Transcribed enhancers lead waves of coordinated transcription in transitioning mammalian cells

Erik Arner, Carsten O. Daub, Kristoffer Vitting-Seerup, Robin Andersson, Berit Lilje, Finn Drabløs, Andreas Lennartsson, Michelle Rönnerblad, Olga Hrydziuszko, Morana Vitezic, Tom C. Freeman, Ahmad M N Alhendi, Peter Arner, Richard Axton, J. Kenneth Baillie, Anthony Beckhouse, Beatrice Bodega, James Briggs, Frank Brombacher, Margaret DavisMichael Detmar, Anna Ehrlund, Mitsuhiro Endoh, Afsaneh Eslami, Michela Fagiolini, Lynsey Fairbairn, Geoffrey J. Faulkner, Carmelo Ferrai, Malcolm E. Fisher, Lesley Forrester, Daniel Goldowitz, Reto Guler, Thomas Ha, Mitsuko Hara, Meenhard Herlyn, Tomokatsu Ikawa, Chieko Kai, Hiroshi Kawamoto, Levon M. Khachigian, S. Peter Klinken, Soichi Kojima, Haruhiko Koseki, Sarah Klein, Niklas Mejhert, Ken Miyaguchi, Yosuke Mizuno, Mitsuru Morimoto, Kelly J. Morris, Christine Mummery, Yutaka Nakachi, Soichi Ogishima, Mariko Okada-Hatakeyama, Yasushi Okazaki, Valerio Orlando, Dmitry Ovchinnikov, Robert Passier, Margaret Patrikakis, Ana Pombo, Xian Yang Qin, Sugata Roy, Hiroki Sato, Suzana Savvi, Alka Saxena, Anita Schwegmann, Daisuke Sugiyama, Rolf Swoboda, Hiroshi Tanaka, Andru Tomoiu, Louise N. Winteringham, Ernst Wolvetang, Chiyo Yanagi-Mizuochi, Misako Yoneda, Susan Zabierowski, Peter Zhang, Imad Abugessaisa, Nicolas Bertin, Alexander D. Diehl, Shiro Fukuda, Masaaki Furuno, Jayson Harshbarger, Akira Hasegawa, Fumi Hori, Sachi Ishikawa-Kato, Yuri Ishizu, Masayoshi Itoh, Tsugumi Kawashima, Miki Kojima, Naoto Kondo, Marina Lizio, Terrence F. Meehan, Christopher J. Mungall, Mitsuyoshi Murata, Hiromi Nishiyori-Sueki, Serkan Sahin, Sayaka Nagao-Sato, Jessica Severin, Michiel J L De Hoon, Jun Kawai, Takeya Kasukawa, Timo Lassmann, Harukazu Suzuki, Hideya Kawaji, Kim M. Summers, Christine Wells, David A. Hume, Alistair R R Forrest, Albin Sandelin, Piero Carninci, Yoshihide Hayashizaki

Research output: Contribution to journalArticle

238 Citations (Scopus)

Abstract

Although it is generally accepted that cellular differentiation requires changes to transcriptional networks, dynamic regulation of promoters and enhancers at specific sets of genes has not been previously studied en masse. Exploiting the fact that active promoters and enhancers are transcribed, we simultaneously measured their activity in 19 human and 14 mouse time courses covering a wide range of cell types and biological stimuli. Enhancer RNAs, then messenger RNAs encoding transcription factors, dominated the earliest responses. Binding sites for key lineage transcription factors were simultaneously overrepresented in enhancers and promoters active in each cellular system. Our data support a highly generalizable model in which enhancer transcription is the earliest event in successive waves of transcriptional change during cellular differentiation or activation.

Original languageEnglish
Pages (from-to)1010-1014
Number of pages5
JournalScience
Volume347
Issue number6225
DOIs
Publication statusPublished - Feb 27 2015

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Transcription Factors
Gene Regulatory Networks
Binding Sites
RNA
Messenger RNA
Genes

ASJC Scopus subject areas

  • General
  • Medicine(all)

Cite this

Arner, E., Daub, C. O., Vitting-Seerup, K., Andersson, R., Lilje, B., Drabløs, F., ... Hayashizaki, Y. (2015). Transcribed enhancers lead waves of coordinated transcription in transitioning mammalian cells. Science, 347(6225), 1010-1014. https://doi.org/10.1126/science.1259418

Transcribed enhancers lead waves of coordinated transcription in transitioning mammalian cells. / Arner, Erik; Daub, Carsten O.; Vitting-Seerup, Kristoffer; Andersson, Robin; Lilje, Berit; Drabløs, Finn; Lennartsson, Andreas; Rönnerblad, Michelle; Hrydziuszko, Olga; Vitezic, Morana; Freeman, Tom C.; Alhendi, Ahmad M N; Arner, Peter; Axton, Richard; Baillie, J. Kenneth; Beckhouse, Anthony; Bodega, Beatrice; Briggs, James; Brombacher, Frank; Davis, Margaret; Detmar, Michael; Ehrlund, Anna; Endoh, Mitsuhiro; Eslami, Afsaneh; Fagiolini, Michela; Fairbairn, Lynsey; Faulkner, Geoffrey J.; Ferrai, Carmelo; Fisher, Malcolm E.; Forrester, Lesley; Goldowitz, Daniel; Guler, Reto; Ha, Thomas; Hara, Mitsuko; Herlyn, Meenhard; Ikawa, Tomokatsu; Kai, Chieko; Kawamoto, Hiroshi; Khachigian, Levon M.; Klinken, S. Peter; Kojima, Soichi; Koseki, Haruhiko; Klein, Sarah; Mejhert, Niklas; Miyaguchi, Ken; Mizuno, Yosuke; Morimoto, Mitsuru; Morris, Kelly J.; Mummery, Christine; Nakachi, Yutaka; Ogishima, Soichi; Okada-Hatakeyama, Mariko; Okazaki, Yasushi; Orlando, Valerio; Ovchinnikov, Dmitry; Passier, Robert; Patrikakis, Margaret; Pombo, Ana; Qin, Xian Yang; Roy, Sugata; Sato, Hiroki; Savvi, Suzana; Saxena, Alka; Schwegmann, Anita; Sugiyama, Daisuke; Swoboda, Rolf; Tanaka, Hiroshi; Tomoiu, Andru; Winteringham, Louise N.; Wolvetang, Ernst; Yanagi-Mizuochi, Chiyo; Yoneda, Misako; Zabierowski, Susan; Zhang, Peter; Abugessaisa, Imad; Bertin, Nicolas; Diehl, Alexander D.; Fukuda, Shiro; Furuno, Masaaki; Harshbarger, Jayson; Hasegawa, Akira; Hori, Fumi; Ishikawa-Kato, Sachi; Ishizu, Yuri; Itoh, Masayoshi; Kawashima, Tsugumi; Kojima, Miki; Kondo, Naoto; Lizio, Marina; Meehan, Terrence F.; Mungall, Christopher J.; Murata, Mitsuyoshi; Nishiyori-Sueki, Hiromi; Sahin, Serkan; Nagao-Sato, Sayaka; Severin, Jessica; De Hoon, Michiel J L; Kawai, Jun; Kasukawa, Takeya; Lassmann, Timo; Suzuki, Harukazu; Kawaji, Hideya; Summers, Kim M.; Wells, Christine; Hume, David A.; Forrest, Alistair R R; Sandelin, Albin; Carninci, Piero; Hayashizaki, Yoshihide.

In: Science, Vol. 347, No. 6225, 27.02.2015, p. 1010-1014.

Research output: Contribution to journalArticle

Arner, E, Daub, CO, Vitting-Seerup, K, Andersson, R, Lilje, B, Drabløs, F, Lennartsson, A, Rönnerblad, M, Hrydziuszko, O, Vitezic, M, Freeman, TC, Alhendi, AMN, Arner, P, Axton, R, Baillie, JK, Beckhouse, A, Bodega, B, Briggs, J, Brombacher, F, Davis, M, Detmar, M, Ehrlund, A, Endoh, M, Eslami, A, Fagiolini, M, Fairbairn, L, Faulkner, GJ, Ferrai, C, Fisher, ME, Forrester, L, Goldowitz, D, Guler, R, Ha, T, Hara, M, Herlyn, M, Ikawa, T, Kai, C, Kawamoto, H, Khachigian, LM, Klinken, SP, Kojima, S, Koseki, H, Klein, S, Mejhert, N, Miyaguchi, K, Mizuno, Y, Morimoto, M, Morris, KJ, Mummery, C, Nakachi, Y, Ogishima, S, Okada-Hatakeyama, M, Okazaki, Y, Orlando, V, Ovchinnikov, D, Passier, R, Patrikakis, M, Pombo, A, Qin, XY, Roy, S, Sato, H, Savvi, S, Saxena, A, Schwegmann, A, Sugiyama, D, Swoboda, R, Tanaka, H, Tomoiu, A, Winteringham, LN, Wolvetang, E, Yanagi-Mizuochi, C, Yoneda, M, Zabierowski, S, Zhang, P, Abugessaisa, I, Bertin, N, Diehl, AD, Fukuda, S, Furuno, M, Harshbarger, J, Hasegawa, A, Hori, F, Ishikawa-Kato, S, Ishizu, Y, Itoh, M, Kawashima, T, Kojima, M, Kondo, N, Lizio, M, Meehan, TF, Mungall, CJ, Murata, M, Nishiyori-Sueki, H, Sahin, S, Nagao-Sato, S, Severin, J, De Hoon, MJL, Kawai, J, Kasukawa, T, Lassmann, T, Suzuki, H, Kawaji, H, Summers, KM, Wells, C, Hume, DA, Forrest, ARR, Sandelin, A, Carninci, P & Hayashizaki, Y 2015, 'Transcribed enhancers lead waves of coordinated transcription in transitioning mammalian cells', Science, vol. 347, no. 6225, pp. 1010-1014. https://doi.org/10.1126/science.1259418
Arner E, Daub CO, Vitting-Seerup K, Andersson R, Lilje B, Drabløs F et al. Transcribed enhancers lead waves of coordinated transcription in transitioning mammalian cells. Science. 2015 Feb 27;347(6225):1010-1014. https://doi.org/10.1126/science.1259418
Arner, Erik ; Daub, Carsten O. ; Vitting-Seerup, Kristoffer ; Andersson, Robin ; Lilje, Berit ; Drabløs, Finn ; Lennartsson, Andreas ; Rönnerblad, Michelle ; Hrydziuszko, Olga ; Vitezic, Morana ; Freeman, Tom C. ; Alhendi, Ahmad M N ; Arner, Peter ; Axton, Richard ; Baillie, J. Kenneth ; Beckhouse, Anthony ; Bodega, Beatrice ; Briggs, James ; Brombacher, Frank ; Davis, Margaret ; Detmar, Michael ; Ehrlund, Anna ; Endoh, Mitsuhiro ; Eslami, Afsaneh ; Fagiolini, Michela ; Fairbairn, Lynsey ; Faulkner, Geoffrey J. ; Ferrai, Carmelo ; Fisher, Malcolm E. ; Forrester, Lesley ; Goldowitz, Daniel ; Guler, Reto ; Ha, Thomas ; Hara, Mitsuko ; Herlyn, Meenhard ; Ikawa, Tomokatsu ; Kai, Chieko ; Kawamoto, Hiroshi ; Khachigian, Levon M. ; Klinken, S. Peter ; Kojima, Soichi ; Koseki, Haruhiko ; Klein, Sarah ; Mejhert, Niklas ; Miyaguchi, Ken ; Mizuno, Yosuke ; Morimoto, Mitsuru ; Morris, Kelly J. ; Mummery, Christine ; Nakachi, Yutaka ; Ogishima, Soichi ; Okada-Hatakeyama, Mariko ; Okazaki, Yasushi ; Orlando, Valerio ; Ovchinnikov, Dmitry ; Passier, Robert ; Patrikakis, Margaret ; Pombo, Ana ; Qin, Xian Yang ; Roy, Sugata ; Sato, Hiroki ; Savvi, Suzana ; Saxena, Alka ; Schwegmann, Anita ; Sugiyama, Daisuke ; Swoboda, Rolf ; Tanaka, Hiroshi ; Tomoiu, Andru ; Winteringham, Louise N. ; Wolvetang, Ernst ; Yanagi-Mizuochi, Chiyo ; Yoneda, Misako ; Zabierowski, Susan ; Zhang, Peter ; Abugessaisa, Imad ; Bertin, Nicolas ; Diehl, Alexander D. ; Fukuda, Shiro ; Furuno, Masaaki ; Harshbarger, Jayson ; Hasegawa, Akira ; Hori, Fumi ; Ishikawa-Kato, Sachi ; Ishizu, Yuri ; Itoh, Masayoshi ; Kawashima, Tsugumi ; Kojima, Miki ; Kondo, Naoto ; Lizio, Marina ; Meehan, Terrence F. ; Mungall, Christopher J. ; Murata, Mitsuyoshi ; Nishiyori-Sueki, Hiromi ; Sahin, Serkan ; Nagao-Sato, Sayaka ; Severin, Jessica ; De Hoon, Michiel J L ; Kawai, Jun ; Kasukawa, Takeya ; Lassmann, Timo ; Suzuki, Harukazu ; Kawaji, Hideya ; Summers, Kim M. ; Wells, Christine ; Hume, David A. ; Forrest, Alistair R R ; Sandelin, Albin ; Carninci, Piero ; Hayashizaki, Yoshihide. / Transcribed enhancers lead waves of coordinated transcription in transitioning mammalian cells. In: Science. 2015 ; Vol. 347, No. 6225. pp. 1010-1014.
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AU - Arner, Erik

AU - Daub, Carsten O.

AU - Vitting-Seerup, Kristoffer

AU - Andersson, Robin

AU - Lilje, Berit

AU - Drabløs, Finn

AU - Lennartsson, Andreas

AU - Rönnerblad, Michelle

AU - Hrydziuszko, Olga

AU - Vitezic, Morana

AU - Freeman, Tom C.

AU - Alhendi, Ahmad M N

AU - Arner, Peter

AU - Axton, Richard

AU - Baillie, J. Kenneth

AU - Beckhouse, Anthony

AU - Bodega, Beatrice

AU - Briggs, James

AU - Brombacher, Frank

AU - Davis, Margaret

AU - Detmar, Michael

AU - Ehrlund, Anna

AU - Endoh, Mitsuhiro

AU - Eslami, Afsaneh

AU - Fagiolini, Michela

AU - Fairbairn, Lynsey

AU - Faulkner, Geoffrey J.

AU - Ferrai, Carmelo

AU - Fisher, Malcolm E.

AU - Forrester, Lesley

AU - Goldowitz, Daniel

AU - Guler, Reto

AU - Ha, Thomas

AU - Hara, Mitsuko

AU - Herlyn, Meenhard

AU - Ikawa, Tomokatsu

AU - Kai, Chieko

AU - Kawamoto, Hiroshi

AU - Khachigian, Levon M.

AU - Klinken, S. Peter

AU - Kojima, Soichi

AU - Koseki, Haruhiko

AU - Klein, Sarah

AU - Mejhert, Niklas

AU - Miyaguchi, Ken

AU - Mizuno, Yosuke

AU - Morimoto, Mitsuru

AU - Morris, Kelly J.

AU - Mummery, Christine

AU - Nakachi, Yutaka

AU - Ogishima, Soichi

AU - Okada-Hatakeyama, Mariko

AU - Okazaki, Yasushi

AU - Orlando, Valerio

AU - Ovchinnikov, Dmitry

AU - Passier, Robert

AU - Patrikakis, Margaret

AU - Pombo, Ana

AU - Qin, Xian Yang

AU - Roy, Sugata

AU - Sato, Hiroki

AU - Savvi, Suzana

AU - Saxena, Alka

AU - Schwegmann, Anita

AU - Sugiyama, Daisuke

AU - Swoboda, Rolf

AU - Tanaka, Hiroshi

AU - Tomoiu, Andru

AU - Winteringham, Louise N.

AU - Wolvetang, Ernst

AU - Yanagi-Mizuochi, Chiyo

AU - Yoneda, Misako

AU - Zabierowski, Susan

AU - Zhang, Peter

AU - Abugessaisa, Imad

AU - Bertin, Nicolas

AU - Diehl, Alexander D.

AU - Fukuda, Shiro

AU - Furuno, Masaaki

AU - Harshbarger, Jayson

AU - Hasegawa, Akira

AU - Hori, Fumi

AU - Ishikawa-Kato, Sachi

AU - Ishizu, Yuri

AU - Itoh, Masayoshi

AU - Kawashima, Tsugumi

AU - Kojima, Miki

AU - Kondo, Naoto

AU - Lizio, Marina

AU - Meehan, Terrence F.

AU - Mungall, Christopher J.

AU - Murata, Mitsuyoshi

AU - Nishiyori-Sueki, Hiromi

AU - Sahin, Serkan

AU - Nagao-Sato, Sayaka

AU - Severin, Jessica

AU - De Hoon, Michiel J L

AU - Kawai, Jun

AU - Kasukawa, Takeya

AU - Lassmann, Timo

AU - Suzuki, Harukazu

AU - Kawaji, Hideya

AU - Summers, Kim M.

AU - Wells, Christine

AU - Hume, David A.

AU - Forrest, Alistair R R

AU - Sandelin, Albin

AU - Carninci, Piero

AU - Hayashizaki, Yoshihide

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