1887

Microbiology Society logo

Volume 155, Issue 3

Type III secretion system 1 of induces oncosis in both epithelial and monocytic cell lines Free

Abstract

The type III secretion system 1 (T3SS1) induces cytotoxicity in mammalian epithelial cells. We characterized the cell death phenotype in both epithelial (HeLa) and monocytic (U937) cell lines following infection with . Using a combination of the wild-type strain and gene knockouts, we confirmed that strain NY-4 was able to induce cell death in both cell lines via a T3SS1-dependent mechanism. Bacterial contact, but not internalization, was required for T3SS1-induced cytotoxicity. The mechanism of cell death involves formation of a pore structure on the surface of infected HeLa and U937 cells, as demonstrated by cellular swelling, uptake of cell membrane-impermeable dye and protection of cytotoxicity by osmoprotectant (PEG3350). Western blot analysis showed that poly ADP ribose polymerase (PARP) was not cleaved and remained in its full-length active form. This result was evident for seven different strains. -induced cytotoxicity was not inhibited by addition of the pan-caspase inhibitor carbobenzoxy-valyl-alanyl-aspartyl-[-methyl]-fluoromethylketone (Z-VAD-FMK) or the caspase-1 inhibitor -acetyl-tyrosyl-valyl-alanyl-aspartyl-aldehyde (Ac-YVAD-CHO); thus, caspases were not involved in T3SS1-induced cytotoxicity. DNA fragmentation was not evident following infection and autophagic vacuoles were not observed after monodansylcadaverine staining. We conclude that T3SS1 of strain NY-4 induces a host cell death primarily via oncosis rather than apoptosis, pyroptosis or autophagy.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): AO, acridine orange , IL, interleukin , LDH, lactate dehydrogenase , MDC, monodansylcadaverine , PARP, poly ADP ribose polymerase , STS, staurosporine , T3SS, type III secretion system and TBH, t-butylhydroperoxide
SGM
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.024919-0
2009-03-01
2023-03-24
Loading full text...

Full text loading...

/deliver/fulltext/micro/155/3/837.html?itemId=/content/journal/micro/10.1099/mic.0.024919-0&mimeType=html&fmt=ahah

References

  1. Affar E. B., Germain M., Winstall E., Vodenicharov M., Shah R. G., Salvesen G. S., Poirier G. G. 2001; Caspase-3-mediated processing of poly(ADP-ribose) glycohydrolase during apoptosis. J Biol Chem 276:2935–2942
     [Google Scholar]
  2. Akeda Y., Nagayama K., Yamamoto K., Honda T. 1997; Invasive phenotype of Vibrio parahaemolyticus . J Infect Dis 176:822–824
     [Google Scholar]
  3. Bej A. K., Patterson D. P., Brasher C. W., Vickery M. C., Jones D. D., Kaysner C. A. 1999; Detection of total and hemolysin-producing Vibrio parahaemolyticus in shellfish using multiplex PCR amplification of tl, tdh and trh . J Microbiol Methods 36:215–225
     [Google Scholar]
  4. Biederbick A., Kern H. F., Elsasser H. P. 1995; Monodansylcadaverine (MDC) is a specific in vivo marker for autophagic vacuoles. Eur J Cell Biol 66:3–14
     [Google Scholar]
  5. Brennan M. A., Cookson B. T. 2000; Salmonella induces macrophage death by caspase-1-dependent necrosis. Mol Microbiol 38:31–40
     [Google Scholar]
  6. Burdette D. L., Yarbrough M. L., Orvedahl A., Gilpin C. J., Orth K. 2008; Vibrio parahaemolyticus orchestrates a multifaceted host cell infection by induction of autophagy, cell rounding, and then cell lysis. Proc Natl Acad Sci U S A 105:12497–12502
     [Google Scholar]
  7. Chen L. M., Kaniga K., Galan J. E. 1996; Salmonella spp. are cytotoxic for cultured macrophages. Mol Microbiol 21:1101–1115
     [Google Scholar]
  8. Cornelis G. R. 2002; The Yersinia Ysc–Yop ‘type III’ weaponry. Nat Rev Mol Cell Biol 3:742–752
     [Google Scholar]
  9. Cornelis G. R. 2006; The type III secretion injectisome. Nat Rev Microbiol 4:811–825
     [Google Scholar]
  10. Cornelis G. R., Van Gijsegem F. 2000; Assembly and function of type III secretory systems. Annu Rev Microbiol 54:735–774
     [Google Scholar]
  11. Dacheux D., Goure J., Chabert J., Usson Y., Attree I. 2001; Pore-forming activity of type III system-secreted proteins leads to oncosis of Pseudomonas aeruginosa-infected macrophages. Mol Microbiol 40:76–85
     [Google Scholar]
  12. Daniels N. A., MacKinnon L., Bishop R., Altekruse S., Ray B., Hammond R. M., Thompson S., Wilson S., Bean N. H. other authors 2000; Vibrio parahaemolyticus infections in the United States, 1973–1998. J Infect Dis 181:1661–1666
     [Google Scholar]
  13. Denecker G., Totemeyer S., Mota L. J., Troisfontaines P., Lambermont I., Youta C., Stainier I., Ackermann M., Cornelis G. R. 2002; Effect of low- and high-virulence Yersinia enterocolitica strains on the inflammatory response of human umbilical vein endothelial cells. Infect Immun 70:3510–3520
     [Google Scholar]
  14. Duclos S., Desjardins M. 2000; Subversion of a young phagosome: the survival strategies of intracellular pathogens. Cell Microbiol 2:365–377
     [Google Scholar]
  15. Fernandez-Prada C. M., Hoover D. L., Tall B. D., Venkatesan M. M. 1997; Human monocyte-derived macrophages infected with virulent Shigella flexneri in vitro undergo a rapid cytolytic event similar to oncosis but not apoptosis. Infect Immun 65:1486–1496
     [Google Scholar]
  16. Fink S. L., Cookson B. T. 2005; Apoptosis, pyroptosis, and necrosis: mechanistic description of dead and dying eukaryotic cells. Infect Immun 73:1907–1916
     [Google Scholar]
  17. Fink S. L., Cookson B. T. 2006; Caspase-1-dependent pore formation during pyroptosis leads to osmotic lysis of infected host macrophages. Cell Microbiol 8:1812–1825
     [Google Scholar]
  18. Germain M., Affar E. B., D'Amours D., Dixit V. M., Salvesen G. S., Poirier G. G. 1999; Cleavage of automodified poly(ADP-ribose) polymerase during apoptosis. Evidence for involvement of caspase-7. J Biol Chem 274:28379–28384
     [Google Scholar]
  19. Handa Y., Suzuki M., Ohya K., Iwai H., Ishijima N., Koleske A. J., Fukui Y., Sasakawa C. 2007; Shigella IpgB1 promotes bacterial entry through the ELMO–Dock180 machinery. Nat Cell Biol 9:121–128
     [Google Scholar]
  20. Hansen-Wester I., Hensel M. 2001; Salmonella pathogenicity islands encoding type III secretion systems. Microbes Infect 3:549–559
     [Google Scholar]
  21. Hersh D., Monack D. M., Smith M. R., Ghori N., Falkow S., Zychlinsky A. 1999; The Salmonella invasin SipB induces macrophage apoptosis by binding to caspase-1. Proc Natl Acad Sci U S A 96:2396–2401
     [Google Scholar]
  22. Hertle R. 2000; Serratia type pore forming toxins. Curr Protein Pept Sci 1:75–89
     [Google Scholar]
  23. Hertle R., Hilger M., Weingardt-Kocher S., Walev I. 1999; Cytotoxic action of Serratia marcescens hemolysin on human epithelial cells. Infect Immun 67:817–825
     [Google Scholar]
  24. Hlady W. G., Klontz K. C. 1996; The epidemiology of Vibrio infections in Florida, 1981–1993. J Infect Dis 173:1176–1183
     [Google Scholar]
  25. Hoashi K., Ogata K., Taniguchi H., Yamashita H., Tsuji K., Mizuguchi Y., Ohtomo N. 1990; Pathogenesis of Vibrio parahaemolyticus: intraperitoneal and orogastric challenge experiments in mice. Microbiol Immunol 34:355–366
     [Google Scholar]
  26. Hueck C. J. 1998; Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol Mol Biol Rev 62:379–433
     [Google Scholar]
  27. Iwai-Kanai E., Yuan H., Huang C., Sayen M. R., Perry-Garza C. N., Kim L., Gottlieb R. A. 2008; A method to measure cardiac autophagic flux in vivo. Autophagy 4:322–329
     [Google Scholar]
  28. Jepson M. A., Pellegrin S., Peto L., Banbury D. N., Leard A. D., Mellor H., Kenny B. 2003; Synergistic roles for the Map and Tir effector molecules in mediating uptake of enteropathogenic Escherichia coli (EPEC) into non-phagocytic cells. Cell Microbiol 5:773–783
     [Google Scholar]
  29. Joseph S. W., Colwell R. R., Kaper J. B. 1982; Vibrio parahaemolyticus and related halophilic Vibrios. Crit Rev Microbiol 10:77–124
     [Google Scholar]
  30. Kato M., Nonaka T., Maki M., Kikuchi H., Imajoh-Ohmi S. 2000; Caspases cleave the amino-terminal calpain inhibitory unit of calpastatin during apoptosis in human Jurkat T cells. J Biochem 127:297–305
     [Google Scholar]
  31. Kirby J. E., Vogel J. P., Andrews H. L., Isberg R. R. 1998; Evidence for pore-forming ability by Legionella pneumophila . Mol Microbiol 27:323–336
     [Google Scholar]
  32. Lazebnik Y. A., Kaufmann S. H., Desnoyers S., Poirier G. G., Earnshaw W. C. 1994; Cleavage of poly(ADP-ribose) polymerase by a proteinase with properties like ICE. Nature 371:346–347
     [Google Scholar]
  33. Lynch T., Livingstone S., Buenaventura E., Lutter E., Fedwick J., Buret A. G., Graham D., DeVinney R. 2005; Vibrio parahaemolyticus disruption of epithelial cell tight junctions occurs independently of toxin production. Infect Immun 73:1275–1283
     [Google Scholar]
  34. Mills S. D., Boland A., Sory M. P., van der Smissen P., Kerbourch C., Finlay B. B., Cornelis G. R. 1997; Yersinia enterocolitica induces apoptosis in macrophages by a process requiring functional type III secretion and translocation mechanisms and involving YopP, presumably acting as an effector protein. Proc Natl Acad Sci U S A 94:12638–12643
     [Google Scholar]
  35. Milton D. L., O'Toole R., Horstedt P., Wolf-Watz H. 1996; Flagellin A is essential for the virulence of Vibrio anguillarum . J Bacteriol 178:1310–1319
     [Google Scholar]
  36. Mota L. J., Cornelis G. R. 2005; The bacterial injection kit: type III secretion systems. Ann Med 37:234–249
     [Google Scholar]
  37. Munafo D. B., Colombo M. I. 2001; A novel assay to study autophagy: regulation of autophagosome vacuole size by amino acid deprivation. J Cell Sci 114:3619–3629
     [Google Scholar]
  38. Navarre W. W., Zychlinsky A. 2000; Pathogen-induced apoptosis of macrophages: a common end for different pathogenic strategies. Cell Microbiol 2:265–273
     [Google Scholar]
  39. Neyt C., Cornelis G. R. 1999; Insertion of a Yop translocation pore into the macrophage plasma membrane by Yersinia enterocolitica: requirement for translocators YopB and YopD, but not LcrG. Mol Microbiol 33:971–981
     [Google Scholar]
  40. Nieminen A. L., Saylor A. K., Tesfai S. A., Herman B., Lemasters J. J. 1995; Contribution of the mitochondrial permeability transition to lethal injury after exposure of hepatocytes to t-butylhydroperoxide. Biochem J 307:99–106
     [Google Scholar]
  41. Nishibuchi M., Fasano A., Russell R. G., Kaper J. B. 1992; Enterotoxigenicity of Vibrio parahaemolyticus with and without genes encoding thermostable direct hemolysin. Infect Immun 60:3539–3545
     [Google Scholar]
  42. Nonaka T., Kuwabara T., Mimuro H., Kuwae A., Imajoh-Ohmi S. 2003; Shigella-induced necrosis and apoptosis of U937 cells and J774 macrophages. Microbiology 149:2513–2527
     [Google Scholar]
  43. Ono T., Park K. S., Ueta M., Iida T., Honda T. 2006; Identification of proteins secreted via Vibrio parahaemolyticus type III secretion system 1. Infect Immun 74:1032–1042
     [Google Scholar]
  44. Palmer L. E., Pancetti A. R., Greenberg S., Bliska J. B. 1999; YopJ of Yersinia spp. is sufficient to cause downregulation of multiple mitogen-activated protein kinases in eukaryotic cells. Infect Immun 67:708–716
     [Google Scholar]
  45. Park K. S., Ono T., Rokuda M., Jang M. H., Okada K., Iida T., Honda T. 2004; Functional characterization of two type III secretion systems of Vibrio parahaemolyticus . Infect Immun 72:6659–6665
     [Google Scholar]
  46. Pizarro-Cerda J., Cossart P. 2006; Bacterial adhesion and entry into host cells. Cell 124:715–727
     [Google Scholar]
  47. Qadri F., Alam M. S., Nishibuchi M., Rahman T., Alam N. H., Chisti J., Kondo S., Sugiyama J., Bhuiyan N. A. other authors 2003; Adaptive and inflammatory immune responses in patients infected with strains of Vibrio parahaemolyticus . J Infect Dis 187:1085–1096
     [Google Scholar]
  48. Reyrat J. M., Pelicic V., Papini E., Montecucco C., Rappuoli R., Telford J. L. 1999; Towards deciphering the Helicobacter pylori cytotoxin. Mol Microbiol 34:197–204
     [Google Scholar]
  49. Ribeiro C., Vignes M., Brehelin M. 2003; Xenorhabdus nematophila (enterobacteriacea) secretes a cation-selective calcium-independent porin which causes vacuolation of the rough endoplasmic reticulum and cell lysis. J Biol Chem 278:3030–3039
     [Google Scholar]
  50. Schlumberger M. C., Hardt W. D. 2006; Salmonella type III secretion effectors: pulling the host cell's strings. Curr Opin Microbiol 9:46–54
     [Google Scholar]
  51. Sun G. W., Lu J., Pervaiz S., Cao W. P., Gan Y. H. 2005; Caspase-1 dependent macrophage death induced by Burkholderia pseudomallei . Cell Microbiol 7:1447–1458
     [Google Scholar]
  52. Swanson M. S., Fernandez-Moreira E. 2002; A microbial strategy to multiply in macrophages: the pregnant pause. Traffic 3:170–177
     [Google Scholar]
  53. Takahashi A., Iida T., Naim R., Naykaya Y., Honda T. 2001; Chloride secretion induced by thermostable direct haemolysin of Vibrio parahaemolyticus depends on colonic cell maturation. J Med Microbiol 50:870–878
     [Google Scholar]
  54. Tewari M., Quan L. T., O'Rourke K., Desnoyers S., Zeng Z., Beidler D. R., Poirier G. G., Salvesen G. S., Dixit V. M. 1995; Yama/CPP32 β, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase. Cell 81:801–809
     [Google Scholar]
  55. Tsuchiya S., Kobayashi Y., Goto Y., Okumura H., Nakae S., Konno T., Tada K. 1982; Induction of maturation in cultured human monocytic leukemia cells by a phorbol diester. Cancer Res 42:1530–1536
     [Google Scholar]
  56. Wada A., Yamasaki E., Hirayama T. 2004; Helicobacter pylori vacuolating cytotoxin, VacA, is responsible for gastric ulceration. J Biochem 136:741–746
     [Google Scholar]
  57. Yeung P. S., Boor K. J. 2004; Epidemiology, pathogenesis, and prevention of foodborne Vibrio parahaemolyticus infections. Foodborne Pathog Dis 1:74–88
     [Google Scholar]
  58. Zhou X., Shah D. H., Konkel M. E., Call D. R. 2008; Type III secretion system 1 genes in Vibrio parahaemolyticus are positively regulated by ExsA and negatively regulated by ExsD. Mol Microbiol 69:747–764
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.024919-0
Loading
Type III secretion system 1 of Vibrio parahaemolyticus induces oncosis in both epithelial and monocytic cell lines
Microbiology 155, 837 (2009); https://doi.org/10.1099/mic.0.024919-0
/content/journal/micro/10.1099/mic.0.024919-0
/content/journal/micro/10.1099/mic.0.024919-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error