Iron-responsive olfactory uptake of manganese improves motor function deficits associated with iron deficiency

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Kim, Jonghan ^a   Li, Yuan ^a   Buckett, Peter D ^a   Böhlke, Mark ^b   Thompson, Khristy J ^a   Takahashi, Masaya ^c   Maher, Timothy J ^b   Wessling Resnick, Marianne ^a  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

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

^c HARVARD INSTITUTES OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOPAMINE 1 RECEPTOR; DOPAMINE 2 RECEPTOR; DOPAMINE TRANSPORTER; MANGANESE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN LEVEL; BRAIN REGION; BRAIN SIZE; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINE BRAIN LEVEL; DRUG EFFICACY; DRUG ELIMINATION; DRUG HALF LIFE; HIPPOCAMPUS; IRON DEFICIENCY; MANGANESE BRAIN LEVEL; MOTOR COORDINATION; MOTOR DYSFUNCTION; MOTOR PERFORMANCE; NONHUMAN; PREFRONTAL CORTEX; RAT; TREATMENT DURATION;

ADMINISTRATION, INTRANASAL; ANIMALS; BRAIN; CORPUS STRIATUM; DOPAMINE; DOPAMINE PLASMA MEMBRANE TRANSPORT PROTEINS; INSTILLATION, DRUG; IRON; IRON, DIETARY; MAGNETIC RESONANCE IMAGING; MANGANESE; MOTOR ACTIVITY; OLFACTORY BULB; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, DOPAMINE;

RATTUS;

EID: 84859132936     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0033533     Document Type: Article

References (42)

1. Thompson K, Molina RM, Donaghey T, Schwob JE, Brain JD, et al. (2007) Olfactory uptake of manganese requires DMT1 and is enhanced by anemia. FASEB J 21: 223-230.
2. Gunshin H, Mackenzie B, Berger UV, Gunshin Y, Romero MF, et al. (1997) Cloning and characterization of a mammalian proton-coupled metal-ion transporter. Nature 388: 482-488.
3. Fleming MD, Romano MA, Su MA, Garrick LM, Garrick MD, et al. (1998) Nramp2 is mutated in the anemic Belgrade (b) rat: evidence of a role for Nramp2 in endosomal iron transport. Proc Natl Acad Sci U S A 95: 1148-1153.
4. Canonne-Hergaux F, Gruenheid S, Ponka P, Gros P, (1999) Cellular and subcellular localization of the Nramp2 iron transporter in the intestinal brush border and regulation by dietary iron. Blood 93: 4406-4417.
5. Youdim MB, Ben-Shachar D, Yehuda S, (1989) Putative biological mechanisms of the effect of iron deficiency on brain biochemistry and behavior. Am J Clin Nutr 50: 607-615; discussion 615-607.
6. Hunt JR, Zito CA, Erjavec J, Johnson LK, (1994) Severe or marginal iron deficiency affects spontaneous physical activity in rats. Am J Clin Nutr 59: 413-418.
7. Beard JL, Chen Q, Connor J, Jones BC, (1994) Altered monamine metabolism in caudate-putamen of iron-deficient rats. Pharmacol Biochem Behav 48: 621-624.
8. Nelson C, Erikson K, Pinero DJ, Beard JL, (1997) In vivo dopamine metabolism is altered in iron-deficient anemic rats. J Nutr 127: 2282-2288.
9. Erikson KM, Jones BC, Beard JL, (2000) Iron deficiency alters dopamine transporter functioning in rat striatum. J Nutr 130: 2831-2837.
10. Lozoff B, (2011) Early iron deficiency has brain and behavior effects consistent with dopaminergic dysfunction. J Nutr 141: 740S-746S.
11. Chen Q, Beard JL, Jones BC, (1995) Abnormal rat brain monoamine metabolism in iron deficiency anemia. Nutr Biochem 6: 486-493.
12. Cotzias GC, (1958) Manganese in health and disease. Physiol Rev 38: 503-532.
13. Takeda A, Sawashita J, Okada S, (1995) Biological half-lives of zinc and manganese in rat brain. Brain Res 695: 53-58.
14. Aschner M, Erikson KM, Dorman DC, (2005) Manganese dosimetry: species differences and implications for neurotoxicity. Crit Rev Toxicol 35: 1-32.
15. EPA (2010) Manganese (CASRN 7439-96-5) Available at: http://www.epa.gov/iris/subst/0373.htm. Accessed January 1, 2010.
16. Heilig E, Molina R, Donaghey T, Brain JD, Wessling-Resnick M, (2005) Pharmacokinetics of pulmonary manganese absorption: evidence for increased susceptibility to manganese loading in iron-deficient rats. Am J Physiol Lung Cell Mol Physiol 288: L887-893.
17. Thompson K, Molina R, Donaghey T, Brain JD, Wessling-Resnick M, (2006) The influence of high iron diet on rat lung manganese absorption. Toxicol Appl Pharmacol 210: 17-23.
18. Tjalve H, Henriksson J, Tallkvist J, Larsson BS, Lindquist NG, (1996) Uptake of manganese and cadmium from the nasal mucosa into the central nervous system via olfactory pathways in rats. Pharmacol Toxicol 79: 347-356.
19. Brenneman KA, Wong BA, Buccellato MA, Costa ER, Gross EA, et al. (2000) Direct olfactory transport of inhaled manganese ((54)MnCl(2)) to the rat brain: toxicokinetic investigations in a unilateral nasal occlusion model. Toxicol Appl Pharmacol 169: 238-248.
20. Nong A, Teeguarden JG, Clewell HJ 3rd, Dorman DC, Andersen ME, (2008) Pharmacokinetic modeling of manganese in the rat IV: Assessing factors that contribute to brain accumulation during inhalation exposure. J Toxicol Environ Health A 71: 413-426.
21. Thompson KJ, Molina RM, Donaghey T, Savaliya S, Schwob JE, et al. (2011) Manganese uptake and distribution in the brain after methyl bromide-induced lesions in the olfactory epithelia. Toxicol Sci 120: 163-172.
22. Takeda A, Kodama Y, Ishiwatari S, Okada S, (1998) Manganese transport in the neural circuit of rat CNS. Brain Res Bull 45: 149-152.
23. Erikson KM, Shihabi ZK, Aschner JL, 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.
24. Fitsanakis VA, Zhang N, Anderson JG, Erikson KM, Avison MJ, et al. (2008) Measuring brain manganese and iron accumulation in rats following 14 weeks of low-dose manganese treatment using atomic absorption spectroscopy and magnetic resonance imaging. Toxicol Sci 103: 116-124.
25. Bonilla E, (1984) Chronic manganese intake induces changes in the motor activity of rats. Exp Neurol 84: 696-700.
26. Nachtman JP, Tubben RE, Commissaris RL, (1986) Behavioral effects of chronic manganese administration in rats: locomotor activity studies. Neurobehav Toxicol Teratol 8: 711-715.
27. Williams JM, Milatovic D, Gore JC, Aschner M, Avison MJ, (2010) Chronic exposure to manganese alters brain responses to amphetamine: a pharmacological magnetic resonance imaging study. Toxicol Sci 114: 310-322.
28. Guilarte TR, Burton NC, McGlothan JL, Verina T, Zhou Y, et al. (2008) Impairment of nigrostriatal dopamine neurotransmission by manganese is mediated by pre-synaptic mechanism(s): implications to manganese-induced parkinsonism. J Neurochem 107: 1236-1247.
29. Subhash MN, Padmashree TS, (1991) Effect of manganese on biogenic amine metabolism in regions of the rat brain. Food Chem Toxicol 29: 579-582.
30. Autissier N, Rochette L, Dumas P, Beley A, Loireau A, et al. (1982) Dopamine and norepinephrine turnover in various regions of the rat brain after chronic manganese chloride administration. Toxicology 24: 175-182.
31. Vidal L, Alfonso M, Campos F, Faro LR, Cervantes RC, et al. (2005) Effects of manganese on extracellular levels of dopamine in rat striatum: an analysis in vivo by brain microdialysis. Neurochem Res 30: 1147-1154.
32. Anderson JG, Cooney PT, Erikson KM, (2007) Inhibition of DAT function attenuates manganese accumulation in the globus pallidus. Environ Toxicol Pharmacol 23: 179-184.
33. Ingersoll RT, Montgomery EB Jr, Aposhian HV, (1999) Central nervous system toxicity of manganese. II: Cocaine or reserpine inhibit manganese concentration in the rat brain. Neurotoxicology 20: 467-476.
34. Chen MK, Lee JS, McGlothan JL, Furukawa E, Adams RJ, et al. (2006) Acute manganese administration alters dopamine transporter levels in the non-human primate striatum. Neurotoxicology 27: 229-236.
35. Kern CH, Stanwood GD, Smith DR, (2010) Preweaning manganese exposure causes hyperactivity, disinhibition, and spatial learning and memory deficits associated with altered dopamine receptor and transporter levels. Synapse 64: 363-378.
36. Kern CH, Smith DR, (2011) Preweaning Mn exposure leads to prolonged astrocyte activation and lasting effects on the dopaminergic system in adult male rats. Synapse 65: 532-544.
37. Yamamoto K, Kobayashi N, Yoshitama K, Teramoto S, Komamine A, (2001) Isolation and purification of tyrosine hydroxylase from callus cultures of Portulaca grandiflora. Plant Cell Physiol 42: 969-975.
38. McEwan AG, (2009) New insights into the protective effect of manganese against oxidative stress. Mol Microbiol 72: 812-814.
39. McNaughton RL, Reddi AR, Clement MH, Sharma A, Barnese K, et al. (2010) Probing in vivo Mn2+ speciation and oxidative stress resistance in yeast cells with electron-nuclear double resonance spectroscopy. Proc Natl Acad Sci U S A 107: 15335-15339.
40. Kankaanpaa A, Meririnne E, Ariniemi K, Seppala T, (2001) Oxalic acid stabilizes dopamine, serotonin, and their metabolites in automated liquid chromatography with electrochemical detection. J Chromatogr B Biomed Sci Appl 753: 413-419.
41. Ferguson SA, Gough BJ, Cada AM, (2003) In vivo basal and amphetamine-induced striatal dopamine and metabolite levels are similar in the spontaneously hypertensive, Wistar-Kyoto and Sprague-Dawley male rats. Physiol Behav 80: 109-114.
42. Gamache P, Ryan E, Svendsen C, Murayama K, Acworth IN, (1993) Simultaneous measurement of monoamines, metabolites and amino acids in brain tissue and microdialysis perfusates. J Chromatogr 614: 213-220.