Abstract
Copper (Cu) metabolism is altered in rats fed diets high in molybdenum (Mo) and low in Cu. This 10-week study was carried out to examine the effects of supplemental Mo (7.5–240 μg/g diet) on male Sprague–Dawley rats fed diets adequate in Cu (5 μg/g diet) and to determine the susceptibility of Mo-treated animals to the environmental pollutant 3,3′,4,4′-tetrabromobiphenyl (TBB). After 7 weeks of dietary treatment, half of the rats in each group received a single IP injection of TBB (150 μM/kg bw), while the other half received the corn oil vehicle. Rats sacrificed at 10 weeks showed no effects of Mo on growth, feed efficiency, or selected organ or tissue weights. Dose-dependent effects on plasma Mo (0–5.1 μg/mL), plasma Cu (0.95–0.20 μg/mL), and bone Cu (3.4–10 μg/g) in control through the high dose were found. Cu sequestration in the bone of Mo-treated rats is a new finding. TBB treatment resulted in dramatic weight loss and loss of absolute organ mass. Relative organ weights were increased, except for the thymus. TBB altered the concentrations of certain amino acids. Compared to control rats, this polybrominated biphenyl congener significantly decreased plasma Cu and ceruloplasmin at higher concentrations of dietary Mo and promoted the process of plasma Cu decrease by Mo, suggesting a combined effect.
Similar content being viewed by others
References
Arrington LR, Davis GK (1953) Molybdenum toxicity in the rabbit. J Nutr 51:295–304
Arthington JD, Corah LR, Blecha F (1996) The effect of molybdenum-induced copper deficiency on acute-phase protein concentrations, superoxide dismutase activity, leukocyte numbers, and lymphocyte proliferation in beef heifers inoculated with bovine herpesvirus-1. J Anim Sci 74:211–217
Badsha K, Eduljee G, Scudamore N (1986) Environmental monitoring for PCB and trace metals in the vicinity of a chemical waste disposal facility - III. Chemosphere 15:947–957
Bagnoli F, Bianchi A, Ceccarini A, Fuoco R, Giannarelli S (2005) Trace metals and organic pollutants in treated and untreated residues from urban solid waste incinerators. Microchem J 79:291–297
Barber EF, Cousins RJ (1988) Interleukin-1—stimulated induction of ceruloplasmin synthesis in normal and copper-deficient rats. J Nutr 118:375–381
Bompart G, Pecher C, Prevot D, Girolami JP (1990) Mild renal failure induced by subchronic exposure to molybdenum: urinary kallikrein excretion as a marker of distal tubular effect. Toxicol Lett 52:293–300
Brewer GJ (2008) The risks of free copper in the body and the development of useful anticopper drugs. Curr Opin Clin Nutr Metab Care 11:727–732
Denko CW (1979) Protective role of ceruloplasmin in inflammation. Agents Actions 9:333–336
Deosthale YG, Gopalan C (1974) The effect of molybdenum levels in sorghum (Sorghum vulgare Pers.) on uric acid and copper excretion in man. Br J Nutr 31:351–355
Dowdy RP, Matrone G (1968) Copper-molybdenum interaction in sheep and chicks. J Nutr 95:191–196
Exhizen H, Ishizaki T, Oda T (1990) Amino acid metabolism in liver failure: its etiologic role in hepatic encephalopathy. In: Yoshida A, Naito H, Niiyama Y, Suzuki T (eds) Nutrition: proteins and amino acids. Japan Sci. Soc. Press, Tokyo, pp 233–243
Fu J, Zhou Q, Liu J, Liu W, Wang T, Zhang Q, Jiang G (2008) High levels of heavy metals in rice (Oryza sativa L.) from a typical E-waste recycling area in southeast China and its potential risk to human health. Chemosphere 71:1269–1275
Geiger T, Andus T, Klapproth J, Hirano T, Kishimoto T, Heinrich PC (1988) Induction of rat acute-phase proteins by interleukin 6 in vivo. Eur J Immunol 18:717–721
Gengelbach GP, Ward JD, Spears JW (1994) Effect of dietary copper, iron, and molybdenum on growth and copper status of beef cows and calves. J Anim Sci 72:2722–2727
Hoefler F, Melzer H, Moeckel HJ, Robertson LW, Anklam E (1988) Relationship between liquid and gas chromatographic retention behavior and calculated molecular surface area of selected polyhalogenated biphenyls. J Agric Food Chem 36:961–965
Humphries WR, Phillippo M, Young BW, Bremner I (1983) The influence of dietary iron and molybdenum on copper metabolism in calves. Br J Nutr 49:77–86
Jeter MA, Davis GK (1954) The effect of dietary molybdenum upon growth, hemoglobin, reproduction and lactation of rats. J Nutr 54:215–220
Jones PH, de Gerlache J, Marti E, Mischer G, Scherrer M, Bontinck WJ, Niessen HJ (1993) The global exposure of man to dioxins: a perspective on industrial waste incineration. Chemosphere 26:1491–1497
Lai I, Chai Y, Simmons D, Luthe G, Coleman MC, Spitz D, Haschek WM, Ludewig G, Robertson LW (2010) Acute toxicity of 3,3′,4,4′,5-pentachlorobiphenyl (PCB 126) in male Sprague–Dawley rats: effects on hepatic oxidative stress, glutathione and metals status. Environ Int 36:918–923
Lai IK, Chai Y, Simmons D, Watson WH, Tan R, Haschek WM, Wang K, Wang B, Ludewig G, Robertson LW (2011) Dietary selenium as a modulator of PCB 126-induced hepatotoxicity in male Sprague-Dawley rats. Toxicol Sci 124:202–214
Largeron M (2011) Amine oxidases of the quinoproteins family: their implication in the metabolic oxidation of xenobiotics. Ann Pharm Fr 69:53–61
Leary SC, Winge DR, Cobine PA (2009) “Pulling the plug” on cellular copper: the role of mitochondria in copper export. Biochim Biophys Acta 1793:146–153
Linder MC, Hazegh-Azam M (1996) Copper biochemistry and molecular biology. Am J Clin Nutr 63:797S–811S
Lloyd OL, Lloyd MM, Williams FL, McKenzie A, Hay A (1991) Toxicity from ragwort and fat cow syndrome, or from industrial chemicals: the value of epidemiological analysis for interpreting clinico-pathological findings. Sci Total Environ 106:83–96
Luna LG (1968) Manual of histologic staining methods of the Armed Forces Institute of Pathology, 3rd edn. McGraw-Hill, New York
Manis J, Kim G (1979) Stimulation of iron absorption by polychlorinated aromatic hydrocarbons. Am J Physiol 236:E763–E768
McClain C, Soutor C, Zieve L (1980) Zinc deficiency: a complication of Crohn’s disease. Gastroenterology 78:272–279
Milne DB, Johnson PE (1993) Assessment of copper status: effect of age and gender on reference ranges in healthy adults. Clin Chem 39:883–887
Nederbragt H (1980) The influence of molybdenum on the copper metabolism of the rat at different Cu levels of the diet. Br J Nutr 43:329–338
Nishimura N, Miyabara Y, Suzuki JS, Sato M, Aoki Y, Satoh M, Yonemoto J, Tohyama C (2001) Induction of metallothionein in the livers of female Sprague-Dawley rats treated with 2,3,7,8-tetrachlorodibenzo-p-dioxin. Life Sci 69:1291–1303
Ramadori G, Sipe JD, Dinarello CA, Mizel SB, Colten HR (1985) Pretranslational modulation of acute phase hepatic protein synthesis by murine recombinant interleukin 1 (IL-1) and purified human IL-1. J Exp Med 162:930–942
Robertson LW, Andres JL, Safe SH, Lovering SL (1983) Toxicity of 3,3′,4,4′- and 2,2′,5,5′-tetrabromobiphenyl: correlation of activity with aryl hydrocarbon hydroxylase induction and lack of protection by antioxidants. J Toxicol Environ Health 11:81–91
Robertson LW, Parkinson A, Bandiera S, Lambert I, Merrill J, Safe SH (1984) PCBs and PBBs: biologic and toxic effects on C57BL/6 J and DBA/2 J inbred mice. Toxicology 31:191–206
Schmidt J, McClain CJ (1991) Separation of o-phthalaldehyde—mercaptoethanol derivatives of amino acids from blood plasma on reversed-phase Nova-Pak C18 cartridges. J Chromatogr B: Biomed Sci Appl 568:207–211
Schmidt J, Marsano LS, McClain CJ (1990) Plasma amino acid profile in alcoholic hepatitis. FASEB J 4:A364
Schwarz G, Mendel RR, Ribbe MW (2009) Molybdenum cofactors, enzymes and pathways. Nature 460:839–847
Stuart SMA, Johnson PE, Hamaker B, Kirleis A (1987) Absorption of zinc and iron by rats fed meals containing sorghum food products. J Cereal Sci 6:81–90
Sunderman FW Jr, Nomoto S (1970) Measurement of human serum ceruloplasmin by its p-phenylenediamine oxidase activity. Clin Chem 16:903–910
Suttle NF (1974) Recent studies of the copper-molybdenum antagonism. Proc Nutr Soc 33:299–305
Thompson SWHR (1966) Selected histochemical and histopathological methods. Charles C. Thomas, Springfield
Ward JD, Spears JW (1997) Long-term effects of consumption of low-copper diets with or without supplemental molybdenum on copper status, performance, and carcass characteristics of cattle. J Anim Sci 75:3057–3065
Williams FLR, Lloyd OL, Lloyd MM (1988) Animal and human disease around a site with two incinerators: a review. Proc ICMR Sem 8:475–483
Zhao GF, Wang ZJ (2009) Dietary intake of PHAHs and cancer risk evaluation for residents living in the e-waste disassembly sites. Huan Jing Ke Xue 30:2414–2418
Zhao G, Wang Z, Dong MH, Rao K, Luo J, Wang D, Zha J, Huang S, Xu Y, Ma M (2008) PBBs, PBDEs, and PCBs levels in hair of residents around e-waste disassembly sites in Zhejiang Province, China, and their potential sources. Sci Total Environ 397:46–57
Zhao G, Wang Z, Zhou H, Zhao Q (2009) Burdens of PBBs, PBDEs, and PCBs in tissues of the cancer patients in the e-waste disassembly sites in Zhejiang, China. Sci Total Environ 407:4831–4837
Acknowledgments
The authors thank William Klaren for the helpful discussion and valuable suggestions. The authors also thank Dr. Izabela Kania-Korwel for independently determining the purity of TBB.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Philippe Garrigues
Farrel R. Robinson passed away prior to the publication of this study.
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(DOC 205 kb)
Rights and permissions
About this article
Cite this article
Salman, K.N., Stuart, M.A., Schmidt, J. et al. The effects of 3,3′,4,4′-tetrabromobiphenyl on rats fed diets containing a constant level of copper and varying levels of molybdenum. Environ Sci Pollut Res 21, 6400–6409 (2014). https://doi.org/10.1007/s11356-013-1638-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-013-1638-5