Nitroaspirin (NCX-4016), an NO donor, is antiangiogenic through induction of loss of redox-dependent viability and cytoskeletal reorganization in endothelial cells

Antioxidants and Redox Signaling

Volumn 9, Issue 11, 2007, Pages 1837-1849

  Parinandi, Narasimham L ^a   Sharma, Ashish ^a   Eubank, Timothy D ^a   Kaufman, Bruce F ^a   Kutala, Vijay Kumar ^a   Marsh, Clay B ^a   Ignarro, Louis J ^b   Kuppusamy, Periannan ^a,c  

^a THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCYSTEINE; ACETYLSALICYLIC ACID 3 (NITROXYMETHYL)PHENYL ESTER; THIOL;

ANALYTIC METHOD; ANIMAL CELL; ANTIANGIOGENIC ACTIVITY; ARTICLE; CELL LABELING; CELL VIABILITY; CONTROLLED STUDY; CYTOSKELETON; DOSE RESPONSE; ELECTRIC RESISTANCE; FLUORESCENCE MICROSCOPY; LUNG ENDOTHELIUM; NONHUMAN; OXIDATION REDUCTION REACTION; OXYGEN CONSUMPTION; PRIORITY JOURNAL;

ANIMALS; ANTIOXIDANTS; ASPIRIN; CAPILLARIES; CATTLE; CELL SURVIVAL; CELLS, CULTURED; CYTOSKELETON; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; HUMANS; HYDROGEN PEROXIDE; LUNG; MICROSCOPY, FLUORESCENCE; NEOVASCULARIZATION, PHYSIOLOGIC; NITRIC OXIDE DONORS; OXIDATION-REDUCTION; UMBILICAL VEINS;

BOVINAE;

EID: 35448939210     PISSN: 15230864     EISSN: None     Source Type: Journal    
DOI: 10.1089/ars.2007.1603     Document Type: Article

References (60)

1. Bolla M, Momi S, Gresele P, and Del Soldato P. Nitric oxide-donating aspirin (NCX 4016): an overview of its pharmacological properties and clinical perspectives. Eur J Clin Pharmacol 62(suppl 13): 145-154, 2006.
2. Boyd CS and Cadenas E. Nitric oxide and cell signaling pathways in mitochondrial-dependent apoptosis. Biol Chem 383: 411-423, 2002.
3. Bratasz A, Weir NM, Parinandi NL, Zweier JL, Sridhar R, Ignarro LJ, and Kuppusamy P. Reversal to cisplatin sensitivity in recurrent human ovarian cancer cells by NCX-4016, a nitro derivative of aspirin. Proc Natl Acad Sci U S A 103: 3914-3919, 2006.
4. Brune B, von Knethen A, and Sandau KB. Nitric oxide (NO): an effector of apoptosis. Cell Death Differ 6: 969-975, 1999.
5. Carini M, Aldini G, Orioli M, and Maffei Facino R. In vitro metabolism of a nitroderivative of acetylsalicylic acid (NCX4016) by rat liver: LC and LC-MS studies. J Pharm Biomed Anal 29: 1061-1071, 2002.
6. Chung HY, Yokozawa T, Kim MS, Lee KH, Kim KW, Yang R, and Choi JH. The mechanism of nitric oxide and/or superoxide cytotoxicity in endothelial cells. Exp Toxicol Pathol 52: 227-233, 2000.
7. Cifone MG, Cironi L, Meccia MA, Roncaioli P, Festuccia C, De Nuntiis G, D'Alo S, and Santoni A. Role of nitric oxide in cell-mediated tumor cytotoxicity. Adv Neuroimmunol 5: 443-461, 1995.
8. Corazzi T, Leone M, Roberti R, Del Soldato P, and Gresele P. Effect of nitric oxide-donating agents on human monocyte cyclooxygenase-2. Biochem Biophys Res Commun 311: 897-903, 2003.
9. Dalgleish AG and O'Byrne K. Inflammation and cancer: the role of the immune response and angiogenesis. Cancer Treat Res 130: 1-38, 2006.
10. De Santo C, Serafini P, Marigo I, Dolcetti L, Bolla M, Del Soldato P, Melani C, Guiducci C, Colombo MP, Iezzi M, Musiani P, Zanovello P, and Bronte V. Nitroaspirin corrects immune dysfunction in tumor-bearing hosts and promotes tumor eradication by cancer vaccination. Proc Natl Acad Sci U S A 102: 4185-4190, 2005.
11. Degnim AC, Morrow SE, Ku J, Zar HA, and Nakayama DK. Nitric oxide inhibits peroxide-mediated endothelial toxicity. J Surg Res 75: 127-134, 1998.
12. Emanueli C, Van Linthout S, Salis MB, Monopoli A, Del Soldato P, Ongini E, and Madeddu P. Nitric oxide-releasing aspirin derivative, NCX 4016, promotes reparative angiogenesis and prevents apoptosis and oxidative stress in a mouse model of peripheral ischemia. Arterioscler Thromb Vasc Biol 24: 2082-2087, 2004.
13. Eubank TD, Galloway M, Montague CM, Waldman WJ, and Marsh CB. M-CSF induces vascular endothelial growth factor production and angiogenic activity from human monocytes. J Immunol 171: 2637-2643, 2003.
14. Eubank TD, Roberts R, Galloway M, Wang Y, Cohn DE, and Marsh CB. GM-CSF induces expression of soluble VEGF receptor-1 from human monocytes and inhibits angiogenesis in mice. Immunity 21: 831-842, 2004.
15. Fenteany G and Zhu S. Small-molecule inhibitors of actin dynamics and cell motility. Curr Top Med Chem 3: 593-616, 2003.
16. Fiorucci S, Mencarelli A, Meneguzzi A, Lechi A, Morelli A, del Soldato P, and Minuz P. NCX-4016 (NO-aspirin) inhibits lipopolysaccharide-induced tissue factor expression in vivo: role of nitric oxide. Circulation 106: 3120-3125, 2002.
17. Gately S and Kerbel R. Therapeutic potential of selective cyclooxygenase-2 inhibitors in the management of tumor angiogenesis. Prog Exp Tumor Res 37: 179-192, 2003.
18. Grosser N and Schroder H. A common pathway for nitric oxide release from NO-aspirin and glyceryl trinitrate. Biochem Biophys Res Commun 274: 255-258, 2000.
19. Hashida K, Sasaki K, and Makino N. Interactions of nitric oxide and oxygen in cytotoxicity: proliferation and antioxidant enzyme activities of endothelial cells in culture. Free Radic Res 33: 147-156, 2000.
20. Ignarro LJ, Buga GM, Wei LH, Bauer PM, Wu G, and del Soldato P. Role of the arginine-nitric oxide pathway in the regulation of vascular smooth muscle cell proliferation. Proc Natl Acad Sci U S A 98: 4202-4208, 2001.
21. Ignarro LJ, Buga GM, Wood KS, Byrns RE, and Chaudhuri G. Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc Natl Acad Sci U S A 84: 9265-9269, 1987.
22. Ignarro LJ, Napoli C, and Loscalzo J. Nitric oxide donors and cardiovascular agents modulating the bioactivity of nitric oxide: an overview. Circ Res 90: 21-28, 2002.
23. Ioannidis I, Batz M, Paul T, Korth HG, Sustmann R, and De Groot H. Enhanced release of nitric oxide causes increased cytotoxicity of S-nitroso-N-acetyl-DL-penicillamine and sodium nitroprusside under hypoxic conditions. Biochem J 318: 789-795, 1996.
24. Kanda S, Miyata Y, and Kanetake H. Current status and perspective of antiangiogenic therapy for cancer: urinary cancer. Int J Clin Oncol 11: 90-107, 2006.
25. Nepler JL Jr, Taher LN, Gupta MP, Patterson C, Pavalko F, Ober MD, and Hart CM. Peroxynitrite causes endothelial cell monolayer barrier dysfunction. Am J Physiol Cell Physiol 281: C1064-C1075, 2001.
26. Law A, Wu J, Zeng LH, and Wu TW. Aortic endothelial cells damaged by a nitric oxide donor and protected by flavonoids. Life Sci 64: PL199-PL204, 1999.
27. Levin RI. Theriac found? Nitric oxide-aspirin and the search for the universal cure. J Am Coll Cardiol 44: 642-643, 2004.
28. Liu L and Stamler JS. NO: an inhibitor of cell death. Cell Death Differ 6: 937-942, 1999.
29. Lu H, Ouyang W, and Huang C. Inflammation, a key event in cancer development. Mol Cancer Res 4: 221-233, 2006.
30. Muscara MN and Wallace JL. Nitric oxide; V: therapeutic potential of nitric oxide donors and inhibitors. Am J Physiol 276: G1313-G1316, 1999.
31. Nakayama GR, Caton MC, Nova MP, and Parandoosh Z. Assessment of the Alamar Blue assay for cellular growth and viability in vitro. J Immunol Methods 204: 205-208, 1997.
32. Napoli C, Aldini G, Wallace JL, de Nigris F, Maffei R, Abete P, Bonaduce D, Condorelli G, Rengo F, Sica V, D'Armiento FP, Mignogna C, de Rosa G, Condorelli M, Lerman LO, and Ignarro LJ. Efficacy and age-related effects of nitric oxide-releasing aspirin on experimental restenosis. Proc Natl Acad Sci U S A 99: 1689-1694, 2002.
33. Nieder C, Wiedenmann N, Andratschke N, and Molls M. Current status of angiogenesis inhibitors combined with radiation therapy. Cancer Treat Rev 2006.
34. O'Brien J, Wilson I, Orton T, and Pognan F. Investigation of the Alamar Blue (resazurin) fluorescent dye for the assessment of mammalian cell cytotoxicity. Eur J Biochem 267(17): 5421-5426, 2000.
35. O'Donnell VB and Freeman BA. Interactions between nitric oxide and lipid oxidation pathways: implications for vascular disease. Circ Res 88: 12-21, 2001.
36. Ongini E, Impagnatiello F, Bonazzi A, Guzzetta M, Govoni M, Monopoli A, Del Soldato P, and Ignarro LJ. Nitric oxide (NO)-releasing statin derivatives, a class of drugs showing enhanced antiproliferative and antiinflammatory properties. Proc Natl Acad Sci U S A 101: 8497-8502, 2004.
37. Pandian RP, Kutala VK, Liaugminas A, Parinandi NL, and Kuppusamy P. Lipopolysaccharide-induced alterations in oxygen consumption and radical generation in endothelial cells. Mol Cell Biochem 278: 119-127, 2005.
38. Patel RP, Levonen A, Crawford JH, and Darley-Usmar VM. Mechanisms of the pro- and anti-oxidant actions of nitric oxide in atherosclerosis. Cardiovasc Res 47: 465-474, 2000.
39. Patel RP, McAndrew J, Sellak H, White CR, Jo H, Freeman BA, and Darley-Usmar VM. Biological aspects of reactive nitrogen species. Biochim Biophys Acta 1411: 385-400, 1999.
40. Polte T, Oberle S, and Schroder H. Nitric oxide protects endothelial cells from tumor necrosis factor-alpha-mediated cytotoxicity: possible involvement of cyclic GMP. FEBS Lett 409: 46-48, 1997.
41. Quesada AR, Munoz-Chapuli R, and Medina MA. Anti-angiogenic drugs: from bench to clinical trials. Med Res Rev 26: 483-530, 2006.
42. Ramachandran A, Moellering DR, Ceaser E, Shiva S, Xu J, and Darley-Usmar V. Inhibition of mitochondrial protein synthesis results in increased endothelial cell susceptibility to nitric oxide-induced apoptosis. Proc Natl Acad Sci U S A 99: 6643-6648, 2002.
43. Rao CV, Reddy BS, Steele VE, Wang CX, Liu X, Ouyang N, Patlolla JM, Simi B, Kopelovich L, and Rigas B. Nitric oxide-releasing aspirin and indomethacin are potent inhibitors against colon cancer in azoxymethane-treated rats: effects on molecular targets. Mol Cancer Ther 5: 1530-1538, 2006.
44. Raz B, Iten M, Grether-Buhler Y, Kaminsky R, and Brun R. The Alamar Blue assay to determine drug sensitivity of African trypanosomes (T.b. rhodesiense and T.b. gambiense) in vitro. Acta Trop 68: 139-147, 1997.
45. Rubbo H, Tarpey M, and Freeman BA. Nitric oxide and reactive oxygen species in vascular injury. Biochem Soc Symp 61: 33-45, 1995.
46. Schnittler HJ. Structural and functional aspects of intercellular junctions in vascular endothelium. Basic Res Cardiol 93(suppl 3): 30-39, 1998.
47. Sheu WH, Ou HC, Chou FP, Lin TM, and Yang CH. Rosiglitazone inhibits endothelial proliferation and angiogenesis. Life Sci 78: 1520-1528, 2006.
48. Shi S, Garcia JG, Roy S, Parinandi NL, and Natarajan V. Involvement of c-Src in diperoxovanadate-induced endothelial cell barrier dysfunction. Am J Physiol Lung Cell Mol Physiol 279: L441-L451, 2000.
49. Stamler JS, Singel DJ, and Loscalzo J. Biochemistry of nitric oxide and its redox-activated forms. Science 258: 1898-1902, 1992.
50. Struck AT, Hogg N, Thomas JP, and Kalyanaraman B. Nitric oxide donor compounds inhibit the toxicity of oxidized low-density lipoprotein to endothelial cells. FEBS Lett 361: 291-294, 1995.
51. Tesei A, Ricotti L, Ulivi P, Medri L, Amadori D, and Zoli W. NCX 4016, a nitric oxide-releasing aspirin derivative, exhibits a significant antiproliferative effect and alters cell cycle progression in human colon adenocarcinoma cell lines. Int J Oncol 22: 1297-1302, 2003.
52. Usatyuk PV, Vepa S, Watkins T, He D, Parinandi NL, and Natarajan V. Redox regulation of reactive oxygen species-induced p38 MAP kinase activation and barrier dysfunction in lung microvascular endothelial cells. Antioxid Redox Signal 5: 723-730, 2003.
53. Varadharaj S, Watkins T, Cardounel AJ, Garcia JG, Zweier JL, Kuppusamy P, Natarajan V, and Parinandi NL. Vitamin C-induced loss of redox-dependent viability in lung microvascular endothelial cells. Antioxid Redox Signal 7: 287-300, 2005.
54. Vepa S, Scribner WM, Parinandi NL, English D, Garcia JG, and Natarajan V. Hydrogen peroxide stimulates tyrosine phosphorylation of focal adhesion kinase in vascular endothelial cells. Am J Physiol 277: L150-L158, 1999.
55. Wallace JL, Del Soldato P, Cirino G, and Muscara MN. Nitric oxide-releasing NSAIDs: GI-safe antithrombotics. IDrugs 2: 321-326, 1999.
56. Wallace JL, Ignarro LJ, and Fiorucci S. Potential cardioprotective actions of no-releasing aspirin. Nat Rev Drug Discov 1: 375-382, 2002.
57. Wink DA, Cook JA, Krishna MC, Hanbauer I, DeGraff W, Gamson J, and Mitchell JB. Nitric oxide protects against alkyl peroxide-mediated cytotoxicity: further insights into the role nitric oxide plays in oxidative stress. Arch Biochem Biophys 319: 402-407, 1995.
58. Wink DA, Cook JA, Pacelli R, DeGraff W, Gamson J, Liebmann J, Krishna MC, and Mitchell JB. The effect of various nitric oxide-donor agents on hydrogen peroxide-mediated toxicity: a direct correlation between nitric oxide formation and protection. Arch Biochem Biophys 331: 241-248, 1996.
59. Wink DA, Miranda KM, and Espey MG. Cytotoxicity related to oxidative and nitrosative stress by nitric oxide. Exp Biol Med (Maywood) 226: 621-623, 2001.
60. Yamamoto T and Bing RJ. Nitric oxide donors. Proc Soc Exp Biol Med 225: 200-206, 2000.