Growing Microtubules Push the Oocyte Nucleus to Polarize the Drosophila Dorsal-Ventral Axis

Abstract

The Drosophila dorsal-ventral (DV) axis is polarized when the oocyte nucleus migrates from the posterior to the anterior margin of the oocyte. Prior work suggested that dynein pulls the nucleus to the anterior side along a polarized microtubule cytoskeleton, but this mechanism has not been tested. By imaging live oocytes, we find that the nucleus migrates with a posterior indentation that correlates with its direction of movement. Furthermore, both nuclear movement and the indentation depend on microtubule polymerization from centrosomes behind the nucleus. Thus, the nucleus is not pulled to the anterior but is pushed by the force exerted by growing microtubules. Nuclear migration and DV axis formation therefore depend on centrosome positioning early in oogenesis and are independent of anterior-posterior axis formation.

Ovarian Development of House Fly (Musca domestica L.) (Diptera: Muscidae)

“…The epithelial cell becomes columnar, resulting in intra cellular separate from the ooplasm forming spaces at the time of vitellogenesis. This finding corroborates with [41]. The presence of yolk granules at the apex of follicular cells in present evidence for the intracellular pathway for protein accumulation inside the oocyte.…”

‘Poking’ microtubules bring about nuclear wriggling to position nuclei

“…Considering that the size of the MTs that poke the nuclei in the follicle cells varies between 2.5 and 6.5 µm and taking flexural rigidity 25x10 -24 Nm 2 , the buckling force appears to vary between 40 and 5 piconewtons, respectively. Similar values were reported, e.g., for the MTs that push the oocyte nucleus during its positioning in the developing Drosophila egg primordia (Inoue and Salmon, 1995;Dogterom and Yurke, 1997;Janson et al, 2003;Zhao et al 2012). Although the MTs keep on poking and make the follicle cell nuclei wriggle already in the very young egg primordia, the nuclei do not drift in the yet dividing, cuboidal cells.…”

“…and 10). MTs poking the nuclei may well exert forces as described earlier for growing MTs that contact cellular structures (Inoue and Salmon, 1995;Li, 2008;Laan and Dogterom 2010;Zhao et al 2012). Thus, it appears that nuclear wriggling is the result of the activity of dynamic MTs that keep on poking the nuclei and make them wriggle.…”

“…(1) The MTOC, tightly associated with the nucleus through dyneins, nucleates the astral MTs which, while growing and pushing against the cell membrane, generate the force required to position the nucleus (reviewed in Reinsch and Gönczy, 1998;Gönczy et al, 1999;Morris, 2003;Tolić-Nørrelykke, 2008 and2010;Zhao et al 2012). The process is reminiscent of the growing interpolar MTs that push apart the daughter centrosomes (Venkei et al, 2006).…”

A stem–loop structure directsoskarmRNA to microtubule minus ends

“…During early oogenesis, the microtubule organizing center (MTOC) of the germline syncytium is restricted to the oocyte, and the microtubules that nucleate within this cell extend through the ring-canals into the neighboring nurse cells (Theurkauf et al 1993); at mid-oogenesis, the microtubule network is reorganized such that the bulk of the microtubules nucleate at the anterior cortex and extend toward the posterior pole of the oocyte (Theurkauf et al 1992;Parton et al 2011); a distinct array of microtubules that emanates from a nuclear membrane-localized MTOC positions the oocyte nucleus at an antero-lateral position in the oocyte (Januschke et al 2006;Zhao et al 2012). Consistent with these observations, Nod-βgal, a reporter of microtubule minus ends also enriches in the oocyte in young egg-chambers, whereas during mid-oogenesis, it is detected at the oocyte anterior, while Kinesin-βgal, a reporter of microtubule plus ends, is enriched at the posterior pole (Clark et al 1994(Clark et al , 1997.…”