De-DUFing the DUFs: Deciphering distant evolutionary relationships of Domains of Unknown Function using sensitive homology detection methods

Biology Direct

Volumn 10, Issue 1, 2015, Pages

  Mudgal, Richa ^a   Sandhya, Sankaran ^a   Chandra, Nagasuma ^a   Srinivasan, Narayanaswamy ^a  

^a INDIAN INSTITUTE OF SCIENCE   (India)

Author keywords

Domain of Unknown Function (DUF); Fold assignment; Function annotation; Homology detection and protein evolution; Remote similarity

Indexed keywords

BIOLOGY; GENOMICS; MOLECULAR EVOLUTION; MOLECULAR GENETICS; PROTEIN DATABASE; PROTEIN TERTIARY STRUCTURE; SEQUENCE HOMOLOGY;

COMPUTATIONAL BIOLOGY; DATABASES, PROTEIN; EVOLUTION, MOLECULAR; GENOMICS; MOLECULAR SEQUENCE ANNOTATION; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84938080548     PISSN: None     EISSN: 17456150     Source Type: Journal    
DOI: 10.1186/s13062-015-0069-2     Document Type: Article

References (74)

1. Eisenhaber F. A decade after the first full human genome sequencing: when will we understand our own genome? J Bioinform Comput Biol.10(5):1271001. doi: 10.1142/S0219720012710011
2. Jaroszewski L, Li Z, Krishna SS, Bakolitsa C, Wooley J, Deacon AM, et al. Exploration of uncharted regions of the protein universe. PLoS Biol. 2009;7(9), e1000205. doi: 10.1371/journal.pbio.1000205 .
3. Sonnhammer EL, Eddy SR, Durbin R. Pfam: a comprehensive database of protein domain families based on seed alignments. Proteins. 1997;28(3):405-20.
4. Goodacre NF, Gerloff DL, Uetz P. Protein domains of unknown function are essential in bacteria. mBio. 2013;5(1):e00744-13. doi: 10.1128/mBio.00744-13 .
5. Finn RD, Mistry J, Schuster-Bockler B, Griffiths-Jones S, Hollich V, Lassmann T, et al. Pfam: clans, web tools and services. Nucleic Acids Res. 2006;34(Database issue):D247-51. doi: 10.1093/nar/gkj149 .
6. Gherardini PF, Helmer-Citterich M. Structure-based function prediction: approaches and applications. Brief Funct Genomic Proteomic. 2008;7(4):291-302. doi: 10.1093/bfgp/eln030 .
7. Kristensen DM, Ward RM, Lisewski AM, Erdin S, Chen BY, Fofanov VY, et al. Prediction of enzyme function based on 3D templates of evolutionarily important amino acids. BMC Bioinformatics. 2008;9:17. doi: 10.1186/1471-2105-9-17 .
8. Thornton JM, Todd AE, Milburn D, Borkakoti N, Orengo CA. From structure to function: approaches and limitations. Nat Struct Biol. 2000;7(Suppl):991-4. doi: 10.1038/80784 .
9. Sadowski MI, Jones DT. The sequence-structure relationship and protein function prediction. Curr Opin Struct Biol. 2009;19(3):357-62. doi: 10.1016/j.sbi.2009.03.008 .
10. Whisstock JC, Lesk AM. Prediction of protein function from protein sequence and structure. Q Rev Biophys. 2003;36(3):307-40.
11. Watson JD, Laskowski RA, Thornton JM. Predicting protein function from sequence and structural data. Curr Opin Struct Biol. 2005;15(3):275-84. doi: 10.1016/j.sbi.2005.04.003 .
12. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997;25(17):3389-402.
13. Sandhya S, Chakrabarti S, Abhinandan KR, Sowdhamini R, Srinivasan N. Assessment of a rigorous transitive profile based search method to detect remotely similar proteins. J Biomol Struct Dyn. 2005;23(3):283-98.
14. Li W, Pio F, Pawlowski K, Godzik A. Saturated BLAST: an automated multiple intermediate sequence search used to detect distant homology. Bioinformatics. 2000;16(12):1105-10.
15. Margelevicius M, Venclovas C. PSI-BLAST-ISS: an intermediate sequence search tool for estimation of the position-specific alignment reliability. BMC Bioinformatics. 2005;6:185. doi: 10.1186/1471-2105-6-185 .
16. Edgar RC, Sjolander K. COACH: profile-profile alignment of protein families using hidden Markov models. Bioinformatics. 2004;20(8):1309-18. doi: 10.1093/bioinformatics/bth091 .
17. Madera M. Profile Comparer: a program for scoring and aligning profile hidden Markov models. Bioinformatics. 2008;24(22):2630-1. doi: 10.1093/bioinformatics/btn504 .
18. Sadreyev RI, Baker D, Grishin NV. Profile-profile comparisons by COMPASS predict intricate homologies between protein families. Protein Sci. 2003;12(10):2262-72.
19. Soding J. Protein homology detection by HMM-HMM comparison. Bioinformatics. 2005;21(7):951-60. doi: 10.1093/bioinformatics/bti125 .
20. Wang Y, Sadreyev RI, Grishin NV. PROCAIN: protein profile comparison with assisting information. Nucleic Acids Res. 2009;37(11):3522-30. doi: 10.1093/nar/gkp212 .
21. Yona G, Levitt M. Within the twilight zone: a sensitive profile-profile comparison tool based on information theory. J Mol Biol. 2002;315(5):1257-75. doi: 10.1006/jmbi.2001.5293 .
22. Mudgal R, Sowdhamini R, Chandra N, Srinivasan N, Sandhya S. Filling-in void and sparse regions in protein sequence space by protein-like artificial sequences enables remarkable enhancement in remote homology detection capability. J Mol Biol. 2014;426:962-79.
23. Mudgal R, Sandhya S, Kumar G, Sowdhamini R, Chandra NR, Srinivasan N. NrichD database: sequence databases enriched with computationally designed protein-like sequences aid in remote homology detection. Nucleic Acids Res. 2014. doi: 10.1093/nar/gku888 .
24. Pandit SB, Gosar D, Abhiman S, Sujatha S, Dixit SS, Mhatre NS, et al. SUPFAM-a database of potential protein superfamily relationships derived by comparing sequence-based and structure-based families: implications for structural genomics and function annotation in genomes. Nucleic Acids Res. 2002;30(1):289-93.
25. Gough J, Chothia C. SUPERFAMILY: HMMs representing all proteins of known structure. SCOP sequence searches, alignments and genome assignments. Nucleic Acids Res. 2002;30(1):268-72.
26. Lobley A, Sadowski MI, Jones DT. pGenTHREADER and pDomTHREADER: new methods for improved protein fold recognition and superfamily discrimination. Bioinformatics. 2009;25(14):1761-7. doi: 10.1093/bioinformatics/btp302 .
27. Murzin AG, Brenner SE, Hubbard T, Chothia C. SCOP: a structural classification of proteins database for the investigation of sequences and structures. J Mol Biol. 1995;247(4):536-40. doi: 10.1006/jmbi.1995.0159 .
28. Eddy SR. Profile hidden Markov models. Bioinformatics. 1998;14(9):755-63.
29. Krishnadev O, Srinivasan N. AlignHUSH: alignment of HMMs using structure and hydrophobicity information. BMC Bioinformatics. 2011;12:275. doi: 10.1186/1471-2105-12-275 .
30. Bateman A, Coggill P, Finn RD. DUFs: families in search of function. Acta Crystallogr Sect F: Struct Biol Cryst Commun. 2010;66(Pt 10):1148-52. doi: 10.1107/S1744309110001685 .
31. Cong Q, Grishin NV. MESSA: MEta-Server for protein Sequence Analysis. BMC Biol.10:82. doi: 10.1186/1741-7007-10-82
32. Marchler-Bauer A, Bryant SH. CD-Search: protein domain annotations on the fly. Nucleic Acids Res. 2004;32(Web Server issue):W327-31. doi: 10.1093/nar/gkh454 .
33. Stenner-Liewen F, Liewen H, Zapata JM, Pawlowski K, Godzik A, Reed JC. CADD, a Chlamydia protein that interacts with death receptors. J Biol Chem. 2002;277(12):9633-6. doi: 10.1074/jbc.C100693200 .
34. Schwarzenbacher R, Stenner-Liewen F, Liewen H, Robinson H, Yuan H, Bossy-Wetzel E, et al. Structure of the Chlamydia protein CADD reveals a redox enzyme that modulates host cell apoptosis. J Biol Chem. 2004;279(28):29320-4. doi: 10.1074/jbc.M401268200 .
35. Rajan SS, Yang X, Shuvalova L, Collart F, Anderson WF. YfiT from Bacillus subtilis is a probable metal-dependent hydrolase with an unusual four-helix bundle topology. Biochemistry. 2004;43(49):15472-9. doi: 10.1021/bi048665r .
36. Rakshambikai R, Gnanavel M, Srinivasan N. Hybrid and rogue kinases encoded in the genomes of model eukaryotes. PLoS One.9(9):e107956. doi: 10.1371/journal.pone.0107956 .
37. Ho MC, Menetret JF, Tsuruta H, Allen KN. The origin of the electrostatic perturbation in acetoacetate decarboxylase. Nature. 2009;459(7245):393-7. doi: 10.1038/nature07938 .
38. Highbarger LA, Gerlt JA, Kenyon GL. Mechanism of the reaction catalyzed by acetoacetate decarboxylase. Importance of lysine 116 in determining the pKa of active-site lysine 115. Biochemistry. 1996;35(1):41-6. doi: 10.1021/bi9518306 .
39. Masuda K, Matsuyama S, Tokuda H. Elucidation of the function of lipoprotein-sorting signals that determine membrane localization. Proc Natl Acad Sci U S A. 2002;99(11):7390-5. doi: 10.1073/pnas.112085599 .
40. Golinelli MP, Chatelet C, Duin EC, Johnson MK, Meyer J. Extensive ligand rearrangements around the [2Fe-2S] cluster of Clostridium pasteurianum ferredoxin. Biochemistry. 1998;37(29):10429-37. doi: 10.1021/bi9806394 .
41. Meyer J, Fujinaga J, Gaillard J, Lutz M. Mutated forms of the [2Fe-2S] ferredoxin from Clostridium pasteurianum with noncysteinyl ligands to the iron-sulfur cluster. Biochemistry. 1994;33(46):13642-50.
42. Atkinson HJ, Babbitt PC. An atlas of the thioredoxin fold class reveals the complexity of function-enabling adaptations. PLoS Comput Biol. 2009;5(10), e1000541. doi: 10.1371/journal.pcbi.1000541 .
43. Hegyi H, Gerstein M. The relationship between protein structure and function: a comprehensive survey with application to the yeast genome. J Mol Biol. 1999;288(1):147-64. doi: 10.1006/jmbi.1999.2661 .
44. Nagano N, Orengo CA, Thornton JM. One fold with many functions: the evolutionary relationships between TIM barrel families based on their sequences, structures and functions. J Mol Biol. 2002;321(5):741-65.
45. Babbitt PC, Gerlt JA. Understanding enzyme superfamilies. Chemistry As the fundamental determinant in the evolution of new catalytic activities. The Journal of biological chemistry. 1997;272(49):30591-4.
46. Bartlett GJ, Borkakoti N, Thornton JM. Catalysing new reactions during evolution: economy of residues and mechanism. J Mol Biol. 2003;331(4):829-60.
47. Gerlt JA, Babbitt PC. Divergent evolution of enzymatic function: mechanistically diverse superfamilies and functionally distinct suprafamilies. Annu Rev Biochem. 2001;70:209-46. doi: 10.1146/annurev.biochem.70.1.209 .
48. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B. The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res. 2009;37(Database issue):D233-8. doi: 10.1093/nar/gkn663 .
49. Omelchenko MV, Galperin MY, Wolf YI, Koonin EV. Non-homologous isofunctional enzymes: a systematic analysis of alternative solutions in enzyme evolution. Biol Direct. 2010;5:31. doi: 10.1186/1745-6150-5-31 .
50. Buttigieg PL, Hankeln W, Kostadinov I, Kottmann R, Yilmaz P, Duhaime MB, et al. Ecogenomic perspectives on domains of unknown function: correlation-based exploration of marine metagenomes. PLoS One. 2013;8(3), e50869. doi: 10.1371/journal.pone.0050869 .
51. Ponting CP. Issues in predicting protein function from sequence. Brief Bioinform. 2001;2(1):19-29.
52. Punta M, Ofran Y. The rough guide to in silico function prediction, or how to use sequence and structure information to predict protein function. PLoS Comput Biol. 2008;4(10), e1000160. doi: 10.1371/journal.pcbi.1000160 .
53. Prakash A, Yogeeshwari S, Sircar S, Agrawal S. Protein domain of unknown function 3233 is a translocation domain of autotransporter secretory mechanism in gamma proteobacteria. PLoS One. 2011;6(11), e25570. doi: 10.1371/journal.pone.0025570 .
54. Fang H, Gough J. DcGO: database of domain-centric ontologies on functions, phenotypes, diseases and more. Nucleic Acids Res. 2013;41(Database issue):D536-44. doi: 10.1093/nar/gks1080 .
55. Cheng H, Schaeffer RD, Liao Y, Kinch LN, Pei J, Shi S, et al. ECOD: An Evolutionary Classification of Protein Domains. PLoS Comput Biol. 2014;10(12), e1003926. doi: 10.1371/journal.pcbi.1003926 .
56. Grishin NV. Fold change in evolution of protein structures. J Struct Biol. 2001;134(2-3):167-85. doi: 10.1006/jsbi.2001.4335 .
57. Krishna SS, Grishin NV. Structural drift: a possible path to protein fold change. Bioinformatics. 2005;21(8):1308-10. doi: 10.1093/bioinformatics/bti227 .
58. Wong WC, Maurer-Stroh S, Eisenhaber B, Eisenhaber F. On the necessity of dissecting sequence similarity scores into segment-specific contributions for inferring protein homology, function prediction and annotation. BMC Bioinformatics. 2014;15:166. doi: 10.1186/1471-2105-15-166 .
59. Wong WC, Maurer-Stroh S, Eisenhaber F. More than 1,001 problems with protein domain databases: transmembrane regions, signal peptides and the issue of sequence homology. PLoS Comput Biol. 2010;6(7), e1000867. doi: 10.1371/journal.pcbi.1000867 .
60. Wong WC, Maurer-Stroh S, Eisenhaber F. Not all transmembrane helices are born equal: Towards the extension of the sequence homology concept to membrane proteins. Biol Direct. 2011;6:57. doi: 10.1186/1745-6150-6-57 .
61. Layer G, Moser J, Heinz DW, Jahn D, Schubert WD. Crystal structure of coproporphyrinogen III oxidase reveals cofactor geometry of Radical SAM enzymes. EMBO J. 2003;22(23):6214-24. doi: 10.1093/emboj/cdg598 .
62. Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, et al. Pfam: the protein families database. Nucleic Acids Res. 2014;42(Database issue):D222-30. doi: 10.1093/nar/gkt1223 .
63. Ginalski K, von Grotthuss M, Grishin NV, Rychlewski L. Detecting distant homology with Meta-BASIC. Nucleic Acids Res. 2004;32(Web Server issue):W576-81. doi: 10.1093/nar/gkh370 .
64. Goonesekere NC, Shipely K, O'Connor K. The challenge of annotating protein sequences: The tale of eight domains of unknown function in Pfam. Comput Biol Chem. 2010;34(3):210-4. doi: 10.1016/j.compbiolchem.2010.04.001 .
65. Wilson D, Madera M, Vogel C, Chothia C, Gough J. The SUPERFAMILY database in 2007: families and functions. Nucleic Acids Res. 2007;35(Database issue):D308-13. doi: 10.1093/nar/gkl910 .
66. 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(Database issue):D304-9. doi: 10.1093/nar/gkt1240 .
67. Soding J, Biegert A, Lupas AN. The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res. 2005;33(Web Server issue):W244-8. doi: 10.1093/nar/gki408 .
68. Magrane M, Consortium U. UniProt Knowledgebase: a hub of integrated protein data. Database (Oxford).2011:bar009. doi: 10.1093/database/bar009 .
69. Federhen S. The NCBI Taxonomy database. Nucleic Acids Res.40(Database issue):D136-43. doi: 10.1093/nar/gkr1178
70. Bernstein FC, Koetzle TF, Williams GJ, Meyer Jr EF, Brice MD, Rodgers JR, et al. The Protein Data Bank: a computer-based archival file for macromolecular structures. J Mol Biol. 1977;112(3):535-42.
71. Pei J, Kim BH, Grishin NV. PROMALS3D: a tool for multiple protein sequence and structure alignments. Nucleic Acids Res. 2008;36(7):2295-300. doi: 10.1093/nar/gkn072 .
72. Eswar N, Webb B, Marti-Renom MA, Madhusudhan MS, Eramian D, Shen MY et al. Comparative protein structure modeling using Modeller. Curr Protoc Bioinformatics. 2006;Chapter 5:Unit 5 6. doi: 10.1002/0471250953.bi0506s15.
73. McGuffin LJ, Bryson K, Jones DT. The PSIPRED protein structure prediction server. Bioinformatics. 2000;16(4):404-5.
74. Leaver-Fay A, Tyka M, Lewis SM, Lange OF, Thompson J, Jacak R, et al. ROSETTA3: an object-oriented software suite for the simulation and design of macromolecules. Methods Enzymol. 2011;487:545-74. doi: 10.1016/B978-0-12-381270-4.00019-6 .