Nontypable haemophilus influenzae displays a prevalent surface structure molecular pattern in clinical isolates

PLoS ONE

Volumn 6, Issue 6, 2011, Pages

  Martí Lliteras, Pau ^a,b   López Gómez, Antonio ^a,b   Mauro, Silvia ^a   Hood, Derek W ^d   Viadas, Cristina ^a   Calatayud, Laura ^b,e,g,h   Morey, Pau ^a,b   Servin, Alain ⁱ   Liñares, Josefina ^b,e,g,h   Oliver, Antonio ^f   Bengoechea, José Antonio ^a,b,c   Garmendia, Junkal ^a,b,c  

^a Laboratory of Microbial Pathogenesis   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c CSIC   (Spain)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e HOSPITAL UNIVERSITARI DE BELLVITGE   (Spain)

^f HOSPITAL UNIVERSITARIO SON ESPASES   (Spain)

^g BELLVITGE BIOMEDICAL RESEARCH INSTITUTE IDIBELL   (Spain)

^h UNIVERSITY OF BARCELONA   (Spain)

ⁱ INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CARCINOEMBRYONIC ANTIGEN RELATED CELL ADHESION MOLECULE 1;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIUM ISOLATE; CONTROLLED STUDY; EPITHELIUM CELL; GENE EXPRESSION PROFILING; GENE SEQUENCE; GENETIC ANALYSIS; GENETIC HETEROGENEITY; GENETIC SCREENING; GENETIC VARIABILITY; GEOGRAPHIC DISTRIBUTION; HAEMOPHILUS INFLUENZAE; HUMAN; HUMAN CELL; IGTF GENE; LIC1D GENE; LIC2A GENE; LIC2C GENE; LIC3A GENE; MOLECULAR EPIDEMIOLOGY; NONHUMAN; OAPA GENE; OMPP5 GENE; OPEN READING FRAME; PHENOTYPE; SIAA GENE; CELL ADHESION; GENETICS; HAEMOPHILUS INFECTION; HELA CELL; ISOLATION AND PURIFICATION; MICROBIOLOGY; PHYSIOLOGY; POLYMERASE CHAIN REACTION;

BACTERIA (MICROORGANISMS); HAEMOPHILUS INFLUENZAE; NEGIBACTERIA;

CELL ADHESION; GENETIC HETEROGENEITY; HAEMOPHILUS INFECTIONS; HAEMOPHILUS INFLUENZAE; HELA CELLS; HUMANS; POLYMERASE CHAIN REACTION;

EID: 79959199052     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0021133     Document Type: Article

References (58)

1. Foxwell AR, Kyd JM, Cripps AW, (1998) Nontypeable Haemophilus influenzae: pathogenesis and prevention. Microbiol Mol Biol Rev 62: 294-308.
2. Hallström T, Riesbeck K, (2010) Haemophilus influenzae and the complement system. Trends Microbiol 18: 258-265.
3. Starner TD, Swords WE, Apicella MA, McCray PB Jr, (2002) Susceptibility of nontypeable Haemophilus influenzae to human β-defensins is influenced by lipooligosaccharide acylation. Infect Immun 70: 5287-5289.
4. Rao VK, Krasan GP, Hendrixson DR, Dawid S, St Geme JW 3rd, (1999) Molecular determinants of the pathogenesis of disease due to non-typable Haemophilus influenzae. FEMS Microbiol Rev 23: 99-129.
5. Erwin AL, Smith AL, (2007) Nontypeable Haemophilus influenzae: understanding virulence and commensal behavior. Trends Microbiol 15: 355-362.
6. Morey P, Cano V, Martí-Lliteras P, López-Gómez A, Regueiro V, et al. (2011) Evidence for a non-replicative intracellular stage of nontypable Haemophilus influenzae in epithelial cells. Microbiology 157: 234-250.
7. Fernaays MM, Lesse AJ, Sethi S, Cai X, Murphy TF, (2006) Differential genome contents of nontypeable Haemophilus influenzae strains from adults with chronic obstructive pulmonary disease. Infect Immun 74: 3366-3374.
8. Gilsdorf JR, Marrs CF, Foxman B, (2004) Haemophilus influenzae: genetic variability and natural selection to identify virulence factors. Infect Immun 72: 2457-2461.
9. Power PM, Sweetman WA, Gallacher NJ, Woodhall MR, Kumar GA, et al. (2009) Simple sequence repeats in Haemophilus influenzae. Infect Genet Evol 9: 216-228.
10. Harvey HA, Swords WE, Apicella MA, (2001) The mimicry of human glycolipids and glycosphingolipids by the lipooligosaccharides of pathogenic Neisseria and Haemophilus. J Autoimmun 16: 257-262.
11. Schweda EK, Richards JC, Hood DW, Moxon ER, (2007) Expression and structural diversity of the lipopolysaccharide of Haemophilus influenzae: implication in virulence. Int J Med Microbiol 297: 297-306.
12. Hood DW, Deadman ME, Cox AD, Makepeace K, Martin A, et al. (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.
13. Weiser JN, Shchepetov M, Chong ST, (1997) Decoration of lipopolysaccharide with phosphorylcholine: a phase-variable characteristic of Haemophilus influenzae. Infect Immun 65: 943-950.
14. Deadman ME, Lundström SL, Schweda EK, Moxon ER, Hood DW, (2006) Specific amino acids of the glycosyltransferase LpsA direct the addition of glucose or galactose to the terminal inner core heptose of Haemophilus influenzae lipopolysaccharide via alternative linkages. J Biol Chem 281: 29455-29467.
15. Fox KL, Cox AD, Gilbert M, Wakarchuk WW, Li J, et al. (2006) Identification of a bifunctional lipopolysaccharide sialyltransferase in Haemophilus influenzae: incorporation of disialic acid. J Biol Chem 281: 40024-40032.
16. Jones PA, Samuels NM, Phillips NJ, Munson RS Jr, Bozue JA, et al. (2002) Haemophilus influenzae type b strain A2 has multiple sialyltransferases involved in lipooligosaccharide sialylation. J Biol Chem 277: 14598-14611.
17. Weiser JN, Pan N, McGowan KL, Musher D, Martin A, et al. (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.
18. Hong W, Mason K, Jurcisek J, Novotny L, Bakaletz LO, et al. (2007) Phosphorylcholine decreases early inflammation and promotes the establishment of stable biofilm communities of nontypeable Haemophilus influenzae strain 86-028NP in a chinchilla model of otitis media. Infect Immun 75: 958-965.
19. Lysenko E, Richards JC, Cox AD, Stewart A, Martin A, et al. (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.
20. Swords WE, Buscher BA, Ver Steeg K Ii, Preston A, Nichols WA, et al. (2000) Non-typeable Haemophilus influenzae adhere to and invade human bronchial epithelial cells via an interaction of lipooligosaccharide with the PAF receptor. Mol Microbiol 37: 13-27.
21. Ho DK, Ram S, Nelson KL, Bonthuis PJ, Smith AL, (2007) lgtC expression modulates resistance to C4b deposition on an invasive nontypeable Haemophilus influenzae. J Immunol 178: 1002-1012.
22. Weiser JN, Pan N, (1998) Adaptation of Haemophilus influenzae to acquired and innate humoral immunity based on phase variation of lipopolysaccharide. Mol Microbiol 30: 767-775.
23. Figueira MA, Ram S, Goldstein R, Hood DW, Moxon ER, et al. (2007) Role of complement in defense of the middle ear revealed by restoring the virulence of nontypeable Haemophilus influenzae siaB mutants. Infect Immun 75: 325-333.
24. Hood DW, Makepeace K, Deadman ME, Rest RF, Thibault P, et al. (1999) Sialic acid in the lipopolysaccharide of Haemophilus influenzae: strain distribution, influence on serum resistance and structural characterization. Mol Microbiol 33: 679-692.
25. Jurcisek J, Greiner L, Watanabe H, Zaleski A, Apicella MA, et al. (2005) Role of sialic acid and complex carbohydrate biosynthesis in biofilm formation by nontypeable Haemophilus influenzae in the chinchilla middle ear. Infect Immun 273: 3210-3218.
26. Pettigrew MM, Foxman B, Marrs CF, Gilsdorf JR, (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.
27. Harrison A, Dyer DW, Gillaspy A, Ray WC, Mungur R, et al. (2005) Genomic sequence of an otitis media isolate of nontypeable Haemophilus influenzae: comparative study with H. influenzae serotype d, strain KW20. J Bacteriol 187: 4627-4636.
28. Moxon R, Bayliss C, Hood D, (2006) Bacterial contingency loci: the role of simple sequence DNA repeats in bacterial adaptation. Annu Rev Genet 40: 307-333.
29. Prasadarao NV, Lysenko E, Wass CA, Kim KS, Weiser JN, (1999) Opacity-associated protein A contributes to the binding of Haemophilus influenzae to Chang epithelial cells. Infect Immun 67: 4153-4160.
30. St Geme JW, (2002) Molecular and cellular determinants of non-typeable Haemophilus influenzae adherence and invasion. Cell Microbiol 4: 191-200.
31. Weiser JN, Chong ST, Greenberg D, Fong W, (1995) Identification and characterization of a cell envelope protein of Haemophilus influenzae contributing to phase variation in colony opacity and nasopharyngeal colonization. Mol Microbiol 17: 555-564.
32. Duim B, Bowler LD, Eijk PP, Jansen HM, Dankert J, et al. (1997) Molecular variation in the major outer membrane protein P5 gene of nonencapsulated Haemophilus influenzae during chronic infections. Infect Immun 65: 1351-1356.
33. Webb DC, Cripps AW, (1998) Secondary structure and molecular analysis of interstrain variability in the P5 outer-membrane protein of non-typable Haemophilus influenzae isolated from diverse anatomical sites. J Med Microbiol 47: 1059-1067.
34. Hill DJ, Toleman MA, Evans DJ, Villullas S, Van Alphen L, et al. (2001) The variable P5 proteins of typeable and non-typeable Haemophilus influenzae target human CEACAM1. Mol Microbiol 39: 850-862.
35. Slevogt H, Zabel S, Opitz B, Hocke A, Eitel J, et al. (2008) CEACAM1 inhibits Toll-like receptor 2-triggered antibacterial responses of human pulmonary epithelial cells. Nat Immunol 9: 1270-1278.
36. Ecevit IZ, McCrea KW, Pettigrew MM, Sen A, Marrs CF, et al. (2004) Prevalence of the hifBC, hmw1A, hmw2A, hmwC, and hia genes in Haemophilus influenzae isolates. J Clin Microbiol 42: 3065-3072.
37. Xie J, Juliao PC, Gilsdorf JR, Ghosh D, Patel M, et al. (2006) Identification of new genetic regions more prevalent in nontypeable Haemophilus influenzae otitis media strains than in throat strains. J Clin Microbiol 44: 4316-4325.
38. Erwin AL, Nelson KL, Mhlanga-Mutangadura T, Bonthuis PJ, Geelhood JL, et al. (2005) Characterization of genetic and phenotypic diversity of invasive nontypeable Haemophilus influenzae. Infect Immun 73: 5853-5863.
39. Lima JB, Ribeiro GS, Cordeiro SM, Gouveia EL, Salgado K, et al. (2010) Poor clinical outcome for meningitis caused by Haemophilus influenzae serotype A strains containing the IS1016-bexA deletion. J Infect Dis 202: 1577-1584.
40. Rodriguez CA, Avadhanula V, Buscher A, Smith AL, St Geme JW, et al. (2003) Prevalence and distribution of adhesins in invasive non-type b encapsulated Haemophilus influenzae. Infect Immun 71: 1635-1642.
41. Satola SW, Napier B, Farley MM, (2008) Association of IS1016 with the hia adhesin gene and biotypes V and I in invasive nontypeable Haemophilus influenzae. Infect Immun 76: 5221-5227.
42. Fleischmann RD, Adams MD, White O, Clayton RA, Kirkness EF, et al. (1995) Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269: 496-512.
43. Martí-Lliteras P, Regueiro V, Morey P, Hood DW, Saus C, et al. (2009) Nontypeable Haemophilus influenzae clearance by alveolar macrophages is impaired by exposure to cigarette smoke. Infect Immun 77: 4232-4242.
44. Dixon K, Bayliss CD, Makepeace K, Moxon ER, Hood DW, (2007) Identification of the functional initiation codons of a phase-variable gene of Haemophilus influenzae, lic2A, with the potential for differential expression. J Bacteriol 189: 511-521.
45. Fox KL, Li J, Schweda EK, Vitiazeva V, Makepeace K, et al. (2008) Duplicate copies of lic1 direct the addition of multiple phosphocholine residues in the lipopolysaccharide of Haemophilus influenzae. Infect Immun 76: 588-600.
46. Mullins MA, Register KB, Bayles DO, Loving CL, Nicholson TL, et al. (2009) Characterization and comparative analysis of the genes encoding Haemophilus parasuis outer membrane proteins P2 and P5. J Bacteriol 191: 5988-6002.
47. Hallstrom T, Riesbeck K, (2010) Haemophilus influenzae and the complement system. Trends Microbiol 18: 258-265.
48. Avadhanula V, Rodriguez CA, Devincenzo JP, Wang Y, Webby RJ, et al. (2006) Respiratory viruses augment the adhesion of bacterial pathogens to respiratory epithelium in a viral species- and cell type-dependent manner. J Virol 80: 1629-36.
49. Singer BB, Scheffrahn I, Kammerer R, Suttorp N, Ergun S, et al. (2010) Deregulation of the CEACAM expression pattern causes undifferentiated cell growth in human lung adenocarcinoma cells. PLoS One 5: e8747.
50. Gray-Owen SD, Dehio C, Haude A, Grunert F, Meyer TF, (1997) CD66 carcinoembryonic antigens mediate interactions between Opa-expressing Neisseria gonorrhoeae and human polymorphonuclear phagocytes. EMBO J 16: 3435-3445.
51. Lamers RP, Stinnett JW, Muthukrishnan G, Parkinson CL, Cole AM, (2011) Evolutionary analyses of Staphylococcus aureus identify genetic relationships between nasal carriage and clinical isolates. PLoS One 6: e16426.
52. Hong W, Pang B, West-Barnette S, Swords WE, (2007) Phosphorylcholine expression by nontypeable Haemophilus influenzae correlates with maturation of biofilm communities in vitro and in vivo. J Bacteriol 189: 8300-8307.
53. Hallstrom T, Resman F, Ristovski M, Riesbeck K, (2010) Binding of complement regulators to invasive nontypeable Haemophilus influenzae isolates is not increased compared to nasopharyngeal isolates, but serum resistance is linked to disease severity. J Clin Microbiol 48: 921-927.
54. Novotny LA, Jurcisek JA, Pichichero ME, Bakaletz LO, (2000) Epitope mapping of the outer membrane protein P5-homologous fimbrin adhesin of nontypeable Haemophilus influenzae. Infect Immun 68: 2119-2128.
55. Pizarro-Cerdá J, Cossart P, (2006) Bacterial adhesion and entry into host cells. Cell 124: 715-727.
56. Tenover FC, Arbeit RD, Goering RV, Mickelsen PA, Murray BE, et al. (1995) Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J Clin Microbiol 33: 2233-2239.
57. Roche RJ, High NJ, Moxon ER, (1994) Phase variation of Haemophilus influenzae lipopolysaccharide: characterization of lipopolysaccharide from individual colonies. FEMS Microbiol Lett 120: 279-283.
58. High NJ, Deadman ME, Hood DW, Moxon ER, (1996) The identification a novel gene required for lipopolysaccharide biosynthesis by Haemophilus influenzae RM7004, using transposon Tn916 mutagenesis. FEMS Microbiol Lett 145: 325-331.