PRIDB: a Protein-RNA Interface Database.
ABSTRACT The Protein-RNA Interface Database (PRIDB) is a comprehensive database of protein-RNA interfaces extracted from complexes in the Protein Data Bank (PDB). It is designed to facilitate detailed analyses of individual protein-RNA complexes and their interfaces, in addition to automated generation of user-defined data sets of protein-RNA interfaces for statistical analyses and machine learning applications. For any chosen PDB complex or list of complexes, PRIDB rapidly displays interfacial amino acids and ribonucleotides within the primary sequences of the interacting protein and RNA chains. PRIDB also identifies ProSite motifs in protein chains and FR3D motifs in RNA chains and provides links to these external databases, as well as to structure files in the PDB. An integrated JMol applet is provided for visualization of interacting atoms and residues in the context of the 3D complex structures. The current version of PRIDB contains structural information regarding 926 protein-RNA complexes available in the PDB (as of 10 October 2010). Atomic- and residue-level contact information for the entire data set can be downloaded in a simple machine-readable format. Also, several non-redundant benchmark data sets of protein-RNA complexes are provided. The PRIDB database is freely available online at http://bindr.gdcb.iastate.edu/PRIDB.
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ABSTRACT: Understanding the details of protein-RNA interactions is important to reveal the functions of both the RNAs and the proteins. In these interactions the secondary structures of the RNAs play an important role. Because RNA secondary structures in protein-RNA complexes are variable, considering the ensemble of RNA secondary structures is a useful approach. In particular, recent studies have supported the idea that, in the analysis of RNA secondary structures, the base-pairing probabilities of RNAs (i.e., the probabilities of forming a base-pair in the ensemble of RNA secondary structures) provide richer and more robust information about the structures than a single RNA secondary structure, for example, the minimum free energy (MFE) structure or a snapshot of structures in the PDB. However, there has been no investigation of the base-paring probabilities in protein-RNA interactions. In this study, we analyzed base-pairing probabilities of RNA molecules involved in known protein-RNA complexes in the PDB. Our analysis suggests that, in the tertiary structures, the base-pairing probabilities (which are computed using only sequence information) for unpaired nucleotides with intermolecular hydrogen bonds to amino acids were significantly lower than those for unpaired nucleotides without hydrogen bonds. On the other hand, no difference was found between the base-pairing probabilities for paired nucleotides with and without intermolecular hydrogen bonds. Those findings were commonly supported by three probabilistic models, which provide the ensemble of RNA secondary structures, including the McCaskill model based on Turner's free energy of secondary structures. email@example.com, firstname.lastname@example.org.Bioinformatics 08/2013; · 5.47 Impact Factor
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ABSTRACT: Non-Watson-Crick pairs like the G·U wobble are frequent in RNA duplexes. Their geometric dissimilarity (nonisostericity) with the Watson-Crick base pairs and among themselves imparts structural variations decisive for biological functions. Through a novel circular representation of base pairs, a simple and general metric scheme for quantification of base-pair nonisostericity, in terms of residual twist and radial difference that can also envisage its mechanistic effect, is proposed. The scheme is exemplified by G·U and U·G wobble pairs, and their predicable local effects on helical twist angle are validated by MD simulations. New insights into a possible rationale for contextual occurrence of G·U and other non-WC pairs, as well as the influence of a G·U pair on other non-Watson-Crick pair neighborhood and RNA-protein interactions are obtained from analysis of crystal structure data. A few instances of RNA-protein interactions along the major groove are documented in addition to the well-recognized interaction of the G·U pair along the minor groove. The nonisostericity-mediated influence of wobble pairs for facilitating helical packing through long-range interactions in ribosomal RNAs is also reviewed.RNA 08/2013; 19(8):1038-53. · 5.09 Impact Factor
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ABSTRACT: In this work, we have analyzed the influence of cation-π interactions to the stability of 59 high resolution protein-RNA complex crystal structures. The total number of Lys and Arg are similar in the dataset as well as the number of their interactions. On the other hand, the aromatic chains of purines are exhibiting more cation-π interactions than pyrimidines. 35% of the total interactions in the dataset are involved in the formation of multiple cation-π interactions. The multiple cation-π interactions have been conserved more than the single interactions. The analysis of the geometry of the cation-π interactions has revealed that the average distance (d) value falls into distinct ranges corresponding to the multiple (4.28Å) and single (5.50Å) cation-π interactions. The G-Arg pair has the strongest interaction energy of -3.68kcalmol(-1) among all the possible pairs of amino acids and bases. Further, we found that the cation-π interactions due to five-membered rings of A and G are stronger than that with the atoms in six-membered rings. 8.7% stabilizing residues are involved in building cation-π interactions with the nucleic bases. There are three types of structural motifs significantly over-represented in protein-RNA interfaces: beta-turn-ir, niche-4r and st-staple. Tetraloops and kink-turns are the most abundant RNA motifs in protein-RNA interfaces. Amino acids deployed in the protein-RNA interfaces are deposited in helices, sheets and coils. Arg and Lys, involved in cation-π interactions, prefer to be in the solvent exposed surface. The results from this study might be used for structure-based prediction and as scaffolds for future protein-RNA complex design.Computational biology and chemistry 08/2013; 47C:105-112. · 1.37 Impact Factor
PRIDB: a protein–RNA interface database
Benjamin A. Lewis1,2,*, Rasna R. Walia1,3, Michael Terribilini4, Jeff Ferguson5,
Charles Zheng5, Vasant Honavar1,3and Drena Dobbs1,2
1Bioinformatics and Computational Biology Program, Iowa State University,2Department of Genetics,
Development and Cell Biology, Iowa State University,3Department of Computer Science, Iowa State University,
Ames, IA 50011,4Department of Biology, Elon University, Elon, NC 27244 and5Computational Systems Biology
Summer Institute, Iowa State University, Ames, IA 50011, USA
Received August 15, 2010; Revised October 15, 2010; Accepted October 18, 2010
The Protein–RNA Interface Database (PRIDB) is a
comprehensive database of protein–RNA interfaces
extracted from complexes in the Protein Data Bank
(PDB). It is designed to facilitate detailed analyses
of individual protein–RNA complexes and their
interfaces, in addition to automated generation
of user-defined data sets of protein–RNA interfaces
applications. For any chosen PDB complex or list
of complexes, PRIDB rapidly displays interfacial
amino acids and ribonucleotides within the primary
sequences of the interacting protein and RNA
chains. PRIDB also identifies ProSite motifs in
protein chains and FR3D motifs in RNA chains
and provides links to these external databases, as
well as to structure files in the PDB. An integrated
JMol applet is provided for visualization of interact-
ing atoms and residues in the context of the 3D
complex structures. The current version of PRIDB
protein–RNA complexes available in the PDB (as of
10 October 2010). Atomic- and residue-level contact
information for the entire data set can be down-
loaded in a simple machine-readable format. Also,
several non-redundant benchmark data sets of
protein–RNA complexes are provided. The PRIDB
database is freely available online at http://bindr
Protein–RNA interactions play critical roles in myriad
and diverse biological processes, including many recently
discovered regulatory functions, in addition to well-studied
roles in protein synthesis, DNA replication, regulation of
gene expression and defense against pathogens (1–9).
Despite their importance, structures of protein–RNA
complexes have proven difficult to obtain using exper-
imental structure determination methods; such structures
(PDB) (10). For this reason, several computational
methods for predicting the interfaces in protein–RNA
complexes have been developed (11–21). Virtually all
such methods require data in the form of information
about structurally characterized protein–RNA complexes
and their interfaces.
PRIDB is a repository of protein–RNA interface
information derived from structures in the PDB. PRIDB
is designed to facilitate detailed analyses of individual
protein–RNA complexes of interest and rapid identifi-
cation of interfacial atoms and residues in both the
protein and RNA chains of a chosen complex or user-
defined set of complexes. In addition, PRIDB can be used
to generate data sets of protein–RNA interfaces for
machine learning applications, such as the generation of
classifiers for predicting interfaces in protein–RNA
complexes for which high-resolution structures are not
To our knowledge, only one other up-to-date and compre-
hensive online repository of protein–RNA interfaces is
currently available: Biological Interaction Database for
Protein-Nucleic Acid (BIPA) (22). BIPA provides a list of
protein–RNA (and protein–DNA) complexes from the
PDB and displays RNA-binding residues within the
linear primary sequence of a chosen protein, or within a
multiple sequence alignment of related RNA-binding
atomic- and residue-level interfacial information for both
the RNA and protein chains of complexes, providing
previously published reduced-redundancy data sets and
allowing users to make advanced queries and compile
custom data sets. Other collections of protein–RNA
*To whom correspondence should be addressed. Tel: +1 515 294 4991; Fax: +1 515 294 6790; Email: email@example.com
The authors wish it to be known that, in their opinion, the first two authors should be regarded as joint First Authors.
Published online 11 November 2010Nucleic Acids Research, 2011, Vol. 39, Database issueD277–D282
? The Author(s) 2010. Published by Oxford University Press.
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/
by-nc/2.5), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
complexes and related resources include NDB (http://
ndbserver.rutgers.edu/) (23), PRID (http://www-bioc.rice
.edu/?shamoo/prid.html) (24), RsiteDB (http://bioinfo3d
.cs.tau.ac.il/RsiteDB/) (25), w3DNA (http://w3dna.rutgers
.edu/) (26), NPIDB (http://monkey.belozersky.msu.ru/
NPIDB) (27), ProNIT (http://gibk26.bse.kyutech.ac.jp/
jouhou/pronit/pronit.html) (28) and the RNP Databases
http://rnp.uthct.edu/index.html/). Several excellent data-
bases of protein–DNA interfaces are also available,
including PDIdb (http://melolab.org/pdidb/) (29) and
Data extraction, interface definition and motif
Atomic coordinate information for all 926 protein–RNA
complexes in the Protein Data Bank (PDB) on 10 October
2010 was extracted using the REST API advanced
search interface. To generate this comprehensive data set
(rRB926), no filters based on sequence redundancy,
structure resolution or other criteria were applied (see
‘Non-redundant Benchmark data sets’ below). The
complex structures in rRB926 were then scanned to
identify interacting amino acids and ribonucleotides using
two different definitions: (i) a simple distance-based
definition in which a given amino acid residue (AA) in a
protein chain is defined as interacting with a ribonucleotide
(rNT) in an RNA chain if any atom in AA is within a 5-A˚
radius of any atom in rNT; and (ii) a rule-based definition
based on that of Allers and Shamoo (30), in which
interactions are classified as van der Waals, hydrogen-
involving specific AAs and rNTs. All such interacting
AAs and rNTs are defined as ‘interface’ residues.
ProSite patterns and profiles (31) appearing in any of
the protein sequences in the database were retrieved using
the ScanProsite REST service (32). RNA structural motifs
were identified in RNA sequences using FR3D’s (33) pure
symbolic search function; specific motif definitions used
for these scans are available in the Tutorial and FAQs
section of the PRIDB online server.
Non-redundant benchmark data sets
Because PRIDB is intended to be a comprehensive
collection of protein–RNA complexes from the PDB, the
rRB926 data set was not filtered on the basis of
redundancy, structure determination method, resolution
or protein/RNA chain length. While it is possible to
filter with such criteria using PRIDB’s advanced search
function, several pre-calculated benchmark data sets,
which have been filtered to limit redundancy and to
exclude low-resolution structures, are also provided for
the user’s convenience. These include two previously
published data sets, RB109 (17,34) and RB147 (35), as
well as a larger, more recently extracted data set
(RB199) (B. Lewis, submitted for publication). Complete
lists of the PDB IDs for protein–RNA complexes in these
data sets, in addition to the pre-calculated interface
residue statistics, can be readily accessed from the
‘Datasets’ section of the PRIDB homepage.
Implementation and availability
PRIDB runs on the Apache 2.2 web server, using MySQL
14.14 as a database backend with AJAX and PHP 5 for
user interface functions. Functions not requiring use of
the database (e.g. calculating interface residues for a user-
submitted complex) are implemented using standalone
Perl 5 scripts and the BioPerl module (36). All PRIDB
code is available on request under the Creative Commons
Attribution Non-Commercial License. All data currently
in PRIDB was obtained from databases or programs
which impose no restrictions on academic use.
PRIDB summary statistics
As summarized in Table 1, the current version of PRIDB
contains structural information for a total of 926 protein–
RNA complexes available in the PDB as of 10 October
2010. These structures contain 9689 total protein chains,
among which there are only 1174 unique sequences. While
this would seem to indicate that most sequences in the
database are repeated several times, this is not the case;
395 of the 1174 (34%) sequences appear only once, and
899 (77%) appear less than eight times (the ‘expected’
average redundancy). This disparity is due to the large
proportion of ribosomal structures in the PDB (and, by
extension, in PRIDB); 9 of the top 10 most abundant
sequences, each present in more than 70 structures, are
repeated more than 100 times, is that of the TRP-
responsive attenuation protein, a protein for which
numerous multimeric structures have been solved.
As shown in Table 2, PRIDB currently contains
1475774 amino acid residues. Based on a 5A˚
cutoff definition for interfacial residues, 397216 of these
residues interact with RNA; of 851853 ribonucleotide
On average, 38% of the amino acids in the RNA-binding
Table 1. PRIDB contents: complexes and chains
aTotal number in PRIDB includes redundant complexes, RNA and
protein chains (i.e. chains with identical sequences).
Table 2. PRIDB summary statistics
D278 Nucleic AcidsResearch, 2011, Vol.39, Database issue
proteins directly interact with RNA, and 28% of the
ribonucleotides in the bound RNAs directly interact with
protein. As before, these averages are skewed by the
prevalence of ribosome structures; ribosomal proteins
account for ?90% of interacting amino acid residues and
?60% of interacting nucleotides.
PRIDB provides a ‘Tutorial and FAQs’ section with
detailed instructions on using PRIDB’s web interface; a
list and brief descriptions of key capabilities of PRIDB are
provided here. Using the ‘Basic Search’ function, users can
retrieve information about protein–RNA complexes using
their PDB ID or a keyword. Using the ‘Advanced Search’
function, users can filter results by specifying:
. the experimental method used to determine the complex
structure (e.g. X-ray diffraction, nuclear magnetic
. a resolutionrange or
microscopy or fiber diffraction);
. the minimum or maximum length of protein or RNA
chains within the complex;
. an amino acid or nucleotide subsequence found within
the sequence of at least one of the protein or RNA
chains in the complex; and
Figure 1. Sample PRIDB output. Amino acid residues and ribonucleotides highlighted in yellow are located in the protein–RNA interface; residues
in red font are part of a ProSite or FR3D motif.
Nucleic Acids Research, 2011,Vol.39, Database issue D279
. a motif (as defined by ProSite for protein chains or
FR3D for RNA chains) found within at least one
chain in the complex.
The ‘Advanced Search’ function also allows users to
either specify a different distance cutoff for the distance-
based interaction definition or choose the alternative rule-
As shown in Figure 1, when viewing search results,
. a summary of and basic information (name, resolution
and structure determination method) about each
complex, as well as a link to that complex’s PDB entry;
. a linear display of the amino acid and nucleotide
residues in each chain of each complex, with residues
in the protein–RNA interface highlighted;
. a display of residues (in red font) that are part of a
protein or RNA motif, with information about that
motif (and a link back to its source) provided on
. a JMol applet for 3D visualization of each complex,
with interacting amino acid and nucleotide residues
colored (Figure 2A); and
. a link to a dynamically-generated file containing
atomic-level interface information for each result in a
machine readable format (Figure 2B).
In addition to providing machine-readable results
files for all searches, pre-computed results files for the
non-redundant RB109, RB147 and RB199 data sets
described above have been made available. These files,
along with the complete PRIDB database (rRB926), can
be downloaded from the ‘Datasets’ section of the website.
Users can also generate a machine-readable list of
interface residues for any arbitrary collection of complexes
by inputting a list of PDB IDs. Results files contain a
single line for each pair of interacting atoms listing
residue number and atom name) and the distance
Users may also calculate interface residues for protein–
RNA complexes that are not in PDB using PRIDB by
submitting a structure file in PDB format. A results file
containing interface residues (as calculated using PRIDB’s
5A˚cutoff) is returned via e-mail.
Figure 2. (A) PRIDB provides a JMol applet for visualizing and manipulating interfaces within 3-D structures. (B) PRIDB output can be
downloaded as a CSV file.
D280 Nucleic AcidsResearch, 2011, Vol.39, Database issue
CONCLUSIONS AND FUTURE DIRECTIONS
PRIDB provides researchers with atomic and residue-level
information about structures of protein–RNA complexes
and their interfaces, facilitating analyses of protein–RNA
information and by providing structural information
both interactively onscreen and in a machine-readable
format. It allows users to rapidly identify and visualize
interfaces in protein–RNA complexes on a residue-by-
residue basis and displays identified ProSite or FR3D
motifs along with the amino acid or ribonucleotide
sequences. PRIDB can be used to generate custom data
sets of protein–RNA interfaces for statistical analyses
and machine learning applications. The PRIDB server
also provides pre-calculated benchmark data sets of
protein–RNA complexes for evaluating the performance
of interface prediction methods. PRIDB will be updated
regularly as new structures are released through PDB, and
is intended to be a stable resource for researchers in the
field of protein–RNA interactions.
Future versions of PRIDB will include additional
protein and RNA motifs from other sources, such as
PRINTS (37), PIRSF (38) and other InterPro (39)
member databases. In addition, the current JMol 3D
structures, allowing for more facile manipulation and
examination of interfaces in complexes not currently in
The authors thank members of our research groups for
helpful discussions and especially Usha Muppirala for
critical comments on the PRIDB server and manuscript.
National Institutes of Health (GM066387 to V.H. and
[IGERT0504304 (to D.D.); GK120947929 (to B.A.L.);
NIBIB-NSF0608769 (to V.H., J.F. and C.Z.)]; Iowa
Computational Intelligence, Learning and Discovery (to
V.H.). Funding for open access charge: Center for
Computational Intelligence, Learning and Discovery.
Conflict of interest statement. None declared.
1. Fabian,M.R., Sonenberg,N. and Filipowicz,W. (2010) Regulation
of mRNA translation and stability by microRNAs. Annu. Rev.
Biochem., 79, 351–379.
2. Hogan,D.J., Riordan,D.P., Gerber,A.P., Herschlag,D. and
Brown,P.O. (2008) Diverse RNA-binding proteins interact with
functionally related sets of RNAs, suggesting an extensive
regulatory system. PLoS Biol., 6, e255.
3. Licatalosi,D.D. and Darnell,R.B. (2010) RNA processing and its
regulation: global insights into biological networks. Nat. Rev.
Genet., 11, 75–87.
4. Lorkovic,Z.J. (2009) Role of plant RNA-binding proteins in
development, stress response and genome organization. Trends
Plant Sci., 14, 229–236.
5. Lukong,K.E., Chang,K.W., Khandjian,E.W. and Richard,S.
(2008) RNA-binding proteins in human genetic disease. Trends
Genet., 24, 416–425.
6. Lunde,B.M., Moore,C. and Varani,G. (2007) RNA-binding
proteins: modular design for efficient function. Nat. Rev. Mol.
Cell Biol., 8, 479–490.
7. Mansfield,K.D. and Keene,J.D. (2009) The ribonome: a dominant
force in co-ordinating gene expression. Biol. Cell, 101, 169–181.
8. Mittal,N., Roy,N., Babu,M.M. and Janga,S.C. (2009) Dissecting
the expression dynamics of RNA-binding proteins in
posttranscriptional regulatory networks. Proc. Natl Acad. Sci.
USA, 106, 20300–20305.
9. Mohammad,M.M., Donti,T.R., Sebastian Yakisich,J., Smith,A.G.
and Kapler,G.M. (2007) Tetrahymena ORC contains a ribosomal
RNA fragment that participates in rDNA origin recognition.
EMBO J., 26, 5048–5060.
10. Berman,H.M., Westbrook,J., Feng,Z., Gilliland,G., Bhat,T.N.,
Weissig,H., Shindyalov,I.N. and Bourne,P.E. (2000) The protein
data bank. Nucleic Acids Res., 28, 235–242.
11. Liu,Z.P., Wu,L.Y., Wang,Y., Zhang,X.S. and Chen,L. (2010)
Prediction of protein-RNA binding sites by a random forest
method with combined features. Bioinformatics, 26, 1616–1622.
12. Murakami,Y., Spriggs,R.V., Nakamura,H. and Jones,S. (2010)
PiRaNhA: a server for the computational prediction of
RNA-binding residues in protein sequences. Nucleic Acids Res.,
13. Perez-Cano,L. and Fernandez-Recio,J. (2010) Optimal
protein-RNA area, OPRA: a propensity-based method to identify
RNA-binding sites on proteins. Proteins, 78, 25–35.
14. Maetschke,S.R. and Yuan,Z. (2009) Exploiting structural and
topological information to improve prediction of RNA-protein
binding sites. BMC Bioinformatics, 10, 341.
15. Shazman,S. and Mandel-Gutfreund,Y. (2008) Classifying
RNA-binding proteins based on electrostatic properties.
PLoS Comput. Biol., 4, e1000146.
16. Wang,L., Huang,C., Yang,M.Q. and Yang,J.Y. (2010) BindN+
for accurate prediction of DNA and RNA-binding residues from
protein sequence features. BMC Syst Biol, 4(Suppl. 1), S3.
17. Terribilini,M., Lee,J.H., Yan,C., Jernigan,R.L., Honavar,V. and
Dobbs,D. (2006) Prediction of RNA binding sites in proteins
from amino acid sequence. RNA, 12, 1450–1462.
18. Wang,L. and Brown,S.J. (2006) Prediction of RNA-binding
residues in protein sequences using support vector machines.
Conf. Proc. IEEE Eng. Med. Biol. Soc., 1, 5830–5833.
19. Towfic,F., Caragea,C., Gemperline,D.C., Dobbs,D. and
Honavar,V. (2010) Struct-NB: predicting protein-RNA binding
sites using structural features. Int. J. Data Min. Bioinform., 4,
20. Kumar,M., Gromiha,M.M. and Raghava,G.P. (2010) SVM based
prediction of RNA-binding proteins using binding residues and
evolutionary information. J. Mol. Recognit., doi:10.1002/jmr.1061.
21. Wang,C.C., Fang,Y., Xiao,J. and Li,M. (2010) Identification of
RNA-binding sites in proteins by integrating various sequence
information. Amino Acids, doi:10.1007/s00726-010-0639-7.
22. Lee,S. and Blundell,T.L. (2009) BIPA: a database for
protein-nucleic acid interaction in 3D structures. Bioinformatics,
23. Berman,H.M., Olson,W.K., Beveridge,D.L., Westbrook,J.,
Gelbin,A., Demeny,T., Hsieh,S.H., Srinivasan,A.R. and
Schneider,B. (1992) The nucleic acid database. A comprehensive
relational database of three-dimensional structures of nucleic
acids. Biophys. J., 63, 751–759.
24. Morozova,N., Allers,J., Myers,J. and Shamoo,Y. (2006)
Protein-RNA interactions: exploring binding patterns with a
three-dimensional superposition analysis of high resolution
structures. Bioinformatics, 22, 2746–2752.
25. Shulman-Peleg,A., Nussinov,R. and Wolfson,H.J. (2009) RsiteDB:
a database of protein binding pockets that interact with RNA
nucleotide bases. Nucleic Acids Res., 37, D369–D373.
26. Zheng,G., Lu,X.J. and Olson,W.K. (2009) Web 3DNA–a web
server for the analysis, reconstruction, and visualization of
Nucleic Acids Research, 2011,Vol.39, Database issueD281
three-dimensional nucleic-acid structures. Nucleic Acids Res., 37,
27. Spirin,S., Titov,M., Karyagina,A. and Alexeevski,A. (2007)
NPIDB: a database of nucleic acids-protein interactions.
Bioinformatics, 23, 3247–3248.
28. Kumar,M.D., Bava,K.A., Gromiha,M.M., Prabakaran,P.,
Kitajima,K., Uedaira,H. and Sarai,A. (2006) ProTherm and
ProNIT: thermodynamic databases for proteins and protein-
nucleic acid interactions. Nucleic Acids Res., 34, D204–D206.
29. Norambuena,T. and Melo,F. (2010) The Protein-DNA Interface
database. BMC Bioinformatics, 11, 262.
30. Allers,J. and Shamoo,Y. (2001) Structure-based analysis of
protein-RNA interactions using the program ENTANGLE.
J. Mol. Biol., 311, 75–86.
31. Sigrist,C.J., Cerutti,L., de Castro,E., Langendijk-Genevaux,P.S.,
Bulliard,V., Bairoch,A. and Hulo,N. (2010) PROSITE, a protein
domain database for functional characterization and annotation.
Nucleic Acids Res., 38, D161–D166.
32. de Castro,E., Sigrist,C.J., Gattiker,A., Bulliard,V., Langendijk-
Genevaux,P.S., Gasteiger,E., Bairoch,A. and Hulo,N. (2006)
ScanProsite: detection of PROSITE signature matches and
ProRule-associated functional and structural residues in proteins.
Nucleic Acids Res., 34, W362–W365.
33. Sarver,M., Zirbel,C.L., Stombaugh,J., Mokdad,A. and Leontis,N.B.
(2008) FR3D: finding local and composite recurrent structural
motifs in RNA 3D structures. J. Math. Biol., 56, 215–252.
34. Terribilini,M., Lee,J.H., Yan,C., Jernigan,R.L., Carpenter,S.,
Honavar,V. and Dobbs,D. (2006) Identifying interaction sites in
‘recalcitrant’ proteins: predicted protein and RNA binding sites in
rev proteins of HIV-1 and EIAV agree with experimental data.
Pac. Symp. Biocomput., 415–426.
35. Terribilini,M., Sander,J.D., Lee,J.H., Zaback,P., Jernigan,R.L.,
Honavar,V. and Dobbs,D. (2007) RNABindR: a server for
analyzing and predicting RNA-binding sites in proteins. Nucleic
Acids Res., 35, W578–W584.
36. Stajich,J.E., Block,D., Boulez,K., Brenner,S.E., Chervitz,S.A.,
Dagdigian,C., Fuellen,G., Gilbert,J.G., Korf,I., Lapp,H. et al.
(2002) The Bioperl toolkit: Perl modules for the life sciences.
Genome Res., 12, 1611–1618.
37. Attwood,T.K., Bradley,P., Flower,D.R., Gaulton,A.,
Maudling,N., Mitchell,A.L., Moulton,G., Nordle,A., Paine,K.,
Taylor,P. et al. (2003) PRINTS and its automatic supplement,
prePRINTS. Nucleic Acids Res., 31, 400–402.
38. Wu,C.H., Nikolskaya,A., Huang,H., Yeh,L.S., Natale,D.A.,
Vinayaka,C.R., Hu,Z.Z., Mazumder,R., Kumar,S., Kourtesis,P.
et al. (2004) PIRSF: family classification system at the protein
information resource. Nucleic Acids Res., 32, D112–D114.
39. Hunter,S., Apweiler,R., Attwood,T.K., Bairoch,A., Bateman,A.,
Binns,D., Bork,P., Das,U., Daugherty,L., Duquenne,L. et al.
(2009) InterPro: the integrative protein signature database.
Nucleic Acids Res., 37, D211–D215.
D282 Nucleic AcidsResearch, 2011, Vol.39, Database issue