An essential role for Katanin p80 and microtubule severing in male gamete production

Liza O'Donnell, Danielle Rhodes, Stephanie J. Smith, D. Jo Merriner, Brett J. Clark, Claire Borg, Belinda Whittle, Anne E. O'Connor, Lee B. Smith, Francis J. McNally, David M. de Kretser, Chris C. Goodnow, Chris J. Ormandy, Duangporn Jamsai, Moira K. O'Bryan

Research output: Contribution to journalArticle

47 Citations (Scopus)

Abstract

Katanin is an evolutionarily conserved microtubule-severing complex implicated in multiple aspects of microtubule dynamics. Katanin consists of a p60 severing enzyme and a p80 regulatory subunit. The p80 subunit is thought to regulate complex targeting and severing activity, but its precise role remains elusive. In lower-order species, the katanin complex has been shown to modulate mitotic and female meiotic spindle dynamics and flagella development. The in vivo function of katanin p80 in mammals is unknown. Here we show that katanin p80 is essential for male fertility. Specifically, through an analysis of a mouse loss-of-function allele (the Taily line), we demonstrate that katanin p80, most likely in association with p60, has an essential role in male meiotic spindle assembly and dissolution and the removal of midbody microtubules and, thus, cytokinesis. Katanin p80 also controls the formation, function, and dissolution of a microtubule structure intimately involved in defining sperm head shaping and sperm tail formation, the manchette, and plays a role in the formation of axoneme microtubules. Perturbed katanin p80 function, as evidenced in the Taily mouse, results in male sterility characterized by decreased sperm production, sperm with abnormal head shape, and a virtual absence of progressive motility. Collectively these data demonstrate that katanin p80 serves an essential and evolutionarily conserved role in several aspects of male germ cell development.

Original languageEnglish (US)
Article numbere1002698
JournalPLoS Genetics
Volume8
Issue number5
DOIs
StatePublished - May 2012

Fingerprint

gametogenesis
gamete
Germ Cells
Microtubules
sperm
microtubules
spermatozoa
male fertility
dissolution
germ cell
sterility
Spindle Apparatus
motility
targeting
mice
cytokinesis
fertility
allele
flagellum
mammal

ASJC Scopus subject areas

  • Genetics
  • Molecular Biology
  • Ecology, Evolution, Behavior and Systematics
  • Cancer Research
  • Genetics(clinical)

Cite this

O'Donnell, L., Rhodes, D., Smith, S. J., Merriner, D. J., Clark, B. J., Borg, C., ... O'Bryan, M. K. (2012). An essential role for Katanin p80 and microtubule severing in male gamete production. PLoS Genetics, 8(5), [e1002698]. https://doi.org/10.1371/journal.pgen.1002698

An essential role for Katanin p80 and microtubule severing in male gamete production. / O'Donnell, Liza; Rhodes, Danielle; Smith, Stephanie J.; Merriner, D. Jo; Clark, Brett J.; Borg, Claire; Whittle, Belinda; O'Connor, Anne E.; Smith, Lee B.; McNally, Francis J.; de Kretser, David M.; Goodnow, Chris C.; Ormandy, Chris J.; Jamsai, Duangporn; O'Bryan, Moira K.

In: PLoS Genetics, Vol. 8, No. 5, e1002698, 05.2012.

Research output: Contribution to journalArticle

O'Donnell, L, Rhodes, D, Smith, SJ, Merriner, DJ, Clark, BJ, Borg, C, Whittle, B, O'Connor, AE, Smith, LB, McNally, FJ, de Kretser, DM, Goodnow, CC, Ormandy, CJ, Jamsai, D & O'Bryan, MK 2012, 'An essential role for Katanin p80 and microtubule severing in male gamete production', PLoS Genetics, vol. 8, no. 5, e1002698. https://doi.org/10.1371/journal.pgen.1002698
O'Donnell L, Rhodes D, Smith SJ, Merriner DJ, Clark BJ, Borg C et al. An essential role for Katanin p80 and microtubule severing in male gamete production. PLoS Genetics. 2012 May;8(5). e1002698. https://doi.org/10.1371/journal.pgen.1002698
O'Donnell, Liza ; Rhodes, Danielle ; Smith, Stephanie J. ; Merriner, D. Jo ; Clark, Brett J. ; Borg, Claire ; Whittle, Belinda ; O'Connor, Anne E. ; Smith, Lee B. ; McNally, Francis J. ; de Kretser, David M. ; Goodnow, Chris C. ; Ormandy, Chris J. ; Jamsai, Duangporn ; O'Bryan, Moira K. / An essential role for Katanin p80 and microtubule severing in male gamete production. In: PLoS Genetics. 2012 ; Vol. 8, No. 5.
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