Abstract
Avian leukemia subgroup J (ALV-J) is one of the most detrimental neoplastic diseases in poultry production. However, the differences between somatic cells and immune cells post-infection remain poorly understood. The aim of our study was to detect the different responses in chicken to infection with ALV-J in different cell lines. In this study, we detected transcriptome expression changes during infection with ALV-J in chicken embryo fibroblast (CEF) and HD11 cell lines. RNA-Seq was used to determine the expression levels of mRNA transcripts from the two cell types after infection with ALV-J at 1, 4, and 7 dpi, and gene ontology analyses were used to cluster differentially expressed genes into pathways. Quantitative real-time PCR confirmed the expression of 336 and 269 differentially expressed genes in CEF and HD11 lines, respectively, involved in innate immunity (OASL, CCL4), adaptive immunity (LYZ, CD72), apoptosis and autophagy (WISP2, COMP), inflammation (JSC, IL8), and tumorgenesis (PCNA, GPX3). The notable signal transduction pathways included the PPARs signaling pathway and ECM-receptor interactions in CEF, and the Toll-like receptor, NOD-like receptor, and RIG-I-like receptor signaling pathways in HD11. To our knowledge, this is the first study to use high-throughput sequencing methods to investigate viral infection in different cell types. The results of the present study form a foundation for developing potential biological markers for viral infection.
Similar content being viewed by others
References
Banerjee S, Dhar G, Haque I, Kambhampati S, Mehta S, Sengupta K et al (2008) CCN5/WISP-2 expression in breast adenocarcinoma is associated with less frequent progression of the disease and suppresses the invasive phenotypes of tumor cells. Cancer Res 68(18):7606–7612
Bergers G, Song S (2005) The role of pericytes in blood-vessel formation and maintenance. Neuro-Oncology 7(4):452
Beug H, von Kirchbach A, Döderlein G, Conscience J-F, Graf T (1979) Chicken hematopoietic cells transformed by seven strains of defective avian leukemia viruses display three distinct phenotypes of differentiation. Cell 18(2):375–390
Borodina T, Adjaye J, Sultan M (2011) A strand-specific library preparation protocol for RNA sequencing. In: Daniel Jameson MV, Hans VW (eds) Methods in enzymology. Volume 500. Academic, Waltham, pp 79–98
Bosinger SE, Hosiawa KA, Cameron MJ, Persad D, Ran L, Xu L et al (2004) Gene expression profiling of host response in models of acute HIV infection. J Immunol 173(11):6858–6863
Brogden KA (2005) Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat Rev Microbiol 3:238–250
Brune K, Leffell MS, Spitznagel JK (1972) Microbicidal activity of peroxidaseless chicken heterophile leukocytes. Infect Immun 5(3):283–287
Brunet A, Datta SR, Greenberg ME (2001) Transcription-dependent and -independent control of neuronal survival by the PI3K-Akt signaling pathway. Curr Opin Neurobiol 11(3):297–305
Burnside J, Ouyang M, Anderson A, Bernberg E (2008) Deep sequencing of chicken microRNAs. BMC Genomics 9:185
Bystry RS, Aluvihare V, Welch KA, Kallikourdis M, Betz AG (2001) B cells and professional APCs recruit regulatory T cells via CCL4. Nat Immunol 2(12):1126–1132
Carmeliet P, Jain RK (2000) Angiogenesis in cancer and other diseases. Nature 407(6801):249–257
Cui Z, Sun S, Zhang Z, Meng S (2009) Simultaneous endemic infections with subgroup J avian leukosis virus and reticuloendotheliosis virus in commercial and local breeds of chickens. Avian Pathol 38:443–448
Daynes RA, Jones DC (2002) Emerging roles of PPARs in inflammation and immunity. Nat Rev Immunol 2:748–759
Diebold S (2010) Innate recognition of viruses. Immunol Lett 128:17–20
El-kott AF, El-baz MA, Mokhtar AA (2006) Proliferating cell nuclear antigen (PCNA) overexpression and microvessel density predict survival in the urinary bladder carcinoma. Int Urol Nephrol 38:237–242
Fadly AM, Smith EJ (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:391–400
Feng S-Z, Cao W-S, Liao M (2011) The PI3K/Akt pathway is involved in early infection of some exogenous avian leukosis viruses. J Gen Virol 92(Pt 7):1688–1697
Ferrara N, Kerbel RS (2005) Angiogenesis as a therapeutic target. Nature 438(7070):967–974
Folkman J (1995) Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med 1(1):27–30
Fritz JH, Ferrero RL, Philpott DJ, Girardin SE (2006) Nod-like proteins in immunity, inflammation and disease. Nat Immunol 7(12):1250–1257
Hang B, Sang J, Qin A, Qian K, Shao H, Mei M et al (2014) Transcription analysis of the response of chicken bursa of Fabricius to avian leukosis virus subgroup J strain JS09GY3. Virus Res 188:8–14
Hansson GK, Libby P, Schönbeck U, Yan ZQ (2002) Innate and adaptive immunity in the pathogenesis of atherosclerosis. Circ Res 91:281–291
Hattori K, Uchida K, Akaza H, Koiso K (1995) Proliferating cell nuclear antigen cyclin in human transitional cell carcinoma. Br J Urol 75:162–166
Heide V (1998) Update on subgroup J of avian leukosis. World Poult 14:2
Hussain AI, Johnson JA, da Silva FM, Heneine W (2003) Identification and characterization of avian retroviruses in chicken embryo-derived yellow fever vaccines: investigation of transmission to vaccine recipients. J Virol 77(2):1105–1111
Kano A, Haruyama T, Akaike T, Watanabe Y (1999) IRF-1 is an essential mediator in IFN-γ-induced cell cycle arrest and apoptosis of primary cultured hepatocytes. Biochem Biophys Res Commun 257:672–677
Lai Y, Gallo RL (2009) AMPed up immunity: how antimicrobial peptides have multiple roles in immune defense. Trends Immunol 30:131–141
Li B, Ruotti V, Stewart RM, Thomson JA, Dewey CN (2010) RNA-Seq gene expression estimation with read mapping uncertainty. Bioinformatics 26(4):493–500
Li H, Ji J, Xie Q, Shang H, Zhang H, Xin X et al (2012) Aberrant expression of liver microRNA in chickens infected with subgroup J avian leukosis virus. Virus Res 169(1):268–271
Li H, Wang T, Xu C, Wang D, Ren J, Li Y et al (2015) Transcriptome profile of liver at different physiological stages reveals potential mode for lipid metabolism in laying hens. BMC Genomics 16(1):763
Liu H, Cao W, Li Y, Feng M, Wu X, Yu K et al (2013) Subgroup J avian leukosis virus infection inhibits autophagy in DF-1 cells. Virol J 10:196
Liu H, Ong S-E, Badu-Nkansah K, Schindler J, White FM, Hynes RO (2011) CUB-domain-containing protein 1 (CDCP1) activates Src to promote melanoma metastasis. Proc Natl Acad Sci 108(4):1379–1384
Liu H-C, Niikura M, Fulton J, Cheng H (2004) Identification of chicken lymphocyte antigen 6 complex, locus E (LY6E, alias SCA2) as a putative Marek’s disease resistance gene via a virus-host protein interaction screen. Cytogenet Genome Res 102(1–4):304–308
Loo YM, Gale M (2011) Immune signaling by RIG-I-like receptors. Immunity 34:680–692
Medzhitov R, Janeway CA (1997) Innate immunity: the virtues of a nonclonal system of recognition. Cell 91:295–298
Metzker ML (2010) Sequencing technologies [mdash] the next generation. Nat Rev Genet 11(1):31–46
Moon RT, Bowerman B, Boutros M, Perrimon N (2002) The promise and perils of Wnt signaling through β-catenin. Science 296(5573):1644–1646
Moresco EMY, LaVine D, Beutler B (2011) Toll-like receptors. Curr Biol 21(13):R488–RR93
Patan S (2004) Vasculogenesis and angiogenesis. Angiogenesis in brain tumors. Springer, New York, pp 3–32
Payne LN (1998) HPRS 103: a retro virus strikes back. The emergence of subgroup J avian leukosis virus. Avian Pathol 27(S1):S36–S45
Payne LN, Nair V (2012) The long view: 40 years of avian leukosis research. Avian Pathol 41(1):11–19
Qin L, Gao Y, Ni W, Sun M, Wang Y, Yin C et al (2013) Development and application of real-time PCR for detection of subgroup J avian leukosis virus. J Clin Microbiol 51(1):149–154
Rosenfeld N, Young JW, Alon U, Swain PS, Elowitz MB (2005) Gene regulation at the single-cell level. Science 307(5717):1962–1965
Roukos DH (2010) Next-generation, genome sequencing-based biomarkers: concerns and challenges for medical practice. Biomark Med 4(4):583–586
Rubin H, Fanshier L, Cornelius A, Hughes WF (1962) Tolerance and immunity in chickens after congenital and contact infection with an avian leukosis virus. Virology 17(1):143–156
Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3(6):1101–1108
Schwarting R, Castello R (1992) Human Lyb-2 homolog CD72 is a marker for progenitor B-cell leukemias. Am J Hematol 41:151–158
Sugiarto H, Yu PL (2004) Avian antimicrobial peptides: the defense role of β-defensins. Biochem Biophys Res Commun 323:721–727
The Gene Ontology Consortium (2004) The gene ontology (GO) database and informatics resource. Nucleic Acids Res 32(suppl 1):D258–D261
Thomas PD, Mi H, Lewis S (2007) Ontology annotation: mapping genomic regions to biological function. Curr Opin Chem Biol 11(1):4–11
Tisoncik JR, Korth MJ, Simmons CP, Farrar J, Martin TR, Katze MG (2012) Into the eye of the cytokine storm. Microbiol Mol Biol Rev 76(1):16–32
Trapnell C, Pachter L, Salzberg SL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics (Oxford, England) 25(9):1105–1111
Funding
This study was supported financially by the National Natural Science Foundation of China (31301966) and Science & Technology Pillar Program of Jiangsu (BE2013392).
Author information
Authors and Affiliations
Corresponding author
Additional information
Editor: Tetsuji Okamoto
Rights and permissions
About this article
Cite this article
Chen, G., Li, Z., Su, S. et al. Identification of key genes fluctuated induced by avian leukemia virus (ALV-J) infection in chicken cells. In Vitro Cell.Dev.Biol.-Animal 54, 41–51 (2018). https://doi.org/10.1007/s11626-017-0198-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11626-017-0198-2