Meaders JL and Burgess DR (2020), Microtubule-Based Mechanisms of Pronuclear Posi...

ECB-ART-49878

Cells 2020 Feb 23;92:. doi: 10.3390/cells9020505.

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Microtubule-Based Mechanisms of Pronuclear Positioning.

Meaders JL , Burgess DR .

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The zygote is defined as a diploid cell resulting from the fusion of two haploid gametes. Union of haploid male and female pronuclei in many animals occurs through rearrangements of the microtubule cytoskeleton into a radial array of microtubules known as the sperm aster. The sperm aster nucleates from paternally-derived centrioles attached to the male pronucleus after fertilization. Nematode, echinoderm, and amphibian eggs have proven as invaluable models to investigate the biophysical principles for how the sperm aster unites male and female pronuclei with precise spatial and temporal regulation. In this review, we compare these model organisms, discussing the dynamics of sperm aster formation and the different force generating mechanism for sperm aster and pronuclear migration. Finally, we provide new mechanistic insights for how sperm aster growth may influence sperm aster positioning.

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	Figure 1. Fertilization and pronuclear migration in C. elegans. (A) The C. elegans oocyte is arrested in metaphase of meiosis I just prior to fertilization. The meiotic spindle is located on the future anterior end of the oocyte, while the sperm/male pronucleus enters on the future posterior end. (B) Early centration phase. Fertilization prompts the completion of meiosis and formation of the female pronucleus (red circle). After sperm entry and maturation of the paternally derived centrioles, two sperm asters form oriented on opposite sides of the male pronucleus (purple circle), perpendicular to the anterior-posterior axis. These asters help define the posterior half (bright blue plasma membrane). The asters migrate toward the egg center due to cytoplasmic dynein-dependent pulling forces that scale with MT length (inset). Force (black arrows) is generated in the opposite direction of movement (orange arrows). Therefore, more force is generated on the longer front MTs relative to the short rear/cortical facing MTs. (C) Late centration phase. The aster pairs expand during the centration phase, enlarging the posterior half relative to the anterior half of the egg (blue and orange membrane, respectively). The female pronucleus is captured by long front astral MTs and is transported to the male pronucleus by dynein. (D) Maintenance phase. The combined male and female pronucleus (pronuclear complex or PNC) finish migrating to the egg center and rotate. This rotation orients centrosomes parallel to the anterior-posterior axis. (E) Posteriorization phase. Nuclear envelope breakdown occurs, combining maternal and paternal chromosomes as the first mitotic apparatus forms in the zygote. The apparatus is pulled toward the posterior side by more dynein activity at the posterior half relative to the anterior (inset). MT catastrophe is also considered as a potential mechanism to generate forces (inset).
	Figure 2. Fertilization and pronuclear migration in the sea urchin (echinoderm). (A) The sea urchin oocyte has already completed meiosis resulting in formation of the female pronucleus (red circle), which is located randomly within the oocyte cytoplasm. Fertilization may also occur anywhere around the oocyte. (B) Almost immediately after fertilization, the paternally-derived centrosome is attached to the male pronucleus (purple circle) and begins forming the interphase sperm aster near the cortex. During this early time-point the sperm aster does not begin to migrate until astral MTs reach the rear cortex. (C and D) As the sperm aster grows, it enters the centration phase where it reaches a constant maximum speed. This velocity is either set by growth rates of rear cortical facing MTs pushing against the cortex as in (C), cytoplasmic dynein-dependent pulling forces that scale with MT lengths as in (D), or a combination of the two. The female pronucleus is captured by astral MTs and is presumably transported towards the aster center/male pronucleus by dynein. Transport causes the female pronucleus to form a âtear dropâ shape (E) The sperm aster slows down as it approaches the egg center, prophase centrosomes separation occurs, and pronuclei fuse forming the zygote nucleus (blue oval).
	Figure 3. Fertilization and pronuclear migration in Xenopus. (A) The frog oocyte is arrested in metaphase II of meiosis. The meiotic spindle is located at the pole of the animal half of the egg (top beige hemisphere). The sperm can fertilize the egg along the side of the animal half. The yolky vegetal half is illustrated as the lower dark yellow hemisphere. (B) Fertilization resumes the cell cycle, resulting in formation of the female pronucleus (red circle) near the animal pole after meiosis completes. The paternally derived centrosomes begin forming the interphase sperm aster attached to the male pronucleus (purple circle). (C) The sperm aster expands and migrates toward the center of the egg, just above the vegetal half. As the astral MTs contact the female pronucleus it is transported retrograde along astral MTs in a dynein dependent manner (inset). Furthermore, cytoplasmic dynein/cargo (inset) likely generates pulling forces through retrograde transport. (D) Simplification of sperm aster growth according the standard growth model (top) and the collective growth model (bottom). The standard growth model predicts that asters are formed solely from centrosome-nucleated MTs, while the collective growth model includes MT-dependent MT nucleation, or MT branching. When considering pushing forces due to MT polymerization against the cell cortex, long individual MTs (numbered 1â3) nucleate from the centrosome and bear a high compression load, which can lead to MT buckling and decentering (see text for details). However, this problem is solved by the collective growth model in which the compression load is redistributed to a greater number of short MTs (numbered 1â6) polymerizing against the cortex.

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Albertson, Formation of the first cleavage spindle in nematode embryos. 1984, Pubmed