Retinoids arrest breast cancer cell proliferation: Retinoic acid selectively reduces the duration of receptor tyrosine kinase signaling

Experimental Cell Research

Volumn 301, Issue 2, 2004, Pages 147-157

  Tighe, Ann P ^a   Talmage, David A ^a  

^a N ^*  (United States)

Author keywords

HBC cells; PKC ; Retinoic acid

Indexed keywords

4 [(5,6,7,8 TETRAHYDRO 5,5,8,8 TETRAMETHYL 2 NAPHTHYL)CARBOXAMIDO]BENZOIC ACID; ADAPTOR PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE 1; ORTHOVANADIC ACID; PHOSPHOTYROSINE; PROTEIN KINASE C ALPHA; PROTEIN SHC; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE PHOSPHATASE; RETINOIC ACID;

ARTICLE; BREAST CANCER; CANCER CELL; CELL CYCLE; CELL PROLIFERATION; CONTROLLED STUDY; CYTOPLASM; DRUG EFFECT; GENE TARGETING; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; SIGNAL TRANSDUCTION; STEADY STATE;

EID: 8644288398     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2004.07.008     Document Type: Article

References (88)

1. Y. Cho, A.P. Tighe, and D.A. Talmage Retinoic acid induced growth arrest of human breast carcinoma cells requires protein kinase C alpha expression and activity J. Cell. Physiol. 172 1997 306 313
2. R. Lotan Retinoids in cancer chemoprevention FASEB J. 10 1996 1031 1039
3. Y. Cho, and D.A. Talmage Protein kinase C-alpha expression confers retinoic acid sensitivity on MDA-MB-231 human breast cancer cells Exp. Cell Res. 269 2001 97 108
4. R. Dow, J. Hendley, A. Pirkmaier, E.A. Musgrove, and D. Germain Retinoic acid-mediated growth arrest requires ubiquitylation and degradation of the F-box protein Skp2 J. Biol. Chem. 276 2001 45945 45951
5. P. Fitzgerald, M. Teng, R.A. Chandraratna, R.A. Heyman, and E.A. Allegretto Retinoic acid receptor alpha expression correlates with retinoid-induced growth inhibition of human breast cancer cells regardless of estrogen receptor status Cancer Res. 57 1997 2642 2650
6. K. Okamoto, F. Andreola, M.V. Chiantore, R.L. Dedrick, and L.M. De Luca Differences in uptake and metabolism of retinoic acid between estrogen receptor-positive and -negative human breast cancer cells Cancer Chemother. Pharmacol. 46 2000 128 134
7. M.S. Sheikh, Z.M. Shao, J.C. Chen, A. Hussain, A.M. Jetten, and J.A. Fontana Estrogen receptor-negative breast cancer cells transfected with the estrogen receptor exhibit increased RAR alpha gene expression and sensitivity to growth inhibition by retinoic acid J. Cell. Biochem. 53 1993 394 404
8. M.S. Sheikh, Z.M. Shao, X.S. Li, M. Dawson, A.M. Jetten, S. Wu, B.A. Conley, M. Garcia, H. Rochefort, and J.A. Fontana Retinoid-resistant estrogen receptor-negative human breast carcinoma cells transfected with retinoic acid receptor-alpha acquire sensitivity to growth inhibition by retinoids J. Biol. Chem. 269 1994 21440 21447
9. B. van der Burg, R. Slager-Davidov, B.M. van der Leede, S.W. de Laat, and P.T. van der Saag Differential regulation of AP1 activity by retinoic acid in hormone-dependent and -independent breast cancer cells Mol. Cell. Endocrinol. 112 1995 143 152
10. B. van der Burg, B.M. van der Leede, L. Kwakkenbos-Isbrucker, S. Salverda, S.W. de Laat, and P.T. van der Saag Retinoic acid resistance of estradiol-independent breast cancer cells coincides with diminished retinoic acid receptor function Mol. Cell. Endocrinol. 91 1993 149 157
11. S.M. Schneider, M. Offterdinger, H. Huber, and T.W. Grunt Activation of retinoic acid receptor alpha is sufficient for full induction of retinoid responses in SK-BR-3 and T47D human breast cancer cells [In Process Citation] Cancer Res. 60 2000 5479 5487
12. P. Chambon A decade of molecular biology of retinoic acid receptors FASEB J. 10 1996 940 954
13. Y. Kamei, L. Xu, T. Heinzel, J. Torchia, R. Kurokawa, B. Gloss, S.C. Lin, R.A. Heyman, D.W. Rose, C.K. Glass, and M.G. Rosenfeld A CBP integrator complex mediates transcriptional activation and AP-1 inhibition by nuclear receptors Cell 85 1996 403 414
14. M. Pfahl Nuclear receptor/AP-1 interaction Endocr. Rev. 14 1993 651 658
15. D.A. Talmage, and M. Listerud Retinoic acid suppresses polyoma virus transformation by inhibiting transcription of the c-fos proto-oncogene Oncogene 9 1994 3557 3563
16. A. Fanjul, M.I. Dawson, P.D. Hobbs, L. Jong, J.F. Cameron, E. Harlev, G. Graupner, X.P. Lu, and M. Pfahl A new class of retinoids with selective inhibition of AP-1 inhibits proliferation Nature 372 1994 107 111
17. C. Huang, W.Y. Ma, M.I. Dawson, M. Rincon, R.A. Flavell, and Z. Dong Blocking activator protein-1 activity, but not activating retinoic acid response element, is required for the antitumor promotion effect of retinoic acid Proc. Natl. Acad. Sci. U. S. A. 94 1997 5826 5830
18. H.F. Yang-Yen, X.K. Zhang, G. Graupner, M. Tzukerman, B. Sakamoto, M. Karin, and M. Pfahl Antagonism between retinoic acid receptors and AP-1: implications for tumor promotion and inflammation New Biol. 3 1991 1206 1219
19. X.F. Zhou, X.Q. Shen, and L. Shemshedini Ligand-activated retinoic acid receptor inhibits AP-1 transactivation by disrupting c-Jun/c-Fos dimerization Mol. Endocrinol. 13 1999 276 285
20. Y. Chen, R. Freund, M. Listerud, Z. Wang, and D.A. Talmage Retinoic acid inhibits transformation by preventing phosphatidylinositol 3-kinase dependent activation of the c-fos promoter Oncogene 18 1999 139 148
21. C. Caelles, J.M. Gonzalez-Sancho, and A. Munoz Nuclear hormone receptor antagonism with AP-1 by inhibition of the JNK pathway Genes Dev. 11 1997 3351 3364
22. G.J. Fisher, H.S. Talwar, J. Lin, P. Lin, F. McPhillips, Z. Wang, X. Li, Y. Wan, S. Kang, and J.J. Voorhees Retinoic acid inhibits induction of c-Jun protein by ultraviolet radiation that occurs subsequent to activation of mitogen-activated protein kinase pathways in human skin in vivo J. Clin. Invest. 101 1998 1432 1440
23. H.Y. Lee, N. Sueoka, W.K. Hong, D.J. Mangelsdorf, F.X. Claret, and J.M. Kurie All-trans-retinoic acid inhibits Jun N-terminal kinase by increasing dual-specificity phosphatase activity Mol. Cell. Biol. 19 1999 1973 1980
24. D.J. Riese II, and D.F. Stern Specificity within the EGF family/ErbB receptor family signaling network Bioessays 20 1998 41 48
25. P. van der Geer, T. Hunter, and R.A. Lindberg Receptor protein-tyrosine kinases and their signal transduction pathways Annu. Rev. Cell Biol. 10 1994 251 337
26. J. Sebastian, R.G. Richards, M.P. Walker, J.F. Wiesen, Z. Werb, R. Derynck, Y.K. Hom, G.R. Cunha, and R.P. DiAugustine Activation and function of the epidermal growth factor receptor and erbB-2 during mammary gland morphogenesis Cell Growth Differ. 9 1998 777 785
27. S.M. Snedeker, C.F. Brown, and R.P. DiAugustine Expression and functional properties of transforming growth factor alpha and epidermal growth factor during mouse mammary gland ductal morphogenesis Proc. Natl. Acad. Sci. U. S. A. 88 1991 276 280
28. M.R. Stampfer, C.H. Pan, J. Hosoda, J. Bartholomew, J. Mendelsohn, and P. Yaswen Blockage of EGF receptor signal transduction causes reversible arrest of normal and immortal human mammary epithelial cells with synchronous reentry into the cell cycle Exp. Cell Res. 208 1993 175 188
29. R.B. Dickson, and M.E. Lippman Growth factors in breast cancer Endocr. Rev. 16 1995 559 589
30. L.M. Wiedemann, and R.P. Perry Characterization of the expressed gene and several processed pseudogenes for the mouse ribosomal protein L30 gene family Mol. Cell. Biol. 4 1984 2518 2528
31. C. Delescluse, M.T. Cavey, B. Martin, B.A. Bernard, U. Reichert, J. Maignan, M. Darmon, and B. Shroot Selective high affinity retinoic acid receptor alpha or beta-gamma ligands Mol. Pharmacol. 40 1991 556 562
32. A.B. Pardee G1 events and regulation of cell proliferation Science 246 1989 603 608
33. C.A. Wallen, R. Higashikubo, and L.A. Dethlefsen Murine mammary tumour cells in vitro. I. The development of a quiescent state Cell Tissue Kinet. 17 1984 65 77
34. C.A. Wallen, R. Higashikubo, and L.A. Dethlefsen Murine mammary tumour cells in vitro. II. Recruitment of quiescent cells Cell Tissue Kinet. 17 1984 79 89
35. A. Agadir, Y.F. Shealy, D.L. Hill, and X. Zhang Retinyl methyl ether down-regulates activator protein 1 transcriptional activation in breast cancer cells Cancer Res. 57 1997 3444 3450
36. X.P. Lu, A. Fanjul, N. Picard, M. Pfahl, D. Rungta, K. Nared-Hood, B. Carter, J. Piedrafita, S. Tang, and E. Fabbrizio Novel retinoid-related molecules as apoptosis inducers and effective inhibitors of human lung cancer cells in vivo Nat. Med. 3 1997 686 690
37. D.A. Talmage, and R.S. Lackey Retinoic acid receptor alpha suppresses polyomavirus transformation and c-fos expression in rat fibroblasts Oncogene 7 1992 1837 1845
38. F.R. Khuri, Y. Cho, and D.A. Talmage Retinoic acid-induced transition from protein kinase C beta to protein kinase C alpha in differentiated F9 cells: correlation with altered regulation of proto-oncogene expression by phorbol esters Cell Growth Differ. 7 1996 595 602
39. N. Clarke, N. Arenzana, T. Hai, A. Minden, and R. Prywes Epidermal growth factor induction of the c-jun promoter by a Rac pathway Mol. Cell. Biol. 18 1998 1065 1073
40. C.S. Hill, and R. Treisman Transcriptional regulation by extracellular signals: mechanisms and specificity Cell 80 1995 199 211
41. M.A. Price, C. Hill, and R. Treisman Integration of growth factor signals at the c-fos serum response element Philos. Trans. R. Soc. London, Ser. B Biol. Sci. 351 1996 551 559
42. R. Treisman Journey to the surface of the cell: fos regulation and the SRE EMBO J. 14 1995 4905 4913
43. A.J. Whitmarsh, and R.J. Davis Transcription factor AP-1 regulation by mitogen-activated protein kinase signal transduction pathways J. Mol. Med. 74 1996 589 607
44. S. Yang, P.R. Yates, A.J. Whitmarsh, R.J. Davis, and A.D. Sharrocks The regulation of TCF transcription factors by MAP kinase cascades Biochem. Soc. Trans. 25 1997 153S
45. Y. Cho, M.G. Klein, and D.A. Talmage Distinct functions of protein kinase Calpha and protein kinase Cbeta during retinoic acid-induced differentiation of F9 cells Cell Growth Differ. 9 1998 147 154
46. G. Martiny-Baron, M.G. Kazanietz, H. Mischak, P.M. Blumberg, G. Kochs, H. Hug, D. Marme, and C. Schachtele Selective inhibition of protein kinase C isozymes by the indolocarbazole Go 6976 J. Biol. Chem. 268 1993 9194 9197
47. S. Bardon, and L. Razanamahefa Retinoic acid suppresses insulin-induced cell growth and cyclin D1 gene expression in human breast cancer cells Int. J. Oncol. 12 1998 355 359
48. C. Teixeira, and M.A. Pratt CDK2 is a target for retinoic acid-mediated growth inhibition in MCF-7 human breast cancer cells Mol. Endocrinol. 11 1997 1191 1202
49. N.R. Wilcken, B. Sarcevic, E.A. Musgrove, and R.L. Sutherland Differential effects of retinoids and antiestrogens on cell cycle progression and cell cycle regulatory genes in human breast cancer cells Cell Growth Differ. 7 1996 65 74
50. N.R. Wilcken, E.A. Musgrove, and R.L. Sutherland Different points of action of retinoids and anti-estrogens in G1 phase identified in synchronized T-47D breast cancer cells Int. J. Oncol. 70 1997 291 296
51. W.Y. Zhu, C.S. Jones, A. Kiss, K. Matsukuma, S. Amin, and L.M. De Luca Retinoic acid inhibition of cell cycle progression in MCF-7 human breast cancer cells Exp. Cell Res. 234 1997 293 299
52. H. Aktas, H. Cai, and G.M. Cooper Ras links growth factor signaling to the cell cycle machinery via regulation of cyclin D1 and the Cdk inhibitor p27KIP1 Mol. Cell. Biol. 17 1997 3850 3857
53. M.H. Ladha, K.Y. Lee, T.M. Upton, M.F. Reed, and M.E. Ewen Regulation of exit from quiescence by p27 and cyclin D1-CDK4 Mol. Cell. Biol. 18 1998 6605 6615
54. E.A. Musgrove, C.S. Lee, M.F. Buckley, and R.L. Sutherland Cyclin D1 induction in breast cancer cells shortens G1 and is sufficient for cells arrested in G1 to complete the cell cycle Proc. Natl. Acad. Sci. U. S. A. 91 1994 8022 8026
55. A.P. Tighe Institute of Human Nutrition 1999 Columbia University New York
56. S. Wakino, U. Kintscher, S. Kim, S. Jackson, F. Yin, S. Nagpal, R.A. Chandraratna, W.A. Hsueh, and R.E. Law Retinoids inhibit proliferation of human coronary smooth muscle cells by modulating cell cycle regulators Arterioscler., Thromb., Vasc. Biol. 21 2001 746 751
57. S.L. Hsu, J.W. Hsu, M.C. Liu, L.Y. Chen, and C.D. Chang Retinoic acid-mediated G1 arrest is associated with induction of p27(Kip1) and inhibition of cyclin-dependent kinase 3 in human lung squamous carcinoma CH27 cells Exp. Cell Res. 258 2000 322 331
58. K. Sasaki, S. Tamura, H. Tachibana, M. Sugita, Y. Gao, J. Furuyama, E. Kakishita, T. Sakai, T. Tamaoki, and T. Hashimoto-Tamaoki Expression and role of p27(kip1) in neuronal differentiation of embryonal carcinoma cells Brain Res. Mol. Brain Res. 77 2000 209 221
59. N. Sueoka, H.Y. Lee, G.L. Walsh, W.K. Hong, and J.M. Kurie Posttranslational mechanisms contribute to the suppression of specific cyclin:CDK complexes by all-trans retinoic acid in human bronchial epithelial cells Cancer Res. 59 1999 3838 3844
60. C.J. Sherr Cancer cell cycles Science 274 1996 1672 1677
61. D.S. Desai, S. Hirai, W.E. Karnes Jr., R.M. Niles, and S. Ohno Cloning and characterization of the murine PKC alpha promoter: identification of a retinoic acid response element Biochem. Biophys. Res. Commun. 263 1999 28 34
62. M. Vecchi, J. Baulida, and G. Carpenter Selective cleavage of the heregulin receptor ErbB-4 by protein kinase C activation J. Biol. Chem. 271 1996 18989 18995
63. X. Ouyang, T. Gulliford, and R.J. Epstein The duration of phorbol-inducible ErbB2 tyrosine dephosphorylation parallels that of receptor endocytosis rather than threonine-686 phosphorylation: implications for the physiological role of protein kinase C in growth factor receptor signalling Carcinogenesis 19 1998 2013 2019
64. X. Ouyang, T. Gulliford, H. Zhang, G.C. Huang, and R. Epstein Human cancer cells exhibit protein kinase C-dependent c-erbB-2 transmodulation that correlates with phosphatase sensitivity and kinase activity J. Biol. Chem. 271 1996 21786 21792
65. P. Morrison, A.R. Saltiel, and M.R. Rosner Role of mitogen-activated protein kinase kinase in regulation of the epidermal growth factor receptor by protein kinase C J. Biol. Chem. 271 1996 12891 12896
66. C. Fitzer-Attas, H. Eldar, L. Eisenbach, and E. Livneh The expression of PDGF-alpha but not PDGF-beta receptors is suppressed in Swiss/3T3 fibroblasts over-expressing protein kinase C-alpha FEBS Lett. 342 1994 165 170
67. H. Eldar, Y. Zisman, A. Ullrich, and E. Livneh Overexpression of protein kinase C alpha-subtype in Swiss/3T3 fibroblasts causes loss of both high and low affinity receptor numbers for epidermal growth factor J. Biol. Chem. 265 1990 13290 13296
68. L.S. Lee, and I.B. Weinstein Tumor-promoting phorbol esters inhibit binding of epidermal growth factor to cellular receptors Science 202 1978 313 315
69. R.J. Davis Independent mechanisms account for the regulation by protein kinase C of the epidermal growth factor receptor affinity and tyrosine-protein kinase activity J. Biol. Chem. 263 1988 9462 9469
70. P. Chen, H. Xie, and A. Wells Mitogenic signaling from the egf receptor is attenuated by a phospholipase C-gamma/protein kinase C feedback mechanism Mol. Biol Cell. 7 1996 871 881
71. J.J. Ho, E.R. Farrelly, and Y.S. Kim Phorbol ester reduces phosphorylation of epidermal growth factor receptor in pancreatic cancer cells by activation of a tyrosine phosphatase Biochem. Biophys. Res. Commun. 265 1999 728 733
72. T. Hunter, N. Ling, and J.A. Cooper Protein kinase C phosphorylation of the EGF receptor at a threonine residue close to the cytoplasmic face of the plasma membrane Nature 311 1984 480 483
73. R.J. Davis, and M.P. Czech Tumor-promoting phorbol diesters cause the phosphorylation of epidermal growth factor receptors in normal human fibroblasts at threonine-654 Proc. Natl. Acad. Sci. U. S. A. 82 1985 1974 1978
74. J. Downward, M.D. Waterfield, and P.J. Parker Autophosphorylation and protein kinase C phosphorylation of the epidermal growth factor receptor. Effect on tyrosine kinase activity and ligand binding affinity J. Biol. Chem. 260 1985 14538 14546
75. E. Livneh, T.J. Dull, E. Berent, R. Prywes, A. Ullrich, and J. Schlessinger Release of a phorbol ester-induced mitogenic block by mutation at Thr-654 of the epidermal growth factor receptor Mol. Cell. Biol. 8 1988 2302 2308
76. K.A. Lund, C.S. Lazar, W.S. Chen, B.J. Walsh, J.B. Welsh, J.J. Herbst, G.M. Walton, M.G. Rosenfeld, G.N. Gill, and H.S. Wiley Phosphorylation of the epidermal growth factor receptor at threonine 654 inhibits ligand-induced internalization and down-regulation J. Biol. Chem. 265 1990 20517 20523
77. B.E. Magun, L.M. Matrisian, and G.T. Bowden Epidermal growth factor. Ability of tumor promoter to alter its degradation, receptor affinity and receptor number J. Biol. Chem. 255 1980 6373 6381
78. M. Errasfa, and A. Stern Inhibition of epidermal growth factor-dependent protein tyrosine phosphorylation by phorbol myristate acetate is mediated by protein tyrosine phosphatase activity FEBS Lett. 339 1994 7 10
79. W. Langgut, and A. Ogilvie Silencing of the epidermal growth factor receptor in the absence of the ligand requires phospholipase C activity FEBS Lett. 372 1995 173 176
80. A. Ostman, and F.D. Bohmer Regulation of receptor tyrosine kinase signaling by protein tyrosine phosphatases Trends Cell Biol. 11 2001 258 266
81. H. Keilhack, T. Tenev, E. Nyakatura, J. Godovac-Zimmermann, L. Nielsen, K. Seedorf, and F.D. Bohmer Phosphotyrosine 1173 mediates binding of the protein-tyrosine phosphatase SHP-1 to the epidermal growth factor receptor and attenuation of receptor signaling J. Biol. Chem. 273 1998 24839 24846
82. T. Tenev, H. Keilhack, S. Tomic, B. Stoyanov, M. Stein-Gerlach, R. Lammers, A.V. Krivtsov, A. Ullrich, and F.D. Bohmer Both SH2 domains are involved in interaction of SHP-1 with the epidermal growth factor receptor but cannot confer receptor-directed activity to SHP-1/SHP-2 chimera J. Biol. Chem. 272 1997 5966 5973
83. S. Tomic, U. Greiser, R. Lammers, A. Kharitonenkov, E. Imyanitov, A. Ullrich, and F.D. Bohmer Association of SH2 domain protein tyrosine phosphatases with the epidermal growth factor receptor in human tumor cells. Phosphatidic acid activates receptor dephosphorylation by PTP1C J. Biol. Chem. 270 1995 21277 21284
84. M.L. Kuo, T.S. Huang, and J.K. Lin Preferential requirement for protein tyrosine phosphatase activity in the 12-O-tetradecanoylphorbol-13-acetate- induced differentiation of human colon cancer cells Biochem. Pharmacol. 50 1995 1217 1222
85. K. Yoshida, and D. Kufe Negative regulation of the SHPTP1 protein tyrosine phosphatase by protein kinase C delta in response to DNA damage Mol. Pharmacol. 60 2001 1431 1438
86. Z. Zhao, S.H. Shen, and E.H. Fischer Phorbol ester-induced expression, phosphorylation, and translocation of protein-tyrosine-phosphatase 1C in HL-60 cells Proc. Natl. Acad. Sci. U. S. A. 91 1994 5007 5011
87. M. Kizaki, M.I. Dawson, R. Heyman, E. Elster, R. Morosetti, S. Pakkala, D.L. Chen, H. Ueno, W. Chao, M. Morikawa, Y. Ikeda, D. Heber, M. Pfahl, and H.P. Koeffler Effects of novel retinoid X receptor-selective ligands on myeloid leukemia differentiation and proliferation in vitro Blood 87 1996 1977 1984
88. Y. Zhang, Y. Huang, A.K. Rishi, M.S. Sheikh, B. Shroot, U. Reichert, M. Dawson, G. Poirer, and J.A. Fontana Activation of the p38 and JNK/SAPK mitogen-activated protein kinase pathways during apoptosis is mediated by a novel retinoid Exp. Cell Res. 247 1999 233 240