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Isolation, identification and evolution analysis of a novel subgroup of avian leukosis virus isolated from a local Chinese yellow broiler in South China

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Abstract

Avian leukosis virus (ALV) causes high mortality associated with tumor formation and decreased fertility, and results in major economic losses in the poultry industry worldwide. Recently, a putative novel ALV subgroup virus named ALV-K was observed in Chinese local chickens. In this study, a novel ALV strain named GD14LZ was isolated from a Chinese local yellow broiler in 2014. The proviral genome was sequenced and phylogenetically analyzed. The replication ability and pathogenicity of this virus were also evaluated. The complete proviral genome sequence of GD14LZ was 7482 nt in length, with a genetic organization typical of replication-competent type C retroviruses lacking viral oncogenes. Sequence analysis showed that the gag, pol and gp37 genes of GD14LZ have high sequence similarity to those of other ALV strains (A–E subgroups), especially to those of ALV-E. The gp85 gene of the GD14LZ isolate showed a low sequence similarity to those other ALV strains (A–E subgroups) but showed high similarity to strains previously described as ALV-K. Phylogenetic analysis of gp85 also suggested that the GD14LZ isolate was related to ALV-K strains. Further study showed that this isolate replicated more slowly and was less pathogenic than other ALV strains. These results indicate that the GD14LZ isolate belongs to the novel subgroup ALV-K and probably arose by recombination of ALV-K with endogenous viruses with low replication and pathogenicity. This virus might have existed in local Chinese chickens for a long time.

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References

  1. Payne LN, Brown SR, Bumstead N, Howes K, Frazier JA, Thouless ME (1991) A novel subgroup of exogenous avian leukosis virus in chickens. J Gen Virol 72(Pt 4):801–807

    Article  PubMed  Google Scholar 

  2. Fadly AM (2003) Neoplastic diseases: leukosis/sarcomagroup. In: Diseases of poultry, 11th edn. Blackwell Publishing Co, Ames

  3. Payne LN, Nair V (2012) The long view: 40 years of avian leukosis research. Avian Pathol 41:11–19

    Article  CAS  PubMed  Google Scholar 

  4. Zhang QC, Zhao DM, Guo HJ, Cui ZZ (2010) Isolation and identification of a subgroup A avian leukosis virus from imported meat-type grand-parent chickens. Virol Sin 25:130–136

    Article  PubMed  Google Scholar 

  5. Reinisova M, Plachy J, Kucerova D, Senigl F, Vinkler M, Hejnar J (2016) Genetic diversity of NHE1, receptor for subgroup J avian leukosis virus, in domestic chicken and wild anseriform species. PLoS One 11:e150589

    Article  Google Scholar 

  6. Zhao DM, Zhang QC, Cui ZZ (2010) Isolation and identification of a subgroup B avian leukosis virus from chickens of Chinese native breed Luhua. Bing Du Xue Bao 26:53–57 (in Chinese, with English abstract)

    CAS  PubMed  Google Scholar 

  7. Ji J, Li H, Zhang H, Xie Q, Chang S, Shang H, Ma J, Bi Y (2012) Complete genome sequence of an avian leukosis virus isolate associated with hemangioma and myeloid leukosis in egg-type and meat-type chickens. J Virol 86:10907–10908

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Li H, Xue C, Ji J, Chang S, Shang H, Zhang L, Ma J, Bi Y, Xie Q (2012) Complete genome sequence of a J subgroup avian leukosis virus isolated from local commercial broilers. J Virol 86:11937–11938

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Chang SW, Hsu MF, Wang CH (2013) Gene detection, virus isolation, and sequence analysis of avian leukosis viruses in Taiwan country chickens. Avian Dis 57:172–177

    Article  PubMed  Google Scholar 

  10. Wang X, Zhao P, Cui ZZ (2012) Identification of a new subgroup of avian leukosis virus isolated from Chinese indigenous chicken breeds. Bing Du Xue Bao 28:609–614 (in Chinese, with English abstract)

    CAS  PubMed  Google Scholar 

  11. Cui N, Su S, Chen Z, Zhao X, Cui Z (2014) Genomic sequence analysis and biological characteristics of a rescued clone of avian leukosis virus strain JS11C1, isolated from indigenous chickens. J Gen Virol 95:2512–2522

    Article  PubMed  Google Scholar 

  12. Dong X, Zhao P, Xu B, Fan J, Meng F, Sun P, Ju S, Li Y, Chang S, Shi W, Cui Z (2015) Avian leukosis virus in indigenous chicken breeds, China. Emerg Microbes Infect 4:e76

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Maas R, van Zoelen D, Oei H, Claassen I (2006) Replacement of primary chicken embryonic fibroblasts (CEF) by the DF-1 cell line for detection of avian leucosis viruses. Biologicals 34:177–181

    Article  CAS  PubMed  Google Scholar 

  14. Smith EJ, Fadly A, Okazaki W (1979) An enzyme-linked immunosorbent assay for detecting avian leukosis-sarcoma viruses. Avian Dis 23:698–707

    Article  CAS  PubMed  Google Scholar 

  15. Chen W, Liu Y, Li H, Chang S, Shu D, Zhang H, Chen F, Xie Q (2015) Intronic deletions of tva receptor gene decrease the susceptibility to infection by avian sarcoma and leukosis virus subgroup A. Sci Rep 5:9900

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Himly M, Foster DN, Bottoli I, Iacovoni JS, Vogt PK (1998) The DF-1 chicken fibroblast cell line: transformation induced by diverse oncogenes and cell death resulting from infection by avian leukosis viruses. Virology 248:295–304

    Article  CAS  PubMed  Google Scholar 

  17. Schaefer-Klein J, Givol I, Barsov EV, Whitcomb JM, VanBrocklin M, Foster DN, Federspiel MJ, Hughes SH (1998) The EV-O-derived cell line DF-1 supports the efficient replication of avian leukosis-sarcoma viruses and vectors. Virology 248:305–311

    Article  CAS  PubMed  Google Scholar 

  18. Chesters PM, Smith LP, Nair V (2006) E (XSR) element contributes to the oncogenicity of Avian leukosis virus (subgroup J). J Gen Virol 87(Pt 9):2685–2692

    Article  CAS  PubMed  Google Scholar 

  19. Laimins LA, Tsichlis P, Khoury G (1984) Multiple enhancer domains in the 3’ terminus of the Prague strain of Rous sarcoma virus. Nucleic Acids Res 12:6427–6442

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Cullen BR, Raymond K, Ju G (1985) Functional analysis of the transcription control region located within the avian retroviral long terminal repeat. Mol Cell Biol 5:438–447

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Zachow KR, Conklin KF (1992) CArG, CCAAT, and CCAAT-like protein binding sites in avian retrovirus long terminal repeat enhancers. J Virol 66:1959–1970

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Barbosa T, Zavala G, Cheng S (2008) Molecular characterization of three recombinant isolates of avian leukosis virus obtained from contaminated Marek’s disease vaccines. Avian Dis 52:245–252

    Article  PubMed  Google Scholar 

  23. Ryden TA, Beemon K (1989) Avian retroviral long terminal repeats bind CCAAT/enhancer-binding protein. Mol Cell Biol 9:1155–1164

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Ruddell A (1995) Transcription regulatory elements of the avian retroviral long terminal repeat. Virology 206:1–7

    Article  CAS  PubMed  Google Scholar 

  25. Zavala G, Cheng S (2006) Detection and characterization of avian leukosis virus in Marek’s disease vaccines. Avian Dis 50:209–215

    Article  PubMed  Google Scholar 

  26. Silva RF, Fadly AM, Taylor SP (2007) Development of a polymerase chain reaction to differentiate avian leukosis virus (ALV) subgroups: detection of an ALV contaminant in commercial Marek’s disease vaccines. Avian Dis 51:663–667

    Article  PubMed  Google Scholar 

  27. Cui Z, Du Y, Zhang Z, Silva RF (2003) Comparison of Chinese field strains of avian leukosis subgroup J viruses with prototype strain HPRS-103 and United States strains. Avian Dis 47:1321–1330

    Article  PubMed  Google Scholar 

  28. Summers BACJ (ed) (1995) Tumors of the central nervous system. In: Veterinary neuropathology. Mosby-Year Book, St Louis

  29. Swayne DEFO (ed) Nervous system. In: Fletcher OJ, Abdul-Aziz T (eds) Avian histopathology, 3rd edn. American Association of Avian Pathologists, Jacksonville, pp 260–291

  30. Iwata N, Ochiai K, Hayashi K, Ohashi K, Umemura T (2002) Avian retrovirus infection causes naturally occurring glioma: Isolation and transmission of a virus from so-called fowl glioma. Avian Pathol 31:193–199

    Article  CAS  Google Scholar 

  31. Nakamura S, Ochiai K, Hatai H, Ochi A, Sunden Y, Umemura T (2011) Pathogenicity of avian leukosis viruses related to fowl glioma-inducing virus. Avian Pathol 40:499–505

    Article  Google Scholar 

  32. Hatai H, Ochiai K, Nagakura K, Imanishi S, Ochi A, Kozakura R, Ono M, Goryo M, Ohashi K, Umemura T (2008) A recombinant avian leukosis virus associated with fowl glioma in layer chickens in Japan. Avian Pathol 37:127–137

    Article  CAS  PubMed  Google Scholar 

  33. Gowda S, Rao AS, Kim YW, Guntaka RV (1998) Identification of sequences in the long terminal repeat of avian sarcoma virus required for efficient transcription. Virology 162:243–247

    Article  Google Scholar 

  34. Gao Y, Guan X, Liu Y, Li X, Yun B, Qi X, Wang Y, Gao H, Cui H, Liu C (2015) An avian leukosis virus subgroup J isolate with a Rous sarcoma virus-like 5’-LTR shows enhanced replication capability. J Gen Virol 96:150–158

    Article  CAS  PubMed  Google Scholar 

  35. Zavala G, Cheng S (2006) Experimental infection with avian leukosis virus isolated from Marek’s disease vaccines. Avian Dis 50:232–237

    Article  PubMed  Google Scholar 

  36. Ochi A, Ochiai K, Kobara A, Nakamura S, Hatai H, Handharyani E, Tiemann I, Tanaka IR, Toyoda T, Abe A (2012) Epidemiological study of fowl glioma-inducing virus in chickens in Asia and Germany. Avian Pathol 41:299–309

    Article  PubMed  Google Scholar 

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Acknowledgements

This study was supported by the Natural Science Foundation of Guangdong Province (Grant No. S2013030013313), the National Natural Science Foundation of China (Grant No. 31472217), and the Guangdong Province Science and Technology Plan Project (Grant No. 2012B020306002, 2012B091100078).

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Authors and Affiliations

  1. College of Animal Science, South China Agricultural University, No. 483 Wushan Road, Tianhe District, Guangzhou, Guangdong, People’s Republic of China

    Xinjian Li, Wencheng Lin, Xinheng Zhang, Yang Liu, Weiguo Chen, Feng Chen & Qingmei Xie

  2. Guangdong Provincial Key Lab of Agro-Animal Genomics and Molecular Breeding and Key Laboratory of Chicken Genetics, Breeding and Reproduction, Ministry of Agriculture, Guangzhou, 510642, People’s Republic of China

    Xinjian Li, Wencheng Lin, Xinheng Zhang, Yang Liu, Weiguo Chen, Feng Chen & Qingmei Xie

  3. College of Veterinary Medicine, Shandong Agricultural University, Taian, 271018, People’s Republic of China

    Shuang Chang & Peng Zhao

  4. Institute of Animal Science, Guangdong Academy of Agriculture Sciences, Guangzhou, 510640, People’s Republic of China

    Baohong Li & Dingming Shu

  5. USDA, Agriculture Research Service, Avian Disease and Oncology Laboratory, East Lansing, MI, 48823, USA

    Huanmin Zhang

  6. Key Laboratory of Animal Health Aquaculture and Environmental Control, Guangzhou, 510642, Guangdong, People’s Republic of China

    Wencheng Lin, Feng Chen & Qingmei Xie

  7. South China Collaborative Innovation Center for Poultry Disease Control and Product Safety, Guangzhou, 510642, People’s Republic of China

    Wencheng Lin & Qingmei Xie

Authors
  1. Xinjian Li
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  2. Wencheng Lin
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  3. Shuang Chang
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  4. Peng Zhao
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  5. Xinheng Zhang
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  6. Yang Liu
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  7. Weiguo Chen
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  8. Baohong Li
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  9. Dingming Shu
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  10. Huanmin Zhang
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  11. Feng Chen
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  12. Qingmei Xie
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Corresponding author

Correspondence to Qingmei Xie.

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The authors declare that have no competing interests.

Ethics statement

The animal experiment was carried out in accordance with the institutional and national guidelines for the use and care of laboratory animals. Use of animals in this study was approved by the South China Agricultural University Committee of Animal Experiments (approval ID: 201004152).

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Li, X., Lin, W., Chang, S. et al. Isolation, identification and evolution analysis of a novel subgroup of avian leukosis virus isolated from a local Chinese yellow broiler in South China. Arch Virol 161, 2717–2725 (2016). https://doi.org/10.1007/s00705-016-2965-x

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  • DOI: https://doi.org/10.1007/s00705-016-2965-x

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