The Quiescin Sulfhydryl Oxidase (hQSOX1b) Tunes the Expression of Resistin-Like Molecule Alpha (RELM-α or mFIZZ1) in a Wheat Germ Cell-Free Extract

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Gad, Wael ^a,b,c   Nair, Meera G ^e,h   van Belle, Karolien ^a,b,c   Wahni, Khadija ^a,b,c   de Greve, Henri ^b,c   van Ginderachter, Jo A ^b,c   Vandenbussche, Guy ^f   Endo, Yaeta ^d   Artis, David ^e,g   Messens, Joris ^a,b,c  

^a Brussels Center for Redox Biology   (Belgium)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^d EHIME UNIVERSITY   (Japan)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

^f UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^g UNIVERSITY OF PENNSYLVANIA   (United States)

^h UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; GLUTATHIONE; INTERLEUKIN 13; INTERLEUKIN 5; QUIESCIN THIOL OXIDASE; RESISTIN; RESISTIN LIKE MOLECULE ALPHA PROTEIN; THIOL OXIDASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CELL FREE SYSTEM; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISULFIDE BOND; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; ENZYME REGULATION; GENE; GERMINATION; IN VITRO STUDY; MFIZZ1 GENE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT CELL; PROCESS OPTIMIZATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN SYNTHESIS INHIBITION; SPLEEN CELL; TH2 CELL; WHEAT GERM;

AMINO ACID SEQUENCE; ANIMALS; DISULFIDES; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GERM CELLS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MOLECULAR SEQUENCE DATA; OXIDATION-REDUCTION; OXIDOREDUCTASES ACTING ON SULFUR GROUP DONORS; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; SEQUENCE ALIGNMENT; SOLUBILITY; TRITICUM;

EID: 84873208973     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0055621     Document Type: Article

References (50)

1. Holcomb IN, Kabakoff RC, Chan B, Baker TW, Gurney A, et al. (2000) FIZZ1, a novel cysteine-rich secreted protein associated with pulmonary inflammation, defines a new gene family. EMBO J 19: 4046-4055.
2. Nair MG, Guild KJ, Artis D, (2006) Novel effector molecules in type 2 inflammation: lessons drawn from helminth infection and allergy. J Immunol 177: 1393-1399.
3. Nair MG, Gallagher IJ, Taylor MD, Loke P, Coulson PS, et al. (2005) Chitinase and Fizz family members are a generalized feature of nematode infection with selective upregulation of Ym1 and Fizz1 by antigen-presenting cells. Infect Immun 73: 385-394.
4. Patel SD, Rajala MW, Rossetti L, Scherer PE, Shapiro L, (2004) Disulfide-dependent multimeric assembly of resistin family hormones. Science 304: 1154-1158.
5. Sandler NG, Mentink-Kane MM, Cheever AW, Wynn TA, (2003) Global gene expression profiles during acute pathogen-induced pulmonary inflammation reveal divergent roles for Th1 and Th2 responses in tissue repair. J Immunol 171: 3655-3667.
6. Depuydt M, Messens J, Collet JF, (2011) How proteins form disulfide bonds. Antioxid Redox Signal 15: 49-66.
7. Wouters MA, Fan SW, Haworth NL, (2010) Disulfides as redox switches: from molecular mechanisms to functional significance. Antioxid Redox Signal 12: 53-91.
8. Messens J, Collet JF, (2006) Pathways of disulfide bond formation in Escherichia coli. Int J Biochem Cell Biol 38: 1050-1062.
9. Riemer J, Bulleid N, Herrmann JM, (2009) Disulfide formation in the ER and mitochondria: two solutions to a common process. Science 324: 1284-1287.
10. Karala AR, Lappi AK, Ruddock LW, (2010) Modulation of an active-site cysteine pKa allows PDI to act as a catalyst of both disulfide bond formation and isomerization. J Mol Biol 396: 883-892.
11. Tu BP, Ho-Schleyer SC, Travers KJ, Weissman JS, (2000) Biochemical basis of oxidative protein folding in the endoplasmic reticulum. Science 290: 1571-1574.
12. Sevier CS, Cuozzo JW, Vala A, Aslund F, Kaiser CA, (2001) A flavoprotein oxidase defines a new endoplasmic reticulum pathway for biosynthetic disulphide bond formation. Nat Cell Biol 3: 874-882.
13. Thorpe C, Hoober KL, Raje S, Glynn NM, Burnside J, et al. (2002) Sulfhydryl oxidases: emerging catalysts of protein disulfide bond formation in eukaryotes. Arch Biochem Biophys 405: 1-12.
14. Coppock DL, Kopman C, Scandalis S, Gilleran S, (1993) Preferential gene expression in quiescent human lung fibroblasts. Cell Growth Differ 4: 483-493.
15. Kodali VK, Thorpe C, (2010) Oxidative protein folding and the Quiescin-sulfhydryl oxidase family of flavoproteins. Antioxid Redox Signal 13: 1217-1230.
16. Wittke I, Wiedemeyer R, Pillmann A, Savelyeva L, Westermann F, et al. (2003) Neuroblastoma-derived sulfhydryl oxidase, a new member of the sulfhydryl oxidase/Quiescin6 family, regulates sensitization to interferon gamma-induced cell death in human neuroblastoma cells. Cancer Res 63: 7742-7752.
17. Coppock DL, Cina-Poppe D, Gilleran S, (1998) The quiescin Q6 gene (QSCN6) is a fusion of two ancient gene families: thioredoxin and ERV1. Genomics 54: 460-468.
18. Powis G, Montfort WR, (2001) Properties and biological activities of thioredoxins. Annu Rev Pharmacol Toxicol 41: 261-295.
19. Lisowsky T, (1992) Dual function of a new nuclear gene for oxidative phosphorylation and vegetative growth in yeast. Mol Gen Genet 232: 58-64.
20. Alon A, Heckler EJ, Thorpe C, Fass D, (2010) QSOX contains a pseudo-dimer of functional and degenerate sulfhydryl oxidase domains. FEBS Lett 584: 1521-1525.
21. Takai K, Sawasaki T, Endo Y, (2010) Practical cell-free protein synthesis system using purified wheat embryos. Nature protocols 5: 227-238.
22. Endo Y, Sawasaki T, (2006) Cell-free expression systems for eukaryotic protein production. Curr Opin Biotechnol 17: 373-380.
23. Juan CC, Kan LS, Huang CC, Chen SS, Ho LT, et al. (2003) Production and characterization of bioactive recombinant resistin in Escherichia coli. J Biotechnol 103: 113-117.
24. Nguyen VD, Hatahet F, Salo KE, Enlund E, Zhang C, et al. (2011) Pre-expression of a sulfhydryl oxidase significantly increases the yields of eukaryotic disulfide bond containing proteins expressed in the cytoplasm of E. coli. Microb Cell Fact 10: 1.
25. Updegrove TB, Correia JJ, Chen Y, Terry C, Wartell RM, (2011) The stoichiometry of the Escherichia coli Hfq protein bound to RNA. RNA 17: 489-500.
26. Panchaud A, Hansson J, Affolter M, Bel Rhlid R, Piu S, et al. (2008) ANIBAL, stable isotope-based quantitative proteomics by aniline and benzoic acid labeling of amino and carboxylic groups. Mol Cell Proteomics 7: 800-812.
27. Banerjee RR, Lazar MA, (2001) Dimerization of resistin and resistin-like molecules is determined by a single cysteine. J Biol Chem 276: 25970-25973.
28. Sreerama N, Woody RW, (2000) Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set. Anal Biochem 287: 252-260.
29. Whitmore L, Wallace BA, (2004) DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data. Nucleic Acids Res 32: W668-673.
30. Nair MG, Du Y, Perrigoue JG, Zaph C, Taylor JJ, et al. (2009) Alternatively activated macrophage-derived RELM-{alpha} is a negative regulator of type 2 inflammation in the lung. J Exp Med 206: 937-952.
31. Munitz A, Seidu L, Cole ET, Ahrens R, Hogan SP, et al. (2009) Resistin-like molecule alpha decreases glucose tolerance during intestinal inflammation. J Immunol 182: 2357-2363.
32. Messens J, Collet JF, Van Belle K, Brosens E, Loris R, et al. (2007) The oxidase DsbA folds a protein with a nonconsecutive disulfide. J Biol Chem 282: 31302-31307.
33. Depuydt M, Messens J, Collet JF, (2011) How proteins form disulfide bonds. Antioxid Redox Signal 15: 49-66.
34. Zapun A, Missiakas D, Raina S, Creighton TE, (1995) Structural and functional characterization of DsbC, a protein involved in disulfide bond formation in Escherichia coli. Biochemistry 34: 5075-5089.
35. Hatahet F, Ruddock LW, (2009) Protein disulfide isomerase: a critical evaluation of its function in disulfide bond formation. Antioxid Redox Signal 11: 2807-2850.
36. Grynberg A, Nicolas J, Drapron R, (1977) Presence of a protein disulfide isomerase (EC 5.3.4.1) in wheat germ. C R Acad Sci Hebd Seances Acad Sci D 284: 235-238.
37. Rancy PC, Thorpe C, (2008) Oxidative protein folding in vitro: a study of the cooperation between quiescin-sulfhydryl oxidase and protein disulfide isomerase. Biochemistry 47: 12047-12056.
38. Paetzel M, Karla A, Strynadka NC, Dalbey RE, (2002) Signal peptidases. Chem Rev 102: 4549-4580.
39. Wilson R, Lees JF, Bulleid NJ, (1998) Protein disulfide isomerase acts as a molecular chaperone during the assembly of procollagen. J Biol Chem 273: 9637-9643.
40. Cai H, Wang CC, Tsou CL, (1994) Chaperone-like activity of protein disulfide isomerase in the refolding of a protein with no disulfide bonds. J Biol Chem 269: 24550-24552.
41. Wang C, Yu J, Huo L, Wang L, Feng W, et al. (2012) Human protein-disulfide isomerase is a redox-regulated chaperone activated by oxidation of domain a'. J Biol Chem 287: 1139-1149.
42. Abskharon RN, Ramboarina S, El Hassan H, Gad W, Apostol MI, et al. (2012) A novel expression system for production of soluble prion proteins in E. coli. Microb Cell Fact 11: 6.
43. Heckler EJ, Alon A, Fass D, Thorpe C, (2008) Human quiescin-sulfhydryl oxidase, QSOX1: probing internal redox steps by mutagenesis. Biochemistry 47: 4955-4963.
44. Bradford MM, (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
45. Van Laer K, Buts L, Foloppe N, Vertommen D, Van Belle K, et al. (2012) Mycoredoxin-1 is one of the missing links in the oxidative stress defense mechanism of Mycobacteria. Mol Microbiol 86: 787-804.
46. Ordóñez E, Van Belle K, Roos G, De Galan S, Letek M, et al. (2009) Arsenate reductase, mycothiol, and mycoredoxin concert thiol/disulfide exchange. J Biol Chem 284: 15107-15116.
47. Depuydt M, Leonard SE, Vertommen D, Denoncin K, Morsomme P, et al. (2009) A periplasmic reducing system protects single cysteine residues from oxidation. Science 326: 1109-1111.
48. Plesa M, Hernalsteens JP, Vandenbussche G, Ruysschaert JM, Cornelis P, (2006) The SlyB outer membrane lipoprotein of Burkholderia multivorans contributes to membrane integrity. Res Microbiol 157: 582-592.
49. Park S, Lippard SJ, (2011) Redox state-dependent interaction of HMGB1 and cisplatin-modified DNA. Biochemistry 50: 2567-2574.
50. Thompson JD, Higgins DG, Gibson TJ, (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.