Afa/Dr-expressing, diffusely adhering Escherichia coli strain C1845 triggers F1845 fimbria-dependent phosphatidylserine externalization on neutrophil-like differentiated PLB-985 cells through an apoptosis-independent mechanism

Infection and Immunity

Volumn 78, Issue 7, 2010, Pages 2974-2983

  Sémiramoth, Nicolas ^a   Gleizes, Aude ^a,b   Turbica, Isabelle ^a   Sandré, Catherine ^a   Marin Esteban, Viviana ^a   Gorges, Roseline ^a   Servin, Alain ^a   Chollet Martin, Sylvie ^a,c  

^a UNIVERSITÉ PARIS SACLAY   (France)

^b HÔPITAL ANTOINE BÉCLÈRE   (France)

^c BICHAT HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; FIMBRIA PROTEIN; GLYCOSYLPHOSPHATIDYLINOSITOL; NITRIC OXIDE SYNTHASE; PHOSPHATIDYLSERINE; PROTEIN AFA; PROTEIN DR; PROTEIN INTERACTING WITH PROTEIN KINASE C; PROTEIN KINASE C; PROTEIN TYROSINE KINASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CELL DIFFERENTIATION; CELL MATURATION; CYTOSKELETON; ENZYME ACTIVATION; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTION; HUMAN; LIPID RAFT; LYSOSOME; MITOCHONDRION; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ADHESINS, ESCHERICHIA COLI; APOPTOSIS; BACTERIAL ADHESION; BLOTTING, WESTERN; CELL LINE, TUMOR; ENTEROPATHOGENIC ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; ESCHERICHIA COLI PROTEINS; FIMBRIAE PROTEINS; FIMBRIAE, BACTERIAL; GRANULOCYTES; HUMANS; LYSOSOMES; MACROPHAGES; NEUTROPHILS; PHAGOCYTOSIS; TRANSCRIPTION FACTORS;

EID: 77953928734     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01354-09     Document Type: Article

References (65)

1. A-Gonzalez, N., S. J. Bensinger, C. Hong, S. Beceiro, M. N. Bradley, N. Zelcer, J. Deniz, C. Ramirez, M. Diaz, G. Gallardo, C. R. de Galarreta, J. Salazar, F. Lopez, P. Edwards, J. Parks, M. Andujar, P. Tontonoz, and A. Castrillo. 2009. Apoptotic cells promote their own clearance and immune tolerance through activation of the nuclear receptor LXR. Immunity 31:245-258.
2. Bassoe, C. F., N. Li, K. Ragheb, G. Lawler, J. Sturgis, and J. P. Robinson. 2003. Investigations of phagosomes, mitochondria, and acidic granules in human neutrophils using fluorescent probes. Cytometry B Clin. Cytom. 51: 21-29.
3. Berger, C. N., O. Billker, T. F. Meyer, A. L. Servin, and I. Kansau. 2004. Differential recognition of members of the carcinoembryonic antigen family by Afa/Dr adhesins of diffusely adhering Escherichia coli (Afa/Dr DAEC). Mol. Microbiol. 52:963-983.
4. Betis, F., P. Brest, V. Hofman, J. Guignot, M. F. Bernet-Camard, B. Rossi, A. Servin, and P. Hofman. 2003. The Afa/Dr adhesins of diffusely adhering Escherichia coli stimulate interleukin-8 secretion, activate mitogen-activated protein kinases, and promote polymorphonuclear transepithelial migration in T84 polarized epithelial cells. Infect. Immun. 71:1068-1074.
5. Betis, F., P. Brest, V. Hofman, J. Guignot, I. Kansau, B. Rossi, A. Servin, and P. Hofman. 2003. Afa/Dr diffusely adhering Escherichia coli infection in T84 cell monolayers induces increased neutrophil transepithelial migration, which in turn promotes cytokine-dependent upregulation of decay-accelerating factor (CD55), the receptor for Afa/Dr adhesins. Infect. Immun. 71: 1774-1783.
6. Bilge, S. S., C. R. Clausen, W. Lau, and S. L. Moseley. 1989. Molecular characterization of a fimbrial adhesin, F1845, mediating diffuse adherence of diarrhea-associated Escherichia coli to HEp-2 cells. J. Bacteriol. 171:4281-4289.
7. Blomgran, R., L. Zheng, and O. Stendahl. 2004. Uropathogenic Escherichia coli triggers oxygen-dependent apoptosis in human neutrophils through the cooperative effect of type 1 fimbriae and lipopolysaccharide. Infect. Immun. 72:4570-4578.
8. Brest, P., F. Betis, N. Cuburu, E. Selva, M. Herrant, A. Servin, P. Auberger, and P. Hofman. 2004. Increased rate of apoptosis and diminished phagocytic ability of human neutrophils infected with Afa/Dr diffusely adhering Escherichia coli strains. Infect. Immun. 72:5741-5749.
9. Cande, C., N. Vahsen, I. Kouranti, E. Schmitt, E. Daugas, C. Spahr, J. Luban, R. T. Kroemer, F. Giordanetto, C. Garrido, J. M. Penninger, and G. Kroemer. 2004. AIF and cyclophilin A cooperate in apoptosis-associated chromatinolysis. Oncogene 23:1514-1521.
10. D'Amours, D., S. Desnoyers, I. D'Silva, and G. G. Poirier. 1999. Poly(ADPribosyl) ation reactions in the regulation of nuclear functions. Biochem. J. 342:249-268. (Pubitemid 29425344)
11. Dias-Baruffi, M., H. Zhu, M. Cho, S. Karmakar, R. P. McEver, and R. D. Cummings. 2003. Dimeric galectin-1 induces surface exposure of phosphatidylserine and phagocytic recognition of leukocytes without inducing apoptosis. J. Biol. Chem. 278:41282-41293.
12. Dinauer, M. C., J. T. Curnutte, H. Rosen, and S. H. Orkin. 1989. A missense mutation in the neutrophil cytochrome b heavy chain in cytochrome-positive X-linked chronic granulomatous disease. J. Clin. Invest. 84:2012-2016.
13. Elliott, J. I., A. Surprenant, F. M. Marelli-Berg, J. C. Cooper, R. L. Cassady- Cain, C. Wooding, K. Linton, D. R. Alexander, and C. F. Higgins. 2005. Membrane phosphatidylserine distribution as a non-apoptotic signalling mechanism in lymphocytes. Nat. Cell Biol. 7:808-816.
14. Erwig, L. P., and P. M. Henson. 2008. Clearance of apoptotic cells by phagocytes. Cell Death Differ. 15:243-250.
15. Erwig, L. P., and P. M. Henson. 2007. Immunological consequences of apoptotic cell phagocytosis. Am. J. Pathol. 171:2-8.
16. Fadeel, B., A. Ahlin, J. I. Henter, S. Orrenius, and M. B. Hampton. 1998. Involvement of caspases in neutrophil apoptosis: regulation by reactive oxygen species. Blood 92:4808-4818. (Pubitemid 29005884)
17. Fadok, V. A., A. de Cathelineau, D. L. Daleke, P. M. Henson, and D. L. Bratton. 2001. Loss of phospholipid asymmetry and surface exposure of phosphatidylserine is required for phagocytosis of apoptotic cells by macrophages and fibroblasts. J. Biol. Chem. 276:1071-1077.
18. Fernandez-Boyanapalli, R. F., S. C. Frasch, K. McPhillips, R. W. Vandivier, B. L. Harry, D. W. Riches, P. M. Henson, and D. L. Bratton. 2009. Impaired apoptotic cell clearance in CGD due to altered macrophage programming is reversed by phosphatidylserine-dependent production of IL-4. Blood 113: 2047-2055.
19. Fernandez-Prada, C., B. D. Tall, S. E. Elliott, D. L. Hoover, J. P. Nataro, and M. M. Venkatesan. 1998. Hemolysin-positive enteroaggregative and celldetaching Escherichia coli strains cause oncosis of human monocyte-derived macrophages and apoptosis of murine J774 cells. Infect. Immun. 66:3918-3924.
20. Francois, S., J. El Benna, P. M. Dang, E. Pedruzzi, M. A. Gougerot-Pocidalo, and C. Elbim. 2005. Inhibition of neutrophil apoptosis by TLR agonists in whole blood: involvement of the phosphoinositide 3-kinase/Akt and NF-kappaB signaling pathways, leading to increased levels of Mcl-1, A1, and phosphorylated Bad. J. Immunol. 174:3633-3642.
21. Frasch, S. C., P. M. Henson, K. Nagaosa, M. B. Fessler, N. Borregaard, and D. L. Bratton. 2004. Phospholipid flip-flop and phospholipid scramblase 1 (PLSCR1) co-localize to uropod rafts in formylated Met-Leu-Phe-stimulated neutrophils. J. Biol. Chem. 279:17625-17633.
22. Galluzzi, L., M. C. Maiuri, I. Vitale, H. Zischka, M. Castedo, L. Zitvogel, and G. Kroemer. 2007. Cell death modalities: classification and pathophysiological implications. Cell Death Differ. 14:1237-1243. (Pubitemid 46969863)
23. Glasser, A. L., J. Boudeau, N. Barnich, M. H. Perruchot, J. F. Colombel, and A. Darfeuille-Michaud. 2001. Adherent invasive Escherichia coli strains from patients with Crohn's disease survive and replicate within macrophages without inducing host cell death. Infect. Immun. 69:5529-5537.
24. Goluszko, P., S. L. Moseley, L. D. Truong, A. Kaul, J. R. Williford, R. Selvarangan, S. Nowicki, and B. Nowicki. 1997. Development of experimental model of chronic pyelonephritis with Escherichia coli O75:K5:H-bearing Dr fimbriae: mutation in the dra region prevented tubulointerstitial nephritis. J. Clin. Invest. 99:1662-1672.
25. Green, D. R., and G. Kroemer. 2004. The pathophysiology of mitochondrial cell death. Science 305:626-629.
26. Grenier, A., S. Chollet-Martin, B. Crestani, C. Delarche, J. El Benna, A. Boutten, V. Andrieu, G. Durand, M. A. Gougerot-Pocidalo, M. Aubier, and M. Dehoux. 2002. Presence of a mobilizable intracellular pool of hepatocyte growth factor in human polymorphonuclear neutrophils. Blood 99:2997-3004.
27. Guicciardi, M. E., M. Leist, and G. J. Gores. 2004. Lysosomes in cell death. Oncogene 23:2881-2890.
28. Guignot, J., S. Hudault, I. Kansau, I. Chau, and A. L. Servin. 2009. Human decay-accelerating factor and CEACAM receptor-mediated internalization and intracellular lifestyle of Afa/Dr diffusely adhering Escherichia coli in epithelial cells. Infect. Immun. 77:517-531.
29. Guignot, J., I. Peiffer, M. F. Bernet-Camard, D. M. Lublin, C. Carnoy, S. L. Moseley, and A. L. Servin. 2000. Recruitment of CD55 and CD66e brush border-associated glycosylphosphatidylinositol-anchored proteins by members of the Afa/Dr diffusely adhering family of Escherichia coli that infect the human polarized intestinal Caco-2/TC7 cells. Infect. Immun. 68:3554-3563.
30. Hiraoka, W., N. Vazquez, W. Nieves-Neira, S. J. Chanock, and Y. Pommier. 1998. Role of oxygen radicals generated by NADPH oxidase in apoptosis induced in human leukemia cells. J. Clin. Invest. 102:1961-1968.
31. Hirt, U. A., and M. Leist. 2003. Rapid, noninflammatory and PS-dependent phagocytic clearance of necrotic cells. Cell Death Differ. 10:1156-1164.
32. Hornef, M. W., M. J. Wick, M. Rhen, and S. Normark. 2002. Bacterial strategies for overcoming host innate and adaptive immune responses. Nat. Immunol. 3:1033-1040.
33. Jeannin, P., S. Jaillon, and Y. Delneste. 2008. Pattern recognition receptors in the immune response against dying cells. Curr. Opin. Immunol. 20:530-537.
34. Jitkaew, S., E. Witasp, S. Zhang, V. E. Kagan, and B. Fadeel. 2009. Induction of caspase- and reactive oxygen species-independent phosphatidylserine externalization in primary human neutrophils: role in macrophage recognition and engulfment. J. Leukoc. Biol. 85:427-437.
35. Kaper, J. B., J. P. Nataro, and H. L. Mobley. 2004. Pathogenic Escherichia coli. Nat. Rev. Microbiol. 2:123-140.
36. Kennedy, A. D., and F. R. DeLeo. 2009. Neutrophil apoptosis and the resolution of infection. Immunol. Res. 43:25-61.
37. Kobayashi, S. D., J. M. Voyich, K. R. Braughton, and F. R. DeLeo. 2003. Down-regulation of proinflammatory capacity during apoptosis in human polymorphonuclear leukocytes. J. Immunol. 170:3357-3368. (Pubitemid 36302215)
38. Kroemer, G., L. Galluzzi, and C. Brenner. 2007. Mitochondrial membrane permeabilization in cell death. Physiol. Rev. 87:99-163.
39. + T regulatory cells inhibit neutrophil function and promote their apoptosis and death. J. Immunol. 177:7155-7163.
40. Li, X. J., F. Fieschi, M. H. Paclet, D. Grunwald, Y. Campion, P. Gaudin, F. Morel, and M. J. Stasia. 2007. Leu505 of Nox2 is crucial for optimal p67phox-dependent activation of the flavocytochrome b558 during phagocytic NADPH oxidase assembly. J. Leukoc. Biol. 81:238-249.
41. Liu, J., T. Akahoshi, T. Sasahana, H. Kitasato, R. Namai, T. Sasaki, M. Inoue, and H. Kondo. 1999. Inhibition of neutrophil apoptosis by verotoxin 2 derived from Escherichia coli O157:H7. Infect. Immun. 67:6203-6205.
42. Lockshin, R. A., and Z. Zakeri. 2004. Caspase-independent cell death? Oncogene 23:2766-2773.
43. Luo, H. R., and F. Loison. 2008. Constitutive neutrophil apoptosis: mechanisms and regulation. Am. J. Hematol. 83:288-295.
44. Maianski, N. A., A. N. Maianski, T. W. Kuijpers, and D. Roos. 2004. Apoptosis of neutrophils. Acta Haematol. 111:56-66.
45. Martin, S. J., C. P. Reutelingsperger, A. J. McGahon, J. A. Rader, R. C. van Schie, D. M. LaFace, and D. R. Green. 1995. Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl. J. Exp. Med. 182:1545-1556.
46. Miyanishi, M., K. Tada, M. Koike, Y. Uchiyama, T. Kitamura, and S. Nagata. 2007. Identification of Tim4 as a phosphatidylserine receptor. Nature 450:435-439.
47. Modjtahedi, N., F. Giordanetto, F. Madeo, and G. Kroemer. 2006. Apoptosis- inducing factor: vital and lethal. Trends Cell Biol. 16:264-272.
48. Nowicki, B., A. Hart, K. E. Coyne, D. M. Lublin, and S. Nowicki. 1993. Short consensus repeat-3 domain of recombinant decay-accelerating factor is recognized by Escherichia coli recombinant Dr adhesin in a model of a cell-cell interaction. J. Exp. Med. 178:2115-2121.
49. Park, S. Y., M. Y. Jung, H. J. Kim, S. J. Lee, S. Y. Kim, B. H. Lee, T. H. Kwon, R. W. Park, and I. S. Kim. 2008. Rapid cell corpse clearance by stabilin-2, a membrane phosphatidylserine receptor. Cell Death Differ. 15: 192-201.
50. Peiffer, I., J. Guignot, A. Barbat, C. Carnoy, S. L. Moseley, B. J. Nowicki, A. L. Servin, and M. F. Bernet-Camard. 2000. Structural and functional lesions in brush border of human polarized intestinal Caco-2/TC7 cells infected by members of the Afa/Dr diffusely adhering family of Escherichia coli. Infect. Immun. 68:5979-5990.
51. Ravichandran, K. S., and U. Lorenz. 2007. Engulfment of apoptotic cells: signals for a good meal. Nat. Rev. Immunol. 7:964-974.
52. Semiramoth, N., A. Gleizes, I. Turbica, C. Sandre, R. Gorges, I. Kansau, A. Servin, and S. Chollet-Martin. 2009. Escherichia coli type 1 pili trigger late IL-8 production by neutrophil-like differentiated PLB-985 cells through a Src family kinase- and MAPK-dependent mechanism. J. Leukoc. Biol. 85:310-321.
53. Servin, A. L. 2005. Pathogenesis of Afa/Dr diffusely adhering Escherichia coli. Clin. Microbiol. Rev. 18:264-292.
54. Smrz, D., L. Draberova, and P. Draber. 2007. Non-apoptotic phosphatidylserine externalization induced by engagement of glycosylphosphatidylinositol- anchored proteins. J. Biol. Chem. 282:10487-10497.
55. Smrz, D., P. Lebduska, L. Draberova, J. Korb, and P. Draber. 2008. Engagement of phospholipid scramblase 1 in activated cells: implication for phosphatidylserine externalization and exocytosis. J. Biol. Chem. 283:10904-10918.
56. Soehnlein, O., L. Lindbom, and C. Weber. 2009. Mechanisms underlying neutrophil-mediated monocyte recruitment. Blood 114:4613-4623.
57. Stowell, S. R., C. M. Arthur, K. A. Slanina, J. R. Horton, D. F. Smith, and R. D. Cummings. 2008. Dimeric galectin-8 induces phosphatidylserine exposure in leukocytes through polylactosamine recognition by the C-terminal domain. J. Biol. Chem. 283:20547-20559.
58. Stowell, S. R., Y. Qian, S. Karmakar, N. S. Koyama, M. Dias-Baruffi, H. Leffler, R. P. McEver, and R. D. Cummings. 2008. Differential roles of galectin-1 and galectin-3 in regulating leukocyte viability and cytokine secretion. J. Immunol. 180:3091-3102.
59. Tucker, K. A., M. B. Lilly, L. Heck, Jr., and T. A. Rado. 1987. Characterization of a new human diploid myeloid leukemia cell line (PLB-985) with granulocytic and monocytic differentiating capacity. Blood 70:372-378.
60. Urban, C. F., S. Lourido, and A. Zychlinsky. 2006. How do microbes evade neutrophil killing? Cell. Microbiol. 8:1687-1696.
61. Verchier, Y., B. Lardy, M. V. Nguyen, F. Morel, S. Arbault, and C. Amatore. 2007. Concerted activities of nitric oxide synthases and NADPH oxidases in PLB-985 cells. Biochem. Biophys. Res. Commun. 361:493-498.
62. Watson, R. W., H. P. Redmond, J. H. Wang, C. Condron, and D. Bouchier- Hayes. 1996. Neutrophils undergo apoptosis following ingestion of Escherichia coli. J. Immunol. 156:3986-3992.
63. Weinrauch, Y., and A. Zychlinsky. 1999. The induction of apoptosis by bacterial pathogens. Annu. Rev. Microbiol. 53:155-187.
64. Zhao, M., J. W. Eaton, and U. T. Brunk. 2000. Protection against oxidantmediated lysosomal rupture: a new anti-apoptotic activity of Bcl-2? FEBS Lett. 485:104-108.
65. Zhen, L., A. A. King, Y. Xiao, S. J. Chanock, S. H. Orkin, and M. C. Dinauer. 1993. Gene targeting of X chromosome-linked chronic granulomatous disease locus in a human myeloid leukemia cell line and rescue by expression of recombinant gp91phox. Proc. Natl. Acad. Sci. U. S. A. 90:9832-9836.