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© The Rockefeller University Press, 0021-9525/1997//1169 $5.00
The Journal of Cell Biology, Volume 136, Number 6, , 1997 1169-1183

Article

Chromosomal Proteins and Cytokinesis: Patterns of Cleavage Furrow Formation and Inner Centromere Protein Positioning in Mitotic Heterokaryons and Mid-anaphase Cells



D. Mark Eckley*,{ddagger}, Alexandra M. Ainsztein*,{ddagger}, Alastair M. Mackay*, Ilya G. Goldberg*,{ddagger}, and William C. Earnshaw*,{ddagger}

* Department of Cell Biology and Anatomy, Johns Hopkins University School of Medicine, Baltimore, Maryland 21205; and {ddagger} The Institute of Cell and Molecular Biology, University of Edinburgh, Edinburgh EH9 3JR, Scotland, United Kingdom

After the separation of sister chromatids in anaphase, it is essential that the cell position a cleavage furrow so that it partitions the chromatids into two daughter cells of roughly equal size. The mechanism by which cells position this cleavage furrow remains unknown, although the best current model is that furrows always assemble midway between asters. We used micromanipulation of human cultured cells to produce mitotic heterokaryons with two spindles fused in a V conformation. The majority (15/19) of these cells cleaved along a single plane that transected the two arms of the V at the position where the metaphase plate had been, a result at odds with current views of furrow positioning. However, four cells did form an additional ectopic furrow between the spindle poles at the open end of the V, consistent with the established view. To begin to address the mechanism of furrow assembly, we have begun a detailed study of the properties of the chromosome passenger inner centromere protein (INCENP) in anaphase and telophase cells. We found that INCENP is a very early component of the cleavage furrow, accumulating at the equatorial cortex before any noticeable cortical shape change and before any local accumulation of myosin heavy chain. In mitotic heterokaryons, INCENP was detected in association with spindle midzone microtubules beneath sites of furrowing and was not detected when furrows were absent. A functional role for INCENP in cytokinesis was suggested in experiments where a nearly full-length INCENP was tethered to the centromere. Many cells expressing the chimeric INCENP failed to complete cytokinesis and entered the next cell cycle with daughter cells connected by a large intercellular bridge with a prominent midbody. Together, these results suggest that INCENP has a role in either the assembly or function of the cleavage furrow.

Abbreviations used in this paper: INCENP, inner centromere protein; Sf9, Spodoptera frugiperda; TD-60, telophase disc protein of 60 kD.

Address all correspondence to William C. Earnshaw, Institute of Cell and Molecular Biology, University of Edinburgh, Swann Building, The King's Buildings, Mayfield Road, Edinburgh EH9 3JR, Scotland, UK. Tel.: 44131-650-7101. Fax: 44-131-650-7100. E-mail: bill.earnshaw{at}ed.ac.uk

D. Mark Eckley, Alexandria M. Ainsztein, and Ilya G. Goldberg's current address is also Institute of Cell and Molecular Biology, University of Edinburgh.

Alastair M. McKay's current address is Osiris Therapeutics, Inc., 2001 Aliceanna St., Baltimore, MD 21231-2001.


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