Neutrophils and macrophages work in concert as inducers and effectors of adaptive immunity against extracellular and intracellular microbial pathogens

Journal of Leukocyte Biology

Volumn 87, Issue 5, 2010, Pages 805-813

  Silva, Manuel T ^a  

^a UNIVERSITY OF PORTO   (Portugal)

Author keywords

Adaptive immunity; Antimicrobial mechanisms; Phagocytosis

Indexed keywords

CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CXCR3; CXCL11 CHEMOKINE; CXCL9 CHEMOKINE; FC RECEPTOR; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 17;

ADAPTIVE IMMUNITY; ANTIMICROBIAL ACTIVITY; CELL DIFFERENTIATION; CYTOKINE PRODUCTION; DEFENSE MECHANISM; DENDRITIC CELL; HELPER CELL; HOST RESISTANCE; HUMAN; MACROPHAGE; MONOCYTE; MYELOID PROGENITOR CELL; NEUTROPHIL; NONHUMAN; OPSONIZATION; PHAGOCYTE; PRIORITY JOURNAL; REVIEW; TH1 CELL; TH17 CELL; TISSUE INJURY; ANIMAL; CYTOLOGY; IMMUNOLOGY; INFECTION; METABOLISM;

ADAPTIVE IMMUNITY; ANIMALS; CELL DIFFERENTIATION; HUMANS; INFECTION; MACROPHAGES; NEUTROPHILS;

EID: 77950285012     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.1109767     Document Type: Review

References (172)

1. Janeway Jr., C. A. (1989) Approaching the asymptote? Evolution and revolution in immunology. Cold Spring Harb. Symp. Quant. Biol. 54 (Pt. 1), 1-13.
2. Serbina, N. V., Jia, T., Hohl, T. M., Pamer, E. G. (2008) Monocyte-mediated defense against microbial pathogens. Annu. Rev. Immunol. 26, 421-452.
3. Van Furth, R., Diesselhoff-den Dulk, M. C., Mattie, H. (1973) Quantitative study on the production and kinetics of mononuclear phagocytes during an acute inflammatory reaction. J. Exp. Med. 138, 1314-1330.
4. Trzcinski, K., Thompson, C. M., Srivastava, A., Basset, A., Malley, R., Lipsitch, M. (2008) Protection against nasopharyngeal colonization by Streptococcus pneumoniae is mediated by antigen-specific CD4+ T cells. Infect. Immun. 76, 2678-2684.
5. Joyce, E. A., Popper, S. J., Falkow, S. (2009) Streptococcus pneumoniae nasopharyngeal colonization induces type I interferons and interferon-induced gene expression. BMC Genomics 10, 404.
6. DeLyria, E. S., Redline, R. W., Blanchard, T. G. (2009) Vaccination of mice against H. pylori induces a strong Th-17 response and immunity that is neutrophil dependent. Gastroenterology 136, 247-256.
7. Silva, M. T., Silva, M. N., Appelberg, R. (1989) Neutrophil-macrophage cooperation in the host defense against mycobacterial infections. Microb. Pathog. 6, 369-380.
8. Appelberg, R., Silva, M. T. (1989) T cell-dependent chronic neutrophilia during mycobacterial infections. Clin. Exp. Immunol. 78, 478-483.
9. Appelberg, R. (1992) Mycobacterial infection primes T cells and macrophages for enhanced recruitment of neutrophils. J. Leukoc. Biol. 51, 472-477.
10. Lyons, M. J., Yoshimura, T., McMurray, D. N. (2002) Mycobacterium bovis BCG vaccination augments interleukin-8 mRNA expression and protein production in guinea pig alveolar macrophages infected with Mycobacterium tuberculosis. Infect. Immun. 70, 5471-5478.
11. Tsai, M. C., Chakravarty, S., Zhu, G., Xu, J., Tanaka, K., Koch, C., Tufariello, J., Flynn, J., Chan, J. (2006) Characterization of the tuberculous granuloma in murine and human lungs: cellular composition and relative tissue oxygen tension. Cell. Microbiol. 8, 218-232.
12. Tam, M. A., Rydstrom, A., Sundquist, M., Wick, M. J. (2008) Early cellular responses to Salmonella infection: dendritic cells, monocytes, and more. Immunol. Rev. 225, 140-162.
13. Mordue, D. G., Sibley, L. D. (2003) A novel population of Gr-1+-activated macrophages induced during acute toxoplasmosis. J. Leukoc. Biol. 74, 1015-1025.
14. Czuprynski, C. J., Henson, P. M., Campbell, P. A. (1984) Killing of Listeria monocytogenes by inflammatory neutrophils and mononuclear phagocytes from immune and nonimmune mice. J. Leukoc. Biol. 35, 193-208.
15. Jalapathy, K. V., Prabha, C., Das, S. D. (2004) Correlates of protective immune response in tuberculous pleuritis. FEMS Immunol. Med. Microbiol. 40, 139-145.
16. Kroegel, C., Antony, V. B. (1997) Immunobiology of pleural inflammation: potential implications for pathogenesis, diagnosis and therapy. Eur. Respir. J. 10, 2411-2418.
17. Mellman, I., Steinman, R. M. (2001) Dendritic cells: specialized and regulated antigen processing machines. Cell 106, 255-258. (Pubitemid 32772607)
18. Scapini, P., Lapinet-Vera, J. A., Gasperini, S., Calzetti, F., Bazzoni, F., Cassatella, M. A. (2000) The neutrophil as a cellular source of chemokines. Immunol. Rev. 177, 195-203.
19. Yamashiro, S., Kamohara, H., Wang, J. M., Yang, D., Gong, W. H., Yoshimura, T. (2001) Phenotypic and functional change of cytokine-activated neutrophils: inflammatory neutrophils are heterogeneous and enhance adaptive immune responses. J. Leukoc. Biol. 69, 698-704.
20. van Gisbergen, K. P., Geijtenbeek, T. B., van Kooyk, Y. (2005) Close encounters of neutrophils and DCs. Trends Immunol. 26, 626-631.
21. Cassatella, M. A. (1999) Neutrophil-derived proteins: selling cytokines by the pound. Adv. Immunol. 73, 369-509.
22. Trinchieri, G. (2003) Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat. Rev. Immunol. 3, 133-146.
23. Tateda, K., Moore, T. A., Deng, J. C., Newstead, M. W., Zeng, X., Matsukawa, A., Swanson, M. S., Yamaguchi, K., Standiford, T. J. (2001) Early recruitment of neutrophils determines subsequent T1/T2 host responses in a murine model of Legionella pneumophila pneumonia. J. Immunol. 166, 3355-3361. (Pubitemid 33117336)
24. Sconocchia, G., Campagnano, L., Adorno, D., Iacona, A., Cococcetta, N. Y., Boffo, V., Amadori, S., Casciani, C. U. (2001) CD44 ligation on peripheral blood polymorphonuclear cells induces interleukin-6 production. Blood 97, 3621-3627.
25. Hoshino, A., Nagao, T., Nagi-Miura, N., Ohno, N., Yasuhara, M., Yamamoto, K., Nakayama, T., Suzuki, K. (2008) MPO-ANCA induces IL-17 production by activated neutrophils in vitro via classical complement pathway-dependent manner. J. Autoimmun. 31, 79-89. (Pubitemid 351685761)
26. Abadie, V., Badell, E., Douillard, P., Ensergueix, D., Leenen, P. J., Tanguy, M., Fiette, L., Saeland, S., Gicquel, B., Winter, N. (2005) Neutrophils rapidly migrate via lymphatics after Mycobacterium bovis BCG intradermal vaccination and shuttle live bacilli to the draining lymph nodes. Blood 106, 1843-1850. (Pubitemid 41208603)
27. Bonneau, M., Epardaud, M., Payot, F., Niborski, V., Thoulouze, M. I., Bernex, F., Charley, B., Riffault, S., Guilloteau, L. A., Schwartz-Cornil, I. (2006) Migratory monocytes and granulocytes are major lymphatic carriers of Salmonella from tissue to draining lymph node. J. Leukoc. Biol. 79, 268-276.
28. Potter, N. S., Harding, C. V. (2001) Neutrophils process exogenous bacteria via an alternate class I MHC processing pathway for presentation of peptides to T lymphocytes. J. Immunol. 167, 2538-2546.
29. Megiovanni, A. M., Sanchez, F., Robledo-Sarmiento, M., Morel, C., Gluckman, J. C., Boudaly, S. (2006) Polymorphonuclear neutrophils deliver activation signals and antigenic molecules to dendritic cells: a new link between leukocytes upstream of T lymphocytes. J. Leukoc. Biol. 79, 977-988.
30. Morel, C., Badell, E., Abadie, V., Robledo, M., Setterblad, N., Gluckman, J. C., Gicquel, B., Boudaly, S., Winter, N. (2008) Mycobacterium bovis BCG-infected neutrophils and dendritic cells cooperate to induce specific T cell responses in humans and mice. Eur. J. Immunol. 38, 437-447.
31. Fanger, N. A., Liu, C., Guyre, P. M., Wardwell, K., O'Neil, J., Guo, T. L., Christian, T. P., Mudzinski, S. P., Gosselin, E. J. (1997) Activation of human T cells by major histocompatability complex class II expressing neutrophils: proliferation in the presence of superantigen, but not tetanus toxoid. Blood 89, 4128-4135. (Pubitemid 27220961)
32. Radsak, M., Iking-Konert, C., Stegmaier, S., Andrassy, K., Hansch, G. M. (2000) Polymorphonuclear neutrophils as accessory cells for T-cell activation: major histocompatibility complex class II restricted antigen-dependent induction of T-cell proliferation. Immunology 101, 521-530. (Pubitemid 32001467)
33. Reinisch, W., Tillinger, W., Lichtenberger, C., Gangl, A., Willheim, M., Scheiner, O., Steger, G. (1996) In vivo induction of HLA-DR on human neutrophils in patients treated with interferon-γ. Blood 87, 3068.
34. Wagner, C., Iking-Konert, C., Hug, F., Stegmaier, S., Heppert, V., Wentzensen, A., Hansch, G. M. (2006) Cellular inflammatory response to persistent localized Staphylococcus aureus infection: phenotypical and functional characterization of polymorphonuclear neutrophils (PMN). Clin. Exp. Immunol. 143, 70-77.
35. Culshaw, S., Millington, O. R., Brewer, J. M., McInnes, I. B. (2008) Murine neutrophils present class II restricted antigen. Immunol. Lett. 118, 49-54.
36. Olson, T. S., Ley, K. (2002) Chemokines and chemokine receptors in leukocyte trafficking. Am. J. Physiol. Regul. Integr. Comp. Physiol. 283, R7-R28.
37. Pelletier, M., Maggi, L., Micheletti, A., Lazzeri, E., Tamassia, N., Costantini, C., Cosmi, L., Lunardi, C., Annunziato, F., Romagnani, S., Cassatella, M. A. (2010) Evidence for a cross-talk between human neutrophils and Th17 cells. Blood 115, 335-343.
38. O'Garra, A., McEvoy, L. M., Zlotnik, A. (1998) T-cell subsets: chemokine receptors guide the way. Curr. Biol. 8, R646-R649.
39. Chertov, O., Yang, D., Howard, O. M., Oppenheim, J. J. (2000) Leukocyte granule proteins mobilize innate host defenses and adaptive immune responses. Immunol. Rev. 177, 68-78.
40. De la Rosa, G., Yang, D., Tewary, P., Varadhachary, A., Oppenheim, J. J. (2008) Lactoferrin acts as an alarmin to promote the recruitment and activation of APCs and antigen-specific immune responses. J. Immunol. 180, 6868-6876.
41. Yang, D., de la Rosa, G., Tewary, P., Oppenheim, J. J. (2009) Alarmins link neutrophils and dendritic cells. Trends Immunol. 30, 531-537.
42. De Yang, Chen, Q., Schmidt, A. P., Anderson, G. M., Wang, J. M., Wooters, J., Oppenheim, J. J., Chertov, O. (2000) LL-37, the neutrophil granule- and epithelial cell-derived cathelicidin, utilizes formyl peptide receptor-like 1 (FPRL1) as a receptor to chemoattract human peripheral blood neutrophils, monocytes, and T cells. J. Exp. Med. 192, 1069-1074.
43. Grigat, J., Soruri, A., Forssmann, U., Riggert, J., Zwirner, J. (2007) Chemoattraction of macrophages, T lymphocytes, and mast cells is evolutionarily conserved within the human α-defensin family. J. Immunol. 179, 3958-3965.
44. Actor, J. K., Hwang, S. A., Olsen, M., Zimecki, M., Hunter Jr., R. L., Kruzel, M. L. (2002) Lactoferrin immunomodulation of DTH response in mice. Int. Immunopharmacol. 2, 475-486.
45. Kirimanjeswara, G. S., Agosto, L. M., Kennett, M. J., Bjornstad, O. N., Harvill, E. T. (2005) Pertussis toxin inhibits neutrophil recruitment to delay antibody-mediated clearance of Bordetella pertussis. J. Clin. Invest. 115, 3594-3601.
46. Andreasen, C., Carbonetti, N. H. (2009) Role of neutrophils in response to Bordetella pertussis infection in mice. Infect. Immun. 77, 1182-1188.
47. Zhang, Z., Clarke, T. B., Weiser, J. N. (2009) Cellular effectors mediating Th17-dependent clearance of pneumococcal colonization in mice. J. Clin. Invest. 119, 1899-1909.
48. Kirimanjeswara, G. S., Golden, J. M., Bakshi, C. S., Metzger, D. W. (2007) Prophylactic and therapeutic use of antibodies for protection against respiratory infection with Francisella tularensis. J. Immunol. 179, 532-539.
49. Dale, D., Liles, W. (2002) Neutrophils and monocytes: normal physiology and disorders of neutrophil and monocyte production. In Blood: Principles and Practice of Hematology (R. I. Handin, S. E. Lux, T. P. Stossel, eds.), Philadelphia, PA, USA, Lippincott Williams & Wilkins, 455-482.
50. Ribeiro-Gomes, F. L., Otero, A. C., Gomes, N. A., Moniz-De-Souza, M. C., Cysne-Finkelstein, L., Arnholdt, A. C., Calich, V. L., Coutinho, S. G., Lopes, M. F., DosReis, G. A. (2004) Macrophage interactions with neutrophils regulate Leishmania major infection. J. Immunol. 172, 4454-4462.
51. Novais, F. O., Santiago, R.C., Bafica, A., Khouri, R., Afonso, L., Borges, V.M., Brodskyn, C., Barral-Netto, M., Barral, A., de Oliveira, C.I. (2009) Neutrophils and macrophages cooperate in host resistance against Leishmania braziliensis infection. J. Immunol. 183, 8088-8098.
52. Tan, B. H., Meinken, C., Bastian, M., Bruns, H., Legaspi, A., Ochoa, M. T., Krutzik, S. R., Bloom, B. R., Ganz, T., Modlin, R. L., Stenger, S. (2006) Macrophages acquire neutrophil granules for antimicrobial activity against intracellular pathogens. J. Immunol. 177, 1864-1871. (Pubitemid 44092525)
53. Segal, A. W. (2005) How neutrophils kill microbes. Annu. Rev. Immunol. 23, 197-223.
54. Soehnlein, O. (2009) Direct and alternative antimicrobial mechanisms of neutrophil-derived granule proteins. J. Mol. Med. 87, 1157-1164.
55. Reinhardt, R. L., Kang, S. J., Liang, H. E., Locksley, R. M. (2006) T helper cell effector fates - who, how and where? Curr. Opin. Immunol. 18, 271-277.
56. Medzhitov, R. (2007) Recognition of microorganisms and activation of the immune response. Nature 449, 819-826. (Pubitemid 47598622)
57. Mosmann, T. R., Coffman, R. L. (1989) TH1 and TH2 cells: different patterns of lymphokine secretion lead to different functional properties. Annu. Rev. Immunol. 7, 145-173.
58. Park, H., Li, Z., Yang, X. O., Chang, S. H., Nurieva, R., Wang, Y. H., Wang, Y., Hood, L., Zhu, Z., Tian, Q., Dong, C. (2005) A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat. Immunol. 6, 1133-1141.
59. Harrington, L. E., Hatton, R. D., Mangan, P. R., Turner, H., Murphy, T. L., Murphy, K. M., Weaver, C. T. (2005) Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat. Immunol. 6, 1123-1132.
60. Stockinger, B., Veldhoen, M., Martin, B. (2007) Th17 T cells: linking innate and adaptive immunity. Semin. Immunol. 19, 353-361.
61. Anthony, R. M., Rutitzky, L. I., Urban Jr., J. F., Stadecker, M. J., Gause, W. C. (2007) Protective immune mechanisms in helminth infection. Nat. Rev. Immunol. 7, 975-987.
62. Chan, S. H., Perussia, B., Gupta, J. W., Kobayashi, M., Pospisil, M., Young, H. A., Wolf, S. F., Young, D., Clark, S. C., Trinchieri, G. (1991) Induction of interferon γ production by natural killer cell stimulatory factor: characterization of the responder cells and synergy with other inducers. J. Exp. Med. 173, 869-879.
63. Trinchieri, G. (1995) Interleukin-12: a proinflammatory cytokine with immunoregulatory functions that bridge innate resistance and antigen-specific adaptive immunity. Annu. Rev. Immunol. 13, 251-276.
64. Boehm, U., Klamp, T., Groot, M., Howard, J. C. (1997) Cellular responses to interferon-γ. Annu. Rev. Immunol. 15, 749-795.
65. Flynn, J. L., Chan, J. (2001) Immunology of tuberculosis. Annu. Rev. Immunol. 19, 93-129.
66. Laurence, A., O'Shea, J. J. (2007) T(H)-17 differentiation: of mice and men. Nat. Immunol. 8, 903-905.
67. Weaver, C. T., Hatton, R. D., Mangan, P. R., Harrington, L. E. (2007) IL-17 family cytokines and the expanding diversity of effector T cell lineages. Annu. Rev. Immunol. 25, 821-852.
68. Ishigame, H., Kakuta, S., Nagai, T., Kadoki, M., Nambu, A., Komiyama, Y., Fujikado, N., Tanahashi, Y., Akitsu, A., Kotaki, H., Sudo, K., Nakae, S., Sasakawa, C., Iwakura, Y. (2009) Differential roles of interleukin-17A and -17F in host defense against mucoepithelial bacterial infection and allergic responses. Immunity 30, 108-119.
69. Annunziato, F., Cosmi, L., Liotta, F., Maggi, E., Romagnani, S. (2009) Type 17 T helper cells - origins, features and possible roles in rheumatic disease. Nat. Rev. Rheumatol. 5, 325-331.
70. Korn, T., Bettelli, E., Oukka, M., Kuchroo, V. K. (2009) IL-17 and Th17 cells. Annu. Rev. Immunol. 27, 485-517.
71. Ferretti, S., Bonneau, O., Dubois, G. R., Jones, C. E., Trifilieff, A. (2003) IL-17, produced by lymphocytes and neutrophils, is necessary for lipopolysaccharide-induced airway neutrophilia: IL-15 as a possible trigger. J. Immunol. 170, 2106-2112. (Pubitemid 36197433)
72. Hue, S., Ahern, P., Buonocore, S., Kullberg, M. C., Cua, D. J., McKenzie, B. S., Powrie, F., Maloy, K. J. (2006) Interleukin-23 drives innate and T cell-mediated intestinal inflammation. J. Exp. Med. 203, 2473-2483.
73. Mangan, P. R., Harrington, L. E., O'Quinn, D. B., Helms, W. S., Bullard, D. C., Elson, C. O., Hatton, R. D., Wahl, S. M., Schoeb, T. R., Weaver, C. T. (2006) Transforming growth factor-β induces development of the T(H)17 lineage. Nature 441, 231-234.
74. Happel, K. I., Dubin, P. J., Zheng, M., Ghilardi, N., Lockhart, C., Quinton, L. J., Odden, A. R., Shellito, J. E., Bagby, G. J., Nelson, S., Kolls, J. K. (2005) Divergent roles of IL-23 and IL-12 in host defense against Klebsiella pneumoniae. J. Exp. Med. 202, 761-769.
75. Aujla, S. J., Kolls, J. K. (2009) IL-22: a critical mediator in mucosal host defense. J. Mol. Med. 87, 451-454.
76. Jones, C. E., Chan, K. (2002) Interleukin-17 stimulates the expression of interleukin-8, growth-related oncogene-α, and granulocyte-colony- stimulating factor by human airway epithelial cells. Am. J. Respir. Cell Mol. Biol. 26, 748-753.
77. Gaffen, S. L. (2008) An overview of IL-17 function and signaling. Cytokine 43, 402-407.
78. Lu, Y. J., Gross, J., Bogaert, D., Finn, A., Bagrade, L., Zhang, Q., Kolls, J. K., Srivastava, A., Lundgren, A., Forte, S., Thompson, C. M., Harney, K. F., Anderson, P. W., Lipsitch, M., Malley, R. (2008) Interleukin-17A mediates acquired immunity to pneumococcal colonization. PLoS Pathog. 4, e1000159.
79. Mikhak, Z., Farsidjani, A., Luster, A. D. (2009) Endotoxin augmented antigen-induced Th1 cell trafficking amplifies airway neutrophilic inflammation. J. Immunol. 182, 7946-7956.
80. Mennechet, F. J., Kasper, L. H., Rachinel, N., Li, W., Vandewalle, A., Buzoni-Gatel, D. (2002) Lamina propria CD4+ T lymphocytes synergize with murine intestinal epithelial cells to enhance proinflammatory response against an intracellular pathogen. J. Immunol. 168, 2988-2996. (Pubitemid 34211680)
81. Jovanovic, D. V., Di Battista, J. A., Martel-Pelletier, J., Jolicoeur, F. C., He, Y., Zhang, M., Mineau, F., Pelletier, J. P. (1998) IL-17 stimulates the production and expression of proinflammatory cytokines, IL-β and TNF-α, by human macrophages. J. Immunol. 160, 3513-3521. (Pubitemid 28164746)
82. Van Kooten, C., Boonstra, J. G., Paape, M. E., Fossiez, F., Banchereau, J., Lebecque, S., Bruijn, J. A., De Fijter, J. W., Van Es, L. A., Daha, M. R. (1998) Interleukin-17 activates human renal epithelial cells in vitro and is expressed during renal allograft rejection. J. Am. Soc. Nephrol. 9, 1526-1534.
83. Tartour, E., Fossiez, F., Joyeux, I., Galinha, A., Gey, A., Claret, E., Sastre-Garau, X., Couturier, J., Mosseri, V., Vives, V., Banchereau, J., Fridman, W. H., Wijdenes, J., Lebecque, S., Sautes-Fridman, C. (1999) Interleukin 17, a T-cell-derived cytokine, promotes tumorigenicity of human cervical tumors in nude mice. Cancer Res. 59, 3698-3704.
84. Sergejeva, S., Ivanov, S., Lotvall, J., Linden, A. (2005) Interleukin-17 as a recruitment and survival factor for airway macrophages in allergic airway inflammation. Am. J. Respir. Cell Mol. Biol. 33, 248-253.
85. Qiu, Z., Dillen, C., Hu, J., Verbeke, H., Struyf, S., Van Damme, J., Opdenakker, G. (2009) Interleukin-17 regulates chemokine and gelatinase B expression in fibroblasts to recruit both neutrophils and monocytes. Immunobiology 214, 835-842.
86. Cassatella, M. A., Bazzoni, F., Flynn, R. M., Dusi, S., Trinchieri, G., Rossi, F. (1990) Molecular basis of interferon-γ and lipopolysaccharide enhancement of phagocyte respiratory burst capability. Studies on the gene expression of several NADPH oxidase components. J. Biol. Chem. 265, 20241-20246.
87. Berton, G., Cassatella, M. A. (1992) Modulation of Neutrophil Functions by γ-Interferon. New York, NY, USA, Marcel Dekker, Inc.
88. Young, H. A., Hardy, K. J. (1995) Role of interferon-γ in immune cell regulation. J. Leukoc. Biol. 58, 373-381.
89. Ellis, T. N., Beaman, B. L. (2004) Interferon-γ activation of polymorphonuclear neutrophil function. Immunology 112, 2-12.
90. Colotta, F., Re, F., Polentarutti, N., Sozzani, S., Mantovani, A. (1992) Modulation of granulocyte survival and programmed cell death by cytokines and bacterial products. Blood 80, 2012-2020.
91. Dibbert, B., Weber, M., Nikolaizik, W. H., Vogt, P., Schoni, M. H., Blaser, K., Simon, H. U. (1999) Cytokine-mediated Bax deficiency and consequent delayed neutrophil apoptosis: a general mechanism to accumulate effector cells in inflammation. Proc. Natl. Acad. Sci. USA 96, 13330-13335.
92. Bettelli, E., Carrier, Y., Gao, W., Korn, T., Strom, T. B., Oukka, M., Weiner, H. L., Kuchroo, V. K. (2006) Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441, 235-238.
93. Veldhoen, M., Hocking, R. J., Atkins, C. J., Locksley, R. M., Stockinger, B. (2006) TGFβ in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 24, 179-189.
94. Higgins, S. C., Jarnicki, A. G., Lavelle, E. C., Mills, K. H. (2006) TLR4 mediates vaccine-induced protective cellular immunity to Bordetella pertussis: role of IL-17-producing T cells. J. Immunol. 177, 7980-7989.
95. Mathers, A. R., Janelsins, B. M., Rubin, J. P., Tkacheva, O. A., Shufesky, W. J., Watkins, S. C., Morelli, A. E., Larregina, A. T. (2009) Differential capability of human cutaneous dendritic cell subsets to initiate Th17 responses. J. Immunol. 182, 921-933.
96. Manicassamy, S., Ravindran, R., Deng, J., Oluoch, H., Denning, T. L., Kasturi, S. P., Rosenthal, K. M., Evavold, B. D., Pulendran, B. (2009) Toll-like receptor 2-dependent induction of vitamin A-metabolizing enzymes in dendritic cells promotes T regulatory responses and inhibits autoimmunity. Nat. Med. 15, 401-409.
97. Andreasen, C., Powell, D. A., Carbonetti, N. H. (2009) Pertussis toxin stimulates IL-17 production in response to Bordetella pertussis infection in mice. PLoS One 4, e7079.
98. Iezzi, G., Sonderegger, I., Ampenberger, F., Schmitz, N., Marsland, B. J., Kopf, M. (2009) CD40-CD40L cross-talk integrates strong antigenic signals and microbial stimuli to induce development of IL-17-producing CD4+ T cells. Proc. Natl. Acad. Sci. USA 106, 876-881.
99. Watford, W. T., Hissong, B. D., Bream, J. H., Kanno, Y., Muul, L., O'Shea, J. J. (2004) Signaling by IL-12 and IL-23 and the immunoregulatory roles of STAT4. Immunol. Rev. 202, 139-156.
100. Annunziato, F., Cosmi, L., Santarlasci, V., Maggi, L., Liotta, F., Mazzinghi, B., Parente, E., Fili, L., Ferri, S., Frosali, F., Giudici, F., Romagnani, P., Parronchi, P., Tonelli, F., Maggi, E., Romagnani, S. (2007) Phenotypic and functional features of human Th17 cells. J. Exp. Med. 204, 1849-1861.
101. Peck, A., Mellins, E. D. (2010) Plasticity of T-cell phenotype and function: the T helper type 17 example. Immunology 129, 147-153.
102. Brucklacher-Waldert, V., Steinbach, K., Lioznov, M., Kolster, M., Holscher, C., Tolosa, E. (2009) Phenotypical characterization of human Th17 cells unambiguously identified by surface IL-17A expression. J. Immunol. 183, 5494-5501.
103. O'Connor, R. A., Prendergast, C. T., Sabatos, C. A., Lau, C. W., Leech, M. D., Wraith, D. C., Anderton, S. M. (2008) Cutting edge: Th1 cells facilitate the entry of Th17 cells to the central nervous system during experimental autoimmune encephalomyelitis. J. Immunol. 181, 3750-3754.
104. Nasso, M., Fedele, G., Spensieri, F., Palazzo, R., Costantino, P., Rappuoli, R., Ausiello, C. M. (2009) Genetically detoxified pertussis toxin induces Th1/Th17 immune response through MAPKs and IL-10-dependent mechanisms. J. Immunol. 183, 1892-1899.
105. Zenaro, E., Donini, M., Dusi, S. (2009) Induction of Th1/Th17 immune response by Mycobacterium tuberculosis: role of dectin-1, mannose receptor, and DC-SIGN. J. Leukoc. Biol. 86, 1393-1401.
106. Shi, G., Cox, C. A., Vistica, B. P., Tan, C., Wawrousek, E. F., Gery, I. (2008) Phenotype switching by inflammation-inducing polarized Th17 cells, but not by Th1 cells. J. Immunol. 181, 7205-7213.
107. Lee, Y. K., Turner, H., Maynard, C. L., Oliver, J. R., Chen, D., Elson, C. O., Weaver, C. T. (2009) Late developmental plasticity in the T helper 17 lineage. Immunity 30, 92-107.
108. Bending, D., De La Pena, H., Veldhoen, M., Phillips, J.M., Uyttenhove, C., Stockinger, B., Cooke, A. (2009) Highly purified Th17 cells from BDC2.5NOD mice convert into Th1-like cells in NOD/SCID recipient mice. J. Clin. Invest. 119, 565-572.
109. Orgun, N. N., Mathis, M. A., Wilson, C. B., Way, S. S. (2008) Deviation from a strong Th1-dominated to a modest Th17-dominated CD4 T cell response in the absence of IL-12p40 and type I IFNs sustains protective CD8 T cells. J. Immunol. 180, 4109-4115.
110. Wozniak, T. M., Ryan, A. A., Britton, W. J. (2006) Interleukin-23 restores immunity to Mycobacterium tuberculosis infection in IL-12p40-deficient mice and is not required for the development of IL-17-secreting T cell responses. J. Immunol. 177, 8684-8692.
111. Paidipally, P., Periasamy, S., Barnes, P. F., Dhiman, R., Indramohan, M., Griffith, D. E., Cosman, D., Vankayalapati, R. (2009) NKG2D-dependent IL-17 production by human T cells in response to an intracellular pathogen. J. Immunol. 183, 1940-1945.
112. Umemura, M., Yahagi, A., Hamada, S., Begum, M. D., Watanabe, H., Kawakami, K., Suda, T., Sudo, K., Nakae, S., Iwakura, Y., Matsuzaki, G. (2007) IL-17-mediated regulation of innate and acquired immune response against pulmonary Mycobacterium bovis bacille Calmette-Guerin infection. J. Immunol. 178, 3786-3796. (Pubitemid 46417647)
113. Khader, S. A., Bell, G. K., Pearl, J. E., Fountain, J. J., Rangel-Moreno, J., Cilley, G. E., Shen, F., Eaton, S. M., Gaffen, S. L., Swain, S. L., Locksley, R. M., Haynes, L., Randall, T. D., Cooper, A. M. (2007) IL-23 and IL-17 in the establishment of protective pulmonary CD4+ T cell responses after vaccination and during Mycobacterium tuberculosis challenge. Nat. Immunol. 8, 369-377.
114. Scriba, T. J., Kalsdorf, B., Abrahams, D. A., Isaacs, F., Hofmeister, J., Black, G., Hassan, H. Y., Wilkinson, R. J., Walzl, G., Gelderbloem, S. J., Mahomed, H., Hussey, G. D., Hanekom, W. A. (2008) Distinct, specific IL-17- and IL-22-producing CD4+ T cell subsets contribute to the human anti-mycobacterial immune response. J. Immunol. 180, 1962-1970.
115. Schulz, S. M., Kohler, G., Holscher, C., Iwakura, Y., Alber, G. (2008) IL-17A is produced by Th17, γδ T cells and other CD4- lymphocytes during infection with Salmonella enterica serovar Enteritidis and has a mild effect in bacterial clearance. Int. Immunol. 20, 1129-1138.
116. Raffatellu, M., Santos, R. L., Verhoeven, D. E., George, M. D., Wilson, R. P., Winter, S. E., Godinez, I., Sankaran, S., Paixao, T. A., Gordon, M. A., Kolls, J. K., Dandekar, S., Baumler, A. J. (2008) Simian immunodeficiency virus-induced mucosal interleukin-17 deficiency promotes Salmonella dissemination from the gut. Nat. Med. 14, 421-428.
117. Wu, Q., Martin, R. J., Rino, J. G., Breed, R., Torres, R. M., Chu, H. W. (2007) IL-23-dependent IL-17 production is essential in neutrophil recruitment and activity in mouse lung defense against respiratory Mycoplasma pneumoniae infection. Microbes Infect. 9, 78-86. (Pubitemid 46149421)
118. Kleinschek, M. A., Muller, U., Brodie, S. J., Stenzel, W., Kohler, G., Blumenschein, W. M., Straubinger, R. K., McClanahan, T., Kastelein, R. A., Alber, G. (2006) IL-23 enhances the inflammatory cell response in Cryptococcus neoformans infection and induces a cytokine pattern distinct from IL-12. J. Immunol. 176, 1098-1106. (Pubitemid 43099711)
119. Pitta, M. G., Romano, A., Cabantous, S., Henri, S., Hammad, A., Kouriba, B., Argiro, L., el Kheir, M., Bucheton, B., Mary, C., El-Safi, S. H., Dessein, A. (2009) IL-17 and IL-22 are associated with protection against human kala azar caused by Leishmania donovani. J. Clin. Invest. 119, 2379-2387.
120. Romani, L. (2008) Cell mediated immunity to fungi: a reassessment. Med. Mycol. 46, 515-529.
121. Blair, C., Naclerio, R. M., Yu, X., Thompson, K., Sperling, A. (2005) Role of type 1 T helper cells in the resolution of acute Streptococcus pneumoniae sinusitis: a mouse model. J. Infect. Dis. 192, 1237-1244.
122. Mahon, B. P., Ryan, M. S., Griffin, F., Mills, K. H. (1996) Interleukin-12 is produced by macrophages in response to live or killed Bordetella pertussis and enhances the efficacy of an acellular pertussis vaccine by promoting induction of Th1 cells. Infect. Immun. 64, 5295-5301.
123. D'Elios, M. M., Manghetti, M., De Carli, M., Costa, F., Baldari, C. T., Burroni, D., Telford, J. L., Romagnani, S., Del Prete, G. (1997) T helper 1 effector cells specific for Helicobacter pylori in the gastric antrum of patients with peptic ulcer disease. J. Immunol. 158, 962-967. (Pubitemid 127492677)
124. Nakae, S., Komiyama, Y., Nambu, A., Sudo, K., Iwase, M., Homma, I., Sekikawa, K., Asano, M., Iwakura, Y. (2002) Antigen-specific T cell sensitization is impaired in IL-17-deficient mice, causing suppression of allergic cellular and humoral responses. Immunity 17, 375-387. (Pubitemid 35279557)
125. Bai, H., Cheng, J., Gao, X., Joyee, A. G., Fan, Y., Wang, S., Jiao, L., Yao, Z., Yang, X. (2009) IL-17/Th17 promotes type 1 T cell immunity against pulmonary intracellular bacterial infection through modulating dendritic cell function. J. Immunol. 183, 5886-5895.
126. Lin, Y., Ritchea, S., Logar, A., Slight, S., Messmer, M., Rangel-Moreno, J., Guglani, L., Alcorn, J. F., Strawbridge, H., Park, S. M., Onishi, R., Nyugen, N., Walter, M. J., Pociask, D., Randall, T. D., Gaffen, S. L., Iwakura, Y., Kolls, J. K., Khader, S. A. (2009) Interleukin-17 is required for T helper 1 cell immunity and host resistance to the intracellular pathogen Francisella tularensis. Immunity 31, 799-810.
127. Sanchez-Mejorada, G., Rosales, C. (1998) Signal transduction by immunoglobulin Fc receptors. J. Leukoc. Biol. 63, 521-533.
128. Repp, R., Valerius, T., Sendler, A., Gramatzki, M., Iro, H., Kalden, J. R., Platzer, E. (1991) Neutrophils express the high affinity receptor for IgG (Fc γ RI, CD64) after in vivo application of recombinant human granulocyte colony-stimulating factor. Blood 78, 885-889.
129. Ravetch, J. V., Bolland, S. (2001) IgG Fc receptors. Annu. Rev. Immunol. 19, 275-290.
130. Witko-Sarsat, V., Rieu, P., Descamps-Latscha, B., Lesavre, P., Halbwachs-Mecarelli, L. (2000) Neutrophils: molecules, functions and pathophysiological aspects. Lab. Invest. 80, 617-653.
131. Caron, E., Hall, A. (1998) Identification of two distinct mechanisms of phagocytosis controlled by different Rho GTPases. Science 282, 1717-1721. (Pubitemid 28549289)
132. Weiser, J. N., Naham, M. H. (2008) Immunity to extracellular bacteria. In Fundamental Immunology (W. E. Paul, ed.), Philadelphia, PA, USA, Lippincott Williams & Wilkins, 1182-1203.
133. Fillion, I., Ouellet, N., Simard, M., Bergeron, Y., Sato, S., Bergeron, M. G. (2001) Role of chemokines and formyl peptides in pneumococcal pneumonia-induced monocyte/macrophage recruitment. J. Immunol. 166, 7353-7361. (Pubitemid 32525611)
134. Bergeron, Y., Ouellet, N., Deslauriers, A. M., Simard, M., Olivier, M., Bergeron, M. G. (1998) Cytokine kinetics and other host factors in response to pneumococcal pulmonary infection in mice. Infect. Immun. 66, 912-922.
135. Standish, A. J., Weiser, J. N. (2009) Human neutrophils kill Streptococcus pneumoniae via serine proteases. J. Immunol. 183, 2602-2609.
136. Marriott, H. M., Ali, F., Read, R. C., Mitchell, T. J., Whyte, M. K., Dockrell, D. H. (2004) Nitric oxide levels regulate macrophage commitment to apoptosis or necrosis during pneumococcal infection. FASEB J. 18, 1126-1128. (Pubitemid 39561545)
137. Gordon, S. B., Irving, G. R., Lawson, R. A., Lee, M. E., Read, R. C. (2000) Intracellular trafficking and killing of Streptococcus pneumoniae by human alveolar macrophages are influenced by opsonins. Infect. Immun. 68, 2286-2293.
138. Liautard, J. P., Jubier-Maurin, V., Boigegrain, R. A., Kohler, S. (2006) Antimicrobials: targeting virulence genes necessary for intracellular multiplication. Trends Microbiol. 14, 109-113. (Pubitemid 43376048)
139. Wright, S. D., Silverstein, S. C. (1983) Receptors for C3b and C3bi promote phagocytosis but not the release of toxic oxygen from human phagocytes. J. Exp. Med. 158, 2016-2023.
140. Malik, Z. A., Denning, G. M., Kusner, D. J. (2000) Inhibition of Ca(2+) signaling by Mycobacterium tuberculosis is associated with reduced phagosome-lysosome fusion and increased survival within human macrophages. J. Exp. Med. 191, 287-302.
141. Morisaki, J. H., Heuser, J. E., Sibley, L. D. (1995) Invasion of Toxoplasma gondii occurs by active penetration of the host cell. J. Cell Sci. 108, 2457-2464.
142. Casadevall, A. (2008) Evolution of intracellular pathogens. Annu. Rev. Microbiol. 62, 19-33.
143. Grosset, J. (2003) Mycobacterium tuberculosis in the extracellular compartment: an underestimated adversary. Antimicrob. Agents Chemother. 47, 833-836.
144. Casadevall, A. (2003) Antibody-mediated immunity against intracellular pathogens: two-dimensional thinking comes full circle. Infect. Immun. 71, 4225-4228.
145. Casadevall, A., Pirofski, L. A. (2006) A reappraisal of humoral immunity based on mechanisms of antibody-mediated protection against intracellular pathogens. Adv. Immunol. 91, 1-44.
146. De Valliere, S., Abate, G., Blazevic, A., Heuertz, R. M., Hoft, D. F. (2005) Enhancement of innate and cell-mediated immunity by antimycobacterial antibodies. Infect. Immun. 73, 6711-6720.
147. MacGowan, A. P., Peterson, P. K., Keane, W., Quie, P. G. (1983) Human peritoneal macrophage phagocytic, killing, and chemiluminescent responses to opsonized Listeria monocytogenes. Infect. Immun. 40, 440-443.
148. Vahidy, R., Jehan, F. (1996) Enhanced in vitro engulfment of Listeria monocytogenes by rabbit polymorphonuclear leukocytes in the presence of sera from immune rabbits. FEMS Immunol. Med. Microbiol. 14, 103-107.
149. Barker, J. H., McCaffrey, R. L., Baman, N. K., Allen, L. A., Weiss, J.
150. Brieland, J. K., Heath, L. A., Huffnagle, G. B., Remick, D. G., McClain, M. S., Hurley, M. C., Kunkel, R. K., Fantone, J. C., Engleberg, C. (1996) Humoral immunity and regulation of intrapulmonary growth of Legionella pneumophila in the immunocompetent host. J. Immunol. 157, 5002-5008.
151. Mukherjee, S., Lee, S. C., Casadevall, A. (1995) Antibodies to Cryptococcus neoformans glucuronoxylomannan enhance antifungal activity of murine macrophages. Infect. Immun. 63, 573-579.
152. Zhong, Z., Pirofski, L. A. (1998) Antifungal activity of a human antiglucuronoxylomannan antibody. Clin. Diagn. Lab. Immunol. 5, 58-64.
153. Nosanchuk, J. D., Steenbergen, J. N., Shi, L., Deepe Jr., G. S., Casadevall, A. (2003) Antibodies to a cell surface histone-like protein protect against Histoplasma capsulatum. J. Clin. Invest. 112, 1164-1175.
154. Shi, L., Albuquerque, P. C., Lazar-Molnar, E., Wang, X., Santambrogio, L., Gacser, A., Nosanchuk, J. D. (2008) A monoclonal antibody to Histoplasma capsulatum alters the intracellular fate of the fungus in murine macrophages. Eukaryot. Cell 7, 1109-1117. (Pubitemid 351969325)
155. Barton, G. M. (2008) A calculated response: control of inflammation by the innate immune system. J. Clin. Invest. 118, 413-420.
156. Weiss, S. J. (1989) Tissue destruction by neutrophils. N. Engl. J. Med. 320, 365-376.
157. Owen, C. A., Campbell, E. J. (1999) The cell biology of leukocyte-mediated proteolysis. J. Leukoc. Biol. 65, 137-150.
158. Steinman, L. (2008) A rush to judgment on Th17. J. Exp. Med. 205, 1517-1522.
159. Peck, A., Mellins, E. D. (2009) Breaking old paradigms: Th17 cells in autoimmune arthritis. Clin. Immunol. 132, 295-304.
160. Brand, S. (2009) Crohn's disease: Th1, Th17 or both? The change of a paradigm: new immunological and genetic insights implicate Th17 cells in the pathogenesis of Crohn's disease. Gut 58, 1152-1167.
161. Cruz, A., Khader, S. A., Torrado, E., Fraga, A., Pearl, J. E., Pedrosa, J., Cooper, A. M., Castro, A. G. (2006) Cutting edge: IFN-γ regulates the induction and expansion of IL-17-producing CD4 T cells during mycobacterial infection. J. Immunol. 177, 1416-1420. (Pubitemid 44092473)
162. Khader, S. A., Cooper, A. M. (2008) IL-23 and IL-17 in tuberculosis. Cytokine 41, 79-83.
163. Cooper, A. M. (2009) Cell-mediated immune responses in tuberculosis. Annu. Rev. Immunol. 27, 393-422.
164. Bacellar, O., Faria, D., Nascimento, M., Cardoso, T. M., Gollob, K. J., Dutra, W. O., Scott, P., Carvalho, E. M. (2009) Interleukin 17 production among patients with American cutaneous leishmaniasis. J. Infect. Dis. 200, 75-78.
165. Allen, L. A., Beecher, B. R., Lynch, J. T., Rohner, O. V., Wittine, L. M. (2005) Helicobacter pylori disrupts NADPH oxidase targeting in human neutrophils to induce extracellular superoxide release. J. Immunol. 174, 3658-3667.
166. Algood, H. M., Gallo-Romero, J., Wilson, K. T., Peek Jr., R. M., Cover, T. L. (2007) Host response to Helicobacter pylori infection before initiation of the adaptive immune response. FEMS Immunol. Med. Microbiol. 51, 577-586.
167. Dannenberg Jr., A. M. (1994) Pathogenesis of pulmonary tuberculosis: an interplay of time-damaging and macrophage activating immune responses. Dual mechanisms that control bacillary multiplication. In Tuberculosis: Protection, Pathogenesis and Control (B. R. Bloom, ed.), Washington, DC, USA, American Society for Microbiology, 459-483.
168. Cooper, A. M., Adams, L. B., Dalton, D. K., Appelberg, R., Ehlers, S. (2002) IFN-γ and NO in mycobacterial disease: new jobs for old hands. Trends Microbiol. 10, 221-226. (Pubitemid 34327814)
169. Casadevall, A., Pirofski, L. A. (1999) Host-pathogen interactions: redefining the basic concepts of virulence and pathogenicity. Infect. Immun. 67, 3703-3713.
170. Silva, M. T. (2010) When two is better than one: macrophages and neutrophils work in concert in innate immunity as complementary and cooperative partners of a myeloid phagocyte system. J. Leukoc. Biol. 87, 93-106.
171. Akashi, K., Traver, D., Miyamoto, T., Weissman, I. L. (2000) A clonogenic common myeloid progenitor that gives rise to all myeloid lineages. Nature 404, 193-197. (Pubitemid 30154488)
172. Friedman, A. D. (2002) Transcriptional regulation of granulocyte and monocyte development. Oncogene 21, 3377-3390.