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01-10-2006 | Original Article

Glial cytoarchitecture in the central nervous system of the soft-shell turtle, Trionyx sinensis, revealed by intermediate filament immunohistochemistry

Authors: Maurizio Lazzari, Valeria Franceschini

Published in: Brain Structure and Function | Issue 5/2006

Abstract

The distribution of the intermediate filament molecular markers, glial fibrillary acidic protein (GFAP) and vimentin, has been studied in the central nervous system (CNS) of the soft-shell turtle (Trionyx sinensis) with immunoperoxidase histochemistry. GFAP immunohistochemistry pointed out the presence of different astroglial cell types. The brain pattern consists of ependymal radial glia whose cell bodies are located in the ependymal layer throughout the brain ventricular system. In the spinal cord, the ependyma is immunonegative, whereas positive radial astrocyte cell bodies are displaced from the ependyma into the periependymal position. Star-shaped astrocytes are observed only in the posterior intumescence of the spinal cord. The different regions of the CNS show a different intensity in GFAP immunostaining even in the same cellular type. Vimentin-immunoreactive structures are absent in the brain and spinal cord. The present study reports an heterogeneous feature of the astroglial pattern in the spinal cord compared to the brain which shows an ancestral condition.

Adams JC (1981) Heavy-metal intensification of DAB-based reaction product. J Histochem Cytochem 29:775PubMed

Benediktsson AM, Schachtele SJ, Green SH, Dailey ME (2005) Ballistic labeling and dynamic imaging of astrocytes in organotypic hippocampal slice cultures. J Neurosci Methods 141:41–53PubMedCrossRef

Bignami A, Dahl D, Rueger DC (1980) Glial fibrillary acidic protein (GFAP) in normal cells and in pathological conditions. Adv Cell Neurobiol 1:285–310

Bodega G, Suarez I, Rubio M, Fernandez B (1994) Ependyma: phylogenetic evolution of glial fibrillary acidic protein (GFAP) and vimentin expression in vertebrate spinal cord. Histochemistry 102:113–122PubMedCrossRef

Butler AB, Hodos W (2005) Vertebrate neuroanatomy. Evolution and adaptation, 2nd edn. Wiley, New York, Chichester, Brisbane, Toronto, Singapore

Cardone B, Roots BJ (1990) Comparative immunohistochemical study of glial filament proteins (glial fibrillary acidic protein and vimentin) in goldfish, octopus and snail. Glia 3:180–192PubMedCrossRef

Dahl D (1976) Isolation and initial characterization of glial fibrillary acidic protein from chicken, turtle, frog, and fish central nervous system. Acta Biochim Biophys 446:41–50

Dahl D, Bignami A (1973) Immunohistochemical and immunofluorescence studies of the glial fibrillary acidic protein in vertebrates. Brain Res 61:279–283PubMedCrossRef

Dahl D, Bignami A (1985) Intermediate filaments in nervous tissue. In: Shay JW (ed) Cell and muscle motility, vol 6. Plenum Press, New York, pp 75–96

Dahl D, Rueger DC, Bignami A, Weber K, Osborn M (1981) Vimentin, the 57,000 molecular weight protein in fibroblast filaments in the major cytoskeletal protein in immature glia. Eur J Cell Biol 24:191–196PubMed

Dahl D, Strocchi P, Bignami A (1982) Vimentin in the central nervous system. A study of the mesenchymal-type intermediate filament-protein in Wallerian degeneration and in postnatal rat development by two-dimensional gel electrophoresis. Differentiation 22:185–190PubMedCrossRef

Dahl D, Crosby CJ, Sethi JS, Bignami A (1985) Glial fibrillary acidic (GFA) protein in vertebrates: immunofluorescence and immunoblotting study with monoclonal and polyclonal antibodies. J Comp Neurol 239:75–88PubMedCrossRef

Ebner FF, Colonnier M (1975) Synaptic patterns in the visual cortex of turtle: an electron microscopic study. J Comp Neurol 160:51–80PubMedCrossRef

Eliasson C, Sahlgren C, Berthold CH, Stakeberg J, Celis JE, Betsholtz C, Eriksson JE, Pekny M (1999) Intermediate filament protein partnership in astrocytes. J Biol Chem 274:23996–24006PubMedCrossRef

Elmquist JK, Swanson JJ, Sakaguchi DS, Ross LR, Jacobson CD (1994) Developmental distribution of GFAP and vimentin in the Brazilian opossum brain. J Comp Neurol 344:283–296PubMedCrossRef

Hajos F, Kalman M (1989) Distribution of glial fibrillary acidic protein (GFAP)-immunoreactive astrocytes in the rat brain. II. Mesencephalon, rhombencephalon and spinal cord. Exp Brain Res 78:164–173PubMedCrossRef

Hedges BS, Poling LL (1999) A molecular phylogeny of reptiles. Science 283:1–7CrossRef

Hirrlinger J, Hulsmann S, Kirchoff F (2004) Astroglial processes show spontaneous motility at active synaptic terminals in situ. Eur J Neurosci 20:2235–2239PubMedCrossRef

Iwabe N, Hara Y, Shibamoto K, Saito Y, Mivata T, Katoh K (2005) Sister group relationship of turtles to the bird-crocodilian clade revealed by nuclear DNA-coded proteins. Mol Biol Evol 22:810–813PubMedCrossRef

Kalman M (1998) Astroglial architecture of the carp (Cyprinus carpio) brain as revealed by immunocytochemical staining against glial fibrillary acidic protein (GFAP). Anat Embryol 198:409–433PubMedCrossRef

Kalman M, Pritz MB (2001) Glial fibrillary acidic protein-immunopositive structures in the brain of a crocodilian, Caiman crocodilus, and its bearing on the evolution of astroglia. J Comp Neurol 431:460–480PubMedCrossRef

Kalman M, Szekely A, Csillag A (1993a) GFAP and vimentin in the developing chicken brain. Anat Anz (Suppl) 175:130–131

Kalman M, Szekely A, Csillag A (1993b) Distribution of glial fibrillary acidic protein-immunoreactive structures in the brain of the domestic chicken (Gallus domesticus). J Comp Neurol 330:221–237PubMedCrossRef

Kalman M, Kiss A, Majorossy K (1994) Distribution of glial fibrillary acidic protein-immunopositive structures in the brain of the red-eared freshwater turtle (Pseudemys scripta elegans). Anat Embryol 189:421–434PubMedCrossRef

Kalman M, Kiss A, Majorossy K (1995) Vimentin-immunopositive structures in the brain of the adult turtle Pseudemys scripta elegans. Ann Anat (Suppl) 177:195

Kalman M, Martin-Partido G, Hidalgo-Sanchez M, Majorossy K (1997) Distribution of glial fibrillary acidic protein–immunopositive structures in the developing brain of the turtle Mauremys leprosa. Anat Embryol 196:47–65PubMedCrossRef

Kalman M, Szekely AD, Csillag A (1998) Distribution of glial fibrillary acidic protein and vimentin-immunopositive elements in the developing chicken brain from hatch to adulthood. Anat Embryol 198:213–235PubMedCrossRef

Krenz JG, Naylor GJP, Shaffer HB, Janzen FJ (2005) Molecular phylogenetics and evolution of turtles. Mol Phylogenet Evol 37:178–191PubMedCrossRef

Kriegstein AR, Shen JM, Eshbar N (1986) Monoclonal antibodies to the turtle cortex reveal neuronal subsets, antigenic cross-reactivity with the mammalian neocortex, and forebrain structures sharing a pallial derivation. J Comp Neurol 254:330–340PubMedCrossRef

Lazzari M, Franceschini V (2001) Glial fibrillary acidic protein and vimentin immunoreactivity of astroglial cells in the central nervous system of adult Podarcis sicula (Squamata, Lacertidae). J Anat 198:67–75PubMedCrossRef

Lazzari M, Franceschini V (2004) Glial fibrillary acidic protein and vimentin immunoreactivity of astroglial cells in the central nervous system of the African lungfish, Protopterus annectens (Dipnoi: Lepidosirenidae). J Morphol 262:741–749PubMedCrossRef

Lazzari M, Franceschini V (2005a) Intermediate filament immunohistochemistry of astroglial cells in the leopard gecko, Eublepharis macularius. Anat Embryol 210:275–286PubMedCrossRef

Lazzari M, Franceschini V (2005b) Astroglial cells in the central nervous system of the Brown Anole Lizard, Anolis sagrei, revealed by intermediate filament immunohistochemistry. J Morphol 265:325–334PubMedCrossRef

Lazzari M, Franceschini V, Ciani F (1997) Glial fibrillary acidic protein and vimentin in radial glia of Ambystoma mexicanum and Triturus carnifex: an immunocytochemical study. J Brain Res 38:187–194

Levitt P, Rakic P (1980) Immunoperoxidase localization of glial fibrillary acidic protein in radial glial cells and astrocytes of the developing Rhesus monkey brain. J Comp Neurol 193:815–840PubMedCrossRef

Mannen H, Li SS (1999) Molecular evidence for a clade of turtles. Mol Phylogen Evol 13:144–148CrossRef

Matsuda Y, Nishida-Umehara C, Tarui H, Kuroiwa A, Yamada K, Isobe T, Ando J, Fujiwara A, Hirao Y, Nishimura O, Ishijima J, Hayashi A, Saito T, Murakami T, Kuratani S, Agata K (2005) Highly conserved linkage homology between birds and turtles: bird and turtle chromosomes are precise counterparts of each other. Chromosome Res 13:601–615PubMedCrossRef

Monzon-Mayor M, Yanes C, Ghandour MS, de Barry J, Gombos G (1990) Glial fibrillary acidic protein and vimentin immunohistochemistry in the developing and adult midbrain of the lizard Gallotia galloti. J Comp Neurol 295:569–579PubMedCrossRef

Monzon-Mayor M, Yanes C, De Barry J, Capdevilla-Carbonell C, Renau-Piqueras J, Tholey G, Gombos G (1998) Heterogeneous immunoreactivity in glial cells in the mesencephalon of a lizard: a double labelling immunohistochemical study. J Morphol 235:109–119PubMedCrossRef

Mulligan SJ, MacVicar BA (2004) Calcium transients in astrocyte endfeet cause cerebrovascular constrictions. Nature 431:195–199PubMedCrossRef

Onteniente B, Kimura H, Maeda T (1983) Comparative study of the glial fibrillary acidic protein in vertebrates by PAP immunohistochemistry. J Comp Neurol 215:427–436PubMedCrossRef

Pixley SK, de Vellis J (1984) Transition between immature radial glia and mature astrocytes studied with a monoclonal antibody to vimentin. Brain Res 317:201–209PubMed

Rieppel O, deBraga M (1996) Turtle as diapsid reptiles. Nature 384:453–455CrossRef

Roots BI (1986) Phylogenetic development of astrocytes. In: Vernadakis A, Fedoroff S (eds) Astrocytes. Academic, Orlando, pp 1–34

Rubio M, Suarez I, Bodega G, Fernandez B (1992) Glial fibrillary acidic protein and vimentin immunohistochemistry in the posterior rhombencephalon of the Iberian barb (Barbus comiza). Neurosci Lett 134:203–206PubMedCrossRef

Schmechel DE, Rakic P (1979) A Golgi study of radial glial cells in developing monkey telencephalon: morphogenesis and transformation into astrocytes. Anat Embryol 156:115–152PubMedCrossRef

Simard M, Arcuino G, Takano T, Liu OS, Nedergaard M (2003) Signaling at the glio–vascular interface. J Neurosci 23:9254–9262PubMed

Stensaas LJ, Stensaas SS (1968) Light microscopy of glial cells in turtles and birds. Z Zellforsch Mikrosk Anat 91:315–340PubMedCrossRef

Szaro BG, Gainer H (1988) Immunocytochemical identification of non-neuronal intermediate filament proteins in the developing Xenopus laevis nervous system. Dev Brain Res 43:207–224CrossRef

Volterra A, Meldolesi J (2005) Astrocytes, from brain glue to communication elements: the revolution continues. Nat Rev Neurosci 6:626–640PubMedCrossRef

Yanes C, Monzon-Mayor M, Ghandour MS, de Barry J, Gombos G (1990) Radial glia and astrocytes in developing and adult telencephalon of the lizard Gallotia galloti as revealed by immunohistochemistry with anti-GFAP and anti-vimentin antibodies. J Comp Neurol 295:559–568PubMedCrossRef

Zamora AJ, Mutin M (1988) Vimentin and glial fibrillary acidic protein filaments in radial glia of the adult urodele spinal cord. Neurosci 27:279–288CrossRef

Zardoya R, Meyer A (1998) Complete mitochondrial genome suggests diapsid affinities of turtles. Proc Natl Acad Sci USA 95:14226–14231PubMedCrossRef

Zardoya R, Meyer A (2001) The evolutionary position of turtles revised. Naturwissenschaften 88:193–200PubMedCrossRef

Title: Glial cytoarchitecture in the central nervous system of the soft-shell turtle, Trionyx sinensis, revealed by intermediate filament immunohistochemistry
Authors: Maurizio Lazzari
Valeria Franceschini
Publication date: 01-10-2006
Publisher: Springer-Verlag
Published in: Brain Structure and Function / Issue 5/2006
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-006-0101-5

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Glial cytoarchitecture in the central nervous system of the soft-shell turtle, Trionyx sinensis, revealed by intermediate filament immunohistochemistry

Abstract

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Abstract

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