Cytotoxic and immune-sensitizing properties of nitric oxide-modified saquinavir in iNOS-positive human melanoma cells

Journal of Cellular Physiology

Volumn 226, Issue 7, 2011, Pages 1803-1812

  Mijatovic, Sanja ^a   Maksimovic Ivanic, Danijela ^a   Mojic, Marija ^a   Timotijevic, Gordana ^b   Miljkovic, Djordje ^a   Mangano, Katia ^c   Donia, Marco ^c   Di Cataldo, Antonio ^c   Al Abed, Yousef ^d   Cheng, Kai Fan ^d   Stosic Grujicic, Stanislava ^a   Nicoletti, Ferdinando ^c  

^a UNIVERSITY OF BELGRADE   (Serbia)

^b Belgrade University   (Serbia)

^c UNIVERSITY OF CATANIA   (Italy)

^d FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INDUCIBLE NITRIC OXIDE SYNTHASE; MITOGEN ACTIVATED PROTEIN KINASE; NITRIC OXIDE; NITRIC OXIDE PLUS SAQUINAVIR; PROTEIN KINASE B; SAQUINAVIR; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG EFFECT; HUMAN; HUMAN CELL; MALE; MELANOMA; MELANOMA CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSCRIPTION REGULATION; UPREGULATION;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; DOSE-RESPONSE RELATIONSHIP, DRUG; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; MALE; MELANOMA; MICE; MICE, NUDE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, TNF-RELATED APOPTOSIS-INDUCING LIGAND; SAQUINAVIR; TIME FACTORS; TNF-RELATED APOPTOSIS-INDUCING LIGAND; UP-REGULATION; XENOGRAFT MODEL ANTITUMOR ASSAYS; YY1 TRANSCRIPTION FACTOR;

MUS MUSCULUS;

EID: 79955042497     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.22513     Document Type: Article

References (49)

1. Boshoff C, Weiss R. 2002. AIDS-related malignancies. Nat Rev Cancer 2: 373-382.
2. Castellano G, Torrisi E, Ligresti G, Malaponte G, Militello L, Russo AE, Mccubrey JA, Canevari S, Libra M. 2009. The involvement of the transcription factor Yin Yang 1 in cancer development and progression. Cell Cycle 8: 1367-1372.
3. Cha YI, Dubois RN. 2007. NSAIDs and cancer prevention: Targets downstream of COX-2. Annu Rev Med 58: 239-252.
4. Chawla-Sarkar M, Bauer JA, Lupica JA, Morrison BH, Tang Z, Oates RK, Almasan A, Didonato JA, Borden EC, Lindner DJ. 2003. Suppression of NF-kappa B survival signaling by nitrosylcobalamin sensitizes neoplasms to the anti-tumor effects of Apo2L/TRAIL. J Biol Chem 278: 39461-39469.
5. Chow WA, Jiang C, Guan M. 2009. Anti-HIV drugs for cancer therapeutics: Back to the future? Lancet Oncol 10: 61-71.
6. Ekmekcioglu S, Ellerhorst J, Smid CM, Prieto VG, Munsell M, Buzaid AC, Grimm EA. 2000. Inducible nitric oxide synthase and nitrotyrosine in human metastatic melanoma tumors correlate with poor survival. Clin Cancer Res 6: 4768-4775.
7. Geusens P. 2009. Naproxcinod, a new cyclooxygenase-inhibiting nitric oxide donator (CINOD). Expert Opin Biol Ther 9: 649-657.
8. Gordon S, Akopyan G, Garban H, Bonavida B. 2006. Transcription factor YY1 structure, function, and therapeutic implications in cancer biology. Oncogene 25: 1125-1142.
9. Griffith TS, Chin WA, Jackson GC, Lynch DH, Kubin MZ. 1998. Intracellular regulation of TRAIL-induced apoptosis in human melanoma cells. J Immunol 161: 2833-2840.
10. Grimm EA, Ellerhorst J, Tang CH, Ekmekcioglu S. 2008. Constitutive intracellular production of iNOS and NO in human melanoma: Possible role in regulation of growth and resistance to apoptosis. Nitric Oxide 19: 133-137.
11. Gupta AK, Cerniglia GJ, Mick R, Mckenna WG, Muschel RJ. 2005. HIV protease inhibitors block Akt signaling and radiosensitize tumor cells both in vitro and in vivo. Cancer Res 65: 8256-8265.
12. Halama N, Zoernig I, Jaeger D. 2010. Advanced malignant melanoma: Immunologic and multimodal therapeutic strategies. J Oncol 2010: 689893.
13. Hayashi H, Matsuzaki O, Muramatsu S, Tsuchiya Y, Harada T, Suzuki Y, Sugano S, Matsuda A, Nishida E. 2006. Centaurin-α1 is a phosphatidylinositol 3-kinase-dependent activator of ERK1/2 mitogen-activated protein kinases. J Biol Chem 281: 1332-1337.
14. Hayashi H, Tsuchiya Y, Nakayama K, Satoh T, Nishida E. 2008. Down-regulation of the PI3-kinase/Akt pathway by ERK MAP kinase in growth factor signaling. Genes Cells 13: 941-947.
15. Hersey P, Zhang XD. 2001. How melanoma cells evade trail-induced apoptosis. Nat Rev Cancer 1: 142-150.
16. Hongo F, Garban H, Huerta-Yepez S, Vega M, Jazirehi AR, Mizutani Y, Miki T, Bonavida B. 2005. Inhibition of the transcription factor Yin Yang 1 activity by S-nitrosation. Biochem Biophys Res Commun 336: 692-701.
17. Huerta-Yepez S, Vega M, Escoto-Chavez SE, Murdock B, Sakai T, Baritaki S, Bonavida B. 2009. Nitric oxide sensitizes tumor cells to TRAIL-induced apoptosis via inhibition of the DR5 transcription repressor Yin Yang 1. Nitric Oxide 20: 39-52.
18. International Collaboration on HIV and Cancer, 2000. 2000. Highly active antiretroviral therapy and incidence of cancer in human immunodeficiency virus-infected adults. J Natl Cancer Inst 92: 1823-1830.
19. Kaludjerovic GN, Miljkovic D, Momcilovic M, Djinovic VM, Mostarica Stojkovic M, Sabo TJ, Trajkovic V. 2005. Novel platinum(IV) complexes induce rapid tumor cell death in vitro. Int J Cancer 116: 479-486.
20. Koblish HK, Zhao S, Franks CF, Donatelli RR, Tominovich RM, Lafrance LV, Leonard KA, Gushue JM, Parks DJ, Calvo RR, Milkiewicz KL, Marugán JJ, Raboisson P, Cummings MD, Grasberger BL, Johnson DL, Lu T, Molloy CJ, Maroney AC. 2006. Benzodiazepinedione inhibitors of the Hdm2:p53 complex suppress human tumor cell proliferation in vitro and sensitize tumors to doxorubicin in vivo. Mol Cancer Ther 5: 160-169.
21. Krubasik D, Iyer NG, English WR, Ahmed AA, Vias M, Roskelley C, Brenton JD, Caldas C, Murphy G. 2006. Absence of p300 induces cellular phenotypic changes characteristic of epithelial to mesenchyme transition. Br J Cancer 94: 1326-1332.
22. Lee ST, Chu K, Park JE, Hong NH, Im WS, Kang L, Han Z, Jung KH, Kim MW, Kim M. 2008. Atorvastatin attenuates mitochondrial toxin-induced striatal degeneration, with decreasing iNOS/c-Jun levels and activating ERK/Akt pathways. J Neurochem 104: 1190-1200.
23. Linos E, Swetter SM, Cockburn MG, Colditz GA, Clarke CA. 2009. Increasing burden of melanoma in the United States. J Invest Dermatol 129: 1666-1674.
24. Maksimovic-Ivanic D, Mijatovic S, Harhaji L, Miljkovic D, Dabideen D, Fan Cheng K, Mangano K, Malaponte G, Al-Abed Y, Libra M, Garotta G, Nicoletti F, Stosic-Grujicic S. 2008. Anticancer properties of the novel nitric oxide-donating compound (S, R)-3-phenyl-4, 5-dihydro-5-isoxazole acetic acid-nitric oxide in vitro and in vivo. Mol Cancer Ther 7: 510-520.
25. Maksimovic-Ivanic D, Mijatovic S, Miljkovic D, Harhaji-Trajkovic L, Timotijevic G, Mojic M, Dabideen D, Cheng KF, Mccubrey JA, Mangano K, Al-Abed Y, Libra M, Garotta G, Stosic-Grujicic S, Nicoletti F. 2009. The antitumor properties of a nontoxic, nitric oxide-modified version of saquinavir are independent of Akt. Mol Cancer Ther 8: 1169-1178.
26. Melnikova VO, Bolshakov SV, Walker C, Ananthaswamy HN. 2004. Genomic alterations in spontaneous and carcinogen-induced murine melanoma cell lines. Oncogene 23: 2347-2356.
27. Mijatovic S, Maksimovic-Ivanic D, Radovic J, Miljkovic DJ, Harhaji LJ, Vuckovic O, Stosic-Grujicic S, Mostarica Stojkovic M, Trajkovic V. 2005. Anti-glioma action of aloe emodin: The role of ERK inhibition. Cell Mol Life Sci 62: 589-598.
28. Mijatovic S, Maksimovic-Ivanic D, Mojic M, Malaponte G, Libra M, Cardile V, Miljkovic D, Harhaji L, Dabideen D, Cheng KF, Bevelacqua Y, Donia M, Garotta G, Al-Abed Y, Stosic-Grujicic S, Nicoletti F. 2008. Novel nitric oxide-donating compound (S, R)-3-phenyl-4, 5-dihydro-5-isoxazole acetic acid-nitric oxide (GIT-27NO) induces p53 mediated apoptosis in human A375 melanoma cells. Nitric Oxide 19: 177-183.
29. Mouly SJ, Paine MF, Watkins PB. 2004. Contributions of CYP3A4, P-glycoprotein, and serum protein binding to the intestinal first-pass extraction of saquinavir. J Pharmacol Exp Ther 308: 941-948.
30. Oh JH, Lee TJ, Park JW, Kwon TK. 2008. Withaferin A inhibits iNOS expression and nitric oxide production by Akt inactivation and down-regulating LPS-induced activity of NF-kappaB in RAW 264.7 cells. Eur J Pharmacol 599: 11-17.
31. Pajonk F, Van Ophoven A, Weissenberger C, Mcbride WH. 2005. The proteasome inhibitor MG-132 sensitizes PC-3 prostate cancer cells to ionizing radiation by a DNA-PK-independent mechanism. BMC Cancer 5: 76-88.
32. Powderly WG. 2002. Long-term exposure to lifelong therapies. J Acquir Immune Defic Syndr 1: 28-40.
33. Rigas B, Kashfi K. 2004. Nitric-oxide-donating NSAIDs as agents for cancer prevention. Trends Mol Med 10: 324-330.
34. Sajan MP, Standaert ML, Bandyopadhyay G, Quon MJ, Burke TR, Jr., Farese RV. 1999. Protein kinase C-ζ and phosphoinositide-dependent protein kinase-1 are required for insulin-induced activation of ERK in rat adipocytes. J Biol Chem 274: 30495-30500.
35. Salvucci O, Carsana M, Bersani I, Tragni G, Anichini A. 2001. Antiapoptotic role of endogenous nitric oxide in human melanoma cells. Cancer Res 61: 318-326.
36. Schütt M, Zhou J, Meier M, Klein HH. 2004. Long-term effects of HIV-1 protease inhibitors on insulin secretion and insulin signaling in INS-1 beta cells. J Endocrinol 183: 445-454.
37. Sgadari C, Monini P, Barillari G, Ensoli B. 2003. Use of HIV protease inhibitors to block Kaposi's sarcoma and tumour growth. Lancet Oncol 4: 537-547.
38. Takenaka Y, Fukumori T, Raz A. 2004. Galectin-3 and metastasis. Glycoconj J 19: 543-549.
39. Tang CH, Grimm EA. 2004. Depletion of endogenous nitric oxide enhances cisplatin-induced apoptosis in a p53-dependent manner in melanoma cell lines. J Biol Chem 279: 288-298.
40. Thomas WD, Hersey P. 1998. TNF-related apoptosis-inducing ligand (TRAIL) induces apoptosis in Fas ligand-resistant melanoma cells and mediates CD4 T cell killing of target cells. J Immunol 161: 2195-2200.
41. Thorburn A, Behbakht K, Ford H. 2008. TRAIL receptor-targeted therapeutics: Resistance mechanisms and strategies to avoid them. Drug Resist Update 11: 17-24.
42. Unni E, Koul D, Yung WK, Sinha R. 2005. Se-methylselenocysteine inhibits phosphatidylinositol 3-kinase activity of mouse mammary epithelial tumor cells in vitro. Breast Cancer Res 7: R699-707.
43. von Kriegsheim A, Baiocchi D, Birtwistle M, Sumpton D, Bienvenut W, Morrice N, Yamada K, Lamond A, Kalna G, Orton R, Gilbert D, Kolch W. 2009. Cell fate decisions are specified by the dynamic ERK interactome. Nat Cell Biol 11: 1458-1464.
44. White N, Knight GE, Butler PE, Burnstock G. 2009. An in vivo model of melanoma: Treatment with ATP. Purinergic Signal 5: 327-333.
45. Wu GS. 2009. TRAIL as a target in anti-cancer therapy. Cancer Lett 285: 1-5.
46. Yang J, Wu LJ, Tashiro S, Onodera S, Ikejima T. 2008. Nitric oxide activated by p38 and NF-kappaB facilitates apoptosis and cell cycle arrest under oxidative stress in evodiamine-treated human melanoma A375-S2 cells. Free Radic Res 42: 1-11.
47. Yart A, Laffargue M, Mayeux P, Chretien S, Peres C, Tonks N, Roche S, Payrastre B, Chap H, Raynal P. 2001. A critical role for phosphoinositide 3-kinase upstream of Gab1 and SHP2 in the activation of ras and mitogen-activated protein kinases by epidermal growth factor. J Biol Chem 276: 8856-8864.
48. Yoshida T, Shiraishi T, Nakata S, Horinaka M, Wakada M, Mizutani Y, Miki T, Sakai T. 2005. Proteasome inhibitor MG132 induces death receptor 5 through CCAAT/enhancer-binding protein homologous protein. Cancer Res 65: 5662-5667.
49. Zhao Y, Man K, Lo CM, Ng KT, Li XL, Sun CK, Lee TK, Dai XW, Fan ST. 2004. Attenuation of small-for-size liver graft injury by FTY720: Significance of cell-survival Akt signaling pathway. Am J Transplant 4: 1399-1407.