Información del artículo
Resumen
Las periodontitis son un conjunto de patologías de naturaleza inflamatoria y etiología infecciosa producidas por el biofilm patogénico subgingival. Porphyromonas gingivalis y Aggregatibacter actinomycetemcomitans son bacterias periodonto-patógenas que pueden causar daño directo a las estructuras periodontales a través de los diversos factores de virulencia que expresan. Sobre la base de estos factores de virulencia, distintos genotipos y serotipos bacterianos se han descrito, cada uno de ellos con una potencial variable patogenicidad. En esta revisión bibliográfica se describen diferentes factores de virulencia de P. gingivalis y A. actinomycetemcomitans y se discute la variable inmunogenicidad y patogenicidad de los distintos genotipos y serotipos descritos para ellos. Tanto P. gingivalis como A. actinomycetemcomitans poseen diversos factores de virulencia asociados al inicio, progresión y severidad de las periodontitis. En P. gingivalis, los factores de virulencia para los cuales se describen distintos genotipos y/o serotipos son fimbria, LPS y cápsula bacteriana, y en A. actinomycetemcomitans son leucotoxina A, Cdt y LPS. Cada uno de estos distintos genotipos y serotipos induce una respuesta inmuno-inflamatoria diferente en el hospedero y, por lo tanto, se podrían asociar a una variable patogenicidad y podrían determinar las características clínicas de la enfermedad.
Palabras clave:
Virulencia
genotipos
serotipos
Porphyromonas gingivalis
Aggregatibacter actinomycetemcomitans
Abstract
Periodontitis represents a heterogenic group of periodontal infections elicited by bacteria residing at the subgingival biofilm. Although this biofilm is constituted by a broad variety of bacterial species, only a limited number has been associated with the periodontitis aetiology, among them Porphyromonas gingivalis and Aggregatibacter actinomycetemcomitans. Both P. gingivalis and A. actinomycetemcomitans express a number of virulence factors that contribute to direct tissue damage and, based on them, distinct genotypes and serotypes have been described, each one with a potential variable pathogenicity. This review aimed to analyze the different virulence factors described for P. gingivalis and A. actinomycetemcomitans and to discuss the variable immunogenicity and pathogenicity of their serotypes and genotypes. P. gingivalis and A. actinomycetemcomitans express different virulence factors and they determine the initiation, progression, and severity of periodontitis. In P. gingivalis, distinct serotypes and/or genotypes are described based on fimbriae, LPS, and capsule. Additionally, in A. actinomycetemcomitans distinct serotypes and/or genotypes are described based on leucotoxin A, Cdt, and LPS. These distinct serotypes and genotypes induce a differential immunoinflammatory response and, thus, could be associated with variations in pathogenicity and reflected in clinic characteristics of the disease.
Key words:
Virulence
genotypes
serotypes
Porphyromonas gingivalis
Aggregatibacter actinomycetemcomitans
El Texto completo está disponible en PDF
Referencias bibliográficas
[1.]
S. Offenbacher, S. Lieff, K.A. Boggess, A.P. Murtha, P.N. Madianos, C.M. Champagne, R.G. McKaig, H.L. Jared, S.M. Mauriello, R.L. Auten, W.N. Herbert, J.D. Beck.
Maternal periodontitis and prematurity Part I: Obstetric outcome of prematurity and growth restriction.
Ann Periodontol, 6 (2001), pp. 164-174
[2.]
M.S. Tonetti, M.A. Imboden, N.P. Lan.
Neutrophil migration into the gingival sulcus is associated with transepithelial gradients of interleukin-8 and ICAM-1.
J Periodontol, 69 (1998), pp. 1139-1147
[3.]
S.S. Socransky, A.D. Haffajee.
Dental biofilms: Difficult therapeutic targets.
Periodontology 2000, 28 (2002), pp. 12-55
[4.]
J. Slots, L. Bragd, M. Wikstrom, G. Dahle.
The occurrence of Actinobacillus actinomycetemcomitans, Bacteroides gingivalis and Bacteroides intermedius in destructive periodontal disease in adults.
J Clin Periodontol, 13 (1986), pp. 570-577
[5.]
A.J. van Winkelhoff, B.G. Loos, W.A. van der Reijden, U. van der Velden.
Spain Porphyromonas gingivalis, Bacteroides forsythus and other putative periodontal pathogens in subjects with and without periodontal destruction.
J Clin Periodontol, 29 (2002), pp. 1023-1028
[6.]
R.C. Page, S. Offenbacher, H.E. Schroeder, G.J. Seymour, K.S. Kornman.
Advances in the pathogenesis of periodontitis: Summary of developments, clinical implications and future directions.
Periodontol 2000, 14 (1997), pp. 216-248
[7.]
N. Dutzan, J. Gamonal, A. Silva, M. Sanz, R. Vernal.
Over-expression of forkhead box P3 and its association with receptor activator of nuclear factor-κβ ligand, interleukin (IL)-17, IL-10 and transforming growth factor-β during the progression of chronic periodontitis.
J Clin Periodontol, 36 (2009), pp. 396-403
[8.]
N. Silva, N. Dutzan, M. Hernández, A. Dezerega, O. Rivera, J.C. Aguillón, et al.
Characterization of progressive periodontal lesions in chronic periodontitis patients: Levels of chemokines, cytokines, matrix metalloproteinase- 13, periodontal pathogens and inflammatory cells.
J Clin Periodontol, 35 (2008), pp. 206-214
[9.]
J.H. Meurman, M. Sanz, S.J. Janket.
Oral health, atherosclerosis, and cardiovascular disease.
Crit Rev Oral Biol Med, 15 (2004), pp. 403-413
[10.]
S. Asikainen, C.H. Lai, S. Alaluusua, J. Slots.
Distribution of Actinobacillus actinomycetemcomitans serotypes in periodontal health and disease.
Oral Microbiol Immunol, 6 (1991), pp. 115-118
[11.]
T. Zhang, T. Kurita-Ochiai, T. Hashizume, Y. Du, S. Ogushi, M. Yamamoto.
Aggregatibacter actinomycetemcomitans accelerates atherosclerosis with an increase in atrherogenic factors in spontaneously hyperlipidemic mice.
Immunol Med Microbiol, 59 (2010), pp. 143-151
[12.]
F. Emamghorashi, S. Farchad, M. Kalani.
Relashionship between O serotype and virulent genes in Escherichia coli causing urinary tratc infections.
Ir J Kidney Diseases, 5 (2011), pp. 234-237
[13.]
S. Morisset, F. Peyron, J.R. Lobry, J. Garweg, J. Ferrandiz, K. Musset, J.E. Gomez- Marin, A. de la Torre, M. Demar, B. Carme, C. Mercier, J.F. Garin, M.F. Cesbron- Delaw.
Serotyping of Toxoplasma gondii: Striking homogeneous patter between symptomatic and asymptomatic infections within Europe and South America.
Microbes and Infection, 10 (2008), pp. 742-747
[14.]
R. Vernal, R. León, A. Silva, A.J. van Winkelhoff, J.A. García-Sanz, M. Sanz.
Differential cytokine expression by human dendritic cells in response to different Porphyromonas gingivalis capsular serotypes.
J Clin Periodontol, 36 (2009), pp. 823-829
[15.]
J. Slots.
Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis in periodontal disease: Introduction.
Periodontology 2000, 20 (1999), pp. 7-13
[16.]
S.C. Holt, J.L. Ebersole.
The oral spirochetes: Their ecology and pathogenesis.
Molecular Biology and Pathogenesis of Treponemal Infections.,
[17.]
S.C. Holt, L. Kesavalu, S. Walker, C.A. Genco.
Virulence factors in Porphyromonas gingivalis.
Periodontol 2000, 20 (1999), pp. 168-238
[18.]
R. Poulin, C. Combes.
The concept of virulence: Interpretations and implications.
Parasitol Today, 15 (1999), pp. 474-475
[19.]
J.L. Ebersole, M.N. Sandoval, M.J. Steffen, D. Cappelli.
Serum-Antibody in Actinobacillus actinomycetemcomitans-Infected pactients with periodontal disease.
Infection and Immunity, 59 (1991), pp. 1795-1802
[20.]
F. Kauffmann.
Ueber neue themolabile Korperantigene der colibakterien.
Acta Pathol Microbiol Scand, 20 (1943), pp. 21-44
[21.]
R.N. Gruneberg.
Antibiotic sensitivities of urinary pathogens, 1971-82.
J Antimicrob Chemother, 14 (1984), pp. 17-23
[22.]
D.K. Howe, L.D. Sibley.
Toxoplasma gondii comprises three clonal lineages: Correlation of parasite genotype with human disease.
J Infect Dis, 172 (1995), pp. 1561-1566
[23.]
L.D. Sibley, D.G. Mordue, C. Su, P.M. Robben, D.K. Howe.
Genetic approaches to studying virulence and pathogenesis in Toxoplasma gondii.
R Soc Lond B Biol Sci, 357 (2002), pp. 81-88
[24.]
T.D. Herath, Y. Wang, C.J. Seneviratne, Q. Lu, R.P. Darveau, C.Y. Wang, L. Jin.
Porphyromonas gingivalis lipopolysaccharide lipid A heterogeneity differentially modulates the expression of IL-6 and IL-8 in human gingival fibroblasts.
J Clin Periodontol, 38 (2011), pp. 694-701
[25.]
T. Yoshino, M. Laine, A.J. van Winkelhoff, G. Dahlén.
Genotype variation and capsular serotypes of Porphyromonas gingivalis from chronic periodontitis and periodontal abcsesses.
FEMS Microbiol Lett, 270 (2007), pp. 75-81
[26.]
S.R.L. Teixeira, F. Mattarazo, M. Ferez, L.C. Figueredo, M. Faveri, M.R.L. Simionato, M.P.A. Mayer.
Quantification of Prohyromonas gingivalis and fimA genotypes in smoker chronic periodontitis.
J Clin Periodontol, 26 (2009), pp. 482-487
[27.]
H. Hiramine, K. Watanabe, N. Hamada, T. Umemoto.
Porphyromonas gingivalis 67-kDa fimbriae induced cytokine production and osteoclast differentiation utilizing TLR2.
FEMS Microbiology Letters, 229 (2003), pp. 49-55
[28.]
M. Kuboniwa, H. Inaba, A. Amano.
Genotyping to distinguish microbial pathogenicity in periodontitis.
Periodontology 2000, 54 (2010), pp. 136-159
[29.]
A. Amano, I. Nakagawa, N. Okahashi, N. Hamada.
Variations of Porphyromonas gingivalis fimbriae in relation to microbial pathogenesis.
J Periodontal Res, 39 (2004), pp. 136-142
[30.]
M. Enersen, I. Olsen, O. Kvalheim, D.A. Caugant.
fimA genotypes and multilocus sequence types of Porphyromonas gingivalis from patients with periodontitis.
J Clin Microbiol, 46 (2008), pp. 31-42
[31.]
A. Amano, M. Kuboniwa, I. Nakagawa, S. Akiyama, I. Morisaki, S. Hamada.
Prevalence of specific genotypes of Porphyromonas gingivalis fimA and periodontal health status.
J Dent Res, 79 (2000), pp. 1664-1668
[32.]
J.R. van der Ploeg, E. Giertsen, B. Lü din, C. Mörgeli, A.S. Zinkernagel, R. Gmur.
Quantitative detection of Porphyromonas gingivalis fimA genotypes in dental plaque.
FEMS Microbiology Letters, 232 (2004), pp. 31-37
[33.]
M. Wang, K. Liang Sm Hosur, H. Domon, F. Yoshimura, A. Amano, G. Hajishengallis.
Differential virulence and innate interactions of Type I and II fimbrial genotypes of Porphyromonas gingivalis.
Oral Microbiol Immunol, 24 (2009), pp. 478-484
[34.]
A. Poltorak, X. He, I. Smirnova, et al.
Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: Mutations in TLR4 gene.
Science, 282 (1998), pp. 2085-2088
[35.]
D.O. Osbourne, W. Aruni, F. Roy, C. Perry, L. Sandberg, A. Muthiah, H. Fletcher.
Role of vimA cell surface biogenesis in Porphyromonas gingivalis.
Microbiology, 156 (2010), pp. 2180-2193
[36.]
J. Travis, R. Pike, T. Imamura, J. Potempa.
Porphyromonas gingivalis proteinases as virulence factors in the development of periodontitis.
J Periodontal Res, 32 (1997), pp. 120-125
[37.]
T. Imamura.
The role of gingipains in the pathogenesis of periodontal disease.
J Periodontol, 71 (2003), pp. 111-118
[38.]
P.G. Stathopoulou, J.C. Galicia, M.R. Benakanakere, C.A. García, J. Potempa, D.F. Kinane.
Porphyromonas gingivalis induce apotosis in human gingival epitelial cells through a gingipain-dependent mechanism.
BMC Microbiol, 9 (2009), pp. 107
[39.]
T. Beikler, U. Peters, K. Prior, B. Ejhmke, T.F. Flemmig.
Sequence variations in rgpA and rgpB of Porphyromonas gingivalis in periodontitis.
J Periodontal Res, 40 (2005), pp. 193-198
[40.]
M. Kubinowa, H. Inaba, A. Amano.
Genotyping to distinguish microbial pathogenicity in periodontitis.
Periodontol 2000, 54 (2000), pp. 136-159
[41.]
D.R. Dixon, R.P. Darveau.
Lipopolysaccharide heterogeneity: Innate host responses to bacterial modification of lipid a structure.
J Dent Res, 84 (2005), pp. 584-595
[42.]
L. Kocgozlu, R. Elkaim, H. Tenenbaum, S. Werner.
Variable cell responses to P. gingivalis lipopolysaccharide.
J Dent Res, 88 (2009), pp. 741-745
[43.]
R. Kikkert, M.L. Laine, L.A. Aarden, A.J. van Winkelhoff.
Activation of toll-like receptors 2 and 4 by gram-negative periodontal bacteria.
Oral Microbiol Immunol, 22 (2007), pp. 145-151
[44.]
G. d’Empaire, M.T. Baer, F.C. Gibson.
K1 serotype capsular polysaccharide of Porphyromonas gingivalis elicits chemokine production from murine macrophages that facilitates cell migration.
Infect Immun, 74 (2006), pp. 6236-6243
[45.]
M.L. Laine, B.J. Appelmelk, van Winkelhoff..
Novel polysaccharide capsular serotypes in Porphyromonas gingivalis.
J Periodontal Res, 31 (1996), pp. 278-284
[46.]
M.L. Laine, A.J. van Winkelhoff.
Virulence of six capsular serotypes of Porphyromonas gingivalis in a mouse model.
Oral Microbiol Immunol, 13 (1998), pp. 322-325
[47.]
N. Suzuki, Y. Nakano, Y. Yoshida, D. Ikeda, T. Koga.
Identification of Actinobacillus actinomycetemcomitans serotypes by multiplex PCR.
J Clin Microbiol, 39 (2001), pp. 2002-2005
[48.]
T. Shimada, N. Sugano, R. Nishihara, K. Suzuki, H. Tanaka, K. Ito.
Differential effects of five Aggregatibacter actinomycetemcomitans strains on gingival epithelial cells.
Oral Microbiol Immunol, 23 (2008), pp. 455-458
[49.]
D.D. Bosshardt, N.P. Lang.
The junctional epithelium: From health to disease.
J Dent Res, 85 (2005), pp. 9-20
[50.]
M. Iniesta, D. Herrera, J. Serrano, M. Sanz.
Análisis de los factores de virulencia de los patógenos de asociación fuerte con la periodontitis: Aggregatibacter actinomycetemcomitans Porphyromonas gingivalis y Tannerella forsythia.
Periodoncia y Oseointegración, 18 (2008), pp. 109-115
[51.]
I. Xynogala, A. Volgina, J.M. DiRienzo, J. Korostoff.
Evaluation of the humoral immune response to the cytolethal distending toxin of Aggregatibacter actinomycetemcomitans in subjects with localized aggresive periodontitis.
Oral Microbiol Immunol, 24 (2009), pp. 116-123
[52.]
S.C. Kachlany.
Aggregatibacter actinomycetemcomitans leukotoxin: From threat to therapy.
J Dent Research, 89 (2010), pp. 561-570
[53.]
P.C. Baehni, C.C. Tsai, W.P. McArthur, B.F. Hammond, B.J. Shenker, N.S. Taichman.
Leukotoxic activity in different strains of the bacterium Actinobacillus actinomycetemcomitans isolated from juvenile periodontitis in man.
Arch Oral Biol, 26 (1981), pp. 671-676
[54.]
R. Diaz, L.A. Ghofaily, J. Patel, N.V. Balashova, A.C. Freitas, I. Labib, et al.
Characterization of leukotoxin from a clinical strain of Actinobacillus actinomycetemcomitans.
Microb Pathog, 40 (2006), pp. 48-55
[55.]
E. Kraig, T. Dailey, D. Kolodrubetz.
Nucleotide sequence of the leucotoxin gene from Actinobacillus actinomycetemcomitans: Homology to the alphahemolysin/leukotoxin gene family.
Infect Immun, 58 (1990), pp. 920-929
[56.]
E.T. Lally, E.E. Golub, I.R. Kieba, N.S. Taichman, J. Rosenbloom, J.C. Rosenbloom, C.W. Gibson, D.R. Demuth.
Analysis of the Actinobacillus actinomycetemcomitans leukotoxin gene Delineation of unique features and comparison to homologous toxins.
J Biol Chem, 264 (1989), pp. 15451-15456
[57.]
W. Heywood, B. Henderson, S.P. Nair.
Cytolethal distending toxin: Creating a gap in the cell cycle.
J Med Microbiol, 54 (2005), pp. 207-216
[58.]
T. Frisan, X. Cortes-Bratti, E. Chaves-Olarte, B. Stenerlow, M. Thelestam.
The hemophilus ducreyi cytolethal distending toxin induces DNA double - strand breaks and promotes ATM-dependent activation of RhoA.
Cell Microbiol, 5 (2003), pp. 707-965
[59.]
E.S. Ando, L.A. De-Gennaro, M. Faveri, M. Feres, J.M. DiRienzo, M.P.A. Mater.
Immune response to cytolethal distending toxin of Aggregatibacter actinomycetemcomitans in peridontitis patiens.
J Periodontal Res, 45 (2010), pp. 471-480
[60.]
J.L. Smith, D.O. Bayles.
The contribution of cytolethal distending toxin to bacterial pathogenesis.
Crit Rev Microbiol, 32 (2006), pp. 227-248
[61.]
A.S. Fabris, J.M. DiRienzo, M. Wikstrom, M.P. Mayer.
Detection of cytolethal distending toxin activity and cdt genes in Actinobacillus actinomycetemcomitans isolates from geographically diverse populations.
Oral Microbiol Immunol, 17 (2002), pp. 231-238
[62.]
G.N. Belibasakis, M. Brage, T. Lagergard, A. Johansson.
Cytolethal distending toxin upregulates RANKL expression in Jurkat T-cells.
Journal Compilation, 116 (2008), pp. 499-506
[63.]
M. Damek-Poprawa, M. Haris, A. Volgina, J. Korostoff, J.M. DiRienzo.
Cytolethal distending toxin damages the oral epithelium of gingival explants.
J Dent Res, 90 (2011), pp. 874-879
[64.]
S. Akifusa, S. Poole, J. Lewthwaite, B. Henderson, S.P. Nair.
Recombinant Actinobacillus actinomycetemcomitans cytolethal distending toxin proteins are required to interact to inhibit human cell cycle progression and to stimulate human leukocyte cytokine synthesis.
Infect Immun, 69 (2001), pp. 5925-5930
[65.]
S.C. Holt, A.C. Tanner, S.S. Socransky.
Morphology and ultrastructure of oral strains of Actinobacillus actinomycetemcomitans and Haemophilus aphrophilus.
Infect Immun, 30 (1980), pp. 588-600
[66.]
J.J. Zambon, C. DeLuca, J. Slots, R.J. Genco.
Studies of leukotoxin from Actinobacillus actinomycetemcomitans using the promyelocytic HL-60 cell line.
Infect Immun, 40 (1983), pp. 205-212
[67.]
J.J. Zambon, J. Slots, R. Genco.
Serology of oral Actinobacillus actinomycetemcomitans and serotipe distribution in human periodontal disease.
Infect Immun, 41 (1983), pp. 19-27
[68.]
E.O. King, H.W. Tatum.
Actinobacillus actinomycetemcomitans and Haemophilus aphrophilus.
J Infect Dis, 111 (1962), pp. 85-94
[69.]
J.B. Kaplan, M.B. Perry, L.L. MacLean, D. Furgang, M.E. Wilson, D.H. Fine.
Structural and genetic analyses of O polysaccharide from Actinobacillus actinomycetemcomitans serotype f.
Infect Immun, 69 (2001), pp. 5375-5384
[70.]
R. Gmür, H. McNabb, T.J.M. van Steenbergen, P. Baehni, A. Mombelli, A.J. van Winkelhoff, B. Guggenheim.
Seroclassification of hitherto nontypeable Actinobacillus actinomycetemcomitans strains: Evidence for a new serotype e.
Oral Microbiol Immunol, 8 (1993), pp. 116-120
[71.]
J.B. Kaplan, H.C. Schreiner, D. Furgang, D.H. Fine.
Population structure and genetic diversity of Actinobacillus actinomycetemcomitans strains isolated from localized juvenile periodontitis patients.
J Clin Microbiol, 40 (2002), pp. 1181-1187
[72.]
K. Poulsen, E. Theilade, E.T. Lally, D.R. Demuth, M. Kilian.
Population structure of Actinobacillus actinomycetemcomitans: A framework for studies of disease-associated properties.
Microbiology, 140 (1994), pp. 2049-2060
[73.]
K. Takada, M. Saito, O. Tsuzukibashi, Y. Kawashima, S. Ishida, M. Hirasawa.
Characterization of a new serotype g isolate of Aggregatibacter actinomycetemcomitans.
Mol Oral Microbiol, 25 (2010), pp. 200-206
[74.]
S. Asikainen, C.H. Lai, S. Alaluusua, J. Slots.
Distribution of Actinobacillus actinomycetemcomitans serotypes in periodontal health and disease.
Oral Microbiol Immunol, 6 (1991), pp. 115-118
[75.]
N. Yamaguchi, M. Kawasaki, Y. Yamashita, K. Nakashima, T. Koga.
Role of the capsular polysaccharide-like serotypespecific antigen in resistance of Actinobacillus actinomycetemcomitans to phagocytosis by human polymorphonuclear leukocytes.
Infect Immun, 63 (1995), pp. 4589-4594
[76.]
J.R. Cortelli, D.R. Aquino, S.C. Cortelli, C.V.G. Roman-Torres, G.C.N. Franco, R.S. Gomez, L.H. Batista, F.O. Costa.
Aggregatibacter actinomycetemcomitans serotypes infections and periodontal conditions: A two way assesment.
Eur J Clin Microbiol Infect Dis, 63 (2011),
[77.]
C.H. Lai, M.A. Listgarten, B.F. Hammond.
Comparative ultrastructure of leucotoxic and non-leucotoxic strains of Actinobacillus actinomycetemcomitans.
J Periodontal Res, 16 (1981), pp. 379-389
[78.]
T. Vernal, R. León, D. Herrera, J.A. García-Sanz, A. Silva, M. Sanz.
Variability in the response of human dendritic cells stimulated with Porphyromonas gingivalis or Aggregatibacter actinomycetemcomitans.
J Periodontol Res, 43 (2008), pp. 689-697
Copyright © 2012. Sociedad de Periodoncia de Chile, Sociedad de Implantología Oral de Chile y Sociedad de Prótesis y Rehabilitación Oral de Chile