myospheroid


EVOLUTIONARY HOMOLOGS


Table of contents

Integrins as Laminin receptors

Receptors of the integrin family are expressed by every cell type and are the primary means by which cells interact with the extracellular matrix. The control of integrin expression affects a wide range of developmental and cellular processes, including the regulation of gene expression, cell adhesion, cell morphogenesis and cell migration. The concentration of substratum-bound ligand (laminin) post-translationally regulates the amount of receptor (alpha6beta1, integrin) expressed on the surface of sensory neurons (See Drosophila Laminin) . When ligand availability is low, surface amounts of receptor increase, whereas integrin RNA and total integrin protein decrease. Ligand concentration determines surface levels of integrin by altering the rate at which receptor is removed from the cell surface. Furthermore, increased expression of integrin at the cell surface is associated with increased neuronal cell adhesion and neurite outgrowth. These results indicate that integrin regulation maintains neuronal growth-cone motility over a broad range of ligand concentrations, allowing axons to invade different tissues during development and regeneration (Condic, 1997).

The development of the heart from a single heart tube to a four chambered organ with two separated unidirectional flows is a highly complex process. Events like looping, septation, tissue remodelling, and development of valves take place at a time when the heart is already pumping. The ability of cells to migrate in such a dynamic environment, and to adhere to one another and to their extracellular matrix is crucial. Integrins and extracellular matrix components have already been implicated in this process. The differential expression of the alpha-6 integrin subunit was studied during late murine heart development, e.g., in the process from looping to the end of septation. A constant and high expression of alpha-6 occurs in the atrial myocardium and a decrease in expression takes place in the ventricular trabecular myocardium. The compact myocardial wall and the ventricular septum do not express alpha-6, except for the myocardium of the distal outflow tract at early stages. The expression of this integrin subunit is described in the endocardial cushions that contribute to the development of the atrioventricular and semilunar valves. A role is proposed for the alpha-6-beta-1 laminin receptor in the adhesion of cells to their extracellular matrix at sites of high stress due to cardiac contraction or shear stress induced by blood flow. This study suggests a distinct role for alpha-6-beta-1 in the heart and provides insight concerning the probable, and no doubt vital roles of integrins and their extracellular matrix ligands during embryonic development (Hierck, 1997).

The interactions between tumor cells and laminin or other components of the extracellular matrix have been shown to play an important role in tumor invasion and metastasis. However, the role of the monomeric 67-kDa laminin receptor (67LR) remains unclear. The regulation of 67LR expression was analyzed under different culture conditions with respect to the expression of other well characterized laminin receptors. In A431 cells treated with laminin for different time periods, the regulation of 67LR expression correlates with expression of the alpha6 integrin subunit but not with the expression of other laminin receptors. Moreover, cytokine treatment results in down-modulated expression of the alpha6 integrin subunit and the 67LR. Co-regulation of the expression of the two receptors is further suggested by the observation that specific down-modulation of the alpha6-chain by antisense oligonucleotides is accompanied by a proportional decrease in the cell surface expression of 67LR. Biochemical analyses indicates co-immunoprecipitation of 67LR and the alpha6 subunit with an anti-alpha6 but not an anti-beta1 monoclonal antibody. Co-regulation of 67LR and alpha6 subunit expression, together with the physical association between the two receptors, supports the hypothesis that 67LR is an auxiliary molecule involved in regulating or stabilizing the interaction of laminin with the alpha6beta4 integrin (Ardini, 1997).

Antibody- or laminin-induced ligation of a laminin receptor involved in morphogenesis and tumor progression, the hemidesmosomal integrin alpha 6 beta 4, causes tyrosine phosphorylation of the beta 4 subunit in intact cells. This event is mediated by a protein kinase(s) physically associated with the integrin. Co-immunoprecipitation and GST fusion protein binding experiments show that the adaptor protein Shc forms a complex with the tyrosine-phosphorylated beta 4 subunit. Shc is then phosphorylated on tyrosine residues and recruits the adaptor Grb2, thereby potentially linking alpha 6 beta 4 to the ras pathway. The beta 4 subunit is phosphorylated at multiple tyrosine residues in vivo, including a tyrosine-based activation motif (TAM) resembling those found in T and B cell receptors. Phenylalanine substitutions at the beta 4 TAM disrupt association of alpha 6 beta 4 with hemidesmosomes, but do not interfere with tyrosine phosphorylation of Shc and recruitment of Grb2. Signal transduction by the alpha 6 beta 4 integrin is mediated by an associated tyrosine kinase and phosphorylation of distinct sites in the beta 4 tail mediate assembly of the hemidesmosomal cytoskeleton and recruitment of Shc/Grb2 (Mainiero, 1995).

The signaling pathways linking integrins to nuclear events are incompletely understood. Intracellular signaling by the alpha6beta4 integrin has been studied. alpha6beta4 is a laminin receptor expressed in basal keratinocytes and other cells. Ligation of alpha6beta4 in primary human keratinocytes causes tyrosine phosphorylation of Shc, recruitment of Grb2, activation of Ras and stimulation of the MAP kinases Erk and Jnk. beta4 is known to be phosphorylated by integrin associated kinase. In contrast, ligation of the laminin- and collagen-binding integrins alpha3beta1 and alpha2beta1 does not cause these events. While the stimulation of Erk by alpha6beta4 is suppressed by dominant-negative Shc, Ras and RhoA, the activation of Jnk is inhibited by dominant-negative Ras and Rac1 and by the phosphoinositide 3-kinase inhibitor Wortmannin. Adhesion mediated by alpha6beta4 induces transcription from the Fos serum response element and promoted cell cycle progression in response to mitogens. In contrast, alpha3beta1- and alpha2beta1-dependent adhesion did not induce these events. These findings suggest that the coupling of alpha6beta4 integrin to the control of cell cycle progression mediated by Shc regulates the proliferation of basal keratinocytes and possibly other cells that are in contact with the basement membrane in vivo. The results of this study support the notion that the recruitment of Shc to the alpha6beta4 is mediated by the cytoplasmic domain of beta4 (Mainiero, 1997).

Subcutaneous injection of beta 1 integrin-deficient embryonic stem cells in mice causes the formation of teratomas, although they occur with a lower frequency and are smaller than those derived from wild-type cells. Immunofluorescence analysis of the deficient tumors indicates a disorganized deposition of several basement membrane proteins. Electron microscopy demonstrates frequent gaps in cell-associated basement membranes or loss of close contact of the basement membrane to the cells. Further aberrant features are multilaminar structures and amorphous deposits, indicating a strong impairment of correct basement membrane assembly. There is a more than 90% decrease in the content of laminin-1 (alpha 1 beta 1 gamma 1) and a 70% decrease in nidogen in the beta 1 integrin-deficient teratomas. No significant changes are detected for other matrix proteins (perlecan, fibronectin, fibulins). This selective change impairs the formation of laminin-nidogen complex and enhances nidogen degradation. There is also a distinctly reduced expression of laminin alpha 1, beta 1, and gamma 1 chains. Similar reductions are also observed in cultured embryonic stem cells prior to any differentiation. No change, or only small changes, are observed for laminin alpha 2 and beta 2 chain, nidogen, and perlecan mRNA. These data emphasize a distinct role for beta 1 integrins in the correct assembly of basement membranes, which may occur through direct ligand binding and/or regulatory events at the transcriptional level (Sasaki, 1998).

F9 embryonal carcinoma cells treated with retinoic acid differentiate in monolayer into parietal endoderm (PE) or in suspension into embryoid bodies with an outer layer of visceral endoderm (VE) surrounding a core of largely undifferentiated cells. Cell-extracellular matrix interactions mediated by the beta 1 integrins play a critical role in the differentiation and migration of PE. The pattern of expression and function of the integrin alpha 6 beta 1 was studied during the differentiation of F9 cells into VE and PE. F9 cells express integrin subunits alpha 3, alpha 5, alpha 6, and beta 1. Cell adhesion and migration assays demonstrate that alpha 6 beta 1 is the major laminin receptor in undifferentiated F9 cells as well as F9-derived PE cells. However, the amount of alpha 6 protein decreases significantly upon F9 cell differentiation into either VE or PE. In contrast, the amount of steady-state alpha 6 message stays constant before and after F9 cell differentiation, suggesting that the down-regulation of alpha 6 beta 1 occurs post-transcriptionally. Two alpha 6 isoforms are generated by alternative RNA processing. While alpha 6B is the major mRNA isoform before and after F9 cell differentiation, alpha 6A mRNA is weakly expressed in undifferentiated F9 cells and is substantially increased following F9 differentiation into PE. An increase in alpha 6A and a dramatic decrease in alpha 6B protein occurs following PE differentiation. Whereas the stability of alpha 6B protein is unaltered, synthesis of alpha 6B protein is decreased at least threefold following PE differentiation. Further experiments demonstrate that alpha 6A localizes to focal contacts in PE cells. The switch from alpha 6B to alpha 6A and the localization of alpha 6A at focal contacts correlate with the acquisition of PE cell motility, which suggests distinct functions for the two alpha 6 isoforms (Jiang, 1995).

Many aspects of myogenesis are believed to be regulated by myoblast interactions with specific components of the extracellular matrix. For example, laminin has been found to promote adhesion, migration, and proliferation of mammalian myoblasts. Based on affinity chromatography, the alpha7beta1 integrin has been presumed to be the major receptor mediating myoblast interactions with laminin. A monoclonal antibody, O26, was prepared that specifically reacts with both the X1 and the X2 extracellular splice variants of the alpha7 integrin chain. This antibody completely and selectively blocks adhesion and migration of rat L8E63 myoblasts on laminin-1, but not on fibronectin. In contrast, a polyclonal antibody to the fibronectin receptor, alpha5beta1 integrin, blocks myoblast adhesion on fibronectin, but not on laminin-1. The alpha7beta1 integrin also binds to a mixture of laminin-2 and laminin-4, the major laminin isoforms in developing and adult skeletal muscle, but O26 is a much less potent inhibitor of myoblast adhesion on the laminin-2/4 mixture than on laminin-1. Based on affinity chromatography, it is suggested that this may be due to higher affinity binding of alpha7X1 to laminin-2/4 than to laminin-1 (Crawley, 1997).

Functional studies of the alpha6beta4 integrin have focused primarily on its role in the organization of hemidesmosomes, stable adhesive structures that associate with the intermediate filament cytoskeleton. The function of the alpha6beta4 integrin was examined in clone A cells, a colon carcinoma cell line that expresses alpha6beta4 but no alpha6beta1 integrin and exhibits dynamic adhesion and motility on laminin-1. Time-lapse videomicroscopy of clone A cells on laminin-1 reveal that their migration is characterized by filopodial extension and stabilization followed by lamellae that extend in the direction of stabilized filopodia. A function-blocking mAb specific for the alpha6beta4 integrin inhibits clone A migration on laminin-1. This mAb also inhibits filopodial formation and stabilization and lamella formation. The alpha6beta4 integrin is localized as discrete clusters in filopodia, lamellae, and retraction fibers. Although beta1 integrins are also localized in the same structures, a spatial separation of these two integrin populations is evident. In filopodia and lamellae, a striking colocalization of the alpha6beta4 integrin and F-actin is seen. An association between alpha6beta4 and F-actin is supported by the fact that alpha6beta4 integrin and actin are released from clone A cells by treatment with the F-actin- severing protein gelsolin and that alpha6beta4 immunostaining at the marginal edges of clone A cells on laminin-1 is resistant to solubilization with Triton X-100. Cytokeratins are not observed in filopodia and lamellipodia: alpha6beta4 was extracted from these marginal edges with a Tween-40/deoxycholate buffer that solubilizes the actin cytoskeleton but not cytokeratins. Three other carcinoma cell lines (MIP-101, CCL-228, and MDA-MB-231) exhibit alpha6beta4 colocalized with actin in filopodia and lamellae. Formation of lamellae in these cells is inhibited with an alpha6-specific antibody. Together, these results indicate that the alpha6beta4 integrin functions in carcinoma migration on laminin-1 through its ability to promote the formation and stabilization of actin-containing motility structures (Rabinovitz, 1997).

Integrins as tenascin receptors

To identify potential cell surface receptors for chicken cytotactin/tenascin (see Drosophila Tenascin major), the ability of recombinant fusion proteins spanning the proximal fibronectin (FN) type III repeats of the molecule to support attachment of glioma and carcinoma cell lines has been examined. The third FN type III repeat, which contains the RGD tripeptide, supports cell attachment and cell spreading; however, mutation of RGD to RAD do not result in significant loss of either activity. The same repeat of mouse CT, which contains a natural mutant, RVD, also supports cell attachment and spreading, although at a lower level; both activities are increased by mutation of the RVD sequence to RGD. Studies utilizing RGD-containing peptides and well-characterized antibodies to integrins indicate that cell attachment to the third FN type III repeat is mediated by at least two different integrin receptors of the alpha v subtype. Additional cellular receptors may also be involved in cell attachment to CT. For example, an antibody to the beta 1 subfamily of integrins partially inhibits binding of cells to intact CT but does not inhibit cell binding to the third FN type III repeat. These findings suggest that the RGD site in CT is able to mediate cell attachment to integrins and thus is not a cryptic adhesion site. They also open the possibility that the functions of CT in processes such as counteradhesion, cell migration, cell proliferation, and cell differentiation may be mediated in part by interaction with multiple integrins (Prieto, 1993).

The integrin alpha 9 subunit is a partner of the beta 1 subunit, which is expressed in basal keratinocytes, hepatocytes, airway epithelial cells, and smooth and skeletal muscle. Alpha 9 beta 1 was expressed on the surface of the human embryonic kidney cell line 293 and the human colon carcinoma cell line SW480. These transfected cells lines were used to identify ligand(s) for this integrin. Transfected cells did not appear to utilize alpha 9 beta 1 for attachment to the extracellular matrix proteins fibronectin, laminin, vitronectin, fibrinogen, thrombospondin, or type I or IV collagen. However, in contrast to mock transfectants, both 293 cells and SW480 cells expressing alpha 9 beta 1 adhered to intact chicken tenascin. By utilizing a variety of recombinant fragments of tenascin, the binding site for alpha 9 beta 1 localizes to the third type III repeat. This repeat contains the arginine-glycine-aspartic acid (RGD) tripeptide that has been shown to serve as a binding site in tenascin for alpha v-integrins. However, the RGD site does not appear to be the binding site for alpha 9 beta 1, as the attachment of alpha 9 transfectants to this fragment is not inhibited by RGD peptide, nor by changing the RGD site to RAD or RAA (Yokosaki, 1994).

Tenascin-C (TN-C) is induced in pulmonary vascular disease, where it colocalizes with proliferating smooth muscle cells (SMCs) and epidermal growth factor (Egf). Cultured SMCs require TN-C for Egf-dependent growth on type I collagen. In this study, the regulation and function of TN-C was explored in SMCs. A matix metalloproteinase (MMP) inhibitor (GM6001) suppresses SMC TN-C expression on native collagen, whereas denatured collagen promotes TN-C expression in a beta3 integrin- dependent manner, independent of MMPs. Floating type I collagen gel also suppresses SMC MMP activity and TN-C protein synthesis and induces apoptosis, in the presence of Egf. Addition of exogenous TN-C to SMCs on floating collagen, or to SMCs treated with GM6001, restores the Egf growth response and "rescues" cells from apoptosis. The mechanism by which TN-C facilitates Egf-dependent survival and growth was then investigated. TN-C interactions with alphavbeta3 integrins modify SMC shape, and Egf-dependent growth. These features are associated with redistribution of filamentous actin to focal adhesion complexes, which colocalize with clusters of Egf-rs, tyrosine-phosphorylated proteins, and increased activation of Egf-rs after addition of Egf. Cross-linking SMC beta3 integrins replicates the effect of TN-C on Egf-r clustering and tyrosine phosphorylation. Together, these studies represent a functional paradigm for ECM-dependent cell survival whereby MMPs upregulate TN-C by generating beta3 integrin ligands in type I collagen. In turn, alphavbeta3 interactions with TN-C alter SMC shape and increase Egf-r clustering and Egf-dependent growth. Conversely, suppression of MMPs downregulates TN-C and induces apoptosis (Jones, 1997).


Table of contents


myospheroid: Biological Overview | Regulation | Developmental Biology | Effects of Mutation | References

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