Characteristics of "Tip-DCs and MDSCs" and their potential role in leishmaniasis

Frontiers in Microbiology

Volumn 3, Issue MAR, 2012, Pages

  Schmid, Maximilian ^a   Wege, Anja K ^a   Ritter, Uwe ^a  

^a UNIVERSITY OF REGENSBURG   (Germany)

Author keywords

Dendritic cell; Langerhans cells; Leishmania parasites; Myeloid suppressor cell; Nitric oxide synthase

Indexed keywords

EID: 84863836962     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2012.00074     Document Type: Article

References (106)

1. Auffray, C., Sieweke, M. H., and Geiss-mann, R (2009). Blood mono-cytes: development, heterogeneity, and relationship with dendritic cells. Annu. Rev. Immunol. 27, 669-692.
2. Bauer, H., Jung, T., Tsikas, D., Stichtenoth, D. O., Frolich, J. C., and Neumann, C. (1997). Nitric oxide inhibits the secretion of T-helper 1- and T-helper 2-associated cytokines in activated human T cells. Immunology 90, 205-211.
3. Bingisser, R. M., Tilbrook, P. A., Holt, P. G., and Kees, U. R. (1998). Macrophage-derived nitric oxide regulates T cell activation via reversible disruption of the Jak3/STAT5 signaling pathway. J. Immunol. 160, 5729-5734.
4. Blank, C., Bogdan, C., Bauer, C., Erb, K., and Moll, H. (1996). Murine epidermal Langerhans cells do not express inducible nitric oxide synthase. Eur. J. Immunol. 26, 792-796.
5. Bogdan, C., Donhauser, N., Doring, R., Rollinghoff, M., Diefenbach, A., and Rittig, M. G. (2000). Fibroblasts as host cells in latent leishmaniosis. J. Exp.Med. 191, 2121-2130.
6. Bogdan, C., and Rollinghoff, M. (1998). The immune response to Leishma-nia: mechanisms of parasite control and evasion. Int. J. Parasitol. 28, 121-134.
7. Bonham, C. A., Lu, L., Li, Y., Hoffman, R. A., Simmons, R. L., and Thomson, A. W. (1996). Nitric oxide production by mouse bone marrow-derived dendritic cells: implications for the regulation of allogeneic T cell responses. Transplantation 62, 1871-1877.
8. Bosschaerts, T., Guilliams, M., Stijle-mans, B., Morias, Y., Engel, D., Tacke, F., Herin, M., De Baetse-lier, P., and Beschin, A. (2010). Tip-DC development during parasitic infection is regulated by IL-10 and requires CCL2/CCR2, IFN-gamma and MyD88 signaling. PLoS Pathog. 6, e1001045. doi:10.1371/journal.ppat.1001045.
9. Brewig, N., Kissenpfennig, A., Malissen, B., Veit, A., Bickert, T., Fleischer, B., Mostbock, S., and Ritter, U. (2009). Priming of CD8+ and CD4+ T cells in experimental leishmaniasis is initiated by different dendritic cell subtypes.J. Immunol. 182, 774-783.
10. Bronte, V., and Zanovello, P. (2005). Regulation of immune responses by L-arginine metabolism. Nat. Rev. Immunol. 5, 641-654.
11. Burnet, E M. (1976). A modification of Jerne's theory of antibody production using the concept of clonal selection. CA Cancer J. Clin. 26, 119-121.
12. Chong, S. Z., Wong, K. L., Lin, G., Yang, C. M., Wong, S. C., Angeli, V., Macary, P. A., and Kemeny, D. M. (2011). Human CD8 T cells drive Th1 responses through the differentiation of TNF/iNOS-producing dendritic cells. Eur. J. Immunol. 41, 1639-1651.
13. Colonna, M., Trinchieri, G., and Liu, Y. J. (2004). Plasmacytoid dendritic cells in immunity. Nat. Immunol. 5, 1219-1226.
14. Cuervo, H., Guerrero, N. A., Carba-josa, S., Beschin, A., De Baetse-lier, P., Girones, N., and Fresno, M. (2011). Myeloid-derived suppressor cells infiltrate the heart in acute Trypanosoma cruzi infection. J. Immunol. 187, 2656-2665.
15. Davison, A. M., and King, N. J. (2011). Accelerated dendritic cell differentiation from migrating Ly6C(lo) bone marrow monocytes in early dermal West Nile virus infection. J. Immunol. 186, 2382-2396.
16. De Trez, C., Magez, S., Akira, S., Ryf-fel, B., Carlier, Y., and Muraille, E. (2009). iNOS-producing inflammatory dendritic cells constitute the major infected cell type during the chronic Leishmania major infection phase of C57BL/6 resistant mice. PLoS Pathog. 5, e1000494. doi:10.1371/journal.ppat.1000494.
17. Diefenbach, A., Schindler, H., Donhauser, N., Lorenz, E., Laskay, T., Macmicking, J., Rollinghoff, M., Gresser, I., and Bogdan, C. (1998). Type 1 interferon (IFNalpha/beta) and type 2 nitric oxide synthase regulate the innate immune response to a protozoan parasite. Immunity 8, 77-87.
18. Dresing, P., Borkens, S., Kocur, M., Kropp, S., and Scheu, S. (2010). A fluorescence reporter model defines "Tip-DCs" as the cellular source of interferon beta in murine lis-teriosis. PLoS ONE 5, e15567. doi:10.1371/journal.pone.0015567.
19. Dupasquier, M., Stoitzner, P., Van Oudenaren, A., Romani, N., and Lee-nen, P. J. (2004). Macrophages and dendritic cells constitute a major subpopulation of cells in the mouse dermis. J. Invest. Dermatol. 123, 876-879.
20. Ezernitchi, A. V., Vaknin, I., Cohen-Daniel, L., Levy, O., Manaster, E., Halabi, A., Pikarsky, E., Shapira, L., and Baniyash, M. (2006). TCR zeta down-regulation under chronic inflammation is mediated by myeloid suppressor cells differentially distributed between various lymphatic organs. J. Immunol. 177, 4763-4772.
21. Fang, F. C., and Vazquez-Torres, A. (2002). Nitric oxide production by human macrophages: there's NO doubt about it. Am. J. Physiol Lung Cell. Mol. Physiol. 282, L941-L943.
22. Fogg, D. K., Sibon, C., Miled, C., Jung, S., Aucouturier, P., Littman, D. R., Cumano, A., and Geissmann, F. (2006). A clonogenic bone marrow progenitor specific for macrophages and dendritic cells. Science 311, 83-87.
23. Gabrilovich, D. I., and Nagaraj, S. (2009). Myeloid-derived suppressor cells as regulators of the immune system. Nat. Rev. Immunol. 9, 162-174.
24. Ginhoux, F., Tacke, F., Angeli, V., Bogunovic, M., Loubeau, M., Dai, X. M., Stanley, E. R., Randolph, G. J., and Merad, M. (2006). Langerhans cells arise from monocytes in vivo. Nat. Immunol. 7, 265-273.
25. Goni, O., Alcaide, P., and Fresno, M. (2002). Immunosuppression during acute Trypanosoma cruzi infection: involvement of Ly6G (Gr1(+))CD11b(+)immature myeloid suppressor cells. Int. Immunol. 14, 1125-1134.
26. Henderson, R. B., Hobbs, J. A., Math-ies, M., and Hogg, N. (2003). Rapid recruitment of inflammatory monocytes is independent of neutrophil migration. Blood 102, 328-335.
27. Huang, B., Pan, P. Y., Li, Q., Sato, A. I., Levy, D. E., Bromberg, J., Divino, C. M., and Chen, S. H. (2006). Gr-1+CD115+ immature myeloid suppressor cells mediate the development of tumor-induced T regulatory cells and T-cell anergy in tumor-bearing host. Cancer Res. 66, 1123-1131.
28. Hume, D. A. (2008). Macrophages as APC and the dendritic cell myth. J. Immunol. 181, 5829-5835.
29. Imhof, B. A., and Aurrand-Lions, M. (2004). Adhesion mechanisms regulating the migration of monocytes. Nat. Rev. Immunol. 4, 432-444.
30. Jimenez, F., Quinones, M. P., Martinez, H. G., Estrada, C. A., Clark, K., Gar-avito, E., Ibarra, J., Melby, P. C., and Ahuja, S. S. (2010). CCR2 plays a critical role in dendritic cell maturation: possible role of CCL2 and NF-ΚB. J. Immunol. 184, 5571-5581.
31. Katsnelson, A. (2006). Kicking off adaptive immunity: the discovery of dendritic cells. J. Exp. Med. 203, 1622.
32. Kautz-Neu, K., Noordegraaf, M., Dinges, S., Bennett, C. L., John, D., Clausen, B. E., and Von Stebut, E. (2011). Langerhans cells are negative regulators of the anti-Leishmania response. J. Exp. Med. 208, 885-891.
33. Kaye, P., and Scott, P. (2011). Leishmaniasis: complexity at the host-pathogen interface. Nat. Rev. Micro-biol. 9, 604-615.
34. Kusmartsev, S., Nefedova, Y., Yoder, D., and Gabrilovich, D. I. (2004). Antigen-specific inhibition of CD8+ T cell response by immature myeloid cells in cancer is mediated by reactive oxygen species. J. Immunol. 172, 989-999.
35. Kusmartsev, S. A., Li, Y., and Chen, S. H. (2000). Gr-1+ myeloid cells derived from tumor-bearing mice inhibit primary T cell activation induced through CD3/CD28 costimulation. J. Immunol. 165, 779-785.
36. Langhorne, J., Albano, F. R., Hensmann, M., Sanni, L., Cadman, E., Voi-sine, C., and Sponaas, A. M. (2004). Dendritic cells, pro-inflammatory responses, and antigen presentation in a rodent malaria infection. Immunol. Rev. 201, 35-47.
37. Larrick, J.W., Morhenn, V., Chiang, Y.L., and Shi, T. (1989). Activated Langerhans cells release tumor necrosis factor. J. Leukoc. Biol. 45, 429-433.
38. Leenen, P. J., De Bruijn, M. F., Voer-man, J. S., Campbell, P. A., and Van Ewijk, W (1994). Markers of mouse macrophage development detected by monoclonal antibodies. J. Immunol. Methods 174, 5-19.
39. Leon, B., and Ardavin, C. (2008). Mono-cyte migration to inflamed skin and lymph nodes is differentially controlled by L-selectin and PSGL-1. Blood 111, 3126-3130.
40. Leon, B., Lopez-Bravo, M., and Ardavin, C. (2007). Monocyte-derived dendritic cells formed at the infection site control the induction of protective T helper 1 responses against Leishmania. Immunity 26, 519-531.
41. Liese, J., Schleicher, U., and Bogdan, C. (2007). TLR9 signaling is essential for the innate NK cell response in murine cutaneous leishmaniasis. Eur. I Immunol. 37, 3424-3434.
42. Liu, K., Waskow, C., Liu, X., Yao, K., Hoh, J., andNussenzweig, M. (2007). Origin of dendritic cells in peripheral lymphoid organs of mice. Nat. Immunol. 8, 578-583.
43. Lowes, M. A., Chamian, F., Abello, M. V., Fuentes-Duculan, J., Lin, S. L., Nussbaum, R., Novitskaya, I., Carbonaro, H., Cardinale, I., Kikuchi, T., Gilleaudeau, P., Sullivan-Whalen, M., Wittkowski, K. M., Papp, K., Garovoy, M., Dummer, W., Steinman, R. M., and Krueger, J. G. (2005). Increase in TNF-alpha and inducible nitric oxide synthase-expressing dendritic cells in psoriasis and reduction with efalizumab (anti-CD11a). Proc. Natl. Acad. Sci. U.S.A. 102, 19057-19062.
44. Lu, L., Bonham, C. A., Chambers, E G., Watkins, S. C., Hoffman, R. A., Simmons, R. L., and Thomson, A. W. (1996). Induction of nitric oxide synthase in mouse dendritic cells by IFN-gamma, endotoxin, and interaction with allogeneic T cells: nitric oxide production is associated with dendritic cell apoptosis. J. Immunol. 157, 3577-3586.
45. Lutz, M. B., Kukutsch, N., Ogilvie, A. L., Rossner, S., Koch, F., Romani, N., and Schuler, G. (1999). An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J. Immunol. Methods 223, 77-92.
46. MacMicking, J., Xie, Q. W., and Nathan, C. (1997). Nitric oxide and macrophage function. Annu. Rev. Immunol. 15, 323-350.
47. Mattner, J., Wandersee-Steinhauser, A., Pahl, A., Rollinghoff, M., Majeau, G. R., Hochman, P. S., and Bogdan, C. (2004). Protection against progressive leishmaniasis by IFN-beta. J. Immunol. 172, 7574-7582.
48. McLellan, A. D., Kapp, M., Eggert, A., Linden, C., Bommhardt, U., Brocker, E. B., Kammerer, U., and Kamp-gen, E. (2002). Anatomic location and T-cell stimulatory functions of mouse dendritic cell subsets defined by CD4 and CD8 expression. Blood 99, 2084-2093.
49. Mencacci, A., Montagnoli, C., Bacci, A., Cenci, E., Pitzurra, L., Spreca, A., Kopf, M., Sharpe, A. H., and Romani, L. (2002). CD80+Gr-1+myeloid cells inhibit development of antifungal Th 1 immunity in mice with candidiasis. J. Immunol. 169, 3180-3190.
50. Merad, M., Ginhoux, F., and Collin, M. (2008). Origin, homeostasis and function of Langerhans cells and other langerin-expressing dendritic cells. Nat. Rev. Immunol. 8, 935-947.
51. Miller, M. J., Safrina, O., Parker, I., and Cahalan, M. D. (2004). Imaging the single cell dynamics of CD4+ T cell activation by dendritic cells in lymph nodes. J. Exp. Med. 200, 847-856.
52. Moreno, J. (2007). Changing views on Langerhans cell functions in leishmaniasis. Trends Parasitol. 23, 86-88.
53. Movahedi, K., Guilliams, M., Van Den Bossche, J., Van Den Bergh, R., Gysemans, C., Beschin, A., De Baetselier, P., and Van Ginder-achter, J. A. (2008). Identification of discrete tumor-induced myeloid-derived suppressor cell subpopula-tions with distinct T cell-suppressive activity. Blood 111, 4233-4244.
54. Munder, M., Eichmann, K., Moran, J. M., Centeno, F., Soler, G., and Mod-olell, M. (1999). Th1/Th2-regulated expression of arginase isoforms in murine macrophages and dendritic cells.J. Immunol. 163, 3771-3777.
55. Nagaraj, S., Gupta, K., Pisarev, V., Kinarsky, L., Sherman, S., Kang, L., Herber, D. L., Schneck, J., and Gabrilovich, D. I. (2007). Altered recognition of antigen is a mechanism of CD8+ T cell tolerance in cancer. Nat. Med. 13, 828-835.
56. Nakano, H., Yanagita, M., and Gunn, M. D. (2001). CD11c(+)B220(+)Gr-1(+) cells in mouse lymph nodes and spleen display characteristics of plasmacytoid dendritic cells. J. Exp. Med. 194, 1171-1178.
57. Okada, T., Lian, Z. X., Naiki, M., Ansari, A. A., Ikehara, S., and Gershwin, M. E. (2003). Murine thymic plasmacy toid dendritic cells. Eur. J. Immunol. 33, 1012-1019.
58. Olivier, M., Gregory, D. J., and Forget, G. (2005). Subversion mechanisms by which Leishmania parasites can escape the host immune response: a signaling point of view. Clin. Microbiol. Rev. 18, 293-305.
59. Palucka, A. K., and Banchereau, J. (2006). Langerhans cells: daughters of monocytes. Nat. Immunol. 7, 223-224.
60. Pereira, W. F., Ribeiro-Gomes, E L., Guillermo, L. V., Vellozo, N. S., Mon-talvao, F., Dosreis, G. A., and Lopes, M. F. (2011). Myeloid-derived suppressor cells help protective immunity to Leishmania major infection despite suppressed T cell responses. J. Leukoc. Biol. 90, 1191-1197.
61. Peters, N. C., Egen, J. G., Secundino, N., Debrabant, A., Kimblin, N., Kamhawi, S., Lawyer, P., Fay, M. P., Germain, R. N., and Sacks, D. (2008). In vivo imaging reveals an essential role for neutrophils in leishmaniasis transmitted by sand flies. Science 321, 970-974.
62. Rappolee, D. A., and Werb, Z. (1988). Secretory products of phagocytes. Curr. Opin. Immunol. 1, 47-55.
63. Ren, G., Su, J., Zhao, X., Zhang, L., Zhang, J., Roberts, A. I., Zhang, H., Das, G., and Shi, Y. (2008). Apop-totic cells induce immunosuppres-sion through dendritic cells: critical roles of IFN-gamma and nitric oxide. J. Immunol. 181, 3277-3284.
64. Ritter, U., Frischknecht, F., and Van Zandbergen, G. (2009). Are neutrophils important host cells for Leishmania parasites? Trends Parasitol. 25, 505-510.
65. Ritter, U., and Korner, H. (2002). Divergent expression of inflammatory dermal chemokines in cutaneous leishmaniasis. Parasite Immunol. 24, 295-301.
66. Ritter, U., Lechner, A., Scharl, K., Kia-fard, Z., Zwirner, J., and Korner, H. (2008). TNF controls the infiltration of dendritic cells into the site of Leishmania major infection. Med. Microbiol. Immunol. 197, 29-37.
67. Ritter, U., Meissner, A., Ott, J., and Korner, H. (2003). Analysis of the maturation process of dendritic cells deficient for TNF and lymphotoxin-alpha reveals an essential role for TNF. J. Leukoc. Biol. 74, 216-222.
68. Ritter, U., and Moll, H. (2000). Mono-cyte chemotactic protein-1 stimulates the killing of Leishmania major by human monocytes, acts syn-ergistically with IFN-gamma and is antagonized by IL-4. Eur. J. Immunol. 30, 3111-3120.
69. Ritter, U., Moll, H., Laskay, T., Brocker, E., Velazco, O., Becker, I., and Gillitzer, R. (1996). Differential expression of chemokines in patients with localized and diffuse cutaneous American leishmaniasis. J. Infect. Dis. 173, 699-709.
70. Ritter, U., and Osterloh, A. (2007). A new view on cutaneous dendritic cell subsets in experimental leishmaniasis. Med. Microbiol. Immunol. 196, 51-59.
71. Rivoltini, L., Carrabba, M., Huber, V., Castelli, C., Novellino, L., Dalerba, P., Mortarini, R., Arancia, G., Ani-chini, A., Fais, S., and Parmiani, G. (2002). Immunity to cancer: attack and escape in T lymphocyte-tumor cell interaction. Immunol. Rev. 188, 97-113.
72. Rodriguez, P. C., Hernandez, C. P., Quiceno, D., Dubinett, S. M., Zabaleta, J., Ochoa, J. B., Gilbert, J., and Ochoa, A. C. (2005). Arginase I in myeloid suppressor cells is induced by COX-2 in lung carcinoma. J. Exp. Med. 202, 931-939.
73. Rodriguez, P. C., and Ochoa, A. C. (2008). Arginine regulation by myeloid derived suppressor cells and tolerance in cancer: mechanisms and therapeutic perspectives. Immunol. Rev. 222, 180-191.
74. Rodriguez, P. C., Quiceno, D. G., and Ochoa, A. C. (2007). L-arginine availability regulates T-lymphocyte cell-cycle progression. Blood 109, 1568-1573.
75. Romani, N., Clausen, B. E., and Stoitzner, P. (2010). Langerhans cells and more: langerin-expressing dendritic cell subsets in the skin. Immunol. Rev. 234, 120-141.
76. Sakaguchi, S. (2011). Regulatory T cells: history and perspective. Methods Mol. Biol. 707, 3-17.
77. Schleicher, U., Liese, J., Knippertz, I., Kurzmann, C., Hesse, A., Heit, A., Fischer, J. A., Weiss, S., Kalinke, U., Kunz, S., and Bogdan, C. (2007). NK cell activation in visceral leishmaniasis requires TLR9, myeloid DCs, and IL-12, but is independent of plasmacytoid DCs. J. Exp. Med. 204, 893-906.
78. Schmielau, J., and Finn, O. J. (2001). Activated granulocytes and granulocyte-derived hydrogen peroxide are the underlying mechanism of suppression of T-cell function in advanced cancer patients. Cancer Res. 61, 4756-4760.
79. Segura, E., Wong, J., and Villadan-gos, J. A. (2009). Cutting edge: B220+CCR9- dendritic cells are not plasmacytoid dendritic cells but are precursors of conventional dendritic cells. J. Immunol. 183, 1514-1517.
80. Serafini, P., Mgebroff, S., Noonan, K., and Borrello, I. (2008). Myeloid-derived suppressor cells promote cross-tolerance in B-cell lymphoma by expanding regulatory T cells. Cancer Res. 68, 5439-5449.
81. Serbina, N. V., and Pamer, E. G. (2006). Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR2. Nat. Immunol. 7, 311-317.
82. Serbina, N. V., Salazar-Mather, T. P., Biron, C. A., Kuziel, W. A., and Pamer, E. G. (2003). TNF/iNOS-producing dendritic cells mediate innate immune defense against bacterial infection. Immunity 19, 59-70.
83. Shortman, K., and Liu, Y. J. (2002). Mouse and human dendritic cell subtypes. Nat. Rev. Immunol. 2, 151-161.
84. Solodova, E., Jablonska, J., Weiss, S., and Lienenklaus, S. (2011). Production of IFN-beta during Lis-teria monocytogenes infection is restricted to monocyte/macrophage lineage. PLoS ONE 6, e18543. doi: 10.1371/journal.pone.00 18543.
85. Steinman, R. M., and Cohn, Z. A. (1973). Identification of a novel cell type in peripheral lymphoid organs of mice. I. Morphology, quantita-tion, tissue distribution. J. Exp. Med. 137, 1142-1162.
86. Stoll, S., Delon, J., Brotz, T. M., and Germain, R. N. (2002). Dynamic imaging of T cell-dendritic cell interactions in lymph nodes. Science 296, 1873-1876.
87. Strober, S. (1984). Natural suppressor (NS) cells, neonatal tolerance, and total lymphoid irradiation: exploring obscure relationships. Annu. Rev. Immunol. 2, 219-237.
88. Sugita, K., Kabashima, K., Yoshiki, R., Ikenouchi-Sugita, A., Tsutsui, M., Nakamura, J., Yanagihara, N., and Tokura, Y. (2010). Inducible nitric oxide synthase downmodulates contact hypersensitivity by suppressing dendritic cell migration and survival. J. Invest. Dermatol. 130, 464-471.
89. Sunderkotter, C., Nikolic, T., Dillon, M. J., Van Rooijen, N., Stehling, M., Drevets, D. A., and Leenen, P. J. (2004). Subpopulations of mouse blood monocytes differ in maturation stage and inflammatory response. J. Immunol. 172, 4410-4417.
90. Szuster-Ciesielska, A., Hryciuk-Umer, E., Stepulak, A., Kupisz, K., and Kandefer-Szerszen, M. (2004). Reactive oxygen species production by blood neutrophils of patients with laryngeal carcinoma and antioxidative enzyme activity in their blood. Acta Oncol. 43, 252-258.
91. Tam, M. A., and Wick, M.J. (2006). Differential expansion, activation and effector functions of conventional and plasmacytoid dendritic cells in mouse tissues transiently infected with Listeria monocytogenes. Cell. Microbiol. 8, 1172-1187.
92. Taylor, P. R., Martinez-Pomares, L., Stacey, M., Lin, H. H., Brown, G. D., and Gordon, S. (2005). Macrophage receptors and immune recognition. Annu. Rev. Immunol. 23, 901-944.
93. Turley, S. J., Fletcher, A. L., and Elpek, K. G. (2010). The stromal and haematopoietic antigen-presenting cells that reside in secondary lymphoid organs. Nat. Rev. Immunol. 10, 813-825.
94. Umemura, N., Saio, M., Suwa, T., Kitoh, Y., Bai, J., Nonaka, K., Ouyang, G. E, Okada, M., Balazs, M., Adany, R., Shibata, T., and Takami, T. (2008). Tumor-infiltrating myeloid-derived suppressor cells are pleiotropic-inflamed monocytes/macrophages that bear M1- and M2-type characteristics. J. Leukoc. Biol. 83, 1136-1144.
95. Virna, S., Deckert, M., Lutjen, S., Soltek, S., Foulds, K. E., Shen, H., Korner, H., Sedgwick, J. D., and Schluter, D. (2006). TNF is important for pathogen control and limits brain damage in murine cerebral listerio-sis. J. Immunol. 177, 3972-3982.
96. Vremec, D. (2010). The isolation of mouse dendritic cells from lymphoid tissues and the identification of dendritic cell subtypes by multi-parameter flow cytometry. Methods Mol. Biol. 595, 205-229.
97. Waskow, C., Liu, K., Darrasse-Jeze, G., Guermonprez, P., Ginhoux, F., Merad, M., Shengelia, T., Yao, K., and Nussenzweig, M. (2008). The receptor tyrosine kinase Flt3 is required for dendritic cell development in peripheral lymphoid tissues. Nat. Immunol. 9, 676-683.
98. Watanabe, S., Deguchi, K., Zheng, R., Tamai, H., Wang, L. X., Cohen, P. A., and Shu, S. (2008). Tumor-induced CD11b+Gr-1+ myeloid cells suppress T cell sensitization in tumor-draining lymph nodes. J. Immunol. 181, 3291-3300.
99. Wenzel, U. A., Bank, E., Florian, C., Forster, S., Zimara, N., Steinacker, J., Klinger, M., Reiling, N., Rit-ter, U., and Van Zandbergen, G. (2011). Leishmania major parasite stage-dependent host cell invasion and immune evasion. FASEB J. 26, 29-39.
100. Wilhelm, P., Ritter, U., Labbow, S., Don-hauser, N., Rollinghoff, M., Bog-dan, C., and Korner, H. (2001). Rapidly fatal leishmaniasis in resistant C57BL/6 mice lacking TNF. J. Immunol. 166, 4012-4019.
101. Wilkins-Rodriguez, A. A., Escalona-Montano, A. R., Aguirre-Garcia, M., Becker, I., and Gutierrez-Kobeh, L. (2010). Regulation of the expression of nitric oxide synthase by Leishmania mexicana amastigotes in murine dendritic cells. Exp. Parasitol. 126, 426-434.
102. Will, A., Blank, C., Rollinghoff, M., and Moll, H. (1992). Murine epidermal Langerhans cells are potent stimulators of an antigen-specific T cell response to Leishmania major, the cause of cutaneous leishmaniasis. Eur. J. Immunol. 22, 1341-1347.
103. Yona, S., and Jung, S. (2010). Monocytes: subsets, origins, fates and functions. Curr. Opin. Hematol. 17, 53-59.
104. Youn, J. I., Collazo, M., Shalova, I. N., Biswas, S. K., and Gabrilovich, D. I. (2011). Characterization of the nature of granulocytic myeloid-derived suppressor cells in tumor-bearing mice. J. Leukoc. Biol. 91, 167-181.
105. Youn, J. I., Nagaraj, S., Collazo, M., and Gabrilovich, D. I. (2008). Subsets of myeloid-derived suppressor cells in tumor-bearing mice. J. Immunol. 181, 5791-5802.
106. Zhu, B., Bando, Y., Xiao, S., Yang, K., Anderson, A. C., Kuchroo, V K., and Khoury, S. J. (2007). CD11b+Ly-6C(hi) suppressive monocytes in experimental autoimmune encephalomyelitis. J. Immunol. 179, 5228-5237.