Crystal structure of an enzyme-substrate complex provides insight into the interaction between human arylsulfatase A and its substrates during catalysis

Bulow von R, Schmidt B, Dierks T, Figura von K, Uson I (2001)
JOURNAL OF MOLECULAR BIOLOGY 305(2): 269-277.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
 
Download
Es wurden keine Dateien hochgeladen. Nur Publikationsnachweis!
Autor*in
Bulow von, R; Schmidt, B; Dierks, ThomasUniBi; Figura von, K; Uson, I
Abstract / Bemerkung
Arylsulfatase A (ASA) belongs to the sulfatase family whose members carry a C-alpha-formylglycine that is post-translationally generated by oxidation of a conserved cysteine or serine residue. The crystal structures of two arylsulfatases, ASA and ASB, and kinetic studies on ASA mutants led to different proposals for the catalytic mechanism in the hydrolysis of sulfate esters. The structures of two ASA mutants that lack the functional C-alpha-formylglycine residue 69, in complex with a synthetic substrate, have been determined in order to unravel the reaction mechanism. The crystal structure of the inactive mutant C69A-ASA in complex with p-nitrocatechol sulfate (pNCS) mimics a reaction intermediate during sulfate ester hydrolysis by the active enzyme, without the covalent bond to the key side-chain FGly69. The structure shows that the side-chains of lysine 123, lysine 302, serine 150, histidine 229, the main-chain of the key residue 69 and the divalent cation in the active center are involved in sulfate binding. It is proposed that histidine 229 protonates the leaving alcoholate after hydrolysis. C69S-ASA is able to bind covalently to the substrate and hydrolyze it, but is unable to release the resulting sulfate. Nevertheless, the resulting sulfation is low. The structure of C69S-ASA shows the serine side-chain in a single conformation, turned away from the position a substrate occupies in the complex. This suggests that the double conformation observed in the structure of wild-tips ASA is more likely to correspond to a formylglycine hydrate than to a twofold disordered aldehyde oxo group, and accounts for the relative inertness of the C69S-ASA mutant. In the C69S-ASA-pNCS complex, the substrate occupies the same position as in the C69A-ASA-pNCS complex, which corresponds to the noncovalently bonded substrate. Based on the structural data, a detailed mechanism for sulfate ester cleavage is proposed, involving an aldehyde hydrate as the functional group. (C) 2001 Academic Press.
Erscheinungsjahr
2001
Zeitschriftentitel
JOURNAL OF MOLECULAR BIOLOGY
Band
305
Ausgabe
2
Seite(n)
269-277
ISSN
0022-2836
Page URI
https://pub.uni-bielefeld.de/record/2350811

Zitieren

Bulow von R, Schmidt B, Dierks T, Figura von K, Uson I. Crystal structure of an enzyme-substrate complex provides insight into the interaction between human arylsulfatase A and its substrates during catalysis. JOURNAL OF MOLECULAR BIOLOGY. 2001;305(2):269-277.
Bulow von, R., Schmidt, B., Dierks, T., Figura von, K., & Uson, I. (2001). Crystal structure of an enzyme-substrate complex provides insight into the interaction between human arylsulfatase A and its substrates during catalysis. JOURNAL OF MOLECULAR BIOLOGY, 305(2), 269-277. https://doi.org/10.1006/jmbi.2000.4297
Bulow von, R., Schmidt, B., Dierks, T., Figura von, K., and Uson, I. (2001). Crystal structure of an enzyme-substrate complex provides insight into the interaction between human arylsulfatase A and its substrates during catalysis. JOURNAL OF MOLECULAR BIOLOGY 305, 269-277.
Bulow von, R., et al., 2001. Crystal structure of an enzyme-substrate complex provides insight into the interaction between human arylsulfatase A and its substrates during catalysis. JOURNAL OF MOLECULAR BIOLOGY, 305(2), p 269-277.
R. Bulow von, et al., “Crystal structure of an enzyme-substrate complex provides insight into the interaction between human arylsulfatase A and its substrates during catalysis”, JOURNAL OF MOLECULAR BIOLOGY, vol. 305, 2001, pp. 269-277.
Bulow von, R., Schmidt, B., Dierks, T., Figura von, K., Uson, I.: Crystal structure of an enzyme-substrate complex provides insight into the interaction between human arylsulfatase A and its substrates during catalysis. JOURNAL OF MOLECULAR BIOLOGY. 305, 269-277 (2001).
Bulow von, R, Schmidt, B, Dierks, Thomas, Figura von, K, and Uson, I. “Crystal structure of an enzyme-substrate complex provides insight into the interaction between human arylsulfatase A and its substrates during catalysis”. JOURNAL OF MOLECULAR BIOLOGY 305.2 (2001): 269-277.

43 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Identification and Signature Sequences of Bacterial Δ4,5Hexuronate-2-O-Sulfatases.
Wang S, Guan J, Zhang Q, Chen X, Li F., Front Microbiol 10(), 2019
PMID: 31024490
New enzymatic and mass spectrometric methodology for the selective investigation of gut microbiota-derived metabolites.
Ballet C, Correia MSP, Conway LP, Locher TL, Lehmann LC, Garg N, Vujasinovic M, Deindl S, Löhr JM, Globisch D., Chem Sci 9(29), 2018
PMID: 30090311
Identification of Novel ARSA Mutations in Chinese Patients with Metachromatic Leukodystrophy.
Chen L, Yan H, Cao B, Wu Y, Gu Q, Xiao J, Yang Y, Yang H, Shi Z, Yang Z, Pan H, Chang X, Chen J, Sun Y, Zhang Y, Wu X, Jiang Y, Wang J., Int J Genomics 2018(), 2018
PMID: 30057904
Structure of a lipid A phosphoethanolamine transferase suggests how conformational changes govern substrate binding.
Anandan A, Evans GL, Condic-Jurkic K, O'Mara ML, John CM, Phillips NJ, Jarvis GA, Wills SS, Stubbs KA, Moraes I, Kahler CM, Vrielink A., Proc Natl Acad Sci U S A 114(9), 2017
PMID: 28193899
Enzyme-Assisted Preparation of Furcellaran-Like κ-/β-Carrageenan.
Préchoux A, Genicot S, Rogniaux H, Helbert W., Mar Biotechnol (NY) 18(1), 2016
PMID: 26585588
Human recombinant lysosomal enzymes produced in microorganisms.
Espejo-Mojica ÁJ, Alméciga-Díaz CJ, Rodríguez A, Mosquera Á, Díaz D, Beltrán L, Díaz S, Pimentel N, Moreno J, Sánchez J, Sánchez OF, Córdoba H, Poutou-Piñales RA, Barrera LA., Mol Genet Metab 116(1-2), 2015
PMID: 26071627
Genetic analysis of 17 children with Hunter syndrome: identification and functional characterization of four novel mutations in the iduronate-2-sulfatase gene.
Chistiakov DA, Kuzenkova LM, Savost'anov KV, Gevorkyan AK, Pushkov AA, Nikitin AG, Vashakmadze ND, Zhurkova NV, Podkletnova TV, Namazova-Baranova LS, Baranov AA., J Genet Genomics 41(4), 2014
PMID: 24780617
Characterization of glycosaminoglycan (GAG) sulfatases from the human gut symbiont Bacteroides thetaiotaomicron reveals the first GAG-specific bacterial endosulfatase.
Ulmer JE, Vilén EM, Namburi RB, Benjdia A, Beneteau J, Malleron A, Bonnaffé D, Driguez PA, Descroix K, Lassalle G, Le Narvor C, Sandström C, Spillmann D, Berteau O., J Biol Chem 289(35), 2014
PMID: 25002587
Role of heparan sulfatases in ovarian and breast cancer.
Khurana A, Beleford D, He X, Chien J, Shridhar V., Am J Cancer Res 3(1), 2013
PMID: 23359864
An Italian cohort study identifies four new pathologic mutations in the ARSA gene.
Galla D, de Gemmis P, Anesi L, Berto S, Dolcetta D, Hladnik U., J Mol Neurosci 50(2), 2013
PMID: 23559313
The structure of the neisserial lipooligosaccharide phosphoethanolamine transferase A (LptA) required for resistance to polymyxin.
Wanty C, Anandan A, Piek S, Walshe J, Ganguly J, Carlson RW, Stubbs KA, Kahler CM, Vrielink A., J Mol Biol 425(18), 2013
PMID: 23810904
Developing therapeutic approaches for metachromatic leukodystrophy.
Patil SA, Maegawa GH., Drug Des Devel Ther 7(), 2013
PMID: 23966770
Arylsulfatase K, a novel lysosomal sulfatase.
Wiegmann EM, Westendorf E, Kalus I, Pringle TH, Lübke T, Dierks T., J Biol Chem 288(42), 2013
PMID: 23986440
Computational and biological evaluation of quinazolinone prodrug for targeting pancreatic cancer.
Pospisil P, Korideck H, Wang K, Yang Y, Iyer LK, Kassis AI., Chem Biol Drug Des 79(6), 2012
PMID: 22304734
Interaction of arylsulfatase-A (ASA) with its natural sulfoglycolipid substrates: a computational and site-directed mutagenesis study.
Schenk M, Koppisetty CA, Santos DC, Carmona E, Bhatia S, Nyholm PG, Tanphaichitr N., Glycoconj J 26(8), 2009
PMID: 19381802
Structural aspects of therapeutic enzymes to treat metabolic disorders.
Kang TS, Stevens RC., Hum Mutat 30(12), 2009
PMID: 19790257
A review of coumarin derivatives in pharmacotherapy of breast cancer.
Musa MA, Cooperwood JS, Khan MO., Curr Med Chem 15(26), 2008
PMID: 18991629
Paralog of the formylglycine-generating enzyme--retention in the endoplasmic reticulum by canonical and noncanonical signals.
Gande SL, Mariappan M, Schmidt B, Pringle TH, von Figura K, Dierks T., FEBS J 275(6), 2008
PMID: 18266766
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
Heparin-degrading sulfatases in hepatocellular carcinoma: roles in pathogenesis and therapy targets.
Lai JP, Thompson JR, Sandhu DS, Roberts LR., Future Oncol 4(6), 2008
PMID: 19086847
The heparanome--the enigma of encoding and decoding heparan sulfate sulfation.
Lamanna WC, Kalus I, Padva M, Baldwin RJ, Merry CL, Dierks T., J Biotechnol 129(2), 2007
PMID: 17337080
The chemistry of protein catalysis.
Holliday GL, Almonacid DE, Mitchell JB, Thornton JM., J Mol Biol 372(5), 2007
PMID: 17727879
Boronic acids as inhibitors of steroid sulfatase.
Ahmed V, Liu Y, Silvestro C, Taylor SD., Bioorg Med Chem 14(24), 2006
PMID: 16973364
Analysis of normal and mutant iduronate-2-sulphatase conformation.
Parkinson-Lawrence E, Turner C, Hopwood J, Brooks D., Biochem J 386(pt 2), 2005
PMID: 15500445
Highly enantioselective sec-alkyl sulfatase activity of the marine planctomycete Rhodopirellula baltica shows retention of configuration.
Wallner SR, Bauer M, Würdemann C, Wecker P, Glöckner FO, Faber K., Angew Chem Int Ed Engl 44(39), 2005
PMID: 16161167
Protein posttranslational modifications: the chemistry of proteome diversifications.
Walsh CT, Garneau-Tsodikova S, Gatto GJ., Angew Chem Int Ed Engl 44(45), 2005
PMID: 16267872
The difluoromethylene group as a replacement for the labile oxygen in steroid sulfates: a new approach to steroid sulfatase inhibitors.
Lapierre J, Ahmed V, Chen MJ, Ispahany M, Guillemette JG, Taylor SD., Bioorg Med Chem Lett 14(1), 2004
PMID: 14684318
Sulfatases: structure, mechanism, biological activity, inhibition, and synthetic utility.
Hanson SR, Best MD, Wong CH., Angew Chem Int Ed Engl 43(43), 2004
PMID: 15493058
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
Crystal structure of a covalent intermediate of endogenous human arylsulfatase A.
Chruszcz M, Laidler P, Monkiewicz M, Ortlund E, Lebioda L, Lewinski K., J Inorg Biochem 96(2-3), 2003
PMID: 12888274
Binding of arylsulfatase A to mouse sperm inhibits gamete interaction and induces the acrosome reaction.
Carmona E, Weerachatyanukul W, Xu H, Fluharty A, Anupriwan A, Shoushtarian A, Chakrabandhu K, Tanphaichitr N., Biol Reprod 66(6), 2002
PMID: 12021068

38 References

Daten bereitgestellt von Europe PubMed Central.

The sulfatase gene family.
Parenti G, Meroni G, Ballabio A., Curr. Opin. Genet. Dev. 7(3), 1997
PMID: 9229115
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
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
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
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
The mucopolysaccharidoses
Neufeld, 1995
Metachromatic leukodystrophy and multiple sulfatase deficiency: sulfatide lipidosis
Kolodny, 1995
Steroid sulfatase deficiency and X-linked ichthyosis
Ballabio, 1995
A cluster of sulfatase genes on Xp22.3: mutations in chondrodysplasia punctata (CDPX) and implications for warfarin embryopathy.
Franco B, Meroni G, Parenti G, Levilliers J, Bernard L, Gebbia M, Cox L, Maroteaux P, Sheffield L, Rappold GA, Andria G, Petit C, Ballabio A., Cell 81(1), 1995
PMID: 7720070
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
Structure of a human lysosomal sulfatase.
Bond CS, Clements PR, Ashby SJ, Collyer CA, Harrop SJ, Hopwood JJ, Guss JM., Structure 5(2), 1997
PMID: 9032078
Refined structure of alkaline phosphatase from Escherichia coli at 2.8 A resolution.
Sowadski JM, Handschumacher MD, Murthy HM, Foster BA, Wyckoff HW., J. Mol. Biol. 186(2), 1985
PMID: 3910843
Amino acid residues forming the active site of arylsulfatase A. Role in catalytic activity and substrate binding.
Waldow A, Schmidt B, Dierks T, von Bulow R, von Figura K., J. Biol. Chem. 274(18), 1999
PMID: 10212197
Purification and properties of feline and human arylsulfatase B isozymes. Evidence for feline homodimeric and human monomeric structures
McGovern, J. Biol. Chem. 257(), 1982
The structural basis of anomalous kinetics of rabbit liver aryl sulfatase A.
Waheed A, Van Etten RL., Arch. Biochem. Biophys. 203(1), 1980
PMID: 6105847
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
Improved coefficients for maps using phases from partial structures with errors
Read, Acta Crystallog. sect. A 42(), 1986
The dipotassium salt of p-nitrocatecholsulfatase
von, Acta Crystallog. sect. C 56(), 2000

von, 1999
Validation of protein crystal structures
Kleywegt, Acta Crystallog. sect. D 56(), 2000
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
Purification and properties of a homogeneous aryl sulfatase A from rabbit liver.
Lee GD, Van Etten RL., Arch. Biochem. Biophys. 166(1), 1975
PMID: 235891
3',5'-Cyclic nucleotide phosphodiesterase activity of the sulphatase A of ox liver.
Uchida T, Egami F, Roy AB., Biochim. Biophys. Acta 657(2), 1981
PMID: 6111349
Residues critical for formylglycine formation and/or catalytic activity of arylsulfatase A.
Knaust A, Schmidt B, Dierks T, von Bulow R, von Figura K., Biochemistry 37(40), 1998
PMID: 9760228
Crystallisation of biological macromolecules
McPherson, J. Crystal Growth 122(), 1998
Processing of X-ray diffraction data collected in oscillation mode
Otwinowski, Methods Enzymol. 276(), 1997
Refinement of macromolecular structures by the maximum-likelihood method
Murshudov, Acta Crystallorg. sect. D 53(), 1997
Assessment of phase accuracy by cross validation: the free R value. Methods and applications
Brünger, Acta Crystallog. sect. D 49(), 1993
Raster3D: photorealistic molecular graphics.
Merritt EA, Bacon DJ., Meth. Enzymol. 277(), 1997
PMID: 18488322
PROCHECK: a program to check the stereochemical quality of protein structures
Laskowski, J. Appl. Crytallog. 26(), 1993
Conformation of polypeptides and proteins
Ramachandran, Advan. Protein Chem. 28(), 1968

Export

Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®

Quellen

PMID: 11124905
PubMed | Europe PMC

Suchen in

Google Scholar