Ectodomain shedding and remnant peptide signalling of EGFRs and their ligands

Journal of Biochemistry

Volumn 150, Issue 1, 2011, Pages 15-22

  Higashiyama, Shigeki ^a,b   Nanba, Daisuke ^a   Nakayama, Hironao ^b   Inoue, Hirofumi ^a,b   Fukuda, Shinji ^b  

^a EHIME UNIVERSITY   (Japan)

^b EHIME UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

ADAM; ectodomain shedding; EGFR; EGFR ligand; remnant peptide signalling

Indexed keywords

ADAM PROTEIN; AMPHIREGULIN; BETACELLULIN; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 4; NEU DIFFERENTIATION FACTOR; PROTEIN TYROSINE KINASE;

ARTICLE; CELL CONTACT; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; LIGAND BINDING; NEOPLASM; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN DOMAIN; SIGNAL TRANSDUCTION;

ADAM PROTEINS; CELL MEMBRANE; HUMANS; LIGANDS; METALLOPROTEASES; PEPTIDES; PROTEIN BINDING; PROTEIN SORTING SIGNALS; PROTEIN STRUCTURE, TERTIARY; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION;

EID: 79960102280     PISSN: 0021924X     EISSN: 17562651     Source Type: Journal    
DOI: 10.1093/jb/mvr068     Document Type: Article

References (57)

1. Black, R.A., Rauch, C.T., Kozlosky, C.J., Peschon, J.J., Slack, J.L., Wolfson, M.F., Castner, B.J., Stocking, K.L., Reddy, P., Srinivasan, S., Nelson, N., Boiani, N., Schooley, K.A., Gerhart, M., Davis, R., Fitzner, J.N., Johnson, R.S., Paxton, R.J., March, C.J., and Cerretti, D.P. (1997) A metalloproteinase disintegrin that releases tumor-necrosis factor- from cells. Nature 385, 729-733
2. Moss, M.L., Jin, S.L.C., Milla, M.E., Burkhart, W., Carter, H.L., Chen, W.J., Clay, W.C., Didsbury, J.R., Hassler, D., Hoffman, C.R., Kost, T.A., Lambert, M.H., Leesnitzer, M.A., McCauley, P., McGeehan, G., Mitchell, J., Moyer, M., Pahel, G., Rocque, W., Overton, L.K., Schoenen, F., Seaton, T., Su, J.L., Warnaer, J., Willard, D., and Becherer, J.D. (1997) Cloning of a disintegrin metalloprotease that processes precursor tumor-necrosis factor-a. Nature 385, 733-7336
3. Prenzel, N., Zwick, E., Daub, H., Leserer, M., Abraham, R., Wallasch, C., and Ullrich, A. (1999) EGF receptor transactivation by G-protein-coupled receptors requires metalloproteinase cleavage of proHB-EGF. Nature 402, 884-888
4. Hartmann, D., Tournoy, J., Safting, P., Annaert, W., and De Strooper, B. (2001) Implication of APP secretases in notch signaling. J. Mol. Neurosci. 17, 171-181 (Pubitemid 33063521)
5. Higashiyama, S., Iwabuki, H., Morimoto, C., Hieda, M., Inoue, H., and Matsushita, N. (2008) Membrane-anchored growth factors, the epidermal growth factor family: beyond receptor ligands. Cancer Sci. 99, 214-220 (Pubitemid 351228472)
6. Bray, S.J. (2006) Notch signaling: a simple pathway becomes complex. Nat. Rev. Mol. Cell Biol. 7, 678-689 (Pubitemid 44268213)
7. 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., and Mekada, E. (2003) Mice with defects in HB-EGF ectodomain shedding show severe developmental abnormalities. J. Cell Biol. 163, 469-475 (Pubitemid 37429861)
8. Prenzel, N., Zwick, E., Leserer, M., and Ullrich, A. (2000) Tyrosine kinase signalling in breast cancer. Epidermal growth factor receptor: convergence point for signal integration and diversification. Breast Cancer Res. 2, 184-190 (Pubitemid 32223583)
9. Liebmann, C. (2011) EGF receptor activation by GPCRs: an universal pathway reveals different versions. Mol. Cell. Endocrinol. 331, 222-231
10. Tice, D.A., Biscardi, J.S., Nickles, A.L., and Parsons, S.J. (1999) Mechanism of biological synergy between cellular Src and epidermal growth factor receptor. Proc. Natl Acad. Sci. USA. 96, 1415-1420 (Pubitemid 29098465)
11. Stirnweiss, J., Valkova, C., Ziesché , E., Drube, S., and Liebmann, C. (2006) Muscarinic M2 receptors mediate transactivation of EGF receptor through Fyn kinase and without matrix metalloproteases. Cell Signal 18, 1338-1349
12. Drube, S., Stirnweiss, J., Valkova, C., and Liebmann, C. (2006) Ligand-independent and EGF receptor-supported transactivation: lessons from b2-adrenergic receptor signalling. Cell Signal 18, 1633-1646
13. Edwards, D.R., Handsley, M.M., and Pennington, C.J. (2008) The ADAM metalloproteases. Mol. Asp. Med. 29, 258-289
14. Sahin, U., Weskamp, G., Kelly, K., Zhou, H.M., Higashiyama, S., Peschon, J., Hartmann, D., Saftig, P., and Blobel, C.P. (2004) Distinct roles for ADAM10 and ADAM17 in ectodomain shedding of six EGFR ligands. J. Cell Biol. 164, 769-779 (Pubitemid 38282960)
15. Takeda, S. (2009) Three-dimensional domain architecture of the ADAM family proteinases. Semin. Cell Dev. Biol. 20, 146-152
16. Takeda, S., Igarashi, T., Mori, H., and Araki, S. (2006) Crystal structures of VAP1 reveal ADAMs MDC domain architecture and its unique C-shaped scaffold. EMBO J. 25, 2388-2396 (Pubitemid 44012222)
17. Nishi, E., Hiraoka, Y., Yoshida, K., Okawa, K., and 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 (Pubitemid 44582170)
18. Ohno, M., Hiraoka, Y., Matsuoka, T., Tomimoto, H., Takao, K., Miyakawa, T., Oshima, N., Kiyonari, H., Kimura, T., Kita, T., and Nishi, E. (2009) Nardilysin regulates axonal maturation and myelination in the central and peripheral nervous system. Nat. Neurosci. 12, 1506-1513
19. Rio, C., Buxbaum, J.D., Peschon, J.J., and Corfas, G. (2000) Tumor necrosis factor-|a-converting enzyme is required for cleavage of erbB4/HER4. J. Biol. Chem. 275, 10379-10387 (Pubitemid 30202097)
20. Vecchi, M., Baulida, J., and Carpenter, G. (1996) Selective cleavage of the heregulin receptor ErbB-4 by protein kinase C activation. J. Biol. Chem. 271, 18989-18995 (Pubitemid 26322776)
21. Zhou, W. and Carpenter, G. (2000) Heregulin-dependent trafficking and cleavage of ErbB-4. J. Biol. Chem. 275, 34737-34743
22. Ni, C.Y., Murphy, M.P., Golde, T.E., and Carpenter, G. (2001) γ-Secretase cleavage and nuclear localization of ErbB-4 receptor tyrosine kinase. Science 294, 2179-2181
23. Lee, H.J., Jung, K.M., Huang, Y.Z., Bennett, L.B., Lee, J.S., Mei, L., and Kim, T.W. (2002) Presenilin-dependent gamma-secretase-like intramembrane cleavage of ErbB4. J. Biol. Chem. 277, 6318-6323 (Pubitemid 34968424)
24. Sardi, S.P., Murtie, J., Koirala, S., Patten, B.A., and Corfas, G. (2006) Presenilin-dependent ErbB4 nuclear signaling regulates the timing of astrogenesis in the developing brain. Cell 127, 185-197
25. Williams, C.C., Allison, J.G., Vidal, G.A., Burow, M.E., Beckman, B.S., Marrero, L., and Jones, F.E. (2004) The ERBB4/HER4 receptor tyrosine kinase regulates gene expression by functioning as a STAT5A nuclear chaperone. J. Cell Biol. 167, 469-478 (Pubitemid 39489055)
26. Jones, F.E. (2008) HER4 intracellular domain (4ICD) activity in the developing mammary gland and breast cancer. J. Mammary Gland Biol. Neoplasia 13, 247-258
27. Linggi, B. and Carpenter, G. (2006) ErbB-4 s80 intracellular domain abrogates ETO2-dependent transcriptional repression. J. Biol. Chem. 281, 25373-25380 (Pubitemid 44401925)
28. Komuro, A., Nagai, M., Navin, N.E., and Sudol, M. (2003) WW domain-containing protein YAP associates with ErbB-4 and acts as a co-transcriptional activator for the carboxyl-terminal fragment of ErbB-4 that translocates to the nucleus. J. Biol. Chem. 278, 33334-33341 (Pubitemid 37055785)
29. Zhu, Y., Sullivan, L.L., Nair, S.S., Williams, C.C., Pandey, A.K., Marrero, L., Vadlamudi, R.K., and Jones, F.E. (2006) Coregulation of estrogen receptor by ERBB4/HER4 establishes a growth-promoting autocrine signal in breast tumor cells. Cancer Res. 66, 7991-7998 (Pubitemid 44299163)
30. Linggi, B., Cheng, Q.C., Rao, A.R., and Carpenter, G. (2006) The ErbB-4 s80 intracellular domain is a constitutively active tyrosine kinase. Oncogene 25, 160-163
31. Arasada, R.R. and Carpenter, G. (2005) Secretase-dependent tyrosine phosphorylation of Mdm2 by the ErbB-4 intracellular domain fragment. J. Biol. Chem. 280, 30783-30787 (Pubitemid 41291808)
32. Birchmeier, C. (2009) ErbB receptors and the development of the nervous system. Exp. Cell Res. 315, 611-618
33. Wen, D., Suggs, S.V., Karunagaran, D., Liu, N., Cupples, R.L., Luo, Y., Janssen, A.M., Ben-Baruch, N., Trollinger, D.B., Jacobsen, V.L., Meng, S.U., Lu, H.S., Hu, S., Chang, D., Yang, W., Yanigahara, D., Koski, R., and Yarden, Y. (1994) Structural and functional aspects of the multiplicity of Neu differentiation factors. Mol. Cell Biol. 4, 1909-1919 (Pubitemid 24074586)
34. Holmes, W.E., Sliwkowski, M.X., Akita, R.W., Henzel, W.J., Lee, J., Park, J.W., Yansura, D., Abadi, N., Raab, H., Lewis, G.D., Shepard, H.M., Kuang, W.J., Wood, W.I., Goeddel, D.V., and Vandlen, R.L. (1992) Identification of heregulin, a specific activator of p185erbB2. Science 256, 1205-1210
35. Horiuchi, K., Zhou, H.M., Kelly, K., Manova, K., and Blobel, C.P. (2005) Evaluation of the contributions of ADAMs 9, 12, 15, 17, and 19 to heart development and ectodomain shedding of neuregulins b1 and b2. Dev. Biol. 283, 459-471
36. Bao, J., Wolpowitz, D., Role, L.W., and Talmage, D.A. (2003) Back signaling by the Nrg-1 intercellular domain. J. Cell Biol. 161, 1133-1141 (Pubitemid 36870174)
37. Bao, J., Lin, H., Ouyang, Y., Lei, D., Osma, A., Kim, T.W., Mei, L., Dai, P., Ohlemiller, K.K., and Ambron, R.T. (2004) Activity-dependent transcription regulation of PSD-95 by neuregulin-1 and Eos. Nat. Neurosci. 7, 1250-1258 (Pubitemid 39426245)
38. Goishi, K., Higashiyama, S., Klagsbrun, M., Ishikawa, M., Mekada, E., and Taniguchi, N. (1995) 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 6, 967-980
39. Jackson, L.F., Qiu, T.H., Sunnarborg, S.W., Chang, A., Zhang, C., Patterson, C., and Lee, D.C. (2003) Defective valvulogenesis in HB-EGF and TACE-null mice is associated with aberrant BMP signaling. EMBO J. 22, 2704-2716 (Pubitemid 36712367)
40. 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., and Itoh, M. (2004) The mechanism of cleavage of EGFR ligands induced by inflammatory cytokines in gastric cancer cells. Gastroenterology 127, 559-569
41. Hart, S., Fischer, O.M., Prenzel, N., Zwick-Wallasch, E., Schneider, M., Hennighausen, L., and Ullich, A. (2005) GPCR-induced migration of breast carcinoma cells depends on both EGFR signal transactivation and EGFR-independent pathways. Biol. Chem. 386, 845-855
42. 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., and Higashiyama, S. (2002) Cardiac hypertrophy is inhibited by antagonism of ADAM12 processing of HB-EGF: metalloproteinase inhibitors as a new therapy. Nat. Med. 8, 35-40 (Pubitemid 34101726)
43. Nanba, D., Mammoto, A., Hashimoto, K., and Higashiyama, S. (2003) Proteolytic release of the carboxy-terminal fragment of heparin-binding EGF-like growth factor causes nuclear export of PLZF. J. Cell Biol. 163, 489-502
44. Hieda, M., Isokane, M., Koizumi, M., Higashi, C., Tachibana, T., Shudo, M., Heida, Y., Taguchi, T., and Higashiyama, S. (2008) Membrane-anchored growth factor HB-EGF on cell surface targets to the inner nuclear membrane. J. Cell Biol. 180, 763-769 (Pubitemid 351397776)
45. Kinugasa, Y., Hieda, M., Hori, M., and Higashiyama, S. (2007) The carboxy-terminal fragment of proHB-EGF reverses Bcl6-mediated gene expression. J. Biol. Chem. 282, 14797-14806 (Pubitemid 47093367)
46. Perissi, V., Jepsen, K., Glass, C.K., and Rosenfeld, M.G. (2010) Deconstructing repression: evolving models of co-repressor action. Nat. Rev. Genet. 11, 109-123
47. Nanba, D., Inoue, H., Shigemi, Y., Shirakata, Y., Hashimoto, K., and Higashiyama, S. (2008) An intermediary role of proHB-EGF shedding in growth factor-induced c-myc expression. J. Cell. Physiol. 214, 465-473 (Pubitemid 350309003)
48. Iwamoto, R., Yamazaki, S, Asakura, M., Takashima, S., Hasuwa, H., Miyado, K., Adachi, S., Kitakaze, M., Hashimoto, K., Rabb, G., Klagsbrun, M., Nanba, D., Higashiyama, S., Hori, M., and Mekada, E. (2003) HB-EGF and ErbB signaling is essential for heart function. Proc. Natl Acad. Sci. USA. 100, 3221-3226
49. Nanba, D., Kinugasa, Y., Morimoto, C., Koizumi, M., Yamamura, H., Takahashi, K., Takakura, N., Mekada, E., Hashimoto, K., and Higashiyama, S. (2006) Loss of HB-EGF in smooth muscle or endothelial cell lineages causes heart valve malformation and cardiac hypertrophy. Biochem. Biophys. Res. Commun. 350, 315-321 (Pubitemid 44498636)
50. Yoshida, T., Fukuda, T., Hatano, M., Koseki, H., Okabe, S., Ishibashi, K., Kojima, S., Arima, M., Komuro, I., Ishii, G., Miki, T., Hirosawa, S., Miyasaka, N., Taniguchi, M., Ochiai, T., Isono, K., and Tokuhisa, T. (1999) The role of Bcl6 in mature cardiac myocytes. Cardiovasc. Res. 42, 670-679 (Pubitemid 29298136)
51. Uetani, T., Nakayama, H., Okayama, H., Okura, T., Higaki, J., Inoue, H., and Higashiyama, S. (2009) Insufficient shedding of proHB-EGF enhances hypoxic cell death in H9c2 cardiomyoblasts via activation of Caspase-3 and c-Jun N-terminal kinase. J. Biol. Chem. 284, 12399-12409
52. Lin, J., Hutchinson, L., Gaston, S.M., Raab, G., and Freeman, M.R. (2001) BAG-1 is a novel cytoplasmic binding partner of the membrane form of heparin-binding EGF-like growth factor: a unique role for proHB-EGF in cell survival regulation. J. Biol. Chem. 267, 30127-30132
53. Townsend, P.A., Cutress, R.I., Sharp, A., Brimmell, M., and Packham, G. (2003) BAG-1: a multifunctional regulator of cell growth and survival. Biochim. Biophys. Acta. 1603, 83-98 (Pubitemid 36262942)
54. Isokane, M., Hieda, M., Hamakawa, H., and Higashiyama, S. (2008) Membrane-anchored growth factor amphiregulin on cell surface targets to the inner nuclear membrane. J. Cell Sci. 121, 3608-3618
55. Stoeck, A., Shang, L., and Dempsey, P.J. (2010) Sequential and gamma-secretase-dependent processing of the betacellulin precursor generates a palmitoylated intracellular-domain fragment that inhibits cell growth. J. Cell Sci. 123, 2319-2331
56. Shum, L., Turck, C.W., and Derynck, R. (1996) Cysteines 153 and 154 of transmembrane transforming growth factor-alpha are palmitoylated and mediate cytoplasmic protein association. J. Biol. Chem. 271, 28502-28508 (Pubitemid 26374672)
57. Cheng, H., Vetrivel, K.S., Drisdel, R.C., Meckler, X., Gong, P., Leem, J.Y, Li, T., Carter, M., Chen, Y., Nguyen, P., Iwatsubo, T., Tomita, T., Wong, P.C., Green, W.N., Kounnas, M.Z., and Thinakaran, G. (2009) S-palmitoylation of gamma-secretase subunits nicastrin and APH-1. J. Biol. Chem. 284, 1373-1384