The moraxella catarrhalis immunoglobulin D-binding protein MID has conserved sequences and is regulated by a mechanism corresponding to phase variation

Journal of Bacteriology

Volumn 185, Issue 7, 2003, Pages 2285-2295

  Möllenkvist, Andrea ^a   Nordström, Therése ^a   Halldén, Christer ^a   Jørgen Christensen, Jens ^b   Forsgren, Arne ^a   Riesbeck, Kristian ^a  

^a LUND UNIVERSITY HOSPITAL   (Sweden)

^b STATENS SERUM INSTITUT   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; BINDING PROTEIN; CARRIER PROTEIN; DNA; FLUORESCEIN ISOTHIOCYANATE; GUANINE; IMMUNOGLOBULIN D; NUCLEOTIDE; OUTER MEMBRANE PROTEIN; POLYCLONAL ANTIBODY; SIGNAL PEPTIDE;

AMINO ACID SEQUENCE; ARTICLE; FLOW CYTOMETRY; GENE; GENE CONTROL; GENE EXPRESSION; IMMUNOBLOTTING; MORAXELLA CATARRHALIS; NONHUMAN; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PULSED FIELD GEL ELECTROPHORESIS; RANDOM AMPLIFIED POLYMORPHIC DNA; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY;

5' FLANKING REGION; ADHESINS, BACTERIAL; AMINO ACID SEQUENCE; BLOOD; CARRIER PROTEINS; CONSERVED SEQUENCE; FLUORESCEIN-5-ISOTHIOCYANATE; FLUORESCENT DYES; GENE EXPRESSION REGULATION, BACTERIAL; GENE FREQUENCY; HUMANS; IMMUNOGLOBULIN D; MOLECULAR SEQUENCE DATA; MORAXELLA (BRANHAMELLA) CATARRHALIS; NASOPHARYNX; POLY G; REPETITIVE SEQUENCES, AMINO ACID; SEQUENCE ANALYSIS; SPUTUM; VARIATION (GENETICS);

MORAXELLA CATARRHALIS; NEGIBACTERIA; NEISSERIA;

EID: 0037379473     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.185.7.2285-2295.2003     Document Type: Article

References (54)

1. 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.
2. Aebi, C., B. Stone, M. Beucher, L. D. Cope, I. Maciver, S. E. Thomas, G. H. McCracken, Jr., P. F. Sparling, and E. J. Hansen. 1996. Expression of the CopB outer membrane protein by Moraxella catarrhalis is regulated by iron and affects iron acquisition from transferrin and lactoferrin. Infect. Immun. 64:2024-2030.
3. Ahrén, I. L., H. Janson, A. Forsgren, and K. Riesbeck. 2001. Protein D expression promotes the adherence and internalization of non-typeable Haemophilus influenzae into human monocytic cells. Microb. Pathog. 3:151-158.
4. Bootsma, H. J., P. C. Aerts, G. Posthuma, T. Harmsen, J. Verhoef, H. van Dijk, and F. R. Mooi. 1999. Moraxella (Branhamella) catarrhalis BRO beta-lactamase: a lipoprotein of gram-positive origin? J. Bacteriol. 181:5090-5093.
5. Brandtzaeg, P., S. T. Gjeruldsen, F. Korsrud, K. Baklien, P. Berdal, and J. Ek. 1979. The human secretory immune system shows striking heterogeneity with regard to involvement of J chain-positive IgD immunocytes. J. Immunol. 122:503-510.
6. Brendel, V., P. Bucher, I. Nourbakhsh, B. E. Blaisdell, and S. Karlin. 1992. Methods and algorithms for statistical analysis of protein sequences. Proc. Natl. Acad. Sci. USA 89:2002-2006.
7. Calvert, J. E., and A. Calogeres. 1986. Characteristics of human B cells responsive to the T-independent mitogen Branhamella catarrhalis. Immunology 58:37-41.
8. Campagnari, A. A., T. F. Ducey, and C. A. Rebmann. 1996. Outer membrane protein B1, an iron-repressible protein conserved in the outer membrane of Moraxella (Branhamella) catarrhalis, binds human transferrin. Infect. Immun. 64:3920-3924.
9. Catlin, B. W. 1990. Branhamella catarrhalis: an organism gaining respect as a pathogen. Clin. Microbiol. Rev. 3:293-320.
10. Chen, C. J., C. Elkins, and P. F. Sparling. 1998. Phase variation of hemoglobin utilization in Neisseria gonorrhoeae. Infect. Immun. 66:987-993.
11. Chen, D., V. Barniak, K. R. VanDerMeid, and J. C. McMichael. 1999. The levels and bactericidal capacity of antibodies directed against the UspA1 and UspA2 outer membrane proteins of Moraxella (Branhamella) catarrhalis in adults and children. Infect. Immun. 67:1310-1316.
12. Christensen, J. J., J. Ursing, and B. Bruun. 1994. Genotypic and phenotypic relatedness of 80 strains of Branhamella catarrhalis of worldwide origin. FEMS Microbiol. Lett. 119:155-159.
13. 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.
14. Forsgren, A., M. Brant, A. Möllenkvist, A. Muyombwe, H. Janson, N. Woin, and K. Riesbeck. 2001. Isolation and characterization of a novel IgD-binding protein from Moraxella catarrhalis. J. Immunol. 167:2112-2120.
15. Forsgren, A., and A. Grubb. 1979. Many bacterial species bind human IgD. J. Immunol. 122:1468-1472.
16. Forsgren, A., A. Penta, S. F. Schlossman, and T. F. Tedder. 1988. Branhamella catarrhalis activates human B lymphocytes following interactions with surface IgD and class I major histocompatibility complex antigens. Cell. Immunol. 112:78-88.
17. Forsgren, A., and J. Sjöqvist. 1966. Protein A from Staphylococcus aureus. Pseudo-immune reaction with human gamma-globulin. J. Immunol. 97:822-827.
18. Frick, I. M., M. Wikström, S. Forsen, T. Drakenberg, H. Gomi, U. Sjöbring, and L. Björck. 1992. Convergent evolution among immunoglobulin G-binding bacterial proteins. Proc. Natl. Acad. Sci. USA 89:8532-8536.
19. Gjörloff Wingren, A., R. Hadzic, A. Forsgren, and K. Riesbeck. 2002. A novel IgD-binding bacterial protein from Moraxella catarrhalis induces human B lymphocyte activation and isotype switching in the presence of Th2 cytokines. J. Immunol. 168:5582-5588.
20. Helminen, M. E., I. Maciver, M. Paris, J. L. Latimer, S. L. Lumbley, L. D. Cope, G. H. McCracken, Jr., and E. J. Hansen. 1993. A mutation affecting expression of a major outer membrane protein of Moraxella catarrhalis alters serum resistance and survival in vivo. J. Infect. Dis. 168:1194-1201.
21. Helminen, M. E., I. Maciver, J. L. Latimer, J. Klesney-Tait, L. D. Cope, M. Paris, G. H. McCracken, Jr., and E. J. Hansen. 1994. A large, antigenically conserved protein on the surface of Moraxella catarrhalis is a target for protective antibodies. J. Infect. Dis. 170:867-872.
22. Henderson, I. R., F. Navarro-Garcia, and J. P. Nataro. 1998. The great escape: structure and function of the autotransporter proteins. Trends Microbiol. 6:370-378.
23. Henderson, I. R., P. Owen, and J. P. Nataro. 1999. Molecular switches-the ON and OFF of bacterial phase variation. Mol. Microbiol. 33:919-932.
24. Hoiczyk, E., A. Roggenkamp, M. Reichenbecher, A. Lupas, and J. Heesemann. 2000. Structure and sequence analysis of Yersinia YadA and Moraxella UspAs reveal a novel class of adhesins. EMBO J. 19:5989-5999.
25. Janson, H., B. Carlén, A. Cervin, A. Forsgren, A. Björk-Magnusdottir, S. Lindberg, and T. Runer. 1999. Effects on the ciliated epithelium of protein D-producing and -nonproducing nontypeable Haemophilus influenzae in nasopharyngeal tissue cultures. J. Infect. Dis. 180:737-746.
26. Karalus, R., and A. Campagnari. 2000. Moraxella catarrhalis: a review of an important human mucosal pathogen. Microbes Infect. 2:547-559.
27. Klingman, K. L., and T. F. Murphy. 1994. Purification and characterization of a high-molecular-weight outer membrane protein of Moraxella (Branhamella) catarrhalis. Infect. Immun. 62:1150-1155.
28. Kyd, J. M., A. W. Cripps, and T. F. Murphy. 1998. Outer-membrane antigen expression by Moraxella (Branhamella) catarrhalis influences pulmonary clearance. J. Med. Microbiol. 47:159-168.
29. 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.
30. Lafontaine, E. R., N. J. Wagner, and E. J. Hansen. 2001. Expression of the Moraxella catarrhalis UspA1 protein undergoes phase variation and is regulated at the transcriptional level. J. Bacteriol. 183:1540-1551.
31. Lewis, L. A., M. Gipson, K. Hartman, T. Ownbey, J. Vaughn, and D. W. Dyer. 1999. Phase variation of HpuAB and HmbR, two distinct haemoglobin receptors of Neisseria meningitidis DNM2. Mol. Microbiol. 32:977-989.
32. Lupas, A., M. Van Dyke, and J. Stock. 1991. Predicting coiled coils from protein sequences. Science 252:1162-1164.
33. McMichael, J. C. 2000. Vaccines for Moraxella catarrhalis. Vaccine 8(Suppl. 1):S101-S107.
34. Mhlanga-Mutangadura, T., G. Morlin, A. L. Smith, A. Eisenstark, and M. Golomb. 1998. Evolution of the major pilus gene cluster of Haemophilus influenzae. J. Bacteriol. 180:4693-4703.
35. Mol, O., and B. Oudega. 1996. Molecular and structural aspects of fimbriae biosynthesis and assembly in Escherichia coli. FEMS Microbiol. Rev. 19:25-52.
36. Murphy, T. F., C. Kirkham, and A. J. Lesse. 1993. The major heat-modifiable outer membrane protein CD is highly conserved among strains of Branhamella catarrhalis. Mol. Microbiol. 10:87-97.
37. Murphy, T. F., J. M. Kyd, A. John, C. Kirkham, and A. W. Cripps. 1998. Enhancement of pulmonary clearance of Moraxella (Branhamella) catarrhalis following immunization with outer membrane protein CD in a mouse model. J. Infect. Dis. 178:1667-1675.
38. Myers, L. E., Y. P. Yang, R. P. Du, Q. Wang, R. E. Harkness, A. B. Schryvers, M. H. Klein, and S. M. Loosmore. 1998. The transferrin binding protein B of Moraxella catarrhalis elicits bactericidal antibodies and is a potential vaccine antigen. Infect. Immun. 66:4183-4192.
39. Needleman, S. B., and C. D. Wunsch. 1970. A general method applicable to the search for similarities in the amino acid sequence of two proteins. J. Mol. Biol. 48:443-453.
40. Nielsen, H., J. Engelbrecht, S. Brunak, and G. von Heijne. 1997. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 10:1-6.
41. Nordström, T., A. Forsgren, and K. Riesbeck. 2002. The immunoglobulin D-binding part of the outer membrane protein MID from Moraxella catarrhalis comprises 238 amino acids and a tetrameric structure. J. Biol. Chem. 277:34692-34699.
42. 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.
43. Reddy, M. S., T. F. Murphy, H. S. Faden, and J. M. Bernstein. 1997. Middle ear mucin glycoprotein: purification and interaction with nontypable Haemophilus influenzae and Moraxella catarrhalis. Otolaryngol. Head Neck Surg. 116:175-180.
44. Rice, P., I. Longden, and A. Bleasby. 2000. "EMBOSS: The European Molecular Biology Open Software Suite." Trends Genet. 16:276-277.
45. Sarkari, J., N. Pandit, E. R. Moxon, and M. Achtman. 1994. Variable expression of the Opc outer membrane protein in Neisseria meningitidis is caused by size variation of a promoter containing poly-cytidine. Mol. Microbiol. 13:207-217.
46. Sasaki, K., R. E. Harkness, and M. H. Klein. September 1998. Nucleic acids encoding high molecular weight major outer membrane protein of Moraxella. U.S. patent 5808024.
47. Sasaki, K., and R. S. Munson, Jr. 1993. Protein D of Haemophilus influenzae is not a universal immunoglobulin D-binding protein. Infect. Immun. 61: 3026-3031.
48. Sørensen, C. H., and P. L. Larsen. 1988. IgD in nasopharyngeal secretions and tonsils from otitis-prone children. Clin. Exp. Immunol. 73:149-154.
49. Versalovic, J., T. Koeuth, and J. R. Lupski. 1991. Distribution of repetitive DNA sequences in eubacteria and application to fingerprinting of bacterial genomes. Nucleic Acids Res. 25:6823-6831.
50. Widders, P. R., L. A. Dorrance, M. Yarnell, and L. B. Corbeil. 1989. Immunoglobulin-binding activity among pathogenic and carrier isolates of Haemophilus somnus. Infect. Immun. 57:639-642.
51. Wolf, B., M. Kools-Sijmons, C. Verduin, L. C. Rey, A. Gama, J. Roord, J. Verhoef, and A. van Belkum. 2000. Genetic diversity among strains of Moraxella catarrhalis cultured from the nasopharynx of young and healthy Brazilian, Angolan, and Dutch children. Eur. J. Clin. Microbiol. Infect. Dis. 19: 759-764.
52. Yarnall, M., P. R. Widders, and L. B. Corbeil. 1988. Isolation and characterization of Fc receptors from Haemophilus somnus. Scand. J. Immunol. 28:129-137.
53. Yu, R. H., R. A. Bonnah, S. Ainsworth, and A. B. Schryvers. 1999. Analysis of the immunological responses to transferrin and lactoferrin receptor proteins from Moraxella catarrhalis. Infect. Immun. 67:3793-3799.
54. Zhang, L., K. Jacobsson, J. Vasi, M. Lindberg, and L. Frykberg. 1998. A second IgG-binding protein in Staphylococcus aureus. Microbiology 144:985-991.