The metalloprotease Kuzbanian (ADAM10) mediates the transactivation of EGF receptor by G protein-coupled receptors

doi:10.1083/jcb.200112026

Published online 15 July 2002. doi:10.1083/jcb.200112026
The Rockefeller University Press, 0021-9525 $8.00
The Journal of Cell Biology

This Article

	Full Text
	Full Text (PDF, 180K)
	PPT slides of all figures
	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 Yan, Y.
	Articles by Werb, Z.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Yan, Y.
	Articles by Werb, Z.


Social Bookmarking

	What's this?

Article

The metalloprotease Kuzbanian (ADAM10) mediates the transactivation of EGF receptor by G protein–coupled receptors

Yibing Yan, Kyoko Shirakabe and Zena Werb

Department of Anatomy, University of California, San Francisco, CA 94143

Address correspondence to Zena Werb, Department of Anatomy, HSW 1321, University of California, 513 Parnassus Ave., San Francisco, CA 94143-0452. Tel.: (415) 476-4622. Fax: (415) 476-4565. E-mail: zena{at}itsa.ucsf.edu

Communication between different signaling pathways enables cellsto coordinate the responses to diverse environmental signals.Activation of the transmembrane growth factor precursors playsa critical role in this communication and often involves metalloprotease-mediatedproteolysis. Stimulation of G protein–coupled receptors(GPCR) transactivates the EGF receptors (EGFRs), which occursvia a metalloprotease-dependent cleavage of heparin-bindingEGF (HB-EGF). However, the metalloprotease mediating the transactivationremains elusive. We show that the integral membrane metalloproteaseKuzbanian (KUZ; ADAM10), which controls Notch signaling in Drosophila,stimulates GPCR transactivation of EGFR. Upon stimulation ofthe bombesin receptors, KUZ increases the docking and activationof adaptors Src homology 2 domain–containing protein andGab1 on the EGFR, and activation of Ras and Erk. In contrast,transfection of a protease domain–deleted KUZ, or blockingendogenous KUZ by morpholino antisense oligonucleotides, suppressesthe transactivation. The effect of KUZ on shedding of HB-EGFand consequent transactivation of the EGFR depends on its metalloproteaseactivity. GPCR activation enhances the association of KUZ andits substrate HB-EGF with tetraspanin CD9. Thus, KUZ regulatesthe relay between the GPCR and EGFR signaling pathways.

Key Words: signal crosstalk; bombesin; HB-EGF; shedding; tetraspanin

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:

Myers, T. J., Brennaman, L. H., Stevenson, M., Higashiyama, S., Russell, W. E., Lee, D. C., Sunnarborg, S. W. (2009). Mitochondrial Reactive Oxygen Species Mediate GPCR-induced TACE/ADAM17-dependent Transforming Growth Factor-{alpha} Shedding. Mol. Biol. Cell 20: 5236-5249 [Abstract] [Full Text]
Yin, J., Yu, F.-S. X. (2009). ERK1/2 Mediate Wounding- and G-protein-Coupled Receptor Ligands-Induced EGFR Activation via Regulating ADAM17 and HB-EGF Shedding. IOVS 50: 132-139 [Abstract] [Full Text]
Arduise, C., Abache, T., Li, L., Billard, M., Chabanon, A., Ludwig, A., Mauduit, P., Boucheix, C., Rubinstein, E., Le Naour, F. (2008). Tetraspanins Regulate ADAM10-Mediated Cleavage of TNF-{alpha} and Epidermal Growth Factor. J. Immunol. 181: 7002-7013 [Abstract] [Full Text]
Rodland, K. D., Bollinger, N., Ippolito, D., Opresko, L. K., Coffey, R. J., Zangar, R., Wiley, H. S. (2008). Multiple Mechanisms Are Responsible for Transactivation of the Epidermal Growth Factor Receptor in Mammary Epithelial Cells. J. Biol. Chem. 283: 31477-31487 [Abstract] [Full Text]
Barreiro, O., Zamai, M., Yanez-Mo, M., Tejera, E., Lopez-Romero, P., Monk, P. N., Gratton, E., Caiolfa, V. R., Sanchez-Madrid, F. (2008). Endothelial adhesion receptors are recruited to adherent leukocytes by inclusion in preformed tetraspanin nanoplatforms. JCB 183: 527-542 [Abstract] [Full Text]
Yanez-Mo, M., Barreiro, O., Gonzalo, P., Batista, A., Megias, D., Genis, L., Sachs, N., Sala-Valdes, M., Alonso, M. A., Montoya, M. C., Sonnenberg, A., Arroyo, A. G., Sanchez-Madrid, F. (2008). MT1-MMP collagenolytic activity is regulated through association with tetraspanin CD151 in primary endothelial cells. Blood 112: 3217-3226 [Abstract] [Full Text]
Shimura, T., Kataoka, H., Ogasawara, N., Kubota, E., Sasaki, M., Tanida, S., Joh, T. (2008). Suppression of proHB-EGF Carboxy-Terminal Fragment Nuclear Translocation: A New Molecular Target Therapy for Gastric Cancer. Clin. Cancer Res. 14: 3956-3965 [Abstract] [Full Text]
Buvinic, S., Bravo-Zehnder, M., Boyer, J. L., Huidobro-Toro, J. P., Gonzalez, A. (2007). Nucleotide P2Y1 receptor regulates EGF receptor mitogenic signaling and expression in epithelial cells. J. Cell Sci. 120: 4289-4301 [Abstract] [Full Text]
Zigrino, P., Steiger, J., Fox, J. W., Loffek, S., Schild, A., Nischt, R., Mauch, C. (2007). Role of ADAM-9 Disintegrin-Cysteine-rich Domains in Human Keratinocyte Migration. J. Biol. Chem. 282: 30785-30793 [Abstract] [Full Text]
Forster, K., Kuno, A., Solenkova, N., Felix, S. B., Krieg, T. (2007). The {delta}-opioid receptor agonist DADLE at reperfusion protects the heart through activation of pro-survival kinases via EGF receptor transactivation. Am. J. Physiol. Heart Circ. Physiol. 293: H1604-H1608 [Abstract] [Full Text]
Langlois, S., Nyalendo, C., Di Tomasso, G., Labrecque, L., Roghi, C., Murphy, G., Gingras, D., Beliveau, R. (2007). Membrane-Type 1 Matrix Metalloproteinase Stimulates Cell Migration through Epidermal Growth Factor Receptor Transactivation. Mol Cancer Res 5: 569-583 [Abstract] [Full Text]
Kinugasa, Y., Hieda, M., Hori, M., Higashiyama, S. (2007). The Carboxyl-terminal Fragment of Pro-HB-EGF Reverses Bcl6-mediated Gene Repression. J. Biol. Chem. 282: 14797-14806 [Abstract] [Full Text]
Fridman, J. S., Caulder, E., Hansbury, M., Liu, X., Yang, G., Wang, Q., Lo, Y., Zhou, B.-B., Pan, M., Thomas, S. M., Grandis, J. R., Zhuo, J., Yao, W., Newton, R. C., Friedman, S. M., Scherle, P. A., Vaddi, K. (2007). Selective Inhibition of ADAM Metalloproteases as a Novel Approach for Modulating ErbB Pathways in Cancer. Clin. Cancer Res. 13: 1892-1902 [Abstract] [Full Text]
Horiuchi, K., Le Gall, S., Schulte, M., Yamaguchi, T., Reiss, K., Murphy, G., Toyama, Y., Hartmann, D., Saftig, P., Blobel, C. P. (2007). Substrate Selectivity of Epidermal Growth Factor-Receptor Ligand Sheddases and their Regulation by Phorbol Esters and Calcium Influx. Mol. Biol. Cell 18: 176-188 [Abstract] [Full Text]
Nishi, E., Hiraoka, Y., Yoshida, K., Okawa, K., Kita, T. (2006). Nardilysin Enhances Ectodomain Shedding of Heparin-binding Epidermal Growth Factor-like Growth Factor through Activation of Tumor Necrosis Factor-{alpha}-converting Enzyme. J. Biol. Chem. 281: 31164-31172 [Abstract] [Full Text]
Chansel, D., Ciroldi, M., Vandermeersch, S., Jackson, L. F, Gomez, A.-M., Henrion, D., Lee, D. C., Coffman, T. M., Richard, S., Dussaule, J.-C., Tharaux, P.-L. (2006). Heparin binding EGF is necessary for vasospastic response to endothelin. FASEB J. 20: 1936-1938 [Abstract] [Full Text]
Gooz, M., Gooz, P., Luttrell, L. M., Raymond, J. R. (2006). 5-HT2A Receptor Induces ERK Phosphorylation and Proliferation through ADAM-17 Tumor Necrosis Factor-{alpha}-converting Enzyme (TACE) Activation and Heparin-bound Epidermal Growth Factor-like Growth Factor (HB-EGF) Shedding in Mesangial Cells. J. Biol. Chem. 281: 21004-21012 [Abstract] [Full Text]
Ohtsu, H., Dempsey, P. J., Eguchi, S. (2006). ADAMs as mediators of EGF receptor transactivation by G protein-coupled receptors. Am. J. Physiol. Cell Physiol. 291: C1-C10 [Abstract] [Full Text]
Huang, L. C., Petkova, T. D., Reins, R. Y., Proske, R. J., McDermott, A. M. (2006). Multifunctional Roles of Human Cathelicidin (LL-37) at the Ocular Surface.. IOVS 47: 2369-2380 [Abstract] [Full Text]
Yang, X. H., Kovalenko, O. V., Kolesnikova, T. V., Andzelm, M. M., Rubinstein, E., Strominger, J. L., Hemler, M. E. (2006). Contrasting Effects of EWI Proteins, Integrins, and Protein Palmitoylation on Cell Surface CD9 Organization. J. Biol. Chem. 281: 12976-12985 [Abstract] [Full Text]
Zhang, Q., Thomas, S. M., Lui, V. W. Y., Xi, S., Siegfried, J. M., Fan, H., Smithgall, T. E., Mills, G. B., Grandis, J. R. (2006). Phosphorylation of TNF-{alpha} converting enzyme by gastrin-releasing peptide induces amphiregulin release and EGF receptor activation. Proc. Natl. Acad. Sci. USA 103: 6901-6906 [Abstract] [Full Text]
Le Naour, F., Andre, M., Greco, C., Billard, M., Sordat, B., Emile, J.-F., Lanza, F., Boucheix, C., Rubinstein, E. (2006). Profiling of the Tetraspanin Web of Human Colon Cancer Cells. Mol. Cell. Proteomics 5: 845-857 [Abstract] [Full Text]
Chattopadhyay, N. (2006). Effects of calcium-sensing receptor on the secretion of parathyroid hormone-related peptide and its impact on humoral hypercalcemia of malignancy. Am. J. Physiol. Endocrinol. Metab. 290: E761-E770 [Abstract] [Full Text]
Conti, M., Hsieh, M., Park, J.-Y., Su, Y.-Q. (2006). Role of the Epidermal Growth Factor Network in Ovarian Follicles. Mol. Endocrinol. 20: 715-723 [Abstract] [Full Text]
Vasyutina, E., Stebler, J., Brand-Saberi, B., Schulz, S., Raz, E., Birchmeier, C. (2005). CXCR4 and Gab1 cooperate to control the development of migrating muscle progenitor cells. Genes Dev. 19: 2187-2198 [Abstract] [Full Text]
Belcheva, M. M., Clark, A. L., Haas, P. D., Serna, J. S., Hahn, J. W., Kiss, A., Coscia, C. J. (2005). {micro} and {kappa} Opioid Receptors Activate ERK/MAPK via Different Protein Kinase C Isoforms and Secondary Messengers in Astrocytes. J. Biol. Chem. 280: 27662-27669 [Abstract] [Full Text]
Mifune, M., Ohtsu, H., Suzuki, H., Nakashima, H., Brailoiu, E., Dun, N. J., Frank, G. D., Inagami, T., Higashiyama, S., Thomas, W. G., Eckhart, A. D., Dempsey, P. J., Eguchi, S. (2005). G Protein Coupling and Second Messenger Generation Are Indispensable for Metalloprotease-dependent, Heparin-binding Epidermal Growth Factor Shedding through Angiotensin II Type-1 Receptor. J. Biol. Chem. 280: 26592-26599 [Abstract] [Full Text]
Braun, A. H., Coffey, R. J. (2005). Lysophosphatidic Acid, a Disintegrin and Metalloprotease-17 and Heparin-Binding Epidermal Growth Factor-Like Growth Factor in Ovarian Cancer: The First Word, Not the Last. Clin. Cancer Res. 11: 4639-4643 [Full Text]
Tanaka, Y., Miyamoto, S., Suzuki, S. O., Oki, E., Yagi, H., Sonoda, K., Yamazaki, A., Mizushima, H., Maehara, Y., Mekada, E., Nakano, H. (2005). Clinical Significance of Heparin-Binding Epidermal Growth Factor-Like Growth Factor and A Disintegrin and Metalloprotease 17 Expression in Human Ovarian Cancer. Clin. Cancer Res. 11: 4783-4792 [Abstract] [Full Text]
Dong, J., Opresko, L. K., Chrisler, W., Orr, G., Quesenberry, R. D., Lauffenburger, D. A., Wiley, H. S. (2005). The Membrane-anchoring Domain of Epidermal Growth Factor Receptor Ligands Dictates Their Ability to Operate in Juxtacrine Mode. Mol. Biol. Cell 16: 2984-2998 [Abstract] [Full Text]
Stewart, J. R., O'Brian, C. A. (2005). Protein kinase C-{alpha} mediates epidermal growth factor receptor transactivation in human prostate cancer cells. Molecular Cancer Therapeutics 4: 726-732 [Abstract] [Full Text]
Jo, M., Thomas, K. S., Marozkina, N., Amin, T. J., Silva, C. M., Parsons, S. J., Gonias, S. L. (2005). Dynamic Assembly of the Urokinase-type Plasminogen Activator Signaling Receptor Complex Determines the Mitogenic Activity of Urokinase-type Plasminogen Activator. J. Biol. Chem. 280: 17449-17457 [Abstract] [Full Text]
Braff, M. H., Hawkins, M. A., Nardo, A. D., Lopez-Garcia, B., Howell, M. D., Wong, C., Lin, K., Streib, J. E., Dorschner, R., Leung, D. Y. M., Gallo, R. L. (2005). Structure-Function Relationships among Human Cathelicidin Peptides: Dissociation of Antimicrobial Properties from Host Immunostimulatory Activities. J. Immunol. 174: 4271-4278 [Abstract] [Full Text]
Sanderson, M. P., Erickson, S. N., Gough, P. J., Garton, K. J., Wille, P. T., Raines, E. W., Dunbar, A. J., Dempsey, P. J. (2005). ADAM10 Mediates Ectodomain Shedding of the Betacellulin Precursor Activated by p-Aminophenylmercuric Acetate and Extracellular Calcium Influx. J. Biol. Chem. 280: 1826-1837 [Abstract] [Full Text]
Sundberg, C., Thodeti, C. K., Kveiborg, M., Larsson, C., Parker, P., Albrechtsen, R., Wewer, U. M. (2004). Regulation of ADAM12 Cell-surface Expression by Protein Kinase C {epsilon}. J. Biol. Chem. 279: 51601-51611 [Abstract] [Full Text]
Bierkamp, C., Bonhoure, S., Mathieu, A., Clerc, P., Fourmy, D., Pradayrol, L., Seva, C., Dufresne, M. (2004). Expression of Cholecystokinin-2/Gastrin Receptor in the Murine Pancreas Modulates Cell Adhesion and Cell Differentiation in Vivo. Am. J. Pathol. 165: 2135-2145 [Abstract] [Full Text]
Schafer, B., Marg, B., Gschwind, A., Ullrich, A. (2004). Distinct ADAM Metalloproteinases Regulate G Protein-coupled Receptor-induced Cell Proliferation and Survival. J. Biol. Chem. 279: 47929-47938 [Abstract] [Full Text]
Zhao, D., Zhan, Y., Koon, H. W., Zeng, H., Keates, S., Moyer, M. P., Pothoulakis, C. (2004). Metalloproteinase-dependent Transforming Growth Factor-{alpha} Release Mediates Neurotensin-stimulated MAP Kinase Activation in Human Colonic Epithelial Cells. J. Biol. Chem. 279: 43547-43554 [Abstract] [Full Text]
Sauer, B., Vogler, R., von Wenckstern, H., Fujii, M., Anzano, M. B., Glick, A. B., Schafer-Korting, M., Roberts, A. B., Kleuser, B. (2004). Involvement of Smad Signaling in Sphingosine 1-Phosphate-mediated Biological Responses of Keratinocytes. J. Biol. Chem. 279: 38471-38479 [Abstract] [Full Text]
Argast, G. M., Campbell, J. S., Brooling, J. T., Fausto, N. (2004). Epidermal Growth Factor Receptor Transactivation Mediates Tumor Necrosis Factor-induced Hepatocyte Replication. J. Biol. Chem. 279: 34530-34536 [Abstract] [Full Text]
Shao, M. X. G., Nakanaga, T., Nadel, J. A. (2004). Cigarette smoke induces MUC5AC mucin overproduction via tumor necrosis factor-{alpha}-converting enzyme in human airway epithelial (NCI-H292) cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 287: L420-L427 [Abstract] [Full Text]
Kim, J. H., Lee, S. Y., Bak, S. M., Suh, I. B., Lee, S. Y., Shin, C., Shim, J. J., In, K. H., Kang, K. H., Yoo, S. H. (2004). Effects of matrix metalloproteinase inhibitor on LPS-induced goblet cell metaplasia. Am. J. Physiol. Lung Cell. Mol. Physiol. 287: L127-L133 [Abstract] [Full Text]
Nagano, O., Murakami, D., Hartmann, D., de Strooper, B., Saftig, P., Iwatsubo, T., Nakajima, M., Shinohara, M., Saya, H. (2004). Cell-matrix interaction via CD44 is independently regulated by different metalloproteinases activated in response to extracellular Ca2+ influx and PKC activation. JCB 165: 893-902 [Abstract] [Full Text]
Fischer, O. M., Hart, S., Gschwind, A., Prenzel, N., Ullrich, A. (2004). Oxidative and Osmotic Stress Signaling in Tumor Cells Is Mediated by ADAM Proteases and Heparin-Binding Epidermal Growth Factor. Mol. Cell. Biol. 24: 5172-5183 [Abstract] [Full Text]
Hinkle, C. L., Sunnarborg, S. W., Loiselle, D., Parker, C. E., Stevenson, M., Russell, W. E., Lee, D. C. (2004). Selective Roles for Tumor Necrosis Factor {alpha}-converting Enzyme/ADAM17 in the Shedding of the Epidermal Growth Factor Receptor Ligand Family: THE JUXTAMEMBRANE STALK DETERMINES CLEAVAGE EFFICIENCY. J. Biol. Chem. 279: 24179-24188 [Abstract] [Full Text]
Little, K. D., Hemler, M. E., Stipp, C. S. (2004). Dynamic Regulation of a GPCR-Tetraspanin-G Protein Complex on Intact Cells: Central Role of CD81 in Facilitating GPR56-G{alpha}q/11 Association. Mol. Biol. Cell 15: 2375-2387 [Abstract] [Full Text]
Ludeman, M. J., Zheng, Y. W., Ishii, K., Coughlin, S. R. (2004). Regulated Shedding of PAR1 N-terminal Exodomain from Endothelial Cells. J. Biol. Chem. 279: 18592-18599 [Abstract] [Full Text]
Wu, W., Samet, J. M., Silbajoris, R., Dailey, L. A., Sheppard, D., Bromberg, P. A., Graves, L. M. (2004). Heparin-Binding Epidermal Growth Factor Cleavage Mediates Zinc-Induced Epidermal Growth Factor Receptor Phosphorylation. Am. J. Respir. Cell Mol. Bio. 30: 540-547 [Abstract] [Full Text]
Hart, S., Fischer, O. M., Ullrich, A. (2004). Cannabinoids Induce Cancer Cell Proliferation via Tumor Necrosis Factor {alpha}-Converting Enzyme (TACE/ADAM17)-Mediated Transactivation of the Epidermal Growth Factor Receptor. Cancer Res. 64: 1943-1950 [Abstract] [Full Text]
Gough, P. J., Garton, K. J., Wille, P. T., Rychlewski, M., Dempsey, P. J., Raines, E. W. (2004). A Disintegrin and Metalloproteinase 10-Mediated Cleavage and Shedding Regulates the Cell Surface Expression of CXC Chemokine Ligand 16. J. Immunol. 172: 3678-3685 [Abstract] [Full Text]
Singh, A. B., Tsukada, T., Zent, R., Harris, R. C. (2004). Membrane-associated HB-EGF modulates HGF-induced cellular responses in MDCK cells. J. Cell Sci. 117: 1365-1379 [Abstract] [Full Text]
Sahin, U., Weskamp, G., Kelly, K., Zhou, H.-M., Higashiyama, S., Peschon, J., Hartmann, D., Saftig, P., Blobel, C. P. (2004). Distinct roles for ADAM10 and ADAM17 in ectodomain shedding of six EGFR ligands. JCB 164: 769-779 [Abstract] [Full Text]
Bertelsen, L. S., Barrett, K. E., Keely, S. J. (2004). Gs Protein-coupled Receptor Agonists Induce Transactivation of the Epidermal Growth Factor Receptor in T84 Cells: IMPLICATIONS FOR EPITHELIAL SECRETORY RESPONSES. J. Biol. Chem. 279: 6271-6279 [Abstract] [Full Text]
Weskamp, G., Schlondorff, J., Lum, L., Becherer, J. D., Kim, T.-W., Saftig, P., Hartmann, D., Murphy, G., Blobel, C. P. (2004). Evidence for a Critical Role of the Tumor Necrosis Factor {alpha} Convertase (TACE) in Ectodomain Shedding of the p75 Neurotrophin Receptor (p75NTR). J. Biol. Chem. 279: 4241-4249 [Abstract] [Full Text]
Kohlstedt, K., Brandes, R. P., Muller-Esterl, W., Busse, R., Fleming, I. (2004). Angiotensin-Converting Enzyme Is Involved in Outside-In Signaling in Endothelial Cells. Circ. Res. 94: 60-67 [Abstract] [Full Text]
Hao, L., Du, M., Lopez-Campistrous, A., Fernandez-Patron, C. (2004). Agonist-Induced Activation of Matrix Metalloproteinase-7 Promotes Vasoconstriction Through the Epidermal Growth Factor-Receptor Pathway. Circ. Res. 94: 68-76 [Abstract] [Full Text]
Shah, B. H., Farshori, M. P., Catt, K. J. (2004). Neuropeptide-induced Transactivation of a Neuronal Epidermal Growth Factor Receptor Is Mediated by Metalloprotease-dependent Formation of Heparin-binding Epidermal Growth Factor. J. Biol. Chem. 279: 414-420 [Abstract] [Full Text]
McCulloch, D. R., Akl, P., Samaratunga, H., Herington, A. C., Odorico, D. M. (2004). Expression of the Disintegrin Metalloprotease, ADAM-10, in Prostate Cancer and Its Regulation by Dihydrotestosterone, Insulin-Like Growth Factor I, and Epidermal Growth Factor in the Prostate Cancer Cell Model LNCaP. Clin. Cancer Res. 10: 314-323 [Abstract] [Full Text]
Tjabringa, G. S., Aarbiou, J., Ninaber, D. K., Drijfhout, J. W., Sorensen, O. E., Borregaard, N., Rabe, K. F., Hiemstra, P. S. (2003). The Antimicrobial Peptide LL-37 Activates Innate Immunity at the Airway Epithelial Surface by Transactivation of the Epidermal Growth Factor Receptor. J. Immunol. 171: 6690-6696 [Abstract] [Full Text]
Belcheva, M. M., Tan, Y., Heaton, V. M., Clark, A. L., Coscia, C. J. (2003). {micro} Opioid Transactivation and Down-Regulation of the Epidermal Growth Factor Receptor in Astrocytes: Implications for Mitogen-Activated Protein Kinase Signaling. Mol. Pharmacol. 64: 1391-1401 [Abstract] [Full Text]
Gardner, O. S., Dewar, B. J., Earp, H. S., Samet, J. M., Graves, L. M. (2003). Dependence of Peroxisome Proliferator-activated Receptor Ligand-induced Mitogen-activated Protein Kinase Signaling on Epidermal Growth Factor Receptor Transactivation. J. Biol. Chem. 278: 46261-46269 [Abstract] [Full Text]
Mori, S., Tanaka, M., Nanba, D., Nishiwaki, E., Ishiguro, H., Higashiyama, S., Matsuura, N. (2003). PACSIN3 Binds ADAM12/Meltrin {alpha} and Up-regulates Ectodomain Shedding of Heparin-binding Epidermal Growth Factor-like Growth Factor. J. Biol. Chem. 278: 46029-46034 [Abstract] [Full Text]
Nanba, D., Mammoto, A., Hashimoto, K., Higashiyama, S. (2003). Proteolytic release of the carboxy-terminal fragment of proHB-EGF causes nuclear export of PLZF. JCB 163: 489-502 [Abstract] [Full Text]
Budnik, L. T., Brunswig-Spickenheier, B., Mukhopadhyay, A. K. (2003). Lysophosphatidic Acid Signals through Mitogen-Activated Protein Kinase-Extracellular Signal Regulated Kinase in Ovarian Theca Cells Expressing the LPA1/edg2-Receptor: Involvement of a Nonclassical Pathway?. Mol. Endocrinol. 17: 1593-1606 [Abstract] [Full Text]
Zhao, H., Tian, W., Tai, C., Cohen, D. M. (2003). Hypertonic induction of COX-2 expression in renal medullary epithelial cells requires transactivation of the EGFR. Am. J. Physiol. Renal Physiol. 285: F281-F288 [Abstract] [Full Text]
Lemjabbar, H., Li, D., Gallup, M., Sidhu, S., Drori, E., Basbaum, C. (2003). Tobacco Smoke-induced Lung Cell Proliferation Mediated by Tumor Necrosis Factor {alpha}-converting Enzyme and Amphiregulin. J. Biol. Chem. 278: 26202-26207 [Abstract] [Full Text]
Huang, Y., Kim, S.-O., Jiang, J., Frank, S. J. (2003). Growth Hormone-induced Phosphorylation of Epidermal Growth Factor (EGF) Receptor in 3T3-F442A Cells: MODULATION OF EGF-INDUCED TRAFFICKING AND SIGNALING. J. Biol. Chem. 278: 18902-18913 [Abstract] [Full Text]
Takenobu, H., Yamazaki, A., Hirata, M., Umata, T., Mekada, E. (2003). The Stress- and Inflammatory Cytokine-induced Ectodomain Shedding of Heparin-binding Epidermal Growth Factor-like Growth Factor Is Mediated by p38 MAPK, Distinct from the 12-O-Tetradecanoylphorbol-13-acetate- and Lysophosphatidic Acid-induced Signaling Cascades. J. Biol. Chem. 278: 17255-17262 [Abstract] [Full Text]
Seals, D. F., Courtneidge, S. A. (2003). The ADAMs family of metalloproteases: multidomain proteins with multiple functions. Genes Dev. 17: 7-30 [Full Text]