Modeling the effects of HER/ErbB1-3 coexpression on receptor dimerization and biological response

Biophysical Journal

Volumn 90, Issue 11, 2006, Pages 3993-4009

  Shankaran, Harish ^a   Wiley, H Steven ^a   Resat, Haluk ^a  

^a PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPIDERMAL GROWTH FACTOR RECEPTOR 3; EPIDERMAL GROWTH FACTOR RECEPTOR 4;

ARTICLE; CELL GROWTH; CELL TRANSFORMATION; KINETICS; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION;

EID: 33744927122     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.105.080580     Document Type: Article

References (60)

1. Downward, J., Y. Yarden, E. Mayes, G. Scrace, N. Totty, P. Stockwell, A. Ullrich, J. Schlessinger, and M. D. Waterfield. 1984. Close similarity of epidermal growth factor receptor and v-Erb-B oncogene protein sequences. Nature. 307:521-527.
2. Slamon, D. J., G. M. Clark, S. G. Wong, W. J. Levin, A. Ullrich, and W. L. McGuire. 1987. Human breast cancer: correlation of relapse and survival with amplification of the HER-2/Neu oncogene. Science. 235:177-182.
3. Jorissen, R. N., F. Walker, N. Pouliot, T. P. Garrett, C. W. Ward, and A. W. Burgess. 2003. Epidermal growth factor receptor: mechanisms of activation and signalling. Exp. Cell Res. 284:31-53.
4. Holbro, T., G. Civenni, and N. E. Hynes. 2003. The ErbB receptors and their role in cancer progression. Exp. Cell Res. 284:99-110.
5. Stern, D. F. 2003. ErbBs in mammary development. Exp. Cell Res. 284:89-98.
6. Wiley, H. S. 2003. Trafficking of the ErbB receptors and its influence on signaling. Exp. Cell Res. 284:78-88.
7. Citri, A., K. B. Skaria, and Y. Yarden. 2003. The deaf and the dumb: the biology of ErbB-2 and ErbB-3. Exp. Cell Res. 284:54-65.
8. Schlessinger, J. 2000. Cell signaling by receptor tyrosine kinases. Cell. 103:211-225.
9. Carpenter, G. 2000. The EGF receptor: a nexus for trafficking and signaling. Bioessays. 22:697-707.
10. 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.
11. Carpenter, G., and S. Cohen. 1976. 125I-labeled human epidermal growth factor. Binding, internalization, and degradation in human fibroblasts. J. Cell Biol. 71:159-171.
12. Haigler, H. T., J. A. McKanna, and S. Cohen. 1979. Direct visualization of the binding and internalization of a ferritin conjugate of epidermal growth factor in human carcinoma cells A-431. J. Cell Biol. 81:382-395.
13. Baulida, J., and G. Carpenter. 1997. Heregulin degradation in the absence of rapid receptor-mediated internalization. Exp. Cell Res. 232:167-172.
14. Wang, Z., L. Zhang, T. K. Yeung, and X. Chen. 1999. Endocytosis deficiency of epidermal growth factor (EGF) receptor-ErbB2 heterodimers in response to EGF stimulation. Mol. Biol. Cell. 10:1621-1636.
15. Waterman, H., I. Sabanai, B. Geiger, and Y. Yarden. 1998. Alternative intracellular routing of ErbB receptors may determine signaling potency. J. Biol. Chem. 273:13819-13827.
16. 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.
17. Olayioye, M. A., R. M. Neve, H. A. Lane, and N. E. Hynes. 2000. The ErbB signaling network: receptor heterodimerization in development and cancer. EMBO J. 19:3159-3167.
18. 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.
19. Yarden, Y., and M. X. Sliwkowski. 2001. Untangling the ErbB signalling network. Nat. Rev. Mol. Cell Biol. 2:127-137.
20. Yen, L., N. Benlimame, Z. R. Nie, D. Xiao, T. Wang, A. E. Al Moustafa, H. Esumi, J. Milanini, N. E. Hynes, G. Pages, and M. A. Alaoui-Jamali. 2002. Differential regulation of tumor angiogenesis by distinct ErbB homo- and heterodimers. Mol. Biol. Cell. 13:4029-4044.
21. Jackson, J. G., P. St Clair, M. X. Sliwkowski, and M. G. Brattain. 2004. Blockade of epidermal growth factor- or heregulin-dependent ErbB2 activation with the anti-ErbB2 monoclonal antibody 2C4 has divergent downstream signaling and growth effects. Cancer Res. 64:2601-2609.
22. Holbro, T., R. R. Beerli, F. Maurer, M. Koziczak, C. F. Barbas 3rd, and N. E. Hynes. 2003. The ErbB2/ErbB3 heterodimer functions as an oncogenic unit: ErbB2 requires ErbB3 to drive breast tumor cell proliferation. Proc. Natl. Acad. Sci. USA. 100:8933-8938.
23. Pinkas-Kramarski, R., M. Shelly, S. Glathe, B. J. Ratzkin, and Y. Yarden. 1996. Neu differentiation factor/neuregulin isoforms activate distinct receptor combinations. J. Biol. Chem. 271:19029-19032.
24. Carraway 3rd, K. L., S. P. Soltoff, A. J. Diamonti, and L. C. Cantley. 1995. Heregulin stimulates mitogenesis and phosphatidylinositol 3-kinase in mouse fibroblasts transfected with ErbB2/Neu and ErbB3. J. Biol. Chem. 270:7111-7116.
25. Cohen, B. D., P. A. Kiener, J. M. Green, L. Foy, H. P. Fell, and K. Zhang. 1996. The relationship between human epidermal growth-like factor receptor expression and cellular transformation in NIH3T3 cells. J. Biol. Chem. 271:30897-30903.
26. 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.
27. Guy, P. M., J. V. Platko, L. C. Cantley, R. A. Cerione, and K. L. Carraway 3rd. 1994. Insect cell-expressed p180ErbB3 possesses an impaired tyrosine kinase activity. Proc. Natl. Acad. Sci. USA. 91:8132-8136.
28. Klapper, L. N., S. Glathe, N. Vaisman, N. E. Hynes, G. C. Andrews, M. Sela, and Y. Yarden. 1999. The ErbB-2/HER2 oncoprotein of human carcinomas may function solely as a shared coreceptor for multiple stroma-derived growth factors. Proc. Natl. Acad. Sci. USA. 96:4995-5000.
29. 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.
30. Soltoff, S. P., K. L. Carraway 3rd, 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.
31. 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.
32. Hendriks, B. S., G. Orr, A. Wells, H. S. Wiley, and D. A. Lauffenburger. 2005. Parsing ERK activation reveals quantitatively equivalent contributions from epidermal growth factor receptor and HER2 in human mammary epithelial cells. J. Biol. Chem. 280:6157-6169.
33. Resat, H., H. S. Wiley, and D. A. Dixon. 2001. Probability-weighted dynamic Monte Carlo method for reaction kinetics simulations. J. Phys. Chem. B. 105:11026-11034.
34. Haugh, J. M., I. C. Schneider, and J. M. Lewis. 2004. On the cross-regulation of protein tyrosine phosphatases and receptor tyrosine kinases in intracellular signaling. J. Theor. Biol. 230:119-132.
35. Morton-Firth, C. J., and D. Bray. 1998. Predicting temporal fluctuations in an intracellular signalling pathway. J. Theor. Biol. 192:117-128.
36. Faeder, J. R., W. S. Hlavacek, I. Reischl, M. L. Blinov, H. Metzger, A. Redondo, C. Wofsy, and B. Goldstein. 2003. Investigation of early events in Fcε RI-mediated signaling using a detailed mathematical model. J. Immunol. 170:3769-3781.
37. Li, Q. J., A. R. Dinner, S. Qi, D. J. Irvine, J. B. Huppa, M. M. Davis, and A. K. Chakraborty. 2004. CD4 enhances T-cell sensitivity to antigen by coordinating Lck accumulation at the immunological synapse. Nat. Immunol. 5:791-799.
38. Pettigrew, M. F., and H. Resat. 2005. Modeling signal transduction networks: a comparison of two stochastic kinetic simulation algorithms. J. Chem. Phys. 123:114707.
39. Jones, J. T., R. W. Akita, and M. X. Sliwkowski. 1999. Binding specificities and affinities of EGF domains for ErbB receptors. FEBS Lett. 447:227-231.
40. Karunagaran, D., E. Tzahar, N. Liu, D. Wen, and Y. Yarden. 1995. Neu differentiation factor inhibits EGF binding. A model for transregulation within the ErbB family of receptor tyrosine kinases. J. Biol. Chem. 270:9982-9990.
41. Schlessinger, J. 2002. Ligand-induced, receptor-mediated dimerization and activation of EGF receptor. Cell. 110:669-672.
42. Resat, H., J. A. Ewald, D. A. Dixon, and H. S. Wiley. 2003. An integrated model of epidermal growth factor receptor trafficking and signal transduction. Biophys. J. 85:730-743.
43. Brown, K. S., and J. P. Sethna. 2003. Statistical mechanical approaches to models with many poorly known parameters. Phys. Rev. E. 68: 021904.
44. Liu, G., M. T. Swihart, and S. Neelamegham. 2005. Sensitivity, principal component and flux analysis applied to signal transduction: the case of epidermal growth factor mediated signaling. Bioinformatics. 21:1194-1202.
45. Hendriks, B. S., L. K. Opresko, H. S. Wiley, and D. Lauffenburger. 2003. Quantitative analysis of HER2-mediated effects on HER2 and epidermal growth factor receptor endocytosis: distribution of homo- and heterodimers depends on relative HER2 levels. J. Biol. Chem. 278:23343-23351.
46. Kholodenko, B. N., O. V. Demin, G. Moehren, and J. B. Hoek. 1999. Quantification of short term signaling by the epidermal growth factor receptor. J. Biol. Chem. 274:30169-30181.
47. Riese 2nd, D. J., and D. F. Stern. 1998. Specificity within the EGF family/ErbB receptor family signaling network. Bioessays. 20:41-48.
48. Prenzel, N., O. M. Fischer, S. Streit, S. Hart, and A. Ullrich. 2001. The epidermal growth factor receptor family as a central element for cellular signal transduction and diversification. Endocr. Relat. Cancer. 8:11-31.
49. Burke, P., K. Schooler, and H. S. Wiley. 2001. Regulation of epidermal growth factor receptor signaling by endocytosis and intracellular trafficking. Mol. Biol. Cell. 12:1897-1910.
50. Haugh, J. M., K. Schooler, A. Wells, H. S. Wiley, and D. A. Lauffenburger. 1999. Effect of epidermal growth factor receptor internalization on regulation of the phospholipase C-γ1 signaling pathway. J. Biol. Chem. 274:8958-8965.
51. Marshall, C. J. 1995. Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell. 80:179-185.
52. Berger, M. B., J. M. Mendrola, and M. A. Lemmon. 2004. ErbB3/HER3 does not homodimerize upon neuregulin binding at the cell surface. FEBS Lett. 569:332-336.
53. Nagy, P., L. Bene, M. Balazs, W. C. Hyun, S. J. Lockett, N. Y. Chiang, F. Waldman, B. G. Feuerstein, S. Damjanovich, and J. Szollosi. 1998. EGF-induced redistribution of ErbB2 on breast tumor cells: flow and image cytometric energy transfer measurements. Cytometry. 32: 120-131.
54. Nagy, P., G. Vereb, Z. Sebestyen, G. Horvath, S. J. Lockett, S. Damjanovich, J. W. Park, T. M. Jovin, and J. Szollosi. 2002. Lipid rafts and the local density of ErbB proteins influence the biological role of homo- and heteroassociations of ErbB2. J. Cell Sci. 115:4251-4262.
55. Gadella, T. W., Jr., and T. M. Jovin. 1995. Oligomerization of epidermal growth factor receptors on A431 cells studied by time-resolved fluorescence imaging microscopy. A stereochemical model for tyrosine kinase receptor activation. J. Cell Biol. 129:1543-1558.
56. Alimandi, M., A. Romano, M. C. Curia, R. Muraro, P. Fedi, S. A. Aaronson, P. P. Di Fiore, and M. H. Kraus. 1995. Cooperative signaling of ErbB3 and ErbB2 in neoplastic transformation and human mammary carcinomas. Oncogene. 10:1813-1821.
57. Wallasch, C., F. U. Weiss, G. Niederfellner, B. Jallal, W. Issing, and A. Ullrich. 1995. Heregulin-dependent regulation of HER2/Neu oncogenic signaling by heterodimerization with HER3. EMBO J. 14:4267-4275.
58. 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.
59. Garrett, T. P., N. M. McKern, M. Lou, T. C. Elleman, T. E. Adams, G. O. Lovrecz, H. J. Zhu, F. Walker, M. J. Frenkel, P. A. Hoyne, R. N. Jorissen, E. C. Nice, A. W. Burgess, and C. W. Ward. 2002. Crystal structure of a truncated epidermal growth factor receptor extracellular domain bound to transforming growth factor-α. Cell. 110:763-773.
60. Ogiso, H., R. Ishitani, O. Nureki, S. Fukai, M. Yamanaka, J. H. Kim, K. Saito, A. Sakamoto, M. Inoue, M. Shirouzu, and S. Yokoyama. 2002. Crystal structure of the complex of human epidermal growth factor and receptor extracellular domains. Cell. 110:775-787.