Nucleolin undergoes partial N- and O-glycosylations in the extranuclear cell compartment

Biochemistry

Volumn 44, Issue 15, 2005, Pages 5804-5815

  Carpentier, Mathieu ^b   Morelle, Willy ^b   Coddeville, Bernadette ^b   Pons, Alexandre ^b   Masson, Maryse ^b   Mazurier, Joël ^b   Legrand, Dominique ^a  

^a UNIVERSITÉ DES SCIENCES ET TECHNOLOGIES DE LILLE   (France)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODIES; BIOCHEMISTRY; CELLS; COMPOSITION; GELS; MASS SPECTROMETRY; RNA;

ANTI-NUCLEOLIN ANTIBODIES; CELL PROLIFERATION; NUCLEOLIN; TRANSCRIPTION REGULATION;

PROTEINS;

BUTYRIC ACID DERIVATIVE; GLYCAN; GLYCOSIDASE; ISOPROTEIN; LECTIN; MONOSACCHARIDE; NUCLEOLIN; SINAPIC ACID; TUNICAMYCIN;

ARTICLE; CARBOHYDRATE ANALYSIS; CHEMICAL STRUCTURE; CONTROLLED STUDY; CROSS REACTION; EXTRACELLULAR SPACE; GAS CHROMATOGRAPHY; GLYCOSYLATION; HUMAN; HUMAN CELL; MASS SPECTROMETRY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOLECULAR WEIGHT; PEPTIDE MAPPING; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; RNA BINDING;

AMINO ACID SEQUENCE; BINDING SITES; CARBOHYDRATE SEQUENCE; CELL COMPARTMENTATION; GLYCOSYLATION; HUMANS; JURKAT CELLS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; MONOSACCHARIDES; PEPTIDE MAPPING; PHOSPHOPROTEINS; POLYSACCHARIDES; PROTEIN ISOFORMS; RNA-BINDING PROTEINS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TUNICAMYCIN;

EID: 17144407973     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi047831s     Document Type: Article

References (56)

1. Lapeyre, B., Bourbon, H., and Amalric, F. (1987) Nucleolin, the major nucleolar protein of growing eukaryotic cells: An unusual protein structure revealed by the nucleotide sequence, Proc. Natl. Acad. Sci. U.S.A. 84, 1472-1476.
2. Tuteja, R., and Tuteja, N. (1998) Nucleolin: A multifunctional major nucleolar phosphoprotein, Crit. Rev. Biochem. Mol. Biol. 33, 407-436.
3. Srivastava, M., and Pollard, H. B. (1999) Molecular dissection of nucleolin's role in growth and cell proliferation: New insights, FASEB J. 13, 1911-1922.
4. Srivastava, M., Fleming, P. J., Pollard, H. B., and Burns, A. L. (1989) Cloning and sequencing of the human nucleolin cDNA, FEBS Lett. 250, 99-105.
5. Bouvet, P., Diaz, J. J., Kindbeiter, K., Madjar, J. J., and Amalric, F. (1998) Nucleolin interacts with several ribosomal proteins through its RGG domain, J. Biol. Chem. 273, 19025-19029.
6. Saïd, E. A., Krust, B., Nisole, S., Svab, J., Briand, J. P., and Hovanessian, A. G. (2002) The anti-HIV cytokine midkine binds the cell surface-expressed nucleolin as a low affinity receptor, J. Biol. Chem. 277, 37492-37502.
7. Semenkovich, C. F., Ostlund, R. E., Jr., Olson, M. O., and Yang, J. W. (1990) A protein partially expressed on the surface of HepG2 cells that binds lipoproteins specifically is nucleolin, Biochemistry 29, 9708-9713.
8. Hovanessian, A. G., Puvion-Dutilleul, F., Nisole, S., Svab, J., Perret, E., Deng, J. S., and Krust, B. (2000) The cell-surface-expressed nucleolin is associated with the actin cytoskeleton, Exp. Cell Res. 267, 312-328.
9. Take, M., Tsutsui, J., Obama, H., Ozawa, M., Nakayama, T., Maruyama, I., Arima, T., and Muramatsu, T. (1994) Identification of nucleolin as a binding protein for midkine (MK) and heparin-binding growth associated molecule (HB-GAM), J. Biochem. 116, 1063-1068.
10. Legrand, D., Vigie, K., Saïd, E. A., Elass, E., Masson, M., Slomianny, M. C., Carpentier, M., Briand, J. P., Mazurier, J., and Hovanessian, A. G. (2004) Surface nucleolin participates in both the binding and endocytosis of lactoferrin in target cells, Eur. J. Biochem. 271, 303-317.
11. Schmidt-Zachmann, M. S., and Nigg, E. A. (1993) Protein localization to the nucleolus: A search for targeting domains in nucleolin, J. Cell. Sci. 105, 799-806.
12. Peter, M., Nakagawa, J., Doree, M., Labbe, J. C., and Nigg, E. A. (1990) Identification of major nucleolar proteins as candidate mitotic substrates of cdc2 kinase, Cell 60, 791-801.
13. Zhou, G., Seibenhener, M. L., and Woolen, M. W. (1997) Nucleolin is a protein kinase C-ζ substrate. Connection between cell surface signaling and nucleus in PC12 cells, J. Biol. Chem. 272, 31130-31137.
14. Najbauer, J., Johnson, B. A., Young, A. L., and Aswad, D. W. (1993) Peptides with sequences similar to glycine, arginine-rich motifs in proteins interacting with RNA are efficiently recognized by methyltransferase(s) modifying arginine in numerous proteins, J. Biol. Chem. 268, 10501-10509.
15. Fang, S. H., and Yeh, N. H. (1993) The self-cleaving activity of nucleolin determines its molecular dynamics in relation to cell proliferation, Exp. Cell. Res. 208, 48-53.
16. Kukuruzinska, M. A., and Lennon, K. (1998) Protein N-glycosylation: Molecular genetics and functional significance, Crit. Rev. Oral Biol. Med. 9, 415-448.
17. Sairam, M. R. (1989) Role of carbohydrates in glycoprotein hormone signal transduction, FASEB J. 3, 915-926.
18. Wells, L., and Hart, G. W. (2003) O-GlcNAc turns twenty: Functional implications for post-translational modification of nuclear and cytosolic proteins with a sugar, FEBS Lett. 546, 154-158.
19. 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. 72, 9308-9315.
20. Galland, S., Degiuli, A., Frot-Coutaz, J., and Got, R. (1998) Transfer of N-acetylglucosamine to endogenous glycoproteins in the nucleus and in non-nuclear membranes of rat hepatocytes: Electrophoretic analysis of the endogenous acceptors, Biochem. Int. 7, 59-67.
21. Pedemonte, C. H., Sachs, G., and Kaplan, J. H. (1990) An intrinsic membrane glycoprotein with cytosolically oriented N-linked sugars, Proc. Natl. Acad. Sci. U.S.A. 87, 9789-9793.
22. Reeves, R., and Chang, D. (1983) Investigations of the possible functions for glycosylation in the high mobility group proteins. Evidence for a role in nuclear matrix association, J. Biol. Chem. 258, 679-687.
23. Roquemore, E. P., Chou, T. Y., and Hart, G. W. (1994) Detection of O-linked N-acetylglucosamine (O-GlcNAc) on cytoplasmic and nuclear proteins, Methods Enzymol. 230, 443-460.
24. Kane, R., Murtagh, J., Finlay, D., Marti, A., Jaggi, R., Blatchford, D., Wilde, C., and Martin, F. (2002) Transcription factor NFIC undergoes N-glycosylation during early mammary gland involution, J. Biol. Chem. 277, 25893-25903.
25. Callebaut, C., Blanco, J., Benkirane, N., Krust, B., Jacotot, E., Guichard, G., Seddiki, N., Svab, J., Dam, E., Muller, S., Briand, J. P., and Hovanessian, A. G. (1998) Identification of V3 loop-binding proteins as potential receptors implicated in the binding of HIV particles to CD4(+) cells, J. Biol. Chem. 273, 21988-21997.
26. Neuhoff, V., Arold, N., Taube, D., and Ehrhardt, W. (1988) Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250, Electrophoresis 6, 255-262.
27. Vercoutter-Edouart, A. S., Lemoine, J., Le Bourhis, X., Louis, H., Boilly, B., Nurcombe, V., Revillion, F., Peyrat, J. P., and Hondermarck, H. (2001) Proteomic analysis reveals that 14-3-3σ is down-regulated in human breast cancer cells, Cancer Res. 1, 76-80.
28. Altin, J. G., and Pagler, E. B. (1995) A one-step procedure for biotinylation and chemical cross-linking of lymphocyte surface and intracellular membrane-associated molecules, Anal. Biochem. 224, 382-389.
29. Palade, G. E., and Siekevitz, P. (1956) Liver microsomes: An integrated morphological and biochemical study, J. Biophys. Biochem. Cytol. 2, 171-200.
30. Pons, A., Riebet, C., Robbe, C., Hermann, A., Timmerman, P., Huet, G., Leroy, Y., Carlstedt, I., Capon, C., and Zanetta, J. P. (2003) Sequential GC/MS analysis of sialic acids, monosaccharides, and amino acids of glycoproteins on a single sample as heptafluorobutyrate derivatives, Biochemistry 42, 8342-8353.
31. Maes, E., Strecker, G., Timmerman, P., Leroy, Y., and Zanetta, J. P. (1999) Quantitative cleavage of the N-glycosidic bond under the normal conditions of methanolysis used for the analysis of glycoprotein monosaccharides, Anal. Biochem. 267, 300-308.
32. Geng, M., Zhang, X., Bina, M., and Regnier, F. (2001) Proteomics of glycoproteins based on affinity selection of glycopeptides from tryptic digests, J. Chromatogr., B: Biomed. Sci. Appl. 752, 293-306.
33. Mechref, Y., and Novotny, M. V. (1998) Mass spectrometric mapping and sequencing of N-linked oligosaccharides derived from submicrogram amounts of glycoproteins, Anal. Chem. 70, 455-463.
34. Chen, C. M., Chiang, S. Y., and Yen, N. H. (1991) Increased stability of nucleolin in proliferating cells by inhibition of its self-cleaving activity, J. Biol. Chem. 266, 7754-7758.
35. Heifetz, A., Keenan, R. W., and Elbein, A. D. (1979) Mechanism of action of tunicamycin on the UDP-GlcNAc:dolichyl-phosphate Glc-NAc-1-phosphate transferase, Biochemistry 18, 2186-2192.
36. Lotan, R., Beattie, G., Hubbell, W., and Nicolson, G. L. (1977) Activities of lectins and their immobilized derivatives in detergent solutions. Implications on the use of lectin affinity chromatography for the purification of membrane glycoproteins, Biochemistry 16, 1787-1794.
37. Hanover, J. A., Cohen, C. K., Willingham, M. C., and Park, M. K. (1987) O-linked N-acetylglucosamine is attached to proteins of the nuclear pore. Evidence for cytoplasmic and nucleoplasmic glycoproteins, J. Biol. Chem. 262, 9887-9894.
38. Yahara, I., and Edelman, G. M. (1972) Restriction of the mobility of lymphocyte immunoglobulin receptors by concanavalin A, Proc. Natl. Acad. Sci U.S.A. 69, 608-612.
39. Shibuya, N., Goldstein, I. J., van Damme, E. J., and Peumans, W. J. (1988) Binding properties of a mannose-specific lectin from the snowdrop (Galanthus nivalis) bulb, J. Biol. Chem. 263, 728-734.
40. Hashimoto, C., Cohen, R. E., Zhang, W. J., and Ballou, C. E. (1981) Carbohydrate chains on yeast carboxypeptidase Y are phosphorylated, Proc. Natl. Acad. Sci. U.S.A. 78, 2244-2248.
41. Nilsson, B., Norden, N. E., and Svensson, S. (1979) Structural studies on the carbohydrate portion of fetuin, J. Biol. Chem. 254. 4545-4553.
42. Edge, A. S., and Spiro, R. G. (1987) Presence of an O-glycosidically linked hexasaccharide in fetuin, J. Biol. Chem. 262, 16135-16141.
43. Finne, J., and Krusius, T. (1979) Structural features of the carbohydrate units of plasma glycoproteins, Eur. J. Biochem. 102, 583-588.
44. Goldstein, I. J., and Hayes, C. E. (1978) The lectins: Carbohydrate-binding proteins of plants and animals, Adv. Carbohydr. Chem. Biochem. 35, 127-140.
45. Crowley, J. F., and Goldstein, I. J. (1982) Datura stramonium lectin, Methods Enzymol. 83, 368-373.
46. Takahashi, T., and Nishibe, H. (1981) Almond glycopeptidase acting on aspartylglycosylamine linkages. Multiplicity and substrate specificity, Biochim. Biophys. Acta 657, 457-467.
47. Michalski, J. C. (1996) Normal and pathological of glycoprotein, New Compr. Biochem. 30, 55-97.
48. Iyer, S. P., and Hart, G. W. (2003) Dynamic nuclear and cytoplasmic glycosylation: Enzymes of O-GlcNAc cycling, Biochemistry 42, 2493-2499.
49. Lefebvre, T., Ferreira, S., Dupont-Wallois, L., Bussiere, T., Dupire, M. J., Delacourte, A., Michalski, J. C., and Caillet-Boudin, M. L. (2003) Evidence of a balance between phosphorylation and O-GlcNAc glycosylation of Tau proteins - A role in nuclear localization, Biochim. Biophys. Acta 1619, 167-176.
50. Salazar, R., Brandt, R., Kellerman, J., and Krantz, S. (2000) Purification and characterization of a 200 kDa fructosyllysine-specific binding protein from cell membranes of U397 cells, Glycoconjugate J. 17, 713-716.
51. Krantz, S., Salazar, R., Kellerman, J., and Lottspeich, F. (1995) Purification and partial amino acid sequencing of a fructosyllysine-specific binding protein from cell membranes of the monocyte-like cell line U397, Biochim. Biophys. Acta 1266, 109-112.
52. Medina, L., and Haltiwanger, R. S. (1998) Calf thymus high mobility group proteins are non-enzymatically glycated but not significantly glycosylated, Glycobiology 8, 191-198.
53. Polet, H., and Molnar, J. (1988) Demonstration that some of the nonhistone proteins, inducible to translocate into the nucleus, are glycosylated, J. Cell. Physiol. 135, 47-54.
54. Yoshida, Y., Chiba, T., Tokunaga, F., Kawasaki, H., Iwai, K., Suzuki, T., Ito, Y., Matsuoka, K., Yoshida, M., Tanaka, K., and Tai, T. (2002) E3 ubiquitin ligase that recognizes sugar chains, Nature 418, 438-442.
55. Tsai, B., Ye, Y., and Rapoport, T. A. (2002) Retro-translocation of proteins from the endoplasmic reticulum into the cytosol, Nat. Rev. Mol. Cell. Biol. 3, 246-255.
56. Allain, F. H. T., Gilbert, D. E., Bouvet, P., and Feigon, J. (2000) Solution structure of the two N-terminal RNA-binding domains of nucleolin and NMR study of the interaction with its RNA target, J. Mol. Biol. 303, 227-236.