Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.
ADVANCED SEARCH
Log in
Top
Archives of Virology
Published in: Archives of Virology 11/2012

01-11-2012 | Original Article

Differential expression of the Toll-like receptor pathway and related genes of chicken bursa after experimental infection with infectious bursa disease virus

Authors: Xinfeng Guo, Liqiong Wang, Defeng Cui, Wenke Ruan, Fenghua Liu, Huanrong Li

Published in: Archives of Virology | Issue 11/2012

Login to get access

Abstract

Infectious bursa disease virus causes an acute infection in bursal B cells. The Toll-like receptor (TLR) signaling pathway plays a key role in innate immunity during virus infection. In this study, an Agilent microarray was used to investigate different transcriptional profiles of the TLR pathway and related genes of chicken bursa at 48 h after infection with IBDV, compared with simulated infection. Expression of >58 genes changed significantly. Forty-six genes associated with chicken bursa proinflammatory effects, chemotactic effects, and T-cell stimulation were upregulated, which meant enhancement of these features. Twelve genes that are related to proliferation and differentiation of bursal cells were downregulated, implying suppression of these features. These results revealed that genes of the TLR pathway play an important role in the pathogenicity of IBDV infection. The findings are helpful for understanding the molecular basis of viral pathogenesis and the underlying mechanism of the host antiviral response.
Literature
1.
Abell AN, Johnson GL (2005) MEKK4 is an effector of the embryonic TRAF4 for JNK activation. J Biol Chem 280:35793–35796PubMedCrossRef
2.
Allan WH, Faragher JT, Cullen GA (1972) Immunosuppression by the infectious bursal agent in chickens immunised against Newcastle disease. Vet Rec 90:511–512PubMedCrossRef
3.
Arvaniti E, Ntoufa S, Papakonstantinou N, Touloumenidou T, Laoutaris N, Anagnostopoulos A, Lamnissou K, Caligaris-Cappio F, Stamatopoulos K, Ghia P, Muzio M, Belessi C (2011) Toll-like receptor signaling pathway in chronic lymphocytic leukemia: distinct gene expression profiles of potential pathogenetic significance in specific subsets of patients. Haematologica 96:1644–1652
4.
Asagiri M, Hirai T, Kunigami T, Kamano S, Gober HJ, Okamoto K, Nishikawa K, Latz E, Golenbock DT, Aoki K, Ohya K, Imai Y, Morishita Y, Miyazono K, Kato S, Saftig P, Takayanagi H (2008) Cathepsin K-dependent toll-like receptor 9 signaling revealed in experimental arthritis. Science 319:624–627PubMedCrossRef
5.
Basiewicz-Worsztynowicz BM, Karnas-Kalemba WZ (2004) Chemokine RANTES activity and its potential role as a target for diagnosis and therapy. Wiad Lek 57:653–658PubMed
6.
Bhattacharyya S, Zhao Y, Kay TW, Muglia LJ (2011) Glucocorticoids target suppressor of cytokine signaling 1 (SOCS1) and type 1 interferons to regulate Toll-like receptor-induced STAT1 activation. Proc Natl Acad Sci USA 108:9554–9559PubMedCrossRef
7.
Bonvin C, Guillon A, van Bemmelen MX, Gerwins P, Johnson GL, Widmann C (2002) Role of the amino-terminal domains of MEKKs in the activation of NF kappa B and MAPK pathways and in the regulation of cell proliferation and apoptosis. Cell Signal 14:123–131PubMedCrossRef
8.
Bosinger SE, Hosiawa KA, Cameron MJ, Persad D, Ran L, Xu L, Boulassel MR, Parenteau M, Fournier J, Rud EW, Kelvin DJ (2004) Gene expression profiling of host response in models of acute HIV infection. J Immunol 173:6858–6863PubMed
9.
Bradley JR, Pober JS (2001) Tumor necrosis factor receptor-associated factors (TRAFs). Oncogene 20:6482–6491PubMedCrossRef
10.
11.
Cao Z, Xiong J, Takeuchi M, Kurama T, Goeddel DV (1996) TRAF6 is a signal transducer for interleukin-1. Nature 383:443–446PubMedCrossRef
12.
Cho YJ, Lee YA, Lee JW, Kim JI, Han JS (2011) Kinetics of proinflammatory cytokines after intraperitoneal injection of tribromoethanol and a tribromoethanol/xylazine combination in ICR mice. Lab Anim Res 27:197–203PubMedCrossRef
13.
Cormican P, Lloyd AT, Downing T, Connell SJ, Bradley D, O’Farrelly C (2009) The avian Toll-Like receptor pathway–subtle differences amidst general conformity. Dev Comp Immunol 33:967–973PubMedCrossRef
14.
de Zoete MR, Bouwman LI, Keestra AM, van Putten JP (2011) Cleavage and activation of a Toll-like receptor by microbial proteases. Proc Natl Acad Sci USA 108:4968–4973PubMedCrossRef
15.
Dhamija S, Doerrie A, Winzen R, Dittrich-Breiholz O, Taghipour A, Kuehne N, Kracht M, Holtmann H (2010) IL-1-induced post-transcriptional mechanisms target overlapping translational silencing and destabilizing elements in IkappaBzeta mRNA. J Biol Chem 285:29165–29178PubMedCrossRef
16.
Dinarello CA (2011) Interleukin-1 in the pathogenesis and treatment of inflammatory diseases. Blood 117:3720–3732PubMedCrossRef
17.
Doyle S, Vaidya S, O’Connell R, Dadgostar H, Dempsey P, Wu T, Rao G, Sun R, Haberland M, Modlin R, Cheng G (2002) IRF3 mediates a TLR3/TLR4-specific antiviral gene program. Immunity 17:251–263PubMedCrossRef
18.
Ekerot M, Stavridis MP, Delavaine L, Mitchell MP, Staples C, Owens DM, Keenan ID, Dickinson RJ, Storey KG, Keyse SM (2008) Negative-feedback regulation of FGF signalling by DUSP6/MKP-3 is driven by ERK1/2 and mediated by Ets factor binding to a conserved site within the DUSP6/MKP-3 gene promoter. Biochem J 412:287–298PubMedCrossRef
19.
Eldaghayes I, Rothwell L, Williams A, Withers D, Balu S, Davison F, Kaiser P (2006) Infectious bursal disease virus: strains that differ in virulence differentially modulate the innate immune response to infection in the chicken bursa. Viral Immunol 19:83–91PubMedCrossRef
20.
Fernandez-Fernandez L, Bellido-Martin L, Garcia de Frutos P (2008) Growth arrest-specific gene 6 (GAS6). An outline of its role in haemostasis and inflammation. Thromb Haemost 100:604–610PubMed
21.
Gelb J, Eidson CS, Fletcher OJ, Kleven SH (1979) Studies on interferon induction by infectious bursal disease virus (IBDV). II. Interferon production in White Leghorn chickens infected with an attenuated or pathogenic isolant of IBDV. Avian Dis 23:634–645PubMedCrossRef
22.
Giambrone JJ, Ewert DL, Eidson CS (1977) Effect of infectious bursal disease virus on the immunological responsiveness of the chicken. Poult Sci 56:1591–1594PubMedCrossRef
23.
Gong L, Wang YZ, Cai JP, Tan ZH, Yu JS (2009) The dynamic change of TLR7 in spleen of chicken infected with attenuated IBD vaccine. Heilong Jiang Animal Sci Veterinary Med 3:72–73
24.
Harada H, Takahashi E, Itoh S, Harada K, Hori TA, Taniguchi T (1994) Structure and regulation of the human interferon regulatory factor 1 (IRF-1) and IRF-2 genes: implications for a gene network in the interferon system. Mol Cell Biol 14:1500–1509PubMed
25.
Heidari M, Sarson AJ, Huebner M, Sharif S, Kireev D, Zhou H (2010) Marek’s disease virus-induced immunosuppression: array analysis of chicken immune response gene expression profiling. Viral Immunol 23:309–319PubMedCrossRef
26.
Ivanyi J, Morris R (1976) Immunodeficiency in the chicken. IV: an immunological study of infectious bursal disease. Clin Exp Immunol 23:154–165PubMed
27.
Karpala AJ, Lowenthal JW, Bean AG (2008) Activation of the TLR3 pathway regulates IFNβ production in chickens. Dev Comp Immunol 32:435–444PubMedCrossRef
28.
Kaufer I, Weiss E (1980) Significance of bursa of Fabricius as target organ in infectious bursal disease of chickens. Infect Immun 27:364–367PubMed
29.
Kawabe T, Matsushima M, Hashimoto N, Imaizumi K, Hasegawa Y (2011) CD40/CD40 ligand interactions in immune responses and pulmonary immunity. Nagoya J Med Sci 73:69–78PubMed
30.
Kawai T, Akira S (2011) Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 34:637–650PubMedCrossRef
31.
Kelly PA, Ali S, Rozakis M, Goujon L, Nagano M, Pellegrini I, Gould D, Djiane J, Edery M, Finidori J et al (1993) The growth hormone/prolactin receptor family. Recent Prog Horm Res 48:123–164PubMed
32.
Khatri M, Palmquist JM, Cha RM, Sharma JM (2005) Infection and activation of bursal macrophages by virulent infectious bursal disease virus. Virus Res 113:44–50PubMedCrossRef
33.
Kim IJ, Karaca K, Pertile TL, Erickson SA, Sharma JM (1998) Enhanced expression of cytokine genes in spleen macrophages during acute infection with infectious bursal disease virus in chickens. Vet Immunol Immunopathol 61:331–341PubMedCrossRef
34.
Kim IJ, You SK, Kim H, Yeh HY, Sharma JM (2000) Characteristics of bursal T lymphocytes induced by infectious bursal disease virus. J Virol 74:8884–8892PubMedCrossRef
35.
Le Bon A, Tough DF (2002) Links between innate and adaptive immunity via type I interferon. Curr Opin Immunol 14:432–436PubMedCrossRef
36.
Li YP, Bang DD, Handberg KJ, Jorgensen PH, Zhang MF (2005) Evaluation of the suitability of six host genes as internal control in real-time RT-PCR assays in chicken embryo cell cultures infected with infectious bursal disease virus. Vet Microbiol 110:155–165PubMedCrossRef
37.
Li YP, Handberg KJ, Juul-Madsen HR, Zhang MF, Jorgensen PH (2007) Transcriptional profiles of chicken embryo cell cultures following infection with infectious bursal disease virus. Arch Virol 152:463–478PubMedCrossRef
38.
Lin Q, Li M, Fang D, Fang J, Su SB (2011) The essential roles of Toll-like receptor signaling pathways in sterile inflammatory diseases. Int Immunopharmacol 11(10):1422–1432PubMedCrossRef
39.
Liu H, Zhang M, Han H, Yuan J, Li Z (2010) Comparison of the expression of cytokine genes in the bursal tissues of the chickens following challenge with infectious bursal disease viruses of varying virulence. Virol J 7:364PubMedCrossRef
40.
Liu M, Vakharia VN (2006) Nonstructural protein of infectious bursal disease virus inhibits apoptosis at the early stage of virus infection. J Virol 80:3369–3377PubMedCrossRef
41.
Lohoff M, Mak TW (2005) Roles of interferon-regulatory factors in T-helper-cell differentiation. Nat Rev Immunol 5:125–135PubMedCrossRef
42.
Lopez-Mejias R, Garcia-Bermudez M, Gonzalez-Juanatey C, Castaneda S, Miranda-Filloy JA, Gomez-Vaquero C, Fernandez-Gutierrez B, Balsa A, Pascual-Salcedo D, Blanco R, Gonzalez-Alvaro I, Llorca J, Martin J, Gonzalez-Gay MA (2011) Lack of association of IL6R rs2228145 and IL6ST/gp130 rs2228044 gene polymorphisms with cardiovascular disease in patients with rheumatoid arthritis. Tissue Antigens 78:438–441PubMedCrossRef
43.
Lu J, Lian G, Lenkinski R, De Grand A, Vaid RR, Bryce T, Stasenko M, Boskey A, Walsh C, Sheen V (2007) Filamin B mutations cause chondrocyte defects in skeletal development. Hum Mol Genet 16:1661–1675PubMedCrossRef
44.
Machida K, Cheng KT, Sung VM, Levine AM, Foung S, Lai MM (2006) Hepatitis C virus induces toll-like receptor 4 expression, leading to enhanced production of beta interferon and interleukin-6. J Virol 80:866–874PubMedCrossRef
45.
Manna SK, Babajan B, Raghavendra PB, Raviprakash N, Sureshkumar C (2010) Inhibiting TRAF2-mediated activation of NF-kappaB facilitates induction of AP-1. J Biol Chem 285:11617–11627PubMedCrossRef
46.
Mansell A, Smith R, Doyle SL, Gray P, Fenner JE, Crack PJ, Nicholson SE, Hilton DJ, O’Neill LA, Hertzog PJ (2006) Suppressor of cytokine signaling 1 negatively regulates Toll-like receptor signaling by mediating Mal degradation. Nat Immunol 7:148–155PubMedCrossRef
47.
McFerran JB, McNulty MS, McKillop ER, Connor TJ, McCracken RM, Collins DS, Allan GM (1980) Isolation and serological studies with infectious bursal disease viruses from fowl, turkeys and ducks: demonstration of a second serotype. Avian Pathol 9:395–404PubMedCrossRef
48.
Montero Vega MT, de Andres MartinA (2008) Toll-like receptors: a family of innate sensors of danger that alert and drive immunity. Allergol Immunopathol (Madr) 36:347–357CrossRef
49.
Moynagh PN (2005) TLR signalling and activation of IRFs: revisiting old friends from the NF-kappaB pathway. Trends Immunol 26:469–476PubMedCrossRef
50.
Nakano H, Oshima H, Chung W, Williams-Abbott L, Ware CF, Yagita H, Okumura K (1996) TRAF5, an activator of NF-kappaB and putative signal transducer for the lymphotoxin-beta receptor. J Biol Chem 271:14661–14664PubMedCrossRef
51.
Nehyba J, Hrdlickova R, Burnside J, Bose HR Jr (2002) A novel interferon regulatory factor (IRF), IRF-10, has a unique role in immune defense and is induced by the v-Rel oncoprotein. Mol Cell Biol 22:3942–3957PubMedCrossRef
52.
Nikolov N, Liutskanov D (1977) Pathomorphology of infectious bursitis in chicks. Vet Med Nauki 14:61–67PubMed
53.
Palladino MA, Johnson TA, Gupta R, Chapman JL, Ojha P (2007) Members of the Toll-like receptor family of innate immunity pattern-recognition receptors are abundant in the male rat reproductive tract. Biol Reprod 76:958–964PubMedCrossRef
54.
Parcellier A, Schmitt E, Gurbuxani S, Seigneurin-Berny D, Pance A, Chantome A, Plenchette S, Khochbin S, Solary E, Garrido C (2003) HSP27 is a ubiquitin-binding protein involved in I-kappaBalpha proteasomal degradation. Mol Cell Biol 23:5790–5802PubMedCrossRef
55.
Poltorak A, He X, Smirnova I, Liu MY, Van Huffel C, Du X, Birdwell D, Alejos E, Silva M, Galanos C, Freudenberg M, Ricciardi-Castagnoli P, Layton B, Beutler B (1998) Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282:2085–2088PubMedCrossRef
56.
Poonia B, Charan S (2004) Infiltration by CD4 + and CD8 + lymphocytes in bursa of chickens infected with Infectious Bursal Disease Virus (IBDV): strain-specific differences. Indian J Exp Biol 42:823–829PubMed
57.
Pothlichet J, Chignard M, Si-Tahar M (2008) Cutting edge: innate immune response triggered by influenza A virus is negatively regulated by SOCS1 and SOCS3 through a RIG-I/IFNAR1-dependent pathway. J Immunol 180:2034–2038PubMed
58.
Rassa JC, Meyers JL, Zhang Y, Kudaravalli R, Ross SR (2002) Murine retroviruses activate B cells via interaction with toll-like receptor 4. Proc Natl Acad Sci USA 99:2281–2286PubMedCrossRef
59.
Rauf A, Khatri M, Murgia MV, Jung K, Saif YM (2011) Differential modulation of cytokine, chemokine and Toll like receptor expression in chickens infected with classical and variant infectious bursal disease virus. Vet Res 42:85PubMedCrossRef
60.
Rauf A, Khatri M, Murgia MV, Saif YM (2011) Expression of perforin-granzyme pathway genes in the bursa of infectious bursal disease virus-infected chickens. Dev Comp Immunol 35:620–627PubMedCrossRef
61.
Rautenschlein S, Yeh HY, Njenga MK, Sharma JM (2002) Role of intrabursal T cells in infectious bursal disease virus (IBDV) infection: T cells promote viral clearance but delay follicular recovery. Arch Virol 147:285–304PubMedCrossRef
62.
Rothe M, Sarma V, Dixit VM, Goeddel DV (1995) TRAF2-mediated activation of NF-kappa B by TNF receptor 2 and CD40. Science 269:1424–1427PubMedCrossRef
63.
Sato M, Suemori H, Hata N, Asagiri M, Ogasawara K, Nakao K, Nakaya T, Katsuki M, Noguchi S, Tanaka N, Taniguchi T (2000) Distinct and essential roles of transcription factors IRF-3 and IRF-7 in response to viruses for IFN-alpha/beta gene induction. Immunity 13:539–548PubMedCrossRef
64.
Shilei W, Wangjing L (2008) A role of toll-like receptor 3 in infectious bursal disease virus infection. In: The 14th Symposium Poultry Health Branch, Chinese Association of Animal and Veterinary Science, China, p 139
65.
Shimazu R, Akashi S, Ogata H, Nagai Y, Fukudome K, Miyake K, Kimoto M (1999) MD-2, a molecule that confers lipopolysaccharide responsiveness on Toll-like receptor 4. J Exp Med 189:1777–1782PubMedCrossRef
66.
Sun Y, Ishibashi M, Seimon T, Lee M, Sharma SM, Fitzgerald KA, Samokhin AO, Wang Y, Sayers S, Aikawa M, Jerome WG, Ostrowski MC, Bromme D, Libby P, Tabas IA, Welch CL, Tall AR (2009) Free cholesterol accumulation in macrophage membranes activates Toll-like receptors and p38 mitogen-activated protein kinase and induces cathepsin K. Circ Res 104:455–465PubMedCrossRef
67.
68.
Tanimura N, Sharma JM (1997) Appearance of T cells in the bursa of Fabricius and cecal tonsils during the acute phase of infectious bursal disease virus infection in chickens. Avian Dis 41:638–645PubMedCrossRef
69.
Telepnev MV, Klimpel GR, Haithcoat J, Knirel YA, Anisimov AP, Motin VL (2009) Tetraacylated lipopolysaccharide of Yersinia pestis can inhibit multiple Toll-like receptor-mediated signaling pathways in human dendritic cells. J Infect Dis 200:1694–1702PubMedCrossRef
70.
Uematsu S, Akira S (2008) Toll-Like receptors (TLRs) and their ligands. Handb Exp Pharmacol:1-20
71.
Wang D, Xiong J, She R, Liu L, Zhang Y, Luo D, Li W, Hu Y, Wang Y, Zhang Q, Sun Q (2008) Mast cell mediated inflammatory response in chickens after infection with very virulent infectious bursal disease virus. Vet Immunol Immunopathol 124:19–28PubMedCrossRef
72.
Wang D, Liu Y, She R, Xu J, Liu L, Xiong J, Yang Y, Sun Q, Peng K (2009) Reduced mucosal injury of SPF chickens by mast cell stabilization after infection with very virulent infectious bursal disease virus. Vet Immunol Immunopathol 131:229–237PubMedCrossRef
73.
Wang R, Wang Z, Yang J, Liu X, Wang L, Guo X, Zeng F, Wu M, Li G (2011) LRRC4 inhibits the proliferation of human glioma cells by modulating the expression of STMN1 and microtubule polymerization. J Cell Biochem 112(12):3621–3629PubMedCrossRef
74.
Wei L, Zhu S, Ruan G, Hou L, Wang J, Wang B, Liu J (2011) Infectious bursal disease virus-induced activation of JNK signaling pathway is required for virus replication and correlates with virus-induced apoptosis. Virology 420(2):156–163PubMedCrossRef
75.
Woronicz JD, Gao X, Cao Z, Rothe M, Goeddel DV (1997) IkappaB kinase-beta: NF-kappaB activation and complex formation with IkappaB kinase-alpha and NIK. Science 278:866–869PubMedCrossRef
76.
Wu MH, Zhang P, Huang X (2010) Toll-like receptors in innate immunity and infectious diseases. Front Med China 4:385–393PubMedCrossRef
77.
Yang IV, Jiang W, Rutledge HR, Lackford B, Warg LA, De Arras L, Alper S, Schwartz DA, Pisetsky DS (2011) Identification of novel innate immune genes by transcriptional profiling of macrophages stimulated with TLR ligands. Mol Immunol 48:1886–1895PubMedCrossRef
Metadata
Title
Differential expression of the Toll-like receptor pathway and related genes of chicken bursa after experimental infection with infectious bursa disease virus
Authors
Xinfeng Guo
Liqiong Wang
Defeng Cui
Wenke Ruan
Fenghua Liu
Huanrong Li
Publication date
01-11-2012
Publisher
Springer Vienna
Published in
Archives of Virology / Issue 11/2012
Print ISSN: 0304-8608
Electronic ISSN: 1432-8798
DOI
https://doi.org/10.1007/s00705-012-1403-y

Other articles of this Issue 11/2012

Archives of Virology 11/2012 Go to the issue

Brief Report

The pan-genotype specificity of the hepatitis C virus anti-core monoclonal antibody C7-50 is contingent on the quasispecies profile of a population

Erratum

Erratum to: An overview of infectious bursal disease

Annotated Sequence Record

Full-length genome analysis of vesicular stomatitis New Jersey virus strains representing the phylogenetic and geographic diversity of the virus

Original Article

Tracing the genetic history of porcine reproductive and respiratory syndrome viruses derived from the complete ORF 5-7 sequences: a Bayesian coalescent approach

Brief Report

Development of a minigenome system for Andes virus, a New World hantavirus

Brief Report

Biology of fowl adenovirus type 1 infection of heterologous cells
Obesity Clinical Trial Summary

At a glance: The STEP trials

Read more

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Pediatric Cardiology Video

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

Cardiopulmonary Comorbidity Video

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Valvular Heart Disease Video

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.

ACC 2024 Congress Coverage

Heart Failure Video

Year in Review: Heart failure and cardiomyopathies

Watch now

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits