Regulation of dynein localization and centrosome positioning by Lis-1 and asunder during Drosophila spermatogenesis

Development. 2012 Aug;139(16):2945-54. doi: 10.1242/dev.077511. Epub 2012 Jul 4.

Abstract

Dynein, a microtubule motor complex, plays crucial roles in cell-cycle progression in many systems. The LIS1 accessory protein directly binds dynein, although its precise role in regulating dynein remains unclear. Mutation of human LIS1 causes lissencephaly, a developmental brain disorder. To gain insight into the in vivo functions of LIS1, we characterized a male-sterile allele of the Drosophila homolog of human LIS1. We found that centrosomes do not properly detach from the cell cortex at the onset of meiosis in most Lis-1 spermatocytes; centrosomes that do break cortical associations fail to attach to the nucleus. In Lis-1 spermatids, we observed loss of attachments between the nucleus, basal body and mitochondria. The localization pattern of LIS-1 protein throughout Drosophila spermatogenesis mirrors that of dynein. We show that dynein recruitment to the nuclear surface and spindle poles is severely reduced in Lis-1 male germ cells. We propose that Lis-1 spermatogenesis phenotypes are due to loss of dynein regulation, as we observed similar phenotypes in flies null for Tctex-1, a dynein light chain. We have previously identified asunder (asun) as another regulator of dynein localization and centrosome positioning during Drosophila spermatogenesis. We now report that Lis-1 is a strong dominant enhancer of asun and that localization of LIS-1 in male germ cells is ASUN dependent. We found that Drosophila LIS-1 and ASUN colocalize and coimmunoprecipitate from transfected cells, suggesting that they function within a common complex. We present a model in which Lis-1 and asun cooperate to regulate dynein localization and centrosome positioning during Drosophila spermatogenesis.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism*
  • Centrosome / metabolism
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism*
  • Drosophila melanogaster / genetics
  • Drosophila melanogaster / growth & development
  • Drosophila melanogaster / metabolism
  • Dynactin Complex
  • Dyneins / genetics
  • Dyneins / metabolism*
  • Humans
  • Male
  • Microtubule-Associated Proteins / genetics
  • Microtubule-Associated Proteins / metabolism*
  • Models, Biological
  • Phenotype
  • Spermatids / metabolism
  • Spermatids / ultrastructure
  • Spermatocytes / metabolism
  • Spermatocytes / ultrastructure
  • Spermatogenesis / genetics
  • Spermatogenesis / physiology*

Substances

  • Cell Cycle Proteins
  • Drosophila Proteins
  • Dynactin Complex
  • Lis-1 protein, Drosophila
  • Microtubule-Associated Proteins
  • asun protein, Drosophila
  • Dyneins