Novel role of protein disulfide isomerase in the regulation of NADPH oxidase activity: Pathophysiological implications in vascular diseases

Antioxidants and Redox Signaling

Volumn 10, Issue 6, 2008, Pages 1101-1113

  Laurindo, Francisco R M ^a   Fernandes, Denise C ^a   Amanso, Angélica M ^a   Lopes, Lucia R ^a   Santos, Célio X C ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN II; NITRIC OXIDE; PROTEIN DISULFIDE ISOMERASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4;

APOPTOSIS; CELL ADHESION; CELL MIGRATION; CELL PROLIFERATION; CYTOSOLIC FRACTION; ENDOPLASMIC RETICULUM; ENDOTHELIUM CELL; HUMAN; IMMUNOPRECIPITATION; NONHUMAN; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN INTERACTION; REVIEW; VASCULAR DISEASE; VASCULAR SMOOTH MUSCLE; WESTERN BLOTTING;

ENDOTHELIUM, VASCULAR; HUMANS; MUSCLE, SMOOTH, VASCULAR; NADPH OXIDASE; OXIDATION-REDUCTION; PROTEIN DISULFIDE-ISOMERASE; SIGNAL TRANSDUCTION; SULFHYDRYL COMPOUNDS; VASCULAR DISEASES;

EID: 41349119823     PISSN: 15230864     EISSN: None     Source Type: Journal    
DOI: 10.1089/ars.2007.2011     Document Type: Review

References (112)

1. Ahamed J, Versteeg HH, Kerver M, Chen VM, Mueller BM, Hogg PJ, and Ruf W. Disulfide isomerization switches tissue factor from coagulation to cell signaling. Proc Natl Acad Sci USA 103: 13932-13937, 2006.
2. Alanen HI, Salo KE, Pirneskoski A, and Ruddock LW. pH dependence of the peptide thiol-disulphide oxidase activity of six members of the human protein disulphide isomerase family. Antioxid Redox Signal 8: 283-291, 2006.
3. Alvarez B, Ferrer-Sueta G, Freeman BA, and Radi R. Kinetics of peroxynitrite reaction with amino acids and human serum albumin. J Biol Chem 274: 842-848, 1999.
4. Ambasta RK, Kumar P, Griendling KK, Schmidt HH, Busse R, and Brandes RP. Direct interaction of the novel Nox proteins with p22phox is required for the formation of a functionally active NADPH oxidase. J Biol Chem 279: 45935-45941, 2004.
5. Arrigo AP. Gene expression and the thiol redox state. Free Radical Biol Med 27: 936-944, 1999.
6. Atkin JD, Farg MA, Turner BJ, Tomas D, Lysaght JA, Nunan J, Rembach A, Nagley P, Beart PM, Cheema SS, and Horne MK. Induction of the unfolded protein response in familial amyotrophic lateral sclerosis and association of protein-disulfide isomerase with superoxide dismutase 1. J Biol Chem 281: 30152-30165, 2006.
7. Barbouche R, Miquelis R, Jones IM, and Fenouillet E. 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.
8. --forming NADPH oxidase solubilized from activated neutrophils. Biochim Biophys Acta 746: 40-47; 1983.
9. Bennett TA, Edwards BS, Sklar LA, and Rogelj S. Sulfhydryl regulation of L-selectin shedding: phenylarsine oxide promotes activation-independent L-selectin shedding from leukocytes. J Immunol 164: 4120-4129. 2000.
10. Bielski BHJ and Shiue GG. Oxygen Free Radicals and Tissue Damage, Ciba Foundation Symposium 65 (New Series), Excerpta Medica, New York, p. 43-56, 1979.
11. Brandes RP and Kreuzer J. Vascular NADPH oxidases: molecular mechanisms of activation. Cardiovasc Res 65: 16-27, 2005.
12. Burgess JK, Hotchkiss KA, Suter C, Dudman NP, Szollosi J, Chesterman CN, Chong BH, and Hogg PJ. Physical proximity and functional association of glycoprotein 1balpha and protein-disulfide isomerase on the platelet plasma membrane. J Biol Chem 275: 9758-9766, 2000.
13. Cabre F, Cascante M, and Canela EI. The molybdoenzymes xanthine oxidase and aldehyde oxidase contain fast- and slow-DTNB reacting sulphydryl groups. J Protein Chem 11: 547-551, 1992.
14. Carballal S, Radi R, Kirk MC, Barnes S, Freeman BA, and Alvarez B. Sulfenic acid formation in human serum albumin by hydrogen peroxide and peroxynitrite. Biochemistry 42: 9906-9914, 2003.
15. Catz SD, Johnson JL, and Babior BM. The C2A domain of JFC1 binds to 3′-phosphorylated phosphoinositides and directs plasma membrane association in living cells. Proc Natl Acad Sci USA 99: 11652-11657, 2002.
16. Cave AC, Brewer AC, Narayanapanicker A, Ray R, Grieve DJ, Walker S, and Shah AM. NADPH oxidases in cardiovascular health and disease. Antioxid Redox Signal 8: 691-728, 2006.
17. Clempus R and Griendling KK. Reactive oxygen signaling in vascular smooth muscle cells. Cardiovasc Res 71: 216-225, 2006.
18. Clissold PM and Bicknell R. The thioredoxin-like fold: hidden domains in protein disulfide isomerases and other chaperone proteins. Bioessays 25: 603-611, 2003.
19. 2 activates Nox4 through PLA2-dependent arachidonic acid production in adult cardiac fibroblasts. FEBS Lett 579: 2533-2540, 2005.
20. Cross AR. Inhibitors of the leukocyte superoxide generating oxidase: Mechanisms of action and methods for their elucidation. Free Radical Biol Med 8: 71-93, 1990.
21. Delom F, Mallet B, Carayon P, and Lejeune PJ. Role of extracellular molecular chaperones in the folding of oxidized proteins. Refolding of colloidal thyroglobulin by protein disulfide isomerase and immunoglobulin heavy chain-binding protein. J Biol Chem 276: 21337-21342, 2001.
22. Desjardins M. ER-mediated phagocytosis: a new membrane for new function. Nat Rev Immunol 3: 280-291, 2003.
23. Donoghue N, Yam, PTW, Jiang X-M, and Hogg PJ. Presence of closely spaced protein thiols on the surface of mammalian cells. Protein Sci 9: 2436-2445, 2000.
24. Doussiere J, Poinas A, Blais C, and Vignais PV. Phenylarsine oxide as an inhibitor of the activation of the neutrophil NADPH oxidase-identification of the beta subunit of the flavocytochrome b component of the NADPH oxidase as a target site for phenylarsine oxide by photoaffinity labeling and photoinactivation. Eur J Biochem 251: 649-658, 1998.
25. Djordjevic T, Pogrebniak A, BelAiba RS, Bonello S, Wotzlaw C, Acker H, Hess J, and Gorlach A. The expression of the NADPH oxidase subunit p22phox is regulated by a redox-sensitive pathway in endothelial cells. Free Radical Biol Med 38: 616-630, 2005.
26. Ellgaard L and Ruddock LW. The human protein disulphide isomerase family: substrate interactions and functional properties. EMBO Rep 6: 28-32, 2005.
27. Ellis RJ. Molecular chaperones: assisting assembly in addition to folding. Trends Biochem Sci 31: 395-401, 2006.
28. Eschenlauer SC and Page AP. The Caenorhabditis elegans ERp60 homolog protein disulfide isomerase-3 has disulfide isomerase and transglutaminase-like cross-linking activity and is involved in the maintenance of body morphology. J Biol Chem 278: 4227-4237, 2003.
29. Essex DW, Chen K, and Swiatkowska M. Localization of protein disulfide isomerase to the external surface of the platelet plasma membrane. Blood 86: 2168-2173, 1995.
30. Essex DW, Li M, Miller A, and Feinman RD. Protein disulfide isomerase and sulfhydryl-dependent pathways in platelet activation. Biochemistry 40: 6070-6075, 2001.
31. Ferrari DM and Soling HD. The protein disulphide-isomerase family: unravelling a string of folds. Biochem J 339: 1-10, 1999.
32. Fernandes DC, Wosniak J, Pescatore LA, Bertoline MA, Liberman M, Laurindo FR, and Santos CX. Analysis of DHE-derived oxidation products by HPLC in the assessment of superoxide production and NADPH oxidase activity in vascular systems. Am J Physiol Cell Physiol 292: C413-422, 2007.
33. Forman HJ, Fukuto JM, and Torres M. Redox signaling: thiol chemistry defines which reactive oxygen and nitrogen species can act as second messengers. Am J Physiol Cell Physiol 287: C246-C256, 2004.
34. Forster ML, Sivick K, Park YN, Arvan P, Lencer WI, and Tsai B. Protein disulfide isomerase-like proteins play opposing roles during retrotranslocation. J Cell Biol 173: 853-859, 2006.
35. Frand AR, Cuozzo JW, and Kaiser CA. Pathways for protein disulphide bond formation. Trends Cell Biol. 10: 203-210, 2000.
36. Fratelli M, Demol H, Puype M, Casagrande S, Eberini I, Salmona M, Bonetto V, Mengozzi M, Duffieux F, Miclet E, Bachi A, Vandekerckhove J, Gianazza E, and Ghezzi P. Identification by redox proteomics of glutathionylated proteins in oxidatively stressed human T lymphocytes. Proc Natl Acad Sci USA 99: 3505-3510, 2002.
37. Gallina A, Hanley TM, Mandel R, Trahey M, Broder CC, Viglianti GA, and Ryser HJ. 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.
38. 2-dependent activation of GCLC-ARE4 reporter occurs by mitogen-activated protein kinase pathways without oxidation of cellular glutathione or thioredoxin-1. J Biol Chem 279: 5837-5845, 2004.
39. Graven KK, Molvar C, Roncarati JS, Klahn BD, Lowrey S, and Farber HW. Identification of protein disulfide as endothelial hypoxic stress protein. Am J Physiol Lung Cell Mol Physiol 282: L996-L1003, 2002.
40. Griendling KK, Sorescu D, and Ushio-Fukai M. NAD(P)H oxidase: role in cardiovascular biology and disease. Circ Res 86: 494-501, 2000.
41. Gross E, Sevier CS, Heldman N, Vitu E, Bentzur M, Kaiser CA, Thorpe C, and Fass D. Generating disulfides enzymatically: Reaction products and electron acceptors of the endoplasmic reticulum thiol oxidase Ero1p. Proc Natl Acad Sci USA 103: 299-304, 2006.
42. Gruber CW, Cemazar M, Heras B, Martiin JL, and Craik DJ. Protein disulfide isomerase: the structure of oxidative folding. Trends Biochem Sci 31: 455-464, 2006.
43. Guthapfel R, Gueguen P, and Quemeneur E. ATP binding and hydrolysis by the multifunctional protein disulfide isomerase. J Biol Chem 271: 2663-2666, 1996.
44. Huang EM, Detwiler TC, Milev Y, and Essex DW. Thiol-disulfide isomerization in thrombospondin: effects of conformation and protein disulfide isomerase. Blood 89: 3205-3212, 1997.
45. Inanami O, Johnson JL, and Babior BM. The leukocyte NADPH oxidase subunit p47PHOX: the role of the cysteine residues. Arch Biochem Biophys 350: 36-40, 1998.
46. Janiszewski M, Pedro MA, Scheffer RC, van Asseldonk JH, Souza LC, da Luz PL, Augusto O, and Laurindo FR. Inhibition of vascular NADH/NADPH oxidase activity by thiol reagents: lack of correlation with cellular glutathione redox status. Free Radical Biol Med 29: 889-899, 2000.
47. Janiszewski M, Lopes LR, Carmo AO, Pedro MA, Brandes RP, Santos CX, and Laurindo FR. Regulation of NAD(P)H oxidase by associated protein disulfide isomerase in vascular smooth muscle cells.J Biol Chem 280: 40813-40819, 2005.
48. Jiang XM, Fitzgerald M, Grant CM, and Hogg PJ. Redox control of exofacial protein thiols/disulfides by protein disulfide isomerase. J Biol Chem 274: 2416-2423, 1999.
49. John DC, Grant ME, and Bulleid NJ. Cell-free synthesis and assembly of prolyl 4-hydroxylase: the role of the beta-subunit (PDI) in preventing misfolding and aggregation of the alpha-subunit. EMBO J 12: 1587-1595, 1993.
50. Jones DP. Redefining oxidative stress. Antiox Redox Signal 8: 1865-1879, 2006.
51. Kaufmann BB and van Ourdenaarden A. Stochastic gene expression: from single molecules to the proteome. Curr Opin Genet Dev 17: 107-112, 2007.
52. Kim JR, Yoon HW, Kwon KS, Lee SR, and Rhee SG. Identification of proteins containing cysteine residues that are sensitive to oxidation by hydrogen peroxide at neutral pH. Anal Biochem 283: 214-221, 2000.
53. Kimura T, Imaishi K, Hagiwara Y, Horibe T, Hayano T, Takahashi N, Urade R, Kato K, and Kikuchi M. ERp57 binds competitively to protein disulfide isomerase and calreticulin. Biochem Biophys Res Commun 331: 224-230, 2005.
54. Klappa P, Hawkins HC, and Freedman RB. Interactions between protein disulphide isomerase and peptides. Eur J Biochem 248: 37-42, 1997.
55. Kobayashi T, Robinson JM, and Seguchi H. Identification of intracellular sites of superoxide production in stimulated neutrophils. J Cell Sci 111: 81-91, 1998.
56. Koivunem P, Salo KEH, Myllyharju J, and Ruddock LW. Three binding sites in protein disulfide isomerase cooperate in collagen prolyl 4-hydroxylase tetramer assembly. J Biol Chem 280: 5227-5235, 2005.
57. Kulp MS, Frickel EM, Ellgaard L, and Weissman JS. Domain architecture of protein-disulfide isomerase facilitates its dual role as an oxidase and an isomerase in Ero1p-mediated disulfide formation. J Biol Chem 281: 876-884, 2006.
58. Laboissiere MC, Sturley SL, and Raines RT. The essential function of protein-disulfide isomerase is to unscramble non-native disulfide bonds. J Biol Chem 270: 28006-28009, 1995.
59. Lahav J, Gofer-Dadosh N, Luboshitz J, Hess O, and Shaklai M. Protein disulfide isomerase mediates integrin-dependent adhesion. FEBS Lett 475: 89-92, 2000.
60. Lahav J, Jurk K, Hess O, Barnes MJ, Farndale RW, Luboshitz J, and Kehrel BE. Sustained integrin ligation involves extracellular free sulfhydryls and enzymatically catalyzed disulfide exchange. Blood 100: 2472-2478, 2002.
61. Lahav J, Wijnen EM, Hess O, Hamaia SW, Griffiths D, Makris M, Knight CG, Essex DW, and Farndale RW. Enzymatically catalyzed disulfide exchange is required for platelet adhesion to collagen via integrin alpha2beta1. Blood 102: 2085-2092, 2003.
62. Langenbach KJ and Sottile J. Identification of protein-disulfide isomerase activity in fibronectin. J Biol Chem 274: 7032-7038, 1999.
63. Lappi AK, Lensink MF, Alanen HI, Salo KE, Lobell M, Juffer AH, and Ruddock LW. A conserved arginine plays a role in the catalytic cycle of the protein disulphide isomerases. J Mol Biol 335: 283-295, 2004.
64. Lassegue B and Clempus RE. Vascular NAD(P)H oxidases: specific features, expression, and regulation. Am J Physiol Regul Integr Comp Physiol 285: R277-297, 2003.
65. Li JM and Shah AM. Mechanism of endothelial cell NADPH oxidase activation by angiotensin II. Role of the p47phox subunit. J Biol Chem 278 12094-12100, 2003.
66. 2-dependent recruitment of TRAF6 to endosomal interleukin-1 receptor complexes. Mol Cell Biol 26: 140-154, 2006.
67. - production by a non-phagocytic NAD(P)H oxidase causes oxidant injury. J Biol Chem 276: 29251-29256, 2001.
68. Lundstrom J, Krause G, and Holmgren A. A Pro to His mutation in active site of thioredoxin increases its disulfide-isomerase activity 10-fold. New refolding systems for reduced or randomly oxidized ribonuclease. J Biol Chem 267: 9047-9052, 1992.
69. Mandel R, Ryser HJ, Ghani F, Wu M, and Peak D. Inhibition of a reductive function of the plasma membrane by bacitracin and antibodies against protein disulfide-isomerase. Proc Natl Acad Sci USA 90: 4112-4116, 1993.
70. Martyn KD, Frederick LM, von Loehneysen K, Dinauer MC, and Knaus UG. Functional analysis of Nox4 reveals unique characteristics compared to other NADPH oxidases. Cell Signal 18: 69-82, 2006.
71. Meunier L, Usherwood YK, Chung KT, and Hendershot LM. A subset of chaperones and folding enzymes form multiprotein complexes in endoplasmic reticulum to bind nascent proteins. Mol Biol Cell 13: 4456-4469, 2002.
72. Meusser B, Hirsch C, Jarosch E, and Sommer T. ERAD: the long road to destruction. Nat Cell Biol 7: 766-772, 2005.
73. Molteni SN, Fassio A, Ciriolo MR, Filomeni G, Pasqualetto E, Fagioli C, and Sitia R. Glutathione limits Ero1-dependent oxidation in the endoplasmic reticulum. J Biol Chem 279: 32667-32673, 2004.
74. Noiva R, Freedman RB, and Lennarz WJ. Peptide binding to protein disulfide isomerase occurs at a site distinct from the active sites. J Biol Chem 268: 19210-19217, 1993.
75. Noiva R. Protein disulfide isomerase: the multifunctional redox chaperone of the endoplasmic reticulum. Semin Cell Dev Biol 10: 481-493, 1999.
76. O'Neill S, Robinson A, Deering A, Ryan M, Fitzgerald DJ, and Moran N. The platelet integrin alpha IIbbeta 3 has an endogenous thiol isomerase activity. J Biol Chem 275: 36984-36990, 2000.
77. Orlandi PA. Protein-disulfide isomerase-mediated reduction of the A subunit of cholera toxin in a human intestinal cell line. J Biol Chem 272: 4591-4599, 1997.
78. Otsu M, Bertoli G, Fagioli C, Guerini-Rocco E, Nerini-Molteni S, Ruffato E, and Sitia R. Dynamic retention of Ero1alpha and Ero1beta in the endoplasmic reticulum by interactions with PDI and ERp44. Antioxid Redox Signal 8: 274-282, 2006.
79. Pariser HP, Zhang J, and Hausman RE. The cell adhesion molecule retina cognin is a cell surface protein disulfide isomerase that uses disulfide exchange activity to modulate cell adhesion. Exp Cell Res 258: 42-52, 2000.
80. Park B, Lee S, Kim E, Cho K, Riddell SR, Cho S, and Ahn K. Redox regulation facilitates optimal peptide selection by MHC class I during antigen processing. Cell 127: 369-382, 2006.
81. Plonka A, Krasiukianis R, Mayer J, Zgirski A, and Hilewiczgrabska M. Pulse-radiolysis studies on reactivity of BSA and BSA-Cu(II) complexes. Radiation Physics Chem 38: 445-447, 1991.
82. Radi R, Beckman JS, Bush KM, and Freeman BA. Peroxynitrite oxidation of sulfhydryls. The cytotoxic potential of superoxide and nitric oxide. J Biol Chem 266: 4244-4250, 1991.
83. Ramachandran N, Root P, Jiang XM, Hogg PJ, and Mutus B. Mechanism of transfer of NO from extracellular S-nitrosothiols into the cytosol by cell-surface protein disulfide isomerase. Proc Natl Acad Sci USA 98: 9539-9544, 2001.
84. Rao ASK and Hausman RE. cDNA for R-cognin: homology with a multifunctional protein. Proc Natl Acad Sci USA 90: 2950-2954, 1993.
85. Rocic P, Seshiah P, and Griendling KK. Reactive oxygen species sensitivity of angiotensin II-dependent translation initiation in vascular smooth muscle cells. J Biol Chem 278: 36973-36979, 2003.
86. Ruddock LW, Hirst TR, and Freedman RB. PH-dependence of the dithiol-oxidizing activity of DsbA (a periplasmic protein thiol:disulphide oxidoreductase) and protein disulphide-isomerase: studies with a novel simple peptide substrate. Biochem J 315: 1001-1005, 1996.
87. Rutkowski DT and Kaufman RJ. A trip to the ER: coping with stress. Trends Cell Biol 14: 20-28, 2004.
88. Saloheimo M, Lund M, and Penttila ME. The protein disulphide isomerase gene of the fungus Trichoderma reesei is induced by endoplasmic reticulum stress and regulated by the carbon source. Mol Gen Genet 262: 35-45, 1999.
89. Sekaki A, Gardes-Albert M, and Ferradini C. Aspects physicochimiques des espéces réactives de l'oxygène. Journ Etude Chim Radiat Societe Francaise de Chimie, Mont Sainte-Odile, France, 1984.
90. Seshiah PN, Weber DS, Rocic P, Valppu L, Taniyama Y, and Griendling KK. Angiotensin II stimulation of NAD(P)H oxidase activity: upstream mediators. Circ Res 91: 406-413, 2002.
91. Shoulders CC and Shelness GS. Current biology of MTP: implications for selective inhibition. Curr Top Med Chem 5: 283-300, 2005.
92. Sitia R, Braakman I. Sitia R, and Braakman I. Quality control in the endoplasmic reticulum protein factory. Nature 426: 891-894, 2003.
93. Sitia R and Molteni SN. Stress, protein (mis)folding, and signaling: the redox connection. Sci STKE 239: 27, 2004.
94. Stockton JD, Merkert MC, and Kellaris KV. A complex of chaperones and disulfide isomerases occludes the cytosolic face of the translocation protein Sec61p and affects translocation of the prion protein. Biochemistry 42: 12821-12834, 2003.
95. Su Y and Block ER. Phenylarsine oxide inhibits nitric oxide synthase in pulmonary artery endothelial cells. Free Radical Biol Med 28: 167-173, 2000.
96. Sullivan DC, Huminiecki L, Moore JW, Boyle JJ, Poulsom R, Creamer D, Barker J, and Bicknell R. EndoPDI, a novel protein-disulfide isomerase-like protein that is preferentially expressed in endothelial cells acts as a stress survival factor. J Biol Chem 278: 47079-47088, 2003.
97. Tanaka S, Uehara T, and Nomura Y. Up-regulation of protein-disulfide isomerase in response to hypoxia/brain ischemia and its protective effect against apoptotic cell death. J Biol Chem 275: 10388-10393, 2000.
98. Terada K, Manchikalapudi P, Noiva R, Jauregui HO, Stockert RJ, and Schilsky ML. Secretion, surface localization, turnover, and steady state expression of protein disulfide isomerase in rat hepatocytes. J Biol Chem 270: 20410-20416, 1995.
99. Tian G, Xiang S, Noiva R, Lennarz WJ, and Schindelin H. The crystal structure of yeast protein disulfide isomerase suggests cooperativity between its active sites. Cell 124: 61-73, 2006.
100. Touyz RM, Tabet F, and Schiffrin EL. Redox-dependent signalling by angiotensin II and vascular remodelling in hypertension. Clin Exper Pharmacol Physiol 30: 860-866, 2003.
101. Touyz RM, Yao G, and Schiffrin EL. c-Src induces phosphorylation and translocation of p47phox: role in superoxide generation by angiotensin II in human vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 23: 981-987, 2003.
102. Tu BP and Weissman JS. The FAD- and O(2)-dependent reaction cycle of Ero1-mediated oxidative protein folding in the endoplasmic reticulum. Mol Cell 10: 983-994, 2002.
103. Uehara T, Nakamura T, Yao D, Shi ZQ, Gu Z, Ma Y, Masliah E, Nomura Y, and Lipton SA. S-nitrosylated protein-disulphide isomerase links protein misfolding to neurodegeneration. Nature 441: 513-517, 2006.
104. Ueyama T, Lekstrom K, Tsujibe S, Saito N, and Leto TL. Subcellular localization and function of alternatively spliced Noxo1 isoforms. Free Radical Biol Med 42: 180-190, 2007.
105. Ushio-Fukai M, Alexander RW, Akers M, Yin Q, Fujio Y, Walsh K, and Griendling KK. Reactive oxygen species mediate the activation of Akt/protein kinase B by angiotensin II in vascular smooth muscle cells. J Biol Chem 274: 22699-22704, 1999.
106. Ushio-Fukai M. Localizing NADPH oxidase-derived ROS. Sci STKE 349(8): 1-6, 2006.
107. Walsh GM, Sheehan D, Kinsella A, Moran N, and O'Neill S. 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.
108. Wang D, De Deken X, Milenkovic M, Song Y, Pirson I, Dumont JE, and Miot F. Identification of a novel partner of duox: EFP1, a thioredoxin-related protein. J Biol Chem 280: 3096-3103, 2005.
109. Wilkinson B and Gilbert HF. Protein disulfide isomerase. Biochim Biophys Acta 1699: 35-44, 2004.
110. Winterbourn CC and Metodiewa D. Reactivity of biologically important thiol compounds with superoxide and hydrogen peroxide. Free Radical Biol Med 27: 322-328, 1999.
111. Yamawaki H, Haendeler J, and Berk BC. Thioredoxin: a key regulator of cardiovascular homeostasis. Circ Res 93: 1029-1033, 2003.
112. Zai A, Rudd MA, Scribner AW, and Loscalzo J. Cell-surface protein disulfide isomerase catalyzes transnitrosation and regulates intracellular transfer of nitric oxide. J Clin Invest 103: 393-399, 1999.