Post-translational regulation of EAAT2 function by co-expressed ubiquitin ligase Nedd4-2 is impacted by SGK kinases

Journal of Neurochemistry

Volumn 97, Issue 4, 2006, Pages 911-921

  Boehmer, Christoph ^a   Palmada, Monica ^a   Rajamanickam, Jeyaganesh ^a   Schniepp, Roman ^a   Amara, Susan ^b   Lang, Florian ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Amyotrophic lateral sclerosis; Glial cells; Glutamate transport; Neuroexcitotoxicity; Xenopus laevis

Indexed keywords

EXCITATORY AMINO ACID TRANSPORTER; GLUTAMATE TRANSPORTER; GLUTAMIC ACID; ION CHANNEL; ISOENZYME; PHOSPHOTRANSFERASE; PROTEIN KINASE B; SERUM AND GLUCOCORTICOID REGULATED KINASE; SERUM AND GLUCOCORTICOID REGULATED KINASE 1; SERUM AND GLUCOCORTICOID REGULATED KINASE 2; SERUM AND GLUCOCORTICOID REGULATED KINASE 3; UBIQUITIN PROTEIN LIGASE NEDD4; UNCLASSIFIED DRUG;

AMINO ACID TRANSPORT; AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; ENZYME SUBSTRATE COMPLEX; EXCITABILITY; EXCITOTOXICITY; FEMALE; GLIA CELL; GLUTAMATE INDUCED INWARD CURRENT; GLUTAMATE TRANSPORT; MEMBRANE CURRENT; NERVE CELL MEMBRANE; NEUROEXCITABILITY; NEUROMODULATION; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; TRANSPORT KINETICS; XENOPUS LAEVIS;

ANIMALS; CATALYTIC DOMAIN; DOWN-REGULATION; EXCITATORY AMINO ACID TRANSPORTER 2; FEMALE; GLUTAMIC ACID; HUMANS; IMMEDIATE-EARLY PROTEINS; MEMBRANE POTENTIALS; OOCYTES; PHOSPHORYLATION; PROTEIN ISOFORMS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS C-AKT; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES; UP-REGULATION; XENOPUS LAEVIS;

ANIMALIA; MAMMALIA; XENOPUS LAEVIS;

EID: 33646113826     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2006.03629.x     Document Type: Article

References (74)

1. Abriel H. Kamynina E. Horisberger J. D. Staub O. 2000 Regulation of the cardiac voltage-gated Na+ channel (H1) by the ubiquitin-protein ligase Nedd4. FEBS Lett. 466 377 380.
2. Alessi D. R. Andjelkovic M. Caudwell B. Cron P. Morrice N. Cohen P. Hemmings B. A. 1996 Mechanism of activation of protein kinase B by insulin and IGF-1. EMBO J. 15 6541 6551.
3. Altomare D. A. Lyons G. E. Mitsuuchi Y. Cheng J. Q. Testa J. R. 1998 Akt2 mRNA is highly expressed in embryonic brown fat and the AKT2 kinase is activated by insulin. Oncogene 16 2407 2411.
4. Bednarski E. Lauterborn J. C. Gall C. M. Lynch G. 1998 Lysosomal dysfunction reduces brain-derived neurotrophic factor expression. Exp. Neurol. 150 128 135.
5. Bergles D. E. Jahr C. E. 1997 Synaptic activation of glutamate transporters in hippocampal astrocytes. Neuron 19 1297 1308.
6. Boehmer C. Henke G. Schniepp R. Palmada M. Rothstein J. D. Broer S. Lang F. 2003a 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.
7. Boehmer C. Wilhelm V. Palmada M. Wallisch S. Henke G. Brinkmeier H. Cohen P. Pieske B. Lang F. 2003b Serum and glucocorticoid inducible kinases in the regulation of the cardiac sodium channel SCN5A. Cardiovasc. Res. 57 1079 1084.
8. Boehmer C. Embark H. M. Bauer A. et al. 2004 Stimulation of renal Na+ dicarboxylate cotransporter 1 by Na+/H+ exchanger regulating factor 2, serum and glucocorticoid inducible kinase isoforms, and protein kinase B. Biochem. Biophys. Res. Commun. 313 998 1003.
9. Böhmer C. Wagner C. A. Beck S. Moschen I. Melzig J. Werner A. Lin J. T. Lang F. Wehner F. 2000 The shrinkage-activated Na(+) conductance of rat hepatocytes and its possible correlation to rENaC. Cell Physiol. Biochem. 10 187 194.
10. 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 27 313 27 317.
11. Chen S. Y. Bhargava A. Mastroberardino L. Meijer O. C. Wang J. Buse P. Firestone G. L. Verrey F. Pearce D. 1999 Epithelial sodium channel regulated by aldosterone-induced protein sgk. Proc. Natl Acad. Sci. USA 96 2514 2519.
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. Dehnes Y. Chaudhry F. A. Ullensvang K. Lehre K. P. Storm-Mathisen J. Danbolt N. C. 1998 The glutamate transporter EAAT4 in rat cerebellar Purkinje cells: a glutamate-gated chloride channel concentrated near the synapse in parts of the dendritic membrane facing astroglia. J. Neurosci. 18 3606 3619.
14. Diamond J. S. Jahr C. E. 1997 Transporters buffer synaptically released glutamate on a submillisecond time scale. J. Neurosci. 17 4672 4687.
15. Douen A. G. Akiyama K. Hogan M. J. Wang F. Dong L. Chow A. K. Hakim A. 2000 Preconditioning with cortical spreading depression decreases intraischemic cerebral glutamate levels and down-regulates excitatory amino acid transporters EAAT1 and EAAT2 from rat cerebal cortex plasma membranes. J. Neurochem. 75 812 818.
16. Dutuit M. Touret M. Szymocha R. Nehlig A. Belin M. F. Didier-Bazes M. 2002 Decreased expression of glutamate transporters in genetic absence epilepsy rats before seizure occurrence. J. Neurochem. 80 1029 1038.
17. Embark H. M. Bohmer C. Vallon V. Luft F. Lang F. 2003 Regulation of KCNE1-dependent K(+) current by the serum and glucocorticoid-inducible kinase (SGK) isoforms. Pflugers Arch. 445 601 606.
18. 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.
19. Firestone G. L. Giampaolo J. R. O'Keeffe B. A. 2003 Stimulus-dependent regulation of serum and glucocorticoid inducible protein kinase (SGK) transcription, subcellular localization and enzymatic activity. Cell Physiol. Biochem. 13 1 12.
20. Friedrich B. Feng Y. Cohen P. Risler T. Vandewalle A. Broer S. Wang J. Pearce D. Lang F. 2003 The serine/threonine kinases SGK2 and SGK3 are potent stimulators of the epithelial Na+ channel alpha,beta,gamma-ENaC. Pflugers Arch. 445 693 696.
21. Gamper N. Fillon S. Feng Y. Friedrich B. Lang P. A. Henke G. Huber S. M. Kobayashi T. Cohen P. Lang F. 2002a K(+) channel activation by all three isoforms of serum- and glucocorticoid-dependent protein kinase SGK. Pflugers Arch. 445 60 66.
22. Gamper N. Fillon S. Huber S. M. Feng Y. Kobayashi T. Cohen P. Lang F. 2002b IGF-1 up-regulates K+ channels via PI3-kinase, PDK1 and SGK1. Pflugers Arch. 443 625 634.
23. Gu S. Langlais P. Liu F. Jiang J. X. 2003 Mouse system-N amino acid transporter, mNAT3, expressed in hepatocytes and regulated by insulin-activated and phosphoinositide 3-kinase-dependent signalling. Biochem. J. 371 721 731.
24. Guo H. Lai L. Butchbach M. E. Stockinger M. P. Shan X. Bishop G. A. Lin C. L. 2003 Increased expression of the glial glutamate transporter EAAT2 modulates excitotoxicity and delays the onset but not the outcome of ALS in mice. Hum. Mol. Genet. 12 2519 2532.
25. Henke G. Setiawan I. Bohmer C. Lang F. 2002 Activation of Na+/K+-ATPase by the serum and glucocorticoid-dependent kinase isoforms. Kidney Blood Press Res. 25 370 374.
26. Honig L. S. Chambliss D. D. Bigio E. H. Carroll S. L. Elliott J. L. 2000 Glutamate transporter EAAT2 splice variants occur not only in ALS, but also in AD and controls. Neurology 55 1082 1088.
27. 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.
28. Kalandadze A. Wu Y. Robinson M. B. 2002 Protein kinase C activation decreases cell surface expression of the GLT-1 subtype of glutamate transporter. Requirement of a carboxyl-terminal domain and partial dependence on serine 486. J. Biol. Chem. 277 45 741 45 750.
29. Kalandadze A. Wu Y. Fournier K. Robinson M. B. 2004 Identification of motifs involved in endoplasmic reticulum retention-forward trafficking of the GLT-1 subtype of glutamate transporter. J. Neurosci. 24 5183 5192.
30. Kobayashi T. Cohen P. 1999 Activation of serum- and glucocorticoid-regulated protein kinase by agonists that activate phosphatidylinositide 3-kinase is mediated by 3-phosphoinositide-dependent protein kinase-1 (PDK1) and PDK2. Biochem. J. 339 319 328.
31. Kugler P. Schmitt A. 1999 Glutamate transporter EAAC1 is expressed in neurons and glial cells in the rat nervous system. Glia 27 129 142.
32. Lang F. Klingel K. Wagner C. A. et al. 2000 Deranged transcriptional regulation of cell-volume-sensitive kinase hSGK in diabetic nephropathy. Proc. Natl Acad. Sci. USA 97 8157 8162.
33. Lang F. Henke G. Embark H. M. Waldegger S. Palmada M. Bohmer C. Vallon V. 2003 Regulation of channels by the serum and glucocorticoid-inducible kinase - implications for transport, excitability and cell proliferation. Cell Physiol. Biochem. 13 41 50.
34. Lawlor M. A. Mora A. Ashby P. R. Williams M. R. Murray-Tait V. Malone L. Prescott A. R. Lucocq J. M. Alessi D. R. 2002 Essential role of PDK1 in regulating cell size and development in mice. EMBO J. 21 3728 3738.
35. Legay V. Deleage C. Beaulieux F. Giraudon P. Aymard M. Lina B. 2003 Impaired glutamate uptake and EAAT2 downregulation in an enterovirus chronically infected human glial cell line. Eur. J. Neurosci. 17 1820 1828.
36. Lehre K. P. Danbolt N. C. 1998 The number of glutamate transporter subtype molecules at glutamatergic synapses: chemical and stereological quantification in young adult rat brain. J. Neurosci. 18 8751 8757.
37. Lehre K. P. Levy L. M. Ottersen O. P. Storm-Mathisen J. Danbolt N. C. 1995 Differential expression of two glial glutamate transporters in the rat brain: quantitative and immunocytochemical observations. J. Neurosci. 15 1835 1853.
38. Lopez-Redondo F. Nakajima K. Honda S. Kohsaka S. 2000 Glutamate transporter GLT-1 is highly expressed in activated microglia following facial nerve axotomy. Brain Res. Mol. Brain Res. 76 429 435.
39. Mennerick S. Shen W. Xu W. Benz A. Tanaka K. Shimamoto K. Isenberg K. E. Krause J. E. Zorumski C. F. 1999 Substrate turnover by transporters curtails synaptic glutamate transients. J. Neurosci. 19 9242 9251.
40. 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.
41. Milton I. D. Banner S. J. Ince P. G. Piggott N. H. Fray A. E. Thatcher N. Horne C. H. Shaw P. J. 1997 Expression of the glial glutamate transporter EAAT2 in the human CNS: an immunohistochemical study. Brain Res. Mol. Brain Res. 52 17 31.
42. Munch C. Ebstein M. Seefried U. Zhu B. Stamm S. Landwehrmeyer G. B. Ludolph A. C. Schwalenstocker B. Meyer T. 2002 Alternative splicing of the 5′-sequences of the mouse EAAT2 glutamate transporter and expression in a transgenic model for amyotrophic lateral sclerosis. J. Neurochem. 82 594 603.
43. Naray-Fejes-Toth A. Canessa C. Cleaveland E. S. Aldrich G. Fejes-Toth G. 1999 SGK is an aldosterone-induced kinase in the renal collecting duct. Effects on epithelial Na+ channels. J. Biol. Chem. 274 16 973 16 978.
44. Palmada M. Dieter M. Speil A. et al. 2004 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.
45. Pearce D. 2003 SGK1 regulation of epithelial sodium transport. Cell Physiol. Biochem. 13 13 20.
46. Proper E. A. Hoogland G. Kappen S. M. et al. 2002 Distribution of glutamate transporters in the hippocampus of patients with pharmaco-resistant temporal lobe epilepsy. Brain 125 32 43.
47. Rodriguez-Kern A. Gegelashvili M. Schousboe A. Zhang J. Sung L. Gegelashvili G. 2003 Beta-amyloid and brain-derived neurotrophic factor, BDNF, up-regulate the expression of glutamate transporter GLT-1/EAAT2 via different signaling pathways utilizing transcription factor NF-kappaB. Neurochem. Int. 43 363 370.
48. Rothstein J. D. 1995 Excitotoxicity and neurodegeneration in amyotrophic lateral sclerosis. Clin. Neurosci. 3 348 359.
49. Rothstein J. D. Martin L. J. Kuncl R. W. 1992 Decreased glutamate transport by the brain and spinal cord in amyotrophic lateral sclerosis. N. Engl. J. Med. 326 1464 1468.
50. Rothstein J. D. Martin L. Levey A. I. Dykes-Hoberg M. Jin L. Wu D. Nash N. Kuncl R. W. 1994 Localization of neuronal and glial glutamate transporters. Neuron 13 713 725.
51. 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.
52. Rothstein J. D. Dykes-Hoberg M. Pardo C. A. et al. 1996 Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron 16 675 686.
53. Sander T. Berlin W. Ostapowicz A. Samochowiec J. Gscheidel N. Hoehe M. R. 2000 Variation of the genes encoding the human glutamate EAAT2, serotonin and dopamine transporters and susceptibility to idiopathic generalized epilepsy. Epilepsy Res. 41 75 81.
54. 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.
55. Setiawan I. Henke G. Feng Y. Bohmer C. Vasilets L. A. Schwarz W. Lang F. 2002 Stimulation of Xenopus oocyte Na(+),K(+) ATPase by the serum and glucocorticoid-dependent kinase sgk1. Pflugers Arch. 444 426 431.
56. Shigaev A. Asher C. Latter H. Garty H. Reuveny E. 2000 Regulation of sgk by aldosterone and its effects on the epithelial Na(+) channel. Am. J. Physiol. Renal Physiol. 278 F613 F619.
57. Shigeri Y. Shimamoto K. Yasuda-Kamatani Y. Seal R. P. Yumoto N. Nakajima T. Amara S. G. 2001 Effects of threo-beta-hydroxyaspartate derivatives on excitatory amino acid transporters (EAAT4 and EAAT5). J. Neurochem. 79 297 302.
58. Snyder P. M. Olson D. R. Thomas B. C. 2002 Serum and glucocorticoid-regulated kinase modulates Nedd4-2-mediated inhibition of the epithelial Na+ channel. J. Biol. Chem. 277 5 8.
59. Sutherland M. L. Martinowich K. Rothstein J. D. 2001 EAAT2 overexpression plays a neuroprotective role in the SOD1 G93A model of amyotrophic lateral sclerosis. Soc. Neurosci. Abs. 27. 607.6
60. 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.
61. Trotti D. Aoki M. Pasinelli P. Berger U. V. Danbolt N. C. Brown R. H. Jr. Hediger M. A. 2001 Amyotrophic lateral sclerosis-linked glutamate transporter mutant has impaired glutamate clearance capacity. J. Biol. Chem. 276 576 582.
62. Vera-Portocarrero L. P. Mills C. D. Ye Z. Fullwood S. D. McAdoo D. J. Hulsebosch C. E. Westlund K. N. 2002 Rapid changes in expression of glutamate transporters after spinal cord injury. Brain Res. 927 104 110.
63. Verrey F. Loffing J. Zecevic M. Heitzmann D. Staub O. 2003 SGK1: aldosterone-induced relay of Na+ transport regulation in distal kidney nephron cells. Cell Physiol. Biochem. 13 21 28.
64. Vorwerk C. K. Naskar R. Schuettauf F. Quinto K. Zurakowski D. Gochenauer G. Robinson M. B. Mackler S. A. Dreyer E. B. 2000 Depression of retinal glutamate transporter function leads to elevated intravitreal glutamate levels and ganglion cell death. Invest. Ophthalmol. Vis. Sci. 41 3615 3621.
65. 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.
66. Waldegger S. Barth P. Raber G. Lang F. 1997 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. USA 94 4440 4445.
67. Wärntges S. Friedrich B. Henke G. et al. 2002 Cerebral localization and regulation of the cell volume-sensitive serum- and glucocorticoid-dependent kinase SGK1. Pflugers Arch. 443 617 624.
68. Webster M. K. Goya L. Firestone G. L. 1993a Immediate-early transcriptional regulation and rapid mRNA turnover of a putative serine/threonine protein kinase. J. Biol. Chem. 268 11 482 11 485.
69. Webster M. K. Goya L. Ge Y. Maiyar A. C. Firestone G. L. 1993b Characterization of sgk, a novel member of the serine/threonine protein kinase gene family which is transcriptionally induced by glucocorticoids and serum. Mol. Cell Biol. 13 2031 2040.
70. Wisman L. A. van Muiswinkel F. L. de Graan P. N. Hol E. M. Bar P. R. 2003 Cells over-expressing EAAT2 protect motoneurons from excitotoxic death in vitro. Neuroreport 14 1967 1970.
71. Wulff P. Vallon V. Huang D. Y. et al. 2002 Impaired renal Na(+) retention in the sgk1-knockout mouse. J. Clin. Invest. 110 1263 1268.
72. Yun C. C. Chen Y. Lang F. 2002a Glucocorticoid activation of Na(+)/H(+) exchanger isoform 3 revisited. The roles of SGK1 and NHERF2. J. Biol. Chem. 277 7676 7683.
73. Yun C. C. Palmada M. Embark H. M. et al. 2002b The serum and glucocorticoid-inducible kinase SGK1 and the Na(+)/H(+) exchange regulating factor NHERF2 synergize to stimulate the renal outer medullary K(+) channel ROMK1. J. Am. Soc. Nephrol. 13 2823 2830.
74. Zerangue N. Schwappach B. Jan Y. N. Jan L. Y. 1999 A new ER trafficking signal regulates the subunit stoichiometry of plasma membrane K(ATP) channels. Neuron 22 537 548.