The yin and yang of nitric oxide in cancer progression

Carcinogenesis

Volumn 34, Issue 3, 2013, Pages 503-512

  Burke, Amy J ^a   Sullivan, Francis J ^a,b   Giles, Francis J ^a   Glynn, Sharon A ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^b UNIVERSITY HOSPITAL GALWAY   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

CELECOXIB; CHEMOKINE RECEPTOR CXCR4 ANTAGONIST; GLYCERYL TRINITRATE; GT 094; INDUCIBLE NITRIC OXIDE SYNTHASE; NITRIC OXIDE; NITRIC OXIDE DONOR; NITRIC OXIDE SYNTHASE INHIBITOR; NONSTEROID ANTIINFLAMMATORY AGENT; UNCLASSIFIED DRUG;

ADENOID CYSTIC CARCINOMA; APOPTOSIS; CANCER GROWTH; CANCER INVASION; CANCER RADIOTHERAPY; CARCINOGENESIS; CELL MIGRATION; CELL PROLIFERATION; EPIGENETICS; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; TUMOR MICROENVIRONMENT;

ANIMALS; APOPTOSIS; CELL PROLIFERATION; DISEASE PROGRESSION; EPIGENESIS, GENETIC; EPITHELIAL-MESENCHYMAL TRANSITION; HUMANS; MOLECULAR TARGETED THERAPY; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; RADIATION TOLERANCE;

EID: 84874779118     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgt034     Document Type: Review

References (152)

1. Ignarro, L.J. (2002) Nitric oxide as a unique signaling molecule in the vascular system: a historical overview. J. Physiol. Pharmacol., 53, 503-514.
2. Gladwin, M.T. et al. (2003) Nitric oxide's reactions with hemoglobin: a view through the SNO-storm. Nat. Med., 9, 496-500.
3. Mocellin, S. et al. (2007) Nitric oxide, a double edged sword in cancer biology: searching for therapeutic opportunities. Med. Res. Rev., 27, 317-352.
4. Muntané, J. et al. (2010) Nitric oxide and cancer. World J. Hepatol., 2, 337-344.
5. Aranda, E. et al. (2012) Nitric oxide and cancer: the emerging role of S-nitrosylation. Curr. Mol. Med., 12, 50-67.
6. Knowles, R.G. et al. (1994) Nitric oxide synthases in mammals. Biochem. J., 298 (Pt 2), 249-258.
7. Alderton, W.K. et al. (2001) Nitric oxide synthases: structure, function and inhibition. Biochem. J., 357(Pt 3), 593-615.
8. Förstermann, U. et al. (2012) Nitric oxide synthases: regulation and function. Eur. Heart J., 33, 829-37, 837a.
9. Noble, M.A. et al. (1999) Potentiometric analysis of the flavin cofactors of neuronal nitric oxide synthase. Biochemistry, 38, 16413-16418.
10. Stuehr, D. et al. (2001) Oxygen reduction by nitric-oxide synthases. J. Biol. Chem., 276, 14533-14536.
11. Singh, S. et al. (2011) Nitric oxide: role in tumour biology and iNOS/ NO-based anticancer therapies. Cancer Chemother. Pharmacol., 67, 1211-1224.
12. Michel, T. et al. (1997) Nitric oxide synthases: which, where, how, and why? J. Clin. Invest., 100, 2146-2152.
13. Nathan, C. et al. (1994) Nitric oxide synthases: roles, tolls, and controls. Cell, 78, 915-918.
14. Feng, C. (2012) Mechanism of nitric oxide synthase regulation: electron transfer and interdomain interactions. Coord. Chem. Rev., 256, 393-411.
15. Ignarro, L.J. (2000) Nitric Oxide: Biology and Pathobiology. Academic Press.
16. Hirst, D.G. et al. (2011) Nitric oxide physiology and pathology. Methods Mol. Biol., 704, 1-13.
17. Shi, H.P. et al. (2000) Supplemental dietary arginine enhances wound healing in normal but not inducible nitric oxide synthase knockout mice. Surgery, 128, 374-378.
18. Garthwaite, J. et al. (1989) NMDA receptor activation induces nitric oxide synthesis from arginine in rat brain slices. Eur. J. Pharmacol., 172, 413-416.
19. Bult, H. et al. (1990) Nitric oxide as an inhibitory non-adrenergic non-cholinergic neurotransmitter. Nature, 345, 346-347.
20. Rolle, U. et al. (2002) Nitrergic innervation of the normal gut and in motility disorders of childhood. J. Pediatr. Surg., 37, 551-567.
21. Tayfun Uzbay, I. et al. (2001) Nitric oxide and substance dependence. Neurosci. Biobehav. Rev., 25, 43-52.
22. Kundu, J.K. et al. (2012) Emerging avenues linking inflammation and cancer. Free Radic. Biol. Med., 52, 2013-2037.
23. Fukumura, D. et al. (2006) The role of nitric oxide in tumour progression. Nat. Rev. Cancer, 6, 521-534.
24. Ridnour, L.A. et al. (2006) The biphasic nature of nitric oxide responses in tumor biology. Antioxid. Redox Signal., 8, 1329-1337.
25. Villalobo, A. (2007) Enhanced cell proliferation induced by nitric oxide. Dyn Cell Biol, 1, 60-64.
26. Ridnour, L.A. et al. (2008) Molecular mechanisms for discrete nitric oxide levels in cancer. Nitric Oxide, 19, 73-76.
27. Jarry, A. et al. (2004) Position in cell cycle controls the sensitivity of colon cancer cells to nitric oxide-dependent programmed cell death. Cancer Res., 64, 4227-4234.
28. Okayama, H. et al. (2013) NOS2 enhances KRAS-induced lung carcinogenesis, inflammation and microRNA-21 expression. Int. J. Cancer, 132, 9-18.
29. Ambs, S. et al. (1998) Vascular endothelial growth factor and nitric oxide synthase expression in human lung cancer and the relation to p53. Br. J. Cancer, 78, 233-239.
30. Ambs, S. et al. (1999) Relationship between p53 mutations and inducible nitric oxide synthase expression in human colorectal cancer. J. Natl. Cancer Inst., 91, 86-88.
31. Ambs, S. et al. (1998) Frequent nitric oxide synthase-2 expression in human colon adenomas: implication for tumor angiogenesis and colon cancer progression. Cancer Res., 58, 334-341.
32. Glynn, S.A. et al. (2010) Increased NOS2 predicts poor survival in estrogen receptor-negative breast cancer patients. J. Clin. Invest., 120, 3843-3854.
33. Thomsen, L.L. et al. (1995) Nitric oxide synthase activity in human breast cancer. Br. J. Cancer, 72, 41-44.
34. Bulut, A.S. et al. (2005) Significance of inducible nitric oxide synthase expression in benign and malignant breast epithelium: an immunohistochemical study of 151 cases. Virchows Arch., 447, 24-30.
35. Grimm, E.A. et al. (2008) Constitutive intracellular production of iNOS and NO in human melanoma: possible role in regulation of growth and resistance to apoptosis. Nitric Oxide, 19, 133-137.
36. Xiong, Q. et al. (2001) Regulation of interleukin-8 expression by nitric oxide in human pancreatic adenocarcinoma. J. Interferon Cytokine Res., 21, 529-537.
37. Hussain, S.P. et al. (2008) Nitric oxide is a key component in inflammationaccelerated tumorigenesis. Cancer Res., 68, 7130-7136.
38. Ying, L. et al. (2007) An emerging role for endothelial nitric oxide synthase in chronic inflammation and cancer. Cancer Res., 67, 1407-1410.
39. Tam, N.N. et al. (2007) Sex hormones induce direct epithelial and inflammation-mediated oxidative/nitrosative stress that favors prostatic carcinogenesis in the noble rat. Am. J. Pathol., 171, 1334-1341.
40. Ambs, S. et al. (2011) Candidate pathways linking inducible nitric oxide synthase to a basal-like transcription pattern and tumor progression in human breast cancer. Cell Cycle, 10, 619-624.
41. Switzer, C.H. et al. (2012) Ets-1 is a transcriptional mediator of oncogenic nitric oxide signaling in estrogen receptor-negative breast cancer. Breast Cancer Res., 14, R125.
42. Sohn, J.J. et al. (2012) Macrophages, nitric oxide and microRNAs are associated with DNA damage response pathway and senescence in inflammatory bowel disease. PLoS ONE, 7, e44156.
43. Krischel, V. et al. (1998) Biphasic effect of exogenous nitric oxide on proliferation and differentiation in skin derived keratinocytes but not fibroblasts. J. Invest. Dermatol., 111, 286-291.
44. Lai, Y. et al. (2010) Synthesis and biological evaluation of furoxan-based nitric oxide-releasing derivatives of glycyrrhetinic acid as anti-hepatocellular carcinoma agents. Bioorg. Med. Chem. Lett., 20, 6416-6420.
45. Kumar, S. et al. (2010) Cdk2 nitrosylation and loss of mitochondrial potential mediate NO-dependent biphasic effect on HL-60 cell cycle. Free Radic. Biol. Med., 48, 851-861.
46. Bal-Price, A. et al. (2006) Nitric oxide stimulates PC12 cell proliferation via cGMP and inhibits at higher concentrations mainly via energy depletion. Nitric Oxide, 14, 238-246.
47. Sang, J. et al. (2011) Nitric oxide inhibits gastric cancer cell growth through the modulation of the Akt pathway. Mol. Med. Report., 4, 1163-1167.
48. Heller, R. et al. (1999) Nitric oxide inhibits proliferation of human endothelial cells via a mechanism independent of cGMP. Atherosclerosis, 144, 49-57.
49. Pervin, S. et al. (2001) 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., 98, 3583-3588.
50. Peña-Altamira, E. et al. (2010) Nitric oxide control of proliferation in nerve cells and in tumor cells of nervous origin. Curr. Pharm. Des., 16, 440-450.
51. Huguenin, S. et al. (2004) Nitrosulindac (NCX 1102): a new nitric oxidedonating non-steroidal anti-inflammatory drug (NO-NSAID), inhibits proliferation and induces apoptosis in human prostatic epithelial cell lines. Prostate, 61, 132-141.
52. Huguenin, S. et al. (2004) Antiproliferative effect of nitrosulindac (NCX 1102), a new nitric oxide-donating non-steroidal anti-inflammatory drug, on human bladder carcinoma cell lines. Mol. Cancer Ther., 3, 291-298.
53. Donia, M. et al. (2009) The novel NO-donating compound GIT-27NO inhibits in vivo growth of human prostate cancer cells and prevents murine immunoinflammatory hepatitis. Eur. J. Pharmacol., 615, 228-233.
54. Donia, M. et al. (2011) In vitro and in vivo anticancer action of Saquinavir-NO, a novel nitric oxide-derivative of the protease inhibitor saquinavir, on hormone resistant prostate cancer cells. Cell Cycle, 10, 492-499.
55. Wouwer, M.V. et al. (2012) Activation of the BRCA1/Chk1/p53/p21(Cip1/ Waf1) pathway by nitric oxide and cell cycle arrest in human neuroblastoma NB69 cells. Nitric Oxide, 26, 182-191.
56. Pervin, S. et al. (2007) Nitric oxide in physiologic concentrations targets the translational machinery to increase the proliferation of human breast cancer cells: involvement of mammalian target of rapamycin/eIF4E pathway. Cancer Res., 67, 289-299.
57. Sanyal, M. et al. (2000) Localization of nitric oxide synthase in human trophoblast cells: role of nitric oxide in trophoblast proliferation and differentiation. Am. J. Reprod. Immunol., 43, 70-77.
58. Keith Bechtel, M. et al. (2001) Inhibitory effects of 17beta-estradiol and progesterone on ovarian carcinoma cell proliferation: a potential role for inducible nitric oxide synthase. Gynecol. Oncol., 82, 127-138.
59. Eyler, C.E. et al. (2011) Glioma stem cell proliferation and tumor growth are promoted by nitric oxide synthase-2. Cell, 146, 53-66.
60. Ziche, M. et al. (1997) Nitric oxide promotes proliferation and plasminogen activator production by coronary venular endothelium through endogenous bFGF. Circ. Res., 80, 845-852.
61. Zheng, J. et al. (2006) Exogenous nitric oxide stimulates cell proliferation via activation of a mitogen-activated protein kinase pathway in ovine fetoplacental artery endothelial cells. Biol. Reprod., 74, 375-382.
62. Wang, B. et al. (2003) A novel model system for studying the double-edged roles of nitric oxide production in pancreatic cancer growth and metastasis. Oncogene, 22, 1771-1782.
63. Thiery, J.P. et al. (2006) Complex networks orchestrate epithelial-mesenchymal transitions. Nat. Rev. Mol. Cell Biol., 7, 131-142.
64. Thiery, J.P. (2002) Epithelial-mesenchymal transitions in tumour progression. Nat. Rev. Cancer, 2, 442-454.
65. Edwards, P. et al. (1996) Tumor cell nitric oxide inhibits cell growth in vitro, but stimulates tumorigenesis and experimental lung metastasis in vivo. J. Surg. Res., 63, 49-52.
66. Shi, Q. et al. (2000) Influence of nitric oxide synthase II gene disruption on tumor growth and metastasis. Cancer Res., 60, 2579-2583.
67. Siegert, A. et al. (2002) Nitric oxide of human colorectal adenocarcinoma cell lines promotes tumour cell invasion. Br. J. Cancer, 86, 1310-1315.
68. Jadeski, L.C. et al. (2000) Nitric oxide promotes murine mammary tumour growth and metastasis by stimulating tumour cell migration, invasiveness and angiogenesis. Int. J. Cancer, 86, 30-39.
69. Ray, J.M. et al. (1994) The role of matrix metalloproteases and their inhibitors in tumour invasion, metastasis and angiogenesis. Eur. Respir. J., 7, 2062-2072.
70. Sun, M.H. et al. (2005) Expressions of inducible nitric oxide synthase and matrix metalloproteinase-9 and their effects on angiogenesis and progression of hepatocellular carcinoma. World J. Gastroenterol., 11, 5931-5937.
71. Babykutty, S. et al. (2012) Insidious role of nitric oxide in migration/invasion of colon cancer cells by upregulating MMP-2/9 via activation of cGMP-PKG-ERK signaling pathways. Clin. Exp. Metastasis, 29, 471-492.
72. Ishii, Y. et al. (2003) Induction of matrix metalloproteinase gene transcription by nitric oxide and mechanisms of MMP-1 gene induction in human melanoma cell lines. Int. J. Cancer, 103, 161-168.
73. Switzer, C.H. et al. (2012) S-nitrosylation of EGFR and Src activates an oncogenic signaling network in human basal-like breast cancer. Mol. Cancer Res., 10, 1203-1215.
74. Le, X. et al. (2005) Nitric oxide synthase II suppresses the growth and metastasis of human cancer regardless of its up-regulation of protumor factors. Proc. Natl Acad. Sci. USA, 102, 8758-8763.
75. Wei, D. et al. (2003) Direct demonstration of negative regulation of tumor growth and metastasis by host-inducible nitric oxide synthase. Cancer Res., 63, 3855-3859.
76. Vyas-Read, S. et al. (2007) Nitric oxide attenuates epithelial-mesenchymal transition in alveolar epithelial cells. Am. J. Physiol. Lung Cell Mol. Physiol., 293, L212-L221.
77. Baritaki, S. et al. (2010) 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, 9, 4931-4940.
78. Bonavida, B. et al. (2011) Dual role of NO donors in the reversal of tumor cell resistance and EMT: downregulation of the NF-κB/Snail/YY1/RKIP circuitry. Nitric Oxide, 24, 1-7.
79. Singh, T. et al. (2012) Nitric oxide donor exisulind is an effective inhibitor of murine photocarcinogenesis. Photochem. Photobiol., 88, 1141-1148.
80. Weiss, J.M. et al. (2010) Macrophage-dependent nitric oxide expression regulates tumor cell detachment and metastasis after IL-2/anti-CD40 immunotherapy. J. Exp. Med., 207, 2455-2467.
81. Jespersen, C. et al. (2009) Molecular mechanisms of nitric oxide-dependent inhibition of TPA-induced matrix metalloproteinase-9 (MMP-9) in MCF-7 cells. J. Cell. Physiol., 219, 276-287.
82. Akool, L.-S. et al. (2003) Nitric oxide increases the decay of matrix metalloproteinase 9 mRNA by inhibiting the expression of mRNA-stabilizing factor HuR. Mol. Cell. Biol., 23, 4901-4916.
83. Hickok, J.R. et al. (2011) Nitric oxide suppresses tumor cell migration through N-Myc downstream-regulated gene-1 (NDRG1) expression: role of chelatable iron. J. Biol. Chem., 286, 41413-41424.
84. Cooke, J.P. (2003) NO and angiogenesis. Atheroscler. Suppl., 4, 53-60.
85. Sessa, W.C. (2004) eNOS at a glance. J. Cell. Sci., 117, 2427-2429.
86. Ziche, M. et al. (1994) Nitric oxide mediates angiogenesis in vivo and endothelial cell growth and migration in vitro promoted by substance P. J. Clin. Invest., 94, 2036-2044.
87. Simon, B.C. et al. (1990) Oxidized low density lipoproteins cause contraction and inhibit endothelium-dependent relaxation in the pig coronary artery. J. Clin. Invest., 86, 75-79.
88. Babaei, S. et al. (1998) Role of nitric oxide in the angiogenic response in vitro to basic fibroblast growth factor. Circ. Res., 82, 1007-1015.
89. Ridnour, L.A. et al. (2005) Nitric oxide regulates angiogenesis through a functional switch involving thrombospondin-1. Proc. Natl Acad. Sci. USA, 102, 13147-13152.
90. Matsunaga, T. et al. (2002) Angiostatin inhibits coronary angiogenesis during impaired production of nitric oxide. Circulation, 105, 2185-2191.
91. Sikora, A.G. et al. (2010) Targeted inhibition of inducible nitric oxide synthase inhibits growth of human melanoma in vivo and synergizes with chemotherapy. Clin. Cancer Res., 16, 1834-1844.
92. Ng, Q.S. et al. (2007) Effect of nitric-oxide synthesis on tumour blood volume and vascular activity: a phase I study. Lancet Oncol., 8, 111-118.
93. Pipili-Synetos, E. et al. (1995) Inhibition of angiogenesis, tumour growth and metastasis by the NO-releasing vasodilators, isosorbide mononitrate and dinitrate. Br. J. Pharmacol., 116, 1829-1834.
94. Pipili-Synetos, E. et al. (1993) Nitric oxide is involved in the regulation of angiogenesis. Br. J. Pharmacol., 108, 855-857.
95. Jones, M.K. et al. (2004) Dual actions of nitric oxide on angiogenesis: possible roles of PKC, ERK, and AP-1. Biochem. Biophys. Res. Commun., 318, 520-528.
96. Pathi, S.S. et al. (2011) GT-094, a NO-NSAID, inhibits colon cancer cell growth by activation of a reactive oxygen species-microRNA-27a: ZBTB10-specificity protein pathway. Mol. Cancer Res., 9, 195-202.
97. Kiziltepe, T. et al. (2010) JS-K has potent anti-angiogenic activity in vitro and inhibits tumour angiogenesis in a multiple myeloma model in vivo. J. Pharm. Pharmacol., 62, 145-151.
98. Malaguarnera, L. (2004) Implications of apoptosis regulators in tumorigenesis. Cancer Metastasis Rev., 23, 367-387.
99. Tarr, J.M. et al. (2006) Nitric oxide and the regulation of apoptosis in tumour cells. Curr. Pharm. Des., 12, 4445-4468.
100. Brown, G.C. (1999) Nitric oxide and mitochondrial respiration. Biochim. Biophys. Acta, 1411, 351-369.
101. Marshall, H.E. et al. (2002) Nitrosative stress-induced apoptosis through inhibition of NF-kappa B. J. Biol. Chem., 277, 34223-34228.
102. Di, J.H. et al. (2012) nNOS downregulation attenuates neuronal apoptosis by inhibiting nNOS-GluR6 interaction and GluR6 nitrosylation in cerebral ischemic reperfusion. Biochem. Biophys. Res. Commun., 420, 594-599.
103. Kim, M.Y. (2012) Nitric oxide triggers apoptosis in A375 human melanoma cells treated with capsaicin and resveratrol. Mol. Med. Report., 5, 585-591.
104. Brüne, B. (2003) Nitric oxide: NO apoptosis or turning it ON? Cell Death Differ., 10, 864-869.
105. Kim, J.E. et al. (2004) S-Nitrosation regulates the activation of endogenous procaspase-9 in HT-29 human colon carcinoma cells. J. Biol. Chem., 279, 9758-9764.
106. Olson, S.Y. et al. (2008) Regulation of apoptosis-related genes by nitric oxide in cancer. Nitric Oxide, 19, 170-176.
107. Pan, X. et al. (2009) Nitric oxide suppresses transforming growth factor-beta1-induced epithelial-to-mesenchymal transition and apoptosis in mouse hepatocytes. Hepatology, 50, 1577-1587.
108. Zhao, H. et al. (1998) B-cell chronic lymphocytic leukemia cells express a functional inducible nitric oxide synthase displaying anti-apoptotic activity. Blood, 92, 1031-1043.
109. Suschek, C.V. et al. (1999) Nitric oxide fully protects against UVAinduced apoptosis in tight correlation with Bcl-2 up-regulation. J. Biol. Chem., 274, 6130-6137.
110. Kim, Y.M. et al. (1998) Nitric oxide suppression of apoptosis occurs in association with an inhibition of Bcl-2 cleavage and cytochrome c release. J. Biol. Chem., 273, 31437-31441.
111. Piplani, H. et al. (2012) Dolastatin 15, a mollusk linear peptide, and Celecoxib, a selective cyclooxygenase-2 inhibitor, prevent preneoplastic colonic lesions and induce apoptosis through inhibition of the regulatory transcription factor NF-κB and an inflammatory protein, iNOS. Eur. J. Cancer Prev., 21, 511-522.
112. Wang, K. et al. (2011) iNOS/NO signaling regulates apoptosis induced by glycochenodeoxycholate in hepatocytes. Cell. Signal., 23, 1677-1685.
113. Oronsky, B.T. et al. (2012) Is nitric oxide (NO) the last word in radiosensitization? A review. Transl. Oncol., 5, 66-71.
114. Su, X. et al. (2011) Nitric oxide radical-induced radioadaptation and radiosensitization are G2/M phase-dependent. J. Radiat. Res., 52, 609-615.
115. Su, X. et al. (2010) Biphasic effects of nitric oxide radicals on radiationinduced lethality and chromosome aberrations in human lung cancer cells carrying different p53 gene status. Int. J. Radiat. Oncol. Biol. Phys., 77, 559-565.
116. Liebmann, J. et al. (1994) In vivo radiation protection by nitric oxide modulation. Cancer Res., 54, 3365-3368.
117. Maxhimer, J.B. et al. (2009) Radioprotection in normal tissue and delayed tumor growth by blockade of CD47 signaling. Sci. Transl. Med., 1, 3ra7.
118. Saleem, W. et al. (2011) Reduction of nitric oxide level enhances the radiosensitivity of hypoxic non-small cell lung cancer. Cancer Sci., 102, 2150-2156.
119. Sonveaux, P. et al. (2003) Irradiation-induced angiogenesis through the up-regulation of the nitric oxide pathway: implications for tumor radiotherapy. Cancer Res., 63, 1012-1019.
120. Cardnell, R.J. et al. (2011) Nitric oxide synthase inhibition enhances the antitumor effect of radiation in the treatment of squamous carcinoma xenografts. PLoS ONE, 6, e20147.
121. Mitchell, J.B. et al. (1993) Hypoxic mammalian cell radiosensitization by nitric oxide. Cancer Res., 53, 5845-5848.
122. Singh, S. et al. (2009) The impact of intracellular generation of nitric oxide on the radiation response of human tumor cells. Radiat. Res., 171, 572-580.
123. Stewart, G.D. et al. (2011) DNA strand breaks and hypoxia response inhibition mediate the radiosensitisation effect of nitric oxide donors on prostate cancer under varying oxygen conditions. Biochem. Pharmacol., 81, 203-210.
124. Policastro, L. et al. (2007) Selective radiosensitization by nitric oxide in tumor cell lines. Cancer Lett., 248, 123-130.
125. Cook, T. et al. (2004) Nitric oxide and ionizing radiation synergistically promote apoptosis and growth inhibition of cancer by activating p53. Cancer Res., 64, 8015-8021.
126. De Ridder, M. et al. (2008) Hypoxic tumor cell radiosensitization through nitric oxide. Nitric Oxide, 19, 164-169.
127. Paradise, W.A. et al. (2010) Nitric oxide: perspectives and emerging studies of a well known cytotoxin. Int. J. Mol. Sci., 11, 2715-2745.
128. Illi, B. et al. (2009) NO sparks off chromatin: tales of a multifaceted epigenetic regulator. Pharmacol. Ther., 123, 344-352.
129. Arif, M. et al. (2010) Nitric oxide-mediated histone hyperacetylation in oral cancer: target for a water-soluble HAT inhibitor, CTK7A. Chem. Biol., 17, 903-913.
130. Vecellio, M. et al. (2012) In vitro epigenetic reprogramming of human cardiac mesenchymal stromal cells into functionally competent cardiovascular precursors. PLoS ONE, 7, e51694.
131. Sha, Y. et al. (2012) S-nitrosylation in the regulation of gene transcription. Biochim. Biophys. Acta, 1820, 701-711.
132. Yakovlev, V.A. et al. (2010) Nitration of the tumor suppressor protein p53 at tyrosine 327 promotes p53 oligomerization and activation. Biochemistry, 49, 5331-5339.
133. Cobbs, C.S. et al. (2003) Inactivation of wild-type p53 protein function by reactive oxygen and nitrogen species in malignant glioma cells. Cancer Res., 63, 8670-8673.
134. Re, A. et al. (2011) Silencing of GSTP1, a prostate cancer prognostic gene, by the estrogen receptor-β and endothelial nitric oxide synthase complex. Mol. Endocrinol., 25, 2003-2016.
135. Li, Q. et al. (2012) Nitric oxide modifies chromatin to suppress ICAM-1 expression during colonic inflammation. Am. J. Physiol. Gastrointest. Liver Physiol., 303, G103-G110.
136. Kjaer-Frifeldt, S. et al. (2012) The prognostic importance of miR-21 in stage II colon cancer: a population-based study. Br. J. Cancer, 107, 1169-1174.
137. Okayama, H. et al. (2012) MicroRNAs and inflammation in the pathogenesis and progression of colon cancer. Dig. Dis., 30 (suppl. 2), 9-15.
138. Siemens, D.R. et al. (2009) Phase II study of nitric oxide donor for men with increasing prostate-specific antigen level after surgery or radiotherapy for prostate cancer. Urology, 74, 878-883.
139. Laschak, M. et al. (2012) JS-K, a glutathione/glutathione S-transferaseactivated nitric oxide releasing prodrug inhibits androgen receptor and WNT-signaling in prostate cancer cells. BMC Cancer, 12, 130.
140. Kozoni, V. et al. (2007) Development of novel agents based on nitric oxide for the control of colon cancer. Acta Pharmacol. Sin., 28, 1429-1433.
141. Rigas, B. et al. (2004) Nitric-oxide-donating NSAIDs as agents for cancer prevention. Trends Mol. Med., 10, 324-330.
142. Williams, J.L. et al. (2001) 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., 61, 3285-3289.
143. Rao, C.V. et al. (2006) 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.
144. Rigas, B. (2007) Novel agents for cancer prevention based on nitric oxide. Biochem. Soc. Trans., 35(Pt 5), 1364-1368.
145. Lampson, B.L. et al. (2012) Targeting eNOS in pancreatic cancer. Cancer Res., 72, 4472-4482.
146. Takaoka, K., et al. (2011) Effect of NOS inhibitors and CXCR4 antagonist on tumor growth and metastasis of human adenoid cystic carcinoma xenografted into nude mice. Int. J. Oral Maxillofac. Surg., 40, 1.
147. Okada, F. et al. (2006) Involvement of reactive nitrogen oxides for acquisition of metastatic properties of benign tumors in a model of inflammationbased tumor progression. Nitric Oxide, 14, 122-129.
148. Capuano, G. et al. (2009) Modulators of arginine metabolism support cancer immunosurveillance. BMC Immunol., 10, 1.
149. Flitney, F.W. et al. (2011) Antitumor actions of ruthenium(III)-based nitric oxide scavengers and nitric oxide synthase inhibitors. Mol. Cancer Ther., 10, 1571-1580.
150. Coulter, J.A. et al. (2010) Transcriptional regulation of inducible nitric oxide synthase gene therapy: targeting early stage and advanced prostate cancer. J. Gene Med., 12, 755-765.
151. McCarthy, H.O. et al. (2011) Evaluation of a multi-functional nanocarrier for targeted breast cancer iNOS gene therapy. Int. J. Pharm., 405, 196-202.
152. Hickok, J.R. et al. (2010) Nitric oxide and cancer therapy: the emperor has NO clothes. Curr. Pharm. Des., 16, 381-391.