EAAT4 phosphorylation at the SGK1 consensus site is required for transport modulation by the kinase

Journal of Neurochemistry

Volumn 102, Issue 3, 2007, Pages 858-866

  Rajamanickam, Jeyaganesh ^a   Palmada, Monica ^a   Lang, Florian ^a   Boehmer, Christoph ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Excitatory amino acid transporter 4; Glutamate transport; Neurotoxicity; Phosphorylation; Serum and glucocorticoid inducible kinase 1

Indexed keywords

EXCITATORY AMINO ACID TRANSPORTER 4; GLUTAMIC ACID; RNA; SERUM AND GLUCOCORTICOID REGULATED KINASE 1; THREONINE; TRITIUM; UBIQUITIN PROTEIN LIGASE NEDD4;

AMINO ACID SEQUENCE; AMINO ACID TRANSPORT; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL SURFACE; CONTROLLED STUDY; NEUROCHEMISTRY; NEUROMODULATION; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PURKINJE CELL; RNA INTERFERENCE; TRANSPORT KINETICS; XENOPUS;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; BIOLOGICAL TRANSPORT, ACTIVE; EXCITATORY AMINO ACID TRANSPORTER 4; FEEDBACK, BIOCHEMICAL; GLUTAMIC ACID; IMMEDIATE-EARLY PROTEINS; MUTATION; OOCYTES; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RNA INTERFERENCE; TRANSFECTION; UBIQUITIN-PROTEIN LIGASES; XENOPUS;

EID: 34447324628     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2007.04585.x     Document Type: Article

References (55)

1. Anantharam A., Lewis A., Panaghie G., Gordon E., McCrossan Z. A., Lerner D. J. Abbott G. W. (2003) RNA interference reveals that endogenous Xenopus MinK-related peptides govern mammalian K+channel function in oocyte expression studies. J. Biol. Chem. 278, 11739 11745.
2. Arriza J. L., Fairman W. A., Wadiche J. I., Murdoch G. H., Kavanaugh M. P. Amara S. G. (1994) Functional comparisons of three glutamate transporter subtypes cloned from human motor cortex. J. Neurosci. 14, 5559 5569.
3. Boehmer C., Henke G., Schniepp R., Palmada M., Rothstein J. D., Broer S. Lang F. (2003) Regulation of the glutamate transporter EAAT1 by the ubiquitin ligase Nedd4-2 and the serum and glucocorticoid-inducible kinase isoforms SGK1/3 and protein kinase B. J. Neurochem. 86, 1181 1188.
4. Boehmer C., Rajamanickam J., Schniepp R., Kohler K., Wulff P., Kuhl D., Palmada M. Lang F. (2005) Regulation of the excitatory amino acid transporter EAAT5 by the serum and glucocorticoid dependent kinases SGK1 and SGK3. Biochem. Biophys. Res. Commun. 329, 738 742.
5. Boehmer C., Palmada M., Rajamanickam J., Schniepp R., Amara S. G. Lang F. (2006) Post-translational regulation of EAAT2 function by co-expressed ubiquitin ligase Nedd4-2 is impacted by SGK kinases. J. Neurochem. 97, 911 921.
6. Bohmer C., Philippin M., Rajamanickam J., Mack A., Broer S., Palmada M. Lang F. (2004) Stimulation of the EAAT4 glutamate transporter by SGK protein kinase isoforms and PKB. Biochem. Biophys. Res. Commun. 324, 1242 1248.
7. Casado M., Bendahan A., Zafra F., Danbolt N. C., Aragon C., Gimenez C. Kanner B. I. (1993) Phosphorylation and modulation of brain glutamate transporters by protein kinase C. J. Biol. Chem. 268, 27313 27317.
8. Chen W., Mahadomrongkul V., Berger U. V., Bassan M., DeSilva T., Tanaka K., Irwin N., Aoki C. Rosenberg P. A. (2004) The glutamate transporter GLT1a is expressed in excitatory axon terminals of mature hippocampal neurons. J. Neurosci. 24, 1136 1148.
9. Conradt M. Stoffel W. (1997) Inhibition of the high-affinity brain glutamate transporter GLAST-1 via direct phosphorylation. J. Neurochem. 68, 1244 1251.
10. Danbolt N. C. (2001) Glutamate uptake. Prog. Neurobiol. 65, 1 105.
11. Davis K. E., Straff D. J., Weinstein E. A., Bannerman P. G., Correale D. M., Rothstein J. D. Robinson M. B. (1998) 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, 2475 2485.
12. Debonneville C., Flores S. Y., Kamynina E. et al. (2001) Phosphorylation of Nedd4-2 by Sgk1 regulates epithelial Na(+) channel cell surface expression. EMBO J. 20, 7052 7059.
13. Dieter M., Palmada M., Rajamanickam J., Aydin A., Busjahn A., Boehmer C., Luft F. C. Lang F. (2004) Regulation of glucose transporter SGLT1 by ubiquitin ligase Nedd4-2 and kinases SGK1, SGK3, and PKB. Obes. Res. 12, 862 870.
14. Dowd L. A. Robinson M. B. (1996) Rapid stimulation of EAAC1-mediated Na+-dependent l-glutamate transport activity in C6 glioma cells by phorbol ester. J. Neurochem. 67, 508 516.
15. Embark H. M., Bohmer C., Palmada M. et al. (2004) Regulation of CLC-Ka/barttin by the ubiquitin ligase Nedd4-2 and the serum- and glucocorticoid-dependent kinases. Kidney Int. 66, 1918 1925.
16. Eskandari S., Kreman M., Kavanaugh M. P., Wright E. M. Zampighi G. A. (2000) Pentameric assembly of a neuronal glutamate transporter. Proc. Natl Acad. Sci. USA 97, 8641 8646.
17. Fairman W. A., Vandenberg R. J., Arriza J. L., Kavanaugh M. P. Amara S. G. (1995) An excitatory amino-acid transporter with properties of a ligand-gated chloride channel. Nature 375, 599 603.
18. Fairman W. A., Sonders M. S., Murdoch G. H. Amara S. G. (1998) Arachidonic acid elicits a substrate-gated proton current associated with the glutamate transporter EAAT4. Nat. Neurosci. 1, 105 113.
19. Furuta A., Rothstein J. D. Martin L. J. (1997) Glutamate transporter protein subtypes are expressed differentially during rat CNS development. J. Neurosci. 17, 8363 8375.
20. Gamboa C. Ortega A. (2002) Insulin-like growth factor-1 increases activity and surface levels of the GLAST subtype of glutamate transporter. Neurochem. Int. 40, 397 403.
21. Gegelashvili G. Schousboe A. (1997) High affinity glutamate transporters: regulation of expression and activity. Mol. Pharmacol. 52, 6 15.
22. Gonzalez M. I. Ortega A. (1997) Regulation of the Na + -dependent high affinity glutamate/aspartate transporter in cultured Bergmann glia by phorbol esters. J. Neurosci. Res. 50, 585 590.
23. Howland D. S., Liu J., She Y. et al. (2002) Focal loss of the glutamate transporter EAAT2 in a transgenic rat model of SOD1 mutant-mediated amyotrophic lateral sclerosis (ALS). Proc. Natl Acad. Sci. USA 99, 1604 1609.
24. Huang Y. H., Dykes-Hoberg M., Tanaka K., Rothstein J. D. Bergles D. E. (2004) Climbing fiber activation of EAAT4 transporters and kainate receptors in cerebellar Purkinje cells. J. Neurosci. 24, 103 111.
25. Jackson M., Song W., Liu M. Y., Jin L., Dykes-Hoberg M., Lin C. I., Bowers W. J., Federoff H. J., Sternweis P. C. Rothstein J. D. (2001) Modulation of the neuronal glutamate transporter EAAT4 by two interacting proteins. Nature 410, 89 93.
26. Kanai Y. Hediger M. A. (1992) Primary structure and functional characterization of a high-affinity glutamate transporter. Nature 360, 467 471.
27. Kanai Y., Smith C. P. Hediger M. A. (1993) A new family of neurotransmitter transporters: the high-affinity glutamate transporters. FASEB J. 7, 1450 1459.
28. Lin C. I., Orlov I., Ruggiero A. M., Dykes-Hoberg M., Lee A., Jackson M. Rothstein J. D. (2001) Modulation of the neuronal glutamate transporter EAAC1 by the interacting protein GTRAP3-18. Nature 410, 84 88.
29. Lortet S., Samuel D., Had-Aissouni L., Masmejean F., Kerkerian-Le Goff L. Pisano P. (1999) Effects of PKA and PKC modulators on high affinity glutamate uptake in primary neuronal cell cultures from rat cerebral cortex. Neuropharmacology 38, 395 402.
30. Lu P. J., Zhou X. Z., Shen M. Lu K. P. (1999) Function of WW domains as phosphoserine- or phosphothreonine-binding modules. Science 283, 1325 1328.
31. Meyer T., Fromm A., Munch C., Schwalenstocker B., Fray A. E., Ince P. G., Stamm S., Gron G., Ludolph A. C. Shaw P. J. (1999) The RNA of the glutamate transporter EAAT2 is variably spliced in amyotrophic lateral sclerosis and normal individuals. J. Neurol. Sci. 170, 45 50.
32. Palmada M., Embark H. M., Yun C., Bohmer C. Lang F. (2003) Molecular requirements for the regulation of the renal outer medullary K(+) channel ROMK1 by the serum- and glucocorticoid-inducible kinase SGK1. Biochem. Biophys. Res. Commun. 311, 629 634.
33. Palmada M., Dieter M., Boehmer C., Waldegger S. Lang F. (2004a) Serum and glucocorticoid inducible kinases functionally regulate ClC-2 channels. Biochem. Biophys. Res. Commun. 321, 1001 1006.
34. Palmada M., Dieter M., Speil A. et al. (2004b) Regulation of intestinal phosphate cotransporter NaPi IIb by ubiquitin ligase Nedd4-2 and by serum- and glucocorticoid-dependent kinase 1. Am. J. Physiol. Gastrointest. Liver Physiol. 287, G143 G150.
35. Palmada M., Poppendieck S., Embark H. M., van de Graaf S. F., Boehmer C., Bindels R. J. Lang F. (2005) Requirement of PDZ domains for the stimulation of the epithelial Ca2+ channel TRPV5 by the NHE regulating factor NHERF2 and the serum and glucocorticoid inducible kinase SGK1. Cell Physiol. Biochem. 15, 175 182.
36. Palmada M., Boehmer C., Akel A., Rajamanickam J., Jeyaraj S., Keller K. Lang F. (2006) SGK1 kinase upregulates GLUT1 activity and plasma membrane expression. Diabetes 55, 421 427.
37. Peghini P., Janzen J. Stoffel W. (1997) Glutamate transporter EAAC-1-deficient mice develop dicarboxylic aminoaciduria and behavioral abnormalities but no neurodegeneration. EMBO J. 16, 3822 3832.
38. Pines G., Danbolt N. C., Bjoras M., Zhang Y., Bendahan A., Eide L., Koepsell H., Storm-Mathisen J., Seeberg E. Kanner B. I. (1992) Cloning and expression of a rat brain l-glutamate transporter. Nature 360, 464 467.
39. Pisano P., Samuel D., Nieoullon A. Kerkerian-Le Goff L. (1996) Activation of the adenylate cyclase-dependent protein kinase pathway increases high affinity glutamate uptake into rat striatal synaptosomes. Neuropharmacology 35, 541 547.
40. Pow D. V. Barnett N. L. (2000) Developmental expression of excitatory amino acid transporter 5: a photoreceptor and bipolar cell glutamate transporter in rat retina. Neurosci. Lett. 280, 21 24.
41. Robinson M. B. Dowd L. A. (1997) Heterogeneity and functional properties of subtypes of sodium-dependent glutamate transporters in the mammalian central nervous system. Adv. Pharmacol. 37, 69 115.
42. Rothstein J. D., Van Kammen M., Levey A. I., Martin L. J. Kuncl R. W. (1995) Selective loss of glial glutamate transporter GLT-1 in amyotrophic lateral sclerosis. Ann. Neurol. 38, 73 84.
43. Schniepp R., Kohler K., Ladewig T., Guenther E., Henke G., Palmada M., Boehmer C., Rothstein J. D., Broer S. Lang F. (2004) Retinal colocalization and in vitro interaction of the glutamate receptor EAAT3 and the serum- and glucocorticoid-inducible kinase SGK1. Invest. Ophthalmol. Vis. Sci. 45, 1442 1449.
44. Sims K. D., Straff D. J. Robinson M. B. (2000) Platelet-derived growth factor rapidly increases activity and cell surface expression of the EAAC1 subtype of glutamate transporter through activation of phosphatidylinositol 3-kinase. J. Biol. Chem. 275, 5228 5237.
45. Storck T., Schulte S., Hofmann K. Stoffel W. (1992) Structure, expression, and functional analysis of a Na(+)-dependent glutamate/aspartate transporter from rat brain. Proc. Natl Acad. Sci. USA 89, 10955 10959.
46. Takayasu Y., Iino M., Kakegawa W. et al. (2005) Differential roles of glial and neuronal glutamate transporters in Purkinje cell synapses. J. Neurosci. 25, 8788 8793.
47. Tanaka K., Watase K., Manabe T. et al. (1997) Epilepsy and exacerbation of brain injury in mice lacking the glutamate transporter GLT-1. Science 276, 1699 1702.
48. Trotti D., Danbolt N. C. Volterra A. (1998) Glutamate transporters are oxidant-vulnerable: a molecular link between oxidative and excitotoxic neurodegeneration? Trends Pharmacol. Sci. 19, 328 334.
49. Vandenberg R. J., Arriza J. L., Amara S. G. Kavanaugh M. P. (1995) Constitutive ion fluxes and substrate binding domains of human glutamate transporters. J. Biol. Chem. 270, 17668 17671.
50. Wagner C. A., Friedrich B., Setiawan I., Lang F. Broer S. (2000) The use of Xenopus laevis oocytes for the functional characterization of heterologously expressed membrane proteins. Cell Physiol. Biochem. 10, 1 12.
51. Watase K., Hashimoto K., Kano M. et al. (1998) Motor discoordination and increased susceptibility to cerebellar injury in GLAST mutant mice. Eur. J. Neurosci. 10, 976 988.
52. Yamada K., Watanabe M., Shibata T., Nagashima M., Tanaka K. Inoue Y. (1998) Glutamate transporter GLT-1 is transiently localized on growing axons of the mouse spinal cord before establishing astrocytic expression. J. Neurosci. 18, 5706 5713.
53. Yamashita A., Makita K., Kuroiwa T. Tanaka K. (2006) Glutamate transporters GLAST and EAAT4 regulate postischemic Purkinje cell death: an in vivo study using a cardiac arrest model in mice lacking GLAST or EAAT4. Neurosci. Res. 55, 264 270.
54. Zelenaia O., Schlag B. D., Gochenauer G. E., Ganel R., Song W., Beesley J. S., Grinspan J. B., Rothstein J. D. Robinson M. B. (2000) Epidermal growth factor receptor agonists increase expression of glutamate transporter GLT-1 in astrocytes through pathways dependent on phosphatidylinositol 3-kinase and transcription factor NF-kappaB. Mol. Pharmacol. 57, 667 678.
55. Zerangue N., Arriza J. L., Amara S. G. Kavanaugh M. P. (1995) Differential modulation of human glutamate transporter subtypes by arachidonic acid. J. Biol. Chem. 270, 6433 6435.