1887

Abstract

Histone deacetylase 6 (HDAC6) is a unique cytoplasmic deacetylase that regulates various important biological processes by preventing protein aggregation and deacetylating different non-histone substrates including tubulin, heat shock protein 90, cortactin, retinoic acid inducible gene I and β-catenin. Growing evidence has indicated a dual role for HDAC6 in viral infection and pathogenesis: HDAC6 may represent a host defence mechanism against viral infection by modulating microtubule acetylation, triggering antiviral immune response and stimulating protective autophagy, or it may be hijacked by the virus to enhance proinflammatory response. In this review, we will highlight current data illustrating the complexity and importance of HDAC6 in viral pathogenesis. We will summarize the structure and functional specificity of HDAC6, and its deacetylase- and ubiquitin-dependent activity in key cellular events in response to virus infection. We will also discuss how HDAC6 exerts its direct or indirect histone modification ability in viral lytic–latency switch.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000679
2017-03-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/jgv/98/3/322.html?itemId=/content/journal/jgv/10.1099/jgv.0.000679&mimeType=html&fmt=ahah

References

  1. Ribet D, Cossart P. Pathogen-mediated posttranslational modifications: a re-emerging field. Cell 2010; 143:694–702 [View Article][PubMed]
    [Google Scholar]
  2. Salomon D, Orth K. What pathogens have taught us about posttranslational modifications. Cell Host Microbe 2013; 14:269–279 [View Article][PubMed]
    [Google Scholar]
  3. Verdel A, Curtet S, Brocard MP, Rousseaux S, Lemercier C et al. Active maintenance of mHDA2/mHDAC6 histone-deacetylase in the cytoplasm. Curr Biol 2000; 10:747–749[PubMed] [Crossref]
    [Google Scholar]
  4. Valenzuela-Fernández A, Cabrero JR, Serrador JM, Sánchez-Madrid F. HDAC6: a key regulator of cytoskeleton, cell migration and cell–cell interactions. Trends Cell Biol 2008; 18:291–297 [View Article][PubMed]
    [Google Scholar]
  5. Hai T, Hao J, Wang L, Jouneau A, Zhou Q. Pluripotency maintenance in mouse somatic cell nuclear transfer embryos and its improvement by treatment with the histone deacetylase inhibitor TSA. Cell Reprogram 2011; 13:47–56 [View Article][PubMed]
    [Google Scholar]
  6. Aldana-Masangkay GI, Sakamoto KM. The role of HDAC6 in cancer. J Biomed Biotechnol 2011; 2011: [View Article][PubMed]
    [Google Scholar]
  7. Li Y, Shin D, Kwon SH. Histone deacetylase 6 plays a role as a distinct regulator of diverse cellular processes. FEBS J 2013; 280:775–793 [View Article][PubMed]
    [Google Scholar]
  8. Carey N, La Thangue NB. Histone deacetylase inhibitors: gathering pace. Curr Opin Pharmacol 2006; 6:369–375 [View Article][PubMed]
    [Google Scholar]
  9. Xu WS, Parmigiani RB, Marks PA. Histone deacetylase inhibitors: molecular mechanisms of action. Oncogene 2007; 26:5541–5552 [View Article][PubMed]
    [Google Scholar]
  10. Yang XJ, Seto E. The Rpd3/Hda1 family of lysine deacetylases: from bacteria and yeast to mice and men. Nat Rev Mol Cell Biol 2008; 9:206–218 [View Article][PubMed]
    [Google Scholar]
  11. Vaquero A, Sternglanz R, Reinberg D. NAD+-dependent deacetylation of H4 lysine 16 by class III HDACs. Oncogene 2007; 26:5505–5520 [View Article][PubMed]
    [Google Scholar]
  12. Yang XJ, Grégoire S. Class II histone deacetylases: from sequence to function, regulation, and clinical implication. Mol Cell Biol 2005; 25:2873–2884 [View Article][PubMed]
    [Google Scholar]
  13. Bertos NR, Gilquin B, Chan GK, Yen TJ, Khochbin S et al. Role of the tetradecapeptide repeat domain of human histone deacetylase 6 in cytoplasmic retention. J Biol Chem 2004; 279:48246–48254 [View Article][PubMed]
    [Google Scholar]
  14. Haggarty SJ, Koeller KM, Wong JC, Grozinger CM, Schreiber SL. Domain-selective small-molecule inhibitor of histone deacetylase 6 (HDAC6)-mediated tubulin deacetylation. Proc Natl Acad Sci USA 2003; 100:4389–4394 [View Article][PubMed]
    [Google Scholar]
  15. Zhang Y, Gilquin B, Khochbin S, Matthias P. Two catalytic domains are required for protein deacetylation. J Biol Chem 2006; 281:2401–2404 [View Article][PubMed]
    [Google Scholar]
  16. Zou H, Wu Y, Navre M, Sang BC. Characterization of the two catalytic domains in histone deacetylase 6. Biochem Biophys Res Commun 2006; 341:45–50 [View Article][PubMed]
    [Google Scholar]
  17. Hai Y, Christianson DW. Histone deacetylase 6 structure and molecular basis of catalysis and inhibition. Nat Chem Biol 2016; 12:741–747 [View Article][PubMed]
    [Google Scholar]
  18. Miyake Y, Keusch JJ, Wang L, Saito M, Hess D et al. Structural insights into HDAC6 tubulin deacetylation and its selective inhibition. Nat Chem Biol 2016; 12:748–754 [View Article][PubMed]
    [Google Scholar]
  19. Ouyang H, Ali YO, Ravichandran M, Dong A, Qiu W et al. Protein aggregates are recruited to aggresome by histone deacetylase 6 via unanchored ubiquitin C termini. J Biol Chem 2012; 287:2317–2327 [View Article][PubMed]
    [Google Scholar]
  20. Kawaguchi Y, Kovacs JJ, McLaurin A, Vance JM, Ito A et al. The deacetylase HDAC6 regulates aggresome formation and cell viability in response to misfolded protein stress. Cell 2003; 115:727–738[PubMed] [Crossref]
    [Google Scholar]
  21. Lee JY, Koga H, Kawaguchi Y, Tang W, Wong E et al. HDAC6 controls autophagosome maturation essential for ubiquitin-selective quality-control autophagy. EMBO J 2010; 29:969–980 [View Article][PubMed]
    [Google Scholar]
  22. Hubbert C, Guardiola A, Shao R, Kawaguchi Y, Ito A et al. HDAC6 is a microtubule-associated deacetylase. Nature 2002; 417:455–458 [View Article][PubMed]
    [Google Scholar]
  23. Matsuyama A, Shimazu T, Sumida Y, Saito A, Yoshimatsu Y et al. In vivo destabilization of dynamic microtubules by HDAC6-mediated deacetylation. EMBO J 2002; 21:6820–6831[PubMed] [Crossref]
    [Google Scholar]
  24. Zhang X, Yuan Z, Zhang Y, Yong S, Salas-Burgos A et al. HDAC6 modulates cell motility by altering the acetylation level of cortactin. Mol Cell 2007; 27:197–213 [View Article][PubMed]
    [Google Scholar]
  25. Ageta-Ishihara N, Miyata T, Ohshima C, Watanabe M, Sato Y et al. Septins promote dendrite and axon development by negatively regulating microtubule stability via HDAC6-mediated deacetylation. Nat Commun 2013; 4:2532 [Crossref]
    [Google Scholar]
  26. Kovacs JJ, Murphy PJ, Gaillard S, Zhao X, Wu JT et al. HDAC6 regulates Hsp90 acetylation and chaperone-dependent activation of glucocorticoid receptor. Mol Cell 2005; 18:601–607 [View Article][PubMed]
    [Google Scholar]
  27. Krämer OH, Mahboobi S, Sellmer A. Drugging the HDAC6-HSP90 interplay in malignant cells. Trends Pharmacol Sci 2014; 35:501–509 [View Article][PubMed]
    [Google Scholar]
  28. Zhang L, Liu S, Liu N, Zhang Y, Liu M et al. Proteomic identification and functional characterization of MYH9, Hsc70, and DNAJA1 as novel substrates of HDAC6 deacetylase activity. Protein Cell 2015; 6:42–54 [View Article][PubMed]
    [Google Scholar]
  29. Seigneurin-Berny D, Verdel A, Curtet S, Lemercier C, Garin J et al. Identification of components of the murine histone deacetylase 6 complex: link between acetylation and ubiquitination signaling pathways. Mol Cell Biol 2001; 21:8035–8044 [View Article][PubMed]
    [Google Scholar]
  30. Vij N. AAA ATPase p97/VCP: cellular functions, disease and therapeutic potential. J Cell Mol Med 2008; 12:2511–2518 [View Article][PubMed]
    [Google Scholar]
  31. Wójcik C, Yano M, DeMartino GN. RNA interference of valosin-containing protein (VCP/p97) reveals multiple cellular roles linked to ubiquitin/proteasome-dependent proteolysis. J Cell Sci 2004; 117:281–292 [View Article][PubMed]
    [Google Scholar]
  32. Boyault C, Gilquin B, Zhang Y, Rybin V, Garman E et al. HDAC6-p97/VCP controlled polyubiquitin chain turnover. EMBO J 2006; 25:3357–3366 [View Article][PubMed]
    [Google Scholar]
  33. Chen S, Owens GC, Makarenkova H, Edelman DB. HDAC6 regulates mitochondrial transport in hippocampal neurons. PLoS One 2010; 5:e10848 [View Article][PubMed]
    [Google Scholar]
  34. Williams KA, Zhang M, Xiang S, Hu C, Wu JY et al. Extracellular signal-regulated kinase (ERK) phosphorylates histone deacetylase 6 (HDAC6) at serine 1035 to stimulate cell migration. J Biol Chem 2013; 288:33156–33170 [Crossref]
    [Google Scholar]
  35. Lafarga V, Aymerich I, Tapia O, Mayor F Jr, Penela P. A novel GRK2/HDAC6 interaction modulates cell spreading and motility. EMBO J 2012; 31:856–869 [View Article][PubMed]
    [Google Scholar]
  36. Penela P, Lafarga V, Tapia O, Rivas V, Nogués L et al. Roles of GRK2 in cell signaling beyond GPCR desensitization: GRK2-HDAC6 interaction modulates cell spreading and motility. Sci Signal 2012; 5: [View Article][PubMed]
    [Google Scholar]
  37. Pugacheva EN, Jablonski SA, Hartman TR, Henske EP, Golemis EA. HEF1-dependent Aurora A activation induces disassembly of the primary cilium. Cell 2007; 129:1351–1363 [View Article][PubMed]
    [Google Scholar]
  38. Du Y, Seibenhener ML, Yan J, Jiang J, Wooten MC. aPKC phosphorylation of HDAC6 results in increased deacetylation activity. PLoS One 2015; 10:e0123191 [View Article][PubMed]
    [Google Scholar]
  39. Watabe M, Nakaki T. Protein kinase CK2 regulates the formation and clearance of aggresomes in response to stress. J Cell Sci 2011; 124:1519–1532 [View Article][PubMed]
    [Google Scholar]
  40. Zhu J, Coyne CB, Sarkar SN. PKC alpha regulates Sendai virus-mediated interferon induction through HDAC6 and β-catenin. EMBO J 2011; 30:4838–4849 [View Article][PubMed]
    [Google Scholar]
  41. Han Y, Jeong HM, Jin YH, Kim YJ, Jeong HG et al. Acetylation of histone deacetylase 6 by p300 attenuates its deacetylase activity. Biochem Biophys Res Commun 2009; 383:88–92 [View Article][PubMed]
    [Google Scholar]
  42. Liu Y, Peng L, Seto E, Huang S, Qiu Y. Modulation of histone deacetylase 6 (HDAC6) nuclear import and tubulin deacetylase activity through acetylation. J Biol Chem 2012; 287:29168–29174 [View Article][PubMed]
    [Google Scholar]
  43. Acevedo K, Li R, Soo P, Suryadinata R, Sarcevic B et al. The phosphorylation of p25/TPPP by LIM kinase 1 inhibits its ability to assemble microtubules. Exp Cell Res 2007; 313:4091–4106 [View Article][PubMed]
    [Google Scholar]
  44. Tokési N, Lehotzky A, Horváth I, Szabó B, Oláh J et al. TPPP/p25 promotes tubulin acetylation by inhibiting histone deacetylase 6. J Biol Chem 2010; 285:17896–17906 [View Article][PubMed]
    [Google Scholar]
  45. Schofield AV, Gamell C, Bernard O. Tubulin polymerization promoting protein 1 (TPPP1) increases β-catenin expression through inhibition of HDAC6 activity in U2OS osteosarcoma cells. Biochem Biophys Res Commun 2013; 436:571–577 [View Article][PubMed]
    [Google Scholar]
  46. Schofield AV, Steel R, Bernard O. Rho-associated coiled-coil kinase (ROCK) protein controls microtubule dynamics in a novel signaling pathway that regulates cell migration. J Biol Chem 2012; 287:43620–43629 [View Article][PubMed]
    [Google Scholar]
  47. Schofield AV, Gamell C, Suryadinata R, Sarcevic B, Bernard O. Tubulin polymerization promoting protein 1 (Tppp1) phosphorylation by Rho-associated coiled-coil kinase (rock) and cyclin-dependent kinase 1 (Cdk1) inhibits microtubule dynamics to increase cell proliferation. J Biol Chem 2013; 288:7907–7917 [View Article][PubMed]
    [Google Scholar]
  48. Deakin NO, Turner CE. Paxillin inhibits HDAC6 to regulate microtubule acetylation, Golgi structure, and polarized migration. J Cell Biol 2014; 206:395–413 [View Article][PubMed]
    [Google Scholar]
  49. Wickström SA, Masoumi KC, Khochbin S, Fässler R, Massoumi R. CYLD negatively regulates cell-cycle progression by inactivating HDAC6 and increasing the levels of acetylated tubulin. EMBO J 2010; 29:131–144 [View Article][PubMed]
    [Google Scholar]
  50. Yang Y, Ran J, Liu M, Li D, Li Y et al. CYLD mediates ciliogenesis in multiple organs by deubiquitinating Cep70 and inactivating HDAC6. Cell Res 2014; 24:1342–1353 [View Article][PubMed]
    [Google Scholar]
  51. Di Fulvio S, Azakir BA, Therrien C, Sinnreich M. Dysferlin interacts with histone deacetylase 6 and increases alpha-tubulin acetylation. PLoS One 2011; 6:e28563 [View Article][PubMed]
    [Google Scholar]
  52. Tala, Sun X, Chen J, Zhang L, Liu N et al. Microtubule stabilization by Mdp3 is partially attributed to its modulation of HDAC6 in addition to its association with tubulin and microtubules. PLoS One 2014; 9:e90932 [View Article][PubMed]
    [Google Scholar]
  53. Yan J, Seibenhener ML, Calderilla-Barbosa L, Diaz-Meco MT, Moscat J et al. SQSTM1/p62 interacts with HDAC6 and regulates deacetylase activity. PLoS One 2013; 8:e76016 [View Article][PubMed]
    [Google Scholar]
  54. Salemi LM, Almawi AW, Lefebvre KJ, Schild-Poulter C. Aggresome formation is regulated by RanBPM through an interaction with HDAC6. Biol Open 2014; 3:418–430 [View Article][PubMed]
    [Google Scholar]
  55. Lee SW, Yang J, Kim SY, Jeong HK, Lee J et al. MicroRNA-26a induced by hypoxia targets HDAC6 in myogenic differentiation of embryonic stem cells. Nucleic Acids Res 2015; 43:2057–2073 [View Article][PubMed]
    [Google Scholar]
  56. Simon D, Laloo B, Barillot M, Barnetche T, Blanchard C et al. A mutation in the 3'-UTR of the HDAC6 gene abolishing the post-transcriptional regulation mediated by hsa-miR-433 is linked to a new form of dominant X-linked chondrodysplasia. Hum Mol Genet 2010; 19:2015–2027 [View Article][PubMed]
    [Google Scholar]
  57. Huang S, Wang S, Bian C, Yang Z, Zhou H et al. Upregulation of miR-22 promotes osteogenic differentiation and inhibits adipogenic differentiation of human adipose tissue-derived mesenchymal stem cells by repressing HDAC6 protein expression. Stem Cells Dev 2012; 21:2531–2540 [View Article][PubMed]
    [Google Scholar]
  58. Lwin T, Zhao X, Cheng F, Zhang X, Huang A et al. A microenvironment-mediated c-Myc/miR-548m/HDAC6 amplification loop in non-Hodgkin B cell lymphomas. J Clin Invest 2013; 123:4612–4626 [Crossref]
    [Google Scholar]
  59. Bae HJ, Jung KH, Eun JW, Shen Q, Kim HS et al. MicroRNA-221 governs tumor suppressor HDAC6 to potentiate malignant progression of liver cancer. J Hepatol 2015; 63:408–419 [View Article][PubMed]
    [Google Scholar]
  60. Wang XC, Ma Y, Meng PS, Han JL, Yu HY et al. miR-433 inhibits oral squamous cell carcinoma (OSCC) cell growth and metastasis by targeting HDAC6. Oral Oncol 2015; 51:674–682 [View Article][PubMed]
    [Google Scholar]
  61. Radtke K, Döhner K, Sodeik B. Viral interactions with the cytoskeleton: a hitchhiker's guide to the cell. Cell Microbiol 2006; 8:387–400 [View Article][PubMed]
    [Google Scholar]
  62. Brice A, Moseley GW. Viral interactions with microtubules: orchestrators of host cell biology?. Future Virol 2013; 8:229–243 [View Article]
    [Google Scholar]
  63. McDonald D, Vodicka MA, Lucero G, Svitkina TM, Borisy GG et al. Visualization of the intracellular behavior of HIV in living cells. J Cell Biol 2002; 159:441–452 [View Article][PubMed]
    [Google Scholar]
  64. Haedicke J, de Los Santos K, Goff SP, Naghavi MH. The Ezrin-radixin-moesin family member ezrin regulates stable microtubule formation and retroviral infection. J Virol 2008; 82:4665–4670 [View Article][PubMed]
    [Google Scholar]
  65. Perdiz D, Mackeh R, Poüs C, Baillet A. The ins and outs of tubulin acetylation: more than just a post-translational modification?. Cell Signal 2011; 23:763–771 [View Article][PubMed]
    [Google Scholar]
  66. Xuan C, Qiao W, Gao J, Liu M, Zhang X et al. Regulation of microtubule assembly and stability by the transactivator of transcription protein of Jembrana disease virus. J Biol Chem 2007; 282:28800–28806 [View Article][PubMed]
    [Google Scholar]
  67. Kannan H, Fan S, Patel D, Bossis I, Zhang YJ. The hepatitis E virus open reading frame 3 product interacts with microtubules and interferes with their dynamics. J Virol 2009; 83:6375–6382 [View Article][PubMed]
    [Google Scholar]
  68. Husain M, Harrod KS. Enhanced acetylation of alpha-tubulin in influenza A virus infected epithelial cells. FEBS Lett 2011; 585:128–132 [View Article][PubMed]
    [Google Scholar]
  69. Wadsworth P. Regional regulation of microtubule dynamics in polarized, motile cells. Cell Motil Cytoskeleton 1999; 42:48–59 [View Article][PubMed]
    [Google Scholar]
  70. Valenzuela-Fernández A, Alvarez S, Gordon-Alonso M, Barrero M, Ursa A et al. Histone deacetylase 6 regulates human immunodeficiency virus type 1 infection. Mol Biol Cell 2005; 16:5445–5454 [View Article][PubMed]
    [Google Scholar]
  71. Malinowsky K, Luksza J, Dittmar MT. Susceptibility to virus-cell fusion at the plasma membrane is reduced through expression of HIV gp41 cytoplasmic domains. Virology 2008; 376:69–78 [View Article][PubMed]
    [Google Scholar]
  72. Zheng K, Kitazato K, Wang Y. Viruses exploit the function of epidermal growth factor receptor. Rev Med Virol 2014; 24:274–286 [View Article][PubMed]
    [Google Scholar]
  73. Gao YS, Hubbert CC, Lu J, Lee YS, Lee JY et al. Histone deacetylase 6 regulates growth factor-induced actin remodeling and endocytosis. Mol Cell Biol 2007; 27:8637–8647 [View Article][PubMed]
    [Google Scholar]
  74. Rey M, Irondelle M, Waharte F, Lizarraga F, Chavrier P. HDAC6 is required for invadopodia activity and invasion by breast tumor cells. Eur J Cell Biol 2011; 90:128–135 [View Article][PubMed]
    [Google Scholar]
  75. Wang D, Meng Q, Huo L, Yang M, Wang L et al. Overexpression of Hdac6 enhances resistance to virus infection in embryonic stem cells and in mice. Protein Cell 2015; 6:152–156 [View Article][PubMed]
    [Google Scholar]
  76. Naranatt PP, Krishnan HH, Smith MS, Chandran B. Kaposi's sarcoma-associated herpesvirus modulates microtubule dynamics via RhoA-GTP-diaphanous 2 signaling and utilizes the dynein motors to deliver its DNA to the nucleus. J Virol 2005; 79:1191–1206 [View Article][PubMed]
    [Google Scholar]
  77. Frampton AR Jr, Uchida H, von Einem J, Goins WF, Grandi P et al. Equine herpesvirus type 1 (EHV-1) utilizes microtubules, dynein, and ROCK1 to productively infect cells. Vet Microbiol 2010; 141:12–21 [View Article][PubMed]
    [Google Scholar]
  78. Sabo Y, Walsh D, Barry DS, Tinaztepe S, de Los Santos K et al. HIV-1 induces the formation of stable microtubules to enhance early infection. Cell Host Microbe 2013; 14:535–546 [View Article][PubMed]
    [Google Scholar]
  79. Lucera MB, Tilton CA, Mao H, Dobrowolski C, Tabler CO et al. The histone deacetylase inhibitor vorinostat (SAHA) increases the susceptibility of uninfected CD4+ T cells to HIV by increasing the kinetics and efficiency of postentry viral events. J Virol 2014; 88:10803–10812 [View Article][PubMed]
    [Google Scholar]
  80. Cao J, Lin C, Wang H, Wang L, Zhou N et al. Circovirus transport proceeds via direct interaction of the cytoplasmic dynein IC1 subunit with the viral capsid protein. J Virol 2015; 89:2777–2791 [View Article][PubMed]
    [Google Scholar]
  81. Elliott G, O'Hare P. Herpes simplex virus type 1 tegument protein VP22 induces the stabilization and hyperacetylation of microtubules. J Virol 1998; 72:6448–6455[PubMed]
    [Google Scholar]
  82. Hyde JL, Gillespie LK, Mackenzie JM. Mouse norovirus 1 utilizes the cytoskeleton network to establish localization of the replication complex proximal to the microtubule organizing center. J Virol 2012; 86:4110–4122 [View Article][PubMed]
    [Google Scholar]
  83. Warren JC, Rutkowski A, Cassimeris L. Infection with replication-deficient adenovirus induces changes in the dynamic instability of host cell microtubules. Mol Biol Cell 2006; 17:3557–3568 [View Article][PubMed]
    [Google Scholar]
  84. Cody JJ, Markert JM, Hurst DR. Histone deacetylase inhibitors improve the replication of oncolytic herpes simplex virus in breast cancer cells. PLoS One 2014; 9:e92919 [View Article][PubMed]
    [Google Scholar]
  85. Nakashima H, Kaufmann JK, Wang PY, Nguyen T, Speranza MC et al. Histone deacetylase 6 inhibition enhances oncolytic viral replication in glioma. J Clin Invest 2015; 125:4269–4280 [View Article][PubMed]
    [Google Scholar]
  86. Huo L, Li D, Sun X, Shi X, Karna P et al. Regulation of Tat acetylation and transactivation activity by the microtubule-associated deacetylase HDAC6. J Biol Chem 2011; 286:9280–9286 [View Article][PubMed]
    [Google Scholar]
  87. Mosley AJ, Meekings KN, McCarthy C, Shepherd D, Cerundolo V et al. Histone deacetylase inhibitors increase virus gene expression but decrease CD8+ cell antiviral function in HTLV-1 infection. Blood 2006; 108:3801–3807 [View Article][PubMed]
    [Google Scholar]
  88. Jouvenet N, Monaghan P, Way M, Wileman T. Transport of African swine fever virus from assembly sites to the plasma membrane is dependent on microtubules and conventional kinesin. J Virol 2004; 78:7990–8001 [View Article][PubMed]
    [Google Scholar]
  89. Dodding MP, Way M. Coupling viruses to dynein and kinesin-1. EMBO J 2011; 30:3527–3539 [View Article][PubMed]
    [Google Scholar]
  90. Husain M, Cheung CY. Histone deacetylase 6 inhibits influenza A virus release by downregulating the trafficking of viral components to the plasma membrane via its substrate, acetylated microtubules. J Virol 2014; 88:11229–11239 [View Article][PubMed]
    [Google Scholar]
  91. Husain M, Harrod KS. Influenza A virus-induced caspase-3 cleaves the histone deacetylase 6 in infected epithelial cells. FEBS Lett 2009; 583:2517–2520 [View Article][PubMed]
    [Google Scholar]
  92. Chen DY, Husain M. Caspase-mediated degradation of host cortactin that promotes influenza A virus infection in epithelial cells. Virology 2016; 497:146–156 [View Article][PubMed]
    [Google Scholar]
  93. Taylor MP, Koyuncu OO, Enquist LW. Subversion of the actin cytoskeleton during viral infection. Nat Rev Microbiol 2011; 9:427–439 [View Article][PubMed]
    [Google Scholar]
  94. Shahriari S, Gordon J, Ghildyal R. Host cytoskeleton in respiratory syncytial virus assembly and budding. Virol J 2016; 13:161 [View Article][PubMed]
    [Google Scholar]
  95. Husain M, Gupta CM. Interactions of viral matrix protein nucleoprotein with the host cell cytoskeletal actin in influenza viral infection. Curr Sci 1997; 73:40–47
    [Google Scholar]
  96. Liu G, Xiang Y, Guo C, Pei Y, Wang Y et al. Cofilin-1 is involved in regulation of actin reorganization during influenza A virus assembly and budding. Biochem Biophys Res Commun 2014; 453:821–825 [View Article][PubMed]
    [Google Scholar]
  97. Roberts KL, Manicassamy B, Lamb RA. Influenza A virus uses intercellular connections to spread to neighboring cells. J Virol 2015; 89:1537–1549 [View Article][PubMed]
    [Google Scholar]
  98. Geller R, Taguwa S, Frydman J. Broad action of Hsp90 as a host chaperone required for viral replication. BBA-Mol Cell Res 2011; 1823:698–706 [View Article]
    [Google Scholar]
  99. Panella S, Marcocci ME, Celestino I, Valente S, Zwergel C et al. MC1568 inhibits HDAC6/8 activity and influenza A virus replication in lung epithelial cells: role of Hsp90 acetylation. Future Med Chem 2016; 8:2017–2031 [View Article]
    [Google Scholar]
  100. Serrador JM, Cabrero JR, Sancho D, Mittelbrunn M, Urzainqui A et al. HDAC6 deacetylase activity links the tubulin cytoskeleton with immune synapse organization. Immunity 2004; 20:417–428[PubMed] [Crossref]
    [Google Scholar]
  101. Takeuchi O, Akira S. Innate immunity to virus infection. Immunol Rev 2009; 227:75–86 [View Article][PubMed]
    [Google Scholar]
  102. Nusinzon I, Horvath CM. Unexpected roles for deacetylation in interferon- and cytokine-induced transcription. J Interferon Cytokine Res 2005; 25:745–748 [View Article][PubMed]
    [Google Scholar]
  103. Nusinzon I, Horvath CM. Positive and negative regulation of the innate antiviral response and beta interferon gene expression by deacetylation. Mol Cell Biol 2006; 26:3106–3113 [View Article][PubMed]
    [Google Scholar]
  104. Chattopadhyay S, Fensterl V, Zhang Y, Veleeparambil M, Wetzel JL et al. Inhibition of viral pathogenesis and promotion of the septic shock response to bacterial infection by IRF-3 are regulated by the acetylation and phosphorylation of its coactivators. MBio 2013; 4:e00636-12 [View Article][PubMed]
    [Google Scholar]
  105. Choi SJ, Lee HC, Kim JH, Park SY, Kim TH et al. HDAC6 regulates cellular viral RNA sensing by deacetylation of RIG-I. EMBO J 2016; 35:429–442 [View Article][PubMed]
    [Google Scholar]
  106. Liu HM, Jiang F, Loo YM, Hsu S, Hsiang TY et al. Regulation of retinoic acid inducible gene-I (RIG-I) activation by the histone deacetylase 6. EBioMedicine 2016; 9:195–206 [View Article][PubMed]
    [Google Scholar]
  107. Faure M, Lafont F. Pathogen-induced autophagy signaling in innate immunity. J Innate Immun 2013; 5:456–470 [View Article][PubMed]
    [Google Scholar]
  108. Richetta C, Faure M. Autophagy in antiviral innate immunity. Cell Microbiol 2013; 15:368–376 [View Article][PubMed]
    [Google Scholar]
  109. Valera MS, de Armas-Rillo L, Barroso-González J, Ziglio S, Batisse J et al. The HDAC6/APOBEC3G complex regulates HIV-1 infectiveness by inducing Vif autophagic degradation. Retrovirology 2015; 12:53 [View Article][PubMed]
    [Google Scholar]
  110. Marin M, Rose KM, Kozak SL, Kabat D. HIV-1 Vif protein binds the editing enzyme APOBEC3G and induces its degradation. Nat Med 2003; 9:1398–1403 [View Article][PubMed]
    [Google Scholar]
  111. Yu X, Yu Y, Liu B, Luo K, Kong W et al. Induction of APOBEC3G ubiquitination and degradation by an HIV-1 Vif-Cul5-SCF complex. Science 2003; 302:1056–1060 [View Article][PubMed]
    [Google Scholar]
  112. Nakashima H, Nguyen T, Goins WF, Chiocca EA. Interferon-stimulated gene 15 (ISG15) and ISG15-linked proteins can associate with members of the selective autophagic process, histone deacetylase 6 (HDAC6) and SQSTM1/p62. J Biol Chem 2015; 290:1485–1495 [View Article][PubMed]
    [Google Scholar]
  113. Durfee LA, Lyon N, Seo K, Huibregtse JM. The ISG15 conjugation system broadly targets newly synthesized proteins: implications for the antiviral function of ISG15. Mol Cell 2010; 38:722–732 [View Article][PubMed]
    [Google Scholar]
  114. Rajsbaum R, García-Sastre A. Viral evasion mechanisms of early antiviral responses involving regulation of ubiquitin pathways. Trends Microbiol 2013; 21:421–429 [Crossref]
    [Google Scholar]
  115. Lazaro E, Kadie C, Stamegna P, Zhang SC, Gourdain P et al. Variable HIV peptide stability in human cytosol is critical to epitope presentation and immune escape. J Clin Invest 2011; 121:2480–2492 [View Article][PubMed]
    [Google Scholar]
  116. Núñez-Andrade N, Iborra S, Trullo A, Moreno-Gonzalo O, Calvo E et al. HDAC6 regulates the dynamics of lytic granules in cytotoxic T lymphocytes. J Cell Sci 2016; 129:1305–1311 [View Article][PubMed]
    [Google Scholar]
  117. Chin LS, Olzmann JA, Li L. Parkin-mediated ubiquitin signalling in aggresome formation and autophagy. Biochem Soc Trans 2010; 38:144–149 [View Article][PubMed]
    [Google Scholar]
  118. Wileman T. Aggresomes and pericentriolar sites of virus assembly: cellular defense or viral design?. Annu Rev Microbiol 2007; 61:149–167 [View Article][PubMed]
    [Google Scholar]
  119. Wileman T. Aggresomes and autophagy generate sites for virus replication. Science 2006; 312:875–878 [View Article][PubMed]
    [Google Scholar]
  120. Moshe A, Gorovits R. Virus-induced aggregates in infected cells. Viruses 2012; 4:2218–2232 [View Article][PubMed]
    [Google Scholar]
  121. Bondzi C, Brunner AM, Munyikwa MR, Connor CD, Simmons AN et al. Recruitment of the oncoprotein v-ErbA to aggresomes. Mol Cell Endocrinol 2011; 332:196–212 [View Article][PubMed]
    [Google Scholar]
  122. Park R, Wang'ondu R, Heston L, Shedd D, Miller G. Efficient induction of nuclear aggresomes by specific single missense mutations in the DNA-binding domain of a viral AP-1 homolog. J Biol Chem 2011; 286:9748–9762 [View Article][PubMed]
    [Google Scholar]
  123. Banerjee I, Miyake Y, Nobs SP, Schneider C, Horvath P et al. Influenza A virus uses the aggresome processing machinery for host cell entry. Science 2014; 346:473–477 [View Article][PubMed]
    [Google Scholar]
  124. Hao R, Nanduri P, Rao Y, Panichelli RS, Ito A et al. Proteasomes activate aggresome disassembly and clearance by producing unanchored ubiquitin chains. Mol Cell 2013; 51:819–828 [View Article][PubMed]
    [Google Scholar]
  125. Santos S, Obukhov Y, Nekhai S, Bukrinsky M, Iordanskiy S. Virus-producing cells determine the host protein profiles of HIV-1 virion cores. Retrovirology 2012; 9:65 [View Article][PubMed]
    [Google Scholar]
  126. Scherer M, Reuter N, Wagenknecht N, Otto V, Sticht H et al. Small ubiquitin-related modifier (SUMO) pathway-mediated enhancement of human cytomegalovirus replication correlates with a recruitment of SUMO-1/3 proteins to viral replication compartments. J Gen Virol 2013; 94:1373–1384 [Crossref]
    [Google Scholar]
  127. Sette P, Nagashima K, Piper RC, Bouamr F. Ubiquitin conjugation to Gag is essential for ESCRT-mediated HIV-1 budding. Retrovirology 2013; 10:79 [Crossref]
    [Google Scholar]
  128. Amor S, Peferoen LA, Vogel DY, Breur M, van der Valk P et al. Inflammation in neurodegenerative diseases—an update. Immunology 2014; 142:151–166 [View Article][PubMed]
    [Google Scholar]
  129. Felice C, Lewis A, Armuzzi A, Lindsay JO, Silver A. Review article: selective histone deacetylase isoforms as potential therapeutic targets in inflammatory bowel diseases. Aliment Pharmacol Ther 2015; 41:26–38 [View Article][PubMed]
    [Google Scholar]
  130. Yan B, Xie S, Liu Z, Ran J, Li Y et al. HDAC6 deacetylase activity is critical for lipopolysaccharide-induced activation of macrophages. PLoS One 2014; 9:e110718 [View Article][PubMed]
    [Google Scholar]
  131. Youn GS, Ju SM, Choi SY, Park J. HDAC6 mediates HIV-1 tat-induced proinflammatory responses by regulating MAPK-NF-kappaB/AP-1 pathways in astrocytes. Glia 2015; 63:1953–1965 [View Article]
    [Google Scholar]
  132. Hara N, Alkanani AK, Dinarello CA, Zipris D. Histone deacetylase inhibitor suppresses virus-induced proinflammatory responses and type 1 diabetes. J Mol Med (Berl) 2014; 92:93–102 [View Article][PubMed]
    [Google Scholar]
  133. Kozlov MV, Kleymenova AA, Romanova LI, Konduktorov KA, Smirnova OA et al. Benzohydroxamic acids as potent and selective anti-HCV agents. Bioorg Med Chem Lett 2013; 23:5936–5940 [Crossref]
    [Google Scholar]
  134. Kozlov MV, Kleymenova AA, Konduktorov KA, Malikova AZ, Kochetkov SN. Selective inhibitor of histone deacetylase 6 (tubastatin A) suppresses proliferation of hepatitis C virus replicon in culture of human hepatocytes. Biochemistry (Mosc) 2014; 79:637–642 [View Article][PubMed]
    [Google Scholar]
  135. Kozlov MV, Kleymenova AA, Romanova LI, Konduktorov KA, Kamarova KA et al. Pyridine hydroxamic acids are specific anti-HCV agents affecting HDAC6. Bioorg Med Chem Lett 2015; 25:2382–2385 [View Article][PubMed]
    [Google Scholar]
  136. Ai T, Xu Y, Qiu L, Geraghty RJ, Chen L. Hydroxamic acids block replication of hepatitis C virus. J Med Chem 2015; 58:785–800 [View Article][PubMed]
    [Google Scholar]
  137. Miura K, Taura K, Kodama Y, Schnabl B, Brenner DA. Hepatitis C virus-induced oxidative stress suppresses hepcidin expression through increased histone deacetylase activity. Hepatology 2008; 48:1420–1429 [View Article][PubMed]
    [Google Scholar]
  138. van Opdenbosch N, Favoreel H, Van de Walle GR. Histone modifications in herpesvirus infections. Biol Cell 2012; 104:139–164 [View Article][PubMed]
    [Google Scholar]
  139. Hsieh YH, Su IJ, Yen CJ, Tsai TF, Tsai HW et al. Histone deacetylase inhibitor suberoylanilide hydroxamic acid suppresses the pro-oncogenic effects induced by hepatitis B virus pre-S2 mutant oncoprotein and represents a potential chemopreventive agent in high-risk chronic HBV patients. Carcinogenesis 2013; 34:475–485 [Crossref]
    [Google Scholar]
  140. Shirakawa K, Chavez L, Hakre S, Calvanese V, Verdin E. Reactivation of latent HIV by histone deacetylase inhibitors. Trends Microbiol 2013; 21:277–285 [Crossref]
    [Google Scholar]
  141. Huber K, Doyon G, Plaks J, Fyne E, Mellors JW et al. Inhibitors of histone deacetylases: correlation between isoform specificity and reactivation of HIV type 1 (HIV-1) from latently infected cells. J Biol Chem 2011; 286:22211–22218 [View Article][PubMed]
    [Google Scholar]
  142. Matalon S, Rasmussen TA, Dinarello CA. Histone deacetylase inhibitors for purging HIV-1 from the latent reservoir. Mol Med 2011; 17:466–472 [View Article][PubMed]
    [Google Scholar]
  143. Barton KM, Archin NM, Keedy KS, Espeseth AS, Zhang YL et al. Selective HDAC inhibition for the disruption of latent HIV-1 infection. PLoS One 2014; 9:e102684 [View Article][PubMed]
    [Google Scholar]
  144. Manson McManamy ME, Hakre S, Verdin EM, Margolis DM. Therapy for latent HIV-1 infection: the role of histone deacetylase inhibitors. Antivir Chem Chemother 2014; 23:145–149 [View Article][PubMed]
    [Google Scholar]
  145. Ye J, Gradoville L, Daigle D, Miller G. De novo protein synthesis is required for lytic cycle reactivation of Epstein-Barr virus, but not Kaposi's sarcoma-associated herpesvirus, in response to histone deacetylase inhibitors and protein kinase C agonists. J Virol 2007; 81:9279–9291 [View Article][PubMed]
    [Google Scholar]
  146. Ghosh SK, Perrine SP, Williams RM, Faller DV. Histone deacetylase inhibitors are potent inducers of gene expression in latent EBV and sensitize lymphoma cells to nucleoside antiviral agents. Blood 2012; 119:1008–1017 [View Article][PubMed]
    [Google Scholar]
  147. Murata T, Kondo Y, Sugimoto A, Kawashima D, Saito S et al. Epigenetic histone modification of Epstein-Barr virus BZLF1 promoter during latency and reactivation in Raji cells. J Virol 2012; 86:4752–4761 [View Article][PubMed]
    [Google Scholar]
  148. Renne R, Zhong W, Herndier B, McGrath M, Abbey N et al. Lytic growth of Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) in culture. Nat Med 1996; 2:342–346[PubMed] [Crossref]
    [Google Scholar]
  149. Shin HJ, DeCotiis J, Giron M, Palmeri D, Lukac DM. Histone deacetylase classes I and II regulate Kaposi's sarcoma-associated herpesvirus reactivation. J Virol 2014; 88:1281–1292 [View Article][PubMed]
    [Google Scholar]
  150. McDonnel SJ, Liepnieks ML, Murphy BG. Treatment of chronically FIV-infected cats with suberoylanilide hydroxamic acid. Antiviral Res 2014; 108:74–78 [View Article][PubMed]
    [Google Scholar]
  151. Karn J. The molecular biology of HIV latency: breaking and restoring the Tat-dependent transcriptional circuit. Curr Opin HIV AIDS 2011; 6:4–11 [View Article][PubMed]
    [Google Scholar]
  152. Westendorf JJ, Zaidi SK, Cascino JE, Kahler R, van Wijnen AJ et al. Runx2 (Cbfa1, AML-3) interacts with histone deacetylase 6 and represses the p21(CIP1/WAF1) promoter. Mol Cell Biol 2002; 22:7982–7992[PubMed] [Crossref]
    [Google Scholar]
  153. Chou CW, Chen CC. HDAC inhibition upregulates the expression of angiostatic ADAMTS1. FEBS Lett 2008; 582:4059–4065 [View Article][PubMed]
    [Google Scholar]
  154. Wang Z, Zang C, Cui K, Schones DE, Barski A et al. Genome-wide mapping of HATs and HDACs reveals distinct functions in active and inactive genes. Cell 2009; 138:1019–1031 [View Article][PubMed]
    [Google Scholar]
  155. Subramanian C, Jarzembowski JA, Opipari AW Jr, Castle VP, Kwok RP. HDAC6 deacetylates Ku70 and regulates Ku70-Bax binding in neuroblastoma. Neoplasia 2011; 13:726–734[PubMed] [Crossref]
    [Google Scholar]
  156. Gao YS, Hubbert CC, Yao TP. The microtubule-associated histone deacetylase 6 (HDAC6) regulates epidermal growth factor receptor (EGFR) endocytic trafficking and degradation. J Biol Chem 2010; 285:11219–11226 [View Article][PubMed]
    [Google Scholar]
  157. Parmigiani RB, Xu WS, Venta-Perez G, Erdjument-Bromage H, Yaneva M et al. HDAC6 is a specific deacetylase of peroxiredoxins and is involved in redox regulation. Proc Natl Acad Sci USA 2008; 105:9633–9638 [View Article][PubMed]
    [Google Scholar]
  158. Riolo MT, Cooper ZA, Holloway MP, Cheng Y, Bianchi C et al. Histone deacetylase 6 (HDAC6) deacetylates survivin for its nuclear export in breast cancer. J Biol Chem 2012; 287:10885–10893 [View Article][PubMed]
    [Google Scholar]
  159. Chang YW, Tseng CF, Wang MY, Chang WC, Lee CC et al. Deacetylation of HSPA5 by HDAC6 leads to GP78-mediated HSPA5 ubiquitination at K447 and suppresses metastasis of breast cancer. Oncogene 2016; 35:1517–1528 [View Article][PubMed]
    [Google Scholar]
  160. Medler TR, Craig JM, Fiorillo AA, Feeney YB, Harrell JC et al. HDAC6 deacetylates HMGN2 to regulate Stat5a activity and breast cancer growth. Mol Cancer Res 2016; 14:994–1008 [View Article][PubMed]
    [Google Scholar]
  161. Nakka KK, Chaudhary N, Joshi S, Bhat J, Singh K et al. Nuclear matrix-associated protein SMAR1 regulates alternative splicing via HDAC6-mediated deacetylation of Sam68. Proc Natl Acad Sci USA 2015; 112:E3374E3383 [View Article][PubMed]
    [Google Scholar]
  162. Mortenson JB, Heppler LN, Banks CJ, Weerasekara VK, Whited MD et al. Histone deacetylase 6 (HDAC6) promotes the pro-survival activity of 14-3-3ζ via deacetylation of lysines within the 14-3-3ζ binding pocket. J Biol Chem 2015; 290:12487–12496 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000679
Loading
/content/journal/jgv/10.1099/jgv.0.000679
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error