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B P Toole

Publications and source records attributed to B P Toole.

At least 37 records · Page 2Linked to original sources

A new alternatively spliced exon between v9 and v10 provides a molecular basis for synthesis of soluble CD44.

The numerous isoforms of murine CD44 contain a common peptide region that is encoded by exons 1-5, 16-18, and 20 and variant regions derived from exons 6-15, usually referred to as v1-v10. We have obtained evidence for expression of an additional exon between v9 (or exon 14) and the exon previously termed v10 (or exon 15). Thus, we now number the variant exons as follows: v1-v9 (exons 6-14), v10 (exon 15), and v11 (exon 16); the remaining 3'-exons become exons 17-21 (newly numbered exons are underlined). The new exon, now termed exon v10, contains 93 base pairs and can be internally spliced; the 5'-region is termed v10a, and the 3'-region, v10b. Stop codons are positioned in v10a such that translated protein would be truncated prior to the transmembrane domain and secreted as a soluble protein. We have also found that the previously described v9 exon (now termed v9a), which is 90 base pairs in length, is actually the 5'-region of a longer exon of 142 base pairs (the 3'-region is termed v9b) and thus arises by internal splicing of the longer exon. Using reverse transcription-polymerase chain reaction, four different cDNAs for CD44 isoforms that use different combinations of the new exonic sequences have been found. The mRNAs containing the new exonic sequences are restricted in their expression; to date, we have demonstrated their presence in murine G8 myoblasts in culture and in embryonic muscle and cartilage tissues in vivo. Of these new isoforms, the predominant, full-length amplified product is encoded by exons 1-5, exon 13 (v8), the 5'-part of exon 14 (v9a), exon 15 (v10), exon 16 (v11), exons 17-19, and exon 21. When COS-7 cells were transfected with v10-containing cDNA constructs, the cells secreted low molecular weight soluble CD44 into their medium. Thus, the stop codons within the new exon v10 provide a molecular basis for de novo synthesis of soluble CD44 isoforms.

Alternative Splicing↗

Expression of multiple CD44 isoforms in the apical ectodermal ridge of the embryonic mouse limb.

Previous immunohistochemical studies have shown that CD44 is highly enriched within the apical ectodermal ridge of the developing limb (Wheatley et al. [1993] Development 119: 295-306), but the particular isoforms of CD44 were not identified. We show here that CD44s (standard or "hemopoietic" isoform) and several CD44 variants, especially V3-V10, V4-V10, and V6-V10, are concentrated in the apical ectodermal ridge in the early mouse limb. Since CD44s is a major cell surface receptor for hyaluronan, we compared its localization with that of hyaluronan. In the early limb bud, hyaluronan is distributed throughout the mesoderm but is absent from all regions of the ectoderm. Hyaluronan is especially enriched in the basement membrane separating ectoderm and mesoderm, except beneath the apical ectodermal ridge where it is absent. Since CD44s is a known endocytic receptor for hyaluronan, its presence in ridge ectoderm could lead to degradation of hyaluronan destined for the neighboring region of basement membrane, thus facilitating interaction of the ridge with underlying mesoderm. The CD44 (V3-V10) isoform found in the ridge is expressed elsewhere as a proteoglycan with heparan sulfate chains that bind fibroblast growth factors. Since fibroblast growth factors are present in the ridge and are essential for limb morphogenesis, CD44 (V3-V10) is likely to act as a cofactor or modulator in the growth-promoting action or maintenance of the ridge.

Animals↗

Increased hyaluronan at sites of attachment to mesentery by CD44-positive mouse ovarian and breast tumor cells.

The mouse ovarian ascites tumor, MOT, and mammary ascites tumor, TA3/St, served as models to follow changes in hyaluronan levels during tumor growth, attachment, and invasion. Subsequent to introduction of tumor cells into the peritoneal cavity, hyaluronan accumulated intraperitoneally and at the initial sites of attachment of tumor cells and cell clumps to the mesenteric surface; the latter co-localized with sites of fibrin deposition as reported earlier. Subsequently, high levels of hyaluronan accumulated throughout the interior of the mesentery. Because neither tumor cell line synthesized substantial amounts of hyaluronan in culture, the large accumulations observed in the mesenteries and ascites fluid of tumor-bearing animals most likely resulted from increased synthesis and secretion by peritoneal-lining mesothelial cells and/or fibroblasts in response to stimulation by the tumor cells or their products. TA3/St tumor cells were universally positive for the hyaluronan receptor, CD44, whereas approximately 90% of MOT tumor cells were CD44-negative. However, the great majority of MOT or TA3/St cells that initially attached to the mesentery were strongly CD44 positive. We propose that hyaluronan-rich matrix is involved in tumor cell attachment to the mesentery possibly via interaction with tumor cell surface CD44.

Animals↗

Production of hyaluronan-dependent pericellular matrix by embryonic rat glial cells.

The extracellular matrix of brain is largely composed of aggregates formed by assembly of many proteoglycan and link protein molecules along a hyaluronan polymer backbone. Some cell types construct large, highly hydrated, pericellular matrices or 'coats' from these hyaluronan-mediated aggregates. We show here that embryonic glial cells produce such hyaluronan-dependent pericellular matrices in response to addition of serum or basic fibroblast growth factor plus transforming growth factor-beta. It is proposed that such a matrix is a significant component of the extracellular milieu of the brain, especially during morphogenesis within the developing brain, and that basic fibroblast growth factor and transforming growth factor-beta regulate its production.

Animals↗

A novel glycosaminoglycan-binding protein is the vertebrate homologue of the cell cycle control protein, Cdc37.

Using a monoclonal antibody, IVd4, that recognizes a novel group of hyaluronan-binding proteins, we have immunoscreened a cDNA library constructed from embryonic chick heart muscle mRNA. One of the cDNAs isolated from the library encodes a 29.3-kDa protein homologous to Cdc37, an essential cell cycle regulatory factor previously characterized genetically in yeast and Drosophila; this is the first vertebrate CDC37 gene to be cloned to date. We also present evidence for the existence of a second chick isoform that is identical to the 29.3-kDa protein over the first 175 amino acids but is entirely different at the carboxyl terminus and lacks the IVd4 epitope. The avian Cdc37 binds hyaluronan, chondroitin sulfate and heparin in vitro, and both isoforms contain glycosaminoglycan-binding motifs previously described in several hyaluronan-binding proteins. These findings suggest a role for glycosaminoglycans in cell division control.

Amino Acid Sequence↗

Ectodermal stimulation of the production of hyaluronan-dependent pericellular matrix by embryonic limb mesodermal cells.

Interaction of ectoderm and underlying mesoderm is essential for normal vertebrate limb morphogenesis. One of the functions of limb bud ectoderm is its influence on the composition of extracellular matrix in subectodermal mesoderm, which in turn participates in morphogenesis of this region of the limb. This matrix is highly enriched in hyaluronan, even at the time when the level of hyaluronan in the chondrogenic and myogenic regions of the limb decreases, due to secretion of a stimulatory factor by the ectoderm. In this study we show that limb bud ectoderm not only stimulates hyaluronan synthesis but induces formation of large hyaluronan-dependent, pericellular matrices around cultured limb bud mesodermal cells. The ectodermal activity is mimicked in great part by fibroblast growth factor-2 and transforming growth factor-beta, and antibodies to these proteins inhibit induction of mesodermal pericellular matrix by the ectodermal factor. It has been shown by other investigators that fibroblast growth factor-2 is produced by limb ectoderm whereas transforming growth factor-2 is produced by limb ectoderm whereas transforming growth factor-beta is present in limb mesodermal tissues. Thus we conclude that the unique properties of mesodermally produced matrix underlying limb bud ectoderm are regulated, at least in part, by ectodermal fibroblast growth factor-2, probably in concert with mesodermal transforming growth factor-beta.

Animals↗

Functional domain mapping using M13 deletions.

We describe a convenient approach for concomitant functional characterization of peptide domains (monoclonal antibody epitopes, receptor-ligand, DNA-protein, and protein-protein interaction sites, etc) encoded by the sequential series of overlapping M13 subclones generated for nucleotide sequence determination of a new cDNA. We have employed this method to rapidly map the location and amino acid sequence of an epitope-containing domain within a polypeptide encoded by a newly isolated cDNA.

Amino Acid Sequence↗

The role of hyaluronan-binding protein in assembly of pericellular matrices.

Hyaluronan-dependent pericellular matrices or "coats" are expressed by a variety of cell types in culture and modulation of their expression may be important in regulation of cell interactions in vivo during development. Monoclonal antibody IVd4, which recognizes hyaluronan-binding protein with the properties of a hyaluronan receptor, was shown to block formation of these coats by a variety of cells. Using rat fibrosarcoma cells, it was found that the antibody not only blocked initial formation of the coats but also caused their loss when added subsequent to formation. The loss of preformed coats in the presence of antibody occurred at 4 degrees and 37 degrees, implying that the function of hyaluronan-binding protein in coat formation is not in mediating metabolic processes. The antibody also had no significant effect on hyaluronan production by the fibrosarcoma cells. In addition, hyaluronan hexasaccharide, a competitive inhibitor of the interaction between polymeric hyaluronan and its cell surface receptor, was found to inhibit coat formation. Thus it is concluded that a hyaluronan-binding protein with the properties of a hyaluronan receptor is required for pericellular matrix formation.

Animals↗

Hyaluronan-binding protein in endothelial cell morphogenesis.

Previous studies from several laboratories have provided evidence that interaction of hyaluronan (HA) with the surface of endothelial cells may be involved in endothelial cell behavior. We have recently characterized a mAb, mAb IVd4, that recognizes and neutralizes HA-binding protein (HABP) from a wide variety of cell types from several different species (Banerjee, S. D., and B. P. Toole. 1991. Dev. Biol. 146:186-197). In this study we have found that mAb IVd4 inhibits migration of endothelial cells from a confluent monolayer after "wounding" of the monolayer. HA hexasaccharide, a fragment of HA with the same disaccharide composition as polymeric HA, also inhibits migration. In addition, both reagents inhibit morphogenesis of capillary-like tubules formed in gels consisting of type I collagen and basement membrane components. Immunocytology revealed that the antigen recognized by mAb IVd4 becomes localized to the cell membrane of migrating cells, including many of their lamellipodia. Treatment with high concentrations of HA hexamer causes loss of immunoreactivity from these structures. We conclude that HABP recognized by mAb IVd4 is involved in endothelial cell migration and tubule formation.

Animals↗

Hyaluronan-dependent pericellular coats of chick embryo limb mesodermal cells: induction by basic fibroblast growth factor.

Basic fibroblast growth factor (FGF) has been shown previously to be present in the chick embryonic limb during early stages of its development, at which time the limb mesodermal cells are proliferating within a hyaluronan-rich extracellular matrix. In this study, basic FGF was found to stimulate hyaluronan synthesis and production of hyaluronan-dependent pericellular coats by mesodermal cells from the chick embryo limb; acidic FGF, platelet-derived growth factor, epidermal growth factor, and retinoic acid either had a much smaller effect than basic FGF or an inhibitory effect. Transforming growth factor-beta stimulated hyaluronan synthesis and coat formation but, unlike basic FGF, this factor also stimulated chondroitin sulfate production by the mesodermal cells.

Animals↗

Monoclonal antibody to chick embryo hyaluronan-binding protein: changes in distribution of binding protein during early brain development.

A monoclonal antibody, MAb IVd4, that recognizes hyaluronan-binding protein (HABP) from chick embryo brain has been produced and characterized. By immunoblotting, MAb IVd4 was shown to recognize three proteins in chick embryo brain of molecular weight 93, 90, and 69 kDa; this interaction was inhibited by addition of hyaluronan hexasaccharides. Overlay of transblots with [3H]hyaluronan showed binding to proteins of similar molecular weight. MAb IVd4 blocked binding of [3H]hyaluronan to brain HABP and to simian virus-transformed 3T3 cells, indicating a possible relationship with the 85-kDa hyaluronan receptor of these cells. The distribution of HABP during early brain development was analyzed by immunohistochemistry. Immunoreactivity was uniform in newly formed neuroectoderm but became more concentrated in the roof of the brain during the second day of embryonic development. As the neuroectoderm becomes layered, the HABP was increasingly restricted to the forming plexiform layer, an area enriched in neural cell processes. Immunoreactivity was greatly enhanced by pretreatment of tissue with hyaluronidase, presumably due to removal of hyaluronan bound to the HABP, and was abolished on treatment with hyaluronan hexasaccharide, presumably due to inhibition of HABP-antibody interaction. These results suggest that a hyaluronan receptor is involved in early cellular events in brain development.

Animals↗

Hyaluronate-binding proteins of murine brain.

The distribution of hyaluronate-binding activity was determined in the soluble and membrane fractions derived from adult mouse brain by sonication in low-ionic-strength buffer. Approximately 60% of the total activity was recovered in the soluble fraction and 33% in membrane fractions. In both cases, the hyaluronate-binding activities were found to be of high affinity (KD = 10(-9) M), specific for hyaluronate, and glycoprotein in nature. Most of the hyaluronate-binding activity from the soluble fraction chromatographed in the void volume of Sepharose CL-4B and CL-6B. Approximately 50% of this activity was highly negatively charged, eluting from diethylaminoethyl (DEAE)-cellulose in 0.5 M NaCl, and contained chondroitin sulfate chains. This latter material also reacted with antibodies raised against cartilage link protein and the core protein of cartilage proteoglycan. Thus, the binding and physical characteristics of this hyaluronate-binding activity are consistent with those of a chondroitin sulfate proteoglycan aggregate similar to that found in cartilage. A 500-fold purification of this proteoglycan-like, hyaluronate-binding material was achieved by wheat germ agglutinin affinity chromatography, molecular sieve chromatography on Sepharose CL-6B, and ion exchange chromatography on DEAE-cellulose. Another class of hyaluronate-binding material (25-50% of that recovered) eluted from DEAE with 0.24 M NaCl; this material had the properties of a complex glycoprotein, did not contain chondroitin sulfate, and did not react with the antibodies against cartilage link protein and proteoglycan. Thus, adult mouse brain contains at least three different forms of hyaluronate-binding macromolecules. Two of these have properties similar to the link protein and proteoglycan of cartilage proteoglycan aggregates; the third is distinguishable from these entities.

Animals↗

The role and regulation of tumour-associated hyaluronan.

Significantly increased levels of the glycosaminoglycan hyaluronan are often associated with human and animal tumours. In the rabbit V2 carcinoma elevated levels of tumour-associated hyaluronan are also closely correlated with invasiveness. We have therefore initiated studies to better define the role and regulation of hyaluronan synthesis in tumour tissues. In cell culture many tumour cell types have reduced capacities to synthesize hyaluronan even when derived from tumours enriched in hyaluronan. We showed that several of these same cells can nevertheless stimulate hyaluronan synthesis by normal fibroblasts. In the LX-1 human lung carcinoma cell line this stimulatory potential resides in a membrane-bound, heat-sensitive, lipophilic, cell surface glycoprotein. These data suggest that production of tumour-associated hyaluronan occurs via tumour-stromal cell interactions. We recently demonstrated that some human tumour cells also possess unoccupied, high affinity, cell surface binding sites for hyaluronan which may allow tumour cells to interact directly with hyaluronan-enriched extracellular matrices. This interaction may in turn allow tumour cells to use hyaluronan as a support for adhesion and locomotion. The spatial organization of hyaluronan could then function to guide tumour cells into surrounding stroma. We attempted to visualize this spatial deposition of hyaluronan in situ within frozen sections of human tumour tissue using a morphological probe that specifically recognizes hyaluronan. Hyaluronan appears most prominently in the partially degraded connective tissue.

Animals↗

Hyaluronate-cell interactions and growth factor regulation of hyaluronate synthesis during limb development.

Hyaluronate is a major component of the intercellular matrix surrounding proliferating and migrating cells in embryonic tissues. When placed in culture, mesodermal cells from the early, proliferative stages of limb development produce high levels of hyaluronate and exhibit prominent hyaluronate-dependent pericellular coats. Cells from the subsequent stages of mesodermal condensation that precede differentiation to cartilage and muscle produce less hyaluronate and do not exhibit these coats. Also at this time, binding sites specific for hyaluronate appear on the surface of the mesodermal cells. These binding sites may participate in the mechanism of condensation by mediating cell aggregation and the endocytosis of hyaluronate. Further changes in hyaluronate-cell interaction occur during differentiation of the condensed mesoderm to cartilage and muscle. Hyaluronate synthesis and pericellular coat formation in the mesoderm are stimulated by a factor, related to transforming growth factor-beta, that is produced by the surrounding ectoderm. The early limb also contains high levels of basic fibroblast growth factor. Its concentration is highest at the earliest stages, when cell proliferation and hyaluronate synthesis are prominent activities, and this factor has been shown to stimulate both these activities in cultures of limb mesodermal cells. Thus fibroblast growth factor and transforming growth factor-beta may be important in the regulation of early growth and morphogenesis of the limb.

Animals↗

Membrane-associated hyaluronate-binding activity of chondrosarcoma chondrocytes.

The association of hyaluronate with the surface of chondrocytes was examined by several approaches using primary cultures of chondrocytes derived from the Swarm rat chondrosarcoma. In culture, chondrosarcoma chondrocytes produced large pericellular coats, which can be visualized by particle exclusion, and which can be removed by Streptomyces hyaluronidase. Exposure of chondrocytes, which had been metabolically labelled with 3H-acetate, to exogenous hyaluronate or to Streptomyces hyaluronidase resulted in the release of 36-38% of the endogenous, labelled chondroitin sulfate from the cell layer into the incubation solution. These results imply that at least 37% of the cell layer chondroitin sulfate proteoglycan is retained there by an interaction with hyaluronate. Thus membranes were prepared from cultured chondrocytes and examined for sites which bind 3H-hyaluronate. Binding was observed and found to be saturable, specific for hyaluronate, of high affinity (Kd = approximately 10(-10) M), and destroyed by treating the membranes with trypsin. The 3H-hyaluronate-binding activity was inhibited competitively by hyaluronate decasaccharides but not by hexasaccharides or octasaccharides, indicating that the binding sites recognize a sequence of hyaluronate composed of five disaccharide repeats. The binding activity was partially purified from a detergent extract of chondrocyte membranes by ion exchange chromatography on DEAE-cellulose, followed by affinity chromatography on wheat germ agglutinin-agarose. Analysis of the partially purified binding activity by SDS-PAGE revealed five protein bands of 48,000-66,000 daltons in silver-stained gels. SDS-PAGE followed by Western blotting and exposure to monoclonal antibodies which recognize epitopes present in link protein and in the hyaluronate-binding region of cartilage proteoglycan revealed no immunoreactive protein bands in the partially purified material. We conclude that one mechanism by which hyaluronate associates with the chondrocyte surface may be via interaction with a membrane-bound hyaluronate-binding protein which is distinct from link protein and proteoglycan.

Animals↗