Annexation of the interchromosomal space during viral infection

Abstract

The nucleus is known to be compartmentalized into units of function1, but the processes leading to the spatial organization of chromosomes and nuclear compartments are not yet well defined. Here we report direct quantitative analysis of the global structural perturbations of interphase chromosome and interchromosome domain distribution caused by infection with herpes simplex virus-1 (HSV-1). Our results show that the peripheral displacement of host chromosomes that correlates with expansion of the viral replication compartment (VRC)2,3,4,5 is coupled to a twofold increase in nuclear volume. Live cell dynamic measurements suggest that viral compartment formation is driven by the functional activity of viral components and underscore the significance of spatial regulation of nuclear activities.

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Figure 1: The H2B–GFP label distributes at the nuclear periphery in infected cells and correlates with electron-dense chromatin regions.
Figure 2: Interchromosomal space is first annexed and then expanded by VRCs in HSV-1-infected cells.
Figure 3: Host chromatin is dynamically compressed during the third stage of HSV-1 infection.

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Acknowledgements

We thank M. R. Wood for his great technical expertise with the electron microscopy study, R. D. Shelby for technical assistance and Y. Usson for making available Edit3D and Ana3D software. This work was supported by grants from the National Institute of General Medical Sciences, GM39068 (K.F.S.) and the National Institute for Allergy and Infectious Disease, AI30627 and Novartis (P.G.).

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Correspondence to Peter Ghazal or Kevin F. Sullivan.

Supplementary information

Movie 1

Biogenesis of a viral replication compartment within the nucleus (MOV 3006 kb)

Movie 2

Annexation and expansion of the viral replication compartment in HSV-1 infected cells. (MOV 3186 kb)

Description of movies (PDF 12 kb)

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Monier, K., Armas, J., Etteldorf, S. et al. Annexation of the interchromosomal space during viral infection. Nat Cell Biol 2, 661–665 (2000). https://doi.org/10.1038/35023615

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