Conformational changes in redox pairs of protein structures

Protein Science

Volumn 18, Issue 8, 2009, Pages 1745-1765

  Fan, Samuel W ^a,b   George, Richard A ^a   Haworth, Naomi L ^a   Feng, Lina L ^a   Liu, Jason Y ^a   Wouters, Merridee A ^a,b  

^a VICTOR CHANG CARDIAC RESEARCH INSTITUTE   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

CLIC1; Disordered proteins; Disulfide redox activity; Molten globule; Oxidative stress; OxyR; Thiol based redox signaling; Zinc signaling

Indexed keywords

CYSTEINE; DISULFIDE; POLYPEPTIDE; PROTEOME; ZINC;

ARTICLE; CATALYSIS; CONFORMATIONAL TRANSITION; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DATA BANK; PROTEIN QUATERNARY STRUCTURE; PROTEIN STABILITY; PROTEIN STRUCTURE; REGULATORY MECHANISM;

COMPUTATIONAL BIOLOGY; DATABASES, PROTEIN; DISULFIDES; METALS; OXIDATION-REDUCTION; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; PROTEINS;

EID: 67749088130     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.175     Document Type: Article

References (118)

1. Yang Y, Song Y, Loscalzo J (2007) Regulation of the protein disulfide proteome by mitochondria in mammalian cells. Proc Natl Acad Sci USA 104:10813-10817.
2. Buchanan BB, Balmer Y (2005) Redox regulation: a broadening horizon. Annu Rev Plant Biol 56:187-220.
3. Ahamed J, Versteeg HH, Kerver M, Chen VM, Mueller BM, Hogg PJ, Ruf W (2006) Disulfide isomerization switches tissue factor from coagulation to cell signaling. Proc Natl Acad Sci USA 103:13932-13937.
4. Matthias LJ, Yam PTW, Jiang XM, Vandegraaff N, Li P, Poumbourios P, Donoghue N, Hogg PJ (2002) Disulfide exchange in domain 2 of CD4 is required for entry of HIV-I. Nat Immunol 3:727-732.
5. Park B, Lee S, Kim E, Cho K, Riddell SR, Cho S, Ahn K (2006) Redox regulation facilitates optimal peptide selection by MHC class I during antigen processing. Cell 127:369-382.
6. Huber-Wunderlich M, Glockshuber R (1998) A single dipeptide sequence modulates the redox properties of a whole enzyme family. Fold Des 3:161-171.
7. Krause G, Holmgren A (1991) Substitution of the conserved tryptophan-31 in Escherichia coli thioredoxin by site-directed mutagenesis and structure-function analysis. J Biol Chem 266:4056-4066.
8. Lin TY, Kim PS (1989) Urea dependence of thiol disulfide equilibria in thioredoxin-confirmation of the linkage relationship and a sensitive assay for structure. Biochemistry 28:5282-5287.
9. Wunderlich M, Glockshuber R (1993) Redox properties of protein disulfide isomerase (DsbA) from Escherichia coli. Protein Sci 2:717-726.
10. Gilbert HF (1990) Molecular and cellular aspects of thiol disulfide exchange. Adv Enzymol Relat Areas Mol Biol 63:69-172.
11. Wiita AP, Ainavarapu SRK, Huang HH, Fernandez JM (2006) Force-dependent chemical kinetics of disulfide bond reduction observed with single-molecule techniques. Proc Natl Acad Sci USA 103:7222-7227.
12. Wouters MA, George RA, Haworth NL (2007) "Forbidden" disulfides: their role as redox switches. Curr Protein Pept Sci 8:484-495.
13. Alphey MS, Gabrielsen M, Micossi E, Leonard GA, McSweeney SM, Ravelli RBG, Tetaud E, Fairlamb AH, Bond CS, Hunter WN (2003) Tryparedoxins from Crithidia fasciculata and Trypanosoma brucei - photoreduction of the redox disulfide using synchrotron radiation and evidence for a conformational switch implicated in function. J Biol Chem 278:25919-25925.
14. Roberts BR, Wood ZA, Jonsson TJ, Poole LB, Karplus PA (2005) Oxidized and synchrotron cleaved structures of the disulfide redox center in the N-terminal domain of Salmonella typhimurium AhpF. Protein Sci 14:2414-2420.
15. Weik M, Ravelli RBG, Kryger G, McSweeney S, Raves ML, Harel M, Gros P, Silman I, Kroon J, Sussman JL (2000) Specific chemical and structural damage to proteins produced by synchrotron radiation. Proc Natl Acad Sci USA 97:623-628.
16. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE (2000) The Protein Data Bank. Nucleic Acids Res 28:235-242.
17. Messens J, Martins JC, Van Belle K, Brosens E, Desmyter A, De Gieter M, Wieruszeski JM, Willem R, Wyns L, Zegers I (2002) All intermediates of the arsenate reductase mechanism, including an intramolecular dynamic disulfide cascade. Proc Natl Acad Sci USA 99:8506-8511.
18. Littler DR, Harrop SJ, Fairlie WD, Brown LJ, Pankhurst GJ, Pankhurst S, DeMaere MZ, Campbell TJ, Bauskin AR, Tonini R, Mazzanti M, Breit SN, Curmi PMG (2004) The intracellular chloride ion channel protein CLIC1 undergoes a redox-controlled structural transition. J Biol Chem 279:9298-9305.
19. Bienert GP, Schjoerring JK, Jahn TP (2006) Membrane transport of hydrogen peroxide. Biochim Biophys Acta 1758:994-1003.
20. Conour JE, Graham WV, Gaskins HR (2004) A combined in vitro/bioinformatic investigation of redox regulatory mechanisms governing cell cycle progression. Physiol Genomics 18:196-205.
21. Sun JP, Wang WQ, Yang H, Liu S, Liang F, Fedorov AA, Almo SC, Zhang ZY (2005) Structure and biochemical properties of PRL-1, a phosphatase implicated in cell growth, differentiation, and tumor invasion. Biochemistry 44:12009-12021.
22. Buhrman G, Parker B, Sohn J, Rudolph J, Mattos C (2005) Structural mechanism of oxidative regulation of the phosphatase Cdc25B via an intramolecular disulfide bond. Biochemistry 44:5307-5316.
23. Choi HJ, Kim SJ, Mukhopadhyay P, Cho S, Woo JR, Storz G, Ryu SE (2001) Structural basis of the redox switch in the OxyR transcription factor. Cell 105:103-113.
24. Mao SS, Holler TP, Yu GX, Bollinger JM, Booker S, Johnston MI, Stubbe J (1992) A model for the role of multiple cysteine residues involved in ribonucleotide reduction - amazing and still confusing. Biochemistry 31:9733-9743.
25. Parsonage D, Karplus PA, Poole LB (2008) Substrate specificity and redox potential of AhpC, a bacterial peroxiredoxin. Proc Natl Acad Sci USA 105:8209-8214.
26. Adam V, Royant A, Nivière V, Molina-Heredia FP, Bourgeois D (2004) Structure of superoxide reductase bound to ferrocyanide and active site expansion upon X-ray-induced photo-reduction. Structure 12:1729-1740.
27. Wouters MA, Lau KK, Hogg PJ (2004) Cross-strand disulphides in cell entry proteins: poised to act. BioEssays 26:73-79.
28. Camon E, Magrane M, Barrell D, Lee V, Dimmer E, Maslen J, Binns D, Harte N, Lopez R, Apweiler R (2004) The Gene Ontology Annotation (GOA) Database: sharing knowledge in Uniprot with Gene Ontology. Nucleic Acids Res 32:D262-D266.
29. Conant CG, Stephens RS (2007) Chlamydia attachment to mammalian cells requires protein disulfide isomerase. Cell Microbiol 9:222-232.
30. Jain S, McGinnes LW, Morrison TG (2006) Thiol/disulfide exchange is required for membrane fusion directed by the Newcastle disease virus fusion protein. J Virol. 81:2328-2339.
31. Gallina A, Hanley TM, Mandel R, Trahey M, Broder CC, Viglianti GA, Ryser HJP (2002) Inhibitors of protein-disulfide isomerase prevent cleavage of disulfide bonds in receptor-bound glycoprotein 120 and prevent HIV-1 entry. J Biol Chem 277:50579-50588.
32. Barbouche R, Miquelis R, Jones IM, Fenouillet E (2003) Protein-disulfide isomerase-mediated reduction of two disulfide bonds of HIV envelope glycoprotein 120 occurs post-CXCR4 binding and is required for fusion. J Biol Chem 278:3131-3136.
33. Katz BA, Kossiakoff A (1986) The crystallographically determined structures of atypical strained disulfides engineered into subtilisin. J Biol Chem 261:5480-5485.
34. Weiner SJ, Kollman PA, Case DA, Singh UC, Ghio C, Alagona G, Profeta S, Weiner P (1984) A new force-field for molecular mechanical simulation of nucleic-acids and proteins. J Am Chem Soc 106:765-784.
35. Wells JA, Powers DB (1986) In vivo formation and stability of engineered disulfide bonds in subtilisin. J Biol Chem 261:6564-6570.
36. Wetzel R (1987) Harnessing disulfide bonds using protein engineering. Trends Biochem Sci 12:478-482.
37. Richardson JS (1981) The anatomy and taxonomy of protein structure. Adv Protein Chem 34:167-339.
38. Thornton JM (1981) Disulfide bridges in globular proteins. J Mol Biol 151:261-287.
39. Numata T, Ikeuchi Y, Fukai S, Suzuki T, Nureki O (2006) Snapshots of tRNA sulphuration via an adenylated intermediate. Nature 442:419-424.
40. Maret W (2006) Zinc coordination environments in proteins as redox sensors and signal transducers. Antioxid Redox Signal 8:1419-1441.
41. Mesecke N, Terziyska N, Kozany C, Baumann F, Neupert W, Hell K, Herrmann JM (2005) A disulfide relay system in the intermembrane space of mitochondria that mediates protein import. Cell 121:1059-1069.
42. Evans JC, Huddler DP, Jiracek J, Castro C, Millian NS, Garrow TA, Ludwig ML (2002) Betaine-homocysteine methyltransferase: zinc in a distorted barrel. Structure 10:1159-1171.
43. Rouhier N, Villarejo A, Srivastava M, Gelhaye E, Keech O, Droux M, Finkemeier I, Samuelsson G, Dietz KJ, Jacquot JP and others (2005) Identification of plant glutaredoxin targets. Antioxid Redox Signal 7:919-929.
44. Leichert LI, Jakob U (2004) Protein thiol modifications visualized in vivo. PLoS Biol 2:1723-1737.
45. Auerbach G, Herrmann A, Bracher A, Bader G, Gutlich M, Fischer M, Neukamm M, Garrido-Franco M, Richardson J, Nar H, Huber R, Bacher A (2000) Zinc plays a key role in human and bacterial GTP cyclohydrolase I. Proc Natl Acad Sci USA 97:13567-13572.
46. Hansen JM, Go Y-M, Jones DP (2006) Nuclear and mitochondrial compartmentation of oxidative stress and redox signaling. Annu Rev Pharmacol Toxicol 46:215-234.
47. Rosenzweig AC, Huffman DL, Hou MY, Wernimont AK, Pufahl RA, O'Halloran TV (1999) Crystal structure of the Atx1 metallochaperone protein at 1.02 Å resolution. Structure 7:605-617.
48. Dimasi N, Pasquo A, Martin F, Di Marco S, Steinkuhler C, Cortese R, Sollazzo M (1998) Engineering, characterization and phage display of hepatitis C virus NS3 protease and NS4A cofactor peptide as a single-chain protein. Protein Eng Des Sel 11:1257-1265.
49. Miyanaga A, Fushinobu S, Ito K, Shoun H, Wakagi T (2004) Mutational and structural analysis of cobalt-containing nitrile hydratase on substrate and metal binding. Eur J Biochem 271:429-438.
50. Li H, Raman CS, Glaser CB, Blasko E, Young TA, Parkinson JF, Whitlow M, Poulos TL (1999) Crystal structures of Zinc-free and -bound heme domain of human inducible nitric-oxide synthase: implications for dimer stability and comparison with endothelial nitric-oxide synthase. J Biol Chem 274:21276-21284.
51. Black S (1986) Reversible interconversion of two forms of a valyl-tRNA synthetase-containing protein complex. Science 234:1111-1114.
52. Lindahl M, Florencio FJ (2003) Thioredoxin-linked processes in cyanobacteria are as numerous as in chloroplasts, but targets are different. Proc Natl Acad Sci USA 100:16107-16112.
53. Kullik I, Toledano MB, Tartaglia LA, Storz G (1995) Mutational analysis of the redox-sensitive transcriptional regulator OxyR: regions important for oxidation and transcriptional activation. J Bacteriol 177:1275-1284.
54. Baena-Gonzalez E, Baginsky S, Mulo P, Summer H, Aro E-M, Link G (2001) Chloroplast transcription at different light intensities. Glutathione-mediated phosphorylation of the major RNA polymerase involved in redoxregulated organellar gene expression. Plant Physiol 127:1044-1052.
55. Wang X, Mukhopadhyay P, Wood MJ, Outten FW, Opdyke JA, Storz G (2006) Mutational analysis to define an activating region on the redox-sensitive transcriptional Regulator OxyR. J Bacteriol 188:8335-8342.
56. Vallee BL, Auld DS (1990) Zinc coordination, function, and structure of zinc enzymes and other proteins. Biochemistry 29:5647-5659.
57. Wouters MA, Husain A (2001) Changes in zinc ligation promote remodeling of the active site in the zinc hydrolase superfamily. J Mol Biol 314:1191-1207.
58. Maynard AT, Covell DG (2001) Reactivity of zinc finger cores: analysis of protein packing and electrostatic screening. J Am Chem Soc 123:1047-1058.
59. Hofmann A, Grella M, Botos I, Filipowicz W, Wlodawer A (2002) Crystal structures of the semireduced and inhibitor-bound forms of cyclic nucleotide phosphodiesterase from Arabidopsis thaliana. J Biol Chem 277:1419-1425.
60. Kim SO, Merchant K, Nudelman R, Beyer WF, Keng T, DeAngelo J, Hausladen A, Stamler JS (2002) OxyR: a molecular code for redox-related signaling. Cell 109:383-396.
61. Haworth NL, Gready JE, George RA, Wouters MA (2007) Evaluating the stability of disulfide bridges in proteins: a torsional potential energy surface for diethyl disulfide. Mol Simul 33:475-485.
62. Chiadmi M, Navaza A, Miginiac-Maslow M, Jacquot JP, Cherfils J (1999) Redox signalling in the chloroplast: structure of oxidized pea fructose-1,6-bisphosphate phosphatase. EMBO J 18:6809-6815.
63. Wenderoth I, Scheibe R, vonSchaewen A (1997) Identification of the cysteine residues involved in redox modification of plant plastidic glucose-6-phosphate dehydrogenase. J Biol Chem 272:26985-26990.
64. Xu S-Z, Sukumar P, Zeng F, Li J, Jairaman A, English A, Naylor J, Ciurtin C, Majeed Y, Milligan CJ, Bahnasi YM, Al-Shawaf E, Porter KE, Jiang L-H, Emery P, Sivaprasadarao A, Beech DJ (2008) TRPC channel activation by extracellular thioredoxin. Nature 451:69-72.
65. Crow A, Acheson RM, Le Brun NE, Oubrie A (2004) Structural basis of redox-coupled protein substrate selection by the cytochrome c biosynthesis protein ResA. J Biol Chem 279:23654-23660.
66. Toral-Barza L, Zhang WG, Huang X, McDonald LA, Salaski EJ, Barbieri LR, Ding WD, Krishnamurthy G, Yong BH, Lucas J, Bernan VS, Cai P, Levin JI, Mansour TS, Gibbons JJ, Abraham RT, Yu K (2007) Discovery of lactoquinomycin and related pyranonaphthoquinones as potent and allosteric inhibitors of AKT/PKB: mechanistic involvement of AKT catalytic activation loop cysteines. Mol Cancer Ther 6:3028-3038.
67. Huang X, Begley M, Morgenstern KA, Gu Y, Rose P, Zhao H, Zhu X (2003) Crystal structure of an inactive Akt2 kinase domain. Structure 11:21-30.
68. Chen W-J, Lee IS, Chen C-Y, Liao T-H (2004) Biological functions of the disulfides in bovine pancreatic deoxyribonuclease. Protein Sci 13:875-883.
69. Korolainen MA, Nyman TA, Nyyssonen P, Hartikainen ES, Pirttila T (2007) Multiplexed proteomic analysis of oxidation and concentrations of cerebrospinal fluid proteins in Alzheimer disease. Clin Chem 53:657-665.
70. Leslie NR (2006) The redox regulation of PI 3-kinase-dependent signaling. Antioxid Redox Signal 8:1765-1774.
71. Lincecum TL, Tukalo M, Yaremchuk A, Mursinna RS, Williams AM, Sproat BS, Van Den Eynde W, Link A, Van Calenbergh S, Grøtli M, Martinis SA, Cusack S (2003) Structural and mechanistic basis of pre- and posttransfer editing by leucyl-tRNA synthetase. Mol Cell 11:951-963.
72. Tukalo M, Yaremchuk A, Fukunaga R, Yokoyama S, Cusack S (2005) The crystal structure of leucyl-tRNA synthetase complexed with tRNALeu in the post-transfer-editing conformation. Nat Struct Mol Biol 12:923-930.
73. Dunker AK, Brown CJ, Lawson JD, Iakoucheva LM, Obradovic Z (2002) Intrinsic disorder and protein function. Biochemistry 41:6573-6582.
74. Oubrie A, Rozeboom HJ, Kalk KH, Olsthoorn AJJ, Duine JA, Dijkstra BW (1999) Structure and mechanism of soluble quinoprotein glucose dehydrogenase. EMBO J 18:5187-5194.
75. Phannachet K, Huang RH (2004) Conformational change of pseudouridine 55 synthase upon its association with RNA substrate. Nucleic Acids Res 32:1422-1429.
76. Romero P, Obradovi Z, Kissinger C, Villafranca JE, Dunker AK (1997) Identifying disordered regions in proteins from amino acid sequence. IEEE Int Conf Neural Networks 1:90-95.
77. Romero P, Obradovic Z, Li X, Garner EC, Brown CJ, Dunker AK (2001) Sequence complexity of disordered protein. Proteins 42:38-48.
78. Head JF, Swamy N, Ray R (2002) Crystal structure of the complex between actin and human vitamin D-binding protein at 2.5 Å resolution. Biochemistry 41:9015-9020.
79. Verboven C, Rabijns A, De Maeyer M, Van Baelen H, Bouillon R, De Ranter C (2002) A structural basis for the unique binding features of the human vitamin D-binding protein. Nat Struct Mol Biol 9:131-136.
80. Oubrie A, Rozeboom HJ, Kalk KH, Duine JA, Dijkstra BW (1999) The 1.7 A crystal structure of the apo form of the soluble quinoprotein glucose dehydrogenase from Acinetobacter calcoaceticus reveals a novel internal conserved sequence repeat. J Mol Biol 289:319-333.
81. Xu L, Benson SD, Butcher SJ, Bamford DH, Burnett RM (2003) The receptor binding protein P2 of PRD1, a virus targeting antibiotic-resistant bacteria, has a novel fold suggesting multiple functions. Structure 11:309-322.
82. Nathan RZ, May AP, Robinson RC, Burtnick LD, Crocker PR, Brossmer R, Kelm S, Jones EY (2007) Crystallographic and in silico analysis of the sialoside-binding characteristics of the Siglec sialoadhesin. J Mol Biol 365:1469-1479.
83. Galang CK, Hauser CA (1993) Cooperative DNA binding of the human HoxB5 (Hox-2.1) protein is under redox regulation in vitro. Mol Cell Biol 13:4609-4617.
84. Sun XZ, Vinci C, Makmura L, Han SB, Tran D, Nguyen J, Hamann M, Grazziani S, Sheppard S, Gutova M, Zhou FM, Thomas J, Momand J (2003) Formation of disulfide bond in p53 correlates with inhibition of DNA binding and tetramerization. Antioxid Redox Signal 5:655-665.
85. Buchanan BB (1980) Role of light in the regulation of chloroplast enzymes. Annu Rev Plant Physiol 31:341-374.
86. Fermani S, Sparla F, Falini G, Martelli PL, Casadio R, Pupillo P, Ripamonti A, Trost P (2007) Molecular mechanism of thioredoxin regulation in photosynthetic A2B2-glyceraldehyde-3-phosphate dehydrogenase. Proc Natl Acad Sci USA 104:11109-11114.
87. Oesterhelt C, Klocke S, Holtgrefe S, Linke V, Weber APM, Scheibe R (2007) Redox regulation of chloroplast enzymes in Galdieria sulphuraria in view of eukaryotic evolution. Plant Cell Physiol 48:1359-1373.
88. Shivapurkar N, Stastny V, Okumura N, Girard L, Xie Y, Prinsen C, Thunnissen FB, Wistuba II, Czerniak B, Frenkel E, Roth JA, Liloglou T, Xinarianos G, Field JK, Minna JD, Gazdar AF (2008) Cytoglobin, the newest member of the globin family, functions as a tumor suppressor gene. Cancer Res 68:7448-7456.
89. Sugimoto H, Makino M, Sawai H, Kawada N, Yoshizato K, Shiro Y (2004) Structural basis of human cytoglobin for ligand binding. J Mol Biol 339:873-885.
90. Mehta RA, Fawcett TW, Porath D, Mattoo AK (1992) Oxidative stress causes rapid membrane translocation and in vivo degradation of ribulose-1,5- bisphosphate carboxylase/oxygenase. J Biol Chem 267:2810-2816.
91. Cámara-Artigas A, Hirasawa M, Knaff DB, Wang M, Allen JP (2006) Crystallization and structural analysis of GADPH from Spinacia oleracea in a new form. Acta Crystallogr Sect F Struct Biol Cryst Commun 62:1087-1092.
92. Hui JO, Woo G, Chow DT, Katta V, Osslund T, Haniu M (1999) The intermolecular disulfide bridge of human glial cell line-derived neurotrophic factor: its selective reduction and biological activity of the modified protein. J Protein Chem 18:585-593.
93. Garcia-Diaz M, Bebenek K, Krahn JM, Kunkel TA, Pedersen LC (2005) A closed conformation for the Polk catalytic cycle. Nat Struct Mol Biol 12:97-98.
94. Hink-Schauer C, Estebanez-Perpina E, Kurschus FC, Bode W, Jenne DE (2003) Crystal structure of the apoptosis-inducing human granzyme A dimer. Nat Struct Mol Biol 10:535-540.
95. Wang Y, Jiang Y, Meyering-Voss M, Sprinzl M, Sigler PB (1997) Crystal structure of the EF-Tu.EF-Ts complex from Thermus thermophilus. Nat Struct Mol Biol 4:650-656.
96. Muto T, Tsuchiya D, Morikawa K, Jingami H (2007) Structures of the extracellular regions of the group II/III metabotropic glutamate receptors. Proc Natl Acad Sci USA 104:3759-3764.
97. Tiwari A, Haward TJ (2005) Mutant SOD1 instability: implications for toxicity in amyotrophic lateral sclerosis. Neurodegener Dis 2:115-127.
98. Furukawa Y, Fu R, Deng HX, Siddique T, O'Halloran T (2006) Disulfide cross-linked protein represents a significant fraction of ALS-associated Cu, Zn-superoxide dismutase aggregates in spinal cords of model mice. Proc Natl Acad Sci USA 103:7148-7153.
99. Ilbert M, Horst J, Ahrens S, Winter J, Graf PCF, Lilie H, Jakob U (2007) The redox-switch domain of Hsp33 functions as dual stress sensor. Nat Struct Mol Biol 14:556-563.
100. Castro C, Millian NS, Garrow TA (2008) Liver betaine-homocysteine S-methyltransferase activity undergoes a redox switch at the active site zinc. Arch Biochem Biophys 472:26-33.
101. Millian NS, Garrow TA (1998) Human betaine-homocysteine methyltransferase is a zinc metalloenzyme. Arch Biochem Biophys 356:93-98.
102. Mayo KH, Barker S, Kuranda MJ, Hunt AJ, Myers JA, Maione TE (1992) Molten globule monomer to condensed dimer: role of disulfide bonds in platelet factor-4 folding and subunit association. Biochemistry 31:12255-12265.
103. Vucetic S, Brown CJ, Dunker AK, Obradovic Z (2003) Flavors of protein disorder. Proteins 52:573-584.
104. 2+. J Mol Biol 310:659-672.
105. Bullough PA, Hughson FM, Skehel JJ, Wiley DC (1994) Structure of influenza hemagglutinin at the pH of membrane-fusion. Nature 371:37-43.
106. Tuinstra RL, Peterson FC, Kutlesa S, Elgin ES, Kron MA, Volkman BF (2008) Interconversion between two unrelated protein folds in the lymphotactin native state. Proc Natl Acad Sci USA 105:5057-5062.
107. Mapelli M, Massimiliano L, Santaguida S, Musacchio A (2007) The Mad2 conformational dimer: structure and implications for the spindle assembly checkpoint. Cell 131:730-743.
108. Murzin AG (2008) Metamorphic proteins. Science 320:1725-1726.
109. Yeates TO (2007) Protein structure: evolutionary bridges to new folds. Curr Biol 17:R48-R50.
110. Milbradt AG, Boulegue C, Moroder L, Renner C (2005) The two cysteine-rich head domains of minicollagen from Hydra nematocysts differ in their cystine framework and overall fold despite an identical cysteine sequence pattern. J Mol Biol 354:591-600.
111. Xu M, Arulandu A, Struck DK, Swanson S, Sacchettini JC, Young R (2005) Disulfide isomerization after membrane release of its SAR domain activates P1 lysozyme. Science 307:113-117.
112. Kabsch W, Sander C (1983) Dictionary of protein secondary structure-pattern-recognition of hydrogen-bonded and geometrical features. Biopolymers 22:2577-2637.
113. van Vlijmen HWT, Gupta A, Narasimhan LS, Singh J (2004) A novel database of disulfide patterns and its application to the discovery of distantly related homologs. J Mol Biol 335:1083-1092.
114. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403-410.
115. Khatri P, Draghici S (2005) Ontological analysis of gene expression data: current tools, limitations, and open problems. Bioinformatics 21:3587-3595.
116. Mateos A, Herrero J, Tamames J, Dopazo J, Supervised neural networks for clustering conditions in DNA array data after reducing noise by clustering gene expression profiles. In: Lin S, Johnson K, Eds. (2002) Methods of microarray data analysis. Boston: Kluwer Academic Publishers, pp 91-103.
117. Flocco MM, Mowbray SL (1995) Ca-based torsion angles: a simple tool to analyze protein conformational changes. Protein Sci 4:2118-2122.
118. Murzin AG, Brenner SE, Hubbard T, Chothia C (1995) SCOP - a structural classification of proteins database for the investigation of sequences and structures. J Mol Biol 247:536-540.