Applications for nitric oxide in halting proliferation of tumor cells

Biochemical and Biophysical Research Communications

Volumn 431, Issue 4, 2013, Pages 647-651

  Reynolds, Melissa M ^a   Witzeling, Scott D ^a   Damodaran, Vinod B ^a   Medeiros, Tysha N ^a   Knodle, Ryan D ^a   Edwards, Melissa A ^a   Lookian, Pashayar P ^a   Brown, Mark A ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

Adjuvant therapy; Cancer therapy; Cell signaling; Nitric oxide; Pro drugs

Indexed keywords

ANTINEOPLASTIC AGENT; DIETHYLAMINE; NITRIC OXIDE; NITRIC OXIDE DONOR;

ADJUVANT THERAPY; ANAPHYLAXIS; ANIMAL CELL; BREAST CANCER; CANCER CHEMOTHERAPY; CANCER THERAPY; CELL PROLIFERATION; DRUG DELIVERY SYSTEM; HUMAN; HUMAN CELL; LUNG NON SMALL CELL CANCER; MOUSE; NONHUMAN; PRIORITY JOURNAL; SHORT SURVEY; TUMOR CELL;

APOPTOSIS; CELL PROLIFERATION; DRUG RESISTANCE, NEOPLASM; HUMANS; NEOPLASMS; NITRIC OXIDE; NITRIC OXIDE DONORS;

EID: 84875260286     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2013.01.041     Document Type: Short Survey

References (71)

1. Hughes M.N. Chemistry of nitric oxide and related species. Methods in Enzymology 2008, 3-19. Academic Press. K.P. Robert (Ed.).
2. Kroncke K.D. Cysteine-Zn2+ complexes: unique molecular switches for inducible nitric oxide synthase-derived NO. FASEB J. 2001, 15:2503-2507.
3. Osorio J., Recchia F. The role of nitric oxide in metabolism regulation: from basic sciences to the clinical setting. Intensive Care Med. 2000, 26:1395-1398.
4. Moncada S. Nitric oxide: discovery and impact on clinical medicine. J. R. Soc. Med. 1999, 92:164-169.
5. Umansky V., Shirrmacher V. Nitric oxide-induced apoptosis in tumor cells. Adv. Cancer Res. 2001, 82:107-131.
6. Albina J., Reichner J. Role of nitric oxide in mediation of macrophage cytotoxicity and apoptosis. Cancer Metastasis Rev. 1998, 17:39-53.
7. Li H., Hu J., Xin W., Zhao B. Production and interaction of oxygen and nitric oxide free radicals in PMA stimulated macrophages during the respiratory burst. Redox Rep. 2000, 5:353-358.
8. Leiro J., Iglesias R., Paramá A., Sanmartin M.L., Ubeira F.M. Respiratory burst responses of rat macrophages to microsporidian spores. Exp. Parasitol. 2001, 98:1-9.
9. Gkaliagkousi E., Ferro A. Nitric oxide signalling in the regulation of cardiovascular and platelet function. Front. Biosci. 2011, 16:1873-1897.
10. Somers M., Harrison D. Reactive oxygen species and the control of vasomotor tone. Curr. Hypertens. Rep. 1999, 1:102-108.
11. Andrew P.J., Mayer B. Enzymatic function of nitric oxide synthases. Cardiovasc. Res. 1999, 43:521-531.
12. Wink D., Hines H., Cheng R., Switzer C., Flores-Santana W., Vitek M., Ridnour L., Colton C. Nitric oxide and the redox mechanisms in the immune response. J. Leukocyte Biol. 2011, 89:873-891.
13. Binder C., Schulz M., Hiddemann W., Oellerich M. Induction of inducible nitric oxide synthase is an essential part of tumor necrosis factor-alpha-induced apoptosis. Lab. Invest. 1999, 79:1703-1712.
14. Farias-Eisner R., Sherman M.P., Aeberhard E., Chaudhuri G. Nitric oxide is an important mediator for tumoricidal activity in vivo. Proc. Natl. Acad. Sci. USA 1994, 91:9407-9411.
15. Sarti P., Forte E., Mastronicola D., Giuffrè A., Arese M. Cytochrome c oxidase and nitric oxide in action: molecular mechanisms and pathophysiological implications. Biochim. Biophys. Acta Bioenerg. 1817, 2012:610-619.
16. Boyd C.S., Cadenas E. Nitric oxide and cell signaling pathways in mitochondrial-dependent apoptosis. Biol. Chem. 2002, 411.
17. Switzer C.H., Flores-Santana W., Mancardi D., Donzelli S., Basudhar D., Ridnour L.A., Miranda K.M., Fukuto J.M., Paolocci N., Wink D.A. The emergence of nitroxyl (HNO) as a pharmacological agent. Biochim. Biophys. Acta Bioenerg. 2009, 1787:835-840.
18. Serafim R., Primi M., Trossini G., Ferreira E. Nitric oxide: state of the art in drug design. Curr. Med. Chem. 2012, 19:386-405.
19. Burgaud J., Ongini E., Del Soldato P. Nitric oxide-releasing drugs: a novel class of effective and safe therapeutic agents. Ann. NY Acad. Sci. 2002, 962:360-371.
20. Huerta S., Chilka S., Bonavida B. Nitric oxide donors: novel cancer therapeutics. Int. J. Oncol. 2008, 33:909-927.
21. Lefèvre-Groboillot D., Boucher J.-L., Mansuy D., Stuehr D.J. Reactivity of the heme-dioxygen complex of the inducible nitric oxide synthase in the presence of alternative substrates. FEBS J. 2006, 273:180-191.
22. Bredt D. Endogenous nitric oxide synthesis: biological functions and pathophysiology. Free Radical Res. 1999, 31:577-596.
23. Derbyshire E.R., Marletta M.A. Structure and regulation of soluble guanylate cyclase. Ann. Rev. Biochem. 2012, 81:533-559.
24. Hess D.T., Stamler J.S. Regulation by S-nitrosylation of protein post-translational modification. J. Biol. Chem. 2012, 287:4411-4418.
25. MacMicking J., Xie Q.-w., Nathan C. Nitric oxide and macrophage function. Ann. Rev. Immunol. 1997, 15:323-350.
26. Hirst D., Robson T. Nitrosative stress as a mediator of apoptosis: implications for cancer therapy. Curr. Pharm. Des. 2010, 16:45-55.
27. Singh S., Gupta A. Nitric oxide: role in tumour biology and iNOS/NO-based anticancer therapies. Cancer Chemother. Pharmacol. 2011, 67:1211-1224.
28. Masini E., Cianchi F., Mastroianni R., Cuzzocrea S. Nitric oxide expression in cancer: nitric oxide (NO) and cancer 2010, 59-82. Springer, New York. B. Bonavida (Ed.).
29. Kröncke K.-D., Fehsel K., Kolb-Bachofen V. Nitric oxide: cytotoxicity versus cytoprotection- how, why, when, and where?. Nitric Oxide 1997, 1:107-120.
30. Wang Z. Protein S-nitrosylation and cancer. Cancer Lett. 2012, 320:123-129.
31. Rigas B. Novel agents for cancer prevention based on nitric oxide. Biochem. Soc. Trans. 2007, 35:1364-1368.
32. Hibbs J., Taintor R., Vavrin Z. Macrophage cytotoxicity: role for L-arginine deiminase and imino nitrogen oxidation to nitrite. Science 1987, 235:473-476.
33. Hibbs J.B., Taintor R.R., Vavrin Z., Rachlin E.M. Nitric oxide: a cytotoxic activated macrophage effector molecule. Biochem. Biophys. Res. Commun. 1988, 157:87-94.
34. Thatcher G.R.J., Nicolescu A.C., Bennett B.M., Toader V. Nitrates and no release: contemporary aspects in biological and medicinal chemistry. Free Radical Biol. Med. 2004, 37:1122-1143.
35. Engin A. Dual function of nitric oxide in carcinogenesis reappraisal. Curr. Drug Metabol. 2011, 12:891-899.
36. Chinje E., Stratford I. Role of nitric oxide in growth of solid tumours: a balancing act. Essays Biochem. 1997, 32:61-72.
37. Lala P.K., Chakraborty C. Role of nitric oxide in carcinogenesis and tumour progression. Lancet Oncol. 2001, 2:149-156.
38. Brune B. Nitric oxide: no apoptosis or turning it on. Cell Death Differ. 2003, 10:864-869.
39. Melino G., Bernassola F., Knight R., Corasaniti M., Nistico G., Finazzi-Agro A. S-nitrosylation regulates apoptosis. Nature 1997, 388:432-433.
40. Aranda E., Lopez-Pedrera C., De La Haba-Rodriguez J., Rodriguez-Ariza A. Nitric oxide and cancer: the emerging role of S-nitrosylation. Curr. Mol. Med. 2012, 12:50-67.
41. Koriyama Y., Kamiya M., Takadera T., Arai K., Sugitani K., Ogai K., Kato S. Protective action of nipradilol mediated through S-nitrosylation of Keap1 and HO-1 induction in retinal ganglion cells. Neurochem. Int. 2012, 61:1242-1253.
42. Inadomi C., Murata H., Ihara Y., Goto S., Urata Y., Yodoi J., Kondo T., Sumikawa K. Overexpression of glutaredoxin protects cardiomyocytes against nitric oxide-induced apoptosis with suppressing the S-nitrosylation of proteins and nuclear translocation of GAPDH. Biochem. Biophys. Res. Commun. 2012, 425:656-661.
43. Switzer C., Cheng R., Ridnour L., Glynn S., Ambs S., Wink D. Ets-1 is a transcriptional mediator of oncogenic nitric oxide signaling in estrogen receptor-negative breast cancer. Breast Cancer Res. 2012, 14:R125.
44. Cronauer M., Ince Y., Engers R., Rinnab L., Weidemann W., Suschek C., Burchardt M., Kleinert H., Wiedemann J., Sies H., Ackermann R., Kroncke K. Nitric oxide-mediated inhibition of androgen receptor activity: possible implications for prostate cancer progression. Oncogene 2007, 26:1875-1884.
45. 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. USA 2001, 98:3583-3588.
46. 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.
47. Bonavida B., Baritaki S., Huerta-Yepez S., Vega M.I., Jazirehi A.R., Berenson J. Nitric oxide donors are a new class of anti-cancer therapeutics for the reversal of resistance and inhibition of metastasis nitric oxide (NO) and cancer 2010, 459-477. Springer, New York. B. Bonavida (Ed.).
48. Millet A., Bettaieb A., Renaud F., Prevotat L., Hammann A., Solary E., Mignotte B., Jeannin J.F. Influence of the nitric oxide donor glyceryl trinitrate on apoptotic pathways in human colon cancer cells. Gastroenterology 2002, 123:235-246.
49. Postovit L.-M., Adams M.A., Lash G.E., Heaton J.P.W., Graham C.H. Nitric oxide-mediated regulation of hypoxia-induced B16F10 melanoma metastasis. Int. J. Cancer 2004, 108:47-53.
50. Frederiksen L.J., Sullivan R., Maxwell L.R., Macdonald-Goodfellow S.K., Adams M.A., Bennett B.M., Siemens D.R., Graham C.H. Chemosensitization of cancer in vitro and in vivo by nitric oxide signaling. Clin. Cancer Res. 2007, 13:2199-2206.
51. Wang F., Zhang R., Xia T., Hsu E., Cai Y., Gu Z., Hankinson O. Inhibitory effects of nitric oxide on invasion of human cancer cells. Cancer Lett. 2007, 257:274-282.
52. Kitamura Y., Kamoshima W., Shimohama S., Nomura Y., Taniguchi T. Nitric oxide donor-induced p53-sensitive cell death is enhanced by Bcl-2 reduction in human neuroblastoma cells. Neurochem. Int. 1998, 32:93-102.
53. Kamoshima W., Kitamura Y., Nomura Y., Taniguchi T. Possible involvement of ADP-ribosylation of particular enzymes in cell death induced by nitric oxide-donors in human neuroblastoma cells. Neurochem. Int. 1997, 30:305-311.
54. Janssens M.Y., Verovski V.N., Van den Berge D.L., Monsaert C.C., Storme G.A. Radiosensitization of hypoxic tumour cells by S-nitroso-N-acetylpenicillamine implicates a bioreductive mechanism of nitric oxide generation. Br. J. Cancer 1999, 79:1085-1089.
55. Jeon H.K., Choi S.U., Jung N.P. Association of the ERK1/2 and p38 kinase pathways with nitric oxide-induced apoptosis and cell cycle arrest in colon cancer cells. Cell Biol. Toxicol. 2005, 21:115-125.
56. Liu Q., Chan S.T.F., Mahendran R. Nitric oxide induces cyclooxygenase expression and inhibits cell growth in colon cancer cell lines. Carcinogenesis 2003, 24:637-642.
57. Inoue S., Kawanishi S. Oxidative DNA damage induced by simultaneous generation of nitric oxide and superoxide. FEBS Lett. 1995, 371:86-88.
58. Dairou J., Atmane N., Rodrigues-Lima F., Dupret J.-M. Peroxynitrite irreversibly inactivates the human xenobioticmetabolizing enzyme arylamine N-acetyltransferase 1 (nat1) in human breast cancer cells. J. Biol. Chem. 2004, 279:7708-7714.
59. Oh-hashi K., Maruyama W., Yi H., Takahashi T., Naoi M., Isobe K. Mitogen-activated protein kinase pathway mediates peroxynitrite-induced apoptosis in human dopaminergic neuroblastoma SH-SY5Y cells. Biochem. Biophys. Res. Commun. 1999, 263:504-509.
60. Keefer L.K. Fifty years of diazeniumdiolate research. From laboratory curiosity to broad-spectrum biomedical advances. ACS Chem. Biol. 2011, 6:1147-1155.
61. Simeone A.-M., Colella S., Krahe R., Johnson M.M., Mora E., Tari A.M. N-(4-Hydroxyphenyl)retinamide and nitric oxide pro-drugs exhibit apoptotic and anti-invasive effects against bone metastatic breast cancer cells. Carcinogenesis 2006, 27:568-577.
62. Janssens M.Y., Van den Berge D.L., Verovski V.N., Monsaert C., Storme G.A. Activation of inducible nitric oxide synthase results in nitric oxide-mediated radiosensitization of hypoxic emt-6 tumor cells. Cancer Res. 1998, 58:5646-5648.
63. Jarry A., Charrier L., Bou-Hanna C., Devilder M.-C., Crussaire V., Denis M.G., Vallette G., Laboisse C.L. Position in cell cycle controls the sensitivity of colon cancer cells to nitric oxide-dependent programmed cell death. Cancer Res. 2004, 64:4227-4234.
64. Srisook K., Jung N.-H., Kim B.-R., Cha S.-H., Kim H.-S., Cha Y.-N. Heme oxygenase-1-mediated partial cytoprotective effect by NO on cadmium-induced cytotoxicity in C6 rat glioma cells. Toxicol. In Vitro 2005, 19:31-39.
65. Niziolek M., Korytowski W., Girotti A.W. Chain-breaking antioxidant and cytoprotective action of nitric oxide on photodynamically stressed tumor cells. Photochem. Photobiol. 2003, 78:262-270.
66. Pervin S., Singh R., Freije W.A., Chaudhuri G. MKP-1-induced dephosphorylation of extracellular signal-regulated kinase is essential for triggering nitric oxide-induced apoptosis in human breast cancer cell lines. Cancer Res. 2003, 63:8853-8860.
67. Pervin S., Singh R., Gau C.-L., Edamatsu H., Tamanoi F., Chaudhuri G. Potentiation of nitric oxide-induced apoptosis of mda-mb-468 cells by farnesyltransferase inhibitor. Cancer Res. 2001, 61:4701-4706.
68. Maciag A.E., Chakrapani H., Saavedra J.E., Morris N.L., Holland R.J., Kosak K.M., Shami P.J., Anderson L.M., Keefer L.K. The nitric oxide prodrug JS-K is effective against non-small-cell lung cancer cells in vitro and in vivo: involvement of reactive oxygen species. J. Pharmacol. Exp. Ther. 2011, 336:313-320.
69. Kiziltepe T., Hideshima T., Ishitsuka K., Ocio E.M., Raje N., Catley L., Li C.-Q., Trudel L.J., Yasui H., Vallet S., Kutok J.L., Chauhan D., Mitsiades C.S., Saavedra J.E., Wogan G.N., Keefer L.K., Shami P.J., Anderson K.C. JS-K, a GST-activated nitric oxide generator, induces DNA double-strand breaks, activates DNA damage response pathways, and induces apoptosis in vitro and in vivo in human multiple myeloma cells. Blood 2007, 110:709-718.
70. Hou Y., Wang J., Andreana P.R., Cantauria G., Tarasia S., Sharp L., Braunschweiger P.G., Wang P.G. Targeting nitric oxide to cancer cells: cytotoxicity studies of glyco-S-nitrosothiols. Bioorg. Med. Chem. Lett. 1999, 9:2255-2258.
71. Damodaran V.B., Place L.W., Kipper M.J., Reynolds M.M. Enzymatically degradable nitric oxide releasing S-nitrosated dextran thiomers for biomedical applications. J. Mater. Chem. 2012, 22:23038-23048.