Nitric oxide initiates progression of human melanoma via a feedback loop mediated by apurinic/apyrimidinic endonuclease-1/redox factor-1, which is inhibited by resveratrol

Molecular Cancer Therapeutics

Volumn 7, Issue 12, 2008, Pages 3751-3760

  Yang, Zhen ^a,b   Yang, Sun ^a   Misner, Bobbye J ^a   Chiu, Rita ^a   Liu, Feng ^a   Meyskens Jr , Frank L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SHANDONG PROVINCIAL HOSPITAL AFFILIATED TO SHANDONG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

APURINIC ACID; DEOXYRIBONUCLEASE I; DIETHYLENETRIAMINE; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERSTITIAL COLLAGENASE; NITRIC OXIDE; PROTEIN BCL 2; REDOX EFFECTOR FACTOR 1; RESVERATROL; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR JUND;

APYRIMIDINIC SITE; ARTICLE; CANCER GROWTH; CELL PROLIFERATION; CELL STIMULATION; CONTROLLED STUDY; ENZYME INHIBITION; FEEDBACK SYSTEM; HUMAN; HUMAN CELL; MELANOMA; METASTASIS; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; CELL LINE, TUMOR; CELL PROLIFERATION; DISEASE PROGRESSION; DNA-(APURINIC OR APYRIMIDINIC SITE) LYASE; FEEDBACK, BIOCHEMICAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MELANOMA; MODELS, BIOLOGICAL; NEOPLASM METASTASIS; NITRIC OXIDE; STILBENES; TRANSCRIPTION FACTOR AP-1;

EID: 57749108574     PISSN: 15357163     EISSN: None     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-08-0562     Document Type: Article

References (50)

1. Moncada S. Nitric oxide in the vasculature: physiology and pathophysiology. Ann N Y Acad Sci 1997;811:60-7.
2. Ignarro LJ, Cirino G, Casini A, Napoli C. Nitric oxide as a signaling molecule in the vascular system: an overview. J Cardiovasc Pharmacol 1999;34:879-86.
3. Murata J, Tada M, Iggo RD, Sawamura Y, Shinohe Y, Abe H. Nitric oxide as a carcinogen: analysis by yeast functional assay of inactivating p53 mutations induced by nitric oxide. Mutat Res 1997;379:211-8.
4. Lala PK, Chakraborty C. Role of nitric oxide in carcinogenesis and tumor progression. Lancet Oncol 2001;2:149-56.
5. Grimm EA, Ellerhorst J, Tang CH, Ekmekcioglu S. Constitutive intracellular production of iNOS and NO in human melanoma: possible role in regulation of growth and resistance to apoptosis. Nitric Oxide 2008;19:133-7.
6. Green A, Siskind V, Bain C, Alexander J. Sunburn and malignant melanoma. Br J Cancer 1985;51:393-7.
7. Didier C, Emonet-Piccardi N, Béani JC, Cadet J, Richard MJ. L-arginine increases UVA cytotoxicity in irradiated human keratinocyte cell line: potential role of nitric oxide. FASEB J 1999;13:1817-24.
8. Deliconstantinos G, Villiotou V, Stavrides J. Increase of particulate nitric oxide synthase activity and peroxynitrite synthesis in UVB-irradiated keratinocyte membranes. Biochem J 1996;320:997-1003.
9. Aitken GR, Henderson JR, Chang SC, McNeil CJ, Birch-Machin MA. Direct monitoringo f UV-induced free radical generation in HaCaT keratinocytes. Clin Exp Dermatol 2007;32:722-7.
10. Gordon PR, Mansur CP, Gilchrest BA. Regulation of human melanocyte growth, dendricity, and melanization by keratinocyte derived factors. J Invest Dermatol 1989;92:565-72.
11. Archaubault M, Yaar M, Gilchrest BA. Keratinocytes and fibroblasts in human skin equivalent model enhance melanocyte survival and melanin synthesis after ultraviolet irradiation. J Invest Dermatol 1995;104:859-67.
12. Kippenberger S, Bernd A, Bereiter-Hahn J, Ramirez-Bosca A, Kaufmann R. The mechanism of melanocyte dendrite formation: the impact of differentiatingkeratinocytes. Pigment Cell Res 1998;11:34-7.
13. Xanthoudakis S, Curran T. Identification and characterization of APE/Ref-1, a nuclear protein that facilitates AP-1 DNA-binding activity. EMBO J 1992;11:653-65.
14. Mitomo K, Nakayama K, Fujimoto K, Sun X, Seki X, Yamamoto K. Two different cellular redox systems regulate the DNA-binding activity of the p50 subunit of NF-κB in vitro. Gene 1994;145:197-203.
15. Tell G, Zecca A, Pellizzari L, et al. An "environment to nucleus" signaling system operates in B lymphocytes: redox status modulates BSAP/Pax-5 activation through Ref-1 nuclear translocation. Nucleic Acids Res 2000;28:1099-105.
16. Tell G, Pellizzari L, Cimarosti D, Pucillo C, Damante G. APE/Ref-1 controls Pax-8 DNA-binding activity. Biochem Biophys Res Commun 1998;252:178-83.
17. Xanthoudakis S, Smeyne RJ, Wallace JD, Curran T. The redox/DNA repair protein, Ref-1, is essential for early embryonic development in mice. Proc Natl Acad Sci U S A 1996;93:8919-23.
18. Walker LJ, Craig RB, Harris AL, Hickson ID. A role for the human DNA repair enzyme HAP1 in cellular protection against DNA damaging agents and hypoxic stress. Nucleic Acids Res 1994;22:4884-9.
19. Valko M, Rhodes CJ, Moncol J, Izakovic M, Mazur M. Free radicals, metals, and antioxidants in oxidative stress-induced cancer. Chem Biol Interact 2006;160:1-40.
20. Meyskens FL, Jr., McNulty SE, Buckmeier JA, et al. Aberrant redox regulation in human metastatic melanoma cells compared to normal melanocytes. Free Radic Biol Med 2001;31:799-808.
21. Yang S, Misner BJ, Chiu RJ, Meyskens FL, Jr. Redox effector factor-1, combined with reactive oxygen species, plays an important role in the transformation of JB6 cells. Carcinogenesis 2007;28:2382-90.
22. Signorelli P, Ghidoni R. Resveratrol as an anticancer nutrient: molecular basis, open questions, and promises. J Nutr Biochem 2005;16:449-66.
23. de la Lastra CA, Villegas I. Resveratrol as an antioxidant and prooxidant agent: mechanisms and clinical implications. Biochem Soc Trans 2007;35:1156-60.
24. Yang S, Irani K, Heffron SE, Jurnak F, Meyskens FL, Jr. Alterations in the expression of the apurinic/apyrimidinic endonuclease-1/redox factor-1 (APE/Ref-1) in human melanoma and identification of the therapeutic potential of resveratrol as an APE/Ref-1 inhibitor. Mol Cancer Ther 2005;4:1923-35.
25. Evans AR, Limp-Foster M, Kelley MR. Going APE over Ref-1. Mutat Res 2001;461:83-108.
26. Weitzman JB, Fiette L, Matsuo K, Yaniv M. JunD protects cells from p53-dependent senescence and apoptosis. Mol Cell 2000;6:1109-19.
27. Weiss C, Faust D, Schreck I, et al. TCDD deregulates contact inhibition in rat liver oval cells via Ah receptor, JunD and cyclin A. Oncogene 2008;27:2198-207.
28. Pilz RB, Suhasini M, Idriss S, Meinkoth JL, Boss GR. Nitric oxide and cGMP analogs activate transcription from AP-1-responsive promoters in mammalian cells. FASEB J 1995;9:552-8.
29. Morris BJ. Stimulation of immediate early gene expression in striatal neurons by nitric oxide. J Biol Chem 1995;270:24740-4.
30. Pokharel YR, Liu QH, Woo ER, Kang KW. 4-Hydroxykobusin inhibits the induction of nitric oxide synthase by inhibiting NF-κB and AP-1 activation. Biol Pharm Bull 2007;30:1097-101.
31. Sheu BC, Lien HC, Ho HN, et al. Increased expression and activation of gelatinolytic matrix metalloproteinases is associated with the progression and recurrence of human cervical cancer. Cancer Res 2003;63:6537-42.
32. Fang W, Li H, Kong L, et al. Role of matrix metalloproteinases (MMPs) in tumor invasion and metastasis: serial studies on MMPs and TIMPs. Beijing Da Xue Xue Bao 2003;35:441-3.
33. Nikkola J, Vihinen P, Vlaykova T, Hahka-Kemppinen M, Kähäri VM, Pyrhönen S. High expression levels of collagenase-1 and stromelysin-1 correlate with shorter disease-free survival in human metastatic melanoma. Int J Cancer 2002;97:432-8.
34. Westermarck J, Seth A, Kahari VM. Differential regulation of interstitial collagenase (MMP-1) gene expression by ETS transcription factors. Oncogene 1997;14:2651-60.
35. Ishii Y, Ogura T, Tatemichi M, Fujisawa H, Otsuka F, Esumi H. Induction of matrix metalloproteinase gene transcription by nitric oxide and mechanisms of MMP-1 gene induction in human melanoma cell lines. Int J Cancer 2003;103:161-8.
36. Genaro AM, Hortelano S, Alvarez A, Martinez C, Bosca L. Splenic B lymphocyte programmed cell death is prevented by nitric oxide release through mechanisms involving sustained Bcl-2 levels. J Clin Invest 1995;95:1884-90.
37. Suschek CV, Krischel V, Bruch-Gerharz D, et al. Nitric oxide fully protects against UVA-induced apoptosis in tight correlation with Bcl-2 upregulation. J Biol Chem 1999;274:6130-7.
38. Guan ZJ, Basi D, Li QL, et al. Loss of redox factor 1 decreases NF-κB activity and increases susceptibility of endothelial cells to apoptosis. Arterioscler Thromb Vasc Biol 2005;25:96-101.
39. Thomsen LL, Lawton FG, Knowles RG, Beesley JE, Riveros-Moreno V, Moncada S. Nitric oxide synthase activity in human gynecological cancer. Cancer Res 1994;54:1352-4.
40. Cobbs CS, Brenman JE, Aldape KD, Bredt DS, Israel MA. Expression of nitric oxide synthase in human central nervous system tumors. Cancer Res 1995;55:727-30.
41. Ekmekcioglu S, Ellerhorst J, Smid CM, et al. Inducible nitric oxide synthase and nitrotyrosine in human metastatic melanoma tumors correlate with poor survival. Clin Cancer Res 2000;6:4768-75.
42. Ahmed B, Van Den Oord JJ. Expression of the inducible isoform of nitric oxide synthase in pigment cell lesions of the skin. Br J Dermatol 2000;142:432-40.
43. Massi D, Franchi A, Sardi I, et al. Inducible nitric oxide synthase expression in benign and malignant cutaneous melanocytic lesions. J Pathol 2001;194:194-200.
44. Xie K, Huang S, Dong Z, et al. Transfection with the inducible nitric oxide synthase gene suppresses tumorigenicity and abrogates metastasis by K-1735 murine melanoma cells. J Exp Med 1995;181:1333-43.
45. Cho MK, Suh SH, Kim SG. JunB/AP-1 and NF-κB-mediated induction of nitric oxide synthase by bovine type I collagen in serum-stimulated murine macrophages. Nitric Oxide 2002;6:319-32.
46. Oh JW, Lee JY, Han SH, et al. Effects of phenylethanoid glycosides from Digitalis purpurea L. on the expression of inducible nitric oxide synthase. J Pharm Pharmacol 2005;57:903-10.
47. Chyu KY, Dimayuga PC, Zhao X, Nilsson J, Shah PK, Cercek B. Altered AP-1/APE/Ref-1 redox pathway and reduced proliferative response in iNOS-deficient vascular smooth muscle cells. Vasc Med 2004;9:177-83.
48. Athar M, Back JH, Tang X, et al. Resveratrol: a review of preclinical studies for human cancer prevention. Toxicol Appl Pharmacol 2007;224:274-83.
49. Bråkenhielm E, Cao R, Cao Y. Suppression of angiogenesis, tumor growth, and wound healing by resveratrol, a natural compound in red wine and grapes. FASEB J 2001;15:1798-800.
50. Gusman J, Malonne H, Atassi G. A reappraisal of the potential chemopreventive and chemotherapeutic properties of resveratrol. Carcinogenesis 2001;22:1111-7.