Department of Molecular Genetics and Microbiology, Stony Brook University, Stony Brook, New York, New York, United States of America.
PLoS One. 2013 Apr 4;8(4):e60791. doi: 10.1371/journal.pone.0060791. Print 2013.
The internal ribosomal entry site (IRES) of picornavirus genomes serves as the nucleation site of a highly structured ribonucleoprotein complex essential to the binding of the 40S ribosomal subunit and initiation of viral protein translation. The transition from naked RNA to a functional "IRESome" complex are poorly understood, involving the folding of secondary and tertiary RNA structure, facilitated by a tightly concerted binding of various host cell proteins that are commonly referred to as IRES trans-acting factors (ITAFs). Here we have investigated the influence of one ITAF, the polypyrimidine tract-binding protein 1 (PTB1), on the tropism of PV1(RIPO), a chimeric poliovirus in which translation of the poliovirus polyprotein is under the control of a human rhinovirus type 2 (HRV2) IRES element. We show that PV1(RIPO)'s growth defect in restrictive mouse cells is partly due to the inability of its IRES to interact with endogenous murine PTB. Over-expression of human PTB1 stimulated the HRV2 IRES-mediated translation, resulting in increased growth of PV1(RIPO) in murine cells and human neuronal SK-N-MC cells. Mutations within the PV1(RIPO) IRES, selected to grow in restrictive mouse cells, eliminated the human PTB1 supplementation requirement, by restoring the ability of the IRES to interact with endogenous murine PTB. In combination with our previous findings these results give a compelling insight into the thermodynamic behavior of IRES structures. We have uncovered three distinct thermodynamic aspects of IRES formation which may independently contribute to overcome the observed PV1(RIPO) IRES block by lowering the free energy δG of the IRESome formation, and stabilizing the correct and functional structure: 1) lowering the growth temperature, 2) modifying the complement of ITAFs in restricted cells, or 3) selection of adaptive mutations. All three mechanisms can conceivably modulate the thermodynamics of RNA folding, and thus facilitate and stabilize the functional IRES structure.
微小核糖核酸病毒基因组的内部核糖体进入位点 (IRES) 作为高度结构化核糖核蛋白复合物的成核位点,对于结合 40S 核糖体亚基和起始病毒蛋白翻译至关重要。从裸露 RNA 到功能性“IRESome”复合物的转变知之甚少,涉及二级和三级 RNA 结构的折叠,这是由各种宿主细胞蛋白紧密协调结合来促进的,这些蛋白通常被称为 IRES 反式作用因子 (ITAFs)。在这里,我们研究了一种 ITAF,多嘧啶 tract 结合蛋白 1 (PTB1) 对嵌合脊髓灰质炎病毒 1 (RIPO) 嗜性的影响,该病毒中脊髓灰质炎病毒多蛋白的翻译受人类鼻病毒 2 (HRV2) IRES 元件的控制。我们表明,PV1(RIPO) 在限制条件下的小鼠细胞中的生长缺陷部分是由于其 IRES 无法与内源性鼠源 PTB 相互作用所致。过表达人源 PTB1 可刺激 HRV2 IRES 介导的翻译,从而增加 PV1(RIPO) 在鼠细胞和人神经元 SK-N-MC 细胞中的生长。选择在限制条件下生长的 PV1(RIPO) IRES 内的突变消除了人源 PTB1 补充的需求,通过恢复 IRES 与内源性鼠源 PTB 相互作用的能力。结合我们之前的发现,这些结果深入了解了 IRES 结构的热力学行为。我们发现了 IRES 形成的三个不同的热力学方面,这些方面可能通过降低 IRESome 形成的自由能 δG 并稳定正确和功能性结构,独立有助于克服观察到的 PV1(RIPO) IRES 阻断:1)降低生长温度,2)在限制细胞中改变 ITAFs 的组成,或 3)选择适应性突变。所有这三种机制都可以想象地调节 RNA 折叠的热力学,从而促进和稳定功能性 IRES 结构。