Type I and Type II Interferon Coordinately Regulate Suppressive Dendritic Cell Fate and Function during Viral Persistence

PLoS Pathogens

Volumn 12, Issue 1, 2016, Pages

  Cunningham, Cameron R ^a   Champhekar, Ameya ^a   Tullius, Michael V ^b   Dillon, Barbara Jane ^b   Zhen, Anjie ^b   de la Fuente, Justin Rafael ^a   Herskovitz, Jonathan ^a   Elsaesser, Heidi ^a,c   Snell, Laura M ^a,c   Wilson, Elizabeth B ^a,f   de la Torre, Juan Carlos ^d   Kitchen, Scott G ^b   Horwitz, Marcus A ^a,b   Bensinger, Steven J ^a,b   Smale, Stephen T ^a   Brooks, David G ^a,c,e  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c PRINCESS MARGARET HOSPITAL   (Canada)

^d SCRIPPS RESEARCH INSTITUTE   (United States)

^e UNIVERSITY OF TORONTO   (Canada)

^f Agensys Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERFERON; INTERLEUKIN 10; PROGRAMMED DEATH 1 LIGAND 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL CYCLE PROGRESSION; CELL FATE; CELL FUNCTION; CELLULAR IMMUNITY; CONTROLLED STUDY; DENDRITIC CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RESPONSE; IMMUNOSUPPRESSIVE TREATMENT; IN VITRO STUDY; INFLAMMATION; MOUSE; NEOPLASM; NONHUMAN; PATHOGENESIS; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; RNA SEQUENCE; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; TUBERCULOSIS; VIRUS INFECTION; ANIMAL; C57BL MOUSE; DISEASE MODEL; DNA MICROARRAY; HUMAN IMMUNODEFICIENCY VIRUS; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; KNOCKOUT MOUSE; LYMPHOCYTIC CHORIOMENINGITIS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; T LYMPHOCYTE;

ANIMALS; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HIV; HIV INFECTIONS; IMMUNE TOLERANCE; INTERFERONS; LYMPHOCYTIC CHORIOMENINGITIS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEOPLASMS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REAL-TIME POLYMERASE CHAIN REACTION; T-LYMPHOCYTES; TUBERCULOSIS; VIRUS DISEASES;

EID: 84956771914     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005356     Document Type: Article

References (55)

1. Wherry EJ, T cell exhaustion. Nat Immunol. 2011;12(6):492–9. Epub 2011/07/09. 21739672
2. Barber DL, Wherry EJ, Masopust D, Zhu B, Allison JP, Sharpe AH, et al. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature. 2006;439(7077):682–7. 16382236
3. Brooks DG, Trifilo MJ, Edelmann KH, Teyton L, McGavern DB, Oldstone MB, Interleukin-10 determines viral clearance or persistence in vivo. Nat Med. 2006;12(11):1301–9. 17041596
4. Ejrnaes M, Filippi CM, Martinic MM, Ling EM, Togher LM, Crotty S, et al. Resolution of a chronic viral infection after interleukin-10 receptor blockade. J Exp Med. 2006;203(11):2461–72. 17030951
5. Snell LM, Brooks DG, New insights into type I interferon and the immunopathogenesis of persistent viral infections. Curr Opin Immunol. 2015;34:91–8. doi: 10.1016/j.coi.2015.03.002 25771184
6. Wilson EB, Kidani Y, Elsaesser H, Barnard J, Raff L, Karp CL, et al. Emergence of Distinct Multiarmed Immunoregulatory Antigen-Presenting Cells during Persistent Viral Infection. Cell Host Microbe. 2012;11(5):481–91. Epub 2012/05/23. doi: 10.1016/j.chom.2012.03.009 22607801
7. Norris BA, Uebelhoer LS, Nakaya HI, Price AA, Grakoui A, Pulendran B, Chronic but not acute virus infection induces sustained expansion of myeloid suppressor cell numbers that inhibit viral-specific T cell immunity. Immunity. 2013;38(2):309–21. Epub 2013/02/27. doi: 10.1016/j.immuni.2012.10.022 23438822
8. Sedaghat AR, German J, Teslovich TM, Cofrancesco J, Jr.Jie CC, Talbot CC, Jr.et al. Chronic CD4+ T-cell activation and depletion in human immunodeficiency virus type 1 infection: type I interferon-mediated disruption of T-cell dynamics. J Virol. 2008;82(4):1870–83. Epub 2007/12/14. 18077723
9. Sauce D, Elbim C, Appay V, Monitoring cellular immune markers in HIV infection: from activation to exhaustion. Curr Opin HIV AIDS. 2013;8(2):125–31. Epub 2013/02/06. doi: 10.1097/COH.0b013e32835d08a9 23380653
10. Wilson EB, Yamada DH, Elsaesser H, Herskovitz J, Deng J, Cheng G, et al. Blockade of chronic type I interferon signaling to control persistent LCMV infection. Science. 2013;340(6129):202–7. Epub 2013/04/13. doi: 10.1126/science.1235208 23580528
11. Teijaro JR, Ng C, Lee AM, Sullivan BM, Sheehan KC, Welch M, et al. Persistent LCMV infection is controlled by blockade of type I interferon signaling. Science. 2013;340(6129):207–11. Epub 2013/04/13. doi: 10.1126/science.1235214 23580529
12. Ohyagi H, Onai N, Sato T, Yotsumoto S, Liu J, Akiba H, et al. Monocyte-Derived Dendritic Cells Perform Hemophagocytosis to Fine-Tune Excessive Immune Responses. Immunity. 2013. Epub 2013/09/17.
13. Pauken KE, Wherry EJ, Overcoming T cell exhaustion in infection and cancer. Trends Immunol. 2015;36(4):265–76. doi: 10.1016/j.it.2015.02.008 25797516
14. McNab F, Mayer-Barber K, Sher A, Wack A, O'Garra A, Type I interferons in infectious disease. Nat Rev Immunol. 2015;15(2):87–103. doi: 10.1038/nri3787 25614319
15. Motz GT, Coukos G, Deciphering and reversing tumor immune suppression. Immunity. 2013;39(1):61–73. doi: 10.1016/j.immuni.2013.07.005 23890064
16. Fahey LM, Brooks DG, Opposing positive and negative regulation of T cell activity during viral persistence. Curr Opin Immunol. 2010;22:348–54. Epub 2010/04/13. doi: 10.1016/j.coi.2010.03.004 20381328
17. Ahmed R, Salmi A, Butler LD, Chiller JM, Oldstone MB, 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. 1984;160(2):521–40. 6332167
18. Maynard CL, Harrington LE, Janowski KM, Oliver JR, Zindl CL, Rudensky AY, et al. Regulatory T cells expressing interleukin 10 develop from Foxp3+ and Foxp3- precursor cells in the absence of interleukin 10. Nat Immunol. 2007;8(9):931–41. 17694059
19. Mascanfroni ID, Yeste A, Vieira SM, Burns EJ, Patel B, Sloma I, et al. IL-27 acts on DCs to suppress the T cell response and autoimmunity by inducing expression of the immunoregulatory molecule CD39. Nat Immunol. 2013;14(10):1054–63. Epub 2013/09/03. doi: 10.1038/ni.2695 23995234
20. Rothlin CV, Carrera-Silva EA, Bosurgi L, Ghosh S, TAM receptor signaling in immune homeostasis. Annu Rev Immunol. 2015;33:355–91. doi: 10.1146/annurev-immunol-032414-112103 25594431
21. Gett AV, Hodgkin PD, A cellular calculus for signal integration by T cells. Nat Immunol. 2000;1(3):239–44. 10973282
22. Ng CT, Oldstone MB, Infected CD8alpha- dendritic cells are the predominant source of IL-10 during establishment of persistent viral infection. Proc Natl Acad Sci U S A. 2012;109(35):14116–21. Epub 2012/08/16. doi: 10.1073/pnas.1211910109 22893686
23. Baca Jones C, Filippi C, Sachithanantham S, Rodriguez-Calvo T, Ehrhardt K, von Herrath M, Direct infection of dendritic cells during chronic viral infection suppresses antiviral T cell proliferation and induces IL-10 expression in CD4 T cells. PLoS One. 2014;9(3):e90855. doi: 10.1371/journal.pone.0090855 24613988
24. Emonet SF, Garidou L, McGavern DB, de la Torre JC, Generation of recombinant lymphocytic choriomeningitis viruses with trisegmented genomes stably expressing two additional genes of interest. Proc Natl Acad Sci U S A. 2009;106(9):3473–8. Epub 2009/02/12. doi: 10.1073/pnas.0900088106 19208813
25. Ng CT, Sullivan BM, Teijaro JR, Lee AM, Welch M, Rice S, et al. Blockade of interferon Beta, but not interferon alpha, signaling controls persistent viral infection. Cell Host Microbe. 2015;17(5):653–61. doi: 10.1016/j.chom.2015.04.005 25974304
26. Clingan JM, Ostrow K, Hosiawa KA, Chen ZJ, Matloubian M, Differential roles for RIG-I-like receptors and nucleic acid-sensing TLR pathways in controlling a chronic viral infection. J Immunol. 2012;188(9):4432–40. Epub 2012/03/27. doi: 10.4049/jimmunol.1103656 22447976
27. Wang Y, Swiecki M, Cella M, Alber G, Schreiber RD, Gilfillan S, et al. Timing and Magnitude of Type I Interferon Responses by Distinct Sensors Impact CD8 T Cell Exhaustion and Chronic Viral Infection. Cell Host Microbe. 2012;11(6):631–42. Epub 2012/06/19. doi: 10.1016/j.chom.2012.05.003 22704623
28. Segura E, Amigorena S, Inflammatory dendritic cells in mice and humans. Trends Immunol. 2013;34(9):440–5. doi: 10.1016/j.it.2013.06.001 23831267
29. Redford PS, Boonstra A, Read S, Pitt J, Graham C, Stavropoulos E, et al. Enhanced protection to Mycobacterium tuberculosis infection in IL-10-deficient mice is accompanied by early and enhanced Th1 responses in the lung. Eur J Immunol. 2010;40(8):2200–10. Epub 2010/06/03. doi: 10.1002/eji.201040433 20518032
30. Berry MP, Graham CM, McNab FW, Xu Z, Bloch SA, Oni T, et al. An interferon-inducible neutrophil-driven blood transcriptional signature in human tuberculosis. Nature. 2010;466(7309):973–7. doi: 10.1038/nature09247 20725040
31. Flynn JL, Chan J, Triebold KJ, Dalton DK, Stewart TA, Bloom BR, An essential role for interferon gamma in resistance to Mycobacterium tuberculosis infection. J Exp Med. 1993;178(6):2249–54. Epub 1993/12/01. 7504064
32. Mayer-Barber KD, Andrade B, Oland S, Amaral E, Barber DL, Gonzales J, et al. Host-directed therapy of tuberculosis based on interleuki-1 and type I interferon crosstalk. Nature. 2014.
33. Topalian SL, Drake CG, Pardoll DM, Immune checkpoint blockade: a common denominator approach to cancer therapy. Cancer Cell. 2015;27(4):450–61. doi: 10.1016/j.ccell.2015.03.001 25858804
34. Hahm B, Trifilo MJ, Zuniga EI, Oldstone MB, Viruses evade the immune system through type I interferon-mediated STAT2-dependent, but STAT1-independent, signaling. Immunity. 2005;22(2):247–57. 15723812
35. Buisson S, Benlahrech A, Gazzard B, Gotch F, Kelleher P, Patterson S, Monocyte-derived dendritic cells from HIV type 1-infected individuals show reduced ability to stimulate T cells and have altered production of interleukin (IL)-12 and IL-10. J Infect Dis. 2009;199(12):1862–71. doi: 10.1086/599122 19419334
36. Miller E, Bhardwaj N, Dendritic cell dysregulation during HIV-1 infection. Immunol Rev. 2013;254(1):170–89. Epub 2013/06/19. doi: 10.1111/imr.12082 23772620
37. Averill L, Lee WM, Karandikar NJ, Differential dysfunction in dendritic cell subsets during chronic HCV infection. Clin Immunol. 2007;123(1):40–9. 17239662
38. Park SJ, Hahn YS, Regulation of host innate immunity by hepatitis C virus: crosstalk between hepatocyte and NK/DC. Rev Infect. 2010;1(3):151–7. 24688607
39. Tran Janco JM, Lamichhane P, Karyampudi L, Knutson KL, Tumor-infiltrating dendritic cells in cancer pathogenesis. J Immunol. 2015;194(7):2985–91. doi: 10.4049/jimmunol.1403134 25795789
40. Brooks DG, McGavern DB, Oldstone MB, Reprogramming of antiviral T cells prevents inactivation and restores T cell activity during persistent viral infection. J Clin Invest. 2006;116:1675–85. 16710479
41. Blackburn SD, Shin H, Freeman GJ, Wherry EJ, Selective expansion of a subset of exhausted CD8 T cells by alphaPD-L1 blockade. Proc Natl Acad Sci U S A. 2008;105(39):15016–21. Epub 2008/09/24. doi: 10.1073/pnas.0801497105 18809920
42. Fisicaro P, Valdatta C, Massari M, Loggi E, Biasini E, Sacchelli L, et al. Antiviral intrahepatic T-cell responses can be restored by blocking programmed death-1 pathway in chronic hepatitis B. Gastroenterology. 2010;138(2):682–93, 93 e1–4. doi: 10.1053/j.gastro.2009.09.052 19800335
43. Nakamoto N, Kaplan DE, Coleclough J, Li Y, Valiga ME, Kaminski M, et al. Functional restoration of HCV-specific CD8 T cells by PD-1 blockade is defined by PD-1 expression and compartmentalization. Gastroenterology. 2008;134(7):1927–37, 37 e1–2. Epub 2008/06/14. doi: 10.1053/j.gastro.2008.02.033 18549878
44. Jiang Y, Li Y, Zhu B, T-cell exhaustion in the tumor microenvironment. Cell Death Dis. 2015;6:e1792. doi: 10.1038/cddis.2015.162 26086965
45. Bosschaerts T, Guilliams M, Stijlemans B, Morias Y, Engel D, Tacke F, et al. Tip-DC development during parasitic infection is regulated by IL-10 and requires CCL2/CCR2, IFN-gamma and MyD88 signaling. PLoS Pathog. 2010;6(8):e1001045. Epub 2010/08/18. doi: 10.1371/journal.ppat.1001045 20714353
46. De Trez C, Magez S, Akira S, Ryffel B, Carlier Y, Muraille E, 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. 2009;5(6):e1000494. Epub 2009/06/27. doi: 10.1371/journal.ppat.1000494 19557162
47. Varanasi V, Khan AA, Chervonsky AV, Loss of the death receptor CD95 (Fas) expression by dendritic cells protects from a chronic viral infection. Proc Natl Acad Sci U S A. 2014;111(23):8559–64. Epub 2014/06/10. doi: 10.1073/pnas.1401750111 24912151
48. Zinselmeyer BH, Heydari S, Sacristan C, Nayak D, Cammer M, Herz J, et al. PD-1 promotes immune exhaustion by inducing antiviral T cell motility paralysis. J Exp Med. 2013;210(4):757–74. Epub 2013/03/27. doi: 10.1084/jem.20121416 23530125
49. Richter K, Perriard G, Behrendt R, Schwendener RA, Sexl V, Dunn R, et al. Macrophage and T cell produced IL-10 promotes viral chronicity. PLoS Pathog. 2013;9(11):e1003735. doi: 10.1371/journal.ppat.1003735 24244162
50. Oxenius A, Bachmann MF, Zinkernagel RM, Hengartner H, Virus-specific MHC-class II-restricted TCR-transgenic mice: effects on humoral and cellular immune responses after viral infection. Eur J Immunol. 1998;28(1):390–400. 9485218
51. Brooks DG, Teyton L, Oldstone MB, McGavern DB, Intrinsic functional dysregulation of CD4 T cells occurs rapidly following persistent viral infection. Journal of Virology. 2005;79(16):10514–27. 16051844
52. Kitchen SG, Levin BR, Bristol G, Rezek V, Kim S, Aguilera-Sandoval C, et al. In vivo suppression of HIV by antigen specific T cells derived from engineered hematopoietic stem cells. PLoS Pathog. 2012;8(4):e1002649. Epub 2012/04/19. doi: 10.1371/journal.ppat.1002649 22511873
53. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL, TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 2013;14(4):R36. doi: 10.1186/gb-2013-14-4-r36 23618408
54. Anders S, Pyl PT, Huber W, HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics. 2015;31(2):166–9. doi: 10.1093/bioinformatics/btu638 25260700
55. D'Andrea D, Grassi L, Mazzapioda M, Tramontano A, FIDEA: a server for the functional interpretation of differential expression analysis. Nucleic Acids Res. 2013;41(Web Server issue):W84–8. doi: 10.1093/nar/gkt516 23754850