Nitric oxide donors: Spermine/NO and diethylenetriamine/NO induce ovarian cancer cell death and affect STAT3 and AKT signaling proteins

Nitric Oxide - Biology and Chemistry

Volumn 35, Issue , 2013, Pages 93-109

  Kielbik, Michal ^a   Klink, Magdalena ^a   Brzezinska, Marta ^a   Szulc, Izabela ^a   Sulowska, Zofia ^a  

^a INSTITUTE OF MEDICAL BIOLOGY   (Poland)

Author keywords

Cytotoxicity; Nitric oxide; Ovarian cancer cells; Signaling proteins

Indexed keywords

4 [[(4 METHYLPHENYL)SULFONYLOXY]ACETAMIDO]SALICYLIC ACID; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; DIETHYLENETRIAMINE; NITRIC OXIDE; NITRITE; PROTEIN KINASE B; SPERMINE; STAT3 PROTEIN; TRICIRIBINE; 1-HYDROXY-2-OXO-3,3-BIS(2-AMINOETHYL)-1-TRIAZENE; AMINOSALICYLIC ACID DERIVATIVE; BENZENESULFONIC ACID DERIVATIVE; NITRIC OXIDE DONOR; PROTEASOME; SPERMINE NITRIC OXIDE COMPLEX; STAT3 PROTEIN, HUMAN; TRIAZENE DERIVATIVE;

APOPTOSIS; ARTICLE; CANCER CELL; CANCER CELL CULTURE; CELL DEATH; CONTROLLED STUDY; FEMALE; HALF LIFE TIME; HUMAN; HUMAN CELL; OVARY CANCER; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; WESTERN BLOTTING; ANALOGS AND DERIVATIVES; CELL SURVIVAL; DRUG EFFECTS; METABOLISM; NONPARAMETRIC TEST; OVARY TUMOR; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

AMINOSALICYLIC ACIDS; APOPTOSIS; BENZENESULFONATES; CELL LINE, TUMOR; CELL SURVIVAL; FEMALE; HUMANS; NITRIC OXIDE DONORS; NITRITES; OVARIAN NEOPLASMS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; SPERMINE; STAT3 TRANSCRIPTION FACTOR; STATISTICS, NONPARAMETRIC; TRIAZENES;

EID: 84884941113     PISSN: 10898603     EISSN: 10898611     Source Type: Journal    
DOI: 10.1016/j.niox.2013.09.001     Document Type: Article

References (55)

1. H. Yu, M. Kortylewski, and D. Pardoll Crosstalk between cancer and immune cells: role of STAT3 in the tumour microenvironment Nat. Rev. Immunol. 7 1 2007 41 51 (Pubitemid 46020826)
2. J.G. Paez, and W.R. Sellers PI3K/PTEN/AKT pathway. A critical mediator of oncogenic signaling Cancer Treat. Res. 115 2003 145 167
3. M. Kortylewski, and H. Yu Role of Stat3 in suppressing anti-tumor immunity Curr. Opin. Immunol. 20 2 2008 228 233
4. S. Huang Regulation of metastases by signal transducer and activator of transcription 3 signaling pathway: clinical implications Clin. Cancer Res. 13 5 2007 1362 1366 (Pubitemid 46450423)
5. T. Wang, G. Niu, M. Kortylewski, L. Burdelya, K. Shain, S. Zhang, R. Bhattacharya, D. Gabrilovich, R. Heller, D. Coppola, W. Dalton, R. Jove, D. Pardoll, and H. Yu Regulation of the innate and adaptive immune response by Stat-3 signaling in tumor cells Nat. Med. 10 2004 48 54 (Pubitemid 38524698)
6. A. Carnero The PKB/AKT pathway in cancer Curr. Pharm. Des. 16 1 2010 34 44
7. B.D. Manning, and L.C. Cantley AKT/PKB signaling: navigating downstream Cell 129 2007 1261 1274 (Pubitemid 46962095)
8. B. Bonavida, S. Baritaki, S. Huerta-Yepez, M.I. Vega, D. Chatterjee, and K. Yeung Novel therapeutic applications of nitric oxide donors in cancer: roles in chemo- and immunosensitization to apoptosis and inhibition of metastases Nitric Oxide 19 2008 152 157
9. P.K.M. Kim, R. Zamora, P. Petrosko, and T.R. Billiar The regulatory role of nitric oxide in apoptosis Int. Immunopharmacol. 1 2001 1421 1441 (Pubitemid 32622788)
10. J.W. Coleman Nitric oxide in immunity and inflammation Int. Immunopharmacol. 1 2001 1397 1406 (Pubitemid 32622786)
11. F. Murad Cellular signaling with nitric oxide and cyclic GMP Braz. J. Med. Biol. Res. 32 1999 1317 1327 (Pubitemid 129544249)
12. H.P. Monteiro Signal transduction by protein tyrosine nitration: competition or cooperation with tyrosine phosphorylation-dependent signaling events? Free Radic. Biol. Med. 33 6 2002 765 773 (Pubitemid 35232312)
13. G.C. Brown, and V. Borutaite Nitric oxide inhibition of mitochondrial respiration and its role in cell death Free Radic. Biol. Med. 33 11 2002 1440 1450 (Pubitemid 35351587)
14. L. Leon, J.F. Jeannin, and A. Bettaieb Post-translational modifications induced by nitric oxide (NO): implication in cancer cell apoptosis Nitric Oxide 19 2 2008 77 83
15. G.A. Blaise, D. Gauvin, M. Gangal, and S. Authier Nitric oxide, cell signaling and cell death Toxicology 208 2 2005 177 192 (Pubitemid 40187330)
16. J.B. Mannick, C. Schonhoff, N. Papeta, P. Ghafourifar, M. Szibor, K. Fang, and B. Gaston S-nitrosylation of mitochondrial caspases J. Cell Biol. 154 6 2001 1111 1116 (Pubitemid 34286189)
17. Y. Meajima, S. Adachi, K. Morikawa, H. Ito, and M. Isobe Nitric oxide inhibits myocardial apoptosis by preventingcaspase-3 activity via S-nitrosylation J. Mol. Cell. Cardiol. 38 1 2005 163 174 (Pubitemid 40038663)
18. M.R. Miller, and I.L. Megson Recent developments in nitric oxide donor drugs Br. J. Pharmacol. 151 2007 305 321 (Pubitemid 46842668)
19. G.H. Liu, S.R. Wang, B. Wang, and B.H. Kong Inhibition of nuclear factor-kappaB by an antioxidant enhances paclitaxel sensitivity in ovarian carcinoma cell line Int. J. Gynecol. Cancer 16 5 2006 1777 1782 (Pubitemid 44470035)
20. E. Maneiro, M.J. López-Armada, M.C. de Andres, B. Caramés, M.A. Martín, A. Bonilla, P. Del Hoyo, F. Galdo, J. Arenas, and F.J. Blanco Effect of nitric oxide on mitochondrial respiratory activity of human articular chondrocytes Ann. Rheum. Dis. 64 2005 388 395 (Pubitemid 40283048)
21. B. Cillero-Pastor, M.A. Martin, J. Arenas, M.J. López-Armada, and F.J. Blanco Effect of nitric oxide on mitochondrial activity of human synovial cells BMC Musculoskelet. Disord. 12 42 2011 10.1186/1471-2474-12-42
22. D. Hirst, and T. Robson Nitric oxide in cancer therapeutics: interaction with cytotoxic chemotherapy Curr. Pharm. Des. 16 4 2010 411 420
23. S. Huerta, S. Chilka, and B. Bonavida Nitric oxide donors: novel cancer therapeutics (review) Int. J. Oncol. 33 5 2008 909 927
24. G. Fotakis, and J.A. Timbrell In vitro cytotoxicity assays: comparison of LDH, neutral red, MTT and protein assay in hepatoma cell lines following exposure to cadmium chloride Toxicol. Lett. 160 2006 171 177 (Pubitemid 41578961)
25. J. Weyermann, D. Lochmann, and A. Zimmer A practical note on the use of cytotoxicity assays Int. J. Pharm. 288 2 2005 369 376 (Pubitemid 40038590)
26. K. Chiba, K. Kawakami, and K. Tohyama Simultaneous evaluation of cell viability by neutral red, MTT and crystal Violet staining assays of the same cells Toxicol. In Vitro 12 3 1998 251 258 (Pubitemid 28331388)
27. D.I. Bounous, R.P. Campagnoli, and J. Brown Comparison of MTT colorimetric assay and tritiated thymidine uptake for lymphocyte proliferation assays using chicken splenocytes Avian Dis. 36 1992 1022 1027
28. S.K. Bopp, and T. Lettieri Comparison of four different colorimetric and fluorometric cytotoxicity assays in a zebrafish liver cell line BMC Pharmacol. 30 2008 10.1186/1471-2210-8-8 (Pubitemid 351917427)
29. A.M. Rieger, K.L. Nelson, J.D. Konowalchuk, D.R. Barreda, Modified annexin V/propidium iodide apoptosis assay for accurate assessment of cell death, J. Vis. Exp. 50 (2011) doi:pii:2597.10.3791/2597.
30. D.J. Granville, and R.A. Gottlieb Mitochondria: regulators of cell death and survival Sci. World J. 2 2002 1569 1578
31. C.Q. Li, and G.N. Wogan Nitric oxide as a modulator of apoptosis Cancer Lett. 226 1 2005 1 16
32. F.J. Blanco, M.J. López-Armada, and E. Maneiro Mitochondrial dysfunction in osteoarthritis Mitochondrion 4 5-6 2004 715 728 (Pubitemid 39646817)
33. M. Brunori, E. Forte, M. Arese, D. Mastronicola, A. Giuffrè, and P. Sarti Nitric oxide and the respiratory enzyme Biochim. Biophys. Acta 1757 2006 1144 1154 (Pubitemid 44442121)
34. R. Radi, A. Cassino, R. Hodara, C. Quijano, and L. Castro Peroxynitrite reactions and formation in mitochondria Free Radic. Biol. Med. 33 11 2002 1451 1464 (Pubitemid 35351588)
35. V. Nikoletopoulou, M. Markaki, K. Palikaras, and N. Tavernarakis Crosstalk between apoptosis, necrosis and autophagy Biochim. Biophys. Acta 2013 10.1016/j.bbamcr.2013.06.001
36. J. Karar, A. Maity, PI3K/AKT/mTOR pathway in angiogenesis, Front. Mol. Neurosci. 4(51) (2011) doi:10.3389/fnmol.2011.00051.
37. Z. Duan, R. Foster, D.A. Bell, J. Mahoney, K. Wolak, A. Vaidya, C. Hampel, H. Lee, and M.V. Seiden Signal transducers and activators of transcription 3 pathway activation in drug-resistant ovarian cancer Clin. Cancer Res. 12 17 2006 5055 5063 (Pubitemid 44453331)
38. C. Gest, P. Mirshahi, H. Li, L.L. Pritchard, U. Joimel, E. Blot, J. Chidiac, B. Poletto, J.P. Vannier, R. Varin, M. Mirshahi, L. Cazin, E. Pujade-Lauraine, J. Soria, and C. Soria Ovarian cancer: Stat3, RhoA and IGF-IR as therapeutic targets Cancer Lett. 317 2012 207 217
39. X. Zhang, P. Liu, B. Zhang, A. Wang, and M. Yang Role of STAT3 decoy oligodeoxynucleotides on cell invasion and chemosensitivity in human epithelial ovarian cancer cells Cancer Genet. Cytogenet. 197 2010 46 53
40. Y. Lu, H. Wang, and G.B. Mills Targeting PI3K-AKT pathway for cancer therapy Rev. Clin. Exp. Hematol. 7 2003 205 228 (Pubitemid 37466220)
41. D.A. Altomare, H.Q. Wang, K.L. Skele, A. de Rienzo, A.J. Klein-Szanto, A.K. Godwin, and J.R. Testa AKT and mTOR phosphorylation is frequently detected in ovarian cancer and can be targeted to disrupt ovarian tumor cell growth Oncogene 23 2004 5853 5857 (Pubitemid 39093031)
42. H. Schindler, and C. Bogdan NO as a signaling molecule: effects on kinases Int. Immunopharmacol. 1 2001 1443 1455 (Pubitemid 32622789)
43. S. Aznar, P.F. Valerón, S.V. del Rincon, L.F. Pérez, R. Perona, and J.C. Lacal Simultaneous tyrosine and serine phosphorylation of STAT3 transcription factor is involved in Rho A GTPase oncogenic transformation Mol. Biol. Cell 12 2001 3282 3294 (Pubitemid 33062979)
44. D.D. Sarbassov, D.A. Guertin, S.M. Ali, and D.M. Sabatini Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex Science 307 2005 1098 1101 (Pubitemid 40262113)
45. X. Wang, H. Sun, and C. Li Nitric oxide induces promyelocytic cell growth arrest and apoptosis through deactivation of Akt pathway Leuk. Res. 5 31 2006 653 660
46. J. Sang, Y. Chen, and Y. Tao Nitric oxide inhibits gastric cancer cell growth through the modulation of the Akt pathway Mol. Med. Rep. 4 6 2011 1163 1167
47. C. Evangelisti, F. Ricci, P. Tazzari, F. Chiarini, M. Battistelli, E. Falcieri, A. Ognibene, P. Pagliaro, L. Cocco, J.A. McCubrey, and A.M. Martelli Preclinical testing of the Akt inhibitor triciribine in T-cell acute lymphoblastic leukemia J. Cell. Physiol. 226 2011 822 831
48. K. Siddiquee, S. Zhang, W.C. Guida, M.A. Blaskovich, B. Greedy, H.R. Lawrence, M.L. Yip, R. Jove, M.M. McLaughlin, N.J. Lawrence, S.M. Sebti, and J. Turkson Selective chemical probe inhibitor of Stat3, identified through structure-based virtual screening, induces antitumor activity Proc. Natl. Acad. Sci. USA 18 104 2007 7391 7396 (Pubitemid 47185916)
49. J. Ma, S. Wang, M. Zhao, X.S. Deng, C.K. Lee, X.D. Yu, B. Liu, Therapeutic potential of cladribine in combination with STAT3 inhibitor against multiple myeloma, BMC Cancer 11 (2011) doi:10.1186/1471-2407-11-255.
50. C.R. Garret, D. Coppola, R.M. Wenham, C.L. Cubitt, A.M. Neuger, T.J. Frost, R.M. Rush, D.M. Sullivan, J.Q. Cheng, and S.M. Sebti Phase I pharmacokinetic and pharmacodynamic study or triciribine phosphate monohydrate, a small-molecule inhibitor of AKT phosphorylation, in adult subjects with solid tumors containing activated AKT Invest. New Drugs 29 2011 1381 1389
51. S.K. Kong, M.B. Yim, E.R. Stadtman, and P.B. Chock Peroxynitrite disables the tyrosine phosphorylation regulatory mechanism: lymphocyte-specific tyrosine kinase fails to phosphorylate nitrated cdc2(6-20)NH2 peptide Proc. Natl. Acad. Sci. USA 93 1996 3377 3382
52. C. Brito, M. Naviliat, A.C. Tiscornia, F. Vuillier, G. Gualco, G. Dighiero, R. Radi, and A.M. Cayota Peroxynitrite inhibits T lymphocyte activation and proliferation by promoting impairment of tyrosine phosphorylation and peroxynitrite-driven apoptotic death J. Immunol. 162 1999 3356 3366 (Pubitemid 29313585)
53. Y.T. Wu, W. Ouyang, A.S. Lazorchak, D. Liu, H.M. Shen, and B. Su MTOR complex 2 targets Akt for proteasomal degradation via phosphorylation at the hydrophobic motif J. Biol. Chem. 286 2011 14190 14198
54. H. Suita, M. Kaneki, S. Furuhashi, M. Hirota, H. Takamori, and H. Baba Nitric oxide inhibits the proliferation and invasion of pancreatic cancer cells through degradation of insulin receptor substrate-1 protein Mol. Cancer Res. 8 2010 1152 1163
55. C. Wojcik Regulation of apoptosis by the ubiquitin and proteasome pathway J. Cell Mol. Med. 6 1 2002 25 48 (Pubitemid 44133981)