Molecular Mechanism of Synonymous Codons Usage Patterns Control Ribosome Scanning Rhythms
GAO Ming-Yang1,2,3, WU Yu-Hu1,2,3, YANG Xuan-Ye1,2,3, WANG Jin-Qian1,2,3, HU Xin-Yan1,2,3, ZHOU Jian-Hua1,2,4,*
1 Key Laboratory of Biotechnology and Bioengineering of State Ethnic Affairs Commission, Biomedical Research Center, Northwest Minzu University, Lanzhou 730030, China; 2 Gansu Tech Innovation Center of Animal Cell, Lanzhou 730030, China; 3 College of Life Science and Engineering, Northwest Minzu University, Lanzhou 730010, China; 4 Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou 730046, China
Abstract:In translation process, the correct folding of the native polypeptide chain is regarded as the cornerstone for the biological activity of proteins. However, the correct spatial conformation of the native polypeptide chain is generally performed by the co-translation folding mechanism. The biogenetic effects of synonymous codon usage patterns on translation play important roles in ribosomal scanning mRNA. More and more studies have shown that although synonymous codon usage variations fail to impair amino acid sequence of protein, the preference of synonymous usage pattern perform a profound effect on the folding dynamic for the native polypeptide chain, especially on the regulation of the ribosomal scanning speeds. The purpose of this review is to explain the important role of synonymous codon usage patterns in the translation process and the mechanism of their influence on translation dynamics, and to identify their important role in the correct folding of proteins into their natural conformations. Synonymous codons are also associated with many diseases, this paper provides ideas for the research of protein synthesis and diseases caused by dysrhythmicity of ribosomes.
[1] 冯茜莉, 王慧慧, 汪梦竹, 等. 2022. 同义密码子通过精微翻译选择机制实现对基因的表达调控[J]. 微生物学报, 62(10): 3681-3695. (Feng X L, Wang H H, Wang M Z, et al.2022. Synonymous codons regulate gene expression through subtle translation selection mechanism[J].Acta Microbiologica Sinica, 62(10): 3681-3695.) [2] 高明阳, 杨宣叶, 吴玉湖, 等. 2024. 核糖体质控在精微调控蛋白质合成中的作用机制及意义[J/OL].微生物学通报, DOI: 10.13344/j.microbiol.china.230897. (Gao M Y, Yang X Y,Wu Y H, et al.2024. Mechanism and significance of ribosome quality control in subtle regulation of protein synthesis[J/OL]. Microbiology China, DOI: 10.13344/j.microbiol.china.230897.) [3] 梁菲菲. 2010. 密码子偏性的影响因素及研究意义[J]. 畜牧与饲料科学, 31(01): 118-119. (Liang F F.2010. Influencing factors and research significance of codon bias[J]. Animal Husbandry and Feed Science,31(01):118-119) [4] 柳树群, 刘次全. 1999. mRNA的序列、结构以及翻译速率与蛋白质结构的关系[J]. 动物学研究, (06): 457-461. (Liu S Q,Liu C Q. 1999. The sequence, structure, and translation rate of mRNA vs protein structure[J]. Zoological Research, (06): 457-461.) [5] 蒲飞洋, 李易聪, 王慧慧, 等. 2022. 同义密码子使用模式对蛋白产物表达及构象形成的影响[J]. 中国生物工程杂志, 42(03): 91-98. (Pu F Y, Li Y C, Wang H H, et al.2022. Effect of synonymous codon usage pattern on protein product expression and conformation[J]. China Biotechnology, 42(03): 91-98.) [6] 吴宪明, 吴松峰, 任大明, 等. 2007. 密码子偏性的分析方法及相关研究进展[J]. 遗传, 29(04): 420-426. (Wu X M,Wu S F, Ren D M, et al.2007. The analysis method and progress in the study of codon bias[J]. Yi Chuan, 29(4): 420-426.) [7] 郑彬琼. 2009. 大肠杆菌同义密码子偏好性概述[J]. 硅谷,(01): 23-24.(Zheng B Q. 2009. Overview of E. coli synonymous codon preference[J]. Silicon Valley, (01): 23-24.) [8] Cao X A, Hu W, Shang Y J, et al.2018. Analyses of nucleotide, synonymous codon and amino acid usages at gene levels of Brucella melitensis strain QY1[J]. Infection Genetics and Evolution, 65: 257-264. [9] Chadani Y, Ito K, Kutsukake K, et al.2012. ArfA recruits release factor 2 to rescue stalled ribosomes by peptidyl-tRNA hydrolysis in Escherichia coli[J]. Molecular Microbiology, 86(1): 37-50. [10] Cho S I.2020. A simple principle for understanding the combined cellular protein folding and aggregation[J]. Current Protein & Peptide Science, 21(1): 3-21. [11] Chong S H, Ham S.2019. Folding free energy landscape of ordered and intrinsically disordered proteins[J]. Scientific Reports, 9(1): 14927. [12] Deckert A, Cassaignau A M E, Wang X L, et al.2021. Common sequence motifs of nascent chains engage the ribosome surface and trigger factor[J]. Proceedings of the National Academy Sciences of the USA, 118(52): e2103015118. [13] Filbeck S, Cerullo F, Pfeffer S, et al.2022. Ribosome-associated quality-control mechanisms from bacteria to humans[J]. Molecular and Cellular Biochemistry, 82(8):1451-1466. [14] Fung K L, Gottesman M M.2009. A synonymous polymorphism in a common MDR1 (ABCB1) haplotype shapes protein function[J]. Acta Biochimica et Biophysica Sinica, 1794(5): 860-871. [15] Gagnon M G, Seetharaman S V, Bulkley D, et al.2012. Structural basis for the rescue of stalled ribosomes: Structure of YaeJ bound to the ribosome[J]. Science, 335(6074):1370-1372. [16] Galaz-Davison P, Román E A, Ramírez-Sarmiento C A.2021. The N-terminal domain of RfaH plays an active role in protein fold-switching[J]. PLOS Computational Biology, 17(9): e1008882. [17] Ge Z Y, Li X R, Cao X A, et al.2020. Viral adaption of staphylococcal phage: A genome-based analysis of the selective preference based on codon usage Bias[J]. Genomics, 112(6): 4657-4665. [18] Gianni S, Freiberger M I, Jemth P, et al.2021. Fuzziness and frustration in the energy landscape of protein folding, function, and assembly[J]. Accounts of Chemical Research, 54(5): 1251-1259. [19] Guyomar C, D'Urso G, Chat S, et al.2021. Structures of tmRNA and SmpB as they transit through the ribosome[J]. Nature Communications, 12(1): 4909. [20] Houben B, Rousseau F, Schymkowitz J.2022. Protein structure and aggregation: A marriage of necessity ruled by aggregation gatekeepers[J]. Trends in Biochemical Sciences, 47(3): 194-205. [21] Joseph J A, Chakraborty D, Wales D J.2019. Energy landscape for fold-switching in regulatory protein RfaH[J]. Ournal of Chemical Theory and Computation, 15(1): 731-742. [22] Kantaev R, Riwen I, Goldenzweig A, et al.2018. Manipulating the folding landscape of a multidomain protein[J]. Journal of Physical Chemistry B, 122(49): 11030-11038. [23] Komar A A.2021. A Code within a code: How codons fine-tune protein folding in the cell[J]. Biochemistry (Moscow), 86(8): 976-991. [24] Komar A A, Lesnik T, Reiss C.1999. Synonymous codon substitutions affect ribosome traffic and protein folding during in vitro translation[J]. FEBS Letters, 462(3): 387-391. [25] Lawson M R, Lessen L N, Wang J F, et al.2021. Mechanisms that ensure speed and fidelity in eukaryotic translation termination[J]. Science, 373(6557): 876-882. [26] Li G, Zhang L, Xue P.2022. Codon usage divergence of important functional genes in Mycobacterium tuberculosis[J]. International Journal of Biological Macromolecules, 209(Pt A): 1197-1204. [27] Liu Y.2020. A code within the genetic code: Codon usage regulates co-translational protein folding[J]. Cell Communication and Signaling, 18(1):145. [28] Ma X X, Wang Y N, Cao X A, et al.2018. The effects of codon usage on the formation of secondary structures of nucleocapsid protein of Peste des petits ruminants virus[J]. Genes & Genomics, 40(9): 905-912. [29] Mauger D M, Cabral B J, Presnyak V, et al.2019. mRNA structure regulates protein expression through changes in functional half-life[J]. Proceedings of the National Academy Sciences of the USA, 116(48): 24075-24083. [30] McCarthy C, Carrea A, Diambra L.2017. Bicodon bias can determine the role of synonymous SNPs in human diseases[J]. BMC Genomics, 18(1): 227. [31] Meng X, Clews J, Kargas V, et al.2017. The cystic fibrosis transmembrane conductance regulator (CFTR) and its stability[J]. Cellular and Molecular Life Sciences, 74(1): 23-38. [32] Monajemi H, Zain S M, Wan Abdullah W A T.2021. A new step in kinetic proofreading due to misacylated-tRNA during ribosomal peptide bond formation[J]. Nucleosides, Nucleotides & Nucleic Acids, 40(6): 635-646. [33] Mondal B, Thirumalai D, Reddy G.2021. Energy landscape of ubiquitin is weakly multidimensional[J]. Journal of Physical Chemistry B, 125(31): 8682-8689. [34] Neelamraju S, Gosavi S, Wales D J.2018. Energy landscape of the designed protein top7[J]. Journal of Physical Chemistry B, 122(51):12282-12291. [35] Palma M, Lejeune F.2021. Deciphering the molecular mechanism of stop codon readthrough[J]. Biological Reviews of the Cambridge Philosophical Society, 96(1): 310-329. [36] Park J, Park J, Lee B, et al.2021. The trinity of ribosome-associated quality control and stress signaling for proteostasis and neuronal physiology[J]. BMB Reports, 54(9): 439-450. [37] Parvathy S T, Udayasuriyan V, Bhadana V.2022. Codon usage bias[J]. Molecular Biology Reports, 49(1): 539-565. [38] Pintó R M, Bosch A.2021. The codon usage code for cotranslational folding of viral capsids[J]. Genome Biology and Evolution, 13(9): evab089. [39] Radhakrishnan A, Chen Y H, Martin S, et al.2016. The DEAD-Box protein dhh1p couples mRNA decay and translation by monitoring codon optimality[J]. Cell, 167(1): 122-132. [40] Rahman S U, Rehman H U, Rahman I U, et al.2023. Evolution of codon usage in Taenia saginata genomes and its impact on the host[J]. Frontiers in Veterinary Science, 9:1021440. [41] Rajasekaran N, Kaiser C M.2022. Co-translational folding of multi-domain proteins[J]. Frontiers in Molecular Biosciences, 9: 869027. [42] Ran X, Xiao J Y, Cheng F, et al.2022. Pan-cancer analyses of synonymous mutations based on tissue-specific codon optimality[J]. Computational and Structural Biotechnology Journal, 20: 3567-3580. [43] Rojano-Nisimura A M, Haning K, Janovksy J, et al.2020. Codon selection affects recruitment of ribosome-associating factors during translation[J]. ACS Synthetic Biology, 9(2): 329-342. [44] Santoni D.2021. The impact of codon choice on translation process in Saccharomyces cerevisiae: Folding class, protein function and secondary structure[J]. Journal of Theoretical Biology, 526: 110806. [45] Schiffrin B, Brockwell D J, RadfordS E.2017. Outer membrane protein folding from an energy landscape perspective[J]. BMC Biology, 15(1): 123. [46] Schwersensky M, Rooman M, Pucci F.2020. Large-scale in silico mutagenesis experiments reveal optimization of genetic code and codon usage for protein mutational robustness[J]. BMC Biology, 18(1): 146. [47] Shen P S, Park J, Qin Y D, et al.2015. Rqc2p and 60S ribosomal subunits mediate mRNA-independent elongation of nascent chains[J]. Science, 347(6217): 75-78. [48] Sørensen M A, Pedersen S.1991. Absolute in vivo translation rates of individual codons in Escherichia coli[J]. Journal of Molecular Biology, 222(2): 265-280. [49] Svetlov M S.2021. Ribosome-associated quality control in bacteria[J]. Biochemistry and cell biology, 86(8): 942-951. [50] Tsai C J, Sauna Z E, Sarfaty C K, et al.2008. Synonymous mutations and ribosome stalling can lead to altered folding pathways and distinct minima[J]. Journal of Molecular Biology, 383(2): 281-291. [51] Verma R, Reichermeier K M, Burrounghs A M, et al.2018. Vms1 and ANKZF1 peptidyl-tRNA hydrolases release nascent chains from stalled ribosomes[J]. Nature, 557(7705): 446-451 [52] Villada J C, Duran M F, Lee P K H.2020. Interplay between position-dependent codon usage bias and hydrogen bonding at the 5' end of ORFeomes[J]. mSystems, 5(4), DOI: 10.1128/mSystems.00613-20. [53] Wada M, Ito K.2019. Misdecoding of rare CGA codon by translation termination factors, eRF1/eRF3, suggests novel class of ribosome rescue pathway in S. cerevisiae[J]. FEBS Journal, 286(4): 788-802. [54] Wang X, Sun J, Zheng Y, et al.2022. Dispersion of synonymous codon usage patterns in Hepatitis E virus genomes derived from various hosts[J]. Journal of Basic Microbiology, 62(8): 975-983. [55] Wang Y N, Ji W H, Li X R, et al.2018. Unique features of nucleotide and codon usage patterns in mycoplasmas revealed by information entropy[J]. Biosystems Engineering, 165: 1-7. [56] Xu Q, Chen H, Sun W, et al.2021. Genome-wide analysis of the synonymous codon usage pattern of Streptococcus suis[J]. Microbial Pathogenesis, 150: 104732. [57] Yang Q, Yu C H, Zhao F J, et al.2019. eRF1 mediates codon usage effects on mRNA translation efficiency through premature termination at rare codons[J]. Nucleic Acids Research, 47(17): 9243-9258. [58] Zhou J H, Li H, Li X R, et al.2021. Tracing Brucella evolutionary dynamics in expanding host ranges through nucleotide, codon and amino acid usages in genomes[J]. Journal of Biomolecular Structure & Dynamics, 39(11): 3986-3995. [59] Zhou J H, Li X R, Lan X, et al.2019. The genetic divergences of codon usage shed new lights on transmission of Hepatitis E virus from swine to human[J]. Infection Genetics Evolution, 68: 23-29. [60] Zhou J H, Su J H, Chen H T, et al.2013a. Clustering of low usage codons in the translation initiation region of Hepatitis C virus[J]. Infection Genetics and Evolution, 18: 8-12. [61] Zhou J H, You Y N, Chen H T, et al.2013b. The effects of the synonymous codon usage and tRNA abundance on protein folding of the 3C protease of Foot-and-mouth disease virus[J]. Infection Genetics Evolution, 16: 270-274. [62] Zhou J H, Zhang J, Chen H T, et al.2011. The codon usage model of the context flanking each cleavage site in the polyprotein of Foot-and-mouth disease virus[J]. Infection Genetics Evolution, 11(7): 1815-1819. [63] Zhou J H, Zhang J, Ding Y J, et al.2010. Characteristics of codon usage bias in two regions downstream of the initiation codons of Foot-and-mouth disease virus[J]. Biosystems Engineering, 101(1): 20-28. [64] Zhou J H, Zhang J, Sun D J, et al.2013c. Potential roles of synonymous codon usage and tRNA concentration in hosts on the two initiation regions of Foot-and-mouth disease virus[J]. Virus Research, 176(1-2): 298-302.