Structural Differences between Pri-miRNA Paralogs Promote Alternative Drosha Cleavage and Expand Target Repertoires

Bofill-De Ros, Xavier; Kasprzak, Wojciech K.; Bhandari, Yuba; Fan, Lixin; Cavanaugh, Quinn; Jiang, Minjie; Dai, Lisheng; Yang, Acong; Shao, Tie-Juan; Shapiro, Bruce A.; Wang, Yun-Xing; Gu, Shuo

doi:10.1016/j.celrep.2018.12.054

Structural Differences between Pri-miRNA Paralogs Promote Alternative Drosha Cleavage and Expand Target Repertoires

Journal Article · Tue Jan 08 00:00:00 EST 2019 · Cell Reports

DOI:https://doi.org/10.1016/j.celrep.2018.12.054· OSTI ID:1502245

Bofill-De Ros, Xavier ^[1]; Kasprzak, Wojciech K. ^[2]; Bhandari, Yuba ^[3]; Fan, Lixin ^[4]; Cavanaugh, Quinn ^[1]; Jiang, Minjie ^[1]; Dai, Lisheng ^[1]; Yang, Acong ^[1]; Shao, Tie-Juan ^[5]; Shapiro, Bruce A. ^[6]; Wang, Yun-Xing ^[3]; ^[1]

National Cancer Institute, Frederic, MD (United States). RNA Mediated Gene Regulation Section, RNA Biology Laboratory, Center for Cancer Research
National Cancer Institute, Frederic, MD (United States). RNA Biology Laboratory, Frederick National Laboratory for Cancer Research
National Cancer Institute, Frederic, MD (United States). Structural Biophysics Laboratory
Leidos Biomedical Research, Inc., Frederick, MD (United States). Frederick National Laboratory for Cancer Research, Center for Cancer Research of the National Cancer Institute
National Cancer Institute, Frederic, MD (United States). RNA Mediated Gene Regulation Section, RNA Biology Laboratory, Center for Cancer Research; Zhejiang Chinese Medical Univ., Hangzhou (China)
National Cancer Institute, Frederic, MD (United States). RNA Biology Laboratory, Center for Cancer Research

MicroRNA (miRNA) processing begins with Drosha cleavage, the fidelity of which is critical for downstream processing and mature miRNA target specificity. To understand how pri-miRNA sequence and structure influence Drosha cleavage, we studied the maturation of three pri-miR-9 paralogs, which encode the same mature miRNA but differ in the surrounding scaffold. Here, we show that pri-miR-9-1 has a unique Drosha cleavage profile due to its distorted and flexible stem structure. Cleavage of pri-miR-9-1, but not pri-miR-9-2 or pri-miR-9-3, generates an alternative miR-9 with a shifted seed sequence that expands the scope of its target RNAs. Analyses of low-grade glioma patient samples indicate that the alternative-miR-9 has a potential role in tumor progression. Furthermore, we provide evidence that distortion of pri-miRNA stems induced by asymmetric internal loops correlates with Drosha cleavage at non-canonical sites. Our studies reveal that pri-miRNA paralogs can have distinct functions via differential Drosha processing.

View Accepted Manuscript (DOE)

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: National Institutes of Health (NIH), National Cancer Institute (NCI); USDOE

OSTI ID:: 1502245

Journal Information:: Cell Reports, Journal Name: Cell Reports Journal Issue: 2 Vol. 26; ISSN 2211-1247

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

References (84)

Improvements and Extensions in the Conformational Database Potential for the Refinement of NMR and X-ray Structures of Proteins and Nucleic Acids Kuszewski, John; Gronenborn, Angela M.; Clore, G. Marius Journal of Magnetic Resonance, Vol. 125, Issue 1 https://doi.org/10.1006/jmre.1997.1116	journal	March 1997
Rethinking the Microprocessor Seitz, Hervé; Zamore, Phillip D. Cell, Vol. 125, Issue 5 https://doi.org/10.1016/j.cell.2006.05.018	journal	June 2006
MicroRNAs: Target Recognition and Regulatory Functions Bartel, David P. Cell, Vol. 136, Issue 2 https://doi.org/10.1016/j.cell.2009.01.002	journal	January 2009
The Loop Position of shRNAs and Pre-miRNAs Is Critical for the Accuracy of Dicer Processing In Vivo Gu, Shuo; Jin, Lan; Zhang, Yue Cell, Vol. 151, Issue 4 https://doi.org/10.1016/j.cell.2012.09.042	journal	November 2012
Beyond Secondary Structure: Primary-Sequence Determinants License Pri-miRNA Hairpins for Processing Auyeung, Vincent C.; Ulitsky, Igor; McGeary, Sean E. Cell, Vol. 152, Issue 4 https://doi.org/10.1016/j.cell.2013.01.031	journal	February 2013
An Unusual Topological Structure of the HIV-1 Rev Response Element Fang, Xianyang; Wang, Jinbu; O’Carroll, Ina P. Cell, Vol. 155, Issue 3 https://doi.org/10.1016/j.cell.2013.10.008	journal	October 2013
Mammalian 5′-Capped MicroRNA Precursors that Generate a Single MicroRNA Xie, Mingyi; Li, Mingfeng; Vilborg, Anna Cell, Vol. 155, Issue 7 https://doi.org/10.1016/j.cell.2013.11.027	journal	December 2013
Argonaute-Bound Small RNAs from Promoter-Proximal RNA Polymerase II Zamudio, Jesse R.; Kelly, Timothy J.; Sharp, Phillip A. Cell, Vol. 156, Issue 5 https://doi.org/10.1016/j.cell.2014.01.041	journal	February 2014
Functional Anatomy of the Human Microprocessor Nguyen, Tuan Anh; Jo, Myung Hyun; Choi, Yeon-Gil Cell, Vol. 161, Issue 6 https://doi.org/10.1016/j.cell.2015.05.010	journal	June 2015
MicroRNA-9 Modulates Hes1 Ultradian Oscillations by Forming a Double-Negative Feedback Loop Bonev, Boyan; Stanley, Peter; Papalopulu, Nancy Cell Reports, Vol. 2, Issue 1 https://doi.org/10.1016/j.celrep.2012.05.017	journal	July 2012
The Menu of Features that Define Primary MicroRNAs and Enable De Novo Design of MicroRNA Genes Fang, Wenwen; Bartel, David P. Molecular Cell, Vol. 60, Issue 1 https://doi.org/10.1016/j.molcel.2015.08.015	journal	October 2015
Genome-wide Mapping of DROSHA Cleavage Sites on Primary MicroRNAs and Noncanonical Substrates Kim, Baekgyu; Jeong, Kyowon; Kim, V. Narry Molecular Cell, Vol. 66, Issue 2 https://doi.org/10.1016/j.molcel.2017.03.013	journal	April 2017
miXED Messages in Ion Channel Modulation Levitan, Irwin B. Neuron, Vol. 59, Issue 2 https://doi.org/10.1016/j.neuron.2008.07.014	journal	July 2008
The Functions of MicroRNAs: mRNA Decay and Translational Repression Iwakawa, Hiro-oki; Tomari, Yukihide Trends in Cell Biology, Vol. 25, Issue 11 https://doi.org/10.1016/j.tcb.2015.07.011	journal	November 2015
Guidelines for the optimal design of miRNA-based shRNAs Bofill-De Ros, Xavier; Gu, Shuo Methods, Vol. 103 https://doi.org/10.1016/j.ymeth.2016.04.003	journal	July 2016
Genes and Mechanisms Related to RNA Interference Regulate Expression of the Small Temporal RNAs that Control C. elegans Developmental Timing Grishok, Alla; Pasquinelli, Amy E.; Conte, Darryl Cell, Vol. 106, Issue 1 https://doi.org/10.1016/s0092-8674(01)00431-7	journal	July 2001
Asymmetry in the Assembly of the RNAi Enzyme Complex Schwarz, Dianne S.; Hutvágner, György; Du, Tingting Cell, Vol. 115, Issue 2 https://doi.org/10.1016/s0092-8674(03)00759-1	journal	October 2003
Functional siRNAs and miRNAs Exhibit Strand Bias Khvorova, Anastasia; Reynolds, Angela; Jayasena, Sumedha D. Cell, Vol. 115, Issue 2 https://doi.org/10.1016/s0092-8674(03)00801-8	journal	October 2003
Big Insights into Small RNAs Rissland, Olivia S. Biochemistry, Vol. 59, Issue 16 https://doi.org/10.1021/acs.biochem.0c00252	journal	April 2020
A Physical Picture of Atomic Motions within the Dickerson DNA Dodecamer in Solution Derived from Joint Ensemble Refinement against NMR and Large-Angle X-ray Scattering Data ^† Schwieters, Charles D.; Clore, G. Marius Biochemistry, Vol. 46, Issue 5 https://doi.org/10.1021/bi061943x	journal	February 2007
Refinement of the Cornell et al. Nucleic Acids Force Field Based on Reference Quantum Chemical Calculations of Glycosidic Torsion Profiles Zgarbová, Marie; Otyepka, Michal; Šponer, Jiří Journal of Chemical Theory and Computation, Vol. 7, Issue 9 https://doi.org/10.1021/ct200162x	journal	August 2011
Drosha and Dicer: Slicers cut from the same cloth Li, Sisi; Patel, Dinshaw J. Cell Research, Vol. 26, Issue 5 https://doi.org/10.1038/cr.2016.19	journal	April 2016
The nuclear RNase III Drosha initiates microRNA processing Lee, Yoontae; Ahn, Chiyoung; Han, Jinju Nature, Vol. 425, Issue 6956 https://doi.org/10.1038/nature01957	journal	September 2003
The Microprocessor complex mediates the genesis of microRNAs Gregory, Richard I.; Yan, Kai-ping; Amuthan, Govindasamy Nature, Vol. 432, Issue 7014 https://doi.org/10.1038/nature03120	journal	November 2004
Intronic microRNA precursors that bypass Drosha processing Ruby, J. Graham; Jan, Calvin H.; Bartel, David P. Nature, Vol. 448, Issue 7149 https://doi.org/10.1038/nature05983	journal	June 2007
Dicer recognizes the 5′ end of RNA for efficient and accurate processing Park, Jong-Eun; Heo, Inha; Tian, Yuan Nature, Vol. 475, Issue 7355 https://doi.org/10.1038/nature10198	journal	July 2011
Myc-modulated miR-9 makes more metastases Khew-Goodall, Yeesim; Goodall, Gregory J. Nature Cell Biology, Vol. 12, Issue 3 https://doi.org/10.1038/ncb0310-209	journal	February 2010
miRNA–target chimeras reveal miRNA 3′-end pairing as a major determinant of Argonaute target specificity Moore, Michael J.; Scheel, Troels K. H.; Luna, Joseph M. Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms9864	journal	November 2015
MicroRNA biogenesis pathways in cancer Lin, Shuibin; Gregory, Richard I. Nature Reviews Cancer, Vol. 15, Issue 6 https://doi.org/10.1038/nrc3932	journal	May 2015
Evolution of microRNA diversity and regulation in animals Berezikov, Eugene Nature Reviews Genetics, Vol. 12, Issue 12 https://doi.org/10.1038/nrg3079	journal	November 2011
MicroRNAs and their targets: recognition, regulation and an emerging reciprocal relationship Pasquinelli, Amy E. Nature Reviews Genetics, Vol. 13, Issue 4 https://doi.org/10.1038/nrg3162	journal	March 2012
Towards a molecular understanding of microRNA-mediated gene silencing Jonas, Stefanie; Izaurralde, Elisa Nature Reviews Genetics, Vol. 16, Issue 7 https://doi.org/10.1038/nrg3965	journal	June 2015
Regulation of microRNA biogenesis Ha, Minju; Kim, V. Narry Nature Reviews Molecular Cell Biology, Vol. 15, Issue 8 https://doi.org/10.1038/nrm3838	journal	July 2014
A feedback regulatory loop involving microRNA-9 and nuclear receptor TLX in neural stem cell fate determination Zhao, Chunnian; Sun, GuoQiang; Li, Shengxiu Nature Structural & Molecular Biology, Vol. 16, Issue 4 https://doi.org/10.1038/nsmb.1576	journal	March 2009
NEAT1 scaffolds RNA-binding proteins and the Microprocessor to globally enhance pri-miRNA processing Jiang, Li; Shao, Changwei; Wu, Qi-Jia Nature Structural & Molecular Biology, Vol. 24, Issue 10 https://doi.org/10.1038/nsmb.3455	journal	August 2017
Structural determinants of RNA recognition and cleavage by Dicer MacRae, Ian J.; Zhou, Kaihong; Doudna, Jennifer A. Nature Structural & Molecular Biology, Vol. 14, Issue 10 https://doi.org/10.1038/nsmb1293	journal	September 2007
A mesenchymal glioma stem cell profile is related to clinical outcome Balbous, A.; Cortes, U.; Guilloteau, K. Oncogenesis, Vol. 3, Issue 3 https://doi.org/10.1038/oncsis.2014.5	journal	March 2014
Recognition and cleavage of primary microRNA precursors by the nuclear processing enzyme Drosha Zeng, Yan; Yi, Rui; Cullen, Bryan R. The EMBO Journal, Vol. 24, Issue 1 https://doi.org/10.1038/sj.emboj.7600491	journal	November 2004
QuagmiR: a cloud-based application for isomiR big data analytics Bofill-De Ros, Xavier; Chen, Kevin; Chen, Susanna Bioinformatics, Vol. 35, Issue 9 https://doi.org/10.1093/bioinformatics/bty843	journal	October 2018
FGL2 as a Multimodality Regulator of Tumor-Mediated Immune Suppression and Therapeutic Target in Gliomas Yan, Jun; Kong, Ling-Yuan; Hu, Jiemiao JNCI: Journal of the National Cancer Institute, Vol. 107, Issue 8 https://doi.org/10.1093/jnci/djv137	journal	May 2015
The Vienna RNA Websuite Gruber, A. R.; Lorenz, R.; Bernhart, S. H. Nucleic Acids Research, Vol. 36, Issue Web Server https://doi.org/10.1093/nar/gkn188	journal	May 2008
miRBase: annotating high confidence microRNAs using deep sequencing data Kozomara, Ana; Griffiths-Jones, Sam Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1181	journal	November 2013
5′ isomiR variation is of functional and evolutionary importance Tan, Geok Chin; Chan, Elcie; Molnar, Attila Nucleic Acids Research, Vol. 42, Issue 14 https://doi.org/10.1093/nar/gku656	journal	July 2014
Cytoplasmic Drosha activity generated by alternative splicing Dai, Lisheng; Chen, Kevin; Youngren, Brenda Nucleic Acids Research https://doi.org/10.1093/nar/gkw668	journal	July 2016
Most mammalian mRNAs are conserved targets of microRNAs Friedman, R. C.; Farh, K. K. -H.; Burge, C. B. Genome Research, Vol. 19, Issue 1 https://doi.org/10.1101/gr.082701.108	journal	October 2008
A comprehensive survey of 3' animal miRNA modification events and a possible role for 3' adenylation in modulating miRNA targeting effectiveness Burroughs, A. M.; Ando, Y.; de Hoon, M. J. L. Genome Research, Vol. 20, Issue 10 https://doi.org/10.1101/gr.106054.110	journal	August 2010
Novel determinants of mammalian primary microRNA processing revealed by systematic evaluation of hairpin-containing transcripts and human genetic variation Roden, Christine; Gaillard, Jonathan; Kanoria, Shaveta Genome Research, Vol. 27, Issue 3 https://doi.org/10.1101/gr.208900.116	journal	January 2017
Evolution, biogenesis, expression, and target predictions of a substantially expanded set of Drosophila microRNAs Ruby, J. G.; Stark, A.; Johnston, W. K. Genome Research, Vol. 17, Issue 12 https://doi.org/10.1101/gr.6597907	journal	December 2007
A Role for the RNase III Enzyme DCR-1 in RNA Interference and Germ Line Development in Caenorhabditis elegans Knight, S. W. Science, Vol. 293, Issue 5538 https://doi.org/10.1126/science.1062039	journal	August 2001
RNase III: Genetics and Function; Structure and Mechanism Court, Donald L.; Gan, Jianhua; Liang, Yu-He Annual Review of Genetics, Vol. 47, Issue 1 https://doi.org/10.1146/annurev-genet-110711-155618	journal	November 2013
A Uniform System for the Annotation of Vertebrate microRNA Genes and the Evolution of the Human microRNAome Fromm, Bastian; Billipp, Tyler; Peck, Liam E. Annual Review of Genetics, Vol. 49, Issue 1 https://doi.org/10.1146/annurev-genet-120213-092023	journal	November 2015
Restoration of miR-29b exerts anti-cancer effects on glioblastoma Shin, Jaekyung; Shim, Hyun Geun; Hwang, Taeyoung Cancer Cell International, Vol. 17, Issue 1 https://doi.org/10.1186/s12935-017-0476-9	journal	November 2017
MicroRNA-9 Modulates Cajal-Retzius Cell Differentiation by Suppressing Foxg1 Expression in Mouse Medial Pallium Shibata, M.; Kurokawa, D.; Nakao, H. Journal of Neuroscience, Vol. 28, Issue 41 https://doi.org/10.1523/jneurosci.3219-08.2008	journal	October 2008
miR-9: a versatile regulator of neurogenesis Coolen, Marion; Katz, Shauna; Bally-Cuif, Laure Frontiers in Cellular Neuroscience, Vol. 7 https://doi.org/10.3389/fncel.2013.00220	journal	January 2013
Acquired resistance to metformin in breast cancer cells triggers transcriptome reprogramming toward a degradome-related metastatic stem-like profile Oliveras-Ferraros, Cristina; Vazquez-Martin, Alejandro; Cuyàs, Elisabet Cell Cycle, Vol. 13, Issue 7 https://doi.org/10.4161/cc.27982	journal	February 2014
Theory and applications of the generalized born solvation model in macromolecular simulations Tsui, Vickie; Case, David A. Biopolymers, Vol. 56, Issue 4 https://doi.org/10.1002/1097-0282(2000)56:4<275::AID-BIP10024>3.0.CO;2-E	journal	January 2000
Vascular gene expression patterns are conserved in primary and metastatic brain tumors Liu, Yang; Carson-Walter, Eleanor B.; Cooper, Anna Journal of Neuro-Oncology, Vol. 99, Issue 1 https://doi.org/10.1007/s11060-009-0105-0	journal	January 2010
Genes and Mechanisms Related to RNA Interference Regulate Expression of the Small Temporal RNAs that Control C. elegans Developmental Timing Grishok, Alla; Pasquinelli, Amy E.; Conte, Darryl Cell, Vol. 106, Issue 1 https://doi.org/10.1016/S0092-8674(01)00431-7	journal	July 2001
Asymmetry in the Assembly of the RNAi Enzyme Complex Schwarz, Dianne S.; Hutvágner, György; Du, Tingting Cell, Vol. 115, Issue 2 https://doi.org/10.1016/S0092-8674(03)00759-1	journal	October 2003
Functional siRNAs and miRNAs Exhibit Strand Bias Khvorova, Anastasia; Reynolds, Angela; Jayasena, Sumedha D. Cell, Vol. 115, Issue 2 https://doi.org/10.1016/S0092-8674(03)00801-8	journal	October 2003
Structural Insight into the Mechanism of Double-Stranded RNA Processing by Ribonuclease III Gan, Jianhua; Tropea, Joseph E.; Austin, Brian P. Cell, Vol. 124, Issue 2 https://doi.org/10.1016/j.cell.2005.11.034	journal	January 2006
Molecular Basis for the Recognition of Primary microRNAs by the Drosha-DGCR8 Complex Han, Jinju; Lee, Yoontae; Yeom, Kyu-Hyeon Cell, Vol. 125, Issue 5 https://doi.org/10.1016/j.cell.2006.03.043	journal	June 2006
Structure of Human DROSHA Kwon, S. Chul; Nguyen, Tuan Anh; Choi, Yeon-Gil Cell, Vol. 164, Issue 1-2 https://doi.org/10.1016/j.cell.2015.12.019	journal	January 2016
Metazoan MicroRNAs Bartel, David P. Cell, Vol. 173, Issue 1 https://doi.org/10.1016/j.cell.2018.03.006	journal	March 2018
Posttranscriptional Regulation of miRNAs Harboring Conserved Terminal Loops Michlewski, Gracjan; Guil, Sonia; Semple, Colin A. Molecular Cell, Vol. 32, Issue 3 https://doi.org/10.1016/j.molcel.2008.10.013	journal	November 2008
Posttranscriptional Regulation of BK Channel Splice Variant Stability by miR-9 Underlies Neuroadaptation to Alcohol Pietrzykowski, Andrzej Z.; Friesen, Ryan M.; Martin, Gilles E. Neuron, Vol. 59, Issue 2 https://doi.org/10.1016/j.neuron.2008.05.032	journal	July 2008
Refinement of Generalized Born Implicit Solvation Parameters for Nucleic Acids and Their Complexes with Proteins Nguyen, Hai; Pérez, Alberto; Bermeo, Sherry Journal of Chemical Theory and Computation, Vol. 11, Issue 8 https://doi.org/10.1021/acs.jctc.5b00271	journal	July 2015
Processing of primary microRNAs by the Microprocessor complex Denli, Ahmet M.; Tops, Bastiaan B. J.; Plasterk, Ronald H. A. Nature, Vol. 432, Issue 7014 https://doi.org/10.1038/nature03049	journal	November 2004
Structural basis for 5′-nucleotide base-specific recognition of guide RNA by human AGO2 Frank, Filipp; Sonenberg, Nahum; Nagar, Bhushan Nature, Vol. 465, Issue 7299 https://doi.org/10.1038/nature09039	journal	May 2010
miR-9, a MYC/MYCN-activated microRNA, regulates E-cadherin and cancer metastasis Ma, Li; Young, Jennifer; Prabhala, Harsha Nature Cell Biology, Vol. 12, Issue 3 https://doi.org/10.1038/ncb2024	journal	February 2010
Lower and upper stem-single-stranded RNA junctions together determine the Drosha cleavage site Ma, H.; Wu, Y.; Choi, J. -G. Proceedings of the National Academy of Sciences, Vol. 110, Issue 51 https://doi.org/10.1073/pnas.1311639110	journal	December 2013
Structural basis of microRNA length variety Starega-Roslan, Julia; Krol, Jacek; Koscianska, Edyta Nucleic Acids Research, Vol. 39, Issue 1 https://doi.org/10.1093/nar/gkq727	journal	August 2010
Automated 3D structure composition for large RNAs Popenda, Mariusz; Szachniuk, Marta; Antczak, Maciej Nucleic Acids Research, Vol. 40, Issue 14 https://doi.org/10.1093/nar/gks339	journal	April 2012
Folding and Finding RNA Secondary Structure Mathews, D. H.; Moss, W. N.; Turner, D. H. Cold Spring Harbor Perspectives in Biology, Vol. 2, Issue 12 https://doi.org/10.1101/cshperspect.a003665	journal	August 2010
The Drosha-DGCR8 complex in primary microRNA processing Han, J. Genes & Development, Vol. 18, Issue 24 https://doi.org/10.1101/gad.1262504	journal	December 2004
Deep annotation of Drosophila melanogaster microRNAs yields insights into their processing, modification, and emergence Berezikov, E.; Robine, N.; Samsonova, A. Genome Research, Vol. 21, Issue 2 https://doi.org/10.1101/gr.116657.110	journal	December 2010
A Cellular Function for the RNA-Interference Enzyme Dicer in the Maturation of the let-7 Small Temporal RNA Hutvagner, G. Science, Vol. 293, Issue 5531 https://doi.org/10.1126/science.1062961	journal	July 2001
TRBP alters human precursor microRNA processing in vitro Lee, H. Y.; Doudna, J. A. RNA, Vol. 18, Issue 11 https://doi.org/10.1261/rna.035501.112	journal	September 2012
A central role for the primary microRNA stem in guiding the position and efficiency of Drosha processing of a viral pri-miRNA Burke, J. M.; Kelenis, D. P.; Kincaid, R. P. RNA, Vol. 20, Issue 7 https://doi.org/10.1261/rna.044537.114	journal	May 2014
The Brain-Enriched MicroRNA miR-9-3p Regulates Synaptic Plasticity and Memory Sim, Su-Eon; Lim, Chae-Seok; Kim, Jae-Ick The Journal of Neuroscience, Vol. 36, Issue 33 https://doi.org/10.1523/JNEUROSCI.0630-16.2016	journal	August 2016
MicroRNA-9 Modulates Cajal-Retzius Cell Differentiation by Suppressing Foxg1 Expression in Mouse Medial Pallium Shibata, M.; Kurokawa, D.; Nakao, H. Journal of Neuroscience, Vol. 28, Issue 41 https://doi.org/10.1523/JNEUROSCI.3219-08.2008	journal	October 2008
The versatile nature of miR-9/9* in human cancer Nowek, Katarzyna; Wiemer, Erik A. C.; Jongen-Lavrencic, Mojca Oncotarget, Vol. 9, Issue 29 https://doi.org/10.18632/oncotarget.24889	journal	April 2018
Restoration of miR-29b exerts anti-cancer effects on glioblastoma Shin, Jaekyung; Shim, Hyun; Hwang, Taeyoung Figshare https://doi.org/10.6084/m9.figshare.c.3933898.v1	collection	January 2017
Predicting effective microRNA target sites in mammalian mRNAs Agarwal, Vikram; Bell, George W.; Nam, Jin-Wu eLife, Vol. 4 https://doi.org/10.7554/eLife.05005	journal	August 2015

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59 BASIC BIOLOGICAL SCIENCES
Drosha
RNA structure
isomiRs
miR-9
microprocessor
paralogs
primary miRNA

Structural Differences between Pri-miRNA Paralogs Promote Alternative Drosha Cleavage and Expand Target Repertoires

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References (84)

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