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Anillin Regulates Cell-Cell Junction Integrity by Organizing Junctional Accumulation of Rho-GTP and Actomyosin

C.C. Reyes, M. Jin, E.B. Breznau, R. Espino, R. Delgado-Gonzalo, A.B. Goryachev, A.L. Miller

Current Biology, vol. 24, no. 11, pp. 1263-1270, June 2, 2014.



Anillin is a scaffolding protein that organizes and stabilizes actomyosin contractile rings and was previously thought to function primarily in cytokinesis [1, 2, 3, 4, 5, 6, 7, 8, 9, 10]. Using Xenopus laevis embryos as a model system to examine Anillin's role in the intact vertebrate epithelium, we find that a population of Anillin surprisingly localizes to epithelial cell-cell junctions throughout the cell cycle, whereas it was previously thought to be nuclear during interphase [5, 11]. Furthermore, we show that Anillin plays a critical role in regulating cell-cell junction integrity. Both tight junctions and adherens junctions are disrupted when Anillin is knocked down, leading to altered cell shape and increased intercellular spaces. Anillin interacts with Rho, F-actin, and myosin II [3, 8, 9], all of which regulate cell-cell junction structure and function. When Anillin is knocked down, active Rho (Rho-guanosine triphosphate [GTP]), F-actin, and myosin II are misregulated at junctions. Indeed, increased dynamic "flares" of Rho-GTP are observed at cell-cell junctions, whereas overall junctional F-actin and myosin II accumulation is reduced when Anillin is depleted. We propose that Anillin is required for proper Rho-GTP distribution at cell-cell junctions and for maintenance of a robust apical actomyosin belt, which is required for cell-cell junction integrity. These results reveal a novel role for Anillin in regulating epithelial cell-cell junctions.

References

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  2. C.M. Field, B.M. Alberts, "Anillin, A Contractile Ring Protein that Cycles from the Nucleus to the Cell Cortex," Journal of Cell Biology, vol. 131, no. 1, pp. 165-178, October 1995.

  3. A.F. Straight, C.M. Field, T.J. Mitchison, "Anillin Binds Nonmuscle Myosin II and Regulates the Contractile Ring," Molecular Biology of the Cell, vol. 16, no. 1, pp. 193-201, January 2005.

  4. C.M. Field, M. Coughlin, S. Doberstein, T. Marty, W. Sullivan, "Characterization of Anillin Mutants Reveals Essential Roles in Septin Localization and Plasma Membrane Integrity," Development, vol. 132, no. 12, pp. 2849-2860, June 2005.

  5. K. Oegema, M.S. Savoian, T.J. Mitchison, C.M. Field, "Functional Analysis of a Human Homologue of the Drosophila Actin Binding Protein Anillin Suggests a Role in Cytokinesis," The Journal of Cell Biology, vol. 150, no. 3, pp. 539-552, August 7, 2000.

  6. P.P. D'Avino, T. Takeda, L. Capalbo, W. Zhang, K.S. Lilley, E.D. Laue, D.M. Glover, "Interaction Between Anillin and RacGAP50C Connects the Actomyosin Contractile Ring with Spindle Microtubules at the Cell Division Site," Journal of Cell Science, vol. 121, no. 8, pp. 1151-1158, April 15, 2008.

  7. S.L. Gregory, S. Ebrahimi, J. Milverton, W.M. Jones, A. Bejsovec, R. Saint, "Cell Division Requires a Direct Link Between Microtubule-Bound RacGAP and Anillin in the Contractile Ring," Current Biology, vol. 18, no. 1, pp. 25-29, January 8, 2008.

  8. A.J. Piekny, M. Glotzer, "Anillin Is a Scaffold Protein that Links RhoA, Actin, And Myosin During Cytokinesis," Current Biology, vol. 18, no. 1, pp. 30-36, January 8, 2008.

  9. K.G. Miller, B.M. Alberts, "F-Actin Affinity Chromatography: Technique for Isolating Previously Unidentified Actin-Binding Proteins," Proceedings of the National Academy of Sciences of the United States of America, vol. 86, no. 13, pp. 4808-4812, July 1989.

  10. P. Frenette, E. Haines, M. Loloyan, M. Kinal, P. Pakarian, A. Piekny, "An Anillin-Ect2 Complex Stabilizes Central Spindle Microtubules at the Cortex During Cytokinesis," PLoS ONE, vol. 7, no. 4, pp. e34888, April 13, 2012.

  11. P.P. D'Avino, "How to Scaffold the Contractile Ring for a Safe Cytokinesis—Lessons from Anillin-Related Proteins," Journal of Cell Science, vol. 122, no. 8, pp. 1071-1079, April 15, 2009.


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