Ingestion of Mn and Pb by rats during and after pregnancy alters iron metabolism and behavior in offspring

NeuroToxicology

Volumn 32, Issue 4, 2011, Pages 413-422

  Molina, Ramon M ^a   Phattanarudee, Siripan ^b   Kim, Jonghan ^a   Thompson, Khristy ^a   Wessling Resnick, Marianne ^a   Maher, Timothy J ^b   Brain, Joseph D ^a  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^b MASSACHUSETTS COLLEGE OF PHARMACY AND HEALTH SCIENCES   (United States)

Author keywords

Anxiety; Biomarker; Heavy metals; Iron metabolism; Metal interaction; Neurotoxicity

Indexed keywords

LEAD; MANGANESE; NATURAL RESISTANCE ASSOCIATED MACROPHAGE PROTEIN 2;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANXIETY DISORDER; ARTICLE; BLOOD LEVEL; BRAIN LEVEL; CONTROLLED STUDY; FEMALE; FETUS OUTCOME; GESTATION PERIOD; HEMATOCRIT; INGESTION; IRON ABSORPTION; IRON METABOLISM; LACTATION; LITTER SIZE; LOW BIRTH WEIGHT; MALE; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; RAT; TOXICITY TESTING;

ADMINISTRATION, ORAL; AGE FACTORS; AGING; ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; BRAIN; CATION TRANSPORT PROTEINS; CHLORIDES; DUODENUM; FEMALE; GESTATIONAL AGE; INTESTINAL ABSORPTION; IRON; IRON METABOLISM DISORDERS; LACTATION; MALE; MANGANESE COMPOUNDS; MATERNAL EXPOSURE; MOTOR ACTIVITY; ORGANOMETALLIC COMPOUNDS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, SPRAGUE-DAWLEY;

RATTUS;

EID: 79955509072     PISSN: 0161813X     EISSN: 18729711     Source Type: Journal    
DOI: 10.1016/j.neuro.2011.03.010     Document Type: Article

References (57)

1. Al-Saleh I., Nester M., Mashhour A., Moncari L., Shinwari N., Mohamed Gel D., et al. Prenatal and postnatal lead exposure and early cognitive development: longitudinal study in Saudi Arabia. J Environ Pathol Toxicol Oncol 2009, 28:283-302.
2. Aschner M., Aschner J.L. Manganese transport across the blood-brain barrier: relationship to iron homeostasis. Brain Res Bull 1990, 24:857-860.
3. Aschner M., Aschner J.L. Manganese neurotoxicity: cellular effects and blood-brain barrier transport. Neurosci Biobehav Rev 1991, 15:333-340.
4. Au C., Benedetto A., Aschner M. Manganese transport in eukaryotes: the role of DMT1. Neurotoxicology 2008, 29:569-576.
5. Barlow P.J. A pilot study on the metal levels in the hair of hyperactive children. Med Hypotheses 1983, 11:309-318.
6. Beard J.L., Erikson K.M., Jones B.C. Neurobehavioral analysis of developmental iron deficiency in rats. Behav Brain Res 2002, 134:517-524.
7. Brockel B.J., Cory-Slechta D.A. The effects of postweaning low-level Pb exposure on sustained attention: a study of target densities, stimulus presentation rate, and stimulus predictability. Neurotoxicology 1999, 20:921-933.
8. Brockel B.J., Cory-Slechta D.A. Lead-induced decrements in waiting behavior: involvement of D2-like dopamine receptors. Pharmacol Biochem Behav 1999, 63:423-434.
9. Brondum J. Attention deficit hyperactivity disorder and blood lead levels in Chinese children. Environ Health Perspect 2009, 117:A286.
10. Cawte J. Psychiatric sequelae of manganese exposure in the adult, foetal and neonatal nervous systems. Aust N Z J Psychiatry 1985, 19:211-217.
11. Chung J., Wessling-Resnick M. Molecular mechanisms and regulation of iron transport. Crit Rev Clin Lab Sci 2003, 40:151-182.
12. Collipp P.J., Chen S.Y., Maitinsky S. Manganese in infant formulas and learning disability. Ann Nutr Metab 1983, 27:488-494.
13. Coscia J.M., Ris M.D., Succop P.A., Dietrich K.N. Cognitive development of lead exposed children from ages 6 to 15 years: an application of growth curve analysis. Child Neuropsychol 2003, 9:10-21.
14. Crowe A., Morgan E.H. Interactions between tissue uptake of lead and iron in normal and iron-deficient rats during development. Biol Trace Elem Res 1996, 52:249-261.
15. Dailey H.A. Metal inhibition of ferrochelatase. Ann N Y Acad Sci 1987, 514:81-86.
16. Dietrich K.N., Succop P.A., Berger O.G., Hammond P.B., Bornschein R.L. Lead exposure and the cognitive development of urban preschool children: the Cincinnati Lead Study cohort at age 4 years. Neurotoxicol Teratol 1991, 13:203-211.
17. Dorman D.C., McElveen A.M., Marshall M.W., Parkinson C.U., Arden James R., Struve M.F., et al. Maternal-fetal distribution of manganese in the rat following inhalation exposure to manganese sulfate. Neurotoxicology 2005, 26:625-632.
18. Dorman D.C., McElveen A.M., Marshall M.W., Parkinson C.U., James R.A., Struve M.F., et al. Tissue manganese concentrations in lactating rats and their offspring following combined in utero and lactation exposure to inhaled manganese sulfate. Toxicol Sci 2005, 84:12-21.
19. Dorman D.C., Struve M.F., Vitarella D., Byerly F.L., Goetz J., Miller R. Neurotoxicity of manganese chloride in neonatal and adult CD rats following subchronic (21-day) high-dose oral exposure. J Appl Toxicol 2000, 20:179-187.
20. Dougherty D.D., Bonab A.A., Spencer T.J., Rauch S.L., Madras B.K., Fischman A.J. Dopamine transporter density in patients with attention deficit hyperactivity disorder. Lancet 1999, 354:2132-2133.
21. Ernst M., Zametkin A.J., Matochik J.A., Jons P.H., Cohen R.M. DOPA decarboxylase activity in attention deficit hyperactivity disorder adults. A [fluorine-18]fluorodopa positron emission tomographic study. J Neurosci 1998, 18:5901-5907.
22. Fitzmaurice G.M., Laird N.M., Ware J.H. Applied longitudinal analysis 2004, John Wiley and Sons, New York.
23. Garcia S.J., Gellein K., Syversen T., Aschner M. A manganese-enhanced diet alters brain metals and transporters in the developing rat. Toxicol Sci 2006, 92:516-525.
24. Garrick M.D., Dolan K.G., Horbinski C., Ghio A.J., Higgins D., Porubcin M., et al. DMT1: a mammalian transporter for multiple metals. Biometals 2003, 16:41-54.
25. Garrick M.D., Singleton S.T., Vargas F., Kuo H.C., Zhao L., Knopfel M., et al. DMT1: which metals does it transport?. Biol Res 2006, 39:79-85.
26. Gu C., Chen S., Xu X., Zheng L., Li Y., Wu K., et al. Lead and cadmium synergistically enhance the expression of divalent metal transporter 1 protein in central nervous system of developing rats. Neurochem Res 2009, 34:1150-1156.
27. Hesslinger B., Tebartz van Elst L., Thiel T., Haegele K., Hennig J., Ebert D. Frontoorbital volume reductions in adult patients with attention deficit hyperactivity disorder. Neurosci Lett 2002, 328:319-321.
28. Itami S., Uno H. Orbitofrontal cortex dysfunction in attention-deficit hyperactivity disorder revealed by reversal and extinction tasks. Neuroreport 2002, 13:2453-2457.
29. Jentsch J.D., Taylor J.R. Impulsivity resulting from frontostriatal dysfunction in drug abuse: implications for the control of behavior by reward-related stimuli. Psychopharmacology (Berl) 1999, 146:373-390.
30. Kern C.H., Stanwood G.D., Smith D.R. Preweaning manganese exposure causes hyperactivity, disinhibition, and spatial learning and memory deficits associated with altered dopamine receptor and transporter levels. Synapse 2010, 64:363-378.
31. Kim J., Kim S.H., Lee M.G. Liver and gastrointestinal first-pass effects of azosemide in rats. J Pharm Pharmacol 1997, 49:878-883.
32. Kontur P.J., Fechter L.D. Brain manganese, catecholamine turnover, and the development of startle in rats prenatally exposed to manganese. Teratology 1985, 32:1-11.
33. Kuhlmann A.C., McGlothan J.L., Guilarte T.R. Developmental lead exposure causes spatial learning deficits in adult rats. Neurosci Lett 1997, 233:101-104.
34. Labbe R.F., Vreman H.J., Stevenson D.K. Zinc protoporphyrin: a metabolite with a mission. Clin Chem 1999, 45:2060-2072.
35. LaHoste G.J., Swanson J.M., Wigal S.B., Glabe C., Wigal T., King N., et al. Dopamine D4 receptor gene polymorphism is associated with attention deficit hyperactivity disorder. Mol Psychiatry 1996, 1:121-124.
36. Lasley S.M., Gilbert M.E. Glutamatergic components underlying lead-induced impairments in hippocampal synaptic plasticity. Neurotoxicology 2000, 21:1057-1068.
37. Lozoff B., Jimenez E., Wolf A.W. Long-term developmental outcome of infants with iron deficiency. N Engl J Med 1991, 325:687-694.
38. McArdle H.J., Andersen H.S., Jones H., Gambling L. Copper and iron transport across the placenta: regulation and interactions. J Neuroendocrinol 2008, 20:427-431.
39. Moreira E.G., Vassilieff I., Vassilieff V.S. Developmental lead exposure: behavioral alterations in the short and long term. Neurotoxicol Teratol 2001, 23:489-495.
40. Pappas B.A., Zhang D., Davidson C.M., Crowder T., Park G.A., Fortin T. Perinatal manganese exposure: behavioral, neurochemical, and histopathological effects in the rat. Neurotoxicol Teratol 1997, 19:17-25.
41. Pellow S., Chopin P., File S.E., Briley M. Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J Neurosci Methods 1985, 14:149-167.
42. Reichel C.M., Wacan J.J., Farley C.M., Stanley B.J., Crawford C.A., McDougall S.A. Postnatal manganese exposure attenuates cocaine-induced locomotor activity and reduces dopamine transporters in adult male rats. Neurotoxicol Teratol 2006, 28:323-332.
43. Rodrigues A.L., Rocha J.B., Mello C.F., Souza D.O. Effect of perinatal lead exposure on rat behaviour in open-field and two-way avoidance tasks. Pharmacol Toxicol 1996, 79:150-156.
44. Soldin O.P., Aschner M. Effects of manganese on thyroid hormone homeostasis: potential links. Neurotoxicology 2007, 28:951-956.
45. St-Pierre A., Normandin L., Carrier G., Kennedy G., Butterworth R., Zayed J. Bioaccumulation and locomotor effect of manganese dust in rats. Inhal Toxicol 2001, 13:623-632.
46. Taylor E.M., Morgan E.H. Developmental changes in transferrin and iron uptake by the brain in the rat. Brain Res Dev Brain Res 1990, 55:35-42.
47. Thompson K., Molina R.M., Donaghey T., Schwob J.E., Brain J.D., Wessling-Resnick M. Olfactory uptake of manganese requires DMT1 and is enhanced by anemia. FASEB J 2007, 21:223-230.
48. Torrance J.D., Bothwell T.H. A simple technique for measuring storage iron concentrations in formalinised liver samples. S Afr J Med Sci 1968, 33:9-11.
49. Tran T.T., Chowanadisai W., Crinella F.M., Chicz-DeMet A., Lonnerdal B. Effect of high dietary manganese intake of neonatal rats on tissue mineral accumulation, striatal dopamine levels, and neurodevelopmental status. Neurotoxicology 2002, 23:635-643.
50. Tran T.T., Chowanadisai W., Lonnerdal B., Le L., Parker M., Chicz-Demet A., et al. Effects of neonatal dietary manganese exposure on brain dopamine levels and neurocognitive functions. Neurotoxicology 2002, 23:645-651.
51. Trombini T.V., Pedroso C.G., Ponce D., Almeida A.A., Godinho A.F. Developmental lead exposure in rats: is a behavioral sequel extended at F2 generation?. Pharmacol Biochem Behav 2001, 68:743-751.
52. Ueno K.I., Togashi H., Mori K., Matsumoto M., Ohashi S., Hoshino A., et al. Behavioural and pharmacological relevance of stroke-prone spontaneously hypertensive rats as an animal model of a developmental disorder. Behav Pharmacol 2002, 13:1-13.
53. Vaidya C.J., Austin G., Kirkorian G., Ridlehuber H.W., Desmond J.E., Glover G.H., et al. Selective effects of methylphenidate in attention deficit hyperactivity disorder: a functional magnetic resonance study. Proc Natl Acad Sci U S A 1998, 95:14494-14499.
54. Verger C., Sassa S., Kappas A. Growth-promoting effects of iron- and cobalt-protoporphyrins on cultured embryonic cells. J Cell Physiol 1983, 116:135-141.
55. Walf A.A., Frye C.A. The use of the elevated plus maze as an assay of anxiety-related behavior in rodents. Nat Protoc 2007, 2:322-328.
56. Waynforth H.B., Flecknell P.A. Experimental and surgical technique in the rat 1992, Academic Press, London. 2nd ed.
57. Yang Y., Ma Y., Ni L., Zhao S., Li L., Zhang J., et al. Lead exposure through gestation-only caused long-term learning/memory deficits in young adult offspring. Exp Neurol 2003, 184:489-495.