Quantitative Microscopy Reveals Stepwise Alteration of Chromatin Structure during Herpesvirus Infection

Aho, Vesa; Mäntylä, Elina; Ekman, Axel; Hakanen, Satu; Mattola, Salla; Chen, Jian-Hua; Weinhardt, Venera; Ruokolainen, Visa; Sodeik, Beate; Larabell, Carolyn; Vihinen-Ranta, Maija

doi:10.3390/v11100935

Quantitative Microscopy Reveals Stepwise Alteration of Chromatin Structure during Herpesvirus Infection

Journal Article · Fri Oct 11 00:00:00 EDT 2019 · Viruses

DOI:https://doi.org/10.3390/v11100935· OSTI ID:2376233

; ; Ekman, Axel; Hakanen, Satu; ; ; ; Ruokolainen, Visa; ; Larabell, Carolyn;

During lytic herpes simplex virus 1 (HSV-1) infection, the expansion of the viral replication compartments leads to an enrichment of the host chromatin in the peripheral nucleoplasm. We have shown previously that HSV-1 infection induces the formation of channels through the compacted peripheral chromatin. Here, we used three-dimensional confocal and expansion microscopy, soft X-ray tomography, electron microscopy, and random walk simulations to analyze the kinetics of host chromatin redistribution and capsid localization relative to their egress site at the nuclear envelope. Our data demonstrated a gradual increase in chromatin marginalization, and the kinetics of chromatin smoothening around the viral replication compartments correlated with their expansion. We also observed a gradual transfer of capsids to the nuclear envelope. Later in the infection, random walk modeling indicated a gradually faster transport of capsids to the nuclear envelope that correlated with an increase in the interchromatin channels in the nuclear periphery. Our study reveals a stepwise and time-dependent mechanism of herpesvirus nuclear egress, in which progeny viral capsids approach the egress sites at the nuclear envelope via interchromatin spaces.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE; USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 2376233

Alternate ID(s):: OSTI ID: 1628589
OSTI ID: 1695713

Journal Information:: Viruses, Journal Name: Viruses Journal Issue: 10 Vol. 11; ISSN VIRUBR; ISSN 1999-4915

Publisher:: MDPI AGCopyright Statement

Country of Publication:: Switzerland

Language:: English

References (67)

Physiological importance of RNA and protein mobility in the cell nucleus Misteli, Tom Histochemistry and Cell Biology, Vol. 129, Issue 1 https://doi.org/10.1007/s00418-007-0355-x	journal	November 2007
Minimum cross entropy thresholding Li, C. H.; Lee, C. K. Pattern Recognition, Vol. 26, Issue 4 https://doi.org/10.1016/0031-3203(93)90115-D	journal	April 1993
Highly localized tracks of specific transcripts within interphase nuclei visualized by in situ hybridization Lawrence, Jeanne Bentley; Singer, Robert H.; Marselle, Lisa M. Cell, Vol. 57, Issue 3 https://doi.org/10.1016/0092-8674(89)90924-0	journal	May 1989
Liquid-crystalline, phage-like packing of encapsidated DNA in herpes simplex virus Booy, F. P.; Newcomb, W. W.; Trus, B. L. Cell, Vol. 64, Issue 5 https://doi.org/10.1016/0092-8674(91)90324-R	journal	March 1991
Movement of nuclear poly(A) RNA throughout the interchromatin space in living cells Politz, Joan C.; Tuft, Richard A.; Pederson, Thoru Current Biology, Vol. 9, Issue 6 https://doi.org/10.1016/S0960-9822(99)80136-5	journal	March 1999
The road much traveled: trafficking in the cell nucleus Gorski, Stanislaw A.; Dundr, Miroslav; Misteli, Tom Current Opinion in Cell Biology, Vol. 18, Issue 3 https://doi.org/10.1016/j.ceb.2006.03.002	journal	June 2006
Structural Basis of Vesicle Formation at the Inner Nuclear Membrane Hagen, Christoph; Dent, Kyle C.; Zeev-Ben-Mordehai, Tzviya Cell, Vol. 163, Issue 7 https://doi.org/10.1016/j.cell.2015.11.029	journal	December 2015
IFI16 Acts as a Nuclear Pathogen Sensor to Induce the Inflammasome in Response to Kaposi Sarcoma-Associated Herpesvirus Infection Kerur, Nagaraj; Veettil, Mohanan Valiya; Sharma-Walia, Neelam Cell Host & Microbe, Vol. 9, Issue 5 https://doi.org/10.1016/j.chom.2011.04.008	journal	May 2011
Herpesvirus capsid assembly: insights from structural analysis Brown, Jay C.; Newcomb, William W. Current Opinion in Virology, Vol. 1, Issue 2 https://doi.org/10.1016/j.coviro.2011.06.003	journal	August 2011
Baculovirus Actin-Based Motility Drives Nuclear Envelope Disruption and Nuclear Egress Ohkawa, Taro; Welch, Matthew D. Current Biology, Vol. 28, Issue 13 https://doi.org/10.1016/j.cub.2018.05.027	journal	July 2018
Polarized DNA Ejection from the Herpesvirus Capsid Newcomb, William W.; Cockrell, Shelley K.; Homa, Fred L. Journal of Molecular Biology, Vol. 392, Issue 4 https://doi.org/10.1016/j.jmb.2009.07.052	journal	October 2009
Automatic alignment and reconstruction of images for soft X-ray tomography Parkinson, Dilworth Y.; Knoechel, Christian; Yang, Chao Journal of Structural Biology, Vol. 177, Issue 2 https://doi.org/10.1016/j.jsb.2011.11.027	journal	February 2012
X-ray tomography of whole cells Le Gros, Mark A.; McDermott, Gerry; Larabell, Carolyn A. Current Opinion in Structural Biology, Vol. 15, Issue 5 https://doi.org/10.1016/j.sbi.2005.08.008	journal	October 2005
Soft X-ray tomography and cryogenic light microscopy: the cool combination in cellular imaging McDermott, Gerry; Le Gros, Mark A.; Knoechel, Christian G. Trends in Cell Biology, Vol. 19, Issue 11 https://doi.org/10.1016/j.tcb.2009.08.005	journal	November 2009
Herpes simplex virus capsid assembly and DNA packaging: a present and future antiviral drug target Baines, Joel D. Trends in Microbiology, Vol. 19, Issue 12 https://doi.org/10.1016/j.tim.2011.09.001	journal	December 2011
Three distinct stages of apoptotic nuclear condensation revealed by time-lapse imaging, biochemical and electron microscopy analysis of cell-free apoptosis Toné, Shigenobu; Sugimoto, Kenji; Tanda, Kazue Experimental Cell Research, Vol. 313, Issue 16 https://doi.org/10.1016/j.yexcr.2007.06.018	journal	October 2007
Diffusional protein transport within the nucleus: a message in the medium Pederson, Thoru Nature Cell Biology, Vol. 2, Issue 5 https://doi.org/10.1038/35010501	journal	May 2000
Annexation of the interchromosomal space during viral infection Monier, Karine; Armas, Juan Carlos González; Etteldorf, Susanne Nature Cell Biology, Vol. 2, Issue 9 https://doi.org/10.1038/35023615	journal	August 2000
Condensed matter in cell death Zamzami, Naoufal; Kroemer, Guido Nature, Vol. 401, Issue 6749 https://doi.org/10.1038/43591	journal	September 1999
Acinus is a caspase-3-activated protein required for apoptotic chromatin condensation Sahara, Setsuko; Aoto, Mamoru; Eguchi, Yutaka Nature, Vol. 401, Issue 6749 https://doi.org/10.1038/43678	journal	September 1999
Protein-retention expansion microscopy of cells and tissues labeled using standard fluorescent proteins and antibodies Tillberg, Paul W.; Chen, Fei; Piatkevich, Kiryl D. Nature Biotechnology, Vol. 34, Issue 9 https://doi.org/10.1038/nbt.3625	journal	July 2016
Nuclear mRNA on the move Noble, Kristen N.; Wente, Susan R. Nature Cell Biology, Vol. 12, Issue 6 https://doi.org/10.1038/ncb0610-525	journal	June 2010
Active intranuclear movement of herpesvirus capsids Forest, Thomas; Barnard, Sandra; Baines, Joel D. Nature Cell Biology, Vol. 7, Issue 4 https://doi.org/10.1038/ncb1243	journal	April 2005
Dynamics of single mRNP nucleocytoplasmic transport and export through the nuclear pore in living cells Mor, Amir; Suliman, Shimrit; Ben-Yishay, Rakefet Nature Cell Biology, Vol. 12, Issue 6 https://doi.org/10.1038/ncb2056	journal	May 2010
Herpesviruses carrying a Brainbow cassette reveal replication and expression of limited numbers of incoming genomes Kobiler, Oren; Lipman, Yaron; Therkelsen, Kate Nature Communications, Vol. 1, Issue 1 https://doi.org/10.1038/ncomms1145	journal	December 2010
Membrane deformation and scission by the HSV-1 nuclear egress complex Bigalke, Janna M.; Heuser, Thomas; Nicastro, Daniela Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms5131	journal	June 2014
Mechanisms and functions of nuclear envelope remodelling Ungricht, Rosemarie; Kutay, Ulrike Nature Reviews Molecular Cell Biology, Vol. 18, Issue 4 https://doi.org/10.1038/nrm.2016.153	journal	January 2017
Nuclear pore complex composition: a new regulator of tissue-specific and developmental functions Raices, Marcela; D'Angelo, Maximiliano A. Nature Reviews Molecular Cell Biology, Vol. 13, Issue 11 https://doi.org/10.1038/nrm3461	journal	October 2012
Chromatin organization regulates viral egress dynamics Aho, Vesa; Myllys, Markko; Ruokolainen, Visa Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-03630-y	journal	June 2017
Chronic lymphocytic leukemia B cells are highly sensitive to infection by herpes simplex virus-1 via herpesvirus-entry-mediator A Eling, Dj; Johnson, Pa; Sharma, S. Gene Therapy, Vol. 7, Issue 14 https://doi.org/10.1038/sj.gt.3301241	journal	July 2000
Herpes simplex virus 1 induces egress channels through marginalized host chromatin Myllys, Markko; Ruokolainen, Visa; Aho, Vesa Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep28844	journal	June 2016
Mechanism of mRNA transport in the nucleus Vargas, D. Y.; Raj, A.; Marras, S. A. E. Proceedings of the National Academy of Sciences, Vol. 102, Issue 47 https://doi.org/10.1073/pnas.0505580102	journal	November 2005
Acetylation modulates cellular distribution and DNA sensing ability of interferon-inducible protein IFI16 Li, T.; Diner, B. A.; Chen, J. Proceedings of the National Academy of Sciences, Vol. 109, Issue 26 https://doi.org/10.1073/pnas.1203447109	journal	June 2012
Nuclear IFI16 induction of IRF-3 signaling during herpesviral infection and degradation of IFI16 by the viral ICP0 protein Orzalli, M. H.; DeLuca, N. A.; Knipe, D. M. Proceedings of the National Academy of Sciences, Vol. 109, Issue 44 https://doi.org/10.1073/pnas.1211302109	journal	October 2012
Remodeling nuclear architecture allows efficient transport of herpesvirus capsids by diffusion Bosse, Jens B.; Hogue, Ian B.; Feric, Marina Proceedings of the National Academy of Sciences, Vol. 112, Issue 42 https://doi.org/10.1073/pnas.1513876112	journal	October 2015
A Single Herpesvirus Protein Can Mediate Vesicle Formation in the Nuclear Envelope Lorenz, Michael; Vollmer, Benjamin; Unsay, Joseph D. Journal of Biological Chemistry, Vol. 290, Issue 11 https://doi.org/10.1074/jbc.M114.627521	journal	January 2015
Efficient Implementation of Marching Cubes' Cases with Topological Guarantees Lewiner, Thomas; Lopes, Hélio; Vieira, Antônio Wilson Journal of Graphics Tools, Vol. 8, Issue 2 https://doi.org/10.1080/10867651.2003.10487582	journal	January 2003
The diffusive way out: Herpesviruses remodel the host nucleus, enabling capsids to access the inner nuclear membrane Bosse, Jens B.; Enquist, Lynn W. Nucleus, Vol. 7, Issue 1 https://doi.org/10.1080/19491034.2016.1149665	journal	February 2016
Microtubule-mediated Transport of Incoming Herpes Simplex Virus 1 Capsids to the Nucleus Sodeik, Beate; Ebersold, Melanie W.; Helenius, Ari Journal of Cell Biology, Vol. 136, Issue 5 https://doi.org/10.1083/jcb.136.5.1007	journal	March 1997
Actin-based motility drives baculovirus transit to the nucleus and cell surface Ohkawa, Taro; Volkman, Loy E.; Welch, Matthew D. The Journal of Cell Biology, Vol. 190, Issue 2 https://doi.org/10.1083/jcb.201001162	journal	July 2010
Intranuclear Localization of Herpes Simplex Virus Immediate-Early and Delayed-Early Proteins: Evidence that ICP 4 Is Associated with Progeny Virus DNA Randall, R. E.; Dinwoodie, N. Journal of General Virology, Vol. 67, Issue 10 https://doi.org/10.1099/0022-1317-67-10-2163	journal	October 1986
Nascent pre-mRNA transcripts are associated with nuclear regions enriched in splicing factors. Huang, S.; Spector, D. L. Genes & Development, Vol. 5, Issue 12a https://doi.org/10.1101/gad.5.12a.2288	journal	December 1991
Dynamics and interactions of parvoviral NS1 protein in the nucleus Ihalainen, Teemu O.; Niskanen, Einari A.; Jylhävä, Juulia Cellular Microbiology, Vol. 9, Issue 8 https://doi.org/10.1111/j.1462-5822.2007.00926.x	journal	August 2007
Germline P Granules Are Liquid Droplets That Localize by Controlled Dissolution/Condensation Brangwynne, C. P.; Eckmann, C. R.; Courson, D. S. Science, Vol. 324, Issue 5935 https://doi.org/10.1126/science.1172046	journal	May 2009
Herpes Simplex Virus 1 Infection Induces Activation and Subsequent Inhibition of the IFI16 and NLRP3 Inflammasomes Johnson, K. E.; Chikoti, L.; Chandran, B. Journal of Virology, Vol. 87, Issue 9 https://doi.org/10.1128/JVI.00082-13	journal	February 2013
Nuclear Marginalization of Host Cell Chromatin Associated with Expansion of Two Discrete Virus-Induced Subnuclear Compartments during Baculovirus Infection Nagamine, T.; Kawasaki, Y.; Abe, A. Journal of Virology, Vol. 82, Issue 13 https://doi.org/10.1128/JVI.00490-08	journal	April 2008
The C Terminus of the Large Tegument Protein pUL36 Contains Multiple Capsid Binding Sites That Function Differently during Assembly and Cell Entry of Herpes Simplex Virus Schipke, J.; Pohlmann, A.; Diestel, R. Journal of Virology, Vol. 86, Issue 7 https://doi.org/10.1128/JVI.06432-11	journal	January 2012
Genome Replication and Postencapsidation Functions Mapping to the Nonstructural Gene Restrict the Host Range of a Murine Parvovirus in Human Cells Rubio, Mari-Paz; Guerra, Susana; Almendral, José M. Journal of Virology, Vol. 75, Issue 23 https://doi.org/10.1128/JVI.75.23.11573-11582.2001	journal	December 2001
Herpesvirus Entry: an Update Spear, P. G.; Longnecker, R. Journal of Virology, Vol. 77, Issue 19 https://doi.org/10.1128/JVI.77.19.10179-10185.2003	journal	September 2003
Recruitment of Herpes Simplex Virus Type 1 Transcriptional Regulatory Protein ICP4 into Foci Juxtaposed to ND10 in Live, Infected Cells Everett, R. D.; Sourvinos, G.; Orr, A. Journal of Virology, Vol. 77, Issue 6 https://doi.org/10.1128/JVI.77.6.3680-3689.2003	journal	March 2003
Herpes Simplex Virus 1 UL31 and UL34 Gene Products Promote the Late Maturation of Viral Replication Compartments to the Nuclear Periphery Simpson-Holley, M.; Baines, J.; Roller, R. Journal of Virology, Vol. 78, Issue 11 https://doi.org/10.1128/JVI.78.11.5591-5600.2004	journal	May 2004
Formation of Nuclear Foci of the Herpes Simplex Virus Type 1 Regulatory Protein ICP4 at Early Times of Infection: Localization, Dynamics, Recruitment of ICP27, and Evidence for the De Novo Induction of ND10-Like Complexes Everett, Roger D.; Sourvinos, George; Leiper, Claire Journal of Virology, Vol. 78, Issue 4 https://doi.org/10.1128/JVI.78.4.1903-1917.2004	journal	February 2004
From Hypothesis to Mechanism: Uncovering Nuclear Pore Complex Links to Gene Expression Burns, L. T.; Wente, S. R. Molecular and Cellular Biology, Vol. 34, Issue 12 https://doi.org/10.1128/MCB.01730-13	journal	March 2014
Herpes Simplex Virus Type 1 Entry into Host Cells: Reconstitution of Capsid Binding and Uncoating at the Nuclear Pore Complex In Vitro Ojala, Päivi M.; Sodeik, Beate; Ebersold, Melanie W. Molecular and Cellular Biology, Vol. 20, Issue 13 https://doi.org/10.1128/MCB.20.13.4922-4931.2000	journal	July 2000
Preexisting nuclear architecture defines the intranuclear location of herpesvirus DNA replication structures. de Bruyn Kops, A.; Knipe, D. M. Journal of Virology, Vol. 68, Issue 6 https://doi.org/10.1128/jvi.68.6.3512-3526.1994	journal	January 1994
Formation of herpes simplex virus type 1 replication compartments by transfection: requirements and localization to nuclear domain 10. Lukonis, C. J.; Weller, S. K. Journal of virology, Vol. 71, Issue 3 https://doi.org/10.1128/jvi.71.3.2390-2399.1997	journal	January 1997
Herpesvirus Replication Compartments Originate with Single Incoming Viral Genomes Kobiler, O.; Brodersen, P.; Taylor, M. P. mBio, Vol. 2, Issue 6 https://doi.org/10.1128/mBio.00278-11	journal	December 2011
Viral DNA Sensors IFI16 and Cyclic GMP-AMP Synthase Possess Distinct Functions in Regulating Viral Gene Expression, Immune Defenses, and Apoptotic Responses during Herpesvirus Infection Diner, Benjamin A.; Lum, Krystal K.; Toettcher, Jared E. mBio, Vol. 7, Issue 6 https://doi.org/10.1128/mBio.01553-16	journal	November 2016
Nuclear Herpesvirus Capsid Motility Is Not Dependent on F-Actin Bosse, Jens B.; Virding, Stina; Thiberge, Stephan Y. mBio, Vol. 5, Issue 5 https://doi.org/10.1128/mBio.01909-14	journal	October 2014
Mapping eGFP Oligomer Mobility in Living Cell Nuclei Dross, Nicolas; Spriet, Corentin; Zwerger, Monika PLoS ONE, Vol. 4, Issue 4 https://doi.org/10.1371/journal.pone.0005041	journal	April 2009
Parvovirus Induced Alterations in Nuclear Architecture and Dynamics Ihalainen, Teemu O.; Niskanen, Einari A.; Jylhävä, Juulia PLoS ONE, Vol. 4, Issue 6 https://doi.org/10.1371/journal.pone.0005948	journal	June 2009
Definition of Herpes Simplex Virus Type 1 Helper Activities for Adeno-Associated Virus Early Replication Events Alazard-Dany, Nathalie; Nicolas, Armel; Ploquin, Aurélie PLoS Pathogens, Vol. 5, Issue 3 https://doi.org/10.1371/journal.ppat.1000340	journal	March 2009
The Herpes Simplex Virus Protein pUL31 Escorts Nucleocapsids to Sites of Nuclear Egress, a Process Coordinated by Its N-Terminal Domain Funk, Christina; Ott, Melanie; Raschbichler, Verena PLOS Pathogens, Vol. 11, Issue 6 https://doi.org/10.1371/journal.ppat.1004957	journal	June 2015
Design stars: how small DNA viruses remodel the host nucleus Jiang, Mengxi; Imperiale, Michael J. Future Virology, Vol. 7, Issue 5 https://doi.org/10.2217/fvl.12.38	journal	May 2012
Actin in Herpesvirus Infection Roberts, Kari L.; Baines, Joel D. Viruses, Vol. 3, Issue 4 https://doi.org/10.3390/v3040336	journal	April 2011
The Role of Nuclear Antiviral Factors against Invading DNA Viruses: The Immediate Fate of Incoming Viral Genomes Komatsu, Tetsuro; Nagata, Kyosuke; Wodrich, Harald Viruses, Vol. 8, Issue 10 https://doi.org/10.3390/v8100290	journal	October 2016
The dynamic pathway of nuclear RNA in eukaryotes Sheinberger, Jonathan; Shav-Tal, Yaron Nucleus, Vol. 4, Issue 3 https://doi.org/10.4161/nucl.24434	journal	May 2013

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