Protein action in nature is largely controlled by the level of expression and by post-translational modifications. Post-translational modifications result in a proteome that is at least two orders of magnitude more diverse than the genome. There are three basic types of post-translational modifications: covalent modification of an amino acid side chain, hydrolytic cleavage or isomerization of a peptide bond, and reductive cleavage of a disulfide bond. This review addresses the modification of disulfide bonds. Protein disulfide bonds perform either a structural or a functional role, and there are two types of functional disulfide: the catalytic and allosteric bonds. The allosteric disulfide bonds control the function of the mature protein in which they reside by triggering a change when they are cleaved. The change can be in ligand binding, substrate hydrolysis, proteolysis, or oligomer formation. The allosteric disulfides are cleaved by oxidoreductases or by thiol/disulfide exchange, and the configurations of the disulfides and the secondary structures that they link share some recurring features. How these bonds are being identified using bioinformatics and experimental screens and what the future holds for this field of research are also discussed. Antioxid. Redox Signal. 18, 1987–2015.
AguzziA, HeikenwalderM. Pathogenesis of prion diseases: current status and future outlook. Nat Rev Microbiol, 4:765–775. 2006.
2.
AmboH, KamataT, HandaM, TakiM, KuwajimaM, KawaiY, OdaA, MurataM, TakadaY, WatanabeK, IkedaY. Three novel integrin beta3 subunit missense mutations (H280P, C560F, and G579S) in thrombasthenia, including one (H280P) prevalent in Japanese patients. Biochem Biophys Res Commun, 251:763–768. 1998.
3.
AndersonDH, SawayaMR, CascioD, ErnstW, ModlinR, KrenskyA, EisenbergD. Granulysin crystal structure and a structure-derived lytic mechanism. J Mol Biol, 325:355–365. 2003.
4.
AnderssonM, HolmgrenA, SpyrouG. NK-lysin, a disulfide-containing effector peptide of T-lymphocytes, is reduced and inactivated by human thioredoxin reductase - implication for a protective mechanism against NK-lysin cytotoxicity. J Biol Chem, 271:10116–10120. 1996.
AuwerxJ, IsacssonO, SoderlundJ, BalzariniJ, JohanssonM, LundbergM. 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, 41:1269–1275. 2009.
7.
AzimiI, MatthiasLJ, CenterRJ, WongJW, HoggPJ. Disulfide bond that constrains the HIV-1 gp120 V3 domain is cleaved by thioredoxin. J Biol Chem, 285:40072–40080. 2010.
8.
AzimiI, WongJW, HoggPJ. Control of mature protein function by allosteric disulfide bonds. Antioxid Redox Signal, 14:113–126. 2011.
9.
BabaH, SueyoshiN, ShigeriY, IshidaA, KameshitaI. Regulation of Ca(2+)/calmodulin-dependent protein kinase phosphatase (CaMKP) by oxidation/reduction at Cys-359. Arch Biochem Biophys, 526:9–15. 2012.
10.
BaldusIB, GraterF. Mechanical force can fine-tune redox potentials of disulfide bonds. Biophys J, 102:622–629. 2012.
11.
BarboucheR, MiquelisR, JonesIM, FenouilletE. 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. 2003.
12.
BargA, OssigR, GoergeT, SchneiderMF, SchillersH, OberleithnerH, SchneiderSW. Soluble plasma-derived von Willebrand factor assembles to a haemostatically active filamentous network. Thromb Haemost, 97:514–526. 2007.
13.
BauerF, SchweimerK, KluverE, Conejo-GarciaJR, ForssmannWG, RoschP, AdermannK, StichtH. Structure determination of human and murine beta-defensins reveals structural conservation in the absence of significant sequence similarity. Protein Sci, 10:2470–2479. 2001.
14.
BeggGE, CarringtonL, StokesPH, MatthewsJM, WoutersMA, HusainA, LorandL, IismaaSE, GrahamRM. Mechanism of allosteric regulation of transglutaminase 2 by GTP. Proc Natl Acad Sci U S A, 103:19683–19688. 2006.
15.
BernardoA, BallC, NolascoL, ChoiH, MoakeJL, DongJF. Platelets adhered to endothelial cell-bound ultra-large von Willebrand factor strings support leukocyte tethering and rolling under high shear stress. J Thromb Haemost, 3:562–570. 2005.
16.
BerndtC, LilligCH, HolmgrenA. Thioredoxins and glutaredoxins as facilitators of protein folding. Biochim Biophys Acta, 1783:641–650. 2008.
17.
Bjorkhem-BergmanL, Jonsson-VidesaterK, PaulC, BjornstedtM, AnderssonM. Mammalian thioredoxin reductase alters cytolytic activity of an antibacterial peptide. Peptides, 25:1849–1855. 2004.
18.
BootheRL, FolkJE. A reversible, calcium-dependent, copper-catalyzed inactivation of guinea pig liver transglutaminase. J Biol Chem, 244:399–405. 1969.
19.
BoumaB, de GrootPG, van den ElsenJM, RavelliRB, SchoutenA, SimmelinkMJ, DerksenRH, KroonJ, GrosP. Adhesion mechanism of human beta(2)-glycoprotein I to phospholipids based on its crystal structure. Embo J, 18:5166–5174. 1999.
20.
BourgeoisR, MercierJ, Paquette-BrooksI, CohenEA. Association between disruption of CD4 receptor dimerization and increased human immunodeficiency virus type 1 entry. Retrovirology, 3:31. 2006.
21.
BraakmanI, BulleidNJ. Protein folding and modification in the mammalian endoplasmic reticulum. Ann Rev Biochem, 80:71–99. 2011.
22.
BrooksDJ, FrescoJR, LeskAM, SinghM. Evolution of amino acid frequencies in proteins over deep time: inferred order of introduction of amino acids into the genetic code. Mol Biol Evol, 19:1645–1655. 2002.
Burke-GaffneyA, CallisterMEJ, NakamuraH. Thioredoxin: friend or foe in human disease?Trends Pharmacol Sci, 26:398–404. 2005.
25.
ButtaN, Arias-SalgadoEG, Gonzalez-ManchonC, FerrerM, LarruceaS, AyusoMS, ParrillaR. Disruption of the beta3 663–687 disulfide bridge confers constitutive activity to beta3 integrins. Blood, 102:2491–2497. 2003.
26.
CaoZ, TavenderTJ, RoszakAW, CogdellRJ, BulleidNJ. Crystal structure of reduced and of oxidized peroxiredoxin IV enzyme reveals a stable oxidized decamer and a non-disulfide-bonded intermediate in the catalytic cycle. J Biol Chem, 286:42257–42266. 2011.
ChenJ, RehemanA, GushikenFC, NolascoL, FuX, MoakeJL, NiH, LopezJA. N-acetylcysteine reduces the size and activity of von Willebrand factor in human plasma and mice. J Clin Invest, 121:593–603. 2011.
29.
ChenP, MelchiorC, BronsNH, SchlegelN, CaenJ, KiefferN. Probing conformational changes in the I-like domain and the cysteine-rich repeat of human beta 3 integrins following disulfide bond disruption by cysteine mutations: identification of cysteine 598 involved in alphaIIbbeta3 activation. J Biol Chem, 276:38628–38635. 2001.
30.
ChiversPT, RainesRT. General acid/base catalysis in the active site of Escherichia coli thioredoxin. Biochemistry, 36:15810–15816. 1997.
31.
ChoiH, AboulfatovaK, PownallHJ, CookR, DongJF. Shear-induced disulfide bond formation regulates adhesion activity of von Willebrand factor. J Biol Chem, 282:35604–35611. 2007.
32.
ChungSI, FolkJE. Mechanism of the inactivation of guinea pig liver transglutaminase by tetrathionate. J Biol Chem, 245:681–689. 1970.
33.
ConnellanJM, FolkJE. Mechanism of the inactivation of guinea pig liver transglutaminase by 5,5′-dithiobis-(2-nitrobenzoic acid)J Biol Chem, 244:3173–3181. 1969.
CuneoMJ, LondonRE. Oxidation state of the XRCC1 N-terminal domain regulates DNA polymerase beta binding affinity. Proc Natl Acad Sci U S A, 107:6805–6810. 2010.
36.
CurboS, GaudinR, CarlstenM, MalmbergKJ, Troye-BlombergM, AhlborgN, KarlssonA, JohanssonM, LundbergM. Regulation of interleukin-4 signaling by extracellular reduction of intramolecular disulfides. Biochem Biophys Res Commun, 390:1272–1277. 2009.
37.
DalyEB, WindT, JiangXM, SunL, HoggPJ. Secretion of phosphoglycerate kinase from tumour cells is controlled by oxygen-sensing hydroxylases. Biochim Biophys Acta, 1691:17–22. 2004.
38.
DavydovaN, StreltsovVA, RoufailS, LovreczGO, StackerSA, AdamsTE, AchenMG. Preparation of human vascular endothelial growth factor-D for structural and preclinical therapeutic studies. Protein Expr Purif, 82:232–239. 2012.
39.
DepuydtM, MessensJ, ColletJF. How proteins form disulfide bonds. Antioxid Redox Signal, 15:49–66. 2011.
40.
DieterichW, EhnisT, BauerM, DonnerP, VoltaU, RieckenEO, SchuppanD. Identification of tissue transglutaminase as the autoantigen of celiac disease. Nat Med, 3:797–801. 1997.
41.
EisenhardtSU, HabersbergerJ, MurphyA, ChenYC, WoollardKJ, BasslerN, QianH, von Zur MuhlenC, HagemeyerCE, AhrensI, Chin-DustingJ, BobikA, PeterK. Dissociation of pentameric to monomeric C-reactive protein on activated platelets localizes inflammation to atherosclerotic plaques. Circ Res, 105:128–137. 2009.
42.
EisenhardtSU, HabersbergerJ, PeterK. Monomeric C-reactive protein generation on activated platelets: the missing link between inflammation and atherothrombotic risk. Trends Cardiovasc Med, 19:232–237. 2009.
43.
EricsonML, HorlingJ, Wendel-HansenV, HolmgrenA, RosenA. Secretion of thioredoxin after in vitro activation of human B cells. Lymphokine Cytokine Res, 11:201–207. 1992.
44.
EssexDW, LiM. Redox control of platelet aggregation. Biochemistry, 42:129–136. 2003.
45.
EssexDW, LiM, MillerA, FeinmanRD. Protein disulfide isomerase and sulfhydryl-dependent pathways in platelet activation. Biochemistry, 40:6070–6075. 2001.
46.
FanSW, GeorgeRA, HaworthNL, FengLL, LiuJY, WoutersMA. Conformational changes in redox pairs of protein structures. Protein Sci, 18:1745–1765. 2009.
47.
FernandesPA, RamosMJ. Theoretical insights into the mechanism for thiol/disulfide exchange. Chemistry, 10:257–266. 2004.
48.
FischerA, MontalM. Crucial role of the disulfide bridge between botulinum neurotoxin light and heavy chains in protease translocation across membranes. J Biol Chem, 282:29604–29611. 2007.
49.
GallinaA, HanleyTM, MandelR, TraheyM, BroderCC, VigliantiGA, RyserHJ. 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. 2002.
50.
GandertonT, BerndtMC, ChestermanCN, HoggPJ. Hypothesis for control of von Willebrand factor multimer size by intra-molecular thiol-disulphide exchange. J Thromb Haemost, 5:204–206. 2007.
51.
GandertonT, WongJW, SchroederC, HoggPJ. Lateral self-association of VWF involves the Cys2431-Cys2453 disulfide/dithiol in the C2 domain. Blood, 118:5312–5318. 2011.
52.
GarrettTP, WangJ, YanY, LiuJ, HarrisonSC. Refinement and analysis of the structure of the first two domains of human CD4. J Mol Biol, 234:763–778. 1993.
53.
GiannakopoulosB, GaoL, QiM, WongJW, YuDM, VlachoyiannopoulosPG, MoutsopoulosHM, AtsumiT, KoikeT, HoggPJ, QiJC, KrilisSA. Factor XI is a substrate for oxidoreductases: enhanced activation of reduced FXI and its role in antiphospholipid syndrome thrombosis. J Autoimmun, 39:121–129. 2012.
54.
GiannakopoulosB, PassamF, IoannouY, KrilisSA. How we diagnose the antiphospholipid syndrome. Blood, 113:985–994. 2009.
55.
GoEP, ZhangY, MenonS, DesaireH. Analysis of the disulfide bond arrangement of the HIV-1 envelope protein CON-S gp140 DeltaCFI shows variability in the V1 and V2 regions. J Proteome Res, 10:578–591. 2011.
56.
GonzalezS, GrohV, SpiesT. Immunobiology of human NKG2D and its ligands. Curr Top Microbiol Immunol, 298:121–138. 2006.
57.
GopalanG, HeZ, BalmerY, RomanoP, GuptaR, HerouxA, BuchananBB, SwaminathanK, LuanS. Structural analysis uncovers a role for redox in regulating FKBP13, an immunophilin of the chloroplast thylakoid lumen. Proc Natl Acad Sci U S A, 101:13945–13950. 2004.
58.
GrimaldiCM, ChenF, ScudderLE, CollerBS, FrenchDL. A Cys374Tyr homozygous mutation of platelet glycoprotein IIIa (beta 3) in a Chinese patient with Glanzmann's thrombasthenia. Blood, 88:1666–1675. 1996.
59.
GrimshawJP, StirnimannCU, BrozzoMS, MalojcicG, GrutterMG, CapitaniG, GlockshuberR. DsbL and DsbI form a specific dithiol oxidase system for periplasmic arylsulfate sulfotransferase in uropathogenic Escherichia coli. J Mol Biol, 380:667–680. 2008.
60.
GrohV, BahramS, BauerS, HermanA, BeauchampM, SpiesT. Cell stress-regulated human major histocompatibility complex class I gene expressed in gastrointestinal epithelium. Proc Natl Acad Sci U S A, 93:12445–12450. 1996.
61.
GrohV, RhinehartR, SecristH, BauerS, GrabsteinKH, SpiesT. Broad tumor-associated expression and recognition by tumor-derived gamma delta T cells of MICA and MICB. Proc Natl Acad Sci U S A, 96:6879–6884. 1999.
62.
GrossoH, MouradianMM. Transglutaminase 2: biology, relevance to neurodegenerative diseases and therapeutic implications. Pharmacol Ther, 133:392–410. 2012.
63.
HanBG, ChoJW, ChoYD, JeongKC, KimSY, LeeBI. Crystal structure of human transglutaminase 2 in complex with adenosine triphosphate. Int J Biol Macromol, 47:190–195. 2010.
64.
HansenRE, OstergaardH, WintherJR. Increasing the reactivity of an artifical dithiol - disulfide pair through modification of the electrostatic milieu. Biochemistry, 44:5899–5906. 2005.
65.
HaraN, BadruzzamanM, SugaeT, ShimoyamaM, TsuchiyaM. Mouse Rt6.1 is a thiol-dependent arginine-specific ADP-ribosyltransferase - Cysteine 201 confers thiol sensitivity on the enzyme. Eur J Biochem, 259:289–294. 1999.
66.
HaraN, TerashimaM, ShimoyamaM, TsuchiyaM. Mouse T-cell antigen Rt6.1 has thiol-dependent NAD glycohydrolase activity. J Biochem, 128:601–607. 2000.
67.
HarderJ, GlaserR, SchroderJM. Human antimicrobial proteins effectors of innate immunity. J Endotoxin Res, 13:317–338. 2007.
68.
HaworthNL, FengLL, WoutersMA. High torsional energy disulfides: relationship between cross-strand disulfides and right-handed staples. J Bioinform Comput Biol, 4:155–168. 2006.
69.
HoggPJ. Disulfide bonds as switches for protein function. Trends Biochem Sci, 28:210–214. 2003.
70.
HongS, BrassA, SemanM, HaagF, Koch-NolteF, DubyakGR. Lipopolysaccharide, IFN-gamma, and IFN-beta induce expression of the thiol-sensitive ART2.1 Ecto-ADP-ribosyltransferase in murine macrophages. J Immunol, 179:6215–6227. 2007.
71.
HongS, BrassA, SemanM, HaagF, Koch-NolteF, DubyakGR. Basal and inducible expression of the thiol-sensitive ART2.1 ecto-ADP-ribosyltransferase in myeloid and lymphoid leukocytes. Purinergic Signal, 5:369–383. 2009.
72.
HooverDM, ChertovO, LubkowskiJ. The structure of human beta-defensin-1: new insights into structural properties of beta-defensins. J Biol Chem, 276:39021–39026. 2001.
73.
HotchkissKA, ChestermanCN, HoggPJ. Catalysis of disulfide isomerization in thrombospondin 1 by protein disulfide isomerase. Biochemistry, 35:9761–9767. 1996.
74.
Huber-WunderlichM, GlockshuberR. A single dipeptide sequence modulates the redox properties of a whole enzyme family. Folding Des, 3:161–171. 1998.
IoannouY, ZhangJY, PassamFH, RahgozarS, QiJC, GiannakopoulosB, QiM, YuP, YuDM, HoggPJ, KrilisSA. Naturally occurring free thiols within beta 2-glycoprotein I in vivo: nitrosylation, redox modification by endothelial cells, and regulation of oxidative stress-induced cell injury. Blood, 116:1961–1970. 2010.
77.
IoannouY, ZhangJY, QiM, GaoL, QiJC, YuDM, LauH, SturgessAD, VlachoyiannopoulosPG, MoutsopoulosHM, RahmanA, PericleousC, AtsumiT, KoikeT, HeritierS, GiannakopoulosB, KrilisSA. Novel assays of thrombogenic pathogenicity in the antiphospholipid syndrome based on the detection of molecular oxidative modification of the major autoantigen beta2-glycoprotein I. Arthritis Rheum, 63:2774–2782. 2011.
78.
JiS-R, MaL, BaiC-J, ShiJ-M, LiH-Y, PotempaLA, FilepJG, ZhaoJ, WuY. Monomeric C-reactive protein activates endothelial cells via interaction with lipid raft microdomains. FASEB J, 23:1806–1816. 2009.
79.
JiSR, WuY, ZhuL, PotempaLA, ShengFL, LuW, ZhaoJ. Cell membranes and liposomes dissociate C-reactive protein (CRP) to form a new, biologically active structural intermediate: mCRP(m)FASEB J, 21:284–294. 2007.
80.
JikimotoT, NishikuboY, KoshibaM, KanagawaS, MorinobuS, MorinobuA, SauraR, MizunoK, KondoS, ToyokuniS, NakamuraH, YodoiJ, KumagaiS. Thioredoxin as a biomarker for oxidative stress in patients with rheumatoid arthritis. Mol Immunol, 38:765–772. 2002.
81.
JinX, StamnaesJ, KlockC, DiRaimondoTR, SollidLM, KhoslaC. Activation of extracellular transglutaminase 2 by thioredoxin. J Biol Chem, 286:37866–37873. 2011.
82.
JordanIK, KondrashovFA, AdzhubeiIA, WolfYI, KooninEV, KondrashovAS, SunyaevS. A universal trend of amino acid gain and loss in protein evolution. Nature, 433:633–638. 2005.
KamataT, AmboH, Puzon-McLaughlinW, TieuKK, HandaM, IkedaY, TakadaY. Critical cysteine residues for regulation of integrin alphaIIbbeta3 are clustered in the epidermal growth factor domains of the beta3 subunit. Biochem J, 378:1079–1082. 2004.
85.
KassamG, KwonM, YoonCS, GrahamKS, YoungMK, GluckS, WaismanDM. Purification and characterization of A61. An angiostatin-like plasminogen fragment produced by plasmin autodigestion in the absence of sulfhydryl donors. J Biol Chem, 276:8924–8933. 2001.
86.
KerkD, TempletonG, MoorheadGB. Evolutionary radiation pattern of novel protein phosphatases revealed by analysis of protein data from the completely sequenced genomes of humans, green algae, and higher plants. Plant Physiol, 146:351–367. 2008.
87.
KhreissT, JozsefL, PotempaLA, FilepJG. Conformational rearrangement in C-reactive protein is required for proinflammatory actions on human endothelial cells. Circulation, 109:2016–2022. 2004.
88.
KhreissT, JozsefL, PotempaLA, FilepJG. Loss of pentameric symmetry in C-reactive protein induces interleukin-8 secretion through peroxynitrite signaling in human neutrophils. Circ Res, 97:690–697. 2005.
89.
KraichM, KleinM, PatinoE, HarrerH, NickelJ, SebaldW, MuellerTD. A modular interface of IL-4 allows for scalable affinity without affecting specificity for the IL-4 receptor. BMC Biol, 4:13. 2006.
90.
KrauseG, LundstromJ, BareaJL, Pueyo de la CuestaC, HolmgrenA. Mimicking the active site of protein disulfide-isomerase by substitution of proline 34 in Escherichia coli thioredoxin. J Biol Chem, 266:9494–9500. 1991.
91.
KwonM, CaplanJF, FilipenkoNR, ChoiKS, FitzpatrickSL, ZhangL, WaismanDM. Identification of annexin II heterotetramer as a plasmin reductase. J Biol Chem, 277:10903–10911. 2002.
92.
LackmanRL, JamiesonAM, GriffithJM, GeuzeH, CresswellP. Innate immune recognition triggers secretion of lysosomal enzymes by macrophages. Traffic, 8:1179–1189. 2007.
93.
LahavJ, Gofer-DadoshN, LuboshitzJ, HessO, ShaklaiM. Protein disulfide isomerase mediates integrin-dependent adhesion. FEBS Lett, 475:89–92. 2000.
LahavJ, WijnenEM, HessO, HamaiaSW, GriffithsD, MakrisM, KnightCG, EssexDW, FarndaleRW. Enzymatically catalyzed disulfide exchange is required for platelet adhesion to collagen via integrin alpha2beta1. Blood, 102:2085–2092. 2003.
96.
LaPorteSL, JuoZS, VaclavikovaJ, ColfLA, QiX, HellerNM, KeeganAD, GarciaKC. Molecular and structural basis of cytokine receptor pleiotropy in the interleukin-4/13 system. Cell, 132:259–272. 2008.
97.
LaragioneT, BonettoV, CasoniF, MassignanT, BianchiG, GianazzaE, GhezziP. Redox regulation of surface protein thiols: identification of integrin alpha-4 as a molecular target by using redox proteomics. Proc Natl Acad Sci U S A, 100:14737–14741. 2003.
98.
LawRHP, Caradoc-DaviesT, CowiesonN, HorvathAJ, QuekAJ, EncarnacaoJA, SteerD, CowanA, ZhangQ, LuBGC, PikeRN, SmithAI, CoughlinPB, WhisstockJC. The X-ray crystal structure of full-length human plasminogen. J Thromb Haemost, 10:E23–E23. 2012.
99.
LayAJ, HoggPJ. Measurement of reduction of disulfide bonds in plasmin by phosphoglycerate kinase. Methods Enzymol, 348:87–92. 2002.
100.
LayAJ, JiangX-M, KiskerO, FlynnE, UnderwoodA, CondronR, HoggPJ. Phosphoglycerate kinase acts in tumour angiogenesis as a disulphide reductase. Nature, 408:869–873. 2000.
101.
LayAJ, JiangXM, DalyE, SunL, HoggPJ. Plasmin reduction by phosphoglycerate kinase is a thiol-independent process. J Biol Chem, 277:9062–9068. 2002.
102.
LemarechalH, AllanoreY, Chenevier-GobeauxC, EkindjianOG, KahanA, BorderieD. High redox thioredoxin but low thioredoxin reductase activities in the serum of patients with rheumatoid arthritis. Clin Chim Acta, 367:156–161. 2006.
103.
LemarechalH, AnractP, BeaudeuxJL, Bonnefont-RousselotD, EkindjianOG, BorderieD. Impairment of thioredoxin reductase activity by oxidative stress in human rheumatoid synoviocytes. Free Radic Res, 41:688–698. 2007.
LeppanenVM, ProtaAE, JeltschM, AnisimovA, KalkkinenN, StrandinT, LankinenH, GoldmanA, Ballmer-HoferK, AlitaloK. Structural determinants of growth factor binding and specificity by VEGF receptor 2. Proc Natl Acad Sci U S A, 107:2425–2430. 2010.
106.
LiP, MorrisDL, WillcoxBE, SteinleA, SpiesT, StrongRK. Complex structure of the activating immunoreceptor NKG2D and its MHC class I-like ligand MICA. Nat Immunol, 2:443–451. 2001.
107.
LiPW, WillieST, BauerS, MorrisDL, SpiesT, StrongRK. Crystal structure of the MHC class I homolog MIC-A, a gamma delta T cell ligand. Immunity, 10:577–584. 1999.
108.
LiY, ChoiH, ZhouZ, NolascoL, PownallHJ, VoorbergJ, MoakeJL, DongJF. Covalent regulation of ULVWF string formation and elongation on endothelial cells under flow conditions. J Thromb Haemost, 6:1135–1143. 2008.
109.
LijnenHR. Elements of the fibrinolytic system. Ann N Y Acad Sci, 936:226–236. 2001.
110.
LiuS, CerioneRA, ClardyJ. Structural basis for the guanine nucleotide-binding activity of tissue transglutaminase and its regulation of transamidation activity. Proc Natl Acad Sci U S A, 99:2743–2747. 2002.
111.
LohelaM, BryM, TammelaT, AlitaloK. VEGFs and receptors involved in angiogenesis versus lymphangiogenesis. Curr Opin Cell Biol, 21:154–165. 2009.
112.
Lopez-OtinC, HunterT. The regulatory crosstalk between kinases and proteases in cancer. Nat Rev Cancer, 10:278–292. 2010.
113.
LukenBM, WinnLY, EmsleyJ, LaneDA, CrawleyJT. The importance of vicinal cysteines, C1669 and C1670, for von Willebrand factor A2 domain function. Blood, 115:4910–4913. 2010.
114.
LummisSC, BeeneDL, LeeLW, LesterHA, BroadhurstRW, DoughertyDA. Cis-trans isomerization at a proline opens the pore of a neurotransmitter-gated ion channel. Nature, 438:248–252. 2005.
115.
MaekawaA, SchmidtB, Fazekas de St GrothB, SanejouandYH, HoggPJ. Evidence for a domain-swapped CD4 dimer as the coreceptor for binding to class II MHC. J Immunol, 176:6873–6878. 2006.
116.
MalojcicG, OwenRL, GrimshawJP, BrozzoMS, Dreher-TeoH, GlockshuberR. A structural and biochemical basis for PAPS-independent sulfuryl transfer by aryl sulfotransferase from uropathogenic Escherichia coli. Proc Natl Acad Sci U S A, 105:19217–19222. 2008.
117.
ManickamN, AhmadSS, EssexDW. Vicinal thiols are required for activation of the αIIbβ3 platelet integrin. J Thromb Haemost, 9:1207–1215. 2011.
118.
ManickamN, SunX, HakalaKW, WeintraubST, EssexDW. Thiols in the alphaIIbbeta3 integrin are necessary for platelet aggregation. Br J Haematol, 142:457–465. 2008.
119.
MarkovicI, StantchevTS, FieldsKH, TiffanyLJ, TomicM, WeissCD, BroderCC, StrebelK, ClouseKA. Thiol/disulfide exchange is a prerequisite for CXCR4-tropic HIV-1 envelope-mediated T-cell fusion during viral entry. Blood, 103:1586–1594. 2004.
120.
MartinG, BurkeB, ThaiR, DeyAK, CombesO, RamosOH, HeydB, GeonnottiAR, MontefioriDC, KanE, LianY, SunY, AbacheT, UlmerJB, MadaouiH, GueroisR, BarnettSW, SrivastavaIK, KesslerP, MartinL. Stabilization of HIV-1 envelope in the CD4-bound conformation through specific cross-linking of a CD4 mimetic. J Biol Chem, 286:21706–21716. 2011.
121.
MatthiasLJ, AzimiI, TabrettCA, HoggPJ. Reduced monomeric CD4 is the preferred receptor for HIV. J Biol Chem, 285:40793–40799. 2010.
122.
MatthiasLJ, YamPT, JiangXM, VandegraaffN, LiP, PoumbouriosP, DonoghueN, HoggPJ. Disulfide exchange in domain 2 of CD4 is required for entry of HIV-1. Nat Immunol, 3:727–732. 2002.
123.
MauriceMM, NakamuraH, GringhuisS, OkamotoT, YoshidaS, KullmannF, LechnerS, van der VoortEA, LeowA, VersendaalJ, Muller-LadnerU, YodoiJ, TakPP, BreedveldFC, VerweijCL. Expression of the thioredoxin-thioredoxin reductase system in the inflamed joints of patients with rheumatoid arthritis. Arthritis Rheum, 42:2430–2439. 1999.
124.
McGarrigleSA, O'NeillS, WalshGM, MoranN, GrahamIM, CooneyM-T, MonavariA, MayneP, CollinsP. Integrin αIIbβ3 exists in an activated state in subjects with elevated plasma homocysteine levels. Platelets, 22:63–71. 2011.
125.
McKinnonTA, GoodeEC, BirdseyGM, NowakAA, ChanAC, LaneDA, LaffanMA. Specific N-linked glycosylation sites modulate synthesis and secretion of von Willebrand factor. Blood, 116:640–648. 2010.
126.
MetcalfeC, CresswellP, BarclayAN. Interleukin-2 signalling is modulated by a labile disulfide bond in the CD132 chain of its receptor. Open Biol, 2:110036. 2012.
127.
MetcalfeC, CresswellP, CiacciaL, ThomasB, BarclayAN. Labile disulfide bonds are common at the leucocyte cell surface. Open Biol, 1:110010. 2011.
128.
MikolajekH, KolstoeSE, PyeVE, MangioneP, PepysMB, WoodSP. Structural basis of ligand specificity in the human pentraxins, C-reactive protein and serum amyloid P component. J Mol Recognit, 24:371–377. 2011.
129.
Milet-MarsalS, BreillatC, PeyruchaudO, NurdenP, CombrieR, NurdenA, BourreF. Two different beta3 cysteine substitutions alter alphaIIb beta3 maturation and result in Glanzmann thrombasthenia. Thromb Haemost, 88:104–110. 2002.
130.
MillsJE, WhitfordPC, ShafferJ, OnuchicJN, AdamsJA, JenningsPA. A novel disulfide bond in the SH2 Domain of the C-terminal Src kinase controls catalytic activity. J Mol Biol, 365:1460–1468. 2007.
131.
MiyakisS, GiannakopoulosB, KrilisSA. Beta 2 glycoprotein I—function in health and disease. Thromb Res, 114:335–346. 2004.
132.
MolinsB, PenaE, VilahurG, MendietaC, SlevinM, BadimonL. C-reactive protein isoforms differ in their effects on thrombus growth. Arterioscler Thromb Vasc Bio, 28:2239–2246. 2008.
133.
MonodJ, WymanJ, ChangeuxJP. On the nature of allosteric transitions: a plausible model. J Mol Biol, 12:88–118. 1965.
134.
MontalM. Botulinum neurotoxin: a marvel of protein design. Ann Rev Biochem, 79:591–617. 2010.
135.
MoorheadGB, Trinkle-MulcahyL, Ulke-LemeeA. Emerging roles of nuclear protein phosphatases. Nat Rev Mol Cell Biol, 8:234–244. 2007.
136.
Mor-CohenR, RosenbergN, EinavY, ZelzionE, LandauM, MansourW, AverbukhY, SeligsohnU. Unique disulfide bonds in epidermal growth factor (EGF) domains of beta3 affect structure and function of alphaIIbbeta3 and alphavbeta3 integrins in different manner. J Biol Chem, 287:8879–8891. 2012.
137.
Mor-CohenR, RosenbergN, LandauM, LahavJ, SeligsohnU. Specific cysteines in beta3 are involved in disulfide bond exchange-dependent and -independent activation of alphaIIbbeta3. J Biol Chem, 283:19235–19244. 2008.
138.
Mor-CohenR, RosenbergN, PeretzH, LandauM, CollerBS, AwidiA, SeligsohnU. Disulfide bond disruption by a beta 3-Cys549Arg mutation in six Jordanian families with Glanzmann thrombasthenia causes diminished production of constitutively active alpha IIb beta 3. Thromb Haemost, 98:1257–1265. 2007.
139.
Mueller-DieckmannC, RitterH, HaagF, Koch-NolteF, SchulzGE. Structure of the ecto-ADP-ribosyl transferase ART2.2 from rat. J Mol Biol, 322:687–696. 2002.
140.
MugfordSG, LeeBR, KoprivovaA, MatthewmanC, KoprivaS. Control of sulfur partitioning between primary and secondary metabolism. Plant J, 65:96–105. 2011.
141.
Mulligan-KehoeMJ, WagnerR, WielandC, PowellR. A truncated plasminogen activator inhibitor-1 protein induces and inhibits angiostatin (kringles 1–3), a plasminogen cleavage product. J Biol Chem, 276:8588–8596. 2001.
142.
NadeauPJ, CharetteSJ, LandryJ. REDOX reaction at ASK1-Cys250 is essential for activation of JNK and induction of apoptosis. Mol Biol Cell, 20:3628–3637. 2009.
143.
NadeauPJ, CharetteSJ, ToledanoMB, LandryJ. Disulfide Bond-mediated multimerization of Ask1 and its reduction by thioredoxin-1 regulate H(2)O(2)-induced c-Jun NH(2)-terminal kinase activation and apoptosis. Mol Biol Cell, 18:3903–3913. 2007.
144.
NairS, LiJ, MitchellWB, MohantyD, CollerBS, FrenchDL. Two new beta3 integrin mutations in Indian patients with Glanzmann thrombasthenia: localization of mutations affecting cysteine residues in integrin beta3. Thromb Haemost, 88:503–509. 2002.
145.
NakamotoH, BardwellJC. Catalysis of disulfide bond formation and isomerization in the Escherichia coli periplasm. Biochim Biophys Acta, 1694:111–119. 2004.
146.
NelsonEJ, NairSC, PeretzH, CollerBS, SeligsohnU, ChandyM, SrivastavaA. Diversity of Glanzmann thrombasthenia in southern India: 10 novel mutations identified among 15 unrelated patients. J Thromb Haemost, 4:1730–1737. 2006.
147.
NiH, LiA, SimonsenN, WilkinsJA. Integrin activation by dithiothreitol or Mn2+ induces a ligand-occupied conformation and exposure of a novel NH2-terminal regulatory site on the beta1 integrin chain. J Biol Chem, 273:7981–7987. 1998.
148.
NiemelaJE, PuckJM, FischerRE, FleisherTA, HsuAP. Efficient detection of thirty-seven new IL2RG mutations in human X-linked severe combined immunodeficiency. Clin Immunol, 95:33–38. 2000.
149.
NiliusB, OwsianikG. The transient receptor potential family of ion channels. Genome Biol, 12:218. 2011.
150.
NolanSM, MathewEC, ScarthSL, Al-ShamkhaniA, LawSK. The effects of cysteine to alanine mutations of CD18 on the expression and adhesion of the CD11/CD18 integrins. FEBS Lett, 486:89–92. 2000.
151.
O'NeillS, RobinsonA, DeeringA, RyanM, FitzgeraldDJ, MoranN. The platelet integrin alpha IIbbeta 3 has an endogenous thiol isomerase activity. J Biol Chem, 275:36984–36990. 2000.
152.
O'ReillyMS, HolmgrenL, ShingY, ChenC, RosenthalRA, MosesM, LaneWS, CaoY, SageEH, FolkmanJ. Angiostatin: a novel angiogenesis inhibitor that mediates the suppression of metastases by a Lewis lung carcinoma. Cell, 79:315–328. 1994.
OloszF, MalekTR. Three loops of the common gamma chain ectodomain required for the binding of interleukin-2 and interleukin-7. J Biol Chem, 275:30100–30105. 2000.
155.
OuW, SilverJ. Role of protein disulfide isomerase and other thiol-reactive proteins in HIV-1 envelope protein-mediated fusion. Virology, 350:406–417. 2006.
156.
PassamFH, RahgozarS, QiM, RafteryMJ, WongJW, TanakaK, IoannouY, ZhangJY, GemmellR, QiJC, GiannakopoulosB, HughesWE, HoggPJ, KrilisSA. Beta 2 glycoprotein I is a substrate of thiol oxidoreductases. Blood, 116:1995–1997. 2010.
157.
PassamFH, RahgozarS, QiM, RafteryMJ, WongJW, TanakaK, IoannouY, ZhangJY, GemmellR, QiJC, GiannakopoulosB, HughesWE, HoggPJ, KrilisSA. Redox control of beta2-glycoprotein I-von Willebrand factor interaction by thioredoxin-1. J Thromb Haemost, 8:1754–1762. 2010.
158.
PinkasDM, StropP, BrungerAT, KhoslaC. Transglutaminase 2 Undergoes a Large Conformational Change upon Activation. PLoS Biol, 5:e327. 2007.
159.
PowersR, GarrettDS, MarchCJ, FriedenEA, GronenbornAM, CloreGM. Three-dimensional solution structure of human interleukin-4 by multidimensional heteronuclear magnetic resonance spectroscopy. Science, 256:1673–1677. 1992.
160.
PowersR, GarrettDS, MarchCJ, FriedenEA, GronenbornAM, CloreGM. The high-resolution, three-dimensional solution structure of human interleukin-4 determined by multidimensional heteronuclear magnetic resonance spectroscopy. Biochemistry, 32:6744–6762. 1993.
161.
PuckJM, de Saint BasileG, SchwarzK, FugmannS, FischerRE. IL2RGbase: a database of γc-chain defects causing human X-SCID. Immunol Today, 17:507–511. 1996.
162.
RaviliousGE, NguyenA, FrancoisJA, JezJM. Structural basis and evolution of redox regulation in plant adenosine-5′-phosphosulfate kinase. Proc Natl Acad Sci U S A, 109:309–314. 2012.
163.
RedfieldC, SmithLJ, BoydJ, LawrenceGM, EdwardsRG, GershaterCJ, SmithRA, DobsonCM. Analysis of the solution structure of human interleukin-4 determined by heteronuclear three-dimensional nuclear magnetic resonance techniques. J Mol Biol, 238:23–41. 1994.
164.
ReiserK, FrancoisKO, ScholsD, BergmanT, JornvallH, BalzariniJ, KarlssonA, LundbergM. Thioredoxin-1 and protein disulfide isomerase catalyze the reduction of similar disulfides in HIV gp120. Int J Biochem Cell Biol, 44:556–562. 2012.
165.
RitterH, Koch-NolteF, MarquezVE, SchulzGE. Substrate binding and catalysis of ecto-ADP-ribosyltransferase 2.2 from rat. Biochemistry, 42:10155–10162. 2003.
166.
RuanJ, SchmuggeM, ClemetsonKJ, CazesE, CombrieR, BourreF, NurdenAT. Homozygous Cys542—>Arg substitution in GPIIIa in a Swiss patient with type I Glanzmann's thrombasthenia. Br J Haematol, 105:523–531. 1999.
167.
RubartelliA, BajettoA, AllavenaG, WollmanE, SitiaR. Secretion of thioredoxin by normal and neoplastic-cells through a leaderless secretory pathway. J Biol Chem, 267:24161–24164. 1992.
168.
RuizC, LiuCY, SunQH, Sigaud-FiksM, FressinaudE, MullerJY, NurdenP, NurdenAT, NewmanPJ, ValentinN. A point mutation in the cysteine-rich domain of glycoprotein (GP) IIIa results in the expression of a GPIIb-IIIa (alphaIIbbeta3) integrin receptor locked in a high-affinity state and a Glanzmann thrombasthenia-like phenotype. Blood, 98:2432–2441. 2001.
169.
RyserHJ, LevyEM, MandelR, DiSciulloGJ. Inhibition of human immunodeficiency virus infection by agents that interfere with thiol-disulfide interchange upon virus-receptor interaction. Proc Natl Acad Sci U S A, 91:4559–4563. 1994.
170.
SadlerJE. Biochemistry and genetics of von willebrand factor. Ann Rev Biochem, 67:395–424. 1998.
171.
SadlerJE. von Willebrand factor assembly and secretion. J Thromb Haemost, 7:24–27. 2009.
172.
SanejouandYH. Domain swapping of CD4 upon dimerization. Proteins, 57:205–212. 2004.
173.
SavageB, SixmaJJ, RuggeriZM. Functional self-association of von Willebrand factor during platelet adhesion under flow. Proc Natl Acad Sci U S A, 99:425–430. 2002.
SchmidtB, HoggPJ. Search for allosteric disulfide bonds in NMR structures. BMC Struct Biol, 7:49. 2007.
176.
SchneiderSW, NuscheleS, WixforthA, GorzelannyC, Alexander-KatzA, NetzRR, SchneiderMF. Shear-induced unfolding triggers adhesion of von Willebrand factor fibers. Proc Natl Acad Sci U S A, 104:7899–7903. 2007.
177.
SchroederBO, WuZ, NudingS, GroscurthS, MarcinowskiM, BeisnerJ, BuchnerJ, SchallerM, StangeEF, WehkampJ. Reduction of disulphide bonds unmasks potent antimicrobial activity of human beta-defensin 1. Nature, 469:419–423. 2011.
178.
SchwarzenbacherR, ZethK, DiederichsK, GriesA, KostnerGM, LaggnerP, PrasslR. Crystal structure of human beta2-glycoprotein I: implications for phospholipid binding and the antiphospholipid syndrome. Embo J, 18:6228–6239. 1999.
179.
SchwedlerSB, AmannK, WernickeK, KrebsA, NauckM, WannerC, PotempaLA, GalleJ. Native C-reactive protein increases whereas modified C-reactive protein reduces atherosclerosis in apolipoprotein E-knockout mice. Circulation, 112:1016–1023. 2005.
ScudieroO, GaldieroS, CantisaniM, Di NotoR, VitielloM, GaldieroM, NaclerioG, CassimanJJ, PedoneC, CastaldoG, SalvatoreF. Novel synthetic, salt-resistant analogs of human beta-defensins 1 and 3 endowed with enhanced antimicrobial activity. Antimicrob Agents Chemother, 54:2312–2322. 2010.
182.
SiedleckiCA, LestiniBJ, Kottke-MarchantKK, EppellSJ, WilsonDL, MarchantRE. Shear-dependent changes in the three-dimensional structure of human von Willebrand factor. Blood, 88:2939–2950. 1996.
183.
SiegelM, StrnadP, WattsRE, ChoiK, JabriB, OmaryMB, KhoslaC. Extracellular transglutaminase 2 is catalytically inactive, but is transiently activated upon tissue injury. PLoS One, 3:e1861. 2008.
184.
SmithLJ, RedfieldC, BoydJ, LawrenceGM, EdwardsRG, SmithRA, DobsonCM. Human interleukin 4. The solution structure of a four-helix bundle protein. J Mol Biol, 224:899–904. 1992.
StathakisP, FitzgeraldM, MatthiasLJ, ChestermanCN, HoggPJ. Generation of angiostatin by reduction and proteolysis of plasmin. Catalysis by a plasmin reductase secreted by cultured cells. J Biol Chem, 272:20641–20645. 1997.
187.
StathakisP, LayAJ, FitzgeraldM, SchliekerC, MatthiasLJ, HoggPJ. Angiostatin formation involves disulfide bond reduction and proteolysis in kringle 5 of plasmin. J Biol Chem, 274:8910–8916. 1999.
188.
StauberDJ, DeblerEW, HortonPA, SmithKA, WilsonIA. Crystal structure of the IL-2 signaling complex: paradigm for a heterotrimeric cytokine receptor. Proc Natl Acad Sci U S A, 103:2788–2793. 2006.
189.
SteppichDM, AngererJI, SritharanK, SchneiderSW, ThalhammerS, WixforthA, Alexander-KatzA, SchneiderMF. Relaxation of ultralarge VWF bundles in a microfluidic-AFM hybrid reactor. Biochem Biophys Res Commun, 369:507–512. 2008.
190.
SunQH, LiuCY, WangR, PaddockC, NewmanPJ. Disruption of the long-range GPIIIa Cys(5)-Cys(435) disulfide bond results in the production of constitutively active GPIIb-IIIa (alpha(IIb)beta(3)) integrin complexes. Blood, 100:2094–2101. 2002.
191.
SwaminathanS, EswaramoorthyS. Structural analysis of the catalytic and binding sites of Clostridium botulinum neurotoxin B. Nat Struct Biol, 7:693–699. 2000.
192.
SwiatkowskaM, SzymanskiJ, PadulaG, CierniewskiCS. Interaction and functional association of protein disulfide isomerase with alphaVbeta3 integrin on endothelial cells. Febs J, 275:1813–1823. 2008.
193.
TagayaY, MaedaY, MitsuiA, KondoN, MatsuiH, HamuroJ, BrownN, AraiK, YokotaT, WakasugiHet al.ATL-derived factor (ADF), an IL-2 receptor/Tac inducer homologous to thioredoxin; possible involvement of dithiol-reduction in the IL-2 receptor induction. Embo J, 8:757–764. 1989.
194.
TakahashiH, ShinY, ChoSJ, ZagoWM, NakamuraT, GuZ, MaY, FurukawaH, LiddingtonR, ZhangD, TongG, ChenHS, LiptonSA. Hypoxia enhances S-nitrosylation-mediated NMDA receptor inhibition via a thiol oxygen sensor motif. Neuron, 53:53–64. 2007.
UlrichtsH, VanhoorelbekeK, GirmaJP, LentingPJ, VauterinS, DeckmynH. The von Willebrand factor self-association is modulated by a multiple domain interaction. J Thromb Haemost, 3:552–561. 2005.
197.
VanderlelieJ, VenardosK, CliftonVL, GudeNM, ClarkeFM, PerkinsAV. Increased biological oxidation and reduced anti-oxidant enzyme activity in pre-eclamptic placentae. Placenta, 26:53–58. 2005.
198.
WakasugiN, TagayaY, WakasugiH, MitsuiA, MaedaM, YodoiJ, TurszT. Adult T-cell leukemia-derived factor/thioredoxin, produced by both human T-lymphotropic virus type I- and Epstein-Barr virus-transformed lymphocytes, acts as an autocrine growth factor and synergizes with interleukin 1 and interleukin 2. Proc Natl Acad Sci, 87:8282–8286. 1990.
199.
WaldmannTA. The biology of interleukin-2 and interleukin-15: implications for cancer therapy and vaccine design. Nat Rev Immunol, 6:595–601. 2006.
200.
WalshCT. Posttranslational Modification of Proteins: Expanding Nature's Inventory. Roberts & Company: Greenwood Village, Colorado, 2006.
201.
WalshGM, SheehanD, KinsellaA, MoranN, O'NeillS. Redox modulation of integrin [correction of integin] alpha IIb beta 3 involves a novel allosteric regulation of its thiol isomerase activity. Biochemistry, 43:473–480. 2004.
WangH, SchultzR, HongJ, CundiffDL, JiangK, SoffGA. Cell surface-dependent generation of angiostatin4.5. Cancer Res, 64:162–168. 2004.
204.
WangJ, WangJ, DaiJ, JungY, WeiCL, WangY, HavensAM, HoggPJ, KellerET, PientaKJ, NorJE, WangCY, TaichmanRS. A glycolytic mechanism regulating an angiogenic switch in prostate cancer. Cancer Res, 67:149–159. 2007.
205.
WangJ, YingG, JungY, LuJ, ZhuJ, PientaKJ, TaichmanRS. Characterization of phosphoglycerate kinase-1 expression of stromal cells derived from tumor microenvironment in prostate cancer progression. Cancer Res, 70:471–480. 2010.
206.
WangM-Y, JiS-R, BaiC-J, El KebirD, LiH-Y, ShiJ-M, ZhuW, CostantinoS, ZhouH-H, PotempaLA, ZhaoJ, FilepJG, WuY. A redox switch in C-reactive protein modulates activation of endothelial cells. FASEB J, 25:3186–3196. 2011.
207.
WangR, PetersonJ, AsterRH, NewmanPJ. Disruption of a long-range disulfide bond between residues Cys406 and Cys655 in glycoprotein IIIa does not affect the function of platelet glycoprotein IIb-IIIa. Blood, 90:1718–1719. 1997.
208.
WangX, RickertM, GarciaKC. Structure of the quaternary complex of interleukin-2 with its alpha, beta, and gammac receptors. Science, 310:1159–1163. 2005.
209.
WiitaAP, AinavarapuSR, HuangHH, FernandezJM. Force-dependent chemical kinetics of disulfide bond reduction observed with single-molecule techniques. Proc Natl Acad Sci U S A, 103:7222–7227. 2006.
210.
WiitaAP, Perez-JimenezR, WaltherKA, GraterF, BerneBJ, HolmgrenA, Sanchez-RuizJM, FernandezJM. Probing the chemistry of thioredoxin catalysis with force. Nature, 450:124–127. 2007.
211.
WlodaverA, PavlovskyA, GustchinaA. Crystal structure of human recombinant interleukin-4 at 2.25 Å resolution. FEBS Lett, 309:59–64. 1992.
212.
WongJW, HoSY, HoggPJ. Disulfide bond acquisition through eukaryotic protein evolution. Mol Biol Evol, 28:327–334. 2011.
213.
WoutersMA, LauKK, HoggPJ. Cross-strand disulphides in cell entry proteins: poised to act. Bioessays, 26:73–79. 2004.
214.
WuHL, ShiGY, BenderML. Preparation and purification of microplasmin. Proc Natl Acad Sci U S A, 84:8292–8295. 1987.
215.
WuHL, ShiGY, WohlRC, BenderML. Structure and formation of microplasmin. Proc Natl Acad Sci U S A, 84:8793–8795. 1987.
216.
XieL, ChestermanCN, HoggPJ. Control of von Willebrand factor multimer size by thrombospondin-1. J Exp Med, 193:1341–1349. 2001.
217.
XiongJP, MahalinghamB, AlonsoJL, BorrelliLA, RuiX, AnandS, HymanBT, RysiokT, Muller-PompallaD, GoodmanSL, ArnaoutMA. Crystal structure of the complete integrin alphaVbeta3 ectodomain plus an alpha/beta transmembrane fragment. J Cell Biol, 186:589–600. 2009.
YamamotoS, TakahashiN, MoriY. Chemical physiology of oxidative stress-activated TRPM2 and TRPC5 channels. Prog Biophys Mol Biol, 103:18–27. 2010.
220.
YanB, SmithJW. A redox site involved in integrin activation. J Biol Chem, 275:39964–39972. 2000.
221.
YanB, SmithJW. Mechanism of integrin activation by disulfide bond reduction. Biochemistry, 40:8861–8867. 2001.
222.
YehHC, ZhouZ, ChoiH, TekeogluS, MayW3rd, WangC, TurnerN, ScheiflingerF, MoakeJL, DongJF. Disulfide bond reduction of von Willebrand factor by ADAMTS-13. J Thromb Haemost, 8:2778–2788. 2010.
223.
YoshidaS, KatohT, TetsukaT, UnoK, MatsuiN, OkamotoT. Involvement of thioredoxin in rheumatoid arthritis: its costimulatory roles in the TNF-alpha-induced production of IL-6 and IL-8 from cultured synovial fibroblasts. J Immunol, 163:351–358. 1999.
224.
ZhangQ, ZhouYF, ZhangCZ, ZhangX, LuC, SpringerTA. Structural specializations of A2, a force-sensing domain in the ultralarge vascular protein von Willebrand factor. Proc Natl Acad Sci U S A, 106:9226–9231. 2009.
225.
ZhouA, CarrellRW, MurphyMP, WeiZ, YanY, StanleyPLD, SteinPE, PipkinFB, ReadRJ. A redox switch in angiotensinogen modulates angiotensin release. Nature, 468:108–111. 2010.
226.
ZhouL, JingY, StybloM, ChenZ, WaxmanS. Glutathione-S-transferase pi inhibits As2O3-induced apoptosis in lymphoma cells: involvement of hydrogen peroxide catabolism. Blood, 105:1198–1203. 2005.
227.
ZhuJ, LuoBH, BarthP, SchonbrunJ, BakerD, SpringerTA. The structure of a receptor with two associating transmembrane domains on the cell surface: integrin alphaIIbbeta3. Mol Cell, 34:234–249. 2009.
228.
ZhuJ, LuoBH, XiaoT, ZhangC, NishidaN, SpringerTA. Structure of a complete integrin ectodomain in a physiologic resting state and activation and deactivation by applied forces. Mol Cell, 32:849–861. 2008.
229.
ZiekerD, KonigsrainerI, TritschlerI, LofflerM, BeckertS, TraubF, NieseltK, BuhlerS, WellerM, GaedckeJ, TaichmanRS, NorthoffH, BrucherBL, KonigsrainerA. Phosphoglycerate kinase 1 a promoting enzyme for peritoneal dissemination in gastric cancer. Int J Cancer, 126:1513–1520. 2010.
230.
ZolkiewskaA. Ecto-ADP-ribose transferases: cell-surface response to local tissue injury. Physiology (Bethesda), 20:374–381. 2005.
