Cited by 127Enzyme Structure and FunctionLysosomal Storage Disorders ResearchProtein Structure and Dynamics

The DOI matches its Crossref record; 52 of the 52 references it cites were found in a registry or an index.

Human sulfatases: A structural perspective to catalysis

Open access

Ghosh, D.·2007·Cellular and Molecular Life Sciences

DOI 10.1007/s00018-007-7175-yPMC PMC11136368

Open this paper in CoChat — free account

Abstract

The sulfatase family of enzymes catalyzes hydrolysis of sulfate ester bonds of a wide variety of substrates. Seventeen genes have been identified in this class of sulfatases, many of which are associated with genetic disorders leading to reduction or loss of function of the corresponding enzymes. Amino acid sequence homology suggests that the enzymes have similar overall folds, mechanisms of action, and bivalent metal ion-binding sites. A catalytic cysteine residue, strictly conserved in prokaryotic and eukaryotic sulfatases, is post-translationally modified into a formylglycine. Hydroxylation of the formylglycine residue by a water molecule forming the activated hydroxylformylglycine (a formylglycine hydrate or a gem-diol) is a necessary step for the enzyme's sulfatase activity. Crystal structures of three human sulfatases, arylsulfatases A and B(ARSA and ARSB), and estrone/dehydroepiandrosterone sulfatase or steroid sulfatase (STS), also known as arylsulfatase C, have been determined. While ARSA and ARSB are water-soluble enzymes, STS has a hydrophobic domain and is an integral membrane protein of the endoplasmic reticulum. In this article, we compare and contrast sulfatase structures and revisit the proposed catalytic mechanism in light of available structural and functional data. Examination of the STS active site reveals substrate-specific interactions previously identified as the estrogen-recognition motif. Because of the proximity of the catalytic cleft of STS to the membrane surface, the lipid bilayer has a critical role in the constitution of the active site, unlike other sulfatases.

Integrity signals

Registry

Crossref · 10.1007/s00018-007-7175-y

Cites

52 of 52 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

We couldn’t retrieve this paper’s full text, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Steroid sulfatase: molecular biology, regulation, and inhibition
Reed, M. J., Purohit, A., Woo, L. W. L., Newman, S. P., & Potter, B. V. L. (2005) · Endocrine Reviews · doi:10.1210/er.2004-0003 · Cited by 524
Multiple Sulfatase Deficiency Is Caused by Mutations in the Gene Encoding the Human Cα-Formylglycine Generating Enzyme
Dierks, T., Schmidt, B., Borissenko, L. V., Peng, J., Preusser-Kunze, A., Mariappan, M., & FIGURA, K. V. (2003) · Cell · doi:10.1016/s0092-8674(03)00347-7 · Cited by 384
The Multiple Sulfatase Deficiency Gene Encodes an Essential and Limiting Factor for the Activity of Sulfatases
Cosma, M. P., Pepe, S., Annunziata, I., Newbold, R. F., Grompe, M., Parenti, G., & Ballabio, A. (2003) · Cell · doi:10.1016/s0092-8674(03)00348-9 · Cited by 364
A novel amino acid modification in sulfatases that is defective in multiple sulfatase deficiency
Schmidt, B., Selmer, T., Ingendoh, A., & von Figurat, K. (1995) · Cell · doi:10.1016/0092-8674(95)90314-3 · Cited by 361
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. W., Selmer, T., Gieselmann, V., FIGURA, K. V., & Saenger, W. (1998) · Biochemistry · doi:10.1021/bi9714924 · Cited by 326
Structure of a human lysosomal sulfatase
Bond, C. S., Clements, P. R., Ashby, S., Collyer, C. A., Harrop, S. J., Hopwood, J. J., & Guss, J. M. (1997) · Structure · doi:10.1016/s0969-2126(97)00185-8 · Cited by 297
Phase I Study of STX 64 (667 Coumate) in Breast Cancer Patients: The First Study of a Steroid Sulfatase Inhibitor
Stanway, S. J., Purohit, A., Woo, L. W. L., Sufi, S., Vigushin, D. M., Ward, R. E., Wilson, R. H., Stanczyk, F. Z., Dobbs, N. A., Kulinskaya, E., et al. (2006) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-05-1996 · Cited by 244
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., FIGURA, K. V., Ficner, R., & Rudolph, M. G. (2005) · Cell · doi:10.1016/j.cell.2005.03.001 · Cited by 195
Estrogen sulfotransferase and steroid sulfatase in human breast carcinoma.
Suzuki, T., Nakata, T., Miki, Y., Kaneko, C., Moriya, T., Ishida, T., Akinaga, S., Hirakawa, H., Kimura, M., & Sasano, H. (2003) · PubMed · Cited by 185
1.3 Å 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 Bülow, R., Dierks, T., Schmidt, B., FIGURA, K. V., Kertesz, M. A., & Usón, I. (2001) · Structure · doi:10.1016/s0969-2126(01)00609-8 · Cited by 174
Inactivation of Steroid Sulfatase by an Active Site-Directed Inhibitor, Estrone-3-O-Sulfamate
Purohit, A., Williams, G. J., Howarth, N. M., Potter, B. V. L., & Reed, M. J. (1995) · Biochemistry · doi:10.1021/bi00036a025 · Cited by 171
The sulfatase gene family
Parenti, G., Meroni, G., & Ballabio, A. (1997) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(97)80153-0 · Cited by 171
Structure of Human Estrone Sulfatase Suggests Functional Roles of Membrane Association
Hernandez-Guzman, F. G., Higashiyama, T., Pangborn, W. A., Osawa, Y., & Ghosh, D. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m211497200 · Cited by 170
X-linked ichthyosis: an update
Hernández-Martín, �., González‐Sarmiento, R., & Unamuno, D. (1999) · British Journal of Dermatology · doi:10.1046/j.1365-2133.1999.03098.x · Cited by 156
Breast Cancer and the Role of Cytokines in Regulating Estrogen Synthesis: An Emerging Hypothesis
Reed, M. J., & Purohit, A. (1997) · Endocrine Reviews · doi:10.1210/edrv.18.5.0314 · Cited by 134
Structure of the ternary complex of human 17β-hydroxysteroid dehydrogenase type 1 with 3-hydroxyestra-1,3,5,7-tetraen-17-one (equilin) and NADP +
Sawicki, M. W., Erman, M., Puranen, T., Vihko, P., & Ghosh, D. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.3.840 · Cited by 113
Self-citation
2-Substituted 4-(Thio)chromenone 6-O-Sulfamates: Potent Inhibitors of Human Steroid Sulfatase
Nußbaumer, P., Lehr, P., & Billich, A. (2002) · Journal of Medicinal Chemistry · doi:10.1021/jm020878w · Cited by 112
Cloning and Expression of Human Steroid-sulfatase
Stein, C., Hille‐Rehfeld, A., Seidel, J., Rijnboutt, S., Waheed, A., Schmidt, B., Geuze, H. J., & FIGURA, K. V. (1989) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)80080-1 · Cited by 110
Steroid sulfatase inhibitors
Nußbaumer, P., & Billich, A. (2004) · Medicinal Research Reviews · doi:10.1002/med.20008 · Cited by 108
Crystal Structure of an Enzyme-Substrate Complex Provides Insight into the Interaction between Human Arylsulfatase A and its Substrates During Catalysis
von Bülow, R., Schmidt, B., Dierks, T., FIGURA, K. V., & Usón, I. (2001) · Journal of Molecular Biology · doi:10.1006/jmbi.2000.4297 · Cited by 106
High expression of steroid sulfatase mRNA predicts poor prognosis in patients with estrogen receptor-positive breast cancer.
Miyoshi, Y., Ando, A., Hasegawa, S., Ishitobi, M., Taguchi, T., Tamaki, Y., & Noguchi, S. (2003) · PubMed · Cited by 99
Stimulation of MCF-7 breast cancer cell proliferation by estrone sulfate and dehydroepiandrosterone sulfate: inhibition by novel non-steroidal steroid sulfatase inhibitors
Billich, A., Nußbaumer, P., & Lehr, P. (2000) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/s0960-0760(00)00077-7 · Cited by 96
Sulfatases, Trapping of the Sulfated Enzyme Intermediate by Substituting the Active Site Formylglycine
Recksiek, M., Selmer, T., Dierks, T., Schmidt, B., & FIGURA, K. V. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.11.6096 · Cited by 91
Structure−Activity Relationships of 17α-Derivatives of Estradiol as Inhibitors of Steroid Sulfatase
Boivin, R. P., Luu-The, V., Lachance, R., Labrie, F., & Poirier, D. (2000) · Journal of Medicinal Chemistry · doi:10.1021/jm0001166 · Cited by 86
Steroid sulfatase and estrogen sulfotransferase in human endometrial carcinoma
Utsunomiya, H., Ito, K., Suzuki, T., Kitamura, T., Kaneko, C., Nakata, T., Niikura, H., Okamura, K., Yaegashi, N., & Sasano, H. (2004) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-04-0040 · Cited by 85
Characterization of Point Mutations in Patients with X-linked Ichthyosis
Alperin, E. S., & Shapiro, L. J. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.33.20756 · Cited by 77
The selective estrogen enzyme modulator (SEEM) in breast cancer
Chetrite, G. S., & Pasqualini, J. R. (2001) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/s0960-0760(01)00046-2 · Cited by 68
Purification, characterization and crystallization of human placental estrone/dehydroepiandrosterone sulfatase, a membrane-bound enzyme of the endoplasmic reticulum
Hernandez-Guzman, F. G., Higashiyama, T., Osawa, Y., & Ghosh, D. (2001) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/s0960-0760(01)00119-4 · Cited by 65
Steroid sulfatase and estrogen sulfotransferase in human prostate cancer
Nakamura, Y., Suzuki, T., Fukuda, T., Ito, A., Endo, M., Moriya, T., Arai, Y., & Sasano, H. (2006) · The Prostate · doi:10.1002/pros.20426 · Cited by 59
Catalytic Mechanism of a C−C Hydrolase Enzyme: Evidence for aGem-Diol Intermediate, Not an Acyl Enzyme
Fleming, S. M., Robertson, T. A., Langley, G. J., & Bugg, T. D. H. (2000) · Biochemistry · doi:10.1021/bi9923095 · Cited by 58
The role of STS and OATP-B mRNA expression in predicting the clinical outcome in human breast cancer.
Sarakbi, W. A., Mokbel, R., Salhab, M., Jiang, W. G., Reed, M. J., & Mokbel, K. (2006) · PubMed · Cited by 57
In vivo Efficacy of STX213, A Second-Generation Steroid Sulfatase Inhibitor, for Hormone-Dependent Breast Cancer Therapy
Foster, P., Newman, S. P., Chander, S. K., Stengel, C., Jhalli, R., Woo, L. W. L., Potter, B. V. L., Reed, M. J., & Purohit, A. (2006) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-06-0632 · Cited by 56
Purification and partial characterization of arylsulphatase C from human placental microsomes
BURNS, G. (1983) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/0304-4165(83)90313-6 · Cited by 46
Boronic acids as inhibitors of steroid sulfatase
Ahmed, V. F., Liu, Y., Silvestro, C., & Taylor, S. D. (2006) · Bioorganic & Medicinal Chemistry · doi:10.1016/j.bmc.2006.08.033 · Cited by 45
Three‐Dimensional Structures of Sulfatases
Ghosh, D. (2005) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(05)00016-9 · Cited by 44
A novel dual-target steroid sulfatase inhibitor and antiestrogen: SR 16157, a promising agent for the therapy of breast cancer
Rasmussen, L. M., Zaveri, N. T., Stenvang, J., Peters, R. H., & Lykkesfeldt, A. E. (2007) · Breast Cancer Research and Treatment · doi:10.1007/s10549-007-9494-y · Cited by 44
Crystal structure of a covalent intermediate of endogenous human arylsulfatase A
Chruszcz, M., Laidler, P. M., Monkiewicz, M., Ortlund, E. A., Lebioda, L., & Lewiński, K. (2003) · Journal of Inorganic Biochemistry · doi:10.1016/s0162-0134(03)00176-4 · Cited by 44
Inhibition of steryl sulfatase activity in LNCaP human prostate cancer cells
Selcer, K. W. (2002) · Steroids · doi:10.1016/s0039-128x(02)00030-2 · Cited by 42
Human Placental Steryl-Sulfatase. Enzyme Purification, Production of Antisera, and Immunoblotting Reactions with Normal and Sulfatase-Deficient Placentas
DIBBELT, L., & Kuss, E. (1986) · Biological Chemistry Hoppe-Seyler · doi:10.1515/bchm3.1986.367.2.1223 · Cited by 42
Human placental steroid sulfatase: Purification and properties
Noël, H., Plante, L., Bleau, G., Chapdelaine, A., & Roberts, K. D. (1983) · Journal of Steroid Biochemistry · doi:10.1016/0022-4731(83)90375-8 · Cited by 39
The difluoromethylene group as a replacement for the labile oxygen in steroid sulfates: a new approach to steroid sulfatase inhibitors
Lapierre, J., Ahmed, V. F., Chen, M.-J., Ispahany, M., Guillemette, J. G., & Taylor, S. D. (2003) · Bioorganic & Medicinal Chemistry Letters · doi:10.1016/j.bmcl.2003.09.089 · Cited by 38
Measuring the Activities of the Sulfs: Two Novel Heparin/Heparan Sulfate Endosulfatases
Uchimura, K., Morimoto‐Tomita, M., & Rosen, S. D. (2006) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(06)16015-2 · Cited by 36
Purification and Properties of Arylsulfatase C from Human Placenta
Vaccaro, A. M., Salvioli, R., Muscillo, M., & Renola, L. (2017) · Enzyme · doi:10.1159/000469248 · Cited by 34
A novel steroidal selective steroid sulfatase inhibitor KW-2581 inhibits sulfated-estrogen dependent growth of breast cancer cells in vitro and in animal models
Ishida, H., Nakata, T., Suzuki, M., Shiotsu, Y., Tanaka, H., Sato, N., Terasaki, Y., Takebayashi, M., Anazawa, H., Murakata, C., et al. (2007) · Breast Cancer Research and Treatment · doi:10.1007/s10549-007-9495-x · Cited by 31
Evidence for a gem-Diol Reaction Intermediate in Bacterial C−C Hydrolase Enzymes BphD and MhpC from 13C NMR Spectroscopy
Li, J., Li, C., Blindauer, C. A., & Bugg, T. D. H. (2006) · Biochemistry · doi:10.1021/bi0612519 · Cited by 31
Synthesis of a non-hydrolyzable estrone sulfate analogue bearing the difluoromethanesulfonamide group and its evaluation as a steroid sulfatase inhibitor
Liu, Y., Ahmed, V. F., Hill, B., & Taylor, S. D. (2005) · Organic & Biomolecular Chemistry · doi:10.1039/b508852f · Cited by 28
Human placental steroid sulphatase—purification and monospecific antibody production in rabbits
van der Loos, C. M., van Breda, A. J., van den Berg, F. M., Walboomers, J. M. M., & Jöbsis, A. C. (1984) · Journal of Inherited Metabolic Disease · doi:10.1007/bf01801762 · Cited by 26
Steroid sulphatase: expression, isolation and inhibition for active-site identification studies
Purohit, A., Potter, B. V. L., Parker, M. G., & Reed, M. J. (1998) · Chemico-Biological Interactions · doi:10.1016/s0009-2797(97)00132-4 · Cited by 26
Purification and Properties of Steroid Sulfatase from Human Placenta.
Suzuki, T., HIRATO, K., Yanaihara, T., Kadofuku, T., Sato, T., Hoshino, M., & Yanaihara, N. (1992) · Endocrinologia Japonica · doi:10.1507/endocrj1954.39.93 · Cited by 25
Inhibition of estrone sulfatase by aromatase inhibitor-based estrogen 3-sulfamates
Numazawa, M., Tominaga, T., Watari, Y., & Tada, Y. (2006) · Steroids · doi:10.1016/j.steroids.2005.12.004 · Cited by 25
Localization and expression of steroid sulfatase in human fallopian tubes
Yanaihara, A., Yanaihara, T., Toma, Y., Shimizu, Y., Saito, H., Okai, T., Higashiyama, T., & Osawa, Y. (2001) · Steroids · doi:10.1016/s0039-128x(00)00204-x · Cited by 22
Mutations in X-linked ichthyosis disrupt the active site structure of estrone/DHEA sulfatase
Ghosh, D. (2004) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2004.09.003 · Cited by 19

Sorted by citations

Sorting of lysosomal proteins
Braulke, T., & Bonifacino, J. S. (2009) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2008.10.016 · Cited by 811
RadicalS-Adenosylmethionine Enzymes
Broderick, J. B., Duffus, B. R., Duschene, K. S., & Shepard, E. M. (2014) · Chemical Reviews · doi:10.1021/cr4004709 · Cited by 843
The Regulation of Steroid Action by Sulfation and Desulfation
Mueller, J. W., Gilligan, L. C., Idkowiak, J., Arlt, W., & Foster, P. A. (2015) · Endocrine Reviews · doi:10.1210/er.2015-1036 · Cited by 419
Intracrine androgen biosynthesis, metabolism and action revisited
Schiffer, L., Arlt, W., & Storbeck, K.-H. (2018) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2017.08.016 · Cited by 217
“STS is a membrane-bound enzyme on the luminal side of the endoplasmic reticulum (Ghosh, 2007) and ubiquitously expressed in all human tissues (Reed et al., 2005).”
The structural biology of oestrogen metabolism
THOMAS, M. P., & Potter, B. V. L. (2013) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2012.12.014 · Cited by 181

See all 127

Authors: Ghosh, D.
Affiliations: Hauptman-Woodward Medical Research Institute (US)
Corresponding author: Ghosh, D.
ORCID: Ghosh, D.
Venue: Cellular and Molecular Life Sciences
Publisher: Springer Science and Business Media LLC
Published: 2007-06-11
Volume: 64
Issue: 15
Pages: 2013-2022
ISSN: 1420-682X (ISSN-L)
1420-9071
DOI: 10.1007/s00018-007-7175-y
PMC: PMC11136368
OpenAlex: W2007796873
Cited by: 123
References: 52
Citations by year: 2026: 3 · 2025: 2 · 2024: 5 · 2023: 8 · 2022: 4 · 2021: 3 · 2020: 9 · 2019: 5 · 2018: 5 · 2017: 2 · 2016: 8 · 2015: 7 · 2014: 12 · 2013: 11 · 2012: 5
FWCI: 4.97
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
Locations: Cellular and Molecular Life Sciences (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute of General Medical Sciences (R01GM062794, GM62794)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Structural Biology › Enzyme Structure and Function
Health Sciences › Medicine › Genetics (clinical) › Lysosomal Storage Disorders Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Structure and Dynamics
Keywords: sulfatase, enzyme mechanism, formylglycine, arylsulfatase A, arylsulfatase B, steroid sulfatase, estrone sulfatase, arylsulfatase C, crystal structure, active site, endoplasmic reticulum membrane protein, lipid bilayers, genetic disorders
MeSH terms: Amino Acids, Breast Neoplasms, Catalysis, Cerebroside-Sulfatase, Female, Humans, Male, Models, Molecular, Pregnancy, Prostatic Neoplasms, Sulfatases, Protein Structure, Tertiary, Crystallography, X-Ray, N-Acetylgalactosamine-4-Sulfatase, Catalytic Domain, Steryl-Sulfatase, Static Electricity, In Vitro Techniques

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Human sulfatases: A structural perspective to catalysis

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cites

Cited by

Related

Metadata

Record

About these checks