Nitric oxide-mediated sensitization of resistant tumor cells to apoptosis by chemo-immunotherapeutics

Redox Biology

Volumn 6, Issue , 2015, Pages 486-494

  Bonavida, Benjamin ^a   Garban, Hermes ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Apoptosis; Chemotherapeutic drugs; Nitric oxide; Nitrosylation; Sensitization; Trail DR5

Indexed keywords

3,3 BIS(2 AMINOETHYL) 1 HYDROXY 2 OXOTRIAZENE; ANTINEOPLASTIC AGENT; BORTEZOMIB; CAMPTOTHECIN; CISPLATIN; CYTOTOXIC AGENT; DEATH RECEPTOR 5; ENDOTHELIAL NITRIC OXIDE SYNTHASE; FAS ANTIGEN; GAMMA INTERFERON; GLYCERYL TRINITRATE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1; NAVELBINE; NITRIC OXIDE; NITRIC OXIDE DONOR; PHOSPHATIDYLETHANOLAMINE BINDING PROTEIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN FARNESYLTRANSFERASE INHIBITOR; PROTEIN P50; RITUXIMAB; SALINOSPORAMIDE A; SMALL INTERFERING RNA; SYNAPTOTAGMIN I; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR YY1; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; CANCER CHEMOTHERAPY; CANCER GENE THERAPY; CANCER IMMUNOTHERAPY; CANCER INHIBITION; CANCER RESISTANCE; COLORECTAL CARCINOMA; DRUG SENSITIVITY; EPITHELIAL MESENCHYMAL TRANSITION; GENE REPRESSION; GLIOMA; HUMAN; LUNG CANCER; METASTASIS INHIBITION; NITROSYLATION; NON SMALL CELL LUNG CANCER; NONHUMAN; PRIORITY JOURNAL; PROSTATE CANCER; REVIEW; TRANSCRIPTION REGULATION; TUMOR CELL; UPREGULATION; ANIMAL; DRUG POTENTIATION; DRUG RESISTANCE; DRUG SCREENING; IMMUNOTHERAPY; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; DRUG RESISTANCE, NEOPLASM; DRUG SCREENING ASSAYS, ANTITUMOR; DRUG SYNERGISM; HUMANS; IMMUNOTHERAPY; NITRIC OXIDE; NITRIC OXIDE DONORS; SIGNAL TRANSDUCTION;

EID: 84942579482     PISSN: 22132317     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.redox.2015.08.013     Document Type: Review

References (130)

1. Aggarwal B.B. Signalling pathways of the TNF superfamily: a double-edged sword. Nat. Rev. Immunol. 2003, 3:745-756.
2. Aggarwal B.B. Nuclear factor-kappa-B: the enemy within. Cancer Cell 2004, 6:203-208.
3. Fariaseisner 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.
4. 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 in MCF-7 and other epithelial tumor cells. Lab. Investig. 1999, 79:1703-1712.
5. Bredt D.S. Endogenous nitric oxide synthesis: biological functions and pathophysiology. Free Radic. Res. 1999, 31:577-596.
6. Boyd C.S., Cadenas E. Nitric oxide and cell signaling pathways in mitochondrial-dependent apoptosis. Biol. Chem. 2002, 383:411-423.
7. Burgaud J.L., Ongini E., Del Soldato P. Nitric oxide-releasing drugs - a novel class of effective and safe therapeutic agents. Nitric Oxide: Novel Actions, Deleterious Effects and Clinical Potential 2002, 360-371. C.C. Chiueh, J.S. Hong, S.K. Leong (Eds.).
8. Huerta S., Chilka S., Bonavida B. Nitric oxide donors: novel cancer therapeutics (Review). Int. J. Oncol. 2008, 33:909-927.
9. 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 2009, 1787. 835-40.
10. Wink D.A., Hines H.B., Cheng R.Y., Switzer C.H., Flores-Santana W., Vitek M.P., Ridnour L.A., Colton C.A. Nitric oxide and redox mechanisms in the immune response. J. Leukoc. Biol. 2011, 89:873-891.
11. Reynolds M.M., Witzeling S.D., Damodaran V.B., Medeiros T.N., Knodle R.D., Edwards M.A., Lookian P.P., Brown M.A. Applications for nitric oxide in halting proliferation of tumor cells. Biochem. Biophys. Res. Commun. 2013, 431:647-651.
12. Ignarro L.J. Nitric Oxide: Biology and Pathobiology 2009, Elsevier Science, Burlington, MA.
13. Bonavida B. Nitric Oxide (NO) and Cancer: Prognosis, Prevention, and Therapy 2010, Springer, New York.
14. Bredt D.S., Snyder S.H. Nitric-oxide: a physiological messenger molecule. Ann. Rev. Biochem. 1994, 63:175-195.
15. Kroncke K.D. Zinc finger proteins as molecular targets for nitric oxide-mediated gene regulation. Antioxid. Redox Signal. 2001, 3:565-575.
16. Stamler J.S., Jia L., Eu J.P., McMahon T.J., Demchenko I.T., Bonaventura J., Gernert K., Piantadosi C.A. Blood flow regulation by S-nitrosohemoglobin in the physiological oxygen gradient. Science 1997, 276:2034-2037.
17. Hess D.T., Matsumoto A., Nudelman R., Stamler J.S. S-nitrosylation: spectrum and specificity. Nat. Cell Biol. 2001, 3:E46-E49.
18. Stamler J.S., Lamas S., Fang F.C. Nitrosylation: the prototypic redox-based signaling mechanism. Cell 2001, 106:675-683.
19. Garban H.J., Marquez-Garban D.C., Pietras R.J., Ignarro L.J. Rapid nitric oxide-mediated S-nitrosylation of estrogen receptor: regulation of estrogen-dependent gene transcription. Proc. Natl. Acad. Sci. USA 2005, 102:2632-2636.
20. Braughler J.M., Mittal C.K., Murad F. Effects of thiols, sugars, and proteins on nitric-oxide activation of guanylate-cyclase. J. Biol. Chem. 1979, 254:2450-2454.
21. Lewicki J.A., Brandwein H.J., Mittal C.K., Arnold W.P., Murad F. Proteins of purified soluble guanylate-cyclase activated by nitric-oxide and sodium-nitroprusside. J. Cycl. Nucleotide Res. 1982, 8:17-25.
22. Bian K., Murad F. sGC-cGMP signaling: target for anticancer therapy. Adv. Exp. Med. Biol. 2014, 814:5-13.
23. Bian K., Murad F. What is next in nitric oxide research? From cardiovascular system to cancer biology. Nitric Oxide 2014, 43:3-7.
24. Foster M.W., McMahon T.J., Stamler J.S. S-nitrosylation in health and disease. Trends Mol. Med. 2003, 9:160-168.
25. Andrew P.J., Mayer B. Enzymatic function of nitric oxide synthases. Cardiovasc. Res. 1999, 43:521-531.
26. Sarti P., Forte E., Mastronicola D., Giuffre A., Arese M. Cytochrome c oxidase and nitric oxide in action: molecular mechanisms and pathophysiological implications. Biochim. Biophys. Acta 2012, 1817. 610-9.
27. Kim P.K., Zamora R., Petrosko P., Billiar T.R. The regulatory role of nitric oxide in apoptosis. Int. Immunopharmacol. 2001, 1:1421-1441.
28. Porasuphatana S., Tsai P., Rosen G.M. The generation of free radicals by nitric oxide synthase. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 2003, 134:281-289.
29. Zou H., Li Y., Liu X., Wang X. An APAF-1 cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9. J. Biol. Chem. 1999, 274:11549-11556.
30. Sedlak T.W., Snyder S.H. Messenger molecules and cell death: therapeutic implications. J. Am. Med. Assoc. 2006, 295:81-89.
31. Serafim R.A., Primi M.C., Trossini G.H., Ferreira E.I. Nitric oxide: state of the art in drug design. Curr. Med. Chem. 2012, 19:386-405.
32. Arrieta O., Blake M., de la Mata-Moya M.D., Corona F., Turcott J., Orta D., Alexander-Alatorre J., Gallardo-Rincon D. Phase II study. Concurrent chemotherapy and radiotherapy with nitroglycerin in locally advanced non-small cell lung cancer. Radiother. Oncol. 2014, 111:311-315.
33. Bonavida B. Nitric Oxide and Cancer: Pathogenesis and Therapy 2015, Springer International Publishing.
34. Huerta-Yepez S., Vega M., Jazirehi A., Garban H., Hongo F., Cheng G.H., 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.
35. Jazirehi A.R., Vega M.I., Chatterjee D., Goodglick L., Bonavida B. Inhibition of the Raf-MEK1/2-ERK1/2 signaling pathway, BCL-xL down-regulation, and chemosensitization of non-Hodgkin's lymphoma B cells by rituximab. Cancer Res. 2004, 64:7117-7126.
36. Vega M.I., Jazirehi A.R., Huerta-Yepez S., Bonavida B. Rituximab-induced inhibition of YY1 and Bcl-xL expression in Ramos non-Hodgkin's lymphoma cell line via inhibition of NF-kappa B activity: role of YY1 and Bcl-xL in Fas resistance and chemoresistance, respectively. J. Immunol. 2005, 175:2174-2183.
37. Baritaki S., Yeung K., Palladino M., Berenson J., Bonavida B. Pivotal roles of snail inhibition and RKIP induction by the proteasome inhibitor NPI-0052 in tumor cell chemoimmunosensitization. Cancer Res. 2009, 69:8376-8385.
38. Bonavida B., Baritaki S. The novel role of yin yang 1 in the regulation of epithelial to mesenchymal transition in cancer via the dysregulated NF-κB/Snail/YY1/RKIP/PTEN Circuitry. Crit. Rev. Oncog. 2011, 16(3-4):211-226.
39. DiDonato J.A., Mercurio F., Karin M. NF-kappaB and the link between inflammation and cancer. Immunol Rev. 2012, 246:379-400.
40. Karin M., Lin A. NF-kappa B at the crossroads of life and death. Nat. Immunol. 2002, 3:221-227.
41. Hongo F., Garban H., Huerta-Yepez S., Vega M., Jazirehi A.R., Mizutani Y., Miki T., Bonavida B. Inhibition of the transcription factor Yin Yang 1 activity by S-nitrosation. Biochem. Biophys. Res. Commun. 2005, 336:692-701.
42. Wang H., Hertlein E., Bakkar N., Sun H., Acharyya S., Wang J., Carathers M., Davuluri R., Guttridge D.C. Inhibition of the transcription factor Yin Yang 1 activity by S-nitrosation. Biochem. Biophys. Res. Commun. 2005, 336:692-701. ; Mol. Cell Biol 27 (2007) 4374-4387.
43. Kleinberg L., Davidson B. Cell survival and apoptosis-related molecules in cancer cells in effusions: a comprehensive review. Diagn. Cytopathol. 2009, 37:613-624.
44. Katsman A., Umezawa K., Bonavida B. Reversal of resistance to cytotoxic cancer therapies: DHMEQ as a chemo-sensitizing and immuno-sensitizing agent. Drug Resist. Updates 2007, 10:1-12.
45. Baritaki S., Suzuki E., Umezawa K., Spandidos D.A., Berenson J., Daniels T.R., Penichet M.L., Jazirehi A.R., Palladino M., Bonavida B. Inhibition of Yin Yang 1-dependent repressor activity of DR5 transcription and expression by the novel proteasome inhibitor NPI-0052 contributes to its TRAIL-enhanced apoptosis in cancer cells. J. Immunol. 2008, 180:6199-6210.
46. Brown M., Cohen J., Arun P., Chen Z., Van Waes C. NF-κB in carcinoma therapy and prevention. Expert Opin. Therap. Targets 2008, 12:1109-1122.
47. Baritaki S., Chapman A., Yeung K., Spandidos D.A., Palladino M., Bonavida B. Inhibition of epithelial to mesenchymal transition in metastatic prostate cancer cells by the novel proteasome inhibitor, NPI-0052: pivotal roles of Snail repression and RKIP induction. Oncogene 2009, 28:3573-3585.
48. Mauro C., Zazzeroni F., Papa S., Bubici C., Franzoso G. The NF-kappaB transcription factor pathway as a therapeutic target in cancer: methods for detection of NF-kappaB activity. Methods Mol. Biol. (Clifton, N.J.) 2009, 512:169-207.
49. Wink D.A., Ridnour L.A., Hussain S.P., Harris C.C. The reemergence of nitric oxide and cancer. Nitric Oxide 2008, 19:65-67.
50. Katsuyama K., Shichiri M., Marumo F., Hirata Y. NO inhibits cytokine-induced iNOS expression and NF-kappa B activation by interfering with phosphorylation and degradation of I kappa B-alpha. Arterioscler. Thromb. Vasc. Biol. 1998, 18:1796-1802.
51. 2-dependent activation of nuclear factor kappa B. Role in sensitization of human tumor cells to tumor necrosis factor-alpha-induced cytotoxicity. J. Biol. Chem. 2001, 276:8918-8923.
52. Connelly L., Palacios-Callender M., Ameixa C., Moncada S., Hobbs A.J. Biphasic regulation of NF-kappa B activity underlies the pro- and anti-inflammatory actions of nitric oxide. J. Immunol. 2001, 166:3873-3881.
53. Marshall H.E., Stamler J.S. Inhibition of NF-kappa B by S-nitrosylation. Biochemistry 2001, 40:1688-1693.
54. Nieto M.A. The snail superfamily of zinc-finger transcription factors. Nat. Rev. Mol. Cell Biol. 2002, 3:155-166.
55. Wu Y., Zhou B.P. Snail: More than EMT. Cell Adhes. Migr. 2010, 4:199-203.
56. Julien S., Puig I., Caretti E., Bonaventure J., Nelles L., van Roy F., Dargemont C., de Herreros A.G., Bellacosa A., Larue L. Activation of NF-kappaB by Akt upregulates snail expression and induces epithelium mesenchyme transition. Oncogene 2007, 26:7445-7456.
57. Palmer M.B., Majumder P., Cooper J.C., Yoon H., Wade P.A., Boss J.M. Yin yang 1 regulates the expression of snail through a distal enhancer. Mol. Cancer Res. 2009, 7:221-229.
58. Cano A., Pérez-Moreno M.A., Rodrigo I., Locascio A., Blanco M.J., del Barrio M.G., Portillo F., Nieto M.A. The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat. Cell Biol. 2000, 2:76-83.
59. Beach S., Tang H., Park S., Dhillon A.S., Keller E.T., Kolch W., Yeung K.C. Snail is a repressor of RKIP transcription in metastatic prostate cancer cells. Oncogene 2008, 27:2243-2248.
60. Gordon S., Akopyan G., Garban H., Bonavida B. Transcription factor YY1: Structure, function, and therapeutic implications in cancer biology. Oncogene 2006, 25:1125-1142.
61. Garban H.J., Bonavida B. Nitric oxide inhibits the transcription repressor Yin-Yang 1 binding activity at the silencer region of the Fas promoter: a pivotal role for nitric oxide in the up-regulation of Fas gene expression in human tumor cells. J. Immunol. 2001, 167:75-81.
62. Baritaki S., Katsman A., Chatterjee D., Yeung K.C., Spandidos D.A., Bonavida B. Regulation of tumor cell sensitivity to TRAIL-induced apoptosis by the metastatic suppressor Raf kinase inhibitor protein via Yin Yang 1 inhibition and death receptor 5 up-regulation. J. Immunol. 2007, 179:5441-5453.
63. Hongo F., Garban H., Huerta-Yepez S., Vega M., Jazirehi A.R., Mizutani Y., Miki T., Bonavida B. Inhibition of the transcription factor Yin Yang 1 activity by S-nitrosation. Biochem. Biophys. Res. Commun. 2005, 336:692-701.
64. Granovsky A.E., Rosner M.R. Raf kinase inhibitory protein: a signal transduction modulator and metastasis suppressor. Cell Res. 2008, 18:452-457.
65. Yeung K., Seitz T., Li S., Janosch P., McFerran B., Kaiser C., Fee F., Katsanakis K.D., Rose D.W., Mischak H., Sedivy J.M., Kolch W. Suppression of Raf-1 kinase activity and MAP kinase signalling by RKIP. Nature 1999, 401:173-177.
66. Tang H., Park S., Sun S.C., Trumbly R., Ren G., Tsung E., Yeung K.C., Rose R.K.I.P.inhibits N.F.- D.W., Mischak H., Sedivy J.M. W. Kolcgnaling components of the IκB kinase complex. FEBS Lett. 2010, 584:662-668.
67. Lorenz K., Lohse M.J., Quitterer U. Protein kinase C switches the Raf kinase inhibitor from Raf-1 to GRK-2. Nature 2003, 426:574-579.
68. Fu Z., Smith P.C., Zhang L., Rubin M.A., Dunn R.L., Yao Z., Keller E.T. Effects of Raf kinase inhibitor protein expression on suppression of prostate cancer metastasis. J. Natl. Cancer Inst. 2003, 95:878-889.
69. Schuierer M.M., Bataille F., Hagan S., Kolch W., Bosserhoff A.K. Reduction in Raf kinase inhibitor protein expression is associated with increased Ras-extracellular signal-regulated kinase signaling in melanoma cell lines. Cancer Res. 2004, 64:5186-5192.
70. Hagan S., Al-Mulla F., Mallon E., Oien K., Ferrier R., Gusterson B., Curto García J.J., Kolch W. Reduction of Raf-1 kinase inhibitor protein expression correlates with breast cancer metastasis. Clin. Cancer Res. 2005, 11:7392-7397.
71. Al-Mulla F., Hagan S., Behbehani A.I., Bitar M.S., George S.S., Going J.J., Curto García J.J., Scott L., Fyfe N., Murray G.I., Kolch W. Raf kinase inhibitor protein expression in a survival analysis of colorectal cancer patients. J. Clin. Oncol. 2006, 24:5672-5679.
72. Fu Z., Kitagawa Y., Shen R., Shah R., Mehra R., Rhodes D., Keller P.J., Mizokami A., Dunn R., Chinnaiyan A.M., Yao Z., Keller E.T. Metastasis suppressor gene Raf kinase inhibitor protein (RKIP) is a novel prognostic marker in prostate cancer. Prostate 2006, 66:248-256.
73. Carracedo A., Pandolfi P.P. The PTEN-PI3K pathway: of feedbacks and cross-talks. Oncogene 2008, 27:5527-5541.
74. Zamai L., Ahmad M., Bennett I.M., Azzoni L., Alnemri E.S., Perussia B. Natural killer (NK) cell-mediated cytotoxicity: differential use of TRAIL and Fas ligand by immature and mature primary human NK cells. J. Exp. Med. 1998, 188:2375-2380.
75. Bonavida B. Sensitization of Cancer Cells for Chemo/Immuno/Radio-therapy 2008, Human Press of Springer Science+Business Media, Totowa, NJ.
76. Keefer L.K., Nims R.W., Davies K.M., Wink D.A. "NONOates" (1-substituted diazen-1-ium-1,2-diolates) as nitric oxide donors: convenient nitric oxide dosage forms. Methods Enzymol. 1996, 268:281-293.
77. Smith D.J., Chakravarthy D., Pulfer S., Simmons M.L., Hrabie J.A., Citro M.L., Saavedra J.E., Davies K.M., Hutsell T.C., Mooradian D.L., Hanson S.R., Keefer L.K. Nitric oxide-releasing polymers containing the [N(O)NO]- group. J. Med. Chem. 1996, 39:1148-1156.
78. Garban H.J., Bonavida B. Nitric oxide sensitizes ovarian tumor cells to Fas-induced apoptosis. Gynecol. Oncol. 1999, 73:257-264.
79. Beg A.A., Baltimore D. An essential role for NF-kappa B in preventing TNF-alpha-induced cell death. Science 1996, 274:782-784.
80. Wang C.Y., Mayo M.W., Baldwin A.S. TNF- and cancer therapy-induced apoptosis: potentiation by inhibition of NF-kappaB. Science 1996, 274:784-787.
81. Tartaglia L.A., Goeddel D.V. Two TNF receptors. Immunol Today 1992, 13:151-153.
82. GarciaRuiz C., Colell A., Mari M., Morales A., FernandezCheca J.C. Direct effect of ceramide on the mitochondrial electron transport chain leads to generation of reactive oxygen species - role of mitochondrial glutathione. J. Biol. Chem. 1997, 272:11369-11377.
83. Suzuki Y.J., Forman H.J., Sevanian A. Oxidants as stimulators of signal transduction. Free Radic. Biol. Med. 1997, 22:269-285.
84. Fukuto J.M. Chemistry of nitric oxide: biologically relevant aspects. Adv. Pharmacol. (San Diego, Calif.) 1995, 34:1-15.
85. Leverkus M., Sprick M.R., Wachter T., Mengling T., Baumann B., Serfling E., Brocker E.B., Goebeler M., Neumann M., Walczak H. Proteasome inhibition results in TRAIL sensitization of primary keratinocytes by removing the resistance-mediating block of effector caspase maturation. Mol. Cell Biol. 2003, 23:777-790.
86. Wang S., El-Deiry W.S. TRAIL and apoptosis induction by TNF-family death receptors. Oncogene 2003, 22:8628-8633.
87. Baritaki S., Huerta-Yepez S., Sakai T., Spandidos D.A., Bonavida B. Chemotherapeutic drugs sensitize cancer cells to TRAIL-mediated apoptosis: up-regulation of DR5 and inhibition of Yin Yang 1. Mol. Cancer Therap. 2007, 6:1387-1399.
88. Jazirehi A.R., Bonavida B. Resveratrol modifies the expression of apoptotic regulatory proteins and sensitizes non-Hodgkin's lymphoma and multiple myeloma cell lines to paclitaxel-induced apoptosis. Mol. Cancer Ther. 2004, 3:71-84.
89. Huerta-Yepez S., Baritaki S., Baay-Guzman G., Hernandez-Luna M.A., Hernandez-Cueto A., Vega M.I., Bonavida B. Contribution of either YY1 or BclXL-induced inhibition by the NO-donor DETANONOate in the reversal of drug resistance, both in vitro and in vivo YY1 and BclXL are overexpressed in prostate cancer. Nitric oxide: Biol. Chem. / Off. J. Nitric Oxide Soc. 2013, 29:17-24.
90. Huerta S., Baay-Guzman G., Gonzalez-Bonilla C.R., Livingston E.H., Huerta-Yepez S., Bonavida B. In vitro and in vivo sensitization of SW620 metastatic colon cancer cells to CDDP-induced apoptosis by the nitric oxide donor DETANONOate: involvement of AIF. Nitric Oxide-Biol. Chem. 2009, 20:182-194.
91. 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.
92. Kumar A., Takada Y., Boriek A.M., Aggarwal B.B. Nuclear factor-kappaB: its role in health and disease. J. Mol. Med. (Berl.) 2004, 82:434-448.
93. Vega M.I., Jazirehi A.R., Huerta-Yepez S., Bonavida B. Rituximab-induced inhibition of YY1 and Bcl-xL expression in Ramos non-Hodgkin's lymphoma cell line via inhibition of NF-ompounds enhance the cytotoxicity of cisplatin, Nitric Od chemoresistance, respectively. J. Immunol. 2005, 175:2174-2183.
94. Santos-Silva M.C., Sampaio de Freitas M., Assreuy J. Killing of lymphoblastic leukemia cells by nitric oxide and taxol: involvement of NF-kappaB activity. Cancer Lett. 2001, 173:53-61.
95. Sun Y., Rigas B. The thioredoxin system mediates redox-induced cell death in human colon cancer cells: implications for the mechanism of action of anticancer agents. Cancer Res. 2008, 68:8269-8277.
96. Huerta-Yepez S., Vega M., Escoto-Chavez S.E., Murdock B., Sakai T., Baritaki S., Bonavida B. Nitric oxide sensitizes tumor cells to TRAIL-induced apoptosis via inhibition of the DR5 transcription repressor Yin Yang 1. Nitric Oxide 2009, 20:39-52.
97. Baritaki S., Huerta-Yepez S., Sahakyan A., Karagiannides I., Bakirtzi K., Jazirehi A., Bonavida B. Mechanisms of nitric oxide-mediated inhibition of EMT in cancer: inhibition of the metastasis-inducer snail and induction of the metastasis-suppressor RKIP. Cell Cycle 2010, 9:4931-4940.
98. Chatterjee D., Bai Y., Wang Z., Beach S., Mott S., Roy R., Braastad C., Sun Y., Mukhopadhyay A., Aggarwal B.B., Darnowski J., Pantazis P., Wyche J., Fu Z., Kitagwa Y., Keller E.T., Sedivy J.M., Yeung K.C. RKIP sensitizes prostate and breast cancer cells to drug-induced apoptosis. J Biol Chem 2004, 279:17515-17523.
99. Bonavida B. Resistance to Immunotherapeutic Antibodies in Cancer 2: Strategies to Overcome Resistance 2013, Springer, New York.
100. Morimoto H., Yonehara S., Bonavida B. Overcoming tumor necrosis factor and drug resistance of human tumor cell lines by combination treatment with anti-Fas antibody and drugs or toxins. Cancer Res. 1993, 53:2591-2596.
101. Uslu R., Borsellino N., Frost P., Garban H., Ng C.P., Mizutani Y., Belldegrun A., Bonavida B. Chemosensitization of human prostate carcinoma cell lines to anti-fas-mediated cytotoxicity and apoptosis. Clin. Cancer Res. 1997, 3:963-972.
102. Mizutani Y., Nakao M., Ogawa O., Yoshida O., Bonavida B., Miki T. Enhanced sensitivity of bladder cancer cells to tumor necrosis factor related apoptosis inducing ligand mediated apoptosis by cisplatin and carboplatin. J. Urol. 2001, 165:263-270.
103. Garban H.J., Bonavida B. Nitric oxide inhibits the transcription repressor Yin-Yang 1 binding activity at the silencer region of the Fas promoter: a pivotal role for nitric oxide in the up-regulation of Fas gene expression in human tumor cells. J. Immunol. 2001, 167:75-81.
104. Zisman A., Ng C.P., Pantuck A.J., Bonavida B., Belldegrun A.S., Actinomycin D. and gemcitabine synergistically sensitize androgen-independent prostate cancer cells to Apo2L/TRAIL-mediated apoptosis. J. Immunother. 2001, 24:459-471.
105. LaVallee T.M., Zhan X.G.H., Johnson M.S., Herbstritt C.J., Swartz G., Williams M.S., Hembrough W.A., Green S.J., Pribluda V.S. 2-methoxyestradiol up-regulates death receptor 5 and induces apoptosis through activation of the extrinsic pathway. Cancer Res. 2003, 63:468-475.
106. Shigeno M., Nakao K., Ichikawa T., Suzuki K., Kawakami A., Abiru S., Miyazoe S., Nakagawa Y., Ishikawa H., Hamasaki K., Nakata K., Ishii N., Eguchi K. Interferon-alpha sensitizes human hepatoma cells to TRAIL-induced apoptosis through DR5 upregulation and NF-kappa B inactivation. Oncogene 2003, 22:1653-1662.
107. Jazirehi A.R., Bonavida B. Cellular and molecular signal transduction pathways modulated by rituximab (rituxan, anti-CD20m Ab) in non-Hodgkin's lymphoma: implications in chemosensitization and therapeutic intervention. Oncogene 2005, 24:2121-2143.
108. Jazirehi A.R., Huerta-Yepez S., Cheng G., Bonavida B. Rituximab (chimeric anti-CD20 monoclonal antibody) inhibits the constitutive nuclear factor-{kappa}B signaling pathway in non-Hodgkin's lymphoma B-cell lines: role in sensitization to chemotherapeutic drug-induced apoptosis. Cancer Res. 2005, 65:264-276.
109. Vega M.I., Huerta-Yepez S., Jazirehi A.R., Garban H., Bonavida B. Rituximab (chimeric anti-CD20) sensitizes B-NHL cell lines to Fas-induced apoptosis. Oncogene 2005, 24:8114-8127.
110. Shami P.J., Saavedra J.E., Wang L.Y., Bonifant C.L., Diwan B.A., Singh S.V., Gu Y., Fox S.D., Buzard G.S., Citro M.L., Waterhouse D.J., Davies K.M., Ji X., Keefer L.K. JS-K, a glutathione/glutathione S-transferase-activated nitric oxide donor of the diazeniumdiolate class with potent antineoplastic activity. Mol. Cancer Ther. 2003, 2:409-417.
111. Weyerbrock A., Osterberg N., Psarras N., Baumer B., Kogias E., Werres A., Bette S., Saavedra J.E., Keefer L.K., Papazoglou A. JS-K, a glutathione S-transferase-activated nitric oxide donor with antineoplastic activity in malignant gliomas. Neurosurgery 2012, 70:497-510. discussion 510.
112. Huerta S., Gao X., Bonavida B. DETANONOate is a potent chemo\radio-sensitizing agent in colon and colorectal cancers as assessed in in vitro and in vivo established tumor xenografts. Forum Immunopathol. Dis. Ther. 2010, 1:281-295.
113. 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: implications in breast cancer. Cancer Res. 2001, 61:4701-4706.
114. Azizzadeh B., Yip H.T., Blackwell K.E., Horvath S., Calcaterra T.C., Buga G.M., Ignarro L.J., Wang M.B. Nitric oxide improves cisplatin cytotoxicity in head and neck squamous cell carcinoma. Laryngoscope 2001, 111:1896-1900.
115. McCarthy H.O., Coulter J.A., Robson T., Hirst D.G. Gene therapy via inducible nitric oxide synthase: a tool for the treatment of a diverse range of pathological conditions. J. Pharm. Pharmacol. 2008, 60:999-1017.
116. Laschak M., Spindler K.-D., Schrader A.J., Hessenauer A., Streicher W., Schrader M., Cronauer M.V. JS-K, a glutathione/glutathione S-transferase-activated nitric oxide releasing prodrug inhibits androgen receptor and WNT-signaling in prostate cancer cells. BMC Cancer 2012, 12.
117. Williams J.L., Borgo S., Hasan I., Castillo E., Traganos F., Rigas B. Nitric oxide-releasing nonsteroidal anti-inflammatory drugs (NSAIDs) alter the kinetics of human colon cancer cell lines more effectively than traditional NSAIDs: Implications for colon cancer chemoprevention. Cancer Res. 2001, 61:3285-3289.
118. Rigas B., Kashfi K. Nitric-oxide-donating NSAIDs as agents for cancer prevention. Trends Mol. Med. 2004, 10:324-330.
119. Kozoni V., Rosenberg T., Rigas B. Development of novel agents based on nitric oxide for the control of colon cancer. Acta Pharmacol. Sin. 2007, 28:1429-1433.
120. Xie K., Huang S., Dong Z., Juang S.H., Gutman M., Xie Q.W., Nathan C., Fidler I.J. Transfection with the inducible nitric oxide synthase gene suppresses tumorigenicity and abrogates metastasis by K-1735 murine melanoma cells. J. Exp. Med. 1995, 181:1333-1343.
121. Xie K., Fidler I.J. Therapy of cancer metastasis by activation of the inducible nitric oxide synthase. Cancer Metastasis Rev. 1998, 17:55-75.
122. Chung P., Cook T., Liu K.H., Vodovotz Y., Zamora R., Finkelstein S., Billiar T., Blumberg D. Overexpression of the human inducible nitric oxide synthase gene enhances radiation-induced apoptosis in colorectal cancer cells via a caspase-dependent mechanism. Nitric Oxide-Biol. Chem. 2003, 8:119-126.
123. 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. Targeting hepatoma using nitric oxide donor strategies. Antioxid. Redox Signal. 2013, 18:491-506.
124. De la Rosa A., Rodríguez-Hernández A., González R., Romero-Brufau S., Navarro-Villarán E., Barrera-Pulido L., Pereira S., Marín L.M., López-Bernal F., Álamo J.M., Gómez-Bravo M.A., Padillo F.J., Muntané J. Antitumoral gene-based strategy involving nitric oxide synthase type III overexpression in hepatocellular carcinoma. Gene Therapy 2015, [Epub ahead of print]. 10.1038/gt.2015.79.
125. Aranda E., Lopez-Pedrera C., De La Haba-Rodriguez J.R., Rodriguez-Ariza A. Nitric oxide and cancer: the emerging role of s-nitrosylation. Curr. Mol. Med. 2012, 12:50-67.
126. Burke A.J., Sullivan F.J., Giles F.J., Glynn S.A. The yin and yang of nitric oxide in cancer progression. Carcinogenesis 2013, 34:503-512.
127. 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.
128. Yasuda H., Yamaya M., Nakayama K., Sasaki T., Ebihara S., Kanda A., Asada M., Inoue D., Suzuki T., Okazaki T., Takahashi H., Yoshida M., Kaneta T., Ishizawa K., Yamanda S., Tomita N., Yamasaki M., Kikuchi A., Kubo H., Sasaki H. Randomized phase II trial comparing nitroglycerin plus vinorelbine and cisplatin with vinorelbine and cisplatin alone in previously untreated stage IIIB/IV non-small-cell lung cancer. J. Clin. Oncol. 2006, 24:688-694.
129. Siemens D.R., Heaton J.P.W., 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.
130. Siemens D.R., Heaton J., Adams M., Graham C. A phase I/II pilot trial of low-dose, sustained-release GTN for prostate cancer patients with recurrence after primary therapy. Nitric Oxide-Biol. Chem. 2007, 17. S15-S15.