PP2A activity is controlled by methylation and regulates oncoprotein expression in melanoma cells: A mechanism which participates in growth inhibition induced by chloroethylnitrosourea treatment

International Journal of Oncology

Volumn 32, Issue 1, 2008, Pages 49-57

  Guénin, Samuel ^a   Schwartz, Laurent ^b   Morvan, Daniel ^a,c   Steyaert, Jean Marc ^d   Poignet, Amandine ^a   Madelmont, Jean Claude ^a   Demidem, Aicha ^a  

^a INSERM   (France)

^b PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^c CLCC d'Auvergne   (France)

^d ÉCOLE POLYTECHNIQUE   (France)

Author keywords

Chloroethylnitrosourea; DNA damage; Oncoproteins; PP2A; Transmethylation; Tumor cell aggressiveness

Indexed keywords

CHLOROETHYLNITROSOUREA; MYC PROTEIN; OKADAIC ACID; ONCOPROTEIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PHOSPHOPROTEIN PHOSPHATASE 2A; PHOSPHOPROTEIN PHOSPHATASE INHIBITOR; PROTEIN KINASE B; UNCLASSIFIED DRUG; XYLULOSE 5 PHOSPHATE;

ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DNA DAMAGE; DOWN REGULATION; DRUG MECHANISM; ENZYME ACTIVATION; GROWTH INHIBITION; MELANOMA CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN METHYLATION;

EID: 38749091638     PISSN: 10196439     EISSN: None     Source Type: Journal    
DOI: 10.3892/ijo.32.1.49     Document Type: Article

References (48)

1. Janssens V and Goris J: Protein phosphatase 2A: a highly regulated family of serine/threonine phosphatases implicated in cell growth and signaling. Biochem J 353: 417-439, 2001.
2. Bellacosa A, Kumar CC, Di Cristofano A and Testa JR: Activation of Akt kinases in cancer: implication for therapeutic targeting. Adv Cancer Res 94: 29-86, 2005.
3. Altomare DA and Testa JR: Perturbations of the AKT signaling pathway in human cancer. Oncogene 24: 7455-7464, 2005.
4. Tokunaga E, Kimura Y, Oki E, et al: Akt is frequently activated in HER2/neu-positive breast cancers and associated with poor prognosis among hormone-treated patients. Int J Cancer 118: 284-289, 2006.
5. Janssens V, Goris J and van Hoof C: PP2A: the expected tumor suppressor. Curr Opin Genet Dev 15: 34-41,2005.
6. Arroyo JD and Hahn WC: Involvement of PP2A in viral and cellular transformation. Oncogene 24: 7746-7755, 2005.
7. Jang YJ, Ji JH, Choi YC, Ryu CJ and Ko SY: Regulation of Polo-like kinase 1 by DNA damage in mitosis: inhibition of mitotic plk-1 by protein phosphatase 2A. J Biol Chem 282: 2473-2482, 2007.
8. Sancar A, Lindsey-Boltz LA, Unsal-Kacmaz K and Linn S: Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu Rev Biochem 73: 39-85, 2004.
9. Coutts AS and La Thangue N: The p53 response during DNA damage: impact of transcriptional cofactors. Biochem Soc Symp 73: 181-189, 2006.
10. Roos WP and Kaina B: DNA damage-induced cell death by apoptosis. Trends Mol Med 12: 440-450, 2006.
11. Godeneche D, Rapp M, Thierry A, Laval F, Madelmont JC, Chollet P and Veyre A: DNA damage induced by a new 2-chloroethyl nitrosourea on malignant melanoma cells. Cancer Res 50: 5898-5903, 1990.
12. Morvan D, Demidem A, Papon J and Madelmont JC: Quantitative HRMAS proton total correlation spectroscopy applied to cultured melanoma cells treated by chloroethyl nitrosourea: demonstration of phospholipid metabolism alterations. Magn Reson Med 49: 241-248, 2003.
13. Demidem A, Morvan D and Madelmont JC: Bystander effects are induced by CENU treatment and associated with altered protein secretory activity of treated tumor cells. A relay for chemotherapy? Int J Cancer 116: 992-1004, 2006.
14. Grillo MA and Colombatto S: S-adenosylmethionine and protein methylation. Amino Acids 28: 357-362, 2005.
15. Bedford MT and Richard S: Arginine methylation an emerging regulator of protein function. Mol Cell 18: 263-272, 2005.
16. Xie H and Clarke S: Protein phosphatase 2A is reversibly modified by methyl esterification at its C-terminal leucine residue in bovine brain. J Biol Chem 269: 1981-1984, 1994.
17. Lee J, Chen Y, Tolstykh T and Stock J: A specific protein carboxyl methylesterase that demethylates phosphoprotein phosphatase 2A in bovine brain. Proc Natl Acad Sci USA 93: 6043-6047, 1996.
18. Kabashima T, Kawaguchi T, Wadzinski BE and Uyeda K: Xylulose 5-phosphate mediates glucose-induced lipogenesis by xylulose 5-phosphate-activated protein phosphatase in rat liver. Proc Natl Acad Sci USA 100: 5107-5112, 2003.
19. 13C NMR spectroscopy. Magn Reson Med 55: 984-996, 2006.
20. Baharians Z and Schönthal A: Reduction of Ha-ras-induced cellular transformation by elevated expression of protein phosphatase type 2A. Mol Carcinog 24: 246-254, 1999.
21. Fujiki H, Suganuma M, Yoshizawa S, Nishiwaki S, Winyar B and Sugimura T: Mechanisms of action of okadaic acid class tumor promoters on mouse skin. Environ Health Perspect 93: 211-214, 1991.
22. Buchdahl C, Papon J, Communal Y, Bourges M and Madelmont JC: G2 accumulation and melanin overproduction in malignant melanocytes treated with a new nitrosourea. Melanoma Res 8: 517-527, 1998.
23. Demidem A, Morvan D, Papon J, De Latour M and Madelmont JC: Cystemustine induces redifferentiation of primary tumors and confers protection against secondary tumor growth in a melanoma murine model. Cancer Res 61: 2294-2300, 2001.
24. Morvan D, Demidem A, Papon J, De Latour M and Madelmont JC: Melanoma tumors acquire a new phospholipid metabolism phenotype under cystemustine as revealed by high-resolution magic angle spinning proton nuclear magnetic resonance spectroscopy of intact tumor samples. Cancer Res 62: 1890-1897, 2002.
25. Lee J and Stock J: Protein phosphatase 2A catalytic subunit is methyl-esterified at its carboxyl terminus by a novel methyltransferase. J Biol Chem 268: 19192-19195, 1993.
26. 0 during retinoic acid-induced granulocytic differentiation and a modification on the catalytic subunit in S phase of HL-60 cells. Arch Biochem Biophys 339: 210-217, 1997.
27. Favre B, Zolnierowicz S, Turowski P and Hemmings BA: The catalytic subunit of protein phosphatase 2A is carboxyl-methylated in vivo. J Biol Chem 269:16311-16317, 1994.
28. Kowluru A, Seavey SE, Rabaglia ME, Nesher R and Metz SA: Carboxylmethylation of the catalytic subunit of protein phosphatase 2A in insulin-secreting cells: evidence for functional consequences on enzyme activity and insulin secretion. Endocrinology 137: 2315-2322, 1996.
29. Stahl JM, Cheung M, Sharma A, Trivedi NR, Shanmugam S and Robertson GP: Loss of PTEN promotes tumor development in malignant melanoma. Cancer Res 63: 2881-2890, 2003.
30. Wu H, Goel V and Haluska FG: PTEN signaling pathways in melanoma. Oncogene 22: 3113-3122, 2003.
31. Pim D, Massimi P, Dilworth SM and Banks L: Activation of the protein kinase B pathway by the HPV-16 E7 oncoprotein occurs through a mechanism involving interaction with PP2A. Oncogene 24: 7830-7838, 2005.
32. Miller SJ, Lou DY, Seldin DC, Lane WS and Neel BG: Direct identification of PTEN phosphorylation sites. FEBS Lett 528: 145-153, 2002.
33. Gericke A, Munson M and Ross AH: Regulation of the PTEN phosphatase. Gene 374: 1-9, 2006.
34. Li J, Yen C, Liaw D, et al: PTEN, a putative protein tyrosine phosphatase gene mutated in human brain, breast, and prostate cancer. Science 275: 1943-1947, 1997.
35. Cai XM, Tao BB, Wang LY, et al: Protein phosphatase activity of PTEN inhibited the invasion of glioma cells with epidermal growth factor receptor mutation type In expression. Int J Cancer 117: 905-912, 2005.
36. Trotman LC, Wang X, Alimonti A, et al: Ubiquitination regulates PTEN nuclear import and tumor suppression. Cell 128: 141-156, 2007.
37. Kins S, Crameri A, Evans DR, Hemmings BA, Nitsch RM and Gotz J: Reduced protein phosphatase 2A activity induces hyperphosphorylation and altered compartmentalization of tau in transgenic mice. J Biol Chem 276: 38193-38200, 2001.
38. Zhu D, Kosik KS, Meigs TE, Yanamadala V and Denker BM: Galpha12 directly interacts with PP2A: evidence for Galpha12-stimulated PP2A phosphatase activity and dephosphorylation of microtubule-associated protein, tau. J Biol Chem 279: 54983-54986, 2004.
39. Christmann M, Pick M, Lage H, Schadendorf D and Kaina B: Acquired resistance of melanoma cells to the antineoplastic agent fotemustine is caused by reactivation of the DNA repair gene MGMT. Int J Cancer 92: 123-129, 2001.
40. Li HH, Cai X, Shouse GP, Piluso LG and Liu X: A specific PP2A regulatory subunit, B56gamma, mediates DNA damage-induced dephosphorylation of p53 at Thr55. EMBO J 26: 402-411,2007.
41. 6-methylguanine-DNA methyltransferase regulation by p53 in astrocytic cells. Cancer Res 67: 580-584, 2007.
42. Ruvolo PP: Intracellular signal transduction pathways activated by ceramides and its metabolites. Pharmacol Res 47: 383-392, 2003.
43. Hirose Y, Katayama M, Mirzoeva OK, Berger MS and Pieper RO: Akt activation suppresses Chk2-mediated, methylating agent-induced G2 arrest and protects from temozolomide-induced mitotic catastrophe and cellular senescence. Cancer Res 65: 4861-4869, 2005.
44. Cha TL, Zhou BP, Xia W, et al: Akt-mediated phosphorylation of EZH2 suppresses methylation of lysine 27 in histone H3. Science 310:306-310, 2005.
45. Sunters A, Grimaldi KA, Souhami RL and Hartley JA: Gene and human tumour cell line specific differences in nitrogen mustard induced DNA alkylation and interstrand crosslinking frequencies. Nucleic Acids Res 26: 5617-5623, 1998.
46. Bellmann K, Martel J, Poirier DJ, Labrie MM and Landry J: Downregulation of the PI3K/Akt survival pathway in cells with deregulated expression of c-Myc. Apoptosis 11: 1311-1319, 2006.
47. Yeh E, Cunningham M, Arnold H, et al: A signalling pathway controlling c-Myc degradation that impacts oncogenic transformation of human cells. Nat Cell Biol 6:308-318, 2004.
48. Biroccio A, Benassi B, Fiorentino F and Zupi G: Glutathione depletion induced by c-Myc downregulation triggers apoptosis on treatment with alkylating agents. Neoplasia 6: 195-206, 2004.