Post-translational formylglycine modification of bacterial sulfatases by the radical S-adenosylmethionine protein AtsB

Fang QH, Peng JH, Dierks T (2004)
JOURNAL OF BIOLOGICAL CHEMISTRY 279(15): 14570-14578.

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Abstract / Bemerkung
C-alpha-Formylglycine (FGly) is the catalytic residue of sulfatases. FGly is generated by post-translational modification of a cysteine ( prokaryotes and eukaryotes) or serine ( prokaryotes) located in a conserved (C/S) XPXR motif. AtsB of Klebsiella pneumoniae is directly involved in FGly generation from serine. AtsB is predicted to belong to the newly discovered radical S-adenosylmethionine (SAM) superfamily. By in vivo and in vitro studies we show that SAM is the critical co-factor for formation of a functional AtsB . SAM . sulfatase complex and for FGly formation by AtsB. The SAM-binding site of AtsB involves (83)GGE(85) and possibly also a juxtaposed FeS center coordinated by Cys(39) and Cys(42), as indicated by alanine scanning mutagenesis. Mutation of these and other conserved cysteines as well as treatment with metal chelators fully impaired FGly formation, indicating that all three predicted FeS centers are crucial for AtsB function. It is concluded that AtsB oxidizes serine to FGly by a radical mechanism that is initiated through reductive cleavage of SAM, thereby generating the highly oxidizing deoxyadenosyl radical, which abstracts a hydrogen from the serine-CbetaH2-OH side chain.
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JOURNAL OF BIOLOGICAL CHEMISTRY
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279
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15
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14570-14578
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Fang QH, Peng JH, Dierks T. Post-translational formylglycine modification of bacterial sulfatases by the radical S-adenosylmethionine protein AtsB. JOURNAL OF BIOLOGICAL CHEMISTRY. 2004;279(15):14570-14578.
Fang, Q. H., Peng, J. H., & Dierks, T. (2004). Post-translational formylglycine modification of bacterial sulfatases by the radical S-adenosylmethionine protein AtsB. JOURNAL OF BIOLOGICAL CHEMISTRY, 279(15), 14570-14578. doi:10.1074/jbc.M313855200
Fang, Q. H., Peng, J. H., and Dierks, T. (2004). Post-translational formylglycine modification of bacterial sulfatases by the radical S-adenosylmethionine protein AtsB. JOURNAL OF BIOLOGICAL CHEMISTRY 279, 14570-14578.
Fang, Q.H., Peng, J.H., & Dierks, T., 2004. Post-translational formylglycine modification of bacterial sulfatases by the radical S-adenosylmethionine protein AtsB. JOURNAL OF BIOLOGICAL CHEMISTRY, 279(15), p 14570-14578.
Q.H. Fang, J.H. Peng, and T. Dierks, “Post-translational formylglycine modification of bacterial sulfatases by the radical S-adenosylmethionine protein AtsB”, JOURNAL OF BIOLOGICAL CHEMISTRY, vol. 279, 2004, pp. 14570-14578.
Fang, Q.H., Peng, J.H., Dierks, T.: Post-translational formylglycine modification of bacterial sulfatases by the radical S-adenosylmethionine protein AtsB. JOURNAL OF BIOLOGICAL CHEMISTRY. 279, 14570-14578 (2004).
Fang, QH, Peng, JH, and Dierks, Thomas. “Post-translational formylglycine modification of bacterial sulfatases by the radical S-adenosylmethionine protein AtsB”. JOURNAL OF BIOLOGICAL CHEMISTRY 279.15 (2004): 14570-14578.

33 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Structure and expression of sulfatase and sulfatase modifying factor genes in the diamondback moth, Plutella xylostella.
Ma XL, He WY, Chen W, Xu XJ, Qi WP, Zou MM, You YC, Baxter SW, Wang P, You MS., Insect Sci 25(6), 2018
PMID: 28569426
Two-fold Bioorthogonal Derivatization by Different Formylglycine-Generating Enzymes.
Krüger T, Weiland S, Falck G, Gerlach M, Boschanski M, Alam S, Müller KM, Dierks T, Sewald N., Angew Chem Int Ed Engl 57(24), 2018
PMID: 29579347
Following the electrons: peculiarities in the catalytic cycles of radical SAM enzymes.
Ruszczycky MW, Zhong A, Liu HW., Nat Prod Rep 35(7), 2018
PMID: 29485151
Glycosulfatase-Encoding Gene Cluster in Bifidobacterium breve UCC2003.
Egan M, Jiang H, O'Connell Motherway M, Oscarson S, van Sinderen D., Appl Environ Microbiol 82(22), 2016
PMID: 27590817
SPASM and twitch domains in S-adenosylmethionine (SAM) radical enzymes.
Grell TA, Goldman PJ, Drennan CL., J Biol Chem 290(7), 2015
PMID: 25477505
Mechanistic Enzymology of the Radical SAM Enzyme DesII.
Ruszczycky MW, Liu HW., Isr J Chem 55(3-4), 2015
PMID: 27635101
Radical S-adenosylmethionine enzymes.
Broderick JB, Duffus BR, Duschene KS, Shepard EM., Chem Rev 114(8), 2014
PMID: 24476342
Further characterization of Cys-type and Ser-type anaerobic sulfatase maturating enzymes suggests a commonality in the mechanism of catalysis.
Grove TL, Ahlum JH, Qin RM, Lanz ND, Radle MI, Krebs C, Booker SJ., Biochemistry 52(17), 2013
PMID: 23477283
X-ray structure of an AdoMet radical activase reveals an anaerobic solution for formylglycine posttranslational modification.
Goldman PJ, Grove TL, Sites LA, McLaughlin MI, Booker SJ, Drennan CL., Proc Natl Acad Sci U S A 110(21), 2013
PMID: 23650368
Radical SAM enzymes in the biosynthesis of sugar-containing natural products.
Ruszczycky MW, Ogasawara Y, Liu HW., Biochim Biophys Acta 1824(11), 2012
PMID: 22172915
The radical SAM enzyme AlbA catalyzes thioether bond formation in subtilosin A.
Flühe L, Knappe TA, Gattner MJ, Schäfer A, Burghaus O, Linne U, Marahiel MA., Nat Chem Biol 8(4), 2012
PMID: 22366720
Thioether crosslinkages created by a radical SAM enzyme.
Zhang Q, Yu Y., Chembiochem 13(8), 2012
PMID: 22556103
Covalent intermediate in the catalytic mechanism of the radical S-adenosyl-L-methionine methyl synthase RlmN trapped by mutagenesis.
McCusker KP, Medzihradszky KF, Shiver AL, Nichols RJ, Yan F, Maltby DA, Gross CA, Fujimori DG., J Am Chem Soc 134(43), 2012
PMID: 23088750
Adenosyl radical: reagent and catalyst in enzyme reactions.
Marsh EN, Patterson DP, Li L., Chembiochem 11(5), 2010
PMID: 20191656
Anaerobic sulfatase-maturating enzyme--a mechanistic link with glycyl radical-activating enzymes?
Benjdia A, Subramanian S, Leprince J, Vaudry H, Johnson MK, Berteau O., FEBS J 277(8), 2010
PMID: 20218986
A consensus mechanism for Radical SAM-dependent dehydrogenation? BtrN contains two [4Fe-4S] clusters.
Grove TL, Ahlum JH, Sharma P, Krebs C, Booker SJ., Biochemistry 49(18), 2010
PMID: 20377206
S-Adenosylmethionine-dependent radical-based modification of biological macromolecules.
Atta M, Mulliez E, Arragain S, Forouhar F, Hunt JF, Fontecave M., Curr Opin Struct Biol 20(6), 2010
PMID: 20951571
The Radical SAM Superfamily.
Frey PA, Hegeman AD, Ruzicka FJ., Crit Rev Biochem Mol Biol 43(1), 2008
PMID: 18307109
Direct evidence for ArO-S bond cleavage upon inactivation of Pseudomonas aeruginosa arylsulfatase by aryl sulfamates.
Bojarová P, Denehy E, Walker I, Loft K, De Souza DP, Woo LW, Potter BV, McConville MJ, Williams SJ., Chembiochem 9(4), 2008
PMID: 18288656
Anaerobic sulfatase-maturating enzymes, first dual substrate radical S-adenosylmethionine enzymes.
Benjdia A, Subramanian S, Leprince J, Vaudry H, Johnson MK, Berteau O., J Biol Chem 283(26), 2008
PMID: 18408004
In vitro characterization of AtsB, a radical SAM formylglycine-generating enzyme that contains three [4Fe-4S] clusters.
Grove TL, Lee KH, St Clair J, Krebs C, Booker SJ., Biochemistry 47(28), 2008
PMID: 18558715
Sulfotransferases, sulfatases and formylglycine-generating enzymes: a sulfation fascination.
Bojarová P, Williams SJ., Curr Opin Chem Biol 12(5), 2008
PMID: 18625336
Iron-sulfur proteins as initiators of radical chemistry.
Marquet A, Bui BT, Smith AG, Warren MJ., Nat Prod Rep 24(5), 2007
PMID: 17898896
Involvement of a putative [Fe-S]-cluster-binding protein in the biogenesis of quinohemoprotein amine dehydrogenase.
Ono K, Okajima T, Tani M, Kuroda S, Sun D, Davidson VL, Tanizawa K., J Biol Chem 281(19), 2006
PMID: 16546999
Molecular basis for multiple sulfatase deficiency and mechanism for formylglycine generation of the human formylglycine-generating enzyme.
Dierks T, Dickmanns A, Preusser-Kunze A, Schmidt B, Mariappan M, von Figura K, Ficner R, Rudolph MG., Cell 121(4), 2005
PMID: 15907468
Carbonylation of milk powder proteins as a consequence of processing conditions.
Fenaille F, Parisod V, Tabet JC, Guy PA., Proteomics 5(12), 2005
PMID: 16038017
Structural and functional comparison of HemN to other radical SAM enzymes.
Layer G, Kervio E, Morlock G, Heinz DW, Jahn D, Retey J, Schubert WD., Biol Chem 386(10), 2005
PMID: 16218869
S-adenosylmethionine radical enzymes.
Marsh EN, Patwardhan A, Huhta MS., Bioorg Chem 32(5), 2004
PMID: 15381399

36 References

Daten bereitgestellt von Europe PubMed Central.

A novel amino acid modification in sulfatases that is defective in multiple sulfatase deficiency.
Schmidt B, Selmer T, Ingendoh A, von Figura K., Cell 82(2), 1995
PMID: 7628016
Crystal structure of human arylsulfatase A: the aldehyde function and the metal ion at the active site suggest a novel mechanism for sulfate ester hydrolysis.
Lukatela G, Krauss N, Theis K, Selmer T, Gieselmann V, von Figura K, Saenger W., Biochemistry 37(11), 1998
PMID: 9521684
A novel protein modification generating an aldehyde group in sulfatases: its role in catalysis and disease.
von Figura K, Schmidt B, Selmer T, Dierks T., Bioessays 20(6), 1998
PMID: 9699462

AUTHOR UNKNOWN, 0
1.3 A structure of arylsulfatase from Pseudomonas aeruginosa establishes the catalytic mechanism of sulfate ester cleavage in the sulfatase family.
Boltes I, Czapinska H, Kahnert A, von Bulow R, Dierks T, Schmidt B, von Figura K, Kertesz MA, Uson I., Structure 9(6), 2001
PMID: 11435113
Sulfatases, trapping of the sulfated enzyme intermediate by substituting the active site formylglycine.
Recksiek M, Selmer T, Dierks T, Schmidt B, von Figura K., J. Biol. Chem. 273(11), 1998
PMID: 9497327

AUTHOR UNKNOWN, 0
Multiple sulfatase deficiency is caused by mutations in the gene encoding the human C(alpha)-formylglycine generating enzyme.
Dierks T, Schmidt B, Borissenko LV, Peng J, Preusser A, Mariappan M, von Figura K., Cell 113(4), 2003
PMID: 12757705
The multiple sulfatase deficiency gene encodes an essential and limiting factor for the activity of sulfatases.
Cosma MP, Pepe S, Annunziata I, Newbold RF, Grompe M, Parenti G, Ballabio A., Cell 113(4), 2003
PMID: 12757706
Conversion of cysteine to formylglycine: a protein modification in the endoplasmic reticulum.
Dierks T, Schmidt B, von Figura K., Proc. Natl. Acad. Sci. U.S.A. 94(22), 1997
PMID: 9342345
Sequence determinants directing conversion of cysteine to formylglycine in eukaryotic sulfatases.
Dierks T, Lecca MR, Schlotterhose P, Schmidt B, von Figura K., EMBO J. 18(8), 1999
PMID: 10205163
Characterization of posttranslational formylglycine formation by luminal components of the endoplasmic reticulum.
Fey J, Balleininger M, Borissenko LV, Schmidt B, von Figura K, Dierks T., J. Biol. Chem. 276(50), 2001
PMID: 11600503
Posttranslational formation of formylglycine in prokaryotic sulfatases by modification of either cysteine or serine.
Dierks T, Miech C, Hummerjohann J, Schmidt B, Kertesz MA, von Figura K., J. Biol. Chem. 273(40), 1998
PMID: 9748219
Arylsulfatase from Klebsiella pneumoniae carries a formylglycine generated from a serine.
Miech C, Dierks T, Selmer T, von Figura K, Schmidt B., J. Biol. Chem. 273(9), 1998
PMID: 9478923
A sulfur- and tyramine-regulated Klebsiella aerogenes operon containing the arylsulfatase (atsA) gene and the atsB gene.
Murooka Y, Ishibashi K, Yasumoto M, Sasaki M, Sugino H, Azakami H, Yamashita M., J. Bacteriol. 172(4), 1990
PMID: 2180918
The iron sulfur protein AtsB is required for posttranslational formation of formylglycine in the Klebsiella sulfatase.
Szameit C, Miech C, Balleininger M, Schmidt B, von Figura K, Dierks T., J. Biol. Chem. 274(22), 1999
PMID: 10336424
Radical mechanisms of enzymatic catalysis.
Frey PA., Annu. Rev. Biochem. 70(), 2001
PMID: 11395404
Adenosylmethionine-dependent iron-sulfur enzymes: versatile clusters in a radical new role.
Cheek J, Broderick JB., J. Biol. Inorg. Chem. 6(3), 2001
PMID: 11315557
Computational analysis of bacterial sulfatases and their modifying enzymes.
Schirmer A, Kolter R., Chem. Biol. 5(8), 1998
PMID: 9710560
Increase of solubility of foreign proteins in Escherichia coli by coproduction of the bacterial thioredoxin.
Yasukawa T, Kanei-Ishii C, Maekawa T, Fujimoto J, Yamamoto T, Ishii S., J. Biol. Chem. 270(43), 1995
PMID: 7592692
A microsomal ATP-binding protein involved in efficient protein transport into the mammalian endoplasmic reticulum.
Dierks T, Volkmer J, Schlenstedt G, Jung C, Sandholzer U, Zachmann K, Schlotterhose P, Neifer K, Schmidt B, Zimmermann R., EMBO J. 15(24), 1996
PMID: 9003769
Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels.
Shevchenko A, Wilm M, Vorm O, Mann M., Anal. Chem. 68(5), 1996
PMID: 8779443
Oxygen-independent coproporphyrinogen-III oxidase HemN from Escherichia coli.
Layer G, Verfurth K, Mahlitz E, Jahn D., J. Biol. Chem. 277(37), 2002
PMID: 12114526
Crystal structure of coproporphyrinogen III oxidase reveals cofactor geometry of Radical SAM enzymes.
Layer G, Moser J, Heinz DW, Jahn D, Schubert WD., EMBO J. 22(23), 2003
PMID: 14633981
Molecular dissection of the S-adenosylmethionine-binding site of phosphatidylethanolamine N-methyltransferase.
Shields DJ, Altarejos JY, Wang X, Agellon LB, Vance DE., J. Biol. Chem. 278(37), 2003
PMID: 12842883
Direct FeS cluster involvement in generation of a radical in lysine 2,3-aminomutase.
Cosper NJ, Booker SJ, Ruzicka F, Frey PA, Scott RA., Biochemistry 39(51), 2000
PMID: 11123891

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