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Published in: Virology Journal 1/2014

Open Access 01-12-2014 | Short report

Comparative analysis of apoptotic changes in peripheral immune organs and lungs following experimental infection of piglets with highly pathogenic and classical porcine reproductive and respiratory syndrome virus

Authors: Gang Wang, Yuli He, Yabin Tu, Yonggang Liu, En-Min Zhou, Zifeng Han, Chenggang Jiang, Shujie Wang, Wenda Shi, Xuehui Cai

Published in: Virology Journal | Issue 1/2014

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Abstract

Background

Our previous studies have demonstrated that piglets infected with highly pathogenic porcine reproductive and respiratory syndrome virus (HP-PRRSV) may develop significant thymus atrophy, which related to thymocytes apoptosis. However, apart from that detected in the thymus, there are no reports describing cell apoptosis induced by HP-PRRSV infection. In this study, we analyzed comparatively the pathological changes, cell apoptosis and viral load in peripheral immune organs including tonsil, inguinal lymph nodes (ILNs) and spleen and lungs following experimental infection of piglets with HP-PRRSV HuN4 and classical PRRSV CH-1a.

Findings

HP-PRRSV HuN4 exhibited much stronger cell tropism than CH-1a in immune organs and lungs of piglets. HuN4 infection led to the serious injuries in tonsils, ILNs, spleens and lungs, especially apoptosis in these organs was significant.

Conclusions

HuN4 infection induced severe lesions (gross pathology, histopathology and cell apoptosis) in the peripheral immune organs and lungs of infected piglets. Large numbers of apoptotic cells in immune organs and lung induced by HuN4 may play a role in the pathogenesis of the HP-PRRS and the distinct injuries caused by HuN4 infection may be associated with the high mortality rate of HP-PRRS in pigs.
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Literature
1.
go back to reference Wensvoort G, Terpstra C, Pol JM, ter Laak EA, Bloemraad M, de Kluyver EP, Kragten C, van Buiten L, den Besten A, Wagenaar F, et al.: Mystery swine disease in The Netherlands: the isolation of Lelystad virus. Vet Q 1991, 13: 121-130. 10.1080/01652176.1991.9694296PubMedCrossRef Wensvoort G, Terpstra C, Pol JM, ter Laak EA, Bloemraad M, de Kluyver EP, Kragten C, van Buiten L, den Besten A, Wagenaar F, et al.: Mystery swine disease in The Netherlands: the isolation of Lelystad virus. Vet Q 1991, 13: 121-130. 10.1080/01652176.1991.9694296PubMedCrossRef
2.
go back to reference Terpstra C, Wensvoort G, Pol JM: Experimental reproduction of porcine epidemic abortion and respiratory syndrome (mystery swine disease) by infection with Lelystad virus: Koch's postulates fulfilled. Vet Q 1991, 13: 131-136. 10.1080/01652176.1991.9694297PubMedCrossRef Terpstra C, Wensvoort G, Pol JM: Experimental reproduction of porcine epidemic abortion and respiratory syndrome (mystery swine disease) by infection with Lelystad virus: Koch's postulates fulfilled. Vet Q 1991, 13: 131-136. 10.1080/01652176.1991.9694297PubMedCrossRef
3.
go back to reference Collins JE, Benfield DA, Christianson WT, Harris L, Hennings JC, Shaw DP, Goyal SM, McCullough S, Morrison RB, Joo HS: Isolation of swine infertility and respiratory syndrome virus (isolate ATCC VR-2332) in North America and experimental reproduction of the disease in gnotobiotic pigs. J Vet Diagn Invest 1992, 4: 117. 10.1177/104063879200400201PubMedCrossRef Collins JE, Benfield DA, Christianson WT, Harris L, Hennings JC, Shaw DP, Goyal SM, McCullough S, Morrison RB, Joo HS: Isolation of swine infertility and respiratory syndrome virus (isolate ATCC VR-2332) in North America and experimental reproduction of the disease in gnotobiotic pigs. J Vet Diagn Invest 1992, 4: 117. 10.1177/104063879200400201PubMedCrossRef
4.
go back to reference Rossow KD: Porcine reproductive and respiratory syndrome. Vet Pathol 1998, 35: 1-20. 10.1177/030098589803500101PubMedCrossRef Rossow KD: Porcine reproductive and respiratory syndrome. Vet Pathol 1998, 35: 1-20. 10.1177/030098589803500101PubMedCrossRef
5.
go back to reference Tian K, Yu X, Zhao T, Feng Y, Cao Z, Wang C, Hu Y, Chen X, Hu D, Tian X, et al.: Emergence of fatal PRRSV variants: unparalleled outbreaks of atypical PRRS in China and molecular dissection of the unique hallmark. PLoS One 2007, 2: e526. 10.1371/journal.pone.0000526PubMedPubMedCentralCrossRef Tian K, Yu X, Zhao T, Feng Y, Cao Z, Wang C, Hu Y, Chen X, Hu D, Tian X, et al.: Emergence of fatal PRRSV variants: unparalleled outbreaks of atypical PRRS in China and molecular dissection of the unique hallmark. PLoS One 2007, 2: e526. 10.1371/journal.pone.0000526PubMedPubMedCentralCrossRef
6.
go back to reference Dukic S, Heurtaux T, Kaltenbach ML, Hoizey G, Lallemand A, Gourdier B, Vistelle R: Pharmacokinetics of methotrexate in the extracellular fluid of brain C6-glioma after intravenous infusion in rats. Pharm Res 1999, 16: 1219-1225. 10.1023/A:1018945529611PubMedCrossRef Dukic S, Heurtaux T, Kaltenbach ML, Hoizey G, Lallemand A, Gourdier B, Vistelle R: Pharmacokinetics of methotrexate in the extracellular fluid of brain C6-glioma after intravenous infusion in rats. Pharm Res 1999, 16: 1219-1225. 10.1023/A:1018945529611PubMedCrossRef
7.
go back to reference Feng WH, Tompkins MB, Xu JS, Brown TT, Laster SM, Zhang HX, McCaw MB: Thymocyte and peripheral blood T lymphocyte subpopulation changes in piglets following in utero infection with porcine reproductive and respiratory syndrome virus. Virology 2002, 302: 363-372. 10.1006/viro.2002.1650PubMedCrossRef Feng WH, Tompkins MB, Xu JS, Brown TT, Laster SM, Zhang HX, McCaw MB: Thymocyte and peripheral blood T lymphocyte subpopulation changes in piglets following in utero infection with porcine reproductive and respiratory syndrome virus. Virology 2002, 302: 363-372. 10.1006/viro.2002.1650PubMedCrossRef
8.
go back to reference Labarque G, Van Gucht S, Nauwynck H, Van Reeth K, Pensaert M: Apoptosis in the lungs of pigs infected with porcine reproductive and respiratory syndrome virus and associations with the production of apoptogenic cytokines. Vet Res 2003, 34: 249-260. 10.1051/vetres:2003001PubMedCrossRef Labarque G, Van Gucht S, Nauwynck H, Van Reeth K, Pensaert M: Apoptosis in the lungs of pigs infected with porcine reproductive and respiratory syndrome virus and associations with the production of apoptogenic cytokines. Vet Res 2003, 34: 249-260. 10.1051/vetres:2003001PubMedCrossRef
9.
go back to reference Sur JH, Doster AR, Osorio FA: Apoptosis induced in vivo during acute infection by porcine reproductive and respiratory syndrome virus. Vet Pathol 1998, 35: 506-514. 10.1177/030098589803500605PubMedCrossRef Sur JH, Doster AR, Osorio FA: Apoptosis induced in vivo during acute infection by porcine reproductive and respiratory syndrome virus. Vet Pathol 1998, 35: 506-514. 10.1177/030098589803500605PubMedCrossRef
10.
go back to reference Sur JH, Doster AR, Christian JS, Galeota JA, Wills RW, Zimmerman JJ, Osorio FA: Porcine reproductive and respiratory syndrome virus replicates in testicular germ cells, alters spermatogenesis, and induces germ cell death by apoptosis. J Virol 1997, 71: 9170-9179.PubMedPubMedCentral Sur JH, Doster AR, Christian JS, Galeota JA, Wills RW, Zimmerman JJ, Osorio FA: Porcine reproductive and respiratory syndrome virus replicates in testicular germ cells, alters spermatogenesis, and induces germ cell death by apoptosis. J Virol 1997, 71: 9170-9179.PubMedPubMedCentral
11.
go back to reference Karniychuk UU, Saha D, Geldhof M, Vanhee M, Cornillie P, Van den Broeck W, Nauwynck HJ: Porcine reproductive and respiratory syndrome virus (PRRSV) causes apoptosis during its replication in fetal implantation sites. Microb Pathog 2011, 51: 194-202. 10.1016/j.micpath.2011.04.001PubMedCrossRef Karniychuk UU, Saha D, Geldhof M, Vanhee M, Cornillie P, Van den Broeck W, Nauwynck HJ: Porcine reproductive and respiratory syndrome virus (PRRSV) causes apoptosis during its replication in fetal implantation sites. Microb Pathog 2011, 51: 194-202. 10.1016/j.micpath.2011.04.001PubMedCrossRef
12.
go back to reference Wang G, Song T, Yu Y, Liu Y, Shi W, Wang S, Rong F, Dong J, Liu H, Cai X, Zhou EM: Immune responses in piglets infected with highly pathogenic porcine reproductive and respiratory syndrome virus. Vet Immunol Immunopathol 2011, 142: 170-178. 10.1016/j.vetimm.2011.05.004PubMedCrossRef Wang G, Song T, Yu Y, Liu Y, Shi W, Wang S, Rong F, Dong J, Liu H, Cai X, Zhou EM: Immune responses in piglets infected with highly pathogenic porcine reproductive and respiratory syndrome virus. Vet Immunol Immunopathol 2011, 142: 170-178. 10.1016/j.vetimm.2011.05.004PubMedCrossRef
13.
go back to reference He Y, Wang G, Liu Y, Shi W, Han Z, Wu J, Jiang C, Wang S, Hu S, Wen H, et al.: Characterization of thymus atrophy in piglets infected with highly pathogenic porcine reproductive and respiratory syndrome virus. Vet Microbiol 2012, 160: 455-462. 10.1016/j.vetmic.2012.05.040PubMedCrossRef He Y, Wang G, Liu Y, Shi W, Han Z, Wu J, Jiang C, Wang S, Hu S, Wen H, et al.: Characterization of thymus atrophy in piglets infected with highly pathogenic porcine reproductive and respiratory syndrome virus. Vet Microbiol 2012, 160: 455-462. 10.1016/j.vetmic.2012.05.040PubMedCrossRef
14.
go back to reference Liu Y, Shi W, Zhou E, Wang S, Hu S, Cai X, Rong F, Wu J, Xu M, Li L: Dynamic changes in inflammatory cytokines in pigs infected with highly pathogenic porcine reproductive and respiratory syndrome virus. Clin Vaccine Immunol 2010, 17: 1439-1445. 10.1128/CVI.00517-09PubMedPubMedCentralCrossRef Liu Y, Shi W, Zhou E, Wang S, Hu S, Cai X, Rong F, Wu J, Xu M, Li L: Dynamic changes in inflammatory cytokines in pigs infected with highly pathogenic porcine reproductive and respiratory syndrome virus. Clin Vaccine Immunol 2010, 17: 1439-1445. 10.1128/CVI.00517-09PubMedPubMedCentralCrossRef
15.
go back to reference Qiu HJ, Tian ZJ, Tong GZ, Zhou YJ, Ni JQ, Luo YZ, Cai XH: Protective immunity induced by a recombinant pseudorabies virus expressing the GP5 of porcine reproductive and respiratory syndrome virus in piglets. Vet Immunol Immunopathol 2005, 106: 309-319. 10.1016/j.vetimm.2005.03.008PubMedCrossRef Qiu HJ, Tian ZJ, Tong GZ, Zhou YJ, Ni JQ, Luo YZ, Cai XH: Protective immunity induced by a recombinant pseudorabies virus expressing the GP5 of porcine reproductive and respiratory syndrome virus in piglets. Vet Immunol Immunopathol 2005, 106: 309-319. 10.1016/j.vetimm.2005.03.008PubMedCrossRef
16.
go back to reference Fenaux M, Halbur PG, Haqshenas G, Royer R, Thomas P, Nawagitgul P, Gill M, Toth TE, Meng XJ: Cloned genomic DNA of type 2 porcine circovirus is infectious when injected directly into the liver and lymph nodes of pigs: characterization of clinical disease, virus distribution, and pathologic lesions. J Virol 2002, 76: 541-551. 10.1128/JVI.76.2.541-551.2002PubMedPubMedCentralCrossRef Fenaux M, Halbur PG, Haqshenas G, Royer R, Thomas P, Nawagitgul P, Gill M, Toth TE, Meng XJ: Cloned genomic DNA of type 2 porcine circovirus is infectious when injected directly into the liver and lymph nodes of pigs: characterization of clinical disease, virus distribution, and pathologic lesions. J Virol 2002, 76: 541-551. 10.1128/JVI.76.2.541-551.2002PubMedPubMedCentralCrossRef
17.
go back to reference Fenaux M, Opriessnig T, Halbur PG, Meng XJ: Immunogenicity and pathogenicity of chimeric infectious DNA clones of pathogenic porcine circovirus type 2 (PCV2) and nonpathogenic PCV1 in weanling pigs. J Virol 2003, 77: 11232-11243. 10.1128/JVI.77.20.11232-11243.2003PubMedPubMedCentralCrossRef Fenaux M, Opriessnig T, Halbur PG, Meng XJ: Immunogenicity and pathogenicity of chimeric infectious DNA clones of pathogenic porcine circovirus type 2 (PCV2) and nonpathogenic PCV1 in weanling pigs. J Virol 2003, 77: 11232-11243. 10.1128/JVI.77.20.11232-11243.2003PubMedPubMedCentralCrossRef
18.
go back to reference Fenaux M, Opriessnig T, Halbur PG, Elvinger F, Meng XJ: A chimeric porcine circovirus (PCV) with the immunogenic capsid gene of the pathogenic PCV type 2 (PCV2) cloned into the genomic backbone of the nonpathogenic PCV1 induces protective immunity against PCV2 infection in pigs. J Virol 2004, 78: 6297-6303. 10.1128/JVI.78.12.6297-6303.2004PubMedPubMedCentralCrossRef Fenaux M, Opriessnig T, Halbur PG, Elvinger F, Meng XJ: A chimeric porcine circovirus (PCV) with the immunogenic capsid gene of the pathogenic PCV type 2 (PCV2) cloned into the genomic backbone of the nonpathogenic PCV1 induces protective immunity against PCV2 infection in pigs. J Virol 2004, 78: 6297-6303. 10.1128/JVI.78.12.6297-6303.2004PubMedPubMedCentralCrossRef
19.
go back to reference Halbur PG, Paul PS, Frey ML, Landgraf J, Eernisse K, Meng XJ, Lum MA, Andrews JJ, Rathje JA: Comparison of the pathogenicity of two US porcine reproductive and respiratory syndrome virus isolates with that of the Lelystad virus. Vet Pathol 1995, 32: 648-660. 10.1177/030098589503200606PubMedCrossRef Halbur PG, Paul PS, Frey ML, Landgraf J, Eernisse K, Meng XJ, Lum MA, Andrews JJ, Rathje JA: Comparison of the pathogenicity of two US porcine reproductive and respiratory syndrome virus isolates with that of the Lelystad virus. Vet Pathol 1995, 32: 648-660. 10.1177/030098589503200606PubMedCrossRef
20.
go back to reference Sgonc R, Wick G: Methods for the detection of apoptosis. Int Arch Allergy Immunol 1994, 105: 327-332. 10.1159/000236777PubMedCrossRef Sgonc R, Wick G: Methods for the detection of apoptosis. Int Arch Allergy Immunol 1994, 105: 327-332. 10.1159/000236777PubMedCrossRef
21.
go back to reference Tong GZ, Zhou YJ, Hao XF, Tian ZJ, An TQ, Qiu HJ: Highly pathogenic porcine reproductive and respiratory syndrome, China. Emerg Infect Dis 2007, 13: 1434-1436. 10.3201/eid1309.070399PubMedPubMedCentralCrossRef Tong GZ, Zhou YJ, Hao XF, Tian ZJ, An TQ, Qiu HJ: Highly pathogenic porcine reproductive and respiratory syndrome, China. Emerg Infect Dis 2007, 13: 1434-1436. 10.3201/eid1309.070399PubMedPubMedCentralCrossRef
22.
go back to reference Bertin A, Mangenot S, Renouard M, Durand D, Livolant F: Structure and phase diagram of nucleosome core particles aggregated by multivalent cations. Biophys J 2007, 93: 3652-3663. 10.1529/biophysj.107.108365PubMedPubMedCentralCrossRef Bertin A, Mangenot S, Renouard M, Durand D, Livolant F: Structure and phase diagram of nucleosome core particles aggregated by multivalent cations. Biophys J 2007, 93: 3652-3663. 10.1529/biophysj.107.108365PubMedPubMedCentralCrossRef
23.
go back to reference Choi C, Chae C: Expression of tumour necrosis factor-alpha is associated with apoptosis in lungs of pigs experimentally infected with porcine reproductive and respiratory syndrome virus. Res Vet Sci 2002, 72: 45-49.PubMedCrossRef Choi C, Chae C: Expression of tumour necrosis factor-alpha is associated with apoptosis in lungs of pigs experimentally infected with porcine reproductive and respiratory syndrome virus. Res Vet Sci 2002, 72: 45-49.PubMedCrossRef
24.
go back to reference Suarez P, Diaz-Guerra M, Prieto C, Esteban M, Castro JM, Nieto A, Ortin J: Open reading frame 5 of porcine reproductive and respiratory syndrome virus as a cause of virus-induced apoptosis. J Virol 1996, 70: 2876-2882.PubMedPubMedCentral Suarez P, Diaz-Guerra M, Prieto C, Esteban M, Castro JM, Nieto A, Ortin J: Open reading frame 5 of porcine reproductive and respiratory syndrome virus as a cause of virus-induced apoptosis. J Virol 1996, 70: 2876-2882.PubMedPubMedCentral
Metadata
Title
Comparative analysis of apoptotic changes in peripheral immune organs and lungs following experimental infection of piglets with highly pathogenic and classical porcine reproductive and respiratory syndrome virus
Authors
Gang Wang
Yuli He
Yabin Tu
Yonggang Liu
En-Min Zhou
Zifeng Han
Chenggang Jiang
Shujie Wang
Wenda Shi
Xuehui Cai
Publication date
01-12-2014
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2014
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/1743-422X-11-2

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