2,095
Views
22
CrossRef citations to date
0
Altmetric
Research Paper

The Vibrio alginolyticus T3SS effectors, Val1686 and Val1680, induce cell rounding, apoptosis and lysis of fish epithelial cells

, Ph.D., , , , , & show all
Pages 318-330 | Received 25 Jul 2017, Accepted 01 Dec 2017, Published online: 27 Feb 2018

References

  • Galan JE, Wolf-Watz H. Protein delivery into eukaryotic cells by type III secretion machines. Nature. 2006;444:567–73. doi:10.1038/nature05272
  • Mueller CA, Broz P, Cornelis GR. The type III secretion system tip complex and translocon. Mol Microbiol. 2008;68:1085–95. doi:10.1111/j.1365-2958.2008.06237.x
  • Enninga J, Rosenshine I. Imaging the assembly, structure and activity of type III secretion systems. Cell Microbiol. 2009;11:1462–70. doi:10.1111/j.1462-5822.2009.01360.x
  • Hueck CJ. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol Mol Biol Rev. 1998;62:379–433.
  • Coburn B, Sekirov I, Finlay BB. Type III secretion systems and disease. Clin Microbiol Rev. 2007;20:535–49. doi:10.1128/CMR.00013-07
  • Troisfontaines P, Cornelis GR. Type III secretion: more systems than you think. Physiology (Bethesda). 2005;20:326–39. doi:10.1152/physiol.00011.2005
  • Michiels T, Wattiau P, Brasseur R, Ruysschaert JM, Cornelis G. Secretion of Yop proteins by Yersiniae. Infect Immun. 1990; 58:2840–9.
  • Makino K, Oshima K, Kurokawa K, Yokoyama K, Uda T, Tagomori K, et al. Genome sequence of Vibrio parahaemolyticus: a pathogenic mechanism distinct from that of V cholerae. Lancet. 2003;361:743–9. doi:10.1016/S0140-6736(03)12659-1
  • Park KS, Ono T, Rokuda M, Jang MH, Okada K, Iida T, et al. Functional characterization of two type III secretion systems of Vibrio parahaemolyticus. Infect Immun. 2004;72:6659–65. doi:10.1128/IAI.72.11.6659-6665.2004
  • Burdette DL, Seemann J, Orth K. Vibrio VopQ induces PI3-kinase-independent autophagy and antagonizes phagocytosis. Mol Microbiol. 2009;73:639–49. doi:10.1111/j.1365-2958.2009.06798.x
  • Zhou X, Konkel ME, Call DR. Type III secretion system 1 of Vibrio parahaemolyticus induces oncosis in both epithelial and monocytic cell lines. Microbiology. 2009;155:837–51. doi:10.1099/mic.0.024919-0
  • Pineyro P, Zhou X, Orfe LH, Friel PJ, Lahmers K, Call DR. Development of two animal models to study the function of Vibrio parahaemolyticus type III secretion systems. Infect Immun. 2010;78:4551–9. doi:10.1128/IAI.00461-10
  • Ritchie JM, Rui H, Zhou X, Iida T, Kodoma T, Ito S, et al. Inflammation and disintegration of intestinal villi in an experimental model for Vibrio parahaemolyticus-induced diarrhea. PLoS Pathog. 2012;8:e1002593. doi:10.1371/journal.ppat.1002593
  • Casselli T, Lynch T, Southward CM, Jones BW, DeVinney R. Vibrio parahaemolyticus inhibition of Rho family GTPase activation requires a functional chromosome I type III secretion system. Infect Immun. 2008;76:2202–11. doi:10.1128/IAI.01704-07
  • Yarbrough ML, Li Y, Kinch LN, Grishin NV, Ball HL, Orth K. AMPylation of Rho GTPases by Vibrio VopS disrupts effector binding and downstream signaling. Science. 2009;323:269–72. doi:10.1126/science.1166382
  • Hall A. Rho GTPases and the actin cytoskeleton. Science 1998; 279:509–14. doi:10.1126/science.279.5350.509
  • Wojnacki J, Quassollo G, Marzolo MP, Caceres A. Rho GTPases at the crossroad of signaling networks in mammals: impact of Rho-GTPases on microtubule organization and dynamics. Small GTPases. 2014;5:e28430. doi:10.4161/sgtp.28430
  • Matsuda S, Okada N, Kodama T, Honda T, Iida T. A cytotoxic type III secretion effector of Vibrio parahaemolyticus targets vacuolar H+-ATPase subunit c and ruptures host cell lysosomes. PLoS Pathog. 2012;8:e1002803. doi:10.1371/journal.ppat.1002803
  • Sreelatha A, Bennett TL, Carpinone EM, O'Brien KM, Jordan KD, Burdette DL, et al. Vibrio effector protein VopQ inhibits fusion of V-ATPase-containing membranes. Proc Natl Acad Sci U S A. 2015;112:100–5. doi:10.1073/pnas.1413764111
  • Salomon D, Guo Y, Kinch LN, Grishin NV, Gardner KH, Orth K. Effectors of animal and plant pathogens use a common domain to bind host phosphoinositides. Nat Commun. 2013;4:2973. doi:10.1038/ncomms3973
  • Ono T, Park KS, Ueta M, Iida T, Honda T. Identification of proteins secreted via Vibrio parahaemolyticus type III secretion system 1. Infect Immun. 2006;74:1032–42. doi:10.1128/IAI.74.2.1032-1042.2006
  • Broberg CA, Zhang L, Gonzalez H, Laskowski-Arce MA, Orth K. A Vibrio effector protein is an inositol phosphatase and disrupts host cell membrane integrity. Science. 2010;329:1660–2. doi:10.1126/science.1192850
  • Thompson CC, Vicente AC, Souza RC, Vasconcelos AT, Vesth T, Alves N, Jr., et al. Genomic taxonomy of Vibrios. BMC Evol Biol. 2009;9:258. doi:10.1186/1471-2148-9-258
  • Nicholas A, Daniels AS. A review of pathogenic vibrio infections for clinicians. Infect Med. 2000;17(10):665–85.
  • Austin B. Vibrios as causal agents of zoonoses. Vet Microbiol. 2010;140:310–7. doi:10.1016/j.vetmic.2009.03.015
  • Xie ZY, Hu CQ, Chen C, Zhang LP, Ren CH. Investigation of seven Vibrio virulence genes among Vibrio alginolyticus and Vibrio parahaemolyticus strains from the coastal mariculture systems in Guangdong, China. Lett Appl Microbiol. 2005;41:202–7. doi:10.1111/j.1472-765X.2005.01688.x
  • Chen MX, Li HY, Li G, Zheng TL. Distribution of Vibrio alginolyticus-like species in Shenzhen coastal waters, China. Braz J Microbiol. 2011;42:884–96. doi:10.1590/S1517-83822011000300007
  • Lee KK, Yu SR, Liu PC. Alkaline serine protease is an exotoxin of Vibrio alginolyticus in kuruma prawn, Penaeus japonicus. Curr Microbiol 1997; 34:110–7. doi:10.1007/s002849900153
  • Zanetti S, Deriu A, Volterra L, Falchi MP, Molicotti P, Fadda G, et al. Virulence factors in Vibrio alginolyticus strains isolated from aquatic environments. Ann Ig. 2000;12:487–91.
  • Gonzalez-Escalona N, Blackstone GM, DePaola A. Characterization of a Vibrio alginolyticus strain, isolated from Alaskan oysters, carrying a hemolysin gene similar to the thermostable direct hemolysin-related hemolysin gene (trh) of Vibrio parahaemolyticus. Appl Environ Microbiol. 2006;72:7925–9. doi:10.1128/AEM.01548-06
  • Wang Q, Liu Q, Cao X, Yang M, Zhang Y. Characterization of two TonB systems in marine fish pathogen Vibrio alginolyticus: their roles in iron utilization and virulence. Arch Microbiol. 2008;190:595–603. doi:10.1007/s00203-008-0407-1
  • Zhao Z, Chen C, Hu CQ, Ren CH, Zhao JJ, Zhang LP, et al. The type III secretion system of Vibrio alginolyticus induces rapid apoptosis, cell rounding and osmotic lysis of fish cells. Microbiology. 2010;156:2864–72. doi:10.1099/mic.0.040626-0
  • Milton DL, O'Toole R, Horstedt P, Wolf-Watz H. Flagellin A is essential for the virulence of Vibrio anguillarum. J Bacteriol 1996; 178:1310–9. doi:10.1128/jb.178.5.1310-1319.1996
  • Nydam SD, Shah DH, Call DR. Transcriptome analysis of Vibrio parahaemolyticus in type III secretion system 1 inducing conditions. Front Cell Infect Microbiol. 2014;4:1. doi:10.3389/fcimb.2014.00001
  • Zhao Z, Zhang L, Ren C, Zhao J, Chen C, Jiang X, et al. Autophagy is induced by the type III secretion system of Vibrio alginolyticus in several mammalian cell lines. Arch Microbiol. 2011;193:53–61. doi:10.1007/s00203-010-0646-9
  • Zhao Z, Orfe LH, Liu J, Lu SY, Besser TE, Call DR. Microcin PDI regulation and proteolytic cleavage are unique among known microcins. Sci Rep. 2017;7:42529. doi:10.1038/srep42529
  • Liu J, Lu SY, Orfe LH, Ren CH, Hu CQ, Call DR, et al. ExsE Is a Negative Regulator for T3SS Gene Expression in Vibrio alginolyticus. Front Cell Infect Microbiol. 2016;6:177. doi:10.3389/fcimb.2016.00177
  • Zhou X, Konkel ME, Call DR. Vp1659 is a Vibrio parahaemolyticus type III secretion system 1 protein that contributes to translocation of effector proteins needed to induce cytolysis, autophagy, and disruption of actin structure in HeLa cells. J Bacteriol. 2010;192:3491–502.
  • Bhavsar AP, Guttman JA, Finlay BB. Manipulation of host-cell pathways by bacterial pathogens. Nature. 2007;449:827–34. doi:10.1038/nature06247
  • Shan L, He P, Sheen J. Intercepting host MAPK signaling cascades by bacterial type III effectors. Cell Host Microbe. 2007;1:167–74. doi:10.1016/j.chom.2007.04.008
  • Benitah SA, Valeron PF, van Aelst L, Marshall CJ, Lacal JC. Rho GTPases in human cancer: an unresolved link to upstream and downstream transcriptional regulation. Biochim Biophys Acta. 2004;1705:121–32.
  • Villalonga P, Ridley AJ. Rho GTPases and cell cycle control. Growth Factors. 2006;24:159–64. doi:10.1080/08977190600560651
  • Etienne-Manneville S, Hall A. Rho GTPases in cell biology. Nature. 2002;420:629–35. doi:10.1038/nature01148
  • Heasman SJ, Ridley AJ. Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat Rev Mol Cell Biol. 2008;9:690–701. doi:10.1038/nrm2476
  • Kaufman MR, Jia J, Zeng L, Ha U, Chow M, Jin S. Pseudomonas aeruginosa mediated apoptosis requires the ADP-ribosylating activity of exoS. Microbiology. 2000;146 (Pt 10):2531–41. doi:10.1099/00221287-146-10-2531
  • Jia J, Alaoui-El-Azher M, Chow M, Chambers TC, Baker H, Jin S. c-Jun NH2-terminal kinase-mediated signaling is essential for Pseudomonas aeruginosa ExoS-induced apoptosis. Infect Immun. 2003;71:3361–70. doi:10.1128/IAI.71.6.3361-3370.2003
  • Fiorentini C, Falzano L, Travaglione S, Fabbri A. Hijacking Rho GTPases by protein toxins and apoptosis: molecular strategies of pathogenic bacteria. Cell Death Differ. 2003;10:147–52. doi:10.1038/sj.cdd.4401151
  • Aktories K. Bacterial protein toxins that modify host regulatory GTPases. Nat Rev Microbiol. 2011;9:487–98. doi:10.1038/nrmicro2592
  • Popoff MR. Bacterial factors exploit eukaryotic Rho GTPase signaling cascades to promote invasion and proliferation within their host. Small GTPases. 2014;5:e983863. doi:10.4161/sgtp.28209.
  • Raymond B, Young JC, Pallett M, Endres RG, Clements A, Frankel G. Subversion of trafficking, apoptosis, and innate immunity by type III secretion system effectors. Trends Microbiol. 2013;21:430–41. doi:10.1016/j.tim.2013.06.008
  • Taylor RC, Cullen SP, Martin SJ. Apoptosis: controlled demolition at the cellular level. Nat Rev Mol Cell Biol. 2008;9:231–41. doi:10.1038/nrm2312
  • Creagh EM, Conroy H, Martin SJ. Caspase-activation pathways in apoptosis and immunity. Immunol Rev. 2003;193:10–21. doi:10.1034/j.1600-065X.2003.00048.x
  • Li J, Yuan J. Caspases in apoptosis and beyond. Oncogene. 2008;27:6194–206. doi:10.1038/onc.2008.297
  • Kantari C, Walczak H. Caspase-8 and bid: caught in the act between death receptors and mitochondria. Biochim Biophys Acta. 2011;1813:558–63. doi:10.1016/j.bbamcr.2011.01.026
  • Chang L, Karin M. Mammalian MAP kinase signalling cascades. Nature. 2001;410:37–40. doi:10.1038/35065000
  • Johnson GL, Lapadat R. Mitogen-activated protein kinase pathways mediated by ERK, JNK, and p38 protein kinases. Science. 2002;298:1911–2. doi:10.1126/science.1072682
  • Wada T, Penninger JM. Mitogen-activated protein kinases in apoptosis regulation. Oncogene. 2004;23:2838–49. doi:10.1038/sj.onc.1207556
  • Kyriakis JM, Avruch J. Mammalian MAPK signal transduction pathways activated by stress and inflammation: a 10-year update. Physiol Rev. 2012;92:689–737. doi:10.1152/physrev.00028.2011