Different inhibitory effects on the proliferation and apoptosis of human and laboratory Borna disease virus‑infected human neuroblastoma SH‑SY5Y cells in vitro

Huang,Hua; Zhang,Hong; Li,Dan; Chen,Shigang; Zhou,Chanjuan; Li,Qi; He,Peng; Fang,Liang; Zhang,Yong; Li,Xiaomei; Zhou,Jingjing; Sun,Lin; Liu,Siwen; Guo,Yujie; Huang,Ying; Xie,Peng

doi:10.3892/mmr.2017.8011

Different inhibitory effects on the proliferation and apoptosis of human and laboratory Borna disease virus‑infected human neuroblastoma SH‑SY5Y cells in vitro

Authors:
- Hua Huang
- Hong Zhang
- Dan Li
- Shigang Chen
- Chanjuan Zhou
- Qi Li
- Peng He
- Liang Fang
- Yong Zhang
- Xiaomei Li
- Jingjing Zhou
- Lin Sun
- Siwen Liu
- Yujie Guo
- Ying Huang
- Peng Xie
View Affiliations

Affiliations: Department of Neurology, The Second Affiliated Hospital of Chongqing Medical University, Chongqing 400010, P.R. China, Department of Neurology, Yongchuan Hospital, Chongqing Medical University, Chongqing 402460, P.R. China, Institute of Neuroscience and The Collaborative Innovation Center for Brain Science, Chongqing Medical University, Chongqing 400016, P.R. China
Published online on: November 8, 2017 https://doi.org/10.3892/mmr.2017.8011
Pages: 925-931
Copyright: © Huang et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

Borna disease virus (BDV) is a neurotropic and non‑cytolytic virus, which causes behavioral disorders in a wide range of warm‑blooded species. It is well established that BDV induces neurodegeneration by impairing neurogenesis and interfering with neuronal functioning in the limbic system. In the present study, the potential role of BDV infection in SH‑SY5Y cells was identified, and comparisons of two original BDV strains (the human Hu‑H1 and the laboratory Strain V) were performed to further elucidate the phenotypes of BDV pathogenesis with strain differences. Cell Counting Kit‑8 and flow cytometric analyses revealed that the two BDV strain‑infected groups exhibited marked anti‑proliferation and cell cycle arrest compared with the control group, and the Hu‑H1 strain caused more evident effects. However, the Hu‑H1 strain did not exert effects on the apoptosis of SH‑SH5Y cells, while Strain V led to a marked increase in apoptosis upon initial infection. Western blot analysis confirmed the upregulation of apoptosis regulator BAX protein and the downregulation of apoptosis regulator Bcl‑2 protein caused by the two BDV strains. The results of the present study provided evidence that infection with BDV suppressed SH‑SY5Y cellular functioning and exhibited divergent antiproliferative and apoptotic roles in cells between the two strains. The present study provided an insight for future investigation of strain differences and underlying pathomechanisms.

View Figures

View References

1	De la Torre JC, Mallory M, Brot M, Gold L, Koob G, Oldstone MB and Masliah E: Viral persistence in neurons alters synaptic plasticity and cognitive functions without destruction of brain cells. Virology. 220:508–515. 1996. View Article : Google Scholar : PubMed/NCBI
2	Dietzschold B, Li J, Faber M and Schnell M: Concepts in the pathogenesis of rabies. Future Virol. 3:481–490. 2008. View Article : Google Scholar : PubMed/NCBI
3	Cubitt B, Oldstone C and de la Torre JC: Sequence and genome organization of Borna disease virus. J Virol. 68:1382–1396. 1994.PubMed/NCBI
4	Briese T, Schneemann A, Lewis AJ, Park YS, Kim S, Ludwig H and Lipkin WI: Genomic organization of Borna disease virus. Proc Natl Acad Sci USA. 91:4362–4366. 1994. View Article : Google Scholar : PubMed/NCBI
5	Dürrwald R and Ludwig H: Borna disease virus (BDV), a (zoonotic?) worldwide pathogen. A review of the history of the disease and the virus infection with comprehensive bibliography. Zentralbl Veterinarmed B. 44:147–184. 1997.PubMed/NCBI
6	Bode L, Dürrwald R and Ludwig H: Borna virus infections in cattle associated with fatal neurological disease. Vet Rec. 135:283–284. 1994. View Article : Google Scholar : PubMed/NCBI
7	Hagiwara K, Tsuge Y, Asakawa M, Kabaya H, Okamoto M, Miyasho T, Taniyama H, Ishihara C, de la Torre JC and Ikuta K: Borna disease virus RNA detected in Japanese macaques (Macaca fuscata). Primates. 49:57–64. 2008. View Article : Google Scholar : PubMed/NCBI
8	Hornig M, Solbrig M, Horscroft N, Weissenböck H and Lipkin WI: Borna disease virus infection of adult and neonatal rats: Models for neuropsychiatric disease. Curr Top Microbiol Immunol. 253:157–177. 2001.PubMed/NCBI
9	Pletnikov MV, Moran TH and Carbone KM: Borna disease virus infection of the neonatal rat: Developmental brain injury model of autism spectrum disorders. Front Biosci. 7:d593–d607. 2002. View Article : Google Scholar : PubMed/NCBI
10	Williams BL, Hornig M, Yaddanapudi K and Lipkin WI: Hippocampal poly(ADP-Ribose) polymerase 1 and caspase 3 activation in neonatal bornavirus infection. J Virol. 82:1748–1758. 2008. View Article : Google Scholar : PubMed/NCBI
11	Zhang L, Xu MM, Zeng L, Liu S, Liu X, Wang X, Li D, Huang RZ, Zhao LB, Zhan QL, et al: Evidence for Borna disease virus infection in neuropsychiatric patients in three western China provinces. Eur J Clin Microbiol Infect Dis. 33:621–627. 2014. View Article : Google Scholar : PubMed/NCBI
12	Das S and Basu A: Viral infection and neural stem/progenitor cell's fate: Implications in brain development and neurological disorders. Neurochem Int. 59:357–366. 2011. View Article : Google Scholar : PubMed/NCBI
13	Brnic D, Stevanovic V, Cochet M, Agier C, Richardson J, Montero-Menei CN, Milhavet O, Eloit M and Coulpier M: Borna disease virus infects human neural progenitor cells and impairs neurogenesis. J Virol. 86:2512–2522. 2012. View Article : Google Scholar : PubMed/NCBI
14	Scordel C, Huttin A, Cochet-Bernoin M, Szelechowski M, Poulet A, Richardson J, Benchoua A, Gonzalez-Dunia D, Eloit M and Coulpier M: Borna disease virus phosphoprotein impairs the developmental program controlling neurogenesis and reduces human GABAergic neurogenesis. PLoS Pathog. 11:e10048592015. View Article : Google Scholar : PubMed/NCBI
15	Poenisch M, Burger N, Staeheli P, Bauer G and Schneider U: Protein X of Borna disease virus inhibits apoptosis and promotes viral persistence in the central nervous systems of newborn-infected rats. J Virol. 83:4297–4307. 2009. View Article : Google Scholar : PubMed/NCBI
16	Wu YJ, Schulz H, Lin CC, Saar K, Patone G, Fischer H, Hübner N, Heimrich B and Schwemmle M: Borna disease virus-induced neuronal degeneration dependent on host genetic background and prevented by soluble factors. Proc Natl Acad Sci USA. 110:1899–1904. 2013. View Article : Google Scholar : PubMed/NCBI
17	Li Q, Wang Z, Zhu D, Xu M, Chen X, Peng D, Iwata Y and Xie P: Detection and analysis of Borna disease virus in Chinese patients with neurological disorders. Eur J Neurol. 16:399–403. 2009. View Article : Google Scholar : PubMed/NCBI
18	Wang X, Zhang L, Lei Y, Liu X, Zhou X, Liu Y, Wang M, Yang L, Zhang L, Fan S and Xie P: Meta-analysis of infectious agents and depression. Sci Rep. 4:45302014. View Article : Google Scholar : PubMed/NCBI
19	Hornig M, Briese T, Licinio J, Khabbaz RF, Altshuler LL, Potkin SG, Schwemmle M, Siemetzki U, Mintz J, Honkavuori K, et al: Absence of evidence for bornavirus infection in schizophrenia, bipolar disorder and major depressive disorder. Mol Psychiatr. 17:486–493. 2012. View Article : Google Scholar
20	Zwick W: Neuere Untersuchungen über die seuchenhafte Gehirn-u. Rückenmarksentzündung (Borna'sche Krankheit) der Pferde. Dtsch. Z. Nervenheilk. 110:316–322. 1929. View Article : Google Scholar
21	Liu S, Bode L, Zhang L, He P, Huang R, Sun L, Chen S, Zhang H, Guo Y, Zhou J, et al: GC-MS-Based metabonomic profiling displayed differing effects of Borna Disease Virus natural strain Hu-H1 and laboratory Strain V infection in rat cortical neurons. Int J Mol Sci. 16:19347–19368. 2015. View Article : Google Scholar : PubMed/NCBI
22	Li D, Lei Y, Deng J, Zhou C, Zhang Y, Li W, Huang H, Cheng S, Zhang H, Zhang L, et al: Human but not laboratory Borna Disease Virus inhibits proliferation and induces apoptosis in human oligodendrocytes in vitro. PLoS One. 8:e666232013. View Article : Google Scholar : PubMed/NCBI
23	Huang R, Gao H, Zhang L, Jia J, Liu X, Zheng P, Ma L, Li W, Deng J, Wang X, et al: Borna disease virus infection perturbs energy metabolites and amino acids in cultured human oligodendroglia cells. PLoS One. 7:e446652012. View Article : Google Scholar : PubMed/NCBI
24	Planz O, Pleschka S, Oesterle K, Berberich-Siebelt F, Ehrhardt C, Stitz L and Ludwig S: Borna disease virus nucleoprotein interacts with the CDC2-cyclin B1 complex. J Virol. 77:11186–11192. 2003. View Article : Google Scholar : PubMed/NCBI
25	Ludwig H, Furuya K, Bode L, Klein N, Dürrwald R and Lee DS: Biology and neurobiology of Borna disease viruses (BDV), defined by antibodies, neutralizability and their pathogenic potential. Arch Virol Suppl. 7:111–133. 1993. View Article : Google Scholar : PubMed/NCBI
26	Kuhn JH, Dürrwald R, Bào Y, Briese T, Carbone K, Clawson AN, deRisi JL, Garten W, Jahrling PB, Kolodziejek J, et al: Taxonomic reorganization of the family Bornaviridae. Arch Virol. 160:621–632. 2015. View Article : Google Scholar : PubMed/NCBI
27	Liu X, Liu S, Bode L, Liu C, Zhang L, Wang X, Li D, Lei Y, Peng X, Cheng Z and Xie P: Persistent human Borna disease virus infection modifies the acetylome of human oligodendroglia cells towards higher energy and transporter levels. Virology. 485:58–78. 2015. View Article : Google Scholar : PubMed/NCBI