ErbB2 potentiates breast tumor proliferation through modulation of p27(Kip1)-Cdk2 complex formation: Receptor overexpression does not determine growth dependency

Molecular and Cellular Biology

Volumn 20, Issue 9, 2000, Pages 3210-3223

  Lane, Heidi A ^a   Beuvink, Iwan ^a   Motoyama, Andrea B ^a   Daly, John M ^a   Neve, Richard M ^a   Hynes, Nancy E ^a  

^a FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN D; MYC PROTEIN; PROTEIN P27; TYROSINE KINASE RECEPTOR;

ARTICLE; BREAST TUMOR; CANCER INHIBITION; CELL CYCLE G1 PHASE; COMPLEX FORMATION; CONTROLLED STUDY; DEPHOSPHORYLATION; DOWN REGULATION; GENE ACTIVITY; GENE CONTROL; GENE INACTIVATION; GENE LOSS; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; MITOSIS INHIBITION; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TUMOR GROWTH;

ANTIBODIES, MONOCLONAL; BREAST NEOPLASMS; CDC2-CDC28 KINASES; CELL CYCLE; CELL CYCLE PROTEINS; CELL DIVISION; CYCLIN-DEPENDENT KINASE 2; CYCLIN-DEPENDENT KINASE INHIBITOR P27; CYCLIN-DEPENDENT KINASES; CYTOPLASM; FLOW CYTOMETRY; G1 PHASE; HUMANS; MICROTUBULE-ASSOCIATED PROTEINS; PHOSPHORYLATION; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; RECEPTOR, ERBB-2; SIGNAL TRANSDUCTION; STOMACH NEOPLASMS; TIME FACTORS; TUMOR CELLS, CULTURED; TUMOR SUPPRESSOR PROTEINS;

EID: 0033996361     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.20.9.3210-3223.2000     Document Type: Article

References (86)

1. 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.
2. Amati, B., K. Alevizopoulos, and J. Vlach. 1998. Myc and the cell cycle. Frontiers Biosci. 3:250-268.
3. Baselga, J., D. Tripathy, J. Mendelsohn, S. Baughman, C. C. Benz, L. Dantis, N. T. Sklarin, A. D. Seidman, C. A. Hudis, J. Moore, P. P. Rosen, T. Twaddell, I. C. Henderson, and L. Norton. 1996. Phase II study of weekly intravenous recombinant humanized anti-p185HER2 monoclonal antibody in patients wilh HER2/neu-overexpressing metastatic breast cancer. J. Clin. Oncol. 14:737-744.
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. 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.
6. Berger, M. S., G. W. Locher, S. Saurer, W. J. Gullick, M. D. Waterfleld, B. Groner, and N. E. Hynes. 1988. Correlation of c-erbB-2 gene amplification and protein expression in human breast cancer with nodal status and nuclear grading. Cancer Res. 48:1238-1243.
7. Berns, K., E. M. Hijmans, and R. Bernards. 1997. Repression of c-Myc responsive genes in cycling cells causes G1 arrest through reduction of cyclin E/CDK2 kinase activity. Oncogene 15:1347-1356.
8. Kip1 with cyclin A-Cdk2 and cyclin D2-Cdk4. J. Biol. Chem. 272:25863-25872.
9. Bodey, B., B. Bodey, Jr., A. M. Groger, J. V. Luck, S. E. Siegel, C. R. Taylor, and H. E. Kaiser. 1997. Clinical and prognostic significance of the expression of the c-erbB-2 and c-erbB-3 oncoproteins in primary and metastatic malignant melanomas and breast carcinomas. Anticancer Res. 17:1319-1330.
10. Bouchard, C., K. Thieke, A. Maier, R. Safrich, J. Hanley-Hyde, W. Ansorge, S. Reed, P. Sicinski, J. Bartek, and M. Eilers. 1999. Direct induction of cyclin D2 by Myc contributes to cell cycle progression and sequestration of p27. EMBO J. 18:5321-5333.
11. 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.
12. Kip1 protein: prognostic implications in primary breast cancer. Nat. Med. 3:227-230.
13. Kip1 CDK 'inhibitors' are essential activators of cyclin D-dependent kinases in murine fihrohlasts. EMBO J. 18:1571-1583.
14. Kip1 for restriction point control of the fibroblast cell cycle. Science 272:877-880.
15. Cobleigh, M. A., C. L. Vogel, D. Tripathy, N. J. Robert, S. Scholl, L. Fehrenbacher, J. Wolter, V. Paton, S. Shak, G. Lieberman, and D. J. Slamon. 1999. Multinational study of the efficacy and safety of humanized anti-HER2 monoclonal antibody in women who have HER2-overexpressing metastatic breast cancer that has progressed after chemotherapy for metastatic disease. J. Clin. Oncol. 17:2639-2648.
16. Daly, R. J. 1999. Take your partners, please - signal diversification by the erbB family of receptor tyrosine kinases. Growth Factors 16:255-263.
17. Diehl, J. A., M. Cheng, M. F. Roussel, and C. J. Sherr. 1998. Glycogen synthase kinase-3β regulates cyclin D1 proteolysis and subcellular localization. Genes Dev. 12:3499-3511.
18. Elledge, S. J., J. Winston, and J. W. Harper. 1996. A question of balance: the role of cyclin-kinase inhibitors in development and tumorigenesis. Trends Cell Biol. 6:388-397.
19. Esposito, V., A. Baldi, A. De Loca, A. M. Groger, M. Loda, G. G. Giordano, M. Caputi, F. Baldi, M. Pagano, and A. Giordano. 1997. Prognostic role of the cyclin-dependent kinase inhibitor p27 in non-small cell lung cancer. Cancer Res. 57:3381-3385.
20. Fedi, P., J. H. Pierce, P. P. DiFiore, 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 the Erb/EGFR family members. Mol. Cell. Biol. 14:492-500.
21. Fuknshige, S.-I,. K.-I. Matsubara, M. Yoshida, M. Sasaki, T. Suzuki, K. Semba, K. Toyoshima, and T. Yamamoto. 1986. Localization of a novel v-erbB-related gene, c-erbB-2, on human chromosome 17 and its amplification in a gastric cancer cell line. Mol. Cell. Biol. 6:955-958.
22. 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.
23. 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.
24. Gullick, W. J., S. B. Love, C. Wright, D. M. Barnes, B. Gusterson, A. L. Harris, and D. G. Altman. 1991. c-erbB-2 protein overexpression in breast cancer is a risk factor in patients with involved and uninvolved lymph nodes. Br. J. Cancer 63:434-438.
25. Harwerth, I.-M, W. Wels, B. Marte, and N. E. Hynes. 1992 Monoclonal antibodies against the extracellular domain of the erbB-2 receptor function as partial ligand agonists. J. Biol. Chem. 267:15160-15167.
26. Harwerth, I.-M., W. Wels, J. Schlegel, M. Müller, and N. E. Hynes. 1993. Monoclonal antibodies directed to the erbB-2 receptor inhibit in vivo tumour cell growth. Br. J. Cancer 68:1140-1145.
27. HER2 monoclonal antibody has antiproliferative effects in vitro and sensitizes human breast tumor cells to tumor necrosis factor. Mol. Cell. Biol. 9:1165-1172.
28. Hunter, T., and J. Pines. 1994. Cyclins and cancer. II. Cyclin D and CDK inhibitors come of age. Cell 79:573-582.
29. Jannot, Ch., R. R. Beerli, S. Mason, W. J. Gullick, and N. E. Hynes. 1996. Intracellular expression of a single-chain antibody directed to the epidermal growth factor receptor leads to growth inhibition of tumor cells. Oncogene 13:275-282.
30. Kamnagaran, 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.
31. Keyomarsi, K., and A. B. Pardee. 1993. Redundant cyclin overexpression and gene amplification in breast cancer cells. Proc. Natl. Acad. Sci. USA 90: 1112-1116.
32. Keyomarsi, K., D. Conte, Jr., W. Toyofuku, and M. P. Fox. 1995. Deregulation of cyclin E in breast cancer. Oncogene 11:941-950.
33. Kumar, R., H. M. Shepard, and J. Mendelsohn. 1991. Regulation of phosphorylation of the c-erbB-2/HER2 gene product by a monoclonal antibody and serum growth factor(s) in human mammary carcinoma cells. Mol. Cell. Biol. 11:979-986.
34. LaBaer, J., M. D. Garrett, L. F. Stevenson, J. M. Slingerland, C. Sandhu, H. S. Chou, A. Fattaey, and E. Harlow. 1997. New functional activities for the p21 family of CDK inhibitors. Genes Dev. 11:847-862.
35. Lane, H. A., and E. A. Nigg. 1996. Antibody microinjection reveals an essential role for human polo-like kinase 1 (Plk1) in the functional maturation of mitotic centrosomes. J. Cell Biol. 135:1701-1713.
36. Leone, G., J. DeGregori, R. Sears, L. Jakoi, and J. R. Kevins. 1997. Myc and Ras collaborate in inducing accumulation of active cyclin E/Cdk2 and E2F. Nature 387:422-426.
37. HER2 monoclonal antibodies. Cancer Immunol. Immunother. 37: 255-263.
38. Lewis, G. D., J. A. Lofgren, A. E. McMurtrey, A. Huijens, B. M. Fendly, K. D. Bauer, and M. X. Sliwkowski. 1996. Growth regulation of human breast and ovarian tumor cells by heregulin: evidence for the requirement of ErbB2 as a critical component in mediating heregulin responsiveness. Cancer Res. 56:1457-1465.
39. Loda, M., B. Cukor, S. W. Tam, P. Lavin, M. Florentino, G. F. Draetta, J. Milburn Jessup, and M. Pagano. 1997. Increased proteosome-dependent degradation of the cyclin-dependent kinase inhibitor p27 in aggressive colorectal carcinomas. Nat. Med. 3:231-234.
40. Lodén, M., N. H. Nielsen, G. Roos, S. O. Emdin, and G. Landberg. 1999. Cyclin E dependent kinase activity in human breast cancer in relation to cyclin E, p27 and p21 expression and retinoblastoma protein phosphorylation. Oncogene 18:2557-2566.
41. Marte, B. M., D. Graus-Porta, M. Jeschke, D. Fabbro, N. E. Hynes, and D. Taverna. 1995. NDF/heregulin activates MAP kinase and p70/p85 S6 kinase during proliferation or differentiation of mammary epithelial cells. Oncogene 10:167-175.
42. 1 kinase activity for cdk6, a novel cyclin D partner. Mol. Cell. Biol. 14:2077-2086.
43. Montagnoli, A., F. Fiore, E. Eytan, A. C. Carrano, G. F. Draetta, A. Hershko, and M. Pagano. 1999. Ubiquitination of p27 is regulated by Cdk-dependent phosphorylation and trimeric complex formation. Genes Dev. 13:1181-1189.
44. Müller, D., C. Bouchard, B. Rudolph, P. Steiner, I. Stuckmann, R. Saffrich, R. Ansorge, W. Huttner, and M. Eilers. 1997. Cdk2-dependent phosphorylation of p27 facilitates its Myc-induced release from cyclin E/Cdk2 complexes. Oncogene 15:2561-2576.
45. Nielsen, N. H., C. Arnerlov, S. O. Emdin, and G. Landberg. 1996. Cyclin E overexpression, a negative prognostic factor in breast cancer with strong correlation to oestrogen receptor status. Br. J. Cancer 74:874-880.
46. Nielsen, N. H., M. Lodén, J. Cajander, S. O. Emdin, and G. Landberg. 1999. G1-S transition defects occur in most breast cancers and predict outcome. Breast Cancer Res. Treat. 56:105-112.
47. Nigg, E. A. 1995. Cyclin-dependent protein kinases: key regulators of the eukaryotic cell cycle. Bioessays 17:471-480.
48. Obaya, A. J., M. K. Mateyak, and J. M. Sedivy. 1999. Mysterious liaisons: the relationship between c-Myc and the cell cycle. Oncogene 18:2934-2941.
49. 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 depending upon their dimerization partner. Mol. Cell. Biol. 18:5042-5051.
50. Kip1 in anchorage-independent cells. Oncogene 16:2575-2583.
51. Pagano, M., S. W. Tam, A. M. Theodoras, P. Beer-Romero, G. Del Sal, V. Chau, P. R. Yew, G. F. Draetta, and M. Rolfe. 1995. Role of the ubiquitin-proteosome pathway in regulating abundance of the cyclin-dependent kinase inhibitor p27. Science 269:682-685.
52. Pegram, M. D., A. Lipton, D. F. Hayes, B. L. Weber, J. M. Baselga, D. Tripathy, D. Baly, S. A. Baughman, T. Twaddell, J. A. Glaspy, and D. J. Slamon. 1998. Phase II study of receptor-enhanced chemosensitivity using recombinant humanized anti-p185HER2/neu monoclonal antibody plus cisplatin in patients with HER2/neu-overexpressing metastatic breast cancer refractory to chemotherapy treatment. J. Clin. Oncol. 16:2659-2671.
53. Kip1 and induces G1 arrest in prostatic cancer cell line DU145. Cancer Res. 56:3666-3669.
54. Perez-Roger, I., S.-H. Kim, B. Griffiths, A. Sewing, and H. Land. 1999. Cyclins D1 and D2 mediate Myc-induced proliferation via sequestration of p27Kip1 and p21Cip1. EMBO J. 18:5310-5320.
55. Pinkas-Kramarski, R., L. Soussan, H. Waterman, G. Levkowitz, I. Alroy, L. Klapper, S. Lavi, R. Seger, B. J. Ralzkin, 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. Kip1, a cyclin-dependent kinase inhibitor and a potential mediator of extracellular antimitogenic signals. Cell 78:59-66.
57. Poon, R. Y., H. Toyoshima, and T. Hunter. 1995. Redistribution of the CDK inhibitor p27 between different cyclin/CDK complexes in the mouse fibroblast cell cycle and in cells arrested with lovastatin or ultraviolet light. Mol. Biol. Cell 6:1197-1213.
58. Porter, P. L., K. E. Malone, P. J. Heagerty, G. M. Alexander, L. A. Gatti, E. J. Firpo, J. R. Dating, and J. M. Roberts. 1997. Expression of cell-cycle regulators p27Kip1 and cyclin E, alone and in combination, correlate with survival in young breast cancer patients. Nat. Med. 3:222-225.
59. Press, M. F., M. C. Pike, V. R. Chazin, G. Hung, J. A. Udove, M. Markowicz, J. Danyluk, W. Godolphin, M. Sliwkowski, R. Akita, M. C. Paterson, and D. J. Slamon. 1993. Her-2/neu expression in node-negative breast cancer: direct tissue quantitation by computerized image analysis and association of overexpression with increased risk of recurrent disease. Cancer Res. 53: 4960-4970.
60. Prigent, S. A., and W. J. Gullick. 1994. Identification of c-erbB-3 binding sites for phosphatidyl 3′kinase and SHC using an EGF receptor/c-erbB-3 chimera. EMBO J. 13:2831-2841.
61. Pusch, O., G. Barnaschek, M. Eilers, and M. Hengstschlager. 1997. Activation of c-Myc uncouples DNA replication from activation of G1-cyclin-dependent kinases. Oncogene 15:649-656.
62. Riese, D. J., II, and D. F. Stern. 1998. Specificity within the EGF family/ErbB receptor family signaling network. Bioessays 20:41-48.
63. HER2 signal transduction in breast tumour cells. J. Biol. Chem. 266:14300-14305.
64. Scott, G. K., R. Robles, J. W. Park, P. A. Montgomery, J. Daniel, W. E. Hohnes, J. Lee, G. A. Keller, W.-L. Li, B. M. Fendly, W. I. Wood, H. M. Shepard, and C. C. Benz. 1993. A truncated intracellular HER2/neu receptor produced by alternative RNA processing affects growth of human carcinoma cells. Mol. Cell. Biol. 13:2247-2257.
65. Sears, R., G. Lone, J. DeGregori, and J. R. Nevins. 1999. Ras enhances Myc protein stability. Mol. Cell 3:169-179.
66. Kip1. Genes Dev. 11:1464-1478.
67. Sherr, C. J., and J. M. Roberts. 1995. Inhibitors of mammalian G1 cyclin-dependent kinases. Genes Dev. 9:1149-1163.
68. Sherr, C. J., and J. M. Roberts. 1999. CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev. 13:1501-1512.
69. Siegel, P. M., E. D. Ryan, R. D. Cardiff, and W. J. Muller. 1999. Elevated expression of activated forms of Neu/ErbB-2 and ErbB-3 are involved in the induction of mammary tumors in transgenic mice: implications for human breast cancer. EMBO J. 18:2149-2164.
70. Slamon, D. J., G. M. Clark, S. G. Wong, W. J. Levin, A. Ullrioh, and W. L. McGuire. 1987. Human breast cancer: correlation of relapse and survival with the amplification of the HER-2/neu oncogene. Science 235:177-182.
71. Slamon, D. J., W. Godolphin, L. A. Jones, J. A. Holt, S. G. Wong, D. E. Keith, W. J. Levin, S. G. Stuart, J. Udove, A. Ullrich, and M. F. Press. 1989. Studies of the HER-2/neu proto-oncogene in human breast and ovarian cancer. Science 244:707-712.
72. Slingerland, J. M., L. Hengst, C. H. Pan, D. Alexander, M. R. Stampfer, and S. I. Reed. 1994. A novel inhibitor of cyclin-Cdk activity detected in transforming growth factor β-arrested epithelial cells. Mol. Cell. Biol. 14:3683-3694.
73. Soos, T. J., H. Kiyokawa, J. S. Yan, M. S. Rubin, A. Giordano, A. DeBlasio, S. Bottega, B. Wong, J. Mendelsohn, and A. Koff. 1996. Formation of p27-CDK complexes during the human mitotic cell cycle. Cell Growth Differ. 7:135-146.
74. 1 cyclin-cdk complexes. EMBO J. 14:4814-4826.
75. Taya, Y. 1997. RB kinases and RB-binding proteins: new points of view. Trends Biochem. Sci. 22:14-17.
76. Toyoshima, H., and T. Hunter. 1994. p27, a novel inhibitor of G1 cyclin/cdk protein kinase activity, is related to p21. Cell 78:67-74.
77. Kip1 is abrogated by c-Myc. EMBO J. 15:6595-6604.
78. Wallasch, C., F. U. Weisse, 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.
79. Weiss, F. U., C. Wallasch, M. Campiglio, W. Issing, and A. Ullrich. 1997. Distinct characteristics of heregulin signals mediated by HER3 or HER4. J. Cell. Physiol. 173:187-195.
80. West, M. J., M. Stoneley, and A. E. Willis. 1998. Translational induction of the c-myc oncogene via activation of the FRAP/TOR signalling pathway. Oncogene 17:769-780.
81. 1 arrest mediated by an anti-epidermal growth factor receptor monoclonal antibody. Oncogene 12:1397-1403.
82. Kip1 is associated with advanced stage and invasiveness of gastric carcinomas. Jpn. J. Cancer Res. 88:625-629.
83. Ye, D., J. Mendelsohn, and Z. Fan. 1999. Augmentation of a humanized Anti-HER2 mAb 4D5 induced growth inhibition by a human-mouse chimeric anti-EGF receptor mAb C225. Oncogene 18:731-738.
84. Yonemura, Y., I. Ninomiya, A. Yamaguchi, S. Fushida, H. Kimura, S. Ohoyama, I. Miyazaki, Y. Endou, M. Tanaka, and T. Sasaki. 1991. Evaluation of immunoreactivity for erbB-2 protein as a marker of poor short-term prognosis in gastric cancer. Cancer Res. 51:1034-1038.
85. Zhang, H., G. J. Hannon, and D. Beach. 1994. p21-containing cyclin-kinases exist in both active and inactive states. Genes Dev. 8:1750-1758.
86. Zhang, K., J. Sun, N. Liu, D. Wen, D. Chang, A. Thomason, and S. K. Yasinaga. 1996. Transformation of NIH 3T3 cells by HER3 or HER4 receptors requires the presence of HER1 or HER2. J. Biol. Chem. 271:3884-3890.