Allosteric Disulfide Bonds

Chapter
Part of the Protein Reviews book series (PRON, volume 14)

Abstract

Protein disulfide bonds link cysteine residues in the polypeptide chain. The bonds contribute, sometimes crucially, to protein stability and function and are strongly conserved through the evolution of species. By analyzing the conservation of all structurally validated disulfide bonds across 29 completely sequenced eukaryotic genomes, we found that disulfide-bonded cysteines are even more conserved than tryptophan – the most conserved amino acid. Moreover, the rate of acquisition of disulfide bonds shows a strong positive correlation with organism complexity, which probably reflects the requirement for more sophistication in protein function in complex species. The majority of disulfide bonds perform a structural role by stabilizing the mature protein. Some disulfide bonds perform a functional role in the mature protein and can be divided into catalytic or allosteric disulfides. Catalytic disulfides/dithiols transfer electrons between proteins, while the allosteric bonds control the function of the protein in which they reside when they break and/or form. There are currently a dozen or so examples of allosteric disulfide bonds. The features of these bonds and their involvement in the respective proteins’ function are discussed. A common aspect of 11 of the 12 allosteric bonds discussed herein is that they link β-strands or β-loops.

Keywords

Allosteric disulfide bonds Functional disulfide bonds Disulfide bond evolution CD4 gp120 β2-glycoprotein I 

Abbreviations

β2GPI

β2-glycoprotein I

Csk

Carboxyl-terminal Src kinase

ERp5

Endoplasmic reticulum protein 5

GFP

Green fluorescent protein

HIV

Human immunodeficiency virus

MHCI

Major histocompatibility complex class I

NK

Natural killer

PDI

Protein disulfide isomerase

TG2

Transglutaminase 2

VWC

von Willebrand factor type C domains

VWF

von Willebrand factor

References

  1. Abreu JG, Coffinier C, Larraín J, Oelgeschläger M, De Robertis EM (2002) Chordin-like cr domains and the regulation of evolutionarily conserved extracellular signalling systems. Gene 287:39–47Google Scholar
  2. 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(38):13932–13937PubMedCrossRefGoogle Scholar
  3. Auwerx J, Isacsson O, Soderlund J, Balzarini J, Johansson M, Lundberg M (2009) Human glutaredoxin-1 catalyzes the reduction of hiv-1 gp120 and cd4 disulfides and its inhibition reduces hiv-1 replication. Int J Biochem Cell Biol 41(6):1269–1275PubMedCrossRefGoogle Scholar
  4. Azimi I, Matthias LJ, Center RJ, Wong JW, Hogg PJ (2010) Disulfide bond that constrains the hiv-1 gp120 v3 domain is cleaved by thioredoxin. J Biol Chem 285(51):40072–40080PubMedCrossRefGoogle Scholar
  5. Bach RR (2006) Tissue factor encryption. Arterioscler Thromb Vasc Biol 26(3):456–461PubMedCrossRefGoogle Scholar
  6. 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(5):3131–3136PubMedCrossRefGoogle Scholar
  7. Begg GE, Carrington L, Stokes PH, Matthews JM, Wouters MA, Husain A, Lorand L, Iismaa SE, Graham RM (2006) Mechanism of allosteric regulation of transglutaminase 2 by gtp. Proc Natl Acad Sci USA 103(52):19683–19688PubMedCrossRefGoogle Scholar
  8. 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(1):235–242PubMedCrossRefGoogle Scholar
  9. Berndt C, Lillig CH, Holmgren A (2008) Thioredoxins and glutaredoxins as facilitators of protein folding. Biochim Biophys Acta 1783(4):641–650PubMedCrossRefGoogle Scholar
  10. Billington J, Hickling TP, Munro GH, Halai C, Chung R, Dodson GG, Daniels RS (2007) Stability of a receptor-binding active human immunodeficiency virus type 1 recombinant gp140 trimer conferred by intermonomer disulfide bonding of the v3 loop: Differential effects of protein disulfide isomerase on cd4 and coreceptor binding. J Virol 81(9):4604–4614PubMedCrossRefGoogle Scholar
  11. Bouma B, de Groot PG, van den Elsen JM, Ravelli RB, Schouten A, Simmelink MJ, Derksen RH, Kroon J, Gros P (1999) Adhesion mechanism of human beta(2)-glycoprotein i to phospholipids based on its crystal structure. EMBO J 18(19):5166–5174PubMedCrossRefGoogle Scholar
  12. Bourgeois R, Mercier J, Paquette-Brooks I, Cohen EA (2006) Association between disruption of cd4 receptor dimerization and increased human immunodeficiency virus type 1 entry. Retrovirology 3:31PubMedCrossRefGoogle Scholar
  13. Brooks DJ, Fresco JR (2002) Increased frequency of cysteine, tyrosine, and phenylalanine residues since the last universal ancestor. Mol Cell Proteomics 1(2):125–131PubMedCrossRefGoogle Scholar
  14. Brooks DJ, Fresco JR, Lesk AM, Singh M (2002) Evolution of amino acid frequencies in proteins over deep time: Inferred order of introduction of amino acids into the genetic code. Mol Biol Evol 19(10):1645–1655PubMedGoogle Scholar
  15. Brooks DJ, Fresco JR, Singh M (2004) A novel method for estimating ancestral amino acid ­composition and its application to proteins of the last universal ancestor. Bioinformatics 20(14):2251–2257PubMedCrossRefGoogle Scholar
  16. Carroll SB (2001) Chance and necessity: The evolution of morphological complexity and diversity. Nature 409(6823):1102–1109PubMedCrossRefGoogle Scholar
  17. Chen VM, Ahamed J, Versteeg HH, Berndt MC, Ruf W, Hogg PJ (2006) Evidence for activation of tissue factor by an allosteric disulfide bond. Biochemistry 45(39):12020–12028PubMedCrossRefGoogle Scholar
  18. Chen VM, Hogg PJ (2006) Allosteric disulfide bonds in thrombosis and thrombolysis. J Thromb Haemost 4(12):2533–2541PubMedCrossRefGoogle Scholar
  19. Cho J, Furie BC, Coughlin SR, Furie B (2008) A critical role for extracellular protein disulfide isomerase during thrombus formation in mice. J Clin Invest 118(3):1123–1131PubMedGoogle Scholar
  20. Choi H, Aboulfatova K, Pownall HJ, Cook R, Dong JF (2007) Shear-induced disulfide bond formation regulates adhesion activity of von willebrand factor. J Biol Chem 282(49):35604–35611PubMedCrossRefGoogle Scholar
  21. Chung SI, Folk JE (1970) Mechanism of the inactivation of guinea pig liver transglutaminase by tetrathionate. J Biol Chem 245(4):681–689PubMedGoogle Scholar
  22. Collet JF, Riemer J, Bader MW, Bardwell JC (2002) Reconstitution of a disulfide isomerization system. J Biol Chem 277(30):26886–26892PubMedCrossRefGoogle Scholar
  23. Connellan JM, Folk JE (1969) Mechanism of the inactivation of guinea pig liver transglutaminase by 5,5’-dithiobis-(2-nitrobenzoic acid). J Biol Chem 244(12):3173–3181PubMedGoogle Scholar
  24. Einfeld D (1996) Maturation and assembly of retroviral glycoproteins. Curr Top Microbiol Immunol 214:133–176PubMedGoogle Scholar
  25. Essex DW (2008) Redox control of platelet function. Antioxidants & redox signaling 11(5):1191–1225Google Scholar
  26. Fernandes PA, Ramos MJ (2004) Theoretical insights into the mechanism for thiol/disulfide exchange. Chemistry (Weinheim an der Bergstrasse, Germany) 10 (1):257–266Google Scholar
  27. Fischer A, Montal M (2007) Crucial role of the disulfide bridge between botulinum neurotoxin light and heavy chains in protease translocation across membranes. J Biol Chem 282(40):29604–29611PubMedCrossRefGoogle Scholar
  28. Furie B, Furie BC (2008) Mechanisms of thrombus formation. N Engl J Med 359(9):938–949PubMedCrossRefGoogle Scholar
  29. Fyhrquist F, Saijonmaa O (2008) Renin-angiotensin system revisited. J Intern Med 264(3):224–236PubMedCrossRefGoogle Scholar
  30. Gallina A, Hanley TM, Mandel R, Trahey M, Broder CC, Viglianti GA, Ryser HJ (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(52):50579–50588PubMedCrossRefGoogle Scholar
  31. Gallo SA, Finnegan CM, Viard M, Raviv Y, Dimitrov A, Rawat SS, Puri A, Durell S, Blumenthal R (2003) The hiv env-mediated fusion reaction. Biochim Biophys Acta 1614(1):36–50PubMedCrossRefGoogle Scholar
  32. Garrett TP, Wang J, Yan Y, Liu J, Harrison SC (1993) Refinement and analysis of the structure of the first two domains of human cd4. J Mol Biol 234(3):763–778PubMedCrossRefGoogle Scholar
  33. Giannakopoulos B, Passam F, Ioannou Y, Krilis SA (2009) How we diagnose the antiphospholipid syndrome. Blood 113(5):985–994PubMedCrossRefGoogle Scholar
  34. Gonnet GH, Cohen MA, Benner SA (1992) Exhaustive matching of the entire protein sequence database. Science 256(5062):1443–1445PubMedCrossRefGoogle Scholar
  35. Gonzalez S, Groh V, Spies T (2006) Immunobiology of human nkg2d and its ligands. Curr Top Microbiol Immunol 298:121–138PubMedCrossRefGoogle Scholar
  36. Gopalan G, He Z, Balmer Y, Romano P, Gupta R, Heroux A, Buchanan BB, Swaminathan K, Luan S (2004) Structural analysis uncovers a role for redox in regulating fkbp13, an immunophilin of the chloroplast thylakoid lumen. Proc Natl Acad Sci USA 101(38):13945–13950PubMedCrossRefGoogle Scholar
  37. Griffin M, Casadio R, Bergamini CM (2002) Transglutaminases: Nature’s biological glues. Biochem J 368(Pt 2):377–396PubMedCrossRefGoogle Scholar
  38. Grimshaw JP, Stirnimann CU, Brozzo MS, Malojcic G, Grutter MG, Capitani G, Glockshuber R (2008) Dsbl and dsbi form a specific dithiol oxidase system for periplasmic arylsulfate sulfotransferase in uropathogenic escherichia coli. J Mol Biol 380(4):667–680PubMedCrossRefGoogle Scholar
  39. Groh V, Bahram S, Bauer S, Herman A, Beauchamp M, Spies T (1996) Cell stress-regulated human major histocompatibility complex class i gene expressed in gastrointestinal epithelium. Proc Natl Acad Sci USA 93(22):12445–12450PubMedCrossRefGoogle Scholar
  40. Groh V, Rhinehart R, Secrist H, Bauer S, Grabstein KH, Spies T (1999) Broad tumor-associated expression and recognition by tumor-derived gamma delta t cells of mica and micb. Proc Natl Acad Sci USA 96(12):6879–6884PubMedCrossRefGoogle Scholar
  41. Hedges SB, Dudley J, Kumar S (2006) Timetree: A public knowledge-base of divergence times among organisms. Bioinformatics 22(23):2971–2972PubMedCrossRefGoogle Scholar
  42. Hogg PJ (2003) Disulfide bonds as switches for protein function. Trends Biochem Sci 28(4):210–214PubMedCrossRefGoogle Scholar
  43. Hogg PJ (2009) Contribution of allosteric disulfide bonds to regulation of hemostasis. J Thromb Haemost 7(Suppl 1):13–16PubMedCrossRefGoogle Scholar
  44. Huang CC, Stricher F, Martin L, Decker JM, Majeed S, Barthe P, Hendrickson WA, Robinson J, Roumestand C, Sodroski J, Wyatt R, Shaw GM, Vita C, Kwong PD (2005) Scorpion-toxin mimics of cd4 in complex with human immunodeficiency virus gp120 crystal structures, molecular mimicry, and neutralization breadth. Structure 13(5):755–768PubMedCrossRefGoogle Scholar
  45. Hubbard TJ, Murzin AG, Brenner SE, Chothia C (1997) Scop: A structural classification of proteins database. Nucleic Acids Res 25(1):236–239PubMedCrossRefGoogle Scholar
  46. Hurvitz JR, Suwairi WM, Van Hul W, El-Shanti H, Superti-Furga A, Roudier J, Holderbaum D, Pauli RM, Herd JK, Van Hul EV, Rezai-Delui H, Legius E, Le Merrer M, Al-Alami J, Bahabri SA, Warman ML (1999) Mutations in the ccn gene family member wisp3 cause progressive pseudorheumatoid dysplasia. Nat Genet 23(1):94–98PubMedCrossRefGoogle Scholar
  47. Ioannou Y, Zhang J-Y, Passam FH, Rahgozar S, Qi JC, Giannakopoulos B, Yu MQP, Yu DM, Hogg PJ, Krilis SA (2010) Naturally occurring free thiols within ß2-glycoprotein i in vivo: Nitrosylation, redox modification by endothelial cells and regulation of oxidative stress induced cell injury. Blood:in pressGoogle Scholar
  48. Jacob-Dubuisson F, Pinkner J, Xu Z, Striker R, Padmanhaban A, Hultgren SJ (1994) Papd chaperone function in pilus biogenesis depends on oxidant and chaperone-like activities of dsba. Proc Natl Acad Sci USA 91(24):11552–11556PubMedCrossRefGoogle Scholar
  49. Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8(3):275–282PubMedGoogle Scholar
  50. Jordan IK, Kondrashov FA, Adzhubei IA, Wolf YI, Koonin EV, Kondrashov AS, Sunyaev S (2005) A universal trend of amino acid gain and loss in protein evolution. Nature 433(7026):633–638PubMedCrossRefGoogle Scholar
  51. Kaiser BK, Yim D, Chow IT, Gonzalez S, Dai Z, Mann HH, Strong RK, Groh V, Spies T (2007) Disulphide-isomerase-enabled shedding of tumour-associated nkg2d ligands. Nature 447(7143):482–486PubMedCrossRefGoogle Scholar
  52. Klipcan L, Safro M (2004) Amino acid biogenesis, evolution of the genetic code and aminoacyl-trna synthetases. J Theor Biol 228(3):389–396PubMedCrossRefGoogle Scholar
  53. Krause G, Lundstrom J, Barea JL, Pueyo de la Cuesta C, Holmgren A (1991) Mimicking the active site of protein disulfide-isomerase by substitution of proline 34 in escherichia coli thioredoxin. J Biol Chem 266(15):9494–9500PubMedGoogle Scholar
  54. Kreisberg R, Buchner V, Arad D (1995) Paired natural cysteine mutation mapping: Aid to constraining models of protein tertiary structure. Protein Sci 4(11):2405–2410PubMedCrossRefGoogle Scholar
  55. Lai TS, Liu Y, Tucker T, Daniel KR, Sane DC, Toone E, Burke JR, Strittmatter WJ, Greenberg CS (2008) Identification of chemical inhibitors to human tissue transglutaminase by screening existing drug libraries. Chem Biol 15(9):969–978PubMedCrossRefGoogle Scholar
  56. Le DT, Rapaport SI, Rao LV (1992) Relations between factor viia binding and expression of factor viia/tissue factor catalytic activity on cell surfaces. J Biol Chem 267(22):15447–15454PubMedGoogle Scholar
  57. Lester WA, Guilliatt AM, Enayat MS, Rose P, Hill FG (2007) The r2464c missense mutation in the von willebrand factor gene causes a novel abnormality of multimer electrophoretic mobility and falls into the subgroup of type 2 von willebrand disease “unclassified”. Thromb Haemost 97(1):159–160PubMedGoogle Scholar
  58. Li P, Morris DL, Willcox BE, Steinle A, Spies T, Strong RK (2001) Complex structure of the activating immunoreceptor nkg2d and its mhc class i-like ligand mica. Nat Immunol 2(5):443–451PubMedGoogle Scholar
  59. Li P, Willie ST, Bauer S, Morris DL, Spies T, Strong RK (1999) Crystal structure of the mhc class i homolog mic-a, a gammadelta t cell ligand. Immunity 10(5):577–584PubMedCrossRefGoogle Scholar
  60. Liang HP, Hogg PJ (2008) Critical importance of the cell system when studying tissue factor ­de-encryption. Blood 112 (3):912–913; author reply 913Google Scholar
  61. Liu J, Bartesaghi A, Borgnia MJ, Sapiro G, Subramaniam S (2008) Molecular architecture of native hiv-1 gp120 trimers. Nature 455(7209):109–113PubMedCrossRefGoogle Scholar
  62. Lundstrom J, Holmgren A (1993) Determination of the reduction-oxidation potential of the thioredoxin-like domains of protein disulfide-isomerase from the equilibrium with glutathione and thioredoxin. Biochemistry 32(26):6649–6655PubMedCrossRefGoogle Scholar
  63. Maekawa A, Schmidt B, de St F, Groth B, Sanejouand YH, Hogg PJ (2006) Evidence for a domain-swapped cd4 dimer as the coreceptor for binding to class ii mhc. J Immunol 176(11):6873–6878PubMedGoogle Scholar
  64. Malojcic G, Owen RL, Grimshaw JP, Brozzo MS, Dreher-Teo H, Glockshuber R (2008) A structural and biochemical basis for paps-independent sulfuryl transfer by aryl sulfotransferase from uropathogenic escherichia coli. Proc Natl Acad Sci USA 105(49):19217–19222PubMedCrossRefGoogle Scholar
  65. Markovic I, Stantchev TS, Fields KH, Tiffany LJ, Tomic M, Weiss CD, Broder CC, Strebel K, Clouse KA (2004) Thiol/disulfide exchange is a prerequisite for cxcr4-tropic hiv-1 envelope-mediated t-cell fusion during viral entry. Blood 103(5):1586–1594PubMedCrossRefGoogle Scholar
  66. Matthias LJ, Azimi I, Tabrett CA, Hogg PJ (2010) Reduced monomeric cd4 is the preferred receptor for hiv. J Biol Chem 285(52):40793–40799PubMedCrossRefGoogle Scholar
  67. Matthias LJ, Yam PT, 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-1. Nat Immunol 3(8):727–732PubMedGoogle Scholar
  68. Miller SL (1953) A production of amino acids under possible primitive earth conditions. Science 117(3046):528–529PubMedCrossRefGoogle Scholar
  69. Miller SL (1987) Which organic compounds could have occurred on the prebiotic earth? Cold Spring Harb Symp Quant Biol 52:17–27PubMedGoogle Scholar
  70. Mills JE, Whitford PC, Shaffer J, Onuchic JN, Adams JA, Jennings PA (2007) A novel disulfide bond in the sh2 domain of the c-terminal src kinase controls catalytic activity. J Mol Biol 365(5):1460–1468PubMedCrossRefGoogle Scholar
  71. Miyakis S, Giannakopoulos B, Krilis SA (2004) Beta 2 glycoprotein i–function in health and disease. Thromb Res 114(5–6):335–346PubMedCrossRefGoogle Scholar
  72. Montal M (2010) Botulinum neurotoxin: A marvel of protein design. Annu Rev Biochem 79:591–617Google Scholar
  73. Muller YA, Ultsch MH, de Vos AM (1996) The crystal structure of the extracellular domain of human tissue factor refined to 1.7 a resolution. J Mol Biol 256(1):144–159PubMedCrossRefGoogle Scholar
  74. 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(4):536–540PubMedGoogle Scholar
  75. Ogawa A, Takayama Y, Sakai H, Chong KT, Takeuchi S, Nakagawa A, Nada S, Okada M, Tsukihara T (2002) Structure of the carboxyl-terminal src kinase, csk. J Biol Chem 277(17):14351–14354PubMedCrossRefGoogle Scholar
  76. Ostergaard H, Henriksen A, Hansen FG, Winther JR (2001) Shedding light on disulfide bond formation: Engineering a redox switch in green fluorescent protein. EMBO J 20(21):5853–5862PubMedCrossRefGoogle Scholar
  77. Ou W, Silver J (2006) Role of protein disulfide isomerase and other thiol-reactive proteins in hiv-1 envelope protein-mediated fusion. Virology 350(2):406–417PubMedCrossRefGoogle Scholar
  78. Passam FH, Rahgozar S, Qi M, Raftery MJ, Wong JWH, Tanaka K, Ioannou Y, Zhang JY, Gemmell R, Qi JC, Giannakopoulos B, Hughes WE, Hogg PJ, Krilis SA (2010a) Redox control of β2gpi-von willebrand factor interaction by thioredoxin-1. J Thromb Haemost 8(8):1754–1762Google Scholar
  79. Passam FH, Rahgozar S, Qi M, Raftery MJ, Wong JWH, Tanaka K, Ioannou Y, Zhang JY, Gemmell R, Qi JC, Hughes WE, Hogg PJ, Krilis SA (2010b) Beta 2 glycoprotein i is a substrate of thiol oxidoreductases. Blood 116(11):1995–1997Google Scholar
  80. Pendurthi UR, Ghosh S, Mandal SK, Rao LV (2007) Tissue factor activation: Is disulfide bond switching a regulatory mechanism? Blood 110(12):3900–3908PubMedCrossRefGoogle Scholar
  81. Persson E (2008) Protein disulfide isomerase has no stimulatory chaperone effect on factor x activation by factor viia-soluble tissue factor. Thrombosis Res 123(1):171–176CrossRefGoogle Scholar
  82. Piatek R, Zalewska B, Kolaj O, Ferens M, Nowicki B, Kur J (2005) Molecular aspects of biogenesis of escherichia coli dr fimbriae: Characterization of drab-drae complexes. Infect Immun 73(1):135–145PubMedCrossRefGoogle Scholar
  83. Pinkas DM, Strop P, Brunger AT, Khosla C (2007) Transglutaminase 2 undergoes a large conformational change upon activation. PLoS Biol 5(12):e327PubMedCrossRefGoogle Scholar
  84. Ploplis VA, Edgington TS, Fair DS (1987) Initiation of the extrinsic pathway of coagulation. Association of factor viia with a cell line expressing tissue factor. J Biol Chem 262(20):9503–9508PubMedGoogle Scholar
  85. Reinhardt C, von Bruhl ML, Manukyan D, Grahl L, Lorenz M, Altmann B, Dlugai S, Hess S, Konrad I, Orschiedt L, Mackman N, Ruddock L, Massberg S, Engelmann B (2008) Protein disulfide isomerase acts as an injury response signal that enhances fibrin generation via tissue factor activation. J Clin Invest 118(3):1110–1122PubMedGoogle Scholar
  86. Richardson J, Richardson D (1989) Prediction of protein structure and the principles of protein conformation. Plenum Press, New YorkGoogle Scholar
  87. Rozhkova A, Glockshuber R (2008) Thermodynamic aspects of dsbd-mediated electron transport. J Mol Biol 380(5):783–788PubMedCrossRefGoogle Scholar
  88. Rubinstein R, Fiser A (2008) Predicting disulfide bond connectivity in proteins by correlated mutations analysis. Bioinformatics 24(4):498–504PubMedCrossRefGoogle Scholar
  89. Ryser HJ, Levy EM, Mandel R, DiSciullo GJ (1994) Inhibition of human immunodeficiency virus infection by agents that interfere with thiol-disulfide interchange upon virus-receptor interaction. Proc Natl Acad Sci USA 91(10):4559–4563PubMedCrossRefGoogle Scholar
  90. Sakai T, Lund-Hansen T, Paborsky L, Pedersen AH, Kisiel W (1989) Binding of human factors vii and viia to a human bladder carcinoma cell line (j82). Implications for the initiation of the extrinsic pathway of blood coagulation. J Biol Chem 264(17):9980–9988PubMedGoogle Scholar
  91. Sanejouand YH (2004) Domain swapping of cd4 upon dimerization. Proteins 57(1):205–212PubMedCrossRefGoogle Scholar
  92. Sauer FG, Pinkner JS, Waksman G, Hultgren SJ (2002) Chaperone priming of pilus subunits facilitates a topological transition that drives fiber formation. Cell 111(4):543–551PubMedCrossRefGoogle Scholar
  93. Schmidt B, Ho L, Hogg PJ (2006) Allosteric disulfide bonds. Biochemistry 45(24):7429–7433PubMedCrossRefGoogle Scholar
  94. Schmidt B, Hogg PJ (2007) Search for allosteric disulfide bonds in nmr structures. BMC Struct Biol 7:49PubMedCrossRefGoogle Scholar
  95. Schwarzenbacher R, Zeth K, Diederichs K, Gries A, Kostner GM, Laggner P, Prassl R (1999) Crystal structure of human beta2-glycoprotein i: Implications for phospholipid binding and the antiphospholipid syndrome. EMBO J 18(22):6228–6239PubMedCrossRefGoogle Scholar
  96. Schwertassek U, Balmer Y, Gutscher M, Weingarten L, Preuss M, Engelhard J, Winkler M, Dick TP (2007) Selective redox regulation of cytokine receptor signaling by extracellular thioredoxin-1. EMBO J 26(13):3086–3097PubMedCrossRefGoogle Scholar
  97. Siegel M, Khosla C (2007) Transglutaminase 2 inhibitors and their therapeutic role in disease states. Pharmacol Ther 115(2):232–245PubMedCrossRefGoogle Scholar
  98. Swaminathan S, Eswaramoorthy S (2000) Structural analysis of the catalytic and binding sites of clostridium botulinum neurotoxin b. Nat Struct Biol 7(8):693–699PubMedCrossRefGoogle Scholar
  99. Thornton JM (1981) Disulphide bridges in globular proteins. J Mol Biol 151(2):261–287PubMedCrossRefGoogle Scholar
  100. Versteeg HH, Ruf W (2007) Tissue factor coagulant function is enhanced by protein-disulfide isomerase independent of oxidoreductase activity. J Biol Chem 282(35):25416–25424PubMedCrossRefGoogle Scholar
  101. Wiita AP, Perez-Jimenez R, Walther KA, Grater F, Berne BJ, Holmgren A, Sanchez-Ruiz JM, Fernandez JM (2007) Probing the chemistry of thioredoxin catalysis with force. Nature 450(7166):124–127PubMedCrossRefGoogle Scholar
  102. Wong JWH, Ho SYW, Hogg PJ (2011) Disulfide bond acquisition through eukaryotic protein evolution. Mol Biol Evol 28(1):327–334Google Scholar
  103. Wouters MA, Lau KK, Hogg PJ (2004) Cross-strand disulphides in cell entry proteins: Poised to act. Bioessays 26(1):73–79PubMedCrossRefGoogle Scholar
  104. Zav’yalov VP, Chernovskaya TV, Chapman DA, Karlyshev AV, MacIntyre S, Zavialov AV, Vasiliev AM, Denesyuk AI, Zav’yalova GA, Dudich IV, Korpela T, Abramov VM (1997) Influence of the conserved disulphide bond, exposed to the putative binding pocket, on the structure and function of the immunoglobulin-like molecular chaperone caf1m of yersinia pestis. Biochem J 324(Pt 2):571–578PubMedGoogle Scholar
  105. Zhang J (2007) Disulfide-bond reshuffling in the evolution of an ape placental ribonuclease. Mol Biol Evol 24(2):505–512PubMedCrossRefGoogle Scholar
  106. Zhang JL, Huang Y, Qiu LY, Nickel J, Sebald W (2007) Von willebrand factor type c domain-containing proteins regulate bone morphogenetic protein signaling through different recognition mechanisms. J Biol Chem 282(27):20002–20014PubMedCrossRefGoogle Scholar
  107. Zhang JL, Qiu LY, Kotzsch A, Weidauer S, Patterson L, Hammerschmidt M, Sebald W, Mueller TD (2008) Crystal structure analysis reveals how the chordin family member crossveinless 2 blocks bmp-2 receptor binding. Developmental Cell 14(5):739–750PubMedCrossRefGoogle Scholar
  108. Zhou A, Carrell RW, Murphy MP, Wei Z, Yan Y, Stanley PL, Stein PE, Broughton Pipkin F, Read RJ (2010) A redox switch in angiotensinogen modulates angiotensin release. Nature 468(7320):108–111PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  1. 1.Lowy Cancer Research Centre, Prince of Wales Clinical SchoolUniversity of New South WalesSydneyAustralia

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