Hydration of Protein-RNA Recognition Sites

Overview

Journal Nucleic Acids Res

Publisher Oxford University Press

Specialty Biochemistry

Date 2014 Aug 13

PMID 25114050

Citations 13

Authors

Amita Barik

Ranjit Prasad Bahadur

Affiliations

Soon will be listed here.

Abstract

We investigate the role of water molecules in 89 protein-RNA complexes taken from the Protein Data Bank. Those with tRNA and single-stranded RNA are less hydrated than with duplex or ribosomal proteins. Protein-RNA interfaces are hydrated less than protein-DNA interfaces, but more than protein-protein interfaces. Majority of the waters at protein-RNA interfaces makes multiple H-bonds; however, a fraction do not make any. Those making H-bonds have preferences for the polar groups of RNA than its partner protein. The spatial distribution of waters makes interfaces with ribosomal proteins and single-stranded RNA relatively 'dry' than interfaces with tRNA and duplex RNA. In contrast to protein-DNA interfaces, mainly due to the presence of the 2'OH, the ribose in protein-RNA interfaces is hydrated more than the phosphate or the bases. The minor groove in protein-RNA interfaces is hydrated more than the major groove, while in protein-DNA interfaces it is reverse. The strands make the highest number of water-mediated H-bonds per unit interface area followed by the helices and the non-regular structures. The preserved waters at protein-RNA interfaces make higher number of H-bonds than the other waters. Preserved waters contribute toward the affinity in protein-RNA recognition and should be carefully treated while engineering protein-RNA interfaces.

Citing Articles

Water-mediated ribonucleotide-amino acid pairs and higher-order structures at the RNA-protein interface: analysis of the crystal structure database and a topological classification.

Jangra R, Trant J, Sharma P NAR Genom Bioinform. 2024; 6(4):lqae161.

PMID: 39664815 PMC: 11632616. DOI: 10.1093/nargab/lqae161.

Elucidating the Role of Groove Hydration on Stability and Functions of Biased DNA Duplexes in Cell-Like Chemical Environments.

Ghosh S, Takahashi S, Ohyama T, Liu L, Sugimoto N J Am Chem Soc. 2024; 146(47):32479-32497.

PMID: 39505325 PMC: 11613987. DOI: 10.1021/jacs.4c09388.

A structural dissection of protein-RNA interactions based on different RNA base areas of interfaces.

Hu W, Qin L, Li M, Pu X, Guo Y RSC Adv. 2022; 8(19):10582-10592.

PMID: 35540439 PMC: 9078961. DOI: 10.1039/c8ra00598b.

PredPRBA: Prediction of Protein-RNA Binding Affinity Using Gradient Boosted Regression Trees.

Deng L, Yang W, Liu H Front Genet. 2019; 10:637.

PMID: 31428122 PMC: 6688581. DOI: 10.3389/fgene.2019.00637.

A structure-based model for the prediction of protein-RNA binding affinity.

Nithin C, Mukherjee S, Bahadur R RNA. 2019; 25(12):1628-1645.

PMID: 31395671 PMC: 6859855. DOI: 10.1261/rna.071779.119.

References

Luo X, Lv F, Pan Y, Kong X, Li Y, Yang Q . Structure-based prediction of the mobility and disorder of water molecules at protein-DNA interface. Protein Pept Lett. 2010; 18(2):203-9. DOI: 10.2174/092986611794475066. View

Barik A, Mishra A, Bahadur R . PRince: a web server for structural and physicochemical analysis of protein-RNA interface. Nucleic Acids Res. 2012; 40(Web Server issue):W440-4. PMC: 3394290. DOI: 10.1093/nar/gks535. View

Reddy C, Das A, Jayaram B . Do water molecules mediate protein-DNA recognition?. J Mol Biol. 2002; 314(3):619-32. DOI: 10.1006/jmbi.2001.5154. View

Rodier F, Bahadur R, Chakrabarti P, Janin J . Hydration of protein-protein interfaces. Proteins. 2005; 60(1):36-45. DOI: 10.1002/prot.20478. View

Levy Y, Onuchic J . Water mediation in protein folding and molecular recognition. Annu Rev Biophys Biomol Struct. 2006; 35:389-415. DOI: 10.1146/annurev.biophys.35.040405.102134. View

Sonavane S, Chakrabarti P . Cavities in protein-DNA and protein-RNA interfaces. Nucleic Acids Res. 2009; 37(14):4613-20. PMC: 2724294. DOI: 10.1093/nar/gkp488. View

Bui H, Schiewe A, Haworth I . WATGEN: an algorithm for modeling water networks at protein-protein interfaces. J Comput Chem. 2007; 28(14):2241-51. DOI: 10.1002/jcc.20751. View

Janin J . Wet and dry interfaces: the role of solvent in protein-protein and protein-DNA recognition. Structure. 2000; 7(12):R277-9. DOI: 10.1016/s0969-2126(00)88333-1. View

Treger M, Westhof E . Statistical analysis of atomic contacts at RNA-protein interfaces. J Mol Recognit. 2001; 14(4):199-214. DOI: 10.1002/jmr.534. View

10.

Lee B, Richards F . The interpretation of protein structures: estimation of static accessibility. J Mol Biol. 1971; 55(3):379-400. DOI: 10.1016/0022-2836(71)90324-x. View

11.

Teyra J, Pisabarro M . Characterization of interfacial solvent in protein complexes and contribution of wet spots to the interface description. Proteins. 2007; 67(4):1087-95. DOI: 10.1002/prot.21394. View

12.

Amadasi A, Spyrakis F, Cozzini P, Abraham D, Kellogg G, Mozzarelli A . Mapping the energetics of water-protein and water-ligand interactions with the "natural" HINT forcefield: predictive tools for characterizing the roles of water in biomolecules. J Mol Biol. 2006; 358(1):289-309. DOI: 10.1016/j.jmb.2006.01.053. View

13.

Bhat T, Bentley G, Boulot G, Greene M, Tello D, DallAcqua W . Bound water molecules and conformational stabilization help mediate an antigen-antibody association. Proc Natl Acad Sci U S A. 1994; 91(3):1089-93. PMC: 521459. DOI: 10.1073/pnas.91.3.1089. View

14.

Westhof E . Water: an integral part of nucleic acid structure. Annu Rev Biophys Biophys Chem. 1988; 17:125-44. DOI: 10.1146/annurev.bb.17.060188.001013. View

15.

Lam P, Jadhav P, Eyermann C, Hodge C, Ru Y, Bacheler L . Rational design of potent, bioavailable, nonpeptide cyclic ureas as HIV protease inhibitors. Science. 1994; 263(5145):380-4. DOI: 10.1126/science.8278812. View

16.

Allers J, Shamoo Y . Structure-based analysis of protein-RNA interactions using the program ENTANGLE. J Mol Biol. 2001; 311(1):75-86. DOI: 10.1006/jmbi.2001.4857. View

17.

Salgado P, Makeyev E, Butcher S, Bamford D, Stuart D, Grimes J . The structural basis for RNA specificity and Ca2+ inhibition of an RNA-dependent RNA polymerase. Structure. 2004; 12(2):307-16. DOI: 10.1016/j.str.2004.01.012. View

18.

Reichmann D, Phillip Y, Carmi A, Schreiber G . On the contribution of water-mediated interactions to protein-complex stability. Biochemistry. 2007; 47(3):1051-60. DOI: 10.1021/bi7019639. View

19.

Makarov V, Pettitt B, Feig M . Solvation and hydration of proteins and nucleic acids: a theoretical view of simulation and experiment. Acc Chem Res. 2002; 35(6):376-84. DOI: 10.1021/ar0100273. View

20.

Roe S, Teeter M . Patterns for prediction of hydration around polar residues in proteins. J Mol Biol. 1993; 229(2):419-27. DOI: 10.1006/jmbi.1993.1043. View