Early evolution of radial glial cells in Bilateria.

Conrad Helm, Anett Karl, Patrick Beckers, Sabrina Kaul-Strehlow, Elke Ulbricht, Ioannis Kourtesis, Heidrun Kuhrt, Harald Hausen, Thomas Bartolomaeus, Andreas Reichenbach, Christoph Bleidorn
Author Information
  1. Conrad Helm: Sars International Center for Marine Molecular Biology, University of Bergen, 5008 Bergen, Norway conrad.helm@uib.no. ORCID
  2. Anett Karl: Paul-Flechsig-Institute for Brain Research, University of Leipzig, 04103 Leipzig, Germany.
  3. Patrick Beckers: Institute of Evolutionary Biology and Ecology, University of Bonn, 53121 Bonn, Germany.
  4. Sabrina Kaul-Strehlow: Department of Integrative Biology, University of Vienna, 1090 Vienna, Austria.
  5. Elke Ulbricht: Biotechnology Center, Technische Universität Dresden, 01307 Dresden, Germany.
  6. Ioannis Kourtesis: Sars International Center for Marine Molecular Biology, University of Bergen, 5008 Bergen, Norway.
  7. Heidrun Kuhrt: Paul-Flechsig-Institute for Brain Research, University of Leipzig, 04103 Leipzig, Germany.
  8. Harald Hausen: Sars International Center for Marine Molecular Biology, University of Bergen, 5008 Bergen, Norway.
  9. Thomas Bartolomaeus: Institute of Evolutionary Biology and Ecology, University of Bonn, 53121 Bonn, Germany. ORCID
  10. Andreas Reichenbach: Paul-Flechsig-Institute for Brain Research, University of Leipzig, 04103 Leipzig, Germany.
  11. Christoph Bleidorn: Museo Nacional de Ciencias Naturales, Spanish National Research Council (CSIC), 28006 Madrid, Spain christoph.bleidorn@gmail.com.

Abstract

Bilaterians usually possess a central nervous system, composed of neurons and supportive cells called glial cells. Whereas neuronal cells are highly comparable in all these animals, glial cells apparently differ, and in deuterostomes, radial glial cells are found. These particular secretory glial cells may represent the archetype of all (macro) glial cells and have not been reported from protostomes so far. This has caused controversial discussions of whether glial cells represent a homologous bilaterian characteristic or whether they (and thus, centralized nervous systems) evolved convergently in the two main clades of bilaterians. By using histology, transmission electron microscopy, immunolabelling and whole-mount hybridization, we show here that protostomes also possess radial glia-like cells, which are very likely to be homologous to those of deuterostomes. Moreover, our antibody staining indicates that the secretory character of radial glial cells is maintained throughout their various evolutionary adaptations. This implies an early evolution of radial glial cells in the last common ancestor of Protostomia and Deuterostomia. Furthermore, it suggests that an intraepidermal nervous system-composed of sensory cells, neurons and radial glial cells-was probably the plesiomorphic condition in the bilaterian ancestor.

Keywords

References

  1. Glia. 2000 Nov;32(2):177-91 [PMID: 11008217]
  2. Philos Trans R Soc Lond B Biol Sci. 2015 Dec 19;370(1684):null [PMID: 26554050]
  3. Front Zool. 2009 Jun 18;6:11 [PMID: 19538733]
  4. Brain Res Mol Brain Res. 2003 Feb 20;110(2):177-92 [PMID: 12591155]
  5. Nat Neurosci. 2002 Apr;5(4):308-15 [PMID: 11896398]
  6. Science. 2008 Oct 31;322(5902):693-4 [PMID: 18974341]
  7. Glia. 2015 Aug;63(8):1303-19 [PMID: 25808466]
  8. Nucleic Acids Res. 2015 Jan;43(Database issue):D257-60 [PMID: 25300481]
  9. Nat Rev Mol Cell Biol. 2005 Oct;6(10):777-88 [PMID: 16314867]
  10. Glia. 2011 Sep;59(9):1215-36 [PMID: 21584869]
  11. Ann N Y Acad Sci. 1965 Nov 30;118(24):1038-51 [PMID: 5221050]
  12. Neuron. 2005 May 5;46(3):369-72 [PMID: 15882633]
  13. BMC Biol. 2013 Apr 18;11:49 [PMID: 23597108]
  14. Proc Natl Acad Sci U S A. 1998 May 26;95(11):5857-64 [PMID: 9600884]
  15. Philos Trans R Soc Lond B Biol Sci. 2015 Dec 19;370(1684):null [PMID: 26554039]
  16. Nat Rev Neurosci. 2016 Jan;17(1):61-72 [PMID: 26675821]
  17. Front Cell Neurosci. 2013 Jun 03;7:80 [PMID: 23761733]
  18. Nat Biotechnol. 2011 May 15;29(7):644-52 [PMID: 21572440]
  19. Mol Biol Evol. 2016 Aug;33(8):1921-36 [PMID: 27189557]
  20. Proc Natl Acad Sci U S A. 2011 Jan 25;108(4):1513-8 [PMID: 21187386]
  21. Acta Histochem. 2001 Feb;103(1):99-112 [PMID: 11252633]
  22. Front Zool. 2010 Nov 09;7:29 [PMID: 21062451]
  23. Evodevo. 2013 Oct 07;4(1):27 [PMID: 24098981]
  24. Evodevo. 2015 Jan 13;6:1 [PMID: 25905000]
  25. Nature. 2014 Jun 5;510(7503):109-14 [PMID: 24847885]
  26. Nature. 2016 Feb 4;530(7588):89-93 [PMID: 26842059]
  27. Glia. 2010 Oct;58(13):1581-93 [PMID: 20578040]
  28. Evodevo. 2015 Dec 22;6:40 [PMID: 26702352]
  29. Microsc Res Tech. 2001 Mar 1;52(5):552-63 [PMID: 11241865]
  30. Z Zellforsch Mikrosk Anat. 1962;56:573-94 [PMID: 13864982]
  31. BMC Evol Biol. 2016 Jun 16;16(1):129 [PMID: 27306767]
  32. Curr Biol. 2015 Sep 21;25(18):R782-6 [PMID: 26394095]
  33. Evodevo. 2012 Oct 01;3(1):23 [PMID: 23020891]
  34. Nat Rev Neurosci. 2001 Apr;2(4):287-93 [PMID: 11283751]
  35. J Exp Biol. 2015 Feb 15;218(Pt 4):598-611 [PMID: 25696823]
  36. Front Zool. 2016 Feb 08;13:5 [PMID: 26862347]
  37. Int J Biochem Cell Biol. 2004 Oct;36(10):1861-7 [PMID: 15203098]
  38. J Cell Sci. 1996 May;109 ( Pt 5):1053-61 [PMID: 8743952]
  39. Neuroscientist. 2011 Jun;17(3):288-302 [PMID: 21558559]
  40. Microsc Res Tech. 1998 Apr 15;41(2):98-123 [PMID: 9579598]
  41. Nucleic Acids Res. 1997 Sep 1;25(17):3389-402 [PMID: 9254694]
  42. Glia. 2003 Jul;43(1):37-43 [PMID: 12761864]

MeSH Term

Animals
Biological Evolution
Central Nervous System
Ependymoglial Cells
Neuroglia
Neurons

Word Cloud

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