PTK6 inhibition promotes apoptosis of Lapatinib-resistant Her2+ breast cancer cells by inducing Bim

Breast Cancer Research

Volumn 17, Issue 1, 2015, Pages

  Park, Sun Hee ^a   Ito, Koichi ^a   Olcott, William ^a   Katsyv, Igor ^a   Halstead Nussloch, Gwyneth ^a   Irie, Hanna Y ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIM PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; JANUS KINASE; LAPATINIB; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN BID; PROTEIN KINASE B; PROTEIN MCL 1; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE 6; PUMA PROTEIN; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; APOPTOSIS REGULATORY PROTEIN; BCL2L11 PROTEIN, HUMAN; ERBB2 PROTEIN, HUMAN; MEMBRANE PROTEIN; ONCOPROTEIN; PROTEIN KINASE INHIBITOR; PTK6 PROTEIN, HUMAN; QUINAZOLINE DERIVATIVE; TUMOR PROTEIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; BREAST CANCER; BREAST CANCER CELL LINE; CANCER INHIBITION; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; DOWN REGULATION; ENZYME INHIBITION; FLUORESCENCE ACTIVATED CELL SORTING; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ANIMAL; BREAST TUMOR; CELL PROLIFERATION; DISEASE MODEL; DRUG EFFECTS; DRUG RESISTANCE; DRUG SCREENING; ENZYME ACTIVATION; FEMALE; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BCL-2-LIKE PROTEIN 11; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; DRUG RESISTANCE, NEOPLASM; ENZYME ACTIVATION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MEMBRANE PROTEINS; NEOPLASM PROTEINS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROTEIN KINASE INHIBITORS; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS; QUINAZOLINES; RECEPTOR, ERBB-2; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84936760736     PISSN: 14655411     EISSN: 1465542X     Source Type: Journal    
DOI: 10.1186/s13058-015-0594-z     Document Type: Article

References (64)

1. Brufsky AM. Current Approaches and Emerging Directions in HER2-resistant Breast Cancer. Breast Cancer (Auckl). 2014;8:109-18.
2. Irie HY, Shrestha Y, Selfors LM, Frye F, Iida N, Wang Z, et al. PTK6 regulates IGF-1-induced anchorage-independent survival. PLoS One. 2010;5, e11729.
3. Schmandt RE, Bennett M, Clifford S, Thornton A, Jiang F, Broaddus RR, et al. The BRK tyrosine kinase is expressed in high-grade serous carcinoma of the ovary. Cancer Biol Ther. 2006;5:1136-41.
4. Derry JJ, Prins GS, Ray V, Tyner AL. Altered localization and activity of the intracellular tyrosine kinase BRK/Sik in prostate tumor cells. Oncogene. 2003;22:4212-20.
5. Mitchell PJ, Barker KT, Martindale JE, Kamalati T, Lowe PN, Page MJ, et al. Cloning and characterisation of cDNAs encoding a novel non-receptor tyrosine kinase, brk, expressed in human breast tumours. Oncogene. 1994;9:2383-90.
6. Brauer PM, Tyner AL. Building a better understanding of the intracellular tyrosine kinase PTK6 - BRK by BRK. Biochim Biophys Acta. 1806;2010:66-73.
7. Ostrander JH, Daniel AR, Lange CA. Brk/PTK6 signaling in normal and cancer cell models. Curr Opin Pharmacol. 2010;10:662-9.
8. Harvey AJ, Pennington CJ, Porter S, Burmi RS, Edwards DR, Court W, et al. Brk protects breast cancer cells from autophagic cell death induced by loss of anchorage. Am J Pathol. 2009;175:1226-34.
9. Harvey AJ, Crompton MR. Use of RNA interference to validate Brk as a novel therapeutic target in breast cancer: Brk promotes breast carcinoma cell proliferation. Oncogene. 2003;22:5006-10.
10. Zheng Y, Wang Z, Bie W, Brauer PM, Perez White BE, Li J, et al. PTK6 activation at the membrane regulates epithelial-mesenchymal transition in prostate cancer. Cancer Res. 2013;73:5426-37.
11. Castro NE, Lange CA. Breast tumor kinase and extracellular signal-regulated kinase 5 mediate Met receptor signaling to cell migration in breast cancer cells. Breast Cancer Res. 2010;12:R60.
12. Derry JJ, Richard S, Valderrama Carvajal H, Ye X, Vasioukhin V, Cochrane AW, et al. Sik (BRK) phosphorylates Sam68 in the nucleus and negatively regulates its RNA binding ability. Mol Cell Biol. 2000;20:6114-26.
13. Coyle JH, Guzik BW, Bor YC, Jin L, Eisner-Smerage L, Taylor SJ, et al. Sam68 enhances the cytoplasmic utilization of intron-containing RNA and is functionally regulated by the nuclear kinase Sik/BRK. Mol Cell Biol. 2003;23:92-103.
14. Liu L, Gao Y, Qiu H, Miller WT, Poli V, Reich NC. Identification of STAT3 as a specific substrate of breast tumor kinase. Oncogene. 2006;25:4904-12.
15. Weaver AM, Silva CM. Signal transducer and activator of transcription 5b: a new target of breast tumor kinase/protein tyrosine kinase 6. Breast Cancer Res. 2007;9:R79.
16. Ikeda O, Miyasaka Y, Sekine Y, Mizushima A, Muromoto R, Nanbo A, et al. STAP-2 is phosphorylated at tyrosine-250 by Brk and modulates Brk-mediated STAT3 activation. Biochem Biophys Res Commun. 2009;384:71-5.
17. Zheng Y, Gierut J, Wang Z, Miao J, Asara JM, Tyner AL. Protein tyrosine kinase 6 protects cells from anoikis by directly phosphorylating focal adhesion kinase and activating AKT. Oncogene. 2013;32:4304-12.
18. Kang SA, Lee ST. PTK6 promotes degradation of c-Cbl through PTK6-mediated phosphorylation. Biochem Biophys Res Commun. 2013;431:734-9.
19. Chen HY, Shen CH, Tsai YT, Lin FC, Huang YP, Chen RH. Brk activates rac1 and promotes cell migration and invasion by phosphorylating paxillin. Mol Cell Biol. 2004;24:10558-72.
20. Zheng Y, Asara JM, Tyner AL. Protein-tyrosine kinase 6 promotes peripheral adhesion complex formation and cell migration by phosphorylating p130 CRK-associated substrate. J Biol Chem. 2012;287:148-58.
21. Haegebarth A, Nunez R, Tyner AL. The intracellular tyrosine kinase Brk sensitizes non-transformed cells to inducers of apoptosis. Cell Cycle. 2005;4:1239-46.
22. Kamalati T, Jolin HE, Mitchell PJ, Barker KT, Jackson LE, Dean CJ, et al. Brk, a breast tumor-derived non-receptor protein-tyrosine kinase, sensitizes mammary epithelial cells to epidermal growth factor. J Biol Chem. 1996;271:30956-63.
23. Xiang B, Chatti K, Qiu H, Lakshmi B, Krasnitz A, Hicks J, et al. Brk is coamplified with ErbB2 to promote proliferation in breast cancer. Proc Natl Acad Sci USA. 2008;105:12463-8.
24. Irie HY, Pearline RV, Grueneberg D, Hsia M, Ravichandran P, Kothari N, et al. Distinct roles of Akt1 and Akt2 in regulating cell migration and epithelial-mesenchymal transition. J Cell Biol. 2005;171:1023-34.
25. O'Brien NA, Browne BC, Chow L, Wang Y, Ginther C, Arboleda J, et al. Activated phosphoinositide 3-kinase/AKT signaling confers resistance to trastuzumab but not lapatinib. Mol Cancer Ther. 2010;9:1489-502.
26. Bean GR, Ganesan YT, Dong Y, Takeda S, Liu H, Chan PM, et al. PUMA and BIM are required for oncogene inactivation-induced apoptosis. Sci Signal. 2013;6:ra20.
27. Cancer Genome Atlas Network. Comprehensive molecular portraits of human breast tumours. Nature. 2012;490:61-70.
28. Tanizaki J, Okamoto I, Fumita S, Okamoto W, Nishio K, Nakagawa K. Roles of BIM induction and survivin downregulation in lapatinib-induced apoptosis in breast cancer cells with HER2 amplification. Oncogene. 2011;30:4097-106.
29. O'Connor L, Strasser A, O'Reilly LA, Hausmann G, Adams JM, Cory S, et al. Bim: a novel member of the Bcl-2 family that promotes apoptosis. The EMBO journal. 1998;17:384-95.
30. Akiyama T, Dass CR, Choong PF. Bim-targeted cancer therapy: a link between drug action and underlying molecular changes. Mol Cancer Ther. 2009;8:3173-80.
31. Faber AC, Corcoran RB, Ebi H, Sequist LV, Waltman BA, Chung E, et al. BIM expression in treatment-naive cancers predicts responsiveness to kinase inhibitors. Cancer discovery. 2011;1:352-65.
32. Ng KP, Hillmer AM, Chuah CT, Juan WC, Ko TK, Teo AS, et al. A common BIM deletion polymorphism mediates intrinsic resistance and inferior responses to tyrosine kinase inhibitors in cancer. Nat Med. 2012;18:521-8.
33. Costa DB, Halmos B, Kumar A, Schumer ST, Huberman MS, Boggon TJ, et al. BIM mediates EGFR tyrosine kinase inhibitor-induced apoptosis in lung cancers with oncogenic EGFR mutations. PLoS Med. 2007;4:1669-79. discussion 1680.
34. Cragg MS, Jansen ES, Cook M, Harris C, Strasser A, Scott CL. Treatment of B-RAF mutant human tumor cells with a MEK inhibitor requires Bim and is enhanced by a BH3 mimetic. J Clin Invest. 2008;118:3651-9.
35. Sunters A. Fernandez de Mattos S, Stahl M, Brosens JJ, Zoumpoulidou G, Saunders CA, et al. FoxO3a transcriptional regulation of Bim controls apoptosis in paclitaxel-treated breast cancer cell lines. J Biol Chem. 2003;278:49795-805.
36. Yano T, Ito K, Fukamachi H, Chi XZ, Wee HJ, Inoue K, et al. The RUNX3 tumor suppressor upregulates Bim in gastric epithelial cells undergoing transforming growth factor beta-induced apoptosis. Mol Cell Biol. 2006;26:4474-88.
37. Wildey GM, Howe PH. Runx1 is a co-activator with FOXO3 to mediate transforming growth factor beta (TGFbeta)-induced Bim transcription in hepatic cells. J Biol Chem. 2009;284:20227-39.
38. Puthalakath H, O'Reilly LA, Gunn P, Lee L, Kelly PN, Huntington ND, et al. ER stress triggers apoptosis by activating BH3-only protein Bim. Cell. 2007;129:1337-49.
39. Heidari N, Miller AV, Hicks MA, Marking CB, Harada H. Glucocorticoid-mediated BIM induction and apoptosis are regulated by Runx2 and c-Jun in leukemia cells. Cell death & disease. 2012;3, e349.
40. McCubrey JA, Steelman LS, Chappell WH, Abrams SL, Wong EW, Chang F, et al. Roles of the Raf/MEK/ERK pathway in cell growth, malignant transformation and drug resistance. Biochim Biophys Acta. 1773;2007:1263-84.
41. Huang H, Tindall DJ. Regulation of FOXO protein stability via ubiquitination and proteasome degradation. Biochim Biophys Acta. 1813;2011:1961-4.
42. Wang XZ, Ron D. Stress-induced phosphorylation and activation of the transcription factor CHOP (GADD153) by p38 MAP Kinase. Science. 1996;272:1347-9.
43. Faber AC, Ebi H, Costa C, Engelman JA. Apoptosis in targeted therapy responses: the role of BIM. Adv Pharmacol. 2012;65:519-42.
44. Ventura A, Young AG, Winslow MM, Lintault L, Meissner A, Erkeland SJ, et al. Targeted deletion reveals essential and overlapping functions of the miR-17 through 92 family of miRNA clusters. Cell. 2008;132:875-86.
45. Bachmann PS, Piazza RG, Janes ME, Wong NC, Davies C, Mogavero A, et al. Epigenetic silencing of BIM in glucocorticoid poor-responsive pediatric acute lymphoblastic leukemia, and its reversal by histone deacetylase inhibition. Blood. 2010;116:3013-22.
46. Pernaute B, Spruce T, Smith KM, Sanchez-Nieto JM, Manzanares M, Cobb B, et al. MicroRNAs control the apoptotic threshold in primed pluripotent stem cells through regulation of BIM. Genes Dev. 2014;28:1873-8.
47. Ley R, Balmanno K, Hadfield K, Weston C, Cook SJ. Activation of the ERK1/2 signaling pathway promotes phosphorylation and proteasome-dependent degradation of the BH3-only protein. Bim J Biol Chem. 2003;278:18811-6.
48. Cai B, Chang SH, Becker EB, Bonni A, Xia Z. p38 MAP kinase mediates apoptosis through phosphorylation of BimEL at Ser-65. J Biol Chem. 2006;281:25215-22.
49. Lu J, Quearry B, Harada H. p38-MAP kinase activation followed by BIM induction is essential for glucocorticoid-induced apoptosis in lymphoblastic leukemia cells. FEBS Lett. 2006;580:3539-44.
50. Phong MS, Van Horn RD, Li S, Tucker-Kellogg G, Surana U, Ye XS. p38 mitogen-activated protein kinase promotes cell survival in response to DNA damage but is not required for the G(2) DNA damage checkpoint in human cancer cells. Mol Cell Biol. 2010;30:3816-26.
51. Cosaceanu D, Budiu RA, Carapancea M, Castro J, Lewensohn R, Dricu A. Ionizing radiation activates IGF-1R triggering a cytoprotective signaling by interfering with Ku-DNA binding and by modulating Ku86 expression via a p38 kinase-dependent mechanism. Oncogene. 2007;26:2423-34.
52. Ostrander JH, Daniel AR, Lofgren K, Kleer CG, Lange CA. Breast tumor kinase (protein tyrosine kinase 6) regulates heregulin-induced activation of ERK5 and p38 MAP kinases in breast cancer cells. Cancer Res. 2007;67:4199-209.
53. Ludyga N, Anastasov N, Gonzalez-Vasconcellos I, Ram M, Hofler H, Aubele M. Impact of protein tyrosine kinase 6 (PTK6) on human epidermal growth factor receptor (HER) signalling in breast cancer. Mol BioSyst. 2011;7:1603-12.
54. Ludyga N, Anastasov N, Rosemann M, Seiler J, Lohmann N, Braselmann H, et al. Effects of simultaneous knockdown of HER2 and PTK6 on malignancy and tumor progression in human breast cancer cells. Mol Cancer Res. 2013;11:381-92.
55. Cufi S, Vazquez-Martin A, Oliveras-Ferraros C, Corominas-Faja B, Urruticoechea A, Martin-Castillo B, et al. Autophagy-related gene 12 (ATG12) is a novel determinant of primary resistance to HER2-targeted therapies: utility of transcriptome analysis of the autophagy interactome to guide breast cancer treatment. Oncotarget. 2012;3:1600-14.
56. Nagy P, Friedlander E, Tanner M, Kapanen AI, Carraway KL, Isola J, et al. Decreased accessibility and lack of activation of ErbB2 in JIMT-1, a herceptin-resistant, MUC4-expressing breast cancer cell line. Cancer Res. 2005;65:473-82.
57. Nagata Y, Lan KH, Zhou X, Tan M, Esteva FJ, Sahin AA, et al. PTEN activation contributes to tumor inhibition by trastuzumab, and loss of PTEN predicts trastuzumab resistance in patients. Cancer Cell. 2004;6:117-27.
58. Sos ML, Koker M, Weir BA, Heynck S, Rabinovsky R, Zander T, et al. PTEN loss contributes to erlotinib resistance in EGFR-mutant lung cancer by activation of Akt and EGFR. Cancer Res. 2009;69:3256-61.
59. Shim HJ, Yang HR, Kim H, Kang SA, No KT, Jung YH, et al. Discovery of (E)-5-(benzylideneamino)-1H-benzo[d]imidazol-2(3H)-one derivatives as inhibitors for PTK6. Bioorg Med Chem Lett. 2014;24:4659-63.
60. Mahmoud KA, Krug M, Wersig T, Slynko I, Schachtele C, Totzke F, et al. Discovery of 4-anilino alpha-carbolines as novel Brk inhibitors. Bioorg Med Chem Lett. 2014;24:1948-51.
61. Zeng H, Belanger DB, Curran PJ, Shipps Jr GW, Miao H, Bracken JB, et al. Discovery of novel imidazo[1,2-a]pyrazin-8-amines as Brk/PTK6 inhibitors. Bioorg Med Chem Lett. 2011;21:5870-5.
62. Haegebarth A, Heap D, Bie W, Derry JJ, Richard S, Tyner AL. The nuclear tyrosine kinase BRK/Sik phosphorylates and inhibits the RNA-binding activities of the Sam68-like mammalian proteins SLM-1 and SLM-2. J Biol Chem. 2004;279:54398-404.
63. Palka-Hamblin HL, Gierut JJ, Bie W, Brauer PM, Zheng Y, Asara JM, et al. Identification of beta-catenin as a target of the intracellular tyrosine kinase PTK6. J Cell Sci. 2010;123:236-45.
64. Shen CH, Chen HY, Lin MS, Li FY, Chang CC, Kuo ML, et al. Breast tumor kinase phosphorylates p190RhoGAP to regulate rho and ras and promote breast carcinoma growth, migration, and invasion. Cancer Res. 2008;68:7779-87.