Regulation of nadph-dependent nitric oxide and reactive oxygen species signalling in endothelial and melanoma cells by a photoactive nadph analogue

Oncotarget

Volumn 5, Issue 21, 2014, Pages 10650-10664

  Rouaud, Florian ^a   Romero Perez, Miguel ^b   Wang, Huan ^c   Lobysheva, Irina ^b   Ramassamy, Booma ^d   Henry, Etienne ^c   Tauc, Patrick ^c   Giacchero, Damien ^e   Boucher, Jean Luc ^d   Deprez, Eric ^c   Rocchi, Stéphane ^a   Slama Schwok, Anny ^f  

^a CENTRE MÉDITERRANÉEN DE MÉDECINE MOLÉCULAIRE C3M   (France)

^b UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^c Ecole Normale Superieure de Cachan   (France)

^d UNIVERSITÉ PARIS DESCARTES   (France)

^e CENTRE HOSPITALIER UNIVERSITAIRE DE NICE   (France)

^f INRA Institut National de la Recherche Agronomique   (France)

Author keywords

Angiogenesis; Cell proliferation; Cellular signaling; Endothelium; Melanoma; NADPH analogue; Ros

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; HYDROGEN PEROXIDE; MITOGEN ACTIVATED PROTEIN KINASE; NANOSHUTTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE INHIBITOR; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; UNCLASSIFIED DRUG; VASCULOTROPIN; ENZYME INHIBITOR; NEURONAL NITRIC OXIDE SYNTHASE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; NOS3 PROTEIN, HUMAN; NOX4 PROTEIN, HUMAN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; VASCULOTROPIN A; VEGFA PROTEIN, HUMAN;

A375 CELL LINE; ANIMAL CELL; ANTIANGIOGENIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CANCER INHIBITION; CONTROLLED STUDY; ENDOTHELIUM CELL; G2 PHASE CELL CYCLE CHECKPOINT; HUMAN; HUMAN CELL; MELANOMA CELL; MOUSE; NONHUMAN; REDOX STRESS; UMBILICAL VEIN ENDOTHELIAL CELL; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; AORTA; APOPTOSIS; C57BL MOUSE; CELL CYCLE; CELL PROLIFERATION; CYTOLOGY; DRUG EFFECTS; ELECTRON SPIN RESONANCE; FLOW CYTOMETRY; LIGHT; MALE; MELANOMA; METABOLISM; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL CULTURE; WESTERN BLOTTING;

ANIMALS; AORTA; APOPTOSIS; BLOTTING, WESTERN; CELL CYCLE; CELL PROLIFERATION; ELECTRON SPIN RESONANCE SPECTROSCOPY; ENZYME INHIBITORS; FLOW CYTOMETRY; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; LIGHT; MALE; MELANOMA; MICE; MICE, INBRED C57BL; NADP; NADPH OXIDASE; NEOVASCULARIZATION, PATHOLOGIC; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE I; NITRIC OXIDE SYNTHASE TYPE III; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84916900281     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2525     Document Type: Article

References (62)

1. Atochin DN and Huang PL. Endothelial nitric oxide synthase transgenic models of endothelial dysfunction. Pflugers Arch. 2010; 460(6):965-974.
2. Frey RS, Ushio-Fukai M and Malik AB. NADPH oxidase-dependent signaling in endothelial cells: role in physiology and pathophysiology. Antioxid Redox Signal. 2009; 11(4):791-810.
3. Kao CL, Chen LK, Chang YL, Yung MC, Hsu CC, Chen YC, Lo WL, Chen SJ, Ku HH and Hwang SJ. Resveratrol protects human endothelium from H(2)O(2)-induced oxidative stress and senescence via SirT1 activation. J Atheroscler Thromb. 2010; 17(9):970-979.
4. Ischiropoulos HB, JS. Oxidative stress and nitration in neurodegeneration: cause, effect, or association? J Clin Invest. 2003; 111(2):163-169.
5. Moncada S, Palmer, R.M., Higgs, E.A. Nitric oxide: physiology, pathophysiology and pharmacology. Pharmacol Rev. 1991; 43(2):109-142.
6. Li H and Forstermann U. Prevention of atherosclerosis by interference with the vascular nitric oxide system. Curr Pharm Des. 2009; 15(27):3133-3145.
7. Kostourou V, Cartwright JE, Johnstone AP, Boult JK, Cullis ER, Whitley G and Robinson SP. The role of tumour-derived iNOS in tumour progression and angiogenesis. Br J Cancer. 2011; 104(1):83-90.
8. Patenaude A, Fuller M, Chang L, Wong F, Paliouras G, Shaw R, Kyle AH, Umlandt P, Baker JH, Diaz E, Tong J, Minchinton AI and Karsan A. Endothelial-specific Notch blockade inhibits vascular function and tumor growth through an eNOS-dependent mechanism. Cancer Res. 2014; 74(9):2402-2411.
9. Wind S, Beuerlein K, Eucker T, Muller H, Scheurer P, Armitage ME, Ho H, Schmidt HH and Wingler K. Comparative pharmacology of chemically distinct NADPH oxidase inhibitors. Br J Pharmacol. 2010; 161(4):885-898.
10. Poulos TL and Li H. Structural basis for isoform-selective inhibition in nitric oxide synthase. Acc Chem Res. 2013; 46(2):390-398.
11. Li Y, Wang H, Tarus B, Perez MR, Morellato L, Henry E, Berka V, Tsai AL, Ramassamy B, Dhimane H, Dessy C, Tauc P, Boucher JL, Deprez E and Slama-Schwok A. Rational design of a fluorescent NADPH derivative imaging constitutive nitric-oxide synthases upon two-photon excitation. Proc Natl Acad Sci U S A. 2012; 109(31):12526-12531.
12. Beaumont E, Lambry JC, Blanchard-Desce M, Martasek P, Panda SP, van Faassen EE, Brochon JC, Deprez E and Slama-Schwok A. NO formation by neuronal NO-synthase can be controlled by ultrafast electron injection from a nanotrigger. Chembiochem. 2009; 10(4):690-701.
13. Beaumont E, Lambry JC, Gautier C, Robin AC, Gmouh S, Berka V, Tsai AL, Blanchard-Desce M and Slama-Schwok A. Synchronous photoinitiation of endothelial NO synthase activity by a nanotrigger targeted at its NADPH site. J Am Chem Soc. 2007; 129(7):2178-2186.
14. Beaumont E, Lambry JC, Robin AC, Martasek P, Blanchard-Desce M and Slama-Schwok A. Two photon-induced electron injection from a nanotrigger in native endothelial NO-synthase. Chemphyschem. 2008; 9(16):2325-2331.
15. Lambry JC, Beaumont E, Tarus B, Blanchard-Desce M and Slama-Schwok A. Selective probing of a NADPH site controlled light-induced enzymatic catalysis. J Mol Recognit. 2010; 23(4):379-388.
16. Vanin AF. Iron diethyldithiocarbamate as spin trap for nitric oxide detection. Methods Enzymol. 1999; 301:269-279.
17. Pfeiffer S, Leopold E, Schmidt K, Brunner F and Mayer B. Inhibition of nitric oxide synthesis by NG-nitro-L-arginine methyl ester (L-NAME): requirement for bioactivation to the free acid, NG-nitro-L-arginine. Br J Pharmacol. 1996; 118(6):1433-1440.
18. Tuynman A, Perollier C, Frapart Y, Schumann-Bard P, Collot V, Rault S and Boucher JL. Inhibitory effects and spectral interactions of isomeric methoxyindazoles on recombinant nitric oxide synthases. Nitric Oxide. 2003; 9(2):86-94.
19. Brouet A, Sonveaux P, Dessy C, Moniotte S, Balligand JL and Feron O. Hsp90 and caveolin are key targets for the proangiogenic nitric oxide-mediated effects of statins. Circ Res. 2001; 89(10):866-873.
20. Dessy C, Saliez J, Ghisdal P, Daneau G, Lobysheva, II, Frerart F, Belge C, Jnaoui K, Noirhomme P, Feron O and Balligand JL. Endothelial beta3-adrenoreceptors mediate nitric oxide-dependent vasorelaxation of coronary microvessels in response to the third-generation beta-blocker nebivolol. Circulation. 2005; 112(8):1198-1205.
21. Stuehr DJ, Wei CC, Santolini J, Wang Z, Aoyagi M and GetzoffED. Radical reactions of nitric oxide synthases. Biochem Soc Symp. 2004; (71):39-49.
22. Liu-Smith F, Dellinger, R.,and Meyskens, F.L., Jr. Updates of reactive oxygen species in melanoma etiology and progression. Arch Biochem Biophys. 2014; in press.
23. Drummond GR, Selemidis S, Griendling KK and Sobey CG. Combating oxidative stress in vascular disease: NADPH oxidases as therapeutic targets. Nat Rev Drug Discov. 2011; 10(6):453-471.
24. Craige SM, Chen, K., Pei, Y., Huang, X., Chen, C., Shibata, R., Sato, K., Walsh, K., Keaney, J.F., Jr. NADPH oxidase 4 promotes endothelial angiogenesis though endothelial nitric oxide synthase activation. Circulation. 2011; 124:731-740.
25. Godoy LC, Anderson CT, Chowdhury R, Trudel LJ and Wogan GN. Endogenously produced nitric oxide mitigates sensitivity of melanoma cells to cisplatin. Proc Natl Acad Sci U S A. 2012; 109(50):20373-20378.
26. Melo FH, Molognoni F, Morais AS, Toricelli M, Mouro MG, Higa EM, Lopes JD and Jasiulionis MG. Endothelial nitric oxide synthase uncoupling as a key mediator of melanocyte malignant transformation associated with sustained stress conditions. Free Radic Biol Med. 2011; 50(10):1263-1273.
27. Yamaura M, Mitsushita J, Furuta S, Kiniwa Y, Ashida A, Goto Y, Shang WH, Kubodera M, Kato M, Takata M, Saida T and Kamata T. NADPH oxidase 4 contributes to transformation phenotype of melanoma cells by regulating G2-M cell cycle progression. Cancer Res. 2009; 69(6):2647-2654.
28. Burch PM and Heintz NH. Redox regulation of cell-cycle re-entry: cyclin D1 as a primary target for the mitogenic effects of reactive oxygen and nitrogen species. Antioxid Redox Signal. 2005; 7(5-6):741-751.
29. Napoli C, Paolisso G, Casamassimi A, Al-Omran M, Barbieri M, Sommese L, Infante T and Ignarro LJ. Effects of nitric oxide on cell proliferation: novel insights. J Am Coll Cardiol. 2013; 62(2):89-95.
30. Garcin ED, Bruns CM, Lloyd SJ, Hosfield DJ, Tiso M, Gachhui R, Stuehr DJ, Tainer JA and GetzoffED. Structural basis for isozyme-specific regulation of electron transfer in nitric-oxide synthase. J Biol Chem. 2004; 279(36):37918-37927.
31. Sonveaux P, Martinive P, DeWever J, Batova Z, Daneau G, Pelat M, Ghisdal P, Gregoire V, Dessy C, Balligand JL and Feron O. Caveolin-1 expression is critical for vascular endothelial growth factor-induced ischemic hindlimb collateralization and nitric oxide-mediated angiogenesis. Circ Res. 2004; 95(2):154-161.
32. Lim KH, Ancrile BB, Kashatus DF and Counter CM. Tumour maintenance is mediated by eNOS. Nature. 2008; 452(7187):646-649.
33. Meierjohann S. Oxidative stress in melanocyte senescence and melanoma transformation. Eur J Cell Biol. 2013.
34. Govindarajan B, Sligh JE, Vincent BJ, Li M, Canter JA, NickoloffBJ, Rodenburg RJ, Smeitink JA, Oberley L, Zhang Y, Slingerland J, Arnold RS, Lambeth JD, Cohen C, Hilenski L, Griendling K, et al. Overexpression of Akt converts radial growth melanoma to vertical growth melanoma. J Clin Invest. 2007; 117(3):719-729.
35. Liu F, Gomez Garcia AM and Meyskens FL, Jr. NADPH oxidase 1 overexpression enhances invasion via matrix metalloproteinase-2 and epithelial-mesenchymal transition in melanoma cells. J Invest Dermatol. 2012; 132(8):2033-2041.
36. Florio T, Morini M, Villa V, Arena S, Corsaro A, Thellung S, Culler MD, Pfeffer U, Noonan DM, Schettini G and Albini A. Somatostatin inhibits tumor angiogenesis and growth via somatostatin receptor-3-mediated regulation of endothelial nitric oxide synthase and mitogen-activated protein kinase activities. Endocrinology. 2003; 144(4):1574-1584.
37. Ying L and Hofseth LJ. An emerging role for endothelial nitric oxide synthase in chronic inflammation and cancer. Cancer Res. 2007; 67(4):1407-1410.
38. Lahdenranta J, Hagendoorn J, Padera TP, Hoshida T, Nelson G, Kashiwagi S, Jain RK and Fukumura D. Endothelial nitric oxide synthase mediates lymphangiogenesis and lymphatic metastasis. Cancer Res. 2009; 69(7):2801-2808.
39. Feng J, Damrauer SM, Lee M, Sellke FW, Ferran C and Abid MR. Endothelium-dependent coronary vasodilatation requires NADPH oxidase-derived reactive oxygen species. Arterioscler Thromb Vasc Biol. 2010; 30(9):1703-1710.
40. Mochizuki T, Furuta S, Mitsushita J, Shang WH, Ito M, Yokoo Y, Yamaura M, Ishizone S, Nakayama J, Konagai A, Hirose K, Kiyosawa K and Kamata T. Inhibition of NADPH oxidase 4 activates apoptosis via the AKT/apoptosis signal-regulating kinase 1 pathway in pancreatic cancer PANC-1 cells. Oncogene. 2006; 25(26):3699-3707.
41. Salmeen A, Park BO and Meyer T. The NADPH oxidases NOX4 and DUOX2 regulate cell cycle entry via a p53-dependent pathway. Oncogene. 2010; 29(31):4473-4484.
42. Luo L, Kaur Kumar J and Clement MV. Redox control of cytosolic Akt phosphorylation in PTEN null cells. Free Radic Biol Med. 2012; 53(9):1697-1707.
43. Zhang C, Lan, T. Hou, J., Li, J., Fang, R., Yang, Z., Zhang, J., Liu, B. NOX4 promotes non-small cell lung cancer cell proliferation and metastasis through positive feedback regulation of PI3K/Akt signalling. Oncotarget. 2014; 5(12):4392-4405.
44. Fenouille N, Puissant A, Tichet M, Zimniak G, Abbe P, Mallavialle A, Rocchi S, Ortonne JP, Deckert M, Ballotti R and Tartare-Deckert S. SPARC functions as an anti-stress factor by inactivating p53 through Akt-mediated MDM2 phosphorylation to promote melanoma cell survival. Oncogene. 2011; 30(49):4887-4900.
45. Liu P, Begley M, Michowski W, Inuzuka H, Ginzberg M, Gao D, Tsou P, Gan W, Papa A, Kim BM, Wan L, Singh A, Zhai B, Yuan M, Wang Z, Gygi SP, et al. Cell-cycle-regulated activation of Akt kinase by phosphorylation at its carboxyl terminus. Nature. 2014; 508(7497):541-545.
46. Mounir Z, Krishnamoorthy JL, Wang S, Papadopoulou B, Campbell S, Muller WJ, Hatzoglou M and Koromilas AE. Akt determines cell fate through inhibition of the PERK-eIF2alpha phosphorylation pathway. Sci Signal. 2011; 4(192):ra62.
47. Piccoli C, D'Aprile A, Ripoli M, Scrima R, Lecce L, Boffoli D, Tabilio A and Capitanio N. Bone-marrow derived hematopoietic stem/progenitor cells express multiple isoforms of NADPH oxidase and produce constitutively reactive oxygen species. Biochem Biophys Res Commun. 2007; 353(4):965-972.
48. Csanyi G, Taylor WR and Pagano PJ. NOX and inflammation in the vascular adventitia. Free Radic Biol Med. 2009; 47(9):1254-1266.
49. Garrido-Urbani S, Jemelin S, Deffert C, Carnesecchi S, Basset O, Szyndralewiez C, Heitz F, Page P, Montet X, Michalik L, Arbiser J, Ruegg C, Krause KH and Imhof BA. Targeting vascular NADPH oxidase 1 blocks tumor angiogenesis through a PPARalpha mediated mechanism. PLoS One. 2011; 6(2):e14665.
50. Altenhofer S, Kleikers PW, Radermacher KA, Scheurer P, Rob Hermans JJ, Schiffers P, Ho H, Wingler K and Schmidt HH. The NOX toolbox: validating the role of NADPH oxidases in physiology and disease. Cell Mol Life Sci. 2012; 69(14):2327-2343.
51. Silverman RB. Design of selective neuronal nitric oxide synthase inhibitors for the prevention and treatment of neurodegenerative diseases. Acc Chem Res. 2009; 42(3):439-451.
52. Huang H, Li H, Yang S, ChreifiG, Martasek P, Roman LJ, Meyskens FL, Poulos TL and Silverman RB. Potent and selective double-headed thiophene-2-carboximidamide inhibitors of neuronal nitric oxide synthase for the treatment of melanoma. J Med Chem. 2014; 57(3):686-700.
53. Jain RK. Normalizing Tumor Microenvironment to Treat Cancer: Bench to Bedside to Biomarkers. J Clin Oncol. 2013; 31(17):2205-18
54. Tomic T, Botton T, Cerezo M, Robert G, Luciano F, Puissant A, Gounon P, Allegra M, Bertolotto C, Bereder JM, Tartare-Deckert S, Bahadoran P, Auberger P, Ballotti R and Rocchi S. Metformin inhibits melanoma development through autophagy and apoptosis mechanisms. Cell Death Dis. 2011; 2:e199.
55. Slama-Schwok A, Boucher JL, Xu-Li Y and Deprez E. (2014). New family of analogues and nadp+ or nadph, their preparation and their application in therapeutics. US Patent US20140193339 A1 and PCT/EP2012/061744).
56. Moali C, Boucher JL, Sari MA, Stuehr DJ and Mansuy D. Substrate specificity of NO synthases: detailed comparison of L-arginine, homo-L-arginine, their N omega-hydroxy derivatives, and N omega-hydroxynor-L-arginine. Biochemistry. 1998; 37(29):10453-10460.
57. Heinzel B, John M, Klatt P, Bohme E and Mayer B. Ca2+/calmodulin-dependent formation of hydrogen peroxide by brain nitric oxide synthase. Biochem J. 1992; 281 (Pt 3):627-630.
58. Nelson DP and Kiesow LA. Enthalpy of decomposition of hydrogen peroxide by catalase at 25 degrees C (with molar extinction coefficients of H2O2 solutions in the UV). Anal Biochem. 1972; 49(2):474-478.
59. Botton T, Puissant A, Bahadoran P, Annicotte JS, Fajas L, Ortonne JP, Gozzerino G, Zamoum T, Tartare-Deckert S, Bertolotto C, Ballotti R and Rocchi S. In vitro and in vivo anti-melanoma effects of ciglitazone. J Invest Dermatol. 2009; 129(5):1208-1218.
60. Botton T, Puissant A, Cheli Y, Tomic T, Giuliano S, Fajas L, Deckert M, Ortonne JP, Bertolotto C, Tartare-Deckert S, Ballotti R and Rocchi S. Ciglitazone negatively regulates CXCL1 signaling through MITF to suppress melanoma growth. Cell Death Differ. 2011; 18(1):109-121.
61. Lobysheva I, Rath G, Sekkali B, Bouzin C, Feron O, Gallez B, Dessy C and Balligand JL. Moderate caveolin-1 downregulation prevents NADPH oxidase-dependent endothelial nitric oxide synthase uncoupling by angiotensin II in endothelial cells. Arterioscler Thromb Vasc Biol. 2011; 31(9):2098-2105.
62. Dikalov S, Griendling KK and Harrison DG. Measurement of reactive oxygen species in cardiovascular studies. Hypertension. 2007; 49(4):717-727.