Serum-derived exosomes from non-viremic animals previously exposed to the porcine respiratory and reproductive virus contain antigenic viral proteins

Montaner-Tarbes, Sergio; Borràs, Francesc E.; Montoya, María; Fraile, Lorenzo; Portillo, Hernando A. del

doi:10.1186/s13567-016-0345-x

Cited by 39 publications

(46 citation statements)

References 47 publications

(52 reference statements)

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“…The role of exosomes in the transfer of infectious agents between cells and tissues has been postulated and demonstrated in several infections. Current studies on exosomes predominately focus on infection and pathogenic mechanisms of human viruses, with little emphasis on the interaction of exosomes and non-human animal virus infection outside of porcine reproductive and respiratory syndrome virus (PRRSV), newcastle disease virus (NDV) and foot-and-month disease viruses (FMDV) [25,28,32]. Exosomes contributed to the virus replication and transmission in the above virus infection, playing various functions as delivering viral components and promoting virus replication at the recipient cells.…”

Section: Discussionmentioning

confidence: 99%

“…Exosomes have proved to carry pathogen-associated materials of infected cells, along with the host components [1,16,25,28]. The viral protein, RNAs even viral particles have been identified in exosomes from virus-infected cells [7,12,28,29]. To characterize the molecular composition of the exosomes, we performed mass spectrometry on the proteins contained in the exosomes for proteomic analysis.…”

Section: Exosomes Delivered Cpiv3 Components and Established Productimentioning

confidence: 99%

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Exosomes promote caprine parainfluenza virus type 3 infection by inhibiting autophagy

Liang

et al. 2020

Journal of General Virology

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Caprine parainfluenza virus type 3 (CPIV3) is a novel important pathogen causing respiratory disease in goats, but the pathogenic mechanism is not clear yet. Evidence suggests that exosomes transfer biologically active molecules between cells. Viral infections can cause profound changes in exosome components, and exosomes have been involved in viral transmission and pathogenicity. In this study, we explored the characteristics and functions of exosomes purified from the supernatant of Madin–Darby bovine kidney (MDBK) cells inoculated with CPIV3. Infection of CPIV3 showed increased exosome secretion and the loading of viral proteins and RNA into exosomes. These exosomes were capable of transferring CPIV3 genetic materials to recipient cells to establish a productive infection and promote the viral replication. To explore the potential mechanism, small RNA deep sequencing revealed that CPIV3 exosomes contained a diverse range of RNA species, including miRNA and piRNA, in proportions different from exosomes isolated from mock-infected cells. Expression patterns of 11 differentially expressed miRNAs were subsequently validated by quantitative reverse transcriptase PCR (qRT-PCR). Targets of miRNAs were predicted and functional annotation analysis showed that the main pathways involved were autophagy signalling ways. Autophagy inhibited by the CPIV3-exosome was further verified, and miR-126–3 p_2 packaged in the vesicles was an important regulation factor in this process. Inhibition of autophagy may be one of the responsible reasons for promoting efficient replication of exosome-mediated CPIV3 infection. The study suggests that exosomes are key in pathogenesis or protection against CPIV3. Further understating of their role in CPIV3 infection may bring novel insight to the development of protection measures.

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Section: Discussionmentioning

confidence: 99%

Section: Exosomes Delivered Cpiv3 Components and Established Productimentioning

confidence: 99%

Exosomes promote caprine parainfluenza virus type 3 infection by inhibiting autophagy

Liang

et al. 2020

Journal of General Virology

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“…The main target cells for PRRSV infection are certain lineages of monocytes/macrophages in vivo. The PRRSV effect on JAK-STAT signaling in T cells would be indirect, such as by exosomes from infected cells (Garcia-Nicolas et al, 2016;Montaner-Tarbes et al, 2016). But its interference of the JAK-STAT signaling in infected macrophages would have significant consequence as the response of PAMs against viral or bacterial pathogens is critical in determining the outcome of infection in the host.…”

Section: Prrsv's Effect On Stat2/5/6 Signalingmentioning

confidence: 99%

Antagonizing cytokine-mediated JAK-STAT signaling by porcine reproductive and respiratory syndrome virus

Yang

Zhang

2017

Veterinary Microbiology

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Janus kinase (JAK)-signal transducer and activator of transcription (STAT) signaling pathway is activated by myriad cytokines, which are involved in regulation of cell growth, proliferation, differentiation, apoptosis, angiogenesis, immunity and inflammatory response. Because of its significance in immune response, JAK-STAT pathway is often targeted by pathogens, including porcine reproductive and respiratory syndrome virus (PRRSV). PRRSV causes reproductive failure in sows and respiratory disease in pigs of all ages. A typical feature of the immune response to PRRSV infection in pigs is delayed production and low titer of virus neutralizing antibodies, and weak cell-mediated immune response. One of the possible reasons for the weak protective immune response is that PRRSV interferes with cytokine-mediated JAK-STAT signaling. PRRSV inhibits interferon-activated JAK-STAT signaling by blocking nuclear translocation of STAT1 and STAT2. The mechanism is that PRRSV non-structural protein 1β (nsp1β) induces degradation of karyopherin α1 (KPNA1), a critical adaptor in nucleo-cytoplasmic transport. PRRSV also antagonizes IL6-activated JAK-STAT3 signaling via inducing degradation of STAT3. In this review, we briefly introduce JAK-STAT signaling, summarize the PRRSV interference with it, and provide perspective on the perturbation in the context of PRRSV-elicited immune response.

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“…We previously analyzed the secretome of cells infected with PRRSV and found that approximately 72.4% of all the secretory proteins identified were listed in the ExoCarta database (17), suggesting that the release of exosomal proteins was strongly activated by PRRSV infection. A recent study also identified viral proteins of PRRSV in serumderived exosomes from pigs actively or previously infected with PRRSV (18).…”

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confidence: 94%

Exosomes Mediate Intercellular Transmission of Porcine Reproductive and Respiratory Syndrome Virus

Wang

Fang

Zhao

et al. 2018

J Virol

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Exosomes are small membrane-enclosed vesicles produced by various cells and actively released into the extracellular space. They participate in intercellular communication and transfer of biologically active proteins, lipids, and nucleic acids. Accumulating evidence suggests that exosomes derived from cells infected by some viruses selectively encapsulate viral proteins, genetic materials, or even virions to mediate cell-to-cell communication and/or virus transmission. Porcine reproductive and respiratory syndrome virus (PRRSV) is an that has been devastating the global swine industry since the late 1980s. Recent studies have shown that major proteins secreted from PRRSV-infected cells are exosomal proteins and that the serum-derived exosomes from PRRSV-infected pigs contain viral proteins. However, the role of exosomes in PRRSV infection remains unclear. In this study, purified exosomes isolated from PRRSV-infected cells were shown with reverse transcription-PCR and mass spectrometry to contain viral genomic RNA and partial viral proteins. Furthermore, exosomes from PRRSV-infected cells established productive infection in both PRRSV-susceptible and -nonsusceptible cells. More importantly, exosome-mediated infection was not completely blocked by PRRSV-specific neutralizing antibodies. In summary, this study demonstrated that exosomes can mediate PRRSV transmission and are even resistant to antibody neutralization, identifying a potential immune evasion mechanism utilized by PRRSV. Exosomes have recently been characterized as bioactive vesicles that function to promote intercellular communication. The exosomes from virally infected cells containing altered compositions confer numerous novel functionalities. A study of the secretome of cells infected with PRRSV indicated that the exosomal pathway is strongly activated by PRRSV infection. Here, we demonstrate that PRRSV can utilize host exosomes to infect naive healthy cells. Furthermore, exosome-mediated viral transmission is largely resistant to PRRSV-specific neutralizing antibodies. Our study provides novel insights into an alternative mechanism of PRRSV transmission that can compromise the host's anti-PRRSV immune response.

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Serum-derived exosomes from non-viremic animals previously exposed to the porcine respiratory and reproductive virus contain antigenic viral proteins

Cited by 39 publications

References 47 publications

Exosomes promote caprine parainfluenza virus type 3 infection by inhibiting autophagy

Exosomes promote caprine parainfluenza virus type 3 infection by inhibiting autophagy

Antagonizing cytokine-mediated JAK-STAT signaling by porcine reproductive and respiratory syndrome virus

Exosomes Mediate Intercellular Transmission of Porcine Reproductive and Respiratory Syndrome Virus

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