Keeping the Vimentin Network under Control: Cell–Matrix Adhesion–associated Plectin 1f Affects Cell Shape and Polarity of Fibroblasts

Burgstaller, Gerald; Gregor, Martin; Winter, Lilli; Wiche, Gerhard

doi:10.1091/mbc.e10-02-0094

Cited by 114 publications

(162 citation statements)

References 54 publications

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“…However, this response appears to be specific to the cell type. In fibroblasts, plectin is necessary for localisation of vimentin intermediate filaments to focal adhesions at the cell periphery (Burgstaller et al, 2010;Spurny et al, 2008) and inhibits cell motility (Gregor et al, 2014). MCF-7 breast cancer cells similarly acquire a slower, less-protrusive phenotype in the absence of plectin (Boczonadi et al, 2007).…”

Section: Discussionmentioning

confidence: 99%

The cytolinker plectin regulates nuclear mechanotransduction in keratinocytes

Almeida

Walko

McMillan

et al. 2015

Journal of Cell Science

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The transmission of mechanical forces to the nucleus is important for intracellular positioning, mitosis and cell motility, yet the contribution of specific components of the cytoskeleton to nuclear mechanotransduction remains unclear. In this study, we examine how crosstalk between the cytolinker plectin and F-actin controls keratin network organisation and the 3D nuclear morphology of keratinocytes. Using micro-patterned surfaces to precisely manipulate cell shape, we find that cell adhesion and spreading regulate the size and shape of the nucleus. Disruption of the keratin cytoskeleton through loss of plectin facilitated greater nuclear deformation, which depended on actomyosin contractility. Nuclear morphology did not depend on direct linkage of the keratin cytoskeleton with the nuclear membrane, rather loss of plectin reduced keratin filament density around the nucleus. We further demonstrate that keratinocytes have abnormal nuclear morphologies in the epidermis of plectin-deficient, epidermolysis bullosa simplex patients. Taken together, our data demonstrate that plectin is an essential regulator of nuclear morphology in vitro and in vivo and protects the nucleus from mechanical deformation.

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Section: Discussionmentioning

confidence: 99%

The cytolinker plectin regulates nuclear mechanotransduction in keratinocytes

Almeida

Walko

McMillan

et al. 2015

Journal of Cell Science

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“…This is regulated by extracellular matrixtransmembrane protein-cytoskeleton interactions (Geiger et al, 2001;Burgstaller et al, 2010;Kim et al, 2011). In bone formation, osteoblasts become highly polarized, align along the bone matrix, and develop intercellular interactions during maturation.…”

Section: Discussionmentioning

confidence: 99%

Type XII collagen regulates osteoblast polarity and communication during bone formation

Izu¹,

Sun²,

Zwolanek³

et al. 2011

J Exp Med

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Abbreviations used in this paper: CT, computed tomography; FACIT, fibrilassociated collagen with interrupted triple helices; HA, hydroxyapatite; H&E, hematoxylin and eosin; HU, Hounsfield unit; shRNA, short hairpin RNA; TMDn, tissue mineral density; TRAP, tartrate resistance acid phosphatase. IntroductionOsteoblast differentiation and maturation are crucial events in the formation of new bone and determination of bone quality (Nakashima et al., 2002;Yoshida et al., 2002;Komori, 2010). Bone formation begins with the differentiation of osteoblasts from pluripotent mesenchymal cells. The progenitors migrate to the sites of bone matrix deposition and differentiate into fully functional, bone matrix-producing osteoblasts (Imai et al., 1998). These events are regulated by the expression of runtrelated gene 2 (Runx2, also known as Cbfa1) and sp7 transcription factor (Sp7, also known as osterix) and by canonical Wnt signaling followed by the secretion of specific bone matrix proteins such as type I collagen (Col1a1), secreted phosphoprotein1 (Spp1, also known as osteopontin), integrin-binding sialoprotein (Ibsp), and bone -carboxyglutamate protein (Bglap, also known as osteocalcin; Harada and Rodan, 2003;Koga et al., 2005). In addition to these changes in gene expression and matrix protein secretion, the mature osteoblasts become aligned along regions of bone deposition with an epithelioid arrangement. The mature, terminally differentiated osteoblasts are highly polarized relative to the site of bone matrix deposition (Ilvesaro et al., 1999;Nakashima et al., 2002;Stains et al., 2002). These features are common to periosteal and endosteal bone and both long and flat bones. Therefore, the alignment, polarization, and interaction of osteoblasts are important events necessary for production of a functional bone matrix.Cell motility, communication, and shape are controlled via the local microenvironment where the extracellular matrix provides a substrate for cell anchorage, stores and presents growth factors or cytokines, and serves as a tissue scaffold (Rozario and DeSimone, 2010). The extracellular matrix interacts with the intracellular actin cytoskeleton via transmembrane proteins that affect cytoskeletal organization, cell motility and polarity, proliferation, and survival (Berthiaume et al., 1996;Geiger et al., 2001;Théry et al., 2005;Parsons et al., 2010;Kim et al., 2011). Thus, extracellular matrix-transmembrane protein-cytoskeleton D ifferentiated osteoblasts are polarized in regions of bone deposition, demonstrate extensive cell interaction and communication, and are responsible for bone formation and quality. Type XII collagen is a fibril-associated collagen with interrupted triple helices and has been implicated in the osteoblast response to mechanical forces. Type XII collagen is expressed by osteoblasts and localizes to areas of bone formation. A transgenic mouse null for type XII collagen exhibits skeletal abnormalities including shorter, more slender long bones with decreased mechanical strength as well as a...

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“…and endothelial cells and is also found in epithelial matrix junctions termed hemidesmosomes (Bhattacharya et al, 2009;Burgstaller et al, 2010;Seifert et al, 1992;Tsuruta et al, 2002;Wiche, 1998). We found plectin enriched in cFAs, where it colocalizes with talin, but is mostly absent from pFAs (Fig.…”

Section: Primary Aec Display Unique Arrangement Of Fasmentioning

confidence: 99%

“…The cFAs in the inner ring in rAEC are involved in keratin cytoskeleton organization Plectin binds intermediate filament (IF) proteins and is involved in linking IFs to the cell surface (Bhattacharya et al, 2009;Burgstaller et al, 2010;Geerts et al, 1999;Gonzales et al, 2001;Karashima et al, 2012;Svitkina et al, 1996;Wiche, 1998). Additionally, there is precedence for FAs being important for IF organization (Bhattacharya et al, 2009;Burgstaller et al, 2010;Windoffer et al, 2006).…”

Section: Fa Double Ring Formation Is Plectin Dependentmentioning

confidence: 99%

“…Additionally, there is precedence for FAs being important for IF organization (Bhattacharya et al, 2009;Burgstaller et al, 2010;Windoffer et al, 2006). Thus, we next determined if the plectincontaining cFAs influence the distribution of the IF keratin cytoskeleton of rAEC (Eisenberg et al, 2011;Takawira et al, 2011).…”

Section: Fa Double Ring Formation Is Plectin Dependentmentioning

confidence: 99%

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Plectin-containing, centrally-localized focal adhesions exert traction forces in primary lung epithelial cells

Eisenberg

Beaumont

Takawira

et al. 2013

Journal of Cell Science

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SummaryReceptor clustering upon cell attachment to the substrate induces assembly of cytoplasmic protein complexes termed focal adhesions (FAs), which connect, albeit indirectly, the extracellular matrix to the cytoskeleton. A subset of cultured primary alveolar epithelial cells (AEC) display a unique pattern of vinculin/paxillin/talin-rich FAs in two concentric circles when cultured on glass and micropatterned substrates: one ring of FAs located at the cell periphery (pFAs), and another FA ring located centrally in the cell (cFAs). Unusually, cFAs associate with an aster-like actin array as well as keratin bundles. Moreover, cFAs show rapid paxillin turnover rates following fluorescence recovery after photobleaching and exert traction forces similar to those generated by FAs at the cell periphery. The plakin protein plectin localizes to cFAs and is normally absent from pFAs, whereas tensin, a marker of mature/fibrillar adhesions, is found in both cFAs and pFAs. In primary AEC in which plectin expression is depleted, cFAs are largely absent, with an attendant reorganization of both the keratin and actin cytoskeletons. We suggest that the mechanical environment in the lung gives rise to the assembly of unconventional FAs in AEC. These FAs not only show a distinctive arrangement, but also possess unique compositional and functional properties.

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Keeping the Vimentin Network under Control: Cell–Matrix Adhesion–associated Plectin 1f Affects Cell Shape and Polarity of Fibroblasts

Cited by 114 publications

References 54 publications

The cytolinker plectin regulates nuclear mechanotransduction in keratinocytes

The cytolinker plectin regulates nuclear mechanotransduction in keratinocytes

Type XII collagen regulates osteoblast polarity and communication during bone formation

Plectin-containing, centrally-localized focal adhesions exert traction forces in primary lung epithelial cells

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