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Review Articles

Distinct enzymatic strategies for de novo generation of disulfide bonds in membranes

Pages 36-49 | Received 02 Jan 2023, Accepted 06 Apr 2023, Published online: 25 Apr 2023

References

  • Bader M, Muse W, Ballou DP, Gassner C, Bardwell JC. 1999. Oxidative protein folding is driven by the electron transport system. Cell. 98(2):217–227.
  • Bader M, Muse W, Zander T, Bardwell J. 1998. Reconstitution of a protein disulfide catalytic system. J Biol Chem. 273(17):10302–10307.
  • Bardwell JC, Lee JO, Jander G, Martin N, Belin D, Beckwith J. 1993. A pathway for disulfide bond formation in vivo. Proc Natl Acad Sci U S A. 90(3):1038–1042.
  • Bardwell JC, McGovern K, Beckwith J. 1991. Identification of a protein required for disulfide bond formation in vivo. Cell. 67(3):581–589.
  • Bevans CG, Krettler C, Reinhart C, Watzka M, Oldenburg J. 2015. Phylogeny of the Vitamin K 2,3-Epoxide Reductase (VKOR) Family and Evolutionary Relationship to the Disulfide Bond Formation Protein B (DsbB) Family. Nutrients. 7(8):6224–6249.
  • Bolhuis A, Venema G, Quax WJ, Bron S, van Dijl JM. 1999. Functional analysis of paralogous thiol-disulfide oxidoreductases in Bacillus subtilis. J Biol Chem. 274(35):24531–24538.
  • Chu P-H, Huang T-Y, Williams J, Stafford DW. 2006. Purified vitamin K epoxide reductase alone is sufficient for conversion of vitamin K epoxide to vitamin K and vitamin K to vitamin KH2. Proc Natl Acad Sci U S A. 103(51):19308–19313.
  • Creighton TE. 1978. Experimental studies of protein folding and unfolding. Prog Biophys Mol Biol. 33(3):231–297.
  • Dailey FE, Berg HC. 1993. Mutants in disulfide bond formation that disrupt flagellar assembly in Escherichia coli. Proc Natl Acad Sci U S A. 90(3):1043–1047.
  • Davey L, Halperin SA, Lee SF. 2016. Thiol-Disulfide Exchange in Gram-Positive Firmicutes. Trends Microbiol. 24(11):902–915.
  • Davis CH, Deerfield D, Wymore T, Stafford DW, Pedersen LG, Transition II. 2007. A quantum chemical study of the mechanism of action of Vitamin K epoxide reductase (VKOR). J Mol Graph Model. 26(2):401–408.
  • Dutton RJ, Boyd D, Berkmen M, Beckwith J. 2008. Bacterial species exhibit diversity in their mechanisms and capacity for protein disulfide bond formation. Proc Natl Acad Sci U S A. 105(33):11933–11938.
  • Dutton RJ, Wayman A, Wei J-R, Rubin EJ, Beckwith J, Boyd D. 2010. Inhibition of bacterial disulfide bond formation by the anticoagulant warfarin. Proc Natl Acad Sci U S A. 107(1):297–301.
  • Fasco MJ, Preusch PC, Hildebrandt E, Suttie JW. 1983. Formation of hydroxyvitamin K by vitamin K epoxide reductase of warfarin-resistant rats. J Biol Chem. 258(7):4372–4380.
  • Feng WK, Wang L, Lu Y, Wang XY. 2011. A protein oxidase catalysing disulfide bond formation is localized to the chloroplast thylakoids. Febs J. 278(18):3419–3430.
  • Fernandes PA, Ramos MJ. 2004. Theoretical insights into the mechanism for thiol/disulfide exchange. Chemistry. 10(1):257–266.
  • Forman-Kay JD, Clore GM, Gronenborn AM. 1992. Relationship between electrostatics and redox function in human thioredoxin: characterization of pH titration shifts using two-dimensional homo- and heteronuclear NMR. Biochemistry. 31(13):3442–3452.
  • Frand AR, Kaiser CA. 1998. The ERO1 gene of yeast is required for oxidation of protein dithiols in the endoplasmic reticulum. Mol Cell. 1(2):161–170.
  • Furie B, Furie BC. 1988. The molecular basis of blood coagulation. Cell. 53(4):505–518.
  • Gilbert HF. 1997. Protein disulfide isomerase and assisted protein folding. J Biol Chem. 272(47):29399–29402.
  • Goldberger RF, Epstein CJ, Anfinsen CB. 1963. Acceleration of reactivation of reduced bovine pancreatic ribonuclease by a microsomal system from rat liver. J Biol Chem. 238(2):628–635.
  • Goodstadt L, Ponting CP. 2004. Vitamin K epoxide reductase: homology, active site and catalytic mechanism. Trends Biochem Sci. 29:2002–2005.
  • Grauschopf U, Winther JR, Korber P, Zander T, Dallinger P, Bardwell JC. 1995. Why is DsbA such an oxidizing disulfide catalyst? Cell. 83(6):947–955.
  • Gross E, Kastner DB, Kaiser CA, Fass D. 2004. Structure of Ero1p, source of disulfide bonds for oxidative protein folding in the cell. Cell. 117(5):601–610.
  • Gross E, Sevier CS, Vala A, Kaiser C, Fass D. 2002. A new FAD-binding fold and intersubunit disulfide shuttle in the thiol oxidase Erv2p. Nat Struct Biol. 9(1):61–67.
  • Hammed A, Matagrin B, Spohn G, Prouillac C, Benoit E, Lattard V. 2013. VKORC1L1, an enzyme rescuing the vitamin K 2,3-epoxide reductase activity in some extrahepatic tissues during anticoagulation therapy. J Biol Chem. 288(40):28733–28742.
  • Hatahet F, Blazyk JL, Martineau E, Mandela E, Zhao Y, Campbell RE, Beckwith J, Boyd D. 2015. Altered Escherichia coli membrane protein assembly machinery allows proper membrane assembly of eukaryotic protein vitamin K epoxide reductase. Proc Natl Acad Sci U S A. 112(49):15184–15189.
  • Hatahet F, Boyd D, Beckwith J. 2014. Disulfide bond formation in prokaryotes: history, diversity and design. Biochim Biophys Acta. 1844(8):1402–1414.
  • Hatahet F, Ruddock LW. 2009. Protein Disulfide Isomerase: A Critical Evaluation of Its Function in Disulfide Bond Formation. Antioxid Redox Signal. 11(11):2807–2850.
  • Heras B, Shouldice SR, Totsika M, Scanlon MJ, Schembri MA, Martin JL. 2009. DSB proteins and bacterial pathogenicity. Nat Rev Microbiol. 7(3):215–225.
  • Hiniker A, Bardwell JC. 2004. In vivo substrate specificity of periplasmic disulfide oxidoreductases. J Biol Chem. 279(13):12967–12973.
  • Hui Y, Chng EL, Chua LP, Liu WZ, Webster RD. 2010. Voltammetric method for determining the trace moisture content of organic solvents based on hydrogen-bonding interactions with quinones. Anal Chem. 82(5):1928–1934.
  • Inaba K, Murakami S, Nakagawa A, Iida H, Kinjo M, Ito K, Suzuki M. 2009. Dynamic nature of disulphide bond formation catalysts revealed by crystal structures of DsbB. Embo J. 28(6):779–791.
  • Inaba K, Murakami S, Suzuki M, Nakagawa A, Yamashita E, Okada K, Ito K. 2006. Crystal Structure of the DsbB-DsbA Complex Reveals a Mechanism of Disulfide Bond Generation. Cell. 127(4):789–801.
  • Inaba K, Takahashi YH, Ito K. 2005. Reactivities of quinone-free DsbB from Escherichia coli. J Biol Chem. 280(38):33035–33044.
  • Ishihara T, Tomita H, Hasegawa Y, Tsukagoshi N, Yamagata H, Udaka S. 1995. Cloning and characterization of the gene for a protein thiol-disulfide oxidoreductase in Bacillus brevis. J Bacteriol. 177(3):745–749.
  • Ito K, Inaba K. 2008. The disulfide bond formation (Dsb) system. Curr Opin Struct Biol. 18(4):450–458.
  • Kadokura H, Beckwith J. 2002. Four cysteines of the membrane protein DsbB act in concert to oxidize its substrate DsbA. Embo J. 21(10):2354–2363.
  • Kadokura H, Katzen F, Beckwith J. 2003. Protein Disulfide Bond Formation in Prokaryotes. Annu Rev Biochem. 72(1):111–135.
  • Kadokura H, Tian H, Zander T, Bardwell JC, Beckwith J. 2004. Snapshots of DsbA in action: detection of proteins in the process of oxidative folding. Science. 303(5657):534–537.
  • Khan MA, Moktar J, Mott PJ, Bishop RE. 2010. A thiolate anion buried within the hydrocarbon ruler perturbs PagP lipid acyl chain selection. Biochemistry. 49(11):2368–2379.
  • Kobayashi T, Kishigami S, Sone M, Inokuchi H, Mogi T, Ito K. 1997. Respiratory chain is required to maintain oxidized states of the DsbA-DsbB disulfide bond formation system in aerobically growing Escherichia coli cells. Proc Natl Acad Sci U S A. 94(22):11857–11862.
  • Kobayashi T, Takahashi Y, Ito K. 2001. Identification of a segment of DsbB essential for its respiration-coupled oxidation. Mol Microbiol. 39(1):158–165.
  • Kortemme T, Creighton TE. 1995. Ionisation of cysteine residues at the termini of model alpha-helical peptides. Relevance to unusual thiol pKa values in proteins of the thioredoxin family. J Mol Biol. 253(5):799–812.
  • Lacombe J, Rishavy MA, Berkner KL, Ferron M. 2018. VKOR paralog VKORC1L1 supports vitamin K-dependent protein carboxylation in vivo. JCI Insight. 3(1):e96501.
  • LaMantia ML, Lennarz WJ. 1993. The essential function of yeast protein disulfide isomerase does not reside in its isomerase activity. Cell. 74(5):899–908.
  • Lambert N, Freedman RB. 1983. Kinetics and specificity of homogeneous protein disulphide-isomerase in protein disulphide isomerization and in thiol-protein-disulphide oxidoreduction. Biochem J. 213(1):235–243.
  • Landeta C, Blazyk JL, Hatahet F, Meehan BM, Eser M, Myrick A, Bronstain L, Minami S, Arnold H, Ke N, et al. 2015. Compounds targeting disulfide bond forming enzyme DsbB of Gram-negative bacteria. Nat Chem Biol. 11(4):292–298.
  • Landeta C, McPartland L, Tran NQ, Meehan BM, Zhang Y, Tanweer Z, Wakabayashi S, Rock J, Kim T, Balasubramanian D, et al. 2019. Inhibition of Pseudomonas aeruginosa and Mycobacterium tuberculosis disulfide bond forming enzymes. Mol Microbiol. 111(4):918–937.
  • Li T, Chang C-YY, Jin D-YY, Lin P-JJ, Khvorova A, Stafford DW. 2004. Identification of the gene for vitamin K epoxide reductase. Nature. 427(6974):541–544.
  • Li W, Schulman S, Dutton RJ, Boyd D, Beckwith J, Rapoport TA. 2010. Structure of a bacterial homologue of vitamin K epoxide reductase. Nature. 463(7280):507–512.
  • Lin D, Rao CV, Slauch JM. 2008. The Salmonella SPI1 type three secretion system responds to periplasmic disulfide bond status via the flagellar apparatus and the RcsCDB system. J Bacteriol. 190(1):87–97.
  • Link KP. 1959. The discovery of dicumarol and its sequels. Circulation. 19(1):97–107.
  • Liu S, Cheng W, Fowle Grider R, Shen G, Li W. 2014. Structures of an intramembrane vitamin K epoxide reductase homolog reveal control mechanisms for electron transfer. Nat Commun. 5:3110–3110.
  • Liu S, Li S, Shen G, Sukumar N, Krezel AM, Li W. 2021. Structural basis of antagonizing the vitamin K catalytic cycle for anticoagulation. Science. 371(6524):eabc5667.
  • Liu S, Li S, Yang Y, Li W. 2020. Termini restraining of small membrane proteins enables structure determination at near-atomic resolution. Sci Adv. 6(51):eabe3717.
  • Lo Bello M, Parker MW, Desideri A, Polticelli F, Falconi M, Del Boccio G, Pennelli A, Federici G, Ricci G. 1993. Peculiar spectroscopic and kinetic properties of Cys-47 in human placental glutathione transferase. Evidence for an atypical thiolate ion pair near the active site. J Biol Chem. 268(25):19033–19038.
  • Mallick P, Boutz DR, Eisenberg D, Yeates TO. 2002. Genomic evidence that the intracellular proteins of archaeal microbes contain disulfide bonds. Proc Natl Acad Sci U S A. 99(15):9679–9684.
  • Malojc G. 2008. Preparation and structure of the charge-transfer intermediate of the transmembrane redox catalyst DsbB ˇ ic. FEBS Lett. 582:3301–3307.
  • Matagrin B, Hodroge A, Montagut-Romans A, Andru J, Fourel I, Besse S, Benoit E, Lattard V. 2013. New insights into the catalytic mechanism of vitamin K epoxide reductase (VKORC1) - The catalytic properties of the major mutations of rVKORC1 explain the biological cost associated to mutations. FEBS Open Bio. 3:144–150.
  • Matthews DA, Dragovich PS, Webber SE, Fuhrman SA, Patick AK, Zalman LS, Hendrickson TF, Love RA, Prins TJ, Marakovits JT, et al. 1999. Structure-assisted design of mechanism-based irreversible inhibitors of human rhinovirus 3C protease with potent antiviral activity against multiple rhinovirus serotypes. Proc Natl Acad Sci U S A. 96(20):11000–11007.
  • Mesecke N, Terziyska N, Kozany C, Baumann F, Neupert W, Hell K, Herrmann JM. 2005. A disulfide relay system in the intermembrane space of mitochondria that mediates protein import. Cell. 121(7):1059–1069.
  • Missiakas D, Georgopoulos C, 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(15):7084–7088.
  • Nelson JW, Creighton TE. 1994. Reactivity and ionization of the active site cysteine residues of DsbA, a protein required for disulfide bond formation in vivo. Biochemistry. 33(19):5974–5983.
  • Phan J, Zdanov A, Evdokimov AG, Tropea JE, Peters HK, 3rd, Kapust RB, Li M, Wlodawer A, Waugh DS. 2002. Structural basis for the substrate specificity of tobacco etch virus protease. J Biol Chem. 277(52):50564–50572.
  • Pollard MG, Travers KJ, Weissman JS. 1998. Ero1p: a novel and ubiquitous protein with an essential role in oxidative protein folding in the endoplasmic reticulum. Mol Cell. 1(2):171–182.
  • Premkumar L, Heras B, Duprez W, Walden P, Halili M, Kurth F, Fairlie DP, Martin JL. 2013. Rv2969c, essential for optimal growth in Mycobacterium tuberculosis, is a DsbA-like enzyme that interacts with VKOR-derived peptides and has atypical features of DsbA-like disulfide oxidases. Acta Crystallogr D Biol Crystallogr. 69(Pt 10):1981–1994.
  • Raczko AM, Bujnicki JM, Pawłowski M, Godlewska R, Lewandowska M, Jagusztyn-Krynicka EK. 2005. Characterization of new DsbB-like thiol-oxidoreductases of Campylobacter jejuni and Helicobacter pylori and classification of the DsbB family based on phylogenomic, structural and functional criteria. Microbiology (Reading). 151(Pt 1):219–231.
  • Ren B, Tibbelin G, de Pascale D, Rossi M, Bartolucci S, Ladenstein R. 1998. A protein disulfide oxidoreductase from the archaeon Pyrococcus furiosus contains two thioredoxin fold units. Nat Struct Biol. 5(7):602–611.
  • Rezaie AR, Neuenschwander PF, Morrissey JH, Esmon CT. 1993. Analysis of the functions of the first epidermal growth factor-like domain of factor X. J Biol Chem. 268(11):8176–8180.
  • Reznik N, Fass D. 2022. Disulfide bond formation and redox regulation in the Golgi apparatus. FEBS Lett. 596(22):2859–2872.
  • Robertson HM. 2004. Genes encoding vitamin-K epoxide reductase are present in Drosophila and trypanosomatid protists. Genetics. 168(2):1077–1080.
  • Rost S, Fregin A, Ivaskevicius V, Conzelmann E, Hörtnagel K, Pelz H-J, Lappegard K, Seifried E, Scharrer I, Tuddenham EGD, et al. 2004. Mutations in VKORC1 cause warfarin resistance and multiple coagulation factor deficiency type 2. Nature. 427(6974):537–541.
  • Rutkevich LA, Williams DB. 2012. Vitamin K epoxide reductase contributes to protein disulfide formation and redox homeostasis within the endoplasmic reticulum. Mol Biol Cell. 23(11):2017–2027.
  • Sadler JE. 2004. K is for koagulation. Nature. 427(6974):493–494.
  • Saxena VP, Wetlaufer DB. 1970. Formation of three-dimensional structure in proteins. I. Rapid nonenzymic reactivation of reduced lysozyme. Biochemistry. 9(25):5015–5023.
  • 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(10):874–882.
  • Sevier CS, Kadokura H, Tam VC, Beckwith J, Fass D, Kaiser CA. 2005. The prokaryotic enzyme DsbB may share key structural features with eukaryotic disulfide bond forming oxidoreductases. Protein Sci. 14(6):1630–1642.
  • Shen G, Cui W, Cao Q, Gao M, Liu H, Su G, Gross ML, Li W. 2021. The catalytic mechanism of vitamin K epoxide reduction in a cellular environment. J Biol Chem. 296:100145.
  • Shen G, Cui W, Zhang H, Zhou F, Huang W, Liu Q, Yang Y, Li S, Bowman GR, Sadler JE, et al. 2017. Warfarin traps human vitamin K epoxide reductase in an intermediate state during electron transfer. Nat Struct Mol Biol. 24(1):69–76.
  • Shen G, Li C, Cao Q, Megta AK, Li S, Gao M, Liu H, Shen Y, Chen Y, Yu H, et al. 2022. Structural features determining the vitamin K epoxide reduction activity in the VKOR family of membrane oxidoreductases. FEBS J
  • Silverman RB. 1981. Chemical model studies for the mechanism of vitamin k epoxide reductase. J Am Chem Soc. 103(19):5939–5941.
  • Singh AK, Bhattacharyya-Pakrasi M, Pakrasi HB. 2008. Identification of an atypical membrane protein involved in the formation of protein disulfide bonds in oxygenic photosynthetic organisms. J Biol Chem. 283(23):15762–15770.
  • Stafford DW. 2005. The vitamin K cycle. J Thromb Haemost. 3(8):1873–1878.
  • Takahashi YH, Inaba K, Ito K. 2004. Characterization of the menaquinone-dependent disulfide bond formation pathway of Escherichia coli. J Biol Chem. 279(45):47057–47065.
  • Tang M, Nesbitt AE, Sperling LJ, Berthold DA, Schwieters CD, Gennis RB, Rienstra CM. 2013. Structure of the disulfide bond generating membrane protein DsbB in the lipid bilayer. J Mol Biol. 425(10):1670–1682.
  • Tie J-K, Jin D-Y, Stafford DW. 2012. Mycobacterium tuberculosis vitamin K epoxide reductase homologue supports vitamin K-dependent carboxylation in mammalian cells. Antioxid Redox Signal. 16(4):329–338.
  • Totsika M, Heras B, Wurpel DJ, Schembri MA. 2009. Characterization of two homologous disulfide bond systems involved in virulence factor biogenesis in uropathogenic Escherichia coli CFT073. J Bacteriol. 191(12):3901–3908.
  • Van Den Berg B, Chung EW, Robinson CV, Mateo PL, Dobson CM. 1999. The oxidative refolding of hen lysozyme and its catalysis by protein disulfide isomerase. Embo J. 18(17):4794–4803.
  • Venetianer P, Straub FB. 1963. The enzymic reactivation of reduced ribonuclease. Biochim Biophys Acta. 67:166–168.
  • Vermeer C, Hamulyak K. 2004. Vitamin K: lessons from the past. J Thromb Haemost. 2(12):2115–2117.
  • Vertommen D, Depuydt M, Pan J, Leverrier P, Knoops L, Szikora JP, Messens J, Bardwell JC, Collet JF. 2008. The disulphide isomerase DsbC cooperates with the oxidase DsbA in a DsbD-independent manner. Mol Microbiol. 67(2):336–349.
  • Voss J, Sun J, Venkatesan P, Kaback HR. 1998. Sulfhydryl oxidation of mutants with cysteine in place of acidic residues in the lactose permease. Biochemistry. 37(22):8191–8196.
  • Wang X, Dutton RJ, Beckwith J, Boyd D. 2011. Membrane topology and mutational analysis of Mycobacterium tuberculosis VKOR, a protein involved in disulfide bond formation and a homologue of human vitamin K epoxide reductase. Antioxid Redox Signal. 14(8):1413–1420.
  • Yu J, Kroll JS. 1999. DsbA: a protein-folding catalyst contributing to bacterial virulence. Microbes Infect. 1(14):1221–1228.
  • Zhou Y, Cierpicki T, Jimenez RHF, Lukasik SM, Ellena JF, Cafiso DS, Kadokura H, Beckwith J, Bushweller JH. 2008. NMR solution structure of the integral membrane enzyme DsbB: functional Insights into DsbB-catalyzed disulfide bond formation. Mol Cell. 31(6):896–908.

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