Intercellular transmission of Seneca Valley virus mediated by exosomes
Tóm tắt
Seneca Valley virus (SVV) is a non-encapsulated single-stranded positive-strand RNA virus whose transmission routes have not yet been fully elucidated. Exosomes have been implicated in the intercellular transport of a variety of materials, such as proteins, RNA, and liposomes. However, whether exosomes can mediate SVV intercellular transmission remains unknown. In this study, we extracted exosomes from SVV-infected IBRS-2 cells to investigate intercellular transmission. Our results suggest that the intercellular transmission of SVV is mediated by exosomes. The results of co-localization and RT-qPCR studies showed that exosomes harbor SVV and enable the virus to proliferate in both susceptible and non-susceptible cells. Furthermore, the replication of SVV was inhibited when IBRS-2 cells were treated with interfering RNA Rab27a and exosome inhibitor GW4869. Finally, neutralization experiments were performed to further verify whether the virus was encapsulated by the exosomes that mediated transmission between cells. It was found that exosome-mediated intercellular transmission was not blocked by SVV-specific neutralizing antibodies. This study reveals a new transmission route of SVV and provides clear evidence regarding the pathogenesis of SVV, information which can also be useful for identifying therapeutic interventions.
Tài liệu tham khảo
Hales LM, Knowles NJ, Reddy PS, Xu L, Hallenbeck PL (2008) Complete genome sequence analysis of Seneca Valley virus-001, a novel oncolytic picornavirus. J Gen Virol 89:1265
Reddy PS, Burroughs KD, Hales LM, Ganesh S, Jones BH, Idamakanti N, Hay C, Li SS, Skele KL, Vasko A-J (2007) Seneca Valley Virus, a systemically deliverable oncolytic picornavirus, and the treatment of neuroendocrine cancers. J Natl Cancer Inst 99:1623
Leme RA (2016) Clinical manifestations of Senecavirus A infection in neonatal pigs, Brazil. Emerg Infect Dis 22:1238–1241
Canning P, Canon A, Bates JL, Gerardy K, Linhares DC, Piñeyro PE, Schwartz KJ, Yoon KJ, Rademacher CJ, Holtkamp D, Karriker L (2016) Neonatal mortality, vesicular lesions and lameness associated with Senecavirus A in a U.S sow farm. Transbound Emerg Dis 63:373–378
Kuo F (1998) Multimedia communications: protocols and applications. Prentice Hall, New Jersey
Chen P, Yang F, Cao W, Liu H, Zhang K, Liu X, Xu Z, Zhu Z, Zheng H (2018) The distribution of different clades of Seneca Valley viruses in Guangdong Province, China. Virol Sin 33:394–401
Jeppesen DK, Fenix AM, Franklin JL, Higginbotham JN, Zhang Q, Zimmerman LJ, Liebler DC, Ping J, Liu Q, Evans R, Fissell WH, Patton JG, Rome LH, Burnette DT, Coffey RJ (2019) Reassessment of exosome composition. Cell 177(428–445):e418
Abdel-Haq H (2019) Blood exosomes as a tool for monitoring treatment efficacy and progression of neurodegenerative diseases. Neural Regen Res 14:72–74
Anderson MR, Pleet ML, Enose-Akahata Y, Erickson J, Monaco MC, Akpamagbo Y, Velluci A, Tanaka Y, Azodi S, Lepene B, Jones J, Kashanchi F, Jacobson S (2018) Viral antigens detectable in CSF exosomes from patients with retrovirus associated neurologic disease: functional role of exosomes. Clin Transl Med 7:24
Sun Z, Yang S, Zhou Q, Wang G, Song J, Li Z, Zhang Z, Xu J, Xia K, Chang Y, Liu J, Yuan W (2018) Emerging role of exosome-derived long non-coding RNAs in tumor microenvironment. Mol Cancer 17:82
Pelchen-Matthews A, Raposo G, Marsh M (2004) Endosomes, exosomes and Trojan viruses. Trends Microbiol 12:310–316
Andrea L (2015) The dual role of exosomes in hepatitis A and C virus transmission and viral immune activation. Viruses 7:6707–6715
Zhu Z, Yang F, Chen P, Liu H, Cao W, Zhang K, Liu X, Zheng H (2017) Emergence of novel Seneca Valley virus strains in China, 2017. Transbound Emerg Dis 64:1024–1029
Shao H, Im H, Castro CM, Breakefield X, Weissleder R, Lee H (2018) New Technologies for Analysis of Extracellular Vesicles. Chemical Reviews 118(4):1917–1950
Nath Neerukonda S, Egan NA, Patria J, Assakhi I, Tavlarides-Hontz P, Modla S, Munoz ER, Hudson MB, Parcells MS (2018) Comparison of exosomes purified via ultracentrifugation (UC) and Total Exosome Isolation (TEI) reagent from the serum of Marek’s disease virus (MDV)-vaccinated and tumor-bearing chickens. J Virol Methods 263:1–9
Fu Y, Zhang L, Zhang F, Tang T, Zhou Q, Feng C, Jin Y, Wu Z (2017) Exosome-mediated miR-146a transfer suppresses type I interferon response and facilitates EV71 infection. PLoS Pathog 13:e1006611
Raposo G, Stoorvogel W (2013) Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol 200:373–383
Abdik H, Avsar Abdik E, Hizli Deniz AA, Tasli PN, Sahin F (2019) A novel virtue in stem cell research: exosomes and their role in differentiation. Adv Exp Med Biol 1144:133–146
Ostrowski M, Carmo NB, Krumeich S, Fanget I, Raposo G, Savina A, Moita CF, Schauer K, Hume AN, Freitas RP, Goud B, Benaroch P, Hacohen N, Fukuda M, Desnos C, Seabra MC, Darchen F, Amigorena S, Moita LF, Thery C (2010) Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat Cell Biol 12(11–13):19–30
Hsu C, Morohashi Y, Yoshimura SI, Manrique-Hoyos N, Jung S, Lauterbach MA, Bakhti M, Grønborg M, Möbius W, Rhee J, Barr FA, Simons M (2010) Regulation of exosome secretion by Rab35 and its GTPase-activating proteins TBC1D10A–C. J Cell Biol 189(2):223–232
Baietti MF, Zhang Z, Mortier E, Melchior A, Degeest G, Geeraerts A, Ivarsson Y, Depoortere F, Coomans C, Vermeiren E, Zimmermann P, David G (2012) Syndecan–syntenin–ALIX regulates the biogenesis of exosomes. Nat Cell Biol 14(7):677–685
Verderio C, Gabrielli M, Giussani P (2018) Role of sphingolipids in the biogenesis and biological activity of extracellular vesicles. J Lipid Res 59(8):1325–1340
Zhang K, Xu S, Shi X, Xu G, Shen C, Liu X, Zheng H (2019) Exosomes-mediated transmission of foot-and-mouth disease virus in vivo and in vitro. Vet Microbiol 233:164–173
Cosset FL, Dreux M (2014) HCV transmission by hepatic exosomes establishes a productive infection. J Hepatol 60:674–675
Wiley RD, Gummuluru S (2006) Immature dendritic cell-derived exosomes can mediate HIV-1 trans infection. Proc Natl Acad Sci USA 103:738–743
Wang T, Fang L, Zhao F, Wang D, Xiao S (2017) Exosomes mediate intercellular transmission of porcine reproductive and respiratory syndrome virus (PRRSV). J Virol 92(4): e01734-17
Guo D, Lui GYL, Lai SL, Wilmott JS, Tikoo S, Jackett LA, Quek C, Brown DL, Sharp DM, Kwan RYQ, Chacon D, Wong JH, Beck D, van Geldermalsen M, Holst J, Thompson JF, Mann GJ, Scolyer RA, Stow JL, Weninger W, Haass NK, Beaumont KA (2019) RAB27A promotes melanoma cell invasion and metastasis via regulation of pro-invasive exosomes. Int J Cancer 144:3070–3085
Ostenfeld MS, Jeppesen DK, Laurberg JR, Boysen AT, Bramsen JB, Primdalbengtson B, An H, Lamy P, Dagnaeshansen F, Rasmussen MH (2014) Cellular disposal of miR23b by RAB27-dependent exosome release is linked to acquisition of metastatic properties. Cancer Res 74:5758–5771
Wu BX, Clarke CJ, Hannun YA (2010) Mammalian neutral sphingomyelinases: regulation and roles in cell signaling responses. Neuromol Med 12(4):320–330
Vilette D, Laulagnier K, Huor A, Alais S, Leblanc P (2015) Efficient inhibition of infectious prions multiplication and release by targeting the exosomal pathway. Cell Mol Life Sci 72:4409–4427
Tamai K, Shiina M, Tanaka N, Nakano T, Yamamoto A, Kondo Y, Kakazu E, Inoue J, Fukushima K, Sano K (2012) Regulation of hepatitis C virus secretion by the Hrs-dependent exosomal pathway. Virology 422:377–385
Ramakrishnaiah V, Thumann C, Fofana I, Habersetzer F, Pan Q, de Ruiter PE, Willemsen R, Demmers JA, Raj VS, Jenster G, Kwekkeboom J, Tilanus HW, Haagmans BL, Baumert TF, van der Laan LJ (2013) Exosome-mediated transmission of hepatitis C virus between human hepatoma Huh7 5 cells. Proc Natl Acad Sci U S A. 110:13109–13113
Wang T, Fang L, Zhao F, Wang D, Xiao S (2018) Exosomes mediate intercellular transmission of porcine reproductive and respiratory syndrome virus. J Virol. https://doi.org/10.1128/JVI.01734-17
Feng Z, Hensley L, McKnight KL, Hu F, Madden V, Ping L, Jeong SH, Walker C, Lanford RE, Lemon SM (2013) A pathogenic picornavirus acquires an envelope by hijacking cellular membranes. Nature 496:367–371
Mao L, Wu J, Shen L, Yang J, Chen J, Xu H (2016) Enterovirus 71 transmission by exosomes establishes a productive infection in human neuroblastoma cells. Virus Genes 52:189–194