The Role of Dicer in DNA Damage Repair
Abstract
:1. Introduction
2. DNA Damage is Accumulated in Dicer-Deficient Cells
3. Molecular Mechanisms by Which Loss of Dicer Leads to DNA Damage
3.1. Accumulation of DNA Damage in Dicer-Deficient Cells Is Attributed to Reduced Efficiency of DNA Damage Repair
3.2. Is Accumulation of DNA Damage in Dicer-Deficient Cells the Consequence of Heterochromatin Decondensation?
3.3. Is Accumulation of DNA Damage in Dicer-Deficient Cells the Consequence of Transposon Activation?
3.4. Is Accumulation of DNA Damage in Dicer-Deficient Cells the Consequence of miRNA Downregulation?
4. Dicer, DNA Damage, and Tumorigenesis
5. Prospects
Acknowledgements
References
- Fire, A.; Xu, S.; Montgomery, M.K.; Kostas, S.A.; Driver, S.E.; Mello, C.C. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 1998, 391, 806–811. [Google Scholar]
- Hamilton, A.J.; Baulcombe, D.C. A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 1999, 286, 950–952. [Google Scholar]
- Hammond, S.M.; Bernstein, E.; Beach, D.; Hannon, G.J. An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells. Nature 2000, 404, 293–296. [Google Scholar]
- Zamore, P.D.; Tuschl, T.; Sharp, P.A.; Bartel, D.P. RNAi: Double-stranded RNA directs the ATP-dependent cleavage of mRNA at 21 to 23 nucleotide intervals. Cell 2000, 101, 25–33. [Google Scholar]
- Bernstein, E.; Caudy, A.A.; Hammond, S.M.; Hannon, G.J. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 2001, 409, 363–366. [Google Scholar]
- Kim, V.N.; Han, J.; Siomi, M.C. Biogenesis of small RNAs in animals. Nat. Rev. Mol. Cell Biol 2009, 10, 126–139. [Google Scholar]
- Lee, Y.; Kim, M.; Han, J.; Yeom, K.H.; Lee, S.; Baek, S.H.; Kim, V.N. MicroRNA genes are transcribed by RNA polymerase II. EMBO J 2004, 23, 4051–4060. [Google Scholar]
- Lee, Y.; Ahn, C.; Han, J.; Choi, H.; Kim, J.; Yim, J.; Lee, J.; Provost, P.; Radmark, O.; Kim, S.; et al. The nuclear RNase III Drosha initiates microRNA processing. Nature 2003, 425, 415–419. [Google Scholar]
- Lejeune, E.; Allshire, R.C. Common ground: Small RNA programming and chromatin modifications. Curr. Opin. Cell Biol 2011, 23, 258–265. [Google Scholar]
- Buhler, M.; Moazed, D. Transcription and RNAi in heterochromatic gene silencing. Nat. Struct. Mol. Biol 2007, 14, 1041–1048. [Google Scholar]
- Locke, S.M.; Martienssen, R.A. Slicing and spreading of heterochromatic silencing by RNA interference. Cold Spring Harb. Symp. Quant. Biol 2006, 71, 497–503. [Google Scholar]
- Peng, J.C.; Karpen, G.H. H3K9 methylation and RNA interference regulate nucleolar organization and repeated DNA stability. Nat. Cell Biol 2007, 9, 25–35. [Google Scholar]
- Jorgensen, H.F.; Azuara, V.; Amoils, S.; Spivakov, M.; Terry, A.; Nesterova, T.; Cobb, B.S.; Ramsahoye, B.; Merkenschlager, M.; Fisher, A.G. The impact of chromatin modifiers on the timing of locus replication in mouse embryonic stem cells. Genome Biol 2007, 8, R169. [Google Scholar]
- Sancar, A.; Lindsey-Boltz, L.A.; Unsal-Kacmaz, K.; Linn, S. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu. Rev. Biochem 2004, 73, 39–85. [Google Scholar]
- Plasterk, R.H. RNA silencing: The genome’s immune system. Science 2002, 296, 1263–1265. [Google Scholar]
- Fire, A. Nucleic acid structure and intracellular immunity: Some recent ideas from the world of RNAi. Q. Rev. Biophys 2005, 38, 303–309. [Google Scholar]
- Sijen, T.; Plasterk, R.H. Transposon silencing in the Caenorhabditis elegans germ line by natural RNAi. Nature 2003, 426, 310–314. [Google Scholar]
- Ketting, R.F.; Haverkamp, T.H.; van Luenen, H.G.; Plasterk, R.H. Mut-7 of C. elegans, required for transposon silencing and RNA interference, is a homolog of Werner syndrome helicase and RNaseD. Cell 1999, 99, 133–141. [Google Scholar]
- Tabara, H.; Sarkissian, M.; Kelly, W.G.; Fleenor, J.; Grishok, A.; Timmons, L.; Fire, A.; Mello, C.C. The rde-1 gene, RNA interference, and transposon silencing in C. elegans. Cell 1999, 99, 123–132. [Google Scholar]
- Gasior, S.L.; Wakeman, T.P.; Xu, B.; Deininger, P.L. The human LINE-1 retrotransposon creates DNA double-strand breaks. J. Mol. Biol 2006, 357, 1383–1393. [Google Scholar]
- Tang, K.F.; Ren, H.; Cao, J.; Zeng, G.L.; Xie, J.; Chen, M.; Wang, L.; He, C.X. Decreased Dicer expression elicits DNA damage and up-regulation of MICA and MICB. J. Cell. Biol 2008, 182, 233–239. [Google Scholar]
- Foster, E.R.; Downs, J.A. Histone H2A phosphorylation in DNA double-strand break repair. FEBS J 2005, 272, 3231–3240. [Google Scholar]
- Zou, Y.; Liu, Y.; Wu, X.; Shell, S.M. Functions of human replication protein A (RPA): From DNA replication to DNA damage and stress responses. J. Cell. Physiol 2006, 208, 267–273. [Google Scholar]
- Peng, J.C.; Karpen, G.H. Heterochromatic genome stability requires regulators of histone H3 K9 methylation. PLoS Genet 2009, 5, e1000435. [Google Scholar]
- Mudhasani, R.; Zhu, Z.; Hutvagner, G.; Eischen, C.M.; Lyle, S.; Hall, L.L.; Lawrence, J.B.; Imbalzano, A.N.; Jones, S.N. Loss of miRNA biogenesis induces p19Arf-p53 signaling and senescence in primary cells. J. Cell. Biol 2008, 181, 1055–1063. [Google Scholar]
- Teta, M.; Choi, Y.S.; Okegbe, T.; Wong, G.; Tam, O.H.; Chong, M.M.; Seykora, J.T.; Nagy, A.; Littman, D.R.; Andl, T.; et al. Inducible deletion of epidermal Dicer and Drosha reveals multiple functions for miRNAs in postnatal skin. Development 2012, 139, 1405–1416. [Google Scholar]
- Kraemer, A.; Anastasov, N.; Angermeier, M.; Winkler, K.; Atkinson, M.J.; Moertl, S. MicroRNA-mediated processes are essential for the cellular radiation response. Radiat. Res 2011, 176, 575–586. [Google Scholar]
- Pothof, J.; Verkaik, N.S.; van IJcken, W.; Wiemer, E.A.; Ta, V.T.; van der Horst, G.T.; Jaspers, N.G.; van Gent, D.C.; Hoeijmakers, J.H.; Persengiev, S.P. MicroRNA-mediated gene silencing modulates the UV-induced DNA-damage response. EMBO J 2009, 28, 2090–2099. [Google Scholar]
- Wei, W.; Ba, Z.; Gao, M.; Wu, Y.; Ma, Y.; Amiard, S.; White, C.I.; Danielsen, J.M.R.; Yang, Y.G.; Qi, Y. A role for small RNAs in DNA double-strand break repair. Cell 2012, 149, 101–112. [Google Scholar]
- Francia, S.; Michelini, F.; Saxena, A.; Tang, D.; de Hoon, M.; Anelli, V.; Mione, M.; Carninci, P.; d’Adda di Fagagna, F. Site-specific DICER and DROSHA RNA products control the DNA-damage response. Nature 2012, 488, 231–235. [Google Scholar]
- Soria, G.; Polo, S.E.; Almouzni, G. Prime, repair, restore: The active role of chromatin in the DNA damage response. Mol. Cell 2012, 46, 722–734. [Google Scholar]
- Miller, K.M.; Jackson, S.P. Histone marks: Repairing DNA breaks within the context of chromatin. Biochem. Soc. Trans 2012, 40, 370–376. [Google Scholar]
- Peng, J.C.; Karpen, G.H. Epigenetic regulation of heterochromatic DNA stability. Curr. Opin. Genet. Dev 2008, 18, 204–211. [Google Scholar]
- Tang, K.F.; He, C.X.; Zeng, G.L.; Wu, J.; Song, G.B.; Shi, Y.S.; Zhang, W.G.; Huang, A.L.; Steinle, A.; Ren, H. Induction of MHC class I-related chain B (MICB) by 5-aza-2′-deoxycytidine. Biochem. Biophys. Res. Commun 2008, 370, 578–583. [Google Scholar]
- Tang, K.-F. Dicer regulates the expression of major histocompatibility complex (MHC) class I chain-related genes A and B. In Histocompatibility; InTech: Rijeka, Croatia, 2012; pp. 73–92. [Google Scholar]
- Mann, J.R.; Mattiske, D.M. RNA interference in mammalian DNA methylation. Biochem. Cell. Biol 2012, 90, 70–77. [Google Scholar]
- Babiarz, J.E.; Ruby, J.G.; Wang, Y.; Bartel, D.P.; Blelloch, R. Mouse ES cells express endogenous shRNAs, siRNAs, and other Microprocessor-independent, Dicer-dependent small RNAs. Genes Dev 2008, 22, 2773–2785. [Google Scholar]
- Calabrese, J.M.; Seila, A.C.; Yeo, G.W.; Sharp, P.A. RNA sequence analysis defines Dicer’s role in mouse embryonic stem cells. Proc. Natl. Acad. Sci. USA 2007, 104, 18097–18102. [Google Scholar]
- Tam, O.H.; Aravin, A.A.; Stein, P.; Girard, A.; Murchison, E.P.; Cheloufi, S.; Hodges, E.; Anger, M.; Sachidanandam, R.; Schultz, R.M.; et al. Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes. Nature 2008, 453, 534–538. [Google Scholar]
- Watanabe, T.; Totoki, Y.; Toyoda, A.; Kaneda, M.; Kuramochi-Miyagawa, S.; Obata, Y.; Chiba, H.; Kohara, Y.; Kono, T.; Nakano, T.; et al. Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes. Nature 2008, 453, 539–543. [Google Scholar]
- Ohnishi, Y.; Totoki, Y.; Toyoda, A.; Watanabe, T.; Yamamoto, Y.; Tokunaga, K.; Sakaki, Y.; Sasaki, H.; Hohjoh, H. Active role of small non-coding RNAs derived from SINE/B1 retrotransposon during early mouse development. Mol. Biol. Rep 2012, 39, 903–909. [Google Scholar]
- Kaneko, H.; Dridi, S.; Tarallo, V.; Gelfand, B.D.; Fowler, B.J.; Cho, W.G.; Kleinman, M.E.; Ponicsan, S.L.; Hauswirth, W.W.; Chiodo, V.A.; et al. DICER1 deficit induces Alu RNA toxicity in age-related macular degeneration. Nature 2011, 471, 325–330. [Google Scholar]
- Ren, Y.F.; Li, G.; Wu, J.; Xue, Y.F.; Song, Y.J.; Lv, L.; Zhang, X.J.; Tang, K.F. Dicer-Dependent Biogenesis of Small RNAs Derived from 7SL RNA. PLoS One 2012, 7, e40705. [Google Scholar]
- Sokolov, M.V.; Panyutin, I.V.; Neumann, R.D. Unraveling the global microRNAome responses to ionizing radiation in human embryonic stem cells. PLoS One 2012, 7, e31028. [Google Scholar]
- Maes, O.C.; An, J.; Sarojini, H.; Wu, H.; Wang, E. Changes in MicroRNA expression patterns in human fibroblasts after low-LET radiation. J. Cell. Biochem 2008, 105, 824–834. [Google Scholar]
- Simone, N.L.; Soule, B.P.; Ly, D.; Saleh, A.D.; Savage, J.E.; Degraff, W.; Cook, J.; Harris, C.C.; Gius, D.; Mitchell, J.B. Ionizing radiation-induced oxidative stress alters miRNA expression. PLoS One 2009, 4, e6377. [Google Scholar]
- Hu, H.; Gatti, R.A. MicroRNAs: New players in the DNA damage response. J. Mol. Cell. Biol 2011, 3, 151–158. [Google Scholar]
- Chang, T.C.; Wentzel, E.A.; Kent, O.A.; Ramachandran, K.; Mullendore, M.; Lee, K.H.; Feldmann, G.; Yamakuchi, M.; Ferlito, M.; Lowenstein, C.J.; et al. Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis. Mol. Cell 2007, 26, 745–752. [Google Scholar]
- Raver-Shapira, N.; Marciano, E.; Meiri, E.; Spector, Y.; Rosenfeld, N.; Moskovits, N.; Bentwich, Z.; Oren, M. Transcriptional activation of miR-34a contributes to p53-mediated apoptosis. Mol. Cell 2007, 26, 731–743. [Google Scholar]
- Suzuki, H.I.; Yamagata, K.; Sugimoto, K.; Iwamoto, T.; Kato, S.; Miyazono, K. Modulation of microRNA processing by p53. Nature 2009, 460, 529–533. [Google Scholar]
- Zhang, X.; Wan, G.; Berger, F.G.; He, X.; Lu, X. The ATM kinase induces microRNA biogenesis in the DNA damage response. Mol. Cell 2011, 41, 371–383. [Google Scholar]
- Pothof, J.; Verkaik, N.S.; Hoeijmakers, J.H.; van Gent, D.C. MicroRNA responses and stress granule formation modulate the DNA damage response. Cell Cycle 2009, 8, 3462–3468. [Google Scholar]
- Lal, A.; Pan, Y.; Navarro, F.; Dykxhoorn, D.M.; Moreau, L.; Meire, E.; Bentwich, Z.; Lieberman, J.; Chowdhury, D. miR-24-mediated downregulation of H2AX suppresses DNA repair in terminally differentiated blood cells. Nat. Struct. Mol. Biol 2009, 16, 492–498. [Google Scholar]
- Song, L.; Lin, C.; Wu, Z.; Gong, H.; Zeng, Y.; Wu, J.; Li, M.; Li, J. miR-18a impairs DNA damage response through downregulation of ataxia telangiectasia mutated (ATM) kinase. PLoS One 2011, 6, e25454. [Google Scholar]
- Hu, H.; Du, L.; Nagabayashi, G.; Seeger, R.C.; Gatti, R.A. ATM is down-regulated by N-myc-regulated microRNA-421. Proc. Natl. Acad. Sci. USA 2010, 107, 1506–1511. [Google Scholar]
- Lu, J.; Getz, G.; Miska, E.A.; Alvarez-Saavedra, E.; Lamb, J.; Peck, D.; Sweet-Cordero, A.; Ebert, B.L.; Mak, R.H.; Ferrando, A.A.; et al. MicroRNA expression profiles classify human cancers. Nature 2005, 435, 834–838. [Google Scholar]
- Merritt, W.M.; Lin, Y.G.; Han, L.Y.; Kamat, A.A.; Spannuth, W.A.; Schmandt, R.; Urbauer, D.; Pennacchio, L.A.; Cheng, J.F.; Nick, A.M.; et al. Dicer, Drosha, and outcomes in patients with ovarian cancer. New Engl. J. Med 2008, 359, 2641–2650. [Google Scholar]
- Ma, Z.; Swede, H.; Cassarino, D.; Fleming, E.; Fire, A.; Dadras, S.S. Up-regulated Dicer expression in patients with cutaneous melanoma. PLoS One 2011, 6, e20494. [Google Scholar]
- Wu, J.F.; Shen, W.; Liu, N.Z.; Zeng, G.L.; Yang, M.; Zuo, G.Q.; Gan, X.N.; Ren, H.; Tang, K.F. Down-regulation of Dicer in hepatocellular carcinoma. Med. Oncol 2011, 28, 804–809. [Google Scholar]
- Kumar, M.S.; Pester, R.E.; Chen, C.Y.; Lane, K.; Chin, C.; Lu, J.; Kirsch, D.G.; Golub, T.R.; Jacks, T. Dicer1 functions as a haploinsufficient tumor suppressor. Genes Dev 2009, 23, 2700–2704. [Google Scholar]
- Heravi-Moussavi, A.; Anglesio, M.S.; Cheng, S.W.; Senz, J.; Yang, W.; Prentice, L.; Fejes, A.P.; Chow, C.; Tone, A.; Kalloger, S.E.; et al. Recurrent somatic DICER1 mutations in nonepithelial ovarian cancers. N. Engl. J. Med 2012, 366, 234–242. [Google Scholar]
- Bartkova, J.; Horejsi, Z.; Koed, K.; Kramer, A.; Tort, F.; Zieger, K.; Guldberg, P.; Sehested, M.; Nesland, J.M.; Lukas, C.; et al. DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 2005, 434, 864–870. [Google Scholar]
- Bartkova, J.; Rezaei, N.; Liontos, M.; Karakaidos, P.; Kletsas, D.; Issaeva, N.; Vassiliou, L.V.; Kolettas, E.; Niforou, K.; Zoumpourlis, V.C.; et al. Oncogene-induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints. Nature 2006, 444, 633–637. [Google Scholar]
- DiTullio, R.A., Jr; Mochan, T.A.; Venere, M.; Bartkova, J.; Sehested, M.; Bartek, J.; Halazonetis, T.D. 53BP1 functions in an ATM-dependent checkpoint pathway that is constitutively activated in human cancer. Nat. Cell Biol. 2002, 4, 998–1002. [Google Scholar]
- Gorgoulis, V.G.; Vassiliou, L.V.; Karakaidos, P.; Zacharatos, P.; Kotsinas, A.; Liloglou, T.; Venere, M.; Ditullio, R.A., Jr; Kastrinakis, N.G.; Levy, B.; et al. Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 2005, 434, 907–913. [Google Scholar]
- Kumar, M.S.; Lu, J.; Mercer, K.L.; Golub, T.R.; Jacks, T. Impaired microRNA processing enhances cellular transformation and tumorigenesis. Nat. Genet 2007, 39, 673–677. [Google Scholar]
- Ravi, A.; Gurtan, A.M.; Kumar, M.S.; Bhutkar, A.; Chin, C.; Lu, V.; Lees, J.A.; Jacks, T.; Sharp, P.A. Proliferation and tumorigenesis of a murine sarcoma cell line in the absence of DICER1. Cancer Cell 2012, 21, 848–855. [Google Scholar]
- Sekine, S.; Ogawa, R.; Ito, R.; Hiraoka, N.; McManus, M.T.; Kanai, Y.; Hebrok, M. Disruption of Dicer1 induces dysregulated fetal gene expression and promotes hepatocarcinogenesis. Gastroenterology 2009, 136, 2304–2315. [Google Scholar]
- Rodriguez, W.; Jin, L.; Janssens, V.; Pierreux, C.; Hick, A.C.; Urizar, E.; Costagliola, S. Deletion of the RNaseIII enzyme dicer in thyroid follicular cells causes hypothyroidism with signs of neoplastic alterations. PLoS One 2012, 7, e29929. [Google Scholar]
- Kim, J.; Coffey, D.M.; Creighton, C.J.; Yu, Z.; Hawkins, S.M.; Matzuk, M.M. High-grade serous ovarian cancer arises from fallopian tube in a mouse model. Proc. Natl. Acad. Sci. USA 2012, 109, 3921–3926. [Google Scholar]
- Wouters, M.D.; van Gent, D.C.; Hoeijmakers, J.H.; Pothof, J. MicroRNAs, the DNA damage response and cancer. Mutat. Res 2011, 717, 54–66. [Google Scholar]
- Wu, J.; Wu, G.; Lv, L.; Ren, Y.F.; Zhang, X.J.; Xue, Y.F.; Li, G.; Lu, X.; Sun, Z.; Tang, K.F. MicroRNA-34a inhibits migration and invasion of colon cancer cells via targeting to Fra-1. Carcinogenesis 2012, 33, 519–528. [Google Scholar]
© 2012 by the authors; licensee Molecular Diversity Preservation International, Basel, Switzerland. This article is an open-access article distributed under the terms and conditions of the Creative Commons Attribution license (http://creativecommons.org/licenses/by/3.0/).
Share and Cite
Tang, K.-F.; Ren, H. The Role of Dicer in DNA Damage Repair. Int. J. Mol. Sci. 2012, 13, 16769-16778. https://doi.org/10.3390/ijms131216769
Tang K-F, Ren H. The Role of Dicer in DNA Damage Repair. International Journal of Molecular Sciences. 2012; 13(12):16769-16778. https://doi.org/10.3390/ijms131216769
Chicago/Turabian StyleTang, Kai-Fu, and Hong Ren. 2012. "The Role of Dicer in DNA Damage Repair" International Journal of Molecular Sciences 13, no. 12: 16769-16778. https://doi.org/10.3390/ijms131216769