Activation of Ras/PI3K/ERK pathway induces c-Myc stabilization to upregulate argininosuccinate synthetase, leading to arginine deiminase resistance in melanoma cells

Cancer Research

Volumn 72, Issue 10, 2012, Pages 2622-2633

  Tsai, Wen Bin ^a   Aiba, Isamu ^a   Long, Yan ^a   Lin, Hui Kuan ^a   Feun, Lynn ^b   Savaraj, Niramol ^b   Kuo, Macus Tien ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b UNIVERSITY OF MIAMI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE DEIMINASE; ARGININOSUCCINATE SYNTHASE; MITOGEN ACTIVATED PROTEIN KINASE; MYC PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; RAS PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER RESISTANCE; CELL KILLING; CONTROLLED STUDY; ENZYME ACTIVATION; FEMALE; MELANOMA; MELANOMA CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; ARGININOSUCCINATE SYNTHASE; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; GENES, RAS; HUMANS; HYDROLASES; MAP KINASE SIGNALING SYSTEM; MELANOMA; MICE; MICE, NUDE; PHOSPHATIDYLINOSITOL 3-KINASE; POLYETHYLENE GLYCOLS; PROTEIN STABILITY; PROTEOLYSIS; PROTO-ONCOGENE PROTEINS C-MYC; SIGNAL TRANSDUCTION; UBIQUITIN; UP-REGULATION;

EID: 84861154164     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-11-3605     Document Type: Article

References (49)

1. Blank CU, Hooijkaas AI, Haanen JB, Schumacher TN. Combination of targeted therapy and immunotherapy in melanoma. Cancer Immunol Immunother 2011;60:1359-71.
2. Gray-Schopfer V, Wellbrock C, Marais R. Melanoma biology and new targeted therapy. Nature 2007;445:851-7.
3. Feun L, Savaraj N. Topoisomerase I inhibitors for the treatment of brain tumors. Expert Rev Anticancer Ther 2008;8:707-16.
4. Kuo MT, Savaraj N, Feun LG. Targeted cellular metabolism for cancer chemotherapy with recombinant arginine-degrading enzymes. Onco-target 2010;1:246-51.
5. Ascierto PA, Scala S, Castello G, Daponte A, Simeone E, Ottaiano A, et al. Pegylated arginine deiminase treatment of patients with meta-static melanoma: results from phase I and II studies. J Clin Oncol 2005;23:7660-8. (Pubitemid 46291831)
6. Ni Y, Schwaneberg U, Sun ZH. Arginine deiminase, a potential anti-tumor drug. Cancer Lett 2008;261:1-11.
7. Cheng PN, Lam TL, Lam WM, Tsui SM, Cheng AW, Lo WH, et al. Pegylated recombinant human arginase (rhArg-peg5,000 mw) inhibits the in vitro and in vivo proliferation of human hepatocellular carcinoma through arginine depletion. Cancer Res 2007;67: 309-17. (Pubitemid 46142789)
8. Izzo F, Marra P, Beneduce G, Castello G, Vallone P, De Rosa V, et al. Pegylated arginine deiminase treatment of patients with unresectable hepatocellular carcinoma: results from phase I/II studies. J Clin Oncol 2004;22:1815-22. (Pubitemid 41095171)
9. Tsai WB, Aiba I, Lee SY, Feun L, Savaraj N, Kuo MT. Resistance to arginine deiminase treatment in melanoma cells is associated with induced argininosuccinate synthetase expression involving c-Myc/ HIF-1alpha/Sp4. Mol Cancer Ther 2009;8:3223-33.
10. Kuo MT, Liu Z, Wei Y, Lin-Lee YC, Tatebe S, Mills GB, et al. Induction of human MDR1 gene expression by 2-acetylaminofluorene is mediated by effectors of the phosphoinositide 3-kinase pathway that activate NF-kappaB signaling. Oncogene 2002;21:1945-54. (Pubitemid 34270883)
11. Feig LA, Cooper GM. Inhibition of NIH 3T3 cell proliferation by a mutant ras protein with preferential affinity for GDP. Mol Cell Biol 1988;8: 3235-43.
12. Pap M, Cooper GM. Role of glycogen synthase kinase-3 in the phosphatidylinositol 3-Kinase/Akt cell survival pathway. J Biol Chem 1998;273:19929-32. (Pubitemid 28377539)
13. Zhang D, Zaugg K, Mak TW, Elledge SJ. A role for the deubiquitinating enzyme USP28 in control of the DNA-damage response. Cell 2006; 126:529-42. (Pubitemid 44163600)
14. Cai Z, Semenza GL. PTEN activity is modulated during ischemia and reperfusion: involvement in the induction and decay of preconditioning. Circ Res 2005;97:1351-9.
15. Tsai WB, Chung YM, Zou Y, Park SH, Xu Z, Nakayama K, et al. Inhibition of FOXO3 tumor suppressor function by betaTrCP1 through ubiquitin-mediated degradation in a tumor mouse model. PLoS One 2010;5:e11171.
16. Hann SR, Eisenman RN. Proteins encoded by the human c-myc oncogene: differential expression in neoplastic cells. Mol Cell Biol 1984;4:2486-97. (Pubitemid 15212264)
17. Salghetti SE, Kim SY, Tansey WP. Destruction of Myc by ubiquitin-mediated proteolysis: cancer-associated and transforming mutations stabilize Myc. EMBO J 1999;18:717-26. (Pubitemid 29057256)
18. Thomas LR, Tansey WP. Proteolytic control of the oncoprotein transcription factor Myc. Adv Cancer Res 2010;110:77-106.
19. Yada M, Hatakeyama S, Kamura T, Nishiyama M, Tsunematsu R, Imaki H, et al. Phosphorylation-dependent degradation of c-Myc ismediated by the F-box protein Fbw7. EMBO J 2004;23:2116-25. (Pubitemid 38737738)
20. Popov N, Wanzel M, Madiredjo M, Zhang D, Beijersbergen R, Bernards R, et al. The ubiquitin-specific protease USP28 is required for MYC stability. Nat Cell Biol 2007;9:765-74. (Pubitemid 47019463)
21. Sears R, Nuckolls F, Haura E, Taya Y, Tamai K, Nevins JR. Multiple Ras-dependent phosphorylation pathways regulate Myc protein stability. Genes Dev 2000;14:2501-14.
22. Sears RC. The life cycle of C-myc: from synthesis to degradation. Cell Cycle 2004;3:1133-7. (Pubitemid 40268631)
23. Stambolic V, Ruel L, Woodgett JR. Lithium inhibits glycogen synthase kinase-3 activity and mimics wingless signalling in intact cells. Curr Biol 1996;6:1664-8. (Pubitemid 27050234)
24. Maehama T, Dixon JE. The tumor suppressor, PTEN/MMAC1, dephosphorylates the lipid second messenger, phosphatidylinositol 3,4,5-trisphosphate. J Biol Chem 1998;273:13375-8. (Pubitemid 28268370)
25. Vazquez F, Sellers WR. The PTEN tumor suppressor protein: an antagonist of phosphoinositide 3-kinase signaling. Biochim Biophys Acta 2000;1470:M21-35. (Pubitemid 30070165)
26. Berggren M, Sittadjody S, Song Z, Samira JL, Burd R, Meuillet EJ. Sodium selenite increases the activity of the tumor suppressor protein, PTEN, in DU-145 prostate cancer cells. Nutr Cancer 2009; 61:322-31.
27. Workman P, Clarke PA, Raynaud FI, van Montfort RL. Drugging the PI3 kinome: from chemical tools to drugs in the clinic. Cancer Res 2010;70:2146-57.
28. Calleja V, Laguerre M, Parker PJ, Larijani B. Role of a novel PH-kinase domain interface in PKB/Akt regulation: structural mechanism for allosteric inhibition. PLoS Biol 2009;7:e17.
29. Gills JJ, Dennis PA. Perifosine: update on a novel Akt inhibitor. Curr Oncol Rep 2009;11:102-10.
30. Fernandez PC, Frank SR, Wang L, Schroeder M, Liu S, Greene J, et al. Genomic targets of the human c-Myc protein. Genes Dev 2003;17: 1115-29. (Pubitemid 36534986)
31. Li Z, Van Calcar S, Qu C, Cavenee WK, Zhang MQ, Ren B. A global transcriptional regulatory role for c-Myc in Burkitt's lymphoma cells. Proc Natl Acad Sci U S A 2003;100:8164-9. (Pubitemid 36842516)
32. Gordan JD, Thompson CB, Simon MC. HIF and c-Myc: sibling rivals for control of cancer cell metabolism and proliferation. Cancer Cell 2007;12:108-13. (Pubitemid 47199124)
33. Wolfer A, Ramaswamy S. MYC and metastasis. Cancer Res 2011; 71:2034-7.
34. Popov N, Herold S, Llamazares M, Schulein C, Eilers M. Fbw7 and Usp28 regulate myc protein stability in response to DNA damage. Cell Cycle 2007;6:2327-31. (Pubitemid 350058681)
35. Ilic N, Utermark T, Widlund HR, Roberts TM. PI3K-targeted therapy can be evaded by gene amplification along the MYC-eukaryotic translation initiation factor 4E (eIF4E) axis. Proc Natl Acad Sci U S A 2011;108: E699-708.
36. Muellner MK, Uras IZ, Gapp BV, Kerzendorfer C, Smida M, Lechtermann H, et al. A chemical-genetic screen reveals a mechanism of resistance to PI3K inhibitors in cancer. Nat Chem Biol 2011;7: 787-93.
37. Liu P, Cheng H, Santiago S, Raeder M, Zhang F, Isabella A, et al. Oncogenic PIK3CA-driven mammary tumors frequently recur via PI3K pathway-dependent and PI3K pathway-independent mechanisms. Nat Med 2011;17:1116-20.
38. Bamford S, Dawson E, Forbes S, Clements J, Pettett R, Dogan A, et al. The COSMIC (Catalogue of Somatic Mutations in Cancer) database and website. Br J Cancer 2004;91:355-8. (Pubitemid 39037083)
39. Bowles DW, Jimeno A. New phosphatidylinositol 3-kinase inhibitors for cancer. Expert Opin Investig Drugs 2011;20:507-18.
40. Pal SK, Reckamp K, Yu H, Figlin RA. Akt inhibitors in clinical development for the treatment of cancer. Expert Opin Investig Drugs 2010;19:1355-66.
41. Chin L, Andersen JN, Futreal PA. Cancer genomics: from discovery science to personalized medicine. Nat Med 2011;17:297-303.
42. Flaherty KT, Puzanov I, Kim KB, Ribas A, McArthur GA, Sosman JA, et al. Inhibition of mutated, activated BRAF in metastatic melanoma. N Engl J Med 2010;363:809-19.
43. Nazarian R, Shi H, Wang Q, Kong X, Koya RC, Lee H, et al. Melanomas acquire resistance to B-RAF(V600E) inhibition by RTK or N-RAS upregulation. Nature 2010;468:973-7.
44. Johannessen CM, Boehm JS, Kim SY, Thomas SR, Wardwell L, Johnson LA, et al. COT drives resistance to RAF inhibition through MAP kinase pathway reactivation. Nature 2010;468:968-72.
45. Villanueva J, Vultur A, Lee JT, Somasundaram R, Fukunaga-Kalabis M, Cipolla AK, et al. Acquired resistance to BRAF inhibitors mediated by a RAF kinase switch in melanoma can be overcome by cotargeting MEK and IGF-1R/PI3K. Cancer Cell 2010;18:683-95.
46. Tsui SM, Lam WM, Lam TL, Chong HC, So PK, Kwok SY, et al. Pegylated derivatives of recombinant human arginase (rhArg1) for sustained in vivo activity incancer therapy: preparation,characterization and analysis of their pharmacodynamics in vivo and in vitro and action upon hepatocellular carcinoma cell (HCC). Cancer Cell Int 2009;9:9.
47. Agrawal V, Woo JH, Mauldin JP, Jo C, Stone EM, Georgiou G, et al. Cytotoxicity of human recombinant arginase I (Co)-PEG5000 in the presence of supplemental L-citrulline is dependent on decreased argininosuccinate synthetase expression in human cells. Anticancer Drugs 2011;23:51-64.
48. Lam TL, Wong GK, Chow HY, Chong HC, Chow TL, Kwok SY, et al. Recombinant human arginase inhibits the in vitro and in vivo proliferation of human melanoma by inducing cell cycle arrest and apoptosis. Pigment Cell Melanoma Res 2010;24:366-76.
49. Stone EM, Glazer ES, Chantranupong L, Cherukuri P, Breece RM, Tierney DL, et al. Replacing Mn(2+) with Co(2+) in human arginase i enhances cytotoxicity toward l-arginine auxotrophic cancer cell lines. ACS Chem Biol 2010;5:333-42.