A RNA interference screen identifies the protein phosphatase 2A subunit PR55γ as a stress-sensitive inhibitor of c-SRC

PLoS Genetics

Volumn 3, Issue 12, 2007, Pages 2381-2394

  Eichhorn, Pieter J A ^a   Creyghton, Menno P ^a   Wilhelmsen, Kevin ^a   Van Dam, Hans ^b   Bernards, René ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHOPROTEIN PHOSPHATASE INHIBITOR; PR 55 DELTA; PR55 GAMMA; SERINE; UNCLASSIFIED DRUG; CSK PROTEIN, HUMAN; ONCOPROTEIN; PHOSPHOPROTEIN PHOSPHATASE 2; PPP2R2C PROTEIN, HUMAN; PRIMER DNA; PROTEIN TYROSINE KINASE; STRESS ACTIVATED PROTEIN KINASE;

ARTICLE; DRUG INHIBITION; ENZYME ACTIVITY; GENE CONTROL; GENE REPRESSION; HUMAN; ONCOGENE; PHOSPHORYLATION; PROTEIN ANALYSIS; PROTEIN PROTEIN INTERACTION; RNA INTERFERENCE; ULTRAVIOLET IRRADIATION; AMINO ACID SUBSTITUTION; APOPTOSIS; CELL LINE; CHEMISTRY; DRUG ANTAGONISM; ENZYME ACTIVATION; GENETIC TRANSFECTION; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; RADIATION EXPOSURE; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; ULTRAVIOLET RADIATION;

AMINO ACID SUBSTITUTION; APOPTOSIS; BASE SEQUENCE; CELL LINE; DNA PRIMERS; ENZYME ACTIVATION; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MUTAGENESIS, SITE-DIRECTED; PHOSPHORYLATION; PROTEIN PHOSPHATASE 2; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS; RNA INTERFERENCE; SERINE; SIGNAL TRANSDUCTION; TRANSFECTION; ULTRAVIOLET RAYS;

EID: 37749015044     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.0030218     Document Type: Article

References (62)

1. Parsons SJ, Parsons JT (2004) Src family kinases, key regulators of signal transduction. Oncogene 23: 7906-7909.
2. Boggon TJ, Eck MJ (2004) Structure and regulation of Src family kinases. Oncogene 23: 7918-7927.
3. Zheng XM, Wang Y, Pallen CJ (1992) Cell transformation and activation of pp60c-src by overexpression of a protein tyrosine phosphatase. Nature 359: 336-339.
4. Bjorge JD, Pang A, Fujita DJ (2000) Identification of protein-tyrosine phosphatase 1B as the major tyrosine phosphatase activity capable of dephosphorylating and activating c-Src in several human breast cancer cell lines. J Biol Chem 275: 41439-41446.
5. Irby RB, Yeatman TJ (2000) Role of Src expression and activation in human cancer. Oncogene 19: 5636-5642.
6. Yeatman TJ (2004) A renaissance for SRC. Nat Rev Cancer 4: 470-480.
7. Biscardi JS, Ishizawar RC, Silva CM, Parsons SJ (2000) Tyrosine kinase signalling in breast cancer: epidermal growth factor receptor and c-Src interactions in breast cancer. Breast Cancer Res 2: 203-210.
8. Irby RB, Mao W, Coppola D, Kang J, Loubeau JM, et al. (1999) Activating SRC mutation in a subset of advanced human colon cancers. Nat Genet 21: 187-190.
9. Ishizawar R, Parsons SJ (2004) c-Src and cooperating partners in human cancer. Cancer Cell 6: 209-214.
10. Davis RJ (2000) Signal transduction by the JNK group of MAP kinases. Cell 103: 239-252.
11. Xie W, Herschman HR (1995) v-src induces prostaglandin synthase 2 gene expression by activation of the c-Jun N-terminal kinase and the c-Jun transcription factor. J Biol Chem 270: 27622-27628.
12. Chen K, Vita JA, Berk BC, Keaney JF Jr. (2001) c-Jun N-terminal kinase activation by hydrogen peroxide in endothelial cells involves SRC-dependent epidermal growth factor receptor transactivation. J Biol Chem 276: 16045-16050.
13. Devary Y, Gottlieb RA, Smeal T, Karin M (1992) The mammalian ultraviolet response is triggered by activation of Src tyrosine kinases. Cell 71: 1081-1091.
14. Sun Y, Yuan J, Liu H, Shi Z, Baker K, et al. (2004) Role of Gab1 in UV-induced c-Jun NH2-terminal kinase activation and cell apoptosis. Mol Cell Biol 24: 1531-1539.
15. Sontag E (2001) Protein phosphatase 2A: the Trojan Horse of cellular signaling. Cell Signal 13: 7-16.
16. Millward TA, Zolnierowicz S, Hemmings BA (1999) Regulation of protein kinase cascades by protein phosphatase 2A. Trends Biochem Sci 24: 186-191.
17. Janssens V, Goris J (2001) Protein phosphatase 2A: a highly regulated family of serine/threonine phosphatases implicated in cell growth and signalling. Biochem J 353: 417-439.
18. Hahn WC, Counter CM, Lundberg AS, Beijersbergen RL, Brooks MW, et al. (1999) Creation of human tumour cells with defined genetic elements. Nature 400: 464-468.
19. Pallas DC, Shahrik LK, Martin BL, Jaspers S, Miller TB, et al. (1990) Polyoma small and middle T antigens and SV40 small t antigen form stable complexes with protein phosphatase 2A. Cell 60: 167-176.
20. Suganuma M, Fujiki H, Furuya-Suguri H, Yoshizawa S, Yasumoto S, et al. (1990) Calyculin A, an inhibitor of protein phosphatases, a potent tumor promoter on CD-1 mouse skin. Cancer Res 50: 3521-3525.
21. Fujiki H, Suganuma M (1993) Tumor promotion by inhibitors of protein phosphatases 1 and 2A: the okadaic acid class of compounds. Adv Cancer Res 61: 143-194.
22. Bialojan C, Takai A (1988) Inhibitory effect of a marine-sponge toxin, okadaic acid, on protein phosphatases. Specificity and kinetics. Biochem J 256: 283-290.
23. Suganuma M, Fujiki H, Suguri H, Yoshizawa S, Hirota M, et al. (1988) Okadaic acid: an additional non-phorbol-12-tetradecanoate-13-acetate-type tumor promoter. Proc Natl Acad Sci U S A 85: 1768-1771.
24. Yang J, Wu J, Tan C, Klein PS (2003) PP2A:B56epsilon is required for Wnt/beta-catenin signaling during embryonic development. Development 130: 5569-5578.
25. Bajpai R, Makhijani K, Rao PR, Shashidhara LS (2004) Drosophila Twins regulates Armadillo levels in response to Wg/Wnt signal. Development 131: 1007-1016.
26. Brummelkamp TR, Nijman SM, Dirac AM, Bernards R (2003) Loss of the cylindromatosis tumour suppressor inhibits apoptosis by activating NF-kappaB. Nature 424: 797-801.
27. Nijman SM, Huang TT, Dirac AM, Brummelkamp TR, Kerkhoven RM, et al. (2005) The deubiquitinating enzyme USP1 regulates the Fanconi anemia pathway. Mol Cell 17: 331-339.
28. Brummelkamp TR, Bernards R, Agami R (2002) Stable suppression of tumorigenicity by virus-mediated RNA interference. Cancer Cell 2: 243-247.
29. Mullane KP, Ratnofsky M, Cullere X, Schaffhausen B (1998) Signaling from polyomavirus middle T and small T defines different roles for protein phosphatase 2A. Mol Cell Biol 18: 7556-7564.
30. Varfolomeev EE, Ashkenazi A (2004) Tumor necrosis factor: an apoptosis JuNKie? Cell 116: 491-497.
31. Yang D, Tournier C, Wysk M, Lu HT, Xu J, et al. (1997) Targeted disruption of the MKK4 gene causes embryonic death, inhibition of c-Jun NH2-terminal kinase activation, and defects in AP-1 transcriptional activity. Proc Natl Acad Sci U S A 94: 3004-3009.
32. Ory S, Zhou M, Conrads TP, Veenstra TD, Morrison DK (2003) Protein phosphatase 2A positively regulates Ras signaling by dephosphorylating KSR1 and Raf-1 on critical 14-3-3 binding sites. Curr Biol 13: 1356-1364.
33. Avdi NJ, Malcolm KC, Nick JA, Worthen GS (2002) A role for protein phosphatase-2A in p38 mitogen-activated protein kinase-mediated regulation of the c-Jun NH(2)-terminal kinase pathway in human neutrophils. J Biol Chem 277: 40687-40696.
34. Shanley TP, Vasi N, Denenberg A, Wong HR (2001) The serine/threonine phosphatase, PP2A: endogenous regulator of inflammatory cell signaling. J Immunol 166: 966-972.
35. Alvarado-Kristensson M, Andersson T (2005) Protein phosphatase 2A regulates apoptosis in neutrophils by dephosphorylating both p38 MAPK and its substrate caspase 3. J Biol Chem 280: 6238-6244.
36. Courtneidge SA, Smith AE (1983) Polyoma virus transforming protein associates with the product of the c-src cellular gene. Nature 303: 435-439.
37. Courtneidge SA (1985) Activation of the pp60c-src kinase by middle T antigen binding or by dephosphorylation. Embo J 4: 1471-1477.
38. Walter G, Ruediger R, Slaughter C, Mumby M (1990) Association of protein phosphatase 2A with polyoma virus medium tumor antigen. Proc Natl Acad Sci U S A 87: 2521-2525.
39. Kitagawa D, Tanemura S, Ohata S, Shimizu N, Seo J, et al. (2002) Activation of extracellular signal-regulated kinase by ultraviolet is mediated through Src-dependent epidermal growth factor receptor phosphorylation. Its implication in an anti-apoptotic function. J Biol Chem 277: 366-371.
40. Shangary S, Lerner EC, Zhan Q, Corey SJ, Smithgall TE, et al. (2003) Lyn regulates the cell death response to ultraviolet radiation through c-Jun N terminal kinase-dependent Fas ligand activation. Exp Cell Res 289: 67-76.
41. Roche S, Koegl M, Barone MV, Roussel MF, Courtneidge SA (1995) DNA synthesis induced by some but not all growth factors requires Src family protein tyrosine kinases. Mol Cell Biol 15: 1102-1109.
42. Minden A, Lin A, Claret FX, Abo A, Karin M (1995) Selective activation of the JNK signaling cascade and c-Jun transcriptional activity by the small GTPases Rac and Cdc42Hs. Cell 81: 1147-1157.
43. Yokoyama N, Miller WT (2001) Inhibition of Src by direct interaction with protein phosphatase 2A. FEBS Lett 505: 460-464.
44. Ogris E, Mudrak I, Mak E, Gibson D, Pallas DC (1999) Catalytically inactive protein phosphatase 2A can bind to polyomavirus middle tumor antigen and support complex formation with pp60(c-src). J Virol 73: 7390-7398.
45. Chackalaparampil I, Bagrodia S, Shalloway D (1994) Tyrosine dephosphorylation of pp60c-src is stimulated by a serine/threonine phosphatase inhibitor. Oncogene 9: 1947-1955.
46. Champagne C, Landry MC, Gingras MC, Lavoie JN (2004) Activation of adenovirus type 2 early region 4 ORF4 cytoplasmic death function by direct binding to Src kinase domain. J Biol Chem 279: 25905-25915.
47. Glover HR, Brewster CE, Dilworth SM (1999) Association between srckinases and the polyoma virus oncogene middle T-antigen requires PP2A and a specific sequence motif. Oncogene 18: 4364-4370.
48. Pallas DC, Fu H, Haehnel LC, Weller W, Collier RJ, et al. (1994) Association of polyomavirus middle tumor antigen with 14-3-3 proteins. Science 265: 535-537.
49. Moyers JS, Bouton AH, Parsons SJ (1993) The sites of phosphorylation by protein kinase C and an intact SH2 domain are required for the enhanced response to beta-adrenergic agonists in cells overexpressing c-src. Mol Cell Biol 13: 2391-2400.
50. Thevenin C, Kim SJ, Kehrl JH (1991) Inhibition of protein phosphatases by okadaic acid induces AP1 in human T cells. J Biol Chem 266: 9363-9366.
51. Al-Murrani SW, Woodgett JR, Damuni Z (1999) Expression of I2PP2A, an inhibitor of protein phosphatase 2A, induces c-Jun and AP-1 activity. Biochem J 341 ( Pt 2): 293-298.
52. Shtrichman R, Sharf R, Barr H, Dobner T, Kleinberger T (1999) Induction of apoptosis by adenovirus E4orf4 protein is specific to transformed cells and requires an interaction with protein phosphatase 2A. Proc Natl Acad Sci U S A 96: 10080-10085.
53. Roopchand DE, Lee JM, Shahinian S, Paquette D, Bussey H, et al. (2001) Toxicity of human adenovirus E4orf4 protein in Saccharomyces cerevisiae results from interactions with the Cdc55 regulatory B subunit of PP2A. Oncogene 20: 5279-5290.
54. Sandilands E, Cans C, Fincham VJ, Brunton VG, Mellor H, et al. (2004) RhoB and actin polymerization coordinate Src activation with endosomemediated delivery to the membrane. Dev Cell 7: 855-869.
55. Schmitt JM, Stork PJ (2002) PKA phosphorylation of Src mediates cAMP's inhibition of cell growth via Rap1. Mol Cell 9: 85-94.
56. Liebenhoff U, Greinacher A, Presek P (1994) The protein tyrosine kinase pp60c-src is activated upon platelet stimulation. Cell Mol Biol (Noisy-legrand) 40: 645-652.
57. Guo CY, Brautigan DL, Larner JM (2002) ATM-dependent dissociation of B55 regulatory subunit from nuclear PP2A in response to ionizing radiation. J Biol Chem 277: 4839-4844.
58. Brummelkamp TR, Bernards R, Agami R (2002) A system for stable expression of short interfering RNAs in mammalian cells. Science 296: 550-553.
59. Gonzalez L, Agullo-Ortuno MT, Garcia-Martinez JM, Calcabrini A, Gamallo C, et al. (2006) Role of c-Src in human MCF7 breast cancer cell tumorigenesis. J Biol Chem 281: 20851-20864.
60. van der Eb AJ, Graham FL (1980) Assay of transforming activity of tumor virus DNA. Methods Enzymol 65: 826-839.
61. van der Geer P, Hunter T (1993) Mutation of Tyr697, a GRB2-binding site, and Tyr721, a PI 3-kinase binding site, abrogates signal transduction by the murine CSF-1 receptor expressed in Rat-2 fibroblasts. Embo J 12: 5161-5172.
62. Wilhelmsen K, Burkhalter S, van der Geer P (2002) C-Cbl binds the CSF-1 receptor at tyrosine 973, a novel phosphorylation site in the receptor's carboxy-terminus. Oncogene 21: 1079-1089.