Microcephaly models in the developing zebrafish retinal neuroepithelium point to an underlying defect in metaphase progression

Open Biol. 2013 Oct 23;3(10):130065. doi: 10.1098/rsob.130065.

Abstract

Autosomal recessive primary microcephaly (MCPH) is a congenital disorder characterized by significantly reduced brain size and mental retardation. Nine genes are currently known to be associated with the condition, all of which encode centrosomal or spindle pole proteins. MCPH is associated with a reduction in proliferation of neural progenitors during fetal development. The cellular mechanisms underlying the proliferation defect, however, are not fully understood. The zebrafish retinal neuroepithelium provides an ideal system to investigate this question. Mutant or morpholino-mediated knockdown of three known MCPH genes (stil, aspm and wdr62) and a fourth centrosomal gene, odf2, which is linked to several MCPH proteins, results in a marked reduction in head and eye size. Imaging studies reveal a dramatic rise in the fraction of proliferating cells in mitosis in all cases, and time-lapse microscopy points to a failure of progression through prometaphase. There was also increased apoptosis in all the MCPH models but this appears to be secondary to the mitotic defect as we frequently saw mitotically arrested cells disappear, and knocking down p53 apoptosis did not rescue the mitotic phenotype, either in whole retinas or clones.

Keywords: ASPM; ODF2; STIL; WDR62; microcephaly; zebrafish retina.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis / genetics
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism
  • Cell Line, Transformed
  • Disease Models, Animal
  • Embryonic Development
  • Evolution, Molecular
  • Eye Abnormalities / embryology
  • Eye Abnormalities / genetics
  • Eye Abnormalities / metabolism
  • Gene Knockdown Techniques
  • Genes, p53
  • Head / abnormalities
  • Head / embryology
  • Humans
  • Metaphase*
  • Microcephaly / genetics
  • Microcephaly / metabolism
  • Microcephaly / physiopathology
  • Mitosis / genetics
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism
  • Retina / cytology
  • Retina / embryology*
  • Retina / metabolism*
  • Retinal Neurons / cytology
  • Retinal Neurons / metabolism
  • Stem Cells / cytology
  • Time-Lapse Imaging
  • Zebrafish / embryology
  • Zebrafish / genetics
  • Zebrafish / metabolism*
  • Zebrafish Proteins / genetics*
  • Zebrafish Proteins / metabolism*

Substances

  • ASPM protein, zebrafish
  • Cell Cycle Proteins
  • Nerve Tissue Proteins
  • Stil protein, zebrafish
  • Zebrafish Proteins

Supplementary concepts

  • Autosomal Recessive Primary Microcephaly