Manganese homeostasis in the nervous system

Journal of Neurochemistry

Volumn 134, Issue 4, 2015, Pages 601-610

  Chen, Pan ^a   Chakraborty, Sudipta ^b   Mukhopadhyay, Somshuvra ^c   Lee, Eunsook ^d   Paoliello, Monica M B ^e   Bowman, Aaron B ^f   Aschner, Michael ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^d MEHARRY MEDICAL COLLEGE   (United States)

^e STATE UNIVERSITY OF LONDRINA   (Brazil)

^f VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

manganese; Parkinson's disease; transport

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CALCIUM CHANNEL; CARRIER PROTEIN; CHOLINE TRANSPORTER; CITRATE TRANSPORTER; DOPAMINE TRANSPORTER; FERROPORTIN; MANGANESE; NATURAL RESISTANCE ASSOCIATED MACROPHAGE PROTEIN 2; PROTEIN ATP13A2; PROTEIN SLC30A10; PROTEIN SPCA1; PROTEIN ZIP14; PROTEIN ZIP8; TRANSFERRIN; TRANSFERRIN RECEPTOR; UNCLASSIFIED DRUG; ZINC TRANSPORTER;

ENERGY METABOLISM; ENVIRONMENTAL EXPOSURE; HOMEOSTASIS; HUMAN; IMMUNE RESPONSE; INTOXICATION; NEUROTOXICITY; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; REVIEW; TRANSPORT KINETICS; ANIMAL; MANGANESE POISONING; METABOLISM; NEURODEGENERATIVE DISEASES; PHYSIOLOGY; PROTEIN TRANSPORT;

ANIMALS; HOMEOSTASIS; HUMANS; MANGANESE; MANGANESE POISONING; MEMBRANE TRANSPORT PROTEINS; NEURODEGENERATIVE DISEASES; PARKINSON DISEASE; PROTEIN TRANSPORT;

EID: 84937813455     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.13170     Document Type: Review

References (103)

1. Aisen P., Leibman A., and, Zweier J., (1978) Stoichiometric and site characteristics of the binding of iron to human transferrin. J. Biol. Chem. 253, 1930-1937.
2. Anderson J. G., Cooney P. T., and, Erikson K. M., (2007) Inhibition of DAT function attenuates manganese accumulation in the globus pallidus. Environ. Toxicol. Pharmacol. 23, 179-184.
3. Aschner J. L., and, Aschner M., (2005) Nutritional aspects of manganese homeostasis. Mol. Aspects Med. 26, 353-362.
4. ATSDR (2008) Toxicological Profile for Manganese (Draft for Public Comment). Department of Health and Human Services, Public Service, U.S.
5. Au C., Benedetto A., and, Aschner M., (2008) Manganese transport in eukaryotes: the role of DMT1. Neurotoxicology 29, 569-576.
6. Baldi C., Vazquez G., and, Boland R., (2002) Characterization of a 1, 25 (OH) 2-vitamin D3-responsive capacitative Ca2 + entry pathway in rat osteoblast-like cells. J. Cell. Biochem. 86, 678-687.
7. Begum N. A., Kobayashi M., Moriwaki Y., Matsumoto M., Toyoshima K., and, Seya T., (2002) Mycobacterium bovis BCG cell wall and lipopolysaccharide induce a novel gene, BIGM103, encoding a 7-TM protein: identification of a new protein family having Zn-transporter and Zn-metalloprotease signatures. Genomics 80, 630-645.
8. Behrens M. I., Brüggemann N., Chana P., et al,. (2010) Clinical spectrum of Kufor-Rakeb syndrome in the Chilean kindred with ATP13A2 mutations. Mov. Disord. 25, 1929-1937.
9. Blasco H., Vourc'h P., Nadjar Y., et al,. (2011) Association between divalent metal transport 1 encoding gene (SLC11A2) and disease duration in amyotrophic lateral sclerosis. J. Neurol. Sci. 303, 124-127.
10. Bosomworth H. J., Thornton J. K., Coneyworth L. J., Ford D., and, Valentine R. A., (2012) Efflux function, tissue-specific expression and intracellular trafficking of the Zn transporter ZnT10 indicate roles in adult Zn homeostasis. Metallomics 4, 771-779.
11. Brissot P., Bardou-Jacquet E., Jouanolle A. M., and, Loreal O., (2011) Iron disorders of genetic origin: a changing world. Trends Mol. Med. 17, 707-713.
12. Burdo J. R., Menzies S. L., Simpson I. A., Garrick L. M., Garrick M. D., Dolan K. G., Haile D. J., Beard J. L., and, Connor J. R., (2001) Distribution of divalent metal transporter 1 and metal transport protein 1 in the normal and Belgrade rat. J. Neurosci. Res. 66, 1198-1207.
13. Butterworth R. F., (2013) Parkinsonism in cirrhosis: pathogenesis and current therapeutic options. Metab. Brain Dis. 28, 261-267.
14. Chen M.-K., Lee J.-S., McGlothan J. L., Furukawa E., Adams R. J., Alexander M., Wong D. F., and, Guilarte T. R., (2006) Acute manganese administration alters dopamine transporter levels in the non-human primate striatum. Neurotoxicology 27, 229-236.
15. Chen P., Parmalee N., and, Aschner M., (2014) Genetic factors and manganese-induced neurotoxicity. Front. Genet. 5, 265. doi: 10.3389/fgene.2014.00265.
16. Ciliax B. J., Heilman C., Demchyshyn L. L., Pristupa Z. B., Ince E., Hersch S. M., Niznik H. B., and, Levey A. I., (1995) The dopamine transporter: immunochemical characterization and localization in brain. J. Neurosci. 15, 1714-1723.
17. Crossgrove J. S., and, Yokel R. A., (2004) Manganese distribution across the blood-brain barrier III: the divalent metal transporter-1 is not the major mechanism mediating brain manganese uptake. Neurotoxicology 25, 451-460.
18. Crossgrove J. S., and, Yokel R. A., (2005) Manganese distribution across the blood-brain barrier: IV. Evidence for brain influx through store-operated calcium channels. Neurotoxicology 26, 297-307.
19. 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 managanese citrate as well as manganese and manganese transferrin. Neurotoxicology 24, 3-13.
20. Dalton T. P., He L., Wang B., Miller M. L., Jin L., Stringer K. F., Chang X., Baxter C. S., and, Nebert D. W., (2005) Identification of mouse SLC39A8 as the transporter responsible for cadmium-induced toxicity in the testis. Proc. Natl Acad. Sci. USA 102, 3401-3406.
21. Davis C. D., Zech L., and, Greger J. L., (1993) Manganese metabolism in rats: an improved methodology for assessing gut endogenous losses. Proc. Soc. Exp. Biol. Med. 202, 103-108.
22. Di Fonzo A., Chien H. F., Socal M., et al,. (2007) ATP13A2 missense mutations in juvenile parkinsonism and young onset Parkinson disease. Neurology 68, 1557-1562.
23. Dobrydneva Y., and, Blackmore P., (2001) 2-Aminoethoxydiphenyl borate directly inhibits store-operated calcium entry channels in human platelets. Mol. Pharmacol. 60, 541-552.
24. Donovan A., Brownlie A., Zhou Y., et al,. (2000) Positional cloning of zebrafish ferroportin1 identifies a conserved vertebrate iron exporter. Nature 403, 776-781.
25. Donovan A., Lima C. A., Pinkus J. L., Pinkus G. S., Zon L. I., Robine S., and, Andrews N. C., (2005) The iron exporter ferroportin/Slc40a1 is essential for iron homeostasis. Cell Metab. 1, 191-200.
26. Eastman R. R., Jursa T. P., Benedetti C., Lucchini R. G., and, Smith D. R., (2013) Hair as a biomarker of environmental manganese exposure. Environ. Sci. Technol. 47, 1629-1637.
27. Erikson K. M., John C. E., Jones S. R., and, Aschner M., (2005a) Manganese accumulation in striatum of mice exposed to toxic doses is dependent upon a functional dopamine transporter. Environ. Toxicol. Pharmacol. 20, 390-394.
28. Erikson K. M., Syversen T., Aschner J. L., and, Aschner M., (2005b) Interactions between excessive manganese exposures and dietary iron-deficiency in neurodegeneration. Environ. Toxicol. Pharmacol. 19, 415-421.
29. Fasolato C., Hoth M., and, Penner R., (1993) Multiple mechanisms of manganese-induced quenching of fura-2 fluorescence in rat mast cells. Pflugers Arch. 423, 225-231.
30. Finley J. W., (1998) Manganese uptake and release by cultured human hepato-carcinoma (Hep-G2) cells. Biol. Trace Elem. Res. 64, 101-118.
31. Finley J. W., Johnson P. E., and, Johnson L. K., (1994) Sex affects manganese absorption and retention by humans from a diet adequate in manganese. Am. J. Clin. Nutr. 60, 949-955.
32. Garrick M. D., Singleton S. T., Vargas F., et al,. (2006) DMT1: which metals does it transport? Biol. Res. 39, 79-85.
33. Genter M. B., Kendig E. L., and, Knutson M. D., (2009) Uptake of materials from the nasal cavity into the blood and brain. Ann. N. Y. Acad. Sci. 1170, 623-628.
34. Girijashanker K., He L., Soleimani M., Reed J. M., Li H., Liu Z., Wang B., Dalton T. P., and, Nebert D. W., (2008) Slc39a14 gene encodes ZIP14, A metal/bicarbonate symporter: similarities to the ZIP8 transporter. Mol. Pharmacol. 73, 1413-1423.
35. Gitler A. D., Chesi A., Geddie M. L., et al,. (2009) Alpha-synuclein is part of a diverse and highly conserved interaction network that includes PARK9 and manganese toxicity. Nat. Genet. 41, 308-315.
36. Gospe S. M., Jr, Caruso R. D., Clegg M. S., Keen C. L., Pimstone N. R., Ducore J. M., Gettner S. S., and, Kreutzer R. A., (2000) Paraparesis, hypermanganesaemia, and polycythaemia: a novel presentation of cirrhosis. Arch. Dis. Child. 83, 439-442.
37. Guarneros M., Ortiz-Romo N., Alcaraz-Zubeldia M., Drucker-Colin R., and, Hudson R., (2013) Nonoccupationet alnvironmentet alxposure to manganese is linked to deficits in peripheral and central olfactory function. Chem. Senses 38, 783-791.
38. Guilarte T. R., (2010) Manganese and Parkinson's disease: a critical review and new findings. Environ. Health Perspect. 118, 1071-1080.
39. Gunter T. E., Gerstner B., Gunter K. K., Malecki J., Gelein R., Valentine W. M., Aschner M., and, Yule D. I., (2013) Manganese transport via the transferrin mechanism. Neurotoxicology 34, 118-127.
40. He L., Girijashanker K., Dalton T. P., Reed J., Li H., Soleimani M., and, Nebert D. W., (2006) ZIP8, Member of the solute-carrier-39 (SLC39) metal-transporter family: characterization of transporter properties. Mol. Pharmacol. 70, 171-180.
41. He Q., Du T., Yu X., et al,. (2011) DMT1 polymorphism and risk of Parkinson's disease. Neurosci. Lett. 501, 128-131.
42. Herrero Hernandez E., Discalzi G., Valentini C., Venturi F., Chio A., Carmellino C., Rossi L., Sacchetti A., and, Pira E., (2006) Follow-up of patients affected by manganese-induced Parkinsonism after treatment with CaNa2EDTA. Neurotoxicology 27, 333-339.
43. Hu Z., Bonifas J. M., Beech J., Bench G., Shigihara T., Ogawa H., Ikeda S., Mauro T., and, Epstein E. H., Jr, (2000) Mutations in ATP2C1, encoding a calcium pump, cause Hailey-Hailey disease. Nat. Genet. 24, 61-65.
44. Huang L., and, Tepaamorndech S., (2013) The SLC30 family of zinc transporters: a review of current understanding of their biological and pathophysiological roles. Mol. Aspects Med. 34, 548-560.
45. Huang C.-C., Weng Y.-H., Lu C.-S., Chu N.-S., and, Yen T.-C., (2003) Dopamine transporter binding in chronic manganese intoxication. J. Neurol. 250, 1335-1339.
46. Huang E., Ong W. Y., and, Connor J. R., (2004) Distribution of divalent metal transporter-1 in the monkey basal ganglia. Neuroscience 128, 487-496.
47. Ingersoll R. T., Montgomery E. B., and, Aposhian H. V., (1999) Central nervous system toxicity of manganese. II: cocaine or reserpine inhibit manganese concentration in the rat brain. Neurotoxicology 20, 467-476.
48. Inoue K., Zhuang L., Maddox D. M., Smith S. B., and, Ganapathy V., (2002) Structure, function, and expression pattern of a novel sodium-coupled citrate transporter (NaCT) cloned from mammalian brain. J. Biol. Chem. 277, 39469-39476.
49. Jamieson S. E., White J. K., Howson J. M. M., et al,. (2005) Candidate gene association study of solute carrier family 11a members 1 (SLC11A1) and 2 (SLC11A2) genes in Alzheimer's disease. Neurosci. Lett. 374, 124-128.
50. Jenkitkasemwong S., Wang C.-Y., Mackenzie B., and, Knutson M., (2012) Physiologic implications of metal-ion transport by ZIP14 and ZIP8. Biometals 25, 643-655.
51. Jiang Y. M., Mo X. A., Du F. Q., et al,. (2006) Effective treatment of manganese-induced occupational Parkinsonism with p-aminosalicylic acid: a case of 17-year follow-up study. J. Occup. Environ. Med. 48, 644-649.
52. Jitrapakdee S., St Maurice M., Rayment I., Cleland W. W., Wallace J. C., and, Attwood P. V., (2008) Structure, mechanism and regulation of pyruvate carboxylase. Biochem. J. 413, 369-387.
53. Kanyo Z. F., Scolnick L. R., Ash D. E., and, Christianson D. W., (1996) Structure of a unique binuclear manganese cluster in arginase. Nature 383, 554-557.
54. Ke Y., Chang Y. Z., Duan X. L., Du J. R., Zhu L., Wang K., Yang X. D., Ho K. P., and, Qian Z.-M., (2005) Age-dependent and iron-independent expression of two mRNA isoforms of divalent metal transporter 1 in rat brain. Neurobiol. Aging 26, 739-748.
55. Kim Y., Kim J. M., Kim J. W., et al,. (2002) Dopamine transporter density is decreased in parkinsonian patients with a history of manganese exposure: what does it mean? Mov. Disord. 17, 568-575.
56. 2+ signaling by thrombin and protease-activated receptor-1-activating peptide in human brain microvascular endothelial cells. Am. J. Physiol. Cell Physiol. 286, C31-C42.
57. Kitzberger R., Madl C., and, Ferenci P., (2005) Wilson disease. Metab. Brain Dis. 20, 295-302.
58. Klos K. J., Ahlskog J. E., Josephs K. A., Fealey R. D., Cowl C. T., and, Kumar N., (2005) Neurologic spectrum of chronic liver failure and basal ganglia T1 hyperintensity on magnetic resonance imaging: probable manganese neurotoxicity. Arch. Neurol. 62, 1385-1390.
59. Koller W. C., Lyons K. E., and, Truly W., (2004) Effect of levodopa treatment for parkinsonism in welders: a double-blind study. Neurology 62, 730-733.
60. Kong S. M. Y., Chan B. K. K., Park J.-S., et al,. (2014) Parkinson's disease-linked human PARK9/ATP13A2 maintains zinc homeostasis and promotes α-Synuclein externalization via exosomes. Hum. Mol. Genet. 23, 2816-2833.
61. La Fontaine S., and, Mercer J. F., (2007) Trafficking of the copper-ATPases, ATP7A and ATP7B: role in copper homeostasis. Arch. Biochem. Biophys. 463, 149-167.
62. Lechpammer M., Clegg M. S., Muzar Z., Huebner P. A., Jin L. W., and, Gospe S. M., Jr, (2014) Pathology of inherited manganese transporter deficiency. Ann. Neurol. 75, 608-612.
63. Lees A. J., Hardy J., and, Revesz T., (2009) Parkinson's disease. Lancet 373, 2055-2066.
64. Leitch S., Feng M., Muend S., Braiterman L. T., Hubbard A. L., and, Rao R., (2011) Vesicular distribution of secretory pathway Ca(2)+-ATPase isoform 1 and a role in manganese detoxification in liver-derived polarized cells. Biometals 24, 159-170.
65. Leyva-Illades D., Chen P., Zogzas C. E., et al,. (2014) SLC30A10 is a cell surface-localized manganese efflux transporter, and parkinsonism-causing mutations block its intracellular trafficking and efflux activity. J. Neurosci. 34, 14079-14095.
66. Liuzzi J. P., and, Cousins R. J., (2004) Mammalian zinc transporters. Annu. Rev. Nutr. 24, 151-172.
67. Liuzzi J. P., Aydemir F., Nam H., Knutson M. D., and, Cousins R. J., (2006) Zip14 (Slc39a14) mediates non-transferrin-bound iron uptake into cells. Proc. Natl Acad. Sci. USA 103, 13612-13617.
68. Lockman P. R., Roder K. E., and, Allen D. D., (2001) Inhibition of the rat blood-brain barrier choline transporter by manganese chloride. J. Neurochem. 79, 588-594.
69. Lucaciu C. M., Dragu C., Copaescu L., and, Morariu V. V., (1997) Manganese transport through human erythrocyte membranes. An EPR study. Biochim. Biophys. Acta 1328, 90-98.
70. Lucchini R. G., Guazzetti S., Zoni S., et al,. (2012) Tremor, olfactory and motor changes in Italian adolescents exposed to historical ferro-manganese emission. Neurotoxicology 33, 687-696.
71. Madejczyk M. S., and, Ballatori N., (2012) The iron transporter ferroportin can also function as a manganese exporter. Biochim. Biophys. Acta 1818, 651-657.
72. 2+ transport pathways in thymic lymphocytes by econazole, miconazole, and SKF 96365. Am. J. Physiol. Cell Physiol. 264, C654-C662.
73. McKie A. T., Marciani P., Rolfs A., et al,. (2000) A novel duodenal iron-regulated transporter, IREG1, implicated in the basolateral transfer of iron to the circulation. Mol. Cell 5, 299-309.
74. Moos T., and, Morgan E., (2000) Transferrin and transferrin receptor function in brain barrier systems. Cell. Mol. Neurobiol. 20, 77-95.
75. Mukhopadhyay S., and, Linstedt A. D., (2011) Identification of a gain-of-function mutation in a Golgi P-type ATPase that enhances Mn2 + efflux and protects against toxicity. Proc. Natl Acad. Sci. USA 108, 858-863.
76. Mukhopadhyay S., Bachert C., Smith D. R., and, Linstedt A. D., (2010) Manganese-induced trafficking and turnover of the cis-Golgi glycoprotein GPP130. Mol. Biol. Cell 21, 1282-1292.
77. Nemeth E., Tuttle M. S., Powelson J., Vaughn M. B., Donovan A., Ward D. M., Ganz T., and, Kaplan J., (2004) Hepcidin regulates cellular iron efflux by binding to ferroportin and inducing its internalization. Science 306, 2090-2093.
78. Park R. M., (2013) Neurobehavioral deficits and parkinsonism in occupations with manganese exposure: a review of methodological issues in the epidemiological literature. Saf. Health Work 4, 123-135.
79. Peng J., Peng L., Stevenson F. F., Doctrow S. R., and, Andersen J. K., (2007) Iron and paraquat as synergistic environmental risk factors in sporadic Parkinson's disease accelerate age-related neurodegeneration. J. Neurosci. 27, 6914-6922.
80. Peng J., Stevenson F. F., Oo M. L., and, Andersen J. K., (2009) Iron-enhanced paraquat-mediated dopaminergic cell death due to increased oxidative stress as a consequence of microglial activation. Free Radic. Biol. Med. 46, 312-320.
81. Quadri M., Federico A., Zhao T., et al,. (2012) Mutations in SLC30A10 cause parkinsonism and dystonia with hypermanganesemia, polycythemia, and chronic liver disease. Am. J. Hum. Genet. 90, 467-477.
82. Racette B. A., McGee-Minnich L., Moerlein S. M., Mink J. W., Videen T. O., and, Perlmutter J. S., (2001) Welding-related parkinsonism: clinical features, treatment, and pathophysiology. Neurology 56, 8-13.
83. Reddi A. R., Jensen L. T., Naranuntarat A., Rosenfeld L., Leung E., Shah R., and, Culotta V. C., (2009) The overlapping roles of manganese and Cu/Zn SOD in oxidative stress protection. Free Radic. Biol. Med. 46, 154-162.
84. Roth J. A., Horbinski C., Higgins D., Lein P., and, Garrick M. D., (2002) Mechanisms of manganese-induced rat pheochromocytoma (PC12) cell death and cell differentiation. Neurotoxicology 23, 147-157.
85. Salazar J., Mena N., Hunot S., et al,. (2008) Divalent metal transporter 1 (DMT1) contributes to neurodegeneration in animal models of Parkinson's disease. Proc. Natl Acad. Sci. USA 105, 18578-18583.
86. Sikk K., Haldre S., Aquilonius S. M., et al,. (2013) Manganese-induced parkinsonism in methcathinone abusers: bio-markers of exposure and follow-up. Eur. J. Neurol. 20, 915-920.
87. Smith E. A., Newland P., Bestwick K. G., and, Ahmed N., (2013) Increased whole blood manganese concentrations observed in children with iron deficiency anaemia. J. Trace Elem. Med. Biol. 27, 65-69.
88. Subramaniam V. N., Summerville L., and, Wallace D., (2002) Molecular and cellular characterization of transferrin receptor 2. Cell Biochem. Biophys. 36, 235-239.
89. Tan J., Zhang T., Jiang L., Chi J., Hu D., Pan Q., Wang D., and, Zhang Z., (2011) Regulation of intracellular manganese homeostasis by Kufor-Rakeb syndrome-associated ATP13A2 protein. J. Biol. Chem. 286, 29654-29662.
90. Ton V. K., Mandal D., Vahadji C., and, Rao R., (2002) Functionet alxpression in yeast of the human secretory pathway Ca(2+), Mn(2+)-ATPase defective in Hailey-Hailey disease. J. Biol. Chem. 277, 6422-6427.
91. Traiffort E., Ruat M., O'Regan S., and, Meunier F. M., (2005) Molecular characterization of the family of choline transporter-like proteins and their splice variants. J. Neurochem. 92, 1116-1125.
92. Troadec M. B., Ward D. M., Lo E., Kaplan J., and, De Domenico I., (2010) Induction of FPN1 transcription by MTF-1 reveals a role for ferroportin in transition metet alfflux. Blood 116, 4657-4664.
93. 2+ dyshomeostasis caused by loss of ATP13A2/PARK9 leads to lysosomal dysfunction and alpha-synuclein accumulation. Hum. Mol. Genet. 23, 2791-2801.
94. Tuschl K., Mills P. B., Parsons H., Malone M., Fowler D., Bitner-Glindzicz M., and, Clayton P. T., (2008) Hepatic cirrhosis, dystonia, polycythaemia and hypermanganesaemia-a new metabolic disorder. J. Inherit. Metab. Dis. 31, 151-163.
95. Tuschl K., Clayton P. T., Gospe S. M., Jr, et al,. (2012) Syndrome of hepatic cirrhosis, dystonia, polycythemia, and hypermanganesemia caused by mutations in SLC30A10, a manganese transporter in man. Am. J. Hum. Genet. 90, 457-466.
96. Tuschl K., Mills P. B., and, Clayton P. T., (2013) Manganese and the brain. Int. Rev. Neurobiol. 110, 277-312.
97. Vidal S., Belouchi A. M., Cellier M., Beatty B., and, Gros P., (1995) Cloning and characterization of a second human NRAMP gene on chromosome 12q13. Mamm. Genome 6, 224-230.
98. Wedler F. C., Denman R. B., and, Roby W. G., (1982) Glutamine synthetase from ovine brain is a manganese(II) enzyme. Biochemistry 21, 6389-6396.
99. Williams K., Wilson M. A., and, Bressler J., (2000) Regulation and developmentet alxpression of the divalent metal-ion transporter in the rat brain. Cell. Mol. Biol. (Noisy-le-Grand) 46, 563-571.
100. Wu L. J.-C., Leenders A. G. M., Cooperman S., et al,. (2004) Expression of the iron transporter ferroportin in synaptic vesicles and the blood-brain barrier. Brain Res. 1001, 108-117.
101. Xiong L., Dion P., Montplaisir J., et al,. (2007) Molecular genetic studies of DMT1 on 12q in French-Canadian restless legs syndrome patients and families. Am. J. Med. Genet. B Neuropsychiatr. Genet. 144B, 911-917.
102. Yin Z., Jiang H., Lee E. S., Ni M., Erikson K. M., Milatovic D., Bowman A. B., and, Aschner M., (2010) Ferroportin is a manganese-responsive protein that decreases manganese cytotoxicity and accumulation. J. Neurochem. 112, 1190-1198.
103. Zeron H. M., Rodriguez M. R., Montes S., and, Castaneda C. R., (2011) Blood manganese levels in patients with hepatic encephalopathy. J. Trace Elem. Med. Biol. 25, 225-229.