HSV-1 Genome Subnuclear Positioning and Associations with Host-Cell PML-NBs and Centromeres Regulate LAT Locus Transcription during Latency in Neurons

PLoS Pathogens

Volumn 8, Issue 8, 2012, Pages

  Catez, Frédéric ^a,b,h   Picard, Christel ^c   Held, Kathrin ^d   Gross, Sylvain ^a,b,e   Rousseau, Antoine ^c   Theil, Diethilde ^d,i   Sawtell, Nancy ^f   Labetoulle, Marc ^c,g   Lomonte, Patrick ^a,b,e  

^a CENTRE DE GÉNÉTIQUE MOLÉCULAIRE ET CELLULAIRE   (France)

^b UNIVERSITÉ LYON 1   (France)

^c CNRS   (France)

^d UNIVERSITY OF MUNICH   (Germany)

^e Laboratoire d'excellence   (France)

^f CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^g BICÊTRE HOSPITAL   (France)

^h CENTRE DE RECHERCHE EN CANCÉROLOGIE DE LYON   (France)

ⁱ NOVARTIS PHARMA AG   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ATRX PROTEIN; DAXX PROTEIN; INTERFERON; LATENCY ASSOCIATED PEPTIDE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL NUCLEUS INCLUSION BODY; CENTROMERE; CONTROLLED STUDY; COPY NUMBER VARIATION; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; GENE LOCUS; GENETIC ASSOCIATION; GENETIC TRANSCRIPTION; HERPES SIMPLEX VIRUS 1; HOST CELL; IMAGE RECONSTRUCTION; MOUSE; NONHUMAN; PROMYELOCYTIC LEUKEMIA; PROTEIN DOMAIN; SENSORY NERVE CELL; THREE DIMENSIONAL IMAGING; VIRUS CELL INTERACTION; VIRUS GENOME; VIRUS LATENCY;

ANIMALS; CARRIER PROTEINS; CELLS, CULTURED; CENTROMERE; DNA HELICASES; GENE EXPRESSION REGULATION, VIRAL; GENETIC LOCI; GENOME, VIRAL; HERPES SIMPLEX; HERPESVIRUS 1, HUMAN; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; NUCLEAR PROTEINS; RABBITS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEINS; VIRUS LATENCY;

HUMAN HERPESVIRUS 1; MUS;

EID: 84866174976     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002852     Document Type: Article

References (109)

1. Roizman B, Knipe D, Whitley R (2007) Herpes Simplex Viruses. In: Fields Virology, 5th edition. Knipe D, Howley P, editors. Philadelphia: Lippincott Williams and Wilkins. 2501-2602.
2. Knipe DM, Cliffe A, (2008) Chromatin control of herpes simplex virus lytic and latent infection. Nat Rev Microbiol 6: 211-221.
3. Bloom DC, Giordani NV, Kwiatkowski DL, (2010) Epigenetic regulation of latent HSV-1 gene expression. Biochim Biophys Acta 1799: 246-256.
4. Maillet S, Naas T, Crepin S, Roque-Afonso AM, Lafay F, et al. (2006) Herpes simplex virus type 1 latently infected neurons differentially express latency-associated and ICP0 transcripts. J Virol 80: 9310-9321.
5. Kramer MF, Coen DM, (1995) Quantification of transcripts from the ICP4 and thymidine kinase genes in mouse ganglia latently infected with herpes simplex virus. J Virol 69: 1389-1399.
6. Chen SH, Kramer MF, Schaffer PA, Coen DM, (1997) A viral function represses accumulation of transcripts from productive-cycle genes in mouse ganglia latently infected with herpes simplex virus. J Virol 71: 5878-5884.
7. 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.
8. Zwaagstra J, Ghiasi H, Nesburn AB, Wechsler SL, (1989) In vitro promoter activity associated with the latency-associated transcript gene of herpes simplex virus type 1. J Gen Virol 70: 2163-2169.
9. Farrell MJ, Dobson AT, Feldman LT, (1991) Herpes simplex virus latency-associated transcript is a stable intron. Proc Natl Acad Sci U S A 88: 790-794.
10. Umbach JL, Kramer MF, Jurak I, Karnowski HW, Coen DM, et al. (2008) MicroRNAs expressed by herpes simplex virus 1 during latent infection regulate viral mRNAs. Nature 454: 780-783.
11. Jurak I, Kramer MF, Mellor JC, van Lint AL, Roth FP, et al. (2010) Numerous conserved and divergent microRNAs expressed by herpes simplex viruses 1 and 2. J Virol 84: 4659-4672.
12. Gordon YJ, Romanowski EG, Araullo-Cruz T, Kinchington PR, (1995) The proportion of trigeminal ganglionic neurons expressing herpes simplex virus type 1 latency-associated transcripts correlates to reactivation in the New Zealand rabbit ocular model. Graefes Arch Clin Exp Ophthalmol 233: 649-654.
13. Thompson RL, Sawtell NM, (1997) The herpes simplex virus type 1 latency-associated transcript gene regulates the establishment of latency. J Virol 71: 5432-5440.
14. Sawtell NM, (1998) The probability of in vivo reactivation of herpes simplex virus type 1 increases with the number of latently infected neurons in the ganglia. J Virol 72: 6888-6892.
15. Thompson RL, Sawtell NM, (2001) Herpes simplex virus type 1 latency-associated transcript gene promotes neuronal survival. J Virol 75: 6660-6675.
16. Branco FJ, Fraser NW, (2005) Herpes simplex virus type 1 latency-associated transcript expression protects trigeminal ganglion neurons from apoptosis. J Virol 79: 9019-9025.
17. Carpenter D, Hsiang C, Brown DJ, Jin L, Osorio N, et al. (2007) Stable cell lines expressing high levels of the herpes simplex virus type 1 LAT are refractory to caspase 3 activation and DNA laddering following cold shock induced apoptosis. Virology 369: 12-18.
18. Mehta A, Maggioncalda J, Bagasra O, Thikkavarapu S, Saikumari P, et al. (1995) In situ DNA PCR and RNA hybridization detection of herpes simplex virus sequences in trigeminal ganglia of latently infected mice. Virology 206: 633-640.
19. Sawtell NM, (1997) Comprehensive quantification of herpes simplex virus latency at the single-cell level. J Virol 71: 5423-5431.
20. Sawtell NM, Poon DK, Tansky CS, Thompson RL, (1998) The latent herpes simplex virus type 1 genome copy number in individual neurons is virus strain specific and correlates with reactivation. J Virol 72: 5343-5350.
21. Chen X-P, Mata M, Kelley M, Glorioso JC, Fink DJ, (2002) The relationship of herpes simplex virus latency associated transcript expression to genome copy number: a quantitative study using laser capture microdissection. J Neurovirol 8: 204-210.
22. Proenca JT, Coleman HM, Connor V, Winton DJ, Efstathiou S, (2008) A historical analysis of herpes simplex virus promoter activation in vivo reveals distinct populations of latently infected neurones. J Gen Virol 89: 2965-2974.
23. Proenca JT, Coleman HM, Nicoll MP, Connor V, Preston CM, et al. (2011) An investigation of HSV promoter activity compatible with latency establishment reveals VP16 independent activation of HSV immediate early promoters in sensory neurones. J Gen Virol 92: 2575-2585.
24. Wang K, Lau TY, Morales M, Mont EK, Straus SE, (2005) Laser-capture microdissection: refining estimates of the quantity and distribution of latent herpes simplex virus 1 and varicella-zoster virus DNA in human trigeminal Ganglia at the single-cell level. J Virol 79: 14079-14087.
25. Misteli T, (2005) Concepts in nuclear architecture. Bioessays 27: 477-487.
26. Sexton T, Schober H, Fraser P, Gasser SM, (2007) Gene regulation through nuclear organization. Nat Struct Mol Biol 14: 1049-1055.
27. Baxter J, Merkenschlager M, Fisher AG, (2002) Nuclear organisation and gene expression. Curr Opin Cell Biol 14: 372-376.
28. Spector DL, (2003) The dynamics of chromosome organization and gene regulation. Annu Rev Biochem 72: 573-608.
29. Francastel C, Schubeler D, Martin DI, Groudine M, (2000) Nuclear compartmentalization and gene activity. Nat Rev Mol Cell Biol 1: 137-143.
30. Georgopoulos K, (2002) Haematopoietic cell-fate decisions, chromatin regulation and ikaros. Nat Rev Immunol 2: 162-174.
31. Fisher AG, Merkenschlager M, (2002) Gene silencing, cell fate and nuclear organisation. Curr Opin Genet Dev 12: 193-197.
32. Ching RW, Dellaire G, Eskiw CH, Bazett-Jones DP, (2005) PML bodies: a meeting place for genomic loci? J Cell Sci 118: 847-854.
33. Bernardi R, Pandolfi PP, (2007) Structure, dynamics and functions of promyelocytic leukaemia nuclear bodies. Nat Rev Mol Cell Biol 8: 1006-1016.
34. Zhao R, Bodnar MS, Spector DL, (2009) Nuclear neighborhoods and gene expression. Curr Opin Genet Dev 19: 172-179.
35. Dellaire G, Bazett-Jones DP, (2004) PML nuclear bodies: dynamic sensors of DNA damage and cellular stress. Bioessays 26: 963-977.
36. Lallemand-Breitenbach V, de Thé H, (2010) PML nuclear bodies. Cold Spring Harb Perspect Biol 2: a000661.
37. Wang J, Shiels C, Sasieni P, Wu PJ, Islam SA, et al. (2004) Promyelocytic leukemia nuclear bodies associate with transcriptionally active genomic regions. J Cell Biol 164: 515-526.
38. Xie SQ, Pombo A, (2006) Distribution of different phosphorylated forms of RNA polymerase II in relation to Cajal and PML bodies in human cells: an ultrastructural study. Histochem Cell Biol 125: 21-31.
39. Zhong S, Salomoni P, Pandolfi PP, (2000) The transcriptional role of PML and the nuclear body. Nat Cell Biol 2: E85-E90.
40. Garrick D, Samara V, McDowell TL, Smith AJH, Dobbie L, et al. (2004) A conserved truncated isoform of the ATR-X syndrome protein lacking the SWI/SNF-homology domain. Gene 326: 23-34.
41. Everett RD, Chelbi-Alix MK, (2007) PML and PML nuclear bodies: implications in antiviral defence. Biochimie 89: 819-830.
42. Bishop CL, Ramalho M, Nadkarni N, May Kong W, Higgins CF, et al. (2006) Role for centromeric heterochromatin and PML nuclear bodies in the cellular response to foreign DNA. Mol Cel Biol 26: 2583-2594.
43. Ishov AM, Maul GG, (1996) The periphery of nuclear domain 10 (ND10) as site of DNA virus deposition. J Cell Biol 134: 815-826.
44. Maul GG, Ishov AM, Everett RD, (1996) Nuclear domain 10 as preexisting potential replication start sites of herpes simplex virus type-1. Virology 217: 67-75.
45. Sourvinos G, Everett RD, (2002) Visualization of parental HSV-1 genomes and replication compartments in association with ND10 in live infected cells. EMBO J 21: 4989-4997.
46. Tang Q, Li L, Ishov AM, Revol V, Epstein AL, et al. (2003) Determination of minimum herpes simplex virus type 1 components necessary to localize transcriptionally active DNA to ND10. J Virol 77: 5821-5828.
47. Fraefel C, Bittermann AG, Bueler H, Heid I, Bachi T, et al. (2004) Spatial and temporal organization of adeno-associated virus DNA replication in live cells. J Virol 78: 389-398.
48. Everett RD, Murray J, (2005) ND10 components relocate to sites associated with herpes simplex virus type 1 nucleoprotein complexes during virus infection. J Virol 79: 5078-5089.
49. Everett RD, (2006) Interactions between DNA viruses, ND10 and the DNA damage response. Cell Microbiol 8: 365-374.
50. Everett RD, Murray J, Orr A, Preston CM, (2007) Herpes simplex virus type 1 genomes are associated with ND10 nuclear substructures in quiescently infected human fibroblasts. J Virol 81: 10991-11004.
51. Wagner EK, Bloom DC, (1997) Experimental investigation of herpes simplex virus latency. Clin Microbiol Rev 10: 419-43.
52. Labetoulle M, Kucera P, Ugolini G, Lafay F, Frau E, et al. (2000) Neuronal propagation of HSV1 from the oral mucosa to the eye. Invest Ophthalmol Vis Sci 41: 2600-2606.
53. Guenatri M, Bailly D, Maison C, Almouzni G, (2004) Mouse centric and pericentric satellite repeats form distinct functional heterochromatin. J Cell Biol 166: 493-505.
54. Kalitsis P, Fowler KJ, Earle E, Griffiths B, Howman E, et al. (2003) Partially functional Cenpa-GFP fusion protein causes increased chromosome missegregation and apoptosis during mouse embryogenesis. Chromosome Res 11: 345-357.
55. Boisvert FM, Hendzel MJ, Bazett-Jones DP, (2000) Promyelocytic leukemia (PML) nuclear bodies are protein structures that do not accumulate RNA. J Cell Biol 148: 283-292.
56. Everett RD, Sourvinos G, Leiper C, Clements JB, Orr A, (2004) Formation of nuclear foci of the herpes simplex virus type 1 regulatory protein ICP4 at early times of infection: localization, dynamics, recruitment of ICP27, and evidence for the de novo induction of ND10-like complexes. J Virol 78: 1903-1917.
57. Cuchet-Lourenço D, Boutell C, Lukashchuk V, Grant K, Sykes A, et al. (2011) SUMO Pathway Dependent Recruitment of Cellular Repressors to Herpes Simplex Virus Type 1 Genomes. PLoS Pathog 7: e1002123.
58. Arthur J, Efstathiou S, Simmons A, (1993) Intranuclear foci containing low abundance herpes simplex virus latency-associated transcripts visualized by non-isotopic in situ hybridization. J Gen Virol 74 (Pt 7): 1363-1370.
59. Camarena V, Kobayashi M, Kim JY, Roehm P, Perez R, et al. (2010) Nature and duration of growth factor signaling through receptor tyrosine kinases regulates HSV-1 latency in neurons. Cell Host Microbe 8: 320-330.
60. Everett RD, Rechter S, Papior P, Tavalai N, Stamminger T, et al. (2006) PML contributes to a cellular mechanism of repression of herpes simplex virus type 1 infection that is inactivated by ICP0. J Virol 80: 7995-8005.
61. Everett RD, Parada C, Gripon P, Sirma H, Orr A, (2008) Replication of ICP0-null mutant herpes simplex virus type 1 is restricted by both PML and Sp100. J Virol 82: 2661-2672.
62. Lukashchuk V, Everett RD, (2010) Regulation of ICP0-null mutant herpes simplex virus type 1 infection by ND10 components ATRX and hDaxx. J Virol 84: 4026-4040.
63. Boutell C, Cuchet-Lourenço D, Vanni E, Orr A, Glass M, et al. (2011) A Viral Ubiquitin Ligase Has Substrate Preferential SUMO Targeted Ubiquitin Ligase Activity that Counteracts Intrinsic Antiviral Defence. PLoS Pathog 7: e1002245.
64. Weidtkamp-Peters S, Lenser T, Negorev D, Gerstner N, Hofmann TG, et al. (2008) Dynamics of component exchange at PML nuclear bodies. J Cell Sci 121: 2731-2743.
65. Luciani JJ, Depetris D, Usson Y, Metzler-Guillemain C, Mignon-Ravix C, et al. (2006) PML nuclear bodies are highly organised DNA-protein structures with a function in heterochromatin remodelling at the G2 phase. J Cell Sci 119: 2518-2531.
66. Lang M, Jegou T, Chung I, Richter K, Münch S, et al. (2010) Three-dimensional organization of promyelocytic leukemia nuclear bodies. J Cell Sci 123: 392-400.
67. Francastel C, Walters MC, Groudine M, Martin DI, (1999) A functional enhancer suppresses silencing of a transgene and prevents its localization close to centrometric heterochromatin. Cell 99: 259-269.
68. Francastel C, Magis W, Groudine M, (2001) Nuclear relocation of a transactivator subunit precedes target gene activation. Proc Natl Acad Sci U S A 98: 12120-12125.
69. Brown KE, Guest SS, Smale ST, Hahm K, Merkenschlager M, et al. (1997) Association of transcriptionally silent genes with Ikaros complexes at centromeric heterochromatin. Cell 91: 845-854.
70. Brown KE, Baxter J, Graf D, Merkenschlager M, Fisher AG, (1999) Dynamic repositioning of genes in the nucleus of lymphocytes preparing for cell division. Mol Cell 3: 207-217.
71. Schubeler D, Francastel C, Cimbora DM, Reik A, Martin DI, et al. (2000) Nuclear localization and histone acetylation: a pathway for chromatin opening and transcriptional activation of the human beta-globin locus. Gen Dev 14: 940-950.
72. Brown KE, Amoils S, Horn JM, Buckle VJ, Higgs DR, et al. (2001) Expression of alpha- and beta-globin genes occurs within different nuclear domains in haemopoietic cells. Nat Cell Biol 3: 602-606.
73. Merkenschlager M, Amoils S, Roldan E, Rahemtulla A, O'Connor E, et al. (2004) Centromeric repositioning of coreceptor loci predicts their stable silencing and the CD4/CD8 lineage choice. J Exp Med 200: 1437-1444.
74. Terranova R, Sauer S, Merkenschlager M, Fisher AG, (2005) The reorganisation of constitutive heterochromatin in differentiating muscle requires HDAC activity. Exp Cell Res 310: 344-356.
75. Guasconi V, Pritchard L-L, Fritsch L, Mesner LD, Francastel C, et al. (2010) Preferential association of irreversibly silenced E2F-target genes with pericentromeric heterochromatin in differentiated muscle cells. Epigenetics 5: 704-709.
76. Pluta AF, Earnshaw WC, Goldberg IG, (1998) Interphase-specific association of intrinsic centromere protein CENP-C with HDaxx, a death domain-binding protein implicated in Fas-mediated cell death. J Cell Sci 111 (Pt 14): 2029-2041.
77. Boutell C, Sadis S, Everett RD, (2002) Herpes simplex virus type 1 immediate-early protein ICP0 and is isolated RING finger domain act as ubiquitin E3 ligases in vitro. J Virol 76: 841-50.
78. Everett RD, Earnshaw WC, Findlay J, Lomonte P, (1999) Specific destruction of kinetochore protein CENP-C and disruption of cell division by herpes simplex virus immediate-early protein Vmw110. EMBO J 18: 1526-38.
79. Lomonte P, Sullivan KF, Everett RD, (2000) Degradation of Nucleosome-associated Centromeric Histone H3-like Protein CENP-A Induced by Herpes Simplex Virus Type 1 Protein ICP0. J Biol Chem 276: 5829-5835.
80. Lomonte P, Morency E, (2007) Centromeric protein CENP-B proteasomal degradation induced by the viral protein ICP0. FEBS Lett 581: 658-662.
81. Morency E, Sabra M, Catez F, Texier P, Lomonte P, (2007) A novel cell response triggered by interphase centromere structural instability. J Cell Biol 177: 757-768.
82. Lomonte P, Everett RD, (1999) Herpes simplex virus type 1 immediate-early protein Vmw110 inhibits progression of cells through mitosis and from G(1) into S phase of the cell cycle. J Virol 73: 9456-67.
83. Hobbs WE 2, DeLuca NA, (1999) Perturbation of cell cycle progression and cellular gene expression as a function of herpes simplex virus ICP0. J Virol 73: 8245-55.
84. Schang LM, Rosenberg A, Schaffer PA, (2000) Roscovitine, a specific inhibitor of cellular cyclin-dependent kinases, inhibits herpes simplex virus DNA synthesis in the presence of viral early proteins. J Virol 74: 2107-2120.
85. Everett RD, Orr A, Elliott M, (1991) High level expression and purification of herpes simplex virus type 1 immediate early polypeptide Vmw110. Nucleic Acids Res 19: 6155-61.
86. Russell J, Stow ND, Stow EC, Preston CM, (1987) Herpes simplex virus genes involved in latency in vitro. J Gen Virol 68 (Pt 12): 3009-3018.
87. Harris RA, Everett RD, Zhu XX, Silverstein S, Preston CM, (1989) Herpes simplex virus type 1 immediate-early protein Vmw110 reactivates latent herpes simplex virus type 2 in an in vitro latency system. J Virol 63: 3513-5.
88. Lomonte P, Thomas J, Texier P, Caron C, Khochbin S, et al. (2004) Functional interaction between class II histone deacetylases and ICP0 of herpes simplex virus type 1. J Virol 78: 6744-6757.
89. Everett RD, Boutell C, Orr A, (2004) Phenotype of a herpes simplex virus type 1 mutant that fails to express immediate-early regulatory protein ICP0. J Virol 78: 1763-1774.
90. Gu H, Liang Y, Mandel G, Roizman B, (2005) Components of the REST/CoREST/histone deacetylase repressor complex are disrupted, modified, and translocated in HSV-1-infected cells. Proc Natl Acad Sci U S A 102: 7571-7576.
91. Gu H, Poon AP, Roizman B, (2009) During its nuclear phase the multifunctional regulatory protein ICP0 undergoes proteolytic cleavage characteristic of polyproteins. Proc Natl Acad Sci U S A 106: 19132-19137.
92. Gu H, Roizman B, (2009) Engagement of the lysine-specific demethylase/HDAC1/CoREST/REST complex by herpes simplex virus 1. J Virol 83: 4376-4385.
93. Kalamvoki M, Roizman B, (2010) Circadian CLOCK histone acetyl transferase localizes at ND10 nuclear bodies and enables herpes simplex virus gene expression. Proc Natl Acad Sci U S A 107: 17721-17726.
94. Preston CM, Nicholl MJ, (1997) Repression of gene expression upon infection of cells with herpes simplex virus type 1 mutants impaired for immediate-early protein synthesis. J Virol 71: 7807-13.
95. Halford WP, Schaffer PA, (2001) ICP0 is required for efficient reactivation of herpes simplex virus type 1 from neuronal latency. J Virol 75: 3240-9.
96. Everett RD, Parsy ML, Orr A, (2009) Analysis of the functions of herpes simplex virus type 1 regulatory protein ICP0 that are critical for lytic infection and derepression of quiescent viral genomes. J Virol 83: 4963-4977.
97. Valgardsdottir R, Chiodi I, Giordano M, Rossi A, Bazzini S, et al. (2008) Transcription of Satellite III non-coding RNAs is a general stress response in human cells. Nucleic Acids Res 36: 423-434.
98. Eymery A, Horard B, Atifi-Borel El M, Fourel G, Berger F, et al. (2009) A transcriptomic analysis of human centromeric and pericentric sequences in normal and tumor cells. Nucleic Acids Res 37: 6340-6354.
99. Eymery A, Souchier C, Vourc'h C, Jolly C, (2010) Heat shock factor 1 binds to and transcribes satellite II and III sequences at several pericentromeric regions in heat-shocked cells. Exp Cell Res 316: 1845-1855.
100. Labetoulle M, Maillet S, Efstathiou S, Dezelee S, Frau E, et al. (2003) HSV1 latency sites after inoculation in the lip: assessment of their localization and connections to the eye. Invest Ophthalmol Vis Sci 44: 217-225.
101. Sawtell NM, Thompson RL, (2004) Comparison of herpes simplex virus reactivation in ganglia in vivo and in explants demonstrates quantitative and qualitative differences. J Virol 78: 7784-7794.
102. Wang ZG, Ruggero D, Ronchetti S, Zhong S, Gaboli M, et al. (1998) PML is essential for multiple apoptotic pathways. Nat Genet 20: 266-272.
103. Ikeno M, Grimes B, Okazaki T, Nakano M, Saitoh K, et al. (1998) Construction of YAC-based mammalian artificial chromosomes. Nat Biotechnol 16: 431-439.
104. Cunningham C, Davison AJ, (1993) A cosmid-based system for constructing mutants of herpes simplex virus type 1. Virology 197: 116-124.
105. Solovei I, Grasser F, Lanctôt C, (2007) FISH on Histological Sections. CSH Protoc 2007: pdb.prot4729.
106. Louria-Hayon I, Alsheich-Bartok O, Levav-Cohen Y, Silberman I, Berger M, et al. (2009) E6AP promotes the degradation of the PML tumor suppressor. Cell Death Differ 16: 1156-1166.
107. Arthur JL, Scarpini CG, Connor V, Lachmann RH, Tolkovsky AM, et al. (2001) Herpes simplex virus type 1 promoter activity during latency establishment, maintenance, and reactivation in primary dorsal root neurons in vitro. J Virol 75: 3885-3895.
108. Guenatri M, Bailly D, Maison C, Almouzni G, (2004) Mouse centric and pericentric satellite repeats form distinct functional heterochromatin. J Cell Biol 166: 493-505.
109. Manuelidis L, Borden J, (1988) Reproducible compartmentalization of individual chromosome domains in human CNS cells revealed by in situ hybridization and three-dimensional reconstruction. Chromosoma 96: 397-410.