Disruption of Microtubule Organization and Centrosome Function by Expression of<i>Tobacco Mosaic Virus</i>Movement Protein

Ferralli, Jacqueline; Ashby, J.; Fasler, Monika; Boyko, Vitaly; Heinlein, Manfred

doi:10.1128/jvi.00254-06

Cited by 51 publications

(56 citation statements)

References 96 publications

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“…Recently, it was determined that MP stabilizes microtubules also upon expression in mammalian cells (33). Modulation of microtubule dynamic instability is a common feature of structural MAPs (83,91,100) and is thought to involve the reduction of interdimer charge-repulsion forces due to binding of MAPs to the microtubule surface (3,20).…”

Section: Discussionmentioning

confidence: 99%

Tobacco Mosaic Virus Movement Protein Functions as a Structural Microtubule-Associated Protein

Ashby

Boutant

Seemanpillai

et al. 2006

J Virol

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The cell-to-cell spread of Tobacco mosaic virus infection depends on virus-encoded movement protein (MP), which is believed to form a ribonucleoprotein complex with viral RNA (vRNA) and to participate in the intercellular spread of infectious particles through plasmodesmata. Previous studies in our laboratory have provided evidence that the vRNA movement process is correlated with the ability of the MP to interact with microtubules, although the exact role of this interaction during infection is not known. Here, we have used a variety of in vivo and in vitro assays to determine that the MP functions as a genuine microtubule-associated protein that binds microtubules directly and modulates microtubule stability. We demonstrate that, unlike MP in whole-cell extract, microtubule-associated MP is not ubiquitinated, which strongly argues against the hypothesis that microtubules target the MP for degradation. In addition, we found that MP interferes with kinesin motor activity in vitro, suggesting that microtubule-associated MP may interfere with kinesin-driven transport processes during infection.

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Section: Discussionmentioning

confidence: 99%

Tobacco Mosaic Virus Movement Protein Functions as a Structural Microtubule-Associated Protein

Ashby

Boutant

Seemanpillai

et al. 2006

J Virol

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“…We cannot exclude the possibility that ABD2:GFP binding to actin filaments interferes with MP:RFP binding. However, since other studies have demonstrated that the filaments to which MP binds in plant and mammalian cells are microtubules (Heinlein et al, 1995(Heinlein et al, , 1998Boyko et al, 2000aBoyko et al, , 2000bAshby et al, 2006;Ferralli et al, 2006), this possibility appears unlikely. Our observation is consistent with the finding that MP does not bind to actin filaments in mammalian cells (Ferralli et al, 2006), and actin is highly conserved between plants and mammals.…”

Section: Mp Does Not Align To Actin Filamentsmentioning

confidence: 83%

“…However, since other studies have demonstrated that the filaments to which MP binds in plant and mammalian cells are microtubules (Heinlein et al, 1995(Heinlein et al, , 1998Boyko et al, 2000aBoyko et al, , 2000bAshby et al, 2006;Ferralli et al, 2006), this possibility appears unlikely. Our observation is consistent with the finding that MP does not bind to actin filaments in mammalian cells (Ferralli et al, 2006), and actin is highly conserved between plants and mammals. The lack of alignment of MP:RFP to ABD2:GFP-tagged actin filaments in living cells does not confirm the previous observations by McLean et al (1995), who showed the alignment of antibody-stained MP to phalloidin-rhodamine-labeled filaments in chemically fixed TMV-infected protoplasts.…”

Section: Mp Does Not Align To Actin Filamentsmentioning

confidence: 83%

Inhibition of Tobacco Mosaic Virus Movement by Expression of an Actin-Binding Protein

et al. 2009

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The tobacco mosaic virus (TMV) movement protein (MP) required for the cell-to-cell spread of viral RNA interacts with the endoplasmic reticulum (ER) as well as with the cytoskeleton during infection. Whereas associations of MP with ER and microtubules have been intensely investigated, research on the role of actin has been rather scarce. We demonstrate that Nicotiana benthamiana plants transgenic for the actin-binding domain 2 of Arabidopsis (Arabidopsis thaliana) fimbrin (AtFIM1) fused to green fluorescent protein (ABD2:GFP) exhibit a dynamic ABD2:GFP-labeled actin cytoskeleton and myosin-dependent Golgi trafficking. These plants also support the movement of TMV. In contrast, both myosin-dependent Golgi trafficking and TMV movement are dominantly inhibited when ABD2:GFP is expressed transiently. Inhibition is mediated through binding of ABD2:GFP to actin filaments, since TMV movement is restored upon disruption of the ABD2:GFP-labeled actin network with latrunculin B. Latrunculin B shows no significant effect on the spread of TMV infection in either wild-type plants or ABD2:GFP transgenic plants under our treatment conditions. We did not observe any binding of MP along the length of actin filaments.Collectively, these observations demonstrate that TMV movement does not require an intact actomyosin system. Nevertheless, actin-binding proteins appear to have the potential to exert control over TMV movement through the inhibition of myosinassociated protein trafficking along the ER membrane.The mechanism by which plant viruses move from cell to cell and systemically to cause systemic infection has been the subject of intense studies (for review, see

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“…Tobacco mosaic virus (TMV) MP, for example, interacts with Arabidopsis thaliana EB1a, and dynamic MTs promote TMV spread (137,138). Other commonalities with mammalian viruses include MPs that affect centrosome function (135). Perhaps most striking about plant MTs, however, is their role in vector transmission.…”

Section: Mt Functions During Infection Of Plants Insects and Bacteriamentioning

confidence: 99%

“…A variety of plant viruses encode what are termed "movement proteins" (MPs), which are involved in the transport of viral proteins, RNAs, replication compartments, and virions (130,132). MPs have been found to bind plant MAPs, which negatively or positively regulate infection, as well as to mimic host MAP functions to stabilize plant MTs (133)(134)(135)(136). Plant MPs have also been found to interact with ϩTIPs.…”

Section: Mt Functions During Infection Of Plants Insects and Bacteriamentioning

confidence: 99%

Microtubule Regulation and Function during Virus Infection

Naghavi

Walsh

2017

J Virol

105

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Microtubules (MTs) form a rapidly adaptable network of filaments that radiate throughout the cell. These dynamic arrays facilitate a wide range of cellular processes, including the capture, transport, and spatial organization of cargos and organelles, as well as changes in cell shape, polarity, and motility. Nucleating from MT-organizing centers, including but by no means limited to the centrosome, MTs undergo rapid transitions through phases of growth, pause, and catastrophe, continuously exploring and adapting to the intracellular environment. Subsets of MTs can become stabilized in response to environmental cues, acquiring distinguishing posttranslational modifications and performing discrete functions as specialized tracks for cargo trafficking. The dynamic behavior and organization of the MT array is regulated by MT-associated proteins (MAPs), which include a subset of highly specialized plus-end-tracking proteins (ϩTIPs) that respond to signaling cues to alter MT behavior. As pathogenic cargos, viruses require MTs to transport to and from their intracellular sites of replication. While interactions with and functions for MT motor proteins are well characterized and extensively reviewed for many viruses, this review focuses on MT filaments themselves. Changes in the spatial organization and dynamics of the MT array, mediated by virus-or host-induced changes to MT regulatory proteins, not only play a central role in the intracellular transport of virus particles but also regulate a wider range of processes critical to the outcome of infection.KEYWORDS virus, cytoskeleton, microtubules, nucleation, microtubule-associated proteins, plus-end-tracking proteins T he dense cytosolic environment poses a major barrier to the free movement of macromolecules, making microtubule (MT)-based transport a critical aspect of virus replication. Indeed, almost as soon as these filaments were identified and characterized, virus particles were observed proximal to "microtubuli," with evidence that MTassociated proteins (MAPs) might mediate this association. Chemicals that disrupt MT networks, still commonly used today, were reported to suppress virus infection. Moreover, either infection or expression of viral proteins was observed to alter the organization of these networks, suggesting that MTs not only facilitated infection but were also likely to be actively manipulated by viruses. In subsequent decades an enormous body of work helped unravel how virus particles exploit MT motors to traffic within infected cells, and we direct readers to a recent review of this subject (1). Here, we discuss recent advances in our understanding of how MTs themselves are regulated and function during infection, limiting this minireview to some illustrative examples in each case. TWO ENDS TO THE STORY: THE BASICS OF MT POLARITY AND ORGANIZATIONMTs form through the polymerization of ␣/␤-tubulin heterodimers into polarized filaments that have minus and plus ends (Fig. 1A and B). MTs nucleate through minus-end seeding at MT-organizing cen...

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Disruption of Microtubule Organization and Centrosome Function by Expression ofTobacco Mosaic VirusMovement Protein

Cited by 51 publications

References 96 publications

Tobacco Mosaic Virus Movement Protein Functions as a Structural Microtubule-Associated Protein

Tobacco Mosaic Virus Movement Protein Functions as a Structural Microtubule-Associated Protein

Inhibition of Tobacco Mosaic Virus Movement by Expression of an Actin-Binding Protein

Microtubule Regulation and Function during Virus Infection

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