Cancer Letters
Volume 226, Issue 1 , Pages 1-15 , 8 August 2005

Nitric oxide as a modulator of apoptosis

Received 10 October 2004 ,Accepted 15 October 2004.

References 

  1. Alderton WK, Cooper CE, Knowles RG. Nitric oxide synthases: structure, function and inhibition. Biochem. J. 2001;357:593–615
  2. Patel RP, McAndrew J, Sellak H, White CR, Jo H, Freeman BA, et al. Biological aspects of reactive nitrogen species. Biochim. Biophys. Acta. 1999;1411:385–400
  3. Ohshima H, Tatemichi M, Sawa T. Chemical basis of inflammation-induced carcinogenesis. Arch. Biochem. Biophys. 2003;417:3–11
  4. Dedon PC, Tannenbaum SR. Reactive nitrogen species in the chemical biology of inflammation. Arch. Biochem. Biophys. 2004;423:12–22
  5. Chen B, Keshive M, Deen WM. Diffusion and reaction of nitric oxide in suspension cell cultures. Biophys. J. 1998;75:745–754
  6. Chen B, Deen WM. Analysis of the effects of cell spacing and liquid depth on nitric oxide and its oxidation products in cell cultures. Chem. Res. Toxicol. 2001;14:135–147
  7. Miller LJ, Marx J. Apoptosis. Science. 1998;281:1301
  8. Chung HT, Pae HO, Choi BM, Billiar TR, Kim YM. Nitric oxide as a bioregulator of apoptosis. Biochem. Biophys. Res. Commun. 2001;282:1075–1079
  9. Brune B, von Knethen A, Sandau KB. Nitric oxide (NO): an effector of apoptosis. Cell Death Differ. 1999;6:969–975
  10. Kim PK, Zamora R, Petrosko P, Billiar TR. The regulatory role of nitric oxide in apoptosis. Int. Immunopharmacol. 2001;1:1421–1441
  11. Messmer UK, Brune B. Nitric oxide (NO) in apoptotic versus necrotic RAW 264.7 macrophage cell death: the role of NO-donor exposure, NAD+ content, and p53 accumulation. Arch. Biochem. Biophys. 1996;327:1–10
  12. Pervin S, Singh R, Chaudhuri G. Nitric-oxide-induced Bax integration into the mitochondrial membrane commits MDA-MB-468 cells to apoptosis: essential role of Akt. Cancer Res. 2003;63:5470–5479
  13. Sandau KB, Brune B. Molecular actions of nitric oxide in mesangial cells. Histol. Histopathol. 2000;15:1151–1158
  14. Moriya R, Uehara T, Nomura Y. Mechanism of nitric oxide-induced apoptosis in human neuroblastoma SH-SY5Y cells. Fed. Eur. Biochem. Soc. Lett. 2000;484:253–260
  15. Yabuki M, Tsutsui K, Horton AA, Yoshioka T, Utsumi K. Caspase activation and cytochrome c release during HL-60 cell apoptosis induced by a nitric oxide donor. Free Radic. Res. 2000;32:507–514
  16. Li CQ, Robles AI, Hanigan CL, Hofseth LJ, Trudel LJ, Harris CC, et al. Apoptotic signaling pathways induced by nitric oxide in human lymphoblastoid cells expressing wild-type or mutant p53. Cancer Res. 2004;64:3022–3029
  17. Li J, Billiar TR. The anti-apoptotic actions of nitric oxide in hepatocytes. Cell Death. Differ. 1999;6:952–955
  18. Wang Y, Vodovotz Y, Kim PK, Zamora R, Billiar TR. Mechanisms of hepatoprotection by nitric oxide. Ann. N.Y. Acad. Sci. 2002;962:415–422
  19. Taylor EL, Megson IL, Haslett C, Rossi AG. Nitric oxide: a key regulator of myeloid inflammatory cell apoptosis. Cell Death. Differ. 2003;10:418–430
  20. Kolb JP. Mechanisms involved in the pro- and anti-apoptotic role of NO in human leukemia. Leukemia. 2000;14:1685–1694
  21. Kim YM, de Vera ME, Watkins SC, Billiar TR. Nitric oxide protects cultured rat hepatocytes from tumor necrosis factor-alpha-induced apoptosis by inducing heat shock protein 70 expression. J. Biol. Chem. 1997;272:1402–1411
  22. Kim YM, Talanian RV, Billiar TR. Nitric oxide inhibits apoptosis by preventing increases in caspase-3-like activity via two distinct mechanisms. J. Biol. Chem. 1997;272:31138–31148
  23. Sciorati C, Rovere P, Ferrarini M, Heltai S, Manfredi AA, Clementi E, et al. Autocrine nitric oxide modulates CD95-induced apoptosis in gammadelta T lymphocytes. J. Biol. Chem. 1997;272:23211–23215
  24. DeMeester SL, Qiu Y, Buchman TG, Hotchkiss RS, Dunnigan K, Karl IE, et al. Nitric oxide inhibits stress-induced endothelial cell apoptosis. Crit. Care Med. 1998;26:1500–1509
  25. Ho FM, Liu SH, Liau CS, Huang PJ, Shiah SG, Lin-Shiau SY, et al. Nitric oxide prevents apoptosis of human endothelial cells from high glucose exposure during early stage. J. Cell Biochem. 1999;75:258–263
  26. Kim YM, Chung HT, Kim SS, Han JA, Yoo YM, Kim KM, et al. Nitric oxide protects PC12 cells from serum deprivation-induced apoptosis by cGMP-dependent inhibition of caspase signaling. J. Neurosci. 1999;19:6740–6747
  27. Sata M, Kakoki M, Nagata D, Nishimatsu H, Suzuki E, Aoyagi T, et al. Adrenomedullin and nitric oxide inhibit human endothelial cell apoptosis via a cyclic GMP-independent mechanism. Hypertension. 2000;36:83–88
  28. Kim YM, Kim TH, Chung HT, Talanian RV, Yin XM, Billiar TR. Nitric oxide prevents tumor necrosis factor alpha-induced rat hepatocyte apoptosis by the interruption of mitochondrial apoptotic signaling through S-nitrosylation of caspase-8. Hepatology. 2000;32:770–778
  29. Kim JE, Tannenbaum SR. S-Nitrosation regulates the activation of endogenous procaspase-9 in HT-29 human colon carcinoma cells. J. Biol. Chem. 2004;279:58–64
  30. Tabuchi A, Sano K, Oh E, Tsuchiya T, Tsuda M. Modulation of AP-1 activity by nitric oxide (NO) in vitro: NO-mediated modulation of AP-1. Fed. Eur. Biochem. Soc. Lett. 1994;351:123–127
  31. Reynaert NL, Ckless K, Korn SH, Vos N, Guala AS, Wouters EF, et al. Nitric oxide represses inhibitory kappaB kinase through S-nitrosylation. Proc. Natl Acad. Sci. USA. 2004;101:8945–8950
  32. Rubbo H, Radi R, Trujillo M, Telleri R, Kalyanaraman B, Barnes S, et al. Nitric oxide regulation of superoxide and peroxynitrite-dependent lipid peroxidation. Formation of novel nitrogen-containing oxidized lipid derivatives. J. Biol. Chem. 1994;269:26066–26075
  33. Brune B, Gotz C, Messmer UK, Sandau K, Hirvonen MR, Lapetina EG. Superoxide formation and macrophage resistance to nitric oxide-mediated apoptosis. J. Biol. Chem. 1997;272:7253–7258
  34. Vieira HL, Belzacq AS, Haouzi D, Bernassola F, Cohen I, Jacotot E, et al. The adenine nucleotide translocator: a target of nitric oxide, peroxynitrite, and 4-hydroxynonenal. Oncogene. 2001;20:4305–4316
  35. Tabor CW, Tabor H. Polyamines in microorganisms. Microbiol. Rev. 1985;49:81–99
  36. Keefer LK, Nims RW, Davies KM, Wink DA. ‘NONOates’ (1-substituted diazen-1-ium-1,2-diolates) as nitric oxide donors: convenient nitric oxide dosage forms. Methods Enzymol. 1996;268:281–293
  37. Chen B, Deen WM. Effect of liquid depth on the synthesis and oxidation of nitric oxide in macrophage cultures. Chem. Res. Toxicol. 2002;15:490–496
  38. McCormick CC, Li WP, Calero M. Oxygen tension limits nitric oxide synthesis by activated macrophages. Biochem. J. 2000;350:709–716
  39. Otto CM, Baumgardner JE. Effect of culture PO2 on macrophage (RAW 264.7) nitric oxide production. Am. J. Physiol. Cell Physiol. 2001;280:C280–C287
  40. Gardner PR, Martin LA, Hall D, Gardner AM. Dioxygen-dependent metabolism of nitric oxide in mammalian cells. Free Radic. Biol. Med. 2001;31:191–204
  41. Cassoly R, Gibson Q. Conformation, co-operativity and ligand binding in human hemoglobin. J. Mol. Biol. 1975;91:301–313
  42. Beckman JS, Koppenol WH. Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly, Am. J. Physiol. 1996;271:C1424–C1437
  43. Lewis RS, Deen WM. Kinetics of the reaction of nitric oxide with oxygen in aqueous solutions. Chem. Res. Toxicol. 1994;7:568–574
  44. Tamir S, Lewis RS, de Rojas Walker T, Deen WM, Wishnok JS, Tannenbaum SR, et al. The influence of delivery rate on the chemistry and biological effects of nitric oxide. Chem. Res. Toxicol. 1993;6:895–899
  45. Wang C, Deen WM. Nitric oxide delivery system for cell culture studies. Ann. Biomed. Eng. 2003;31:65–79
  46. Wang C, Trudel LJ, Wogan GN, Deen WM. Thresholds of nitric oxide-mediated toxicity in human lymphoblastoid cells. Chem. Res. Toxicol. 2003;16:1004–1013
  47. Li J, Billiar TR. Nitric oxide IV. Determinants of nitric oxide protection and toxicity in live. Am. J. Physiol. 1999;276:G1069–G1073
  48. Li CQ, Trudel LJ, Wogan GN. Nitric oxide-induced genotoxicity, mitochondrial damage, and apoptosis in human lymphoblastoid cells expressing wild-type and mutant p53. Proc. Natl Acad. Sci. USA. 2002;99:10364–10369
  49. Leist M, Nicotera P. The shape of cell death. Biochem. Biophys. Res. Commun. 1997;236:1–9
  50. Leist M, Single B, Castoldi AF, Kuhnle S, Nicotera P. Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis. J. Exp. Med. 1997;185:1481–1486
  51. Ankarcrona M, Dypbukt JM, Bonfoco E, Zhivotovsky B, Orrenius S, Lipton SA, et al. Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron. 1995;15:961–973
  52. Okada H, Mak TW. Pathways of apoptotic and non-apoptotic death in tumour cells. Nat. Rev. Cancer. 2004;4:592–603
  53. Bonfoco E, Krainc D, Ankarcrona M, Nicotera P, Lipton SA. Apoptosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N-methyl-d-aspartate or nitric oxide/superoxide in cortical cell cultures. Proc. Natl Acad. Sci. USA. 1995;92:7162–7166
  54. Okuno S, Shimizu S, Ito T, Nomura M, Hamada E, Tsujimoto Y, et al. Bcl-2 prevents caspase-independent cell death. J. Biol. Chem. 1998;273:34272–34277
  55. Brown GC. Nitric oxide and mitochondrial respiration. Biochim. Biophys. Acta. 1999;1411:351–369
  56. Brown GC, Borutaite V. Nitric oxide inhibition of mitochondrial respiration and its role in cell death. Free Radic. Biol. Med. 2002;33:1440–1450
  57. Nicotera P, Melino G. Regulation of the apoptosis-necrosis switch. Oncogene. 2004;23:2757–2765
  58. Zhuang JC, Wright TL, deRojas-Walker T, Tannenbaum SR, Wogan GN. Nitric oxide-induced mutations in the HPRT gene of human lymphoblastoid TK6 cells and in Salmonella typhimurium. Environ. Mol. Mutagen. 2000;35:39–47
  59. Wink DA, Kasprzak KS, Maragos CM, Elespuru RK, Misra M, Dunams TM, et al. DNA ability and genotoxicity of nitric oxide and its progenitors. Science. 1991;254:1001–1003
  60. deRojas-Walker T, Tamir S, Ji H, Wishnok JS, Tannenbaum SR. Nitric oxide induces oxidative damage in addition to deamination in macrophage DNA. Chem. Res. Toxicol. 1995;8:473–477
  61. Li CQ, Trudel LJ, Wogan GN. Genotoxicity, mitochondrial damage, and apoptosis in human lymphoblastoid cells exposed to peroxynitrite generated from SIN-1. Chem. Res. Toxicol. 2002;15:527–535
  62. Juedes MJ, Wogan GN. Peroxynitrite-induced mutation spectra of pSP189 following replication in bacteria and in human cells. Mutat. Res. 1996;349:51–61
  63. Lichtenauer-Kaligis EG, Thijssen JC, den Dulk H, Van de Putte P, Giphart-Gassler M, Tasseron-de JG, et al. Spontaneous mutation spectrum in the hprt gene in human lymphoblastoid TK6 cells. Mutagenesis. 1995;10:137–143
  64. Zhuang JC, Lin C, Lin D, Wogan GN. Mutagenesis associated with nitric oxide production in macrophages. Proc. Natl Acad. Sci. USA. 1998;95:8286–8291
  65. Schopfer FJ, Baker PR, Freeman BA. NO-dependent protein nitration: a cell signaling event or an oxidative inflammatory response?. Trends Biochem. Sci. 2003;28:646–654
  66. Haendeler J, Hoffmann J, Tischler V, Berk BC, Zeiher AM, Dimmeler S, et al. Redox regulatory and anti-apoptotic functions of thioredoxin depend on S-nitrosylation at cysteine 69. Nat. Cell Biol. 2002;4:743–749
  67. Hofseth LJ, Saito S, Hussain SP, Espey MG, Miranda KM, Araki Y, et al. Nitric oxide-induced cellular stress and p53 activation in chronic inflammation. Proc. Natl Acad. Sci. USA. 2003;100:143–148
  68. Ischiropoulos H. Biological selectivity and functional aspects of protein tyrosine nitration. Biochem. Biophys. Res. Commun. 2003;305:776–783
  69. Gow AJ, Farkouh CR, Munson DA, Posencheg MA, Ischiropoulos H. Biological significance of nitric oxide-mediated protein modifications. Am. J. Physiol. Lung Cell Mol. Physiol. 2004;287:L262–L268
  70. Stamler JS, Hausladen A. Oxidative modifications in nitrosative stress. Nat. Struct. Biol. 1998;5:247–249
  71. Landar A, Darley-Usmar VM. Nitric oxide and cell signaling: modulation of redox tone and protein modification. Amino Acids. 2003;25:313–321
  72. Hussain SP, Hofseth LJ, Harris CC. Radical causes of cancer. Nat. Rev. Cancer. 2003;3:276–285
  73. Stamler JS, Lamas S, Fang FC. Nitrosylation: the prototypic redox-based signaling mechanism. Cell. 2001;106:675–683
  74. Davis DW, Weidner DA, Holian A, McConkey DJ. Nitric oxide-dependent activation of p53 suppresses bleomycin-induced apoptosis in the lung. J. Exp. Med. 2000;192:857–869
  75. Brune B. Nitric oxide: NO apoptosis or turning it ON?. Cell Death Differ. 2003;10:864–869
  76. Ambs S, Merriam WG, Ogunfusika MO, Bennett WP, Ishibe N, Hussain SP, et al. p53 and vascular endothelial growth factor regulate tumor growth of NOS2-expressing human carcinoma cells. Nat. Med. 1998;4:1371–1376
  77. Hussain SP, Amstad P, Raja K, Ambs S, Nagashima M, Bennett WP, et al. Increased p53 mutation load in noncancerous colon tissue from ulcerative colitis: a cancer-prone chronic inflammatory disease. Cancer Res. 2000;60:3333–3337
  78. Goodman JE, Hofseth LJ, Hussain SP, Harris CC. Nitric oxide and p53 in cancer-prone chronic inflammation and oxyradical overload disease. Environ. Mol. Mutagen. 2004;44:3–9
  79. Beltran B, Mathur A, Duchen MR, Erusalimsky JD, Moncada S. The effect of nitric oxide on cell respiration: a key to understanding its role in cell survival or death. Proc. Natl Acad. Sci. USA. 2000;97:14602–14607
  80. Palacios-Callender M, Quintero M, Hollis VS, Springett RJ, Moncada S. Endogenous NO regulates superoxide production at low oxygen concentrations by modifying the redox state of cytochrome c oxidase. Proc. Natl Acad. Sci. USA. 2004;101:7630–7635
  81. Moncada S, Erusalimsky JD. Does nitric oxide modulate mitochondrial energy generation and apoptosis?. Nat. Rev. Mol. Cell Biol. 2002;3:214–220
  82. Brown GC, Cooper CE. Nanomolar concentrations of nitric oxide reversibly inhibit synaptosomal respiration by competing with oxygen at cytochrome oxidase. Fed. Eur. Biochem. Soc. Lett. 1994;356:295–298
  83. Brookes PS, Salinas EP, Darley-Usmar K, Eiserich JP, Freeman,V BA, Darley-Usmar M, et al. Concentration-dependent effects of nitric oxide on mitochondrial permeability transition and cytochrome c release. J. Biol. Chem. 2000;275:20474–20479
  84. Zech B, Kohl R, von Knethen A, Brune B. Nitric oxide donors inhibit formation of the Apaf-1/caspase-9 apoptosome and activation of caspases. Biochem. J. 2003;371:1055–1064
  85. Jaiswal AK. Nrf2 signaling in coordinated activation of antioxidant gene expression. Free Radic. Biol. Med. 2004;36:1199–1207
  86. Mytilineou C, Kramer BC, Yabut JA. Glutathione depletion and oxidative stress. Parkinsonism Relat. Disord. 2002;8:385–387
  87. Pompella A, Visvikis A, Paolicchi A, de Tata V, Casini AF. The changing faces of glutathione, a cellular protagonist. Biochem. Pharmacol. 2003;66:1499–1503
  88. Boggs SE, McCormick TS, Lapetina EG. Glutathione levels determine apoptosis in macrophages. Biochem. Biophys. Res. Commun. 1998;247:229–233
  89. Butzer U, Weidenbach H, Gansauge S, Gansauge F, Beger HG, Nussler AK, et al. Increased oxidative stress in the RAW 264.7 macrophage cell line is partially mediated via the S-nitrosothiol-induced inhibition of glutathione reductase. Fed. Eur. Biochem. Soc. Lett. 1999;445:274–278
  90. Umansky V, Rocha M, Breitkreutz R, Hehner S, Bucur M, Erbe N, et al. Glutathione is a factor of resistance of Jurkat leukemia cells to nitric oxide-mediated apoptosis. J. Cell Biochem. 2000;78:578–587
  91. Birnboim HC, Privora H. Depletion of intracellular glutathione reduces mutations by nitric oxide-donating drugs. Nitric Oxide. 2000;4:496–504
  92. Luperchio S, Tamir S, Tannenbaum SR. No-induced oxidative stress and glutathione metabolism in rodent and human cells. Free Radic. Biol. Med. 1996;21:513–519
  93. Troy CM, Derossi D, Prochiantz A, Greene LA, Shelanski ML. Downregulation of Cu/Zn superoxide dismutase leads to cell death via the nitric oxide-peroxynitrite pathway. J. Neurosci. 1996;16:253–261
  94. Elroy-Stein O, Bernstein Y, Groner Y. Overproduction of human Cu/Zn-superoxide dismutase in transfected cells: extenuation of paraquat-mediated cytotoxicity and enhancement of lipid peroxidation. Eur. Mol. Biol. Org. J. 1986;5:615–622
  95. Huang TT, Carlson EJ, Leadon SA, Epstein CJ. Relationship of resistance to oxygen free radicals to CuZn-superoxide dismutase activity in transgenic, transfected, and trisomic cells. Fed. Am. Soc. Exp. Biol. J. 1992;6:903–910
  96. Sano H, Hirai M, Saito H, Nakashima I, Isobe KI. A nitric oxide-releasing reagent, S-nitroso-N-acetylpenicillamine, enhances the expression of superoxide dismutases mRNA in the murine macrophage cell line RAW264-7. Immunology. 1997;92:118–122
  97. Brockhaus F, Brune B. Overexpression of CuZn superoxide dismutase protects RAW 264.7 macrophages against nitric oxide cytotoxicity. Biochem. J. 1999;338:295–303
  98. Ciriolo MR, de Martino A, Lafavia E, Rossi L, Carri MT, Rotilio G. Cu,Zn-superoxide dismutase-dependent apoptosis induced by nitric oxide in neuronal cells. J. Biol. Chem. 2000;275:5065–5072
  99. Morrison BM, Morrison JH. Amyotrophic lateral sclerosis associated with mutations in superoxide dismutase: a putative mechanism of degeneration. Brain Res. Brain Res. Rev. 1999;29:121–135
  100. Hussain SP, Amstad P, He P, Robles A, Lupold S, Kaneko I, et al. p53-induced up-regulation of MnSOD and GPx but not catalase increases oxidative stress and apoptosis. Cancer Res. 2004;64:2350–2356
  101. Gao B, Flores SC, Leff JA, Bose SK, McCord JM. Synthesis and anti-inflammatory activity of a chimeric recombinant superoxide dismutase: SOD2/3. Am. J. Physiol. Lung Cell Mol. Physiol. 2003;284:L917–L925
  102. Gow A, Ischiropoulos H. Super-SOD: superoxide dismutase chimera fights off inflammation. Am. J. Physiol. Lung Cell Mol. Physiol. 2003;284:L915–L916
  103. Itoh K, Tong KI, Yamamoto M. Molecular mechanism activating Nrf2-Keap1 pathway in regulation of adaptive response to electrophiles. Free Radic. Biol. Med. 2004;36:1208–1213
  104. Kang MI, Kobayashi A, Wakabayashi N, Kim SG, Yamamoto M. Scaffolding of Keap1 to the actin cytoskeleton controls the function of Nrf2 as key regulator of cytoprotective phase 2 genes. Proc. Natl Acad. Sci. USA. 2004;101:2046–2051
  105. Dhakshinamoorthy S, Porter AG. Nitric oxide-induced transcriptional up-regulation of protective genes by Nrf2 via the antioxidant response element counteracts apoptosis of neuroblastoma cells. J. Biol. Chem. 2004;279:20096–20107
  106. Bloom DA, Jaiswal AK. Phosphorylation of Nrf2 at Ser40 by protein kinase C in response to antioxidants leads to the release of Nrf2 from INrf2, but is not required for Nrf2 stabilization/accumulation in the nucleus and transcriptional activation of antioxidant response element-mediated NAD(P)H:quinone oxidoreductase-1 gene expression. J. Biol. Chem. 2003;278:44675–44682
  107. Wakabayashi N, Dinkova-Kostova AT, Holtzclaw WD, Kang MI, Kobayashi A, Yamamoto M, et al. Protection against electrophile and oxidant stress by induction of the phase 2 response: fate of cysteines of the Keap1 sensor modified by inducers. Proc. Natl Acad. Sci. USA. 2004;101:2040–2045
  108. Zhang DD, Hannink M. Distinct cysteine residues in Keap1 are required for Keap1-dependent ubiquitination of Nrf2 and for stabilization of Nrf2 by chemopreventive agents and oxidative stress. Mol. Cell Biol. 2003;23:8137–8151
  109. Jaffrey SR, Erdjument-Bromage H, Ferris CD, Tempst P, Snyder SH. Protein S-nitrosylation: a physiological signal for neuronal nitric oxide. Nat. Cell Biol. 2001;3:193–197
  110. Lane P, Hao G, Gross SS. S-nitrosylation is emerging as a specific and fundamental posttranslational protein modification: head-to-head comparison with O-phosphorylation. Sci. STKE. 2001;86:RE1
  111. Offer H, Erez N, Zurer I, Tang X, Milyavsky M, Goldfinger N, et al. The onset of p53-dependent DNA repair or apoptosis is determined by the level of accumulated damaged DNA. Carcinogenesis. 2002;23:1025–1032

PII: S0304-3835(04)00818-3

doi: 10.1016/j.canlet.2004.10.021

Cancer Letters
Volume 226, Issue 1 , Pages 1-15 , 8 August 2005

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