Radial glial cells, proliferating periventricular cells, and microglia might contribute to successful structural repair in the cerebral cortex of the lizard Gallotia galloti

Experimental Neurology

Volumn 188, Issue 1, 2004, Pages 74-85

  Romero Aleman M M ^a   Monzon Mayor M ^a   Yanes, C ^b   Lang, D ^c  

^a UNIVERSITY OF LAS PALMAS DE GRAN CANARIA   (Spain)

^b UNIVERSIDAD DE LA LAGUNA   (Spain)

^c UNIVERSITY OF CAPE TOWN   (South Africa)

Author keywords

Cell proliferation; Cerebral cortex; Gliosis; Immunohistochemistry; Injury; Radial glial cells; Regeneration; Reptile; Sulci

Indexed keywords

CELL MARKER; CYCLINE; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMATE AMMONIA LIGASE; LECTIN; PROTEIN S 100;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN CORTEX; BRAIN CORTEX LESION; BRAIN VENTRICLE; CELL DIVISION; CONTROLLED STUDY; GALLOTIA GALLOTI; GLIA CELL; LIZARD; MACROPHAGE; MICROGLIA; NERVE CELL; NERVE REGENERATION; NONHUMAN; PRIORITY JOURNAL; STAINING; STATISTICAL SIGNIFICANCE; UPREGULATION;

ANIMALS; BIOLOGICAL MARKERS; BRAIN INJURIES; CELL DIFFERENTIATION; CELL DIVISION; CEREBRAL CORTEX; DENERVATION; GLIAL FIBRILLARY ACIDIC PROTEIN; GLIOSIS; GLUTAMATE-AMMONIA LIGASE; IMMUNOHISTOCHEMISTRY; LIZARDS; MICROGLIA; NERVE REGENERATION; NEURAL PATHWAYS; NEUROGLIA; NEURONAL PLASTICITY; NEURONS; PROLIFERATING CELL NUCLEAR ANTIGEN; REACTION TIME; S100 PROTEINS; STEM CELLS; UP-REGULATION;

EID: 2942578314     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.expneurol.2004.03.014     Document Type: Article

References (59)

1. Anderson M.J., Swanson K.A., Waxman S.G., Eng L.F. Glial fibrillary acidic protein in regenerating teleost spinal cord. J. Histochem. Cytochem. 31:1984;1099-1106
2. Ankerhold R., Leppert C.A., Bastmeyer M., Stuermer C.A.O. E587 antigen is upregulated by goldfish oligodendrocytes after optic nerve lesion and supports retinal axon regeneration. Glia. 23:1998;257-270
3. Attardi D.G., Sperry R.B. Preferential selection of central pathways by regenerating optic fibers. Exp. Neurol. 7:1963;46-64
4. Bastmeyer M., Beckman M., Schwab M.E., Stuermer C.A.O. Growth of regenerating goldfish axons is inhibited by rat oligodendrocytes and CNS myelin but not by goldfish optic nerve/tract oligodendrocyte-like cells and fish CNS myelin. J. Neurosci. 11:1991;626-640
5. Beazley L.D., Sheard P.W., Tennant M., Starac D., Dunlop S.A. Optic nerve regenerates but does not restore topographic projections in the lizard Ctenophorus ornatus. J. Comp. Neurol. 377:1997;105-120
6. Benton R.L., Ross C.D., Miller K.E. Glutamine synthetase activities in spinal white and gray matter 7 days following spinal cord injury in rats. Neurosci. Lett. 291:2000;1-4
7. Bischoff W. Die innerntriche gliederung won Gallotia galloti (Dumeril D. Bibron, 1839) (Reptilia, Sauria: Lacertidae) anf Tenriffa, Kanarische Inseln. Bonn. Zool. Beitr. 33:1982;363-381
8. Blaugrund E., Duvdevani R., Lavie V., Solomon A., Schwartz M. Disappearance of astrocytes and invasion of macrophages following crush injury of adult rodent optic nerves: implications for regeneration. Exp. Neurol. 118:1992;105-115
9. Brunet J.F., Grollimund L., Chatton J.Y., Lengacher S., Magistretti P.J., Villemure J.G., Pellerin L. Early acquisition of typical metabolic features upon differentiation of mouse stem cells into astrocytes. Glia. 46:2004;8-17
10. Cooper N.G.F., Steindler D.A. Lectins demarcate the barrel subfield in the somatosensory cortex of the early postnatal mouse. J. Comp. Neurol. 249:1986;157-169
11. Cooper N.G.F., Steindler D.A. Monoclonal antibody to glial fibrillary acidic protein reveals a parcellation of individual barrels in the early postnatal mouse somatosensory cortex. Brain Res. 380:1986;341-348
12. Font E., García-Verdugo J.M., Desfilis E., Pérez- Cañellas M. Neuron-glia interrelations during 3-acetylpyrydine-induced degeneration and regeneration in the adult lizard brain. Vernadakis A., Roots B. Neuron-Glia Interrelations During Phylogeny: II. Plasticity and Regeneration. 1995;275-302 Humana Press, New Jersey
13. Font E., Defilis E., Pérez-Cañellas M., García- Verdugo J.M. Neurogenesis and neuronal regeneration in the adult reptilian brain. Brain Behav. Evol. 58:2001;276-295
14. García-Verdugo J.M., Fariñas I., Molowny A., López-García C. Ultrastructure of putative migrating cells in the cerebral cortex of Lacerta galloti. J. Morphol. 189:1986;189-197
15. Gaze R.M. The Formation of Nerve Connections. 1970;Academic Press, London
16. Giulian D., Li J., Li X., George J., Rutecki P.A. The impact of microglia-derived cytokines upon gliosis in the CNS. Dev. Neurosci. 16:1994;128-136
17. Gorovits R., Avidan N., Avisar N., Shaked I., Vardimon L. Glutamine synthetase protects against neuronal degeneration in injured retinal tissue. Proc. Natl. Acad. Sci. U. S. A. 94:1997;7024-7029
18. Hirsch S., Bähr M. Glial response to injury. Ingoglia N.A., Murray M. Axonal Regeneration in the Central Nervous System. 2001;315-336 Marcel Dekker, New York
19. Holder N., Clarke J.D.W. Is there a correlation between continuous neurogenesis and directed axon regeneration in the vertebrate nervous system? Trends Neurosci. 11:1988;94-99
20. Kaur C., Hao A.J., Wu C.H., Ling E.A. Origin of microglia. Microsc. Res. Tech. 54:2001;2-9
21. Lang D.M., Rubin B.P., Schwab M.E., Stuermer C.A.O. CNS myelin and oligodendrocytes of Xenopus spinal cord - but not optic nerve - are non-permissive for axon growth. J. Neurosci. 15:1995;99-109
22. Lang D.M., Monzón-Mayor M., Bandlow C.E., Stuermer C.A.O. Retinal axon regeneration in the lizard Gallotia galloti in the presence of CNS myelin and oligodendrocytes. Glia. 22:1998;1-14
23. Lang D.M., Romero-Alemán M.M., Arbelo-Galván J.F., Stuermer C.A.O., Monzón-Mayor M. Regeneration of retinal axons in the lizard Gallotia galloti is not linked to generation of new retinal cells. J. Neurobiol. 52:2002;322-335
24. Lanuza E., Novejarque A., Moncho-Bogani J., Hernández A., Martínez-García F. Understanding the basic circuitry of the cerebral hemispheres: the case of lizards and its implications in the evolution of the telencephalon. Brain Res. Bull. 57:2002;471-473
25. Lavilla J.C. Estabilización de las coloraciones cromoargénticas. Arch. Histol. Norm. Patol. 1:1943;442
26. Lindsay R.M. Reactive gliosis. Fedoroff S., Vernadakis A. Astrocytes. Cell Biology and Pathology of Astrocytes. 1986;231-261 Academic Press, London
27. López-García C., Molowny A., Martínez-Guijarro F.J., Blasco-Ibañez J.M., Luis de la Iglesia J.A., Bernabeu A., García-Verdugo J.M. Lesion and regeneration in the medial cerebral cortex of lizards. Histol. Histopathol. 7:1992;725-746
28. López-García C., Nácher J., Castellano B., Luis de la Iglesia J.A., Molowny A. Transitory disappearance of microglia during the regeneration of the lizard medial cortex. Glia. 12:1994;52-61
29. Martínez-Guijarro F.J., Soriano E., Del Rio J.A., López-García C. Zinc-positive boutons in the cerebral cortex of lizards show glutamate immunoreactivity. J. Neurocytol. 20:1991;834-843
30. Maturana H.R., Letvin J.Y., McCulloch W.S., Pitt W.H. Evidence that cut optic fibers in a frog regenerate to their proper places in tectum. Science. 130:1959;1709-1710
31. Minelli G., Del Grande P., Mambelli C. Preliminary study of the regenerative processes of the dorsal cortex of the telencephalon of Lacerta viridis. Z. Mikrosk.-Anat. Forsch. vol. 91:1978;241-246. Leipzig
32. Monzón-Mayor M., Yanes C., Tholey G., de Barry J., Gombos G. Immunohistochemical localization of glutamine synthetase in mesencephalon and telencephalon of the lizard Gallotia galloti during ontogeny. Glia. 3:1990;81-97
33. Monzón-Mayor M., Yanes C., James J.L., Sturrock R.R. An ultrastructural study of the development of astrocytes in the midbrain of the lizard. J. Anat. 170:1990;33-41
34. Monzón-Mayor M., Yanes C., James J.L., Sturrock R.R. An ultrastructural study of the development of oligodendrocytes in the midbrain of the lizard. J. Anat. 170:1990;43-49
35. Monzón-Mayor M., Yanes C., Ghandour M.S., 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. 295:1990;569-579
36. Monzón-Mayor M., Yanes C., James J.L., Sturrock R.R. An ultrastructural study of ependymal cell differentiation during lizard (Gallotia galloti) midbrain development. J. Anat. 174:1991;251-261
37. Monzón-Mayor M., Yanes-Méndez C., De Barry J., Capdevilla-Carbonell C., Renau-Piqueras J., Tholey G., Gombos G. Heterogeneous immunoreactivity of glial cells in the mesencephalon of a lizard: a double labeling immunohistochemical study. J. Morphol. 235:1998;109-119
38. Morest D.K., Silver J. Precursors of neurons, neuroglia, and ependymal cells in the CNS: what are they? where are they from? how do they get where they are going? Glia. 43:2003;6-18
39. Nácher J., Ramírez J.J., Palop A., Artal P., Molowny A., López-García C. Microglial cells during the lesion-regeneration of the lizard medial cortex. Histol. Histopathol. 14:1999;103-117
40. Nácher J., Ramírez J.J., Palop A., Molowny A., Luis de la Iglesia J.A., López-García C. Radial glia and cell debris removal during lesion-regeneration of the lizard medial cortex. Histol. Histopathol. 14:1999;89-101
41. O'Hara C.M., Chernoff E.A. Growth factor modulation of injury reactive ependymal cell proliferation and migration. Tissue Cell. 26:1994;599-611
42. Plaza-Pérez, M.L., 2002. Células de microglía NDPasa y lectina positivas durante la ontogenia del reptil Gallotia galloti. Comparación de la corteza telencefálica y del techo óptico. University of Las Palmas de Gran Canaria, Doctoral Thesis.
43. Qiu J., Cai D., Filbin M.T. Glial inhibition of nerve regeneration in the mature mammalian CNS. Glia. 29:2000;166-174
44. Ramón y Cajal S. Estudios Sobre la Degeneración y Regeneración del Sistema Nervioso. vol. II:1914;Imprenta de hijos de Nicolás Moya, Madrid
45. Rio J.P., Reperant J., Ward R., Peyrichoux J., Vesselkin N. A preliminary description of the regeneration of the optic nerve fibers in a reptile, Vipera aspis. Brain Res. 479:1989;151-156
46. Romero-Alemán M.M., Monzón-Mayor M., Plaza-Pérez M.L., Yanes C. Development of astroglial cells in the encephalon of Gallotia galloti: a Golgi technique study. J. Morphol. 223:1995;13-20
47. Romero-Alemán M.M., Monzón-Mayor M., Yanes C., Arbelo-Galván J.F., Lang D., Renau-Piqueras J., Negrín- Martínez C. S100 immunoreactive glial cells in the forebrain and midbrain of the lizard Gallotia galloti during ontogeny. J. Neurobiol. 57:2003;54-66
48. Schnell L., Schawb M.E. Axonal regeneration in the rat spinal cord produced by an antibody against myelin-associated neurite growth inhibitors. Nature. 343:1990;269-272
49. Schwab M.E., Caroni P. Oligodendrocytes and CNS myelin are nonpermissive substrate for neurite growth and fibroblast spreading in vitro. J. Neurosci. 8:1988;2381-2393
50. Schwartz M., Lavie V., Cohen A., Murray M., Solomon A., Belkin M. Glial cell differentiation in regeneration and myelination. Jeserich G., Althaus H.H., Waehneldt T.V. Cellular and Molecular Biology of Myelination. 1990;143-154 Springer-Verlag, Berlin
51. Simpson S.B., Duffy M. The lizard spinal cord: a model system for the study of spinal cord injury and repair. Seil F.J. Prog. Brain Res. vol. 103:1994;229-241 Elsevier, New York
52. Sivron T., Schwartz M. The enigma of myelin-associated growth inhibitors in spontaneously regenerating nervous systems. Trends Neurosci. 17:1994;277-281. (Erratum in: 17, 398)
53. Stafford C.A., Shehad S.A., Nona S.N., Cronly-Dillon J.R. Expression of GFAP in Goldfish optic nerve following injury. Glia. 3:1990;33-42
54. Stuermer C.A.O., Bastmeyer M., Bähr M., Strobel G., Paschke K. Trying to understand axonal regeneration in de CNS of fish. J. Neurobiol. 23:1992;537-550
55. Weissman T., Noctor S.C., Clinton B.K., Honing L.S., Kriegstein A.R. Neurogenic radial glial cells in reptile, rodent and human: from mitosis to migration. Cereb. Cortex. 13:2003;550-559
56. Yanes-Méndez C., Martín-Trujillo J.M., Pérez-Batista M.A., Monzón-Mayor M., Marrero A. Ependymogenesis of the lizard Basal Areas: I. Ependymal zones. Z. Mikrosk.-Anat. Forsch. vol. 102:1988;555-572. Leipzig
57. Yanes-Méndez C., Martín-Trujillo J.M., Pérez-Batista M.A., Monzón-Mayor M., Marrero A. Ependymogenesis of the lizard Basal Areas: II. Sulcus. Z. Mikrosk.-Anat. Forsch. vol. 102:1988;573-589. Leipzig
58. Yanes C., Monzón-Mayor M., Ghandour M.S., de Barry J., Gombos G. 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. 295:1990;559-568
59. Yanes C., Monzón-Mayor M., Gombos G., Renau-Piqueras J., Sturrock R.R. Glial cells in the lizard Gallotia galloti subpallial nuclei during ontogeny: an ultrastructural study. J. Morphol. 233:1997;1-13