A DNA tumor virus globally reprograms host 3D genome architecture to achieve immortal growth.

Humans Herpesvirus 4, Human / physiology Epstein-Barr Virus Infections Epstein-Barr Virus Nuclear Antigens / metabolism Cell Line B-Lymphocytes / metabolism

Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
22 03 2023
Historique:
received: 28 08 2019
accepted: 13 03 2023
entrez: 23 3 2023
pubmed: 24 3 2023
medline: 25 3 2023
Statut: epublish

Résumé

Epstein-Barr virus (EBV) immortalization of resting B lymphocytes (RBLs) to lymphoblastoid cell lines (LCLs) models human DNA tumor virus oncogenesis. RBL and LCL chromatin interaction maps are compared to identify the spatial and temporal genome architectural changes during EBV B cell transformation. EBV induces global genome reorganization where contact domains frequently merge or subdivide during transformation. Repressed B compartments in RBLs frequently switch to active A compartments in LCLs. LCLs gain 40% new contact domain boundaries. Newly gained LCL boundaries have strong CTCF binding at their borders while in RBLs, the same sites have much less CTCF binding. Some LCL CTCF sites also have EBV nuclear antigen (EBNA) leader protein EBNALP binding. LCLs have more local interactions than RBLs at LCL dependency factors and super-enhancer targets. RNA Pol II HiChIP and FISH of RBL and LCL further validate the Hi-C results. EBNA3A inactivation globally alters LCL genome interactions. EBNA3A inactivation reduces CTCF and RAD21 DNA binding. EBNA3C inactivation rewires the looping at the CDKN2A/B and AICDA loci. Disruption of a CTCF site at AICDA locus increases AICDA expression. These data suggest that EBV controls lymphocyte growth by globally reorganizing host genome architecture to facilitate the expression of key oncogenes.

Identifiants

DOI: 10.1038/s41467-023-37347-6 PMID: 36949074 PMC: PMC10033825
pubmed: 36949074
doi: 10.1038/s41467-023-37347-6
pii: 10.1038/s41467-023-37347-6
pmc: PMC10033825
doi:

Substances chimiques

Epstein-Barr Virus Nuclear Antigens 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1598

Subventions

Organisme : NIAID NIH HHS
ID : DP2 AI171139
Pays : United States

Informations de copyright

© 2023. The Author(s).

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Auteurs

Chong Wang (C)

Division of Infectious Disease, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, 181 Longwood Avenue, Boston, MA, 02115, USA.
Department of Diagnostic and Biological Sciences, School of Dentistry, University of Minnesota, Minneapolis, MN, 55455, USA.

Xiang Liu (X)

Department of Biostatistics and Bioinformatics, H. Lee Moffitt Cancer Center and Research Institute, Tampa, FL, 33612, USA.
ORCID: 0000-0002-7081-3694

Jun Liang (J)

Division of Infectious Disease, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, 181 Longwood Avenue, Boston, MA, 02115, USA.

Yohei Narita (Y)

Division of Infectious Disease, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, 181 Longwood Avenue, Boston, MA, 02115, USA.
ORCID: 0000-0002-8867-3669

Weiyue Ding (W)

Division of Infectious Disease, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, 181 Longwood Avenue, Boston, MA, 02115, USA.

Difei Li (D)

Division of Infectious Disease, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, 181 Longwood Avenue, Boston, MA, 02115, USA.

Luyao Zhang (L)

Division of Infectious Disease, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, 181 Longwood Avenue, Boston, MA, 02115, USA.

Hongbo Wang (H)

Division of Infectious Disease, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, 181 Longwood Avenue, Boston, MA, 02115, USA.

Merrin Man Long Leong (MML)

Division of Infectious Disease, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, 181 Longwood Avenue, Boston, MA, 02115, USA.

Isabella Hou (I)

Division of Infectious Disease, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, 181 Longwood Avenue, Boston, MA, 02115, USA.

Catherine Gerdt (C)

Division of Infectious Disease, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, 181 Longwood Avenue, Boston, MA, 02115, USA.

Chang Jiang (C)

Division of Infectious Disease, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, 181 Longwood Avenue, Boston, MA, 02115, USA.
Department of Cancer Physiology, H. Lee Moffitt Cancer Center and Research Institute, Tampa, FL, 33612, USA.

Qian Zhong (Q)

State Key Laboratory of Oncology in South China, Collaborative Innovation Center for Cancer Medicine, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Sun Yat-sen University Cancer Center, Guangzhou, 510060, China.
ORCID: 0000-0003-1071-6996

Zhonghui Tang (Z)

Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou, 510060, China.

Carmy Forney (C)

Center for Autoimmune Genomics and Etiology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, 45229, USA.

Leah Kottyan (L)

Center for Autoimmune Genomics and Etiology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, 45229, USA.
ORCID: 0000-0003-3979-2220

Matthew T Weirauch (MT)

Center for Autoimmune Genomics and Etiology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, 45229, USA.
ORCID: 0000-0001-7977-9122

Benjamin E Gewurz (BE)

Division of Infectious Disease, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, 181 Longwood Avenue, Boston, MA, 02115, USA.
ORCID: 0000-0002-3965-3418

Mu-Sheng Zeng (MS)

State Key Laboratory of Oncology in South China, Collaborative Innovation Center for Cancer Medicine, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Sun Yat-sen University Cancer Center, Guangzhou, 510060, China.
ORCID: 0000-0003-3509-5591

Sizun Jiang (S)

Center for Virology and Vaccine Research, Beth Israel Deaconess Medical Center and Harvard Medical School, Boston, MA, 02115, USA. sjiang3@bidmc.harvard.edu.
ORCID: 0000-0001-6149-3142

Mingxiang Teng (M)

Department of Biostatistics and Bioinformatics, H. Lee Moffitt Cancer Center and Research Institute, Tampa, FL, 33612, USA. mingxiang.teng@moffitt.org.
ORCID: 0000-0002-8536-8941

Bo Zhao (B)

Division of Infectious Disease, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, 181 Longwood Avenue, Boston, MA, 02115, USA. bzhao@bwh.harvard.edu.
ORCID: 0000-0002-8612-5597

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Classifications MeSH

questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Primates › Haplorhini › Catarrhini › Hominidae › Humains › A DNA tumor virus globally reprograms host 3D...
questionsmedicales.fr › Virus › Virus oncogènes › Virus tumoraux à ADN › Gammaherpesvirinae › Lymphocryptovirus › Herpèsvirus humain de type 4 › A DNA tumor virus globally reprograms host 3D...
questionsmedicales.fr › Infection › Maladies virales › Infections à virus oncogènes › Infections à virus Epstein-Barr › A DNA tumor virus globally reprograms host 3D...
questionsmedicales.fr › Facteurs biologiques › Antigènes › Antigènes viraux › Antigènes nucléaires du virus d'Epstein-Barr › A DNA tumor virus globally reprograms host 3D...
questionsmedicales.fr › Cellules › Cellules cultivées › Lignée cellulaire › A DNA tumor virus globally reprograms host 3D...
questionsmedicales.fr › Systèmes sanguin et immunitaire › Système immunitaire › Leucocytes › Agranulocytes › Lymphocytes › Lymphocytes B › A DNA tumor virus globally reprograms host 3D...