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Original

Control of ErbB signaling through metalloprotease mediated ectodomain shedding of EGF-like factors

, &
Pages 121-136 | Received 24 Oct 2005, Published online: 11 Jul 2009

References

  • Aaronson SA. Growth factors and cancer. Science 1991; 254: 1146–1153
  • Abram CL, Seals DF, Pass I, Salinsky D, Maurer L, Roth TM, Courtneidge SA. The adaptor protein fish associates with members of the ADAMs family and localizes to podosomes of Src-transformed cells. J Biol Chem 2003; 278: 16844–16851
  • Althoff K, Mullberg J, Aasland D, Voltz N, Kallen K, Grotzinger J, Rose-John S. Recognition sequences and structural elements contribute to shedding susceptibility of membrane proteins. Biochem J 2001; 353: 663–672
  • Andrechek ER, Hardy WR, Girgis-Gabardo AA, Perry RL, Butler R, Graham FL, Kahn RC, Rudnicki MA, Muller WJ. ErbB2 is required for muscle spindle and myoblast cell survival. Mol Cell Biol 2002; 22: 4714–4722
  • Anklesaria P, Teixido J, Laiho M, Pierce JH, Greenberger JS, Massague J. Cell–cell adhesion mediated by binding of membrane-anchored transforming growth factor alpha to epidermal growth factor receptors promotes cell proliferation. Proc Natl Acad Sci USA 1990; 87: 3289–3293
  • Asakura M, Kitakaze M, Takashima S, Liao Y, Ishikura F, Yoshinaka T, Ohmoto H, Node K, Yoshino K, Ishiguro H, Asanuma H, Sanada S, Matsumura Y, Takeda H, Beppu S, Tada M, Hori M, Higashiyama S. Cardiac hypertrophy is inhibited by antagonism of ADAM12 processing of HB-EGF: Metalloproteinase inhibitors as a new therapy. Nat Med 2002; 8: 35–40
  • Baba I, Shirasawa S, Iwamoto R, Okumura K, Tsunoda T, Nishioka M, Fukuyama K, Yamamoto K, Mekada E, Sasazuki T. Involvement of deregulated epiregulin expression in tumorigenesis in vivo through activated Ki-Ras signaling pathway in human colon cancer cells. Cancer Res 2000; 60: 6886–6889
  • Bao J, Wolpowitz D, Role LW, Talmage DA. Back signaling by the NRG-1 intracellular domain. J Cell Biol 2003; 161: 1133–1141
  • Becherer JD, Blobel CP. Biochemical properties and functions of membrane-anchored metalloprotease-disintegrin proteins (ADAMs). Curr Top Dev Biol 2003; 54: 101–123
  • Borrell-Pages M, Rojo F, Albanell J, Baselga J, Arribas J. TACE is required for the activation of the EGFR by TGF-alpha in tumors. Embo J 2003; 22: 1114–1124
  • Brachmann R, Lindquist PB, Nagashima M, Kohr W, Lipari T, Napier M, Derynck R. Transmembrane TGF-alpha precursors activate EGF/TGF-alpha receptors. Cell 1989; 56: 691–700
  • Brown CL, Meise KS, Plowman GD, Coffey RJ, Dempsey PJ. Cell surface ectodomain cleavage of human amphiregulin precursor is sensitive to a metalloprotease inhibitor. Release of a predominant N-glycosylated 43-kDa soluble form. J Biol Chem 1998; 273: 17258–17268
  • Buonanno A, Fischbach GD. Neuregulin and ErbB receptor signaling pathways in the nervous system. Curr Opin Neurobiol 2001; 11: 287–296
  • Burgess TL, Ross SL, Qian YX, Brankow D, Hu S. Biosynthetic processing of neu differentiation factor. Glycosylation trafficking, and regulated cleavage from the cell surface. J Biol Chem 1995; 270: 19188–19196
  • Burgess AW, Cho HS, Eigenbrot C, Ferguson KM, Garrett TP, Leahy DJ, Lemmon MA, Sliwkowski MX, Ward CW, Yokoyama S. An open-and-shut case? Recent insights into the activation of EGF/ErbB receptors. Mol Cell 2003; 12: 541–552
  • Buteau J, Foisy S, Joly E, Prentki M. Glucagon-like peptide 1 induces pancreatic beta-cell proliferation via transactivation of the epidermal growth factor receptor. Diabetes 2003; 52: 124–132
  • Carpenter G. EGF receptor transactivation mediated by the proteolytic production of EGF-like agonists. Sci STKE 2000; 2000: PE1
  • Carraway KL, 3rd, Sliwkowski MX, Akita R, Platko JV, Guy PM, Nuijens A, Diamonti AJ, Vandlen RL, Cantley LC, Cerione RA. The ErbB3 gene product is a receptor for heregulin. J Biol Chem 1994; 269: 14303–14306
  • Citri A, Skaria KB, Yarden Y. The deaf and the dumb: The biology of ErbB-2 and ErbB-3. Exp Cell Res 2003; 284: 54–65
  • Codony-Servat J, Albanell J, Lopez-Talavera JC, Arribas J, Baselga J. Cleavage of the HER2 ectodomain is a pervanadate-activable process that is inhibited by the tissue inhibitor of metalloproteases-1 in breast cancer cells. Cancer Res 1999; 59: 1196–1201
  • Crone SA, Lee KF. Gene targeting reveals multiple essential functions of the neuregulin signaling system during development of the neuroendocrine and nervous systems. Ann N Y Acad Sci 2002; 971: 547–553
  • Crone SA, Zhao YY, Fan L, Gu Y, Minamisawa S, Liu Y, Peterson KL, Chen J, Kahn R, Condorelli G, Ross J, Jr, Chien KR, Lee KF. ErbB2 is essential in the prevention of dilated cardiomyopathy. Nat Med 2002; 8: 459–465
  • Das SK, Lim H, Wang J, Paria BC, BazDresch M, Dey SK. Inappropriate expression of human transforming growth factor (TGF)-alpha in the uterus of transgenic mouse causes down regulation of TGF-beta receptors and delays the blastocyst-attachment reaction. J Mol Endocrinol 1997; 18: 243–257
  • Davies BR, Platt-Higgins AM, Schmidt G, Rudland PS. Development of hyperplasias, preneoplasias, and mammary tumors in MMTV–c-ErbB-2 and MMTV–TGF-alpha transgenic rats. Am J Pathol 1999; 155: 303–314
  • de Bono JS, Rowinsky EK. The ErbB receptor family: A therapeutic target for cancer. Trends Mol Med 2002; 8: S19–S26
  • De Larco JE, Reynolds R, Carlberg K, Engle C, Todaro GJ. Sarcoma growth factor from mouse sarcoma virus-transformed cells. Purification by binding and elution from epidermal growth factor receptor-rich cells. J Biol Chem 1980; 255: 3685–3690
  • Dello Sbarba P, Rovida E. Transmodulation of cell surface regulatory molecules via ectodomain shedding. Biol Chem 2002; 383: 69–83
  • Dempsey PJ, Meise KS, Yoshitake Y, Nishikawa K, Coffey RJ. Apical enrichment of human EGF precursor in Madin-Darby canine kidney cells involves preferential basolateral ectodomain cleavage sensitive to a metalloprotease inhibitor. J Cell Biol 1997; 138: 747–758
  • Deng P, Wang YL, Haga Y, Pattengale PK. Multiple factors determine the selection of the ectodomain cleavage site of human cell surface macrophage colony-stimulating factor. Biochemistry 1998; 37: 17898–17904
  • Diaz-Rodriguez E, Esparis-Ogando A, Montero JC, Yuste L, Pandiella A. Stimulation of cleavage of membrane proteins by calmodulin inhibitors. Biochem J 2000; 346(Pt 2)359–367
  • Diaz-Rodriguez E, Montero JC, Esparis-Ogando A, Yuste L, Pandiella A. Extracellular signal-regulated kinase phosphorylates tumor necrosis factor alpha-converting enzyme at threonine 735: A potential role in regulated shedding. Mol Biol Cell 2002; 13: 2031–2044
  • Dlugosz AA, Cheng C, Williams EK, Darwiche N, Dempsey PJ, Mann B, Dunn AR, Coffey RJ, Jr, Yuspa SH. Autocrine transforming growth factor alpha is dispensible for v-ras Ha-induced epidermal neoplasia: Potential involvement of alternate epidermal growth factor receptor ligands. Cancer Res 1995; 55: 1883–1893
  • Dong J, Opresko LK, Dempsey PJ, Lauffenburger DA, Coffey RJ, Wiley HS. Metalloprotease-mediated ligand release regulates autocrine signaling through the epidermal growth factor receptor. Proc Natl Acad Sci USA 1999; 96: 6235–6240
  • Dong J, Wiley HS. Trafficking and proteolytic release of epidermal growth factor receptor ligands are modulated by their membrane-anchoring domains. J Biol Chem 2000; 275: 557–564
  • Duffy MJ, Lynn DJ, Lloyd AT, O'Shea CM. The ADAMs family of proteins: From basic studies to potential clinical applications. Thromb Haemost 2003; 89: 622–631
  • Dunbar AJ, Goddard C. Structure–function and biological role of betacellulin. Int J Biochem Cell Biol 2000; 32: 805–815
  • Ebert M, Yokoyama M, Kobrin MS, Friess H, Lopez ME, Buchler MW, Johnson GR, Korc M. Induction and expression of amphiregulin in human pancreatic cancer. Cancer Res 1994; 54: 3959–3962
  • Ekstrand AJ, Sugawa N, James CD, Collins VP. Amplified and rearranged epidermal growth factor receptor genes in human glioblastomas reveal deletions of sequences encoding portions of the N- and/or C-terminal tails. Proc Natl Acad Sci USA 1992; 89: 4309–4313
  • Erickson SL, O'Shea KS, Ghaboosi N, Loverro L, Frantz G, Bauer M, Lu LH, Moore MW. ErbB3 is required for normal cerebellar and cardiac development: A comparison with ErbB2-and heregulin-deficient mice. Development 1997; 124: 4999–5011
  • Falls DL. Neuregulins: Functions, forms and signaling strategies. Exp Cell Res 2003; 284: 14–30
  • Fan H, Turck CW, Derynck R. Characterization of growth factor-induced serine phosphorylation of tumor necrosis factor-alpha converting enzyme and of an alternatively translated polypeptide. J Biol Chem 2003; 278: 18617–18627
  • Feehan C, Darlak K, Kahn J, Walcheck B, Spatola AF, Kishimoto TK. Shedding of the lymphocyte l-selectin adhesion molecule is inhibited by a hydroxamic acid-based protease inhibitor. Identification with an l-selectin-alkaline phosphatase reporter. J Biol Chem 1996; 271: 7019–7024
  • Ferguson KM, Darling PJ, Mohan MJ, Macatee TL, Lemmon MA. Extracellular domains drive homo- but not hetero-dimerization of ErbB receptors. Embo J 2000; 19: 4632–4643
  • Fischer OM, Hart S, Gschwind A, Ullrich A. EGFR signal transactivation in cancer cells. Biochem Soc Trans 2003; 31: 1203–1208
  • Garrett TP, McKern NM, Lou M, Elleman TC, Adams TE, Lovrecz GO, Zhu HJ, Walker F, Frenkel MJ, Hoyne PA, Jorissen RN, Nice EC, Burgess AW, Ward CW. Crystal structure of a truncated epidermal growth factor receptor extracellular domain bound to transforming growth factor alpha. Cell 2002; 110: 763–773
  • Garrett TP, McKern NM, Lou M, Elleman TC, Adams TE, Lovrecz GO, Kofler M, Jorissen RN, Nice EC, Burgess AW, Ward CW. The crystal structure of a truncated ErbB2 ectodomain reveals an active conformation, poised to interact with other ErbB receptors. Mol Cell 2003; 11: 495–505
  • Gassmann M, Casagranda F, Orioli D, Simon H, Lai C, Klein R, Lemke G. Aberrant neural and cardiac development in mice lacking the ErbB4 neuregulin receptor. Nature 1995; 378: 390–394
  • Gechtman Z, Alonso JL, Raab G, Ingber DE, Klagsbrun M. 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 1999; 274: 28828–28835
  • Goishi K, Higashiyama S, Klagsbrun M, Nakano N, Umata T, Ishikawa M, Mekada E, Taniguchi N. Phorbol ester induces the rapid processing of cell surface heparin-binding EGF-like growth factor: Conversion from juxtacrine to paracrine growth factor activity. Mol Biol Cell 1995; 6: 967–980
  • Golding JP, Trainor P, Krumlauf R, Gassmann M. Defects in path finding by cranial neural crest cells in mice lacking the neuregulin receptor ErbB4. Nat Cell Biol 2000; 2: 103–109
  • Greenwald I. lin-12, a nematode homeotic gene, is homologous to a set of mammalian proteins that includes epidermal growth factor. Cell 1985; 43: 583–590
  • Gschwind A, Prenzel N, Ullrich A. Lysophosphatidic acid-induced squamous cell carcinoma cell proliferation and motility involves epidermal growth factor receptor signal transactivation. Cancer Res 2002; 62: 6329–6336
  • Gschwind A, Hart S, Fischer OM, Ullrich A. TACE cleavage of proamphiregulin regulates GPCR-induced proliferation and motility of cancer cells. Embo J 2003; 22: 2411–2421
  • Han B, Fischbach GD. The release of acetylcholine receptor inducing activity (ARIA) from its transmembrane precursor in transfected fibroblasts. J Biol Chem 1999; 274: 26407–26415
  • Hao L, Du M, Lopez-Campistrous A, Fernandez-Patron C. Agonist-induced activation of matrix metalloproteinase-7 promotes vasoconstriction through the epidermal growth factor-receptor pathway. Circ Res 2004; 94: 68–76
  • Hardie WD, Le Cras TD, Jiang K, Tichelaar JW, Azhar M, Korfhagen TR. Conditional expression of transforming growth factor-alpha in adult mouse lung causes pulmonary fibrosis. Am J Physiol Lung Cell Mol Physiol 2004; 286: L741–L749
  • Harris RC, Chung E, Coffey RJ. EGF receptor ligands. Exp Cell Res 2003; 284: 2–13
  • Haugen DR, Akslen LA, Varhaug JE, Lillehaug JR. Expression of c-ErbB-3 and c-ErbB-4 proteins in papillary thyroid carcinomas. Cancer Res 1996; 56: 1184–1188
  • Higashiyama S, Abraham JA, Miller J, Fiddes JC, Klagsbrun M. A heparin-binding growth factor secreted by macrophage-like cells that is related to EGF. Science 1991; 251: 936–939
  • Hinkle CL, Sunnarborg SW, Loiselle D, Parker CE, Stevenson M, Russell WE, Lee DC. Selective roles for TACE/ADAM17 in the shedding of the epidermal growth factor receptor ligand family. The juxtamembrane stalk determines cleavage efficiency. J Biol Chem 2004; 279: 24179–24188
  • Holbro T, Hynes NE. ErbB receptors: Directing key signaling networks throughout life. Annu Rev Pharmacol Toxicol 2004; 44: 195–217
  • Hom YK, Young P, Wiesen JF, Miettinen PJ, Derynck R, Werb Z, Cunha GR. Uterine and vaginal organ growth requires epidermal growth factor receptor signaling from stroma. Endocrinology 1998; 139: 913–921
  • Howard L, Nelson KK, Maciewicz RA, Blobel CP. Interaction of the metalloprotease disintegrins MDC9 and MDC15 with two SH3 domain-containing proteins, endophilin I and SH3PX1. J Biol Chem 1999; 274: 31693–31699
  • Howard L, Maciewicz RA, Blobel CP. Cloning and characterization of ADAM28: Evidence for autocatalytic pro-domain removal and for cell surface localization of mature ADAM28. Biochem J 2000; 348(Pt 1)21–27
  • Huang L, Feng L, Yang L, Zhou W, Zhao S, Li C. Screen and identification of proteins interacting with ADAM19 cytoplasmic tail. Mol Biol Rep 2002; 29: 317–323
  • Hynes NE, Stern DF. The biology of ErbB-2/neu/HER-2 and its role in cancer. Biochim Biophys Acta 1994; 1198: 165–184
  • Iwamoto R, Mekada E. Heparin-binding EGF-like growth factor: A juxtacrine growth factor. Cytokine Growth Factor Rev 2000; 11: 335–344
  • 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. Heparin-binding EGF-like growth factor and ErbB signaling is essential for heart function. Proc Natl Acad Sci USA 2003; 100: 3221–3226
  • Izumi Y, Hirata M, Hasuwa H, Iwamoto R, Umata T, Miyado K, Tamai Y, Kurisaki T, Sehara-Fujisawa A, Ohno S, Mekada E. A metalloprotease-disintegrin, MDC9/meltrin-gamma/ADAM9 and PKC delta are involved in TPA-induced ectodomain shedding of membrane-anchored heparin-binding EGF-like growth factor. Embo J 1998; 17: 7260–7272
  • Jackson LF, Qiu TH, Sunnarborg SW, Chang A, Zhang C, Patterson C, Lee DC. Defective valvulogenesis in HB-EGF and TACE-null mice is associated with aberrant BMP signaling. Embo J 2003; 22: 2704–2716
  • Janes PW, Saha N, Barton WA, Kolev MV, Wimmer-Kleikamp SH, Nievergall E, Blobel CP, Himanen JP, Lackmann M, Nikolov DB. Adam meets Eph: An ADAM substrate recognition module acts as a molecular switch for ephrin cleavage in trans. Cell 2005; 123: 291–304
  • Janne PA, Engelman JA, Johnson BE. Epidermal growth factor receptor mutations in non-small-cell lung cancer: Implications for treatment and tumor biology. J Clin Oncol 2005; 23: 3227–3234
  • Jhappan C, Stahle C, Harkins RN, Fausto N, Smith GH, Merlino GT. TGF-alpha overexpression in transgenic mice induces liver neoplasia and abnormal development of the mammary gland and pancreas. Cell 1990; 61: 1137–1146
  • Jones FE, Stern DF. Expression of dominant-negative ErbB2 in the mammary gland of transgenic mice reveals a role in lobuloalveolar development and lactation. Oncogene 1999; 18: 3481–3490
  • Jones FE, Welte T, Fu XY, Stern DF. ErbB4 signaling in the mammary gland is required for lobuloalveolar development and Stat5 activation during lactation. J Cell Biol 1999; 147: 77–88
  • Junttila TT, Sundvall M, Maatta JA, Elenius K. ErbB4 and its isoforms: Selective regulation of growth factor responses by naturally occurring receptor variants. Trends Cardiovasc Med 2000; 10: 304–310
  • Junttila TT, Laato M, Vahlberg T, Soderstrom KO, Visakorpi T, Isola J, Elenius K. Identification of patients with transitional cell carcinoma of the bladder overexpressing ErbB2, ErbB3 or specific ErbB4 isoforms: Real-time reverse transcription-PCR analysis in estimation of ErbB receptor status from cancer patients. Clin Cancer Res 2003; 9: 5346–5357
  • Kang Q, Cao Y, Zolkiewska A. Metalloprotease-disintegrin ADAM12 binds to the SH3 domain of Src and activates Src tyrosine kinase in C2C12 cells. Biochem J 2000; 352(Pt 3)883–892
  • Kang Q, Cao Y, Zolkiewska A. Direct interaction between the cytoplasmic tail of ADAM 12 and the Src homology 3 domain of p85alpha activates phosphatidylinositol 3-kinase in C2C12 cells. J Biol Chem 2001; 276: 24466–24472
  • Kew TY, Bell JA, Pinder SE, Denley H, Srinivasan R, Gullick WJ, Nicholson RI, Blamey RW, Ellis IO. c-ErbB-4 protein expression in human breast cancer. Br J Cancer 2000; 82: 1163–1170
  • Kiguchi K, Bol D, Carbajal S, Beltran L, Moats S, Chan K, Jorcano J, DiGiovanni J. Constitutive expression of ErbB2 in epidermis of transgenic mice results in epidermal hyperproliferation and spontaneous skin tumor development. Oncogene 2000; 19: 4243–4254
  • Kinugasa Y, Ishiguro H, Tokita Y, Oohira A, Ohmoto H, Higashiyama S. Neuroglycan C a novel member of the neuregulin family. Biochem Biophys Res Commun 2004; 321: 1045–1049
  • Klapper LN, Kirschbaum MH, Sela M, Yarden Y. Biochemical and clinical implications of the ErbB/HER signaling network of growth factor receptors. Adv Cancer Res 2000; 77: 25–79
  • Knowlden JM, Gee JM, Seery LT, Farrow L, Gullick WJ, Ellis IO, Blamey RW, Robertson JF, Nicholson RI. c-ErbB3 and c-ErbB4 expression is a feature of the endocrine responsive phenotype in clinical breast cancer. Oncogene 1998; 17: 1949–1957
  • Kochupurakkal BS, Harari D, Di-Segni A, Maik-Rachline G, Lyass L, Gur G, Kerber G, Citri A, Lavi S, Eilam R, Chalifa-Caspi V, Eshhar Z, Pikarsky E, Pinkas-Kramarski R, Bacus SS, Yarden Y. Epigen, the last ligand of ErbB receptors, reveals intricate relationships between affinity and mitogenicity. J Biol Chem 2005; 280: 8503–8512
  • Kornblum HI, Hussain R, Wiesen J, Miettinen P, Zurcher SD, Chow K, Derynck R, Werb Z. Abnormal astrocyte development and neuronal death in mice lacking the epidermal growth factor receptor. J Neurosci Res 1998; 53: 697–717
  • Krane IM, Leder P. NDF/heregulin induces persistence of terminal end buds and adenocarcinomas in the mammary glands of transgenic mice. Oncogene 1996; 12: 1781–1788
  • Le Cras TD, Hardie WD, Fagan K, Whitsett JA, Korfhagen TR. Disrupted pulmonary vascular development and pulmonary hypertension in transgenic mice overexpressing transforming growth factor-alpha. Am J Physiol Lung Cell Mol Physiol 2003; 285: L1046–L1054
  • Le Gall S, Auger R, Dreux C, Mauduit P. Regulated cell surface proEGF ectodomain shedding is a zinc–metalloprotease dependent process. J Biol Chem 2003; 278: 45255–45268
  • Lee KF, Simon H, Chen H, Bates B, Hung MC, Hauser C. Requirement for neuregulin receptor ErbB2 in neural and cardiac development. Nature 1995; 378: 394–398
  • Lee D, Pearsall RS, Das S, Dey SK, Godfrey VL, Threadgill DW. Epiregulin is not essential for development of intestinal tumors but is required for protection from intestinal damage. Mol Cell Biol 2004; 24: 8907–8916
  • Lemmon MA, Bu Z, Ladbury JE, Zhou M, Pinchasi D, Lax I, Engelman DM, Schlessinger J. Two EGF molecules contribute additively to stabilization of the EGFR dimer. Embo J 1997; 16: 281–294
  • Lenferink AE, Pinkas-Kramarski R, van de Poll ML, van Vugt MJ, Klapper LN, Tzahar E, Waterman H, Sela M, van Zoelen EJ, Yarden Y. Differential endocytic routing of homo- and hetero-dimeric ErbB tyrosine kinases confers signaling superiority to receptor heterodimers. Embo J 1998; 17: 3385–3397
  • Leu M, Bellmunt E, Schwander M, Farinas I, Brenner HR, Muller U. ErbB2 regulates neuromuscular synapse formation and is essential for muscle spindle development. Development 2003; 130: 2291–2301
  • Levine E, Cupp AS, Miyashiro L, Skinner MK. Role of transforming growth factor-alpha and the epidermal growth factor receptor in embryonic rat testis development. Biol Reprod 2000; 62: 477–490
  • Li Q, Park PW, Wilson CL, Parks WC. Matrilysin shedding of syndecan-1 regulates chemokine mobilization and transepithelial efflux of neutrophils in acute lung injury. Cell 2002; 111: 635–646
  • Lin J, Freeman MR. Transactivation of ErbB1 and ErbB2 receptors by angiotensin II in normal human prostate stromal cells. Prostate 2003; 54: 1–7
  • Liu X, Hwang H, Cao L, Buckland M, Cunningham A, Chen J, Chien KR, Graham RM, Zhou M. Domain-specific gene disruption reveals critical regulation of neuregulin signaling by its cytoplasmic tail. Proc Natl Acad Sci USA 1998a; 95: 13024–13029
  • Liu X, Hwang H, Cao L, Wen D, Liu N, Graham RM, Zhou M. Release of the neuregulin functional polypeptide requires its cytoplasmic tail. J Biol Chem 1998b; 273: 34335–34340
  • Lodge AJ, Anderson JJ, Gullick WJ, Haugk B, Leonard RC, Angus B. Type 1 growth factor receptor expression in node positive breast cancer: Adverse prognostic significance of c-ErbB-4. J Clin Pathol 2003; 56: 300–304
  • Loeb JA, Susanto ET, Fischbach GD. The neuregulin precursor proARIA is processed to ARIA after expression on the cell surface by a protein kinase C-enhanced mechanism. Mol Cell Neurosci 1998; 11: 77–91
  • Luetteke NC, Qiu TH, Peiffer RL, Oliver P, Smithies O, Lee DC. TGF-alpha deficiency results in hair follicle and eye abnormalities in targeted and waved-1 mice. Cell 1993; 73: 263–278
  • Luetteke NC, Qiu TH, Fenton SE, Troyer KL, Riedel RF, Chang A, Lee DC. Targeted inactivation of the EGF and amphiregulin genes reveals distinct roles for EGF receptor ligands in mouse mammary gland development. Development 1999; 126: 2739–2750
  • Mann GB, Fowler KJ, Gabriel A, Nice EC, Williams RL, Dunn AR. Mice with a null mutation of the TGF-alpha gene have abnormal skin architecture, wavy hair, and curly whiskers and often develop corneal inflammation. Cell 1993; 73: 249–261
  • Manning CB, Cummins AB, Jung MW, Berlanger I, Timblin CR, Palmer C, Taatjes DJ, Hemenway D, Vacek P, Mossman BT. A mutant epidermal growth factor receptor targeted to lung epithelium inhibits asbestos-induced proliferation and proto-oncogene expression. Cancer Res 2002; 62: 4169–4175
  • Martin FM, Beckett RP, Bellamy CL, Courtney PF, Davies SJ, Drummond AH, Dodd R, Pratt LM, Patel SR, Ricketts ML, Todd RS, Tuffnell AR, Ward JW, Whittaker M. The synthesis and biological evaluation of non-peptidic matrix metalloproteinase inhibitors. Bioorg Med Chem Lett 1999; 9: 2887–2892
  • Massova I, Kotra LP, Fridman R, Mobashery S. Matrix metalloproteinases: Structures, evolution and diversification. FASEB J 1998; 12: 1075–1095
  • Matthews V, Schuster B, Schutze S, Bussmeyer I, Ludwig A, Hundhausen C, Sadowski T, Saftig P, Hartmann D, Kallen KJ, Rose-John S. Cellular cholesterol depletion triggers shedding of the human interleukin-6 receptor by ADAM10 and ADAM17 (TACE). J Biol Chem 2003; 278: 38829–38839
  • Mendelsohn J, Baselga J. The EGF receptor family as targets for cancer therapy. Oncogene 2000; 19: 6550–6565
  • Meyer D, Birchmeier C. Multiple essential functions of neuregulin in development. Nature 1995; 378: 386–390
  • Mezyk R, Bzowska M, Bereta J. Structure and functions of tumor necrosis factor-alpha converting enzyme. Acta Biochim Pol 2003; 50: 625–645
  • Michailov GV, Sereda MW, Brinkmann BG, Fischer TM, Haug B, Birchmeier C, Role L, Lai C, Schwab MH, Nave KA. Axonal neuregulin-1 regulates myelin sheath thickness. Science 2004; 304: 700–703
  • Miettinen PJ, Berger JE, Meneses J, Phung Y, Pedersen RA, Werb Z, Derynck R. Epithelial immaturity and multiorgan failure in mice lacking epidermal growth factor receptor. Nature 1995; 376: 337–341
  • Migaki GI, Kahn J, Kishimoto TK. Mutational analysis of the membrane-proximal cleavage site of l-selectin: Relaxed sequence specificity surrounding the cleavage site. J Exp Med 1995; 182: 549–557
  • Miyamoto S, Hirata M, Yamazaki A, Kageyama T, Hasuwa H, Mizushima H, Tanaka Y, Yagi H, Sonoda K, Kai M, Kanoh H, Nakano H, Mekada E. Heparin-binding EGF-like growth factor is a promising target for ovarian cancer therapy. Cancer Res 2004; 64: 5720–5727
  • Miyoshi E, Higashiyama S, Nakagawa T, Hayashi N, Taniguchi N. Membrane-anchored heparin-binding epidermal growth factor-like growth factor acts as a tumor survival factor in a hepatoma cell line. J Biol Chem 1997; 272: 14349–14355
  • Molina MA, Codony-Servat J, Albanell J, Rojo F, Arribas J, Baselga J. Trastuzumab (herceptin), a humanized anti-Her2 receptor monoclonal antibody, inhibits basal and activated Her2 ectodomain cleavage in breast cancer cells. Cancer Res 2001; 61: 4744–4749
  • Montero JC, Yuste L, Diaz-Rodriguez E, Esparis-Ogando A, Pandiella A. Differential shedding of transmembrane neuregulin isoforms by the tumor necrosis factor-alpha-converting enzyme. Mol Cell Neurosci 2000; 16: 631–648
  • Mori S, Tanaka M, Nanba D, Nishiwaki E, Ishiguro H, Higashiyama S, Matsuura N. PACSIN3 binds ADAM12/meltrin alpha and up-regulates ectodomain shedding of heparin-binding epidermal growth factor-like growth factor. J Biol Chem 2003; 278: 46029–46034
  • Moscatello DK, Holgado-Madruga M, Godwin AK, Ramirez G, Gunn G, Zoltick PW, Biegel JA, Hayes RL, Wong AJ. Frequent expression of a mutant epidermal growth factor receptor in multiple human tumors. Cancer Res 1995; 55: 5536–5539
  • Muller WJ, Arteaga CL, Muthuswamy SK, Siegel PM, Webster MA, Cardiff RD, Meise KS, Li F, Halter SA, Coffey RJ. Synergistic interaction of the neu proto-oncogene product and transforming growth factor-alpha in the mammary epithelium of transgenic mice. Mol Cell Biol 1996; 16: 5726–5736
  • Nagano O, Murakami D, Hartmann D, De Strooper B, Saftig P, Iwatsubo T, Nakajima M, Shinohara M, Saya H. Cell–matrix interaction via CD44 is independently regulated by different metalloproteinases activated in response to extracellular Ca2+ influx and PKC activation. J Cell Biol 2004; 165: 893–902
  • Nakayama K. Furin: A mammalian subtilisin/Kex2p-like endoprotease involved in processing of a wide variety of precursor proteins. Biochem J 1997; 327(Pt 3)625–635
  • Nelson KK, Schlondorff J, Blobel CP. Evidence for an interaction of the metalloprotease–disintegrin tumour necrosis factor-alpha convertase (TACE) with mitotic arrest deficient 2 (MAD2), and of the metalloprotease-disintegrin MDC9 with a novel MAD2-related protein, MAD2 beta. Biochem J 1999; 343(Pt 3)673–680
  • Olayioye MA, Neve RM, Lane HA, Hynes NE. The ErbB signaling network: Receptor heterodimerization in development and cancer. Embo J 2000; 19: 3159–3167
  • Ozcelik C, Erdmann B, Pilz B, Wettschureck N, Britsch S, Hubner N, Chien KR, Birchmeier C, Garratt AN. Conditional mutation of the ErbB2 (HER2) receptor in cardiomyocytes leads to dilated cardiomyopathy. Proc Natl Acad Sci USA 2002; 99: 8880–8885
  • Pandiella A, Massague J. Cleavage of the membrane precursor for transforming growth factor-alpha is a regulated process. Proc Natl Acad Sci USA 1991a; 88: 1726–1730
  • Pandiella A, Massague J. Multiple signals activate cleavage of the membrane transforming growth factor-alpha precursor. J Biol Chem 1991b; 266: 5769–5773
  • Pang S, Chubb AJ, Schwager SL, Ehlers MR, Sturrock ED, Hooper NM. Roles of the juxtamembrane and extracellular domains of angiotensin-converting enzyme in ectodomain shedding. Biochem J 2001; 358: 185–192
  • Peiretti F, Deprez-Beauclair P, Bonardo B, Aubert H, Juhan-Vague I, Nalbone G. Identification of SAP97 as an intracellular binding partner of TACE. J Cell Sci 2003; 116: 1949–1957
  • Peschon JJ, Slack JL, Reddy P, Stocking KL, Sunnarborg SW, Lee DC, Russell WE, Castner BJ, Johnson RS, Fitzner JN, Boyce RW, Nelson N, Kozlosky CJ, Wolfson MF, Rauch CT, Cerretti DP, Paxton RJ, March CJ, Black RA. An essential role for ectodomain shedding in mammalian development. Science 1998; 282: 1281–1284
  • Poghosyan Z, Robbins SM, Houslay MD, Webster A, Murphy G, Edwards DR. Phosphorylation-dependent interactions between ADAM15 cytoplasmic domain and Src family protein-tyrosine kinases. J Biol Chem 2002; 277: 4999–5007
  • Prenzel N, Zwick E, Daub H, Leserer M, Abraham R, Wallasch C, Ullrich A. EGF receptor transactivation by G-protein-coupled receptors requires metalloproteinase cleavage of proHB-EGF. Nature 1999; 402: 884–888
  • Prenzel N, Fischer OM, Streit S, Hart S, Ullrich A. The epidermal growth factor receptor family as a central element for cellular signal transduction and diversification. Endocr Relat Cancer 2001; 8: 11–31
  • Prevot V, Rio C, Cho GJ, Lomniczi A, Heger S, Neville CM, Rosenthal NA, Ojeda SR, Corfas G. Normal female sexual development requires neuregulin-ErbB receptor signaling in hypothalamic astrocytes. J Neurosci 2003; 23: 230–239
  • Razandi M, Pedram A, Park ST, Levin ER. Proximal events in signaling by plasma membrane estrogen receptors. J Biol Chem 2003; 278: 2701–2712
  • Rho O, Beltran LM, Gimenez-Conti IB, DiGiovanni J. Altered expression of the epidermal growth factor receptor and transforming growth factor-alpha during multistage skin carcinogenesis in SENCAR mice. Mol Carcinog 1994; 11: 19–28
  • Richter A, O'Donnell RA, Powell RM, Sanders MW, Holgate ST, Djukanovic R, Davies DE. Autocrine ligands for the epidermal growth factor receptor mediate interleukin-8 release from bronchial epithelial cells in response to cigarette smoke. Am J Respir Cell Mol Biol 2002; 27: 85–90
  • Rio C, Buxbaum JD, Peschon JJ, Corfas G. Tumor necrosis factor-alpha-converting enzyme is required for cleavage of ErbB4/HER4. J Biol Chem 2000; 275: 10379–10387
  • Roh M, Paterson AJ, Asa SL, Chin E, Kudlow JE. Stage-sensitive blockade of pituitary somatomammotrope development by targeted expression of a dominant negative epidermal growth factor receptor in transgenic mice. Mol Endocrinol 2001; 15: 600–613
  • Ross JS, Fletcher JA. The HER-2/neu oncogene in breast cancer: Prognostic factor, predictive factor, and target for therapy. Stem Cells 1998; 16: 413–428
  • Sahin U, Weskamp G, Kelly K, Zhou HM, Higashiyama S, Peschon J, Hartmann D, Saftig P, Blobel CP. Distinct roles for ADAM10 and ADAM17 in ectodomain shedding of six EGFR ligands. J Cell Biol 2004; 164: 769–779
  • Salomon DS, Brandt R, Ciardiello F, Normanno N. Epidermal growth factor-related peptides and their receptors in human malignancies. Crit Rev Oncol Hematol 1995; 19: 183–232
  • Sanderson MP, Erickson SN, Gough PJ, Garton KJ, Wille PT, Raines EW, Dunbar AJ, Dempsey PJ. ADAM10 mediates ectodomain shedding of the betacellulin precursor activated by p-aminophenylmercuric acetate and extracellular calcium influx. J Biol Chem 2005; 280: 1826–1837
  • Sandgren EP, Luetteke NC, Palmiter RD, Brinster RL, Lee DC. Overexpression of TGF-alpha in transgenic mice: Induction of epithelial hyperplasia, pancreatic metaplasia and carcinoma of the breast. Cell 1990; 61: 1121–1135
  • Schafer B, Gschwind A, Ullrich A. Multiple G-protein-coupled receptor signals converge on the epidermal growth factor receptor to promote migration and invasion. Oncogene 2004; 23: 991–999
  • Schlomann U, Wildeboer D, Webster A, Antropova O, Zeuschner D, Knight CG, Docherty AJ, Lambert M, Skelton L, Jockusch H, Bartsch JW. The metalloprotease disintegrin ADAM8. Processing by autocatalysis is required for proteolytic activity and cell adhesion. J Biol Chem 2002; 277: 48210–48219
  • Sharp R, Babyatsky MW, Takagi H, Tagerud S, Wang TC, Bockman DE, Brand SJ, Merlino G. Transforming growth factor-alpha disrupts the normal program of cellular differentiation in the gastric mucosa of transgenic mice. Development 1995; 121: 149–161
  • Shing Y, Christofori G, Hanahan D, Ono Y, Sasada R, Igarashi K, Folkman J. Betacellulin: A mitogen from pancreatic beta cell tumors. Science 1993; 259: 1604–1607
  • Shirakabe K, Wakatsuki S, Kurisaki T, Fujisawa-Sehara A. Roles of Meltrin beta /ADAM19 in the processing of neuregulin. J Biol Chem 2001; 276: 9352–9358
  • Shirasawa S, Sugiyama S, Baba I, Inokuchi J, Sekine S, Ogino K, Kawamura Y, Dohi T, Fujimoto M, Sasazuki T. Dermatitis due to epiregulin deficiency and a critical role of epiregulin in immune-related responses of keratinocyte and macrophage. Proc Natl Acad Sci USA 2004; 101: 13921–13926
  • Shoyab M, McDonald VL, Bradley JG, Todaro GJ. Amphiregulin: A bifunctional growth-modulating glycoprotein produced by the phorbol 12-myristate 13-acetate-treated human breast adenocarcinoma cell line MCF-7. Proc Natl Acad Sci USA 1988; 85: 6528–6532
  • Sibilia M, Wagner EF. Strain-dependent epithelial defects in mice lacking the EGF receptor. Science 1995; 269: 234–238
  • Singh AB, Tsukada T, Zent R, Harris RC. Membrane-associated HB-EGF modulates HGF-induced cellular responses in MDCK cells. J Cell Sci 2004; 117: 1365–1379
  • Slack BE, Ma LK, Seah CC. Constitutive shedding of the amyloid precursor protein ectodomain is up-regulated by tumour necrosis factor-alpha converting enzyme. Biochem J 2001; 357: 787–794
  • Srinivasan R, Benton E, McCormick F, Thomas H, Gullick WJ. Expression of the c-ErbB-3/HER-3 and c-ErbB-4/HER-4 growth factor receptors and their ligands, neuregulin-1 alpha, neuregulin-1 beta and betacellulin, in normal endometrium and endometrial cancer. Clin Cancer Res 1999; 5: 2877–2883
  • Stenflo J. Structure-function relationships of epidermal growth factor modules in vitamin K-dependent clotting factors. Blood 1991; 78: 1637–1651
  • Strachan L, Murison JG, Prestidge RL, Sleeman MA, Watson JD, Kumble KD. Cloning and biological activity of epigen, a novel member of the epidermal growth factor superfamily. J Biol Chem 2001; 276: 18265–18271
  • Sunnarborg SW, Hinkle CL, Stevenson M, Russell WE, Raska CS, Peschon JJ, Castner BJ, Gerhart MJ, Paxton RJ, Black RA, Lee DC. Tumor necrosis factor-alpha converting enzyme (TACE) regulates epidermal growth factor receptor ligand availability. J Biol Chem 2002; 277: 12838–12845
  • Suo Z, Berner HS, Risberg B, Karlsson MG, Nesland JM. Estrogen receptor-alpha and C-ErbB4 expression in breast carcinomas. Virchows Arch 2001; 439: 62–69
  • Suzuki M, Raab G, Moses MA, Fernandez CA, Klagsbrun M. Matrix metalloproteinase-3 releases active heparin-binding EGF-like growth factor by cleavage at a specific juxtamembrane site. J Biol Chem 1997; 272: 31730–31737
  • Takenobu H, Yamazaki A, Hirata M, Umata T, Mekada E. 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 2003; 278: 17255–17262
  • Tanida S, Joh T, Itoh K, Kataoka H, Sasaki M, Ohara H, Nakazawa T, Nomura T, Kinugasa Y, Ohmoto H, Ishiguro H, Yoshino K, Higashiyama S, Itoh M. The mechanism of cleavage of EGFR ligands induced by inflammatory cytokines in gastric cancer cells. Gastroenterology 2004; 127: 559–569
  • Thathiah A, Carson DD. MT1-MMP mediates MUC1 shedding independently of TACE/ADAM17. Biochem J 2004; 382: 363–373
  • Threadgill DW, Dlugosz AA, Hansen LA, Tennenbaum T, Lichti U, Yee D, LaMantia C, Mourton T, Herrup K, Harris RC, Barnard JA, Yuspa SH, Coffey RJ, TM. Targeted disruption of mouse EGF receptor: Effect of genetic background on mutant phenotype. Science 1995; 269: 230–234
  • Todaro GJ, De Larco JE, Cohen S. Transformation by murine and feline sarcoma viruses specifically blocks binding of epidermal growth factor to cells. Nature 1976; 264: 26–31
  • Toyoda H, Komurasaki T, Uchida D, Takayama Y, Isobe T, Okuyama T, Hanada K. Epiregulin. A novel epidermal growth factor with mitogenic activity for rat primary hepatocytes. J Biol Chem 1995; 270: 7495–7500
  • Troyer KL, Luetteke NC, Saxon ML, Qiu TH, Xian CJ, Lee DC. Growth retardation, duodenal lesions, and aberrant ileum architecture in triple null mice lacking EGF, amphiregulin and TGF-alpha. Gastroenterology 2001; 121: 68–78
  • Tzahar E, Yarden Y. The ErbB-2/HER2 oncogenic receptor of adenocarcinomas: From orphanhood to multiple stromal ligands. Biochim Biophys Acta 1998; 1377: M25–M37
  • Uchida T, Wada K, Akamatsu T, Yonezawa M, Noguchi H, Mizoguchi A, Kasuga M, Sakamoto C. A novel epidermal growth factor-like molecule containing two follistatin modules stimulates tyrosine phosphorylation of ErbB-4 in MKN28 gastric cancer cells. Biochem Biophys Res Commun 1999; 266: 593–602
  • van der Geer P, Hunter T, Lindberg RA. Receptor protein-tyrosine kinases and their signal transduction pathways. Annu Rev Cell Biol 1994; 10: 251–337
  • Vecchi M, Baulida J, Carpenter G. Selective cleavage of the heregulin receptor ErbB-4 by protein kinase C activation. J Biol Chem 1996; 271: 18989–18995
  • Wallasch C, Crabtree JE, Bevec D, Robinson PA, Wagner H, Ullrich A. Helicobacter pylori-stimulated EGF receptor transactivation requires metalloprotease cleavage of HB-EGF. Biochem Biophys Res Commun 2002; 295: 695–701
  • Wang XY, Smith DI, Frederick L, James CD. Analysis of EGF receptor amplicons reveals amplification of multiple expressed sequences. Oncogene 1998; 16: 191–195
  • Weskamp G, Kratzschmar J, Reid MS, Blobel CP. MDC9, a widely expressed cellular disintegrin containing cytoplasmic SH3 ligand domains. J Cell Biol 1996; 132: 717–726
  • Wetzker R, Bohmer FD. Transactivation joins multiple tracks to the ERK/MAPK cascade. Nat Rev Mol Cell Biol 2003; 4: 651–657
  • Wharton KA, Johansen KM, Xu T, Artavanis-Tsakonas S. Nucleotide sequence from the neurogenic locus notch implies a gene product that shares homology with proteins containing EGF-like repeats. Cell 1985; 43: 567–581
  • Wolfsberg TG, White JM. ADAMs in fertilization and development. Dev Biol 1996; 180: 389–401
  • Wong ST, Winchell LF, McCune BK, Earp HS, Teixido J, Massague J, Herman B, Lee DC. The TGF-alpha precursor expressed on the cell surface binds to the EGF receptor on adjacent cells, leading to signal transduction. Cell 1989; 56: 495–506
  • Wouters MA, Rigoutsos I, Chu CK, Feng LL, Sparrow DB, Dunwoodie SL. Evolution of distinct EGF domains with specific functions. Protein Sci 2005; 14: 1091–1103
  • Xie W, Paterson AJ, Chin E, Nabell LM, Kudlow JE. Targeted expression of a dominant negative epidermal growth factor receptor in the mammary gland of transgenic mice inhibits pubertal mammary duct development. Mol Endocrinol 1997; 11: 1766–1781
  • Xu KP, Ding Y, Ling J, Dong Z, Yu FS. Wound-induced HB-EGF ectodomain shedding and EGFR activation in corneal epithelial cells. Invest Ophthalmol Vis Sci 2004; 45: 813–820
  • Yamazaki S, Iwamoto R, Saeki K, Asakura M, Takashima S, Yamazaki A, Kimura R, Mizushima H, Moribe H, Higashiyama S, Endoh M, Kaneda Y, Takagi S, Itami S, Takeda N, Yamada G, Mekada E. Mice with defects in HB-EGF ectodomain shedding show severe developmental abnormalities. J Cell Biol 2003; 163: 469–475
  • Yan Y, Shirakabe K, Werb Z. The metalloprotease Kuzbanian (ADAM10) mediates the transactivation of EGF receptor by G-protein-coupled receptors. J Cell Biol 2002; 158: 221–226
  • Yang H, Jiang D, Li W, Liang J, Gentry LE, Brattain MG. Defective cleavage of membrane bound TGF-alpha leads to enhanced activation of the EGF receptor in malignant cells. Oncogene 2000; 19: 1901–1914
  • Yarden Y, Sliwkowski MX. Untangling the ErbB signalling network. Nat Rev Mol Cell Biol 2001; 2: 127–137
  • Yu WH, Woessner JF, Jr, McNeish JD, Stamenkovic I. 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 2002; 16: 307–323
  • Zhang XP, Kamata T, Yokoyama K, Puzon-McLaughlin W, Takada Y. Specific interaction of the recombinant disintegrin-like domain of MDC-15 (metargidin, ADAM-15) with integrin alphavbeta3. J Biol Chem 1998; 273: 7345–7350
  • Zhang Z, Oliver P, Lancaster JJ, Schwarzenberger PO, Joshi MS, Cork J, Kolls JK. Reactive oxygen species mediate tumor necrosis factor-alpha-converting, enzyme-dependent ectodomain shedding induced by phorbol myristate acetate. FASEB J 2001; 15: 303–305
  • Zhang J, Li H, Wang J, Dong Z, Mian S, Yu FS. Role of EGFR transactivation in preventing apoptosis in Pseudomonas aeruginosa-infected human corneal epithelial cells. Invest Ophthalmol Vis Sci 2004; 45: 2569–2576
  • Zhao L, Shey M, Farnsworth M, Dailey MO. Regulation of membrane metalloproteolytic cleavage of l-selectin (CD62l) by the epidermal growth factor domain. J Biol Chem 2001; 276: 30631–30640
  • Zheng Y, Schlondorff J, Blobel CP. Evidence for regulation of the tumor necrosis factor-alpha-convertase (TACE) by protein-tyrosine phosphatase PTPH1. J Biol Chem 2002; 277: 42463–42470

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