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Abstract
Cytokinesis is powered by the contraction of actomyosin filaments within the newly assembled contractile ring. Microtubules are a spindle component that is essential for the induction of cytokinesis. This induction could use central spindle and/or astral microtubules to stimulate cortical contraction around the spindle equator (equatorial stimulation). Alternatively, or in addition, induction could rely on astral microtubules to relax the polar cortex (polar relaxation). To investigate the relationship between microtubules, cortical stiffness, and contractile ring assembly, we used different configurations of microtubules to manipulate the distribution of actin in living silkworm spermatocytes. Mechanically repositioned, noninterdigitating microtubules can induce redistribution of actin at any region of the cortex by locally excluding cortical actin filaments. This cortical flow of actin promotes regional relaxation while increasing tension elsewhere (normally at the equatorial cortex). In contrast, repositioned interdigitating microtubule bundles use a novel mechanism to induce local stimulation of contractility anywhere within the cortex; at the antiparallel plus ends of central spindle microtubules, actin aggregates are rapidly assembled de novo and transported laterally to the equatorial cortex. Relaxation depends on microtubule dynamics but not on RhoA activity, whereas stimulation depends on RhoA activity but is largely independent of microtubule dynamics. We conclude that polar relaxation and equatorial stimulation mechanisms redundantly supply actin for contractile ring assembly, thus increasing the fidelity of cleavage.
Highlights
The contractile ring is a dynamic, actomyosin-based structure whose constriction generates a cleavage furrow, producing two daughter cells
The site of cleavage must occur between the segregating chromosomes—at the spindle equator—to ensure that each cell receives the proper number of chromosomes
The ‘‘polar relaxation’’ hypothesis proposes that the astral microtubules, which radiate outward, cause contractile elements to flow from the polar cortex toward the equator, resulting in furrowing
Summary
The contractile ring is a dynamic, actomyosin-based structure whose constriction generates a cleavage furrow, producing two daughter cells. To ensure accurate distribution of chromosomes to each cell, the location of the division plane and the timing of cleavage must be tightly regulated to coordinate with chromosomal segregation. In animal cells, this coordination is mediated by the spindle apparatus, which both segregates the chromosomes during anaphase and signals the cortex as to where and when the contractile ring should be assembled (reviewed in, e.g., [1,2,3,4]). Some proteins are localized both to the central spindle and the equatorial cortex in a temporally dynamic manner. It is not known whether these proteins represent independent pools or whether the proteins diffuse or are somehow transported between locations
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