Corynebacterium diphtheriae 67-72p hemagglutinin, characterized as the protein DIP0733, contributes to invasion and induction of apoptosis in HEp-2 cells

Sabbadini PS, Assis MC, Trost E, Gomes DLR, Moreira LO, Dos Santos CS, Pereira GA, Nagao PE, Azevedo VA de C, Hirata Junior R, Dos Santos ALS, et al. (2012)
Microbial Pathogenesis 52(3): 165-176.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
 
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Autor*in
Sabbadini, Priscila Soares; Assis, Maria Cristina; Trost, EvaUniBi ; Gomes, Debora Leandro Rama; Moreira, Lilian Oliveira; Dos Santos, Cintia Silva; Pereira, Gabriela Andrade; Nagao, Prescilla Emy; Azevedo, Vasco Ariston de Carvalho; Hirata Junior, Raphael; Dos Santos, Andre Luis Souza; Tauch, AndreasUniBi
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Abstract / Bemerkung
Although Corynebacterium diphtheriae has been classically described as an exclusively extracellular pathogen, there is growing evidence that it may be internalized by epithelial cells. The aim of the present report was to investigate the nature and involvement of the surface-exposed non-fimbrial 67-72kDa proteins (67-72p), previously characterized as adhesin/hemagglutinin, in C.diphtheriae internalization by HEp-2 cells. Transmission electron microscopy and bacterial internalization inhibition assays indicated the role of 67-72p as invasin for strains of varied sources. Cytoskeletal changes with accumulation of polymerized actin in HEp-2 cells beneath adherent 67-72p-adsorbed microspheres were observed by the Fluorescent actin staining test. Trypan blue staining method and Methylthiazole tetrazolium reduction assay showed a significant decrease in viability of HEp-2 cells treated with 67-72p. Morphological changes in HEp-2 cells observed after treatment with 67-72p included vacuolization, nuclear fragmentation and the formation of apoptotic bodies. Flow cytometry revealed an apoptotic volume decrease in HEp-2 cells treated with 67-72p. Moreover, a double-staining assay using Propidium Iodide/Annexin V gave information about the numbers of vital vs. early apoptotic cells and late apoptotic or secondary necrotic cells. The comparative analysis of MALDI-TOF MS experiments with the probes provided for 67-72p CDC-E8392 with an in silico proteome deduced from the complete genome sequence of C.diphtheriae identified with significant scores 67-72p as the protein DIP0733. In conclusion, DIP0733 (67-72p) may be directly implicated in bacterial invasion and apoptosis of epithelial cells in the early stages of diphtheria and C.diphtheriae invasive infection. Copyright 2011 Elsevier Ltd. All rights reserved.
Erscheinungsjahr
2012
Zeitschriftentitel
Microbial Pathogenesis
Band
52
Ausgabe
3
Seite(n)
165-176
ISSN
0882-4010
Page URI
https://pub.uni-bielefeld.de/record/2471667

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Sabbadini PS, Assis MC, Trost E, et al. Corynebacterium diphtheriae 67-72p hemagglutinin, characterized as the protein DIP0733, contributes to invasion and induction of apoptosis in HEp-2 cells. Microbial Pathogenesis. 2012;52(3):165-176.
Sabbadini, P. S., Assis, M. C., Trost, E., Gomes, D. L. R., Moreira, L. O., Dos Santos, C. S., Pereira, G. A., et al. (2012). Corynebacterium diphtheriae 67-72p hemagglutinin, characterized as the protein DIP0733, contributes to invasion and induction of apoptosis in HEp-2 cells. Microbial Pathogenesis, 52(3), 165-176. doi:10.1016/j.micpath.2011.12.003
Sabbadini, P. S., Assis, M. C., Trost, E., Gomes, D. L. R., Moreira, L. O., Dos Santos, C. S., Pereira, G. A., Nagao, P. E., Azevedo, V. A. de C., Hirata Junior, R., et al. (2012). Corynebacterium diphtheriae 67-72p hemagglutinin, characterized as the protein DIP0733, contributes to invasion and induction of apoptosis in HEp-2 cells. Microbial Pathogenesis 52, 165-176.
Sabbadini, P.S., et al., 2012. Corynebacterium diphtheriae 67-72p hemagglutinin, characterized as the protein DIP0733, contributes to invasion and induction of apoptosis in HEp-2 cells. Microbial Pathogenesis, 52(3), p 165-176.
P.S. Sabbadini, et al., “Corynebacterium diphtheriae 67-72p hemagglutinin, characterized as the protein DIP0733, contributes to invasion and induction of apoptosis in HEp-2 cells”, Microbial Pathogenesis, vol. 52, 2012, pp. 165-176.
Sabbadini, P.S., Assis, M.C., Trost, E., Gomes, D.L.R., Moreira, L.O., Dos Santos, C.S., Pereira, G.A., Nagao, P.E., Azevedo, V.A. de C., Hirata Junior, R., Dos Santos, A.L.S., Tauch, A., Mattos-Guaraldi, A.L.: Corynebacterium diphtheriae 67-72p hemagglutinin, characterized as the protein DIP0733, contributes to invasion and induction of apoptosis in HEp-2 cells. Microbial Pathogenesis. 52, 165-176 (2012).
Sabbadini, Priscila Soares, Assis, Maria Cristina, Trost, Eva, Gomes, Debora Leandro Rama, Moreira, Lilian Oliveira, Dos Santos, Cintia Silva, Pereira, Gabriela Andrade, Nagao, Prescilla Emy, Azevedo, Vasco Ariston de Carvalho, Hirata Junior, Raphael, Dos Santos, Andre Luis Souza, Tauch, Andreas, and Mattos-Guaraldi, Ana Luiza. “Corynebacterium diphtheriae 67-72p hemagglutinin, characterized as the protein DIP0733, contributes to invasion and induction of apoptosis in HEp-2 cells”. Microbial Pathogenesis 52.3 (2012): 165-176.

12 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Adhesion properties of toxigenic corynebacteria.
Ott L., AIMS Microbiol 4(1), 2018
PMID: 31294205
The C-terminal coiled-coil domain of Corynebacterium diphtheriae DIP0733 is crucial for interaction with epithelial cells and pathogenicity in invertebrate animal model systems.
Weerasekera D, Stengel F, Sticht H, de Mattos Guaraldi AL, Burkovski A, Azevedo Antunes C., BMC Microbiol 18(1), 2018
PMID: 30180805
Analysis of Corynebacterium diphtheriae macrophage interaction: Dispensability of corynomycolic acids for inhibition of phagolysosome maturation and identification of a new gene involved in synthesis of the corynomycolic acid layer.
Ott L, Hacker E, Kunert T, Karrington I, Etschel P, Lang R, Wiesmann V, Wittenberg T, Singh A, Varela C, Bhatt A, Sangal V, Burkovski A., PLoS One 12(7), 2017
PMID: 28686600
Reactive oxygen species involved in apoptosis induction of human respiratory epithelial (A549) cells by Streptococcus agalactiae.
da Costa AF, Moraes JA, de Oliveira JS, dos Santos MH, Santos Gda S, Barja-Fidalgo C, Mattos-Guaraldi AL, Nagao PE., Microbiology 162(1), 2016
PMID: 26490153
A novel experimental platform for toxigenic and non-toxigenic Corynebacterium ulcerans infection in mice.
Mochizuki Y, Saeki H, Iwaki M, Takagi H, Shibayama K, Amao H, Yamamoto A., Pathog Dis 74(2), 2016
PMID: 26607400
Corynebacterium ulcerans, an emerging human pathogen.
Hacker E, Antunes CA, Mattos-Guaraldi AL, Burkovski A, Tauch A., Future Microbiol 11(), 2016
PMID: 27545005
Pathogenic properties of a Corynebacterium diphtheriae strain isolated from a case of osteomyelitis.
Peixoto RS, Hacker E, Antunes CA, Weerasekera D, Dias AA, Martins CA, Hirata R, Santos KR, Burkovski A, Mattos-Guaraldi AL., J Med Microbiol 65(11), 2016
PMID: 27902402
Adherence and invasive properties of Corynebacterium diphtheriae strains correlates with the predicted membrane-associated and secreted proteome.
Sangal V, Blom J, Sutcliffe IC, von Hunolstein C, Burkovski A, Hoskisson PA., BMC Genomics 16(), 2015
PMID: 26452736
Induction of the NFκ-B signal transduction pathway in response to Corynebacterium diphtheriae infection.
Ott L, Scholz B, Höller M, Hasselt K, Ensser A, Burkovski A., Microbiology 159(pt 1), 2013
PMID: 23125120
SubMICs of penicillin and erythromycin enhance biofilm formation and hydrophobicity of Corynebacterium diphtheriae strains.
Gomes DL, Peixoto RS, Barbosa EA, Napoleão F, Sabbadini PS, dos Santos KR, Mattos-Guaraldi AL, Hirata R., J Med Microbiol 62(pt 5), 2013
PMID: 23449875

59 References

Daten bereitgestellt von Europe PubMed Central.

The changing epidemiology of diphtheria in the vaccine era
Galazka, J Infect Dis 181(), 2000
Resurgence of diphtheria in the vaccination era.
Khan N, Shastri J, Aigal U, Doctor B., Indian J Med Microbiol 25(4), 2007
PMID: 18087111
Molecular epidemiology of diphtheria in Russia, 1985–1994
Popovic, J Infect Dis 174(), 1996
Successful control of epidemic diphtheria in the State of the former Union of Soviet Socialist Republics: lessons learned
Dittman, J Infect Dis 181(), 2000
Resurgence of diphtheria in India in the 21st century.
Jacob John T., Indian J. Med. Res. 128(5), 2008
PMID: 19179691
Clinical and molecular study of Corynebacterium diphtheriae systemic infections in France. Coryne Study Group
Patey, J Clin Microbiol 35(), 1997
Emergence of an invasive clone of nontoxigenic Corynebacterium diphtheriae in the urban poor population of Vancouver, Canada
Romney, J Clin Microbiol 44(), 2006
Potential pathogenic role of aggregative-adhering Corynebacterium diphtheriae of different clonal groups in endocarditis.
Hirata R Jr, Pereira GA, Filardy AA, Gomes DL, Damasco PV, Rosa AC, Nagao PE, Pimenta FP, Mattos-Guaraldi AL., Braz. J. Med. Biol. Res. 41(11), 2008
PMID: 19099151
Corynebacterium diphtheriae threats in cancer patients.
Mattos-Guaraldi AL, Formiga LC, Camello TC, Pereira GA, Hirata R Jr, Halpern M., Rev. Argent. Microbiol. 33(2), 2001
PMID: 11494762
Corynebacterium diphtheriae as an emerging pathogen in nephrostomy catheter-related infection: evaluation of traits associated with bacterial virulence
Gomes, J Med Microbiol 58(), 2009
Bacterial adherence.
Ofek I, Beachey EH., Adv Intern Med 25(), 1980
PMID: 6987850
Internalization of non-toxigenic Corynebacterium diphtheriae by cultured human respiratory epithelial cells.
Bertuccini L, Baldassarri L, von Hunolstein C., Microb. Pathog. 37(3), 2004
PMID: 15351033
Intracellular viability of toxigenic Corynebacterium diphtheriae strains in HEp-2 cells.
Hirata R, Napoleao F, Monteiro-Leal LH, Andrade AF, Nagao PE, Formiga LC, Fonseca LS, Mattos-Guaraldi AL., FEMS Microbiol. Lett. 215(1), 2002
PMID: 12393210
Technetium-99m labeling and fibronectin binding ability of Corynebacterium diphtheriae
Souza, Rev Bras Eng Biomed 20(), 2004
Corynebacterium diphtheriae surface proteins as adhesins to human erythrocytes.
Colombo AV, Hirata R Jr, de Souza CM, Monteiro-Leal LH, Previato JO, Formiga LC, Andrade AF, Mattos-Guaraldi AL., FEMS Microbiol. Lett. 197(2), 2001
PMID: 11313140
Patterns of adherence to HEp-2 cells and actin polymerisation by toxigenic Corynebacterium diphtheriae strains.
Hirata R Jr, Souza SM, Rocha-de-Souza CM, Andrade AF, Monteiro-Leal LH, Formiga LC, Mattos-Guaraldi AL., Microb. Pathog. 36(3), 2004
PMID: 14726229
Corynebacterium diphtheriae employs specific minor pilins to target human pharyngeal epithelial cells.
Mandlik A, Swierczynski A, Das A, Ton-That H., Mol. Microbiol. 64(1), 2007
PMID: 17376076
Adhesins and invasins of pathogenic bacteria: a structural view.
Niemann HH, Schubert WD, Heinz DW., Microbes Infect. 6(1), 2004
PMID: 14738899
Extracellular adherence protein from Staphylococcus aureus enhances internalization into eukaryotic cells.
Haggar A, Hussain M, Lonnies H, Herrmann M, Norrby-Teglund A, Flock JI., Infect. Immun. 71(5), 2003
PMID: 12704099
Invasion of epithelial mammalian cells by Paracoccidioides brasiliensis leads to cytoskeletal rearrangement and apoptosis of the host cell.
Mendes-Giannini MJ, Hanna SA, da Silva JL, Andreotti PF, Vincenzi LR, Benard G, Lenzi HL, Soares CP., Microbes Infect. 6(10), 2004
PMID: 15310464
Group A Streptococcus induces apoptosis in human epithelial cells.
Tsai PJ, Lin YS, Kuo CF, Lei HY, Wu JJ., Infect. Immun. 67(9), 1999
PMID: 10456871
Outer membrane protein 38 of Acinetobacter baumannii localizes to the mitochondria and induces apoptosis of epithelial cells.
Choi CH, Lee EY, Lee YC, Park TI, Kim HJ, Hyun SH, Kim SA, Lee SK, Lee JC., Cell. Microbiol. 7(8), 2005
PMID: 16008580
Internalization of Staphylococcus aureus by endothelial cells induces apoptosis.
Menzies BE, Kourteva I., Infect. Immun. 66(12), 1998
PMID: 9826383
Staphylococcus aureus RN6390 replicates and induces apoptosis in a pulmonary epithelial cell line.
Kahl BC, Goulian M, van Wamel W, Herrmann M, Simon SM, Kaplan G, Peters G, Cheung AL., Infect. Immun. 68(9), 2000
PMID: 10948168
Apoptosis induced by Staphylococcus aureus in epithelial cells utilizes a mechanism involving caspases 8 and 3.
Wesson CA, Deringer J, Liou LE, Bayles KW, Bohach GA, Trumble WR., Infect. Immun. 68(5), 2000
PMID: 10769002
Fate of Streptococcus pyogenes and epithelial cells following internalization
Marouni, J Med Microbiol 53(), 2004
Apoptosis in bacterial pathogenesis
Zychlinsky, J Clin Invest 100(), 1997
Non-opsonic phagocytosis of homologous non-toxigenic and toxigenic Corynebacterium diphtheriae strains by human U-937 macrophages.
dos Santos CS, dos Santos LS, de Souza MC, dos Santos Dourado F, de Souza de Oliveira Dias AA, Sabbadini PS, Pereira GA, Cabral MC, Hirata Junior R, de Mattos-Guaraldi AL., Microbiol. Immunol. 54(1), 2010
PMID: 20055937
Diphtheria toxin and Pseudomonas A toxin-mediated apoptosis
Morimoto, J Immunol 149(), 1992
Enhancement of diphtheria toxin-induced apoptosis in Vero cells by combination treatment with brefeldin A and okadaic acid.
Kusano I, Kageyama A, Tamura T, Oda T, Muramatsu T., Cell Struct. Funct. 26(5), 2001
PMID: 11831360
Immunotoxins in the treatment of hematologic malignancies.
Kreitman RJ, Pastan I., Curr Drug Targets 7(10), 2006
PMID: 17073592
Pseudomonas aeruginosa induction of apoptosis in respiratory epithelial cells: analysis of the effects of cystic fibrosis transmembrane conductance regulator dysfunction and bacterial virulence factors
Rajan, Am J Resp Cell Mol Biol 23(), 2000
Apoptotic volume decrease and the incredible shrinking cell.
Bortner CD, Cidlowski JA., Cell Death Differ. 9(12), 2002
PMID: 12478467
Flow cytometry of apoptotic cell death
Vermes, J Immunol Methods 243(), 2000
The complete genome sequence and analysis of Corynebacterium diphtheriae NCTC13129.
Cerdeno-Tarraga AM, Efstratiou A, Dover LG, Holden MT, Pallen M, Bentley SD, Besra GS, Churcher C, James KD, De Zoysa A, Chillingworth T, Cronin A, Dowd L, Feltwell T, Hamlin N, Holroyd S, Jagels K, Moule S, Quail MA, Rabbinowitsch E, Rutherford KM, Thomson NR, Unwin L, Whitehead S, Barrell BG, Parkhill J., Nucleic Acids Res. 31(22), 2003
PMID: 14602910
Molecular characterization of Legionella pneumophila-induced interleukin-8 expression in T cells.
Takamatsu R, Teruya H, Takeshima E, Ishikawa C, Matsumoto K, Mukaida N, Li JD, Heuner K, Higa F, Fujita J, Mori N., BMC Microbiol. 10(), 2010
PMID: 20051107
A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples.
Markwell MA, Haas SM, Bieber LL, Tolbert NE., Anal. Biochem. 87(1), 1978
PMID: 98070
Effects of iron limitation on adherence and cell surface carbohydrates of Corynebacterium diphtheriae strains.
Moreira LO, Andrade AF, Vale MD, Souza SM, Hirata R Jr, Asad LM, Asad NR, Monteiro-Leal LH, Previato JO, Mattos-Guaraldi AL., Appl. Environ. Microbiol. 69(10), 2003
PMID: 14532043
Influence of polarisation and differentiation on interaction of 43-kDa outer-membrane protein of Aeromonas caviae with human enterocyte-like Caco-2 cell line.
Rocha-De-Souza CM, Mattos-Guaraldi AL, Hirata R Jr, Moreira LO, Monteiro-Leal LH, Freitas-Almeida AC, Mendonca-Previato L, Previato JO, Andrade AF., Int. J. Mol. Med. 11(5), 2003
PMID: 12684708
Rapid colorimetric assay for cell growth and survival. Modification of the tetrazolium dye procedure giving improved sensibility and reliability
Denizot, J Immunol Methods 89(), 1986
Clinical concentrations of thioridazine kill intracellular multidrug-resistant Mycobacterium tuberculosis.
Ordway D, Viveiros M, Leandro C, Bettencourt R, Almeida J, Martins M, Kristiansen JE, Molnar J, Amaral L., Antimicrob. Agents Chemother. 47(3), 2003
PMID: 12604522
Lipoarabinomannan induced cytotoxic effects in human mononuclear cells.
Ghosh S, Pal S, Das S, Dasgupta SK, Majumdar S., FEMS Immunol. Med. Microbiol. 21(3), 1998
PMID: 9718207
Mouse 24p3 protein has an effect on L929 cell viability.
Li PT, Lee YC, Elangovan N, Chu ST., Int. J. Biol. Sci. 3(2), 2007
PMID: 17304338
Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes
Krogh, J Mol Biol 305(), 2001

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