Regulation of the Na+-coupled glutamate transporter EAAT3 by PIKfyve

Neurochemistry International

Volumn 54, Issue 5-6, 2009, Pages 372-377

  Klaus, Fabian ^a   Gehring, Eva Maria ^a   Zürn, Agathe ^a   Laufer, Joerg ^a   Lindner, Ricco ^a   Strutz Seebohm, Nathalie ^a   Tavaré, Jeremy M ^b   Rothstein, Jeffrey D ^c   Boehmer, Christoph ^a,d   Palmada, Monica ^a,d   Gruner, Ivonne ^a   Lang, Undine E ^e   Seebohm, Guiscard ^a   Lang, Florian ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF DUISBURG ESSEN   (Germany)

^e CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

Excitatory amino acid transporter 3; Glucocorticoids; Glutamate transport; Neuroexcitability; Neurotransmission; PIP5K3

Indexed keywords

AMINO ACID; GLUTAMATE TRANSPORTER; GLUTAMATE TRANSPORTER EAAT3; PHOSPHATIDYLINOSITOL 3 PHOSPHATE; PHOSPHATIDYLINOSITOL 3 PHOSPHATE PIKFYVE; SERUM AND GLUCOCORTICOID REGULATED KINASE 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; XENOPUS;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; CELL MEMBRANE; EXCITATORY AMINO ACID TRANSPORTER 3; FEMALE; GLUTAMIC ACID; HUMANS; IMMEDIATE-EARLY PROTEINS; MUTATION; OOCYTES; PATCH-CLAMP TECHNIQUES; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; XENOPUS LAEVIS;

MAMMALIA;

EID: 61449221817     PISSN: 01970186     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuint.2009.01.002     Document Type: Article

References (73)

1. Alessi D.R., Deak M., Casamayor A., Caudwell F.B., Morrice N., Norman D.G., Gaffney P., Reese C.B., MacDougall C.N., Harbison D., Ashworth A., and Bownes M. 3-Phosphoinositide-dependent protein kinase-1 (PDK1): structural and functional homology with the Drosophila DSTPK61 kinase. Curr. Biol. 7 (1997) 776-789
2. Amara S.G., and Fontana A.C. Excitatory amino acid transporters: keeping up with glutamate. Neurochem. Int. 41 (2002) 313-318
3. Berwick D.C., Dell G.C., Welsh G.I., Heesom K.J., Hers I., Fletcher L.M., Cooke F.T., and Tavare J.M. Protein kinase B phosphorylation of PIKfyve regulates the trafficking of GLUT4 vesicles. J. Cell. Sci. 117 (2004) 5985-5993
4. Bianchi M.G., Rotoli B.M., Dall'Asta V., Gazzola G.C., Gatti R., and Bussolati O. PKC-dependent stimulation of EAAT3 glutamate transporter does not require the integrity of actin cytoskeleton. Neurochem. Int. 48 (2006) 341-349
5. Biondi R.M., Kieloch A., Currie R.A., Deak M., and Alessi D.R. The PIF-binding pocket in PDK1 is essential for activation of S6K and SGK, but not PKB. EMBO J. 20 (2001) 4380-4390
6. Boehmer C., Rajamanickam J., Schniepp R., Kohler K., Wulff P., Kuhl D., Palmada M., and Lang F. Regulation of the excitatory amino acid transporter EAAT5 by the serum and glucocorticoid dependent kinases SGK1 and SGK3. Biochem. Biophys. Res. Commun. 329 (2005) 738-742
7. Chan H., Zwingmann C., Pannunzio M., and Butterworth R.F. Effects of ammonia on high affinity glutamate uptake and glutamate transporter EAAT3 expression in cultured rat cerebellar granule cells. Neurochem. Int. 43 (2003) 137-146
8. Collin M., Backberg M., Ovesjo M.L., Fisone G., Edwards R.H., Fujiyama F., and Meister B. Plasma membrane and vesicular glutamate transporter mRNAs/proteins in hypothalamic neurons that regulate body weight. Eur. J. Neurosci. 18 (2003) 1265-1278
9. Cooper T.G., Wagenfeld A., Cornwall G.A., Hsia N., Chu S.T., Orgebin-Crist M.C., Drevet J., Vernet P., Avram C., Nieschlag E., and Yeung C.H. Gene and protein expression in the epididymis of infertile c-ros receptor tyrosine kinase-deficient mice. Biol. Reprod. 69 (2003) 1750-1762
10. Crino P.B., Jin H., Shumate M.D., Robinson M.B., Coulter D.A., and Brooks-Kayal A.R. Increased expression of the neuronal glutamate transporter (EAAT3/EAAC1) in hippocampal and neocortical epilepsy. Epilepsia 43 (2002) 211-218
11. Davis K.E., Straff D.J., Weinstein E.A., Bannerman P.G., Correale D.M., Rothstein J.D., and Robinson M.B. Multiple signaling pathways regulate cell surface expression and activity of the excitatory amino acid carrier 1 subtype of Glu transporter in C6 glioma. J. Neurosci. 18 (1998) 2475-2485
12. Deng X., Shibata H., Takeuchi N., Rachi S., Sakai M., Ninomiya H., Iwata N., Ozaki N., and Fukumaki Y. Association study of polymorphisms in the glutamate transporter genes SLC1A1, SLC1A3, and SLC1A6 with schizophrenia. Am. J. Med. Genet. B: Neuropsychiatr. Genet. 144 (2007) 271-278
13. Do S.H., Fang H.Y., Ham B.M., and Zuo Z. The effects of lidocaine on the activity of glutamate transporter EAAT3: the role of protein kinase C and phosphatidylinositol 3-kinase. Anesth. Analg. 95 (2002) 1263-1268 (table)
14. Do S.H., Ham B.M., and Zuo Z. Effects of propofol on the activity of rat glutamate transporter type 3 expressed in Xenopus oocytes: the role of protein kinase C. Neurosci. Lett. 343 (2003) 113-116
15. +-dependent glutamate transport activity in synaptosomes, C6 glioma, and Xenopus oocytes expressing excitatory amino acid carrier 1 (EAAC1). Mol. Pharmacol. 49 (1996) 465-473
16. +-dependent l-glutamate transport activity in C6 glioma cells by phorbol ester. J. Neurochem. 67 (1996) 508-516
17. Furuta A., Martin L.J., Lin C.L., Dykes-Hoberg M., and Rothstein J.D. Cellular and synaptic localization of the neuronal glutamate transporters excitatory amino acid transporter 3 and 4. Neuroscience 81 (1997) 1031-1042
18. Furuta A., Takashima S., Yokoo H., Rothstein J.D., Wada K., and Iwaki T. Expression of glutamate transporter subtypes during normal human corticogenesis and type II lissencephaly. Brain Res. Dev. Brain Res. 155 (2005) 155-164
19. Gloy J., Reitinger S., Fischer K.G., Schreiber R., Boucherot A., Kunzelmann K., Mundel P., and Pavenstadt H. Amino acid transport in podocytes. Am. J. Physiol. Renal Physiol. 278 (2000) F999-F1005
20. Hsu L., Rockenstein E., Mallory M., Hashimoto M., and Masliah E. Altered expression of glutamate transporters under hypoxic conditions in vitro. J. Neurosci. Res. 64 (2001) 193-202
21. Huang Y., Feng X., Sando J.J., and Zuo Z. Critical role of serine 465 in isoflurane-induced increase of cell-surface redistribution and activity of glutamate transporter type 3. J. Biol. Chem. 281 (2006) 38133-38138
22. Huang Y., and Zuo Z. Isoflurane induces a protein kinase C alpha-dependent increase in cell-surface protein level and activity of glutamate transporter type 3. Mol. Pharmacol. 67 (2005) 1522-1533
23. Huang Y.H., Dykes-Hoberg M., Tanaka K., Rothstein J.D., and Bergles D.E. Climbing fiber activation of EAAT4 transporters and kainate receptors in cerebellar Purkinje cells. J. Neurosci. 24 (2004) 103-111
24. Huerta I., McCullumsmith R.E., Haroutunian V., Gimenez-Amaya J.M., and Meador-Woodruff J.H. Expression of excitatory amino acid transporter interacting protein transcripts in the thalamus in schizophrenia. Synapse 59 (2006) 394-402
25. Ikonomov O.C., Sbrissa D., Foti M., Carpentier J.L., and Shisheva A. PIKfyve controls fluid phase endocytosis but not recycling/degradation of endocytosed receptors or sorting of procathepsin D by regulating multivesicular body morphogenesis. Mol. Biol. Cell 14 (2003) 4581-4591
26. Ikonomov O.C., Sbrissa D., Mlak K., Kanzaki M., Pessin J., and Shisheva A. Functional dissection of lipid and protein kinase signals of PIKfyve reveals the role of PtdIns 3.5-P2 production for endomembrane integrity. J. Biol. Chem. 277 (2002) 9206-9211
27. Ikonomov O.C., Sbrissa D., and Shisheva A. Mammalian cell morphology and endocytic membrane homeostasis require enzymatically active phosphoinositide 5-kinase PIKfyve. J. Biol. Chem. 276 (2001) 26141-26147
28. Ikonomov O.C., Sbrissa D., and Shisheva A. Localized PtdIns 3, 5-P2 synthesis to regulate early endosome dynamics and fusion. Am. J. Physiol. Cell Physiol. 291 (2006) C393-C404
29. Kim J.H., Do S.H., Kim Y.L., and Zuo Z. Effects of chronic exposure to ethanol on glutamate transporter EAAT3 expressed in Xenopus oocytes: evidence for protein kinase C involvement. Alcohol Clin. Exp. Res. 29 (2005) 2046-2052
30. King N., Lin H., McGivan J.D., and Suleiman M.S. Aspartate transporter expression and activity in hypertrophic rat heart and ischaemia-reperfusion injury. J. Physiol. 556 (2004) 849-858
31. Kobayashi T., Deak M., Morrice N., and Cohen P. Characterization of the structure and regulation of two novel isoforms of serum- and glucocorticoid-induced protein kinase. Biochem. J. 344 Pt 1 (1999) 189-197
32. Lang F., Bohmer C., Palmada M., Seebohm G., Strutz-Seebohm N., and Vallon V. (Patho)physiological significance of the serum- and glucocorticoid-inducible kinase isoforms. Physiol. Rev. 86 (2006) 1151-1178
33. Lang U.E., Puls I., Muller D.J., Strutz-Seebohm N., and Gallinat J. Molecular mechanisms of schizophrenia. Cell Physiol. Biochem. 20 (2007) 687-702
34. Maragakis N.J., Dietrich J., Wong V., Xue H., Mayer-Proschel M., Rao M.S., and Rothstein J.D. Glutamate transporter expression and function in human glial progenitors. Glia 45 (2004) 133-143
35. Mathern G.W., Mendoza D., Lozada A., Pretorius J.K., Dehnes Y., Danbolt N.C., Nelson N., Leite J.P., Chimelli L., Born D.E., Sakamoto A.C., Assirati J.A., Fried I., Peacock W.J., Ojemann G.A., and Adelson P.D. Hippocampal GABA and glutamate transporter immunoreactivity in patients with temporal lobe epilepsy. Neurology 52 (1999) 453-472
36. Matthews J.C., Beveridge M.J., Dialynas E., Bartke A., Kilberg M.S., and Novak D.A. Placental anionic and cationic amino acid transporter expression in growth hormone overexpressing and null IGF-II or null IGF-I receptor mice. Placenta 20 (1999) 639-650
37. McCullumsmith R.E., and Meador-Woodruff J.H. Striatal excitatory amino acid transporter transcript expression in schizophrenia, bipolar disorder, and major depressive disorder. Neuropsychopharmacology 26 (2002) 368-375
38. + dependent glutamate transporters (EAAT1, EAAT2, and EAAT3) in primary astrocyte cultures: effect of oxidative stress. Brain Res. 922 (2001) 21-29
39. Nieoullon A., Canolle B., Masmejean F., Guillet B., Pisano P., and Lortet S. The neuronal excitatory amino acid transporter EAAC1/EAAT3: does it represent a major actor at the brain excitatory synapse?. J. Neurochem. 98 (2006) 1007-1018
40. Noorlander C.W., de Graan P.N., Nikkels P.G., Schrama L.H., and Visser G.H. Distribution of glutamate transporters in the human placenta. Placenta 25 (2004) 489-495
41. Nudmamud-Thanoi S., Piyabhan P., Harte M.K., Cahir M., and Reynolds G.P. Deficits of neuronal glutamatergic markers in the caudate nucleus in schizophrenia. J. Neural Transm. Suppl. (2007) 281-285
42. O'Kane R.L., Martinez-Lopez I., DeJoseph M.R., Vina J.R., and Hawkins R.A. Na(+)-dependent glutamate transporters (EAAT1, EAAT2, and EAAT3) of the blood-brain barrier. A mechanism for glutamate removal. J. Biol. Chem. 274 (1999) 31891-31895
43. Paul J., Jeyaraj S., Huber S.M., Seebohm G., Bohmer C., Lang F., Kremsner P.G., and Kun J.F. Alterations in the cytoplasmic domain of CLCN2 result in altered gating kinetics. Cell Physiol. Biochem. 20 (2007) 441-454
44. Pradillo J.M., Hurtado O., Romera C., Cardenas A., Fernandez-Tome P., Alonso-Escolano D., Lorenzo P., Moro M.A., and Lizasoain I. TNFR1 mediates increased neuronal membrane EAAT3 expression after in vivo cerebral ischemic preconditioning. Neuroscience 138 (2006) 1171-1178
45. Proper E.A., Hoogland G., Kappen S.M., Jansen G.H., Rensen M.G., Schrama L.H., van Veelen C.W., van Rijen P.C., van Nieuwenhuizen O., Gispen W.H., and de Graan P.N. Distribution of glutamate transporters in the hippocampus of patients with pharmaco-resistant temporal lobe epilepsy. Brain 125 (2002) 32-43
46. Rainesalo S., Keranen T., Saransaari P., and Honkaniemi J. GABA and glutamate transporters are expressed in human platelets. Brain Res. Mol. Brain Res. 141 (2005) 161-165
47. Rakhade S.N., and Loeb J.A. Focal reduction of neuronal glutamate transporters in human neocortical epilepsy. Epilepsia 49 (2008) 226-236
48. Rexhepaj R., Grahammer F., Volkl H., Remy C., Wagner C.A., Sandulache D., Artunc F., Henke G., Nammi S., Capasso G., Alessi D.R., and Lang F. Reduced intestinal and renal amino acid transport in PDK1 hypomorphic mice. FASEB J. 20 (2006) 2214-2222
49. Romera C., Hurtado O., Botella S.H., Lizasoain I., Cardenas A., Fernandez-Tome P., Leza J.C., Lorenzo P., and Moro M.A. In vitro ischemic tolerance involves upregulation of glutamate transport partly mediated by the TACE/ADAM17-tumor necrosis factor-alpha pathway. J. Neurosci. 24 (2004) 1350-1357
50. Rusten T.E., Rodahl L.M., Pattni K., Englund C., Samakovlis C., Dove S., Brech A., and Stenmark H. Fab1 phosphatidylinositol 3-phosphate 5-kinase controls trafficking but not silencing of endocytosed receptors. Mol. Biol. Cell 17 (2006) 3989-4001
51. Rutherford A.C., Traer C., Wassmer T., Pattni K., Bujny M.V., Carlton J.G., Stenmark H., and Cullen P.J. The mammalian phosphatidylinositol 3-phosphate 5-kinase (PIKfyve) regulates endosome-to-TGN retrograde transport. J. Cell. Sci. 119 (2006) 3944-3957
52. Sato J.D., Chapline M.C., Thibodeau R., Frizzell R.A., and Stanton B.A. Regulation of human cystic fibrosis transmembrane conductance regulator (CFTR) by serum- and glucocorticoid-inducible kinase (SGK1). Cell Physiol. Biochem. 20 (2007) 91-98
53. Sbrissa D., Ikonomov O.C., Deeb R., and Shisheva A. Phosphatidylinositol 5-phosphate biosynthesis is linked to PIKfyve and is involved in osmotic response pathway in mammalian cells. J. Biol. Chem. 277 (2002) 47276-47284
54. Sbrissa D., Ikonomov O.C., and Shisheva A. PIKfyve, a mammalian ortholog of yeast Fab1p lipid kinase, synthesizes 5-phosphoinositides. Effect of insulin. J. Biol. Chem. 274 (1999) 21589-21597
55. Sbrissa D., Ikonomov O.C., Strakova J., and Shisheva A. Role for a novel signaling intermediate, phosphatidylinositol 5-phosphate, in insulin-regulated F-actin stress fiber breakdown and GLUT4 translocation. Endocrinology 145 (2004) 4853-4865
56. Schmitt A., Zink M., Petroianu G., May B., Braus D.F., and Henn F.A. Decreased gene expression of glial and neuronal glutamate transporters after chronic antipsychotic treatment in rat brain. Neurosci. Lett. 347 (2003) 81-84
57. Schniepp R., Kohler K., Ladewig T., Guenther E., Henke G., Palmada M., Boehmer C., Rothstein J.D., Broer S., and Lang F. Retinal colocalization and in vitro interaction of the glutamate transporter EAAT3 and the serum- and glucocorticoid-inducible kinase SGK1 [correction]. Invest. Ophthalmol. Vis. Sci. 45 (2004) 1442-1449
58. Seebohm G., Strutz-Seebohm N., Baltaev R., Korniychuk G., Knirsch M., Engel J., and Lang F. Regulation of KCNQ4 potassium channel prepulse dependence and current amplitude by SGK1 in Xenopus oocytes. Cell Physiol. Biochem. 16 (2005) 255-262
59. Seebohm G., Strutz-Seebohm N., Birkin R., Dell G., Bucci C., Spinosa M.R., Baltaev R., Mack A.F., Korniychuk G., Choudhury A., Marks D., Pagano R.E., Attali B., Pfeufer A., Kass R.S., Sanguinetti M.C., Tavare J.M., and Lang F. Regulation of endocytic recycling of KCNQ1/KCNE1 potassium channels. Circ. Res. 100 (2007) 686-692
60. Shashidharan P., Huntley G.W., Murray J.M., Buku A., Moran T., Walsh M.J., Morrison J.H., and Plaitakis A. Immunohistochemical localization of the neuron-specific glutamate transporter EAAC1 (EAAT3) in rat brain and spinal cord revealed by a novel monoclonal antibody. Brain Res. 773 (1997) 139-148
61. Shisheva A. PIKfyve: partners, significance, debates and paradoxes. Cell Biol. Int. 32 (2008) 591-604
62. Shojaiefard M., Strutz-Seebohm N., Tavare J.M., Seebohm G., and Lang F. Regulation of the Na(+), glucose cotransporter by PIKfyve and the serum and glucocorticoid inducible kinase SGK1. Biochem. Biophys. Res. Commun. 359 (2007) 843-847
63. Simantov R., Crispino M., Hoe W., Broutman G., Tocco G., Rothstein J.D., and Baudry M. Changes in expression of neuronal and glial glutamate transporters in rat hippocampus following kainate-induced seizure activity. Brain Res. Mol. Brain Res. 65 (1999) 112-123
64. Smith R.E., Haroutunian V., Davis K.L., and Meador-Woodruff J.H. Expression of excitatory amino acid transporter transcripts in the thalamus of subjects with schizophrenia. Am. J. Psychiatry 158 (2001) 1393-1399
65. Strutz-Seebohm N., Shojaiefard M., Christie D., Tavare J., Seebohm G., and Lang F. PIKfyve in the SGK1 mediated regulation of the creatine transporter SLC6A8. Cell Physiol. Biochem. 20 (2007) 729-734
66. van Landeghem F.K., Weiss T., and von Deimling A. Expression of PACAP and glutamate transporter proteins in satellite oligodendrocytes of the human CNS. Regul. Pept. 142 (2007) 52-59
67. Wagner C.A., Friedrich B., Setiawan I., Lang F., and Broer S. The use of Xenopus laevis oocytes for the functional characterization of heterologously expressed membrane proteins. Cell Physiol. Biochem. 10 (2000) 1-12
68. Waldegger S., Barth P., Raber G., and Lang F. Cloning and characterization of a putative human serine/threonine protein kinase transcriptionally modified during anisotonic and isotonic alterations of cell volume. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 4440-4445
69. Watson R.T., and Pessin J.E. Bridging the GAP between insulin signaling and GLUT4 translocation. Trends Biochem. Sci. 31 (2006) 215-222
70. Welsh G.I., Hers I., Berwick D.C., Dell G., Wherlock M., Birkin R., Leney S., and Tavare J.M. Role of protein kinase B in insulin-regulated glucose uptake. Biochem. Soc. Trans. 33 (2005) 346-349
71. Yun J.Y., Kim J.H., Kim H.K., Lim Y.J., Do S.H., and Zuo Z. Effects of intravenous anesthetics on the activity of glutamate transporter EAAT3 expressed in Xenopus oocytes: evidence for protein kinase C involvement. Eur. J. Pharmacol. 531 (2006) 133-139
72. Yun J.Y., Park K.S., Kim J.H., Do S.H., and Zuo Z. Propofol reverses oxidative stress-attenuated glutamate transporter EAAT3 activity: evidence of protein kinase C involvement. Eur. J. Pharmacol. 565 (2007) 83-88
73. Zoia C., Cogliati T., Tagliabue E., Cavaletti G., Sala G., Galimberti G., Rivolta I., Rossi V., Frattola L., and Ferrarese C. Glutamate transporters in platelets: EAAT1 decrease in aging and in Alzheimer's disease. Neurobiol. Aging 25 (2004) 149-157