Duh Yulander, Hsiao Yu-Yuan, Li Chia-Lung, Huang Jason C, Yuan Hanna S
Institute of Molecular Biology, Academia Sinica, Taipei, Taiwan, 11529, Republic of China.
Department of Biotechnology and Laboratory Science in Medicine, National Yang-Ming University, Taipei, Taiwan, 112, Republic of China.
Protein Sci. 2015 Dec;24(12):1934-41. doi: 10.1002/pro.2800. Epub 2015 Sep 18.
RNase T is a classical member of the DEDDh family of exonucleases with a unique sequence preference in that its 3'-to-5' exonuclease activity is blocked by a 3'-terminal dinucleotide CC in digesting both single-stranded RNA and DNA. Our previous crystal structure analysis of RNase T-DNA complexes show that four phenylalanine residues, F29, F77, F124, and F146, stack with the two 3'-terminal nucleobases. To elucidate if the π-π stacking interactions between aromatic residues and nucleobases play a critical role in sequence-specific protein-nucleic acid recognition, here we mutated two to four of the phenylalanine residues in RNase T to tryptophan (W mutants) and tyrosine (Y mutants). The Escherichia coli strains expressing either the W mutants or the Y mutants had slow growth phenotypes, suggesting that all of these mutants could not fully substitute the function of the wild-type RNase T in vivo. DNA digestion assays revealed W mutants shared similar sequence specificity with wild-type RNase T. However, the Y mutants exhibited altered sequence-dependent activity, digesting ssDNA with both 3'-end CC and GG sequences. Moreover, the W and Y mutants had reduced DNA-binding activity and lower thermal stability as compared to wild-type RNase T. Taken together, our results suggest that the four phenylalanine residues in RNase T not only play critical roles in sequence-specific recognition, but also in overall protein stability. Our results provide the first evidence showing that the π-π stacking interactions between nucleobases and protein aromatic residues may guide the sequence-specific activity for DNA and RNA enzymes.
核糖核酸酶T是核酸外切酶DEDDh家族的经典成员,具有独特的序列偏好性,即其3'至5'核酸外切酶活性在消化单链RNA和DNA时会被3'末端二核苷酸CC阻断。我们之前对核糖核酸酶T-DNA复合物的晶体结构分析表明,四个苯丙氨酸残基F29、F77、F124和F146与两个3'末端核碱基堆积。为了阐明芳香族残基与核碱基之间的π-π堆积相互作用在序列特异性蛋白质-核酸识别中是否起关键作用,我们将核糖核酸酶T中的两个至四个苯丙氨酸残基突变为色氨酸(W突变体)和酪氨酸(Y突变体)。表达W突变体或Y突变体的大肠杆菌菌株具有生长缓慢的表型,这表明所有这些突变体在体内都不能完全替代野生型核糖核酸酶T的功能。DNA消化试验表明,W突变体与野生型核糖核酸酶T具有相似的序列特异性。然而,Y突变体表现出改变的序列依赖性活性,能够消化3'末端为CC和GG序列的单链DNA。此外,与野生型核糖核酸酶T相比,W和Y突变体的DNA结合活性降低,热稳定性也较低。综上所述,我们的结果表明,核糖核酸酶T中的四个苯丙氨酸残基不仅在序列特异性识别中起关键作用,而且在整体蛋白质稳定性中也起关键作用。我们的结果提供了首个证据,表明核碱基与蛋白质芳香族残基之间的π-π堆积相互作用可能指导DNA和RNA酶的序列特异性活性。