Cytotoxic effects of Kingella kingae outer membrane vesicles on human cells

Microbial Pathogenesis

Volumn 51, Issue 1-2, 2011, Pages 22-30

  Maldonado, R ^a   Wei, R ^a   Kachlany, S C ^a   Kazi, M ^a   Balashova, N V ^a  

^a RUTGERS SCHOOL OF DENTAL MEDICINE   (United States)

Author keywords

Kingella kingae; Outer membrane vesicles

Indexed keywords

GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 6; MEMBRANE PROTEIN; OUTER MEMBRANE PROTEIN; PROTEIN RTXA; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; BIOMASS; CELL FUNCTION; CELL VIABILITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; HUMAN; HUMAN CELL; IMMUNOREACTIVITY; INTERNALIZATION; KINGELLA KINGAE; MEMBRANE VESICLE; NONHUMAN; OSTEOBLAST; OSTEOCLASTOGENESIS; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; PROTEIN PURIFICATION; PROTEIN SECRETION; SIGNAL TRANSDUCTION; SYNOVIOCYTE;

ANIMALS; ARTHRITIS, INFECTIOUS; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL TOXINS; CELL MEMBRANE; CHILD; CYTOKINES; FIMBRIAE PROTEINS; HUMANS; KINGELLA KINGAE; MICE; OSTEOBLASTS; SYNOVIAL FLUID; VIRULENCE FACTORS;

BACTERIA (MICROORGANISMS); KINGELLA KINGAE; OAT MOSAIC VIRUS;

EID: 79955635247     PISSN: 08824010     EISSN: 10961208     Source Type: Journal    
DOI: 10.1016/j.micpath.2011.03.005     Document Type: Article

References (73)

1. Yagupsky P., Bar-Ziv Y., Howard C.B., Dagan R. Epidemiology, etiology, and clinical features of septic arthritis in children younger than 24 months. Arch Pediatr Adolesc Med 1995, 149:537-540.
2. Yagupsky P., Dagan R., Howard C.B., Einhorn M., Kassis I., Simu A. Clinical features and epidemiology of invasive Kingella kingae infections in southern Israel. Pediatrics 1993, 92:800-804.
3. Yagupsky P., Peled N., Katz O. Epidemiological features of invasive Kingella kingae infections and respiratory carriage of the organism. J Clin Microbiol 2002, 40:4180-4184.
4. Dubnov-Raz G., Ephros M., Garty B.Z., Schlesinger Y., Maayan-Metzger A., Hasson J., et al. Invasive Pediatric Kingella kingae Infections: A Nationwide Collaborative Study. Pediatr Infect Dis J 2010.
5. Yagupsky P. Kingella kingae: from medical rarity to an emerging paediatric pathogen. Lancet Infect Dis 2004, 4:358-367.
6. Ceroni D., Cherkaoui A., Ferey S., Kaelin A., Schrenzel J. Kingella Kingae osteoarticular infections in young children: clinical features and contribution of a new specific real-time PCR assay to the diagnosis. J Pediatr Orthop 2010, 30:301-304.
7. Chometon S., Benito Y., Chaker M., Boisset S., Ploton C., Berard J., et al. Specific real-time polymerase chain reaction places Kingella kingae as the most common cause of osteoarticular infections in young children. Pediatr Infect Dis J 2007, 26:377-381.
8. Gene A., Garcia-Garcia J.J., Sala P., Sierra M., Huguet R. Enhanced culture detection of Kingella kingae, a pathogen of increasing clinical importance in pediatrics. Pediatr Infect Dis J 2004, 23:886-888.
9. Ilharreborde B., Bidet P., Lorrot M., Even J., Mariani-Kurkdjian P., Liguori S., et al. New real-time PCR-based method for Kingella kingae DNA detection: application to samples collected from 89 children with acute arthritis. J Clin Microbiol 2009, 47:1837-1841.
10. Korach A., Olshtain-Pops K., Schwartz D., Moses A. Kingella kingae prosthetic valve endocarditis complicated by a paravalvular abscess. Isr Med Assoc J 2009, 11:251-253.
11. Moumile K., Merckx J., Glorion C., Berche P., Ferroni A. Osteoarticular infections caused by Kingella kingae in children: contribution of polymerase chain reaction to the microbiologic diagnosis. Pediatr Infect Dis J 2003, 22:837-839.
12. Nguyen S., Fayad G., Modine T., Leroy O. Mitral acute bacterial endocarditis caused by HACEK microorganisms. J Heart Valve Dis 2009, 18:353-354.
13. Verdier I., Gayet-Ageron A., Ploton C., Taylor P., Benito Y., Freydiere A.M., et al. Contribution of a broad range polymerase chain reaction to the diagnosis of osteoarticular infections caused by Kingella kingae: description of twenty-four recent pediatric diagnoses. Pediatr Infect Dis J 2005, 24:692-696.
14. 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.
15. Sena A.C., Seed P., Nicholson B., Joyce M., Cunningham C.K. Kingella kingae endocarditis and a cluster investigation among daycare attendees. Pediatr Infect Dis J 2010, 29:86-88.
16. Yagupsky P., Erlich Y., Ariela S., Trefler R., Porat N. Outbreak of Kingella kingae skeletal system infections in children in daycare. Pediatr Infect Dis J 2006, 25:526-532.
17. Kehl-Fie T.E., Miller S.E., St Geme J.W. Kingella kingae expresses type IV pili that mediate adherence to respiratory epithelial and synovial cells. J Bacteriol 2008, 190:7157-7163.
18. Kehl-Fie T.E., Porsch E.A., Miller S.E., St Geme J.W. Expression of Kingella kingae type IV pili is regulated by sigma54, PilS, and PilR. J Bacteriol 2009, 191:4976-4986.
19. Kehl-Fie T.E., Porsch E.A., Yagupsky P., Grass E.A., Obert C., Benjamin D.K., et al. Examination of type IV pilus expression and pilus-associated phenotypes in Kingella kingae clinical isolates. Infect Immun 2010, 78:1692-1699.
20. Kehl-Fie T.E., St Geme J.W. Identification and characterization of an RTX toxin in the emerging pathogen Kingella kingae. J Bacteriol 2007, 189:430-436.
21. Coote J.G. Structural and functional relationships among the RTX toxin determinants of gram-negative bacteria. FEMS Microbiol Rev 1992, 8:137-161.
22. Ludwig A., Jarchau T., Benz R., Goebel W. The repeat domain of Escherichia coli haemolysin (HlyA) is responsible for its Ca2+-dependent binding to erythrocytes. Mol Gen Genet 1988, 214:553-561.
23. Ostolaza H., Soloaga A., Goni F.M. The binding of divalent cations to Escherichia coli alpha-haemolysin. Eur J Biochem 1995, 228:39-44.
24. Kachlany S.C. Aggregatibacter actinomycetemcomitans leukotoxin: from threat to therapy. J Dent Res 2010.
25. Lally E.T., Kieba I.R., Sato A., Green C.L., Rosenbloom J., Korostoff J., et al. RTX toxins recognize a beta2 integrin on the surface of human target cells. J Biol Chem 1997, 272:30463-30469.
26. 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.
27. Benz R., Maier E., Ladant D., Ullmann A., Sebo P. Adenylate cyclase toxin (CyaA) of Bordetella pertussis. Evidence for the formation of small ion-permeable channels and comparison with HlyA of Escherichia coli. J Biol Chem 1994, 269:27231-27239.
28. Forestier C., Welch R.A. Identification of RTX toxin target cell specificity domains by use of hybrid genes. Infect Immun 1991, 59:4212-4220.
29. Hess J.F., Angelos J.A. The Moraxella bovis RTX toxin locus mbx defines a pathogenicity island. J Med Microbiol 2006, 55:443-449.
30. Thompson S.A., Wang L.L., West A., Sparling P.F. Neisseria meningitidis produces iron-regulated proteins related to the RTX family of exoproteins. J Bacteriol 1993, 175:811-818.
31. Kulp A., Kuehn M.J. Biological functions and biogenesis of secreted bacterial outer membrane vesicles. Annu Rev Microbiol 2010, 64:163-184.
32. Unal C.M., Schaar V., Riesbeck K. Bacterial outer membrane vesicles in disease and preventive medicine. Semin Immunopathol 2010.
33. Holst J., Martin D., Arnold R., Huergo C.C., Oster P., O'Hallahan J., et al. Properties and clinical performance of vaccines containing outer membrane vesicles from Neisseria meningitidis. Vaccine 2009, 27(Suppl. 2):B3-12.
34. Jonsson A.B., Rahman M., Normark S. Pilus biogenesis gene, pilC, of Neisseria gonorrhoeae: pilC1 and pilC2 are each part of a larger duplication of the gonococcal genome and share upstream and downstream homologous sequences with opa and pil loci. Microbiology 1995, 141(Pt 10):2367-2377.
35. Dewhirst F.E., Chen C.K., Paster B.J., Zambon J.J. Phylogeny of species in the family Neisseriaceae isolated from human dental plaque and description of Kingella oralis sp. nov [corrected]. Int J Syst Bacteriol 1993, 43:490-499.
36. Perera V.Y., Penn C.W., Smith H. Purification of pili and outer membrane vesicles of Neisseria gonorrhoeae by wheat germ agglutinin affinity chromatography. J Gen Microbiol 1982, 128:1613-1622.
37. Balsalobre C., Silvan J.M., Berglund S., Mizunoe Y., Uhlin B.E., Wai S.N. Release of the type I secreted alpha-haemolysin via outer membrane vesicles from Escherichia coli. Mol Microbiol 2006, 59:99-112.
38. Dutta S., Iida K., Takade A., Meno Y., Nair G.B., Yoshida S. Release of Shiga toxin by membrane vesicles in Shigella dysenteriae serotype 1 strains and in vitro effects of antimicrobials on toxin production and release. Microbiol Immunol 2004, 48:965-969.
39. Fiocca R., Necchi V., Sommi P., Ricci V., Telford J., Cover T.L., et al. Release of helicobacter pylori vacuolating cytotoxin by both a specific secretion pathway and budding of outer membrane vesicles. Uptake of released toxin and vesicles by gastric epithelium. J Pathol 1999, 188:220-226.
40. 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.
41. Lindmark B., Rompikuntal P.K., Vaitkevicius K., Song T., Mizunoe Y., Uhlin B.E., et al. Outer membrane vesicle-mediated release of cytolethal distending toxin (CDT) from Campylobacter jejuni. BMC Microbiol 2009, 9:220.
42. Negrete-Abascal E., Garcia R.M., Reyes M.E., Godinez D., de la Garza M. Membrane vesicles released by Actinobacillus pleuropneumoniae contain proteases and Apx toxins. FEMS Microbiol Lett 2000, 191:109-113.
43. Wensink J., Gankema H., Jansen W.H., Guinee P.A., Witholt B. Isolation of the membranes of an enterotoxigenic strain of Escherichia coli and distribution of enterotoxin activity in different subcellular fractions. Biochim Biophys Acta 1978, 514:128-136.
44. Aldick T., Bielaszewska M., Uhlin B.E., Humpf H.U., Wai S.N., Karch H. Vesicular stabilization and activity augmentation of enterohaemorrhagic Escherichia coli haemolysin. Mol Microbiol 2009, 71:1496-1508.
45. 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.
46. Murphy G.L., Whitworth L.C., Clinkenbeard K.D., Clinkenbeard P.A. Hemolytic activity of the Pasteurella haemolytica leukotoxin. Infect Immun 1995, 63:3209-3212.
47. Vanden Bergh P.G., Zecchinon L.L., Fett T., Desmecht D. Probing of Actinobacillus pleuropneumoniae ApxIIIA toxin-dependent cytotoxicity towards mammalian peripheral blood mononucleated cells. BMC Res Notes 2008, 1:121.
48. Diaz R., Ghofaily L.A., Patel J., Balashova N.V., Freitas A.C., Labib I., et al. Characterization of leukotoxin from a clinical strain of Actinobacillus actinomycetemcomitans. Microb Pathog 2006, 40:48-55.
49. Thompson S.A., Sparling P.F. The RTX cytotoxin-related FrpA protein of Neisseria meningitidis is secreted extracellularly by meningococci and by HlyBD+ Escherichia coli. Infect Immun 1993, 61:2906-2911.
50. Backman M., Kallstrom H., Jonsson A.B. The phase-variable pilus-associated protein PilC is commonly expressed in clinical isolates of Neisseria gonorrhoeae, and shows sequence variability among strains. Microbiology 1998, 144(Pt 1):149-156.
51. Rahman M., Kallstrom H., Normark S., Jonsson A.B. PilC of pathogenic Neisseria is associated with the bacterial cell surface. Mol Microbiol 1997, 25:11-25.
52. Grenier D., Mayrand D. Functional characterization of extracellular vesicles produced by Bacteroides gingivalis. Infect Immun 1987, 55:111-117.
53. Inagaki S., Onishi S., Kuramitsu H.K., Sharma A. Porphyromonas gingivalis vesicles enhance attachment, and the leucine-rich repeat BspA protein is required for invasion of epithelial cells by "Tannerella forsythia" Infect Immun 2006, 74:5023-5028.
54. Parker H., Chitcholtan K., Hampton M.B., Keenan J.I. Uptake of Helicobacter pylori outer membrane vesicles by gastric epithelial cells. Infect Immun 2010, 78:5054-5061.
55. Buck C., Bundschu J., Gallati H., Bartmann P., Pohlandt F. Interleukin-6: a sensitive parameter for the early diagnosis of neonatal bacterial infection. Pediatrics 1994, 93:54-58.
56. Le Moine O., Deviere J., Devaster J.M., Crusiaux A., Durand F., Bernuau J., et al. Interleukin-6: an early marker of bacterial infection in decompensated cirrhosis. J Hepatol 1994, 20:819-824.
57. Schrum L.W., Marriott I., Butler B.R., Thomas E.K., Hudson M.C., Bost K.L. Functional CD40 expression induced following bacterial infection of mouse and human osteoblasts. Infect Immun 2003, 71:1209-1216.
58. de Man P., van Kooten C., Aarden L., Engberg I., Linder H., Svanborg Eden C. Interleukin-6 induced at mucosal surfaces by gram-negative bacterial infection. Infect Immun 1989, 57:3383-3388.
59. Tichomirowa M., Theodoropoulou M., Lohrer P., Schaaf L., Losa M., Uhl E., et al. Bacterial endotoxin (lipopolysaccharide) stimulates interleukin-6 p.oduction and inhibits growth of pituitary tumour cells expressing the toll-like receptor 4. J Neuroendocrinol 2005, 17:152-160.
60. Smith J.B., Bocchieri M.H., Smith J.B., Sherbin-Allen L., Abruzzo J.L. Colony stimulating factor occurs in both inflammatory and noninflammatory synovial fluids. Rheumatol Int 1990, 10:131-134.
61. Katano M., Okamoto K., Arito M., Kawakami Y., Kurokawa M.S., Suematsu N., et al. Implication of granulocyte-macrophage colony-stimulating factor induced neutrophil gelatinase-associated lipocalin in pathogenesis of rheumatoid arthritis revealed by proteome analysis. Arthritis Res Ther 2009, 11:R3.
62. Babior B.M. Oxidants from phagocytes: agents of defense and destruction. Blood 1984, 64:959-966.
63. Smith J.A. Neutrophils, host defense, and inflammation: a double-edged sword. J Leukocyte Biol 1994, 56:672-686.
64. Beaulieu A.D., McColl S.R. Differential expression of two major cytokines produced by neutrophils, interleukin-8 and the interleukin-1 receptor antagonist, in neutrophils isolated from the synovial fluid and peripheral blood of patients with rheumatoid arthritis. Arthritis Rheum 1994, 37:855-859.
65. Konttinen Y.T., Lindy O., Kemppinen P., Saari H., Suomalainen K., Vauhkonen M., et al. Collagenase reserves in polymorphonuclear neutrophil leukocytes from synovial fluid and peripheral blood of patients with rheumatoid arthritis. Matrix 1991, 11:296-301.
66. Hattersley G., Chambers T.J. Effects of interleukin 3 and of granulocyte-macrophage and macrophage colony stimulating factors on osteoclast differentiation from mouse hemopoietic tissue. J Cell Physiol 1990, 142:201-209.
67. Liggett W., Shevde N., Anklesaria P., Sohoni S., Greenberger J., Glowacki J. Effects of macrophage colony stimulating factor and granulocyte-macrophage colony stimulating factor on osteoclastic differentiation of hematopoietic progenitor cells. Stem Cells 1993, 11:398-411.
68. Takahashi N., Udagawa N., Akatsu T., Tanaka H., Shionome M., Suda T. Role of colony-stimulating factors in osteoclast development. J Bone Miner Res 1991, 6:977-985.
69. Bost K.L., Bento J.L., Ellington J.K., Marriott I., Hudson M.C. Induction of colony-stimulating factor expression following Staphylococcus or Salmonella interaction with mouse or human osteoblasts. Infect Immun 2000, 68:5075-5083.
70. Fine D.H., Furgang D., Kaplan J., Charlesworth J., Figurski D.H. Tenacious adhesion of Actinobacillus actinomycetemcomitans strain CU1000 to salivary-coated hydroxyapatite. Arch Oral Biol 1999, 44:1063-1076.
71. 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.
72. Kim K.J., Kanellopoulos-Langevin C., Merwin R.M., Sachs D.H., Asofsky R. Establishment and characterization of BALB/c lymphoma lines with B cell properties. J Immunol 1979, 122:549-554.
73. Barenkamp S.J., Munson R.S., Granoff D.M. Subtyping isolates of Haemophilus influenzae type b by outer-membrane protein profiles. J Infect Dis 1981, 143:668-676.