Duplication and differential expression of hemagglutinin genes in Porphyromonas gingivalis

Oral Microbiology and Immunology

Volumn 11, Issue 2, 1996, Pages 65-78

  Lepine G ^b   Progulske Fox, A ^a,c  

^a UNIVERSITY OF FLORIDA COLLEGE OF DENTISTRY   (United States)

^b UNIVERSITY AT BUFFALO   (United States)

^c UNIVERSITY OF FLORIDA HEALTH   (United States)

Author keywords

Gene duplication; Hemagglutinin; Porphyromonas gingivalis

Indexed keywords

ADHESIN; BACTERIAL PROTEIN; HAGB PROTEIN, PORPHYROMONAS GINGIVALIS; HAGC PROTEIN, PORPHYROMONAS GINGIVALIS; HEMAGGLUTININ; HEMIN; LECTIN;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GENE; BIOSYNTHESIS; CULTURE MEDIUM; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MOLECULAR GENETICS; MULTIGENE FAMILY; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PORPHYROMONAS GINGIVALIS; SEQUENCE HOMOLOGY; VIRULENCE;

ADHESINS, BACTERIAL; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BASE SEQUENCE; CULTURE MEDIA; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; HEMAGGLUTININS; HEMIN; LECTINS; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PORPHYROMONAS GINGIVALIS; SEQUENCE HOMOLOGY, NUCLEIC ACID; TRANSCRIPTION, GENETIC; VIRULENCE;

EID: 0030131180     PISSN: 09020055     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1399-302X.1996.tb00339.x     Document Type: Article

References (70)

1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. A basic local alignment search tool. J Mol Biol 1990: 215: 403-410.
2. Applied Biosystems. High-quality template DNA for Tag cycle sequencing using dyedeoxy terminators: an improved preparation procedure. User Bull 1991; 18. 1-4
3. Ausubel FM, Brent R, Kingston RE, et al. Preparation and analysis of DNA. In: Janssen K, ed. Current protocols in molecular biology. New York: Greene Publishing Associates and Wiley-Interscience. 1987: 2.0.1-2.13.3.
4. Birnstiel M, Telford J, Weinberg E, Stafford D. Isolation and some properties of the genes coding histone proteins. Proc Natl Acad Sci USA 1974: 71: 2900-2904.
5. Boyd J, McBride BC. Fractionation of hemagglutinating and bacterial binding adhesins of Bacteroides gingivalis. Infect Immun 1984: 45: 403-409.
6. Bramanti TE, Holt SC. Iron-regulated outer membrane proteins in the periodontopathic bacterium, Bacteroides gingivalis. Biochem Biophys Res Commun 1990: 166: 1146-1154.
7. Bramanti TE, Holt SC. Roles of porphyrins and host iron transport proteins in regulation of growth of Porphyromonas gingivalis W50. J Bacteriol 1991: 173: 7330-7339.
8. Burnette WN. "Western blotting": electrophoretic transfer of proteins from sodium-dodecyl sulfate-polyacrylamide gels to radiographic detection with antibody and radioiodinated protein A. Anal Biochem 1981: 112: 195-203.
9. Carlsson J, Höfling JF, Sundqvist GK. Degradation of albumin, haemopexin, haptoglobin and traasferrin, by black-pigmented Bacteroides species. J Med Microbiol 1984: 18. 39-46.
10. Carman RJ, Ramakrishnan MD, Harper FH. Hemin levels in culture medium of Porphyromonas (Bacteroides) gingivalis regulate both hemin binding and trypsinlike protease production. Infect Immun 1990: 58: 4016-4019.
11. Chandad F, Mouton C. Molecular size variation of the hemagglutinating adhesin HA-Ag2, a common antigen of Bacteroides gingivalis. Can J Microbiol 1990: 36: 690-696.
12. Cimansoni G, Song M, McBride BC. Effect of crevicular fluid and lysosomal enzymes on the adherence of streptococci and Bacteroides to hydroxyapatite. Infect Immun 1987: 55: 1484-1489.
13. Devereux J, Haeberli P, Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 1984: 12: 387-395.
14. Dickinson DP, Kubinec MA, Yoshimura F, Genco RJ Molecular cloning and sequencing of the gene encoding the fimbrial subunit protein of Bacteroides gingivalis. J Bacteriol 1988: 170: 1658-1665.
15. Duerden BI. Pigment production by Bacteroides species with reference to sub-classification. J Med Microbiol 1975. 8: 113-125.
16. Dusek DM, Progulske-Fox A, Whitlock J, Brown TA. Isolation and characterization of a cloned Porphyromonas gingivalis hemagglutinin from an avirulent strain of Salmonella typhimurium. Infect Immun 1993: 61; 940-946.
17. Gibbons RJ, Macdonald JB. Hemin and vitamin K compounds as required factors for the cultivation of certain strains of Bacteroides melaninogenicus. J Bacteriol 1960. 80: 164-170.
18. Grenier D, Mayrand D. Etudes d'infections mixtes anaérobies comportant Bacteroides gingivalis. Can J Microbiol 1983: 29: 612-618.
19. Grenier D, Mayrand D. Nutritional relationships between oral bacteria. Infect Immun 1986: 53: 616-620.
20. Haapasalo M, Shah H, Gharbia S, Seddon S, Lounatmaa K. Surface properties and ultrastructure of Porphyromonas gingivalis W50 and pleiotropic mutants. Scand J Dent Res 1989; 97: 355-360.
21. Hayashi H, Nagata A, Hinode D, Sato M, Nakamura R. Survey of a receptor protein in human erythrocytes for hemagglutinin of Porphyromonas gingivalis. Oral Microbiol Immunol 1992: 7: 204-211.
22. Hobbs MM, Seiler A, Achtman M, Cannon JG. 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 1994: 12: 171-180.
23. Inoshita E, Amano A, Hanioka T, Tamagawa H, Shizukuishi S, Tsunemitsu A. Isolation and some properties of exohemagglutinin from the culture medium of Bacteroides gingivalis. Infect Immun 1986: 57: 421-427.
24. Isogai H, Isogai E, Yoshimura F, Suzuki T, Kagota W, Takano K. Specific inhibition of adherence of an oral strain of P. gingivalis 381 to epithelial cells by monoclonal antibodies against the bacterial fimbriae. Arch Oral Biol 1988: 33: 479-485.
25. Iwabe N, Kuma KI, Hasegawa M, Osawa S, Miyata T. Evolutionary relationship of archaebacteria, eubacteria, and eukaryotes inferred from phylogenetic trees of duplicated genes. Proc Natl Acad Sci U S A 1989: 86: 9355-9359.
26. Kinoshita T, Imamura J, Nagai H, Shimotohno K. Quantification of gene expression over a wide range by the polymerase chain reaction. Anal Biochem 1992: 206: 231-235.
27. Kolenbrander PE. Surface recognition among oral bacteria: multigeneric coaggregations and their mediators. Crit Rev Microbiol 1988: 17; 137-159.
28. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970: 227. 680-685.
29. Lantz MS, Allen RD, Bounelis P, Switalski LM, Hook M. Bacteroides gingivalis and Bacteroides intermedius recognize different sites on human fibrinogen. J Bacteriol 1990: 172; 716-726.
30. Lee JJ, Smith HO, Redfield RJ. Organization of the Haemophilus influenzae Rd genome. J Bacteriol 1989: 171: 3016-3024.
31. Lépine G, Savett DA, Progulske-Fox A. Restriction fragment length polymorphism analysis of two hemagglulinin loci, serotyping and agglutinating activity of Porphyromonas gingivalis. Oral Microbiol Immunol 1995: 10: 1-7.
32. Lépine G, Whitlock JA, Progulske-Fox A. Cloning and characterization of a fourth putative hemagglutinin gene from P. gingivalis. Abstr 94th Annu Meet Am Soc Microbiol 1994: abstr D117.
33. Lydyard P, Grossi C. Cells involved in the immune response. In: Roitt I, Brostoff J, Male D, ed. Immunology. New York: Grower Medical Publishing, 1989: 2.1-2.18.
34. Maeda N, Smithies O. The evolution of multigene families: human haptoglobin genes. Annu Rev Genet 1986: 20: 81-108.
35. Mayrand D, Holt SC. Biology of asaccharolytic black-pigmented Bacteroides species. Microbiol Rev 1988: 52: 134-152.
36. Mayrand D, McBride BC. Ecological relationships of bacteria involved in a simple mixed anaerobic infection. Infect Immun 1980: 27: 44-50.
37. Mayrand D, McBride BC, Edwards T, Jensen S. Characterization of Bacteroides asaccharolyticus and B. melaninogenicus oral isolates. Can J Microbiol 1980: 26: 1178-1183.
38. McBride BC, Joe A, Singh U. Cloning of Bacteroides gingivalis surface antigens involved in adherence. Arch Oral Biol 1990: 35 (suppl): 59S-68S.
39. McKee AS, McDermid AS, Baskerville A, Dowsett AB, Ellwood DC, Marsh PD. Effect of hemin on the physiology and virulence of Bacteroides gingivalis W50. Infect Immun 1986: 52: 349-355.
40. Mouton C, Bouchard D, Deslauriers M, Lamonde L. Immunochemical identification and preliminary characterization of a nonfimbrial hemagglutinating adhesin of Bacteroides gingivalis. Infect Immun 1989: 57: 566-5873.
41. Mouton C, Ni Eidhin D, Deslauriers M, Lamy L. The hemagglutinating adhesin HA-Ag2 of Bacteroides gingivalis is distinct from the fimbrillin. Oral Microbiol Immunol 1991: 6: 6-11.
42. Nishibushi M, Kaper JB. Duplication and variation of the thermostable direct haemolysin (idh) gene in Vibrio parahaemolyticus. Mol Microbiol 1990: 4: 87-99.
43. Nishikata M, Yoshimura F. Characterization of Porphyromonas gingivalis hemagglutinin as a protease. Biochem Biophys Res Commun 1991: 178: 336-342.
44. Normark S, Båga M, Goransson M et al. Genetics and biogenesis of Escherichia coli adhesins. In: Mirelman D, ed. Microbial lectins and agglutinins. New York: Wiley, 1986: 113-143.
45. Ohno S. Evolution by gene duplication. New York: Springer-Verlag, 1970.
46. Okuda K, Slots J, Genco RJ. Bacteroides gingivalis, Bacteroides asaccharolyticus, and Bacteroides melaninogenicus subspecies: cell surface morphology and adherence to erythrocytes and human buccal epithelial cells. Curr Microbiol 1981. 6: 7-12.
47. Okuda K, Takazoe I. Hemagglutinating activity of Bacteroides melaninogenicus. Arch Oral Biol 1974: 19: 415-416.
48. Okuda K, Yamamoto A, Naito Y, Takazoe I, Slots J, Genco RJ. Purification and properties of hemagglutinin from culture supernatant of Bacteroides gingivalis. Infect Immun 1986: 54: 659-665.
49. Pannetier C, Delassus S, Darche S, Saucier C, Kourilsky P. Quantitative titration of nucleic acids by enzymatic amplification reactions run to saturation. Nucleic Acids Res 1993: 21: 577-583.
50. Progulske-Fox A, Tumwarson S, Holt SC. The expression and function of Bacteroides gingivalis hemagglutinin gene in Escherichia coli. Oral Microbiol Immunol 1989: 4: 121-131.
51. Progulske-Fox A, Tumwasorn S, Lépine G et al. The cloning, expression and sequence analysis of a second Porphyromonas gingivalis gene which codes for a protein involved in hemagglutination. Oral Microbiol Immunol 1995: 10: 311-318.
52. Rizza V, Sinclair PR, White DC, Cuorant PR. Electron transport system of the protoheme-requiring anaerobe Bacteroides melaninogenicus. J Bacteriol 1968: 96: 665-671.
53. Rosen KM, Villa-Komaroff L. An alternative method for the visualization of RNA in formaldehyde agarose gels. Focus 1990: 12: 23-24.
54. Sambrook J, Fritsch EF, Maniatis T. Molecular cloning. A laboratory manual. 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press. 1989.
55. Shah HN, Bonnett R, Mateen B, Williams RAD. The porphyrin pigmentation of subspecies of Bacteroides melaninogenicus. Biochem J 1979: 180: 45-50.
56. Silhavy TJ, Berman ML, Enquist LW. Experiments with gene fusions. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, 1984.
57. Slots J Subgingival microflora and periodontal disease. J Clin Periodontol 1979: 6: 351-382.
58. Slots J, Genco RJ. Black-pigmented Bacteroides species, Capnocytophaga species, and Actinobacillus actinomycetemcomitans in human periodontal disease: virulence factors in colonization, survival, and tissue destruction. J Dent Res 1984: 63: 412-421.
59. Slots J, Gibbons RJ. Attachment of Bacteroides melaninogenicus subsp. asaccharolyticus to oral surfaces and its possible role in colonization of the mouth and of periodontal pockets. Infect Immun 1978: 9: 254-264.
60. Slots J, Moenbo D, Langebaek J, Frandsen A. Microbiota of gingivitis in man. Scand J Dent Res 1978: 86: 174-181.
61. Smalley JW, Birss AJ. Trypsin-like enzyme activity of the extracellular membrane vesicles of Bacteroides gingivalis. J Gen Microbiol 1987: 133: 2883-2894.
62. Smalley JW, Birss AJ, Kay HM, McKee AS, Marsh PD. The distribution of trypsin-like enzyme activity in cultures of a virulent and an avirulent strain of Bacteroides gingivalis. Oral Microbiol Immunol 1989: 4: 178-181.
63. Smalley JW, Birss AJ, McKee AS, Marsh PD. Haemin-restriction influences haemin-binding, haemagglutination and protease activity of cells and extracellular membrane vesicles of Porphyromonas gingivalis W50. FEMS Microbiol Lett 1991: 90: 63-68.
64. Socransky SS, Tanner ACR, Haffajee AD, Hillman JD, Goodson JM. Present status of studies on the microbiological etiology of periodontal diseases. In: Genco RJ, Mergenhagen SE, ed. Host-parasite interactions in periodontal diseases. Washington, DC: Am Soc Microbiol. 1982: 1-12.
65. Takazoe I, Nakamura T, Okuda K. Colonization of the subgingival area by Bacteroides gingivalis. J Dent Res 1984: 63: 422-426.
66. Tanner ACR, Haffajee C, Bratthall RA, Visconti RA, Socransky SS. A study of the bacteria associated with advancing periodontitis in man. J Clin Periodontol 1979: 6: 278-307.
67. Whitlock J, Han N, Lantz MS. DNA sequences of a hemagglutinin gene (hagA) of P gingivalis. Abstr 93rd Annu Meet Am Soc Microbiol 1993: Abstr D120.
68. Wilson AC, Carlson SS, White TJ. Biochemical evolution. Annu Rev Biochem 1977: 46: 573-639.
69. Yoshimura F, Takashi K, Nodasaka Y, Suzuki T. Purification and characterization of a novel type of fimbriae from the oral anaerobe Bacteroides gingivalis. J Bacteriol 1984: 160: 949-957.
70. Zambon JJ. Microbiology of periodontal disease. In: Genco RJ, Goldman HJ, Cohen DW, ed. Contemporary periodontics. St. Louis, MO; Mosby, 1990: 147-160.