The glutamate transporter EAAT2 is transiently expressed in developing human cerebral white matter

Journal of Comparative Neurology

Volumn 501, Issue 6, 2007, Pages 879-890

  Desilva, Tara M ^a,c   Kinney, Hannah C ^a   Borenstein, Natalia S ^a   Trachtenberg, Felicia L ^b   Irwin, Nina ^a   Volpe, Joseph J ^a,c   Rosenberg, Paul A ^a,c  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b NEW ENGLAND RESEARCH INSTITUTES   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Cerebral palsy; Excitoxicity; Hypoxic ischemic injury; Myelination; Oligodendrocyte; Periventricular leukomalacia

Indexed keywords

DIGOXIGENIN; GLUTAMATE TRANSPORTER; PROTEIN EAAT1; PROTEIN EAAT2; PROTEIN EAAT3; UNCLASSIFIED DRUG; EXCITATORY AMINO ACID TRANSPORTER 1; EXCITATORY AMINO ACID TRANSPORTER 2; EXCITATORY AMINO ACID TRANSPORTER 3; MESSENGER RNA;

ARTICLE; BRAIN DEVELOPMENT; BRAIN ISCHEMIA; CONTROLLED STUDY; EXCITOTOXICITY; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; IN SITU HYBRIDIZATION; LEUKOMALACIA; NEUROFILAMENT; NUCLEOTIDE SEQUENCE; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; WHITE MATTER; ADULT; AGED; BRAIN CORTEX; COMPARATIVE STUDY; CYTOLOGY; FETUS; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOHISTOCHEMISTRY; LEARNING; METABOLISM; MIDDLE AGED; MYELINATED NERVE; NEWBORN; PHYSIOLOGY; TISSUE DISTRIBUTION;

ADULT; AGED; CEREBRAL CORTEX; CRITICAL PERIOD (PSYCHOLOGY); EXCITATORY AMINO ACID TRANSPORTER 1; EXCITATORY AMINO ACID TRANSPORTER 2; EXCITATORY AMINO ACID TRANSPORTER 3; FETUS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; IMMUNOHISTOCHEMISTRY; INFANT, NEWBORN; MIDDLE AGED; NERVE FIBERS, MYELINATED; OLIGODENDROGLIA; RNA, MESSENGER; TISSUE DISTRIBUTION;

EID: 34247559802     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21289     Document Type: Article

References (74)

1. Abercrombie M. 1946. Estimation of nuclear population from microtome sections. Anat Ree 94:239-247.
2. 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.
3. Arriza JL, Eliasof S, Kavanaugh MP, Amara SG. 1997. Excitatory amino acid transporter 5, a retinal glutamate transporter coupled to a chloride conductance. Proc Natl Acad Sci U S A 94:4155-4160.
4. Back SA, Luo NL, Borenstein NS, Levine JM, Volpe JJ, Kinney HC. 2001. Late oligodendrocyte progenitors coincide with the developmental window of vulnerability for human perinatal white matter injury. J Neurosci 21:1302-1312.
5. Bar-Peled O, Ben-Hur H, Biegon A, Groner Y, Dewhurst S, Furuta A, Rothstein JD. 1997. Distribution of glutamate transporter subtypes during human brain development. J Neurochem 69:2571-2580.
6. Benveniste H, Drejer J, Schousboe A, Diemer NH. 1984. Elevation of the extracellular concentrations of glutamate and aspartate in rat hippocampus during transient cerebral ischemia monitored by intracerebral microdialysis. J Neurochem 43:1369-1374.
7. Berger UV, Hediger MA. 1998. Comparative analysis of glutamate transporter expression in rat brain using differential double in situ hybridization. Anat Embryol 198:13-30.
8. Berger UV, Desilva TM, Chen W, Rosenberg PA. 2005. Cellular and subcellular mRNA localization of glutamate transporter isoforms GLT1a and GLT1b in rat brain by in situ hybridization. J Comp Neurol 492:78-89.
9. Bergles DE, Diamond JS, Jahr CE. 1999. Clearance of glutamate inside the synapse and beyond. Curr Opin Neurobiol 9:293-298.
10. Bergles DE, Roberts JDB, Somogyi P, Jahr CE. 2000. Glutamatergic synapses on oligodendrocyte precursor cells in the hippocampus. Nature 405:187-191.
11. Bezzi P, Carmignoto G, Pasti L, Vesce S, Rossi D, Rizzini BL, Pozzan T, Volterra A. 1998. Prostaglandins stimulate calcium-dependent glutamate release in astrocytes. Nature 391:281-285.
12. Bezzi P, Domercq M, Brambilla L, Galli R, Schols D, De Clercq E, Vescovi A, Bagetta G, Kollias G, Meldolesi J, Volterra A. 2001. CXCR4-activated astrocyte glutamate release via TNFalpha: amplification by microglia triggers neurotoxicity. Nat Neurosci 4:702-710.
13. Chen W, Aoki C, Mahadomrongkul V, Gruber CE, Wang GJ, Blitzblau R, Irwin N, Rosenberg PA. 2002. Expression of a variant form of the glutamate transporter GLT1 in neuronal cultures and in neurons and astrocytes in the rat brain. J Neurosci 22:2142-2152.
14. Chen W, Mahadomrongkul V, Berger UV, Bassan M, DeSilva T, Tanaka K, Irwin N, Aoki C, Rosenberg PA. 2004. The glutamate transporter GLT1a is expressed in excitatory axon terminals of mature hippocampal neurons. J Neurosci 24:1136-1148.
15. Danbolt NC. 2001. Glutamate uptake. Prog Neurobiol 65:1-105.
16. Deng W, Rosenberg PA, Volpe JJ, Jensen FE. 2003. Calcium-permeable AMPA/kainate receptors mediate toxicity and preconditioning by oxygen-glucose deprivation in oligodendrocyte precursors. Proc Natl Acad Sci U S A 100:6801-6806.
17. Fairman WA, Vandenberg RJ, Arriza JL, Kavanaugh MP, Amara SG. 1995. An excitatory amino-acid transporter with properties of a ligand-gated chloride channel. Nature 375:599-603.
18. Fern R, Möller T. 2000. Rapid ischemic cell death in immature oligodendrocytes: a fatal glutamate release feedback loop. J Neurosci 20:34-42.
19. Fine SM, Angel RA, Perry SW, Epstein LG, Rothstein JD, Dewhurst S, Gelbard HA. 1996. Tumor necrosis factor α inhibits glutamate uptake by primary human astrocytes - implications for pathogenesis of HIV-1 dementia. J Biol Chem 271:15303-15306.
20. Follett PL, Rosenberg PA, Volpe JJ, Jensen FE. 2000. NBQX attenuates excitotoxic injury in developing white matter. J Neurosci 20:9235-9241.
21. Follett PL, Talos DM, Volpe JJ, Jensen FE. 2003. AMPA receptor subunit expression in human white matter during window of susceptibility to periventricular leukomalacia. Ann Neurol 54(Suppl 3):S103.
22. Follett PL, Deng W, Dai W, Talos DM, Massillon LJ, Rosenberg PA, Volpe JJ, Jensen FE. 2004. Glutamate receptor-mediated oligodendrocyte toxicity in periventricular leukomalacia: a protective role for topiramate. J Neurosci 24:4412-4420.
23. Furuta A, Rothstein JD, Martin LJ. 1997. Glutamate transporter protein subtypes are expressed differentially during rat CNS development. J Neurosci 17:8363-8375.
24. Furuta A, Takashima S, Yokoo H, Rothstein JD, Wada K, Iwaki T. 2005. Expression of glutamate transporter subtypes during normal human corticogenesis and type II lissencephaly. Brain Res Dev Brain Res 155:155-164.
25. + channel block. J Neurosci 16:2659-2670.
26. Guillery RW. 2002. On counting and counting errors. J Comp Neurol 447:1-7.
27. Hagberg H. 1992. Hypoxic-ischemic damage in the neonatal brain: excitatory amino acids. Dev Pharmacol Ther 18:139-144.
28. Hu S, Sheng WS, Ehrlich LC, Peterson PK, Chao CC. 2000. Cytokine effects on glutamate uptake by human astrocytes. Neuroimmunomodulation 7:153-159.
29. Itoh T, Beesley J, Itoh A, Cohen AS, Kavanaugh B, Coulter DA, Grinspan JB, Pleasure D. 2002. AMPA glutamate receptor-mediated calcium signaling is transiently enhanced during development of oligodendrocytes. J Neurochem 81:390-402.
30. Karadottir R, Cavelier P, Bergersen LH, Attwell D. 2005. NMDA receptors are expressed in oligodendrocytes and activated in ischaemia. Nature 438:1162-1166.
31. Kimelberg HK, Goderie SK, Higman S, Pang S, Waniewski RA. 1990. Swelling-induced release of glutamate, aspartate, and taurine from astrocyte cultures. J Neurosci 10:1583-1591.
32. +-dependent transport in spinal cord white matter. Neuroscience 107:675-683.
33. Liao SL, Chen CJ. 2001. Differential effects of cytokines and redox potential on glutamate uptake in rat cortical glial cultures. Neurosci Lett 299:113-116.
34. Lin SC, Huck JH, Roberts JD, Macklin WB, Somogyi P, Bergles DE. 2005. Climbing fiber innervation of NG2-expressing glia in the mammalian cerebellum. Neuron 46:773-785.
35. Lipton SA, Rosenberg PA. 1994. Mechanisms of disease: excitatory amino acids as a final common pathway for neurologic disorders. N Engl J Med 330:613-622.
36. Loeliger M, Watson CS, Reynolds JD, Penning DH, Harding R, Bocking AD, Rees SM. 2003. Extracellular glutamate levels and neuropathology in cerebral white matter following repeated umbilical cord occlusion in the near term fetal sheep. Neuroscience 116:705-714.
37. Maragakis NJ, Dietrich J, Wong V, Xue H, Mayer-Proschel M, Rao MS, Rothstein JD. 2004. Glutamate transporter expression and function in human glial progenitors. Glia 45:133-143.
38. Matute C, Sánchez-Gómez MV, Martínez-Millán L, Miledi R. 1997. Glutamate receptor-mediated toxicity in optic nerve oligodendrocytes. Proc Natl Acad Sci U S A 94:8830-8835.
39. McDonald JW, Althomsons SP, Hyrc KL, Choi DW, Goldberg MP. 1998. Oligodendrocytes from forebrain are highly vulnerable to AMPA/kainate receptor-mediated excitotoxicity. Nat Med 4:291-297.
40. Meldrum B, Garthwaite J. 1990. Excitatory amino acid neurotoxicity and neurodegenerative disease. Trends Pharmacol Sci 11:379-387.
41. Micu I, Jiang Q, Coderre E, Ridsdale A, Zhang L, Woulfe J, Yin X, Trapp BD, McRory JE, Rehak R, Zamponi GW, Wang W, Stys PK. 2006. NMDA receptors mediate calcium accumulation in myelin during chemical ischaemia. Nature 439:988-992.
42. Milton ID, Banner SJ, Ince PG, Piggott NH, Fray AE, Thatcher N, Horne CH, Shaw PJ. 1997. Expression of the glial glutamate transporter EAAT2 in the human CNS: an immunohistochemical study. Brain Res Mol Brain Res 52:17-31.
43. Mitani A, Tanaka K. 2003. Functional changes of glial glutamate transporter GLT-1 during ischemia: an in vivo study in the hippocampal CA1 of normal mice and mutant mice lacking GLT-1. J Neurosci 23:7176-7182.
44. Nakamura Y, Ohmaki M, Murakami K, Yoneda Y. 2003. Involvement of protein kinase C in glutamate release from cultured microglia. Brain Res 962:122-128.
45. Nakayama T, Kawakami H, Tanaka K, Nakamura S. 1996. Expression of three glutamate transporter subtype mRNAs in human brain regions and peripheral tissues. Brain Res Mol Brain Res 36:189-192.
46. Nicholls D, Attwell D. 1990. The release and uptake of excitatory amino acids. Trends Pharmacol Sci 11:462-468.
47. Northington FJ, Traystman RJ, Koehler RC, Martin LJ. 1999. GLT1, glial glutamate transporter, is transiently expressed in neurons and develops astrocyte specificity only after midgestation in the ovine fetal brain. J Neurobiol 39:515-526.
48. Parpura V, Basarsky TA, Liu F, Jeftinija K, Jeftinija S, Haydon PG. 1994. Glutamate-mediated astrocyte-neuron signalling. Nature 369:744-747.
49. Pines G, Danbolt NC, Bjoras M, Zhang Y, Bendahan A, Eide L, Koepsell H, Storm-Mathisen J, Seeberg E, Kanner BI. 1992. Cloning and expression of a rat brain L-glutamate transporter. Nature 360:464-467.
50. Pitt D, Werner P, Raine CS. 2000. Glutamate excitotoxicity in a model of multiple sclerosis. Nat Med 6:67-70.
51. Roettger V, Lipton P. 1996. Mechanism of glutamate release from rat hippocampal slices during in vitro ischemia. Neuroscience 75:677-685.
52. Rosenberg PA, Aizenman E. 1989. Hundred-fold increase in neuronal vulnerability to glutamate toxicity in astrocyte-poor cultures of rat cerebral cortex. Neurosci Lett 103:162-168.
53. Rosenberg PA, Dai WM, Gan XD, Ali S, Fu J, Back SA, Sanchez RM, Segal MM, Follett PL, Jensen FE, Volpe JJ. 2003. Mature myelin basic protein-expressing oligodendrocytes are insensitive to kainate toxicity. J Neurosci Res 71:237-245.
54. Rossi DJ, Oshima T, Attwell D. 2000. Glutamate release in severe brain ischaemia is mainly by reversed uptake. Nature 403:316-321.
55. Salter MG, Fern R. 2005. NMDA receptors are expressed in developing oligodendrocyte processes and mediate injury. Nature 438:1167-1171.
56. Sambrook J, Russell DW. 2001. Northern Hybridization. Molecular Cloning. Cold Spring Harbor: CSHL Press p. 7.42-7.44.
57. Schaeren-Wiemers N, Gerfin-Moser A. 1993. A single protocol to detect transcripts of various types and expression levels in neural tissue and cultured cells: in situ hybridization using digoxigenin-labelled cRNA probes. Histochemistry 100:431-440.
58. Schmitt A, Asan E, Lesch K-P, Kugler P. 2002. A splice variant of glutamate transporter GLT1/EAAT2 expressed in neurons: cloning and localization in rat nervous system. Neuroscience 109:45-61.
59. Seki Y, Feustel PJ, Keller RW Jr, Tranmer BI, Kimelberg HK. 1999. Inhibition of ischemia-induced glutamate release in rat striatum by dihydrokinate and an anion channel blocker. Stroke 30:433-440.
60. Silverstein FS, Naik B, Simpson J. 1991. Hypoxia-ischemia stimulates hippocampal glutamate efflux in perinatal rat brain: an in vivo microdialysis study. Pediatr Res 30:587-590.
61. +-dependent glutamate/aspartate transporter from rat brain. Proc Natl Acad Sci U S A 89:10955-10959.
62. Szatkowski M, Barbour B, Attwell D. 1990. Non-vesicular release of glutamate from glial cells by reversed electrogenic glutamate uptake. Nature 348:443-446.
63. Takano T, Kang J, Jaiswal JK, Simon SM, Lin JH, Yu Y, Li Y, Yang J, Dienel G, Zielke HR, Nedergaard M. 2005. Receptor-mediated glutamate release from volume sensitive channels in astrocytes. Proc Natl Acad Sci U S A 102:16466-16471.
64. Takeuchi H, Jin S, Wang J, Zhang G, Kawanokuchi J, Kuno R, Sonobe Y, Mizuno T, Suzumura A. 2002. Tumor necrosis factor-α induces neurotoxicity via glutamate release from hemichannels of activated microglia in an autocrine manner. J Biol Chem 281:21362-21368.
65. Talos DM, Fishman RE, Park H-K, Folkerth RD, Follett PL, Volpe JJ, Jensen FE. 2005a. Developmental regulation of AMPA receptor subunit expression in forebrain and relationship to regional susceptibility to hypoxic/ischcemic injury: part I. Rodent cerebral white matter and cortex. J Comp Neurol (in press).
66. Talos DM, Follett PL, Folkerth RD, Fishman RE, Trachtenberg FL, Volpe JJ, Jensen FE. 2005b. Developmental regulation of AMPA receptor subunit expression in forebrain and relationship to regional susceptibility to hypoxic/ischemic injury: part II. Human cerebral white matter and cortex. J Comp Neurol (in press).
67. Tanaka K, Watase K, Manabe T, Yamada K, Watanabe M, Takahashi K, Iwama H, Nishikawa T, Ichihara N, Kikuchi T, Okuyama S, Kawashima N, Hori S, Takimoto M, Wada K. 1997. Epilepsy and exacerbation of brain injury in mice lacking the glutamate transporter GLT-I. Science 276:1699-1702.
68. Trotti D, Rossi D, Gjesdal O, Levy LM, Racagni G, Danbolt NC, Volterra A. 1996. Peroxynitrite inhibits glutamate transporter subtypes. J Biol Chem 271:5976-5979.
69. Volpe JJ. 2003. Cerebral white matter injury of the premature infant - more common than you think. Pediatrics 112:176-180.
70. Volterra A, Trotti D, Floridi S, Racagni G. 1994. Reactive oxygen species inhibit high-affinity glutamate uptake: molecular mechanism and neuropathological implications. Ann N Y Acad Sci 738:153-162.
71. 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.
72. Ye ZC, Sontheimer H. 1996. Cytokine modulation of glial glutamate uptake: a possible involvement of nitric oxide. Neuroreport 7:2181-2185.
73. Yoshioka A, Ikegaki N, Williams M, Pleasure D. 1996. Expression of N-methyl-D-aspartate (NMDA) and non-NMDA glutamate receptor genes in neuroblastoma, medulloblastoma, and other cell lines. J Neurosci Res 46:164-172.
74. Yuan X, Eisen AM, McBain CJ, Gallo V. 1998. A role for glutamate and its receptors in the regulation of oligodendrocyte development in cerebellar tissue slices. Development 125:2901-2914.