1887

Abstract

-acetylglucosamine-binding protein GbpA is a secretory protein that facilitates the initial adherence of bacteria in the human intestine. Until now, considerable progress in the characterization of GbpA has been done, yet little is known about its role in host response. Our present studies demonstrated that GbpA at the amount secreted in the intestine resulted in decreased cell viability, altered cell morphology, disruption of cell membrane integrity and damage of cellular DNA indicating necrotic cell death. We observed that GbpA exposure leads to mitochondrial dysfunction, characterized by accumulation of reactive oxygen species (ROS), depolarization of mitochondrial membrane potential and depletion of ATP pool in host cells. Additionally, the intra-cellular ROS, accumulated in response to GbpA, were found to induce the migration of NF-κB from cytoplasm into nucleus in host cells. Taken together, these results prompted us to conclude that GbpA orchestrates a necrotic response in host cells which may have implications in immune response.

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2016-08-01
2021-10-16
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References

  1. Ashida H., Mimuro H., Ogawa M., Kobayashi T., Sanada T., Kim M., Sasakawa C. 2011; Cell death and infection: a double-edged sword for host and pathogen survival. J Cell Biol 195:931–942 [View Article][PubMed]
    [Google Scholar]
  2. Bhowmick R., Ghosal A., Das B., Koley H., Saha D. R., Ganguly S., Nandy R. K., Bhadra R. K., Chatterjee N. S. 2008; Intestinal adherence of Vibrio cholerae involves a coordinated interaction between colonization factor GbpA and mucin. Infect Immun 76:4968–4977 [View Article][PubMed]
    [Google Scholar]
  3. Chatterjee N. S., Ghosh A., Sabui S., Acharya S., Banerjee K. K. 2012; Chitin-binding protein GbpA of Vibrio cholerae induces interleukin-8 gene expression in intestinal cells through a TLR2/TLR1/CD14 complex. FASEB J 26:
    [Google Scholar]
  4. Choi K., Kim J., Kim G. W., Choi C. 2009; Oxidative stress-induced necrotic cell death via mitochondria-dependent burst of reactive oxygen species. Curr Neurovasc Res 6:213–222 [View Article][PubMed]
    [Google Scholar]
  5. Coelho A., Andrade J. R., Vicente A. C., DiRita V. J. 2000; Cytotoxic cell vacuolating activity from V. cholerae hemolysin. Infect Immun 68:1700–1705 [CrossRef]
    [Google Scholar]
  6. De S. N., Chatterjee D. N. 1953; An experimental study of the mechanism of action of Vibrio cholerae on the intestinal mucus membranes. J Pathol Bacteriol 66:559–562 [CrossRef]
    [Google Scholar]
  7. Festjens N., Vanden Berghe T., Vandenabeele P. 2006; Necrosis, a well-orchestrated form of cell demise: signalling cascades, important mediators and concomitant immune response. Biochim Biophys Acta 1757:1371–1387 [View Article][PubMed]
    [Google Scholar]
  8. Golstein P., Kroemer G. 2007; Cell death by necrosis: towards a molecular definition. Trends Biochem Sci 32:37–43 [View Article][PubMed]
    [Google Scholar]
  9. Gupta S., Prasad G. V., Mukhopadhaya A. 2015; Vibrio cholerae porin OmpU induces caspase-independent programmed cell death upon translocation to the host cell mitochondria. J Biol Chem 290:31051–31068 [CrossRef]
    [Google Scholar]
  10. Gutierrez M. G., Saka H. A., Chinen I., Zoppino F. C. M., Yoshimori T., Bocco J. L., Colombo M. I. 2007; Protective role of autophagy against Vibrio cholerae cytolysin, a pore-forming toxin from V. cholerae . Proc Natl Acad Sci U S A 104:1829–1834 [View Article]
    [Google Scholar]
  11. Ioannou Y. A., Chen F. W. 1996; Quantitation of DNA fragmentation in apoptosis. Nucleic Acids Res 24:992–993 [CrossRef]
    [Google Scholar]
  12. Kirkinezos I. G., Moraes C. T. 2001; Reactive oxygen species and mitochondrial diseases. Semin Cell Dev Biol 12:449–457 [View Article][PubMed]
    [Google Scholar]
  13. Kirn T. J., Jude B. A., Taylor R. K. 2005; A colonization factor links Vibrio cholerae environmental survival and human infection. Nature 438:863–866 [View Article][PubMed]
    [Google Scholar]
  14. Kyung K. J., So Y. G., Jong G. L., Sang H. C. 2016; Regulatory characteristics of Vibrio vulnificus gbpA encoding a mucin-binding protein essential for pathogenesis. J Biol Chem 291:5774–5787 [CrossRef]
    [Google Scholar]
  15. Lamkanfi M., Dixit V. M. 2010; Manipulation of host cell death pathways during microbial infections. Cell Host Microbe 8:44–54 [View Article][PubMed]
    [Google Scholar]
  16. Lang A., Schoonhoven R., Tuvia S., Brenner D. A., Rippe R. A. 2000; Nuclear factor κB in proliferation, activation, and apoptosis in rat hepatic stellate cells. J Hepatol 33:49–58 [View Article][PubMed]
    [Google Scholar]
  17. Lee S. J., Jung Y. H., Oh S. Y., Song E. J., Choi S. H., Han H. J. 2015a; Vibrio vulnificus VvhA induces NF-κB-dependent mitochondrial cell death via lipid raft-mediated ROS production in intestinal epithelial cells. Cell Death Dis 6:1655 [View Article][PubMed]
    [Google Scholar]
  18. Lee S. J., Jung Y. H., Song E. J., Jang K. K., Choi S. H., Han H. J. 2015b; Vibrio vulnificus VvpE stimulates IL-1β production by the hypomethylation of the IL-1β promoter and NF-κB activation via lipid raft-dependent ANXA2 recruitment and reactive oxygen species signaling in intestinal epithelial cells. J Immunol 195:2282–2293 [View Article][PubMed]
    [Google Scholar]
  19. Li Z., Venegas V., Nagaoka Y., Morino E., Raghavan P., Audhya A., Nakanishi Y., Zhou Z. 2015; Necrotic cells actively attract phagocytes through the collaborative action of two distinct PS-exposure mechanisms. PLoS Genet 11:e1005418 [View Article][PubMed]
    [Google Scholar]
  20. Loose J. S., Forsberg Z., Fraaije M. W., Eijsink V. G., Vaaje-Kolstad G. 2014; A rapid quantitative activity assay shows that the Vibrio cholerae colonization factor GbpA is an active lytic polysaccharide monooxygenase. FEBS Lett 588:3435–3440 [View Article][PubMed]
    [Google Scholar]
  21. Lu Y., Bhushan S., Tchatalbachev S., Marconi M., Bergmann M., Weidner W., Chakraborty T., Meinhardt A. 2013; Necrosis is the dominant cell death pathway in uropathogenic Escherichia coli elicited epididymo-orchitis and is responsible for damage of rat testis. PLoS One 8:e52919 [View Article][PubMed]
    [Google Scholar]
  22. Matzinger P. 1994; Tolerance, danger, and the extended family. Annu Rev Immunol 12:991–1045 [CrossRef]
    [Google Scholar]
  23. Meibom K. L., Li X. B., Nielsen A. T., Wu C.-Y., Roseman S., Schoolnik G. K. 2004; The Vibrio cholerae chitin utilization program. Proc Natl Acad Sci U S A 101:2524–2529 [View Article]
    [Google Scholar]
  24. Mondal A., Tapader R., Chatterjee N. S., Ghosh A., Sinha R., Koley H., Saha D. R., Chakrabarti M. K., Wai S. N., Pal A. 2016; Cytotoxic and inflammatory responses induced by outer membrane vesicle-associated biologically active proteases from Vibrio cholerae . Infect Immun 84:1478–1490 [View Article][PubMed]
    [Google Scholar]
  25. Montiel-Duarte C., Ansorena E., López-Zabalza M. J., Cenarruzabeitia E., Iraburu M. J. 2004; Role of reactive oxygen species, glutathione and NF-kappaB in apoptosis induced by 3,4-methylenedioxymethamphetamine ("Ecstasy") on hepatic stellate cells. Biochem Pharmacol 67:1025–1033 [View Article][PubMed]
    [Google Scholar]
  26. Morgan M. J., Kim Y. S., Liu Z. G. 2008; TNF α and reactive oxygen species in necrotic cell death. Cell Res 18:343–349 [View Article][PubMed]
    [Google Scholar]
  27. Ou G., Rompikuntal P. K., Bitar A., Lindmark B., Vaitkevicius K., Wai S. N., Hammarström M. L. 2009; Vibrio cholerae cytolysin causes an inflammatory response in human intestinal epithelial cells that is modulated by the PrtV protease. PLoS One 4:e7806 [View Article][PubMed]
    [Google Scholar]
  28. Ray T., Pal A. 2016; PAR-1 mediated apoptosis of breast cancer cells by V. cholerae hemagglutinin protease. Apoptosis 21:609–620 [View Article][PubMed]
    [Google Scholar]
  29. Saile B., Matthes N., El Armouche H., Neubauer K., Ramadori G. 2001; The bcl, NFkappaB and p53/p21WAF1 systems are involved in spontaneous apoptosis and in the anti-apoptotic effect of TGF-beta or TNF-alpha on activated hepatic stellate cells. Eur J Cell Biol 80:554–561 [View Article][PubMed]
    [Google Scholar]
  30. Saka H. A., Bidinost C., Sola C., Carranza P., Collino C., Ortiz S., Echenique J. R., Bocco J. L. 2008; Vibrio cholerae cytolysin is essential for high enterotoxicity and apoptosis induction produced by a cholera toxin gene-negative V. cholerae non-O1, non-O139 strain. Microb Pathog 44:118–128 [View Article][PubMed]
    [Google Scholar]
  31. Seper A., Hosseinzadeh A., Gorkiewicz G., Lichtenegger S., Roier S., Leitner D. R., Röhm M., Grutsch A., Reidl J. et al. 2013; Vibrio cholerae evades neutrophil extracellular traps by the activity of two extracellular nucleases. PLoS Pathog 9:e1003614 [View Article]
    [Google Scholar]
  32. Shi Y., Zheng W., Rock K. L. 2000; Cell injury releases endogenous adjuvants that stimulate cytotoxic T cell responses. Proc Natl Acad Sci U S A 97:14590–14595 [View Article]
    [Google Scholar]
  33. Simon F., Fernández R. 2009; Early lipopolysaccharide-induced reactive oxygen species production evokes necrotic cell death in human umbilical vein endothelial cells. J Hypertens 27:1202–1216 [View Article][PubMed]
    [Google Scholar]
  34. Stauder M., Huq A., Pezzati E., Grim C. J., Ramoino P., Pane L., Colwell R. R., Pruzzo C., Vezzulli L. 2012; Role of GbpA protein, an important virulence-related colonization factor, for Vibrio cholerae's survival in the aquatic environment. Environ Microbiol Rep 4:439–445 [View Article][PubMed]
    [Google Scholar]
  35. Stauder M., Vezzulli L., Pezzati E., Repetto B., Pruzzo C. 2010; Temperature affects Vibrio cholerae O1 El Tor persistence in the aquatic environment via an enhanced expression of GbpA and MSHA adhesins. Environ Microbiol Rep 2:140–144 [View Article][PubMed]
    [Google Scholar]
  36. Storz P., Toker A. 2003; Protein kinase D mediates a stress-induced NF-κB activation and survival pathway. EMBO J 22:109–120 [View Article][PubMed]
    [Google Scholar]
  37. Storz P., Döppler H., Toker A. 2004; Protein kinase CΔ selectively regulates protein kinase D-dependent activation of NF-κB in oxidative stress signaling. Mol Cell Biol 24:2614–2626[PubMed] [CrossRef]
    [Google Scholar]
  38. Suman S., Pandey A., Chandna S. 2012; An improved non-enzymatic “DNA ladder assay” for more sensitive and early detection of apoptosis. Cytotechnology 64:9–14 [View Article][PubMed]
    [Google Scholar]
  39. Tang J. B., Xu Y., Wang X. T. 2004; Tendon healing in vitro: activation of NIK, IKKα, IKKβ and NF-κB. Plast Reconstr Surg 8:1819–1827
    [Google Scholar]
  40. Trancíková A., Weisová P., Kissová I., Zeman I., Kolarov J. 2004; Production of reactive oxygen species and loss of viability in yeast mitochondrial mutants: protective effect of Bcl-XL . FEMS Yeast Res 5:149–156 [View Article][PubMed]
    [Google Scholar]
  41. Upton J. W., Kaiser W. J., Mocarski E. S. 2010; Virus inhibition of RIP3-dependent necrosis. Cell Host Microbe 7:302–313 [View Article][PubMed]
    [Google Scholar]
  42. Wang X., Chen W., Lin Y. 2007; Sensitization of TNF-induced cytotoxicity in lung cancer cells by concurrent suppression of the NF-kappaB and Akt pathways. Biochem Biophys Res Commun 355:807–812 [View Article][PubMed]
    [Google Scholar]
  43. Wong E., Vaaje-Kolstad G., Ghosh A., Hurtado-Guerrero R., Konarev P., Ibrahim A. F., Svergun D., Eijsink V. G., Chatterjee N. S., van Aalten D. M. 2012; The Vibrio cholerae colonization factor GbpA possesses a modular structure that governs binding to different host surfaces. PLoS Pathog 8:e1002373 [View Article][PubMed]
    [Google Scholar]
  44. Yuan X., Zhou Y., Wang W., Li J., Xie G., Zhao Y., Xu D., Shen L. 2013; Activation of TLR4 signaling promotes gastric cancer progression by inducing mitochondrial ROS production. Cell DeathDis 4:e794 [View Article]
    [Google Scholar]
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