HER2-mediated effects on EGFR endosomal sorting: Analysis of biophysical mechanisms

Biophysical Journal

Volumn 85, Issue 4, 2003, Pages 2732-2745

  Hendriks, Bart S ^a   Wiley, H Steven ^c   Lauffenburger, Douglas ^a,b  

^a Massachusetts Institute of Technology Cambridge   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; GENE PRODUCT; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG;

ARTICLE; BIOPHYSICS; CELLULAR DISTRIBUTION; COMPLEX FORMATION; CONTROLLED STUDY; ENDOSOME; GENE OVEREXPRESSION; INTERNALIZATION; MOLECULAR MODEL; NONHUMAN; ONCOGENE NEU; PROMOTER REGION; PROTEIN DEGRADATION; PROTEIN FAMILY; QUALITATIVE ANALYSIS; RECYCLING; SIGNAL TRANSDUCTION;

EID: 0141530936     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(03)74696-7     Document Type: Article

References (58)

1. Agus, D. B., R. W. Akita, W. D. Fox, G. D. Lewis, B. Higgins, P. I. Pisacane, J. A. Lofgren, C. Tindell, D. P. Evans, K. Maiese, H. I. Scher, and M. X. Sliwkowski. 2002. Targeting ligand-activated ErbB2 signaling inhibits breast and prostate tumor growth. Cancer Cell. 2:127-137.
2. Alroy, I., and Y. Yarden. 1997. The ErbB signaling network in embryogenesis and oncogenesis: signal diversification through combinatorial ligand-receptor interactions. Fed. Eur. Biol. Sci. Lett. 410:83-86.
3. Baselga, J. 2002. A new anti-ErbB2 strategy in the treatment of cancer: prevention of ligand-dependent ErbB2 receptor heterodimerization. Cancer Cell. 2:93-94.
4. Baulida, J., M. H. Kraus, M. Alimandi, P. P. DiFiore, and G. Carpenter. 1996. All ErbB receptors other than the epidermal growth factor receptor are endocytosis impaired. J. Biol. Chem. 271:5251-5257.
5. Brandt, B. H., A. Roetger, T. Dittmar, G. Nikolai, M. Seeling, A. Merschjann, J.-R. Nofer, G. Dehmer-Moller, R. Junker, G. Assmann, and K. S. Zaenker. 1999. c-ErbB-2/EGFR as dominant heterodimerization partners determine a motogenic phenotype in human breast cancer cells. FASEB J. 13:1939-1950.
6. Burke, P. M., 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.
7. Chazin, V. R., M. Kaleko, A. D. Miller, and D. J. Slamon. 1992. Transformation mediated by the human HER-2 gene independent of the epidemial growth factor receptor. Oncogene. 7:1859-1866.
8. DiFiore, P. P., J. H. Pierce, T. P. Fleming, R. Hazan, A. Aullrich, C. R. King, J. Schlessinger, and S. A. Aaronson. 1987a. Overexpression of the human EGF receptor confers an EGF-dependent transformed phenotype to NIH 3T3 cells. Cell. 51:1063-1070.
9. DiFiore, P. P., J. H. Pierce, M. H. Kraus, O. Segatto, C. R. King, and S. A. Aaronson. 1987b. ErbB-2 is a potent oncogene when overexpressed in NIH/3T3 cells. Science. 237:178-182.
10. Earp, H. S., T. L. Dawson, X. Li, and H. Yu. 1995. Heterodimerization and function interaction between EGF receptor family members: a new signaling paradigm with implications for breast cancer research. Breast Cancer Res. Treat. 35:115-132.
11. Fendly, B. M., M. Winget, R. M. Hudziak, M. T. Lipari, M. A. Napier, and A. Ullrich. 1990. Characterization of murine monoclonal antibodies reactive to either the human epidermal growth factor receptor or HER2/neu gene product. Cancer Res. 50:1550-1558.
12. French, A. R., and D. A. Lauffenburger. 1996. Intracellular receptor/ligand sorting based on endosomal retention components. Biotechnol. Bioeng. 51:281-297.
13. French, A. R., and D. A. Lauffenburger. 1997. Controlling receptor/ ligand trafficking: effects of cellular and molecular properties on endosomal sorting. Ann. Biomed. Eng. 25:690-707.
14. French, A. R., G. P. Sudlow, H. S. Wiley, and D. A. Lauffenburger. 1994. Postendocytic trafficking of epidermal growth factor-receptor complexes is mediated through saturable and specific endosomal interactions. J. Biol. Chem. 269:15749-15755.
15. French, A. R., D. K. Tadaki, S. K. Niyogi, and D. A. Lauffenburger. 1995. Intracellular trafficking of epidemial growth factor family ligands is directly influenced by the pH sensitivity of the receptor/ligand interaction. J. Biol. Chem. 270:4334-4340.
16. Glading, A., F. Uberall, S. M. Keyse, D. A. Lauffenburger, and A. Wells. 2001. Membrane proximal ERK signaling is required for M-calpain activation downstream of epidermal growth factor receptor signaling. J. Biol. Chem. 276:23341-23348.
17. 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. Eur. Mol. Biol. Org. J. 16:1647-1655.
18. Haugh, J. M., A. C. Huang, H. S. Wiley, A. Wells, and D. A. Lauffenburger. 1999a. Internalized epidermal growth factor receptors participate in the activation of p21ras in fibroblasts. J. Biol. Chem. 274:34350-34360.
19. Haugh, J. M., K. Schooler, A. Wells, H. S. Wiley, and D. A. Lauffenburger. 1999b. Effect of epidermal growth factor receptor internalization on regulation of the phospholipase C-γ1 signaling pathway. J. Biol. Chem. 274:8958-8965.
20. Hendriks, B. S., L. K. Opresko, H. S. Wiley, and D. A. Lauffenburger. 2003a. Co-regulation of EGFR/HER2 levels and locations: quantitative analysis of HER2 overexpression effects. Cancer Res. 63:1130-1137.
21. Hendriks, B. S., L. K. Opresko, H. S. Wiley, and D. A. Lauffenburger. 2003b. Quantitative analysis of HER2-mediated effects on HER2 and EGFR endocytosis: distribution of homo- and hetero-dimers depends on relative HER2 levels. J. Biol. Chem. 278:23343-23351.
22. Herbst, J. J., L. K. Opresko, B. J. Walsh, D. A. Lauffenburger, and H. S. Wiley. 1994. Regulation of postendocytic trafficking of the epidermal growth factor receptor through endosomal retention. J. Biol. Chem. 269:12865-12873.
23. Hynes, N. E., and D. F. Stern. 1994. The biology of erbB-2/neu/HER-2 and its role in cancer. Biochim. Biophys. Acta. 1198:165-184.
24. Ignatoski, K. M. W., A. J. Lapointe, E. H. Radany, and S. P. Ethier. 1999. ErbB-2 overexpression in human mammary epithelial cells confers growth factor independence. Endocrinology. 140:3615-3622.
25. 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. Eur. Mol. Biol. Org. ET J. 15:254-264.
26. Kil, S. J., and C. Carlin. 2000. EGF receptor residues Leu679, Leu680 mediate selective sorting of ligand-receptor complexes in early endosomal compartments. J. Cell. Physiol. 185:47-60.
27. Kil, S. J., M. Hobert, and C. Carlin. 1999. A leucine-based determinant in the epidermal growth factor receptor juxtamembrane domain is required for the efficient transport of ligand-receptor complexes to lysosomes. J. Biol. Chem. 274:3141-3150.
28. Komilova, E. S., T. Sorkina, L. Beguinot, and A. Sorkin. 1996. Lysosomal targeting of epidermal growth factor receptors via a kinase-dependent pathway is mediated by the receptor carboxyl-terminal residues 1022-1123. J. Biol. Chem. 271:30340-30346.
29. Kurten, R. C., D. L. Cadena, and G. N. Gill. 1996. Enhanced degradation of EGF receptors by a sorting nexin, SNX1. Science. 272:1008-1010.
30. Lauffenburger, D. A., and J. J. Linderman. 1993. Receptors. Oxford University Press, New York.
31. Lenferink, A. E. G., R. Pinkas-Kramarski, M. L. M. van der Poll, M. J. H. von Vugt, L. N. Klapper, E. Tzahar, H. Waterman, M. Sela, E. J. J. von Zoelen, and Y. Yarden. 1998. Differential endocytic routing of homo- and hetero-dimeric ErbB tyrosine kinases confers signaling superiority to receptor heterodimers. Eur. Mol. Biol. Org. J. 17:3385-3397.
32. 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.
33. Levkowitz, G., H. Waterman, S. A. Ettenberg, M. Katz, A. Y. Tsygankov, I. Alroy, S. Lavi, K. Iwai, Y. Reiss, A. Ciechanover, S. Lipkowitz, and Y. Yarden. 1999. Ubiquitin ligase activity and tyrosine phosphorylation underlie suppression of growth factor signaling by c-Cbl/Sli-1. Mol. Cell. 4:1029-1040.
34. 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.
35. Lewis, G. D., J. A. Lofgren, A. E. McMurtrey, A. Nuijens, B. M. Fendly, B. D. Bauer, and M. X. Sliwkowski. 1996. Growth regulation of human breast and ovarian tumor cells by heregulin: evidence of the requirement of ErbB2 as a critical component in mediating heregulin responsiveness. Cancer Res. 56:1457-1465.
36. Linderman, J. J., and D. A. Lauffenburger. 1986. Analysis of intracellular sorting: calculation of mean surface and bulk diffusion times within a sphere. Biophys. J. 50:295-305.
37. Lund, K. A., L. K. Opresko, C. Starbuck, B. J. Walsh, and H. S. Wiley. 1990. Quantitative analysis of the endocytic system involved in horm-one-induced receptor internalization. J. Biol. Chem. 265:15713-15723.
38. Muthuswamy, S., M. Gilman, and J. S. Brugge. 1999. Controlled dimerization of ErbB receptors provides evidence for differential signaling by homo- and heterodimers. Mol. Cell. Biol. 19:6845-6857.
39. 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.
40. Opresko, L., C. Chang, B. Will, P. M. Burke, G. N. Gill, and H. S. Wiley. 1995. Endocytosis and lysosomal targeting of epidermal growth factor receptors are mediated by distinct sequences independent of tyrosine kinase domain. J. Biol. Chem. 270:4325-4333.
41. Schechter, A. L., M.-C. Hung, L. Vaidyanathan, R. A. Weinberg, T. L. Yang-Feng, U. Francke, A. Ullrich, and L. Coussens. 1985. The neu gene: an ErbB-homologous gene distinct from and unlinked to the gene encoding the EGF receptor. Science. 229:976-978.
42. Shea, L. D., G. M. Omann, and J. J. Linderman. 1997. Calculation of diffusion-limited kinetics for the reactions in collision coupling and receptor cross-linking. Biophys. J. 73:2949-2959.
43. Sorkin, A., P. P. DiFiore, and G. Carpenter. 1993. The carboxyl terminus of epidermal growth factor receptor/ErbB-2 chimerae is internalization impaired. Oncogene. 8:3021-3028.
44. Sorkin, A., and C. M. Waters. 1993. Endocytosis of growth factor receptors. Bioessays. 15:375-382.
45. Spencer, K. S. R., D. Graus-Porta, J. Leng, N. Hynes, and R. L. Klemke. 2000. ErbB2 is necessary for induction of carcinoma cell invasion by ErbB family receptor tyrosine kinases. J. Cell Biol. 148:385-397.
46. Ullrich, A., L. Coussens, J. S. Hayflick, T. J. Dul, A. Gray, A. W. Tam, J. Lee, Y. Yarden, T. A. Libermann, J. Schlessinger, J. Downward, J. Bye, N. Whittle, M. Waterfield, and P. Seeburg. 1984. Human epidermal growth factor receptor cDNA sequence and aberrant expression of the amplified gene in A431 epidermoid carncinoma cells. Nature. 309:418-425.
47. Vieira, A. V., C. Lamaze, and S. L. Schmid. 1996. Control of EGF receptor signaling by clathrin-mediated endocytosis. Science. 274:2086-2089.
48. Wada, T., X. Qian, and M. I. Greene. 1990. Intermolecular association of the p185neu protein and EGF receptor modulates EGF receptor function. Cell. 61:1339-1347.
49. 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.
50. 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.
51. Wells, A., J. B. Welsh, C. S. Lazar, H. S. Wiley, G. N. Gill, and M. G. Rosenfeld. 1990. Ligand-induced transformation by a noninternalizing epidermal growth factor receptor. Science. 247:962-964.
52. 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.
53. Wiley, H. S., and P. M. Burke. 2001. Regulation of receptor tyrosine kinase signaling by endocytic trafficking. Traffic. 2:12-18.
54. Wiley, H. S., J. J. Herbst, B. J. Walsh, D. A. Lauffenburger, M. G. Rosenfeld, and G. N. Gill. 1991. The role of tyrosine kinase activity in endocytosis, compartmentation, and down-regulation of the epidermal growth factor receptor. J. Biol. Chem. 266:11083-11094.
55. Worthylake, R., L. K. Opresko, and H. S. Wiley. 1999. ErbB-2 amplification inhibits down-regulation and induces constitutive activation of both ErbB-2 and epidermal growth factor receptors. J. Biol. Chem. 274:8865-8874.
56. Worthylake, R., and H. S. Wiley. 1997. Structural aspects of the epidermal growth factor receptor required for transmodulation of ErbB-2/neu. J. Biol. Chem. 272:8594-8601.
57. Yarden, Y., and M. X. Sliwkowski. 2001. Untangling the ErbB signalling network. Nat. Rev. Mol. Cell Biol. 2:127-137.
58. Zhong, Q., C. S. Lazar, H. Tronchere, T. Sato, T. Meerloo, M. Yeo, Z. Songyang, S. D. Emr, and G. N. Gill. 2002. Endosomal localization and function of sorting nexin 1. Proc. Natl. Acad. Sci. USA. 99:6767-6772.