Skip to main content
Top
Published in: Virology Journal 1/2017

Open Access 01-12-2017 | Research

Transcriptional profiles in bursal B-lymphoid DT40 cells infected with very virulent infectious bursal disease virus

Authors: Rong Quan, Shanshan Zhu, Li Wei, Jing Wang, Xu Yan, Zixuan Li, Jue Liu

Published in: Virology Journal | Issue 1/2017

Login to get access

Abstract

Background

Infectious bursal disease virus (IBDV) causes a highly contagious, immunosuppressive disease in chickens. The virus mainly infects immature B lymphocytes in the bursa of Fabricius (BF). Chicken B cell line DT40, an avian leukosis virus-induced B cell line, supports very virulent IBDV (vvIBDV) infection in vitro and thereby serves as a good model for investigating the infection and pathogenesis of this virus. However, a transcriptome-wide understanding of the interaction between vvIBDV and B cells has not yet been achieved. This study aimed to employ time-course DNA microarrays to investigate gene expression patterns in DT40 cells after infection with vvIBDV strain LX.

Results

DT40 cells infected with vvIBDV exhibited alterations in the expression of many important host genes involved in signal transduction pathways, including MAPK signaling, PI3K/mTOR signaling, cell death and survival, BCR signaling, and antigen presentation. The changes in cellular mRNA levels identified by microarray analysis were confirmed for 8 selected genes using real-time reverse transcription-PCR. The upregulation of inflammatory cytokines and Toll-like receptors (TLRs) in the bursa of vvIBDV-infected chickens might involve excessive activation of the innate immune and inflammatory responses and contribute to tissue damage.

Conclusions

The present study is the first to provide a comprehensive differential transcriptional profile of cultured DT40 cells in response to vvIBDV infection and further extends our understanding of the molecular mechanisms underlying vvIBDV infection and pathogenesis.
Literature
1.
go back to reference Mundt E, Beyer J, Muller H. Identification of a novel viral protein in infectious bursal disease virus-infected cells. J Gen Virol. 1995;76:437–43.CrossRefPubMed Mundt E, Beyer J, Muller H. Identification of a novel viral protein in infectious bursal disease virus-infected cells. J Gen Virol. 1995;76:437–43.CrossRefPubMed
2.
go back to reference McFerran JB, McNulty MS, McKillop ER, Connor TJ, McCracken RM, Collins DS, et al. Isolation and serological studies with infectious bursal disease viruses from fowl, turkeys and ducks: demonstration of a second serotype. Avi Pathol. 1980;9:395–404.CrossRef McFerran JB, McNulty MS, McKillop ER, Connor TJ, McCracken RM, Collins DS, et al. Isolation and serological studies with infectious bursal disease viruses from fowl, turkeys and ducks: demonstration of a second serotype. Avi Pathol. 1980;9:395–404.CrossRef
3.
go back to reference Ismail NM, Saif YM, Moorhead PD. Lack of pathogenicity of five serotype 2 infectious bursal disease viruses in chickens. Avi Dis. 1988;32:757–9.CrossRef Ismail NM, Saif YM, Moorhead PD. Lack of pathogenicity of five serotype 2 infectious bursal disease viruses in chickens. Avi Dis. 1988;32:757–9.CrossRef
4.
go back to reference Becht H, Muller H. Infectious bursal disease--B cell dependent immunodeficiency syndrome in chickens. Behring Inst Mitt. 1991;89:217–25. Becht H, Muller H. Infectious bursal disease--B cell dependent immunodeficiency syndrome in chickens. Behring Inst Mitt. 1991;89:217–25.
5.
go back to reference Berg TP. Acute infectious bursal disease in poultry: a review. Avi Pathol. 2000;29:175–94.CrossRef Berg TP. Acute infectious bursal disease in poultry: a review. Avi Pathol. 2000;29:175–94.CrossRef
6.
go back to reference Lin TW, Lo CW, Lai SY, Fan RJ, Lo CJ, Chou YM, et al. Chicken heat shock protein 90 is a component of the putative cellular receptor complex of infectious bursal disease virus. J Virol. 2007;81:8730–41.CrossRefPubMedPubMedCentral Lin TW, Lo CW, Lai SY, Fan RJ, Lo CJ, Chou YM, et al. Chicken heat shock protein 90 is a component of the putative cellular receptor complex of infectious bursal disease virus. J Virol. 2007;81:8730–41.CrossRefPubMedPubMedCentral
7.
go back to reference Delgui L, Oña A, Gutiérrez S, Luque D, Navarro A, Castón JR, et al. The capsid protein of infectious bursal disease virus contains a functional alpha 4 beta 1 integrin ligand motif. Virology. 2009;386:360–72.CrossRefPubMed Delgui L, Oña A, Gutiérrez S, Luque D, Navarro A, Castón JR, et al. The capsid protein of infectious bursal disease virus contains a functional alpha 4 beta 1 integrin ligand motif. Virology. 2009;386:360–72.CrossRefPubMed
8.
go back to reference Delgui LR, Rodriguez JF, Colombo MI. The endosomal pathway and the Golgi complex are involved in the infectious bursal disease virus life cycle. J Virol. 2013;87:8993–9007.CrossRefPubMedPubMedCentral Delgui LR, Rodriguez JF, Colombo MI. The endosomal pathway and the Golgi complex are involved in the infectious bursal disease virus life cycle. J Virol. 2013;87:8993–9007.CrossRefPubMedPubMedCentral
9.
go back to reference Fernandez-Arias A, Martinez S, Rodriguez JF. The major antigenic protein of infectious bursal disease virus, VP2, is an apoptotic inducer. J Virol. 1997;71:8014–8.PubMedPubMedCentral Fernandez-Arias A, Martinez S, Rodriguez JF. The major antigenic protein of infectious bursal disease virus, VP2, is an apoptotic inducer. J Virol. 1997;71:8014–8.PubMedPubMedCentral
10.
go back to reference Yao K, Vakharia VN. Induction of apoptosis in vitro by the 17-kDa nonstructural protein of infectious bursal disease virus: possible role in viral pathogenesis. Virology. 2001;285:50–8.CrossRefPubMed Yao K, Vakharia VN. Induction of apoptosis in vitro by the 17-kDa nonstructural protein of infectious bursal disease virus: possible role in viral pathogenesis. Virology. 2001;285:50–8.CrossRefPubMed
11.
go back to reference Khatri M, Sharma JM. Infectious bursal disease virus infection induces macrophage activation via p38 MAPK and NF-kappaB pathways. Virus Res. 2006;118:70–7.CrossRefPubMed Khatri M, Sharma JM. Infectious bursal disease virus infection induces macrophage activation via p38 MAPK and NF-kappaB pathways. Virus Res. 2006;118:70–7.CrossRefPubMed
12.
go back to reference Wei L, Hou L, Zhu S, Wang J, Zhou J, Liu J. Infectious bursal disease virus activates the phosphatidylinositol 3-kinase (PI3K)/Akt signaling pathway by interaction of VP5 protein with the p85alpha subunit of PI3K. Virology. 2011;417:211–20.CrossRefPubMed Wei L, Hou L, Zhu S, Wang J, Zhou J, Liu J. Infectious bursal disease virus activates the phosphatidylinositol 3-kinase (PI3K)/Akt signaling pathway by interaction of VP5 protein with the p85alpha subunit of PI3K. Virology. 2011;417:211–20.CrossRefPubMed
13.
go back to reference Wei L, Zhu S, Ruan G, Hou L, Wang J, Wang B, et al. Infectious bursal disease virus-induced activation of JNK signaling pathway is required for virus replication and correlates with virus-induced apoptosis. Virology. 2011;420:156–63.CrossRefPubMed Wei L, Zhu S, Ruan G, Hou L, Wang J, Wang B, et al. Infectious bursal disease virus-induced activation of JNK signaling pathway is required for virus replication and correlates with virus-induced apoptosis. Virology. 2011;420:156–63.CrossRefPubMed
14.
go back to reference Li Z, Wang Y, Li X, Li X, Cao H, Zheng SJ. Critical roles of glucocorticoid-induced leucine zipper in infectious bursal disease virus (IBDV)-induced suppression of type I Interferon expression and enhancement of IBDV growth in host cells via interaction with VP4. J Virol. 2013;87:1221–31.CrossRefPubMedPubMedCentral Li Z, Wang Y, Li X, Li X, Cao H, Zheng SJ. Critical roles of glucocorticoid-induced leucine zipper in infectious bursal disease virus (IBDV)-induced suppression of type I Interferon expression and enhancement of IBDV growth in host cells via interaction with VP4. J Virol. 2013;87:1221–31.CrossRefPubMedPubMedCentral
15.
go back to reference Wu Y, Hong L, Ye J, Huang Z, Zhou J. The VP5 protein of infectious bursal disease virus promotes virion release from infected cells and is not involved in cell death. Arch Virol. 2009;154:1873–82.CrossRefPubMed Wu Y, Hong L, Ye J, Huang Z, Zhou J. The VP5 protein of infectious bursal disease virus promotes virion release from infected cells and is not involved in cell death. Arch Virol. 2009;154:1873–82.CrossRefPubMed
16.
go back to reference Yan Q. Bioinformatics databases and tools in virology research: an overview. In Silico Biol. 2008;8:71–85.PubMed Yan Q. Bioinformatics databases and tools in virology research: an overview. In Silico Biol. 2008;8:71–85.PubMed
17.
go back to reference Wong RT, Hon CC, Zeng F, Leung FC. Screening of differentially expressed transcripts in infectious bursal disease virus-induced apoptotic chicken embryonic fibroblasts by using cDNA microarrays. J Gen Virol. 2007;88:1785–96.CrossRefPubMed Wong RT, Hon CC, Zeng F, Leung FC. Screening of differentially expressed transcripts in infectious bursal disease virus-induced apoptotic chicken embryonic fibroblasts by using cDNA microarrays. J Gen Virol. 2007;88:1785–96.CrossRefPubMed
18.
go back to reference Hui RK, Leung FC. Differential expression profile of chicken embryo fibroblast DF-1 cells infected with cell-adapted infectious bursal disease virus. PLoS One. 2015;10(6):e0111771.CrossRefPubMedPubMedCentral Hui RK, Leung FC. Differential expression profile of chicken embryo fibroblast DF-1 cells infected with cell-adapted infectious bursal disease virus. PLoS One. 2015;10(6):e0111771.CrossRefPubMedPubMedCentral
19.
go back to reference Zheng X, Hong L, Shi L, Guo J, Sun Z, Zhou J. Proteomics analysis of host cells infected with infectious bursal disease virus. Mol Cell Proteomics. 2008;7(3):612–25.CrossRefPubMed Zheng X, Hong L, Shi L, Guo J, Sun Z, Zhou J. Proteomics analysis of host cells infected with infectious bursal disease virus. Mol Cell Proteomics. 2008;7(3):612–25.CrossRefPubMed
20.
go back to reference Wu Y, Peng C, Xu L, Zheng X, Liao M, Yan Y, et al. Proteome dynamics in primary target organ of infectious bursal disease virus. Proteomics. 2012;12:1844–59.CrossRefPubMed Wu Y, Peng C, Xu L, Zheng X, Liao M, Yan Y, et al. Proteome dynamics in primary target organ of infectious bursal disease virus. Proteomics. 2012;12:1844–59.CrossRefPubMed
21.
go back to reference Baba TW, Giroir BP, Humphries EH. Cell lines derived from avian lymphomas exhibit two distinct phenotypes. Virology. 1985;144:139–51.CrossRefPubMed Baba TW, Giroir BP, Humphries EH. Cell lines derived from avian lymphomas exhibit two distinct phenotypes. Virology. 1985;144:139–51.CrossRefPubMed
22.
go back to reference Delgui L, Gonzalez D, Rodriguez JF. Infectious bursal disease virus persistently infects bursal B-lymphoid DT40 cells. J Gen Virol. 2009;90:1148–52.CrossRefPubMed Delgui L, Gonzalez D, Rodriguez JF. Infectious bursal disease virus persistently infects bursal B-lymphoid DT40 cells. J Gen Virol. 2009;90:1148–52.CrossRefPubMed
23.
go back to reference Terasaki K, Hirayama H, Kasanga CJ, Maw MT, Ohya K, Yamaguchi T, et al. Chicken B lymphoma DT40 cells as a useful tool for in vitro analysis of pathogenic infectious bursal disease virus. J Vet Med Sci. 2008;70:407–10.CrossRefPubMed Terasaki K, Hirayama H, Kasanga CJ, Maw MT, Ohya K, Yamaguchi T, et al. Chicken B lymphoma DT40 cells as a useful tool for in vitro analysis of pathogenic infectious bursal disease virus. J Vet Med Sci. 2008;70:407–10.CrossRefPubMed
24.
go back to reference Zhang W, Liu HT. MAPK signal pathways in the regulation of cell proliferation in mammalian cells. Cell Res. 2002;12:9–18.CrossRefPubMed Zhang W, Liu HT. MAPK signal pathways in the regulation of cell proliferation in mammalian cells. Cell Res. 2002;12:9–18.CrossRefPubMed
25.
go back to reference Hynes NE, Ingham PW, Lim WA, Marshall CJ, Massague J, Pawson T. Signalling change: signal transduction through the decades. Nat Rev Mol Cell Biol. 2013;14:393–8.CrossRefPubMed Hynes NE, Ingham PW, Lim WA, Marshall CJ, Massague J, Pawson T. Signalling change: signal transduction through the decades. Nat Rev Mol Cell Biol. 2013;14:393–8.CrossRefPubMed
26.
go back to reference Hu B, Zhang Y, Jia L, Wu H, Fan C, Sun Y, et al. Binding of the pathogen receptor HSP90AA1 to avibirnavirus VP2 induces autophagy by inactivating the AKT-MTOR pathway. Autophagy. 2015;11:503–15.CrossRefPubMedPubMedCentral Hu B, Zhang Y, Jia L, Wu H, Fan C, Sun Y, et al. Binding of the pathogen receptor HSP90AA1 to avibirnavirus VP2 induces autophagy by inactivating the AKT-MTOR pathway. Autophagy. 2015;11:503–15.CrossRefPubMedPubMedCentral
28.
go back to reference Efeyan A, Zoncu R, Chang S, Gumper I, Snitkin H, Wolfson RL, et al. Regulation of mTORC1 by the Rag GTPases is necessary for neonatal autophagy and survival. Nature. 2013;493:679–83.CrossRefPubMed Efeyan A, Zoncu R, Chang S, Gumper I, Snitkin H, Wolfson RL, et al. Regulation of mTORC1 by the Rag GTPases is necessary for neonatal autophagy and survival. Nature. 2013;493:679–83.CrossRefPubMed
29.
go back to reference Kang R, Zeh HJ, Lotze MT, Tang D. The Beclin 1 network regulates autophagy and apoptosis. Cell Death Diff. 2011;18:571–80.CrossRef Kang R, Zeh HJ, Lotze MT, Tang D. The Beclin 1 network regulates autophagy and apoptosis. Cell Death Diff. 2011;18:571–80.CrossRef
31.
go back to reference Rodriguez-Lecompte JC, Nino-Fong R, Lopez A, Frederick Markham RJ, Kibenge FS. Infectious bursal disease virus (IBDV) induces apoptosis in chicken B cells. Comp Immunol Microbiol Infect Dis. 2005;28:321–37.CrossRefPubMed Rodriguez-Lecompte JC, Nino-Fong R, Lopez A, Frederick Markham RJ, Kibenge FS. Infectious bursal disease virus (IBDV) induces apoptosis in chicken B cells. Comp Immunol Microbiol Infect Dis. 2005;28:321–37.CrossRefPubMed
32.
go back to reference Tham KM, Moon CD. Apoptosis in cell cultures induced by infectious bursal disease virus following in vitro infection. Avi Dis. 1996;40:109–13.CrossRef Tham KM, Moon CD. Apoptosis in cell cultures induced by infectious bursal disease virus following in vitro infection. Avi Dis. 1996;40:109–13.CrossRef
34.
go back to reference Wang L, Kurosaki T, Corey SJ. Engagement of the B-cell antigen receptor activates STAT through Lyn in a Jak-independent pathway. Oncogene. 2007;26:2851–9.CrossRefPubMed Wang L, Kurosaki T, Corey SJ. Engagement of the B-cell antigen receptor activates STAT through Lyn in a Jak-independent pathway. Oncogene. 2007;26:2851–9.CrossRefPubMed
35.
go back to reference Saeki K, Miura Y, Aki D, Kurosaki T, Yoshimura A. The B cell-specific major raft protein, Raftlin, is necessary for the integrity of lipid raft and BCR signal transduction. EMBO J. 2003;22:3015–26.CrossRefPubMedPubMedCentral Saeki K, Miura Y, Aki D, Kurosaki T, Yoshimura A. The B cell-specific major raft protein, Raftlin, is necessary for the integrity of lipid raft and BCR signal transduction. EMBO J. 2003;22:3015–26.CrossRefPubMedPubMedCentral
36.
go back to reference Alinikula J, Nera KP, Junttila S, Lassila O. Alternate pathways for Bcl6-mediated regulation of B cell to plasma cell differentiation. Eur J Iimmunol. 2011;41:2404–13.CrossRef Alinikula J, Nera KP, Junttila S, Lassila O. Alternate pathways for Bcl6-mediated regulation of B cell to plasma cell differentiation. Eur J Iimmunol. 2011;41:2404–13.CrossRef
37.
go back to reference Philbin VJ, Iqbal M, Boyd Y, Goodchild MJ, Beal RK, Bumstead N, et al. Identification and characterization of a functional, alternatively spliced Toll-like receptor 7 (TLR7) and genomic disruption of TLR8 in chickens. Immunol. 2005;114:507–21.CrossRef Philbin VJ, Iqbal M, Boyd Y, Goodchild MJ, Beal RK, Bumstead N, et al. Identification and characterization of a functional, alternatively spliced Toll-like receptor 7 (TLR7) and genomic disruption of TLR8 in chickens. Immunol. 2005;114:507–21.CrossRef
38.
go back to reference Iqbal M, Philbin VJ, Smith AL. Expression patterns of chicken Toll-like receptor mRNA in tissues, immune cell subsets and cell lines. Vet Immunol Immunopathol. 2005;104:117–27.CrossRefPubMed Iqbal M, Philbin VJ, Smith AL. Expression patterns of chicken Toll-like receptor mRNA in tissues, immune cell subsets and cell lines. Vet Immunol Immunopathol. 2005;104:117–27.CrossRefPubMed
39.
go back to reference Gobel TW, Schneider K, Schaerer B, Mejri I, Puehler F, Weigend S, et al. IL-18 stimulates the proliferation and IFN-gamma release of CD4+ T cells in the chicken: conservation of a Th1-like system in a nonmammalian species. J Immunol. 2003;171:1809–15.CrossRefPubMed Gobel TW, Schneider K, Schaerer B, Mejri I, Puehler F, Weigend S, et al. IL-18 stimulates the proliferation and IFN-gamma release of CD4+ T cells in the chicken: conservation of a Th1-like system in a nonmammalian species. J Immunol. 2003;171:1809–15.CrossRefPubMed
40.
go back to reference Boyd AC, Peroval MY, Hammond JA, Prickett MD, Young JR, Smith AL. TLR15 is unique to avian and reptilian lineages and recognizes a yeast-derived agonist. J Immunol. 2012;189:4930–8.CrossRefPubMed Boyd AC, Peroval MY, Hammond JA, Prickett MD, Young JR, Smith AL. TLR15 is unique to avian and reptilian lineages and recognizes a yeast-derived agonist. J Immunol. 2012;189:4930–8.CrossRefPubMed
41.
go back to reference Rauf A, Khatri M, Murgia MV, Jung K, Saif YM. Differential modulation of cytokine, chemokine and Toll like receptor expression in chickens infected with classical and variant infectious bursal disease virus. Vet Res. 2011;42:85.CrossRefPubMedPubMedCentral Rauf A, Khatri M, Murgia MV, Jung K, Saif YM. Differential modulation of cytokine, chemokine and Toll like receptor expression in chickens infected with classical and variant infectious bursal disease virus. Vet Res. 2011;42:85.CrossRefPubMedPubMedCentral
42.
go back to reference Guo X, Wang L, Cui D, Ruan W, Liu F, Li H. Differential expression of the Toll-like receptor pathway and related genes of chicken bursa after experimental infection with infectious bursa disease virus. Arch Virol. 2012;157:2189–99.CrossRefPubMed Guo X, Wang L, Cui D, Ruan W, Liu F, Li H. Differential expression of the Toll-like receptor pathway and related genes of chicken bursa after experimental infection with infectious bursa disease virus. Arch Virol. 2012;157:2189–99.CrossRefPubMed
43.
go back to reference Wong JP, Christopher ME, Viswanathan S, Karpoff N, Dai X, Das D, et al. Activation of toll-like receptor signaling pathway for protection against influenza virus infection. Vaccine. 2009;27:3481–3.CrossRefPubMed Wong JP, Christopher ME, Viswanathan S, Karpoff N, Dai X, Das D, et al. Activation of toll-like receptor signaling pathway for protection against influenza virus infection. Vaccine. 2009;27:3481–3.CrossRefPubMed
44.
go back to reference Khatri M, Palmquist JM, Cha RM, Sharma JM. Infection and activation of bursal macrophages by virulent infectious bursal disease virus. Virus Res. 2005;113:44–50.CrossRefPubMed Khatri M, Palmquist JM, Cha RM, Sharma JM. Infection and activation of bursal macrophages by virulent infectious bursal disease virus. Virus Res. 2005;113:44–50.CrossRefPubMed
45.
go back to reference Palmquist JM, Khatri M, Cha RM, Goddeeris BM, Walcheck B, Sharma JM. In vivo activation of chicken macrophages by infectious bursal disease virus. Viral Immunol. 2006;19:305–15.CrossRefPubMed Palmquist JM, Khatri M, Cha RM, Goddeeris BM, Walcheck B, Sharma JM. In vivo activation of chicken macrophages by infectious bursal disease virus. Viral Immunol. 2006;19:305–15.CrossRefPubMed
46.
go back to reference Barker KA, Hampe A, Stoeckle MY, Hanafusa H. Transformation-associated cytokine 9E3/CEF4 is chemotactic for chicken peripheral blood mononuclear cells. J Virol. 1993;67:3528–33.PubMedPubMedCentral Barker KA, Hampe A, Stoeckle MY, Hanafusa H. Transformation-associated cytokine 9E3/CEF4 is chemotactic for chicken peripheral blood mononuclear cells. J Virol. 1993;67:3528–33.PubMedPubMedCentral
47.
go back to reference Liu J, Liu SG, Zhou J. Isolation and identification of very virulent infectious bursal disease virus strain LX in chickens. Chinese J Vet Med. 2000;26(5):17–9. Liu J, Liu SG, Zhou J. Isolation and identification of very virulent infectious bursal disease virus strain LX in chickens. Chinese J Vet Med. 2000;26(5):17–9.
Metadata
Title
Transcriptional profiles in bursal B-lymphoid DT40 cells infected with very virulent infectious bursal disease virus
Authors
Rong Quan
Shanshan Zhu
Li Wei
Jing Wang
Xu Yan
Zixuan Li
Jue Liu
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2017
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/s12985-016-0668-2

Other articles of this Issue 1/2017

Virology Journal 1/2017 Go to the issue