Type I interferons and NK cells restrict gammaherpesvirus lymph node infection

Journal of Virology

Volumn 90, Issue 20, 2016, Pages 9046-9057

  Lawler, Clara ^a   Tan, Cindy S E ^a   Simas, J Pedro ^b   Stevenson, Philip G ^a  

^a ROYAL CHILDREN'S HOSPITAL   (Australia)

^b INSTITUTO DE MEDICINA MOLECULAR   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; GAMMAHERPESVIRINAE; INNATE IMMUNITY; LYMPHADENOPATHY; LYSIS; MACROPHAGE; MOUSE; MURINE HERPESVIRUS 4; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; SUBCAPSULAR SINUS MACROPHAGE; VIRION; VIRUS INHIBITION; VIRUS REPLICATION; VIRUS TRANSMISSION; ANIMAL; HERPES VIRUS INFECTION; IMMUNOLOGY; LYMPH NODE; RHADINOVIRUS; VIROLOGY; VIRUS INFECTION;

ANIMALS; HERPESVIRIDAE INFECTIONS; INTERFERON TYPE I; KILLER CELLS, NATURAL; LYMPH NODES; MACROPHAGES; MICE; RHADINOVIRUS; TUMOR VIRUS INFECTIONS;

EID: 84990068723     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01108-16     Document Type: Article

References (63)

1. Cesarman E, Mesri EA. 2007. Kaposi sarcoma-associated herpesvirus and other viruses in human lymphomagenesis. Curr Top Microbiol Immunol 312:263-287.
2. Joseph AM, Babcock GJ, Thorley-Lawson DA. 2000. Cells expressing the Epstein-Barr virus growth program are present in and restricted to the naive B-cell subset of healthy tonsils. J Virol 74:9964-9971. http://dx.doi.org/10.1128/JVI.74.21.9964-9971.2000.
3. Balfour HH. 2014. Progress, prospects, and problems in Epstein-Barr virus vaccine development. Curr Opin Virol 6:1-5. http://dx.doi.org/10.1016/j.coviro.2014.02.005.
4. Dunmire SK, Grimm JM, Schmeling DO, Balfour HH, Jr, Hogquist KA. 2015 The incubation period of primary Epstein-Barr virus infection: viral dynamics and immunologic events. PLoS Pathog 11:e1005286. http://dx.doi.org/10.1371/journal.ppat.1005286.
5. McGeoch DJ. 2001. Molecular evolution of the gamma-Herpesvirinae. Philos Trans R Soc Lond B Biol Sci 356:421-435. http://dx.doi.org/10.1098/rstb.2000.0775.
6. Stevenson PG, Simas JP, Efstathiou S. 2009. Immune control of mammalian gamma-herpesviruses: lessons from murid herpesvirus-4. J Gen Virol 90:2317-2330. http://dx.doi.org/10.1099/vir.0.013300-0.
7. Virgin HW, Latreille P, Wamsley P, Hallsworth K, Weck KE, Dal Canto AJ, Speck SH. 1997. Complete sequence and genomic analysis of murine gammaherpesvirus 68. J Virol 71:5894-5904.
8. Goodnow CC. 1992. Transgenic mice and analysis of B-cell tolerance. Annu Rev Immunol 10:489-518. http://dx.doi.org/10.1146/annurev.iy.10.040192.002421.
9. Garside P, Brewer JM. 2008. Real-time imaging of the cellular interactions underlying tolerance, priming, and responses to infection. Immunol Rev 221:130-146. http://dx.doi.org/10.1111/j.1600-065X.2008.00587.x.
10. Gaspar M, May JS, Sukla S, Frederico B, Gill MB, Smith CM, Belz GT, Stevenson PG. 2011. Murid herpesvirus-4 exploits dendritic cells to infect B cells. PLoS Pathog 7:e1002346. http://dx.doi.org/10.1371/journal.ppat.1002346.
11. Frederico B, Milho R, May JS, Gillet L, Stevenson PG. 2012. Myeloid infection links epithelial and B cell tropisms of murid herpesvirus-4. PLoS Pathog 8:e1002935. http://dx.doi.org/10.1371/journal.ppat.1002935.
12. Frederico B, Chao B, May JS, Belz GT, Stevenson PG. 2014. A murid gamma-herpesviruses exploits normal splenic immune communication routes for systemic spread. Cell Host Microbe 15:457-470. http://dx.doi.org/10.1016/j.chom.2014.03.010.
13. Lawler C, Milho R, May JS, Stevenson PG. 2015. Rhadinovirus host entry by co-operative infection. PLoS Pathog 11:e1004761. http://dx.doi.org/10.1371/journal.ppat.1004761.
14. Rosa GT, Gillet L, Smith CM, de Lima BD, Stevenson PG. 2007. IgG fc receptors provide an alternative infection route for murine gammaherpesvirus-68 PLoS One 2:e560. http://dx.doi.org/10.1371/journal.pone.0000560.
15. Carrasco YR, Batista FD. 2007. B cells acquire particulate antigen in a macrophage-rich area at the boundary between the follicle and the subcapsular sinus of the lymph node. Immunity 27:160-171. http://dx.doi.org/10.1016/j.immuni.2007.06.007.
16. Frederico B, Chao B, Lawler C, May JS, Stevenson PG. 2015. Subcapsular sinus macrophages limit acute gammaherpesvirus dissemination. J Gen Virol 96:2314-2327. http://dx.doi.org/10.1099/vir.0.000140.
17. Kuka M, Iannacone M. 2014. The role of lymph node sinus macrophages in host defense. Ann N Y Acad Sci 1319:38-46. http://dx.doi.org/10.1111/nyas.12387.
18. Iannacone M, Moseman EA, Tonti E, Bosurgi L, Junt T, Henrickson SE, Whelan SP, Guidotti LG, von Andrian UH. 2010. Subcapsular sinus macrophages prevent CNS invasion on peripheral infection with a neurotropic virus. Nature 465:1079-1083. http://dx.doi.org/10.1038/nature09118.
19. Honke N, Shaabani N, Cadeddu G, Sorg UR, Zhang DE, Trilling M, Klingel K, Sauter M, Kandolf R, Gailus N, van Rooijen N, Burkart C, Baldus SE, Grusdat M, Löhning M, Hengel H, Pfeffer K, Tanaka M, Häussinger D, Recher M, Lang PA, Lang KS. 2011. Enforced viral replication activates adaptive immunity and is essential for the control of a cytopathic virus. Nat Immunol 13:51-57. http://dx.doi.org/10.1038/ni.2169.
20. Garcia Z, Lemaître F, van Rooijen N, Albert ML, Levy Y, Schwartz O, Bousso P. 2012. Subcapsular sinus macrophages promote NK cell accumulation and activation in response to lymph-borne viral particles. Blood 120:4744-4750. http://dx.doi.org/10.1182/blood-2012-02-408179.
21. Randall RE, Goodbourn S. 2008. Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J Gen Virol 89:1-47. http://dx.doi.org/10.1099/vir.0.83391-0.
22. Milho R, Frederico B, Efstathiou S, Stevenson PG. 2012. A heparandependent herpesvirus targets the olfactory neuroepithelium for host entry. PLoS Pathog 8:e1002986. http://dx.doi.org/10.1371/journal.ppat.1002986.
23. Hwang S, Kim KS, Flano E, Wu TT, Tong LM, Park AN, Song MJ, Sanchez DJ, O'Connell RM, Cheng G, Sun R. 2009. Conserved herpesviral kinase promotes viral persistence by inhibiting the IRF-3-mediated type I interferon response. Cell Host Microbe 5:166-178. http://dx.doi.org/10.1016/j.chom.2008.12.013.
24. Kang HR, Cheong WC, Park JE, Ryu S, Cho HJ, Youn H, Ahn JH, Song MJ. 2014. Murine gammaherpesvirus 68 encoding open reading frame 11 targets TANK binding kinase 1 to negatively regulate the host type I interferon response. J Virol 88:6832-6846. http://dx.doi.org/10.1128/JVI.03460-13.
25. Leang RS, Wu TT, Hwang S, Liang LT, Tong L, Truong JT, Sun R. 2011. The anti interferon activity of conserved viral dUTPase ORF54 is essential for an effective MHV-68 infection. PLoS Pathog 7:e1002292. http://dx.doi.org/10.1371/journal.ppat.1002292.
26. Liang X, Shin YC, Means RE, Jung JU. 2004. Inhibition of interferonmediated antiviral activity by murine gammaherpesvirus 68 latencyassociated M2 protein. J Virol 78:12416-12427. http://dx.doi.org/10.1128/JVI.78.22.12416-12427.2004.
27. Sheridan V, Polychronopoulos L, Dutia BM, Ebrahimi B. 2014. A shutoff and exonuclease mutant of murine gammaherpesvirus-68 yields infectious virus and causes RNA loss in type I interferon receptor knockout cells. J Gen Virol 95:1135-1143. http://dx.doi.org/10.1099/vir.0.059329-0.
28. Ku B, Woo JS, Liang C, Lee KH, Hong HS, E X, Kim KS, Jung JU, Oh BH. 2008. Structural and biochemical bases for the inhibition of autophagy and apoptosis by viral BCL-2 of murine gamma-herpesvirus 68. PLoS Pathog 4:e25. http://dx.doi.org/10.1371/journal.ppat.0040025.
29. Zhao J, He S, Minassian A, Li J, Feng P. 2015. Recent advances on viral manipulation of NF-κB signaling pathway. Curr Opin Virol 15:103-111. http://dx.doi.org/10.1016/j.coviro.2015.08.013.
30. Gaspar M, Gill MB, Lösing JB, May JS, Stevenson PG. 2008. Multiple functions for ORF75c in murid herpesvirus-4 infection. PLoS One 3:e2781. http://dx.doi.org/10.1371/journal.pone.0002781.
31. Ling PD, Tan J, Sewatanon J, Peng R. 2008. Murine gammaherpesvirus 68 open reading frame 75c tegument protein induces the degradation of PML and is essential for production of infectious virus. J Virol 82:8000-8012 http://dx.doi.org/10.1128/JVI.02752-07.
32. Weck KE, Dal Canto AJ, Gould JD, O'Guin AK, Roth KA, Saffitz JE, Speck SH, Virgin HW. 1997. Murine gamma-herpesvirus 68 causes severe large-vessel arteritis in mice lacking interferon-gamma responsiveness: a new model for virus-induced vascular disease. Nat Med 3:1346-1353 http://dx.doi.org/10.1038/nm1297-1346.
33. Dutia BM, Allen DJ, Dyson H, Nash AA. 1999. Type I interferons and IRF-1 play a critical role in the control of a gammaherpesvirus infection. Virology 261:173-179. http://dx.doi.org/10.1006/viro.1999.9834.
34. Mandal P, Krueger BE, Oldenburg D, Andry KA, Beard RS, White DW, Barton ES. 2011. A gammaherpesvirus cooperates with interferon-alpha/ beta-induced IRF2 to halt viral replication, control reactivation, and min-imize host lethality. PLoS Pathog 7:e1002371. http://dx.doi.org/10.1371/journal.ppat.1002371.
35. May JS, Coleman HM, Smillie B, Efstathiou S, Stevenson PG. 2004. Forced lytic replication impairs host colonization by a latency-deficient mutant of murine gammaherpesvirus-68. J Gen Virol 85:137-146. http://dx.doi.org/10.1099/vir.0.19599-0.
36. Tan CS, Lawler C, May JS, Belz GT, Stevenson PG. 2016. Type I interferons direct gammaherpesvirus host colonization. PLoS Pathog 12: e1005654. http://dx.doi.org/10.1371/journal.ppat.1005654.
37. Clausen BE, Burkhardt C, Reith W, Renkawitz R, Förster I. 1999. Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res 8:265-277. http://dx.doi.org/10.1023/A:1008942828960.
38. Caton ML, Smith-Raska MR, Reizis B. 2007. Notch-RBP-J signaling controls the homeostasis of CD8+ dendritic cells in the spleen. J Exp Med 204:1653-1664. http://dx.doi.org/10.1084/jem.20062648.
39. Van Rooijen N, Sanders A. 1994. Liposome mediated depletion of macrophages: mechanism of action, preparation of liposomes and applications. J Immunol Methods 174:83-93. http://dx.doi.org/10.1016/0022-1759(94)90012-4.
40. Milho R, Smith CM, Marques S, Alenquer M, May JS, Gillet L, Gaspar M, Efstathiou S, Simas JP, Stevenson PG. 2009. In vivo imaging of murid herpesvirus-4 infection. J Gen Virol 90:21-32. http://dx.doi.org/10.1099/vir.0.006569-0.
41. May JS, Stevenson PG. 2010. Vaccination with murid herpesvirus-4 glycoprotein B reduces viral lytic replication but does not induce detectable virion neutralization. J Gen Virol 91:2542-2552. http://dx.doi.org/10.1099/vir.0.023085-0.
42. de Lima BD, May JS, Stevenson PG. 2004. Murine gammaherpesvirus 68 lacking gp150 shows defective virion release but establishes normal latency in vivo. J Virol 78:5103-5112. http://dx.doi.org/10.1128/JVI.78.10.5103-5112.2004.
43. Gillet L, Adler H, Stevenson PG. 2007. Glycosaminoglycan interactions in murine gammaherpesvirus-68 infection. PLoS One 2:e347. http://dx.doi.org/10.1371/journal.pone.0000347.
44. Swiecki M, Colonna M. 2015. The multifaceted biology of plasmacytoid dendritic cells. Nat Rev Immunol 15:471-485. http://dx.doi.org/10.1038/nri3865.
45. Asselin-Paturel C, Brizard G, Pin J-J, Briere F, Trinchieri G. 2003. Mouse strain differences in plasmacytoid dendritic cell frequency and function revealed by a novel monoclonal antibody. J Immunol 171:6466-6477 http://dx.doi.org/10.4049/jimmunol.171.12.6466.
46. Gaya M, Castello A, Montaner B, Rogers N, Reis e Sousa C, Bruckbauer A, Batista FD. 2015. Host response. Inflammation-induced disruption of SCS macrophages impairs B cell responses to secondary infection. Science 347:667-672. http://dx.doi.org/10.1126/science.aaa1300.
47. Martinez-Pomares L, Platt N, McKnight AJ, da Silva RP, Gordon S. 1996 Macrophage membrane molecules: markers of tissue differentiation and heterogeneity. Immunobiology 195:407-416. http://dx.doi.org/10.1016/S0171-2985(96)80012-X.
48. Simas JP, Swann D, Bowden R, Efstathiou S. 1999. Analysis of murine gammaherpesvirus-68 transcription during lytic and latent infection. J Gen Virol 80:75-82. http://dx.doi.org/10.1099/0022-1317-80-1-75.
49. van Berkel V, Preiter K, Virgin HW, Speck SH. 1999. Identification and initial characterization of the murine gammaherpesvirus 68 gene M3, encoding an abundantly secreted protein. J Virol 73:4524-4529.
50. Marques S, Efstathiou S, Smith KG, Haury M, Simas JP. 2003. Selective gene expression of latent murine gammaherpesvirus 68 in B lymphocytes. J Virol 77:7308-7318. http://dx.doi.org/10.1128/JVI.77.13.7308-7318.2003.
51. Stevenson PG, Doherty PC. 1998. Kinetic analysis of the specific host response to a murine gammaherpesvirus. J Virol 72:943-949.
52. Lisnić B, Lisnić VJ, Jonjić S. 2015. NK cell interplay with cytomegaloviruses. Curr Opin Virol 15:9-18. http://dx.doi.org/10.1016/j.coviro.2015.07.001.
53. Kastenmüller W, Torabi-Parizi P, Subramanian N, Lämmermann T, Germain RN. 2012. A spatially-organized multicellular innate immune response in lymph nodes limits systemic pathogen spread. Cell 150:1235-1248 http://dx.doi.org/10.1016/j.cell.2012.07.021.
54. Usherwood EJ, Meadows SK, Crist SG, Bellfy SC, Sentman CL. 2005. Control of murine gammaherpesvirus infection is independent of NK cells. Eur J Immunol 35:2956-2961. http://dx.doi.org/10.1002/eji.200526245.
55. Carneiro-Sampaio M, Coutinho A. 2007. Immunity to microbes: lessons from primary immunodeficiencies. Infect Immun 75:1545-1555. http://dx.doi.org/10.1128/IAI.00787-06.
56. Hislop AD. 2015. Early virological and immunological events in Epstein-Barr virus infection. Curr Opin Virol 15:75-79. http://dx.doi.org/10.1016/j.coviro.2015.08.002.
57. Chijioke O, Müller A, Feederle R, Barros MH, Krieg C, Emmel V, Marcenaro E, Leung CS, Antsiferova O, Landtwing V, Bossart W, Moretta A, Hassan R, Boyman O, Niedobitek G, Delecluse HJ, Capaul R, Münz C. 2013. Human natural killer cells prevent infectious mononucleosis features by targeting lytic Epstein-Barr virus infection. Cell Rep 5:1489-1498. http://dx.doi.org/10.1016/j.celrep.2013.11.041.
58. Smith CM, Gill MB, May JS, Stevenson PG. 2007. Murine gammaherpesvirus-68 inhibits antigen presentation by dendritic cells. PLoS One 2:e1048. http://dx.doi.org/10.1371/journal.pone.0001048.
59. Moltedo B, Li W, Yount JS, Moran TM. 2011. Unique type I interferon responses determine the functional fate of migratory lung dendritic cells during influenza virus infection. PLoS Pathog 7:e1002345. http://dx.doi.org/10.1371/journal.ppat.1002345.
60. Cardin RD, Brooks JW, Sarawar SR, Doherty PC. 1996. Progressive loss of CD8+ T cell-mediated control of a gamma-herpesvirus in the absence of CD4+ T cells. J Exp Med 184:863-871. http://dx.doi.org/10.1084/jem.184.3.863.
61. Smith CM, Wilson NS, Waithman J, Villadangos JA, Carbone FR, Heath WR, Belz GT. 2004. Cognate CD4+ T cell licensing of dendritic cells in CD8+ T cell immunity. Nat Immunol 5:1143-1148. http://dx.doi.org/10.1038/ni1129.
62. Christensen JP, Cardin RD, Branum KC, Doherty PC. 1999. CD4+ T cell-mediated control of a gamma-herpesvirus in B cell-deficient mice is mediated by IFN-gamma. Proc Natl Acad Sci U S A 96:5135-5140. http://dx.doi.org/10.1073/pnas.96.9.5135.
63. Schroder K, Hertzog PJ, Ravasi T, Hume DA. 2004. Interferongamma: an overview of signals, mechanisms and functions. J Leukoc Biol 75:163-189.