Adhesion of Aggregatibacter actinomycetemcomitans to extracellular matrix proteins is mediated by antennae-like surface structures composed of EmaA oligomers. EmaA is an outer-membrane protein orthologous to the autotransporter YadA, a virulence determinant of Yersinia. emaA was present in the 27 strains examined, covering the six serotypes of A. actinomycetemcomitans. Ten individual genotypes and three different forms of the protein (full-length, intermediate and truncated) were predicted. The prototypic, full-length EmaA (202 kDa) was only associated with serotypes b and c, which displayed antennae-like surface structures. These strains bound to collagen embedded in a 3D matrix. The intermediate form of EmaA (173 kDa) was exclusively associated with serotypes d and a, which contained a 279 aa in-frame deletion, as well as a different N-terminal head domain sequence. These differences modified the appearance of the EmaA structures on the cell surface but maintained collagen-binding activity. Strains containing the truncated form of EmaA had single or multiple substitutions, deletions or insertions in the sequences, which resulted in the absence of EmaA molecules on the outer membrane and loss of collagen-binding activity. Population structure analyses of this organism, based on emaA, indicated that serotypes b and c belonged to one subpopulation, which was independent of the other serotypes. The main divergence was found in the functional head domain. The conserved emaA genotype within serotypes suggests a stable clonal linkage between this autotransporter protein and other virulence determinants.
BeckerJ.,
SchuppanD.,
RabanusJ.,
RauchR.,
NiechoyU.,
GelderblomH.1991; Immunoelectron microscopic localization of collagens type I, V, VI and of procollagen type III in human periodontal ligament and cementum. J Histochem Cytochem 39:103–110
BornsteinP.,
TraubW.1979; The chemistry and biology of collagen. In The Proteins , 3rd edn. vol 4 pp 411–632 Edited by
NeurathH.,
LR.
Orlando, FL: Hill Academic Press;
CotterS. E.,
SuranaN. K.,
GrassS.,
St. GemeJ. W.2006; Trimeric autotransporters require trimerization of the passenger domain for stability and adhesive activity. J Bacteriol 188:5400–5407
DingemansK. P.,
TeelingP.,
LagendijkJ. H.,
BeckerA. E.2000; Extracellular matrix of the human aortic media: an ultrastructural histochemical and immunohistochemical study of the adult aortic media. Anat Rec 258:1–14
DixonD. R.,
DarveauR. P.2005; Lipopolysaccharide heterogeneity: innate host responses to bacterial modification of lipid A structure. J Dent Res 84:584–595
DoganB.,
SaarelaM.,
Jousimies-SomerH.,
AlaluusuaS.,
AsikainenS.1999; Actinobacillus actinomycetemcomitans serotype e – biotypes, genetic diversity and distribution in relation to periodontal status. Oral Microbiol Immunol 14:98–103
FelsensteinJ.2005phylip (Phylogeny Inference Package) version 3.6. Distributed by the author. Department of Genome Sciences University of Washington; Seattle:
FineD. H.,
VelliyagounderK.,
FurgangD.,
KaplanJ.2005; The Actinobacillus actinomycetemcomitans autotransporter adhesin Aae exhibits specificity for buccal epithelial cells from humans and old world primates. Infect Immun 73:1947–1953
HaubekD.,
PoulsenK.,
AsikainenS.,
KilianM.1995; Evidence for absence in northern Europe of especially virulent clonal types of Actinobacillus actinomycetemcomitans . J Clin Microbiol 33:395–401
HaubekD.,
EnnibiO.,
AbdellaouiL.,
BenzartiN.,
PoulsenS.2002; Attachment loss in Moroccan early onset periodontitis patients and infection with the JP2-type of Actinobacillus actinomycetemcomitans . J Clin Periodontol 29:657–660
HoiczykE.,
RoggenkampA.,
ReichenbecherM.,
LupasA.,
HeesemannJ.2000; Structure and sequence analysis of Yersinia YadA and Moraxella UspAs reveal a novel class of adhesins. EMBO J 19:5989–5999
JainS.,
van UlsenP.,
BenzI.,
SchmidtM. A.,
FernadezR.,
TommassenJ.,
GoldbergM. B.2006; Polar localization of the autotransporter family of large bacterial virulence proteins. J Bacteriol 188:4841–4850
KaplanJ. B.,
PerryM. B.,
MacLeanL. L.,
FurgangD.,
WilsonM. E.,
FineD. H.2001; Structural and genetic analyses of O polysaccharide from Actinobacillus actinomycetemcomitans serotype f. Infect Immun 69:5375–5384
KolodrubetzD.,
DaileyT.,
EbersoleJ.,
KraigE.1989; Cloning and expression of the leukotoxin gene from Actinobacillus actinomycetemcomitans . Infect Immun 57:1465–1469
LallyE. T.,
GolubE. E.,
KiebaI. R.1994; Identification and immunological characterization of the domain of Actinobacillus actinomycetemcomitans leukotoxin that determines its specificity for human target cells. J Biol Chem 269:31289–31295
MintzK. P.2004; Identification of an extracellular matrix protein adhesin, EmaA, which mediates the adhesion of Actinobacillus actinomycetemcomitans to collagen. Microbiology 150:2677–2688
NakanoY.,
YoshidaY.,
SuzukiN.,
YamashitaY.,
KogaT.2000; A gene cluster for the synthesis of serotype d-specific polysaccharide antigen in Actinobacillus actinomycetemcomitans . Biochim Biophys Acta 1493:259–263
Nørskov-LauritsenN.,
KilianM.2006; Reclassification of Actinobacillus actinomycetemcomitans , Haemophilus aphrophilus , Haemophilus paraphrophilus and Haemophilus segnis as Aggregatibacter actinomycetemcomitans gen.nov., comb. nov., Aggregatibacter aphrophilus comb. nov. and Aggregatibacter segnis comb. nov., and emended description of Aggregatibacter aphrophilus to include V factor-dependent and V factor-independent isolates . Int J Syst Evol Microbiol 56:2135–2146
PajuS.,
CarlsonP.,
Jousimies-SomerH.,
AsikainenS.2000; Heterogeneity of Actinobacillus actinomycetemcomitans strains in various human infections and relationships between serotype, genotype, and antimicrobial susceptibility. J Clin Microbiol 38:79–84
PoulsenK.,
TheiladeE.,
LallyE. T.,
DemuthD. R.,
KilianM.1994; Population structure of Actinobacillus actinomycetemcomitans : a framework for studies of disease-associated properties. Microbiology 140:2049–2060
RoggenkampA.,
AckermannN.,
JacobiC.,
TruelzschK.,
HoffmannH.,
HeesemannJ.2003; Molecular analysis of transport and oligomerization of the Yersinia enterocolitica adhesin YadA. J Bacteriol 185:3735–3744
RoseJ. E.,
MeyerD. H.,
Fives-TaylorP. M.2003; Aae, an autotransporter involved in adhesion of Actinobacillus actinomycetemcomitans to epithelial cells. Infect Immun 71:2384–2393
RuizT.,
LenoxC.,
RadermacherM.,
MintzK. P.2006; Novel surface structures are associated with the adhesion of Actinobacillus actinomycetemcomitans to collagen. Infect Immun 74:6163–6170
SpahrA.,
KleinE.,
KhuseyinovaN.,
BoeckhC.,
MucheR.,
KunzeM.,
RothenbacherD.,
PezeshkiG.,
HoffmeisterA.,
KoenigW.2006; Periodontal infections and coronary heart disease: role of periodontal bacteria and importance of total pathogen burden in the Coronary Event and Periodontal Disease (CORODONT) study. Arch Intern Med 166:554–559
SprattB. G.,
SmithN. H.,
ZhouJ.,
O'RourkeM.,
FeilE.1995; The population genetics of the pathogenic Neisseria . In Population Genetics of Bacteria pp 143–160 Edited by
BaumbergS.,
YoungJ. P. W.,
WellingtonE. M. H.,
SaundersJ. R.
Cambridge, UK: Press Syndicate of University of Cambridge;
St GemeJ. W., III.,
CutterD.2000; The Haemophilus influenzae Hia adhesin is an autotransporter protein that remains uncleaved at the C terminus and fully cell associated. J Bacteriol 182:6005–6013
SuzukiN.,
NakanoY.,
YoshidaY.,
NakaoH.,
YamashitaY.2000Genetic analysis of the gene cluster for the synthesis of serotype a-specific polysaccharide antigen in Actinobacillus actinomycetemcomitans Biochim Biophys Acta; 1517135–138
TeixeiraR. E.,
MendesE. N.,
Rogue de CarvalhoM. A.,
NicoliJ. R.,
Farias LdeM.,
MagalhaesP. P.2006; Actinobacillus actinomycetemcomitans serotype-specific genotypes and periodontal status in Brazilian subjects. Can J Microbiol 52:182–188
YangH. W.,
AsikainenS.,
DoganB.,
SudaR.,
LaiC. H.2004; Relationship of Actinobacillus actinomycetemcomitans serotype b to aggressive periodontitis: frequency in pure cultured isolates. J Periodontol 75:592–599
YoshidaY.,
NakanoY.,
YamashitaY.,
KogaT.1998; Identification of a genetic locus essential for serotype b-specific antigen synthesis in Actinobacillus actinomycetemcomitans . Infect Immun 66:107–114
YoshidaY.,
SuzukiN.,
NakanoY.,
ShibuyaK.,
OgawaY.,
KogaT.2003; Distribution of Actinobacillus actinomycetemcomitans serotypes and Porphyromonas gingivalis in Japanese adults. Oral Microbiol Immunol 18:135–139
ZambonJ. J.,
SlotsJ.,
GencoR. J.1983; Serology of oral Actinobacillus actinomycetemcomitans and serotype distribution in human periodontal disease. Infect Immun 41:19–27