The alternative splice variant of protein tyrosine kinase 6 negatively regulates growth and enhances PTK6-mediated inhibition of β-catenin

PLoS ONE

Volumn 6, Issue 3, 2011, Pages

  Brauer, Patrick M ^a   Zheng, Yu ^a   Evans, Mark D ^a   Dominguez Brauer, Carmen ^a   Peehl, Donna M ^b   Tyner, Angela L ^a  

^a UNIVERSITY OF ILLINOIS   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; CYCLIN D1; MYC PROTEIN; PROTEIN SAM68; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE 6; RNA; TETRACYCLINE; UNCLASSIFIED DRUG; MESSENGER RNA; PTK6 PROTEIN, HUMAN; REPRESSOR PROTEIN; T CELL FACTOR PROTEIN; TUMOR PROTEIN;

ALTERNATIVE RNA SPLICING; ARTICLE; CANCER CELL CULTURE; CELL PROLIFERATION; CELLULAR DISTRIBUTION; COLON CANCER; COLONY FORMATION; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME REGULATION; ENZYME SUBSTRATE; GENETIC TRANSCRIPTION; GROWTH REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; NUCLEOTIDE SEQUENCE; PROSTATE CANCER; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; CELL NUCLEUS; COLON TUMOR; DRUG ANTAGONISM; DRUG SCREENING; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; PHOSPHORYLATION; PROSTATE TUMOR; TUMOR CELL LINE;

ALTERNATIVE SPLICING; BETA CATENIN; CELL LINE, TUMOR; CELL NUCLEUS; CELL PROLIFERATION; COLONIC NEOPLASMS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; NEOPLASM PROTEINS; PHOSPHORYLATION; PROSTATIC NEOPLASMS; PROTEIN-TYROSINE KINASES; REPRESSOR PROTEINS; RNA, MESSENGER; TCF TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TUMOR STEM CELL ASSAY;

EID: 79953316023     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0014789     Document Type: Article

References (64)

1. Brauer PM, Tyner AL, (2010) Building a better understanding of the intracellular tyrosine kinase PTK6- BRK by BRK. Biochim Biophys Acta 1806: 66-73.
2. 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.
3. Lee ST, Strunk KM, Spritz RA, (1993) A survey of protein tyrosine kinase mRNAs expressed in normal human melanocytes. Oncogene 8: 3403-3410.
4. Mitchell PJ, Barker KT, Martindale JE, Kamalati T, Lowe PN, et al. (1994) Cloning and characterisation of cDNAs encoding a novel non-receptor tyrosine kinase, brk, expressed in human breast tumours. Oncogene 9: 2383-2390.
5. Siyanova EY, Serfas MS, Mazo IA, Tyner AL, (1994) Tyrosine kinase gene expression in the mouse small intestine. Oncogene 9: 2053-2057.
6. Vasioukhin V, Serfas MS, Siyanova EY, Polonskaia M, Costigan VJ, et al. (1995) A novel intracellular epithelial cell tyrosine kinase is expressed in the skin and gastrointestinal tract. Oncogene 10: 349-357.
7. Llor X, Serfas MS, Bie W, Vasioukhin V, Polonskaia M, et al. (1999) BRK/Sik expression in the gastrointestinal tract and in colon tumors. Clin Cancer Res 5: 1767-1777.
8. Lee H, Kim M, Lee KH, Kang KN, Lee ST, (1998) Exon-intron structure of the human PTK6 gene demonstrates that PTK6 constitutes a distinct family of non-receptor tyrosine kinase. Mol Cells 8: 401-407.
9. Chen T, Boisvert FM, Bazett-Jones DP, Richard S, (1999) A role for the GSG domain in localizing Sam68 to novel nuclear structures in cancer cell lines. Mol Biol Cell 10: 3015-3033.
10. Petro BJ, Tan RC, Tyner AL, Lingen MW, Watanabe K, (2004) Differential expression of the non-receptor tyrosine kinase BRK in oral squamous cell carcinoma and normal oral epithelium. Oral Oncol 40: 1040-1047.
11. 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.
12. Wang TC, Jee SH, Tsai TF, Huang YL, Tsai WL, et al. (2005) Role of breast tumour kinase in the in vitro differentiation of HaCaT cells. Br J Dermatol 153: 282-289.
13. Kasprzycka M, Majewski M, Wang ZJ, Ptasznik A, Wysocka M, et al. (2006) Expression and oncogenic role of Brk (PTK6/Sik) protein tyrosine kinase in lymphocytes. Am J Pathol 168: 1631-1641.
14. 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.
15. Haegebarth A, Bie W, Yang R, Crawford SE, Vasioukhin V, et al. (2006) Protein tyrosine kinase 6 negatively regulates growth and promotes enterocyte differentiation in the small intestine. Mol Cell Biol 26: 4949-4957.
16. Haegebarth A, Nunez R, Tyner AL, (2005) The intracellular tyrosine kinase Brk sensitizes non-transformed cells to inducers of apoptosis. Cell Cycle 4: 1239-1246.
17. Haegebarth A, Perekatt AO, Bie W, Gierut JJ, Tyner AL, (2009) Induction of protein tyrosine kinase 6 in mouse intestinal crypt epithelial cells promotes DNA damage-induced apoptosis. Gastroenterology 137: 945-954.
18. Barker KT, Jackson LE, Crompton MR, (1997) BRK tyrosine kinase expression in a high proportion of human breast carcinomas. Oncogene 15: 799-805.
19. 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.
20. Harvey AJ, Pennington CJ, Porter S, Burmi RS, Edwards DR, et al. (2009) Brk protects breast cancer cells from autophagic cell death induced by loss of anchorage. Am J Pathol 175: 1226-1234.
21. Schmandt RE, Bennett M, Clifford S, Thornton A, Jiang F, et al. (2006) The BRK tyrosine kinase is expressed in high-grade serous carcinoma of the ovary. Cancer Biol Ther 5: 1136-1141.
22. Ostrander JH, Daniel AR, Lange CA, (2010) Brk/PTK6 signaling in normal and cancer cell models. Curr Opin Pharmacol.
23. Palka-Hamblin HL, Gierut JJ, Bie W, Brauer PM, Zheng Y, et al. (2010) Identification of {beta}-catenin as a target of the intracellular tyrosine kinase PTK6. J Cell Sci 123: 236-245.
24. Ie Kim H, Lee ST, (2009) Oncogenic functions of PTK6 are enhanced by its targeting to plasma membrane but abolished by its targeting to nucleus. J Biochem 146: 133-139.
25. Brauer PM, Zheng Y, Wang L, Tyner AL, (2010) Cytoplasmic retention of protein tyrosine kinase 6 promotes growth of prostate tumor cells. Cell Cycle 9: 4190-4199.
26. Beildeck ME, Gelmann EP, Byers SW, (2010) Cross-regulation of signaling pathways: an example of nuclear hormone receptors and the canonical Wnt pathway. Exp Cell Res 316: 1763-1772.
27. Robinson DR, Zylstra CR, Williams BO, (2008) Wnt signaling and prostate cancer. Curr Drug Targets 9: 571-580.
28. Wang G, Wang J, Sadar MD, (2008) Crosstalk between the androgen receptor and beta-catenin in castrate-resistant prostate cancer. Cancer Res 68: 9918-9927.
29. Playford MP, Bicknell D, Bodmer WF, Macaulay VM, (2000) Insulin-like growth factor 1 regulates the location, stability, and transcriptional activity of beta-catenin. Proc Natl Acad Sci U S A 97: 12103-12108.
30. Verras M, Sun Z, (2005) Beta-catenin is involved in insulin-like growth factor 1-mediated transactivation of the androgen receptor. Mol Endocrinol 19: 391-398.
31. Yang F, Li X, Sharma M, Sasaki CY, Longo DL, et al. (2002) Linking beta-catenin to androgen-signaling pathway. J Biol Chem 277: 11336-11344.
32. Wai PY, Kuo PC, (2008) Osteopontin: regulation in tumor metastasis. Cancer Metastasis Rev 27: 103-118.
33. Robertson BW, Chellaiah MA, (2010) Osteopontin induces beta-catenin signaling through activation of Akt in prostate cancer cells. Exp Cell Res 316: 1-11.
34. Essers MA, de Vries-Smits LM, Barker N, Polderman PE, Burgering BM, et al. (2005) Functional interaction between beta-catenin and FOXO in oxidative stress signaling. Science 308: 1181-1184.
35. Jin T, George Fantus I, Sun J, (2008) Wnt and beyond Wnt: multiple mechanisms control the transcriptional property of beta-catenin. Cell Signal 20: 1697-1704.
36. Pasco MY, Catoire H, Parker JA, Brais B, Rouleau GA, et al. (2010) Cross-talk between canonical Wnt signaling and the sirtuin-FoxO longevity pathway to protect against muscular pathology induced by mutant PABPN1 expression in C. elegans. Neurobiol Dis.
37. Irie HY, Shrestha Y, Selfors LM, Frye F, Iida N, et al. PTK6 regulates IGF-1-induced anchorage-independent survival. PLoS One 5: e11729.
38. Qiu H, Zappacost F, Su W, Annan RS, Miller WT, (2005) Interaction between Brk kinase and insulin receptor substrate-4. Oncogene 24: 5656-5664.
39. Chakraborty G, Jain S, Kundu GC, (2008) Osteopontin promotes vascular endothelial growth factor-dependent breast tumor growth and angiogenesis via autocrine and paracrine mechanisms. Cancer Res 68: 152-161.
40. Zheng Y, Peng M, Wang Z, Asara JM, Tyner AL, (2010) Protein tyrosine kinase 6 directly phosphorylates AKT and promotes AKT activation in response to epidermal growth factor. Mol Cell Biol 30: 4280-4292.
41. Zhang P, Ostrander JH, Faivre EJ, Olsen A, Fitzsimmons D, et al. (2005) Regulated association of protein kinase b/akt with breast tumor kinase. J Biol Chem 280: 1982-1991.
42. Chan E, Nimnual AS, (2010) Deregulation of the cell cycle by breast tumor kinase (Brk). Int J Cancer.
43. Hoogeboom D, Essers MA, Polderman PE, Voets E, Smits LM, et al. (2008) Interaction of FOXO with beta-catenin inhibits beta-catenin/T cell factor activity. J Biol Chem 283: 9224-9230.
44. Manolagas SC, Almeida M, (2007) Gone with the Wnts: beta-catenin, T-cell factor, forkhead box O, and oxidative stress in age-dependent diseases of bone, lipid, and glucose metabolism. Mol Endocrinol 21: 2605-2614.
45. Takahashi-Yanaga F, Kahn M, Targeting Wnt signaling: can we safely eradicate cancer stem cells? Clin Cancer Res 16: 3153-3162.
46. Mitchell PJ, Barker KT, Shipley J, Crompton MR, (1997) Characterisation and chromosome mapping of the human non receptor tyrosine kinase gene, brk. Oncogene 15: 1497-1502.
47. Qiu H, Miller WT, (2002) Regulation of the nonreceptor tyrosine kinase Brk by autophosphorylation and by autoinhibition. J Biol Chem 277: 34634-34641.
48. Kim HI, Jung J, Lee ES, Kim YC, Lee WP, et al. (2007) Molecular dissection of the interaction between the SH3 domain and the SH2-Kinase Linker region in PTK6. Biochem Biophys Res Commun 362: 829-834.
49. Ko S, Ahn KE, Lee YM, Ahn HC, Lee W, (2009) Structural basis of the auto-inhibition mechanism of nonreceptor tyrosine kinase PTK6. Biochem Biophys Res Commun 384: 236-242.
50. Derry JJ, Richard S, Valderrama Carvajal H, Ye X, Vasioukhin V, et al. (2000) Sik (BRK) phosphorylates Sam68 in the nucleus and negatively regulates its RNA binding ability. Mol Cell Biol 20: 6114-6126.
51. Veeman MT, Axelrod JD, Moon RT, (2003) A second canon. Functions and mechanisms of beta-catenin-independent Wnt signaling. Dev Cell 5: 367-377.
52. MacDonald BT, Tamai K, He X, (2009) Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev Cell 17: 9-26.
53. Haegebarth A, Heap D, Bie W, Derry JJ, Richard S, et al. (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: 54398-54404.
54. Lukong KE, Huot ME, Richard S, (2009) BRK phosphorylates PSF promoting its cytoplasmic localization and cell cycle arrest. Cell Signal 21: 1415-1422.
55. Matter N, Herrlich P, Konig H, (2002) Signal-dependent regulation of splicing via phosphorylation of Sam68. Nature 420: 691-695.
56. Cohen CD, Doran PP, Blattner SM, Merkle M, Wang GQ, et al. (2005) Sam68-like mammalian protein 2, identified by digital differential display as expressed by podocytes, is induced in proteinuria and involved in splice site selection of vascular endothelial growth factor. J Am Soc Nephrol 16: 1958-1965.
57. Greco-Stewart VS, Thibault CS, Pelchat M, (2006) Binding of the polypyrimidine tract-binding protein-associated splicing factor (PSF) to the hepatitis delta virus RNA. Virology 356: 35-44.
58. Paronetto MP, Cappellari M, Busa R, Pedrotti S, Vitali R, et al. (2010) Alternative Splicing of the Cyclin D1 Proto-Oncogene Is Regulated by the RNA-Binding Protein Sam68. Cancer Res 70: 229-239.
59. Brignatz C, Paronetto MP, Opi S, Cappellari M, Audebert S, et al. (2009) Alternative splicing modulates autoinhibition and SH3 accessibility in the Src kinase Fyn. Mol Cell Biol 29: 6438-6448.
60. Hayward SW, Dahiya R, Cunha GR, Bartek J, Deshpande N, et al. (1995) Establishment and characterization of an immortalized but non-transformed human prostate epithelial cell line: BPH-1. In Vitro Cell Dev Biol Anim 31: 14-24.
61. Peehl DM, (1992) Culture of human prostatic epithelial cells. In: Culture of Epithelial Cells; RF, editors. Wiley-Liss New York pp. 159-180.
62. Peehl DM, (2005) Primary cell cultures as models of prostate cancer development. Endocr Relat Cancer 12: 19-47.
63. Rasband WS, (1997) Bethesda, Maryland, USA ImageJ. U S National Institutes of Health http://imagej.nih.gov/ij/.
64. Dominguez-Brauer C, Chen YJ, Brauer PM, Pimkina J, Raychaudhuri P, (2009) ARF stimulates XPC to trigger nucleotide excision repair by regulating the repressor complex of E2F4. EMBO Rep 10: 1036-1042.