Contribution of Moraxella catarrhalis type IV pili to nasopharyngeal colonization and biofilm formation

Infection and Immunity

Volumn 75, Issue 12, 2007, Pages 5559-5564

  Luke, Nicole R ^a,b   Jurcisek, Joseph A ^c   Bakaletz, Lauren O ^c   Campagnari, Anthony A ^a,b  

^a UNIVERSITY AT BUFFALO   (United States)

^b UNIVERSITY AT BUFFALO   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

PILIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; BACTERIUM PILUS; BIOFILM; CHINCHILLA; CONTINUOUS FLOW REACTOR; CONTROLLED STUDY; EUKARYOTIC CELL; GENETIC CONSERVATION; HUMAN; HUMAN TISSUE; MORAXELLA CATARRHALIS; NASOPHARYNX; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS;

ANIMALS; BIOFILMS; CHINCHILLA; FIMBRIAE, BACTERIAL; HUMANS; MODELS, ANIMAL; MORAXELLA (BRANHAMELLA) CATARRHALIS; MORAXELLACEAE INFECTIONS; NASOPHARYNX;

EID: 36749067795     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.00946-07     Document Type: Article

References (44)

1. Aebi, C., L. D. Cope, J. L. Latimer, S. E. Thomas, C. A. Slaughter, G. H. McCracken, Jr., and E. J. Hansen. 1998. Mapping of a protective epitope of the CopB outer membrane protein of Moraxella catarrhalis. Infect. Immun. 66:540-548.
2. Aebi, C., E. R. Lafontaine, L. D. Cope, J. L. Latimer, S. L. Lumbley, G. H. McCracken, Jr., and E. J. Hansen. 1998. Phenotypic effect of isogenic uspA1 and uspA2 mutations on Moraxella catarrhalis 035E. Infect. Immun. 66:3113-3119.
3. Aebi, C., I. Maciver, J. L. Latimer, L. D. Cope, M. K. Stevens, S. E. Thomas, G. H. McCracken, Jr., and E. J. Hansen. 1997. A protective epitope of Moraxella catarrhalis is encoded by two different genes. Infect. Immun. 65:4367-4377.
4. Bakaletz, L. O., R. L. Daniels, and D. J. Lim. 1993. Modeling adenovirus type 1-induced otitis media in the chinchilla: effect on ciliary activity and fluid transport function of eustachian tube mucosal epithelium. J. Infect. Dis. 168:865-872.
5. Becker, P. D., G. M. Bertot, D. Souss, T. Ebensen, C. A. Guzman, and S. Grinstein. 2007. Intranasal vaccination with recombinant outer membrane protein CD and adamantylamide dipeptide as the mucosal adjuvant enhances pulmonary clearance of Moraxella catarrhalis in an experimental murine model. Infect. Immun. 75:1778-1784.
6. Bieber, D., S. W. Ramer, C. Y. Wu, W. J. Murray, T. Tobe, R. Fernandez, and G. K. Schoolnik. 1998. Type IV pili, transient bacterial aggregates, and virulence of enteropathogenic Escherichia coli. Science 280:2114-2118.
7. Bullard, B., S. Lipski, and E. R. Lafontaine. 2007. Regions important for the adhesin activity of Moraxella catarrhalis Hag. BMC Microbiol. 7:65.
8. Cope, L. D., E. R. Lafontaine, C. A. Slaughter, C. A. Hasemann, Jr., C. Aebi, F. W. Henderson, G. H. McCracken, Jr., and E. J. Hansen. 1999. Characterization of the Moraxella catarrhalis uspA1 and uspA2 genes and their encoded products. J. Bacteriol. 181:4026-4034.
9. Costerton, J. W., P. S. Stewart, and E. P. Greenberg. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284:1318-1322.
10. Davey, M. E., and G. A. O'Toole. 2000. Microbial biofilms: from ecology to molecular genetics. Microbiol. Mol. Biol. Rev. 64:847-867.
11. Donlan, R. M., and J. W. Costerton. 2002. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin. Microbiol. Rev. 15:167-193.
12. Giltner, C. L., E. J. van Schaik, G. F. Audette, D. Kao, R. S. Hodges, D. J. Hassett, and R. T. Irvin. 2006. The Pseudomonas aeruginosa type IV pilin receptor binding domain functions as an adhesin for both biotic and abiotic surfaces. Mol. Microbiol. 59:1083-1096.
13. Greiner, L. L., H. Watanabe, N. J. Phillips, J. Shao, A. Morgan, A. Zaleski, B. W. Gibson, and M. A. Apicella. 2004. Nontypeable Haemophilus influenzae strain 2019 produces a biofilm containing N-acetylneuraminic acid that may mimic sialylated O-linked glycans. Infect. Immun. 72:4249-4260.
14. Hall-Stoodley, L., F. Z. Hu, A. Gieseke, L. Nistico, D. Nguyen, J. Hayes, M. Forbes, D. P. Greenberg, B. Dice, A. Burrows, P. A. Wackym, P. Stoodley, J. C. Post, G. D. Ehrlich, and J. E. Kerschner. 2006. Direct detection of bacterial biofilms on the middle-ear mucosa of children with chronic otitis media. JAMA 296:202-211.
15. Hansen, J. K., and K. T. Forest. 2006. Type IV pilin structures: insights on shared architecture, fiber assembly, receptor binding and type II secretion. J. Mol. Microbiol. Biotechnol. 11:192-207.
16. Holm, M. M., S. L. Vanlerberg, I. M. Foley, D. D. Sledjeski, and E. R. Lafontaine. 2004. The Moraxella catarrhalis porin-like outer membrane pro-tein CD is an adhesin for human lung cells. Infect. Immun. 72:1906-1913.
17. Jurcisek, J. A., J. E. Bookwalter, B. D. Baker, S. Fernandez, L. A. Novotny, R. S. Munson, Jr., and L. O. Bakaletz. 2007. The PilA protein of nontypeable Haemophilus influenzae plays a role in biofilm formation, adherence to epithelial cells and colonization of the mammalian upper respiratory tract. Mol. Microbiol. 65:1288-1299.
18. Jurcisek, J. A., J. E. Durbin, D. F. Kusewitt, and L. O. Bakaletz. 2003. Anatomy of the nasal cavity in the chinchilla. Cells Tissues Organs 174:136-152.
19. Klausen, M., A. Aaes-Jorgensen, S. Molin, and T. Tolker-Nielsen. 2003. Involvement of bacterial migration in the development of complex multicellular structures in Pseudomonas aeruginosa biofilms. Mol. Microbiol. 50:61-68.
20. Klausen, M, A. Heydorn, P. Ragas, L. Lambertsen, A. Aaes-Jorgensen, S. Molin, and T. Tolker-Nielsen. 2003. Biofilm formation by Pseudomonas aeruginosa wild type, flagella and type IV pili mutants. Mol. Microbiol. 48:1511-1524.
21. Lafontaine, E. R., L. D. Cope, C. Aebi, J. L. Latimer, G. H. McCracken, Jr., and E. J. Hansen. 2000. The UspA1 protein and a second type of UspA2 protein mediate adherence of Moraxella catarrhalis to human epithelial cells in vitro. J. Bacteriol. 182:1364-1373.
22. Lee, K., J. W. Costerton, J. Ravel, R. K. Auerbach, D. M. Wagner, P. Keim, and J. G. Leid. 2007. Phenotypic and functional characterization of Bacillus anthracis biofilms. Microbiology 153:1693-1701.
23. Liu, D. F., J. C. McMichael, and S. M. Baker. 2007. Moraxella catarrhalis outer membrane protein CD elicits antibodies that inhibit CD binding to human mucin and enhance pulmonary clearance of M. catarrhalis in a mouse model. Infect. Immun. 75:2818-2825.
24. Luke, N. R., S. Allen, B. W. Gibson, and A. A. Campagnari. 2003. Identification of a 3-deoxy-D-manno-octulosonic acid biosynthetic operon in Moraxella catarrhalis and analysis of a KdsA-deficient isogenic mutant. Infect. Immun. 71:6426-6434.
25. Luke, N. R., and A. A. Campagnari. 1999. Construction and characterization of Moraxella catarrhalis mutants defective in expression of transferrin receptors. Infect. Immun. 67:5815-5819.
26. Luke, N. R., A. J. Howlett, J. Shao, and A. A. Campagnari. 2004. Expression of type IV pili by Moraxella catarrhalis is essential for natural competence and is affected by iron limitation. Infect. Immun. 72:6262-6270.
27. Mason, K. M., R. S. Munson, Jr., and L. O. Bakaletz. 2005. A mutation in the sap operon attenuates survival of nontypeable Haemophilus influenzae in a chinchilla model of otitis media. Infect. Immun. 73:599-608.
28. Mattick, J. S. 2002. Type IV pili and twitching motility. Annu. Rev. Microbiol. 56:289-314.
29. McMichael, J. C. 2000. Vaccines for Moraxella catarrhalis. Vaccine 19(Suppl. 1):S101-S107.
30. Meier, P. S., R. Troller, N. Heiniger, J. P. Hays, A. van Belkum, and C. Aebi. 2006. Unveiling electrotransformation of Moraxella catarrhalis as a process of natural transformation. FEMS Microbiol. Lett. 262:72-76.
31. Murphy, T. F. 2005. Vaccine development for non-typeable Haemophilus influenzae and Moraxella catarrhalis: progress and challenges. Expert Rev. Vaccines 4:843-853.
32. O'Toole, G., H. B. Kaplan, and R. Kolter. 2000. Biofilm formation as microbial development. Annu. Rev. Microbiol. 54:49-79.
33. O'Toole, G. A., and R. Kolter. 1998. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 30:295-304.
34. Paranjpye, R. N., and M. S. Strom. 2005. A Vibrio vulnificus type IV pilin contributes to biofilm formation, adherence to epithelial cells, and virulence. Infect. Immun. 73:1411-1422.
35. Pearson, M. M., E. R. Lafontaine, N. J. Wagner, J. W. St Geme III, and E. J. Hansen. 2002. A hag mutant of Moraxella catarrhalis strain O35E is deficient in hemagglutination, autoagglutination, and immunoglobulin D-binding activities. Infect. Immun. 70:4523-4533.
36. Peng, D., B. P. Choudhury, R. S. Petralia, R. W. Carlson, and X. X. Gu. 2005. Roles of 3-deoxy-D-manno-2-octulosonic acid transferase from Moraxella catarrhalis in lipooligosaccharide biosynthesis and virulence. Infect. Immun. 73:4222-4230.
37. Stanley, N. R., and B. A. Lazazzera. 2004. Environmental signals and regulatory pathways that influence biofilm formation. Mol. Microbiol. 52:917-924.
38. Strom, M. S., and S. Lory. 1993. Structure-function and biogenesis of the type IV pili. Annu. Rev. Microbiol. 47:565-596.
39. Tan, T. T., T. Nordstrom, A. Forsgren, and K. Riesbeck. 2005. The respiratory pathogen Moraxella catarrhalis adheres to epithelial cells by interacting with fibronectin through ubiquitous surface proteins A1 and A2. J. Infect. Dis. 192:1029-1038.
40. Unhanand, M., I. Maciver, O. Ramilo, O. Arencibia-Mireles, J. C. Argyle, G. H. McCracken, Jr., and E. J. Hansen. 1992. Pulmonary clearance of Moraxella catarrhalis in an animal model. J. Infect. Dis. 165:644-650.
41. Verduin, C. M., C. Hol, A. Fleer, H. van Dijk, and A. van Belkum. 2002. Moraxella catarrhalis: from emerging to established pathogen. Clin. Microbiol. Rev. 15:125-144.
42. Wang, Y., W. Shi, W. Chen, and C. Chen. 2003. Type IV pilus gene homologs pilABCD are required for natural transformation in Actinobacillus actinomycetemcomitans. Gene 312:249-255.
43. Watnick, P. I., and R. Kolter. 1999. Steps in the development of a Vibrio cholerae El Tor biofilm. Mol. Microbiol. 34:586-595.
44. Yokota, S., A. Harimaya, K. Sato, Y. Somekawa, T. Himi, and N. Fujii. 2007. Colonization and turnover of Streptococcus pneumoniae, Haemophilus influenzae, and Moraxella catarrhalis in otitis-prone children. Microbiol. Immunol. 51:223-230.