Enterohemorrhagic escherichia coli virulence regulation by two bacterial adrenergic kinases, QseC and QseE

Infection and Immunity

Volumn 80, Issue 2, 2012, Pages 688-703

  Njoroge, Jacqueline ^a   Sperandio, Vanessa ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADRENALIN; PROTEIN HISTIDINE KINASE; TRANSCRIPTOME; VIRULENCE FACTOR;

ARTICLE; BACTERIAL GENE; BACTERIAL VIRULENCE; CELL ADHESION; CELL CULTURE; ENTEROHEMORRHAGIC ESCHERICHIA COLI; EPITHELIUM CELL; GENE DELETION; GENE LOCUS; GENETIC TRANSCRIPTION; HELA CELL; HUMAN; HUMAN CELL; NONHUMAN; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL;

ENTEROHEMORRHAGIC ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HELA CELLS; HUMANS; RECEPTORS, ADRENERGIC; SIGNAL TRANSDUCTION; VIRULENCE;

EID: 84857175330     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.05921-11     Document Type: Article

References (80)

1. Bailey MT, Karaszewski JW, Lubach GR, Coe CL, Lyte M. 1999. In vivo adaptation of attenuated Salmonella typhimurium results in increased growth upon exposure to norepinephrine. Physiol. Behav. 67:359 -364.
2. Barba J, et al. 2005. A positive regulatory loop controls expression of the locus of enterocyte effacement-encoded regulators Ler and GrlA. J. Bacteriol. 187:7918 -7930.
3. Bearson BL, Bearson SM. 2008. The role of the QseC quorum-sensing sensor kinase in colonization and norepinephrine-enhanced motility of Salmonella enterica serovar Typhimurium. Microb. Pathog. 44:271-278.
4. Bearson BL, Bearson SM, Lee IS, Brunelle BW. 2010. The Salmonella enterica serovar Typhimurium QseB response regulator negatively regulates bacterial motility and swine colonization in the absence of the QseC sensor kinase. Microb. Pathog. 48:214 -219.
5. Bolstad BM, Irizarry RA, Astrand M, Speed TP. 2003. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19:185-193.
6. Bustamante VH, Santana FJ, Calva E, Puente JL. 2001. Transcriptional regulation of type III secretion genes in enteropathogenic Escherichia coli: Ler antagonizes H-NS-dependent repression. Mol. Microbiol. 39:664-678.
7. Campellone KG, Robbins D, Leong JM. 2004. EspFU is a translocated EHEC effector that interacts with Tir and N-WASP and promotes Nckindependent actin assembly. Dev. Cell 7:217-228.
8. Clarke MB, Hughes DT, Zhu C, Boedeker EC, Sperandio V. 2006. The QseC sensor kinase: a bacterial adrenergic receptor. Proc. Natl. Acad. Sci. U. S. A. 103:10420 -10425.
9. Clarke MB, Sperandio V. 2005. Transcriptional autoregulation by quorum sensing Escherichia coli regulators B and C (QseBC) in enterohaemorrhagic E. coli (EHEC). Mol. Microbiol. 58:441-455.
10. Clarke MB, Sperandio V. 2005. Transcriptional regulation of flhDC by QseBC and sigma (FliA) in enterohaemorrhagic Escherichia coli. Mol. Microbiol. 57:1734 -1749.
11. Datsenko KA, Wanner BL. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A. 97:6640-6645.
12. Eberhard A. 1972. Inhibition and activation of bacterial luciferase synthesis. J. Bacteriol. 109:1101-1105.
13. Elliott SJ, et al. 1998. The complete sequence of the locus of enterocyte effacement (LEE) from enteropathogenic Escherichia coli E2348/69. Mol. Microbiol. 28:1-4.
14. Gao R, Stock AM. 2009. Biological insights from structures of twocomponent proteins. Annu. Rev. Microbiol. 63:133-154.
15. Garmendia J, et al. 2004. TccP is an enterohaemorrhagic Escherichia coli O157:H7 type III effector protein that couples Tir to the actincytoskeleton. Cell. Microbiol. 6:1167-1183.
16. Gilman AG. 1987. G proteins: transducers of receptor-generated signals. Annu. Rev. Biochem. 56:615-649.
17. Gotoh Y, et al. 2010. Two-component signal transduction as potential drug targets in pathogenic bacteria. Curr. Opin. Microbiol. 13:232-239.
18. Griffin PM, et al. 1988. Illnesses associated with Escherichia coli O157:H7 infections. A broad clinical spectrum. Ann. Intern. Med. 109:705-712.
19. Gruenheid S, et al. 2004. Identification and characterization of NleA, a non-LEE-encoded type III translocated virulence factor of enterohaemorrhagic Escherichia coli O157:H7. Mol. Microbiol. 51:1233-1249.
20. Guzman LM, Belin D, Carson MJ, Beckwith J. 1995. Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J. Bacteriol. 177:4121-4130.
21. Hughes DT, Clarke MB, Yamamoto K, Rasko DA, Sperandio V. 2009. The QseC adrenergic signaling cascade in enterohemorrhagic E. coli (EHEC). PLoS Pathog. 5:e1000553.
22. Hughes DT, Sperandio V. 2008. Inter-kingdom signaling: communication between bacteria and host. Nat. Rev. Microbiol. 6:111-120.
23. Irizarry RA, et al. 2003. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4:249 -264.
24. Islam MS, Bingle LE, Pallen MJ, Busby SJ. 2010. Organization of the LEE1 operon regulatory region of enterohaemorrhagic Escherichia coli O157:H7 and activation by GrlA. Mol. Microbiol. 79:468-483.
25. Iyoda S, Watanabe H. 2004. Positive effects of multiple pch genes on expression of the locus of enterocyte effacement genes and adherence of enterohaemorrhagic Escherichia coli O157:H7 to HEp-2 cells. Microbiology 150:2357-2571.
26. Jarvis KG, et al. 1995. Enteropathogenic Escherichia coli contains a putative type III secretion system necessary for the export of proteins involved in attaching and effacing lesion formation. Proc. Natl. Acad. Sci. U. S. A. 92:7996-8000.
27. Jarvis KG, Kaper JB. 1996. Secretion of extracellular proteins by enterohemorrhagic Escherichia coli via a putative type III secretion system. Infect. Immun. 64:4826-4829.
28. Jerse AE, Kaper JB. 1991. The eae gene of enteropathogenic Escherichia coli encodes a 94-kilodalton membrane protein, the expression of which is influenced by the EAF plasmid. Infect. Immun. 59:4302-4309.
29. Jerse AE, Yu J, Tall BD, Kaper JB. 1990. A genetic locus of enteropathogenic Escherichia coli necessary for the production of attaching and effacing lesions on tissue culture cells. Proc. Natl. Acad. Sci. U. S. A. 87:7839-7843.
30. Kailasan Vanaja S, Bergholz TM, Whittam TS. 2009. Characterization of the Escherichia coli O157:H7 Sakai GadE regulon. J. Bacteriol. 191:1868-1877.
31. Kaper JB, Nataro JP, Mobley HL. 2004. Pathogenic Escherichia coli. Nat. Rev. Microbiol. 2:123-140.
32. Kendall MM, Gruber CC, Rasko DA, Hughes DT, Sperandio V. 2011. Hfq virulence regulation in enterohemorrhagic Escherichia coli O157:H7 strain 86-24. J. Bacteriol. 193:6843-6851.
33. Kenny B, et al. 1997. Enteropathogenic E. coli (EPEC) transfers its receptor for intimate adherence into mammalian cells. Cell 91:511-520.
34. Kenny B, Lai LC, Finlay BB, Donnenberg MS. 1996. EspA, a protein secreted by enteropathogenic Escherichia coli, is required to induce signals in epithelial cells. Mol. Microbiol. 20:313-323.
35. Kim J, et al. 2007. The bacterial virulence factor NleA inhibits cellular protein secretion by disrupting mammalian COPII function. Cell Host Microbe 2:160 -171.
36. Knutton S, Baldwin T, Williams PH, McNeish AS. 1989. Actin accumulation at sites of bacterial adhesion to tissue culture cells: basis of a new diagnostic test for enteropathogenic and enterohemorrhagic Escherichia coli. Infect. Immun. 57:1290 -1298.
37. Kostakioti M, Hadjifrangiskou M, Pinkner JS, Hultgren SJ. 2009. QseCmediated dephosphorylation of QseB is required for expression of genes associated with virulence in uropathogenic Escherichia coli. Mol. Microbiol. 73:1020 -1031.
38. Kresse AU, Beltrametti F, Muller A, Ebel F, Guzman CA. 2000. Characterization of SepL of enterohemorrhagic Escherichia coli. J. Bacteriol. 182:6490-6498.
39. Li L, et al. 2002. A global pH sensor: Agrobacterium sensor protein ChvG regulates acid-inducible genes on its two chromosomes and Ti plasmid. Proc. Natl. Acad. Sci. U. S. A. 99:12369 -12374.
40. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193:265-275.
41. Lyte M, Arulanandam BP, Frank CD. 1996. Production of Shiga-like toxins by Escherichia coli O157:H7 can be influenced by the neuroendocrine hormone norepinephrine. J. Lab. Clin. Med. 128:392-398.
42. Lyte M, et al. 1997. Norepinephrine-induced expression of the K99 pilus adhesin of enterotoxigenic Escherichia coli. Biochem. Biophys. Res. Commun. 232:682-686.
43. McCarthy Y, et al. 2010. A sensor kinase recognizing the cell-cell signal BDSF (cis-2-dodecenoic acid) regulates virulence in Burkholderia cenocepacia. Mol. Microbiol. 77:1220 -1236.
44. McDaniel TK, Jarvis KG, Donnenberg MS, Kaper JB. 1995. A genetic locus of enterocyte effacement conserved among diverse enterobacterial pathogens. Proc. Natl. Acad. Sci. U. S. A. 92:1664 -1668.
45. Mellies JL, Elliott SJ, Sperandio V, Donnenberg MS, Kaper JB. 1999. The Per regulon of enteropathogenic Escherichia coli: identification of a regulatory cascade and a novel transcriptional activator, the locus of enterocyte effacement (LEE)-encoded regulator (Ler). Mol. Microbiol. 33: 296-306.
46. Mitrophanov AY, Groisman EA. 2008. Signal integration in bacterial two-component regulatory systems. Genes Dev. 22:2601-2611.
47. Mokrievich AN, et al. 2010. Biological properties and structure of the lipopolysaccharide of a vaccine strain of Francisella tularensis generated by inactivation of a quorum sensing system gene qseC. Biochemistry (Mosc.). 75:443-451.
48. Moon HW, Whipp SC, Argenzio RA, Levine MM, Giannella RA. 1983. Attaching and effacing activities of rabbit and human enteropathogenic Escherichia coli in pig and rabbit intestines. Infect. Immun. 41:1340-1351.
49. Moreira CG, Weinshenker D, Sperandio V. 2009. QseC mediates Salmonella enterica serovar Typhimurium virulence in vitro and in vivo. Infect. Immun. 78:914 -926.
50. Mundy R, Jenkins C, Yu J, Smith H, Frankel G. 2004. Distribution of espI among clinical enterohaemorrhagic and enteropathogenic Escherichia coli isolates. J. Med. Microbiol. 53:1145-1149.
51. Mundy R, et al. 2004. Identification of a novel Citrobacter rodentium type III secreted protein, EspI, and roles of this and other secreted proteins in infection. Infect. Immun. 72:2288 -2302.
52. Nakano M, Takahashi A, Sakai Y, Nakaya Y. 2007. Modulation of pathogenicity with norepinephrine related to the type III secretion system of Vibrio parahaemolyticus. J. Infect. Dis. 195:1353-1360.
53. Nakayama J, et al. 2001. Gelatinase biosynthesis-activating pheromone: a peptide lactone that mediates a quorum sensing in Enterococcus faecalis. Mol. Microbiol. 41:145-154.
54. Nealson KH. 1977. Autoinduction of bacterial luciferase. Occurrence, mechanism and significance. Arch. Microbiol. 112:73-79.
55. Nealson KH, Platt T, Hastings JW. 1970. Cellular control of the synthesis and activity of the bacterial luminescent system. J. Bacteriol. 104:313-322.
56. Neves BC, et al. 1998. Molecular and ultrastructural characterisation of EspA from different enteropathogenic Escherichia coli serotypes. FEMS Microbiol. Lett. 169:73-80.
57. Novak EA, Shao H, Daep CA, Demuth DR. 2010. Autoinducer-2 and QseC control biofilm formation and in vivo virulence of Aggregatibacter actinomycetemcomitans. Infect. Immun. 78:2919 -2926.
58. Parkinson JS, Kofoid EC. 1992. Communication modules in bacterial signaling proteins. Annu. Rev. Genet. 26:71-112.
59. Rasko DA, et al. 2008. Targeting QseC signaling and virulence for antibiotic development. Science 321:1078 -1080.
60. Reading NC, Rasko D, Torres AG, Sperandio V. 2010. A transcriptome study of the QseEF two-component system and the QseG membrane protein in enterohaemorrhagic Escherichia coli O157:H7. Microbiology 156: 1167-1175.
61. Reading NC, Rasko DA, Torres AG, Sperandio V. 2009. The twocomponent system QseEF and the membrane protein QseG link adrenergic and stress sensing to bacterial pathogenesis. Proc. Natl. Acad. Sci. U. S. A. 106:5889 -5894.
62. Reading NC, et al. 2007. A novel two-component signaling system that activates transcription of an enterohemorrhagic Escherichia coli effector involved in remodeling of host actin. J. Bacteriol. 189:2468 -2476.
63. Roe AJ, et al. 2007. Analysis of the expression, regulation and export of NleA-E in Escherichia coli O157:H7. Microbiology 153:1350 -1360.
64. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
65. Sanchez-SanMartin C, Bustamante VH, Calva E, Puente JL. 2001. Transcriptional regulation of the orf19 gene and the tir-cesT-eae operon of enteropathogenic Escherichia coli. J. Bacteriol. 183:2823-2833.
66. Shapiro JA. 1998. Thinking about bacterial populations as multicellular organisms. Annu. Rev. Microbiol. 52:81-104.
67. Sharp FC, Sperandio V. 2007. QseA directly activates transcription of LEE1 in enterohemorrhagic Escherichia coli. Infect. Immun. 75:2432-2440.
68. Simons RW, Houman F, Kleckner N. 1987. Improved single and multicopy lac-based cloning vectors for protein and operon fusions. Gene 53:85-96.
69. Sperandio V, et al. 2000. Activation of enteropathogenic Escherichia coli (EPEC) LEE2 and LEE3 operons by Ler. Mol. Microbiol. 38:781-793.
70. Sperandio V, Torres AG, Giron JA, Kaper JB. 2001. Quorum sensing is a global regulatory mechanism in enterohemorrhagic Escherichia coli O157:H7. J. Bacteriol. 183:5187-5197.
71. Sperandio V, Torres AG, Jarvis B, Nataro JP, Kaper JB. 2003. Bacteriahost communication: the language of hormones. Proc. Natl. Acad. Sci. U. S. A. 100:8951-8956.
72. Sperandio V, Torres AG, Kaper JB. 2002. Quorum sensing Escherichia coli regulators B and C (QseBC): a novel two-component regulatory system involved in the regulation of flagella and motility by quorum sensing in E. coli. Mol. Microbiol. 43:809-821.
73. Staley TE, Jones EW, Corley LD. 1969. Attachment and penetration of Escherichia coli into intestinal epithelium of the ileum in newborn pigs. Am. J. Pathol. 56:371-392.
74. Thanabalasuriar A, et al. 2009. The bacterial virulence factor NleA is required for the disruption of intestinal tight junctions by enteropathogenic Escherichia coli. Cell. Microbiol. 12:31-41.
75. Tiaden A, et al. 2010. The autoinducer synthase LqsA and putative sensor kinase LqsS regulate phagocyte interactions, extracellular filaments and a genomic island of Legionella pneumophila. Environ. Microbiol. 12:1243-1259.
76. Tobe T, et al. 2005. Dual regulatory pathways integrating the RcsC-RcsDRcsB signalling system control enterohaemorrhagic Escherichia coli pathogenicity. Mol. Microbiol. 58:320 -333.
77. Tobe T, et al. 2006. An extensive repertoire of type III secretion effectors in Escherichia coli O157 and the role of lambdoid phages in their dissemination. Proc. Natl. Acad. Sci. U. S. A. 103:14941-14946.
78. Walters M, Sperandio V. 2006. Autoinducer 3 and epinephrine signaling in the kinetics of locus of enterocyte effacement gene expression in enterohemorrhagic Escherichia coli. Infect. Immun. 74:5445-5455.
79. Wang X, et al. 2011. QseBC controls flagellar motility, fimbrial hemagglutination and intracellular virulence in fish pathogen Edwardsiella tarda. Fish Shellfish Immunol. 30:944 -953.
80. Yamamoto K, et al. 2005. Functional characterization in vitro of all two-component signal transduction systems from Escherichia coli. J. Biol. Chem. 280:1448 -1456.