Liqin Liao, Weiguo Chen, Xiangyu Zhang, Huanmin Zhang, Aijun Li, Yiming Yan, Zi Xie, Hongxing Li, Wencheng Lin, Jingyun Ma, Xinheng Zhang and Qingmei Xie. Semen extracellular vesicles mediate vertical transmission of subgroup J avian leukosis virus[J]. Virologica Sinica, 2022, 37(2): 284-294. doi: 10.1016/j.virs.2022.01.026
Citation: Liqin Liao, Weiguo Chen, Xiangyu Zhang, Huanmin Zhang, Aijun Li, Yiming Yan, Zi Xie, Hongxing Li, Wencheng Lin, Jingyun Ma, Xinheng Zhang, Qingmei Xie. Semen extracellular vesicles mediate vertical transmission of subgroup J avian leukosis virus .VIROLOGICA SINICA, 2022, 37(2) : 284-294.  http://dx.doi.org/10.1016/j.virs.2022.01.026

精液细胞外囊泡介导J亚型禽白血病病毒垂直传播

  • J亚型禽白血病病毒(ALV-J)属于致瘤性的逆转录病毒,对全世界的养禽业造成严重的影响。垂直传播是J亚型禽白血病病毒的主要传染途径。大量研究表明,来源于病毒感染的细胞或者体液的细胞外囊泡可作为病毒传播的载体。然而,关于细胞外囊泡在J亚型禽白血病病毒感染中的作用尚未阐明。在本研究中,从ALV-J感染的鸡精液中分离纯化了细胞外囊泡(SE-ALV-J),通过转录组测序、反转录定量PCR和蛋白免疫印迹证明其包含了ALV-J病毒的基因组RNA和病毒蛋白;并证明SE-ALV-J能够感染宿主细胞。更重要的是,通过人工授精的方法,展示了SE-ALV-J可以感染成年母鸡进而介导ALV-J感染后代的垂直传播。总的来说,我们的结果揭示了J亚型禽白血病病毒可利用宿主精液的细胞外囊泡作为垂直传播的新的传播途径,加深了对J亚型禽白血病病毒传播机制的理解。

Semen extracellular vesicles mediate vertical transmission of subgroup J avian leukosis virus

  • Subgroup J avian leukosis virus (ALV-J) is a highly oncogenic retrovirus that has been devastating the global poultry industry since the late 1990s. The major infection model of ALV-J is vertical transmission, which is responsible for the congenital infection of progeny from generation to generation. Increasing evidence has suggested that extracellular vesicles (EVs) derived from virus-infected cells or biological fluids have been thought to be vehicles of transmission for viruses. However, the role of EVs in infection and transmission of ALV-J remains obscure. In the present study, semen extracellular vesicles (SE) were isolated and purified from ALV-J-infected rooster seminal plasma (SE-ALV-J), which was shown to contain ALV-J genomic RNA and partial viral proteins, as determined by RNA sequencing, reverse transcription-quantitative PCR and Western blotting. Furthermore, SE-ALV-J was proved to be able to transmit ALV-J infection to host cells and establish productive infection. More importantly, artificial insemination experiments showed that SE-ALV-J transmitted ALV-J infection to SPF hens, and subsequently mediated vertical transmission of ALV-J from the SPF hens to the progeny chicks. Taken together, the results of the present study suggested that ALV-J utilized host semen extracellular vesicles as a novel means for vertical transmission, enhancing our understanding on mechanisms underlying ALV-J transmission.

  • 加载中
    1. Alenquer, M., Amorim, M.J., 2015. Exosome biogenesis, regulation, and function in viral infection. Viruses 7, 5066–5083.

    2. Bai, J.H.K., Payne, L.N., Skinner, M.A., 1998. Sequence of host-range determinants in the env gene of a full-length, infectious proviral clone of exogenous avian leukosis virus HPRS-103 confirms that it represents a new subgroup (designated J). Avian Dis. 27, S92–S93.

    3. Bukong, T.N., Momen-Heravi, F., Kodys, K., Bala, S., Szabo, G., 2014. Exosomes from hepatitis C infected patients transmit HCV infection and contain replication competent viral RNA in complex with Ago2-miR122-HSP90. PLoS Pathog. 10, e1004424.

    4. Chahar, H.S., Bao, X., Casola, A., 2015. Exosomes and their role in the life cycle and pathogenesis of RNA viruses. Viruses 7, 3204–3225.

    5. Colombo, M., Raposo, G., Thery, C., 2014. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu. Rev. Cell Dev. Biol. 30, 255–289.

    6. Crenshaw, B.J., Gu, L., Sims, B., Matthews, Q.L., 2018. Exosome biogenesis and biological function in response to viral infections. Open Virol. J. 12, 134–148.

    7. Dhama, K., Singh, R., Karthik, K., Chakraborty, S., Tiwari, R., Wani, M.Y., Mohan, J., 2014. Artificial insemination in poultry and possible transmission of infectious pathogens: a review. Asian J. Anim. Vet. Adv. 9, 211–228.

    8. Fadly, A.M., Smith, E.J., 1999. Isolation and some characteristics of a subgroup J-like avian leukosis virus associated with myeloid leukosis in meat-type chickens in the United States. Avian Dis. 43, 391–400.

    9. Federspiel, M.J., Hughes, S.H., 1997. Retroviral gene delivery. Methods Cell Biol. 52, 179–214.

    10. Gurunathan, S., Kang, M.H., Jeyaraj, M., Qasim, M., Kim, J.H., 2019. Review of the isolation, characterization, biological function, and multifarious therapeutic approaches of exosomes. Cells 8.

    11. Johnstone, R.M., Adam, M., Hammond, J.R., Orr, L., Turbide, C., 1987. Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J. Biol. Chem. 262, 9412–9420.

    12. Kalluri, R., LeBleu, V.S., 2020. The biology, function, and biomedical applications of exosomes. Science 367.

    13. Kechin, A., Boyarskikh, U., Kel, A., Filipenko, M., 2017. cutPrimers: a new tool for accurate cutting of primers from reads of targeted next generation sequencing. J. Comput. Biol. 24, 1138–1143.

    14. Kumar, A., Kodidela, S., Tadrous, E., Cory, T.J., Walker, C.M., Smith, A.M., Mukherjee, A., Kumar, S., 2020. Extracellular vesicles in viral replication and pathogenesis and their potential role in therapeutic intervention. Viruses 12.

    15. Landman, W.J., Post, J., Boonstra-Blom, A.G., Buyse, J., Elbers, A.R., Koch, G., 2002. Effect of an in ovo infection with a Dutch avian leukosis virus subgroup J isolate on the growth and immunological performance of SPF broiler chickens. Avian Pathol. 31, 59–72.

    16. Langmead, B., Salzberg, S.L., 2012. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359.

    17. Li, T., Yao, X., Li, C., Zhang, J., Xie, Q., Wang, W., Lu, H., Fu, H., Li, L., Xie, J., Shao, H., Gao, W., Qin, A., Ye, J., 2020. Gp37 regulates the pathogenesis of avian leukosis virus subgroup J via its C terminus. J. Virol. 94.

    18. Lin, Y., Xia, J., Zhao, Y., Wang, F.Y., Yu, S.C., Zou, N.L., Wen, X.T., Cao, S.J., Huang, Y., 2013. Reproduction of hemangioma by infection with subgroup J avian leukosis virus:the vertical transmission is more hazardous than the horizontal way. Virol. J. 10.

    19. Longatti, A., 2015. The dual role of exosomes in hepatitis A and C virus transmission and viral immune activation. Viruses 7, 6707–6715.

    20. Madison, M.N., Jones, P.H., Okeoma, C.M., 2015. Exosomes in human semen restrict HIV-1 transmission by vaginal cells and block intravaginal replication of LP-BM5 murine AIDS virus complex. Virology 482, 189–201.

    21. Madison, M.N., Roller, R.J., Okeoma, C.M., 2014. Human semen contains exosomes with potent anti-HIV-1 activity. Retrovirology 11, 102.

    22. Malhotra, S., Justice, J., Lee, N., Li, Y., Zavala, G., Ruano, M., Morgan, R., Beemon, K., 2015. Complete genome sequence of an American avian leukosis virus subgroup J isolate that causes hemangiomas and myeloid leukosis. Genome Announc. 3, e01586-01514.

    23. Meng, F., Li, Q., Zhang, Y., Cui, Z., Chang, S., Zhao, P., 2018a. Isolation and characterization of subgroup J Avian Leukosis virus associated with hemangioma in commercial Hy-Line chickens. Poultry Sci. 97, 2667–2674.

    24. Meng, F., Li, Q., Zhang, Y., Zhang, Z., Tian, S., Cui, Z., Chang, S., Zhao, P., 2018b. Characterization of subgroup J avian Leukosis virus isolated from Chinese indigenous chickens. Virol. J. 15, 33.

    25. Muller, L., 2020. Exosomes: nanodust? HNO 68, 56–59.

    26. Neoplastic Diseases. Diseases of Poultry. https://doi.org/10.1002/9781119421481.ch1 52013, 513-673.

    27. Payne, L.N., Brown, S.R., Bumstead, N., Howes, K., Frazier, J.A., Thouless, M.E., 1991. A novel subgroup of exogenous avian leukosis virus in chickens. J. Gen. Virol. 72 (Pt 4), 801–807.

    28. Payne, L.N., Gillespie, A.M., Howes, K., 1993. Unsuitability of chicken sera for detection of exogenous ALV by the group-specific antigen ELISA. Vet. Rec. 132, 555–557.

    29. Payne, L.N., Nair, V., 2012. The long view: 40 years of avian leukosis research. Avian Pathol. 41, 11–19.

    30. Rubin, H., Fanshier, L., Cornelius, A., Hughes, W.F., 1962. Tolerance and immunity in chickens after congenital and contact infection with an avian leukosis virus. Virology 17, 143–156.

    31. Sadri, N.J., Bokharaei-Salim, F., Karimzadeh, M., Moghoofei, M., Karampoor, S., Mirzaei, H.R., Tabibzadeh, A., Jafari, A., Ghaderi, A., Asemi, Z., Mirzaei, H., Hamblin, M.R., 2019. MicroRNAs and Exosomes: Key Players in HIV Pathogenesis. HIV Med.

    32. Shen, Y., Cai, L., Wang, Y., Wei, R., He, M., Wang, S., Wang, G., Cheng, Z., 2014. Genetic mutations of avian leukosis virus subgroup J strains extended their host range. J. Gen. Virol. 95, 691–699.

    33. Slonchak, A., Clarke, B., Mackenzie, J., Amarilla, A.A., Setoh, Y.X., Khromykh, A.A., 2019. West Nile virus infection and interferon alpha treatment alter the spectrum and the levels of coding and noncoding host RNAs secreted in extracellular vesicles. BMC Genom. 20, 474.

    34. Smith, E.J., Fadly, A.M., 1994. Male-mediated venereal transmission of endogenous avian leukosis virus. Poultry Sci. 73, 488–494.

    35. Thery, C., Zitvogel, L., Amigorena, S., 2002. Exosomes: composition, biogenesis and function. Nat. Rev. Immunol. 2, 569–579.

    36. Urbanelli, L., Buratta, S., Tancini, B., Sagini, K., Delo, F., Porcellati, S., Emiliani, C., 2019. The role of extracellular vesicles in viral infection and transmission. Vaccines (Basel) vol. 7.

    37. van Niel, G., D'Angelo, G., Raposo, G., 2018. Shedding light on the cell biology of extracellular vesicles. Nat. Rev. Mol. Cell Biol. 19, 213–228.

    38. Venugopal, K., Howes, K., Barron, G.S., Payne, L.N., 1997. Recombinant env-gp85 of HPRS-103 (subgroup J) avian leukosis virus: antigenic characteristics and usefulness as a diagnostic reagent. Avian Dis. 41, 283–288.

    39. Vojtech, L., Woo, S., Hughes, S., Levy, C., Ballweber, L., Sauteraud, R.P., Strobl, J., Westerberg, K., Gottardo, R., Tewari, M., Hladik, F., 2014. Exosomes in human semen carry a distinctive repertoire of small non-coding RNAs with potential regulatory functions. Nucleic Acids Res. 42, 7290–7304.

    40. Vora, A., Zhou, W., Londono-Renteria, B., Woodson, M., Sherman, M.B., Colpitts, T.M., Neelakanta, G., Sultana, H., 2018. Arthropod EVs mediate dengue virus transmission through interaction with a tetraspanin domain containing glycoprotein Tsp29Fb.Proc. Natl. Acad. Sci. U. S. A. 115, E6604–E6613.

    41. Wang, G., Wang, Z., Zhuang, P., Zhao, X., Cheng, Z., 2017. Exosomes carring gag/env of ALV-J possess negative effect on immunocytes. Microb. Pathog. 112, 142–147.

    42. Wang, P., Li, M., Li, H., Lin, L., Shi, M., Gu, Z., Gao, Y., Huang, T., Mo, M., Wei, T., Wei, P., 2020. Full-length cDNA sequence analysis of 85 avian leukosis virus subgroup J strains isolated from chickens in China during the years 1988-2018:coexistence of 2 extremely different clusters that are highly dependent upon either the host genetic background or the geographic location. Poultry Sci. 99, 3469–3480.

    43. Wang, P., Lin, L., Li, H., Yang, Y., Huang, T., Wei, P., 2018. Diversity and evolution analysis of glycoprotein GP85 from avian leukosis virus subgroup J isolates from chickens of different genetic backgrounds during 1989-2016: coexistence of five extremely different clusters. Arch. Virol. 163, 377–389.

    44. Wang, Q., Gao, Y., Wang, Y., Qin, L., Qi, X., Qu, Y., Gao, H., Wang, X., 2012. A 205-nucleotide deletion in the 30 untranslated region of avian leukosis virus subgroup J, currently emergent in China, contributes to its pathogenicity. J. Virol. 86, 12849.

    45. Wang, T., Fang, L., Zhao, F., Wang, D., Xiao, S., 2018. Exosomes mediate intercellular transmission of porcine reproductive and respiratory syndrome virus. J. Virol. 92.

    46. Welch, J.L., Kaddour, H., Schlievert, P.M., Stapleton, J.T., Okeoma, C.M., 2018. Semen exosomes promote transcriptional silencing of HIV-1 by disrupting NF-kappaB/Sp1/Tat circuitry. J. Virol. 92.

    47. Welch, J.L., Madison, M.N., Margolick, J.B., Galvin, S., Gupta, P., Martinez-Maza, O., Dash, C., Okeoma, C.M., 2017. Effect of prolonged freezing of semen on exosome recovery and biologic activity. Sci. Rep. 7, 45034.

    48. Zhang, X., Yan, Z., Li, X., Lin, W., Dai, Z., Yan, Y., Lu, P., Chen, W., Zhang, H., Chen, F., Ma, J., Xie, Q., 2016. GADD45beta, an anti-tumor gene, inhibits avian leukosis virus subgroup J replication in chickens. Oncotarget 7, 68883–68893.

    49. Zhou, D., Xue, J., Zhang, Y., Wang, G., Feng, Y., Hu, L., Shang, Y., Cheng, Z., 2019. Outbreak of myelocytomatosis caused by mutational avian leukosis virus subgroup J in China, 2018. Transboundary Emerg. Dis. 66, 622–626.

    50. Zhou, W., Woodson, M., Neupane, B., Bai, F., Sherman, M.B., Choi, K.H., Neelakanta, G., Sultana, H., 2018. 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. 14, e1006764.

    51. Zhou, Y., McNamara, R.P., Dittmer, D.P., 2020. Purification methods and the presence of RNA in virus particles and extracellular vesicles. Viruses 12.

  • 加载中
  • 10.1016j.virs.2022.01.026-ESM.docx

Article Metrics

Article views(4720) PDF downloads(11) Cited by(0)

Related
Proportional views
    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Semen extracellular vesicles mediate vertical transmission of subgroup J avian leukosis virus

      Corresponding author: Xinheng Zhang, xhzhang@scau.edu.cn
      Corresponding author: Qingmei Xie, qmx@scau.edu.cn
    • a Heyuan Branch, Guangdong Provincial Laboratory of Lingnan Modern Agricultural Science and Technology, College of Animal Science, South China Agricultural University, Guangzhou, 510642, China

    Abstract: Subgroup J avian leukosis virus (ALV-J) is a highly oncogenic retrovirus that has been devastating the global poultry industry since the late 1990s. The major infection model of ALV-J is vertical transmission, which is responsible for the congenital infection of progeny from generation to generation. Increasing evidence has suggested that extracellular vesicles (EVs) derived from virus-infected cells or biological fluids have been thought to be vehicles of transmission for viruses. However, the role of EVs in infection and transmission of ALV-J remains obscure. In the present study, semen extracellular vesicles (SE) were isolated and purified from ALV-J-infected rooster seminal plasma (SE-ALV-J), which was shown to contain ALV-J genomic RNA and partial viral proteins, as determined by RNA sequencing, reverse transcription-quantitative PCR and Western blotting. Furthermore, SE-ALV-J was proved to be able to transmit ALV-J infection to host cells and establish productive infection. More importantly, artificial insemination experiments showed that SE-ALV-J transmitted ALV-J infection to SPF hens, and subsequently mediated vertical transmission of ALV-J from the SPF hens to the progeny chicks. Taken together, the results of the present study suggested that ALV-J utilized host semen extracellular vesicles as a novel means for vertical transmission, enhancing our understanding on mechanisms underlying ALV-J transmission.

    Reference (51) Relative (20)

    目录

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return