Extracellular vesicles during Herpes Simplex Virus type 1 infection: An inquire

Virology Journal

Volumn 13, Issue 1, 2016, Pages

  Kalamvoki, Maria ^a   Deschamps, Thibaut ^a  

^a UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

Author keywords

Exosomes; Extracellular vesicles; Herpes simplex virus; Innate immunity; STING; Tetraspanins

Indexed keywords

CD63 ANTIGEN; CD81 ANTIGEN; CD9 ANTIGEN; MESSENGER RNA; MICRORNA; UNTRANSLATED RNA; VIRUS PROTEIN; VIRUS RNA;

CYTOPLASM; DNA VIRUS; EXOSOME; HERPES SIMPLEX VIRUS 1; HERPES VIRUS INFECTION; HOST CELL; HUMAN; INFECTION CONTROL; INNATE IMMUNITY; NONHUMAN; PERSISTENT INFECTION; REVIEW; STIMULATOR OF INTERFERON GENE; VIRUS CELL INTERACTION; VIRUS GENE; VIRUS ISOLATION; VIRUS TRANSCRIPTION; VIRUS TRANSMISSION; CHEMISTRY; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; TRANSPORT AT THE CELLULAR LEVEL;

BIOLOGICAL TRANSPORT; EXTRACELLULAR VESICLES; HERPESVIRUS 1, HUMAN; HOST-PATHOGEN INTERACTIONS; HUMANS; MICRORNAS; RNA, MESSENGER; RNA, VIRAL;

EID: 84964413541     PISSN: None     EISSN: 1743422X     Source Type: Journal    
DOI: 10.1186/s12985-016-0518-2     Document Type: Review

References (128)

1. Harding C, Heuser J, Stahl P. Endocytosis and intracellular processing of transferrin and colloidal gold-transferrin in rat reticulocytes: demonstration of a pathway for receptor shedding. Eur J Cell Biol. 1984;35(2):256-63.
2. Pan BT, Johnstone RM. Fate of the transferrin receptor during maturation of sheep reticulocytes in vitro: selective externalization of the receptor. Cell. 1983;33(3):967-78.
3. Johnstone RM, Adam M, Hammond JR, Orr L, Turbide C. Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J Biol Chem. 1987;262(19):9412-20.
4. Yanez-Mo M, Siljander PR, Andreu Z, Zavec AB, Borras FE, Buzas EI, et al. Biological properties of extracellular vesicles and their physiological functions. J Extracell Vesicles. 2015;4:27066. doi: 10.3402/jev.v4.27066.eCollection;2015.:27066.
5. Schwab A, Meyering SS, Lepene B, Iordanskiy S, van Hoek ML, Hakami RM, et al. Extracellular vesicles from infected cells: potential for direct pathogenesis. Front Microbiol. 2015;6:1132. doi: 10.3389/fmicb.2015.01132. eCollection; 2015.:1132.
6. Raposo G, Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol. 2013;200(4):373-83.
7. Stoorvogel W, Kleijmeer MJ, Geuze HJ, Raposo G. The biogenesis and functions of exosomes. Traffic. 2002;3(5):321-30.
8. Colombo M, Moita C, van NG, Kowal J, Vigneron J, Benaroch P, et al. Analysis of ESCRT functions in exosome biogenesis, composition and secretion highlights the heterogeneity of extracellular vesicles. J Cell Sci. 2013;126(Pt 24):5553-65.
9. Colombo M, Raposo G, Thery C. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu Rev Cell Dev Biol. 2014;30:255-89. doi: 10.1146/annurev-cellbio-101512-122326. Epub; 2014 Aug 21.:255-289.
10. Bobrie A, Colombo M, Raposo G, Thery C. Exosome secretion: molecular mechanisms and roles in immune responses. Traffic. 2011;12(12):1659-68.
11. Fyfe I, Schuh AL, Edwardson JM, Audhya A. Association of the endosomal sorting complex ESCRT-II with the Vps20 subunit of ESCRT-III generates a curvature-sensitive complex capable of nucleating ESCRT-III filaments. J Biol Chem. 2011;286(39):34262-70.
12. Hanson PI, Shim S, Merrill SA. Cell biology of the ESCRT machinery. Curr Opin Cell Biol. 2009;21(4):568-74.
13. Metcalf D, Isaacs AM. The role of ESCRT proteins in fusion events involving lysosomes, endosomes and autophagosomes. Biochem Soc Trans. 2010;38(6):1469-73.
14. Wollert T, Wunder C, Lippincott-Schwartz J, Hurley JH. Membrane scission by the ESCRT-III complex. Nature. 2009;458(7235):172-7.
15. Piper RC, Katzmann DJ. Biogenesis and function of multivesicular bodies. Annu Rev Cell Dev Biol. 2007;23:519-47. 519-547.
16. Trajkovic K, Hsu C, Chiantia S, Rajendran L, Wenzel D, Wieland F, et al. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science. 2008;319(5867):1244-7.
17. Wubbolts R, Leckie RS, Veenhuizen PT, Schwarzmann G, Mobius W, Hoernschemeyer J, et al. Proteomic and biochemical analyses of human B cell-derived exosomes. Potential implications for their function and multivesicular body formation. J Biol Chem. 2003;278(13):10963-72.
18. Bellingham SA, Coleman BM, Hill AF. Small RNA deep sequencing reveals a distinct miRNA signature released in exosomes from prion-infected neuronal cells. Nucleic Acids Res. 2012;40(21):10937-49.
19. Baj-Krzyworzeka M, Szatanek R, Weglarczyk K, Baran J, Urbanowicz B, Branski P, et al. Tumour-derived microvesicles carry several surface determinants and mRNA of tumour cells and transfer some of these determinants to monocytes. Cancer Immunol Immunother. 2006;55(7):808-18.
20. Huang X, Yuan T, Tschannen M, Sun Z, Jacob H, Du M, et al. Characterization of human plasma-derived exosomal RNAs by deep sequencing. BMC Genomics. 2013;14:319. doi: 10.1186/1471-2164-14-319.:319-14.
21. Hunter MP, Ismail N, Zhang X, Aguda BD, Lee EJ, Yu L, et al. Detection of microRNA expression in human peripheral blood microvesicles. PLoS One. 2008;3(11):e3694.
22. Kogure T, Lin WL, Yan IK, Braconi C, Patel T. Intercellular nanovesicle-mediated microRNA transfer: a mechanism of environmental modulation of hepatocellular cancer cell growth. Hepatology. 2011;54(4):1237-48.
23. Kogure T, Yan IK, Lin WL, Patel T. Extracellular Vesicle-Mediated Transfer of a Novel Long Noncoding RNA TUC339: A Mechanism of Intercellular Signaling in Human Hepatocellular Cancer. Genes Cancer. 2013;4(7-8):261-72.
24. Turchinovich A, Weiz L, Langheinz A, Burwinkel B. Characterization of extracellular circulating microRNA. Nucleic Acids Res. 2011;39(16):7223-33.
25. Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol. 2007;9(6):654-9.
26. Skog J, Wurdinger T, van RS, Meijer DH, Gainche L, Sena-Esteves M, et al. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol. 2008;10(12):1470-6.
27. Llorente A, Skotland T, Sylvanne T, Kauhanen D, Rog T, Orlowski A, et al. Molecular lipidomics of exosomes released by PC-3 prostate cancer cells. Biochim Biophys Acta. 2013;1831(7):1302-9.
28. Phuyal S, Hessvik NP, Skotland T, Sandvig K, Llorente A. Regulation of exosome release by glycosphingolipids and flotillins. FEBS J. 2014;281(9):2214-27.
29. Laulagnier K, Grand D, Dujardin A, Hamdi S, Vincent-Schneider H, Lankar D, et al. PLD2 is enriched on exosomes and its activity is correlated to the release of exosomes. FEBS Lett. 2004;572(1-3):11-4.
30. Laulagnier K, Vincent-Schneider H, Hamdi S, Subra C, Lankar D, Record M. Characterization of exosome subpopulations from RBL-2H3 cells using fluorescent lipids. Blood Cells Mol Dis. 2005;35(2):116-21.
31. Subra C, Laulagnier K, Perret B, Record M. Exosome lipidomics unravels lipid sorting at the level of multivesicular bodies. Biochimie. 2007;89(2):205-12.
32. Li J, Liu K, Liu Y, Xu Y, Zhang F, Yang H, et al. Exosomes mediate the cell-to-cell transmission of IFN-alpha-induced antiviral activity. Nat Immunol. 2013;14(8):793-803.
33. Coleman BM, Hill AF. Extracellular vesicles - Their role in the packaging and spread of misfolded proteins associated with neurodegenerative diseases. Semin Cell Dev Biol. 2015;40:89-96. doi: 10.1016/j.semcdb.2015.02.007. Epub; 2015 Feb; 20.:89-96.
34. Kalani A, Tyagi A, Tyagi N. Exosomes: mediators of neurodegeneration, neuroprotection and therapeutics. Mol Neurobiol. 2014;49(1):590-600.
35. Aguzzi A, Lakkaraju AK. Cell Biology of Prions and Prionoids: A Status Report. Trends Cell Biol. 2016;26(1):40-51.
36. Wahlgren J, Statello L, Skogberg G, Telemo E, Valadi H. Delivery of Small Interfering RNAs to Cells via Exosomes. Methods Mol Biol. 2016;1364:105-25. doi: 10.1007/978-1-4939-3112-5-10.:105-125.
37. Alenquer M, Amorim MJ. Exosome Biogenesis, Regulation, and Function in Viral Infection. Viruses. 2015;7(9):5066-83.
38. Madison MN, Okeoma CM. Exosomes: Implications in HIV-1 Pathogenesis. Viruses. 2015;7(7):4093-118.
39. Chahar HS, Bao X, Casola A. Exosomes and Their Role in the Life Cycle and Pathogenesis of RNA Viruses. Viruses. 2015;7(6):3204-25.
40. Gould SJ, Booth AM, Hildreth JE. The Trojan exosome hypothesis. Proc Natl Acad Sci U S A. 2003;100(19):10592-7.
41. Nguyen DG, Booth A, Gould SJ, Hildreth JE. Evidence that HIV budding in primary macrophages occurs through the exosome release pathway. J Biol Chem. 2003;278(52):52347-54.
42. Columba CS, Federico M. Sequences within RNA coding for HIV-1 Gag p17 are efficiently targeted to exosomes. Cell Microbiol. 2013;15(3):412-29.
43. Narayanan A, Iordanskiy S, Das R, Van DR, Santos S, Jaworski E, et al. Exosomes derived from HIV-1-infected cells contain trans-activation response element RNA. J Biol Chem. 2013;288(27):20014-33.
44. Bernard MA, Zhao H, Yue SC, Anandaiah A, Koziel H, Tachado SD. Novel HIV-1 miRNAs stimulate TNFalpha release in human macrophages via TLR8 signaling pathway. PLoS One. 2014;9(9):e106006.
45. Mack M, Kleinschmidt A, Bruhl H, Klier C, Nelson PJ, Cihak J, et al. Transfer of the chemokine receptor CCR5 between cells by membrane-derived microparticles: a mechanism for cellular human immunodeficiency virus 1 infection. Nat Med. 2000;6(7):769-75.
46. Rozmyslowicz T, Majka M, Kijowski J, Murphy SL, Conover DO, Poncz M, et al. Platelet- and megakaryocyte-derived microparticles transfer CXCR4 receptor to CXCR4-null cells and make them susceptible to infection by X4-HIV. AIDS. 2003;17(1):33-42.
47. Sheehy AM, Gaddis NC, Choi JD, Malim MH. Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature. 2002;418(6898):646-50.
48. Sheehy AM, Gaddis NC, Malim MH. The antiretroviral enzyme APOBEC3G is degraded by the proteasome in response to HIV-1 Vif. Nat Med. 2003;9(11):1404-7.
49. Khatua AK, Taylor HE, Hildreth JE, Popik W. Exosomes packaging APOBEC3G confer human immunodeficiency virus resistance to recipient cells. J Virol. 2009;83(2):512-21.
50. Khatua AK, Taylor HE, Hildreth JE, Popik W. Inhibition of LINE-1 and Alu retrotransposition by exosomes encapsidating APOBEC3G and APOBEC3F. Virology. 2010;400(1):68-75.
51. Strebel K. APOBEC3G & HTLV-1: inhibition without deamination. Retrovirology. 2005;2:37.
52. Newman EN, Holmes RK, Craig HM, Klein KC, Lingappa JR, Malim MH, et al. Antiviral function of APOBEC3G can be dissociated from cytidine deaminase activity. Curr Biol. 2005;15(2):166-70.
53. Esser MT, Graham DR, Coren LV, Trubey CM, Bess Jr JW, Arthur LO, et al. Differential incorporation of CD45, CD80 (B7-1), CD86 (B7-2), and major histocompatibility complex class I and II molecules into human immunodeficiency virus type 1 virions and microvesicles: implications for viral pathogenesis and immune regulation. J Virol. 2001;75(13):6173-82.
54. Lenassi M, Cagney G, Liao M, Vaupotic T, Bartholomeeusen K, Cheng Y, et al. HIV Nef is secreted in exosomes and triggers apoptosis in bystander CD4+ T cells. Traffic. 2010;11(1):110-22.
55. Arenaccio C, Chiozzini C, Columba-Cabezas S, Manfredi F, Affabris E, Baur A, et al. Exosomes from human immunodeficiency virus type 1 (HIV-1)-infected cells license quiescent CD4+ T lymphocytes to replicate HIV-1 through a Nef- and ADAM17-dependent mechanism. J Virol. 2014;88(19):11529-39.
56. Muratori C, Cavallin LE, Kratzel K, Tinari A, De MA, Fais S, et al. Massive secretion by T cells is caused by HIV Nef in infected cells and by Nef transfer to bystander cells. Cell Host Microbe. 2009;6(3):218-30.
57. Schaefer MR, Wonderlich ER, Roeth JF, Leonard JA, Collins KL. HIV-1 Nef targets MHC-I and CD4 for degradation via a final common beta-COP-dependent pathway in T cells. PLoS Pathog. 2008;4(8):e1000131.
58. daSilva LL, Sougrat R, Burgos PV, Janvier K, Mattera R, Bonifacino JS. Human immunodeficiency virus type 1 Nef protein targets CD4 to the multivesicular body pathway. J Virol. 2009;83(13):6578-90.
59. Aqil M, Naqvi AR, Mallik S, Bandyopadhyay S, Maulik U, Jameel S. The HIV Nef protein modulates cellular and exosomal miRNA profiles in human monocytic cells. J Extracell Vesicles 2014;3. doi: 10.3402/jev.v3.23129. eCollection; 2014.:10.
60. Feng Z, Hensley L, McKnight KL, Hu F, Madden V, Ping L, et al. A pathogenic picornavirus acquires an envelope by hijacking cellular membranes. Nature. 2013;496(7445):367-71.
61. Cosset FL, Dreux M. HCV transmission by hepatic exosomes establishes a productive infection. J Hepatol. 2014;60(3):674-5.
62. Dreux M, Garaigorta U, Boyd B, Decembre E, Chung J, Whitten-Bauer C, et al. Short-range exosomal transfer of viral RNA from infected cells to plasmacytoid dendritic cells triggers innate immunity. Cell Host Microbe. 2012;12(4):558-70.
63. Greenhill C. Hepatitis: New route of HCV transmission. Nat Rev Gastroenterol Hepatol. 2013;10(9):504.
64. Patman G. Hepatitis: Exosomal route of HCV transmission exists in patients. Nat Rev Gastroenterol Hepatol. 2014;11(12):704.
65. Ramakrishnaiah V, Thumann C, Fofana I, Habersetzer F, Pan Q, de Ruiter PE, et al. Exosome-mediated transmission of hepatitis C virus between human hepatoma Huh7.5 cells. Proc Natl Acad Sci U S A. 2013;110(32):13109-13.
66. Bukong TN, Momen-Heravi F, Kodys K, Bala S, Szabo G. Exosomes from hepatitis C infected patients transmit HCV infection and contain replication competent viral RNA in complex with Ago2-miR122-HSP90. PLoS Pathog. 2014;10(10):e1004424.
67. Masciopinto F, Giovani C, Campagnoli S, Galli-Stampino L, Colombatto P, Brunetto M, et al. Association of hepatitis C virus envelope proteins with exosomes. Eur J Immunol. 2004;34(10):2834-42.
68. Pileri P, Uematsu Y, Campagnoli S, Galli G, Falugi F, Petracca R, et al. Binding of hepatitis C virus to CD81. Science. 1998;282(5390):938-41.
69. Longatti A. The Dual Role of Exosomes in Hepatitis A and C Virus Transmission and Viral Immune Activation. Viruses. 2015;7(12):6707-15.
70. Feng Z, Li Y, McKnight KL, Hensley L, Lanford RE, Walker CM, et al. Human pDCs preferentially sense enveloped hepatitis A virions. J Clin Invest. 2015;125(1):169-76.
71. Meckes Jr DG, Shair KH, Marquitz AR, Kung CP, Edwards RH, Raab-Traub N. Human tumor virus utilizes exosomes for intercellular communication. Proc Natl Acad Sci U S A. 2010;107(47):20370-5.
72. Shair KH, Schnegg CI, Raab-Traub N. Epstein-Barr virus latent membrane protein-1 effects on junctional plakoglobin and induction of a cadherin switch. Cancer Res. 2009;69(14):5734-42.
73. Kung CP, Meckes Jr DG, Raab-Traub N. Epstein-Barr virus LMP1 activates EGFR, STAT3, and ERK through effects on PKCdelta. J Virol. 2011;85(9):4399-408.
74. Keryer-Bibens C, Pioche-Durieu C, Villemant C, Souquere S, Nishi N, Hirashima M, et al. Exosomes released by EBV-infected nasopharyngeal carcinoma cells convey the viral latent membrane protein 1 and the immunomodulatory protein galectin 9. BMC Cancer. 2006;6:283.
75. Ceccarelli S, Visco V, Raffa S, Wakisaka N, Pagano JS, Torrisi MR. Epstein-Barr virus latent membrane protein 1 promotes concentration in multivesicular bodies of fibroblast growth factor 2 and its release through exosomes. Int J Cancer. 2007;121(7):1494-506.
76. Ariza ME, Rivailler P, Glaser R, Chen M, Williams MV. Epstein-Barr virus encoded dUTPase containing exosomes modulate innate and adaptive immune responses in human dendritic cells and peripheral blood mononuclear cells. PLoS One. 2013;8(7):e69827.
77. Meckes Jr DG, Gunawardena HP, Dekroon RM, Heaton PR, Edwards RH, Ozgur S, et al. Modulation of B-cell exosome proteins by gamma herpesvirus infection. Proc Natl Acad Sci U S A. 2013;110(31):E2925-33.
78. Altenberg B, Greulich KO. Genes of glycolysis are ubiquitously overexpressed in 24 cancer classes. Genomics. 2004;84(6):1014-20.
79. Kondoh H, Lleonart ME, Gil J, Wang J, Degan P, Peters G, et al. Glycolytic enzymes can modulate cellular life span. Cancer Res. 2005;65(1):177-85.
80. Orzalli MH, DeLuca NA, Knipe DM. Nuclear IFI16 induction of IRF-3 signaling during herpesviral infection and degradation of IFI16 by the viral ICP0 protein. Proc Natl Acad Sci U S A. 2012;109(44):E3008-17.
81. Gariano GR, Dell'Oste V, Bronzini M, Gatti D, Luganini A, De AM, et al. The intracellular DNA sensor IFI16 gene acts as restriction factor for human cytomegalovirus replication. PLoS Pathog. 2012;8(1):e1002498.
82. Johnson KE, Bottero V, Flaherty S, Dutta S, Singh VV, Chandran B. IFI16 restricts HSV-1 replication by accumulating on the hsv-1 genome, repressing HSV-1 gene expression, and directly or indirectly modulating histone modifications. PLoS Pathog. 2014;10(11):e1004503.
83. Kerur N, Veettil MV, Sharma-Walia N, Bottero V, Sadagopan S, Otageri P, et al. IFI16 acts as a nuclear pathogen sensor to induce the inflammasome in response to Kaposi Sarcoma-associated herpesvirus infection. Cell Host Microbe. 2011;9(5):363-75.
84. Jochum S, Ruiss R, Moosmann A, Hammerschmidt W, Zeidler R. RNAs in Epstein-Barr virions control early steps of infection. Proc Natl Acad Sci U S A. 2012;109(21):E1396-404.
85. Jochum S, Moosmann A, Lang S, Hammerschmidt W, Zeidler R. The EBV immunoevasins vIL-10 and BNLF2a protect newly infected B cells from immune recognition and elimination. PLoS Pathog. 2012;8(5):e1002704.
86. Guo Q, Qian L, Guo L, Shi M, Chen C, Lv X, et al. Transactivators Zta and Rta of Epstein-Barr virus promote G0/G1 to S transition in Raji cells: a novel relationship between lytic virus and cell cycle. Mol Immunol. 2010;47(9):1783-92.
87. Kalla M, Schmeinck A, Bergbauer M, Pich D, Hammerschmidt W. AP-1 homolog BZLF1 of Epstein-Barr virus has two essential functions dependent on the epigenetic state of the viral genome. Proc Natl Acad Sci U S A. 2010;107(2):850-5.
88. Altmann M, Hammerschmidt W. Epstein-Barr virus provides a new paradigm: a requirement for the immediate inhibition of apoptosis. PLoS Biol. 2005;3(12):e404.
89. Temme S, Eis-Hubinger AM, McLellan AD, Koch N. The herpes simplex virus-1 encoded glycoprotein B diverts HLA-DR into the exosome pathway. J Immunol. 2010;184(1):236-43.
90. Mori Y, Koike M, Moriishi E, Kawabata A, Tang H, Oyaizu H, et al. Human herpesvirus-6 induces MVB formation, and virus egress occurs by an exosomal release pathway. Traffic. 2008;9(10):1728-42.
91. Szilagyi JF, Cunningham C. Identification and characterization of a novel non-infectious herpes simplex virus-related particle. J Gen Virol. 1991;72(Pt 3):661-8.
92. McLauchlan J, Addison C, Craigie MC, Rixon FJ. Noninfectious L-particles supply functions which can facilitate infection by HSV-1. Virology. 1992;190(2):682-8.
93. McLauchlan J, Rixon FJ. Characterization of enveloped tegument structures (L particles) produced by alphaherpesviruses: integrity of the tegument does not depend on the presence of capsid or envelope. J Gen Virol. 1992;73(Pt 2):269-76.
94. Heilingloh CS, Kummer M, Muhl-Zurbes P, Drassner C, Daniel C, Klewer M, et al. L Particles Transmit Viral Proteins from Herpes Simplex Virus 1-Infected Mature Dendritic Cells to Uninfected Bystander Cells, Inducing CD83 Downmodulation. J Virol. 2015;89(21):11046-55.
95. Ennaciri J, Menezes J, Proulx F, Toledano BJ. Induction of apoptosis by herpes simplex virus-1 in neonatal, but not adult, neutrophils. Pediatr Res. 2006;59(1):7-12.
96. Miles DH, Thakur A, Cole N, Willcox MD. The induction and suppression of the apoptotic response of HSV-1 in human corneal epithelial cells. Invest Ophthalmol Vis Sci. 2007;48(2):789-96.
97. Watanabe D, Honda T, Nishio K, Tomita Y, Sugiura Y, Nishiyama Y. Corneal infection of herpes simplex virus type 2 - induced neuronal apoptosis in the brain stem of mice with expression of tumor suppressor gene (p53) and transcription factors. Acta Neuropathol. 2000;100(6):647-53.
98. Wilson SE, Pedroza L, Beuerman R, Hill JM. Herpes simplex virus type-1 infection of corneal epithelial cells induces apoptosis of the underlying keratocytes. Exp Eye Res. 1997;64(5):775-9.
99. Ishikawa H, Ma Z, Barber GN. STING regulates intracellular DNA-mediated, type I interferon-dependent innate immunity. Nature. 2009;461(7265):788-92.
100. Luecke S, Paludan SR. Innate recognition of alphaherpesvirus DNA. Adv Virus Res. 2015;92:63-100. doi: 10.1016/bs.aivir.2014.11.003. Epub; 2015 Jan 15.:63-100.
101. Parker ZM, Murphy AA, Leib DA. Role of the DNA Sensor STING in Protection from Lethal Infection following Corneal and Intracerebral Challenge with Herpes Simplex Virus 1. J Virol. 2015;89(21):11080-91.
102. Kalamvoki M, Roizman B. HSV-1 degrades, stabilizes, requires, or is stung by STING depending on ICP0, the US3 protein kinase, and cell derivation. Proc Natl Acad Sci U S A. 2014;111(5):E611-7.
103. Kalamvoki M, Du T, Roizman B. Cells infected with herpes simplex virus 1 export to uninfected cells exosomes containing STING, viral mRNAs, and microRNAs. Proc Natl Acad Sci U S A. 2014;111(46):E4991-6.
104. Desai P, DeLuca NA, Glorioso JC, Person S. Mutations in herpes simplex virus type 1 genes encoding VP5 and VP23 abrogate capsid formation and cleavage of replicated DNA. J Virol. 1993;67(3):1357-64.
105. Burdette DL, Vance RE. STING and the innate immune response to nucleic acids in the cytosol. Nat Immunol. 2013;14(1):19-26.
106. Shu C, Li X, Li P. The mechanism of double-stranded DNA sensing through the cGAS-STING pathway. Cytokine Growth Factor Rev. 2014;25(6):641-8.
107. Dobbs N, Burnaevskiy N, Chen D, Gonugunta VK, Alto NM, Yan N. STING Activation by Translocation from the ER Is Associated with Infection and Autoinflammatory Disease. Cell Host Microbe. 2015;18(2):157-68.
108. Hemler ME. Tetraspanin proteins mediate cellular penetration, invasion, and fusion events and define a novel type of membrane microdomain. Annu Rev Cell Dev Biol. 2003;19:397-422.
109. Pols MS, Klumperman J. Trafficking and function of the tetraspanin CD63. Exp Cell Res. 2009;315(9):1584-92.
110. Hemler ME. Tetraspanin functions and associated microdomains. Nat Rev Mol Cell Biol. 2005;6(10):801-11.
111. Spear PG, Roizman B. Proteins specified by herpes simplex virus. V. Purification and structural proteins of the herpesvirion. J Virol. 1972;9(1):143-59.
112. Konadu KA, Huang MB, Roth W, Armstrong W, Powell M, Villinger F, et al. Isolation of Exosomes from the Plasma of HIV-1 Positive Individuals. J Vis Exp. 2016;107:10.
113. Tauro BJ, Greening DW, Mathias RA, Ji H, Mathivanan S, Scott AM, et al. Comparison of ultracentrifugation, density gradient separation, and immunoaffinity capture methods for isolating human colon cancer cell line LIM1863-derived exosomes. Methods. 2012;56(2):293-304.
114. Azmi AS, Bao B, Sarkar FH. Exosomes in cancer development, metastasis, and drug resistance: a comprehensive review. Cancer Metastasis Rev. 2013;32(3-4):623-42.
115. Borges FT, Reis LA, Schor N. Extracellular vesicles: structure, function, and potential clinical uses in renal diseases. Braz J Med Biol Res. 2013;46(10):824-30.
116. Kharaziha P, Ceder S, Li Q, Panaretakis T. Tumor cell-derived exosomes: a message in a bottle. Biochim Biophys Acta. 2012;1826(1):103-11.
117. Minciacchi VR, Freeman MR, Di VD. Extracellular vesicles in cancer: exosomes, microvesicles and the emerging role of large oncosomes. Semin Cell Dev Biol. 2015;40:51. doi: 10.1016/j.semcdb.2015.02.010. Epub;2015 Feb 23.:41-51.
118. Schorey JS, Cheng Y, Singh PP, Smith VL. Exosomes and other extracellular vesicles in host-pathogen interactions. EMBO Rep. 2015;16(1):24-43.
119. Fleming A, Sampey G, Chung MC, Bailey C, van Hoek ML, Kashanchi F, et al. The carrying pigeons of the cell: exosomes and their role in infectious diseases caused by human pathogens. Pathog Dis. 2014;71(2):109-20.
120. Lippe R. Characterization of extracellular HSV-1 virions by proteomics. Methods Mol Biol. 2014;1144:181-90. doi: 10.1007/978-1-4939-0428-0-12.:181-190.
121. Loret S, Guay G, Lippe R. Comprehensive characterization of extracellular herpes simplex virus type 1 virions. J Virol. 2008;82(17):8605-18.
122. Stegen C, Yakova Y, Henaff D, Nadjar J, Duron J, Lippe R. Analysis of virion-incorporated host proteins required for herpes simplex virus type 1 infection through a RNA interference screen. PLoS One. 2013;8(1):e53276.
123. Sciortino MT, Suzuki M, Taddeo B, Roizman B. RNAs extracted from herpes simplex virus 1 virions: apparent selectivity of viral but not cellular RNAs packaged in virions. J Virol. 2001;75(17):8105-16.
124. Sarcinella E, Brown M, Tellier R, Petric M, Mazzulli T. Detection of RNA in purified cytomegalovirus virions. Virus Res. 2004;104(2):129-37.
125. Terhune SS, Schroer J, Shenk T. RNAs are packaged into human cytomegalovirus virions in proportion to their intracellular concentration. J Virol. 2004;78(19):10390-8.
126. Lasser C, Alikhani VS, Ekstrom K, Eldh M, Paredes PT, Bossios A, et al. Human saliva, plasma and breast milk exosomes contain RNA: uptake by macrophages. J Transl Med. 2011;9:9. doi: 10.1186/1479-5876-9-9.:9.
127. Properzi F, Logozzi M, Fais S. Exosomes: the future of biomarkers in medicine. Biomark Med. 2013;7(5):769-78.
128. Simpson RJ, Lim JW, Moritz RL, Mathivanan S. Exosomes: proteomic insights and diagnostic potential. Expert Rev Proteomics. 2009;6(3):267-83.