Iron deficient and manganese supplemented diets alter metals and transporters in the developing rat brain

Toxicological Sciences

Volumn 95, Issue 1, 2007, Pages 205-214

  Garcia, Stephanie J ^a   Gellein, Kristin ^b   Syversen, Tore ^b   Aschner, Michael ^c  

^a WAKE FOREST UNIVERSITY HEALTH SCIENCES   (United States)

^b NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^c VANDERBILT UNIVERSITY   (United States)

Author keywords

Brain; Development; Iron deficiency; Manganese; Metal transport; Rat

Indexed keywords

4AMINOBUTYRIC ACID; ALUMINUM; CARRIER PROTEIN; CHROMIUM; COBALT; COPPER; GLUTAMIC ACID; HEMOGLOBIN; IRON; MANGANESE; METAL; MOLYBDENUM; NATURAL RESISTANCE ASSOCIATED MACROPHAGE PROTEIN 2; NEUROTRANSMITTER; TRANSFERRIN; TRANSFERRIN RECEPTOR; VANADIUM; ZINC;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN DISEASE; BRAIN LEVEL; BREAST MILK; CONTROLLED STUDY; DIET SUPPLEMENTATION; EXPOSURE; FEMALE; HOMEOSTASIS; IRON BINDING CAPACITY; IRON BLOOD LEVEL; IRON DEFICIENCY; IRON RESTRICTION; LACTATION; NEWBORN; NONHUMAN; PERINATAL PERIOD; RAT; TRANSFERRIN BLOOD LEVEL;

AMINO ACIDS; ANIMALS; ANIMALS, NEWBORN; BODY WEIGHT; BRAIN; CATION TRANSPORT PROTEINS; DIETARY SUPPLEMENTS; FEMALE; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; HEMOGLOBINS; HOMEOSTASIS; IRON COMPOUNDS; LACTATION; MALE; MANGANESE COMPOUNDS; MEMBRANE TRANSPORT PROTEINS; METALS; ORGAN SIZE; PROTEIN BINDING; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, TRANSFERRIN; TIME FACTORS; TRANSFERRIN; UP-REGULATION;

EID: 33845657881     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfl139     Document Type: Article

References (55)

1. Agency for Toxic Substances and Disease Registry, A. (2000). Toxicological profile for manganese (Update). U.S. Department of Health and Human Services, Public Health Service, Atlanta, GA.
2. Aschner, M. (2000). Manganese in health and disease: From transport to neurotoxicity. In Handbook of Neurotoxicology (E. Massaro, Ed.), pp. 195-209. Humana Press, Totowa, NJ.
3. Aschner, M., and Aschner, J. (1991). Manganese neurotoxicity: Cellular effects and blood-brain barrier transport. Neurosci. Biobehav. Rev. 15, 333-340.
4. Aschner, M., Shanker, G., Erikson, K., Yang, J., and Mutkus, L. A. (2002). The uptake of manganese in brain endothelial cultures. Neurotoxicology 23, 165-168.
5. Aschner, M., Vrana, K. E., and Zheng, W. (1999). Manganese uptake and distribution in the central nervous system (CNS). Neurotoxicology 20, 173-180.
6. Barron, T. F., Devenyi, A. G., and Mamourian, A. C. (1994). Symptomatic manganese neurotoxicity in a patient with chronic liver disease: Correlation of clinical symptoms with MRI findings. Pediatr. Neurol. 10, 145-148.
7. Beard, J. L. (2001). Iron biology in immune function, muscle metabolism and neuronal functioning. J. Nutr. 131, 568S-580S.
8. Beard, J. L., Felt, B., Schallert, T., Burhans, M., Connor, J. R., and Georgieff, M. K. (2006). Moderate iron deficiency in infancy: Biology and behavior in young rats. Behav. Brain Res. 170, 224-232.
9. 2) to the rat brain: Toxicokinetic investigations in a unilateral nasal occlusion model. Toxicol. Appl. Pharmacol. 169, 238-248.
10. Chandra, S., and Shukla, G. (1976). Role of iron deficiency in inducing susceptibility to manganese toxicity. Arch. Toxicol. 35, 319-323.
11. Chandra, S. V., Malhotra, K. M., and Shukla, G. S. (1982). GABAergic neuro-chemistry in manganese exposed rats. Acta Pharmacol. Toxicol. 51, 456-458.
12. Chen, M. T., Yiin, S. J., Sheu, J. Y., and Huang, Y. L. (2002). Brain lipid peroxidation and changes of trace metals in rats following chronic manganese chloride exposure. J. Toxicol. Environ. Health A 65, 305-316.
13. Connor, J., Menzies, S., Burdo, J., and Boyer, P. (2001). Iron and iron management proteins in neurobiology. Pediatr. Neurol. 25, 118-129.
14. Crossgrove, J. S., Allen, D. D., Bukaveckas, B. L., Rhineheimer, S. S., and Yokel, R. A. (2003). Manganese distribution across the blood-brain barrier: I. Evidence for carrier-mediated influx of manganese citrate as well as manganese and manganese transferrin. Neurotoxicology 24, 3-13.
15. deUngria, M. Rao, R., Wobken, J. D., Luciana, M., Nelson, C. A., and Georgieff, M. K. (2000). Perinatal iron deficiency decreases cytochrome c oxidase (CytOx) activity in selected regions of neonatal rat brain. Pediatr. Res. 48, 169-176.
16. Devenyi, A., Barron, T. F., and Mamourian, A. (1994). Dystonia, hyperintense basal ganglia, and high whole blood manganese levels in Alagille's syndrome. Gastroenterology 106, 1068-1071.
17. Dorman, D. C., Struve, M. F., Vitarella, D., Byerly, F. L., Goetz, J., and Miller, R. (2000). Neurotoxicity of manganese chloride in neonatal and adult CD rat following subchronic (21-day) high-dose oral exposure. J. Appl. Toxicol. 20, 179-187.
18. Erikson, K., Jones, B., Hess, E., Zhang, Q., and Beard, J. (2001). Iron deficiency decreases dopamine D1 and D2 receptors in rat brain. Pharmacol. Biochem. Behav. 69, 409-418.
19. Erikson, K., Shihabi, Z. K., Aschner, J., and Aschner, M. (2002). Manganese accumulates in iron-deficient rat brain regions in a heterogeneous fashion and is associated with neurochemical alterations. Biol. Trace Elem. Res. 87, 143-156.
20. Erikson, K. M., Syversen, T., Steinnes, E., and Aschner, M. (2004). Globus pallidus: A target brain region for divalent metal accumulation associated with dietary iron deficiency. J. Nutr. Biochem. 15, 335-341.
21. Fell, J. M. E., Meadows, N., Khan, K., Long, S. G., Milla, P. J., Reynolds, A. P., Quaghebeur, G., and Taylor, W. J. (1996). Manganese toxicity in children receiving long-term parenteral nutrition. The Lancet 347, 1218-1221.
22. Felt, B., and Lozoff, B. (1996). Brain iron and behavior of rats are not normalized by treatment of iron deficiency anemia during early development. J. Nutr. 126, 693-701.
23. Garcia, S., Gellein, K., Syversen, T., and Aschner, M. (2006). A manganese-enhanced diet alters brain metals and transporters in the developing rat. Toxicol. Sci. 92, 516-525.
24. Garrick, M. D., Dolan, K. G., Horbinski, C., Chio, A. J., Higgins, D., Porubcin, M., Moore, E. G., Hainsworth, L. N., Umbreit, J. N., et al. (2003). DMT1: A mammalian transporter for multiple metals. Biometals 16, 41-54.
25. Gerber, G. B., Leonard, A., and Hantson, P. (2002). Carcinogenicity, mutagenicity and teratogenicity of manganese compounds. Crit. Rev. Oncol. Hematol. 42, 25-34.
26. Golub, M., Han, B., and Keen, C. (1996a). Iron and manganese uptake by offspring of lactating mice fed a high aluminum diet. Toxicology 109, 111-118.
27. Golub, M. S., Han, B., and Keen, C. L. (1996b). Aluminum alters iron and manganese uptake and regulation of surface transferrin receptors in primary rat oligodendrocyte cultures. Brain Res. 719, 72-77.
28. Grantham-McGregor, S., and Ani, C. (2001). A review of studies on the effect of iron deficiency on cognitive development in children. J. Nutr. 131, 649S-668S.
29. Grass, G., Franke, S., Taudte, N., Nies, D. H., Kucharski, L. M., Maguire, M. E., and Rensing, C. (2005). The metal permease ZupT from Escherichia coli is a transporter with a broad substrate spectrum. J. Bacteriol. 187, 1604-1611.
30. Gunshin, H., Mackenzie, B., Berger, U., Gunshin, Y., Romero, M., Boron, W., Nussberger, S., Gollan, J., and Hediger, M. (1997). Cloning and characterization of a mammalian proton-coupled metal-ion transporter. Nature 388, 482-488.
31. He, L., Girijashanker, K., Dalton, T., Reed, J., Li, H., Soleimani, M., and Nebert, D. (2006). ZIP8, member of the solute-carrier-39 (SLC39) metal-transporter family: Characterization of transporter properties. Mol. Pharmacol. 70, 171-180.
32. Kontur, P., and Fechter, L. (1985). Brain manganese, catecholamine turnover, and the development of startle in rats prenatally exposed to manganese. Teratology, 32, 1-11.
33. Kwik-Uribe, C., Golub, M., and Keen, C. (1999). Behavioral consequences of marginal iron deficiency during development in a murine model. Neurotoxicol. Teratol. 21, 661-672.
34. Kwik-Uribe, C. L., Golub, M. S., and Keen, C. L. (2000). Chronic marginal iron intakes during early development in mice alter brain iron concentrations and behavior despite postnatal iron supplimentation. J. Nutr. 130, 2040-2048.
35. Li, D. (1998). Effects of iron deficiency on iron distribution and γ-aminobutyric acid (GABA) metabolism in young rat brain tissues. Hokkaido J. Med. Sci. 73, 215-225.
36. Lowry, O. H., Rosebrough, N. J., Farr, A. L., and Randall, R. (1951). Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265-270.
37. Malecki, E., Devenyi, A., Barron, T., Mosher, T., Eslinger, P., Flaherty-Craig, C., and Rossaro, L. (1999a). Iron and manganese homeostasis in chronic liver disease: Relationship to pallidal T1-weighted magnetic resonance signal hyperintensity. Neurotoxicology 20, 647-652.
38. Malecki, E. A., Devenyi, A. G., Beard, J. L., and Connor, J. R. (1999b). Existing and emerging mechanisms for transport of iron and manganese to the brain. J. Neurosci. Res. 56, 113-122.
39. Malhotra, K. M., Murthy, R. C., Srivastava, R. S., and Chandra, S. V. (1984). Concurrent exposure of lead and manganese to iron-deficient rats: Effect on lipid peroxidation and contents of some metals in the brain. J. Appl. Toxicol. 4, 22-25.
40. Mena, I. (1974). The role of manganese in human disease. Ann. Clin. Lab. Sci. 4, 487-491.
41. Noel, L., Guerin, T., and Kolf-Clauw, M. (2004). Subchronic dietary exposure of rats to cadmium alters the metabolism of metals essential to bone health. Food Chem. Toxicol. 42, 1203-1210.
42. Olanow, C., Good, P., Shinotoh, H., Hewitt, K., Vingerhoets, F., Snow, B., Beal, M., Calne, D., and Perl, D. (1996). Manganese intoxication in the rhesus monkey: A clinical, imaging, pathologic, and biochemical study. Neurology 46, 492-498.
43. Ono, J., et al. (1995). Manganese deposition in the brain during long-term total parenteral nutrition. J. Parenter. Enteral Nutr. 19, 310-312.
44. Pal, P. K., Samii, A., and Calne, D. B. (1999). Manganese neurotoxicity: A review of clinical features, imaging and pathology. Neurotoxicology 20, 227-238.
45. Pinero, D., et al. (2000). Variations in dietary iron alter brain iron metabolism in developing rats. J. Nutr. 130, 254-263.
46. Racette, B., Antenor, J., McGee-Minnich, L., Moerlein, S., Videen, T., Kotagal, V, and Perlmutter, J. (2005). [18F]FDOPA PET and clinical features in parkinsonism due to manganism. Mov. Disord. 20, 492-496.
47. Roth, J. A., and Garrick, M. D. (2003). Iron interactions and other biological reactions mediating the physiological and toxic actions of manganese. Biochem. Pharmacol. 66, 1-13.
48. Roth, J. A., Horbinski, C., Higgins, D., Lein, P., Garrick, M. D. (2002). Mechanisms of manganese-induce rat pheochromocytoma (PC12) cell death and cell differentiation. Neurotoxicology 23, 147-157.
49. Shukla, A., Agarwal, K., and Shukla, G. (1990). Effect of latent iron deficiency on the levels of iron, calcium, zinc, copper, manganese, cadmium, and lead in liver, kidney, and spleen of growing rats. Experientia 46, 751-752.
50. Smith, Q., Rabin, O., and Chikhale, E. (1997). Delivery of metals to brain and the role of the blood-brain barrier. In Metals and Oxidative Damage in Neurological Disorders (J. Connor, Ed.). pp. 113-130. Plenum Press, New York.
51. Verity, M. A. (1999). Manganese neurotoxicity: A mechanistic hypothesis. Neurotoxicology 20, 489-498.
52. Yokel, R. (2002). Brain uptake, retention, and efflux of aluminum and manganese. Environ. Health Perspect. 110, 699-704.
53. Yokel, R., and Crossgrove, J. (2004). Manganese toxicokinetics at the blood-brain barrier. Res. Rep. Health Eff. Inst. 119, 7-58.
54. Yokoi, K., Kimura, M., and Itokawa, Y. (1991). Effect of dietary iron deficiency on mineral levels in tissues of rats. Biol. Trace Elem. Res. 29, 257-265.
55. Zheng, W., Aschner, M., and Ghersi-Egea, J.F. (2003). Brain barrier systems: A new frontier in metal neurotoxicological research. Toxicol. Appl. Pharmacol. 192, 1-11.