Smith Kyle P, Chakravarthy Srinivas, Rahi Amit, Chakraborty Manas, Vosberg Kristen M, Tonelli Marco, Plach Maximilian G, Grigorescu Arabela A, Curtis Joseph E, Varma Dileep
Department of Cell & Developmental Biology, Northwestern University Feinberg School of Medicine, Chicago, Illinois, USA.
Biophysics Collaborative Access Team, Argonne National Laboratory, Argonne, Illinois, USA.
Cytoskeleton (Hoboken). 2024 Nov 6. doi: 10.1002/cm.21954.
Cdt1 is a mixed folded protein critical for DNA replication licensing and it also has a "moonlighting" role at the kinetochore via direct binding to microtubules and the Ndc80 complex. However, it is unknown how the structure and conformations of Cdt1 could allow it to participate in these multiple, unique sets of protein complexes. While robust methods exist to study entirely folded or unfolded proteins, structure-function studies of combined, mixed folded/disordered proteins remain challenging. In this work, we employ orthogonal biophysical and computational techniques to provide structural characterization of mitosis-competent human Cdt1. Thermal stability analyses shows that both folded winged helix domains1 are unstable. CD and NMR show that the N-terminal and linker regions are intrinsically disordered. DLS shows that Cdt1 is monomeric and polydisperse, while SEC-MALS confirms that it is monomeric at high concentrations, but without any apparent inter-molecular self-association. SEC-SAXS enabled computational modeling of the protein structures. Using the program SASSIE, we performed rigid body Monte Carlo simulations to generate a conformational ensemble of structures. We observe that neither fully extended nor extremely compact Cdt1 conformations are consistent with SAXS. The best-fit models have the N-terminal and linker disordered regions extended into the solution and the two folded domains close to each other in apparent "folded over" conformations. We hypothesize the best-fit Cdt1 conformations could be consistent with a function as a scaffold protein that may be sterically blocked without binding partners. Our study also provides a template for combining experimental and computational techniques to study mixed-folded proteins.
Cdt1是一种对DNA复制许可至关重要的混合折叠蛋白,它还通过直接结合微管和Ndc80复合体在动粒上发挥“兼职”作用。然而,尚不清楚Cdt1的结构和构象如何使其能够参与这些多种独特的蛋白质复合体。虽然存在研究完全折叠或未折叠蛋白质的强大方法,但对组合的、混合折叠/无序蛋白质的结构-功能研究仍然具有挑战性。在这项工作中,我们采用正交的生物物理和计算技术来提供有丝分裂能力的人类Cdt1的结构表征。热稳定性分析表明,两个折叠的翼状螺旋结构域1都不稳定。圆二色光谱(CD)和核磁共振(NMR)表明,N端和连接区本质上是无序的。动态光散射(DLS)表明Cdt1是单体且多分散的,而尺寸排阻色谱-多角度激光光散射(SEC-MALS)证实它在高浓度下是单体,但没有任何明显的分子间自缔合。尺寸排阻色谱-小角X射线散射(SEC-SAXS)实现了蛋白质结构的计算建模。使用SASSIE程序,我们进行了刚体蒙特卡罗模拟以生成结构的构象集合。我们观察到,完全伸展或极其紧凑的Cdt1构象都与小角X射线散射不一致。最佳拟合模型中,N端和连接无序区延伸到溶液中,两个折叠结构域以明显的“折叠”构象彼此靠近。我们推测,最佳拟合的Cdt1构象可能与作为支架蛋白的功能一致,在没有结合伴侣的情况下可能会受到空间位阻。我们的研究还为结合实验和计算技术研究混合折叠蛋白提供了一个模板。