Nitric oxide and cancer

Nitric Oxide와 종양

Yim, Chang-Yeol
임창열

  • Published : 20100400

Abstract

Nitric oxide (NO) is emerging as a potential anti-cancer agent to overcome tumor cell resistance to conventional therapeutic agents. NO is a short-life molecule produced from L-arginine by the nitric oxide synthase (NOS). There are three isoforms of the enzyme: neuronal NOS (nNOS or NOS1), inducible NOS (iNOS or NOS2), and endothelial NOS (eNOS or NOS3). Each of these isoforms may be expressed in a variety of cell types. The actions of NO are highly variable in oncology revealing both sides of the spectrum as an anti-neoplastic versus a pro-neoplastic agent. The final activity of NO is dependent on its working microenvironment, including the type of cell exposed to NO, the redox state of the reaction, as well as the final intracellular concentration and the duration of exposure to NO. NO donors mimic continuous production of NO in a wide range of time intervals (seconds to days). Thus, multiple biological and (pro- versus anti-) neoplastic responses are elicited from NO donors depending on the half-life and the type of cell exposed to the compound. This paper is a review of the current knowledge of various roles of NO in cancer.

Keywords

References

  1. SoRelle R. Nobel Prize awarded to scientists for nitric oxide discoveries. Circulation 98:2365-2366, 1998
  2. Moncada S, Higgs A. The L-arginine-nitric oxide pathway. N Engl J Med 329:2002-2012, 1993
  3. Kroncke KD, Fehsel K, Kolb-Bachofen V. Nitric oxide: cytotoxicity versus cytoprotection - how, why, when and where? Nitric Oxide 1:107-120, 1997 https://doi.org/10.1006/niox.1997.0118
  4. Lala PK, Chakraborty C. Role of nitric oxide in carcinogenesis and tumour progression. Lancet Oncol 2:149-156, 2001 https://doi.org/10.1016/S1470-2045(00)00256-4
  5. Bredt DS, Snyder SH. Isolation of nitric oxide synthetase, a calmodulin- requiring enzyme. Proc Natl Acad Sci USA 87:682-685, 1990 https://doi.org/10.1073/pnas.87.2.682
  6. Bredt DS, Snyder SH. Nitric oxide, a novel neuronal messenger. Neuron 8:3-11, 1992 https://doi.org/10.1016/0896-6273(92)90104-L
  7. Stamler JS, Meissner G. Physiology of nitric oxide in skeletal muscle. Physiol Rev 81:209-237, 2001
  8. Wang Y, Newton DC, Marsden PA. Neuronal NOS: gene structure, mRNA diversity and functional relevance. Crit Rev Neurobiol 13:21-43, 1999
  9. Janssens SP, Shimouchi A, Quertermous T, Bloch DB, Bloch KD. Cloning and expression of a cDNA encoding human endothelium- derived relaxing factor/nitric oxide synthase. J Biol Chem 267:14519-14522, 1992
  10. Lechner M, Lirk P, Rieder J. Inducible nitric oxide synthase (iNOS) in tumor biology: the two sides of the same coin. Semin Cancer Biol 15:277-289, 2005 https://doi.org/10.1016/j.semcancer.2005.04.004
  11. MacMicking J, Xie QW, Nathan C. Nitric oxide and macrophage function. Annu Rev Immunol 15:323-350, 1997 https://doi.org/10.1146/annurev.immunol.15.1.323
  12. Kroncke KD, Fehsel K, Kolb-Bachofen V. Inducible nitric oxide synthase in human diseases. Clin Exp Immunol 113:147-156, 1998 https://doi.org/10.1046/j.1365-2249.1998.00648.x
  13. Nathan C. Inducible nitric oxide synthase: what difference does it make? J Clin Invest 100:2417-2423, 1997 https://doi.org/10.1172/JCI119782
  14. Brennan PA, Downie IP, Langdon JD, Zaki GA. Emerging role of nitric oxide in cancer. Br J Oral Maxillofac Surg 37:370-373, 1999 https://doi.org/10.1054/bjom.1999.0201
  15. Chang K, Lee SJ, Cheong I, Billiar TR, Chung HT, Han JA, Kwon YG, Ha KS, Kim YM. Nitric oxide suppresses inducible nitric oxide synthase expression by inhibiting posttranslational modification of IkappaB. Exp Mol Med 36:311-324, 2004
  16. Blaise GA, Gauvin D, Gangal M, Authier S. Nitric oxide, cell signaling and cell death. Toxicology 208:177-192, 2005 https://doi.org/10.1016/j.tox.2004.11.032
  17. Laurent M, Lepoivre M, Tenu JP. Kinetic modelling of the nitric oxide gradient generated in vitro by adherent cells expressing inducible nitric oxide synthase. Biochem J 3141:109-113, 1996
  18. Jenkins DC, Charles IG, Thomsen LL, Moss DW, Holmes LS, Baylis SA, Rhodes P, Westmore K, Emson PC, Moncada S. Roles of nitric oxide in tumor growth. Proc Natl Acad Sci USA 92: 4392-4396, 1995 https://doi.org/10.1073/pnas.92.10.4392
  19. Xie K, Huang S. Contribution of nitric oxide-mediated apoptosis to cancer metastasis inefficiency. Free Radic Biol Med 34: 969-986, 2003 https://doi.org/10.1016/S0891-5849(02)01364-3
  20. Melino G, Bernassola F, Knight RA, Corasaniti MT, Nistico G, Finazzi-Agro A. S-nitrosylation regulates apoptosis. Nature 388: 432-433, 1997 https://doi.org/10.1038/41237
  21. Brune B. Nitric oxide. NO apoptosis or turning it ON? Cell Death Differ 10:864-869, 2003 https://doi.org/10.1038/sj.cdd.4401261
  22. Li J, Billiar TR, Talanian RV, Kim YM. Nitric oxide reversibly inhibits seven members of the caspase family via Snitrosylation. Biochem Biophys Res Commun 240:419-424, 1997 https://doi.org/10.1006/bbrc.1997.7672
  23. Zech B, Kohl R, von KA, Brune B. Nitric oxide donors inhibit formation of the Apaf-1/caspase-9 apoptosome and activation of caspases. Biochem J 371:1055-1064, 2003 https://doi.org/10.1042/BJ20021720
  24. Chazotte-Aubert L, Hainaut P, Ohshima H. Nitric oxide nitrates tyrosine residues of tumor-suppressor p53 protein in MCF-7 cells. Biochem Biophys Res Commun 267:609-613, 2000 https://doi.org/10.1006/bbrc.1999.2003
  25. Forrester K, Ambs S, Lupold SE, Kapust RB, Spillare EA, Weinberg WC, Felley-Bosco E, Wang XW, Geller DA, Tzeng E, Billiar TR, Harris CC. Nitric oxide-induced p53 accumulation and regulation of inducible nitric oxide synthase expression by wild-type p53. Proc Natl Acad Sci USA 93:2442-2447, 1996 https://doi.org/10.1073/pnas.93.6.2442
  26. Rao CV. Nitric oxide signaling in colon cancer chemoprevention. Mutat Res 555:107-119, 2004 https://doi.org/10.1016/j.mrfmmm.2004.05.022
  27. Von KA, Brune B. Cyclooxygenase-2: an essential regulator of NO-mediated apoptosis. FASEB J 11:887-895, 1997
  28. Kawasaki K, Smith RS Jr, Hsieh CM, Sun J, Chao J, Liao JK. Activation of the phosphatidylinositol 3-kinase/protein kinase Akt pathway mediates nitric oxide-induced endothelial cell migration and angiogenesis. Mol Cell Biol 23:5726-5737, 2003 https://doi.org/10.1128/MCB.23.16.5726-5737.2003
  29. Oliveira CJ, Schindler F, Ventura AM, Morais MS, Arai RJ, Debbas V, Stern A, Monteiro HP. Nitric oxide and cGMP activate the Ras-MAP kinase pathway-stimulating protein tyrosine phosphorylation in rabbit aortic endothelial cells. Free Radic Biol Med 35:381-396, 2003 https://doi.org/10.1016/S0891-5849(03)00311-3
  30. Zaragoza C, Soria E, Lopez E, Browning D, Balbin M, Lopez- Otin C, Lamas S. Activation of the mitogen activated protein kinase extracellular signal-regulated kinase 1 and 2 by the nitric oxide- cGMP-cGMP-dependent protein kinase axis regulates the expression of matrix metalloproteinase 13 in vascular endothelial cells. Mol Pharmacol 62:927-935, 2002 https://doi.org/10.1124/mol.62.4.927
  31. Beckman JS. The double-edged role of nitric oxide in brain function and superoxide- mediated injury. J Dev Physiol 15:53-59, 1991
  32. Salgo MG, Stone K, Squadrito GL, Battista JR, Pryor WA. Peroxynitrite causes DNA nicks in plasmid pBR322. Biochem Biophys Res Commun 210:1025-1030, 1995 https://doi.org/10.1006/bbrc.1995.1759
  33. Nguyen T, Brunson D, Crespi CL, Penman BW, Wishnok JS, Tannenbaum SR. DNA damage and mutation in human cells exposed to nitric oxide in vitro. Proc Natl Acad Sci USA 89: 3030-3034, 1992 https://doi.org/10.1073/pnas.89.7.3030
  34. Wink DA, Kasprzak KS, Maragos C.M, Elespuru RK, Misra M, Dunams TM, Cebula TA, Koch WH, Andrews AW, Allen JS. DNA deaminating ability and genotoxicity of nitric oxide and its progenitors. Science 254:1001-1003, 1991 https://doi.org/10.1126/science.1948068
  35. Laval F, Wink DA. Inhibition by nitric oxide of the repair protein, O6-methylguanine- DNA-methyltransferase. Carcinogenesis 15: 443-447, 1994
  36. Laval F, Wink DA, Laval J. A discussion of mechanisms of NO genotoxicity: implication of inhibition of DNA repair proteins. Rev Physiol Biochem Pharmacol 131:175-191, 1997 https://doi.org/10.1007/3-540-61992-5_8
  37. Wink DA, Mitchell JB. Chemical biology of nitric oxide: insights into regulatory, cytotoxic and cytoprotective mechanisms of nitric oxide. Free Radic Biol Med 25:434-456, 1998 https://doi.org/10.1016/S0891-5849(98)00092-6
  38. Messmer UK, Ankarcrona M, Nicotera P, Brune B. p53 expression in nitric oxide-induced apoptosis. FEBS Lett 355:23-26, 1994 https://doi.org/10.1016/0014-5793(94)01161-3
  39. Messmer UK, Brune B. Nitric oxide-induced apoptosis. p53-dependent and p53-independent signalling pathways. Biochem J 319:299-305, 1996
  40. Glockzin S, von KA, Scheffner M, Brune B. Activation of the cell death program by nitric oxide involves inhibition of the proteasome. J Biol Chem 274:19581-19586, 1999 https://doi.org/10.1074/jbc.274.28.19581
  41. Li CQ, Robles AI, Hanigan CL, Hofseth LJ, Trudel LJ, Harris CC, Wogan GN. Apoptotic signaling pathways induced by nitric oxide in human lymphoblastoid cells expressing wild-type or mutant p53. Cancer Res 64:3022-3029, 2004 https://doi.org/10.1158/0008-5472.CAN-03-1880
  42. Boyd CS, Cadenas E. Nitric oxide and cell signaling pathways in mitochondrial- dependent apoptosis. Biol Chem 383:411-423, 2002 https://doi.org/10.1515/BC.2002.045
  43. Shimaoka M, Iida T, Ohara A, Taenaka N, Mashimo T, Honda T, Yoshiya I. NOC, a nitric-oxide-releasing compound, induces dose-dependent apoptosis in macrophages. Biochem Biophys Res Commun 209:519-526, 1995 https://doi.org/10.1006/bbrc.1995.1532
  44. Heller R, Polack T, Grabner R, Till U. Nitric oxide inhibits proliferation of human endothelial cells via a mechanism independent of cGMP. Atherosclerosis 144:49-57, 1999
  45. Lau YT, Ma WC. Nitric oxide inhibits migration of cultured endothelial cells. Biochem Biophys Res Commun 221:670-674, 1996 https://doi.org/10.1006/bbrc.1996.0654
  46. Pipili-Synetos E, Papageorgiou A, Sakkoula E, Sotiropoulou G, Fotsis T, Karakiulakis G, Maragoudakis ME. Inhibition of angiogenesis, tumour growth and metastasis by the NO-releasing vasodilators, isosorbide mononitrate and dinitrate. Br J Pharmacol 116:1829-1834, 1995
  47. Mortensen K, Christensen IJ, Nielsen HJ, Hansen U, Larsson LI. High expression of endothelial cell nitric oxide synthase in peritumoral microvessels predicts increased diseasefree survival in colorectal cancer. Cancer Lett 216:109-114, 2004 https://doi.org/10.1016/j.canlet.2004.05.025
  48. Olson SY, Garbán HJ. Regulation of apoptosis-related genes by nitric oxide in cancer. Nitric Oxide 19:170-176, 2008 https://doi.org/10.1016/j.niox.2008.04.005
  49. Hibbs JB Jr, Westenfelder C, Taintor R, Vavrin Z, Kablitz C, Baranowski RL, Ward JH, Menlove RL, McMurry MP, Kushner JP, Samlowski WE. Evidence for cytokine-inducible nitric oxide synthesis from L-arginine in patients receiving interleukin-2 therapy. J Clin Invest 89:867-877, 1992 https://doi.org/10.1172/JCI115666
  50. Jansson OT, Morcos E, Brundin L, Lundberg JO, Adolfsson J, S$\"{o}$derh$\"{a}$ll M, Wiklund NP. The role of nitric oxide in bacillus Calmette-Gu$\'{e}$rin mediated anti-tumour effects in human bladder cancer. Br J Cancer 78:588-592, 1998
  51. Becker Y. Success and failure of dendritic cell (DC) anticancer activity may be modulated by nitric oxide synthetase (NOS) gene expression: a hypothesis. In Vivo 7:285-288, 1993
  52. Song EK, Lee NR, Sohn MH, Kwak JY, Yim CY. Nitric oxide synthesis contributes to inhibition of graft-versus-tumor-effects against intraperitoneal Meth A tumor. Cell Immunol 230:109-118, 2004 https://doi.org/10.1016/j.cellimm.2004.10.002
  53. Yim CY, Lee CW, Choi SM, Park SS, Lee SJ, Kim JH, Song JS, Yoo WH, Kwak JY, Sohn MH. Effects of nitric oxide (NO) synthesis inhibition on antitumor responses during interleukin-2 (IL-2) treatment of mice. Korean J Intern Med 11:93-100, 1996
  54. Zhao J. Interplay among nitric oxide and reactive oxygen species: a complex network determining cell survival or death. Plant Signal Behav 2:544-547, 2007 https://doi.org/10.4161/psb.2.6.4802
  55. Munder M. Arginase: an emerging key player in the mammalian immune system. Br J Pharmacol 158:638-651, 2009 https://doi.org/10.1111/j.1476-5381.2009.00291.x