Mass Spectrometric Kinetic Analysis of Human Tyrosylprotein Sulfotransferase-1 and -2

Journal of the American Society for Mass Spectrometry

Volumn 19, Issue 10, 2008, Pages 1459-1466

  Danan, Lieza M ^a   Yu, Zhihao ^a   Hoffhines, Adam J ^c   Moore, Kevin L ^b,c,d   Leary, Julie A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

^c UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY OF OKLAHOMA HEALTH SCIENCES CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINES; CATALYSTS; CHROMATOGRAPHIC ANALYSIS; ELECTROSPRAY IONIZATION; ENZYMES; ESTERS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IONIZATION OF LIQUIDS; LIQUID CHROMATOGRAPHY; MASS SPECTROMETERS; MASS SPECTROMETRY; ORGANIC COMPOUNDS; PROTEINS; SPECTROMETRY;

ALLERGIC INFLAMMATION; ATHEROGENESIS; CHEMOKINE RECEPTORS; G-PROTEIN-COUPLED RECEPTORS; HYDROXYL GROUPS; KINETIC ANALYSES; KINETIC PROPERTIES; LC/ESI-MS; LIQUID CHROMATOGRAPHY ELECTROSPRAY; POST-TRANSLATIONAL MODIFICATIONS; SULFOTRANSFERASE; TYROSINE RESIDUES;

AMINO ACIDS;

CHEMOKINE RECEPTOR CCR8; ISOENZYME; SULFOTRANSFERASE; TYROSYLPROTEIN SULFOTRANSFERASE PROTEIN 1; TYROSYLPROTEIN SULFOTRANSFERASE PROTEIN 2; UNCLASSIFIED DRUG;

ANALYTIC METHOD; ARTICLE; ELECTROSPRAY MASS SPECTROMETRY; ENZYME ASSAY; HUMAN; KINETICS; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY;

CATALYSIS; CHROMATOGRAPHY, LIQUID; HUMANS; KINETICS; MEMBRANE PROTEINS; PHOSPHOADENOSINE PHOSPHOSULFATE; RECOMBINANT PROTEINS; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; SULFOTRANSFERASES;

EID: 53149153135     PISSN: 10440305     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jasms.2008.06.021     Document Type: Article

References (50)

1. Huttner W.B. Sulfation of Tyrosine Residues-a Widespread Modification of Proteins. Nature 299 (1982) 273-276
2. Baeuerle P.A., and Huttner W.B. Tyrosine Sulfation of Yolk Proteins 1, 2, and 3 in Drosophila melanogaster. J. Biol. Chem. 260 (1985) 6434-6439
3. Hille A., Rosa P., and Huttner W.B. Tyrosine Sulfation: A Post-Translational Modification of Proteins Destined for Secretion?. FEBS Lett. 177 (1984) 129-134
4. Hille A., Braulke T., von Figura K., and Huttner W.B. Occurrence of Tyrosine Sulfate in Proteins-A Balance Sheet. 1. Secretory and Lysosomal Proteins. Eur. J. Biochem. 188 (1990) 577-586
5. Hille A., and Huttner W.B. Occurrence of Tyrosine Sulfate in Proteins-A Balance Sheet. 2. Membrane Proteins. Eur. J. Biochem. 188 (1990) 587-596
6. Moore K.L. The Biology and Enzymology of Protein Tyrosine O-Sulfation. J Biol. Chem. 278 (2003) 24243-24246
7. Huttner W.B. Tyrosine Sulfation and the Secretory Pathway. Annu. Rev. Physiol. 50 (1988) 363-376
8. Walsh G., and Jefferis R. Post-Translational Modifications in the Context of Therapeutic Proteins. Nat. Biotechnol. 24 (2006) 1241-1252
9. Kehoe J.W., and Bertozzi C.R. Tyrosine Sulfation: A Modulator of Extracellular Protein-Protein Interactions. Chem. Biol. 7 (2000) R57-R61
10. Rossi D., and Zlotnik A. The Biology of Chemokines and Their Receptors. Annu. Rev. Immunol. 18 (2000) 217-242
11. Monigatti F., Hekking B., and Steen H. Protein Sulfation Analysis-A Primer. Biochim. Biophys. Acta 1764 (2006) 1904-1913
12. Preobrazhensky A.A., Dragan S., Kawano T., Gavrilin M.A., Gulina I.V., Chakravarty L., and Kolattukudy P.E. Monocyte Chemotactic Protein-1 Receptor Ccr2b Is a Glycoprotein That Has Tyrosine Sulfation in a Conserved Extracellular N-Terminal Region. J. Immunol. 165 (2000) 5295-5303
13. Gutierrez J., Kremer L., Zaballos A., Goya I., Martinez A.C., and Marquez G. Analysis of Post-Translational Ccr8 Modifications and Their Influence on Receptor Activity. J. Biol. Chem. 279 (2004) 14726-14733
14. Colvin R.A., Campanella G.S., Manice L.A., and Luster A.D. Cxcr3 Requires Tyrosine Sulfation for Ligand Binding and a Second Extracellular Loop Arginine Residue for Ligand-Induced Chemotaxis. Mol. Cell. Biol. 26 (2006) 5838-5849
15. Feng Y., Broder C.C., Kennedy P.E., and Berger E.A. Hiv-1 Entry Cofactor: Functional cDNA Cloning of a Seven-Transmembrane, G Protein-Coupled Receptor. Science 272 (1996) 872-877
16. Farzan M., Mirzabekov T., Kolchinsky P., Wyatt R., Cayabyab M., Gerard N.P., Gerard C., Sodroski J., and Choe H. Tyrosine Sulfation of the Amino Terminus of Ccr5 Facilitates HIV-1 Entry. Cell 96 (1999) 667-676
17. Farzan M., Babcock G.J., Vasilieva N., Wright P.L., Kiprilov E., Mirzabekov T., and Choe H. The Role of Post-Translational Modifications of the Cxcr4 Amino Terminus in Stromal-Derived Factor 1 α Association and HIV-1 Entry. J. Biol. Chem. 277 (2002) 29484-29489
18. Deng H., Liu R., Ellmeier W., Choe S., Unutmaz D., Burkhart M., Di Marzio P., Marmon S., Sutton R.E., Hill C.M., Davis C.B., Peiper S.C., Schall T.J., Littman D.R., and Landau N.R. Identification of a Major Co-Receptor for Primary Isolates of HIV-1. Nature 381 (1996) 661-666
19. Lusso P. HIV and the Chemokine System: 10 Years Later. EMBO J. 25 (2006) 447-456
20. Lee R.W., and Huttner W.B. Tyrosine-O-Sulfated Proteins of Pc12 Pheochromocytoma Cells and Their Sulfation by a Tyrosylprotein Sulfotransferase. J. Biol. Chem. 258 (1983) 11326-11334
21. Baeuerle P.A., and Huttner W.B. Tyrosine Sulfation Is a Trans-Golgi-Specific Protein Modification. J. Cell Biol. 105 (1987) 2655-2664
22. Bundgaard J.R., Vuust J., and Rehfeld J.F. New Consensus Features for Tyrosine O-Sulfation Determined by Mutational Analysis. J. Biol. Chem. 272 (1997) 21700-21705
23. Ouyang Y., Lane W.S., and Moore K.L. Tyrosylprotein Sulfotransferase: Purification and Molecular Cloning of an Enzyme That Catalyzes Tyrosine O-Sulfation, a Common Post-Translational Modification of Eukaryotic Proteins. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 2896-2901
24. Ouyang Y.B., and Moore K.L. Molecular Cloning and Expression of Human and Mouse Tyrosylprotein Sulfotransferase-2 and a Tyrosylprotein Sulfotransferase Homologue in Caenorhabditis elegans. J. Biol. Chem. 273 (1998) 24770-24774
25. Beisswanger R., Corbeil D., Vannier C., Thiele C., Dohrmann U., Kellner R., Ashman K., Niehrs C., and Huttner W.B. Existence of Distinct Tyrosylprotein Sulfotransferase Genes: Molecular Characterization of Tyrosylprotein Sulfotransferase-2. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 11134-11139
26. Ouyang Y.B., Crawley J.T., Aston C.E., and Moore K.L. Reduced Body Weight and Increased Postimplantation Fetal Death in Tyrosylprotein Sulfotransferase-1-Deficient Mice. J. Biol. Chem. 277 (2002) 23781-23787
27. Borghei A., Ouyang Y.B., Westmuckett A.D., Marcello M.R., Landel C.P., Evans J.P., and Moore K.L. Targeted Disruption of Tyrosylprotein Sulfotransferase-2, an Enzyme That Catalyzes Post-Translational Protein Tyrosine O-Sulfation, Causes Male Infertility. J. Biol. Chem. 281 (2006) 9423-9431
28. Westmuckett A.D., Hoffhines A.J., Borghei A., and Moore K.L. Early Postnatal Pulmonary Failure and Primary Hypothyroidism in Mice with Combined Tpst-1 and Tpst-2 Deficiency. Gen. Comp. Endocrinol. 156 (2008) 145-153
29. Seibert C., Cadene M., Sanfiz A., Chait B.T., and Sakmar T.P. Tyrosine Sulfation of Ccr5 N-Terminal Peptide by Tyrosylprotein Sulfotransferases 1 and 2 Follows a Discrete Pattern and Temporal Sequence. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 11031-11036
30. Yu Y., Hoffhines A.J., Moore K.L., and Leary J.A. Determination of the Sites of Tyrosine O-Sulfation in Peptides and Proteins. Nat. Methods 4 (2007) 583-588
31. Mishiro E., Sakakibara Y., Liu M.C., and Suiko M. Differential Enzymatic Characteristics and Tissue-Specific Expression of Human Tpst-1 and Tpst-2. J. Biochem. (Tokyo) 140 (2006) 731-737
32. Lee R.W., and Huttner W.B. (Glu62, Ala30, Tyr8)N Serves as High-Affinity Substrate for Tyrosylprotein Sulfotransferase: A Golgi Enzyme. Proc. Natl. Acad. Sci. U.S.A. 82 (1985) 6143-6147
33. Niehrs C., Kraft M., Lee R.W., and Huttner W.B. Analysis of the Substrate Specificity of Tyrosylprotein Sulfotransferase Using Synthetic Peptides. J. Biol. Chem. 265 (1990) 8525-8532
34. Niehrs C., and Huttner W.B. Purification and Characterization of Tyrosylprotein Sulfotransferase. EMBO J. 9 (1990) 35-42
35. Ge X., Sirich T.L., Beyer M.K., Desaire H., and Leary J.A. A Strategy for the Determination of Enzyme Kinetics Using Electrospray Ionization with an Ion Trap Mass Spectrometer. Anal. Chem. 73 (2001) 5078-5082
36. Pi N., Armstrong J.I., Bertozzi C.R., and Leary J.A. Kinetic Analysis of NodST Sulfotransferase Using an Electrospray Ionization Mass Spectrometry Assay. Biochemistry 41 (2002) 13283-13288
37. Gao H., and Leary J.A. Multiplex Inhibitor Screening and Kinetic Constant Determinations for Yeast Hexokinase Using Mass Spectrometry Based Assays. J. Am. Soc. Mass Spectrom. 14 (2003) 173-181
38. Pi N., Hoang M.B., Gao H., Mougous J.D., Bertozzi C.R., and Leary J.A. Kinetic Measurements and Mechanism Determination of Stf0 Sulfotransferase Using Mass Spectrometry. Anal. Biochem. 341 (2005) 94-104
39. Gao H., and Leary J.A. Kinetic Measurements of Phosphoglucomutase by Direct Analysis of Glucose-1-Phosphate and Glucose-6-Phosphate Using Ion/Molecule Reactions and Fourier Transform Ion Cyclotron Resonance Mass Spectrometry. Anal. Biochem. 329 (2004) 269-275
40. Singer S.S. Enzymatic Sulfation of Steroids. VI. A Simple, Rapid Method for Routine Enzymatic Preparation of 3′-Phosphoadenosine-5′-Phosphosulfate. Anal. Biochem. 96 (1979) 34-38
41. Fenn J.B., Mann M., Meng C.K., Wong S.F., and Whitehouse C.M. Electrospray Ionization for Mass Spectrometry of Large Biomolecules. Science 246 (1989) 64-71
42. Gibson B.W., and Cohen P. Liquid Secondary Ion Mass Spectrometry of Phosphorylated and Sulfated Peptides and Proteins. Methods. Enzymol. 193 (1990) 480-501
43. Rappsilber J., Steen H., and Mann M. Labile Sulfogroup Allows Differentiation of Sulfotyrosine and Phosphotyrosine in Peptides. J. Mass Spectrom. 36 (2001) 832-833
44. Vargas F., Frerot O., Tuong M.D., and Schwartz J.C. Characterization of a Tyrosine Sulfotransferase in Rat Brain Using Cholecystokinin Derivatives as Acceptors. Biochemistry 24 (1985) 5938-5943
45. Rens-Domiano S., and Roth J.A. Characterization of Tyrosylprotein Sulfotransferase from Rat Liver and Other Tissues. J. Biol. Chem. 264 (1989) 899-905
46. Lin W.H., and Roth J.A. Characterization of a Tyrosylprotein Sulfotransferase in Human Liver. Biochem. Pharmacol. 40 (1990) 629-635
47. Kasinathan C., Sundaram P., Slomiany B.L., and Slomiany A. Identification of Tyrosylprotein Sulfotransferase in Rat Gastric Mucosa. Enzyme 46 (1992) 179-187
48. Sundaram P., Slomiany A., Slomiany B.L., and Kasinathan C. Tyrosylprotein Sulfotransferase in Rat Submandibular Salivary Glands. Int. J. Biochem. 24 (1992) 663-667
49. Sane D.C., and Baker M.S. Human Platelets Possess Tyrosylprotein Sulfotransferase (TPST) Activity. Thromb. Haemost. 69 (1993) 272-275
50. Suiko M., Fernando P.H., Sakakibara Y., Kudo H., Nakamura T., and Liu M.C. Characterization of Bovine Heart Sulfotransferase Catalyzing the Sulfation of Tyrosine-Containing Peptides. J. Nutr. Sci. Vitaminol. (Tokyo). 43 (1997) 485-490