A comparative encyclopedia of DNA elements in the mouse genome

Feng Yue; Yong Cheng; Alessandra Breschi; Jeff Vierstra; Weisheng Wu; Tyrone Ryba; Richard Sandstrom; Zhihai Ma; Carrie Davis; Benjamin D. Pope; Yin Shen; Dmitri D. Pervouchine; Sarah Djebali; Robert E. Thurman; Rajinder Kaul; Eric Rynes; Anthony Kirilusha; Georgi K. Marinov; Brian A. Williams; Diane Trout; Henry Amrhein; Katherine Fisher-Aylor; Igor Antoshechkin; Gilberto DeSalvo; Lei Hoon See; Meagan Fastuca; Jorg Drenkow; Chris Zaleski; Alex Dobin; Pablo Prieto; Julien Lagarde; Giovanni Bussotti; Andrea Tanzer; Olgert Denas; Kanwei Li; M. A. Bender; Miaohua Zhang; Rachel Byron; Mark T. Groudine; David McCleary; Long Pham; Zhen Ye; Samantha Kuan; Lee Edsall; Yi Chieh Wu; Matthew D. Rasmussen; Mukul S. Bansal; Manolis Kellis; Cheryl A. Keller; Christapher S. Morrissey; Tejaswini Mishra; Deepti Jain; Nergiz Dogan; Robert S. Harris; Philip Cayting; Trupti Kawli; Alan P. Boyle; Ghia Euskirchen; Anshul Kundaje; Shin Lin; Yiing Lin; Camden Jansen; Venkat S. Malladi; Melissa S. Cline; Drew T. Erickson; Vanessa M. Kirkup; Katrina Learned; Cricket A. Sloan; Kate R. Rosenbloom; Beatriz Lacerda De Sousa; Kathryn Beal; Miguel Pignatelli; Paul Flicek; Jin Lian; Tamer Kahveci; Dongwon Lee; W. James Kent; Miguel Ramalho Santos; Javier Herrero; Cedric Notredame; Audra Johnson; Shinny Vong; Kristen Lee; Daniel Bates; Fidencio Neri; Morgan Diegel; Theresa Canfield; Peter J. Sabo; Matthew S. Wilken; Thomas A. Reh; Erika Giste; Anthony Shafer; Tanya Kutyavin; Eric Haugen; Douglas Dunn; Alex P. Reynolds; Shane Neph; Richard Humbert; R. Scott Hansen; Marella De Bruijn; Licia Selleri; Alexander Rudensky; Steven Josefowicz; Robert Samstein; Evan E. Eichler; Stuart H. Orkin; Dana Levasseur; Thalia Papayannopoulou; Kai Hsin Chang; Arthur Skoultchi; Srikanta Gosh; Christine Disteche; Piper Treuting; Yanli Wang; Mitchell J. Weiss; Gerd A. Blobel; Xiaoyi Cao; Sheng Zhong; Ting Wang; Peter J. Good; Rebecca F. Lowdon; Leslie B. Adams; Xiao Qiao Zhou; Michael J. Pazin; Elise A. Feingold; Barbara Wold; James Taylor; Ali Mortazavi; Sherman M. Weissman; John A. Stamatoyannopoulos; Michael P. Snyder; Roderic Guigo; Thomas R. Gingeras; David M. Gilbert; Ross C. Hardison; Michael A. Beer; Bing Ren

doi:10.1038/nature13992

A comparative encyclopedia of DNA elements in the mouse genome

Feng Yue, Yong Cheng, Alessandra Breschi, Jeff Vierstra, Weisheng Wu, Tyrone Ryba, Richard Sandstrom, Zhihai Ma, Carrie Davis, Benjamin D. Pope, Yin Shen, Dmitri D. Pervouchine, Sarah Djebali, Robert E. Thurman, Rajinder Kaul, Eric Rynes, Anthony Kirilusha, Georgi K. Marinov, Brian A. Williams, Diane TroutHenry Amrhein, Katherine Fisher-Aylor, Igor Antoshechkin, Gilberto DeSalvo, Lei Hoon See, Meagan Fastuca, Jorg Drenkow, Chris Zaleski, Alex Dobin, Pablo Prieto, Julien Lagarde, Giovanni Bussotti, Andrea Tanzer, Olgert Denas, Kanwei Li, M. A. Bender, Miaohua Zhang, Rachel Byron, Mark T. Groudine, David McCleary, Long Pham, Zhen Ye, Samantha Kuan, Lee Edsall, Yi Chieh Wu, Matthew D. Rasmussen, Mukul S. Bansal, Manolis Kellis, Cheryl A. Keller, Christapher S. Morrissey, Tejaswini Mishra, Deepti Jain, Nergiz Dogan, Robert S. Harris, Philip Cayting, Trupti Kawli, Alan P. Boyle, Ghia Euskirchen, Anshul Kundaje, Shin Lin, Yiing Lin, Camden Jansen, Venkat S. Malladi, Melissa S. Cline, Drew T. Erickson, Vanessa M. Kirkup, Katrina Learned, Cricket A. Sloan, Kate R. Rosenbloom, Beatriz Lacerda De Sousa, Kathryn Beal, Miguel Pignatelli, Paul Flicek, Jin Lian, Tamer Kahveci, Dongwon Lee, W. James Kent, Miguel Ramalho Santos, Javier Herrero, Cedric Notredame, Audra Johnson, Shinny Vong, Kristen Lee, Daniel Bates, Fidencio Neri, Morgan Diegel, Theresa Canfield, Peter J. Sabo, Matthew S. Wilken, Thomas A. Reh, Erika Giste, Anthony Shafer, Tanya Kutyavin, Eric Haugen, Douglas Dunn, Alex P. Reynolds, Shane Neph, Richard Humbert, R. Scott Hansen, Marella De Bruijn, Licia Selleri, Alexander Rudensky, Steven Josefowicz, Robert Samstein, Evan E. Eichler, Stuart H. Orkin, Dana Levasseur, Thalia Papayannopoulou, Kai Hsin Chang, Arthur Skoultchi, Srikanta Gosh, Christine Disteche, Piper Treuting, Yanli Wang, Mitchell J. Weiss, Gerd A. Blobel, Xiaoyi Cao, Sheng Zhong, Ting Wang, Peter J. Good, Rebecca F. Lowdon, Leslie B. Adams, Xiao Qiao Zhou, Michael J. Pazin, Elise A. Feingold, Barbara Wold, James Taylor, Ali Mortazavi, Sherman M. Weissman, John A. Stamatoyannopoulos, Michael P. Snyder, Roderic Guigo, Thomas R. Gingeras, David M. Gilbert, Ross C. Hardison, Michael A. Beer, Bing Ren

Cell Biology

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Abstract

The laboratory mouse shares the majority of its protein-coding genes with humans, making it the premier model organism in biomedical research, yet the two mammals differ in significant ways. To gain greater insights into both shared and species-specific transcriptional and cellular regulatory programs in the mouse, the Mouse ENCODE Consortium has mapped transcription, DNase I hypersensitivity, transcription factor binding, chromatin modifications and replication domains throughout the mouse genome in diverse cell and tissue types. By comparing with the human genome, we not only confirm substantial conservation in the newly annotated potential functional sequences, but also find a large degree of divergence of sequences involved in transcriptional regulation, chromatin state and higher order chromatin organization. Our results illuminate the wide range of evolutionary forces acting on genes and their regulatory regions, and provide a general resource for research into mammalian biology and mechanisms of human diseases.

Original language	English (US)
Pages (from-to)	355-364
Number of pages	10
Journal	Nature
Volume	515
Issue number	7527
DOIs	https://doi.org/10.1038/nature13992
State	Published - Nov 20 2014

ASJC Scopus subject areas

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Yue, F., Cheng, Y., Breschi, A., Vierstra, J., Wu, W., Ryba, T., Sandstrom, R., Ma, Z., Davis, C., Pope, B. D., Shen, Y., Pervouchine, D. D., Djebali, S., Thurman, R. E., Kaul, R., Rynes, E., Kirilusha, A., Marinov, G. K., Williams, B. A., ... Ren, B. (2014). A comparative encyclopedia of DNA elements in the mouse genome. Nature, 515(7527), 355-364. https://doi.org/10.1038/nature13992

Yue, F, Cheng, Y, Breschi, A, Vierstra, J, Wu, W, Ryba, T, Sandstrom, R, Ma, Z, Davis, C, Pope, BD, Shen, Y, Pervouchine, DD, Djebali, S, Thurman, RE, Kaul, R, Rynes, E, Kirilusha, A, Marinov, GK, Williams, BA, Trout, D, Amrhein, H, Fisher-Aylor, K, Antoshechkin, I, DeSalvo, G, See, LH, Fastuca, M, Drenkow, J, Zaleski, C, Dobin, A, Prieto, P, Lagarde, J, Bussotti, G, Tanzer, A, Denas, O, Li, K, Bender, MA, Zhang, M, Byron, R, Groudine, MT, McCleary, D, Pham, L, Ye, Z, Kuan, S, Edsall, L, Wu, YC, Rasmussen, MD, Bansal, MS, Kellis, M, Keller, CA, Morrissey, CS, Mishra, T, Jain, D, Dogan, N, Harris, RS, Cayting, P, Kawli, T, Boyle, AP, Euskirchen, G, Kundaje, A, Lin, S, Lin, Y, Jansen, C, Malladi, VS, Cline, MS, Erickson, DT, Kirkup, VM, Learned, K, Sloan, CA, Rosenbloom, KR, De Sousa, BL, Beal, K, Pignatelli, M, Flicek, P, Lian, J, Kahveci, T, Lee, D, Kent, WJ, Santos, MR, Herrero, J, Notredame, C, Johnson, A, Vong, S, Lee, K, Bates, D, Neri, F, Diegel, M, Canfield, T, Sabo, PJ, Wilken, MS, Reh, TA, Giste, E, Shafer, A, Kutyavin, T, Haugen, E, Dunn, D, Reynolds, AP, Neph, S, Humbert, R, Hansen, RS, De Bruijn, M, Selleri, L, Rudensky, A, Josefowicz, S, Samstein, R, Eichler, EE, Orkin, SH, Levasseur, D, Papayannopoulou, T, Chang, KH, Skoultchi, A, Gosh, S, Disteche, C, Treuting, P, Wang, Y, Weiss, MJ, Blobel, GA, Cao, X, Zhong, S, Wang, T, Good, PJ, Lowdon, RF, Adams, LB, Zhou, XQ, Pazin, MJ, Feingold, EA, Wold, B, Taylor, J, Mortazavi, A, Weissman, SM, Stamatoyannopoulos, JA, Snyder, MP, Guigo, R, Gingeras, TR, Gilbert, DM, Hardison, RC, Beer, MA & Ren, B 2014, 'A comparative encyclopedia of DNA elements in the mouse genome', Nature, vol. 515, no. 7527, pp. 355-364. https://doi.org/10.1038/nature13992

@article{bbac2b2f86614b4da95b21d1ccb28a36,

title = "A comparative encyclopedia of DNA elements in the mouse genome",

abstract = "The laboratory mouse shares the majority of its protein-coding genes with humans, making it the premier model organism in biomedical research, yet the two mammals differ in significant ways. To gain greater insights into both shared and species-specific transcriptional and cellular regulatory programs in the mouse, the Mouse ENCODE Consortium has mapped transcription, DNase I hypersensitivity, transcription factor binding, chromatin modifications and replication domains throughout the mouse genome in diverse cell and tissue types. By comparing with the human genome, we not only confirm substantial conservation in the newly annotated potential functional sequences, but also find a large degree of divergence of sequences involved in transcriptional regulation, chromatin state and higher order chromatin organization. Our results illuminate the wide range of evolutionary forces acting on genes and their regulatory regions, and provide a general resource for research into mammalian biology and mechanisms of human diseases.",

author = "Feng Yue and Yong Cheng and Alessandra Breschi and Jeff Vierstra and Weisheng Wu and Tyrone Ryba and Richard Sandstrom and Zhihai Ma and Carrie Davis and Pope, {Benjamin D.} and Yin Shen and Pervouchine, {Dmitri D.} and Sarah Djebali and Thurman, {Robert E.} and Rajinder Kaul and Eric Rynes and Anthony Kirilusha and Marinov, {Georgi K.} and Williams, {Brian A.} and Diane Trout and Henry Amrhein and Katherine Fisher-Aylor and Igor Antoshechkin and Gilberto DeSalvo and See, {Lei Hoon} and Meagan Fastuca and Jorg Drenkow and Chris Zaleski and Alex Dobin and Pablo Prieto and Julien Lagarde and Giovanni Bussotti and Andrea Tanzer and Olgert Denas and Kanwei Li and Bender, {M. A.} and Miaohua Zhang and Rachel Byron and Groudine, {Mark T.} and David McCleary and Long Pham and Zhen Ye and Samantha Kuan and Lee Edsall and Wu, {Yi Chieh} and Rasmussen, {Matthew D.} and Bansal, {Mukul S.} and Manolis Kellis and Keller, {Cheryl A.} and Morrissey, {Christapher S.} and Tejaswini Mishra and Deepti Jain and Nergiz Dogan and Harris, {Robert S.} and Philip Cayting and Trupti Kawli and Boyle, {Alan P.} and Ghia Euskirchen and Anshul Kundaje and Shin Lin and Yiing Lin and Camden Jansen and Malladi, {Venkat S.} and Cline, {Melissa S.} and Erickson, {Drew T.} and Kirkup, {Vanessa M.} and Katrina Learned and Sloan, {Cricket A.} and Rosenbloom, {Kate R.} and {De Sousa}, {Beatriz Lacerda} and Kathryn Beal and Miguel Pignatelli and Paul Flicek and Jin Lian and Tamer Kahveci and Dongwon Lee and Kent, {W. James} and Santos, {Miguel Ramalho} and Javier Herrero and Cedric Notredame and Audra Johnson and Shinny Vong and Kristen Lee and Daniel Bates and Fidencio Neri and Morgan Diegel and Theresa Canfield and Sabo, {Peter J.} and Wilken, {Matthew S.} and Reh, {Thomas A.} and Erika Giste and Anthony Shafer and Tanya Kutyavin and Eric Haugen and Douglas Dunn and Reynolds, {Alex P.} and Shane Neph and Richard Humbert and Hansen, {R. Scott} and {De Bruijn}, Marella and Licia Selleri and Alexander Rudensky and Steven Josefowicz and Robert Samstein and Eichler, {Evan E.} and Orkin, {Stuart H.} and Dana Levasseur and Thalia Papayannopoulou and Chang, {Kai Hsin} and Arthur Skoultchi and Srikanta Gosh and Christine Disteche and Piper Treuting and Yanli Wang and Weiss, {Mitchell J.} and Blobel, {Gerd A.} and Xiaoyi Cao and Sheng Zhong and Ting Wang and Good, {Peter J.} and Lowdon, {Rebecca F.} and Adams, {Leslie B.} and Zhou, {Xiao Qiao} and Pazin, {Michael J.} and Feingold, {Elise A.} and Barbara Wold and James Taylor and Ali Mortazavi and Weissman, {Sherman M.} and Stamatoyannopoulos, {John A.} and Snyder, {Michael P.} and Roderic Guigo and Gingeras, {Thomas R.} and Gilbert, {David M.} and Hardison, {Ross C.} and Beer, {Michael A.} and Bing Ren",

note = "Funding Information: Acknowledgements This work is funded by grants R01HG003991 (B.R.), 1U54HG007004 (T.R.G.), 3RC2HG005602 (M.P.S.), GM083337 and GM085354 (D.M.G.), F31CA165863 (B.D.P.), RC2HG005573 andR01DK065806 (R.C.H.) from the National Institutes of Health, andBIO2011-26205 from the Spanish Plan Nacional and ERC 294653 (to R.G.). J.V. is supported by a National Science Foundation Graduate Research Fellowship under grant no. DGE-071824. K.B., M.P., J.H. and P.F. acknowledge the Wellcome Trust (grant number 095908), the NHGRI (grant number U01HG004695) and the European Molecular Biology Laboratory. We thank G. Hon for helping the analysis of high-throughput enhancer validation. L.S. is supported by R01HD043997-09. S.L. was supported by grants F32HL110473 and K99HL119617. Publisher Copyright: {\textcopyright} 2014 Macmillan Publishers Limited. All rights reserved.",

year = "2014",

month = nov,

day = "20",

doi = "10.1038/nature13992",

language = "English (US)",

volume = "515",

pages = "355--364",

journal = "Nature",

issn = "0028-0836",

publisher = "Nature Publishing Group",

number = "7527",

}

TY - JOUR

T1 - A comparative encyclopedia of DNA elements in the mouse genome

AU - Yue, Feng

AU - Cheng, Yong

AU - Breschi, Alessandra

AU - Vierstra, Jeff

AU - Wu, Weisheng

AU - Ryba, Tyrone

AU - Sandstrom, Richard

AU - Ma, Zhihai

AU - Davis, Carrie

AU - Pope, Benjamin D.

AU - Shen, Yin

AU - Pervouchine, Dmitri D.

AU - Djebali, Sarah

AU - Thurman, Robert E.

AU - Kaul, Rajinder

AU - Rynes, Eric

AU - Kirilusha, Anthony

AU - Marinov, Georgi K.

AU - Williams, Brian A.

AU - Trout, Diane

AU - Amrhein, Henry

AU - Fisher-Aylor, Katherine

AU - Antoshechkin, Igor

AU - DeSalvo, Gilberto

AU - See, Lei Hoon

AU - Fastuca, Meagan

AU - Drenkow, Jorg

AU - Zaleski, Chris

AU - Dobin, Alex

AU - Prieto, Pablo

AU - Lagarde, Julien

AU - Bussotti, Giovanni

AU - Tanzer, Andrea

AU - Denas, Olgert

AU - Li, Kanwei

AU - Bender, M. A.

AU - Zhang, Miaohua

AU - Byron, Rachel

AU - Groudine, Mark T.

AU - McCleary, David

AU - Pham, Long

AU - Ye, Zhen

AU - Kuan, Samantha

AU - Edsall, Lee

AU - Wu, Yi Chieh

AU - Rasmussen, Matthew D.

AU - Bansal, Mukul S.

AU - Kellis, Manolis

AU - Keller, Cheryl A.

AU - Morrissey, Christapher S.

AU - Mishra, Tejaswini

AU - Jain, Deepti

AU - Dogan, Nergiz

AU - Harris, Robert S.

AU - Cayting, Philip

AU - Kawli, Trupti

AU - Boyle, Alan P.

AU - Euskirchen, Ghia

AU - Kundaje, Anshul

AU - Lin, Shin

AU - Lin, Yiing

AU - Jansen, Camden

AU - Malladi, Venkat S.

AU - Cline, Melissa S.

AU - Erickson, Drew T.

AU - Kirkup, Vanessa M.

AU - Learned, Katrina

AU - Sloan, Cricket A.

AU - Rosenbloom, Kate R.

AU - De Sousa, Beatriz Lacerda

AU - Beal, Kathryn

AU - Pignatelli, Miguel

AU - Flicek, Paul

AU - Lian, Jin

AU - Kahveci, Tamer

AU - Lee, Dongwon

AU - Kent, W. James

AU - Santos, Miguel Ramalho

AU - Herrero, Javier

AU - Notredame, Cedric

AU - Johnson, Audra

AU - Vong, Shinny

AU - Lee, Kristen

AU - Bates, Daniel

AU - Neri, Fidencio

AU - Diegel, Morgan

AU - Canfield, Theresa

AU - Sabo, Peter J.

AU - Wilken, Matthew S.

AU - Reh, Thomas A.

AU - Giste, Erika

AU - Shafer, Anthony

AU - Kutyavin, Tanya

AU - Haugen, Eric

AU - Dunn, Douglas

AU - Reynolds, Alex P.

AU - Neph, Shane

AU - Humbert, Richard

AU - Hansen, R. Scott

AU - De Bruijn, Marella

AU - Selleri, Licia

AU - Rudensky, Alexander

AU - Josefowicz, Steven

AU - Samstein, Robert

AU - Eichler, Evan E.

AU - Orkin, Stuart H.

AU - Levasseur, Dana

AU - Papayannopoulou, Thalia

AU - Chang, Kai Hsin

AU - Skoultchi, Arthur

AU - Gosh, Srikanta

AU - Disteche, Christine

AU - Treuting, Piper

AU - Wang, Yanli

AU - Weiss, Mitchell J.

AU - Blobel, Gerd A.

AU - Cao, Xiaoyi

AU - Zhong, Sheng

AU - Wang, Ting

AU - Good, Peter J.

AU - Lowdon, Rebecca F.

AU - Adams, Leslie B.

AU - Zhou, Xiao Qiao

AU - Pazin, Michael J.

AU - Feingold, Elise A.

AU - Wold, Barbara

AU - Taylor, James

AU - Mortazavi, Ali

AU - Weissman, Sherman M.

AU - Stamatoyannopoulos, John A.

AU - Snyder, Michael P.

AU - Guigo, Roderic

AU - Gingeras, Thomas R.

AU - Gilbert, David M.

AU - Hardison, Ross C.

AU - Beer, Michael A.

AU - Ren, Bing

N1 - Funding Information: Acknowledgements This work is funded by grants R01HG003991 (B.R.), 1U54HG007004 (T.R.G.), 3RC2HG005602 (M.P.S.), GM083337 and GM085354 (D.M.G.), F31CA165863 (B.D.P.), RC2HG005573 andR01DK065806 (R.C.H.) from the National Institutes of Health, andBIO2011-26205 from the Spanish Plan Nacional and ERC 294653 (to R.G.). J.V. is supported by a National Science Foundation Graduate Research Fellowship under grant no. DGE-071824. K.B., M.P., J.H. and P.F. acknowledge the Wellcome Trust (grant number 095908), the NHGRI (grant number U01HG004695) and the European Molecular Biology Laboratory. We thank G. Hon for helping the analysis of high-throughput enhancer validation. L.S. is supported by R01HD043997-09. S.L. was supported by grants F32HL110473 and K99HL119617. Publisher Copyright: © 2014 Macmillan Publishers Limited. All rights reserved.

PY - 2014/11/20

Y1 - 2014/11/20

N2 - The laboratory mouse shares the majority of its protein-coding genes with humans, making it the premier model organism in biomedical research, yet the two mammals differ in significant ways. To gain greater insights into both shared and species-specific transcriptional and cellular regulatory programs in the mouse, the Mouse ENCODE Consortium has mapped transcription, DNase I hypersensitivity, transcription factor binding, chromatin modifications and replication domains throughout the mouse genome in diverse cell and tissue types. By comparing with the human genome, we not only confirm substantial conservation in the newly annotated potential functional sequences, but also find a large degree of divergence of sequences involved in transcriptional regulation, chromatin state and higher order chromatin organization. Our results illuminate the wide range of evolutionary forces acting on genes and their regulatory regions, and provide a general resource for research into mammalian biology and mechanisms of human diseases.

AB - The laboratory mouse shares the majority of its protein-coding genes with humans, making it the premier model organism in biomedical research, yet the two mammals differ in significant ways. To gain greater insights into both shared and species-specific transcriptional and cellular regulatory programs in the mouse, the Mouse ENCODE Consortium has mapped transcription, DNase I hypersensitivity, transcription factor binding, chromatin modifications and replication domains throughout the mouse genome in diverse cell and tissue types. By comparing with the human genome, we not only confirm substantial conservation in the newly annotated potential functional sequences, but also find a large degree of divergence of sequences involved in transcriptional regulation, chromatin state and higher order chromatin organization. Our results illuminate the wide range of evolutionary forces acting on genes and their regulatory regions, and provide a general resource for research into mammalian biology and mechanisms of human diseases.

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U2 - 10.1038/nature13992

DO - 10.1038/nature13992

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C2 - 25409824

AN - SCOPUS:84911462077

VL - 515

SP - 355

EP - 364

JO - Nature

JF - Nature

SN - 0028-0836

IS - 7527

ER -

A comparative encyclopedia of DNA elements in the mouse genome

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