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On the organization of astrocytic gap junctions in rat brain as suggested by LM and EM immunohistochemistry of connexin43 expression
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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“Astrocytes express gap junction proteins CX30 and CX43 (167, 377, 665).”
From Blood-Brain Barrier: From Physiology to Disease and Back (2019) · cites this paper as [665]
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Self-citationYamamoto, T., Hossain, M. Z., Hertzberg, E. L., Uemura, H., Murphy, L. J., & Nagy, J. I. (1993) · Histochemistry and Cell Biology · doi:10.1007/bf00268878 · Cited by 56
“…in astrocytes and in various cell types lining the brain surfaces, that connexin26 is expressed in addition by leptomeningial cells and that connexin32 (Cx32) is expressed by oligodendrocytes (Dermietzel et al. 1989; Micevych and Abelson 1991; Yamamoto et al. 1990a, b, 1992b; Nagy et al. 1992).”
BackgroundMethodResultInfluentialSelf-citationVukelic, J. I., Yamamoto, T., Hertzberg, E. L., & Nagy, J. I. (1991) · Neuroscience Letters · doi:10.1016/0304-3940(91)90242-l · Cited by 52
Self-citationNagy, J. I., Lynn, B. D., Tress, O., Willecke, K., & Rash, J. E. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07741.x · Cited by 53
“…in which macroglial cells form gap junctions and targeting of connexins to these compartments has been extensively investigated (Mugnaini, 1986; Yamamoto et al., 1990; Wolburg & Rohlmann, 1995; Rash et al., 1997, 2001a; Kamasawa et al., 2005; reviewed in Theis et al., 2005; Orthmann-Murphy et…”
BackgroundSelf-citationSyncytial isopotentiality: A system‐wide electrical feature of astrocytic networks in the brain
Kiyoshi, C. M., Du, Y., Zhong, S., Wang, W., Taylor, A. T., Xiong, B., Ma, B., Terman, D. H., & Zhou, M. (2018) · Glia · doi:10.1002/glia.23525 · Cited by 53
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“Within the brain, astrocytes are coupled in vivo extensively through the intermembrane channels known as gap junctions (Mugnaini, 1986; Yamamoto et al., 1990; Binmoeller and Muller, 1992).”
BackgroundExpression of connexins in the developing olfactory system of the mouse
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Chapter 17 Signal processing in the C2 module of the flocculus and its role in head movement control
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Characteristics of C6 glioma cells overexpressing a gap junction protein
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“It has been previously speculated that astrocytic populations in distinct compartments of the brain could even form distinct syncytia (Mugnaini, 1986; Yamamoto et al., 1990).”
BackgroundGap junctions are involved in cell migration in the early postnatal subventricular zone
Marins, M., Xavier, A. L. R., Viana, N. B., Fortes, F. S. A., Fróes, M. M., & Menezes, J. R. L. (2009) · Developmental Neurobiology · doi:10.1002/dneu.20737 · Cited by 49
“These junctions have been detected in the SVZ/RMS by electron microscopy and imunohistochemistry (Yamamoto et al., 1990; Miragall et al., 1997).”
BackgroundBall, K. K., Gandhi, G. K., Thrash, J., Cruz, N. F., & Dienel, G. A. (2007) · Journal of Neuroscience Research · doi:10.1002/jnr.21376 · Cited by 49
“G; 200 lm in H. Journal of Neuroscience Research DOI 10.1002/jnr Astrocytic endfeet are linked together by gap junctions (Yamamoto et al., 1990a,b) and, after injection into a cerebral cortical astrocyte, LY can be transferred along an immediately adjacent vessel via endfeet (Simard et al., 2003).”
BackgroundMethodInfluentialIntercellular calcium signaling between astrocytes and oligodendrocytes via gap junctions in culture
Parys, J. B., Côté, A., Gallo, V., Koninck, P. D., & Attila Gabor, S. I. K. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.03.004 · Cited by 47
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The many ways astroglial connexins regulate neurotransmission and behavior
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“In the central nervous system, Cx43 immunoreactivity has not been generally observed in neurons of adult animals ~Dermietzel et al., 1989; Yamamoto et al., 1990; Rash et al., 2001; but see Nadarajah et al., 1996 and Simburger et al., 1997 for reports of neuronal Cx43!, nor in resting microglia…”
BackgroundLocalization of connexin26 and connexin32 in putative CO2-chemosensitive brainstem regions in rat
Solomon, I. C., Halat, T. J., El‐Maghrabi, M. R., & O'Neal, M. H. (2001) · Respiration Physiology · doi:10.1016/s0034-5687(01)00299-7 · Cited by 47
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“In this study, the major effect of Cx43 mimetic peptide s assumed to be on astrocytic gap junctions since Cx43 is hought to be predominantly expressed by astrocytes (Nagy t al., 1999; Yamamoto et al., 1990).”
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Self-citationFunction of Glia in Aging and the Brain Diseases
Vallés, S. L., Iradi, A., Aldasoro, M., Vila, J. M., Aldasoro, C., de la Torre, J., Campos-Campos, J., & Jorda, A. (2019) · International Journal of Medical Sciences · doi:10.7150/ijms.37769 · Cited by 45
“However, astrocytes have different populations surrounding neuron types and that is true for protoplasmic astrocytes, which make contact with neurons, and for fibrous astrocytes that contact neuronal extensions (40,41).”
BackgroundLi, W., & Nagy, J. I. (2000) · Neuroscience · doi:10.1016/s0306-4522(00)00032-4 · Cited by 44
Self-citationBrain Disorders and Chemical Pollutants: A Gap Junction Link?
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Astrocyte Role in Temporal Lobe Epilepsy and Development of Mossy Fiber Sprouting
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Gap junctions in glia. Types, roles, and plasticity.
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Subcellular Topography and Plasticity of Gap Junction Distribution on Astrocytes
Rohlmann, A., & Wolff, J. R. (1996) · Neuroscience intelligence unit · doi:10.1007/978-3-662-21935-5_10 · Cited by 43
Astrocytes mediate analogous memory in a multi-layer neuron–astrocyte network
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“…yet clear, but may to some extent be related to their utilization of some of these connexins at different subcellular compartments (Mugnaini, 1986; Yamamoto et al., 1990; Wolburg & Rohlmann, 1995; Rash et al., 1997, 2001a,b; Kamasawa et al., 2005; Theis et al., 2005; OrthmannMurphy et al., 2008;…”
BackgroundInfluentialSelf-citationChapter 5 Astrocytes in the mammalian circadian clock: putative roles
Serviere, J., & Lavialle, M. (1996) · Progress in brain research · doi:10.1016/s0079-6123(08)60400-8 · Cited by 36
Is connexin36 critical for GABAergic hypersynchronization in the hippocampus?
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“Therefore, the antiepileptic effect of carbenoxolone in wild-type and Cx36 KO mice may simply suggest that other connexins expressed by glial cells or pyramidal neurons (Yamamoto et al. 1990; Belluardo et al. 2000; Nagy et al. 2004; Weickert et al. 2005) are the real molecular targets.”
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Paternostro, M. A., Reyher, C. K. H., & Brunjes, P. C. (1995) · Developmental Brain Research · doi:10.1016/0165-3806(94)00146-q · Cited by 36
Molecular Diversity and Plasticity of Gap Junctions in the Nervous System
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Temporal profile of connexin 43 expression after photothrombotic lesion in rat brain
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“Astrocytes are extensively coupled through gap junctions (Mugnaini, 1986; Yamamoto et al., 1990; Binmoeller and Muller, 1992).”
BackgroundGap junctions and connexins in the mammalian central nervous system
Nagy, J. I., & Dermietzel, R. (2000) · Advances in molecular and cell biology · doi:10.1016/s1569-2558(00)30009-1 · Cited by 31
Self-citationGap Junction Disorders of Myelinating Cells
Kleopa, K. A., Orthmann‐Murphy, J. L., & Sargiannidou, I. (2010) · Reviews in the Neurosciences · doi:10.1515/revneuro.2010.21.5.397 · Cited by 31
Connexins and Information Transfer Through Glia
Bruzzone, R., & Giaume, C. (1999) · Advances in experimental medicine and biology · doi:10.1007/978-1-4615-4685-6_26 · Cited by 33
Differences in the expression of connexin genes in rat hepatomas in vivo and in vitro
Neveu, M. J., Sattler, C. A., Sattler, G. L., Hully, J. R., Hertzberg, E. L., Paul, D. L., Nicholson, B. J., & Pitot, H. C. (1994) · Molecular Carcinogenesis · doi:10.1002/mc.2940110305 · Cited by 32
Self-citationEXPRESSION OF GAP JUNCTION CONNEXIN36 IN ADULT RAT RETINAL GANGLION CELLS
Hidaka, S., Kato, T., & Miyachi, E. (2002) · Journal of Integrative Neuroscience · doi:10.1142/s0219635202000025 · Cited by 31
Lutz, S. E., Raine, C. S., & Brosnan, C. F. (2012) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2012.01.007 · Cited by 30
“These data show that loss of the astrocytic connexins, Cx43 and Cx30, and the white matter pathology observed in these mice does not statistically affect clinical or pathological expression of EAE and show that astrocyte gap junctions do not regulate autoimmune inflammation and associated BBB disruption in acute EAE.”
InfluentialSolomon, I. C., Halat, T. J., El-Maghrabi, R. M., & O'Neal, M. H. (2001) · The Journal of Comparative Neurology · doi:10.1002/cne.1366 · Cited by 30
“It should be noted that punctate labeling, when seen as plaques in the plasma membrane, is considered to represent the organization of fully functional gap junctions between neighboring cells (Yamamoto et al., 1990, 1992; Nagy et al., 1992).”
BackgroundYamane, Y., Shiga, H., Asou, H., & Ito, E. (2002) · Neuroscience · doi:10.1016/s0306-4522(02)00095-7 · Cited by 30
Condamine, S., Lavoie, R., Verdier, D., & Kolta, A. (2017) · Glia · doi:10.1002/glia.23244 · Cited by 29
Rash, J. E., Kamasawa, N., Davidson, K. G. V., Yasumura, T., Pereda, A. E., & Nagy, J. I. (2012) · The Journal of Membrane Biology · doi:10.1007/s00232-012-9454-2 · Cited by 27
“…issues of gap junction connexin composition and the ‘‘sidedness’’ of connexin expression, ultrastructural approaches have been employed, including thin-section TEM (Nagy et al. 1999, 2001; Ochalski et al. 1997; Yamamoto et al. 1990a, b), FRIL and, more recently, double-replica FRIL (DR-FRIL).”
MethodSelf-citationThe K‐ATP channel regulates the effect of Ca2+ on gap junction permeability in cultured astrocytes
Granda, B., Tabernero, A., Sánchez‐Abarca, L. I., & Medina, J. M. (1998) · FEBS Letters · doi:10.1016/s0014-5793(98)00390-1 · Cited by 27
Gap Junction-Mediated Coupling in the Postnatal Anterior Subventricular Zone
Menezes, J. R. L., Fróes, M. M., Moura‐Neto, V., & Lent, R. (2000) · Developmental Neuroscience · doi:10.1159/000017425 · Cited by 27
“Although cell coupling by gap junctions is not an obligatory property of germinal layers [Rossi and Slater, 1993], there are reasons to believe that the SVZa cells are also coupled, since these junctions were identified by EM therein [Miragall et al., 1992; Yamamoto et al., 1990] and connexins have been detected in th…”
BackgroundConsequences of Impaired Gap Junctional Communication in Glial Cells
Naus, C. C. G., Bani‐Yaghoub, M., Bechberger, J. F., & Rushlow, W. J. (1999) · Advances in experimental medicine and biology · doi:10.1007/978-1-4615-4685-6_29 · Cited by 25
The “Connexin” Between Bone Cells and Skeletal Functions
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“It is expressed in cells of almost all tissues in the body, including the brain [Yamamoto et al., 1990; Simburger et al., 1997], heart [Beyer et al.”
BackgroundSleep deprivation and sleep recovery modifies connexin36 and connexin43 protein levels in rat brain
Franco‐Pérez, J., Ballesteros‐Zebadúa, P., Fernández-Figueroa, E. A., Ruiz-Olmedo, I., Reyes‐Grajeda, J. P., & Paz, C. (2011) · Neuroreport · doi:10.1097/wnr.0b013e32834e8fcb · Cited by 25
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Connexin 43 mRNA expression in two experimental models of epilepsy
Elisevich, K. V., Rempel, S. A., Smith, B. J., & Allar, N. (1997) · Molecular and Chemical Neuropathology · doi:10.1007/bf02815168 · Cited by 23
Vasoactive intestinal polypeptide in sacral primary sensory pathways in the cat
Morgan, C. W., Ohara, P. T., & Scott, D. E. (1999) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19990510)407:3 · Cited by 25
Umino, Y., & Saito, T. (2002) · The Journal of Comparative Neurology · doi:10.1002/cne.10429 · Cited by 21
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“most other brain regions, together with the close proximity of some of these junctions to the plasma membranes of neuronal somata and dendrites (Yamamoto et al., 1990), which can be < 0.”
BackgroundInfluentialSelf-citationBiswas, J., Gupta, S., Verma, D., & Singh, S. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.05.018 · Cited by 21
“Studies have also showed that the connexin 30 and 43 are the most prominent connexin in astrocytes (Yamamoto et al., 1990b, a, Rash et al., 2001) which contribute to local metabolic homeostasis (Walz, 1989) by gap junction mediated intercellular coupling between these cells (Dermietzel et al.,…”
Connexin43 mRNA and protein expression during postnatal development of defined brain regions
Åberg, N. D., Rönnbäck, L., & Eriksson, P. S. (1999) · Developmental Brain Research · doi:10.1016/s0165-3806(99)00052-8 · Cited by 19
Nagy, J. I., & Rash, J. E. (2017) · European Journal of Neuroscience · doi:10.1111/ejn.13614 · Cited by 19
“…localization of Cx45-puncta to Bergmann glial cell processes, together with previous reports showing the association of Cx43 with these processes (Yamamoto et al., 1990a,b, 1992), prompted © 2017 Federation of European Neuroscience Societies and John Wiley & Sons Ltd European Journal of…”
BackgroundInfluentialSelf-citationSituation-Based Neuromorphic Memory in Spiking Neuron-Astrocyte Network
Gordleeva, S., Tsybina, Y., Krivonosov, M., Tyukin, I., Kazantsev, V., Zaikin, A. A., & Gorban, A. N. (2023) · IEEE Transactions on Neural Networks and Learning Systems · doi:10.1109/tnnls.2023.3335450 · Cited by 18
“Gap junctions are permeable to the second messenger IP 3 and to calcium ions [46], [47].”
Proximity of excitatory synapses and astroglial gap junctions in layer IV of the mouse barrel cortex
Genoud, C., Houades, V., Kraftsik, R., Welker, E., & Giaume, C. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.01.051 · Cited by 18
“(Yamamoto et al., 1990).”
General anesthetics attenuate gap junction coupling in P19 cell line
Wentlandt, K., Carlen, P. L., Kushnir, M., Naus, C. C. G., & El‐Beheiry, H. (2005) · Journal of Neuroscience Research · doi:10.1002/jnr.20577 · Cited by 18
“First, in contrast to astrocytic gap junctions, which are predominantly made up of connexin43 (Yamamoto et al., 1990; Hofer and Dermietzel, 1998), the P19 cells used in this study express several other gap junction proteins that are identified in mammalian central neurons, i.”
BackgroundGap junction proteins in inhibitory neurons of the adult barrel neocortex
Priest, A. J. T. C. A. (2001) · Somatosensory & Motor Research · doi:10.1080/01421590120089631 · Cited by 18
Postnatal development of GFAP, connexin43 and connexin30 in cat visual cortex.
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Affinity purification of a rat‐brain junctional protein, connexin 43
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InfluentialCyclooxygenase inhibitor induces the upregulation of connexin-43 expression in C6 glioma cells
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Effect of Gap Junctional Communication on Glioma Cell Function
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Metadata
- 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.
- 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
- 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
- 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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