Methodological limitations in determining astrocytic gene expression

Frontiers in Endocrinology

Volumn 4, Issue NOV, 2013, Pages

  Peng, Liang ^a   Guo, Chuang ^b   Wang, Tao ^b   Li, Baoman ^a   Gu, Li ^a   Wang, Zhanyou ^b  

^a CHINA MEDICAL UNIVERSITY   (China)

^b NORTHEASTERN UNIVERSITY   (China)

Author keywords

Astrocyte culture; BAC transgenic animals; Fluorescence assisted cell sorting; GFAP; Immunohistochemistry; In situ hybridization

Indexed keywords

EID: 84890305229     PISSN: None     EISSN: 16642392     Source Type: Journal    
DOI: 10.3389/fendo.2013.00176     Document Type: Review

References (149)

1. Norenberg MD, Martinez-Hernandez A. Fine structural localization of glutamine synthetase in astrocytes of rat brain. Brain Res (1979) 161:303-10. doi:10.1016/0006-8993(79)90071-4
2. Shank RP, Bennett GS, Freytag SO, Campbel GL. Pyruvate carboxylase: an astrocyte-specific enzyme implicated in the replenishment of amino acid neurotransmitter pools. Brain Res (1985) 329:364-7. doi:10.1016/0006-8993(85)90552-9
3. Kurz GM, Wiesinger H, Hamprecht B. Purification of cytosolic malic enzyme from bovine brain, generation of monoclonal antibodies, and immunocytochemical localization of the enzyme in glial cells of neural primary cultures. J Neurochem (1993) 60:1467-74. doi:10.1111/j.1471-4159.1993.tb03309.x
4. Lovatt D, Sonnewald U, Waagepetersen HS, Schousboe A, He W, Lin JH, et al. The transcriptome and metabolic gene signature of protoplasmic astrocytes in the adult murine cortex. J Neurosci (2007) 27:12255-66. doi:10.1523/JNEUROSCI.3404-07.2007
5. Li B, Hertz L, Peng L. Aralar mRNA and protein levels in neurons and astrocytes freshly isolated from young and adult mouse brain and in maturing cultured astrocytes. Neurochem Int (2012) 61:1325-32. doi:10.1016/j.neuint.2012.09.009
6. Cahoy JD, Emery B, Kaushal A, Foo LC, Zamanian JL, Christopherson KS, et al. A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J Neurosci (2008) 28:264-78. doi:10.1523/JNEUROSCI.4178-07.2008
7. Nolte C, Matyash M, Pivneva T, Schipke CG, Ohlemeyer C, Hanisch UK, et al. GFAP promoter-controlled EGFP-expressing transgenic mice: a tool to visualize astrocytes and astrogliosis in living brain tissue. Glia (2001) 33:72-86. doi:10.1002/1098-1136(20010101)33:1<72::AID-GLIA1007>3.0.CO;2-A
8. Hertz L, Lovatt D, Goldman SA, Nedergaard M. Adrenoceptors in brain: cellular gene expression and effects on astrocytic metabolism and [Ca(2+)]i. Neurochem Int (2010) 57:411-20. doi:10.1016/j.neuint.2010.03.019
9. Lovatt D, Nedergaard M. The astrocyte transcriptome. In: Kettenmann H, Ransom BR editors. Neuroglia. New York: Oxford University Press (2012). p. 347-57.
10. Doyle JP, Dougherty JD, Heiman M, Schmidt EF, Stevens TR, Ma G, et al. Application of a translational profiling approach for the comparative analysis of CNS cell types. Cell (2008) 135:749-62. doi:10.1016/j.cell.2008.10.029
11. 2+-regulated mitochondrial aspartate-glutamate carrier aralar1 in brain and prominent expression in the spinal cord. Brain Res Dev Brain Res (2003) 143:33-46. doi:10.1016/S0165-3806(03)00097-X
12. Berkich DA, Ola MS, Cole J, Sweatt AJ, Hutson M, LaNoue KF. Mitochondrial transport proteins of the brain. J Neurosci Res (2007) 85:3367-77. doi:10.1002/jnr.21500
13. Pardo B, Rodrigues TB, Contreras L, Garzón M, Llorente-Folch I, Kobayashi K, et al. Brain glutamine synthesis requires neuronal-born aspartate as amino donor for glial glutamate formation. J Cereb Blood Flow Metab (2011) 31:90-101. doi:10.1038/jcbfm.2010.146
14. Schmitt A, Asan E, Püschel B, Kugler P. Cellular and regional distribution of the glutamate transporter GLAST in the CNS of rats: nonradioactive in situ hybridization and comparative immunocytochemistry. J Neurosci (1997) 17:1-10.
15. Lehre KP, Levy LM, Ottersen OP, Storm-Mathisen J, Danbolt NC. Differential expression of two glial glutamate transporters in the rat brain: quantitative and immunocytochemical observations. J Neurosci (1995) 15:1835-53.
16. Chaudhry FA, Lehre KP, van Lookeren CM, Ottersen OP, Danbolt NC, Storm-Mathisen J. Glutamate transporters in glial plasma membranes: highly differentiated localizations revealed by quantitative ultrastructural immunocytochemistry. Neuron (1995) 15:711-20. doi:10.1016/0896-6273(95)90158-2
17. Derouiche A, Rauen T. 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 (1995) 42:131-43. doi:10.1002/jnr.490420115
18. Kondo K, Hashimoto H, Kitanaka J, Sawada M, Suzumura A, Marunouchi T, et al. Expression of glutamate transporters in cultured glial cells. Neurosci Lett (1995) 188:140-2. doi:10.1016/0304-3940(95)11408-O
19. Yamada K, Watanabe M, Shibata T, Nagashima M, Tanaka K, Inoue Y. Glutamate transporter GLT-1 is transiently localized on growing axons of the mouse spinal cord before establishing astrocytic expression. J Neurosci (1998) 18:5706-13.
20. Utsumi M, Ohno K, Onchi H, Sato K, Tohyama M. Differential expression patterns of three glutamate transporters (GLAST, GLT1 and EAAC1) in the rat main olfactory bulb. Brain Res Mol Brain Res (2001) 92:1-11. doi:10.1016/S0169-328X(01)00098-5
21. Bruhn T, Levy LM, Nielsen M, Christensen T, Johansen FF, Diemer NH. Ischemia induced changes in expression of the astrocyte glutamate transporter GLT1 in hippocampus of the rat. Neurochem Int (2000) 37:277-85. doi:10.1016/S0197-0186(00)00029-2
22. +-dependent glutamate transporters by cyclic AMP analogs and neurons. Mol Pharmacol (1998) 53:355-69.
23. Rodriguez-Kern A, Gegelashvili M, Schousboe A, Zhang J, Sung L, Gegelashvili G. 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 (2003) 43:363-70. doi:10.1016/S0197-0186(03)00023-8
24. Voutsinos B, Dutuit M, Reboul A, Fevre-Montange M, Bernard A, Trouillas P, et al. Serotoninergic control of the activity and expression of glial GABA transporters in the rat cerebellum. Glia (1998) 23:45-60. doi:10.1002/(SICI)1098-1136(199805)23:1<45::AID-GLIA5>3.0.CO;2-3
25. Gadea A, López-Colomé AM. Glial transporters for glutamate, glycine, and GABA: II. GABA transporters. J Neurosci Res (2001) 63:461-8. doi:10.1002/jnr.1040
26. Minelli A, DeBiasi S, Brecha NC, Zuccarello LV, Conti F. GAT-3, a high-affinity GABA plasma membrane transporter, is localized to astrocytic processes, and it is not confined to the vicinity of GABAergic synapses in the cerebral cortex. J Neurosci (1996) 16:6255-64.
27. Itouji A, Sakai N, Tanaka C, Saito N. Neuronal and glial localization of two GABA transporters (GAT1 and GAT3) in the rat cerebellum. Brain Res Mol Brain Res (1996) 37:309-16. doi:10.1016/0169-328X(95)00342-P
28. Vitellaro-Zuccarello L, Calvaresi N, De Biasi S. Expression of GABA transporters, GAT-1 and GAT-3, in the cerebral cortex and thalamus of the rat during postnatal development. Cell Tissue Res (2003) 313:245-57. doi:10.1007/s00441-003-0746-9
29. Guthmann A, Fritschy JM, Ottersen OP, Torp R, Herbert H. GABA, GABA transporters, GABA(A) receptor subunits, and GAD mRNAs in the rat parabrachial and Kölliker-Fuse nuclei. J Comp Neurol (1998) 400:229-43. doi:10.1002/(SICI)1096-9861(19981019)400:2<229::AID-CNE5>3.3.CO;2-C
30. Bitoun M, Tappaz M. Gene expression of the transporters and biosynthetic enzymes of the osmolytes in astrocyte primary cultures exposed to hyperosmotic conditions. Glia (2000) 32:165-76. doi:10.1002/1098-1136(200011)32:2<165::AID-GLIA60>3.3.CO;2-U
31. Olsen M, Sarup A, Larsson OM, Schousboe A. Effect of hyperosmotic conditions on the expression of the betaine-GABA-transporter (BGT-1) in cultured mouse astrocytes. Neurochem Res (2005) 30:855-65. doi:10.1007/s11064-005-6879-3
32. Anderson CM, Xiong W, Geiger JD, Young JD, Cass CE, Baldwin SA, et al. Distribution of equilibrative, nitrobenzylthioinosine-sensitive nucleoside transporters (ENT1) in brain. J Neurochem (1999) 73:867-73. doi:10.1046/j.1471-4159.1999.0730867.x
33. Parkinson FE, Damaraju VL, Graham K, Yao SY, Baldwin SA, Cass CE, et al. Molecular biology of nucleoside transporters and their distributions and functions in the brain. Curr Top Med Chem (2011) 11:948-72. doi:10.2174/156802611795347582
34. Li B, Gu L, Hertz L, Peng L. Expression of nucleoside transporter in freshly isolated neurons and astrocytes from mouse brain. Neurochem Res (2013) 38(11):2351-8. doi:10.1007/s11064-013-1146-5
35. Peng L, Huang R, Yu AC, Fung KY, Rathbone MP, Hertz L. Nucleoside transporter expression and function in cultured mouse astrocytes. Glia (2005) 52:25-35. doi:10.1002/glia.20216
36. Dahlin A, Xia L, Kong W, Hevner R, Wang J. Expression and immunolocalization of the plasma membrane monoamine transporter in the brain. Neuroscience (2007) 146:1193-211. doi:10.1016/j.neuroscience.2007.01.072
37. Redzic ZB, Malatiali SA, Al-Bader M, Al-Sarraf H. Effects of hypoxia, glucose deprivation and recovery on the expression of nucleoside transporters and adenosine uptake in primary culture of rat cortical astrocytes. Neurochem Res (2010) 35:1434-44. doi:10.1007/s11064-010-0203-6
38. Kaplan JH. Biochemistry of Na,K-ATPase. Annu Rev Biochem (2002) 71:511-35. doi:10.1146/annurev.biochem.71.102201.141218
39. Lecuona E, Luquín S, Avila J, García-Segura LM, Martín-Vasallo P. Expression of the beta 1 and beta 2(AMOG) subunits of the Na,K-ATPase in neural tissues: cellular and developmental distribution patterns. Brain Res Bull (1996) 40:167-74. doi:10.1016/0361-9230(96)00042-1
40. McGrail KM, Phillips JM, Sweadner KJ. Immunofluorescent localization of three Na, K-ATPase isozymes in the rat central nervous system: both neurons and glia can express more than one Na, K-ATPase. J Neurosci (1991) 11:381-91.
41. Peng L, Martin-Vasallo P, Sweadner KJ. Isoforms of Na,K-ATPase alpha and beta subunits in the rat cerebellum and in granule cell cultures. J Neurosci (1997) 17:3488-502.
42. +-ATPase alpha-and beta-subunit isoforms within the rat central nervous system. Proc Natl Acad Sci U S A (1991) 88:7425-9. doi:10.1073/pnas.88.16.7425
43. Li B, Hertz L, Peng L. Cell-specific mRNA alterations in Na(+), K(+)-ATPase a and ß isoforms and FXYD in mice treated chronically with carbamazepine, an anti-bipolar drug. Neurochem Res (2013) 38:834-41. doi:10.1007/s11064-013-0986-3
44. Brines ML, Gulanski BI, Gilmore-Hebert M, Greene AL, Benz EJ, Robbins RJ. Cytoarchitectural relationships between [3H]ouabain binding and mRNA for isoforms of the sodium pump catalytic subunit in rat brain. Brain Res Mol Brain Res (1991) 10:139-50. doi:10.1016/0169-328X(91)90104-6
45. Price TJ, Hargreaves KM, Cervero F. Protein expression and mRNA cellular distribution of the NKCC1 cotransporter in the dorsal root and trigeminal ganglia of the rat. Brain Res (2006) 1112:146-58. doi:10.1016/j.brainres.2006.07.012
46. MacVicar BA, Feighan D, Brown A, Ransom B. Intrinsic optical signals in the rat optic nerve: role for K(+) uptake via NKCC1 and swelling of astrocytes. Glia (2002) 37:114-23. doi:10.1002/glia.10023
47. Li B, Dong L, Wang B, Cai L, Jiang N, Peng L. Cell type-specific gene expression and editing responses to chronic fluoxetine treatment in the in vivo mouse brain and their relevance for stress-induced anhedonia. Neurochem Res (2012) 37:2480-95. doi:10.1007/s11064-012-0814-1
48. Song D, Li B, Yan E, Man Y, Wolfson M, Chen Y, et al. Chronic treatment with anti-bipolar drugs causes intracellular alkalinization in astrocytes, altering their functions. Neurochem Res (2012) 37:2524-40. doi:10.1007/s11064-012-0837-7
49. Kimelberg HK. Functions of mature mammalian astrocytes: a current view. Neuroscientist (2010) 16:79-106. doi:10.1177/1073858409342593
50. Foo LC, Allen NJ, Bushong EA, Ventura PB, Chung WS, Zhou L, et al. Development of a method for the purification and culture of rodent astrocytes. Neuron (2011) 8:799-811. doi:10.1016/j.neuron.2011.07.022
51. Hertz L, Code WE. Calcium channel signalling in astrocytes. In: Paoletti R, Godfraind T, Vankoullen PM editors. Calcium Antagonists: Pharmacology and Clinical Research. Boston: Kluwer (1993). p. 205-13.
52. + at concentrations reached in the extracellular space during neuronal activity promotes a Ca2+-dependent glycogen hydrolysis in mouse cerebral cortex. J Neurosci (1988) 8:1922-8.
53. Juurlink BH, Hertz L. Astrocytes. In: Boulton AA, Baker GB, Walz W editors. Practical Cell Culture Techniques. Tatowa, NJ: The Humana Press (1992). p. 269-321.
54. Walz W, Kimelberg HK. Differences in cation transport properties of primary astrocyte cultures from mouse and rat brain. Brain Res (1985) 340:333-40. doi:10.1016/0006-8993(85)90930-8
55. Hawkins RA, DeJoseph MR, Hawkins PA. Regional brain glutamate transport in rats at normal and raised concentrations of circulating glutamate. Cell Tissue Res (1995) 281:207-14. doi:10.1007/BF00583389
56. Dienel GA, Hertz L. Glucose and lactate metabolism during brain activation. J Neurosci Res (2001) 66:824-38. doi:10.1002/jnr.10079
57. Fonnum F. The distribution of glutamate decarboxylase and aspartate transaminase in subcellular fractions of rat and guinea-pig brain. Biochem J (1968) 106:401-12.
58. Horio Y, Tanaka T, Taketoshi M, Uno T, Wada H. Rat cytosolic aspartate aminotransferase: regulation of its mRNA and contribution to gluconeogenesis. J Biochem (1988) 103:805-8.
59. McKenna MC, Stevenson JH, Huang X, Tildon JT, Zielke CL, Hopkins IB. Mitochondrial malic enzyme activity is much higher in mitochondria from cortical synaptic terminals compared with mitochondria from primary cultures of cortical neurons or cerebellar granule cells. Neurochem Int (2000) 36:451-9. doi:10.1016/S0197-0186(99)00148-5
60. Schousboe A, Svenneby G, Hertz L. Uptake and metabolism of glutamate in astrocytes cultured from dissociated mouse brain hemispheres. J Neurochem (1977) 2:999-1005. doi:10.1111/j.1471-4159.1977.tb06503.x
61. Erecinska M, Pleasure D, Nelson D, Nissim I, Yudkoff M. Cerebral aspartate utilization: near-equilibrium relationships in aspartate aminotransferase reaction. J Neurochem (1993) 60:1696-706. doi:10.1111/j.1471-4159.1993.tb13393.x
62. Kugler P. Cytochemical demonstration of aspartate aminotransferase in the mossy-fibre system of the rat hippocampus. Histochemistry (1987) 87:623-5. doi:10.1007/BF00492481
63. Würdig S, Kugler P. Histochemistry of glutamate metabolizing enzymes in the rat cerebellar cortex. Neurosci Lett (1991) 130:165-8. doi:10.1016/0304-3940(91)90388-A
64. Altschuler RA, Neises GR, Harmison GG, Wenthold RJ, Fex J. Immunocytochemical localization of aspartate aminotransferase immunoreactivity in cochlear nucleus of the guinea pig. Proc Natl Acad Sci U S A (1981) 78:6553-7. doi:10.1073/pnas.78.10.6553
65. Contreras L, Urbieta A, Kobayashi K, Saheki T, Satrústegui J. Low levels of citrin (SLC25A13) expression in adult mouse brain restricted to neuronal clusters. J Neurosci Res (2010) 88:1009-16. doi:10.1002/jnr.22283
66. Yu AC, Drejer J, Hertz L, Schousboe A. Pyruvate carboxylase activity in primary cultures of astrocytes and neurons. J Neurochem (1983) 41:1484-7. doi:10.1111/j.1471-4159.1983.tb00849.x
67. Kao-Jen J, Wilson JE. Localization of hexokinase in neural tissue: electron microscopic studies of rat cerebellar cortex. J Neurochem (1980) 35:667-78. doi:10.1111/j.1471-4159.1980.tb03706.x
68. 14C-trajectography combined with immunohistochemistry. J Cereb Blood Flow Metab (2004) 24:1004-114. doi:10.1097/01.WCB.0000128533.84196.D8
69. Hertz L, Dienel GA. Energy metabolism in the brain. Int Rev Neurobiol (2002) 51:1-102. doi:10.1016/S0074-7742(02)51003-5
70. Hertz L. Astrocytic energy metabolism and glutamate formation-relevance for 13C-NMR spectroscopy and importance of cytosolic/mitochondrial trafficking. Magn Reson Imaging (2011) 29:1319-29. doi:10.1016/j.mri.2011.04.013
71. Itoh Y, Esaki T, Shimoji K, Cook M, Law MJ, Kaufman E, et al. Dichloroacetate effects on glucose and lactate oxidation by neurons and astroglia in vitro and on glucose utilization by brain in vivo. Proc Natl Acad Sci U S A (2003) 100:4879-84. doi:10.1073/pnas.0831078100
72. Colombo JA, Schleicher A, Zilles K. Patterned distribution of immunoreactive astroglial processes in the striate (V1) cortex of New World monkeys. Glia (1999) 25:85-92. doi:10.1002/(SICI)1098-1136(19990101)25:1<85::AID-GLIA8>3.0.CO;2-R
73. Hutson SM, Cole JT, Sweatt AJ, LaNoue KF. Is the anaplerotic enzyme pyruvate carboxylase (PC) only expressed in astrocytes? J Neurochem (2008) 104(Suppl 1):58-9. doi:10.1002/mrmp.22419970129
74. Vogel R, Hamprecht B, Wiesinger H. Malic enzyme isoforms in astrocytes: comparative study on activities in rat brain tissue and astroglia-rich primary cultures. Neurosci Lett (1998) 247:123-6. doi:10.1016/S0304-3940(98)00290-0
75. Juurlink BH, Schousboe A, Jørgensen OS, Hertz L. Induction by hydrocortisone of glutamine synthetase in mouse primary astrocyte cultures. J Neurochem (1981) 36:136-42. doi:10.1111/j.1471-4159.1981.tb02388.x
76. Tardy M, Costa MF, Fages C, Bardakdjian J, Gonnard P. Uptake and binding of serotonin by primary cultures of mouse astrocytes. Dev Neurosci (1982) 5:19-26. doi:10.1159/000112658
77. Cammer W. Glutamine synthetase in the central nervous system is not confined to astrocytes. J Neuroimmunol (1990) 26:173-8. doi:10.1016/0165-5728(90)90088-5
78. D'Amelio F, Eng LF. Glutamine synthetase in the spinal cord and brain. Glia (1991) 4:332. doi:10.1002/glia.440040312
79. Miyake T, Kitamura T. Glutamine synthetase immunoreactivity in two types of mouse brain glial cells. Brain Res (1992) 586:53-60. doi:10.1016/0006-8993(92)91370-T
80. Derouiche A. Immunocytochemical studies on astrocyte compartmentation. In: Hertz L editor. Non-Neuronal Cells in the Nervous System: Function and Dysfunction, Adv Mol Cell Bio 31. Amsterdam: Elsevier Press (2004). p. 147-63.
81. Hertz L, Yu A, Svenneby G, Kvamme E, Fosmark H, Schousboe A. Absence of preferential glutamine uptake into neurons-an indication of a net transfer of TCA constituents from nerve endings to astrocytes? Neurosci Lett (1980) 16:103-9. doi:10.1016/0304-3940(80)90109-3
82. Boulland JL, Osen KK, Levy LM, Danbolt NC, Edwards RH, Storm-Mathisen J, et al. Cell-specific expression of the glutamine transporter SN1 suggests differences in dependence on the glutamine cycle. Eur J Neurosci (2002) 15:1615-31. doi:10.1046/j.1460-9568.2002.01995.x
83. Melone M, Varoqui H, Erickson JD, Conti F. Localization of the Na(+)-coupled neutral amino acid transporter 2 in the cerebral cortex. Neuroscience (2006) 140:281-92. doi:10.1016/j.neuroscience.2006.02.042
84. Chaudhry FA, Krizaj D, Larsson P, Reimer RJ, Wreden C, Storm-Mathisen J, et al. Coupled and uncoupled proton movement by amino acid transport system N. EMBO J (2011) 20:7041-51. doi:10.1093/emboj/20.24.7041
85. Hamdaniel H, Gudbrandsen M, Bjørkmo M, Chaudhry FA. The system N transporter SN2 doubles as a transmitter precursor furnisher and a potential regulator of NMDA receptors. Glia (2012) 60:1671-83. doi:10.1002/glia.22386
86. Danbolt NC. Glutamate uptake. Prog Neurobiol (2001) 65:1-105. doi:10.1016/S0301-0082(00)00067-8
87. Aoki C, Milner TA, Berger SB, Sheu KF, Blass JP, Pickel VM. Glial glutamate dehydrogenase: ultrastructural localization and regional distribution in relation to the mitochondrial enzyme, cytochrome oxidase. J Neurosci Res (1987) 18:305-18. doi:10.1002/jnr.490180207
88. Kugler P. In situ measurements of enzyme activities in the brain. Histochem J (1993) 25:329-38. doi:10.1007/BF00159497
89. Selkirk JV, Stiefel TH, Stone IM, Naeve GS, Foster AC, Poulsen DJ. Over-expression of the human EAAT2 glutamate transporter within neurons of mouse organotypic hippocampal slice cultures leads to increased vulnerability of CA1 pyramidal cells. Eur J Neurosci (2005) 21:2291-6. doi:10.1111/j.1460-9568.2005.04059.x
90. Hertz L, Schousboe A, Boechler N, Mukerji S, Fedoroff S. Kinetic characteristics of the glutamate uptake into normal astrocytes in cultures. Neurochem Res (1978) 3:1-14. doi:10.1007/BF00964356
91. Swanson RA, Liu J, Miller JW, Rothstein JD, Farrell K, Stein BA, et al. Neuronal regulation of glutamate transporter subtype expression in astrocytes. J Neurosci (1997) 17:932-40.
92. Hertz L, Wu PH, Schousboe A. Evidence for net uptake of GABA into mouse astrocytes in primary cultures-its sodium dependence and potassium independence. Neurochem Res (1978) 3:313-23. doi:10.1007/BF00965577
93. Larsson OM, Thorbek P, Krogsgaard-Larsen P, Schousboe A. Effect of homo-beta-proline and other heterocyclic GABA analogues on GABA uptake in neurons and astroglial cells and on GABA receptor binding. J Neurochem (1981) 37:1509-16. doi:10.1111/j.1471-4159.1981.tb06320.x
94. Hertz L, Dienel GA. Lactate transport and transporters: general principles and functional roles in brain cells. J Neurosci Res (2005) 79:11-8. doi:10.1002/jnr.20294
95. Matz H, Hertz L. Adenosine metabolism in neurons and astrocytes in primary cultures. J Neurosci Res (1989) 24:260-7. doi:10.1002/jnr.490240218
96. Studer FE, Fedele DE, Marowsky A, Schwerdel C, Wernli K, Vogt K, et al. Shift of adenosine kinase expression from neurons to astrocytes during postnatal development suggests dual functionality of the enzyme. Neuroscience (2006) 142:125-37. doi:10.1016/j.neuroscience.2006.06.016
97. Parkinson FE, Ferguson J, Zamzow CR, Xiong W. Gene expression for enzymes and transporters involved in regulating adenosine and inosine levels in rat forebrain neurons, astrocytesand C6 glioma cells. J Neurosci Res (2006) 84:801-8. doi:10.1002/jnr.20988
98. Kimelberg HK, Frangakis MV. Furosemide-and bumetanide-sensitive ion transport and volume control in primary astrocyte cultures from ratbrain. Brain Res (1985) 361:125-34. doi:10.1016/0006-8993(85)91282-X
99. Walz W, Hinks EC. A transmembrane sodium cycle in astrocytes. Brain Res (1986) 368:226-32. doi:10.1016/0006-8993(86)90565-2
100. +/Cl-cotransport in primary cultures of rat astrocytes. Biochim Biophys Acta (1987) 903:411-6. doi:10.1016/0005-2736(87)90047-2
101. Kanaka C, Ohno K, Okabe A, Kuriyama K, Itoh T, Fukuda A, et al. The differential expression patterns of messenger RNAs encoding K-Cl cotransporters (KCC1,2) and Na-K-2Cl cotransporter (NKCC1) in the rat nervous system. Neuroscience (2001) 104:933-46. doi:10.1016/S0306-4522(01)00149-X
102. Mikawa S, Wang C, Shu F, Wang T, Fukuda A, Sato K. Developmental changes in KCC1, KCC2 and NKCC1 mRNAs in the rat cerebellum. Brain Res Dev Brain Res (2002) 136:93-100. doi:10.1016/S0165-3806(02)00345-0
103. Walz W. Role of Na/K/Cl cotransport in astrocytes. Can J Physiol Pharmacol (1992) 70(Suppl):S260-2. doi:10.1139/y92-270
104. Walz W, Hertz L. Intense furosemide-sensitive potassium accumulation in astrocytes in the presence of pathologically high extracellular potassium levels. J Cereb Blood Flow Metab (1984) 4:301-4. doi:10.1038/jcbfm.1984.42
105. Cherksey BD, Zeuthen T. [3H]bumetanide binding to the purified putative co-transporter protein. Acta Physiol Scand (1988) 133:267-8. doi:10.1111/j.1748-1716.1988.tb08406.x
106. +-dependent transport of chloride. J Neurochem (1972) 19:663-85. doi:10.1111/j.1471-4159.1972.tb01383.x
107. Jayakumar AR, Panickar KS, Curtis KM, Tong XY, Moriyama M, Norenberg MD. Na-K-Cl cotransporter-1 in the mechanism of cell swelling in cultured astrocytes after fluid percussion injury. J Neurochem (2011) 117:437-48. doi:10.1111/j.1471-4159.2011.07211.x
108. Ramos-Vara JA. Technical aspects of immunohistochemistry. Vet Pathol (2005) 42:405-26. doi:10.1354/vp.42-4-405
109. Sofroniew MV, Vinters HV. Astrocytes: biology and pathology. Acta Neuropathol (2010) 119:7-35. doi:10.1007/s00401-009-0619-8
110. + astrocytes in vivo in astroglial reporter mice. Glia (2011) 59:200-7. doi:10.1002/glia.21089
111. + exchanger regulatory factor 1 is a PDZ scaffold for the astroglial glutamate transporter GLAST. Glia (2007) 55:119-29. doi:10.1002/glia.20439
112. Williams SM, Sullivan RK, Scott HL, Finkelstein DI, Colditz PB, Lingwood BE, et al. Glial glutamate transporter expression patterns in brains from multiple mammalian species. Glia (2005) 49:520-41. doi:10.1002/glia.20139
113. Derouiche A, Frotscher M. Peripheral astrocyte processes: monitoring by selective immunostaining for the actin-binding ERM proteins. Glia (2001) 36:330-41. doi:10.1002/glia.1120
114. Lee CK, Sunkin SM, Kuan C, Thompson CL, Pathak S, Ng L, et al. Quantitative methods for genome-scale analysis of in situ hybridization and correlation with microarray data. Genome Biol (2008) 9:R23. doi:10.1186/gb-2008-9-1-r23
115. Lein ES, Hawrylycz MJ, Ao N. Genome-wide atlas of gene expression in the adult mouse brain. Nature (2007) 445:168-76. doi:10.1038/nature05453
116. Guo Y, Xiao P, Lei S, Deng F, Xiao GG, Liu Y, et al. How is mRNA expression predictive for protein expression? A correlation study on human circulating monocytes. Acta Biochim Biophys Sin (Shanghai) (2008) 40:426-36. doi:10.1111/j.1745-7270.2008.00418.x
117. Gry M, Rimini R, Strömberg S, Asplund A, Pontén F, Uhlén M, et al. Correlations between RNA and protein expression profiles in 23 human cell lines. BMC Genomics (2009) 10:365. doi:10.1186/1471-2164-10-365
118. Schwanhäusser B, Busse D, Li N, Dittmar G, Schuchhardt J, Wolf J, et al. Global quantification of mammalian gene expression control. Nature (2011) 473:337-42. doi:10.1038/nature10098
119. Hydén H, Rapallino MV, Cupello A. Unraveling of important neurobiological mechanisms by the use of pure, fully differentiated neurons obtained from adult animals. Prog Neurobiol (2000) 60:471-99. doi:10.1016/S0301-0082(99)00035-0
120. Hertz L, Hansson E, Rönnbäck L. Signaling and gene expression in the neuron-glia unit during brain function and dysfunction: Holger Hyden in memoriam. Neurochem Int (2001) 39:227-52. doi:10.1016/S0197-0186(01)00017-1
121. Norton WT, Poduslo SE. Neuronal soma and whole neuroglia of rat brain: a new isolation technique. Science (1970) 167:1144-5. doi:10.1126/science.167.3921.1144
122. Henn FA, Goldstein MN, Hamberger A. Uptake of the neurotransmitter candidate glutamate by glia. Nature (1974) 249:663-4. doi:10.1038/249663a0
123. Hamberger A, Nyström B, Sellström A, Woiler CT. Amino acid transport in isolated neurons and glia. Adv Exp Med Biol (1976) 69:221-36. doi:10.1007/978-1-4684-3264-0_17
124. Seifert G, Rehn L, Weber M, Steinhäuser C. AMPA receptor subunits expressed by single astrocytes in the juvenile mouse hippocampus. Brain Res Mol Brain Res (1997) 47:286-94. doi:10.1016/S0169-328X(97)00059-4
125. Seifert G, Weber M, Schramm J, Steinhäuser C. Changes in splice variant expression and subunit assembly of AMPA receptors during maturation of hippocampal astrocytes. Mol Cell Neurosci (2003) 22:248-58. doi:10.1016/S1044-7431(03)00039-3
126. Seifert G, Hüttmann K, Schramm J, Steinhäuser C. Enhanced relative expression of glutamate receptor 1 flip AMPA receptor subunits in hippocampal astrocytes of epilepsy patients with Ammon's horn sclerosis. J Neurosci (2004) 24:1996-2003. doi:10.1523/JNEUROSCI.3904-03.2004
127. Lambolez B, Audinat E, Bochet P, Crépel F, Rossier J. AMPA receptor subunits expressed by single Purkinje cells. Neuron (1992) 9:247-58. doi:10.1016/0896-6273(92)90164-9
128. Schousboe A. Development of potassium effects on ion concentrations and indicator spaces in rat brain-cortex slices during postnatal ontogenesis. Exp Brain Res (1972) 15:521-31. doi:10.1007/BF00236406
129. Sun W, McConnell E, Pare JF, Xu Q, Chen M, Peng W, et al. Glutamate-dependent neuroglial calcium signaling differs between young and adult brain. Science (2013) 339:197-200. doi:10.1126/science.1226740
130. Hertz L. The glutamate-glutamine (GABA) cycle: importance of late postnatal development and potential reciprocal interactions between biosynthesis and degradation. Front Endocrinol (Lausanne) (2013) 4:59. doi:10.3389/fendo.2013.00059
131. Guez-Barber D, Fanous S, Harvey BK, Zhang Y, Lehrmann E, Becker KG, et al. FACS purification of immunolabeled cell types from adult rat brain. J Neurosci Methods (2012) 203:10-8. doi:10.1016/j.jneumeth.2011.08.045
132. Zhuo L, Sun B, Zhang CL, Fine A, Chiu SY, Messing A. Live astrocytes visualized by green fluorescent protein in transgenic mice. Dev Biol (1997) 187:36-42. doi:10.1006/dbio.1997.8601
133. Fu H, Li B, Hertz L, Peng L. Contributions in astrocytes of SMIT1/2 and HMIT to myo-inositol uptake at different concentrations and pH. Neurochem Int (2012) 61:187-94. doi:10.1016/j.neuint.2012.04.010
134. Jungblut M, Tiveron MC, Barral S, Abrahamsen B, Knöbel S, Pennartz S, et al. Isolation and characterization of living primary astroglial cells using the new GLAST-specific monoclonal antibody ACSA-1. Glia (2012) 60:894-907. doi:10.1002/glia.22322
135. Heiman M, Schaefer A, Gong S, Peterson JD, Day M, Ramsey KE, et al. A translational profiling approach for the molecular characterization of CNS cell types. Cell (2008) 135:738-48. doi:10.1016/j.cell.2008.10.028
136. Ozsolak F, Milos PM. Single-molecule direct RNA sequencing without cDNA synthesis. Wiley Interdiscip Rev RNA (2011) 2:565-70. doi:10.1002/wrna.84
137. Thomsen R, Pallesen J, Daugaard TF, Børglum AD, Nielsen AL. Genome wide assessment of mRNA in astrocyte protrusions by direct RNA sequencing reveals mRNA localization for the intermediate filament protein nestin. Glia (2013) 61:1922-37. doi:10.1002/glia.22569
138. Booher J, Sensenbrenner M. Growth and cultivation of dissociated neurons and glial cells from embryonic chick, rat and human brain in flask cultures. Neurobiology (1972) 2:97-105.
139. Lange SC, Bak LK, Waagepetersen HS, Schousboe A, Norenberg MD. Primary cultures of astrocytes: their value in understanding astrocytes in health and disease. Neurochem Res (2012) 37:2569-88. doi:10.1007/s11064-012-0868-0
140. Hertz L, Peng L, Lai JC. Functional studies in cultured astrocytes. Methods (1998) 16:293-310. doi:10.1006/meth.1998.0686
141. Hertz L. Isotope-based quantitation of uptake, release, and metabolism of glutamate and glucose in cultured astrocytes. Methods Mol Biol (2012) 814:305-23. doi:10.1007/978-1-61779-452-0_20
142. Hertz L. Dibutyryl cyclic AMP treatment of astrocytes in primary cultures as a substitute for normal morphogenic and 'functiogenic' transmitter signals. Adv Exp Med Biol (1990) 265:227-43. doi:10.1007/978-1-4757-5876-4_22
143. Meier E, Hertz L, Schousboe A. Neurotransmitters as developmental signals. Neurochem Int (1991) 19:1-15. doi:10.1016/0197-0186(91)90113-R
144. Schubert P, Morino T, Miyazaki H, Ogata T, Nakamura Y, Marchini C, et al. Cascading glia reactions: a common pathomechanism and its differentiated control by cyclic nucleotide signaling. Ann N Y Acad Sci (2000) 903:24-33. doi:10.1111/j.1749-6632.2000.tb06346.x
145. Moonen G, Sensenbrenner M. Effects of dibutyryl cyclic AMP on cultured brain cells from chick embryos of different ages. Experientia (1976) 32:40-2. doi:10.1007/BF01932612
146. Lodin Z, Faltin J, Korínková P. The effect of dibutyryl cyclic AMP on cultivated glial cells from corpus callosum of 30-day-old rats. Physiol Bohemoslov (1979) 28:105-11.
147. Hertz L, Juurlink BHJ, Szuchet S. Cell cultures. In: Lajtha A editor. Handbook of Neurochemistry. Plenum Press (1985). p. 603-61.
148. Foote SL, Bloom FE, Aston-Jones G. Nucleus locus ceruleus: new evidence of anatomical and physiological specificity. Physiol Rev (1983) 63:844-914.
149. Sanders JD, Happe HK, Bylund DB, Murrin LC. Changes in postnatal norepinephrine alter alpha-2 adrenergic receptor development. Neuroscience (2011) 192:761-72. doi:10.1016/j.neuroscience.2011.06.045