Comparative analysis of metazoan chromatin organization

Joshua W K Ho, Youngsook L. Jung, Tao Liu, Burak H. Alver, Soohyun Lee, Kohta Ikegami, Kyung Ah Sohn, Aki Minoda, Michael Y. Tolstorukov, Alex Appert, Stephen C J Parker, Tingting Gu, Anshul Kundaje, Nicole C. Riddle, Eric Bishop, Thea A. Egelhofer, Sheng'En Shawn Hu, Artyom A. Alekseyenko, Andreas Rechtsteiner, Dalal AskerJason A. Belsky, Sarah K. Bowman, Q. Brent Chen, Ron A J Chen, Daniel S. Day, Yan Dong, Andrea C. Dose, Xikun Duan, Charles B. Epstein, Sevinc Ercan, Elise A. Feingold, Francesco Ferrari, Jacob M. Garrigues, Nils Gehlenborg, Peter J. Good, Psalm Haseley, Daniel He, Moritz Herrmann, Michael M. Hoffman, Tess E. Jeffers, Peter V. Kharchenko, Paulina Kolasinska-Zwierz, Chitra V. Kotwaliwale, Nischay Kumar, Sasha A. Langley, Erica N. Larschan, Isabel Latorre, Maxwell W. Libbrecht, Xueqiu Lin, Richard Park, Michael J. Pazin, Hoang N. Pham, Annette Plachetka, Bo Qin, Yuri B. Schwartz, Noam Shoresh, Przemyslaw Stempor, Anne Vielle, Chengyang Wang, Christina M. Whittle, Huiling Xue, Robert E. Kingston, Ju Han Kim, Bradley E. Bernstein, Abby F. Dernburg, Vincenzo Pirrotta, Mitzi I. Kuroda, William S. Noble, Thomas D. Tullius, Manolis Kellis, David M. MacAlpine, Susan Strome, Sarah C R Elgin, Xiaole Shirley Liu, Jason D. Lieb, Julie Ahringer, Gary H. Karpen, Peter J. Park

Research output: Contribution to journalArticle

Abstract

Genome function is dynamically regulated in part by chromatin, which consists of the histones, non-histone proteins and RNA molecules that package DNA. Studies in Caenorhabditis elegans and Drosophila melanogaster have contributed substantially to our understanding of molecular mechanisms of genome function in humans, and have revealed conservation of chromatin components and mechanisms. Nevertheless, the three organisms have markedly different genome sizes, chromosome architecture and gene organization. On human and fly chromosomes, for example, pericentric heterochromatin flanks single centromeres, whereas worm chromosomes have dispersed heterochromatin-like regions enriched in the distal chromosomal 'arms', and centromeres distributed along their lengths. To systematically investigate chromatin organization and associated gene regulation across species, we generated and analysed a large collection of genome-wide chromatin data sets from cell lines and developmental stages in worm, fly and human. Here we present over 800 new data sets from our ENCODE and modENCODE consortia, bringing the total to over 1,400. Comparison of combinatorial patterns of histone modifications, nuclear lamina-associated domains, organization of large-scale topological domains, chromatin environment at promoters and enhancers, nucleosome positioning, and DNA replication patterns reveals many conserved features of chromatin organization among the three organisms. We also find notable differences in the composition and locations of repressive chromatin. These data sets and analyses provide a rich resource for comparative and species-specific investigations of chromatin composition, organization and function.

Original languageEnglish (US)
Pages (from-to)449-452
Number of pages4
JournalNature
Volume512
Issue number7515
DOIs
StatePublished - Aug 28 2014

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Chromatin
Heterochromatin
Centromere
Genome
Diptera
Histone Code
Chromosomes
Nuclear Lamina
Genome Size
Nucleosomes
Caenorhabditis elegans
Human Chromosomes
Drosophila melanogaster
DNA Replication
Histones
Genes
RNA
Cell Line
DNA
Datasets

ASJC Scopus subject areas

  • General

Cite this

Ho, J. W. K., Jung, Y. L., Liu, T., Alver, B. H., Lee, S., Ikegami, K., ... Park, P. J. (2014). Comparative analysis of metazoan chromatin organization. Nature, 512(7515), 449-452. https://doi.org/10.1038/nature13415

Comparative analysis of metazoan chromatin organization. / Ho, Joshua W K; Jung, Youngsook L.; Liu, Tao; Alver, Burak H.; Lee, Soohyun; Ikegami, Kohta; Sohn, Kyung Ah; Minoda, Aki; Tolstorukov, Michael Y.; Appert, Alex; Parker, Stephen C J; Gu, Tingting; Kundaje, Anshul; Riddle, Nicole C.; Bishop, Eric; Egelhofer, Thea A.; Hu, Sheng'En Shawn; Alekseyenko, Artyom A.; Rechtsteiner, Andreas; Asker, Dalal; Belsky, Jason A.; Bowman, Sarah K.; Chen, Q. Brent; Chen, Ron A J; Day, Daniel S.; Dong, Yan; Dose, Andrea C.; Duan, Xikun; Epstein, Charles B.; Ercan, Sevinc; Feingold, Elise A.; Ferrari, Francesco; Garrigues, Jacob M.; Gehlenborg, Nils; Good, Peter J.; Haseley, Psalm; He, Daniel; Herrmann, Moritz; Hoffman, Michael M.; Jeffers, Tess E.; Kharchenko, Peter V.; Kolasinska-Zwierz, Paulina; Kotwaliwale, Chitra V.; Kumar, Nischay; Langley, Sasha A.; Larschan, Erica N.; Latorre, Isabel; Libbrecht, Maxwell W.; Lin, Xueqiu; Park, Richard; Pazin, Michael J.; Pham, Hoang N.; Plachetka, Annette; Qin, Bo; Schwartz, Yuri B.; Shoresh, Noam; Stempor, Przemyslaw; Vielle, Anne; Wang, Chengyang; Whittle, Christina M.; Xue, Huiling; Kingston, Robert E.; Kim, Ju Han; Bernstein, Bradley E.; Dernburg, Abby F.; Pirrotta, Vincenzo; Kuroda, Mitzi I.; Noble, William S.; Tullius, Thomas D.; Kellis, Manolis; MacAlpine, David M.; Strome, Susan; Elgin, Sarah C R; Liu, Xiaole Shirley; Lieb, Jason D.; Ahringer, Julie; Karpen, Gary H.; Park, Peter J.

In: Nature, Vol. 512, No. 7515, 28.08.2014, p. 449-452.

Research output: Contribution to journalArticle

Ho, JWK, Jung, YL, Liu, T, Alver, BH, Lee, S, Ikegami, K, Sohn, KA, Minoda, A, Tolstorukov, MY, Appert, A, Parker, SCJ, Gu, T, Kundaje, A, Riddle, NC, Bishop, E, Egelhofer, TA, Hu, SES, Alekseyenko, AA, Rechtsteiner, A, Asker, D, Belsky, JA, Bowman, SK, Chen, QB, Chen, RAJ, Day, DS, Dong, Y, Dose, AC, Duan, X, Epstein, CB, Ercan, S, Feingold, EA, Ferrari, F, Garrigues, JM, Gehlenborg, N, Good, PJ, Haseley, P, He, D, Herrmann, M, Hoffman, MM, Jeffers, TE, Kharchenko, PV, Kolasinska-Zwierz, P, Kotwaliwale, CV, Kumar, N, Langley, SA, Larschan, EN, Latorre, I, Libbrecht, MW, Lin, X, Park, R, Pazin, MJ, Pham, HN, Plachetka, A, Qin, B, Schwartz, YB, Shoresh, N, Stempor, P, Vielle, A, Wang, C, Whittle, CM, Xue, H, Kingston, RE, Kim, JH, Bernstein, BE, Dernburg, AF, Pirrotta, V, Kuroda, MI, Noble, WS, Tullius, TD, Kellis, M, MacAlpine, DM, Strome, S, Elgin, SCR, Liu, XS, Lieb, JD, Ahringer, J, Karpen, GH & Park, PJ 2014, 'Comparative analysis of metazoan chromatin organization', Nature, vol. 512, no. 7515, pp. 449-452. https://doi.org/10.1038/nature13415
Ho JWK, Jung YL, Liu T, Alver BH, Lee S, Ikegami K et al. Comparative analysis of metazoan chromatin organization. Nature. 2014 Aug 28;512(7515):449-452. https://doi.org/10.1038/nature13415
Ho, Joshua W K ; Jung, Youngsook L. ; Liu, Tao ; Alver, Burak H. ; Lee, Soohyun ; Ikegami, Kohta ; Sohn, Kyung Ah ; Minoda, Aki ; Tolstorukov, Michael Y. ; Appert, Alex ; Parker, Stephen C J ; Gu, Tingting ; Kundaje, Anshul ; Riddle, Nicole C. ; Bishop, Eric ; Egelhofer, Thea A. ; Hu, Sheng'En Shawn ; Alekseyenko, Artyom A. ; Rechtsteiner, Andreas ; Asker, Dalal ; Belsky, Jason A. ; Bowman, Sarah K. ; Chen, Q. Brent ; Chen, Ron A J ; Day, Daniel S. ; Dong, Yan ; Dose, Andrea C. ; Duan, Xikun ; Epstein, Charles B. ; Ercan, Sevinc ; Feingold, Elise A. ; Ferrari, Francesco ; Garrigues, Jacob M. ; Gehlenborg, Nils ; Good, Peter J. ; Haseley, Psalm ; He, Daniel ; Herrmann, Moritz ; Hoffman, Michael M. ; Jeffers, Tess E. ; Kharchenko, Peter V. ; Kolasinska-Zwierz, Paulina ; Kotwaliwale, Chitra V. ; Kumar, Nischay ; Langley, Sasha A. ; Larschan, Erica N. ; Latorre, Isabel ; Libbrecht, Maxwell W. ; Lin, Xueqiu ; Park, Richard ; Pazin, Michael J. ; Pham, Hoang N. ; Plachetka, Annette ; Qin, Bo ; Schwartz, Yuri B. ; Shoresh, Noam ; Stempor, Przemyslaw ; Vielle, Anne ; Wang, Chengyang ; Whittle, Christina M. ; Xue, Huiling ; Kingston, Robert E. ; Kim, Ju Han ; Bernstein, Bradley E. ; Dernburg, Abby F. ; Pirrotta, Vincenzo ; Kuroda, Mitzi I. ; Noble, William S. ; Tullius, Thomas D. ; Kellis, Manolis ; MacAlpine, David M. ; Strome, Susan ; Elgin, Sarah C R ; Liu, Xiaole Shirley ; Lieb, Jason D. ; Ahringer, Julie ; Karpen, Gary H. ; Park, Peter J. / Comparative analysis of metazoan chromatin organization. In: Nature. 2014 ; Vol. 512, No. 7515. pp. 449-452.
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T1 - Comparative analysis of metazoan chromatin organization

AU - Ho, Joshua W K

AU - Jung, Youngsook L.

AU - Liu, Tao

AU - Alver, Burak H.

AU - Lee, Soohyun

AU - Ikegami, Kohta

AU - Sohn, Kyung Ah

AU - Minoda, Aki

AU - Tolstorukov, Michael Y.

AU - Appert, Alex

AU - Parker, Stephen C J

AU - Gu, Tingting

AU - Kundaje, Anshul

AU - Riddle, Nicole C.

AU - Bishop, Eric

AU - Egelhofer, Thea A.

AU - Hu, Sheng'En Shawn

AU - Alekseyenko, Artyom A.

AU - Rechtsteiner, Andreas

AU - Asker, Dalal

AU - Belsky, Jason A.

AU - Bowman, Sarah K.

AU - Chen, Q. Brent

AU - Chen, Ron A J

AU - Day, Daniel S.

AU - Dong, Yan

AU - Dose, Andrea C.

AU - Duan, Xikun

AU - Epstein, Charles B.

AU - Ercan, Sevinc

AU - Feingold, Elise A.

AU - Ferrari, Francesco

AU - Garrigues, Jacob M.

AU - Gehlenborg, Nils

AU - Good, Peter J.

AU - Haseley, Psalm

AU - He, Daniel

AU - Herrmann, Moritz

AU - Hoffman, Michael M.

AU - Jeffers, Tess E.

AU - Kharchenko, Peter V.

AU - Kolasinska-Zwierz, Paulina

AU - Kotwaliwale, Chitra V.

AU - Kumar, Nischay

AU - Langley, Sasha A.

AU - Larschan, Erica N.

AU - Latorre, Isabel

AU - Libbrecht, Maxwell W.

AU - Lin, Xueqiu

AU - Park, Richard

AU - Pazin, Michael J.

AU - Pham, Hoang N.

AU - Plachetka, Annette

AU - Qin, Bo

AU - Schwartz, Yuri B.

AU - Shoresh, Noam

AU - Stempor, Przemyslaw

AU - Vielle, Anne

AU - Wang, Chengyang

AU - Whittle, Christina M.

AU - Xue, Huiling

AU - Kingston, Robert E.

AU - Kim, Ju Han

AU - Bernstein, Bradley E.

AU - Dernburg, Abby F.

AU - Pirrotta, Vincenzo

AU - Kuroda, Mitzi I.

AU - Noble, William S.

AU - Tullius, Thomas D.

AU - Kellis, Manolis

AU - MacAlpine, David M.

AU - Strome, Susan

AU - Elgin, Sarah C R

AU - Liu, Xiaole Shirley

AU - Lieb, Jason D.

AU - Ahringer, Julie

AU - Karpen, Gary H.

AU - Park, Peter J.

PY - 2014/8/28

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AB - Genome function is dynamically regulated in part by chromatin, which consists of the histones, non-histone proteins and RNA molecules that package DNA. Studies in Caenorhabditis elegans and Drosophila melanogaster have contributed substantially to our understanding of molecular mechanisms of genome function in humans, and have revealed conservation of chromatin components and mechanisms. Nevertheless, the three organisms have markedly different genome sizes, chromosome architecture and gene organization. On human and fly chromosomes, for example, pericentric heterochromatin flanks single centromeres, whereas worm chromosomes have dispersed heterochromatin-like regions enriched in the distal chromosomal 'arms', and centromeres distributed along their lengths. To systematically investigate chromatin organization and associated gene regulation across species, we generated and analysed a large collection of genome-wide chromatin data sets from cell lines and developmental stages in worm, fly and human. Here we present over 800 new data sets from our ENCODE and modENCODE consortia, bringing the total to over 1,400. Comparison of combinatorial patterns of histone modifications, nuclear lamina-associated domains, organization of large-scale topological domains, chromatin environment at promoters and enhancers, nucleosome positioning, and DNA replication patterns reveals many conserved features of chromatin organization among the three organisms. We also find notable differences in the composition and locations of repressive chromatin. These data sets and analyses provide a rich resource for comparative and species-specific investigations of chromatin composition, organization and function.

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