Characterization of novel structural features in the lipopolysaccharide of nondisease associated nontypeable Haemophilus influenzae

European Journal of Biochemistry

Volumn 271, Issue 5, 2004, Pages 941-953

  Landerholm, Malin K ^a   Li, Jianjun ^b   Richards, James C ^b   Hood, Derek W ^c   Moxon, E Richard ^c   Schweda, Elke K H ^a  

^a SÖDERTÖRN UNIVERSITY   (Sweden)

^b NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Carriage; ESI MS; Haemophilus influenzae; Lipopolysaccharide; NMR

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; GLYCINE; HEPTOSE; HEXOSE; LIPID A; N ACETYLNEURAMINIC ACID; OLIGOSACCHARIDE; PHOSPHORYLCHOLINE;

ACETYLATION; ARTICLE; BACTERIAL STRAIN; BACTERIUM IDENTIFICATION; CAPILLARY ELECTROPHORESIS; CARBOHYDRATE ANALYSIS; CHILD; CONTROLLED STUDY; DEACYLATION; ELECTROSPRAY MASS SPECTROMETRY; HAEMOPHILUS INFLUENZAE; HUMAN; LINKAGE ANALYSIS; NASOPHARYNX; NONHUMAN; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL;

CARBOHYDRATE CONFORMATION; CARBOHYDRATE SEQUENCE; HAEMOPHILUS INFLUENZAE; HUMANS; INFANT; LIPOPOLYSACCHARIDES; MOLECULAR SEQUENCE DATA; NASOPHARYNX; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; OLIGOSACCHARIDES; OTITIS MEDIA; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION;

BACTERIA (MICROORGANISMS); HAEMOPHILUS INFLUENZAE; NEGIBACTERIA;

EID: 1542344866     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1432-1033.2004.03996.x     Document Type: Article

References (42)

1. Teele, D.W., Klein, J.O., Rosner, B., Bratton, L., Fisch, G.R., Mathieu, O.R., Porter, P.J., Starobin, S.G., Tarlin, L.D. & Younes, R.P. (1983) Middle ear disease and the practice of pediatrics. Burden during the first five years of life. JAMA 249, 1026-1029.
2. Trottier, S., Stenberg, K. & Svanborg-Eden, C. (1989) Turnover of nontypeable Haemophilus influenzae in the nasopharynges of healthy children. J. Clin. Microbiol. 27, 2175-2179.
3. Peerbooms, P.G.H., Engelen, M.N., Stokman, D.A.J., van Benthem, B.H.B., van Weert, M.-L., Bruisten, S.M., van Belkum, A. & Coutinho, R.A. (2002) Nasopharyngeal carriage of potential bacterial pathogens related to day care attendance, with special reference to the molecular epidemiology of Haemophilus influenzae. J. Clin. Microbiol. 40, 2832-2836.
4. Faden, H., Duffy, L., Wasielewski, R., Wolf, J., Krystofik, D. & Tung, Y. (1997) Relationship between nasopharyngeal colonization and the development of otitis media in children. Tonawanda/Williamsville Pediatrics. J. Infect. Dis. 175, 1440-1445.
5. Vesa, S., Kleemola, M., Blomqvist, S., Takala, A., Kilpi, T. & Hovi, T. (2001) Epidemiology of documented viral respiratory infections and acute otitis media in a cohort of children followed from two to twenty-four months of age. Pediatr. Infect. Dis. J. 20, 1113-1123.
6. Fleischmann, R.D., Adams, M.D., White, O., Clayton, R.A., Kirkness, E.F., Kerlavage, A.R., Bult, C.J., Tomb, J.-F., Dougherty, B.A., Merrick, J.M., et al. (1995) Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269, 496-512.
7. Hood, D.W., Deadman, M.E., Allen, T., Masoud, H., Martin, A., Brisson, J.R., Fleischmann, R., Venter, J.C., Richards, J.C. & Moxon, E.R. (1996) Use of the complete genome sequence information of Haemophilus influenzae strain Rd to investigate lipopolysaccharide biosynthesis. Mol. Microbiol. 22, 951-965.
8. Hood, D.W., Cox, A.D., Wakarchuk, W.W., Schur, M., Schweda, E.K.H., Walsh, S.L., Deadman, M.E., Martin, A., Moxon, E.R. & Richards, J.C. (2001) Genetic basis for expression of the major globotetraose-containing lipopolysaccharide from H. influenzae strain Rd (RM118). Glycobiology 11, 957-967.
9. Risberg, A., Masoud, H., Martin, A., Richards, J.C., Moxon, E.R. & Schweda, E.K.H. (1999) Structural analysis of the lipopolysaccharide oligosaccharide epitopes expressed by a capsule-deficient strain of Haemophilus influenzae Rd. Eur. J. Biochem. 261, 171-180.
10. Månsson, M., Hood, D.W., Li, J., Richards, J.C., Moxon, E.R. & Schweda, E.K.H. (2002) Structural analysis of the lipopolysaccharide from nontypeable Haemophilus influenzae strain 1003. Eur. J. Biochem. 269, 808-818.
11. Månsson, M., Hood, D.W., Moxon, E.R. & Schweda, E.K.H. (2003) Structural diversity in lipopolysaccharide expression in nontypeable Haemophilus influenzae: Identification of L-glycero-D-manno-heptose in the outer-core region in three clinical isolates. Eur. J. Biochem. 270, 610-624.
12. Masoud, H., Moxon, E.R., Martin, A., Krajcarski, D. & Richards, J.C. (1997) Structure of the variable and conserved lipopolysaccharide oligosaccharide epitopes expressed by Haemophilus influenzae serotype b strain Eagan. Biochemistry 36, 2091-2103.
13. Månsson, M., Hood, D.W., Li, J., Richards, J.C., Moxon, E.R. & Schweda, E.K.H. (2001) A new structural type for Haemophilus influenzae lipopolysaccharide. Structural analysis of the lipopolysaccharide from nontypeable Haemophilus influenzae strain 486. Eur. J. Biochem. 268, 2148-2159.
14. Yildirim, H.H., Hood, D.W., Moxon, E.R. & Schweda, E.K.H. (2003) Structural analysis of lipopolysaccharides from Haemophilus influenzae serotype f. Structural diversity observed in three strains. Eur. J. Biochem. 270, 3153-3167.
15. Hood, D.W., Makepeace, K., Deadman, M.E., Rest, R.F., Thibault, P., Martin, A., Richards, J.C. & Moxon, E.R. (1999) Sialic acid in the lipopolysaccharide of Haemophilus influenzae: strain distribution, influence on serum resistance and structural characterization. Mol. Microbiol. 33, 679-692.
16. Li, J., Bauer, S.H.J., Månsson, M., Moxon, E.R., Richards, J.C. & Schweda, E.K.H. (2001) Glycine is a common substituent of the inner-core in Haemophilus influenzae lipopolysaccharide. Glycobiology 11, 1009-1015.
17. Schweda, E.K.H., Li, J., Moxon, E.R. & Richards, J.C. (2002) Structural analysis of lipopolysaccharide oligosaccharide epitopes expressed by non-typeable Haemophilus influenzae strain 176. Carbohydr. Res. 337, 409-420.
18. Bauer, S.H.J., Månsson, M., Hood, D.W., Richards, J.C., Moxon, E.R. & Schweda, E.K.H. (2001) A rapid and sensitive procedure for determination of sialic acid in lipopolysaccharides of Haemophilus influenzae: a survey of 24 non-typeable H. influenzae strains. Carbohydr. Res. 335, 251-260.
19. Månsson, M., Hood, D.W., Moxon, E.R. & Schweda, E.K.H. (2003) Structural characterization of a novel branching pattern in the lipopolysaccharide from nontypeable Haemophilus influenzae. Eur. J. Biochem. 270, 2979-2991.
20. Schweda, E.K.H., Landerholm, M.K., Li, J., Moxon, E.R. & Richards, J.C. (2003) Structural profiling of lipopolysaccharide glycoforms expressed by non-typeable Haemophilus influenzae: Phenotypic similarities between NTHi 162 and the genome strain, Rd. Carbohydr. Res. 338, 2731-2744.
21. Bouchet, V., Hood, D.W., Li, J., Brisson, J.-R., Randle, G.A., Martin, A., Li, Z., Goldstein, R., Schweda, E.K.H., Pelton, S.I., Richards, J.C. & Moxon, E.R. (2003) Host-derived sialic acid is incorporated into Haemophilus influenzae lipopolysaccharide and is a major virulence factor in experimental otitis media. Proc. Natl Acad. Sci. USA 100, 8898-8903.
22. Cody, A.J., Field, D., Feil E.J., Stringer, S., Deadman, M.E., Tsolaki, A.G., Gratz, B., Bouchet, V., Goldstein, R., Hood, D.W. & Moxon, E.R. (2003) High rates of recombination in otitis media isolates of non-typeable Haemophilus influenzae. Infect. Genet. Evol. 3, 57-66.
23. Meats, E., Feil, E.J., Stinger, S., Cody, A.J., Goldstein, R., Kroll, J.S., Popovic, T. & Spratt, B.G. (2003) Characterization of encapsulated and noncapsulated Haemophilus influenzae and determination of phylogenetic relationships by multilocus sequence typing. J. Clin. Microbiol. 41, 1623-1636.
24. Kilpi, T., Herva, E., Kaijalainen, T., Syrjänen, R. & Takala, A.K. (2001) Bacteriology of acute otitis media in a cohort of Finnish children followed for the first two years of life. Pediatr. Infect. Dis. J. 20, 654-662.
25. Eskola, J., Kilpi, T., Palmu, A., Jokinen, J., Haapakoski, J., Herva, E., Takala, A., Kayhty, H., Karma, P., Kohberger, R., Siber, G. & Makelä, H. (2001) Efficacy of a pneumococcal conjugate vaccine against acute otitis media. N. Engl. J. Med. 344, 403-409.
26. Holst, O., Brade, L., Kosma, P. & Brade, H. (1991) Structure, serological specificity, and synthesis of artificial glycoconjugates representing the genus-specific lipopolysaccharide epitope of Chlamydia spp. J. Bacteriol. 173, 1862-1866.
27. Kussak, A. & Weintraub, A. (2002) Quadrupole ion-trap mass spectrometry to locate fatty acids on lipid A from Gram-negative bacteria. Anal. Biochem. 307, 131-137.
28. Sawardeker, J.S., Sloneker, J.H. & Jeanes, A. (1965) Quantitative determination of monosaccharides as their alditol acetates by gas liquid chromatography. Anal. Chem. 37, 1602-1604.
29. Blakeney, A.B. & Stone, B.A. (1985) Methylation of carbohydrates with lithium methylsulphinyl carbanion. Carbohydr. Res. 140, 319-324.
30. Gerwig, G.J., Kamerling, J.P. & Vliegenthart, J.F.G. (1979) Determination of the absolute configuration of monosaccharides in complex carbohydrates by capillary G.L.C. Carbohydr. Res. 77, 1-7.
31. Helander, I.M., Lindner, B., Brade, H., Altmann, K., Lindberg, A.A., Rietschel, E.T. & Zähringer, U. (1988) Chemical structure of the lipopolysaccharide of Haemophilus influenzae strain I-69 Rd-/ b+. Description of a novel deep-rough chemotype. Eur J. Biochem. 177, 483-492.
32. Jansson, P.-E., Kenne, L. & Schweda, E. (1987) Nuclear magnetic resonance and conformational studies on monoacetylated methyl D-gluco-and D-galacto-pyranosids. J. Chem. Soc. Perkin Trans. I, 377-383.
33. Phillips, N.J., Apicella, M.A., Griffiss, J.M. & Gibson, B.W. (1992) Structural characterization of the cell surface lipooligosaccharides from a nontypable strain of Haemophilus influenzae. Biochemistry 31, 4515-4526.
34. Rahman, M.M., Gu, X.-X., Tsai, C.-M., Kolli, V.S.K. & Carlson, R.W. (1999) The structural heterogeneity of the lipooligosaccharide (LOS) expressed by pathogenic non-typeable Haemophilus influenzae strain NTHi 9274. Glycobiology 9, 1371-1380.
35. Cox, A.D., Masoud, H., Thibault, P., Brisson, J.-R., van der Zwan, M., Perry, M.B. & Richards, J.C. (2001) Structural analysis of the lipopolysaccharide from the nontypable Haemophilus influenzae strain SB 33. Eur. J. Biochem. 268, 5278-5286.
36. Masoud, H., Martin, A., Thibault, P., Moxon, E.R. & Richards, J.C. (2003) Structure of extended lipopolysaccharide glycoforms containing two globotriose units in Haemophilus influenzae serotype b strain RM7004. Biochemistry 42, 4463-4475.
37. Weiser, J.N., Pan, N., McGowan, K.L., Musher, D., Martin, A. & Richards, J. (1998) 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, 631-640.
38. Schweda, E.K.H., Brisson, J.-R., Alvelius, G., Martin, A., Weiser, J.N., Hood, D.W., Moxon, E.R. & Richards, J.C. (2000) Characterization of the phosphocholine substituted oligosaccharide in lipopolysaccharides of type b Haemophilus influenzae. Eur. J. Biochem. 261, 1-12.
39. Weiser, J.N., Shchepetov, M. & Chong, S.T.H. (1997) Decoration of lipopolysaccharide with phosphorylcholine: a phase-variable characteristic of Haemophilus influenzae. Infect. Immunity 65, 943-950.
40. Lysenko, E., Richards, J.C., Cox, A.D., Stewart, A., Martin, A., Kapoor, M. & Weiser, J.N. (2000) The position of phosphorylcholine on the lipopolysaccharide of Haemophilus influenzae affects binding and sensitivity to C-reactive protein-mediated killing. Mol. Microbiol. 35, 234-245.
41. Hood, D.W., Cox, A.D., Gilbert, M., Makepeace, K., Walsh, S., Deadman, M.E., Cody, A., Martin, A., Månsson, M., Schweda, E.K.H., Brisson, J.-R., Richards, J.C., Moxon, E.R. & Wakarchuk, W.W. (2001) Identification of a lipopolysaccharide α-2,3-sialyltransferase from Haemophilus influenzae. Mol. Microbiol. 39, 341-350.
42. Berry, D.S., Lynn, F., Lee, C.-H., Frasch, C.E. & Bash, M.C. (2002) Effect of O-acetylation of Neisseria meningitidis serogroup A capsular polysaccharide on development of functional immune responses. Infect. Immun. 70, 3707-3713.