Department of Biochemistry and Biophysics, University of North Carolina at Chapel Hill, USA.
Mol Biol Evol. 2010 Feb;27(2):283-95. doi: 10.1093/molbev/msp236. Epub 2009 Oct 5.
The vertebrate filamin family (A, B, and C) is part of the spectrin family of actin cross-linking proteins. Family members share high sequence similarity (>64%) and have both common and isoform-distinct functionalities. To identify the basis for isoform-specific functionality, we perform an evolutionary trace of chordate filamin at the granularity of single residues. Our trace methodology is constrained to focus on neofunctionality by requiring that one isoform remain the ancestral type, whereas at least one isoform has an accepted mutation. We call divergence meeting these characteristics "class-distinctive." To obtain a temporal and spatial context for class-distinctive residues, we derive an all-atom model of full-length filamin A by homology modeling and joining individual domains. We map onto our model both conserved and class-distinctive residues along with the period (Teleostei, Amphibian, and Mammalian) in which they diverged. Our phylogenetic analysis suggests that filamins diverged from a common ancestral gene between urochordate and vertebrate lineages. Filamins also diverged the most just after gene duplication, in the Teleostei period, with filamin C remaining closest to ancestral filamin. At the residue level, domains with well-characterized interfaces, IgFLN 17 and IgFLN 21 (immunoglobulin, Ig), have diverged in potentially critical residues in their adhesion protein-binding interfaces, signifying that isoforms may bind or regulate ligand binding differentially. Similarly, isoform divergence in a region associated with F actin-binding regulation suggests that isoforms differentially regulate F-actin binding. In addition, we observe some class-distinctive residues in the vicinity of missense mutations that cause filamin A and B-associated skeletal disorders. Our analysis, utilizing both spatial and temporal granularity, has identified potentially important residues responsible for vertebrate filamin isoform-specific divergence-significantly in regions where few binding partners have been discovered to date- and suggests yet to be discovered filamin-binding partners and isoform-specific differential regulation with these binding partners.
脊椎动物细丝蛋白家族(A、B 和 C)是肌动蛋白交联蛋白 spectrin 家族的一部分。家族成员具有高度的序列相似性(>64%),具有共同的和同工型特异性的功能。为了确定同工型特异性功能的基础,我们在单个残基的粒度上对脊索动物细丝蛋白进行进化追踪。我们的追踪方法通过要求一个同工型保持祖先类型,而至少一个同工型具有公认的突变,从而受到限制,以专注于新功能。我们将符合这些特征的分歧称为“类别独特”。为了获得类别独特残基的时间和空间背景,我们通过同源建模和连接各个结构域来获得全长细丝蛋白 A 的全原子模型。我们将保守残基和类别独特残基以及它们在哪个时期(硬骨鱼、两栖动物和哺乳动物)发生分歧映射到我们的模型上。我们的系统发育分析表明,细丝蛋白是在尾索动物和脊椎动物谱系之间的共同祖先基因中分化出来的。细丝蛋白也在基因复制后最分化,在硬骨鱼时期,细丝蛋白 C 与祖先细丝蛋白最接近。在残基水平上,具有特征化界面的结构域,IgFLN17 和 IgFLN21(免疫球蛋白,Ig),在其粘附蛋白结合界面的潜在关键残基中发生了分化,这表明同工型可能以不同的方式结合或调节配体结合。同样,与 F 肌动蛋白结合调节相关的同工型分化表明同工型以不同的方式调节 F 肌动蛋白结合。此外,我们在导致细丝蛋白 A 和 B 相关骨骼疾病的错义突变附近观察到一些类别独特的残基。我们的分析利用空间和时间的粒度,确定了可能负责脊椎动物细丝蛋白同工型特异性分化的重要残基——在迄今为止发现的少数结合伙伴的区域中——并表明尚未发现细丝蛋白结合伙伴以及与这些结合伙伴的同工型特异性差异调节。