Aggregatibacter actinomycetemcomitans is divided into 6 serotypes. Occurrence of non-serotypeable strains is known, but background reasons are unclear. We hypothesized that non-serotypeable strains represent new serotypes or have altered expression of serotype-specific polysaccharide antigen (S-PA). We first characterized 311 strains from 189 individuals using both immunoassay- and PCR-based serotyping. Next, using natural human infection and rabbit immunization approaches, we clarified whether the phenotypically non-serotypeable strains expressed S-PA. Immunoassay identified serotypes a–f among 216 strains from 159 individuals. The remaining 95 strains from 30 individuals were phenotypically non-serotypeable. Yet, all these strains were identified by PCR-typing as serotype a-, b-, c-, or f. Non-serotypeability was confirmed by Western immunoblot with respective rabbit antisera. Patient sera remained non-reactive with autologous non-serotypeable strains at the serotype-specific region. Rabbit immunization with a phenotypically non-serotypeable strain induced no antibody production against S-PA. Thus, phenotypically non-serotypeable strains did not include novel serotypes, but lacked S-PA expression.
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References
1.
Armitage GC (1999). Development of a classification system for periodontal diseases and conditions. Ann Periodontol4:1–6.
2.
Asakawa R, Komatsuzawa H, Kawai T, Yamada G, Gonçalves RB, Izumi S, et al. (2003). Outer membrane protein 100, a versatile virulence factor of Actinobacillus actinomycetemcomitans. Mol Microbiol50: 1125–1139.
3.
Asikainen S, Lai CH, Alaluusua S, Slots J (1991). Distribution of Actinobacillus actinomycetemcomitans serotypes in periodontal health and disease. Oral Microbiol Immunol6:115–118.
4.
Asikainen S, Chen C, Slots J (1995). Actinobacillus actinomycetemcomitans genotypes in relation to serotypes and periodontal status. Oral Microbiol Immunol10:65–68.
5.
Asikainen S, Chen C, Saarela M, Saxén L, Slots J (1997). Clonal specificity of Actinobacillus actinomycetemcomitans in destructive periodontal disease. Clin Infect Dis25(Suppl 2):227–229.
6.
Califano JV, Schenkein HA, Tew JG (1989). Immunodominant antigen of Actinobacillus actinomycetemcomitans Y4 in high-responder patients. Infect Immun57:1582–1589.
7.
Dahlén G, Widar F, Teanpaisan R, Papapanou PN, Baelum V, Fejerskov O (2002). Actinobacillus actinomycetemcomitans in a rural adult population in southern Thailand. Oral Microbiol Immunol17:137–142.
8.
Doğan B, Saarela MH, Jousimies-Somer H, Alaluusua S, Asikainen S (1999). Actinobacillus actinomycetemcomitans serotype e—biotypes, genetic diversity and distribution in relation to periodontal status. Oral Microbiol Immunol14:98–103.
9.
Doğan B, Antinheimo J, Cetiner D, Bodur A, Emingil G, Buduneli E, et al. (2003). Subgingival microflora in Turkish patients with periodontitis. J Periodontol74:803–814.
10.
Doğan B, Buduneli E, Emingil G, Atilla G, Akilli A, Antinheimo J, et al. (2005). Characteristics of periodontal microflora in acute myocardial infarction. J Periodontol76:740–748.
11.
Fujise O, Wang Y, Chen W, Chen C (2008). Adherence of Aggregatibacter actinomycetemcomitans via serotype-specific polysaccharide antigens in lipopolysaccharides. Oral Microbiol Immunol23:226–233.
12.
Haubek D, Poulsen K, Asikainen S, Kilian M (1995). Evidence for absence in northern Europe of especially virulent clonal types of Actinobacillus actinomycetemcomitans. J Clin Microbiol33:395–401.
13.
Haubek D, Dirienzo JM, Tinoco EM, Westergaard J, López NJ, Chung CP, et al. (1997). Racial tropism of a highly toxic clone of Actinobacillus actinomycetemcomitans associated with juvenile periodontitis. J Clin Microbiol35:3037–3042.
14.
Kaplan JB, Perry MB, MacLean LL, Furgang D, Wilson ME, Fine DH (2001). Structural and genetic analyses of O polysaccharide from Actinobacillus actinomycetemcomitans serotype f. Infect Immun69:5375–5384.
15.
Karched M, Ihalin R, Eneslätt K, Zhong D, Oscarsson J, Wai SN, et al. (2008). Vesicle-independent extracellular release of a proinflammatory outer membrane lipoprotein in free-soluble form. BMC Microbiol8:18.
16.
Lakio L, Paju S, Alfthan G, Tiirola T, Asikainen S, Pussinen PJ (2003). Actinobacillus actinomycetemcomitans serotype d-specific antigen contains the O antigen of lipopolysaccharide. Infect Immun71: 5005–5011.
17.
Mombelli A, Gmür R, Frey J, Meyer J, Zee KY, Tam JO, et al. (1998). Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis in young Chinese adults. Oral Microbiol Immunol13:231–237.
18.
Nakashima K, Usui C, Koseki T, Nishihara T, Ishikawa I (1998). Two different types of humoral immune response to Actinobacillus actinomycetemcomitans in high-responder periodontitis patients. J Med Microbiol47:569–575.
19.
Oscarsson J, Karched M, Thay B, Chen C, Asikainen S (2008). Proinflammatory effect in whole blood by free soluble bacterial components released from planktonic and biofilm cells. BMC Microbiol8:206.
20.
Page RC, Sims TJ, Engel LD, Moncla BJ, Bainbridge B, Stray J, et al. (1991). The immunodominant outer membrane antigen of Actinobacillus actinomycetemcomitans is located in the serotype-specific high-molecular-mass carbohydrate moiety of lipopolysaccharide. Infect Immun59:3451–3462.
21.
Paju S, Saarela M, Alaluusua S, Fives-Taylor P, Asikainen S (1998). Characterization of serologically nontypeable Actinobacillus actinomycetemcomitans isolates. J Clin Microbiol36:2019–2022.
22.
Paju S, Carlson P, Jousimies-Somer H, Asikainen S (2000a). Heterogeneity of Actinobacillus actinomycetemcomitans strains in various human infections and relationships between serotype, genotype, and antimicrobial susceptibility. J Clin Microbiol38:79–84.
23.
Paju S, Saarela M, Chen C, Jousimies-Somer H, Uitto V, Asikainen S (2000b). Altered antigenicity is seen in the lipopolysaccharide profile of non-serotypeable Actinobacillus actinomycetemcomitans strains. FEMS Immunol Med Microbiol27:171–177.
24.
Poulsen K, Theilade E, Lally ET, Demuth DR, Kilian M (1994). Population structure of Actinobacillus actinomycetemcomitans: a framework for studies of disease-associated properties. Microbiology140(Pt 8):2049–2060.
25.
Rupani D, Izano EA, Schreiner HC, Fine DH, Kaplan JB (2008). Aggregatibacter actinomycetemcomitans serotype f O-polysaccharide mediates coaggregation with Fusobacterium nucleatum. Oral Microbiol Immunol23:127–130.
26.
Saarela M, Asikainen S, Alaluusua S, Pyhälä L, Lai CH, Jousimies-Somer H (1992). Frequency and stability of mono- or poly-infection by Actinobacillus actinomycetemcomitans serotypes a, b, c, d or e. Oral Microbiol Immunol7:277–279.
27.
Sims TJ, Moncla BJ, Darveau RP, Page RC (1991). Antigens of Actinobacillus actinomycetemcomitans recognized by patients with juvenile periodontitis and periodontally normal subjects. Infect Immun59:913–924.
28.
Sundqvist G, Johansson E (1982). Bactericidal effect of pooled human serum on Bacteroides melaninogenicus, Bacteroides asaccharolyticus and Actinobacillus actinomycetemcomitans. Scand J Dent Res90:29–36.
29.
Suzuki N, Nakano Y, Yoshida Y, Ikeda D, Koga T (2001). Identification of Actinobacillus actinomycetemcomitans serotypes by multiplex PCR. J Clin Microbiol39:2002–2005.
30.
Suzuki N, Nakano Y, Kiyoura Y (2006). Characterizing the specific coaggregation between Actinobacillus actinomycetemcomitans serotype c strains and Porphyromonas gingivalis ATCC 33277. Oral Microbiol Immunol21:385–391.
31.
Teixeira RE, Mendes EN, Roque de Carvalho MA, Nicoli JR, Farias LdeM, Magalhães PP (2006). Actinobacillus actinomycetemcomitans serotype-specific genotypes and periodontal status in Brazilian subjects. Can J Microbiol52:182–188.
32.
Wilson ME, Schifferle RE (1991). Evidence that the serotype b antigenic determinant of Actinobacillus actinomycetemcomitans Y4 resides in the polysaccharide moiety of lipopolysaccharide. Infect Immun59:1544–1551.
33.
von Troil-Lindén B, Torkko H, Alaluusua S, Wolf J, Jousimies-Somer H, Asikainen S (1995). Periodontal findings in spouses. A clinical, radiographic and microbiological study. J Clin Periodontol19:93–99.
34.
Yang HW, Huang YF, Chan Y, Chou MY (2005). Relationship of Actinobacillus actinomycetemcomitans serotypes to periodontal condition: prevalence and proportions in subgingival plaque. Eur J Oral Sci113:28–33.
35.
Zambon JJ (1985). Actinobacillus actinomycetemcomitans in human periodontal disease. J Clin Periodontol12:1–20.
36.
Zambon JJ, Slots J, Genco RJ (1983). Serology of oral Actinobacillus actinomycetemcomitans and serotype distribution in human periodontal disease. Infect Immun41:19–27.
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