New water-soluble phosphines as reductants of peptide and protein disulfide bonds: Reactivity and membrane permeability

Biochemistry

Volumn 43, Issue 48, 2004, Pages 15195-15203

  Cline, Daniel J ^a   Redding, Sarah E ^a   Brohawn, Stephen G ^a   Psathas, James N ^a   Schneider, Joel P ^a   Thorpe, Colin ^a  

^a UNIVERSITY OF DELAWARE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESTERS; NEGATIVE IONS; OXIDATION; PHOSPHORUS;

BIOCHEMICAL SYSTEMS; WATER SOLUBLE PHOSPHINES;

PROTEINS;

ANION; CARBOXYLIC ACID; DISULFIDE; DITHIOTHREITOL; ESTER DERIVATIVE; PEPTIDE; PHOSPHINE DERIVATIVE; PHOSPHOLIPID; PHOSPHORUS; PROTEIN; REDUCING AGENT; THIOL OXIDASE; THIOREDOXIN; WATER;

ARTICLE; CHEMICAL BOND; CHEMICAL REACTION; DISULFIDE BOND; ESTERIFICATION; EVALUATION; FLUORESCENCE; LIPOPHILICITY; MEMBRANE PERMEABILITY; MODEL; MOLECULAR MODEL; MOLECULE; PH; PHOSPHOLIPID BILAYER; PRIORITY JOURNAL; REACTION ANALYSIS; REDUCTION; SOLUBILITY; SYNTHESIS;

DISULFIDES; DITHIOTHREITOL; ESCHERICHIA COLI; ESTERIFICATION; ESTERS; HYDROGEN-ION CONCENTRATION; LIPID BILAYERS; MODELS, MOLECULAR; OLIGOPEPTIDES; PERMEABILITY; PHOSPHINES; PROTEINS; REDUCING AGENTS; SOLUBILITY; THIOREDOXIN; WATER;

EID: 10044276833     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi048329a     Document Type: Article

References (62)

1. Burns, J. A., Butler, J. C., Moran, J., and Whitesides, G. M. (1991) Selective Reduction of Disulfides by Tris(2-Carboxyethyl)Phosphine, J. Org. Chem. 56, 2648-2650.
2. Levison, M. E., Josephson, A. S., and Kirschenbaum, D. M. (1969) Reduction of Biological Substances by Water-Soluble Phosphines: γ-Globulin (Igg), Experientia 25, 126-127.
3. Han, J. C., and Han, G. Y. (1994) A procedure for quantitative determination of tris(2-carboxyethyl)phosphine, an odorless reducing agent more stable and effective than dithiothreitol, Anal. Biochem. 220, 5-10.
4. Gray, W. R. (1993) Disulfide structures of highly bridged peptides: a new strategy for analysis, Protein Sci. 2, 1732-1748.
5. Getz, E. B., Xiao, M., Chakrabarty, T., Cooke, R., and Selvin, P. R. (1999) A comparison between the sulfhydryl reductants tris-(2-carboxyethyl) phosphine and dithiothreitol for use in protein biochemistry, Anal. Biochem. 273, 73-80.
6. Geiger, L. K., Kortuem, K. R., Alexejun, C., and Levin, L. A. (2002) Reduced redox state allows prolonged survival of axotomized neonatal retinal ganglion cells, Neuroscience 109, 635-642.
7. de Lamirande, E., and Gagnon, C. (1998) Paradoxical effect of reagents for sulfhydryl and disulfide groups on human sperm capacitation and superoxide production, Free Radical Biol. Med. 25, 803-817.
8. Ruegg, U. T., and Rudinger, J. (1977) Reductive cleavage of cystine disulfides with tributylphosphine, Methods Enzymol. 47, 111-116.
9. Overman, L. E., and Oconnor, E. M. (1976) Nucleophilic Cleavage of Sulfur-Sulfur Bond by Phosphorus Nucleophiles. 4. Kinetic Study of Reduction of Alkyl Disulfides with Triphenylphosphine and Water, J. Am. Chem. Soc. 98, 771-775.
10. Overman, L. E., and Petty, S. T. (1975) Nucleophilic Cleavage of Sulfur-Sulfur Bond by Phosphorus Nucleophiles. 3. Kinetic Study of Reduction of a Series of Ethyl Aryl Disulfides with Triphenylphosphine and Water, J. Org. Chem. 40, 2779-2782.
11. Overman, L. E., Matzinge, D., Oconnor, E. M., and Overman, J. D. (1974) Nucleophilic Cleavage of Sulfur-Sulfur Bond by Phosphorus Nucleophiles: Kinetic Study of Reduction of Aryl Disulfides with Triphenylphosphine and Water, J. Am. Chem. Soc. 96, 6081-6089.
12. Lambert, G., Forster, I. C., Biber, J., and Murer, H. (2000) Cysteine residues and the structure of the rat renal proximal tubular type II sodium phosphate cotransporter (rat NaPi IIa), J. Membr. Biol. 176, 133-141.
13. Lambert, G., Traebert, M., Biber, J., and Murer, H. (2000) Cleavage of disulfide bonds leads to inactivation and degradation of the type IIa, but not type IIb sodium phosphate cotransporter expressed in Xenopus laevis oocytes, J. Membr. Biol. 176, 143-149.
14. Gozlan, H., Diabira, D., Chinestra, P., and Ben-Ari, Y. (1994) Anoxic LTP is mediated by the redox modulatory site of the NMDA receptor. J. Neurophysiol. 72, 3017-3022.
15. Sanchez, R. M., Wang, C., Gardner, G., Orlando, L., Tauck, D. L., Rosenberg, P. A., Aizenman, E., and Jensen, F. E. (2000) Novel role for the NMDA receptor redox modulatory site in the pathophysiology of seizures, J. Neurosci. 20, 2409-2417.
16. Brohawn, S. G., Rudik, I., and Thorpe, C. (2003) Avian Sulfhydryl Oxidase is not a Metalloenzyme: Adventitious Binding of Divalent Metal Ions to the Enzyme, Biochemistry 42, 11074-11082.
17. Cline, D. J., Thorpe, C., and Schneider, J. P. (2003) Structure Based Design of a Fluorimetric Redox Active Peptide Probe, Anal. Biochem. 325, 144-150.
18. Hoober, K. L. (1999) The isolation and initial characterization of a sulfhydryl oxidase from chicken egg white, Ph.D. Dissertation, University of Delaware, Newark, DE.
19. Hoober, K. L., and Thorpe, C. (2002) Flavin-dependent sulfhydryl oxidases in protein disulfide bond formation, Methods Enzymol. 348, 30-34.
20. Eyer, P., Worek, F., Kiderlen, D., Sinko, G., Stuglin, A., Simeon-Rudolf, V., and Reiner, E. (2003) Molar absorption coefficients for the reduced Ellman reagent: reassessment, Anal. Biochem. 312, 224-227.
21. Cleland, W. W. (1964) Dithiothreitol New Protective Reagent for SH Groups, Biochemistry 3, 480-482.
22. Holmgren, A., and Reichard, P. (1967) Thioredoxin 2: cleavage with cyanogen bromide, Eur. J. Biochem. 2, 187-196.
23. Holmgren, A. (1972) Tryptophan Fluorescence Study of Conformational Transitions of the Oxidized and Reduced Forms of Thioredoxin, J. Biol. Chem. 247, 1992-1998.
24. Jain, M. K. (1988) Introduction to Biological Membranes, 2nd ed., John Wiley & Sons, New York.
25. Hoober, K., and Thorpe, C. (2002) Flavin-dependent Sulfhydryl Oxidases in Protein Disulfide Bond Formation, Methods Enzymol. 348, 30-34.
26. Hoober, K. L., Joneja, B., White, H. B., III, and Thorpe, C. (1996) A Sulfhydryl Oxidase from Chicken Egg White, J. Biol. Chem. 271, 30510-30516.
27. Fernandas, A. P., and Holmgren, A. (2004) Glutaredoxins: glutathione-dependent redox enzymes with functions far beyond a simple thioredoxin backup system, Antioxid. Redox Signaling 6, 63-74.
28. Chivers, P. T., Prehoda, K. E., and Raines, R. T. (1997) The CXXC motif: a rheostat in the active site, Biochemistry 36, 4061-4066.
29. Kadokura, H., Katzen, F., and Beckwith, J. (2003) Protein Disulfide Bond Formation in Prokaryotes, Annu. Rev. Biochem. 72, 111-135.
30. Aslund, F., Berndt, K. D., and Holmgren, A. (1997) Redox potentials of glutaredoxins and other thiol-disulfide oxidoreductases of the thioredoxin superfamily determined by direct protein-protein redox equilibria. J. Biol. Chem. 272, 30780-30786.
31. Frand, A. R., and Kaiser, C. A. (2000) Two pairs of conserved cysteines are required for the oxidative activity of Erolp in protein disulfide bond formation in the endoplasmic reticulum, Mol. Biol. Cell 11, 2833-2843.
32. Benham, A. M., Cabibbo, A., Fassio, A., Bulleid, N., Sitia, R., and Braakman, I. (2000) The CXXCXXC motif determines the folding, structure and stability of human Erol-Lα, EMBO J. 19, 4493-4502.
33. Frand, A. R., and Kaiser, C. A. (1998) The ERO1 gene of yeast is required for oxidation of protein dithiols in the endoplasmic reticulum, Mol. Cell 1, 161-170.
34. Pollard, M. G., Travers, K. J., and Weissman, J. S. (1998) Ero1p: a novel and ubiquitous protein with an essential role in oxidative protein folding in the endoplamic reticulum, Mol. Cell 1, 171-182.
35. Williams, C. H., Arscott, L. D., Muller, S., Lennon, B. W., Ludwig, M. L., Wang, P. F., Veine, D. M., Becker, K., and Schirmer, R. H. (2000) Thioredoxin reductase two modes of catalysis have evolved, Eur. J. Biochem. 267, 6110-6117.
36. Collet, J. F., and Bardwell, J. C. (2002) Oxidative protein folding in bacteria, Mol. Microbiol. 44, 1-8.
37. Freedman, R. B., Klappa, P., and Ruddock, L. W. (2002) Protein disulfide isomerases exploit synergy between catalytic and specific binding domains, EMBO Rep. 3, 136-140.
38. Gilbert, H. F. (1997) Protein disulfide isomerase and assisted protein folding, J. Biol. Chem. 272, 29399-29402.
39. Ferrari, D. M., and Soling, H.-D. (1999) The protein disulfide-isomerase family: unravelling a string of folds, Biochem. J. 339, 1-10.
40. Gross, E., Sevier, C. S., Vala, A., Kaiser, C. A., and Fass, D. (2002) A new FAD-binding fold and intersubunit disulfide shuttle in the thiol oxidase Erv2p, Nat. Struct. Biol. 9, 61-67.
41. Gerber, J., Muhlenhoff, U., Hofhaus, G., Lill, R., and Lisowsky, T. (2001) Yeast ERV2p is the first microsomal FAD-linked sulfhydryl oxidase of the Erv1p/A1rp protein family, J. Biol. Chem. 276, 23486-23491.
42. Lisowsky, T., Lee, J. E., Polimeno, L., Francavilla, A., and Hofhaus, G. (2001) Mammalian augmenter of liver regeneration protein is a sulfhydryl oxidase, Dig. Liver Dis. 33, 173-180.
43. Thorpe, C., Hoober, K., Raje, S., Glynn, N., Burnside, J., Turi, G., and Coppock, D. (2002) Sulfhydryl oxidases: emerging catalysts of protein disulfide bond formation in eukaryotes, Arch. Biochem. Biophys. 405, 1-12.
44. Raje, S., and Thorpe, C. (2003) Inter-domain redox communication in flavoenzymes of the quiescin/sulfhydryl oxidase family: role of a thioredoxin domain in disulfide bond formation, Biochemistry 42, 4560-4568.
45. Podlaha, J., and Podlahov, J. (1973) Compounds Structurally Related to Complexone. 1. Tris(Carboxyethyl)Phosphine, Collect. Czech. Chem. Commun. 38, 1730-1736.
46. Krezel, A., Latajka, R., Bujacz, G. D., and Bal, W. (2003) Coordination properties of tris(2-carboxyethyl)phosphine, a newly introduced thiol reductant, and its oxide, Inorg. Chem. 42, 1994-2003.
47. Siedler, F., Rudolphbohner, S., Doi, M., Musiol, H. J., and Moroder, L. (1993) Redox Potentials of Active-Site Bis(Cysteinyl) Fragments of Thiol-Protein Oxidoreductases, Biochemistry 32, 7488-7495.
48. Woycechowsky, K. J., and Raines, R. T. (2003) The CXC motif: A functional mimic of protein disulfide isomerase, Biochemistry 42, 5387-5394.
49. Holmgren, A. (1979) Thioredoxin catalyzes the reduction of insulin disulfides by dithiothreitol and dihydrolipoamide, J. Biol. Chem. 254, 9627-9632.
50. March, J. (1985) Advanced Organic Chemistry, 3rd ed., John Wiley, New York.
51. Missiakas, D., Georgopoulos, C., and Raina, S. (1994) The Escherichia coli dsbC (xprA) gene encodes a periplasmic protein involved in disulfide bond formation, EMBO J. 13, 2013-2020.
52. Missiakas, D., Georgopoulos, C., and Raina, S. (1993) Identification and characterization of the Escherichia coli gene dsbB, whose product is involved in the formation of disulfide bonds in vivo, Proc. Natl. Acad. Sci. U.S.A. 90, 7084-7088.
53. Holst, B., Tachibana, C., and Winther, J. R. (1997) Active site mutations in yeast protein disulfide isomerase cause dithiothreitol sensitivity and a reduced rate of protein folding in the endoplasmic reticulum, J. Cell Biol. 138, 1229-1238.
54. Cabibbo, A., Pagani, M., Fabbri, M., Rocchi, M., Farmery, M. R., Bulleid, N. J., and Sitia, R. (2000) ERO1-L, a human protein that favors disulfide bond formation in the endoplasmic reticulum, J. Biol. Chem. 275, 4827-4833.
55. Pakula, T. M., Laxell, M., Huuskonen, A., Uusitalo, J., Saloheimo, M., and Penttila, M. (2003) The effects of drugs inhibiting protein secretion in the filamentous fungus Trichoderma reesei. Evidence for down-regulation of genes that encode secreted proteins in the stressed cells, J. Biol. Chem. 278, 45011-45020.
56. Tatu, U., Braakman, I., and Helenius, A. (1993) Membrane glycoprotein folding, oligomerization and intracellular transport: effects of dithiothreitol in living cells, EMBO J. 12, 2151-2157.
57. Braakman, I., Helenius, J., and Helenius, A. (1992) Manipulating disulfide bond formation and protein folding in the endoplasmic reticulum, EMBO J. 11, 1717-1722.
58. Valetti, C., and Sitia, R. (1994) The differential effects of dithiothreitol and 2-mercaptoethanol on the secretion of partially and completely assembled immunoglobulins suggest that thiol-mediated retention does not take place in or beyond the Golgi, Mol. Biol. Cell 5, 1311-1324.
59. Lodish, H. F., and Kong, N. (1993) The secretory pathway is normal in dithiothreitol-treated cells, but disulfide-bonded proteins are reduced and reversibly retained in the endoplasmic reticulum, J. Biol. Chem. 268, 20598-20605.
60. Burch, W. L., and Herscovitz, H. (2000) Disulfide bonds are required for folding and secretion of apolipoprotein B regardless of its lipidation state, J. Biol. Chem. 275, 16267-16274.
61. Wittrup, K. D. (1995) Disulfide bond formation and eukaryotic secretory productivity, Curr. Opin. Biotechnol. 6, 203-208.
62. Henderson, W. A., Jr., and Streuli, C. A. (1960) Basicity of Phosphines, J. Am. Chem. Soc. 82, 5794-5800.