Heterogeneity in tandem octanucleotides within Haemophilus influenzae lipopolysaccharide biosynthetic gene losA affects serum resistance

Infection and Immunity

Volumn 74, Issue 6, 2006, Pages 3408-3414

  Erwin, Alice L ^a   Bonthuis, Paul J ^a   Geelhood, Jennifer L ^a   Nelson, Kevin L ^a   McCrea, Kirk W ^b   Gilsdorf, Janet R ^b   Smith, Arnold L ^a  

^a SEATTLE BIOMEDICAL RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; NUCLEOTIDE; TANDEM OCTANUCLEOTIDE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIAL STRAIN; BACTERIUM COLONY; CAT GENE; ELECTROPHORETIC MOBILITY; GENE EXPRESSION; GENE INACTIVATION; GENE INSERTION; GENE SEQUENCE; HAEMOPHILUS INFLUENZAE; LOSA GENE; NONHUMAN; NUCLEOTIDE REPEAT; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RNA TRANSLATION; SEQUENCE ANALYSIS; SERUM; SERUM BACTERICIDAL ACTIVITY; SERUM RESISTANCE;

BLOOD BACTERICIDAL ACTIVITY; GENOME, BACTERIAL; GLYCOSYLTRANSFERASES; HAEMOPHILUS INFLUENZAE; HUMANS; LIPOPOLYSACCHARIDES; OLIGONUCLEOTIDES; REPETITIVE SEQUENCES, NUCLEIC ACID;

EID: 33646927215     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.01540-05     Document Type: Article

References (33)

1. Barenkamp, S. J., and E. Leininger. 1992. Cloning, expression, and DNA sequence analysis of genes encoding nontypeable Haemophilus influenzae high-molecular-weight surface-exposed proteins related to filamentous hemagglutinin of Bordetella pertussis. Infect. Immun. 60:1302-1313.
2. Bayliss, C. D., D. Field, and E. R. Moxon. 2001. The simple sequence contingency loci of Haemophilus influenzae and Neissena meningitidis. J. Clin. Investig. 107:657-662.
3. Benson, G. 1999. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res. 27:573-580.
4. Daines, D. A., and A. L. Smith. 2001. Design and construction of a Haemophilus influenzae conjugal expression system. Gene 281:95-102.
5. Dawid, S., S. J. Barenkamp, and J. W. St. Geme III. 1999. Variation in expression of the Haemophilus influenzae HMW adhesins: a prokaryotic system reminiscent of eukaryotes. Proc. Natl. Acad. Sci. USA 96:1077-1082.
6. de Bolle, X., C. D. Bayliss, D. Field, T. van de Yen, N. J. Saunders, D. W. Hood, and E. R. Moxon. 2000. The length of a tetranucleotide repeat tract in Haemophilus influenzae determines the phase variation rate of a gene with homology to type III DNA methyltransferases. Mol. Microbiol. 35:211-222.
7. Erwin, A. L., K. L. Nelson, T. Mhlanga-Mutangadura, P. J. Bonthuis, J. L. Geelhood, G. Morlin, W. C. Unrath, J. Campos, D. W. Crook, M. M. Farley, F. W. Henderson, R. F. Jacobs, K. Muhlemann, S. W. Satola, L. van Alphen, M. Golomb, and A. L. Smith. 2005. Characterization of genetic and phenotypic diversity of invasive nontypeable Haemophilus influenzae. Infect. Immun. 73:5853-5863.
8. Fleischmann, R. D., M. D. Adams, O. White, R. A. Clayton, E. F. Kirkness, A. R. Kerlavage, C. J. Bult, J. F. Tomb, B. A. Dougherty, J. M. Merrick, et al. 1995. Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269:496-512.
9. Gibson, B. W., A. A. Campagnari, W. Melaugh, N. J. Phillips, M. A. Apicella, S. Grass, J. Wang, K. L. Palmer, and R. S. Munson, Jr. 1997. Characterization of a transposon Tn916-generated mutant of Haemophilus ducreyi 35000 defective in lipooligosaccharide biosynthesis. J. Bacteriol. 179:5062-5071.
10. Griffin, R., A. D. Cox, K. Makepeace, J. C. Richards, E. R. Moxon, and D. W. Hood. 2005. Elucidation of the monoclonal antibody 5G8-reactive, virulence-associated lipopolysaccharide epitope of Haemophilus influenzae and its role in bacterial resistance to complement-mediated killing. Infect. Immun. 73: 2213-2221.
11. Herriott, R. M., E. M. Meyer, and M. Vogt. 1970. Defined nongrowth media for stage II development of competence in Haemophilus influenzae. J. Bacteriol. 101:517-524.
12. Hood, D. W., M. E. Deadman, T. Allen, H. Masoud, A. Martin, J. R. Brisson, R. Fleischmann, J. C. Venter, J. C. Richards, and E. R. Moxon. 1996. Use of the complete genome sequence information of Haemophilus influenzae strain Rd to investigate lipopolysaccharide biosynthesis. Mol. Microbiol. 22:951-965.
13. Hood, D. W., M. E. Deadman, A. D. Cox, K. Makepeace, A. Martin, J. C. Richards, and E. R. Moxon. 2004. Three genes, lgtF, lic2C and lpsA, have a primary role in determining the pattern of oligosaccharide extension from the inner core of Haemophilus influenzae LPS. Microbiology 150:2089-2097.
14. Hood, D. W., M. E. Deadman, M. P. Jennings, M. Bisercic, R. D. Fleischmann, J. C. Venter, and E. R. Moxon. 1996. DNA repeats identify novel virulence genes in Haemophilus influenzae. Proc. Natl. Acad. Sci. USA 93:11121-11125.
15. Jones, P. A., N. M. Samuels, N. J. Phillips, R. S. Munson, Jr., J. A. Bozue, J. A. Arseneau, W. A. Nichols, A. Zaleski, B. W. Gibson, and M. A. Apicella. 2002. Haemophilus influenzae type b strain A2 has multiple sialyltransferases involved in lipooligosaccharide sialylation. J. Biol. Chem. 277:14598-14611.
16. Kimura, A., C. C. Patrick, E. E. Miller, L. D. Cope, G. H. McCracken, Jr., and E. J. Hansen. 1987. Haemophilus influenzae type b lipooligosaccharide: stability of expression and association with virulence. Infect. Immun. 55: 1979-1986.
17. Lesse, A. J., A. A. Campagnari, W. E. Bittner, and M. A. Apicella. 1990. Increased resolution of lipopolysaccharides and lipooligosaccharides utilizing tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis. J. Immunol. Methods 126:109-117.
18. Månsson, M., D. W. Hood, E. R. Moxon, and E. K. Schweda. 2003. Structural diversity in lipopolysaccharide expression in nontypeable Haemophilus influenzae. Identification of L-glycerol-D-manno-heptose in the outer-core region in three clinical isolates. Eur. J. Biochem. 270:610-624.
19. Martin, K., G. Morlin, A. Smith, A. Nordyke, A. Eisenstark, and M. Golomb. 1998. The tryptophanase gene cluster of Haemophilus influenzae type b: evidence for horizontal gene transfer. J. Bacteriol. 180:107-118.
20. Martin, P., T. van de Ven, N. Mouchel, A. C. Jeffries, D. W. Hood, and E. R. Moxon. 2003. Experimentally revised repertoire of putative contingency loci in Neisseria meningitidis strain MC58: evidence for a novel mechanism of phase variation. Mol. Microbiol. 50:245-257.
21. Meats, E., E. J. Feil, S. Stringer, A. J. Cody, R. Goldstein, J. S. Kroll, T. Popovic, and B. G. Spratt. 2003. Characterization of encapsulated and noncapsulated Haemophilus influenzae and determination of phylogenetic relationships by multilocus sequence typing. J. Clin. Microbiol. 41:1623-1636.
22. Nizet, V., K. F. Colina, J. R. Almquist, C. E. Rubens, and A. L. Smith. 1996. A virulent nonencapsulated Haemophilus influenzae. J. Infect. Dis. 173:180-186.
23. O'Neill, J. M., J. W. St. Geme III, D. Cutter, E. E. Adderson, J. Anyanwu, R. F. Jacobs, and G. E. Schutze. 2003. Invasive disease due to nontypeable Haemophilus influenzae among children in Arkansas. J. Clin. Microbiol. 41:3064-3069.
24. Pettigrew, M. M., B. Foxman, C. F. Marrs, and J. R. Gilsdorf. 2002. Identification of the lipooligosaccharide biosynthesis gene lic2B as a putative virulence factor in strains of nontypeable Haemophilus influenzae that cause otitis media. Infect. Immun. 70:3551-3556.
25. Richards, J. C., A. D. Cox, E. K. Schweda, A. Martin, D. W. Hood, and E. R. Moxon. 2001. Structure and functional genomics of lipopolysaccharide expression in Haemophilus influenzae. Adv. Exp. Med. Biol. 491:515-524.
26. Severi, E., G. Randle, P. Kivlin, K. Whitfield, R. Young, R. Moxon, D. Kelly, D. Hood, and G. H. Thomas. 2005. Sialic acid transport in Haemophilus influenzae is essential for lipopolysaccharide sialylation and serum resistance and is dependent on a novel tripartite ATP-independent periplasmic transporter. Mol. Microbiol. 58:1173-1185.
27. Srikhanta, Y. N., T. L. Maguire, K. J. Stacey, S. M. Grimmond, and M. P. Jennings. 2005. The phasevarion: a genetic system controlling coordinated, random switching of expression of multiple genes. Proc. Natl. Acad. Sci. USA 102:5547-5551.
28. Tsai, C. M., and C. E. Frasch. 1982. A sensitive silver stain for detecting lipopolysaccharides in polyacrylamide gels. Anal. Biochem. 119:115-119.
29. Tullius, M. V., N. J. Phillips, N. K. Scheffler, N. M. Samuels, J. R. Munson, Jr., E. J. Hansen, M. Stevens-Riley, A. A. Campagnari, and B. W. Gibson. 2002. The lbg4B gene cluster of Haemophilus ducreyi encodes a beta-1,4-galactosyltransferase and an alpha-1,6-DD-heptosyltransferase involved in lipooligosaccharide biosynthesis. Infect. Immun. 70:2853-2861.
30. van Belkum, A., S. Scherer, W. van Leeuwen, D. Willemse, L. van Alphen, and H. Verbrugh. 1997. Variable number of tandem repeats in clinical strains of Haemophilus influenzae. Infect. Immun. 65:5017-5027.
31. van Ham, S. M., L. van Alphen, F. R. Mooi, and J. P. van Putten. 1993. Phase variation of H. influenzae fimbriae: transcriptional control of two divergent genes through a variable combined promoter region. Cell 73:1187-1196.
32. Weiser, J. N. 2000. The generation of diversity by Haemophilus influenzae. Trends Microbiol. 8:433-435.
33. Weiser, J. N., and N. Pan. 1998. Adaptation of Haemophilus influenzae to acquired and innate humoral immunity based on phase variation of lipopolysaccharide. Mol. Microbiol. 30:767-775.