ErbB-2-induced mammary tumor growth: The role of cyclin D1 and p27Kip1

Biochemical Pharmacology

Volumn 64, Issue 5-6, 2002, Pages 827-836

  Hulit, James ^a   Lee, Richard J ^a   Russell, Robert G ^b   Pestell, Richard G ^a  

^a ALBERT EINSTEIN CANCER CENTER   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Breast cancer; Cyclin D1; Haplo insufficiency; p27; Transgenic mice

Indexed keywords

CELL CYCLE PROTEIN; CYCLIN D1; EPIDERMAL GROWTH FACTOR RECEPTOR; GROWTH FACTOR RECEPTOR; PROTEIN P27; PROTEIN TYROSINE KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST TUMOR; CARCINOGENESIS; CELL CYCLE; CONTROLLED STUDY; DISEASE COURSE; ERBB 2 GENE; GENE; GENE OVEREXPRESSION; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PATHOLOGY; PRIORITY JOURNAL; PROTO ONCOGENE; TRANSGENIC MOUSE; TUMOR GROWTH;

ANIMALS; CARCINOGENICITY TESTS; CELL CYCLE PROTEINS; CYCLIN D1; CYCLIN-DEPENDENT KINASE INHIBITOR P27; DISEASE MODELS, ANIMAL; FEMALE; GENES, TUMOR SUPPRESSOR; MAMMARY NEOPLASMS, ANIMAL; MICE; MICE, KNOCKOUT; RECEPTOR, ERBB-2; TUMOR SUPPRESSOR PROTEINS;

EID: 0036710683     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-2952(02)01145-0     Document Type: Article

References (93)

1. Slamon D.J., Clark G.M., Wong S.G., Levin W.J., Ullrich A., McGuire W.L. Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science. 235:1987;177-182.
2. Bargmann C.I., Weinberg R.A. Oncogenic activation of the neu-encoded receptor protein by point mutation and deletion. EMBO J. 7:1988;2043-2052.
3. Zhou B.P., Hu M.C., Miller S.A., Yu Z., Xia W., Lin S.Y., Hung M.C. HER-2/neu blocks tumor necrosis factor-induced apoptosis via the Akt/NF-kappaB pathway. J. Biol. Chem. 275:2000;8027-8031.
4. Webster M.A., Hutchinson J.N., Rauh M.J., Muthuswamy S.K., Anton M., Tortorice C.G., Cardiff R.D., Graham F.L., Hassell J.A., Muller W.J. Requirement for both Shc and phosphatidylinositol 3′ kinase signaling pathways in polyomavirus middle T-mediated mammary tumorigenesis. Mol. Cell Biol. 18:1998;2344-2359.
5. Hutchinson J., Jin J., Cardiff R.D., Woodgett J., Muller W.J. Activation of Akt (protein kinase B) in mammary epithelium provides a critical cell survival signal required or tumor progression. Mol. Cell Biol. 21:2001;2203-2212.
6. Biswas D.K., Cruz A.P., Gansberger E., Pardee A.B. Epidermal growth factor-induced nuclear factor kB activation: a major pathway of cell-cycle progression in estrogen-receptor negative breast cancer cells. Proc. Natl. Acad. Sci. U.S.A. 97:2000;8542-8547.
7. Hynes N.E., Lane H.A. Myc and mammary cancer: Myc is a downstream effector of the ErbB-2 receptor tyrosine kinase. J. Mammary Gland Biol. Neoplasia. 6:2001;141-150.
8. Lee R.J., Albanese C., Fu M., D'Amico M., Lin B., Watanabe G., Haines G.K.I., Siegel P.M., Hung M.C., Yarden Y., Horowitz J.M., Muller W.J., Pestell R.G. Cyclin D1 is required for transformation by activated Neu and is induced through an E2F-dependent signaling pathway. Mol. Cell Biol. 20:2000;672-683.
9. Dickson R.B., Lippman M.E. Growth factors in breast cancer. Endocr. Rev. 16:1995;559-589.
10. King C.R., Kraus M.H., Aaronson S.A. Amplification of a novel v-erbB related gene in human mammary carcinoma. Science. 229:1985;974-976.
11. Gullick W.J., Love S.B., Wright C., Barnes D.M., Gutterson B., Harris A.L., Altman D.G. c-erbB-2 protein over-expression in breast cancer is a risk factor in patients with involved and uninvolved lymph nodes. Br. J. Cancer. 63:1991;434-438.
12. Paterson M.C., Dietrich K.D., Danyluk J., Paterson A.H., Lees A.W., Jamil N., Hanson J., Jenkins B., Krause B.E., McBlain W.A., Slamon D.J., Fourney R.M. Correlation between c-erbB-2 amplification and risk of recurrent disease in node-negative breast cancer. Cancer Res. 51:1991;556-567.
13. Dankort D., Muller W. Signal transduction in mammary tumorigenesis: a transgenic perspective. Oncogene. 19:2000;1038-1044.
14. Bouzahzah B., Albanese C., Ahmed F., Pixley F., Lisanti M.P., Segall J.D., Condeelis J., Joyce D., Minden A., Der C.J., Chan A., Symons M., Pestell R.G. Rho family GTPases regulate mammary epithelium cell growth and metastasis through distinguishable pathways. Mol. Med. 7:2001;816-830.
15. Clark E.A., Golub T.R., Lander E.S., Hynes R.O. Genomic analysis of metastasis reveals an essential role for RhoC. Nature. 406:2000;532-535.
16. Downward J. Mechanisms and consequences of activation of protein kinase B/Akt. Curr. Opin. Cell Biol. 10:1998;262-267.
17. Neve R.M., Sutterluty H., Pullen N., Ha L., Daly J.M., Krek W., Hynes N.E. Effects of oncogenic ErbB-2 on G1 cell-cycle regulators in breast tumor cells. Oncogene. 19:2000;1647-1656.
18. Hunter T., Pines J. Cyclins and cancer II: cyclin D and CDK inhibitors come of age. Cell. 79:1994;573-582.
19. Weinberg R.A. The retinoblastoma protein and cell-cycle control. Cell. 81:1995;323-330.
20. Sherr C.J. Cancer cell-cycles. Science. 274:1996;1672-1677.
21. Pestell R.G., Albanese C., Reutens A.T., Segall J.E., Lee R.J., Arnold A. The cyclins and cyclin-dependent kinase inhibitors in hormonal regulation of proliferation and differentiation. Endocrine Rev. 20:1999;501-534.
22. Zafonte B.T., Hulit J., Amanatullah D.F., Albanese C., Wang C., Rosen E., Reutens A., Sparano J.A., Lisanti M.P., Pestell R.G. Cell-cycle dysregulation in breast cancer: breast cancer therapies targeting the cell-cycle. Front Biosci. 5:2000;D938-D961.
23. Kenny F.S., Hui R., Musgrove E.A., Gee J.M., Blamey R.W., Nicholson R.I., Sutherland R.L., Robertson J.F. Over-expression of cyclin D1 messenger RNA predicts for poor prognosis in estrogen receptor-positive breast cancer. Clin. Cancer Res. 5:1999;2069-2076.
24. Jiang W., Kahn S.M., Zhou P., Zhang Y.-J., Cacace A.M., Infante A.S., Doi S., Santella R.M., Weinstein I.B. Over-expression of cyclin D1 in rat fibroblasts causes abnormalities in growth control, cell-cycle progression and gene expression. Oncogene. 8:1993;3447-3457.
25. Quelle D.E., Ashmun R.A., Shurtleff S.A., Bar-Sagi D., Roussel M.F., Sherr C.J., Kato J.-Y. Over-expression of mouse D-type cyclins accelerates G1 phase in rodent fibroblasts. Genes Dev. 7:1993;1559-1571.
26. Resnitzky D., Gossen M., Bujard H., Reed S.I. Acceleration of the G1/S-phase transition by expression of cyclins D1 and E with an inducible system. Mol. Cell Biol. 14:1994;1669-1679.
27. Baldin V., Lukas J., Marcote M.J., Pagano M., Draetta G. Cyclin D1 is a nuclear protein required for cell-cycle progression in G1. Genes Dev. 7:1993;812-821.
28. Xiong W., Pestell R.G., Watanabe G., Li J., Rosner M.R., Hershenson M.B. Cyclin D1 is required for S-phase traversal in bovine tracheal myocytes. Am. J. Physiol. 272:1997;L1205-L1210.
29. Lukas J., Bartkova J., Bartek J. Convergence of mitogenic signalling cascades from diverse classes of receptors at the cyclin D-cyclin-dependent kinase-pRb-controlled G1 checkpoint. Mol. Cell Biol. 16:1996;6917-6925.
30. Guttridge D.C., Albanese C., Reuther J.Y., Pestell R.G., Baldwin A.S. NF-κB controls cell growth and differentiation through the transcriptional regulation of cyclin D1. Mol. Cell Biol. 19:1999;5785-5799.
31. Akama K.T., Albanese C., Pestell R.G., Van Eldik L.J. Amyloid β-peptide stimulates nitric oxide production in astrocytes through an NF-κB-dependent mechanism. Proc. Natl. Acad. Sci. U.S.A. 95:1998;5795-5800.
32. Shtutman M., Zhurinsky J., Simcha I., Albanese C., D'Amico M., Pestell R., Ben-Ze'ev A. The cyclin D1 gene is a target of the β-catenin/LEF-1 pathway. Proc. Natl. Acad. Sci. U.S.A. 96:1999;5522-5527.
33. ras mutants and c-Ets-2 activate the cyclin D1 promoter through distinguishable regions. J. Biol. Chem. 270:1995;23589-23597.
34. 2-terminal kinase, p38/Mpk2, serum response factor, or c-Jun. J. Biol. Chem. 273:1998;16739-16747.
35. Westwick J.K., Lambert Q.T., Clark G.J., Symons M., Van Aelst L., Pestell R.G., Der C.J. Rac regulation of transformation, gene expression and actin organisation by multiple, PAK-independent pathways. Mol. Cell Biol. 17:1997;1324-1335.
36. Joyce D., Bouzahzah B., Fu M., Albanese C., D'Amico M., Steer J., Klein J.U., Lee R.J., Segall J.E., Westwick J.K., Der C.J., Pestell R.G. Integration of Rac-dependent regulation of cyclin D1 transcription through an NF-κB-dependent pathway. J. Biol. Chem. 274:1999;25245-25249.
37. v-src signaling in breast cancer cells. J. Biol. Chem. 274:1999;7341-7350.
38. Watanabe G., Lee R.J., Albanese C., Rainey W.E., Batlle D., Pestell R.G. Angiotensin II (AII) activation of cyclin D1-dependent kinase activity. J. Biol. Chem. 271:1996;22570-22577.
39. Brown J.R., Nigh E., Lee R.J., Ye H., Thompson M.A., Saudou F., Pestell R.G., Greenberg M.E. Fos family members induce cell-cycle entry by activating cyclin D1. Mol. Cell Biol. 18:1998;5609-5619.
40. Watanabe G., Howe A., Lee R.J., Albanese C., Karnezis A.N., Zon L., Kyriakis J., Rundell K., Pestell R.G., Shu I.-W. Induction of cyclin D1 by simian virus 40 small tumor antigen. Proc. Natl. Acad. Sci. U.S.A. 93:1996;12861-12866.
41. Watanabe G., Albanese C., Lee R.J., Reutens A., Vairo G., Henglein B., Pestell R.G. Inhibition of cyclin D1 kinase activity is associated with E2F-mediated inhibition of cyclin D1 promoter activity through E2F and Sp1. Mol. Cell Biol. 18:1998;3212-3222.
42. Beier F., Lee R.J., Taylor A.C., Pestell R.G., LuValle P. Identification of the cyclin D1 gene as a target of ATF-2 in chondrocytes. Proc. Natl. Acad. Sci. U.S.A. 96:1999;1433-1438.
43. Albanese C., D'Amico M., Reutens A.T., Fu M., Watanabe G., Lee R.J., Kitsis R.N., Henglein B., Avantaggiati M., Somasundaram K., Thimmapaya B., Pestell R.G. Activation of the cyclin D1 gene by the E1A-associated protein p300 through AP-1 inhibits cellular apoptosis. J. Biol. Chem. 274:1999;34186-34195.
44. Reutens A.T., Fu M., Watanabe G., Albanese C., McPhaul M.J., Balk S.P., Janne O.A., Palvimo J.J., Pestell R.G. Cyclin D1 binds the androgen receptor and regulates hormone-dependent signaling in a p300/CBP-associated factor (P/CAF)-dependent manner. Mol. Endocrinol. 15:2001;797-811.
45. McMahon C., Suthiphongchai T., DiRenzo J., Ewen M.E. P/CAF associates with cyclin D1 and potentiates its activation of the estrogen receptor. Proc. Natl. Acad. Sci. U.S.A. 96:1999;5382-5387.
46. Ewen M.E., Sluss H.K., Sherr C.J., Matsushime H., Kato J.-Y., Livingston D.M. Functional interactions of the retinoblastoma protein with mammalian D-type cyclins. Cell. 73:1993;487-497.
47. Dowdy S.F., Hinds P.W., Louie K., Reed S.I., Arnold A., Weinberg R.A. Physical interaction of the retinoblastoma protein with human D cyclins. Cell. 73:1993;499-511.
48. Knudson K.E., Cavenee W.K., Arden K.C. D-type cyclins complex with the androgen receptor and inhibit its transcriptional transactivation ability. Cancer Res. 59:1999;2297-2301.
49. Wang C., Fu M., Mani S., Wadler S., Senderowicz A.M., Pestell R.G. Histone acetylation and the cell-cycle in cancer. Frontiers Biosci. 6:2001;D610-D629.
50. Neuman E., Ladha M.H., Lin N., Upton T.M., Miller S.J., DiRenzo J., Pestell R.G., Hinds P.W., Dowdy S.F., Brown M., Ewen M.E. Cyclin D1 stimulation of estrogen receptor transcriptional activity independent of cdk4. Mol. Cell Biol. 17:1997;5338-5347.
51. Zwijsen R.M.L., Wientjens E., Klompmaker R., van der Sman J., Bernards R., Michalides R.J.A.M. CDK-independent activation of estrogen receptor by cyclin D1. Cell. 88:1997;405-415.
52. Zwijsen R.M.L., Klompmaker R., Wientjens E.B.H.G.M., Kristel P.M.P., van der Burg B., Michalides R.J.A.M. Cyclin D1 triggers autonomous growth of breast cancer cells by governing cell-cycle exit. Mol. Cell Biol. 16:1996;2554-2560.
53. Zwijsen R.M.L., Buckle R.S., Hijmans E.M., Loomans C.J.M., Bernards R. Ligand-independent recruitment of steroid receptor coactivators to estrogen receptor by cyclin D1. Genes Dev. 12:1998;3488-3498.
54. Fan S., Wang J.-A., Yuan R., Ma Y., Meng Q., Erdos M.R., Pestell R.G., Yuan F., Auborn K.J., Goldberg I.D., Rosen E.M. BRCA inhibition of estrogen receptor signaling in transfected cells. Science. 284:1999;1354-1356.
55. Fan S., Yuan R., Ma Y.X., Erdos M., Zhao J.-N., Goldberg I.D., Pestell R.G., Rosen E.M. Disruption of BRCA1 LXCXE alters BRCA1 functional activity and regulation of RB family but not RB protein binding. Oncogene. 20:2001;4827-4841.
56. Fan S., Ma Y.X., Wang C., Yuan R.Q., Meng Q., Wang J.-A., Erdos M., Goldberg I.D., Webb P., Kushner P.J., Pestell R.G., Rosen E.M. p300 Modulates the BRCA1 Inhibition of estrogen receptor activity. Cancer Res. 62(1):2002;141-151.
57. Fan S., Ma Y.X., Wang C., Yuan R.Q., Meng Q., Wang J.-A., Erdos M., Goldberg I.D., Webb P., Kushner P.J., Pestell R.G., Rosen E.M. Role of direct interaction in BRCA1 inhibition of estrogen receptor activity. Oncogene. 20:2001;77-87.
58. Motokura T., Bloom T., Kim H.G., Jüppner H., Ruderman J.V., Kronenberg H.M., Arnold A. A novel cyclin encoded by a bcl1-linked candidate oncogene. Nature. 350:1991;512-515.
59. Motokura T., Arnold A. Cyclin D and oncogenesis. Curr. Opin. Genet. Dev. 3:1993;5-10.
60. Hinds P.W., Dowdy S.F., Eaton E.N., Arnold A., Weinberg R.A. Function of a human cyclin gene as an oncogene. Proc. Natl. Acad. Sci. U.S.A. 91:1994;709-713.
61. Hinds P.W., Mittnacht S., Dulic V., Arnold A., Reed S.I., Weinberg R.A. Regulation of retinoblastoma protein functions by ectopic expression of human cyclins. Cell. 70:1992;993-1006.
62. Liu J.-J., Chao J.-R., Jiang M.-C., Ng S.-Y., Yen J.J.-Y., Yang-Yen H.-F. Ras transformation results in an elevated level of cyclin D1 and acceleration of G1 progression in NIH3T3 cells. Mol. Cell Biol. 15:1995;3654-3663.
63. Robles A.I., Rodriguez-Puebla M.L., Glick A.B., Trempus C., Hansen L., Sicinski P., Tennant R.W., Weinbergh R.A., Yuspa S.H., Conti C.J. Reduced skin tumor development in cyclin D1-deficient mice highlights the oncogenic ras pathway in vivo. Genes Dev. 12:1998;2469-2474.
64. Wang T.C., Cardiff R.D., Zukerberg L., Lees E., Arnold A., Schmidt E.V. Mammary hyperplasia and carcinoma in MMTV-cyclin D1 transgenic mice. Nature. 369:1994;669-671.
65. Yu Q., Geng Y., Sicinski P. Specific protection against breast cancers by cyclin D1 ablation. Nature. 411:2001;1017-1021.
66. Bowe D.B., Kenney N.J., Adereth Y., Maroulakou I.G. Suppression of Neu-induced mammary tumor growth in cyclin D1 deficient mice is compensated for by cyclin E. Oncogene. 21:2002;291-298.
67. Fantl V., Stamp G., Andrews A., Rosewell I., Dickson C. Mice lacking cyclin D1 are small and show defects in eye and mammary gland development. Genes Dev. 9:1995;2364-2372.
68. Sicinski P., Donaher J.L., Parker S.B., Li T., Fazeli A., Gardner H., Haslam S.Z., Bronson R.T., Elledge S.J., Weinberg R.A. Cyclin D1 provides a link between development and oncogenesis in the retina and breast. Cell. 82:1995;621-630.
69. -/- mice during pregnancy and lactation is epithelial cell autonomous. Development. 212:1999;1-11.
70. Tong W., Pollard J.W. Genetic evidence for the interactions of cyclin D1 and p27(Kip1) in mice. Mol. Cell Biol. 4:2001;1319-1328.
71. Geng Y., Yu Q., Sicinska E., Das M., Bronson R.T., Sicinski P. Deletion of the p27Kip1 gene restores normal development in cyclin D1-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 98:2000;194-199.
72. Toyoshima H., Hunter T. p27, a novel inhibitor of G1 cyclin-Cdk protein kinase activity, is related to p21. Cell. 78:1994;67-74.
73. Kip1. J. Biol. Chem. 274:1999;20805-20811.
74. Kip1 CDK 'inhibitors' are essential activators of cyclin D-dependent kinases in murine fibroblasts. EMBO J. 18:1999;1571-1583.
75. Kip1 protein: prognostic implications in primary breast cancer. Nat. Med. 3:1997;227-230.
76. Sgambato A., Arber N., Hibshoosh H., Doki Y., Ciaparrone M., Santella R.M., Weinstein I.B., Zhang Y.-J. Deregulated expression of p27Kip1 in human breast cancers. Clin. Cancer Res. 3:1997;1879-1887.
77. Fredersdorf S., Burns J., Milne A.M., Packham G., Fallis L., Gillett C.E., Royds J.A., Peston D., Hall P.A., Hanby A.M., Barnes D.M., Shousha S., O'Hare M.J., Lu X. High level expression of p27kip1 and cyclin D1 in some human breast cancer cells: inverse correlation between the expression of p27kip1 and degree of malignancy in human breast and colorectal cancers. Proc. Natl. Acad. Sci. U.S.A. 94:1997;6380-6385.
78. Porter P.L., Malone K.E., Heagerty P.J., Alexander G.M., Gatti L.A., Firpo E.J., Daling J.R., Roberts J.M. Expression of cell-cycle regulators p27Kip1 and cyclin E, alone and in combination, correlate with survival in young breast cancer patients. Nat. Med. 3:1997;222-225.
79. Sutterluty H., Chatelain E., Marti A., Wirbelauer C., Senften M., Muller U., Krek W. p45SKP2 promotes p27Kip1 degradation and induces S-phase in quiescent cells. Nat. Cell Biol. 1:1999;207-214.
80. Rolfe M., Chiu M.I., Pagano M. The ubiquitin-mediated proteolytic pathway as a therapeutic area. J. Mol. Med. 75:1997;5-17.
81. Carrano A., Eytan E., Hershko A., Pagano M. SKP2 is required for ubiquitin-mediated degradation of the Cdk inhibitor p27. Nat. Cell Biol. 1:1999;193-199.
82. Zhang H., Kobayashi R., Galaktionov K., Beach D. p19Skp1 and p45Skp2 are essential elements of the cyclin A-CDK2 S-phase kinase. Cell. 82:1995;915-925.
83. Nakayama K., Nagahama H., Minamishima Y.A., Matsumoto M., Nakamichi I., Kitagawa K., Shirane M., Tsunematsu R., Tsukiyama T., Ishida N., Kitagawa M., Nakayama K., Hatakeyama S. Targeted disruption of Skp2 results in accumulation of cyclin E and p27(Kip1), polyploidy and centrosome overduplication. EMBO J. 19:2000;2069-2081.
84. Chiarle R., Pagano M., Inghirami G. The cyclin-dependent kinase inhibitor p27 and its prognostic role in breast cancer. Breast Cancer Res. 3(2):2001;91-194.
85. Kip1 is haplo-insufficient for tumour suppression. Nature. 396:1998;177-180.
86. Hulit J, Lee RJ, Zhou JN, Wang C, Di Vizio D, Wu K, Albanese C, Russell R, Koff A, Muller WJ, Inghirami G, RGP. Mechanisms of p27 haplo-insufficent breast tumor suppression in transgenic mice. Cell signaling. Transcription and Translation as Therapeutic Targets (Luxembourg). 2002 Oral Session 5B.
87. Kip1. Cell. 85:1996;721-732.
88. Kip1-deficient mice. Cell. 85:1996;733-744.
89. Kip1 display increased body size, multiple organ hyperplasia, retinal dysplasia, and pituitary tumors. Cell. 85:1996;707-720.
90. Slingerland J., Pagano M. Regulation of the cdk inhibitor p27 and its deregulation in cancer. J. Cell Physiol. 183:2000;10-17.
91. Weinstein I.B. Disorders in cell circuitry during multistage carcinogenesis the role of homeostasis. Carcinogenesis. 21:2000;857-864.
92. Di Cristofano A., De Acetis M., Koff A., Cordon-Cardo C., Pandolfi P.P. Pten and p27Kip1 cooperate in prostate cancer tumor suppression in the mouse. Nat. Genet. 27:2001;222-224.
93. Malek N.P., Sundberg H., McGrew S., Nakayama K., Kyriakidisk T.R., Roberts J.M. A mouse knock-in model exposes sequential proteolytic pathways that regulate p27Kip1 in G1 and S-phase. Nature. 413:2001;323-326.