Home LiteratureArticle Details
PMID: 17620607 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Aristolochic acid and the etiology of endemic (Balkan) nephropathy.

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, Vukelić M, Jelaković B

Abstract

Endemic (Balkan) nephropathy (EN), a devastating renal disease affecting men and women living in rural areas of Bosnia, Bulgaria, Croatia, Romania, and Serbia, is characterized by its insidious onset, invariable progression to chronic renal failure and a strong association with transitional cell (urothelial) carcinoma of the upper urinary tract. Significant epidemiologic features of EN include its focal occurrence in certain villages and a familial, but not inherited, pattern of disease. Our experiments test the hypothesis that chronic dietary poisoning by aristolochic acid is responsible for EN and its associated urothelial cancer. Using (32)P-postlabeling/PAGE and authentic standards, we identified dA-aristolactam (AL) and dG-AL DNA adducts in the renal cortex of patients with EN but not in patients with other chronic renal diseases. In addition, urothelial cancer tissue was obtained from residents of endemic villages with upper urinary tract malignancies. The AmpliChip p53 microarray was then used to sequence exons 2-11 of the p53 gene where we identified 19 base substitutions. Mutations at A:T pairs accounted for 89% of all p53 mutations, with 78% of these being A:T --> T:A transversions. Our experimental results, namely, that (i) DNA adducts derived from aristolochic acid (AA) are present in renal tissues of patients with documented EN, (ii) these adducts can be detected in transitional cell cancers, and (iii) A:T --> T:A transversions dominate the p53 mutational spectrum in the upper urinary tract malignancies found in this population lead to the conclusion that dietary exposure to AA is a significant risk factor for EN and its attendant transitional cell cancer.

MeSH Terms
Aristolochic Acids/adverse effects,analysis,chemistry Balkan Nephropathy/chemically induced,etiology Carcinoma, Transitional Cell/pathology DNA Adducts/analysis,chemistry Female Humans Kidney/chemistry,pathology Male Mutation/genetics Spectrometry, Mass, Electrospray Ionization Tumor Suppressor Protein p53/genetics Urologic Neoplasms/pathology
Chemicals
Aristolochic Acids DNA Adducts Tumor Suppressor Protein p53 aristolochic acid I
Authors & Affiliations
18 authors, click to expand affiliations / ORCID
Grollman Arthur P
Laboratory of Chemical Biology, Department of Pharmacological Sciences, Stony Brook University, Stony Brook, NY 11794, USA. [email protected]
Shibutani Shinya
Moriya Masaaki
Miller Frederick
Wu Lin
Moll Ute
Suzuki Naomi
Fernandes Andrea
Rosenquist Thomas
Medverec Zvonimir
Jakovina Krunoslav
Brdar Branko
Slade Neda
Turesky Robert J
Goodenough Angela K
Rieger Robert
Vukelić Mato
Jelaković Bojan
References (35)
35 references, click to expand
  1. Mutations in the p53 tumor suppressor gene: clues to cancer etiology and molecular pathogenesis.
    Cancer Res. 1994 Sep 15;54(18):4855-78 PMID: 8069852
  2. Renal function, protein excretion, and pathology of Balkan endemic nephropathy. III. Light and electron microscopic studies.
    Kidney Int Suppl. 1991 Nov;34:S57-67 PMID: 1762337
  3. Mutations induced by carcinogenic doses of aristolochic acid in kidney of Big Blue transgenic rats.
    Toxicol Lett. 2006 Sep 10;165(3):250-6 PMID: 16764999
  4. Characteristics of proteinuria in endemic nephropathy.
    J Clin Chem Clin Biochem. 1983 Sep;21(9):569-71 PMID: 6631337
  5. 32P-post-labelling analysis of DNA adducts formed by aristolochic acid in tissues from patients with Chinese herbs nephropathy.
    Carcinogenesis. 1997 May;18(5):1063-7 PMID: 9163697
  6. Endemic nephropathy: the case for chronic poisoning by aristolochia.
    Croat Med J. 2005 Feb;46(1):116-25 PMID: 15726685
  7. Fifty years of Balkan endemic nephropathy: daunting questions, elusive answers.
    Kidney Int. 2006 Feb;69(4):644-6 PMID: 16467889
  8. Pathologic aspects of a newly described nephropathy related to the prolonged use of Chinese herbs.
    Am J Kidney Dis. 1994 Aug;24(2):172-80 PMID: 8048421
  9. Critical evaluation of environmental exposure agents suspected in the etiology of Balkan endemic nephropathy.
    Int J Occup Environ Health. 2006 Oct-Dec;12(4):369-76 PMID: 17168225
  10. Urothelial malignant disease and Chinese herbal nephropathy.
    Lancet. 2001 Nov 3;358(9292):1515-6 PMID: 11705569
  11. Etiology of Balkan endemic nephropathy and associated urothelial cancer.
    Am J Nephrol. 2006;26(1):1-11 PMID: 16391464
  12. Ochratoxin A: the continuing enigma.
    Crit Rev Toxicol. 2005 Jan;35(1):33-60 PMID: 15742902
  13. Ochratoxin A: An overview on toxicity and carcinogenicity in animals and humans.
    Mol Nutr Food Res. 2007 Jan;51(1):61-99 PMID: 17195275
  14. The etiology of Balkan endemic nephropathy: still more questions than answers.
    Environ Health Perspect. 1998 Nov;106(11):689-700 PMID: 9799184
  15. Ochratoxin A: lack of formation of covalent DNA adducts.
    Chem Res Toxicol. 2004 Feb;17(2):234-42 PMID: 14967011
  16. Aristolochic acid activates ras genes in rat tumors at deoxyadenosine residues.
    Cancer Res. 1990 Sep 1;50(17):5464-9 PMID: 2201437
  17. Activating mutations at codon 61 of the c-Ha-ras gene in thin-tissue sections of tumors induced by aristolochic acid in rats and mice.
    Cancer Lett. 1991 Aug;59(2):139-43 PMID: 1884371
  18. Perspective: ochratoxin A is not a genotoxic carcinogen.
    Chem Res Toxicol. 2005 Jul;18(7):1082-90 PMID: 16022500
  19. Is aristolochic acid a risk factor for Balkan endemic nephropathy-associated urothelial cancer?
    Int J Cancer. 2002 Oct 10;101(5):500-2 PMID: 12216081
  20. Low molecular weight proteinuria in Chinese herbs nephropathy.
    Kidney Int. 1995 Nov;48(5):1571-6 PMID: 8544416
  21. The IARC TP53 database: new online mutation analysis and recommendations to users.
    Hum Mutat. 2002 Jun;19(6):607-14 PMID: 12007217
  22. Human tumor p53 mutations are selected for in mouse embryonic fibroblasts harboring a humanized p53 gene.
    Proc Natl Acad Sci U S A. 2004 Mar 2;101(9):2963-8 PMID: 14976251
  23. THE ENDEMIC NEPHROPATHY OF SOUTH-EASTERN EUROPE.
    Bull World Health Organ. 1965;32:431-48 PMID: 14315715
  24. Quantitative determination of aristolochic acid-derived DNA adducts in rats using 32P-postlabeling/polyacrylamide gel electrophoresis analysis.
    Drug Metab Dispos. 2006 Jul;34(7):1122-7 PMID: 16611860
  25. Metabolism of ochratoxin A: absence of formation of genotoxic derivatives by human and rat enzymes.
    Chem Res Toxicol. 2001 Jan;14(1):34-45 PMID: 11170506
  26. Mutagenicity of aristolochic acid in the lambda/lacZ transgenic mouse (MutaMouse).
    Mutat Res. 2002 Mar 25;515(1-2):63-72 PMID: 11909755
  27. Novel LC-ESI/MS/MS(n) method for the characterization and quantification of 2'-deoxyguanosine adducts of the dietary carcinogen 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine by 2-D linear quadrupole ion trap mass spectrometry.
    Chem Res Toxicol. 2007 Feb;20(2):263-76 PMID: 17305409
  28. Chronic nephritis due to ingestion of lead-contaminated flour.
    Br Med J. 1958 Jan 4;1(5061):27-8 PMID: 13489301
  29. Aristolochic acid as a probable human cancer hazard in herbal remedies: a review.
    Mutagenesis. 2002 Jul;17(4):265-77 PMID: 12110620
  30. Rapidly progressive interstitial renal fibrosis in young women: association with slimming regimen including Chinese herbs.
    Lancet. 1993 Feb 13;341(8842):387-91 PMID: 8094166
  31. Urothelial lesions in Chinese-herb nephropathy.
    Am J Kidney Dis. 1999 Jun;33(6):1011-7 PMID: 10352187
  32. Further studies with a cell immortalization assay to investigate the mutation signature of aristolochic acid in human p53 sequences.
    Mutat Res. 2006 Sep 28;608(2):163-8 PMID: 16835015
  33. Chinese herbs nephropathy: a clue to Balkan endemic nephropathy?
    Kidney Int. 1994 Jun;45(6):1680-8 PMID: 7933816
  34. Aristolochic acid and 'Chinese herbs nephropathy': a review of the evidence to date.
    Drug Saf. 2003;26(1):33-48 PMID: 12495362
  35. Ochratoxin a: its cancer risk and potential for exposure.
    J Toxicol Environ Health B Crit Rev. 2006 May-Jun;9(3):265-96 PMID: 16621780
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2007-07-17
Epub
2007-00-09
Pages
12129-34
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC1913550
Subset
IM
Grants
NIEHS NIH HHS · P01 ES004068 · United States
PHS HHS · 1203-07042 · United States
NIEHS NIH HHS · ES-04068 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]