Interactive effects of nitric oxide and the p53 tumor suppressor gene in carcinogenesis and tumor progression

FASEB Journal

Volumn 11, Issue 6, 1997, Pages 443-448

  Ambs, Stefan ^a   Hussain, S Perwez ^a   Harris, Curtis C ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Apoptosis; DNA damage; Molecular epidemiology; Mutagenesis

Indexed keywords

DNA; NITRIC OXIDE; PEROXYNITRITE;

ANGIOGENESIS; APOPTOSIS; DIAGNOSIS; DNA DAMAGE; ENZYME INDUCTION; ETIOLOGY; GENOTOXICITY; GROWTH INHIBITION; HUMAN; HUMAN CELL; NEGATIVE FEEDBACK; PRIORITY JOURNAL; REVIEW; TUMOR SUPPRESSOR GENE;

EID: 0030986262     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fasebj.11.6.9194524     Document Type: Review

References (89)

1. Hollstein, M., Sidransky, D., Vogelstein, B., and Harris, C. C. (1991) p53 mutations in human cancer. Science 253, 49-53
2. Levine, A. J., Momand, J., and Finlay, C. A. (1991) The p53 tumour suppressor gene. Nature (London) 351, 453-156
3. Greenblatt, M. S., Bennett, W. P., Hollstein, M., and Harris, C. C. (1994) Mutations in the p53 tumor suppressor gene: clues to cancer etiology and molecular pathogenesis. Cancer Res. 54, 4855-4878
4. Harris, C. C. (1996) Structure and function of the p53 tumor suppressor gene: clues for rational cancer therapeutic strategies. J. Natl. Cancer Inst. 88, 1442-1445
5. Dittmer, D., Pati, S., Zambetti, G., Chu, S., Teresky, A. K., Moore, M., Finlay, C., and Levine, A. J. (1993) Gain of function mutations in p53. Nature Genet. 4, 42-46
6. Prives, C. (1994) How loops, beta sheets, and alpha helices help us to understand p53. Cell 78, 543-546
7. Milner, J., Medcalf, E. A., and Cook, A. C. (1991) Tumor suppressor p53: analysis of wild-type and mutant p53 complexes. Mol. Cell. Biol. 11, 12-19
8. Bakalkin, G., Selivanova, G., Yakovleva, T., Kiseleva, E., Kashuba, E., Magnusson, K. P., Szekely, L., Klein, G., Terenius, L., and Wiman, K. G. (1995) p53 binds single-stranded DNA ends through the C-terminal domain and internal DNA segments via the middle domain. Nucleic Acids Res. 23, 362-369
9. Reed, M., Woelker, B., Wang, P., Wang, Y., Anderson, M. E., and Tegtmeyer, P. (1995) The C-terminal domain of p53 recognizes DNA damaged by ionizing radiation. Proc. Natl. Acad. Sci. USA 92, 9455-9459
10. Horikoshi, N., Usheva, A., Chen, J., Levine, A. J., Weinmann, R., and Shenk, T. (1995) Two domains of p53 interact with the TATA-binding protein, and the adenovirus 13S E1A protein disrupts the association, relieving p53-mediated transcriptional repression. Mol. Cell. Biol. 15, 227-234
11. Wang, X. W., Vermeulen, W., Coursen, J. D., Gibson, M., Lupold, S. E., Forrester, K., Xu, G., Elmore, L., Yeh, H., Hoeijmakers, J. H. J., and Harris, C. C. (1996) The XPB and XPD helicases are components of the p53-mediated apoptosis pathway. Genes & Dev. 10, 1219-1232
12. Wang, X. W., Gibson, M. K., Vermeulen, W., Yeh, H., Forrester, K., Stuerzbecher, H.-W., Hoeijmakers, J. H. J., and Harris, C. C. (1995) Abrogation of p53-induced apoptosis by the hepatitis B virus X gene. Cancer Res. 55, 6012-6016
13. Ko, L.J., and Prives, C. (1996) p53: puzzle and paradigm. Genes & Dev. 10, 1054-1072
14. Gottlieb, T. M., and Oren, M. (1996) p53 in growth control and neoplasia. Biochim. Biophys. Acta 1287, 77-102
15. Kastan, M. B., Onyekwere, O., Sidransky, D., Vogelstein, B., and Craig, R. W. (1991) Participation of p53 protein in the cellular response to DNA damage. Cancer Res. 51, 6304-6311
16. Huang, L-C., Clarkin, K. C., and Wahl, G. M. (1996) Sensitivity and selectivity of the DNA damage sensor responsible for activating p53-dependent G1 arrest. Proc. Natl. Acad. Sci. USA 93, 4827-4832
17. Messmer, U. K., Ankarcrona, M., Nicotera, P., and Brune, B. (1994) p53 expression in nitric oxide-induced apoptosis. FEBS Lett. 355, 23-26
18. Forrester, K., Ambs, S., Lupold, S. E., Kapust, R. B., Spillare, E. A., Weinberg, W. C., Felley-Bosco, E., Wang, X. W., Geller, D. A., Billiar, T. R., and Harris, C. C. (1996) Nitric oxide-induced p53 accumulation and regulation of inducible nitric oxide synthase (NOS2) expression by wild-type p53. Proc. Natl. Acad. Sci. USA 93, 2442-2447
19. Ho, Y. S., Wang, Y. J., and Lin, J. K. (1996) Induction of p53 and p21/WAF1/CIP1 expression by nitric oxide and their association with apoptosis in human cancer cells. Mol. Carcinog. 16, 20-31
20. Fehsel, K., Kroncke, K.-D., Meyer, K. L., Huber, H., Wahn, V., and Kolb-Bachofen, V. (1995) Nitric oxide induces apoptosis in mouse thymocytes. J. Immunol. 155, 2858-2865
21. Geng, Y. J., Hellstrand, K., Wennmalm, A., and Hansson, G. K. (1996) Apoptotic death of human leukemic cells induced by vascular cells expressing nitric oxide synthase in response to gamma-interferon and tumor necrosis factor-alpha. Cancer Res. 56, 866-874
22. Maki, C. G., Huibregtse, J. M., and Howley, P. M. (1996) In vivo ubiquitination and proteasome-mediated degradation of p53. Cancer Res. 56, 2649-2654
23. El-Deiry, W. S., Harper, J. W., O'Connor, P. M., Velculescu, V. E., Canman, C. E., Jackman, J., Pietenpol, J. A., Burrell, M., Hill, D. E., Wang, Y., and et al. (1994) WAF1/CIP1 is induced in p53-mediated G1 arrest and apoptosis. Cancer Res. 54, 1169-1174
24. Hollander, M. C., Alamo, I., Jackman, J., Wang, M. G., McBride, O. W., and Fornace, A. J., Jr. (1993) Analysis of the mammalian gadd45 gene and its response to DNA damage. J. Biol. Chem 268, 24385-24393
25. Okamoto, K., and Beach, D. (1994) Cyclin G is a transcriptional target of the p53 tumor suppressor protein. EMBO J. 13, 4816-4822
26. Miyashita, T., and Reed, J. C. (1995) Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell 80, 293-299
27. Buckbinder, L., Talbott, R., Velasco-Miguel, S., Takenaka, I., Faha, B., Seizinger, B. R., and Kley, N. (1996) Induction of the growth inhibitor IGF-hinding protein 3 by p53. Nature (London) 377, 646-649
28. Tamura, T., Aoyama, N., Saya, H., Haga, H., Futami, S., Miyamoto, M., Koh, T., Ariyasu, T., Tachi, M., Kasuga, M., and Takahashi, R. (1995) Induction of Fas-mediated apoptosis in p53-transfected human colon carcinoma cells. Oncogene 11, 1939-1946
29. Seto, E., Usheva, A., Zambetti, G. P., Momand, J., Horikoshi, N., Weinmann, R., Levine, A. J., and Shenk, T. (1992) Wild-type p53 binds to the TATA-binding protein and represses transcription. Proc. Natl. Acad. Sci. USA 89, 12028-12032
30. Truant, R., Xiao, H., Ingles, C. J., and Greenblatt, J. (1993) Direct interaction between the transcriptional activation domain of human p53 and the TATA box-binding protein. J. Biol. Chem 268, 2284-2287
31. Miller, S. D., Farmer, G., and Prives, C. (1995) p53 inhibits DNA replication in vitro and in a DNA-binding-dependent manner. Mol. Cell. Biol. 15, 6554-6560
32. Cox, L. S., Hupp, T., Midgley, C. A., and Lane, D. P. (1995) A direct effect of activated human p53 on nuclear DNA replication. EMBO J. 14, 2099-2105
33. Li, R., Waga, S., Hannon, G.J., Beach, D., and Stillman, B. (1994) Differential effects by the p21 CDK inhibitor on PCNA-dependent DNA replication and repair. Nature (London) 371, 534-537
34. Dutta, A., Ruppert, J. M., Aster, J. C., and Winchester, E. (1993) Inhibition of DNA replication factor RPA by p53. Nature (London) 365, 79-82
35. Wang, X. W., Yeh, H., Schaeffer, L., Roy, R., Moncollin, V., Egly, J. M., Wang, Z., Friedberg, E. C., Evans, M. K., Taffe, B. G., Bohr, V. A., Hoeijmakers, J. H., Forrester, K., and Harris, C.C. (1995) p53 Modulation of TFIIH-associated nucleotide excision repair activity. Nature Genet. 10, 188-195
36. Caelles, C., Helmberg, A., and Karin, M. (1994) p53-dependent apoptosis in the absence of transcriptional activation of p53-target genes [see comments]. Nature (London) 370, 220-223
37. Crook, T., Wrede, D., Tidy, J. A., Mason, W. P., Evans, D. J., and Vousden, K. H. (1992) Clonal p53 mutation in primary cervical cancer: association with human-papilloma-virus-negative tumours. Lancet 339, 1070-1073
38. Haupt, Y., Rowan, S., Shaulian, E., Vousden, K., and Oren, M. (1995) Induction of apoptosis in HeLa cells by transactivation-deficient p53. Genes & Dev. 9, 2170-2183
39. Sabbatini, P., Lin, J., Levine, A. J., and White, E. (1995) Essential role for p53-mediated transcription in E1A-induced apoptosis. Genes & Dev. 9, 2184-2192
40. Harris, C. C., Grady, H., and Svoboda, D. (1968) Alterations in pancreatic and hepatic ultrastructure following acute cycloheximide intoxication. J. Ultrastruct. Res. 22, 240-251
41. Hollstein, M., Shomer, B., Greenblatt, M., Soussi, T., Hovig, E., Montesano, R., and Harris, C. C. (1996) Somatic point mutations in the p53 gene of human tumors and cell lines: updated compilation. Nucleic Acids Res. 24, 141-146
42. Ohue, M., Tomita, N., Monden, T., Fujita, M., Fukunaga, M., Takami, K., Yana, I., Ohnishi, T., Enomoto, T., Inoue, M., Shimano, T., and Mori, T. (1994) A frequent alteration of p53 gene in carcinoma in adenoma of colon. Cancer Res. 54, 4798-4804
43. Sidransky, D., Mikkelsen, T., Schwechheimer, K., Rosenblum, M. L., Cavenee, W., and Vogelstein, B. (1992) Clonal expansion of p53 mutant cells is associated with brain tumour progression. Nature (London) 355, 846-847
44. Fearon, E. R., and Vogelstein, B. (1990) A genetic model for colorectal tumorigenesis. Cell 61, 759-767
45. Moncada, S., Palmer, R. M., and Higgs, E. A. (1991) Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol. Rev 43, 109-142
46. Bredt, D. S., and Snyder, S. H. (1994) Nitric oxide: a physiologic messenger molecule. Annu. Rev Biochem. 63, 175-195
47. Paraskeva, E., and Hentze, M. W. (1996) Iron-sulphur clusters as genetic regulatory switches: the bifunctional iron regulatory protein-1. FEBS Lett. 389, 40-43
48. Nathan, C., and Xie, Q. W. (1994) Nitric oxide synthases: roles, tolls, and controls. Cell 78, 915-918
49. Tamir, S., and Tannenbaum, S. R. (1996) The role of nitric oxide (NO·) in the carcinogenic process. Biochim. Biophys. Acta 1288, F31-F36
50. Wink, D. A., Hanbauer, I., Grisham, M. B., Laval, F., Nims, R. W., Laval, J., Cook, J., Pacelli, R., Liebmann, J., Krishna, M., Ford, P. C., and Mitchell, J. B. (1996) Chemical biology of nitric oxide: regulation and protective and toxic mechanisms. Curr Top. Cell Regul. 34, 159-187
51. Crow, J. P., and Beckman, J. S. (1995) Reactions between nitric oxide, superoxide, and peroxynitrite: footprints of peroxynitrite in vivo. Adv. Pharmacol. 34, 17-43
52. Wink, D. A., Kasprzak, K. S., Maragos, C. M., Elespuru, R. K., Misra, M., Dunams, T. M., Cebula, T. A., Koch, W. H., Andrews, A. W., Allen, J. S., and Keefer, L. K. (1991) DNA deaminating ability and genotoxicity of nitric oxide and its progenitors. Science 254, 1001-1003
53. Nguyen, T., Brunson, D., Crespi, C. L., Penman, B. W., Wishnok, J. S., and Tannenbaum, S. R. (1992) DNA damage and mutation in human cells exposed to nitric oxide in vitro. Proc. Natl. Acad. Sci. USA 89, 3030-3034
54. Gorsdorf, S., Appel, K. E., Engeholm, C., and Obe, G. (1990) Nitrogen dioxide induces DNA single-strand breaks in cultured Chinese hamster cells. Carcinogenesis 11, 37-41
55. Yermilov, V., Rubio, J., Becchi, M., Friesen, M. D., Pignatelli, B., and Ohshima, H. (1995) Formation of 8-nitroguanine by the reaction of guanine with peroxynitrite in vitro. Carcinogenesis 16, 2045-2050
56. Marletta, M. A. (1988) Mammalian synthesis of nitrite, nitrate, nitric oxide, and N-nitrosating agents. Chem Res. Toxicol 1, 249-257
57. Wu, Y., Brouet, I., Calmels, S., Bartsch, H., and Ohshima, H. (1993) Increased endogenous N-nitrosamine and nitrate formation by induction of nitric oxide synthase in rats with acute hepatic injury caused by Propionibacterium acnes and lipopolysaccharide administration. Carcinogenesis 14, 7-10
58. Rubbo, H., Tarpey, M., and Freeman, B. A. (1995) Nitric oxide and reactive oxygen species in vascular injury. Biochem. Soc. Symp. 61, 33-45
59. 6-methylguanine-DNA-methyltransferase. Carcinogenesis 15, 443-447
60. Wink, D. A., and Laval, F. (1994) The Fpg protein, a DNA repair enzyme, is inhibited by the biomediator nitric oxide in vitro and in vivo. Carcinogenesis 15, 2125-2129
61. Szabo, C., Zingarelli, B., O'Connor, M., and Salzman, A. L. (1996) DNA strand breakage, activation of poly (ADP-ribose) synthetase, and cellular energy depletion are involved in the cytotoxicity of macrophages and smooth muscle cells exposed to peroxynitrite. Proc. Natl. Acad. Sci. USA 93, 1753-1758
62. Kwon, N. S., Stuehr, D. J., and Nathan, C. F. (1991) Inhibition of tumor cell ribonucleotide reductase by macrophage-derived nitric oxide. J. Exp. Med. 174, 761-767
63. Wink, D. A., Hanbauer, I., Krishna, M. C., DeGraff, W., Gamson, J., and Mitchell, J. B. (1993) Nitric oxide protects against cellular damage and cytotoxicity from reactive oxygen species. Proc. Natl. Acad. Sci. USA 90, 9813-9817
64. Mannick, J. B., Asano, K., Izumi, K., Kieff, E., and Stamler, J. S. (1994) Nitric oxide produced by human B lymphocytes inhibits apoptosis and Epstein-Barr virus reactivation. Cell 79, 1137-1146
65. Genaro, A. M., Hortelano, S., Alvarez, A., Martinez-A. C., and Bosca, L. (1995) Splenic B lymphocyte programmed cell death is prevented by nitric oxide release through mechanisms involving sustained Bcl-2 levels. J Clin. Invest. 95, 1884-1890.
66. Xie, K., Huang, S., Dong, Z., Juang, S. H., Gutman, M., Xie, Q. W., Nathan, C., and Fidler, I. J. (1995) Transfection with the inducible nitric oxide synthase gene suppresses tumorigenicity and abrogates metastasis by K-1735 murine melanoma cells. J. Exp. Med. 181, 1333-1343
67. Jenkins, D. C., Charles, I. G., Thomsen, L. L., Moss, D. W., Holmes, L. S., Baylis, S. A., Rhodes, P., Westmore, K., Emson, P. C., and Moncada, S. (1995) Roles of nitric oxide in tumor growth. Proc. Natl. Acad. Sci. USA 92, 4392-4396
68. Marletta, M. A. (1994) Nitric oxide synthase: aspects concerning structure and catalysis. Cell 78, 927-930
69. Foerstermann, U., and Kleinert, H. (1995) Nitric oxide synthase: expression and expressional control of the three isoforms. Naunyn-Schmiedeberg's Arch Pharmacol. 352, 351-364
70. Guo, F. H., de Raeve, H. R., Rice, T. W., Stuehr, D. J., Thunnissen, F. B., and Erzurum, S. C. (1995) Continuous nitric oxide synthesis by inducible nitric oxide synthase in normal human airway epithelium in vivo. Proc. Natl. Acad. Sci. USA 92, 7809-7813
71. Hoffman, R. A., Zhang, G., Nuessler, T. C., Gleixner, S. L., Ford, H. R., Simmons, R. L., and Watkins, S. C. (1997) Constitutive expression of inducible nitric oxide synthase in the mouse ileal mucosa. Am. J. Physiol. 272, G383-G392
72. Melillo, G., Musso, T., Sica, A., Taylor, L. S., Cox, G. W., and Varesio, L. (1995) A hypoxia-responsive element mediates a novel pathway of activation of the inducible nitric oxide synthase promoter. J. Exp. Med. 182, 1683-1693
73. Billiar, T. R., Curran, R. D., Harbrecht, B. G., Stuehr, D. J., Demetris, A. J., and Simmons, R. L. (1990) Modulation of nitric oxide synthesis in vivo: NG-monomethyl-L-arginine inhibits endotoxin-induced nitrite/nitrate biosynthesis while promoting hepatic damage. J. Leukoc.Biol. 48, 565-569
74. deRojas-Walker, T., Tamir, S., Ji, H., Wishnok, J. S., and Tannenbaum, S. R. (1995) Nitric oxide induces oxidative damage in addition to deamination in macrophage DNA. Chem. Res. Toxicol 8, 473-477
75. Felley-Bosco, E., Mirkovitch, J., Ambs, S., Mace, K., Pfeifer, A., Keefer, L. K., and Harris, C. C. (1995) Nitric oxide and ethylnitrosurea: relative mutagenicity in the p53 tumor suppressor and hypoxanthine-phosphoribosyltransferase gene. Carcinogenesis 16, 2069-2074
76. Lindahl, T. (1993) Instability and decay of the primary structure of DNA. Nature (London) 362, 709-715
77. Cooper, D. N., and Youssoufian, H. (1988) The CpG dinucleotide and human genetic disease. Human Genet 78, 151-155
78. Thomsen, L. L., Lawton, F. G., Knowles, R. G., Beesley, J. E., Riveros-Moreno, V., and Moncada, S. (1994) Nitric oxide synthase activity in human gynecological cancer. Cancer Res. 54, 1352-1354
79. Thomsen, L. L., Miles, D. W., Happerfield, L., Bobrow, L. G., Knowles, R. G., and Moncada, S. (1995) Nitric oxide synthase activity in human breast cancer. Br. J. Cancer 72, 41-44
80. Cobbs, C. S., Brenman, J. E., Aldape, K. D., Bredt, D. S., and Israel, M. A. (1995) Expression of nitric oxide synthase in human central nervous system tumors. Cancer Res. 55, 727-730
81. Maeda, H., Noguchi, Y., Sato, K., and Akaike, T. (1994) Enhanced vascular permeability in solid tumor is mediated by nitric oxide and inhibited by both new nitric oxide scavenger and nitric oxide synthase inhibitor. Jpn. J. Cancer Res. 85, 331-334
82. Xie, K., Dong, Z., and Fidler, I. J. (1996) Activation of nitric oxide synthase gene for inhibition of cancer metastasis. J. Leukoc. Biol. 59, 797-803
83. Edwards, P., Cendan, J. C., Topping, D. B., Moldawer, L. L., MacKay, S., Copeland, E. M., III, and Lind, S. (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
84. Graeber, T. G., Osmanian, C., Jacks, T., Housman, D. E., Koch, C. J., Lowe, S. W., and Giaccia, A. J. (1996) Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumours. Nature (London) 379, 88-91
85. Takahashi, Y., Kitadai, Y., Bucana, C. D., Cleary, K. R., and Ellis, L. M. (1995) Expression of vascular endothelial growth factor and its receptor, KDR, correlates with vascularity, metastasis, and proliferation of human colon cancer. Cancer Res. 55, 3964-3968
86. Hanahan, D., and Folkman, J. (1996) Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 86, 353-364
87. Kieser, A., Weich, H. A., Brandner, G., Marme, D., and Kolch, W. (1994) Mutant p53 potentiates protein kinase C induction of vascular endothelial growth factor expression. Oncogene 9, 963-969
88. Aguilar, F., Hussain, S. P., and Cerutti, P. (1993) Aflatoxin B1 induces the transversion of G to T in codon 249 of the tumor suppressor gene in human hepatocytes. Proc. Natl. Acad. Sci. USA 90, 8586-8590
89. Wang, X. W., Forrester, K., Yeh, H., Feitelson, M. A., Gu, J. R., and Harris, C. C. (1994) Hepatitis B virus X protein inhibits p53 sequence-specific DNA binding, transcriptional activity, and association with transcription factor ERCC3. Proc. Natl. Acad. Sci. USA 91, 2230-2234