Nitric oxide and cell death in liver cancer cells

Mitochondrion

Volumn 13, Issue 3, 2013, Pages 257-262

  Muntané, Jordi ^a,b   De la Rosa, Angel J ^a   Marín, Luís M ^a   Padillo, Francisco J ^a,b  

^a Instituto de Biomedicina de Sevilla   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

Cancer; Hepatocytes; Liver; Nitric oxide; Nitrosative stress; Therapy

Indexed keywords

CALCIUM ION; CYCLIC GMP; DEATH RECEPTOR 4; DEATH RECEPTOR 5; FAS ANTIGEN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; ISOENZYME; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; PROTEIN P53; TUMOR NECROSIS FACTOR RECEPTOR 1; HYPOXIA INDUCIBLE FACTOR 1; NITRIC OXIDE SYNTHASE; TP53 PROTEIN, HUMAN;

CANCER CELL; CANCER GROWTH; CELL DEATH; CELL PROLIFERATION; DOWN REGULATION; ENZYME ACTIVITY; ENZYME LOCALIZATION; HUMAN; INTRACELLULAR SIGNALING; LIVER CANCER; MOLECULAR CLONING; MOLECULAR PATHOLOGY; NITROSYLATION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; REVIEW; SENSITIVITY ANALYSIS; TUMOR MICROENVIRONMENT; UPREGULATION; ANIMAL; APOPTOSIS; GENETICS; LIVER CELL CARCINOMA; LIVER TUMOR; METABOLISM; PATHOLOGY;

ANIMALS; APOPTOSIS; CARCINOMA, HEPATOCELLULAR; CYCLIC GMP; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1; LIVER NEOPLASMS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84883760816     PISSN: 15677249     EISSN: 18728278     Source Type: Journal    
DOI: 10.1016/j.mito.2012.09.004     Document Type: Review

References (107)

1. Aaltoma S.H., Lipponen P.K., Kosma V.M. Inducible nitric oxide synthase (iNOS) expression and its prognostic value in prostate cancer. Anticancer Res. 2001, 21:3101-3106.
2. Abate C., Patel L., Rauscher F.J., Curran T. Redox regulation of fos and jun DNA-binding activity in vitro. Science 1990, 249:1157-1161.
3. Abou-Elella A.M., Siendones E., Padillo J., Montero J.L., De la Mata M., Muntane Relat J. Tumour necrosis factor-alpha and nitric oxide mediate apoptosis by D-galactosamine in a primary culture of rat hepatocytes: exacerbation of cell death by cocultured Kupffer cells. Can. J. Gastroenterol. 2002, 16:791-799.
4. Akazawa Y., Gores G.J. Death receptor-mediated liver injury. Semin. Liver Dis. 2007, 27:327-338.
5. Alderton W.K., Cooper C.E., Knowles R.G. Nitric oxide synthases: structure, function and inhibition. Biochem. J. 2001, 357:593-615.
6. Ambs S., Merriam W.G., Bennett W.P., Felley-Bosco E., Ogunfusika M.O., Oser S.M., Klein S., Shields P.G., Billiar T.R., Harris C.C. Frequent nitric oxide synthase-2 expression in human colon adenomas: implication for tumor angiogenesis and colon cancer progression. Cancer Res. 1998, 58:334-341.
7. Ambs S., Merriam W.G., Ogunfusika M.O., Bennett W.P., Ishibe N., Hussain S.P., Tzeng E.E., Geller D.A., Billiar T.R., Harris C.C. p53 and vascular endothelial growth factor regulate tumor growth of NOS2-expressing human carcinoma cells. Nat. Med. 1998, 4:1371-1376.
8. Beckman J.S., Beckman T.W., Chen J., Marshall P.A., Freeman B.A. Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc. Natl. Acad. Sci. U. S. A. 1990, 87:1620-1624.
9. Bolanos J.P., Peuchen S., Heales S.J., Land J.M., Clark J.B. Nitric oxide-mediated inhibition of the mitochondrial respiratory chain in cultured astrocytes. J. Neurochem. 1994, 63:910-916.
10. Bolotina V.M., Najibi S., Palacino J.J., Pagano P.J., Cohen R.A. Nitric oxide directly activates calcium-dependent potassium channels in vascular smooth muscle. Nature 1994, 368:850-853.
11. Bonavida B., Baritaki S., Huerta-Yepez S., Vega M.I., Chatterjee D., Yeung K. Novel therapeutic applications of nitric oxide donors in cancer: roles in chemo- and immunosensitization to apoptosis and inhibition of metastases. Nitric Oxide 2008, 19:152-157.
12. Boo Y.C., Kim H.J., Song H., Fulton D., Sessa W., Jo H. Coordinated regulation of endothelial nitric oxide synthase activity by phosphorylation and subcellular localization. Free Radic. Biol. Med. 2006, 41:144-153.
13. Bredt D.S., Hwang P.M., Snyder S.H. Localization of nitric oxide synthase indicating a neural role for nitric oxide. Nature 1990, 347:768-770.
14. Bredt D.S., Hwang P.M., Glatt C.E., Lowenstein C., Reed R.R., Snyder S.H. Cloned and expressed nitric oxide synthase structurally resembles cytochrome P-450 reductase. Nature 1991, 351:714-718.
15. Brown G.C. Nitric oxide regulates mitochondrial respiration and cell functions by inhibiting cytochrome oxidase. FEBS Lett. 1995, 369:136-139.
16. Brown G.C., Cooper C.E. Nanomolar concentrations of nitric oxide reversibly inhibit synaptosomal respiration by competing with oxygen at cytochrome oxidase. FEBS Lett. 1994, 356:295-298.
17. Buechler W.A., Ivanova K., Wolfram G., Drummer C., Heim J.M., Gerzer R. Soluble guanylyl cyclase and platelet function. Ann. N. Y. Acad. Sci. 1994, 714:151-157.
18. Church J.E., Fulton D. Differences in eNOS activity because of subcellular localization are dictated by phosphorylation state rather than the local calcium environment. J. Biol. Chem. 2006, 281:1477-1488.
19. Cleeter M.W., Cooper J.M., Darley-Usmar V.M., Moncada S., Schapira A.H. Reversible inhibition of cytochrome c oxidase, the terminal enzyme of the mitochondrial respiratory chain, by nitric oxide. Implications for neurodegenerative diseases. FEBS Lett. 1994, 345:50-54.
20. Cobbs C.S., Brenman J.E., Aldape K.D., Bredt D.S., Israel M.A. Expression of nitric oxide synthase in human central nervous system tumors. Cancer Res. 1995, 55:727-730.
21. Cook J.A., Krishna M.C., Pacelli R., DeGraff W., Liebmann J., Mitchell J.B., Russo A., Wink D.A. Nitric oxide enhancement of melphalan-induced cytotoxicity. Br. J. Cancer 1997, 76:325-334.
22. Degerman E., Belfrage P., Manganiello V.C. Structure, localization, and regulation of cGMP-inhibited phosphodiesterase (PDE3). J. Biol. Chem. 1997, 272:6823-6826.
23. Egeblad M., Werb Z. New functions for the matrix metalloproteinases in cancer progression. Nat. Rev. Cancer 2002, 2:161-174.
24. Ema M., Hirota K., Mimura J., Abe H., Yodoi J., Sogawa K., Poellinger L., Fujii-Kuriyama Y. Molecular mechanisms of transcription activation by HLF and HIF1alpha in response to hypoxia: their stabilization and redox signal-induced interaction with CBP/p300. EMBO J. 1999, 18:1905-1914.
25. Feron O., Belhassen L., Kobzik L., Smith T.W., Kelly R.A., Michel T. Endothelial nitric oxide synthase targeting to caveolae. Specific interactions with caveolin isoforms in cardiac myocytes and endothelial cells. J. Biol. Chem. 1996, 271:22810-22814.
26. Friebe A., Koesling D. Regulation of nitric oxide-sensitive guanylyl cyclase. Circ. Res. 2003, 93:96-105.
27. Fukumura D., Kashiwagi S., Jain R.K. The role of nitric oxide in tumour progression. Nat. Rev. Cancer 2006, 6:521-534.
28. Furchgott R.F., Zawadzki J.V. The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature 1980, 288:373-376.
29. Gallo O., Masini E., Morbidelli L., Franchi A., Fini-Storchi I., Vergari W.A., Ziche M. Role of nitric oxide in angiogenesis and tumor progression in head and neck cancer. J. Natl. Cancer Inst. 1998, 90:587-596.
30. Giulivi C. Functional implications of nitric oxide produced by mitochondria in mitochondrial metabolism. Biochem. J. 1998, 332(Pt 3):673-679.
31. González R., Cruz A., Ferrin G., Lopez-Cillero P., Fernandez-Rodriguez R., Briceno J., Gomez M.A., Rufian S., Mata M.D., Martinez-Ruiz A., Marin J.J., Muntane J. Nitric oxide mimics transcriptional and post-translational regulation during alpha-Tocopherol cytoprotection against glycochenodeoxycholate-induced cell death in hepatocytes. J. Hepatol. 2011, 55:13-144.
32. González, R., Ferrín, G., Aguilar-Melero, P., Ranchal, I., Linares, C.I., Bello, R.I., De la Mata, M., Gogvadze, V., Bárcena, J.A., Alamo, J.M., Orrenius, S., Padillo, F.J., Zhivotovsky, B, Muntané J., accepted for publication. Targeting hepatoma using NO donor strategies. Antioxid. Redox Signal. ( PMID: 22861189).
33. Grasemann H., Drazen J.M., Deykin A., Israel E., De Sanctis G.T., Pillari A., Yandava C.H. Simple tandem repeat polymorphisms in the neuronal nitric oxide synthase gene in different ethnic populations. Hum. Hered. 1999, 49:139-141.
34. Gressner O., Schilling T., Lorenz K., Schulze Schleithoff E., Koch A., Schulze-Bergkamen H., Lena A.M., Candi E., Terrinoni A., Catani M.V., Oren M., Melino G., Krammer P.H., Stremmel W., Muller M. TAp63alpha induces apoptosis by activating signaling via death receptors and mitochondria. EMBO J. 2005, 24:2458-2471.
35. Gruetter C.A., Barry B.K., McNamara D.B., Gruetter D.Y., Kadowitz P.J., Ignarro L. Relaxation of bovine coronary artery and activation of coronary arterial guanylate cyclase by nitric oxide, nitroprusside and a carcinogenic nitrosoamine. J. Cyclic Nucleotide Res. 1979, 5:211-224.
36. Hanafy K.A., Krumenacker J.S., Murad F. NO, nitrotyrosine, and cyclic GMP in signal transduction. Med. Sci. Monit. 2001, 7:801-819.
37. Hibbs J.B., Taintor R.R., Vavrin Z. Macrophage cytotoxicity: role for l-arginine deiminase and imino nitrogen oxidation to nitrite. Science 1987, 235:473-476.
38. Houslay M.D., Milligan G. Tailoring cAMP-signalling responses through isoform multiplicity. Trends Biochem. Sci. 1997, 22:217-224.
39. Huerta-Yepez S., Vega M., Jazirehi A., Garban H., Hongo F., Cheng G., Bonavida B. Nitric oxide sensitizes prostate carcinoma cell lines to TRAIL-mediated apoptosis via inactivation of NF-kappa B and inhibition of Bcl-xl expression. Oncogene 2004, 23:4993-5003.
40. Ignarro L.J., Harbison R.G., Wood K.S., Kadowitz P.J. Activation of purified soluble guanylate cyclase by endothelium-derived relaxing factor from intrapulmonary artery and vein: stimulation by acetylcholine, bradykinin and arachidonic acid. J. Pharmacol. Exp. Ther. 1986, 237:893-900.
41. Ignarro L.J., Buga G.M., Wood K.S., Byrns R.E., Chaudhuri G. Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc. Natl. Acad. Sci. U. S. A. 1987, 84:9265-9269.
42. Ischiropoulos H. Biological selectivity and functional aspects of protein tyrosine nitration. Biochem. Biophys. Res. Commun. 2003, 305:776-783.
43. Iwakiri Y., Satoh A., Chatterjee S., Toomre D.K., Chalouni C.M., Fulton D., Groszmann R.J., Shah V.H., Sessa W.C. Nitric oxide synthase generates nitric oxide locally to regulate compartmentalized protein S-nitrosylation and protein trafficking. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:19777-19782.
44. Jaffrey S.R., Snyder S.H. Nitric oxide: a neural messenger. Annu. Rev. Cell Dev. Biol. 1995, 11:417-440.
45. Jaffrey S.R., Erdjument-Bromage H., Ferris C.D., Tempst P., Snyder S.H. Protein S-nitrosylation: a physiological signal for neuronal nitric oxide. Nat. Cell Biol. 2001, 3:193-197.
46. Jaiswal M., LaRusso N.F., Nishioka N., Nakabeppu Y., Gores G.J. Human Ogg1, a protein involved in the repair of 8-oxoguanine, is inhibited by nitric oxide. Cancer Res. 2001, 61:6388-6393.
47. Jazirehi A.R., Bonavida B. Cellular and molecular signal transduction pathways modulated by rituximab (rituxan, anti-CD20 mAb) in non-Hodgkin's lymphoma: implications in chemosensitization and therapeutic intervention. Oncogene 2005, 24:2121-2143.
48. Katsuki S., Arnold W.P., Murad F. Effects of sodium nitroprusside, nitroglycerin, and sodium azide on levels of cyclic nucleotides and mechanical activity of various tissues. J. Cyclic Nucleotide Res. 1977, 3:239-247.
49. Klatt P., Molina E.P., Lamas S. Nitric oxide inhibits c-Jun DNA binding by specifically targeted S-glutathionylation. J. Biol. Chem. 1999, 274:15857-15864.
50. Kojima M., Morisaki T., Tsukahara Y., Uchiyama A., Matsunari Y., Mibu R., Tanaka M. Nitric oxide synthase expression and nitric oxide production in human colon carcinoma tissue. J. Surg. Oncol. 1999, 70:222-229.
51. Kroncke K.D., Carlberg C. Inactivation of zinc finger transcription factors provides a mechanism for a gene regulatory role of nitric oxide. FASEB J. 2000, 14:166-173.
52. Kurose I., Miura S., Fukumura D., Yonei Y., Saito H., Tada S., Suematsu M., Tsuchiya M. Nitric oxide mediates Kupffer cell-induced reduction of mitochondrial energization in hepatoma cells: a comparison with oxidative burst. Cancer Res. 1993, 53:2676-2682.
53. Kuzkaya N., Weissmann N., Harrison D.G., Dikalov S. Interactions of peroxynitrite, tetrahydrobiopterin, ascorbic acid, and thiols: implications for uncoupling endothelial nitric-oxide synthase. J. Biol. Chem. 2003, 278:22546-22554.
54. Lala P.K., Chakraborty C. Role of nitric oxide in carcinogenesis and tumour progression. Lancet Oncol. 2001, 2:149-156.
55. Lancaster J.R. Simulation of the diffusion and reaction of endogenously produced nitric oxide. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:8137-8141.
56. Lancaster J.R. A tutorial on the diffusibility and reactivity of free nitric oxide. Nitric Oxide 1997, 1:18-30.
57. Lancaster J.R., Xie K. Tumors face NO problems?. Cancer Res. 2006, 66:6459-6462.
58. Lander H.M. An essential role for free radicals and derived species in signal transduction. FASEB J. 1997, 11:118-124.
59. Lander H.M., Sehajpal P.K., Novogrodsky A. Nitric oxide signaling: a possible role for G proteins. J. Immunol. 1993, 151:7182-7187.
60. Laval F., Wink D.A. Inhibition by nitric oxide of the repair protein, O6-methylguanine-DNA-methyltransferase. Carcinogenesis 1994, 15:443-447.
61. Leon-Bollotte L., Subramaniam S., Cauvard O., Plenchette-Colas S., Paul C., Godard C., Martinez-Ruiz A., Legembre P., Jeannin J.F., Bettaieb A. S-nitrosylation of the death receptor fas promotes fas ligand-mediated apoptosis in cancer cells. Gastroenterology 2011, 140:2009-2018.
62. Li J., Billiar T.R., Talanian R.V., Kim Y.M. Nitric oxide reversibly inhibits seven members of the caspase family via S-nitrosylation. Biochem. Biophys. Res. Commun. 1997, 240:419-424.
63. Lohmann S.M., Vaandrager A.B., Smolenski A., Walter U., De Jonge H.R. Distinct and specific functions of cGMP-dependent protein kinases. Trends Biochem. Sci. 1997, 22:307-312.
64. Lyons C.R., Orloff G.J., Cunningham J.M. Molecular cloning and functional expression of an inducible nitric oxide synthase from a murine macrophage cell line. J. Biol. Chem. 1992, 267:6370-6374.
65. Marrogi A.J., Travis W.D., Welsh J.A., Khan M.A., Rahim H., Tazelaar H., Pairolero P., Trastek V., Jett J., Caporaso N.E., Liotta L.A., Harris C.C. Nitric oxide synthase, cyclooxygenase 2, and vascular endothelial growth factor in the angiogenesis of non-small cell lung carcinoma. Clin. Cancer Res. 2000, 6:4739-4744.
66. Marsden P.A., Schappert K.T., Chen H.S., Flowers M., Sundell C.L., Wilcox J.N., Lamas S., Michel T. Molecular cloning and characterization of human endothelial nitric oxide synthase. FEBS Lett. 1992, 307:287-293.
67. Marshall H.E., Merchant K., Stamler J.S. Nitrosation and oxidation in the regulation of gene expression. FASEB J. 2000, 14:1889-1900.
68. Massi D., Franchi A., Sardi I., Magnelli L., Paglierani M., Borgognoni L., Maria Reali U., Santucci M. Inducible nitric oxide synthase expression in benign and malignant cutaneous melanocytic lesions. J. Pathol. 2001, 194:194-200.
69. Melino G., Bernassola F., Knight R.A., Corasaniti M.T., Nistico G., Finazzi-Agro A. S-nitrosylation regulates apoptosis. Nature 1997, 388:432-433.
70. Nikitovic D., Holmgren A., Spyrou G. Inhibition of AP-1 DNA binding by nitric oxide involving conserved cysteine residues in Jun and Fos. Biochem. Biophys. Res. Commun. 1998, 242:109-112.
71. Oess S., Icking A., Fulton D., Govers R., Muller-Esterl W. Subcellular targeting and trafficking of nitric oxide synthases. Biochem. J. 2006, 396:401-409.
72. Palmer R.M., Ferrige A.G., Moncada S. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 1987, 327:524-526.
73. Pervin S., Singh R., Chaudhuri G. Nitric oxide-induced cytostasis and cell cycle arrest of a human breast cancer cell line (MDA-MB-231): potential role of cyclin D1. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:3583-3588.
74. Radi R., Beckman J.S., Bush K.M., Freeman B.A. Peroxynitrite oxidation of sulfhydryls. The cytotoxic potential of superoxide and nitric oxide. J. Biol. Chem. 1991, 266:4244-4250.
75. Rainwater R., Parks D., Anderson M.E., Tegtmeyer P., Mann K. Role of cysteine residues in regulation of p53 function. Mol. Cell. Biol. 1995, 15:3892-3903.
76. Rodriguez-Ariza A., Lopez-Sanchez L.M., González R., Corrales F.J., Lopez P., Bernardos A., Muntane J. Altered protein expression and protein nitration pattern during d-galactosamine-induced cell death in human hepatocytes: a proteomic analysis. Liver Int. 2005, 25:1259-1269.
77. Sase K., Michel T. Expression and regulation of endothelial nitric oxide synthase. Trends Cardiovasc. Med. 1997, 7:28-37.
78. Schmidt H.H., Walter U. NO at work. Cell 1994, 78:919-925.
79. Schweizer M., Richter C. Nitric oxide potently and reversibly deenergizes mitochondria at low oxygen tension. Biochem. Biophys. Res. Commun. 1994, 204:169-175.
80. Seitz S.J., Schleithoff E.S., Koch A., Schuster A., Teufel A., Staib F., Stremmel W., Melino G., Krammer P.H., Schilling T., Muller M. Chemotherapy-induced apoptosis in hepatocellular carcinoma involves the p53 family and is mediated via the extrinsic and the intrinsic pathway. Int. J. Cancer 2010, 126:2049-2066.
81. Sekkai D., Aillet F., Israel N., Lepoivre M. Inhibition of NF-kappaB and HIV-1 long terminal repeat transcriptional activation by inducible nitric oxide synthase 2 activity. J. Biol. Chem. 1998, 273:3895-3900.
82. Siemens D.R., Heaton J.P., Adams M.A., Kawakami J., Graham C.H. Phase II study of nitric oxide donor for men with increasing prostate-specific antigen level after surgery or radiotherapy for prostate cancer. Urology 2009, 74:878-883.
83. Soler M.N., Bobe P., Benihoud K., Lemaire G., Roos B.A., Lausson S. Gene therapy of rat medullary thyroid cancer by naked nitric oxide synthase II DNA injection. J. Gene Med. 2000, 2:344-352.
84. Spiecker M., Peng H.B., Liao J.K. Inhibition of endothelial vascular cell adhesion molecule-1 expression by nitric oxide involves the induction and nuclear translocation of IkappaBalpha. J. Biol. Chem. 1997, 272:30969-30974.
85. Stamler J.S. Redox signaling: nitrosylation and related target interactions of nitric oxide. Cell 1994, 78:931-936.
86. Stamler J.S., Hausladen A. Oxidative modifications in nitrosative stress. Nat. Struct. Biol. 1998, 5:247-249.
87. Stamler J.S., Singel D.J., Loscalzo J. Biochemistry of nitric oxide and its redox-activated forms. Science 1992, 258:1898-1902.
88. Stuehr D.J., Santolini J., Wang Z.Q., Wei C.C., Adak S. Update on mechanism and catalytic regulation in the NO synthases. J. Biol. Chem. 2004, 279:36167-36170.
89. Swana H.S., Smith S.D., Perrotta P.L., Saito N., Wheeler M.A., Weiss R.M. Inducible nitric oxide synthase with transitional cell carcinoma of the bladder. J. Urol. 1999, 161:630-634.
90. Takabuchi S., Hirota K., Nishi K., Oda S., Oda T., Shingu K., Takabayashi A., Adachi T., Semenza G.L., Fukuda K. The inhibitory effect of sodium nitroprusside on HIF-1 activation is not dependent on nitric oxide-soluble guanylyl cyclase pathway. Biochem. Biophys. Res. Commun. 2004, 324:417-423.
91. Thomsen L.L., Lawton F.G., Knowles R.G., Beesley J.E., Riveros-Moreno V., Moncada S. Nitric oxide synthase activity in human gynecological cancer. Cancer Res. 1994, 54:1352-1354.
92. Thomsen L.L., Miles D.W., Happerfield L., Bobrow L.G., Knowles R.G., Moncada S. Nitric oxide synthase activity in human breast cancer. Br. J. Cancer 1995, 72:41-44.
93. Uotila P., Valve E., Martikainen P., Nevalainen M., Nurmi M., Harkonen P. Increased expression of cyclooxygenase-2 and nitric oxide synthase-2 in human prostate cancer. Urol. Res. 2001, 29:23-28.
94. Vakkala M., Kahlos K., Lakari E., Paakko P., Kinnula V., Soini Y. Inducible nitric oxide synthase expression, apoptosis, and angiogenesis in in situ and invasive breast carcinomas. Clin. Cancer Res. 2000, 6:2408-2416.
95. Vaupel P., Mayer A. Hypoxia in cancer: significance and impact on clinical outcome. Cancer Metastasis Rev. 2007, 26:225-239.
96. Vaupel P., Mayer A., Hockel M. Tumor hypoxia and malignant progression. Methods Enzymol. 2004, 381:335-354.
97. Warner T.D., Mitchell J.A., Sheng H., Murad F. Effects of cyclic GMP on smooth muscle relaxation. Adv. Pharmacol. 1994, 26:171-194.
98. Wink D.A., Cook J.A., Christodoulou D., Krishna M.C., Pacelli R., Kim S., DeGraff W., Gamson J., Vodovotz Y., Russo A., Mitchell J.B. Nitric oxide and some nitric oxide donor compounds enhance the cytotoxicity of cisplatin. Nitric Oxide 1997, 1:88-94.
99. Xie Q.W., Cho H.J., Calaycay J., Mumford R.A., Swiderek K.M., Lee T.D., Ding A., Troso T., Nathan C. Cloning and characterization of inducible nitric oxide synthase from mouse macrophages. Science 1992, 256:225-228.
100. Xu L., Eu J.P., Meissner G., Stamler J.S. Activation of the cardiac calcium release channel (ryanodine receptor) by poly-S-nitrosylation. Science 1998, 279:234-237.
101. Xu W., Liu L., Charles I.G. Microencapsulated iNOS-expressing cells cause tumor suppression in mice. FASEB J. 2002, 16:213-215.
102. Yasuda H., Nakayama K., Watanabe M., Suzuki S., Fuji H., Okinaga S., Kanda A., Zayasu K., Sasaki T., Asada M., Suzuki T., Yoshida M., Yamanda S., Inoue D., Kaneta T., Kondo T., Takai Y., Sasaki H., Yanagihara K., Yamaya M. Nitroglycerin treatment may enhance chemosensitivity to docetaxel and carboplatin in patients with lung adenocarcinoma. Clin. Cancer Res. 2006, 12:6748-6757.
103. Ying L., Hofseth L.J. An emerging role for endothelial nitric oxide synthase in chronic inflammation and cancer. Cancer Res. 2007, 67:1407-1410.
104. Zagotta W.N., Siegelbaum S.A. Structure and function of cyclic nucleotide-gated channels. Annu. Rev. Neurosci. 1996, 19:235-263.
105. Zhang J., Dawson V.L., Dawson T.M., Snyder S.H. Nitric oxide activation of poly(ADP-ribose) synthetase in neurotoxicity. Science 1994, 263:687-689.
106. Ziche M., Morbidelli L. Molecular regulation of tumour angiogenesis by nitric oxide. Eur. Cytokine Netw. 2009, 20:164-170.
107. Zou M.H., Hou X.Y., Shi C.M., Nagata D., Walsh K., Cohen R.A. Modulation by peroxynitrite of Akt- and AMP-activated kinase-dependent Ser1179 phosphorylation of endothelial nitric oxide synthase. J. Biol. Chem. 2002, 277:32552-32557.