1.3 angstrom structure of arylsulfatase from Pseudomonas aeruginosa establishes the catalytic mechanism of sulfate ester cleavage in the sulfatase family

Boltes I, Czapinska H, Kahnert A, Bulow von R, Dierks T, Schmidt B, Figura von K, Kertesz MA, Uson I (2001)
STRUCTURE 9(6): 483-491.

Download
No fulltext has been uploaded. References only!
Journal Article | Published | English

No fulltext has been uploaded

Author
; ; ; ; ; ; ; ;
Abstract
Background: Sulfatases constitute a family of enzymes with a highly conserved active site region including a C alpha -formylglycine that is posttranslationally generated by the oxidation of a conserved cysteine or serine residue. The crystal structures of two human arylsulfatases, ASA and ASB, along with ASA mutants and their complexes led to different proposals for the catalytic mechanism in the hydrolysis of sulfate esters. Results: The crystal structure of a bacterial sulfatase from Pseudomonas aeruginosa (PAS) has been determined at 1.3 Angstrom. Fold and active site region are strikingly similar to those of the known human sulfatases. The structure allows a precise determination of the active site region, unequivocally showing the presence of a C alpha -formylglycine hydrate as the key catalytic residue. Furthermore, the cation located in the active site is unambiguously characterized as calcium by both its B value and the geometry of its coordination sphere. The active site contains a noncovalently bonded sulfate that occupies the same position as the one in para-nitrocate-cholsulfate in previously studied ASA complexes. Conclusions: The structure of PAS shows that the resting state of the key catalytic residue in sulfatases is a formylglycine hydrate. These structural data establish a mechanism for sulfate ester cleavage involving an aldehyde hydrate as the functional group that initiates the reaction through a nucleophilic attack on the sulfur atom in the substrate. The alcohol is eliminated from a reaction intermediate containing pentacoordinated sulfur. Subsequent elimination of the sulfate regenerates the aldehyde, which is again hydrated. The metal cation involved in stabilizing the charge and anchoring the substrate during catalysis is established as calcium.
Publishing Year
ISSN
PUB-ID

Cite this

Boltes I, Czapinska H, Kahnert A, et al. 1.3 angstrom structure of arylsulfatase from Pseudomonas aeruginosa establishes the catalytic mechanism of sulfate ester cleavage in the sulfatase family. STRUCTURE. 2001;9(6):483-491.
Boltes, I., Czapinska, H., Kahnert, A., Bulow von, R., Dierks, T., Schmidt, B., Figura von, K., et al. (2001). 1.3 angstrom structure of arylsulfatase from Pseudomonas aeruginosa establishes the catalytic mechanism of sulfate ester cleavage in the sulfatase family. STRUCTURE, 9(6), 483-491. doi:10.1016/S0969-2126(01)00609-8
Boltes, I., Czapinska, H., Kahnert, A., Bulow von, R., Dierks, T., Schmidt, B., Figura von, K., Kertesz, M. A., and Uson, I. (2001). 1.3 angstrom structure of arylsulfatase from Pseudomonas aeruginosa establishes the catalytic mechanism of sulfate ester cleavage in the sulfatase family. STRUCTURE 9, 483-491.
Boltes, I., et al., 2001. 1.3 angstrom structure of arylsulfatase from Pseudomonas aeruginosa establishes the catalytic mechanism of sulfate ester cleavage in the sulfatase family. STRUCTURE, 9(6), p 483-491.
I. Boltes, et al., “1.3 angstrom structure of arylsulfatase from Pseudomonas aeruginosa establishes the catalytic mechanism of sulfate ester cleavage in the sulfatase family”, STRUCTURE, vol. 9, 2001, pp. 483-491.
Boltes, I., Czapinska, H., Kahnert, A., Bulow von, R., Dierks, T., Schmidt, B., Figura von, K., Kertesz, M.A., Uson, I.: 1.3 angstrom structure of arylsulfatase from Pseudomonas aeruginosa establishes the catalytic mechanism of sulfate ester cleavage in the sulfatase family. STRUCTURE. 9, 483-491 (2001).
Boltes, I, Czapinska, H, Kahnert, A, Bulow von, R, Dierks, Thomas, Schmidt, B, Figura von, K, Kertesz, MA, and Uson, I. “1.3 angstrom structure of arylsulfatase from Pseudomonas aeruginosa establishes the catalytic mechanism of sulfate ester cleavage in the sulfatase family”. STRUCTURE 9.6 (2001): 483-491.
This data publication is cited in the following publications:
This publication cites the following data publications:

69 Citations in Europe PMC

Data provided by Europe PubMed Central.

A homozygous founder missense variant in arylsulfatase G abolishes its enzymatic activity causing atypical Usher syndrome in humans.
Khateb S, Kowalewski B, Bedoni N, Damme M, Pollack N, Saada A, Obolensky A, Ben-Yosef T, Gross M, Dierks T, Banin E, Rivolta C, Sharon D., Genet. Med. (), 2018
PMID: 29300381
Differential catalytic promiscuity of the alkaline phosphatase superfamily bimetallo core reveals mechanistic features underlying enzyme evolution.
Sunden F, AlSadhan I, Lyubimov A, Doukov T, Swan J, Herschlag D., J. Biol. Chem. 292(51), 2017
PMID: 29070681
Heterologous expression in Pichia pastoris and biochemical characterization of the unmodified sulfatase from Fusarium proliferatum LE1.
Korban SA, Bobrov KS, Maynskova MA, Naryzhny SN, Vlasova OL, Eneyskaya EV, Kulminskaya AA., Protein Eng. Des. Sel. 30(7), 2017
PMID: 28651356
Insights into Hunter syndrome from the structure of iduronate-2-sulfatase.
Demydchuk M, Hill CH, Zhou A, Bunkoczi G, Stein PE, Marchesan D, Deane JE, Read RJ., Nat Commun 8(), 2017
PMID: 28593992
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
Characterization of an arylsulfatase from a mutant library of Pseudoalteromonas carrageenovora arylsulfatase.
Zhu Y, Liu H, Qiao C, Li L, Jiang Z, Xiao A, Ni H., Int. J. Biol. Macromol. 96(), 2017
PMID: 27940339
Detection, production, and application of microbial arylsulfatases.
Stressler T, Seitl I, Kuhn A, Fischer L., Appl. Microbiol. Biotechnol. 100(21), 2016
PMID: 27654655
Chondroitin sulfate/dermatan sulfate sulfatases from mammals and bacteria.
Wang S, Sugahara K, Li F., Glycoconj. J. 33(6), 2016
PMID: 27526113
Striking Effects of Storage Buffers on Apparent Half-Lives of the Activity of Pseudomonas aeruginosa Arylsulfatase.
Li Y, Yang X, Wang D, Hu X, Yuan M, Pu J, Zhan CG, Yang Z, Liao F., Protein J. 35(4), 2016
PMID: 27372107
Stereochemistry and Mechanism of Enzymatic and Non-Enzymatic Hydrolysis of Benzylic sec-Sulfate Esters.
Toesch M, Schober M, Breinbauer R, Faber K., European J Org Chem 2014(18), 2014
PMID: 25232289
One-Pot Deracemization of sec-Alcohols: Enantioconvergent Enzymatic Hydrolysis of Alkyl Sulfates Using Stereocomplementary Sulfatases.
Schober M, Toesch M, Knaus T, Strohmeier GA, van Loo B, Fuchs M, Hollfelder F, Macheroux P, Faber K., Angew Chem Weinheim Bergstr Ger 125(11), 2013
PMID: 25821253
One-pot deracemization of sec-alcohols: enantioconvergent enzymatic hydrolysis of alkyl sulfates using stereocomplementary sulfatases.
Schober M, Toesch M, Knaus T, Strohmeier GA, van Loo B, Fuchs M, Hollfelder F, Macheroux P, Faber K., Angew. Chem. Int. Ed. Engl. 52(11), 2013
PMID: 23401148
Steroid derivatives as inhibitors of steroid sulfatase.
Mostafa YA, Taylor SD., J. Steroid Biochem. Mol. Biol. 137(), 2013
PMID: 23391659
Highly enantioselective stereo-inverting sec-alkylsulfatase activity of hyperthermophilic Archaea.
Wallner SR, Nestl BM, Faber K., Org. Biomol. Chem. 3(14), 2005
PMID: 15999201

36 References

Data provided by Europe PubMed Central.

Automated protein model building combined with iterative structure refinement.
Perrakis A, Morris R, Lamzin VS., Nat. Struct. Biol. 6(5), 1999
PMID: 10331874
SHELXL: high-resolution refinement.
Sheldrick GM, Schneider TR., Meth. Enzymol. 277(), 1997
PMID: 18488315
Assessment of phase accuracy by cross validation: the free R value. Methods and applications.
Brunger AT., Acta Crystallogr. D Biol. Crystallogr. 49(Pt 1), 1993
PMID: 15299543
1.7 Å structure of the stabilized REIv mutant T39K paper. Application of local NCS restraints
Usón, Acta Crystallogr. D 55(), 1997
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 RA, MacArthur MW, Moss DS, Thornton JM., J Appl Crystallogr 26(2), 1993
PMID: c6802
WHAT IF: a molecular modeling and drug design program.
Vriend G., J Mol Graph 8(1), 1990
PMID: 2268628
Conformation of polypeptides and proteins
Ramachandran, Adv. Protein Chem. 28(), 1968

Export

0 Marked Publications

Open Data PUB

Web of Science

View record in Web of Science®

Sources

PMID: 11435113
PubMed | Europe PMC

Search this title in

Google Scholar