Members of the NIMA-related kinase family promote disassembly of cilia by multiple mechanisms

Mol Biol Cell. 2006 Jun;17(6):2799-810. doi: 10.1091/mbc.e05-05-0450. Epub 2006 Apr 12.

Abstract

The genome of Tetrahymena thermophila contains 39 loci encoding NIMA-related kinases (NRKs), an extraordinarily large number for a unicellular organism. Evolutionary analyses grouped these sequences into several subfamilies, some of which have orthologues in animals, whereas others are protist specific. When overproduced, NRKs of three subfamilies caused rapid shortening of cilia. Ultrastructural studies revealed that each NRK triggered ciliary resorption by a distinct mechanism that involved preferential depolymerization of a subset of axonemal microtubules, at either the distal or proximal end. Overexpression of a kinase-inactive variant caused lengthening of cilia, indicating that constitutive NRK-mediated resorption regulates the length of cilia. Each NRK preferentially resorbed a distinct subset of cilia, depending on the location along the anteroposterior axis. We also show that normal Tetrahymena cells maintain unequal length cilia. We propose that ciliates used a large number of NRK paralogues to differentially regulate the length of specific subsets of cilia in the same cell.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Cell Cycle Proteins / classification
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism*
  • Cilia / physiology*
  • Genes, Protozoan
  • Genes, Reporter
  • Genome
  • Green Fluorescent Proteins / genetics
  • NIMA-Related Kinase 1
  • Phylogeny
  • Protein-Serine-Threonine Kinases / classification
  • Protein-Serine-Threonine Kinases / genetics
  • Protein-Serine-Threonine Kinases / metabolism*
  • Protozoan Proteins / chemistry
  • Protozoan Proteins / metabolism
  • Tetrahymena thermophila / physiology
  • Tetrahymena thermophila / ultrastructure

Substances

  • Cell Cycle Proteins
  • Protozoan Proteins
  • Green Fluorescent Proteins
  • NIMA-Related Kinase 1
  • Protein-Serine-Threonine Kinases