Abstract
Avian leukosis virus (ALV) caused tremendous economic losses to poultry industry all over the world, especially in China. One natural recombinant ALV strain, designated as HB2015032, was isolated from indigenous chickens with neoplastic diseases in Hubei, China. The complete proviral genome of HB2015032 is 7703 bp in length. Sequence analysis showed that the Env of HB2015032 exhibited 99.3% similarity with that of a ALV subgroup K (ALV-K) isolate JS11C1 at amino acid level. Phylogenetic analysis revealed that both gp85 and gp37 of HB2015032 were clustered in the same branch with JS11C1 and other ALV-K strains isolated from Chinese indigenous chickens in recent years. However, the pol gene, the 3′ untranslated region (3′ UTR), and the 3′ long terminal repeat (3′ LTR) of HB2015032 were more closely related to ALV-J prototype HPRS-103, and clustered in the same branch with ALV-J strains. Furthermore, the pol gene of HB2015032 contained a premature stop codon that resulted in a truncated Pol protein with 22 amino acid residues missing, which was a unique feature of the pol gene of ALV-J. 3′UTR of HB2015032 containing entire DR1, E element and U3. E element of HB2015032 contained one base deletion, which resulted in a c-Ets-1 binding site. In addition, U3 region of HB2015032 contains most of the transcription regulatory elements of ALV-J, including two CAAT boxes, Y boxes, CArG boxes, PRE boxes, NFAP-1 boxes, and one TATA box. These results suggest that isolate HB2015032 was a novel recombinant ALV-K containing the ALV-K env gene and the ALV-J backbone and exhibiting high pathogenicity.
References
Fadly AM (2000) Isolation and identification of avian leukosis viruses: a review. Avian Pathol 29:529–535
Payne LN, Nair V (2012) The long view: 40 years of avian leukosis research. Avian Pathol 41:11–19
Kim YJ, Park SI, Park SJ, Kim HH, Jung YW, Kwon JT, Jang BG, Kim HK, Cho KO (2008) Molecular analysis of endogenous avian leukosis/sarcoma virus genomes in Korean chicken embryos. J Vet Med Sci 70:17–23
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
Smith LM, Toye AA, Howes K, Bumstead N, Payne LN, Venugopal K (1999) Novel endogenous retroviral sequences in the chicken genome closely related to HPRS-103 (subgroup J) avian leukosis virus. J Gen Virol 80(Pt 1):261–268
Payne LN, Howes K, Gillespie AM, Smith LM (1992) Host range of Rous sarcoma virus pseudotype RSV(HPRS-103) in 12 avian species: support for a new avian retrovirus envelope subgroup, designated J. J Gen Virol 73(Pt 11):2995–2997
Gao YL, Qin LT, Pan W, Wang YQ, Le Qi X, Gao HL, Wang XM (2010) Avian leukosis virus subgroup J in layer chickens, China. Emerg Infect Dis 16:1637–1638
Li J, Meng F, Li W, Wang Y, Chang S, Zhao P, Cui Z (2018) Characterization of avian leukosis virus subgroup J isolated between 1999 and 2013 in China. Poult Sci 97:3532–3539
Pan W, Gao Y, Sun F, Qin L, Liu Z, Yun B, Wang Y, Qi X, Gao H, Wang X (2011) Novel sequences of subgroup J avian leukosis viruses associated with hemangioma in Chinese layer hens. Virol J 8:552
Wang G, Jiang Y, Yu L, Wang Y, Zhao X, Cheng Z (2013) Avian leukosis virus subgroup J associated with the outbreak of erythroblastosis in chickens in China. Virol J 10:92
Wang P, Yang Y, Lin L, Li H, Wei P (2017) Complete genome sequencing and characterization revealed a recombinant subgroup B isolate of avian leukosis virus with a subgroup J-like U3 region. Virus Genes 53:927–930
Lin L, Wang P, Yang Y, Li H, Huang T, Wei P (2017) Full-length genome sequence analysis of four subgroup J avian leukosis virus strains isolated from chickens with clinical hemangioma. Virus Genes 53:868–875
Zhou D, Xue J, Zhang Y, Wang G, Feng Y, Hu L, Shang Y, Cheng Z (2018) Outbreak of myelocytomatosis caused by mutational avian leukosis virus subgroup J in China, 2018. Transbound Emerg Dis 66:622–626
Cai L, Shen Y, Wang G, Guo H, Liu J, Cheng Z (2013) Identification of two novel multiple recombinant avian leukosis viruses in two different lines of layer chicken. J Gen Virol 94:2278–2286
Wu X, Zhao J, Zeng Y, Wu Y, Wang Q, Wu B, Huang Y (2017) A novel avian retrovirus associated with lymphocytoma isolated from a local Chinese flock induced significantly reduced growth and immune suppression in SPF chickens. Vet Microbiol 205:34–38
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
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
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
Li X, Lin W, Chang S, Zhao P, Zhang X, Liu Y, Chen W, Li B, Shu D, Zhang H, Chen F, Xie Q (2016) 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
Shao H, Wang L, Sang J, Li T, Liu Y, Wan Z, Qian K, Qin A, Ye J (2017) Novel avian leukosis viruses from domestic chicken breeds in mainland China. Arch Virol 162:2073–2076
Su Q, Li Y, Li W, Cui S, Tian S, Cui Z, Zhao P, Chang S (2018) Molecular characteristics of avian leukosis viruses isolated from indigenous chicken breeds in China. Poult Sci 97:2917–2925
Gao Q, Yun B, Wang Q, Jiang L, Zhu H, Gao Y, Qin L, Wang Y, Qi X, Gao H, Wang X, Gao Y (2014) Development and application of a multiplex PCR method for rapid differential detection of subgroup A, B, and J avian leukosis viruses. J Clin Microbiol 52:37–44
Gopal S, Manoharan P, Kathaperumal K, Chidambaram B, Divya KC (2012) Differential detection of avian oncogenic viruses in poultry layer farms and Turkeys by use of multiplex PCR. J Clin Microbiol 50:2668–2673
Dong X, Zhao P, Li W, Chang S, Li J, Li Y, Ju S, Sun P, Meng F, Liu J, Cui Z (2015) Diagnosis and sequence analysis of avian leukosis virus subgroup J isolated from Chinese Partridge Shank chickens. Poult Sci 94:668–672
Benson SJ, Ruis BL, Garbers AL, Fadly AM, Conklin KF (1998) Independent isolates of the emerging subgroup J avian leukosis virus derive from a common ancestor. J Virol 72:10301–10304
Su Q, Zhang Y, Li Y, Cui Z, Chang S, Zhao P (2018) Epidemiological investigation of the novel genotype avian hepatitis E virus and co-infected immunosuppressive viruses in farms with hepatic rupture haemorrhage syndrome, recently emerged in China. Transbound Emerg Dis 66:776–784
Bai J, Payne LN, Skinner MA (1995) HPRS-103 (exogenous avian leukosis virus, subgroup J) has an env gene related to those of endogenous elements EAV-0 and E51 and an E element found previously only in sarcoma viruses. J Virol 69:779–784
Liu C, Zheng S, Wang Y, Jing L, Gao H, Gao Y, Qi X, Qin L, Pan W, Wang X (2011) Detection and molecular characterization of recombinant avian leukosis viruses in commercial egg-type chickens in China. Avian Pathol 40:269–275
Zavala G, Cheng S, Jackwood MW (2007) Molecular epidemiology of avian leukosis virus subgroup J and evolutionary history of its 3′ untranslated region. Avian Dis 51:942–953
Gao Y, Yun B, Qin L, Pan W, Qu Y, Liu Z, Wang Y, Qi X, Gao H, Wang X (2012) Molecular epidemiology of avian leukosis virus subgroup J in layer flocks in China. J Clin Microbiol 50:953–960
Lai H, Zhang H, Ning Z, Chen R, Zhang W, Qing A, Xin C, Yu K, Cao W, Liao M (2011) Isolation and characterization of emerging subgroup J avian leukosis virus associated with hemangioma in egg-type chickens. Vet Microbiol 151:275–283
Zeng X, Liu L, Hao R, Han C (2014) Detection and molecular characterization of J subgroup avian leukosis virus in wild ducks in China. PLoS ONE 9:e94980
Lv L, Li T, Hu M, Deng J, Liu Y, Xie Q, Shao H, Ye J, Qin A (2019) A recombination efficiently increases the pathogenesis of the novel K subgroup of avian leukosis virus. Vet Microbiol 231:214–217
Acknowledgements
This work was supported by National Natural Science Foundation of China (Grant No. 31640081) and State Key Laboratory of Veterinary Biotechnology Foundation, China (Grant No. SKLVBF201708).
Author information
Authors and Affiliations
Contributions
This work was designed, performed, and written by XL and YG. XC, TL, YG, XW, SF, and CF helped in virus isolation and data analysis. YY contributed materials and reagents, supervised the work, and evaluated the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
No potential conflict of interest was declared by the authors.
Ethical approval
All applicable international, national, and institutional guidelines for the use and care of animals were followed.
Additional information
Edited by Juergen A Richt.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Liang, X., Gu, Y., Chen, X. et al. Identification and characterization of a novel natural recombinant avian leucosis virus from Chinese indigenous chicken flock. Virus Genes 55, 726–733 (2019). https://doi.org/10.1007/s11262-019-01695-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11262-019-01695-7