The Biology and Enzymology of Protein Tyrosine O-Sulfation (2003)

Post-translational tyrosine O-sulfation of proteins was first observed by Bettelheim in bovine fibrinopeptide B in 1954 (1Bettelheim F.R. J. Am. Chem. Soc. 1954; 76: 2838-2839Google Scholar). In the 1960s several small peptides including gastrin, phyllokinin, cholecystokinin, and caerulein were shown to be tyrosine-sulfated as well (2Gregory H. Hardy P.M. Jones D.S. Kenner G.W. Sheppard R.C. Nature. 1964; 204: 931-933Google Scholar, 3Anastasi A. Bertaccini G. Erspamer V. Br. J. Pharmocol. 1966; 27: 479-485Google Scholar, 4Mutt V. Jorpes J.E. Eur. J. Biochem. 1968; 6: 156-162Google Scholar, 5Anastasi A. Erspamer V. Endean R. Arch. Biochem. Biophys. 1968; 125: 57-68Google Scholar). However, the widespread occurrence of tyrosine O-sulfation was not fully appreciated until 1982, when Huttner (6Huttner W.B. Nature (Lond.). 1982; 299: 273-276Google Scholar) demonstrated that many proteins expressed in various mammalian cells and tissues undergo this modification. Later, Lee and Huttner (7Lee R.W.H. Huttner W.B. J. Biol. Chem. 1983; 258: 11326-11334Google Scholar) directly demonstrated that tyrosine O-sulfation was mediated by an enzyme, designated tyrosylprotein sulfotransferase (TPST, 1The abbreviations used are: TPST, tyrosylprotein sulfotransferase; PAPS, adenosine 3′-phosphate 5′-phosphosulfate; EST, expressed sequence tag data base; PSGL-1, P-selectin glycoprotein ligand-1; GPCR, G-proteincoupled receptor; HIV, human immunodeficiency virus; RANTES, regulated on activation normal T cell expressed and secreted; APS, adenosine phosphosulfate. 1The abbreviations used are: TPST, tyrosylprotein sulfotransferase; PAPS, adenosine 3′-phosphate 5′-phosphosulfate; EST, expressed sequence tag data base; PSGL-1, P-selectin glycoprotein ligand-1; GPCR, G-proteincoupled receptor; HIV, human immunodeficiency virus; RANTES, regulated on activation normal T cell expressed and secreted; APS, adenosine phosphosulfate. EC 2.8.2.20). The enzyme was shown to catalyze the transfer of sulfate from the universal sulfate donor adenosine 3′-phosphate 5′-phosphosulfate (PAPS) to the hydroxyl group of a peptidyltyrosine residue to form a tyrosine O4-sulfate ester and 3′,5′-ADP (Fig. 1) (7Lee R.W.H. Huttner W.B. J. Biol. Chem. 1983; 258: 11326-11334Google Scholar). Huttner and colleagues (8Baeuerle P.A. Huttner W.B. J. Cell Biol. 1987; 105: 2655-2664Google Scholar, 9Lee R.W.H. Huttner W.B. Proc. Natl. Acad. Sci. U. S. A. 1985; 82: 6143-6147Google Scholar) further showed that tyrosine O-sulfation occurred in the trans-Golgi network, and biochemical studies indicated that the enzyme was membrane-bound and that its active site was luminally oriented in highly enriched Golgi membranes.Niehrs and Huttner (10Niehrs C. Huttner W.B. EMBO J. 1990; 9: 35-42Google Scholar) reported the purification of TPST from bovine adrenal medulla in 1990 and William et al. (11William S. Ramaprasad P. Kasinathan C. Arch. Biochem. Biophys. 1997; 338: 90-96Google Scholar) reported the purification of TPST from rat submandibular glands in 1997. Mouse and human cDNAs encoding TPST-1 were first isolated in our laboratory using amino acid sequences obtained from a purified rat liver TPST (12Ouyang Y.B. Lane W.S. Moore K.L. Proc. Natl. Acad. Sci. U. S. A. 1998; 95: 2896-2901Google Scholar). Subsequently, and a of the on its of to TPST-1 Y.B. Moore K.L. J. Biol. Chem. 1998; Scholar, R. C. C. U. R. C. Huttner W.B. Proc. Natl. Acad. Sci. U. S. A. 1998; 95: Scholar). TPST a a a and a (Fig. TPST-1 and of and and in and membrane-bound in TPST-1 and In the sulfotransferase in of the 3′-phosphate of the 3′,5′-ADP and designated the and Biochem. Sci. 1998; Scholar). The amino acid sequences of human and TPST-1 and a of and TPST-1 to human and sequence of from various that the of the acid a that be to that in many The human and on and the and on the of human TPST in expressed sequence tag data of tyrosylprotein TPST-1 and proteins of a a a a and that in from as the and that in of the and 3′-phosphate of the and of proteins TPST in many the and including the of the W.B. P.A. Cell Biol. 6: Scholar, Chem. Biol. Scholar). In studies in the rat shown that as tyrosine many and proteins in tissues A. Huttner W.B. Eur. J. Biochem. 1990; Scholar, A. Huttner W.B. Eur. J. Biochem. 1990; Scholar). demonstrated the of TPST-1 and in tissues (12Ouyang Y.B. Lane W.S. Moore K.L. Proc. Natl. Acad. Sci. U. S. A. 1998; 95: 2896-2901Google Scholar, Y.B. Moore K.L. J. Biol. Chem. 1998; Scholar, R. C. C. U. R. C. Huttner W.B. Proc. Natl. Acad. Sci. U. S. A. 1998; 95: Scholar). In expressed in cell and in human and The many of the several human and TPST-1 and in the data a widespread and of TPST-1 and mammalian cell cell that not to that the and of the TPST the in tissues cells not to the of and data that TPST-1 and in mammalian of the data cDNAs encoding TPST-1 in many and and and several TPST cDNAs and the sequences in including TPST H. TPST-1 and to that a TPST including C. TPST proteins Proc. Natl. Acad. Sci. U. S. A. Scholar) and TPST H. Scholar) in several TPST and in the tyrosine-sulfated TPST TPST in in of biochemical data and TPST-1 and expressed in cells as proteins in the Golgi as by and W.B. The Golgi and the active site of TPST-1 and that tyrosine O-sulfation on proteins that the trans-Golgi (Fig. In this that this tyrosine-sulfated proteins to and proteins of many and proteins the and studies of various cell that that tyrosine sulfate in proteins A. Huttner W.B. Eur. J. Biochem. 1990; Scholar). on was on in of the proteins by cells and in of by tyrosine sulfate residue A. Huttner W.B. Eur. J. Biochem. 1990; Scholar). studies that membrane-bound proteins as to be as The of tyrosine sulfate in proteins to activation and tyrosine sulfate the cell by the of of several sulfate in Scholar). in the sulfate by the of of in Scholar). a and an adenosine In the first of sulfate and sulfate to and by directly the and active In the by the a to the of the of to and the Golgi by a that purified not Proc. Natl. Acad. Sci. U. S. A. Scholar, J. Scholar). an as the J. Scholar). the Golgi as the sulfate donor and and the in the of the trans-Golgi of in several on the amino acid sequences tyrosine O-sulfation in studies on the of various that tyrosine O-sulfation tyrosine O-sulfation proteins to be tyrosine-sulfated not W.B. P.A. Cell Biol. 6: Scholar). that the of that and amino of the the of a that tyrosine O-sulfation in proteins A. Scholar). the of this be used to the of tyrosine-sulfated proteins in a of the proteins in the data were to tyrosine O-sulfation by the were and proteins that a were as were proteins in the in of the that as many as proteins be that the that to the of the of of in the on the of tyrosine O-sulfation in a was shown to be tyrosine-sulfated P. R. C. J. H. Scholar). and studies showed that of tyrosine in the of of and and in tyrosine in the were to and studies shown that peptides on the of not to the and cells Proc. Natl. Acad. Sci. U. S. A. Scholar). studies that of tyrosine in the of and the an of and H. J. Biol. Chem. Scholar, S. J. Scholar, J. Biol. Chem. Scholar, J. C. H. J. Scholar, S. V. J. G. G. EMBO J. Scholar). In studies shown that to and to the of the sequences of the that highly and tyrosine The that this the of tyrosine that and of the be and in and and A. Scholar). the that as a tyrosine not TPST-1 and of However, in studies using in reported that peptides on the of human and by TPST-1 by Y.B. Moore K.L. J. Biol. Chem. 1998; Scholar). In et al. of a on the of human that tyrosine O-sulfation C. A. Proc. Natl. Acad. Sci. U. S. A. Scholar). the of of various showed that enzyme the in a and were by and However, TPST-1 as the studies that TPST-1 and not of that the TPST-1 to of to cells reported to TPST-1 and the and of S. H. P. Biochem. Biophys. Scholar). TPST-1 and in the liver and of in to of and in and cells in to a were J. and that tyrosine O-sulfation be by the of However, several of that to tyrosine sulfate in proteins tyrosine sulfate not the cell in the et al. Biochem. J. Scholar) reported that in tyrosine was by the were of the sulfate Jones et al. Biochem. J. Scholar) reported that of fibrinopeptide B in the the was in the as tyrosine its sulfate a normal of human S. Moore S. J. Biol. Chem. Scholar). in the the sulfate ester of tyrosine that tyrosine a mammalian Biochem. J. tyrosine-sulfated peptides and proteins purified from and the and of However, in were isolated using to purification that on the of the sulfate an of in were purified from an of the were purified from and were isolated using that were of the of the The activation of human H. S. J. S. J. J. G. H. Scholar). glycoprotein purified from human tyrosine O-sulfation and A. Scholar). in in human a sequence G. J. Scholar). In et al. H. A. Scholar) showed that the of fibrinopeptide B and in the data the of an in the that tyrosine O-sulfation in of in tyrosine-sulfated proteins the of a in the of the proteins not et al. Huttner W.B. J. Cell Biol. Scholar) reported that of the from was when was using when the tyrosine O-sulfation site in was to However, of tyrosine O-sulfation not of tyrosine-sulfated including P-selectin glycoprotein glycoprotein and and In in by in tyrosine-sulfated proteins and a J. Scholar). In of and of in an the of A. J. Biol. Scholar). tyrosine O-sulfation of to P-selectin Moore K.L. J. Biol. Chem. Scholar). In the of the of P-selectin and a of the of PSGL-1, the sulfate and in W.S. J. Scholar). In in and activation of proteins and of the data on the of tyrosine O-sulfation in from in In in a in the of a that in the of tyrosine O-sulfation not The that tyrosine O-sulfation in from of to that to in the that in a in the site the of the B and C. S. 1990; 6: Scholar). of in to as a in the of in A. C. Huttner W.B. J. Biol. Chem. Scholar). this directly the to in from and to the of tyrosine O-sulfation in using in the Y.B. Moore K.L. J. Biol. Chem. Scholar) and to in showed that of not of the and normal and when of normal a of the of not of the and of of the including on and Y.B. Moore K.L. J. Biol. Chem. Scholar). showed that of and However, to and to the of and was The in occurred of the of and was on that of However, normal of and to of of the of a in not In and a was by a a the of in of the that normal as by normal and and and In observed in the data that of in tyrosine O-sulfation and the that catalyze its TPST regulated and the TPST to not the of TPST-1 and in of the and in in directly the of TPST-1 to of TPST data that the of this enzyme the observed in of the not and further data that the TPST and the of tyrosine O-sulfation in several that not including of and Post-translational tyrosine O-sulfation of proteins was first observed by Bettelheim in bovine fibrinopeptide B in 1954 (1Bettelheim F.R. J. Am. Chem. Soc. 1954; 76: 2838-2839Google Scholar). In the 1960s several small peptides including gastrin, phyllokinin, cholecystokinin, and caerulein were shown to be tyrosine-sulfated as well (2Gregory H. Hardy P.M. Jones D.S. Kenner G.W. Sheppard R.C. Nature. 1964; 204: 931-933Google Scholar, 3Anastasi A. Bertaccini G. Erspamer V. Br. J. Pharmocol. 1966; 27: 479-485Google Scholar, 4Mutt V. Jorpes J.E. Eur. J. Biochem. 1968; 6: 156-162Google Scholar, 5Anastasi A. Erspamer V. Endean R. Arch. Biochem. Biophys. 1968; 125: 57-68Google Scholar). However, the widespread occurrence of tyrosine O-sulfation was not fully appreciated until 1982, when Huttner (6Huttner W.B. Nature (Lond.). 1982; 299: 273-276Google Scholar) demonstrated that many proteins expressed in various mammalian cells and tissues undergo this modification. Later, Lee and Huttner (7Lee R.W.H. Huttner W.B. J. Biol. Chem. 1983; 258: 11326-11334Google Scholar) directly demonstrated that tyrosine O-sulfation was mediated by an enzyme, designated tyrosylprotein sulfotransferase (TPST, 1The abbreviations used are: TPST, tyrosylprotein sulfotransferase; PAPS, adenosine 3′-phosphate 5′-phosphosulfate; EST, expressed sequence tag data base; PSGL-1, P-selectin glycoprotein ligand-1; GPCR, G-proteincoupled receptor; HIV, human immunodeficiency virus; RANTES, regulated on activation normal T cell expressed and secreted; APS, adenosine phosphosulfate. 1The abbreviations used are: TPST, tyrosylprotein sulfotransferase; PAPS, adenosine 3′-phosphate 5′-phosphosulfate; EST, expressed sequence tag data base; PSGL-1, P-selectin glycoprotein ligand-1; GPCR, G-proteincoupled receptor; HIV, human immunodeficiency virus; RANTES, regulated on activation normal T cell expressed and secreted; APS, adenosine phosphosulfate. EC 2.8.2.20). The enzyme was shown to catalyze the transfer of sulfate from the universal sulfate donor adenosine 3′-phosphate 5′-phosphosulfate (PAPS) to the hydroxyl group of a peptidyltyrosine residue to form a tyrosine O4-sulfate ester and 3′,5′-ADP (Fig. 1) (7Lee R.W.H. Huttner W.B. J. Biol. Chem. 1983; 258: 11326-11334Google Scholar). Huttner and colleagues (8Baeuerle P.A. Huttner W.B. J. Cell Biol. 1987; 105: 2655-2664Google Scholar, 9Lee R.W.H. Huttner W.B. Proc. Natl. Acad. Sci. U. S. A. 1985; 82: 6143-6147Google Scholar) further showed that tyrosine O-sulfation occurred in the trans-Golgi network, and biochemical studies indicated that the enzyme was membrane-bound and that its active site was luminally oriented in highly enriched Golgi and Huttner (10Niehrs C. Huttner W.B. EMBO J. 1990; 9: 35-42Google Scholar) reported the purification of TPST from bovine adrenal medulla in 1990 and William et al. (11William S. Ramaprasad P. Kasinathan C. Arch. Biochem. Biophys. 1997; 338: 90-96Google Scholar) reported the purification of TPST from rat submandibular glands in 1997. Mouse and human cDNAs encoding TPST-1 were first isolated in our laboratory using amino acid sequences obtained from a purified rat liver TPST (12Ouyang Y.B. Lane W.S. Moore K.L. Proc. Natl. Acad. Sci. U. S. A. 1998; 95: 2896-2901Google Scholar). Subsequently, and a of the on its of to TPST-1 Y.B. Moore K.L. J. Biol. Chem. 1998; Scholar, R. C. C. U. R. C. Huttner W.B. Proc. Natl. Acad. Sci. U. S. A. 1998; 95: Scholar). TPST a a a and a (Fig. TPST-1 and of and and in and membrane-bound in TPST-1 and In the sulfotransferase in of the 3′-phosphate of the 3′,5′-ADP and designated the and Biochem. Sci. 1998; Scholar). The amino acid sequences of human and TPST-1 and a of and TPST-1 to human and sequence of from various that the of the acid a that be to that in many The human and on and the and on the of human TPST in expressed sequence tag data and of proteins TPST in many the and including the of the W.B. P.A. Cell Biol. 6: Scholar, Chem. Biol. Scholar). In studies in the rat shown that as tyrosine many and proteins in tissues A. Huttner W.B. Eur. J. Biochem. 1990; Scholar, A. Huttner W.B. Eur. J. Biochem. 1990; Scholar). demonstrated the of TPST-1 and in tissues (12Ouyang Y.B. Lane W.S. Moore K.L. Proc. Natl. Acad. Sci. U. S. A. 1998; 95: 2896-2901Google Scholar, Y.B. Moore K.L. J. Biol. Chem. 1998; Scholar, R. C. C. U. R. C. Huttner W.B. Proc. Natl. Acad. Sci. U. S. A. 1998; 95: Scholar). In expressed in cell and in human and The many of the several human and TPST-1 and in the data a widespread and of TPST-1 and mammalian cell cell that not to that the and of the TPST the in tissues cells not to the of and data that TPST-1 and in mammalian of the data cDNAs encoding TPST-1 in many and and and several TPST cDNAs and the sequences in including TPST H. TPST-1 and to that a TPST including C. TPST proteins Proc. Natl. Acad. Sci. U. S. A. Scholar) and TPST H. Scholar) in several TPST and in the tyrosine-sulfated TPST TPST in in proteins TPST in many the and including the of the W.B. P.A. Cell Biol. 6: Scholar, Chem. Biol. Scholar). In studies in the rat shown that as tyrosine many and proteins in tissues A. Huttner W.B. Eur. J. Biochem. 1990; Scholar, A. Huttner W.B. Eur. J. Biochem. 1990; Scholar). demonstrated the of TPST-1 and in tissues (12Ouyang Y.B. Lane W.S. Moore K.L. Proc. Natl. Acad. Sci. U. S. A. 1998; 95: 2896-2901Google Scholar, Y.B. Moore K.L. J. Biol. Chem. 1998; Scholar, R. C. C. U. R. C. Huttner W.B. Proc. Natl. Acad. Sci. U. S. A. 1998; 95: Scholar). In expressed in cell and in human and The many of the several human and TPST-1 and in the data a widespread and of TPST-1 and mammalian cell cell that not to that the and of the TPST the in tissues cells not to the of and data that TPST-1 and in mammalian of the data cDNAs encoding TPST-1 in many and and and several TPST cDNAs and the sequences in including TPST H. TPST-1 and to that a TPST including C. TPST proteins Proc. Natl. Acad. Sci. U. S. A. Scholar) and TPST H. Scholar) in several TPST and in the tyrosine-sulfated TPST TPST in in of biochemical data and TPST-1 and expressed in cells as proteins in the Golgi as by and W.B. The Golgi and the active site of TPST-1 and that tyrosine O-sulfation on proteins that the trans-Golgi (Fig. In this that this tyrosine-sulfated proteins to and proteins of many and proteins the and studies of various cell that that tyrosine sulfate in proteins A. Huttner W.B. Eur. J. Biochem. 1990; Scholar). on was on in of the proteins by cells and in of by tyrosine sulfate residue A. Huttner W.B. Eur. J. Biochem. 1990; Scholar). studies that membrane-bound proteins as to be as The of tyrosine sulfate in proteins to of in several on the amino acid sequences tyrosine O-sulfation in studies on the of various that tyrosine O-sulfation tyrosine O-sulfation proteins to be tyrosine-sulfated not W.B. P.A. Cell Biol. 6: Scholar). that the of that and amino of the the of a that tyrosine O-sulfation in proteins A. Scholar). the of this be used to the of tyrosine-sulfated proteins in a of the proteins in the data were to tyrosine O-sulfation by the were and proteins that a were as were proteins in the in of the that as many as proteins be that the that to the of the of of in the on the of tyrosine O-sulfation in a was shown to be tyrosine-sulfated P. R. C. J. H. Scholar). and studies showed that of tyrosine in the of of and and in tyrosine in the were to and studies shown that peptides on the of not to the and cells Proc. Natl. Acad. Sci. U. S. A. Scholar). studies that of tyrosine in the of and the an of and H. J. Biol. Chem. Scholar, S. J. Scholar, J. Biol. Chem. Scholar, J. C. H. J. Scholar, S. V. J. G. G. EMBO J. Scholar). In studies shown that to and to the of the sequences of the that highly and tyrosine The that this the of tyrosine that and of the be and in and and A. Scholar). the that as a tyrosine not TPST-1 and of However, in studies using in reported that peptides on the of human and by TPST-1 by Y.B. Moore K.L. J. Biol. Chem. 1998; Scholar). In et al. of a on the of human that tyrosine O-sulfation C. A. Proc. Natl. Acad. Sci. U. S. A. Scholar). the of of various showed that enzyme the in a and were by and However, TPST-1 as the studies that TPST-1 and not biochemical data and TPST-1 and expressed in cells as proteins in the Golgi as by and W.B. The Golgi and the active site of TPST-1 and that tyrosine O-sulfation on proteins that the trans-Golgi (Fig. In this that this tyrosine-sulfated proteins to and proteins of many and proteins the and studies of various cell that that tyrosine sulfate in proteins A. Huttner W.B. Eur. J. Biochem. 1990; Scholar). on was on in of the proteins by cells and in of by tyrosine sulfate residue A. Huttner W.B. Eur. J. Biochem. 1990; Scholar). studies that membrane-bound proteins as to be as The of tyrosine sulfate in proteins to The of in several on the amino acid sequences tyrosine O-sulfation in studies on the of various that tyrosine O-sulfation tyrosine O-sulfation proteins to be tyrosine-sulfated not W.B. P.A. Cell Biol. 6: Scholar). that the of that and amino of the The the of a that tyrosine O-sulfation in proteins A. Scholar). the of this be used to the of tyrosine-sulfated proteins in a of the proteins in the data were to tyrosine O-sulfation by the were and proteins that a were as were proteins in the in of the that as many as proteins be that the that to the of the of of in the on the of tyrosine O-sulfation in a was shown to be tyrosine-sulfated P. R. C. J. H. Scholar). and studies showed that of tyrosine in the of of and and in tyrosine in the were to and studies shown that peptides on the of not to the and cells Proc. Natl. Acad. Sci. U. S. A. Scholar). studies that of tyrosine in the of and the an of and H. J. Biol. Chem. Scholar, S. J. Scholar, J. Biol. Chem. Scholar, J. C. H. J. Scholar, S. V. J. G. G. EMBO J. Scholar). In studies shown that to and to the of the sequences of the that highly and tyrosine The that this the of tyrosine that and of the be and in and and A. Scholar). the that as a tyrosine not TPST-1 and of However, in studies using in reported that peptides on the of human and by TPST-1 by Y.B. Moore K.L. J. Biol. Chem. 1998; Scholar). In et al. of a on the of human that tyrosine O-sulfation C. A. Proc. Natl. Acad. Sci. U. S. A. Scholar). the of of various showed that enzyme the in a and were by and However, TPST-1 as the studies that TPST-1 and not of that the TPST-1 to of to cells reported to TPST-1 and the and of S. H. P. Biochem. Biophys. Scholar). TPST-1 and in the liver and of in to of and in and cells in to a were J. and that tyrosine O-sulfation be by the of However, several of that to tyrosine sulfate in proteins tyrosine sulfate not the cell in the et al. Biochem. J. Scholar) reported that in tyrosine was by the were of the sulfate Jones et al. Biochem. J. Scholar) reported that of fibrinopeptide B in the the was in the as tyrosine its sulfate a normal of human S. Moore S. J. Biol. Chem. Scholar). in the the sulfate ester of tyrosine that tyrosine a mammalian Biochem. J. tyrosine-sulfated peptides and proteins purified from and the and of However, in were isolated using to purification that on the of the sulfate an of in were purified from an of the were purified from and were isolated using that were of the of the The activation of human H. S. J. S. J. J. G. H. Scholar). glycoprotein purified from human tyrosine O-sulfation and A. Scholar). in in human a sequence G. J. Scholar). In et al. H. A. Scholar) showed that the of fibrinopeptide B and in the data the of an in the that tyrosine O-sulfation in that the TPST-1 to of to cells reported to TPST-1 and the and of S. H. P. Biochem. Biophys. Scholar). TPST-1 and in the liver and of in to of and in and cells in to a were J. and that tyrosine O-sulfation be by the of However, several of that to tyrosine sulfate in proteins tyrosine sulfate not the cell in the et al. Biochem. J. Scholar) reported that in tyrosine was by the were of the sulfate Jones et al. Biochem. J. Scholar) reported that of fibrinopeptide B in the the was in the as tyrosine its sulfate a normal of human S. Moore S. J. Biol. Chem. Scholar). in the the sulfate ester of tyrosine that tyrosine a mammalian Biochem. J. Scholar). tyrosine-sulfated peptides and proteins purified from and the and of However, in were isolated using to purification that on the of the sulfate an of in were purified from an of the were purified from and were isolated using that were of the of the The activation of human H. S. J. S. J. J. G. H. Scholar). glycoprotein purified from human tyrosine O-sulfation and A. Scholar). in in human a sequence G. J. Scholar). In et al. H. A. Scholar) showed that the of fibrinopeptide B and in the data the of an in the that tyrosine O-sulfation in of in tyrosine-sulfated proteins the of a in the of the proteins not et al. Huttner W.B. J. Cell Biol. Scholar) reported that of the from was when was using when the tyrosine O-sulfation site in was to However, of tyrosine O-sulfation not of tyrosine-sulfated including P-selectin glycoprotein glycoprotein and and In in by in tyrosine-sulfated proteins and a J. Scholar). In of and of in an the of A. J. Biol. Scholar). tyrosine O-sulfation of to P-selectin Moore K.L. J. Biol. Chem. Scholar). In the of the of P-selectin and a of the of PSGL-1, the sulfate and in W.S. J. Scholar). In in and activation of proteins and of the data on the of tyrosine O-sulfation in from in In in a in the of a that in the of tyrosine O-sulfation not The that tyrosine O-sulfation in from of to that to in the that in a in the site the of the B and C. S. 1990; 6: Scholar). of in to as a in the of in A. C. Huttner W.B. J. Biol. Chem. Scholar). this directly the to in tyrosine-sulfated proteins the of a in the of the proteins not et al. Huttner W.B. J. Cell Biol. Scholar) reported that of the from was when was using when the tyrosine O-sulfation site in was to However, of tyrosine O-sulfation not of tyrosine-sulfated including P-selectin glycoprotein glycoprotein and and In in by in tyrosine-sulfated proteins and a J. Scholar). In of and of in an the of A. J. Biol. Scholar). tyrosine O-sulfation of to P-selectin Moore K.L. J. Biol. Chem. Scholar). In the of the of P-selectin and a of the of PSGL-1, the sulfate and in W.S. J. Scholar). In in and activation of proteins and of the data on the of tyrosine O-sulfation in from in In in a in the of a that in the of tyrosine O-sulfation not The that tyrosine O-sulfation in from of to that to in the that in a in the site the of the B and C. S. 1990; 6: Scholar). of in to as a in the of in A. C. Huttner W.B. J. Biol. Chem. Scholar). this directly the to in from and to the of tyrosine O-sulfation in using in the Y.B. Moore K.L. J. Biol. Chem. Scholar) and to in showed that of not of the and normal and when of normal a of the of not of the and of of the including on and Y.B. Moore K.L. J. Biol. Chem. Scholar). showed that of and However, to and to the of and was The in occurred of the of and was on that of However, normal of and to of of the of a in not In and a was by a a the of in of the that normal as by normal and and and In observed in the data that of in tyrosine O-sulfation and the that catalyze its TPST regulated and the TPST to not the of TPST-1 and in of the and in in directly the of TPST-1 to of TPST data that the of this enzyme the observed in of the not and further data that the TPST and the of tyrosine O-sulfation in several that not including of and to the of tyrosine O-sulfation in using in the Y.B. Moore K.L. J. Biol. Chem. Scholar) and to in showed that of not of the and normal and when of normal a of the of not of the and of of the including on and Y.B. Moore K.L. J. Biol. Chem. Scholar). showed that of and However, to and In to the of and was The in occurred of the of and was on that of However, normal of and to of of the of a in not In and a was by a a the of in of the that normal as by normal and and and In observed in the data that of in tyrosine O-sulfation and the that catalyze its TPST regulated and the TPST to not the of TPST-1 and in of the and in in directly the of TPST-1 to of TPST data that the of this enzyme the observed in of the not and further data that the TPST and the of tyrosine O-sulfation in several that not including of and