A carcinoembryonic antigen-related cell adhesion molecule 1 homologue plays a pivotal role in nontypeable Haemophilus influenzae colonization of the chinchilla nasopharynx via the outer membrane protein P5-homologous adhesin

Infection and Immunity

Volumn 76, Issue 1, 2008, Pages 48-55

  Bookwalter, James E ^a   Jurcisek, Joseph A ^a   Gray Owen, Scott D ^b   Fernandez, Soledad ^c   McGillivary, Glen ^a   Bakaletz, Lauren O ^a,d  

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

^b UNIVERSITY OF TORONTO   (Canada)

^c OHIO STATE UNIVERSITY   (United States)

^d THE RESEARCH INSTITUTE AT NATIONWIDE CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; CARCINOEMBRYONIC ANTIGEN RELATED CELL ADHESION MOLECULE 1; CEACAM RECEPTOR; OUTER MEMBRANE PROTEIN; OUTER MEMBRANE PROTEIN P5; PROTEIN NTHI P5; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIUM IDENTIFICATION; CHINCHILLA; CONTROLLED STUDY; EAR INFECTION; HAEMOPHILUS INFLUENZAE; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; IN VIVO STUDY; NASOPHARYNX; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; RECEPTOR BINDING;

ANIMALS; ANTIGENS, CD; BACTERIAL OUTER MEMBRANE PROTEINS; CARRIER STATE; CELL ADHESION MOLECULES; CHINCHILLA; GENE EXPRESSION REGULATION; HAEMOPHILUS INFLUENZAE; HELA CELLS; HUMANS; NASOPHARYNX;

EID: 37749009078     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.00980-07     Document Type: Article

References (56)

1. Avadhanula, V., C. A. Rodriguez, J. P. Devincenzo, Y. Wang, R. J. Webby, G. C. Ulett, and E. E. Adderson. 2006. Respiratory viruses augment the adhesion of bacterial pathogens to respiratory epithelium in a viral species-and cell type-dependent manner. J. Virol. 80:1629-1636.
2. Avadhanula, V., C. A. Rodriguez, G. C. Ulett, L. O. Bakaletz, and E. E. Adderson. 2006. Nontypeable Haemophilus influenzae adheres to intercellular adhesion molecule 1 (ICAM-1) on respiratory epithelial cells and up-regulates ICAM-1 expression. Infect. Immun. 74:830-838.
3. 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.
4. Bakaletz, L. O., T. Hoepf, and D. J. Lim. 1991. Inhibition of adherence of NTHi to human oropharyngeal cells - and ELISA assay, abstr. 145. Abstr. 5th Int. Symp. Recent Adv. Otitis Media.
5. Bakaletz, L. O., B. J. Kennedy, L. A. Novotny, G. Dequesne, J. Cohen, and Y. Lobet. 1999. 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. 67:2746-2762.
6. Bakaletz, L. O., E. R. Leake, J. M. Billy, and P. T. Kaumaya. 1997. Relative immunogenicity and efficacy of two synthetic chimeric peptides of fimbrin as vaccinogens against nasopharyngeal colonization by nontypeable Haemophilus influenzae in the chinchilla. Vaccine 15:955-961.
7. Bakaletz, L. O., B. M. Tallan, T. Hoepf, T. F. DeMaria, H. G. Birck, and D. J. Lim. 1988. Frequency of fimbriation of nontypable Haemophilus influenzae and its ability to adhere to chinchilla and human respiratory epithelium. Infect. Immun. 56:331-335.
8. Bos, M. P., F. Grunert, and R. J. Belland. 1997. Differential recognition of members of the carcinoembryonic antigen family by Opa variants of Neisseria gonorrhoeae. Infect. Immun. 65:2353-2361.
9. Boulton, I. C., and S. D. Gray-Owen. 2002. Neisserial binding to CEACAM1 arrests the activation and proliferation of CD4+ T lymphocytes. Nat. Immunol. 3:229-236.
10. Chen, T., and E. C. Gotschlich. 1996. CGM1a antigen of neutrophils, a receptor of gonococcal opacity proteins. Proc. Natl. Acad. Sci. USA 93: 14851-14856.
11. Chen, T., F. Grunert, A. Medina-Marino, and E. C. Gotschlich. 1997. Several carcinoembryonic antigens (CD66) serve as receptors for gonococcal opacity proteins. J. Exp. Med. 185:1557-1564.
12. Gray-Owen, S. D. 2003. Neisserial Opa proteins: impact on colonization, dissemination and immunity. Scand. J. Infect. Dis. 35:614-618.
13. Gray-Owen, S. D., and R. S. Blumberg. 2006. CEACAM1: contact-dependent control of immunity. Nat. Rev. Immunol. 6:433-446.
14. Gray-Owen, S. D., C. Dehio, A. Haude, F. Grunert, and T. F. Meyer. 1997. CD66 carcinoembryonic antigens mediate interactions between Opa-expressing Neisseria gonorrhoeae and human polymorphonuclear phagocytes. EMBO J. 16:3435-3445.
15. Gray-Owen, S. D., D. R. Lorenzen, A. Haude, T. F. Meyer, and C. Dehio. 1997. Differential Opa specificities for CD66 receptors influence tissue interactions and cellular response to Neisseria gonorrhoeae. Mol. Microbiol. 26:971-980.
16. Hammarstrom, S. 1999. The carcinoembryonic antigen (CEA) family: structures, suggested functions and expression in normal and malignant tissues. Semin. Cancer Biol. 9:67-81.
17. Han, E., D. Phan, P. Lo, M. N. Poy, R. Behringer, S. M. Najjar, and S. H. Lin. 2001. Differences in tissue-specific and embryonic expression of mouse Ceacam1 and Ceacam2 genes. Biochem. J. 355:417-423.
18. Harrison, A., D. W. Dyer, A. Gillaspy, W. C. Ray, R. Mungur, M. B. Carson, H. Zhong, J. Gipson, M. Gipson, L. S. Johnson, L. Lewis, L. O. Bakaletz, and R. S. Munson, Jr. 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.
19. Hill, D. J., A. M. Edwards, H. A. Rowe, and M. Virji. 2005. Carcinoembryonic antigen-related cell adhesion molecule (CEACAM)-binding recombinant polypeptide confers protection against infection by respiratory and urogenital pathogens. Mol. Microbiol. 55:1515-1527.
20. Hill, D. J., M. A. Toleman, D. J. Evans, S. Villullas, L. Van Alphen, and M. Virji. 2001. The variable P5 proteins of typeable and non-typeable Haemophilus influenzae target human CEACAM1. Mol. Microbiol. 39:850-862.
21. Hill, D. J., and M. Virji. 2003. A novel cell-binding mechanism of Moraxella catarrhalis ubiquitous surface protein UspA: specific targeting of the N-domain of carcinoembryonic antigen-related cell adhesion molecules by UspA1. Mol. Microbiol. 48:117-129.
22. Jiang, Z., N. Nagata, E. Molina, L. O. Bakaletz, H. Hawkins, and J. A. Patel. 1999. Fimbria-mediated enhanced attachment of nontypeable Haemophilus influenzae to respiratory syncytial virus-infected respiratory epithelial cells. Infect. Immun. 67:187-192.
23. 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.
24. Kennedy, B. J., L. A. Novotny, J. A. Jurcisek, Y. Lobet, and L. O. Bakaletz. 2000. 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. 68:2756-2765.
25. Kuespert, K., S. Pils, and C. R. Hauck. 2006. CEACAMs: their role in physiology and pathophysiology. Curr. Opin. Cell Biol. 18:565-571.
26. Kyd, J. M., A. W. Cripps, L. A. Novotny, and L. O. Bakaletz. 2003. Efficacy of the 26-kilodalton outer membrane protein and two P5 fimbrin-derived immunogens to induce clearance of nontypeable Haemophilus influenzae from the rat middle ear and lungs as well as from the chinchilla middle ear and nasopharynx. Infect. Immun. 71:4691-4699.
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. Mason, K. M., R. S. Munson, Jr., and L. O. Bakaletz. 2003. Nontypeable Haemophilus influenzae gene expression induced in vivo in a chinchilla model of otitis media. Infect. Immun. 71:3454-3462.
29. McCaw, S. E., J. Schneider, E. H. Liao, W. Zimmermann, and S. D. Gray-Owen. 2003. Immunoreceptor tyrosine-based activation motif phosphorylation during engulfment of Neisseria gonorrhoeae by the neutrophil-restricted CEACAM3 (CD66d) receptor. Mol. Microbiol. 49:623-637.
30. McGillivary, G., W. C. Ray, C. L. Bevins, R. S. Munson, Jr., and L. O. Bakaletz. 2007. A member of the cathelicidin family of antimicrobial peptides is produced in the upper airway of the chinchilla and its mRNA expression is altered by common viral and bacterial co-pathogens of otitis media. Mol. Immunol. 44:2446-2458.
31. Miyamoto, N., and L. O. Bakaletz. 1997. Kinetics of the ascension of NTHi from the nasopharynx to the middle ear coincident with adenovirus-induced compromise in the chinchilla. Microb. Pathog. 23:119-126.
32. Miyamoto, N., and L. O. Bakaletz. 1996. Selective adherence of non-typeable Haemophilus influenzae (NTHi) to mucus or epithelial cells in the chinchilla Eustachian tube and middle ear. Microb. Pathog. 21:343-356.
33. Muenzner, P., C. Dehio, T. Fujiwara, M. Achtman, T. F. Meyer, and S. D. Gray-Owen. 2000. Carcinoembryonic antigen family receptor specificity of Neisseria meningitidis Opa variants influences adherence to and invasion of proinflammatory cytokine-activated endothelial cells. Infect. Immun. 68: 3601-3607.
34. Muenzner, P., M. Naumann, T. F. Meyer, and S. D. Gray-Owen. 2001. Pathogenic Neisseria trigger expression of their carcinoembryonic antigen-related cellular adhesion molecule 1 (CEACAM1; previously CD66a) receptor on primary endothelial cells by activating the immediate early response transcription factor, nuclear factor-kappaB. J. Biol. Chem. 276:24331-24340.
35. Najjar, S. M. 2002. Regulation of insulin action by CEACAM1. Trends Endocrinol. Metab. 13:240-245.
36. Nakamura, A., T. F. DeMaria, D. J. Lim, and C. A. van Blitterswyk. 1991. Primary culture of chinchilla middle ear epithelium. Ann. Otol. Rhinol. Laryngol. 100:774-782.
37. Nakamura, A., T. F. DeMaria, C. van Blitterswijk, and D. J. Lim. 1992. Effect of endotoxin on cultured chinchilla middle ear epithelium. Ann. Otol. Rhinol. Laryngol. 101:607-611.
38. Novotny, L. A., J. A. Jurcisek, F. Godfroid, J. T. Poolman, P. A. Denoel, and L. O. Bakaletz. 2006. 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 24:4804-4811.
39. Novotny, L. A., J. A. Jurcisek, M. E. Pichichero, and L. O. Bakaletz. 2000. Epitope mapping of the outer membrane protein P5-homologous fimbrin adhesin of nontypeable Haemophilus influenzae. Infect. Immun. 68:2119-2128.
40. Novotny, L. A., K. M. Mason, and L. O. Bakaletz. 2005. Development of a chinchilla model to allow direct, continuous, biophotonic imaging of bioluminescent nontypeable Haemophilus influenzae during experimental otitis media. Infect. Immun. 73:609-611.
41. Novotny, L. A., M. E. Pichichero, P. A. Denoel, C. Neyt, S. Vanderschrick, G. Dequesne, and L. O. Bakaletz. 2002. Detection and characterization of pediatric serum antibody to the OMP P5-homologous adhesin of nontypeable Haemophilus influenzae during acute otitis media. Vaccine 20:3590-3597.
42. Odin, P., M. Asplund, C. Busch, and B. Obrink. 1988. Immunohistochemical localization of cellCAM 105 in rat tissues: appearance in epithelia, platelets, and granulocytes. J. Histochem. Cytochem. 36:729-739.
43. Odin, P., and B. Obrink. 1987. Quantitative determination of the organ distribution of the cell adhesion molecule cell-CAM 105 by radioimmunoassay. Exp. Cell Res. 171:1-15.
44. Prall, F., P. Nollau, M. Neumaier, H. D. Haubeck, Z. Drzeniek, U. Helmchen, T. Loning, and C. Wagener. 1996. CD66a (BGP), an adhesion molecule of the carcinoembryonic antigen family, is expressed in epithelium, endothelium, and myeloid cells in a wide range of normal human tissues. J. Histochem. Cytochem. 44:35-41.
45. Reddy, M. S., J. M. Bernstein, T. F. Murphy, and H. S. Faden. 1996. Binding between outer membrane proteins of nontypeable Haemophilus influenzae and human nasopharyngeal mucin. Infect. Immun. 64:1477-1479.
46. Sarantis, H., and S. D. Gray-Owen. 2007. The specific innate immune receptor CEACAM3 triggers neutrophil bactericidal activities via a Syk kinase-dependent pathway. Cell. Microbiol. 9:2167-2180.
47. Schmitter, T., F. Agerer, L. Peterson, P. Munzner, and C. R. Hauck. 2004. Granulocyte CEACAM3 is a phagocytic receptor of the innate immune system that mediates recognition and elimination of human-specific pathogens. J. Exp. Med. 199:35-46.
48. Sirakova, T., P. E. Kolattukudy, D. Murwin, J. Billy, E. Leake, D. Lim, T. DeMaria, and L. Bakaletz. 1994. Role of fimbriae expressed by nontypeable Haemophilus influenzae in pathogenesis of and protection against otitis media and relatedness of the fimbrin subunit to outer membrane protein A. Infect. Immun. 62:2002-2020.
49. Sundberg, U., N. Beauchemin, and B. Obrink. 2004. The cytoplasmic domain of CEACAM1-L controls its lateral localization and the organization of desmosomes in polarized epithelial cells. J. Cell Sci. 117:1091-1104.
50. Suzuki, K., and L. O. Bakaletz. 1994. Synergistic effect of adenovirus type 1 and nontypeable Haemophilus influenzae in a chinchilla model of experimental otitis media. Infect. Immun. 62:1710-1718.
51. Toleman, M., E. Aho, and M. Virji. 2001. Expression of pathogen-like Opa adhesins in commensal Neisseria: genetic and functional analysis. Cell. Microbiol. 3:33-44.
52. Virji, M., K. Makepeace, D. J. Ferguson, and S. M. Watt. 1996. Carcinoembryonic antigens (CD66) on epithelial cells and neutrophils are receptors for Opa proteins of pathogenic neisseriae. Mol. Microbiol. 22:941-950.
53. Virji, M., S. M. Watt, S. Barker, K. Makepeace, and R. Doyonnas. 1996. The N-domain of the human CD66a adhesion molecule is a target for Opa proteins of Neisseria meningitidis and Neisseria gonorrhoeae. Mol. Microbiol. 22:929-939.
54. Wang, J., S. D. Gray-Owen, A. Knorre, T. F. Meyer, and C. Dehio. 1998. Opa binding to cellular CD66 receptors mediates the transcellular traversal of Neisseria gonorrhoeae across polarized T84 epithelial cell monolayers. Mol. Microbiol. 30:657-671.
55. Wong, R. L., D. Mytych, S. Jacobs, R. Bordens, and S. J. Swanson. 1997. Validation parameters for a novel biosensor assay which simultaneously measures serum concentrations of a humanized monoclonal antibody and detects induced antibodies. J. Immunol. Methods 209:1-15.
56. Yu, Q., E. M. Chow, H. Wong, J. Gu, O. Mandelboim, S. D. Gray-Owen, and M. A. Ostrowski. 2006. CEACAM1 (CD66a) promotes human monocyte survival via a phosphatidylinositol 3-kinase- and AKT-dependent pathway. J. Biol. Chem. 281:39179-39193.