208.
96. Derrick J.P., Urwin R., Suker J., Feavers I.M., Maiden M.C. Structural and evolutionary inference from molecular variation in Neisseria porins. Infect. Immun. 14:1999;2406-2413.
97. Claassen I., Meylis J., Van Der Ley P., Peeters C., Brons H., Robert J., Borsboom D., Van Der Ark A., Van Straaten I., Roholl P., Kuipers B., Poolman J. Production, characterization and control of a Neisseria meningitidis hexavalent class 1 outer membrane protein containing vesicle vaccine. Vaccine. 30:1996;1001-1008.
98. Feavers I.M., Maiden M.C. A gonococcal porA pseudogene: implications for understanding the evolution and pathogenicity of Neisseria gonorrhoeae. Mol. Microbiol. 30:1998;647-656.
99. Newcombe J., Cartwright K., Dyer S., McFadden J. Naturally occurring insertional inactivation of the porA gene of Neisseria meningitidis by integration of IS1301. Mol. Micriobiol. 67:1998;453-454.
100. Van Der Ende A., Hopman C.T., Dankert J. Deletion of porA by recombination between clusters of repetitive extragenic palindromic sequences in Neiserria meningitidis. Infect. Immun. 32:1999;2928-2934.
101. Vogel U., Frosch M. Mechanisms of neisserial serum resistance. Mol. Microbiol. 142:1999;1133-1139.
102. Blake M.S., Gotschlich E.C. Inouy E.M. Bacterial outer membranes as model systems. 1987;377-400 John Wiley & Sons, New York.
103. Weel J.F., Van Putten J.P. Fate of the major outer membrane protein P. IA in early and late events of gonococcal infection of epithelial cells. Res. Microbiol. 85:1991;985-993.
104. Rudel T., Schmid A., Benz R., Kolb H.A., Lang F., Meyer T.F. Modulation of Neisseria porin (PorB) by cytosolic ATP/GTP of target cells: parallels between pathogen accommodation and mitochondrial endosymbiosis. Cell. 18:1996;391-402.
105. Muller A., Gunther D., Dux F., Naumann M., Meyer T.F., Rudel T. Neisserial porin (PorB) causes rapid calcium influx in target cells and induces apoptosis by the activation of cysteine proteases. EMBO J. 11:1999;339-352.
106. Munkley A., Tinsley C.R., Virji M., Heckels J.E. Blocking of bactericidal killing of Neisseria meningitidis by antibodies directed against class 4 outer membrane protein. Microb. Pathog. 164:1991;447-452.
107. Achtman M., Wall R.A., Bopp M., Kusecek B., Morelli G., Saken E., Hassan-King M. Variation in class 5 protein expression by serogroup A meningococci during a meningitis epidemic. J. Infect. Dis. 22:1991;375-382.
108. Virji M., Watt S.M., Barker S., Makepeace K., Doyonnas R. The N-domain of the human CD66a adhesion molecule is a target for Opa proteins of Neisseria meningitidis and Neisseria gonorrhoeae. Mol. Microbiol. 14:1996;929-939.
109. Virji M., Makepeace K., Moxon E.R. Distinct mechanisms of interactions of Opc-expressing meningococci at apical and basolateral surfaces of human endothelial cells; the role of integrins in apical interactions. Mol. Microbiol. 33:1994;173-184.
110. Zhu P., Morelli G., Achtman M. The opcA and YopcB regions in Neisseria: genes, pseudogenes, deletions, insertion elements and DNA islands. Mol. Microbiol. 23:1999;635-650.
111. Belland R.J., Morrison S.G., Carlson J.H., Hogan D.M. Promoter strength influences phase variation of neisserial opa genes. Mol. Microbiol. 13:1997;123-135.
112. Sarkari J., Pandit N., Moxon E.R., Achtman M. Variable expression of the Opc outer membrane protein in Neisseria meningitidis is caused by size variation of a promoter containing poly-cytidine. Mol. Microbiol. 64:1994;207-217.
113. De Vries F.P., Van Der Ende A., Van Putten J.P., Dankert J. Invasion of primary nasopharyngeal epithelial cells by Neisseria meningitidis is controlled by phase variation of multiple surface antigens. Infect. Immun. 10:1996;2998-3006.
114. Virji M., Makepeace K., Ferguson D.J., Achtman M., Moxon E.R. Meningococcal Opa and Opc proteins: their role in colonization and invasion of human epithelial and endothelial cells. Mol. Microbiol. 32:1993;499-510.
115. Schryvers A.B., Stojiljkovic I. Iron acquisition systems in the pathogenic Neisseria. Mol. Microbiol. 178:1999;1117-1123.
116. Stojiljkovic I., Larson J., Hwa V., Anic S., So M. HmbR outer membrane receptors of pathogenic Neisseria spp.: iron-regulated, hemoglobin-binding proteins with a high level of primary structure conservation. J. Bacteriol. 32:1996;4670-4678.
117. Lewis L.A., Gipson M., Hartman K., Ownbey T., Vaughn J., Dyer D.W. Phase variation of HpuAB and HmbR, two distinct hemogobin receptors of Neisseria meningitidis DNM2. Mol. Microbiol. 4:1999;977-989.
118. Gray-Owen S.D., Schryvers A.B. Bacterial transferrin and lactoferrin receptors. Trends Microbiol. 25:1996;185-191.
119. Retzer M.D., Yu R., Zhang Y., Gonzalez G.C., Schryvers A.B. Discrimination between apo and iron-loaded forms of transferrin by transferrin binding protein B and its N-terminal subfragment. Microb. Pathog. 110:1998;175-180.
120. Rokbi B., Mazarin V., Maitre-Wilmotte G., Quentin-Millet M.J. Identification of two major families of transferrin receptors among Neisseria meningitidis strains based on antigenic and genomic features. FEMS Microbiol. Lett. 27:1993;51-57.
121. Pettersson A., Prinz T., Umar A., Van Der Biezen J., Tommassen J. Molecular characterization of LbpB, the second lactoferrin-binding protein of Neisseria meningitidis. Mol. Microbiol. 23:1998;599-610.
122. Lewis L.A., Gray E., Wang Y.P., Roe B.A., Dyer D.W. Molecular characterization of hpuAB, the haemoglobin-haptoglobin-utilization operon of Neisseria meningitidis. Mol. Microbiol. 29:1997;737-749.
123. Hershko C. The fate of circulating haemoglobin. Br. J. Haematol. 65:1975;199-204.
124. Rokbi B., Mignon M., Maitre-Wilmotte G., Lissolo L., Danve B., Caugant D.A., Quentin-Millet M.J. Evaluation of recombinant transferrin-binding protein B variants from Neisseria meningitidis for their ability to induce cross-reactive and bactericidal antibodies against a genetically diverse collection of serogroup B strains. Infect. Immun. 95:1997;55-63.
125. Kroll J.S., Wilks K.E., Farrant J.L., Langford P.R. Natural genetic exchange between Haemophilus and Neisseria: intergeneric transfer of chromosomal genes between major human pathogens. Proc. Natl. Acad. Sci. USA. 67:1998;12381-12385.
126. Bart A., Dankert J., Van Der Ende A. Antigenic variation of the class I outer membrane protein in hyperendemic Neisseria meningitidis strains in the Netherlands. Infect. Immun. 12:1999;3842-3846.
127. Suker J., Feavers I.M., Achtman M., Morelli G., Wang J.F., Maiden M.C. The porA gene in serogroup A meningococci: evolutionary stability and mechanism of genetic variation. Mol. Microbiol. 5:1994;253-265.
128. Frosch M., Edwards U., Bousset K., Krausse B., Weisgerber C. Evidence for a common molecular origin of the capsule gene loci in gram-negative bacteria expressing group II capsular polysaccharides. Mol. Microbiol. 168:1991;1251-1263.
129. Mandrell R.E., Griffiss J.M., Macher B.A. Lipooligosaccharides (LOS) of Neisseria gonorrhoeae and Neisseria meningitidis have components that are immunochemically similar to precursors of human blood group antigens. Carbohydrate sequence specificity of the mouse monoclonal antibodies that recognize crossreacting antigens on LOS and human erythrocytes. J. Exp. M. 138:1988;107-126.
130. Finne J., Bitter-Suermann D., Goridis C., Finne U. An IgG monoclonal antibody to group B meningococci cross-reacts with developmentally regulated polysialic acid units of glycoproteins in neural and extraneural tissues. J. Immunol. 59:1987;4402-4407.
131. Tsai C.M., Civin C.I. Eight lipooligosaccharides of Neisseria meningitidis react with a monoclonal antibody which binds lacto-N-neotetraose (Gal 1-4GlcNAc 1-3Gal 1-4Glc). Infect. Immun. 14:1991;3604-3609.
132. Mandrell R.E., Griffiss J.M., Smith H., Cole J.A. Distribution of a lipooligosaccharide-specific sialyltransferase in pathogenic and non-pathogenic Neisseria. Microb. Pathog. 10:1993;315-327.
133. McAllister C.F., Stephens D.S. Analysis in Neisseria meningitidis and other Neisseria species of genes homologous to the FKBP immunophilin family. Mol. Microbiol. 138:1993;13-23.
134. Devoe I.W., Gilchrist J.E. Release of endotoxin in the form of cell wall blebs during in vitro growth of Neisseria meningitidis. J. Exp. M. 4:1973;1156-1167.
135. Poolman J.T. Development of a meningococcal vaccine. Infect. Agents Dis. 126:1995;13-28.
136. Wyle F.A., Artenstein M.S., Brandt B.L., Tramont E.C., Kasper D.L., Altieri P.L., Berman S.L., Lowenthal J.P. Immunologic response of man to group B meningococcal polysaccharide vaccines. J. Infect. Dis. 185:1972;514-521.
137. Pon R.A., Lussier M., Yang Q.L., Jennings H.J. N-Propionylated group B meningococcal polysaccharide mimics a unique bactericidal capsular epitope in group B Neisseria meningitidis. J. Exp. M. 15:1997;1929-1938.
138. Andersen S.R., Bjune G., Hoiby E.A., Michaelsen T.E., Aase A., Rye U., Jantzen E. Outer membrane vesicle vaccines made from short-chain lipopolysaccharide mutants of serogroup B Neisseria meningitidis: effect of the carbohydrate chain length on the immune response. Vaccine. 67:1997;1225-1234.
139. Saunders N.B., Shoemaker D.R., Brandt B.L., Moran E.E., Larsen T., Zollinger W.D. Immunogenicity of intranasally administered meningococcal native outer membrane vesicles in mice. Infect. Immun. 350:1999;113-119.
140. Robbins J.B., Towne D.W., Gotschlich E.C., Schneerson R. 'Love's labours lost': failure to implement mass vaccination against group A meningococcal meningitis in sub-Saharan Africa. Lancet. 62:1997;880-882.
141. Anderson E.L., Bowers T., Mink C.M., Kennedy D.J., Belshe R.B., Harakeh H., Pais L., Holder P., Carlone G.M. Safety and immunogenicity of meningococcal A and C polysaccharide conjugate vaccine in adults. Infect. Immun. 171:1994;3391-3395.
142. Twumasi P.A. Jr, Kumah S., Leach A., O'Dempsey T.J., Ceesay S.J., Todd J., Broome C.V., Carlone G.M., Pais L.B., Holder P.K. A trial of a group A plus group C meningococcal polysaccharide-protein conjugate vaccine in African infants. J. Infect. Dis. 1995;632-638.