Sensing of latent EBV infection through exosomal transfer of 5'pppRNA

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 5, 2016, Pages E587-E596

  Baglio, S Rubina ^a   Van Eijndhoven, Monique A J ^a   Koppers Lalic, Danijela ^a   Berenguer, Jordi ^a   Lougheed, Sinéad M ^b   Gibbs, Susan ^a,c   Léveillé, Nicolas ^d   Rinkel, Rico N P M ^a   Hopmans, Erik S ^a   Swaminathan, Sankar ^e   Verkuijlen, Sandra A W M ^a   Scheffer, George L ^a   Van Kuppeveld, Frank J M ^f   De Gruijl, Tanja D ^b   Bultink, Irene E M ^b   Jordanova, Ekaterina S ^b   Hackenberg, Michael ^g   Piersma, Sander R ^a   Knol, Jaco C ^a   Voskuyl, Alexandre E ^b   Wurdinger, Thomas ^a   Jiménez, Connie R ^a   Middeldorp, Jaap M ^a   Pegtel, D Michiel ^a   more..

^a Amsterdam Gastroenterology Metabolism   (Netherlands)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

^d ACADEMIC MEDICAL CENTER   (Netherlands)

^e VETERANS AFFAIRS MEDICAL CENTER   (United States)

^f UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^g UNIVERSITY OF GRANADA   (Spain)

Author keywords

Dendritic Cells; EBV EBER; Exosomes; Innate Sensing; Skin Inflammation

Indexed keywords

ANTIGEN; PHOSPHATIDYLSERINE; RIBONUCLEOPROTEIN; RNA; 5'PPP-RNA; PROTEOME; VIRUS RNA;

ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; DENDRITIC CELL; EPSTEIN BARR VIRUS; EPSTEIN BARR VIRUS INFECTION; EX VIVO STUDY; EXOSOME; HUMAN; HUMAN CELL; IN VITRO STUDY; LUPUS ERYTHEMATOSUS; PRIORITY JOURNAL; SKIN DEFECT; TONSIL; VIRUS IMMUNITY; VIRUS LOAD; VIRUS STRAIN; GENETICS; IMMUNOLOGY; METABOLISM; TRANSPORT AT THE CELLULAR LEVEL; VIROLOGY;

BIOLOGICAL TRANSPORT; DENDRITIC CELLS; EPSTEIN-BARR VIRUS INFECTIONS; EXOSOMES; HERPESVIRUS 4, HUMAN; HUMANS; PROTEOME; RNA, VIRAL;

EID: 84956629623     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1518130113     Document Type: Article

References (71)

1. Goubau D, Deddouche S, Reis e Sousa C (2013) Cytosolic sensing of viruses. Immunity 38(5):855-869.
2. Horner SM, Gale M, Jr (2013) Regulation of hepatic innate immunity by hepatitis C virus. Nat Med 19(7):879-888.
3. Dreux M, et al. (2012) Short-range exosomal transfer of viral RNA from infected cells to plasmacytoid dendritic cells triggers innate immunity. Cell Host Microbe 12(4): 558-570.
4. Feng Z, et al. (2015) Human pDCs preferentially sense enveloped hepatitis A virions. J Clin Invest 125(1):169-176.
5. Paludan SR, Bowie AG, Horan KA, Fitzgerald KA (2011) Recognition of herpesviruses by the innate immune system. Nat Rev Immunol 11(2):143-154.
6. Münz C, Lünemann JD, Getts MT, Miller SD (2009) Antiviral immune responses: Triggers of or triggered by autoimmunity? Nat Rev Immunol 9(4):246-258.
7. Lerner MR, Andrews NC, Miller G, Steitz JA (1981) Two small RNAs encoded by Epstein-Barr virus and complexed with protein are precipitated by antibodies from patients with systemic lupus erythematosus. Proc Natl Acad Sci USA 78(2):805-809.
8. Gregorovic G, et al. (2015) Epstein-Barr viruses (EBVs) deficient in EBV-encoded RNAs have higher levels of latentmembrane protein 2 RNA expression in lymphoblastoid cell lines and efficiently establish persistent infections in humanized mice. J Virol 89(22):11711-11714.
9. Iwakiri D, et al. (2009) Epstein-Barr virus (EBV)-encoded small RNA is released from EBV-infected cells and activates signaling from Toll-like receptor 3. J Exp Med 206(10): 2091-2099.
10. Samanta M, Iwakiri D, Takada K (2008) Epstein-Barr virus-encoded small RNA induces IL-10 through RIG-I-mediated IRF-3 signaling. Oncogene 27(30):4150-4160.
11. Ruf IK, Lackey KA, Warudkar S, Sample JT (2005) Protection from interferon-induced apoptosis by Epstein-Barr virus small RNAs is not mediated by inhibition of PKR. J Virol 79(23):14562-14569.
12. Quan TE, Roman RM, Rudenga BJ, Holers VM, Craft JE (2010) Epstein-Barr virus promotes interferon-alpha production by plasmacytoid dendritic cells. Arthritis Rheum 62(6):1693-1701.
13. Kawai T, Akira S (2010) The role of pattern-recognition receptors in innate immunity: Update on Toll-like receptors. Nat Immunol 11(5):373-384.
14. Bowie AG, Fitzgerald KA (2007) RIG-I: Tri-ing to discriminate between self and nonself RNA. Trends Immunol 28(4):147-150.
15. Pichlmair A, et al. (2011) IFIT1 is an antiviral protein that recognizes 5'-triphosphate RNA. Nat Immunol 12(7):624-630.
16. Nallagatla SR, et al. (2007) 5'-triphosphate-dependent activation of PKR by RNAs with short stem-loops. Science 318(5855):1455-1458.
17. Eckard SC, et al. (2014) The SKIV2L RNA exosome limits activation of the RIG-I-like receptors. Nat Immunol 15(9):839-845.
18. Bernard JJ, et al. (2012) Ultraviolet radiation damages self noncoding RNA and is detected by TLR3. Nat Med 18(8):1286-1290.
19. Malathi K, et al. (2010) RNase L releases a small RNA from HCV RNA that refolds into a potent PAMP. RNA 16(11):2108-2119.
20. Stetson DB (2009) Connections between antiviral defense and autoimmunity. Curr Opin Immunol 21(3):244-250.
21. Tycowski KT, et al. (2015) Viral noncoding RNAs: More surprises. Genes Dev 29(6): 567-584.
22. Jochum S, Ruiss R, Moosmann A, Hammerschmidt W, Zeidler R (2012) RNAs in Epstein-Barr virions control early steps of infection. Proc Natl Acad Sci USA 109(21): E1396-E1404.
23. Ahmed W, Philip PS, Tariq S, Khan G (2014) Epstein-Barr virus-encoded small RNAs (EBERs) are present in fractions related to exosomes released by EBV-transformed cells. PLoS One 9(6):e99163.
24. Pegtel DM, van de Garde MD, Middeldorp JM (2011) Viral miRNAs exploiting the endosomal-exosomal pathway for intercellular cross-talk and immune evasion. Biochim Biophys Acta 1809(11-12):715-721.
25. Pegtel DM, et al. (2010) Functional delivery of viral miRNAs via exosomes. Proc Natl Acad Sci USA 107(14):6328-6333.
26. Blanc M, et al. (2011) Host defense against viral infection involves interferon mediated down-regulation of sterol biosynthesis. PLoS Biol 9(3):e1000598.
27. Der SD, Zhou A, Williams BR, Silverman RH (1998) Identification of genes differentially regulated by interferon alpha, beta, or gamma using oligonucleotide arrays. Proc Natl Acad Sci USA 95(26):15623-15628.
28. Li J, et al. (2013) Exosomes mediate the cell-to-cell transmission of IFN-α-induced antiviral activity. Nat Immunol 14(8):793-803.
29. Franceschini A, et al. (2013) STRING v9.1: Protein-protein interaction networks, with increased coverage and integration. Nucleic Acids Res 41(Database issue, D1): D808-D815.
30. Verweij FJ, van Eijndhoven MAJ, Middeldorp J, Pegtel DM (2013) Analysis of viral microRNA exchange via exosomes in vitro and in vivo. Methods Mol Biol 1024:53-68.
31. Yount JS, et al. (2010) Palmitoylome profiling reveals S-palmitoylation-dependent antiviral activity of IFITM3. Nat Chem Biol 6(8):610-614.
32. Felton-Edkins ZA, et al. (2006) Epstein-Barr virus induces cellular transcription factors to allow active expression of EBER genes by RNA polymerase III. J Biol Chem 281(45): 33871-33880.
33. Guiducci C, et al. (2013) RNA recognition by human TLR8 can lead to autoimmune inflammation. J Exp Med 210(13):2903-2919.
34. Swaminathan S, Tomkinson B, Kieff E (1991) Recombinant Epstein-Barr virus with small RNA (EBER) genes deleted transforms lymphocytes and replicates in vitro. Proc Natl Acad Sci USA 88(4):1546-1550.
35. Villarroya-Beltri C, et al. (2013) Sumoylated hnRNPA2B1 controls the sorting of miRNAs into exosomes through binding to specific motifs. Nat Commun 4:2980.
36. Amort M, et al. (2015) Expression of the vault RNA protects cells from undergoing apoptosis. Nat Commun 6(May):7030.
37. Bitko V, Musiyenko A, Bayfield MA, Maraia RJ, Barik S (2008) Cellular La protein shields nonsegmented negative-strand RNA viral leader RNA from RIG-I and enhances virus growth by diverse mechanisms. J Virol 82(16):7977-7987.
38. Mittelbrunn M, Sánchez-Madrid F (2012) Intercellular communication: Diverse structures for exchange of genetic information. Nat Rev Mol Cell Biol 13(5):328-335.
39. Kosaka N, et al. (2010) Secretory mechanisms and intercellular transfer of microRNAs in living cells. J Biol Chem 285(23):17442-17452.
40. Roughan JE, Thorley-Lawson DA (2009) The intersection of Epstein-Barr virus with the germinal center. J Virol 83(8):3968-3976.
41. Yu M, et al. (2015) Expression profile and histological distribution of IFITM1 and IFITM3 during H9N2 avian influenza virus infection in BALB/c mice. Med Microbiol Immunol (Berl) 204(4):505-514.
42. Feeley EM, et al. (2011) IFITM3 inhibits influenza A virus infection by preventing cytosolic entry. PLoS Pathog 7(10):e1002337.
43. Miyanishi M, et al. (2007) Identification of Tim4 as a phosphatidylserine receptor. Nature 450(7168):435-439.
44. Gross AJ, Hochberg D, Rand WM, Thorley-Lawson DA (2005) EBV and systemic lupus erythematosus: A new perspective. J Immunol 174(11):6599-6607.
45. Qiu J, et al. (2011) A novel persistence associated EBV miRNA expression profile is disrupted in neoplasia. PLoS Pathog 7(8):e1002193.
46. Samanta M, Iwakiri D, Kanda T, Imaizumi T, Takada K (2006) EB virus-encoded RNAs are recognized by RIG-I and activate signaling to induce type I IFN. EMBO J 25(18): 4207-4214.
47. Nanbo A, Inoue K, Adachi-Takasawa K, Takada K (2002) Epstein-Barr virus RNA confers resistance to interferon-alpha-induced apoptosis in Burkitt's lymphoma. EMBO J 21(5):954-965.
48. Snudden DK, Hearing J, Smith PR, Grässer FA, Griffin BE (1994) EBNA-1, the major nuclear antigen of Epstein-Barr virus, resembles 'RGG' RNA binding proteins. EMBO J 13(20):4840-4847.
49. Conrad NK, Fok V, Cazalla D, Borah S, Steitz JA (2006) The challenge of viral snRNPs. Cold Spring Harb Symp Quant Biol 71:377-384.
50. Fok V, Friend K, Steitz JA (2006) Epstein-Barr virus noncoding RNAs are confined to the nucleus, whereas their partner, the human La protein, undergoes nucleocytoplasmic shuttling. J Cell Biol 173(3):319-325.
51. Fairley JA, et al. (2005) Human La is found at RNA polymerase III-transcribed genes in vivo. Proc Natl Acad Sci USA 102(51):18350-18355.
52. Ablasser A, et al. (2009) RIG-I-dependent sensing of poly(dA:dT) through the induction of an RNA polymerase III-transcribed RNA intermediate. Nat Immunol 10(10): 1065-1072.
53. Chiu YH, Macmillan JB, Chen ZJ (2009) RNA polymerase III detects cytosolic DNA and induces type I interferons through the RIG-I pathway. Cell 138(3):576-591.
54. Boelens MC, et al. (2014) Exosome transfer from stromal to breast cancer cells regulates therapy resistance pathways. Cell 159(3):499-513.
55. Unterholzner L, et al. (2010) IFI16 is an innate immune sensor for intracellular DNA. Nat Immunol 11(11):997-1004.
56. Lee N, Moss WN, Yario TA, Steitz JA (2015) EBV noncoding RNA binds nascent RNA to drive host PAX5 to viral DNA. Cell 160(4):607-618.
57. Guiducci C, et al. (2010) Autoimmune skin inflammation is dependent on plasmacytoid dendritic cell activation by nucleic acids via TLR7 and TLR9. J Exp Med 207(13): 2931-2942.
58. Bordon Y (2011) Innate immunity: An inducible RNA sensor? IFITs the bill. Nat Rev Immunol 11(7):440-441.
59. Farkas L, Beiske K, Lund-Johansen F, Brandtzaeg P, Jahnsen FL (2001) Plasmacytoid dendritic cells (natural interferon-alpha/beta-producing cells) accumulate in cutaneous lupus erythematosus lesions. Am J Pathol 159(1):237-243.
60. Wollenberg A, et al. (2002) Plasmacytoid dendritic cells: A new cutaneous dendritic cell subset with distinct role in inflammatory skin diseases. J Invest Dermatol 119(5): 1096-1102.
61. Donaghy H, et al. (2009) Role for plasmacytoid dendritic cells in the immune control of recurrent human herpes simplex virus infection. J Virol 83(4):1952-1961.
62. KalamvokiM, Du T, Roizman B (2014) Cells infected with herpes simplex virus 1 export to uninfected cells exosomes containing STING, viral mRNAs, and microRNAs. Proc Natl Acad Sci USA 111(46):E4991-E4996.
63. Strowig T, et al. (2008) Tonsilar NK cells restrict B cell transformation by the Epstein-Barr virus via IFN-gamma. PLoS Pathog 4(2):e27.
64. Hislop AD, et al. (2010) Impaired Epstein-Barr virus-specific CD8+ T-cell function in X-linked lymphoproliferative disease is restricted to SLAM family-positive B-cell targets. Blood 116(17):3249-3257.
65. Wubbolts R, et al. (2003) Proteomic and biochemical analyses of human B cell-derived exosomes. Potential implications for their function and multivesicular body formation. J Biol Chem 278(13):10963-10972.
66. Wiesner M, et al. (2008) Conditional immortalization of human B cells by CD40 ligation. PLoS One 3(1):e1464.
67. Hochberg D, et al. (2004) Acute infection with Epstein-Barr virus targets and overwhelms the peripheral memory B-cell compartment with resting, latently infected cells. J Virol 78(10):5194-5204.
68. Piersma SR, et al. (2010) Workflow comparison for label-free, quantitative secretome proteomics for cancer biomarker discovery: Method evaluation, differential analysis, and verification in serum. J Proteome Res 9(4):1913-1922.
69. Koppers-Lalic D, et al. (2014) Nontemplated nucleotide additions distinguish the small RNA composition in cells from exosomes. Cell Reports 8(6):1649-1658.
70. HackenbergM, Rodriguez-Ezpeleta N, Aransay AM (2011) miRanalyzer: An update on the detection and analysis of microRNAs in high-throughput sequencing experiments. Nucleic Acids Res 39(Web Server issue):W132-W138.
71. Dieci G, Fiorino G, Castelnuovo M, Teichmann M, Pagano A (2007) The expanding RNA polymerase III transcriptome. Trends Genet 23(12):614-622.