Mitral cell development in the olfactory bulb of sharks: evidences of a conserved pattern of glutamatergic neurogenesis

Brain Struct Funct. 2019 Sep;224(7):2325-2341. doi: 10.1007/s00429-019-01906-9. Epub 2019 Jun 15.

Abstract

In mammals, the development of the olfactory bulb (OB) relies in part on the expression of transcription factors involved in the specifications/differentiation of glutamatergic cells. In a previous study from our group, a high molecular similarity was reported between mammals and cartilaginous fishes regarding the neurogenic mechanisms underlying the development of glutamatergic cells in the telencephalon. However, information about the transcriptional program operating in the development of the glutamatergic system (mainly represented by mitral cells) in the OB is lacking in the catshark Scyliorhinus canicula, a cartilaginous fish. Using immunohistochemistry and in situ hybridization techniques, we have found that, previously to the appearance of the olfactory primordium (OP), proliferating cells expressing Pax6 with molecular hallmarks of progenitor radial glia were located in the ventrolateral pallial ventricular zone. Later in development, when the OP is recognizable, a stream of Pax6-positive cells were observed between the ventricular zone and the OP, where transcription factors involved in mitral cell development in mammals (ScTbr2, ScNeuroD, Tbr1) are expressed. Later in development, these transcription factors became expressed in a layered-like structure where ScVglut1, a marker of mitral cells, is also present. Our data suggest that the transcriptional program related with the specification/differentiation of glutamatergic cells in the telencephalon has been conserved throughout the evolution of vertebrates. These results, in combination with previous studies concerning GABAergic neurogenesis in sharks, have evidenced that the OB of mammals and sharks shares similarities in the timing and molecular programs of development.

Keywords: Catshark; Development; Glutamatergic lineage; Mitral cells; Olfactory bulb; Pax6.

MeSH terms

  • Animals
  • Cell Differentiation / physiology*
  • Cell Movement / physiology
  • Cell Proliferation / physiology
  • Eye Proteins / metabolism
  • Homeodomain Proteins / metabolism
  • Neural Stem Cells / metabolism*
  • Neurogenesis / physiology*
  • Olfactory Bulb / metabolism*
  • Paired Box Transcription Factors / metabolism
  • Sharks / metabolism
  • Telencephalon / metabolism

Substances

  • Eye Proteins
  • Homeodomain Proteins
  • Paired Box Transcription Factors