Dithiolethione compounds inhibit Akt signaling in human breast and lung cancer cells by increasing PP2A activity

Oncogene

Volumn 28, Issue 43, 2009, Pages 3837-3846

  Switzer, C H ^a   Ridnour, L A ^a   Cheng, R Y S ^a   Sparatore, A ^b   Del Soldato, P ^c   Moody, T W ^a   Vitek, M P ^d   Roberts, D D ^a   Wink, D A ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b UNIVERSITY OF MILAN   (Italy)

^c Sulfidris   (Italy)

^d DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Akt; Breast; Cancer; Dithiolethione; Lung; PP2A

Indexed keywords

CYCLIC AMP; DITHIOLETHIONE DERIVATIVE; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; FIBRONECTIN; INTEGRIN; MAMMALIAN TARGET OF RAPAMYCIN; MYC PROTEIN; OKADAIC ACID; PHOSPHOPROTEIN PHOSPHATASE 2A; PROTEIN KINASE B; SERINE; THIOL DERIVATIVE; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CANCER PREVENTION; CELL PROLIFERATION; CHEMOPROPHYLAXIS; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; LUNG CANCER; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANTICARCINOGENIC AGENTS; BREAST NEOPLASMS; CELL LINE, TUMOR; FEMALE; HUMANS; LUNG NEOPLASMS; PHOSPHORYLATION; PROTEIN PHOSPHATASE 2; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION;

MAMMALIA;

EID: 70350690313     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2009.244     Document Type: Article

References (49)

1. Andjelkovic M, Jakubowicz T, Cron P, Ming XF, Han JW, Hemmings BA. (1996). Activation and phosphorylation of a pleckstrin homology domain containing protein kinase (RAC-PK/PKB) promoted by serum and protein phosphatase inhibitors. Proc Natl Acad Sci USA 93: 5699-5704.
2. Arnold H, Sears R. (2008). A tumor suppressor role for PP2A-B56a through negative regulation of c-Myc and other key oncoproteins. Cancer Metastasis Rev 27: 147-158.
3. Arnold HK, Sears RC. (2006). Protein phosphatase 2A regulatory subunit B56{alpha} associates with c-Myc and negatively regulates c-Myc accumulation. Mol Cell Biol 26: 2832-2844.
4. Bae EJ, Yang YM, Kim JW, Kim SG. (2007). Identification of a novel class of dithiolethiones that prevent hepatic insulin resistance via the adenosine monophosphate-activated protein kinase-p70 ribosomal S6 kinase-1 pathway. Hepatology 46: 730-739.
5. Bass SE, Sienkiewicz P, MacDonald CJ, Cheng RYS, Sparatore A, Del Soldato P et al. (2009). Novel dithiolethione-modified nonsteroidal anti-inflammatory drugs in human hepatoma HepG2 and colon LS180 cells. Clin Cancer Res 15: 1964-1972.
6. Busserolles J, Meg?as J, Terencio MC, Alcaraz MJ. (2006). Heme oxygenase-1 inhibits apoptosis in Caco-2 cells via activation of Akt pathway. Inter J Biochem Cell Biol 38: 1510-1517.
7. Cai W-J, Wang M-J, Moore PK, Jin H-M, Yao T, Zhu Y-C. (2007). The novel proangiogenic effect of hydrogen sulfide is dependent on Akt phosphorylation. Cardiovasc Res 76: 29-40.
8. Carnero A, Blanco-Aparicio C, Renner O, Link W, Leal JF. (2008). The PTEN/PI3K/AKT signalling pathway in cancer, therapeutic implications. Curr Cancer Drug Targets 8: 187-198.
9. Chen J, Martin BL, Brautigan DL. (1992). Regulation of protein serine-threonine phosphatase type-2A by tyrosine phosphorylation. Science 257: 1261-1264.
10. Danen EHJ, Yamada KM. (2001). Fibronectin, integrins, and growth control. J Cell Physiol 189: 1-13.
11. Dillon RL, White DE, Muller WJ. (2007). The phosphatidyl inositol 3-kinase signaling network: implications for human breast cancer. Oncogene 26: 1338-1345.
12. Dulak J, Deshane J, Jozkowicz A, Agarwal A. (2008). Heme oxygenase-1 and carbon monoxide in vascular pathobiology: focus on angiogenesis. Circulation 117: 231-241.
13. Eichhorn PJA, Creyghton MP, Bernards R. (2009). Protein phospha-tase 2A regulatory subunits and cancer. Biochimica et Biophysica Acta (BBA)-Reviews on Cancer 1795: 1-15.
14. Feschenko MS, Stevenson E, Nairn AC, Sweadner KJ. (2002). A novel cAMP-stimulated pathway in protein phosphatase 2A activation. J Pharmacol Exp Ther 302: 111-118.
15. Guadagni F, Ferroni P, Palmirotta R, Del Monte G, Formica V, Roselli M. (2007). Non-steroidal anti-inflammatory drugs in cancer prevention and therapy. Anticancer Res 27: 3147-3162.
16. Hamada T, Nakane T, Kimura T, Arisawa K, Yoneda K, Yamamoto T et al. (1999). Treatment of xerostomia with the bile secretion-stimulating drug anethole trithione: a clinical trial. Am J Med Sci 318: 146-151.
17. Hresko RC, Mueckler M. (2005). mTOR/RICTOR is the Ser473 kinase for Akt/protein kinase B in 3T3-L1 adipocytes. J Biol Chem 280: 40406-40416.
18. Isenberg JS, Jia Y, Field L, Ridnour LA, Sparatore A, Del Soldato P et al. (2007). Modulation of angiogenesis by dithiolethione-modified NSAIDs and valproic acid. Br J Pharmacol 151: 142-151.
19. 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.
20. Kim SG, Nam SY, Kim CW. (1998). In vivo radioprotective effects of Oltipraz in [gamma]-irradiated mice. Biochem Pharmacol 55: 1585-1590.
21. Kwak M-K, Egner PA, Dolan PM, Ramos-Gomez M, Groopman JD, Itoh K et al. (2001). Role of phase 2 enzyme induction in chemoprotection by dithiolethiones. Mutat Res 480-481: 305-315.
22. Kwak M-K, Wakabayashi N, Itoh K, Motohashi H, Yamamoto M, Kensler TW. (2003). Modulation of gene expression by cancer chemopreventive dithiolethiones through the Keap1-Nrf2 pathway. Identification of novel gene clusters for cell survival. J Biol Chem 278: 8135-8145.
23. Lam S, MacAulay C, le Riche JC, Dyachkova Y, Coldman A, Guillaud M et al. (2002). A randomized phase IIb trial of anethole dithiolethione in smokers with bronchial dysplasia. J Natl Cancer Inst 94: 1001-1009.
24. Lee J-S, Surh Y-J. (2005). Nrf2 as a novel molecular target for chemoprevention. Cancer Lett 224: 171-184.
25. Li L, Rossoni G, Sparatore A, Lee LC, Del Soldato P, Moore PK. (2007). Anti-inflammatory and gastrointestinal effects of a novel diclofenac derivative. Free Rad Biol Med 42: 706-719.
26. Li M, Guo H, Damuni Z. (1995). Purification and characterization of two potent heat-stable protein inhibitors of protein phosphatase 2A from Bovine kidney. Biochemistry 34: 1988-1996.
27. Liang J, Zubovitz J, Petrocelli T, Kotchetkov R, Connor MK, Han K et al. (2002). PKB/Akt phosphorylates p27, impairs nuclear import of p27 and opposes p27-mediated G1 arrest. Nat Med 8: 1153-1160.
28. Longin S, Zwaenepoel K, Louis JV, Dilworth S, Goris J, Janssens V. (2007). Selection of protein phosphatase 2A regulatory subunits is mediated by the C terminus of the catalytic subunit. J Biol Chem 282: 26971-26980.
29. Martin D, Rojo AI, Salinas M, Diaz R, Gallardo G, Alam J et al. (2004). Regulation of heme oxygenase-1 expression through the Phosphatidylinositol 3-kinase/Akt pathway and the Nrf2 transcription factor in response to the antioxidant phytochemical carnosol. J Biol Chem 279: 8919-8929.
30. Matsuoka Y, Nagahara Y, Ikekita M, Shinomiya T. (2003). A novel immunosuppressive agent FTY720 induced Akt dephosphorylation in leukemia cells. Br J Pharmacol 138: 1303-1312.
31. Moody TW, Switzer C, Santana-Flores W, Ridnour LA, Berna M, Thill M et al. (2009). Dithiolethione modified valproate and diclofenac increase E-cadherin expression and decrease proliferation of non-small cell lung cancer cells. Lung Cancer; doi:10.1016/ j.lungcan.2009.06.012.
32. Paugh SW, Cassidy MP, He H, Milstien S, Sim-Selley LJ, Spiegel S et al. (2006). Sphingosine and its analog, the immunosuppressant 2-amino-2-(2-[4- octylphenyl]ethyl)-1,3-propanediol, interact with the CB1 cannabinoid receptor. Mol Pharmacol 70: 41-50.
33. Perrotti D, Neviani P. (2008). Protein phosphatase 2A (PP2A), a drugable tumor suppressor in Ph1(+) leukemias. Cancer Metastasis Rev 27: 159-168.
34. Persad S, Dedhar S. (2003). The role of integrin-linked kinase (ILK) in cancer progression. Cancer Metastasis Rev 22: 375-384.
35. Prickett TD, Brautigan DL. (2006). The {alpha}4 regulatory subunit exerts opposing allosteric effects on protein phosphatases PP6 and PP2A. J Biol Chem 281: 30503-30511.
36. Qiao M, Sheng S, Pardee AB. (2008). Metastasis and AKT activation. Cell Cycle 7: 2991-2996.
37. Resjo S, Goransson O, Harndahl L, Zolnierowicz S, Manganiello V, Degerman E. (2002). Protein phosphatase 2A is the main phosphatase involved in the regulation of protein kinase B in rat adipocytes. Cell Signal 14: 231-238. (Pubitemid 34102452)
38. Rocher G, Letourneux C, Lenormand P, Porteu F. (2007). Inhibition of B56-containing protein phosphatase 2As by the early response gene IEX-1 leads to control of Akt activity. J Biol Chem 282: 5468-5477.
39. Sablina AA, Chen W, Arroyo JD, Corral L, Hector M, Bulmer SE et al. (2007). The tumor suppressor PP2A A[beta] regulates the RalA GTPase. Cell 129: 969-982.
40. Sarnataro D, Pisanti S, Santoro A, Gazzerro P, Malfitano AM, Laezza C et al. (2006). The Cannabinoid CB1 receptor antagonist rimonabant (SR141716) inhibits human breast cancer cell proliferation through a lipid raft-mediated mechanism. Mol Pharmacol 70: 1298-1306.
41. Sato S, Fujita N, Tsuruo T. (2000). Modulation of Akt kinase activity by binding to Hsp90. Proce Natl Acad Sci USA 97: 10832-10837.
42. Sawai H, Okada Y, Funahashi H, Matsuo Y, Takahashi H, Takeyama H et al. (2006). Integrin-linked kinase activity is associated with interleukin-1[alpha]- induced progressive behavior of pancreatic cancer and poor patient survival. Oncogene 25: 3237-3246.
43. Schmidt A, Wenzel D, Thorey I, Sasaki T, Hescheler J, Timpl R et al. (2006). Endostatin influences endothelial morphology via the activated ERK1/2-kinase endothelial morphology and signal transduction. Microvasc Res 71: 152-162.
44. Trotta R, Ciarlariello D, Col JD, Allard II J, Neviani P, Santhanam R et al. (2007). The PP2A inhibitor SET regulates natural killer cell IFN-{gamma} production. J Exp Med 204: 2397-2405.
45. Ugi S, Imamura T, Maegawa H, Egawa K, Yoshizaki T, Shi K et al. (2004). Protein phosphatase 2A negatively regulates insulin's metabolic signaling pathway by inhibiting Akt (protein kinase B) activity in 3T3-L1 adipocytes. Mol Cell Biol 24: 8778-8789.
46. Ugi S, Imamura T, Ricketts W, Olefsky JM. (2002). Protein phosphatase 2A forms a molecular complex with Shc and regulates Shc tyrosine phosphorylation and downstream mitogenic signaling. Mol Cell Biol 22: 2375-2387.
47. Xing Y, Li Z, Chen Y, Stock JB, Jeffrey PD, Shi Y. (2008). Structural mechanism of demethylation and inactivation of protein phospha-tase 2A. Cell 133: 154-163.
48. Yuan TL, Cantley LC. (2008). PI3K pathway alterations in cancer: variations on a theme. Oncogene 27: 5497-5510.
49. Zhang Y, Munday R. (2008). Dithiolethiones for cancer chemopreven-tion: where do we stand? Mol Cancer Ther 7: 3470-3479.