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Vol. 20, Issue 11, 2709-2721, June 1, 2009

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asunder Is a Critical Regulator of Dynein–Dynactin Localization during Drosophila Spermatogenesis

Michael A. Anderson^*, Jeanne N. Jodoin^*, Ethan Lee^*, Karen G. Hales, Thomas S. Hays, and Laura A. Lee^*

*Department of Cell and Developmental Biology, Vanderbilt University Medical Center, Nashville, TN 37232-8240; Department of Genetics, Cell Biology, and Development, University of Minnesota, Minneapolis, MN 55455; and Department of Biology, Davidson College, Davidson, NC 28035-7118

Submitted December 3, 2008; Revised March 26, 2009; Accepted March 27, 2009
Monitoring Editor: Erika Holzbaur

Spermatogenesis uses mitotic and meiotic cell cycles coordinated with growth and differentiation programs to generate functional sperm. Our analysis of a Drosophila mutant has revealed that asunder (asun), which encodes a conserved protein, is an essential regulator of spermatogenesis. asun spermatocytes arrest during prophase of meiosis I. Strikingly, arrested spermatocytes contain free centrosomes that fail to stably associate with the nucleus. Spermatocytes that overcome arrest exhibit severe defects in meiotic spindle assembly, chromosome segregation, and cytokinesis. Furthermore, the centriole-derived basal body is detached from the nucleus in asun postmeiotic spermatids, resulting in abnormalities later in spermatogenesis. We find that asun spermatocytes and spermatids exhibit drastic reduction of perinuclear dynein–dynactin, a microtubule motor complex. We propose a model in which asun coordinates spermatogenesis by promoting dynein–dynactin recruitment to the nuclear surface, a poorly understood process required for nucleus–centrosome coupling at M phase entry and fidelity of meiotic divisions.

Address correspondence to: Laura A. Lee (laura.a.lee{at}vanderbilt.edu)