The Pseudomonas aeruginosa periplasmic protease CtpA can affect systems that impact its ability to mount both acute and chronic infections

Infection and Immunity

Volumn 81, Issue 12, 2013, Pages 4561-4570

  Seo, Jin ^a   Darwin, Andrew J ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; PROTEINASE; SIGMA FACTOR;

ACUTE DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL GENOME; BACTERIAL VIRULENCE; CHRONIC DISEASE; CHRONICITY; CONTROLLED STUDY; ENZYME ANALYSIS; FEMALE; LUNG INFECTION; MOUSE; NONHUMAN; NULL ALLELE; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTION; REGULON;

ANIMALS; BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; CARBOXYPEPTIDASES; CHO CELLS; CRICETULUS; ENDOPEPTIDASES; FEMALE; GENE EXPRESSION REGULATION, BACTERIAL; MICE; MICE, INBRED BALB C; PNEUMONIA; PROPROTEIN CONVERTASES; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; SIGMA FACTOR;

EID: 84890189776     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01035-13     Document Type: Article

References (68)

1. Stover CK, Pham XQ, Erwin AL, Mizoguchi SD, Warrener P, Hickey MJ, Brinkman FS, Hufnagle WO, Kowalik DJ, Lagrou M, Garber RL, Goltry L, Tolentino E, Westbrock-Wadman S, Yuan Y, Brody LL, Coulter SN, Folger KR, Kas A, Larbig K, Lim R, Smith K, Spencer D, Wong GK, Wu Z, Paulsen IT, Reizer J, Saier MH, Hancock RE, Lory S, Olson MV. 2000. Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406:959-964.
2. Bleves S, Viarre V, Salacha R, Michel GP, Filloux A, Voulhoux R. 2010. Protein secretion systems in Pseudomonas aeruginosa: a wealth of pathogenic weapons. Int. J. Med. Microbiol. 300:534-543.
3. Hauser AR. 2009. The type III secretion system of Pseudomonas aeruginosa: infection by injection. Nat. Rev. Microbiol. 7:654-665.
4. Fleiszig SM, Zaidi TS, Preston MJ, Grout M, Evans DJ, Pier GB. 1996. Relationship between cytotoxicity and corneal epithelial cell invasion by clinical isolates of Pseudomonas aeruginosa. Infect. Immun. 64:2288-2294.
5. Finck-Barbancon V, Goranson J, Zhu L, Sawa T, Wiener-Kronish JP, Fleiszig SM, Wu C, Mende-Mueller L, Frank DW. 1997. ExoU expression by Pseudomonas aeruginosa correlates with acute cytotoxicity and epithelial injury. Mol. Microbiol. 25:547-557.
6. Nicas TI, Iglewski BH. 1985. The contribution of exoproducts to virulence of Pseudomonas aeruginosa. Can. J. Microbiol. 31:387-392.
7. Sato H, Frank DW. 2004. ExoU is a potent intracellular phospholipase. Mol. Microbiol. 53:1279-1290.
8. Yahr TL, Vallis AJ, Hancock MK, Barbieri JT, Frank DW. 1998. ExoY, an adenylate cyclase secreted by the Pseudomonas aeruginosa type III system. Proc. Natl. Acad. Sci. U. S. A. 95:13899-13904.
9. Govan JR, Harris GS. 1986. Pseudomonas aeruginosa and cystic fibrosis: unusual bacterial adaptation and pathogenesis. Microbiol. Sci. 3:302-308.
10. Lyczak JB, Cannon CL, Pier GB. 2002. Lung infections associated with cystic fibrosis. Clin. Microbiol. Rev. 15:194-222.
11. DeVries CA, Ohman DE. 1994. Mucoid-to-nonmucoid conversion in alginate-producing Pseudomonas aeruginosa often results from spontaneous mutations in algT, encoding a putative alternate sigma factor, and shows evidence for autoregulation. J. Bacteriol. 176:6677-6687.
12. Martin DW, Holloway BW, Deretic V. 1993. Characterization of a locus determining the mucoid status of Pseudomonas aeruginosa: AlgU shows sequence similarities with a Bacillus sigma factor. J. Bacteriol. 175:1153-1164.
13. Martin DW, Schurr MJ, Mudd MH, Govan JR, Holloway BW, Deretic V. 1993. Mechanism of conversion to mucoidy in Pseudomonas aeruginosa infecting cystic fibrosis patients. Proc. Natl. Acad. Sci. U. S. A. 90:8377-8381.
14. Llamas MA, Mooij MJ, Sparrius M, Vandenbroucke-Grauls CM, Ratledge C, Bitter W. 2008. Characterization of five novel Pseudomonas aeruginosa cell-surface signalling systems. Mol. Microbiol. 67:458-472.
15. Martinez-Bueno MA, Tobes R, Rey M, Ramos JL. 2002. Detection of multiple extracytoplasmic function (ECF) sigma factors in the genome of Pseudomonas putida KT2440 and their counterparts in Pseudomonas aeruginosa PAO1. Environ. Microbiol. 4:842-855.
16. Lyczak JB, Cannon CL, Pier GB. 2000. Establishment of Pseudomonas aeruginosa infection: lessons from a versatile opportunist. Microbes Infect. 2:1051-1060.
17. Damron FH, Goldberg JB. 2012. Proteolytic regulation of alginate overproduction in Pseudomonas aeruginosa. Mol. Microbiol. 84:595-607.
18. Wood LF, Leech AJ, Ohman DE. 2006. Cell wall-inhibitory antibiotics activate the alginate biosynthesis operon in Pseudomonas aeruginosa: roles of sigma (AlgT) and the AlgW and Prc proteases. Mol. Microbiol. 62:412-426.
19. Reiling SA, Jansen JA, Henley BJ, Singh S, Chattin C, Chandler M, Rowen DW. 2005. Prc protease promotes mucoidy in mucA mutants of Pseudomonas aeruginosa. Microbiology 151:2251-2261.
20. Sautter R, Ramos D, Schneper L, Ciofu O, Wassermann T, Koh CL, Heydorn A, Hentzer M, Hoiby N, Kharazmi A, Molin S, Devries CA, Ohman DE, Mathee K. 2012. A complex multilevel attack on Pseudomonas aeruginosa algT/U expression and algT/U activity results in the loss of alginate production. Gene 498:242-253.
21. Pallen MJ, Ponting CP. 1997. PDZ domains in bacterial proteins. Mol. Microbiol. 26:411-413.
22. Beebe KD, Shin J, Peng J, Chaudhury C, Khera J, Pei D. 2000. Substrate recognition through a PDZ domain in tail-specific protease. Biochemistry 39:3149-3155.
23. Hara H, Nishimura Y, Kato J, Suzuki H, Nagasawa H, Suzuki A, Hirota Y. 1989. Genetic analyses of processing involving C-terminal cleavage in penicillin-binding protein 3 of Escherichia coli. J. Bacteriol. 171:5882-5889.
24. Hara H, Yamamoto Y, Higashitani A, Suzuki H, Nishimura Y. 1991. Cloning, mapping, and characterization of the Escherichia coli prc gene, which is involved in C-terminal processing of penicillin-binding protein 3. J. Bacteriol. 173:4799-4813.
25. Nagasawa H, Sakagami Y, Suzuki A, Suzuki H, Hara H, Hirota Y. 1989. Determination of the cleavage site involved in C-terminal processing of penicillin-binding protein 3 of Escherichia coli. J. Bacteriol. 171:5890-5893.
26. Silber KR, Keiler KC, Sauer RT. 1992. Tsp: a tail-specific protease that selectively degrades proteins with nonpolar C termini. Proc. Natl. Acad. Sci. U. S. A. 89:295-299.
27. Keiler KC, Waller PR, Sauer RT. 1996. Role of a peptide tagging system in degradation of proteins synthesized from damaged messenger RNA. Science 271:990-993.
28. Bandara AB, DeShazer D, Inzana TJ, Sriranganathan N, Schurig GG, Boyle SM. 2008. A disruption of ctpA encoding carboxy-terminal protease attenuates Burkholderia mallei and induces partial protection in CD1 mice. Microb. Pathog. 45:207-216.
29. Bandara AB, Sriranganathan N, Schurig GG, Boyle SM. 2005. Carboxylterminal protease regulates Brucella suis morphology in culture and persistence in macrophages and mice. J. Bacteriol. 187:5767-5775.
30. Mitchell SJ, Minnick MF. 1997. A carboxy-terminal processing protease gene is located immediately upstream of the invasion-associated locus from Bartonella bacilliformis. Microbiology 143:1221-1233.
31. Hoge R, Laschinski M, Jaeger KE, Wilhelm S, Rosenau F. 2011. The subcellular localization of a C-terminal processing protease in Pseudomonas aeruginosa. FEMS Microbiol. Lett. 316:23-30.
32. Potvin E. 2007. Functional genomics of Pseudomonas aeruginosa and analysis of the molecular function of a sigma-anti-sigma factor. Ph. D. thesis. Université Laval, Sainte-Foy, Québec, Canada. http://archimede.bibl.ulaval.ca/archimede/fichiers/24237/24237.html.
33. Strom MS, Lory S. 1986. Cloning and expression of the pilin gene of Pseudomonas aeruginosa PAK in Escherichia coli. J. Bacteriol. 165:367-372.
34. Miller VL, Mekalanos JJ. 1988. A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J. Bacteriol. 170:2575-2583.
35. Becher A, Schweizer HP. 2000. Integration-proficient Pseudomonas aeruginosa vectors for isolation of single-copy chromosomal lacZ and lux gene fusions. Biotechniques 29:948-952.
36. Gueguen E, Flores-Kim J, Darwin AJ. 2011. The Yersinia enterocolitica phage shock proteins B and C can form homodimers and heterodimers in vivo with the possibility of close association between multiple domains. J. Bacteriol. 193:5747-5758.
37. Seo J, Brencic A, Darwin AJ. 2009. Analysis of secretin-induced stress in Pseudomonas aeruginosa suggests prevention rather than response and identifies a novel protein involved in secretin function. J. Bacteriol. 191:898-908.
38. Bochner BR, Gadzinski P, Panomitros E. 2001. Phenotype microarrays for high-throughput phenotypic testing and assay of gene function. Genome Res. 11:1246-1255.
39. Sonawane A, Jyot J, Ramphal R. 2006. Pseudomonas aeruginosa LecB is involved in pilus biogenesis and protease IV activity but not in adhesion to respiratory mucins. Infect. Immun. 74:7035-7039.
40. Yamaguchi S, Darwin AJ. 2012. Recent findings about the Yersinia enterocolitica phage shock protein response. J. Microbiol. 50:1-7.
41. Wurtzel O, Yoder-Himes DR, Han K, Dandekar AA, Edelheit S, Greenberg EP, Sorek R, Lory S. 2012. The single-nucleotide resolution transcriptome of Pseudomonas aeruginosa grown in body temperature. PLoS Pathog. 8:e1002945. doi:10.1371/journal.ppat.1002945.
42. Uehara T, Bernhardt TG. 2011. More than just lysins: peptidoglycan hydrolases tailor the cell wall. Curr. Opin. Microbiol. 14:698-703.
43. Keiler KC, Sauer RT. 1995. Identification of active site residues of the Tsp protease. J. Biol. Chem. 270:28864-28868.
44. Bochner BR. 2003. New technologies to assess genotype-phenotype relationships. Nat. Rev. Genet. 4:309-314.
45. Cabral JP. 1991. Damage to the cytoplasmic membrane and cell death caused by dodine (dodecylguanidine monoacetate) in Pseudomonas syringae ATCC 12271. Antimicrob. Agents Chemother. 35:341-344.
46. Lee VT, Smith RS, Tummler B, Lory S. 2005. Activities of Pseudomonas aeruginosa effectors secreted by the type III secretion system in vitro and during infection. Infect. Immun. 73:1695-1705.
47. Head NE. 2006. Regulation of biofilm formation of Pseudomonas aeruginosa. Ph. D. thesis. Marshall University, Huntington, WV.
48. Staron A, Sofia HJ, Dietrich S, Ulrich LE, Liesegang H, Mascher T. 2009. The third pillar of bacterial signal transduction: classification of the extracytoplasmic function (ECF) sigma factor protein family. Mol. Microbiol. 74:557-581.
49. Potvin E, Lehoux DE, Kukavica-Ibrulj I, Richard KL, Sanschagrin F, Lau GW, Levesque RC. 2003. In vivo functional genomics of Pseudomonas aeruginosa for high-throughput screening of new virulence factors and antibacterial targets. Environ. Microbiol. 5:1294-1308.
50. Ho TD, Ellermeier CD. 2012. Extra cytoplasmic function sigma factor activation. Curr. Opin. Microbiol. 15:182-188.
51. Helmann JD. 2002. The extracytoplasmic function (ECF) sigma factors. Adv. Microb. Physiol. 46:47-110.
52. Wood LF, Ohman DE. 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.
53. Brooks BE, Buchanan SK. 2008. Signaling mechanisms for activation of extracytoplasmic function (ECF) sigma factors. Biochim. Biophys. Acta 1778:1930-1945.
54. Yeung AT, Torfs EC, Jamshidi F, Bains M, Wiegand I, Hancock RE, Overhage J. 2009. Swarming of Pseudomonas aeruginosa is controlled by a broad spectrum of transcriptional regulators, including MetR. J. Bacteriol. 191:5592-5602.
55. Seoane A, Sabbaj A, McMurry LM, Levy SB. 1992. Multiple antibiotic susceptibility associated with inactivation of the prc gene. J. Bacteriol. 174:7844-7847.
56. O'Toole GA, Kolter R. 1998. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 30:295-304.
57. Rietsch A, Vallet-Gely I, Dove SL, Mekalanos JJ. 2005. ExsE, a secreted regulator of type III secretion genes in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. U. S. A. 102:8006-8011.
58. Urbanowski ML, Lykken GL, Yahr TL. 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.
59. Howard SP, Gebhart C, Langen GR, Li G, Strozen TG. 2006. Interactions between peptidoglycan and the ExeAB complex during assembly of the type II secretin of Aeromonas hydrophila. Mol. Microbiol. 59:1062-1072.
60. Pucciarelli MG, Garcia-del Portillo F. 2003. Protein-peptidoglycan interactions modulate the assembly of the needle complex in the Salmonella invasion-associated type III secretion system. Mol. Microbiol. 48:573-585.
61. Dotsch A, Eckweiler D, Schniederjans M, Zimmermann A, Jensen V, Scharfe M, Geffers R, Haussler S. 2012. The Pseudomonas aeruginosa transcriptome in planktonic cultures and static biofilms using RNA sequencing. PLoS One 7:e31092. doi:10.1371/journal.pone.0031092.
62. Moir DT, Di M, Moore RA, Schweizer HP, Woods DE. 2008. Cellular reporter screens for inhibitors of Burkholderia pseudomallei targets in Pseudomonas aeruginosa. Trans. R. Soc. Trop. Med. Hyg. 102(Suppl 1): S152-S162.
63. Anbudurai PR, Mor TS, Ohad I, Shestakov SV, Pakrasi HB. 1994. The ctpA gene encodes the C-terminal processing protease for the D1 protein of the photosystem II reaction center complex. Proc. Natl. Acad. Sci. U. S. A. 91:8082-8086.
64. Shestakov SV, Anbudurai PR, Stanbekova GE, Gadzhiev A, Lind LK, Pakrasi HB. 1994. Molecular cloning and characterization of the ctpA gene encoding a carboxyl-terminal processing protease. J. Biol. Chem. 269:19354-19359.
65. Goodman AL, Kulasekara B, Rietsch A, Boyd D, Smith RS, Lory S. 2004. A signaling network reciprocally regulates genes associated with acute infection and chronic persistence in Pseudomonas aeruginosa. Dev. Cell 7:745-754.
66. Qiu D, Damron FH, Mima T, Schweizer HP, Yu HD. 2008. PBAD-based shuttle vectors for functional analysis of toxic and highly regulated genes in Pseudomonas and Burkholderia spp. and other bacteria. Appl. Environ. Microbiol. 74:7422-7426.
67. Hoang TT, Karkhoff-Schweizer RR, Kutchma AJ, Schweizer HP. 1998. A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212:77-86.
68. de Lorenzo V, Eltis L, Kessler B, Timmis KN. 1993. Analysis of Pseudomonas gene products using lacIq/Ptrp-lac plasmids and transposons that confer conditional phenotypes. Gene 123:17-24.