OmpA is the critical component for escherichia coli invasion-induced astrocyte activation

Journal of Neuropathology and Experimental Neurology

Volumn 68, Issue 6, 2009, Pages 677-690

  Wu, Hsueh Hsia ^a,b   Yang, Yi Yuan ^b   Hsieh, Wen Shyang ^c   Lee, Chi Hsin ^b   Leu, Sy Jye C ^b   Chen, Mei Ru ^a  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^c MACKAY MEMORIAL HOSPITAL   (Taiwan)

Author keywords

Astrocyte; Cyclooxygenase 2; Escherichia coli; Glial fibrillary acidic protein; Nitric oxide synthase 2; Outer membrane protein A

Indexed keywords

ACTIN; CYCLOOXYGENASE 2; GLIAL FIBRILLARY ACIDIC PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; OUTER MEMBRANE PROTEIN A; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN TYROSINE KINASE; ENOLASE; ESCHERICHIA COLI PROTEIN; NOS2 PROTEIN, MOUSE; OMPA OUTER MEMBRANE PROTEINS; OUTER MEMBRANE PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BACTERIAL STRAIN; BACTERIUM ADHERENCE; BRAIN DAMAGE; BRAIN INFECTION; BRAIN TISSUE; CELL ACTIVATION; CELL DIFFERENTIATION; CELL INVASION; CONTROLLED STUDY; ESCHERICHIA COLI; GLIOMA CELL; IN VITRO STUDY; MOUSE; NEUROPROTECTION; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REACTION ANALYSIS; SURVIVAL RATE; TISSUE SECTION; ANIMAL; C57BL MOUSE; ESCHERICHIA COLI INFECTION; GENE EXPRESSION REGULATION; GLIOMA; METABOLISM; MICROBIOLOGY; MORTALITY; PATHOGENICITY; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; SURVIVAL; TIME; TUMOR CELL LINE;

ACTINS; ANIMALS; ASTROCYTES; BACTERIAL OUTER MEMBRANE PROTEINS; CELL LINE, TUMOR; CYCLOOXYGENASE 2; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GLIAL FIBRILLARY ACIDIC PROTEIN; GLIOMA; MICE; MICE, INBRED C57BL; NITRIC OXIDE SYNTHASE TYPE II; PHOSPHOPYRUVATE HYDRATASE; RATS; SIGNAL TRANSDUCTION; SURVIVAL ANALYSIS; TIME FACTORS;

EID: 67649389709     PISSN: 00223069     EISSN: None     Source Type: Journal    
DOI: 10.1097/NEN.0b013e3181a77d1e     Document Type: Article

References (53)

1. Shah DK, Daley AJ, Hunt RW, et al. Cerebral white matter injury in the newborn following Escherichia coli meningitis. Eur J Paediatr Neurol 2005;9:13-17
2. Leib SL, Tauber MG. Pathogenesis of bacterial meningitis. Infect Dis Clin North Am 1999;13:527-48, vYvi. Review
3. Kim KS. Escherichia coli translocation at the blood-brain barrier. Infect Immun 2001;69:5217-5222
4. Teng CH, Cai M, Shin S, et al. Escherichia coli K1 RS218 interacts with human brain microvascular endothelial cells via type 1 fimbria bacteria in the fimbriated state. Infect Immun 2005;73:2923-2931
5. Hoffman JA, Wass C, Stins MF, et al. The capsule supports survival but not traversal of Escherichia coli K1 across the blood-brain barrier. Infect Immun 1999;67:3566-3570
6. Khan NA, Shin S, Chung JW, et al. Outer membrane protein A and cytotoxic necrotizing factorY1 use diverse signaling mechanisms for Escherichia coli K1 invasion of human brain microvascular endothelial cells. Microb Pathog 2003;35:35-42
7. Kim KS. Pathogenesis of bacterial meningitis: From bacteraemia to neuronal injury. Nat Rev Neurosci 2003;4:376-385
8. Shin S, Lu G, Cai M, et al. Escherichia coli outer membrane protein A adheres to human brain microvascular endothelial cells. Biochem Biophys Res Commun 2005;330:1199-1204
9. Koebnik R. Structural and functional roles of the surface-exposed loops of the beta-barrel membrane protein OmpA from Escherichia coli. J Bacteriol 1999;181:3688-3694
10. Klimke WA, Frost LS. Genetic analysis of the role of the transfer gene, traN, of the F and R100-1 plasmids in mating pair stabilization during conjugation. J Bacteriol 1998;180:4036-4043
11. Klimke WA, Rypien CD, Klinger B, et al. The mating pair stabilization protein, TraN, of the F plasmid is an outer-membrane protein with two regions that are important for its function in conjugation. Microbiology 2005;151:3527-3540
12. Schwarz H, Riede I, Sonntag I, et al. Degrees of relatedness of T-even type E. coli phages using different or the same receptors and topology of serologically cross-reacting sites. EMBO J 1983;2:375-380
13. Morona R, Klose M, Henning U. Escherichia coli K-12 outer membrane protein (OmpA) as a bacteriophage receptor: Analysis of mutant genes expressing altered proteins. J Bacteriol 1984;159:570-578
14. Riede I, Eschbach ML, Henning U. DNA sequence heterogeneity in the genes of T-even type Escherichia coli phages encoding the receptor recognizing protein of the long tail fibers. Mol Gen Genet 1984;195: 144-152
15. Montag D, Riede I, Eschbach ML, et al. Receptor-recognizing proteins of T-even type bacteriophages. Constant and hypervariable regions and an unusual case of evolution. J Mol Biol 1987;196:165-174
16. Pautsch A, Schulz GE. Structure of the outer membrane protein A transmembrane domain. Nat Struct Biol 1998;5:1013-1017
17. Prasadarao NV, Wass CA, Weiser JN, et al. Outer membrane protein A of Escherichia coli contributes to invasion of brain microvascular endothelial cells. Infect Immun 1996;64:146-153
18. Condorelli DF, Dell'Albani P, Kaczmarek L, et al. Glial fibrillary acidic protein messenger RNA and glutamine synthetase activity after nervous system injury. J Neurosci Res 1990;26:251-257
19. Chiu FC, Norton WT, Fields KL. The cytoskeleton of primary astrocytes in culture contains actin, glial fibrillary acidic protein, and the fibroblast-type filament protein, vimentin. J Neurochem 1981;37:147-155
20. Farina C, Aloisi F, Meinl E. Astrocytes are active players in cerebral innate immunity. Trends Immunol 2007;28:138-145
21. Lieberman AP, Pitha PM, Shin HS, et al. Production of tumor necrosis factor and other cytokines by astrocytes stimulated with lipopolysaccharide or a neurotropic virus. Proc Natl Acad Sci U S A 1989;86:6348-6352
22. Murphy S, Simmons ML, Agullo L, et al. Synthesis of nitric oxide in CNS glial cells. Trends Neurosci 1993;16:323-328
23. Tsao N, Hsu HP, Lei HY. TNFalpha-induced cyclooxygenase 2 not only increases the vasopermeability of blood-brain barrier but also enhances the neutrophil survival in Escherichia coliYinduced brain inflammation. Prostaglandins Other Lipid Mediat 1999;57:371-382
24. Azuma I. Review: Inducer of cytokines in vivo: Overview of field and romurtide experience. Int J Immunopharmacol 1992;14:487-496
25. Dong Y, Benveniste EN. Immune function of astrocytes. Glia 2001;36: 180-190
26. Salazar-Mather TP, Hokeness KL. Calling in the troops: Regulation of inflammatory cell trafficking through innate cytokine/chemokine networks. Viral Immunol 2003;16:291-306
27. Kronfeld I, Zsukerman A, Kazimirsky G, et al. Staurosporine induces astrocytic phenotypes and differential expression of specific PKC isoforms in C6 glial cells. J Neurochem 1995;65:1505-1514
28. Mangoura D, Sakellaridis N, Jones J, et al. Early and late passage C-6 glial cell growth: Similarities with primary glial cells in culture. Neurochem Res 1989;14:941-947
29. Meier C, Oelschlaeger TA, Merkert H, et al. Ability of Escherichia coli isolates that cause meningitis in newborns to invade epithelial and endothelial cells. Infect Immun 1996;64:2391-2399
30. Prasadarao NV, Wass CA, Stins MF, et al. Outer membrane protein AYpromoted actin condensation of brain microvascular endothelial cells is required for Escherichia coli invasion. Infect Immun 1999;67:5775-5783
31. Greiffenberg L, Goebel W, Kim KS, et al. Interaction of Listeria monocytogenes with human brain microvascular endothelial cells: InlB-dependent invasion, long-term intracellular growth, and spread from macrophages to endothelial cells. Infect Immun 1998;66:5260-5267
32. Nizet V, Kim KS, Stins M, et al. Invasion of brain microvascular endo-thelial cells by group B streptococci. Infect Immun 1997;65:5074-5081
33. Slevogt H, Seybold J, Tiwari KN, et al. Moraxella catarrhalis is internalized in respiratory epithelial cells by a trigger-like mechanism and initiates a TLR2- and partly NOD1-dependent inflammatory immune response. Cell Microbiol 2007;9:694-707
34. Reddy MA, Wass CA, Kim KS, et al. Involvement of focal adhesion kinase in Escherichia coli invasion of human brain microvascular endothelial cells. Infect Immun 2000;68:6423-6430
35. Lindmo K, Stenmark H. Regulation of membrane traffic by phosphoi-nositide 3Ykinases. J Cell Sci 2006;119:605-614
36. Spring TG, Wold F. The purification and characterization of Escherichia coli enolase. J Biol Chem 1971;246:6797-6802
37. Torres AG, Kaper JB. Multiple elements controlling adherence of enter-ohemorrhagic Escherichia coli O157:H7 to HeLa cells. Infect Immun 2003;71:4985-4995
38. Torres AG, Li Y, Tutt CB, et al. Outer membrane protein A of Escherichia coli O157:H7 stimulates dendritic cell activation. Infect Immun 2006;74:2676-2685
39. Sukumaran SK, Shimada H, Prasadarao NV. Entry and intracellular replication of Escherichia coli K1 in macrophages require expression of outer membrane protein A. Infect Immun 2003;71:5951-5961
40. Teng CH, Xie Y, Shin S, et al. 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 2006;74:5609-5616
41. Henning U, Cole ST, Bremer E, et al. Gene fusions using the ompA gene coding for a major outer-membrane protein of Escherichia coli K12. Eur J Biochem 1983;136:233-240
42. Bremer E, Cole ST, Hindennach I, et al. Export of a protein into the outer membrane of Escherichia coli K12. Stable incorporation of the OmpA protein requires less than 193 amino-terminal amino-acid residues. Eur J Biochem 1982;122:223-231
43. Smith SG, Dorman CJ. Functional analysis of the FimE integrase of Escherichia coli K-12: Isolation of mutant derivatives with altered DNA inversion preferences. Mol Microbiol 1999;34:965-979
44. Reddy MA, Prasadarao NV, Wass CA, et al. Phosphatidylinositol 3Ykinase activation and interaction with focal adhesion kinase in Escherichia coli K1 invasion of human brain microvascular endothelial cells. J Biol Chem 2000;275:36769-36774
45. Ireton K, Payrastre B, Cossart P. The Listeria monocytogenes protein InlB is an agonist of mammalian phosphoinositide 3Ykinase. J Biol Chem 1999;274:17025-17032
46. Kerr MC, Teasdale RD. Defining macropinocytosis. Traffic 2009;10: 364-371
47. Sukumaran SK, Selvaraj SK, Prasadarao NV. Inhibition of apoptosis by Escherichia coli K1 is accompanied by increased expression of BclXL and blockade of mitochondrial cytochrome c release in macrophages. Infect Immun 2004;72:6012-6022
48. Kreutzberg GW. Microglia: A sensor for pathological events in the CNS. Trends Neurosci 1996;19:312-318
49. Fu H, Belaaouaj AA, Dahlgren C, et al. Outer membrane protein A deficient Escherichia coli activates neutrophils to produce superoxide and shows increased susceptibility to antibacterial peptides. Microbes Infect 2003;5:781-788
50. Eng LF, Ghirnikar RS, Lee YL. Glial fibrillary acidic protein: GFAP-thirty-one years (1969-2000). Neurochem Res 2000;25:1439-1451
51. Kim JM, Oh YK, Lee JH, et al. Induction of proinflammatory mediators requires activation of the TRAF, NIK, IKK and NF-kappaB signal transduction pathway in astrocytes infected with Escherichia coli. Clin Exp Immunol 2005;140:450-460
52. Galanakis E, Di Cello F, Paul-Satyaseela M, et al. Escherichia coli K1 induces IL-8 expression in human brain microvascular endothelial cells. Eur Cytokine Netw 2006;17:260-265
53. Selvaraj SK, Periandythevar P, Prasadarao NV. Outer membrane protein A of Escherichia coli K1 selectively enhances the expression of intercellular adhesion moleculeY1 in brain microvascular endothelial cells. Microbes Infect 2007;9:547-57