Functional involvement of Tudor and dPRMT5 in the piRNA processing pathway in Drosophila germlines
Open accessAbstract
In Drosophila, the PIWI proteins, Aubergine (Aub), AGO3, and Piwi are expressed in germlines and function in silencing transposons by associating with PIWI-interacting RNAs (piRNAs). Recent studies show that PIWI proteins contain symmetric dimethyl-arginines (sDMAs) and that dPRMT5/Capsuleen/DART5 is the modifying enzyme. Here, we show that Tudor (Tud), one of Tud domain-containing proteins, associates with Aub and AGO3, specifically through their sDMA modifications and that these three proteins form heteromeric complexes. piRNA precursor-like molecules are detected in these complexes. The expression levels of Aub and AGO3, along with their degree of sDMA modification, were not changed by tud mutations. However, the population of transposon-derived piRNAs associated with Aub and AGO3 was altered by tud mutations, whereas the total amounts of small RNAs on Aub and AGO3 was increased. Loss of dprmt5 did not change the stability of Aub, but impaired its association with Tud and lowered piRNA association with Aub. Thus, in germline cells, piRNAs are quality-controlled by dPRMT5 that modifies PIWI proteins, in tight association with Tud.
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csul interacts with histones, spliceosomal proteins and other small ribonucleoproteins and can affect protein-RNA affinity and intracellular localization of certain mRNAs.
“The gene csul interacts with histones, splicesosomal proteins and other small ribonucleoproteins and can affect protein–RNA affinity and intracellular localization of certain mRNAs (70–72).”
From Functional genomic screen and network analysis reveal novel modifiers of tauopathy dissociated from tau phosphorylation (2011) · cites this paper as [72]
The Introduction identifies Csul as dPRMT5 and discusses methylation of spliceosomal Sm proteins and snRNP assembly. The section ‘sDMA modification of Aub affects PIWI-piRNA loading’ reports effects on Aub’s association with piRNAs and Aub’s localization in nurse cells. Our copy does not establish Csul interactions with histones or other small ribonucleoproteins, or an effect on the intracellular localization of mRNAs; the localization result concerns a protein. (LLM, conf=0.85)
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Cites
Origins and Mechanisms of miRNAs and siRNAs
Carthew, R. W., & Sontheimer, E. J. (2009) · Cell · doi:10.1016/j.cell.2009.01.035 · Cited by 5,023 · see citing works
Biogenesis of small RNAs in animals
Kim, V. N., Han, J., & Siomi, M. C. (2009) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2632 · Cited by 3,181 · see citing works
Self-citationDiscrete Small RNA-Generating Loci as Master Regulators of Transposon Activity in Drosophila
Brennecke, J., Aravin, A. A., Stark, A., Dus, M., Kellis, M., Sachidanandam, R., & Hannon, G. J. (2007) · Cell · doi:10.1016/j.cell.2007.01.043 · Cited by 2,524 · see citing works
Protein Arginine Methylation in Mammals: Who, What, and Why
Bedford, M. T., & Clarke, S. G. (2009) · Molecular Cell · doi:10.1016/j.molcel.2008.12.013 · Cited by 1,810 · see citing works
A Distinct Small RNA Pathway Silences Selfish Genetic Elements in the Germline
Vagin, V. V., Sigova, A. A., Li, C., Seitz, H., Gvozdev, V. A., & Zamore, P. D. (2006) · Science · doi:10.1126/science.1129333 · Cited by 1,342 · see citing works
A Slicer-Mediated Mechanism for Repeat-Associated siRNA 5' End Formation in Drosophila
Gunawardane, L. S., Saito, K., Nishida, K. M., Miyoshi, K., Kawamura, Y., Nagami, T., Siomi, H., & Siomi, M. C. (2007) · Science · doi:10.1126/science.1140494 · Cited by 1,173 · see citing works
Self-citationA Role for Piwi and piRNAs in Germ Cell Maintenance and Transposon Silencing in Zebrafish
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., et al. (2007) · Cell · doi:10.1016/j.cell.2007.03.026 · Cited by 1,118 · see citing works
The Piwi-piRNA Pathway Provides an Adaptive Defense in the Transposon Arms Race
Aravin, A. A., Hannon, G. J., & Brennecke, J. (2007) · Science · doi:10.1126/science.1146484 · Cited by 1,096 · see citing works
Specialized piRNA Pathways Act in Germline and Somatic Tissues of the Drosophila Ovary
Malone, C. D., Brennecke, J., Dus, M., Stark, A., McCombie, W. R., Sachidanandam, R., & Hannon, G. J. (2009) · Cell · doi:10.1016/j.cell.2009.03.040 · Cited by 864 · see citing works
Small RNAs in transcriptional gene silencing and genome defence
Moazed, D. (2009) · Nature · doi:10.1038/nature07756 · Cited by 825 · see citing works
Purified Argonaute2 and an siRNA form recombinant human RISC
Rivas, F. V., Tolia, N. H., Song, J., Aragon, J. P., Liu, J., Hannon, G. J., & Joshua‐Tor, L. (2005) · Nature Structural & Molecular Biology · doi:10.1038/nsmb918 · Cited by 760 · see citing works
A three-dimensional view of the molecular machinery of RNA interference
Jínek, M., & Doudna, J. A. (2008) · Nature · doi:10.1038/nature07755 · Cited by 746 · see citing works
On the road to reading the RNA-interference code
Siomi, H., & Siomi, M. C. (2009) · Nature · doi:10.1038/nature07754 · Cited by 674 · see citing works
Self-citationSaito, K., Nishida, K. M., Mori, T., Kawamura, Y., Miyoshi, K., Nagami, T., Siomi, H., & Siomi, M. C. (2006) · Genes & Development · doi:10.1101/gad.1454806 · Cited by 648 · see citing works
Self-citationImproved northern blot method for enhanced detection of small RNA
Pall, G. S., & Hamilton, A. J. (2008) · Nature Protocols · doi:10.1038/nprot.2008.67 · Cited by 557 · see citing works
Essential Role for the SMN Complex in the Specificity of snRNP Assembly
Pellizzoni, L., Yong, J., & Dreyfuss, G. (2002) · Science · doi:10.1126/science.1074962 · Cited by 544 · see citing works
A <i>Drosophila</i> fragile X protein interacts with components of RNAi and ribosomal proteins
Ishizuka, A., Siomi, M. C., & Siomi, H. (2002) · Genes & Development · doi:10.1101/gad.1022002 · Cited by 486 · see citing works
Self-citationA regulatory circuit for piwi by the large Maf gene traffic jam in Drosophila
Saito, K., Inagaki, S., Mitsuyama, T., Kawamura, Y., Ono, Y., Sakota, E., Kotani, H., Asai, K., Siomi, H., & Siomi, M. C. (2009) · Nature · doi:10.1038/nature08501 · Cited by 440 · see citing works
Self-citationSlicer function of Drosophila Argonautes and its involvement in RISC formationPreprint
Miyoshi, K., Tsukumo, H., Nagami, T., Siomi, H., & Siomi, M. C. (2005) · Genes & Development · doi:10.1101/gad.1370605 · Cited by 402 · see citing works
Self-citationVagin, V. V., Wohlschlegel, J. A., Qu, J., Jónsson, Z. O., Huang, X., Chuma, S., Girard, A., Sachidanandam, R., Hannon, G. J., & Aravin, A. A. (2009) · Genes & Development · doi:10.1101/gad.1814809 · Cited by 313 · see citing works
Gene silencing mechanisms mediated by Aubergine–piRNA complexes in Drosophila male gonad
Nishida, K. M., Saito, K., Mori, T., Kawamura, Y., Nagami-Okada, T., Inagaki, S., Siomi, H., & Siomi, M. C. (2007) · RNA · doi:10.1261/rna.744307 · Cited by 264 · see citing works
Self-citationTudor Domains Bind Symmetrical Dimethylated Arginines
Côté, J., & Richard, S. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m414328200 · Cited by 261 · see citing works
Reuter, M., Chuma, S., Tanaka, T. S. T., Franz, T., Stark, A., & Pillai, R. S. (2009) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1615 · Cited by 256 · see citing works
Arginine methylation of Piwi proteins catalysed by dPRMT5 is required for Ago3 and Aub stability
Kirino, Y., Kim, N., Planell-Saguer, M. D., Khandros, E., Chiorean, S., Klein, P. S., Rigoutsos, I., Jongens, T. A., & Mourelatos, Z. (2009) · Nature Cell Biology · doi:10.1038/ncb1872 · Cited by 237 · see citing works
An Assembly Chaperone Collaborates with the SMN Complex to Generate Spliceosomal SnRNPs
Chari, A., Golas, M. M., Klingenhäger, M., Neuenkirchen, N., Sander, B. O., Englbrecht, C., Sickmann, A., Stark, H., & Fischer, U. (2008) · Cell · doi:10.1016/j.cell.2008.09.020 · Cited by 232 · see citing works
Tudor domains in proteins that interact with RNA
Ponting, C. P. (1997) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(96)30049-2 · Cited by 196 · see citing works
Vasileva, A., Tiedau, D., Firooznia, A., Müller‐Reichert, T., & Jessberger, R. (2009) · Current Biology · doi:10.1016/j.cub.2009.02.047 · Cited by 193 · see citing works
Why do cells need an assembly machine for RNA–protein complexes?
Yong, J., Wan, L., & Dreyfuss, G. (2004) · Trends in Cell Biology · doi:10.1016/j.tcb.2004.03.010 · Cited by 167 · see citing works
Hosokawa, M., Shoji, M., KITAMURA, K., Tanaka, T. S. T., Noce, T., Chuma, S., & Nakatsuji, N. (2006) · Developmental Biology · doi:10.1016/j.ydbio.2006.10.046 · Cited by 155 · see citing works
Gillespie, D., & Berg, C. A. (1995) · Genes & Development · doi:10.1101/gad.9.20.2495 · Cited by 152 · see citing works
Bardsley, A., McDonald, K. L., & Boswell, R. E. (1993) · Development · doi:10.1242/dev.119.1.207 · Cited by 137 · see citing works
The role of Tudor domains in germline development and polar granule architecture
Arkov, A. L., Wang, J.-Y. S., Ramos, A., & Lehmann, R. (2006) · Development · doi:10.1242/dev.02572 · Cited by 133 · see citing works
Isolation of new polar granule components in Drosophila reveals P body and ER associated proteins
Thomson, T., Liu, N., Arkov, A. L., Lehmann, R., & Lasko, P. F. (2008) · Mechanisms of Development · doi:10.1016/j.mod.2008.06.005 · Cited by 118 · see citing works
Snee, M. J., & Macdonald, P. M. (2004) · Journal of Cell Science · doi:10.1242/jcs.01059 · Cited by 113 · see citing works
The Sm-Protein Methyltransferase, Dart5, Is Essential for Germ-Cell Specification and Maintenance
Gonsalvez, G. B., Rajendra, T. K., Tian, L., & Matera, A. G. (2006) · Current Biology · doi:10.1016/j.cub.2006.04.037 · Cited by 112 · see citing works
Deciphering the assembly pathway of Sm‐class U snRNPs
Neuenkirchen, N., Chari, A., & Fischer, U. (2008) · FEBS Letters · doi:10.1016/j.febslet.2008.03.009 · Cited by 107 · see citing works
Thomson, T., & Lasko, P. F. (2004) · genesis · doi:10.1002/gene.20079 · Cited by 95 · see citing works
Anne, J., Ollo, R., Ephrussi, A., & Mechler, B. M. (2007) · Development · doi:10.1242/dev.02687 · Cited by 78 · see citing works
Anne, J., & Mechler, B. M. (2005) · Development · doi:10.1242/dev.01809 · Cited by 60 · see citing works
Siomi, M. C., & Kuramochi‐Miyagawa, S. (2009) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2009.02.003 · Cited by 38 · see citing works
Self-citationFully automated online multi-dimensional protein profiling system for complex mixtures
Fujii, K., Nakano, T., Hike, H., Usui, F., Bando, Y., Tojo, H., & Nishimura, T. (2004) · Journal of Chromatography A · doi:10.1016/j.chroma.2004.09.078 · Cited by 36 · see citing works
Keller, B. O., Wang, Z., & Li, L. (2002) · Journal of Chromatography B · doi:10.1016/s1570-0232(02)00565-2 · Cited by 23 · see citing works
Siomi, H., & Siomi, M. C. (2008) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2008.01.002 · Cited by 22 · see citing works
Self-citationIdentification of 36-kDa Flagellar Phosphoproteins Associated with Hamster Sperm Motility
Fujinoki, M. (2003) · The Journal of Biochemistry · doi:10.1093/jb/mvg048 · Cited by 22 · see citing works
Flagged first, then by citations
1 of the 45 references couldn’t be matched to a known paper.
Cited by
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Targeting the dynamic HSP90 complex in cancer
Trepel, J. B., Mollapour, M., Giaccone, G., & Neckers, L. (2010) · Nature reviews. Cancer · doi:10.1038/nrc2887 · Cited by 1,523 · see citing works
PIWI-interacting small RNAs: the vanguard of genome defence
Siomi, M. C., Sato, K., Pezic, D., & Aravin, A. A. (2011) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3089 · Cited by 1,319 · see citing works
Self-citationPIWI-interacting RNAs: small RNAs with big functions
Özata, D. M., Gainetdinov, I. V., Zoch, A., O’Carroll, D., & Zamore, P. D. (2018) · Nature Reviews Genetics · doi:10.1038/s41576-018-0073-3 · Cited by 1,157 · see citing works
A genome-scale shRNA resource for transgenic RNAi in Drosophila
Ni, J.-Q., Zhou, R., Czech, B., Liu, L., Holderbaum, L., Yang‐Zhou, D., Shim, H.-S., Tao, R., Handler, D., Karpowicz, P. A., et al. (2011) · Nature Methods · doi:10.1038/nmeth.1592 · Cited by 797 · see citing works
PIWI-Interacting RNA: Its Biogenesis and Functions
Iwasaki, Y. W., Siomi, M. C., & Siomi, H. (2015) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-060614-034258 · Cited by 765 · see citing works
Self-citationpiRNA-Guided Genome Defense: From Biogenesis to Silencing
Czech, B., Munafò, M., Ciabrelli, F., Eastwood, E. L., Fabry, M., Kneuss, E., & Hannon, G. J. (2018) · Annual Review of Genetics · doi:10.1146/annurev-genet-120417-031441 · Cited by 548 · see citing works
The PRMT5 arginine methyltransferase: many roles in development, cancer and beyond
Stopa, N., Krebs, J. E., & Shechter, D. (2015) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-015-1847-9 · Cited by 529 · see citing works
One Loop to Rule Them All: The Ping-Pong Cycle and piRNA-Guided Silencing
Czech, B., & Hannon, G. J. (2016) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2015.12.008 · Cited by 510 · see citing works
RNA Granules in Germ CellsPreprint
Voronina, E., Seydoux, G., Sassone‐Corsi, P., & Nagamori, I. (2011) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a002774 · Cited by 377 · see citing works
Juliano, C., Wang, J., & Lin, H. (2011) · Annual Review of Genetics · doi:10.1146/annurev-genet-110410-132541 · Cited by 374 · see citing works
Ketting, R. F. (2011) · Developmental Cell · doi:10.1016/j.devcel.2011.01.012 · Cited by 341 · see citing works
Ishizu, H., Siomi, H., & Siomi, M. C. (2012) · Genes & Development · doi:10.1101/gad.203786.112 · Cited by 337 · see citing works
Self-citationDeciphering arginine methylation: Tudor tells the tale
Chen, C., Nott, T. J., Jin, J., & Pawson, T. J. (2011) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3185 · Cited by 301 · see citing works
Olivieri, D., Sykora, M. M., Sachidanandam, R., Mechtler, K., & Brennecke, J. (2010) · The EMBO Journal · doi:10.1038/emboj.2010.212 · Cited by 268 · see citing works
The piRNA pathway: a fly's perspective on the guardian of the genome
Senti, K.-A., & Brennecke, J. (2010) · Trends in Genetics · doi:10.1016/j.tig.2010.08.007 · Cited by 267 · see citing works
Mili and Miwi target RNA repertoire reveals piRNA biogenesis and function of Miwi in spermiogenesis
Vourekas, A., Zheng, Q., Alexiou, P., Maragkakis, M., Kirino, Y., Gregory, B. D., & Mourelatos, Z. (2012) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2347 · Cited by 250 · see citing works
The piRNA Pathway Guards the Germline Genome Against Transposable Elements
Tóth, K. F., Pezić, D., Stuwe, E., & Webster, A. (2015) · Advances in experimental medicine and biology · doi:10.1007/978-94-017-7417-8_4 · Cited by 232 · see citing works
The Genetic Makeup of the Drosophila piRNA Pathway
Handler, D., Meixner, K., Pizka, M., Lauss, K., Schmied, C., Gruber, F. S., & Brennecke, J. (2013) · Molecular Cell · doi:10.1016/j.molcel.2013.04.031 · Cited by 230 · see citing works
Tripsianes, K., Madl, T., Machyna, M., Fessas, D., Englbrecht, C., Fischer, U., Neugebauer, K. M., & Sattler, M. (2011) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2185 · Cited by 203 · see citing works
PIWI proteins and their interactors in piRNA biogenesis, germline development and gene expression
Ku, H.-Y., & Lin, H. (2014) · National Science Review · doi:10.1093/nsr/nwu014 · Cited by 199 · see citing works
The winding path of protein methylation research: milestones and new frontiers
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Siomi, M. C., Mannen, T., & Siomi, H. (2010) · Genes & Development · doi:10.1101/gad.1899210 · Cited by 193 · see citing works
Self-citationHandler, D., Olivieri, D., Novatchkova, M., Gruber, F. S., Meixner, K., Mechtler, K., Stark, A., Sachidanandam, R., & Brennecke, J. (2011) · The EMBO Journal · doi:10.1038/emboj.2011.308 · Cited by 190 · see citing works
Patil, V. S., & Kai, T. (2010) · Current Biology · doi:10.1016/j.cub.2010.02.046 · Cited by 178 · see citing works
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Zhang, Z., Xu, J. L., Koppetsch, B. S., Wang, J., Tipping, C., Ma, S., Weng, Z., Theurkauf, W. E., & Zamore, P. D. (2011) · Molecular Cell · doi:10.1016/j.molcel.2011.10.011 · Cited by 177 · see citing works
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Saito, K., & Siomi, M. C. (2010) · Developmental Cell · doi:10.1016/j.devcel.2010.10.011 · Cited by 172 · see citing works
Self-citationpiRNAs, transposon silencing, and Drosophila germline development
Khurana, J. S., & Theurkauf, W. E. (2010) · The Journal of Cell Biology · doi:10.1083/jcb.201006034 · Cited by 167 · see citing works
Structural basis for recognition of arginine methylated Piwi proteins by the extended Tudor domain
Liu, K., Chen, C., Guo, Y., Lam, R., Bian, C., Xu, C., Zhao, D. Y., Jin, J., MacKenzie, F., Pawson, T. J., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1013106107 · Cited by 154 · see citing works
Structural insights into protein arginine symmetric dimethylation by PRMT5
Sun, L., Wang, M., Lv, Z., Yang, N., Liu, Y., Bao, S., Gong, W., & Xu, R.-M. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1106946108 · Cited by 149 · see citing works
Olivieri, D., Senti, K.-A., Subramanian, S. L., Sachidanandam, R., & Brennecke, J. (2012) · Molecular Cell · doi:10.1016/j.molcel.2012.07.021 · Cited by 147 · see citing works
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Pek, J. W., Anand, A., & Kai, T. (2012) · Development · doi:10.1242/dev.073304 · Cited by 139 · see citing works
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Suzuki, R., Honda, S., & Kirino, Y. (2012) · Frontiers in Genetics · doi:10.3389/fgene.2012.00204 · Cited by 139 · see citing works
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Liu, H., Wang, J.-Y. S., Huang, Y., Li, Z., Gong, W., Lehmann, R., & Xu, R.-M. (2010) · Genes & Development · doi:10.1101/gad.1956010 · Cited by 134 · see citing works
Small Molecule Inhibitors of Protein Arginine Methyltransferases
Hu, H., Qian, K., Ho, M., & Zheng, Y. G. (2016) · Expert Opinion on Investigational Drugs · doi:10.1517/13543784.2016.1144747 · Cited by 129 · see citing works
Webster, A., Li, S., Hur, J. K., Wachsmuth, M., Bois, J. S., Perkins, E. M., Patel, D. J., & Aravin, A. A. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.07.017 · Cited by 123 · see citing works
PIWI-Interacting RNA in Drosophila : Biogenesis, Transposon Regulation, and Beyond
Yamashiro, H., & Siomi, M. C. (2017) · Chemical Reviews · doi:10.1021/acs.chemrev.7b00393 · Cited by 120 · see citing works
Self-citationZamparini, A. L., Davis, M. Y., Malone, C. D., Vieira, E., Zavadil, J., Sachidanandam, R., Hannon, G. J., & Lehmann, R. (2011) · Development · doi:10.1242/dev.069187 · Cited by 121 · see citing works
The ancestral gene repertoire of animal stem cells
Alié, A., Hayashi, T., Sugimura, I., Manuel, M., Sugano, W., Mano, A., Satoh, N., Agata, K., & Funayama, N. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1514789112 · Cited by 119 · see citing works
Biogenesis pathways of piRNAs loaded onto AGO3 in the Drosophila testis
Nagao, A., Mitsuyama, T., Huang, H., Chen, D., Siomi, M. C., & Siomi, H. (2010) · RNA · doi:10.1261/rna.2270710 · Cited by 114 · see citing works
Self-citationAmbegaokar, S. S., & Jackson, G. R. (2011) · Human Molecular Genetics · doi:10.1093/hmg/ddr432 · Cited by 113 · see citing works
Untangling the web: The diverse functions of the PIWI/piRNA pathway
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Control of maternal mRNA stability in germ cells and early embryos
Barckmann, B., & Simonelig, M. (2013) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2012.12.011 · Cited by 108 · see citing works
Liu, L., Qi, H., Wang, J., & Lin, H. (2011) · Development · doi:10.1242/dev.059287 · Cited by 107 · see citing works
Anand, A., & Kai, T. (2011) · The EMBO Journal · doi:10.1038/emboj.2011.449 · Cited by 100 · see citing works
Ge, D. T., Wang, W., Tipping, C., Gainetdinov, I. V., Weng, Z., & Zamore, P. D. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.04.006 · Cited by 99 · see citing works
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Sato, K., & Siomi, M. C. (2020) · Proceedings of the Japan Academy Series B · doi:10.2183/pjab.96.003 · Cited by 95 · see citing works
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Palmer, W. H., Hadfield, J. D., & Obbard, D. J. (2018) · Genetics · doi:10.1534/genetics.117.300567 · Cited by 86 · see citing works
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Huang, H., Houwing, S., Kaaij, L. J. T., Meppelink, A., Redl, S., Gauci, S., Vos, H. R., Draper, B. W., Moens, C. B., Burgering, B. M. T., et al. (2011) · The EMBO Journal · doi:10.1038/emboj.2011.228 · Cited by 90 · see citing works
Self-citationRoovers, E. F., Kaaij, L. J. T., Redl, S., Bronkhorst, A. W., Wiebrands, K., Domingues, A. M. D. J., Huang, H., Han, T., Riemer, S., Dosch, R., et al. (2018) · Developmental Cell · doi:10.1016/j.devcel.2018.07.009 · Cited by 86 · see citing works
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Gao, M., & Arkov, A. L. (2012) · Molecular Reproduction and Development · doi:10.1002/mrd.22115 · Cited by 84 · see citing works
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Arkov, A. L., & Ramos, A. (2010) · Trends in Cell Biology · doi:10.1016/j.tcb.2010.05.004 · Cited by 83 · see citing works
Mitochondrial protein BmPAPI modulates the length of mature piRNAs
Honda, S., Kirino, Y., Maragkakis, M., Alexiou, P., Ohtaki, A., Murali, R., Mourelatos, Z., & Kirino, Y. (2013) · RNA · doi:10.1261/rna.040428.113 · Cited by 83 · see citing works
Aphids: A Model for Polyphenism and Epigenetics
Srinivasan, D. G., & Brisson, J. A. (2012) · Genetics Research International · doi:10.1155/2012/431531 · Cited by 80 · see citing works
Krimper Enforces an Antisense Bias on piRNA Pools by Binding AGO3 in the Drosophila Germline
Sato, K., Iwasaki, Y. W., Shibuya, A., Carninci, P., Tsuchizawa, Y., Ishizu, H., Siomi, M. C., & Siomi, H. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.06.024 · Cited by 76 · see citing works
Self-citationPRMT5 and the role of symmetrical dimethylarginine in chromatoid bodies of planarian stem cells
Rouhana, L., Vieira, A. P., Roberts-Galbraith, R. H., & Newmark, P. A. (2012) · Development · doi:10.1242/dev.076182 · Cited by 75 · see citing works
Regulatory role of the 90-kDa-heat-shock protein (Hsp90) and associated factors on gene expression
Erlejman, A. G., Lagadari, M., Toneatto, J., Piwien‐Pilipuk, G., & Galigniana, M. D. (2014) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2013.12.006 · Cited by 74 · see citing works
Plant PRMTs Broaden the Scope of Arginine Methylation
Ahmad, A., & Cao, X. (2012) · Journal of genetics and genomics/Journal of Genetics and Genomics · doi:10.1016/j.jgg.2012.04.001 · Cited by 74 · see citing works
LOTUS, a new domain associated with small RNA pathways in the germline
Callebaut, I., & Mornon, J. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btq122 · Cited by 74 · see citing works
A tudor domain protein, SIMR-1, promotes siRNA production at piRNA-targeted mRNAs in C. elegans
Manage, K. I., Rogers, A., Wallis, D. C., Uebel, C. J., Anderson, D. C., Nguyen, D. A. H., Arca, K., Brown, K. C., Rodrigues, R. J. C., de Albuquerque, B. F. M., et al. (2020) · eLife · doi:10.7554/elife.56731 · Cited by 73 · see citing works
New Insights into the Regulation of RNP Granule Assembly in Oocytes
Schisa, J. A. (2012) · International review of cytology · doi:10.1016/b978-0-12-394306-4.00013-7 · Cited by 73 · see citing works
Burroughs, A. M., Ando, Y., & Aravind, L. (2013) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1210 · Cited by 67 · see citing works
piRNAs and Aubergine cooperate with Wispy poly(A) polymerase to stabilize mRNAs in the germ plasm
Dufourt, J., Bontonou, G., Chartier, A., Jahan, C., Meunier, A., Pierson, S., Harrison, P. F., Papin, C., Beilharz, T. H., & Simonelig, M. (2017) · Nature Communications · doi:10.1038/s41467-017-01431-5 · Cited by 70 · see citing works
Evolutionarily conserved protein arginine methyltransferases in non‐mammalian animal systems
Wang, Y., & Li, C. (2012) · FEBS Journal · doi:10.1111/j.1742-4658.2012.08490.x · Cited by 66 · see citing works
Ma, X., Zhu, X., Han, Y., Story, B. A., Do, T., Song, X., Wang, S., Zhang, Y., Blanchette, M., Gogol, M., et al. (2017) · Developmental Cell · doi:10.1016/j.devcel.2017.03.023 · Cited by 64 · see citing works
piRNA-mediated silencing in Drosophila germlines
Siomi, M. C., Miyoshi, T., & Siomi, H. (2010) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2010.01.011 · Cited by 62 · see citing works
Self-citationPIWI pathway against viruses in insects
Κολλιοπούλου, Ά., Santos, D., Taning, C. N. T., Wynant, N., Broeck, J. V., Smagghe, G. J., & Swevers, L. (2019) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1555 · Cited by 62 · see citing works
The PIWI protein Aubergine recruits eIF3 to activate translation in the germ plasm
Ramat, A., García-Silva, M. R., Jahan, C., Naït-Saïdi, R., Dufourt, J., Garret, C., Chartier, A., Cremaschi, J., Patel, V., Decourcelle, M., et al. (2020) · Cell Research · doi:10.1038/s41422-020-0294-9 · Cited by 57 · see citing works
Dual regulation of Arabidopsis AGO2 by arginine methylation
Hu, P., Zhao, H., Zhu, P., Xiao, Y., Miao, W., Wang, Y., & Jin, H. (2019) · Nature Communications · doi:10.1038/s41467-019-08787-w · Cited by 53 · see citing works
Mathioudakis, N., Palencia, A., Kadlec, J., Round, A. R., Tripsianes, K., Sattler, M., Pillai, R. S., & Cusack, S. (2012) · RNA · doi:10.1261/rna.034181.112 · Cited by 54 · see citing works
Subcellular Specialization and Organelle Behavior in Germ Cells
Yamashita, Y. M. (2018) · Genetics · doi:10.1534/genetics.117.300184 · Cited by 51 · see citing works
Protecting and Diversifying the Germline
Gleason, R. J., Anand, A., Kai, T., & Chen, X. (2018) · Genetics · doi:10.1534/genetics.117.300208 · Cited by 52 · see citing works
Small RNAs, spermatogenesis, and male infertility: a decade of retrospect
Joshi, M., Sethi, S., Mehta, P., Kumari, A., & Rajender, S. (2023) · Reproductive Biology and Endocrinology · doi:10.1186/s12958-023-01155-w · Cited by 51 · see citing works
Chen, D., Zeng, S., Huang, M., Xu, H., Liang, L., & Yang, X. (2016) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.13020 · Cited by 51 · see citing works
Self-citationpiRNA pathway and the potential processing site, the nuage, in the Drosophila germline
Pek, J. W., Patil, V. S., & Kai, T. (2012) · Development Growth & Differentiation · doi:10.1111/j.1440-169x.2011.01316.x · Cited by 50 · see citing works
The birth of piRNAs: how mammalian piRNAs are produced, originated, and evolved
Sun, Y. H., Lee, B., & Li, X. Z. (2021) · Mammalian Genome · doi:10.1007/s00335-021-09927-8 · Cited by 50 · see citing works
Du, K., Arai, S., Kawamura, T., Matsushita, A., & Kurokawa, R. (2010) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2010.12.097 · Cited by 48 · see citing works
Self-citationPatil, V. S., Anand, A., Chakrabarti, A., & Kai, T. (2014) · BMC Biology · doi:10.1186/s12915-014-0061-9 · Cited by 48 · see citing works
A piece of the pi(e): The diverse roles of animal piRNAs and their PIWI partners
Lim, R. S. M., & Kai, T. (2015) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2015.10.025 · Cited by 48 · see citing works
Kibanov, M. V., Egorova, K. S., Ryazansky, S. S., Sokolova, O. A., Kotov, A. A., Olenkina, O. M., Stolyarenko, A. D., Gvozdev, V. A., & Olenina, L. V. (2011) · Molecular Biology of the Cell · doi:10.1091/mbc.e11-02-0168 · Cited by 48 · see citing works
Structural insights into piRNA biogenesis
Zhang, J., Chen, S., & Liu, K. (2022) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2022.194799 · Cited by 47 · see citing works
Structure and function of eTudor domain containing TDRD proteins
Gan, B. S., Chen, S., Liu, H., Min, J., & Liu, K. (2019) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.1080/10409238.2019.1603199 · Cited by 45 · see citing works
Small RNAs in the animal gonad: Guarding genomes and guiding development
Lau, N. C. (2010) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2010.03.005 · Cited by 43 · see citing works
Piwi-interacting RNAs: biological functions and biogenesis
Sato, K., & Siomi, M. C. (2013) · Essays in Biochemistry · doi:10.1042/bse0540039 · Cited by 41 · see citing works
Self-citationSpatial organization of translation and translational repression in two phases of germ granules
Ramat, A., Haidar, A., Garret, C., & Simonelig, M. (2024) · Nature Communications · doi:10.1038/s41467-024-52346-x · Cited by 36 · see citing works
Nguyen, D. A. H., & Phillips, C. M. (2021) · Nature Communications · doi:10.1038/s41467-021-24526-6 · Cited by 36 · see citing works
Lim, S. L., Tsend‐Ayush, E., Kortschak, R. D., Jacob, R., Ricciardelli, C., Oehler, M. K., & Grützner, F. (2013) · Biology of Reproduction · doi:10.1095/biolreprod.113.111211 · Cited by 36 · see citing works
Lasko, P. F. (2010) · Current Biology · doi:10.1016/j.cub.2010.05.056 · Cited by 36 · see citing works
Piwi Proteins and piRNAs Step onto the Systems Biology Stage
Clark, J. P., & Lau, N. C. (2014) · Advances in experimental medicine and biology · doi:10.1007/978-1-4939-1221-6_5 · Cited by 31 · see citing works
Gender-Specific Hierarchy in Nuage Localization of PIWI-Interacting RNA Factors in Drosophila
Nagao, A., Sato, K., Nishida, K. M., Siomi, H., & Siomi, M. C. (2011) · Frontiers in Genetics · doi:10.3389/fgene.2011.00055 · Cited by 29 · see citing works
Self-citationHuang, X., Hu, H., Webster, A., Zou, F., Du, J., Patel, D. J., Sachidanandam, R., Tóth, K. F., Aravin, A. A., & Li, S. (2021) · Nature Communications · doi:10.1038/s41467-021-24351-x · Cited by 29 · see citing works
The Prmt5-Vasa module is essential for spermatogenesis in Bombyx mori
Xu, Y., Chen, D., Zheng, S., Yi, M., Wang, S., Liu, Y., Jing, L., Liu, Z., Yang, D., Liu, Y., et al. (2023) · PLoS Genetics · doi:10.1371/journal.pgen.1010600 · Cited by 29 · see citing works
Self-citationGell, S. L., & Reenan, R. A. (2012) · Genetics · doi:10.1534/genetics.112.147561 · Cited by 29 · see citing works
The Drosophila fragile X mental retardation protein participates in the piRNA pathway
Bozzetti, M. P., Specchia, V., Cattenoz, P. B., Laneve, P., Geusa, A., Şahin, H. B., Tommaso, S. D., Friscini, A., Massari, S., Diebold, C., et al. (2015) · Journal of Cell Science · doi:10.1242/jcs.161810 · Cited by 29 · see citing works
Piccolo, L. L., Mochizuki, H., & Nagai, Y. (2019) · Journal of Cell Science · doi:10.1242/jcs.236836 · Cited by 28 · see citing works
Zebrafish prmt5 arginine methyltransferase is essential for germ cell development
Zhu, J., Zhang, D., Liu, X., Yu, G., Cai, X., Xu, C., Rong, F., Ouyang, G., Wang, J., & Xiao, W. (2019) · Development · doi:10.1242/dev.179572 · Cited by 28 · see citing works
The PIWI‐Interacting RNA Molecular Pathway: Insights From Cultured Silkworm Germline Cells
Sakakibara, K., & Siomi, M. C. (2017) · BioEssays · doi:10.1002/bies.201700068 · Cited by 26 · see citing works
Self-citationVo, H. D. L., Wahiduzzaman, Tindell, S. J., Zheng, J., Gao, M., & Arkov, A. L. (2019) · Scientific Reports · doi:10.1038/s41598-019-55747-x · Cited by 27 · see citing works
- Authors
- Nishida, K. M., Okada, T. N., Kawamura, T., Mituyama, T., Kawamura, Y., Inagaki, S., Huang, H., Chen, D., Kodama, T., Siomi, H., & Siomi, M. C.
- Affiliations
- Keio University (JP)
- Research Center for Advanced Science and Technology, The University of Tokyo (JP)
- Chinese Academy of Sciences (CN)
- Corresponding author
- Siomi, Mikiko C
- ORCID
- Venue
- The EMBO Journal
- Published
- 2009-12-03
- Volume
- 28
- Issue
- 24
- Pages
- 3820-3831
- ISSN
- 0261-4189 (ISSN-L)
- 1460-2075
- PMC
- PMC2797066
- OpenAlex
- W2136921460
- Cited by
- 197
- References
- 45
- Citations by year
- 2026: 2 · 2025: 8 · 2024: 9 · 2023: 6 · 2022: 7 · 2021: 8 · 2020: 11 · 2019: 10 · 2018: 16 · 2017: 11 · 2016: 11 · 2015: 13 · 2014: 11 · 2013: 16 · 2012: 20
- FWCI
- 23.47
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- The EMBO Journal (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Ministry of Education, Culture, Sports, Science and Technology (CREST)
- University of Tokushima
- Japan Society for the Promotion of Science (CREST)
- Japan Science and Technology Agency (CREST)
- Core Research for Evolutional Science and Technology
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
- 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
- Tudor domain, piRNA, PIWI proteins, eggplant, AGO3, Piwi, symmetric dimethylarginine, arginine methylation, transposon silencing, germline, Drosophila
- MeSH terms
- Amino Acid Sequence, Animals, Arginine, Chromatography, Liquid, Drosophila melanogaster, Gene Expression Regulation, Molecular Sequence Data, Mutation, Protein-Arginine N-Methyltransferases, Protein Methyltransferases, Mass Spectrometry, Sequence Homology, Amino Acid, Membrane Transport Proteins, Drosophila Proteins, Databases, Protein, RNA Interference
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