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Targeting heterochromatin formation to transposable elements in Drosophila: Potential roles of the piRNA system

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Abstract

Successful heterochromatin formation is critical for genome stability in eukaryotes, both to maintain structures needed for mitosis and meiosis and to silence potentially harmful transposable elements. Conversely, inappropriate heterochromatin assembly can lead to inappropriate silencing and other deleterious effects. Hence targeting heterochromatin assembly to appropriate regions of the genome is of utmost importance. Here we focus on heterochromatin assembly in Drosophila melanogaster, the model organism in which variegation, or cell-to-cell variable gene expression resulting from heterochromatin formation, was first described. In particular, we review the potential role of transposable elements as genetic determinants of the chromatin state and examine how small RNA pathways may participate in the process of targeted heterochromatin formation.

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References

  1. Britten, R. J., and Kohne, D. E. (1968) Science, 161, 529–540.

    Article  PubMed  CAS  Google Scholar 

  2. Beisel, C., and Paro, R. (2011) Nat. Rev. Genet., 12, 123–135.

    Article  PubMed  CAS  Google Scholar 

  3. Foe, V. E., and Alberts, B. M. (1983) J. Cell. Sci., 61, 31–70.

    PubMed  CAS  Google Scholar 

  4. Lu, B. Y., Ma, J., and Eissenberg, J. C. (1998) Development, 125, 2223–2234.

    PubMed  CAS  Google Scholar 

  5. Vlassova, I. E., Graphodatsky, A. S., Belyaeva, E. S., and Zhimulev, I. F. (1991) Mol. Gen. Genet., 229, 316–318.

    Article  PubMed  CAS  Google Scholar 

  6. Rudolph, T., Yonezawa, M., Lein, S., Heidrich, K., Kubicek, S., Schafer, C., Phalke, S., Walther, M., Schmidt, A., Jenuwein, T., and Reuter, G. (2007) Mol. Cell, 26, 103–115.

    Article  PubMed  CAS  Google Scholar 

  7. Brower-Toland, B., Riddle, N. C., Jiang, H., Huisinga, K. L., and Elgin, S. C. R. (2009) Genetics, 181, 1303–1319.

    Article  PubMed  CAS  Google Scholar 

  8. Aagaard, L., Laible, G., Selenko, P., Schmid, M., Dorn, R., Schotta, G., Kuhfittig, S., Wolf, A., Lebersorger, A., Singh, P. B., Reuter, G., and Jenuwein, T. (1999) EMBO J., 18, 1923–1938.

    Article  PubMed  CAS  Google Scholar 

  9. Ekwall, K., Nimmo, E. R., Javerzat, J. P., Borgstrom, B., Egel, R., Cranston, G., and Allshire, R. (1996) J. Cell. Sci., 109(Pt. 11), 2637–2648.

    PubMed  CAS  Google Scholar 

  10. Fanti, L., Giovinazzo, G., Berloco, M., and Pimpinelli, S. (1998) Mol. Cell, 2, 527–538.

    Article  PubMed  CAS  Google Scholar 

  11. Wang, S. H., and Elgin, S. C. (2011) Proc. Natl. Acad. Sci. USA, 108, 21164–21169.

    Article  PubMed  CAS  Google Scholar 

  12. Kuhfittig, S., Szabad, J., Schotta, G., Hoffmann, J., Mathe, E., and Reuter, G. (2001) Genetics, 157, 1227–1244.

    PubMed  CAS  Google Scholar 

  13. Kharchenko, P. V., Alekseyenko, A. A., Schwartz, Y. B., Minoda, A., Riddle, N. C., Ernst, J., Sabo, P. J., Larschan, E., Gorchakov, A. A., Gu, T., Linder-Basso, D., Plachetka, A., Shanower, G., Tolstorukov, M. Y., Luquette, L. J., Xi, R., Jung, Y. L., Park, R. W., Bishop, E. P., Canfield, T. K., Sandstrom, R., Thurman, R. E., MacAlpine, D. M., Stamatoyannopoulos, J. A., Kellis, M., Elgin, S. C., Kuroda, M. I., Pirrotta, V., Karpen, G. H., and Park, P. J. (2011) Nature, 471, 480–485.

    Article  PubMed  CAS  Google Scholar 

  14. Muller, H. J. (1930) J. Genet., 22, 299–334.

    Article  Google Scholar 

  15. Wallrath, L. L., and Elgin, S. C. R. (1995) Genes Dev., 9, 1263–1277.

    Article  PubMed  CAS  Google Scholar 

  16. Sun, F. L., Cuaycong, M. H., and Elgin, S. C. R. (2001) Mol. Cell Biol., 21, 2867–2879.

    Article  PubMed  CAS  Google Scholar 

  17. Cryderman, D. E., Tang, H., Bell, C., Gilmour, D. S., and Wallrath, L. L. (1999) Nucleic Acids Res., 27, 3364–3370.

    Article  PubMed  CAS  Google Scholar 

  18. Vogel, M. J., Pagie, L., Talhout, W., Nieuwland, M., Kerkhoven, R. M., and van Steensel, B. (2009) Epigenetics & Chromatin, 2, 1.

    Article  Google Scholar 

  19. Slotkin, R. K., and Martienssen, R. A. (2007) Nat. Rev. Genet., 8, 272–285.

    Article  PubMed  CAS  Google Scholar 

  20. Kloc, A., and Martienssen, R. A. (2008) Trends Genet., 24, 511–517.

    Article  PubMed  CAS  Google Scholar 

  21. Irvine, D. V., Zaratiegui, M., Tolia, N. H., Goto, D. B., Chitwood, D. H., Vaughn, M. W., Joshua-Tor, L., and Martienssen, R. A. (2006) Science, 313, 1134–1137.

    Article  PubMed  CAS  Google Scholar 

  22. Huisinga, K. L., and Elgin, S. C. R. (2009) Biochim. Biophys. Acta, 1789, 3–16.

    Article  PubMed  CAS  Google Scholar 

  23. Dai, Q., Smibert, P., and Lai, E. C. (2012) Curr. Top. Dev. Biol., 99, 201–235.

    Article  PubMed  CAS  Google Scholar 

  24. Kawamura, Y., Saito, K., Kin, T., Ono, Y., Asai, K., Sunohara, T., Okada, T. N., Siomi, M. C., and Siomi, H. (2008) Nature, 453, 793–797.

    Article  PubMed  CAS  Google Scholar 

  25. Ghildiyal, M., Seitz, H., Horwich, M. D., Li, C., Du, T., Lee, S., Xu, J., Kittler, E. L. W., Zapp, M. L., Weng, Z., and Zamore, P. D. (2008) Science, 320, 1077–1081.

    Article  PubMed  CAS  Google Scholar 

  26. Moshkovich, N., Nisha, P., Boyle, P. J., Thompson, B. A., Dale, R. K., and Lei, E. P. (2011) Genes Dev., 25, 1686–1701.

    Article  PubMed  CAS  Google Scholar 

  27. Cernilogar, F. M., Onorati, M. C., Kothe, G. O., Burroughs, A. M., Parsi, K. M., Breiling, A., Lo Sardo, F., Saxena, A., Miyoshi, K., Siomi, H., Siomi, M. C., Carninci, P., Gilmour, D. S., Corona, D. F., and Orlando, V. (2011) Nature, 480, 391–395.

    Article  PubMed  CAS  Google Scholar 

  28. Gunawardane, L. S., Saito, K., Nishida, K. M., Miyoshi, K., Kawamura, Y., Nagami, T., Siomi, H., and Siomi, M. C. (2007) Science, 315, 1587–1590.

    Article  PubMed  CAS  Google Scholar 

  29. Brennecke, J., Aravin, A. A., Stark, A., Dus, M., Kellis, M., Sachidanandam, R., and Hannon, G. J. (2007) Cell, 128, 1089–1103.

    Article  PubMed  CAS  Google Scholar 

  30. Klenov, M. S., Sokolova, O. A., Yakushev, E. Y., Stolyarenko, A. D., Mikhaleva, E. A., Lavrov, S. A., and Gvozdev, V. A. (2011) Proc. Natl. Acad. Sci. USA, 108, 18760–18765.

    Article  PubMed  CAS  Google Scholar 

  31. Feschotte, C. (2008) Nat. Rev. Genet., 9, 397–405.

    Article  PubMed  CAS  Google Scholar 

  32. Gangaraju, V. K., Yin, H., Weiner, M. M., Wang, J., Huang, X. A., and Lin, H. (2010) Nat. Genet., 43, 153–158.

    Article  PubMed  Google Scholar 

  33. Cam, H. P., Noma, K.-I., Ebina, H., Levin, H. L., and Grewal, S. I. S. (2008) Nature, 451, 431–436.

    Article  PubMed  CAS  Google Scholar 

  34. Aravind, L. (2000) Trends Biochem. Sci., 25, 421–423.

    Article  PubMed  CAS  Google Scholar 

  35. Aulner, N., Monod, C., Mandicourt, G., Jullien, D., Cuvier, O., Sall, A., Janssen, S., Laemmli, U. K., and Kas, E. (2002) Mol. Cell Biol., 22, 1218–1232.

    Article  PubMed  CAS  Google Scholar 

  36. Filion, G. J., van Bemmel, J. G., Braunschweig, U., Talhout, W., Kind, J., Ward, L. D., Brugman, W., de Castro, I. J., Kerkhoven, R. M., Bussemaker, H. J., and van Steensel, B. (2010) Cell, 143, 212–224.

    Article  PubMed  CAS  Google Scholar 

  37. Smith, M. B., and Weiler, K. S. (2010) Chromosoma, 119, 287–309.

    Article  PubMed  Google Scholar 

  38. Kapitonov, V. V., and Jurka, J. (2003) Proc. Natl. Acad. Sci. USA, 100, 6569–6574.

    Article  PubMed  CAS  Google Scholar 

  39. Lander, E. S., Linton, L. M., Birren, B., Nusbaum, C., Zody, M. C., Baldwin, J., Devon, K., Dewar, K., Doyle, M., FitzHugh, W., Funke, R., Gage, D., Harris, K., Heaford, A., Howland, J., Kann, L., Lehoczky, J., LeVine, R., McEwan, P., McKernan, K., Meldrim, J., Mesirov, J. P., Miranda, C., Morris, W., Naylor, J., Raymond, C., Rosetti, M., Santos, R., Sheridan, A., Sougnez, C., Stange-Thomann, N., Stojanovic, N., Subramanian, A., Wyman, D., Rogers, J., Sulston, J., Ainscough, R., Beck, S., Bentley, D., Burton, J., Clee, C., Carter, N., Coulson, A., Deadman, R., Deloukas, P., Dunham, A., Dunham, I., Durbin, R., French, L., Grafham, D., Gregory, S., Hubbard, T., Humphray, S., Hunt, A., Jones, M., Lloyd, C., McMurray, A., Matthews, L., Mercer, S., Milne, S., Mullikin, J. C., Mungall, A., Plumb, R., Ross, M., Shownkeen, R., Sims, S., Waterston, R. H., Wilson, R. K., Hillier, L. W., McPherson, J. D., Marra, M. A., Mardis, E. R., Fulton, L. A., Chinwalla, A. T., Pepin, K. H., Gish, W. R., Chissoe, S. L., Wendl, M. C., Delehaunty, K. D., Miner, T. L., Delehaunty, A., Kramer, J. B., Cook, L. L., Fulton, R. S., Johnson, D. L., Minx, P. J., Clifton, S. W., Hawkins, T., Branscomb, E., Predki, P., Richardson, P., Wenning, S., Slezak, T., Doggett, N., Cheng, J. F., Olsen, A., Lucas, S., Elkin, C., Uberbacher, E., Frazier, M., Gibbs, R. A., Muzny, D. M., Scherer, S. E., Bouck, J. B., Sodergren, E. J., Worley, K. C., Rives, C. M., Gorrell, J. H., Metzker, M. L., Naylor, S. L., Kucherlapati, R. S., Nelson, D. L., Weinstock, G. M., Sakaki, Y., Fujiyama, A., Hattori, M., Yada, T., Toyoda, A., Itoh, T., Kawagoe, C., Watanabe, H., Totoki, Y., Taylor, T., Weissenbach, J., Heilig, R., Saurin, W., Artiguenave, F., Brottier, P., Bruls, T., Pelletier, E., Robert, C., Wincker, P., Smith, D. R., Doucette-Stamm, L., Rubenfield, M., Weinstock, K., Lee, H. M., Dubois, J., Rosenthal, A., Platzer, M., Nyakatura, G., Taudien, S., Rump, A., Yang, H., Yu, J., Wang, J., Huang, G., Gu, J., Hood, L., Rowen, L., Madan, A., Qin, S., Davis, R. W., Federspiel, N. A., Abola, A. P., Proctor, M. J., Myers, R. M., Schmutz, J., Dickson, M., Grimwood, J., Cox, D. R., Olson, M. V., Kaul, R., Shimizu, N., Kawasaki, K., Minoshima, S., Evans, G. A., Athanasiou, M., Schultz, R., Roe, B. A., Chen, F., Pan, H., Ramser, J., Lehrach, H., Reinhardt, R., McCombie, W. R., de la Bastide, M., Dedhia, N., Blocker, H., Hornischer, K., Nordsiek, G., Agarwala, R., Aravind, L., Bailey, J. A., Bateman, A., Batzoglou, S., Birney, E., Bork, P., Brown, D. G., Burge, C. B., Cerutti, L., Chen, H. C., Church, D., Clamp, M., Copley, R. R., Doerks, T., Eddy, S. R., Eichler, E. E., Furey, T. S., Galagan, J., Gilbert, J. G., Harmon, C., Hayashizaki, Y., Haussler, D., Hermjakob, H., Hokamp, K., Jang, W., Johnson, L. S., Jones, T. A., Kasif, S., Kaspryzk, A., Kennedy, S., Kent, W. J., Kitts, P., Koonin, E. V., Korf, I., Kulp, D., Lancet, D., Lowe, T. M., McLysaght, A., Mikkelsen, T., Moran, J. V., Mulder, N., Pollara, V. J., Ponting, C. P., Schuler, G., Schultz, J., Slater, G., Smit, A. F., Stupka, E., Szustakowski, J., Thierry-Mieg, D., Thierry-Mieg, J., Wagner, L., Wallis, J., Wheeler, R., Williams, A., Wolf, Y. I., Wolfe, K. H., Yang, S. P., Yeh, R. F., Collins, F., Guyer, M. S., Peterson, J., Felsenfeld, A., Wetterstrand, K. A., Patrinos, A., Morgan, M. J., de Jong, P., Catanese, J. J., Osoegawa, K., Shizuya, H., Choi, S., and Chen, Y. J. (2001) Nature, 409, 860–921.

    Article  PubMed  CAS  Google Scholar 

  40. Aravin, A. A., Lagos-Quintana, M., Yalcin, A., Zavolan, M., Marks, D., Snyder, B., Gaasterland, T., Meyer, J., and Tuschl, T. (2003) Dev. Cell, 5, 337–350.

    Article  PubMed  CAS  Google Scholar 

  41. Sun, F.-L., Haynes, K. A., Simpson, C. L., Lee, S. D., Collins, L., Wuller, J., Eissenberg, J. C., and Elgin, S. C. R. (2004) Mol. Cell Biol., 24, 8210–8220.

    Article  PubMed  CAS  Google Scholar 

  42. Haynes, K. A., Caudy, A. A., Collins, L., and Elgin, S. C. (2006) Curr. Biol., 16, 2222–2227.

    Article  PubMed  CAS  Google Scholar 

  43. Sentmanat, M. F., and Elgin, S. C. (2012) Proc. Natl. Acad. Sci. USA, 109, 14104–14109.

    Article  PubMed  CAS  Google Scholar 

  44. Sienski, G., Donertas, D., and Brennecke, J. (2012) Cell, 151, 964–980.

    Article  PubMed  CAS  Google Scholar 

  45. Le Thomas, A., Rogers, A. K., Webster, A., Marinov, G. K., Liao, S. E., Perkins, E. M., Hur, J. K., Aravin, A. A., and Toth, K. F. (2013) Genes Dev., in press.

    Google Scholar 

  46. Fagegaltier, D., Bouge, A.-L., Berry, B., Poisot, E., Sismeiro, O., Coppee, J.-Y., Theodore, L., Voinnet, O., and Antoniewski, C. (2009) Proc. Natl. Acad. Sci. USA, 106, 21258–21263.

    Article  PubMed  CAS  Google Scholar 

  47. Deshpande, G., Calhoun, G., and Schedl, P. (2005) Genes Dev., 19, 1680–1685.

    Article  PubMed  CAS  Google Scholar 

  48. Rouget, C., Papin, C., Boureux, A., Meunier, A.-C., Franco, B., Robine, N., Lai, E. C., Pelisson, A., and Simonelig, M. (2010) Nature, 467, 1128–1132.

    Article  PubMed  CAS  Google Scholar 

  49. Cox, D. N., Chao, A., Baker, J., Chang, L., Qiao, D., and Lin, H. (1998) Genes Dev., 12, 3715–3727.

    Article  PubMed  CAS  Google Scholar 

  50. Pal-Bhadra, M., Leibovitch, B. A., Gandhi, S. G., Rao, M., Bhadra, U., Birchler, J. A., and Elgin, S. C. R. (2004) Science, 303, 669–672.

    Article  PubMed  CAS  Google Scholar 

  51. Klenov, M. S., Lavrov, S. A., Stolyarenko, A. D., Ryazansky, S. S., Aravin, A. A., Tuschl, T., and Gvozdev, V. A. (2007) Nucleic Acids Res., 35, 5430–5438.

    Article  PubMed  CAS  Google Scholar 

  52. Brower-Toland, B., Findley, S. D., Jiang, L., Liu, L., Yin, H., Dus, M., Zhou, P., Elgin, S. C. R., and Lin, H. (2007) Genes Dev., 21, 2300–2311.

    Article  PubMed  CAS  Google Scholar 

  53. Mendez, D. L., Kim, D., Chruszcz, M., Stephens, G. E., Minor, W., Khorasanizadeh, S., and Elgin, S. C. (2011) Chembiochem, 12, 1084–1096.

    Article  PubMed  CAS  Google Scholar 

  54. Girton, J. R., and Johansen, K. M. (2008) Adv. Genet., 61, 1–43.

    Article  PubMed  CAS  Google Scholar 

  55. Li, C., Vagin, V. V., Lee, S., Xu, J., Ma, S., Xi, H., Seitz, H., Horwich, M. D., Syrzycka, M., Honda, B. M., Kittler, E. L. W., Zapp, M. L., Klattenhoff, C., Schulz, N., Theurkauf, W. E., Weng, Z., and Zamore, P. D. (2009) Cell, 137, 509–521.

    Article  PubMed  CAS  Google Scholar 

  56. Saito, K., Ishizu, H., Komai, M., Kotani, H., Kawamura, Y., Nishida, K. M., Siomi, H., and Siomi, M. C. (2010) Genes Dev., 24, 2493–2498.

    Article  PubMed  CAS  Google Scholar 

  57. Shpiz, S., Olovnikov, I., Sergeeva, A., Lavrov, S., Abramov, Y., Savitsky, M., and Kalmykova, A. (2011) Nucleic Acids Res., 39, 8703–8711.

    Article  PubMed  CAS  Google Scholar 

  58. Sigova, A., Vagin, V., and Zamore, P. D. (2006) Cold Spring Harb. Symp. Quant. Biol., 71, 335–341.

    Article  PubMed  CAS  Google Scholar 

  59. Rangan, P., Malone, C. D., Navarro, C., Newbold, S. P., Hayes, P. S., Sachidanandam, R., Hannon, G. J., and Lehmann, R. (2011) Curr. Biol., 21, 1373–1379.

    Article  PubMed  CAS  Google Scholar 

  60. Seum, C., Delattre, M., Spierer, A., and Spierer, P. (2001) EMBO J., 20, 812–818.

    Article  PubMed  CAS  Google Scholar 

  61. Li, Y., Danzer, J. R., Alvarez, P., Belmont, A. S., and Wallrath, L. L. (2003) Development, 130, 1817–1824.

    Article  PubMed  CAS  Google Scholar 

  62. Doheny, J. G., Mottus, R., and Grigliatti, T. A. (2008) PLoS One, 3, e3864.

    Article  PubMed  Google Scholar 

  63. Cryderman, D. E., Morris, E. J., Biessmann, H., Elgin, S. C., and Wallrath, L. L. (1999) EMBO J., 18, 3724–3735.

    Article  PubMed  CAS  Google Scholar 

  64. Haynes, K. A., Gracheva, E., and Elgin, S. C. R. (2007) Genetics, 175, 1539–1542.

    Article  PubMed  CAS  Google Scholar 

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  1. Department of Biology, Washington University, Campus Box 1137, One Brookings Drive, St. Louis, MO, 63130-4899, USA

    M. Sentmanat, S. H. Wang & S. C. R. Elgin

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  1. M. Sentmanat
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Published in Russian in Biokhimiya, 2013, Vol. 78, No. 6, pp. 735–746.

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Sentmanat, M., Wang, S.H. & Elgin, S.C.R. Targeting heterochromatin formation to transposable elements in Drosophila: Potential roles of the piRNA system. Biochemistry Moscow 78, 562–571 (2013). https://doi.org/10.1134/S0006297913060023

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