University of Groningen
Preface: Special issue on the physics of viral capsids
Cieplak, Marek; Roos, Wouter
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Journal of Physics-Condensed Matter
DOI:
10.1088/1361-648X/aacb6c
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Publication date: 2018
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Cieplak, M., & Roos, W. (2018). Preface: Special issue on the physics of viral capsids. Journal of Physics-Condensed Matter, 30(29), 1-3. https://doi.org/10.1088/1361-648X/aacb6c
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Special issue on the physics of viral capsids
To cite this article before publication: Marek Cieplak et al 2018 J. Phys.: Condens. Matter in press https://doi.org/10.1088/1361-648X/aacb6c
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Special Issue on the Physics of Viral Capsids
Marek Cieplak_Institute of Physics, Polish Academy of Sciences, Al. Lotników 32/46, 02-668 Warsaw,
Poland
Wouter H. Roos†
Zernike Instituut, Rijksuniversiteit Gronigen, Nijenborgh 4, 9747 AG Gronningen,
The Netherlands
_Electronic address: mc@ifpan.edu.pl
†Electronic address: w.h.roos@rug.nl
In the late 19th century infectious disease research started to shape up. These developments were further catalysed after the publication in 1898 by Martinus Beijerinck from the Polytechnische School in Delft (now Technische Universiteit Delft) about a contagium vivum fluidum [1]. He was the first to show and realize that there must be a new type of infectious agent, smaller than bacteria, that is able to reproduce in infected organisms [2]. With his publication the field of virology was born. The
contagium vivum fluidum that was discovered is the tobacco mosaic virus (TMV), responsible for
brownish spots on tobacco leaves. Crystallography and electron microscopy studies in the 1930s revealed that TMV is a rod-shaped aggregate. These experiments, where physics techniques were used to study viruses, are early examples of research in the field that is now known as Physical Virology. After the discovery of TMV a multitude of other viruses were discovered, infecting archaea, bacteria, plants and animals.
The protein shell that surrounds the genome of many viruses is known as a capsid (in Latin, capsa means a box) and can have all sorts of shapes, though the most common shape is icosahedral [3]. In addition to the capsid, a variety of eukaryotic viruses also possess a lipid envelope, which is essential for successful interactions with the host cell. Interestingly, mechanical, thermal, morphological and biological properties differ a lot between viruses, depending on the nature of the proteins (and sometimes lipids), of which the virus has self-assembled. This makes it especially interesting as objects of study to biophysicists, both from experimental and theoretical perspectives. With the advent of advanced modelling approaches, high resolution electron and atomic force microscopy techniques, native mass spectrometry and advanced fluorescence microscopy approaches over the last ~25 years, the field of Physical Virology has made a tremendous development. This was catalysed by the steady increasing input of physicists to describe virological features in a quantitative manner. This Special Issue provides a survey of current biophysical research in this area.
Despite decades of studies on viral self-assembly and disassembly these essential steps in the viral life cycle remain poorly understood and a variety of groups is working on these issues to attempt to finally elucidate the physics behind (dis)assembly. Temperature induced disassembly of cowpea chlorotic mottle virus (CCMV) was scrutinized by small angle neutron scattering and analysed using lattice models [4], whereas the influence of RNA on assembly was studied using self consistent field theory [5], coarse-grained molecular dynamics [6] and polymer field theory [7]. In this latter study it was demonstrated that there are preferences for a capsid to encapsulate linear RNA as opposed to highly branched genomes and this is explained in terms of a difference in stiffness. RNA encapsulation was also studied in terms of the spatial compactness of the viral genome. In particular this was analysed for phage MS2 and brome mosaic virus by comparing compactness of wild type genomes with that of mutated ones [8]. Electron microscopy (EM) experiments were performed to explore possibilities to encapsulate cargo into infectious bursal disease virus using an in vitro assembly/disassembly system [9]. A related EM study focused on the impact of the length of the encapsulated oligonucleotide cargo on the stability and structure of alphavirus particles [10]. Furthermore, förster resonance energy transfer was applied as a strategy to study the assembly of CCMV viruses without labelling the
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exterior of viruses, but by using fluorescently labelled DNA oligomers [11].These publications show that in a variety of recent assembly/disassembly studies the influence of cargo is a main theme.
Bozic and Podgornik [12] analyze the electrostatic signature of viruses theoretically and show that N-terminal disordered tails of the capsid proteins, responsible for aggregation of the proteins around the nucleic acids, stay positively charged even at very basic pH values. The pH dependent stability of norovirus-like particles has been explored experimentally using native mass spectrometry and EM by Pogan et al [13]. These latter studies are part of the wider research effort to study stability and mechanical properties of viruses. In this regard, Dharmavaram et al [14] argue that the capsids of certain Archaea-infecting viruses are in a smectic liquid crystalline state in which they can undergo large shape transformations while remaining stable against rupture by osmotic pressure. Using atomic force microscopy (AFM), the issue of virus stability after desiccation was scrutinised, focusing on the role of the genome and structural ions to keep triatoma virus in shape [15]. A ”virtual AFM” for numerical studies of AFM nanoindentation has been proposed by Aznar et al [16], whereas “TensorCalulator” was used to predict stress distributions in indented CCMV particles [17], a virus that serves as model system for a variety of physical virology approaches.
Finally, viral budding as well as viral fusion has been studied. Membrane vesiculation by dengue virus proteins was scrutinized, whereby residues were identified that lead to essential membrane bending stress [18]. Influenza virus fusion with the host cell membrane was scrutinised in a single-particle approach [19]. Using total internal reflection fluorescence microscopy it was demonstrated that the composition of the membrane exerts a major impact on the process.
This collection of recent work covering the physics of viruses and their capsids illustrates the fast developments in which the physical virology field moves forward. While we are increasingly better understanding viral (dis)assembly and mechanics, there remain large gaps in our knowledge. We also notice that physicists additionally turn to more complex systems by introducing and studying the effects of the lipid envelope surrounding some viruses. Overall we expect a further increase in physical virology studies in the years to come, as the power of this approach is increasingly being recognised.
References
[1] Martinus W Beijerinck 1898 Verh Kon Akad Wetensch VI: 3–21 Über ein Contagium vivum fluidum als Ursache der Flekkenkrankheit der Tabaksblätter
[2] Ab van Kammen 1999 Arch Virol Suppl., 15:1-8 Beijerinck's contribution to the virus concept-an introduction
[3] Adam Zlotnick 2004 Proc. Natl. Acad. Scie. USA vol. 101 15549–15550 Viruses and the physics of soft condensed matter
[4] Jingzhi Chen et al 2017 J. Phys.: Condens. Matter 29 474001 Investigating the thermal dissociation of viral capsid by lattice model
[5] Siyu Li et al 2018 J. Phys.: Condens. Matter 30 144002, Self consistent field theory of virus assembly.
[6] Karol Wolek and Marek Cieplak 2017 J. Phys.: Condens. Matter 29 474003, Self-assembly of model proteins into virus capsid.
[7] Siyu Li et al 2018 J. Phys.: Condens. Matter 30 044002, The effect of RNA stiffness on the self-assembly of virus particles.
[8] Anze Losdorfer Bozic et al 2018 J. Phys.: Condens. Matter 30 084006, Compactness of viral genomes: effect of disperse and localized random mutations.
[9] Elena Pascual et al 2017 J. Phys.: Condens. Matter 29 494001, Assembly/disassembly of a complex icosahedral virus to incorporate heterologous nucleic acids.
[10] Vamseedhar Rayaprolu et al 2017 J. Phys.: Condens. Matter 29 484003, Length of encapsidated cargo impacts stability and structure of in vitro assembled alphavirus core-like particles.
[11] Mark V de Ruiter et al 2018 J. Phys.: Condens. Matter 30 184002, Induced Frster resonance energy transfer by encapsulation of DNAscaffold based probes inside a plant virus based protein cage.
[12] Anze Losdorfer Bozic and Rudolf Podgornik 2018 J. Phys.: Condens. Matter 30 024001, Varieties of charge distributions in coat proteins of ssRNA+viruses.
[13] Ronja Pogan et al 2018 J. Phys.: Condens. Matter 30 064006, Norovirus-like VP1 particles exhibit isolate dependent stability profiles.
[14] S Dharmavaram et al 2018 J. Phys.: Condens. Matter 30 204004, Smectic viral capsids and the aneurysm instability.
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[15] Natalia Martn-Gonzlez et al 2018 J. Phys.: Condens. Matter 30 104001, Exploring the role of genome and structural ions in preventing viral capsid collapse during dehydration.
[16] Maria Aznar, Sergi Roca-Bonet, David Reguera (in press), Viral Nanomechanics with a Virtual Atomic Force Microscope.
[17] Olga Kononova et al 2018 J. Phys.: Condens. Matter 30 044006, TensorCalculator: exploring the evolution of mechanical stress in the CCMV capsid.
[18] Ricardo de Oliveira dos Santos Soares et al 2017 J. Phys.: Condens. Matter 29 504002, Membrane vesiculation induced by proteins of the dengue virus envelope studied by molecular dynamics simulations.
[19] Guus van der Borg et al 2018 J. Phys.: Condens.Matter 30 204005, Single-particle fusion of influenza viruses reveals complex interactions with target membranes.
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