Vibrio cholerae represses polysaccharide synthesis to promote motility in mucosa

Infection and Immunity

Volumn 83, Issue 3, 2015, Pages 1114-1121

  Liu, Zhenyu ^a,b   Wang, Yuning ^a,c   Liu, Shengyan ^d   Sheng, Ying ^a,b   Rueggeberg, Karl Gustav ^c   Wang, Hui ^a   Li, Jie ^b   Gu, Frank X ^d   Zhong, Zengtao ^a   Kan, Biao ^b,e   Zhu, Jun ^a,c  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

^b CHINESE CENTER FOR DISEASE CONTROL AND PREVENTION   (China)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d UNIVERSITY OF WATERLOO   (Canada)

^e ZHEJIANG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

MUCIN; POLYSACCHARIDE; UNCLASSIFIED DRUG; VIBRIO POLYSACCHARIDE; BACTERIAL POLYSACCHARIDE; PROTEIN BINDING;

ADHESION; ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; CARBOHYDRATE SYNTHESIS; CONTROLLED STUDY; INFANT; MOUSE; NONHUMAN; PRIORITY JOURNAL; STOMACH MOTILITY; STOMACH MUCUS; VIBRIO CHOLERAE; ANIMAL; BACTERIAL GENOME; BIOSYNTHESIS; CHEMISTRY; CHOLERA; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; INTESTINE MUCOSA; METABOLISM; MICROBIOLOGY; MOVEMENT (PHYSIOLOGY); NEWBORN; SIGNAL TRANSDUCTION; SMALL INTESTINE;

ANIMALS; ANIMALS, NEWBORN; CHOLERA; GENE EXPRESSION REGULATION, BACTERIAL; GENOME, BACTERIAL; HOST-PATHOGEN INTERACTIONS; INTESTINAL MUCOSA; INTESTINE, SMALL; MICE; MOVEMENT; MUCINS; POLYSACCHARIDES, BACTERIAL; PROTEIN BINDING; SIGNAL TRANSDUCTION; VIBRIO CHOLERAE;

EID: 84923037764     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.02841-14     Document Type: Article

References (48)

1. Faruque SM, Albert MJ, Mekalanos JJ. 1998. Epidemiology, genetics, and ecology of toxigenic Vibrio cholerae. Microbiol Mol Biol Rev 62:1301-1314.
2. Sack DA, Sack RB, Nair GB, Siddique AK. 2004. Cholera. Lancet 363: 223-233. http://dx.doi.org/10.1016/S0140-6736(03)15328-7.
3. Watnick PI, Kolter R. 1999. Steps in the development of a Vibrio cholerae El Tor biofilm. Mol Microbiol 34:586-595. http://dx.doi.org/10.1046/j.1365-2958.1999.01624.x.
4. Watnick PI, Lauriano CM, Klose KE, Croal L, Kolter R. 2001. The absence of a flagellum leads to altered colony morphology, biofilm development and virulence in Vibrio cholerae O139. Mol Microbiol 39:223-235. http://dx.doi.org/10.1046/j.1365-2958.2001.02195.x.
5. Yildiz FH, Schoolnik GK. 1999. Vibrio cholerae O1 El Tor: identification of a gene cluster required for the rugose colony type, exopolysaccharide production, chlorine resistance, and biofilm formation. Proc Natl Acad Sci USA 96:4028-4033. http://dx.doi.org/10.1073/pnas.96.7.4028.
6. ETr-associated phenotypes in Vibrio cholerae O1 El Tor. J Bacteriol 183:1716-1726. http://dx.doi.org/10.1128/JB.183.5.1716-1726.2001.
7. Casper-Lindley C, Yildiz FH. 2004. 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. J Bacteriol 186: 1574-1578. http://dx.doi.org/10.1128/JB.186.5.1574-1578.2004.
8. Krukonis ES, DiRita VJ. 2003. From motility to virulence: sensing and responding to environmental signals in Vibrio cholerae. Curr Opin Microbiol 6:186-190. http://dx.doi.org/10.1016/S1369-5274(03)00032-8.
9. Reidl J, Klose KE. 2002. Vibrio cholerae and cholera: out of the water and into the host. FEMS Microbiol Rev 26:125-139. http://dx.doi.org/10.1111/j.1574-6976.2002.tb00605.x.
10. Cone RA. 2009. Barrier properties of mucus. Adv Drug Deliv Rev 61:75-85. http://dx.doi.org/10.1016/j.addr.2008.09.008.
11. Johansson ME, Sjovall H, Hansson GC. 2013. The gastrointestinal mucus system in health and disease. Nat Rev Gastroenterol Hepatol 10:352-361. http://dx.doi.org/10.1038/nrgastro.2013.35.
12. Millet YA, Alvarez D, Ringgaard S, von Andrian UH, Davis BM, Waldor MK. 2014. Insights into Vibrio cholerae intestinal colonization from monitoring fluorescently labeled bacteria. PLoS Pathog 10: e1004405. http://dx.doi.org/10.1371/journal.ppat.1004405.
13. Bhowmick R, Ghosal A, Das B, Koley H, Saha DR, Ganguly S, Nandy RK, Bhadra RK, Chatterjee NS. 2008. Intestinal adherence of Vibrio cholerae involves a coordinated interaction between colonization factor GbpA and mucin. Infect Immun 76:4968-4977. http://dx.doi.org/10.1128/IAI.01615-07.
14. Silva AJ, Pham K, Benitez JA. 2003. Haemagglutinin/protease expression and mucin gel penetration in El Tor biotype Vibrio cholerae. Microbiology 149:1883-1891. http://dx.doi.org/10.1099/mic.0.26086-0.
15. Szabady RL, Yanta JH, Halladin DK, Schofield MJ, Welch RA. 2011. TagA is a secreted protease of Vibrio cholerae that specifically cleaves mucin glycoproteins. Microbiology 157:516-525. http://dx.doi.org/10.1099/mic.0.044529-0.
16. Yeung AT, Parayno A, Hancock RE. 2012. Mucin promotes rapid surface motility in Pseudomonas aeruginosa. mBio 3(3):e00073-12. http://dx.doi.org/10.1128/mBio.00073-12.
17. Skoog EC, Sjoling A, Navabi N, Holgersson J, Lundin SB, Linden SK. 2012. Human gastric mucins differently regulate Helicobacter pylori proliferation, gene expression and interactions with host cells. PLoS One 7:e36378. http://dx.doi.org/10.1371/journal.pone.0036378.
18. Verghese A, Catanese A, Arbeit RD. 1988. Staphylococcus aureus pneumonia in hamsters with elastase-induced emphysema-the virulence enhancing activity of mucin. Proc Soc Exp Biol Med 188:1-6.
19. Joelsson A, Liu Z, Zhu J. 2006. Genetic and phenotypic diversity of quorum-sensing systems in clinical and environmental isolates of Vibrio cholerae. Infect Immun 74:1141-1147. http://dx.doi.org/10.1128/IAI.74.2.1141-1147.2006.
20. Metcalf WW, Jiang W, Daniels LL, Kim SK, Haldimann A, Wanner BL. 1996. Conditionally replicative and conjugative plasmids carrying lacZα for cloning, mutagenesis, and allele replacement in bacteria. Plasmid 35: 1-13.
21. Yang M, Liu Z, Hughes C, Stern AM, Wang H, Zhong Z, Kan B, Fenical W, Zhu J. 2013. Bile salt-induced intermolecular disulfide bond formation activates Vibrio cholerae virulence. Proc Natl Acad Sci USA 110: 2348-2353. http://dx.doi.org/10.1073/pnas.1218039110.
22. Liu Z, Yang M, Peterfreund GL, Tsou AM, Selamoglu N, Daldal F, Zhong Z, Kan B, Zhu J. 2011. Vibrio cholerae anaerobic induction of virulence gene expression is controlled by thiol-based switches of virulence regulator AphB. Proc Natl Acad Sci USA 108:810-815. http://dx.doi.org/10.1073/pnas.1014640108.
23. Judson N, Mekalanos JJ. 2000. Transposon-based approaches to identify essential bacterial genes. Trends Microbiol 8:521-526. http://dx.doi.org/10.1016/S0966-842X(00)01865-5.
24. Liu Z, Miyashiro T, Tsou A, Hsiao A, Goulian M, Zhu J. 2008. Mucosal penetration primes Vibrio cholerae for host colonization by repressing quorum sensing. Proc Natl Acad Sci USA 105:9769-9774. http://dx.doi.org/10.1073/pnas.0802241105.
25. Lee DW, Shirley SA, Lockey RF, Mohapatra SS. 2006. Thiolated chitosan nanoparticles enhance anti-inflammatory effects of intranasally delivered theophylline. Respir Res 7:112. http://dx.doi.org/10.1186/1465-9921-7-112.
26. Gardel CL, Mekalanos JJ. 1996. Alterations in Vibrio cholerae motility phenotypes correlate with changes in virulence factor expression. Infect Immun 64:2246-2255.
27. Gosink KK, Kobayashi R, Kawagishi I, Hase CC. 2002. Analyses of the roles of the three cheA homologs in chemotaxis of Vibrio cholerae. J Bacteriol 184:1767-1771. http://dx.doi.org/10.1128/JB.184.6.1767-1771.2002.
28. Beyhan S, Bilecen K, Salama SR, Casper-Lindley C, Yildiz FH. 2007. Regulation of rugosity and biofilm formation in Vibrio cholerae: comparison of VpsT and VpsR regulons and epistasis analysis of vpsT, vpsR, and hapR. J Bacteriol 189:388-402. http://dx.doi.org/10.1128/JB.00981-06.
29. Fong JC, Syed KA, Klose KE, Yildiz FH. 2010. Role of Vibrio polysaccharide (vps) genes in VPS production, biofilm formation and Vibrio cholerae pathogenesis. Microbiology 156:2757-2769. http://dx.doi.org/10.1099/mic.0.040196-0.
30. Zhu J, Mekalanos JJ. 2003. Quorum sensing-dependent biofilms enhance colonization in Vibrio cholerae. Dev Cell 5:647-656. http://dx.doi.org/10.1016/S1534-5807(03)00295-8.
31. Khutoryanskiy VV. 2011. Advances in mucoadhesion and mucoadhesive polymers. Macromol Biosci 11:748-764. http://dx.doi.org/10.1002/mabi.201000388.
32. Colwell RR, Huq A, Islam MS, Aziz KM, Yunus M, Khan NH, Mahmud A, Sack RB, Nair GB, Chakraborty J, Sack DA, Russek-Cohen E. 2003. Reduction of cholera in Bangladeshi villages by simple filtration. Proc Natl Acad Sci USA 100:1051-1055. http://dx.doi.org/10.1073/pnas.0237386100.
33. Liu Z, Stirling FR, Zhu J. 2007. Temporal quorum-sensing induction regulates Vibrio cholerae biofilm architecture. Infect Immun 75:122-126. http://dx.doi.org/10.1128/IAI.01190-06.
34. Hay AJ, Zhu J. 2015. Host intestinal signal-promoted biofilm dispersal induces Vibrio cholerae colonization. Infect Immun 83:317-323. http://dx.doi.org/10.1128/IAI.02617-14.
35. McGuckin MA, Linden SK, Sutton P, Florin TH. 2011. Mucin dynamics and enteric pathogens. Nat Rev Microbiol 9:265-278. http://dx.doi.org/10.1038/nrmicro2538.
36. Henderson IR, Czeczulin J, Eslava C, Noriega F, Nataro JP. 1999. Characterization of Pic, a secreted protease of Shigella flexneri and enteroaggregative Escherichia coli. Infect Immun 67:5587-5596.
37. Jansen HJ, Hart CA, Rhodes JM, Saunders JR, Smalley JW. 1999. A novel mucin-sulphatase activity found in Burkholderia cepacia and Pseudomonas aeruginosa. J Med Microbiol 48:551-557.
38. Celli JP, Turner BS, Afdhal NH, Keates S, Ghiran I, Kelly CP, Ewoldt RH, McKinley GH, So P, Erramilli S, Bansil R. 2009. Helicobacter pylori moves through mucus by reducing mucin viscoelasticity. Proc Natl Acad Sci USA 106:14321-14326. http://dx.doi.org/10.1073/pnas.0903438106.
39. Siebers A, Finlay BB. 1996. M cells and the pathogenesis of mucosal and systemic infections. Trends Microbiol 4:22-29.
40. Tu QV, McGuckin MA, Mendz GL. 2008. Campylobacter jejuni response to human mucin Muc2: modulation of colonization and pathogenicity determinants. J Med Microbiol 57:795-802. http://dx.doi.org/10.1099/jmm.0.47752-0.
41. Hammer BK, Bassler BL. 2003. Quorum sensing controls biofilm formation in Vibrio cholerae. Mol Microbiol 50:101-104. http://dx.doi.org/10.1046/j.1365-2958.2003.03688.x.
42. Yildiz FH, Visick KL. 2009. Vibrio biofilms: so much the same yet so different. Trends Microbiol 17:109-118. http://dx.doi.org/10.1016/j.tim.2008.12.004.
43. Camilli A, Bassler BL. 2006. Bacterial small-molecule signaling pathways. Science 311:1113-1116. http://dx.doi.org/10.1126/science.1121357.
44. Tischler AD, Camilli A. 2004. Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation. Mol Microbiol 53:857-869. http://dx.doi.org/10.1111/j.1365-2958.2004.04155.x.
45. Lim B, Beyhan S, Meir J, Yildiz FH. 2006. Cyclic-diGMP signal transduction systems in Vibrio cholerae: modulation of rugosity and biofilm formation. Mol Microbiol 60:331-348. http://dx.doi.org/10.1111/j.1365-2958.2006.05106.x.
46. Liu X, Beyhan S, Lim B, Linington RG, Yildiz FH. 2010. Identification and characterization of a phosphodiesterase that inversely regulates motility and biofilm formation in Vibrio cholerae. J Bacteriol 192:4541-4552. http://dx.doi.org/10.1128/JB.00209-10.
47. Tischler AD, Camilli A. 2005. Cyclic diguanylate regulates Vibrio cholerae virulence gene expression. Infect Immun 73:5873-5882. http://dx.doi.org/10.1128/IAI.73.9.5873-5882.2005.
48. Tamayo R, Schild S, Pratt JT, Camilli A. 2008. Role of cyclic di-GMP during El Tor biotype Vibrio cholerae infection: characterization of the in vivo-induced cyclic di-GMP phosphodiesterase CdpA. Infect Immun 76: 1617-1627. http://dx.doi.org/10.1128/IAI.01337-07.