Removal of the membrane-anchoring domain of epidermal growth factor leads to intracrine signaling and disruption of mammary epithelial cell organization

Journal of Cell Biology

Volumn 143, Issue 5, 1998, Pages 1317-1328

  Wiley, H Steven ^a   Woolf, Margaret F ^a   Opresko, Lee K ^a   Burke, Patrick M ^a   Will, Birgit ^a   Morgan, Jeffrey R ^b   Lauffenburger, Douglas A ^c  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Autocrine; Epidermal growth factor; Epithelium; Intracrine; Receptors

Indexed keywords

EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; MATRIGEL;

ARTICLE; AUTOCRINE EFFECT; BREAST EPITHELIUM; CELL PROLIFERATION; CONTROLLED STUDY; CYTOPLASM VESICLE; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANIMALS; ANTIBODIES, MONOCLONAL; BASE SEQUENCE; BREAST; CELL COMMUNICATION; CELL LINE; DNA PRIMERS; EPIDERMAL GROWTH FACTOR; EPITHELIAL CELLS; FEMALE; HUMANS; LIGANDS; MEMBRANES; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION;

EID: 0032583167     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.143.5.1317     Document Type: Article

References (81)

1. Agard, D.A., Y. Hiraoka, P. Shaw, and J.W. Sedat. 1989. Fluorescence microscopy in three dimensions. In; Fluorescence Microscopy of Living Cells in Culture. Vol. 30. D.L. Taylor and Y.L. Wang, editors. Academic Press, San Diego, CA. 353-377.
2. Alroy, I., and Y. Yarden. 1997. The ErbB signaling network in embryogenesis and oncogenesis: signal diversification through combinatorial ligand-receptor interactions. FEBS Lett. 410:83-86.
3. Anklesaria, P., J. Teixido, M. Laiho, J.H. Pierce, J.S. Greenberger, and J. Massagué. 1990. 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. 87:3289-3293.
4. Aroian, R.V., G.M. Lesa, and P.W. Sternberg. 1994. Mutations in the Cae-norhabditis elegans let-23 EGFR-like gene define elements important for cell-type specificity and function. EMBO (Eur. Mol. Biol. Organ.) J. 13:360-366.
5. Atlas, I., J. Mendelsohn, J. Baselga, W.R. Fair, H. Masui, and R. Kumar. 1992. Growth regulation of human renal carcinoma cells: role of transforming growth factor alpha. Cancer Res. 52:3335-3339.
6. Band, V., and R. Sager. 1989. Distinctive traits of normal and tumor-derived human mammary epithelial cells expressed in a medium that supports long-term growth of both cell types. Proc. Natl. Acad. Sci. USA. 86:1249-1253.
7. Barnard, J.A., R. Graves-Deal, M.R. Pittelkow, R. DuBois, P. Cook, G.W. Ramsey, P.R. Bishop, L. Damstrup, and R.J. Coffey. 1994. Auto- and cross-induction within the mammalian epidermal growth factor-related peptide family. J. Biol. Chem. 269:22817-22822.
8. Barrandon, Y., and H. Green. 1987. Cell migration is essential for sustained growth of keratinocyte colonies: the roles of transforming growth factor-alpha and epidermal growth factor. Cell. 50:1131-1137.
9. Baselga, J., J. Mendelsohn, Y.M. Kim, and A. Pandiella. 1996. Autocrine regulation of membrane transforming growth factor-alpha cleavage. J. Biol. Chem. 271:3279-3284.
10. Battegay, E.J., J. Rupp, L. Iruela-Arispe, E.H. Sage, and M. Pech. 1994. PDGF-BB modulates endothelial proliferation and angiogenesis in vitro via PDGF beta-receptors. J. Cell Biol. 125:917-928.
11. Beerli, R.R., and N.E. Hynes. 1996. Epidermal growth factor-related peptides activate distinct subsets of ErbB receptors and differ in their biological activities. J. Biol. Chem. 271:6071-6076.
12. Bejcek, B.E., D.Y. Li, and T.F. Deuel. 1989. Transformation by v-sis occurs by an internal autoactivation mechanism. Science. 245:1496-1499.
13. Besner, G.E., D. Whelton, M.A. Crissman-Combs, C.L. Steffen, G.Y. Kim, and D.R. Brigstock. 1992. Interaction of heparin-binding EGF-like growth factor (HB-EGF) with the epidermal growth factor receptor: modulation by heparin, heparinase, or synthetic heparin-binding HB-EGF fragments. Growth Factors. 7:289-296.
14. Bosenberg, M.W., A. Pandiella, and J. Massagué. 1993. Activated release of membrane-anchored TGF-alpha in the absence of cytosol. J. Cell Biol. 122: 95-101.
15. Brachmann, R., P.B. Lindquist, M. Nagashima, W. Kohr, T. Lipari, M. Napier, and R. Derynck. 1989. Transmembrane TGF-alpha precursors activate EGF/TGF-alpha receptors. Cell. 56:691-700.
16. Carpenter, G., and S. Cohen. 1990. Epidermal growth factor. J. Biol. Chem. 265:7709-7712.
17. Carrway, K.L., and C.A. Carraway. 1995. Signaling, mitogenesis and the cytoskeleton: where the action is. Bioessays. 17:171-175.
18. Chang, W., C. Upton, S.L. Hu, A.F. Purchio, and G. McFadden. 1987. The genome of Shope fibroma virus, a tumorigenic poxvirus, contains a growth factor gene with sequence similarity to those encoding epidermal growth factor and transforming growth factor alpha. Mol. Cell. Biol. 7:535-540.
19. Chiu, I.M., E.P. Reddy, D. Givol, K.C. Robbins, S.R. Tronick, and S.A. Aaronson. 1984. Nucleotide sequence analysis identifies the human c-sis proto-oncogene as a structural gene for platelet-derived growth factor. Cell. 37:123-129.
20. Cook, P.W., N.M. Ashton, C.E. Karkaria, D.C. Siess, and G.D. Shipley. 1995. Differential effects of a heparin antagonist (hexadimethrine) or chlorate on amphiregulin, basic fibroblast growth factor, and heparin-binding EGF-like growth factor activity. J. Cell Physiol. 163:418-429.
21. Danos, O., and R.C. Mulligan. 1988. Safe and efficient generation of recombinant retroviruses with amphotropic and ecotropic host ranges. Proc. Natl. Acad. Sci. USA. 85:6460-6464.
22. Dempsey, P.J., and R.J. Coffey. 1994. Basolateral targeting and efficient consumption of transforming growth factor-alpha when expressed in Madin-Darby canine kidney cells. J. Biol. Chem. 269:16878-16889.
23. Dempsey, P.J., K.S. Meise, Y. Yoshitake, K. Nishikawa, and R.J. Coffey. 1997. 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. 138:747-758.
24. Derynck, R. 1992. The physiology of transforming growth factor-alpha. Adv. Cancer Res. 58:27-52.
25. Downing, M.T., D.R. Brigstock, M.H. Luquette, M. Crissman-Combs, and G.E. Besner. 1997. Immunohistochemical localization of heparin-binding epidermal growth factor-like growth factor in normal skin and skin cancers. Histochem. J. 29:735-744.
26. Earp, H.S., T.L. Dawson, X. Li, and H. Yu. 1995. Heterodimerization and functional interaction between EGF receptor family members: a new signaling paradigm with implications for breast cancer research. Breast Cancer Res. Treat. 35:115-132.
27. Ebner, R., and R. Derynck. 1991. Epidermal growth factor and transforming growth factor-alpha: differential intracellular routing and processing of ligand-receptor complexes. Cell Regul. 2:599-612.
28. Eming, S.A., J. Lee, R.G. Snow, R.G. Tompkins, M.L. Yarmush, and J.R. Morgan. 1995. Genetically modified human epidermis overexpressing PDGF-A directs the development of a cellular and vascular connective tissue stroma when transplanted to athymic mice-implications for the use of genetically modified keratinocytes to modulate dermal regeneration. J. Invest. Dermatol. 105:756-763.
29. Engler, D.A., R.K. Matsunami, S.R. Campion, C.D. Stringer, A. Stevens, and S.K. Niyogi. 1988. Cloning of authentic human epidermal growth factor as a bacterial secretory protein and its initial structure-function analysis by site-directed mutagenesis. J. Biol. Chem. 263:12384-12390.
30. Fisher, D.A., E.C. Salido, and L. Barajas. 1989. Epidermal growth factor and the kidney. Annu. Rev. Physiol. 51:67-80.
31. Fowler, K.J., F, Walker, W. Alexander, M.L. Hibbs, E.C. Nice, R.M. Bohmer, G.B. Mann, C. Thumwood, R. Maglitto, J.A. Danks, et al. 1995. A mutation in the epidermal growth factor receptor in waved-2 mice has a profound effect on receptor biochemistry that results in impaired lactation. Proc. Natl. Acad Sci. USA. 92:1465-1469.
32. French, A.R., D.K. Tadaki, S.K. Niyogi, and D.A. Lauffenburger. 1995. Intracellular trafficking of epidermal growth factor family ligands is directly influenced by the pH sensitivity of the receptor/ligand interaction. J. Biol. Chem. 270:4334-4340.
33. Gill, G.N., T. Kawamoto, C. Cochet, A. Le. J.D. Sato, H. Masui, C. McLeod, and J. Mendelsohn. 1984. Monoclonal anti-epidermal growth factor receptor antibodies which are inhibitors of epidermal growth factor binding and antagonists of epidermal growth factor-stimulated tyrosine protein kinase activity. J. Biol. Chem. 259:7755-7760.
34. Gill, G.N., and W. Weber. 1987. Purification of functionally active epidermal growth factor receptor protein using a competitive antagonistic monoclonal antibody and a competitive elution with epidermal growth factor. Methods Enzymol. 146:82-88.
35. Goishi, K., S. Higashiyama, M. Klagsbrun, N. Nakano, T. Umata, M. Ishikawa, E. Mekada, and N. Taniguchi. 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.
36. Gomm, J.J., R.C. Coope, P.J. Browne, and R.C. Coombes. 1997. Separated human breast epithelial and myoepithelial cells have different growth factor requirements in vitro but can reconstitute normal breast lobuloalveolar structure. J. Cell. Physiol. 171:11-19.
37. Hammond, S.L., R.G. Ham, and M.R. Stampfer. 1984. Serum-free growth of human mammary epithelial cells: rapid clonal growth in defined medium and extended serial passage with pituitary extract. Proc. Natl. Acad. Sci. USA. 81:5435-5439.
38. Hashimoto, K., S. Higashiyama, H. Asada, E. Hashimura, T. Kobayashi, K. Sudo, T. Nakagawa, D. Damm, K. Yoshikawa, and N. Taniguchi. 1994. Heparin-binding epidermal growth factor-like growth factor is an autocrine growth factor for human keratinocytes. J. Biol. Chem. 269:20060-20066.
39. Higashiyama, S., J.A. Abraham, J. Miller, J.C. Fiddes, and M. Klagsbrun. 1991. A heparin-binding growth factor secreted by macrophage-like cells that is related to EGF. Science. 251:936-939.
40. Higashiyama, S., R. Iwamoto, K. Goishi, G. Raab, N. Taniguchi, M. Klagsbrun, and E. Mekada. 1995. The membrane protein CD9/DRAP 27 potentiates the juxtacrine growth factor activity of the membrane-anchored heparin-binding EGF-like growth factor. J. Cell Biol. 128:929-938.
41. Lee, B.A., and D.J. Donoghue. 1992. Intracellular retention of membrane-anchored v-sis protein abrogates autocrine signal transduction. J. Cell Biol. 118:1057-1070.
42. Leevers, S.J., H.F. Paterson, and C.J. Marshall. 1994. Requirement for Ras in Rat activation is overcome by targeting Raf to the plasma membrane. Nature. 369:411-414.
43. Li, S., G.D. Plowman, S.D. Buckley, and G.D. Shipley. 1992. Heparin inhibition of autonomous growth implicates amphiregulin as an autocrine growth factor for normal human mammary epithelial cells. J. Cell. Physiol. 153:103-111.
44. Luetteke, N.C., T.H. Qiu, R.L. Peiffer, P. Oliver, O. Smithies, and D.C. Lee. 1993. TGF alpha deficiency results in hair follicle and eye abnormalities in targeted and waved-1 mice. Cell. 73:263-278.
45. Lupu, R., M. Cardillo, L. Harris, M. Hijazi, and K. Rosenberg. 1995. Interaction between erbB-receptors and heregulin in breast cancer tumor progression and drug resistance. Semin. Cancer Biol. 6:135-145.
46. Mann, G.B., K.J. Fowler, A. Gabriel, E.C. Nice, R.L. Williams, and A.R. Dunn. 1993. 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. 73:249-261.
47. Massagué, J., and A. Pandiella. 1993. Membrane-anchored growth factors. Annu. Rev. Biochem. 62:515-541.
48. Matthay, M.A., J.P. Thiery, F. Lafont, F. Stampfer, and B. Boyer. 1993. Transient effect of epidermal growth factor on the motility of an immortalized mammary epithelial cell line. J. Cell Sci. 106:869-878.
49. Miettinen, P.J., J.E. Berger, J. Meneses, Y. Phung, R.A. Pedersen, Z. Werb, and R. Derynck. 1995. Epithelial immaturity and multiorgan failure in mice lacking epidermal growth factor receptor. Nature. 376:337-341.
50. Mroczkowski, B., M. Reich, K. Chen, G.I. Bell, and S. Cohen. 1989. Recombinant human epidermal growth factor precursor is a glycosylated membrane protein with biological activity. Mol. Cell Biol. 9:2771-2778.
51. Opgenorth, A., D. Strayer, C. Upton, and G, McFadden. 1992. Deletion of the growth factor gene related to EGF and TGF alpha reduces virulence of malignant rabbit fibroma virus. Virology. 186:175-191.
52. Opresko, L.K., and H.S. Wiley. 1990. Functional reconstitutional of the human epidermal growth factor receptor system in Xenopus oocytes. J. Cell Biol. 111:1661-1671.
53. Pandiella, A., M.W. Bosenberg, E.J. Huang, P. Besmer, and J. Massagué. 1992. Cleavage of membrane-anchored growth factors involves distinct protease activities regulated through common mechanisms. J. Biol. Chem. 267:24028-24033.
54. Riese, D.J., E.D. Kim, K. Elenius, S. Buckley, M. Klagsbrun, G.D. Plowman, and D.F. Stern. 1996. The epidermal growth factor receptor couples transforming growth factor-alpha, heparin-binding epidermal growth factor-like factor, and amphiregulin to Neu, ErbB-3, and ErbB-4. J. Biol. Chem. 271: 20047-20052.
55. Ruff-Jamison, S., J. McGlade, T. Pawson, K. Chen, and S. Cohen. 1993. Epidermal growth factor stimulates the tyrosine phosphorylation of SHC in the mouse. J. Biol. Chem. 268:7610-7612.
56. Saeki, T., K. Stromberg, C.F. Qi, W.J. Gullick, E. Tahara, N. Normanno, F. Ciardieilo, N. Kenney, G.R. Johnson, and D.S. Salomon. 1992. Differential immunohistochemical detection of amphiregulin and cripto in human normal colon and colorectal tumors. Cancer Res. 52:3467-3473.
57. Sakurai, H., T. Tsukamoto, C.A. Kjelsberg, L.G. Cantley, and S.K. Nigam. 1997. EGF receptor ligands are a large fraction of in vitro branching morphogens secreted by embryonic kidney. Am. J. Physiol. 273:F463-F472.
58. Schneider, C., R.A. Newman, D.R. Sutherland, U. Asser, and M.F. Greaves. 1982. A one-step purification of membrane proteins using a high efficiency immunomatrix. J. Biol. Chem. 257:10766-10769.
59. Schreiber, A.B., M.E. Winkler, and R. Derynck. 1986. Transforming growth factor-alpha: a more potent angiogenic mediator than epidermal growth factor. Science. 232:1250-1253.
60. Schuetz, E.G., D. Li, C.J. Omiecinski, U. Muller-Eberhard, H.K. Kleinman, B. Elswick, and P.S. Guzelian. 1988. Regulation of gene expression in adult rat hepatocytes cultured on a basement membrane matrix. J. Cell. Physiol. 134: 309-323.
61. Shing, Y., G. Christofori, D. Hanahan, Y. Ono, R. Sasada, K. Igarashi, and J. Folkman. 1993. Betacellulin: a mitogen from pancreatic beta cell tumors. Science. 259:1604-1607.
62. Shoyab, M., G.D. Plowman, V.L. McDonald, J.G. Bradley, and G.J. Todaro. 1989. Structure and function of human amphiregulin: a member of the epidermal growth factor family. Science. 243:1074-1076.
63. Sibilia, M., and E.F. Wagner. 1995. Strain-dependent epithelial defects in mice lacking the EGF receptor. Science. 269:234-238.
64. Simske, J.S., S.M. Kaech, S.A. Harp, and S.K. Kim. 1996. LET-23 receptor localization by the cell junction protein LIN-7 during C. elegans vulval induction. Cell. 85:195-204.
65. Snedeker, S.M., C.F. Brown, and R.P. DiAugustine. 1991. Expression and functional properties of transforming growth factor alpha and epidermal growth factor during mouse mammary gland ductal morphogenesis. Proc. Natl. Acad. Sci. USA. 88:276-280.
66. Stampfer, M.R., A. Bodnar, J. Garbe, M. Wong, A. Pan, B. Villeponteau, and P. Yaswen. 1997. Gradual phenotypic conversion associated with immortalization of cultured human mammary epithelial cells. Mol. Biol. Cell. 8:2391-2405.
67. Stampfer, M.R., C.H. Pan, J. Hosoda, J. Bartholomew, J. Mendelsohn, and P. Yaswen. 1993. Blockage of EGF receptor signal transduction causes reversible arrest of normal and immortal human mammary epithelial cells with synchronous reentry into the cell cycle. Exp. Cell Res. 208:175-188.
68. Stampfer, M.R., and P. Yaswen. 1994. Growth, differentiation, and transformation of human mammary epithelial cells in culture. Cancer Treat. Res. 71:29-48.
69. Thompson, S.A., S. Higashiyama, K. Wood, N.S. Pollitt, D. Damm, G. McEnroe, B. Garrick, N. Ashton, K. Lau, N. Hancock, et al. 1994. Characterization of sequences within heparin-binding EGF-like growth factor that mediate interaction with heparin. J. Biol. Chem. 269:2541-2549.
70. Thorne, B.A., and G.D. Plowman. 1994. The heparin-binding domain of amphiregulin necessitates the precursor pro-region for growth factor secretion Mol. Cell. Biol. 14:1635-1646.
71. Threadgill, D.W., A.A. Dlugosz, L.A. Hansen, T. Tennenbaum, U. Lichti, D. Yee, C. LaMantia, T. Mourton, K. Herrup, R.C. Harris, et al. 1995. Targeted disruption of mouse EGF receptor: effect of genetic background on mutant phenotype. Science. 269:230-234.
72. Toyoda, H., T. Komurasaki, Y. Ikeda, M. Yoshimoto, and S. Morimoto. 1995. Molecular cloning of mouse epiregulin, a novel epidermal growth factor-related protein, expressed in the early stage of development. FEBS Lett. 377: 403-407.
73. Traverse, S., K. Seedorf, H. Paterson, C.J. Marshall, P. Cohen, and A. Ullrich. 1994. EGF triggers neuronal differentiation of PC12 cells that overexpress the EGF receptor. Curr. Biol. 4:694-701.
74. Tzahar, E., R. Pinkas-Kramarski, J.D. Moyer, L.N. Klapper, I. Alroy, G. Levkowitz, M. Shelly, S. Henis, M. Eisenstein, B.J. Ratzkin, et al. 1997. Bivalence of EGF-like ligands drives the ErbB signaling network. EMBO (Eur. Mol. Biol. Organ.) J. 16:4938-4950.
75. Upton, C., J.L. Macen, and G. McFadden. 1987. Mapping and sequencing of a gene from myxoma virus that is related to those encoding epidermal growth factor and transforming growth factor alpha. J. Virol. 61:1271-1275.
76. Wiley, H.S. 1985. Receptors as models for the mechanisms of membrane protein turnover and dynamics. Curr. Top. Membr. Transp. 24:369-412.
77. Wiley, H.S. 1988. Anomalous binding of epidermal growth factor to A431 cells is due to the effect of high receptor densities and a saturable endocytic system. J. Cell Biol. 107:801-810.
78. Winkler, M.E., L. O'Connor, M. Winget, and B. Fendly. 1989. Epidermal growth factor and transforming growth factor alpha bind differently to the epidermal growth factor receptor. Biochemistry. 28:6373-6378.
79. Wong, S.T., L.F. Winchell, B.K. McCune, H.S. Earp, J. Teixido, J. Massagué, B. Herman, and D.C. Lee. 1989. The TGF-alpha precursor expressed on the cell surface binds to the EGF receptor on adjacent cells, leading to signal transduction. Cell. 56:495-506.
80. Xie, W., A.J. Paterson, E. Chin, L.M. Nabell, and J.E. Kudlow. 1997. Targeted expression of a dominant negative epidermal growth factor receptor in the mammary gland of transgenic mice inhibits pubertal mammary duct development. Mol. Endocrinol. 11:1766-1781.
81. Yoshitake, Y., and K. Nishikawa. 1988. Production of monoclonal antibodies with specificity for different epitopes on the human epidermal growth factor molecule. Arch. Biochem. Biophys. 263:437-446.