publication . Article . Other literature type . 2016

Structural basis underlying viral hijacking of a histone chaperone complex

Zhong Deng; Hongda Huang; Paul M. Lieberman; Fang Lu; Andreas Wiedmer; Dinshaw J. Patel; Olga Vladimirova;
Open Access
  • Published: 01 Sep 2016 Journal: Nature Communications, volume 7 (eissn: 2041-1723, Copyright policy)
  • Publisher: Springer Science and Business Media LLC
Abstract
The histone H3.3 chaperone DAXX is implicated in formation of heterochromatin and transcription silencing, especially for newly infecting DNA virus genomes entering the nucleus. Epstein-Barr virus (EBV) can efficiently establish stable latent infection as a chromatinized episome in the nucleus of infected cells. The EBV tegument BNRF1 is a DAXX-interacting protein required for the establishment of selective viral gene expression during latency. Here we report the structure of BNRF1 DAXX-interaction domain (DID) in complex with DAXX histone-binding domain (HBD) and histones H3.3-H4. BNRF1 DID contacts DAXX HBD and histones through non-conserved loops. The BNRF1-D...
Subjects
Medical Subject Headings: viruses
free text keywords: General Biochemistry, Genetics and Molecular Biology, General Physics and Astronomy, General Chemistry, Article, Genetics, Histone, biology.protein, biology, Chaperone (protein), Cell biology, Virus, Viral tegument, Death-associated protein 6, Viral gene, Chaperone complex
Funded by
NIH| MOUSE GENETICS
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 2P30CA008748-43
  • Funding stream: NATIONAL CANCER INSTITUTE
,
NIH| CONSOLIDATED BASIC CANCER RESEARCH PROGRAM
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5P30CA010815-28
  • Funding stream: NATIONAL CANCER INSTITUTE
,
NIH| Pixel Array Detector for X-ray Crystallography
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 1S10RR029205-01
  • Funding stream: NATIONAL CENTER FOR RESEARCH RESOURCES
,
NIH| NE-CAT Center for Advanced Macromolecular Crystallography
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 4P41GM103403-14
  • Funding stream: NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCES
,
NIH| Chromatin Regulation of KSHV Primary Infection
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 1P01CA174439-01A1
  • Funding stream: NATIONAL CANCER INSTITUTE
31 references, page 1 of 3

Alabert C. & Groth A. Chromatin replication and epigenome maintenance. Nat. Rev. Mol. Cell Biol. 13, 153–167 (2012).22358331 [OpenAIRE] [PubMed]

Avvakumov N., Nourani A. & Cote J. Histone chaperones: modulators of chromatin marks. Mol. Cell 41, 502–514 (2011).2136 2547 [OpenAIRE] [PubMed]

Burgess R. J. & Zhang Z. Histone chaperones in nucleosome assembly and human disease. Nat. Struct. Mol. Biol. 20, 14–22 (2013).23288364 [OpenAIRE] [PubMed]

Gurard-Levin Z. A., Quivy J. P. & Almouzni G. Histone chaperones: assisting histone traffic and nucleosome dynamics. Annu. Rev. Biochem. 83, 487–517 (2014).24905786 [OpenAIRE] [PubMed]

Ransom M., Dennehey B. K. & Tyler J. K. Chaperoning histones during DNA replication and repair. Cell 140, 183–195 (2010).20141833 [OpenAIRE] [PubMed]

Filipescu D., Muller S. & Almouzni G. Histone H3 variants and their ch aperones during development and disease: contributing to epigenetic control. Annu. Rev. Cell. Dev. Biol. 30, 615–646 (2014).25288118 [OpenAIRE] [PubMed]

Maze I., Noh K. M., Soshnev A. A. & Allis C. D. Every amino acid matters: essential contributions of histone variants to mammalian development and disease. Nat. Rev. Genet. 15, 259–271 (2014).24614311 [OpenAIRE] [PubMed]

Drane P., Ouararhni K., Depaux A., Shuaib M. & Hamiche A. The death-associated protein DAXX is a novel histone chaperone involved in the replication-independent deposition of H3.3. Genes Dev. 24, 1253–1265 (2010).20504901 [OpenAIRE] [PubMed]

Elsasser S. J., Noh K. M., Diaz N., Allis C. D. & Banaszynski L. A. Histone H3.3 is required for endogenous retroviral element silencing in embryonic stem cells. Nature 522, 240–244 (2015).25938714 [OpenAIRE] [PubMed]

Goldberg A. D.. Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell 140, 678–691 (2010).20211137 [OpenAIRE] [PubMed]

Lewis P. W., Elsaesser S. J., Noh K. M., Stadler S. C. & Allis C. D. Daxx is an H3.3-specific histone chaperone and cooperates with ATRX in replication-independent chromatin assembly at telomeres. Proc. Natl Acad. Sci. USA 107, 14075–14080 (2010).20651253 [OpenAIRE] [PubMed]

Wong L. H.. ATRX interacts with H3.3 in maintaining telomere structural integrity in pluripotent embryonic stem cells. Genome Res.20, 351–360 (2010).20110566 [OpenAIRE] [PubMed]

Everett R. D. & Chelbi-Alix M. K. PML and PML nuclear bodies: implications in antiviral defence. Biochimie 89, 819–830 (2007).17343971 [OpenAIRE] [PubMed]

Lieberman P. M.Chromatin structure of Epstein-Barr virus latent episomes. Curr. Top. Microbiol. Immunol.390, 71–102 (2015).26424644 [PubMed]

Schreiner S. & Wodrich H. Virion factors that target Daxx to overcome intrinsic immunity. J. Virol. 87, 10412–10422 (2013).23864634 [OpenAIRE] [PubMed]

31 references, page 1 of 3
Abstract
The histone H3.3 chaperone DAXX is implicated in formation of heterochromatin and transcription silencing, especially for newly infecting DNA virus genomes entering the nucleus. Epstein-Barr virus (EBV) can efficiently establish stable latent infection as a chromatinized episome in the nucleus of infected cells. The EBV tegument BNRF1 is a DAXX-interacting protein required for the establishment of selective viral gene expression during latency. Here we report the structure of BNRF1 DAXX-interaction domain (DID) in complex with DAXX histone-binding domain (HBD) and histones H3.3-H4. BNRF1 DID contacts DAXX HBD and histones through non-conserved loops. The BNRF1-D...
Subjects
Medical Subject Headings: viruses
free text keywords: General Biochemistry, Genetics and Molecular Biology, General Physics and Astronomy, General Chemistry, Article, Genetics, Histone, biology.protein, biology, Chaperone (protein), Cell biology, Virus, Viral tegument, Death-associated protein 6, Viral gene, Chaperone complex
Funded by
NIH| MOUSE GENETICS
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 2P30CA008748-43
  • Funding stream: NATIONAL CANCER INSTITUTE
,
NIH| CONSOLIDATED BASIC CANCER RESEARCH PROGRAM
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5P30CA010815-28
  • Funding stream: NATIONAL CANCER INSTITUTE
,
NIH| Pixel Array Detector for X-ray Crystallography
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 1S10RR029205-01
  • Funding stream: NATIONAL CENTER FOR RESEARCH RESOURCES
,
NIH| NE-CAT Center for Advanced Macromolecular Crystallography
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 4P41GM103403-14
  • Funding stream: NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCES
,
NIH| Chromatin Regulation of KSHV Primary Infection
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 1P01CA174439-01A1
  • Funding stream: NATIONAL CANCER INSTITUTE
31 references, page 1 of 3

Alabert C. & Groth A. Chromatin replication and epigenome maintenance. Nat. Rev. Mol. Cell Biol. 13, 153–167 (2012).22358331 [OpenAIRE] [PubMed]

Avvakumov N., Nourani A. & Cote J. Histone chaperones: modulators of chromatin marks. Mol. Cell 41, 502–514 (2011).2136 2547 [OpenAIRE] [PubMed]

Burgess R. J. & Zhang Z. Histone chaperones in nucleosome assembly and human disease. Nat. Struct. Mol. Biol. 20, 14–22 (2013).23288364 [OpenAIRE] [PubMed]

Gurard-Levin Z. A., Quivy J. P. & Almouzni G. Histone chaperones: assisting histone traffic and nucleosome dynamics. Annu. Rev. Biochem. 83, 487–517 (2014).24905786 [OpenAIRE] [PubMed]

Ransom M., Dennehey B. K. & Tyler J. K. Chaperoning histones during DNA replication and repair. Cell 140, 183–195 (2010).20141833 [OpenAIRE] [PubMed]

Filipescu D., Muller S. & Almouzni G. Histone H3 variants and their ch aperones during development and disease: contributing to epigenetic control. Annu. Rev. Cell. Dev. Biol. 30, 615–646 (2014).25288118 [OpenAIRE] [PubMed]

Maze I., Noh K. M., Soshnev A. A. & Allis C. D. Every amino acid matters: essential contributions of histone variants to mammalian development and disease. Nat. Rev. Genet. 15, 259–271 (2014).24614311 [OpenAIRE] [PubMed]

Drane P., Ouararhni K., Depaux A., Shuaib M. & Hamiche A. The death-associated protein DAXX is a novel histone chaperone involved in the replication-independent deposition of H3.3. Genes Dev. 24, 1253–1265 (2010).20504901 [OpenAIRE] [PubMed]

Elsasser S. J., Noh K. M., Diaz N., Allis C. D. & Banaszynski L. A. Histone H3.3 is required for endogenous retroviral element silencing in embryonic stem cells. Nature 522, 240–244 (2015).25938714 [OpenAIRE] [PubMed]

Goldberg A. D.. Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell 140, 678–691 (2010).20211137 [OpenAIRE] [PubMed]

Lewis P. W., Elsaesser S. J., Noh K. M., Stadler S. C. & Allis C. D. Daxx is an H3.3-specific histone chaperone and cooperates with ATRX in replication-independent chromatin assembly at telomeres. Proc. Natl Acad. Sci. USA 107, 14075–14080 (2010).20651253 [OpenAIRE] [PubMed]

Wong L. H.. ATRX interacts with H3.3 in maintaining telomere structural integrity in pluripotent embryonic stem cells. Genome Res.20, 351–360 (2010).20110566 [OpenAIRE] [PubMed]

Everett R. D. & Chelbi-Alix M. K. PML and PML nuclear bodies: implications in antiviral defence. Biochimie 89, 819–830 (2007).17343971 [OpenAIRE] [PubMed]

Lieberman P. M.Chromatin structure of Epstein-Barr virus latent episomes. Curr. Top. Microbiol. Immunol.390, 71–102 (2015).26424644 [PubMed]

Schreiner S. & Wodrich H. Virion factors that target Daxx to overcome intrinsic immunity. J. Virol. 87, 10412–10422 (2013).23864634 [OpenAIRE] [PubMed]

31 references, page 1 of 3
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