Nuclear localization of PAPS synthetase 1: A sulfate activation pathway in the nucleus of eukaryotic cells

FASEB Journal

Volumn 14, Issue 2, 2000, Pages 345-354

  Besset, Steve ^a   Vincourt, Jean Baptiste ^a   Amalric, François ^a   Girard, Jean Philippe ^a  

^a INSTITUT DE PHARMACOLOGIE ET DE BIOLOGIE STRUCTURALE   (France)

Author keywords

PAPS synthesis; Subcellular localization; Sulfate activation; Sulfation

Indexed keywords

ADENOSINE 3' PHOSPHATE 5' PHOSPHOSULFATE; PROTEOGLYCAN; SULFATE; SULFATE ADENYLYLTRANSFERASE; SULFOTRANSFERASE; SYNTHETASE;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; BONE DEVELOPMENT; CATALYSIS; CELLULAR DISTRIBUTION; DROSOPHILA MELANOGASTER; ENZYME ACTIVATION; ENZYME ACTIVITY; EUKARYOTE; GENE EXPRESSION; GENE MUTATION; MAMMAL; NEUROTRANSMITTER RELEASE; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; YEAST;

ANIMALIA; DROSOPHILA MELANOGASTER; EUKARYOTA; MAMMALIA; MELANOGASTER; MURINAE;

EID: 0033960622     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fasebj.14.2.345     Document Type: Article

References (51)

1. Falany, C. N. (1997) Sulfation and sulfotransferases. Introduction: changing view of sulfation and the cytosolic sulfotransferases. FASEB J. 11, 1-2
2. Roche, P., Debelle, F., Maillet, F., Lerouge, P., Faucher, C., Truchet, G., Denairie, J., and Prome, J. C. (1991) Molecular basis of symbiotic host specificity in Rhizobium meliloti: nodH and nodPQ genes encode the sulfation of lipo-oligosaccharide signals. Cell 67, 1131-1143
3. Farzan, M., Mirzabekov, T., Kolchinksy, P., Wyatt, R., Cayabyab, M., Gerard, N. P., Gerard, C., Sodroski, J., and Choe, H. (1999) Tyrosine sulfation of the amino terminus of CCR5 facilitates HIV-1 entry. Cell 96, 667-676
4. Imai, Y., Lasky, L. A., and Rosen, S. D. (1993) Sulphation requirement for GlyCAM-1, an endothelial ligand for L-selectin. Nature (London) 361, 555-557
5. Hemmerich, S., Butcher, E. C., and Rosen, S. D. (1994) Sulfation-dependent recognition of high endothelial venules (HEV) ligands by L-selectin and MECA 79, and adhesion-blocking monoclonal antibody. J. Exp. Med. 180, 2219-2226
6. Pouyani, T., and Seed, B. (1995) PSGL-1 recognition of P-selectin is controlled by a tyrosine sulfation consensus at the PSGL-1 amino terminus. Cell 83, 333-343
7. Wilkins, P. P., Moore, K. L., McEver, R. P., and Cummings, R. D. (1995) Tyrosine sulfation of P-selectin glycoprotein ligand-1 is required for high affinity binding to P-seleclin. J. Biol. Chem. 270, 22677-22680
8. Sako, D., Comess, K. M., Barone, K. M., Camphausen, R. T., Cumming, D. A., and Shaw, G. D. (1995) A sulfated peptide segment at the amino terminus of PSGL-1 is critical for P-selectin binding. Cell 83, 323-331
9. Pye, D. A., Vives, R. R., Turnbull, J. E., Hyde, P., and Gallagher, J. T. (1998) Heparan sulfate oligosaccharides require 6-O-sulfation for promotion of basic fibroblast growth factor mitogenic activity. J. Biol. Chem. 273, 22936-22942
10. Orkin, R. W., Pratt, R. M., and Martin, G. R. (1976) Undersulfated chondroitin sulfate in the cartilage matrix of brachymorphic mice. Dev. Biol. 50, 82-94
11. Falany, C. N. (1997) Enzymology of human cytosolic sulfotransferases. FASEB J. 11, 206-216
12. Weinshilboum, R. M., Otterness, D. M., Aksoy, I. A., Wood, T. C., Her, C., and Raftogianis, R. B. (1997) Sulfation and sulfotransferases 1: Sulfotransferase molecular biology: cDNAs and genes. FASEB J. 11, 3-14
13. Beisswanger, R., Corbeil, D., Vannier, C., Thiele, C., Dohrmann, U., Kellner, R., Ashman, K., Niehrs, C., and Huttner, W. B. (1998) Existence of distinct tyrosylprotein sulfotransferase genes: molecular characterization of tyrosylprotein sulfotransferase-2. Proc. Natl. Acad. Sci. USA 95, 11134-11139
14. Ouyang, Y., Lane, W. S., and Moore, K. L. (1998) Tyrosylprotein sulfotransferase: purification and molecular cloning of an enzyme that catalyzes tyrosine O-sulfation, a common posttranslational modification of eukaryotic proteins. Proc. Natl. Acad. Sci. USA 95, 2896-2901
15. Hooper, L. V., Manzella, S. M., and Baenziger, J. U. (1996) From legumes to leukocytes: biological roles for sulfated carbohydrates. FASEB J. 10, 1137-1146
16. Bowman, K. G., and Bertozzi, C. R. (1999) Carbohydrate sulfotransferases: mediators of extracellular communication. Chem. Biol. 6, R9-R22
17. Brickman, Y. G., Ford, M. D., Gallagher, J. T., Nurcombe, V., Bartlett, P. F., and Turnbull, J. E. (1998) Structural modification of fibroblast growth factor-binding heparan sulfate at a determinative stage of neural development. J. Biol. Chem. 273, 4350-4359
18. Dong, J. F., Hyun, W., and Lopez, J. A. (1995) Aggregation of mammalian cells expressing the platelet glycoprotein (GP) Ib-IX complex and the requirement for tyrosine sulfation of GP Ib alpha. Blood 86, 4175-4183
19. Leyh, T. S. (1993) The physical biochemistry and molecular genetics of sulfate activation. Crit. Rev. Biochem. Mol. Biol. 28, 515-542
20. Rosen, S. D., and Bertozzi, C. R. (1996) Leukocyte adhesion: two selectins converge on sulphate. Curr. Biol. 6, 261-264
21. Girard, J. P., and Amalric, F. (1998) Biosynthesis of sulfated L-selectin ligands in human high endothelial venules (HEV). Adv. Exp. Med. Biol. 435, 55-62
22. Robbins, P. W., and Lipmann, F. (1958) Separation of the two enzymatic phases in active sulfate synthesis. J. Biol. Chem. 233, 681-686
23. Thomas, D., and Surdin-Kerjan, Y. (1997) Metabolism of sulfur amino acids in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 61, 503-532
24. Girard, J. P., Baekkevold, E. S., and Amalric, F. (1998) Sulfation in high endothelial venules: cloning and expression of the human PAPS synthetase. FASEB J. 12, 603-612
25. Li, H., Deyrup, A., Mensch, J. R., Jr., Domowicz, M., Konstantinidis, A. K., and Schwartz, N. B. (1995) The isolation and characterization of cDNA encoding the mouse bifunctional ATP sulfurylase-adenosine 5′-phosphosulfate kinase. J. Biol. Chem. 270, 29453-29459
26. Rosenthal, E., and Leustek, T. (1995) A multifunctional Urechis caupo protein, PAPS synthetase, has both ATP sulfurylase and APS kinase activities. Gene 165, 243-248
27. Jullien, D., Crozatier, M., and Kas, E. (1997) cDNA sequence and expression pattern of the Drosophila melanogaster PAPS synthetase gene: a new salivary gland marker. Mech. Dev. 68, 179-186
28. Kurima, K., Warman, M. L., Krishnan, S., Domowicz, M., Krueger, R. C., Jr., Deyrup, A., and Schwartz, N. B. (1998) A member of a family of sulfate-activating enzymes causes murine brachymorphism. Proc. Natl, Acad. Sci. USA 95, 8681-8685
29. ul Haque, M. F., King, L. M., Krakow, D., Cantor, R. M., Rusiniak, M. E., Swank, R. T., Superti-Furga, A., Haque, S., Abbas, H., Ahmad, W., Ahmad, M., and Cohn, D. H. (1998) Mutations in orthologous genes in human spondyloepimetaphyseal dysplasia and the brachymorphic mouse. Nat. Genet. 20, 157-162
30. Franzon, V. L., Gibson, M. A., Hatzinikolas, G., Woollatt, E., Sutherland, G. R., and Cleary, E. G. (1999) Molecular cloning of a novel human PAPS synthetase which is differentially expressed in metastatic and non-metastatic colon carcinoma cells. Int. J. Biochem. Cell Biol. 31, 613-626
31. Klaassen, C. D., and Boles, J. W. (1997) Sulfation and sulfotransferases 5: the importance of 3′-phosphoadenosine 5′-phosphosulfate (PAPS) in the regulation of sulfation. FASEB J. 11, 404-418
32. Baeuerle, P. A., and Huttner, W. B. (1986) Chlorate - a potent inhibitor of protein sulfation in intact cells. Biochem. Biophys. Res. Commun. 141, 870-877
33. Mandon, E. C., Milla, M. E., Kempner, E., and Hirschberg, C. B. (1994) Purification of the Golgi adenosine 3′-phosphate 5′-phosphosulfate transporter, a homodimer within the membrane. Proc. Natl. Acad. Sci. USA 91, 10707-10711
34. Ozeran, J. D., Westley, J., and Schwartz, N. B. (1996) Identification and partial purification of PAPS translocase. Biochemistry 35, 3695-3703
35. Tyers, M., Tokiwa, G., Nash, R., and Futcher, B. (1992) The Cln3-Cdc28 kinase complex of S. cerevisiae is regulated by proteolysis and phosphorylation. EMBO J. 11, 1773-1784
36. Deyrup, A. T., Krishnan, S., Coekburn, B. N., and Schwartz, N. B. (1998) Deletion and site-directed mutagenesis of the ATP-binding motif (P-loop) in the bifunctional murine ATP-sulfurylase/adenosine 5′-phosphosulfate kinase enzyme. J. Biol. Chem. 273, 9450-9456
37. Brion, F., Schwartz, J. C., and Vargas, F. (1987) Properties and localization of the sulfate-activating system in rat brain. J. Neurochem. 48, 1171-1177
38. Isaac, R. E., Phua, K. K., and Rees, H. H. (1982) 3′-phosphoadenosine-5′-phosphosulphate synthesis and involvement in sulphotransferase reactions in the insect, Spodoptera littoralis. Biochem. J. 204, 127-133
39. Koizumi, T., Suematsu, T., Kawasaki, A., Hiramatsu, K., and Iwabori, N. (1969) Synthesis and degradation of active sulfate in liver. Biochim. Biophys. Acta 184, 106-113
40. Farooqui, A. A. (1980) 3′-phosphoadenosine 5′-phosphosulphate metabolism in mammalian tissues. Int. J. Biochem. 12, 529-536
41. Coates, S. W., Gurney, T., Jr., Sommers, L. W., Yeh, M., and Hirschberg, C. B. (1980) Subcellular localization of sugar nucleotide synthetases. J. Biol. Chem. 255, 9225-9229
42. Munster, A. K., Eckhardt, M., Potvin, B., Muhlenhoff, M., Stanley, P., and Gerardy-Schahn, R. (1998) Mammalian cytidine 5′-monophosphate N-acetylneuraminic acid synthetase: a nuclear protein with evolutionarily conserved structural motifs. Proc. Natl. Acad. Sci. USA 95, 9140-9145
43. Varki, A. (1997) Sialic acids as ligands in recognition phenomena. FASEB J. 11, 248-255
44. Hemmerich, S., Leffler, H., and Rosen, S. D. (1995) Structure of the O-glycans in GlyCAM-1, an endothelial-derived ligand for L-selectin. J. Biol. Chem. 270, 12035-12047
45. Mitsuoka, C., Sawada-Kasugai, M., Ando-Furui, K., Izawa, M., Nakanishi, H., Nakamura, S., Ishida, H., Kiso, M., and Kannagi, R. (1998) Identification of a major carbohydrate capping group of the L-selectin ligand on high endothelial venules in human lymph nodes as 6-sulfo sialyl Lewis X. J. Biol. Chem. 273, 11225-11233
46. Margolis, R. K., Crockett, C. P., Kiang, W. L., and Margolis, R. U. (1976) Glycosaminoglycans and glycoproteins associated with rat brain nuclei. Biochim. Biophys. Acta 451, 465-469
47. Ferraro, A., Grandi, P., Eufemi, M., Altieri, F., Cervoni, L., and Turano, C. (1991) The presence of N-glycosylated proteins in cell nuclei. Biochem. Biophys. Res. Commun. 178, 1365-1370
48. Bhavanandan, V. P., and Davidson, E. A. (1975) Mucopolysaccharides associated with nuclei of cultured mammalian cells. Proc. Natl. Acad. Sci. USA 72, 2032-2036
49. Liang, Y., Haring, M., Roughley, P. J., Margolis, R. K., and Margolis, R. U. (1997) Glypican and biglycan in the nuclei of neurons and glioma cells: presence of functional nuclear localization signals and dynamic changes in glypican during the cell cycle. J. Cell Biol. 139, 851-864
50. Hart, G. W. (1997) Dynamic O-linked glycosylation of nuclear and cytoskeletal proteins. Annu. Rev. Biochem. 66, 315-335
51. Kreppel, L. K., Blomberg, M. A., and Hart, G. W. (1997) Dynamic glycosylation of nuclear and cytosolic proteins. Cloning and characterization of a unique O-GlcNAc transferase with multiple tetratricopeptide repeats. J. Biol. Chem. 272, 9308-9315