Extracellular vesicles provide a capsid-free vector for oncolytic adenoviral DNA delivery

References

• van der Pol E, Boing AN, Harrison P, et al. Classification, functions, and clinical relevance of extracellular vesicles. Pharmacol Rev. 2012;64(3):676–24.
   PubMed Web of Science ®Google Scholar
• Yáñez-Mó M, Siljander PR-M, Andreu Z, et al. Biological properties of extracellular vesicles and their physiological functions. J Extracell Vesicles. 2015;4(1):27066.
   Google Scholar
• Pegtel DM, Cosmopoulos K, Thorley-Lawson DA, et al. Functional delivery of viral miRNAs via exosomes. Proc Nat Acad Sci. 2010;107(14):6328–6333.
   Web of Science ®Google Scholar
• Kouwaki T, Okamoto M, Tsukamoto H, et al. Extracellular vesicles deliver host and virus RNA and regulate innate immune response. Int J Mol Sci. 2017;18(3):666.
   Web of Science ®Google Scholar
• Sadeghipour S, Mathias RA. Herpesviruses hijack host exosomes for viral pathogenesis. Semin Cell Dev Biol. 2017;67:91–100.
   Web of Science ®Google Scholar
• Takahashi A, Okada R, Nagao K, et al. Exosomes maintain cellular homeostasis by excreting harmful DNA from cells. Nat Commun. 2017;8(1). DOI:10.1038/ncomms15287
   Web of Science ®Google Scholar
• Wang T, Fang L, Zhao F, et al. Exosomes mediate intercellular transmission of porcine reproductive and respiratory syndrome virus (PRRSV). J Virol. 2017;JVI.01734-17. DOI:10.1128/JVI.01734-17
   Web of Science ®Google Scholar
• Yang Y, Han Q, Hou Z, et al. Exosomes mediate hepatitis B virus (HBV) transmission and NK-cell dysfunction. Cell Mol Immunol. 2017;14(5):465–475.
   Web of Science ®Google Scholar
• Zhao X, Wu Y, Duan J, et al. Quantitative proteomic analysis of exosome protein content changes induced by hepatitis B virus in Huh-7 cells using SILAC labeling and LC-MS/MS. J Proteome Res. 2014;13(12):5391–5402.
   Web of Science ®Google Scholar
• Zhou W, Woodson M, Neupane B, et al. Exosomes serve as novel modes of tick-borne flavivirus transmission from arthropod to human cells and facilitates dissemination of viral RNA and proteins to the vertebrate neuronal cells. PLoS Pathog. 2018;14(1):e1006764.
   Web of Science ®Google Scholar
• Kapoor NR, Chadha R, Kumar S, et al. The HBx gene of hepatitis B virus can influence hepatic microenvironment via exosomes by transferring its mRNA and protein. Virus Res. 2017;240:166–174.
   Web of Science ®Google Scholar
• Böker KO, Lemus-Diaz N, Rinaldi Ferreira R, et al. The impact of the CD9 tetraspanin on lentivirus infectivity and exosome secretion. Mol Ther. 2018;26(2):634–647.
   Web of Science ®Google Scholar
• Mack M, Kleinschmidt A, Brühl H, 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.
   PubMed Web of Science ®Google Scholar
• Nolte-‘t Hoen E, Cremer T, Gallo RC, et al. Extracellular vesicles and viruses: are they close relatives? Proc Nat Acad Sci. 2016;113(33):9155–9161.
   Web of Science ®Google Scholar
• Gould SJ, Booth AM, Hildreth JE. The Trojan exosome hypothesis. Proc Natl Acad Sci U S A. 2003;100:10592–10597.
   PubMed Web of Science ®Google Scholar
• Fu Y, Zhang L, Zhang F, et al. Exosome-mediated miR-146a transfer suppresses type I interferon response and facilitates EV71 infection. PLoS Pathog. 2017;(13(9): e1006611).
   Web of Science ®Google Scholar
• Bird SW, Maynard ND, Covert MW, et al. Nonlytic viral spread enhanced by autophagy components. Proc Natl Acad Sci U S A. 2014;111(36):13081–13086.
   PubMed Web of Science ®Google Scholar
• Jourdan N, Maurice M, Delautier D, et al. Rotavirus is released from the apical surface of cultured human intestinal cells through nonconventional vesicular transport that bypasses the Golgi apparatus. J Virol. 1997;71(11):8268–8278.
   PubMed Web of Science ®Google Scholar
• Méndez F, Romero N, Cubas LL, et al. Non-lytic egression of infectious bursal disease virus (IBDV) particles from infected cells. PloS One. 2017;12(1):e0170080.
   Web of Science ®Google Scholar
• Robinson SM, Tsueng G, Sin J, et al. Coxsackievirus B exits the host cell in shed microvesicles displaying autophagosomal markers. PLoS Pathog. 2014;10(4):e1004045.
   PubMed Web of Science ®Google Scholar
• Nagashima S, Jirintai S, Takahashi M, et al. Hepatitis E virus egress depends on the exosomal pathway, with secretory exosomes derived from multivesicular bodies. J Gen Virol. 2014;95:2166–2175.
   PubMed Web of Science ®Google Scholar
• van der Grein SG, Defourny KAY, Slot EFJ, et al. Intricate relationships between naked viruses and extracellular vesicles in the crosstalk between pathogen and host. Springer Semin Immunopathol. 2018;40(5):491–504.
   Web of Science ®Google Scholar
• Ran L, Tan X, Li Y, et al. Delivery of oncolytic adenovirus into the nucleus of tumorigenic cells by tumor microparticles for virotherapy. Biomaterials. 2016;89:56–66.
   Web of Science ®Google Scholar
• Maguire CA, Balaj L, Sivaraman S, et al. Microvesicle-associated AAV vector as a novel gene delivery system. Mol Ther. 2012;20(5):960–971.
   Web of Science ®Google Scholar
• Rana S, Yue S, Stadel D, et al. Toward tailored exosomes: the exosomal tetraspanin web contributes to target cell selection. Int J Biochem Cell Biol. 2012;44(9):1574–1584.
   PubMed Web of Science ®Google Scholar
• Wiklander OPB, Nordin JZ, O’Loughlin A, et al. Extracellular vesicle in vivo biodistribution is determined by cell source, route of administration and targeting. J Extracell Vesicles. 2015;4(1):26316.
   PubMed Web of Science ®Google Scholar
• Hoshino A, Costa-Silva B, Shen T-L, et al. Tumour exosome integrins determine organotropic metastasis. Nature. 2015;527(7578):329.
   PubMed Web of Science ®Google Scholar
• Peinado H, Alečković M, Lavotshkin S, et al. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat Med. 2012;18(6):883–+.
   Web of Science ®Google Scholar
• Grange C, Tapparo M, Collino F, et al. Microvesicles released from human renal cancer stem cells stimulate angiogenesis and formation of lung premetastatic niche. Cancer Res. 2011;71(15):5346–5356.
   PubMed Web of Science ®Google Scholar
• Tian T, Zhu Y-L, Hu F-H, et al. Dynamics of exosome internalization and trafficking. J Cell Physiol. 2013;228(7):1487–1495.
   PubMed Web of Science ®Google Scholar
• Tian T, Wang Y, Wang H, et al. Visualizing of the cellular uptake and intracellular trafficking of exosomes by live-cell microscopy. J Cell Biochem. 2010;111(2):488–496.
   PubMed Web of Science ®Google Scholar
• Escrevente C, Keller S, Altevogt P, et al. Interaction and uptake of exosomes by ovarian cancer cells. BMC Cancer. 2011;11(1):108.
   PubMed Web of Science ®Google Scholar
• del Conde I, Shrimpton CN, Thiagarajan P, et al. Tissue-factor–bearing microvesicles arise from lipid rafts and fuse with activated platelets to initiate coagulation. Blood. 2005;106(5):1604–1611.
   PubMed Web of Science ®Google Scholar
• Mulcahy LA, Pink RC, Carter DRF. Routes and mechanisms of extracellular vesicle uptake. J Extracell Vesicles. 2014;3(1):24641.
   Google Scholar
• Garofalo M, Saari H, Somersalo P, et al. Antitumor effect of oncolytic virus and paclitaxel encapsulated in extracellular vesicles for lung cancer treatment. J Controlled Release. 2018;283:223–234.
   Web of Science ®Google Scholar
• György B, Sage C, Indzhykulian AA, et al. Rescue of hearing by gene delivery to inner-ear hair cells using exosome-associated AAV. Mol Ther. 2017;25(2):379–391.
   Web of Science ®Google Scholar
• Wassmer SJ, Carvalho LS, György B, et al. Exosome-associated AAV2 vector mediates robust gene delivery into the murine retina upon intravitreal injection. Sci Rep. 2017;7(1). DOI:10.1038/srep45329
   Web of Science ®Google Scholar
• Koski A, Kangasniemi L, Escutenaire S, et al. Treatment of cancer patients with a serotype 5/3 chimeric oncolytic adenovirus expressing GMCSF. Mol Ther. 2010;18(10):1874–1884.
   PubMed Web of Science ®Google Scholar
• Dormond E, Chahal P, Bernier A, et al. An efficient process for the purification of helper-dependent adenoviral vector and removal of helper virus by iodixanol ultracentrifugation. J Virol Methods. 2010;165(1):83–89.
   Web of Science ®Google Scholar
• Tauro BJ, Greening DW, Mathias RA, 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.
   PubMed Web of Science ®Google Scholar
• Iwai K, Minamisawa T, Suga K, et al. Isolation of human salivary extracellular vesicles by iodixanol density gradient ultracentrifugation and their characterizations. J Extracell Vesicles. 2016;5(1):30829.
   Web of Science ®Google Scholar
• Saari H, Lázaro-Ibáñez E, Viitala T, et al. Microvesicle- and exosome-mediated drug delivery enhances the cytotoxicity of Paclitaxel in autologous prostate cancer cells. J Controlled Release. 2015;220:727–737.
   PubMed Web of Science ®Google Scholar
• Koifman N, Biran I, Aharon A, et al. A direct-imaging cryo-EM study of shedding extracellular vesicles from leukemic monocytes. J Struct Biol. 2017;198(3):177–185.
   Web of Science ®Google Scholar
• Höög JL, Lötvall J. Diversity of extracellular vesicles in human ejaculates revealed by cryo-electron microscopy. J Extracell Vesicles. 2015;4(1):28680.
   PubMed Web of Science ®Google Scholar
• Gros A, Guedan S. Adenovirus release from the infected cell as a key factor for adenovirus oncolysis. Open Gene Ther J. 2010;3(2):24–30.
   Google Scholar
• San Martín C. Latest insights on adenovirus structure and assembly. Viruses. 2012;4(5):847–877.
   Web of Science ®Google Scholar
• Saraste A, Pulkki K. Morphologic and biochemical hallmarks of apoptosis. Cardiovasc Res. 2000;45(3):528–537.
   Web of Science ®Google Scholar
• Osteikoetxea X, Sódar B, Németh A, et al. Differential detergent sensitivity of extracellular vesicle subpopulations. Org Biomol Chem. 2015;13(38):9775–9782.
   PubMed Web of Science ®Google Scholar
• Lázaro-Ibáñez E, Sanz-Garcia A, Visakorpi T, et al. Different gDNA content in the subpopulations of prostate cancer extracellular vesicles: apoptotic bodies, microvesicles, and exosomes. Prostate. 2014;74(14):1379–1390.
   PubMed Web of Science ®Google Scholar
• Thakur BK, Zhang H, Becker A, et al. Double-stranded DNA in exosomes: a novel biomarker in cancer detection. Cell Res. 2014;24(6):766–769.
   Web of Science ®Google Scholar
• Waldenström A, Gennebäck N, Hellman U, et al. Cardiomyocyte microvesicles contain DNA/RNA and convey biological messages to target cells. PLoS ONE. 2012;7(4):e34653.
   Web of Science ®Google Scholar
• Cai J, Wu G, Tan X, et al. Transferred BCR/ABL DNA from K562 extracellular vesicles causes chronic myeloid leukemia in immunodeficient mice. PLoS One. 2014;9(8):e105200.
   Web of Science ®Google Scholar
• Shelke GV, Jang SC, Yin Y, et al. Human mast cells release extracellular vesicle-associated DNA. Matters (Zürich). 2016;2:1.
   Google Scholar
• Németh A, Orgovan N, Sódar BW, et al. Antibiotic-induced release of small extracellular vesicles (exosomes) with surface-associated DNA. Sci Rep. 2017;7(1):8202.
   Web of Science ®Google Scholar
• Lázaro-Ibáñez E, Lässer C, Shelke GV, et al. DNA analysis of low- and high-density fractions defines heterogeneous subpopulations of small extracellular vesicles based on their DNA cargo and topology. J Extracell Vesicles. 2019;8(1):1656993.
   PubMed Web of Science ®Google Scholar
• Benevento M, Di Palma S, Snijder J, et al. Adenovirus composition, proteolysis, and disassembly studied by in-depth qualitative and quantitative proteomics. J Biol Chem. 2014;289(16):11421–11430.
   Web of Science ®Google Scholar
• Wiethoff CM, Wodrich H, Gerace L, et al. Adenovirus protein VI mediates membrane disruption following capsid disassembly. J Virol. 2005;79(4):1992–2000.
   PubMed Web of Science ®Google Scholar
• Baggen J, Thibaut H, Strating JR, et al. The life cycle of non-polio enteroviruses and how to target it. Nature Rev Microbiol. 2018;1:368–381.
   Google Scholar
• Zell R. Picornaviridae—the ever-growing virus family. Arch Virol. 2018;163.2 : 299–317.
   Web of Science ®Google Scholar
• Fay N, Panté N. Nuclear entry of DNA viruses. Front Microbiol. 2015;6:467.
   PubMed Web of Science ®Google Scholar
• Cai J, Han Y, Ren H, et al. Extracellular vesicle-mediated transfer of donor genomic DNA to recipient cells is a novel mechanism for genetic influence between cells. J Mol Cell Biol. 2013;5(4):227–238.
   PubMed Web of Science ®Google Scholar
• Smith JG, Cassany A, Gerace L, et al. Neutralizing antibody blocks adenovirus infection by arresting microtubule-dependent cytoplasmic transport. J Virol. 2008;82(13):6492–6500.
   Web of Science ®Google Scholar
• Lan YY, Londoño D, Bouley R, et al. Dnase2a deficiency uncovers lysosomal clearance of damaged nuclear DNA via autophagy. Cell Rep. 2014;9(1):180–192.
   Web of Science ®Google Scholar
• Rasmussen SB, Horan KA, Holm CK, et al. Activation of autophagy by α-herpesviruses in myeloid cells is mediated by cytoplasmic viral DNA through a mechanism dependent on stimulator of IFN genes. J Immunol. 2011;187(10):5268–5276.
   PubMed Web of Science ®Google Scholar
• Lam E, Stein S, Falck-Pedersen E. Adenovirus detection by the cGAS/STING/TBK1 DNA sensing cascade. J Virol. 2014;88(2):974–981.
   PubMed Web of Science ®Google Scholar
• Scherer J, Vallee RB. Conformational changes in the adenovirus hexon subunit responsible for regulating cytoplasmic dynein recruitment. J Virol. 2015;89:1013–1023.
   Web of Science ®Google Scholar
• Balakireva L, Schoehn G, Thouvenin E, et al. Binding of adenovirus capsid to dipalmitoyl phosphatidylcholine provides a novel pathway for virus entry. J Virol. 2003;77(8):4858–4866.
   Web of Science ®Google Scholar
• Fabry CMS, Rosa-Calatrava M, Conway JF, et al. A quasi‐atomic model of human adenovirus type 5 capsid. Embo J. 2005;24(9):1645–1654.
   Web of Science ®Google Scholar
• Fujiwara Y, Kikuchi H, Aizawa S, et al. Direct uptake and degradation of DNA by lysosomes. Autophagy. 2013;9(8):1167–1171.
   PubMed Web of Science ®Google Scholar
• Okegawa T, Li Y, Pong RC, et al. The dual impact of coxsackie and adenovirus receptor expression on human prostate cancer gene therapy. Cancer Res. 2000;60(18):5031–5036.
   Web of Science ®Google Scholar
• Murakami M, Ugai H, Belousova N, et al. Chimeric adenoviral vectors incorporating a fiber of human adenovirus 3 efficiently mediate gene transfer into prostate cancer cells. Prostate. 2010;70(4):362–376.
   Web of Science ®Google Scholar
• Barber AG, Castillo-Martin M, Bonal DM, et al. Characterization of desmoglein expression in the normal prostatic gland. Desmoglein 2 is an independent prognostic factor for aggressive prostate cancer. PLoS One. 2014;9(6):e98786.
   Web of Science ®Google Scholar
• Peng HH, Wu S, Davis JJ, et al. A rapid and efficient method for purification of recombinant adenovirus with arginine-glycine-aspartic acid-modified fibers. Anal Biochem. 2006;354(1):140–147.
   Web of Science ®Google Scholar
• Preuss MA, Lam JT, Wang M, et al. Transcriptional blocks limit adenoviral replication in primary ovarian tumor. Clin Cancer Res. 2004;10(9):3189–3194.
   Web of Science ®Google Scholar