Brk/Protein Tyrosine Kinase 6 Phosphorylates p27^KIP1, Regulating the Activity of Cyclin D–Cyclin-Dependent Kinase 4

REFERENCES

• Bockstaele L, Coulonval K, Kooken H, Paternot S, Roger PP. 2006. Regulation of CDK4. Cell Div 1:25. http://dx.doi.org/10.1186/1747-1028-1-25.
   PubMed Web of Science ®Google Scholar
• Ortega S, Malumbres M, Barbacid M. 2002. Cyclin D-dependent kinases, INK4 inhibitors and cancer. Biochim Biophys Acta 1602:73–87. http://dx.doi.org/10.1016/S0304-419X(02)00037-9.
   PubMed Web of Science ®Google Scholar
• Malumbres M, Barbacid M. 2006. Is cyclin D1-CDK4 kinase a bona fide cancer target? Cancer Cell 9:2–4. http://dx.doi.org/10.1016/j.ccr.2005.12.026.
   PubMed Web of Science ®Google Scholar
• Malumbres M, Sotillo R, Santamaria D, Galan J, Cerezo A, Ortega S, Dubus P, Barbacid M. 2004. Mammalian cells cycle without the D-type cyclin-dependent kinases Cdk4 and Cdk6. Cell 118:493–504. http://dx.doi.org/10.1016/j.cell.2004.08.002.
   PubMed Web of Science ®Google Scholar
• Yu Q, Geng Y, Sicinski P. 2001. Specific protection against breast cancers by cyclin D1 ablation. Nature 411:1017–1021. http://dx.doi.org/10.1038/35082500.
   PubMed Web of Science ®Google Scholar
• Yu Q, Sicinska E, Geng Y, Ahnstrom M, Zagozdzon A, Kong Y, Gardner H, Kiyokawa H, Harris NL, Stal O, Sicinski P. 2006. Requirement for CDK4 kinase function in breast cancer. Cancer Cell 9:23–32. http://dx.doi.org/10.1016/j.ccr.2005.12.012.
   PubMed Web of Science ®Google Scholar
• Sherr CJ, Roberts JM. 1999. CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev 13:1501–1512. http://dx.doi.org/10.1101/gad.13.12.1501.
   PubMed Web of Science ®Google Scholar
• Blain SW. 2008. Switching cyclin D-cdk4 kinase activity on and off. Cell Cycle 7:892–898. http://dx.doi.org/10.4161/cc.7.7.5637.
   PubMed Web of Science ®Google Scholar
• Jäkel H, Peschel I, Kunze C, Weinl C, Hengst L. 2012. Regulation of p27 (Kip1) by mitogen-induced tyrosine phosphorylation. Cell Cycle 11:1910–1917. http://dx.doi.org/10.4161/cc.19957.
   PubMed Web of Science ®Google Scholar
• Chu I, Sun J, Arnaout A, Kahn H, Hanna W, Narod S, Sun P, Tan CK, Hengst L, Slingerland JM. 2007. p27 phosphorylation by Src regulates inhibition of cyclin E-Cdk2. Cell 128:281–294. http://dx.doi.org/10.1016/j.cell.2006.11.049.
   PubMed Web of Science ®Google Scholar
• Grimmler M, Wang Y, Mund T, Cilensek Z, Keidel EM, Waddell MB, Jakel H, Kullmann M, Kriwacki RW, Hengst L. 2007. Cdk-inhibitory activity and stability of p27Kip1 are directly regulated by oncogenic tyrosine kinases. Cell 128:269–280. http://dx.doi.org/10.1016/j.cell.2006.11.047.
   PubMed Web of Science ®Google Scholar
• James MK, Ray A, Leznova D, Blain SW. 2008. Differential modification of p27Kip1 controls its cyclin D-cdk4 activity. Mol Cell Biol 28:498–510. http://dx.doi.org/10.1128/MCB.02171-06.
   PubMed Web of Science ®Google Scholar
• Kardinal C, Dangers M, Kardinal A, Koch A, Brandt DT, Tamura T, Welte K. 2006. Tyrosine phosphorylation modulates binding preference to a cyclin-dependent kinases and subcellular localization of p27 kip1 in the acute promyelocytic leukemia cell line NB4. Blood 107:1133–1140. http://dx.doi.org/10.1182/blood-2005-05-1771.
   PubMedGoogle Scholar
• Ray A, James MK, Larochelle S, Fisher RP, Blain SW. 2009. p27Kip1 inhibits cyclin D-cyclin-dependent kinase 4 by two independent modes. Mol Cell Biol 29:986–999. http://dx.doi.org/10.1128/MCB.00898-08.
   PubMed Web of Science ®Google Scholar
• Russo AA, Jeffrey PD, Patten A, Massagué J, Pavletich N. 1996. Crystal structure of the p27Kip1 cyclin-dependent kinase inhibitor bound to the cyclin A-cdk2 complex. Nature 382:325–331. http://dx.doi.org/10.1038/382325a0.
   PubMed Web of Science ®Google Scholar
• Galea CA, Nourse A, Wang Y, Sivakolundu SG, Heller WT, Kriwacki RW. 2008. Role of intrinsic flexibility in signal transduction mediated by the cell cycle regulator, p27 Kip1. J Mol Biol 376:827–838. http://dx.doi.org/10.1016/j.jmb.2007.12.016.
   PubMed Web of Science ®Google Scholar
• Jäkel H, Weinl C, Hengst L. 2011. Phosphorylation of p27Kip1 by JAK2 directly links cytokine receptor signaling to cell cycle control. Oncogene 30:3502–3512. http://dx.doi.org/10.1038/onc.2011.68.
   PubMed Web of Science ®Google Scholar
• Manning G, Whyte DB, Martinez R, Hunter T, Sudarsanam S. 2002. The protein kinase complement of the human genome. Science 298:1912–1934. http://dx.doi.org/10.1126/science.1075762.
   PubMed Web of Science ®Google Scholar
• Neet K, Hunter T. 1996. Vertebrate non-receptor protein-tyrosine kinase families. Genes Cells 1:147–169. http://dx.doi.org/10.1046/j.1365-2443.1996.d01-234.x.
   PubMedGoogle Scholar
• Serfas MS, Tyner AL. 2003. Brk, Srm, Frk, and Src42A form a distinct family of intracellular Src-like tyrosine kinases. Oncol Res 13:409–419. http://dx.doi.org/10.3727/096504003108748438.
   PubMed Web of Science ®Google Scholar
• Harrison SC. 2003. Variation on an Src-like theme. Cell 112:737–740. http://dx.doi.org/10.1016/S0092-8674(03)00196-X.
   PubMed Web of Science ®Google Scholar
• Miller TW, Shirley TL, Wolfgang WJ, Kang X, Messer A. 2003. DNA vaccination against mutant huntingtin ameliorates the HDR6/2 diabetic phenotype. Mol Ther 7:572–579. http://dx.doi.org/10.1016/S1525-0016(03)00063-7.
   PubMed Web of Science ®Google Scholar
• Qiu H, Miller TW. 2004. Role of the Brk SH3 domain in substrate recognition. Oncogene 23:2216–2223. http://dx.doi.org/10.1038/sj.onc.1207339.
   PubMedGoogle Scholar
• Brauer PM, Tyner AL. 2010. Building a better understanding of the intracellular tyrosine kinase PTK6—BRK by BRK. Biochim Biophys Acta 1806:66–73. http://dx.doi.org/10.1016/j.bbcan.2010.02.003.
   PubMed Web of Science ®Google Scholar
• Mitchell PJ, Barker KT, Martindale JE, Kamalati T, Lowe PN, Page MJ, Gusterson BA, Crompton MR. 1994. Cloning and characterisation of cDNAs encoding a novel non-receptor tyrosine kinase, brk, expressed in human breast tumours. Oncogene 9:2383–2390.
   PubMed Web of Science ®Google Scholar
• Siyanova E, Serfas M, Mazo I, Tyner A. 1994. Tyrosine kinase gene expression in the mouse small intestine. Oncogene 9:2053–2057.
   PubMed Web of Science ®Google Scholar
• Asbach B, Ludwig C, Saksela K, Wagner R. 2012. Comprehensive analysis of interactions between the Src-associated protein in mitosis of 68 kDa and the human Src-homology 3 proteome. PLoS One 7:e38540. http://dx.doi.org/10.1371/journal.pone.0038540.
   PubMedGoogle Scholar
• Vasioukhin V, Tyner AL. 1997. A role for the epithelial-cell-specific tyrosine kinase Sik during keratinocyte differentiation. Proc Natl Acad Sci U S A 94:14477–14482. http://dx.doi.org/10.1073/pnas.94.26.14477.
   PubMed Web of Science ®Google Scholar
• Brauer PM, Zheng Y, Evans MD, Dominguez-Brauer C, Peehl DM, Tyner AL. 2011. The alternative splice variant of protein tyrosine kinase 6 negatively regulates growth and enhances PTK6-mediated inhibition of β-catenin. PLoS One 6:e14789. http://dx.doi.org/10.1371/journal.pone.0014789.
   PubMedGoogle Scholar
• Nguyen KD, Blain SW, Gress F, Treem WR. 2010. Inflammatory mediators of esophagitis alter p27 kip1 expression in esophageal epithelial cells. J Pediatr Gastroeneterol Nutr 51:556–562. http://dx.doi.org/10.1097/MPG.0b013e3181ecd65d.
   PubMedGoogle Scholar
• Palka-Hamblin HL, Gierut JJ, Bie W, Brauer PM, Zheng Y, Asara JM, Tyner AL. 2010. Identification of beta-catenin as a target of the intracellular tyrosine kinase PTK6. J Cell Sci 123:236–245. http://dx.doi.org/10.1242/jcs.053264.
   PubMed Web of Science ®Google Scholar
• Cesareni G, Panni S, Nardelli G, Castagnoli L. 2002. Can we infer peptide recognition specificity mediated by SH3 domains? FEBS Lett 513:38–44. http://dx.doi.org/10.1016/S0014-5793(01)03307-5.
   PubMed Web of Science ®Google Scholar
• Ai M, Qiu S, Lu Y, Fan Z. 2013. HER2 regulates Brk/PTK6 stability via upregulating calpastatin, an inhibitor of calpain. Cell Signal 25:1754–1761. http://dx.doi.org/10.1016/j.cellsig.2013.05.010.
   PubMed Web of Science ®Google Scholar
• Qiu H, Zappacosta F, Su W, Annan RS, Miller WT. 2005. Interaction between Brk kinase and insulin receptor substrate-4. Oncogene 24:5656–5664. http://dx.doi.org/10.1038/sj.onc.1208721.
   PubMedGoogle Scholar
• Gierut JJ, Mathur PS, Bie W, Han J, Tyner AL. 2012. Targeting protein tyrosine kinase 6 enhances apoptosis of colon cancer cells following DNA damage. Mol Cancer Ther 11:2311–2320. http://dx.doi.org/10.1158/1535-7163.MCT-12-0009.
   PubMedGoogle Scholar
• Schmidt M, Fernandez de Matto S, Van der Horst A, Klompmaker R, Kops GJ, Lam EW, Burgering BM, Medema RH. 2002. Cell cycle inhibition by FoxO forkhead transcription factors involves downregulation of cyclin D. Mol Cell Biol 22:7842–7852. http://dx.doi.org/10.1128/MCB.22.22.7842-7852.2002.
   PubMed Web of Science ®Google Scholar
• Baughn LB, Di Liberto M, Niesvizky R, Cho HJ, Jayabalan D, Lane J, Liu F, Chen-Kiang S. 2009. CDK2 phosphorylation of Smad2 disrupts TGF-beta transcriptional regulation in resistant primary bone marrow myeloma cells. J Immunol 182:1810–1817. http://dx.doi.org/10.4049/jimmunol.0713726.
   PubMedGoogle Scholar
• Fry DW, Harvey PJ, Keller PR, Elliott WL, Meade M, Trachet E, Albassam M, Zheng X, Leopold WR, Pryer NK, Toogood PL. 2004. Specific inhibition of cyclin-dependent kinase 4/6 by PD 0332991 and associated antitumor activity in human tumor xenografts. Mol Cancer Ther 3:1427–1438.
   PubMed Web of Science ®Google Scholar
• Finn RS, Dering J, Conklin D, Kalous O, Cohen DJ, Desai AJ, Ginther C, Atefi M, Chen I, Fowst C, Los G, Slamon DJ. 2009. PD 0332991, a selective cyclin D kinase 4/6 inhibitor, preferentially inhibits proliferation of luminal estrogen receptor-positive human breast cancer cell lines. Breast Cancer Res 11:R77. http://dx.doi.org/10.1186/bcr2419.
   PubMed Web of Science ®Google Scholar
• Mitchell PJ, Barker KT, Shipley J, Crompton MR. 1997. Characterisation and chromosome mapping of the human non receptor tyrsoine kinase gene, brk. Oncogene 15:1497–1502. http://dx.doi.org/10.1038/sj.onc.1201292.
   PubMed Web of Science ®Google Scholar
• Barker KT, Jackson LE, Crompton MR. 1997. BRK tyrosine kinase expression in a high proportion of human breast carcinomas. Oncogene 15:799–805. http://dx.doi.org/10.1038/sj.onc.1201241.
   PubMed Web of Science ®Google Scholar
• Ostrander JH, Daniel AR, Lofgren K, Kleer CG, Lange CA. 2007. Breast tumor kinase (protein tyrosine kinase 6) regulates heregulin-induced activation of ERK5 and p38 MAP kinases in breast cancer cells. Cancer Res 67:4199–4209. http://dx.doi.org/10.1158/0008-5472.CAN-06-3409.
   PubMed Web of Science ®Google Scholar
• Peng M, Emmadi R, Wang Z, Wiley EL, Gann PH, Khan S, Banerji N, McDonald W, Asztalos S, Pham TN, Tonetti DA, Tyner AL. 2014. PTK6/BRK is expressed in the normal mammary gland and activated at the plasma membrane in breast tumors. Oncotarget 5:6038–6048.
   PubMedGoogle Scholar
• Derry JJ, Richard S, Valderrama Carvajal H, Ye X, Vasioukhin V, Cochrane AW, Chen T, Tyner AL. 2000. Sik (BRK) phosphorylates Sam68 in the nucleus and negatively regulates its RNA binding ability. Mol Cell Biol 20:6114–6126. http://dx.doi.org/10.1128/MCB.20.16.6114-6126.2000.
   PubMed Web of Science ®Google Scholar
• Derry JJ, Prins GS, Ray V, Tyner AL. 2003. Altered localization and activity of the intracellular tyrosine kinase BRK/Sik in prostate tumor cells Oncogene 22:4212–4220. http://dx.doi.org/10.1038/sj.onc.1206465.
   Google Scholar
• Zheng Y, Gierut J, Wang Z, Miao J, Asara JM, Tyner AL. 2013. Protein tyrosine kinase 6 protects cells from anoikis by directly phosphorylating focal adhesion kinase and activating AKT. Oncogene 32:4304–4312. http://dx.doi.org/10.1038/onc.2012.427.
   PubMedGoogle Scholar
• Zheng Y, Asara JM, Tyner AL. 2012. Protein-tyrosine kinase 6 promotes peripheral adhesion complex formation and cell migration by phosphorylating p130 CRK-associated substrate. J Biol Chem 287:148–158. http://dx.doi.org/10.1074/jbc.M111.298117.
   PubMedGoogle Scholar
• Chan E, Nimnual AS. 2010. Deregulation of the cell cycle by breast tumor kinase (Brk). Int J Cancer 127:2723–2731. http://dx.doi.org/10.1002/ijc.25263.
   PubMedGoogle Scholar
• Blain SW, Scher HI, Cordon-Cardo C, Koff A. 2003. p27 as a target for cancer therapeutics. Cancer Cell 3:111–115. http://dx.doi.org/10.1016/S1535-6108(03)00026-6.
   PubMed Web of Science ®Google Scholar
• Borriello A, Bencivenga D, Criscuolo M, Caldarelli I, Cucciolla V, Tramontano A, Borgia A, Spina A, Oliva A, Naviglio S, Della Ragione F. 2011. Targeting p27Kip1 protein: its relevance in the therapy of human cancer. Expert Opin Ther Targets 15:677–693. http://dx.doi.org/10.1517/14728222.2011.561318.
   PubMed Web of Science ®Google Scholar
• Hulit J, Lee RJ, Russell RG, Pestell RG. 2002. ErbB-2-induced mammary tumor growth: the role of cyclin D1 and p27Kip1. Biochem Pharm 64:827–836. http://dx.doi.org/10.1016/S0006-2952(02)01145-0.
   PubMedGoogle Scholar
• Wander SA, Zhao D, Slingerland JM. 2011. p27: a barometer of signaling deregulation and potential predictor of response to targeted therapies. Clin Cancer Res 17:12–18. http://dx.doi.org/10.1158/1078-0432.CCR-10-0752.
   PubMed Web of Science ®Google Scholar
• Hukkelhoven E, Liu Y, Yeh N, Ciznadija D, Blain SW, Koff A. 2012. Tyrosine phosphorylation of the p21 cyclin-dependent kinase inhibitor facilitates the development of proneural glioma. J Biol Chem 287:38523–38530. http://dx.doi.org/10.1074/jbc.M112.366542.
   PubMedGoogle Scholar
• Dickson MA. 2014. Molecular pathways: CDK4 inhibitors for cancer therapy. Clin Cancer Res 20:3379–3383. http://dx.doi.org/10.1158/1078-0432.CCR-13-1551.
   PubMed Web of Science ®Google Scholar
• Cadoo KA, Gucalp A, Traina TA. 2014. Palbociclib: an evidence-based review of its potential in the treatment of breast cancer. Breast Cancer (Dove Med Press) 6:123–133. http://dx.doi.org/10.2147/BCTT.S46725.
   PubMedGoogle Scholar
• Heilmann AM, Perera RM, Ecker V, Nicolay BN, Bardeesy N, Benes CH, Dyson NJ. 2014. CDK4/6 and IGF1 receptor inhibitors synergize to suppress the growth of p16INK4A-deficient pancreatic cancers. Cancer Res 74:3947–3958. http://dx.doi.org/10.1158/0008-5472.CAN-13-2923.
   PubMed Web of Science ®Google Scholar
• Muraoka RS, Lenferink AEG, Law B, Hamilton E, Brantley DM, Roebuck LR, Arteaga CL. 2002. Erb2/Neu-induced cyclin D1-dependent transformation is accelerated in p27-haploinsufficient mammary epithelial cells but impaired in p27-null cells. Mol Cell Biol 22:2204–2219. http://dx.doi.org/10.1128/MCB.22.7.2204-2219.2002.
   PubMed Web of Science ®Google Scholar