The Tumor Suppressor PP2A Aβ Regulates the RalA GTPase

Cell

Volumn 129, Issue 5, 2007, Pages 969-982

  Sablina, Anna A ^a   Chen, Wen ^a,d   Arroyo, Jason D ^a,b   Corral, Laura ^a   Hector, Melissa ^a   Bulmer, Sara E ^a   DeCaprio, James A ^a   Hahn, William C ^a,b,c  

^a DANA FARBER CANCER INSTITUTE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d SUN YAT SEN UNIVERSITY   (China)

Author keywords

HUMDISEASE; PROTEINS

Indexed keywords

GUANOSINE TRIPHOSPHATASE; PHOSPHOPROTEIN PHOSPHATASE 2A; PHOSPHOPROTEIN PHOSPHATASE 2A ABETA; PROTEIN; PROTEIN RAIA; SERINE; UNCLASSIFIED DRUG;

ALLELE; ARTICLE; CARCINOGENESIS; CELL TRANSFORMATION; COMPLEX FORMATION; CONTROLLED STUDY; GENE MUTATION; HUMAN; HUMAN CELL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; TUMOR SUPPRESSOR GENE;

EID: 34249291096     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2007.03.047     Document Type: Article

References (58)

1. Ali S.H., and DeCaprio J.A. Cellular transformation by SV40 large T antigen: interaction with host proteins. Semin. Cancer Biol. 11 (2001) 15-23
2. Altschuler D., and Lapetina E.G. Mutational analysis of the cAMP-dependent protein kinase-mediated phosphorylation site of Rap1b. J. Biol. Chem. 268 (1993) 7527-7531
3. Baysal B.E., Willett-Brozick J.E., Taschner P.E., Dauwerse J.G., Devilee P., and Devlin B. A high-resolution integrated map spanning the SDHD gene at 11q23: a 1.1-Mb BAC contig, a partial transcript map and 15 new repeat polymorphisms in a tumour-suppressor region. Eur. J. Hum. Genet. 9 (2001) 121-129
4. Boehm J.S., Hession M.T., Bulmer S.E., and Hahn W.C. Transformation of human and murine fibroblasts without viral oncoproteins. Mol. Cell. Biol. 25 (2005) 6464-6474
5. Broach J.R., and Levine A.J. Oncogenes and cell proliferation. Curr. Opin. Genet. Dev. 7 (1997) 1-6
6. Calin G.A., di Iasio M.G., Caprini E., Vorechovsky I., Natali P.G., Sozzi G., Croce C.M., Barbanti-Brodano G., Russo G., and Negrini M. Low frequency of alterations of the alpha (PPP2R1A) and beta (PPP2R1B) isoforms of the subunit A of the serine-threonine phosphatase 2A in human neoplasms. Oncogene 19 (2000) 1191-1195
7. Camonis J.H., and White M.A. Ral GTPases: corrupting the exocyst in cancer cells. Trends Cell Biol. 15 (2005) 327-332
8. Chen W., Arroyo J.D., Timmons J.C., Possemato R., and Hahn W.C. Cancer-associated PP2A Aalpha subunits induce functional haploinsufficiency and tumorigenicity. Cancer Res. 65 (2005) 8183-8192
9. Chen W., Possemato R., Campbell K.T., Plattner C.A., Pallas D.C., and Hahn W.C. Identification of specific PP2A complexes involved in human cell transformation. Cancer Cell 5 (2004) 127-136
10. Chien Y., and White M.A. RAL GTPases are linchpin modulators of human tumour-cell proliferation and survival. EMBO Rep. 4 (2003) 800-806
11. Cho U.S., and Xu W. Crystal structure of a protein phosphatase 2A heterotrimeric holoenzyme. Nature 445 (2007) 53-57
12. Drayton S., Rowe J., Jones R., Vatcheva R., Cuthbert-Heavens D., Marshall J., Fried M., and Peters G. Tumor suppressor p16INK4a determines sensitivity of human cells to transformation by cooperating cellular oncogenes. Cancer Cell 4 (2003) 301-310
13. Emkey R., Freedman S., and Feig L.A. Characterization of a GTPase-activating protein for the Ras-related Ral protein. J. Biol. Chem. 266 (1991) 9703-9706
14. Feig L.A. Ral-GTPases: approaching their 15 minutes of fame. Trends Cell Biol. 13 (2003) 419-425
15. Feinstein E. Ral-GTPases: good chances for a long-lasting fame. Oncogene 24 (2005) 326-328
16. Gildea J.J., Harding M.A., Seraj M.J., Gulding K.M., and Theodorescu D. The role of Ral A in epidermal growth factor receptor-regulated cell motility. Cancer Res. 62 (2002) 982-985
17. Goi T., Shipitsin M., Lu Z., Foster D.A., Klinz S.G., and Feig L.A. An EGF receptor/Ral-GTPase signaling cascade regulates c-Src activity and substrate specificity. EMBO J. 19 (2000) 623-630
18. Gotz J., Probst A., Mistl C., Nitsch R.M., and Ehler E. Distinct role of protein phosphatase 2A subunit Calpha in the regulation of E-cadherin and beta-catenin during development. Mech. Dev. 93 (2000) 83-93
19. Hahn W.C., Dessain S.K., Brooks M.W., King J.E., Elenbaas B., Sabatini D.M., DeCaprio J.A., and Weinberg R.A. Enumeration of the simian virus 40 early region elements necessary for human cell transformation. Mol. Cell. Biol. 22 (2002) 2111-2123
20. Hahn W.C., Stewart S.A., Brooks M.W., York S.G., Eaton E., Kurachi A., Beijersbergen R.L., Knoll J.H., Meyerson M., and Weinberg R.A. Inhibition of telomerase limits the growth of human cancer cells. Nat. Med. 5 (1999) 1164-1170
21. Hahn W.C., and Weinberg R.A. Rules for making human tumor cells. N. Engl. J. Med. 347 (2002) 1593-1603
22. Hamad N.M., Elconin J.H., Karnoub A.E., Bai W., Rich J.N., Abraham R.T., Der C.J., and Counter C.M. Distinct requirements for Ras oncogenesis in human versus mouse cells. Genes Dev. 16 (2002) 2045-2057
23. Hanahan D., and Weinberg R.A. The hallmarks of cancer. Cell 100 (2000) 57-70
24. Hemmings B.A., Adams-Pearson C., Maurer F., Muller P., Goris J., Merlevede W., Hofsteenge J., and Stone S.R. alpha- and beta-forms of the 65-kDa subunit of protein phosphatase 2A have a similar 39 amino acid repeating structure. Biochemistry 29 (1990) 3166-3173
25. Hendrix P., Mayer-Jackel R.E., Cron P., Goris J., Hofsteenge J., Merlevede W., and Hemmings B.A. Structure and expression of a 72-kDa regulatory subunit of protein phosphatase 2A. Evidence for different size forms produced by alternative splicing. J. Biol. Chem. 268 (1993) 15267-15276
26. Hu C.D., Kariya K., Okada T., Qi X., Song C., and Kataoka T. Effect of phosphorylation on activities of Rap1A to interact with Raf-1 and to suppress Ras-dependent Raf-1 activation. J. Biol. Chem. 274 (1999) 48-51
27. Janssens V., and Goris J. Protein phosphatase 2A: a highly regulated family of serine/threonine phosphatases implicated in cell growth and signalling. Biochem. J. 353 (2001) 417-439
28. Jiang H., Luo J.Q., Urano T., Frankel P., Lu Z., Foster D.A., and Feig L.A. Involvement of Ral GTPase in v-Src-induced phospholipase D activation. Nature 378 (1995) 409-412
29. Lim K.H., Baines A.T., Fiordalisi J.J., Shipitsin M., Feig L.A., Cox A.D., Der C.J., and Counter C.M. Activation of RalA is critical for Ras-induced tumorigenesis of human cells. Cancer Cell 7 (2005) 533-545
30. Lim K.H., O'Hayer K., Adam S.J., Kendall S.D., Campbell P.M., Der C.J., and Counter C.M. Divergent roles for RalA and RalB in malignant growth of human pancreatic carcinoma cells. Curr. Biol. 16 (2006) 2385-2394
31. Lundberg A.S., Randell S.H., Stewart S.A., Elenbaas B., Hartwell K.A., Brooks M.W., Fleming M.D., Olsen J.C., Miller S.W., Weinberg R.A., and Hahn W.C. Immortalization and transformation of primary human airway epithelial cells by gene transfer. Oncogene 21 (2002) 4577-4586
32. Moskalenko S., Henry D.O., Rosse C., Mirey G., Camonis J.H., and White M.A. The exocyst is a Ral effector complex. Nat. Cell Biol. 4 (2002) 66-72
33. Ohta Y., Suzuki N., Nakamura S., Hartwig J.H., and Stossel T.P. The small GTPase RalA targets filamin to induce filopodia. Proc. Natl. Acad. Sci. USA 96 (1999) 2122-2128
34. Pallas D.C., Shahrik L.K., Martin B.L., Jaspers S., Miller T.B., Brautigan D.L., and Roberts T.M. Polyoma small and middle T antigens and SV40 small t antigen form stable complexes with protein phosphatase 2A. Cell 60 (1990) 167-176
35. Panner A., Nakamura J.L., Parsa A.T., Rodriguez-Viciana P., Berger M.S., Stokoe D., and Pieper R.O. mTOR-independent translational control of the extrinsic cell death pathway by RalA. Mol. Cell Biol. 26 (2006) 7345-7357
36. Quilliam L.A., Mueller H., Bohl B.P., Prossnitz V., Sklar L.A., Der C.J., and Bokoch G.M. Rap1A is a substrate for cyclic AMP-dependent protein kinase in human neutrophils. J. Immunol. 147 (1991) 1628-1635
37. Quilliam L.A., Rebhun J.F., and Castro A.F. A growing family of guanine nucleotide exchange factors is responsible for activation of Ras-family GTPases. Prog. Nucleic Acid Res. Mol. Biol. 71 (2002) 391-444
38. Rangarajan A., Hong S.J., Gifford A., and Weinberg R.A. Species- and cell type-specific requirements for cellular transformation. Cancer Cell 6 (2004) 171-183
39. Ruediger R., Pham H.T., and Walter G. Alterations in protein phosphatase 2A subunit interaction in human carcinomas of the lung and colon with mutations in the A beta subunit gene. Oncogene 20 (2001) 1892-1899
40. Ruediger R., Pham H.T., and Walter G. Disruption of protein phosphatase 2A subunit interaction in human cancers with mutations in the A alpha subunit gene. Oncogene 20 (2001) 10-15
41. Schonthal A.H. Role of serine/threonine protein phosphatase 2A in cancer. Cancer Lett. 170 (2001) 1-13
42. Seger Y.R., Garcia-Cao M., Piccinin S., Cunsolo C.L., Doglioni C., Blasco M.A., Hannon G.J., and Maestro R. Transformation of normal human cells in the absence of telomerase activation. Cancer Cell 2 (2002) 401-413
43. Silverstein A.M., Barrow C.A., Davis A.J., and Mumby M.C. Actions of PP2A on the MAP kinase pathway and apoptosis are mediated by distinct regulatory subunits. Proc. Natl. Acad. Sci. USA 99 (2002) 4221-4226
44. Sugano S., Yamaguchi N., and Shimojo H. Small t protein of simian virus 40 is required for dense focus formation in a rat cell line. J. Virol. 41 (1982) 1073-1075
45. Suganuma M., Fujiki H., Suguri H., Yoshizawa S., Hirota M., Nakayasu M., Ojika M., Wakamatsu K., Yamada K., and Sugimura T. Okadaic acid: an additional non-phorbol-12-tetradecanoate-13-acetate-type tumor promoter. Proc. Natl. Acad. Sci. USA 85 (1988) 1768-1771
46. Takagi Y., Futamura M., Yamaguchi K., Aoki S., Takahashi T., and Saji S. Alterations of the PPP2R1B gene located at 11q23 in human colorectal cancers. Gut 47 (2000) 268-271
47. Tamaki M., Goi T., Hirono Y., Katayama K., and Yamaguchi A. PPP2R1B gene alterations inhibit interaction of PP2A-Abeta and PP2A-C proteins in colorectal cancers. Oncol. Rep. 11 (2004) 655-659
48. Urano T., Emkey R., and Feig L.A. Ral-GTPases mediate a distinct downstream signaling pathway from Ras that facilitates cellular transformation. EMBO J. 15 (1996) 810-816
49. van Dam E.M., and Robinson P.J. Ral: Mediator of membrane trafficking. Int. J. Biochem. Cell Biol. 38 (2006) 1841-1847
50. Voorhoeve P.M., and Agami R. The tumor-suppressive functions of the human INK4A locus. Cancer Cell 4 (2003) 311-319
51. Wang S.S., Esplin E.D., Li J.L., Huang L., Gazdar A., Minna J., and Evans G.A. Alterations of the PPP2R1B gene in human lung and colon cancer. Science 282 (1998) 284-287
52. Wu J.C., Chen T.Y., Yu C.T., Tsai S.J., Hsu J.M., Tang M.J., Chou C.K., Lin W.J., Yuan C.J., and Huang C.Y. Identification of V23RalA-Ser194 as a critical mediator for Aurora-A-induced cellular motility and transformation by small pool expression screening. J. Biol. Chem. 280 (2005) 9013-9022
53. Xu Y., Xing Y., Chen Y., Chao Y., Lin Z., Fan E., Yu J.W., Strack S., Jeffrey P.D., and Shi Y. Structure of the protein phosphatase 2A holoenzyme. Cell 127 (2006) 1239-1251
54. Yeh E., Cunningham M., Arnold H., Chasse D., Monteith T., Ivaldi G., Hahn W.C., Stukenberg P.T., Shenolikar S., Uchida T., et al. A signalling pathway controlling c-Myc degradation that impacts oncogenic transformation of human cells. Nat. Cell Biol. 6 (2004) 308-318
55. Yu J., Boyapati A., and Rundell K. Critical role for SV40 small-t antigen in human cell transformation. Virology 290 (2001) 192-198
56. Zhao J.J., Gjoerup O.V., Subramanian R.R., Cheng Y., Chen W., Roberts T.M., and Hahn W.C. Human mammary epithelial cell transformation through the activation of phosphatidylinositol 3-kinase. Cancer Cell 3 (2003) 483-495
57. Zhao J.J., Roberts T.M., and Hahn W.C. Functional genetics and experimental models of human cancer. Trends Mol. Med. 10 (2004) 344-350
58. Zhou J., Pham H.T., Ruediger R., and Walter G. Characterization of the Aalpha and Abeta subunit isoforms of protein phosphatase 2A: differences in expression, subunit interaction, and evolution. Biochem. J. 369 (2003) 387-398