Elements of error correction in mitosis: microtubule capture, release, and tension.

The correction of certain errors in mitosis requires capture and release: new kinetochore microtubules must be captured and old, misdirected ones must be released. We studied capture and release in living grasshopper spermatocytes. Capture is remarkably efficient over a broad range in the angle at which a microtubule encounters a kinetochore. However, capture is inefficient when kinetochores point directly away from the source of properly directed microtubules. Capture in that situation is required for correction of the most common error; microtubule-kinetochore encounters are improbable and capture occurs only once every 8 min, on average. Release from the improper attachment caused by misdirected microtubules allows kinetochore movement and the completion of error correction. We tugged on kinetochores with a micromanipulation needle and found they are free to move less than one time in two. Thus error correction depends on two improbable events, capture and release, and they must happen by chance to coincide. In spermatocytes this will occur only once every 18 min, on average, but a leisurely cell cycle provides ample time. Capture and release generate only change, not perfection. Tension from mitotic forces brings change to a halt by stabilizing the one correct attachment of chromosomes to the spindle. We show that tension directly affects stability, rather than merely constraining kinetochore position. This implies that chromosomes are attached to the spindle by tension-sensitive linkers whose stability is necessary for proper chromosome distribution but whose loss is necessary for the correction of errors.