Exposure to Pb, Cd, and As mixtures potentiates the production of oxidative stress precursors: 30-day, 90-day, and 180-day drinking water studies in rats

Toxicology and Applied Pharmacology

Volumn 254, Issue 2, 2011, Pages 154-166

  Whittaker, Margaret H ^a   Wang, Gensheng ^a,c   Chen, Xue Qing ^a   Lipsky, Michael ^a   Smith, Donald ^b   Gwiazda, Roberto ^b   Fowler, Bruce A ^a,d  

^a UNIVERSITY OF MARYLAND   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c LOVELACE RESPIRATORY RESEARCH INSTITUTE   (United States)

^d AGENCY FOR TOXIC SUBSTANCES AND DISEASE REGISTRY   (United States)

Author keywords

(Pb)(Cd)(As); Chemical interactions; Chemical mixtures; Drinking water; Oxidative stress; Risk assessment

Indexed keywords

AMINOLEVULINIC ACID; ARSENIC; CADMIUM; CARBONYL DERIVATIVE; COPPER; DRINKING WATER; IRON; LEAD; PORPHOBILINOGEN SYNTHASE; PROTOPORPHYRIN ZINC; TRACE ELEMENT;

ANIMAL EXPERIMENT; CHEMICAL INTERACTION; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; ENZYME ACTIVITY; EXPERIMENTAL DESIGN; FACTORIAL DESIGN; HEALTH HAZARD; HEMATOCRIT; KIDNEY; MALE; NONHUMAN; OXIDATIVE STRESS; RAT; REVIEW; STATISTICAL SIGNIFICANCE;

ANIMALS; ARSENIC; CADMIUM; LEAD; MALE; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY; TIME FACTORS; TISSUE DISTRIBUTION; WATER SUPPLY;

RATTUS;

EID: 79959925197     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2010.10.025     Document Type: Review

References (84)

1. Abdulla M., Haeger-Aronson B. Antagonistic effect of zinc in relatively high concentration on inhibition of ALA-dehydratase activity by heavy metals in vitro. Int. Res. Commun. Syst. 1973, 73078.
2. Agency for Toxic Substances and Disease Registry (ATSDR) Guidance Manual for the Assessment of Joint Toxic Action of Chemical Mixtures http://www.atsdr.cdc.gov/interactionprofiles/ipga.html.
3. Agency for Toxic Substances and Disease Registry (ATSDR) Guidance Manual for the Joint Toxic Action of Chemical Mixtures http://www.atsdr.cdc.gov/interactionprofiles/ipga.html.
4. Ahamed M., Siddiqui M.K.J. Low level lead exposure and oxidative stress: current opinions. Clin. Chim. Acta 2007, 383:57-64.
5. Baskin S.I., Kuhar K.P., Uricchio F.J., Harper G.R. The effect of age on five ions of the kidney in the Fischer 344 rat. Reprod. Nutr. Dev. 1981, 21:689-694.
6. Bellinger D.C. Lead. Pediatrics 2004, 113:1016-1022.
7. Boobis A.R. The future of mixture toxicology. Toxicology 2007, 240:129-153.
8. Bottomley S.S. Porphyrin and iron metabolism in sideroblastic anemia. Semin. Hematol. 1977, 14:169-185.
9. Bottomley S.S., Muller-Eberhard U. Pathophysiology of heme synthesis. Semin. Hematol. 1988, 25:282-302.
10. Boyle, R., 1661. The Sceptical Chymist. Reprint of second ed. The Classics of Science Library, New York.
11. Buchet J.P., Roels H., Hubermont G., Lauwerys R. Effect of lead on some parameters of the heme biosynthetic pathway in rat tissues in vivo. Toxicology 1976, 6:21-34.
12. Caldwell B.S. Chronic myeloproliferative disorders. Clinical Hematology and Fundamentals of Hemostasis 1997, 375-403. F.A. Davis & Company, Philadelphia. D.M. Harmening (Ed.).
13. Canfield R.L., Henderson C.R., Cory-Slechta D.A., Cox C., Jusko T.A., Lanphear B.P. Intellectual impairment in children with blood lead concentrations below 10microg per deciliter. N Engl J. Med. 2003, 348:1517-1526.
14. Cerklewski F.L., Forbes R.M. Influence of dietary copper on lead toxicity in the young male rat. J. Nutr. 1977, 107:143-146.
15. Chiodo L.M., Jacobson S.W., Jacobson J.L. Neurodevelopmental effects of postnatal lead exposure at very low levels. Neurotoxicol. Teratol. 2004, 26:359-371.
16. Chiodo L.M., Covington C., Sokol R.J., Hannigan J.H., Jannise J., Ager J., Greenwald M., Delaney-Black V. Blood lead levels and specific attention effects in young children. Neurotoxicol. Teratol. 2007, 29(5):538-546.
17. Christison R. Of compound poisoning. Chapter 17. A Treatise on Poisons: In Relation to Medical Jurisprudence, Physiology, and the Practice of Physic 1845, 970-974. Stark and Company, London. fourth ed.
18. Conner E.A., Yamauchi H., Fowler B.A. Alterations in the heme biosynthetic pathway from the III-V semiconductor metal, indium arsenide (InAs). Chem. Biol. Interact. 1995, 96:273-285.
19. Conover W.J., Iman R.I. Rank transformations as a bridge between parametric and nonparametric statistics. Am. Stat. 1981, 35:124-129.
20. Dailey H.A. Enzymes of heme biosynthesis. J. Biol. Inorg. Chem. 1997, 2:411-417.
21. Dalton J.T., Yates C.R., Yin D., Straughn A., Marcus S.L., Golub A.L., Meyer M.C. Clinical pharmacokinetics of 5-aminolevulinic acid in health volunteers and patients at high risk for recurrent bladder cancer. J. Pharmacol. Exp. Ther. 2002, 301(2):507-512.
22. Davis J.R., Avram M.J. A comparison of the stimulatory effects of cadmium and zinc on normal and lead-inhibited human erythrocytic delta-aminolevulinic acid dehydratase activity in vitro. Toxicol. Appl. Pharmacol. 1978, 44:181-190.
23. De Rosa C.T., Hansen H., Wilbur S.B., Pohl H.R., Selene C.H., Cou J., Durkin P.R., Fay M., Hertzberg R.C., Mumtaz M.M. Weight of evidence of assessment of chemical interactions: further guidance. Impact of Hazardous Chemicals on Public Health, Policy, and Service 2002, 403-416. International Toxicology Books, Princeton.
24. Feron V.J., Groten J.P. Toxicological evaluation of chemical mixtures. Food Chem. Toxicol. 2002, 40:825-839.
25. Flora S.J., Kumar P., Kannan G.M., Rai G.P. Acute oral gallium arsenide exposure and changes in certain hematological, hepatic, renal and immunological indices at different time intervals in male Wistar rats. Toxicol. Lett. 1998, 94:103-113.
26. Flora S.J., Kannan G.M., Pant B.P., Jaiswal D.K. Combined administration of oxalic acid, succimer and its analogue for the reversal of gallium arsenide-induced oxidative stress in rats. Arch. Toxicol. 2002, 76:269-276.
27. Fujita H. Measurement of 1-aminolevulinate dehydratase activity. Current Protocols in Toxicology. Unit 8.6 1999, 8.6.1-8.6.11. John Wiley & Sons, New York. L.G. Costa, E. Hodgson, D.A. Lawrence, D.J. Reed (Eds.).
28. Goering P.L., Fowler B.A. Metal constitution of metallothionein influences inhibition of delta-aminolevulinic acid dehydratase (porphobilinogen synthase) by lead. Biochem. J. 1987, 245:339-345.
29. Goering P.L., Maronpot R.R., Fowler B.A. Effect of intratracheal gallium arsenide administration on delta-aminolevulinic acid dehydratase in rats: relationship to urinary excretion of aminolevulinic acid. Toxicol. Appl. Pharmacol. 1988, 92:179-193.
30. Groten J.P. Mixtures and interactions. Food Chem. Toxicol. 2000, 38:S65-S71.
31. Gupta G.S., Singh J., Parkash P. Renal toxicity after oral administration of lead acetate during pre- and post-implantation periods: effects on trace metal composition, metallo-enzymes and glutathione. Pharmacol. Toxicol. 1995, 76:206-211.
32. Henderson B.R., Seiser C., Kuhn L.C. Characterization of a second RNA-binding protein in rodents with specificity for iron-responsive elements. J. Biol. Chem. 1993, 268:27327-27334.
33. Hiraku Y., Kawanishi S. Mechanism of oxidative DNA damage induced by aminolevulinic acid in the presence of copper ion. Cancer Res. 1996, 56:1786-1793.
34. Hopenhayn-Rich C., Smith A.H., Goeden H.M. Human studies do not support the methylation threshold hypothesis for the toxicity of inorganic arsenic. Environ. Res. 1993, 60:161-177.
35. Jadhav S.H., Sarkar S.N., Patil R.D., Tripathi H.C. Effects of subchronic exposure via drinking water to a mixture of eight-water-contaminating metals: a biochemical and histopathological study in male rats. Arch. Environ. Contam. Toxicol. 2007, 53:667-677.
36. Järup L. Cadmium overload and toxicity. Nephrol. Dial. Transplant. 2002, 17:35-39.
37. Kannan G.M., Tripathi N., Dube S.N., Gupta M., Flora S.J. Toxic effects of arsenic (III) on some hematopoeitic and central nervous system variables in rats and guinea pigs. J. Toxicol. Clin. Toxicol. 2001, 39:675-682.
38. Klimczak J., Wisniewska-Knypl J.M., Kolakowski J. Stimulation of lipid peroxidation and heme oxygenase activity with inhibition of cytochrome P-450 monooxygenase in the liver of rats repeatedly exposed to cadmium. Toxicology 1984, 32:267-276.
39. Lalioti V., Muruais G., Tsuchiya Y., Pulido D., Sandoval I.V. Molecular mechanisms of copper homeostasis. Front Biosci. 2009, 14:4878-4903.
40. Leclair S.J. Iron metabolism and hypochromic anemias. Clinical Hematology and Fundamentals of Hemostatis 1997, 97-115. F.A. Davis & Company, Philadelphia. third ed. D.M. Harmening (Ed.).
41. Lehman E.L. Nonparametrics: Statistical Methods Based on Ranks 1977, Holden-Day, San Francisco, 94 pp.
42. Lima-Hermes M., Pereira B., Bechara E.J.H. Are free radicals involved in lead poisoning?. Xenobiotica 1991, 21:1085-1090.
43. Liu F., Jan K. DNA damage in arsenite- and cadmium-treated bovine aortic endothelial cells. Free Radic. Biol. Med. 2000, 28:55-63.
44. Mahaffey K.R., Capar S.G., Gladen B., Fowler B.A. Concurrent exposure to lead, cadmium and arsenic: effects on toxicity and tissue metal concentrations in the rat. J. Lab. Clin. Med. 1981, 98:463-481.
45. Miller G.W., Schenellmann R.G. Biochemical mechanisms of proximal tubule cellular death. Comprehensive Toxicology 1997, 7:263-277. Elsevier Science, New York. A.J. Gandolfi (Ed.).
46. Min M.O., Singer L.T., Kirchner H.L., Minnes S., Short E., Hussain Z., Nelson S. Cognitive development and low-level lead exposure in poly-drug exposed children. Neurotoxicol. Teratol. 2009, 31:225-231.
47. Mitchell R.A., Drake J.E., Wittlin L.A., Rejent T.A. Erythrocyte porphobilinogen synthase (delta aminolevulinic acid dehydratase) activity: a reliable and quantitative indicator or lead exposure in humans. Clin. Chem. 1978, 23:105-111.
48. Monteiro H.P., Abdalla D.S.P., Faljoni-Alario A., Bechara E. Generation of active oxygen species during coupled autooxidation of oxyhemoglobin and aminolevulinic acid. Biochem. Biophys. Acta 1986, 881:100-106.
49. Monteiro H.P., Abdalla D.S.P., Augusto O., Bechara E.J.H. Free radical generation during aminolevulinic acid autoxidation: induction by hemoglobin and connections with porphyrinopathies. Arch. Biochem. Biophys. 1989, 271:206-216.
50. Mumtaz M.M., Poirier K.A., Colman J.T. Risk assessment for chemical mixtures: fine-tuning the hazard index approach. Impact of Hazardous Chemicals on Public Health, Policy, and Service 2002, 417-432. International Toxicology Books, New Jersey. C.T. De Rosa, J.S. Holler, M.A. Mehlman (Eds.).
51. Newill V.A. Keynote address: significance of risk assessment in the management of environmental exposures of chemical mixtures. Toxicol. Ind. Health 1989, 5:635.
52. Nicol S.L., Harmening D.M., Green R. Hemolytic anemias: extracorpuscular defects. Clinical Hematology and Fundamentals of Hemostatis third ed 1997, 221-243. Davis & Company, Philadelphia. D.M. Harmening (Ed.).
53. Oskarsson A., Fowler B.A. Effects of lead on the heme biosynthetic pathway in rat kidney. Exp. Mol. Pathol. 1985, 43:409-417.
54. Oteiza P.I., Adonaylo V.N., Keen C.L. Cadmium-induced testes oxidative damage in rats can be influenced by dietary zinc intake. Toxicology 1999, 13:13-22.
55. Petrovi M., Gonzalez S., Barceló D. Analysis and removal of emerging contaminants in wastewater and drinking water. Trends Anal. Chem. 2003, 22(10):685-696.
56. Pratt J.W. Robustness of some procedures for the two-sample location problem. J. Am. Stat. Assoc. 1964, 59:665-680.
57. Reed D.J. The glutathione pathway. Current Protocols in Toxicology 2001, 6.0.1-6.1.8. John Wiley & Sons, New York, Chapter 6. L.G. Costa, E. Hodgson, D.A. Lawrence, D.J. Reed (Eds.).
58. Reznick A.Z., Packer L. Oxidative damage to proteins: spectrophotometric method for carbonyl assay. Meth. Enzymol. 1994, 233:357-363.
59. Roels H.A., Buchet J.P., Lauwerys R.R., Sonnet J. Comparison of in vivo effect of inorganic lead and cadmium on glutathione reductase system and delta-aminolevulinic acid dehydratase in human erythrocytes. Br. J. Ind. Med. 1975, 32:181-192.
60. Sandhir R., Julka D., Gill K.D. Lipoperoxidative damage on lead treatment in rat brain and its implications on membrane bound enzymes. Pharmacol. Toxicol. 1994, 74:66-71.
61. Sedlak J., Lindsey R.H. Estimation of total, protein-bound, and non-protein sulfhydryl groups in tissue with Ellman's reagent. Anal. Biochem. 1968, 25:192-205.
62. Sergejew T., Forgiarini P., Schnebli H.P. Chelator-induced iron excretion in iron-overloaded marmosets. Br. J. Hematol. 2000, 110:985-992.
63. Singh V., Ahmad S., Rao G.S. Release of aldehydic products from glutamate or deoxyuridine by delta-aminolevulinic acid in presence of copper ions. Indian J. Exp. Biol. 1996, 34:208-210.
64. Smith G.F., McCurdy W.H., Diehl H. The colorimetric determination of iron in raw and treated municipal water supplies by use of 4:7-diphenyl-1:10-phenanthroline. Analyst 1952, 77:418-422.
65. Stackelberg P.E., Furlong E.T., Meyer M.T., Zaugg S.D., Hederson A.K., Reissman D.B. Persistence of pharmaceutical compounds and other organic wastewater contaminants in a conventional drinking-water-treatment plant. Sci. Total Environ. 2004, 329(1-3):99-113.
66. Stackelberg P.E., Gibs J., Furlong E.T., Meyer M.T., Zaugg S.D., Lippincott R.L. Efficiency of conventional drinking-water-treatment processes in removal of pharmaceuticals and other organic compounds. Sci. Total Environ. 2007, 377(2-3):255-272.
67. Stohs S.J., Bagchi D. Oxidative mechanisms in the toxicity of metal ions. Free Radic. Biol. Med. 1995, 18:321-336.
68. Takeda T., Kimura M., Yokoi K., Itokawa Y. Effect of age and dietary protein level on tissue mineral levels in female rats. Biol. Trace Elem. Res. 1996, 54:55-74.
69. Teuschler L.K. Deciding which chemical mixtures risk assessment methods work best for what mixtures. Toxicol. Appl. Pharmacol. 2007, 223(2):139-147.
70. Uchino E., Tsuzuki T., Inoue K. The effects of age and sex on seven elements of Sprague-Dawley organs. Lab. Anim. 1990, 24:253-264.
71. United States Environmental Protection Agency (U.S.EPA) Guidelines for the Health Risk Assessment of Chemical Mixtures. Fed. Regist. 51, 34014-34025. 24 September 1986 http://cfpub.epa.gov/ncea/cfm/recordisplay.cfm?deid=20533.
72. United States Environmental Protection Agency (U.S.EPA) Supplementary Guidance for Conducting Health Risk Assessment of Chemical Mixtures. EPA/630/R-00/002 http://cfpub.epa.gov/ncea/raf/chem_mix.cfm.
73. United States Environmental Protection Agency (U.S.EPA) Framework for Inorganic Metals Risk Assessment (External Review Draft). U.S. Environmental Protection Agency, Washington, D.C., EPA/630/P-04/068B http://cfpub.epa.gov/ncea/raf/recordisplay.cfm?deid=88903.
74. Valko M., Morris H., Cronin M.T.D. Metals, toxicity and oxidative stress. Curr. Med. Chem. 2005, 12:1161-1208.
75. Valko M., Rhodes C.J., Moncol J., Izakovic M., Mazur M. Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem. Biol. Interact. 2006, 160:1-40.
76. Van der Vaart H.R. On the robustness of Wilcoxin's two-sample test. Quantitative Methods in Pharmacology 1961, 140-158. Interscience, New York. H. de Jonge (Ed.).
77. Wang G., Fowler B.A. Roles of biomarkers in evaluating interactions among mixtures of lead, cadmium and arsenic. Toxicol. Appl. Pharmacol. 2008, 233(1):92-99.
78. Wang G., Whittaker M.H., Lipsky M., Chen X., Fowler B.A. Six-month drinking water study to establish a LOEL for cadmium toxicity. Toxicologist 2002, 66(1S):203.
79. Wang G., Chen X., Lipsky M., Whittaker M.H., Fowler B.A. Interactions of lead, cadmium and arsenic in rat kidneys. Toxicologist 2004, 78:238. Interscience, Abstract No 1159.
80. Wareing M., Ferguson C.J., Green R., Riccardi D., Smith C.P. In vivo characterization of renal iron transport in the anaesthetized rat. J. Physiol. 2000, 524:581-586.
81. Whittaker M.H., Lipsky M., Wang G., Chen X., Fowler B.A. Chronic dose response study of lead toxicity in rats: assignment of a lowest observed effect level in a drinking water study. Toxicologist 2002, 66(1S):31.
82. Wilson M.P., Schwarzman M.R. Toward a new U.S. chemicals policy: rebuilding the foundation to advance new science, green chemistry, and environmental health. Environ. Health Perspect. 2009, 117(8). http://ehsehplp03.niehs.nih.gov/article/fetchArticle.action;jsessionid=DEDD106F12D2C86F73182BEA5A7AB90E?articleURI=info%3Adoi%2F10.1289%2Fehp.0800404.
83. Wilson E.L., Burger P.E., Dowdle E.B. Beef liver 5-aminolevulinic acid dehydratase: purification and properties. Eur. J. Biochem. 1972, 29:563-571.
84. World Health Organization (WHO) Health Effects of Combined Exposures in the Workplace. Technical report number 662 http://whqlibdoc.who.int/trs/WHO_TRS_662.pdf.