BMB Reports

생화학분자생물학회 (Korean Society for Biochemistry and Molecular Biology)
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Identification of piRNAs in Hela cells by massive parallel sequencing

  • Lu, Yilu (Department of Medical Genetics and Division of Morbid Genomics, State Key Laboratory of Biotherapy, West China Hospital, Sichuan University) ;
  • Li, Chao (Department of Medical Genetics and Division of Morbid Genomics, State Key Laboratory of Biotherapy, West China Hospital, Sichuan University) ;
  • Zhang, Kun (Department of Medical Genetics and Division of Morbid Genomics, State Key Laboratory of Biotherapy, West China Hospital, Sichuan University) ;
  • Sun, Huaqin (Department of Medical Genetics and Division of Morbid Genomics, State Key Laboratory of Biotherapy, West China Hospital, Sichuan University) ;
  • Tao, Dachang (Department of Medical Genetics and Division of Morbid Genomics, State Key Laboratory of Biotherapy, West China Hospital, Sichuan University) ;
  • Liu, Yunqiang (Department of Medical Genetics and Division of Morbid Genomics, State Key Laboratory of Biotherapy, West China Hospital, Sichuan University) ;
  • Zhang, Sizong (Department of Medical Genetics and Division of Morbid Genomics, State Key Laboratory of Biotherapy, West China Hospital, Sichuan University) ;
  • Ma, Yongxin (Department of Medical Genetics and Division of Morbid Genomics, State Key Laboratory of Biotherapy, West China Hospital, Sichuan University)
  • 투고 : 2010.07.05
  • 심사 : 2010.08.06
  • 발행 : 2010.09.30
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초록

Piwi proteins and Piwi-interacting RNAs (piRNAs) have been implicated in transposon control in germline from Drosophila to mammals. To examine the profile of small RNA expression in human cancer cells and explore difference in small RNA transcriptome, small RNA libraries prepared from wildtype, HILI overexpressed and HILI knockdowned Hela cells were sequenced using Solexa technology. piRNAs and other repeat-associated small RNAs were observed in Hela cells. By using in situ hybridization, piR-49322 was localized in the nucleolus and around the periphery of nuclear membrane in Hela cells. Following the overexpression of HILI, the retrotransposon elements LINE1 was significantly repressed, while LINE1-associated small RNAs decreased in abundance. The present study demonstrated that HILI along with piRNAs plays a role in LINE1 suppression in Hela cancer cell line.

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참고문헌

  1. Aravin, A. A., Hannon, G. J. and Brennecke, J. (2007) The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science 318, 761-764. https://doi.org/10.1126/science.1146484
  2. Zamore, P. D. and Haley, B. (2005) Ribo-gnome: the big world of small RNAs. Science 309, 1519-1524. https://doi.org/10.1126/science.1111444
  3. Carmell, M. A., Xuan, Z., Zhang, M. Q., and Hannon, G. J. (2002) The Argonaute family: tentacles that reach into RNAi, developmental control, stem cell maintenance, and tumorigenesis. Genes Dev. 16, 2733-2742. https://doi.org/10.1101/gad.1026102
  4. Farazi, T. A., Juranek, S. A. and Tuschl, T. (2008) The growing catalog of small RNAs and their association with distinct Argonaute/Piwi family members. Development 135, 1201-1214. https://doi.org/10.1242/dev.005629
  5. Houwing, S., Kamminga, L. M., Berezikov, E., Cronembold, D., Girard, A., van den Elst, H., Filippov, D. V., Blaser, H., Raz, E., Moens, C. B., Plasterk, R. H., Hannon, G. J., Draper, B. W. and Ketting, R. F. (2007) A role for Piwi and piRNAs in germ cell maintenance and transposon silencing in zebrafish. Cell 129, 69-83. https://doi.org/10.1016/j.cell.2007.03.026
  6. Seto, A. G., Kingston, R. E. and Lau, N. C. (2007) The coming of age for Piwi proteins. Mol. Cell 26, 603-609. https://doi.org/10.1016/j.molcel.2007.05.021
  7. 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 selfrenewal. Genes Dev. 12, 3715- 3727. https://doi.org/10.1101/gad.12.23.3715
  8. 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.
  9. Carmell, M. A., Girard, A. l., van de Kant, H. J., Bourc'his, D., Bestor, T. H., de Rooij, D. G. and Hannon, G. J. (2007) MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline. Dev. Cell 12, 503-514. https://doi.org/10.1016/j.devcel.2007.03.001
  10. Deng, W. and Lin, H. (2002) Miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis. Dev. Cell 2, 819-830. https://doi.org/10.1016/S1534-5807(02)00165-X
  11. 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. https://doi.org/10.1242/dev.00973
  12. Aravin, A., Gaidatzis, D., Pfeffer, S., Lagos-Quintana, M., Landgraf, P., Iovino, N., Morris, P., Brownstein, M. J., Kuramochi-Miyagawa, S., Nakano, T., Chien, M., Russo, J. J., Ju, J., Sheridan, R., Sander, C., Zavolan, M. and Tuschl, T. (2006) A novel class of small RNAs bind to MILI protein in mouse testes. Nature 442, 203-207.
  13. 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.
  14. Grivna, S. T., Beyret, E., Wang, Z. and Lin, H. (2006) A novel class of small RNAs in mouse spermatogenic cells. Genes Dev. 20, 1709-1714. https://doi.org/10.1101/gad.1434406
  15. 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. https://doi.org/10.1126/science.1130164
  16. Batista, P. J., Ruby, G., Claycomb, J. M., Chiang, R., Fahlgren, N., Kasschau, K. D., Chaves, D. A., Gu, W., Vasale, J. J., Duan, S., Conte, D. Jr., Luo, S., Schroth, G. P., Carrington, J. C., Bartel, D. P. and Mello, C. C. (2008) PRG-1 and 21U-RNAs interact to form the piRNA complex required for fertility in C. elegans. Mol. Cell 31, 67-78. https://doi.org/10.1016/j.molcel.2008.06.002
  17. 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, 1089-1903. https://doi.org/10.1016/j.cell.2007.01.043
  18. Das, P. P., Bagijn, M. P., Goldstein, L. D., Woolford, J. R., Lehrbach, N. J., Sapetschnig, A., Buhecha, H. R., Gilchrist, M. J., Howe, K. L., Stark, R., Matthews, N., Berezikov, E., Ketting, R. F., Tavare, S. and Miska, E. A. (2008) Piwi and piRNAs act upstream of an endogenous siRNA pathway to suppress Tc3 transposon mobility in the Caenorhabditis elegans germline. Mol. Cell 31, 79-90. https://doi.org/10.1016/j.molcel.2008.06.003
  19. Gunawardane, L. S., Saito, K., Nishida, K. M., Miyoshi, K., Kawamura, Y., Nagami, T., Siomi, H. and Siomi, M. C. (2007) A slicer-mediated mechanism for repeat-associated siRNA 5' end formation in Drosophila. Science 315, 1587-1590. https://doi.org/10.1126/science.1140494
  20. Klattenhoff, C. and Theurkauf, W. (2008) Biogenesis and germline functions of piRNAs. Development 135, 3-9. https://doi.org/10.1242/dev.006486
  21. Ruby, J. G., Jan, C., Player, C., Axtell, M. J., Lee, W., Nusbaum, C., Ge, H. and Bartel, D. P. (2006) Large-scale sequencing reveals 21U-RNAs and additional microRNAs and endogenous siRNAs in C. elegans. Cell 127, 1193-1207. https://doi.org/10.1016/j.cell.2006.10.040
  22. 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. https://doi.org/10.1126/science.1129333
  23. 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. Genes Dev. 20, 1732-1743. https://doi.org/10.1101/gad.1425706
  24. Lee, J. H., Engel, W and Nayernia, K. (2006) Stem cell protein Piwil2 modulates expression of murine spermatogonial stem cell expressed genes. Mol. Re-prod. Dev. 73, 173-179. https://doi.org/10.1002/mrd.20391
  25. Wang, J., Saxe, J. P., Tanaka, T., Chuma, S. and Lin, H. (2009) Mili interacts with tudor domain-containing protein 1 in regulating spermatogenesis. Curr. Biol. 19, 640-644. https://doi.org/10.1016/j.cub.2009.02.061
  26. Houwing, S., Berezikov, E. and Ketting, R. F. (2008) Zili is required for germ cell differentiation and meiosis in zebrafish. EMBO J. 27, 2702-2711. https://doi.org/10.1038/emboj.2008.204
  27. Lee, J. H., Schutte, D., Wulf, G., Fuzesi, L., Radzun, H. J., Schweyer, S., Engel, W. and Nayernia, K. (2006) Stem-cell protein Piwil2 is widely expressed in tumors and inhibits apoptosis through activation of Stat3/Bcl-XL pathway. Hum. Mol. Genet 15, 201-211. https://doi.org/10.1093/hmg/ddi430
  28. Aravin, A. A., Lagos-Quintana, M., Yalcin, A., Zavolan, M., Marks, D., Snyder, B., Gaasterland, T., Meyer, J. and Tuschl, T. (2003) The small RNA profile during Drosophila melanogaster development. Dev. Cell 5, 337-350. https://doi.org/10.1016/S1534-5807(03)00228-4
  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. https://doi.org/10.1101/gad.1454806
  30. Aravin, A. A., Sachidanandam, R., Bourc'his, D., Schaefer, C., Pezic, D., Toth, K. F., Bestor, T. and Hannon, G. J. (2008) A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol. Cell 31, 785-799. https://doi.org/10.1016/j.molcel.2008.09.003
  31. Kalmykova, A. I., Klenov, M. S. and Gvozdev, V. A. (2005) Argonaute protein PIWI controls mobilization of retrotransposons in the Drosophila male germline. Nucleic. Acids. Res. 33, 2052-2059. https://doi.org/10.1093/nar/gki323
  32. Kuramochi-Miyagawa, S., Watanabe, T., Gotoh, K., Totoki, Y., Toyoda, A., Ikawa, M., Asada, N., Kojima, K., Yamaguchi, Y., Ijiri, T. W., Hata, K., Li, E., Matsuda, Y., Kimura, T., Okabe, M., Sakaki, Y., Sasaki, H. and Nakano, T. (2008) DNA methylation of retrotransposon genes is regulated by Piwi family members MILI and MIWI2 in murine fetal testes. Genes Dev. 22, 908-917. https://doi.org/10.1101/gad.1640708

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  1. The expression of stem cell protein Piwil2 and piR-932 in breast cancer vol.22, pp.4, 2013, https://doi.org/10.1016/j.suronc.2013.07.001
  2. Concise Review: The Piwi-piRNA Axis: Pivotal Beyond Transposon Silencing vol.30, pp.12, 2012, https://doi.org/10.1002/stem.1237
  3. Detection of circulating tumor cells in peripheral blood from patients with gastric cancer using piRNAs as markers vol.44, pp.13, 2011, https://doi.org/10.1016/j.clinbiochem.2011.06.004
  4. Deep sequencing analysis of small non-coding RNAs reveals the diversity of microRNAs and piRNAs in the human epididymis vol.497, pp.2, 2012, https://doi.org/10.1016/j.gene.2012.01.038
  5. Databases and resources for human small non-coding RNAs vol.5, pp.3, 2011, https://doi.org/10.1186/1479-7364-5-3-192
  6. Profiling of the small RNA populations in human testicular germ cell tumors shows global loss of piRNAs vol.14, pp.1, 2015, https://doi.org/10.1186/s12943-015-0411-4
  7. Emerging roles for PIWI proteins in cancer vol.47, pp.5, 2015, https://doi.org/10.1093/abbs/gmv018
  8. Physiological and pathophysiological roles for phospholipase D vol.56, pp.12, 2015, https://doi.org/10.1194/jlr.R059220
  9. Identification of novel piRNAs in bladder cancer vol.356, pp.2, 2015, https://doi.org/10.1016/j.canlet.2014.10.004
  10. Noncoding RNAs in DNA Repair and Genome Integrity vol.20, pp.4, 2014, https://doi.org/10.1089/ars.2013.5514
  11. A SnoRNA-derived piRNA interacts with human interleukin-4 pre-mRNA and induces its decay in nuclear exosomes 2015, https://doi.org/10.1093/nar/gkv954
  12. Piwis and piwi-interacting RNAs in the epigenetics of cancer vol.113, pp.2, 2012, https://doi.org/10.1002/jcb.23363
  13. HILI destabilizes microtubules by suppressing phosphorylation and Gigaxonin-mediated degradation of TBCB vol.7, 2017, https://doi.org/10.1038/srep46376
  14. piR-651 and its function in 95-D lung cancer cells vol.4, pp.5, 2016, https://doi.org/10.3892/br.2016.628
  15. piRNA, the new non-coding RNA, is aberrantly expressed in human cancer cells vol.412, pp.17-18, 2011, https://doi.org/10.1016/j.cca.2011.05.015
  16. Altered expression of piRNAs and their relation with clinicopathologic features of breast cancer vol.15, pp.7, 2013, https://doi.org/10.1007/s12094-012-0966-0
  17. Non-Coding RNAs and Cancer vol.14, pp.8, 2013, https://doi.org/10.3390/ijms140817085
  18. Non-coding RNAs and diseases vol.47, pp.4, 2013, https://doi.org/10.1134/S0026893313040171
  19. An efficient and sensitive method for preparing cDNA libraries from scarce biological samples vol.43, pp.1, 2015, https://doi.org/10.1093/nar/gku637
  20. The human Piwi protein Hiwi2 associates with tRNA-derived piRNAs in somatic cells vol.42, pp.14, 2014, https://doi.org/10.1093/nar/gku620
  21. V-ELMpiRNAPred: Identification of human piRNAs by the voting-based extreme learning machine (V-ELM) with a new hybrid feature vol.15, pp.01, 2017, https://doi.org/10.1142/S0219720016500463
  22. The Piwi-piRNA pathway: road to immortality vol.16, pp.5, 2017, https://doi.org/10.1111/acel.12630
  23. Piwil2 Suppresses P53 by Inducing Phosphorylation of Signal Transducer and Activator of Transcription 3 in Tumor Cells vol.7, pp.1, 2012, https://doi.org/10.1371/journal.pone.0030999
  24. Novel dimensions of piRNAs in cancer vol.336, pp.1, 2013, https://doi.org/10.1016/j.canlet.2013.04.008
  25. Unique somatic and malignant expression patterns implicate PIWI-interacting RNAs in cancer-type specific biology vol.5, pp.1, 2015, https://doi.org/10.1038/srep10423
  26. Small Non-coding RNAs Govern Mammary Gland Tumorigenesis vol.17, pp.1, 2012, https://doi.org/10.1007/s10911-012-9246-4
  27. piR-823, a novel non-coding small RNA, demonstrates in vitro and in vivo tumor suppressive activity in human gastric cancer cells vol.315, pp.1, 2012, https://doi.org/10.1016/j.canlet.2011.10.004
  28. Small RNA Detection by in Situ Hybridization Methods vol.16, pp.6, 2015, https://doi.org/10.3390/ijms160613259
  29. Non-coding RNAs in human disease vol.12, pp.12, 2011, https://doi.org/10.1038/nrg3074
  30. piClust: A density based piRNA clustering algorithm vol.50, 2014, https://doi.org/10.1016/j.compbiolchem.2014.01.008
  31. The epigenetic regulation of HsMar1, a human DNA transposon vol.20, pp.1, 2019, https://doi.org/10.1186/s12863-019-0719-y