CD28 deficiency enhances type i IFN production by murine plasmacytoid dendritic cells

Journal of Immunology

Volumn 196, Issue 4, 2016, Pages 1900-1909

  Macal, Monica ^a   Tam, Miguel A ^a   Hesser, Charles ^a   Di Domizio, Jeremy ^b   Leger, Psylvia ^a   Gilliet, Michel ^b   Zuniga, Elina I ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CD28 ANTIGEN; INTERFERON; T LYMPHOCYTE RECEPTOR; TOLL LIKE RECEPTOR; TRANSCRIPTOME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ARTICLE; CELL MATURATION; CELL STIMULATION; CELL SURVIVAL; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DNA VIRUS INFECTION; DOWN REGULATION; GENE EXPRESSION PROFILING; HUMAN; HUMAN CELL; IMMUNOREGULATION; IN VIVO STUDY; INNATE IMMUNITY; MOUSE; NONHUMAN; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RNA VIRUS INFECTION; SKIN INJURY; VIROGENESIS; VIRUS CELL INTERACTION; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; DNA MICROARRAY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; REAL TIME POLYMERASE CHAIN REACTION;

ANIMALS; ANTIGENS, CD28; DENDRITIC CELLS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HUMANS; INTERFERON TYPE I; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REAL-TIME POLYMERASE CHAIN REACTION; TRANSCRIPTOME;

EID: 84958576534     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1501658     Document Type: Article

References (72)

1. Tomasello, E., E. Pollet, T. P. Vu Manh, G. Uzé, and M. Dalod. 2014. Harnessing mechanistic knowledge on beneficial versus deleterious IFN-I effects to design innovative immunotherapies targeting cytokine activity to specific cell types. Front. Immunol. 5: 526.
2. García-Sastre, A., and C. A. Biron. 2006. Type 1 interferons and the virus-host relationship: A lesson in détente. Science 312: 879-882.
3. Reizis, B., A. Bunin, H. S. Ghosh, K. L. Lewis, and V. Sisirak. 2011. Plasmacytoid dendritic cells: recent progress and open questions. Annu. Rev. Immunol. 29: 163-183.
4. Wang, Y., M. Swiecki, S. A. McCartney, and M. Colonna. 2011. dsRNA sensors and plasmacytoid dendritic cells in host defense and autoimmunity. Immunol. Rev. 243: 74-90.
5. Asselin-Paturel, C., G. Brizard, J. J. Pin, F. Brière, and G. Trinchieri. 2003. Mouse strain differences in plasmacytoid dendritic cell frequency and function revealed by a novel monoclonal antibody. J. Immunol. 171: 6466-6477.
6. Asselin-Paturel, C., and G. Trinchieri. 2005. Production of type I interferons: plasmacytoid dendritic cells and beyond. J. Exp. Med. 202: 461-465.
7. Takeuchi, O., and S. Akira. 2009. Innate immunity to virus infection. Immunol. Rev. 227: 75-86.
8. McKenna, K., A. S. Beignon, and N. Bhardwaj. 2005. Plasmacytoid dendritic cells: linking innate and adaptive immunity. J. Virol. 79: 17-27.
9. Ito, T., R. Amakawa, T. Kaisho, H. Hemmi, K. Tajima, K. Uehira, Y. Ozaki, H. Tomizawa, S. Akira, and S. Fukuhara. 2002. Interferon-A and interleukin-12 are induced differentially by Toll-like receptor 7 ligands in human blood dendritic cell subsets. J. Exp. Med. 195: 1507-1512.
10. Loré, K., M. R. Betts, J. M. Brenchley, J. Kuruppu, S. Khojasteh, S. Perfetto, M. Roederer, R. A. Seder, and R. A. Koup. 2003. Toll-like receptor ligands modulate dendritic cells to augment cytomegalovirus-and HIV-1-specific T cell responses. J. Immunol. 171: 4320-4328.
11. Dalod, M., T. P. Salazar-Mather, L. Malmgaard, C. Lewis, C. Asselin-Paturel, F. Brière, G. Trinchieri, and C. A. Biron. 2002. Interferon a/b and interleukin 12 responses to viral infections: pathways regulating dendritic cell cytokine expression in vivo. J. Exp. Med. 195: 517-528.
12. Krug, A., A. R. French, W. Barchet, J. A. Fischer, A. Dzionek, J. T. Pingel, M. M. Orihuela, S. Akira, W. M. Yokoyama, and M. Colonna. 2004. TLR9-dependent recognition of MCMV by IPC and DC generates coordinated cytokine responses that activate antiviral NK cell function. Immunity 21: 107-119.
13. Smit, J. J., B. D. Rudd, and N. W. Lukacs. 2006. Plasmacytoid dendritic cells inhibit pulmonary immunopathology and promote clearance of respiratory syncytial virus. J. Exp. Med. 203: 1153-1159.
14. Wang, H., N. Peters, and J. Schwarze. 2006. Plasmacytoid dendritic cells limit viral replication, pulmonary inflammation, and airway hyperresponsiveness in respiratory syncytial virus infection. J. Immunol. 177: 6263-6270.
15. Cervantes-Barragan, L., K. L. Lewis, S. Firner, V. Thiel, S. Hugues, W. Reith, B. Ludewig, and B. Reizis. 2012. Plasmacytoid dendritic cells control T-cell response to chronic viral infection. Proc. Natl. Acad. Sci. USA 109: 3012-3017.
16. Lund, J. M., M. M. Linehan, N. Iijima, and A. Iwasaki. 2006. Cutting edge: plasmacytoid dendritic cells provide innate immune protection against mucosal viral infection in situ. J. Immunol. 177: 7510-7514.
17. Takahashi, K., S. Asabe, S. Wieland, U. Garaigorta, P. Gastaminza, M. Isogawa, and F. V. Chisari. 2010. Plasmacytoid dendritic cells sense hepatitis C virusinfected cells, produce interferon, and inhibit infection. Proc. Natl. Acad. Sci. USA 107: 7431-7436.
18. Fitzgerald-Bocarsly, P., and E. S. Jacobs. 2010. Plasmacytoid dendritic cells in HIV infection: striking a delicate balance. J. Leukoc. Biol. 87: 609-620.
19. Jung, A., H. Kato, Y. Kumagai, H. Kumar, T. Kawai, O. Takeuchi and S. Akira. 2008. Lymphocytoid choriomeningitis virus activates plasmacytoid dendritic cells and induces a cytotoxic T-cell response via MyD88. J. Virol. 82: 196-206.
20. Macal, M., G. M. Lewis, S. Kunz, R. Flavell, J. A. Harker, and E. I. Zúnĩga. 2012. Plasmacytoid dendritic cells are productively infected and activated through TLR-7 early after arenavirus infection. Cell Host Microbe 11: 617-630.
21. Lee, L. N., S. Burke, M. Montoya, and P. Borrow. 2009. Multiple mechanisms contribute to impairment of type 1 interferon production during chronic lymphocytic choriomeningitis virus infection of mice. J. Immunol. 182: 7178-7189.
22. Zuniga, E. I., L. Y. Liou, L. Mack, M. Mendoza, and M. B. Oldstone. 2008. Persistent virus infection inhibits type I interferon production by plasmacytoid dendritic cells to facilitate opportunistic infections. Cell Host Microbe 4: 374-386.
23. Dolganiuc, A., S. Chang, K. Kodys, P. Mandrekar, G. Bakis, M. Cormier, and G. Szabo. 2006. Hepatitis C virus (HCV) core protein-induced, monocytemediated mechanisms of reduced IFN-A and plasmacytoid dendritic cell loss in chronic HCV infection. J. Immunol. 177: 6758-6768.
24. Sisirak, V., J. Faget, M. Gobert, N. Goutagny, N. Vey, I. Treilleux, S. Renaudineau, G. Poyet, S. I. Labidi-Galy, S. Goddard-Leon, et al. 2012. Impaired IFN-A production by plasmacytoid dendritic cells favors regulatory Tcell expansion that may contribute to breast cancer progression. Cancer Res. 72: 5188-5197.
25. Nestle, F. O., C. Conrad, A. Tun-Kyi, B. Homey, M. Gombert, O. Boyman, G. Burg, Y. J. Liu, and M. Gilliet. 2005. Plasmacytoid predendritic cells initiate psoriasis through interferon-A production. J. Exp. Med. 202: 135-143.
26. Li, Q., B. Xu, S. A. Michie, K. H. Rubins, R. D. Schreriber, and H. O. McDevitt. 2008. Interferon-A initiates type 1 diabetes in nonobese diabetic mice. Proc. Natl. Acad. Sci. USA 105: 12439-12444.
27. Isaksson, M., B. Ardesjö, L. Rönnblom, O. Kämpe, H. Lassmann, M. L. Eloranta, and A. Lobell. 2009. Plasmacytoid DC promote priming of autoimmune Th17 cells and EAE. Eur. J. Immunol. 39: 2925-2935.
28. Guiducci, C., M. Gong, Z. Xu, M. Gill, D. Chaussabel, T. Meeker, J. H. Chan, T. Wright, M. Punaro, S. Bolland, et al. 2010. TLR recognition of self nucleic acids hampers glucocorticoid activity in lupus. Nature 465: 937-941.
29. Rowland, S. L., J. M. Riggs, S. Gilfillan, M. Bugatti, W. Vermi, R. Kolbeck, E. R. Unanue, M. A. Sanjuan, and M. Colonna. 2014. Early, transient depletion of plasmacytoid dendritic cells ameliorates autoimmunity in a lupus model. J. Exp. Med. 211: 1977-1991.
30. Sisirak, V., D. Ganguly, K. L. Lewis, C. Couillault, L. Tanaka, S. Bolland, V. D'Agati, K. B. Elkon, and B. Reizis. 2014. Genetic evidence for the role of plasmacytoid dendritic cells in systemic lupus erythematosus. J. Exp. Med. 211: 1969-1976.
31. Gregorio, J., S. Meller, C. Conrad, A. Di Nardo, B. Homey, A. Lauerma, N. Arai, R. L. Gallo, J. Digiovanni, and M. Gilliet. 2010. Plasmacytoid dendritic cells sense skin injury and promote wound healing through type I interferons. J. Exp. Med. 207: 2921-2930.
32. Lenschow, D. J., T. L. Walunas, and J. A. Bluestone. 1996. CD28/B7 system of T cell costimulation. Annu. Rev. Immunol. 14: 233-258.
33. Ahmed, R., A. Salmi, L. D. Butler, J. M. Chiller, and M. B. Oldstone. 1984. Selection of genetic variants of lymphocytic choriomeningitis virus in spleens of persistently infected mice: role in suppression of cytotoxic T lymphocyte response and viral persistence. J. Exp. Med. 160: 521-540.
34. Tabeta, K., P. Georgel, E. Janssen, X. Du, K. Hoebe, K. Crozat, S. Mudd, L. Shamel, S. Sovath, J. Goode, et al. 2004. Toll-like receptors 9 and 3 as essential components of innate immune defense against mouse cytomegalovirus infection. Proc. Natl. Acad. Sci. USA 101: 3516-3521.
35. Macal, M., S. Sankaran, T. W. Chun, E. Reay, J. Flamm, T. J. Prindiville, and S. Dandekar. 2008. Effective CD4+ T-cell restoration in gut-associated lymphoid tissue of HIV-infected patients is associated with enhanced Th17 cells and polyfunctional HIV-specific T-cell responses. Mucosal Immunol. 1: 475-488.
36. Zuniga, E. I., D. B. McGavern, J. L. Pruneda-Paz, C. Teng, and M. B. Oldstone. 2004. Bone marrow plasmacytoid dendritic cells can differentiate into myeloid dendritic cells upon virus infection. Nat. Immunol. 5: 1227-1234.
37. Jiang, Z., P. Georgel, X. Du, L. Shamel, S. Sovath, S. Mudd, M. Huber, C. Kalis, S. Keck, C. Galanos, et al. 2005. CD14 is required for MyD88-independent LPS signaling. Nat. Immunol. 6: 565-570.
38. Edgar, R., M. Domrachev, and A. E. Lash. 2002. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 30: 207-210.
39. Pear, W. S., J. P. Miller, L. Xu, J. C. Pui, B. Soffer, R. C. Quackenbush, A. M. Pendergast, R. Bronson, J. C. Aster, M. L. Scott, and D. Baltimore. 1998. Efficient and rapid induction of a chronic myelogenous leukemia-like myeloproliferative disease in mice receiving P210 bcr/abl-transduced bone marrow. Blood 92: 3780-3792.
40. Dalod, M., R. Chelbi, B. Malissen, and T. Lawrence. 2014. Dendritic cell maturation: functional specialization through signaling specificity and transcriptional programming. EMBO J. 33: 1104-1116.
41. Robbins, S. H., T. Walzer, D. Dembélé, C. Thibault, A. Defays, G. Bessou, H. Xu, E. Vivier, M. Sellars, P. Pierre, et al. 2008. Novel insights into the relationships between dendritic cell subsets in human and mouse revealed by genome-wide expression profiling. Genome Biol. 9: R17.
42. Riley, J. L., and C. H. June. 2005. The CD28 family: A T-cell rheostat for therapeutic control of T-cell activation. Blood 105: 13-21.
43. Maeda, T., K. Murata, T. Fukushima, K. Sugahara, K. Tsuruda, M. Anami, Y. Onimaru, K. Tsukasaki, M. Tomonaga, R. Moriuchi, et al. 2005. A novel plasmacytoid dendritic cell line, CAL-1, established from a patient with blastic natural killer cell lymphoma. Int. J. Hematol. 81: 148-154.
44. Giard, D. J., S. A. Aaronson, G. J. Todaro, P. Arnstein, J. H. Kersey, H. Dosik, and W. P. Parks. 1973. In vitro cultivation of human tumors: establishment of cell lines derived from a series of solid tumors. J. Natl. Cancer Inst. 51: 1417-1423.
45. Tsuchiya, S., M. Yamabe, Y. Yamaguchi, Y. Kobayashi, T. Konno, and K. Tada. 1980. Establishment and characterization of a human acute monocytic leukemia cell line (THP-1). Int. J. Cancer 26: 171-176.
46. Liu, Y. J. 2005. IPC: professional type 1 interferon-producing cells and plasmacytoid dendritic cell precursors. Annu. Rev. Immunol. 23: 275-306.
47. Harding, F. A., J. G. McArthur, J. A. Gross, D. H. Raulet, and J. P. Allison. 1992. CD28-mediated signalling co-stimulates murine T cells and prevents induction of anergy in T-cell clones. Nature 356: 607-609.
48. Waterhouse, P., J. M. Penninger, E. Timms, A. Wakeham, A. Shahinian, K. P. Lee, C. B. Thompson, H. Griesser, and T. W. Mak. 1995. Lymphoproliferative disorders with early lethality in mice deficient in Ctla-4. Science 270: 985-988.
49. Bond, E., F. Liang, K. J. Sandgren, A. Smed-Sörensen, P. Bergman, S. Brighenti, W. C. Adams, S. A. Betemariam, M. X. Rangaka, C. Lange, et al. 2012. Plasmacytoid dendritic cells infiltrate the skin in positive tuberculin skin test indurations. J. Invest. Dermatol. 132: 114-123.
50. Wojcik, S. M., D. S. Bundman, and D. R. Roop. 2000. Delayed wound healing in keratin 6a knockout mice. Mol. Cell. Biol. 20: 5248-5255.
51. Medzhitov, R., and C. A. Janeway, Jr. 1998. Innate immune recognition and control of adaptive immune responses. Semin. Immunol. 10: 351-353.
52. Galea-Lauri, J., D. Darling, S. U. Gan, L. Krivochtchapov, M. Kuiper, J. Gäken, B. Souberbielle, and F. Farzaneh. 1999. Expression of a variant of CD28 on a subpopulation of human NK cells: implications for B7-mediated stimulation of NK cells. J. Immunol. 163: 62-70.
53. Woerly, G., P. Lacy, A. B. Younes, N. Roger, S. Loiseau, R. Moqbel, and M. Capron. 2002. Human eosinophils express and release IL-13 following CD28-dependent activation. J. Leukoc. Biol. 72: 769-779.
54. Woerly, G., N. Roger, S. Loiseau, D. Dombrowicz, A. Capron, and M. Capron. 1999. Expression of CD28 and CD86 by human eosinophils and role in the secretion of type 1 cytokines (interleukin 2 and interferon g): inhibition by immunoglobulin a complexes. J. Exp. Med. 190: 487-495.
55. Venuprasad, K., P. Parab, D. V. Prasad, S. Sharma, P. R. Banerjee, M. Deshpande, D. K. Mitra, S. Pal, R. Bhadra, D. Mitra, and B. Saha. 2001. Immunobiology of CD28 expression on human neutrophils. I. CD28 regulates neutrophil migration by modulating CXCR-1 expression. Eur. J. Immunol. 31: 1536-1543.
56. Venuprasad, K., P. P. Banerjee, S. Chattopadhyay, S. Sharma, S. Pal, P. B. Parab D. Mitra, and B. Saha. 2002. Human neutrophil-expressed CD28 interacts with macrophage B7 to induce phosphatidylinositol 3-kinase-dependent IFN-g secretion and restriction of Leishmania growth. J. Immunol. 169: 920-928.
57. Delogu, A., A. Schebesta, Q. Sun, K. Aschenbrenner, T. Perlot, and M. Busslinger. 2006. Gene repression by Pax5 in B cells is essential for blood cell homeostasis and is reversed in plasma cells. Immunity 24: 269-281.
58. Njau, M. N., J. H. Kim, C. P. Chappell, R. Ravindran, L. Thomas, B. Pulendran, and J. Jacob. 2012. CD28-B7 interaction modulates short-and long-lived plasma cell function. J. Immunol. 189: 2758-2767.
59. Rozanski, C. H., R. Arens, L. M. Carlson, J. Nair, L. H. Boise, A. A. Chanan-Khan, S. P. Schoenberger, and K. P. Lee. 2011. Sustained antibody responses depend on CD28 function in bone marrow-resident plasma cells. J. Exp. Med. 208: 1435-1446.
60. Agudo, J., A. Ruzo, N. Tung, H. Salmon, M. Leboeuf, D. Hashimoto, C. Becker, L. A. Garrett-Sinha, A. Baccarini, M. Merad, and B. D. Brown. 2014. The miR-126-VEGFR2 axis controls the innate response to pathogen-associated nucleic acids. Nat. Immunol. 15: 54-62.
61. Hannier, S., M. Tournier, G. Bismuth, and F. Triebel. 1998. CD3/TCR complexassociated lymphocyte activation gene-3 molecules inhibit CD3/TCR signaling. J. Immunol. 161: 4058-4065.
62. Workman, C. J., and D. A. Vignali. 2005. Negative regulation of T cell homeostasis by lymphocyte activation gene-3 (CD223). J. Immunol. 174: 688-695.
63. Workman, C. J., Y. Wang, K. C. El Kasmi, D. M. Pardoll, P. J. Murray, C. G. Drake, and D. A. Vignali. 2009. LAG-3 regulates plasmacytoid dendritic cell homeostasis. J. Immunol. 182: 1885-1891.
64. Cisse, B., M. L. Caton, M. Lehner, T. Maeda, S. Scheu, R. Locksley, D. Holmberg, C. Zweier, N. S. den Hollander, S. G. Kant, et al. 2008. Transcription factor E2-2 is an essential and specific regulator of plasmacytoid dendritic cell development. Cell 135: 37-48.
65. Waskow, C., K. Liu, G. Darrasse-Jèze, P. Guermonprez, F. Ginhoux, M. Merad, T. Shengelia, K. Yao, and M. Nussenzweig. 2008. The receptor tyrosine kinase Flt3 is required for dendritic cell development in peripheral lymphoid tissues. Nat. Immunol. 9: 676-683.
66. Sathaliyawala, T., W. E. O'Gorman, M. Greter, M. Bogunovic, V. Konjufca, Z. E. Hou, G. P. Nolan, M. J. Miller, M. Merad, and B. Reizis. 2010. Mammalian target of rapamycin controls dendritic cell development downstream of Flt3 ligand signaling. Immunity 33: 597-606.
67. Gilliet, M., W. Cao, and Y. J. Liu. 2008. Plasmacytoid dendritic cells: sensing nucleic acids in viral infection and autoimmune diseases. Nat. Rev. Immunol. 8: 594-606.
68. Salomon, B., D. J. Lenschow, L. Rhee, N. Ashourian, B. Singh, A. Sharpe, and J. A. Bluestone. 2000. B7/CD28 costimulation is essential for the homeostasis of the CD4+CD25+ immunoregulatory T cells that control autoimmune diabetes. Immunity 12: 431-440.
69. Schmidt, J., K. Elflein, M. Stienekemeier, M. Rodriguez-Palmero, C. Schneider, K. V. Toyka, R. Gold, and T. Hunig. 2003. Treatment and prevention of experimental autoimmune neuritis with superagonistic CD28-specific monoclonal antibodies. J. Neuroimmunol. 140: 143-152.
70. Finck, B. K., P. S. Linsley, and D. Wofsy. 1994. Treatment of murine lupus with CTLA4Ig. Science 265: 1225-1227.
71. Peterson, K. E., G. C. Sharp, H. Tang, and H. Braley-Mullen. 1999. B7.2 has opposing roles during the activation versus effector stages of experimental autoimmune thyroiditis. J. Immunol. 162: 1859-1867.
72. Tada, Y., K. Nagasawa, A. Ho, F. Morito, O. Ushiyama, N. Suzuki, H. Ohta, and T. W. Mak. 1999. CD28-deficient mice are highly resistant to collagen-induced arthritis. J. Immunol. 162: 203-208.