Tyrosine Sulfation As a Protein Post-translational Modification

Overview

Journal Molecules

Publisher MDPI

Specialty Biology

Date 2015 Jan 31

PMID 25635379

Citations 52

Authors

Yuh-Shyong Yang

Chen-Chu Wang

Bo-Han Chen

You-Hua Hou

Kuo-Sheng Hung

Yi-Chih Mao

Affiliations

Soon will be listed here.

Abstract

Integration of inorganic sulfate into biological molecules plays an important role in biological systems and is directly involved in the instigation of diseases. Protein tyrosine sulfation (PTS) is a common post-translational modification that was first reported in the literature fifty years ago. However, the significance of PTS under physiological conditions and its link to diseases have just begun to be appreciated in recent years. PTS is catalyzed by tyrosylprotein sulfotransferase (TPST) through transfer of an activated sulfate from 3'-phosphoadenosine-5'-phosphosulfate to tyrosine in a variety of proteins and peptides. Currently, only a small fraction of sulfated proteins is known and the understanding of the biological sulfation mechanisms is still in progress. In this review, we give an introductory and selective brief review of PTS and then summarize the basic biochemical information including the activity and the preparation of TPST, methods for the determination of PTS, and kinetics and reaction mechanism of TPST. This information is fundamental for the further exploration of the function of PTS that induces protein-protein interactions and the subsequent biochemical and physiological reactions.

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References

Matsubayashi Y . MBSJ MCC Young Scientist Award 2010. Recent progress in research on small post-translationally modified peptide signals in plants. Genes Cells. 2012; 17(1):1-10. DOI: 10.1111/j.1365-2443.2011.01569.x. View

Nishimura Y, Shimojima M, Tano Y, Miyamura T, Wakita T, Shimizu H . Human P-selectin glycoprotein ligand-1 is a functional receptor for enterovirus 71. Nat Med. 2009; 15(7):794-7. DOI: 10.1038/nm.1961. View

Bossio R, Marshall A . Baseline resolution of isobaric phosphorylated and sulfated peptides and nucleotides by electrospray ionization FTICR ms: another step toward mass spectrometry-based proteomics. Anal Chem. 2002; 74(7):1674-9. DOI: 10.1021/ac0108461. View

Kim D, Konishi L, KOBASHI K . Purification, characterization and reaction mechanism of novel arylsulfotransferase obtained from an anaerobic bacterium of human intestine. Biochim Biophys Acta. 1986; 872(1-2):33-41. DOI: 10.1016/0167-4838(86)90144-5. View

Stuhrwohldt N, Dahlke R, Kutschmar A, Peng X, Sun M, Sauter M . Phytosulfokine peptide signaling controls pollen tube growth and funicular pollen tube guidance in Arabidopsis thaliana. Physiol Plant. 2014; 153(4):643-53. DOI: 10.1111/ppl.12270. View

Mishiro E, Sakakibara Y, Liu M, Suiko M . Differential enzymatic characteristics and tissue-specific expression of human TPST-1 and TPST-2. J Biochem. 2006; 140(5):731-7. DOI: 10.1093/jb/mvj206. View

Taylor S, Sun C, Hsieh A, Andon N, Ghosh S . A sulfated, phosphorylated 7 kDa secreted peptide characterized by direct analysis of cell culture media. J Proteome Res. 2008; 7(2):795-802. DOI: 10.1021/pr7006686. View

Chen B, Wang C, Lu L, Hung K, Yang Y . Fluorescence assay for protein post-translational tyrosine sulfation. Anal Bioanal Chem. 2012; 405(4):1425-9. DOI: 10.1007/s00216-012-6540-3. View

Preobrazhensky A, Dragan S, Kawano T, Gavrilin M, Gulina I, Chakravarty L . Monocyte chemotactic protein-1 receptor CCR2B is a glycoprotein that has tyrosine sulfation in a conserved extracellular N-terminal region. J Immunol. 2000; 165(9):5295-303. DOI: 10.4049/jimmunol.165.9.5295. View

10.

Lu L, Chen B, Wu J, Wang C, Chen D, Yang Y . Implantation of post-translational tyrosylprotein sulfation into a prokaryotic expression system. Chembiochem. 2011; 12(3):377-9. DOI: 10.1002/cbic.201000540. View

11.

Hille A, Braulke T, von Figura K, Huttner W . Occurrence of tyrosine sulfate in proteins--a balance sheet. 1. Secretory and lysosomal proteins. Eur J Biochem. 1990; 188(3):577-86. DOI: 10.1111/j.1432-1033.1990.tb15438.x. View

12.

William S, Ramaprasad P, Kasinathan C . Purification of tyrosylprotein sulfotransferase from rat submandibular salivary glands. Arch Biochem Biophys. 1997; 338(1):90-6. DOI: 10.1006/abbi.1996.9800. View

13.

Lu L, Hsu Y, Yang Y . Spectrofluorometric assay for monoamine-preferring phenol sulfotransferase (SULT1A3). Anal Biochem. 2010; 404(2):241-3. DOI: 10.1016/j.ab.2010.06.001. View

14.

Ludeman J, Stone M . The structural role of receptor tyrosine sulfation in chemokine recognition. Br J Pharmacol. 2013; 171(5):1167-79. PMC: 3952796. DOI: 10.1111/bph.12455. View

15.

Dong J, Ye P, Schade A, Gao S, Romo G, Turner N . Tyrosine sulfation of glycoprotein I(b)alpha. Role of electrostatic interactions in von Willebrand factor binding. J Biol Chem. 2001; 276(20):16690-4. DOI: 10.1074/jbc.M101035200. View

16.

Kim T, Kim D, Nam H, Park S, Shim J, Cho J . Tyrosylprotein sulfotransferase regulates collagen secretion in Caenorhabditis elegans. Mol Cells. 2010; 29(4):413-8. DOI: 10.1007/s10059-010-0049-4. View

17.

Toesch M, Schober M, Faber K . Microbial alkyl- and aryl-sulfatases: mechanism, occurrence, screening and stereoselectivities. Appl Microbiol Biotechnol. 2013; 98(4):1485-96. PMC: 3920027. DOI: 10.1007/s00253-013-5438-0. View

18.

Kehoe J, Bertozzi C . Tyrosine sulfation: a modulator of extracellular protein-protein interactions. Chem Biol. 2000; 7(3):R57-61. DOI: 10.1016/s1074-5521(00)00093-4. View

19.

Stuhrwohldt N, Dahlke R, Steffens B, Johnson A, Sauter M . Phytosulfokine-α controls hypocotyl length and cell expansion in Arabidopsis thaliana through phytosulfokine receptor 1. PLoS One. 2011; 6(6):e21054. PMC: 3116886. DOI: 10.1371/journal.pone.0021054. View

20.

Westmuckett A, Thacker K, Moore K . Tyrosine sulfation of native mouse Psgl-1 is required for optimal leukocyte rolling on P-selectin in vivo. PLoS One. 2011; 6(5):e20406. PMC: 3102115. DOI: 10.1371/journal.pone.0020406. View