Critical determinants of host receptor targeting by Neisseria meningitidis and Neisseria gonorrhoeae: Identification of Opa adhesiotopes on the N-domain of CD66 molecules

Molecular Microbiology

Volumn 34, Issue 3, 1999, Pages 538-551

  Virji, Mumtaz ^a   Evans, Debbie ^a   Hadfield, Andrea ^a   Grunert, Fritz ^b   Telxeira, Ana M ^c   Watt, Suzanne M ^c  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b UNIVERSITY OF FREIBURG   (Germany)

^c NONE

Author keywords

[No Author keywords available]

Indexed keywords

CARCINOEMBRYONIC ANTIGEN; CELL ADHESION MOLECULE; CELL RECEPTOR; COMPLEMENTARY DNA; GLYCOPROTEIN; ISOLEUCINE; MONOCLONAL ANTIBODY; MUTANT PROTEIN; OUTER MEMBRANE PROTEIN; TYROSINE;

AMINO ACID SUBSTITUTION; ARTICLE; BACTERIUM ADHERENCE; CONTROLLED STUDY; DNA TRANSFECTION; HELA CELL; HUMAN; HUMAN CELL; MOLECULAR MODEL; NEISSERIA GONORRHOEAE; NEISSERIA MENINGITIDIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION;

AMINO ACID SEQUENCE; ANTIGENS, BACTERIAL; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION; BACTERIAL ADHESION; BACTERIAL OUTER MEMBRANE PROTEINS; BINDING SITES; CELL ADHESION MOLECULES; HEPARAN SULFATE PROTEOGLYCANS; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; NEISSERIA GONORRHOEAE; NEISSERIA MENINGITIDIS; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, CELL SURFACE; TUMOR CELLS, CULTURED;

ANIMALIA; BACTERIA (MICROORGANISMS); NEGIBACTERIA; NEISSERIA GONORRHOEAE; NEISSERIA MENINGITIDIS;

EID: 0032752835     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1999.01620.x     Document Type: Article

References (68)

1. Achtman, M. (1995) Epidemic spread and antigenic variability of Neisseria meningitidis. Trends Microbiol 3: 186-192.
2. Aho, E.L., Dempsey, J.A., Hobbs, M.M., Klapper, D.G., and Cannon, J.G. (1991) Characterization of the Opa (class-5) gene family of Neisseria meningitidis. Mol Microbiol 5: 1429-1437.
3. Bates, P.A., Luo, J., and Sternberg, M.J. (1992) A predicted three-dimensional structure for the carcinoembryonic antigen (CEA). FEBS Lett 301: 207-214.
4. Beauchemin, N., Benchimol, S., Cournoyer, D., Fuks, A., and Stanners, C.P. (1987) Isolation and characterization of full-length functional cDNA clones for human carcinoembryonic antigen. Mol Cell Biol 7: 3221-3230.
5. Beauchemin, N. et al. (1999) New nomenclature for the CEA gene family. Exp Cell Res 252: in press.
6. Berling, B., Kolbinger, F., Grunert, F., Thompson, J.A., Brombacher, F., Buchegger, F., et al. (1990) Cloning of a carcinoembryonic antigen gene family member expressed in leukocytes of chronic myeloid leukemia patients and bone marrow. Cancer Res 50: 6534-6539.
7. Bhat, K.S., Gibbs, C.P., Barrera, O., Morrison, S.G., Jahnig, F., Stern, A., et al. (1991) The opacity proteins of Neisseria gonorrhoeae strain MS11 are encoded by a family of 11 complete genes. Mol Microbiol 5: 1889-1901.
8. Bodian, D.L., Jones, E.Y., Harlos, K., Stuart, D.I., and Davis, S.J. (1994) Crystal structure of the extracellular region of the human cell adhesion molecule CD2 at 2.5 Å resolution. Structure 2: 755-766.
9. Bos, M.P., Grunert, F., and Belland, R.J. (1997) Differential recognition of members of the carcinoembryonic antigen family by Opa variants of Neisseria gonorrhoeae. Infect Immun 65: 2353-2361.
10. Bos, M.P., Kuroki, M., Krop-Watorek, A., Hogan, D., and Belland, R.J. (1998) CD66 receptor specificity exhibited by neisserial Opa variants is controlled by protein determinants in CD66 N-domains. Proc Natl Acad Sci USA 95: 9584-9589.
11. Cartwright, K.A., Stuart, J.M., Jones, D.M., and Noah, N.D. (1987) The Stonehouse survey: nasopharyngeal carriage of meningococci and Neisseria lactamica. Epidemiol Infect 99: 591-601.
12. Chen, T., and Gotschlich, E.C. (1996) CGM1a antigen of neutrophils, a receptor of gonococcal opacity proteins. Proc Natl Acad Sci USA 93: 14851-14856.
13. Chen, T., Belland, R.J., Wilson, J., and Swanson, J. (1995) Adherence of pilus- Opa+ gonococci to epithelial cells in vitro involves heparan sulfate. J Exp Med 182: 511-517.
14. Chen, T., Grunert, F., Medina-Marino, A., and Gotschlich, E.C. (1997) Several carcinoembryonic antigens (CD66) serve as receptors for gonococcal opacity proteins. J Exp Med 185: 1557-1564.
15. Chothia, C., Gelfand, I., and Kister, A. (1998) Structural determinants in the sequences of immunoglobulin variable domain. J Mol Biol 278: 457-479.
16. Connell, T.D., Black, W.J., Kawula, T.H., Barritt, D.S., Dempsey, J.A., Kverneland, K., et al. (1988) Recombination among protein II genes of Neisseria gonorrhoeae generates new coding sequences and increases structural variability in the protein II family. Mol Microbiol 2: 227-236.
17. Connell, T.D., Shaffer, D., and Cannon, J.G. (1990) Characterization of the repertoire of hypervariable regions in the protein II (opa) gene family of Neisseria gonorrhoeae. Mol Microbiol 4: 439-449.
18. Daniel, S., Nagel, G., Johnson, J.P., Lobo, F.M., Hirn, M., Jantscheff, P., et al. (1993) Determination of the specificities of monoclonal antibodies recognizing members of the CEA family using a panel of transfectants. Int J Cancer 55: 303-310.
19. Duensing, T.D., and van Putten, J.P.M. (1997) Vitronectin mediates internalization of Neisseria gonorrhoeae by Chinese hamster ovary cells. Infect Immun 65: 964-970.
20. Epp, O., Lattman, E.E., Schiffer, M., Huber, R., and Palm, W. (1975) The molecular structure of a dimer composed of the variable portions of the Bence-Jones protein REI refined at 2 Å resolution. Biochemistry 14: 4943-4952.
21. Gallagher, J.T., Lyon, M., and Steward, W.P. (1986) Structure and function of heparan sulphate proteoglycans. Biochem J 236: 313-325.
22. Grant, C.C., Bos, M.P., and Belland, R.J. (1999) Proteoglycan receptor binding by Neisseria gonorrhoeae MS11 is determined by the HV-1 region of OpaA. Mol Microbiol 32: 233-242.
23. Gray-Owen, S.D., Lorenzen, D.R., Haude, A., Meyer, T.F., and Dehio, C. (1997) Differential Opa specificities for CD66 receptors influence tissue interactions and cellular response to Neisseria gonorrhoeae. Mol Microbiol 26: 971-980.
24. Hitchcock, P.J. (1989) Unified nomenclature for pathogenic Neisseria species. Clin Microbiol Rev 2: S64-S65.
25. Hobbs, M.M., Seiler, A., Achtman, M., and Cannon, J.G. (1994) Microevolution within a clonal population of pathogenic bacteria - recombination, gene duplication and horizontal genetic exchange in the opa gene family of Neisseria meningitidis. Mol Microbiol 12: 171-180.
26. Hobbs, M.M., Malorny, B., Prasad, P., Morelli, G., Kusecek, B., Heckels, J.E., et al. (1998) Recombinational reassortment among Opa genes from ET-37 complex Neisseria meningitidis isolates of diverse geographical origins. Microbiology 144: 157-166.
27. Jackson, R.L., Busch, S.J., and Cardin, A.D. (1991) Glycosaminoglycans: molecular properties, protein interactions, and role in physiological processes. Physiol Rev 71: 481-539.
28. Jerse, A.E., Cohen, M.S., Drown, P.M., Whicker, L.G., Isbey, S.F., Seifert, H.S., and Cannon, J.G. (1994) Multiple gonococcal opacity proteins are expressed during experimental urethral infection in the male. J Exp Med 179: 911-920.
29. Jones, T.A., Zou, J.Y., Cowan, S.W., and Kjeldgaard (1991) Improved methods for binding protein models in electron density maps and the location of errors in these models. Acta Crystallogr A 47: 110-119.
30. Jonsson, A.B., Nyberg, G., and Normark, S. (1991) Phase variation of gonococcal pili by frameshift mutation in pilC, a novel gene for pilus assembly. EMBO J 10; 477-488.
31. King, G.J., and Swanson, J. (1978) Studies on gonococcus infection. XV. Identification of surface proteins of Neisseria gonorrhoeae correlated with leukocyte association. Infect Immun 21: 575-584.
32. Klein, N.J., Ison, C.A., Peakman, M., Levin, M., Hammerschmidt, S., Frosch, M., and Heyderman, R.S. (1996) The influence of capsulation and lipooligosaccharide structure on neutrophil adhesion, molecule expression and endothelial injury by Neisseria meningitidis. J Infect Dis 173: 172-179.
33. Koumare, B., Achtman, M., Cisse, M., Wang, J.F., Giovanna, M., and Doumbia, T. (1995) Antigenic study of 337 strains of Neisseria meningitidis isolated in Mali - epidemlologic and vaccinal interest. Med Mal Infect 25: 1132-1136.
34. Majuri, M.L., Hakkarainen, M., Paavonen, T., and Renkonen, R. (1994) Carcinoembryonic antigen is expressed on endothelial cells. A putative mediator of tumor cell extravasation and metastasis. APMIS 102: 432-438.
35. Malorny, B., Morelli, G., Kusecek, B., Kolberg, J., and Achtman, M. (1998) Sequence diversity, predicted two-dimensional protein structure, and epitope mapping of neisserial Opa proteins. J Bacteriol 180: 1323-1330.
36. Mcbride, H.M., Lambden, P.R., Heckels, J.E., and Watt, P.J. (1981) The role of outer-membrane proteins in the survival of Neisseria gonorrhoeae P9 within guinea pig subcutaneous chambers. J Gen Microbiol 126: 63-67.
37. McNeil, G., and Virji, M. (1997) Phenotypic variants of meningococci and their potential in phagocytic interactions: the influence of opacity proteins, pili, PilC and surface sialic acids. Microb Pathog 22: 295-304.
38. McNeil, G., Virji, M., and Moxon, E.R. (1994) Interactions of Neisseria meningitidis with human monocytes. Microb Pathog 16: 153-163.
39. Nagel, G., Grunert, F., Kuijpers, T.W., Watt, S.M., Thompson, J., and Zimmermann, W. (1993) Genomic organization, splice variants and expression of CGM1, a CD66-related member of the carcinoembryonic antigen gene family. Eur J Biochem 214: 27-35.
40. Pinner, R.W., Spellman, P.A., and Stephens, D.S. (1991) Evidence for functionally distinct pili expressed by Neisseria meningitidis. Infect Immun 59: 3169-3175.
41. Prall, F., Nollau, P., Neumaier, M., Haubeck, H.D., Drzeniek, Z., Helmchen, U., et al. (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.
42. van Putten, J.P.M., and Paul, S.M. (1995) Binding of syndecan-like cell-surface proteoglycan receptors is required for Neisseria gonorrhoeae entry into human mucosal cells. EMBO J 14: 2144-2154.
43. van Putten, J.P.M., Hayes, S.F., and Duensing, T.D. (1997) Natural proteoglycan receptor analogs determine the dynamics of Opa adhesin-mediated gonococcal infection of Chang epithelial cells. Infect Immun 65: 5028-5034.
44. Ramachandran, G.N., Ramakrishnan, C., and Sasisekharan, V. (1963) Stereochemistry of polypeptide chain conformations. J Mol Biol 7: 95-99.
45. Rest, R.F., and Shafer, W.M. (1989) Interactions of Neisseria gonorrhoeae with human neutrophils. Clin Microbiol Rev 2: S83-S91.
46. Rostand, K.S., and Esko, J.D. (1997) Microbial adherence to and invasion through proteoglycans. Infect Immun 65: 1-8.
47. Skubitz, K.M., Micklem, K., and van der Schoot, C.E. (1995) Leukocyte Typing. V. Schlossman, S.E. (ed.). Oxford: Oxford University Press, pp. 889-899.
48. Stanners, C.P., DeMarte, L., Rojas, M., Gold, P., and Fuks, A. (1995) Opposite functions for 2 classes of genes of the human carcinoembryonic antigen family. Tumor Biol 16: 23-31.
49. Stern, A., Brown, M., Nickel, P., and Meyer, T.F. (1986) Opacity genes in Neisseria gonorrhoeae - control of phase and antigenic variation. Cell 47: 61-71.
50. Swanson, J., Barrera, O., Sola, J., and Boslego, J. (1988) Expression of outer membrane protein II by gonococci in experimental gonorrhea. J Exp Med 168: 2121-2129.
51. Tanaka, Y., Adams, D.H., and Shaw, S. (1993) Proteoglycans on endothelial cells present adhesion-inducing cytokines to leukocytes. Immunol Today 14: 111-115.
52. Teixeira, A.M., Fawcett, J., Simmons, D.L., and Watt, S.M. (1994) The N-domain of the biliary glycoprotein (BGP) adhesion molecule mediates homotypic binding - domain interactions and epitope analysis of BGPc. Blood 84: 211-219.
53. Virji, M., and Everson, J.S. (1981) Comparative virulence of opacity variants of Neisseria gonorrhoeae strain P9. Infect Immun 31: 965-970.
54. Virji, M., Kayhty, H., Ferguson, D.J.P., Alexandrescu, C., Heckels, J.E., and Moxon, E.R. (1991) The role of pili in the interactions of pathogenic Neisseria with cultured human endothelial cells. Mol Microbiol 5: 1831-1841.
55. Virji, M., Makepeace, K., Ferguson, D.J.P., Achtman, M., Sarkari, J., and Moxon, E.R. (1992) Expression of the Opc protein correlates with invasion of epithelial and endothelial cells by Neisseria meningitidis. Mol Microbiol 6: 2785-2795.
56. Virji, M., Makepeace, K., Ferguson, D.J.P., Achtman, M., and Moxon, E.R. (1993) Meningococcal Opa and Opc proteins - their role in colonization and invasion of human epithelial and endothelial cells. Mol Microbiol 10: 499-510.
57. Virji, M., Makepeace, K., and Moxon, E.R. (1994) Distinct mechanisms of interactions of Opc-expressing meningococci at apical and basolateral surfaces of human endothelial cells: the role of integrins in apical interactions. Mol Microbiol 14: 173-184.
58. Virji, M., Makepeace, K., Peak, I.R.A., Ferguson, D.J.P., Jennings, M.P., and Moxon, E.R. (1995) Opc- and pilus-dependent interactions of meningococci with human endothelial cells: molecular mechanisms and modulation by surface polysaccharides. Mol Microbiol 18: 741-754.
59. Virji, M., Watt, S.M., Barker, S., Makepeace, K., and Doyonnas, R. (1996a) 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.
60. Virji, M., Makepeace, K., Ferguson, D.J.P., and Watt, S.M. (1996b) Carcinoembryonic antigens (CD66a) on epithelial cells and neutrophils are receptors for Opa proteins of pathogenic Neisseriae. Mol Microbiol 22: 941-950.
61. deVries, F.P., Cole, R., Dankert, J., Frosch, M., and Vanputten, J.P.M. (1998) Neisseria meningitidis producing the Opc adhesin binds epithelial cell proteoglycan receptors. Mol Microbiol 27: 1203-1212.
62. Wang, J.H., Yan, Y.W., Garrett, T.P., Liu, J.H., Rodgers, D.W., Garlick, R.L., et al. (1990) Atomic structure of a fragment of human CD4 containing two immunoglobulin-like domains. Nature 348: 411-418.
63. Watt, S.M., Salanewby, G., Hoang, T., Gilmore, D.J., Grunert, F., Nagel, G., et al. (1991) CD66 identifies a neutrophil-specific epitope within the hematopoietic system that is expressed by members of the carcinoembryonic antigen family of adhesion molecules. Blood 78: 63-74.
64. Watt, S.M., Williamson, J., Genevier, H., Fawcett, J., Simmons, D.L., Hatzfeld, A., et al. (1993) The heparin binding PECAM-1 adhesion molecule is expressed by CD34+ hematopoietic precursor cells with early myeloid and B-lymphoid cell phenotypes. Blood 82: 2649-2663.
65. Wessner, D.R., Shick, P.C., Lu, J.H., Cardellichio, C.B., Gagneten, S.E., Beauchemin, N., et al. (1998) Mutational analysis of the virus and monoclonal antibody binding sites in MHVR, the cellular receptor of the murine coronavirus mouse hepatitis virus strain A59. J Virol 72: 1941-1948.
66. Williams, J.M., Chen, G.C., Zhu, L., and Rest, R.F. (1998) Using the yeast two-hybrid system to identify human epithelial cell proteins that bind gonococcal Opa proteins: intracellular gonococci bind pyruvate kinase via their Opa proteins and require host pyruvate for growth. Mol Microbiol 27: 171-186.
67. Woods, J.P., and Cannon, J.G. (1990) Variation in expression of class-1 and class-5 outer-membrane proteins during nasopharyngeal carriage of Neisseria meningitidis. Infect Immun 58: 569-572.
68. Zak, K., Diaz, J.L., Jackson, D., and Heckels, J.E. (1984) Antigenic variation during infection with Neisseria gonorrhoeae - detection of antibodies to surface proteins in sera of patients with gonorrhea. J Infect Dis 149: 166-174.