Hcp family proteins secreted via the type VI secretion system coordinately regulate Escherichia coli K1 interaction with human brain microvascular endothelial cells

Infection and Immunity

Volumn 80, Issue 3, 2012, Pages 1243-1251

  Zhou, Yan ^a,b   Tao, Jing ^a   Yu, Hao ^c   Ni, Jinjing ^a   Zeng, Lingbing ^a   Teng, Qihui ^a   Kim, Kwang Sik ^c   Zhao, Guo Ping ^d   Guo, Xiaokui ^a   Yao, Yufeng ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b SHANGHAI CHEST HOSPITAL   (China)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d INSTITUTE OF PLANT PHYSIOLOGY AND ECOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CASPASE 8; HEMOLYSIN COREGULATED PROTEIN; HEMOLYSIN COREGULATED PROTEIN 1; INTERLEUKIN 6; INTERLEUKIN 8; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ACTIN FILAMENT; APOPTOSIS; ARTICLE; BACTERIAL SURVIVAL; CELL INTERACTION; CONTROLLED STUDY; CYTOKINE RELEASE; ESCHERICHIA COLI; ESCHERICHIA COLI K1; GENE CLUSTER; GENE DELETION; HUMAN; HUMAN CELL; MICROVASCULAR ENDOTHELIAL CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN SECRETION; SEQUENCE ANALYSIS; TYPE VI SECRETION SYSTEM;

BACTERIAL ADHESION; BACTERIAL CAPSULES; CELLS, CULTURED; ENDOTHELIAL CELLS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HUMANS; MEMBRANE TRANSPORT PROTEINS; VIRULENCE FACTORS;

EID: 84863230242     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.05994-11     Document Type: Article

References (50)

1. Aschtgen MS, Gavioli M, Dessen A, Lloubes R, Cascales E. 2010. The SciZ protein anchors the enteroaggregative Escherichia coli type VI secretion system to the cell wall. Mol. Microbiol. 75:886-899.
2. Aubert DF, Flannagan RS, Valvano MA. 2008. A novel sensor kinaseresponse regulator hybrid controls biofilm formation and type VI secretion system activity in Burkholderia cenocepacia. Infect. Immun. 76:1979-1991.
3. Cascales E. 2008. The type VI secretion toolkit. EMBO Rep. 9:735-741.
4. Charpentier X, Oswald E. 2004. Identification of the secretion and translocation domain of the enteropathogenic and enterohemorrhagic Escherichia coli effector Cif, using TEM-1 beta-lactamase as a new fluorescencebased reporter. J. Bacteriol. 186:5486-5495.
5. 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.
6. de Pace F, et al. 2010. The type VI secretion system plays a role in type 1 fimbria expression and pathogenesis of an avian pathogenic Escherichia coli strain. Infect. Immun. 78:4990-4998.
7. Dudley EG, Thomson NR, Parkhill J, Morin NP, Nataro JP. 2006. Proteomic and microarray characterization of the AggR regulon identifies a pheU pathogenicity island in enteroaggregative Escherichia coli. Mol. Microbiol. 61:1267-1282.
8. Eisenhauer PB, et al. 2004. Escherichia coli Shiga toxin 1 and TNF-alpha induce cytokine release by human cerebral microvascular endothelial cells. Microb. Pathog. 36:189-196.
9. Filloux A, Hachani A, Bleves S. 2008. The bacterial type VI secretion machine: yet another player for protein transport across membranes. Microbiology 154:1570-1583.
10. Fiorentini C, Falzano L, Travaglione S, Fabbri A. 2003. Hijacking Rho GTPases by protein toxins and apoptosis: molecular strategies of pathogenic bacteria. Cell Death Differ. 10:147-152.
11. Galanakis E, Di Cello F, Paul-Satyaseela M, Kim KS. 2006. Escherichia coli K1 induces IL-8 expression in human brain microvascular endothelial cells. Eur. Cytokine Netw. 17:260-265.
12. 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.
13. Hood RD, et al. 2010. A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe 7:25-37.
14. Ishikawa T, Rompikuntal PK, Lindmark B, Milton DL, Wai SN. 2009. Quorum sensing regulation of the two hcp alleles in Vibrio cholerae O1 strains. PLoS One 4:e6734.
15. Jayasekera S, Matin A, Sissons J, Maghsood AH, Khan NA. 2005. Balamuthia mandrillaris stimulates interleukin-6 release in primary human brain microvascular endothelial cells via a phosphatidylinositol 3-kinase-dependent pathway. Microbes Infect. 7:1345-1351.
16. Khan NA, Kim Y, Shin S, Kim KS. 2007. FimH-mediated Escherichia coli K1 invasion of human brain microvascular endothelial cells. Cell Microbiol. 9:169-178.
17. Khan NA, et al. 2003. Outer membrane protein A and cytotoxic necrotizing factor-1 use diverse signaling mechanisms for Escherichia coli K1 invasion of human brain microvascular endothelial cells. Microb. Pathog. 35:35-42.
18. Khan NA, et al. 2002. Cytotoxic necrotizing factor-1 contributes to Escherichia coli K1 invasion of the central nervous system. J. Biol. Chem. 277:15607-15612.
19. Kim KJ, Elliott SJ, Di Cello F, Stins MF. 2003. The K1 capsule modulates trafficking of E. coli-containing vacuoles and enhances intracellular bacterial survival in human brain microvascular endothelial cells. Cell Microbiol. 5:245-252.
20. Kim KS. 2003. Neurological diseases: pathogenesis of bacterial meningitis: from bacteremia to neuronal injury. Nat. Rev. Neurosci. 4:376-385.
21. Ledesma MA, et al. 2010. The hemorrhagic coli pilus (HCP) of Escherichia coli O157:H7 is an inducer of proinflammatory cytokine secretion in intestinal epithelial cells. PLoS One 5:e12127.
22. Leiman PG, et al. 2009. Type VI secretion apparatus and phage tailassociated protein complexes share a common evolutionary origin. Proc. Natl. Acad. Sci. U. S. A. 106:4154-4159.
23. Lloyd AL, Henderson TA, Vigil PD, Mobley HL. 2009. Genomic islands of uropathogenic Escherichia coli contribute to virulence. J. Bacteriol. 191:3469-3481.
24. Ma AT, McAuley S, Pukatzki S, Mekalanos JJ. 2009. Translocation of a Vibrio cholerae type VI secretion effector requires bacterial endocytosis by host cells. Cell Host Microbe 5:234-243.
25. Moriel DG, et al. 2010. Identification of protective and broadly conserved vaccine antigens from the genome of extraintestinal pathogenic Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 107:9072-9077.
26. Mougous JD, et al. 2006. A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science 312:1526-1530.
27. Parthasarathy G, Yao Y, Kim KS. 2007. Flagella promote Escherichia coli K1 association with and invasion of human brain microvascular endothelial cells. Infect. Immun. 75:2937-2945.
28. Pell LG, Kanelis V, Donaldson LW, Howell PL, Davidson AR. 2009. The phage lambda major tail protein structure reveals a common evolution for long-tailed phages and the type VI bacterial secretion system. Proc. Natl. Acad. Sci. U. S. A. 106:4160-4165.
29. Prasadarao NV, et al. 1996. Outer membrane protein A of Escherichia coli contributes to invasion of brain microvascular endothelial cells. Infect. Immun. 64:146-153.
30. Pukatzki S, Ma AT, Revel AT, Sturtevant D, Mekalanos JJ. 2007. Type VI secretion system translocates a phage tail spike-like protein into target cells where it cross-links actin. Proc. Natl. Acad. Sci. U. S. A. 104:15508-15513.
31. Pukatzki S, et al. 2006. Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc. Natl. Acad. Sci. U. S. A. 103:1528-1533.
32. Rao PS, Yamada Y, Tan YP, Leung KY. 2004. Use of proteomics to identify novel virulence determinants that are required for Edwardsiella tarda pathogenesis. Mol. Microbiol. 53:573-586.
33. Russo TA, et al. 2005. E. coli virulence factor hemolysin induces neutrophil apoptosis and necrosis/lysis in vitro and necrosis/lysis and lung injury in a rat pneumonia model. Am. J. Physiol. Lung Cell. Mol. Physiol. 289: L207-L216.
34. Schell MA, et al. 2007. Type VI secretion is a major virulence determinant in Burkholderia mallei. Mol. Microbiol. 64:1466-1485.
35. Shrivastava S, Mande SS. 2008. Identification and functional characterization of gene components of type VI secretion system in bacterial genomes. PLoS One 3:e2955.
36. Suarez G, et al. 2010. A type VI secretion system effector protein, VgrG1, from Aeromonas hydrophila that induces host cell toxicity by ADP ribosylation of actin. J. Bacteriol. 192:155-168.
37. Suarez G, et al. 2008. Molecular characterization of a functional type VI secretion system from a clinical isolate of Aeromonas hydrophila. Microb. Pathog. 44:344-361.
38. Tenenbaum T, et al. 2007. Streptococcus agalactiae invasion of human brain microvascular endothelial cells is promoted by the laminin-binding protein Lmb. Microbes Infect. 9:714-720.
39. Teng CH, et al. 2005. Escherichia coli K1 RS218 interacts with human brain microvascular endothelial cells via type 1 fimbria bacteria in the fimbriated state. Infect. Immun. 73:2923-2931.
40. Teng CH, et al. 2010. NlpI contributes to Escherichia coli K1 strain RS218 interaction with human brain microvascular endothelial cells. Infect. Immun. 78:3090-3096.
41. Teng CH, et al. 2006. Effects of ompA deletion on expression of type 1 fimbriae in Escherichia coli K1 strain RS218 and on the association of E. coli with human brain microvascular endothelial cells. Infect. Immun. 74:5609-5616.
42. van Furth AM, Roord JJ, van Furth R. 1996. Roles of proinflammatory and anti-inflammatory cytokines in pathophysiology of bacterial meningitis and effect of adjunctive therapy. Infect. Immun. 64:4883-4890.
43. Williams SG, Varcoe LT, Attridge SR, Manning PA. 1996. Vibrio cholerae Hcp, a secreted protein coregulated with HlyA. Infect. Immun. 64:283-289.
44. Wu HY, Chung PC, Shih HW, Wen SR, Lai EM. 2008. Secretome analysis uncovers an Hcp-family protein secreted via a type VI secretion system in Agrobacterium tumefaciens. J. Bacteriol. 190:2841-2850.
45. Xie Y, et al. 2006. Identification and characterization of Escherichia coli RS218-derived islands in the pathogenesis of E. coli meningitis. J. Infect. Dis. 194:358-364.
46. Xie Y, Yao Y, Kolisnychenko V, Teng CH, Kim KS. 2006. HbiF regulates type 1 fimbriation independently of FimB and FimE. Infect. Immun. 74:4039-4047.
47. Yao Y, Xie Y, Kim KS. 2006. Genomic comparison of Escherichia coli K1 strains isolated from the cerebrospinal fluid of patients with meningitis. Infect. Immun. 74:2196-2206.
48. Yao Y, et al. 2009. The type III secretion system is involved in the invasion and intracellular survival of Escherichia coli K1 in human brain microvascular endothelial cells. FEMS Microbiol. Lett. 300:18-24.
49. Yu H, Kim KS. 2010. Ferredoxin is involved in secretion of cytotoxic necrotizing factor 1 across the cytoplasmic membrane in Escherichia coli K1. Infect. Immun. 78:838-844.
50. Zheng J, Leung KY. 2007. Dissection of a type VI secretion system in Edwardsiella tarda. Mol. Microbiol. 66:1192-1206.