Spire and Formin 2 Synergize and Antagonize in Regulating Actin Assembly in Meiosis by a Ping-pong Mechanism

Overview

Journal PLoS Biol

Specialty Biology

Date 2014 Mar 4

PMID 24586110

Citations 45

Authors

Pierre Montaville

Antoine Jegou

Julien Pernier

Christel Compper

Berengere Guichard

Binyam Mogessie

Melina Schuh

Guillaume Romet-Lemonne

Marie-France Carlier

Affiliations

Soon will be listed here.

Abstract

In mammalian oocytes, three actin binding proteins, Formin 2 (Fmn2), Spire, and profilin, synergistically organize a dynamic cytoplasmic actin meshwork that mediates translocation of the spindle toward the cortex and is required for successful fertilization. Here we characterize Fmn2 and elucidate the molecular mechanism for this synergy, using bulk solution and individual filament kinetic measurements of actin assembly dynamics. We show that by capping filament barbed ends, Spire recruits Fmn2 and facilitates its association with barbed ends, followed by rapid processive assembly and release of Spire. In the presence of actin, profilin, Spire, and Fmn2, filaments display alternating phases of rapid processive assembly and arrested growth, driven by a "ping-pong" mechanism, in which Spire and Fmn2 alternately kick off each other from the barbed ends. The results are validated by the effects of injection of Spire, Fmn2, and their interacting moieties in mouse oocytes. This original mechanism of regulation of a Rho-GTPase-independent formin, recruited by Spire at Rab11a-positive vesicles, supports a model for modulation of a dynamic actin-vesicle meshwork in the oocyte at the origin of asymmetric positioning of the meiotic spindle.

Citing Articles

Coordination of actin plus-end dynamics by IQGAP1, formin, and capping protein.

Pimm M, Haarer B, Nobles A, Haney L, Marcin A, Alcaide Eligio M J Cell Biol. 2024; 223(9).

PMID: 38787349 PMC: 11117073. DOI: 10.1083/jcb.202305065.

The Axonal Actin Filament Cytoskeleton: Structure, Function, and Relevance to Injury and Degeneration.

Gallo G Mol Neurobiol. 2024; 61(8):5646-5664.

PMID: 38216856 DOI: 10.1007/s12035-023-03879-7.

Cyclase-associated protein interacts with actin filament barbed ends to promote depolymerization and formin displacement.

Alimov N, Hoeprich G, Padrick S, Goode B J Biol Chem. 2023; 299(12):105367.

PMID: 37863260 PMC: 10692737. DOI: 10.1016/j.jbc.2023.105367.

Multicomponent regulation of actin barbed end assembly by twinfilin, formin and capping protein.

Ulrichs H, Gaska I, Shekhar S Nat Commun. 2023; 14(1):3981.

PMID: 37414761 PMC: 10326068. DOI: 10.1038/s41467-023-39655-3.

Coordination of actin plus-end dynamics by IQGAP1, formin, and capping protein.

Pimm M, Haarer B, Nobles A, Haney L, Marcin A, Alcaide Eligio M bioRxiv. 2023; .

PMID: 37205555 PMC: 10187324. DOI: 10.1101/2023.05.04.539490.

References

Li H, Guo F, Rubinstein B, Li R . Actin-driven chromosomal motility leads to symmetry breaking in mammalian meiotic oocytes. Nat Cell Biol. 2008; 10(11):1301-8. DOI: 10.1038/ncb1788. View

Azoury J, Lee K, Georget V, Hikal P, Verlhac M . Symmetry breaking in mouse oocytes requires transient F-actin meshwork destabilization. Development. 2011; 138(14):2903-8. DOI: 10.1242/dev.060269. View

Pinot M, Steiner V, Dehapiot B, Yoo B, Chesnel F, Blanchoin L . Confinement induces actin flow in a meiotic cytoplasm. Proc Natl Acad Sci U S A. 2012; 109(29):11705-10. PMC: 3406835. DOI: 10.1073/pnas.1121583109. View

Manseau L, Calley J, Phan H . Profilin is required for posterior patterning of the Drosophila oocyte. Development. 1996; 122(7):2109-16. DOI: 10.1242/dev.122.7.2109. View

Sagot I, Rodal A, Moseley J, Goode B, Pellman D . An actin nucleation mechanism mediated by Bni1 and profilin. Nat Cell Biol. 2002; 4(8):626-31. DOI: 10.1038/ncb834. View

Dumont J, Desai A . Acentrosomal spindle assembly and chromosome segregation during oocyte meiosis. Trends Cell Biol. 2012; 22(5):241-9. PMC: 3348331. DOI: 10.1016/j.tcb.2012.02.007. View

Imamura H, Tanaka K, Hihara T, Umikawa M, Kamei T, Takahashi K . Bni1p and Bnr1p: downstream targets of the Rho family small G-proteins which interact with profilin and regulate actin cytoskeleton in Saccharomyces cerevisiae. EMBO J. 1997; 16(10):2745-55. PMC: 1169884. DOI: 10.1093/emboj/16.10.2745. View

Romero S, Clainche C, Didry D, Egile C, Pantaloni D, Carlier M . Formin is a processive motor that requires profilin to accelerate actin assembly and associated ATP hydrolysis. Cell. 2004; 119(3):419-29. DOI: 10.1016/j.cell.2004.09.039. View

Verlhac M, Lefebvre C, Guillaud P, Rassinier P, Maro B . Asymmetric division in mouse oocytes: with or without Mos. Curr Biol. 2000; 10(20):1303-6. DOI: 10.1016/s0960-9822(00)00753-3. View

10.

Ramabhadran V, Hatch A, Higgs H . Actin monomers activate inverted formin 2 by competing with its autoinhibitory interaction. J Biol Chem. 2013; 288(37):26847-55. PMC: 3772231. DOI: 10.1074/jbc.M113.472415. View

11.

Seth Chhabra E, Higgs H . INF2 Is a WASP homology 2 motif-containing formin that severs actin filaments and accelerates both polymerization and depolymerization. J Biol Chem. 2006; 281(36):26754-67. DOI: 10.1074/jbc.M604666200. View

12.

Ito T, Narita A, Hirayama T, Taki M, Iyoshi S, Yamamoto Y . Human spire interacts with the barbed end of the actin filament. J Mol Biol. 2011; 408(1):18-25. DOI: 10.1016/j.jmb.2010.12.045. View

13.

Rosales-Nieves A, Johndrow J, Keller L, Magie C, Pinto-Santini D, Parkhurst S . Coordination of microtubule and microfilament dynamics by Drosophila Rho1, Spire and Cappuccino. Nat Cell Biol. 2006; 8(4):367-76. PMC: 1997291. DOI: 10.1038/ncb1385. View

14.

Kinosian H, Selden L, Gershman L, Estes J . Actin filament barbed end elongation with nonmuscle MgATP-actin and MgADP-actin in the presence of profilin. Biochemistry. 2002; 41(21):6734-43. DOI: 10.1021/bi016083t. View

15.

Pernier J, Orban J, Avvaru B, Jegou A, Romet-Lemonne G, Guichard B . Dimeric WH2 domains in Vibrio VopF promote actin filament barbed-end uncapping and assisted elongation. Nat Struct Mol Biol. 2013; 20(9):1069-76. DOI: 10.1038/nsmb.2639. View

16.

Schuh M, Ellenberg J . Self-organization of MTOCs replaces centrosome function during acentrosomal spindle assembly in live mouse oocytes. Cell. 2007; 130(3):484-98. DOI: 10.1016/j.cell.2007.06.025. View

17.

Kovar D, Kuhn J, Tichy A, Pollard T . The fission yeast cytokinesis formin Cdc12p is a barbed end actin filament capping protein gated by profilin. J Cell Biol. 2003; 161(5):875-87. PMC: 2172974. DOI: 10.1083/jcb.200211078. View

18.

Dahlgaard K, Raposo A, Niccoli T, St Johnston D . Capu and Spire assemble a cytoplasmic actin mesh that maintains microtubule organization in the Drosophila oocyte. Dev Cell. 2007; 13(4):539-53. PMC: 2034408. DOI: 10.1016/j.devcel.2007.09.003. View

19.

Chaigne A, Campillo C, Gov N, Voituriez R, Azoury J, Umana-Diaz C . A soft cortex is essential for asymmetric spindle positioning in mouse oocytes. Nat Cell Biol. 2013; 15(8):958-66. DOI: 10.1038/ncb2799. View

20.

Kovar D, Harris E, Mahaffy R, Higgs H, Pollard T . Control of the assembly of ATP- and ADP-actin by formins and profilin. Cell. 2006; 124(2):423-35. DOI: 10.1016/j.cell.2005.11.038. View