Immunocytochemical localization of tubulin and microtubule-associated protein 2 during the development of hippocampal neurons in culture.
- Authors
- CΓ‘ceres, A; Banker, G A; Binder, L
- Year
- 1986
- Journal
- The Journal of neuroscience : the official journal of the Society for Neuroscience
- PMID
- 3514816
- DOI
- 10.1523/JNEUROSCI.06-03-00714.1986
- PMCID
- PMC6568475
In dissociated-cell cultures prepared from the embryonic rat hippocampus, neurons establish both axons and dendrites, which differ in geometry, in ultrastructure, and in synaptic polarity. We have used immunocytochemistry with monoclonal antibodies to study the regional distribution of beta-tubulin and micro-tubule-associated protein 2 (MAP2) in hippocampal cultures and their localization during early stages of axonal and dendritic development. After development for a week or more in culture, when axons and dendrites were well-differentiated, the distribution of these two proteins was quite different. Beta-tubulin was present throughout the nerve cell, in soma, dendrites, and axon. It was also present in all classes of non-neuronal cells, astrocytes, fibroblasts, and a presumptive glial progenitor cell. In contrast, MAP2 was preferentially localized to nerve cells; within neurons, MAP2 was present in soma and dendrites, but little or no immunostaining was detectable in axons. Both beta-tubulin and MAP2 were present in nerve cells at the time of plating. From the earliest stages of process extension, beta-tubulin was present in all neuronal processes, both axons and dendrites. Surprisingly, MAP2 was also initially present in both axons and dendrites, extending as far as the axonal growth cone. With subsequent development, MAP2 staining was selectively lost from the axon so that after 1 week in vitro little or no axonal staining remained. Taken together with earlier results (CΓ‘ceres et al., 1984a), these data indicate that the establishment of neuronal polarity, as manifested by the molecular differentiation of the axonal and dendritic cytoskeleton, occurs largely under endogenous control, even under culture conditions in which cell interactions are greatly restricted.(ABSTRACT TRUNCATED AT 250 WORDS)
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| Translational machinery in dendrites of hippocampal neurons in culture. | Tiedge H et al. | β | 1996 | β |
| An increase in phosphorylation of microtubule-associated protein 2 accompanies dendrite extension during the differentiation of cultured hippocampal neurones. | DΓez-Guerra FJ et al. | β | 1995 | β |
| A regulatory role for sphingolipids in neuronal growth. Inhibition of sphingolipid synthesis and degradation have opposite effects on axonal branching. | Schwarz A et al. | β | 1995 | β |
| Astroglia demonstrate regional differences in their ability to maintain primary dendritic outgrowth from mouse cortical neurons in vitro. | Le Roux PD et al. | β | 1995 | β |
| beta-amyloid fibrils induce tau phosphorylation and loss of microtubule binding. | Busciglio J et al. | β | 1995 | β |
| Cloning of AL-1, a ligand for an Eph-related tyrosine kinase receptor involved in axon bundle formation. | Winslow JW et al. | β | 1995 | β |
| Control of neuronal morphology in vitro: interplay between adhesive substrate forces and molecular instruction. | Lochter A et al. | β | 1995 | β |
| High potassium promotes differentiation of retinal neurons but does not favor rod differentiation. | Araki M et al. | β | 1995 | β |
| Long-term bFGF neuronal culture: reintroduction into serum medium yields neurons and non-neuronal cells with neuronal characteristics. | Eubanks JH et al. | β | 1995 | β |
| Polyamines promote regeneration of injured axons of cultured rat hippocampal neurons. | Chu PJ et al. | β | 1995 | β |
| Regionally specific properties of midbrain glia: I. Interactions with midbrain neurons. | Garcia-Abreu J et al. | β | 1995 | β |
| Selective enhancement of axonal branching of cultured dentate gyrus neurons by neurotrophic factors. | Patel MN et al. | β | 1995 | β |
| Synaptogenesis and distribution of presynaptic axonal varicosities in low density primary cultures of neocortex: an immunocytochemical study utilizing synaptic vesicle-specific antibodies, and an electrophysiological examination utilizing whole cell recording. | Lowenstein PR et al. | β | 1995 | β |
| Transport of dendritic microtubules establishes their nonuniform polarity orientation. | Sharp DJ et al. | β | 1995 | β |
| Accumulation of delta 2-tubulin, a major tubulin variant that cannot be tyrosinated, in neuronal tissues and in stable microtubule assemblies. | Paturle-LafanechΓ¨re L et al. | β | 1994 | β |
| A comparison of the developing dopamine neuron phenotype in cultures of embryonic rat mesencephalon and hypothalamus. | Kapatos G et al. | β | 1994 | β |
| Characterization of basic fibroblast growth factor-mediated acceleration of axonal branching in cultured rat hippocampal neurons. | Aoyagi A et al. | β | 1994 | β |
| Developing rat pineal cells manifest potential of neuronal differentiation in vitro. | Araki M et al. | β | 1994 | β |
| Distribution and trafficking of JHM coronavirus structural proteins and virions in primary neurons and the OBL-21 neuronal cell line. | Pasick JM et al. | β | 1994 | β |
| Diverse distribution and function of fibrous microtubule-associated proteins in the nervous system. | Schoenfeld TA et al. | β | 1994 | β |
| Expression of Bcl-2 protein in murine neural cells in culture. | Mizuguchi M et al. | β | 1994 | β |
| Myelin basic protein mediates extracellular signals that regulate microtubule stability in oligodendrocyte membrane sheets. | Dyer CA et al. | β | 1994 | β |
| Neurotrophin-3 enhances neurite outgrowth in cultured hippocampal pyramidal neurons. | Morfini G et al. | β | 1994 | β |
| Polarized distribution of the trans-Golgi network marker TGN38 during the in vitro development of neocortical neurons: effects of nocodazole and brefeldin A. | Lowenstein PR et al. | β | 1994 | β |
| The axonal gamma-aminobutyric acid transporter GAT-1 is sorted to the apical membranes of polarized epithelial cells. | Pietrini G et al. | β | 1994 | β |
| Effects of selective inhibition of protein kinase C, cyclic AMP-dependent protein kinase, and Ca(2+)-calmodulin-dependent protein kinase on neurite development in cultured rat hippocampal neurons. | Cabell L et al. | β | 1993 | β |
| Even in culture, oligodendrocytes myelinate solely axons. | Lubetzki C et al. | β | 1993 | β |
| Glutamate neurotoxicity in mesencephalic dopaminergic neurons in culture. | Kikuchi S et al. | β | 1993 | β |
| Hippocampal growth cone responses to focally applied electric fields. | Davenport RW et al. | β | 1993 | β |
| Localization of the multiple calmodulin messenger RNAs in differentiated PC12 cells. | Zhang SP et al. | β | 1993 | β |
| NILE/L1 and NCAM-polysialic acid expression on growing axons of isolated neurons. | van den Pol AN et al. | β | 1993 | β |
| Okadaic acid induces early changes in microtubule-associated protein 2 and tau phosphorylation prior to neurodegeneration in cultured cortical neurons. | Arias C et al. | β | 1993 | β |
| Peripherin expression in hippocampal neurons induced by muscle soluble factor(s). | Djabali K et al. | β | 1993 | β |
| Preferential dendritic localization of pericentriolar material in hippocampal pyramidal neurons in culture. | Ferreira A et al. | β | 1993 | β |
| Process formation in Sf9 cells induced by the expression of a microtubule-associated protein 2C-like construct. | LeClerc N et al. | β | 1993 | β |
| The distribution of glutamate receptors in cultured rat hippocampal neurons: postsynaptic clustering of AMPA-selective subunits. | Craig AM et al. | β | 1993 | β |
| The segregation and expression of glutamate receptor subunits in cultured hippocampal neurons. | Eshhar N et al. | β | 1993 | β |
| A real-time analysis of growth cone-target cell interactions during the formation of stable contacts between hippocampal neurons in culture. | Cooper MW et al. | β | 1992 | β |
| Chronic treatment with sabeluzole protects cultured rat brain neurons from the neurotoxic effects of excitatory amino acids. | Pauwels PJ et al. | β | 1992 | β |
| Corticosterone accelerates hypoxia- and cyanide-induced ATP loss in cultured hippocampal astrocytes. | Tombaugh GC et al. | β | 1992 | β |
| Developmental differentiation of MAP2 expression in the central versus the peripheral and efferent projections of the inner ear. | Hafidi A et al. | β | 1992 | β |
| Expression of the class III beta-tubulin isotype in developing neurons in culture. | Ferreira A et al. | β | 1992 | β |
| Glucocorticoids exacerbate hypoxic and hypoglycemic hippocampal injury in vitro: biochemical correlates and a role for astrocytes. | Tombaugh GC et al. | β | 1992 | β |
| Immortal rat hippocampal cell lines exhibit neuronal and glial lineages and neurotrophin gene expression. | Eves EM et al. | β | 1992 | β |
| Isoforms of the Na,K-ATPase are present in both axons and dendrites of hippocampal neurons in culture. | Pietrini G et al. | β | 1992 | β |
| Laminin selectively enhances axonal growth and accelerates the development of polarity by hippocampal neurons in culture. | Lein PJ et al. | β | 1992 | β |
| Redistribution of B-50/growth-associated protein 43 during differentiation and maturation of rat hippocampal neurons in vitro. | van Lookeren Campagne M et al. | β | 1992 | β |
| Alpha 1-antichymotrypsin supports short-term survival of cerebral neurons in culture. | Mizuguchi M et al. | β | 1991 | β |
| Association of microtubule-associated protein (MAP1B) with growing axons in cultured hippocampal neurons. | Fischer I et al. | β | 1991 | β |
| Calpain-mediated proteolysis of microtubule associated proteins MAP1B and MAP2 in developing brain. | Fischer I et al. | β | 1991 | β |
| Evidence for calcium-reducing and excito-protective roles for the calcium-binding protein calbindin-D28k in cultured hippocampal neurons. | Mattson MP et al. | β | 1991 | β |
| Expression of a neuromodulin-beta-galactosidase fusion protein in primary cultured neurons and its accumulation in growth cones. | Liu YC et al. | β | 1991 | β |
| Isolation and characterization of mouse neural precursor cells in primary culture. | Kitani H et al. | β | 1991 | β |
| MAP5 in cultured hippocampal neurons: expression diminishes with time and growth cones are not immunostained. | Denny JB | β | 1991 | β |
| Microtubule dynamics in axons and dendrites. | Baas PW et al. | β | 1991 | β |
| Ontogeny of MAP2 and GFAP antigens in primary cultures of embryonic chick brain. Effect of substratum, oxygen tension, serum and Ara-C. | Bruinink A et al. | β | 1991 | β |
| Synchronous neurite branchings in single goldfish retinal ganglion cells. | Ishida AT et al. | β | 1991 | β |
| Tau protein and the establishment of an axonal morphology. | Kosik KS et al. | β | 1991 | β |
| Temporal pattern of survival and dendritic growth of fetal hippocampal cells transplanted into ischemic lesions of the adult rat hippocampus. | Katayama Y et al. | β | 1991 | β |
| Adhesion and the in vitro development of axons and dendrites. | Prochiantz A et al. | β | 1990 | β |
| Cell culture of cryopreserved human fetal cerebral cortical and hippocampal neurons: neuronal development and responses to trophic factors. | Mattson MP et al. | β | 1990 | β |
| Differential subcellular localization of particular mRNAs in hippocampal neurons in culture. | Kleiman R et al. | β | 1990 | β |
| Localized calcium influx orients axon formation in embryonic hippocampal pyramidal neurons. | Mattson MP et al. | β | 1990 | β |
| Nerve growth factor potentiates the neurotoxicity of beta amyloid. | Yankner BA et al. | β | 1990 | β |
| Neurotrophic and neurotoxic effects of amyloid beta protein: reversal by tachykinin neuropeptides. | Yankner BA et al. | β | 1990 | β |
| Phosphorylation of microtubule proteins in rat brain at different developmental stages: comparison with that found in neuronal cultures. | DΓaz-Nido J et al. | β | 1990 | β |
| Polarized sorting of viral glycoproteins to the axon and dendrites of hippocampal neurons in culture. | Dotti CG et al. | β | 1990 | β |
| An immunohistochemical characterization of the primitive and maturing neuroepithelial components in the OTT-6050 transplantable mouse teratoma. | Caccamo DV et al. | β | 1989 | β |
| An immunohistochemical study of neuropeptides and neuronal cytoskeletal proteins in the neuroepithelial component of a spontaneous murine ovarian teratoma. Primitive neuroepithelium displays immunoreactivity for neuropeptides and neuron-associated beta-tubulin isotype. | Caccamo DV et al. | β | 1989 | β |
| Characteristics of microtubules at the different stages of neuronal differentiation and maturation. | Meininger V et al. | β | 1989 | β |
| Compartmentation of alpha-tubulin in neurons: identification of a somatodendritic-specific variant of alpha-tubulin. | Baas PW et al. | β | 1989 | β |
| Development and selective neurodegeneration in cell cultures from different hippocampal regions. | Mattson MP et al. | β | 1989 | β |
| Excitatory and inhibitory neurotransmitters in the generation and degeneration of hippocampal neuroarchitecture. | Mattson MP et al. | β | 1989 | β |
| Experimental observations on the development of polarity by hippocampal neurons in culture. | Goslin K et al. | β | 1989 | β |
| Immunocytochemical localization of microtubule-associated proteins 1A and 2 in the rat retina. | Okabe S et al. | β | 1989 | β |
| Influence of extracellular matrix proteins on the expression of neuronal polarity. | Chamak B et al. | β | 1989 | β |
| Localization and mobility of omega-conotoxin-sensitive Ca2+ channels in hippocampal CA1 neurons. | Jones OT et al. | β | 1989 | β |
| Microtubular reorganization and dendritic growth response in Alzheimer's disease. | McKee AC et al. | β | 1989 | β |
| Microtubule formation and neurite growth in cerebellar macroneurons which develop in vitro: evidence for the involvement of the microtubule-associated proteins, MAP-1a, HMW-MAP2 and Tau. | Ferreira A et al. | β | 1989 | β |
| Monoclonal antibody markers for amphibian oligodendrocytes and neurons. | Steen P et al. | β | 1989 | β |
| Neuroblastic differentiation potential of the human retinoblastoma cell lines Y-79 and WERI-Rb1 maintained in an organ culture system. An immunohistochemical, electron microscopic, and biochemical study. | Herman MM et al. | β | 1989 | β |
| Rapid turnover of microtubule-associated protein MAP2 in the axon revealed by microinjection of biotinylated MAP2 into cultured neurons. | Okabe S et al. | β | 1989 | β |
| Rearrangement of microtubule associated protein parallels the morphological transformation of neurons from dorsal root ganglion. | HernΓ‘ndez MA et al. | β | 1989 | β |
| Survival and growth of hippocampal neurons in defined medium at low density: advantages of a sandwich culture technique or low oxygen. | Brewer GJ et al. | β | 1989 | β |
| The establishment of polarity by hippocampal neurons: the relationship between the stage of a cell's development in situ and its subsequent development in culture. | Fletcher TL et al. | β | 1989 | β |
| The expression of acetylated microtubules during axonal and dendritic growth in cerebellar macroneurons which develop in vitro. | Ferreira A et al. | β | 1989 | β |
| Tyrosination state of tubulin and the activity of tubulin:tyrosine ligase and tubulin carboxypeptidase in the developing retina of the chick. | Arregui C et al. | β | 1989 | β |
| What distinguishes axons from dendrites? Neurons know more than we do. | Sargent PB | β | 1989 | β |
| Development of neuronal polarity: GAP-43 distinguishes axonal from dendritic growth cones. | Goslin K et al. | β | 1988 | β |
| Interactions between entorhinal axons and target hippocampal neurons: a role for glutamate in the development of hippocampal circuitry. | Mattson MP et al. | β | 1988 | β |
| Intracellular messengers in the generation and degeneration of hippocampal neuroarchitecture. | Mattson MP et al. | β | 1988 | β |
| Isolated hippocampal neurons in cryopreserved long-term cultures: development of neuroarchitecture and sensitivity to NMDA. | Mattson MP et al. | β | 1988 | β |
| Microtubule-associated protein 2 (MAP 2) immunoreactivity in human fetal neocortex. | Sims KB et al. | β | 1988 | β |
| Microtubule-associated proteins characteristic of embryonic brain are found in the adult mammalian retina. | Tucker RP et al. | β | 1988 | β |
| Morphological differentiation of embryonic rat sympathetic neurons in tissue culture. I. Conditions under which neurons form axons but not dendrites. | Bruckenstein DA et al. | β | 1988 | β |
| Neurotransmitters in the regulation of neuronal cytoarchitecture. | Mattson MP | β | 1988 | β |
| Polarity orientation of microtubules in hippocampal neurons: uniformity in the axon and nonuniformity in the dendrite. | Baas PW et al. | β | 1988 | β |
| Protein synthesis and processing in cytoplasmic microdomains beneath postsynaptic sites on CNS neurons. A mechanism for establishing and maintaining a mosaic postsynaptic receptive surface. | Steward O et al. | β | 1988 | β |
| The distribution of microtubule-associated protein 2 changes when dendritic growth is induced in rat sympathetic neurons in vitro. | Higgins D et al. | β | 1988 | β |
| Aluminum and Alzheimer's disease: perspectives for a cytoskeletal mechanism. | Bertholf RL | β | 1987 | β |
| An immunocytochemical analysis of the ontogeny of the microtubule-associated proteins MAP-2 and Tau in the nervous system of the rat. | Ferreira A et al. | β | 1987 | β |
| Changes in the number of chick ciliary ganglion neuron processes with time in cell culture. | Role LW et al. | β | 1987 | β |
| Role of microtubules in the cytoplasmic compartmentation of neurons. | Baas PW et al. | β | 1987 | β |
| Sequential appearance of cytoskeletal components during the early stages of neurite outgrowth from cerebellar granule cells in vitro. | Cambray-Deakin MA et al. | β | 1987 | β |
| The expression and distribution of the microtubule-associated proteins tau and microtubule-associated protein 2 in hippocampal neurons in the rat in situ and in cell culture. | Dotti CG et al. | β | 1987 | β |