Depletion of the insulator protein CTCF results in herpes simplex virus 1 reactivation in vivo

Journal of Virology

Volumn 92, Issue 11, 2018, Pages

  Washington, Shannan D ^a   Edenfield, Samantha I ^a   Lieux, Caroline ^a   Watson, Zachary L ^b   Taasan, Sean M ^b   Dhummakupt, Adit ^b   Bloom, David C ^b   Neumann, Donna M ^a,c  

^a LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^c LSU EYE CENTER   (United States)

Author keywords

AAV8; Chromatin; CTCF; Epigenetics; Gene delivery; HSV 1; HSV 1 reactivation; In vivo reactivation; Insulator; Rabbit ocular

Indexed keywords

ADENOVIRUS VECTOR; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR CTCF; CTCF PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING SITE; CONTROLLED STUDY; DNA BINDING; GENE TARGETING; HUMAN ALPHAHERPESVIRUS 1; IN VIVO STUDY; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; TRIGEMINUS GANGLION; VIRUS LATENCY; VIRUS REACTIVATION; 3T3 CELL LINE; ANIMAL; CHEMISTRY; CORNEA; DISEASE MODEL; GANGLION; GENE KNOCKOUT; GENETICS; HERPES SIMPLEX; LEPORIDAE; METABOLISM; PHYSIOLOGY; PROCEDURES; VIROLOGY; VIRUS ACTIVATION; VIRUS GENOME; VIRUS SHEDDING;

3T3 CELLS; ANIMALS; BINDING SITES; CCCTC-BINDING FACTOR; CORNEA; DISEASE MODELS, ANIMAL; GANGLIA; GENE KNOCKOUT TECHNIQUES; GENOME, VIRAL; HERPES SIMPLEX; HERPESVIRUS 1, HUMAN; MICE; RABBITS; VIRUS ACTIVATION; VIRUS LATENCY; VIRUS SHEDDING;

EID: 85046884862     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00173-18     Document Type: Article

References (40)

1. Croen KD, Ostrove JM, Dragovic LJ, Smialek JE, Straus SE. 1987. Latent herpes simplex virus in human trigeminal ganglia. Detection of an immediate early gene "anti-sense" transcript by in situ hybridization. N Engl J Med 317:1427-1432
2. Austin A, Lietman T, Rose-Nussbaumer J. 2017. Update on the management of infectious keratitis. Ophthalmology 124:1678-1689. https://doi.org/10.1016/j.ophtha.2017.05.012
3. Stevens JG, Wagner EK, Devi-Rao GB, Cook ML, Feldman LT. 1987. RNA complementary to a herpesvirus alpha gene mRNA is prominent in latently infected neurons. Science 235:1056-1059. https://doi.org/10.1126/science.2434993
4. Deshmane SL, Fraser NW. 1989. During latency, herpes simplex virus type 1 DNA is associated with nucleosomes in a chromatin structure. J Virol 63:943-947
5. Kubat NJ, Amelio AL, Giordani NV, Bloom DC. 2004. The herpes simplex virus type 1 latency-associated transcript (LAT) enhancer/rcr is hyperacetylated during latency independently of LAT transcription. J Virol 78:12508-12518. https://doi.org/10.1128/JVI.78.22.12508-12518.2004
6. Kubat NJ, Tran RK, McAnany P, Bloom DC. 2004. Specific histone tail modification and not DNA methylation is a determinant of HSV-1 latent gene expression. J Virol 78:1139-1149. https://doi.org/10.1128/JVI.78.3.1139-1149.2004
7. Neumann DM, Bhattacharjee PS, Giordani NV, Bloom DC, Hill JM. 2007. In vivo changes in the patterns of chromatin structure associated with the latent herpes simplex virus type 1 genome in mouse trigeminal ganglia can be detected at early times after butyrate treatment. J Virol 81:13248-13253. https://doi.org/10.1128/JVI.01569-07
8. Wang QY, Zhou C, Johnson KE, Colgrove RC, Coen DM, Knipe DM. 2005. Herpesviral latency-associated transcript gene promotes assembly of heterochromatin on viral lytic-gene promoters in latent infection. Proc Natl Acad Sci U S A 102:16055-16059. https://doi.org/10.1073/pnas.0505850102
9. Kristie TM, Liang Y, Vogel JL. 2010. Control of alpha-herpesvirus IE gene expression by HCF-1 coupled chromatin modification activities. Biochim Biophys Acta 1799:257-265. https://doi.org/10.1016/j.bbagrm.2009.08.003
10. Kwiatkowski DL, Thompson HW, Bloom DC. 2009. The polycomb group protein Bmi1 binds to the herpes simplex virus 1 latent genome and maintains repressive histone marks during latency. J Virol 83:8173-8181. https://doi.org/10.1128/JVI.00686-09
11. Cliffe AR, Garber DA, Knipe DM. 2009. Transcription of the herpes simplex virus latency-associated transcript promotes the formation of facultative heterochromatin on lytic promoters. J Virol 83:8182-8190. https://doi.org/10.1128/JVI.00712-09
12. Creech CC, Neumann DM. 2010. Changes to euchromatin on LAT and ICP4 following reactivation are more prevalent in an efficiently reactivating strain of HSV-1. PLoS One 5:e15416. https://doi.org/10.1371/journal.pone.0015416
13. Amelio AL, Giordani NV, Kubat NJ, O'Neil J, Bloom DC. 2006. Deacetylation of the herpes simples virus type 1 latency-associated transcript (LAT) enhancer and a decrease in LAT abundance precede an increase in ICP0 transcriptional permissiveness at early times postexplant. J Virol 80:2063-2068. https://doi.org/10.1128/JVI.80.4.2063-2068.2006
14. Amelio AL, McAnany PK, Bloom DC. 2006. A chromatin insulator-like element in the herpes simplex virus type 1 latency-associated transcript region binds CCCTC-binding factor and displays enhancer-blocking and silencing activities. J Virol 80:2358-2368. https://doi.org/10.1128/JVI.80.5.2358-2368.2006
15. Chen Q, Lin L, Smith S, Huang J, Berger SL, Zhou J. 2007. CTCF-dependent chromatin boundary element between the latency-associated transcript and ICP0 promoters in the herpes simplex virus type 1 genome. J Virol 81: 5192-5201. https://doi.org/10.1128/JVI.02447-06
16. West AG, Gaszner M, Felsenfeld G. 2002. Insulators: many functions, many mechanisms. Genes Dev 16:271-288. https://doi.org/10.1101/gad.954702
17. Ghirlando R, Felsenfeld G. 2016. CTCF: making the right connections. Genes Dev 30:881-891. https://doi.org/10.1101/gad.277863.116
18. Paris C, Pentland I, Groves I, Roberts DC, Powis SJ, Coleman N, Roberts S, Parish JL. 2015. CCCTC-binding factor recruitment to the early region of the human papillomavirus 18 genome regulates viral oncogene expression. J Virol 89:4770-4785. https://doi.org/10.1128/JVI.00097-15
19. Martinez FP, Cruz R, Lu F, Plasschaert R, Deng Z, Rivera-Molina YA, Bartolomei MS, Lieberman PM, Tang Q. 2014. CTCF binding to the first intron of the major immediate early (MIE) gene of human cytomegalovirus (HCMV) negatively regulates MIE gene expression and HCMV replication. J Virol 88:7389-7401. https://doi.org/10.1128/JVI.00845-14
20. Kang H, Lieberman PM. 2009. Cell cycle control of Kaposi's sarcomaassociated herpesvirus latency transcription by CTCF-cohesin interactions. J Virol 83:6199-6210. https://doi.org/10.1128/JVI.00052-09
21. Tempera I, Klichinsky M, Lieberman PM. 2011. EBV latency types adopt alternative chromatin conformations. PLoS Pathog 7:e1002180. https://doi.org/10.1371/journal.ppat.1002180
22. Ertel MK, Cammarata AL, Hron RJ, Neumann DM. 2012. CTCF occupation of the HSV-1 genome is disrupted at early times post-reactivation in a transcription-dependent manner. J Virol 86:12741-12759. https://doi.org/10.1128/JVI.01655-12
23. Hirata RK, Russell DW. 2000. Design and packaging of adeno-associated virus gene targeting vectors. J Virol 74:4612-4620. https://doi.org/10.1128/JVI.74.10.4612-4620.2000
24. Lovric J, Mano M, Zentilin L, Eulalio A, Zacchigna S, Giacca M. 2012. Terminal differentiation of cardiac and skeletal myocytes induces permissivity to AAV transduction by relieving inhibition imposed by DNA damage response proteins. Mol Ther 20:2087-2097. https://doi.org/10.1038/mt.2012.144
25. McCarty DM, Fu H, Monahan PE, Toulson CE, Naik P, Samulski RJ. 2003. Adeno-associated virus terminal repeat (TR) mutant generates selfcomplementary vectors to overcome the rate-limiting step to transduction in vivo. Gene Ther 10:2112-2118. https://doi.org/10.1038/sj.gt.3302134
26. McCarty DM, Monahan PE, Samulski RJ. 2001. Self-complementary recombinant adeno-associated virus (scAAV) vectors promote efficient transduction independently of DNA synthesis. Gene Ther 8:1248-1254. https://doi.org/10.1038/sj.gt.3301514
27. Watson ZL, Ertel MK, Lewin AS, Tuli SS, Schultz GS, Neumann DM, Bloom DC. 2016. Adeno-associated virus vectors efficiently transduce mouse and rabbit sensory neurons coinfected with herpes simplex virus 1 following peripheral inoculation. J Virol 90:7894-7901. https://doi.org/10.1128/JVI.01028-16
28. Bloom DC, Lewin AS, Neumann DM, Watson ZL, Tuli SS, Schultz GS. 2017. Method for delivering RNA to neurons to treat herpes infections. USWO Patent 2017/223248 A1
29. Kim KK, Adelstein RS, Kawamoto S. 2009. Identification of neuronal nuclei (NeuN) as Fox-3, a new member of the Fox-1 gene family of splicing factors. J Biol Chem 284:31052-31061. https://doi.org/10.1074/jbc.M109.052969
30. Estrada FS, Hernandez VS, Medina MP, Corona-Morales AA, Gonzalez-Perez O, Vega-Gonzalez A, Zhang L. 2009. Astrogliosis is temporally correlated with enhanced neurogenesis in adult rat hippocampus fol-lowing a glucoprivic insult. Neurosci Lett 459:109-114. https://doi.org/10.1016/j.neulet.2009.05.016
31. Ahn HC, Yoo KY, Hwang IK, Cho JH, Lee CH, Choi JH, Li H, Cho BR, Kim YM, Won MH. 2009. Ischemia-related changes in naive and mutant forms of ubiquitin and neuroprotective effects of ubiquitin in the hippocampus following experimental transient ischemic damage. Exp Neurol 220:120-132. https://doi.org/10.1016/j.expneurol.2009.07.031
32. Goodman T, Trouche S, Massou I, Verret L, Zerwas M, Roullet P, Rampon C. 2010. Young hippocampal neurons are critical for recent and remote spatial memory in adult mice. Neuroscience 171:769-778. https://doi.org/10.1016/j.neuroscience.2010.09.047
33. Sams DS, Nardone S, Getselter D, Raz D, Tal M, Rayi PR, Kaphzan H, Hakim O, Elliott E. 2016. Neuronal CTCF is necessary for basal and experience-dependent gene regulation, memory formation, and genomic structure of BDNF and Arc. Cell Rep 17:2418-2430. https://doi.org/10.1016/j.celrep.2016.11.004
34. Marsman J, O'Neill AC, Kao BR-Y, Rhodes JM, Meier M, Antony J, Mönnich M, Horsfield JA. 2014. Cohesin and CTCF differentially regulate spatiotemporal runx1 expression during zebrafish development. Biochim Biophys Acta 1839:50-61. https://doi.org/10.1016/j.bbagrm.2013.11.007
35. Lee JS, Raja P, Pan D, Pesola JM, Coen DM, Knipe DM. 2018. CCCTCbinding factor acts as a heterochromatin barrier on herpes simplex viral latent chromatin and contributes to poised latent infection. mBio 9:e02372-17. https://doi.org/10.1128/mBio.02372-17
36. Mineur YS, Taylor SR, Picciotto MR. 2014. Calcineurin downregulation in the amygdala is sufficient to induce anxiety-like and depression-like behaviors in C57BL/6J male mice. Biol Psychiatry 75:991-998. https://doi.org/10.1016/j.biopsych.2014.03.009
37. Li DJ, Verma D, Mosbruger T, Swaminathan S. 2014. CTCF and Rad21 act as host cell restriction factors for Kaposi's sarcoma-associated herpesvirus (KSHV) lytic replication by modulating viral gene transcription. PLoS Pathog 10:e1003880. https://doi.org/10.1371/journal.ppat.1003880
38. Hill JM, O'Callaghan RJ, Hobden JA. 1993. Ocular iontophoresis, p 331-354. In Mitra AK (ed), Ophthalmic drug delivery systems. Marcel Dekker, Inc, New York, NY
39. Hill JM, Shimomura Y, Kwon BS, Gangarosa LP, Sr. 1985. Iontophoresis of epinephrine isomers to rabbit eyes induced HSV-1 ocular shedding. Invest Ophthalmol Vis Sci 26:1299-1303
40. Washington SD, Musarrat F, Ertel MK, Backes GL, Neumann DM. 2018. CTCF binding sites in the herpes simplex virus 1 genome display sitespecific CTCF occupation, protein recruitment, and insulator function. J Virol 92:e00156-18. https://doi.org/10.1128/JVI.00156-18