PHiD-CV induces anti-Protein D antibodies but does not augment pulmonary clearance of nontypeable Haemophilus influenzae in mice

Vaccine

Volumn 33, Issue 38, 2015, Pages 4954-4961

  Siggins, Matthew K ^a   Gill, Simren K ^a   Langford, Paul R ^a   Li, Yanwen ^a   Ladhani, Shamez N ^b,c   Tregoning, John S ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b PUBLIC HEALTH ENGLAND   (United Kingdom)

^c ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Antibody; Co infection; Influenza; Innate immunity; Nontypeable Haemophilus influenzae; Pneumococcal conjugate vaccine; Pneumonia

Indexed keywords

CXCL1 CHEMOKINE; INTERLEUKIN 6; PNEUMOCOCCUS VACCINE; PROTEIN ANTIBODY; PROTEIN D ANTIBODY; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; BACTERIUM ANTIBODY; CARRIER PROTEIN; GLPQ PROTEIN, HAEMOPHILUS INFLUENZAE; IMMUNOGLOBULIN D; LIPOPROTEIN; PHID-CV VACCINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ARTICLE; BACTERIAL CLEARANCE; BACTERIAL LOAD; BACTERIAL SUPERINFECTION; CELL INFILTRATION; CONTROLLED STUDY; FEMALE; HAEMOPHILUS INFECTION; INFLUENZA A (H1N1); INFLUENZA A VIRUS (H1N1); LUNG CLEARANCE; LUNG INFECTION; MOUSE; NEUTROPHILIA; NONHUMAN; NONTYPEABLE HAEMOPHILUS INFLUENZAE; PRIORITY JOURNAL; WEIGHT REDUCTION; ANIMAL; BAGG ALBINO MOUSE; BLOOD; BODY WEIGHT; COMPLICATION; DISEASE MODEL; HAEMOPHILUS INFECTIONS; HAEMOPHILUS INFLUENZAE; IMMUNOLOGY; MICROBIOLOGY; NEUTROPHIL; ORTHOMYXOVIRUS INFECTION; PATHOLOGY; PNEUMONIA, BACTERIAL; RESPIRATORY SYSTEM; SUPERINFECTION;

ANIMALS; ANTIBODIES, BACTERIAL; BACTERIAL PROTEINS; BODY WEIGHT; CARRIER PROTEINS; DISEASE MODELS, ANIMAL; FEMALE; HAEMOPHILUS INFECTIONS; HAEMOPHILUS INFLUENZAE; IMMUNOGLOBULIN D; LIPOPROTEINS; MICE, INBRED BALB C; NEUTROPHILS; ORTHOMYXOVIRIDAE INFECTIONS; PNEUMOCOCCAL VACCINES; PNEUMONIA, BACTERIAL; RESPIRATORY SYSTEM; SUPERINFECTION;

EID: 84940718602     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2015.07.034     Document Type: Article

References (50)

1. Mukundan D., Ecevit Z., Patel M., Marrs C.F., Gilsdorf J.R. Pharyngeal colonization dynamics of Haemophilus influenzae and Haemophilus haemolyticus in healthy adult carriers. J Clin Microbiol 2007, 45:3207-3217.
2. Pichichero M.E., Casey J.R., Hoberman A., Schwartz R. Pathogens causing recurrent and difficult-to-treat acute otitis media, 2003-2006. Clin Pediatr (Phila) 2008, 47:901-906.
3. Gkentzi D., Slack M.P., Ladhani S.N. The burden of nonencapsulated Haemophilus influenzae in children and potential for prevention. Curr Opin Infect Dis 2012, 25:266-272.
4. Collins S., Ramsay M., Slack M.P., Campbell H., Flynn S., Litt D., et al. Risk of invasive Haemophilus influenzae infection during pregnancy and association with adverse fetal outcomes. JAMA 2014, 311:1125-1132.
5. Van Eldere J., Slack M.P.E., Ladhani S., Cripps A.W. Non-typeable Haemophilus influenzae, an under-recognised pathogen. Lancet Infect Dis 2014, 14:1281-1292.
6. Chiang W.C., Teoh O.H., Chong C.Y., Goh A., Tang J.P., Chay O.M. Epidemiology, clinical characteristics and antimicrobial resistance patterns of community-acquired pneumonia in 1702 hospitalized children in Singapore. Respirology 2007, 12:254-261.
7. Ikeogu M.O. Acute pneumonia in Zimbabwe: bacterial isolates by lung aspiration. Arch Dis Child 1988, 63:1266-1267.
8. Saito A., Kohno S., Matsushima T., Watanabe A., Oizumi K., Yamaguchi K., et al. Prospective multicenter study of the causative organisms of community-acquired pneumonia in adults in Japan. J Infect Chemother 2006, 12:63-69.
9. Johansson N., Kalin M., Tiveljung-Lindell A., Giske C.G., Hedlund J. Etiology of community-acquired pneumonia: increased microbiological yield with new diagnostic methods. Clin Infect Dis 2010, 50:202-209.
10. Smith C.B., Golden C., Klauber M.R., Kanner R., Renzetti A. Interactions between viruses and bacteria in patients with chronic bronchitis. J Infect Dis 1976, 134:552-561.
11. McCullers J.A. The co-pathogenesis of influenza viruses with bacteria in the lung. Nat Rev Micro 2014, 12:252-262.
12. Bandi V., Apicella M.A., Mason E., Murphy T.F., Siddiqi A., Atmar R.L., et al. Nontypeable Haemophilus influenzae in the lower respiratory tract of patients with chronic bronchitis. Am J Respir Crit Care Med 2001, 164:2114-2119.
13. De Schutter I., De Wachter E., Crokaert F., Verhaegen J., Soetens O., Pierard D., et al. Microbiology of bronchoalveolar lavage fluid in children with acute nonresponding or recurrent community-acquired pneumonia: identification of nontypeable Haemophilus influenzae as a major pathogen. Clin Infect Dis 2011, 52:1437-1444.
14. Moghaddam S.J., Ochoa C.E., Sethi S., Dickey B.F. Nontypeable Haemophilus influenzae in chronic obstructive pulmonary disease and lung cancer. Int J Chronic Obstr Pulm Dis 2011, 6:113-123.
15. Tandon M.K., Phillips M., Waterer G., Dunkley M., Comans P., Clancy R. Oral immunotherapy with inactivated nontypeable Haemophilus influenzae reduces severity of acute exacerbations in severe COPD. Chest 2010, 137:805-811.
16. Murphy T.F. Vaccine development for non-typeable Haemophilus influenzae and Moraxella catarrhalis: progress and challenges. Expert Rev Vaccines 2005, 4:843-853.
17. Puig C., Calatayud L., Marti S., Tubau F., Garcia-Vidal C., Carratala J., et al. Molecular epidemiology of nontypeable Haemophilus influenzae causing community-acquired pneumonia in adults. PLOS ONE 2013, 8:e82515.
18. Ladhani S.N., Andrews N.J., Waight P., Borrow R., Slack M.P., Miller E. Invasive pneumococcal disease, comorbidities, and polysaccharide vaccine use in children aged 5-15 years in England and Wales. Clin infect Dis 2014, 58:517-525.
19. McVernon J., Ramsay M.E., McLean A.R. Understanding the impact of Hib conjugate vaccine on transmission, immunity and disease in the United Kingdom. Epidemiol Infect 2008, 136:800-812.
20. Forsgren A., Riesbeck K., Janson H. Protein D of Haemophilus influenzae: a protective nontypeable H. influenzae antigen and a carrier for pneumococcal conjugate vaccines. Clin Infect Dis 2008, 46:726-731.
21. 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, 67:2746-2762.
22. van den Bergh M.R., Spijkerman J., Francois N., Swinnen K., Borys D., Schuerman L., et al. Immunogenicity, safety, and reactogenicity of the 10-valent pneumococcal nontypeable Haemophilus influenzae Protein D conjugate vaccine and DTPa-IPV-Hib when coadministered as a 3-dose primary vaccination schedule in The Netherlands: a randomized controlled trial. Pediatr Infect Dis J 2011, 30:e170-e178.
23. Prymula R., Pazdiora P., Traskine M., Ruggeberg J.U., Borys D. Safety and immunogenicity of an investigational vaccine containing two common pneumococcal proteins in toddlers: a phase II randomized clinical trial. Vaccine 2014.
24. 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, 367:740-748.
25. Hood D.W., Makepeace K., Deadman M.E., Rest R.F., Thibault P., Martin A., et al. Sialic acid in the lipopolysaccharide of Haemophilus influenzae: strain distribution, influence on serum resistance and structural characterization. Mol Microbiol 1999, 33:679-692.
26. Bouchet V., Hood D.W., Li J., Brisson J.R., Randle G.A., Martin A., et al. Host-derived sialic acid is incorporated into Haemophilus influenzae lipopolysaccharide and is a major virulence factor in experimental otitis media. Proc Natl Acad Sci U S A 2003, 100:8898-8903.
27. Baillie G.J., Galiano M., Agapow P.M., Myers R., Chiam R., Gall A., et al. Evolutionary dynamics of local pandemic H1N1/2009 influenza virus lineages revealed by whole-genome analysis. J Virol 2012, 86:11-18.
28. Elleman C.J., Barclay W.S. The M1 matrix protein controls the filamentous phenotype of influenza A virus. Virology 2004, 321:144-153.
29. Hansen E.J., Toews G.B. Animal models for the study of noninvasive Haemophilus influenzae disease: pulmonary clearance systems. J Infect Dis 1992, 165(Suppl. 1):S185-S187.
30. Hansen E.J., Hart D.A., McGehee J.L., Toews G.B. Immune enhancement of pulmonary clearance of nontypable Haemophilus influenzae. Infect Immun 1988, 56:182-190.
31. Tregnaghi M.W., Saez-Llorens X., Lopez P., Abate H., Smith E., Posleman A., et al. Efficacy of pneumococcal nontypable Haemophilus influenzae Protein D conjugate vaccine (PHiD-CV) in young Latin American children: a double-blind randomized controlled trial. PLOS Med 2014, 11:e1001657.
32. Prymula R., Habib A., Francois N., Borys D., Schuerman L. Immunological memory and nasopharyngeal carriage in 4-year-old children previously primed and boosted with 10-valent pneumococcal non-typeable Haemophilus influenzae Protein D conjugate vaccine (PHiD-CV) with or without concomitant prophylactic paracetamol. Vaccine 2013, 31:2080-2088.
33. Prymula R., Hanovcova I., Splino M., Kriz P., Motlova J., Lebedova V., et al. Impact of the 10-valent pneumococcal non-typeable Haemophilus influenzae Protein D conjugate vaccine (PHiD-CV) on bacterial nasopharyngeal carriage. Vaccine 2011, 29:1959-1967.
34. van den Bergh M.R., Spijkerman J., Swinnen K.M., Francois N.A., Pascal T.G., Borys D., et al. Effects of the 10-valent pneumococcal nontypeable Haemophilus influenzae Protein D-conjugate vaccine on nasopharyngeal bacterial colonization in young children: a randomized controlled trial. Clin Infect Dis 2012, 56:e30-e39.
35. Sun W., Jacoby P., Riley T.V., Bowman J., Leach A.J., Coates H., et al. Association between early bacterial carriage and otitis media in aboriginal and non-aboriginal children in a semi-arid area of Western Australia: a cohort study. BMC Infect Dis 2012, 12:366.
36. Faden H., Duffy L., Wasielewski R., Wolf J., Krystofik D., Tung Y. Relationship between nasopharyngeal colonization and the development of otitis media in children. Tonawanda/Williamsville Pediatrics. J Infect Dis 1997, 175:1440-1445.
37. Wiertsema S.P., Corscadden K.J., Mowe E.N., Zhang G., Vijayasekaran S., Coates H.L., et al. IgG responses to Pneumococcal and Haemophilus influenzae protein antigens are not impaired in children with a history of recurrent acute otitis media. PloS ONE 2012, 7:e49061.
38. Akkoyunlu M., Forsgren A. Local and systemic antibody levels against Protein D of Haemophilus influenzae following immunization and infection in rats. APMIS 1996, 104:709-717.
39. Janson H., Heden L.O., Forsgren A. Protein D, the immunoglobulin D-binding protein of Haemophilus influenzae, is a lipoprotein. Infect Immun 1992, 60:1336-1342.
40. De Chiara M., Hood D., Muzzi A., Pickard D.J., Perkins T., Pizza M., et al. Genome sequencing of disease and carriage isolates of nontypeable Haemophilus influenzae identifies discrete population structure. Proc Natl Acad Sci U S A 2014, 111:5439-5444.
41. Morey P., Viadas C., Euba B., Hood D.W., Barberan M., Gil C., et al. Relative contributions of lipooligosaccharide inner and outer core modifications to nontypeable Haemophilus influenzae pathogenesis. Infect Immun 2013, 81:4100-4111.
42. Ganesan S., Faris A.N., Comstock A.T., Sonstein J., Curtis J.L., Sajjan U.S. Elastase/LPS-exposed mice exhibit impaired innate immune responses to bacterial challenge: role of scavenger receptor A. Am J Pathol 2012, 180:61-72.
43. Foxwell A.R., Cripps A.W., Dear K.B. Haemophilus influenzae oral whole cell vaccination for preventing acute exacerbations of chronic bronchitis. Cochrane Database Syst Rev 2006, [CD001958].
44. Pang B., Hong W., West-Barnette S.L., Kock N.D., Swords W.E. Diminished ICAM-1 expression and impaired pulmonary clearance of nontypeable Haemophilus influenzae in a mouse model of chronic obstructive pulmonary disease/emphysema. Infect Immun 2008, 76:4959-4967.
45. Toews G.B., Vial W.C., Hansen E.J. Role of C5 and recruited neutrophils in early clearance of nontypable Haemophilus influenzae from murine lungs. Infect Immun 1985, 50:207-212.
46. Wang X., Moser C., Louboutin J.P., Lysenko E.S., Weiner D.J., Weiser J.N., et al. Toll-like receptor 4 mediates innate immune responses to Haemophilus influenzae infection in mouse lung. J Immunol 2002, 168:810-815.
47. Gaschler G.J., Skrtic M., Zavitz C.C., Lindahl M., Onnervik P.O., Murphy T.F., et al. Bacteria challenge in smoke-exposed mice exacerbates inflammation and skews the inflammatory profile. Am J Respir Crit Care Med 2009, 179:666-675.
48. Berenson C.S., Kruzel R.L., Eberhardt E., Dolnick R., Minderman H., Wallace P.K., et al. Impaired innate immune alveolar macrophage response and the predilection for COPD exacerbations. Thorax 2014.
49. Unger B.L., Faris A.N., Ganesan S., Comstock A.T., Hershenson M.B., Sajjan U.S. Rhinovirus attenuates non-typeable Hemophilus influenzae-stimulated IL-8 responses via TLR2-dependent degradation of IRAK-1. PLoS Pathog 2012, 8:e1002969.
50. McGillivary G., Mason K.M., Jurcisek J.A., Peeples M.E., Bakaletz L.O. Respiratory syncytial virus-induced dysregulation of expression of a mucosal beta-defensin augments colonization of the upper airway by non-typeable Haemophilus influenzae. Cell Microbiol 2009, 11:1399-1408.