Aggregatibacter actinomycetemcomitans leukotoxin: A powerful tool with capacity to cause imbalance in the host inflammatory response

Toxins

Volumn 3, Issue 3, 2011, Pages 242-259

  Johansson, Anders ^a  

^a UMEÅ UNIVERSITY   (Sweden)

Author keywords

Aggregatibacter actinomycetemcomitans; Leukotoxin; Proinflammatory response; Virulence mechanisms

Indexed keywords

LEUKOTOXIN;

ADAPTIVE IMMUNITY; AGGREGATIBACTER ACTINOMYCETEMCOMITANS; ARTICLE; BACTERIAL VIRULENCE; CELL SPECIFICITY; ERYTHROCYTE; HUMAN; HUMORAL IMMUNITY; IMMUNE RESPONSE; INFLAMMATION; INTRACELLULAR SIGNALING; LYMPHOCYTE; MACROPHAGE; MOLECULAR INTERACTION; MONOCYTE; NEUTROPHIL; NONHUMAN; OPERON; PROTEIN EXPRESSION; PROTEIN SECRETION; TARGET CELL; TOXIN ANALYSIS; TOXIN STRUCTURE; TOXIN SYNTHESIS;

AGGREGATIBACTER ACTINOMYCETEMCOMITANS; LEUKOTOXIN; PROINFLAMMATORY RESPONSE; VIRULENCE MECHANISMS;

ACTINOBACILLUS ACTINOMYCETEMCOMITANS; CELL DEATH; CELL MEMBRANE; EXOTOXINS; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNITY, HUMORAL; LYMPHOCYTE FUNCTION-ASSOCIATED ANTIGEN-1; LYMPHOCYTES; MONOCYTES; NEUTROPHILS; PERIODONTITIS; PROTEIN BINDING; VIRULENCE;

BACTERIA (MICROORGANISMS);

EID: 79953236747     PISSN: None     EISSN: 20726651     Source Type: Journal    
DOI: 10.3390/toxins3030242     Document Type: Article

References (89)

1. Henderson, B.; Ward, J.M.; Ready, D. Aggregatibacter (Actinobacillus) actinomycetemcomitans: a triple A* periodontopathogen? Periodontol. 2000 2010, 54, 78-105.
2. Kinane, D.; Bouchard, P. Group E of the European Workshop on Peri odontology, Periodontal diseases and health: Consensus Report of the Sixth European Workshop on Periodontology. J. Clin. Periodontol. 2008, 35, 333-337.
3. Haubek, D. The highly leukotoxic JP2 clone of Aggregatibacter actinomycetemcomitans: evolutionary aspects, epidemiology and etiological role in aggressive periodontitis. APMIS 2010, 118, 1-53.
4. Fine, D.H.; Kaplan, J.B.; Kachlany, S.C.; Schreiner, H.C. How we got attached to Actinobacillus actinomycetemcomitans: a model for infectious diseases. Periodontol. 2000 2006, 42, 114-157.
5. Darveau, R.P. Periodontitis: a polymicrobial disruption of host homeostasis. Nat. Rev. Microbiol. 2010, 8, 481-490.
6. Pihlstrom, B.C.; Michalowicz, B.S.; Johnson, D.W. Periodontal diseases. Lancet 2005, 366, 1809-1820.
7. Berezow, A.B.; Darveau, R.P. Microbial shift and periodontitis. Periodontol. 2000 2011, 55, 36-47.
8. Belibasakis, G.N.; Mattsson, A.; Wang, Y.; Chen, C; Johansson, A. Cell cycle arrest of human gingival fibroblasts and periodontal ligament cells by Actinobacillus actinomycetemcomitans: involvement of the cytolethal distending toxin. Acta Physiol. Microbiol. Immunol. Scand. 2004, 112, 674-685.
9. Lally, E.T.; Hill, R.B; Kieba, I.R.; Korostoff, J. The interaction between RTX toxins and target cells. Trends Microbiol. 1999, 7, 356-361.
10. Linhartová, I.; Bumba, L.; Mašín, J.; Basler, M.; Osička, R.; Kamanová, J.; Procházková, K.; Adkins, I.; Hejnová-Holubová, J.; Sadílková, L.; Morová, J.; Šebo, P. RTX proteins: a highly diverse family secreted by a common mechanism. FEMS Microbiol. Rev. 2010, 34, 1076-1112.
11. Kachlany, S.C. Aggregatibacter actinomycetemcomitans leukotoxin: from threat to therapy. J. Dent. Res. 2010, 89, 561-570.
12. Zambon, J.J.; Slots, J.; Genco, R.J. Serology of oral Actinobacillus actinomycetemcomitans and serotype distribution in human periodontal disease. Infect. Immun. 1983, 41, 19-27.
13. Brogan, J.M.; Lally, E.T.; Poulsen, K.; Kilian, M.; Demuth, D.R. Regulation of Actinobacillus actinomycetemcomitans leukotoxin expression: Analysis of the promoter regions of leukotoxic and minimally leukotoxic strains. Infect. Immun. 1994, 62, 501-508.
14. He, T.; Nishihara, T.; Demuth, D.R.; Ishikawa, I. A novel insertion sequence increases the expression of leukotoxicity in Actinobacillus actinomycetemcomitans clinical isolates. J. Periodontol. 1999, 70, 1261-1268.
15. Johansson, A.; Hänström, L.; Kalfas, S. Inhibition of Actinobacillus actinomycetemcomitans leukotoxicity by bacteria from the subgingival flora. Oral Microbiol. Immunol. 2000, 15, 218-225.
16. Haubek, D.; Ennibi, O.K.; Poulsen, K.; Vaeth, M.; Poulsen, S.; Kilian, M. Risk of aggressive periodontitis in adolescent carriers of the JP2 clone of Aggregatibacter (Actinobacillus) actinomycetemcomitans in Morocco: a perspective longitudinal cohort study. Lancet 2008, 371, 237-242.
17. Claesson, R.; Lagervall, M.; Höglund-Aberg, C.; Johansson, A.; Haubek, D. Detection of the highly leucotoxic JP2 clone of Aggregatibacter actinomycetemcomitans in members of a Caucasian family living in Sweden. J. Clin. Periodontol. 2011, 38, 115-121.
18. Haubek, D.; Poulsen, K.; Kilian, M. Microevolution and patterns of dissemination of the JP2 clone of Aggregatibacter (Actinobacillus) actinomycetemcomitans. Infect. Immun. 2007, 75, 3080-3088.
19. Pasteurellaceae: Biology, Genomics and Molecular Aspects; Kuhnert, P., Christensen, H., Eds.; Caister Academic Press: Norfolk, UK, 2008.
20. Crosby, J.A.; Kachlany, S.C. TdeA, a TolC-like protein required for toxin and drug export in Aggregatibacter (Actinobacillus) actinomycetemcomitans. Gene 2007, 388, 83-92.
21. Gallant, C.V.; Sedic, M.; Chicoine, E.A.; Ruiz, T.; Mintz, K.P. Membrane morphology and leukotoxin secretion are associated with a novel membrane protein of Aggregatibacter actinomycetemcomitans. J. Bacteriol. 2008, 190, 5972-5980.
22. Berthold, P.; Forti, D.; Kieba, I.R.; Rosenbloom, J.; Taichman, N.S.; Lally, E.T. Electron immunocytochemical localization of Actinobacillus actinomycetemcomitans leukotoxin. Oral Microbiol. Immunol. 1992, 7, 24-27.
23. Kato, S.; Kowashi, Y.; Demuth, D.R. Outer membrane-like vesicles secreted by Actinobacillus actinomycetemcomitans are enriched in leukotoxin. Microb. Pathog. 2002, 32, 1-13.
24. Lally, E.T.; Golub, E.E.; Kieba, I.R.; Taichman, N.S.; Rosenbloom, J.; Rosenbloom, J.C.; Gibson, C.W.; Demuth, D.R. Analysis of the Actinobacillus actinomycetemcomitans leukotoxin gene. Delineation of unique features and comparison to homologous toxins. J. Biol. Chem. 1989, 264, 15451-15456.
25. Ohta, H.; Kato, K.; Kokeguchi, S.; Hara, H.; Fukui, K.; Murayama, Y. Nuclease-sensitive binding of an Actinobacillus actinomycetemcomitans leukotoxin to the bacterial cell surface. Infect. Immun. 1991, 59, 4599-4605.
26. Ohta, H.; Hara, H.; Fukui, K.; Kurihara, H.; Murayama, Y.; Kato, K. Association of Actinobacillus actinomycetemcomitans leukotoxin with nucleic acids on the bacterial cell surface. Infect. Immun. 1993, 61, 4878-4884.
27. Johansson, A.; Claesson, R.; Hänström, L.; Kalfas, S. Serum-mediated release of leukotoxin from the cell surface of the periodontal pathogen Actinobacillus actinomycetemcomitans. Eur. J. Oral Sci. 2003, 111, 209-215.
28. Kachlany, S.C.; Fine, D.H.; Figurski, D.H. Secretion of RTX leukotoxin by Actinobacillus actinomycetemcomitans. Infect. Immun. 2000, 68, 6094-6100.
29. Brage, M.; Holmlund, A.; Johansson, A. Humoral immune response to Aggregatibacter actinomycetemcomitans leukotoxin. J. Periodontal Res. 2011, 46, 170-175.
30. Johansson, A.; Claesson, R.; Hänström, L.; Sandström, G.; Kalfas, S. Polymorphonuclear leukocyte degranulation induced by leukotoxin from Actinobacillus actinomycetemcomitans. J. Periodontal Res. 2000, 35, 85-92.
31. Johansson, A.; Claesson, R.; Belibasakis, G.; Makoveichuk, E.; Hänström, L.; Olivecrona, G.; Sandström, G.; Kalfas, S. Protease inhibitors, the responsible components for the serum-dependent enhancement of Actinobacillus actinomycetemcomitans leukotoxicity. Eur. J. Oral Sci. 2001, 109, 335-341.
32. Balashova, N.V.; Park, D.H.; Patel, J.K.; Figurski, D.H.; Kachlany, S.C. Interaction between leukotoxin and Cu, Zn superoxide dismutase in Aggregatibacter actinomycetemcomitans. Infect. Immun. 2007, 75, 4490-4497.
33. de Haar, S.F.; Hiemstra, P.S.; van Steenbergen, M.T.; Everts, V.; Beertsen, W. Role of polymorphonuclear leukocyte-derived serine proteinases in defense against Actinobacillus actinomycetemcomitans. Infect. Immun. 2006, 74, 5284-5291.
34. McArthur, W.P.; Tsai, C.C.; Baehni, P.C.; Genco, R.J.; Taichman, N.S. Leukotoxic effects of Actinobacillus actinomycetemcomitans. Modulation by serum components. J. Periodontal Res. 1981, 16, 159-170.
35. Kraig, E.; Dailey, T.; Kolodrubetz, D. Nucleotide sequence of the leukotoxin gene from Actinobacillus actinomycetemcomitans: homology to the alpha-hemolysin/leukotoxin gene family. Infect. Immun. 1990, 58, 920-929.
36. Lally, E.T.; Kieba, I.R; Golub, E.E.; Lear, J.D.; Tanaka, J.C. Structure/function Aspects of Actinobacillus actinomycetemcomitans leukotoxin. J. Periodontol. 1996, 67, 298-308.
37. Welch, R.A. RTX toxin structure and function: a story of numerous anomalies and few analogies in toxin biology. Curr. Top. Microbiol. Immunol. 2001, 257, 85-111.
38. Balashova, N.V.; Shah, C.; Patel, J.K.; Megalla, S.; Kachlany, S.C. Aggregatibacter actinomycetemcomitans LtxC is required for leukotoxin activity and initial interaction between toxin and host cells. Gene 2009, 443, 42-47.
39. Stanley, P.; Packman, L.C.; Koronakis, V.; Hughes, C. Fatty acylation of two internal lysine residues required for the toxic activity of Escherichia coli hemolysin. Science 1994, 266, 1992-1996.
40. Lally, E.T.; Golub, E.E.; Kieba, I.R. Identification and immunological characterization of the domain of Actinobacillus actinomycetemcomitans leukotoxin that determines its specificity for human target cells. J. Biol. Chem. 1994, 269, 31289-31295.
41. Lally, E.T.; Kieba, I.R.; Sato, A.; Green, C.L.; Rosenbloom, J.; Korostoff, J.; Wang, J.F.; Shenker, B.J.; Ortlepp, S.; Robinson, M.K. et al. RTX toxins recognize a beta2 integrin on the surface of human target cells. J. Biol. Chem. 1997, 272, 30463-30469.
42. 2+ on the binding of Actinobacillus actinomycetemcomitans leukotoxin and the cytotoxicity to promyelocytic leukemia HL-60 cells. Biochem. Mol. Biol. Int. 1993, 29, 899-905.
43. Lear, J.D.; Karakelian, D.; Furblur, U.; Lally, E.T.; Tanaka, J.C. Conformational studies of Actinobacillus actinomycetemcomitans leukotoxin: partial denaturation enhances toxicity. Biochim. Biophys. Acta 2000, 1476, 350-362.
44. Chen, C.; Kittichotirat, W.; Si, Y.; Bumgarner, R. Genome sequence of Aggregatibacter actinomycetemcomitans serotype c strain D11S-1. J. Bacteriol. 2009, 191, 7378-7379.
45. Dileepan, T.; Kachlany, S.C.; Balashova, N.V.; Patel, J.; Maheswaran, S.K. Human CD18 is the functional receptor for Aggregatibacter actinomycetemcomitans leukotoxin. Infect. Immun. 2007, 75, 4851-4856.
46. Kieba, I.R.; Fong, K.P.; Tang, H.Y.; Hoffman, K.E.; Speicher, D.W.; Klickstein, L.B.; Lally, E.T. Aggregatibacter actinomycetemcomitans leukotoxin requires beta-sheets 1 and 2 of the human CD11a beta-propeller for cytotoxicity. Cell. Microbiol. 2007, 9, 2689-2699.
47. Fong, K.P.; Pacheco, C.M.; Otis, L.L.; Baranwal, S.; Kieba, I.R.; Harrison, G.; Hersh, E.V.; Boesze-Battaglia, K.; Lally, E.T. Actinobacillus actinomycetemcomitans leukotoxin requires lipid microdomains for target cell cytotoxicity. Cell. Microbiol. 2006, 8, 1753-1767.
48. Dustin, M.L.; Bivona, T.G.; Philips, M.R. Membranes as messengers in T cell adhesion signaling. Nat. Immunol. 2004, 5, 363-372.
49. Shimaoka, M.; Xiao, T.; Liu, J.H.; Yang, Y.; Dong, Y.; Jun, C.D.; McCormack, A.; Zhang, R.; Joachimiak, A.; Takagi, J. et al. Structures of the alpha L I domain and its complex with ICAM-1 reveal a shape-shifting pathway for integrin regulation. Cell 2003, 112, 99-111.
50. Baehni, P.; Tsai, C.C.; McArthur, W.P.; Hammond, B.F.; Taichman, N.S. Interaction of inflammatory cells and oral microorganisms. VIII. Detection of leukotoxic activity of a plaque-derived gram-negative microorganism. Infect. Immun. 1979, 24, 233-243.
51. Tsai, C.C.; McArthur, W.P.; Baehni, P.C.; Hammond, B.F.; Taichman, N.S. Extraction and partial characterization of a leukotoxin from a plaque-derived Gram-negative microorganism. Infect. Immun. 1979, 25, 427-439.
52. Taichman, N.S.; Dean, R.T.; Sanderson, C.J. Biochemical and morphological characterization of the killing of human monocytes by a leukotoxin derived from Actinobacillus actinomycetemcomitans. Infect. Immun. 1980, 28, 258-268.
53. Mangan, D.F.; Taichman, N.S.; Lally, E.T.; Wahl, S.M. Lethal effects of Actinobacillus actinomycetemcomitans leukotoxin on human T lymphocytes. Infect. Immun. 1991, 59, 3267-3272.
54. Balashova, N.V.; Crosby, J.A.; Al Ghofaily, L.; Kachlany, S.C. Leukotoxin confers beta-hemolytic activity to Actinobacillus actinomycetemcomitans. Infect. Immun. 2006, 74, 2015-2021.
55. Kantarci, A.; van Dyke, T.E. Resolution of inflammation in periodontitis. J. Periodontol. 2005,76, 2168-2174.
56. Kantarci, A.M.; Oyaizu, K.; van Dyke, T.E. Neutrophil-mediated tissue injury in periodontal disease pathogenesis: findings from localized aggressive periodontitis. J. Periodontol. 2003, 74, 66-75.
57. Lamster, I.B.; Novak, M.J. Host mediators in gingival crevicular fluid: implications for the pathogenesis of periodontal disease. Crit. Rev. Oral Biol. Med. 1992, 3, 31-60.
58. Johansson, A.; Sandström, G.; Claesson, R.; Hanström, L.; Kalfas, S. Anaerobic neutrophil-dependent killing of Actinobacillus actinomycetemcomitans in relation to the bacterial leukotoxicity. Eur. J. Oral Sci. 2000, 108, 136-146.
59. Carlsson, G.; Wahlin, Y.B.; Johansson, A.; Olsson, A.; Eriksson, T.; Claesson, R.; Hänström, L.; Henter, J.I. Periodontal disease in patients from the original Kostmann family with severe congenital neutropenia. J. Periodontol. 2006, 77, 744-751.
60. Claesson, R.; Johansson, A.; Belibasakis, G.; Hanström, L.; Kalfas, S. Release and activation of matrix metalloproteinase 8 from human neutrophils triggered by the leukotoxin of Actinobacillus actinomycetemcomitans. J. Periodontal Res. 2002, 37, 353-359.
61. Pütsep, K.; Carlsson, G.; Boman, H.G.; Andersson, M. Deficiency of antibacterial peptides in patients with morbus Kostmann: an observation study. Lancet 2002, 360, 1144-1149.
62. Simpson, D.L.; Berthold, P.; Taichman, N.S. Killing of human myelomonocytic leukemia and lymphocytic cell lines by Actinobacillus actinomycetemcomitans leukotoxin. Infect. Immun. 1988, 56, 1162-1166.
63. Rabie, G.; Lally, E.T.; Shenker, B.J. Immunosuppressive properties of Actinobacillus actinomycetemcomitans leukotoxin. Infect. Immun. 1988, 56, 122-127.
64. Shenker, B.J.; Vitale, L.A.; Keiba, I.; Harrison, G.; Berthold, P.; Golub, E.; Lally, E.T. Flow cytometric analysis of the cytotoxic effects of Actinobacillus actinomycetemcomitans leukotoxin on human natural killer cells. J. Leukoc. Biol. 1994, 55, 153-160.
65. Kelk, P.; Johansson, A.; Claesson, R.; Hanstrom, L.; Kalfas, S. Caspase 1 involvement in human monocyte lysis induced by Actinobacillus actinomycetemcomitans leukotoxin. Infect. Immun. 2003, 71, 4448-4455.
66. Korostoff, J.; Wang, J.F.; Kieba, I.; Miller, M.; Shenker, B.J.; Lally, E.T. Actinobacillus actinomycetemcomitans leukotoxin induces apoptosis in HL-60 cells. Infect. Immun. 1998, 66, 4474-4483.
67. Kinane, D.F.; Lappin, D.F. Immune processes in periodontal disease: a review. Ann. Periodontol. 2002, 7, 62-71.
68. Ohlrich, E.; Cullinan, M.; Seymour, G. The immunopathogenesis of periodontal disease. Aust. Dent. J. 2009, 54, S2-S10.
69. Garlet, G.P. Destructive and protective roles of cytokines in periodontitis: a re-appraisal from host defense and tissue destruction viewpoints. J. Dent. Res. 2010, 89, 1349-1363.
70. Califano, J.V.; Pace, B.E.; Gunsolley, J.C.; Schenkein, H.A.; Lally, E.T.; Tew, J.G. Antibody reactive with Actinobacillus actinomycetemcomitans leukotoxin in early-onset periodontitis patients. Oral Microbiol. Immunol. 1997, 12, 20-26.
71. Dinarello, C.A. Immunological and inflammatory functions of the interleukin-1 family. Annu. Rev. Immunol. 2009, 27, 519-550.
72. Dinarello, C.A. Anti-inflammatory Agents: Present and Future. Cell 2010, 140, 935-950.
73. Latz, E. The inflammasomes: mechanisms of activation and function. Curr. Opin. Immunol. 2010, 22, 28-33.
74. Kelk, P.; Abd, H.; Claesson, R.; Sandström, G.; Sjöstedt, A.; Johansson, A. Cellular and molecular response of human macrophages exposed to Aggregatibacter actinomycetemcomitans leukotoxin. Cell Death Dis. 2011, 2, e126.
75. Miao, E.A.; Leaf, I.A.; Treuting, P.M.; Mao, D.P.; Dors, M.; Sarkar, A.; Warren, S.E.; Wewers, M.D.; Aderem, A. Caspase-1-induced pyroptosis is an innate immune effector mechanism against intracellular bacteria. Nat. Immunol. 2010, 11, 1136-1142.
76. Kelk, P.; Claesson, R.; Hanstrom, L.; Lerner, U.H.; Kalfas, S.; Johansson, A. Abundant secretion of bioactive interleukin-1beta by human macrophages induced by Actinobacillus actinomycetemcomitans leukotoxin. Infect. Immun. 2005, 73, 453-458.
77. Kelk, P.; Claesson, R.; Chen, C.; Sjostedt, A.; Johansson, A. IL-1beta secretion induced by Aggregatibacter (Actinobacillus) actinomycetemcomitans is mainly caused by the leukotoxin. Int. J. Med. Microbiol. 2008, 298, 529-541.
78. Geissmann, F.; Manz, M.G.; Jung, S.; Sieweke, M.H.; Merad, M.; Ley, K. Development of monocytes, macrophages, and dendritic cells. Science 2010, 327, 656-661.
79. Dinarello, C.A. Interleukin-1beta and the autoinflammatory diseases. N. Engl. J. Med. 2009, 360, 2467-2470.
80. Kimizuka, R.; Miura, T.; Okuda, K. Characterization of Actinobacillus actinomycetemcomitans hemolysin. Microbiol. Immunol. 1996, 40, 717-723.
81. Haubek, D.; Dirienzo, J.M.; Tinoco, E.M.; Westergaard, J.; López, N.J.; Chung, C.P.; Poulsen, K.; Kilian, M. Racial tropism of a highly toxic clone of Actinobacillus actinomycetemcomitans associated with juvenile periodontitis. J. Clin. Microbiol. 1997, 35, 3037-3042.
82. Ebersole, J.L. Humoral immune responses in gingival crevice fluid: local and systemic implications. Periodontol. 2000 2003, 31, 135-166.
83. Taubman, M.A.; Valverde, P.; Han, X.; Kawai, T. Immune response: the key to bone resorption in periodontal disease. J. Periodontol. 2005, 76, 2033-2041.
84. Teng, Y.T. The role of acquired immunity and periodontal disease progression. Crit. Rev. Oral Biol. Med. 2003, 14, 237-252.
85. Källestål, C.; Matsson, L.; Persson, S. Proximal attachment loss in Swedish adolescents. J. Clin. Periodontol. 1991, 18, 760-765.
86. Sjödin, B.; Arnrup, K.; Matsson, L.; Wranne, L.; Carlsson, J.; Hänström, L. Periodontal and systemic findings in children with marginal bone loss in the primary dentition. J. Clin. Periodontol. 1995, 22, 214-224.
87. Johansson, A.; Eriksson, M.; Åhrén, A.-M.; Boman, K.; Jansson, J.H.; Hallmans, G.; Johansson, I. Prevalence of systemic immunoreactivity to Aggregatibacter actinomycetemcomitans leukotoxin in relation to the incidence of myocardial infarction. BMC Infect. Dis. 2011, 11, 55.
88. Johansson, A.; Johansson, I.; Eriksson, M.; Ahrén, A.M.; Hallmans, G., Stegmayr, B. Systemic antibodies to the leukotoxin of the oral pathogen Actinobacillus actinomycetemcomitans correlate negatively with stroke in women. Cerebrovasc. Dis. 2005, 20, 226-232.
89. Deas, D.E.; Mealey, B.L. Response of chronic and aggressive periodontitis to treatment. Periodontol. 2000 2010, 53, 154-166.