Transcriptional competence of the integrated HIV-1 provirus at the nuclear periphery

EMBO Journal

Volumn 28, Issue 15, 2009, Pages 2231-2243

  Dieudonné, Mariacarolina ^a   Maiuri, Paolo ^a   Biancotto, Chiara ^b   Knezevich, Anna ^a   Kula, Anna ^a   Lusic, Marina ^a   Marcello, Alessandro ^a  

^a INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

^b FIRC INSTITUTE OF MOLECULAR ONCOLOGY   (Italy)

Author keywords

Chromatin; HIV 1; Latency; Nucleus; Transcription

Indexed keywords

ARTICLE; CELL NUCLEUS; CHROMATIN; CONFORMATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; LYMPHOCYTE; NONHUMAN; PRIORITY JOURNAL; PROVIRUS; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; VIRUS GENOME; VIRUS TRANSCRIPTION;

CELL NUCLEUS; CENTROMERE; CHROMATIN; GENE EXPRESSION REGULATION, VIRAL; HIV-1; HUMANS; JURKAT CELLS; LYMPHOCYTES; MODELS, BIOLOGICAL; PROVIRUSES; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 68249138715     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2009.141     Document Type: Article

References (76)

1. Albanese A, Arosio D, Terreni M, Cereseto A (2008) HIV-1 preintegration complexes selectively target decondensed chromatin in the nuclear periphery. PLoS ONE 3: e2413
2. Andrulis ED, Neiman AM, Zappulla DC, Sternglanz R (1998) Perinuclear localization of chromatin facilitates transcriptional silencing. Nature 394: 592-595
3. Baldini A, Rocchi M, Archidiacono N, Miller OJ, Miller DA (1990) A human alpha satellite DNA subset specific for chromosome 12. Am J Hum Genet 46: 784-788
4. Boireau S, Maiuri P, Basyuk E, de la Mata M, Knezevich A, Pradet-Balade B, Backer V, Kornblihtt A, Marcello A, Bertrand E (2007) The transcriptional cycle of HIV-1 in real-time and live cells. J Cell Biol 179: 291-304
5. Bolzer A, Kreth G, Solovei I, Koehler D, Saracoglu K, Fauth C, Muller S, Eils R, Cremer C, Speicher MR, Cremer T (2005) Three-dimensional maps of all chromosomes in human male fibroblast nuclei and prometaphase rosettes. PLoS Biol 3: e157
6. Branco MR, Branco T, Ramirez F, Pombo A (2008) Changes in chromosome organization during PHA-activation of resting human lymphocytes measured by cryo-FISH. Chromosome Res 16: 413-426
7. Brown KE, Amoils S, Horn JM, Buckle VJ, Higgs DR, Merkenschlager M, Fisher AG (2001) Expression of alpha- and beta-globin genes occurs within different nuclear domains in haemopoietic cells. Nat Cell Biol 3: 602-606
8. 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
9. Brown KE, Guest SS, Smale ST, Hahm K, Merkenschlager M, Fisher AG (1997) Association of transcriptionally silent genes with Ikaros complexes at centromeric heterochromatin. Cell 91: 845-854
10. Casolari JM, Brown CR, Komili S, West J, Hieronymus H, Silver PA (2004) Genome-wide localization of the nuclear transport machinery couples transcriptional status and nuclear organization. Cell 117: 427-439
11. Chambeyron S, Bickmore WA (2004) Chromatin decondensation and nuclear reorganization of the HoxB locus upon induction of transcription. Genes Dev 18: 1119-1130
12. Chuang CH, Carpenter AE, Fuchsova B, Johnson T, de Lanerolle P, Belmont AS (2006) Long-range directional movement of an interphase chromosome site. Curr Biol 16: 825-831
13. Chubb JR, Boyle S, Perry P, Bickmore WA (2002) Chromatin motion is constrained by association with nuclear compartments in human cells. Curr Biol 12: 439-445
14. Cremer T, Cremer M, Dietzel S, Muller S, Solovei I, Fakan S (2006) Chromosome territories - a functional nuclear landscape. Curr Opin Cell Biol 18: 307-316
15. Csink AK, Henikoff S (1996) Genetic modification of heterochromatic association and nuclear organization in Drosophila. Nature 381: 529-531
16. De Marco A, Biancotto C, Knezevich A, Maiuri P, Vardabasso C, Marcello A (2008) Intragenic transcriptional cis-activation of the human immunodeficiency virus 1 does not result in allele-specific inhibition of the endogenous gene. Retrovirology 5: 98
17. Dekker J, Rippe K, Dekker M, Kleckner N (2002) Capturing chromosome conformation. Science 295: 1306-1311
18. Dernburg AF, Broman KW, Fung JC, Marshall WF, Philips J, Agard DA, Sedat JW (1996) Perturbation of nuclear architecture by long-distance chromosome interactions. Cell 85: 745-759
19. Dietzel S, Zolghadr K, Hepperger C, Belmont AS (2004) Differential large-scale chromatin compaction and intranuclear positioning of transcribed versus non-transcribed transgene arrays containing beta-globin regulatory sequences. J Cell Sci 117: 4603-4614
20. Dillon N, Festenstein R (2002) Unravelling heterochromatin: competition between positive and negative factors regulates accessibility. Trends Genet 18: 252-258
21. du Chene I, Basyuk E, Lin YL, Triboulet R, Knezevich A, Chable-Bessia C, Mettling C, Baillat V, Reynes J, Corbeau P, Bertrand E, Marcello A, Emiliani S, Kiernan R, Benkirane M (2007) Suv39H1 and HP1gamma are responsible for chromatin-mediated HIV-1 transcriptional silencing and post-integration latency. EMBO J 26: 424-435
22. Finlan LE, Sproul D, Thomson I, Boyle S, Kerr E, Perry P, Ylstra B, Chubb JR, Bickmore WA (2008) Recruitment to the nuclear periphery can alter expression of genes in human cells. PLoS Genet 4: e1000039
23. Folks TM, Justement J, Kinter A, Dinarello CA, Fauci AS (1987) Cytokine-induced expression of HIV-1 in a chronically infected promonocyte cell line. Science 238: 800-802
24. Fraser P, Bickmore W (2007) Nuclear organization of the genome and the potential for gene regulation. Nature 447: 413-417
25. Gondor A, Rougier C, Ohlsson R (2008) High-resolution circular chromosome conformation capture assay. Nat Protoc 3: 303-313
26. Guelen L, Pagie L, Brasset E, Meuleman W, Faza MB, Talhout W, Eussen BH, de Klein A, Wessels L, de Laat W, van Steensel B (2008) Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature 453: 948-951
27. Han Y, Lin YB, An W, Xu J, Yang HC, O'Connell K, Dordai D, Boeke JD, Siliciano JD, Siliciano RF (2008) Orientation-dependent regulation of integrated HIV-1 expression by host gene transcriptional readthrough. Cell Host Microbe 4: 134-146
28. Hewitt SL, High FA, Reiner SL, Fisher AG, Merkenschlager M (2004) Nuclear repositioning marks the selective exclusion of lineage-inappropriate transcription factor loci during T helper cell differentiation. Eur J Immunol 34: 3604-3613
29. Jackson DA, Iborra FJ, Manders EM, Cook PR (1998) Numbers and organization of RNA polymerases, nascent transcripts, and transcription units in HeLa nuclei. Mol Biol Cell 9: 1523-1536
30. Jordan A, Bisgrove D, Verdin E (2003) HIV reproducibly establishes a latent infection after acute infection of T cells in vitro. EMBO J 22: 1868-1877
31. Jordan A, Defechereux P, Verdin E (2001) The site of HIV-1 integration in the human genome determines basal transcriptional activity and response to Tat transactivation. EMBO J 20: 1726-1738
32. Kao SY, Calman AF, Luciw PA, Peterlin BM (1987) Anti-termination of transcription within the long terminal repeat of HIV-1 by tat gene product. Nature 330: 489-493
33. Kim SH, McQueen PG, Lichtman MK, Shevach EM, Parada LA, Misteli T (2004) Spatial genome organization during T-cell differentiation. Cytogenet Genome Res 105: 292-301
34. Kosak ST, Skok JA, Medina KL, Riblet R, Le Beau MM, Fisher AG, Singh H (2002) Subnuclear compartmentalization of immunoglobulin loci during lymphocyte development. Science 296: 158-162
35. Kumaran RI, Spector DL (2008) A genetic locus targeted to the nuclear periphery in living cells maintains its transcriptional competence. J Cell Biol 180: 51-65
36. Lanctot C, Cheutin T, Cremer M, Cavalli G, Cremer T (2007) Dynamic genome architecture in the nuclear space: regulation of gene expression in three dimensions. Nat Rev Genet 8: 104-115
37. Lassen KG, Bailey JR, Siliciano RF (2004) Analysis of human immunodeficiency virus type 1 transcriptional elongation in resting CD4+ T cells in vivo. J Virol 78: 9105-9114
38. Lenasi T, Contreras X, Peterlin BM (2008) Transcriptional interference antagonizes proviral gene expression to promote HIV latency. Cell Host Microbe 4: 123-133
39. Lomvardas S, Barnea G, Pisapia DJ, Mendelsohn M, Kirkland J, Axel R (2006) Interchromosomal interactions and olfactory receptor choice. Cell 126: 403-413
40. Louvet E, Percipalle P (2009) Transcriptional control of gene expression by actin and myosin. Int Rev Cell Mol Biol 272: 107-147
41. Lusic M, Marcello A, Cereseto A, Giacca M (2003) Regulation of HIV-1 gene expression by histone acetylation and factor recruitment at the LTR promoter. EMBO J 22: 6550-6561
42. Marban C, Suzanne S, Dequiedt F, de Walque S, Redel L, Van Lint C, Aunis D, Rohr O (2007) Recruitment of chromatin-modifying enzymes by CTIP2 promotes HIV-1 transcriptional silencing. EMBO J 26: 412-423
43. Marcello A (2006) Latency: the hidden HIV-1 challenge. Retrovirology 3: 7
44. Marcello A, Lusic M, Pegoraro G, Pellegrini V, Beltram F, Giacca M (2004) Nuclear organization and the control of HIV-1 transcription. Gene 326: 1-11
45. Marcello A, Zoppe M, Giacca M (2001) Multiple modes of transcriptional regulation by the HIV-1 Tat transactivator. IUBMB Life 51: 175-181
46. Marshall WF, Dernburg AF, Harmon B, Agard DA, Sedat JW (1996) Specific interactions of chromatin with the nuclear envelope: positional determination within the nucleus in Drosophila melanogaster. Mol Biol Cell 7: 825-842
47. Martinez AM, Colomb S, Dejardin J, Bantignies F, Cavalli G (2006) Polycomb group-dependent Cyclin A repression in Drosophila. Genes Dev 20: 501-513
48. Mateescu B, Bourachot B, Rachez C, Ogryzko V, Muchardt C (2008) Regulation of an inducible promoter by an HP1beta-HP1gamma switch. EMBO Rep 9: 267-272
49. Merkenschlager M, Amoils S, Roldan E, Rahemtulla A, O'Connor E, Fisher AG, Brown KE (2004) Centromeric repositioning of coreceptor loci predicts their stable silencing and the CD4/CD8 lineage choice. J Exp Med 200: 1437-1444
50. Misteli T (2007) Beyond the sequence: cellular organization of genome function. Cell 128: 787-800
51. Mitchell AR, Gosden JR, Miller DA (1985) A cloned sequence, p82H, of the alphoid repeated DNA family found at the centromeres of all human chromosomes. Chromosoma 92: 369-377
52. Nielsen JA, Hudson LD, Armstrong RC (2002) Nuclear organization in differentiating oligodendrocytes. J Cell Sci 115: 4071-4079
53. Noordermeer D, Branco MR, Splinter E, Klous P, van Ijcken W, Swagemakers S, Koutsourakis M, van der Spek P, Pombo A, de Laat W (2008) Transcription and chromatin organization of a housekeeping gene cluster containing an integrated beta-globin locus control region. PLoS Genet 4: e1000016
54. Osborne CS, Chakalova L, Brown KE, Carter D, Horton A, Debrand E, Goyenechea B, Mitchell JA, Lopes S, Reik W, Fraser P (2004) Active genes dynamically colocalize to shared sites of ongoing transcription. Nat Genet 36: 1065-1071
55. Parada LA, McQueen PG, Misteli T (2004) Tissue-specific spatial organization of genomes. Genome Biol 5: R44
56. Pereira LA, Bentley K, Peeters A, Churchill MJ, Deacon NJ (2000) A compilation of cellular transcription factor interactions with the HIV-1 LTR promoter. Nucleic Acids Res 28: 663-668
57. Perkins KJ, Lusic M, Mitar I, Giacca M, Proudfoot NJ (2008) Transcription-dependent gene looping of the HIV-1 provirus is dictated by recognition of pre-mRNA processing signals. Mol Cell 29: 56-68
58. Pickersgill H, Kalverda B, de Wit E, Talhout W, Fornerod M, van Steensel B (2006) Characterization of the Drosophila melanogaster genome at the nuclear lamina. Nat Genet 38: 1005-1014
59. Reddy KL, Zullo JM, Bertolino E, Singh H (2008) Transcriptional repression mediated by repositioning of genes to the nuclear lamina. Nature 452: 243-247
60. Saurin AJ, Shiels C, Williamson J, Satijn DP, Otte AP, Sheer D, Freemont PS (1998) The human polycomb group complex associates with pericentromeric heterochromatin to form a novel nuclear domain. J Cell Biol 142: 887-898
61. Schneider U, Schwenk HU, Bornkamm G (1977) Characterization of EBV-genome negative 'null' and 'T' cell lines derived from children with acute lymphoblastic leukemia and leukemic transformed non-Hodgkin lymphoma. Int J Cancer 19: 621-626
62. Sexton T, Schober H, Fraser P, Gasser SM (2007) Gene regulation through nuclear organization. Nat Struct Mol Biol 14: 1049-1055
63. Simonis M, Klous P, Splinter E, Moshkin Y, Willemsen R, de Wit E, van Steensel B, de Laat W (2006) Nuclear organization of active and inactive chromatin domains uncovered by chromosome conformation capture-on-chip (4C). Nat Genet 38: 1348-1354
64. Solovei I, Kreysing M, Lanctot C, Kosem S, Peichl L, Cremer T, Guck J, Joffe B (2009) Nuclear architecture of rod photoreceptor cells adapts to vision in mammalian evolution. Cell 137: 356-368
65. Solovei I, Schermelleh L, During K, Engelhardt A, Stein S, Cremer C, Cremer T (2004) Differences in centromere positioning of cycling and postmitotic human cell types. Chromosoma 112: 410-423
66. Solovei I, Walter J, Cremer M, Schermelleh L, Cremer T (2006) FISH on three-dimensional preserved nuclei. In FISH, A Practical Approach, Beatty B, Mai S, Squire J (eds), pp 119-157. Oxford, UK: Oxford University Press.
67. Spector D.L. (2003) The dynamics of chromosome organization and gene regulation. Annu Rev Biochem 72: 573-608
68. Spilianakis CG, Lalioti MD, Town T, Lee GR, Flavell RA (2005) Interchromosomal associations between alternatively expressed loci. Nature 435: 637-645
69. Taddei A, Van Houwe G, Hediger F, Kalck V, Cubizolles F, Schober H, Gasser SM (2006) Nuclear pore association confers optimal expression levels for an inducible yeast gene. Nature 441: 774-778
70. Van Lint C, Emiliani S, Ott M, Verdin E (1996) Transcriptional activation and chromatin remodeling of the HIV-1 promoter in response to histone acetylation. EMBO J 15: 1112-1120
71. Volpi EV, Chevret E, Jones T, Vatcheva R, Williamson J, Beck S, Campbell RD, Goldsworthy M, Powis SH, Ragoussis J, Trowsdale J, Sheer D (2000) Large-scale chromatin organization of the major histocompatibility complex and other regions of human chromosome 6 and its response to interferon in interphase nuclei. J Cell Sci 113(Part 9): 1565-1576
72. Weierich C, Brero A, Stein S, von Hase J, Cremer C, Cremer T, Solovei I (2003) Three-dimensional arrangements of centromeres and telomeres in nuclei of human and murine lymphocytes. Chromosome Res 11: 485-502
73. Williams RR, Azuara V, Perry P, Sauer S, Dvorkina M, Jorgensen H, Roix J, McQueen P, Misteli T, Merkenschlager M, Fisher AG (2006) Neural induction promotes large-scale chromatin reorganisation of the Mash1 locus. J Cell Sci 119: 132-140
74. Zhao Z, Tavoosidana G, Sjolinder M, Gondor A, Mariano P, Wang S, Kanduri C, Lezcano M, Sandhu KS, Singh U, Pant V, Tiwari V, Kurukuti S, Ohlsson R (2006) Circular chromosome conformation capture (4C) uncovers extensive networks of epigenetically regulated intra- and interchromosomal interactions. Nat Genet 38: 1341-1347
75. Zhou J, Ermakova OV, Riblet R, Birshtein BK, Schildkraut CL (2002) Replication and subnuclear location dynamics of the immunoglobulin heavy-chain locus in B-lineage cells. Mol Cell Biol 22: 4876-4889
76. Zink D, Amaral MD, Englmann A, Lang S, Clarke LA, Rudolph C, Alt F, Luther K, Braz C, Sadoni N, Rosenecker J, Schindelhauer D (2004) Transcription-dependent spatial arrangements of CFTR and adjacent genes in human cell nuclei. J Cell Biol 166: 815-825