Drosophila gene tao-1 encodes proteins with and without a Ste20 kinase domain that affect cytoskeletal architecture and cell migration differently

Open Biol. 2015 Jan;5(1):140161. doi: 10.1098/rsob.140161.

Abstract

Tao-1, the single representative of the Sterile 20 kinase subfamily in Drosophila, is best known for destabilizing microtubules at the actin-rich cortex, regulating the cytoskeletal architecture of cells. More recently, Tao-1 was shown to act in the Salvador-Warts-Hippo pathway by phosphorylating Hippo, regulating cell growth as well as cell polarity. Here, we show that tao-1 encodes two proteins, one with the Sterile 20 kinase domain (Tao-L) and one without it (Tao-S), and that they act in an antagonistic manner. Tao-L expression causes lamellipodia-like cell protrusions, whereas Tao-S expression results in filopodia-like structures that make cells stick to the surface they attach to. Ectopic Tao-1 expression in the anterior region of Drosophila embryos results in pole cell formation as normally observed at the posterior end. Tao-S expression causes primordial germ cells (PGCs) to adhere to the inner wall of the gut primordia and prevents proper transepithelial migration to the gonads. Conversely, RNAi knockdowns of Tao-1 cause disordered migration of PGCs out of the gut epithelium, their dispersal within the embryo and cell death. The results reveal a novel function of Tao-1 in cell migration, which is based on antagonistic activities of two proteins encoded by a single gene.

Keywords: Ste20 kinase; cytoskeletal architecture; ectopic pole cell induction; germline cell migration.

MeSH terms

  • Actin Cytoskeleton / metabolism*
  • Animals
  • Cell Movement*
  • Cell Surface Extensions / metabolism
  • Drosophila / embryology
  • Drosophila / genetics
  • Drosophila / metabolism*
  • Germ Cells / metabolism
  • Germ Cells / physiology
  • MAP Kinase Kinase Kinases / chemistry
  • MAP Kinase Kinase Kinases / genetics
  • MAP Kinase Kinase Kinases / metabolism*
  • Protein Binding
  • Protein Serine-Threonine Kinases
  • Protein Structure, Tertiary

Substances

  • Protein Serine-Threonine Kinases
  • TAO1 protein kinase
  • MAP Kinase Kinase Kinases