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The molecular basis for the broad substrate specificity of human sulfotransferase 1A1.

Berger I, Guttman C, Amar D, Zarivach R, Aharoni A
PLoS One 6 e26794 (2011)
Related entries: 3u3j, 3u3k, 3u3o, 3u3r

Cited: 35 times
EuropePMC logo PMID: 22069470

Abstract

Cytosolic sulfotransferases (SULTs) are mammalian enzymes that detoxify a wide variety of chemicals through the addition of a sulfate group. Despite extensive research, the molecular basis for the broad specificity of SULTs is still not understood. Here, structural, protein engineering and kinetic approaches were employed to obtain deep understanding of the molecular basis for the broad specificity, catalytic activity and substrate inhibition of SULT1A1. We have determined five new structures of SULT1A1 in complex with different acceptors, and utilized a directed evolution approach to generate SULT1A1 mutants with enhanced thermostability and increased catalytic activity. We found that active site plasticity enables binding of different acceptors and identified dramatic structural changes in the SULT1A1 active site leading to the binding of a second acceptor molecule in a conserved yet non-productive manner. Our combined approach highlights the dominant role of SULT1A1 structural flexibility in controlling the specificity and activity of this enzyme.

Reviews - 3u3m mentioned but not cited (3)

  1. The structural biology of oestrogen metabolism. Thomas MP, Potter BV. J Steroid Biochem Mol Biol 137 27-49 (2013)
  2. Sulfation pathways from red to green. Günal S, Hardman R, Kopriva S, Mueller JW. J Biol Chem 294 12293-12312 (2019)
  3. From Steroid and Drug Metabolism to Glycobiology, Using Sulfotransferase Structures to Understand and Tailor Function. Pedersen LC, Yi M, Pedersen LG, Kaminski AM. Drug Metab Dispos 50 1027-1041 (2022)

Articles - 3u3m mentioned but not cited (2)

  1. Insights into the substrate binding mechanism of SULT1A1 through molecular dynamics with excited normal modes simulations. Dudas B, Toth D, Perahia D, Nicot AB, Balog E, Miteva MA. Sci Rep 11 13129 (2021)
  2. Celecoxib influences steroid sulfonation catalyzed by human recombinant sulfotransferase 2A1. Ambadapadi S, Wang PL, Palii SP, James MO. J Steroid Biochem Mol Biol 152 101-113 (2015)


Reviews citing this publication (10)

  1. The Regulation of Steroid Action by Sulfation and Desulfation. Mueller JW, Gilligan LC, Idkowiak J, Arlt W, Foster PA. Endocr Rev 36 526-563 (2015)
  2. The multi-protein family of sulfotransferases in plants: composition, occurrence, substrate specificity, and functions. Hirschmann F, Krause F, Papenbrock J. Front Plant Sci 5 556 (2014)
  3. Interactions of cytosolic sulfotransferases with xenobiotics. James MO, Ambadapadi S. Drug Metab Rev 45 401-414 (2013)
  4. Crystal structures of human sulfotransferases: insights into the mechanisms of action and substrate selectivity. Dong D, Ako R, Wu B. Expert Opin Drug Metab Toxicol 8 635-646 (2012)
  5. SULFATION PATHWAYS: Insights into steroid sulfation and desulfation pathways. Foster PA, Mueller JW. J Mol Endocrinol 61 T271-T283 (2018)
  6. Structure, dynamics and selectivity in the sulfotransferase family. Leyh TS, Cook I, Wang T. Drug Metab Rev 45 423-430 (2013)
  7. Understanding substrate selectivity of human UDP-glucuronosyltransferases through QSAR modeling and analysis of homologous enzymes. Dong D, Ako R, Hu M, Wu B. Xenobiotica 42 808-820 (2012)
  8. Mechanism of sulfotransferase pharmacogenetics in altered xenobiotic metabolism. Chen BH, Wang CC, Hou YH, Mao YC, Yang YS. Expert Opin Drug Metab Toxicol 11 1053-1071 (2015)
  9. Intra-site differential inhibition of multi-specific enzymes. Cappiello M, Balestri F, Moschini R, Mura U, Del-Corso A. J Enzyme Inhib Med Chem 35 840-846 (2020)
  10. Employing directed evolution for the functional analysis of multi-specific proteins. Levin M, Amar D, Aharoni A. Bioorg Med Chem 21 3511-3516 (2013)

Articles citing this publication (20)

  1. The gate that governs sulfotransferase selectivity. Cook I, Wang T, Almo SC, Kim J, Falany CN, Leyh TS. Biochemistry 52 415-424 (2013)
  2. Identification of sulfated metabolites of 4-chlorobiphenyl (PCB3) in the serum and urine of male rats. Dhakal K, He X, Lehmler HJ, Teesch LM, Duffel MW, Robertson LW. Chem Res Toxicol 25 2796-2804 (2012)
  3. Structural and Dynamic Characterizations Highlight the Deleterious Role of SULT1A1 R213H Polymorphism in Substrate Binding. Dash R, Ali MC, Dash N, Azad MAK, Hosen SMZ, Hannan MA, Moon IS. Int J Mol Sci 20 E6256 (2019)
  4. Sulphation of acetaminophen by the human cytosolic sulfotransferases: a systematic analysis. Yamamoto A, Liu MY, Kurogi K, Sakakibara Y, Saeki Y, Suiko M, Liu MC. J Biochem 158 497-504 (2015)
  5. The allosteric binding sites of sulfotransferase 1A1. Cook I, Wang T, Falany CN, Leyh TS. Drug Metab Dispos 43 418-423 (2015)
  6. Directed evolution of a soluble human IL-17A receptor for the inhibition of psoriasis plaque formation in a mouse model. Zaretsky M, Etzyoni R, Kaye J, Sklair-Tavron L, Aharoni A. Chem Biol 20 202-211 (2013)
  7. In silico mechanistic profiling to probe small molecule binding to sulfotransferases. Martiny VY, Carbonell P, Lagorce D, Villoutreix BO, Moroy G, Miteva MA. PLoS One 8 e73587 (2013)
  8. Unleashing the potential of noncanonical amino acid biosynthesis to create cells with precision tyrosine sulfation. Chen Y, Jin S, Zhang M, Hu Y, Wu KL, Chung A, Wang S, Tian Z, Wang Y, Wolynes PG, Xiao H. Nat Commun 13 5434 (2022)
  9. A measure of the broad substrate specificity of enzymes based on 'duplicate' catalytic residues. Chakraborty S, Ásgeirsson B, Rao BJ. PLoS One 7 e49313 (2012)
  10. Expression of the orphan cytosolic sulfotransferase SULT1C3 in human intestine: characterization of the transcript variant and implications for function. Duniec-Dmuchowski Z, Rondini EA, Tibbs ZE, Falany CN, Runge-Morris M, Kocarek TA. Drug Metab Dispos 42 352-360 (2014)
  11. A robust protocol for directed aryl sulfotransferase evolution toward the carbohydrate building block GlcNAc. Islam S, Mate DM, Martínez R, Jakob F, Schwaneberg U. Biotechnol Bioeng 115 1106-1115 (2018)
  12. An activity-based fluorescent sensor for the detection of the phenol sulfotransferase SULT1A1 in living cells. Baglia RA, Mills KR, Mitra K, Tutol JN, Ball D, Page KM, Kallu J, Gottipolu S, D'Arcy S, Nielsen SO, Dodani SC. RSC Chem Biol 2 830-834 (2021)
  13. 3D-QSAR studies on UDP-glucuronosyltransferase 2B7 substrates using the pharmacophore and VolSurf approaches. Ako R, Dong D, Wu B. Xenobiotica 42 891-900 (2012)
  14. Impact of dietary interventions on pre-diabetic oral and gut microbiome, metabolites and cytokines. Shoer S, Shilo S, Godneva A, Ben-Yacov O, Rein M, Wolf BC, Lotan-Pompan M, Bar N, Weiss EI, Houri-Haddad Y, Pilpel Y, Weinberger A, Segal E. Nat Commun 14 5384 (2023)
  15. SULT1A1-dependent sulfonation of alkylators is a lineage-dependent vulnerability of liver cancers. Shi L, Shen W, Davis MI, Kong K, Vu P, Saha SK, Adil R, Kreuzer J, Egan R, Lee TD, Greninger P, Shrimp JH, Zhao W, Wei TY, Zhou M, Eccleston J, Sussman J, Manocha U, Weerasekara V, Kondo H, Vijay V, Wu MJ, Kearney SE, Ho J, McClanaghan J, Murchie E, Crowther GS, Patnaik S, Boxer MB, Shen M, Ting DT, Kim WY, Stanger BZ, Deshpande V, Ferrone CR, Benes CH, Haas W, Hall MD, Bardeesy N. Nat Cancer 4 365-381 (2023)
  16. Secretory expression of the rat aryl sulfotransferases IV with improved catalytic efficiency by molecular engineering. Zhou Z, Li Q, Xu R, Wang B, Du G, Kang Z. 3 Biotech 9 246 (2019)
  17. The impact of ligands on the structure and flexibility of sulfotransferases: a molecular dynamics simulation study. Zhao L, Zhang P, Long S, Wang L, Tian P. J Mol Model 21 190 (2015)
  18. Metabolic Activation of Heterocyclic Amines and Expression of Xenobiotic-Metabolizing Enzymes in the Gastrointestinal Tract of Rats. Darwish WS, Nakayama SM, Itotani Y, Ohno M, Ikenaka Y, Ishizuka M. J Food Sci 80 T1627-32 (2015)
  19. Role of Conformational Dynamics of Sulfotransferases SULT1A1 and SULT1A3 in Substrate Specificity. Toth D, Dudas B, Miteva MA, Balog E. Int J Mol Sci 24 16900 (2023)
  20. The effect of ligands on the thermal stability of sulfotransferases: a molecular dynamics simulation study. Zhang PP, Zhao L, Long SY, Tian P. J Mol Model 21 72 (2015)


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