Type III IFNs are produced by and stimulate human plasmacytoid dendritic cells

Journal of Immunology

Volumn 189, Issue 6, 2012, Pages 2735-2745

  Yin, Zhiwei ^a,b,c   Dai, Jihong ^a   Deng, Jing ^a,c   Sheikh, Faruk ^d   Natalia, Mahwish ^a,c   Shih, Tiffany ^a,c   Lewis Antes, Anita ^b   Amrute, Sheela B ^a   Garrigues, Ursula ^e   Doyle, Sean ^e   Donnelly, Raymond P ^d   Kotenko, Sergei V ^b,c   Fitzgerald Bocarsly, Patricia ^a,c  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^b University of Medicine and Dentistry of New Jersey   (United States)

^c The State University of New Jersey   (United States)

^d CENTER FOR BIOLOGICS EVALUATION AND RESEARCH   (United States)

^e ZYMOGENETICS INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; INTERFERON; INTERFERON LAMBDA RECEPTOR; INTERFERON TYPE III; INTERLEUKIN 28A; INTERLEUKIN 29; TOLL LIKE RECEPTOR 9; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY TITER; ARTICLE; CELL FUNCTION; CELL STIMULATION; CELL SURFACE; CELL SURVIVAL; CONTROLLED STUDY; CYTOKINE PRODUCTION; FLOW CYTOMETRY; GENETIC TRANSCRIPTION; HERPES SIMPLEX VIRUS; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; INFLUENZA VIRUS; MOUSE; NATURAL KILLER CELL; NONHUMAN; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN EXPRESSION; PURIFICATION; SENDAI VIRUS; SIGNAL TRANSDUCTION; T LYMPHOCYTE; UPREGULATION; VIRUS REPLICATION;

CELLS, CULTURED; DENDRITIC CELLS; HEK293 CELLS; HEP G2 CELLS; HERPESVIRUS 1, HUMAN; HUMANS; INFLUENZA A VIRUS; INTERLEUKINS; RECEPTORS, CYTOKINE; SENDAI VIRUS;

EID: 84866163478     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1102038     Document Type: Article

References (58)

1. Novick, D., B. Cohen, and M. Rubinstein. 1994. The human interferon alpha/beta receptor: characterization and molecular cloning. Cell 77: 391-400. (Pubitemid 24145200)
2. Uzé, G., G. Lutfalla, and I. Gresser. 1990. Genetic transfer of a functional human interferon alpha receptor into mouse cells: cloning and expression of its cDNA. Cell 60: 225-234.
3. Stark, G. R., I. M. Kerr, B. R. Williams, R. H. Silverman, and R. D. Schreiber. 1998. How cells respond to interferons. Annu. Rev. Biochem. 67: 227-264. (Pubitemid 28411130)
4. Taniguchi, T., and A. Takaoka. 2002. The interferon-alpha/beta system in anti-viral responses: a multimodal machinery of gene regulation by the IRF family of transcription factors. Curr. Opin. Immunol. 14: 111-116. (Pubitemid 34085114)
5. Biron, C. A. 1998. Role of early cytokines, including alpha and beta interferons (IFN-alpha/beta), in innate and adaptive immune responses to viral infections. Semin. Immunol. 10: 383-390. (Pubitemid 28499552)
6. Kadowaki, N., and Y. J. Liu. 2002. Natural type I interferon-producing cells as a link between innate and adaptive immunity. Hum. Immunol. 63: 1126-1132. (Pubitemid 36025987)
7. Farrar, M. A., and R. D. Schreiber. 1993. The molecular cell biology of interferon-gamma and its receptor. Annu. Rev. Immunol. 11: 571-611. (Pubitemid 23115018)
8. Pestka, S., S. V. Kotenko, G. Muthukumaran, L. S. Izotova, J. R. Cook, and G. Garotta. 1997. The interferon gamma (IFN-gamma) receptor: a paradigm for the multichain cytokine receptor. Cytokine Growth Factor Rev. 8: 189-206. (Pubitemid 28077927)
9. Sheppard, P., W. Kindsvogel, W. Xu, K. Henderson, S. Schlutsmeyer, T. E. Whitmore, R. Kuestner, U. Garrigues, C. Birks, J. Roraback, et al. 2003. IL-28, IL-29 and their class II cytokine receptor IL-28R. Nat. Immunol. 4: 63-68. (Pubitemid 36104710)
10. Kotenko, S. V., G. Gallagher, V. V. Baurin, A. Lewis-Antes, M. Shen, N. K. Shah, J. A. Langer, F. Sheikh, H. Dickensheets, and R. P. Donnelly. 2003. IFN-lambdas mediate antiviral protection through a distinct class II cytokine receptor complex. Nat. Immunol. 4: 69-77. (Pubitemid 36109115)
11. Zitzmann, K., S. Brand, S. Baehs, B. Göke, J. Meinecke, G. Spöttl, H. Meyer, and C. J. Auernhammer. 2006. Novel interferon-lambdas induce antiproliferative effects in neuroendocrine tumor cells. Biochem. Biophys. Res. Commun. 344: 1334-1341.
12. Ank, N., H. West, C. Bartholdy, K. Eriksson, A. R. Thomsen, and S. R. Paludan. 2006. Lambda interferon (IFN-lambda), a type III IFN, is induced by viruses and IFNs and displays potent antiviral activity against select virus infections in vivo. J. Virol. 80: 4501-4509.
13. Meager, A., K. Visvalingam, P. Dilger, D. Bryan, and M. Wadhwa. 2005. Biological activity of interleukins-28 and -29: comparison with type I interferons. Cytokine 31: 109-118. (Pubitemid 40910226)
14. Onoguchi, K., M. Yoneyama, A. Takemura, S. Akira, T. Taniguchi, H. Namiki, and T. Fujita. 2007. Viral infections activate types I and III interferon genes through a common mechanism. J. Biol. Chem. 282: 7576-7581. (Pubitemid 47093699)
15. Bartlett, N. W., K. Buttigieg, S. V. Kotenko, and G. L. Smith. 2005. Murine interferon lambdas (type III interferons) exhibit potent antiviral activity in vivo in a poxvirus infection model. J. Gen. Virol. 86: 1589-1596. (Pubitemid 40766871)
16. Doyle, S. E., H. Schreckhise, K. Khuu-Duong, K. Henderson, R. Rosler, H. Storey, L. Yao, H. Liu, F. Barahmand-pour, P. Sivakumar, et al. 2006. Interleukin-29 uses a type 1 interferon-like program to promote antiviral responses in human hepatocytes. Hepatology 44: 896-906. (Pubitemid 46489554)
17. Marcello, T., A. Grakoui, G. Barba-Spaeth, E. S. Machlin, S. V. Kotenko, M. R. MacDonald, and C. M. Rice. 2006. Interferons alpha and lambda inhibit hepatitis C virus replication with distinct signal transduction and gene regulation kinetics. Gastroenterology 131: 1887-1898. (Pubitemid 44958521)
18. Zhou, Z., O. J. Hamming, N. Ank, S. R. Paludan, A. L. Nielsen, and R. Hartmann. 2007. Type III interferon (IFN) induces a type I IFN-like response in a restricted subset of cells through signaling pathways involving both the JakSTAT pathway and the mitogen-activated protein kinases. J. Virol. 81: 7749-7758. (Pubitemid 47047861)
19. Sommereyns, C., S. Paul, P. Staeheli, and T. Michiels. 2008. IFN-lambda (IFN-lambda) is expressed in a tissue-dependent fashion and primarily acts on epithelial cells in vivo. PLoS Pathog. 4: e1000017.
20. Ank, N., M. B. Iversen, C. Bartholdy, P. Staeheli, R. Hartmann, U. B. Jensen, F. Dagnaes-Hansen, A. R. Thomsen, Z. Chen, H. Haugen, et al. 2008. An important role for type III interferon (IFN-lambda/IL-28) in TLR-induced antiviral activity. J. Immunol. 180: 2474-2485.
21. Mennechet, F. J., and G. Uzé. 2006. Interferon-lambda-treated dendritic cells specifically induce proliferation of FOXP3-expressing suppressor T cells. Blood 107: 4417-4423. (Pubitemid 43801368)
22. Jordan, W. J., J. Eskdale, S. Srinivas, V. Pekarek, D. Kelner, M. Rodia, and G. Gallagher. 2007. Human interferon lambda-1 (IFN-lambda1/IL-29) modulates the Th1/Th2 response. Genes Immun. 8: 254-261. (Pubitemid 46679436)
23. Melchjorsen, J., J. Sirén, I. Julkunen, S. R. Paludan, and S. Matikainen. 2006. Induction of cytokine expression by herpes simplex virus in human monocyte-derived macrophages and dendritic cells is dependent on virus replication and is counteracted by ICP27 targeting NF-kappaB and IRF-3. J. Gen. Virol. 87: 1099-1108.
24. Wolk, K., K. Witte, E. Witte, S. Proesch, G. Schulze-Tanzil, K. Nasilowska, J. Thilo, K. Asadullah, W. Sterry, H. D. Volk, and R. Sabat. 2008. Maturing dendritic cells are an important source of IL-29 and IL-20 that may cooperatively increase the innate immunity of keratinocytes. J. Leukoc. Biol. 83: 1181-1193.
25. Osterlund, P., V. Veckman, J. Sirén, K. M. Klucher, J. Hiscott, S. Matikainen, and I. Julkunen. 2005. Gene expression and antiviral activity of alpha/beta interferons and interleukin-29 in virus-infected human myeloid dendritic cells. J. Virol. 79: 9608-9617. (Pubitemid 41022304)
26. Coccia, E. M., M. Severa, E. Giacomini, D. Monneron, M. E. Remoli, I. Julkunen, M. Cella, R. Lande, and G. Uzé. 2004. Viral infection and Toll-like receptor agonists induce a differential expression of type I and lambda interferons in human plasmacytoid and monocyte-derived dendritic cells. Eur. J. Immunol. 34: 796-805. (Pubitemid 39255927)
27. Feldman, S. B., M. Ferraro, H. M. Zheng, N. Patel, S. Gould-Fogerite, and P. Fitzgerald-Bocarsly. 1994. Viral induction of low frequency interferon-alpha producing cells. Virology 204: 1-7. (Pubitemid 24305312)
28. Fitzgerald-Bocarsly, P. 2002. Natural interferon-alpha producing cells: the plasmacytoid dendritic cells. Biotechniques (Suppl.): 16-20, 22, 24-29.
29. Cederblad, B., and G. V. Alm. 1990. Infrequent but efficient interferon-alpha-producing human mononuclear leukocytes induced by herpes simplex virus in vitro studied by immuno-plaque and limiting dilution assays. J. Interferon Res. 10: 65-73. (Pubitemid 20084379)
30. Megjugorac, N. J., H. A. Young, S. B. Amrute, S. L. Olshalsky, and P. Fitzgerald-Bocarsly. 2004. Virally stimulated plasmacytoid dendritic cells produce chemokines and induce migration of T and NK cells. J. Leukoc. Biol. 75: 504-514. (Pubitemid 38316382)
31. Jego, G., A. K. Palucka, J. P. Blanck, C. Chalouni, V. Pascual, and J. Banchereau. 2003. Plasmacytoid dendritic cells induce plasma cell differentiation through type I interferon and interleukin 6. Immunity 19: 225-234. (Pubitemid 37011337)
32. Zitvogel, L., M. Terme, C. Borg, and G. Trinchieri. 2006. Dendritic cell-NK cell cross-talk: regulation and physiopathology. Curr. Top. Microbiol. Immunol. 298: 157-174.
33. Ito, T., R. Amakawa, M. Inaba, T. Hori, M. Ota, K. Nakamura, M. Takebayashi, M. Miyaji, T. Yoshimura, K. Inaba, and S. Fukuhara. 2004. Plasmacytoid dendritic cells regulate Th cell responses through OX40 ligand and type I IFNs. J. Immunol. 172: 4253-4259. (Pubitemid 38375238)
34. Fanning, S. L., T. C. George, D. Feng, S. B. Feldman, N. J. Megjugorac, A. G. Izaguirre, and P. Fitzgerald-Bocarsly. 2006. Receptor cross-linking on human plasmacytoid dendritic cells leads to the regulation of IFN-alpha production. J. Immunol. 177: 5829-5839. (Pubitemid 44628796)
35. Paladino, P., S. E. Collins, and K. L. Mossman. 2010. Cellular localization of the herpes simplex virus ICP0 protein dictates its ability to block IRF3-mediated innate immune responses. PLoS ONE 5: e10428.
36. Lauterbach, H., B. Bathke, S. Gilles, C. Traidl-Hoffmann, C. A. Luber, G. Fejer, M. A. Freudenberg, G. M. Davey, D. Vremec, A. Kallies, et al. 2010. Mouse CD8alpha+ DCs and human BDCA3+ DCs are major producers of IFN-lambda in response to poly IC. J. Exp. Med. 207: 2703-2717.
37. Krug, A., A. Towarowski, S. Britsch, S. Rothenfusser, V. Hornung, R. Bals, T. Giese, H. Engelmann, S. Endres, A. M. Krieg, and G. Hartmann. 2001. Toll-like receptor expression reveals CpG DNA as a unique microbial stimulus for plasmacytoid dendritic cells which synergizes with CD40 ligand to induce high amounts of IL-12. Eur. J. Immunol. 31: 3026-3037. (Pubitemid 32994554)
38. Prescott, J., P. Hall, M. Acuna-Retamar, C. Ye, M. G. Wathelet, H. Ebihara, H. Feldmann, and B. Hjelle. 2010. New World hantaviruses activate IFNlambda production in type I IFN-deficient vero E6 cells. PLoS ONE 5: e11159.
39. Sato, M., N. Hata, M. Asagiri, T. Nakaya, T. Taniguchi, and N. Tanaka. 1998. Positive feedback regulation of type I IFN genes by the IFN-inducible transcription factor IRF-7. FEBS Lett. 441: 106-110. (Pubitemid 29012382)
40. Dzionek, A., Y. Sohma, J. Nagafune, M. Cella, M. Colonna, F. Facchetti, G. Günther, I. Johnston, A. Lanzavecchia, T. Nagasaka, et al. 2001. BDCA-2, a novel plasmacytoid dendritic cell-specific type II C-type lectin, mediates antigen capture and is a potent inhibitor of interferon alpha/beta induction. J. Exp. Med. 194: 1823-1834. (Pubitemid 34028661)
41. Morrison, L. A. 2004. The Toll of herpes simplex virus infection. Trends Microbiol. 12: 353-356. (Pubitemid 38987820)
42. Lund, J., A. Sato, S. Akira, R. Medzhitov, and A. Iwasaki. 2003. Toll-like receptor 9-mediated recognition of Herpes simplex virus-2 by plasmacytoid dendritic cells. J. Exp. Med. 198: 513-520. (Pubitemid 36976063)
43. Hornung, V., J. Schlender, M. Guenthner-Biller, S. Rothenfusser, S. Endres, K. K. Conzelmann, and G. Hartmann. 2004. Replication-dependent potent IFN-alpha induction in human plasmacytoid dendritic cells by a single-stranded RNA virus. J. Immunol. 173: 5935-5943. (Pubitemid 39487747)
44. Siegal, F. P., N. Kadowaki, M. Shodell, P. A. Fitzgerald-Bocarsly, K. Shah, S. Ho, S. Antonenko, and Y. J. Liu. 1999. The nature of the principal type 1 interferon-producing cells in human blood. Science 284: 1835-1837.
45. Maher, S. G., F. Sheikh, A. J. Scarzello, A. L. Romero-Weaver, D. P. Baker, R. P. Donnelly, and A. M. Gamero. 2008. IFNalpha and IFNlambda differ in their antiproliferative effects and duration of JAK/STAT signaling activity. Cancer Biol. Ther. 7: 1109-1115.
46. Dai, J., N. J. Megjugorac, S. B. Amrute, and P. Fitzgerald-Bocarsly. 2004. Regulation of IFN regulatory factor-7 and IFN-alpha production by enveloped virus and lipopolysaccharide in human plasmacytoid dendritic cells. J. Immunol. 173: 1535-1548. (Pubitemid 38971583)
47. Shodell, M., K. Shah, and F. P. Siegal. 2003. Circulating human plasmacytoid dendritic cells are highly sensitive to corticosteroid administration. Lupus 12: 222-230. (Pubitemid 36458681)
48. Fitzgerald-Bocarsly, P., M. Feldman, M. Mendelsohn, S. Curl, and C. Lopez. 1988. Human mononuclear cells which produce interferon-alpha during NK (HSV-FS) assays are HLA-DR positive cells distinct from cytolytic natural killer effectors. J. Leukoc. Biol. 43: 323-334.
49. Guiducci, C., G. Ott, J. H. Chan, E. Damon, C. Calacsan, T. Matray, K. D. Lee, R. L. Coffman, and F. J. Barrat. 2006. Properties regulating the nature of the plasmacytoid dendritic cell response to Toll-like receptor 9 activation. J. Exp. Med. 203: 1999-2008. (Pubitemid 44188473)
50. Honda, K., Y. Ohba, H. Yanai, H. Negishi, T. Mizutani, A. Takaoka, C. Taya, and T. Taniguchi. 2005. Spatiotemporal regulation of MyD88-IRF-7 signalling for robust type-I interferon induction. Nature 434: 1035-1040. (Pubitemid 40586053)
51. Izaguirre, A., B. J. Barnes, S. Amrute, W. S. Yeow, N. Megjugorac, J. Dai, D. Feng, E. Chung, P. M. Pitha, and P. Fitzgerald-Bocarsly. 2003. Comparative analysis of IRF and IFN-alpha expression in human plasmacytoid and monocyte-derived dendritic cells. J. Leukoc. Biol. 74: 1125-1138. (Pubitemid 38040335)
52. Iversen, M. B., N. Ank, J. Melchjorsen, and S. R. Paludan. 2010. Expression of type III interferon (IFN) in the vaginal mucosa is mediated primarily by dendritic cells and displays stronger dependence on NF-kappaB than type I IFNs. J. Virol. 84: 4579-4586.
53. Stoltz, M., and J. Klingström. 2010. Alpha/beta interferon (IFN-alpha/beta)-independent induction of IFN-lambda1 (interleukin-29) in response to Hantaan virus infection. J. Virol. 84: 9140-9148.
54. Zhou, P., C. Cowled, S. Todd, G. Crameri, E. R. Virtue, G. A. Marsh, R. Klein, Z. Shi, L. F. Wang, and M. L. Baker. 2011. Type III IFNs in pteropid bats: differential expression patterns provide evidence for distinct roles in antiviral immunity. J. Immunol. 186: 3138-3147.
55. Hochrein, H., B. Schlatter, M. O'Keeffe, C. Wagner, F. Schmitz, M. Schiemann, S. Bauer, M. Suter, and H. Wagner. 2004. Herpes simplex virus type-1 induces IFN-alpha production via Toll-like receptor 9-dependent and -independent pathways. Proc. Natl. Acad. Sci. USA 101: 11416-11421. (Pubitemid 39038361)
56. Krug, A., G. D. Luker, W. Barchet, D. A. Leib, S. Akira, and M. Colonna. 2004. Herpes simplex virus type 1 activates murine natural interferon-producing cells through toll-like receptor 9. Blood 103: 1433-1437. (Pubitemid 38168659)
57. Megjugorac, N. J., G. E. Gallagher, and G. Gallagher. 2009. Modulation of human plasmacytoid DC function by IFN-lambda1 (IL-29). J. Leukoc. Biol. 86: 1359-1363.
58. Ank, N., and S. R. Paludan. 2009. Type III IFNs: new layers of complexity in innate antiviral immunity. Biofactors 35: 82-87.