Dynamics of Viral and Host 3D Genome Structure upon Infection
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Eukaryotic chromatin is highly organized in the 3D nuclear space and dynamically regulated in response to environmental stimuli. This genomic organization is arranged in a hierarchical fashion to support various cellular functions, including transcriptional regulation of gene expression. Like other host cellular mechanisms, viral pathogens utilize and modulate host chromatin architecture and its regulatory machinery to control features of their life cycle, such as lytic versus latent status. Combined with previous research focusing on individual loci, recent global genomic studies employing conformational assays coupled with high-throughput sequencing technology have informed models for host and, in some cases, viral 3D chromosomal structure re-organization during infection and the contribution of these alterations to virus-mediated diseases. Here, we review recent discoveries and progress in host and viral chromatin structural dynamics during infection, focusing on a subset of DNA (human herpesviruses and HPV) as well as RNA (HIV, influenza virus and SARS-CoV-2) viruses. An understanding of how host and viral genomic structure affect gene expression in both contexts and ultimately viral pathogenesis can facilitate the development of novel therapeutic strategies.
Abstract
Eukaryotic chromatin is highly organized in the 3D nuclear space and dynamically regulated in response to environmental stimuli. This genomic organization is arranged in a hierarchical fashion to support various cellular functions, including transcriptional regulation of gene expression. Like other host cellular mechanisms, viral pathogens utilize and modulate host chromatin architecture and its regulatory machinery to control features of their life cycle, such as lytic versus latent status. Combined with previous research focusing on individual loci, recent global genomic studies employing conformational assays coupled with high-throughput sequencing technology have informed models for host and, in some cases, viral 3D chromosomal structure re-organization during infection and the contribution of these alterations to virus-mediated diseases. Here, we review recent discoveries and progress in host and viral chromatin structural dynamics during infection, focusing on a subset of DNA (human herpesviruses and HPV) as well as RNA (HIV, influenza virus and SARS-CoV-2) viruses. An understanding of how host and viral genomic structure affect gene expression in both contexts and ultimately viral pathogenesis can facilitate the development of novel therapeutic strategies.
참고문헌 (107)
- Benabdallah NS, "Decreased enhancer-promoter proximity accompanying enhancer activation", Mol. Cell, 76, pp.473~484 (2019)[DOI]
- Zheng H, "The role of 3D genome organization in development and cell differentiation", Nat. Rev. Mol. Cell Biol, 20, pp.535~550 (2019)
- Kubo N, "Promoter-proximal CTCF binding promotes distal enhancerdependent gene activation", Nat. Struct. Mol. Biol, 28, pp.152~161 (2021)
- Oh S, "Enhancer release and retargeting activates disease-susceptibility genes", Nature, 595, pp.735~740 (2021)
- Simonis M, "Nuclear organization of active and inactive chromatin domains uncovered by chromosome conformation capture-on-chip(4C)", Nat. Genet, 38, pp.1348~1354 (2006)
- Dostie J, "Chromosome conformation capture carbon copy(5C) : a massively parallel solution for mapping interactions between genomic elements", Genome Res, 16, pp.1299~1309 (2006)
- Jäger R, "Capture Hi-C identifies the chromatin interactome of colorectal cancer risk loci", Nat. Commun, 6, pp.6178~ (2015)
- Fang R, "Mapping of long-range chromatin interactions by proximity ligationassisted ChIP-seq", Cell Res, 26, pp.1345~1348 (2016)
- Fullwood MJ, "Next-generation DNA sequencing of paired-end tags(PET)for transcriptome and genome analyses", Genome Res, 19, pp.521~532 (2009)
- Sati S, "Chromosome conformation capture technologies and their impact in understanding genome function", Chromosoma, 126, pp.33~44 (2017)
- Hsieh TH, "Mapping nucleosome resolution chromosome folding in yeast by micro-C", Cell, 162, pp.108~119 (2015)
- Quinodoz SA, "SPRITE : a genome-wide method for mapping higher-order 3D interactions in the nucleus using combinatorial split-and-pool barcoding", Nat. Protoc, 17, pp.36~75 (2022)
- Beagrie RA, "Complex multi-enhancer contacts captured by genome architecture mapping", Nature, 543, pp.519~524 (2017)
- Consortium IH, "The international HapMap project", Nature, 426, pp.789~796 (2003)
- Consortium EP, "An integrated encyclopedia of DNA elements in the human genome", Nature, 489, pp.57~74 (2021)
- Arvey A, "An atlas of the Epstein-Barr virus transcriptome and epigenome reveals host-virus regulatory interactions", Cell Host Microbe, 12, pp.233~245 (2012)
- Rao SS, "A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping", Cell, 159, pp.1665~1680 (2014)
- Quinodoz SA, "Higher-order inter-chromosomal hubs shape 3D genome organization in the nucleus", Cell, 174, pp.744~757 (2018)[DOI]
- Buschle A, "Epigenetic lifestyle of Epstein-Barr virus", Semin Immunopathol, 42, pp.131~142 (2020)
- Toth Z, "The chromatin landscape of Kaposi's sarcoma-associated herpesvirus", Viruses, 5, pp.1346~1373 (2013)
- Chen HS, "Cohesins repress Kaposi's sarcoma-associated herpesvirus immediate early gene transcription during latency", J. Virol, 8, pp.9454~9464 (2012)
- Zhao B, "Epstein-Barr virus exploits intrinsic B-lymphocyte transcription programs to achieve immortal cell growth", Proc. Natl. Acad. Sci. USA, 108, pp.14902~14907 (2011)
- Chau CM, "Regulation of Epstein-Barr virus latency type by the chromatin boundary factor CTCF", J. Virol, 80, pp.5723~5732 (2006)
- Hughes DJ, "Contributions of CTCF and DNA methyltransferases DNMT1 and DNMT3B to Epstein-Barr virus restricted latency", J. Virol, 86, pp.1034~1045 (2012)
- Tempera I, "CTCF prevents the epigenetic drift of EBV latency promoter Qp", PLoS Pathog, 6, pp.e1001048~ (2010)
- Chen HS, "Epigenetic deregulation of the LMP1", LMP2 locus of Epstein-Barr virus by mutation of a single CTCF-cohesin binding site, 2014, pp.88, 1703~1713
- Molyneux EM, "Burkitt's lymphoma", Lancet, 379, pp.1234~1244 (2012)
- Wang LW, "Epstein-Barr-v-induced one-carbon metabolism drives B cell transformation", Cell Metab, 30, pp.539~555 (2019)
- Wood CD, "MYC activation and BCL2L11 silencing by a tumour virus through the large-scale reconfiguration of enhancer-promoter hubs", Elife, 5, pp.e18270~ (2016)
- Jiang S, "The Epstein-Barr virus regulome in lymphoblastoid cells", Cell Host Microbe, 22, pp.561~573 (2017)[DOI]
- Guo R, "MYC controls the epstein-barr virus lytic switch", Mol. Cell, 78, pp.653~669 (2020)[DOI]
- Knipe DM, "Snapshots : chromatin control of viral infection", Virology, 435, pp.141~156 (2013)
- zStedman W, "Cohesins localize with CTCF at the KSHV latency control region and at cellular c-myc and H19", Igf2 insulators, 2008, pp.27, 654~666
- Li DJ, "CTCF and Rad21 act as host cell restriction factors for Kaposi's sarcomaassociated herpesvirus(KSHV)lytic replication by modulating viral gene transcription", PLoS Pathog, 10, pp.e1003880~ (2014)
- Park A, "Global epigenomic analysis of KSHV-infected primary effusion lymphoma identifies functional MYC superenhancers and enhancer RNAs", Proc. Natl. Acad. Sci. USA, 117, pp.21618~21627 (2020)
- Bloom DC, "Epigenetic regulation of latent HSV-1 gene expression", Biochim. Biophys. Acta, 1799, pp.246~256 (2010)
- Ertel MK, "CTCF occupation of the herpes simplex virus 1 genome is disrupted at early times postreactivation in a transcription-dependent manner", J. Virol, 86, pp.12741~12759 (2012)
- Martínez FP, "CTCF binding to the first intron of the major immediate early(MIE)gene of human cytomegalovirus(HCMV)negatively regulates MIE gene expression and HCMV replication", J. Virol, 88, pp.7389~7401 (2014)
- Lee JS, "CCCTC-binding factor acts as a heterochromatin barrier on herpes simplex viral latent chromatin and contributes to poised latent infection", mBio, 9, pp.e02372~17 (2018)
- Lang F, "CTCF interacts with the lytic HSV-1 genome to promote viral transcription", Sci. Rep, 7, pp.39861~ (2017)
- Li X, "Cohesin promotes HSV-1 lytic transcription by facilitating the binding of RNA Pol II on viral genes", Virol. J, 18, pp.26~ (2021)
- Morgan SM, "The three-dimensional structure of Epstein-Barr virus genome varies by latency type and is regulated by PARP1 enzymatic activity", Nat. Commun, 13, pp.187~ (2022)
- Campbell M, "KSHV episomes reveal dynamic chromatin loop formation with domain-specific gene regulation", Nat. Commun, 9, pp.49~ (2018)
- Campbell M, "KSHV topologically associating domains in latent and reactivated viral chromatin", J. Virol, 96, pp.e0056522~ (2022)
- Moquin SA, "The epstein-barr virus episome maneuvers between nuclear chromatin compartments during reactivation", J. Virol, 92, pp.e01413~17 (2018)
- Kim, "Epigenetic specifications of host chromosome docking sites for latent Epstein-Barr virus", Nat. Commun, 11, pp.877~ (2020)
- Okabe A, "Cross-species chromatin interactions drive transcriptional rewiring in Epstein-Barr virus-positive gastric adenocarcinoma", Nat. Genet, 52, pp.919~930 (2020)
- Caruso LB, "The nuclear lamina binds the EBV genome during latency and regulates viral gene expression", PLoS Pathog, 18, pp.e1010400~ (2022)
- Luopin Wang, "Epstein-Barr Virus Episome Physically Interacts with Active Regions of the Host Genome in Lymphoblastoid Cells", Journal of Virology, 94(24) (2020), American Society for Microbiology[DOI]
- Kumar A, "KSHV episome tethering sites on host chromosomes and regulation of latency-lytic switch by CHD4", Cell Rep, 39, pp.110788~ (2022)
- Ballestas ME, "The latency-associated nuclear antigen, a multifunctional protein central to Kaposi's sarcomaassociated herpesvirus latency", Future Microbiol, 6, pp.1399~1413 (2011)
- Walboomers JM, "Human papillomavirus is a necessary cause of invasive cervical cancer worldwide", J. Pathol, 189, pp.12~19 (1999)
- McLaughlin-Drubin ME, "Oncogenic activities of human papillomaviruses", Virus Res, 143, pp.195~208 (2009)
- Cao C, "HPV-CCDC106 integration alters local chromosome architecture and hijacks an enhancer by three-dimensional genome structure remodeling in cervical cancer", J. Genet. Genomics, 47, pp.437~450 (2020)
- Zhou, C., "Papillomavirus immune evasion strategies target the infected cell and the local immune system", Front. Oncol, 9, pp.682~ (2019)
- Mehta K, "Human papillomaviruses activate and recruit SMC1 cohesin proteins for the differentiation-dependent life cycle through association with CTCF insulators", PLoS Pathog, 11, pp.e1004763~ (2015)
- Mehta K, "Human papillomaviruses preferentially recruit DNA repair factors to viral genomes for rapid repair and amplification", mBio, 9, pp.e00064~18 (2018)
- Paris C, "CCCTC-binding factor recruitment to the early region of the human papillomavirus 18 genome regulates viral oncogene expression", J. Virol, 89, pp.4770~4785 (2015)
- Pentland I, "Disruption of CTCF-YY1-dependent looping of the human papillomavirus genome activates differentiation-induced viral oncogene transcription", PLoS Biol, 16, pp.e2005752~ (2018)
- Ferguson J, "The chromatin insulator CTCF regulates HPV18 transcript splicing and differentiation-dependent late gene expression", PLoS Pathog, 17, pp.e1010032~ (2021)
- McBride AA, "The role of integration in oncogenic progression of HPV-associated cancers", PLoS Pathog, 13, pp.e1006211~ (2017)
- Ojesina AI, "Landscape of genomic alterations in cervical carcinomas", Nature, 506, pp.371~375 (2014)
- Dixon JR, "Integrative detection and analysis of structural variation in cancer genomes", Nat. Genet, 50, pp.1388~1398 (2018)
- Shen C, "Long-distance interaction of the integrated HPV fragment with MYC gene and 8q24.22 region upregulating the allele-specific MYC expression in HeLa cells", Int. J. Cancer, 141, pp.540~548 (2017)
- Bodelon C, "Genomic characterization of viral integration sites in HPV-related cancers", Int. J. Cancer, 139, pp.2001~2011 (2016)
- Kelley DZ, "Integrated analysis of whole-genome ChIP-Seq and RNA-Seq data of primary head and neck tumor samples associates HPV integration sites with open chromatin marks", Cancer Res, 77, pp.6538~6550 (2017)
- Hu Z, "Genome-wide profiling of HPV integration in cervical cancer identifies clustered genomic hot spots and a potential microhomology-mediated integration mechanism", Nat. Genet, 47, pp.158~163 (2015)
- Warburton A, "Recurrent integration of human papillomavirus genomes at transcriptional regulatory hubs", NPJ Genom. Med, 6, pp.101~ (2021)
- Warburton A, "HPV integration hijacks and multimerizes a cellular enhancer to generate a viral-cellular super-enhancer that drives high viral oncogene expression", PLoS Genet, 14, pp.e1007179~ (2018)
- Zhou L, "Long-read sequencing unveils high-resolution HPV integration and its oncogenic progression in cervical cancer", Nat. Commun, 13, pp.2563~ (2022)
- Turner KM, "Extrachromosomal oncogene amplification drives tumour evolution and genetic heterogeneity", Nature, 543, pp.122~125 (2017)
- Adeel MM, "Structural variations of the 3D genome architecture in cervical cancer development", Front. Cell Dev. Biol, 9, pp.706375~ (2021)
- Mehran Karimzadeh, "Human papillomavirus integration transforms chromatin to drive oncogenesis" (2022)[DOI]
- Lusic M, "Nuclear landscape of HIV-1 infection and integration", Nat. Rev. Microbiol, 15, pp.69~82 (2017)
- Marini B, "Nuclear architecture dictates HIV-1 integration site selection", Nature, 521, pp.227~231 (2015)
- Chen H-C, "Position effects influence HIV latency reversal", Nat. Struct. Mol. Biol, 24, pp.47~54 (2017)
- Vansant G, "The chromatin landscape at the HIV-1 provirus integration site determines viral expression", Nucleic Acids Res, 48, pp.7801~7817 (2020)
- Perkins KJ, "Transcription-dependent gene looping of the HIV-1 provirus is dictated by recognition of pre-mRNA processing signals", Mol. Cell, 29, pp.56~68 (2008)
- Dieudonné M, "Transcriptional competence of the integrated HIV-1 provirus at the nuclear periphery", EMBO J, 28, pp.2231~2243 (2009)
- Lucic B, "Spatially clustered loci with multiple enhancers are frequent targets of HIV-1 integration", Nat. Commun, 10, pp.4059~ (2019)
- "Genomic profiling of HIV-1 integration in microglia links viral insertions to TAD organization" (2022)[URL]
- "An integrated genomics approach towards deciphering human genome codes shaping HIV-1 proviral transcription and fate" (2020)[URL]
- Heinz S, "Transcription elongation can affect genome 3D structure", Cell, 174, pp.1522~1536 (2018)[DOI]
- Shiimori M, "Suv4-20h2 protects against influenza virus infection by suppression of chromatin loop formation", iScience, 24, pp.102660~ (2021)
- Shiimori M, "Dynamics of the host chromatin three-dimensional response to influenza virus infection", Int. Immunol, 33, pp.541~545 (2021)
- Chen T, "A low-producing haplotype of interleukin-6 disrupting CTCF binding is protective against severe COVID-19", mBio, 12, pp.e0137221~ (2021)
- Nakanishi T, "Age-dependent impact of the major common genetic risk factor for COVID-19 on severity and mortality", J. Clin. Invest, 131, pp.e152386~ (2021)
- Stikker BS, "Severe COVID-19-associated variants linked to chemokine receptor gene control in monocytes and macrophages", Genome Biol, 23, pp.96~ (2022)
- Merad M, "Pathological inflammation in patients with COVID-19 : a key role for monocytes and macrophages", Nat. Rev. Immunol, 20, pp.355~362 (2020)
- Szabo PA, "Longitudinal profiling of respiratory and systemic immune responses reveals myeloid cell-driven lung inflammation in severe COVID-19", Immunity, 54, pp.797~814 (2021)[DOI]
- Salgado-Albarrán M, "Comparative transcriptome analysis reveals key epigenetic targets in SARS-CoV-2 infection", NPJ Syst. Biol. Appl, 7, pp.21~ (2021)
- Huoman J, "Epigenome-wide DNA methylation profiling of healthy COVID-19 recoverees reveals a unique signature in circulating immune cells", MedRXiv (2021)[DOI]
- Merkenschlager M, "CTCF and cohesin in genome folding and transcriptional gene regulation", Annu. Rev. Genomics Hum. Genet, 17, pp.17~43 (2016)
- Yuen, "Taking cohesin and condensin in context", PLoS Genet, pp.14~ (2018)
- Bjornevik K, "Longitudinal analysis reveals high prevalence of Epstein-Barr virus associated with multiple sclerosis", Science, 375, pp.296~301 (2022)
- Itzhaki RF, "Does antiherpetic antiviral therapy reduce the risk of dementia?", Nat. Rev. Neurol, 18, pp.63~64 (2022)
- Young-Xu Y, "Symptomatic herpes simplex virus infection and risk of dementia in US veterans : a cohort study", Neurotherapeutics, 18, pp.2458~2467 (2021)
- Ma H, "Multicolor CRISPR labeling of chromosomal loci in human cells", Proc. Natl. Acad. Sci. USA, 112, pp.3002~3007 (2015)
- Chen B, "Dynamic imaging of genomic loci in living human cells by an optimized CRISPR", Cas system, 2013, pp.155, 1479~1491
- Washington SD, "Depletion of the insulator protein CTCF results in herpes simplex virus 1 reactivation", J. Virol, 92, pp.e00173~18 (2018)
- Lupey-Green LN, "PARP1 restricts Epstein Barr Virus lytic reactivation by binding the BZLF1 promoter", Virology, 507, pp.220~230 (2017)
- Kang H, "Coordination of KSHV latent and lytic gene control by CTCFcohesin mediated chromosome conformation", PLoS Pathog, 7, pp.e1002140~ (2011)
- Jefferys SR, "Epigenomic characterization of latent HIV infection identifies latency regulating transcription factors", PLoS Pathog, 17, pp.e1009346~ (2021)
- D'Arienzo V, "The CCCTC-binding factor CTCF represses hepatitis B virus enhancer I and regulates viral transcription", Cell. Microbiol, 23, pp.e13274~ (2021)
- Decorsière A, "Hepatitis B virus X protein identifies the Smc5", 6 complex as a host restriction factor, 2016, pp.531, 386~389
- Komatsu T, "DNA replication-dependent binding of CTCF plays a critical role in adenovirus genome functions", Sci. Rep, 3, pp.2187~ (2013)
