Top

Published in:

01-04-2012 | Original Article

Local and remote cellular responses following a surgical lesion in the Cebus apella cerebral cortex

Authors: Ximena A. Lanosa, Alberto Yáñez, Sabina Alzugaray, Jorge A. Colombo

Published in: Brain Structure and Function | Issue 2/2012

Abstract

Distribution of bromodeoxyuridine immunoreactive (BrdU-IR) cell nuclei was analyzed at proximal and remote cortical sites in adult Cebus apella monkeys after a programmed surgical lesion placed either in the prefrontal or in the striate cerebral cortex. Increased GFAP-IR and vimentin-IR astrocytes, as well as IsolectinB4 labeled microglial cells, were observed both at lesional and perilesional areas. After injury at either location, the BrdU nuclear incorporation spread to supragranular layers in remote cortical areas functionally related to the injured cortex, probably due to involvement of degenerated cortico-cortical association fibers. Double labeling with Ki-67 suggested that remote BrdU-IR nuclei belong to proliferating cells, but the cell type remains to be determined, since these nuclei did not correspond to NeuN, MAP2, GFAP, Vimentin and isolectinB4 labeled cells. This remote effect should be incorporated to current clinical and experimental appraisal of cortical lesions.

Amat J, Ishiguro H, Nakamura K, Norton W (1996) Phenotypic diversity and kinetic of proliferating microglia and astrocytes following cortical stab wounds. Glia 16:368–382PubMedCrossRef

Bähr M, Bonhoeffer F (1994) Perspectives on axonal regeneration in the mammalian CNS. TINS 17:473–479PubMed

Balajee A, May A, Bohr V (1998) Fine structural analysis of DNA repair in mammalian cells. Mutat Res 404:3–11PubMedCrossRef

Balasingam V, Tejada-Berges T, Wright E, Bouckova R, Yong V (1994) Reactive astrogliosis in the neonatal mouse brain and its modulation by cytokines. J Neurosci 14:846–856PubMed

Bauer S, Patterson P (2005) The cell cycle—apoptosis connection revisited in the adult brain. J Cell Biol 171:641–650PubMedCrossRef

Bignami A, Dahl D (1976) The astroglial response to stabbing. Immunofluorescence studies with antibodies to astrocyte-specific protein (GFA) in mammalian and submammalian vertebrates. Neuropathol Appl Neurobiol 2:99–110CrossRef

Bignami A, Raju T, Dahl D (1982) Localization of vimentin, the non-specific intermediate filament protein, in embryonal glia and in early differentiating neurons. In vivo and in vitro immunofluorescence study of the rat embryo with vimentin and neurofilament antisera. Dev Biol 91:286–295PubMedCrossRef

Bressler S (1996) Interareal synchronization in the visual cortex. Behav Brain Res 76:37–49PubMedCrossRef

Brodmann K (1909) Vergleichende Localisationslehre der Grosshirnrinde in thren Prinzipien Dargestellt auf Grund des Zellenbaues. Barth, Leipzig

Campana D, Coustan-Smith E, Janossy G (1988) Double and triple staining methods for studying the proliferative activity of human B and T lymphoid cells. J Immunol Methods 107:79–88PubMedCrossRef

Coe C, Savage A, Bromley L (1992) Phylogenetic influences on hormone levels across the primate order. Am J Primatol 28:81–100CrossRef

Colombo J (2001) A columnar—supporting mode of astroglial architecture in the cerebral cortex of adult primates? Neurobiology 9:1–16PubMedCrossRef

Colombo J, Reisin H (2004) Interlaminar astroglia of the cerebral cortex: a marker of the primate brain. Brain Res 1006:126–131PubMedCrossRef

Colombo J, Yáñez A, Puissant V, Lipina S (1995) Long, interlaminar astroglial cell processes in the cortex of adult monkeys. J Neurosci Res 40:551–556PubMedCrossRef

Colombo J, Lipina S, Yáñez A, Puissant V (1997a) Postnatal development of interlaminar astroglial processes in the cerebral cortex of primates. Int J Dev Neurosci 15:823–833PubMedCrossRef

Colombo J, Yáñez A, Lipina S (1997b) Interlaminar astroglial processes in the cerebral cortex of non-human primates: response to injury. Brain Res 38:503–512

Colombo J, Reisin H, Jones M, Bentham C (2005) Development of human interlaminar astroglial processes in the cerebral cortex of control and Down’s Syndrome cases. Exp Neurol 193:207–217PubMedCrossRef

Cuzick J (1985) A method for analysing case-control studies with ordinal exposure variables. Biometrics 41:609–621PubMedCrossRef

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

Eng L, Ghirnikar R (1994) GFAP and astrogliosis. Brain Pathol 4:229–237PubMedCrossRef

Eng L, Vanderhaeghen J, Bignami A, Gersh B (1971) An acidic protein isolated from fibrous astrocytes. Brain Res 28:351–354PubMedCrossRef

Fiorani M Jr, Gattass R, Rosa M, Sousa A (1989) Visual area MT in the Cebus monkey: location, visuotopic organization, and variability. J Comp Neurol 287:98–118PubMedCrossRef

Franke H, Krügel U, Illes P (1999) P2 receptor-mediated proliferative effects on astrocytes in vivo. Glia 28:190–200PubMedCrossRef

Gould E, Gross C (2002) Neurogenesis in adult mammals: some progress and problems. J Neurosci 22:619–623PubMed

Gould E, Tanapat P, McEwen B, Flügge G, Fuchs E (1998) Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proc Natl Acad Sci USA 95:3168–3171PubMedCrossRef

Gould E, Reeves A, Graziano M, Gross C (1999) Neurogenesis in the neocortex of adult primates. Science 286:548–552PubMedCrossRef

Gould E, Vail N, Wagers M, Gross C (2001) Adult-generated hippocampal and neocortical neurons in macaques have a transient existence. Proc Natl Acad Sci USA 98:10910–10917PubMedCrossRef

Hampton D, Rhodes K, Zhao C, Franklin R, Fawcett J (2004) The responses of oligodendrocyte precursor cells, astrocytes and microglia to a cortical stab injury, in the brain. Neuroscience 127:813–820PubMedCrossRef

Jones L, Yamaguchi Y, Stallcup W, Tuszynski M (2002) NG2 is a major chondroitin sulfate proteoglycan produced after spinal cord injury and is expressed by macrophages and oligodendrocyte progenitors. J Neurosci 22:2792–2803PubMed

Kalle W, Hazekamp-van Dokkum A, Lohman P, Natarajan A, van Zeeland A, Mullenders L (1993) The use of streptavidin-coated magnetic beads and biotinylated antibodies to investigate induction and repair of DNA damage: analysis of repair patches in specific sequences of uv-irradiated human fibroblasts. Anal Biochem 208:228–236PubMedCrossRef

Kao G, McKenna W, Yen T (2001) Detection of repair activity during the DNA damage-induced G2 delay in human cancer cells. Oncogene 20:3486–3496PubMedCrossRef

Kee N, Sivalingam S, Boostra R, Wojtowicz J (2002) The utility of Ki-67 and BrdU as proliferative markers of adult neurogenesis. J Neurosci Methods 115:97–105PubMedCrossRef

Koketsu D, Mikami A, Miyamoto Y, Hisatsune T (2003) Nonrenewal of neurons in the cerebral neocortex of adult macaque monkeys. J Neurosci 23:937–942PubMed

Kornack D, Rakic P (1999) Continuation of neurogenesis in the hippocampus of adult macaque monkey. Proc Natl Acad Sci USA 96:5768–5773PubMedCrossRef

Környei Z, Czirók A, Vicsek T, Madarász E (2000) Proliferative and migratory responses of astrocytes to in vitro injury. J Neurosci Res 61:421–429PubMedCrossRef

Lahoz M, Nagle C, Porta M, Farinati Z, Manssur T (2006) Cortisol response and ovarian hormones in juvenile and cycling female Cebus monkeys: effect of stress and dexamethasone. Am J Primatol 69:551–561CrossRef

Landis D (1994) The early reactions of non-neuronal cells to brain injury. Annu Rev Neurosci 17:133–151PubMedCrossRef

Lanosa X, Reisin H, Santacroce I, Colombo J (2008) Astroglial dye-coupling: an in vitro analysis of regional and interspecies differences in rodents and primates. Brain Res 1240:82–86PubMedCrossRef

Levine J (1994) Increased expression of the NG2 chondroitin-sulfate proteoglycan after brain injury. J Neurosci 14:4716–4730PubMed

Limsirichaikul S, Niimi A, Fawcett F, Lehmann A, Yamashita S, Ogi T (2009) A rapid non-radioactive technique for measurement of repair synthesis in primary human fibroblasts by incorporation of ethynyl deoxyuridine (EdU). Nucleic Acids Res 37:e31PubMedCrossRef

Lin J, Weigel H, Cotrina M, Liu Sh, Bueno E, Hansen A, Hansen T, Goldman S, Nedergaard M (1998) Gap-junction-mediated propagation and amplification of cell injury. Nature 1:494–501

Manocha S, Shantha T, Bourne G (1968) A stereotaxic atlas of the brain of Cebus monkey (Cebus apella). Oxford University Press, London

Miyake T, Hattori T, Fukuda M, Kitamura T, Fijita S (1988) Quantitative studies on proliferative changes of reactive astrocytes in mouse cerebral cortex. Brain Res 451:133–138PubMedCrossRef

Moore N, Okocha F, Cui J, Liu P (2002) Homogeneous repair of nuclear genes after experimental stroke. J Neurochem 80:111–118PubMedCrossRef

Nathaniel E, Nathaniel D (1981) The reactive astrocyte. In: Advances in cellular neurobiology, vol 2. Academic Press, New York, pp 249–301

NIH (1985) Guide for the care and use of laboratory animals. National Academies Press, 500 Fifth Street, NW, Lockbox 285, Washington, DC, p 20055

Norton W, Aquino D, Hozumi I, Chiu F, Brosnan C (1992) Quantitative aspects of reactive gliosis: a review. Neurochem Res 17:877–885PubMedCrossRef

Nowakowski R, Hayes N (2000) New neurons: extraordinary evidence or extraordinary conclusion? Science 288:771aCrossRef

Oberheim N, Wang X, Goldman S, Nedergaard M (2006) Astrocytic complexity distinguishes the human brain. Trends Neurosci 29:547–553PubMedCrossRef

Pons T, Garraghty P, Ommaya A, Kaas J, Taub E, Mishkin M (1991) Massive cortical reorganization after sensory deafferentation in adult macaques. Science 252:1857–1860PubMedCrossRef

Rakic P (2002) Adult neurogenesis in mammals: an identity crisis. J Neurosci 22:614–618PubMed

Reisin H, Colombo J (2004) Glial changes in primate cerebral cortex following long-term sensory deprivation. Brain Res 1000:179–182PubMedCrossRef

Rockland K, Pandya D (1979) Laminar origins and terminations o cortical connections of the occipital lobe in the Rhesus monkey. Brain Res 179:3–20PubMedCrossRef

Roitbak T, Syková E (1999) Diffusion barriers evoked in rat cortex by reactive astrogliosis. Glia 28:40–48PubMedCrossRef

Salin P, Bullier J (1995) Cortico-cortical connections in the visual system: structure and function. Physiol Rev 75:107–154PubMed

Sanal N, Tramontin A, Quiñones-Hinojosa A, Barbaro N, Gupta N, Kunwar S, Lawton M, McDermott M, Parsa A, Manuel-García Verdugo J, Berger M, Alvarez-Buylla A (2004) Unique astrocyte ribbon in adult human contains neural stem cell but lack chain migration. Nature 427:740–744CrossRef

Schwartz M, Goldman-Rakic P (1982) Single cortical neurons have axon collaterals to ipsilateral and contralateral cortex in fetal and adult primates. Nature 299:154–155PubMedCrossRef

Selden J, Dolbeare F, Clair J, Nichols W, Miller J, Kleemeyer K, Hyland R, DeLuca J (1993) Statistical confirmation that immunofluorescent detection of DNA repair in human fibroblasts by measurement of bromodeoxyuridine incorporation is stoichiometric and sensitive. Cytometry 14:154–167PubMedCrossRef

Solomon D, Cardoso M, Knudsen E (2004) Dynamic targeting of the replication machinery to sites of DNA damage. J Cell biol 166:455–463PubMedCrossRef

Spalding K, Bhardwaj R, Buchholz B, Druid H, Frisén J (2005) Retrospective birth dating of cells in humans. Cell 122:133–143PubMedCrossRef

Stallcup W (2002) The NG2 proteoglycan: past insights and future prospects. J Neurocytol 31:423–435PubMedCrossRef

Takano T, Oberheim N, Cotrina M, Nedergaard M (2009) Astrocytes and ischemic injury. Stroke 40:S8–S12PubMedCrossRef

Tan A, Zhang W, Levine J (2005) NG2: a component of the glial scar that inhibits axon growth. J Anat 207:717–725PubMedCrossRef

Watanabe M, Toyama Y, Nishiyama A (2002) Differentiation of proliferated NG2-positive glial progenitor cells in a remyelinating lesion. J Neurosci Res 69:826–836PubMedCrossRef

Title: Local and remote cellular responses following a surgical lesion in the Cebus apella cerebral cortex
Authors: Ximena A. Lanosa
Alberto Yáñez
Sabina Alzugaray
Jorge A. Colombo
Publication date: 01-04-2012
Publisher: Springer-Verlag
Published in: Brain Structure and Function / Issue 2/2012
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-011-0356-3

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Local and remote cellular responses following a surgical lesion in the Cebus apella cerebral cortex

Abstract

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 2/2012

Reduction of cerebellar grey matter in Crus I and II in schizophrenia

Brain grey matter deficits in smokers: focus on the cerebellum

Hippocampal levels of GluR1 and GluR2 complexes are modulated by training in the multiple T-Maze in C57BL/6J mice

The red nucleus and the rubrospinal projection in the mouse

Sensory deprivation differentially impacts the dendritic development of pyramidal versus non-pyramidal neurons in layer 6 of mouse barrel cortex

Parasagittal compartmentation of cerebellar mossy fibers as revealed by the patterned expression of vesicular glutamate transporters VGLUT1 and VGLUT2