Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-24T10:47:26.092Z Has data issue: false hasContentIssue false
  • English
  • Français

Exposure to environmental enrichment prior to a cerebral cortex stab wound attenuates the postlesional astroglia response in rats

Published online by Cambridge University Press:  06 July 2012

Ximena A. Lanosa ,
Ignacio Santacroce  and
Jorge A. Colombo
Ximena A. Lanosa*
Affiliation:
Unidad de Neurobiología Aplicada (CEMIC-CONICET), Buenos Aires, Argentina
Ignacio Santacroce
Affiliation:
Unidad de Neurobiología Aplicada (CEMIC-CONICET), Buenos Aires, Argentina
Jorge A. Colombo
Affiliation:
Unidad de Neurobiología Aplicada (CEMIC-CONICET), Buenos Aires, Argentina
*
Correspondence should be addressed to: Ximena A. Lanosa, Unidad de Neurobiología Aplicada (CEMIC-CONICET), Av. Galván 4102, C1431FWO Buenos Aires, Argentina phone: (+5411) 45 45 65 89 email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Modulation of astroglial components involved in reactive postlesional responses in the rat cerebral cortex was analyzed following exposure to environmental enrichment (EE) condition prior to injury. For this purpose, changes in % immunoreactive (IR) area of GFAP, vimentin, EAAT1 and ezrin were evaluated in the perilesional zone after placing a cortical stab wound in the visual cerebral cortex of adult rats. GFAP-IR postlesional reactive astrocytosis in the perilesional cortex was significantly lower in the animal group exposed to EE during postnatal development. This GFAP-IR reaction seems to be associated with existing astroglia, because neither BrdU- nor endogenous Ki-67-labeled nuclei were found in the perilesional cortex analyzed. Increased ezrin-IR area in the visual cortex of rats exposed to EE condition suggests the formation of new synapses or the enhancement of astroglial involvement in the existing ones. No effects of EE were found on either EAAT1- or vimentin-IR area. Results suggest that exposure to EE conditions prior to injury attenuates the postlesional astroglia GFAP-response in the perilesional cortex of rats. Whether this attenuated postlesional astroglia GFAP-response promotes or not protective effects on the cortical neuropil remains to be explored in futures studies.

Keywords

Enriched environmentreactive GFAP-astrocytesezrincortical injuryprotective effects
Type
Research Article
Information
Neuron Glia Biology , Volume 7 , Issue 2-4 , May 2011 , pp. 163 - 175
Copyright
Copyright © Cambridge University Press 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Amat, J., Ishiguro, H., Nakamura, K. and Norton, W. (1996) Phenotypic diversity and kinetics of proliferating microglia and astrocytes following cortical stab wounds. Glia 16, 368–382.Google Scholar
Bähr, M. and Bonhoeffer, F. (1994) Perspectives on axonal regeneration in the mammalian CNS. Trends in Neurosciences 17, 473–479.Google Scholar
Beschorner, R., Dietz, K., Schauer, N., Mittelbronn, M., Schluesener, H.J., Trautmann, K. et al. (2007) Expression of EAAT1 reflects a possible neuroprotective function of reactive astrocytes and activated microglia following human traumatic brain injury. Histology and Histopathology 22, 515–526.Google Scholar
Black, J., Sirevaag, A. and Greenough, W. (1987) Complex experience promotes capillary formation in young rat visual cortex. Neuroscience Letters 83, 351–355.Google Scholar
Bovolenta, P., Fernaud-Espinosa, I., Méndez-Otero, R. and Nieto-Sampedro, M. (1997) Neurite outgrowth inhibitor of gliotic brain tissue. Mode of action and cellular localization, studied with specific monoclonal antibodies. European Journal of Neuroscience 9, 977–989.Google Scholar
Bovolenta, P., Wandosell, F. and Nieto-Sampedro, M. (1993) Characterization of a neurite outgrowth inhibitor expressed after CNS injury. European Journal of Neuroscience 5, 454–465.Google Scholar
Calvo, J., Carbonell, A. and Boya, J. (1991) Co-expression of glial fibrillary acidic protein and vimentin in reactive astrocytes following brain injury in rats. Brain Research 566, 333–336.Google Scholar
Campana, D., Coustan-Smith, E. and Janossy, G. (1988) Double and triple staining methods for studying the proliferative activity of human B and T lymphoid cells. Journal of Immunology Methods 107, 79–88.Google Scholar
Colombo, J., Fuchs, E., Härtig, W., Marotte, L. and Puissant, V. (2000) “Rodent-like” and “primatelike” types of astroglial architecture in the adult cerebral cortex of mammals: a comparative study. Anatomy and Embryology 201, 111–120.Google Scholar
Colombo, J., Härtig, W., Lipina, S. and Bons, N. (1998) Astroglial interlaminar processes in the cerebral cortex of prosimians and Old World monkeys. Anatomy and Embryology 197, 369–376.Google Scholar
Colombo, J., Schleicher, A. and Zilles, K. (1999) Patterned distribution of immunoreactive astroglial processes in the striate (V1) cortex of New World monkeys. Glia 25, 85–92.Google Scholar
Colombo, J., Yáñez, A. and Lipina, S. (1997) Interlaminar astroglial processes in the cerebral cortex of non-human primates: response to injury. Brain Research 38, 503–512.Google Scholar
Cui, Q., Yin, Y. and Benowitz, L. (2009) The role of macrophages in optic nerve regeneration. Neuroscience 158, 1039–1048.Google Scholar
Derouiche, A., Anlauf, E., Aumann, G., Mühlstädt, B. and Lavialle, M. (2002) Anatomical aspects of glia-synapse interaction: the perisynaptic glial sheath consists of a specialized astrocyte compartment. Journal of Physiology Paris 96, 177–182.Google Scholar
Derouiche, A. and Frotscher, M. (2001) Peripheral astrocyte processes: monitoring by selective immunostaining for the actin-binding ERM proteins. Glia 36, 330–341.Google Scholar
Emirandetti, A., Graciele Zanon, R., Sabha, M. Jr. and de Oliveira, A. (2006) Astrocyte reactivity influences the number of presynaptic terminals apposed to spinal motoneurons after axotomy. Brain Research 1095, 35–42.Google Scholar
Eng, L. and Ghirnikar, R. (1994) GFAP and astrogliosis. Brain Pathology 4, 229–237.Google Scholar
Farah, M., Illes, J., Cook-Deegan, R., Gardner, H., Kandel, E., King, P. et al. (2004) Neurocognitive enhancement: what can we do and what should we do? Nature Reviews Neuroscience 5, 421–425.Google Scholar
Fawcett, J. and Asher, R. (1999) The glial scar and central nervous system repair. Brain Research Bulletin 46, 377–391.Google Scholar
Fisher, B., Petzinger, G., Nixon, K., Hogg, E., Bremner, S., Mwshul, C. et al. (2004) Exercise-induced behavioral recovery and neuroplasticity in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-lesioned mouse basal ganglia. Journal of Neuroscience Research 77, 378–390.Google Scholar
Geiger, K., Stoldt, P., Schlote, W. and Derouiche, A. (2000) Ezrin immunoreactivity is associated with increasing malignancy of astrocytic tumors but is absent in oligodendrogliomas. American Journal of Pathology 157, 1785–1793.Google Scholar
Grönholm, M., Teesalu, T., Tyynelä, J., Piltti, K., Böhling, T., Wartiovaara, K. et al. (2005) Characterization of the NF2 protein merlin and the ERM protein ezrin in human, rat, and mouse central nervous system. Molecular and Cellular Neuroscience 28, 683–693.Google Scholar
Grossman, A., Churchill, J., Bates, K., Kleim, J. and Greenough, W. (2002) A brain adaptation view of plasticity: is synaptic plasticity an overly limited concept? Progress in Brain Research 138, 91–108.Google Scholar
Grossman, A., Churchill, J., McKinney, B., Kodish, I., Otte, S. and Greenough, W. (2003) Experience effects on brain development: possible contributions to psychopathology. Journal of Child Psychology and Psychiatry 44, 33–63.Google Scholar
Hampton, D., Rhodes, K., Zhao, C., Franklin, R. and Fawcett, J. (2004) The responses of oligodendrocyte precursor cells, astrocytes and microglia to a cortical stab injury, in the brain. Neuroscience 127, 813–820.Google Scholar
Hess, G. (2004) Synaptic plasticity of local connections in rat motor cortex. Acta Neurobiologiae Experimentalis 64, 271–276.Google Scholar
Howard, V. and Reed, M. (eds) (2005) Unbiased Stereology: Three-Dimensional Measurement in Microscopy. Oxford, UK: BIOS Scientific Publishers.Google Scholar
Johansson, B. (1996) Functional outcome in rats transferred to an enriched environment 15 days after focal brain ischemia. Stroke 27, 324–326.Google Scholar
Johansson, B. (2000) Brain plasticity and stroke rehabilitation. The Willis lecture. Stroke 31, 223–230.Google Scholar
Johansson, B. and Belichenko, P. (2002) Neuronal plasticity and dendritic spines: effect of environmental enrichment on intact and postischemic rat brain. Journal of Cerebral Blood Flow and Metabolism 22, 89–96.Google Scholar
Johnson, A. (1993) Contact inhibition in the failure of mammalian CNS axonal regeneration. Bioessays 15, 807–813.Google Scholar
Jones, T. and Greenough, W. (1996) Ultrastructural evidence for increased contact between astrocytes and synapses in rats reared in a complex environment. Neurobiology of Learning and Memory 65, 48–56.Google Scholar
Kim, J., Kim, J., Park, J., Lee, S., Kim, W., Yu, Y. et al. (2006) Blood-neural barrier: intercellular communication at glio-vascular interface. Journal of Biochemistry and Molecular Biology 39, 339–345.Google Scholar
Komitova, M., Perfilieva, E., Mattsson, B., Eriksson, P. and Johansson, B. (2002) Effects of cortical ischemia and postischemic environmental enrichment on hippocampal cell genesis and differentiation in the adult rat. Journal of Cerebral Blood Flow and Metabolism 22, 852–860.Google Scholar
Lanosa, X. and Colombo, J. (2008) Cell contact-inhibition signaling as part of brain tissue wound-healing processes. Neuron Glia Biology 13, 1–8.Google Scholar
Lanosa, X., Yañez, A., Alzugaray, S. and Colombo, J. (2012) Local and remote cortical cellular responses following a surgical lesion in the Cebus Apella cerebral cortex. Brain Structure and Function, 217, 485–501.Google Scholar
Lavialle, M., Aumann, G., Anlauf, E., Pröls, F., Arpin, M. and Derouiche, A. (2011) Structural plasticity of perisynaptic a0073trocyte processes involves ezrin and metabotropic glutamate receptors. Proceedings of the National Academy of Sciences of the U.S.A. 108, 12915–12919.Google Scholar
Lindsay, R. (1986) Reactive gliosis. In Fedoroff, S. and Vernadakis, A. (eds) Astrocytes, vol. 3, pp. 231–262. Orlando: Academic Press.Google Scholar
Lipina, S. and Colombo, J. (2007) Premorbid exercising in specific cognitive tasks prevents impairment of performance in parkinsonian monkeys. Brain Research 1134, 180–186.Google Scholar
Lippert-Gruener, M., Maegele, M., Garbe, J. and Angelov, D. (2007) Late effects of enriched environment (EE) plus multimodal early onset stimulation (MEOS) after traumatic brain injury in rats: Ongoing improvement of neuromotor function despite sustained volume of the CNS lesion. Experimental Neurology 203, 82–94.Google Scholar
Miguel-Hidalgo, J., Waltzer, R., Whittom, A., Austin, M., Rajkowska, G. and Stockmeier, C. (2010) Glial and glutamatergic markers in depression, alcoholism, and their comorbidity. Journal of Affective Disorders 127, 230–240.Google Scholar
Miyake, T., Hattori, T., Fukuda, M., Kitamura, T. and Fijita, S. (1988) Quantitative studies on proliferative changes of reactive astrocytes in mouse cerebral cortex. Brain Research 451, 133–138.Google Scholar
Nieto-Sampedro, M. (1999) Neurite outgrowth inhibitors in gliotic tissue. Advances in Experimental Medicine and Biology 468, 207–224.Google Scholar
Paxinos, G. and Watson, C. (1982) The Rat Brain in Stereotaxic Coordinates. New York: Academic Press.Google Scholar
Raivich, G., Bohatschek, M., Kloss, C.U., Werner, A., Jones, L.L. and Kreutzberg, G.W. (1999) Neuroglial activation repertoire in the injured brain: graded response, molecular mechanisms and cues to physiological function. Brain Research Reviews 30, 77–105.Google Scholar
Ridet, J., Malhotra, S., Privat, A. and Gage, F. (1997) Reactive astrocytes: cellular and molecular cues to biological function. Trends in Neurosciences 20, 570–576.Google Scholar
Robertson, I. and Murre, J. (1999) Rehabilitation of brain damage: brain plasticity and principles of guided recovery. Psychological Bulletin 125, 544–575.Google Scholar
Schiffer, D., Giordana, M.T., Migheli, A., Giaccone, G., Pezzotta, S. and Mauro, A. (1986) Glial fibrillary acidic protein and vimentin in the experimental glial reaction of the rat brain. Brain Research 374, 110–118.Google Scholar
Schutte, B., Reynders, M., Bosman, F. and Blijham, G. (1987) Effect of tissue fixation on antibromodeoxyuridine immunohistochemistry. Journal of Histochemistry and Cytochemistry 35, 1343–1345.Google Scholar
Tator, C. and Fehlings, M. (1991) Review of the secondary injury theory of acute spinal cord trauma with emphasis on vascular mechanisms. Journal of Neurosurgery 75, 15–26.Google Scholar
Wang, K., Bekar, L., Furber, K. and Walz, W. (2004) Vimentin-expressing proximal reactive astrocytes correlate with migration rather than proliferation following focal brain injury. Brain Research 1024, 193–202.Google Scholar
Weiloch, T. and Nikolich, K. (2006) Mechanisms of neural plasticity following brain injury. Current Opinon in Neurobiology 16, 258–264.Google Scholar
Will, B., Rosenzweig, M., Bennett, E., Hebert, M. and Morimoto, H. (1977) Relatively brief environmental enrichment aids recovery of learning capacity and alters brain measures after postweaning brain lesions in rats. Journal of Comparative and Physiological Psychology 91, 33–50.Google Scholar
Winocur, G., Moscovitch, M., Fogel, S., Rosenbaum, R. and Sekeres, M. (2005) Preserved spatial memory after hippocampal lesions: effects of extensive experience in a complex environment. Nature Neuroscience 8, 273–275.Google Scholar
Xerri, C. and Zennou-Azogui, Y. (2003) Influence of the postlesion environment and chronic piracetam treatment on the organization of the somatotopic map in the rat primary somatosensory cortex after focal cortical injury. Neuroscience 118, 161–177.Google Scholar
Supplementary material: Image

Lanosa et al. supplementary material

Supplementary material

Download Lanosa et al. supplementary material(Image)
Image 162.4 KB
Supplementary material: Image

Lanosa et al. supplementary material

Supplementary material

Download Lanosa et al. supplementary material(Image)
Image 4 MB
Supplementary material: Image

Lanosa et al. supplementary material

Supplementary material

Download Lanosa et al. supplementary material(Image)
Image 2.8 MB