Laminar and subcellular heterogeneity of GLAST and GLT-1 immunoreactivity in the developing postnatal mouse hippocampus

Journal of Comparative Neurology

Volumn 522, Issue 1, 2014, Pages 204-224

  Schreiner, Alexandra E ^a   Durry, Simone ^a   Aida, Tomomi ^b   Stock, Martin C ^a   Rüther, Ulrich ^a   Tanaka, Kohichi ^b,c   Rose, Christine R ^a   Kafitz, Karl W ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Astrocyte; EAAT; GFAP, S100 ; Perivascular endfeet

Indexed keywords

EXCITATORY AMINO ACID TRANSPORTER; GLIAL FIBRILLARY ACIDIC PROTEIN; PROTEIN S100B; VESICULAR GLUTAMATE TRANSPORTER 1;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BIRTH; BLOOD BRAIN BARRIER; BRAIN DEVELOPMENT; CELL DENSITY; CELL HETEROGENEITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; JUVENILE ANIMAL; MOUSE; NEWBORN; NONHUMAN; PERINATAL PERIOD; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONTENT; PROTEIN EXPRESSION; STRATUM LACUNOSUM MOLECULARE; STRATUM PYRAMIDALE; UPREGULATION; WESTERN BLOTTING;

ASTROCYTE; EAAT; GFAP, S100Β; PERIVASCULAR ENDFEET;

ANIMALS; ASTROCYTES; BLOTTING, WESTERN; EXCITATORY AMINO ACID TRANSPORTER 1; EXCITATORY AMINO ACID TRANSPORTER 2; FEMALE; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED BALB C; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; NERVE TISSUE PROTEINS; SUBCELLULAR FRACTIONS; UP-REGULATION;

EID: 84888226782     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23450     Document Type: Article

References (86)

1. Aida T, Ito Y, Takahashi YK, Tanaka K. 2012. Overstimulation of NMDA receptors impairs early brain development in vivo. PLoS ONE 7:e36853.
2. Allaman I, Belanger M, Magistretti PJ. 2011. Astrocyte-neuron metabolic relationships: for better and for worse. Trends Neurosci 34:76-87.
3. Arnth-Jensen N, Jabaudon D, Scanziani M. 2002. Cooperation between independent hippocampal synapses is controlled by glutamate uptake. Nat Neurosci 5:325-331.
4. Arranz AM, Hussein A, Alix JJ, Ṕrez-Cerdá F, Allcock N, Matute C, Fern R. 2008. Functional glutamate transport in rodent optic nerve axons and glia. Glia 56:1353-1367.
5. Beart PM, O'Shea RD. 2007. Transporters for L-glutamate: an update on their pharmacological involvement. Br J Pharmacol 150:5-17.
6. Benediktsson AM, Marrs GS, Tu JC, Worley PF, Rothstein JD, Bergles DE, Dailey ME. 2012. Neuronal activity regulates glutamate transporter dynamics in developing astrocytes. Glia 60:175-188.
7. Bergles DE, Tzingounis AV, Jahr CE. 2002. Comparison of coupled and uncoupled currents during glutamate uptake by GLT-1 transporters. J Neurosci 22:10153-10162.
8. Bordey A, Sontheimer H. 1997. Postnatal development of ionic currents in rat hippocampal astrocytes in situ. J Neurophysiol 78:461-477.
9. Brunne B, Zhao S, Derouiche A, Herz J, May P, Frotscher M, Bock HH. 2010. Origin, maturation, and astroglial transformation of secondary radial glial cells in the developing dentate gyrus. Glia 58:1553-1569.
10. Bushong EA, Martone ME, Ellisman MH. 2004. Maturation of astrocyte morphology and the establishment of astrocyte domains during postnatal hippocampal development. Int J Dev Neurosci 22:73-86.
11. Chaudhry FA, Lehre KP, van Lookeren Campagne M, Ottersen OP, Danbolt NC, Storm-Mathisen J. 1995. Glutamate transporters in glial plasma membranes: highly differentiated localizations revealed by quantitative ultrastructural immunocytochemistry. Neuron 15:711-720.
12. Cholet N, Pellerin L, Magistretti PJ, Hamel E. 2002. Similar perisynaptic glial localization for the Na+, K+-ATPase alpha 2 subunit and the glutamate transporters GLAST and GLT-1 in the rat somatosensory cortex. Cereb Cortex 12:515-525.
13. Cooper AJ, Lai JC. 1987. Cerebral ammonia metabolism in normal and hyperammonemic rats. Neurochem Pathol 6:67-95.
14. Cooper AJ, McDonald JM, Gelbard AS, Gledhill RF, Duffy TE. 1979. The metabolic fate of 13N-labeled ammonia in rat brain. J Biol Chem 254:4982-4992.
15. Danbolt NC. 2001. Glutamate uptake. Prog Neurobiol 65:1-105.
16. +]coupled L-glutamate transporter purified from rat brain is located in glial cell processes. Neuroscience 51:295-310.
17. Deitmer JW, Rose CR. 2010. Ion changes and signalling in perisynaptic glia. Brain Res Rev 63:113-129.
18. Derouiche A, Rauen T. 1995. Coincidence of L-glutamate/L-aspartate transporter (GLAST) and glutamine synthetase (GS) immunoreactions in retinal glia: evidence for coupling of GLAST and GS in transmitter clearance. J Neurosci Res 42:131-143.
19. Derouiche A, Anlauf E, Aumann G, Muhlstadt B, Lavialle M. 2002. Anatomical aspects of glia-synapse interaction: the perisynaptic glial sheath consists of a specialized astrocyte compartment. J Physiol Paris 96:177-182.
20. Freeman MR. 2010. Specification and morphogenesis of astrocytes. Science 330:774-778.
21. Fritschy JM. 2008. Is my antibody-staining specific? How to deal with pitfalls of immunohistochemistry. Eur J Neurosci 28:2365-2370.
22. Furness DN, Dehnes Y, Akhtar AQ, Rossi DJ, Hamann M, Grutle NJ, Gundersen V, Holmseth S, Lehre KP, Ullensvang K, Wojewodzic M, Zhou Y, Attwell D, Danbolt NC. 2008. A quantitative assessment of glutamate uptake into hippocampal synaptic terminals and astrocytes: new insights into a neuronal role for excitatory amino acid transporter 2 (EAAT2). Neuroscience 157:80-94.
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. Gilley JA, Kernie SG. 2011. Excitatory amino acid transporter 2 and excitatory amino acid transporter 1 negatively regulate calcium-dependent proliferation of hippocampal neural progenitor cells and are persistently upregulated after injury. Eur J Neurosci 34:1712-1723.
25. Hartfuss E, Galli R, Heins N, Gotz M. 2001. Characterization of CNS precursor subtypes and radial glia. Dev Biol 229:15-30.
26. Haugeto O, Ullensvang K, Levy LM, Chaudhry FA, Honore T, Nielsen M, Lehre KP, Danbolt NC. 1996. Brain glutamate transporter proteins form homomultimers. J Biol Chem 271:27715-27722.
27. Hawkins RA, DeJoseph MR, Hawkins PA. 1995. Regional brain glutamate transport in rats at normal and raised concentrations of circulating glutamate. Cell Tissue Res 281:207-214.
28. Helms HC, Madelung R, Waagepetersen HS, Nielsen CU, Brodin B. 2012. In vitro evidence for the brain glutamate efflux hypothesis: brain endothelial cells cocultured with astrocytes display a polarized brain-to-blood transport of glutamate. Glia 60:2523-2533.
29. Hughes EG, Maguire JL, McMinn MT, Scholz RE, Sutherland ML. 2004. Loss of glial fibrillary acidic protein results in decreased glutamate transport and inhibition of PKA-induced EAAT2 cell surface trafficking. Brain Res Mol Brain Res 124:114-123.
30. Ishikawa M, Yoshitomi T, Zorumski CF, Izumi Y. 2011. Downregulation of glutamine synthetase via GLAST suppression induces retinal axonal swelling in a rat ex vivo hydrostatic pressure model. Invest Ophthalmol Vis Sci 52:6604-6616.
31. Jungblut M, Tiveron MC, Barrai S, Abrahamsen B, Knöbel S, Pennartz S. Schmitz J, Perraut M, Pfrieger FW, Stoffel W, Cremer H, Bosio A. 2012. Isolation and characterization of living primary astroglial cells using the new GLAST-specific monoclonal antibody ACSA-1. GLIA 60:894-907
32. Kim JS, Kim J, Kim Y, Yang M, Jang H, Kang S, Kim JC, Kim SH, Shin T, Moon C. 2011. Differential patterns of nestin and glial fibrillary acidic protein expression in mouse hippocampus during postnatal development. J Vet Sci 12:1-6.
33. Kimoto H, Eto R, Abe M, Kato H, Araki T. 2009. Alterations of glial cells in the mouse hippocampus during postnatal development. Cell Mol Neurobiol 29:1181-1189.
34. Kudryashov IE, Onufriev MV, Kudryashova IV, Gulyaeva NV. 2001. Periods of postnatal maturation of hippocampus: synaptic modifications and neuronal disconnection. Brain Res 132:113-120.
35. Kugler P, Schleyer V. 2004. Developmental expression of glutamate transporters and glutamate dehydrogenase in astrocytes of the postnatal rat hippocampus. Hippocampus 14:975-985.
36. Langer J, Rose CR. 2009. Synaptically induced sodium signals in hippocampal astrocytes in situ. J Physiol 587:5859-5877.
37. Lee A, Pow DV. 2010. Astrocytes: Glutamate transport and alternate splicing of transporters. Int J Biochem Cell Biol 42:1901-1906.
38. Lehre KP, Danbolt NC. 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.
39. Lehre KP, Levy LM, Ottersen OP, Storm-Mathisen J, Danbolt NC. 1995. Differential expression of two glial glutamate transporters in the rat brain: quantitative and immunocytochemical observations. J Neurosci 15:1835-1853.
40. Lieth E, Barber AJ, Xu B, Dice C, Ratz MJ, Tanase D, Strother JM. 1998. Glial reactivity and impaired glutamate metabolism in short-term experimental diabetic retinopathy. Diabetes 47:815-820.
41. Liu X, Bolteus AJ, Balkin DM, Henschel O, Bordey A. 2006. GFAP-expressing cells in the postnatal subventricular zone display a unique glial phenotype intermediate between radial glia and astrocytes. Glia 54:394-410.
42. Magavi S, Friedmann D, Banks G, Stolfi A, Lois C. 2012. Coincident generation of pyramidal neurons and protoplasmic astrocytes in neocortical columns. J Neurosci 32:4762-4772.
43. Mathiisen TM, Lehre KP, Danbolt NC, Ottersen OP. 2010. The perivascular astroglial sheath provides a complete covering of the brain microvessels: an electron microscopic 3D reconstruction. Glia 58:1094-1103.
44. Matsugami TR, Tanemura K, Mieda M, Nakatomi R, Yamada K, Kondo T, Ogawa M, Obata K, Watanabe M, Hashikawa T, Tanaka K. 2006. From the cover: indispensability of the glutamate transporters GLAST and GLT1 to brain development. Proc Natl Acad Sci U S A 103:12161-12166.
45. Meyer L, Wildanger D, Medda R, Punge A, Rizzoli SO, Donnert G, Hell SW. 2008. Dual-color STED microscopy at 30-nm focal-plane resolution. Small 4:1095-1100.
46. Middeldorp J, Hol EM. 2011. GFAP in health and disease. Prog Neurobiol 93:421-443.
47. Minelli A, Barbaresi P, Reimer RJ, Edwards RH, Conti F. 2001. The glial glutamate transporter GLT-1 is localized both in the vicinity of and at distance from axon terminals in the rat cerebral cortex. Neuroscience 108:51-59.
48. Ming GL, Song H. 2005. Adult neurogenesis in the mammalian central nervous system. Ann Rev Neurosci 28:223-250.
49. Nakagawa T, Otsubo Y, Yatani Y, Shirakawa H, Kaneko S. 2008. Mechanisms of substrate transport-induced clustering of a glial glutamate transporter GLT-1 in astroglial-neuronal cultures. Eur J Neurosci 28:1719-1730.
50. Nixdorf-Bergweiler BE, Albrecht D, Heinemann U. 1994. Developmental changes in the number, size, and orientation of GFAP-positive cells in the CA1 region of rat hippocampus. Glia 12:180-195.
51. Nosyreva ED, Huber KM. 2005. Developmental switch in synaptic mechanisms of hippocampal metabotropic glutamate receptor-dependent long-term depression. J Neurosci 25:2992-3001.
52. Olabarria M, Noristani HN, Verkhratsky A, Rodriguez JJ. 2010. Concomitant astroglial atrophy and astrogliosis in a triple transgenic animal model of Alzheimer's disease. Glia 58:831-838.
53. Omrani A, Melone M, Bellesi M, Safiulina V, Aida T, Tanaka K, Cherubini E, Conti F. 2009. Up-regulation of GLT-1 severely impairs LTD at mossy fibre-CA3 synapses. J Physiol 587:4575-4588.
54. Peacey E, Miller CC, Dunlop J, Rattray M. 2009. The four major N- and C-terminal splice variants of the excitatory amino acid transporter GLT-1 form cell surface homomeric and heteromeric assemblies. Mol Pharm 75:1062-1073.
55. Pekny M, Eliasson C, Siushansian R, Ding M, Dixon SJ, Pekna M, Wilson JX, Hamberger A. 1999. The impact of genetic removal of GFAP and/or vimentin on glutamine levels and transport of glucose and ascorbate in astrocytes. Neurochem Res 24:1357-1362.
56. Pfrieger FW. 2002. Role of glia in synapse development. Curr Opinion Neurobiol 12:486-490.
57. 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.
58. Raponi E, Agenes F, Delphin C, Assard N, Baudier J, Legraverend C, Deloulme JC. 2007. S100B expression defines a state in which GFAP-expressing cells lose their neural stem cell potential and acquire a more mature developmental stage. Glia 55:165-177.
59. Reichenbach A, Derouiche A, Kirchhoff F. 2010. Morphology and dynamics of perisynaptic glia. Brain Res Rev 63:11-25.
60. Riol H, Fages C, Tardy M. 1992. Transcriptional regulation of glial fibrillary acidic protein (GFAP)-mRNA expression during postnatal development of mouse brain. J Neurosci Res 32:79-85.
61. Rodnight R, Goncalves CA, Wofchuk ST, Leal R. 1997. Control of the phosphorylation of the astrocyte marker glial fibrillary acidic protein (GFAP) in the immature rat hippocampus by glutamate and calcium ions: possible key factor in astrocytic plasticity. Braz J Med Biol Res 30:325-338.
62. Rothstein JD, Martin L, Levey AI, Dykes-Hoberg M, Jin L, Wu D, Nash N, Kuncl RW. 1994. Localization of neuronal and glial glutamate transporters. Neuron 13:713-725.
63. Schlag BD, Vondrasek JR, Munir M, Kalandadze A, Zelenaia OA, Rothstein JD, Robinson MB. 1998. Regulation of the glial Na+-dependent glutamate transporters by cyclic AMP analogs and neurons. Mol Pharmacol 53:355-369.
64. Schools GP, Zhou M, Kimelberg HK. 2006. Development of gap junctions in hippocampal astrocytes: evidence that whole cell electrophysiological phenotype is an intrinsic property of the individual cell. J Neurophysiol 96:1383-1392.
65. Seifert G, Huttmann K, Binder DK, Hartmann C, Wyczynski A, Neusch C, Steinhauser C. 2009. Analysis of astroglial K+ channel expression in the developing hippocampus reveals a predominant role of the Kir4.1 subunit. J Neurosci 29:7474-7488.
66. Shibata T, Yamada K, Watanabe M, Ikenaka K, Wada K, Tanaka K, Inoue Y. 1997. Glutamate transporter GLAST is expressed in the radial glia-astrocyte lineage of developing mouse spinal cord. J Neurosci 17:9212-9219.
67. 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 U S A 89:10955-10959.
68. Suarez I, Bodega G, Fernandez B. 2000. Modulation of glutamate transporters (GLAST, GLT-1 and EAAC1) in the rat cerebellum following portocaval anastomosis. Brain Res 859:293-302.
69. Sullivan SM, Lee A, Bjorkman ST, Miller SM, Sullivan RK, Poronnik P, Colditz PB, Pow DV. 2007a. Cytoskeletal anchoring of GLAST determines susceptibility to brain damage: an identified role for GFAP. J Biol Chem 282:29414-29423.
70. Sullivan SM, Macnab LT, Bjorkman ST, Colditz PB, Pow DV. 2007b. GLAST1b, the exon-9 skipping form of the glutamate-aspartate transporter EAAT1 is a sensitive marker of neuronal dysfunction in the hypoxic brain. Neuroscience 149:434-445.
71. Takasaki C, Okada R, Mitani A, Fukaya M, Yamasaki M, Fujihara Y, Shirakawa T, Tanaka K, Watanabe M. 2008. Glutamate transporters regulate lesion-induced plasticity in the developing somatosensory cortex. J Neurosci 28:4995-5006.
72. Takayasu Y, Iino M, Takatsuru Y, Tanaka K, Ozawa S. 2009. Functions of glutamate transporters in cerebellar Purkinje cell synapses. Acta Physiol 197:1-12.
73. 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-1. Science 276:1699-1702.
74. Ullensvang K, Lehre KP, Storm-Mathisen J, Danbolt NC. 1997. Differential developmental expression of the two rat brain glutamate transporter proteins GLAST and GLT. Eur J Neurosci 9:1646-1655.
75. Ullian EM, Christopherson KS, Barres BA. 2004. Role for glia in synaptogenesis. Glia 47:209-216.
76. Vallejo-Illarramendi A, Domercq M, Matute C. 2005. A novel alternative splicing form of excitatory amino acid transporter 1 is a negative regulator of glutamate uptake. J Neurochem 95:341-348.
77. Verbich D, Prenosil GA, Chang PK, Murai KK, McKinney RA. 2012. Glial glutamate transport modulates dendritic spine head protrusions in the hippocampus. Glia 60:1067-1077.
78. Vina JR, DeJoseph MR, Hawkins PA, Hawkins RA. 1997. Penetration of glutamate into brain of 7-day-old rats. Metab Brain Dis 12:219-227.
79. Watase K, Hashimoto K, Kano M, Yamada K, Watanabe M, Inoue Y, Okuyama S, Sakagawa T, Ogawa S, Kawashima N, Hori S, Takimoto M, Wada K, Tanaka K. 1998. Motor discoordination and increased susceptibility to cerebellar injury in GLAST mutant mice. Eur J Neurosci 10:976-988.
80. Weir MD, Thomas DG. 1984. Effect of dexamethasone on glutamine synthetase and glial fibrillary acidic protein in normal and transformed astrocytes. Clin Neuropharm 7:303-306.
81. Willig KI, Kellner RR, Medda R, Hein B, Jakobs S, Hell SW. 2006. Nanoscale resolution in GFP-based microscopy. Nat Methods 3:721-723.
82. Wu Y, Zhang AQ, Yew DT. 2005. Age related changes of various markers of astrocytes in senescence-accelerated mice hippocampus. Neurochem Int 46:565-574.
83. Yang Y, Gozen O, Watkins A, Lorenzini I, Lepore A, Gao Y, Vidensky S, Brennan J, Poulsen D, Won Park J, Li Jeon N, Robinson MB, Rothstein JD. 2009. Presynaptic regulation of astroglial excitatory neurotransmitter transporter GLT1. Neuron 61:880-894.
84. Zhou J, Sutherland ML. 2004. Glutamate transporter cluster formation in astrocytic processes regulates glutamate uptake activity. J Neurosci 24:6301-6306.
85. Zhou M, Schools GP, Kimelberg HK. 2006. Development of GLAST(+) astrocytes and NG2(+) glia in rat hippocampus CA1: mature astrocytes are electrophysiologically passive. J Neurophysiol 95:134-143.
86. Zhu X, Bergles DE, Nishiyama A. 2008. NG2 cells generate both oligodendrocytes and gray matter astrocytes. Development 135:145-157.