A novel epigenetic mechanism in Drosophila somatic cells mediated by PIWI and piRNAs

Cold Spring Harbor Symposia on Quantitative Biology

Volumn 73, Issue , 2008, Pages 273-281

  Lin, H ^a   Yin, H ^a,b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ARGONAUTE PROTEIN; HETEROCHROMATIN PROTEIN 1; HETEROCHROMATIN PROTEIN 1A; HISTONE 3 AT LYSINE 9; LYSINE DERIVATIVE; PIWI INTERACTING RNA; PIWI PROTEIN; PROTEIN METHYLTRANSFERASE; RNA; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN; HETEROCHROMATIN PROTEIN 1, DROSOPHILA; NONHISTONE PROTEIN; PIWI PROTEIN, DROSOPHILA; RNA INDUCED SILENCING COMPLEX; SMALL INTERFERING RNA; H3K9 PROTEIN; HISTONE;

AMINO ACID SEQUENCE; CHROMATIN; CHROMOSOME; CONFERENCE PAPER; DROSOPHILA; EPIGENETICS; GENOME; GERM LINE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; SEQUENCE ANALYSIS; SOMATIC CELL; ANIMAL; BINDING SITE; BIOLOGICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; CYTOLOGY; GENETIC EPIGENESIS; GENETICS; METABOLISM; MOLECULAR GENETICS; REVIEW; HISTONE METHYLATION; INTRACELLULAR SIGNALING; MEDICAL LITERATURE; MOLECULAR BIOLOGY; PROTEIN PROTEIN INTERACTION;

MAMMALIA;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CHROMATIN; CHROMOSOMAL PROTEINS, NON-HISTONE; DROSOPHILA; DROSOPHILA PROTEINS; EPIGENESIS, GENETIC; MODELS, GENETIC; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; RNA, SMALL INTERFERING; RNA-INDUCED SILENCING COMPLEX;

EID: 68549085526     PISSN: 00917451     EISSN: None     Source Type: Book Series    
DOI: 10.1101/sqb.2008.73.056     Document Type: Review

References (42)

1. Aravin, A., Gaidatzis, D., Pfeffer, S., Lagos-Quintana, M., Landgraf, P., Iovino, N., Morris, P., Brownstein, M.J., Kuramochi-Miyagawa, S., Nakano, T., et al. 2006. A novel class of small RNAs bind to MILI protein in mouse testes. Nature 442: 203-207.
2. Brennecke, J., Aravin, A.A., Stark, A., Dus, M., Kellis, M., Sachidanandam, R., and Hannon, G.J. 2007. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 128: 1089-1103.
3. Brower-Toland, B., Findley, S.D., Jiang, L., Liu, L., Yin, H., Dus, M., Zhou, P., Elgin, S.C., and Lin, H. 2007. Drosophila PIWI associates with chromatin and interacts directly with HP1a. Genes Dev. 21: 2300-2311.
4. Cox,D.N. 1999. "Function of the Drosophila piwi gene in the self-renewing division of germline stemcells and in germline development." Ph.D. thesis. Duke University, Durham, North Carolina.
5. Cox, D.N., Chao, A., and Lin, H. 2000. piwi encodes a nucleoplasmic factor whose activity modulates the number and division rate of germline stem cells. Development 127: 503-514.
6. Cox, D.N., Chao, A., Baker, J., Chang, L., Qiao, D., and Lin, H. 1998. A novel class of evolutionarily conserved genes defined by piwi are essential for stem cell self-renewal. Genes Dev. 12: 3715-3727.
7. Deng, W. and Lin, H. 2002. miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis. Dev. Cell 2: 819-830.
8. Girard, A. and Hannon, G.J. 2008. Conserved themes in small-RNA-mediated transposon control. Trends Cell Biol. 18: 136-148.
9. Girard, A., Sachidanandam, R., Hannon, G.J., and Carmell, M.A. 2006. A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature 442: 199-202.
10. Grivna, S.T., Beyret, E.,Wang, Z., and Lin,H. 2006.Anovel class of small RNAs in mouse spermatogenic cells. Genes Dev. 20: 1709-1714.
11. Harris, A.N. and Macdonald, P.M. 2001. aubergine encodes a Drosophila polar granule component required for pole cell formation and related to eIF2C. Development 128: 2823-2832.
12. Hediger, F. and Gasser, S.M. 2006. Heterochromatin protein 1: Don't judge the book by its cover! Curr. Opin. Genet. Dev. 16: 143-150.
13. Hiragami, K. and Festenstein, R. 2005. Heterochromatin protein 1: A pervasive controlling influence. Cell. Mol. Life Sci. 62: 2711-2726.
14. James, T.C., Eissenberg, J.C., Craig, C., Dietrich, V., Hobson, A., and Elgin, S.C. 1989. Distribution patterns of HP1, a heterochromatin-associated nonhistone chromosomal protein of Drosophila. Eur. J. Cell Biol. 50: 170-180.
15. Kim, V.N. 2006. Small RNAs just got bigger: Piwi-interacting RNAs (piRNAs) in mammalian testes. Genes Dev. 20: 1993-1997.
16. Kuramochi-Miyagawa, S., Kimura, T., Ijiri, T.W., Isobe, T., Asada, N., Fujita, Y., Ikawa, M., Iwai, N., Okabe, M., Deng, W., Lin, H., Matsuda, Y., and Nakano, T. 2004. Mili, a mammalian member of piwi family gene, is essential for spermatogenesis. Development 131: 839-849.
17. Lau, N.C., Seto, A.G., Kim, J., Kuramochi-Miyagawa, S., Nakano, T., Bartel, D.P., and Kingston, R.E. 2006. Characterization of the piRNA complex from rat testes. Science 313: 363-367.
18. Lechner, M.S., Schultz, D.C., Negorev, D., Maul, G.G., and Rauscher III, F.J. 2005. The mammalian heterochromatin protein 1 binds diverse nuclear proteins through a common motif that targets the chromoshadow domain. Biochem. Biophys. Res. Commun. 331: 929-937.
19. Liu, J., Carmell, M.A., Rivas, F.V., Marsden, C.G., Thomson, J.M., Song, J.J., Hammond, S.M., Joshua-Tor, L., and Hannon, G.J. 2004. Argonaute2 is the catalytic engine of mammalian RNAi. Science 305: 1437-1441.
20. Liu, X., Sun, Y., Guo, J., Ma, H., Li, J., Dong, B., Jin, G., Zhang, J., Wu, J., Meng, L., and Shou, C. 2006. Expression of hiwi gene in human gastric cancer was associated with proliferation of cancer cells. Int. J. Cancer 118: 1922-1929.
21. Megosh, H.B., Cox, D.N., Campbell, C., and Lin, H. 2006. The role of PIWI and the miRNA machinery in Drosophila germline determination. Curr. Biol. 16: 1884-1894.
22. Motamedi, M.R., Verdel, A., Colmenares, S.U., Gerber, S.A., Gygi, S.P., and Moazed, D. 2004. Two RNAi complexes, RITS and RDRC, physically interact and localize to noncoding centromeric RNAs. Cell 119: 789-802.
23. Noma, K., Sugiyama, T., Cam, H., Verdel, A., Zofall, M., Jia, S., Moazed, D., and Grewal, S.I. 2004. RITS acts in cis to promote RNA interference-mediated transcriptional and post-transcriptional silencing. Nat. Genet. 36: 1174-1180.
24. Palakodeti, D., Smielewska, M., Lu, Y.C., Yeo, G.W., and Graveley, B.R. 2008. The PIWI proteins SMEDWI-2 and SMEDWI-3 are required for stem cell function and piRNA expression in planarians. RNA 14: 1174-1186.
25. Pal-Bhadra,M., Leibovitch, B.A., Gandhi, S.G., Rao,M., Bhadra, U., Birchler, J.A., and Elgin, S.C. 2004. Heterochromatic silencing and HP1 localization in Drosophila are dependent on the RNAi machinery. Science 303: 669-672.
26. Qiao, D., Zeeman, A.M., Deng, W., Looijenga, L.H., and Lin, H. 2002. Molecular characterization of hiwi, a human member of the piwi gene family whose overexpression is correlated to seminomas. Oncogene 21: 3988-3999.
27. Reddien, P.W., Oviedo, N.J., Jennings, J.R., Jenkin, J.C., and Sanchez Alvarado, A. 2005. SMEDWI-2 is a PIWI-like protein that regulates planarian stem cells. Science 310: 1327-1330.
28. Rossi, L., Salvetti, A., Lena, A., Batistoni, R., Deri, P., Pugliesi, C., Loreti, E., and Gremigni, V. 2006. DjPiwi-1, a member of the PAZ-Piwi gene family, defines a subpopulation of planarian stem cells. Dev. Genes Evol. 216: 335-346.
29. Saito, K., Nishida, K.M., Mori, T., Kawamura, Y., Miyoshi, K., Nagami, T., Siomi, H., and Siomi, M.C. 2006. Specific association of Piwi with rasiRNAs derived from retrotransposon and heterochromatic regions in the Drosophila genome. Genes Dev. 20: 2214-2222.
30. + stem cells express the hiwi gene, a human homologue of the Drosophila gene piwi. Blood 97: 426-434.
31. Smothers, J.F. and Henikoff, S. 2000. The HP1 chromo shadow domain binds a consensus peptide pentamer. Curr. Biol. 10: 27-30.
32. Sugiyama, T., Cam, H., Verdel, A., Moazed, D., and Grewal, S.I. 2005. RNA-dependent RNA polymerase is an essential component of a self-enforcing loop coupling heterochromatin assembly to siRNA production. Proc. Natl. Acad. Sci. 102: 152-157.
33. Surani, M.A. 2001. Reprogramming of genome function through epigenetic inheritance. Nature 414: 122-128.
34. Thiru, A., Nietlispach, D., Mott, H.R., Okuwaki, M., Lyon, D., Nielsen, P.R., Hirshberg,M., Verreault, A.,Murzina, N.V., and Laue, E.D. 2004. Structural basis of HP1/PXVXL motif peptide interactions and HP1 localisation to heterochromatin. EMBO J. 23: 489-499.
35. Unhavaithaya, Y., Hao, Y., Beyret, E., Yin, H., Kuramochi-Miyagawa, S., Nakano, T., and Lin, H. 2009. MILI, a piRNA binding protein, is required for germline stem cell self-renewal and appears to positively regulate translation. J. Biol. Chem. (in press).
36. Vagin, V.V., Sigova, A., Li, C., Seitz, H., Gvozdev, V., and Zamore, P.D. 2006. A distinct small RNA pathway silences selfish genetic elements in the germline. Science 313: 320-324.
37. Verdel, A., Jia, S., Gerber, S., Sugiyama, T., Gygi, S., Grewal, S.I., andMoazed, D. 2004. RNAi-mediated targeting of heterochromatin by the RITS complex. Science 303: 672-676.
38. Volpe, T.A., Kidner, C., Hall, I.M., Teng, G., Grewal, S.I., and Martienssen, R.A. 2002. Regulation of heterochromatic silencing and histoneH3 lysine-9methylation by RNAi. Science 297: 1833-1837.
39. Wang, Y., Juranek, S., Li, H., Sheng, G., Tuschl, T., and Patel, D.J. 2008. Structure of an argonaute silencing complex with a seed-containing guide DNA and target RNA duplex. Nature 456: 921-926.
40. Wassenegger, M. 2005. The role of the RNAi machinery in heterochromatin formation. Cell 122: 13-16.
41. Watanabe, T., Takeda, A., Tsukiyama, T., Mise, K., Okuno, T., Sasaki, H., Minami, N., and Imai, H. 2006. Identification and characterization of two novel classes of small RNAs in the mouse germline: Retrotransposon-derived siRNAs in oocytes and germline small RNAs in testes. GenesDev. 20: 1732-1743.
42. Yin, H. and Lin, H. 2007. An epigenetic activation role of Piwi and a Piwi-associated piRNA in Drosophila melanogaster. Nature 450: 304-308.