Natural killer cell-mediated host defense against uropathogenic E. coli is counteracted by bacterial hemolysinA-dependent killing of NK cells

Cell Host and Microbe

Volumn 14, Issue 6, 2013, Pages 664-674

  Gur, Chamutal ^a,c   Coppenhagen Glazer, Shunit ^b   Rosenberg, Shilo ^c   Yamin, Rachel ^a   Enk, Jonatan ^a   Glasner, Ariella ^a   Bar On, Yotam ^a   Fleissig, Omer ^a,b   Naor, Ronit ^b   Abed, Jawad ^b   Mevorach, Dror ^c   Granot, Zvi ^a   Bachrach, Gilad ^b   Mandelboim, Ofer ^a  

^a HEBREW UNIVERSITY   (Israel)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^c HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA HEMOLYSIN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ARTICLE; BACTERIAL LOAD; CELL ADHESION; CELL STRUCTURE; CONFOCAL MICROSCOPY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENZYME LINKED IMMUNOSORBENT ASSAY; ESCHERICHIA; FLOW CYTOMETRY; HEMOLYSIS; HOST RESISTANCE; HUMAN; IN VITRO STUDY; MOUSE; NATURAL KILLER CELL; NATURAL KILLER CELL MEDIATED CYTOTOXICITY; NONHUMAN; PRIORITY JOURNAL; URINARY TRACT INFECTION; UROPATHOGENIC ESCHERICHIA COLI;

ANIMALS; BACTERIAL LOAD; CELL SURVIVAL; CELLS, CULTURED; DNA TRANSPOSABLE ELEMENTS; ESCHERICHIA COLI PROTEINS; GENE KNOCKOUT TECHNIQUES; HEMOLYSIN PROTEINS; HOST-PATHOGEN INTERACTIONS; HUMANS; KILLER CELLS, NATURAL; MICE; MICE, INBRED C57BL; MUTAGENESIS, INSERTIONAL; TUMOR NECROSIS FACTOR-ALPHA; UROPATHOGENIC ESCHERICHIA COLI; VIRULENCE FACTORS;

EID: 84890305860     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2013.11.004     Document Type: Article

References (33)

1. O. Bahar, T. Goffer, and S. Burdman Type IV Pili are required for virulence, twitching motility, and biofilm formation of acidovorax avenae subsp. Citrulli Mol. Plant Microbe Interact. 22 2009 909 920
2. C. Balsalobre, J.M. Silván, S. Berglund, Y. Mizunoe, B.E. Uhlin, and S.N. Wai Release of the type I secreted alpha-haemolysin via outer membrane vesicles from Escherichia coli Mol. Microbiol. 59 2006 99 112
3. J. Bouckaert, J. Mackenzie, J.L. de Paz, B. Chipwaza, D. Choudhury, A. Zavialov, K. Mannerstedt, J. Anderson, D. Piérard, and L. Wyns The affinity of the FimH fimbrial adhesin is receptor-driven and quasi-independent of Escherichia coli pathotypes Mol. Microbiol. 61 2006 1556 1568
4. S.J. Cavalieri, G.A. Bohach, and I.S. Snyder Escherichia coli alpha-hemolysin: characteristics and probable role in pathogenicity Microbiol. Rev. 48 1984 326 343
5. S. Chaushu, A. Wilensky, C. Gur, L. Shapira, M. Elboim, G. Halftek, D. Polak, H. Achdout, G. Bachrach, and O. Mandelboim Direct recognition of Fusobacterium nucleatum by the NK cell natural cytotoxicity receptor NKp46 aggravates periodontal disease PLoS Pathog. 8 2012 e1002601
6. B.K. Dhakal, and M.A. Mulvey The UPEC pore-forming toxin α-hemolysin triggers proteolysis of host proteins to disrupt cell adhesion, inflammatory, and survival pathways Cell Host Microbe 11 2012 58 69
7. L. Emody, M. Kerényi, and G. Nagy Virulence factors of uropathogenic Escherichia coli Int. J. Antimicrob. Agents 22 Suppl 2 2003 29 33
8. D. Engel, U. Dobrindt, A. Tittel, P. Peters, J. Maurer, I. Gütgemann, B. Kaissling, W. Kuziel, S. Jung, and C. Kurts Tumor necrosis factor alpha- and inducible nitric oxide synthase-producing dendritic cells are rapidly recruited to the bladder in urinary tract infection but are dispensable for bacterial clearance Infect. Immun. 74 2006 6100 6107
9. O.V. Gadeberg, I. Orskov, and J.M. Rhodes Cytotoxic effect of an alpha-hemolytic Escherichia coli strain on human blood monocytes and granulocytes in vitro Infect. Immun. 41 1983 358 364
10. R. Gazit, R. Gruda, M. Elboim, T.I. Arnon, G. Katz, H. Achdout, J. Hanna, U. Qimron, G. Landau, and E. Greenbaum Lethal influenza infection in the absence of the natural killer cell receptor gene Ncr1 Nat. Immunol. 7 2006 517 523
11. G.G. Halfteck, M. Elboim, C. Gur, H. Achdout, H. Ghadially, and O. Mandelboim Enhanced in vivo growth of lymphoma tumors in the absence of the NK-activating receptor NKp46/NCR1 J. Immunol. 182 2009 2221 2230
12. T.J. Hannan, I.U. Mysorekar, S.L. Chen, J.N. Walker, J.M. Jones, J.S. Pinkner, S.J. Hultgren, and P.C. Seed LeuX tRNA-dependent and -independent mechanisms of Escherichia coli pathogenesis in acute cystitis Mol. Microbiol. 67 2008 116 128
13. M. Haraoka, L. Hang, B. Frendéus, G. Godaly, M. Burdick, R. Strieter, and C. Svanborg Neutrophil recruitment and resistance to urinary tract infection J. Infect. Dis. 180 1999 1220 1229
14. A. Jewett, X.H. Gan, L.T. Lebow, and B. Bonavida Differential secretion of TNF-alpha and IFN-gamma by human peripheral blood-derived NK subsets and association with functional maturation J. Clin. Immunol. 16 1996 46 54
15. J.R. Johnson Virulence factors in Escherichia coli urinary tract infection Clin. Microbiol. Rev. 4 1991 80 128
16. J. Jones-Carson, E. Balish, and D.T. Uehling Susceptibility of immunodeficient gene-knockout mice to urinary tract infection J. Urol. 161 1999 338 341
17. I. Jorgensen, and P.C. Seed How to make it in the urinary tract: a tutorial by Escherichia coli PLoS Pathog. 8 2012 e1002907
18. J.B. Kaper, J.P. Nataro, and H.L. Mobley Pathogenic Escherichia coli Nat. Rev. Microbiol. 2 2004 123 140
19. J. Koch, A. Steinle, C. Watzl, and O. Mandelboim Activating natural cytotoxicity receptors of natural killer cells in cancer and infection Trends Immunol. 34 2013 182 191
20. B. König, A. Ludwig, W. Goebel, and W. König Pore formation by the Escherichia coli alpha-hemolysin: role for mediator release from human inflammatory cells Infect. Immun. 62 1994 4611 4617
21. R. Kucheria, P. Dasgupta, S.H. Sacks, M.S. Khan, and N.S. Sheerin Urinary tract infections: new insights into a common problem Postgrad. Med. J. 81 2005 83 86
22. F.N. Lauw, D.R. Caffrey, and D.T. Golenbock Of mice and man: TLR11 (finally) finds profilin Trends Immunol. 26 2005 509 511
23. M.F. Mian, N.M. Lauzon, D.W. Andrews, B.D. Lichty, and A.A. Ashkar FimH can directly activate human and murine natural killer cells via TLR4 Mol. Ther. 18 2010 1379 1388
24. H.L. Mobley, K.G. Jarvis, J.P. Elwood, D.I. Whittle, C.V. Lockatell, R.G. Russell, D.E. Johnson, M.S. Donnenberg, and J.W. Warren Isogenic P-fimbrial deletion mutants of pyelonephritogenic Escherichia coli: the role of alpha Gal(1-4) beta Gal binding in virulence of a wild-type strain Mol. Microbiol. 10 1993 143 155
25. B. Ragnarsdóttir, N. Lutay, J. Grönberg-Hernandez, B. Köves, and C. Svanborg Genetics of innate immunity and UTI susceptibility Nat. Rev. Urol. 8 2011 449 468
26. E. Seidel, A. Glasner, and O. Mandelboim Virus-mediated inhibition of natural cytotoxicity receptor recognition Cell. Mol. Life Sci. 69 2012 3911 3920
27. K.E. Sivick, M.A. Schaller, S.N. Smith, and H.L. Mobley The innate immune response to uropathogenic Escherichia coli involves IL-17A in a murine model of urinary tract infection J. Immunol. 184 2010 2065 2075
28. A. Stapleton Novel mechanism of P-fimbriated Escherichia coli virulence in pyelonephritis J. Am. Soc. Nephrol. 16 2005 3458 3460
29. M. Totsika, B. Heras, D.J. Wurpel, and M.A. Schembri Characterization of two homologous disulfide bond systems involved in virulence factor biogenesis in uropathogenic Escherichia coli CFT073 J. Bacteriol. 191 2009 3901 3908
30. G.C. Ulett, M. Totsika, K. Schaale, A.J. Carey, M.J. Sweet, and M.A. Schembri Uropathogenic Escherichia coli virulence and innate immune responses during urinary tract infection Curr. Opin. Microbiol. 16 2013 100 107
31. J. Warawa, B.B. Finlay, and B. Kenny Type III secretion-dependent hemolytic activity of enteropathogenic Escherichia coli Infect. Immun. 67 1999 5538 5540
32. T.J. Wiles, R.R. Kulesus, and M.A. Mulvey Origins and virulence mechanisms of uropathogenic Escherichia coli Exp. Mol. Pathol. 85 2008 11 19
33. D. Zhang, G. Zhang, M.S. Hayden, M.B. Greenblatt, C. Bussey, R.A. Flavell, and S. Ghosh A toll-like receptor that prevents infection by uropathogenic bacteria Science 303 2004 1522 1526