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Closed Chromatin Architecture Is Induced by an RNA Duplex Targeting the HIV-1 Promoter Region

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Suzuki, Kazuo, Juelich, Torsten, Lim, Heidi, Ishida, Takaomi, Watanebe, Toshiki, Cooper, David A., Rao, Sudha, Kelleher, Anthony D.·2008·Journal of Biological Chemistry
DOI 10.1074/jbc.m709651200PMC PMC2516975
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Abstract

In some mammalian systems small interfering RNAs (siRNA) targeting homologous sequences in promoter regions of genes induce transcriptional gene silencing (TGS). We have previously reported the induction of TGS by an siRNA (prom-A siRNA) targeting the tandem NF-kappaB-binding motifs within the human immunodeficiency virus, type 1 (HIV-1), promoter region. Here we report that induction of TGS by prom-A siRNA is accompanied by immediate and sustained local recruitment of Argonaute-1 (Ago1), histone deacetylase-1 (HDAC1), and induction of dimethylation of histone 3 at lysine 9 (H3K9me2), processes known to be associated with transcriptional silencing. Elevated levels of H3K9me2 and HDAC1 spread upstream of the target sequence, and elevated H3K9me2 levels also spread downstream into the coding region. Moreover, this siRNA induces an immediate change in DNA accessibility to restriction enzyme digestion in the region of the transcription initiation site of the HIV-1. This change in accessibility is because of the relocation of a nucleosome known to be associated with this region of the integrated pro-virus. Although there is a theoretical possibility that the observed viral suppression could be mediated by the PTGS mechanism with this siRNA acting at the 3 (R)-long term repeat of the virus, we demonstrate that this siRNA, and three other U3 targeted siRNAs, are inefficient inducers of PTGS. These data strongly suggest that siRNA targeting the promoter region acts predominantly at a site within the 5 (R)-long term repeat of HIV to induce transcriptional silencing and alterations to chromatin structure of the HIV promoter region that extend well beyond the immediate siRNA target site. These induced changes are consistent with those described in latent HIV-1 infection.

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  • The first anti-HIV-1, siPromA, targeted the unique and highly conserved NK-κB transcription factor sites in the HIV-1 promoter to induce potent epigenetic silencing.

    “The first anti-HIV-1, siPromA, was first identified in 2005 [309], and targeted the unique and highly conserved NK-κB transcription factor sites in the HIV-1 promoter to induce potent epigenetic silencing [70,310,311,312].”

    From Current State of Therapeutics for HTLV-1 (2024) · cites this paper as [310]

    The Discussion (page not available) says prom-A targets NF-κB-binding sites in the HIV-1 promoter and links its silencing effect to sustained epigenetic and chromatin changes. The Results report substantial suppression of viral production. Our copy does not establish that the target sites are unique or highly conserved; the sentence cites a different source for the 2005 identification. (LLM, conf=0.84)

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  1. [1]Lippman, Z., and Martienssen, R. (2004) Nature 431 364-370 15372044
  2. [2]de Fougerolles, A., Vornlocher, H. P., Maraganore, J., and Lieberman, J. (2007) Nat. Rev. Drug Discov. 6 443-453 17541417 PMC7098199
  3. [3]Soifer, H. S., Rossi, J. J., and Saetrom, P. (2007) Mol. Ther. 15 2070-2079 17878899
  4. [4]Mette, M. F., Aufsatz, W., van der Winden, J., Matzke, M. A., and Matzke, A. J. (2000) EMBO J. 19 5194-5201 11013221 PMC302106
  5. [5]Matzke, M., Matzke, A. J., and Kooter, J. M. (2001) Science 293 1080-1083 11498576
  6. [6]Xie, Z., Johansen, L. K., Gustafson, A. M., Kasschau, K. D., Lellis, A. D., Zilberman, D., Jacobsen, S. E., and Carrington, J. C. (2004) Plos Biol. 2 642-652 PMC350667 15024409
  7. [7]Matzke, M. A., and Birchler, J. A. (2005) Nat. Rev. Genet. 6 24-35 15630419
  8. [8]Grewal, S. I., and Jia, S. (2007) Nat. Rev. Genet. 8 35-46 17173056
  9. [9]Morris, K. V., Chan, S. W., Jacobsen, S. E., and Looney, D. J. (2004) Science 305 1289-1292 15297624
  10. [10]Buhler, M., Mohn, F., Stalder, L., and Muhlemann, O. (2005) Mol. Cell 18 307-317 15866173
  11. [11]Castanotto, D., Tommasi, S., Li, M., Li, H., Yanow, S., Pfeifer, G. P., and Rossi, J. J. (2005) Mol. Ther. 12 179-183 15963934
  12. [12]Suzuki, K., Shijuuku, T., Fukamachi, T., Zaunders, J., Guillemin, G., Cooper, D., and Kelleher, A. (2005) J. RNAi Gene Silencing 1 66-78 PMC2737205 19771207
  13. [13]Janowski, B. A., Kaihatsu, K., Huffman, K. E., Schwartz, J. C., Ram, R., Hardy, D., Mendelson, C. R., and Corey, D. R. (2005) Nat. Chem. Biol. 1 210-215 16408037
  14. [14]Ting, A. H., Schuebel, K. E., Herman, J. G., and Baylin, S. B. (2005) Nat. Genet. 37 906-910 16025112 PMC2659476
  15. [15]Zhang, M. X., Ou, H., Shen, Y. H., Wang, J., Wang, J., Coselli, J., and Wang, X. L. (2005) Proc. Natl. Acad. Sci. U. S. A. 102 16967-16972 16284254 PMC1287968
  16. [16]Janowski, B. A., Huffman, K. E., Schwartz, J. C., Ram, R., Hardy, D., Shames, D. S., Minna, J. D., and Corey, D. R. (2005) Nat. Chem. Biol. 1 216-222 16408038
  17. [17]Weinberg, M. S., Villeneuve, L. M., Ehsani, A., Amarzguioui, M., Aagaard, L., Chen, Z. X., Riggs, A. D., Rossi, J. J., and Morris, K. V. (2006) RNA (N. Y.) 12 256-262 PMC1370905 16373483
  18. [18]Janowski, B. A., Huffman, K. E., Schwartz, J. C., Ram, R., Nordsell, R., Shames, D. S., Minna, J. D., and Corey, D. R. (2006) Nat. Struct. Mol. Biol. 13 787-792 16936728
  19. [19]Kim, D. H., Villeneuve, L. M., Morris, K. V., and Rossi, J. J. (2006) Nat. Struct. Mol. Biol. 13 793-797 16936726
  20. [20]Pulukuri, S. M., and Rao, J. S. (2007) Cancer Res. 67 6637-6646 17638874 PMC2390768
  21. [21]Wang, X., Feng, Y., Pan, L., Wang, Y., Xu, X., Lu, J., and Huang, B. (2007) Mol. Cell. Biochem. 301 259-266 17333389
  22. [22]Weinberg, M. S., Barichievy, S., Schaffer, L., Han, J., and Morris, K. V. (2007) Nucleic Acids Res. 35 1-10 17959645 PMC2175361
  23. [23]Kim, J. W., Zhang, Y. H., Zern, M. A., Rossi, J. J., and Wu, J. (2007) Biochem. Biophys. Res. Commun. 359 292-297 17533113 PMC2474738
  24. [24]Noma, K., Sugiyama, T., Cam, H., Verdel, A., Zofall, M., Jia, S., Moazed, D., and Grewal, S. I. (2004) Nat. Genet. 36 1174-1180 15475954
  25. [25]Verdel, A., Jia, S., Gerber, S., Sugiyama, T., Gygi, S., Grewal, S. I., and Moazed, D. (2004) Science 303 672-676 14704433 PMC3244756
  26. [26]Hutvagner, G., and Simard, M. J. (2008) Nat. Rev. Mol. Cell Biol. 105 512-517 18073770
  27. [27]Peters, L., and Meister, G. (2007) Mol. Cell 26 611-623 17560368
  28. [28]Vire, E., Brenner, C., Deplus, R., Blanchon, L., Fraga, M., Didelot, C., Morey, L., Van Eynde, A., Bernard, D., Vanderwinden, J. M., Bollen, M., Esteller, M., Di Croce, L., de Launoit, Y., and Fuks, F. (2006) Nature 439 871-874 16357870
  29. [29]Han, J., Kim, D., and Morris, K. V. (2007) Proc. Natl. Acad. Sci. U. S. A. 104 12422-12427 17640892 PMC1924466
  30. [30]Bennasser, Y., Le, S. Y., Yeung, M. L., and Jeang, K. T. (2004) Retrovirology 1 43 15601472 PMC544590
  31. [31]Li, L. C., Okino, S. T., Zhao, H., Pookot, D., Place, R. F., Urakami, S., Enokida, H., and Dahiya, R. (2006) Proc. Natl. Acad. Sci. U. S. A. 103 17337-17342 17085592 PMC1859931
  32. [32]Triboulet, R., Mari, B., Lin, Y. L., Chable-Bessia, C., Bennasser, Y., Lebrig- and, K., Cardinaud, B., Maurin, T., Barbry, P., Baillat, V., Reynes, J., Corbeau, P., Jeang, K. T., and Benkirane, M. (2007) Science 315 1579-1582 17322031
  33. [33]Klase, Z., Kale, P., Winograd, R., Gupta, M. V., Heydarian, M., Berro, R., McCaffrey, T., and Kashanchi, F. (2007) BMC Mol. Biol. 8 63 17663774 PMC1955452
  34. [34]Smith, A. E., Hurd, P. J., Bannister, A. J., Kouzarides, T., and Ford, K. G. (2008) J. Biol. Chem. 283 9878-9885 18272522
  35. [35]Lim, H. G., Suzuki, K., Cooper, D. A., and Kelleher, A. D. (2008) Mol. Ther. 16 565-570 18227841
  36. [36]Aldovini, A., and Walker, B. D. (1990) Techniques in HIV Research: HIV-Laboratory Manuals, pp. 51-128, Macmillan Press, Ltd., Hants, UK
  37. [37]Suzuki, K., Craddock, B. P., Okamoto, N., Kano, T., and Steigbigel, R. T. (1993) J. Virol. Methods 44 189-198 7505283
  38. [38]Rao, S., Procko, E., and Shannon, M. F. (2001) J. Immunol. 167 4494-4503 11591776
  39. [39]Nakayama, J., Rice, J. C., Strahl, B. D., Allis, C. D., and Grewal, S. I. (2001) Science 292 110-113 11283354
  40. [40]Peters, A. H., Mermoud, J. E., O'Carroll, D., Pagani, M., Schweizer, D., Brockdorff, N., and Jenuwein, T. (2002) Nat. Genet. 30 77-80 11740497
  41. [41]Verdin, E., Paras, P., Jr., and Van Lint, C. (1993) EMBO J. 12 3249-3359 8344262 PMC413592
  42. [42]Van Lint, C., Emiliani, S., Ott, M., and Verdin, E. (1996) EMBO J. 15 1112-1120 8605881 PMC450009
  43. [43]Pazin, M. J., Sheridan, P. L., Cannon, K., Cao, Z., Keck, J. G., Kadonaga, J. T., and Jones, K. A. (1996) Genes Dev. 10 37-49 8557193
  44. [44]Jordan, A., Bisgrove, D., and Verdin, E. (2003) EMBO J. 22 1868-1877 12682019 PMC154479
  45. [45]Williams, S. A., Chen, L. F., Kwon, H., Fenard, D., Bisgrove, D., Verdin, E., and Greene, W. C. (2004) J. Biol. Chem. 279 42008-42017 15284245
  46. [46]Williams, S. A., Chen, L. F., Kwon, H., Ruiz-Jarabo, C. M., Verdin, E., and Greene, W. C. (2006) EMBO J. 25 139-149 16319923 PMC1356344
  47. [47]Marban, C., Suzanne, S., Dequiedt, F., de Walque, S., Redel, L., Van Lint, C., Aunis, D., and Rohr, O. (2007) EMBO J. 26 412-423 17245431 PMC1783449
  48. [48]du Chene, I., Basyuk, E., Lin, Y. L., Triboulet, R., Knezevich, A., Chable-Bessia, C., Mettling, C., Baillat, V., Reynes, J., Corbeau, P., Bertrand, E., Marcello, A., Emiliani, S., Kiernan, R., and Benkirane, M. (2007) EMBO J. 26 424-435 17245432 PMC1783455
  49. [49]Hall, I. M., Shankaranarayana, G. D., Noma, K., Ayoub, N., Cohen, A., and Grewal, S. I. (2002) Science 297 2232-2237 12215653
  50. [50]Buhler, M., Verdel, A., and Moazed, D. (2006) Cell 125 873-886 16751098
  51. [51]Coffin, J. M., Hughes, S. H., and Varmus, H. E. (1997) Retroviruses, pp. 205-261, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY 21433340
  52. [52]Kim, D. H., and Rossi, J. J. (2007) Nat. Rev. Genet. 8 173-184 17304245
  53. [53]Piacentini, L., Fanti, L., Berloco, M., Perrini, B., and Pimpinelli, S. (2003) J. Cell Biol. 161 707-714 12756231 PMC2199350
  54. [54]Vakoc, C. R., Mandat, S. A., Olenchock, B. A., and Blobel, G. A. (2005) Mol. Cell 19 381-391 16061184
  55. [56]Weiler, K. S., and Wakimoto, B. T. (1995) Annu. Rev. Genet. 29 577-605 8825487
  56. [57]Lu, B. Y., Emtage, P. C., Duyf, B. J., Hilliker, A. J., and Eissenberg, J. C. (2000) Genetics 155 699-708 10835392 PMC1461102
  57. [58]Yasuhara, J. C., and Wakimoto, B. T. (2006) Trends Genet. 22 330-338 16690158
  58. [59]Greil, F., van der Kraan, I., Delrow, J., Smothers, J. F., de Wit, E., Busse-maker, H. J., van Driel, R., Henikoff, S., and van Steensel, B. (2003) Genes Dev. 17 2825-2838 14630943 PMC280630
  59. [60]Cryderman, D. E., Grade, S. K., Li, Y., Fanti, L., Pimpinelli, S., and Wallrath, L. L. (2005) Dev. Dyn. 232 767-774 15704177
  60. [61]Carrozza, M. J., Li, B., Florens, L., Suganuma, T., Swanson, S. K., Lee, K. K., Shia, W. J., Anderson, S., Yates, J., Washburn, M. P., and Workman, J. L. (2005) Cell 123 581-592 16286007
  61. [62]Joshi, A. A., and Struhl, K. (2005) Mol. Cell 20 971-978 16364921
  62. [63]Keogh, M. C., Kurdistani, S. K., Morris, S. A., Ahn, S. H., Podolny, V., Collins, S. R., Schuldiner, M., Chin, K., Punna, T., Thompson, N. J., Boone, C., Emili, A., Weissman, J. S., Hughes, T. R., Strahl, B. D., Grunstein, M., Greenblatt, J. F., Buratowski, S., and Krogan, N. J. (2005) Cell 123 593-605 16286008
  63. [64]Fuks, F., Hurd, P. J., Deplus, R., and Kouzarides, T. (2003) Nucleic Acids Res. 31 2305-2312 12711675 PMC154218
  64. [65]Morris, S. A., Rao, B., Garcia, B. A., Hake, S. B., Diaz, R. L., Shabanowitz, J., Hunt, D. F., Allis, C. D., Lieb, J. D., and Strahl, B. D. (2007) J. Biol. Chem. 282 7632-7640 17189264 PMC2811852
  65. [66]Fuks, F., Hurd, P. J., Wolf, D., Nan, X., Bird, A. P., and Kouzarides, T. (2003) J. Biol. Chem. 278 4035-4040 12427740
  66. [67]Reynolds, A., Leake, D., Boese, Q., Scaringe, S., Marshall, W. S., and Khvorova, A. (2004) Nat. Biotechnol. 22 326-330 14758366
  67. [68]Eulalio, A., Behm-Ansmant, I., and Izaurralde, E. (2007) Nat. Rev. Mol. Cell Biol. 8 9-22 17183357
  68. [69]Parker, R., and Sheth, U. (2007) Mol. Cell 25 635-646 17349952
  69. [70]Janowski, B. A., Younger, S. T., Hardy, D. B., Ram, R., Huffman, K. E., and Corey, D. R. (2007) Nat. Chem. Biol. 3 166-173 17259978
  70. [71]Han, Y., Wind-Rotolo, M., Yang, H. C., Siliciano, J. D., and Siliciano, R. F. (2007) Nat. Rev. Microbiol. 5 95-106 17224919
  71. [72]Haynes, K. A., Caudy, A. A., Collins, L., and Elgin, S. C. (2006) Curr. Biol. 16 2222-2227 17113386 PMC1712676
  72. [73]Sugiyama, T., Cam, H. P., Sugiyama, R., Noma, K., Zofall, M., Kobayashi, R., and Grewal, S. I. (2007) Cell 128 491-504 17289569
  73. [74]Harbers, K., Schnieke, A., Stuhlmann, H., Jahner, D., and Jaenisch, R. (1981) Proc. Natl. Acad. Sci. U. S. A. 78 7609-7613 6950402 PMC349318
  74. [75]Hu, W. S., Fanning, T. G., and Cardiff, R. D. (1984) J. Virol. 49 66-71 6317895 PMC255425
  75. [76]Clarke, M. F., Trainor, C. D., Mann, D. L., Gallo, R. C., and Reitz, M. S. (1984) Virology 135 97-104 6328756
  76. [77]Adachi, A., Gendelman, H. E., Koenig, S., Folks, T., Willey, R., Rabson, A., and Martin, M. A. (1986) J. Virol. 59 284-291 3016298 PMC253077
  77. [78]Koiwa, T., Hamano-Usami, A., Ishida, T., Okayama, A., Yamaguchi, K., Kamihira, S., and Watanabe, T. (2002) J. Virol. 76 9389-9397 12186921 PMC136445
  78. [79]Siliciano, J. D., Kajdas, J., Finzi, D., Quinn, T. C., Chadwick, K., Margolick, J. B., Kovacs, C., Gange, S. J., and Siliciano, R. F. (2003) Nat. Med. 9 727-728 12754504
  79. [80]Lassen, K., Han, Y., Zhou, Y., Siliciano, J., and Siliciano, R. F. (2004) Trends Mol. Med. 10 525-531 15519278

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Authors
Suzuki, K., Juelich, T., Lim, H., Ishida, T., Watanebe, T., Cooper, D. A., Rao, S., & Kelleher, A. D.
Affiliations
  • St Vincent's Hospital Sydney (AU)
  • UNSW Sydney (AU)
  • The University of Tokyo (JP)
Corresponding author
Suzuki, Kazuo
ORCID
Venue
Journal of Biological Chemistry
Publisher
Elsevier BV
Published
2008-08
Volume
283
Issue
34
Pages
23353-23363
ISSN
0021-9258 (ISSN-L)
DOI
10.1074/jbc.m709651200
PMC
PMC2516975
OpenAlex
W1993695454
Cited by
108
References
79
Citations by year
2026: 1 · 2025: 3 · 2024: 4 · 2023: 5 · 2022: 2 · 2021: 1 · 2020: 4 · 2019: 3 · 2018: 6 · 2017: 4 · 2016: 4 · 2015: 10 · 2014: 12 · 2013: 9 · 2012: 5
FWCI
4.80
Type
journal article
Language
en
Open access
Licence
Locations
  • Journal of Biological Chemistry (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by-nc)
  • PubMed (publishedVersion)
  • ANU Open Research (Australian National University) (submittedVersion)
Funders
  • National Institutes of Health (pNL4-3)
  • Medical Research Council
  • National Health and Medical Research Council
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Interference and Gene Delivery
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
Keywords
HIV-1 promoter, transcriptional silencing, siRNA, RNA duplex, AGO1, HDAC1, H3K9 dimethylation, chromatin structure, DNA accessibility, long terminal repeat, HIV latency
MeSH terms
Binding Sites, Chromatin, HeLa Cells, HIV, Humans, Models, Biological, Nucleosomes, Promoter Regions, Genetic, RNA, Transcription, Genetic, Transfection, HIV-1, NF-kappa B, Gene Silencing, RNA, Small Interfering

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