Klp10A, a stem cell centrosome-enriched kinesin, balances asymmetries in Drosophila male germline stem cell division.

Cuie Chen,Zsolt G Venkei,Mayu Inaba,Yukiko M Yamashita

doi:10.7554/elife.20977

Abstract

Asymmetric stem cell division is often accompanied by stereotypical inheritance of the mother and daughter centrosomes. However, it remains unknown whether and how stem cell centrosomes are uniquely regulated and how this regulation may contribute to stem cell fate. Here we identify Klp10A, a microtubule-depolymerizing kinesin of the kinesin-13 family, as the first protein enriched in the stem cell centrosome in Drosophila male germline stem cells (GSCs). Depletion of klp10A results in abnormal elongation of the mother centrosomes in GSCs, suggesting the existence of a stem cell-specific centrosome regulation program. Concomitant with mother centrosome elongation, GSCs form asymmetric spindle, wherein the elongated mother centrosome organizes considerably larger half spindle than the other. This leads to asymmetric cell size, yielding a smaller differentiating daughter cell. We propose that klp10A functions to counteract undesirable asymmetries that may result as a by-product of achieving asymmetries essential for successful stem cell divisions.

Highlights

Asymmetric cell division (ACD) is a key process that balances stem cell self-renewal and differentiation by producing one stem cell and one differentiating cell (Inaba and Yamashita, 2012; Morrison and Kimble, 2006)
We have shown that biased segregation of sister chromatids (Yadlapalli and Yamashita, 2013) and asymmetric inheritance of the midbody ring (Salzmann et al, 2014) depend on the centrosomes in Drosophila male germline stem cells (GSCs)
It remained unknown whether stem cell centrosomes are unique, and whether the stem cell mother centrosome is distinct from the daughter centrosome

Summary

Introduction

Asymmetric cell division (ACD) is a key process that balances stem cell self-renewal and differentiation by producing one stem cell and one differentiating cell (Inaba and Yamashita, 2012; Morrison and Kimble, 2006). During ACD, many cellular components have been reported to segregate asymmetrically, including fate determinants, certain organelles, sister chromatids/histones and damaged proteins (Chen et al, 2016; Tajbakhsh and Gonzalez, 2009). Cellular asymmetries are critical aspects of ACD, the essence of successful cell division is the precise replication and segregation of cellular contents, such as chromosomes and essential organelles. It has been underexplored how cells may achieve productive ACD without interfering with the basic requirement of cell divisions. It is reported that aggresomes (damaged protein aggregates) are segregated asymmetrically to only one cells during cell division, by being associated with a centrosome (Rujano et al, 2006). It is reported that proteins destined for degradation are targeted to the centrosomes and segregated asymmetrically during human

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