The human carcinogen aristolochic acid i is activated to form DNA adducts by human NAD(P)H:quinone oxidoreductase without the contribution of acetyltransferases or sulfotransferases

Environmental and Molecular Mutagenesis

Volumn 52, Issue 6, 2011, Pages 448-459

  Stiborová, Marie ^a   Mareîs, Jaroslav ^b   Frei, Eva ^c   Arlt, Volker M ^d   Martínek, Václav ^a   Schmeiser, Heinz H ^c  

^a CHARLES UNIVERSITY   (Czech Republic)

^b UNIVERSITY HOSPITAL MOTOL   (Czech Republic)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^d INSTITUTE OF CANCER RESEARCH   (United Kingdom)

Author keywords

Acetyltransferase; Aristolochic acid; DNA adducts; Molecular modeling; NAD(P)H:quinone oxidoreductase; Sulfotransferase

Indexed keywords

ACYLTRANSFERASE; ARISTOLOCHIC ACID; AROMATIC NITRO COMPOUND; CARBOXYL GROUP; HYDROXAMIC ACID; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE); SILICON; SULFOTRANSFERASE;

CARCINOGENICITY; CHEMICAL REACTION; DNA ADDUCT; ELECTRON TRANSPORT; ENZYME ACTIVE SITE; ENZYME BINDING; HUMAN; LIVER CYTOSOL; METABOLIC ACTIVATION; MOLECULAR DOCKING; PROTEIN INTERACTION; REDUCTION; REVIEW; UROTHELIUM;

ACETYLTRANSFERASES; ARISTOLOCHIC ACIDS; DNA ADDUCTS; HUMANS; MOLECULAR STRUCTURE; NAD(P)H DEHYDROGENASE (QUINONE); SULFOTRANSFERASES;

EID: 79955436820     PISSN: 08936692     EISSN: 10982280     Source Type: Journal    
DOI: 10.1002/em.20642     Document Type: Review

References (74)

1. Anusevicius Z, Sarlauskas J, Cenas N. 2002. Two-electron reduction of quinones by rat liver NAD(P)H:quinone oxidoreductase: Quantitative structure-activity relationships. Arch Biochem Biophys 404: 254-262.
2. Arlt VM. 2005. 3-Nitrobenzanthrone, a potential human cancer hazard in diesel exhaust and urban air pollution: A review of the evidence. Mutagenesis 20: 399-410.
3. Arlt VM, Schmeiser HH, Pfeifer GP. 2001. Sequence-specific detection of aristolochic acid-DNA adducts in the human p53 gene by terminal transferase-dependent PCR. Carcinogenesis 22: 133-140.
4. Arlt VM, Ferluga D, Stiborova M, Pfohl-Leszkowicz A, Vukelic M, Ceovic S, Schmeiser HH, Cosyns JP. 2002a. Is aristolochic acid a risk factor for Balkan endemic nephropathy-associated urothelial cancer? Int J Cancer 101: 500-502.
5. Arlt VM, Stiborová M, Schmeiser HH. 2002b. Aristolochic acid as a probable human cancer hazard in herbal remedies: A review. Mutagenesis 17: 265-277.
6. Arlt VM, Alunni-Perret V, Quatrehomme G, Ohayon P, Albano L, Gaid H, Michiels JF, Meyrier A, Cassuto E, Wiessler M, Schmeiser HH, Cosyns JP. 2004. Aristolochic acid (AA)-DNA adduct as marker of AA exposure and risk factor for AA nephropathy-associated cancer. Int J Cancer 111: 977-980.
7. Arlt VM, Stiborova M, Henderson CJ, Osborne MR, Bieler CA, Frei E, Martinek V, Sopko B, Wolf CR, Schmeiser HH, Phillips DH. 2005. Environmental pollutant and potent mutagen 3-nitrobenzanthrone forms DNA adducts after reduction by NAD(P)H:quinone oxidoreductase and conjugation by acetyltransferases and sulfotransferases in human hepatic cytosols. Cancer Res 65: 2644-2652.
8. Arlt VM, Stiborova M, vom Brocke J, Simoes ML, Lord GM, Nortier JL, Hollstein M, Phillips DH, Schmeiser HH. 2007. Aristolochic acid mutagenesis: Molecular clues to the aetiology of Balkan endemic nephropathy-associated urothelial cancer. Carcinogenesis 28: 2253-2261.
9. Arlt VM, Zuo J, Trenz K, Roufosse CA, Lord GM, Nortier JL, Schmeiser HH, Hollstein M, Phillips DH. 2011. Gene expression changes induced by the human carcinogen aristolochic acid I in renal and hepatic tissue of mice. Int J Cancer 128: 21-32.
10. Atanasova S, von Ahsen N, Toncheva DI, Dimitrov TG, Oellerich M, Amstrong VM. 2005. Genetic polymorphism of cytochrome P450 among patients with Balkan endemic nephropathy (BEN). Clin Biochem 38: 223-228.
11. 32P-post-labelling analysis of DNA adducts formed by aristolochic acid in tissues from patients with Chinese herbs nephropathy. Carcinogenesis 18: 1063-1067.
12. Cavelier G, Amzel LM. 2001. Mechanism of NAD(P)H:quinone reductase: Ab initio studies of reduced flavin. Proteins 43: 420-432.
13. Chan W, Luo HB, Zheng Y, Cheng YK,Cai Z. 2007. Investigation of the metabolism and reductive activation of carcinogenic aristolochic acids in rats. Drug Metab Dispos 35: 66-74.
14. Chen HW, Luni A, Seifried A, Wilkens LR, Le Marchand L. 1999. Association of the NAD(P)H-quinone oxidoreductase C-609-T polymorphism with a decreased lung-cancer risk. Cancer Res 59: 3045-3048.
15. Cleland WW. 1983. Statistical analysis of the enzyme kinetic data. Methods Enzymol 63: 103-138.
16. Cosyns JP, Jadoul M, Squifflet JP, De Plaen JF, Ferluga D, van Ypersele de Strihou C. 1994. Chinese herbs nephropathy: A clue to Balkan endemic nephropathy? Kidney Int 45: 1680-1688.
17. Cosyns JP, Jadoul M, Squifflet JP, Wese FX, van Ypersele de Strihou C. 1999. Urothelial lesions in Chinese-herb nephropathy. Am J Kidney Dis 33: 1011-1017.
18. Debelle FD, Vanherweghem JL. Nortier JL. 2008. Aristolochic acid nephropathy: A worldwide problem. Kidney Int 74: 158-169.
19. Dhakshinamoorthy S, Long DJII, Jaiswal AK. 2000. Antioxidant regulation of genes enconding enzymes that detoxify xenobitoics and carcinogens. Curr Top Cell Regul 36: 201-216.
20. Ernster L. 1987. DT-diaphorase: A historical review. Chem Scr A 27: 1-13.
21. Faig M, Bianchet MA, Talalay P, Chen S, Winski S, Ross D, Amzel LM. 2000. Structures of recombinant human and mouse NAD(P)H:quinone oxidoreductases: Species comparison and structural changes with substrate binding and release. Proc Natl Acad Sci USA 97: 3177-3182.
22. Faig M, Bianchet MA, Winski S, Hargreaves R, Moody CJ, Hudnott AR, Ross D, Amzel LM. 2001. Structure-based development of anticancer drugs: Complexes of NAD(P)H:quinone oxidoreductase 1 with chemotherapeutic quinines. Structure 9: 659-667.
23. Feldmeyer N, Schmeiser HH, Muehlbauer KR, Belharazem D, Knyazev Y, Nedelko T, Hollstein M. 2006. Further studies with a cell immortalization assay to investigate the mutation signature of aristolochic acid in human p53 sequences. Mutat Res 608: 163-168.
24. Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, Cheeseman JR, Montgomery JAJr, Vreven T, Kudin KN, Burant JC, Millam JM, Iyengar SS, Tomasi J, Barone V, Mennucci B, Cossi M, Scalmani G, Rega N, Petersson GA, Nakatsuji H, Hada M, Ehara M, Toyota K, Fukuda R, Hasegawa J, Ishida M, Nakajima T, Honda Y, Kitao O, Nakai H, Klene M, Li X, Knox JE, Hratchian HP, Cross JB, Bakken V, Adamo C, Jaramillo J, Gomperts R, Stratmann RE, Yazyev O, Austin AJ, Cammi R, Pomelli C, Ochterski JW, Ayala PY, Morokuma K, Voth GA, Salvador P, Dannenberg JJ, Zakrzewski VG, Dapprich S, Daniels AD, Strain MC, Farkas O, Malick DK, Rabuck AD, Raghavachari K, Foresman JB, Ortiz JV, Cui Q, Baboul AG, Clifford S, Cioslowski J, Stefanov BB, Liu G, Liashenko A, Piskorz P, Komaromi I, Martin RL, Fox DJ, Keith T, Al-Laham MA, Peng CY, Nanayakkara A, Challacombe M, Gill PMW, Johnson B, Chen W, Wong MW, Gonzalez C, Pople JA. 2003. Gaussian 03, Gaussian, Inc., Wallingford, CT.
25. Fukuzumi S, Ohkubo K, Tokuda Y, Suenobu T. 2000. Hydride transfer from 9-substituted 10-methyl-9, 10-dihydroacridines to hydride acceptors via charge-transfer complexes and sequential electron-proton-electron transfer. A negative temperature dependence of the rates. J Am Chem Soc 122: 4286-4294.
26. Glatt H. 2000. Sulfotransferases in the bioactivation of xenobiotics. Chem Biol Interact 129: 141-170.
27. Glatt H, Boeing H, Engelke CEH, Kuhlow LMA, Pabel U, Pomplun D, Teubner W, Meinl W. 2001. Human cytosolic sulphotransferases: Genetics, characteristics, toxicological aspects. Mutat Res 482: 27-40.
28. Grollman AP, Shibutani S, Moriya M, Miller F, Wu L, Moll U, Suzuki N, Fernandes A, Rosenquist T, Medverec Z, Jakovina K, Brdar B, Slade N, Turesky RJ, Goodenough AK, Rieger R, Vukelic M, Jelakovic B. 2007. Aristolochic acid and the etiology of endemic (Balkan) nephropathy. Proc Natl Acad Sci USA 104: 12129-12134.
29. Grosse Y, Baan R, Straif K, Secretan B, El Ghissassi F, Bouvard V, Benbrahim-Tallaa L, Guha N, Galichet L, Cogliano V. 2009. A review of human carcinogens-Part A: Pharmaceuticals. Lancet Oncol 10: 13-14.
30. Hein DW. 2002. Molecular genetics and function of NAT1 and NAT2: Role in aromatic amine metabolism and carcinogenesis. Mutat Res 506-507: 65-77.
31. Hein DW, Doll MA, Fretland AJ, Leff MA, Webb SJ, Xiao GH, Devanaboyina US, Nangju NA, Feng Y. 2000. Molecular genetics and epidemiology of the NAT1 and NAT2 acetylation polymorphisms. Cancer Epidemiol Biomarkers Prev 9: 29-42.
32. Huey R, Morris GM, Olson AJ, Goodsell DS. 2007. A semiempirical free energy force field with charge-based desolvation. J Comput Chem 28: 1145-1152.
33. Joseph P, Jaiswal AK, Stobbe CC, Chapman JD. 1994. The role of specific reductases in the intracellular activation and binding of 2-nitroimidazoles. Int J Radiat Oncol Biol Phys 29: 351-355.
34. Kucab JE, Phillips DH, Arlt VM. 2010. Linking environmental carcinogen exposure to TP53 mutations in human tumours using thehuman TP53 knock-in (Hupki) mouse model. FEBS J 277: 2567-2583.
35. Lai MN, Wang SM, Chen PC, Chen YY, Wang JD. 2010. Population-based case-control study of Chinese herbal products containing aristolochic acid and urinary tract cancer risk. J Natl Cancer Inst 102: 179-186.
36. Lemy A, Wissing KM, Rorive S, Zlotta A, Roumeguere T, Muniz Martinez MC, Decaestecker C, Salmon I, Abramowicz D, Vanherweghem JL, Nortier J. 2008. Late onset of bladder urothelial carcinoma after kidney transplantation for end-stage aristolochic acid nephropathy: A case series with 15-year follow-up. Am J Kidney Dis 51: 471-477.
37. Li R, Bianchet MA, Talalay P, Amzel LM. 1995. The three-dimensional structure of NAD(P)H:quinone reductase, a flavoprotein involved in cancer chemoprotection and chemotherapy: Mechanism of the two-electron reduction. Proc Natl Acad Sci USA 92: 8846-8850.
38. Liu Z, Hergenhahn M, Schmeiser HH, Wogan GN, Hong A, Hollstein M. 2004. Human tumor p53 mutations are selected for in mouse embryonic fibroblasts harboring a humanized p53 gene. Proc Natl Acad Sci USA 101: 2963-1968.
39. Lo SH, Wong KS, Arlt VM, Phillips DH, Lai CK, Poon WT, Chan CK, Mo KL, Chan KW, Chan A. 2005. Detection of Herba Aristolochia Mollissemae in a patient with unexplained nephropathy. Am J Kidney Dis 45: 407-410.
40. Long DJII, Jaiswal AK. 2000. NRH:Quinone oxidoreductase2 (NQO2). Chem-Biol Interact 129: 99-112.
41. Lord GM, Cook T, Arlt VM, Schmeiser HH, Williams G, Pusey CD. 2001. Urothelial malignant disease and Chinese herbal nephropathy. Lancet 358: 1515-1516.
42. Lord GM, Hollstein M, Arlt VM, Roufosse C, Pusey CD, Cook T, Schmeiser HH. 2004. DNA adducts and p53 mutations in a patient with aristolochic acid-associated nephropathy. Am J Kidney Dis 43: e11-e17.
43. Martinez MC, Nortier J, Vereerstraeten P, Vanherweghem JL. 2002. Progression rate of Chinese herb nephropathy: Impact of Aristolochia fangchi ingested dose. Nephrol Dial Transpl 17: 408-412.
44. Meinl W, Pabel U, Osterloh-Quitroz H, Hengstler JG, Glatt H. 2006. Human sulphotransferases are involved in the activation of aristolochic acids and are expressed in renal target tissue. Int J Cancer 118: 1090-1097.
45. Miseviciene L, Anusevicius Z, Sarlauskas J, Cenas N. 2006. Reduction of nitroaromatic compounds by NAD(P)H:quinone oxidoreductase (NQO1): The role of electron-accepting potency and structural parameters in the substrate specificity. Acta Biochim Pol 53: 569-576.
46. Nedelko T, Arlt VM, Phillips DH, Hollstein M. 2009. TP53 mutation signature supports involvement of aristolochic acid in the aetiology of endemic nephropathy-associated tumours. Int J Cancer 124: 987-990.
47. Nortier JL, Martinez MC, Schmeiser HH, Arlt VM, Bieler CA, Petein M, Depierreux MF, De Pauw L, Abramowicz D, Vereerstraeten P, Vanherweghem JL. 2000. Urothelial carcinoma associated with the use of a Chinese herb (Aristolochia fangchi). N Engl J Med 342: 1686-1692.
48. 32P-postlabelling analysis of the DNA adducts formed by aristolochic acid I, II. Carcinogenesis 11: 1627-1633.
49. 32P-postlabelling assay for DNA adducts. Nat Protoc 2: 2772-2781.
50. Riley RJ, Workman P. 1992. DT-diaphorase and cancer chemotherapy. Biochem Pharmacol 43: 1657-1669.
51. Ross D, Kepa JK, Winski SL, Beall HD, Anwar A, Siegel D. 2000. NAD(P)H:quinone oxidoreductase (NQO1): Chemoprotection, bioactivation, gene regulation and genetic polymorphisms. Chem-Biol Interact 129: 77-97.
52. Schmeiser HH, Schoepe KB, Wiessler M. 1988. DNA adduct formation of aristolochic acid I, II in vitro and in vivo. Carcinogenesis 9: 297-303.
53. Schmeiser HH, Bieler CA, Wiessler M, van Ypersele de Strihou C, Cosyns JP. 1996. Detection of DNA adducts formed by aristolochic acid in renal tissue from patients with Chinese herbs nephropathy. Cancer Res 56: 2025-2028.
54. 32P-post-labeling: Evidence for reductive activation by peroxidases. Carcinogenesis 18: 1055-1062.
55. Schmeiser HH, Stiborová M, Arlt VM. 2009. Chemical and molecular basis of the carcinogenicity of Aristolochia plants. Curr Opin Drug Discov Dev 12: 141-148.
56. Schulz WA, Krummeck A, Rosinger I, Eickelman P, Neuhaus C, Ebert T, Schmitz-Drager BJ, Sies H. 1997. Increased frequency of a null-allele for NAD(P)H-quinone oxidoreductase in patients with urological malignancies. Pharmacogenetics 7: 235-239.
57. Smith G, Stanley LA, Sim E, Strange RC, Wolf R. 1995. Metabolic polymorphism and cancer susceptibility. Cancer Surveys 25: 27-65.
58. 32P-postlabelling analysis using different chromatographic procedures. Carcinogenesis 15: 1187-1192.
59. 32P-postlabeling analysis of DNA adduct formation. Mutat Res 493: 153-164.
60. Stiborová M, Frei E, Hájek M, Schmeiser HH. 2001b. Carcinogenic and nephrotoxic aristolochic acids upon activation by NADPH:cytochrome P450 reductase form adducts found in DNA of patients with Chinese herbs nephropathy. Gen Physiol Biophys 20: 375-392.
61. Stiborová M, Frei E, Wiessler M, Schmeiser HH. 2001c. Human enzymes involved in the metabolic activation of carcinogenic aristolochic acids: Evidence for reductive activation by cytochrome P450 1A1 and 1A2. Chem Res Toxicol 14: 1128-1137.
62. Stiborová M, Hájek M, Vošmiková H, Frei E, Schmeiser HH. 2001d. Isolation of DT-diaphorase [NAD(P)H dehydrogenase (quinone)] from rat liver cytosol: Identification of new enzyme substrates, carcinogenic aristolochic acids. Collect Czech Chem Commun 66: 959-972.
63. Stiborová M, Frei E, Sopko B, Wiessler, M.Schmeiser H.H. 2002. Carcinogenic aristolochic acids upon activation by DT-diaphorase form adducts found in DNA of patients with Chinese herbs nephropathy. Carcinogenesis 23: 617-265.
64. Stiborová M, Frei E, Sopko B, Sopková K, Marková V, Laňková Kumstýřová T, Wiessler M, Schmeiser HH. 2003. Human cytosolic enzymes involved in the metabolic activation of carcinogenic aristolochic acid: Evidence for reductive activation by human NAD(P)H:quinone oxidoreductase. Carcinogenesis 24: 1695-1703.
65. Stiborová M, Frei E, Hodek P, Wiessler M, Schmeiser HH. 2005a. Human hepatic and renal microsomes, cytochromes P450 1A1/2, NADPH:cytochrome P450 reductase and prostaglandin H synthase mediate the formation of aristolochic acid-DNA adducts found in patients with urothelial cancer. Int J Cancer 113: 189-197.
66. Stiborová M, Sopko B, Hodek P, Frei E, Schmeiser HH, Hudecek J. 2005b. The binding of aristolochic acid I to the active site of human cytochromes P450 1A1 and 1A2 explains their potential to reductively activate this human carcinogen. Cancer Lett 229: 193-204.
67. Stiborová M, Frei E, Arlt VM, Schmeiser HH. 2008a. Metabolic activation of carcinogenic aristolochic acid, a risk factor for Balkan endemic nephropathy. Mutat Res 658: 55-67.
68. Stiborová M, Frei E, Schmeiser HH. 2008b. Biotransformation enzymes in development of renal injury and urothelial cancer caused by aristolochic acid. Kidney Int 73: 1209-1211.
69. Stiborová M, Martínek V, Svobodová M, Šístková J, Dvořák Z, Ulrichová J, Šimánek V, Frei E, Schmeiser HH, Phillips DH, Arlt VM. 2010. Mechanisms of the different DNA adduct forming potentials of the urban air pollutants 2-nitrobenzanthrone and carcinogenic3-nitrobenzanthrone. Chem Res Toxicol 23: 1192-1120.
70. Talalay P, Prochaska HJ. 1998. Mechanism of induction of NAD(P)H:quinone reductase. Chem Scr A 27: 61-66.
71. Toncheva DI, von Ahsen N, Atanasova SY, Dimitrov TG, Amstrong VM. 2004. Identification of NQO1 and GSTs genotype frequencies in Bulgarian patients with Balkan endemic nephropathy. J Nephrol 17: 384-389.
72. Vanherweghem JL. 1998. Misuse of herbal remedies: The case of an outbreak of terminal renal failure in Belgium (Chinese herbs nephropathy). J Altern Complement Med 4: 9-13.
73. Vanherweghem JL, Depierreux M, Tielemans C, Abramowicz D, Dratwa M, Jadoul M, Richard C, Vandervelde D, Verbeelen D, Vanhaelen-Fastre R, Vanhaelen M. 1993. Rapidly progressive interstitial renal fibrosis in young women: Association with slimming regimen including Chinese herbs. Lancet 341: 387-391.
74. Zhou Z, Fisher D, Spidel J, Greenfield J, Patson B, Fazal A, Wigal C, Moe OA, Madura JD. 2003. Kinetic and docking studies of the interaction of quinones with the quinone reductase active site. Biochemistry 42: 1985-1994.