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

Liqin Liao; Weiguo Chen; Xiangyu Zhang; Huanmin Zhang; Aijun Li; Yiming Yan; Zi Xie; Hongxing Li; Wencheng Lin; Jingyun Ma; Xinheng Zhang; Qingmei Xie

doi:10.1016/j.virs.2022.01.026

April 2022

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

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

Liqin Liao ^a,b,e ,
Weiguo Chen ^a,b,e,f ,
Xiangyu Zhang ^a,e ,
Huanmin Zhang ^c ,
Aijun Li ^d ,
Yiming Yan ^a,b,e ,
Zi Xie ^a,b,e ,
Hongxing Li ^a,b,e ,
Wencheng Lin ^a,b,e,f ,
Jingyun Ma ^a,b,e,f ,
Xinheng Zhang ^{a,b,e
,,} ,
Qingmei Xie ^{a,b,e,f
,,}

a Heyuan Branch, Guangdong Provincial Laboratory of Lingnan Modern Agricultural Science and Technology, College of Animal Science, South China Agricultural University, Guangzhou, 510642, China

Corresponding author: Xinheng Zhang, xhzhang@scau.edu.cn
Qingmei Xie, qmx@scau.edu.cn
Received Date: 16 June 2021
Accepted Date: 27 December 2021
Available online: 22 January 2022

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.
- Semen extracellular vesicles (SE)
- , Subgroup J avian leukosis virus (ALV-J)
- , Infection
- , Vertical transmission

Electronic Supplementary Material

10.1016j.virs.2022.01.026-ESM.docx
References
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.
Proportional views