TY - JOUR
T1 - Transport of germ plasm on astral microtubules directs germ cell development in Drosophila
AU - Lerit, Dorothy A.
AU - Gavis, Elizabeth R.
N1 - Funding Information:
We are grateful to T. Weil, whose observation of nos ∗ GFP particle motility during embryogenesis initiated this project; J. Brechbiel for characterizing nos-(ms2) 18 expression levels; and J. Goodhouse and S. Thiberge, respectively, for assistance with confocal and two-photon microscopy. We thank D. Glover, P. Lasko, T. Megraw, T. Orr-Weaver, J. Raff, W. Saxton, R. Warrior, M. Welte, and the Bloomington Drosophila Stock Center for fly stocks; T. Hays, T. Kaufman, P. Lasko, R. Lehmann, P. Schedl, E. Wieschaus, and the Drosophila Studies Hybridoma Bank for antibodies; and P. Lasko for the GFP-Vas plasmid. We are also grateful to G. Deshpande, J. Lee, H. Lipshitz, N. Siddiqui, and T. Schüpbach for comments on the manuscript and to T. Weil, G. Deshpande, and members of the Gavis laboratory for discussions and advice. This work was supported by National Institutes of Health (NIH) Center Grant P50GM071508 to the Lewis-Sigler Institute and by a Johnson & Johnson Imaging Center Award and NIH grant GM067758 to E.R.G.
PY - 2011/3/22
Y1 - 2011/3/22
N2 - Background: In many organisms, germ cells are segregated from the soma through the inheritance of the specialized germ plasm, which contains mRNAs and proteins that specify germ cell fate and promote germline development. Whereas germ plasm assembly has been well characterized, mechanisms mediating germ plasm inheritance are poorly understood. In the Drosophila embryo, germ plasm is anchored to the posterior cortex, and nuclei that migrate into this region give rise to the germ cell progenitors, or pole cells. How the germ plasm interacts with these nuclei for pole cell induction and is selectively incorporated into the forming pole cells is not known. Results: Live imaging of two conserved germ plasm components, nanos mRNA and Vasa protein, revealed that germ plasm segregation is a dynamic process involving active transport of germ plasm RNA-protein complexes coordinated with nuclear migration. We show that centrosomes accompanying posterior nuclei induce release of germ plasm from the cortex and recruit these components by dynein-dependent transport on centrosome-nucleated microtubules. As nuclei divide, continued transport on astral microtubules partitions germ plasm to daughter nuclei, leading to its segregation into pole cells. Disruption of these transport events prevents incorporation of germ plasm into pole cells and impairs germ cell development. Conclusions: Our results indicate that active transport of germ plasm is essential for its inheritance and ensures the production of a discrete population of germ cell progenitors endowed with requisite factors for germline development. Transport on astral microtubules may provide a general mechanism for the segregation of cell fate determinants.
AB - Background: In many organisms, germ cells are segregated from the soma through the inheritance of the specialized germ plasm, which contains mRNAs and proteins that specify germ cell fate and promote germline development. Whereas germ plasm assembly has been well characterized, mechanisms mediating germ plasm inheritance are poorly understood. In the Drosophila embryo, germ plasm is anchored to the posterior cortex, and nuclei that migrate into this region give rise to the germ cell progenitors, or pole cells. How the germ plasm interacts with these nuclei for pole cell induction and is selectively incorporated into the forming pole cells is not known. Results: Live imaging of two conserved germ plasm components, nanos mRNA and Vasa protein, revealed that germ plasm segregation is a dynamic process involving active transport of germ plasm RNA-protein complexes coordinated with nuclear migration. We show that centrosomes accompanying posterior nuclei induce release of germ plasm from the cortex and recruit these components by dynein-dependent transport on centrosome-nucleated microtubules. As nuclei divide, continued transport on astral microtubules partitions germ plasm to daughter nuclei, leading to its segregation into pole cells. Disruption of these transport events prevents incorporation of germ plasm into pole cells and impairs germ cell development. Conclusions: Our results indicate that active transport of germ plasm is essential for its inheritance and ensures the production of a discrete population of germ cell progenitors endowed with requisite factors for germline development. Transport on astral microtubules may provide a general mechanism for the segregation of cell fate determinants.
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U2 - 10.1016/j.cub.2011.01.073
DO - 10.1016/j.cub.2011.01.073
M3 - Article
C2 - 21376599
AN - SCOPUS:79952815118
SN - 0960-9822
VL - 21
SP - 439
EP - 448
JO - Current Biology
JF - Current Biology
IS - 6
ER -