Comparative analysis of permanent and transient domain-domain interactions in multi-domain proteins.
domain repeats
hydrophobic interactions
multi-domain proteins
normal mode analysis
protein folds
residue conservation
Journal
Proteins
ISSN: 1097-0134
Titre abrégé: Proteins
Pays: United States
ID NLM: 8700181
Informations de publication
Date de publication:
12 Oct 2023
12 Oct 2023
Historique:
revised:
09
08
2023
received:
31
05
2023
accepted:
11
08
2023
pubmed:
13
10
2023
medline:
13
10
2023
entrez:
13
10
2023
Statut:
aheadofprint
Résumé
Protein domains are structural, functional, and evolutionary units. These domains bring out the diversity of functionality by means of interactions with other co-existing domains and provide stability. Hence, it is important to study intra-protein inter-domain interactions from the perspective of types of interactions. Domains within a chain could interact over short timeframes or permanently, rather like protein-protein interactions (PPIs). However, no systematic study has been carried out between two classes, namely permanent and transient domain-domain interactions. In this work, we studied 263 two-domain proteins, belonging to either of these classes and their interfaces on the basis of several factors, such as interface area and details of interactions (number, strength, and types of interactions). We also characterized them based on residue conservation at the interface, correlation of residue motions across domains, its involvement in repeat formation, and their involvement in particular molecular processes. Finally, we could analyze the interactions arising from domains in two-domain monomeric proteins, and we observed significant differences between these two classes of domain interactions and a few similarities. This study will help to obtain a better understanding of structure-function and folding principles of multi-domain proteins.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Department of Biotechnology, Ministry of Science and Technology, India
ID : BT/PR40187/BTIS/137/9/2021
Organisme : Institute of Bioinformatics and Applied Biotechnology
ID : IBAB/MSCB/182/2022
Organisme : Science and Engineering Research Board
ID : JBR/2021/000006
Informations de copyright
© 2023 Wiley Periodicals LLC.
Références
Levy ED, Pereira-Leal JB. Evolution and dynamics of protein interactions and networks. Curr Opin Struct Biol. 2008;18(3):349-357. doi:10.1016/j.sbi.2008.03.003
Reichmann D, Rahat O, Cohen M, Neuvirth H, Schreiber G. The molecular architecture of protein-protein binding sites. Curr Opin Struct Biol. 2007;17(1):67-76. doi:10.1016/j.sbi.2007.01.004
Vidal M, Cusick ME, Barabási AL. Interactome networks and human disease. Cell. 2011;144(6):986-998. doi:10.1016/j.cell.2011.02.016
Nooren IMA, Thornton JM. Diversity of protein-protein interactions. EMBO J. 2003;22(14):3486-3492. doi:10.1093/emboj/cdg359
Janin J, Bahadur RP, Chakrabarti P. Protein-protein interaction and quaternary structure. Q Rev Biophys. 2008;41(2):133-180. doi:10.1017/S0033583508004708
Acuner Ozbabacan SE, Engin HB, Gursoy A, Keskin O. Transient protein-protein interactions. Protein Eng Des Sel. 2011;24(9):635-648. doi:10.1093/protein/gzr025
Perkins JR, Diboun I, Dessailly BH, Lees JG, Orengo C. Transient protein-protein interactions: structural, functional, and network properties. Structure. 2010;18(10):1233-1243. doi:10.1016/J.STR.2010.08.007
Ohlson S. Designing transient binding drugs: a new concept for drug discovery. Drug Discov Today. 2008;13(9-10):433-439. doi:10.1016/J.DRUDIS.2008.02.001
Rudolph J. Inhibiting transient protein-protein interactions: lessons from the Cdc25 protein tyrosine phosphatases. Nat Rev Cancer. 2007;7(3):202-211. doi:10.1038/nrc2087
Nooren IMA, Thornton JM. Structural characterisation and functional significance of transient protein-protein interactions. J Mol Biol. 2003;325(5):991-1018. doi:10.1016/S0022-2836(02)01281-0
De S, Krishnadev O, Srinivasan N, Rekha N. Interaction preferences across protein-protein interfaces of obligatory and non-obligatory components are different. BMC Struct Biol. 2005;5(1):1-16. doi:10.1186/1472-6807-5-15
Jones S, Thornton JM. Principles of protein-protein interactions. Proc Natl Acad Sci USA. 1996;93(1):13-20. doi:10.1073/pnas.93.1.13
Lo CL, Chothia C, Janin J. The atomic structure of protein-protein recognition sites. J Mol Biol. 1999;285(5):2177-2198. doi:10.1006/JMBI.1998.2439
Bahadur RP, Chakrabarti P, Rodier F, Janin J. A dissection of specific and non-specific protein-protein interfaces. J Mol Biol. 2004;336(4):943-955. doi:10.1016/J.JMB.2003.12.073
Mintseris J, Weng Z. Structure, function, and evolution of transient and obligate protein-protein interactions. Proc Natl Acad Sci USA. 2005;102(31):10930-10935. doi:10.1073/PNAS.0502667102/SUPPL_FILE/INDEX.HTML
Zhu H, Domingues FS, Sommer I, Lengauer T. NOXclass: prediction of protein-protein interaction types. BMC Bioinformatics. 2006;7(1):27. doi:10.1186/1471-2105-7-27
Kottha S, Schroeder Biotec M, Dresden T. Classifying Permanent and Transient Protein Interactions. 2006.
Vennmann E, Schneider N, Rarey M. Discrimination of permanent and transient heterodimers: The real challenge in the classification of protein-protein interactions. Published online, 1-9. 2012.
Block P, Paern J, Hüllermeier E, Sanschagrin P, Sotriffer CA, Klebe G. Physicochemical descriptors to discriminate protein-protein interactions in permanent and transient complexes selected by means of machine learning algorithms. Proteins: Struct Funct Genet. 2006;65(3):607-622. doi:10.1002/prot.21104
Liu Q, Li J. Propensity vectors of low-ASA residue pairs in the distinction of protein interactions. Proteins: Struct Funct Bioinformatics. 2009;78(3):589-602. doi:10.1002/prot.22583
Mintseris J, Weng Z. Atomic contact vectors in protein-protein recognition. Proteins: Struct Funct Genet. 2003;53(3):629-639. doi:10.1002/prot.10432
Maleki M, Hall M, Rueda L, Using structural domains to predict obligate and non-obligate protein-protein interactions. IEEE symposium on computational intelligence and computational biology, CIBCB 2012. Published online. Vol 2012; 2012:9-15. doi:10.1109/CIBCB.2012.6217204
Maleki M, Aziz MM, Rueda L. Analysis of relevant physicochemical properties in obligate and non-obligate protein-protein interactions. IEEE international conference on bioinformatics and biomedicine workshops, BIBMW 2011. Published online. Vol 2011; 2011:345-351. doi:10.1109/BIBMW.2011.6112397
Maleki M, Mominul Aziz M, Rueda L. Analysis of obligate and non-obligate complexes using Desolvation energies in domain-domain interactions. Published online 2011.
Rueda L, Banerjee S, Aziz MM, Raza M. Protein-protein interaction prediction using desolvation energies and interface properties. Proceedings-2010 IEEE International Conference on Bioinformatics and Biomedicine, BIBM 2010. Published online. Vol 2010:17-22. doi:10.1109/BIBM.2010.5706528
Ofran Y, Rost B. Analysing six types of protein-protein interfaces. J Mol Biol. 2003;325(2):377-387. doi:10.1016/S0022-2836(02)01223-8
Goebels F, Frishman D. Prediction of protein interaction types based on sequence and network features. BMC Syst Biol. 2013;7(6):16-18. doi:10.1186/1752-0509-7-S6-S5
La D, Kong M, Hoffman W, Choi YI, Kihara D. Predicting permanent and transient protein-protein interfaces. Proteins: Struct Funct Bioinformatics. 2013;81(5):805-818. doi:10.1002/PROT.24235
Phillips DC. The three-dimensional structure of an enzyme molecule. Sci Am. 1966;215(5):78-90. doi:10.1038/SCIENTIFICAMERICAN1166-78
Wetlaufer DB. Nucleation, rapid folding, and globular Intrachain regions in proteins. Proc Natl Acad Sci USA. 1973;70(3):697-701. doi:10.1073/PNAS.70.3.697
Orengo CA, Thornton JM. Protein families and their evolution-a structural perspective. Annu Rev Biochem. 2005;74(1):867-900. doi:10.1146/annurev.biochem.74.082803.133029
Vinayagam A, Shi J, Pugalenthi G, Meenakshi B, Blundell TL, Sowdhamini R. DDBASE2.0: updated domain database with improved identification of structural domains. Bioinformatics. 2003;19(14):1760-1764. doi:10.1093/BIOINFORMATICS/BTG233
Sowdhamini R, Blundell TL. An automatic method involving cluster analysis of secondary structures for the identification of domains in proteins. Protein Sci. 1995;4(3):506-520. doi:10.1002/PRO.5560040317
Holm L, Sander C. Parser for protein folding units. Proteins: Struct Funct Bioinformatics. 1994;19(3):256-268. doi:10.1002/PROT.340190309
Swindells MB. A procedure for detecting structural domains in proteins. Protein Sci. 1995;4(1):103-112. doi:10.1002/PRO.5560040113
Siddiqui AS, Barton GJ. Continuous and discontinuous domains: an algorithm for the automatic generation of reliable protein domain definitions. Protein Sci. 1995;4(5):872-884. doi:10.1002/PRO.5560040507
Gelly JC, de Brevern AG, Hazout S. ‘Protein peeling’: an approach for splitting a 3D protein structure into compact fragments. Bioinformatics. 2006;22(2):129-133. doi:10.1093/BIOINFORMATICS/BTI773
Taheri-Ledari M, Zandieh A, Shariatpanahi SP, Eslahchi C. Assignment of structural domains in proteins using diffusion kernels on graphs. BMC Bioinformatics. 2022;23(1):369. doi:10.1186/S12859-022-04902-9
Islam SA, Luo J, Sternberg MJE. Identification and analysis of domains in proteins. Protein Eng Des Sel. 1995;8(6):513-526. doi:10.1093/PROTEIN/8.6.513
Vogel C, Bashton M, Kerrison ND, Chothia C, Teichmann SA. Structure, function and evolution of multidomain proteins. Curr Opin Struct Biol. 2004;14(2):208-216. doi:10.1016/J.SBI.2004.03.011
Itzhaki Z, Akiva E, Altuvia Y, Margalit H. Evolutionary conservation of domain-domain interactions. Genome Biol. 2006;7(12):1-12. doi:10.1186/GB-2006-7-12-R125/TABLES/4
Memišević V, Wallqvist A, Reifman J. Reconstituting protein interaction networks using parameter-dependent domain-domain interactions. BMC Bioinformatics. 2013;14(1):1-15. doi:10.1186/1471-2105-14-154/FIGURES/5
Aloy P, Russell RB. InterPreTS: protein interaction prediction through tertiary structure. Bioinformatics. 2003;19(1):161-162. doi:10.1093/BIOINFORMATICS/19.1.161
Li X, Yang L, Zhang X, Jiao X. Prediction of protein-protein interactions based on domain. Comput Math Methods Med. 2019;2019:1-7. doi:10.1155/2019/5238406
Deng M, Mehta S, Sun F, Chen T. Inferring domain-domain interactions from protein-protein interactions. Genome Res. 2002;12(10):1540-1548. doi:10.1101/GR.153002
González AJ, Liao L. Predicting domain-domain interaction based on domain profiles with feature selection and support vector machines. BMC Bioinformatics. 2010;11(1):1-14. doi:10.1186/1471-2105-11-537/TABLES/3
Zhao XM, Chen L. Domain-Domain Interaction Identification With A Feature Selection Approach. Lecture Notes in Computer Science (Including Subseries Lecture Notes in Artificial Intelligence and Lecture Notes in Bioinformatics). Springer, Berlin, Heidelberg, Vol 5265; 2008:178-186. doi:10.1007/978-3-540-88436-1_16/COVER
Sprinzak E, Margalit H. Correlated sequence-signatures as markers of protein-protein interaction. J Mol Biol. 2001;311(4):681-692. doi:10.1006/JMBI.2001.4920
Basu MK, Poliakov E, Rogozin IB. Domain mobility in proteins: functional and evolutionary implications. Brief Bioinform. 2009;10(3):205-216. doi:10.1093/BIB/BBN057
Basu MK, Carmel L, Rogozin IB, Koonin EV. Evolution of protein domain promiscuity in eukaryotes. Genome Res. 2008;18(3):449-461. doi:10.1101/GR.6943508
Yu L, Tanwar DK, Penha EDS, Wolf YI, Koonin EV, Basu MK. Grammar of protein domain architectures. Proc Natl Acad Sci USA. 2019;116(9):3636-3645. doi:10.1073/pnas.1814684116
Bhaskara RM, Srinivasan N. Stability of domain structures in multi-domain proteins. Sci Rep. 2011;1:40. doi:10.1038/SREP00040
Vishwanath S, de Brevern AG, Srinivasan N. Same but not alike: structure, flexibility and energetics of domains in multi-domain proteins are influenced by the presence of other domains. PLoS Comput Biol. 2018;14(2):e1006008. doi:10.1371/JOURNAL.PCBI.1006008
Winter C, Henschel A, Kim WK, Schroeder M. SCOPPI: a structural classification of protein-protein interfaces. Nucleic Acids Res. 2006;34(suppl_1):D310-D314. doi:10.1093/NAR/GKJ099
von Eichborn J, Günther S, Preissner R. Structural features and evolution of protein-protein interactions. Genome Inform. 2010;22:1-10. doi:10.1142/9781848165786_0001
Jones S, Marin A, Thornton JM. Protein domain interfaces: characterization and comparison with oligomeric protein interfaces. Protein Eng. 2000;13(2):77-82. doi:10.1093/protein/13.2.77
Fox NK, Brenner SE, Chandonia JM. SCOPe: structural classification of proteins-extended, integrating SCOP and ASTRAL data and classification of new structures. Nucleic Acids Res. 2014;42(D1):D304-D309. doi:10.1093/nar/gkt1240
Li W, Godzik A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics. 2006;22(13):1658-1659. doi:10.1093/BIOINFORMATICS/BTL158
Berman HM, Westbrook J, Feng Z, et al. The protein data Bank. Nucleic Acids Res. 2000;28(1):235-242. doi:10.1093/nar/28.1.235
Gong S, Yoon G, Jang I, et al. PSIbase: a database of protein structural Interactome map (PSIMAP). Bioinformatics. 2005;21(10):2541-2543. doi:10.1093/BIOINFORMATICS/BTI366
Tina KG, Bhadra R, Srinivasan N. PIC: protein interactions calculator. Nucleic Acids Res. 2007;35(SUPPL.2):W473-W476. doi:10.1093/nar/gkm423
Bhaskara RM, de Brevern AG, Srinivasan N. Understanding the role of domain-domain linkers in the spatial orientation of domains in multi-domain proteins. J Biomol Struct Dyn. 2013;31(12):1467-1480. doi:10.1080/07391102.2012.743438
George RA, Heringa J. An analysis of protein domain linkers: their classification and role in protein folding. Protein Eng. 2002;15(11):871-879. doi:10.1093/protein/15.11.871
Rodrigues JPGLM, Teixeira JMC, Trellet M, Bonvin AMJJ. pdb-tools: a swiss army knife for molecular structures. F1000Research. 2018;7:1961. doi:10.12688/f1000research.17456.1
Konagurthu AS, Whisstock JC, Stuckey PJ, Lesk AM. MUSTANG: A multiple structural alignment algorithm. Proteins: Struct Funct Genet. 2006;64(3):559-574. doi:10.1002/prot.20921
Sukhwal A, Sowdhamini R. Oligomerisation status and evolutionary conservation of interfaces of protein structural domain superfamilies. Mol Biosyst. 2013;9(7):1652-1661. doi:10.1039/C3MB25484D
Abraham MJ, Murtola T, Schulz R, et al. GROMACS: high performance molecular simulations through multi-level parallelism from laptops to supercomputers. SoftwareX. 2015;1-2:19-25. doi:10.1016/J.SOFTX.2015.06.001
Thomas PD, Ebert D, Muruganujan A, Mushayahama T, Albou LP, Mi H. PANTHER: making genome-scale phylogenetics accessible to all. Protein Sci. 2022;31(1):8-22. doi:10.1002/PRO.4218
Ben Chorin A, Masrati G, Kessel A, et al. ConSurf-DB: an accessible repository for the evolutionary conservation patterns of the majority of PDB proteins. Protein Sci. 2020;29(1):258-267. doi:10.1002/PRO.3779
Bakan A, Meireles LM, Bahar I. ProDy: protein dynamics inferred from theory and experiments. Bioinformatics. 2011;27(11):1575-1577. doi:10.1093/BIOINFORMATICS/BTR168
Bateman A. UniProt: a worldwide hub of protein knowledge. Nucleic Acids Res. 2019;47(D1):D506-D515. doi:10.1093/NAR/GKY1049
di Domenico T, Potenza E, Walsh I, et al. RepeatsDB: a database of tandem repeat protein structures. Nucleic Acids Res. 2014;42(D1):D352-D357. doi:10.1093/NAR/GKT1175
Chothia C, Lesk AM. The relation between the divergence of sequence and structure in proteins. EMBO J. 1986;5(4):823-826. doi:10.1002/J.1460-2075.1986.TB04288.X
Argos P. An investigation of protein subunit and domain interfaces. Protein Eng Des Sel. 1988;2(2):101-113. doi:10.1093/PROTEIN/2.2.101
Keskin O, Gursoy A, Ma B, Nussinov R. Principles of protein-protein interactions: what are the preferred ways for proteins to interact? Chem Rev. 2008;108(4):1225-1244. doi:10.1021/CR040409X/ASSET/IMAGES/LARGE/CR040409XF00013.JPEG
Chothia C, Janin J. Principles of protein-protein recognition. Nature. 1975;256(5520):705-708. doi:10.1038/256705a0
Fersht AR. Basis of biological specificity. Trends Biochem Sci. 1984;9(4):145-147. doi:10.1016/0968-0004(84)90122-1
Caffrey DR, Somaroo S, Hughes JD, Mintseris J, Huang ES. Are protein-protein interfaces more conserved in sequence than the rest of the protein surface? Protein Sci. 2004;13(1):190-202. doi:10.1110/PS.03323604
Bordner AJ, Abagyan R. Statistical analysis and prediction of protein-protein interfaces. Proteins: Struct Funct Bioinformatics. 2005;60(3):353-366. doi:10.1002/PROT.20433
Choi YS, Yang JS, Choi Y, Ryu SH, Kim S. Evolutionary conservation in multiple faces of protein interaction. Proteins: Struct Funct Bioinformatics. 2009;77(1):14-25. doi:10.1002/PROT.22410
Kajava AV. Tandem repeats in proteins: from sequence to structure. J Struct Biol. 2012;179(3):279-288. doi:10.1016/J.JSB.2011.08.009
Doolittle RF. The multiplicity of domains in proteins. Annu Rev Biochem. 1995;64:287-314. doi:10.1146/annurev.bi.64.070195.001443
Orengo CA, Jones DT, Thornton JM. Protein superfamilles and domain superfolds. Nature. 1994;372(6507):631-634. doi:10.1038/372631a0
Koonin EV, Wolf YI, Karev GP. The structure of the protein universe and genome evolution. Nature. 2002;420(6912):218-223. doi:10.1038/nature01256
Karev GP, Wolf YI, Rzhetsky AY, Berezovskaya FS, Koonin EV. Birth and death of protein domains: a simple model of evolution explains power law behavior. BMC Evol Biol. 2002;2(1):1-26. doi:10.1186/1471-2148-2-18
Naveenkumar N, Kumar G, Sowdhamini R, Srinivasan N, Vishwanath S. Fold combinations in multi-domain proteins. Bioinformation. 2019;15(5):342-350. doi:10.6026/97320630015342