Calmodulin signaling: Analysis and prediction of a disorder-dependent molecular recognition

Proteins: Structure, Function and Genetics

Volumn 63, Issue 2, 2006, Pages 398-410

  Radivojac, Predrag ^a   Vucetic, Slobodan ^b   O'Connor, Timothy R ^c   Uversky, Vladimir N ^d   Obradovic, Zoran ^b   Dunker, A Keith ^d  

^a INDIANA UNIVERSITY   (United States)

^b TEMPLE UNIVERSITY   (United States)

^c Washington State University   (United States)

^d INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Protein function; Protein protein interactions; Unfolded; Unstructured

Indexed keywords

BINDING PROTEIN; CALMODULIN; TRYPSIN;

AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; MOLECULAR RECOGNITION; NONHUMAN; PREDICTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN TARGETING; TARGET CELL;

ANIMALS; CALMODULIN; CHICKENS; DATABASES, FACTUAL; HUMANS; PROTEIN BINDING; REPRODUCIBILITY OF RESULTS; SIGNAL TRANSDUCTION;

EUKARYOTA;

EID: 33645292569     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.20873     Document Type: Article

References (101)

1. Van Eldik LJ, Watterson DM, editors. Calmodulin and signal transduction; San Diego: Academic Press; 1998.
2. Stull JT. Ca2+-dependent cell signaling through calmodulin-activated protein phosphatase and protein kinases minireview series. J Biol Chem 2001;276(4):2311-2312.
3. Vetter SW, Leclerc E. Novel aspects of calmodulin target recognition and activation. Eur J Biochem 2003;270(3):404-414.
4. Barbato G, Ikura M, Kay LE, Pastor RW, Bax A. Backbone dynamics of calmodulin studied by 15N relaxation using inverse detected two-dimensional NMR spectroscopy: the central helix is flexible. Biochemistry 1992;31(23):5269-5278.
5. Wall ME, Clarage JB, Phillips GN. Motions of calmodulin characterized using both Bragg and diffuse X-ray scattering. Structure 1997;5(12):1599-1612.
6. Finn BE, Evenas J, Drakenberg T, Waltho JP, Thulin E, Forsen S. Calcium-induced structural changes and domain autonomy in calmodulin. Nat Struct Biol 1995;2(9):777-783.
7. Babu YS, Sack JS, Greenhough TJ, Bugg CE, Means AR, Cook WJ. Three-dimensional structure of calmodulin. Nature 1985;315(6014):37-40.
8. Babu Y, Bugg CE, Cook WJ. Structure of calmodulin refined at 2.2 Å resolution. J Mol Biol 1988;203:191-204.
9. Chin D, Means AR. Calmodulin: a prototypical calcium sensor. Trends Cell Biol 2000;10(8):322-328.
10. Hook SS, Means AR. Ca(2+)/CaM-dependent kinases: from activation to function. Annu Rev Pharmacol Toxicol 2001;41:471-505.
11. Klee CB, Ren H, Wang X. Regulation of the calmodulin-stimulated protein phosphatase, calcineurin. J Biol Chem 1998;273(22):13367-13370.
12. Osawa M, Swindells MB, Tanikawa J, Tanaka T, Mase T, Furuya T, Ikura M. Solution structure of calmodulin-W-7 complex: the basis of diversity in molecular recognition. J Mol Biol 1998;276(1):165-176.
13. Albrecht K, Hart J, Shaw A, Dunker AK. Quaternion contact ribbons: a new tool for visualizing intra- and intermolecular interactions in proteins. Pac Symp Biocomput 1996;1:41-52.
14. Yap K, Kim J, Truong K, Sherman M, Yuan T, Ikura M. Calmodulin target database. J Struct Funct Genomics 2000;1:8-14.
15. Osawa M, Tokumitsu H, Swindells MB, Kurihara H, Orita M, Shibanuma T, Furuya T, Ikura M. A novel target recognition revealed by calmodulin in complex with Ca2+-calmodulin-dependent kinase kinase. Nat Struct Biol 1999;6(9):819-824.
16. Yuan T, Vogel HJ, Sutherland C, Walsh MP. Characterization of the Ca2+-dependent and -independent interactions between calmodulin and its binding domain of inducible nitric oxide synthase. FEBS Lett 1998;431(2):210-214.
17. Wright PE, Dyson HJ. Intrinsically unstructured proteins: reassessing the protein structure-function paradigm. J Mol Biol 1999;293:321-331.
18. Dunker AK, Lawson JD, Brown CJ, Williams RM, Romero P, Oh JS, Oldfield CJ, Campen AM, Ratliff CM, Hipps KW, Ausio J, Nissen MS, Reeves R, Kang C, Kissinger CR, Bailey RW, Griswold MD, Chiu W, Garner EC, Obradovic Z. Intrinsically disordered protein. J Mol Graph Model 2001;19(1):26-59.
19. Uversky VN. What does it mean to be natively unfolded? Eur J Biochem 2002;269(1):2-12.
20. Tompa P. Intrinsically unstructured proteins. Trends Biochem Sci 2002;27:527-533.
21. Dyson HJ, Wright PE. Intrinsically unstructured proteins and their functions. Nat Rev Mol Cell Biol 2005;6(3):197-208.
22. Depaoli-Roach AA, Gibbs JB, Roach PJ. Calcium and calmodulin activation of muscle phosphorylase kinase: effect of tryptic proteolysis. FEBS Lett 1979;105(2):321-324.
23. Toscano WA Jr, Westcott KR, LaPorte DC, Storm DR. Evidence for a dissociable protein subunit required for calmodulin stimulation of brain adenylate cyclase. Proc Natl Acad Sci USA 1979;76(11):5582-5586.
24. Tucker MM, Robinson JB Jr, Stellwagen E. The effect of proteolysis on the calmodulin activation of cyclic nucleotide phosphodiesterase. J Biol Chem 1981;256(17):9051-9058.
25. Meijer L, Guerrier P. Activation of calmodulin-dependent NAD+ kinase by trypsin. Biochim Biophys Acta 1982;702(1):143-146.
26. Manalan AS, Klee CB. Activation of calcineurin by limited proteolysis. Proc Natl Acad Sci USA 1983;80:4291-4295.
27. Fontana A, de Laureto PP, de Filippis V, Scaramella L, Zambonin M. Limited proteolysis in the study of protein conformation. In: Sterchi EE, Stöcker W, editors. Proteolytic enzymes: tool and targets. Springer-Verlag; 1999. p 257-284.
28. O'Neil KT, Wolfe HR Jr, Erickson-Viitanen S, DeGrado WF. Fluorescence properties of calmodulin-binding peptides reflect alpha-helical periodicity. Science 1987;236(4807):1454-1456.
29. Krueger JK, Bishop NA, Blumenthal DK, Zhi G, Beckingham K, Stull JT, Trewhella J. Calmodulin binding to myosin light chain kinase begins at substoichiometric Ca2+ concentrations: a small-angle scattering study of binding and conformational transitions. Biochemistry 1998;37(51):17810-17817.
30. Pappu RV, Srinivasan R, Rose GD. The Flory isolated-pair hypothesis is not valid for polypeptide chains: implications for protein folding. Proc Natl Acad Sci USA 2000;97(23):12565-12570.
31. Pappu RV, Rose GD. A simple model for polyproline II structure in unfolded states of alanine-based peptides. Protein Sci 2002;11(10):2437-2455.
32. Rose GD, Richards FM, Eisenberg DS, Kuriyan J, editors. Unfolded proteins. Volume 62, Advances in protein chemistry. New York: Academic Press; 2002.
33. Dunker AK, Brown CJ, Lawson JD, Iakoucheva LM, Obradovic Z. Intrinsic disorder and protein function. Biochemistry 2002;41(21):6573-6582.
34. Rost B, Liu J, Nair R, Wrzeszczynski KO, Ofran Y. Automatic prediction of protein function. Cell Mol Life Sci 2003;60(12):2637-2650.
35. Vucetic S, Obradovic Z, Vacic V, Radivojac P, Peng K, Iakoucheva LM, Cortese MS, Lawson JD, Brown CJ, Sikes JG, Newton CD, Dunker AK. DisProt: a database of protein disorder. Bioinformatics 2005;21(1):137-140.
36. Smith DK, Radivojac P, Obradovic Z, Dunker AK, Zhu G. Improved amino acid flexibility parameters. Protein Sci 2003;12:1060-1072.
37. Boeckmann B, Bairoch A, Apweiler R, Blatter M-C, Estreicher A, Gasteiger E, Martin MJ, Michoud K, O'Donovan C, Phan I, Pilbout S, Schneider M. The SWISS-PROT protein knowledge-base and its supplement TrEMBL in 2003. Nucleic Acids Res 2003;31:365-370.
38. Wootton JC, Federhen S. Analysis of compositionally biased regions in sequence databases. Methods Enzymol 1996;266:554-571.
39. Eisenberg D, Weiss RM, Terwilliger TC. The hydrophobic moment detects periodicity in protein hydrophobicity. Proc Natl Acad Sci USA 1984;81:140-144.
40. Rost B, Sander C, Schneider R. PHD-an automatic mail server for protein secondary structure prediction. Comput Appl Biosci (CABIOS) 1994;10(1):53-60.
41. Romero P, Obradovic Z, Li X, Garner EC, Brown CJ, Dunker AK. Sequence complexity of disordered protein. Proteins 2001;42:38-48.
42. Obradovic Z, Peng K, Vucetic S, Radivojac P, Brown CJ, Dunker AK. Predicting intrinsic disorder from amino acid sequence. Proteins 2003;53(S6):566-572.
43. Vucetic S, Brown CJ, Dunker AK, Obradovic Z. Flavors of protein disorder. Proteins 2003;52:573-584.
44. Blum A, Mitchell T. Combining labeled and unlabeled data with co-training. Proceedings of the 11th Annual Conference on Computational Learning Theory; Madison, WI, 1998. p 92-100.
45. Vucetic S, Obradovic Z. Classification on data with biased class distribution. Proceedings of the 12th European Conference on Machine Learning, Freiburg, Germany. 2001. p 527-538.
46. Kyte J, Doolittle RF. A simple method for displaying the hydropathic character of a protein. J Mol Biol 1982;157:105-132.
47. Vihinen M, Torkkila E, Riikonen P. Accuracy of protein flexibility predictions. Proteins 1994;19:141-149.
48. Galaktionov SG, Marshall GR. Prediction of protein structure in terms of intraglobular contacts: 1D to 2D to 3D. In: States DJ, Agarwal P, Gaasterland T, Hunter L, Smith RF, editors. Proc Int Conf Intell Syst Mol Biol; June 12-15, 1996; Washington University Institute for Biomedical Computing, Center for Molecular Design, St. Louis, MO. AAAI Press. 1996. p 42.
49. Peng K, Obradovic Z, Vucetic S. Exploring bias in the Protein Data Bank using contrast classifiers. Pac Symp Biocomput 2004:435-446.
50. Garner E, Cannon P, Romero P, Obradovic Z, Dunker AK. Predicting disordered regions from amino acid sequence: common themes despite differing structural characterization. Genome Inform Ser Workshop Genome Inform 1998;9:201-213.
51. Hazzard J, Sudhof TC, Rizo J. NMR analysis of the structure of synaptobrevin and of its interaction with syntaxin. J Biomol NMR 1999;14:203-207.
52. DeGrado WF, Erickson-Viitanen S, Wolfe HR Jr, O'Neil KT. Predicted calmodulin-binding sequence in the gamma subunit of phosphorylase b kinase. Proteins 1987;2(1):20-33.
53. Fraser ID, Copeland O, Bing W, Marston SB. The inhibitory complex of smooth muscle caldesmon with actin and tropomyosin involves three interacting segments of the C-terminal domain 4. Biochemistry 1997;36(18):5483-5492.
54. Gusev NB. Some properties of caldesmon and calponin and the participation of these proteins in regulation of smooth muscle contraction and cytoskeleton formation. Biochemistry (Mosc) 2001;66(10):1112-1121.
55. Huber PA, El-Mezgueldi M, Grabarek Z, Slatter DA, Levine BA, Marston SB. Multiple-sited interaction of caldesmon with Ca(2+)-calmodulin. Biochem J 1996;316(Pt 2):413-420.
56. Medvedeva MV, Kolobova EA, Huber PA, Fraser ID, Marston SB, Gusev NB. Mapping of contact sites in the caldesmon-calmodulin complex. Biochem J 1997;324(Pt 1):255-262.
57. Wang E, Zhuang S, Kordowska J, Grabarek Z, Wang CL. Calmodulin binds to caldesmon in an antiparallel manner. Biochemistry 1997;36(48):15026-15034.
58. Marston SB, Redwood CS. The molecular anatomy of caldesmon. Biochem J 1991;279(Pt 1):1-16.
59. Lynch WP, Riseman VM, Bretscher A. Smooth muscle caldesmon J is an extended flexible monomeric protein in solution that can readily undergo reversible intra- and intermolecular sulfhydryl cross-linking. A mechanism for caldesmon's F-actin bundling activity. J Biol Chem 1987;262(15):7429-7437.
60. Zhu H, Bilgin M, Bangham R, Hall D, Casamayor A, Bertone P, Lan N, Jansen R, Bidlingmaier S, Houfek T, Mitchell T, Miller P, Dean RA, Gerstein M, Snyder M. Global analysis of protein activities using proteome chips. Science 2001;293(5537):2101-2105.
61. Sobue K, Sellers JR. Caldesmon, a novel regulatory protein in smooth muscle and nonmuscle actomyosin systems. J Biol Chem 1991;266(19):12115-12118.
62. Matsumura F, Yamashiro S. Caldesmon. Curr Opin Cell Biol 1993;5(1):70-76.
63. Sobue K, Muramoto Y, Fujita M, Kakiuchi S. Purification of a calmodulin-binding protein from chicken gizzard that interacts with F-actin. Proc Natl Acad Sci USA 1981;78(9):5652-5655.
64. Huber PA. Caldesmon. Int J Biochem Cell Biol 1997;29(8-9):1047-1051.
65. Dabrowska R, Kulikova N, Gagola M. Nonmuscle caldesmon: its distribution and involvement in various cellular processes. Review article. Protoplasma 2004;224(1-2):1-13.
66. Morgan KG, Gangopadhyay SS. Invited review: cross-bridge regulation by thin filament-associated proteins. J Appl Physiol 2001;91(2):953-962.
67. Adelstein RS, Eisenberg E. Regulation and kinetics of the actin-myosin-ATP interaction. Annu Rev Biochem 1980;49:921-956.
68. Bouche N, Scharlat A, Snedden W, Bouchez D, Fromm H. A novel family of calmodulin-binding transcription activators in multicellular organisms. J Biol Chem 2002;277(24):21851-21861.
69. Luan S, Kudla J, Rodriguez-Concepcion M, Yalovsky S, Gruissem W. Calmodulins and calcineurin B-like proteins: calcium sensors for specific signal response coupling in plants. Plant Cell 2002;14 Suppl:S389-S400.
70. Liao B, Paschal BM, Luby-Phelps K. Mechanism of Ca2+-dependent nuclear accumulation of calmodulin. Proc Natl Acad Sci USA 1999;96(11):6217-6222.
71. Szymanski DB, Liao B, Zielinski RE. Calmodulin isoforms differentially enhance the binding of cauliflower nuclear proteins and recombinant TGA3 to a region derived from the Arabidopsis Cam-3 promoter. Plant Cell 1996;8(6):1069-1077.
72. Jeffery CJ. Molecular mechanisms for multitasking: recent crystal structures of moonlighting proteins. Curr Opin Struct Biol 2004;14(6):663-668.
73. Wool IG. Extraribosomal functions of ribosomal proteins. Trends Biochem Sci 1996;21(5):164-165.
74. Chan YL, Suzuki K, Olvera J, Wool IG. Zinc finger-like motifs in rat ribosomal proteins S27 and S29. Nucleic Acids Res 1993;21(3):649-655.
75. Chan YL, Olvera J, Gluck A, Wool IG. A leucine zipper-like motif and a basic region-leucine zipper-like element in rat ribosomal protein L13a. Identification of the turn-transplantation antigen P198. J Biol Chem 1994;269(8):5589-5594.
76. Rice PA, Steitz TA. Ribosomal protein L7/L12 has a helix-turn-helix motif similar to that found in DNA-binding regulatory proteins. Nucleic Acids Res 1989;17(10):3757-3762.
77. Mazumder B, Sampath P, Seshadri V, Maitra RK, DiCorleto PE, Fox PL. Regulated release of L13a from the 60S ribosomal subunit as a mechanism of transcript-specific translational control. Cell 2003;115(2):187-198.
78. Tompa P. Intrinsically unstructured proteins evolve by repeat expansion. Bioessays 2003;25(9):847-855.
79. Iakoucheva LM, Radivojac P, Brown CJ, O'Connor TR, Sikes JG, Obradovic Z, Dunker AK. The importance of intrinsic disorder for protein phosphorylation. Nucleic Acids Res 2004;32(3):1037-1049.
80. Kissinger CR, Parge HE, Knighton DR, Lewis CT, Pelletier LA, Tempczyk A, Kalish VJ, Tucker KD, Showalter RE, Moomaw EW, Gastinel LN, Habuka N, Chen X, Maldanado F, Barker JE, Bacquet R, Villafranca JE. Crystal structures of human calcineurin and the human FKBP12-FK506-calcineurin complex. Nature 1995;378:641-644.
81. Garcin ED, Bruns CM, Lloyd SJ, Hosfield DJ, Tiso M, Gachhui R, Stuehr DJ, Tainer JA, Getzoff ED. Structural basis for isozyme-specific regulation of electron transfer in nitric-oxide synthase. J Biol Chem 2004;279(36):37918- 37927.
82. Dhe-Paganon S, Ottinger EA, Nolte RT, Eck MJ, Shoelson SE. Crystal structure of the pleckstrin homology-phosphotyrosine binding (PH-PTB) targeting region of insulin receptor substrate 1. Proc Natl Acad Sci USA 1999;96(15):8378-8383.
83. Holbourn KP, Sutton JM, Evans HR, Shone CC, Acharya KR. Molecular recognition of an ADP-ribosylating Clostridium botulinum C3 exoenzyme by RaIA GTPase. Proc Natl Acad Sci USA 2005;102(15):5357-5362.
84. Dawson R, Muller L, Dehner A, Klein C, Kessler H, Buchner J. The N-terminal domain of p53 is natively unfolded. J Mol Biol 2003;332(5):1131-1141.
85. Kussie PH, Gorina S, Marechal V, Elenbaas B, Moreau J, Levine AJ, Pavletich NP. Structure of the MDM2 oncoprotein bound to the p53 tumor suppressor transactivation domain [comment]. Science 1996;274(5289):948-953.
86. Bell S, Klein C, Muller L, Hansen S, Buchner J. p53 contains large unstructured regions in its native state. J Mol Biol 2002;322(5):917-927.
87. Rustandi RR, Baldisseri DM, Weber DJ. Structure of the negative regulatory domain of p53 bound to S100B(bb). Nat Struct Biol 2000;7(7):570-574.
88. Fuxreiter M, Simon I, Friedrich P, Tompa P. Preformed structural elements feature in partner recognition by intrinsically unstructured proteins. J Mol Biol 2004;338(5):1015-1026.
89. Garner E, Romero P, Dunker AK, Brown C, Obradovic Z. Predicting binding regions within disordered proteins. Genome Inform Ser Workshop Genome Inform 1999;10:41-50.
90. Bourhis JM, Johansson K, Receveur-Brechot V, Oldfield CJ, Dunker KA, Canard B, Longhi S. The C-terminal domain of measles virus nucleoprotein belongs to the class of intrinsically disordered proteins that fold upon binding to their physiological partner. Virus Res 2004;99(2):157-167.
91. Callaghan AJ, Aurikko JP, Ilag LL, Gunter Grossmann J, Chandran V, Kuhnel K, Poljak L, Carpousis AJ, Robinson CV, Symmons MF, Luisi BF. Studies of the RNA degradosome-organizing domain of the Escherichia coli ribonuclease RNase E. J Mol Biol 2004;340(5):965-979.
92. Kingston RL, Hamel DJ, Gay LS, Dahlquist FW, Matthews BW. Structural basis for the attachment of a paramyxoviral polymerase to its template. Proc Natl Acad Sci USA 2004;101(22):8301-8306.
93. Oldfield CJ, Cheng Y, Cortese MS, Romero PR, Uversky VN, Dunker AK. Structural disorder-to-order transitions in proteins: predicting alpha-helical molecular recognition elements. Biochemistry 2005. Submitted for publication.
94. Spolar RS, Record II MT. Coupling of local folding to site-specific binding of proteins to DNA. Science 1994;263:777-784.
95. Dyson HJ, Wright PE. Coupling of folding and binding for unstructured proteins. Curr Opin Struct Biol 2002;12(1):54-60.
96. Demchenko AP. Recognition between flexible protein molecules: induced and assisted folding. J Mol Recognit 2001;14(1):42-61.
97. Uversky VN, Oldfield CJ, Dunker AK. Showing your ID: intrinsic disorder as an ID for regcognition, regulation, and cell signaling. J Mol Recogntion 2005;18:343-384.
98. Fischer E. Einfluss der configuration auf die Wirkung der enzyme. Ber Dt Chem Ges 1894;27:2985-2993.
99. Koshland DE Jr. Application of a theory of enzyme specificity to protein synthesis. Proc Natl Acad Sci USA 1958;44:98-104.
100. Sobolev V, Sorokine A, Prilusky J, Abola EE, Edelman M. Automated analysis of interatomic contacts in proteins. Bioinformatics 1999;15(4):327-332.
101. Coureux PD, Sweeney HL, Houdusse A. Three myosin V structures delineate essential features of chemo-mechanical transduction. EMBO 2004;23(23):4527-4537.