Manganese efflux in Parkinsonism: Insights from newly characterized SLC30A10 mutations

Biochemical and Biophysical Research Communications

Volumn 432, Issue 1, 2013, Pages 1-4

  DeWitt, Margaret R ^a   Chen, Pan ^b   Aschner, Michael ^a,b  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Ferroportin 1; Iron; Manganese; Parkinson's disease; SLC30A10

Indexed keywords

CARRIER PROTEIN; FERROPORTIN; IRON; LEVODOPA; MANGANESE; NATURAL RESISTANCE ASSOCIATED MACROPHAGE PROTEIN 2; SLC30A10 PROTEIN; TRANSFERRIN RECEPTOR; UNCLASSIFIED DRUG;

DOPAMINERGIC NERVE CELL; DRUG ABSORPTION; DYSTONIA; GENE IDENTIFICATION; GENE MUTATION; HISTOPATHOLOGY; HUMAN; HYPERMAGNESEMIA; INTESTINE; NEUROIMAGING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PARKINSON DISEASE; PARKINSONISM; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; SHORT SURVEY; SUBSTANTIA NIGRA; SYMPTOM;

CATION TRANSPORT PROTEINS; HUMANS; ION TRANSPORT; MANGANESE; MUTATION; PARKINSONIAN DISORDERS;

PARKINSONIA;

EID: 84875364921     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2013.01.058     Document Type: Short Survey

References (75)

1. Bowman A.B., Kwakye G.F., Hernández E.H., Aschner M. Role of manganese in neurodegenerative diseases. J. Trace Elem. Med. Biol. 2011, 25:191-203.
2. Aschner M., Erikson K.M., Hernández E.H., Tjalkens R. Manganese and its role in disease: from transport to neuropathology. Neuromolecular Med. 2009, 11:252-266.
3. Morello M., Zatta P., Zambenedetti P., Martorana A., D'Angelo V., Melchiorri G., Bernardi G., Sancesario G. Manganese intoxication decreases the expression of manganoproteins in the rat basal ganglia: an immunohistochemical study. Brain Res. Bull. 2007, 74:406-415.
4. Sidoryk-Wegrzynowicz M., Lee E., Albrecht J., Aschner M. Manganese disrupts astrocyte glutamine transporter expression and function. J. Neurochem. 2009, 110:822-830.
5. Stanwood G.D., Leitch D.B., Savchenko V., Wu J., Fitsanakis V.A., Anderson D.J., Stankowski J.N., Aschner M., McLaughlin B. Manganese exposure is cytotoxic and alters dopaminergic and GABAergic neurons within the basal ganglia. J. Neurochem. 2009, 110:378-389.
6. Kern C., Smith D. Preweaning Mn exposure leads to prolonged astrocyte activation and lasting effects on the dopaminergic system in adult male rats. Synapse 2010, 65:532-544.
7. Yokoyama H., Uchida H., Kuroiwa H., Kasahara J., Araki T. Role of glial cells in neurotoxin-induced animal models of Parkinson's disease. Neurol. Sci. 2011, 32:1-7.
8. Kim Y., Kim J.W., Ito K., Lim H.S., Cheong H.K., Kim J.Y., Shin Y.C., Kim K.S., Moon Y. Idiopathic parkinsonism with superimposed manganese exposure: utility of positron emission tomography. Neurotoxicology 1999, 20:249-252.
9. Cersosimo M.G., Koller W.C. The diagnosis of manganese-induced parkinsonism. Neurotoxicology 2006, 27:340-346.
10. Racette B.A., McGee-Minnich L., Moerlein S.M., Mink J.W., Videen T.O., Perlmutter J.S. Welding-related parkinsonism: clinical features, treatment, and pathophysiology. Neurology 2001, 56:8-13.
11. Sriram K., Lin G.X., Jefferson A.M., Roberts J.R., Chapman R.S., Chen B.T., Soukup J.M., Ghio A.J., Antonini J.M. Dopaminergic neurotoxicity following pulmonary exposure to manganese-containing welding fumes. Arch. Toxicol. 2010, 84:521-540.
12. Racette B.A., Criswell S.R., Lundin J.I., Hobson A., Seixas N., Kotzbauer P.T., Evanoff B.A., Perlmutter J.S., Zhang J., Sheppard L., Checkoway H. Increased risk of parkinsonism associated with welding exposure. Neurotoxicology 2012, 33:1356-1361.
13. Criswell S.R., Perlmutter J.S., Huang J.L., Golchin N., Flores H.P., Hobson A., Aschner M., Erikson K.M., Checkoway H., Racette B.A. Basal ganglia intensity indices and diffusion weighted imaging in manganese-exposed welders. Occup. Environ. Med. 2012, 69:437-443.
14. Dickerson R.N. Manganese intoxication and parenteral nutrition. Nutrition 2001, 17:689-693.
15. Chalela J.A., Bonillha L., Neyens R., Hays A. Manganese encephalopathy: an under-recognized condition in the intensive care unit. Neurocrit. Care 2010, 14:456-458.
16. Normandin L., Panisset M., Zayed J. Manganese neurotoxicity: behavioral, pathological, and biochemical effects following various routes of exposure. Rev. Environ. Health 2002, 17:189-217.
17. Calne D.B., Chu N.S., Huang C.C., Lu C.S., Olanow W. Manganism and idiopathic parkinsonism: similarities and differences. Neurology 1994, 44:1583-1586.
18. Gorell J.M., Rybicki B.A., Cole Johnson C., Peterson E.L. Occupational metal exposures and the risk of Parkinson's disease. Neuroepidemiology 1999, 18:303-308.
19. Hudnell H.K. Effects from environmental Mn exposures: a review of the evidence from non-occupational exposure studies. Neurotoxicology 1999, 20:379-397.
20. Finkelstein M., Jerrett M. A study of the relationships between Parkinson's disease and markers of traffic-derived and environmental manganese air pollution in two canadian cities. Environ. Res. 2007, 104:420-432.
21. Gorell J.M., Johnson C.C., Rybicki B.A., Peterson E.L., Kortsha G.X., Brown G.G., Richardson R.J. Occupational exposure to manganese, copper, lead, iron, mercury and zinc and the risk of Parkinson's disease. Neurotoxicology 1999, 20:239-247.
22. Pienaar I.S., Götz J., Feany M.B. Parkinson's disease: insights from non-traditional model organisms. Prog. Neurobiol. 2010, 92:558-571.
23. Forno L.S. Neuropathology of Parkinson's disease. J. Neuropathol. Exp. Neurol. 1996, 55:259-272.
24. Kumar K.R., Lohmann K., Klein C. Genetics of Parkinson disease and other movement disorders. Curr. Opin. Neurol. 2012, 25:466-474.
25. Nuytemans K., Theuns J., Cruts M., Van Broeckhoven C. Genetic etiology of Parkinson disease associated with mutations in the SNCA, PARK2, PINK1, PARK7, and LRRK2 genes: a mutation update. Hum. Mutat. 2010, 31:763-780.
26. Bonifati V. Genetics of Parkinson's disease. Minerva Med. 2005, 96:175-186.
27. Lees A.J., Selikhova M., Andrade L.A., Duyckaerts C. The black stuff and Konstantin Nikolaevich Tretiakoff. Mov. Disord. 2008, 23:777-783.
28. Lu C.S., Huang C.C., Chu N.S., Calne D.B. Levodopa failure in chronic manganism. Neurology 1994, 44:1600-1602.
29. Erikson K., Aschner M. Increased manganese uptake by primary astrocyte cultures with altered iron status is mediated primarily by divalent metal transporter. Neurotoxicology 2006, 27:125-130.
30. Aboud A.A., Tidball A.M., Kumar K.K., Neely M.D., Ess K.C., Erikson K.M., Bowman A.B. Genetic risk for Parkinson's disease correlates with alterations in neuronal manganese sensitivity between two human subjects. Neurotoxicology 2012, 1-7.
31. Gitler A., Chesi A., Geddie M., Strathearn K., Hamamichi S., Hill K., Caldwell K., Caldwell G., Cooper A., Rochet J., Lindquist S. Alpha-synuclein is part of a diverse and highly conserved interaction network that includes PARK9 and manganese toxicity. Nat. Genet. 2009, 41:308-315.
32. Tan J., Zhang T., Jiang L., Chi J., Hu D., Pan Q., Wang D., Zhang Z. Regulation of intracellular manganese homeostasis by Kufor-Rakeb syndrome-associated ATP13A2 protein. J. Biol. Chem. 2011, 286:29654-29662.
33. Yang H., Zhou H.Y., Li B., Niu G.Z., Chen S.D. Downregulation of parkin damages antioxidant defenses and enhances proteasome inhibition-induced toxicity in PC12 cells. J. Neuroimmune pharmacol. 2007, 2:276-283.
34. Schneider S.A., Bhatia K.P. Rare causes of dystonia parkinsonism. Curr. Neurol. Neurosci. Rep. 2010, 10:431-439.
35. Roth J.A., Singleton S., Feng J., Garrick M., Paradkar P.N. Parkin regulates metal transport via proteasomal degradation of the 1B isoforms of divalent metal transporter 1. J. Neurochem. 2010, 113:454-464.
36. Fukushima T., Tan X., Luo Y., Kanda H. Relationship between blood levels of heavy metals and Parkinson's disease in china. Neuroepidemiology 2010, 34:18-24.
37. Au C., Benedetto A., Aschner M. Manganese transport in eukaryotes: the role of DMT1. Neurotoxicology 2008, 29:569-576.
38. He Q., Du T., Yu X., Xie A., Song N., Kang Q., Yu J., Tan L., Xie J., Jiang H. DMT1 polymorphism and risk of Parkinson's disease. Neurosci. Lett. 2011, 501:128-131.
39. Settivari R., Levora J., Nass R. The divalent metal transporter homologues SMF-1/2 mediate dopamine neuron sensitivity in caenorhabditis elegans models of manganism and parkinson disease. J. Biol. Chem. 2009, 284:35758-35768.
40. Aschner M., Guilarte T.R., Dydak U., Criswell S.R., Zheng W. Neurotoxicology 2012, 33:881-886. 10.1016/j.neuro.2011.12.010.
41. Moos T., Rosengren Nielsen T. Ferroportin in the postnatal rat brain: implications for axonal transport and neuronal export of iron. Semin. Pediatr. Neurol. 2006, 13:149-157.
42. Benedetto A., Au C., Aschner M. Manganese-induced dopaminergic neurodegeneration: insights into mechanisms and genetics shared with Parkinson's disease. Chem. Rev. 2009, 109:4862-4884.
43. Greco V., De Marco E.V., Rocca F.E., Annesi F., Civitelli D., Provenzano G., Tarantino P., Scornaienchi V., Pucci F., Salsone M., Novellino F., Morelli M., Paglionico S., Gambardella A., Quattrone A., Annesi G. Association study between four polymorphisms in the HFE, TF and TFR genes and Parkinson's disease in southern italy. Neurol. Sci. 2011, 32:525-527.
44. Ward D.M., Kaplan J. Ferroportin-mediated iron transport: expression and regulation. BBA-Mol. Cell Res. 1823, 2012:1426-1433.
45. Erikson K.M., Shihabi Z.K., Aschner J.L., Aschner M. Manganese accumulates in iron-deficient rat brain regions in a heterogeneous fashion and is associated with neurochemical alterations. Biol Trace Elem. Res. 2002, 87:143-156.
46. Fitsanakis V.A., Zhang N., Garcia S., Aschner M. Manganese (Mn) and iron (Fe): interdependency of transport and regulation. Neurotox. Res. 2009, 18:124-131.
47. Wang X., Li G.J., Zheng W. Efflux of iron from the cerebrospinal fluid to the blood at the blood-csf barrier: effect of manganese exposure. Exp. Biol. Med. 2008, 233:1561-1571.
48. Yin Z., Jiang H., Lee E.-S.Y., Ni M., Erikson K.M., Milatovic D., Bowman A.B., Aschner M. Ferroportin is a manganese-responsive protein that decreases manganese cytotoxicity and accumulation. J. Neurochem. 2010, 112:1190-1198.
49. De Domenico I., Ward D.M., Musci G., Kaplan J. Evidence for the multimeric structure of ferroportin. Blood 2007, 109:2205-2209.
50. Madejczyk M.S., Ballatori N. The iron transporter ferroportin can also function as a manganese exporter. BBA-Biomembranes 1818, 2012:651-657.
51. Liu X.-B., Yang F., Haile D.J. Functional consequences of ferroportin 1 mutations. Blood Cells Mol. Dis. 2005, 35:33-46.
52. Mayr R., Griffiths W.J.H., Hermann M., McFarlane I., Halsall D.J., Finkenstedt A., Douds A., Davies S.E., Janecke A.R., Vogel W., Cox T.M., Zoller H. Identification of mutations in SLC40A1 that affect ferroportin function and phenotype of human ferroportin iron overload. Gastroenterology 2011, 140:2056-2063. e2051.
53. Speletas M., Kioumi A., Loules G., Hytiroglou P., Tsitouridis J., Christakis J., Germenis A.E. Analysis of SLC40A1 gene at the mRNA level reveals rapidly the causative mutations in patients with hereditary hemochromatosis type IV. Blood Cells Mol. Dis. 2008, 40:353-359.
54. Hoppe M., Brün B., Larsson M.P., Moraeus L., Hulthén L. Heme iron-based dietary intervention for improvement of iron status in young women. Nutrition 2013, 29:89-95.
55. R.C. Hider, X. Kong, Iron speciation in the cytosol: an overview, Dalton Tras. (2012), [Epub ahead of print].
56. Fitsanakis V.A., Zhang N., Garcia S., Aschner M. Manganese (Mn) and iron (Fe): interdependency of transport and regulation. Neurotox. Res. 2010, 18:124-131.
57. Mochizuki H., Yasuda T. Iron accumulation in Parkinson's disease. J. Neural. Transm. 2012, 119:1511-1514.
58. Moos T., Nielsen T.R., Skjørringe T., Morgan E.H. Iron trafficking inside the brain. J. Neurochem. 2007, 103:1730-1740.
59. Dexter D.T., Wells F.R., Lees A.J., Agid F., Agid Y., Jenner P., Marsden C.D. Increased nigral iron content and alterations in other metal ions occurring in brain in Parkinson's disease. J. Neurochem. 1989, 52:1830-1836.
60. Erikson K.M., Syversen T., Aschner J.L., Aschner M. Interactions between excessive manganese exposures and dietary iron-deficiency in neurodegeneration. Environ. Toxicol. pharmacol. 2005, 19:415-421.
61. Beard J., Erikson K., Jones B.C. Neonatal iron deficiency results in irreversible changes in dopamine function in rats. J. Nutr. 2003, 133:1174-1179.
62. Aschner M., Shanker G., Erikson K., Yang J., Mutkus L.A. The uptake of manganese in brain endothelial cultures. Neurotoxicology 2002, 23:165-168.
63. Erikson K.M., Jones B.C., Beard J.L. Iron deficiency alters dopamine transporter functioning in rat striatum. J. Nutr. 2000, 130:2831-2837.
64. Erikson K.M., Pinero D.J., Connor J.R., Beard J.L. Regional brain iron, ferritin and transferrin concentrations during iron deficiency and iron repletion in developing rats. J. Nutr. 1997, 127:2030-2038.
65. Zoller H., Koch R.O., Theurl I., Obrist P., Pietrangelo A., Montosi G., Haile D.J., Vogel W., Weiss G. Expression of the duodenal iron transporters divalent-metal transporter 1 and ferroportin 1 in iron deficiency and iron overload. Gastroenterology 2001, 120:1412-1419.
66. Nam H., Knutson M.D. Effect of dietary iron deficiency and overload on the expression of ZIP metal-ion transporters in rat liver. Biometals 2012, 25:115-124.
67. Brna P., Gordon K., Dooley J.M., Price V. Manganese toxicity in a child with iron deficiency and polycythemia. J. Child Neurol. 2011, 26:891-894.
68. Kim Y., Lee B.K. Iron deficiency increases blood manganese level in the korean general population according to KNHANES 2008. Neurotoxicology 2011, 32:247-254.
69. Tuschl K., Clayton P.T., Gospe S.M., Gulab S., Ibrahim S., Singhi P., Aulakh R., Ribeiro R.T., Barsottini O.G., Zaki M.S., Del Rosario M.L., Dyack S., Price V., Rideout A., Gordon K., Wevers R.A., Chong W.K.K., Mills P.B. Syndrome of hepatic cirrhosis, dystonia, polycythemia, and hypermanganesemia caused by mutations in SLC30A10, a manganese transporter in man. Am. J. Hum. Genet. 2012, 90:457-466.
70. Kwik-Uribe C., Smith D. Temporal responses in the disruption of iron regulation by manganese. J. Neurosci. Res. 2006, 83:1601-1610.
71. Crooks D.R., Ghosh M.C., Braun-Sommargren M., Rouault T.A., Smith D. Manganese targets m-aconitase and activates iron regulatory protein 2 in AF5 GABAergic cells. J. Neurosci. Res. 2007, 85:1797-1809.
72. Stamelou M., Tuschl K., Chong W.K., Burroughs A.K., Mills P.B., Bhatia K.P., Clayton P.T. Dystonia with brain manganese accumulation resulting from SLC30A10mutations: a new treatable disorder. Mov. Disord. 2012, 27:1317-1322.
73. Quadri M., Federico A., Zhao T., Breedveld G.J., Battisti C., Delnooz C., Severijnen L.-A., Di Toro Mammarella L., Mignarri A., Monti L., Sanna A., Lu P., Punzo F., Cossu G., Willemsen R., Rasi F., Oostra B.A., van de Warrenburg B.P., Bonifati V. Mutations in SLC30A10 cause Parkinsonism and dystonia with hypermanganesemia, polycythemia, and chronic liver disease. Am. J. Hum. Genet. 2012, 90:467-477.
74. Tuschl K., Mills P.B., Parsons H., Malone M., Fowler D., Bitner-Glindzicz M., Clayton P.T. Hepatic cirrhosis, dystonia, polycythaemia and hypermanganesaemia-a new metabolic disorder. J. Inherit. Metab. Dis. 2008, 31:151-163.
75. Baquer N.Z., Taha A., Kumar P., McLean P., Cowsik S.M., Kale R.K., Singh R., Sharma D. A metabolic and functional overview of brain aging linked to neurological disorders. Biogerontology 2009, 10:377-413.