Home LiteratureArticle Details
PMID: 17488107 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Characterization of molecular recognition features, MoRFs, and their binding partners.

Journal of proteome research ·Vol. 6 ·No. 6 ·2007-06-00 ·Pages 2351-66

Vacic V, Oldfield CJ, Mohan A, Radivojac P, Cortese MS, Uversky VN, Dunker AK

Abstract

Molecular Recognition Features (MoRFs) are short, interaction-prone segments of protein disorder that undergo disorder-to-order transitions upon specific binding, representing a specific class of intrinsically disordered regions that exhibit molecular recognition and binding functions. MoRFs are common in various proteomes and occupy a unique structural and functional niche in which function is a direct consequence of intrinsic disorder. Example MoRFs collected from the Protein Data Bank (PDB) have been divided into three subtypes according to their structures in the bound state: alpha-MoRFs form alpha-helices, beta-MoRFs form beta-strands, and iota-MoRFs form structures without a regular pattern of backbone hydrogen bonds. These example MoRFs were indicated to be intrinsically disordered in the absence of their binding partners by several criteria. In this study, we used several geometric and physiochemical criteria to examine the properties of 62 alpha-, 20 beta-, and 176 iota-MoRF complex structures. Interface residues were examined by calculating differences in accessible surface area between the complex and isolated monomers. The compositions and physiochemical properties of MoRF and MoRF partner interface residues were compared to the interface residues of homodimers, heterodimers, and antigen-antibody complexes. Our analysis indicates that there are significant differences in residue composition and several geometric and physicochemical properties that can be used to discriminate, with a high degree of accuracy, between various interfaces in protein interaction data sets. Implications of these findings for the development of MoRF-partner interaction predictors are discussed. In addition, structural changes upon MoRF-to-partner complex formation were examined for several illustrative examples.

MeSH Terms
Animals Databases, Protein Humans Protein Folding Protein Interaction Mapping/standards Protein Structure, Secondary Proteins/chemistry,classification
Chemicals
Proteins
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Vacic Vladimir
Center for Computational Biology and Bioinformatics, Department of Biochemistry and Molecular Biology, Indiana University School of Medicine, Indianapolis, Indiana 46202, USA.
Oldfield Christopher J
Mohan Amrita
Radivojac Predrag
Cortese Marc S
Uversky Vladimir N
Dunker A Keith
References (83)
83 references, click to expand
  1. Surface, subunit interfaces and interior of oligomeric proteins.
    J Mol Biol. 1988 Nov 5;204(1):155-64 PMID: 3216390
  2. Insufficiently dehydrated hydrogen bonds as determinants of protein interactions.
    Proc Natl Acad Sci U S A. 2003 Jan 7;100(1):113-8 PMID: 12518060
  3. Conservation of gene order: a fingerprint of proteins that physically interact.
    Trends Biochem Sci. 1998 Sep;23(9):324-8 PMID: 9787636
  4. Enzymes and reactions at the eukaryotic DNA replication fork.
    J Biol Chem. 1997 Feb 21;272(8):4647-50 PMID: 9081985
  5. Prediction and functional analysis of native disorder in proteins from the three kingdoms of life.
    J Mol Biol. 2004 Mar 26;337(3):635-45 PMID: 15019783
  6. What does it mean to be natively unfolded?
    Eur J Biochem. 2002 Jan;269(1):2-12 PMID: 11784292
  7. Structure of the constitutively active double mutant CheYD13K Y106W alone and in complex with a FliM peptide.
    J Mol Biol. 2004 Sep 24;342(4):1325-35 PMID: 15351654
  8. The Protein Data Bank.
    Nucleic Acids Res. 2000 Jan 1;28(1):235-42 PMID: 10592235
  9. CAPRI: a Critical Assessment of PRedicted Interactions.
    Proteins. 2003 Jul 1;52(1):2-9 PMID: 12784359
  10. Dissecting protein-protein recognition sites.
    Proteins. 2002 May 15;47(3):334-43 PMID: 11948787
  11. Structure of the C-terminal region of p21(WAF1/CIP1) complexed with human PCNA.
    Cell. 1996 Oct 18;87(2):297-306 PMID: 8861913
  12. Principles of protein-protein recognition.
    Nature. 1975 Aug 28;256(5520):705-8 PMID: 1153006
  13. The Saccharomyces cerevisiae nucleoporin Nup2p is a natively unfolded protein.
    J Biol Chem. 2002 Sep 6;277(36):33447-55 PMID: 12065587
  14. Analysis of protein-protein interaction sites using surface patches.
    J Mol Biol. 1997 Sep 12;272(1):121-32 PMID: 9299342
  15. Molecular mechanism of PCNA-dependent base excision repair.
    Prog Nucleic Acid Res Mol Biol. 2001;68:129-38 PMID: 11554292
  16. Solvent-accessible surfaces of proteins and nucleic acids.
    Science. 1983 Aug 19;221(4612):709-13 PMID: 6879170
  17. An overview of structural genomics.
    Nat Struct Biol. 2000 Nov;7 Suppl:932-4 PMID: 11103991
  18. Protein import into nuclei: association and dissociation reactions involving transport substrate, transport factors, and nucleoporins.
    Cell. 1995 Dec 1;83(5):683-92 PMID: 8521485
  19. Principles of protein-protein interactions.
    Proc Natl Acad Sci U S A. 1996 Jan 9;93(1):13-20 PMID: 8552589
  20. Calculation of ensembles of structures representing the unfolded state of an SH3 domain.
    J Mol Biol. 2001 May 18;308(5):1011-32 PMID: 11352588
  21. Coupling of folding and binding for unstructured proteins.
    Curr Opin Struct Biol. 2002 Feb;12(1):54-60 PMID: 11839490
  22. Intrinsic protein disorder in complete genomes.
    Genome Inform Ser Workshop Genome Inform. 2000;11:161-71 PMID: 11700597
  23. Optimal docking area: a new method for predicting protein-protein interaction sites.
    Proteins. 2005 Jan 1;58(1):134-43 PMID: 15495260
  24. Endocytosis and vesicle trafficking.
    Curr Opin Struct Biol. 2002 Dec;12(6):814-21 PMID: 12504687
  25. Predictions of protein segments with the same aminoacid sequence and different secondary structure: a benchmark for predictive methods.
    Proteins. 2000 Dec 1;41(4):535-44 PMID: 11056040
  26. The relationship between the flexibility of proteins and their conformational states on forming protein-protein complexes with an application to protein-protein docking.
    J Mol Biol. 2005 Apr 15;347(5):1077-101 PMID: 15784265
  27. Extended disordered proteins: targeting function with less scaffold.
    Trends Biochem Sci. 2003 Feb;28(2):81-5 PMID: 12575995
  28. Comparing and combining predictors of mostly disordered proteins.
    Biochemistry. 2005 Feb 15;44(6):1989-2000 PMID: 15697224
  29. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features.
    Biopolymers. 1983 Dec;22(12):2577-637 PMID: 6667333
  30. Prediction of protein-protein interaction sites using patch analysis.
    J Mol Biol. 1997 Sep 12;272(1):133-43 PMID: 9299343
  31. Crystal structure of the p27Kip1 cyclin-dependent-kinase inhibitor bound to the cyclin A-Cdk2 complex.
    Nature. 1996 Jul 25;382(6589):325-31 PMID: 8684460
  32. Toward the structural genomics of complexes: crystal structure of a PE/PPE protein complex from Mycobacterium tuberculosis.
    Proc Natl Acad Sci U S A. 2006 May 23;103(21):8060-5 PMID: 16690741
  33. Why are "natively unfolded" proteins unstructured under physiologic conditions?
    Proteins. 2000 Nov 15;41(3):415-27 PMID: 11025552
  34. Detecting protein function and protein-protein interactions from genome sequences.
    Science. 1999 Jul 30;285(5428):751-3 PMID: 10427000
  35. The protein trinity--linking function and disorder.
    Nat Biotechnol. 2001 Sep;19(9):805-6 PMID: 11533628
  36. Sequence complexity of disordered protein.
    Proteins. 2001 Jan 1;42(1):38-48 PMID: 11093259
  37. Predicting Binding Regions within Disordered Proteins.
    Genome Inform Ser Workshop Genome Inform. 1999;10:41-50 PMID: 11072341
  38. On the role of methionine residues in the sequence-independent recognition of nonpolar protein surfaces.
    Biochemistry. 1991 Jul 9;30(27):6633-6 PMID: 2065050
  39. Calmodulin: a prototypical calcium sensor.
    Trends Cell Biol. 2000 Aug;10(8):322-8 PMID: 10884684
  40. Protein-protein interactions: a review of protein dimer structures.
    Prog Biophys Mol Biol. 1995;63(1):31-65 PMID: 7746868
  41. The yeast nuclear pore complex: composition, architecture, and transport mechanism.
    J Cell Biol. 2000 Feb 21;148(4):635-51 PMID: 10684247
  42. The atomic structure of protein-protein recognition sites.
    J Mol Biol. 1999 Feb 5;285(5):2177-98 PMID: 9925793
  43. Overexpression and sequence of the Escherichia coli cheY gene and biochemical activities of the CheY protein.
    J Bacteriol. 1984 Oct;160(1):36-41 PMID: 6090423
  44. Residue frequencies and pairing preferences at protein-protein interfaces.
    Proteins. 2001 May 1;43(2):89-102 PMID: 11276079
  45. Binding of small molecules to an adaptive protein-protein interface.
    Proc Natl Acad Sci U S A. 2003 Feb 18;100(4):1603-8 PMID: 12582206
  46. Identification of the binding interfaces on CheY for two of its targets, the phosphatase CheZ and the flagellar switch protein fliM.
    J Mol Biol. 1999 Jun 25;289(5):1423-33 PMID: 10373376
  47. Calcium-induced conformational transition revealed by the solution structure of apo calmodulin.
    Nat Struct Biol. 1995 Sep;2(9):758-67 PMID: 7552747
  48. Analysis of molecular recognition features (MoRFs).
    J Mol Biol. 2006 Oct 6;362(5):1043-59 PMID: 16935303
  49. Distribution and complementarity of hydropathy in multisubunit proteins.
    Proteins. 1991;9(1):37-55 PMID: 2017435
  50. Close encounters: why unstructured, polymeric domains can increase rates of specific macromolecular association.
    Trends Biochem Sci. 1993 May;18(5):181-6 PMID: 8328018
  51. Showing your ID: intrinsic disorder as an ID for recognition, regulation and cell signaling.
    J Mol Recognit. 2005 Sep-Oct;18(5):343-84 PMID: 16094605
  52. Structural biology of the Bcl-2 family of proteins.
    Biochim Biophys Acta. 2004 Mar 1;1644(2-3):83-94 PMID: 14996493
  53. Signal transduction schemes of bacteria.
    Cell. 1993 Jun 4;73(5):857-71 PMID: 8098993
  54. Okazaki fragment processing: modulation of the strand displacement activity of DNA polymerase delta by the concerted action of replication protein A, proliferating cell nuclear antigen, and flap endonuclease-1.
    Proc Natl Acad Sci U S A. 2001 Dec 4;98(25):14298-303 PMID: 11724925
  55. Interior and surface of monomeric proteins.
    J Mol Biol. 1987 Aug 5;196(3):641-56 PMID: 3681970
  56. Exploiting heterogeneous sequence properties improves prediction of protein disorder.
    Proteins. 2005;61 Suppl 7:176-82 PMID: 16187360
  57. An investigation of protein subunit and domain interfaces.
    Protein Eng. 1988 Jul;2(2):101-13 PMID: 3244692
  58. Coupled folding and binding with alpha-helix-forming molecular recognition elements.
    Biochemistry. 2005 Sep 20;44(37):12454-70 PMID: 16156658
  59. Hydrophobic docking: a proposed enhancement to molecular recognition techniques.
    Proteins. 1994 Dec;20(4):320-9 PMID: 7731951
  60. The structure of a Bcl-xL/Bim fragment complex: implications for Bim function.
    Immunity. 2003 Sep;19(3):341-52 PMID: 14499110
  61. Structural basis for simultaneous binding of two carboxy-terminal peptides of plant glutamate decarboxylase to calmodulin.
    J Mol Biol. 2003 Apr 18;328(1):193-204 PMID: 12684008
  62. Protein-protein interfaces: analysis of amino acid conservation in homodimers.
    Proteins. 2001 Jan 1;42(1):108-24 PMID: 11093265
  63. GlobPlot: Exploring protein sequences for globularity and disorder.
    Nucleic Acids Res. 2003 Jul 1;31(13):3701-8 PMID: 12824398
  64. The structure of protein-protein recognition sites.
    J Biol Chem. 1990 Sep 25;265(27):16027-30 PMID: 2204619
  65. Structural basis for FEN-1 substrate specificity and PCNA-mediated activation in DNA replication and repair.
    Cell. 2004 Jan 9;116(1):39-50 PMID: 14718165
  66. Calmodulin signaling: analysis and prediction of a disorder-dependent molecular recognition.
    Proteins. 2006 May 1;63(2):398-410 PMID: 16493654
  67. High-resolution protein-protein docking.
    Curr Opin Struct Biol. 2006 Apr;16(2):183-93 PMID: 16546374
  68. Accuracy of protein flexibility predictions.
    Proteins. 1994 Jun;19(2):141-9 PMID: 8090708
  69. Multiple significance tests: the Bonferroni method.
    BMJ. 1995 Jan 21;310(6973):170 PMID: 7833759
  70. Signal transduction via the multi-step phosphorelay: not necessarily a road less traveled.
    Cell. 1996 Sep 20;86(6):845-8 PMID: 8808618
  71. Structural studies of p21Waf1/Cip1/Sdi1 in the free and Cdk2-bound state: conformational disorder mediates binding diversity.
    Proc Natl Acad Sci U S A. 1996 Oct 15;93(21):11504-9 PMID: 8876165
  72. Context-dependent secondary structure formation of a designed protein sequence.
    Nature. 1996 Apr 25;380(6576):730-4 PMID: 8614471
  73. Studies of protein-protein interfaces: a statistical analysis of the hydrophobic effect.
    Protein Sci. 1997 Jan;6(1):53-64 PMID: 9007976
  74. The nucleoporin Nup60p functions as a Gsp1p-GTP-sensitive tether for Nup2p at the nuclear pore complex.
    J Cell Biol. 2001 Sep 3;154(5):937-50 PMID: 11535617
  75. Analysis of ordered and disordered protein complexes reveals structural features discriminating between stable and unstable monomers.
    J Mol Biol. 2004 Aug 27;341(5):1327-41 PMID: 15321724
  76. Morphology of protein-protein interfaces.
    Structure. 1998 Apr 15;6(4):421-7 PMID: 9562553
  77. ADVICE: Automated Detection and Validation of Interaction by Co-Evolution.
    Nucleic Acids Res. 2004 Jul 1;32(Web Server issue):W69-72 PMID: 15215353
  78. Studies of the RNA degradosome-organizing domain of the Escherichia coli ribonuclease RNase E.
    J Mol Biol. 2004 Jul 23;340(5):965-79 PMID: 15236960
  79. Speeding molecular recognition by using the folding funnel: the fly-casting mechanism.
    Proc Natl Acad Sci U S A. 2000 Aug 1;97(16):8868-73 PMID: 10908673
  80. Evolutionary rate heterogeneity in proteins with long disordered regions.
    J Mol Evol. 2002 Jul;55(1):104-10 PMID: 12165847
  81. Surface and inside volumes in globular proteins.
    Nature. 1979 Feb 8;277(5696):491-2 PMID: 763335
  82. A role for surface hydrophobicity in protein-protein recognition.
    Protein Sci. 1994 May;3(5):717-29 PMID: 8061602
  83. The Bcl-2 protein family: arbiters of cell survival.
    Science. 1998 Aug 28;281(5381):1322-6 PMID: 9735050
Article Info
Journal
Journal of proteome research
Abbr.
J Proteome Res
ISSN
1535-3893
Published
2007-06-00
Epub
2007-00-09
Pages
2351-66
Language
English
Region
United States
NLM ID
101128775
PMCID
PMC2570643
Subset
IM
Grants
NLM NIH HHS · R01 LM007688-01A1 · United States
NLM NIH HHS · R01 LM007688 · United States
NLM NIH HHS · LM007688 · United States
NIGMS NIH HHS · R01 GM071714 · United States
NLM NIH HHS · R56 LM007688 · United States
NIGMS NIH HHS · R01 GM071714-01A2 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com