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The role of Vibrio vulnificus virulence factors and regulators in its infection-induced sepsis

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Abstract

Due to the development of Marine aquaculture, infections caused by Vibrio vulnificus are common all over the world. Symptoms of V. vulnificus infection vary from gastrointestinal illness to septicemia. After infection with V. vulnificus, some patients showed gastrointestinal symptoms, including vomiting, fever, diarrhea, and so on. Others appeared wound infection at the site of contact with bacteria, and even developed sepsis. Once it develops into sepsis, the prognosis of patients is very poor. However, its underlying pathogenic mechanism remains largely undetermined. Growing evidence shows that it can induce primary septicemia mainly via essential virulence factors and regulators. Therefore, it is important to identify the factors that play roles in sepsis. In this review, we systematically expounded the role of V. vulnificus virulence factors and regulators in its infection-induced sepsis in order to provide useful information for the treatment and prevention of V. vulnificus.

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References

  • Actis LA, Tolmasky ME, Crosa LM, Crosa JH (1995) Characterization and regulation of the expression of FatB, an iron transport protein encoded by the pJM1 virulence plasmid. Mol Microbiol 17:197–204

    CAS  PubMed  Google Scholar 

  • Alice AF, Crosa JH (2012) The TonB3 system in the human pathogen Vibrio vulnificus is under the control of the global regulators Lrp and cyclic AMP receptor protein. J Bacteriol 194:1897–1911

    CAS  PubMed  PubMed Central  Google Scholar 

  • Antunes LC, Ferreira RB, Buckner MM et al (2010) Quorum sensing in bacterial virulence. Microbiology 156:2271–2282

    CAS  PubMed  Google Scholar 

  • Busenlehner LS, Weng TC, Penner-Hahn JE et al (2002) Elucidation of primary (alpha(3)N) and vestigial (alpha(5)) heavy metal-binding sites in Staphylococcus aureus pI258 CadC: evolutionary implications for metal ion selectivity of ArsR/SmtB metal sensor proteins. J Mol Biol 319:685–701

    CAS  PubMed  Google Scholar 

  • Cheng JC, Shao CP, Hor LI (1996) Cloning and nucleotide sequencing of the protease gene of Vibrio vulnificus. Gene 183:255–257

    CAS  PubMed  Google Scholar 

  • Choi HK, Park NY, Kim DI, Chung HJ, Ryu S, Choi SH (2002) Promoter analysis and regulatory characteristics of vvhBA encoding cytolytic hemolysin of Vibrio vulnificus. J Biol Chem 277:47292–47299

    CAS  PubMed  Google Scholar 

  • Chuang YC, Sheu HM, Ko WC, Chang TM, Chang MC, Huang KY (1997) Mouse skin damage caused by cytolysin from Vibrio vulnificus and by V. vulnificus infection. J Formos Med Assoc 96:677–684

    CAS  PubMed  Google Scholar 

  • Dhakal BK, Lee W, Kim YR et al (2006) Caenorhabditis elegans as a simple model host for Vibrio vulnificus infection. Biochem Biophys Res Commun 346:751–757

    CAS  PubMed  Google Scholar 

  • Eicken C, Pennella MA, Chen X, Koshlap KM, VanZile M, Sacchettini JC, Giedroc DP (2003) A metal–ligand-mediated intersubunit allosteric switch in related SmtB/ArsR zinc sensor proteins. J Mol Biol 333:683–695

    CAS  PubMed  Google Scholar 

  • El Chaer F, Holtzman NG, Baer MR et al (2018) Sickle cell disease complicated by Iron overload: an under-recognized risk factor for Vibrio vulnificus infection. Acta Haematol 139:199–200

    PubMed  Google Scholar 

  • Elgaml A, Miyoshi SI (2017) Regulation systems of protease and hemolysin production in Vibrio vulnificus. Microbiol Immunol 61:1–11

    CAS  PubMed  Google Scholar 

  • Elgaml A, Higaki K, Miyoshi S (2014a) Effects of temperature, growth phase and luxO-disruption on regulation systems of toxin production in Vibrio vulnificus strain L-180, a human clinical isolate. World J Microbiol Biotechnol 30:681–691

    CAS  PubMed  Google Scholar 

  • Elgaml A, Higaki K, Miyoshi S (2014b) Effects of temperature, growth phase and luxO-disruption on regulation systems of toxin production in Vibrio vulnificus strain L-180, a human clinical isolate. World J Microbiol Biotechnol 30:681–691

    CAS  PubMed  Google Scholar 

  • Garrett SB, Garrison-Schilling KL, Cooke JT, Pettis GS (2016) Capsular polysaccharide production and serum survival of Vibrio vulnificus are dependent on antitermination control by RfaH. FEBS Lett 590:4564–4572

    CAS  PubMed  Google Scholar 

  • Garrison-Schilling KL, Grau BL, McCarter KS, Olivier BJ, Comeaux NE, Pettis GS (2011) Calcium promotes exopolysaccharide phase variation and biofilm formation of the resulting phase variants in the human pathogen Vibrio vulnificus. Environ Microbiol 13:643–654

    CAS  PubMed  Google Scholar 

  • Gavin HE, Satchell KJF (2018) RRSP and RID effector domains dominate virulence impact of Vibrio vulnificus MARTX toxin. J Infect Dis 219:889–897

    PubMed Central  Google Scholar 

  • Görke B, Stülke J (2008) Carbon catabolite repression in bacteria: many ways to make the most out of nutrients. Nat Rev Microbiol 6:613–624

    PubMed  Google Scholar 

  • Gray LD, Kreger AS (1985) Purification and characterization of an extracellular cytolysin produced by Vibrio vulnificus. Infect Immun 48:62–72

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gray LD, Kreger AS (1987) Mouse skin damage caused by cytolysin from Vibrio vulnificus and by V. vulnificus infection. J Infect Dis 155:236–241

    CAS  PubMed  Google Scholar 

  • Guo RH, Lim JY, Tra My DN et al (2018) Vibrio vulnificus RtxA1 toxin expression upon contact with host cells is RpoS-dependent. Front Cell Infect Microbiol 8:70

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guo RH, Im YJ, Shin SI, Jeong K, Rhee JH, Kim YR (2019) Vibrio vulnificus RtxA1 cytotoxin targets filamin A to regulate PAK1- and MAPK-dependent cytoskeleton reorganization and cell death. Emerg Microbes Infect 8:934–945

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ha C, Kim SK, Lee MN et al (2014) Quorum sensing-dependent metalloprotease VvpE is important in the virulence of Vibrio vulnificus to invertebrates. Microb Pathog 71-72:8–14

    CAS  PubMed  Google Scholar 

  • Henke JM, Bassler BL (2004) Bacterial social engagements. Trends Cell Biol 14:648–656

    CAS  PubMed  Google Scholar 

  • Hoffmann E, Dittrich-Breiholz O, Holtmann H, Kracht M (2002) Multiple control of interleukin-8 gene expression. J Leukoc Biol 72:847–855

    CAS  PubMed  Google Scholar 

  • Hollis DG, Weaver RE, Baker CN, Thornsberry C (1976) Halophilic Vibrio species isolated from blood cultures. J Clin Microbiol 3:425–431

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hsueh PR, Lin CY, Tang HJ et al (2004) Vibrio vulnificus in Taiwan. Emerg Infect Dis 10:1363–1368

    PubMed  PubMed Central  Google Scholar 

  • Imdad S, Batool N, Pradhan S et al (2018a) Identification of 2′,4′-dihydroxychalcone as an antivirulence agent targeting HlyU, a master virulence regulator in Vibrio vulnificus. Molecules 23(6)

    PubMed Central  Google Scholar 

  • Imdad S, Chaurasia AK, Kim KK (2018b) Identification and validation of an antivirulence agent targeting HlyU-regulated virulence in Vibrio vulnificus. Front Cell Infect Microbiol 8:152

    PubMed  PubMed Central  Google Scholar 

  • Jeong HG, Choi SH (2008) Evidence that AphB, essential for the virulence of Vibrio vulnificus, is a global regulator. J Bacteriol 190:3768–3773

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jeong HG, Satchell KJ (2012) Additive function of Vibrio vulnificus MARTX (Vv) and VvhA cytolysins promotes rapid growth and epithelial tissue necrosis during intestinal infection. PLoS Pathog 8:e1002581

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jeong HS, Lee MH, Lee KH, Park SJ, Choi SH (2003) SmcR and cyclic AMP receptor protein coactivate Vibrio vulnificus vvpE encoding elastase through the RpoS-dependent promoter in a synergistic manner. J Biol Chem 278:45072–45081

    CAS  PubMed  Google Scholar 

  • Jeong HS, Kim SM, Lim MS, Kim KS, Choi SH (2010) Direct interaction between quorum-sensing regulator SmcR and RNA polymerase is mediated by integration host factor to activate vvpE encoding elastase in Vibrio vulnificus. J Biol Chem 285:9357–9366

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kashimoto T, Akita T, Kado T et al (2017) Both polarity and aromatic ring in the side chain of tryptophan 246 are involved in binding activity of Vibrio vulnificus hemolysin to target cells. Microb Pathog 109:71–77

    CAS  PubMed  Google Scholar 

  • Kaus K, Lary JW, Cole JL, Olson R (2014) Glycan specificity of the Vibrio vulnificus hemolysin lectin outlines evolutionary history of membrane targeting by a toxin family. J Mol Biol 426:2800–2812

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kawase T, Miyoshi S, Sultan Z, Shinoda S (2004) Regulation system for protease production in Vibrio vulnificus. FEMS Microbiol Lett 240:55–59

    CAS  PubMed  Google Scholar 

  • Kawase T, Miura F, Debnath A, Imakura K, Miyoshi SI (2018) Functional analysis of N-terminal propeptide in the precursor of Vibrio vulnificus metalloprotease by using cell-free translational system. Protein Expr Purif 149:13–16

    CAS  PubMed  Google Scholar 

  • Kim BS, Kim JS (2002) Cholesterol induce oligomerization of Vibrio vulnificus cytolysin specifically. Exp Mol Med 34:239–242

    CAS  PubMed  Google Scholar 

  • Kim YR, Kim SY, Kim CM et al (2005) Essential role of an adenylate cyclase in regulating Vibrio vulnificus virulence. FEMS Microbiol Lett 243:497–503

    CAS  PubMed  Google Scholar 

  • Kim CM, Park YJ, Choi MH et al (2007a) Ferrophilic characteristics of Vibrio vulnificus and potential usefulness of iron chelation therapy. J Infect Dis 195:90–98

    CAS  PubMed  Google Scholar 

  • Kim HY, Chang AK, Park JE et al (2007b) Procaspase-3 activation by a metalloprotease secreted from Vibrio vulnificus. Int J Mol Med 20:591–595

    CAS  PubMed  Google Scholar 

  • Kim YR, Kim BU, Kim SY, Kim CM, Na HS, Koh JT, Choy HE, Rhee JH, Lee SE (2010) Outer membrane vesicles of Vibrio vulnificus deliver cytolysin-hemolysin VvhA into epithelial cells to induce cytotoxicity. Biochem Biophys Res Commun 399:607–612

    CAS  PubMed  Google Scholar 

  • Kim BS, Hwang J, Kim MH, Choi SH (2011a) Cooperative regulation of the Vibrio vulnificus nan gene cluster by NanR protein, cAMP receptor protein, and N-acetylmannosamine 6-phosphate. J Biol Chem 286:40889–40899

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kim BS, Hwang J, Kim MH, Choi SH (2011b) Cooperative regulation of the Vibrio vulnificus nan gene cluster by NanR protein, cAMP receptor protein, and N-acetylmannosamine 6-phosphate. J Biol Chem 286:40889–40899

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kim SP, Kim CM, Shin SH (2012a) Cyclic AMP and cyclic AMP-receptor protein modulate the autoinducer-2-mediated quorum sensing system in Vibrio vulnificus. Curr Microbiol 65:701–710

    CAS  PubMed  Google Scholar 

  • Kim WB, Lee BC, Choi SH (2012b) Vibrio vulnificus AphB is involved in interleukin-8 production via an NF-κB-dependent pathway in human intestinal epithelial cells. Biochem Biophys Res Commun 417:1265–1270

    CAS  PubMed  Google Scholar 

  • Kim IH, Wen Y, Son JS, Lee KH, Kim KS (2013a) The fur-iron complex modulates expression of the quorum-sensing master regulator, SmcR, to control expression of virulence factors in Vibrio vulnificus. Infect Immun 81:2888–2898

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kim SM, Park JH, Lee HS, Kim WB, Ryu JM, Han HJ, Choi SH (2013b) LuxR homologue SmcR is essential for Vibrio vulnificus pathogenesis and biofilm detachment, and its expression is induced by host cells. Infect Immun 81:3721–3730

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kim YR, Lee SE, Kim B et al (2013c) A dual regulatory role of cyclic adenosine monophosphate receptor protein in various virulence traits of Vibrio vulnificus. Microbiol Immunol 57:273–280

    CAS  PubMed  Google Scholar 

  • Kim HY, Ayrapetyan M, Oliver JD (2014) Survival of Vibrio vulnificus genotypes in male and female serum, and production of siderophores in human serum and seawater. Foodborne Pathog Dis 11:119–125

    CAS  PubMed  Google Scholar 

  • Kim JA, Park JH, Lee MA, Lee HJ, Park SJ, Kim KS, Choi SH, Lee KH (2015a) Stationary-phase induction of vvpS expression by three transcription factors: repression by LeuO and activation by SmcR and CRP. Mol Microbiol 97:330–346

    CAS  PubMed  Google Scholar 

  • Kim YR, Lee SE, Kim JR et al (2015b) Safety and vaccine efficacy of an attenuated Vibrio vulnificus strain with deletions in major cytotoxin genes. FEMS Microbiol Lett 362:fnv169

    PubMed  Google Scholar 

  • Kovacikova G, Skorupski K (1999) A Vibrio cholera LysR homolog, AphB, cooperates with AphA at the tcpPH promoter to activate expression of the ToxR virulence cascade. J Bacteriol 181:4250–4256

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kwon KB, Yang JY, Ryu DG et al (2001) Vibrio vulnificus cytolysin induces superoxide anion-initiated apoptotic signaling pathway in human ECV304 cells. J Biol Chem 276:47518–47523

    CAS  PubMed  Google Scholar 

  • Kwon JY, Chang AK, Park JE, Shin SY, Yoon SM, Lee JS (2007) Vibrio extracellular protease with prothrombin activation and fibrinolytic activities. Int J Mol Med 19:157–163

    CAS  PubMed  Google Scholar 

  • Lee SE, Ryu PY, Kim SY, Kim YR, Koh JT, Kim OJ, Chung SS, Choy HE, Rhee JH (2004) Production of Vibrio vulnificus hemolysin in vivo and its pathogenic significance. Biochem Biophys Res Commun 324:86–91

    CAS  PubMed  Google Scholar 

  • Lee JH, Kim MW, Kim BS et al (2007) Identification and characterization of the Vibrio vulnificus RtxA essential for cytotoxicity in vitro and virulence in mice. J Microbiol 45:146–152

    CAS  PubMed  Google Scholar 

  • Lee KM, Yoon MY, Park Y, Lee JH, Yoon SS (2011) Anaerobiosis-induced loss of cytotoxicity is due to inactivation of quorum sensing in Pseudomonas aeruginosa. Infect Immun 79:2792–2800

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lee MA, Kim JA, Yang YJ et al (2014a) VvpM, an extracellular metalloprotease of Vibrio vulnificus, induces apoptotic death of human cells. J Microbiol 52:1036–1043

    CAS  PubMed  Google Scholar 

  • Lee TH, Cha SS, Lee CS et al (2014b) Monoclonal antibodies against Vibrio vulnificus RtxA1 elicit protective immunity through distinct mechanisms. Infect Immun 82:4813–4823

    PubMed  PubMed Central  Google Scholar 

  • Lee SJ, Jung YH, Oh SY et al (2015a) Vibrio vulnificus VvpE inhibits mucin 2 expression by hypermethylation via lipid raft-mediated ROS signaling in intestinal epithelial cells. Cell Death Dis 6:e1787

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lee SJ, Jung YH, Song EJ et al (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

    CAS  PubMed  Google Scholar 

  • Lee SJ, Jung YH, Ryu JM, Jang KK, Choi SH, Han HJ (2016) VvpE mediates the intestinal colonization of Vibrio vulnificus by the disruption of tight junctions. Int J Med Microbiol 306:10–19

    CAS  PubMed  Google Scholar 

  • Lee SJ, Lee HJ, Jung YH et al (2018) Melatonin inhibits apoptotic cell death induced by Vibrio vulnificus VvhA via melatonin receptor 2 coupling with NCF-1. Cell Death Dis 9:48

    PubMed  PubMed Central  Google Scholar 

  • Li X, Zhou Y, Jiang Q, Yang H et al (2019) Virulence properties of Vibrio vulnificus isolated from diseased zoea of freshness shrimp Macrobrachium rosenbergii. Microb Pathog 127:166–171

    CAS  PubMed  Google Scholar 

  • Litwin CM, Byrne BL (1998) Cloning and characterization of an outer membrane protein of Vibrio vulnificus required for heme utilization: regulation of expression and determination of the gene sequence. Infect Immun 66:3134–3141

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu M, Crosa JH (2012) The regulator HlyU, the repeat-in-toxin gene rtxA1, and their roles in the pathogenesis of Vibrio vulnificus infections. Microbiologyopen. 1:502–513

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu T, Golden JW, Giedroc DP (2005) A zinc (II)/lead (II)/cadmium (II)-inducible operon from the Cyanobacterium anabaena is regulated by AztR, an alpha3N ArsR/SmtB metalloregulator. Biochemistry. 44:8673–8683

    CAS  PubMed  Google Scholar 

  • Liu M, Alice AF, Naka H, Crosa JH (2007) The HlyU protein is a positive regulator of rtxA1, a gene responsible for cytotoxicity and virulence in the human pathogen Vibrio vulnificus. Infect Immun 75:3282–3289

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu M, Naka H, Crosa JH (2009) HlyU acts as an H-NS antirepressor in the regulation of the RTX toxin gene essential for the virulence of the human pathogen Vibrio vulnificus CMCP6. Mol Microbiol 72:491–505

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu M, Rose M, Crosa JH (2011) Homodimerization and binding of specific domains to the target DNA are essential requirements for HlyU to regulate expression of the virulence gene rtxA1, encoding the repeat-in-toxin protein in the human pathogen Vibrio vulnificus. J Bacteriol 193:6895–6901

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lo HR, Lin JH, Chen YH, Chen CL, Shao CP, Lai YC, Hor LI (2011) RTX toxin enhances the survival of Vibrio vulnificus during infection by protecting the organism from phagocytosis. J Infect Dis 203:1866–1874

    CAS  PubMed  Google Scholar 

  • Lohith GK, Kingston JJ, Singh AK et al (2015) Evaluation of recombinant leukocidin domain of VvhA exotoxin of Vibrio vulnificus as an effective toxoid in mouse model. Immunol Lett 167:47–53

    CAS  PubMed  Google Scholar 

  • López-Pérez M, Jayakumar JM, Haro-Moreno JM et al (2019) Evolutionary model of cluster divergence of the emergent marine pathogen Vibrio vulnificus: from genotype to ecotype. MBio 10

  • Maruo K, Akaike T, Ono T et al (1998) Involvement of bradykinin generation in intravascular dissemination of Vibrio vulnificus and prevention of invasion by a bradykinin antagonist. Infect Immun 66:866–869

    CAS  PubMed  PubMed Central  Google Scholar 

  • McDougald D, Rice SA, Kjelleberg S (2001) SmcR-dependent regulation of adaptive phenotypes in Vibrio vulnificus. J Bacteriol 183:758–762

    CAS  PubMed  PubMed Central  Google Scholar 

  • Menon MP, Yu PA, Iwamoto M, Painter J (2014) Pre-existing medical conditions associated with Vibrio vulnificus septicaemia. Epidemiol Infect 142:878–881

    CAS  PubMed  Google Scholar 

  • Miyoshi S (2013) Extracellular proteolytic enzymes produced by human pathogenic vibrio species. Front Microbiol:4339

  • Miyoshi N, Miyoshi S, Sugiyama K, Suzuki Y, Furuta H, Shinoda S (1987) Activation of the plasma kallikrein-kinin system by Vibrio vulnificus protease. Infect Immun 55:1936–1939

    CAS  PubMed  PubMed Central  Google Scholar 

  • Miyoshi S, Abe Y, Senoh M, Mizuno T, Maehara Y, Nakao H (2011) Inactivation of Vibrio vulnificus hemolysin through mutation of the N- or C-terminus of the lectin-like domain. Toxicon 57:904–908

    CAS  PubMed  Google Scholar 

  • Miyoshi S, 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

    CAS  PubMed  Google Scholar 

  • Neupane GP, Kim DM (2009) Comparison of the effects of deferasirox, deferiprone, and deferoxamine on the growth and virulence of Vibrio vulnificus. Transfusion 49(8):1762–1769

    CAS  PubMed  Google Scholar 

  • Ng WL, Bassler BL (2009) Bacterial quorum-sensing network architectures. Annu Rev Genet 43:197–222

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nishi K, Lee HJ, Park SY (2010a) Crystal structure of the transcriptional activator HlyU from Vibrio vulnificus CMCP6. FEBS Lett 584:1097–1102

    CAS  PubMed  Google Scholar 

  • Nishi K, Lee HJ, Park SY et al (2010b) Crystal structure of the transcriptional activator HlyU from Vibrio vulnificus CMCP6. FEBS Lett 584:1097–1102

    CAS  PubMed  Google Scholar 

  • Oh MH, Lee SM, Lee DH, Choi SH (2009) Regulation of the Vibrio vulnificus hupA gene by temperature alteration and cyclic AMP receptor protein and evaluation of its role in virulence. Infect Immun 77:1208–1215

    CAS  PubMed  PubMed Central  Google Scholar 

  • Oliver JD (2015) The biology of Vibrio vulnificus. Microbiol Spectr 3

  • Oliver JD, Wear JE, Thomas MB et al (1986) Production of extracellular enzymes and cytotoxicity by Vibrio vulnificus. Diagn Microbiol Infect Dis 5:99–111

    CAS  PubMed  Google Scholar 

  • Ottemann KM, Miller JF (1997) Role for motility in bacterial-host interactions. Mol Microbiol 24:1109–1117

    CAS  PubMed  Google Scholar 

  • Pajuelo D, Hernández-Cabanyero C, Sanjuan E, Lee CT, Silva-Hernández FX, Hor LI, MacKenzie S, Amaro C (2016) Iron and Fur in the life cycle of the zoonotic pathogen Vibrio vulnificus. Environ Microbiol 18:4005–4022

    CAS  PubMed  Google Scholar 

  • Park JW, Ma SN, Song ES et al (1996) Pulmonary damage by Vibrio vulnificus cytolysin. Infect Immun 64:2873–2876

    CAS  PubMed  PubMed Central  Google Scholar 

  • Park KH, Kim JS, Lee YR et al (2007) Low-density lipoprotein protects Vibrio vulnificus-induced lethality through blocking lipopolysaccharide action. Exp Mol Med 9:673–678

    Google Scholar 

  • Park N, Song S, Choi G, Jang KK, Jo I, Choi SH, Ha NC (2017) Crystal structure of the regulatory domain of AphB from Vibrio vulnificus, a virulence gene regulator. Mol Cells 40:299–306

    CAS  PubMed  PubMed Central  Google Scholar 

  • Petersen S, Young GM (2002) Essential role for cyclic AMP and its receptor protein in Yersinia enterocolitica virulence. Infect Immun 70:3665–3672

    CAS  PubMed  PubMed Central  Google Scholar 

  • Raz N, Danin-Poleg Y, Hayman RB et al (2014) Genome-wide SNP-genotyping array to study the evolution of the human pathogen Vibrio vulnificus biotype 3. PLoS One 9:e114576

    PubMed  PubMed Central  Google Scholar 

  • Roh JB, Lee MA, Lee HJ et al (2006) Transcriptional regulatory cascade for elastase production in Vibrio vulnificus: LuxO activates luxT expression and LuxT represses smcR expression. J Biol Chem 281:34775–34784

    CAS  PubMed  Google Scholar 

  • Ryu Y, Kim YJ, Kim YR, Seok YJ (2012) Expression of Vibrio vulnificus insulin-degrading enzyme is regulated by the cAMP-CRP complex. Microbiology 158:1294–1303

    CAS  PubMed  Google Scholar 

  • Saffarini DA, Schultz R, Beliaev A (2003) Involvement of cyclic AMP (cAMP) and cAMP receptor protein in anaerobic respiration of Shewanella oneidensis. J Bacteriol 185:3668–3671

    CAS  PubMed  PubMed Central  Google Scholar 

  • Senoh M, Miyoshi S, Okamoto K, Fouz B, Amaro C, Shinoda S (2005) The cytotoxin-hemolysin genes of human and eel pathogenic Vibrio vulnificus strains: comparison of nucleotide sequences and application to genetic grouping. Microbiol Immunol 49:513–519

    CAS  PubMed  Google Scholar 

  • Septer AN, Lyell NL, Stabb EV (2013) The iron-dependent regulator fur controls pheromone signaling systems and luminescence in the squid symbiont Vibrio fischeri ES114. Appl Environ Microbiol 79:1826–1834

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shao CP, Lo HR, Lin JH, Hor LI (2011) Regulation of cytotoxicity by quorum-sensing signaling in Vibrio vulnificus is mediated by SmcR, a repressor of hlyU. J Bacteriol 193:2557–2565

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sheer AJ, Kline KP, Lo MC (2017) From sea to bloodstream: Vibrio vulnificus sepsis. Am J Med 130:1167–1169

    PubMed  Google Scholar 

  • Song EJ, Lee SJ, Lim HS et al (2016) Vibrio vulnificus VvhA induces autophagy-related cell death through the lipid raft-dependent c-Src/NOX signaling pathway. Sci Rep 6:27080

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stefanova D, Raychev A, Arezes et al (2017) Endogenous hepcidin and its agonist mediate resistance to selected infections by clearing non-transferrin-bound iron. Blood 130:245–257

    CAS  PubMed  PubMed Central  Google Scholar 

  • Strasser A, Jost PJ, Nagata S (2009) The many roles of FAS receptor signaling in the immune system. Immunity 30:180–192

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sugiyama H, Kashimoto T, Ueno S et al (2011) Relationship between localization on cellular membranes and cytotoxicity of Vibrio vulnificus hemolysin. PLoS One 6:e26018

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sugiyama H, Kashimoto T, Ueno S et al (2013) Inhibition of binding of Vibrio vulnificus hemolysin (VVH) by MβCD. J Vet Med Sci 75:649–652

    CAS  PubMed  Google Scholar 

  • Wen Y, Kim IH, Kim KS (2016) Iron- and quorum-sensing signals converge on small quorum-regulatory RNAs for coordinated regulation of virulence factors in Vibrio vulnificus. J Biol Chem 291:14213–14230

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wright AC, Morris JG Jr, Maneval DR Jr et al (1985) Cloning of the cytotoxin-hemolysin gene of Vibrio vulnificus. Infect Immun 50:922–924

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshimura H, Yanagisawa S, Kanehisa M, Ohmori M (2002) Screening for the target gene of cyanobacterial cAMP receptor protein SYCRP1. Mol Microbiol 43:843–853

    CAS  PubMed  Google Scholar 

  • Yu HN, Lee YR, Park KH, Rah SY, Noh EM, Song EK, Han MK, Kim BS, Lee SH, Kim JS (2007) Membrane cholesterol is required for activity of Vibrio vulnificus cytolysin. Arch Microbiol 187:467–473

    CAS  PubMed  Google Scholar 

  • Yun JH, Kim H, Park JE, Lee JS, Lee W (2013) Solution structure and dynamics of C-terminal regulatory domain of Vibrio vulnificus extracellular metalloprotease. Biochem Biophys Res Commun 430:541–546

    CAS  PubMed  Google Scholar 

  • Ziolo KJ, Jeong HG, Kwak JS et al (2014) Vibrio vulnificus biotype 3 multifunctional autoprocessing RTX toxin is an adenylate cyclase toxin essential for virulence in mice. Infect Immun 82:2148–2157

    PubMed  PubMed Central  Google Scholar 

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Funding

This work was supported by Primary Research & Development Plan of Shandong Province (No. 2016GSF121036).

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Correspondence to Ming-Yi Wang.

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Li, G., Wang, MY. The role of Vibrio vulnificus virulence factors and regulators in its infection-induced sepsis. Folia Microbiol 65, 265–274 (2020). https://doi.org/10.1007/s12223-019-00763-7

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  • DOI: https://doi.org/10.1007/s12223-019-00763-7

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