Differential in vitro infectious abilities of two common Japan-specific sequence-type (ST) clones of disease-associated ST-2032 and carrier-associated ST-2046 Neisseria meningitidis strains in human endothelial and epithelial cell lines

FEMS Immunology and Medical Microbiology

Volumn 52, Issue 1, 2008, Pages 36-46

  Takahashi, Hideyuki ^a   Kim, Kwang Sik ^b   Watanabe, Haruo ^a  

^a NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Japan specific; MLST; Neisseria meningitidis; ST 2032; ST 2046

Indexed keywords

BACTERIAL PROTEIN; LIPOOLIGOSACCHARIDE; PILIN; PROTEIN OPA; PROTEIN OPC; PROTEIN PILC; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL MENINGITIS; BACTERIAL STRAIN; BACTERIUM ADHERENCE; CONTROLLED STUDY; ENDOTHELIUM CELL; EPITHELIUM CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; NEISSERIA MENINGITIDIS; NONHUMAN; PATHOGENICITY; PRIORITY JOURNAL; PROTEIN EXPRESSION;

BACTERIAL ADHESION; BACTERIAL PROTEINS; BLOTTING, WESTERN; CELL LINE; COLONY COUNT, MICROBIAL; ENDOTHELIAL CELLS; EPITHELIAL CELLS; HUMANS; NEISSERIA MENINGITIDIS;

EID: 38149042085     PISSN: 09288244     EISSN: 1574695X     Source Type: Journal    
DOI: 10.1111/j.1574-695X.2007.00342.x     Document Type: Article

References (51)

1. Achtman M, Kusecek B, Morelli G et al 1992) A comparison of the variable antigens expressed by clone IV-1 and subgroup III of Neisseria meningitidis serogroup A. J Infect Dis 165 : 53 68.
2. Albiger B, Johansson L Jonsson AB (2003) Lipooligosaccharide-deficient Neisseria meningitidis shows altered pilus-associated characteristics. Infect Immun 71 : 155 162.
3. Berrington AW, Tan YC, Srikhanta Y, Kuipers B, van der Ley P, Peak IR Jennings MP (2002) Phase variation in meningococcal lipooligosaccharide biosynthesis genes. FEMS Immunol Med Microbiol 34 : 267 275.
4. Cartwright KA, Stuart JM, Jones DM Noah ND (1987) The Stonehouse survey: nasopharyngeal carriage of meningococci and Neisseria lactamica. Epidemiol Infect 99 : 591 601.
5. Caugant DA, Mocca LF, Frasch CE, Froholm LO, Zollinger WD Selander RK (1987) Genetic structure of populations in relation to serogroup, serotype, and outer membrane protein pattern. J Bacteriol 169 : 2781 2792.
6. Caugant DA, Bol P, Hoiby EA, Zanen HC Froholm LO (1990) Clones of serogroup B Neisseria meningitidis causing systemic disease in the Netherlands, 1958-1986. J Infect Dis 162 : 867 874.
7. Dehio C, Gray-Owen SD Meyer TF (1998) The role of neisserial Opa proteins in interactions with host cells. Trends Microbiol 6 : 489 495.
8. Frosch M, Schultz E, Glenn-Calvo E Meyer TF (1990) Generation of capsule-deficient Neisseria meningitidis strains by homologous recombination. Mol Microbiol 4 : 1215 1218.
9. Hammerschmidt S, Birkholz C, Zahringer U, Robertson BD, van Putten J, Ebeling O Frosch M (1994) Contribution of genes from the capsule gene complex (cps) to lipooligosaccharide biosynthesis and serum resistance in Neisseria meningitidis. Mol Microbiol 11 : 885 896.
10. Hammerschmidt S, Hilse R, van Putten JP, Gerardy-Schahn R, Unkmeir A Frosch M (1996a) Modulation of cell surface sialic acid expression in Neisseria meningitidis via a transposable genetic element. EMBO J 15 : 192 198.
11. Hammerschmidt S, Muller A, Sillmann H et al 1996b) 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 : 1211 1220.
12. Hardy SJ, Christodoulides M, Weller RO Heckels JE (2000) Interactions of Neisseria meningitidis with cells of the human meninges. Mol Microbiol 36 : 817 829.
13. Jennings MP, Srikhanta YN, Moxon ER, Kramer M, Poolman JT, Kuipers B van der Ley P (1999) The genetic basis of the phase variation repertoire of lipopolysaccharide immunotypes in Neisseria meningitidis. Microbiology 145 : 3013 3021.
14. Kahler CM, Lyons-Schindler S, Choudhury B, Glushka J, Carlson RW Stephens DS (2006) O-acetylation of the terminal N-acetylglucosamine of the lipooligosaccharide inner core in Neisseria meningitidis. Influence on inner core structure and assembly. J Biol Chem 281 : 19939 19948.
15. Kurzai O, Schmitt C, Claus H, Vogel U, Frosch M Kolb-Maurer A (2005) Carbohydrate composition of meningococcal lipopolysaccharide modulates the interaction of Neisseria meningitidis with human dendritic cells. Cell Microbiol 7 : 1319 1334.
16. Maiden MC, Bygraves JA, Feil E et al 1998) Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc Natl Acad Sci USA 95 : 3140 3145.
17. Malorny B, Morelli G, Kusecek B, Kolberg J Achtman M (1998) Sequence diversity, predicted two-dimensional protein structure, and epitope mapping of neisserial Opa proteins. J Bacteriol 180 : 1323 1330.
18. Mayer LW, Reeves MW, Al-Hamdan N et al 2002) Outbreak of W135 meningococcal disease in 2000: not emergence of a new W135 strain but clonal expansion within the electophoretic type-37 complex. J Infect Dis 185 : 1596 1605.
19. Moore PS, Reeves MW, Schwartz B, Gellin BG Broome CV (1989) Intercontinental spread of an epidemic group A Neisseria meningitidis strain. Lancet 2 : 260 263.
20. Nassif X (1999) Interaction mechanisms of encapsulated meningococci with eucaryotic cell: what does this tell us about the crossing of the blood-brain barrier by Neisseria meningitidis? Curr Opin Microbiol 2 : 71 77.
21. Nassif X So M (1995) Interaction of pathogenic neisseriae with nonphagocytic cells. Clin Microbiol Rev 8 : 376 388.
22. Nassif X, Lowy J, Stenberg P, O'Gaora P, Ganji A So M (1993) Antigenic variation of pilin regulates adhesion of Neisseria meningitidis to human epithelial cells. Mol Microbiol 8 : 719 725.
23. Nassif X, Beretti JL, Lowy J et al 1994) Roles of pilin and PilC in adhesion of Neisseria meningitidis to human epithelial and endothelial cells. Proc Natl Acad Sci USA 91 : 3769 3773.
24. Nassif X, Marceau M, Pujol C, Pron B, Beretti JL Taha MK (1997) Type-4 pili and meningococcal adhesiveness. Gene 192 : 149 153.
25. Nassif X, Pujol C, Morand P Eugene E (1999) Interactions of pathogenic Neisseria with host cells. Is it possible to assemble the puzzle? Mol Microbiol 32 : 1124 1132.
26. Plant L, Sundqvist J, Zughaier S, Lovkvist L, Stephens DS Jonsson AB (2006) Lipooligosaccharide structure contributes to multiple steps in the virulence of Neisseria meningitidis. Infect Immun 74 : 1360 1367.
27. Poolman JT, Lind I, Jonsdottir K, Froholm LO, Jones DM Zanen HC (1986) Meningococcal serotypes and serogroup B disease in north-west Europe. Lancet 2 : 555 558.
28. Popovic T, Sacchi CT, Reeves MW et al 2000) Neisseria meningitidis serogroup W135 isolates associated with the ET-37 complex. Emerg Infect Dis 6 : 428 429.
29. Seiler A, Reinhardt R, Sarkari J, Caugant DA Achtman M (1996) Allelic polymorphism and site-specific recombination in the opc locus of Neisseria meningitidis. Mol Microbiol 19 : 841 856.
30. Selander RK, Caugant DA, Ochman H, Musser JM, Gilmour MN Whittam TS (1986) Methods of multilocus enzyme electrophoresis for bacterial population genetics and systematics. Appl Environ Microbiol 51 : 873 884.
31. Sjolinder H Jonsson AB (2007) Imaging of disease dynamics during meningococcal sepsis. PLoS ONE 2 : e241.
32. Stark MJ (1987) Multicopy expression vectors carrying the lac repressor gene for regulated high-level expression of genes in Escherichia coli. Gene 51 : 255 267.
33. Steeghs L, van Vliet SJ, Uronen-Hansson H et al 2006) Neisseria meningitidis expressing lgtB lipopolysaccharide targets DC-SIGN and modulates dendritic cell function. Cell Microbiol 8 : 316 325.
34. Stephens DS, Spellman PA Swartley JS (1993) Effect of the (alpha 2->8)-linked polysialic acid capsule on adherence of Neisseria meningitidis to human mucosal cells. J Infect Dis 167 : 475 479.
35. Stins MF, Gilles F Kim KS (1997) Selective expression of adhesion molecules on human brain microvascular endothelial cells. J Neuroimmunol 76 : 81 90.
36. Swartley JS, Liu LJ, Miller YK, Martin LE, Edupuganti S Stephens DS (1998) Characterization of the gene cassette required for biosynthesis of the (alpha1->6)-linked N-acetyl-d-mannosamine-1-phosphate capsule of serogroup A Neisseria meningitidis. J Bacteriol 180 : 1533 1539.
37. Takahashi H Watanabe H (2002) A broad-host-range vector of incompatibility group Q can work as a plasmid vector in Neisseria meningitidis: a new genetical tool. Microbiology 148 : 229 236.
38. Takahashi H, Kuroki T, Watanabe Y, Tanaka H, Inouye H, Yamai S Watanabe H (2004) Characterization of Neisseria meningitidis isolates collected from 1974 to 2003 in Japan by multilocus sequence typing. J Med Microbiol 53 : 657 662.
39. Tanaka H, Kuroki T, Watanabe Y et al 2005) Isolation of Neisseria meningitidis from healthy persons in Japan. Kansenshogaku Zasshi 79 : 527 533.
40. Townsend R, Goodwin L, Stevanin TM, Silcocks PB, Parker A, Maiden MC Read RC (2002) Invasion by Neisseria meningitidis varies widely between clones and among nasopharyngeal mucosae derived from adult human hosts. Microbiology 148 : 1467 1474.
41. Tzeng YL Stephens DS (2000) Epidemiology and pathogenesis of Neisseria meningitidis. Microbes Infect 2 : 687 700.
42. Unkmeir A, Latsch K, Dietrich G et al 2002) Fibronectin mediates Opc-dependent internalization of Neisseria meningitidis in human brain microvascular endothelial cells. Mol Microbiol 46 : 933 946.
43. Virji M, Kayhty H, Ferguson DJ, Alexandrescu C, Heckels JE Moxon ER (1991a) The role of pili in the interactions of pathogenic Neisseria with cultured human endothelial cells. Mol Microbiol 5 : 1831 1841.
44. Virji M, Kayhty H, Ferguson DJ, Alexandrescu C Moxon ER (1991b) Interactions of Haemophilus influenzae with cultured human endothelial cells. Microb Pathog 10 : 231 245.
45. Virji M, Alexandrescu C, Ferguson DJ, Saunders JR Moxon ER (1992a) Variations in the expression of pili: the effect on adherence of Neisseria meningitidis to human epithelial and endothelial cells. Mol Microbiol 6 : 1271 1279.
46. Virji M, Makepeace K, Ferguson DJ, Achtman M, Sarkari J Moxon ER (1992b) Expression of the Opc protein correlates with invasion of epithelial and endothelial cells by Neisseria meningitidis. Mol Microbiol 6 : 2785 2795.
47. Virji M, Makepeace K, Ferguson DJ, Achtman M Moxon ER (1993) Meningococcal Opa and Opc proteins: their role in colonization and invasion of human epithelial and endothelial cells. Mol Microbiol 10 : 499 510.
48. Virji M, Makepeace K, Peak I, Payne G, Saunders JR, Ferguson DJ Moxon ER (1995) Functional implications of the expression of PilC proteins in meningococci. Mol Microbiol 16 : 1087 1097.
49. Vogel U Frosch M (1999) Mechanisms of neisserial serum resistance. Mol Microbiol 32 : 1133 1139.
50. WHO (1998) Control of Epidemic Meningococcal Disease. WHO Practical Guidelines, WHO, Geneva.
51. Yazdankhah SP Caugant DA (2004) Neisseria meningitidis: an overview of the carriage state. J Med Microbiol 53 : 821 832.