The essential role of neutrophils during infection with the intracellular bacterial pathogen listeria monocytogenes

Journal of Immunology

Volumn 197, Issue 5, 2016, Pages 1557-1565

  Witter, Alexandra R ^a   Okunnu, Busola M ^a   Berg, Rance E ^a  

^a UNIVERSITY OF NORTH TEXAS HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CXCR2; CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; EXTRACELLULAR SUPEROXIDE DISMUTASE; INTERLEUKIN 12; INTERLEUKIN 15; INTERLEUKIN 17; INTERLEUKIN 22; INTERLEUKIN 6; MYELOID DIFFERENTIATION FACTOR 88; NEUTROPHIL COLLAGENASE; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR; CYTOKINE;

BACTERIAL CLEARANCE; BACTERIAL VIRULENCE; BONE MARROW; CD8+ T LYMPHOCYTE; CELL FUNCTION; CELL MIGRATION; CELLULAR DISTRIBUTION; CELLULAR IMMUNITY; CELLULAR, SUBCELLULAR AND MOLECULAR BIOLOGICAL PHENOMENA AND FUNCTIONS; CYTOKINE PRODUCTION; DISEASE ASSOCIATION; EXTRACELLULAR TRAP; HOST RESISTANCE; HUMAN; IMMUNOREGULATION; INCUBATION TIME; INNATE IMMUNITY; LEUKOCYTE ACTIVATION; LISTERIA MONOCYTOGENES; LISTERIOSIS; MOLECULAR DYNAMICS; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NEUTROPHIL EXTRAVASATION; NEUTROPHIL RELEASE; NONHUMAN; PHAGOCYTOSIS; PRIMARY INFECTION; PRIORITY JOURNAL; REVIEW; SECONDARY INFECTION; ANIMAL; BIOSYNTHESIS; CYTOPLASM; IMMUNOLOGY; MICROBIOLOGY; MIXED INFECTION; MOUSE; PATHOGENICITY; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; BONE MARROW; COINFECTION; CYTOKINES; CYTOPLASM; HUMANS; LISTERIA MONOCYTOGENES; LISTERIOSIS; MICE; NEUTROPHILS; PHAGOCYTOSIS; SIGNAL TRANSDUCTION;

EID: 84983797290     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1600599     Document Type: Review

References (112)

1. Manz, M. G., and S. Boettcher. 2014. Emergency granulopoiesis. Nat. Rev. Immunol. 14: 302-314.
2. Kwak, H. J., P. Liu, B. Bajrami, Y. Xu, S. Y. Park, C. Nombela-Arrieta, S. Mondal, Y. Sun, H. Zhu, L. Chai, et al. 2015. Myeloid cell-derived reactive oxygen species externally regulate the proliferation of myeloid progenitors in emergency granulopoiesis. Immunity 42: 159-171.
3. Stark, M. A., Y. Huo, T. L. Burcin, M. A. Morris, T. S. Olson, and K. Ley. 2005. Phagocytosis of apoptotic neutrophils regulates granulopoiesis via IL-23 and IL-17. Immunity 22: 285-294.
4. Strydom, N., and S. M. Rankin. 2013. Regulation of circulating neutrophil numbers under homeostasis and in disease. J. Innate Immun. 5: 304-314.
5. Casanova-Acebes, M., C. Pitaval, L. A. Weiss, C. Nombela-Arrieta, R. Chèvre, N. A-González, Y. Kunisaki, D. Zhang, N. van Rooijen, L. E. Silberstein, et al. 2013. Rhythmic modulation of the hematopoietic niche through neutrophil clearance. Cell 153: 1025-1035.
6. Nauseef, W. M., and N. Borregaard. 2014. Neutrophils at work. Nat. Immunol. 15: 602-611.
7. Mócsai, A. 2013. Diverse novel functions of neutrophils in immunity, inflammation, and beyond. J. Exp. Med. 210: 1283-1299.
8. Mayadas, T. N., X. Cullere, and C. A. Lowell. 2014. The multifaceted functions of neutrophils. Annu. Rev. Pathol. 9: 181-218.
9. Scallan, E., R. M. Hoekstra, F. J. Angulo, R. V. Tauxe, M. A. Widdowson, S. L. Roy, J. L. Jones, and P. M. Griffin. 2011. Foodborne illness acquired in the United States-major pathogens. Emerg. Infect. Dis. 17: 7-15.
10. Hardy, J., P. Chu, and C. H. Contag. 2009. Foci of Listeria monocytogenes persist in the bone marrow. Dis. Model. Mech. 2: 39-46.
11. Join-Lambert, O. F., S. Ezine, A. Le Monnier, F. Jaubert, M. Okabe, P. Berche, and S. Kayal. 2005. Listeria monocytogenes-infected bone marrow myeloid cells promote bacterial invasion of the central nervous system. Cell. Microbiol. 7: 167-180.
12. Alonzo, F., III, L. D. Bobo, D. J. Skiest, and N. E. Freitag. 2011. Evidence for subpopulations of Listeria monocytogenes with enhanced invasion of cardiac cells. J. Med. Microbiol. 60: 423-434.
13. Pamer, E. G. 2004. Immune responses to Listeria monocytogenes. Nat. Rev. Immunol. 4: 812-823.
14. Cossart, P., and M. Lecuit. 1998. Interactions of Listeria monocytogenes with mammalian cells during entry and actin-based movement: bacterial factors, cellular ligands and signaling. EMBO J. 17: 3797-3806.
15. Czuprynski, C. J., J. F. Brown, N. Maroushek, R. D. Wagner, and H. Steinberg. 1994. Administration of anti-granulocyte mAb RB6-8C5 impairs the resistance of mice to Listeria monocytogenes infection. J. Immunol. 152: 1836-1846.
16. Conlan, J. W., and R. J. North. 1994. Neutrophils are essential for early anti-Listeria defense in the liver, but not in the spleen or peritoneal cavity, as revealed by a granulocyte-depleting monoclonal antibody. J. Exp. Med. 179: 259-268.
17. Conlan, J. W. 1997. Critical roles of neutrophils in host defense against experimental systemic infections of mice by Listeria monocytogenes, Salmonella typhimurium, and Yersinia enterocolitica. Infect. Immun. 65: 630-635.
18. Rakhmilevich, A. L. 1995. Neutrophils are essential for resolution of primary and secondary infection with Listeria monocytogenes. J. Leukoc. Biol. 57: 827-831.
19. Rogers, H. W., and E. R. Unanue. 1993. Neutrophils are involved in acute, nonspecific resistance to Listeria monocytogenes in mice. Infect. Immun. 61: 5090-5096.
20. Gregory, S. H., A. J. Sagnimeni, and E. J.Wing. 1996. Bacteria in the bloodstream are trapped in the liver and killed by immigrating neutrophils. J. Immunol. 157: 2514-2520.
21. Fleming, T. J., M. L. Fleming, and T. R. Malek. 1993. Selective expression of Ly-6G on myeloid lineage cells in mouse bone marrow. RB6-8C5 mAb to granulocyte-differentiation antigen (Gr-1) detects members of the Ly-6 family. J. Immunol. 151: 2399-2408.
22. Daley, J. M., A. A. Thomay, M. D. Connolly, J. S. Reichner, and J. E. Albina. 2008. Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice. J. Leukoc. Biol. 83: 64-70.
23. Edelson, B. T., T. R. Bradstreet, K. Hildner, J. A. Carrero, K. E. Frederick, W. Kc, R. Belizaire, T. Aoshi, R. D. Schreiber, M. J. Miller, et al. 2011. CD8a(+) dendritic cells are an obligate cellular entry point for productive infection by Listeria monocytogenes. Immunity 35: 236-248.
24. Carr, K. D., A. N. Sieve, M. Indramohan, T. J. Break, S. Lee, and R. E. Berg. 2011. Specific depletion reveals a novel role for neutrophil-mediated protection in the liver during Listeria monocytogenes infection. Eur. J. Immunol. 41: 2666-2676.
25. Shi, C., T. M. Hohl, I. Leiner, M. J. Equinda, X. Fan, and E. G. Pamer. 2011. Ly6G+ neutrophils are dispensable for defense against systemic Listeria monocytogenes infection. J. Immunol. 187: 5293-5298.
26. Lieschke, G. J., D. Grail, G. Hodgson, D.Metcalf, E. Stanley, C. Cheers, K. J. Fowler, S. Basu, Y. F. Zhan, and A. R. Dunn. 1994. Mice lacking granulocyte colonystimulating factor have chronic neutropenia, granulocyte and macrophage progenitor cell deficiency, and impaired neutrophil mobilization. Blood 84: 1737-1746.
27. Zhan, Y., G. J. Lieschke, D. Grail, A. R. Dunn, and C. Cheers. 1998. Essential roles for granulocyte-macrophage colony-stimulating factor (GM-CSF) and G-CSF in the sustained hematopoietic response of Listeria monocytogenes-infected mice. Blood 91: 863-869.
28. Zhu, G., M. M. Augustine, T. Azuma, L. Luo, S. Yao, S. Anand, A. C. Rietz, J. Huang, H. Xu, A. S. Flies, et al. 2009. B7-H4-deficient mice display augmented neutrophil-mediated innate immunity. Blood 113: 1759-1767.
29. Navarini, A. A., K. S. Lang, A. Verschoor, M. Recher, A. S. Zinkernagel, V. Nizet, B. Odermatt, H. Hengartner, and R. M. Zinkernagel. 2009. Innate immuneinduced depletion of bone marrow neutrophils aggravates systemic bacterial infections. Proc. Natl. Acad. Sci. USA 106: 7107-7112.
30. Gregory, S. H., L. P. Cousens, N. van Rooijen, E. A. Döpp, T. M. Carlos, and E. J. Wing. 2002. Complementary adhesion molecules promote neutrophil-Kupffer cell interaction and the elimination of bacteria taken up by the liver. J. Immunol. 168: 308-315.
31. Pinto, A. J., D. Stewart, N. van Rooijen, and P. S. Morahan. 1991. Selective depletion of liver and splenic macrophages using liposomes encapsulating the drug dichloromethylene diphosphonate: effects on antimicrobial resistance. J. Leukoc. Biol. 49: 579-586.
32. Seki, E., H. Tsutsui, N. M. Tsuji, N. Hayashi, K. Adachi, H. Nakano, S. Futatsugi-Yumikura, O. Takeuchi, K. Hoshino, S. Akira, et al. 2002. Critical roles of myeloid differentiation factor 88-dependent proinflammatory cytokine release in early phase clearance of Listeria monocytogenes in mice. J. Immunol. 169: 3863-3868.
33. Tripp, C. S., S. F. Wolf, and E. R. Unanue. 1993. Interleukin 12 and tumor necrosis factor alpha are costimulators of interferon gamma production by natural killer cells in severe combined immunodeficiency mice with listeriosis, and interleukin 10 is a physiologic antagonist. Proc. Natl. Acad. Sci. USA 90: 3725-3729.
34. Soudja, S. M., A. L. Ruiz, J. C. Marie, and G. Lauvau. 2012. Inflammatory monocytes activate memory CD8(+) T and innate NK lymphocytes independent of cognate antigen during microbial pathogen invasion. Immunity 37: 549-562.
35. Serbina, N. V., T. P. Salazar-Mather, C. A. Biron, W. A. Kuziel, and E. G. Pamer. 2003. TNF/iNOS-producing dendritic cells mediate innate immune defense against bacterial infection. Immunity 19: 59-70.
36. + T cells provide innate immune protection against Listeria monocytogenes in the absence of cognate antigen. J. Exp. Med. 198: 1583-1593.
37. Eash, K. J., J. M. Means, D. W. White, and D. C. Link. 2009. CXCR4 is a key regulator of neutrophil release from the bone marrow under basal and stress granulopoiesis conditions. Blood 113: 4711-4719.
38. Ebe, Y., G. Hasegawa, H. Takatsuka, H. Umezu, M. Mitsuyama, M. Arakawa, N. Mukaida, and M. Naito. 1999. The role of Kupffer cells and regulation of neutrophil migration into the liver by macrophage inflammatory protein-2 in primary listeriosis in mice. Pathol. Int. 49: 519-532.
39. Semerad, C. L., F. Liu, A. D. Gregory, K. Stumpf, and D. C. Link. 2002. G-CSF is an essential regulator of neutrophil trafficking from the bone marrow to the blood. Immunity 17: 413-423.
40. Pittman, K., and P. Kubes. 2013. Damage-associated molecular patterns control neutrophil recruitment. J. Innate Immun. 5: 315-323.
41. Thomas, C. J., and K. Schroder. 2013. Pattern recognition receptor function in neutrophils. Trends Immunol. 34: 317-328.
42. Southgate, E. L., R. L. He, J. L. Gao, P. M. Murphy, M. Nanamori, and R. D. Ye. 2008. Identification of formyl peptides from Listeria monocytogenes and Staphylococcus aureus as potent chemoattractants for mouse neutrophils. J. Immunol. 181: 1429-1437.
43. Liu, M., K. Chen, T. Yoshimura, Y. Liu, W. Gong, A. Wang, J. L. Gao, P. M. Murphy, and J. M. Wang. 2012. Formylpeptide receptors are critical for rapid neutrophil mobilization in host defense against Listeria monocytogenes. Sci. Rep. 2: 786.
44. Gao, J. L., E. J. Lee, and P. M. Murphy. 1999. Impaired antibacterial host defense in mice lacking the N-formylpeptide receptor. J. Exp. Med. 189: 657-662.
45. Czuprynski, C. J., J. F. Brown, H. Steinberg, and D. Carroll. 1998. Mice lacking the murine interleukin-8 receptor homologue demonstrate paradoxical responses to acute and chronic experimental infection with Listeria monocytogenes. Microb. Pathog. 24: 17-23.
46. Cacalano, G., J. Lee, K. Kikly, A. M. Ryan, S. Pitts-Meek, B. Hultgren, W. I. Wood, and M. W. Moore. 1994. Neutrophil and B cell expansion in mice that lack the murine IL-8 receptor homolog. Science 265: 682-684.
47. Shuster, D. E., M. E. Kehrli, Jr., and M. R. Ackermann. 1995. Neutrophilia in mice that lack the murine IL-8 receptor homolog. Science 269: 1590-1591.
48. Brzoza-Lewis, K. L., J. J. Hoth, and E. M. Hiltbold. 2012. Type I interferon signaling regulates the composition of inflammatory infiltrates upon infection with Listeria monocytogenes. Cell. Immunol. 273: 41-51.
49. Arnaout, M. A. 1990. Structure and function of the leukocyte adhesion molecules CD11/CD18. Blood 75: 1037-1050.
50. Wu, H., J. E. Prince, C. F. Brayton, C. Shah, D. Zeve, S. H. Gregory, C. W. Smith, and C. M. Ballantyne. 2003. Host resistance of CD18 knockout mice against systemic infection with Listeria monocytogenes. Infect. Immun. 71: 5986-5993.
51. Miyamoto, M., M. Emoto, Y. Emoto, V. Brinkmann, I. Yoshizawa, P. Seiler, P. Aichele, E. Kita, and S. H. E. Kaufmann. 2003. Neutrophilia in LFA-1-deficient mice confers resistance to listeriosis: possible contribution of granulocyte-colony-stimulating factor and IL-17. J. Immunol. 170: 5228-5234.
52. Rosen, H., S. Gordon, and R. J. North. 1989. Exacerbation of murine listeriosis by a monoclonal antibody specific for the type 3 complement receptor of myelomonocytic cells. Absence of monocytes at infective foci allows Listeria to multiply in nonphagocytic cells. J. Exp. Med. 170: 27-37.
53. Hamada, S., M. Umemura, T. Shiono, K. Tanaka, A. Yahagi, M. D. Begum, K. Oshiro, Y. Okamoto, H. Watanabe, K. Kawakami, et al. 2008. IL-17A produced by gammadelta T cells plays a critical role in innate immunity against listeria monocytogenes infection in the liver. J. Immunol. 181: 3456-3463.
54. Meeks, K. D., A. N. Sieve, J. K. Kolls, N. Ghilardi, and R. E. Berg. 2009. IL-23 is required for protection against systemic infection with Listeria monocytogenes. J. Immunol. 183: 8026-8034.
55. Severa, M., S. A. Islam, S. N. Waggoner, Z. Jiang, N. D. Kim, G. Ryan, E. Kurt-Jones, I. Charo, D. R. Caffrey, V. L. Boyartchuk, et al. 2014. The transcriptional repressor BLIMP1 curbs host defenses by suppressing expression of the chemokine CCL8. J. Immunol. 192: 2291-2304.
56. Czuprynski, C. J., and J. F. Brown. 1987. Purified human and recombinant murine interleukin-1 alpha induced accumulation of inflammatory peritoneal neutrophils and mononuclear phagocytes: possible contributions to antibacterial resistance. Microb. Pathog. 3: 377-386.
57. Czuprynski, C. J., and J. F. Brown. 1987. Recombinant murine interleukin-1 alpha enhancement of nonspecific antibacterial resistance. Infect. Immun. 55: 2061-2065.
58. Czuprynski, C. J., J. F. Brown, K. M. Young, A. J. Cooley, and R. S. Kurtz. 1988. Effects of murine recombinant interleukin 1 alpha on the host response to bacterial infection. J. Immunol. 140: 962-968.
59. Kurlander, R. J., M. Hoffman, S. S. Kratz, and J. Gates. 1989. Comparison of the effects of IL-1 alpha and TNF-alpha on phagocyte accumulation and murine antibacterial immunity. Cell. Immunol. 123: 9-22.
60. Havell, E. A., L. L. Moldawer, D. Helfgott, P. L. Kilian, and P. B. Sehgal. 1992. Type I IL-1 receptor blockade exacerbates murine listeriosis. J. Immunol. 148: 1486-1492.
61. Zheng, H., D. Fletcher, W. Kozak, M. Jiang, K. J. Hofmann, C. A. Conn, D. Soszynski, C. Grabiec, M. E. Trumbauer, A. Shaw, et al. 1995. Resistance to fever induction and impaired acute-phase response in interleukin-1 beta-deficient mice. Immunity 3: 9-19.
62. Rogers, H. W., C. S. Tripp, R. D. Schreiber, and E. R. Unanue. 1994. Endogenous IL-1 is required for neutrophil recruitment and macrophage activation during murine listeriosis. J. Immunol. 153: 2093-2101.
63. Dalrymple, S. A., L. A. Lucian, R. Slattery, T. McNeil, D. M. Aud, S. Fuchino, F. Lee, and R. Murray. 1995. Interleukin-6-deficient mice are highly susceptible to Listeria monocytogenes infection: correlation with inefficient neutrophilia. Infect. Immun. 63: 2262-2268.
64. Kopf, M., H. Baumann, G. Freer, M. Freudenberg, M. Lamers, T. Kishimoto, R. Zinkernagel, H. Bluethmann, and G. Köhler. 1994. Impaired immune and acute-phase responses in interleukin-6-deficient mice. Nature 368: 339-342.
65. Hoge, J., I. Yan, N. Jänner, V. Schumacher, A. Chalaris, O. M. Steinmetz, D. R. Engel, J. Scheller, S. Rose-John, and H. W. Mittrucker. 2013. IL-6 controls the innate immune response against Listeria monocytogenes via classical IL-6 signaling. J. Immunol. 190: 703-711.
66. Break, T. J., S. Jun, M. Indramohan, K. D. Carr, A. N. Sieve, L. Dory, and R. E. Berg. 2012. Extracellular superoxide dismutase inhibits innate immune responses and clearance of an intracellular bacterial infection. J. Immunol. 188: 3342-3350.
67. Helmy, K. Y., K. J. Katschke, Jr., N. N. Gorgani, N. M. Kljavin, J. M. Elliott, L. Diehl, S. J. Scales, N. Ghilardi, and M. van Lookeren Campagne. 2006. CRIg: a macrophage complement receptor required for phagocytosis of circulating pathogens. Cell 124: 915-927.
68. Arnett, E., S. Vadia, C. C. Nackerman, S. Oghumu, A. R. Satoskar, K. R. McLeish, S. M. Uriarte, and S. Seveau. 2014. The pore-forming toxin listeriolysin O is degraded by neutrophil metalloproteinase-8 and fails to mediate Listeria monocytogenes intracellular survival in neutrophils. J. Immunol. 192: 234-244.
69. Zhang, H., R. A. Clemens, F. Liu, Y. Hu, Y. Baba, P. Theodore, T. Kurosaki, and C. A. Lowell. 2014. STIM1 calcium sensor is required for activation of the phagocyte oxidase during inflammation and host defense. Blood 123: 2238-2249.
70. Lee, S. C., S. A. Ju, H. N. Pack, S. K. Heo, J. H. Suh, S. M. Park, B. K. Choi, B. S. Kwon, and B. S. Kim. 2005. 4-1BB (CD137) is required for rapid clearance of Listeria monocytogenes infection. Infect. Immun. 73: 5144-5151.
71. Lee, S. C., S. A. Ju, B. H. Sung, S. K. Heo, H. R. Cho, E. A. Lee, J. D. Kim, I. H. Lee, S. M. Park, Q. T. Nguyen, et al. 2009. Stimulation of the molecule 4-1BB enhances host defense against Listeria monocytogenes infection in mice by inducing rapid infiltration and activation of neutrophils and monocytes. Infect. Immun. 77: 2168-2176.
72. Segal, A. W. 1989. The electron transport chain of the microbicidal oxidase of phagocytic cells and its involvement in the molecular pathology of chronic granulomatous disease. J. Clin. Invest. 83: 1785-1793.
73. Babior, B. M. 2004. NADPH oxidase. Curr. Opin. Immunol. 16: 42-47.
74. Dinauer, M. C., M. B. Deck, and E. R. Unanue. 1997. Mice lacking reduced nicotinamide adenine dinucleotide phosphate oxidase activity show increased susceptibility to early infection with Listeria monocytogenes. J. Immunol. 158: 5581-5583.
75. Shiloh, M. U., J. D. MacMicking, S. Nicholson, J. E. Brause, S. Potter, M. Marino, F. Fang, M. Dinauer, and C. Nathan. 1999. Phenotype of mice and macrophages deficient in both phagocyte oxidase and inducible nitric oxide synthase. Immunity 10: 29-38.
76. LaCourse, R., L. Ryan, and R. J. North. 2002. Expression of NADPH oxidasedependent resistance to listeriosis in mice occurs during the first 6 to 12 hours of liver infection. Infect. Immun. 70: 7179-7181.
77. Endres, R., A. Luz, H. Schulze, H. Neubauer, A. Futterer, S. M. Holland, H. Wagner, and K. Pfeffer. 1997. Listeriosis in p47(phox-/-) and TRp55-/-mice: protection despite absence of ROI and susceptibility despite presence of RNI. Immunity 7: 419-432.
78. Freeman, J. L., and J. D. Lambeth. 1996. NADPH oxidase activity is independent of p47phox in vitro. J. Biol. Chem. 271: 22578-22582.
79. West, A. P., I. E. Brodsky, C. Rahner, D. K. Woo, H. Erdjument-Bromage, P. Tempst, M. C. Walsh, Y. Choi, G. S. Shadel, and S. Ghosh. 2011. TLR signalling augments macrophage bactericidal activity through mitochondrial ROS. Nature 472: 476-480.
80. Geng, J., X. Sun, P. Wang, S. Zhang, X. Wang, H. Wu, L. Hong, C. Xie, X. Li, H. Zhao, et al. 2015. Kinases Mst1 and Mst2 positively regulate phagocytic induction of reactive oxygen species and bactericidal activity. Nat. Immunol. 16: 1142-1152.
81. Noubade, R., K. Wong, N. Ota, S. Rutz, C. Eidenschenk, P. A. Valdez, J. Ding, I. Peng, A. Sebrell, P. Caplazi, et al. 2014. NRROS negatively regulates reactive oxygen species during host defence and autoimmunity. Nature 509: 235-239.
82. Hampton, M. B., A. J. Kettle, and C. C. Winterbourn. 1996. Involvement of superoxide and myeloperoxidase in oxygen-dependent killing of Staphylococcus aureus by neutrophils. Infect. Immun. 64: 3512-3517.
83. Bortolussi, R., C. M. Vandenbroucke-Grauls, B. S. van Asbeck, and J. Verhoef. 1987. Relationship of bacterial growth phase to killing of Listeria monocytogenes by oxidative agents generated by neutrophils and enzyme systems. Infect. Immun. 55: 3197-3203.
84. Aratani, Y., H. Koyama, S. Nyui, K. Suzuki, F. Kura, and N. Maeda. 1999. Severe impairment in early host defense against Candida albicans in mice deficient in myeloperoxidase. Infect. Immun. 67: 1828-1836.
85. MacMicking, J. D. C., C. Nathan, G. Hom, N. Chartrain, D. S. Fletcher, M. Trumbauer, K. Stevens, Q. W. Xie, K. Sokol, N. Hutchinson, et al. 1995. Altered responses to bacterial infection and endotoxic shock in mice lacking inducible nitric oxide synthase. Cell 81: 641-650.
86. Cole, C., S. Thomas, H. Filak, P. M. Henson, and L. L. Lenz. 2012. Nitric oxide increases susceptibility of Toll-like receptor-activated macrophages to spreading Listeria monocytogenes. Immunity 36: 807-820.
87. Muller, M., R. Althaus, D. Fröhlich, K. Frei, and H. P. Eugster. 1999. Reduced antilisterial activity of TNF-deficient bone marrow-derived macrophages is due to impaired superoxide production. Eur. J. Immunol. 29: 3089-3097.
88. Edelson, B. T., and E. R. Unanue. 2002. MyD88-dependent but Toll-like receptor 2-independent innate immunity to Listeria: no role for either in macrophage listericidal activity. J. Immunol. 169: 3869-3875.
89. Arnold-Schrauf, C., M. Dudek, A. Dielmann, L. Pace, M. Swallow, F. Kruse, A. A. Kuhl, B. Holzmann, L. Berod, and T. Sparwasser. 2014. Dendritic cells coordinate innate immunity via MyD88 signaling to control Listeria monocytogenes infection. Cell Reports 6: 698-708.
90. Mosa, A., C. Trumstedt, E. Eriksson, O. Soehnlein, F. Heuts, K. Janik, A. Klos, O. Dittrich-Breiholz, M. Kracht, A. Hidmark, et al. 2009. Nonhematopoietic cells control the outcome of infection with Listeria monocytogenes in a nucleotide oligomerization domain 1-dependent manner. Infect. Immun. 77: 2908-2918.
91. Jeong, Y. J., M. J. Kang, S. J. Lee, C. H. Kim, J. C. Kim, T. H. Kim, D. J. Kim, D. Kim, G. Núñez, and J. H. Park. 2014. Nod2 and Rip2 contribute to innate immune responses in mouse neutrophils. Immunology 143: 269-276.
92. Anand, P. K., R. K. Malireddi, J. R. Lukens, P. Vogel, J. Bertin, M. Lamkanfi, and T. D. Kanneganti. 2012. NLRP6 negatively regulates innate immunity and host defence against bacterial pathogens. Nature 488: 389-393.
93. Xia, P., S. Wang, B. Ye, Y. Du, G. Huang, P. Zhu, and Z. Fan. 2015. Sox2 functions as a sequence-specific DNA sensor in neutrophils to initiate innate immunity against microbial infection. Nat. Immunol. 16: 366-375.
94. Lang, K. S., P. A. Lang, A. Meryk, A. A. Pandyra, L. M. Boucher, V. I. Pozdeev, M. W. Tusche, J. R. Göthert, J. Haight, A. Wakeham, et al. 2013. Involvement of Toso in activation of monocytes, macrophages, and granulocytes. Proc. Natl. Acad. Sci. USA 110: 2593-2598.
95. Harty, J. T., and M. J. Bevan. 1995. Specific immunity to Listeria monocytogenes in the absence of IFN gamma. Immunity 3: 109-117.
96. Huang, S., W. Hendriks, A. Althage, S. Hemmi, H. Bluethmann, R. Kamijo, J. Vilcek, R. M. Zinkernagel, and M. Aguet. 1993. Immune response in mice that lack the interferon-gamma receptor. Science 259: 1742-1745.
97. + T cells to innate immunity: IFN-γamma secretion induced by IL-12 and IL-18. Eur. J. Immunol. 32: 2807-2816.
98. Berg, R. E., E. Crossley, S. Murray, and J. Forman. 2005. Relative contributions of NK and CD8 T cells to IFN-γamma mediated innate immune protection against Listeria monocytogenes. J. Immunol. 175: 1751-1757.
99. Yin, J., and T. A. Ferguson. 2009. Identification of an IFN-γamma-producing neutrophil early in the response to Listeria monocytogenes. J. Immunol. 182: 7069-7073.
100. Conlan, J. W. 1997. Neutrophils and tumour necrosis factor-alpha are important for controlling early gastrointestinal stages of experimental murine listeriosis. J. Med. Microbiol. 46: 239-250.
101. Rothe, J., W. Lesslauer, H. Lötscher, Y. Lang, P. Koebel, F. Köntgen, A. Althage, R. Zinkernagel, M. Steinmetz, and H. Bluethmann. 1993. Mice lacking the tumour necrosis factor receptor 1 are resistant to TNF-mediated toxicity but highly susceptible to infection by Listeria monocytogenes. Nature 364: 798-802.
102. Pasparakis, M., L. Alexopoulou, V. Episkopou, and G. Kollias. 1996. Immune and inflammatory responses in TNF alpha-deficient mice: a critical requirement for TNF alpha in the formation of primary B cell follicles, follicular dendritic cell networks and germinal centers, and in the maturation of the humoral immune response. J. Exp. Med. 184: 1397-1411.
103. Pfeffer, K., T. Matsuyama, T. M. Kundig, A. Wakeham, K. Kishihara, A. Shahinian, K. Wiegmann, P. S. Ohashi, M. Krönke, and T. W. Mak. 1993. Mice deficient for the 55 kd tumor necrosis factor receptor are resistant to endotoxic shock, yet succumb to L. monocytogenes infection. Cell 73: 457-467.
104. Grivennikov, S. I., A. V. Tumanov, D. J. Liepinsh, A. A. Kruglov, B. I. Marakusha, A. N. Shakhov, T. Murakami, L. N. Drutskaya, I. Förster, B. E. Clausen, et al. 2005. Distinct and nonredundant in vivo functions of TNF produced by t cells and macrophages/neutrophils: protective and deleterious effects. Immunity 22: 93-104.
105. Leist, M., F. Gantner, S. Jilg, and A. Wendel. 1995. Activation of the 55 kDa TNF receptor is necessary and sufficient for TNF-induced liver failure, hepatocyte apoptosis, and nitrite release. J. Immunol. 154: 1307-1316.
106. Leist, M., F. Gantner, I. Bohlinger, P. G. Germann, G. Tiegs, and A. Wendel. 1994. Murine hepatocyte apoptosis induced in vitro and in vivo by TNF-alpha requires transcriptional arrest. J. Immunol. 153: 1778-1788.
107. Czuprynski, C. J., J. F. Brown, R. D. Wagner, and H. Steinberg. 1994. Administration of antigranulocyte monoclonal antibody RB6-8C5 prevents expression of acquired resistance to Listeria monocytogenes infection in previously immunized mice. Infect. Immun. 62: 5161-5163.
108. Narni-Mancinelli, E., S. M. Soudja, K. Crozat, M. Dalod, P. Gounon, F. Geissmann, and G. Lauvau. 2011. Inflammatory monocytes and neutrophils are licensed to kill during memory responses in vivo. PLoS Pathog. 7: e1002457.
109. + T cells mediate antibacterial immunity via CCL3 activation of TNF/ROI+ phagocytes. J. Exp. Med. 204: 2075-2087.
110. Soudja, S. M., C. Chandrabos, E. Yakob, M. Veenstra, D. Palliser, and G. Lauvau. 2014. Memory-T-cell-derived interferon-g instructs potent innate cell activation for protective immunity. Immunity 40: 974-988.
111. Chaturvedi, V., J. M. Ertelt, T. T. Jiang, J. M. Kinder, L. Xin, K. J. Owens, H. N. Jones, and S. S. Way. 2015. CXCR3 blockade protects against Listeria monocytogenes infection-induced fetal wastage. J. Clin. Invest. 125: 1713-1725.
112. Ordoñez-Rueda, D., F. Jönsson, D. A. Mancardi, W. Zhao, A. Malzac, Y. Liang, E. Bertosio, P. Grenot, V. Blanquet, S. Sabrautzki, et al. 2012. A hypomorphic mutation in the Gfi1 transcriptional repressor results in a novel form of neutropenia. Eur. J. Immunol. 42: 2395-2408.