Members of the genus Actinomyces are predominant primary colonizers of the oral cavity and play an important role in initiating plaque development. These bacteria have evolved unique mechanisms that favor colonization and persistence in this micro-environment. The expression of cell-surface fimbriae is correlated with the ability of these bacteria to adhere to specific receptors on the tooth and mucosal surfaces, and to interact with other plaque bacteria. The elaboration of sialidase is thought to enhance fimbriae-mediated adherence by unmasking the fimbrial receptors on mammalian cells. The presence of certain cell-associated or extracellular enzymes, including those involved in sucrose or urea metabolism, may provide the means for these bacteria to thrive under conditions when other growth nutrients are not available. Moreover, these enzyme activities may influence the distribution of other plaque bacteria and promote selection for Actinomyces spp. in certain ecological niches. The recent development of a genetic transfer system for Actinomyces spp. has allowed for studies the results of which demonstrate the existence of multiple genes involved in fimbriae synthesis and function, and facilitated the construction of allelic replacement mutants at each gene locus. Analyses of these mutants have revealed a direct correlation between the synthesis of assembled fimbriae and the observed adherence properties. Further genetic analysis of the various enzyme activities detected from strains of Actinomyces should allow for an assessment of the role of these components in microbial ecology, and their contribution to the overall success of Actinomyces spp. as a primary colonizer and a key player in oral health and disease.
References
1.
Allen PZ, Bowen WH (1990). Immunochemical studies on levans from several strains of Actinomyces viscosus. Arch Oral Biol35:55-62.
2.
Barsotti O., Comby C., Morrier JJ, Benay G., Decoret D., Guniet R., et al. (1988). Improved SDS-PAGE method for protein profiles analysis of Actinomyces species. J Biol Buccale16:219-224.
3.
Barsotti O., Morrier JJ, Decoret D., Benay G., Rocca JP (1993). An investigation into the use of restriction endonuclease analysis for the study of transmission of Actinomyces. J Clin Periodontol20:436-442.
4.
Barsotti O., Decoret D., Benay G., Carlotti A., Freney J., Guerin-Faublee V., et al. (1994). rRNA gene restriction patterns as possible taxonomic tools for the genus Actinomyces. Zbl Blakt281:433-441.
5.
Beighton D., Whiley RA (1990). Sialidase activity of the "Streptococcus milleri group" and other viridans group streptococci. J Clin Microbiol28:1431-1433.
6.
Birkhed D., Rosell K-G., Granath K. (1979). Structure of extracellular water-soluble polysaccharides synthesized from sucrose by oral strains of Streptococcus mutans, Streptococcus salivarius, Streptococcus sanguis and Actinomyces viscosus. Arch Oral Biol24:53-61.
7.
Bowden G., Johnson J., Schachtele C. (1993). Characterization of Actinomyces with genomic DNA fingerprints and rRNA gene probes. J Dent Res72:1171-1179.
8.
Brennan MJ, Cisar JO, Vatter AE, Sandberg AL (1984). Lectin-dependent attachment of Actinomyces naeslundii to receptors on epithelial cells. Infect Immun46:459-464. Brennan MJ, Cisar IO, Sandberg AL (1986). A 160-kilodalton epithelial cell surface glycoprotein recognized by plant lectins that inhibit the adherence of Actinomyces naeslundii. Infect Immun52:840-845.
9.
Brander MA, Jousimies-Somer HR (1992). Evaluation of the RapID ANA II and API ZYM systems for identification of Actinomyces species from clinical specimens. J Clin Microbiol30:3112-3116.
10.
Burne RA, Schilling K., Bowen WH, Yasbin RE (1987). Expression, purification, and characterization of an exo-β-D-fructosidase of Streptococcus mutans. J Bacteriol169:4507-4517.
11.
Campbell AM (1962). Episomes. Adv Genet11:101-145. Celig DM, Schreckenberger PC ( 1991 ). Clinical evaluation of the RapID-ANA II panel for identification of anaerobic bacteria. J Clin Microbiol29:457-462.
12.
Chak W., Kuramitsu HK (1981). Effects of metabolic inhibitors on extracellular fructosyltransferase production in Actinomyces viscosus. Infect Immun34:930-937.
13.
Chen Y-Y M., Clancy KA, Burne RA (1996). Streptococcus salivarius urease: genetic and biochemical characterization and expression in a dental plaque streptococcus. Infect Immun64:585-592.
14.
Cisar JO (1986). Fimbrial lectins of the oral actinomyces. In: Microbial lectins and agglutinins: properties and biological activity. Mirelman D, editor. New York: John Wiley & Sons, pp. 183-196.
15.
Cisar JO, Barsumian EL, Curl SH, Vatter AE, Sandberg AL, Siraganian PR (1981). Detection and localization of a lectin on Actinomyces viscosus T14V by monoclonal antibodies. J Immunol127:1318-1322.
16.
Cisar JO, David VA, Curl SH, Vatter AE (1984). Exclusive presence of lactose-sensitive fimbriae on a typical strain (WVU45) of Actinomyces naeslundii. Infect lmmun46:453-458.
17.
Cisar JO, Vatter AE, Clark WB, Curl SH, Hurst-Calderone S., Sandberg AL (1988). Mutants of Actinomyces viscosus T14V lacking type 1, type 2 or both types of fimbriae. Infect lmmun56:2984-2989.
18.
Cisar JO, Barsumian EL, Siraganian RP, Clark WB, Yeung MK, Hsu SD, et al. (1991). Immunochemical and functional studies of Actinomyces viscosus T14V type 1 fimbriae with monoclonal and polyclonal antibodies directed against the fimbrial subunit. J Gen Microbiol137:1971-1979.
19.
Cisar JO, Sandberg AL, Abeygunawardana C., Reddy GP, Bush CA ( 1995). Lectin recognition of host-like saccharide motifs in streptococcal cell wall polysaccharides. Glycobiology5:655-662.
20.
Cisar JO, Takahashi Y., Ruhl S., Donkersloot JA, Sandberg AL (1997). Specific inhibitors of bacterial adhesion: observations from the study of Gram-positive bacteria that initiate biofilm formation on the tooth surface. Adv Dent Res11:168-175.
21.
Clark WB, Beem JE, Nesbitt WE, Cisar JO, Tseng CC, Levine MJ ( 1989). Pellicle receptors for Actinomyces viscosus type I fimbriae in vitro. Infect Immun57:3003-3008.
22.
Corfield AP, Schauer R. (1982). Sialic acid: chemistry, metabolism and function. Cell Biol Monogr10:195-261.
Costello AH, Cisar JO, Kolenbrander PE, Gabriel O. (1979). Neuraminidase-dependent hemagglutination of human erythrocytes by human strains of Actinomyces viscosus and Actinomyces naeslundii. Infect Immun26:563-572.
25.
Coykendall AL, Munzenmaier AJ (1979). Deoxyribonucleic acid hybridization among strains of Actinomyces viscosus and Actinomyces naeslundii. Int J Syst Bacteriol29:234-240.
26.
Davis G., Gibbons RJ (1990). Accessible sialic acid content of oral epithelial cells from healthy and gingivitis subjects. J Periodont Res25:250-253.
27.
Davison J., Heusterspreute M., Chevalier N., Ha-Thi V., Brunel F. (1987). Vectors with restriction site banks. V. p)RD215, a wide-host-range cosmid vector with multiple cloning sites. Gene51:275-280.
28.
de Graaf FK (1990). Genetics of adhesive fimbriae of intestinal Escherichia coli. Curr Top Microbiol Immunol151:29-53.
29.
Devereux J., Haeberli P., Smithies O. (1984). A comprehensive set of sequence analysis programs for VAX. Nucleic Acids Res12:387-396.
30.
Donkersloot JA, Cisar JO, Wax ME, Harr RJ, Chassy BM (1985). Expression of Actinomyces viscosus antigens in Escherichia coli: cloning of a structural gene (fimA) for type 2 fimbriae. J Bacteriol162:1075-1078.
31.
Ebisu S., Keijiro K., Kotani S., Misaka A. (1975). Structural differences in the fructans elaborated by Streptococcus mutans and Strep. salivarius. J Biochem78:879-887.
32.
Ellen RP, Fillery ED, Chan KH, Grove DA (1980). Sialidase-enhanced lectin-like mechanism for Actinomyces viscosus and Actinomyces naeslundii hemagglutination. Infect Immun27:335-343.
33.
Fillery ED, Bowden GH, Hardie JM (1978). A comparison of strains of bacteria designated Actinomyces viscosus and Actinomyces naeslundii. Caries Res12:299-312.
34.
Firtel M., Fillery ED (1988). Distribution of antigenic determinants between Actinomyces viscosus and Actinomyces naeslundii. J Dent Res67:15-20.
35.
Fives-Taylor PM, Macrina FL, Pritchard TJ, Peene SS (1987), Expression of Streptococcus sanguis antigens in Escherichia coli: cloning of a structural gene for adhesion fimbriae. Infect Immun55:123-128.
36.
Fox GE, Pechman KJ, Woese CR (1977). Comparative cataloging of 16S ribosomal ribonucleic acid: molecular approach to procaryotic systematics. Int J Syst Bacteriol27:44-57.
37.
Funke G., Stubbs S., von Graevenitz A., Collins MD (1994). Assignment of human-derived CDC group I coryneform bacteria and CDC group 1-like coryneform bacteria to the genus Actinomyces as Actinomyces neuii subsp. neuii spp. nov., subsp. nov., and Actinomyces neuii subsp. anitratus subsp. nov Int J Syst Bacteriol44:167-171.
38.
Gabriel O., Heeb MJ, Hinrichs M. (1985). Interaction of the surface adhesins of the oral Actinomyces spp. with mammalian cells. In: Molecular basis of oral microbial adhesion. Mergenhagen SE, Rosan B, editors. Washington, DC: American Society for Microbiology, pp. 45-52.
39.
Genco RJ, Loos BG ( 1991). The use of genomic DNA fingerprinting in studies of the epidemiology of bacteria in periodontitis. J Clin Periodontol18:396-405.
40.
Gerencser MJ (1979). The application of fluorescent antibody techniques to the identification of Actinomyces and Arachnia. In: Methods in microbiology. Vol. 13. Bergen T, Norris JR, editors. London: Academic Press Ltd., pp. 287-321.
41.
Gibbons R.) (1989). Bacterial adhesion to oral tissues: a model for infectious diseases. J Dent Res68:750-760.
42.
Gibbons RJ, Hay DI, Cisar JO, Clark WB (1988). Adsorbed salivary proline-rich protein 1 and statherin: receptors for type 1 fimbriae of Actinomyces viscosus T14V-J1 on apatitic surfaces. Infect Immun56:2990-2993.
43.
Goulbourne PA, Ellen RP (1991). Evidence that Porphyromonas (Bacteroides) gingivalis fimbriae function in adhesion to Actinomyces viscosus. J Bacteriol173:5266-5274.
44.
Grimaudo NJ, Nesbitt WE, Clark WB (1996). Coaggregation of Candida albicans with oral Actinomyces species. Oral Microbiol Immunol11:59-61.
45.
Guerin-Faublee V., Decoret D., Kodjo A., Tilly B., Carlotti A., Freney J., et al. (1994). Molecular typing of Actinomyces pyogenes isolates. Zbl Bakt281:174-182.
46.
Hacker J. (1990). Genetic determinants coding for fimbriae and adhesins of extraintestinal Escherichia coli. Curr Top Microbiol Immunol151:1-27.
47.
Handley PS, Carter PL, Wyatt JE, Hesketh LM (1985). Surface structures (peritrichous fibrils and tufts of fibrils) found on Streptococcus sanguis strains may be related to their ability to coaggregate with other oral genera. Infect Immun47:217-227.
48.
Haslam DB, Boren T., Falk P., liver D., Chou A., Xu Z., et al. (1994). The amino-terminal domain of the P-pilus adhesin determines receptor specificity. Mol Microbiol14:399-409.
49.
Henningsen M., Roggentin P., Schauer R. (1991). Cloning, sequencing and expression of the sialidase gene from Actinomyces viscosus DSM 43798. Biol Chem Hoppe-Seyler372:1065-1072.
50.
Hermans J., Martin C., Huijberts GNM, Goosen T., de Bont JAM (1991). Transformation of Mycobacterium aurum and Mycobacterium smegmatis with the broad-host-range Gram-negative cosmid vector pJRD215. Mol Microbiol5:1561-1566.
51.
Holmberg K., Forsum U. (1973). Identification of Actinomyces, Arachnia, Bacterionema, Rothia and Propionibacteria species by defined immunofluorescence. Appl Microbiol25:834-843.
52.
Holmberg K., Nord C.-E (1975). Numerical taxonomy and laboratory identification of Actinomyces and Arachnia and some related bacteria. J Gen Microbiol91:17-44.
53.
Hoyer LL, Hamilton AC, Steenbergen SM, Vimr ER ( 1992). Cloning, sequencing and distribution of the Salmonella typhimurium LT2 sialidase gene, nanH, provides evidence for interspecies gene transfer. Mol Microbiol6:873-884.
54.
Hsu SD, Cisar JO, Sandberg AL, Kilian M. (1994). Adhesive properties of viridans streptococcal species. Microb Ecol Health Dis7:125-137.
55.
Hultgren SJ, Jones CH, Normark S. (1996). Bacterial adhesins and their assembly. In: Escherichia coli and Salmonella. Cellular and molecular biology. Neidhardt FC, Curtiss R III, Ingraham JL, editors. Washington, DC: American Society for Microbiology, pp. 2730-2756.
56.
Igarashi T., Takahashi M., Yamamoto A., Etoh Y., Takamori K. (1987). Purification and characterization of levanase from Actinomyces viscosus ATCC 19246. Infect Immun55:3001-3005.
57.
Ikeda H., Tomizawa J-I. (1968). Prophage P1, an extrachromosomal replication unit. Cold Spring Harbor Symp Quant Biol33:791-798.
58.
Jacobs WR Jr, Kalpana GV, Cirillo JD, Pascopella L., Snapper SB, Udani RA, et al. (1991). Genetic systems for Mycobacteria. Meth Enzymol204:537-555.
59.
Jacques NA (1985). Inhibition of the expression of cell-associated fructosyltransferase in Streptococcus salivarius by octyl β-D-glucopyranoside. J Gen Microbiol131:3243-3250.
Johnson JL, Moore LVH, Kaneko B., Moore WEC (1990). Actinomyces georgiae sp. nov., Actinomyces gerencseriae sp. nov., designation of two genospecies of Actinomyces naeslundii, and inclusion of A. naeslundii serotypes II and III and Actinomyces viscosus serotype II in A. naeslundii genospecies 2. Int J Syst Bacteriol40:273-286.
62.
Kalfas S. (1987). Comparison of different methods for detection of urease activity in oral Actinomyces species. Oral Microbiol Immunol2:190-192.
63.
Kalfas S., Edwardsson S. (1990). Identification procedures for oral Actinomyces species. Oral Microbiol Immunol5:39-42.
64.
Kiser T., Hopwood DA (1991). Genetic manipulation of Streptomyces: integrating vectors and gene replacement. Meth Enzymol204:430-459.
65.
Kiyama M., Hiratsuka K., Saito S., Shiroza T., Takiguchi H., Abiko Y. (1996). Detection of Actinomyces species using nonradioactive riboprobes coupled with polymerase chain reaction. Biochem Mol Med58:151-155.
66.
Kolenbrander PE (1989). Intergeneric coaggregation among human oral bacteria and ecology of dental plaque. Ann Rev Microbiol42:627-656.
67.
Kuramitsu HK (1993). Virulence factors of mutans streptococci-role of molecular genetics. Crit Rev Oral Biol Med4:159-176.
68.
Lee KK, Sheth HB, Wong WY, Sherburne R., Paranchych W., Hodges RS, et al. (1994). The binding of Pseudomonas aeruginosa pili to glycosphingolipids is a tip-associated event involving the C-terminal region of the structural pilin subunit. Mol Microbiol11:705-713.
69.
Li J., Ellen RP, Hoover CI, Felton JR (1991). Association of proteases of Porphyromonas (Bacteroides) gingivalis with its adhesion to Actinomyces viscosus. J Dent Res70:82-86.
70.
Liljemark WF, Bloomquist CG, Fenner LJ, Antonelli PJ, Coulter MC (1989). Effect of neuraminidase on the adherence to salivary pellicle of Streptococcus sanguis and Streptococcus mitis. Caries Res23:141-145.
71.
Macrina FL, Dertzbaugh MT, Halula MC, Krah R. III, Jones KR (1990). Genetic approaches to the study of oral microflora: a review. Oral Biol Med1:207-227.
72.
Maiden MFJ, Tanner A., Macuch PJ (1996). Rapid characterization of periodontal bacterial isolates by using fluorogenic substrate tests. J Clin Microbiol34:376-384.
73.
Marsh PD, Martin MV (1992). Dental plaque. In: Oral microbiology. Marsh PD, Martin MV, editors. London: Chapman & Hall, pp. 98-132.
74.
Mattick JS, Whitchurch CB, Aim RA (1996). The molecular genetics of type-4 fimbriae in Pseudomonas aeruginosa-a review. Gene179:147-155.
75.
McCormick SS, Mengoli HF, Gerencser MA (1985). Polyacrylamide gel electrophoresis of whole-cell preparations of Actinomyces spp. Int J Syst Bacteriol35:429-433.
76.
Mclntire FC, Crosby LK, Vatter AE, Cisar JO, McNeil MR, Bush CA, et al. (1988). A polysaccharide from Streptococcus sanguis 34 that inhibits coaggregation of S. sanguis 34 with Actinomyces viscosus T14V. J Bacteriol170:2229-2235.
77.
Miller PH, Wiggs LS, Miller JM (1995). Evaluation of API An-IDENT and RapID ANA II systems for identification of Actinomyces species from clinical specimens. J Clin Microbiol33:329-330.
78.
Mobley HLT, Island MD, Hausinger RP (1995). Molecular biology of microbial ureases. Microbial Rev59:451-480.
79.
Moncla BJ, Braham P. (1989). Detection of sialidase (neuraminidase) activity in Actinomyces species by using 2-(4-methylumbelliferyl)α-D-N-acetylneuraminic acid in a filter paper spot test. J Clin Microbiol27:182-184.
80.
Moore WEC, Moore LVH (1994). The bacteria of periodontal disease. Periodontology20005:66-77.
81.
Morou-Bermudez E., Burne RA (1996). Isolation of urease genes of Actinomyces naeslundii WVU45 (abstract). J Dent Res75(Spec Iss):93.
82.
Morou-Bermudez E., Burne RA (1999). Genetic and physiologic characterization of the urease of Actinomyces naeslundii. Infect Immun67:504-512.
83.
Murray PA, Levine MJ, Reddy MS, Tabak LA, Bergey EJ (1986). Preparation of a sialic acid-binding protein from Streptococcus mitis KS32AR. Infect Immun53:359-365.
84.
Nesbitt WE, Beem JE, Leung K.-P, Clark WB (1992). Isolation and characterization of Actinomyces viscosus mutants defective in binding salivary proline-rich proteins. Infect Immun60:1095-1100.
85.
Nesbitt WE, Fukushima H., Leung K.-P, Clark WB (1993). Coaggregation of Prevotella intermedia with oral Actinomyces species. Infect Immun61:2011-2014.
86.
Nijjar MS, Pritchard ET, Dawes C., Philips SR (1970). Neuraminidase activity in the salivary glands of rats and human saliva. Arch Oral Biol15:89-92.
87.
Norman JM, Bunny KL, Giffard PM (1995). Characterization of levJ, a sucrase/fructanase-encoding gene from Actinomyces naeslundii T14V, and comparison of its product with other sucrose-clearing enzymes. Gene152:93-98.
88.
Nyvad B., Kilian M. (1987). Microbiology of the early colonization of human enamel and root surfaces in vivo. Scand J Dent Res95:369-380.
89.
Pabst MJ (1977). Levan and levansucrase of Actinomyces viscosus. Infect Immun15:518-526.
90.
Perlitsh MJ, Glickman I. (1966). Salivary neuraminidase. I. The presence of neuraminidase in human saliva. J Periodontol37:368-373.
91.
Ramos CP, Foster G., Matthew MD (1997). Phylogenetic analysis of the genus Actinomyces based on 16S rRNA gene sequences: description of Arcanobacterium phocae sp. nov., Arcanobacterium bernardiae comb. nov., and Arcanobacterium pyogenes comb. nov. Int J Syst Bacteriol47:46-53.
92.
Rogers R., Newbrun E., Tatevossian A. (1979). Neuraminidase activity in human dental plaque fluid. Arch Oral Biol24:703-705.
93.
Roggentin P., Rothe B., Kaper JB, Galen J., Lawrisuk L., Vimr ER, et al. (1989). Conserved sequences in bacterial and viral sialidases. Glycoconjugate J6:349-353.
94.
Russell RRB (1994). The application of molecular genetics to the microbiology of dental caries. Caries Res28:69-82.
95.
Salako NO, Kleinberg I. (1989). Incidence of selected ureolytic bacteria in human dental plaque from sites with differing salivary access. Arch Oral Biol34:787-791.
96.
Sandberg AL, Mudrick LL, Cisar JO, Brennan MJ, Mergenhagen SE, Vatter AE (1986). Type 2 fimbrial lectin-mediated phagocytosis of oral Actinomyces spp. by polymorphonuclear leukocytes. Infect Immun54:472-476.
97.
Sandberg AL, Ruhl S., Joralmon RA, Brennan MJ, Sutphin MJ, Cisar JO (1995). Putative glycoprotein and glycolipid polymorphonuclear leukocyte receptors for the Actinomyces naeslundii WVU45 fimbrial lectin. Infect Immun63:2625-2631.
98.
Schneewind O., Mihaylova-Petkov D., Model P. (1993). Cell wall sorting signals in surface proteins of Gram-positive bacteria. EMBO J12:4803-4811.
99.
Servellon CH (1982). Determination and isolation of bacterial neuraminidase from Actinomyces viscosus T14V (dissertation). Washington, DC: Georgetown University.
100.
Slack JM (1974). Family I. Actinomycetaceae. In: Bergey's manual of determinative bacteriology. Buchanan RE, Gibbons NE, editors. Baltimore: Williams & Wilkins, pp. 659-681.
101.
Smyth CJ, Marron MB, Twohig JMGJ, Smith SGJ (1996). Fimbrial adhesins: similarities and variations in structure and biogenesis. FEMS Immunol Med Microbiol16:127-139.
102.
Socransky SS, Hubersak C., Propas D. (1970). Induction of periodontal destruction in gnotobiotic rats by a human oral strain of Actinomyces naeslundii. Arch Oral Biol15:993-995.
103.
Socransky SS, Manganiello AD, Propas D., Oram V., van Houte J. (1977). Bacteriological studies of developing supragingival dental plaque. I Periodont Res12:90-106.
104.
Stackebrandt E., Charfreitag O. (1990). Partial 16S rRNA primary structure of five Actinomyces species: phylogenetic implications and development of an Actinomyces israelii-specific oligonucleotide probe. J Gen Microbiol136:37-43.
105.
Stackebrandt E., Woese CR (1981). Towards a phylogeny of the Actinomycetes and related organisms. Curr Microbiol5:197-202.
106.
Takahashi N., Mizuno F., Takamori K. (1983). Isolation and properties of levanase from Streptococcus salivarius KTA-19. Infect Immun42:231-236.
107.
Takahashi Y., Sandberg AL, Ruhl S., Muller J., Cisar JO (1997). A specific cell surface antigen of Streptococcus gordonii is associated with bacterial hemagglutination and adhesion to α2-3-linked sialic-acid containing receptors. Infect Immun65:5042-5051.
108.
Teufel M., Roggentin P., Schauer R. (1989). Properties of sialidase isolated from Actinomyces viscosus DSM 43798. Biol Chem Hoppe-Seyler370:435-443.
109.
Thankavel K., Madison B., Ikeda T., Malaviya R., Shah AH, Arumugam PM, et al. (1997). Localization of a domain in the FimH adhesin of Escherichia coli type 1 fimbriae capable of receptor recognition and use of a domain-specific antibody to confer protection against experimental urinary tract infection. J Clin Invest100:1123-1136.
110.
Theilade E., Theilade J., Mikkelsen L. (1982). Microbiological studies on early dento-gingival plaque. J Periodont Res17:12-25.
111.
Tuyau JE, Sims W. ( 1975). Occurrence of haemophili in dental plaque and their association with neuraminidase activity. J Dent Res54:737-739.
112.
Tylenda CA, Calvert C., Kolenbrander PE, Tylenda A. (1985). Isolation of Actinomyces bacteriophage from human dental plaque. Infect Immun49:1-6.
113.
van der Hoeven JS, Vogels GD, Bekkers MFJ (1976). A levansucrase from Actinomyces viscosus. Caries Res10:33-48.
114.
von Heijne G. (1986). A new method for predicting signal sequence cleavage sites. Nucleic Acids Res14:4683-4690.
115.
Weerkamp AH, Handley PS, Baars A., Slots JW (1986). Negative staining and immunoelectron microscopy of adhesion deficient mutants of Streptococcus salivarius reveal that the adhesive protein antigens are separate classes of cell surface fibril. J Bacteriol165:746-755.
Wust J., Stubbs S., Weiss N., Funke G., Collins MD (1995). Assignment of Actinomyces pyogenes-like (CDC coryneform group E) bacteria to the genus Actinomyces as Actinomyces radingae sp. nov. and Actinomyces turicensis sp. nov. Lett Appl Microbiol20:76-81.
118.
Yanagawa R., Honda E. (1976). Presence of pili in species of human and animal parasites and pathogens of the genus Corynebacterium. Infect Immun13:1293-1295.
119.
Yeung MK (1992). Conservation of an Actinomyces viscosus T14V type 1 fimbrial subunit homolog among divergent groups of Actinomyces spp. Infect Immun60:1047-1054.
120.
Yeung MK (1993). Complete nucleotide sequence of the Actinomyces viscosus T14V sialidase gene: presence of a conserved repeating sequence among strains of Actinomyces spp. Infect Immun61:109-116.
121.
Yeung MK (1995). Construction and use of integration plasmids to generate site-specific mutations in the Actinomyces viscosus T14V chromosome. Infect Immun63:2924-2930.
122.
Yeung MK, Cisar JO (1988). Cloning and nucleotide sequence of a gene for Actinomyces naeslundii WVU45 type 2 fimbriae. J Bacteriol170:3803-3809.
123.
Yeung MK, Cisar JO (1990). Sequence homology between the subunits of two immunologically and functionally distinct types of fimbriae of Actinomyces spp. J Bacteriol172:2462-2468.
124.
Yeung MK, Fernandez SR (1991). Isolation of a neuraminidase gene from Actinomyces viscosus T14V. Appl Environ Microbiol37:3062-3069.
125.
Yeung MK, Kozelsky CS (1994). Transformation of Actinomyces spp. by a Gram-negative broad-host-range plasmid. J Bacteriol176:4173-4176.
126.
Yeung MK, Kozelsky CS (1997). Transfection of Actinomyces spp. by genomic DNA of bacteriophages from human dental plaque. Plasmid37:141-153.
127.
Yeung MK, Ragsdale PA (1997). Synthesis and function of the Actinomyces naeslundii T14V type I fimbriae require the expression of additional fimbria-associated genes. Infect Immun65:2629-2639.
128.
Yeung MK, Ragsdale PA (1998). Analysis of the Actinomyces naeslundii T14V type 2 fimbrial gene cluster (abstract). J Dent Res77(Spec Iss):731.
129.
Yeung MK, Chassy BM, Cisar JO (1987). Cloning and expression of a type I fimbrial subunit of Actinomyces viscosus T14V. J Bacteriol169:1678-1683.
130.
Yeung MK, Donkersloot JA, Cisar JO, Ragsdale PA (1998). Identification of a gene involved in assembly of Actinomyces naeslundii T14V type 2 fimbriae. Infect Immun66:1482-1491.
