The MyD88 pathway in plasmacytoid and CD4+ dendritic cells primarily triggers type I IFN production against measles virus in a mouse infection model

Journal of Immunology

Volumn 191, Issue 9, 2013, Pages 4740-4747

  Takaki, Hiromi ^a   Takeda, Makoto ^b   Tahara, Maino ^b   Shingai, Masashi ^a,c   Oshiumi, Hiroyuki ^a   Matsumoto, Misako ^a   Seya, Tsukasa ^a  

^a HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; ALPHA INTERFERON RECEPTOR; ALPHA4 INTERFERON; BETA INTERFERON; CD150 ANTIGEN; CD19 ANTIGEN; CD4 ANTIGEN; CD8ALPHA ANTIGEN; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GLYCOPROTEIN P 15095; INTERFERON; MESSENGER RNA; MITOCHONDRIAL ANTIVIRAL SIGNALING PROTEIN; MITOCHONDRIAL PROTEIN; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR 7; UNCLASSIFIED DRUG; ALPHA BETA INTERFERON RECEPTOR; CD8 ANTIGEN; CELL SURFACE RECEPTOR; IFNAR1 PROTEIN, MOUSE; IPS-1 PROTEIN, MOUSE; LEUKOCYTE ANTIGEN; MYD88 PROTEIN, MOUSE; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL ISOLATION; CELL PROTECTION; CELLULAR IMMUNITY; CONTROLLED STUDY; CXCL10 GENE; CYTOKINE PRODUCTION; CYTOKINE RELEASE; GENE; GENE EXPRESSION REGULATION; IFIT1 GENE; IFN B GENE; IN VITRO STUDY; IN VIVO STUDY; MEASLES; MEASLES VIRUS; MOUSE; NONHUMAN; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SPLEEN CELL; TRANSGENIC MOUSE; UPREGULATION; VIRUS REPLICATION; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL CULTURE; CYTOLOGY; DENDRITIC CELL; DISEASE MODEL; GENETICS; HUMAN; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; SPLEEN; T LYMPHOCYTE; VIROLOGY;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ANTIGENS, CD; ANTIGENS, CD4; ANTIGENS, CD8; B-LYMPHOCYTES; CELLS, CULTURED; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; HUMANS; INTERFERON TYPE I; MEASLES; MEASLES VIRUS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYELOID DIFFERENTIATION FACTOR 88; RECEPTOR, INTERFERON ALPHA-BETA; RECEPTORS, CELL SURFACE; SPLEEN; T-LYMPHOCYTES;

EID: 84884942143     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1301744     Document Type: Article

References (46)

1. Honda, K., A. Takaoka, and T. Taniguchi. 2006. Type I interferon [corrected] gene induction by the interferon regulatory factor family of transcription factors. Immunity 25: 349-360.
2. Yoneyama, M., K. Onomoto, and T. Fujita. 2008. Cytoplasmic recognition of RNA. Adv. Drug Deliv. Rev. 60: 841-846.
3. Takeuchi, O., and S. Akira. 2009. Innate immunity to virus infection. Immunol. Rev. 227: 75-86.
4. Yamamoto, M., S. Sato, K. Mori, K. Hoshino, O. Takeuchi, K. Takeda, and S. Akira. 2002. Cutting edge: a novel Toll/IL-1 receptor domain-containing adapter that preferentially activates the IFN-beta promoter in the Toll-like receptor signaling. J. Immunol. 169: 6668-6672.
5. Oshiumi, H., M. Matsumoto, K. Funami, T. Akazawa, and T. Seya. 2003. TICAM-1, an adaptor molecule that participates in Toll-like receptor 3-mediated interferon-beta induction. Nat. Immunol. 4: 161-167.
6. Kawai, T., K. Takahashi, S. Sato, C. Coban, H. Kumar, H. Kato, K. J. Ishii, O. Takeuchi, and S. Akira. 2005. IPS-1, an adaptor triggering RIG-I- and Mda5mediated type I interferon induction. Nat. Immunol. 6: 981-988.
7. Yamamoto, M., S. Sato, H. Hemmi, K. Hoshino, T. Kaisho, H. Sanjo, O. Takeuchi, M. Sugiyama, M. Okabe, K. Takeda, and S. Akira. 2003. Role of adaptor TRIF in the MyD88-independent toll-like receptor signaling pathway. Science 301: 640-643.
8. Kumar, H., T. Kawai, H. Kato, S. Sato, K. Takahashi, C. Coban, M. Yamamoto, S. Uematsu, K. J. Ishii, O. Takeuchi, and S. Akira. 2006. Essential role of IPS-1 in innate immune responses against RNA viruses. J. Exp. Med. 203: 1795-1803.
9. Ikegame, S., M. Takeda, S. Ohno, Y. Nakatsu, Y. Nakanishi, and Y. Yanagi. 2010. Both RIG-I and MDA5 RNA helicases contribute to the induction of alpha/beta interferon in measles virus-infected human cells. J. Virol. 84: 372-379.
10. Berghäll, H., J. Sirén, D. Sarkar, I. Julkunen, P. B. Fisher, R. Vainionpää, and S. Matikainen. 2006. The interferon-inducible RNA helicase, mda-5, is involved in measles virus-induced expression of antiviral cytokines. Microbes Infect. 8: 2138-2144.
11. Griffin, D. E. 1995. Immune responses during measles virus infection. Curr. Top. Microbiol. Immunol. 191: 117-134.
12. Tatsuo, H., N. Ono, K. Tanaka, and Y. Yanagi. 2000. SLAM (CDw150) is a cellular receptor for measles virus. Nature 406: 893-897.
13. Mühlebach, M. D., M. Mateo, P. L. Sinn, S. Prüfer, K. M. Uhlig, V. H. Leonard, C. K. Navaratnarajah, M. Frenzke, X. X. Wong, B. Sawatsky, et al. 2011. Adherens junction protein nectin-4 is the epithelial receptor for measles virus. Nature 480: 530-533.
14. Noyce, R. S., D. G. Bondre, M. N. Ha, L. T. Lin, G. Sisson, M. S. Tsao, and C. D. Richardson. 2011. Tumor cell marker PVRL4 (nectin 4) is an epithelial cell receptor for measles virus. PLoS Pathog. 7: e1002240.
15. Delpeut, S., R. S. Noyce, R. W. Siu, and C. D. Richardson. 2012. Host factors and measles virus replication. Curr Opin Virol 2: 773-783.
16. Shingai, M., N. Inoue, T. Okuno, M. Okabe, T. Akazawa, Y. Miyamoto, M. Ayata, K. Honda, M. Kurita-Taniguchi, M. Matsumoto, et al. 2005. Wild-type measles virus infection in human CD46/CD150-transgenic mice: CD11cpositive dendritic cells establish systemic viral infection. J. Immunol. 175: 3252-3261.
17. Ferreira, C. S., M. Frenzke, V. H. Leonard, G. G. Welstead, C. D. Richardson, and R. Cattaneo. 2010. Measles virus infection of alveolar macrophages and dendritic cells precedes spread to lymphatic organs in transgenic mice expressing human signaling lymphocytic activation molecule (SLAM, CD150). J. Virol. 84: 3033-3042.
18. Lemon, K., R. D. de Vries, A. W. Mesman, S. McQuaid, G. van Amerongen, S. Yüksel, M. Ludlow, L. J. Rennick, T. Kuiken, B. K. Rima, et al. 2011. Early target cells of measles virus after aerosol infection of non-human primates. PLoS Pathog. 7: e1001263.
19. Mesman, A. W., R. D. de Vries, S. McQuaid, W. P. Duprex, R. L. de Swart, and T. B. Geijtenbeek. 2012. A prominent role for DC-SIGN+ dendritic cells in initiation and dissemination of measles virus infection in non-human primates. PLoS ONE 7: e49573.
20. Schneider-Schaulies, S., I. M. Klagge, and V. ter Meulen. 2003. Dendritic cells and measles virus infection. Curr. Top. Microbiol. Immunol. 276: 77-101.
21. Servet-Delprat, C., P. O. Vidalain, H. Valentin, and C. Rabourdin-Combe. 2003. Measles virus and dendritic cell functions: how specific response cohabits with immunosuppression. Curr. Top. Microbiol. Immunol. 276: 103-123.
22. Welstead, G. G., C. Iorio, R. Draker, J. Bayani, J. Squire, S. Vongpunsawad, R. Cattaneo, and C. D. Richardson. 2005. Measles virus replication in lymphatic cells and organs of CD150 (SLAM) transgenic mice. Proc. Natl. Acad. Sci. USA 102: 16415-16420.
23. Sellin, C. I., N. Davoust, V. Guillaume, D. Baas, M. F. Belin, R. Buckland, T. F. Wild, and B. Horvat. 2006. High pathogenicity of wild-type measles virus infection in CD150 (SLAM) transgenic mice. J. Virol. 80: 6420-6429.
24. Ohno, S., N. Ono, F. Seki, M. Takeda, S. Kura, T. Tsuzuki, and Y. Yanagi. 2007. Measles virus infection of SLAM (CD150) knockin mice reproduces tropism and immunosuppression in human infection. J. Virol. 81: 1650-1659.
25. Akazawa, T., T. Ebihara, M. Okuno, Y. Okuda, M. Shingai, K. Tsujimura, T. Takahashi, M. Ikawa, M. Okabe, N. Inoue, et al. 2007. Antitumor NK activation induced by the Toll-like receptor 3-TICAM-1 (TRIF) pathway in myeloid dendritic cells. Proc. Natl. Acad. Sci. USA 104: 252-257.
26. Oshiumi, H., M. Okamoto, K. Fujii, T. Kawanishi, M. Matsumoto, S. Koike, and T. Seya. 2011. The TLR3/TICAM-1 pathway is mandatory for innate immune responses to poliovirus infection. J. Immunol. 187: 5320-5327.
27. Kobune, F., H. Sakata, and A. Sugiura. 1990. Marmoset lymphoblastoid cells as a sensitive host for isolation of measles virus. J. Virol. 64: 700-705.
28. Takeda, M., K. Takeuchi, N. Miyajima, F. Kobune, Y. Ami, N. Nagata, Y. Suzaki, Y. Nagai, and M. Tashiro. 2000. Recovery of pathogenic measles virus from cloned cDNA. J. Virol. 74: 6643-6647.
29. Takeda, M., M. Tahara, T. Hashiguchi, T. A. Sato, F. Jinnouchi, S. Ueki, S. Ohno, and Y. Yanagi. 2007. A human lung carcinoma cell line supports efficient measles virus growth and syncytium formation via a SLAM- and CD46independent mechanism. J. Virol. 81: 12091-12096.
30. Shingai, M., T. Ebihara, N. A. Begum, A. Kato, T. Honma, K. Matsumoto, H. Saito, H. Ogura, M. Matsumoto, and T. Seya. 2007. Differential type I IFNinducing abilities of wild-type versus vaccine strains of measles virus. J. Immunol. 179: 6123-6133.
31. Sheehan, K. C., K. S. Lai, G. P. Dunn, A. T. Bruce, M. S. Diamond, J. D. Heutel, C. Dungo-Arthur, J. A. Carrero, J. M. White, P. J. Hertzog, and R. D. Schreiber. 2006. Blocking monoclonal antibodies specific for mouse IFN-alpha/beta receptor subunit 1 (IFNAR-1) from mice immunized by in vivo hydrodynamic transfection. J. Interferon Cytokine Res. 26: 804-819.
32. Vremec, D., J. Pooley, H. Hochrein, L. Wu, and K. Shortman. 2000. CD4 and CD8 expression by dendritic cell subtypes in mouse thymus and spleen. J. Immunol. 164: 2978-2986.
33. Asselin-Paturel, C., A. Boonstra, M. Dalod, I. Durand, N. Yessaad, C. DezutterDambuyant, A. Vicari, A. O'Garra, C. Biron, F. Brière, and G. Trinchieri. 2001. Mouse type I IFN-producing cells are immature APCs with plasmacytoid morphology. Nat. Immunol. 2: 1144-1150.
34. Edwards, A. D., S. S. Diebold, E. M. Slack, H. Tomizawa, H. Hemmi, T. Kaisho, S. Akira, and C. Reis e Sousa. 2003. Toll-like receptor expression in murine DC subsets: lack of TLR7 expression by CD8 alpha+ DC correlates with unresponsiveness to imidazoquinolines. Eur. J. Immunol. 33: 827-833.
35. Luber, C. A., J. Cox, H. Lauterbach, B. Fancke, M. Selbach, J. Tschopp, S. Akira, M. Wiegand, H. Hochrein, M. O'Keeffe, and M. Mann. 2010. Quantitative proteomics reveals subset-specific viral recognition in dendritic cells. Immunity 32: 279-289.
36. Hemmi, H., T. Kaisho, O. Takeuchi, S. Sato, H. Sanjo, K. Hoshino, T. Horiuchi, H. Tomizawa, K. Takeda, and S. Akira. 2002. Small anti-viral compounds activate immune cells via the TLR7 MyD88-dependent signaling pathway. Nat. Immunol. 3: 196-200.
37. Heil, F., H. Hemmi, H. Hochrein, F. Ampenberger, C. Kirschning, S. Akira, G. Lipford, H. Wagner, and S. Bauer. 2004. Species-specific recognition of single-stranded RNA via toll-like receptor 7 and 8. Science 303: 1526-1529.
38. Diebold, S. S., T. Kaisho, H. Hemmi, S. Akira, and C. Reis e Sousa. 2004. Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science 303: 1529-1531.
39. Hornung, V., M. Guenthner-Biller, C. Bourquin, A. Ablasser, M. Schlee, S. Uematsu, A. Noronha, M. Manoharan, S. Akira, A. de Fougerolles, et al. 2005. Sequence-specific potent induction of IFN-alpha by short interfering RNA in plasmacytoid dendritic cells through TLR7. Nat. Med. 11: 263-270.
40. Loiarro, M., C. Sette, G. Gallo, A. Ciacci, N. Fantò, D. Mastroianni, P. Carminati, and V. Ruggiero. 2005. Peptide-mediated interference of TIR domain dimerization in MyD88 inhibits interleukin-1-dependent activation of NFkappaB. J. Biol. Chem. 280: 15809-15814.
41. Kumagai, Y., O. Takeuchi, H. Kato, H. Kumar, K. Matsui, E. Morii, K. Aozasa, T. Kawai, and S. Akira. 2007. Alveolar macrophages are the primary interferon-alpha producer in pulmonary infection with RNA viruses. Immunity 27: 240-252.
42. Hahm, B., N. Arbour, and M. B. Oldstone. 2004. Measles virus interacts with human SLAM receptor on dendritic cells to cause immunosuppression. Virology 323: 292-302.
43. Koga, R., S. Ohno, S. Ikegame, and Y. Yanagi. 2010. Measles virus-induced immunosuppression in SLAM knock-in mice. J. Virol. 84: 5360-5367.
44. Takaki, H., K. Honda, K. Atarashi, F. Kobayashi, T. Ebihara, H. Oshiumi, M. Matsumoto, M. Shingai, and T. Seya. 2013. MAVS-dependent IRF3/IRF7 bypass of interferon β-induction restricts the response to measles infection in CD150Tg mouse bone marrow-derived dendritic cells. Molec. Immunol. In press.
45. Datta, S. K., V. Redecke, K. R. Prilliman, K. Takabayashi, M. Corr, T. Tallant, J. DiDonato, R. Dziarski, S. Akira, S. P. Schoenberger, and E. Raz. 2003. A subset of Toll-like receptor ligands induces cross-presentation by bone marrowderived dendritic cells. J. Immunol. 170: 4102-4110.
46. von Messling, V., D. Milosevic, and R. Cattaneo. 2004. Tropism illuminated: lymphocyte-based pathways blazed by lethal morbillivirus through the host immune system. Proc. Natl. Acad. Sci. USA 101: 14216-14221.