Heparin-binding EGF-like growth factor stimulation of smooth muscle cell migration: dependence on interactions with cell surface heparan sulfate

doi:10.1083/jcb.122.4.933

This Article

	Full Text (PDF, 952K)
	Alert me when this article is cited
	Citation Map

Services

	Email this article
	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new content in the JCB
	Download to citation manager

Citing Articles

	Citing Articles via HighWire
	Citing Articles via CrossRef
	Citing Articles via Google Scholar

Google Scholar

	Articles by Higashiyama, S.
	Articles by Klagsbrun, M.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Higashiyama, S.
	Articles by Klagsbrun, M.


Social Bookmarking

	What's this?

ARTICLES

Heparin-binding EGF-like growth factor stimulation of smooth muscle cell migration: dependence on interactions with cell surface heparan sulfate

S Higashiyama, JA Abraham and M Klagsbrun
Department of Biochemistry, Osaka University Medical School, Japan.

Heparin-binding EGF-like growth factor (HB-EGF), but not EGF, binds to cell surface heparan sulfate proteoglycan (HSPG). This was demonstrated in (a) the binding of 125I-HB-EGF to mutant CHO cells deficient in HS production was diminished by 70% compared to wild-type CHO cells, (b) the binding of 125I-HB-EGF to CHO cells and bovine aortic smooth muscle cells (BASMC) was diminished 80% by heparitinase or chlorate treatment, and (c) 125I-EGF did not bind to CHO cells and its binding to BASMC was not diminished at all by heparitinase and only slightly by chlorate treatment. Accordingly, the role of HB-EGF interactions with HSPG in modulating bioactivity was examined. Heparitinase or chlorate treatment of BASMC diminished the ability of HB-EGF to stimulate BASMC migration by 60-80%. A similar inhibition of migration occurred when BASMC were treated with a synthetic peptide (P21) corresponding to the sequence of the putative heparin-binding domain of HB-EGF. As a control for BASMC viability, and for specificity, it was found that heparitinase and P21 did not inhibit at all and chlorate inhibited only slightly the stimulation of BASMC migration by PDGF AB. Since heparitinase, chlorate, and P21 treatment also diminished by 70-80% the cross-linking of 125I-HB-EGF to the EGF receptor, it was concluded that the interaction of HB-EGF, via its heparin-binding domain, with cell surface HSPG was essential for its optimal binding to the EGF receptor on BASMC and hence for its optimal ability to stimulate migration.
Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Facebook Add to Reddit Reddit Add to Technorati Technorati Twitter What's this?

This article has been cited by other articles:

Das, S. K (2009). Cell cycle regulatory control for uterine stromal cell decidualization in implantation. Reproduction 137: 889-899 [Abstract] [Full Text]
Koide, M., Penar, P. L., Tranmer, B. I., Wellman, G. C. (2007). Heparin-binding EGF-like growth factor mediates oxyhemoglobin-induced suppression of voltage-dependent potassium channels in rabbit cerebral artery myocytes. Am. J. Physiol. Heart Circ. Physiol. 293: H1750-H1759 [Abstract] [Full Text]
Kageyama, T., Ohishi, M., Miyamoto, S., Mizushima, H., Iwamoto, R., Mekada, E. (2007). Diphtheria Toxin Mutant CRM197 Possesses Weak EF2-ADP-ribosyl Activity that Potentiates its Anti-tumorigenic Activity. J Biochem 142: 95-104 [Abstract] [Full Text]
Xu, K.-P., Yu, F.-S. X. (2007). Cross Talk between c-Met and Epidermal Growth Factor Receptor during Retinal Pigment Epithelial Wound Healing. IOVS 48: 2242-2248 [Abstract] [Full Text]
Novgorodov, A. S., El-Alwani, M., Bielawski, J., Obeid, L. M., Gudz, T. I. (2007). Activation of sphingosine-1-phosphate receptor S1P5 inhibits oligodendrocyte progenitor migration. FASEB J. 21: 1503-1514 [Abstract] [Full Text]
Gerthoffer, W. T. (2007). Mechanisms of Vascular Smooth Muscle Cell Migration. Circ. Res. 100: 607-621 [Abstract] [Full Text]
Akayama, Y., Takekida, S., Ohara, N., Tateiwa, H., Chen, W., Nakabayashi, K., Maruo, T. (2005). Gene expression and immunolocalization of heparin-binding epidermal growth factor-like growth factor and human epidermal growth factor receptors in human corpus luteum. Hum Reprod 20: 2708-2714 [Abstract] [Full Text]
Wang, J., Ohara, N., Takekida, S., Xu, Q., Maruo, T. (2005). Comparative effects of heparin-binding epidermal growth factor-like growth factor on the growth of cultured human uterine leiomyoma cells and myometrial cells. Hum Reprod 20: 1456-1465 [Abstract] [Full Text]
Zhang, H., Chalothorn, D., Jackson, L. F., Lee, D. C., Faber, J. E. (2004). Transactivation of Epidermal Growth Factor Receptor Mediates Catecholamine-Induced Growth of Vascular Smooth Muscle. Circ. Res. 95: 989-997 [Abstract] [Full Text]
Takazaki, R., Shishido, Y., Iwamoto, R., Mekada, E. (2004). Suppression of the Biological Activities of the Epidermal Growth Factor (EGF)-like Domain by the Heparin-binding Domain of Heparin-binding EGF-like Growth Factor. J. Biol. Chem. 279: 47335-47343 [Abstract] [Full Text]
Elenius, V., Gotte, M., Reizes, O., Elenius, K., Bernfield, M. (2004). Inhibition by the Soluble Syndecan-1 Ectodomains Delays Wound Repair in Mice Overexpressing Syndecan-1. J. Biol. Chem. 279: 41928-41935 [Abstract] [Full Text]
Shah, M. M., Sampogna, R. V., Sakurai, H., Bush, K. T., Nigam, S. K. (2004). Branching morphogenesis and kidney disease. Development 131: 1449-1462 [Abstract] [Full Text]
Anderson, H. D. I., Wang, F., Gardner, D. G. (2004). Role of the Epidermal Growth Factor Receptor in Signaling Strain-dependent Activation of the Brain Natriuretic Peptide Gene. J. Biol. Chem. 279: 9287-9297 [Abstract] [Full Text]
Schraufstatter, I. U., Trieu, K., Zhao, M., Rose, D. M., Terkeltaub, R. A., Burger, M. (2003). IL-8-Mediated Cell Migration in Endothelial Cells Depends on Cathepsin B Activity and Transactivation of the Epidermal Growth Factor Receptor. J. Immunol. 171: 6714-6722 [Abstract] [Full Text]
Liu, J., Rich, C. B., Buczek-Thomas, J. A., Nugent, M. A., Panchenko, M. P., Foster, J. A. (2003). Heparin-binding EGF-like growth factor regulates elastin and FGF-2 expression in pulmonary fibroblasts. Am. J. Physiol. Lung Cell. Mol. Physiol. 285: L1106-L1115 [Abstract] [Full Text]
IIVANAINEN, E., NELIMARKKA, L., ELENIUS, V., HEIKKINEN, S.-M., JUNTTILA, T. T., SIHOMBING, L., SUNDVALL, M., MAATTA, J. A., LAINE, V. J. O., YLA-HERTTUALA, S., HIGASHIYAMA, S., ALITALO, K., ELENIUS, K. (2003). Angiopoietin-regulated recruitment of vascular smooth muscle cells by endothelial-derived heparin binding EGF-like growth factor. FASEB J. 17: 1609-1621 [Abstract] [Full Text]
Lai, J., Chien, J., Staub, J., Avula, R., Greene, E. L., Matthews, T. A., Smith, D. I., Kaufmann, S. H., Roberts**, L. R., Shridhar**, V. (2003). Loss of HSulf-1 Up-regulates Heparin-binding Growth Factor Signaling in Cancer. J. Biol. Chem. 278: 23107-23117 [Abstract] [Full Text]
Iwamoto, R., Yamazaki, S., Asakura, M., Takashima, S., Hasuwa, H., Miyado, K., Adachi, S., Kitakaze, M., Hashimoto, K., Raab, G., Nanba, D., Higashiyama, S., Hori, M., Klagsbrun, M., Mekada, E. (2003). Heparin-binding EGF-like growth factor and ErbB signaling is essential for heart function. Proc. Natl. Acad. Sci. USA 100: 3221-3226 [Abstract] [Full Text]
Milenkovic, I., Weick, M., Wiedemann, P., Reichenbach, A., Bringmann, A. (2003). P2Y Receptor-Mediated Stimulation of Muller Glial Cell DNA Synthesis: Dependence on EGF and PDGF Receptor Transactivation. IOVS 44: 1211-1220 [Abstract] [Full Text]
van den Born, J., Pikas, D. S., Pisa, B. J.M., Eriksson, I., Kjellen, L., Berden, J. H.M. (2003). Antibody-based assay for N-deacetylase activity of heparan sulfate/heparin N-deacetylase/N-sulfotransferase (NDST): novel characteristics of NDST-1 and -2. Glycobiology 13: 1-10 [Abstract] [Full Text]
Mamluk, R., Gechtman, Z.'e., Kutcher, M. E., Gasiunas, N., Gallagher, J., Klagsbrun, M. (2002). Neuropilin-1 Binds Vascular Endothelial Growth Factor 165, Placenta Growth Factor-2, and Heparin via Its b1b2 Domain. J. Biol. Chem. 277: 24818-24825 [Abstract] [Full Text]
Grzeszkiewicz, T. M., Lindner, V., Chen, N., Lam, S. C.-T., Lau, L. F. (2002). The Angiogenic Factor Cysteine-Rich 61 (CYR61, CCN1) Supports Vascular Smooth Muscle Cell Adhesion and Stimulates Chemotaxis through Integrin {alpha}6{beta}1 and Cell Surface Heparan Sulfate Proteoglycans. Endocrinology 143: 1441-1450 [Abstract] [Full Text]
Yu, W.-H., Woessner, J. F. Jr., McNeish, J. D., Stamenkovic, I. (2002). CD44 anchors the assembly of matrilysin/MMP-7 with heparin-binding epidermal growth factor precursor and ErbB4 and regulates female reproductive organ remodeling. Genes Dev. 16: 307-323 [Abstract] [Full Text]
Matsuda, K., Maruyama, H., Guo, F., Kleeff, J., Itakura, J., Matsumoto, Y., Lander, A. D., Korc, M. (2001). Glypican-1 Is Overexpressed in Human Breast Cancer and Modulates the Mitogenic Effects of Multiple Heparin-binding Growth Factors in Breast Cancer Cells. Cancer Res. 61: 5562-5569 [Abstract] [Full Text]
TAKEMURA, T., HINO, S., KUWAJIMA, H., YANAGIDA, H., OKADA, M., NAGATA, M., SASAKI, S., BARASCH, J., HARRIS, R. C., YOSHIOKA, K. (2001). Induction of Collecting Duct Morphogenesis In Vitro by Heparin-Binding Epidermal Growth Factor-Like Growth Factor. J. Am. Soc. Nephrol. 12: 964-972 [Abstract] [Full Text]
Tokumaru, S., Higashiyama, S., Endo, T., Nakagawa, T., Miyagawa, J.-i., Yamamori, K., Hanakawa, Y., Ohmoto, H., Yoshino, K., Shirakata, Y., Matsuzawa, Y., Hashimoto, K., Taniguchi, N. (2000). Ectodomain Shedding of Epidermal Growth Factor Receptor Ligands Is Required for Keratinocyte Migration in Cutaneous Wound Healing. JCB 151: 209-220 [Abstract] [Full Text]
Nguyen, H. T., Bride, S. H., Badawy, A.-B., Adam, R. M., Lin, J., Orsola, A., Guthrie, P. D., Freeman, M. R., Peters, C. A. (2000). Heparin-Binding EGF-Like Growth Factor Is Up-Regulated in the Obstructed Kidney in a Cell- and Region-Specific Manner and Acts to Inhibit Apoptosis. Am. J. Pathol. 156: 889-898 [Abstract] [Full Text]
Wang, J, Mayernik, L, Schultz, J., Armant, D. (2000). Acceleration of trophoblast differentiation by heparin-binding EGF-like growth factor is dependent on the stage-specific activation of calcium influx by ErbB receptors in developing mouse blastocysts. Development 127: 33-44 [Abstract]
Vinante, F., Marchi, M., Rigo, A., Scapini, P., Pizzolo, G., Cassatella, M. A. (1999). Granulocyte-Macrophage Colony-Stimulating Factor Induces Expression of Heparin-Binding Epidermal Growth Factor-Like Growth Factor/Diphtheria Toxin Receptor and Sensitivity to Diphtheria Toxin in Human Neutrophils. Blood 94: 3169-3177 [Abstract] [Full Text]
Gechtman, Z.'e., Alonso, J. L., Raab, G., Ingber, D. E., Klagsbrun, M. (1999). The Shedding of Membrane-anchored Heparin-binding Epidermal-like Growth Factor Is Regulated by the Raf/Mitogen-activated Protein Kinase Cascade and by Cell Adhesion and Spreading. J. Biol. Chem. 274: 28828-28835 [Abstract] [Full Text]
Veugelers, M., De Cat, B., Ceulemans, H., Bruystens, A.-M., Coomans, C., Durr, J., Vermeesch, J., Marynen, P., David, G. (1999). Glypican-6, a New Member of the Glypican Family of Cell Surface Heparan Sulfate Proteoglycans. J. Biol. Chem. 274: 26968-26977 [Abstract] [Full Text]
Leach, R. E., Khalifa, R., Ramirez, N. D., Das, S. K., Wang, J., Dey, S. K., Romero, R., Armant, D. R. (1999). Multiple Roles for Heparin-Binding Epidermal Growth Factor-Like Growth Factor Are Suggested by Its Cell-Specific Expression during the Human Endometrial Cycle and Early Placentation. J. Clin. Endocrinol. Metab. 84: 3355-3363 [Abstract] [Full Text]
Clasper, S., Vekemans, S., Fiore, M., Plebanski, M., Wordsworth, P., David, G., Jackson, D. G. (1999). Inducible Expression of the Cell Surface Heparan Sulfate Proteoglycan Syndecan-2 (Fibroglycan) on Human Activated Macrophages Can Regulate Fibroblast Growth Factor Action. J. Biol. Chem. 274: 24113-24123 [Abstract] [Full Text]
Belting, M., Petersson, P. (1999). Intracellular Accumulation of Secreted Proteoglycans Inhibits Cationic Lipid-mediated Gene Transfer. CO-TRANSFER OF GLYCOSAMINOGLYCANS TO THE NUCLEUS. J. Biol. Chem. 274: 19375-19382 [Abstract] [Full Text]
Brigstock, D. R. (1999). The Connective Tissue Growth Factor/Cysteine- Rich 61/Nephroblastoma Overexpressed (CCN) Family. Endocr. Rev. 20: 189-206 [Abstract] [Full Text]
Wong, L., Deb, T. B., Thompson, S. A., Wells, A., Johnson, G. R. (1999). A Differential Requirement for the COOH-terminal Region of the Epidermal Growth Factor (EGF) Receptor in Amphiregulin and EGF Mitogenic Signaling. J. Biol. Chem. 274: 8900-8909 [Abstract] [Full Text]
Vinante, F., Rigo, A., Papini, E., Cassatella, M. A., Pizzolo, G. (1999). Heparin-Binding Epidermal Growth Factor-Like Growth Factor/Diphtheria Toxin Receptor Expression by Acute Myeloid Leukemia Cells. Blood 93: 1715-1723 [Abstract] [Full Text]
Hirschi, K. K., Rohovsky, S. A., Beck, L. H., Smith, S. R., D'Amore, P. A. (1999). Endothelial Cells Modulate the Proliferation of Mural Cell Precursors via Platelet-Derived Growth Factor-BB and Heterotypic Cell Contact. Circ. Res. 84: 298-305 [Abstract] [Full Text]
Newby, A. C, Zaltsman, A. B (1999). Fibrous cap formation or destruction -- the critical importance of vascular smooth muscle cell proliferation, migration and matrix formation. Cardiovasc Res 41: 345-360 [Abstract] [Full Text]
Paria, B., Elenius, K, Klagsbrun, M, Dey, S. (1999). Heparin-binding EGF-like growth factor interacts with mouse blastocysts independently of ErbB1: a possible role for heparan sulfate proteoglycans and ErbB4 in blastocyst implantation. Development 126: 1997-2005 [Abstract]
Tohda, G., Oida, K., Okada, Y., Kosaka, S., Okada, E., Takahashi, S., Ishii, H., Miyamori, I. (1998). Expression of Thrombomodulin in Atherosclerotic Lesions and Mitogenic Activity of Recombinant Thrombomodulin in Vascular Smooth Muscle Cells. Arterioscler. Thromb. Vasc. Bio. 18: 1861-1869 [Abstract] [Full Text]
Behar, T. N., Schaffner, A. E., Scott, C. A., O'Connell, C., Barker, J. L. (1998). Differential Response of Cortical Plate and Ventricular Zone Cells to GABA as a Migration Stimulus. J. Neurosci. 18: 6378-6387 [Abstract] [Full Text]
Koyama, N., Kinsella, M. G., Wight, T. N., Hedin, U., Clowes, A. W. (1998). Heparan Sulfate Proteoglycans Mediate a Potent Inhibitory Signal for Migration of Vascular Smooth Muscle Cells. Circ. Res. 83: 305-313 [Abstract] [Full Text]
Muranaka, Y., Yamasaki, Y., Nozawa, Y., Terakawa, H., Tanahashi, Y., Oda, N., Satoh, A., Asao, T., Miyake, H., Matsuura, N. (1998). TAS-301, an Inhibitor of Smooth Muscle Cell Migration and Proliferation, Inhibits Intimal Thickening after Balloon Injury to Rat Carotid Arteries. J. Pharmacol. Exp. Ther. 285: 1280-1286 [Abstract] [Full Text]
Fujino, T., Hasebe, N., Fujita, M., Takeuchi, K., Kawabe, J.-i., Tobise, K., Higashiyama, S., Taniguchi, N., Kikuchi, K. (1998). Enhanced expression of heparin-binding EGF-like growth factor and its receptor in hypertrophied left ventricle of spontaneously hypertensive rats. Cardiovasc Res 38: 365-374 [Abstract] [Full Text]
Jayson, G. C., Lyon, M., Paraskeva, C., Turnbull, J. E., Deakin, J. A., Gallagher, J. T. (1998). Heparan Sulfate Undergoes Specific Structural Changes during the Progression from Human Colon Adenoma to Carcinoma in Vitro. J. Biol. Chem. 273: 51-57 [Abstract] [Full Text]
Suzuki, M., Raab, G., Moses, M. A., Fernandez, C. A., Klagsbrun, M. (1997). Matrix Metalloproteinase-3 Releases Active Heparin-binding EGF-like Growth Factor by Cleavage at a Specific Juxtamembrane Site. J. Biol. Chem. 272: 31730-31737 [Abstract] [Full Text]
Kenagy, R. D., Hart, C. E., Stetler-Stevenson, W. G., Clowes, A. W. (1997). Primate Smooth Muscle Cell Migration From Aortic Explants Is Mediated by Endogenous Platelet-Derived Growth Factor and Basic Fibroblast Growth Factor Acting Through Matrix Metalloproteinases 2 and 9. Circulation 96: 3555-3560 [Abstract] [Full Text]
Kaneto, H., Miyagawa, J.-i., Kajimoto, Y., Yamamoto, K., Watada, H., Umayahara, Y., Hanafusa, T., Matsuzawa, Y., Yamasaki, Y., Higashiyama, S., Taniguchi, N. (1997). Expression of Heparin-binding Epidermal Growth Factor-like Growth Factor during Pancreas Development. A POTENTIAL ROLE OF PDX-1 IN TRANSCRIPTIONAL ACTIVATION. J. Biol. Chem. 272: 29137-29143 [Abstract] [Full Text]
Fukuda, K., Kawata, S., Inui, Y., Higashiyama, S., Matsuda, Y., Igura, T., Tamura, S., Taniguchi, N., Matsuzawa, Y. (1997). High Concentration of Glucose Increases Mitogenic Responsiveness to Heparin-Binding Epidermal Growth Factor�like Growth Factor in Rat Vascular Smooth Muscle Cells. Arterioscler. Thromb. Vasc. Bio. 17: 1962-1968 [Abstract] [Full Text]
Brigstock, D. R., Steffen, C. L., Kim, G. Y., Vegunta, R. K., Diehl, J. R., Harding, P. A. (1997). Purification and Characterization of Novel Heparin-binding Growth Factors in Uterine Secretory Fluids. IDENTIFICATION AS HEPARIN-REGULATED Mr 10,000�FORMS OF CONNECTIVE TISSUE GROWTH FACTOR. J. Biol. Chem. 272: 20275-20282 [Abstract] [Full Text]
Cizmeci-Smith, G., Langan, E., Youkey, J., Showalter, L. J., Carey, D. J. (1997). Syndecan-4 Is a Primary-Response Gene Induced by Basic Fibroblast Growth Factor and Arterial Injury in Vascular Smooth Muscle Cells. Arterioscler. Thromb. Vasc. Bio. 17: 172-180 [Abstract] [Full Text]
Igura, T., Kawata, S., Miyagawa, J.-i., Inui, Y., Tamura, S., Fukuda, K., Isozaki, K., Yamamori, K., Taniguchi, N., Higashiyama, S., Matsuzawa, Y. (1996). Expression of Heparin-Binding Epidermal Growth Factor�Like Growth Factor in Neointimal Cells Induced by Balloon Injury in Rat Carotid Arteries. Arterioscler. Thromb. Vasc. Bio. 16: 1524-1531 [Abstract] [Full Text]
Nakata, A., Miyagawa, J.-i., Yamashita, S., Nishida, M., Tamura, R., Yamamori, K., Nakamura, T., Nozaki, S., Kameda-Takemura, K., Kawata, S., Taniguchi, N., Higashiyama, S., Matsuzawa, Y. (1996). Localization of Heparin-Binding Epidermal Growth Factor�Like Growth Factor in Human Coronary Arteries: Possible Roles of HB-EGF in the Formation of Coronary Atherosclerosis. Circulation 94: 2778-2786 [Abstract] [Full Text]
Nakagawa, T., Higashiyama, S., Mitamura, T., Mekada, E., Taniguchi, N. (1996). Amino-terminal Processing of Cell Surface Heparin-binding Epidermal Growth Factor-like Growth Factor Up-regulates Its Juxtacrine but Not Its Paracrine Growth Factor Activity. J. Biol. Chem. 271: 30858-30863 [Abstract] [Full Text]
Inaba, T., Ishibashi, S., Harada, K., Ohsuga, J.-i., Ohashi, K., Yagyu, H., Yazaki, Y., Higashiyama, S., Kawata, S., Matsuzawa, Y., Yamada, N. (1996). Induction of Macrophage Colony-stimulating Factor Receptor (c-fms) Expression in Vascular Medial Smooth Muscle Cells Treated with Heparin Binding Epidermal Growth Factor-like Growth Factor. J. Biol. Chem. 271: 24413-24417 [Abstract] [Full Text]
Kainulainen, V., Nelimarkka, L., Jarvelainen, H., Laato, M., Jalkanen, M., Elenius, K. (1996). Suppression of Syndecan-1 Expression in Endothelial Cells by Tumor Necrosis Factor-alpha. J. Biol. Chem. 271: 18759-18766 [Abstract] [Full Text]
Peifley, K. A., Alberts, G. F., Hsu, D. K.W., Feng, S.-L. Y., Winkles, J. A. (1996). Heparin-Binding Epidermal Growth Factor-Like Growth Factor Regulates Fibroblast Growth Factor-2 Expression in Aortic Smooth Muscle Cells. Circ. Res. 79: 263-270 [Abstract] [Full Text]
Thompson, S. A., Harris, A., Hoang, D., Ferrer, M., Johnson, G. R. (1996). COOH-terminal Extended Recombinant Amphiregulin with Bioactivity Comparable with Naturally Derived Growth Factor. J. Biol. Chem. 271: 17927-17931 [Abstract] [Full Text]
Rossi, S. G., Rotundo, R. L. (1996). Transient Interactions between Collagen-tailed Acetylcholinesterase and Sulfated Proteoglycans Prior to Immobilization on the Extracellular Matrix. J. Biol. Chem. 271: 1979-1987 [Abstract] [Full Text]
Raab, G, Kover, K, Paria, B., Dey, S., Ezzell, R., Klagsbrun, M (1996). Mouse preimplantation blastocysts adhere to cells expressing the transmembrane form of heparin-binding EGF-like growth factor. Development 122: 637-645 [Abstract]
Shishido, Y., Sharma, K. D., Higashiyama, S., Klagsbrun, M., Mekada, E. (1995). Heparin-like Molecules on the Cell Surface Potentiate Binding of Diphtheria Toxin to the Diphtheria Toxin Receptor/Membrane-anchored Heparin-binding Epidermal Growth Factor-like Growth Factor. J. Biol. Chem. 270: 29578-29585 [Abstract] [Full Text]
Fukuda, K., Inui, Y., Kawata, S., Higashiyama, S., Matsuda, Y., Maeda, Y., Igura, T., Yoshida, S., Taniguchi, N., Matsuzawa, Y. (1995). Increased Mitogenic Response to Heparin-Binding Epidermal Growth Factor�like Growth Factor in Vascular Smooth Muscle Cells of Diabetic Rats. Arterioscler. Thromb. Vasc. Bio. 15: 1680-1687 [Abstract] [Full Text]
McCarthy, S A, Samuels, M L, Pritchard, C A, Abraham, J A, McMahon, M (1995). Rapid induction of heparin-binding epidermal growth factor/diphtheria toxin receptor expression by Raf and Ras oncogenes.. Genes Dev. 9: 1953-1964 [Abstract]
Chen, X., Raab, G., Deutsch, U., Zhang, J., Ezzell, R. M., Klagsbrun, M. (1995). Induction of Heparin-binding EGF-like Growth Factor Expression during Myogenesis. J. Biol. Chem. 270: 18285-18294 [Abstract] [Full Text]
Pan, Z., Kravchenko, V. V., Ye, R. D. (1995). Platelet-activating Factor Stimulates Transcription of the Heparin-binding Epidermal Growth Factor-like Growth Factor in Monocytes. J. Biol. Chem. 270: 7787-7790 [Abstract] [Full Text]
Elenius, K, Jalkanen, M (1994). Function of the syndecans--a family of cell surface proteoglycans. J. Cell Sci. 107: 2975-2982
Mesri, E., Ono, M, Kreitman, R., Klagsbrun, M, Pastan, I (1994). The heparin-binding domain of heparin-binding EGF-like growth factor can target Pseudomonas exotoxin to kill cells exclusively through heparan sulfate proteoglycans. J. Cell Sci. 107: 2599-2608 [Abstract]
Li, Q., Loeb, J. A. (2001). Neuregulin-Heparan-sulfate Proteoglycan Interactions Produce Sustained erbB Receptor Activation Required for the Induction of Acetylcholine Receptors in Muscle. J. Biol. Chem. 276: 38068-38075 [Abstract] [Full Text]