The Involvement of Histone H3 Acetylation in Bovine Herpesvirus 1 Replication in MDBK Cells

Overview

Journal Viruses

Publisher MDPI

Specialty Microbiology

Date 2018 Sep 29

PMID 30261679

Citations 5

Authors

Liqian Zhu

Xinyi Jiang

Xiaotian Fu

Yanhua Qi

Guoqiang Zhu

Affiliations

Soon will be listed here.

Abstract

During bovine herpesvirus 1 (BoHV-1) productive infection in cell cultures, partial of intranuclear viral DNA is present in nucleosomes, and viral protein VP22 associates with histones and decreases histone H4 acetylation, indicating the involvement of histone H4 acetylation in virus replication. In this study, we demonstrated that BoHV-1 infection at the late stage (at 24 h after infection) dramatically decreased histone H3 acetylation [at residues K9 (H3K9ac) and K18 (H3K18ac)], which was supported by the pronounced depletion of histone acetyltransferases (HATs) including CBP/P300 (CREB binding protein and p300), GCN5L2 (general control of amino acid synthesis yeast homolog like 2) and PCAF (P300/CBP-associated factor). The depletion of GCN5L2 promoted by virus infection was partially mediated by ubiquitin-proteasome pathway. Interestingly, the viral replication was enhanced by HAT (histone acetyltransferase) activator CTPB [-(4-Chloro-3-trifluoromethylphenyl)-2-ethoxy-6-pentadecylbenzamide], and vice versa, inhibited by HAT inhibitor Anacardic acid (AA), suggesting that BoHV-1 may take advantage of histone acetylation for efficient replication. Taken together, we proposed that the HAT-dependent histone H3 acetylation plays an important role in BoHV-1 replication in MDBK (Madin-Darby bovine kidney) cells.

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References

Sun Y, Jiang X, Chen S, Price B . Inhibition of histone acetyltransferase activity by anacardic acid sensitizes tumor cells to ionizing radiation. FEBS Lett. 2006; 580(18):4353-6. DOI: 10.1016/j.febslet.2006.06.092. View

Jones C . Regulation of Innate Immune Responses by Bovine Herpesvirus 1 and Infected Cell Protein 0 (bICP0). Viruses. 2011; 1(2):255-75. PMC: 3185490. DOI: 10.3390/v1020255. View

Chen X, Barozzi I, Termanini A, Prosperini E, Recchiuti A, Dalli J . Requirement for the histone deacetylase Hdac3 for the inflammatory gene expression program in macrophages. Proc Natl Acad Sci U S A. 2012; 109(42):E2865-74. PMC: 3479529. DOI: 10.1073/pnas.1121131109. View

Nakashima H, Kaufmann J, Wang P, Nguyen T, Speranza M, Kasai K . Histone deacetylase 6 inhibition enhances oncolytic viral replication in glioma. J Clin Invest. 2015; 125(11):4269-80. PMC: 4639993. DOI: 10.1172/JCI80713. View

Danaher R, Jacob R, Steiner M, Allen W, Hill J, Miller C . Histone deacetylase inhibitors induce reactivation of herpes simplex virus type 1 in a latency-associated transcript-independent manner in neuronal cells. J Neurovirol. 2005; 11(3):306-17. PMC: 1361429. DOI: 10.1080/13550280590952817. View

Risalde M, Molina V, Sanchez-Cordon P, Pedrera M, Panadero R, Romero-Palomo F . Response of proinflammatory and anti-inflammatory cytokines in calves with subclinical bovine viral diarrhea challenged with bovine herpesvirus-1. Vet Immunol Immunopathol. 2011; 144(1-2):135-43. DOI: 10.1016/j.vetimm.2011.07.022. View

Chen L, Wang C, Luo J, Su W, Li M, Zhao N . Histone Deacetylase 1 Plays an Acetylation-Independent Role in Influenza A Virus Replication. Front Immunol. 2018; 8:1757. PMC: 5733105. DOI: 10.3389/fimmu.2017.01757. View

Neibergs H, Seabury C, Wojtowicz A, Wang Z, Scraggs E, Kiser J . Susceptibility loci revealed for bovine respiratory disease complex in pre-weaned holstein calves. BMC Genomics. 2014; 15:1164. PMC: 4445561. DOI: 10.1186/1471-2164-15-1164. View

Koppers-Lalic D, Rijsewijk F, Verschuren S, van Gaans-van den Brink J, Neisig A, Ressing M . The UL41-encoded virion host shutoff (vhs) protein and vhs-independent mechanisms are responsible for down-regulation of MHC class I molecules by bovine herpesvirus 1. J Gen Virol. 2001; 82(Pt 9):2071-2081. DOI: 10.1099/0022-1317-82-9-2071. View

10.

Hancock M, Cliffe A, Knipe D, Smiley J . Herpes simplex virus VP16, but not ICP0, is required to reduce histone occupancy and enhance histone acetylation on viral genomes in U2OS osteosarcoma cells. J Virol. 2009; 84(3):1366-75. PMC: 2812316. DOI: 10.1128/JVI.01727-09. View

11.

Zou C, Mallampalli R . Regulation of histone modifying enzymes by the ubiquitin-proteasome system. Biochim Biophys Acta. 2014; 1843(4):694-702. PMC: 3966433. DOI: 10.1016/j.bbamcr.2013.12.016. View

12.

Myung J, Kim K, Crews C . The ubiquitin-proteasome pathway and proteasome inhibitors. Med Res Rev. 2001; 21(4):245-73. PMC: 2556558. DOI: 10.1002/med.1009. View

13.

Fulton R, dOffay J, Landis C, Miles D, Smith R, Saliki J . Detection and characterization of viruses as field and vaccine strains in feedlot cattle with bovine respiratory disease. Vaccine. 2016; 34(30):3478-92. PMC: 7173208. DOI: 10.1016/j.vaccine.2016.04.020. View

14.

Herrera F, Triezenberg S . VP16-dependent association of chromatin-modifying coactivators and underrepresentation of histones at immediate-early gene promoters during herpes simplex virus infection. J Virol. 2004; 78(18):9689-96. PMC: 515004. DOI: 10.1128/JVI.78.18.9689-9696.2004. View

15.

Zhang Y, Jiang Y, Geiser V, Zhou J, Jones C . Bovine herpesvirus 1 immediate-early protein (bICP0) interacts with the histone acetyltransferase p300, which stimulates productive infection and gC promoter activity. J Gen Virol. 2006; 87(Pt 7):1843-1851. DOI: 10.1099/vir.0.81766-0. View

16.

Cliffe A, Knipe D . Herpes simplex virus ICP0 promotes both histone removal and acetylation on viral DNA during lytic infection. J Virol. 2008; 82(24):12030-8. PMC: 2593313. DOI: 10.1128/JVI.01575-08. View

17.

Saira K, Zhou Y, Jones C . The infected cell protein 0 encoded by bovine herpesvirus 1 (bICP0) induces degradation of interferon response factor 3 and, consequently, inhibits beta interferon promoter activity. J Virol. 2007; 81(7):3077-86. PMC: 1866033. DOI: 10.1128/JVI.02064-06. View

18.

Ghizzoni M, Wu J, Gao T, Haisma H, Dekker F, Zheng Y . 6-alkylsalicylates are selective Tip60 inhibitors and target the acetyl-CoA binding site. Eur J Med Chem. 2011; 47(1):337-44. PMC: 3399519. DOI: 10.1016/j.ejmech.2011.11.001. View

19.

Bannister A, Kouzarides T . Regulation of chromatin by histone modifications. Cell Res. 2011; 21(3):381-95. PMC: 3193420. DOI: 10.1038/cr.2011.22. View

20.

Ren X, Harms J, Splitter G . Bovine herpesvirus 1 tegument protein VP22 interacts with histones, and the carboxyl terminus of VP22 is required for nuclear localization. J Virol. 2001; 75(17):8251-8. PMC: 115069. DOI: 10.1128/jvi.75.17.8251-8258.2001. View