ArticlebioRxiv : the preprint server for biology2024
An integrated view of the structure and function of the human 4D nucleome.
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91 authors.
4D Nucleome Consortium
Job DekkerDepartment of Systems Biology, University of Massachusetts Chan Medical School, Worcester, MA 01605, USA.ORCID 0000-0001-5631-0698
Betul Akgol OksuzDepartment of Systems Biology, University of Massachusetts Chan Medical School, Worcester, MA 01605, USA.
Yang ZhangRay and Stephanie Lane Computational Biology Department, School of Computer Science, Carnegie Mellon University.
Ye WangDepartment of Microbiology, Immunology, and Molecular Genetics; Institute for Quantitative and Computational Biosciences, University of California Los Angeles, Los Angeles, CA, USA.
Miriam K MinskDepartment of Genetics, Department of Bioengineering, Epigenetics Institute, University of Pennsylvania, Philadelphia, PA, USA.
Shuzhen KuangGladstone Institutes, San Francisco, CA 94158.
Liyan YangDepartment of Systems Biology, University of Massachusetts Chan Medical School, Worcester, MA 01605, USA.
Johan H GibcusDepartment of Systems Biology, University of Massachusetts Chan Medical School, Worcester, MA 01605, USA.
Nils KrietensteinNovo Nordisk Foundation Center for Protein Research, University of Copenhagen.
Oliver J RandoDepartment of Biochemistry and Molecular Biotechnology, University of Massachusetts Chan Medical School, Worcester, Massachusetts 01605, USA.
Jie XuDepartment of Biochemistry and Molecular Genetics, Feinberg School of Medicine Northwestern University, Chicago, Illinois, USA.
Derek H JanssensBasic Sciences Division, Fred Hutchinson Cancer Center, Seattle, WA, USA.
Steven HenikoffBasic Sciences Division, Fred Hutchinson Cancer Center, Seattle, WA, USA.
Alexander KukalevMax-Delbrück-Center for Molecular Medicine in the Helmholtz Association (MDC), Berlin Institute for Medical Systems Biology (BIMSB), Epigenetic Regulation and Chromatin Architecture Group, 10115 Berlin, Germany.
Andréa WilleminMax-Delbrück-Center for Molecular Medicine in the Helmholtz Association (MDC), Berlin Institute for Medical Systems Biology (BIMSB), Epigenetic Regulation and Chromatin Architecture Group, 10115 Berlin, Germany.
Warren Winick-NgMax-Delbrück-Center for Molecular Medicine in the Helmholtz Association (MDC), Berlin Institute for Medical Systems Biology (BIMSB), Epigenetic Regulation and Chromatin Architecture Group, 10115 Berlin, Germany.
Rieke KempferMax-Delbrück-Center for Molecular Medicine in the Helmholtz Association (MDC), Berlin Institute for Medical Systems Biology (BIMSB), Epigenetic Regulation and Chromatin Architecture Group, 10115 Berlin, Germany.
Ana PomboMax-Delbrück-Center for Molecular Medicine in the Helmholtz Association (MDC), Berlin Institute for Medical Systems Biology (BIMSB), Epigenetic Regulation and Chromatin Architecture Group, 10115 Berlin, Germany.ORCID 0000-0002-7493-6288
Miao YuUniversity of California, San Diego School of Medicine, Department of Cellular and Molecular Medicine, La Jolla, CA, USA.
Pradeep KumarDepartment of Cell and Developmental Biology, University of Illinois at Urbana-Champaign, Urbana, IL, USA.
Liguo ZhangDepartment of Cell and Developmental Biology, University of Illinois at Urbana-Champaign, Urbana, IL, USA.
Andrew S BelmontDepartment of Cell and Developmental Biology, University of Illinois at Urbana-Champaign, Urbana, IL, USA.
Takayo SasakiSan Diego Biomedical Research Institute, San Diego, CA, USA.
Tom van SchaikDivision of Gene Regulation, Netherlands Cancer Institute, Amsterdam, the Netherlands.
Laura BruecknerDivision of Gene Regulation, Netherlands Cancer Institute, Amsterdam, the Netherlands.
Daan Peric-HupkesDivision of Gene Regulation, Netherlands Cancer Institute, Amsterdam, the Netherlands.
Bas van SteenselDivision of Gene Regulation, Netherlands Cancer Institute, Amsterdam, the Netherlands.ORCID 0000-0002-0284-0404
Ping WangDepartment of Biochemistry and Molecular Genetics, Feinberg School of Medicine Northwestern University, Chicago, Illinois, USA.
Haoxi ChaiLife Sciences Institute, Zhejiang University, Hangzhou, Zhejiang Province, 310058, P.R. China.
Minji KimDepartment of Computational Medicine and Bioinformatics, University of Michigan, Ann Arbor, MI 48109, USA.ORCID 0000-0002-7282-8224
Yijun RuanLife Sciences Institute, Zhejiang University, Hangzhou, Zhejiang Province, 310058, P.R. China.
Ran ZhangDepartment of Genome Sciences, University of Washington, Seattle, WA 98195.
Sofia A QuinodozDivision of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA 91125, USA.
Prashant BhatDivision of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA 91125, USA.
Mitchell GuttmanDivision of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA 91125, USA.
Wenxin ZhaoShu Chien-Gene Lay Department of Bioengineering, University of California San Diego, La Jolla, CA, USA.
Shu ChienShu Chien-Gene Lay Department of Bioengineering, University of California San Diego, La Jolla, CA, USA.
Yuan LiuShu Chien-Gene Lay Department of Bioengineering, University of California San Diego, La Jolla, CA, USA.
Sergey V VenevDepartment of Systems Biology, University of Massachusetts Chan Medical School, Worcester, MA 01605, USA.
Dariusz PlewczynskiLaboratory of Bioinformatics and Computational Genomics, Faculty of Mathematics and Information Science, Warsaw University of Technology ul. Koszykowa 75, 00-662 Warsaw, Poland.ORCID 0000-0002-3840-7610
Ibai Irastorza AzcarateMax-Delbrück-Center for Molecular Medicine in the Helmholtz Association (MDC), Berlin Institute for Medical Systems Biology (BIMSB), Epigenetic Regulation and Chromatin Architecture Group, 10115 Berlin, Germany.
Dominik SzabóMax-Delbrück-Center for Molecular Medicine in the Helmholtz Association (MDC), Berlin Institute for Medical Systems Biology (BIMSB), Epigenetic Regulation and Chromatin Architecture Group, 10115 Berlin, Germany.
Christoph J ThiemeMax-Delbrück-Center for Molecular Medicine in the Helmholtz Association (MDC), Berlin Institute for Medical Systems Biology (BIMSB), Epigenetic Regulation and Chromatin Architecture Group, 10115 Berlin, Germany.
Teresa SzczepińskaMax-Delbrück-Center for Molecular Medicine in the Helmholtz Association (MDC), Berlin Institute for Medical Systems Biology (BIMSB), Epigenetic Regulation and Chromatin Architecture Group, 10115 Berlin, Germany.
Mateusz ChilińskiLaboratory of Bioinformatics and Computational Genomics, Faculty of Mathematics and Information Science, Warsaw University of Technology ul. Koszykowa 75, 00-662 Warsaw, Poland.
Kaustav SenguptaLaboratory of Bioinformatics and Computational Genomics, Faculty of Mathematics and Information Science, Warsaw University of Technology ul. Koszykowa 75, 00-662 Warsaw, Poland.
Mattia ConteDepartment of Physics, University of Naples "Federico II", Naples, Italy; INFN, Naples, Italy.
Andrea EspositoDepartment of Physics, University of Naples "Federico II", Naples, Italy; INFN, Naples, Italy.
Alex AbrahamDepartment of Physics, University of Naples "Federico II", Naples, Italy; INFN, Naples, Italy.
Ruochi ZhangRay and Stephanie Lane Computational Biology Department, School of Computer Science, Carnegie Mellon University.
Yuchuan WangRay and Stephanie Lane Computational Biology Department, School of Computer Science, Carnegie Mellon University.
Xingzhao WenProgram in Bioinformatics and Systems Biology, University of California San Diego, La Jolla, CA, USA.
Qiuyang WuShu Chien-Gene Lay Department of Bioengineering, University of California San Diego, La Jolla, CA, USA.
Yang YangRay and Stephanie Lane Computational Biology Department, School of Computer Science, Carnegie Mellon University.
Jie LiuDepartment of Computational Medicine and Bioinformatics, University of Michigan, Ann Arbor, MI 48109, USA.
Lorenzo BoninsegnaDepartment of Microbiology, Immunology, and Molecular Genetics; Institute for Quantitative and Computational Biosciences, University of California Los Angeles, Los Angeles, CA, USA.
Asli YildirimDepartment of Microbiology, Immunology, and Molecular Genetics; Institute for Quantitative and Computational Biosciences, University of California Los Angeles, Los Angeles, CA, USA.
Yuxiang ZhanDepartment of Microbiology, Immunology, and Molecular Genetics; Institute for Quantitative and Computational Biosciences, University of California Los Angeles, Los Angeles, CA, USA.
Andrea Maria ChiarielloDepartment of Physics, University of Naples "Federico II", Naples, Italy; INFN, Naples, Italy.
Simona BiancoDepartment of Physics, University of Naples "Federico II", Naples, Italy; INFN, Naples, Italy.
Lindsay LeeDepartment of Quantitative Health Sciences, Lerner Research Institute, Cleveland Clinic Foundation, Cleveland, OH, USA.
Ming HuDepartment of Quantitative Health Sciences, Lerner Research Institute, Cleveland Clinic Foundation, Cleveland, OH, USA.
Yun LiDepartment of Biostatistics, Department of Genetics, University of North Carolina, Chapel Hill, NC 27599, USA.ORCID 0000-0002-9275-4189
R Jordan BarnettDepartment of Genetics, Department of Bioengineering, Epigenetics Institute, University of Pennsylvania, Philadelphia, PA, USA.
Ashley L CookDepartment of Genetics, Department of Bioengineering, Epigenetics Institute, University of Pennsylvania, Philadelphia, PA, USA.
Daniel J EmersonDepartment of Genetics, Department of Bioengineering, Epigenetics Institute, University of Pennsylvania, Philadelphia, PA, USA.
Claire MarchalIn silichrom Ltd, Newbury, UK.
Peiyao ZhaoSan Diego Biomedical Research Institute, San Diego, CA, USA.
Peter ParkDepartment of Biomedical Informatics, Harvard Medical School, Boston, MA, 02115.
Burak H AlverDepartment of Biomedical Informatics, Harvard Medical School, Boston, MA, 02115.
Andrew SchroederDepartment of Biomedical Informatics, Harvard Medical School, Boston, MA, 02115.
Rahi NavelkarDepartment of Biomedical Informatics, Harvard Medical School, Boston, MA, 02115.
Clara BakkerDepartment of Biomedical Informatics, Harvard Medical School, Boston, MA, 02115.
William RonchettiDepartment of Biomedical Informatics, Harvard Medical School, Boston, MA, 02115.
Shannon EhmsenDepartment of Biomedical Informatics, Harvard Medical School, Boston, MA, 02115.
Alexander VeitDepartment of Biomedical Informatics, Harvard Medical School, Boston, MA, 02115.
Nils GehlenborgDepartment of Biomedical Informatics, Harvard Medical School, Boston, MA, 02115.
Ting WangDepartment of Genetics, Center for Genome Sciences and Systems Biology, Washington University School of Medicine, St. Louis, MO, USA.
Daofeng LiDepartment of Genetics, Center for Genome Sciences and Systems Biology, Washington University School of Medicine, St. Louis, MO, USA.ORCID 0000-0001-7492-3703
Xiaotao WangDepartment of Biochemistry and Molecular Genetics, Feinberg School of Medicine Northwestern University, Chicago, Illinois, USA.
Mario NicodemiDepartment of Physics, University of Naples "Federico II", Naples, Italy; INFN, Naples, Italy.
Bing RenUniversity of California, San Diego School of Medicine, Department of Cellular and Molecular Medicine, La Jolla, CA, USA.
Sheng ZhongShu Chien-Gene Lay Department of Bioengineering, University of California San Diego, La Jolla, CA, USA.
Jennifer E Phillips-CreminsDepartment of Genetics, Department of Bioengineering, Epigenetics Institute, University of Pennsylvania, Philadelphia, PA, USA.
David M GilbertSan Diego Biomedical Research Institute, San Diego, CA, USA.ORCID 0000-0001-8087-9737
Katherine S PollardGladstone Institutes, San Francisco, CA 94158.
Frank AlberDepartment of Microbiology, Immunology, and Molecular Genetics; Institute for Quantitative and Computational Biosciences, University of California Los Angeles, Los Angeles, CA, USA.
Jian MaRay and Stephanie Lane Computational Biology Department, School of Computer Science, Carnegie Mellon University.ORCID 0000-0002-4202-5834
William S NobleDepartment of Genome Sciences, University of Washington, Seattle, WA 98195.
Feng YueDepartment of Biochemistry and Molecular Genetics, Feinberg School of Medicine Northwestern University, Chicago, Illinois, USA.
Funding
UCLA-Caltech Medical Scientist Training ProgramT32GM008042 · NIGMS · UNIVERSITY OF CALIFORNIA LOS ANGELES · PI AJIJOLA, OLUJIMI A, DAWSON, DAVID WAYNE · 1985 to 2023
$29.9M4D Nucleome Network Data Coordination and Integration CenterU01CA200059 · NCI · HARVARD MEDICAL SCHOOL · PI PARK, PETER J · 2015 to 2024
$24.4MThe second phase of NIH Common Fund 4D Nucleome Network Organizational HubU01CA200147 · NCI · UNIVERSITY OF CALIFORNIA, SAN DIEGO · PI ZHONG, SHENG · 2015 to 2024
$22.0MCenter for 3D Structure and Physics of the GenomeU54DK107980 · NIDDK · UNIV OF MASSACHUSETTS MED SCH WORCESTER · PI DEKKER, JOB, MIRNY, LEONID A · 2015 to 2019
$14.9MUniversity of Washington Center for Nuclear Organization and FunctionU54DK107979 · NIDDK · UNIVERSITY OF WASHINGTON · PI NOBLE, WILLIAM STAFFORD · 2015 to 2019
$11.8MCenter for 3D Structure and Physics of the GenomeUM1HG011536 · NHGRI · UNIV OF MASSACHUSETTS MED SCH WORCESTER · PI DEKKER, JOB, MIRNY, LEONID A · 2020 to 2024
$11.8MMultiscale Analyses of 4D Nucleome Structure and Function by Comprehensive Multimodal Data IntegrationUM1HG011593 · NHGRI · CARNEGIE-MELLON UNIVERSITY · PI ALBER, FRANK, BELMONT, ANDREW STEVEN · 2020 to 2024
$10.4MSan Diego Center for 4D Nucleome ResearchU54DK107977 · NIDDK · LUDWIG INSTITUTE FOR CANCER RES LTD · PI MURRE, CORNELIS, REN, BING · 2015 to 2019
$9.4MMapping Technology DevelopmentU54DK107965 · NIDDK · UNIVERSITY OF ILLINOIS AT URBANA-CHAMPAIGN · PI BELMONT, ANDREW STEVEN · 2015 to 2019
$8.6MCenter for Integrated Multi-modal and Multi-scale Nucleome ResearchUM1HG011585 · NHGRI · UNIVERSITY OF CALIFORNIA, SAN DIEGO · PI DULAC, CATHERINE, LEIN, ED · 2020 to 2024
$6.7MDynamics of chromosome organization and chromatin states in single cellsU01DK127420 · NIDDK · CALIFORNIA INSTITUTE OF TECHNOLOGY · PI CAI, LONG, ELOWITZ, MICHAEL B · 2020 to 2024
$5.7MEngineering and Imaging 3D genome structure-function dynamics across time scalesU01DK127405 · NIDDK · UNIVERSITY OF PENNSYLVANIA · PI BLOBEL, GERD A, PHILLIPS-CREMINS, JENNIFER ELIZABETH · 2020 to 2024
$5.7MNCI NIH HHS U01 CA200059NCI NIH HHS U01 CA200060NCI NIH HHS U01 CA200147NHGRI NIH HHS UM1 HG011536NHGRI NIH HHS UM1 HG011585NHGRI NIH HHS UM1 HG011593NHLBI NIH HHS U01 HL129998NHLBI NIH HHS U01 HL130007NHLBI NIH HHS U01 HL157989NIDA NIH HHS U01 DA040612NIDA NIH HHS U01 DA052715NIDA NIH HHS U01 DA052769NIDDK NIH HHS U01 DK127405NIDDK NIH HHS U01 DK127420NIDDK NIH HHS U54 DK107965NIDDK NIH HHS U54 DK107967NIDDK NIH HHS U54 DK107977NIDDK NIH HHS U54 DK107979NIDDK NIH HHS U54 DK107980NIDDK NIH HHS U54 DK107981NIGMS NIH HHS T32 GM008042
Abstract
The dynamic three-dimensional (3D) organization of the human genome (the "4D Nucleome") is closely linked to genome function. Here, we integrate a wide variety of genomic data generated by the 4D Nucleome Project to provide a detailed view of human 3D genome organization in widely used embryonic stem cells (H1-hESCs) and immortalized fibroblasts (HFFc6). We provide extensive benchmarking of 3D genome mapping assays and integrate these diverse datasets to annotate spatial genomic features across scales. The data reveal a rich complexity of chromatin domains and their sub-nuclear positions, and over one hundred thousand structural loops and promoter-enhancer interactions. We developed 3D models of population-based and individual cell-to-cell variation in genome structure, establishing connections between chromosome folding, nuclear organization, chromatin looping, gene transcription, and DNA replication. We demonstrate the use of computational methods to predict genome folding from DNA sequence, uncovering potential effects of genetic variants on genome structure and function. Together, this comprehensive analysis contributes insights into human genome organization and enhances our understanding of connections between the regulation of genome function and 3D genome organization in general.
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