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Organotypic slice culture of the mammalian retina

Published online by Cambridge University Press:  02 June 2009

Andreas Feigenspan
Affiliation:
Max-Planck Institut für Hirnforschung, Neuroanatomische Abteilung, Deutschordenstrasse 46, W 6000 Frankfurt, Germany.
Joachim Bormann
Affiliation:
Max-Planck Institut für Hirnforschung, Neuroanatomische Abteilung, Deutschordenstrasse 46, W 6000 Frankfurt, Germany.
Heinz Wässle
Affiliation:
Max-Planck Institut für Hirnforschung, Neuroanatomische Abteilung, Deutschordenstrasse 46, W 6000 Frankfurt, Germany.

Abstract

Vertical slices of 6-day postnatal (P6) rat retina were cut at a thickness of 100 μm and cultured using the roller-tube technique. After 14–21 days in vitro there was significant distortion of normal retinal architecture, but localized areas of the slices showed the typical pattern of layering of mature retina. The following immunocytochemical markers were used to characterize the different retinal cell types: antibodies against protein kinase C (PKC), calcium binding protein (CabP 28kD), neurofilaments (NF), glia-specific antibodies (GFAP, vimentin), and transmitter-specific antibodies (GABA, TH). The expression of these markers was compared in P6 retina, adult retina, and slice culture. To further characterize the cultured cells, patch-clamp recordings were performed in combination with intracellular injection of Lucifer Yellow (LY). Transmitter-and voltage-gated membrane currents were recorded from morphologically identified neurons. The experiments show that a mammalian slice culture can be used to study differentiation and function of retinal cell types.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1993

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References

Adler, R. (1987). The differentiation of retinal photoreceptors and neurons in vitro. Progress in Retinal Research 6, 127.Google Scholar
Akagawa, K. (1990). Presence of light-responding neurons in the re-aggregate cultures of rat retinae. Developmental Brain Research 57, 143145.Google Scholar
Akagawa, K. & Barnstable, C.J. (1986). Identification and characterization of cell types in monolayer cultures of rat retina using monoclonal antibodies. Brain Research 383, 110120.CrossRefGoogle ScholarPubMed
Aramant, R., Seiler, M., Emnger, B., Bergstrom, A., Adolph, A.R. & Turner, J.E. (1990). Neuronal markers in rat retinal grafts. Developmental Brain Research 53, 4761.Google Scholar
Bähr, W. & Eschweiler, G.W. (1991). Regenerating adult rat retinal axons reconnect with target neurons in vitro. Neuro Report 2, 581584.Google Scholar
Barnes, S. & Werblin, F. (1986). Gated currents generate single spike activity in amacrine cells of the tiger salamander. Proceedings of the National Academy of Sciences of the U.S.A. 83, 15091512.CrossRefGoogle ScholarPubMed
Barnstable, C.J. (1987). A molecular view of vertebrate retinal development. Molecular Neurobiology 1, 946.Google Scholar
Barnstable, C.J. & Dräger, U.C. (1984). THY-1 antigen: A ganglion cell specific marker in rodent retina. Neuroscience 11, 847855.CrossRefGoogle ScholarPubMed
Barres, B.A., Silverstein, B.E., Corey, D.P. & Chun, L.L.Y. (1988). Immunological, morphological, and electrophysiological variation among retinal ganglion cells purified by panning. Neuron 1, 791803.CrossRefGoogle ScholarPubMed
Berrebi, A.S., Oberdick, J., Sangameswaran, L., Christiakos, S., Morgan, J.I. & Mugnaini, E. (1991). Cerebellar Purkinje cell markers are expressed in retinal bipolar neurons. Journal of Comparative Neurology 308, 630649.Google Scholar
Bolz, J., Novak, N., Götz, M. & Bonhoeffer, T. (1990). Formation of target-specific neuronal projections in organotypic slice cultures from rat visual cortex. Nature 346, 359362.Google Scholar
Bonhoeffer, F. & Huf, J. (1985). Position-dependent properties of retinal axons and their growth cones. Nature 315, 409410.Google Scholar
Bormann, J. (1988). Electrophysiology of GABAA and GABAB receptors. Trends in Neurosciences 11, 112116.CrossRefGoogle Scholar
Bormann, J. (1992). U-tube drug application. In Electrophysiological Methods for In Vitro Studies in Vertebrate Neurobiology, ed. Kettenmann, H. & Grantyn, R.New York: Wiley.Google Scholar
Bormann, J., Hamill, O.P. & Sakmann, B. (1987). Mechanism of anion permeation through channels gated by glycine and γ-aminobu-tyric acid in mouse cultured spinal neurones. Journal of Physiology (London) 385, 243286.CrossRefGoogle ScholarPubMed
Braekevelt, C.R. & Hollenberg, M.J. (1970). The development of the retina of the albino rat. American Journal of Anatomy 111, 281302.Google Scholar
Caffé, A.R., Visser, H., Jansen, H.B. & Sanyal, S. (1989). Histotypic differentiation of neonatal mouse retina in organ culture. Current Eye Research 8, 10831092.Google Scholar
Celio, M.R. & Heizmann, C.W. (1981). Calcium-binding protein parv-albumin as a neuronal marker. Nature 293, 300302.Google Scholar
Christiakos, S., Rhoten, W.B. & Feldman, S.C. (1987). Rat calbindin-D28K purification, quantitation, immunocytochemical localization and comparative aspects. Methods in Enzymology 139, 534551.Google Scholar
Cutting, G.R., Lu, L., O’Hara, B.F., Kasch, L.M., Montrose-Rafizadeh, C., Donovan, D.M., Shimada, S., Antonarakis, S.E., Guggino, W.B., Uhl, G.R. & Kazazian, H.H. Jr., (1991). Cloning of the γ-aminobutyric acid (GABA) ρ 1 cDNA: A GABA receptor subunit highly expressed in the retina. Proceedings of the National Academy of Sciences of the U.S.A. 81, 26732677.CrossRefGoogle Scholar
Debus, E., Weber, K. & Oxborn, M. (1983). Monoclonal antibodies specific to glial fibrillary acidic (GFA) protein and for each of the neurofilament triplet polypeptides. Differentiation 25, 193203.CrossRefGoogle ScholarPubMed
DelCerro, M., Ison, J.R., Bowen, G.P., Lazar, E. & Cerro, C.Del (1991). Intraretinal grafting restores visual function in light-blinded rats. Neuro Report 2, 529532.Google Scholar
Dixon, R.G. & Eng, L.F. (1981). Glial fibrillary acidic protein in the retina of the developing albino rat: An immunoperoxidase study of paraffin-embedded tissue. Journal of Comparative Neurology 195, 305321.CrossRefGoogle Scholar
Dowling, J.E. & Boycott, B.B. (1966). Organization of the primate retina: electron microscopy. Proceedings of the Royal Society B (London) 166, 80111.Google ScholarPubMed
DräGer, U.C. (1983). Coexistence of neurofilaments and vimentin in a neuron of the adult mouse retina. Nature 303, 169172.CrossRefGoogle Scholar
DräGer, U.C, Edwards, D.L. & Barnstable, C.J. (1984). Antibodies against filamentous components in discrete cell types of the mouse retina. Journal of Neuroscience 4, 20252042.Google Scholar
Edwards, F.A., Konnerth, A., Sakmann, B. & Takahashi, T. (1989). A thin slice preparation for patch clamp recordings from neurones of the mammalian central nervous system. Pflügers Archives 414, 600612.CrossRefGoogle ScholarPubMed
Eisenfeld, A., Bunt-Milam, A.H. & Sarthy, P.V. (1984). Müller cell expression of glial fibrillary acidic protein after genetic and experimental photoreceptor degeneration in the rat retina. Investigative Ophthalmology and Visual Science 25, 13211328.Google Scholar
Fenwick, E.M., Marthy, A. & Neher, E. (1982). A patch-clamp study of bovine chromaffin cells and their sensitivity to acetylcholine. Journal of Physiology (London) 331, 577597.Google Scholar
Fry, K.R., Tavella, D., Su, Y.Y.T., Peng, Y.W., Watt, C.B. & Lam, D.M.K. (1985). A monoclonal antibody specific for retinal ganglion cells of mammals. Brain Research 338, 360365.Google Scholar
Gähwiler, B.H. (1981 a). Morphological differentiation of nerve cells in thin organotypic cultures derived from rat hippocampus and cerebellum. Proceedings of the Royal Society B (London) 211, 287290.Google Scholar
Gähwiler, B.H. (1981 b). Organotypic monolayer cultures of nervous tissue. Journal of Neuroscience Methods 4, 329342.Google Scholar
Gähwtler, B.H. (1984). Development of the hippocampus in vitro: Cell types, synapses and receptors. Neuroscience 11, 751760.CrossRefGoogle Scholar
Gahwiler, B.H., Thompson, S.M., Audinat, E. & Robertson, R.T. (1991). Organotypic slice cultures of neural tissue. In Culturing Nerve Cells, ed. Banker, G. & Kimberly, G., pp. 379411. Cambridge, Massachusetts: MIT Press.Google Scholar
Greferath, U., GrüNert, U. & Wässle, H. (1990). Rod bipolar cells in the mammalian retina show protein kinase C-like immunoreactivity. Journal of Comparative Neurology 301, 433442.Google Scholar
GrüNert, U. & Martin, P.R. (1991). Rod bipolar cells in the macaque monkey retina: Immunoreactivity and connectivity. Journal of Neuroscience 11, 27422758.Google Scholar
Halfter, W. & Deiss, S. (1984). Axon growth in embryonic chick and quail retinal whole mounts in vitro. Developmental Biology 102, 344355.CrossRefGoogle ScholarPubMed
Hamill, O.P., Marthy, A., Neher, E., Sakmann, B. & Sigworth, F.J. (1981). Improved patch-clamp techniques for high resolution current recording from cells and cell-free membrane patches. Pflügers Archives 391, 85100.CrossRefGoogle ScholarPubMed
Hansson, H.A. & Sourander, P. (1964). Studies on cultures of mammalian retina. Zeitschrift für Zellforschung 62, 2647.Google Scholar
Harrison, R.G. (1912). The cultivation of tissues in extraneous media as a method of morphogenic study. Anatomical Record 6, 181193.Google Scholar
Hicks, D. & Barnstable, C.J. (1987). Different rhodopsin monoclonal antibodies reveal different binding patterns on developing and adult rat retina. Journal of Histochemistry and Cytochemistry 35, 13171328.Google Scholar
Hicks, D. & Courtois, Y. (1990). The growth and behaviour of rat retinal Müller cells in vitro, 1: An improved method for isolation and culture. Experimental Eye Research 51, 119129.Google Scholar
Hild, W. & Callas, G. (1967). The behavior of retinal tissue in vitro, light and electron microscopic observations. Zeitschrift für Zellforschung 80, 121.CrossRefGoogle ScholarPubMed
Hofmann, H.D. (1988). Development of cholinergic retinal neurons from embryonic chicken in monolayer cultures: Stimulation by glial cell-derived factors. Journal of Neuroscience 8, 13611369.Google Scholar
Kaneko, A., Pinto, L.H. & Tachibana, M. (1989). Transient calcium current of retinal bipolar cells of the mouse. Journal of Physiology (London) 410, 613629.Google Scholar
Karschin, A. & Wässle, H. (1990). Voltage- and transmitter-gated currents in isolated rod bipolar cells of the rat retina. Journal of Neurophysiology 63, 860876.CrossRefGoogle ScholarPubMed
Knöpfel, T., Vranesic, I., Gähwiler, B.H. & Brown, D.A. (1990). Muscarinic and β-adrenergic depression of the slow Ca2+-activated potassium conductance in hippocampal CA3 pyramidal cells is not mediated by a reduction of depolarization-induced cytosolic Ca2+ transients. Proceedings of the National Academy of Sciences of the U.S.A. 87, 40834097.Google Scholar
Kolb, H., Cuenca, N. & Dekorver, L. (1991). Postembedding immunocytochemistry for GABA and glycine reveals the synaptic relationships of the dopaminergic amacrine cell of the cat retina. Journal of Neurology 310, 267284.Google Scholar
Vail, M.M.La & Hild, W. (1971). Histotypic organization of the rat retina in vitro. Zeitschrift für Zellforschung 114, 557579.Google ScholarPubMed
Leifer, D., Lipton, S.A., Barnstable, C.J. & Masland, R.H. (1984). Monoclonal antibody to Thy-1 enhances regeneration of processes by rat retinal ganglion cells in culture. Science 224, 303306.Google Scholar
Llano, I., Marty, A., Johnson, J.W., Ascher, P. & Gähwiler, B.H. (1988). Patch-clamping of amino acid-activated responses in “organotypic” slice cultures. Proceedings of the National Academy of Sciences of the U.S.A. 85, 32213225.Google Scholar
Mack, A.F. & Fernald, R.D. (1991). Thin slices of teleost retina continue to grow in culture. Journal of Neuroscience Methods 36, 195202.Google Scholar
MacLeish, P.R., Barnstable, C.J. & Townes-Anderson, E. (1983). Use of monoclonal antibody as a substrate for mature neurons in vitro. Proceedings of the National Academy of Sciences of the U.S.A. 80, 70147018.CrossRefGoogle ScholarPubMed
MacLeish, P.R. & Townes-Anderson, E. (1988). Growth and synapse formation among major classes of adult salamander retinal neurons in vitro. Neuron 1, 751760.CrossRefGoogle ScholarPubMed
Massey, S.C. & Redburn, D.A. (1987). Transmitter circuits in the vertebrate retina. Progress in Neurobiology 28, 5596.Google Scholar
McLoon, L.K., Lund, R.D. & McLoon, S.C. (1982). Transplantation of reaggregates of embryonic neural retina to neonatal rat brain: Differentiation and formation of connections. Journal of Comparative Neurology 205, 179189.CrossRefGoogle ScholarPubMed
McLoon, L.K., McLoon, S.C. & Lund, R.D. (1981). Cultured embryonic retinae transplanted to rat brain: Differentiation and formation of connections. Brain Research 226, 1531.CrossRefGoogle Scholar
Meyer, H. (1936). Züchtung der Retina des Huhnes in vitro. Zeitschrift f¨r mikroskopische und anatomische Forschung 33, 151160.Google Scholar
Mitrofanis, J., Maslim, J. & Stone, J. (1988). Catecholaminergic and cholinergic neurons in the developing retina of the rat. Journal of Comparative Neurology 276, 343359.Google Scholar
Molday, R.S., Molday, L.L., Dose, A., Clark-Lewis, I., Illing, M., Cook, N.J., Eismann, E. & Kaupp, U.B. (1991). The cGMP-gated channel of the rod photoreceptor cell characterization and orientation of the amino terminus. Journal of Biological Chemistry 266, 2191721922.Google Scholar
Mori, K., Fujita, S.C., Imamura, K. & Obata, K. (1985). Immunohistochemical study of subclasses of olfactory nerve fibers and their projection to the olfactory bulb in the rabbit. Journal of Comparative Neurology 242, 214229.Google Scholar
Moscona, A.A. (1965). Recombination of dissociated cells and the development of cell aggregates. In The Biology of Cells and Tissues in Culture, ed. Willmer, E.M., pp. 489529. New York: Academic Press.CrossRefGoogle Scholar
Nawy, S. & Jahr, C.E. (1990). Suppression by glutamate of cGMP-activated conductance in retinal bipolar cells. Nature 346, 269271.Google Scholar
Negishi, K., Kato, S. & Teranishi, T. (1988). Dopamine cells and rod bipolar cells contain protein kinase C-like immunoreactivity in some vertebrate retinas. Neuroscience Letters 94, 247252.CrossRefGoogle ScholarPubMed
Nguyen-Legros, J. (1988). Morphology and distribution of catecholamine-neurons in mammalian retina. Progress in Retinal Research 7, 113147.CrossRefGoogle Scholar
Nguyen-Legros, J., Vigny, A. & Gay, M. (1983). Post-natal development of TH-like immunoreactivity in the rat retina. Experimental Eye Research 37, 2332.CrossRefGoogle ScholarPubMed
Nishizuka, Y. (1988). The molecular heterogeneity of protein kinase C and its implications for cellular regulation. Nature 334, 661665.Google Scholar
Noble, M., Bok-Seang, J. & Cohen, J. (1984). Glia are a unique substrate for the in vitro growth of central nervous neurons. Journal of Neuroscience 4, 18921903.Google Scholar
Oberdick, J., Smeyne, R.J., Mann, J.R., Zackson, S. & Morgan, J.I. (1990). A promoter that drives transgene expression in cerebellar Purkinje and retinal bipolar neurons. Science 248, 223226.CrossRefGoogle ScholarPubMed
Onoda, N. (1988). A monoclonal antibody specific for a subpopulation of retinal bipolar cells in vertebrates. Neuroscience Research 8, 113115.Google ScholarPubMed
Onoda, N. & Fujita, S.C. (1987). A monoclonal antibody specific for a subpopulation of retinal bipolar cells in the frog and other vertebrates. Brain Research 416, 359363.CrossRefGoogle ScholarPubMed
Osborn, M., Debus, E. & Weber, K. (1984). Monoclonal antibodies specific to vimentin. European Journal of Cell Biology 34, 137143.Google Scholar
Pasteels, B., Rogers, J., Blachier, F. & Pochet, R. (1990). Calbindin and calretinin localization in retina from different species. Visual Neuroscience 5, 116.Google Scholar
Pourcho, R.G. (1982). Dopaminergic amacrine cells in the cat retina. Brain Research 252, 101109.Google Scholar
Rabié, A., Thomasset, M., Parkes, C.o. & Clavel, M.C. (1985). Immunocytochemical detection of 28000-MW calcium-binding protein in horizontal cells of the rat retina. Cell and Tissue Research 240, 493496.Google Scholar
Reh, T.A. & Kljavin, I.J. (1989). Age of differentiation determines rat retinal germinal cell phenotype: Induction of differentiation by dissociation. Journal of Neuroscience 9, 41794189.Google Scholar
Reichenbach, A., Schnitzer, J., Friedrich, A., Knothe, A.K. & Henke, A. (1991). Development of the rabbit retina: II. Müller cells. Journal of Comparative Neurology 311, 3344.Google Scholar
Röhrenbeck, J., Wässle, H. & Heizmann, C.W. (1987). Immunocytochemical labelling of horizontal cells in mammalian retina using antibodies against calcium-binding proteins. Neuroscience Letters 77, 255260.Google Scholar
Röhrenbeck, J., Wässle, H. & Boycott, B.B. (1989). Horizontal cells in the monkey retina: Immunocytochemical staining with antibodies against calcium-binding proteins. European Journal of Neuroscience 1, 407420.CrossRefGoogle ScholarPubMed
Rohrer, H., Acheson, A.L., Thibault, J. & Thoenen, H. (1986). Developmental potential of quail dorsal root ganglion cells analyzed in vitro and in vivo. Journal of Neuroscience 6, 26162624.CrossRefGoogle ScholarPubMed
Sanna, P.P., Keyser, K.T., Battenberg, E. & Bloom, F.E. (1990). Parvalbumin immunoreactivity in the rat retina. Neuroscience Letters 118, 136139.Google Scholar
Sarthy, P.V. (1985). Establishment of Müller cell cultures from adult rat retina. Brain Research 337, 138141.Google Scholar
Sarthy, P.V. (1987). Retinal neurons: their separation and characterization. Progress in Retinal Research 6, 4567.Google Scholar
Sarthy, P.V. & Lam, D.M.K. (1979). Isolated cells from a mammalian retina. Brain Research 176, 208212.Google Scholar
Schnitzer, J. (1988). Astrocytes in the guinea pig, horse, and monkey retina: Their occurrence coincides with the presence of blood vessels. Glia 1, 7489.Google Scholar
Schnitzer, J. (1989). Enzyme-histochemical demonstration of microglial cells in the adult and postnatal rabbit retina. Journal of Comparative Neurology 282, 249263.Google Scholar
Seiler, M., Aramant, R., Ehinger, B., Bergström, A. & Adolph, A.R. (1991). Characteristics of embryonic retina transplanted to rat and rabbit retina. Neuro-Ophthalmology 11, 263279.Google Scholar
Shaw, G. & Weber, K. (1983). The structure and development of the rat retina: An immunofluorescence microscopical study using antibodies specific for intermediate filament proteins. European Journal of Cell Biology 30, 219232.Google Scholar
Shaw, G. & Weber, K. (1984). The intermediate filament complement of the retina: a comparison between different mammalian species. European Journal of Cell Biology 33, 95104.Google Scholar
Shiells, R.A. & Falck, G. (1990). Glutamate receptors of rod bipolar cells are linked to a cyclic GMP cascade via a G-protein. Proceedings of the Royal Society B (London) 242, 9194.Google Scholar
Sparrow, J.R., Hicks, D. & Barnstable, C.J. (1990). Cell commitment and differentiation in explants of embryonic rat neural retina. Comparison with the developmental potential of dissociated retina. Developmental Brain Research 51, 6984.Google Scholar
Stichel, C.C., Kägi, U. & Heizmann, C.W. (1986). Parvalbumin in cat brain: Isolation, characterization, and localization. Journal ofNeurochemistry 47, 4653.Google Scholar
Suzuki, S., Tachibana, M. & Kaneko, A. (1990). Effects of glycine and GABA on isolated bipolar cells of the mouse retina. Journal of Physiology (London) 421, 645662.Google Scholar
Tansley, K. (1933). The formation of rosettes in the rat retina. British Journal of Ophthalmology 17, 321336.Google Scholar
Tauchi, M. & Masland, R.H. (1984). The shape and arrangement of the cholinergic neurons in the rabbit retina. Proceedings of the Royal Society B (London) 223, 101119.Google Scholar
Townes-Anderson, E., MacLeish, P.R. & Raviola, E. (1985). Rod cells dissociated from mature salamander retina: Ultrastructure and uptake of horseradish peroxidase. Journal of Cell Biology 100, 175188.Google Scholar
Turner, D.L. & Cepko, C.L. (1987). A common progenitor for neurons and glia persists in rat retina late in development. Nature 328, 131136.Google Scholar
Turner, D.L., Synder, E.Y. & Cepko, C.L. (1990). Lineage-independent determination of cell type in the embryonic mouse retina. Neuron 4, 833845.Google Scholar
Vaney, D.I. (1990). The mosaic of amacrine cells in the mammalian retina. Progress in Retinal Research 9, 49100.CrossRefGoogle Scholar
Voigt, T. & Wässle, H. (1987). Dopaminergic innervation of An amacrine cells in mammalian retina. Journal of Neuroscience 7, 41154128.Google Scholar
Vollmer, G. & Layer, P.G. (1986 a). An in vitro model of proliferation and differentiation of the chick retina: Coaggregates of retinal and pigment epithelial cells. Journal of Neuroscience 6, 18851896.Google Scholar
Vollmer, G. & Layer, P.G. (1986 b). Reaggregation of chick retinal and mixtures of retinal and pigment epithelium cells: The degree of laminar organization is dependent on age. Neuroscience Letters 63, 9195.Google Scholar
Wässle, H. & Boycott, B.B. (1991). Functional architecture of the mammalian retina. Physiological Review 71, 447480.Google Scholar
Wässle, H. & Chun, M.H. (1988). Dopaminergic and indoleamine-accumulating amacrine cells express GABA-like immunoreactivity in the cat retina. Journal of Neuroscience 8, 33833394.Google Scholar
Wässle, H. & Chun, M.H. (1989). GABA-like immunoreactivity in the cat retina: Light microscopy. Journal of Comparative Neurology 279, 4354.Google Scholar
Wässle, H., Yamashita, M., Greferath, U., Grünert, U. & Müller, F. (1991). The rod bipolar cell of the mammalian retina. Visual Neuroscience 7, 99112.CrossRefGoogle ScholarPubMed
Weidman, T.A. & Kuwabara, T. (1968). Postnatal development of the rat retina. Archives of Ophthalmology 79, 470484.Google Scholar
Willams, A.F. & Gagnon, J. (1982). Neuronal cell Thy-1 glycoprotein: Homology with immunoglobulin. Science 216, 696703.Google Scholar
Yamashita, M. & Wässle, H. (1991). Responses of rod bipolar cells isolated from the rat retina to the glutamate against 2-amino-4-phosphonobutyric acid (APB). Journal of Neuroscience 11, 23722382.Google Scholar
Young, H.M. & Vaney, D.I. (1991). Rod-signal interneurons in the rabbit retina: 1. rod bipolar cells. Journal of Comparative Neurology 310, 139153.Google Scholar
Zhang, D. & Yeh, H.H. (1991). Protein kinase C-like immunoreactivity in rod bipolar cells of the rat retina: A developmental study. Visual Neuroscience 6, 429437.Google Scholar
Ziai, R., Pan, Y.C.E., Hulmes, J.D., Sangameswaran, L. & Morgan, J.I. (1986). Isolation, sequence, and development profile of a brain-specific polypeptide, PEP-19. Proceedings of the National Academy of Sciences of the U.S.A. 83, 84208423.Google Scholar