Ballistic labeling and dynamic imaging of astrocytes in organotypic hippocampal slice cultures

Journal of Neuroscience Methods

Volumn 141, Issue 1, 2005, Pages 41-53

  Benediktsson, Adrienne M ^a   Schachtele, Scott J ^a   Green, Steven H ^a   Dailey, Michael E ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

Astrocyte; Biolistics; Calcium; Confocal microscopy; GFP; Morphology; Slice culture; Time lapse

Indexed keywords

CALCIUM; COMPLEMENTARY DNA; DYE; FLUORESCENT DYE; GLIAL FIBRILLARY ACIDIC PROTEIN; GOLD; GREEN FLUORESCENT PROTEIN; TUNGSTEN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL LABELING; CELL STRUCTURE; CONTROLLED STUDY; CYTOARCHITECTURE; GENE GUN; GENETIC TRANSFECTION; HIPPOCAMPUS; IMAGING; MORPHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; TISSUE CULTURE; TISSUE DISTRIBUTION;

ANIMALS; ANIMALS, NEWBORN; ASTROCYTES; BIOLISTICS; CALCIUM SIGNALING; CELL COMMUNICATION; CELL MEMBRANE; DNA, COMPLEMENTARY; FLUORESCENT DYES; GLIAL FIBRILLARY ACIDIC PROTEIN; GREEN FLUORESCENT PROTEINS; HIPPOCAMPUS; INDICATORS AND REAGENTS; MICROSCOPY, CONFOCAL; ORGAN CULTURE TECHNIQUES; RATS; STAINING AND LABELING;

EID: 10044242541     PISSN: 01650270     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jneumeth.2004.05.013     Document Type: Article

References (117)

1. Araque A., Carmignoto G., Haydon P.G. Dynamic signaling between astrocytes and neurons. Annu Rev Physiol. 63:2001;795-813
2. Araque A., Martin E.D., Perea G., Arellano J.I., Buño W. Synaptically released acetylcholine evokes Ca2+ elevations in astrocytes in hippocampal slices. J. Neurosci. 22(7):2002;2443-2450
3. Araque A., Parpura V., Sanzgiri R., Haydon P.G. Glutamate-dependent astrocyte modulation of synaptic transmission between cultured hippocampal neurons. Eur. J. Neurosci. 10:1998;2129-2142
4. Bergles D.E., Jahr C.E. Synaptic activation of glutamate transporters in hippocampal astrocytes. Neuron. 19:1997;1297-1308
5. Bergles D.E., Jahr C.E. Glial contribution to glutamate uptake at Schaffer collateral-commissural synapses in the hippocampus. J. Neurosci. 18:1998;7709-7716
6. Bezzi P., Carmignoto G., Pasti L., Vesce S., Rossi D., Lodi Rizzini B., et al. Prostaglandins stimulate calcium-dependent glutamate release in astrocytes. Nature. 391:1998;281-285
7. Bridgman P.C., Brown M.E., Balan I. Biolistic transfection. Methods Cell Biol. 71:2003;353-368
8. Bröer S., Brookes N. Transfer of glutamine between astrocytes and neurons. J Neurochem. 77:2001;705-719
9. Buchs P.A., Stoppini L., Muller D. Structural modifications associated with synaptic development in area CA1 of rat hippocampal organotypic cultures. Brain Res Dev Brain Res. 71(1):1993;81-91
10. Bushong E.A., Martone M.E., Ellisman M.H. Examination of the relationship between astrocyte morphology and laminar boundaries in the molecular layer of adult dentate gyrus. J Comp Neurol. 462:2003;241-251
11. Bushong E.A., Martone M.E., Jones Y.Z., Ellisman M.H. Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains. J. Neurosci. 22(1):2002;183-192
12. Butt A.M., Ransom B.R. Visualization of oligodendrocytes and astrocytes in the intact rat optic nerve by intracellular injection of lucifer yellow and horseradish peroxidase. GLIA. 2:1989;470-475
13. Butt A.M., Colquhoun K., Tutton M., Berry M. Three-dimensional morphology of astrocytes and oligodendrocytes in the intact mouse optic nerve. J Neurocytol. 23(8):1994;469-485
14. Carmignoto G, Pozzan T. Calcium oscillations as a signaling system that mediates the bi-directional communication between neurons and astrocytes. In: Volterra A, Magistretti PJ, Haydon PG, editors. The Tripartite Synapse: Glia in synaptic transmission. Great Britain: Oxford University Press; 2002. p. 151-163.
15. Catalani A., Sabbatini M., Consoli C., Cinque C., Tomassoni D., Azmitia E., et al. Glial fibrillary acidic protein immunoreactive astrocytes in developing rat hippocampus. Mech Age Devel. 123:2002;481-490
16. Chao TI, Rickmann M, Wolff JR. The synapse-astrocyte boundary: an anatomical basis for an integrative role of glia in synaptic transmission. In: Volterra A, Magistretti PJ, Haydon PG, editors. The Tripartite Synapse: Glia in synaptic transmission. Great Britain: Oxford University Press; 2002. p. 3-23.
17. Cornell-Bell A.H., Thomas P.G., Smith S.J. The excitatory neurotransmitter glutamate causes filopodia formation in cultured hippocampal astrocytes. GLIA. 3(5):1990;322-334
18. Dailey ME. Dynamic optical imaging of neuronal structure and physiology: confocal fluorescence microscopy in living brain slices. In: Toga A, Mazziotta J, editors. Brain Mapping: The Methods. San Diego: Academic Press; 1996. p. 29-54.
19. Dailey M.E., Buchanan J., Bergles D.E., Smith S.J. Mossy fiber growth and synaptogenesis in rat hippocampal slices in vitro. J. Neurosci. 14:1994;1060-1078
20. Dailey M.E., Smith S.J. The dynamics of dendritic structure in developing hippocampal slices. J. Neurosci. 16(9):1996;2983-2994
21. Danbolt N.C. Glutamate uptake. Prog Neurobiol. 65:2001;1-105
22. Dani J.W., Chernjavsky A., Smith S.J. Neuronal activity triggers calcium waves in hippocampal astrocyte networks. Neuron. 8:1992;429-440
23. Deitmer JW. pH Regulation. In: Kettenmann H, Ransom BR, editors. Neuroglia. Great Britain: Oxford University Press; 1995. p. 230-245.
24. Deitmer J.W., Schlue W.R. The regulation of intracellular pH by identified glial cells and neurons in the central nervous system of the leech. J Physiol. 388:1987;261-283
25. del Rio J.A., Heimrich B., Soriano E., Schwegler H., Frotscher M. Proliferation and differentiation of glial fibrillary acidic protein-immunoreactive glial cells in organotypic slice cultures of rat hippocampus. Neuroscience. 43(2/3):1991;335-347
26. Derouiche A., Frotscher M. Astroglial processes around identified glutamatergic synapses contain glutamine synthetase: evidence for transmitter degradation. Brain Res. 552:1991;346-350
27. Derouiche A., Heimrich B., Frotscher M. Loss of layer specific astrocytic glutamine synthetase immunoreactivity in slice cultures of hippocampus. Eur. J. Neurosci. 5(2):1993;122-127
28. Derouiche A., Frotscher M. Peripheral astrocyte processes: monitoring by selective immunostaining for the actin-binding ERM proteins. GLIA. 36:2001;330-341
29. Distler C., Dreher Z., Stone J. Contact spacing among astrocytes in the central nervous system: an hypothesis of their structural role. GLIA. 4:1991;484-494
30. Duan S.M., Anderson Cm., Stein B.A., Swanson R.A. Glutamate induces rapid upregulation of astrocyte glutamate transport and cell-surface expression of GLAST. J. Neurosci. 19(10):1999;193-200
31. Frotscher M., Zafirov S., Heimrich B. Development of identified neuronal types and of specific synaptic connections in slice cultures of rat hippocampus. Prog Neurobiol. 45:1995;143-164
32. Gähwiler B.H. Organotypic monolayer cultures of nervous tissue. J. Neurosci. Methods. 4(4):1981;329-342
33. Gähwiler B.H., Capogna M., Debanne D., McKinney R.A., Thompson S.M. Organotypic slice cultures: a technique has come of age. Trends Neurosci. 20:1997;471-477
34. Gan W.-B., Grutzendler J., Wong W.T., Wong R.O., Lichtman J.W. Multicolor "DiOlistic" labeling of the nervous system using lipophilic dye combinations. Neuron. 27:2000;219-225
35. Grosche J., Kettenmann H., Reichenbach A. Bergmann glial cells form distinct morphological structure to interact with cerebellar neurons. J. Neurosci. Res. 68(2):2002;138-149
36. Grosche J., Matyash V., Moller T., Verkhratsky A., Reichenbach A., Kettenmann H. Microdomains for neuron-glia interaction: parallel fiber signaling to Bergmann glial cells. Nat Neurosci. 2:1999;139-143
37. Güldner F.H., Wolff J.R. Multi-lamellar astroglial wrapping of neuronal elements in the hypothalamus of the rat. Experientia (Basel). 29:1973;1355-1356
38. Hailer N.P., Heppner F.L., Haas D., Nitsch R. Fluorescent dye prelabelled microglial cells migrate into organotypic hippocampal slice cultures and ramify. Eur. J. Neurosci. 9:1997;863-866
39. Hailer N.P., Jarhult J.D., Nitsch R. Resting microglial cells in vitro: analysis of morphology and adhesion molecule expression in organotypic hippocampal slice cultures. GLIA. 18:1996;319-331
40. Hama K., Arii T., Kosaka T. Three-dimensional organization of neuronal and glial processes: high voltage electron microscopy. Microsc Res Tech. 29:1994;357-367
41. Harris-White M.E., Zanotti S.A., Frautschy S.A., Charles A.C. Spiral intercellular calcium waves in hippocampal slice cultures. J Neurophysiol. 79(2):1998;1045-1052
42. Hatton G. Function-related plasticity in hypothalamus. Annu Rev Neurosci. 20:1997;375-397
43. Horner P.J., Palmer T.D. New roles for astrocytes: The nightlife of an 'astrocyte'. La vida loca! Trends Neurosci. 26(11):2003;597-603
44. + and pH homeostasis in the neonatal rat spinal cord. GLIA. 4:1991;56-63
45. Kang J., Jiang L., Goldman S.A., Nedergaard M. Astrocyte-mediated potentiation of inhibitory synaptic transmission. Nat Neurosci. 1(8):1998;683-692
46. Kettenmann H, Ransom BR, Neuroglia. New York: Oxford University Press Oxford; 1995.
47. Kettunen P., Demas J., Lohmann C., Kasthuri N., Gong Y., Wong R.O., et al. Imaging calcium dynamics in the nervous system by means of ballistic delivery of indicators. J. Neurosci. Methods. 119:2002;37-43
48. Kimelberg H.K., Schools G.P., Cai Z., Zhou M. Freshly isolated astrocyte (FIA) preparations: a useful single cell system for studying astrocyte properties. J. Neurosci. Res. 61:2000;577-587
49. Környei Z., Czirók A., Vicsek T., Madarász E. Proliferative and migratory responses of astrocytes to in vitro injury. J. Neurosci. Res. 61:2000;421-429
50. Kosaka T., Hama K. Three-dimensional structure of astrocytes in the rat dentate gyrus. J Comp Neurol. 249:1986;242-260
51. Kunkler P.E., Kraig R.P. Reactive astrocytosis from excitotoxic injury in hippocampal organotypic culture parallels that seen in vivo. J Cereb Blood Flow Metab. 17(1):1997;26-43
52. 2+ responses in glial cells evoked by exogenous and endogenous glutamate in rat hippocampus. Hippocampus. 11(2):2001;132-145
53. Lemkey-Johnston N., Larramendi L.M.H. Morphological characteristics of mouse stellate and basket cells and their neuroglial envelope: an electron microscopic study. J Comp Neurol. 134:1968;39-72
54. Lo D.C., McAllister A.K., Katz L.C. Neuronal transfection in brain slices using particle-mediated gene transfer. Neuron. 13:1994;1263-1268
55. Lohmann C., Myrh K., Wong R.O. Transmitter-evoked local calcium release stabilizes developing dendrites. Nature. 418:2002;177-181
56. Marrs G.S., Green S.H., Dailey M.E. Rapid formation and remodeling of postsynaptic densities in developing dendrites. Nature Neurosci. 4(10):2001;1006-1012
57. McAllister A.K. Biolistic transfection of neurons. Sci. STKE 2000; 26 september 2000; (51): PL1.
58. Miyaguchi K., Maeda Y., Collin C., Sihag R. Gene transfer into hippocampal slice cultures with an adenovirus vector driven by cytomegalovirus promoter: stable co-expression of green fluorescent protein and lacZ genes. Brain Res Bull. 51(3):2000;195-202
59. Murphy R.C., Messer A. Gene transfer methods for CNS organotypic cultures: A comparison of three nonviral methods. Mol. Ther. 3(1):2001;113-121
60. Nägler K., Mauch D.H., Pfrieger F.W. Glia-derived signals induce synapse formation in neurons of the rat central nervous system. J. Physiol. 533(3):2001;665-679
61. Nedergaard M., Ransom B., Goldman S.A. New roles for astrocytes: redefining the functional architecture of the brain. Trends Neurosci. 26(10):2003;523-530
62. Nedergaard M., Takano T., Hansen A.J. Beyond the role of glutamate as neurotransmitter. Nat Rev Neurosci. 3(9):2002;748-755
63. Nett W.J., Oloff S.H., McCarthy K.D. Hippocampal astrocytes in situ exhibit calcium oscillations that occur independent of neuronal activity. J Neurophysiol. 87:2002;528-537
64. Newman EA. Glial cell regulation of extracellular potassium. In: Kettenmann H, Ransom BR, editors. Neuroglia. New York: Oxford University Press Oxford; 1995. p. 717-731.
65. Newman E.A. New roles for astrocytes: regulation of synaptic transmission. Trends Neurosci. 26(10):2003;536-542
66. Nolte C., Matyash M., Pivneva T., Schipke C.G., Ohlemeyer C., Hanisch U.-K, et al. GFAP promoter-controlled GFP-expressing transgenic mice: A tool to visualize astrocyte and astrogliosis in living brain tissue. GLIA. 33:2001;72-86
67. Norenberg M., Martinez-Hernandez A. Fine structural localization of glutamine synthetase in astrocytes of rat brain. Brain Res. 161:1979;303-310
68. Ogata K., Kosaka T. Structural and quantitative analysis of astrocytes in the mouse hippocampus. Neuroscience. 113(1):2002;221-233
69. Oliet S. Functional consequences of morphological neuroglial changes in the magnocellular nuclei of the hypothalamus. J Neuroendocrinol. 14:2002;241-246
70. Parpura V., Haydon P.G. Physiological astrocytic calcium levels stimulate glutamate release to modulate adjacent neurons. Proc Natl Acad Sci. 97(15):2000;8629-8634
71. 2+ oscillations in situ drive NMDAR-mediated neuronal excitation. Nat Neurosci. 4(8):2001;803-812
72. Pasti L., Volterra A., Pozzan T., Carmignoto G. Intracellular calcium oscillations in astrocytes: a highly plastic, bidirectional form of communication between neurons and astrocytes in situ. J. Neurosci. 17(20):1997;7817-7830
73. Pellerin L., Pellegri G., Bittar P.G., Charnay Y., Bouras C., Martin J.L., et al. Evidence supporting the existence of an activity dependent astrocyte neuron lactate shuttle. Dev Neurosci. 20:1998;291-299
74. Penfield W. Neuroglia: normal and pathological. In: Penfield W, editor. Cytology and Cellular Pathology of the Nervous System. vol 2. New York: P.B. Hoeber Inc.; 1932. p. 423-79.
75. Perez Velazquez J.L., Frantseva M., Naus C.C.G., Bechberger J.F., Juneja S.C., Velumaian A., et al. Development of astrocytes and neurons in cultured brain slices from mice lacking connexin43. Dev Brain Res. 97:1996;293-296
76. Pfrieger F., Barres B.A. Synaptic efficacy enhanced by glial cells in vitro. Science. 277(5332):1997;1684-1687
77. Poritsky R. Two and three dimensional ultrastructure of boutons and glial cells on the motoneuronal surface in the cat spinal cord. J Comp Neurol. 135:1969;423-452
78. i. GLIA. 13:1995;101-112
79. Powell E.M., Meiners S., DiProspero N.A., Geller H.M. Mechanisms of astrocyte-directed neurite guidance. Cell Tissue Res. 290:1997;385-393
80. Pozzo Miller L.D., Landis D.M. Cytoplasmic structure in organotypic cultures of rat hippocampus prepared by rapid freezing and freeze-substitution fixation. Synapse. 13(3):1993;195-205
81. Privat A, Gimenez-Ribott M, Ridet J-L. Morphology of astrocytes. In: Kettenmann H, Ransom BR, editors. Neuroglia. New York: Oxford University Press Oxford; 1995. p. 3-22.
82. Qin L., Marrs G.S., McKim R., Dailey M.E. Hippocampal mossy fibers induce assembly and clustering of PSD95-containing postsynaptic densities independent of glutamate receptor activation. J Comp Neurol. 440:2001;284-298
83. Ramón y Cajal S, Histologie du Système Nerveux de l'Homme et des Vertébrés. A., Maloine: Paris, 1909. p. 230-252.
84. Ransom B., Behar T., Nedergaard M. New roles for astrocytes (stars at last). Trends Neurosci. 26(10):2003;520-522
85. Ridet J.L., Malhotra S.K., Privat A., Gage F.H. Reactive astrocytes: cellular and molecular cues to biological function. TINS. 20:1997;570-577
86. 2 stimulates receptor-dependent astrocyte neuromodulation in cultured hippocampal cells. J Neurobiol. 41(2):1999;221-229
87. Sasaki H., Sato F., Mannen H. Morphological analysis of single astrocytes of the adult cat central nervous system visualized by HRP microinjection. Brain Res. 501:1989;339-354
88. Scheffler B., Schmandt T., Schröder W., Steinfarz B., Husseini L., Wellmer J., et al. Functional network integration of embryonic stem cell-derived astrocytes in hippocampal slice cultures. Development. 130:2003;5533-5541
89. 2+ waves trigger responses in microglial cells in brain slices. FASEB J. 16:2002;255-257
90. Sepp K.J., Auld V.J. Reciprocal interactions between neurons and glia are required for Drosophila peripheral nervous system development. J. Neurosci. 23(23):2003;8221-8230
91. Shao Y., McCarthy K.D. Plasticity of astrocytes. GLIA. 11:1994;147-155
92. Shelton M.K., McCarthy K.D. Mature hippocampal astrocytes exhibit functional metabotropic and ionotropic glutamate receptors in situ. GLIA. 26:1999;1-11
93. Slezak M., Pfrieger F.W. New roles for astrocytes: regulation of CNS synaptogenesis. Trends Neurosci. 26(10):2003;531-535
94. Song H., Stevens C.F., Gage F.H. Astroglia induce neurogenesis from adult neural stem cells. Nature. 417:2002;39-44
95. Spacek J. Three-dimensional analysis of dendritic spines. III. Glial sheets. Anat Embryol. 171:1985;245-252
96. Stoppini L., Buchs P.-A., Muller D. A simple method for organotypic cultures of nervous tissue. J. Neurosci. Methods. 27:1991;173-182
97. Sul J.-Y. Orosz, Givens R.S., Haydon P.G. Astrocytic connectivity in the hippocampus. Neuron Glial Biol. 1:2004;3-11
98. Suzuki R., Watanabe J., Arata S., Funahashi H., Kikuyama S., Shioda S. A transgenic mouse model for the detailed morphological study of astrocytes. Neurosci Res. 47:2003;451-454
99. Theodosis D., Bonhomme R., Vitiello S., Rougon G., Poulain D. Cell surface expression of polysialic acid on NCAM is a prerequisite for activity-dependent morphological neuronal and glial plasticity. J. Neurosci. 19(23):1999;10228-10236
100. Theodosis D.T., Poulain D.A. Activity-dependent neuronal-glial and synaptic plasticity in the adult mammalian hypothalamus. Neuroscience. 57:1993;501-535
101. Tsacopoulos M. Metabolic signaling between neurons and glial cells: a short review. J Physiol Paris. 96(3-4):2002;283-288
102. Tsacopoulos M., Magistretti P.J. Metabolic coupling between glia and neurons. J. Neurosci. 16:1996;877-885
103. Tsacopoulos M., Veuthey A.L., Saravelos G., Perrottet P., Tsoupras G. Glial cells transform glucose to alanine which fuels the neurons in the honeybee retina. J. Neurosci. 14:1994;1339-1351
104. + currents in acutely isolated hippocampal astrocytes. J. Neurosci. 12:1992;1781-1788
105. Ullian E.M., Sapperstein S.K., Christopherson K.S., Barres B.A. Control of synapse number by glia. Science. 291:2001;657-660
106. Ventura R., Harris K.M. Three-dimensional relationships between hippocampal synapses and astrocytes. J. Neurosci. 19(16):1999;6897-6906
107. Verkhratsky A., Orkand R.K., Kettenmann H. Glial calcium: homeostasis and signaling function. Physiol Rev. 78(1):1998;99-141
108. Volterra A, Magistretti PJ, Haydon PG. The tripartite synapse: glia in synaptic transmission. Great Britain: Oxford University Press; 2002.
109. Wang Z., Tymianski M., Jones O.T., Nedergaard M. Impact of cytoplasmic calcium buffering on the spatial and temporal characteristics of intercellular calcium signals in astrocytes. J. Neurosci. 17(19):1997;7359-7371
110. Wellman H., Kaltschmidt B., Kaltschmidt C. Optimized protocol for biolistic transfection of brain slices and dissociated cultured neurons with a hand-held gene gun. J. Neurosci. Methods. 92:1999;55-64
111. Willmott N.J., Wong K., Strong A.J. Intercellular Ca(2+) waves in rat hippocampal slice and dissociated glial-neuron cultures mediated by nitric oxide. FEBS Lett. 487(2):2000a;239-247
112. Willmott N.J., Wong K., Strong A.J. A fundamental role for the nitric oxide-G-kinase signaling pathway in mediating intercellular Ca(2+) waves in glia. J. Neurosci. 20(5):2000b;1767-1779
113. Won C.-K., Oh Y. cAMP-induced stellation in primary astrocyte cultures with regional heterogeneity. Brain Res. 887:2000;250-258
114. Wu V.W., Schwartz J.P. Cell culture models for reactive gliosis: new perspectives. J. Neurosci. Res. 51:1998;675-681
115. Zhou L., Sun B., Zhang C.-L., Fine A., Chiu S.-Y., Messing A. Live astrocytes visualized by green fluorescent protein in transgenic mice. Dev Biol. 187:1997;36-42
116. Zlatkine P., Mehul B., Magee A.I. Retargeting of cytosolic proteins to the plasma membrane by the Lck protein tyrosine kinase dual acylation motif. J Cell Sci. 110:1997;673-679
117. Zonta M., Angulo M.C., Gobbo S., Rosengarten B., Hossmann K.-A., Possan T., et al. Neuron-to-astrocyte signaling is central to the dynamic control of brain microcirculation. Nat Neurosci. 6(1):2003;43-50