Interactions among a Fimbrin, a Capping Protein, and an Actin-depolymerizing Factor in Organization of the Fission Yeast Actin Cytoskeleton

Nakano, Kentaro; Satoh, Kazuomi; Morimatsu, Akeshi; Ohnuma, Mio; Mabuchi, Issei

doi:10.1091/mbc.12.11.3515

Cited by 81 publications

(117 citation statements)

References 56 publications

(64 reference statements)

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“…Actin aggregates may function as an assembly center in the localization of integrin and other signaling molecules that are critical in the maturation of actin aggregates to functional sealing rings. L-plastin was described to be homologous with the F-actin-bundling protein fimbrin (59), and it is present in the podosomes of osteoclasts (2,60). However, its function in osteoclasts is highly unknown.…”

Section: Discussionmentioning

confidence: 99%

Regulation of Sealing Ring Formation by L-plastin and Cortactin in Osteoclasts

Sadashivaiah

Chellaiah

2010

Journal of Biological Chemistry

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The aim of this study is to identify the exact mechanism(s) by which cytoskeletal structures are modulated during bone resorption. In this study, we have shown the possible role of different actin-binding and signaling proteins in the regulation of sealing ring formation. Our analyses have demonstrated a significant increase in cortactin and a corresponding decrease in L-plastin protein levels in osteoclasts subjected to bone resorption for 18 h in the presence of RANKL, M-CSF, and native bone particles. Time-dependent changes in the localization of L-plastin (in actin aggregates) and cortactin (in the sealing ring) suggest that these proteins may be involved in the initial and maturation phases of sealing ring formation, respectively. siRNA to cortactin inhibits this maturation process but not the formation of actin aggregates. Osteoclasts treated as above but with TNF-␣ demonstrated very similar effects as observed with RANKL. Osteoclasts treated with a neutralizing antibody to TNF-␣ displayed podosome-like structures in the entire subsurface and at the periphery of osteoclast. It is possible that TNF-␣ and RANKL-mediated signaling may play a role in the early phase of sealing ring configuration (i.e. either in the disassembly of podosomes or formation of actin aggregates). Furthermore, osteoclasts treated with alendronate or ␣v reduced the formation of the sealing ring but not actin aggregates. The present study demonstrates a novel mechanistic link between L-plastin and cortactin in sealing ring formation. These results suggest that actin aggregates formed by L-plastin independent of integrin signaling function as a core in assembling signaling molecules (integrin ␣v␤3, Src, cortactin, etc.) involved in the maturation process.Osteoclasts, the multinucleated and terminally differentiated giant cells, are involved in bone resorption. The adhesion of osteoclasts to the bone during bone resorption leads to the formation of the clear zone, an actin-rich ring-like adhesion zone circumscribing an area of bone resorption. Formation of a clear zone or sealing zone (also known as the sealing ring) has been considered to be a marker of osteoclast activation and is fundamental to the process of osteoclast bone resorption. Sealing ring formation is mediated by the dynamics of the actin cytoskeleton. Distinct pathways and signaling molecules have been shown to play roles in the organization of the sealing ring during bone resorption. Our previous observations in gelsolin null (Gsn Ϫ/Ϫ ) 2 osteoclasts demonstrated that deficiency of this protein blocks podosome assembly and motility. However, the cells still exhibit sealing ring and matrix resorption (1). Therefore, Gsn Ϫ/Ϫ osteoclasts are capable of resorbing bone, but the resorbed areas are small due to the absence of podosomes and the resulting hypomotile nature of osteoclasts (1). Observations in Gsn Ϫ/Ϫ osteoclasts also suggest that the organization of the sealing ring presumably reflect changes in the role of actinbinding proteins. Spatial configurations of actin fil...

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Section: Discussionmentioning

confidence: 99%

Regulation of Sealing Ring Formation by L-plastin and Cortactin in Osteoclasts

Sadashivaiah

Chellaiah

2010

Journal of Biological Chemistry

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“…Journal of Cell Science 118 (6) stabilized F-actin structures by displacing cofilin (Nakano et al, 2001). Whether T-plastin and cofilin compete for binding to the same site on the actin filament or might indirectly influence their binding by inducing a conformational change in the actin subunit, as supported by structural and biochemical data (Hanein et al, 1998;McGough et al, 1997), remains to be experimentally evaluated.…”

Section: Discussionmentioning

confidence: 99%

Actin-filament cross-linking protein T-plastin increases Arp2/3-mediated actin-based movement

Giganti

Plastino

Janji

et al. 2005

Journal of Cell Science

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Increasing evidence suggests that actin cross-linking or bundling proteins might not only structure the cortical actin cytoskeleton but also control actin dynamics. Here, we analyse the effects of T-plastin/T-fimbrin, a representative member of an important actin-filament cross-linking protein by combining a quantitative biomimetic motility assay with biochemical and cell-based approaches. Beads coated with the VCA domain of the Wiskott/Aldrich-syndrome protein (WASP) recruit the actin-nucleating Arp2/3 complex, polymerize actin at their surface and undergo movement when placed in cell-free extracts. T-Plastin increased the velocity of VCA beads 1.5 times, stabilized actin comets and concomitantly displaced cofilin, an actin-depolymerizing protein. T-Plastin also decreased the F-actin disassembly rate and inhibited cofilin-mediated depolymerization of actin filaments in vitro. Importantly, a bundling-incompetent variant comprising the first actin-binding domain (ABD1) had similar effects. In cells, this domain induced the formation of long actin cables to which other actin-regulating proteins were recruited. Altogether, these results favor a mechanism in which binding of ABD1 controls actin turnover independently of cross-link formation. In vivo, this activity might contribute to the assembly and maintenance of the actin cytoskeleton of plasma-membrane protrusions.

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“…Calcium insensitivity could be due to poor conservation of the N-terminal calmodulin-like calcium binding domain (McCurdy and Kim, 1998;Staiger and Hussey, 2004). Calcium insensitivity was also reported for chicken fimbrin (Bretscher, 1981) and S. pombe Fim1p (Nakano et al, 2001). By contrast, plastins from mammalian cells (Namba et al, 1992;Lin et al, 1994) and Dictyostelium (Prassler et al, 1997) have been shown to be calcium sensitive.…”

Section: Fim5 Is a Bona Fide Actin Bundling Factormentioning

confidence: 98%

“…In addition, fimbrin has been shown to localize to the cortical region of the cleavage furrow in Tetrahymena pyriformis and to the cortical actin patches and the medial ring in the fission yeast S. pombe, suggesting a possible role for fimbrin in cytokinesis Shirayama and Numata, 2003;Wu and Pollard, 2005). Fission yeast fim1+ organizes actin filaments into bundles in vitro, and loss-of-function of S. pombe fim1+ increases the sensitivity of actin filaments to latrunculin A treatment (Nakano et al, 2001), suggesting that fim1+ is involved in stabilization of actin filaments in cytokinesis. Interestingly, mutation of fimbrin in Dictyostelium does not affect growth, endocytosis, exocytosis, or chemotaxis but causes a small cell phenotype (Pikzack et al, 2005).…”

Section: Introductionmentioning

confidence: 99%

ArabidopsisFIMBRIN5, an Actin Bundling Factor, Is Required for Pollen Germination and Pollen Tube Growth

et al. 2010

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Actin cables in pollen tubes serve as molecular tracks for cytoplasmic streaming and organelle movement and are formed by actin bundling factors like villins and fimbrins. However, the precise mechanisms by which actin cables are generated and maintained remain largely unknown. Fimbrins comprise a family of five members in Arabidopsis thaliana. Here, we characterized a fimbrin isoform, Arabidopsis FIMBRIN5 (FIM5). Our results show that FIM5 is required for the organization of actin cytoskeleton in pollen grains and pollen tubes, and FIM5 loss-of-function associates with a delay of pollen germination and inhibition of pollen tube growth. FIM5 decorates actin filaments throughout pollen grains and tubes. Actin filaments become redistributed in fim5 pollen grains and disorganized in fim5 pollen tubes. Specifically, actin cables protrude into the extreme tips, and their longitudinal arrangement is disrupted in the shank of fim5 pollen tubes. Consequently, the pattern and velocity of cytoplasmic streaming were altered in fim5 pollen tubes. Additionally, loss of FIM5 function rendered pollen germination and tube growth hypersensitive to the actin-depolymerizing drug latrunculin B. In vitro biochemical analyses indicated that FIM5 exhibits actin bundling activity and stabilizes actin filaments. Thus, we propose that FIM5 regulates actin dynamics and organization during pollen germination and tube growth via stabilizing actin filaments and organizing them into higher-order structures.

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Interactions among a Fimbrin, a Capping Protein, and an Actin-depolymerizing Factor in Organization of the Fission Yeast Actin Cytoskeleton

Cited by 81 publications

References 56 publications

Regulation of Sealing Ring Formation by L-plastin and Cortactin in Osteoclasts

Regulation of Sealing Ring Formation by L-plastin and Cortactin in Osteoclasts

Actin-filament cross-linking protein T-plastin increases Arp2/3-mediated actin-based movement

ArabidopsisFIMBRIN5, an Actin Bundling Factor, Is Required for Pollen Germination and Pollen Tube Growth

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