CD11c identifies a subset of murine liver natural killer cells that responds to adenoviral hepatitis

Journal of Leukocyte Biology

Volumn 84, Issue 4, 2008, Pages 1039-1046

  Burt, Bryan M ^a   Plitas, George ^a   Stableford, Jennifer A ^a   Nguyen, Hoang M ^a   Bamboat, Zubin M ^a   Pillarisetty, Venu G ^a   DeMatteo, Ronald P ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

Adenovirus; Dendritic cells; Hepatic; IFN ; Toll like receptor 9

Indexed keywords

GAMMA INTERFERON; GLYCOPROTEIN P 15095; INTERLEUKIN 12; INTERLEUKIN 18; TOLL LIKE RECEPTOR 9;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL FUNCTION; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOKINE PRODUCTION; HEPATITIS; IMMUNOCOMPETENT CELL; INNATE IMMUNITY; LIVER; LYSIS; MALE; MOUSE; NATURAL KILLER CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL;

ADENOVIRIDAE; ADENOVIRIDAE INFECTIONS; ANIMALS; ANTIGENS, CD11C; HEPATITIS, VIRAL, ANIMAL; INTERFERON TYPE II; INTERLEUKIN-12; INTERLEUKIN-18; KILLER CELLS, NATURAL; LIVER; MICE; TOLL-LIKE RECEPTOR 9;

ADENOVIRIDAE; ANIMALIA; MURINAE;

EID: 54249122236     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0408256     Document Type: Article

References (48)

1. Liu, Z. X., Govindarajan, S., Okamoto, S., Dennert, G. (2000) NK cells cause liver injury and facilitate the induction of T cell-mediated immunity to a viral liver infection. J. Immunol. 164, 6480-6486.
2. Yang, Y., Xiang, Z., Ertl, H. C., Wilson, J. M. (1995) Upregulation of class I major histocompatibility complex antigens by interferon γ is necessary for T-cell-mediated elimination of recombinant adenovirus-infected hepatocytes in vivo. Proc. Natl. Acad. Sci. USA 92, 7257-7261.
3. Biron, C. A., Nguyen, K. B., Pien, G. C., Cousens, L. P., Salazar-Mather, T. P. (1999) Natural killer cells in antiviral defense: function and regulation by innate cytokines. Annu. Rev. Immunol. 17, 189-220.
4. Heise, M. T., Virgin, H. W. (1995) The T-cell-independent role of γ interferon and tumor necrosis factor α in macrophage activation during murine cytomegalovirus and herpes simplex virus infections. J. Virol. 69, 904-909.
5. Novelli, F., Casanova, J. L. (2004) The role of IL-12, IL-23 and IFN-γ in immunity to viruses. Cytokine Growth Factor Rev. 15, 367-377.
6. Orange, J. S., Biron, C. A. (1996) An absolute and restricted requirement for IL-12 in natural killer cell IFN-γ production and antiviral defense. Studies of natural killer and T cell responses in contrasting viral infections. J. Immunol. 156, 1138-1142.
7. Orange, J. S., Wang, B., Terhorst, C., Biron, C. A. (1995) Requirement for natural killer cell-produced interferon γ in defense against murine cytomegalovirus infection and enhancement of this defense pathway by interleukin 12 administration. J. Exp. Med. 182, 1045-1056.
8. Tay, C. H., Welsh, R. M. (1997) Distinct organ-dependent mechanisms for the control of murine cytomegalovirus infection by natural killer cells. J. Virol. 71, 267-275.
9. Peng, Y., Falck-Pedersen, E., Elkon, K. B. (2001) Variation in adenovirus transgene expression between BALB/c and C57BL/6 mice is associated with differences in interleukin-12 and γ interferon production and NK cell activation. J. Virol. 75, 4540-4550.
10. Chen, J., Zajac, A. J., McPherson, S. A., Hsu, H. C., Yang, P., Wu, Q., Xu, X., Wang, X., Fujihashi, K., Curiel, D. T., Mountz, J. D. (2005) Primary adenovirus-specific cytotoxic T lymphocyte response occurs after viral clearance and liver enzyme elevation. Gene Ther. 12, 1079-1088.
11. Gregoire, C., Chasson, L., Luci, C., Tomasello, E., Geissmann, F., Vivier, E., Walzer, T. (2007) The trafficking of natural killer cells. Immunol. Rev. 220, 169-182.
12. Pien, G. C., Satoskar, A. R., Takeda, K., Akira, S., Biron, C. A. (2000) Cutting edge: selective IL-18 requirements for induction of compartmental IFN-γ responses during viral infection. J. Immunol. 165, 4787-4791.
13. Xing, Z., Zganiacz, A., Wang, J., Divangahi, M., Nawaz, F. (2000) IL-12-independent Th1-type immune responses to respiratory viral infection: requirement of IL-18 for IFN-γ release in the lung but not for the differentiation of viral-reactive Th1-type lymphocytes. J. Immunol. 164, 2575-2584.
14. Nociari, M., Ocheretina, O., Schoggins, J. W., Falck-Pedersen, E. (2007) Sensing infection by adenovirus: Toll-like receptor-independent viral DNA recognition signals activation of the interferon regulatory factor 3 master regulator. J. Virol. 81, 4145-4157.
15. Zhu, J., Huang, X., Yang, Y. (2007) Innate immune response to adenoviral vectors is mediated by both Toll-like receptor-dependent and -independent pathways. J. Virol. 81, 3170-3180.
16. Hemmi, H., Takeuchi, O., Kawai, T., Kaisho, T., Sato, S., Sanjo, H., Matsumoto, M., Hoshino, K., Wagner, H., Takeda, K., Akira, S. (2000) A Toll-like receptor recognizes bacterial DNA. Nature 408, 740-745.
17. Pillarisetty, V. G., Shah, A. B., Miller, G., Bleier, J. I., DeMatteo, R. P. (2004) Liver dendritic cells are less immunogenic than spleen dendritic cells because of differences in subtype composition. J. Immunol. 172, 1009-1017.
18. Pillarisetty, V. G., Katz, S. C., Bleier, J. I., Shah, A. B., Dematteo, R. P. (2005) Natural killer dendritic cells have both antigen presenting and lytic function and in response to CpG produce IFN-γ via autocrine IL-12. J. Immunol. 174, 2612-2618.
19. Kim, S., Iizuka, K., Kang, H. S., Dokun, A., French, A. R., Greco, S., Yokoyama, W. M. (2002) In vivo developmental stages in murine natural killer cell maturation. Nat. Immunol. 3, 523-528.
20. Trinite, B., Voisine, C., Yagita, H., Josien, R. (2000) A subset of cytolytic dendritic cells in rat. J. Immunol. 165, 4202-4208.
21. Kataoka, T., Shinohara, N., Takayama, H., Takaku, K., Kondo, S., Yonehara, S., Nagai, K. (1996) Concanamycin A, a powerful tool for characterization and estimation of contribution of perforin- and Fas-based lytic pathways in cell-mediated cytotoxicity. J. Immunol. 156, 3678-3686.
22. Moretta, A., Bottino, C., Mingari, M. C., Biassoni, R., Moretta, L. (2002) What is a natural killer cell? Nat. Immunol. 3, 6-8.
23. Takeda, K., Cretney, E., Hayakawa, Y., Ota, T., Akiba, H., Ogasawara, K., Yagita, H., Kinoshita, K., Okumura, K., Smyth, M. J. (2005) TRAIL identifies immature natural killer cells in newborn mice and adult mouse liver. Blood 105, 2082-2089.
24. Takeda, K., Hayakawa, Y., Smyth, M. J., Kayagaki, N., Yamaguchi, N., Kakuta, S., Iwakura, Y., Yagita, H., Okumura, K. (2001) Involvement of tumor necrosis factor-related apoptosis-inducing ligand in surveillance of tumor metastasis by liver natural killer cells. Nat. Med. 7, 94-100.
25. Tu, Z., Bozorgzadeh, A., Crispe, I. N., Orloff, M. S. (2007) The activation state of human intrahepatic lymphocytes. Clin. Exp. Immunol. 149, 186-193.
26. Vermijlen, D., Luo, D., Froelich, C. J., Medema, J. P., Kummer, J. A., Willems, E., Braet, F., Wisse, E. (2002) Hepatic natural killer cells exclusively kill splenic/blood natural killer-resistant tumor cells by the perforin/granzyme pathway. J. Leukoc. Biol. 72, 668-676.
27. Ishiyama, K., Ohdan, H., Ohira, M., Mitsuta, H., Arihiro, K., Asahara, T. (2006) Difference in cytotoxicity against hepatocellular carcinoma between liver and periphery natural killer cells in humans. Hepatology 43, 362-372.
28. Jomantaite, I., Dikopoulos, N., Kroger, A., Leithauser, F., Hauser, H., Schirmbeck, R., Reimann, J. (2004) Hepatic dendritic cell subsets in the mouse. Eur. J. Immunol. 34, 355-365.
29. Lian, Z. X., Okada, T., He, X. S., Kita, H., Liu, Y. J., Ansari, A. A., Kikuchi, K., Ikehara, S., Gershwin, M. E. (2003) Heterogeneity of dendritic cells in the mouse liver: identification and characterization of four distinct populations. J. Immunol. 170, 2323-2330.
30. Hensley, S. E., Amalfitano, A. (2007) Toll-like receptors impact on safety and efficacy of gene transfer vectors. Mol. Ther. 15, 1417-1422.
31. Chaudhry, U. I., Kingham, T. P., Plitas, G., Katz, S. C., Raab, J. R., DeMatteo, R. P. (2006) Combined stimulation with interleukin-18 and CpG induces murine natural killer dendritic cells to produce IFN-γ and inhibit tumor growth. Cancer Res. 66, 10497-10504.
32. Welner, R. S., Pelayo, R., Garrett, K. P., Chen, X., Perry, S. S., Sun, X. H., Kee, B. L., Kincade, P. W. (2007) Interferon-producing killer dendritic cells (IKDC) arise via a unique differentiation pathway from primitive c-kitHiCD62L+ lymphoid progenitors. Blood 109, 4825-4831.
33. Roncarolo, M. G., Bigler, M., Haanen, J. B., Yssel, H., Bacchetta, R., de Vries, J. E., Spits, H. (1991) Natural killer cell clones can efficiently process and present protein antigens. J. Immunol. 147, 781-787.
34. Hanna, J., Gonen-Gross, T., Fitchett, J., Rowe, T., Daniels, M., Arnon, T. I., Gazit, R., Joseph, A., Schjetne, K. W., Steinle, A., Porgador, A., Mevorach, D., Goldman-Wohl, D., Yagel, S., LaBarre, M. J., Buckner, J. H., Mandelboim, O. (2004) Novel APC-like properties of human NK cells directly regulate T cell activation. J. Clin. Invest. 114, 1612-1623.
35. Zingoni, A., Sornasse, T., Cocks, B. G., Tanaka, Y., Santoni, A., Lanier, L. L. (2004) Cross-talk between activated human NK cells and CD4+ T cells via OX40-OX40 ligand interactions. J. Immunol. 173, 3716-3724.
36. Fanger, N. A., Maliszewski, C. R., Schooley, K., Griffith, T. S. (1999) Human dendritic cells mediate cellular apoptosis via tumor necrosis factor-related apoptosis-inducing ligand (TRAIL). J. Exp. Med. 190, 1155-1164.
37. Schmitz, M., Zhao, S., Deuse, Y., Schakel, K., Wehner, R., Wohner, H., Holig, K., Wienforth, F., Kiessling, A., Bornhäuser, M., Temme, A., Rieger, M. A., Weigle, B., Bachmann, M., Rieber, E. P. (2005) Tumoricidal potential of native blood dendritic cells: direct tumor cell killing and activation of NK cell-mediated cytotoxicity. J. Immunol. 174, 4127-4134.
38. Stary, G., Bangert, C., Tauber, M., Strohal, R., Kopp, T., Stingl, G. (2007) Tumoricidal activity of TLR7/8-activated inflammatory dendritic cells. J. Exp. Med. 204, 1441-1451.
39. Chaperot, L., Blum, A., Manches, O., Lui, G., Angel, J., Molens, J. P., Plumas, J. (2006) Virus or TLR agonists induce TRAIL-mediated cytotoxic activity of plasmacytoid dendritic cells. J. Immunol. 176, 248-255.
40. Hardy, A. W., Graham, D. R., Shearer, G. M., Herbeuval, J. P. (2007) HIV turns plasmacytoid dendritic cells (pDC) into TRAIL-expressing killer pDC and down-regulates HIV coreceptors by Toll-like receptor 7-induced IFN-α. Proc. Natl. Acad. Sci. USA 104, 17453-17458.
41. Janjic, B. M., Lu, G., Pimenov, A., Whiteside, T. L., Storkus, W. J., Vujanovic, N. L. (2002) Innate direct anticancer effector function of human immature dendritic cells. I. Involvement of an apoptosis-inducing pathway. J. Immunol. 168, 1823-1830.
42. Huleatt, J. W., Lefrancois, L. (1995) Antigen-driven induction of CD11c on intestinal intraepithelial lymphocytes and CD8+ T cells in vivo. J. Immunol. 154, 5684-5693.
43. Lin, Y., Roberts, T. J., Sriram, V., Cho, S., Brutkiewicz, R. R. (2003) Myeloid marker expression on antiviral CD8+ T cells following an acute virus infection. Eur. J. Immunol. 33, 2736-2743.
44. Chaudhry, U. I., Katz, S. C., Kingham, T. P., Pillarisetty, V. G., Raab, J. R., Shah, A. B., DeMatteo, R. P. (2006) In vivo overexpression of Flt3 ligand expands and activates murine spleen natural killer dendritic cells. FASEB J. 20, 982-984.
45. Chan, C. W., Crafton, E., Fan, H. N., Flook, J., Yoshimura, K., Skarica, M., Brockstedt, D., Dubensky, T. W., Stins, M. F., Lanier, L. L., Pardoll, D. M., Housseau, F. (2006) Interferon-producing killer dendritic cells provide a link between innate and adaptive immunity. Nat. Med. 12, 207-213.
46. Chen, L., Calomeni, E., Wen, J., Ozato, K., Shen, R., Gao, J. X. (2007) Natural killer dendritic cells are an intermediate of developing dendritic cells. J. Leukoc. Biol. 81, 1422-1433.
47. Vosshenrich, C. A., Lesjean-Pottier, S., Hasan, M., Richard-Le Goff, O., Corcuff, E., Mandelboim, O., Di Santo, J. P. (2007) CD11cloB220+ interferon-producing killer dendritic cells are activated natural killer cells. J. Exp. Med. 204, 2569-2578.
48. Caminschi, I., Ahmet, F., Heger, K., Brady, J., Nutt, S. L., Vremec, D., Pietersz, S., Lahoud, M. H., Schofield, L., Hansen, D. S., O'Keeffe, M., Smyth, M. J., Bedoui, S., Davey, G. M., Villadangos, J. A., Heath, W. R., Shortman, K. (2007) Putative IKDCs are functionally and developmentally similar to natural killer cells, but not to dendritic cells. J. Exp. Med. 204, 2579-2590.