Haemophilus influenzae forms biofilms on airway epithelia: Implications in cystic fibrosis

American Journal of Respiratory and Critical Care Medicine

Volumn 174, Issue 2, 2006, Pages 213-220

  Starner, Timothy D ^a   Zhang, Niu ^a   Kim, GunHee ^a   Apicella, Michael A ^a   McCray Jr , Paul B ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

Bacterial infections; Inflammation; Lung diseases

Indexed keywords

ANTIBIOTIC AGENT; CHEMOKINE; CYTOKINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN;

APICAL MEMBRANE; ARTICLE; BIOFILM; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; HAEMOPHILUS INFLUENZAE TYPE A; HUMAN; HUMAN CELL; IN VIVO CULTURE; INFANT; LUNG FIBROSIS; LUNG LAVAGE; MORPHOLOGY; PATHOGENESIS; PRIORITY JOURNAL; RESPIRATORY EPITHELIUM; RESPIRATORY TRACT INFECTION;

BIOFILMS; BRONCHOALVEOLAR LAVAGE FLUID; CHILD; CHILD, PRESCHOOL; COCULTURE TECHNIQUES; CYSTIC FIBROSIS; GENTAMICINS; HAEMOPHILUS INFLUENZAE; HUMANS; INFANT; INTERLEUKIN-8; MICROBIAL SENSITIVITY TESTS; NF-KAPPA B; RESPIRATORY MUCOSA;

EID: 33745757955     PISSN: 1073449X     EISSN: 1073449X     Source Type: Journal    
DOI: 10.1164/rccm.200509-1459OC     Document Type: Article

References (48)

1. Lam J, Chan R, Lam K, Costerton JW. Production of mucoid microcolonies by Pseudomonas aeruginosa within infected lungs in cystic fibrosis. Infect Immun 1980;28:546-556.
2. Singh PK, Schaefer AL, Parsek MR, Moninger TO, Welsh MJ, Greenberg EP. Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. Nature 2000;407:762-764.
3. Parsek MR, Singh PK. Bacterial biofilms: an emerging link to disease pathogenesis. Annu Rev Microbiol 2003;57:677-701.
4. Nickel JC, Ruseska I, Wright JB, Costerton JW. Tobramycin resistance of Pseudomonas aeruginosa cells growing as a biofilm on urinary catheter material. Antimicrob Agents Chemother 1985;27:619-624.
5. Jesaitis AJ, Franklin MJ, Berglund D, Sasaki M, Lord CI, Bleazard JB, Duffy JE, Beyenal H, Lewandowski Z. Compromised host defense on Pseudomonas aeruginosa biofilms: characterization of neutrophil and biofilm interactions. J Immunol 2003;171:4329-4339.
6. Swords WE, Moore ML, Godzicki L, Bukofzer G, Mitten MJ, VonCannon J. Sialylation of lipooligosaccharides promotes biofilm formation by nontypeable Haemophilus influenzae. Infect Immun 2004;72:106-113.
7. Greiner LL, Watanabe H, Phillips NJ, Shao J, Morgan A, Zaleski A, Gibson BW, Apicella MA. Nontypeable Haemophilus influenzae strain 2019 produces a biofilm containing N-acetylneuraminic acid that may mimic sialylated O-linked glycans. Infect Immun 2004;72:4249-4260.
8. Murphy TF, Kirkham C. Biofilm formation by nontypeable Haemophilus influenzae: strain variability, outer membrane antigen expression and role of pili. BMC Microbiol 2002;2:7.
9. Ehrlich GD, Veeh R, Wang X, Costerton JW, Hayes JD, Hu FZ, Daigle BJ, Ehrlich MD, Post JC. Mucosal biofilm formation on middle-ear mucosa in the chinchilla model of otitis media. JAMA 2002;287:1710-1715.
10. Post JC. Direct evidence of bacterial biofilms in otitis media. Laryngoscope 2001;111:2083-2094.
11. Bilton D, Pye A, Johnson MM, Mitchell JL, Dodd M, Webb AK, Stockley RA, Hill SL. The isolation and characterization of non-typeable Haemophilus influenzae from the sputum of adult cystic fibrosis patients. Eur Respir J 1995;8:948-953.
12. Rosenfeld M, Gibson RL, McNamara S, Emerson J, Burns JL, Castile R, Hiatt P, McCoy K, Wilson CB, Inglis A, et al. Early pulmonary infection, inflammation, and clinical outcomes in infants with cystic fibrosis. Pediatr Pulmonol 2001;32:356-366.
13. Smith A. Pathogenesis of bacterial bronchitis in cystic fibrosis. Pediatr Infect Dis J 1997;16:91-95. [Discussion 95-96, 123-126.]
14. Abman SH, Ogle JW, Harbeck RJ, Butler-Simon N, Hammond KB, Accurso FJ. Early bacteriologic, immunologic, and clinical courses of young infants with cystic fibrosis identified by neonatal screening. J Pediatr 1991;119:211-217.
15. Muhlebach MS, Stewart PW, Leigh MW, Noah TL. Quantitation of inflammatory responses to bacteria in young cystic fibrosis and control patients. Am J Respir Crit Care Med 1999;160:186-191.
16. Starner TD, Zhang N, Shao J, Apicella MA, McCray PB Jr. Haemophilus influenzae forms biofilms on airway epithelia: implications for early cystic fibrosis lung disease. Pediatr Pulmonol Suppl 2005;28:300.
17. Starner TD, Zhang N, Shao J, Apicella MA, McCray PB Jr. Nontypeable Haemophilus influenzae forms biofilms on human airway epithelia. Pediatr Pulmonol Suppl 2004;27:278.
18. Campagnari AA, Spinola SM, Lesse AJ, Kwaik YA, Mandrell RE, Apicella MA. Lipooligosaccharide epitopes shared among gram-negative non-enteric mucosal pathogens. Microb Pathog 1990;8:353-362.
19. Campagnari AA, Gupta MR, Dudas KC, Murphy TF, Apicella MA. Antigenic diversity of lipooligosaccharides of nontypable Haemophilus influenzae. Infect Immun 1987;55:882-887.
20. Jones PA, Samuels NM, Phillips NJ, Munson RS Jr, Bozue JA, Arseneau JA, Nichols WA, Zaleski A, Gibson BW, Apicella MA. Haemophilus influenzae type b strain A2 has multiple sialyltransferases involved in lipooligosaccharide sialylation. J Biol Chem 2002;277:14598-14611.
21. Hood DW, Cox AD, Gilbert M, Makepeace K, Walsh S, Deadman ME, Cody A, Martin A, Mansson M, Schweda EK, et al. Identification of a lipopolysaccharide alpha-2,3-sialyltransferase from Haemophilus influenzae. Mol Microbiol 2001;39:341-350.
22. Mason KM, Munson RS Jr, Bakaletz LO. Nontypeable Haemophilus influenzae gene expression induced in vivo in a chinchilla model of otitis media. Infect Immun 2003;71:3454-3462.
23. Mitchell MA, Skowronek K, Kauc L, Goodgal SH. Electroporation of Haemophilus influenzae is effective for transformation of plasmid but not chromosomal DNA. Nucleic Acids Res 1991;19:3625-3628.
24. O'Toole GA, Kolter R. Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol Microbiol 1998;28:449-461.
25. Karp PH, Moninger TO, Weber SP, Nesselhauf TS, Launspach JL, Zabner J, Welsh MJ. An in vitro model of differentiated human airway epithelia: methods for establishing primary cultures. Methods Mol Biol 2002;188:115-137.
26. Heydorn A, Nielsen AT, Hentzer M, Sternberg C, Givskov M, Ersboll BK, Molin S. Quantification of biofilm structures by the novel computer program COMSTAT. Microbiology 2000;146:2395-2407.
27. Isberg RR, Falkow S. A single genetic locus encoded by Yersinia pseudotuberculosis permits invasion of cultured animal cells by Escherichia coli K-12. Nature 1985;317:262-264.
28. Swords WE, Buscher BA, Ver Steeg Ii K, Preston A, Nichols WA, Weiser JN, Gibson BW, Apicella MA. Non-typeable Haemophilus influenzae adhere to and invade human bronchial epithelial cells via an interaction of lipooligosaccharide with the PAF receptor. Mol Microbiol 2000;37:13-27.
29. Sanlioglu S, Williams CM, Samavati L, Butler NS, Wang G, McCray PB Jr, Ritchie TC, Hunninghake GW, Zandi E, Engelhardt JF. Lipopolysaccharide induces Rac1-dependent reactive oxygen species formation and coordinates tumor necrosis factor-alpha secretion through IKK regulation of NF-kappa B. J Biol Chem 2001;276:30188-30198.
30. Armstrong DS, Grimwood K, Carlin JB, Carzino R, Olinsky A, Phelan PD. Bronchoalveolar lavage or oropharyngeal cultures to identify lower respiratory pathogens in infants with cystic fibrosis. Pediatr Pulmonol 1996;21:267-275.
31. Rayner MG, Zhang Y, Gorry MC, Chen Y, Post JC, Ehrlich GD. Evidence of bacterial metabolic activity in culture-negative otitis media with effusion. JAMA 1998;279:296-299.
32. Chmiel JF, Berger M, Konstan MW. The role of inflammation in the pathophysiology of CF lung disease. Clin Rev Allergy Immunol 2002;23:5-27.
33. Anwar H, van Biesen T, Dasgupta M, Lam K, Costerton JW. Interaction of biofilm bacteria with antibiotics in a novel in vitro chemostat system. Antimicrob Agents Chemother 1989;33:1824-1826.
34. Williams I, Venables WA, Lloyd D, Paul F, Critchley I. The effects of adherence to silicone surfaces on antibiotic susceptibility in Staphylococcus aureus. Microbiology 1997;143:2407-2413.
35. Murphy TF, Brauer AL, Schiffmacher AT, Sethi S. Persistent colonization by Haemophilus influenzae in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2004;170:266-272.
36. Kuklinska D, Kilian M. Relative proportions of Haemophilus species in the throat of healthy children and adults. Eur J Clin Microbiol 1984;3:249-252.
37. Farjo RS, Foxman B, Patel MJ, Zhang L, Pettigrew MM, McCoy SI, Marrs CF, Gilsdorf JR. Diversity and sharing of Haemophilus influenzae strains colonizing healthy children attending day-care centers. Pediatr Infect Dis J 2004;23:41-46.
38. Rayner RJ, Hiller EJ, Ispahani P, Baker M. Haemophilus infection in cystic fibrosis. Arch Dis Child 1990;65:255-258.
39. Moller LV, Timens W, van der Bij W, Kooi K, de Wever B, Dankert J, van Alphen L. Haemophilus influenzae in lung explants of patients with end-stage pulmonary disease. Am J Respir Crit Care Med 1998;157:950-956.
40. Roman F, Canton R, Perez-Vazquez M, Baquero F, Campos J. Dynamics of long-term colonization of respiratory tract by Haemophilus influenzae in cystic fibrosis patients shows a marked increase in hypermutable strains. J Clin Microbiol 2004;42:1450-1459.
41. Miravitlles M, Espinosa C, Fernandez-Laso E, Martos JA, Maldonado JA, Gallego M. Relationship between bacterial flora in sputum and functional impairment in patients with acute exacerbations of COPD. Study Group of Bacterial Infection in COPD. Chest 1999;116:40-46.
42. Dagan R, Abramson O, Leibovitz E, Greenberg D, Lang R, Goshen S, Yagupsky P, Leiberman A, Fliss DM. Bacteriologic response to oral cephalosporins: are established susceptibility breakpoints appropriate in the case of acute otitis media? J Infect Dis 1997;176:1253-1259.
43. Groeneveld K, van Alphen L, Eijk PP, Visschers G, Jansen HM, Zanen HC. Endogenous and exogenous reinfections by Haemophilus influenzae in patients with chronic obstructive pulmonary disease: the effect of antibiotic treatment on persistence. J Infect Dis 1990;161:512-517.
44. Frick AG, Joseph TD, Pang L, Rabe AM, St Geme JW III, Look DC. Haemophilus influenzae stimulates ICAM-1 expression on respiratory epithelial cells. J Immunol 2000;164:4185-4196.
45. Wang X, Moser C, Louboutin JP, Lysenko ES, Weiner DJ, Weiser JN, Wilson JM. Toll-like receptor 4 mediates innate immune responses to Haemophilus influenzae infection in mouse lung. J Immunol 2002;168:810-815.
46. Starner TD, Barker CK, Jia HP, Kang Y, McCray PB Jr. CCL20 is an inducible product of human airway epithelia with innate immune properties. Am J Respir Cell Mol Biol 2003;29:627-633.
47. Singh P, Parsek M, Tack B, Costerton J, Greenberg E, Welsh M. The activity of airway surface liquid antimicrobial factors against P. aeruginosa biofilms [abstract]. Am J Respir Crit Care Med 2000;161:A128.
48. Doring G, Hoiby N. Early intervention and prevention of lung disease in cystic fibrosis: a European consensus. J Cyst Fibros 2004;3:67-91.