Abrogation of nontypeable Haemophilus influenzae Protein D function reduces phosphorylcholine decoration, adherence to airway epithelial cells, and fitness in a chinchilla model of otitis media

Vaccine

Volumn 29, Issue 6, 2011, Pages 1211-1221

  Johnson, Ryan W ^a   McGillivary, Glen ^a   Denoël, Philippe ^b   Poolman, Jan ^b   Bakaletz, Lauren O ^a  

^a THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b GLAXOSMITHKLINE BIOLOGICALS   (Belgium)

Author keywords

GlpQ; PHiD CV; Synflorix

Indexed keywords

BACTERIAL PROTEIN; GLYCEROPHOSPHODIESTER PHOSPHODIESTERASE; OUTER MEMBRANE PROTEIN; PHOSPHORYLCHOLINE; PNEUMOCOCCUS VACCINE; PROTEIN D; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ADHESION; CHINCHILLA; HAEMOPHILUS INFLUENZAE; HUMAN; HUMAN CELL; IN VITRO STUDY; NONHUMAN; OTITIS MEDIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RESPIRATORY EPITHELIUM;

ANIMALS; BACTERIAL ADHESION; BACTERIAL PROTEINS; CARRIER PROTEINS; CHINCHILLA; EPITHELIAL CELLS; HAEMOPHILUS INFLUENZAE; HUMANS; IMMUNOGLOBULIN D; LIPOPROTEINS; OTITIS MEDIA; PHOSPHORYLCHOLINE; VIRULENCE FACTORS;

EID: 78751574049     PISSN: 0264410X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vaccine.2010.12.003     Document Type: Article

References (57)

1. Vergison A. Microbiology of otitis media: a moving target. Vaccine 2008, 26(December (Suppl. 7)):G5-G10.
2. Rovers M.M. The burden of otitis media. Vaccine 2008, 26(December (Suppl. 7)):G2-G4.
3. Hardy G.G., Tudor S.M., St Geme J.W. The pathogenesis of disease due to nontypeable Haemophilus influenzae. Methods Mol Med 2003, 71:1-28.
4. West-Barnette S., Rockel A., Swords W.E. Biofilm growth increases phosphorylcholine content and decreases potency of nontypeable Haemophilus influenzae endotoxins. Infect Immun 2006, 74(March (3)):1828-1836.
5. Swords W.E., Moore M.L., Godzicki L., Bukofzer G., Mitten M.J., VonCannon J. Sialylation of lipooligosaccharides promotes biofilm formation by nontypeable Haemophilus influenzae. Infect Immun 2004, 72(January (1)):106-113.
6. Pereira M.B., Pereira M.R., Cantarelli V., Costa S.S. Prevalence of bacteria in children with otitis media with effusion. J Pediatr (Rio J) 2004, 80(January-February (1)):41-48.
7. Broides A., Leibovitz E., Dagan R., Press J., Raiz S., Kafka M., et al. Cytology of middle ear fluid during acute otitis media. Pediatr Infect Dis J 2002, 21(January (1)):57-61.
8. Dagan R., Hoberman A., Johnson C., Leibovitz E.L., Arguedas A., Rose F.V., et al. Bacteriologic and clinical efficacy of high dose amoxicillin/clavulanate in children with acute otitis media. Pediatr Infect Dis J 2001, 20(September (9)):829-837.
9. Rosenblut A., Santolaya M.E., Gonzalez P., Corbalan V., Avendano L.F., Martinez M.A., et al. Bacterial and viral etiology of acute otitis media in Chilean children. Pediatr Infect Dis J 2001, 20(May (5)):501-507.
10. Hsu K., Pelton S., Karumuri S., Heisey-Grove D., Klein J. Massachusetts Department of Public Health E. Population-based surveillance for childhood invasive pneumococcal disease in the era of conjugate vaccine. Pediatr Infect Dis J 2005, 24(January (1)):17-23.
11. Prymula R., Peeters P., Chrobok V., Kriz P., Novakova E., Kaliskova E., et al. Pneumococcal capsular polysaccharides conjugated to protein D for prevention of acute otitis media caused by both Streptococcus pneumoniae and non-typable Haemophilus influenzae: a randomised double-blind efficacy study. Lancet 2006, 367(March (9512)):740-748.
12. Munson R.S., Sasaki K. Protein D, a putative immunoglobulin D-binding protein produced by Haemophilus influenzae, is glycerophosphodiester phosphodiesterase. J Bacteriol 1993, 175(July (14)):4569-4571.
13. Toropainen M., Raitolehto A., Henckaerts I., Wauters D., Poolman J., Lestrate P., et al. Pneumococcal Haemophilus influenzae protein D conjugate vaccine induces antibodies that inhibit glycerophosphodiester phosphodiesterase activity of protein D. Infect Immun 2008, 76(October (10)):4546-4553.
14. Ahren I.L., Janson H., Forsgren A., Riesbeck K. Protein D expression promotes the adherence and internalization of non-typeable Haemophilus influenzae into human monocytic cells. Microb Pathog 2001, 31(September (3)):151-158.
15. Fan X., Goldfine H., Lysenko E., Weiser J.N. The transfer of choline from the host to the bacterial cell surface requires glpQ in Haemophilus influenzae. Mol Microbiol 2001, 41(September (5)):1029-1036.
16. Janson H., Carl n B., Cervin A., Forsgren A., Magnusdottir A.B., Lindberg S., et al. Effects on the ciliated epithelium of protein D-producing and -nonproducing nontypeable Haemophilus influenzae in nasopharyngeal tissue cultures. J Infect Dis 1999, 180(September (3)):737-746.
17. Janson H., Melhus A., Hermansson A., Forsgren A. Protein D, the glycerophosphodiester phosphodiesterase from Haemophilus influenzae with affinity for human immunoglobulin D, influences virulence in a rat otitis model. Infect Immun 1994, 62(November (11)):4848-4854.
18. Bakaletz L.O., Tallan B.M., Hoepf T., DeMaria T.F., Birck H.G., Lim D.J. Frequency of fimbriation of nontypable Haemophilus influenzae and its ability to adhere to chinchilla and human respiratory epithelium. Infect Immun 1988, 56(February (2)):331-335.
19. Harrison A., Dyer D.W., Gillaspy A., Ray W.C., Mungur R., Carson M.B., et al. Genomic sequence of an otitis media isolate of nontypeable Haemophilus influenzae: comparative study with H. influenzae serotype d, strain KW20. J Bacteriol 2005, 187(July (13)):4627-4636.
20. Jurcisek J.A., Bookwalter J.E., Baker B.D., Fernandez S., Novotny L.A., Munson R.S., et al. The PilA protein of non-typeable Haemophilus influenzae plays a role in biofilm formation, adherence to epithelial cells and colonization of the mammalian upper respiratory tract. Mol Microbiol 2007, 65(September (5)):1288-1299.
21. Novotny L.A., Mason K.M., Bakaletz L.O. Development of a chinchilla model to allow direct, continuous, biophotonic imaging of bioluminescent nontypeable Haemophilus influenzae during experimental otitis media. Infect Immun 2005, 73(January (1)):609-611.
22. Tracy E., Ye F., Baker B.D., Munson R.S. Construction of non-polar mutants in Haemophilus influenzae using FLP recombinase technology. BMC Mol Biol 2008, 9:101.
23. Spencer H.T., Herriott R.M. Development of competence of Haemophilus influenzae. J Bacteriol 1965, 90(October (4)):911-920.
24. Mason K.M., Munson R.S., Bakaletz L.O. A mutation in the sap operon attenuates survival of nontypeable Haemophilus influenzae in a chinchilla model of otitis media. Infect Immun 2005, 73(January (1)):599-608.
25. Mason K.M., Munson R.S., Bakaletz L.O. Nontypeable Haemophilus influenzae gene expression induced in vivo in a chinchilla model of otitis media. Infect Immun 2003, 71(June (6)):3454-3462.
26. Mitchell M.A., Skowronek K., Kauc L., Goodgal S.H. Electroporation of Haemophilus influenzae is effective for transformation of plasmid but not chromosomal DNA. Nucleic Acids Res 1991, 19(July (13)):3625-3628.
27. Coleman H.N., Daines D.A., Jarisch J., Smith A.L. Chemically defined media for growth of Haemophilus influenzae strains. J Clin Microbiol 2003, 41(September (9)):4408-4410.
28. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227(August (5259)):680-685.
29. Bakaletz L.O., Leake E.R., Billy J.M., Kaumaya P.T. Relative immunogenicity and efficacy of two synthetic chimeric peptides of fimbrin as vaccinogens against nasopharyngeal colonization by nontypeable Haemophilus influenzae in the chinchilla. Vaccine 1997, 15(June (9)):955-961.
30. Seilly D.J. A chemical test to determine the end point of EDTA decalcification. Med Lab Sci 1982, 39(January (1)):71-73.
31. Akkoyunlu M., Ruan M., Forsgren A. Distribution of protein D, an immunoglobulin D-binding protein, in Haemophilus strains. Infect Immun 1991, 59(April (4)):1231-1238.
32. Fan X., Pericone C.D., Lysenko E., Goldfine H., Weiser J.N. Multiple mechanisms for choline transport and utilization in Haemophilus influenzae. Mol Microbiol 2003, 50(October (2)):537-548.
33. Hong W., Mason K., Jurcisek J., Novotny L., Bakaletz L.O., Swords W.E. 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 2007, 75(February (2)):958-965.
34. Hong W., Pang B., West-Barnette S., Swords W.E. Phosphorylcholine expression by nontypeable Haemophilus influenzae correlates with maturation of biofilm communities in vitro and in vivo. J Bacteriol 2007, 189(November (22)):8300-8307.
35. Swords W.E., Buscher B.A., Ver Steeg Ii K., Preston A., Nichols W.A., Weiser J.N., et al. Non-typeable Haemophilus influenzae adhere to and invade human bronchial epithelial cells via an interaction of lipooligosaccharide with the PAF receptor. Mol Microbiol 2000, 37(July (1)):13-27.
36. Novotny L.A., Jurcisek J.A., Godfroid F., Poolman J.T., Denoel P.A., Bakaletz L.O. Passive immunization with human anti-protein D antibodies induced by polysaccharide protein D conjugates protects chinchillas against otitis media after intranasal challenge with Haemophilus influenzae. Vaccine 2006, 24(May (22)):4804-4811.
37. Bakaletz L.O., Kennedy B.J., Novotny L.A., Duquesne G., Cohen J., Lobet Y. Protection against development of otitis media induced by nontypeable Haemophilus influenzae by both active and passive immunization in a chinchilla model of virus-bacterium superinfection. Infect Immun 1999, 67(June (6)):2746-2762.
38. Kennedy B.J., Novotny L.A., Jurcisek J.A., Lobet Y., Bakaletz L.O. Passive transfer of antiserum specific for immunogens derived from a nontypeable Haemophilus influenzae adhesin and lipoprotein D prevents otitis media after heterologous challenge. Infect Immun 2000, 68(May (5)):2756-2765.
39. Moriyama S., Hotomi M., Shimada J., Billal D.S., Fujihara K., Yamanaka N. Formation of biofilm by Haemophilus influenzae isolated from pediatric intractable otitis media. Auris Nasus Larynx 2009, 36(October (5)):525-531.
40. Starner T.D., Zhang N., Kim G., Apicella M.A., McCray P.B. Haemophilus influenzae forms biofilms on airway epithelia: implications in cystic fibrosis. Am J Respir Crit Care Med 2006, 174(July (2)):213-220.
41. Weiser J.N. Phase variation in colony opacity by Streptococcus pneumoniae. Microb Drug Resist 1998, 4(Summer (2)):129-135.
42. Pang B., Winn D., Johnson R., Hong W., West-Barnette S., Kock N., et al. Lipooligosaccharides containing phosphorylcholine delay pulmonary clearance of nontypeable Haemophilus influenzae. Infect Immun 2008, 76(May (5)):2037-2043.
43. Serino L., Virji M. Genetic and functional analysis of the phosphorylcholine moiety of commensal Neisseria lipopolysaccharide. Mol Microbiol 2002, 43(January (2)):437-448.
44. Weiser J.N., Shchepetov M., Chong S.T. Decoration of lipopolysaccharide with phosphorylcholine: a phase-variable characteristic of Haemophilus influenzae. Infect Immun 1997, 65(March (3)):943-950.
45. Zhang J.R., Idanpaan-Heikkila I., Fischer W., Tuomanen E.I. Pneumococcal licD2 gene is involved in phosphorylcholine metabolism. Mol Microbiol 1999, 31(March (5)):1477-1488.
46. Cundell D.R., Gerard C., Idanpaan-Heikkila I., Tuomanen E.I., Gerard N.P. PAf receptor anchors Streptococcus pneumoniae to activated human endothelial cells. Adv Exp Med Biol 1996, 416:89-94.
47. Lysenko E.S., Gould J., Bals R., Wilson J.M., Weiser J.N. Bacterial phosphorylcholine decreases susceptibility to the antimicrobial peptide LL-37/hCAP18 expressed in the upper respiratory tract. Infect Immun 2000, 68(March (3)):1664-1671.
48. Hanamure Y., Lim D.J. Anatomy of the chinchilla bulla and Eustachian tube: I. Gross and microscopic study. Am J Otolaryngol 1987, 8(May-June (3)):127-143.
49. Jurcisek J.A., Durbin J.E., Kusewitt D.F., Bakaletz L.O. Anatomy of the nasal cavity in the chinchilla. Cells Tissues Organs 2003, 174(3):136-152.
50. Lim D.J., Chun Y.M., Lee H.Y., Moon S.K., Chang K.H., Li J.D., et al. Cell biology of tubotympanum in relation to pathogenesis of otitis media-a review. Vaccine 2000, 19(December (Suppl. 1)):S17-S25.
51. Lysenko E., Richards J.C., Cox A.D., Stewart A., Martin A., Kapoor M., et al. The position of phosphorylcholine on the lipopolysaccharide of Haemophilus influenzae affects binding and sensitivity to C-reactive protein-mediated killing. Mol Microbiol 2000, 35(January (1)):234-245.
52. Sun J., Chen J., Cheng Z., Robbins J.B., Battey J.F., Gu X.X. Biological activities of antibodies elicited by lipooligosaccharide based-conjugate vaccines of nontypeable Haemophilus influenzae in an otitis media model. Vaccine 2000, 18(January (13)):1264-1272.
53. Song X.M., Forsgren A., Janson H. The gene encoding protein D (hpd) is highly conserved among Haemophilus influenzae type b and nontypeable strains. Infect Immun 1995, 63(February (2)):696-699.
54. Janson H., Ruan M., Forsgren A. Limited diversity of the protein D gene (hpd) among encapsulated and nonencapsulated Haemophilus influenzae strains. Infect Immun 1993, 61(November (11)):4546-4552.
55. Benninger M.S. Acute bacterial rhinosinusitis and otitis media: changes in pathogenicity following widespread use of pneumococcal conjugate vaccine. Otolaryngol Head Neck Surg 2008, 138(March (3)):274-278.
56. Erwin A.L., Smith A.L. Nontypeable Haemophilus influenzae: understanding virulence and commensal behavior. Trends Microbiol 2007, 15(August (8)):355-362.
57. Murphy T.F. The role of bacteria in airway inflammation in exacerbations of chronic obstructive pulmonary disease. Curr Opin Infect Dis 2006, 19(June (3)):225-230.