Cortical actin dynamics

The actin cytoskeleton plays essential roles in cell polarization and cell morphogenesis of the budding yeast Saccharomyces cerevisiae. Yeast cells utilize formin-generated actin cables as tracks for polarized transport, which forms the basis for a positive feedback loop driving Cdc42 dependent cell polarization. Previous studies on cable organization mostly focused on polarized actin cables in budded cells and their role as relatively static tracks for myosin-dependent organelle transport. Using quantitative live cell imaging, we have recently characterized the dynamics of cortical actin cables throughout the yeast cell cycle. Surprisingly, randomly oriented actin cables in G1 cells exhibited the highest level of dynamics, while cable dynamics was markedly slowed down upon cell polarization. We further demonstrated that the rapid dynamics of randomly oriented cables were driven by the formin Bni1 and Myosin V. Our data suggested a precise spatio-temporal regulation of the two yeast formins, as well as an unexpected mechanism of actin cable rearrangement through myosins. Here we discuss the immediate significance of these findings, which illustrates the importance of generating randomness for cellular organization.

[1]  A. Bretscher,et al.  Tropomyosin-containing actin cables direct the Myo2p-dependent polarized delivery of secretory vesicles in budding yeast. , 1998, The Journal of cell biology.

[2]  B. Goode,et al.  Actin nucleation and elongation factors: mechanisms and interplay. , 2009, Current opinion in cell biology.

[3]  L. Pon,et al.  Actin cable dynamics in budding yeast , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[4]  Lani Wu,et al.  Spontaneous Cell Polarization Through Actomyosin-Based Delivery of the Cdc42 GTPase , 2003, Science.

[5]  Julie Grantham,et al.  The Polarisome Is Required for Segregation and Retrograde Transport of Protein Aggregates , 2010, Cell.

[6]  Roland Wedlich-Söldner,et al.  Cortical actin dynamics driven by formins and myosin V , 2011, Journal of Cell Science.

[7]  Navin Pokala,et al.  High Rates of Actin Filament Turnover in Budding Yeast and Roles for Actin in Establishment and Maintenance of Cell Polarity Revealed Using the Actin Inhibitor Latrunculin-A , 1997, The Journal of cell biology.

[8]  J. Moseley,et al.  Differential Activities and Regulation of Saccharomyces cerevisiae Formin Proteins Bni1 and Bnr1 by Bud6* , 2005, Journal of Biological Chemistry.

[9]  D. Kovar.  Molecular details of formin-mediated actin assembly. , 2006, Current opinion in cell biology.

[10]  A. Bretscher,et al.  Mechanisms of polarized growth and organelle segregation in yeast. , 2004, Annual review of cell and developmental biology.

[11]  D. Pellman,et al.  Yeast formins Bni1 and Bnr1 utilize different modes of cortical interaction during the assembly of actin cables. , 2007, Molecular biology of the cell.

[12]  Alex R. Hodges,et al.  Differential Regulation of Unconventional Fission Yeast Myosins via the Actin Track , 2010, Current Biology.

[13]  Daniel P. Mulvihill,et al.  The recruitment of acetylated and unacetylated tropomyosin to distinct actin polymers permits the discrete regulation of specific myosins in fission yeast , 2010, Journal of Cell Science.

[14]  Anthony Bretscher,et al.  Stable and dynamic axes of polarity use distinct formin isoforms in budding yeast. , 2004, Molecular biology of the cell.

[15]  Thomas Schmidt,et al.  Robust cell polarity is a dynamic state established by coupling transport and GTPase signaling , 2004, The Journal of cell biology.

[16]  Bruce L. Goode,et al.  The Yeast Actin Cytoskeleton: from Cellular Function to Biochemical Mechanism , 2006, Microbiology and Molecular Biology Reviews.

[17]  James Moseley,et al.  An actin nucleation mechanism mediated by Bni1 and Profilin , 2002, Nature Cell Biology.

[18]  A. Bretscher,et al.  The Cooh-Terminal Domain of Myo2p, a Yeast Myosin V, Has a Direct Role in Secretory Vesicle Targeting , 1999, The Journal of cell biology.

[19]  James G. McNally,et al.  Assembly and Function of the Actin Cytoskeleton of Yeast: Relationships between Cables and Patches , 1998, The Journal of cell biology.

[20]  Samara L. Reck-Peterson,et al.  Role of actin and Myo2p in polarized secretion and growth of Saccharomyces cerevisiae. , 2000, Molecular biology of the cell.

[21]  Anthony Bretscher,et al.  Formin-dependent actin assembly is regulated by distinct modes of Rho signaling in yeast , 2003, The Journal of cell biology.

[22]  L. Pon,et al.  Roles of type II myosin and a tropomyosin isoform in retrograde actin flow in budding yeast , 2006, The Journal of cell biology.

[23]  D. Kovar,et al.  Fimbrin and Tropomyosin Competition Regulates Endocytosis and Cytokinesis Kinetics in Fission Yeast , 2010, Current Biology.

[24]  A. Bretscher,et al.  Ras regulates the polarity of the yeast actin cytoskeleton through the stress response pathway. , 2001, Molecular biology of the cell.

[25]  Eugenio Marco,et al.  Endocytosis Optimizes the Dynamic Localization of Membrane Proteins that Regulate Cortical Polarity , 2007, Cell.

[26]  Haochen Yu.  Dynamics of cortical actin in budding yeast Saccharomyces cerevisiae , 2010 .

[27]  M. Lord,et al.  Tropomyosin and Myosin-II Cellular Levels Promote Actomyosin Ring Assembly in Fission Yeast , 2010, Molecular biology of the cell.

[28]  Charles Boone,et al.  Formins direct Arp2/3-independent actin filament assembly to polarize cell growth in yeast , 2002, Nature Cell Biology.