Advertisement

Brain Structure and Function

, Volume 223, Issue 9, pp 3909–3917 | Cite as

Radial glial elements in the cerebral cortex of the lesser hedgehog tenrec

  • Andreas F. Mack
  • Heinz Künzle
  • Mario Lange
  • Bianca Mages
  • Andreas Reichenbach
  • Wolfgang Härtig
Original Article
  • 130 Downloads

Abstract

We investigated astroglial cells in several areas of the telencephalic cortex of the lesser hedgehog tenrec (Echinops telfairi). Compared to other mammals, the cortex of the tenrec has a relatively large paleocortex and a low encephalization index. We stained sections from tenrec forebrains with structural and functional glia markers focusing on selected cortical areas, the paleocortex, rhinal cortex, neocortex and the dentate gyrus of the hippocampal formation. We found that in all parts of the tenrec forebrain cortex, radial processes exist which are positive for glial fibrillary acidic protein (GFAP) although with differential localization: in the rhinal cortex and neocortical region radial glial fibers are located in the subventricular regions, whereas in the dentate gyrus and paleocortex they appear to arise from the cells in the respective granular layers. The relatively high abundance of the radial fibers in layer III of the paleocortex was very conspicuous. Only few of these radial processes were also co-labeled with doublecortin (DCX), yet most of the DCX-positive cells were negative for GFAP. The GFAP-positive radial fibers were in turn neither positive for glutamine synthetase, nor did they show immunoreactivity for the astroglia-specific water channel aquaporin-4 (AQP4). Star-shaped astrocytes, however, displayed the typical perivascular and subpial expression patterns for AQP4. We conclude that the radial glia in the adult tenrec represents an immature form of astroglia that persists in these animals throughout life.

Keywords

Astrocytes Glia evolution Aquaporin-4 Afrotheria 

Notes

Acknowledgements

The authors wish to thank Dr. Jens Grosche, Ms. Ute Bauer and Dr. Yulia Popkova (all from Leipzig University), and Karin Tiedemann (Tübingen) for excellent technical assistance.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. As outlined in the “Materials and methods” the brain tissue used in this study was derived from previous studies which were in line with the ethical guidelines of the laboratory animal care and use committee at the University of Munich and were approved by the administration of Upper Bavaria (License no. 55.2-1-54-2531-85-05). This article does not contain any studies with human participants performed by any of the authors.

References

  1. Alpar A et al (2010) Slow age-dependent decline of doublecortin expression and BrdU labeling in the forebrain from lesser hedgehog tenrecs. Brain Res 1330:9–19.  https://doi.org/10.1016/j.brainres.2010.03.026 CrossRefPubMedGoogle Scholar
  2. Arendt T et al (2003) Reversible paired helical filament-like phosphorylation of tau is an adaptive process associated with neuronal plasticity in hibernating animals. J Neurosci 23:6972–6981  CrossRefGoogle Scholar
  3. Averianov AO, Lopatin AV (2014) High-level systematics of placental mammals: current status of the problem. Biol Bull 41:801–816.  https://doi.org/10.1134/s1062359014090039 CrossRefGoogle Scholar
  4. Barry G et al (2008) Specific glial populations regulate hippocampal morphogenesis. J Neurosci 28:12328–12340.  https://doi.org/10.1523/JNEUROSCI.4000-08.2008 CrossRefPubMedGoogle Scholar
  5. Bentivoglio M, Mazzarello P (1999) The history of radial glia. Brain Res Bull 49:305–315.  https://doi.org/10.1016/S0361-9230(99)00065-9 CrossRefPubMedGoogle Scholar
  6. Campbell K, Götz M (2002) Radial glia: multi-purpose cells for vertebrate brain development. Trends Neurosci 25:235–238CrossRefGoogle Scholar
  7. Colombo JA (2017) The interlaminar glia: from serendipity to hypothesis. Brain Struct Funct 222:1109–1129.  https://doi.org/10.1007/s00429-016-1332-8 CrossRefPubMedGoogle Scholar
  8. Colombo JA, Yáñez A, Puissant V, Lipina S (1995) Long, interlaminar astroglial cell processes in the cortex of adult monkeys. J Neurosci Res 40:551–556.  https://doi.org/10.1002/jnr.490400414 CrossRefPubMedGoogle Scholar
  9. Colombo JA, Fuchs E, Härtig W, Marotte LR, Puissant V (2000) “Rodent-like” and “primate-like” types of astroglial architecture in the adult cerebral cortex of mammals: a comparative study. Anat Embryol 201:111–120.  https://doi.org/10.1007/pl00008231 CrossRefPubMedGoogle Scholar
  10. Fallier-Becker P, Vollmer JP, Bauer H-C, Noell S, Wolburg H, Mack AF (2014) Onset of aquaporin-4 expression in the developing mouse brain. Int J Dev Neurosci 36:81–89.  https://doi.org/10.1016/j.ijdevneu.2014.06.001 CrossRefPubMedGoogle Scholar
  11. Gleiser C, Wagner A, Fallier-Becker P, Wolburg H, Hirt B, Mack A (2016) Aquaporin-4 in astroglial cells in the CNS and supporting cells of sensory organs—a comparative perspective. Int J Mol Sci 17:1411CrossRefGoogle Scholar
  12. Götz M, Huttner WB (2005) The cell biology of neurogenesis. Nat Rev Mol Cell Biol 6:777–788CrossRefGoogle Scholar
  13. Grupp L, Wolburg H, Mack AF (2010) Astroglial structures in the zebrafish brain. J Comp Neurol 518:4277–4287CrossRefGoogle Scholar
  14. Gubert F, Zaverucha-Do-Valle C, Pimentel-Coelho PM, Mendez-Otero R, Santiago MF (2009) Radial glia-like cells persist in the adult rat brain. Brain Res 1258:43–52CrossRefGoogle Scholar
  15. Härtig W, Brückner G, Holzer M, Brauer K, Bigl V (1995) Digoxigenylated primary antibodies for sensitive dual-peroxidase labelling of neural markers. Histochem Cell Biol 104:467–472.  https://doi.org/10.1007/bf01464337 CrossRefPubMedGoogle Scholar
  16. Hartline DK (2011) The evolutionary origins of glia. Glia 59:1215–1236.  https://doi.org/10.1002/glia.21149 CrossRefPubMedGoogle Scholar
  17. Hatten ME (1999) Central nervous system neuronal migration. Annu Rev Neurosci 22:511–539CrossRefGoogle Scholar
  18. Kálmán M (1998) Astroglial architecture of the carp (Cyprinus carpio) brain as revealed by immunohistochemical staining against glial fibrillary acidic protein (GFAP). Anat Embryol 198:409–433CrossRefGoogle Scholar
  19. Krubitzer L, Künzle H, Kaas J (1997) Organization of sensory cortex in a Madagascan insectivore, the tenrec (Echinops telfairi). J Comp Neurol 379:399–414  https://doi.org/10.1002/(sici)1096-9861(19970317)379:3%3C399::aid-cne6%3E3.0.co;2-z CrossRefPubMedGoogle Scholar
  20. Künzle H, Radtke-Schuller S (2000) The subrhinal paleocortex in the hedgehog tenrec: a multiarchitectonic characterization and an analysis of its connections with the olfactory bulb. Anat Embryol 202:491–506.  https://doi.org/10.1007/s004290000137 CrossRefPubMedGoogle Scholar
  21. Künzle H, Rehkämper G (1992) Distribution of cortical neurons projecting to dorsal column nuclear complex and spinal cord in the hedgehog tenrec, Echinops telfairi. Somatosens Motor Res 9:185–197.  https://doi.org/10.3109/08990229209144770 CrossRefGoogle Scholar
  22. Mack AF, Wolburg H (2013) A Novel Look at astrocytes: aquaporins, ionic homeostasis, and the role of the microenvironment for regeneration in the CNS. Neurosci 19:195–207.  https://doi.org/10.1177/1073858412447981 CrossRefGoogle Scholar
  23. Mack AF, Germer A, Janke C, Reichenbach A (1998) Müller (glial) cells in the teleost retina: consequences of continuous growth. Glia 22:306–313CrossRefGoogle Scholar
  24. Malatesta P, Appolloni I, Calzolari F (2008) Radial glia and neural stem cells. Cell Tissue Res 331:165–178CrossRefGoogle Scholar
  25. Mashanov VS, Zueva OR, Garcia-Arraras JE (2013) Radial glial cells play a key role in echinoderm neural regeneration. BMC Biol 11:49.  https://doi.org/10.1186/1741-7007-11-49 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Morawski M, Brückner G, Jäger C, Seeger G, Künzle H, Arendt T (2010) Aggrecan-based extracellular matrix shows unique cortical features and conserved subcortical principles of mammalian brain organization in the Madagascan lesser hedgehog tenrec (Echinops telfairi Martin, 1838). Neuroscience 165:831–849.  https://doi.org/10.1016/j.neuroscience.2009.08.018 CrossRefPubMedGoogle Scholar
  27. Nielsen S, Arnulf Nagelhus E, Amiry-Moghaddam M, Bourque C, Agre P, Petter Ottersen O (1997) Specialized membrane domains for water transport in glial cells: high-resolution immunogold cytochemistry of aquaporin-4 in rat. Brain J Neurosci 17:171–180CrossRefGoogle Scholar
  28. O’Leary MA et al (2013) The placental mammal ancestor and the post-k-Pg radiation of placentals. Science 339:662–667.  https://doi.org/10.1126/science.1229237 CrossRefPubMedGoogle Scholar
  29. Papadopoulos MC, Verkman AS (2013) Aquaporin water channels in the nervous system. Nat Rev Neurosci 14:265–277.  https://doi.org/10.1038/nrn3468 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Patzke N et al (2014) The distribution of doublecortin-immunopositive cells in the brains of four afrotherian mammals: the hottentot golden mole (Amblysomus hottentotus), the rock hyrax (Procavia capensis), the eastern rock sengi (Elephantulus myurus) and the four-toed sengi (Petrodromus tetradactylus). Brain Behav Evol 84:227–241CrossRefGoogle Scholar
  31. Rakic P (1981) Neuronal-glial interaction during brain development. Trends Neurosci 4:184–187CrossRefGoogle Scholar
  32. Ramón y Cajal S (1895) Elementos de Histologìa normal. Imprente y Liberìa de Nicolas Moya, Madrid, pp 396–397  Google Scholar
  33. Rowitch DH, Kriegstein AR (2010) Developmental genetics of vertebrate glial-cell specification. Nature 468:214–222CrossRefGoogle Scholar
  34. Seki T, Arai Y (1999) Different polysialic acid-neural cell adhesion molecule expression patterns in distinct types of mossy fiber boutons in the adult hippocampus. J Comp Neurol 410:115–125CrossRefGoogle Scholar
  35. Sild M, Ruthazer ES (2011) Radial glia: progenitor, pathway partner. Neuroscience 17:288–302.  https://doi.org/10.1177/1073858410385870 CrossRefGoogle Scholar
  36. Stephan H, Baron G, Frahm H (1991) Comparative brain characteristics. In: Insectivora. Comparative brain research in mammals, vol 1. Springer, New YorkGoogle Scholar
  37. Weissman T, Noctor SC, Clinton BK, Honig LS, Kriegstein AR (2003) Neurogenic radial glial cells in reptile, rodent and human: from mitosis to migration. Cereb Cortex 13:550–559.  https://doi.org/10.1093/cercor/13.6.550 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Institute of Clinical Anatomy and Cell AnalysisEberhard Karls University TübingenTübingenGermany
  2. 2.Institute of AnatomyLudwigs Maximilian University MunichMunichGermany
  3. 3.Paul Flechsig Institute for Brain ResearchUniversity of LeipzigLeipzigGermany
  4. 4.Department of NeurologyUniversity of LeipzigLeipzigGermany

Personalised recommendations