Impaired expression of protein phosphatase 2A subunits enhances metastatic potential of human prostate cancer cells through activation of AKT pathway

British Journal of Cancer

Volumn 108, Issue 12, 2013, Pages 2590-2600

  Pandey, P ^a   Seshacharyulu, P ^a   Das, S ^a   Rachagani, S ^a   Ponnusamy, M P ^a   Yan, Y ^b   Johansson, S L ^a,b   Datta, K ^a,b   Lin, M Fong ^a,b   Batra, S K ^a,b  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHOPROTEIN PHOSPHATASE 2A; PROTEIN KINASE B;

ARTICLE; CANCER CELL; CANCER GROWTH; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME DEFECT; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INTRACELLULAR SIGNALING; MALE; METASTASIS POTENTIAL; PRIORITY JOURNAL; PROSTATE CANCER; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ADENOCARCINOMA; CELL LINE, TUMOR; DISEASE PROGRESSION; DOWN-REGULATION; ENZYME ACTIVATION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; MODELS, BIOLOGICAL; NEOPLASM METASTASIS; ONCOGENE PROTEIN V-AKT; PROSTATIC NEOPLASMS; PROTEIN PHOSPHATASE 2; PROTEIN SUBUNITS; SIGNAL TRANSDUCTION;

EID: 84879687996     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2013.160     Document Type: Article

References (67)

1. Baharians Z, Schonthal AH (1998) Autoregulation of protein phosphatase type 2A expression. J Biol Chem 273(30): 19019-19024.
2. Bhardwaj A, Singh S, Srivastava SK, Honkanen RE, Reed E, Singh AP (2011) Modulation of protein phosphatase 2A activity alters androgen-independent growth of prostate cancer cells: therapeutic implications. Mol Cancer Ther 10(5): 720-731.
3. Bononi A, Agnoletto C, De ME, Marchi S, Patergnani S, Bonora M, Giorgi C, Missiroli S, Poletti F, Rimessi A, Pinton P (2011) Protein kinases and phosphatases in the control of cell fate. Enzyme Res 2011: 329098.
4. Brinkmann AO (2001) Lessons to be learned from the androgen receptor. Eur J Dermatol 11(4): 301-303.
5. Calin GA, di Iasio MG, Caprini E, Vorechovsky I, Natali PG, Sozzi G, Croce CM, Barbanti-Brodano G, Russo G, Negrini M (2000) 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(9): 1191-1195.
6. Chen W, Arroyo JD, Timmons JC, Possemato R, Hahn WC (2005) Cancer-associated PP2A Aalpha subunits induce functional haploinsufficiency and tumorigenicity. Cancer Res 65(18): 8183-8192.
7. Chen W, Possemato R, Campbell KT, Plattner CA, Pallas DC, Hahn WC (2004) Identification of specific PP2A complexes involved in human cell transformation. Cancer Cell 5(2): 127-136.
8. Cho US, Morrone S, Sablina AA, Arroyo JD, Hahn WC, Xu W (2007) Structural basis of PP2A inhibition by small t antigen. PLoS Biol 5(8): e202.
9. Cho US, Xu W (2007) Crystal structure of a protein phosphatase 2A heterotrimeric holoenzyme. Nature 445(7123): 53-57.
10. Chuu CP, Kokontis JM, Hiipakka RA, Fukuchi J, Lin HP, Lin CY, Huo C, Su LC (2011) Androgens as therapy for androgen receptor-positive castration-resistant prostate cancer. J Biomed Sci 18: 63.
11. Cohen P (2001) The role of protein phosphorylation in human health and disease. The Sir Hans Krebs Medal Lecture. Eur J Biochem 268(19): 5001-5010.
12. Esplin ED, Ramos P, Martinez B, Tomlinson GE, Mumby MC, Evans GA (2006) The glycine 90 to aspartate alteration in the Abeta subunit of PP2A (PPP2R1B) associates with breast cancer and causes a deficit in protein function. Genes Chromosomes Cancer 45(2): 182-190.
13. Grochola LF, Vazquez A, Bond EE, Wurl P, Taubert H, Muller TH, Levine AJ, Bond GL (2009) Recent natural selection identifies a genetic variant in a regulatory subunit of protein phosphatase 2A that associates with altered cancer risk and survival. Clin Cancer Res 15(19): 6301-6308.
14. Hankey BF, Feuer EJ, Clegg LX, Hayes RB, Legler JM, Prorok PC, Ries LA, Merrill RM, Kaplan RS (1999) Cancer surveillance series: interpreting trends in prostate cancer-part I: evidence of the effects of screening in recent prostate cancer incidence, mortality, and survival rates. J Natl Cancer Inst 91(12): 1017-1024.
15. Hoffman RM (2011) Clinical practice. Screening for prostate cancer. N Engl J Med 365(21): 2013-2019.
16. Igawa T, Lin FF, Lee MS, Karan D, Batra SK, Lin MF (2002) Establishment and characterization of androgen-independent human prostate cancer LNCaP cell model. Prostate 50(4): 222-235.
17. Inagaki N, Ito M, Nakano T, Inagaki M (1994) Spatiotemporal distribution of protein kinase and phosphatase activities. Trends Biochem Sci 19(11): 448-452.
18. Ito A, Kataoka TR, Watanabe M, Nishiyama K, Mazaki Y, Sabe H, Kitamura Y, Nojima H (2000) A truncated isoform of the PP2A B56 subunit promotes cell motility through paxillin phosphorylation. EMBO J 19(4): 562-571.
19. Jackson J, Meisinger J, Patel S, Lim ZC, Vellody K, Metz R, Young MR (1997) Protein phosphatase-2A associates with the cytoskeleton to maintain cell spreading and reduced motility of nonmetastatic Lewis lung carcinoma cells: the loss of this regulatory control in metastatic cells. Invas Metast 17(4): 199-209.
20. 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.
21. Janssens V, Longin S, Goris J (2008) PP2A holoenzyme assembly: in cauda venenum (the sting is in the tail). Trends Biochem Sci 33(3): 113-121.
22. Kamibayashi C, Estes R, Lickteig RL, Yang SI, Craft C, Mumby MC (1994) Comparison of heterotrimeric protein phosphatase 2A containing different B subunits. J Biol Chem 269(31): 20139-20148.
23. Kreisberg JI, Malik SN, Prihoda TJ, Bedolla RG, Troyer DA, Kreisberg S, Ghosh PM (2004) Phosphorylation of Akt (Ser473) is an excellent predictor of poor clinical outcome in prostate cancer. Cancer Res 64(15): 5232-5236.
24. Kremmer E, Ohst K, Kiefer J, Brewis N, Walter G (1997) Separation of PP2A core enzyme and holoenzyme with monoclonal antibodies against the regulatory A subunit: abundant expression of both forms in cells. Mol Cell Biol 17(3): 1692-1701.
25. Letourneux C, Rocher G, Porteu F (2006) B56-containing PP2A dephosphorylate ERK and their activity is controlled by the early gene IEX-1 and ERK. EMBO J 25(4): 727-738.
26. Li HH, Cai X, Shouse GP, Piluso LG, Liu X (2007) A specific PP2A regulatory subunit, B56gamma, mediates DNA damage-induced dephosphorylation of p53 at Thr55. EMBO J 26(2): 402-411.
27. Li L, Ittmann MM, Ayala G, Tsai MJ, Amato RJ, Wheeler TM, Miles BJ, Kadmon D, Thompson TC (2005) The emerging role of the PI3-K-Akt pathway in prostate cancer progression. Prostate Cancer Prostat Dis 8(2): 108-118.
28. Li X, Scuderi A, Letsou A, Virshup DM (2002) B56-associated protein phosphatase 2A is required for survival and protects from apoptosis in Drosophila melanogaster. Mol Cell Biol 22(11): 3674-3684.
29. Longin S, Zwaenepoel K, Martens E, Louis JV, Rondelez E, Goris J, Janssens V (2008) Spatial control of protein phosphatase 2A (de)methylation. Exp Cell Res 314(1): 68-81.
30. Margolis SS, Perry JA, Forester CM, Nutt LK, Guo Y, Jardim MJ, Thomenius MJ, Freel CD, Darbandi R, Ahn JH, Arroyo JD, Wang XF, Shenolikar S, Nairn AC, Dunphy WG, Hahn WC, Virshup DM, Kornbluth S (2006) Role for the PP2A/B56delta phosphatase in regulating 14-3-3 release from Cdc25 to control mitosis. Cell 127(4): 759-773.
31. Meisinger J, Patel S, Vellody K, Bergstrom R, Benefield J, Lozano Y, Young MR (1997) Protein phosphatase-2A association with microtubules and its role in restricting the invasiveness of human head and neck squamous cell carcinoma cells. Cancer Lett 111(1-2): 87-95.
32. Millward TA, Zolnierowicz S, Hemmings BA (1999) Regulation of protein kinase cascades by protein phosphatase 2A. Trends Biochem Sci 24(5): 186-191.
33. Moniaux N, Chakraborty S, Yalniz M, Gonzalez J, Shostrom VK, Standop J, Lele SM, Ouellette M, Pour PM, Sasson AR, Brand RE, Hollingsworth MA, Jain M, Batra SK (2008) Early diagnosis of pancreatic cancer: neutrophil gelatinase-associated lipocalin as a marker of pancreatic intraepithelial neoplasia. Br J Cancer 98(9): 1540-1547.
34. Mumby M (2007) PP2A: unveiling a reluctant tumor suppressor. Cell 130(1): 21-24.
35. Muneer S, Ramalingam V, Wyatt R, Schultz RA, Minna JD, Kamibayashi C (2002) Genomic organization and mapping of the gene encoding the PP2A B56gamma regulatory subunit. Genomics 79(3): 344-348.
36. Nolan C, Novoa WB, Krebs EG, Fischer EH (1964) Further studies on the site phosphorylated in the phosphorylase b to a reaction. Biochemistry 3: 542-551.
37. Perrotti D, Neviani P (2008) Protein phosphatase 2A (PP2A), a drugable tumor suppressor in Ph1(+) leukemias. Cancer Metast Rev 27(2): 159-168.
38. Prowatke I, Devens F, Benner A, Grone EF, Mertens D, Grone HJ, Lichter P, Joos S (2007) Expression analysis of imbalanced genes in prostate carcinoma using tissue microarrays. Br J Cancer 96(1): 82-88.
39. 12D is associated with invasion and metastasis of pancreatic cancer cells through inhibition of E-cadherin. Br J Cancer 104(6): 1038-1048.
40. Ross SH, Spanjaard E, Post A, Vliem MJ, Kristyanto H, Bos JL, de RJ (2012) Rap1 can bypass the FAK-Src-paxillin cascade to induce cell spreading and focal adhesion formation. PLoS One 7(11): e50072.
41. Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132: 365-386.
42. Ruediger R, Pham HT, Walter G (2001) 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(15): 1892-1899.
43. Ruediger R, Ruiz J, Walter G (2011) Human cancer-associated mutations in the Aalpha subunit of protein phosphatase 2A increase lung cancer incidence in Aalpha knock-in and knockout mice. Mol Cell Biol 31(18): 3832-3844.
44. Sablina AA, Chen W, Arroyo JD, Corral L, Hector M, Bulmer SE, DeCaprio JA, Hahn WC (2007) The tumor suppressor PP2A Abeta regulates the RalA GTPase. Cell 129(5): 969-982.
45. Sablina AA, Hector M, Colpaert N, Hahn WC (2010) Identification of PP2A complexes and pathways involved in cell transformation. Cancer Res 70(24): 10474-10484.
46. Seeling JM, Miller JR, Gil R, Moon RT, White R, Virshup DM (1999) Regulation of beta-catenin signaling by the B56 subunit of protein phosphatase 2A. Science 283(5410): 2089-2091.
47. Senapati S, Rachagani S, Chaudhary K, Johansson SL, Singh RK, Batra SK (2010) Overexpression of macrophage inhibitory cytokine-1 induces metastasis of human prostate cancer cells through the FAK-RhoA signaling pathway. Oncogene 29(9): 1293-1302.
48. Sharifi N, Gulley JL, Dahut WL (2005) Androgen deprivation therapy for prostate cancer. JAMA 294(2): 238-244.
49. Shi Y (2009) Serine/threonine phosphatases: mechanism through structure. Cell 139(3): 468-484.
50. Siegel R, Naishadham D, Jemal A (2012) Cancer statistics, 2012. CA Cancer J Clin 62(1): 10-29.
51. Singh AP, Bafna S, Chaudhary K, Venkatraman G, Smith L, Eudy JD, Johansson SL, Lin MF, Batra SK (2008) Genome-wide expression profiling reveals transcriptomic variation and perturbed gene networks in androgen-dependent and androgen-independent prostate cancer cells. Cancer Lett 259(1): 28-38.
52. Slack JK, Adams RB, Rovin JD, Bissonette EA, Stoker CE, Parsons JT (2001) Alterations in the focal adhesion kinase/Src signal transduction pathway correlate with increased migratory capacity of prostate carcinoma cells. Oncogene 20(10): 1152-1163.
53. Stephenson RA, Dinney CP, Gohji K, Ordonez NG, Killion JJ, Fidler IJ (1992) Metastatic model for human prostate cancer using orthotopic implantation in nude mice. J Natl Cancer Inst 84(12): 951-957.
54. Suzuki K, Takahashi K (2003) Reduced expression of the regulatory A subunit of serine/threonine protein phosphatase 2A in human breast cancer MCF-7 cells. Int J Oncol 23(5): 1263-1268.
55. Takagi Y, Futamura M, Yamaguchi K, Aoki S, Takahashi T, Saji S (2000) Alterations of the PPP2R1B gene located at 11q23 in human colorectal cancers. Gut 47(2): 268-271.
56. Tamaki M, Goi T, Hirono Y, Katayama K, Yamaguchi A (2004) PPP2R1B gene alterations inhibit interaction of PP2A-Abeta and PP2A-C proteins in colorectal cancers. Oncol Rep 11(3): 655-659.
57. Van Kanegan MJ, Adams DG, Wadzinski BE, Strack S (2005) Distinct protein phosphatase 2A heterotrimers modulate growth factor signaling to extracellular signal-regulated kinases and Akt. J Biol Chem 280(43): 36029-36036.
58. Virshup DM, Shenolikar S (2009) From promiscuity to precision: protein phosphatases get a makeover. Mol Cell 33(5): 537-545.
59. Wang SS, Esplin ED, Li JL, Huang L, Gazdar A, Minna J, Evans GA (1998) Alterations of the PPP2R1B gene in human lung and colon cancer. Science 282(5387): 284-287.
60. Wera S, Hemmings BA (1995) Serine/threonine protein phosphatases. Biochem J 311: 17-29.
61. Westermarck J, Hahn WC (2008) Multiple pathways regulated by the tumor suppressor PP2A in transformation. Trends Mol Med 14(4): 152-160.
62. Xu Y, Xing Y, Chen Y, Chao Y, Lin Z, Fan E, Yu JW, Strack S, Jeffrey PD, Shi Y (2006) Structure of the protein phosphatase 2A holoenzyme. Cell 127(6): 1239-1251.
63. Yang J, Phiel C (2010) Functions of B56-containing PP2As in major developmental and cancer signaling pathways. Life Sci 87(23-26): 659-666.
64. Yang J, Wu J, Tan C, Klein PS (2003) PP2A:B56epsilon is required for Wnt/beta-catenin signaling during embryonic development. Development 130(23): 5569-5578.
65. Young MR, Kolesiak K, Meisinger J (2002) Protein phosphatase-2A regulates endothelial cell motility and both the phosphorylation and the stability of focal adhesion complexes. Int J Cancer 100(3): 276-282.
66. Young MR, Liu SW, Meisinger J (2003) Protein phosphatase-2A restricts migration of Lewis lung carcinoma cells by modulating the phosphorylation of focal adhesion proteins. Int J Cancer 103(1): 38-44.
67. Zhang Q, Claret FX (2012) Phosphatases: the new brakes for cancer development? Enzyme Res 2012: 659649.