Manganese accumulation in membrane fractions of primary astrocytes is associated with decreased γ-aminobutyric acid (GABA) uptake, and is exacerbated by oleic acid and palmitate

Environmental Toxicology and Pharmacology

Volumn 37, Issue 3, 2014, Pages 1148-1156

  Fordahl, Steve C ^a   Erikson, Keith M ^a  

^a UNIVERSITY OF NORTH CAROLINA AT GREENSBORO   (United States)

Author keywords

Astrocyte; Fatty acid; GABA; Manganese; Neurotoxicity

Indexed keywords

4 AMINOBUTYRIC ACID CARRIER; MANGANESE; OLEIC ACID; PALMITIC ACID; 4 AMINOBUTYRIC ACID; PALMITIC ACID DERIVATIVE; PROTEIN KINASE C; SLC6A11 PROTEIN, RAT;

4 AMINOBUTYRIC ACID UPTAKE; ANIMAL CELL; ARTICLE; ASTROCYTE; CELL MEMBRANE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; RAT; ANIMAL; CELL CULTURE; DRUG EFFECTS; METABOLISM; SPRAGUE DAWLEY RAT; TOXICITY;

ANIMALS; ASTROCYTES; CELL MEMBRANE; CELLS, CULTURED; GABA PLASMA MEMBRANE TRANSPORT PROTEINS; GAMMA-AMINOBUTYRIC ACID; MANGANESE; OLEIC ACID; PALMITATES; PROTEIN KINASE C; RATS, SPRAGUE-DAWLEY;

EID: 84899835960     PISSN: 13826689     EISSN: 18727077     Source Type: Journal    
DOI: 10.1016/j.etap.2014.03.016     Document Type: Article

References (45)

1. Allen J.W., Mutkus L.A., Aschner M. Isolation of neonatal rat cortical astrocytes for primary cultures. Curr. Protoc. Toxicol. 2001, 4:12.4.1-12.4.15.
2. Allen J.A., Halverson-Tamboli R.A., Rasenick M.M. Lipid raft microdomains and neurotransmitter signaling. Nat. Rev. Neurosci. 2007, 8(2):128-140.
3. Anderson J.G., Cooney P.T., Erikson K.M. Inhibition of DAT function attenuates manganese accumulation in the globus pallidus. Environ. Toxicol. Pharmacol. 2007, 23:179-184.
4. Anderson J.G., Cooney P.T., Erikson K.M. Brain manganese accumulation is inversely related to γ-amino butyric acid uptake in male and female rats. Toxicol. Sci. 2007, 95(1):188-195.
5. Anderson J.G., Fordahl S.C., Cooney P.T., Weaver T.L., Colyer C.L., Erikson K.M. Manganese exposure alters extracellular GABA, GABA receptor and transporter protein and mRNA levels in the developing rat brain. Neurotoxicology 2008, 29:1044-1053.
6. Aschner M., Gannon M., Kimelberg H.K. Manganese uptake and efflux in cultured rat astrocytes. J. Neurochem. 1992, 58(2):730-735.
7. Bonilla E. Increased GABA content in caudate nucleus of rats after chronic manganese chloride administration. J. Neurochem. 1978, 31:551-552.
8. de Boer V.C.J., Dihal A.A., van der Woude H., Arts I.C.W., Wolffram S., Alink G.M., Rietjens I.M.C.M., Keijer J., Hollman P.C.H. Tissue distribution of quercetin in rats and pigs. J. Nutr. 2005, 135:1617-1618.
9. Erikson K.M., Aschner M. Manganese neurotoxicity and glutamate-GABA interaction. Neurochem. Int. 2003, 43(4-5):475-480.
10. Erikson K.M., Aschner M. Manganese causes differential regulation of glutamate transporter (GLAST) taurine transporter and metallothionein in cultured rat astrocytes. Neurotoxicology 2002, 23:595-602.
11. Fisher N.S., Jones G.J. Heavy metals and marine phytoplankton: correlation of toxicity and sulfhydryl-binding. J. Phycol. 1981, 17:108-111.
12. Fordahl S.C., Anderson J.G., Cooney P.T., Weaver T.L., Colyer C.L., Erikson K.M. Manganese exposure inhibits the clearance of extracellular GABA and influenced taurine homeostasis in the striatum of developing rats. Neurotoxicology 2010, 31:639-646.
13. Fordahl S., Cooney P., Qiu Y., Xie G., Jia W., Erikson K.M. Waterborne manganese exposure alters plasma, brain, and liver metabolites accompanied by changes in stereotypic behaviors. Neurotoxicol. Teratol. 2012, 34:27-36.
14. Gadea A., Lopez-Colome A.M. Glial transporters for glutamate, glycine, and GABA: II GABA transporters. J. Neurosci. Res. 2001, 63(6):461-468.
15. Gianutsos G., Murray M.T. Alterations in brain dopamine and GABA following inorganic or organic manganese administration. Neurotoxicology 1982, 3(3):75-81.
16. Grabauskas G. Time course of GABA in the synaptic clefts of inhibitory synapses in the rostral nucleus of the solitary tract. Neurosci. Lett. 2005, 373:10-15.
17. Gwiazda R.H., Lee D., Sheridan J., Smith D.R. Low cumulative manganese exposure affects striatal GABA but not dopamine. Neurotoxicology 2002, 23:69-76.
18. Hulbert A.J., Turner N., Storlein L.H., Else P. Dietary fats and membrane function: implications for metabolism and disease. Biol. Rev. 2005, 80(1):155-169.
19. Kersanté F., Rowley S.C., Pavlov I., Gutièrrez-Macinas M., Semyanov A., Reul J.M.H.M., Walker M.C., Linthorst A.C.E. A functional role for both GABA transporter-1 and GABA transporter-3 in the modulation of extracellular GABA and GABAergic tonic conductances in the rat hippocampus. J. Physiol. 2012, 591(10):2429-2441.
20. Khan W.A., Blobe G.C., Hannun Y.A. Activation of protein kinase C by oleic acid. J. Biol. Chem. 1992, 267(6):3605-3612.
21. Kitazawa M., Anantharam V., Yang Y., Hirata Y., Kanthasamy A., Kanthasamy A.G. Activation of protein kinase Cδ by proteolytic cleavage contributes to manganese-induced apoptosis in dopaminergic cells: protective role of Bcl-2. Biochem. Pharmacol. 2005, 69:133-146.
22. Latchoumycandane C., Anantharam V., Kitazawa M., Yang Y., Kanthasamy A., Kanthasamy A.G. Protein kinase Cδ is a key downstream mediator of manganese-induced apoptosis in dopaminergic neuronal cells. J. Pharmacol. Exp. Ther. 2005, 313(1):46-55.
23. Malecki E.A. Manganese toxicity is associated with mitochondrial dysfunction and DNA fragmentation in rat primary striatal neurons. Brain Res. Bull. 2001, 55(2):225-228.
24. Milatovic D., Yin Z., Gupta R.C., Sidoryk S., Albrecht J., Aschner J.L., Aschner M. Manganese induces oxidative impairment in cultured rat astrocytes. Toxicol. Sci. 2007, 98(1):198-205.
25. Milatovic D., Zaja-Milatovic S., Gupta R.C., Yu Y., Aschner M. Oxidative damage and neurodegeneration in manganese-induced neurotoxicity. Toxicol. Appl. Pharmacol. 2009, 240:219-225.
26. Norregaard L., Frederiksen D., Nielsen E.Ø., Gether U. Delineation of an endogenous zinc-binding site in the human dopamine transporter. EMBO J. 1998, 17(15):4266-4273.
27. North P., Fleischer S. Alteration of synaptic membrane cholesterol/phospholipid ratio using a lipid transfer protein. J. Biol. Chem. 1982, 258(2):1242-1253.
28. Quick M.W., Hu J., Wang D., Zhang H.Y. Regulation of a γ-aminobutyric acid transporter by reciprocal tyrosine and serine phosphorylation. J. Biol. Chem. 2004, 279(16):15961-15967.
29. Quick M.W. The role of SNARE proteins in trafficking and function of neurotransmitter transporters. Handb. Exp. Pharmacol. 2006, 175:181-196.
30. Ragheb R., Shanab G.M.L., Medhat A.M., Seoudi D.M., Adeli D., Fantus I.G. Free fatty acid-induced muscle insulin resistance and glucose uptake dysfunction: evidence for PKC activation and oxidative stress-activated signaling pathways. Biochem. Biophys. Res. Commun. 2009, 389:211-216.
31. Rhoads D.E., Kaplan M.A., Peterson N.A., Raghupathy E. Effects of free fatty acids on synaptosomal amino acid uptake systems. J. Neurochem. 1982, 38:1255-1260.
32. Sato K., Betz H., Schloss P. The recombinant GABA transporter GAT1 is downregulated upon activation of protein kinase C. FEBS Lett. 1995, 375:99-102.
33. Schumann J., Leichtle A., Thiery J., Fuhrmann H. Fatty acid and peptide profiles in plasma membrane and membrane rafts of PUFA supplemented RAW264.7 macrophages. PLoS ONE 2011, 6(8):e24066.
34. Sidoryk-Wegrzynowicz M., Lee E., Mingwei N., Aschner M. Disruption of astrocytic glutamine turnover by manganese is mediated by the protein kinase C pathway. Glia 2011, 59:1732-1743.
35. Suzuki Y., Mouri T., Suzuki Y., Nishiyama K., Fujii N. Study of subacute toxicity of manganese dioxide in monkeys. Tokushima J. Exp. Med. 1975, 22:5-10.
36. Takeda A., Sotogaku N., Oku N. Manganese influences the levels of neurotransmitters in synapses in rat brain. Neuroscience 2002, 114:669-674.
37. Takeda A., Sotogaku N., Oku N. Influence of manganese on the release of neurotransmitters in rat striatum. Brain Res. 2003, 965(1-2):279-282.
38. Tracqui A., Tayot J., Kintz P., Alves G., Bosque M.A., Mangin P. Determination of manganese in human brain samples. Forensic Sci. Int. 1995, 76:199-203.
39. Troeger M.B., Rafalowska U., Erecińska M. Effect of oleate on neurotransmitter transport and other plasma membrane functions in rat brain synaptosomes. J. Neurochem. 1984, 42:1735-1742.
40. Wang D., Deken S.L., Whitworth T.L., Quick M.W. Syntaxin 1A inhibits GABA flux, efflux, and exchange mediated by the rat brain GABA transporter GAT1. Mol. Pharmacol. 2003, 64(4):905-913.
41. Wang D., Quick M.W. Trafficking of the plasma membrane GABA transporter GAT1: size and rates of an acutely recycling pool. J. Biol. Chem. 2005, 280(19):18703-18709.
42. Whitworth T.L., Quick M.W. Substrait-induced regulation of γ-aminobutyric acid transporter Trafficking requires tyrosine phosphorylation. J. Biol. Chem. 2001, 276(46):42932-42937.
43. Yiin S.J., Lin T.H., Shih T.S. Lipid peroxidation in workers exposed to manganese. Scand. J. Work. Environ. Health 1996, 22(5):381-386.
44. Yoon H., Kim D.S., Lee G.H., Kim K.W., Kim H.R., Chae H.J. Apoptosis induced by manganese on neuronal SK-N-MC cell line: endoplasmic reticulum (ER) stress and mitochondria dysfunction. Eviron. Health Toxicol. 2011, 26:e2011017.
45. Zomot E., Kanner B.I. The Interaction of the γ-aminobutyric acid transporter GAT-1 with the neurotransmitter is selectively impaired by sulfhydryl modification of a conformationally sensitive cysteine residue engineered into extracellular loop IV. J. Biol. Chem. 2003, 278:42950-42958.