Laminin isoforms: biological roles and effects on the intracellular distribution of nuclear proteins in intestinal epithelial cells

Turck, Natacha; Groß, Isabelle; Gendry, Patrick; Stutzmann, J; Freund, Jean–Noël; Kédinger, Michèle; Simon‐Assmann, Patricia; Launay, Jean-François

doi:10.1016/j.yexcr.2004.10.025

Cited by 48 publications

(44 citation statements)

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“…This might be explained by a recent finding that the binding of the Hey ovarian cancer cell line to laminin, but not to collagen and vitronectin, induces LPA production and activates PI3-kinase signaling that subsequently enhances migration 45 and proliferation. 26 The SKOV3ip.1 and HeyA8 cells showed the strongest adhesion and invasion into collagen I, which is consistent with a strong expression of a3b1-integrin on the cell surfaces of both cell lines (data not shown) and, as we show, the abundant expression of collagen in the submesothelial omental basement membrane. It is also consistent with reports that many ovarian cancer cell lines have a predisposition to adhere to collagen.…”

Section: Discussionsupporting

confidence: 85%

Use of a novel 3D culture model to elucidate the role of mesothelial cells, fibroblasts and extra‐cellular matrices on adhesion and invasion of ovarian cancer cells to the omentum

Kenny

Krausz

Yamada

et al. 2007

Intl Journal of Cancer

221

267

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The omentum is a major site of ovarian cancer metastasis. Our goal was to establish a three-dimensional (3D) model of the key components of the omental microenvironment (mesothelial cells, fibroblasts and extracellular matrices) to study ovarian cancer cell adhesion and invasion. The 3D model comprised of primary human fibroblasts extracted from normal human omentum, mixed with ECM and covered by a layer of primary human mesothelial cells, also from normal human omentum. After addition of ovarian cancer cells, the histological appearance of the 3D culture mimicked microscopic metastases to the omentum from patients with ovarian cancer. When ovarian cancer cells, SKOV3ip.1 and HeyA8, were applied to the 3D omental culture, 60% and 68% of all cells attached, respectively, but only 18% and 25% were able to invade. Ovarian cancer cells preferentially adhered to and invaded collagen I, followed by binding to collagen IV, fibronectin, vitronectin, laminin 10 and 1. Omental mesothelial cells significantly inhibited ovarian cancer cell adhesion and invasion, while omental fibroblasts induced adhesion and invasion. This effect is clearly mediated by direct cell-cell contact, since conditioned medium from mesothelial cells or fibroblasts has a minimal, or no, effect on ovarian cancer cell adhesion and invasion. In summary, we have established a 3D model to study the early steps of ovarian cancer metastasis to the human omentum, and found that omental mesothelial cells inhibit, while omental fibroblasts and the ECM enhance, the attachment and invasion of ovarian cancer cells. ' 2007 Wiley-Liss, Inc.Key words: 3-dimensional culture; 3D; tumor-stroma interaction; metastasis; ovarian cancer Ovarian cancer is typically diagnosed at an advanced stage, because most patients develop clinical symptoms late in the course of the disease, after the tumor has metastasized.1 The most common sites of metastasis from the primary ovarian tumor are the abdominal peritoneum and the omentum. Often the pliable, semitransparent omental tissue is transformed into a dense omental ''cake'' that impinges on the stomach and the transverse colon, causing a bowel obstruction. Even after infragastric removal of the omentum, which is regularly performed for ovarian cancer staging or debulking at the time of surgery, recurrent tumor cells home to residual areas of the omentum at the splenic hilum, the stomach and the transverse colon causing the reappearance of significant clinical symptoms.The majority of ovarian cancers are of epithelial origin, arising from the single layer of cells that covers the ovary, which is separated by a basement membrane from the underlying ovarian stroma.2,3 There are features unique to ovarian cancer that might facilitate its intraperitonel (ip) spread. The ovarian epithelium can adopt a mesenchymal phenotype characterized by cells that lack tight junctions, which makes them prone to exfoliation. 4 Once an ovarian epithelial cell undergoes transformation it is free to disseminate throughout the peritoneal cavity, carried b...

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Section: Discussionsupporting

confidence: 85%

Use of a novel 3D culture model to elucidate the role of mesothelial cells, fibroblasts and extra‐cellular matrices on adhesion and invasion of ovarian cancer cells to the omentum

Kenny

Krausz

Yamada

et al. 2007

Intl Journal of Cancer

221

267

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“…The three chains comprising laminin-1 (LAMA1, LAMB1, and LAMC1) are all most highly expressed at early time points, and LAMA1 transcript levels, in particular, peak early in the time course. This is consistent with the role of laminin-1 in enterocyte differentiation, and particularly the ␣-1 chain (LAMA1), which is required for the efficient secretion of the other two chains and deposition of ECM (De Arcangelis et al, 1996;Turck et al, 2005). The three chains of laminin-5 (LAMA3, LAMB3, and LAMC2) were all up-regulated as cell polarization proceeded.…”

supporting

confidence: 82%

Transcriptional Modulation of Genes Encoding Structural Characteristics of Differentiating Enterocytes During Development of a Polarized Epithelium In Vitro

Halbleib

Sääf²,

Brown

et al. 2007

MBoC

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Although there is considerable evidence implicating posttranslational mechanisms in the development of epithelial cell polarity, little is known about the patterns of gene expression and transcriptional regulation during this process. We characterized the temporal program of gene expression during cell-cell adhesion-initiated polarization of human Caco-2 cells in tissue culture, which develop structural and functional polarity similar to that of enterocytes in vivo. A distinctive switch in gene expression patterns occurred upon formation of cell-cell contacts between neighboring cells. Expression of genes involved in cell proliferation was down-regulated concomitant with induction of genes necessary for functional specialization of polarized epithelial cells. Transcriptional up-regulation of these latter genes correlated with formation of important structural and functional features in enterocyte differentiation and establishment of structural and functional cell polarity; components of the apical microvilli were induced as the brush border formed during polarization; as barrier function was established, expression of tight junction transmembrane proteins peaked; transcripts encoding components of the apical, but not the basal-lateral trafficking machinery were increased during polarization. Coordinated expression of genes encoding components of functional cell structures were often observed indicating temporal control of expression and assembly of multiprotein complexes. INTRODUCTIONThe human intestinal epithelium has a distinctive organization in which a small population of stem cells in the crypt gives rise to postmitotic cells that differentiate as they migrate away from the crypt into the villus (Clatworthy and Subramanian, 2001;Vidrich et al., 2003;Pinto and Clevers, 2005). The major polarized cell type, the enterocyte, forms a tight epithelial monolayer along the crypt-villus axis of the intestine, serving as a permeability barrier between luminal contents and the blood supply and as a conduit for nutrient absorption and enzyme secretion (Clatworthy and Subramanian, 2001).Enterocyte polarization requires the formation of functionally and structurally distinct plasma membrane domains, termed apical and basal-lateral. The apical surface faces the lumen and consists of a dense array of microvilli, the "brush border," which increases the absorptive surface area and contains enzymes and transporters to facilitate uptake of nutrients. The basal-lateral surface, which is separated from the apical surface by the tight junction, faces neighboring cells and the extracellular matrix (ECM). Basallateral membranes contain intercellular junctional complexes, ECM receptors, and channels and transporters that regulate ion/solute transfer from the intestinal lumen to the interstitium (Yeaman et al., 1999b).Differentiation and polarization of epithelial cells involves the reorganization of cytoskeletal structures to initiate changes in cell shape and correct orientation of vesicle trafficking machineries to generate and ma...

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“…Our studies demonstrated that TAA90K-His (or TAA90K) expressed by colon cancer cells, like TAA90K isolated from fibroblasts [Sasaki et al, 1998;Hellstern et al, 2002], exhibits multi-adhesive properties since it bound fibronectin, collagen IV, laminin-1, and to a lesser extent collagen I. In addition, TAA90K-His bound to laminins-5 and -10, components of basement membranes shown to modulate adhesion and proliferation of the human colon carcinoma cell line CaCo-2/ TC7 [Turck et al, 2005]. TAA90K-His also bound well to galectin-3 in a carbohydratedependent manner.…”

Section: Discussionmentioning

confidence: 75%

Tumor‐associated antigen 90K/Mac‐2‐binding protein: Possible role in colon cancer

Ulmer

Keeler

Loh

et al. 2006

J of Cellular Biochemistry

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The tumor-associated antigen 90K (TAA90K)/Mac-2-binding protein implicated in cancer progression and metastasis is modified by beta1-6 branched N-linked oligosaccharides in colon cancer cells, glycans shown to contribute to cancer metastasis. To elucidate the role of TAA90K in colon cancer, we examined its expression and function in human colon tumors and colon carcinoma cell lines. Immunohistochemical analyses of colon tumors revealed elevated expression of TAA90K in all samples analyzed compared to normal colon. To examine the function of TAA90K in colon cancer, we carried out protein and cell binding assays using TAA90K-His purified from HT-29 cells colon carcinoma cells infected with recombinant vaccinia virus expressing TAA90K containing a C-terminal poly-histidine tag. TAA90K-His bound to fibronectin, collagen IV, laminins-1, -5, and -10 and galectin-3 (Mac-2) but poorly to collagen I and galectin-1. As expected, binding of TAA90K to galectin-3 was dependent on carbohydrate since it was inhibitable by lactose and asiolofetuin, and a TAA90K-His glycoform purified from HT-29 cells treated with the glycosylation inhibitor 1-deoxymannojirimycin bound poorly to galectin-3. Unlike TAA90K isolated from other cell types, TAA90K-His isolated from colon cancer cells failed to mediate adhesion of colon cancer and normal cell lines, possibly due to cell-type specific glycosylation of TAA90K-His and/or its putative cellular receptor. However, at low concentrations, TAA90K-His enhanced galectin-3-mediated HT-29 cell adhesion while at high concentrations, it inhibited cell adhesion. Thus, a possible mechanism by which TAA90K may contribute to colon cancer progression is by modulating tumor cell adhesion to extracellular proteins, including galectin-3.

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Laminin isoforms: biological roles and effects on the intracellular distribution of nuclear proteins in intestinal epithelial cells

Cited by 48 publications

References 45 publications

Use of a novel 3D culture model to elucidate the role of mesothelial cells, fibroblasts and extra‐cellular matrices on adhesion and invasion of ovarian cancer cells to the omentum

Use of a novel 3D culture model to elucidate the role of mesothelial cells, fibroblasts and extra‐cellular matrices on adhesion and invasion of ovarian cancer cells to the omentum

Transcriptional Modulation of Genes Encoding Structural Characteristics of Differentiating Enterocytes During Development of a Polarized Epithelium In Vitro

Tumor‐associated antigen 90K/Mac‐2‐binding protein: Possible role in colon cancer

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