Attenuation of human neutrophil migration and function by uropathogenic bacteria

Microbes and Infection

Volumn 13, Issue 6, 2011, Pages 555-565

  Loughman, Jennifer A ^a   Hunstad, David A ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Escherichia coli; Migration; Neutrophil

Indexed keywords

REACTIVE OXYGEN METABOLITE;

ARTICLE; BACTERIAL INFECTION; BACTERIAL VIRULENCE; BACTERICIDAL ACTIVITY; CELL ADHESION; CONTROLLED STUDY; CYSTITIS; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; LEUKOCYTE FUNCTION; LEUKOCYTE MIGRATION; NEUTROPHIL CHEMOTAXIS; PHAGOCYTOSIS; PHENOTYPE; POLYMORPHONUCLEAR CELL; PRIORITY JOURNAL; URINARY TRACT INFECTION; UROPATHOGENIC ESCHERICHIA COLI;

ADULT; ANIMALS; CELL MIGRATION ASSAYS, LEUKOCYTE; CELL MOVEMENT; DISEASE MODELS, ANIMAL; GENE EXPRESSION PROFILING; HUMANS; IMMUNE EVASION; MICE; MICROBIAL VIABILITY; NEUTROPHILS; PHAGOCYTOSIS; REACTIVE OXYGEN SPECIES; UROPATHOGENIC ESCHERICHIA COLI;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; MURINAE;

EID: 79955650633     PISSN: 12864579     EISSN: 1769714X     Source Type: Journal    
DOI: 10.1016/j.micinf.2011.01.017     Document Type: Article

References (49)

1. Segal A.W. How neutrophils kill microbes. Annu. Rev. Immunol. 2005, 23:197-223.
2. Nathan C. Neutrophils and immunity: challenges and opportunities. Nat. Rev. Immunol. 2006, 6:173-182.
3. Springer T.A. Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell 1994, 76:301-314.
4. Stamm W.E., Norrby S.R. Urinary tract infections: disease panorama and challenges. J. Infect. Dis. 2001, 183(Suppl. 1):S1-S4.
5. Foxman B. Epidemiology of urinary tract infections: incidence, morbidity, and economic costs. Dis. Mon. 2003, 49:53-70.
6. Foxman B., Brown P. Epidemiology of urinary tract infections: transmission and risk factors, incidence, and costs. Infect. Dis. Clin. North Am. 2003, 17:227-241.
7. Martinez J.J., Mulvey M.A., Schilling J.D., Pinkner J.S., Hultgren S.J. Type 1 pilus-mediated bacterial invasion of bladder epithelial cells. EMBO J. 2000, 19:2803-2812.
8. Min G., Stolz M., Zhou G., Liang F., Sebbel P., Stoffler D., Glockshuber R., Sun T.T., Aebi U., Kong X.P. Localization of uroplakin Ia, the urothelial receptor for bacterial adhesin FimH, on the six inner domains of the 16 nm urothelial plaque particle. J. Mol. Biol. 2002, 317:697-706.
9. Mulvey M.A., Lopez-Boado Y.S., Wilson C.L., Roth R., Parks W.C., Heuser J., Hultgren S.J. Induction and evasion of host defenses by type 1-piliated uropathogenic Escherichia coli. Science 1998, 282:1494-1497.
10. Anderson G.G., Palermo J.J., Schilling J.D., Roth R., Heuser J., Hultgren S.J. Intracellular bacterial biofilm-like pods in urinary tract infections. Science 2003, 301:105-107.
11. Justice S.S., Hung C., Theriot J.A., Fletcher D.A., Anderson G.G., Footer M.J., Hultgren S.J. Differentiation and developmental pathways of uropathogenic Escherichia coli in urinary tract pathogenesis. Proc. Natl. Acad. Sci. U S A 2004, 101:1333-1338.
12. Mysorekar I.U., Hultgren S.J. Mechanisms of uropathogenic Escherichia coli persistence and eradication from the urinary tract. Proc. Natl. Acad. Sci. U S A 2006, 103:14170-14175.
13. Schilling J.D., Martin S.M., Hunstad D.A., Patel K.P., Mulvey M.A., Justice S.S., Lorenz R.G., Hultgren S.J. CD14- and Toll-like receptor-dependent activation of bladder epithelial cells by lipopolysaccharide and type 1 piliated Escherichia coli. Infect. Immun. 2003, 71:1470-1480.
14. Hunstad D.A., Justice S.S., Hung C.S., Lauer S.R., Hultgren S.J. Suppression of bladder epithelial cytokine responses by uropathogenic Escherichia coli. Infect. Immun. 2005, 73:3999-4006.
15. Billips B.K., Forrestal S.G., Rycyk M.T., Johnson J.R., Klumpp D.J., Schaeffer A.J. Modulation of host innate immune response in the bladder by uropathogenic Escherichia coli. Infect. Immun. 2007, 75:5353-5360.
16. Klumpp D.J., Weiser A.C., Sengupta S., Forrestal S.G., Batler R.A., Schaeffer A.J. Uropathogenic Escherichia coli potentiates type 1 pilus-induced apoptosis by suppressing NF-kappa B. Infect. Immun. 2001, 69:6689-6695.
17. Justice S.S., Hunstad D.A., Seed P.C., Hultgren S.J. Filamentation by Escherichia coli subverts innate defenses during urinary tract infection. Proc. Natl. Acad. Sci. U S A 2006, 103:19884-19889.
18. Agace W.W. The role of the epithelial cell in Escherichia coli induced neutrophil migration into the urinary tract. Eur. Respir. J. 1996, 9:1713-1728.
19. Agace W.W., Patarroyo M., Svensson M., Carlemalm E., Svanborg C. Escherichia coli induces transuroepithelial neutrophil migration by an intercellular adhesion molecule-1-dependent mechanism. Infect. Immun. 1995, 63:4054-4062.
20. Parkos C.A., Delp C., Arnaout M.A., Madara J.L. Neutrophil migration across a cultured intestinal epithelium. Dependence on a CD11b/CD18-mediated event and enhanced efficiency in physiological direction. J. Clin. Invest. 1991, 88:1605-1612.
21. Hultgren S.J., Schwan W.R., Schaeffer A.J., Duncan J.L. Regulation of production of type 1 pili among urinary tract isolates of Escherichia coli. Infect. Immun. 1986, 54:613-620.
22. Mobley H.L., Green D.M., Trifillis A.L., Johnson D.E., Chippendale G.R., Lockatell C.V., Jones B.D., Warren J.W. Pyelonephritogenic Escherichia coli and killing of cultured human renal proximal tubular epithelial cells: role of hemolysin in some strains. Infect. Immun. 1990, 58:1281-1289.
23. Blattner F.R., Plunkett G., Bloch C.A., Perna N.T., Burland V., Riley M., Collado-Vides J., Glasner J.D., Rode C.K., Mayhew G.F., Gregor J., Davis N.W., Kirkpatrick H.A., Goeden M.A., Rose D.J., Mau B., Shao Y. The complete genome sequence of Escherichia coli K-12. Science 1997, 277:1453-1474.
24. Guyer M.S., Reed R.R., Steitz J.A., Low K.B. Identification of a sex-factor-affinity site in E. coli as gamma delta. Cold Spring Harb Symp. Quant Biol. 1981, 45(1):135-140.
25. Wright K.J., Seed P.C., Hultgren S.J. Development of intracellular bacterial communities of uropathogenic Escherichia coli depends on type 1 pili. Cell. Microbiol. 2007, 9:2230-2241.
26. Di Cello F., Xie Y., Paul-Satyaseela M., Kim K.S. Approaches to bacterial RNA isolation and purification for microarray analysis of Escherichia coli K1 interaction with human brain microvascular endothelial cells. J. Clin. Microbiol. 2005, 43:4197-4199.
27. Li C., Hung Wong W. Model-based analysis of oligonucleotide arrays: model validation, design issues and standard error application. Genome Biol. 2001, 2. RESEARCH0032.
28. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2-Δ Δ C T method. Methods 2001, 25:402-408.
29. Lipschutz J.H., O'Brien L.E., Altschuler Y., Avrahami D., Nguyen Y., Tang K., Mostov K.E. Analysis of membrane traffic in polarized epithelial cells. Curr. Protoc. Cell Biol. 2001, Chapter 15Unit 15 15.
30. Blomgran R., Zheng L., Stendahl O. Uropathogenic Escherichia coli triggers oxygen-dependent apoptosis in human neutrophils through the cooperative effect of type 1 fimbriae and lipopolysaccharide. Infect. Immun. 2004, 72:4570-4578.
31. Hampton M.B., Kettle A.J., Winterbourn C.C. Inside the neutrophil phagosome: oxidants, myeloperoxidase, and bacterial killing. Blood 1998, 92:3007-3017.
32. Godaly G., Proudfoot A.E., Offord R.E., Svanborg C., Agace W.W. Role of epithelial interleukin-8 (IL-8) and neutrophil IL-8 receptor A in Escherichia coli-induced transuroepithelial neutrophil migration. Infect. Immun. 1997, 65:3451-3456.
33. Martinez J.J., Hultgren S.J. Requirement of Rho-family GTPases in the invasion of Type 1-piliated uropathogenic Escherichia coli. Cell. Microbiol. 2002, 4:19-28.
34. Duncan M.J., Li G., Shin J.S., Carson J.L., Abraham S.N. Bacterial penetration of bladder epithelium through lipid rafts. J. Biol. Chem. 2004, 279:18944-18951.
35. Smith Y.C., Grande K.K., Rasmussen S.B., O'Brien A.D. Novel three-dimensional organoid model for evaluation of the interaction of uropathogenic Escherichia coli with terminally differentiated human urothelial cells. Infect. Immun. 2006, 74:750-757.
36. Bar-Shavit Z., Goldman R., Ofek I., Sharon N., Mirelman D. Mannose-binding activity of Escherichia coli: a determinant of attachment and ingestion of the bacteria by macrophages. Infect. Immun. 1980, 29:417-424.
37. Goetz M.B., Silverblatt F.J. Stimulation of human polymorphonuclear leukocyte oxidative metabolism by type 1 pili from Escherichia coli. Infect. Immun. 1987, 55:534-540.
38. Ohman L., Hed J., Stendahl O. Interaction between human polymorphonuclear leukocytes and two different strains of type 1 fimbriae-bearing Escherichia coli. J. Infect. Dis. 1982, 146:751-757.
39. Bergsten G., Wullt B., Schembri M.A., Leijonhufvud I., Svanborg C. Do type 1 fimbriae promote inflammation in the human urinary tract?. Cell Microbiol. 2007, 9:1766-1781.
40. Billips B.K., Schaeffer A.J., Klumpp D.J. Molecular basis of uropathogenic Escherichia coli evasion of the innate immune response in the bladder. Infect. Immun. 2008, 76:3891-3900.
41. Caprioli A., Falbo V., Roda L.G., Ruggeri F.M., Zona C. Partial purification and characterization of an Escherichia coli toxic factor that induces morphological cell alterations. Infect. Immun. 1983, 39:1300-1306.
42. Davis J.M., Rasmussen S.B., O'Brien A.D. Cytotoxic necrotizing factor type 1 production by uropathogenic Escherichia coli modulates polymorphonuclear leukocyte function. Infect. Immun. 2005, 73:5301-5310.
43. Hofman P., Le Negrate G., Mograbi B., Hofman V., Brest P., Alliana-Schmid A., Flatau G., Boquet P., Rossi B. Escherichia coli cytotoxic necrotizing factor-1 (CNF-1) increases the adherence to epithelia and the oxidative burst of human polymorphonuclear leukocytes but decreases bacteria phagocytosis. J. Leukoc. Biol. 2000, 68:522-528.
44. Cirl C., Wieser A., Yadav M., Duerr S., Schubert S., Fischer H., Stappert D., Wantia N., Rodriguez N., Wagner H., Svanborg C., Miethke T. Subversion of Toll-like receptor signaling by a unique family of bacterial Toll/interleukin-1 receptor domain-containing proteins. Nat. Med. 2008, 14:399-406.
45. Chen S.L., Hung C.S., Xu J., Reigstad C.S., Magrini V., Sabo A., Blasiar D., Bieri T., Meyer R.R., Ozersky P., Armstrong J.R., Fulton R.S., Latreille J.P., Spieth J., Hooton T.M., Mardis E.R., Hultgren S.J., Gordon J.I. Identification of genes subject to positive selection in uropathogenic strains of Escherichia coli: a comparative genomics approach. Proc. Natl. Acad. Sci. U S A 2006, 103:5977-5982.
46. Vazquez-Torres A., Xu Y., Jones-Carson J., Holden D.W., Lucia S.M., Dinauer M.C., Mastroeni P., Fang F.C. Salmonella pathogenicity island 2-dependent evasion of the phagocyte NADPH oxidase. Science 2000, 287:1655-1658.
47. Allen L.A., Beecher B.R., Lynch J.T., Rohner O.V., Wittine L.M. Helicobacter pylori disrupts NADPH oxidase targeting in human neutrophils to induce extracellular superoxide release. J. Immunol. 2005, 174:3658-3667.
48. Criss A.K., Katz B.Z., Seifert H.S. Resistance of Neisseria gonorrhoeae to non-oxidative killing by adherent human polymorphonuclear leucocytes. Cell. Microbiol. 2009, 11:1074-1087.
49. Criss A.K., Seifert H.S. Neisseria gonorrhoeae suppresses the oxidative burst of human polymorphonuclear leukocytes. Cell. Microbiol. 2008, 10:2257-2270.