Building a better understanding of the intracellular tyrosine kinase PTK6 — BRK by BRK

Lee, 1993, A survey of protein tyrosine kinase mRNAs expressed in normal human melanocytes, Oncogene, 8, 3403 Mitchell, 1994, Cloning and characterisation of cDNAs encoding a novel non-receptor tyrosine kinase, brk, expressed in human breast tumours, Oncogene, 9, 2383 Siyanova, 1994, Tyrosine kinase gene expression in the mouse small intestine, Oncogene, 9, 2053 Brauer, 2009, RAKing in AKT: a tumor suppressor function for the intracellular tyrosine kinase FRK, Cell Cycle, 8, 2728, 10.4161/cc.8.17.9389 Kohmura, 1994, A novel nonreceptor tyrosine kinase, Srm: cloning and targeted disruption, Mol. Cell Biol., 14, 6915, 10.1128/MCB.14.10.6915 Kawachi, 1997, Isolation of a cDNA encoding a tyrosine kinase expressed in murine skin, Exp. Dermatol., 6, 140, 10.1111/j.1600-0625.1997.tb00161.x Neet, 1996, Vertebrate non-receptor protein-tyrosine kinase families, Genes Cells, 1, 147, 10.1046/j.1365-2443.1996.d01-234.x Mitchell, 1997, Characterisation and chromosome mapping of the human non receptor tyrosine kinase gene, brk, Oncogene, 15, 1497, 10.1038/sj.onc.1201292 Serfas, 2003, Brk, Srm, Frk, and Src42A form a distinct family of intracellular Src-like tyrosine kinases, Oncol. Res., 13, 409, 10.3727/096504003108748438 D'Aniello, 2008, Gene expansion and retention leads to a diverse tyrosine kinase superfamily in amphioxus, Mol. Biol. Evol., 25, 1841, 10.1093/molbev/msn132 Park, 1997, Assignment of the human PTK6 gene encoding a non-receptor protein tyrosine kinase to 20q13.3 by fluorescence in situ hybridization, Cytogenet. Cell Genet., 77, 271, 10.1159/000134595 Llor, 1999, BRK/Sik expression in the gastrointestinal tract and in colon tumors, Clin. Cancer Res., 5, 1767 Lee, 1998, Exon–intron structure of the human PTK6 gene demonstrates that PTK6 constitutes a distinct family of non-receptor tyrosine kinase, Mol Cells, 8, 401 Kang, 2002, Characterization of the 5′-flanking region of the human PTK6 gene, Biochim. Biophys. Acta, 1574, 365, 10.1016/S0167-4781(02)00234-8 Simmen, 2007, Dysregulation of intestinal crypt cell proliferation and villus cell migration in mice lacking Kruppel-like factor 9, Am. J. Physiol. Gastrointest. Liver Physiol., 292, G1757, 10.1152/ajpgi.00013.2007 Qiu, 2002, Regulation of the nonreceptor tyrosine kinase Brk by autophosphorylation and by autoinhibition, J. Biol. Chem., 277, 34634, 10.1074/jbc.M203877200 Kim, 2005, An intramolecular interaction between SH2-kinase linker and kinase domain is essential for the catalytic activity of protein-tyrosine kinase-6, J. Biol. Chem., 280, 28973, 10.1074/jbc.M504568200 Derry, 2000, Sik (BRK) phosphorylates Sam68 in the nucleus and negatively regulates its RNA binding ability, Mol. Cell. Biol., 20, 6114, 10.1128/MCB.20.16.6114-6126.2000 Kim, 2007, Molecular dissection of the interaction between the SH3 domain and the SH2-Kinase Linker region in PTK6, Biochem. Biophys. Res. Commun., 362, 829, 10.1016/j.bbrc.2007.08.055 Ko, 2009, Structural basis of the auto-inhibition mechanism of nonreceptor tyrosine kinase PTK6, Biochem. Biophys. Res. Commun., 384, 236, 10.1016/j.bbrc.2009.04.103 Koo, 2002, Purification and spectroscopic characterization of the human protein tyrosine kinase-6 SH3 domain, J. Biochem. Mol. Biol., 35, 343, 10.5483/BMBRep.2002.35.3.343 Qiu, 2004, Role of Brk SH3 domain in substrate recognition, Oncogene, 23, 2216, 10.1038/sj.onc.1207339 Qiu, 2005, Interaction between Brk kinase and insulin receptor substrate-4, Oncogene, 24, 5656, 10.1038/sj.onc.1208721 Lukong, 2009, BRK phosphorylates PSF promoting its cytoplasmic localization and cell cycle arrest, Cell Signal., 21, 1415, 10.1016/j.cellsig.2009.04.008 Hong, 2001, Complete sequence-specific 1H, 13C and 15N resonance assignments of the human PTK6 SH2 domain, J. Biomol. NMR, 19, 291, 10.1023/A:1011221125013 Hong, 2004, Solution structure and backbone dynamics of the non-receptor protein-tyrosine kinase-6 Src homology 2 domain, J. Biol. Chem., 279, 29700, 10.1074/jbc.M313185200 Vasioukhin, 1997, A role for the epithelial-cell-specific tyrosine kinase Sik during keratinocyte differentiation, Proc. Natl. Acad. Sci. USA, 94, 14477, 10.1073/pnas.94.26.14477 Mitchell, 2000, A novel adaptor-like protein which is a substrate for the non-receptor tyrosine kinase, BRK, Oncogene, 19, 4273, 10.1038/sj.onc.1203775 Zhang, 2005, Regulated association of protein kinase b/akt with breast tumor kinase, J. Biol. Chem., 280, 1982, 10.1074/jbc.M412038200 Palka-Hamblin, 2010, Identification of {beta}-catenin as a target of the intracellular tyrosine kinase PTK6, J. Cell Sci., 123, 236, 10.1242/jcs.053264 Lukong, 2008, Breast tumor kinase BRK requires kinesin-2 subunit KAP3A in modulation of cell migration, Cell. Signal., 20, 432, 10.1016/j.cellsig.2007.11.003 Shen, 2008, Breast tumor kinase phosphorylates p190RhoGAP to regulate rho and ras and promote breast carcinoma growth, migration, and invasion, Cancer Res., 68, 7779, 10.1158/0008-5472.CAN-08-0997 Coyle, 2003, Sam68 enhances the cytoplasmic utilization of intron-containing RNA and is functionally regulated by the nuclear kinase Sik/BRK, Mol. Cell. Biol., 23, 92, 10.1128/MCB.23.1.92-103.2003 Lukong, 2005, Tyrosine phosphorylation of sam68 by breast tumor kinase regulates intranuclear localization and cell cycle progression, J. Biol. Chem., 280, 38639, 10.1074/jbc.M505802200 Aubele, 2008, Prognostic value of protein tyrosine kinase 6 (PTK6) for long-term survival of breast cancer patients, Br. J. Cancer, 99, 1089, 10.1038/sj.bjc.6604660 Haegebarth, 2004, 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., 279, 54398, 10.1074/jbc.M409579200 Ikeda, 2009, STAP-2 is phosphorylated at tyrosine-250 by Brk and modulates Brk-mediated STAT3 activation, Biochem. Biophys. Res. Commun., 384, 71, 10.1016/j.bbrc.2009.04.076 Liu, 2006, Identification of STAT3 as a specific substrate of breast tumor kinase, Oncogene, 25, 4904, 10.1038/sj.onc.1209501 Weaver, 2007, Signal transducer and activator of transcription 5b: a new target of breast tumor kinase/protein tyrosine kinase 6, Breast Cancer Res., 9, R79, 10.1186/bcr1794 Shin, 2008, Solid-phase peptide library synthesis on HiCore resin for screening substrate specificity of Brk protein tyrosine kinase, J. Comb. Chem., 10, 20, 10.1021/cc7001217 Zhong, 2008, Distinct functions of natural ADAM-15 cytoplasmic domain variants in human mammary carcinoma, Mol. Cancer Res., 6, 383, 10.1158/1541-7786.MCR-07-2028 Kamalati, 1996, Brk, a breast tumor-derived non-receptor protein-tyrosine kinase, sensitizes mammary epithelial cells to epidermal growth factor, J. Biol. Chem., 271, 30956, 10.1074/jbc.271.48.30956 Xiang, 2008, Brk is coamplified with ErbB2 to promote proliferation in breast cancer, Proc. Natl. Acad. Sci. USA, 105, 12463, 10.1073/pnas.0805009105 Mosnier, 2006, ADAM15 upregulation and interaction with multiple binding partners in inflammatory bowel disease, Lab. Invest., 86, 1064, 10.1038/labinvest.3700465 Charrier-Hisamuddin, 2008, ADAM-15: a metalloprotease that mediates inflammation, FASEB J., 22, 641, 10.1096/fj.07-8876rev Kamalati, 2000, Expression of the BRK tyrosine kinase in mammary epithelial cells enhances the coupling of EGF signalling to PI 3-kinase and Akt, via erbB3 phosphorylation, Oncogene, 19, 5471, 10.1038/sj.onc.1203931 Ostrander, 2007, Breast tumor kinase (protein tyrosine kinase 6) regulates heregulin-induced activation of ERK5 and p38 MAP kinases in breast cancer cells, Cancer Res., 67, 4199, 10.1158/0008-5472.CAN-06-3409 Najy, 2008, The ectodomain shedding of E-cadherin by ADAM15 supports ErbB receptor activation, J. Biol. Chem., 283, 18393, 10.1074/jbc.M801329200 Ellis, 1990, Phosphorylation of GAP and GAP-associated proteins by transforming and mitogenic tyrosine kinases, Nature, 343, 377, 10.1038/343377a0 Moran, 1991, Protein-tyrosine kinases regulate the phosphorylation, protein interactions, subcellular distribution, and activity of p21ras GTPase-activating protein, Mol. Cell. Biol., 11, 1804, 10.1128/MCB.11.4.1804 Filvaroff, 1992, Specific changes of Ras GTPase-activating protein (GAP) and a GAP-associated p62 protein during calcium-induced keratinocyte differentiation, Mol. Cell. Biol., 12, 5319, 10.1128/MCB.12.12.5319 Tsuruzoe, 2001, Insulin receptor substrate 3 (IRS-3) and IRS-4 impair IRS-1- and IRS-2-mediated signaling, Mol. Cell. Biol., 21, 26, 10.1128/MCB.21.1.26-38.2001 Giovannone, 2000, Insulin receptor substrate (IRS) transduction system: distinct and overlapping signaling potential, Diab. Metab. Res. Rev., 16, 434, 10.1002/1520-7560(2000)9999:9999<::AID-DMRR159>3.0.CO;2-8 Sesti, 2001, Defects of the insulin receptor substrate (IRS) system in human metabolic disorders, FASEB J., 15, 2099, 10.1096/fj.01-0009rev Taniguchi, 2006, Critical nodes in signalling pathways: insights into insulin action, Nat. Rev. Mol. Cell Biol., 7, 85, 10.1038/nrm1837 Bae, 2000, The human PTK6 interacts with a 23-kDa tyrosine-phosphorylated protein and is localized in cytoplasm in breast carcinoma T-47D cells, J. Biochem. Mol. Biol., 34, 33 Vasioukhin, 1995, A novel intracellular epithelial cell tyrosine kinase is expressed in the skin and gastrointestinal tract, Oncogene, 10, 349 Haegebarth, 2005, The intracellular tyrosine kinase Brk sensitizes non-transformed cells to inducers of apoptosis, Cell Cycle, 4, 1239, 10.4161/cc.4.9.1965 Haegebarth, 2006, Protein tyrosine kinase 6 negatively regulates growth and promotes enterocyte differentiation in the small intestine, Mol. Cell. Biol., 26, 4949, 10.1128/MCB.01901-05 Derry, 2003, Altered localization and activity of the intracellular tyrosine kinase BRK/Sik in prostate tumor cells, Oncogene, 22, 4212, 10.1038/sj.onc.1206465 Wang, 2005, Role of breast tumour kinase in the in vitro differentiation of HaCaT cells, Br. J. Dermatol., 153, 282, 10.1111/j.1365-2133.2005.06604.x Petro, 2004, Differential expression of the non-receptor tyrosine kinase BRK in oral squamous cell carcinoma and normal oral epithelium, Oral Oncol., 40, 1040, 10.1016/j.oraloncology.2004.05.010 Kasprzycka, 2006, Expression and oncogenic role of Brk (PTK6/Sik) protein tyrosine kinase in lymphocytes, Am. J. Pathol., 168, 1631, 10.2353/ajpath.2006.050521 Wang, 2009, NDRG3 is an androgen regulated and prostate enriched gene that promotes in vitro and in vivo prostate cancer cell growth, Int. J. Cancer, 124, 521, 10.1002/ijc.23961 Harvell, 2006, Estradiol regulates different genes in human breast tumor xenografts compared with the identical cells in culture, Endocrinology, 147, 700, 10.1210/en.2005-0617 Rinaudo, 2004, Effects of embryo culture on global pattern of gene expression in preimplantation mouse embryos, Reproduction, 128, 301, 10.1530/rep.1.00297 Whitehead, 2008, Conditionally immortalized colonic epithelial cell line from a Ptk6 null mouse that polarizes and differentiates in vitro, J. Gastroenterol. Hepatol., 23, 1119, 10.1111/j.1440-1746.2008.05308.x Haegebarth, 2009, Induction of protein tyrosine kinase 6 in mouse intestinal crypt epithelial cells promotes DNA damage-induced apoptosis, Gastroenterology, 137, 945, 10.1053/j.gastro.2009.05.054 Barker, 1997, BRK tyrosine kinase expression in a high proportion of human breast carcinomas, Oncogene, 15, 799, 10.1038/sj.onc.1201241 Harvey, 2009, Brk protects breast cancer cells from autophagic cell death induced by loss of anchorage, Am. J. Pathol., 175, 1226, 10.2353/ajpath.2009.080811 Schmandt, 2006, The BRK tyrosine kinase is expressed in high-grade serous carcinoma of the ovary, Cancer Biol. Ther., 5, 1136, 10.4161/cbt.5.9.2953 Chen, 1999, A role for the GSG domain in localizing Sam68 to novel nuclear structures in cancer cell lines, Mol. Biol. Cell, 10, 3015, 10.1091/mbc.10.9.3015 Lin, 2004, Identification of tyrosine kinases overexpressed in head and neck cancer, Arch. Otolaryngol. Head Neck Surg., 130, 311, 10.1001/archotol.130.3.311 Borczuk, 2003, Non-small-cell lung cancer molecular signatures recapitulate lung developmental pathways, Am. J. Pathol., 163, 1949, 10.1016/S0002-9440(10)63553-5 Yauch, 2005, Epithelial versus mesenchymal phenotype determines in vitro sensitivity and predicts clinical activity of erlotinib in lung cancer patients, Clin. Cancer Res., 11, 8686, 10.1158/1078-0432.CCR-05-1492 Coldren, 2006, Baseline gene expression predicts sensitivity to gefitinib in non-small cell lung cancer cell lines, Mol. Cancer Res., 4, 521, 10.1158/1541-7786.MCR-06-0095 Rikova, 2007, Global survey of phosphotyrosine signaling identifies oncogenic kinases in lung cancer, Cell, 131, 1190, 10.1016/j.cell.2007.11.025 Ruhe, 2007, Genetic alterations in the tyrosine kinase transcriptome of human cancer cell lines, Cancer Res., 67, 11368, 10.1158/0008-5472.CAN-07-2703 Kubo, 2009, Resequencing analysis of the human tyrosine kinase gene family in pancreatic cancer, Pancreas, 38, e200, 10.1097/MPA.0b013e3181b8feb0 Kubo, 2009, Resequencing and copy number analysis of the human tyrosine kinase gene family in poorly differentiated gastric cancer, Carcinogenesis, 30, 1857, 10.1093/carcin/bgp206 Prickett, 2009, Analysis of the tyrosine kinome in melanoma reveals recurrent mutations in ERBB4, Nat. Genet., 41, 1127, 10.1038/ng.438 Aubele, 2009, Overexpression of PTK6 (breast tumor kinase) protein—a prognostic factor for long-term breast cancer survival—is not due to gene amplification, Virchows Arch., 455, 117, 10.1007/s00428-009-0809-8 Meric, 2002, Expression profile of tyrosine kinases in breast cancer, Clin. Cancer Res., 8, 361 Chen, 2004, Brk activates rac1 and promotes cell migration and invasion by phosphorylating paxillin, Mol. Cell. Biol., 24, 10558, 10.1128/MCB.24.24.10558-10572.2004 Chakraborty, 2008, Osteopontin promotes vascular endothelial growth factor-dependent breast tumor growth and angiogenesis via autocrine and paracrine mechanisms, Cancer Res., 68, 152, 10.1158/0008-5472.CAN-07-2126 Lecrone, 2000, Calcium signals in prostate cancer cells: specific activation by bone-matrix proteins, Cell Calcium, 27, 35, 10.1054/ceca.1999.0083 Macri, 2009, Role of osteopontin in breast cancer patients, Tumori, 95, 48, 10.1177/030089160909500109 Shevde, 2010, Osteopontin: an effector and an effect of tumor metastasis, Curr. Mol. Med., 10, 71, 10.2174/156652410791065381 Ibrahim, 2010, Pathogenesis of osteoblastic bone metastases from prostate cancer, Cancer, 6, 1406, 10.1002/cncr.24896 Harvey, 2003, Use of RNA interference to validate Brk as a novel therapeutic target in breast cancer: Brk promotes breast carcinoma cell proliferation, Oncogene, 22, 5006, 10.1038/sj.onc.1206577 Ie Kim, 2009, Oncogenic functions of PTK6 are enhanced by its targeting to plasma membrane but abolished by its targeting to nucleus, J. Biochem., 146, 133, 10.1093/jb/mvp050 Zhao, 2003, Elevated expression levels of NCOA3, TOP1, and TFAP2C in breast tumors as predictors of poor prognosis, Cancer, 98, 18, 10.1002/cncr.11482 Aubele, 2007, PTK (protein tyrosine kinase)-6 and HER2 and 4, but not HER1 and 3 predict long-term survival in breast carcinomas, Br. J. Cancer, 96, 801, 10.1038/sj.bjc.6603613 Watson, 2008, The Stat family of transcription factors have diverse roles in mammary gland development, Semin. Cell Dev. Biol., 19, 401, 10.1016/j.semcdb.2008.07.021 Groner, 2008, The function of Stat3 in tumor cells and their microenvironment, Semin. Cell Dev. Biol., 19, 341, 10.1016/j.semcdb.2008.06.005 Wei, 2008, New insights into the roles of Stat5a/b and Stat3 in T cell development and differentiation, Semin. Cell Dev. Biol., 19, 394, 10.1016/j.semcdb.2008.07.011 Walker, 2009, Reciprocal effects of STAT5 and STAT3 in breast cancer, Mol. Cancer Res., 7, 966, 10.1158/1541-7786.MCR-08-0238 Madson, 2006, Erbb2 regulates inflammation and proliferation in the skin after ultraviolet irradiation, Am. J. Pathol., 169, 1402, 10.2353/ajpath.2006.060082 Yim, 2009, Rak functions as a tumor suppressor by regulating PTEN protein stability and function, Cancer Cell, 15, 304, 10.1016/j.ccr.2009.02.012 Richard, 2008, Sam68 haploinsufficiency delays onset of mammary tumorigenesis and metastasis, Oncogene, 27, 548, 10.1038/sj.onc.1210652 Nigg, 1997, Nucleocytoplasmic transport: signals, mechanisms and regulation, Nature, 386, 779, 10.1038/386779a0 Baselga, 2009, Novel anticancer targets: revisiting ERBB2 and discovering ERBB3, Nat. Rev. Cancer, 9, 463, 10.1038/nrc2656 Nahta, 2007, Trastuzumab: triumphs and tribulations, Oncogene, 26, 3637, 10.1038/sj.onc.1210379 Bender, 2008, Her2 cross talk and therapeutic resistance in breast cancer, Front. Biosci., 13, 3906, 10.2741/2978 Singer, 2008, Predicting the efficacy of trastuzumab-based therapy in breast cancer: current standards and future strategies, Biochim. Biophys. Acta, 1786, 105 Born, 2005, Simultaneous over-expression of the Her2/neu and PTK6 tyrosine kinases in archival invasive ductal breast carcinomas, J. Pathol., 205, 592, 10.1002/path.1720 Harvey, 2004, The Brk protein tyrosine kinase as a therapeutic target in cancer: opportunities and challenges, Anticancer Drugs, 15, 107, 10.1097/00001813-200402000-00002 Rogers, 2009, Determinants of response to epidermal growth factor receptor tyrosine kinase inhibition in squamous cell carcinoma of the head and neck, J. Pathol., 218, 122, 10.1002/path.2515 Uckun, 2007, Anti-breast cancer activity of LFM-A13, a potent inhibitor of Polo-like kinase (PLK), Bioorg. Med. Chem., 15, 800, 10.1016/j.bmc.2006.10.050