Motor regulation results in distal forces that bend partially disintegrated Chlamydomonas axonemes into circular arcs

Biophys J. 2014 Jun 3;106(11):2434-42. doi: 10.1016/j.bpj.2014.03.046.

Abstract

The bending of cilia and flagella is driven by forces generated by dynein motor proteins. These forces slide adjacent microtubule doublets within the axoneme, the motile cytoskeletal structure. To create regular, oscillatory beating patterns, the activities of the axonemal dyneins must be coordinated both spatially and temporally. It is thought that coordination is mediated by stresses or strains, which build up within the moving axoneme, and somehow regulate dynein activity. During experimentation with axonemes subjected to mild proteolysis, we observed pairs of doublets associating with each other and forming bends with almost constant curvature. By modeling the statics of a pair of filaments, we show that the activity of the motors concentrates at the distal tips of the doublets. Furthermore, we show that this distribution of motor activity accords with models in which curvature, or curvature-induced normal forces, regulates the activity of the motors. These observations, together with our theoretical analysis, provide evidence that dynein activity can be regulated by curvature or normal forces, which may, therefore, play a role in coordinating the beating of cilia and flagella.

MeSH terms

  • Adenosine Triphosphate / metabolism
  • Axonemal Dyneins / chemistry*
  • Axonemal Dyneins / metabolism
  • Axoneme / metabolism*
  • Axoneme / ultrastructure
  • Chlamydomonas reinhardtii / metabolism*
  • Models, Biological*
  • Shear Strength
  • Tensile Strength

Substances

  • Adenosine Triphosphate
  • Axonemal Dyneins