Walking along chromosomes with super-resolution imaging, contact maps, and integrative modeling

Guy Nir; Irene Farabella; Cynthia Pérez Estrada; Carl G. Ebeling; Brian J. Beliveau; Hiroshi M. Sasaki; Soun H. Lee; Son C. Nguyen; Ruth B. McCole; Shyamtanu Chattoraj; Jelena Erceg; Jumana AlHaj Abed; Nuno M.C. Martins; Huy Q. Nguyen; Mohammed A. Hannan; Sheikh Russell; Neva C. Durand; Suhas S.P. Rao; Jocelyn Y. Kishi; Paula Soler-Vila; Michele Di Pierro; José N. Onuchic; Steven P. Callahan; John M. Schreiner; Jeff A. Stuckey; Peng Yin; Erez Lieberman Aiden; Marc A. Marti-Renom; C. Ting Wu

doi:10.1371/journal.pgen.1007872

Walking along chromosomes with super-resolution imaging, contact maps, and integrative modeling

Guy Nir, Irene Farabella, Cynthia Pérez Estrada, Carl G. Ebeling, Brian J. Beliveau, Hiroshi M. Sasaki, Soun H. Lee, Son C. Nguyen, Ruth B. McCole, Shyamtanu Chattoraj, Jelena Erceg, Jumana AlHaj Abed, Nuno M.C. Martins, Huy Q. Nguyen, Mohammed A. Hannan, Sheikh Russell, Neva C. Durand, Suhas S.P. Rao, Jocelyn Y. Kishi, Paula Soler-VilaMichele Di Pierro, José N. Onuchic, Steven P. Callahan, John M. Schreiner, Jeff A. Stuckey, Peng Yin, Erez Lieberman Aiden, Marc A. Marti-Renom, C. Ting Wu

Research output: Contribution to journal › Article › peer-review

171 Scopus citations

Abstract

Chromosome organization is crucial for genome function. Here, we present a method for visualizing chromosomal DNA at super-resolution and then integrating Hi-C data to produce three-dimensional models of chromosome organization. Using the super-resolution microscopy methods of OligoSTORM and OligoDNA-PAINT, we trace 8 megabases of human chromosome 19, visualizing structures ranging in size from a few kilobases to over a megabase. Focusing on chromosomal regions that contribute to compartments, we discover distinct structures that, in spite of considerable variability, can predict whether such regions correspond to active (A-type) or inactive (B-type) compartments. Imaging through the depths of entire nuclei, we capture pairs of homologous regions in diploid cells, obtaining evidence that maternal and paternal homologous regions can be differentially organized. Finally, using restraint-based modeling to integrate imaging and Hi-C data, we implement a method–integrative modeling of genomic regions (IMGR)–to increase the genomic resolution of our traces to 10 kb.

Original language	English (US)
Article number	e1007872
Journal	PLoS genetics
Volume	14
Issue number	12
DOIs	https://doi.org/10.1371/journal.pgen.1007872
State	Published - Dec 2018
Externally published	Yes

ASJC Scopus subject areas

Ecology, Evolution, Behavior and Systematics
Molecular Biology
Genetics
Genetics(clinical)
Cancer Research

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10.1371/journal.pgen.1007872

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Nir, G., Farabella, I., Pérez Estrada, C., Ebeling, C. G., Beliveau, B. J., Sasaki, H. M., Lee, S. H., Nguyen, S. C., McCole, R. B., Chattoraj, S., Erceg, J., AlHaj Abed, J., Martins, N. M. C., Nguyen, H. Q., Hannan, M. A., Russell, S., Durand, N. C., Rao, S. S. P., Kishi, J. Y., ... Wu, C. T. (2018). Walking along chromosomes with super-resolution imaging, contact maps, and integrative modeling. PLoS genetics, 14(12), Article e1007872. https://doi.org/10.1371/journal.pgen.1007872

Nir, G, Farabella, I, Pérez Estrada, C, Ebeling, CG, Beliveau, BJ, Sasaki, HM, Lee, SH, Nguyen, SC, McCole, RB, Chattoraj, S, Erceg, J, AlHaj Abed, J, Martins, NMC, Nguyen, HQ, Hannan, MA, Russell, S, Durand, NC, Rao, SSP, Kishi, JY, Soler-Vila, P, Di Pierro, M, Onuchic, JN, Callahan, SP, Schreiner, JM, Stuckey, JA, Yin, P, Aiden, EL, Marti-Renom, MA & Wu, CT 2018, 'Walking along chromosomes with super-resolution imaging, contact maps, and integrative modeling', PLoS genetics, vol. 14, no. 12, e1007872. https://doi.org/10.1371/journal.pgen.1007872

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title = "Walking along chromosomes with super-resolution imaging, contact maps, and integrative modeling",

abstract = "Chromosome organization is crucial for genome function. Here, we present a method for visualizing chromosomal DNA at super-resolution and then integrating Hi-C data to produce three-dimensional models of chromosome organization. Using the super-resolution microscopy methods of OligoSTORM and OligoDNA-PAINT, we trace 8 megabases of human chromosome 19, visualizing structures ranging in size from a few kilobases to over a megabase. Focusing on chromosomal regions that contribute to compartments, we discover distinct structures that, in spite of considerable variability, can predict whether such regions correspond to active (A-type) or inactive (B-type) compartments. Imaging through the depths of entire nuclei, we capture pairs of homologous regions in diploid cells, obtaining evidence that maternal and paternal homologous regions can be differentially organized. Finally, using restraint-based modeling to integrate imaging and Hi-C data, we implement a method–integrative modeling of genomic regions (IMGR)–to increase the genomic resolution of our traces to 10 kb.",

author = "Guy Nir and Irene Farabella and {P{\'e}rez Estrada}, Cynthia and Ebeling, {Carl G.} and Beliveau, {Brian J.} and Sasaki, {Hiroshi M.} and Lee, {Soun H.} and Nguyen, {Son C.} and McCole, {Ruth B.} and Shyamtanu Chattoraj and Jelena Erceg and {AlHaj Abed}, Jumana and Martins, {Nuno M.C.} and Nguyen, {Huy Q.} and Hannan, {Mohammed A.} and Sheikh Russell and Durand, {Neva C.} and Rao, {Suhas S.P.} and Kishi, {Jocelyn Y.} and Paula Soler-Vila and {Di Pierro}, Michele and Onuchic, {Jos{\'e} N.} and Callahan, {Steven P.} and Schreiner, {John M.} and Stuckey, {Jeff A.} and Peng Yin and Aiden, {Erez Lieberman} and Marti-Renom, {Marc A.} and Wu, {C. Ting}",

note = "Publisher Copyright: {\textcopyright} 2018 Nir et al. http://creativecommons.org/licenses/by/4.0/.",

year = "2018",

month = dec,

doi = "10.1371/journal.pgen.1007872",

language = "English (US)",

volume = "14",

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T1 - Walking along chromosomes with super-resolution imaging, contact maps, and integrative modeling

AU - Nir, Guy

AU - Farabella, Irene

AU - Pérez Estrada, Cynthia

AU - Ebeling, Carl G.

AU - Beliveau, Brian J.

AU - Sasaki, Hiroshi M.

AU - Lee, Soun H.

AU - Nguyen, Son C.

AU - McCole, Ruth B.

AU - Chattoraj, Shyamtanu

AU - Erceg, Jelena

AU - AlHaj Abed, Jumana

AU - Martins, Nuno M.C.

AU - Nguyen, Huy Q.

AU - Hannan, Mohammed A.

AU - Russell, Sheikh

AU - Durand, Neva C.

AU - Rao, Suhas S.P.

AU - Kishi, Jocelyn Y.

AU - Soler-Vila, Paula

AU - Di Pierro, Michele

AU - Onuchic, José N.

AU - Callahan, Steven P.

AU - Schreiner, John M.

AU - Stuckey, Jeff A.

AU - Yin, Peng

AU - Aiden, Erez Lieberman

AU - Marti-Renom, Marc A.

AU - Wu, C. Ting

PY - 2018/12

Y1 - 2018/12

N2 - Chromosome organization is crucial for genome function. Here, we present a method for visualizing chromosomal DNA at super-resolution and then integrating Hi-C data to produce three-dimensional models of chromosome organization. Using the super-resolution microscopy methods of OligoSTORM and OligoDNA-PAINT, we trace 8 megabases of human chromosome 19, visualizing structures ranging in size from a few kilobases to over a megabase. Focusing on chromosomal regions that contribute to compartments, we discover distinct structures that, in spite of considerable variability, can predict whether such regions correspond to active (A-type) or inactive (B-type) compartments. Imaging through the depths of entire nuclei, we capture pairs of homologous regions in diploid cells, obtaining evidence that maternal and paternal homologous regions can be differentially organized. Finally, using restraint-based modeling to integrate imaging and Hi-C data, we implement a method–integrative modeling of genomic regions (IMGR)–to increase the genomic resolution of our traces to 10 kb.

AB - Chromosome organization is crucial for genome function. Here, we present a method for visualizing chromosomal DNA at super-resolution and then integrating Hi-C data to produce three-dimensional models of chromosome organization. Using the super-resolution microscopy methods of OligoSTORM and OligoDNA-PAINT, we trace 8 megabases of human chromosome 19, visualizing structures ranging in size from a few kilobases to over a megabase. Focusing on chromosomal regions that contribute to compartments, we discover distinct structures that, in spite of considerable variability, can predict whether such regions correspond to active (A-type) or inactive (B-type) compartments. Imaging through the depths of entire nuclei, we capture pairs of homologous regions in diploid cells, obtaining evidence that maternal and paternal homologous regions can be differentially organized. Finally, using restraint-based modeling to integrate imaging and Hi-C data, we implement a method–integrative modeling of genomic regions (IMGR)–to increase the genomic resolution of our traces to 10 kb.

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JO - PLoS genetics

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ER -

Walking along chromosomes with super-resolution imaging, contact maps, and integrative modeling

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