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GFAP expression withdraws—a trend of glial evolution?
Brain Research Bulletin, Vol. 57, Nos. 3/4, pp. 509 –511, 2002 Copyright © 2002 Elsevier Science Inc. Printed in the USA. All rights reserved 0361-9230/02/$–see front matter
PII S0361-9230(01)00713-4
GFAP expression withdraws—a trend of glial evolution? Miha´ly Ka´lma´n* Department of Anatomy, Histology and Embryology, Semmelweis University, Budapest, Hungary ABSTRACT: This study is a summary of investigations in the last decade with several collaborators on representatives of different vertebrate stocks. The results suggest that in the main vertebrate stocks (Agnathi, Chondrichthyes, Actinopterygii, Sarcopterygii-Amniotes), which had their parallel brain evolutions from the laminar brains to the elaborated ones, the astroglia also developed in parallel, and had a common trend of evolution. With growing brain complexity, free astrocytes arose and tended to predominate, and the spontaneous glial fibrillary acidic protein (GFAP)-expression regressed, in several areas. In the mammalian, avian, teleost, and batoid brains, therefore, large areas display a paucity, almost a lack of GFAP-immunoreactivity. The GFAPexpression in the GFAP-free areas seems to be inducible only in the presence of free astrocytes. © 2002 Elsevier Science Inc. KEY WORDS: Astroglia, Astrocytes, Chondrichthyes, Teleostei, Turtle, Crocodile.
INTRODUCTION
FIG. 1. Uneven distribution of GFAP in the rat brain. GP, globus pallidus; CPu, caudate-putamen complex. Scale bar: 100 m.
This study is a summary of investigations in the last decade with several collaborators on representatives of different vertebrate stocks: rat [4,9,18], chicken [13], finch (unpublished), Pseudemys scripta elegans and Mauremys leprosa turtles (Anapsida, [10,12]), Caiman crocodilus (Diapsida, Archosauria, [11]), Cyprinus carpio and Carassius aureatus (Teleostei, [5,6]), Acipenser ruthenus (Ganoidei, Chondrostei, unpublished), Squalus acanthias (a squalomorph shark), and Raia erinacea and Dasyatis pastinaca (skates, Batoidei, Chondrichthyes, [7,8]). The immunohistochemical staining of neuroglial glial fibrillary acidic protein (GFAP) was performed on floating Vibratome sections, with mouse monoclonal antibodies produced against porcine GFAP (Boehringer, Mannheim, Germany) according to the avidin– biotin method. In accordance with other authors [2,3,15], the anti-mammalian GFAP antibodies produced a sensitive cross-reaction with the GFAP of other vertebrates. In the representatives of mammals and birds, large brain areas displayed a paucity, almost a lack of GFAP-immunoreactivity (e.g., striatum and tectum in mammals, neostriatum, paleostriatum augmentatum, and the superficial zone of tectum in birds), despite the rich GFAP-content of the adjacent areas (Figs. 1 and 2). In these animals, astrocytes were the most abundant form of astroglia. On the other hand, the turtles studied had an approximately even distribution of GFAP-im-
munoreactive structures, except for the largest brain tracts. The radial ependymoglia was the most abundant astroglia, and no free astrocytes (free stellate shaped cells) were seen. Caiman, the closest relative of birds among the animals investigated, had an intermediate position. Although the caiman brain displayed a variety in the intensity of GFAP immunostaining (mainly in the dorsal ventricular ridge and in the brain stem nuclei), no areas lacked GFAP, and whereas astrocytes occurred widely, they were not predominant. It is noteworthy that MonzonMayor et al. [14] and Yanes et al. [17] did not detect considerable regional differences of GFAP immunostaining in a lizard (Gallotia galloti, a diapsid reptile, but a lepidosaur, not an archosaur), in which free astrocytes were confined to some mesencephalic regions. The squalomorph shark brain had ependymoglia, but no free astrocytes, and an approximately even distribution of GFAPimmunopositivity (Fig. 3). In the skate brains, however, large areas displayed a paucity, almost a lack of GFAP-immunopositivity. GFAP-immunopositive astrocytes were numerous but confined to the vicinity of blood vessels, the meningeal surface, and some diencephalic and mesencephalic regions (Fig. 4).
* Address for correspondence: Dr. Miha´ly Ka´lma´n, Department of Anatomy, Histology and Embryology, Semmelweis University, Tu¨zolto´ 58, Budapest, H-1094 Hungary. Fax: 36-1-215-5158; E-mail: [email protected]
509
´ LMA ´N KA
510
FIG. 2. Different GFAP-expression in chicken in the paleostriatum augmentatum and primitivum (PA and PP, respectively). V, lateral ventricle. Scale bar: 50 m.
Ependymoglial fibers were scarce. However, it is to be noted that glutamine synthetase and S-100b protein proved to be proper astroglial markers in cartilaginous and bony fishes, like in mammals and birds, and revealed several astroglial structures in the GFAP-free areas [7]. In the teleost fishes, ependymoglia was ubiquitous, but limited brain areas lacked GFAP-immunopositivity; the largest of them was the zone of sensory neurons in the vagal lobe. In this area, however, GFAP-expression could not be induced even by a lesion [6], in contrast to findings in mammals, and also in birds. In the chondrostean fish Acipenser, the corresponding areas were poor but not devoid of GFAP (Figs. 5 and 6). In addition, Wicht et al. [16] demonstrated that the brain of the pacific hagfish (Eptatretus stouti, a myxiniform agnathan) contains GFAP-immunoreactive astrocyte-like structures, which are not found in lampreys (petromyzoniform agnathans). The results suggest that in the main vertebrate stocks (Ag-
FIG. 3. Squalus. Evenly distributed ependymoglia in the brain of Squalus. Scale bar: 90 m.
FIG. 4. Telencephalon of Raia. The GFAP immunoreactivity is confined to the periventricular ependymoglia and the perivascular and submeningeal astrocytes (arrowheads). X16. V, lateral ventricle. Inset: astrocytes. Scale bar: 300 m; for the inset: 30 m.
nathi, Chondrichthyes, Actinopterygii, Sarcopterygii-Amniotes), which had their parallel brain evolutions from the laminar to the elaborated forms [1], the astroglia also developed in parallel, and had a common trend of evolution. With growing brain complexity, free astrocytes arose and tended to predominate, and the spontaneous GFAP-expression regressed in several areas. The inducible GFAP-expression in the GFAP-free areas seems to be astrocyte-dependent. REFERENCES 1. Butler, A. B.; Hodos, W. Comparative vertebrate neuroanatomy. Evolution and adaption. New York: Wiley; 1996. 2. Dahl, D.; Bignami, A. Immunohistochemical and immunofluorescence studies of the glial fibrillary acidic protein in vertebrates. Brain Res. 61:279 –283; 1973.
FIG. 5. Vagal lobe of Acipenser. The layer system is less complex than in Cyprinus, and no layer is devoid of GFAP. E, ependymal surface. Scale bar: 80 m.
GFAP: EVOLUTIONARY TRENDS
FIG. 6. Vagal lobe of Cyprinus. Fe, zone of external (capsular) fibers; S, zone of sensory neurons; Fi, zone of inner fibers; M, zone of motoric neurons; E, ependyma. Note the areas devoid of GFAP. Scale bar: 200 m.
3. Dahl, D.; Crosby, C. J.; Sethi, A.; Bignami, A. Glial fibrillary acidic (GFA) protein in vertebrates: Immunofluores-cence and immunoblotting study with monoclonal and polyclonal antibodies. J. Comp. Neurol. 239:75– 88; 1985. 4. Hajo´ s, F.; Ka´ lma´ n, M. Distribution of glial fibrillary acidic protein (GFAP)-immunoreactive astrocytes in the rat brain. II. Mesencephalon, rhombencephalon and spinal cord. Exp. Brain Res. 78:164 –173; 1989. 5. Ka´ lma´ n, M. Astroglial architecture of the carp (Cyprinus carpio) brain as revealed by immunohistochemical staining against glial fibrillary acidic protein (GFAP). Anat. Embryol. 198:409 – 433; 1998. 6. Ka´ lma´ n, M.; Ajtai, B. M. Lesions do not provoke GFAP-expression in the GFAP-immunonegative areas of the teleost brain. Ann. Anat. 182:459 – 463; 2000. 7. Ka´ lma´ n, M.; Ari, C. Comparative study on astroglial markers, GFAP, glutamine synthetase and S-100 in skate brain. Ann. Anat. 183(suppl.): 104; 2001.
511 8. Ka´ lma´ n, M.; Gould, R. M. GFAP immunopositive structures in spiny dogfish, Squalus acanthias, and little skate, Raia erinacea, brains: Differences have evolutionary implications. Anat. Embryol. 204:59 – 80; 2001. 9. Ka´ lma´ n, M.; Hajo´ s, F. Distribution of glial fibrillary acidic protein (GFAP)-immunoreactive astrocytes in the rat brain. I. Forebrain. Exp. Brain Res. 78:147–163; 1989. ´ .; Majorossy, K. Distribution of glial fibrillary 10. Ka´ lma´ n, M.; Kiss, A acidic protein-immunopositive structures in the brain of the red-eared freshwater turtle (Pseudemys scripta elegans). Anat. Embryol. 189: 421– 434; 1994. 11. Ka´ lma´ n, M.; Pritz, M. B. 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 – 480; 2001. 12. Ka´ lma´ n, M.; Martin-Partido, G.; Hidalgo-Sanchez, M.; Majorossy, K. Distribution of glial fibrillary acidic protein-immunopositive structures in the developing brain of the turtle Mauremys leprosa. Anat. Embryol. 196:47– 65; 1997. 13. Ka´ lma´ n, M.; Sze´ kely, A.; Csillag, A. Distribution of glial fibrillary acidic protein-immunopositive structures in the brain of the domestic chicken (Gallus domesticus). J. Comp. Neurol. 330:221–237; 1993. 14. Monzon-Mayor, M.; Yanes, C.; Tholey, G.; de Barry, J.; Gombos, G. Glial fibrillary acidic protein and vimentin immunohistochemistry in the developing and adult midbrain of the lizard Gallotia galloti. J. Comp. Neurol. 295:569 –579; 1990. 15. Onteniente, B.; Kimura, H.; Maeda, T. Comparative study of the glial fibrillary acidic protein in vertebrates by PAP immunohistochemistry. J. Comp. Neurol. 215:427– 436; 1983. 16. Wicht, H.; Derouiche, A.; Korf, H. W. An immunocytochemical investigation of glial morphology in the Pacific hagfish: Radial and astrocyte-like glia have the same phylogenetic age. J. Neurocytol. 23:565–576; 1994. 17. Yanes, C.; Monzon-Mayor, M.; Ghandour, M. S.; de Barry, J.; Gombos, G. Radial glia and astrocytes in the adult and developing telencephalon of the lizard Gallotia galloti as revealed by immunohistochemistry with anti-GFAP and anti-vimentin antibodies. J. Comp. Neurol. 295:559 –568; 1990. 18. Zilles, K.; Hajo´ s, F.; Ka´ lma´ n, M.; Schleicher, A. Mapping of glial fibrillary acidic protein (GFAP) immunoreactivity in the rat forebrain and mesencephalon by computerized image analysis. J. Comp. Neurol. 308:340 –355; 1991.
PII S0361-9230(01)00713-4
GFAP expression withdraws—a trend of glial evolution? Miha´ly Ka´lma´n* Department of Anatomy, Histology and Embryology, Semmelweis University, Budapest, Hungary ABSTRACT: This study is a summary of investigations in the last decade with several collaborators on representatives of different vertebrate stocks. The results suggest that in the main vertebrate stocks (Agnathi, Chondrichthyes, Actinopterygii, Sarcopterygii-Amniotes), which had their parallel brain evolutions from the laminar brains to the elaborated ones, the astroglia also developed in parallel, and had a common trend of evolution. With growing brain complexity, free astrocytes arose and tended to predominate, and the spontaneous glial fibrillary acidic protein (GFAP)-expression regressed, in several areas. In the mammalian, avian, teleost, and batoid brains, therefore, large areas display a paucity, almost a lack of GFAP-immunoreactivity. The GFAPexpression in the GFAP-free areas seems to be inducible only in the presence of free astrocytes. © 2002 Elsevier Science Inc. KEY WORDS: Astroglia, Astrocytes, Chondrichthyes, Teleostei, Turtle, Crocodile.
INTRODUCTION
FIG. 1. Uneven distribution of GFAP in the rat brain. GP, globus pallidus; CPu, caudate-putamen complex. Scale bar: 100 m.
This study is a summary of investigations in the last decade with several collaborators on representatives of different vertebrate stocks: rat [4,9,18], chicken [13], finch (unpublished), Pseudemys scripta elegans and Mauremys leprosa turtles (Anapsida, [10,12]), Caiman crocodilus (Diapsida, Archosauria, [11]), Cyprinus carpio and Carassius aureatus (Teleostei, [5,6]), Acipenser ruthenus (Ganoidei, Chondrostei, unpublished), Squalus acanthias (a squalomorph shark), and Raia erinacea and Dasyatis pastinaca (skates, Batoidei, Chondrichthyes, [7,8]). The immunohistochemical staining of neuroglial glial fibrillary acidic protein (GFAP) was performed on floating Vibratome sections, with mouse monoclonal antibodies produced against porcine GFAP (Boehringer, Mannheim, Germany) according to the avidin– biotin method. In accordance with other authors [2,3,15], the anti-mammalian GFAP antibodies produced a sensitive cross-reaction with the GFAP of other vertebrates. In the representatives of mammals and birds, large brain areas displayed a paucity, almost a lack of GFAP-immunoreactivity (e.g., striatum and tectum in mammals, neostriatum, paleostriatum augmentatum, and the superficial zone of tectum in birds), despite the rich GFAP-content of the adjacent areas (Figs. 1 and 2). In these animals, astrocytes were the most abundant form of astroglia. On the other hand, the turtles studied had an approximately even distribution of GFAP-im-
munoreactive structures, except for the largest brain tracts. The radial ependymoglia was the most abundant astroglia, and no free astrocytes (free stellate shaped cells) were seen. Caiman, the closest relative of birds among the animals investigated, had an intermediate position. Although the caiman brain displayed a variety in the intensity of GFAP immunostaining (mainly in the dorsal ventricular ridge and in the brain stem nuclei), no areas lacked GFAP, and whereas astrocytes occurred widely, they were not predominant. It is noteworthy that MonzonMayor et al. [14] and Yanes et al. [17] did not detect considerable regional differences of GFAP immunostaining in a lizard (Gallotia galloti, a diapsid reptile, but a lepidosaur, not an archosaur), in which free astrocytes were confined to some mesencephalic regions. The squalomorph shark brain had ependymoglia, but no free astrocytes, and an approximately even distribution of GFAPimmunopositivity (Fig. 3). In the skate brains, however, large areas displayed a paucity, almost a lack of GFAP-immunopositivity. GFAP-immunopositive astrocytes were numerous but confined to the vicinity of blood vessels, the meningeal surface, and some diencephalic and mesencephalic regions (Fig. 4).
* Address for correspondence: Dr. Miha´ly Ka´lma´n, Department of Anatomy, Histology and Embryology, Semmelweis University, Tu¨zolto´ 58, Budapest, H-1094 Hungary. Fax: 36-1-215-5158; E-mail: [email protected]
509
´ LMA ´N KA
510
FIG. 2. Different GFAP-expression in chicken in the paleostriatum augmentatum and primitivum (PA and PP, respectively). V, lateral ventricle. Scale bar: 50 m.
Ependymoglial fibers were scarce. However, it is to be noted that glutamine synthetase and S-100b protein proved to be proper astroglial markers in cartilaginous and bony fishes, like in mammals and birds, and revealed several astroglial structures in the GFAP-free areas [7]. In the teleost fishes, ependymoglia was ubiquitous, but limited brain areas lacked GFAP-immunopositivity; the largest of them was the zone of sensory neurons in the vagal lobe. In this area, however, GFAP-expression could not be induced even by a lesion [6], in contrast to findings in mammals, and also in birds. In the chondrostean fish Acipenser, the corresponding areas were poor but not devoid of GFAP (Figs. 5 and 6). In addition, Wicht et al. [16] demonstrated that the brain of the pacific hagfish (Eptatretus stouti, a myxiniform agnathan) contains GFAP-immunoreactive astrocyte-like structures, which are not found in lampreys (petromyzoniform agnathans). The results suggest that in the main vertebrate stocks (Ag-
FIG. 3. Squalus. Evenly distributed ependymoglia in the brain of Squalus. Scale bar: 90 m.
FIG. 4. Telencephalon of Raia. The GFAP immunoreactivity is confined to the periventricular ependymoglia and the perivascular and submeningeal astrocytes (arrowheads). X16. V, lateral ventricle. Inset: astrocytes. Scale bar: 300 m; for the inset: 30 m.
nathi, Chondrichthyes, Actinopterygii, Sarcopterygii-Amniotes), which had their parallel brain evolutions from the laminar to the elaborated forms [1], the astroglia also developed in parallel, and had a common trend of evolution. With growing brain complexity, free astrocytes arose and tended to predominate, and the spontaneous GFAP-expression regressed in several areas. The inducible GFAP-expression in the GFAP-free areas seems to be astrocyte-dependent. REFERENCES 1. Butler, A. B.; Hodos, W. Comparative vertebrate neuroanatomy. Evolution and adaption. New York: Wiley; 1996. 2. Dahl, D.; Bignami, A. Immunohistochemical and immunofluorescence studies of the glial fibrillary acidic protein in vertebrates. Brain Res. 61:279 –283; 1973.
FIG. 5. Vagal lobe of Acipenser. The layer system is less complex than in Cyprinus, and no layer is devoid of GFAP. E, ependymal surface. Scale bar: 80 m.
GFAP: EVOLUTIONARY TRENDS
FIG. 6. Vagal lobe of Cyprinus. Fe, zone of external (capsular) fibers; S, zone of sensory neurons; Fi, zone of inner fibers; M, zone of motoric neurons; E, ependyma. Note the areas devoid of GFAP. Scale bar: 200 m.
3. Dahl, D.; Crosby, C. J.; Sethi, A.; Bignami, A. Glial fibrillary acidic (GFA) protein in vertebrates: Immunofluores-cence and immunoblotting study with monoclonal and polyclonal antibodies. J. Comp. Neurol. 239:75– 88; 1985. 4. Hajo´ s, F.; Ka´ lma´ n, M. Distribution of glial fibrillary acidic protein (GFAP)-immunoreactive astrocytes in the rat brain. II. Mesencephalon, rhombencephalon and spinal cord. Exp. Brain Res. 78:164 –173; 1989. 5. Ka´ lma´ n, M. Astroglial architecture of the carp (Cyprinus carpio) brain as revealed by immunohistochemical staining against glial fibrillary acidic protein (GFAP). Anat. Embryol. 198:409 – 433; 1998. 6. Ka´ lma´ n, M.; Ajtai, B. M. Lesions do not provoke GFAP-expression in the GFAP-immunonegative areas of the teleost brain. Ann. Anat. 182:459 – 463; 2000. 7. Ka´ lma´ n, M.; Ari, C. Comparative study on astroglial markers, GFAP, glutamine synthetase and S-100 in skate brain. Ann. Anat. 183(suppl.): 104; 2001.
511 8. Ka´ lma´ n, M.; Gould, R. M. GFAP immunopositive structures in spiny dogfish, Squalus acanthias, and little skate, Raia erinacea, brains: Differences have evolutionary implications. Anat. Embryol. 204:59 – 80; 2001. 9. Ka´ lma´ n, M.; Hajo´ s, F. Distribution of glial fibrillary acidic protein (GFAP)-immunoreactive astrocytes in the rat brain. I. Forebrain. Exp. Brain Res. 78:147–163; 1989. ´ .; Majorossy, K. Distribution of glial fibrillary 10. Ka´ lma´ n, M.; Kiss, A acidic protein-immunopositive structures in the brain of the red-eared freshwater turtle (Pseudemys scripta elegans). Anat. Embryol. 189: 421– 434; 1994. 11. Ka´ lma´ n, M.; Pritz, M. B. 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 – 480; 2001. 12. Ka´ lma´ n, M.; Martin-Partido, G.; Hidalgo-Sanchez, M.; Majorossy, K. Distribution of glial fibrillary acidic protein-immunopositive structures in the developing brain of the turtle Mauremys leprosa. Anat. Embryol. 196:47– 65; 1997. 13. Ka´ lma´ n, M.; Sze´ kely, A.; Csillag, A. Distribution of glial fibrillary acidic protein-immunopositive structures in the brain of the domestic chicken (Gallus domesticus). J. Comp. Neurol. 330:221–237; 1993. 14. Monzon-Mayor, M.; Yanes, C.; Tholey, G.; de Barry, J.; Gombos, G. Glial fibrillary acidic protein and vimentin immunohistochemistry in the developing and adult midbrain of the lizard Gallotia galloti. J. Comp. Neurol. 295:569 –579; 1990. 15. Onteniente, B.; Kimura, H.; Maeda, T. Comparative study of the glial fibrillary acidic protein in vertebrates by PAP immunohistochemistry. J. Comp. Neurol. 215:427– 436; 1983. 16. Wicht, H.; Derouiche, A.; Korf, H. W. An immunocytochemical investigation of glial morphology in the Pacific hagfish: Radial and astrocyte-like glia have the same phylogenetic age. J. Neurocytol. 23:565–576; 1994. 17. Yanes, C.; Monzon-Mayor, M.; Ghandour, M. S.; de Barry, J.; Gombos, G. Radial glia and astrocytes in the adult and developing telencephalon of the lizard Gallotia galloti as revealed by immunohistochemistry with anti-GFAP and anti-vimentin antibodies. J. Comp. Neurol. 295:559 –568; 1990. 18. Zilles, K.; Hajo´ s, F.; Ka´ lma´ n, M.; Schleicher, A. Mapping of glial fibrillary acidic protein (GFAP) immunoreactivity in the rat forebrain and mesencephalon by computerized image analysis. J. Comp. Neurol. 308:340 –355; 1991.