Phase separation drives aberrant chromatin looping and cancer development

The development of cancer is intimately associated with genetic abnormalities that target proteins with intrinsically disordered regions (IDRs). In human haematological malignancies, recurrent chromosomal translocation of nucleoporin (NUP98 or NUP214) generates an aberrant chimera that invariably re...

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Published inNature (London) Vol. 595; no. 7868; pp. 591 - 595
Main Authors Ahn, Jeong Hyun, Davis, Eric S., Daugird, Timothy A., Zhao, Shuai, Quiroga, Ivana Yoseli, Uryu, Hidetaka, Li, Jie, Storey, Aaron J., Tsai, Yi-Hsuan, Keeley, Daniel P., Mackintosh, Samuel G., Edmondson, Ricky D., Byrum, Stephanie D., Cai, Ling, Tackett, Alan J., Zheng, Deyou, Legant, Wesley R., Phanstiel, Douglas H., Wang, Gang Greg
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 22.07.2021
Nature Publishing Group
Subjects
14/63
38/15
38/91
631/208/68/2486
631/337/100/101
631/67/1990/283/1897
Abnormalities
Animals
Binding
Cancer
Carcinogenesis
Chimeras
Chromatin
Chromatin - genetics
Chromosome translocations
Development and progression
Ewings sarcoma
Female
Genes
Genetic abnormalities
Genetic aspects
Genetic transformation
Genomes
Glycine
Health aspects
HEK293 Cells
HeLa Cells
Homeobox
Homeodomain Proteins - genetics
Humanities and Social Sciences
Humans
Intrinsically Disordered Proteins - genetics
Leukemia
Liquid phases
Mice
Mice, Inbred BALB C
Molecular structure
multidisciplinary
Mutation
Neoplasms - genetics
Neoplasms - pathology
Nuclear Pore Complex Proteins - genetics
Occupancy
Oncogene Proteins, Fusion - genetics
Phase separation
Phenylalanine
Proteins
Proto-oncogenes
Science
Science (multidisciplinary)
Transcription activation
Transcription factors
Transcription Factors - genetics
Transcriptional Activation
Translocation
Translocation, Genetic
Tumorigenesis
United States
Online AccessGet full text

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Abstract The development of cancer is intimately associated with genetic abnormalities that target proteins with intrinsically disordered regions (IDRs). In human haematological malignancies, recurrent chromosomal translocation of nucleoporin (NUP98 or NUP214) generates an aberrant chimera that invariably retains the nucleoporin IDR—tandemly dispersed repeats of phenylalanine and glycine residues 1 , 2 . However, how unstructured IDRs contribute to oncogenesis remains unclear. Here we show that IDRs contained within NUP98–HOXA9, a homeodomain-containing transcription factor chimera recurrently detected in leukaemias 1 , 2 , are essential for establishing liquid–liquid phase separation (LLPS) puncta of chimera and for inducing leukaemic transformation. Notably, LLPS of NUP98–HOXA9 not only promotes chromatin occupancy of chimera transcription factors, but also is required for the formation of a broad ‘super-enhancer’-like binding pattern typically seen at leukaemogenic genes, which potentiates transcriptional activation. An artificial HOX chimera, created by replacing the phenylalanine and glycine repeats of NUP98 with an unrelated LLPS-forming IDR of the FUS protein 3 , 4 , had similar enhancing effects on the genome-wide binding and target gene activation of the chimera. Deeply sequenced Hi-C revealed that phase-separated NUP98–HOXA9 induces CTCF-independent chromatin loops that are enriched at proto-oncogenes. Together, this report describes a proof-of-principle example in which cancer acquires mutation to establish oncogenic transcription factor condensates via phase separation, which simultaneously enhances their genomic targeting and induces organization of aberrant three-dimensional chromatin structure during tumourous transformation. As LLPS-competent molecules are frequently implicated in diseases 1 , 2 , 4 – 7 , this mechanism can potentially be generalized to many malignant and pathological settings. The NUP98–HOXA9 oncogenic fusion protein found in leukaemia undergoes phase separation in the nucleus, which helps to promote activation of leukaemic genes and to establish aberrant chromatin looping.
AbstractList The development of cancer is intimately associated with genetic abnormalities that target proteins with intrinsically disordered regions (IDRs). In human haematological malignancies, recurrent chromosomal translocation of nucleoporin (NUP98 or NUP214) generates an aberrant chimera that invariably retains the nucleoporin IDR--tandemly dispersed repeats of phenylalanine and glycine residues.sup.1,2. However, how unstructured IDRs contribute to oncogenesis remains unclear. Here we show that IDRs contained within NUP98-HOXA9, a homeodomain-containing transcription factor chimera recurrently detected in leukaemias.sup.1,2, are essential for establishing liquid-liquid phase separation (LLPS) puncta of chimera and for inducing leukaemic transformation. Notably, LLPS of NUP98-HOXA9 not only promotes chromatin occupancy of chimera transcription factors, but also is required for the formation of a broad 'super-enhancer'-like binding pattern typically seen at leukaemogenic genes, which potentiates transcriptional activation. An artificial HOX chimera, created by replacing the phenylalanine and glycine repeats of NUP98 with an unrelated LLPS-forming IDR of the FUS protein.sup.3,4, had similar enhancing effects on the genome-wide binding and target gene activation of the chimera. Deeply sequenced Hi-C revealed that phase-separated NUP98-HOXA9 induces CTCF-independent chromatin loops that are enriched at proto-oncogenes. Together, this report describes a proof-of-principle example in which cancer acquires mutation to establish oncogenic transcription factor condensates via phase separation, which simultaneously enhances their genomic targeting and induces organization of aberrant three-dimensional chromatin structure during tumourous transformation. As LLPS-competent molecules are frequently implicated in diseases.sup.1,2,4-7, this mechanism can potentially be generalized to many malignant and pathological settings.
The development of cancer is intimately associated with genetic abnormalities that target proteins with intrinsically disordered regions (IDRs). In human hematological malignancies, recurrent chromosomal translocation of nucleoporin (NUP98 or NUP214) generates an aberrant chimera that invariably retains the nucleoporin’s IDR, tandemly dispersed phenylalanine-and-glycine (FG) repeats 1 , 2 . However, it remains elusive how unstructured IDRs contribute to oncogenesis. We show that IDR harbored within NUP98-HOXA9, a homeodomain-containing transcription factor (TF) chimera recurrently detected in leukemias 1 , 2 , is essential for establishing liquid-liquid phase separation (LLPS) puncta of chimera and for inducing leukemic transformation. Notably, LLPS of NUP98-HOXA9 not only promotes chromatin occupancy of chimera TFs but is also required for formation of a broad, ‘super-enhancer’-like binding pattern, typically seen at a battery of leukemogenic genes, potentiating their transcriptional activation. An artificial HOX chimera, created by replacing NUP98’s FG repeats with an unrelated LLPS-forming IDR of FUS 3 , 4 , had similar enhancement effects on chimera’s genome-wide binding and target gene activation. Chromosome conformation capture techniques such as Hi-C mapping further demonstrated that phase-separated NUP98-HOXA9 induces CTCF-independent chromatin looping enriched at proto-oncogenes. Together, this report describes a proof-of-principle example wherein cancer acquires mutation to establish oncogenic TF condensates via phase separation, which simultaneously enhances their genomic targeting and induces organization of aberrant three-dimensional chromatin structure during tumorous transformation. As LLPS-competent molecules are frequently implicated in diseases 1 , 2 , 4 – 7 , this mechanism can potentially be generalized to many malignant and pathological settings.
The development of cancer is intimately associated with genetic abnormalities that target proteins with intrinsically disordered regions (IDRs). In human haematological malignancies, recurrent chromosomal translocation of nucleoporin (NUP98 or NUP214) generates an aberrant chimera that invariably retains the nucleoporin IDR—tandemly dispersed repeats of phenylalanine and glycine residues 1 , 2 . However, how unstructured IDRs contribute to oncogenesis remains unclear. Here we show that IDRs contained within NUP98–HOXA9, a homeodomain-containing transcription factor chimera recurrently detected in leukaemias 1 , 2 , are essential for establishing liquid–liquid phase separation (LLPS) puncta of chimera and for inducing leukaemic transformation. Notably, LLPS of NUP98–HOXA9 not only promotes chromatin occupancy of chimera transcription factors, but also is required for the formation of a broad ‘super-enhancer’-like binding pattern typically seen at leukaemogenic genes, which potentiates transcriptional activation. An artificial HOX chimera, created by replacing the phenylalanine and glycine repeats of NUP98 with an unrelated LLPS-forming IDR of the FUS protein 3 , 4 , had similar enhancing effects on the genome-wide binding and target gene activation of the chimera. Deeply sequenced Hi-C revealed that phase-separated NUP98–HOXA9 induces CTCF-independent chromatin loops that are enriched at proto-oncogenes. Together, this report describes a proof-of-principle example in which cancer acquires mutation to establish oncogenic transcription factor condensates via phase separation, which simultaneously enhances their genomic targeting and induces organization of aberrant three-dimensional chromatin structure during tumourous transformation. As LLPS-competent molecules are frequently implicated in diseases 1 , 2 , 4 – 7 , this mechanism can potentially be generalized to many malignant and pathological settings. The NUP98–HOXA9 oncogenic fusion protein found in leukaemia undergoes phase separation in the nucleus, which helps to promote activation of leukaemic genes and to establish aberrant chromatin looping.
The development of cancer is intimately associated with genetic abnormalities that target proteins with intrinsically disordered regions (IDRs). In human haematological malignancies, recurrent chromosomal translocation of nucleoporin (NUP98 or NUP214) generates an aberrant chimera that invariably retains the nucleoporin IDR-tandemly dispersed repeats of phenylalanine and glycine residues . However, how unstructured IDRs contribute to oncogenesis remains unclear. Here we show that IDRs contained within NUP98-HOXA9, a homeodomain-containing transcription factor chimera recurrently detected in leukaemias , are essential for establishing liquid-liquid phase separation (LLPS) puncta of chimera and for inducing leukaemic transformation. Notably, LLPS of NUP98-HOXA9 not only promotes chromatin occupancy of chimera transcription factors, but also is required for the formation of a broad 'super-enhancer'-like binding pattern typically seen at leukaemogenic genes, which potentiates transcriptional activation. An artificial HOX chimera, created by replacing the phenylalanine and glycine repeats of NUP98 with an unrelated LLPS-forming IDR of the FUS protein , had similar enhancing effects on the genome-wide binding and target gene activation of the chimera. Deeply sequenced Hi-C revealed that phase-separated NUP98-HOXA9 induces CTCF-independent chromatin loops that are enriched at proto-oncogenes. Together, this report describes a proof-of-principle example in which cancer acquires mutation to establish oncogenic transcription factor condensates via phase separation, which simultaneously enhances their genomic targeting and induces organization of aberrant three-dimensional chromatin structure during tumourous transformation. As LLPS-competent molecules are frequently implicated in diseases , this mechanism can potentially be generalized to many malignant and pathological settings.
The development of cancer is intimately associated with genetic abnormalities that target proteins with intrinsically disordered regions (IDRs). In human haematological malignancies, recurrent chromosomal translocation of nucleoporin (NUP98 or NUP214) generates an aberrant chimera that invariably retains the nucleoporin IDR--tandemly dispersed repeats of phenylalanine and glycine residues.sup.1,2. However, how unstructured IDRs contribute to oncogenesis remains unclear. Here we show that IDRs contained within NUP98-HOXA9, a homeodomain-containing transcription factor chimera recurrently detected in leukaemias.sup.1,2, are essential for establishing liquid-liquid phase separation (LLPS) puncta of chimera and for inducing leukaemic transformation. Notably, LLPS of NUP98-HOXA9 not only promotes chromatin occupancy of chimera transcription factors, but also is required for the formation of a broad 'super-enhancer'-like binding pattern typically seen at leukaemogenic genes, which potentiates transcriptional activation. An artificial HOX chimera, created by replacing the phenylalanine and glycine repeats of NUP98 with an unrelated LLPS-forming IDR of the FUS protein.sup.3,4, had similar enhancing effects on the genome-wide binding and target gene activation of the chimera. Deeply sequenced Hi-C revealed that phase-separated NUP98-HOXA9 induces CTCF-independent chromatin loops that are enriched at proto-oncogenes. Together, this report describes a proof-of-principle example in which cancer acquires mutation to establish oncogenic transcription factor condensates via phase separation, which simultaneously enhances their genomic targeting and induces organization of aberrant three-dimensional chromatin structure during tumourous transformation. As LLPS-competent molecules are frequently implicated in diseases.sup.1,2,4-7, this mechanism can potentially be generalized to many malignant and pathological settings. The NUP98-HOXA9 oncogenic fusion protein found in leukaemia undergoes phase separation in the nucleus, which helps to promote activation of leukaemic genes and to establish aberrant chromatin looping.
The development of cancer is intimately associated with genetic abnormalities that target proteins with intrinsically disordered regions (IDRs). In human haematological malignancies, recurrent chromosomal translocation of nucleoporin (NUP98 or NUP214) generates an aberrant chimera that invariably retains the nucleoporin IDR-tandemly dispersed repeats of phenylalanine and glycine residues1,2. However, how unstructured IDRs contribute to oncogenesis remains unclear. Here we show that IDRs contained within NUP98-HOXA9, a homeodomain-containing transcription factor chimera recurrently detected in leukaemias1,2, are essential for establishing liquid-liquid phase separation (LLPS) puncta of chimera and for inducing leukaemic transformation. Notably, LLPS of NUP98-HOXA9 not only promotes chromatin occupancy of chimera transcription factors, but also is required for the formation of a broad 'super-enhancer'-like binding pattern typically seen at leukaemogenic genes, which potentiates transcriptional activation. An artificial HOX chimera, created by replacing the phenylalanine and glycine repeats of NUP98 with an unrelated LLPS-forming IDR of the FUS protein3,4, had similar enhancing effects on the genome-wide binding and target gene activation of the chimera. Deeply sequenced Hi-C revealed that phase-separated NUP98-HOXA9 induces CTCF-independent chromatin loops that are enriched at proto-oncogenes. Together, this report describes a proof-of-principle example in which cancer acquires mutation to establish oncogenic transcription factor condensates via phase separation, which simultaneously enhances their genomic targeting and induces organization of aberrant three-dimensional chromatin structure during tumourous transformation. As LLPS-competent molecules are frequently implicated in diseases1,2,4-7, this mechanism can potentially be generalized to many malignant and pathological settings.
Audience Academic
Author Wang, Gang Greg
Keeley, Daniel P.
Zhao, Shuai
Phanstiel, Douglas H.
Quiroga, Ivana Yoseli
Uryu, Hidetaka
Zheng, Deyou
Storey, Aaron J.
Edmondson, Ricky D.
Davis, Eric S.
Byrum, Stephanie D.
Tsai, Yi-Hsuan
Cai, Ling
Tackett, Alan J.
Daugird, Timothy A.
Mackintosh, Samuel G.
Ahn, Jeong Hyun
Li, Jie
Legant, Wesley R.
AuthorAffiliation 1 Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill School of Medicine, Chapel Hill, NC 27599, USA
7 Department of Biochemistry and Molecular Biology, University of Arkansas for Medical Sciences, Little Rock, AR 72205, USA
8 UNC Neuroscience Center and Carolina Institute for Developmental Disabilities, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA
11 Joint Department of Biomedical Engineering, University of North Carolina, Chapel Hill, and North Carolina State University, Raleigh, NC 27599, USA
9 Department of Genetics, University of North Carolina at Chapel Hill School of Medicine, Chapel Hill, NC 27599, USA
12 Department of Cell Biology and Physiology, University of North Carolina at Chapel Hill School of Medicine, Chapel Hill, NC 27599, USA
2 Department of Biochemistry and Biophysics, University of North Carolina at Chapel Hill School of Medicine, Chapel Hill, NC 27599, USA
5 Thurston Arthritis Research Center, University of North
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– name: 5 Thurston Arthritis Research Center, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA
– name: 10 Departments of Genetics, Neurology, and Neuroscience, Albert Einstein College of Medicine, Bronx, NY 10461, USA
– name: 2 Department of Biochemistry and Biophysics, University of North Carolina at Chapel Hill School of Medicine, Chapel Hill, NC 27599, USA
– name: 3 Curriculum in Bioinformatics and Computational Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA
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– name: 1 Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill School of Medicine, Chapel Hill, NC 27599, USA
– name: 8 UNC Neuroscience Center and Carolina Institute for Developmental Disabilities, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA
– name: 11 Joint Department of Biomedical Engineering, University of North Carolina, Chapel Hill, and North Carolina State University, Raleigh, NC 27599, USA
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  givenname: Daniel P.
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  organization: UNC Neuroscience Center and Carolina Institute for Developmental Disabilities, University of North Carolina at Chapel Hill
– sequence: 11
  givenname: Samuel G.
  surname: Mackintosh
  fullname: Mackintosh, Samuel G.
  organization: Department of Biochemistry and Molecular Biology, University of Arkansas for Medical Sciences
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  givenname: Ricky D.
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  givenname: Deyou
  orcidid: 0000-0003-4354-5337
  surname: Zheng
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– sequence: 17
  givenname: Wesley R.
  surname: Legant
  fullname: Legant, Wesley R.
  organization: Department of Pharmacology, University of North Carolina at Chapel Hill School of Medicine, Joint Department of Biomedical Engineering, University of North Carolina, Chapel Hill, and North Carolina State University
– sequence: 18
  givenname: Douglas H.
  orcidid: 0000-0003-2123-0051
  surname: Phanstiel
  fullname: Phanstiel, Douglas H.
  email: douglas_phanstiel@med.unc.edu
  organization: Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill School of Medicine, Curriculum in Bioinformatics and Computational Biology, University of North Carolina at Chapel Hill, Thurston Arthritis Research Center, University of North Carolina at Chapel Hill, Department of Cell Biology and Physiology, University of North Carolina at Chapel Hill School of Medicine
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  givenname: Gang Greg
  orcidid: 0000-0002-7210-9940
  surname: Wang
  fullname: Wang, Gang Greg
  email: greg_wang@med.unc.edu
  organization: Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill School of Medicine, Department of Biochemistry and Biophysics, University of North Carolina at Chapel Hill School of Medicine, Department of Pharmacology, University of North Carolina at Chapel Hill School of Medicine, Curriculum in Genetics and Molecular Biology, University of North Carolina at Chapel Hill
BackLink https://www.ncbi.nlm.nih.gov/pubmed/34163069$$D View this record in MEDLINE/PubMed
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Notes J.H.A. designed the research, performed experiments, interpreted data and wrote the manuscript. J.H.A., Y-H. T., H.U., J. L., L. C., D.Z. and G.G.W. performed genomic data analysis. J.H.A. and S.Z. performed in vitro phase separation assays. D.P.K. conducted imaging quantification analysis. A.J.S., S.G.M, R.D.E. and S.D.B performed proteomic analysis under the supervision of A.J.T.. T.A.D. and J.H.A. performed single molecule tracking studies under the supervision of W.R.L.. J.H.A and J.L performed murine leukemia assays. E.S.D., I.Y.Q. and J.H.A. performed Hi-C mapping, data analysis and interpretation under the supervision of D.H.P.. G.G.W. conceived the idea, supervised and designed the research, interpreted data, and wrote the manuscript with the inputs from all authors.
These authors jointly supervised this work.
Author contributions
ORCID 0000-0002-1783-3610
0000-0002-7210-9940
0000-0003-2107-4300
0000-0003-2123-0051
0000-0003-4051-3217
0000-0003-4354-5337
0000-0002-6799-0059
OpenAccessLink https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8647409
PMID 34163069
PQID 2554692468
PQPubID 40569
PageCount 5
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crossref_primary_10_1038_s41586_021_03662_5
pubmed_primary_34163069
springer_journals_10_1038_s41586_021_03662_5
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PublicationDate 2021-07-22
PublicationDateYYYYMMDD 2021-07-22
PublicationDate_xml – month: 07
  year: 2021
  text: 2021-07-22
  day: 22
PublicationDecade 2020
PublicationPlace London
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PublicationSubtitle International weekly journal of science
PublicationTitle Nature (London)
PublicationTitleAbbrev Nature
PublicationTitleAlternate Nature
PublicationYear 2021
Publisher Nature Publishing Group UK
Nature Publishing Group
Publisher_xml – name: Nature Publishing Group UK
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Snippet The development of cancer is intimately associated with genetic abnormalities that target proteins with intrinsically disordered regions (IDRs). In human...
SourceID pubmedcentral
proquest
gale
crossref
pubmed
springer
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Aggregation Database
Index Database
Publisher
StartPage 591
SubjectTerms 14/63
38/15
38/91
631/208/68/2486
631/337/100/101
631/67/1990/283/1897
Abnormalities
Animals
Binding
Cancer
Carcinogenesis
Chimeras
Chromatin
Chromatin - genetics
Chromosome translocations
Development and progression
Ewings sarcoma
Female
Genes
Genetic abnormalities
Genetic aspects
Genetic transformation
Genomes
Glycine
Health aspects
HEK293 Cells
HeLa Cells
Homeobox
Homeodomain Proteins - genetics
Humanities and Social Sciences
Humans
Intrinsically Disordered Proteins - genetics
Leukemia
Liquid phases
Mice
Mice, Inbred BALB C
Molecular structure
multidisciplinary
Mutation
Neoplasms - genetics
Neoplasms - pathology
Nuclear Pore Complex Proteins - genetics
Occupancy
Oncogene Proteins, Fusion - genetics
Phase separation
Phenylalanine
Proteins
Proto-oncogenes
Science
Science (multidisciplinary)
Transcription activation
Transcription factors
Transcription Factors - genetics
Transcriptional Activation
Translocation
Translocation, Genetic
Tumorigenesis
Title Phase separation drives aberrant chromatin looping and cancer development
URI https://link.springer.com/article/10.1038/s41586-021-03662-5
https://www.ncbi.nlm.nih.gov/pubmed/34163069
https://www.proquest.com/docview/2554692468
https://pubmed.ncbi.nlm.nih.gov/PMC8647409
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