A novel function for a ubiquitous plant enzyme pectin methylesterase: the host‐cell receptor for the tobacco mosaic virus movement protein

Dorokhov, Yu. L.; Mäkinen, Kristiina; Frolova, Olga; Merits, Andres; Saarinen, Jyrki; Kalkkinen, Nisse; Atabekov, J.G.; Saarma, Märt

doi:10.1016/s0014-5793(99)01447-7

Cited by 170 publications

(98 citation statements)

References 24 publications

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“…In this regard, it may be significant that calreticulin is not the only ER-associated protein that interacts with TMV MP. Indeed, TMV MP has been shown to interact with PME (Dorokhov et al, 1999;Chen et al, 2000), suggesting that binding to the host cell factors containing signal sequences may represent a general strategy employed by TMV MP to enter the ER secretory pathway; because ER strands span plasmodesmata (Ding et al, 1992b), TMV MP may utilize its association with the ER for transport to plasmodesmata. Obviously, a more active role for calreticulin in viral movement cannot be excluded.…”

Section: Discussionmentioning

confidence: 99%

“…Figure 4A shows the interaction between TMV MP and full-length AtCRT1 (lane 1). No interaction was observed between lamin C, known as a nonspecific activator in the two-hybrid system (Bartel et al, 1993), and calreticulin ( Finally, the binding of calreticulin to TMV MP was examined directly using a renatured-blot overlay assay for protein-protein interactions (Dorokhov et al, 1999;Chen et al, 2000). In this approach, calreticulincontaining cell extract is electrophoresed, immobilized on a polyvinylidene difluoride membrane by electroblotting, reacted with purified TMV MP or with an unrelated protein, e.g.…”

Section: Calreticulin-tmv Mp Interaction In Vivo and In Vitromentioning

confidence: 99%

“…To date, MP has been shown to bind TMV RNA (Citovsky et al, 1990(Citovsky et al, , 1992, associate with the cytoskeleton (Heinlein et al, 1995;McLean et al, 1995;Boyko et al, 2000) and endoplasmic reticulum (ER; Heinlein et al, 1998;Reichel and Beachy, 1999), target to plasmodesmata within plant cell walls (Tomenius et al, 1987;Ding et al, 1992a), increase plasmodesmal permeability (Wolf et al, 1989;Waigmann et al, 1994), and undergo negative regulation by phosphorylation (Citovsky et al, 1993;Waigmann et al, 2000;Trutnyeva et al, 2005). To perform many of these functions, TMV MP most likely cooperates with different cellular factors, some of which, such as cell wall pectin methylesterases (PME; Dorokhov et al, 1999;Chen et al, 2000), microtubules (MTs) and actin filaments (Heinlein et al, 1995;McLean et al, 1995;Boyko et al, 2000), and a RIO protein kinase (Yoshioka et al, 2004), are known, while others remain to be discovered. It would be especially interesting to determine whether cellular proteins exist that not only recognize TMV MP but also coreside with it within plasmodesmata.…”

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Effects of Calreticulin on Viral Cell-to-Cell Movement

et al. 2005

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Cell-to-cell tobacco mosaic virus movement protein (TMV MP) mediates viral spread between the host cells through plasmodesmata. Although several host factors have been shown to interact with TMV MP, none of them coresides with TMV MP within plasmodesmata. We used affinity purification to isolate a tobacco protein that binds TMV MP and identified it as calreticulin. The interaction between TMV MP and calreticulin was confirmed in vivo and in vitro, and both proteins were shown to share a similar pattern of subcellular localization to plasmodesmata. Elevation of the intracellular levels of calreticulin severely interfered with plasmodesmal targeting of TMV MP, which, instead, was redirected to the microtubular network. Furthermore, in TMV-infected plant tissues overexpressing calreticulin, the inability of TMV MP to reach plasmodesmata substantially impaired cell-to-cell movement of the virus. Collectively, these observations suggest a functional relationship between calreticulin, TMV MP, and viral cell-to-cell movement.Following initial infection (usually by mechanical inoculation), many plant viruses, such as tobacco mosaic virus (TMV), spread from cell to cell through plasmodesmata (for review, see Heinlein, 2002;Waigmann et al., 2004), presumably utilizing the existing cellular pathways of plasmodesmal transport. In the case of TMV, this virus encodes a specific cell-to-cell movement protein (MP), which mediates the transport of the viral genomic RNA through plasmodesmata (Deom et al., 1987). To date, MP has been shown to bind TMV RNA (Citovsky et al., 1990(Citovsky et al., , 1992, associate with the cytoskeleton (Heinlein et al., 1995;McLean et al., 1995;Boyko et al., 2000) and endoplasmic reticulum (ER; Heinlein et al., 1998;Reichel and Beachy, 1999), target to plasmodesmata within plant cell walls (Tomenius et al., 1987;Ding et al., 1992a), increase plasmodesmal permeability (Wolf et al., 1989;Waigmann et al., 1994), and undergo negative regulation by phosphorylation (Citovsky et al., 1993;Waigmann et al., 2000;Trutnyeva et al., 2005). To perform many of these functions, TMV MP most likely cooperates with different cellular factors, some of which, such as cell wall pectin methylesterases (PME; Dorokhov et al., 1999;Chen et al., 2000), microtubules (MTs) and actin filaments (Heinlein et al., 1995;McLean et al., 1995;Boyko et al., 2000), and a RIO protein kinase (Yoshioka et al., 2004), are known, while others remain to be discovered. It would be especially interesting to determine whether cellular proteins exist that not only recognize TMV MP but also coreside with it within plasmodesmata.Using TMV MP as specific ligand in a biochemical purification protocol, we showed that it interacts with plant calreticulin. Calreticulin is a Ca 21 -sequestering protein that is highly conserved between different species, including plants ( Nelson et al., 1997; Borisjuk et al., 1998, and refs. therein;Michalak et al., 1998). Functionally, calreticulin is involved in Ca 21 storage and signaling, chaperone activity, cell ad...

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Section: Discussionmentioning

confidence: 99%

Section: Calreticulin-tmv Mp Interaction In Vivo and In Vitromentioning

confidence: 99%

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Effects of Calreticulin on Viral Cell-to-Cell Movement

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“…PMEs produced by plants take part in important physiological processes, such as microsporogenesis, pollen growth, seed germination, root development, polarity of leaf growth, stem elongation, fruit ripening, and loss of tissue integrity (Tieman and Handa, 1994;Wen et al, 1999;Micheli et al, 2000;Pilling et al, 2000;Micheli, 2001;Pilling et al, 2004). They have also been reported to play a role in response to fungal pathogens (Wietholter et al, 2003) and are required for the systemic spread of Tobacco mosaic virus through the plant (Dorokhov et al, 1999;Chen et al, 2000;Chen and Citovsky, 2003). PMEs are not only produced by plants but also by microbial pathogens (De Lorenzo et al, 1997) and by symbiotic microorganisms during their interactions with plants (Lievens et al, 2002).…”

Section: Introductionmentioning

confidence: 99%

Structural Basis for the Interaction between Pectin Methylesterase and a Specific Inhibitor Protein

Matteo¹,

Giovane

Raiola³

et al. 2005

Plant Cell

201

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Pectin, one of the main components of the plant cell wall, is secreted in a highly methyl-esterified form and subsequently deesterified in muro by pectin methylesterases (PMEs). In many developmental processes, PMEs are regulated by either differential expression or posttranslational control by protein inhibitors (PMEIs). PMEIs are typically active against plant PMEs and ineffective against microbial enzymes. Here, we describe the three-dimensional structure of the complex between the most abundant PME isoform from tomato fruit (Lycopersicon esculentum) and PMEI from kiwi (Actinidia deliciosa) at 1.9-Å resolution. The enzyme folds into a right-handed parallel b-helical structure typical of pectic enzymes. The inhibitor is almost all helical, with four long a-helices aligned in an antiparallel manner in a classical up-and-down fourhelical bundle. The two proteins form a stoichiometric 1:1 complex in which the inhibitor covers the shallow cleft of the enzyme where the putative active site is located. The four-helix bundle of the inhibitor packs roughly perpendicular to the main axis of the parallel b-helix of PME, and three helices of the bundle interact with the enzyme. The interaction interface displays a polar character, typical of nonobligate complexes formed by soluble proteins. The structure of the complex gives an insight into the specificity of the inhibitor toward plant PMEs and the mechanism of regulation of these enzymes.

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“…So far, a cell wall-associated pectin methyl esterase (PME; Dorokhov et al, 1999;Tzfira et al, 2000) was shown to specifically interact with TMV-MP30. Also, binding studies of MP30 with cell fractions enriched in plasmodesmal components indicate the presence of potential receptor molecules mediating protein movement via plasmodesmata (Kragler et al, 1998).…”

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MPB2C, a Microtubule-Associated Plant Protein Binds to and Interferes with Cell-to-Cell Transport of Tobacco Mosaic Virus Movement Protein

et al. 2003

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The movement protein of tobacco mosaic virus, MP30, mediates viral cell-to-cell transport via plasmodesmata. The complex MP30 intra-and intercellular distribution pattern includes localization to the endoplasmic reticulum, cytoplasmic bodies, microtubules, and plasmodesmata and likely requires interaction with plant endogenous factors. We have identified and analyzed an MP30-interacting protein, MPB2C, from the host plant Nicotiana tabacum. MPB2C constitutes a previously uncharacterized microtubule-associated protein that binds to and colocalizes with MP30 at microtubules. In vivo studies indicate that MPB2C mediates accumulation of MP30 at microtubules and interferes with MP30 cell-to-cell movement. In contrast, intercellular transport of a functionally enhanced MP30 mutant, which does not accumulate and colocalize with MP30 at microtubules, is not impaired by MPB2C. Together, these data support the concept that MPB2C is not required for MP30 cell-to-cell movement but may act as a negative effector of MP30 cell-to-cell transport activity.Plant viruses produce movement proteins required to mediate cell-to-cell spread of the viral genomic information via plasmodesmata (Lucas, 1995;Lazarowitz and Beachy, 1999;McLean and Zambryski, 2000;Tzfira et al., 2000;Haywood et al., 2002;Heinlein, 2002). Tobacco mosaic virus (TMV), a virus with a (ϩ) single-stranded RNA genome encodes one of the most extensively studied movement proteins, MP30. Several biochemical and cell biological features of MP30 were revealed: MP30 binds cooperatively single-stranded nucleic acids (Citovsky et al., 1990), interacts with the tubulin-and actin-based cytoskeleton (Heinlein et al., 1995;McLean et al., 1995), associates to the endoplasmic reticulum (ER; Heinlein et al., 1998;Reichel and Beachy, 1998;Mas and Beachy, 1999;Gillespie et al., 2002), and increases the size exclusion limit of plasmodesmata (Wolf et al., 1989;Waigmann et al., 1994). In the current model, MP30 is proposed to form complexes with genomic TMV-RNA (vRNA) and to move these vRNA-protein complexes from ER-associated sites of synthesis throughout the cell via the cytoskeletal network toward plasmodesmata. There, MP30 induces an increase in plasmodesmal size exclusion limit and facilitates the transport of the vRNA-MP30 complex through the enlarged plasmodesmal channels into adjacent cells (Lazarowitz and Beachy, 1999;Tzfira et al., 2000;Haywood et al., 2002;Heinlein, 2002). In line with this model, microtubules have been functionally implicated in guiding vRNA-MP30 complexes toward plasmodesmata (Mas and Beachy, 2000; Boyko et al., 2000a Boyko et al., , 2000b. However, an alternate, non-movement-promoting role of microtubules in providing a route toward an MP30 degradation site was suggested (Padgett et al., 1996;Mas and Beachy, 1999;Reichel and Beachy, 2000). This model is supported by the observation that TMV was able to spread in tissues with functionally impaired microtubules and by studies performed with a mutant variant of MP30, MP R3 with strongly decreased affinity...

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A novel function for a ubiquitous plant enzyme pectin methylesterase: the host‐cell receptor for the tobacco mosaic virus movement protein

Cited by 170 publications

References 24 publications

Effects of Calreticulin on Viral Cell-to-Cell Movement

Effects of Calreticulin on Viral Cell-to-Cell Movement

Structural Basis for the Interaction between Pectin Methylesterase and a Specific Inhibitor Protein

MPB2C, a Microtubule-Associated Plant Protein Binds to and Interferes with Cell-to-Cell Transport of Tobacco Mosaic Virus Movement Protein

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