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Redundant mechanisms for anaphase chromosome movements: crane-fly spermatocyte spindles normally use actin filaments but also can function without them

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Summary.

Actin inhibitors block or slow anaphase chromosome movements in crane-fly spermatocytes, but stopping of movement is only temporary; we assumed that cells adapt to loss of actin by switching to mechanism(s) involving only microtubules. To test this, we produced actin-filament-free spindles: we added latrunculin B during prometaphase, 9–80 min before anaphase, after which chromosomes generally moved normally during anaphase. We confirmed the absence of actin filaments by staining with fluorescent phalloidin and by showing that cytochalasin D had no effect on chromosome movement. Thus, actin filaments are involved in normal anaphase movements, but in vivo, spindles nonetheless can function normally without them. We tested whether chromosome movements in actin-filament-free spindles arise via microtubules by challenging such spindles with anti-myosin drugs. Y-27632 and BDM (2,3-butanedione monoxime), inhibitors that affect myosin at different regulatory levels, blocked chromosome movement in normal spindles and in actin-filament-free spindles. We tested whether BDM has side effects on microtubule motors. BDM had no effect on ciliary and sperm motility or on ATPase activity of isolated ciliary axonemes, and thus it does not directly block dynein. Nor does it block kinesin, assayed by a microtubule sliding assay. BDM could conceivably indirectly affect these microtubule motors, though it is unlikely that it would have the same side effect on the motors as Y-27632. Since BDM and Y-27632 both affect chromosome movement in the same way, it would seem that both affect spindle myosin; this suggests that spindle myosin interacts with kinetochore microtubules, either directly or via an intermediate component.

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Correspondence to Arthur Forer.

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Correspondence and reprints: Biology Department, York University, 4700 Keele Street, Toronto, ON M3J 1P3, Canada.

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Movie 1. Control crane-fly spermatocyte undergoing meiosis I and starting cleavage. Three pairs of bivalents are visible (two pairs in one focal plane and one pair in another focal plane). The smaller sex chromosomes remain at the equator until the half-bivalents reach the poles. Time is in hours, minutes, seconds

Movie 2. A double-treated crane-fly spermatocyte. The spermatocyte was treated with Latrunculin B during prometaphase (at 16:59:00). The cell entered anaphase at about 17:38:00 and it was treated with Cytochalasin D and Latrunculin B at 17:38:50. Chromosome movements were not affected by the Cytochalasin D. Note that only two bivalents aligned at the equator in metaphase, which is not uncommon in cells treated with Latrunculin B during prometaphase. Time is in hours, minutes, seconds

Movie 3. Rhodamine-labelled microtubules sliding along kinesin-coated coverslips. The first sequence is from a control preparation. The second sequence is from a different preparation to which 5 mM BDM was added. The third sequence is from the same preparation as the control experiment but was recorded after 20 mM BDM was added. The speed of microtubule sliding is similar in all three experiments

Movie 3. Rhodamine-labelled microtubules sliding along kinesin-coated coverslips. The first sequence is from a control preparation. The second sequence is from a different preparation to which 5 mM BDM was added. The third sequence is from the same preparation as the control experiment but was recorded after 20 mM BDM was added. The speed of microtubule sliding is similar in all three experiments

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Fabian, L., Forer, A. Redundant mechanisms for anaphase chromosome movements: crane-fly spermatocyte spindles normally use actin filaments but also can function without them. Protoplasma 225, 169–184 (2005). https://doi.org/10.1007/s00709-005-0094-6

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  • Key words: Chromosome movement; Myosin; Microtubule; 2,3-Butanedione monoxime; Latrunculin B; Crane-fly spermatocyte; Rho-kinase inhibitor Y-27632.