Comparative RNA-Seq based dissection of the regulatory networks and environmental stimuli underlying Vibrio parahaemolyticus gene expression during infection

Nucleic Acids Research

Volumn 42, Issue 19, 2014, Pages 12212-12223

  Livny, Jonathan ^a,b   Zhou, Xiaohui ^b,c   Mandlik, Anjali ^b   Hubbard, Troy ^b   Davis, Brigid M ^b   Waldor, Matthew K ^a,b  

^a BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON; MESSENGER RNA; RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR VTRB; TRANSCRIPTOME; TRANSFER RNA; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; EXSA PROTEIN, BACTERIA; OPAR PROTEIN, VIBRIO PARAHAEMOLYTICUS; SMALL UNTRANSLATED RNA; TRANSACTIVATOR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GROWTH; CARBON SOURCE; CONTROLLED STUDY; GENE CONTROL; GENE EXPRESSION; GENE IDENTIFICATION; GENE REGULATORY NETWORK; IN VITRO STUDY; IN VIVO STUDY; INFANT; INTESTINE; NONHUMAN; PRIORITY JOURNAL; RNA ANALYSIS; RNA ISOLATION; RNA SEQUENCE; TRANSCRIPTION REGULATION; TRANSCRIPTOMICS; VIBRIO CHOLERAE; VIBRIO PARAHAEMOLYTICUS; VIBRIO PARAHAEMOLYTICUS INFECTION; ANIMAL; BACTERIAL SECRETION SYSTEM; ENVIRONMENT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOGENICITY; RABBIT; REGULON; SEQUENCE ANALYSIS; VIBRIOSIS; VIROLOGY; VIRULENCE;

ANIMALS; BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; ENVIRONMENT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENE REGULATORY NETWORKS; INTESTINES; RABBITS; REGULON; RNA, SMALL UNTRANSLATED; SEQUENCE ANALYSIS, RNA; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; VIBRIO CHOLERAE; VIBRIO INFECTIONS; VIBRIO PARAHAEMOLYTICUS; VIRULENCE;

EID: 84925283832     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku891     Document Type: Article

References (41)

1. Qadri, F., Alam, M.S., Nishibuchi, M., Rahman, T., Alam, N.H., Chisti, J., Kondo, S., Sugiyama, J., Bhuiyan, N.A., Mathan, M.M. et al. (2003) Adaptive and inflammatory immune responses in patients infected with strains of Vibrio parahaemolyticus. J. Infect. Dis., 187, 1085-1096.
2. Ritchie, J.M., Rui, H., Zhou, X., Iida, T., Kodoma, T., Ito, S., Davis, B.M., Bronson, R.T. and Waldor, M.K. (2012) Inflammation and disintegration of intestinal villi in an experimental model for Vibrio parahaemolyticus-induced diarrhea. PLoS Pathog., 8, e1002593.
3. Park, K.-S., Ono, T., Rokuda, M., Jang, M.-H., Okada, K., Iida, T. and Honda, T. (2004) Functional characterization of two type III secretion systems of Vibrio parahaemolyticus. Infect. Immun., 72, 6659-6665.
4. Zhou, X., Gewurz, B.E., Ritchie, J.M., Takasaki, K., Greenfeld, H., Kieff, E., Davis, B.M. and Waldor, M.K. (2013) A Vibrio parahaemolyticus T3SS effector mediates pathogenesis by independently enabling intestinal colonization and inhibiting TAK1 activation. Cell Rep., 3, 1690-1702.
5. Hiyoshi, H., Kodama, T., Saito, K., Gotoh, K., Matsuda, S., Akeda, Y., Honda, T. and Iida, T. (2011) VopV, an F-Actin-binding type III secretion effector, is required for Vibrio parahaemolyticus-induced enterotoxicity. Cell Host Microbe., 10, 401-409.
6. Makino, K., Oshima, K., Kurokawa, K., Yokoyama, K., Uda, T., Tagomori, K., Iijima, Y., Najima, M., Nakano, M., Yamashita, A. et al. (2003) Genome sequence of Vibrio parahaemolyticus: A pathogenic mechanism distinct from that of V cholerae. Lancet, 361, 743-749.
7. Broberg, C.A., Calder, T.J. and Orth, K. (2011) Vibrio parahaemolyticus cell biology and pathogenicity determinants. Microbes Infect., 13, 992-1001.
8. Hiyoshi, H., Kodama, T., Iida, T. and Honda, T. (2010) Contribution of Vibrio parahaemolyticus virulence factors to cytotoxicity, enterotoxicity, and lethality in mice. Infect. Immun., 78, 1772-1780.
9. Izutsu, K., Kurokawa, K., Tashiro, K., Kuhara, S., Hayashi, T., Honda, T. and Iida, T. (2008) Comparative genomic analysis using microarray demonstrates a strong correlation between the presence of the 80-kilobase pathogenicity island and pathogenicity in Kanagawa phenomenon-positive Vibrio parahaemolyticus strains. Infect. Immun., 76, 1016-1023.
10. Gotoh, K., Kodama, T., Hiyoshi, H., Izutsu, K., Park, K.-S., Dryselius, R., Akeda, Y., Honda, T. and Iida, T. (2010) Bile acid-induced virulence gene expression of Vibrio parahaemolyticus reveals a novel therapeutic potential for bile acid sequestrants. PLoS ONE, 5, e13365.
11. Kodama, T., Gotoh, K., Hiyoshi, H., Morita, M., Izutsu, K., Akeda, Y., Park, K.-S., Cantarelli, V.V., Dryselius, R., Iida, T. et al. (2010) Two regulators of Vibrio parahaemolyticus play important roles in enterotoxicity by controlling the expression of genes in the Vp-PAI region. PLoS ONE, 5, e8678.
12. Zhou, X., Shah, D.H., Konkel, M.E. and Call, D.R. (2008) Type III secretion system 1 genes in Vibrio parahaemolyticusare positively regulated by ExsA and negatively regulated by ExsD. Mol. Microbiol., 69, 747-764.
13. Gode-Potratz, C.J., Chodur, D.M. and McCarter, L.L. (2010) Calcium and iron regulate swarming and type III secretion in Vibrio parahaemolyticus. J. Bacteriol., 192, 6025-6038.
14. McCarter, L. (1999) The multiple identities of Vibrio parahaemolyticus. J. Mol. Microbiol. Biotechnol., 1, 51-57.
15. Stewart, B.J. and McCarter, L.L. (2003) Lateral flagellar gene system of Vibrio parahaemolyticus. J. Bacteriol., 185, 4508-4518.
16. Gode-Potratz, C.J., Kustusch, R.J., Breheny, P.J., Weiss, D.S. and McCarter, L.L. (2010) Surface sensing in Vibrio parahaemolyticus triggers a programme of gene expression that promotes colonization and virulence. Mol. Microbiol., 79, 240-263.
17. Russell, A.B., Peterson, S.B. and Mougous, J.D. (2014) Type VI secretion system effectors: Poisons with a purpose. Nat. Rev. Micro., 12, 137-148.
18. Ho, B.T., Dong, T.G. and Mekalanos, J.J. (2014) A view to a kill: The bacterial type VI secretion system. Cell Host Microbe., 15, 9-21.
19. Yu, Y., Yang, H., Li, J., Zhang, P., Wu, B., Zhu, B., Zhang, Y. and Fang, W. (2012) Putative type VI secretion systems of Vibrio parahaemolyticus contribute to adhesion to cultured cell monolayers. Arch Microbiol., 194, 827-835.
20. Salomon, D., Gonzalez, H., Updegraff, B.L. and Orth, K. (2013) Vibrio parahaemolyticus type VI secretion system 1 is activated in marine conditions to target bacteria, and is differentially regulated from system 2. PLoS ONE, 8, e61086.
21. Gode-Potratz, C.J. and McCarter, L.L. (2011) Quorum sensing and silencing in Vibrio parahaemolyticus. J. Bacteriol., 193, 4224-4237.
22. Ritchie, J.M., Rui, H., Bronson, R.T. and Waldor, M.K. (2010) Back to the future: Studying cholera pathogenesis using infant rabbits. MBio, 1, e00047.
23. Ritchie, J.M. and Waldor, M.K. (2009) Vibrio cholerae interactions with the gastrointestinal tract: Lessons from animal studies. Current topics in microbiology and immunology, 337, 37-59
24. Mandlik, A., Livny, J., Robins, W.P., Ritchie, J.M., Mekalanos, J.J. and Waldor, M.K. (2011) RNA-Seq-based monitoring of infection-linked changes in Vibrio cholerae gene expression. Cell Host Microbe., 10, 165-174.
25. Ferreira, R.B.R., Chodur, D.M., Antunes, L.C.M., Trimble, M.J. and McCarter, L.L. (2012) Output targets and transcriptional regulation by a cyclic dimeric GMP-responsive circuit in the Vibrio parahaemolyticus Scr network. J. Bacteriol., 194, 914-924.
26. Morales, V.M., Bäckman, A. and Bagdasarian, M. (1991) A series of wide-host-range low-copy-number vectors that allow direct screening for recombinants. Gene, 97, 39-47.
27. Li, H. and Durbin, R. (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics, 25, 1754-1760.
28. Gardner, P.P., Daub, J., Tate, J.G., Nawrocki, E.P., Kolbe, D.L., Lindgreen, S., Wilkinson, A.C., Finn, R.D., Griffiths-Jones, S., Eddy, S.R. et al. (2009) Rfam: Updates to the RNA families database. Nucleic Acids Res., 37, D136-D140.
29. Anders, S. and Huber, W. (2010) Differential expression analysis for sequence count data. Genome Biol., 11, R106.
30. Haas, B.J., Chin, M., Nusbaum, C., Birren, B.W. and Livny, J. (2012) How deep is deep enough for RNA-Seq profiling of bacterial transcriptomes? BMC Genom., 13, 734.
31. Conesa, A., Gotz, S., Garcia-Gomez, J.M., Terol, J., Talon, M. and Robles, M. (2005) Blast2GO: A universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics, 21, 3674-3676.
32. Carver, T., Harris, S.R., Berriman, M., Parkhill, J. and McQuillan, J.A. (2012) Artemis: An integrated platform for visualization and analysis of high-throughput sequence-based experimental data. Bioinformatics, 28, 464-469.
33. Zhou, X., Ritchie, J.M., Hiyoshi, H., Iida, T., Davis, B.M., Waldor, M.K. and Kodama, T. (2012) The hydrophilic translocator for Vibrio parahaemolyticus, T3SS2, is also translocated. Infect. Immun., 80, 2940-2947.
34. Ono, T., Park, K.-S., Ueta, M., Iida, T. and Honda, T. (2006) Identification of proteins secreted via Vibrio parahaemolyticus type III secretion system 1. Infect. Immun., 74, 1032-1042.
35. Sun, F., Zhang, Y., Wang, L., Yan, X., Tan, Y., Guo, Z., Qiu, J., Yang, R., Xia, P. and Zhou, D. (2012) Molecular characterization of direct target genes and cis-acting consensus recognized by Quorum-sensing regulator AphA in Vibrio parahaemolyticus. PLoS ONE, 7, e44210.
36. Gomelsky, M. (2012) Cyclic dimeric GMP-mediated decisions in surface-grown Vibrio parahaemolyticus: A different kind of motile-to-sessile transition. J. Bacteriol., 194, 911-913.
37. Hansen, G.A., Ahmad, R., Hjerde, E., Fenton, C.G., Willassen, N.-P. and Haugen, P. (2012) Expression profiling reveals Spot 42 small RNA as a key regulator in the central metabolism of Aliivibrio salmonicida. BMC Genom., 13, 37.
38. Beisel, C.L. and Storz, G. (2011) The base-pairing RNA Spot 42 participates in a multioutput feedforward loop to help enact catabolite repression in Escherichia coli. Mol. Cell, 41, 286-297.
39. Tanabe, T., Funahashi, T., Nakao, H., Maki, J. and Yamamoto, S. (2013) The Vibrio parahaemolyticus small RNA RyhB promotes production of the siderophore vibrioferrin by stabilizing the polycistronic mRNA. J. Bacteriol., 195, 3692-3703.
40. Sudarsan, N., Lee, E.R., Weinberg, Z., Moy, R.H., Kim, J.N., Link, K.H. and Breaker, R.R. (2008) Riboswitches in eubacteria sense the second messenger cyclic di-GMP. Science, 321, 411-413.
41. Zhou, X., Massol, R.H., Nakamura, F., Chen, X., Gewurz, B.E., Davis, B.M., Lencer, W.I. and Waldor, M.K. Remodeling of the intestinal brush border underlies adhesion and virulence of an enteric pathogen. MBio, 5 , e01639-14.