A new water soluble MAPK activator exerts antitumor activity in melanoma cells resistant to the BRAF inhibitor vemurafenib

Biochemical Pharmacology

Volumn 95, Issue 1, 2015, Pages 16-27

  Graziani, Grazia ^a   Artuso, Simona ^b   De Luca, Anastasia ^a   Muzi, Alessia ^a   Rotili, Dante ^c   Scimeca, Manuel ^a   Atzori, Maria Grazia ^a   Ceci, Claudia ^a   Mai, Antonello ^c   Leonetti, Carlo ^b   Levati, Lauretta ^d   Bonanno, Elena ^a   Tentori, Lucio ^a   Caccuri, Anna Maria ^a  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

^b REGINA ELENA NATIONAL CANCER INSTITUTE   (Italy)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d LABORATORIO DI PATOLOGIA VASCOLARE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

6-(7-NITRO-2,1,3-BENZOXADIAZOL-4-YLTHIO)HEXANOL; ANTINEOPLASTIC AGENT; B RAF KINASE; BRAF PROTEIN, HUMAN; INDOLE DERIVATIVE; OXADIAZOLE DERIVATIVE; PROTEIN KINASE INHIBITOR; SULFONAMIDE; VEMURAFENIB; WATER;

ANIMAL; ANTAGONISTS AND INHIBITORS; DOSE RESPONSE; DRUG EFFECTS; DRUG RESISTANCE; DRUG SCREENING; ENZYME ACTIVATION; HUMAN; MALE; MELANOMA; METABOLISM; MOUSE; NUDE MOUSE; PHYSIOLOGY; PROCEDURES; SIGNAL TRANSDUCTION; SOLUBILITY; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG RESISTANCE, NEOPLASM; ENZYME ACTIVATION; HUMANS; INDOLES; MALE; MAP KINASE SIGNALING SYSTEM; MELANOMA; MICE; MICE, NUDE; OXADIAZOLES; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS B-RAF; SOLUBILITY; SULFONAMIDES; WATER; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84930886228     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2015.03.004     Document Type: Article

References (43)

1. G. Graziani, L. Tentori, and P. Navarra Ipilimumab: a novel immunostimulatory monoclonal antibody for the treatment of cancer Pharmacol. Res. 65 2012 9 22
2. L. Tentori, P.M. Lacal, and G. Graziani Challenging resistance mechanisms to therapies for metastatic melanoma Trends Pharmacol. Sci. 34 2013 656 666
3. G. Ricci, F. De Maria, G. Antonini, P. Turella, A. Bullo, and L. Stella 7-Nitro-2,1,3-benzoxadiazole derivatives, a new class of suicide inhibitors for glutathione S-transferases. Mechanism of action of potential anticancer drugs J. Biol. Chem. 280 2005 26397 26405
4. P. Turella, G. Filomeni, M.L. Dupuis, M.R. Ciriolo, A. Molinari, and F. De Maria A strong glutathione S-transferase inhibitor overcomes the P-glycoprotein-mediated resistance in tumor cells. 6-(7-Nitro-2,1,3-benzoxadiazol-4-ylthio)hexanol (NBDHEX) triggers a caspase-dependent apoptosis in MDR1-expressing leukemia cells J. Biol. Chem. 281 2006 23725 23732
5. F. Pellizzari Tregno, A. Sau, S. Pezzola, C. Geroni, C. Lapenta, and M. Spada In vitro and in vivo efficacy of 6-(7-nitro-2,1,3-benzoxadiazol-4-ylthio)hexanol (NBDHEX) on human melanoma Eur. J. Cancer 45 2009 2606 2617
6. M. Pasello, M.C. Manara, F. Michelacci, M. Fanelli, C.M. Hattinger, and G. Nicoletti Targeting glutathione-S transferase enzymes in musculoskeletal sarcomas: a promising therapeutic strategy Anal. Cell. Pathol. (Amst.) 34 2011 131 145
7. A. Sau, G. Filomeni, S. Pezzola, S. D'Aguanno, F.P. Tregno, and A. Urbani Targeting GSTP 1-1 induces JNK activation and leads to apoptosis in cisplatin-sensitive and -resistant human osteosarcoma cell lines Mol. Biosyst. 8 2012 994 1006
8. A. De Luca, F. Pellizzari Tregno, A. Sau, A. Pastore, C. Palumbo, and A. Alama Glutathione S-transferase P 1-1 as a target for mesothelioma treatment Cancer Sci. 104 2013 223 230
9. J.D. Hayes, J.U. Flanagan, and I.R. Jowsey Glutathione transferases Annu. Rev. Pharmacol. Toxicol. 45 2005 51 88
10. K.D. Tew, and Z. Ronai GST function in drug and stress response Drug Resist. Updat. 2 1999 143 147
11. E. Laborde Glutathione transferases as mediators of signaling pathways involved in cell proliferation and cell death Cell Death Differ. 17 2010 1373 1380
12. V. Adler, Z. Yin, S.Y. Fuchs, M. Benezra, L. Rosario, and K.D. Tew Regulation of JNK signaling by GSTp EMBO J. 18 1999 1321 1334
13. P. Turella, C. Cerella, G. Filomeni, A. Bullo, F. De Maria, and L. Ghibelli Proapoptotic activity of new glutathione S-transferase inhibitors Cancer Res. 65 2005 3751 3761
14. A. De Luca, L. Federici, M. De Canio, L. Stella, and A.M. Caccuri New insights into the mechanism of JNK1 inhibition by glutathione transferase P 1-1 Biochemistry 51 2012 7304 7312
15. Y. Wu, Y. Fan, B. Xue, L. Luo, J. Shen, and S. Zhang Human glutathione S-transferase P 1-1 interacts with TRAF2 and regulates TRAF2-ASK1 signals Oncogene 25 2006 5787 5800
16. A. De Luca, G. Mei, N. Rosato, E. Nicolai, L. Federici, and C. Palumbo The fine-tuning of TRAF2-GSTP 1-1 interaction: effect of ligand binding and in situ detection of the complex Cell Death Dis. 5 2014 e1015
17. H. Nishitoh, M. Saitoh, Y. Mochida, K. Takeda, H. Nakano, and M. Rothe ASK1 is essential for JNK/SAPK activation by TRAF2 Mol. Cell 2 1998 389 395
18. L. Tentori, A.S. Dorio, E. Mazzon, A. Muzi, A. Sau, and S. Cuzzocrea The glutathione transferase inhibitor 6-(7-nitro-2,1,3-benzoxadiazol-4-ylthio)hexanol (NBDHEX) increases temozolomide efficacy against malignant melanoma Eur. J. Cancer 47 2011 1219 1230
19. D. Rotili, A. De Luca, D. Tarantino, S. Pezzola, M. Forgione, and B. Morozzo della Rocca Synthesis and structure-activity relationship of new cytotoxic agents targeting human glutathione-S-transferases Eur. J. Med. Chem. 89 2015 156 171
20. A. De Luca, D. Rotili, D. Carpanese, A. Lenoci, L. Calderan, and M. Scimeca A novel orally active water-soluble inhibitor of human glutathione transferase exerts a potent and selective antitumor activity against human melanoma xenografts Oncotarget 2014 [Epub ahead of print]
21. K.S. Smalley, N.K. Haass, P.A. Brafford, M. Lioni, K.T. Flaherty, and M. Herlyn Multiple signaling pathways must be targeted to overcome drug resistance in cell lines derived from melanoma metastases Mol. Cancer Ther. 5 2006 1136 1144
22. H. Yang, B. Higgins, K. Kolinsky, K. Packman, Z. Go, and R. Iyer RG7204 (PLX4032), a selective BRAFV600E inhibitor, displays potent antitumor activity in preclinical melanoma models Cancer Res. 70 2010 5518 5527
23. L. Tentori, C. Leonetti, M. Scarsella, G. D'Amati, M. Vergati, and I. Portarena Systemic administration of GPI 15427, a novel poly(ADP-ribose) polymerase-1 inhibitor, increases the antitumor activity of temozolomide against intracranial melanoma, glioma, lymphoma Clin. Cancer Res. 9 2003 5370 5379
24. L. Tentori, A. Muzi, A.S. Dorio, S. Bultrini, E. Mazzon, and P.M. Lacal Stable depletion of poly (ADP-ribose) polymerase-1 reduces in vivo melanoma growth and increases chemosensitivity Eur. J. Cancer 44 2008 1302 1314
25. F. Su, W.D. Bradley, Q. Wang, H. Yang, L. Xu, and B. Higgins Resistance to selective BRAF inhibition can be mediated by modest upstream pathway activation Cancer Res. 72 2012 969 978
26. E. Castellano, and J. Downward RAS interaction with PI3K: more than just another effector pathway Genes Cancer. 2 2011 261 274
27. D.V. Bulavin, S. Saito, M.C. Hollander, K. Sakaguchi, C.W. Anderson, and E. Appella Phosphorylation of human p53 by p38 kinase coordinates N-terminal phosphorylation and apoptosis in response to UV radiation EMBO J. 18 1999 6845 6854
28. E. Appella, and C.W. Anderson Post-translational modifications and activation of p53 by genotoxic stresses Eur. J. Biochem. 268 2001 2764 2772
29. H. Davies, G.R. Bignell, C. Cox, P. Stephens, S. Edkins, and S. Clegg Mutations of the BRAF gene in human cancer Nature 417 2002 949 954
30. M.S. Brose, P. Volpe, M. Feldman, M. Kumar, I. Rishi, and R. Gerrero BRAF and RAS mutations in human lung cancer and melanoma Cancer Res. 62 2002 6997 7000
31. L. Boussemart, H. Malka-Mahieu, I. Girault, D. Allard, O. Hemmingsson, and G. Tomasic eIF4F is a nexus of resistance to anti-BRAF and anti-MEK cancer therapies Nature 513 2014 105 109
32. L.C. Vredeveld, P.A. Possik, M.A. Smit, K. Meissl, C. Michaloglou, and H.M. Horlings Abrogation of BRAFV600E-induced senescence by PI3K pathway activation contributes to melanomagenesis Genes Dev. 26 2012 1055 1069
33. K. Trunzer, A.C. Pavlick, L. Schuchter, R. Gonzalez, G.A. McArthur, and T.E. Hutson Pharmacodynamic effects and mechanisms of resistance to vemurafenib in patients with metastatic melanoma J. Clin. Oncol. 31 14 2013 1767 1774
34. J.S. Wilmott, V. Tembe, J.R. Howle, R. Sharma, J.F. Thompson, and H. Rizos Intratumoral molecular heterogeneity in a BRAF-mutant, BRAF inhibitor-resistant melanoma: a case illustrating the challenges for personalized medicine Mol. Cancer Ther. 11 2012 2704 2708
35. M.A. Wilson, F. Zhao, R. Letrero, K. D'Andrea, D.L. Rimm, and J.M. Kirkwood Correlation of somatic mutations and clinical outcome in melanoma patients treated with carboplatin, paclitaxel, and sorafenib Clin. Cancer Res. 20 2014 3328 3337
36. E. Shtivelman, M.Q. Davies, P. Hwu, J. Yang, M. Lotem, and M. Oren Pathways and therapeutic targets in melanoma Oncotarget 5 2014 1701 1752
37. J.L. Perfettini, M. Castedo, R. Nardacci, F. Ciccosanti, P. Boya, and T. Roumier Essential role of p53 phosphorylation by p38 MAPK in apoptosis induction by the HIV-1 envelope J. Exp. Med. 201 2005 279 289
38. L. Smeenk, S.J. van Heeringen, M. Koeppel, B. Gilbert, E. Janssen-Megens, and H.G. Stunnenberg Role of p53 serine 46 in p53 target gene regulation PLoS ONE 6 2011 e17574
39. P.S. Gowda, F. Zhou, L.V. Chadwell, and D.G. McEwen p53 binding prevents phosphatase-mediated inactivation of diphosphorylated c-Jun N-terminal kinase J. Biol. Chem. 287 2012 17554 17567
40. S. Cagnol, and J.C. Chambard ERK and cell death: mechanisms of ERK-induced cell death - apoptosis, autophagy and senescence FEBS J. 277 2010 2 21
41. V. Baud, Z.G. Liu, B. Bennett, N. Suzuki, Y. Xia, and M. Karin Signaling by proinflammatory cytokines: oligomerization of TRAF2 and TRAF6 is sufficient for JNK and IKK activation and target gene induction via an amino-terminal effector domain Genes Dev. 13 1999 1297 1308
42. M. Karandikar, S. Xu, and M.H. Cobb MEKK1 binds raf-1 and the ERK2 cascade components J. Biol. Chem. 275 2000 40120 40127
43. B. Bjorkblom, J.C. Vainio, V. Hongisto, T. Herdegen, M.J. Courtney, and E.T. Coffey All JNKs can kill, but nuclear localization is critical for neuronal death J. Biol. Chem. 283 2008 19704 19713