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On the organization of astrocytic gap junctions in rat brain as suggested by LM and EM immunohistochemistry of connexin43 expression

Yamamoto, T., Ochalski, A., Hertzberg, E. L., Nagy, J. I.·1990·Journal of Comparative Neurology

DOI 10.1002/cne.903020414

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Abstract

Gap junctions and the intercellular communication syncytium they form between glial cells are thought to play a critical role in glial maintenance of appropriate metabolic environments in neural tissues. We have previously suggested (Yamamoto et al., Brain Res. 508:313–319, '90) that the vast majority of astrocytes in rat brain express connexin43, one of several recently identified gap junction proteins. Here, we confirm ultrastructurally that astrocytes in a number of brain regions of rat are immunolabelled with an antibody against connexin43 and that neurons and oligodendrocytes are devoid of labelling. The distribution of connexin43 immunoreactivity throughout the brain is presented at the light microscope (LM) level. By LM, immunoreactive structures consisted primarily of round or elongated puncta ranging from 0.3 μm to 4 μm in length and of annular profiles ranging from 1 to 10 μm in diameter. Immunolabelled fibrous processes were only occasionally seen and no labelling was observed in astrocytic cell bodies. Long, linear arrays of puncta were rare in gray matter but were common in white matter where they were arranged parallel to myelinated fibers. Puncta organized in a honeycomb pattern were seen near the cerebral cortical surface and frequently around blood vessels. Regional immunoreaction density, which was a reflection of either the concentration or staining intensity of immunoreactive elements, was remarkably heterogeneous; dramatic differences in labelling intensity frequently delineated anatomical boundaries between adjacent nuclei. Abrupt as well as graded fluctuations of immunoreaction intensity were also observed within nuclear structures. By electron microscopy (EM), gap junctions of fibrous and protoplasmic astrocytes were intensely stained and labelled organelles were often observed intracellularly in areas near gap junctions. These junctions and the spread of immunoreaction product to perijunctional organelles in their vicinity were considered to correspond to puncta seen by LM. Labelling within astrocytic cell bodies was seen in only a few instances. In some brain areas, astrocytic processes commonly gave rise to immunoreactive lamellae that partially ensheathed neuronal cell bodies, axon terminals, dendrites, and synaptic glomeruli. Such lamellae were considered to correspond to immunoreactive annular profiles seen by LM. Perivascular endfoot processes of astrocytes displayed intense staining of their gap junctions and portions of their apposing membranes. To the extent that regional differences and ultrastructural localization of connexin43 immunoreactivity reveal global distributions of astrocytic gap junctions composed of connexin43, we suggest (1) that the absence of widespread cytoplasmic labelling within astrocytes may be indicative of local connexin43 synthesis near gap junctions, (2) that small scale heterogeneities within nuclei may reflect relationships between the organizational patterns of glial gap junctions and neural systems, and (3) that enormous variations in demands for gap junctional coupling within astrocytic “functional syncytia” of different brain regions may lead to the establishment of largely separate syncytial compartments.

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BackgroundSelf-citation
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Immunorecognition, ultrastructure and phosphorylation status of astrocytic gap junctions and connexin43 in rat brain after cerebral focal ischaemia
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“Astrocytes in the central nervous system (CNS) are extensively coupled via gap junctions containing high levels of Cx43 (Yamamoto et al., 1990a,b; Wolburg & Rohlmann, 1995; Giaume & McCarthy, 1996; Ochalskiet al., 1996).”
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Protein and messenger RNA expression of connexin43 in astrocytomas: implications in brain tumor gene therapy
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β4 integrin and other Schwann cell markers in axonal neuropathy
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Selective Monoclonal Antibody Recognition and Cellular Localization of an Unphosphorylated Form of Connexin43
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Expression of connexin genes in hippocampus of kainate-treated and kindled rats under conditions of experimental epilepsy
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BackgroundResultInfluential
Structure-Function Relationships in Gap Junctions
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Association Between Dendritic Lamellar Bodies and Complex Spike Synchrony in the Olivocerebellar System
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Self-citation
Connexin29 and connexin32 at oligodendrocyte and astrocyte gap junctions and in myelin of the mouse central nervous system
Nagy, J. I., Ionescu, A. V., Lynn, B. D., & Rash, J. E. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.10797 · Cited by 95
“Immunofluorescence for Cx43 throughout the brain appeared as densely distributed puncta, most of which represented labeling of gap junctions between astrocytes (Yamamoto et al., 1990a,b).”
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Glial and neuronal connexin expression patterns in the rat spinal cord during development and following injury
Lee, I., Lindqvist, E., Kiehn, O., Widenfalk, J., & Olson, L. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20567 · Cited by 96
“Gap junctions are targets for a number of cytokines, neurotransmitters, growth factors, and endogenous bioactive lipids (Rouach et al., 2002) and also are sensitive to pH (Morley et al., 1996) and phosphorylation (Zhou et al., 1999).”
Background
GJA1 (connexin43) is a key regulator of Alzheimer’s disease pathogenesis
Kajiwara, Y., Wang, E., Wang, M., Sin, W. C., Brennand, K., Schadt, E. E., Naus, C. C. G., Buxbaum, J. D., & Zhang, B. (2018) · Acta Neuropathologica Communications · doi:10.1186/s40478-018-0642-x · Cited by 99
Ischemia-induced cellular redistribution of the astrocytic gap junctional protein connexin43 in rat brain
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Self-citation
Evidence for the co-localization of another connexin with connexin-43 at astrocytic gap junctions in rat brain
Nagy, J. I., Ochalski, P. A. Y., Li, J., & Hertzberg, E. L. (1997) · Neuroscience · doi:10.1016/s0306-4522(96)00584-2 · Cited by 92
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Postnatal development of dye‐coupling among astrocytes in rat visual cortex
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Connexin-43 in rat spinal cord: localization in astrocytes and identification of heterotypic astro-oligodendrocytic gap junctions
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Interconnectivity between the amygdaloid complex and the amygdalostriatal transition area: A PHA‐L study in rat
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Light and electron microscopic immunocytochemical analysis of the neurovascular relationships of choline acetyltransferase and vasoactive intestinal polypeptide nerve terminals in the rat cerebral cortex
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Alterations in metabolism and gap junction expression may determine the role of astrocytes as “good samaritans” or executioners
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“Therefore, it is important to investigate the kinetic and regulatory properties of glycolytic and TCA cycle enzymes in astrocytes, in comparison to neurons, to improve our understanding of these two important pathways in other CNS cell types.”
BackgroundInfluential
Identification of connexin36 in gap junctions between neurons in rodent locus coeruleus
Rash, J. E., Olson, C. O., Davidson, K. G. V., Yasumura, T., Kamasawa, N., & Nagy, J. I. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.04.061 · Cited by 85
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Heterogeneity in gap junction expression in astrocytes cultured from different brain regions
Batter, D. K., Corpina, R. A., Roy, C., Spray, D. C., Hertzberg, E. L., & Kessler, J. A. (1992) · Glia · doi:10.1002/glia.440060309 · Cited by 85
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New insights into the expression and function of neural connexins with transgenic mouse mutants
Söhl, G., Odermatt, B., Maxeiner, S., Degen, J., & Willecke, K. (2004) · Brain Research Reviews · doi:10.1016/j.brainresrev.2004.05.006 · Cited by 88
Differential anatomical and cellular patterns of connexin43 expression during postnatal development of rat brain
Yamamoto, T., Vukelic, J., Hertzberg, E. L., & Nagy, J. I. (1992) · Developmental Brain Research · doi:10.1016/0165-3806(92)90077-a · Cited by 83
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Modulation of Burst Frequency, Duration, and Amplitude in the Zero-Ca2+ Model of Epileptiform Activity
Bikson, M., Ghai, R. S., Baraban, S. C., & Durand, D. M. (1999) · Journal of Neurophysiology · doi:10.1152/jn.1999.82.5.2262 · Cited by 83
“…a small number of nearby CA1 pyramidal cells (Perez-Velazquez et al. 1984), CA1 astrocytes are characterized by an extremely high degree of cell-to-cell coupling among hundreds of cells (D’Ambrosio et al. 1998) and express high levels of connexins (Dermietzel and Spray 1993; Yamamoto et al. 1990).”
Background
Astrocytic dye coupling in rat hippocampus: Topography, developmental onset, and modulation by protein kinase C
Konietzko, U., & Müller, C. M. (1994) · Hippocampus · doi:10.1002/hipo.450040313 · Cited by 84
Modeling Working Memory in a Spiking Neuron Network Accompanied by Astrocytes
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Astroglia: Important mediators of traumatic brain injury
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Gap Junctions Formed of Connexin43 Are Found Between Smooth Muscle Cells of Human Corpus Cavernosum
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Up-regulation of Connexin43 in the glial scar following photothrombotic ischemic injury.
Haupt, C., Witte, O., & Frahm, C. (2007) · Molecular and cellular neurosciences · doi:10.1016/j.mcn.2007.02.005 · Cited by 76
“Therefore, although both proteins are localized in astrocytes, their subcellular colocalization is rather poor (Yamamoto et al., 1990).”
Background
Homotypic and Heterotypic Coupling Mediated by Gap Junctions During Glial Cell Differentiation In Vitro
Venance, L., Cordier, J., Monge, M., Zalc, B., Glowinski, J., & Giaume, C. (1995) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1995.tb00341.x · Cited by 74
Expression and function of astrocytic gap junctions in aging
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Quantitative immunohistochemical and biochemical correlates of connexin43 localization in rat brain
Nagy, J. I., Yamamoto, T., Sawchuk, M. A., Nance, D. M., & Hertzberg, E. L. (1992) · Glia · doi:10.1002/glia.440050102 · Cited by 71
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Connexin immunoreactivity in glial cells of the rat retina
Zahs, K. R., Kofuji, P., Meier, C., & Dermietzel, R. (2002) · The Journal of Comparative Neurology · doi:10.1002/cne.10524 · Cited by 68
Facial nerve lesions lead to increased immunostaining of the astrocytic gap junction protein (connexin 43) in the corresponding facial nucleus of rats
Rohlmann, A., Laskawi, R., Hofer, A., Dobó, E., Dermietzel, R., & Wolff, J. R. (1993) · Neuroscience Letters · doi:10.1016/0304-3940(93)90208-3 · Cited by 66
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“Connexin43 immunoreactivity was most abundant in astrocytes, as was evident from ultrathin brain sections and postnatal cultured astrocytes (Dermietzel et al. 1989; Shiosaka et al. 1989; Yamamoto et al. 1990; Dermietzel et al. 1991; Giaume et al. 1991).”
Phosphorylated Forms of Connexin43 Predominate in Rat Brain: Demonstration by Rapid Inactivation of Brain Metabolism
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“Only a moderate degree of Cx43 dephosphorylation occurs under standard perfusion fixation conditions previously used to prepare brain tissue for immunohistochemical analysis (Yamamoto et al., 1990; Nagy et al., 1992).”
BackgroundResultSelf-citation
Recent advances in Bio-conjugated nanocarriers for crossing the Blood-Brain Barrier in (pre-)clinical studies with an emphasis on vesicles
Poustforoosh, A., Nematollahi, M. H., Hashemipour, H., & Pardakhty, A. (2022) · Journal of Controlled Release · doi:10.1016/j.jconrel.2022.02.015 · Cited by 62
Intercellular calcium signaling and gap junctional communication in astrocytes
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Physiology of Bergmann Gllal Cells
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Developmental regulation and asymmetric expression of the gene encoding Cx43 gap junctions in the mouse limb bud
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Ablation of Cx47 in transgenic mice leads to the loss of MUPP1, ZONAB and multiple connexins at oligodendrocyte–astrocyte gap junctions
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“Homologous intercellular as well as autologous astrocyte– astrocyte gap junctions formed by various combinations of Cx26, Cx30 and Cx43 link astrocyte processes at their ensheathments of neuronal and vascular elements (Mugnaini, 1986; Yamamoto et al., 1990; Wolburg & Rohlmann, 1995).”
BackgroundSelf-citation
Biochemical and ultrastructural evidence for the association of basic fibroblast growth factor with cardiac gap junctions.
Kardami, E., Stoski, R. M., Doble, B. W., Yamamoto, T., Hertzberg, E. L., & Nagy, J. I. (1991) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)55030-4 · Cited by 58
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Expression of a connexin 43/beta-galactosidase fusion protein inhibits gap junctional communication in NIH3T3 cells.
Sullivan, R., & Lo, C. W. (1995) · The Journal of Cell Biology · doi:10.1083/jcb.130.2.419 · Cited by 58
“…polyclonal antibody (generously provided by Elliot Hertzberg, Albert Einstein College of Medicine, Bronx, NY; directed to the carboxy terminus at amino acid residues 346-360; Nagy et al., 1992; Yamamoto, et al., 1990) or anti-13-gal polyclonal antibody (Cappel Laboratories, West Chester , PA).”
Background
Kainic acid induced alterations in antibody recognition of connexin43 and loss of astrocytic gap junctions in rat brain
Hossain, M. Z., Sawchuk, M. A., Murphy, L. J., Hertzberg, E. L., & Nagy, J. I. (1994) · Glia · doi:10.1002/glia.440100404 · Cited by 57
“We previously reported that the distribution of Cx43 in rat brain is highly heterogeneous as observed by regional immunohistochemical and Western blot analysis (Nagy et al., 1992; Yamamoto et al., 1990).”
Self-citation

Authors: Yamamoto, T., Ochalski, A., Hertzberg, E. L., & Nagy, J. I.
Affiliations: University of Manitoba (CA)
Albert Einstein College of Medicine (US)
Corresponding author: Nagy, J. I.
ORCID: Yamamoto, T.
Nagy, J. I.
Venue: Journal of Comparative Neurology
Publisher: Wiley
Published: 1990-12-22
Volume: 302
Issue: 4
Pages: 853-883
ISSN: 0021-9967 (ISSN-L)
1096-9861
DOI: 10.1002/cne.903020414
OpenAlex: W2116763991
Cited by: 230
References: 110
Citations by year: 2026: 3 · 2025: 3 · 2024: 1 · 2023: 4 · 2022: 3 · 2021: 5 · 2020: 2 · 2019: 1 · 2018: 6 · 2017: 5 · 2016: 2 · 2015: 3 · 2014: 2 · 2013: 5 · 2012: 3
FWCI: 3.00
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor, 5040 d)
Locations: The Journal of Comparative Neurology (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (5r01gm030667-14)
National Institute of General Medical Sciences (GM 30667)
Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD00713)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Connexins and lens biology
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Neurology › Barrier Structure and Function Studies
Keywords: astrocytes, connexin 43, gap junctions, astrocyte ultrastructure, immunoreactivity distribution, white matter, gray matter, astrocyte-neuron communication, cerebral cortex, rat brain
MeSH terms: Animals, Astrocytes, Brain Chemistry, Immunoenzyme Techniques, Intercellular Junctions, Male, Membrane Proteins, Microscopy, Electron, Myocardium, Nerve Tissue Proteins, Organ Specificity, Rats, Inbred Strains, Connexins, Rats

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On the organization of astrocytic gap junctions in rat brain as suggested by LM and EM immunohistochemistry of connexin43 expression

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