Direct evidence for intracellular anterograde co-transport of M-PMV Gag and Env on microtubules

Pereira, Lara; Clark, Jasmine; Grznarova, Petra; Wen, Xin; LaCasse, Rachel; Ruml, Tomáš; Spearman, Paul; Hunter, Eric

doi:10.1016/j.virol.2013.11.006

Cited by 17 publications

(24 citation statements)

References 39 publications

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“…Specific mutations in MA abolish both the interaction and the localization of M-PMV to the assembly sites in a similar manner to the silencing of DYNLT1 (Vlach et al, 2008). M-PMV Env and Gag co-localize at the MTOC and are cotransported in an anterograde manner (Pereira et al, 2014;Sfakianos & Hunter, 2003).…”

Section: Retroviruses and Microtubule-associated Motor Proteinsmentioning

confidence: 93%

“…The model foamy virus is prototype foamy virus (PFV) that was isolated from an African cancer patient. (Pereira et al, 2014;Sfakianos & Hunter, 2003). Overexpression of a dominant negative peptide of the p150 Glued subunit of dynactin, which abolishes the activity of dynein, blocks the association of PFV PIC with the MTOC.…”

Section: Retroviruses and Microtubule-associated Motor Proteinsmentioning

confidence: 99%

“…When cytoskeleton disruptive drugs were used, the anterograde transport of M-PMV Gag and Env was interrupted (Pereira et al, 2014), suggesting that kinesin might mediate trafficking of the newly formed viral particle from the MTOC to the plasma membrane ( Figure 1c). The M-MPV genomic RNA (gRNA) also has to arrive to the assembly site; this is mediated by nuclear export elements present in the gRNA that govern the trafficking behavior of the genomes (Pocock, Becker, Swanson, Ahlquist, & Sherer, 2016).…”

Section: Masonmentioning

confidence: 99%

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Retroviruses and microtubule-associated motor proteins

Arriagada

2017

Cellular Microbiology

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Retroviruses are obligate intracellular parasites of eukaryotic cells. After reverse transcription, the viral DNA contained in the preintegration complex is delivered to the nucleus of the host cell, where it integrates. Before reaching the nucleus, the incoming particle and the preintegration complex must travel throughout the cytoplasm. Likewise, the newly synthesized viral proteins and viral particles must transit the cytoplasm during exit. The cytoplasm is a crowded environment, and simple diffusion is difficult. Therefore, viruses have evolved to utilize the cellular mechanisms of movement through the cytoplasm, where microtubules are the roads, and the ATP-dependent motors dynein and kinesin are the vehicles for retrograde and anterograde trafficking. This review will focus on how different retroviruses (Mazon-Pfizer monkey virus, prototype foamy virus, bovine immunodeficiency virus, human immunodeficiency virus type 1, and murine leukemia virus) have subjugated the microtubule-associated motor proteins for viral replication. Although there have been advances in our understanding of how retroviruses move along microtubules, the strategies are different among them. Thus, a better understanding of the mechanisms used by each retrovirus to functionally subvert microtubule motor proteins will provide important clues in the design of new antiretroviral drugs that can specifically disrupt intracellular viral trafficking.

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Section: Retroviruses and Microtubule-associated Motor Proteinsmentioning

confidence: 93%

Section: Retroviruses and Microtubule-associated Motor Proteinsmentioning

confidence: 99%

Section: Masonmentioning

confidence: 99%

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Retroviruses and microtubule-associated motor proteins

Arriagada

2017

Cellular Microbiology

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“…Dynamic intracellular processes, such as viral and bacterial infection (Chenouard et al, 2009a;Brandenburg and Zhuang, 2007;Sun et al, 2013;Mercer et al, 2010;Li et al, 2017;Pereira et al, 2014;Ewers et al, 2005), vesicular trafficking (Siebrasse et al, 2016;Aoyama et al, 2017;Gramlich and Klyachko, 2017;Jandt et al, 2011;Jandt and Zeng, 2012;Loerke et al, 2009), membrane receptors dynamics (Jaqaman et al, 2016;Sergé et al, 2008;Block et al, 2016;Saxton and Jacobson, 1997), cytoskeletal rearrangement (Applegate et al, 2011;Akhmanova and Steinmetz, 2008), focal adhesion reorganization (Berginski et al, 2011), gene transcription (Sinha et al, 2010), and genome maintenance (Agarwal et al, 2011) are important for many clinically relevant fields of study including immune regulation, metabolic disorders, infectious diseases, and cancer. In all of these cases, diverse individual sub-resolution 'particles' (e.g.…”

Section: Description Of the Problemmentioning

confidence: 99%

“…Example use-case using real-life imaging data: treatment with Nocodazole drastically reduces Gagcontaining viral particles during M-PMV viral assembly. M-PMV producing, rhesus macaques CMMT cells were co-transfected with pSARM-GagGFP-M100A and p-mCherry-Tubulin to visualize the cytoplasmic assembly and trafficking of immature viral particles (Clark et al, 2013;Pereira et al, 2012;Pereira et al, 2014). 7 hr post-transfection cells were either mock-treated (Untreated) or treated with Nocodazole for 1 hour (Treated), before microscopic observation under 60X magnification using a Delta vision deconvolution fluorescence microscope (Applied Precision Inc., Issaquah, WA), equipped with a Cool Snap CCD camera.…”

Section: Figurementioning

confidence: 99%

OMEGA: a software tool for the management, analysis, and dissemination of intracellular trafficking data that incorporates motion type classification and quality control

Rigano

Galli

Clark

et al. 2018

Preprint

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MOTIVATIONParticle tracking coupled with time-lapse microscopy is critical for understanding the dynamics of intracellular processes of clinical importance. Spurred on by advances in the spatiotemporal resolution of microscopy and automated computational methods, this field is increasingly amenable to multi-dimensional high-throughput data collection schemes (Snijder et al., 2012). Typically, complex particle tracking datasets generated by individual laboratories are produced with incompatible methodologies that preclude comparison to each other. There is therefore an unmet need for data management systems that facilitate data standardization, meta-analysis, and structured data dissemination. The integration of analysis, visualization, and quality control capabilities into such systems would eliminate the need for manual transfer of data to diverse downstream analysis tools. At the same time, it would lay the foundation for shared trajectory data, particle tracking, and motion analysis standards.RESULTSHere, we present Open Microscopy Environment inteGrated Analysis (OMEGA), a cross-platform data management, analysis, and visualization system, for particle tracking data, with particular emphasis on results from viral and vesicular trafficking experiments. OMEGA provides intuitive graphical interfaces to implement integrated particle tracking and motion analysis workflows while providing easy to use facilities to automatically keep track of error propagation, harvest data provenance and ensure the persistence of analysis results and metadata. Specifically, OMEGA: 1) imports image data and metadata from data management tools such as the Open Microscopy Environment Remote Objects (OMERO; Allan et al., 2012); 2) tracks intracellular particles movement; 3) facilitates parameter optimization and trajectory results inspection and validation; 4) performs downstream trajectory analysis and motion type classification; 5) estimates the uncertainty propagating through the motion analysis pipeline; and, 6) facilitates storage and dissemination of analysis results, and analysis definition metadata, on the basis of our newly proposed FAIRsharing.org complainant Minimum Information About Particle Tracking Experiments (MIAPTE; Rigano and Strambio-De-Castillia, 2016; 2017) guidelines in combination with the OME-XML data model (Goldberg et al., 2005). In so doing, OMEGA maintains a persistent link between raw image data, intermediate analysis steps, the overall analysis output, and all necessary metadata to repeat the analysis process and reproduce its results.Availability and implementationOMEGA is a cross-platform, open-source software developed in Java. Source code and cross-platform binaries are freely available on GitHub at https://github.com/OmegaProject/Omega (doi: 10.5281/zenodo.2535523), under the GNU General Public License v.3.Contactcaterina.strambio@umassmed.edu and alex.rigano@umassmed.eduSupplementary informationSupplementary Material is available at BioRxiv.org

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Evidence for the role of Rab11-positive recycling endosomes as intermediates in coronavirus egress from epithelial cells

Saraste

Enyioko

Dale

et al. 2022

Histochem Cell Biol

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After their assembly by budding into the lumen of the intermediate compartment (IC) at the endoplasmic reticulum (ER)–Golgi interface, coronaviruses (CoVs) are released from their host cells following a pathway that remains poorly understood. The traditional view that CoV exit occurs via the constitutive secretory route has recently been questioned by studies suggesting that this process involves unconventional secretion. Here, using the avian infectious bronchitis virus (IBV) as a well-established model virus, we have applied confocal microscopy to investigate the pathway of CoV egress from epithelial Vero cells. We report a novel effect of IBV infection on cellular endomembranes, namely, the compaction of the pericentrosomal endocytic recycling compartment (ERC) defined by the GTPase Rab11, which coincides with the previously described Golgi fragmentation, as well as virus release. Despite Golgi disassembly, the IC elements containing the major IBV membrane protein (M)—which mostly associates with newly formed virus particles—maintain their close spatial connection with the Rab11-positive endocytic recycling system. Moreover, partial colocalization of the M protein with Rab11 was observed, whereas M displayed negligible overlap with LAMP-1, indicating that IBV egress does not occur via late endosomes or lysosomes. Synchronization of virus release using temperature-shift protocols was accompanied by increased colocalization of M and Rab11 in vesicular and vacuolar structures in the pericentrosomal region and at the cell periphery, most likely representing IBV-containing transport carriers. In conclusion, these results add CoVs to the growing list of viruses exploiting the endocytic recycling apparatus defined by Rab11 for their assembly and/or release.

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Direct evidence for intracellular anterograde co-transport of M-PMV Gag and Env on microtubules

Cited by 17 publications

References 39 publications

Retroviruses and microtubule-associated motor proteins

Retroviruses and microtubule-associated motor proteins

OMEGA: a software tool for the management, analysis, and dissemination of intracellular trafficking data that incorporates motion type classification and quality control

Evidence for the role of Rab11-positive recycling endosomes as intermediates in coronavirus egress from epithelial cells

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