Abstract
Vibrio parahaemolyticus, a Gram-negative bacterium, inhabits marine and estuarine environments and it is a major pathogen responsible globally for most cases of seafood-associated gastroenteritis in humans and acute hepatopancreatic necrosis syndrome in shrimps. There has been a dramatic worldwide increase in V. parahaemolyticus infections over the last two decades. The pathogenicity of V. parahaemolyticus has been linked to the expression of different kinds of virulence factors including extracellular proteases, such as metalloproteases and serine proteases. V. parahaemolyticus expresses the metalloproteases; PrtV, VppC, VPM and the serine proteases; VPP1/Protease A, VpSP37, PrtA. Extracellular proteases have been identified as potential virulence factors which directly digest many kinds of host proteins or indirectly are involved in the processing of other toxic protein factors. This review summarizes findings on the metalloproteases and serine proteases produced by V. parahaemolyticus and their roles in infections. Identifying the role of V. parahaemolyticus virulence-associated extracellular proteases deepens our understanding of diseases caused by this bacterium.
Similar content being viewed by others
References
Abdel-Sattar ES, Miyoshi SI, Elgaml A (2016) Regulation of Vibrio mimicus metalloprotease (VMP) production by the quorum-sensing master regulatory protein, LuxR. J Basic Microbiol 56:1051–1058
Baker-Austin C, Trinanes JA, Taylor NG, Hartnell R, Siitonen A, Martinez-Urtaza J (2013) Emerging Vibrio risk at high latitudes in response to ocean warming. Nat Clim Change 3:73
Ball AS, Chaparian RR, van Kessel JC (2017) Quorum sensing gene regulation by LuxR/HapR master regulators in Vibrios. J Bacteriol. https://doi.org/10.1128/jb.00105-17
Benitez JA, Silva AJ (2016) Vibrio cholerae hemagglutinin(HA)/protease: an extracellular metalloprotease with multiple pathogenic activities. Toxicon 115:55–62. https://doi.org/10.1016/j.toxicon.2016.03.003
Broberg CA, Zhang L, Gonzalez H, Laskowski-Arce MA, Orth K (2010) A Vibrio effector protein is an inositol phosphatase and disrupts host cell membrane integrity. Science 329:1660–1662
Broberg CA, Calder TJ, Orth K (2011) Vibrio parahaemolyticus cell biology and pathogenicity determinants. Microbes Infect 13:992–1001
Chang S-C, Lee C-Y (2017) OpaR and RpoS are positive regulators of a virulence factor PrtA in Vibrio parahaemolyticus. Microbiology 164:221–231
Crisafi F, Denaro R, Yakimov M, Felice MR, Giuliano L, Genovese L (2015) NaCl concentration in the medium modulates the secretion of active EmpA protease in Vibrio anguillarum at post-transcriptional level. J Appl Microbiol 119:1494–1501. https://doi.org/10.1111/jam.12957
Defoirdt T, Boon N, Sorgeloos P, Verstraete W, Bossier P (2008) Quorum sensing and quorum quenching in Vibrio harveyi: lessons learned from in vivo work. ISME J 2:19–26. https://doi.org/10.1038/ismej.2007.92
Duarte AS, Correia A, Esteves AC (2016) Bacterial collagenases: a review. Crit Rev Microbiol 42:106–126. https://doi.org/10.3109/1040841x.2014.904270
Gode-Potratz CJ, McCarter LL (2011) Quorum sensing and silencing in Vibrio parahaemolyticus. J Bacteriol 193:4224–4237. https://doi.org/10.1128/jb.00432-11
Guo RH, Lim JY, My T, Nu D, Jo SJ, Park JU, Rhee JH, Kim YR (2018) Vibrio vulnificus RtxA1 toxin expression upon contact with host cells is RpoS-dependent. Front Cell Infect Microbiol 8:70. https://doi.org/10.3389/fcimb.2018.00070
Ha C, Kim S-K, Lee M-N, Lee J-H (2014) Quorum sensing-dependent metalloprotease VvpE is important in the virulence of Vibrio vulnificus to invertebrates. Microb Pathog 71:8–14
Ham H, Orth K (2012) The role of type III secretion system 2 in Vibrio parahaemolyticus pathogenicity. J Microb 50:719–725
Han Y, Mo Z, **ao P, Hao B, Li J, Yang G (2011) Characterization of EmpA protease in Vibrio anguillarum M3. J Ocean Univ China 10:379–384
Ishihara M, Kawanishi A, Watanabe H, Tomochika K, Miyoshi S, Shinoda S (2002) Purification of a serine protease of Vibrio parahaemolyticus and its characterization. Microbiol Immunol 46:299–303
Kahla-Nakbi AB, Chaieb K, Bakhrouf A (2009) Investigation of several virulence properties among Vibrio alginolyticus strains isolated from diseased cultured fish in Tunisia. Dis Aquat Org 86:21–28
Kalburge SS, Carpenter MR, Rozovsky S, Boyd EF (2017) Quorum sensing regulators are required for metabolic fitness in Vibrio parahaemolyticus. Infect Immun 85:e00930–00916
Kim S-K, Yang J-Y, Cha J (2002) Cloning and sequence analysis of a novel metalloprotease gene from Vibrio parahaemolyticus 04. Gene 283:277–286
Kim JA et al (2015) Stationary-phase induction of vvpS expression by three transcription factors: repression by LeuO and activation by SmcR and CRP. Mol Microbiol 97:330–346. https://doi.org/10.1111/mmi.13028
Kim JA, Lee MA, Jung YC, Jang BR, Lee KH (2018) Repression of VvpM protease expression by quorum sensing and the cAMP-cAMP receptor protein complex in Vibrio vulnificus. J Bacteriol. https://doi.org/10.1128/jb.00526-17
Lee C-Y, Su S-C, Liaw R-B (1995) Molecular analysis of an extracellular protease gene from Vibrio parahaemolyticus. Microbiology 141:2569–2576
Lee CY, Cheng MF, Yu MS, Pan MJ (2002) Purification and characterization of a putative virulence factor, serine protease, from Vibrio parahaemolyticus. FEMS Microbiol Lett 209:31–37
Lee MA, Kim JA, Yang YJ, Shin MY, Park SJ, Lee KH (2014) VvpM, an extracellular metalloprotease of Vibrio vulnificus, induces apoptotic death of human cells. J Microbiol 52:1036–1043. https://doi.org/10.1007/s12275-014-4531-0
Lee MA, Kim JA, Shin MY, Lee JK, Park SJ, Lee KH (2015a) VvpM induces human cell death via multifarious modes including necroptosis and autophagy. J Microbiol Biotechnol 25:302–306
Lee CT et al (2015b) The opportunistic marine pathogen Vibrio parahaemolyticus becomes virulent by acquiring a plasmid that expresses a deadly toxin. Proc Natl Acad Sci USA 112:10798–10803. https://doi.org/10.1073/pnas.1503129112
Lee KJ, Jung YC, Park SJ, Lee KH (2018) Role of heat shock proteases in quorum-sensing-mediated regulation of biofilm formation by Vibrio species. mBio. https://doi.org/10.1128/mBio.02086-17
Letchumanan V, Chan K-G, Lee L-H (2014) Vibrio parahaemolyticus: a review on the pathogenesis, prevalence, and advance molecular identification techniques. Front Microbiol 5:705
Lin SJ, Hsu KC, Wang HC (2017) Structural insights into the cytotoxic mechanism of Vibrio parahaemolyticus PirA(vp) and PirB(vp) toxins. Marine Drugs. https://doi.org/10.3390/md15120373
Liu X, Gao H, **ao N, Liu Y, Li J, Li L (2015) Outer membrane protein U (OmpU) mediates adhesion of Vibrio mimicus to host cells via two novel N-terminal motifs. PLoS ONE 10:e0119026. https://doi.org/10.1371/journal.pone.0119026
Lu R, Osei-Adjei G, Huang X, Zhang Y (2018) Role and regulation of the orphan AphA protein of quorum sensing in pathogenic Vibrios. Future Microbiol 13:383–391. https://doi.org/10.2217/fmb-2017-0165
Luan X, Chen J, Zhang X-h, Li Y, Hu G (2007) Expression and characterization of a metalloprotease from a Vibrio parahaemolyticus isolate. Can J Microbiol 53:1168–1173
Madala PK, Tyndall JD, Nall T, Fairlie DP (2010) Update 1 of: proteases universally recognize beta strands in their active sites. Chem Rev. https://doi.org/10.1021/cr900368a
Martinez-Urtaza J et al (2016) Epidemiological investigation of a foodborne outbreak in Spain associated with US West Coast genotypes of Vibrio parahaemolyticus. SpringerPlus 5:87
Matlawska-Wasowska K, Finn R, Mustel A, O’Byrne CP, Baird AW, Coffey ET, Boyd A (2010) The Vibrio parahaemolyticus Type III Secretion Systems manipulate host cell MAPK for critical steps in pathogenesis. BMC Microbiol 10:329
Miyoshi S (2013) Extracellular proteolytic enzymes produced by human pathogenic Vibrio species. Front Microbiol 4:339. https://doi.org/10.3389/fmicb.2013.00339
Miyoshi S-i, Shinoda S (2000) Microbial metalloproteases and pathogenesis. Microbes Infect 2:91–98
Miyoshi S-i et al (2008) Differential gene expression and extracellular secretion of the collagenolytic enzymes by the pathogen Vibrio parahaemolyticus. FEMS Microbiol Lett 283:176–181
Miyoshi S-i, Wang J, Katoh K, Senoh M, Mizuno T, Maehara Y (2012) An extracellular serine protease produced by Vibrio vulnificus NCIMB 2137, a metalloprotease-gene negative strain isolated from a diseased eel. World J Microbiol Biotechnol 28:1633–1639
Newton A, Kendall M, Vugia DJ, Henao OL, Mahon BE (2012) Increasing rates of vibriosis in the United States, 1996–2010: review of surveillance data from 2 systems. Clin Infect Dis. https://doi.org/10.1093/cid/cis243
O’Boyle N, Boyd A (2014) Manipulation of intestinal epithelial cell function by the cell contact-dependent type III secretion systems of Vibrio parahaemolyticus. Front Cell Infect Microbiol 3:114
Papenfort K, Bassler BL (2016) Quorum sensing signal-response systems in Gram-negative bacteria. Nat Rev Microbiol 14:576–588. https://doi.org/10.1038/nrmicro.2016.89
Pereira CS, Thompson JA, Xavier KB (2013) AI-2-mediated signalling in bacteria. FEMS Microbiol Rev 37:156–181. https://doi.org/10.1111/j.1574-6976.2012.00345.x
Rawlings ND, Barrett AJ, Finn R (2016) Twenty years of the MEROPS database of proteolytic enzymes, their substrates and inhibitors. Nucleic Acids Res 44:D343–D350 https://doi.org/10.1093/nar/gkv1118
Rui H, Liu Q, Wang Q, Ma Y, Liu H, Shi C, Zhang Y (2009) Role of alkaline serine protease, asp, in vibrio alginolyticus virulence and regulation of its expression by luxO-luxR regulatory system. J Microbiol Biotechnol 19:431–438
Rutherford ST, Bassler BL (2012) Bacterial quorum sensing: its role in virulence and possibilities for its control. Cold Spring Harb Perspect Med. https://doi.org/10.1101/cshperspect.a012427
Salamone M et al (2015) Comprehensive analysis of a Vibrio parahaemolyticus strain extracellular serine protease VpSP. PLoS ONE 10:e0126349
Scallan E et al (2011) Foodborne illness acquired in the United States–major pathogens. Emerg Infect Dis 17:7–15. https://doi.org/10.3201/eid1701.P11101
Shikuma NJ, Fong JC, Odell LS, Perchuk BS, Laub MT, Yildiz FH (2009) Overexpression of VpsS, a hybrid sensor kinase, enhances biofilm formation in Vibrio cholerae. J Bacteriol 191:5147–5158. https://doi.org/10.1128/jb.00401-09
Shinoda S (2011) Sixty years from the discovery of Vibrio parahaemolyticus and some recollections. Biocontrol Sci 16:129–137
Somorin Y, Bouchard G, Gallagher J, Abram F, Brennan F, O’Byrne C (2017) Roles for RpoS in survival of Escherichia coli during protozoan predation and in reduced moisture conditions highlight its importance in soil environments. FEMS Microbiol Lett. https://doi.org/10.1093/femsle/fnx198
Srivastava D, Harris RC, Waters CM (2011) Integration of cyclic di-GMP and quorum sensing in the control of vpsT and aphA in Vibrio cholerae. J Bacteriol 193:6331–6341. https://doi.org/10.1128/jb.05167-11
Sun F et al (2012) Molecular characterization of direct target genes and cis-acting consensus recognized by quorum-sensing regulator AphA in Vibrio parahaemolyticus. PLoS ONE 7:e44210
Tran L, Nunan L, Redman RM, Mohney LL, Pantoja CR, Fitzsimmons K, Lightner DV (2013) Determination of the infectious nature of the agent of acute hepatopancreatic necrosis syndrome affecting penaeid shrimp. Dis Aquat Org 105:45–55
van Kessel JC, Rutherford ST, Shao Y, Utria AF, Bassler BL (2013) Individual and combined roles of the master regulators AphA and LuxR in control of the Vibrio harveyi quorum-sensing regulon. J Bacteriol 195:436–443. https://doi.org/10.1128/jb.01998-12
Wang F et al (2011a) Prevalence and antimicrobial susceptibility of major foodborne pathogens in imported seafood. J Food Prot 74:1451–1461
Wang H, Wu J-H, Ayala JC, Benitez JA, Silva AJ (2011b) Interplay among cyclic diguanylate, HapR, and the general stress response regulator (RpoS) in the regulation of Vibrio cholerae hemagglutinin/protease. J Bacteriol 193:6529–6538
Wang L et al (2013a) AphA is required for biofilm formation, motility, and virulence in pandemic Vibrio parahaemolyticus. Int J Food Microbiol 160:245–251
Wang L et al (2013b) Cell density-and quorum sensing-dependent expression of type VI secretion system 2 in Vibrio parahaemolyticus. PLoS ONE 8:e73363
Watanabe H, Miyoshi S-i, Kawase T, Tomochika K-i, Shinoda S (2004) High growing ability of Vibrio vulnificus biotype 1 is essential for production of a toxic metalloprotease causing systemic diseases in humans. Microbial Pathog 36:117–123
Wei Y, Perez LJ, Ng WL, Semmelhack MF, Bassler BL (2011) Mechanism of Vibrio cholerae autoinducer-1 biosynthesis. ACS Chem Biol 6:356–365. https://doi.org/10.1021/cb1003652
Wu Y, Wen J, Ma Y, Ma X, Chen Y (2014) Epidemiology of foodborne disease outbreaks caused by Vibrio parahaemolyticus, China, 2003–2008. Food Control 46:197–202
Yu M-S, Lee C-Y (1999) Expression and characterization of the prtV gene encoding a collagenase from Vibrio parahaemolyticus in Escherichia coli. Microbiology 145:143–150
Yu M-S, Yap M-N, Lee C-Y (2000) Metal content and biochemical analyses of a recombinant collagenase PrtV from Vibrio parahaemolyticus. Microbiol Immunol 44:805–813
Zamorano-Sanchez D, Fong JC, Kilic S, Erill I, Yildiz FH (2015) Identification and characterization of VpsR and VpsT binding sites in Vibrio cholerae. J Bacteriol 197:1221–1235. https://doi.org/10.1128/jb.02439-14
Zhang L, Krachler AM, Broberg CA, Li Y, Mirzaei H, Gilpin CJ, Orth K (2012a) Type III effector VopC mediates invasion for Vibrio species. Cell Rep 1:453–460
Zhang Y, Qiu Y, Tan Y, Guo Z, Yang R, Zhou D (2012b) Transcriptional regulation of opaR, qrr2–4 and aphA by the master quorum-sensing regulator OpaR in Vibrio parahaemolyticus. PLoS ONE 7:e34622
Zhang YZ, Ran LY, Li CY, Chen XL (2015) Diversity, structures, and collagen-degrading mechanisms of bacterial collagenolytic proteases. Appl Environ Microbiol 81:6098–6107. https://doi.org/10.1128/aem.00883-15
Zhang H et al (2018) Application of a phage in decontaminating Vibrio parahaemolyticus in oysters. Int J Food Microbiol 275:24–31. https://doi.org/10.1016/j.ijfoodmicro.2018.03.027
Zhou D et al (2013) Quorum sensing modulates transcription of cpsQ-mfpABC and mfpABC in Vibrio parahaemolyticus. Int J Food Microbiol 166:458–463
Acknowledgements
We apologize to colleagues whose research is omitted here. Work in our laboratory has been supported by the National Natural Science Foundation of China (31671290, 81601809, and 31471184) and the Natural Science Foundation of Jiangsu Province (BK20160505).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
We have no conflict of interest situation to disclose.
Rights and permissions
About this article
Cite this article
Osei-Adjei, G., Huang, X. & Zhang, Y. The extracellular proteases produced by Vibrio parahaemolyticus. World J Microbiol Biotechnol 34, 68 (2018). https://doi.org/10.1007/s11274-018-2453-4
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11274-018-2453-4