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1. Comparative transcriptomics of primary cells in vertebrates

Author

Hideya Kawaji, Imad Abugessaisa, Takeya Kasukawa, Luigi Marchionni, Jessica Severin, Martin S. Taylor, Shohei Noma, Erik Arner, Robin Andersson, Yoshihide Hayashizaki, Akira Hasegawa, Tanvir Alam, Levon M. Khachigian, Hiroshi Tarui, Michiel J. L. de Hoon, Saumya Agrawal, Piero Carninci, Yuri Ishizu, Robert Young, Guojun Sheng, Timo Lassmann, Masayoshi Itoh, Marina Lizio, Jordan A. Ramilowski, and Alistair R. R. Forrest

Subjects
Biology, Evolution, Molecular, Transcriptome, Mice, 03 medical and health sciences, Dogs, 0302 clinical medicine, Species Specificity, Gene expression, Genetics, Transcriptional regulation, Animals, Humans, Gene Regulatory Networks, Nucleotide Motifs, Promoter Regions, Genetic, Enhancer, Gene, Genetics (clinical), 030304 developmental biology, Principal Component Analysis, 0303 health sciences, Research, Gene Expression Profiling, Promoter, Phenotype, Rats, Gene expression profiling, MicroRNAs, Chickens, 030217 neurology & neurosurgery, Transcription Factors
Abstract

Gene expression profiles in homologous tissues have been observed to be different between species, which may be due to differences between species in the gene expression program in each cell type, but may also reflect differences in cell type composition of each tissue in different species. Here, we compare expression profiles in matching primary cells in human, mouse, rat, dog, and chicken using Cap Analysis Gene Expression (CAGE) and short RNA (sRNA) sequencing data from FANTOM5. While we find that expression profiles of orthologous genes in different species are highly correlated across cell types, in each cell type many genes were differentially expressed between species. Expression of genes with products involved in transcription, RNA processing, and transcriptional regulation was more likely to be conserved, while expression of genes encoding proteins involved in intercellular communication was more likely to have diverged during evolution. Conservation of expression correlated positively with the evolutionary age of genes, suggesting that divergence in expression levels of genes critical for cell function was restricted during evolution. Motif activity analysis showed that both promoters and enhancers are activated by the same transcription factors in different species. An analysis of expression levels of mature miRNAs and of primary miRNAs identified by CAGE revealed that evolutionary old miRNAs are more likely to have conserved expression patterns than young miRNAs. We conclude that key aspects of the regulatory network are conserved, while differential expression of genes involved in cell-to-cell communication may contribute greatly to phenotypic differences between species.

Published
2020
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2. Global analysis of pre-mRNA subcellular localization following splicing inhibition by spliceostatin A

Author

Yumi Kawamura, Daisuke Kaida, Minoru Yoshida, Masaaki Furuno, A. Maxwell Burroughs, Akila Mayeda, Shohei Noma, Rei Yoshimoto, Harukazu Suzuki, and Yoshihide Hayashizaki

Subjects
0301 basic medicine, Cytoplasm, Spliceosome, RNA Splicing, Biology, Article, 03 medical and health sciences, Neoplasms, RNA Precursors, medicine, Humans, Spiro Compounds, snRNP, Molecular Biology, Pyrans, Cell Nucleus, Sequence Analysis, RNA, Intron, Subcellular localization, Cell biology, Gene Expression Regulation, Neoplastic, stomatognathic diseases, Cell nucleus, 030104 developmental biology, medicine.anatomical_structure, RNA splicing, Precursor mRNA, Cyclin-Dependent Kinase Inhibitor p27, HeLa Cells
Abstract

Spliceostatin A (SSA) is a methyl ketal derivative of FR901464, a potent antitumor compound isolated from a culture broth of Pseudomonas sp. no. 2663. These compounds selectively bind to the essential spliceosome component SF3b, a subcomplex of the U2 snRNP, to inhibit pre-mRNA splicing. However, the mechanism of SSA's antitumor activity is unknown. It is noteworthy that SSA causes accumulation of a truncated form of the CDK inhibitor protein p27 translated from CDKN1B pre-mRNA, which is involved in SSA-induced cell-cycle arrest. However, it is still unclear whether pre-mRNAs are uniformly exported from the nucleus following SSA treatment. We performed RNA-seq analysis on nuclear and cytoplasmic fractions of SSA-treated cells. Our statistical analyses showed that intron retention is the major consequence of SSA treatment, and a small number of intron-containing pre-mRNAs leak into the cytoplasm. Using a series of reporter plasmids to investigate the roles of intronic sequences in the pre-mRNA leakage, we showed that the strength of the 5′ splice site affects pre-mRNA leakage. Additionally, we found that the level of pre-mRNA leakage is related to transcript length. These results suggest that the strength of the 5′ splice site and the length of the transcripts are determinants of the pre-mRNA leakage induced by SF3b inhibitors.

Published
2016
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3. FANTOM5 CAGE profiles of human and mouse samples

Author

Jun Kawai, Anthony G Beckhouse, Dipti Vijayan, Michael Rehli, Toshiyuki Nakamura, Yuki Hasegawa, Timothy C. Barnett, Hisashi Shimoji, Erik Arner, Masayoshi Itoh, Masahide Hamaguchi, Sarah Klein, Reto Guler, Patrizia Rizzu, Atsutaka Kubosaki, Soichi Kojima, Timo Lassmann, Kelly J. Morris, Mutsumi Kanamori-Katayama, Ri Ichiroh Manabe, Hiromasa Morikawa, Kelly J Hitchens, Fumi Hori, Linda M. van den Berg, Yasushi Okazaki, Andru Tomoiu, Antti Sajantila, Akiko Saka, Thierry Sengstag, Alessandro Bonetti, Haruhiko Koseki, Matthias Edinger, Mitsuhiro Ohshima, Carsten O. Daub, Jayson Harshbarger, Sachi Ishikawa-Kato, Tsugumi Kawashima, Christine L. Mummery, Niklas Mejhert, Jun Takai, Dan Goldowitz, Naoko Suzuki, Guojun Sheng, David A. Hume, Hiroshi Kawamoto, Ai Kaiho, Jun Ichi Furusawa, Ailsa J Carlisle, Tomokatsu Ikawa, Shiro Fukuda, Peter G. Zhang, Akira Hasegawa, James Briggs, Toshio Kitamura, Alistair R. R. Forrest, Takahiro Arakawa, Marcvande Wetering, Shohei Noma, Fumio Nakahara, Jessica Severin, Sven Guhl, Atsushi Kondo, Mary C. Farach-Carson, Hans Clevers, Afsaneh Eslami, Christian Schmidl, Peter Heutink, Hideki Tatsukawa, Anita Schwegmann, Noriko Ninomiya, Antje Blumenthal, Yoshihide Hayashizaki, Suzana Savvi, Thomas J. Ha, Claudio Schneider, Daisuke Sugiyama, Hironori Satoh, Mitsuru Morimoto, Hiroki Sato, Yosuke Mizuno, Meenhard Herlyn, Hozumi Motohashi, Shigehiro Yoshida, Hiroo Toyoda, Christophe Simon, Piero Carninci, Tadasuke Nozaki, Hideya Kawaji, Louise N. Winteringham, Swati Pradhan-Bhatt, Imad Abugessaisa, Michihira Tagami, Tony J. Kenna, Yoko Yamaguchi, Geoffrey J. Faulkner, Alka Saxena, Naoto Kondo, Dmitry A. Ovchinnikov, Rie Fujita, Ernst J. Wolvetang, Michael Detmar, Miki Kojima, Peter Arner, Mitsuko Hara, Stefano Gustincich, Carrie A. Davis, Judith S. Kempfle, Margaret Patrikakis, Alan Mackay-Sim, Carmelo Ferrai, Yutaka Nakachi, Juha Kere, Mitsuyoshi Murata, Shimon Sakaguchi, Soichi Ogishima, Silvia Zucchelli, Andreas Lennartsson, Thomas R. Gingeras, Masanori Suzuki, Beatrice Bodega, Sugata Roy, Sayaka Nagao-Sato, Mitsuhiro Endoh, Anna Ehrlund, J Kenneth Baillie, Mizuho Sakai, Michela Fagiolini, Taeko Dohi, Christine A. Wells, Frank Brombacher, Masayuki Yamamoto, Robert Passier, Lynsey Fairbairn, Teunis B. H. Geijtenbeek, Shigeo Koyasu, Hiromi Nishiyori-Sueki, Yuri Ishizu, Yuki I. Kawamura, Chiyo Yanagi-Mizuochi, Roberto Verardo, Misako Yoneda, Mariko Okada-Hatakeyama, Kaoru Kaida, Ana Pombo, Gundula Schulze-Tanzil, Lesley M. Forrester, Kim M. Summers, Harukazu Suzuki, Naganari Ohkura, Weon Ju Lee, Hiroshi Tanaka, Alan J. Knox, Karl Ekwall, Yukio Nakamura, Serkan Sahin, Shuhei Noguchi, Hiroshi Ohno, Yohei Yonekura, Richard A Axton, Marina Lizio, S. Peter Klinken, Malcolm E. Fisher, Shoko Watanabe, Magda Babina, Xian-Yang Qin, Takaaki Sugiyama, B. Albert S. Edge, Eri Saijyo, Valerio Orlando, Takeya Kasukawa, Kazuyo Moro, Kenichi Nakazato, Naoko Takahashi, Levon M. Khachigian, Chieko Kai, Masaaki Furuno, Jay W. Shin, Hideki Enomoto, Hubrecht Institute for Developmental Biology and Stem Cell Research, AII - Infectious diseases, Infectious diseases, and AII - Amsterdam institute for Infection and Immunity

Subjects
0301 basic medicine, 500 Naturwissenschaften und Mathematik::570 Biowissenschaften, Biologie, Data Descriptor, Molecular biology, 600 Technik, Medizin, angewandte Wissenschaften::610 Medizin und Gesundheit, Genome, Mice, 0302 clinical medicine, Transcription (biology), Promoter Regions, Genetic, Non-U.S. Gov't, Regulation of gene expression, Research Support, Non-U.S. Gov't, Statistics, Computer Science Applications1707 Computer Vision and Pattern Recognition, Computer Science Applications, Library and Information Sciences, Information Systems, Statistics, Probability and Uncertainty, Statistics and Probability, ddc:500, Cell activation, Systems biology, Cell biology, Computational biology, Biology, Research Support, Education, 03 medical and health sciences, Species Specificity, Developmental biology, Journal Article, Animals, Humans, Enhancer, Gene Expression Profiling, Promoter, Cap analysis gene expression, Computational biology and bioinformatics, Gene expression profiling, 030104 developmental biology, Gene Expression Regulation, Cardiovascular and Metabolic Diseases, Probability and Uncertainty, 030217 neurology & neurosurgery
Abstract

Scientific Data, 4, ISSN:2052-4463

Published
2017
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4. An atlas of human long non-coding RNAs with accurate 5′ ends

Author

Yukio Nakamura, Mickal Mendez, Julian Gough, Jessica Severin, Owen J. L. Rackham, Dave Tang, A. Maxwell Burroughs, Masayoshi Itoh, Timo Lassmann, Carsten O. Daub, Leonard Lipovich, Erik Arner, Yoshihide Hayashizaki, Sarah Djebali, Soichi Kojima, Magda Babina, Shohei Noma, Piero Carninci, Hideya Kawaji, Sebastian Schmeier, Peter Heutink, Yulia A. Medvedeva, Tanvir Alam, Alison C. Testa, Elena Denisenko, Marina Lizio, Christine A. Wells, Chi Wai Yip, Akira Hasegawa, Jordan A. Ramilowski, Alistair R. R. Forrest, Michiel J. L. de Hoon, Harukazu Suzuki, Takeya Kasukawa, Nicolas Bertin, Thomas M. Poulsen, Imad Abugessaisa, Jayson Harshbarger, Chung-Chau Hon, Ctr Life Sci Technol, Div Gen Technol, Tsurumi Ku, RIKEN - Institute of Physical and Chemical Research [Japon] (RIKEN), Omics Sci Ctr, Tsurumi Ku, Ctr Translat Med, Canc Sci Inst Singapore, National University of Singapore (NUS), Human Longev Singapore Pte Ltd, Dept Comp Sci, Life Sci, University of Bristol [Bristol], Cardiovasc & Metab Disorders, Duke-NUS Medical School [Singapore], Inst Nat & Math Sci, Biotechnol Res Inst Drug Discovery BRD, Natl Inst Adv Ind Sci & Technol, Prevent Med & Diag Innovat Program, Natl Lib Med, Natl Ctr Biotechnol Informat, Génétique Physiologie et Systèmes d'Elevage (GenPhySE ), École nationale supérieure agronomique de Toulouse [ENSAT]-Institut National de la Recherche Agronomique (INRA)-Ecole Nationale Vétérinaire de Toulouse (ENVT), Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées, Ctr Gen Regulat CRG, Barcelona Institute of Science and Technology (BIST), Universitat Pompeu Fabra [Barcelona] (UPF), Computat Biosci Res Ctr, Comp Elect & Math Sci & Engn Div, King Abdullah University of Science and Technology (KAUST), Biotechnol Res Ctr, Inst Bioengn, the Russian Academy of Sciences [Moscow, Russia] (RAS), Vavilov Inst Gen Genet, Russian Academy of Sciences [Moscow] (RAS), QEII Med Ctr, Harry Perkins Inst Med Res, The University of Western Australia (UWA), Med Res Ctr, Ctr Mol Med & Genet, Wayne State University [Detroit], Sch Med, Dept Neurol, Dept Comp Sci, North Dakota State University (NDSU), Telethon Kids Inst, German Research Center for Neurodegenerative Diseases - Deutsches Zentrum für Neurodegenerative Erkrankungen (DZNE), Dept Dermatol & Allergy, Charité - UniversitätsMedizin = Charité - University Hospital [Berlin], Australian Inst Bioengn & Nanotechno, University of Queensland [Brisbane], Fac Med, Dept Anat & Neurosci, University of Melbourne, CLST Div Biofunct Dynam Imaging, BioResource Ctr, Cell Engn Div, Université de Tsukuba = University of Tsukuba, Dept Biosci & Nutr, Karolinska Institute, QEII Med Ctr, Harry Perkins Inst Med Re, Duke NUS Medical School, Institut National de la Recherche Agronomique (INRA)-Ecole Nationale Vétérinaire de Toulouse (ENVT), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-École nationale supérieure agronomique de Toulouse [ENSAT], Universitat Pompeu Fabra [Barcelona], Russian Academy of Sciences, Wayne State University, Charité - Universitätsmedizin Berlin / Charite - University Medicine Berlin, and University of Tsukuba

Subjects
0301 basic medicine, RNA Stability, [SDV]Life Sciences [q-bio], genetics [Transcriptome], Datasets as Topic, genetics [RNA, Long Noncoding], Genome, Epigenesis, Genetic, 0302 clinical medicine, Databases, Genetic, Promoter Regions, Genetic, Cells, Cultured, Conserved Sequence, Genetics, Regulation of gene expression, Multidisciplinary, genetics [Organ Specificity], Genomics, Enhancer Elements, Genetic, annotation, Organ Specificity, 030220 oncology & carcinogenesis, RNA, Long Noncoding, ddc:500, pr interval, transcription, architecture, Quantitative Trait Loci, Biology, Polymorphism, Single Nucleotide, Article, genetics [RNA, Messenger], 03 medical and health sciences, seq, evolution, genetics [Conserved Sequence], Humans, genetics [Genome, Human], RNA, Messenger, Gene, Internet, genetics [Quantitative Trait Loci], Genome, Human, Gene Expression Profiling, genetics [Enhancer Elements, Genetic], Molecular Sequence Annotation, landscape, gene-expression, Cap analysis gene expression, promoter usage, Gene expression profiling, chemistry [RNA, Long Noncoding], 030104 developmental biology, Gene Expression Regulation, genetics [Promoter Regions, Genetic], Expression quantitative trait loci, genome-wide association, Human genome, Transcriptome, Genome-Wide Association Study
Abstract

Long non-coding RNAs (lncRNAs) are largely heterogeneous and functionally uncharacterized. Here, using FANTOM5 cap analysis of gene expression (CAGE) data, we integrate multiple transcript collections to generate a comprehensive atlas of 27,919 human lncRNA genes with high-confidence 5' ends and expression profiles across 1,829 samples from the major human primary cell types and tissues. Genomic and epigenomic classification of these lncRNAs reveals that most intergenic lncRNAs originate from enhancers rather than from promoters. Incorporating genetic and expression data, we show that lncRNAs overlapping trait-associated single nucleotide polymorphisms are specifically expressed in cell types relevant to the traits, implicating these lncRNAs in multiple diseases. We further demonstrate that lncRNAs overlapping expression quantitative trait loci (eQTL)-associated single nucleotide polymorphisms of messenger RNAs are co-expressed with the corresponding messenger RNAs, suggesting their potential roles in transcriptional regulation. Combining these findings with conservation data, we identify 19,175 potentially functional lncRNAs in the human genome.

Published
2017
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5. The transcriptional network that controls growth arrest and differentiation in a human myeloid leukemia cell line

Author

Albin Sandelin, Takashi Gojobori, Timo Lassmann, Hiroshi Asahara, Claes Wahlestedt, Lukasz Huminiecki, Georges St. Laurent, Yoshinari Ando, Takehiro Hashimoto, Denis C. Bauer, Ariel S. Schwartz, Pär G. Engström, Michael Rehli, Hiromi Nishiyori, Katharine M. Irvine, Andreas Lennartsson, Susanne Heinzel, Yoichi Takenaka, Ole Winther, Nicole Cloonan, Megumi Hashimoto, Winston Hide, Takuma Sano, Boris Lenhard, Michiel J. L. de Hoon, Sarah A. Teichmann, Timothy Ravasi, Naoko Imamoto, Ryoko Ishihara, Syuhei Kimura, Mariko Hatakeyama, Yusuke Inoue, Joe Chiba, Shizu Takeda, Linda Wu, Julian Gough, John Quackenbush, Miho Sera, Yasumasa Kimura, Vladimir B. Bajic, Frank Brombacher, Kazumi Yamaguchi, Toshitsugu Okayama, David Fredman, Hideya Kawaji, Colin A. Semple, Ryan J. Taft, Cas Simons, Ko Fujimori, Masaaki Furuno, Andrew Waterhouse, Ajit Kumar, Jesper Tegnér, Tsugumi Kawashima, Nikolai Petrovsky, J. Lynn Fink, Michihira Tagami, Jun Otomo, Etsuko Miyamoto-Sato, Shiro Fukuda, Cameron Ross MacPherson, Shintaro Katayama, Erika Bulger, Toshio Kojima, Alistair R. R. Forrest, Anders Jacobsen, Yasushi Okazaki, Rohan D. Teasdale, Chikatoshi Kai, Johan Björkegren, Takahiro Suzuki, Carsten O. Daub, Christian Schönbach, Miki Kojima, Sebastian Schmeier, Alistair M. Chalk, Hiroaki Kitano, Sanne Nygaard, Kazuhiko Nakabayashi, Kai Tan, Yasuhiro Tomaru, Noriko Ninomiya, Piotr J. Balwierz, Marina Lizio, Altuna Akalin, Maki Asada, Norihiro Maeda, Satoshi Inoue, Takahiro Arakawa, Shohei Noma, Adam Dawe, Michael Hörnquist, Mika Gustafsson, Stuart Meier, Sei Miyamoto, Ryuichiro Kimura, Takeshi Konno, Kate Schroder, Christine A. Wells, Kazunori Waki, Christopher G. Maher, Nicolas Bertin, Ai Kaiho, Chihiro Ogawa, Shinji Kondo, Mika Nakano, Sean M. Grimmond, Matthew J. Sweet, Jun Yasuda, Aleksandar Radovanovic, Valerio Orlando, Yukari Takahashi, Mihaela Zavolan, Jessica Severin, Markus C. Kerr, Anders Krogh, Hiroshi Yanagawa, Hisashi Miura, John S. Mattick, Eivind Valen, Josée Dostie, Magbubah Essack, Monique Maqungo, Haruka Okuda-Yabukami, Oliver Hofmann, Anthony G Beckhouse, Rintaro Saito, Yutaka Nakachi, Yuki Hasegawa, Masanori Suzuki, Mitsuyoshi Murata, Harukazu Suzuki, Nicholas Matigian, Takao Iwayanagi, Hisashi Koga, Jun Kawai, Hideo Matsuda, Charles Plessy, Mikhail Pachkov, Kengo Imamura, Morten Lindow, Yayoi Kitazume, Erik Arner, Kazuho Ikeo, Yoshihide Hayashizaki, Timothy L. Bailey, Geoffrey J. Faulkner, Martin S. Taylor, Mutsumi Kanamori-Katayama, Mandeep Kaur, Christophe Simon, Piero Carninci, Atsutaka Kubosaki, Chika Kawazu, Katsuhiko Shirahige, Adele Kruger, Jessica C. Mar, Kayoko Murakami, David A. Hume, and Erik van Nimwegen

Subjects
Transcription, Genetic, Cellular differentiation, Molecular Sequence Data, Gene regulatory network, Biology, Bioinformatics, Article, Cell Line, 03 medical and health sciences, 0302 clinical medicine, Transcription (biology), Serum response factor, Genetics, Humans, Gene Regulatory Networks, RNA, Small Interfering, Promoter Regions, Genetic, Transcription factor, 030304 developmental biology, Cell Proliferation, Oligonucleotide Array Sequence Analysis, 0303 health sciences, Base Sequence, Models, Genetic, Gene Expression Profiling, Pioneer factor, Myeloid leukemia, Cell Differentiation, Cell biology, Gene expression profiling, Leukemia, Myeloid, 030220 oncology & carcinogenesis
Abstract

Using deep sequencing (deepCAGE), the FANTOM4 study measured the genome-wide dynamics of transcription-start-site usage in the human monocytic cell line THP-1 throughout a time course of growth arrest and differentiation. Modeling the expression dynamics in terms of predicted cis-regulatory sites, we identified the key transcription regulators, their time-dependent activities and target genes. Systematic siRNA knockdown of 52 transcription factors confirmed the roles of individual factors in the regulatory network. Our results indicate that cellular states are constrained by complex networks involving both positive and negative regulatory interactions among substantial numbers of transcription factors and that no single transcription factor is both necessary and sufficient to drive the differentiation process.

Published
2009
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