HIV-1 requires capsid remodelling at the nuclear pore for nuclear entry and integration Article Swipe
Anabel Guedán
,
Callum D. Donaldson
,
Ophélie Cosnefroy
,
Ian A. Taylor
,
Kate N. Bishop
·
YOU?
·
· 2021
· Open Access
·
· DOI: https://doi.org/10.1101/2021.03.18.436028
YOU?
·
· 2021
· Open Access
·
· DOI: https://doi.org/10.1101/2021.03.18.436028
The capsid (CA) lattice of the HIV-1 core plays a key role during infection. From the moment the core is released into the cytoplasm, it interacts with a range of cellular factors that, ultimately, direct the pre-integration complex to the integration site. For integration to occur, the CA lattice must disassemble. Early uncoating or a failure to do so has detrimental effects on virus infectivity, indicating that an optimal stability of the viral core is crucial for infection. Here, we introduced cysteine residues into HIV-1 CA in order to induce disulphide bond formation and engineer hyper-stable mutants that are slower or unable to uncoat, and then followed their replication. From a panel of mutants, we identified three with increased capsid stability in cells and found that, whilst the M68C/E212C mutant had a 5-fold reduction in reverse transcription, two mutants, A14C/E45C and E180C, were able to reverse transcribe to approximately WT levels. Moreover, these mutants only had a 5-fold reduction in 2-LTR circle production, suggesting that not only could reverse transcription complete in hyper-stable cores, but that the nascent viral cDNA could enter the nuclear compartment. Furthermore, we observed significant levels of A14C/E45C mutant capsid in nuclear and chromatin-associated fractions implying that the hyper-stable cores themselves entered the nucleus. Immunofluorescence studies revealed that although the A14C/E45C mutant capsid reached the nuclear pore with the same kinetics as wild type capsid, it was then retained at the pore in association with Nup153. Crucially, infection with the hyper-stable mutants did not promote CPSF6 re-localisation to nuclear speckles, despite the mutant capsids being competent for CPSF6 binding. These observations suggest that hyper-stable cores are not able to uncoat, or remodel, enough to pass through or dissociate from the nuclear pore and integrate successfully. This, is turn, highlights the importance of capsid lattice flexibility for nuclear entry. In conclusion, we hypothesise that during a productive infection, a capsid remodelling step takes place at the nuclear pore that releases the core complex from Nup153, and relays it to CPSF6, which then localises it to chromatin ready for integration. AUTHOR SUMMARY The mature viral core of human immunodeficiency virus (HIV) consists of a highly organised lattice formed by capsid molecules that encloses the viral RNA and viral enzymes. This lattice is crucial during the early stages of viral replication, as it has to break down – uncoat – at the right time and place in order for the viral DNA to integrate successfully. Lentiviruses, like HIV, can infect non-dividing cells and are able to access the host cell DNA by entering the nucleus through nuclear pores. Until recently, uncoating was thought to occur in the cytoplasm as the whole core was thought too large to pass through the nuclear pore. However, lately it has been suggested that uncoating might occur at the nuclear pore or even inside the nucleus and the site of uncoating is currently hotly debated. By investigating HIV mutants with an increased lattice stability, we have shown that lattice flexibility is crucial for nuclear entry. Provocatively, we observed hyper-stable mutant capsid in nuclear and chromatin-associated fractions suggesting that uncoating is not required for nuclear entry. Nonetheless, microscopy experiments suggested that these hyper-stable mutants were retained on the inner side of the nuclear pore, and were impaired for downstream events in the nucleus, leading to a severe infectivity defect. Therefore, we believe that an essential uncoating, or capsid lattice remodelling event normally takes place at the nuclear pore.
Related Topics
Concepts
Capsid
Nuclear pore
Mutant
Cell biology
Cytoplasm
Nuclear transport
Infectivity
Biology
Reverse transcriptase
Cell nucleus
Virus
Molecular biology
Chemistry
Virology
Genetics
RNA
Gene
Metadata
- Type
- preprint
- Language
- en
- Landing Page
- https://doi.org/10.1101/2021.03.18.436028
- https://www.biorxiv.org/content/biorxiv/early/2021/03/18/2021.03.18.436028.full.pdf
- OA Status
- green
- Cited By
- 11
- References
- 89
- Related Works
- 10
- OpenAlex ID
- https://openalex.org/W3139327304
All OpenAlex metadata
Raw OpenAlex JSON
- OpenAlex ID
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https://openalex.org/W3139327304Canonical identifier for this work in OpenAlex
- DOI
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https://doi.org/10.1101/2021.03.18.436028Digital Object Identifier
- Title
-
HIV-1 requires capsid remodelling at the nuclear pore for nuclear entry and integrationWork title
- Type
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preprintOpenAlex work type
- Language
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enPrimary language
- Publication year
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2021Year of publication
- Publication date
-
2021-03-18Full publication date if available
- Authors
-
Anabel Guedán, Callum D. Donaldson, Ophélie Cosnefroy, Ian A. Taylor, Kate N. BishopList of authors in order
- Landing page
-
https://doi.org/10.1101/2021.03.18.436028Publisher landing page
- PDF URL
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https://www.biorxiv.org/content/biorxiv/early/2021/03/18/2021.03.18.436028.full.pdfDirect link to full text PDF
- Open access
-
YesWhether a free full text is available
- OA status
-
greenOpen access status per OpenAlex
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https://www.biorxiv.org/content/biorxiv/early/2021/03/18/2021.03.18.436028.full.pdfDirect OA link when available
- Concepts
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Capsid, Nuclear pore, Mutant, Cell biology, Cytoplasm, Nuclear transport, Infectivity, Biology, Reverse transcriptase, Cell nucleus, Virus, Molecular biology, Chemistry, Virology, Genetics, RNA, GeneTop concepts (fields/topics) attached by OpenAlex
- Cited by
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11Total citation count in OpenAlex
- Citations by year (recent)
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2025: 2, 2024: 5, 2022: 1, 2021: 3Per-year citation counts (last 5 years)
- References (count)
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89Number of works referenced by this work
- Related works (count)
-
10Other works algorithmically related by OpenAlex
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