Sweeney Meredith O, Collins Agnieszka, Padrick Shae B, Goode Bruce L
Rosenstiel Basic Medical Sciences Research Center, Brandeis University, Waltham, MA 02454;
Howard Hughes Medical Institute and Department of Biophysics, University of Texas Southwestern Medical Center, Dallas, TX 75390.
Mol Biol Cell. 2015 Feb 1;26(3):495-505. doi: 10.1091/mbc.E14-10-1477. Epub 2014 Dec 3.
Branched actin filament networks in cells are assembled through the combined activities of Arp2/3 complex and different WASP/WAVE proteins. Here we used TIRF and electron microscopy to directly compare for the first time the assembly kinetics and architectures of actin filament networks produced by Arp2/3 complex and dimerized VCA regions of WAVE1, WAVE2, or N-WASP. WAVE1 produced strikingly different networks from WAVE2 or N-WASP, which comprised unexpectedly short filaments. Further analysis showed that the WAVE1-specific activity stemmed from an inhibitory effect on filament elongation both in the presence and absence of Arp2/3 complex, which was observed even at low stoichiometries of WAVE1 to actin monomers, precluding an effect from monomer sequestration. Using a series of VCA chimeras, we mapped the elongation inhibitory effects of WAVE1 to its WH2 ("V") domain. Further, mutating a single conserved lysine residue potently disrupted WAVE1's inhibitory effects. Taken together, our results show that WAVE1 has unique activities independent of Arp2/3 complex that can govern both the growth rates and architectures of actin filament networks. Such activities may underlie previously observed differences between the cellular functions of WAVE1 and WAVE2.
细胞中的分支肌动蛋白丝网络是通过Arp2/3复合物和不同的WASP/WAVE蛋白的联合活动组装而成的。在这里,我们首次使用全内反射荧光显微镜(TIRF)和电子显微镜直接比较了由Arp2/3复合物以及WAVE1、WAVE2或N-WASP的二聚化VCA区域产生的肌动蛋白丝网络的组装动力学和结构。WAVE1产生的网络与WAVE2或N-WASP产生的网络显著不同,其包含意外短的细丝。进一步分析表明,WAVE1的特异性活性源于在有和没有Arp2/3复合物的情况下对细丝伸长的抑制作用,即使在WAVE1与肌动蛋白单体的低化学计量比下也能观察到这种作用,排除了单体隔离的影响。使用一系列VCA嵌合体,我们将WAVE1的伸长抑制作用定位到其WH2(“V”)结构域。此外,突变单个保守赖氨酸残基会有力地破坏WAVE1的抑制作用。综上所述,我们的结果表明,WAVE1具有独立于Arp2/3复合物的独特活性,可控制肌动蛋白丝网络的生长速率和结构。这些活性可能是先前观察到的WAVE1和WAVE2细胞功能差异的基础。