The Journal of Cell Biology, Vol 126, 189-198, Copyright © 1994 by The Rockefeller University Press

ARTICLES

Feedback control of the metaphase-anaphase transition in sea urchin zygotes: role of maloriented chromosomes

G Sluder, FJ Miller, EA Thompson and DE Wolf
Worcester Foundation for Experimental Biology, Shrewsbury, Massachusetts 01545.

To help ensure the fidelity of chromosome transmission during mitosis, sea urchin zygotes have feedback control mechanisms for the metaphase- anaphase transition that monitor the assembly of spindle microtubules and the complete absence of proper chromosome attachment to the spindle. The way in which these feedback controls work has not been known. In this study we directly test the proposal that these controls operate by maloriented chromosomes producing a diffusible inhibitor of the metaphase-anaphase transition. We show that zygotes having 50% of their chromosomes (approximately 20) unattached or monoriented initiate anaphase at the same time as the controls, a time that is well within the maximum period these zygotes will spend in mitosis. In vivo observations of the unattached maternal chromosomes indicate that they are functionally within the sphere of influence of the molecular events that cause chromosome disjunction in the spindle. Although the unattached chromosomes disjoin (anaphase onset without chromosome movement) several minutes after spindle anaphase onset, their disjunction is correlated with the time of spindle anaphase onset, not the time their nucleus breaks down. This suggests that the molecular events that trigger chromosome disjunction originate in the central spindle and propagate outward. Our results show that the mechanisms for the feedback control of the metaphase-anaphase transition in sea urchin zygotes do not involve a diffusible inhibitor produced by maloriented chromosomes. Even though the feedback controls for the metaphase- anaphase transition may detect the complete absence of properly attached chromosomes, they are insensitive to unattached or mono- oriented chromosomes as long as some chromosomes are properly attached to the spindle.
CiteULike    Complore    Connotea    Del.icio.us    Digg    Facebook    Reddit    Technorati    Twitter    What's this?

This article has been cited by other articles:

• Corellou, F., Brownlee, C., Detivaud, L., Kloareg, B., Bouget, F.-Y. (2001). Cell Cycle in the Fucus Zygote Parallels a Somatic Cell Cycle but Displays a Unique Translational Regulation of Cyclin-Dependent Kinases. Plant Cell 13: 585-598 [Abstract] [Full Text]  
• Gonczy, P., Schnabel, H., Kaletta, T., Amores, A. D., Hyman, T., Schnabel, R. (1999). Dissection of Cell Division Processes in the One Cell Stage Caenorhabditis elegans Embryo by Mutational Analysis. JCB 144: 927-946 [Abstract] [Full Text]  
• Hinchcliffe, E., Thompson, E., Miller, F., Yang, J, Sluder, G (1999). Nucleo-cytoplasmic interactions that control nuclear envelope breakdown and entry into mitosis in the sea urchin zygote. J. Cell Sci. 112: 1139-1148 [Abstract]  
• Hinchcliffe, E. H., Cassels, G. O., Rieder, C. L., Sluder, G. (1998). The Coordination of Centrosome Reproduction with Nuclear Events of the Cell Cycle in the Sea Urchin Zygote. JCB 140: 1417-1426 [Abstract] [Full Text]  
• Mackay, A. M., Ainsztein, A. M., Eckley, D. M., Earnshaw, W. C. (1998). A Dominant Mutant of Inner Centromere Protein (INCENP), a Chromosomal Protein, Disrupts Prometaphase Congression and Cytokinesis. JCB 140: 991-1002 [Abstract] [Full Text]  
• LeMaire-Adkins, R., Radke, K., Hunt, P. A. (1997). Lack of Checkpoint Control at the Metaphase/Anaphase Transition: A Mechanism of Meiotic Nondisjunction in Mammalian Females. JCB 139: 1611-1619 [Abstract] [Full Text]  
• Rieder, C. L., Khodjakov, A., Paliulis, L. V., Fortier, T. M., Cole, R. W., Sluder, G. (1997). Mitosis in vertebrate somatic cells with two spindles: Implications for the metaphase/anaphase transition checkpoint and cleavage. Proc. Natl. Acad. Sci. USA 94: 5107-5112 [Abstract] [Full Text]  
• Eckley, D. M., Ainsztein, A. M., Mackay, A. M., Goldberg, I. G., Earnshaw, W. C. (1997). Chromosomal Proteins and Cytokinesis: Patterns of Cleavage Furrow Formation and Inner Centromere Protein Positioning in Mitotic Heterokaryons and Mid-anaphase Cells. JCB 136: 1169-1183 [Abstract] [Full Text]  
• Li, X, Nicklas, R. (1997). Tension-sensitive kinetochore phosphorylation and the chromosome distribution checkpoint in praying mantid spermatocytes. J. Cell Sci. 110: 537-545 [Abstract]  
• Sluder, G, Thompson, E., Miller, F., Hayes, J, Rieder, C. (1997). The checkpoint control for anaphase onset does not monitor excess numbers of spindle poles or bipolar spindle symmetry. J. Cell Sci. 110: 421-429 [Abstract]  
• Callaini, G, Dallai, R, Riparbelli, M. (1997). Wolbachia-induced delay of paternal chromatin condensation does not prevent maternal chromosomes from entering anaphase in incompatible crosses of Drosophila simulans. J. Cell Sci. 110: 271-280 [Abstract]  
• Pluta, A. F., Mackay, A. M., Ainsztein, A. M., Goldberg, I. G., Earnshaw, W. C. (1995). The Centromere: Hub of Chromosomal Activities. Science 270: 1591-1594 [Abstract]  
• McKim, K. S., Hawley, R. S. (1995). Chromosomal Control of Meiotic Cell Division. Science 270: 1595-1601 [Abstract]  

Home | Help | Feedback | Subscriptions | Archive | Search | Table of Contents