Neurosteroid allopregnanolone regulates EAAC1-mediated glutamate uptake and triggers actin changes in Schwann cells

Journal of Cellular Physiology

Volumn 227, Issue 4, 2012, Pages 1740-1751

  Perego, Carla ^a   di Cairano, Eliana S ^a   Ballabio, Marinella ^a   Magnaghi, Valerio ^a  

^a UNIVERSITY OF MILAN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

3ALPHA HYDROXY 5ALPHA PREGNAN 20 ONE; 4 AMINOBUTYRIC ACID A RECEPTOR; ACTIN; EXCITATORY AMINO ACID TRANSPORTER 3; GLUTAMIC ACID; PROTEIN KINASE C;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL PROLIFERATION; CELL STRUCTURE; CELL VACUOLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DEPOLYMERIZATION; ENDOCYTOSIS; ENZYME ACTIVATION; EXOCYTOSIS; INTRACELLULAR SIGNALING; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; SCHWANN CELL; UPREGULATION;

ACTINS; AMINO ACID TRANSPORT SYSTEM X-AG; ANIMALS; ASPARTIC ACID; BIOLOGICAL TRANSPORT, ACTIVE; EXCITATORY AMINO ACID TRANSPORTER 3; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; IMMUNOHISTOCHEMISTRY; MODELS, NEUROLOGICAL; PREGNANOLONE; RATS; RNA, MESSENGER; SCHWANN CELLS; UP-REGULATION;

EID: 84855753465     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.22898     Document Type: Article

References (62)

1. Aoyama K, Suh SW, Hamby AM, Liu J, Chan WY, Chen Y, Swanson RA. 2006. Neuronal glutathione deficiency and age-dependent neurodegeneration in the EAAC1 deficient mouse. Nat Neurosci 9:119-126.
2. Arkaravichien T, Sattayasai N, Daduang S, Sattayasai J. 2003. Dose-dependent effects of glutamate in pyridoxine-induced neuropathy. Food Chem Toxicol 41:1375-1380.
3. Arriza JL, Fairman WA, Wadiche JI, Murdoch GH, Kavanaugh MP, Amara SG. 1994. Functional comparisons of three glutamate transporter subtypes cloned from human motor cortex. J Neurosci 14:5559-5569.
4. Axelrod D. 2001. Total internal reflection fluorescence microscopy in cell biology. Traffic 2:764-774.
5. Bacich DJ, Wozniak KM, Lu XC, O'Keefe DS, Callizot N, Heston WD, Slusher BS. 2005. Mice lacking glutamate carboxypeptidase II are protected from peripheral neuropathy and ischemic brain injury. J Neurochem 95:314-323.
6. Bak LK, Schousboe A, Waagepetersen HS. 2006. The glutamate/GABA-glutamine cycle: Aspects of transport, neurotransmitter homeostasis and ammonia transfer. J Neurochem 98:641-653.
7. Basu SK, Goldstein JL, Anderson RG, Brown MS. 1981. Monensin interrupts the recycling of low density lipoprotein receptors in human fibroblasts. Cell 1:493-502.
8. Belelli D, Lambert JJ. 2005. Neurosteroids: Endogenous regulators of the GABA(A) receptor. Nat Rev Neurosci 6:565-575.
9. Brockes JP, Fields KL, Raff MC. 1979. Studies on cultured rat Schwann cells. I Establishment of purified populations from cultures of peripheral nerve. Brain Res 165:105-118.
10. Brone B, Eggermont J. 2005. PDZ proteins retain and regulate membrane transporters in polarized epithelial cell membranes. Am J Physiol Cell Physiol 288:C20-C29.
11. Callachan H, Cottrell GA, Hather NY, Lambert JJ, Nooney JM, Peters JA. 1987. Modulation of the GABAA receptor by progesterone metabolites. Proc R Soc Lond B Biol Sci 231:359-369.
12. Carlton SM. 2001. Peripheral excitatory amino acids. Curr Opin Pharmacol 1:52-56.
13. Carozzi VA, Canta A, Oggioni N, Ceresa C, Marmiroli P, Konvalinka J, Zoia C, Bossi M, Ferrarese C, Tredici G, Cavaletti G. 2008. Expression and distribution of 'high affinity' glutamate transporters GLT1, GLAST, EAAC1 and of GCPII in the rat peripheral nervous system. J Anat 213:539-546.
14. Chavez-Delgado ME, Gomez-Pinedo U, Feria-Velasco A, Huerta-Viera M, Castaneda SC, Toral FA, Parducz A, Anda SL, Mora-Galindo J, Garcia-Estrada J. 2005. Ultrastructural analysis of guided nerve regeneration using progesterone- and pregnenolone-loaded chitosan prostheses. J Biomed Mater Res B Appl Biomater 74:589-600.
15. Choi DW, Maulucci-Gedde M, Kriegstein AR. 1987. Glutamate neurotoxicity in cortical cell culture. J Neurosci 7:357-368.
16. Chomczynski P, Sacchi N. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156-159.
17. D'Amico A, Soragna A, Di Cairano E, Panzeri N, Anzai N, Sacchi FV, Perego C. 2010. The surface density of the glutamate transporter EAAC1 is controlled by interactions with PDZK1 and AP2 adaptor complexes. Traffic 11:1455-1470.
18. Danbolt NC. 2001. Glutamate uptake. Prog Neurobiol 65:1-105.
19. Fancsik A, Linn DM, Tasker JG. 2000. Neurosteroid modulation of GABA IPSCs is phosphorylation dependent. J Neurosci 20:3067-3075.
20. Fink T, Davey DF, Ansselin AD. 1999. Glutaminergic and adrenergic receptors expressed on adult guinea pig Schwann cells in vitro. Can J Physiol Pharmacol 77:204-210.
21. Franklin RB, Zou J, Yu Z, Costello LC. 2006. EAAC1 is expressed in rat and human prostate epithelial cells; functions as a high-affinity L-aspartate transporter; and is regulated by prolactin and testosterone. BMC Biochem 7:10.
22. Funicello M, Conti P, De Amici M, De Micheli C, Mennini T, Gobbi M. 2004. Dissociation of [3H]L-glutamate uptake from L-glutamate-induced [3H]D-aspartate release by 3-hydroxy-4, 5, 6, 6a-tetrahydro-3aH-pyrrolo[3, 4-d]isoxazole-4-carboxylic acid and 3-hydroxy-4, 5, 6, 6a-tetrahydro-3aH-pyrrolo[3, 4-d]isoxazole-6-carboxylic acid, two conformationally constrained aspartate and glutamate analogs. Mol Pharmacol 66:522-529.
23. Garbay B, Heape AM, Sargueil F, Cassagne C. 2000. Myelin synthesis in the peripheral nervous system. Prog Neurobiol 61:267-304.
24. Gatto CL, Walker BJ, Lambert S. 2003. Local ERM activation and dynamic growth cones at Schwann cell tips implicated in efficient formation of nodes of Ranvier. J Cell Biol 162:489-498.
25. Gonzalez MI, Robinson MB. 2004a. Neurotransmitter transporters: Why dance with so many partners? Curr Opin Pharmacol 4:30-35.
26. Gonzalez MI, Robinson MB. 2004b. Protein kinase C-dependent remodeling of glutamate transporter function. Mol Interv 4:48-58.
27. Gonzalez MI, Susarla BT, Fournier KM, Sheldon AL, Robinson MB. 2007. Constitutive endocytosis and recycling of the neuronal glutamate transporter, excitatory amino acid carrier 1. J Neurochem 103:1917-1931.
28. Heja L, Barabas P, Nyitrai G, Kekesi KA, Lasztoczi B, Toke O, Tarkanyi G, Madsen K, Schousboe A, Dobolyi A, Palkovits M, Kardos J. 2009. Glutamate uptake triggers transporter-mediated GABA release from astrocytes. PLoS ONE 4:e7153.
29. Huettner JE, Kerchner GA, Zhuo M. 2002. Glutamate and the presynaptic control of spinal sensory transmission. Neuroscientist 8:89-92.
30. Kanai Y, Hediger MA. 1992. Primary structure and functional characterization of a high-affinity glutamate transporter. Nature 360:467-471.
31. Keast JR, Stephensen TM. 2000. Glutamate and aspartate immunoreactivity in dorsal root ganglion cells supplying visceral and somatic targets and evidence for peripheral axonal transport. J Comp Neurol 424:577-587.
32. Keller EA, Zamparini A, Borodinsky LN, Gravielle MC, Fiszman ML. 2004. Role of allopregnanolone on cerebellar granule cells neurogenesis. Brain Res Dev Brain Res 153:13-17.
33. Kinkelin I, Brocker EB, Koltzenburg M, Carlton SM. 2000. Localization of ionotropic glutamate receptors in peripheral axons of human skin. Neurosci Lett 283:149-152.
34. Krishek BJ, Xie X, Blackstone C, Huganir RL, Moss SJ, Smart TG. 1994. Regulation of GABAA receptor function by protein kinase C phosphorylation. Neuron 12:1081-1095.
35. Lambert JJ, Belelli D, Hill-Venning C, Peters JA. 1995. Neurosteroids and GABAA receptor function. Trends Pharmacol Sci 16:295-303.
36. Lieberman EM, Abbott NJ, Hassan S. 1989. Evidence that glutamate mediates axon-to-Schwann cell signaling in the squid. Glia 2:94-102.
37. Magnaghi V. 2007. GABA and neuroactive steroid interactions in glia: New roles for old players? Curr Neuropharmacol 5:47-64.
38. Magnaghi V, Ballabio M, Cavarretta IT, Froestl W, Lambert JJ, Zucchi I, Melcangi RC. 2004. GABAB receptors in Schwann cells influence proliferation and myelin protein expression. Eur J Neurosci 19:2641-2649.
39. Magnaghi V, Veiga S, Ballabio M, Gonzalez LC, Garcia-Segura LM, Melcangi RC. 2006. Sex-dimorphic effects of progesterone and its reduced metabolites on gene expression of myelin proteins by rat Schwann cells. J Peripher Nerv Syst 11:111-118.
40. Magnaghi V, Procacci P, Tata AM. 2009. Novel pharmacological approaches to schwann cells as neuroprotective agents for peripheral nerve regeneration. Int Rev Neurobiol 87:295-315.
41. Magnaghi V, Parducz A, Frasca A, Ballabio M, Procacci P, Racagni G, Bonanno G, Fumagalli F. 2010. GABA synthesis in Schwann cells is induced by the neuroactive steroid allopregnanolone. J Neurochem 112:980-990.
42. Majewska MD, Harrison NL, Schwartz RD, Barker JL, Paul SM. 1986. Steroid hormone metabolites are barbiturate-like modulators of the GABA receptor. Science 232:1004-1007.
43. Melcangi RC, Cavarretta IT, Ballabio M, Leonelli E, Schenone A, Azcoitia I, Miguel Garcia-Segura L, Magnaghi V. 2005. Peripheral nerves: A target for the action of neuroactive steroids. Brain Res Brain Res Rev 48:328-338.
44. Perego C, Bulbarelli A, Longhi R, Caimi M, Villa A, Caplan MJ, Pietrini G. 1997. Sorting of two polytopic proteins, the gamma-aminobutyric acid and betaine transporters, in polarized epithelial cells. J Biol Chem 272:6584-6592.
45. Perego C, Vanoni C, Villa A, Longhi R, Kaech SM, Frohli E, Hajnal A, Kim SK, Pietrini G. 1999. PDZ-mediated interactions retain the epithelial GABA transporter on the basolateral surface of polarized epithelial cells. EMBO J 18:2384-2393.
46. Perego C, Vanoni C, Bossi M, Massari S, Basudev H, Longhi R, Pietrini G. 2000a. The GLT-1 and GLAST glutamate transporters are expressed on morphologically distinct astrocytes and regulated by neuronal activity in primary hippocampal cocultures. J Neurochem 75:1076-1084.
47. Perego C, Vanoni C, Massari S, Longhi R, Pietrini G. 2000b. Mammalian LIN-7 PDZ proteins associate with beta-catenin at the cell-cell junctions of epithelia and neurons. EMBO J 19:3978-3989.
48. Pinard A, Levesque S, Vallee J, Robitaille R. 2003. Glutamatergic modulation of synaptic plasticity at a PNS vertebrate cholinergic synapse. Eur J Neurosci 18:3241-3250.
49. Saitoh F, Araki T. 2010. Proteasomal degradation of glutamine synthetase regulates schwann cell differentiation. J Neurosci 30:1204-1212.
50. Schaffar N, Rao H, Kessler JP, Jean A. 1997. Immunohistochemical detection of glutamate in rat vagal sensory neurons. Brain Res 778:302-308.
51. Schumacher M, Akwa Y, Guennoun R, Robert F, Labombarda F, Desarnaud F, Robel P, De Nicola AF, Baulieu EE. 2000. Steroid synthesis and metabolism in the nervous system: Trophic and protective effects. J Neurocytol 29:307-326.
52. Schumacher M, Guennoun R, Stein DG, De Nicola AF. 2007. Progesterone: Therapeutic opportunities for neuroprotection and myelin repair. Pharmacol Ther 116:77-106.
53. Sedlacek M, Korinek M, Petrovic M, Cais O, Adamusova E, Chodounska H, Vyklicky L, Jr. 2008. Neurosteroid modulation of ionotropic glutamate receptors and excitatory synaptic transmission. Physiol Res 57:S49-S57.
54. Shimamoto K, Lebrun B, Yasuda-Kamatani Y, Sakaitani M, Shigeri Y, Yumoto N, Nakajima T. 1998. DL-threo-beta-benzyloxyaspartate, a potent blocker of excitatory amino acid transporters. Mol Pharmacol 53:195-201.
55. Sorkina T, Brian RH, Nancy RZ, Sorkin A. 2005. Constitutive and protein kinase C-induced internalization of the dopamine transporter is mediated by a clathrin-dependent mechanism. Traffic 6:157-170.
56. Sullivan SM, Lee A, Bjorkman ST, Miller SM, Sullivan RK, Poronnik P, Colditz PB, Pow DV. 2007. Cytoskeletal anchoring of GLAST determines susceptibility to brain damage: An identified role for GFAP. J Biol Chem 282:29414-29423.
57. Swanson RA, Liu J, Miller JW, Rothstein JD, Farrell K, Stein BA, Longuemare MC. 1997. Neuronal regulation of glutamate transporter subtype expression in astrocytes. J Neurosci 17:932-940.
58. Thompson HM, McNiven MA. 2006. Discovery of a new 'dynasore'. Nat Chem Biol 2:355-356.
59. Watkins JC. 2000. L-Glutamate as a central neurotransmitter: Looking back. Biochem Soc Trans 28:297-309.
60. Wu SZ, Jiang S, Sims TJ, Barger SW. 2005. Schwann cells exhibit excitotoxicity consistent with release of NMDA receptor agonists. J Neurosci Res 79:638-643.
61. Yoshimura M, Jessell T. 1990. Amino acid-mediated EPSPs at primary afferent synapses with substantia gelatinosa neurones in the rat spinal cord. J Physiol 430:315-335.
62. Zhang W, Slusher B, Murakawa Y, Wozniak KM, Tsukamoto T, Jackson PF, Sima AA. 2002. GCPII (NAALADase) inhibition prevents long-term diabetic neuropathy in type 1 diabetic BB/Wor rats. J Neurol Sci 194:21-28.