Activated Abl kinase inhibits oncogenic transforming growth factor-β signaling and tumorigenesis in mammary tumors

FASEB Journal

Volumn 23, Issue 12, 2009, Pages 4231-4243

  Allington, Tressa M ^a   Galliher Beckley, Amy J ^a   Schiemann, William P ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

EMT; Imatinib; Matrix metalloproteinases; Organotypic cultures; Signal transduction

Indexed keywords

ABELSON KINASE; IMATINIB; MATRIX METALLOPROTEINASE; TRANSFORMING GROWTH FACTOR BETA;

ADJUVANT THERAPY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; BREAST CARCINOGENESIS; CANCER INHIBITION; CANCER THERAPY; CELL STRUCTURE; CONTROLLED STUDY; CYTOSTASIS; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INACTIVATION; ENZYME RELEASE; EPITHELIUM CELL; FEMALE; MESENCHYME CELL; METASTASIS; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ANIMALS; CELL LINE, TUMOR; EPITHELIAL CELLS; FEMALE; MAMMARY GLANDS, ANIMAL; MAMMARY NEOPLASMS, ANIMAL; METALLOPROTEASES; MICE; MICE, INBRED BALB C; PIPERAZINES; PROTEIN KINASE INHIBITORS; PYRIMIDINES; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

MUS;

EID: 72749120841     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.09-138412     Document Type: Article

References (68)

1. Benson, J. R. (2004) Role of TGF-β in breast carcinogenesis. Lancet Oncol. 5, 229-239
2. Dumont, N., and Arteaga, C. L. (2000) TGF-β and breast cancer: Tumor promoting effects of TGF-β. Breast Cancer Res. 2, 125-132
3. Pardali, K., and Moustakas, A. (2007) Actions of TGF-β as tumor suppressor and pro-metastatic factor in human cancer. Biochim. Biophys. Acta 1775, 21-62 (Pubitemid 44881193)
4. Wakefield, L. M., Piek, E., and Bottinger, E. P. (2001) TGF-β signaling in mammary gland development and tumorigenesis. J. Mammary Gland Biol. Neoplasia 6, 67-82 (Pubitemid 33640647)
5. Wakefield, L. M., and Roberts, A. B. (2002) TGF-β signaling: positive and negative effects on tumorigenesis. Curr. Opin. Genet. Dev. 12, 22-29 (Pubitemid 34094985)
6. Thiery, J. P. (2003) EMT in development and pathologies. Curr. Opin. Cell Biol. 15, 740-746
7. Xu, J., Lamouille, S., and Derynck, R. (2009) TGF-β-induced EMT. Cell Res. 19, 156-172
8. Moustakas, A., and Heldin, C. H. (2007) Signaling networks guiding EMT during embryogenesis and cancer progression. Cancer Sci. 98, 1512-1520
9. Kominsky, S. L., Doucet, M., Thorpe, M., and Weber, K. L. (2008) MMP-13 is over-expressed in renal cell carcinoma bone metastasis and is induced by TGF-β1. Clin. Exp. Metastasis 25, 865-870
10. Sinpitaksakul, S. N., Pimkhaokham, A., Sanchavanakit, N., and Pavasant, P. (2008) TGF-β1 induced MMP-9 expression in HNSCC cell lines via Smad/MLCK pathway. Biochem. Biophys. Res. Commun. 371, 713-718
11. Yan, C., and Boyd, D. D. (2007) Regulation of matrix metalloproteinase gene expression. J. Cell. Physiol. 211, 19-26 (Pubitemid 46363892)
12. Mott, J. D., and Werb, Z. (2004) Regulation of matrix biology by matrix metalloproteinases. Curr. Opin. Cell Biol. 16, 558-564
13. Woodring, P. J., Litwack, E. D., O'Leary, D. D., Lucero, G. R., Wang, J. Y., and Hunter, T. (2002) Modulation of the F-actin cytoskeleton by c-Abl tyrosine kinase in cell spreading and neurite extension. J. Cell Biol. 156, 879-892
14. Woodring, P. J., Meisenhelder, J., Johnson, S. A., Zhou, G. L., Field, J., Shah, K., Bladt, F., Pawson, T., Niki, M., Pandolfi, P. P., Wang, J. Y., and Hunter, T. (2004) c-Abl phosphorylates Dok1 to promote filopodia during cell spreading. J. Cell Biol. 165, 493-503 (Pubitemid 38679615)
15. Pendergast, A. M. (2002) The Abl family kinases: mechanisms of regulation and signaling. Adv. Cancer Res. 85, 51-100
16. Pendergast, A. M. (1996) Nuclear tyrosine kinases: from Abl to WEE1. Curr. Opin. Cell Biol. 8, 174-181
17. Zandy, N. L., and Pendergast, A. M. (2008) Abl tyrosine kinases modulate cadherin-dependent adhesion upstream and downstream of Rho family GTPases. Cell Cycle 7, 444-448
18. Lin, J., and Arlinghaus, R. (2008) Activated c-Abl tyrosine kinase in malignant solid tumors. Oncogene 27, 4385-4391
19. Srinivasan, D., Sims, J. T., and Plattner, R. (2008) Aggressive breast cancer cells are dependent on activated Abl kinases for proliferation, anchorage-independent growth and survival. Oncogene 27, 1095-1105 (Pubitemid 351253178)
20. Srinivasan, D., and Plattner, R. (2006) Activation of Abl tyrosine kinases promotes invasion of aggressive breast cancer cells. Cancer Res. 66, 5648-5655 (Pubitemid 43927117)
21. Plattner, R., Kadlec, L., DeMali, K. A., Kazlauskas, A., and Pendergast, A. M. (1999) c-Abl is activated by growth factors and Src family kinases and has a role in the cellular response to PDGF. Genes Dev. 13, 2400-2411 (Pubitemid 29453611)
22. Sirvent, A., Boureux, A., Simon, V., Leroy, C., and Roche, S. (2007) The tyrosine kinase Abl is required for Src-transforming activity in mouse fibroblasts and human breast cancer cells. Oncogene 26, 7313-7323 (Pubitemid 350115977)
23. Li, L. S., Morales, J. C., Hwang, A., Wagner, M. W., and Boothman, D. A. (2008) DNA mismatch repair-dependent activation of c-Abl/p73α/ GADD45α-mediated apoptosis. J. Biol. Chem. 283, 21394-21403
24. Wagner, M. W., Li, L. S., Morales, J. C., Galindo, C. L., Garner, H. R., Bornmann, W. G., and Boothman, D. A. (2008) Role of c-Abl kinase in DNA mismatch repair-dependent G2 cell cycle checkpoint arrest responses. J. Biol. Chem. 283, 21382-21393
25. Hamer, G., Gademan, I. S., Kal, H. B., and de Rooij, D. G. (2001) Role for c-Abl and p73 in the radiation response of male germ cells. Oncogene 20, 4298-4304 (Pubitemid 32726871)
26. Ongkeko, W. M., An, Y., Chu, T. S., Aguilera, J., Dang, C. L., and Wang-Rodriguez, J. (2006) Gleevec suppresses p63 expression in head and neck squamous cell carcinoma despite p63 activation by DNA-damaging agents. Laryngoscope 116, 1390-1396 (Pubitemid 44181453)
27. Noren, N. K., Foos, G., Hauser, C. A., and Pasquale, E. B. (2006) The EphB4 receptor suppresses breast cancer cell tumorigenicity through an Abl-Crk pathway. Nat. Cell Biol. 8, 815-825 (Pubitemid 44151584)
28. Gharibo, M., Patrick-Miller, L., Zheng, L., Guensch, L., Juvidian, P., and Poplin, E. (2008) A phase II trial of imatinib mesylate in patients with metastatic pancreatic cancer. Pancreas 36, 341-345 (Pubitemid 351591575)
29. Modi, S., Seidman, A. D., Dickler, M., Moasser, M., D'Andrea, G., Moynahan, M. E., Menell, J., Panageas, K. S., Tan, L. K., Norton, L., and Hudis, C. A. (2005) A phase II trial of imatinib mesylate monotherapy in patients with metastatic breast cancer. Breast Cancer Res. Treat. 90, 157-163
30. Chew, H. K., Barlow, W. E., Albain, K., Lew, D., Gown, A., Hayes, D. F., Gralow, J., Hortobagyi, G. N., and Livingston, R. (2008) A phase II study of imatinib mesylate and capecitabine in metastatic breast cancer: Southwest Oncology Group Study 0338. Clin. Breast Cancer 8, 511-515
31. Cristofanilli, M., Morandi, P., Krishnamurthy, S., Reuben, J. M., Lee, B. N., Francis, D., Booser, D. J., Green, M. C., Arun, B. K., Pusztai, L., Lopez, A., Islam, R., Valero, V., and Hortobagyi, G. N. (2008) Imatinib mesylate (Gleevec) in advanced breast cancer-expressing C-Kit or PDGFR-β: clinical activity and biological correlations. Ann. Oncol. 19, 1713-1719
32. Lin, A. M., Rini, B. I., Derynck, M. K., Weinberg, V., Park, M., Ryan, C. J., Rosenberg, J. E., Bubley, G., and Small, E. J. (2007) A phase I trial of docetaxel/estramustine/imatinib in patients with hormone-refractory prostate cancer. Clin. Genitourin. Cancer 5, 323-328 (Pubitemid 47265551)
33. Lin, A. M., Rini, B. I., Weinberg, V., Fong, K., Ryan, C. J., Rosenberg, J. E., Fong, L., and Small, E. J. (2006) A phase II trial of imatinib mesylate in patients with biochemical relapse of prostate cancer after definitive local therapy. BJU Int. 98, 763-769 (Pubitemid 44368021)
34. Bajaj, G. K., Zhang, Z., Garrett-Mayer, E., Drew, R., Sinibaldi, V., Pili, R., Denmeade, S. R., Carducci, M. A., Eisenberger, M. A., and DeWeese, T. L. (2007) Phase II study of imatinib mesylate in patients with prostate cancer with evidence of biochemical relapse after definitive radical retropubic prostatectomy or radiotherapy. Urology 69, 526-531 (Pubitemid 46428397)
35. Chen, J., Rocken, C., Nitsche, B., Hosius, C., Gschaidmeier, H., Kahl, S., Malfertheiner, P., and Ebert, M. P. (2006) The tyrosine kinase inhibitor imatinib fails to inhibit pancreatic cancer progression. Cancer Lett. 233, 328-337 (Pubitemid 43327389)
36. Woodring, P. J., Hunter, T., and Wang, J. Y. (2001) Inhibition of c-Abl tyrosine kinase activity by filamentous actin. J. Biol. Chem. 276, 27104-27110 (Pubitemid 37410618)
37. Schiemann, W. P., Blobe, G. C., Kalume, D. E., Pandey, A., and Lodish, H. F. (2002) Context-specific effects of fibulin-5 (DANCE/EVEC) on cell proliferation, motility, and invasion. Fibulin-5 is induced by TGF-β and affects protein kinase cascades. J. Biol. Chem. 277, 27367-27377 (Pubitemid 34951757)
38. Albini, A., Iwamoto, Y., Kleinman, H. K., Martin, G. R., Aaronson, S. A., Kozlowski, J. M., and McEwan, R. N. (1987) A rapid in vitro assay for quantitating the invasive potential of tumor cells. Cancer Res. 47, 3239-3245 (Pubitemid 17082655)
39. Schiemann, B. J., Neil, J. R., and Schiemann, W. P. (2003) SPARC inhibits epithelial cell proliferation in part through stimulation of the TGF-β-signaling system. Mol. Biol. Cell 14, 3977-3988
40. Echarri, A., and Pendergast, A. M. (2001) Activated c-Abl is degraded by the ubiquitin-dependent proteasome pathway. Curr. Biol. 11, 1759-1765 (Pubitemid 33092163)
41. Butcher, D. T., Alliston, T., and Weaver, V. M. (2009) A tense situation: forcing tumour progression. Nat. Rev. Cancer 9, 108-122
42. Kumar, S., and Weaver, V. M. (2009) Mechanics, malignancy, and metastasis: the force journey of a tumor cell. Cancer Metastasis Rev. 28, 113-127
43. Erler, J. T., and Weaver, V. M. (2009) Three-dimensional context regulation of metastasis. Clin. Exp. Metastasis 26, 35-49
44. Paszek, M. J., Zahir, N., Johnson, K. R., Lakins, J. N., Rozenberg, G. I., Gefen, A., Reinhart-King, C. A., Margulies, S. S., Dembo, M., Boettiger, D., Hammer, D. A., and Weaver, V. M. (2005) Tensional homeostasis and the malignant phenotype. Cancer Cell 8, 241-254
45. Lemaitre, V., and D'Armiento, J. (2006) Matrix metalloproteinases in development and disease. Birth Defects Res. C Embryo Today 78, 1-10
46. Radisky, D. C., and Przybylo, J. A. (2008) Matrix metalloproteinase- induced fibrosis and malignancy in breast and lung. Proc. Am. Thorac. Soc. 5, 316-322
47. Przybylo, J. A., and Radisky, D. C. (2007) Matrix metalloproteinase- induced EMT: tumor progression at Snail's pace. Int. J. Biochem. Cell Biol. 39, 1082-1088
48. Bissell, M. J., Kenny, P. A., and Radisky, D. C. (2005) Microenvironmental regulators of tissue structure and function also regulate tumor induction and progression: the role of extracellular matrix and its degrading enzymes. Cold Spring Harb. Symp. Quant. Biol. 70, 343-356
49. Radisky, D. C., Levy, D. D., Littlepage, L. E., Liu, H., Nelson, C. M., Fata, J. E., Leake, D., Godden, E. L., Albertson, D. G., Nieto, M. A., Werb, Z., and Bissell, M. J. (2005) Rac1b and reactive oxygen species mediate MMP-3-induced EMT and genomic instability. Nature 436, 123-127 (Pubitemid 40966197)
50. Galliher-Beckley, A. J., and Schiemann, W. P. (2008) Grb2 binding to Tyr284 in TβR-II is essential for mammary tumor growth and metastasis stimulated by TGF-β. Carcinogenesis 29, 244-251
51. Neil, J. R., and Schiemann, W. P. (2008) Altered TAB1:I B kinase interaction promotes TGF-β-mediated NF-κB activation during breast cancer progression. Cancer Res. 68, 1462-1470
52. Lee, Y. H., Albig, A. R., Regner, M., Schiemann, B. J., and Schiemann, W. P. (2008) Fibulin-5 initiates EMT and enhances EMT induced by TGF-β in mammary epithelial cells via a MMP-dependent mechanism. Carcinogenesis 29, 2243-2251
53. Soverini, S., Martinelli, G., Iacobucci, I., and Baccarani, M. (2008) Imatinib mesylate for the treatment of chronic myeloid leukemia. Expert Rev. Anticancer Ther. 8, 853-864
54. Wang, J. Y. (2006) Eph tumour suppression: the dark side of Gleevec. Nat. Cell Biol. 8, 785-786
55. Kain, K. H., and Klemke, R. L. (2001) Inhibition of cell migration by Abl family tyrosine kinases through uncoupling of Crk-CAS complexes. J. Biol. Chem. 276, 16185-16192 (Pubitemid 37391659)
56. Frasca, F., Vigneri, P., Vella, V., Vigneri, R., and Wang, J. Y. (2001) Tyrosine kinase inhibitor STI571 enhances thyroid cancer cell motile response to hepatocyte growth factor. Oncogene 20, 3845-3856 (Pubitemid 32646195)
57. Tian, M., and Schiemann, W. P. (2009) The TGF-β paradox in human cancer: an update. Future Oncol. 5, 259-271
58. Schiemann, W. P. (2007) Targeted TGF-β chemotherapies: friend or foe in treating human malignancies? Expert Rev. Anticancer Ther. 7, 609-611
59. Bhattacharyya, S., Ishida, W., Wu, M., Wilkes, M., Mori, Y., Hinchcliff, M., Leof, E., and Varga, J. (2009) A non-Smad mechanism of fibroblast activation by TGF-β via c-Abl and Egr-1: selective modulation by imatinib mesylate. Oncogene 28, 1285-1297
60. Wilkes, M. C., and Leof, E. B. (2006) TGF-β activation of c-Abl is independent of receptor internalization and regulated by phosphatidylinositol 3-kinase and PAK2 in mesenchymal cultures. J. Biol. Chem. 281, 27846-27854
61. Wang, S., Wilkes, M. C., Leof, E. B., and Hirschberg, R. (2005) Imatinib mesylate blocks a non-Smad TGF-β pathway and reduces renal fibrogenesis in vivo. FASEB J. 19, 1-11 (Pubitemid 40069914)
62. Daniels, C. E., Wilkes, M. C., Edens, M., Kottom, T. J., Murphy, S. J., Limper, A. H., and Leof, E. B. (2004) Imatinib mesylate inhibits the profibrogenic activity of TGF-β and prevents bleomycin-mediated lung fibrosis. J. Clin. Invest. 114, 1308-1316 (Pubitemid 40385302)
63. Mani, S. A., Guo, W., Liao, M. J., Eaton, E. N., Ayyanan, A., Zhou, A. Y., Brooks, M., Reinhard, F., Zhang, C. C., Shipitsin, M., Campbell, L. L., Polyak, K., Brisken, C., Yang, J., and Weinberg, R. A. (2008) The EMT generates cells with properties of stem cells. Cell 133, 704-715
64. Bissell, M. J., and Labarge, M. A. (2005) Context, tissue plasticity, and cancer: are tumor stem cells also regulated by the microenvironment? Cancer Cell 7, 17-23
65. Mintz, B., and Illmensee, K. (1975) Normal genetically mosaic mice produced from malignant teratocarcinoma cells. Proc. Natl. Acad. Sci. U. S. A. 72, 3585-3589
66. Hochedlinger, K., Blelloch, R., Brennan, C., Yamada, Y., Kim, M., Chin, L., and Jaenisch, R. (2004) Reprogramming of a melanoma genome by nuclear transplantation. Genes Dev. 18, 1875-1885 (Pubitemid 39025097)
67. Skiles, J. W., Gonnella, N. C., and Jeng, A. Y. (2004) The design, structure, and clinical update of small molecular weight matrix metalloproteinase inhibitors. Curr. Med. Chem. 11, 2911-2977
68. Skiles, J. W., Gonnella, N. C., and Jeng, A. Y. (2001) The design, structure, and therapeutic application of matrix metalloproteinase inhibitors. Curr. Med. Chem. 8, 425-474