RAKing in AKT: A tumor suppressor function for the intracellular tyrosine kinase FRK

Cell Cycle

Volumn 8, Issue 17, 2009, Pages 2728-2732

  Brauer, Patrick M ^a   Tyner, Angela L ^a  

^a UNIVERSITY OF ILLINOIS   (United States)

Author keywords

AKT; BRK; FRK; PTEN; PTK6; RAK; Tumor suppressor; Tyrosine kinase

Indexed keywords

PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; PROTEIN KINASE FYN; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE 6; UBIQUITIN PROTEIN LIGASE NEDD4; UNCLASSIFIED DRUG;

APOPTOSIS; ASSOCIATION; BREAST CELL; BREAST TUMOR; CANCER CELL; CELL DIFFERENTIATION; EPITHELIUM CELL; HUMAN; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; REVIEW;

EID: 69749083045     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.8.17.9389     Document Type: Review

References (65)

1. Hunter T. Tyrosine phosphorylation: thirty years and counting. Curr Opin Cell Biol 2009; 21:140-146
2. Pawson T, Kofler M. Kinome signaling through regulated protein-protein interactions in normal and cancer cells. Curr Opin Cell Biol 2009; 21:147-153
3. Serfas MS, Tyner AL. Brk, Srm, Frk and Src42A form a distinct family of intracellular Src-like tyrosine kinases. Oncol Res 2003; 13:409-419
4. D'Aniello S, Irimia M, Maeso I, Pascual-Anaya J, Jimenez-Delgado S, Bertrand S, et al. Gene expansion and retention leads to a diverse tyrosine kinase superfamily in amphioxus. Mol Biol Evol 2008; 25:1841-1854
5. Thuveson M, Albrecht D, Zurcher G, Andres AC, Ziemiecki A. iyk, a novel intracellular protein tyrosine kinase differentially expressed in the mouse mammary gland and intestine [published erratum appears in Biochem Biophys Res Commun 1995; 211:1100]. Biochem Biophys Res Commun 1995; 209:582-589
6. Craven RJ, Cance WG, Liu ET. The nuclear tyrosine kinase Rak associates with the retinoblastoma protein pRb. Cancer Res 1995; 55:3969-3972
7. Cance WG, Craven RJ, Bergman M, Xu L, Aitalo K, Liu ET. Rak, a novel nuclear tyrosine kinase expressed in epithelial cells. Cell Growth Diff 1994; 5:1347-1355 (Pubitemid 24381523)
8. 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; 20:6114-6126 (Pubitemid 30613059)
9. 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; 22:4212-4220 (Pubitemid 36876242)
10. 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; 279:54398-54404 (Pubitemid 40053179)
11. Cance WG, Craven RJ, Weiner TM, Liu ET. Novel protein kinases expresed in human breast cancer. Int J Cancer 1993; 54:571-577
12. Lee ST, Strunk KM, Spritz RA. A survey of protein tyrosine kinase mRNAs expressed in normal human melanocytes. Oncogene 1993; 8:3403-3410 (Pubitemid 23342639)
13. Lee J, Wang Z, Luoh S-M, Wood WL, Scadden DT. Cloning of FRK, a novel human intracellular SRC-like tyrosine kinase-encoding gene. Gene 1994; 138:247-251 (Pubitemid 24087586)
14. Sunitha I, Avigan MI. A newly identified tyrosine kinase is preferentially expressed in the gastrointestinal tract. Biochim Biophys Acta 1994; 1221:348-352 (Pubitemid 24130879)
15. Sunitha I, Avigan MI. The apical membranes of maturing gut columnar epithelial cells contain the enzymatically active form of a newly identified fyn-related tyrosine kinase. Oncogene 1996; 13:547-559 (Pubitemid 26283851)
16. Oberg-Welsh C, Welsh M. Cloning of BSK, a murine FRK homologue with a specific pattern of tissue distribution. Gene 1995; 152:239-242
17. Sunitha I, Shen R, McKillop IH, Lee JH, Resau J, Avigan M. A src-related kinase in the brush border membranes of gastrointestinal cells is regulated by c-met. Exp Cell Res 1999; 250:86-98. (Pubitemid 29391573)
18. Berclaz G, Altermatt HJ, Rohrbach V, Dreher E, Ziemiecki A, Andres AC. Hormone-dependent nuclear localization of the tyrosine kinase iyk in the normal human breast epithelium and loss of expression during carcinogenesis. Int J Cancer 2000; 85:889-894 (Pubitemid 30131483)
19. Oberg-Welsh C, Anneren C, Welsh M. Mutation of C-terminal tyrosine residues Y497/Y504 of the Src-family member Bsk/Iyk decreases NIH3T3 cell proliferation. Growth Factors 1998; 16:111-124 (Pubitemid 29056120)
20. Akerblom B, Anneren C, Welsh M. A role of FRK in regulation of embryonal pancreatic beta cell formation. Mol Cell Endocrinol 2007; 270:73-78 (Pubitemid 46670553)
21. Anneren C, Reedquist KA, Bos JL, Welsh M. GTK, a Src-related tyrosine kinase, induces nerve growth factor-independent neurite outgrowth in PC12 cells through activation of the Rap1 pathway. Relationship to Shb tyrosine phosphorylation and elevated levels of focal adhesion kinase. J Biol Chem 2000; 275:29153-29161 (Pubitemid 30704258)
22. Anneren C, Lindholm CK, Kriz V, Welsh M. The FRK/RAK-SHB signaling cascade: a versatile signal-transduction pathway that regulates cell survival, differentiation and proliferation. Curr Mol Med 2003; 3:313-324 (Pubitemid 36621789)
23. Anneren C, Welsh M. Increased cytokine-induced cytotoxicity of pancreatic islet cells from transgenic mice expressing the Src-like tyrosine kinase GTK. Mol Med 2001; 7:301-310 (Pubitemid 33701980)
24. Anneren C, Welsh M, Jansson L. Glucose intolerance and reduced islet blood flow in transgenic mice expressing the FRK tyrosine kinase under the control of the rat insulin promoter. Am J Physiol Endocrinol Metab 2007; 292:1183-1190 (Pubitemid 46536519)
25. Anneren C. Dual role of the tyrosine kinase GTK and the adaptor protein SHB in beta-cell growth: enhanced beta-cell replication after 60% pancreatectomy and increased sensitivity to streptozotocin. J Endocrinol 2002; 172:145-153 (Pubitemid 34082953)
26. Welsh M, Welsh C, Ekman M, Dixelius J, Hagerkvist R, Anneren C, et al. The tyrosine kinase FRK/RAK participates in cytokine-induced islet cell cytotoxicity. Biochem J 2004; 382:261-268 (Pubitemid 39141590)
27. Meyer T, Xu L, Chang J, Liu ET, Craven RJ, Cance WG. Breast cancer cell line proliferation blocked by the Src-related Rak tyrosine kinase. Int J Cancer 2003; 104:139-146 (Pubitemid 36249787)
28. Anneren C, Welsh M. Role of the Bsk/Iyk non-receptor tyrosine kinase for the control of growth and hormone production in RINm5F cells. Growth Factors 2000; 17:233-247 (Pubitemid 30219333)
29. Myers MP, Stolarov JP, Eng C, Li J, Wang SI, Wigler MH, et al. P-TEN, the tumor suppressor from human chromosome 10q23, is a dual-specificity phosphatase. Proc Natl Acad Sci USA 1997; 94:9052-9057 (Pubitemid 27357780)
30. Li J, Yen C, Liaw D, Podsypanina K, Bose S, Wang SI, et al. PTEN, a putative protein tyrosine phosphatase gene mutated in human brain, breast and prostate cancer. Science 1997; 275:1943-1947 (Pubitemid 27148818)
31. Carracedo A, Pandolfi PP. The PTEN-PI3K pathway: of feedbacks and cross-talks. Oncogene 2008; 27:5527-41.
32. Trotman LC, Wang X, Alimonti A, Chen Z, Teruya-Feldstein J, Yang H, et al. Ubiquitination regulates PTEN nuclear import and tumor suppression. Cell 2007; 128:141-156 (Pubitemid 46048885)
33. Yin Y, Shen WH. PTEN: a new guardian of the genome. Oncogene 2008; 27:5443-5453
34. Planchon SM, Waite KA, Eng C. The nuclear affairs of PTEN. J Cell Sci 2008; 121:249-253
35. Yim EK, Peng G, Dai H, Hu R, Li K, Lu Y, et al. Rak functions as a tumor suppressor by regulating PTEN protein stability and function. Cancer Cell 2009; 15:304-314
36. Wang X, Trotman LC, Koppie T, Alimonti A, Chen Z, Gao Z, et al. NEDD4-1 is a proto-oncogenic ubiquitin ligase for PTEN. Cell 2007; 128:129-139 (Pubitemid 46048884)
37. Fouladkou F, Landry T, Kawabe H, Neeb A, Lu C, Brose N, et al. The ubiquitin ligase Nedd4-1 is dispensable for the regulation of PTEN stability and localization. Proc Natl Acad Sci USA 2008; 105:8585-8590 (Pubitemid 351987724)
38. Wang X, Jiang X. Post-translational regulation of PTEN. Oncogene 2008; 27:5454-5463
39. Chandrasekharan S, Qiu TH, Alkharouf N, Brantley K, Mitchell JB, Liu ET. Characterization of mice deficient in the Src family nonreceptor tyrosine kinase Frk/rak. Mol Cell Biol 2002; 22:5235-5247 (Pubitemid 34700712)
40. 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; 9:2383-2390 (Pubitemid 24228691)
41. Siyanova EY, Serfas MS, Mazo IA, Tyner AL. Tyrosine kinase gene expression in the mouse small intestine. Oncogene 1994; 9:2053-2057 (Pubitemid 24194173)
42. Vasioukhin V, Serfas MS, Siyanova EY, Polonskaia M, Costigan VJ, Liu B, et al. A novel intracellular epithelial cell tyrosine kinase is expressed in the skin and gastrointestinal tract. Oncogene 1995; 10:349-357
43. Haegebarth A, Bie W, Yang R, Crawford SE, Vasioukhin V, Fuchs E, et al. Protein tyrosine kinase 6 negatively regulates growth and promotes enterocyte differentiation in the small intestine. Mol Cell Biol 2006; 26:4949-4957 (Pubitemid 43955811)
44. Vasioukhin V, Tyner AL. A role for the epithelial-cell-specific tyrosine kinase Sik during keratinocyte differentiation. Proc Natl Acad Sci USA 1997; 94:14477-14482 (Pubitemid 28041399)
45. Wang TC, Jee SH, Tsai TF, Huang YL, Tsai WL, Chen RH. Role of breast tumour kinase in the in vitro differentiation of HaCaT cells. Br J Dermatol 2005; 153:282-289
46. Haegebarth A, Nunez R, Tyner AL. The intracellular tyrosine kinase Brk sensitizes non-transformed cells to inducers of apoptosis. Cell Cycle 2005; 4:1239-1246 (Pubitemid 41365396)
47. Haegebarth A, Perekatt AO, Bie W, Gierut JJ, Tyner AL. Induction of protein tyrosine kinase 6 in mouse intestinal crypt epithelial cells promotes DNA-damage induced apoptosis. Gastroenterology 2009.
48. Zhang P, Ostrander JH, Faivre EJ, Olsen A, Fitzsimmons D, Lange CA. Regulated association of protein kinase B/Akt with breast tumor kinase. J Biol Chem 2005; 280:1982-1991
49. Kim HI, Lee ST. Oncogenic Functions of PTK6 Are enhanced by Its targeting to plasma membrane but abolished by its targeting to nucleus. J Biochem 2009.
50. Martin-Belmonte F, Gassama A, Datta A, Yu W, Rescher U, Gerke V, et al. PTEN-mediated apical segregation of phosphoinositides controls epithelial morphogenesis through Cdc42. Cell 2007; 128:383-397 (Pubitemid 46123512)
51. Barker KT, Jackson LE, Crompton MR. BRK tyrosine kinase expression in a high proportion of human breast carcinomas. Oncogene 1997; 15:799-805.
52. Llor X, Serfas MS, Bie W, Vasioukhin V, Polonskaia M, Derry J, et al. BRK/Sik expression in the gastrointestinal tract and in colon tumors. Clin Cancer Res 1999; 5:1767-1777 (Pubitemid 29334458)
53. 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; 67:4199-4209 (Pubitemid 46815066)
54. Park SH, Lee KH, Kim H, Lee ST. Assignment of the human PTK6 gene encoding a non-receptor protein tyrosine kinase to 20q13.3 by fluorescence in situ hybridization. Cytogenet Cell Genet 1997; 77:271-272 (Pubitemid 27370947)
55. Born M, Quintanilla-Fend L, Braselmann H, Reich U, Richter M, Hutzler P, et al. Simultaneous overexpression of the Her2/neu and PTK6 tyrosine kinases in archival invasive ductal breast carcinomas. J Pathol 2005; 205:592-596 (Pubitemid 40514832)
56. 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; 105:12463-12468
57. Kamalati T, Jolin HE, Fry MJ, Crompton MR. 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 2000; 19:5471-5476 (Pubitemid 32000914)
58. 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; 22:5006-5010
59. 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; 24:10558-10572
60. 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; 9:79.
61. Sheng ZM, Marchetti A, Buttitta F, Champeme MH, Campani D, Bistocchi M, et al. Multiple regions of chromosome 6q affected by loss of heterozygosity in primary human breast carcinomas. Br J Cancer 1996; 73:144-147 (Pubitemid 26028326)
62. Armistead PM, Thorp HH. Electrochemical detection of gene expression in tumor samples: overexpression of Rak nuclear tyrosine kinase. Bioconjug Chem 2002; 13:172-176
63. Hosoya N, Qiao Y, Hangaishi A, Wang L, Nannya Y, Sanada M, et al. Identification of a SRC-like tyrosine kinase gene, FRK, fused with ETV6 in a patient with acute myelogenous leukemia carrying a t(6;12)(q21;p13) translocation. Genes Chromosomes Cancer 2005; 42:269-279 (Pubitemid 40171191)
64. Anneren C, Welsh M. GTK tyrosine kinase-induced alteration of IRS-protein signalling in insulin producing cells. Mol Med 2002; 8:705-713 (Pubitemid 36337497)
65. 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. (Pubitemid 36008504)