Vibrio cholerae Biofilms and Cholera Pathogenesis

PLoS Neglected Tropical Diseases

Volumn 10, Issue 2, 2016, Pages

  Silva, Anisia J ^a   Benitez, Jorge A ^a  

^a MOREHOUSE SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE LIKE NUCLEOID STRUCTURING PROTEIN; VIRULENCE FACTOR;

BIOFILM; CARBON SOURCE; CELLULAR STRESS RESPONSE; CHOLERA; DIMERIZATION; DISEASE TRANSMISSION; GENE DELETION; GENE EXPRESSION; MICROBIAL COLONIZATION; NONHUMAN; NUTRIENT LIMITATION; QUORUM SENSING; REVIEW; VIBRIO CHOLERAE; VIRUS PATHOGENESIS; BIOSYNTHESIS; GASTROINTESTINAL TRACT; GROWTH, DEVELOPMENT AND AGING; HUMAN; MICROBIOLOGY; PHYSIOLOGY; VIRULENCE;

BIOFILMS; CHOLERA; GASTROINTESTINAL TRACT; HUMANS; VIBRIO CHOLERAE; VIRULENCE; VIRULENCE FACTORS;

EID: 84959284597     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0004330     Document Type: Review

References (191)

1. Alam M, Hasan NA, Sadique A, Bhuiyan NA, Ahmed KU, Nusrin S, et al. Seasonal cholera caused by Vibrio cholerae serogroups O1 and O139 in the coastal aquatic environment of Bangladesh. Applied and environmental microbiology. 2006;72(6):4096–104. Epub 2006/06/06. doi: 10.1128/AEM.00066-0616751520; PubMed Central PMCID: PMC1489596.
2. Alam M, Islam A, Bhuiyan NA, Rahim N, Hossain A, Khan GY, et al. Clonal transmission, dual peak, and off-season cholera in Bangladesh. Infection ecology & epidemiology. 2011;1. Epub 2011/01/01. doi: 10.3402/iee.v1i0.727322957115; PubMed Central PMCID: PMC3426334.
3. Colwell RR, Infectious disease and environment: cholera as a paradigm for waterborne disease. International microbiology: the official journal of the Spanish Society for Microbiology. 2004;7(4):285–9. Epub 2005/01/25. 15666250.
4. Colwell RR, A voyage of discovery: cholera, climate and complexity. Environmental microbiology. 2002;4(2):67–9. Epub 2002/04/26. 11972615.
5. Colwell RR, Global climate and infectious disease: the cholera paradigm. Science. 1996;274(5295):2025–31. Epub 1996/12/20. 8953025.
6. Islam MS, Talukder KA, Khan NH, Mahmud ZH, Rahman MZ, Nair GB, et al. Variation of toxigenic Vibrio cholerae O1 in the aquatic environment of Bangladesh and its correlation with the clinical strains. Microbiology and immunology. 2004;48(10):773–7. Epub 2004/10/27. 15502411.
7. Lipp EK, Huq A, Colwell RR, Effects of global climate on infectious disease: the cholera model. Clinical microbiology reviews. 2002;15(4):757–70. Epub 2002/10/05. 12364378; PubMed Central PMCID: PMC126864.
8. Lobitz B, Beck L, Huq A, Wood B, Fuchs G, Faruque AS, et al. Climate and infectious disease: use of remote sensing for detection of Vibrio cholerae by indirect measurement. Proceedings of the National Academy of Sciences of the United States of America. 2000;97(4):1438–43. Epub 2000/03/04. 10677480; PubMed Central PMCID: PMC26452.
9. Butler SM, Nelson EJ, Chowdhury N, Faruque SM, Calderwood SB, Camilli A, Cholera stool bacteria repress chemotaxis to increase infectivity. Molecular microbiology. 2006;60(2):417–26. Epub 2006/04/01. doi: 10.1111/j.1365-2958.2006.05096.x16573690; PubMed Central PMCID: PMC2754204.
10. Merrell DS, Butler SM, Qadri F, Dolganov NA, Alam A, Cohen MB, et al. Host-induced epidemic spread of the cholera bacterium. Nature. 2002;417(6889):642–5. Epub 2002/06/07. doi: 10.1038/nature0077812050664; PubMed Central PMCID: PMC2776822.
11. Hartley DM, Morris JG, Jr.Smith DL, Hyperinfectivity: a critical element in the ability of V. cholerae to cause epidemics?PLoS medicine. 2006;3(1):e7. Epub 2005/12/02. doi: 10.1371/journal.pmed.003000716318414; PubMed Central PMCID: PMC1298942.
12. Morris JG, Jr.Cholera—modern pandemic disease of ancient lineage. Emerging infectious diseases. 2011;17(11):2099–104. Epub 2011/11/22. doi: 10.3201/eid1711.11110922099113; PubMed Central PMCID: PMC3310593.
13. Kaper JB, Morris JG, Jr.Levine MM, Cholera. Clinical microbiology reviews. 1995;8(1):48–86. Epub 1995/01/01. 7704895; PubMed Central PMCID: PMC172849.
14. Albert MJ, Vibrio cholerae O139 Bengal. Journal of clinical microbiology. 1994;32(10):2345–9. Epub 1994/10/01. 7814463; PubMed Central PMCID: PMC264063.
15. Herrington DA, Hall RH, Losonsky G, Mekalanos JJ, Taylor RK, Levine MM, Toxin, toxin-coregulated pili, and the toxR regulon are essential for Vibrio cholerae pathogenesis in humans. The Journal of experimental medicine. 1988;168(4):1487–92. Epub 1988/10/01. 2902187; PubMed Central PMCID: PMC2189073.
16. Tacket CO, Taylor RK, Losonsky G, Lim Y, Nataro JP, Kaper JB, et al. Investigation of the roles of toxin-coregulated pili and mannose-sensitive hemagglutinin pili in the pathogenesis of Vibrio cholerae O139 infection. Infection and immunity. 1998;66(2):692–5. Epub 1998/02/07. 9453628; PubMed Central PMCID: PMC107958.
17. Thelin KH, Taylor RK, Toxin-coregulated pilus, but not mannose-sensitive hemagglutinin, is required for colonization by Vibrio cholerae O1 El Tor biotype and O139 strains. Infection and immunity. 1996;64(7):2853–6. Epub 1996/07/01. 8698524; PubMed Central PMCID: PMC174155.
18. Waldor MK, Mekalanos JJ, Lysogenic conversion by a filamentous phage encoding cholera toxin. Science. 1996;272(5270):1910–4. Epub 1996/06/28. 8658163.
19. Karaolis DK, Johnson JA, Bailey CC, Boedeker EC, Kaper JB, Reeves PR, A Vibrio cholerae pathogenicity island associated with epidemic and pandemic strains. Proceedings of the National Academy of Sciences of the United States of America. 1998;95(6):3134–9. Epub 1998/04/18. 9501228; PubMed Central PMCID: PMC19707.
20. Kojima S, Yamamoto K, Kawagishi I, Homma M, The polar flagellar motor of Vibrio cholerae is driven by an Na+ motive force. Journal of bacteriology. 1999;181(6):1927–30. Epub 1999/03/12. 10074090; PubMed Central PMCID: PMC93596.
21. Prouty MG, Correa NE, Klose KE, The novel sigma54- and sigma28-dependent flagellar gene transcription hierarchy of Vibrio cholerae. Molecular microbiology. 2001;39(6):1595–609. Epub 2001/03/22. 11260476.
22. Hase CC, Analysis of the role of flagellar activity in virulence gene expression in Vibrio cholerae. Microbiology. 2001;147(Pt 4):831–7. Epub 2001/04/03. 11283279.
23. Hase CC, Mekalanos JJ, Effects of changes in membrane sodium flux on virulence gene expression in Vibrio cholerae. Proceedings of the National Academy of Sciences of the United States of America. 1999;96(6):3183–7. Epub 1999/03/17. 10077658; PubMed Central PMCID: PMC15916.
24. Silva AJ, Leitch GJ, Camilli A, Benitez JA, Contribution of hemagglutinin/protease and motility to the pathogenesis of El Tor biotype cholera. Infection and immunity. 2006;74(4):2072–9. Epub 2006/03/23. doi: 10.1128/IAI.74.4.2072–2079.200616552036; PubMed Central PMCID: PMC1418906.
25. Syed KA, Beyhan S, Correa N, Queen J, Liu J, Peng F, et al. The Vibrio cholerae flagellar regulatory hierarchy controls expression of virulence factors. Journal of bacteriology. 2009;191(21):6555–70. Epub 2009/09/01. doi: 10.1128/JB.00949-0919717600; PubMed Central PMCID: PMC2795290.
26. Wang H, Zhang L, Silva AJ, Benitez JA, A quinazoline-2,4-diamino analog suppresses Vibrio cholerae flagellar motility by interacting with motor protein PomB and induces envelope stress. Antimicrobial agents and chemotherapy. 2013;57(8):3950–9. Epub 2013/06/05. doi: 10.1128/AAC.00473-1323733460; PubMed Central PMCID: PMC3719709.
27. Faruque SM, Nair GB, Molecular ecology of toxigenic Vibrio cholerae. Microbiology and immunology. 2002;46(2):59–66. Epub 2002/04/10. 11939579.
28. Matz C, McDougald D, Moreno AM, Yung PY, Yildiz FH, Kjelleberg S, Biofilm formation and phenotypic variation enhance predation-driven persistence of Vibrio cholerae. Proceedings of the National Academy of Sciences of the United States of America. 2005;102(46):16819–24. Epub 2005/11/04. doi: 10.1073/pnas.050535010216267135; PubMed Central PMCID: PMC1283802.
29. Louis P, O'Byrne CP, Life in the gut: microbial responses to stress in the gastrointestinal tract. Science progress. 2010;93(Pt 1):7–36. Epub 2010/03/13. 20222354.
30. Merrell DS, Tischler AD, Lee SH, Camilli A, Vibrio cholerae requires rpoS for efficient intestinal colonization. Infection and immunity. 2000;68(12):6691–6. Epub 2000/11/18. 11083783; PubMed Central PMCID: PMC97768.
31. Kovacikova G, Skorupski K, The alternative sigma factor sigma(E) plays an important role in intestinal survival and virulence in Vibrio cholerae. Infection and immunity. 2002;70(10):5355–62. Epub 2002/09/14. 12228259; PubMed Central PMCID: PMC128310.
32. Donlan RM, Costerton JW, Biofilms: survival mechanisms of clinically relevant microorganisms. Clinical microbiology reviews. 2002;15(2):167–93. Epub 2002/04/05. 11932229; PubMed Central PMCID: PMC118068.
33. Hall-Stoodley L, Costerton JW, Stoodley P, Bacterial biofilms: from the natural environment to infectious diseases. Nature reviews Microbiology. 2004;2(2):95–108. Epub 2004/03/26. doi: 10.1038/nrmicro82115040259.
34. Moorthy S, Watnick PI, Identification of novel stage-specific genetic requirements through whole genome transcription profiling of Vibrio cholerae biofilm development. Molecular microbiology. 2005;57(6):1623–35. Epub 2005/09/02. doi: 10.1111/j.1365-2958.2005.04797.x16135229; PubMed Central PMCID: PMC2600799.
35. Moorthy S, Watnick PI, Genetic evidence that the Vibrio cholerae monolayer is a distinct stage in biofilm development. Molecular microbiology. 2004;52(2):573–87. Epub 2004/04/07. doi: 10.1111/j.1365-2958.2004.04000.x15066042; PubMed Central PMCID: PMC2501105.
36. Liu Z, Stirling FR, Zhu J, Temporal quorum-sensing induction regulates Vibrio cholerae biofilm architecture. Infection and immunity. 2007;75(1):122–6. Epub 2006/11/01. doi: 10.1128/IAI.01190-0617074850; PubMed Central PMCID: PMC1828391.
37. Wang H, Wu JH, Ayala JC, Benitez JA, Silva AJ, Interplay among cyclic diguanylate, HapR, and the general stress response regulator (RpoS) in the regulation of Vibrio cholerae hemagglutinin/protease. Journal of bacteriology. 2011;193(23):6529–38. Epub 2011/10/04. doi: 10.1128/JB.05166-1121965573; PubMed Central PMCID: PMC3232884.
38. Yildiz FH, Visick KL, Vibrio biofilms: so much the same yet so different. Trends in microbiology. 2009;17(3):109–18. Epub 2009/02/24. doi: 10.1016/j.tim.2008.12.00419231189; PubMed Central PMCID: PMC2729562.
39. Fong JN, Yildiz FH, Biofilm Matrix Proteins. Microbiology spectrum. 2015;3(2). Epub 2015/06/25. doi: 10.1128/microbiolspec.MB-0004-201426104709; PubMed Central PMCID: PMC4480581.
40. Teschler JK, Zamorano-Sanchez D, Utada AS, Warner CJ, Wong GC, Linington RG, et al. Living in the matrix: assembly and control of Vibrio cholerae biofilms. Nature reviews Microbiology. 2015;13(5):255–68. Epub 2015/04/22. doi: 10.1038/nrmicro343325895940; PubMed Central PMCID: PMC4437738.
41. Tischler AD, Camilli A, Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation. Molecular microbiology. 2004;53(3):857–69. Epub 2004/07/17. doi: 10.1111/j.1365-2958.2004.04155.x15255898; PubMed Central PMCID: PMC2790424.
42. Beyhan S, Odell LS, Yildiz FH, Identification and characterization of cyclic diguanylate signaling systems controlling rugosity in Vibrio cholerae. Journal of bacteriology. 2008;190(22):7392–405. Epub 2008/09/16. doi: 10.1128/JB.00564-0818790873; PubMed Central PMCID: PMC2576663.
43. Beyhan S, Yildiz FH, Smooth to rugose phase variation in Vibrio cholerae can be mediated by a single nucleotide change that targets c-di-GMP signalling pathway. Molecular microbiology. 2007;63(4):995–1007. Epub 2007/01/20. doi: 10.1111/j.1365-2958.2006.05568.x17233827.
44. Fong JC, Yildiz FH, Interplay between cyclic AMP-cyclic AMP receptor protein and cyclic di-GMP signaling in Vibrio cholerae biofilm formation. Journal of bacteriology. 2008;190(20):6646–59. Epub 2008/08/19. doi: 10.1128/JB.00466-0818708497; PubMed Central PMCID: PMC2566190.
45. Lim B, Beyhan S, Meir J, Yildiz FH, Cyclic-diGMP signal transduction systems in Vibrio cholerae: modulation of rugosity and biofilm formation. Molecular microbiology. 2006;60(2):331–48. Epub 2006/04/01. doi: 10.1111/j.1365-2958.2006.05106.x16573684.
46. Shikuma NJ, Fong JC, Yildiz FH, Cellular levels and binding of c-di-GMP control subcellular localization and activity of the Vibrio cholerae transcriptional regulator VpsT. PLoS pathogens. 2012;8(5):e1002719. Epub 2012/06/02. doi: 10.1371/journal.ppat.100271922654664; PubMed Central PMCID: PMC3359988.
47. Krasteva PV, Giglio KM, Sondermann H, Sensing the messenger: the diverse ways that bacteria signal through c-di-GMP. Protein science: a publication of the Protein Society. 2012;21(7):929–48. Epub 2012/05/18. doi: 10.1002/pro.209322593024; PubMed Central PMCID: PMC3403432.
48. Tamayo R, Pratt JT, Camilli A, Roles of cyclic diguanylate in the regulation of bacterial pathogenesis. Annual review of microbiology. 2007;61:131–48. Epub 2007/05/08. doi: 10.1146/annurev.micro.61.080706.09342617480182; PubMed Central PMCID: PMC2776827.
49. Srivastava D, Hsieh ML, Khataokar A, Neiditch MB, Waters CM, Cyclic di-GMP inhibits Vibrio cholerae motility by repressing induction of transcription and inducing extracellular polysaccharide production. Molecular microbiology. 2013;90(6):1262–76. Epub 2013/10/19. doi: 10.1111/mmi.1243224134710; PubMed Central PMCID: PMC3881292.
50. Yildiz FH, Dolganov NA, Schoolnik GK, VpsR, a Member of the Response Regulators of the Two-Component Regulatory Systems, Is Required for Expression of vps Biosynthesis Genes and EPS(ETr)-Associated Phenotypes in Vibrio cholerae O1 El Tor. Journal of bacteriology. 2001;183(5):1716–26. Epub 2001/02/13. doi: 10.1128/JB.183.5.1716–1726.200111160103; PubMed Central PMCID: PMC95057.
51. Casper-Lindley C, Yildiz FH, VpsT is a transcriptional regulator required for expression of vps biosynthesis genes and the development of rugose colonial morphology in Vibrio cholerae O1 El Tor. Journal of bacteriology. 2004;186(5):1574–8. Epub 2004/02/20. 14973043; PubMed Central PMCID: PMC344397.
52. Krasteva PV, Fong JC, Shikuma NJ, Beyhan S, Navarro MV, Yildiz FH, et al. Vibrio cholerae VpsT regulates matrix production and motility by directly sensing cyclic di-GMP. Science. 2010;327(5967):866–8. Epub 2010/02/13. doi: 10.1126/science.118118520150502; PubMed Central PMCID: PMC2828054.
53. Pratt JT, Tamayo R, Tischler AD, Camilli A, PilZ domain proteins bind cyclic diguanylate and regulate diverse processes in Vibrio cholerae. The Journal of biological chemistry. 2007;282(17):12860–70. Epub 2007/02/20. doi: 10.1074/jbc.M61159320017307739; PubMed Central PMCID: PMC2790426.
54. Yildiz FH, Schoolnik GK, Vibrio cholerae O1 El Tor: identification of a gene cluster required for the rugose colony type, exopolysaccharide production, chlorine resistance, and biofilm formation. Proceedings of the National Academy of Sciences of the United States of America. 1999;96(7):4028–33. Epub 1999/03/31. 10097157; PubMed Central PMCID: PMC22414.
55. Fong JC, Yildiz FH, The rbmBCDEF gene cluster modulates development of rugose colony morphology and biofilm formation in Vibrio cholerae. Journal of bacteriology. 2007;189(6):2319–30. Epub 2007/01/16. doi: 10.1128/JB.01569-0617220218; PubMed Central PMCID: PMC1899372.
56. Berk V, Fong JC, Dempsey GT, Develioglu ON, Zhuang X, Liphardt J, et al. Molecular architecture and assembly principles of Vibrio cholerae biofilms. Science. 2012;337(6091):236–9. Epub 2012/07/17. doi: 10.1126/science.122298122798614; PubMed Central PMCID: PMC3513368.
57. Smith DR, Maestre-Reyna M, Lee G, Gerard H, Wang AH, Watnick PI, In situ proteolysis of the Vibrio cholerae matrix protein RbmA promotes biofilm recruitment. Proceedings of the National Academy of Sciences of the United States of America. 2015. Epub 2015/08/05. doi: 10.1073/pnas.151242411226240338.
58. Giglio KM, Fong JC, Yildiz FH, Sondermann H, Structural basis for biofilm formation via the Vibrio cholerae matrix protein RbmA. Journal of bacteriology. 2013;195(14):3277–86. Epub 2013/05/21. doi: 10.1128/JB.00374-1323687270; PubMed Central PMCID: PMC3697633.
59. Absalon C, Van Dellen K, Watnick PI, A communal bacterial adhesin anchors biofilm and bystander cells to surfaces. PLoS pathogens. 2011;7(8):e1002210. Epub 2011/09/09. doi: 10.1371/journal.ppat.100221021901100; PubMed Central PMCID: PMC3161981.
60. Beyhan S, Tischler AD, Camilli A, Yildiz FH, Transcriptome and phenotypic responses of Vibrio cholerae to increased cyclic di-GMP level. Journal of bacteriology. 2006;188(10):3600–13. Epub 2006/05/05. doi: 10.1128/JB.188.10.3600–3613.200616672614; PubMed Central PMCID: PMC1482859.
61. Okshevsky M, Meyer RL, The role of extracellular DNA in the establishment, maintenance and perpetuation of bacterial biofilms. Critical reviews in microbiology. 2015;41(3):341–52. Epub 2013/12/07. doi: 10.3109/1040841X.2013.84163924303798.
62. McDonough E, Lazinski DW, Camilli A, Identification of in vivo regulators of the Vibrio cholerae xds gene using a high-throughput genetic selection. Molecular microbiology. 2014;92(2):302–15. Epub 2014/03/29. doi: 10.1111/mmi.1255724673931; PubMed Central PMCID: PMC4005888.
63. Seper A, Fengler VH, Roier S, Wolinski H, Kohlwein SD, Bishop AL, et al. Extracellular nucleases and extracellular DNA play important roles in Vibrio cholerae biofilm formation. Molecular microbiology. 2011;82(4):1015–37. Epub 2011/10/29. doi: 10.1111/j.1365-2958.2011.07867.x22032623; PubMed Central PMCID: PMC3212620.
64. McDonough E, Kamp H, Camilli A, Vibrio cholerae phosphatases required for the utilization of nucleotides and extracellular DNA as phosphate sources. Molecular microbiology. 2015. Epub 2015/07/16. doi: 10.1111/mmi.1312826175126.
65. Pratt JT, McDonough E, Camilli A, PhoB regulates motility, biofilms, and cyclic di-GMP in Vibrio cholerae. Journal of bacteriology. 2009;191(21):6632–42. Epub 2009/09/08. doi: 10.1128/JB.00708-0919734314; PubMed Central PMCID: PMC2795287.
66. Sultan SZ, Silva AJ, Benitez JA, The PhoB regulatory system modulates biofilm formation and stress response in El Tor biotype Vibrio cholerae. FEMS microbiology letters. 2010;302(1):22–31. Epub 2009/11/17. doi: 10.1111/j.1574-6968.2009.01837.x19909344; PubMed Central PMCID: PMC2792938.
67. Haugo AJ, Watnick PI, Vibrio cholerae CytR is a repressor of biofilm development. Molecular microbiology. 2002;45(2):471–83. Epub 2002/07/19. 12123457; PubMed Central PMCID: PMC2515492.
68. Nelson ET, Clements JD, Finkelstein RA, Vibrio cholerae adherence and colonization in experimental cholera: electron microscopic studies. Infection and immunity. 1976;14(2):527–47. Epub 1976/08/01. 971962; PubMed Central PMCID: PMC420916.
69. Jones GW, Freter R, Adhesive properties of Vibrio cholerae: nature of the interaction with isolated rabbit brush border membranes and human erythrocytes. Infection and immunity. 1976;14(1):240–5. Epub 1976/07/01. 985805; PubMed Central PMCID: PMC420869.
70. Yamamoto T, Kamano T, Uchimura M, Iwanaga M, Yokota T, Vibrio cholerae O1 adherence to villi and lymphoid follicle epithelium: in vitro model using formalin-treated human small intestine and correlation between adherence and cell-associated hemagglutinin levels. Infection and immunity. 1988;56(12):3241–50. Epub 1988/12/01. 2903129; PubMed Central PMCID: PMC259731.
71. Yamamoto T, Yokota T, Electron microscopic study of Vibrio cholerae O1 adherence to the mucus coat and villus surface in the human small intestine. Infection and immunity. 1988;56(10):2753–9. Epub 1988/10/01. 3417355; PubMed Central PMCID: PMC259640.
72. Millet YA, Alvarez D, Ringgaard S, von Andrian UH, Davis BM, Waldor MK, Insights into Vibrio cholerae intestinal colonization from monitoring fluorescently labeled bacteria. PLoS pathogens. 2014;10(10):e1004405. Epub 2014/10/03. doi: 10.1371/journal.ppat.100440525275396; PubMed Central PMCID: PMC4183697.
73. Nelson EJ, Chowdhury A, Harris JB, Begum YA, Chowdhury F, Khan AI, et al. Complexity of rice-water stool from patients with Vibrio cholerae plays a role in the transmission of infectious diarrhea. Proceedings of the National Academy of Sciences of the United States of America. 2007;104(48):19091–6. Epub 2007/11/21. doi: 10.1073/pnas.070635210418024592; PubMed Central PMCID: PMC2141913.
74. Faruque SM, Biswas K, Udden SM, Ahmad QS, Sack DA, Nair GB, et al. Transmissibility of cholera: in vivo-formed biofilms and their relationship to infectivity and persistence in the environment. Proceedings of the National Academy of Sciences of the United States of America. 2006;103(16):6350–5. Epub 2006/04/08. doi: 10.1073/pnas.060127710316601099; PubMed Central PMCID: PMC1458881.
75. Xu Q, Dziejman M, Mekalanos JJ, Determination of the transcriptome of Vibrio cholerae during intraintestinal growth and midexponential phase in vitro. Proceedings of the National Academy of Sciences of the United States of America. 2003;100(3):1286–91. Epub 2003/01/29. doi: 10.1073/pnas.033747910012552086; PubMed Central PMCID: PMC298765.
76. Fong JC, Syed KA, Klose KE, Yildiz FH, Role of Vibrio polysaccharide (vps) genes in VPS production, biofilm formation and Vibrio cholerae pathogenesis. Microbiology. 2010;156(Pt 9):2757–69. Epub 2010/05/15. doi: 10.1099/mic.0.040196–020466768; PubMed Central PMCID: PMC3068689.
77. Watnick PI, Lauriano CM, Klose KE, Croal L, Kolter R, The absence of a flagellum leads to altered colony morphology, biofilm development and virulence in Vibrio cholerae O139. Molecular microbiology. 2001;39(2):223–35. Epub 2001/01/03. 11136445; PubMed Central PMCID: PMC2860545.
78. Blow NS, Salomon RN, Garrity K, Reveillaud I, Kopin A, Jackson FR, et al. Vibrio cholerae infection of Drosophila melanogaster mimics the human disease cholera. PLoS pathogens. 2005;1(1):e8. Epub 2005/10/05. doi: 10.1371/journal.ppat.001000816201020; PubMed Central PMCID: PMC1238743.
79. Purdy AE, Watnick PI, Spatially selective colonization of the arthropod intestine through activation of Vibrio cholerae biofilm formation. Proceedings of the National Academy of Sciences of the United States of America. 2011;108(49):19737–42. Epub 2011/11/23. doi: 10.1073/pnas.111153010822106284; PubMed Central PMCID: PMC3241763.
80. Lauriano CM, Ghosh C, Correa NE, Klose KE, The sodium-driven flagellar motor controls exopolysaccharide expression in Vibrio cholerae. Journal of bacteriology. 2004;186(15):4864–74. Epub 2004/07/21. doi: 10.1128/JB.186.15.4864–4874.200415262923; PubMed Central PMCID: PMC451641.
81. Watnick PI, Kolter R, Steps in the development of a Vibrio cholerae El Tor biofilm. Molecular microbiology. 1999;34(3):586–95. Epub 1999/11/17. 10564499; PubMed Central PMCID: PMC2860543.
82. Richardson K, Roles of motility and flagellar structure in pathogenicity of Vibrio cholerae: analysis of motility mutants in three animal models. Infection and immunity. 1991;59(8):2727–36. Epub 1991/08/01. 1855990; PubMed Central PMCID: PMC258079.
83. Postnova T, Gomez-Duarte OG, Richardson K, Motility mutants of Vibrio cholerae O1 have reduced adherence in vitro to human small intestinal epithelial cells as demonstrated by ELISA. Microbiology. 1996;142 (Pt 10):2767–76. Epub 1996/10/01. 8885392.
84. Van Dellen KL, Houot L, Watnick PI, Genetic analysis of Vibrio cholerae monolayer formation reveals a key role for DeltaPsi in the transition to permanent attachment. Journal of bacteriology. 2008;190(24):8185–96. Epub 2008/10/14. doi: 10.1128/JB.00948-0818849423; PubMed Central PMCID: PMC2593239.
85. Utada AS, Bennett RR, Fong JC, Gibiansky ML, Yildiz FH, Golestanian R, et al. Vibrio cholerae use pili and flagella synergistically to effect motility switching and conditional surface attachment. Nature communications. 2014;5:4913. Epub 2014/09/23. doi: 10.1038/ncomms591325234699.
86. Watnick PI, Fullner KJ, Kolter R, A role for the mannose-sensitive hemagglutinin in biofilm formation by Vibrio cholerae El Tor. Journal of bacteriology. 1999;181(11):3606–9. Epub 1999/05/29. 10348878; PubMed Central PMCID: PMC93833.
87. Chiavelli DA, Marsh JW, Taylor RK, The mannose-sensitive hemagglutinin of Vibrio cholerae promotes adherence to zooplankton. Applied and environmental microbiology. 2001;67(7):3220–5. Epub 2001/06/27. doi: 10.1128/AEM.67.7.3220–3225.200111425745; PubMed Central PMCID: PMC93004.
88. Chiang SL, Taylor RK, Koomey M, Mekalanos JJ, Single amino acid substitutions in the N-terminus of Vibrio cholerae TcpA affect colonization, autoagglutination, and serum resistance. Molecular microbiology. 1995;17(6):1133–42. Epub 1995/09/01. 8594332.
89. Jude BA, Taylor RK, The physical basis of type 4 pilus-mediated microcolony formation by Vibrio cholerae O1. Journal of structural biology. 2011;175(1):1–9. Epub 2011/04/30. doi: 10.1016/j.jsb.2011.04.00821527347; PubMed Central PMCID: PMC3102138.
90. Krebs SJ, Taylor RK, Protection and attachment of Vibrio cholerae mediated by the toxin-coregulated pilus in the infant mouse model. Journal of bacteriology. 2011;193(19):5260–70. Epub 2011/08/02. doi: 10.1128/JB.00378-1121804008; PubMed Central PMCID: PMC3187450.
91. Rhine JA, Taylor RK, TcpA pilin sequences and colonization requirements for O1 and O139 vibrio cholerae. Molecular microbiology. 1994;13(6):1013–20. Epub 1994/09/01. 7854116.
92. Tischler AD, Camilli A, Cyclic diguanylate regulates Vibrio cholerae virulence gene expression. Infection and immunity. 2005;73(9):5873–82. Epub 2005/08/23. doi: 10.1128/IAI.73.9.5873–5882.200516113306; PubMed Central PMCID: PMC1231145.
93. Tischler AD, Lee SH, Camilli A, The Vibrio cholerae vieSAB locus encodes a pathway contributing to cholera toxin production. Journal of bacteriology. 2002;184(15):4104–13. Epub 2002/07/11. 12107127; PubMed Central PMCID: PMC135224.
94. Tamayo R, Schild S, Pratt JT, Camilli A, Role of cyclic Di-GMP during el tor biotype Vibrio cholerae infection: characterization of the in vivo-induced cyclic Di-GMP phosphodiesterase CdpA. Infection and immunity. 2008;76(4):1617–27. Epub 2008/01/30. doi: 10.1128/IAI.01337-0718227161; PubMed Central PMCID: PMC2292854.
95. Schild S, Tamayo R, Nelson EJ, Qadri F, Calderwood SB, Camilli A, Genes induced late in infection increase fitness of Vibrio cholerae after release into the environment. Cell host & microbe. 2007;2(4):264–77. Epub 2007/11/17. doi: 10.1016/j.chom.2007.09.00418005744; PubMed Central PMCID: PMC2169296.
96. Angelichio MJ, Spector J, Waldor MK, Camilli A, Vibrio cholerae intestinal population dynamics in the suckling mouse model of infection. Infection and immunity. 1999;67(8):3733–9. Epub 1999/07/23. 10417131; PubMed Central PMCID: PMC96647.
97. Matson JS, Withey JH, DiRita VJ, Regulatory networks controlling Vibrio cholerae virulence gene expression. Infection and immunity. 2007;75(12):5542–9. Epub 2007/09/19. doi: 10.1128/IAI.01094-0717875629; PubMed Central PMCID: PMC2168339.
98. Childers BM, Klose KE, Regulation of virulence in Vibrio cholerae: the ToxR regulon. Future microbiology. 2007;2(3):335–44. Epub 2007/07/31. doi: 10.2217/17460913.2.3.33517661707.
99. Hase CC, Mekalanos JJ, TcpP protein is a positive regulator of virulence gene expression in Vibrio cholerae. Proceedings of the National Academy of Sciences of the United States of America. 1998;95(2):730–4. Epub 1998/01/22. 9435261; PubMed Central PMCID: PMC18489.
100. Kovacikova G, Skorupski K, Overlapping binding sites for the virulence gene regulators AphA, AphB and cAMP-CRP at the Vibrio cholerae tcpPH promoter. Molecular microbiology. 2001;41(2):393–407. Epub 2001/08/08. 11489126.
101. Miller VL, Mekalanos JJ, Genetic analysis of the cholera toxin-positive regulatory gene toxR. Journal of bacteriology. 1985;163(2):580–5. Epub 1985/08/01. 2991197; PubMed Central PMCID: PMC219161.
102. Miller VL, DiRita VJ, Mekalanos JJ, Identification of toxS, a regulatory gene whose product enhances toxR-mediated activation of the cholera toxin promoter. Journal of bacteriology. 1989;171(3):1288–93. Epub 1989/03/01. 2646275; PubMed Central PMCID: PMC209743.
103. DiRita VJ, Parsot C, Jander G, Mekalanos JJ, Regulatory cascade controls virulence in Vibrio cholerae. Proceedings of the National Academy of Sciences of the United States of America. 1991;88(12):5403–7. Epub 1991/06/15. 2052618; PubMed Central PMCID: PMC51881.
104. Lee SH, Hava DL, Waldor MK, Camilli A, Regulation and temporal expression patterns of Vibrio cholerae virulence genes during infection. Cell. 1999;99(6):625–34. Epub 1999/12/28. 10612398.
105. Dorman CJ, H-NS, the genome sentinel. Nature reviews Microbiology. 2007;5(2):157–61. Epub 2006/12/28. doi: 10.1038/nrmicro159817191074.
106. Nye MB, Pfau JD, Skorupski K, Taylor RK, Vibrio cholerae H-NS silences virulence gene expression at multiple steps in the ToxR regulatory cascade. Journal of bacteriology. 2000;182(15):4295–303. Epub 2000/07/14. 10894740; PubMed Central PMCID: PMC101945.
107. Yu RR, DiRita VJ, Regulation of gene expression in Vibrio cholerae by ToxT involves both antirepression and RNA polymerase stimulation. Molecular microbiology. 2002;43(1):119–34. Epub 2002/02/19. 11849541.
108. Stonehouse E, Kovacikova G, Taylor RK, Skorupski K, Integration host factor positively regulates virulence gene expression in Vibrio cholerae. Journal of bacteriology. 2008;190(13):4736–48. Epub 2008/05/06. doi: 10.1128/JB.00089-0818456804; PubMed Central PMCID: PMC2446820.
109. Stonehouse EA, Hulbert RR, Nye MB, Skorupski K, Taylor RK, H-NS binding and repression of the ctx promoter in Vibrio cholerae. Journal of bacteriology. 2011;193(4):979–88. Epub 2010/12/21. doi: 10.1128/JB.01343-0921169492; PubMed Central PMCID: PMC3028689.
110. Wang H, Ayala JC, Benitez JA, Silva AJ, RNA-Seq Analysis Identifies New Genes Regulated by the Histone-Like Nucleoid Structuring Protein (H-NS) Affecting Vibrio cholerae Virulence, Stress Response and Chemotaxis. PloS one. 2015;10(2):e0118295. Epub 2015/02/14. doi: 10.1371/journal.pone.011829525679988; PubMed Central PMCID: PMC4332508.
111. Wang H, Ayala JC, Silva AJ, Benitez JA, The histone-like nucleoid structuring protein (H-NS) is a repressor of Vibrio cholerae exopolysaccharide biosynthesis (vps) genes. Applied and environmental microbiology. 2012;78(7):2482–8. Epub 2012/01/31. doi: 10.1128/AEM.07629-1122287003; PubMed Central PMCID: PMC3302599.
112. Ayala JC, Wang H, Silva AJ, Benitez JA, Repression by H-NS of genes required for the biosynthesis of the Vibrio cholerae biofilm matrix is modulated by the second messenger cyclic diguanylic acid. Molecular microbiology. 2015. Epub 2015/05/20. doi: 10.1111/mmi.1305825982817.
113. Ayala JC, Wang H, Benitez JA, Silva AJ, RNA-Seq analysis and whole genome DNA-binding profile of the histone-like nucleoid structuring protein (H-NS). Genomics data. 2015;5:147–50. Epub 2015/06/23. doi: 10.1016/j.gdata.2015.05.03926097806; PubMed Central PMCID: PMC4470426.
114. Zamorano-Sanchez D, Fong JC, Kilic S, Erill I, Yildiz FH, Identification and characterization of VpsR and VpsT binding sites in Vibrio cholerae. Journal of bacteriology. 2015;197(7):1221–35. Epub 2015/01/28. doi: 10.1128/JB.02439-1425622616; PubMed Central PMCID: PMC4352665.
115. Dorman CJ, Genome architecture and global gene regulation in bacteria: making progress towards a unified model?Nature reviews Microbiology. 2013;11(5):349–55. Epub 2013/04/04. doi: 10.1038/nrmicro300723549066.
116. Hatfield GW, Benham CJ, DNA topology-mediated control of global gene expression in Escherichia coli. Annual review of genetics. 2002;36:175–203. Epub 2002/11/14. doi: 10.1146/annurev.genet.36.032902.11181512429691.
117. Miller MB, Skorupski K, Lenz DH, Taylor RK, Bassler BL, Parallel quorum sensing systems converge to regulate virulence in Vibrio cholerae. Cell. 2002;110(3):303–14. Epub 2002/08/15. 12176318.
118. Rutherford ST, van Kessel JC, Shao Y, Bassler BL, AphA and LuxR/HapR reciprocally control quorum sensing in vibrios. Genes & development. 2011;25(4):397–408. Epub 2011/02/18. doi: 10.1101/gad.201501121325136; PubMed Central PMCID: PMC3042162.
119. Lenz DH, Mok KC, Lilley BN, Kulkarni RV, Wingreen NS, Bassler BL, The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae. Cell. 2004;118(1):69–82. Epub 2004/07/10. doi: 10.1016/j.cell.2004.06.00915242645.
120. Kovacikova G, Skorupski K, Regulation of virulence gene expression in Vibrio cholerae by quorum sensing: HapR functions at the aphA promoter. Molecular microbiology. 2002;46(4):1135–47. Epub 2002/11/08. 12421317.
121. Yang M, Frey EM, Liu Z, Bishar R, Zhu J, The virulence transcriptional activator AphA enhances biofilm formation by Vibrio cholerae by activating expression of the biofilm regulator VpsT. Infection and immunity. 2010;78(2):697–703. Epub 2009/11/26. doi: 10.1128/IAI.00429-0919933826; PubMed Central PMCID: PMC2812199.
122. Waters CM, Lu W, Rabinowitz JD, Bassler BL, Quorum sensing controls biofilm formation in Vibrio cholerae through modulation of cyclic di-GMP levels and repression of vpsT. Journal of bacteriology. 2008;190(7):2527–36. Epub 2008/01/29. doi: 10.1128/JB.01756-0718223081; PubMed Central PMCID: PMC2293178.
123. Deutscher J, Francke C, Postma PW, How phosphotransferase system-related protein phosphorylation regulates carbohydrate metabolism in bacteria. Microbiology and molecular biology reviews: MMBR. 2006;70(4):939–1031. Epub 2006/12/13. doi: 10.1128/MMBR.00024-0617158705; PubMed Central PMCID: PMC1698508.
124. Liang W, Pascual-Montano A, Silva AJ, Benitez JA, The cyclic AMP receptor protein modulates quorum sensing, motility and multiple genes that affect intestinal colonization in Vibrio cholerae. Microbiology. 2007;153(Pt 9):2964–75. Epub 2007/09/05. doi: 10.1099/mic.0.2007/006668-017768239.
125. Silva AJ, Benitez JA, Transcriptional regulation of Vibrio cholerae hemagglutinin/protease by the cyclic AMP receptor protein and RpoS. Journal of bacteriology. 2004;186(19):6374–82. Epub 2004/09/18. doi: 10.1128/JB.186.19.6374–6382.200415375117; PubMed Central PMCID: PMC516606.
126. Liang W, Sultan SZ, Silva AJ, Benitez JA, Cyclic AMP post-transcriptionally regulates the biosynthesis of a major bacterial autoinducer to modulate the cell density required to activate quorum sensing. FEBS letters. 2008;582(27):3744–50. Epub 2008/10/22. doi: 10.1016/j.febslet.2008.10.00818930049; PubMed Central PMCID: PMC2586060.
127. Merrell DS, Hava DL, Camilli A, Identification of novel factors involved in colonization and acid tolerance of Vibrio cholerae. Molecular microbiology. 2002;43(6):1471–91. Epub 2002/04/16. 11952899.
128. Houot L, Chang S, Absalon C, Watnick PI, Vibrio cholerae phosphoenolpyruvate phosphotransferase system control of carbohydrate transport, biofilm formation, and colonization of the germfree mouse intestine. Infection and immunity. 2010;78(4):1482–94. Epub 2010/02/04. doi: 10.1128/IAI.01356-0920123708; PubMed Central PMCID: PMC2849402.
129. Liang W, Silva AJ, Benitez JA, The cyclic AMP receptor protein modulates colonial morphology in Vibrio cholerae. Applied and environmental microbiology. 2007;73(22):7482–7. Epub 2007/10/09. doi: 10.1128/AEM.01564-0717921282; PubMed Central PMCID: PMC2168207.
130. Houot L, Chang S, Pickering BS, Absalon C, Watnick PI, The phosphoenolpyruvate phosphotransferase system regulates Vibrio cholerae biofilm formation through multiple independent pathways. Journal of bacteriology. 2010;192(12):3055–67. Epub 2010/04/20. doi: 10.1128/JB.00213-1020400550; PubMed Central PMCID: PMC2901703.
131. Houot L, Watnick PI, A novel role for enzyme I of the Vibrio cholerae phosphoenolpyruvate phosphotransferase system in regulation of growth in a biofilm. Journal of bacteriology. 2008;190(1):311–20. Epub 2007/11/06. doi: 10.1128/JB.01410-0717981973; PubMed Central PMCID: PMC2223720.
132. Lamarche MG, Wanner BL, Crepin S, Harel J, The phosphate regulon and bacterial virulence: a regulatory network connecting phosphate homeostasis and pathogenesis. FEMS microbiology reviews. 2008;32(3):461–73. Epub 2008/02/06. doi: 10.1111/j.1574-6976.2008.00101.x18248418.
133. Pratt JT, Ismail AM, Camilli A, PhoB regulates both environmental and virulence gene expression in Vibrio cholerae. Molecular microbiology. 2010;77(6):1595–605. Epub 2010/07/28. doi: 10.1111/j.1365-2958.2010.07310.x20659293; PubMed Central PMCID: PMC2981138.
134. Sikora AE, Beyhan S, Bagdasarian M, Yildiz FH, Sandkvist M, Cell envelope perturbation induces oxidative stress and changes in iron homeostasis in Vibrio cholerae. Journal of bacteriology. 2009;191(17):5398–408. Epub 2009/06/23. doi: 10.1128/JB.00092-0919542276; PubMed Central PMCID: PMC2725621.
135. Hung DT, Zhu J, Sturtevant D, Mekalanos JJ, Bile acids stimulate biofilm formation in Vibrio cholerae. Molecular microbiology. 2006;59(1):193–201. Epub 2005/12/20. doi: 10.1111/j.1365-2958.2005.04846.x16359328.
136. Koestler BJ, Waters CM, Bile acids and bicarbonate inversely regulate intracellular cyclic di-GMP in Vibrio cholerae. Infection and immunity. 2014;82(7):3002–14. Epub 2014/05/07. doi: 10.1128/IAI.01664-1424799624; PubMed Central PMCID: PMC4097643.
137. Hay AJ, Zhu J, Host intestinal signal-promoted biofilm dispersal induces Vibrio cholerae colonization. Infection and immunity. 2015;83(1):317–23. Epub 2014/11/05. doi: 10.1128/IAI.02617-1425368110; PubMed Central PMCID: PMC4288906.
138. Gupta S, Chowdhury R, Bile affects production of virulence factors and motility of Vibrio cholerae. Infection and immunity. 1997;65(3):1131–4. Epub 1997/03/01. 9038330; PubMed Central PMCID: PMC175102.
139. Chatterjee A, Dutta PK, Chowdhury R, Effect of fatty acids and cholesterol present in bile on expression of virulence factors and motility of Vibrio cholerae. Infection and immunity. 2007;75(4):1946–53. Epub 2007/01/31. doi: 10.1128/IAI.01435-0617261615; PubMed Central PMCID: PMC1865667.
140. Schuhmacher DA, Klose KE, Environmental signals modulate ToxT-dependent virulence factor expression in Vibrio cholerae. Journal of bacteriology. 1999;181(5):1508–14. Epub 1999/02/27. 10049382; PubMed Central PMCID: PMC93540.
141. Plecha SC, Withey JH, The mechanism for inhibition of Vibrio cholerae ToxT activity by the unsaturated fatty acid components of bile. Journal of bacteriology. 2015. Epub 2015/03/04. doi: 10.1128/JB.02409-1425733618.
142. Abuaita BH, Withey JH, Bicarbonate Induces Vibrio cholerae virulence gene expression by enhancing ToxT activity. Infection and immunity. 2009;77(9):4111–20. Epub 2009/07/01. doi: 10.1128/IAI.00409-0919564378; PubMed Central PMCID: PMC2738005.
143. Thomson JJ, Withey JH, Bicarbonate increases binding affinity of Vibrio cholerae ToxT to virulence gene promoters. Journal of bacteriology. 2014;196(22):3872–80. Epub 2014/09/04. doi: 10.1128/JB.01824-1425182489; PubMed Central PMCID: PMC4248830.
144. McGuckin MA, Linden SK, Sutton P, Florin TH, Mucin dynamics and enteric pathogens. Nature reviews Microbiology. 2011;9(4):265–78. Epub 2011/03/17. doi: 10.1038/nrmicro253821407243.
145. Atuma C, Strugala V, Allen A, Holm L, The adherent gastrointestinal mucus gel layer: thickness and physical state in vivo. American journal of physiology Gastrointestinal and liver physiology. 2001;280(5):G922–9. Epub 2001/04/09. 11292601.
146. Klose KE, The suckling mouse model of cholera. Trends in microbiology. 2000;8(4):189–91. Epub 2001/02/07. 10754579.
147. Ritchie JM, Rui H, Bronson RT, Waldor MK, Back to the future: studying cholera pathogenesis using infant rabbits. mBio. 2010;1(1). Epub 2010/08/07. doi: 10.1128/mBio.00047-1020689747; PubMed Central PMCID: PMC2912669.
148. Cameron DE, Urbach JM, Mekalanos JJ, A defined transposon mutant library and its use in identifying motility genes in Vibrio cholerae. Proceedings of the National Academy of Sciences of the United States of America. 2008;105(25):8736–41. Epub 2008/06/25. doi: 10.1073/pnas.080328110518574146; PubMed Central PMCID: PMC2438431.
149. Chiang SL, Mekalanos JJ, Use of signature-tagged transposon mutagenesis to identify Vibrio cholerae genes critical for colonization. Molecular microbiology. 1998;27(4):797–805. Epub 1998/03/27. 9515705.
150. Fu Y, Waldor MK, Mekalanos JJ, Tn-Seq analysis of Vibrio cholerae intestinal colonization reveals a role for T6SS-mediated antibacterial activity in the host. Cell host & microbe. 2013;14(6):652–63. Epub 2013/12/18. doi: 10.1016/j.chom.2013.11.00124331463; PubMed Central PMCID: PMC3951154.
151. Mandlik A, Livny J, Robins WP, Ritchie JM, Mekalanos JJ, Waldor MK, RNA-Seq-based monitoring of infection-linked changes in Vibrio cholerae gene expression. Cell host & microbe. 2011;10(2):165–74. Epub 2011/08/17. doi: 10.1016/j.chom.2011.07.00721843873; PubMed Central PMCID: PMC3166260.
152. Camilli A, Beattie DT, Mekalanos JJ, Use of genetic recombination as a reporter of gene expression. Proceedings of the National Academy of Sciences of the United States of America. 1994;91(7):2634–8. Epub 1994/03/29. 8146167; PubMed Central PMCID: PMC43424.
153. Camilli A, Mekalanos JJ, Use of recombinase gene fusions to identify Vibrio cholerae genes induced during infection. Molecular microbiology. 1995;18(4):671–83. Epub 1995/11/01. 8817490.
154. Lee SH, Butler SM, Camilli A, Selection for in vivo regulators of bacterial virulence. Proceedings of the National Academy of Sciences of the United States of America. 2001;98(12):6889–94. Epub 2001/06/08. doi: 10.1073/pnas.11158159811391007; PubMed Central PMCID: PMC34448.
155. Lombardo MJ, Michalski J, Martinez-Wilson H, Morin C, Hilton T, Osorio CG, et al. An in vivo expression technology screen for Vibrio cholerae genes expressed in human volunteers. Proceedings of the National Academy of Sciences of the United States of America. 2007;104(46):18229–34. Epub 2007/11/08. doi: 10.1073/pnas.070563610417986616; PubMed Central PMCID: PMC2084325.
156. Taylor RK, Miller VL, Furlong DB, Mekalanos JJ, Use of phoA gene fusions to identify a pilus colonization factor coordinately regulated with cholera toxin. Proceedings of the National Academy of Sciences of the United States of America. 1987;84(9):2833–7. Epub 1987/05/01. 2883655; PubMed Central PMCID: PMC304754.
157. Megli CJ, Yuen AS, Kolappan S, Richardson MR, Dharmasena MN, Krebs SJ, et al. Crystal structure of the Vibrio cholerae colonization factor TcpF and identification of a functional immunogenic site. Journal of molecular biology. 2011;409(2):146–58. Epub 2011/03/29. doi: 10.1016/j.jmb.2011.03.02721440558; PubMed Central PMCID: PMC3098003.
158. Tamayo R, Patimalla B, Camilli A, Growth in a biofilm induces a hyperinfectious phenotype in Vibrio cholerae. Infection and immunity. 2010;78(8):3560–9. Epub 2010/06/03. doi: 10.1128/IAI.00048-1020515927; PubMed Central PMCID: PMC2916270.
159. Zhu J, Mekalanos JJ, Quorum sensing-dependent biofilms enhance colonization in Vibrio cholerae. Developmental cell. 2003;5(4):647–56. Epub 2003/10/11. 14536065.
160. Mudrak B, Tamayo R, The Vibrio cholerae Pst2 phosphate transport system is upregulated in biofilms and contributes to biofilm-induced hyperinfectivity. Infection and immunity. 2012;80(5):1794–802. Epub 2012/02/23. doi: 10.1128/IAI.06277-1122354023; PubMed Central PMCID: PMC3347447.
161. Butler SM, Camilli A, Both chemotaxis and net motility greatly influence the infectivity of Vibrio cholerae. Proceedings of the National Academy of Sciences of the United States of America. 2004;101(14):5018–23. Epub 2004/03/24. doi: 10.1073/pnas.030805210115037750; PubMed Central PMCID: PMC387366.
162. Butler SM, Camilli A, Going against the grain: chemotaxis and infection in Vibrio cholerae. Nature reviews Microbiology. 2005;3(8):611–20. Epub 2005/07/14. doi: 10.1038/nrmicro120716012515; PubMed Central PMCID: PMC2799996.
163. Wong E, Vaaje-Kolstad G, Ghosh A, Hurtado-Guerrero R, Konarev PV, Ibrahim AF, et al. The Vibrio cholerae colonization factor GbpA possesses a modular structure that governs binding to different host surfaces. PLoS pathogens. 2012;8(1):e1002373. Epub 2012/01/19. doi: 10.1371/journal.ppat.100237322253590; PubMed Central PMCID: PMC3257281.
164. Stauder M, Huq A, Pezzati E, Grim CJ, Ramoino P, Pane L, et al. Role of GbpA protein, an important virulence-related colonization factor, for Vibrio cholerae's survival in the aquatic environment. Environmental microbiology reports. 2012;4(4):439–45. Epub 2013/06/14. doi: 10.1111/j.1758-2229.2012.00356.x23760830.
165. Bhowmick R, Ghosal A, Das B, Koley H, Saha DR, Ganguly S, et al. Intestinal adherence of Vibrio cholerae involves a coordinated interaction between colonization factor GbpA and mucin. Infection and immunity. 2008;76(11):4968–77. Epub 2008/09/04. doi: 10.1128/IAI.01615-0718765724; PubMed Central PMCID: PMC2573318.
166. Liu Z, Miyashiro T, Tsou A, Hsiao A, Goulian M, Zhu J, Mucosal penetration primes Vibrio cholerae for host colonization by repressing quorum sensing. Proceedings of the National Academy of Sciences of the United States of America. 2008;105(28):9769–74. Epub 2008/07/09. doi: 10.1073/pnas.080224110518606988; PubMed Central PMCID: PMC2474479.
167. Atsumi T, Maekawa Y, Yamada T, Kawagishi I, Imae Y, Homma M, Effect of viscosity on swimming by the lateral and polar flagella of Vibrio alginolyticus. Journal of bacteriology. 1996;178(16):5024–6. Epub 1996/08/01. 8759871; PubMed Central PMCID: PMC178290.
168. Brown II, Hase CC, Flagellum-independent surface migration of Vibrio cholerae and Escherichia coli. Journal of bacteriology. 2001;183(12):3784–90. Epub 2001/05/24. doi: 10.1128/JB.183.12.3784–3790.200111371543; PubMed Central PMCID: PMC95256.
169. Hase CC, Finkelstein RA, Cloning and nucleotide sequence of the Vibrio cholerae hemagglutinin/protease (HA/protease) gene and construction of an HA/protease-negative strain. Journal of bacteriology. 1991;173(11):3311–7. Epub 1991/06/01. 2045361; PubMed Central PMCID: PMC207942.
170. Silva AJ, Pham K, Benitez JA, Haemagglutinin/protease expression and mucin gel penetration in El Tor biotype Vibrio cholerae. Microbiology. 2003;149(Pt 7):1883–91. Epub 2003/07/12. 12855739.
171. Liu Z, Wang Y, Liu S, Sheng Y, Rueggeberg KG, Wang H, et al. Vibrio cholerae Represses Polysaccharide Synthesis To Promote Motility in Mucosa. Infection and immunity. 2015;83(3):1114–21. Epub 2015/01/07. doi: 10.1128/IAI.02841-1425561707.
172. Reguera G, Kolter R, Virulence and the environment: a novel role for Vibrio cholerae toxin-coregulated pili in biofilm formation on chitin. Journal of bacteriology. 2005;187(10):3551–5. Epub 2005/05/04. doi: 10.1128/JB.187.10.3551–3555.200515866944; PubMed Central PMCID: PMC1112007.
173. Zhu J, Miller MB, Vance RE, Dziejman M, Bassler BL, Mekalanos JJ, Quorum-sensing regulators control virulence gene expression in Vibrio cholerae. Proceedings of the National Academy of Sciences of the United States of America. 2002;99(5):3129–34. Epub 2002/02/21. doi: 10.1073/pnas.05269429911854465; PubMed Central PMCID: PMC122484.
174. Finkelstein RA, Boesman-Finkelstein M, Chang Y, Hase CC, Vibrio cholerae hemagglutinin/protease, colonial variation, virulence, and detachment. Infection and immunity. 1992;60(2):472–8. Epub 1992/02/01. 1730478; PubMed Central PMCID: PMC257651.
175. Benitez JA, Spelbrink RG, Silva A, Phillips TE, Stanley CM, Boesman-Finkelstein M, et al. Adherence of Vibrio cholerae to cultured differentiated human intestinal cells: an in vitro colonization model. Infection and immunity. 1997;65(8):3474–7. Epub 1997/08/01. 9234816; PubMed Central PMCID: PMC175493.
176. Robert A, Silva A, Benitez JA, Rodriguez BL, Fando R, Campos J, et al. Tagging a Vibrio cholerae El Tor candidate vaccine strain by disruption of its hemagglutinin/protease gene using a novel reporter enzyme: Clostridium thermocellum endoglucanase A. Vaccine. 1996;14(16):1517–22. Epub 1996/11/01. 9014293.
177. Jobling MG, Holmes RK, Characterization of hapR, a positive regulator of the Vibrio cholerae HA/protease gene hap, and its identification as a functional homologue of the Vibrio harveyi luxR gene. Molecular microbiology. 1997;26(5):1023–34. Epub 1998/01/13. 9426139.
178. Finkelstein RA, Boesman-Finkelstein M, Holt P, Vibrio cholerae hemagglutinin/lectin/protease hydrolyzes fibronectin and ovomucin: F.M. Burnet revisited. Proceedings of the National Academy of Sciences of the United States of America. 1983;80(4):1092–5. Epub 1983/02/01. 6341990; PubMed Central PMCID: PMC393534.
179. Jude BA, Martinez RM, Skorupski K, Taylor RK, Levels of the secreted Vibrio cholerae attachment factor GbpA are modulated by quorum-sensing-induced proteolysis. Journal of bacteriology. 2009;191(22):6911–7. Epub 2009/09/08. doi: 10.1128/JB.00747-0919734310; PubMed Central PMCID: PMC2772460.
180. Smith DR, Maestre-Reyna M, Lee G, Gerard H, Wang AH, Watnick PI, In situ proteolysis of the Vibrio cholerae matrix protein RbmA promotes biofilm recruitment. Proceedings of the National Academy of Sciences of the United States of America. 2015;112(33):10491–6. Epub 2015/08/05. doi: 10.1073/pnas.151242411226240338.
181. Wang H, Ayala JC, Benitez JA, Silva AJ, Interaction of the histone-like nucleoid structuring protein and the general stress response regulator RpoS at Vibrio cholerae promoters that regulate motility and hemagglutinin/protease expression. Journal of bacteriology. 2012;194(5):1205–15. Epub 2011/12/24. doi: 10.1128/JB.05900-1122194453; PubMed Central PMCID: PMC3294804.
182. Nielsen AT, Dolganov NA, Otto G, Miller MC, Wu CY, Schoolnik GK, RpoS controls the Vibrio cholerae mucosal escape response. PLoS pathogens. 2006;2(10):e109. Epub 2006/10/24. doi: 10.1371/journal.ppat.002010917054394; PubMed Central PMCID: PMC1617127.
183. Wang H, Ayala JC, Benitez JA, Silva AJ, The LuxR-type regulator VpsT negatively controls the transcription of rpoS, encoding the general stress response regulator, in Vibrio cholerae biofilms. Journal of bacteriology. 2014;196(5):1020–30. Epub 2013/12/24. doi: 10.1128/JB.00993-1324363348; PubMed Central PMCID: PMC3957697.
184. Silva AJ, Sultan SZ, Liang W, Benitez JA, Role of the histone-like nucleoid structuring protein in the regulation of rpoS and RpoS-dependent genes in Vibrio cholerae. Journal of bacteriology. 2008;190(22):7335–45. Epub 2008/09/16. doi: 10.1128/JB.00360-0818790865; PubMed Central PMCID: PMC2576668.
185. Bina XR, Provenzano D, Nguyen N, Bina JE, Vibrio cholerae RND family efflux systems are required for antimicrobial resistance, optimal virulence factor production, and colonization of the infant mouse small intestine. Infection and immunity. 2008;76(8):3595–605. Epub 2008/05/21. doi: 10.1128/IAI.01620-0718490456; PubMed Central PMCID: PMC2493215.
186. Provenzano D, Klose KE, Altered expression of the ToxR-regulated porins OmpU and OmpT diminishes Vibrio cholerae bile resistance, virulence factor expression, and intestinal colonization. Proceedings of the National Academy of Sciences of the United States of America. 2000;97(18):10220–4. Epub 2000/08/16. doi: 10.1073/pnas.17021999710944196; PubMed Central PMCID: PMC27820.
187. Ante VM, Bina XR, Howard MF, Sayeed S, Bina JE, Vibrio cholerae leuO transcription is positively regulated by ToxR and contributes to bile resistance. Journal of bacteriology. 2015. Epub 2015/08/26. doi: 10.1128/JB.00419-1526303831.
188. Bilecen K, Fong JC, Cheng A, Jones CJ, Zamorano-Sanchez D, Yildiz FH, Polymyxin B Resistance and Biofilm Formation in Vibrio cholerae Are Controlled by the Response Regulator CarR. Infection and immunity. 2015;83(3):1199–209. Epub 2015/01/15. doi: 10.1128/IAI.02700-1425583523.
189. Hammer BK, Bassler BL, Distinct sensory pathways in Vibrio cholerae El Tor and classical biotypes modulate cyclic dimeric GMP levels to control biofilm formation. Journal of bacteriology. 2009;191(1):169–77. Epub 2008/10/28. doi: 10.1128/JB.01307-0818952786; PubMed Central PMCID: PMC2612459.
190. Muller J, Miller MC, Nielsen AT, Schoolnik GK, Spormann AM, vpsA- and luxO-independent biofilms of Vibrio cholerae. FEMS microbiology letters. 2007;275(2):199–206. Epub 2007/08/19. doi: 10.1111/j.1574-6968.2007.00884.x17697110.
191. Seper A, Pressler K, Kariisa A, Haid AG, Roier S, Leitner DR, et al. Identification of genes induced in Vibrio cholerae in a dynamic biofilm system. International journal of medical microbiology: IJMM. 2014;304(5–6):749–63. Epub 2014/06/26. doi: 10.1016/j.ijmm.2014.05.01124962154; PubMed Central PMCID: PMC4101255.