Skip to main content
SpringerLink
Log in

Developmental profiles of GFAP-positive astrocytes in sheep cerebellum

  • Original Article
  • Published:
Veterinary Research Communications Aims and scope Submit manuscript

Abstract

Astroglial account for the largest glial population in the brain and play a variety of vital functions in the development of the central nervous system (CNS). An immunohistochemical study was performed in 19 ovine foetuses ranging from 2 to 5 months of gestation, one newborn lamb and three adult sheep. Using the anit-glial fibrillary acidic protein (GFAP) marker, several variations were found in the degree of GFAP positive (GFAP+) astrocyte distribution between the different zones in the cerebellum of sheep during brain development. Our study indicates that the first appearance of astrocytes from restricted zones in the cerebellum occurs around the eighth week of gestation. Bergmann cells were found to be present from around the 15th week of gestation onwards. Our findings suggest that the maturation of astrocytes begins in the caudal parts of the cerebellum, developing from their initial ventral regions to spread first to dorsal regions radially within the white matter, then followed by the more rostral parts of the cerebellum. Astrocytes were also found to proliferate in the vermis before appearing in the cerebellar hemispheres.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Alcock J, Scotting P, Sottile V (2007) Bergmann glia as putative stem cells of the mature cerebellum. Med Hypotheses 69:341–345

    Article  CAS  PubMed  Google Scholar 

  • Argandoña EG, Rossi ML, Lafuente JV (2003) Visual deprivation effects on the s100beta positive astrocytic population in the developing rat visual cortex: a quantitative study. Brain Res Dev Brain Res 141:63–69

    Article  PubMed  Google Scholar 

  • Bignami A, Eng LF, Dahl D, Uyeda CT (1972) Localization of the glial fibrillary acidic protein in astrocytes by immunofluorescence. Brain Res 43:429–435

    Article  CAS  PubMed  Google Scholar 

  • Brunne B, Zhao S, Derouiche A, Herz J, May P, Frotscher M, Bock HH (2010) Origin, maturation, and astroglial transformation of secondary radial glial cells in the developing dentate gyrus. Glia 58:1553–1569

    PubMed Central  PubMed  Google Scholar 

  • Butt AM, Ransom BR (1993) Morphology of astrocytes and oligodendrocytes during development in the intact rat optic nerve. J Comp Neurol 338:141–158

    Article  CAS  PubMed  Google Scholar 

  • Cahoy JD, Emery B, Kaushal A, Foo LC, Zamanian JL, Christopherson KS, Xing Y, Lubischer JL, Krieg PA, Krupenko SA, Thompson WJ, Barres BA (2008) Transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J Neurosci 28:264–278

    Article  CAS  PubMed  Google Scholar 

  • Cameron RS, Rakic P (1991) Glial cell lineage in the cerebral cortex: a review and synthesis. Glia 4:124–137

    Article  CAS  PubMed  Google Scholar 

  • Castan P (1968) Les fonctions métaboliques de l’astroglie cérébrale, élément fondamental de la barrière hémato-encéphalique: applications aux encéphalopathies métaboliques, toxiques et glio-spongieuses subaiguës. J Neurol Sci 6:237–248

    Article  CAS  PubMed  Google Scholar 

  • Chahrour M, Zoghbi HY (2007) The story of Rett syndrome: from clinic to neurobiology. Neuron 56:422–437

    Article  CAS  PubMed  Google Scholar 

  • Clarke LE, Barres BA (2013) Emerging roles of astrocytes in neural circuit development. Nat Rev Neurosci 14:311–321

    Article  CAS  PubMed  Google Scholar 

  • 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 Com Neurol 239:75–88

    Article  CAS  Google Scholar 

  • Deazevedo LC, Fallet C, Moura-neto V, Daumas-duport C, Hedin-pereira C, Lent R (2003) Cortical radial glial cells in human foetuses: depth-correlated transformation into astrocytes. J Neurobiol 55:288–298

    Article  PubMed  Google Scholar 

  • Emsley JG, Macklis JD (2006) Astroglial heterogeneity closely reflects the neuronal-defined anatomy of the adult murine CNS. Neuron Glia Biol 2:175–86

    Article  PubMed Central  PubMed  Google Scholar 

  • Eng LF (1985) Glial fibrillary acidic protein (GFAP): the major protein of glial intermediate filaments in differentiated astrocytes. J Neuroimmunol 8:203–14

    Article  CAS  PubMed  Google Scholar 

  • Eng LF, Ghirnikar R, LEE Y (2000) Glial fibrillary acidic protein: GFAP-thirty-one years (1969–2000). Neurochem Res 25:1439–1451

    Article  CAS  PubMed  Google Scholar 

  • Freeman MR (2010) Specification and morphogenesis of astrocytes. Sci 330:774–778

    Article  CAS  Google Scholar 

  • Georgsson G, Gísladóttir E, Arnadóttir S (1993) Quantitative assessment of the astrocytic response in natural scrapie of sheep. J Com Pathol 108:229–240

    Article  CAS  Google Scholar 

  • Hartfuss E, Galli R, Heins N, Götz M (2001) Characterization of CNS precursor subtypes and radial glia. Dev Biol 229:15–30

    Article  CAS  PubMed  Google Scholar 

  • Herculano-houzel S (2009) The human brain in numbers: a linearly scaled-up primate brain. Fron Hum Neurosci 3:31

    Google Scholar 

  • Hewicker-Trautwein M, Trautwein G (1993) An immunohistochemical study of the foetal sheep neocortex and cerebellum with antibodies against nervous system-specific proteins. J Com Pathol 109:409–421

    Article  CAS  Google Scholar 

  • Huang WL, Harper CG, Evans SF, Newnham JP, Dunlop SA (2001) Repeated prenatal corticosteroid administration delays astrocyte and capillary tight junction maturation in foetal sheep. Int J Dev Neurosci 19:487–493

    Article  CAS  PubMed  Google Scholar 

  • Hunter KE, Hatten ME (1995) Radial glial cell transformation to astrocytes is bidirectional: regulation by a diffusible factor in embryonic forebrain. Proc Natl Acad Sci U S A 92:2061–5

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ihrie R, Alvarez-buylla A (2008) Cells in the astroglial lineage are neural stem cells. Cell Tissue Res 331:179–191

    Article  PubMed  Google Scholar 

  • Jacobs S, Nathwani M, Doering L (2010) Fragile X astrocytes induce developmental delays in dendrite maturation and synaptic protein expression. BMC Neurosci 11:132

    Article  PubMed Central  PubMed  Google Scholar 

  • Jacobsen CT, Miller RH (2003) Control of astrocyte migration in the developing cerebral cortex. Dev Neurosci 25:207–16

    Article  CAS  PubMed  Google Scholar 

  • Kim JV, Dustin ML (2006) Innate response to focal necrotic injury inside the blood–brain barrier. J Immunol 177:5269–5277

    Article  CAS  PubMed  Google Scholar 

  • Lee A, Kessler JD, Read TA, Kaiser C, Corbeil D, Huttner WB, Johnson JE, Wechsler-Reya RJ (2005) Isolation of neural stem cells from the postnatal cerebellum. Nat Neurosci 8:723–9

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lepore G, Gadau S, Peruffo A, Mura A, Mura E, Floris A, Balzano F, Zedda M, Farina V (2011) Aromatase expression in cultured foetal sheep astrocytes after nitrosative/oxidative damage. Cell Tissue Res 344:407–413

    Article  CAS  PubMed  Google Scholar 

  • Lossi L, Ghidella S, Marroni P, Merighi A (1995) The neurochemical maturation of the rabbit cerebellum. J Anat 187:709–22

    CAS  PubMed Central  PubMed  Google Scholar 

  • Low VF, Faull RLM, Bennet L, Gunn AJ, Curtis MA (2013) Neurogenesis and progenitor cell distribution in the subgranular zone and subventricular zone of the adult sheep brain. Neurosci 244:173–187

    Article  CAS  Google Scholar 

  • Marshall CAG, Suzuki SO, Goldman JE (2003) Gliogenic and neurogenic progenitors of the subventricular zone: who are they, where did they come from, and where are they going? Glia 43:52–61

    Article  PubMed  Google Scholar 

  • Meyer-franke A, Shen S, Barres BA (1999) Astrocytes induce oligodendrocyte processes to align with and adhere to axons. Mol Cell Neurosci 14:385–397

    Article  CAS  PubMed  Google Scholar 

  • Miller R, Raff M (1984) Fibrous and protoplasmic astrocytes are biochemically and developmentally distinct. J Neurosci 4:585–592

    CAS  PubMed  Google Scholar 

  • Montgomery DL (1994) Astrocytes: form, functions, and roles in disease. Vet Pathol 31:145–167

    Article  CAS  PubMed  Google Scholar 

  • Naruse M, Shibasaki K, Yokoyama S, Kurachi M, Ishizaki Y (2013) Dynamic changes of CD44 expression from progenitors to subpopulations of astrocytes and neurons in developing cerebellum. PLoS ONE 8:e53109

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pringle NP, Yu WP, Howell M, Colvin JS, Ornitz DM, Richardson WD (2003) Fgfr3 expression by astrocytes and their precursors: evidence that astrocytes and oligodendrocytes originate in distinct neuroepithelial domains. Development 130:93–102

  • Quinlan RA, Brenner M, Goldman JE, Messing A (2007) GFAP and its role in Alexander disease. Exp Cell Res 313:2077–2087

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rees S, Stringer M, Just Y, Hooper SB, Harding R (1997) The vulnerability of the foetal sheep brain to hypoxemia at mid-gestation. Brain research. Dev Brain Res 103:103–118

    Article  CAS  Google Scholar 

  • Reichenbach A, Derouiche A, Kirchhoff F (2010) Morphology and dynamics of perisynaptic glia. Brain Res Rev 63:11–25

    Article  PubMed  Google Scholar 

  • Salouci M, Engelen V, Gyan M, Antoine N, Jacqmot O, Mignon Y, Kirschvink N, Gabriel A (2012) Development of purkinje cells in the ovine brain. Anat Histol Embryol 41:227–232

    Article  CAS  PubMed  Google Scholar 

  • Seri B, Garcia-verdugo JM, Mcewen BS, Alvarez-buylla A (2001) Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 21:7153–60

    CAS  PubMed  Google Scholar 

  • Shibasaki K, Ishizaki Y, Mandadi S (2013) Astrocytes express functional TRPV2 ion channels. Biochem Biophys Res Commun 441:327–332

    Article  CAS  PubMed  Google Scholar 

  • Shibasaki K, Ikenaka K, Tamalu F, Tominaga M, Ishizaki Y (2014) A novel subtype of astrocytes expressing TRPV4 (transient receptor potential vanilloid 4) regulates neuronal excitability via release of gliotransmitters. J Biol Chem 289:14470–14480

    Article  CAS  PubMed  Google Scholar 

  • Slezak M, Pfrieger FW, Soltys Z (2006) Synaptic plasticity, astrocytes and morphological homeostasis. J Physiol Paris 99:84–91

    Article  CAS  PubMed  Google Scholar 

  • Steiner J, Bernstein H-G, Bielau H, Berndt A, Brisch R, Mawrin C, Keilhoff G, Bogerts B (2007) Evidence for a wide extra-astrocytic distribution of S100B in human brain. BMC Neurosci 8:2

    Article  PubMed Central  PubMed  Google Scholar 

  • Strackx E, Gantert M, Moers V, Kooten IJ, RiekE R, Hürter H, Lemmens MM, Steinbusch HM, Zimmermann LJI, Vles JH, Garnier Y, Gavilanes AD, Kramer B (2012) Increased number of cerebellar granule cells and astrocytes in the internal granule layer in sheep following prenatal intra-amniotic injection of lipopolysaccharide. Cerebellum 11:132–144

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Taft JR, Vertes RP, Perry GW (2005) Distribution of GFAP+ astrocytes in adult and neonatal rat brain. Int J Neurosci 115:1333–1343

    Article  CAS  PubMed  Google Scholar 

  • Ullian EM, Christopherson KS, Barres BA (2004) Role for glia in synaptogenesis. Glia 47:209–16

    Article  PubMed  Google Scholar 

  • Watkins TA, Emery B, Mulinyawe S, Barres BA (2008) Distinct stages of myelination regulated by gamma-secretase and astrocytes in a rapidly myelinating CNS coculture system. Neuron 60:555–69

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wolburg H, Noell S, Mack A, Wolburg-buchholz K, Fallier-becker P (2009) Brain endothelial cells and the glio-vascular complex. Cell Tissue Res 335:75–96

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank the Federation Wallonie-Brussels for financial support.

Conflict of interest

None of the authors of this paper has a financial or personal relationship with other persons or organizations that could inappropriately influence or bias the content of the paper.

Author information

Authors and Affiliations

  1. Department of Morphology and Pathology, University of Liège, Boulevard de Colonster 20, 4000, Liège, Sart Tilman, Belgium

    Moustafa Salouci, Nadine Antoine, Mohamad Khir Shikh Al Sook, Joëlle Piret, Yvan Mignon & Annick Gabriel

  2. Veterinary Department, NARILIS (Namur Research Institute for Life Sciences), University of Namur (UNamur), Rue de Bruxelles 61, B-5000, Namur, Belgium

    Nathalie Kirschvink

Authors
  1. Moustafa Salouci
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nadine Antoine
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mohamad Khir Shikh Al Sook
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Joëlle Piret
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yvan Mignon
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Nathalie Kirschvink
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Annick Gabriel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Moustafa Salouci.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Salouci, M., Antoine, N., Shikh Al Sook, M.K. et al. Developmental profiles of GFAP-positive astrocytes in sheep cerebellum. Vet Res Commun 38, 279–285 (2014). https://doi.org/10.1007/s11259-014-9614-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11259-014-9614-1

Keywords

Search

Navigation