Expression of a low-molecular weight (10 kDa) calcium binding protein in glial cells of the brain of the trout (Teleostei)

Anatomy and Embryology

Volumn 196, Issue 5, 1997, Pages 403-416

  Manso, Maria Jesús ^a   Becerra, Manuela ^a   Becerra, Manuel ^b   Anadón, Ramón ^b  

^a UNIVERSITY OF A CORUÑA   (Spain)

^b UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

Author keywords

Calbindin; Glia; Immunocytochemistry; NADPH diaphorase; Salmo trutta fario

Indexed keywords

CALBINDIN; CALCIUM BINDING PROTEIN; PROTEIN S 100;

ANIMAL TISSUE; ARTICLE; BRAIN; BRAIN STEM; GLIA CELL; HYPOTHALAMUS; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; NONHUMAN; OPTIC TECTUM; PRIORITY JOURNAL; RHOMBENCEPHALON; TELENCEPHALON; TROUT;

AGE FACTORS; ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODY SPECIFICITY; BIOLOGICAL MARKERS; BLOTTING, WESTERN; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CATTLE; CEREBELLUM; CHICKENS; DIENCEPHALON; EPENDYMA; GLIAL FIBRILLARY ACIDIC PROTEIN; IMMUNOHISTOCHEMISTRY; MEDULLA OBLONGATA; MESENCEPHALON; MOLECULAR WEIGHT; NADPH DEHYDROGENASE; NEUROGLIA; RATS; S100 PROTEINS; SPECIES SPECIFICITY; TROUT;

ANIMALIA; BOVINAE; SALMO; SALMO TRUTTA FARIO; SALMONIDAE; TELEOSTEI; VERTEBRATA;

EID: 0030694616     PISSN: 03402061     EISSN: None     Source Type: Journal    
DOI: 10.1007/s004290050108     Document Type: Article

References (81)

1. Achúcarro N (1915) De l'évolution de la névroglie, et spécialement de ses relations avec l'appareil vasculaire. Trab Lab Invest Biol 13:169-212
2. Andressen C, Blümke I, Celio MR (1993) Calcium-binding proteins: selective markers of nerve cells. Cell Tissue Res 271:181-208
3. Arévalo R, Alonso JR, Porteros A, Briñón JG, Crespo C, Lara J, Aijón J (1995) Calretinin-like immunoreactivity in the optic tectum of the tench (Tinea tinea L.). Brain Res 671:112-118
4. Benjelloun-Touimi S, Jacque CM, Derer P, De Vitry F, Maunoury R, Dupouey P (1985) Evidence that mouse astrocytes may be derived from the radial glia. An immunohistochemical study of the cerebellum in the normal and reeler mouse. J Neuroimmunol 9:87-97
5. Bergquist H (1932) Zur Morphologie des Zwischenhirns bei niederen Wirbeltieren. Acta Zool 13:53-303
6. Bignami A, Dahl D (1974) Astrocyte-specific protein and neuroglial differentiation. An immunofluorescent study with antibodies to the glial fibrillary acidic protein. J Comp Neurol 153:27-38
7. Bodega G, Fernández B, Suárez I, Gianonatti C (1988) Glioarchitecture de la moelle épinière du crapaud (Bufo bufo L.): étude au microscope optique avec des techniques d'impregnation métallique. Can J Zool 66:2415-2420
8. Bodega G, Suárez I, Fernández B (1990a) Radial astrocytes and ependymocytes in the spinal cord of the adult toad (Bufo bufo L.). Cell Tissue Res 260:307-314
9. Bodega G, Suárea I, Rubio M, Fernández B (1990b) Distribution and characteristics of the different astroglial cell types in the adult lizard (Lucerta lepida) spinal cord. Anal Embryol 181: 567-575
10. Bodega G, Suárez I, Oteruelo F, Fernández B, Gianonatti C (1990c) Ultrastructure of the subpial gliul limituns in the cerebellum of the lizard (Lacerta lepida). Anat Anz 171:153-158
11. Bodega G, Suárez I, Rubio M, Villalba RM, Fernández B (1993) Astroglial pattern in the spinal cord of the adult barbel (Karhua comiza). Anat Embryol 187:385-398
12. Bondareff W, McLone DG (1973) The external glial limiting membrane in macaca: ultrastructure of a laminated glioepithelium. Am J Anat 136:277-296
13. Braak E (1975) On the fine structure of the external glial layer in the isocortex of man. Cell Tissue Res 157:367-390
14. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254
15. Celio MR (1990) Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 35:375-475
16. Celio MR, Norman AW (1985) Nucleus basalis Meynert neurons contain the vitamin D-induced calcium-binding protein (Calbindin-D 28k). Anat Embryol 173:143-148
17. Celio MR, Baier W, Scharer L, Gregersen HJ, Viragh PA de, Norman AW (1990) Monoclonal antibodies directed against the calcium binding protein Calbindin D-28k. Cell Calcium 11:599-602
18. Chouaf L, Didier-Bazes M, Aguera M, Tardy M, Sallanon M, Kitahama K, Belin MF (1989) Comparative marker analysis of the ependymocytes of the subcommissural organ in four different mammalian species. Cell Tissue Res 257:255-262
19. Chouaf L, Didier-Bazes M, Tardy M, Aguera M, Fevre-Montange M, Voutsinos B, Belin MF (1991) Developmental expression of glial markers in ependymocytes of the rat subcommissural organ: role of the environment. Cell Tissue Res 266:553-561
20. Corujo A, Anadón R (1990) The development of the diencephalon of the rainbow trout (Salmo gairdneri). II. Thalamus and hypothalamus. J Hirnforsch 31:669-680
21. Corujo A, Rodriguez-Moldes I, Anadón R (1990) Light and ultrastructural study of the development of the saccus vasculosus in the rainbow trout. Oncorhynchus mykiss. J Morphol 206:79-93
22. Cuadrado MI (1992) Calbindin D-28 K in the nucleus pretectalis superficialis parvicellularis of Salmo gairdneri: an immunocytochemical study. Arch Ital Biol 130:11-18
23. Cuadrado MI (1993) Calbindin D-28 K immunoreactivity in the nucleus pretectalis superficialis magnocellularis of the rainbow trout (Salmo gairdneri, teleost). Arch Ital Biol 131:37-45
24. Dahl D (1976) Isolation and initial characterization of glial fibrillary acidic protein from chicken, turtle, frog and fish central nervous systems. Biochim Biophys Acta 446:41-50
25. 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 239:75-88
26. Dalil-Thiney N, Pochet R, Versaux-Botteri C, Vesselkin N, Reperant J, Nguyen-Legros J (1994) Immunohistochemical localization of calbindin-D28 K and calretinin in the lamprey retina. J Comp Neurol 340:140-147
27. De Leon M, Coveñas R, Narváez JA, Aguirre JA, González-Barón S (1994) Distribution of calbindin D-28k-immunoreactivity in the cat brainstem. Arch Ital Biol 132:229-241
28. Denizot JP, Bratton BO, Brehier A, Thomasset M (1988) Immunohistochemical demonstration of calbindin-D 28 K (CABP28 K) in the spinal cord motoneurons of teleost fish. Cell Tissue Res 254:629-634
29. Díaz-Regueira S, Alvarez-Otero R, Anadón R (1993) An immunocytochemical and ultrastructural study of a specialized glial layer of the medulla oblongata in a teleost, Chelon labrosus. Tissue Cell 25:657-668
30. Didier M, Harandi M, Aguera M, Bancel B, Tardy M, Fages C, Calas A, Stagaard M, Mollgard K, Belin MF (1986) Differential immunocytochemical staining for glial fibrillary acidic (GFA) protein, S-100 protein and glutamine synthetase in the rat subcommissural organ, nonspecialized ventricular ependyma and adjacent neuropil. Cell Tissue Res 245:343-351
31. Dyck RH, Van Eldik LJ, Cynader MS (1993) Immunohistochemical localization of the S-100 beta protein in postnatal cat visual cortex: spatial and temporal patterns of expression in cortical and subcortical glia. Brain Res Dev Brain Res 72:181-192
32. Enderlin S, Norman AW, Celio MR (1987) Ontogeny of the calcium binding protein calbindin D-28k in the rat nervous system. Anat Embryol 177:15-28
33. Engel AK, Müller CM (1989) Postnatal development of vimentinimmunoreactive radial glial cells in the primary visual cortex of the cat. J Neurocytol 18:437-450
34. Fedoroff S (1986) Prenatal ontogenesis of astrocytes. In: Fedoroff S, Vernadakis A (eds) Astrocytes. Cell biology and pathology of astrocytes, vol 1. Academic Press. Orlando, pp 35-74
35. Feldman SC, Christakos S (1983) Vitamin D-dependent calcium-binding protein in rat brain: biochemical and immunocytochemical characterization. Endocrinology 112:290-302
36. García-Segura LM, Baetens D, Roth J, Norman AW, Orci L (1984) Immunohistochemical mapping of calcium-binding protein immunoreactivity in the rat central nervous system. Brain Res 296:75-86
37. Gary KA, Chronwall BM (1995) Regulation of GFAP expression in glial-like cells of the rat pituitary intermediate lobe by lactation, salt-loading, and adrenalectomy. Glia 13:272-282
38. Gómez LA, Brusco A, Saavedra JP (1990) Immunocytochemical study of S-100 positive glial cells in the brainstem and spinal cord of the rat embryo. Int J Dev Neurosci 8:55-64
39. Hajós F, Kálmán M (1989) Distribution of glial fibrillary acidicprotein (GFAP)-immunoreactive astrocytes in the rat brain. II. Mesencephalon, rhombencephalon and spinal cord. Exp Brain Res 78:164-173
40. Hartesveldt C van, Moore B, Hartman BK (1986) Transient midline raphe glial structure in the developing rat. J Comp Neurol 253:174-184
41. Katsetos CD, Frankfurter A, Christakos S, Mancall EL, Vlachos IN, Urich H (1993) Differential localization of class III. betatubulin isotype and calbindin-D28k defines distinct neuronal types in the developing human cerebellar cortex. J Neuropathol Exp Neurol 52:655-666
42. Kranz D, Richter W (1970) Autoradiographische Untersuchungen über die Lokalisation der Matrixzonen des Diencephalons von juvenilen und adulten Lebistes reticulatus (Teleosteil. Z Mikrosk Anat Forsch 82:42-66
43. Landry CF, Ivy GO, Dunn RJ, Marks A, Brown IR (1989) Expression of the gene encoding the beta-subunit of S-100 protein in the developing rat brain analyzed by in situ hybridization. Brain Res Mol Brain Res 6:251-262
44. Lauriola L, Coli A, Cocchia D, Tallini G, Michetti F (1987) Comparative study by S-100 and GFAP immunohistochemistry of glial cell populations in the early stages of human spinal cord development. Brain Res 465:251-255
45. Leonhardt H (1980) Ependym und circumventriculäre Organe. In: Oksche A, Vollrath L (eds) Handbuch der mikroskopischen Anatomie des Menschen, vol 4/10. Neuroglia I. Springer, Berlin Heidelberg New York, pp 177-666
46. Linser PJ (1985) Multiple marker analysis in the avian optic tectum reveals three classes of neuroglia and carbonic anhydrasecontaining neurons. J Neurosci 5:2388-2396
47. Liu FC, Graybiel AM (1992) Transient calbindin-D28k-positive systems in the telencephalon: ganglionic eminence, developing striatum and cerebral cortex. J Neurosci 12:674-690
48. Losier BJ, Matsubara JA (1990) Comparison of calbindin D28k and cytochrome C oxidase in electrosensory nuclei of highland low-frequency weakly electric fish (Gymnotiformes). Cell Tissue Res 260:29-39
49. Ludwin SK, Kosek JC, Eng LF (1976) The topographical distribution of S-100 and GFA proteins in the adult rat brain: an immunohistochemical study using horseradish peroxidase-labelled antibodies. J Comp Neurol 165:197-207
50. Ma PM (1993) Tanycytes in the sunfish brain: NADPH-diaphorase histochemistry and regional distribution. J Comp Neurol 336:77-95
51. Maggs A, Scholes J (1986) Glial domains and nerve fiber patterns in the fish retinotectal pathway. J Neurosci 6:424-438
52. Maler L, Jande S, Lawson DEM (1984) Localization of vitamin D-dependent calcium binding protein in the electrosensory and electromotor system of high frequency gymnotid fish. Brain Res 301:166-170
53. McKanna JA (1993) Primitive glial compartments in the floor plate of mammalian embryos: distinct progenitors of adult astrocytes and microglia support the notoplate hypothesis. Perspect Dev Neurobiol 1:245-255
54. Müller CM (1992) Astrocytes in cat visual cortex studied by GFAP and S-100 immunocytochemistry during postnatal development. J Comp Neurol 317:309-323
55. Nona SN, Shehab SAS, Stafford CA, Cronly-Dillon JR (1989) Glial fibrillary acidic protein (GFAP) from goldfish: its location in visual pathway. Glia 2:189-200
56. Onteniente B, Kimura H, Maeda T (1983) Comparative study of the glial fibrillary acidic protein in vertebrates by PAP immunohistochemistry. J Comp Neurol 215:427-436
57. Parmentier M, Ghysens M, Rypens F, Lawson DE, Pasteeis JL, Pochet R (1987) Calbindin in vertebrate classes: immunohistochemical localization and Western blot analysis. Gen Comp Endocrinol 65:399-407
58. Pérez SE, Adrio F, Rodríguez MA, Rodníguez-Moldes I, Anadón R (1996) NADPH-diaphorase histochemistry reveals oligodendrocytes in the rainbow trout (teleosts). Neurosci Lett 205:1-4
59. Pfister C (1971) Elektive Darstellung der postembryonalen Matrixzonen im Gehirn von Lampetra planeri (Bloch) (Cyclostomata) und Salmo (Trutta) irideus (Teleostei) mit Pseudoisozyanin. Z Mikrosk Anat Forsch 84:286-292
60. Pochet R, Pasteels B, Seto-Ohshima A, Bastianelli E, Kitajima S, Van Eldik LJ (1991) Calmodulin and calbindin localization in retina from six vertebrate species. J Comp Neurol 314:750-762
61. Puelles L (1995) A segmental morphological paradigm for understanding vertebrate forebrains. Brain Behav Evol 46:319-337
62. Puelles L, Sánchez MP, Spreafico R, Fairén A (1992) Prenatal development of calbindin immunoreactivity in the dorsal thalamus of the rat. Neuroscience 46:135-147
63. Richter W, Heinrich D (1969) Über die postnatale mitotische Aktivität in einigen Matrixzonen des Diencephalons von Lebistes reticulatus (Teleostei) in Abhängigkeit vom Lebensalter. Z Mikrosk Anat Forsch 80:433-449
64. Rodríguez-Moldes I, Timmermans JP, Adriaensen D, De Groodt-Lasseel MH, Scheuermann DW, Anadón R (1990) Immunohistochemical localization of calbindin-D28 K in the brain of a cartilaginous fish, the dogfish (Scyliorhinus canicula L.). Acta Anat 137:293-302
65. Roth J, Baetens D, Norman AW, García-Segura LM (1981) Specific neurons in chick central nervous system stain with an antibody against chick intestinal vitamin D-dependent calcium-binding protein. Brain Res 222:452-157
66. Rubio M, Suárez I, Bodega G, Fernández B (1992) Glial fibrillary acidic protein and vimentin immunohistochemistry in the posterior rhombencephalon of the Iberian barb (Barbus comiza). Neurosci Lett 134:203-206
67. Schäfer BW, Heizmann CW (1996) The S100 family of EF-hand calcium-binding proteins: functions and pathology. Trends Biochem Sci 21:134-140
68. Scherer-Singler U, Vincent SR, Kimura H, McGeer EG (1983) Demonstration of a unique population of neurons with NADPH-diaphorase histochemistry. J Neurosci Methods 9:229-234
69. Schwaller B, Buchwald P, Blumcke I, Celio MR, Hunziker W (1993) Characterization of a polyclonal antiserum against the purified human recombinant calcium binding protein calretinin. Cell Calcium 14:639-648
70. Seto-Ohshima A (1994) Calcium-binding proteins in the central nervous system. Acta Histochem Cytochem 27:93-106
71. Stagaard Janas M, Nowakowski RS, Terkelsen OB, Mollgard K (1991) Glial cell differentiation in neuron-free and neuron-rich regions. I. Selective appearance of S-100 protein in radial glial cells of the hippocampal fimbria in human fetuses. Anat Embryol 184:549-558
72. Stevenson JA, Yoon MG (1982) Morphology of radial glia. ependymul cells, and periventricular neurons in the optic tectum of goldfish (Carassius auratus). J Comp Neurol 205:128-138
73. Szabo T, Libouban S, Denizot JP (1990) A well defined spinocerebellar system in the weakly electric teleost fish Gnathonemus petersii. A tracing and immuno-histochemicul study. Arch Ital Biol 128:229-247
74. Tabuchi K, Ohnishi R, Nishimoto A, Isobe T, Okuyama T (1984) Reverse cellular distribution of calmodulin to S-100 protein in primate brain. Brain Res 298:353-357
75. Toyoshima T, Yamagami S, Ahme BYd, Jin L, Miyamoto O, Itano T, Tokuda M, Matsui H, Hatase O (1996) Expression of calbindin-D28 K by reactive astrocytes in gerbil hippocampus after ischaemia. Neuroreport 7:2087-2091
76. Vecino E, Garcia-Briñón J, Velasco A, Caminos E, Lara J (1993) Calbindin D-28 K distribution in the retina of the developing troul (Salmo fario L.). Neurosci Lett 152:91-95
77. Vecino E, Velasco A, Caminos E, Aijón J (1997) Distribution of S100) immunoreactivity in the retina and optic nerve head of the teleost Tinca tinca L. Microsc Res Tech 36:17-25
78. Vernier J-M (1969) Table chronologique du developpement embryonaire de la truite arc-en-ciel. Salmo gairdneri Rich. 1836. Ann Embryol Morphog 2:495-520
79. Yang Q, Hamberger A, Hyden H, Wang S, Stigbrand T, Haglid KG (1995) S-100 beta has a neuronal localisation in the rat hindbrain revealed by an antigen retrieval method. Brain Res 696:49-61
80. Yang Q, Hamberger A, Wang S, Haglid KG (1996) Appearance of neuronal S-100 beta during development of the rat brain. Brain Res Dev Brain Res 91:181-189
81. Zamora AJ, Mutin M (1988) Vimentin and glial fibrillary acidic protein filaments in radial glia of the adult urodele spinal cord. Neuroscience 27:279-288