Molecular Basis of 4‐Nitroquinoline 1‐Oxide Carcinogenesis

Japanese Journal of Cancer ResearchVolume 80, Issue 8 p. 691-697 Open Access Molecular Basis of 4-Nitroquinoline 1-Oxide Carcinogenesis Bernard Bailleul, Bernard Bailleul Unité INSERM n124, Institut de Recherches sur le Cancer tie Lille, Place de Verdun, 59045 Lille, FranceSearch for more papers by this authorPierre Daubersies, Pierre Daubersies Unité INSERM n124, Institut de Recherches sur le Cancer tie Lille, Place de Verdun, 59045 Lille, FranceSearch for more papers by this authorSylvie Galiègue-Zouitina, Sylvie Galiègue-Zouitina Unité INSERM n124, Institut de Recherches sur le Cancer tie Lille, Place de Verdun, 59045 Lille, FranceSearch for more papers by this authorMarie-Henriette Loucheux-Lefebvre, Marie-Henriette Loucheux-Lefebvre Unité INSERM n124, Institut de Recherches sur le Cancer tie Lille, Place de Verdun, 59045 Lille, FranceSearch for more papers by this author Bernard Bailleul, Bernard Bailleul Unité INSERM n124, Institut de Recherches sur le Cancer tie Lille, Place de Verdun, 59045 Lille, FranceSearch for more papers by this authorPierre Daubersies, Pierre Daubersies Unité INSERM n124, Institut de Recherches sur le Cancer tie Lille, Place de Verdun, 59045 Lille, FranceSearch for more papers by this authorSylvie Galiègue-Zouitina, Sylvie Galiègue-Zouitina Unité INSERM n124, Institut de Recherches sur le Cancer tie Lille, Place de Verdun, 59045 Lille, FranceSearch for more papers by this authorMarie-Henriette Loucheux-Lefebvre, Marie-Henriette Loucheux-Lefebvre Unité INSERM n124, Institut de Recherches sur le Cancer tie Lille, Place de Verdun, 59045 Lille, FranceSearch for more papers by this author First published: August 1989 https://doi.org/10.1111/j.1349-7006.1989.tb01698.xCitations: 51AboutSectionsPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinked InRedditWechat Abbreviations: 4NQO 4-nitroquinoline 1-oxide 4 HAQO 4-hydroxyaminoquinoline 1-oxide 4AQO 4-aminoquinoline 1-oxide Ac-4HAQO 4-acetoxyaminoquinoline 1-oxide diAc-4HAQO O, O’ 4-hydroxyaminoquinoline 1-oxide; HPLC high-performance liquid chromatograpy dGuo-C8-AQO N-(deoxyguanosin-8-yl)-4-aminoquinoline 1-oxide dGuo-N2-AQO 3-(deoxyguanosin-N2-yl)-4-aminoquinoline 1-oxide dAdo-N6-AQO 3-(deoxyadenosin-N6-yl)-4-aminoquinoline 1-oxide 3Me-4NQO 3-methyl-4-nitroquinoline 1-oxide SSBs single strand breaks REFERENCES 1 ) Nakahara , W. , Fukuoka , F. and Sugimura , T. Carcinogenic action of 4-nitroquinoline-N-oxide . Gann , 48 , 129 – 137 ( 1957 ). PubMedGoogle Scholar 2 ) Mori , K. and Yasuno , A. Induction of pulmonary tumors in mice by subcutaneous injection of 4-nitroquinoline N-oxide . Gann , 52 , 52 – 149 ( 1961 ). Google Scholar 3 ) Hayashi , Y. and Hasegawa , T. Experimental pancreatic tumor in rats after intravenous injection of 4-hydroxy-aminoquinoline 1-oxide . Gann , 62 , 329 – 330 ( 1971 ). CASPubMedWeb of Science®Google Scholar 4 ) Mori , K. Carcinoma of the glandular stomach of mice by instillation of 4-nitroquinoline 1-oxide , Gann , 58 , 389 – 393 ( 1967 ). CASPubMedWeb of Science®Google Scholar 5 ) Endo , H. , Ono , T. and Sugimura , T. Chemistry and biological actions of 4-nitroquinoline 1-oxide . Recent Results Cancer Res. , 34 , 1 – 99 ( 1971 ). CrossrefGoogle Scholar 6 ) Sugimura , T. The nitroquinolines . In “ Carcinogenesis, A Comprehensive Survey ,“ Vol. 6 , pp. 1 – 153 ( 1981 ). Raven Press , New York ). Google Scholar 7 ) Nagao , M. and Sugimura , T. Molecular biology of the carcinogen, 4-nitroquinoline 1-oxide . Adv. Cancer Res. , 23 , 131 – 169 ( 1976 ). CrossrefCASPubMedGoogle Scholar 8 ) Miller , J. A. Carcinogenesis by chemicals: an overview. G.H.A. Clowes Memorial Lecture . Cancer Res. , 30 , 559 – 576 ( 1970 ). CASPubMedWeb of Science®Google Scholar 9 ) Tada , M. and Tada , M. Main binding sites of the carcinogen, 4-nitroquinoline 1-oxide in nucleic acids . Biochim. Biophys. Acta , 454 , 558 – 566 ( 1976 ). CrossrefCASPubMedWeb of Science®Google Scholar 10 ) Ames , B. N. , Lee , F. D. and Durston , W. E. An improved bacterial test system for the detection and classification of mutagens and carcinogens . Proc. Natl. Acad. Sci. USA , 70 , 782 – 786 ( 1973 ). CrossrefCASPubMedWeb of Science®Google Scholar 11 ) Coulondre , C. and Miller , J. M. Genetic studies of the lac represser. IV Mutagenic specificity in the lac I gene of Escherichia coll J. Mol Biol. , 117 , 577 – 606 ( 1977 ). CrossrefCASPubMedWeb of Science®Google Scholar 12 ) Prakash , L. , Stewart , J. W. and Sherman , F. Specific induction of transitions and transversions of G-C base pairs by 4-nitroquinoline-1-oxide in iso-1-cytochrome c mutants of yeast . J. Mol. Biol. , 85 , 51 – 65 ( 1974 ). CrossrefCASPubMedWeb of Science®Google Scholar 13 ) Reddy , E. P. , Reynolds , R. K. , Santos , E , and Barbacid , M. A point mutation is responsible for the acquisition of transforming properties by the T24 human bladder carcinoma . Nature , 300 , 149 – 152 ( 1982 ). CrossrefCASPubMedWeb of Science®Google Scholar 14 ) Bailleul , B. , Brown , K. , Ramsden , M. , Akhurst , R. J. , Fee , F. and Balmain , A. Chemical induction of oncogene mutations and growth factor activity in mouse skin Carcinogenesis . In “ Environmental Health Perspectives ,“ ed. A. Upton , Niehs Press , North Carolina . In press . Google Scholar 15 ) Okabayashi , T. and Yoshimoto , A. Reduction of 4-nitroquinoline 1-oxide by microorganism . Chem. Pharm. Bull. , 10 , 1221 – 1226 ( 1962 ). CrossrefCASPubMedWeb of Science®Google Scholar 16 ) Shirasu , Y. Further studies on carcinogenic action of 4-hydroxyaminoquinoline 1-oxide . Gann , 54 , 487 – 495 ( 1963 ). CASPubMedWeb of Science®Google Scholar 17 ) Kato , R. , Takahashi , A. and Oshima , T. Characteristics of nitro reduction of the carcinogenic agent, 4-nitroquinoline 1-oxide . Biochem. Pharmacol. , 19 , 45 – 55 ( 1970 ). CrossrefPubMedGoogle Scholar 18 ) Sugimura , T. , Okabe , K. and Nagao , M. The metabolism of 4-nitroquinoline 1-oxide, a carcinogen. III. An enzyme catalysing the conversion of 4-nitroquinoline-1-oxide to 4-hydroxyaminoquinoline 1-oxide in rat liver and hepa-tomas . Cancer Res. , 26 , 1717 – 1721 ( 1966 ). CASPubMedWeb of Science®Google Scholar 19 ) Mori , K. , Kondo , M. , Koibuchi , E. and Hashimoto , A. Induction of lung cancer in mice by injection of 4-hydroxyaminoquinoline 1-oxide . Gann , 58 , 105 – 106 ( 1961 ). PubMedWeb of Science®Google Scholar 20 ) Mori , K. and Ohta , A. Carcinoma of the glandular stomach of mice by 4-hydroxyaminoquinoline 1-oxide . Gann , 58 , 551 – 554 ( 1967 ). CASPubMedWeb of Science®Google Scholar 21 ) Tada , M. and Tada , M. Seryl-tRNA synthetase and activation of the carcinogen 4-nitroquinoline-1-oxide . Nature , 255 , 510 – 512 ( 1975 ). CrossrefCASPubMedWeb of Science®Google Scholar 22 ) Enomoto , M. , Sato , K. , Miller , E. C. and Miller , J. A. Reactivity of the diacetyl derivative of the carcinogen 4HAQO with DNA, RNA, and other nucleophiles . Life Sci. , 7 , 1025 – 1032 ( 1968 ). CrossrefCASPubMedWeb of Science®Google Scholar 23 ) Galiègue , S. , Bailleul , B. and Loucheux-Lefebvre , M. H. Reactivity of the O,O'-diacetyl derivative of the carcinogen 4-hydroxyaminoquinoline 1-oxide with DNA. Comparison with in vivo-reacted DNA . Eur. J. Cancer , 16 , 1283 – 1287 ( 1980 ). CrossrefPubMedWeb of Science®Google Scholar 24 ) Bailleul , B. , Galiegue , S. and Loucheux-Lefebvre , M. H. Adducts from the reaction of O,O'-diacetyl or O-acetyl derivatives of the carcinogen 4-hydroxyaminoquinoline 1-oxide with purine nucleosides . Cancer Res. , 41 , 4559 – 4565 ( 1981 ). CASPubMedWeb of Science®Google Scholar 25 ) Kawazoe , Y. , Ogawa , O. and Huang , G. F. Studies on chemical carcinogens. XVII. Structure of carcinogenic 4-hydroxyaminoquinoline 1-oxide derivatives . Tetrahedron , 36 , 2833 – 2838 ( 1980 ). Google Scholar 26 ) Galiegue , S. , Bailleul , B. and Loucheux-Lefebvre , M. H. In vitro DNA reaction with an ultimate carcinogen model of 4-nitroquinoline 1-oxide: the acetoxyaminoquinoline 1-oxide. Enzymatic degradation of the modified DNA . Carcinogenesis , 4 , 249 – 254 ( 1983 ). CrossrefPubMedWeb of Science®Google Scholar 27 ) Galiègue-Zouitina , S. , Bailleul , B. and Loucheux-Lefebvre , M. H. Adducts from in vivo action of the carcinogen 4-hydroxyaminoquinoline 1-oxide in rats and from in vitro reaction of 4-acetoxyaminoquinoline 1-oxide with DNA and polynucleotides . Cancer Res. , 45 , 520 – 525 ( 1985 ). CASPubMedWeb of Science®Google Scholar 28 ) Kawazoe , Y. and Araki , M. Studies on chemical carcinogens. V. O,O'-Diacetyl-4-hydroxyaminoquinoline 1-oxide . Gann , 58 , 485 – 487 ( 1967 ). CASPubMedWeb of Science®Google Scholar 29 ) Kawazoe , Y. Chemistry of 4-nitroquinoline 1-oxide and related compounds . In “ Carcinogenesis, A Comprehensive Survey ,“ Vol. 6 . ed. T. Sugimura , pp. 1 – 24 ( 1981 ). Raven Press , New York ). Google Scholar 30 ) Kawazoe , Y. , Araki , M. , Huang , G. F. , Okamoto , T. , Tada , M , and Tada , M. Chemical structure of QAII, one of the covalently bound adducts of carcinogenic 4-nitroquinoline 1-oxide with nucleic acid bases of cellular nucleic acids . Chem. Phartn. Bull. , 23 , 3041 – 3043 ( 1975 ). CrossrefCASPubMedWeb of Science®Google Scholar 31 ) Tada , M. , Kohda , K. H. and Kawazoe , Y. Biomimetic preparation and structure determination of QG1, one of the quinoline-DNA base adducts formed in cells treated with 4 -nitroquinoline 1-oxide . Gann , 75 , 976 – 985 ( 1984 ). CASPubMedWeb of Science®Google Scholar 32 ) Galiègue-Zouitina , S. , Bailleul , B. , Ginot , Y-M. , Perly , B. , Vigny , P. and Loucheux-Lefebvre , M. H. N-2 guanyl and N-6 adenyl arylation of chicken erythrocyte DNA by the ultimate carcinogen of 4-nitroquinoline 1-oxide . Cancer Res. , 46 , 1858 – 1863 ( 1986 ). CASPubMedWeb of Science®Google Scholar 33 ) Miller , E. C. Some current perspectives on chemical carcinogens in humans and experimental animals: presidential address . Cancer Res. , 38 , 1479 – 1496 ( 1978 ). CASPubMedWeb of Science®Google Scholar 34 ) Bailleul , B. , Galiègue , S. , Demeunynck , M. , Lhomme , M. F. , Lhomme , J. and Loucheux-Lefebvre , M. H. Identification of 4-acetoxyaminoquinoline from the hydrolysis of 1-acetoxy-4-acetoxyimino- 1–4-dihydroquinoline; in vitro and in vivo properties . Chem. Biol. Interact. , 43 , 87 – 98 ( 1983 ). CrossrefCASPubMedWeb of Science®Google Scholar 35 ) Purchase , I. F. , Longstaff , E. , Ashby , J. A. , Anderson , D. , Lefevre , P. A. and Westwood , F. R. Evaluation of six short term tests for detecting organic chemical carcinogens and recommendations for their use . Nature , 264 , 624 – 627 ( 1976 ). CrossrefCASPubMedWeb of Science®Google Scholar 36 ) Edwards , S. , Fielding , S. and Waters , R. The response to DNA damage induced by 4-nitroquinoline 1-oxide or its 3-methyI derivative in xeroderma pigmentosum fibroblasts belonging to different complementation groups: evidence for different epistasis groups involved in the repair of large adducts in human DNA . Carcinogenesis , 9 , 1071 – 1075 ( 1987 ). CrossrefPubMedWeb of Science®Google Scholar 37 ) Mirzayans , R. and Waters , R. DNA damage and repair in human normal or xeroderma pigmentosum fibroblasts treated with 4-nttroquinoline 1-oxide or its 3-methyl derivative . Carcinogenesis , 2 , 1359 – 1362 ( 1981 ). CrossrefCASPubMedWeb of Science®Google Scholar 38 ) Mirzayans , R. , Paterson , M. C. and Waters , R. Defective repair of a class of 4-NQO-induced alkali-labile DNA lesions in xeroderma pigmentosum complementation group A fibroblasts . Carcinogenesis , 6 , 555 – 559 ( 1985 ). CrossrefCASPubMedWeb of Science®Google Scholar 39 ) Kohda , K , Tada , M. , Hakura , A. , Kasai , H. and Kawazoe , Y. Formation of 8-hydroxyguanine residues in DNA treated with 4-hydroxyaminoquinoline 1-oxide and its related compounds in the presence of seryl-AMP . Biochem. Biophys. Res. Commun. , 149 , 1141 – 1148 ( 1987 ). CrossrefCASPubMedWeb of Science®Google Scholar 40 ) Kohda , K. , Tada , M. , Kasai , H. , Nishimura , S. and Kawazoe , Y. Formation of 8-hydroxyguanine residues in cellular DNA exposed to the carcinogen 4-nitroquinoline 1-oxide . Biochem. Biophys. Res. Commun. , 139 , 626 – 632 ( 1986 ). CrossrefCASPubMedWeb of Science®Google Scholar 41 ) Spodheim-Maurizot , M. , Dreux , M. , Saint-Ruf , G. and Leng , M. Alkaline stability of guanosine and some of its derivatives modified by the carcinogen N-acetoxyacetyl-aminofluorene . Nucleic Acids Res. , 7 , 2347 – 2356 ( 1979 ). CrossrefCASPubMedWeb of Science®Google Scholar 42 ) Kriek , E. and Westra , J. G. Structural identification of the pyrimidine derivatives formed from N-(deoxyguanosin-8-yl)-2-aminofluorene in aqueous solution at alkaline pH . Carcinogenesis , 1 , 459 – 68 ( 1980 ). CrossrefCASPubMedWeb of Science®Google Scholar 43 ) Kadlubar , F. F , Unruh , L. E. , Beland , F. A. , Straub , K. M. and Evans , F. E. In vitro reaction of the carcinogen N-hydroxy-2-naphthylamine with DNA at the C-8 and N2 atoms of guanine and at N6 atom of adenine . Carcinogenesis , 1 , 139 – 150 ( 1980 ). CrossrefCASPubMedWeb of Science®Google Scholar 44 ) Hertzog , P. G. , Lindsay-Smith , J. R. and Garner , R. C. 4NQO-DNA Adducts and Biological Relevance Characterization of the imidazole ring-opened forms of trans- 8,9-dihydro - 8 - (7 - guanyl) - 9 - hydroxyaflatoxin B1 . Carcinogenesis , 3 , 723 – 725 ( 1982 ). CrossrefCASPubMedWeb of Science®Google Scholar 45 ) Bailleul , B. , Galiègue-Zouitina , S. , Perly , B. and Loucheux-Lefebvre , M. H. Structural identification of the purine ring-opened form of N-(deoxyguanosin-8-yl)-4-aminoquinoline 1-oxide . Carcinogenesis , 6 , 319 – 322 ( 1985 ). CrossrefCASPubMedWeb of Science®Google Scholar 46 ) Galiegue-Zouitina , S. , Bailleul , B. and Loucheux-Lefebvre , M. H. Guanyl-C8-arylamination of DNA by the ultimate carcinogen of 4-nitroquinoline 1-oxide: a spectrophoto-metric titration . Anal. Biochem. , 138 , 454 – 457 ( 1984 ). CrossrefCASPubMedWeb of Science®Google Scholar 47 ) Fuchs , R. P. P. Arylamidation and arylation by the carcinogen N-2-fluorenyl-acetamide; a sensitive and rapid chemical assay . Anal Biochem. , 91 , 663 – 673 ( 1978 ). CrossrefCASPubMedWeb of Science®Google Scholar 48 ) Walker , I. G. Alkaline sucrose sedimentation an analysis as an indicator of repair. Capability of xeroderma pigmentosum fibroblasts for repair of 4-nitroquinoline 1-oxide damage . Carcinogenesis , 2 , 691 – 695 ( 1981 ). CrossrefCASPubMedWeb of Science®Google Scholar 49 ) Bigalow , J. E. , Jacobson , B. E. and Nygaard , O. F. Metabolic reduction of 4-nitroquinoline 1-oxide and other radical-producing drugs to oxygen-reactive intermediates . Cancer Res. , 37 , 3306 – 3313 ( 1977 ). PubMedWeb of Science®Google Scholar 50 ) Walker , I. G. Lack of effect of 4-nitroquinoline 1-oxide on cellular NAD levels . Mutat. Res. , 139 , 155 – 159 ( 1984 ). CrossrefCASPubMedWeb of Science®Google Scholar 51 ) Regan , J. D. and Setlow , R. B. Two forms of repair in the DNA of human cells damaged by chemical carcinogens and mutagens . Cancel Res. , 34 , 3318 – 3325 ( 1974 ). CASPubMedWeb of Science®Google Scholar 52 ) Ikenaga , M. , Ichikawa-Ryo , H. and Kondo , S. The major cause of inactivation and mutation by 4-nitroquinoline-1-oxide in Escherichia coli: excisable 4NQO-purine adducts . J. Mol. Biol. , 92 , 341 – 356 ( 1975 ). CrossrefCASPubMedWeb of Science®Google Scholar 53 ) Kuhnlein , V. , Penhoet , E. E. and Linn , S. An altered apurinic endonuclease activity in group A and group D xeroderma pigmentosum fibroblasts . Proc. Natl. Acad. Sci. USA , 73 , 1169 – 1173 ( 1976 ). CrossrefCASPubMedWeb of Science®Google Scholar 54 ) Lindhal , T. and Anderson , A. Rate of chain breakage at apurinic sites in double-stranded deoxyribonucleic acid . Biochemistry , 11 , 3618 ( 1972 ). CrossrefPubMedWeb of Science®Google Scholar 55 ) F. J. Serres and Ashby ( ed ). “ Evaluation of Short-term Tests for Carcinogens “ ( 1981 ). Elsevier/North Holland , Amsterdam ). Google Scholar 56 ) Fuchs , R. P. P. , Schwartz , N. and Daune , M. P. Hot spots of frameshift mutations induced by the ultimate carcinogen N-acetoxy-N- 2 -acetylaminofluorene . Nature , 294 , 657 – 659 ( 1981 ). CrossrefCASPubMedWeb of Science®Google Scholar Citing Literature Volume80, Issue8August 1989Pages 691-697 ReferencesRelatedInformation