Katanin disrupts the microtubule lattice and increases polymer number in C. elegans meiosis.
Katanin is a heterodimer that exhibits ATP-dependent microtubule-severing activity in vitro. In Xenopus egg extracts, katanin activity correlates with the addition of cyclin B/cdc2, suggesting a role for microtubule severing in the disassembly of long interphase microtubules as the cell prepares for mitosis. However, studies from plant cells, cultured neurons, and nematode embryos suggest that katanin could be required for the organization or postnucleation processing of microtubules, rather than the dissolution of microtubule structures. Here we reexamine katanin's role by studying acentrosomal female meiotic spindles in C. elegans embryos. In mutant embryos lacking katanin, microtubules form around meiotic chromatin but do not organize into bipolar spindles. By using electron tomography, we found that katanin converts long microtubule polymers into shorter microtubule fragments near meiotic chromatin. We further show that turning on katanin during mitosis also creates a large pool of short microtubules near the centrosome. Furthermore, the identification of katanin-dependent microtubule lattice defects supports a mechanism involving an initial perforation of the protofilament wall. Taken together, our data suggest that katanin is used during meiotic spindle assembly to increase polymer number from a relatively inefficient chromatin-based microtubule nucleation pathway.
Srayko
Martin
M
Max Planck Institute of Molecular Cell Biology and Genetics, D-01307 Dresden, Germany.
O'toole
Eileen T
ET
Hyman
Anthony A
AA
Müller-Reichert
Thomas
T
D000251:Adenosine Triphosphatases / Q000235:genetics / Q000502:physiology*; D000818:Animals; D017173:Caenorhabditis elegans / Q000166:cytology / Q000196:embryology / Q000201:enzymology*; D029742:Caenorhabditis elegans Proteins / Q000235:genetics / Q000502:physiology*; D002843:Chromatin / Q000648:ultrastructure; D003198:Computer Simulation; D004625:Embryo, Nonmammalian / Q000166:cytology / Q000201:enzymology; D000074201:Katanin; D008540:Meiosis / Q000502:physiology*; D008868:Microtubule Proteins / Q000235:genetics / Q000502:physiology*; D008870:Microtubules / Q000378:metabolism* / Q000648:ultrastructure*; D008954:Models, Biological; D008958:Models, Molecular; D008941:Spindle Apparatus / Q000378:metabolism / Q000648:ultrastructure
D029742:Caenorhabditis elegans Proteins; D002843:Chromatin; D008868:Microtubule Proteins; D000251:Adenosine Triphosphatases; D000074201:Katanin