Controlled dimerization of ErbB receptors provides evidence for differential signaling by homo- and heterodimers

Molecular and Cellular Biology

Volumn 19, Issue 10, 1999, Pages 6845-6857

  Muthuswamy, Senthil K ^a   Gilman, Michael ^b,c   Brugge, Joan S ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b ARIAD PHARMACEUTICALS INC   (United States)

^c BIOGEN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN ERB; PROTEIN TYROSINE KINASE; RAPAMYCIN; TACROLIMUS; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING SITE; DIMERIZATION; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; RAT; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 0032860819     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.19.10.6845     Document Type: Article

References (83)

1. Alroy, I., and Y. Yarden. 1997. The ErbB signaling network in embyrogensis and oncogenesis: signal diversification through combinatorial ligand-receptor interactions. FEBS Lett. 410:83-86.
2. Amara, J. F., T. Clackson, V. M. Rivera, T. Guo, T. Keenan, S. Natesan, R. Pollock, W. Yang, N. L. Courage, D. A. Holt, and M. Gilman. 1997. A versatile synthetic dimerizer for the regulation of protein-protein interactions. Proc. Natl. Acad. Sci. USA 94:10618-10623.
3. Baulida, J., M. H. Kraus, M. Alimandi, P. P. Di Fiore, and G. Carpenter. 1996. All ErbB receptors other than the epidermal growth factor receptor are endocytosis impaired. J. Biol. Chem. 271:5251-5257.
4. Beerli, R. R., D. Graus-Porta, K. Woods-Cook, X. Chen, Y. Yarden, and N. E. Hynes. 1995. Neu differentiation factor activation of ErbB-3 and ErbB-4 is cell specific and displays a differential requirement for ErbB-2. Mol. Cell. Biol. 15:6496-6505.
5. Belsches, A. P., M. D. Haskell, and S. J. Parsons. 1997. Role of c-Src tyrosine kinase in EGF-induced mitogenesis. Front. Biosci. 2:d501-d518.
6. Birge, R. B., B. S. Knudsen, D. Besser, and H. Hanafusa. 1996. SH2 and SH3-containing adaptor proteins: redundant or independent mediators of intracellular signal transduction. Genes Cells 1:595-613.
7. Blau, C. A., K. R. Peterson, J. G. Drachman, and D. M. Spencer. 1997. A proliferation switch for genetically modified cells. Proc. Natl. Acad. Sci. USA 94:3076-3081.
8. Boyer, B., S. Roche, M. Denoyelle, and J. P. Thiery. 1997. Src and Ras are involved in separate pathways in epithelial cell scattering. EMBO J. 16: 5904-5913.
9. Burden, S., and Y. Yarden. 1997. Neuregulins and their receptors: a versatile signaling module in organogenesis and oncogenesis. Neuron 18:847-855.
10. Burgering, B. M., and P. J. Coffer. 1995. Protein kinase B (c-Akt) in phosphatidylinositol-3-OH kinase signal transduction. Nature 376:599-602. (Comment, 376:553-554.)
11. Burke, C. L., M. A. Lemmon, B. A. Coren, D. M. Engelman, and D. F. Stern. 1997. Dimerization of the p185neu transmembrane domain is necessary but not sufficient for transformation. Oncogene 14:687-696.
12. Burke, C. L., and D. F. Stern. 1998. Activation of Neu (ErbB-2) mediated by disulfide bond-induced dimerization reveals a receptor tyrosine kinase dimer interface. Mol. Cell. Biol. 18:5371-5379.
13. Campbell, S. L., R. Khosravi-Far, K. L. Rossman, G. J. Clark, and C. J. Der. 1998. Increasing complexity of Ras signaling. Oncogene 17:1395-1413.
14. Cao, H., L. Bangalore, C. Dompe, B. J. Bormann, and D. F. Stern. 1992. An extra cysteine proximal to the transmembrane domain induces differential cross-linking of p185neu and p185neu. J. Biol. Chem. 267:20489-20492.
15. Carpenter, C. D., H. A. Ingram, C. Cochet, G. M. Walton, C. S. Lazar, J. M. Sowadski, M. G. Rosenfeld, and G. N. Gill. 1991. Structural analysis of the transmembrane domain of the epidermal growth factor receptor. J. Biol. Chem. 266:5750-5755.
16. Carpenter, G. 1992. Receptor tyrosine kinase substrates: src homology domains and signal transduction. FASEB J. 6:3283-3289.
17. Carraway, K. L., III. 1996. Involvement of the neuregulins and their receptors in cardiac and neural development. Bioessays 18:263-266.
18. Carraway, K. L., III, and L. C. Cantley. 1994. A neu acquaintance for erbB3 and erbB4: a role for receptor heterodimerization in growth signaling. Cell 78:5-8.
19. Clackson, T. Personal communication.
20. Coffer, P. J., J. Jin, and J. R. Woodgett. 1998. Protein kinase B (c-Akt): a multifunctional mediator of phosphatidylinositol 3-kinase activation. Biochem. J. 335:1-13.
21. Crovello, C. S., and K. L. Carraway III. Personal communication.
22. Daly, R. J. 1998. The Grb7 family of signalling proteins. Cell. Signal. 10: 613-618.
23. Di Fiore, P. P., O. Segatto, W. G. Taylor, S. A. Aaronson, and J. H. Pierce. 1990. EGF receptor and erbB-2 tyrosine kinase domains confer cell specificity for mitogenic signaling. Science 248:79-83.
24. Fazioli, F., L. Minichiello, V. Matoska, P. Castagnino, T. Miki, W. T. Wong, and P. P. Di Fiore. 1993. Eps8, a substrate for the epidermal growth factor receptor kinase, enhances EGF-dependent mitogenic signals. EMBO J. 12: 3799-3808.
25. Fazioli, F., L. Minichiello, B. Mat̂oŝkovā, W. T. Wong, and P. P. Di Fiore. 1993. eps15, a novel tyrosine kinase substrate, exhibits transforming activity. Mol. Cell. Biol. 13:5814-5828.
26. Fedi, P., J. H. Pierce, P. P. di Fiore, and M. H. Kraus. 1994. Efficient coupling with phosphatidylinositol 3-kinase, but not phospholipase Cγ or GTPase-activating protein, distinguishes ErbB-3 signaling from that of other ErbB/EGFR family members. Mol. Cell. Biol. 14:492-500.
27. Feng, G. S., and T. Pawson. 1994. Phosphotyrosine phosphatases with SH2 domains: regulators of signal transduction. Trends Genet. 10:54-58.
28. Flanagan, J. G., and P. Leder. 1988. neu protooncogene fused to an immunoglobulin heavy chain gene requires immunoglobulin light chain for cell surface expression and oncogenic transformation. Proc. Natl. Acad. Sci. USA 85:8057-8061.
29. 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.
30. Gassmann, M., and G. Lemke. 1997. Neuregulins and neuregulin receptors in neural development. Curr. Opin. Neurobiol. 7:87-92.
31. Graus-Porta, D., R. R. Beerli, and N. E. Hynes. 1995. Single-chain antibody-mediated intracellular retention of ErbB-2 impairs Neu differentiation factor and epidermal growth factor signaling. Mol. Cell. Biol. 15:1182-1191.
32. Graus-Porta, D., R. R. Beerli, J. M. Daly, and N. E. Hynes. 1997. ErbB-2, the preferred heterodimerization partner of all ErbB receptors, is a mediator of lateral signaling. EMBO J. 16:1647-1655.
33. Hato, T., N. Pampori, and S. J. Shattil. 1998. Complementary roles for receptor clustering and conformational change in the adhesive and signaling functions of integrin alphaIIb beta3. J. Cell Biol. 141:1685-1695.
34. Hijazi, M. M., P. E. Young, M. K. Dougherty, D. S. Bressette, T. T. Cao, J. H. Pierce, L. M. Wong, M. Alimandi, and C. R. King. 1998. NRG-3 in human breast cancers: activation of multiple erbB family proteins. Int. J. Oncol. 13: 1061-1067.
35. Ho, S. N., S. R. Biggar, D. M. Spencer, S. L. Schreiber, and G. R. Crabtree. 1996. Dimeric ligands define a role for transcriptional activation domains in reinitiation. Nature 382:822-826.
36. Hoisinger, L. J., D. M. Spencer, D. J. Austin, S. L. Schreiber, and G. R. Crabtree. 1995. Signal transducticn in T lymphocytes using a conditional allele of Sos. Proc. Natl. Acad. Sci. USA 92:9810-9814.
37. Hoschuetzky, H., H. Aberle, and R. Kemler. 1994. Beta-catenin mediates the interaction of the cadherin-catenin complex with epidermal growth factor receptor. J. Cell Biol. 127:1375-1380.
38. Hynes, N., and D. F. Stern. 1994. The biology of erb-2/neu/HER-2 and its role in cancer. Biochim. Biophys. Acta 1198:165-184.
39. Karunagaran, D., E. Tzahar, R. R. Beerli, X. Chen, D. Graus-Porta, B. J. Ratzkin, R. Seger, N. E. Hynes, and Y. Yarden. 1996. ErbB-2 is a common auxiliary subunit of NDF and EGF receptors: implications for breast cancer. EMBO J. 15:254-264.
40. Kashles, O., D. Szapary, F. Bellot, A. Ullrich, J. Schlessinger, and A. Schmidt. 1988. Ligand-induced stimulation of epidermal growth factor receptor mutants with altered transmembrane regions. Proc. Natl. Acad. Sci. USA 85:9567-9571.
41. Kim, H. H., S. L. Sierke, and J. G. Koland. 1994. Epidermal growth factor-dependent association of phosphatidylinositol 3-kinase with the erbB3 gene product. J. Biol. Chem. 269:24747-24755.
42. Lenferink, A. E., R. Pinkas-Kramarski, M. L. van de Poll, M. J. van Vugt, L. N. Klapper, E. Tzahar, H. Waterman, M. Sela, E. J. van Zoelen, and Y. Yarden. 1998. Differential endocytic routing of homo- and hetero-dimeric ErbB tyrosine kinases confers signaling superiority to receptor heterodimers. EMBO J. 17:3385-3397.
43. Levkowitz, G., L. N. Klapper, E. Tzahar, A. Freywald, M. Sela, and Y. Yarden. 1996. Coupling of the c-Cbl protooncogene product to ErbB-1/EGF-receptor but not to other ErbB proteins. Oncogene 12:1117-1125.
44. Levkowitz, G., H. Waterman, E. Zamir, Z. Kam, S. Oved, W. Y. Langdon, L. Beguinot, B. Geiger, and Y. Yarden. 1998. c-Cbl/Sli-1 regulates endocytic sorting and ubiquitination of the epidermal growth factor receptor. Genes Dev. 12:3663-3674.
45. Liberles, S. D., S. T. Diver, D. J. Austin, and S. L. Schreiber. 1997. Inducible gene expression and protein translocation using nontoxic ligands identified by a mammalian three-hybrid screen. Proc. Natl. Acad. Sci. USA 94:7825-7830.
46. Liu, Y., and A. Altman. 1998. Cbl: complex formation and functional implications. Cell. Signal. 10:377-385.
47. MacCorkle, R. A, K. W. Freeman, and D. M. Spencer. 1998. Synthetic activation of caspases: artificial death switches. Proc. Natl. Acad. Sci. USA 95:3655-3660.
48. Miloso, M., M. Mazzotti, W. C. Vass, and L. Beguinot. 1995. SHC and GRB-2 are constitutively activated by an epidermal growth factor receptor with a point mutation in the transmembrane domain. J. Biol. Chem. 270: 19557-19562.
49. Miyake, S., M. L. Lupher, Jr., C. E. Andoniou, N. L. Lill, S. Ota, P. Douillard, N. Rao, and H. Band. 1997. The Cbl protooncogene product: from an enigmatic oncogene to center stage of signal transduction. Crit. Rev. Oncog. 8:189-218.
50. Morgenstern, J. P., and H. Land. 1990. Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids Res. 18:3587-3596.
51. Muthuswamy, S. K., and W. J. Muller. 1995. Direct and specific interaction of c-Src with Neu is involved in signaling by the epidermal growth factor receptor. Oncogene 11:271-279.
52. Nolan, G. P. 1997, posting date. Protocol. [Online.] http://www.stanford.edu/group/nolan/NL-retropage.html. [11 August 1999, last date accessed.]
53. Ojanlemi, M., and K. Vuori. 1997. Epidermal growth factor modulates tyrosine phosphorylation of p130Cas. Involvement of phosphatidylinositol 3′-kinase and actin cytoskeleton. J. Biol. Chem. 272:25993-25998.
54. Olayioye, M. A., D. Graus-Porta, R. R. Beerli, J. Rohrer, B. Gay, and N. E. Hynes. 1998. ErbB-1 and ErbB-2 acquire distinct signaling properties dependent upon their dimerization partner. Mol. Cell. Biol. 18:5042-5051.
55. Pinkas-Kramarski, R., L. Soussan, H. Waterman, G. Levkowitz, I. Alroy, L. Klapper, S. Lavi, R. Seger, B. J. Ratzkin, M. Sela, and Y. Yarden. 1996. Diversification of Neu differentiation factor and epidermal growth factor signaling by combinatorial receptor interactions. EMBO J. 15:2452-2467.
56. Prigent, S. A., and W. Gullick. 1994. Identification of c-erbB-3 binding sites for phosphotidyl 3′-kinase and SHC using an EGF receptor/c-erbB-3 chimera. EMBO J. 13:2831-2841.
57. Rankin, S., R. Hooshmand-Rad, L. Claesson-Welsh, and E. Rozengurt. 1996. Requirement for phosphatidylinositol 3′-kinase activity in platelet-derived growth factor-stimulated tyrosine phosphorylation of p125 focal adhesion kinase and paxillin. J. Biol. Chem. 271:7829-7834.
58. Riese, D. J., II, and D. F. Stern. 1998. Specificity within the EGF family/ErbB receptor family signaling network. Bioessays 20:41-48.
59. Riese, D. J., II, T. M. van Raaji, G. D. Plowman, G. C. Andrews, and D. F. Stern. 1995. The cellular response to neuregulins is governed by complex interactions of the erbB receptor family. Mol. Cell. Biol. 15:5770-5776.
60. Rivera, V. M., T. Clackson, S. Natesan, R. Pollock, J. F. Amara, T. Keenan, S. R. Magari, T. Phillips, N. L. Courage, F. Cerasoli, Jr., D. A. Holt, and M. Gilman. 1996. A humanized system for pharmacologic control of gene expression. Nat. Med. 2:1028-1032. (Comment, 2:977-978.)
61. Romano, A., W. T. Wong, M. Santoro, P. J. Wirth, S. S. Thorgeirsson, and P. P. Di Fiore. 1994. The high transforming potency of erbB-2 and ret is associated with phosphorylation of paxillin and a 23 kDa protein. Oncogene 9:2923-2933.
62. Siegel, P. M., D. L. Dankort, W. R. Hardy, and W. J. Muller. 1994. Novel activating mutations in the neu proto-oncogene involved in induction of mammary tumors. Mol. Cell. Biol. 14:7068-7077.
63. Siegel, P. M., and W. J. Muller. 1996. Mutations affecting conserved cysteine residues within the extracellular domain of Neu promote receptor dimerization and activation. Proc. Natl. Acad. Sci. USA 93:8878-8883.
64. Skolnik, E. Y., B. Margolis, M. Mohammadi, E. Lowenstein, R. Fischer, A. Drepps, A. Ullrich, and J. Schlessinger. 1991. Cloning of PI3 kinase-associated p85 utilizing a novel method for expression/cloning of target proteins for receptor tyrosine kinases. Cell 65:83-90.
65. Sliwkowski, M. X., G. Schaefer, R. W. Akita, J. A. Lofgren, V. D. Fitzpatrick, A. Nuijens, B. M. Fendly. R. A. Cerione, R. L. Vandlen, and K. L. Carraway III. 1994. Coexpression of erbB2 and erbB3 proteins reconstitutes a high affinity receptor for heregulin. J. Biol. Chem. 269:14661-14665.
66. Soltoff, S. P., and L. C. Cantley. 1996. p120cbl is a cytosolic adapter protein that associates with phosphoinositide 3-kinase in response to epidermal growth factor in PC12 and other cells. J. Biol. Chem. 271:563-567.
67. Soltoff, S. P., K. L. Carraway III, S. A. Prigent, W. G. Gullick, and L. C. Cantley. 1994. ErbB3 is involved in activation of phosphatidylinositol 3-kinase by epidermal growth factor. Mol. Cell. Biol. 14:3550-3558.
68. Sorkin, A., and C. M. Waters. 1993. Endocytosis of growth factor receptors. Bioessays 15:375-382.
69. Sorokin, A., M. A. Lemmon, A. Ullrich, and J. Schlessinger. 1994. Stabilization of an active dimeric form of the epidermal growth factor receptor by introduction of an inter-receptor disulfide bond. J. Biol. Chem. 269:9752-9759.
70. Spencer, D. M. 1996. Creating conditional mutations in mammals. Trends Genet. 12:181-187.
71. Spencer, D. M., P. J. Belshaw, L. Chen, S. N. Ho, F. Randazzo, G. R. Crabtree, and S. L. Schreiber. 1996. Functional analysis of Fas signaling in vivo using synthetic inducers of dimerization. Curr. Biol. 6:839-847.
72. Spencer, D. M., I. Graef, D. J. Austin, S. L. Schreiber, and G. R. Crabtree. 1995. A general strategy for producing conditional alleles of Src-like tyrosine kinases. Proc. Natl. Acad. Sci. USA 92:9805-9809.
73. Spencer, D. M., T. J. Wandless, S. L. Schreiber, and G. R. Crabtree. 1993. Controlling signal transduction with synthetic ligands. Science 262:1019-1024. (Comment, 262:989.)
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, M. Sela, G. C. Andrews, and Y. Yarden. 1997. Bivalence of EGF-like ligands drives the ErbB signaling network. EMBO J. 16:4938-4950.
75. Tzahar, E., H. Waterman, X. Chen, G. Levkowitz, D. Karunagaran, S. Lavi, B. J. Ratzkin, and Y. Yarden. 1996. A hierarchical network of interreceptor interactions determines signal transduction by Neu differentiation factor/neuregulin and epidermal growth factor. Mol. Cell. Biol. 16:5276-5287.
76. Wang, L. M., A. Kuo, M. Almandi, M. C. Veri, C. C. Lee, V. Kapoor, N. Ellmore, X. H. Chen, and J. H. Pierce. 1998. ErbB2 expression increases the spectrum and potency of ligand-mediated signal transduction through ErbB4. Proc. Natl. Acad. Sci. USA 95:6809-6814.
77. Webster, M. A., and W. J. Muller. 1994. Mammary tumorigenesis and metastasis in transgenic mice. Semin. Cancer Biol. 5:69-76.
78. Weiner, D. B., J. Liu, J. A. Cohen, W. V. Williams, and M. I. Greene. 1989. A point mutation in the neu oncogene mimics ligand induction of receptor aggregation. Nature 339:230-231.
79. Weiss, A., and J. Schlessinger. 1998. Switching signals on or off by receptor dimerization. Cell 94:277-280.
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. Yang, J., K. Symes, M. Mercola, and S. L. Schreiber. 1998. Small-molecule control of insulin and PDGF receptor signaling and the role of membrane attachment. Curr. Biol. 8:11-18.
82. Zhang, K., J. Sun, N. Liu, D. Wen, D. Chang, A. Thomason, and S. K. Yoshinaga. 1996. Transformation of NIH 3T3 cells by HER3 or HER4 receptors requires the presence of HER1 or HER2. J. Biol. Chem. 271: 3884-3890.
83. Zrihan-Licht, S., J. Lim, I. Keydar, M. X. Sliwkowski, J. E. Groopman, and H. Avraham. 1997. Association of csk-homologous kinase (CHK) (formerly MATK) with HER-2/ErbB-2 in breast cancer cells. J. Biol. Chem. 272: 1856-1863.