Intrinsic and extrinsic regulation of type III secretion gene expression in Pseudomonas aeruginosa

Frontiers in Microbiology

Volumn 2, Issue APR, 2011, Pages

  Diaz, Manisha R ^a   King, Jessica M ^a   Yahr, Timothy L ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

cAMP; ExsA; Gene regulation; Injectisome; Pseudomonas aeruginosa; RsmA; Type III secretion; Vfr

Indexed keywords

EID: 84861375222     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2011.00089     Document Type: Article

References (97)

1. Allmond, L. R., Ajayi, T., Moriyama, K., Wiener-Kronish, J. P., and Sawa, T. (2004). V-antigen genotype and phenotype analyses of clinical isolates of Pseudomonas aeruginosa. J. Clin. Microbiol. 42, 3857-3860.
2. Alonso, A., Rojo, F., and Martinez, J. L. (1999). Environmental and clinical isolates of Pseudomonas aeruginosa show pathogenic and biodegradative properties irrespective of their origin. Environ. Microbiol. 1, 421-430.
3. Aspedon, A., Palmer, K., and Whiteley, M. (2006). Microarray analysis of the osmotic stress response in Pseudomonas aeruginosa. J. Bacteriol. 188, 2721-2725.
4. Bernhards, R. C., Jing, X., Vogelaar, N. J., Robinson, H., and Schubot, F. D. (2009). Structural evidence suggests that antiactivator ExsD from Pseudomonas aeruginosa is a DNA binding protein. Protein Sci. 18, 503-513.
5. Bleves, S., Soscia, C., Nogueira-Orlandi, P., Lazdunski, A., and Filloux, A. (2005). Quorum sensing negatively controls type III secretion regulon expression in Pseudomonas aeruginosa PAO1. J. Bacteriol. 187, 3898-3902.
6. Boucher, J. C., Yu, H., Mudd, M. H., and Deretic, V. (1997). Mucoid Pseudomonas aeruginosa in cystic fibrosis: characterization of muc mutations in clinical isolates and analysis of clearance in a mouse model of respiratory infection. Infect. Immun. 65, 3838-3846.
7. Brannon, M. K., Davis, J. M., Mathias, J. R., Hall, C. J., Emerson, J. C., Crosier, P. S., Huttenlocher, A., Ramakrishnan, L., and Moskowitz, S. M. (2009). Pseudomonas aeruginosa type III secretion system interacts with phagocytes to modulate systemic infection of zebrafish embryos. Cell. Microbiol. 11, 755-768.
8. Brencic, A., and Lory, S. (2009). Determination of the regulon and identification of novel mRNA targets of Pseudomonas aeruginosa RsmA. Mol. Microbiol. 72, 612-632.
9. Brutinel, E. D., Vakulskas, C. A., Brady, K. M., and Yahr, T. L. (2008). Characterization of ExsA and of ExsA-dependent promoters required for expression of the Pseudomonas aeruginosa type III secretion system. Mol. Microbiol. 68, 657-671.
10. Brutinel, E. D., Vakulskas, C. A., and Yahr, T. L. (2009). Functional domains of ExsA, the transcriptional activator of the Pseudomonas aeruginosa type III secretion system. J. Bacteriol. 191, 3811-3821.
11. Brutinel, E. D., Vakulskas, C. A., and Yahr, T. L. (2010). ExsD inhibits expressionof the Pseudomonas aeruginosa type III secretion system by disrupting ExsA self-association and DNA binding activity. J. Bacteriol. 192, 1479-1486.
12. Brutinel, E. D., and Yahr, T. L. (2008). Control of gene expression by type III secretory activity. Curr. Opin. Microbiol. 11, 128-133.
13. Coburn, B., Sekirov, I., and Finlay, B. B. (2007). Type III secretion systems and disease. Clin. Microbiol. Rev. 20, 535-549.
14. Dacheux, D., Epaulard, O., De Groot, A., Guery, B., Leberre, R., Attree, I., Polack, B., and Toussaint, B. (2002). Activation of the Pseudomonas aeruginosa type III secretion system requires an intact pyruvate dehydrogenase aceAB operon. Infect. Immun. 70, 3973-3977.
15. Dasgupta, N., Lykken, G. L., Wolfgang, M. C., and Yahr, T. L. (2004). A novel anti-anti-activator mechanism regulates expression of the Pseudomonas aeruginosa type III secretion system. Mol. Microbiol. 53, 297-308.
16. Dubnau, D., and Losick, R. (2006). Bistability in bacteria. Mol. Microbiol. 61, 564-572.
17. Engel, J., and Balachandran, P. (2009). Role of Pseudomonas aeruginosa type III effectors in disease. Curr. Opin. Microbiol. 12, 61-66.
18. Feltman, H., Schulert, G., Khan, S., Jain, M., Peterson, L., and Hauser, A. R. (2001). Prevalence of type III secretion genes in clinical and environmental isolates of Pseudomonas aeruginosa. Microbiology 147, 2659-2669.
19. Franchi, L., Stoolman, J., Kanneganti, T. D., Verma, A., Ramphal, R., and Nunez, G. (2007). Critical role for Ipaf in Pseudomonas aeruginosa-induced caspase-1 activation. Eur. J. Immunol. 37, 3030-3039.
20. Frank, D. W. (1997). The exoenzyme S regulon of Pseudomonas aeruginosa. Mol. Microbiol. 26, 621-629.
21. Fuchs, E. L., Brutinel, E. D., Klem, E. R., Fehr, A. R., Yahr, T. L., and Wolfgang, M. C. (2010). In vitro and in vivo characterization of the Pseudomonas aeruginosa cyclic AMP (cAMP) phosphodiesterase CpdA, required for cAMP homeostasis and virulence factor regulation. J. Bacteriol. 192, 2779-2790.
22. Galle, M., Schotte, P., Haegman, M., Wullaert, A., Yang, H. J., Jin, S., and Beyaert, R. (2007). The Pseudomonas aeruginosa type III secretion system plays a dual role in the regulation of caspase-1 mediated IL-1beta maturation. J. Cell. Mol. Med. 12, 1767-1776.
23. Gillis, R. J., White, K. G., Choi, K. H., Wagner, V. E., Schweizer, H. P., and Iglewski, B. H. (2005). Molecular basis of azithromycin-resistant Pseudomonas aeruginosa biofilms.Antimicrob. Agents Chemother. 49, 3858-3867.
24. Gomez, M. I., and Prince, A. (2007). Opportunistic infections in lung disease: Pseudomonas infections in cystic fibrosis. Curr. Opin. Pharmacol. 7, 244-251.
25. Gooderham, W. J., Bains, M., Mcphee, J. B., Wiegand, I., and Hancock, R. E. (2008). Induction by cationic antimicrobial peptides and involvement in intrinsic polymyxin and antimicrobial peptide resistance, biofilm formation, and swarming motility of PsrA in Pseudomonas aeruginosa. J. Bacteriol. 190, 5624-5634.
26. Goodman, A. L., Kulasekara, B., Rietsch, A., Boyd, D., Smith, R. S., and Lory, S. (2004). A signaling network reciprocally regulates genes associated with acute infection and chronic persistence in Pseudomonas aeruginosa. Dev. Cell 7, 745-754.
27. Govan, J. R., and Deretic, V. (1996). Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol. Rev. 60, 539-574.
28. Grier, M. C., Garrity-Ryan, L. K., Bartlett, V. J., Klausner, K. A., Donovan, P. J., Dudley, C., Alekshun, M. N., Tanaka, S. K., Draper, M. P., Levy, S. B., and Kim, O. K. (2010). N-hydroxybenzimidazole inhibitors of ExsA MAR transcription factor in Pseudomonas aeruginosa: in vitro anti-virulence activity and metabolic stability. Bioorg. Med. Chem. Lett. 20, 3380-3383.
29. Ha, U. H., Kim, J., Badrane, H., Jia, J., Baker, H. V., Wu, D., and Jin, S. (2004). An in vivo inducible gene of Pseudomonas aeruginosa encodes an anti-ExsA to suppress the type III secretion system. Mol. Microbiol. 54, 307-320.
30. Harmsen, M., Yang, L., Pamp, S. J., and Tolker-Nielsen, T. (2010). An update on Pseudomonas aeruginosa biofilm formation, tolerance, and dispersal. FEMS Immunol. Med. Microbiol. 59, 253-268.
31. Hauser, A. R. (2009). The type III secretion system of Pseudomonas aeruginosa: infection by injection. Nat. Rev. Microbiol. 7, 654-665.
32. Hayes, C. S., Aoki, S. K., and Low, D. A. (2010). Bacterial contact-dependent delivery systems. Annu. Rev. Genet. 44, 71-90.
33. Heurlier, K., Williams, F., Heeb, S., Dormond, C., Pessi, G., Singer, D., Camara, M., Williams, P., and Haas, D. (2004). Positive control of swarming, rhamnolipid synthesis, and lipase production by the posttranscriptional RsmA/RsmZ system in Pseudomonas aeruginosa PAO1. J. Bacteriol. 186, 2936-2945.
34. Hogardt, M., Roeder, M., Schreff, A. M., Eberl, L., and Heesemann, J. (2004). Expression of Pseudomonas aeruginosa exoS is controlled by quorum sensing and RpoS. Microbiology 150, 843-851.
35. Hornef, M. W., Roggenkamp, A., Geiger, A. M., Hogardt, M., Jacobi, C. A., and Heesemann, J. (2000). Triggering the ExoS regulon of Pseudomonas aeruginosa: a GFP-reporter analysis of exoenzyme (Exo) S, ExoT and ExoU synthesis. Microb. Pathog. 29, 329-343.
36. Hovey, A. K., and Frank, D. W. (1995). Analyses of the DNA-binding and transcriptional activation properties of ExsA, the transcriptional activator of the Pseudomonas aeruginosa exoenzyme S regulon. J. Bacteriol. 177, 4427-4436.
37. Irie, Y., Starkey, M., Edwards, A. N., Wozniak, D. J., Romeo, T., and Parsek, M. R. (2010). Pseudomonas aeruginosa biofilm matrix polysaccharide Psl is regulated transcriptionally by RpoS and post-transcriptionally by RsmA. Mol. Microbiol. 78, 158-172.
38. Jones, A. K., Fulcher, N. B., Balzer, G. J., Urbanowski, M. L., Pritchett, C. L., Schurr, M. J., Yahr, T. L., and Wolfgang, M. C. (2010). Activation of the Pseudomonas aeruginosa AlgU regulon through mucA mutation inhibits cyclic AMP/Vfr signaling. J. Bacteriol. 192, 5709-5717.
39. Kanack, K. J., Runyen-Janecky, L. J., Ferrell, E. P., Suh, S. J., and West, S. E. (2006). Characterization of DNA-binding specificity and analysis of binding sites of the Pseudomonas aeruginosa global regulator, Vfr, a homologue of the Escherichia coli cAMP receptor protein. Microbiology 152, 3485-3496.
40. Kang, Y., Lunin, V. V., Skarina, T., Savchenko, A., Schurr, M. J., and Hoang, T. T. (2009). The long-chain fatty acid sensor, PsrA, modulates the expression of rpoS and the type III secretion exsCEBA operon in Pseudomonas aeruginosa. Mol. Microbiol. 73, 120-136.
41. Kim, J., Ahn, K., Min, S., Jia, J., Ha, U., Wu, D., and Jin, S. (2005). Factors triggering type III secretion in Pseudomonas aeruginosa. Microbiology 151, 3575-3587.
42. Lapouge, K., Schubert, M., Allain, F. H., and Haas, D. (2008). Gac/Rsm signal transduction pathway of gamma-proteobacteria: from RNA recognition to regulation of social behaviour. Mol. Microbiol. 67, 241-253.
43. Li, Z., Kosorok, M. R., Farrell, P. M., Laxova, A., West, S. E., Green, C. G., Collins, J., Rock, M. J., and Splaingard, M. L. (2005). Longitudinal development of mucoid Pseudomonas aeruginosa infection and lung diseaseprogression in children with cystic fibrosis. JAMA 293, 581-588.
44. Linares, J. F., Gustafsson, I., Baquero, F., and Martinez, J. L. (2006). Antibiotics as intermicrobial signaling agents instead of weapons. Proc. Natl. Acad. Sci. U.S.A. 103, 19484-19489.
45. Linares, J. F., Lopez, J. A., Camafeita, E., Albar, J. P., Rojo, F., and Martinez, J. L. (2005). Overexpression of the multidrug efflux pumps MexCD-OprJ and MexEF-OprN is associated with a reduction of type III secretion in Pseudomonas aeruginosa. J. Bacteriol. 187, 1384-1391.
46. Lykken, G. L., Chen, G., Brutinel, E. D., Chen, L., and Yahr, T. L. (2006). Characterization of ExsC and ExsD self-association and heterocomplex formation. J. Bacteriol. 188, 6832-6840.
47. Mathee, K., Mcpherson, C. J., and Ohman, D. E. (1997). Posttranslational control of the algT (algU)-encoded sigma22 for expression of the alginate regulon in Pseudomonas aeruginosa and localization of its antagonist proteins MucA and MucB (AlgN). J. Bacteriol. 179, 3711-3720.
48. Mccaw, M. L., Lykken, G. L., Singh, P. K., and Yahr, T. L. (2002). ExsD is a negative regulator of the Pseudomonas aeruginosa type III secretion regulon. Mol. Microbiol. 46, 1123-1133.
49. Miao, E. A., Ernst, R. K., Dors, M., Mao, D. P., and Aderem, A. (2008). Pseudomonas aeruginosa activates caspase 1 through Ipaf. Proc. Natl. Acad. Sci. U.S.A. 105, 2562-2567.
50. Mikkelsen, H., Bind, N. J., Skindersoe, M. E., Givskov, M., Lilley, K. S., and Welch, M. (2009). Biofims and type III secretion are not mutually exclusive in Pseudomonas aeruginosa. Microbiology 155, 687-698.
51. Miyata, S., Casey, M., Frank, D. W., Ausubel, F. M., and Drenkard, E. (2003). Use of the Galleria mellonella caterpillar as a model host to study the role of the type III secretion system in Pseudomonas aeruginosa pathogenesis. Infect. Immun. 71, 2404-2413.
52. Moraes, T. F., Spreter, T., and Strynadka, N. C. (2008). Piecing together the type III injectisome of bacterial pathogens. Curr. Opin. Struct. Biol. 18, 258-266.
53. Mulcahy, H., O'callaghan, J., O'grady, E. P., Adams, C., and O'gara, F. (2006). The posttranscriptional regulator RsmA plays a role in the interaction between Pseudomonas aeruginosa and human airway epithelial cells by positively regulating the type III secretion system. Infect. Immun. 74, 3012-3015.
54. Overhage, J., Bains, M., Brazas, M. D., and Hancock, R. E. (2008). Swarming of Pseudomonas aeruginosa is a complex adaptation leading to increased production of virulence factors andantibiotic resistance. J. Bacteriol. 190, 2671-2679.
55. Pedersen, S. S., Hoiby, N., Espersen, F., and Koch, C. (1992). Role of alginate in infection with mucoid Pseudomonas aeruginosa in cystic fibrosis. Thorax 47, 6-13.
56. Pessi, G., Williams, F., Hindle, Z., Heurlier, K., Holden, M. T., Camara, M., Haas, D., and Williams, P. (2001). The global posttranscriptional regulator RsmA modulates production of virulence determinants and N-acylhomoserine lactones in Pseudomonas aeruginosa. J. Bacteriol. 183, 6676-6683.
57. Pukatzki, S., Kessin, R. H., and Mekalanos, J. J. (2002). The human pathogen Pseudomonas aeruginosa utilizes conserved virulence pathways to infect the social amoeba Dictyostelium discoideum. Proc. Natl. Acad. Sci. U.S.A. 99, 3159-3164.
58. Rau, M. H., Hansen, S. K., Johansen, H. K., Thomsen, L. E., Workman, C. T., Nielsen, K. F., Jelsbak, L., Hoiby, N., Yang, L., and Molin, S. (2010). Early adaptive developments of Pseudomonas aeruginosa after the transition from life in the environment to persistent colonization in the airways of human cystic fibrosis hosts. Environ. Microbiol. 12, 1643-1658.
59. Rietsch, A., and Mekalanos, J. J. (2006). Metabolic regulation of type III secretion gene expression in Pseudomonas aeruginosa. Mol. Microbiol. 59, 807-820.
60. Rietsch, A., Vallet-Gely, I., Dove, S. L., and Mekalanos, J. J. (2005). ExsE, a secreted regulator of type III secretion genes in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. U.S.A. 102, 8006-8011.
61. Rietsch, A., Wolfgang, M. C., and Mekalanos, J. J. (2004). Effect of metabolic imbalance on expression of type III secretion genes in Pseudomonas aeruginosa. Infect. Immun. 72, 1383-1390.
62. Romeo, T., Gong, M., Liu, M. Y., and Brun-Zinkernagel, A. M. (1993). Identification and molecular characterization of csrA, a pleiotropic gene from Escherichia coli that affects glycogen biosynthesis, gluconeogenesis, cell size, and surface properties. J. Bacteriol. 175, 4744-4755.
63. Ryder, C., Byrd, M., and Wozniak, D. J. (2007). Role of polysaccharides in Pseudomonas aeruginosa biofilm development. Curr. Opin. Microbiol. 10, 644-648.
64. Sandoz, K. M., Mitzimberg, S. M., and Schuster, M. (2007). Social cheating in Pseudomonas aeruginosa quorum sensing. Proc. Natl. Acad. Sci. U.S.A. 104, 15876-15881.
65. Schurr, M. J., Yu, H., Martinez-Salazar, J. M., Boucher, J. C., and Deretic, V. (1996). Control of AlgU, a member of the sigma E-like family of stress sigma factors, by the negative regulators MucA and MucB and Pseudomonas aeruginosa conversion to mucoidy in cystic fibrosis. J. Bacteriol. 178, 4997-5004.
66. Shen, D. K., Filopon, D., Chaker, H., Boullanger, S., Derouazi, M., Polack, B., and Toussaint, B. (2008). High-cell-density regulation of the Pseudomonas aeruginosa type III secretion system: implications for tryptophan catabolites. Microbiology 154, 2195-2208.
67. Shen, D. K., Filopon, D., Kuhn, L., Polack, B., and Toussaint, B. (2006). PsrA is a positive transcriptional regulator of the type III secretion system in Pseudomonas aeruginosa. Infect. Immun. 74, 1121-1129.
68. Singh, G., Wu, B., Baek, M. S., Camargo, A., Nguyen, A., Slusher, N. A., Srinivasan, R., Wiener-Kronish, J. P., and Lynch, S. V. (2010). Secretion of Pseudomonas aeruginosa type III cytotoxins is dependent on Pseudomonas quinolone signal concentration. Microb. Pathog. 49, 196-203.
69. Singh, P. K., Schaefer, A. L., Parsek, M. R., Moninger, T. O., Welsh, M. J., and Greenberg, E. P. (2000). Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. Nature 407, 762-764.
70. Soscia, C., Hachani, A., Bernadac, A., Filloux, A., and Bleves, S. (2007). Cross talk between type III secretion and flagellar assembly systems in Pseudomonas aeruginosa. J. Bacteriol. 189, 3124-3132.
71. Stover, C. K., Pham, X. Q., Erwin, A. L., Mizoguchi, S. D., Warrener, P., Hickey, M. J., Brinkman, F. S., Hufnagle, W. O., Kowalik, D. J., Lagrou, M., Garber, R. L., Goltry, L., Tolentino, E., Westbrock-Wadman, S., Yuan, Y., Brody, L. L., Coulter, S. N., Folger, K. R., Kas, A., Larbig, K., Lim, R., Smith, K., Spencer, D., Wong, G. K., Wu, Z., Paulsen, I. T., Reizer, J., Saier, M. H., Hancock, R. E., Lory, S., and Olson, M. V. (2000). Complete genome sequence of Pseudomonas aeruginosa PA01, an opportunistic pathogen. Nature 406, 959-964.
72. Sundin, C., Wolfgang, M. C., Lory, S., Forsberg, A., and Frithz-Lindsten, E. (2002). Type IV pili are not specifically required for contact dependent translocation of exoenzymes by Pseudomonas aeruginosa. Microb. Pathog. 33, 265-277.
73. Sutterwala, F. S., Mijares, L. A., Li, L., Ogura, Y., Kazmierczak, B. I., and Flavell, R. A. (2007). Immune recognition of Pseudomonas aeruginosa mediated by the IPAF/NLRC4 inflammasome. J. Exp. Med. 204, 3235-3245.
74. Thibault, J., Faudry, E., Ebel, C., Attree, I., and Elsen, S. (2009). Anti-activator ExsD forms a 1:1 complex with ExsA to inhibit transcription of type III secretion operons. J. Biol. Chem. 284, 15762-15770.
75. Tralau, T., Vuilleumier, S., Thibault, C., Campbell, B. J., Hart, C. A., and Kertesz, M. A. (2007). Transcriptomic analysis of the sulfate starvation response of Pseudomonas aeruginosa. J. Bacteriol. 189, 6743-6750.
76. Urbanowski, M. L., Brutinel, E. D., and Yahr, T. L. (2007). Translocation of ExsE into Chinese hamster ovary cells is required for transcriptional induction of the Pseudomonas aeruginosa type III secretion system. Infect. Immun. 75, 4432-4439.
77. Urbanowski, M. L., Lykken, G. L., and Yahr, T. L. (2005). A secreted regulatory protein couples transcription to the secretory activity of the Pseudomonas aeruginosa type III secretion system. Proc. Natl. Acad. Sci. U.S.A. 102, 9930-9935.
78. Vakulskas, C. A., Brady, K. M., and Yahr, T. L. (2009). Mechanism of Transcriptional Activation by Pseudomonas aeruginosa ExsA. J. Bacteriol. 191, 6654-6664.
79. Vakulskas, C. A., Brutinel, E. D., and Yahr, T. L. (2010). ExsA recruits RNA polymerase to an extended-10 promoter by contacting region 4.2 of Sigma-70. J. Bacteriol. 192, 3597-3607.
80. Vallis, A. J., Yahr, T. L., Barbieri, J. T., and Frank, D. W. (1999). Regulation of ExoS production and secretion by Pseudomonas aeruginosa in response to tissue culture conditions. Infect. Immun. 67, 914-920.
81. Van Alst, N. E., Wellington, M., Clark, V. L., Haidaris, C. G., and Iglewski, B. H. (2009). Nitrite reductase NirS is required for type III secretion system expression and virulence in the human monocyte cell line THP-1 by Pseudomonas aeruginosa. Infect. Immun. 77, 4446-4454.
82. Ventre, I., Goodman, A. L., Vallet-Gely, I., Vasseur, P., Soscia, C., Molin, S., Bleves, S., Lazdunski, A., Lory, S., and Filloux, A. (2006). Multiple sensors control reciprocal expression of Pseudomonas aeruginosa regulatory RNA and virulence genes. Proc. Natl. Acad. Sci. U.S.A. 103, 171-176.
83. Vogelaar, N. J., Jing, X., Robinson, H. H., and Schubot, F. D. (2010). Analysis of the crystal structure of the ExsC. ExsE complex reveals distinctive binding interactions of the Pseudomonas aeruginosa type III secretion chaperone ExsC with ExsE and ExsD. Biochemistry 49, 5870-5879.
84. Wagner, S., Konigsmaier, L., Lara-Tejero, M., Lefebre, M., Marlovits, T. C., andGalan, J. E. (2010). Organization and coordinated assembly of the type III secretion export apparatus. Proc. Natl. Acad. Sci. U.S.A. 41, 17745-17750.
85. Wei, B. L., Brun-Zinkernagel, A. M., Simecka, J. W., Pruss, B. M., Babitzke, P., and Romeo, T. (2001). Positive regulation of motility and flhDC expression by the RNA-binding protein CsrA of Escherichia coli. Mol. Microbiol. 40, 245-256.
86. West, S. E., Sample, A. K., and Runyen-Janecky, L. J. (1994). The vfr gene product, required for Pseudomonas aeruginosa exotoxin A and protease production, belongs to the cyclic AMP receptor protein family. J. Bacteriol. 176, 7532-7542.
87. Wolfgang, M. C., Lee, V. T., Gilmore, M. E., and Lory, S. (2003). Coordinate regulation of bacterial virulence genes by a novel adenylate cyclase-dependent signaling pathway. Dev. Cell 4, 253-263.
88. Wood, L. F., and Ohman, D. E. (2009). Use of cell wall stress to characterize sigma 22 (AlgT/U) activation by regulated proteolysis and its regulon in Pseudomonas aeruginosa. Mol. Microbiol. 72, 183-201.
89. Worrall, L. J., Lameignere, E., and Strynadka, N. C. (2011). Structural overview of the bacterial injectisome. Curr. Opin. Microbiol. 14, 3-8.
90. Wozniak, D. J., and Ohman, D. E. (1994). Transcriptional analysis of the Pseudomonas aeruginosa genes algR, algB, and algD reveals a hierarchy of alginate gene expression which is modulated by algT. J. Bacteriol. 176, 6007-6014.
91. Wu, W., Badrane, H., Arora, S., Baker, H. V., and Jin, S. (2004). MucA-mediated coordination of type III secretion and alginate synthesis in Pseudomonas aeruginosa. J. Bacteriol. 186, 7575-7585.
92. Wu, W., and Jin, S. (2005). PtrB of Pseudomonas aeruginosa suppresses the type III secretion system under the stress of DNA damage. J. Bacteriol. 187, 6058-6068.
93. Yahr, T. L., and Frank, D. W. (1994). Transcriptional organization of the trans-regulatory locus which controls exoenzyme S synthesis in Pseudomonas aeruginosa. J. Bacteriol. 176, 3832-3838.
94. Yahr, T. L., Hovey, A. K., Kulich, S. M., and Frank, D. W. (1995). Transcriptional analysis of the Pseudomonas aeruginosa exoenzyme S structural gene. J. Bacteriol. 177, 1169-1178.
95. Yahr, T. L., and Wolfgang, M. C. (2006). Transcriptional regulation of the Pseudomonas aeruginosa type III secretion system. Mol. Microbiol. 62, 631-640.
96. Zheng, Z., Chen, G., Joshi, S., Brutinel, E. D., Yahr, T. L., and Chen, L. (2007). Biochemical characterization of a regulatory cascade controlling transcription of the Pseudomonas aeruginosa type III secretion system. J. Biol. Chem. 282, 6136-6142.
97. Zhou, L., Wang, J., and Zhang, L. H. (2007). Modulation of bacterial type III secretion system by a spermidine transporter dependent signaling pathway. PLoS ONE 2, e1291. doi: 10.1371/journal.pone.0001291