Nucleolin: Acharan sulfate-binding protein on the surface of cancer cells

Glycobiology

Volumn 15, Issue 1, 2005, Pages 1-9

  Joo, Eun Ji ^a   ten Dam, Gerdy B ^b   van Kuppevelt, Toin H ^b   Toida, Toshihiko ^c   Linhardt, Robert J ^d   Kim, Yeong Shik ^a  

^a Seoul National University   (South Korea)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c CHIBA UNIVERSITY   (Japan)

^d RENSSELAER POLYTECHNIC INSTITUTE   (United States)

Author keywords

AS binding protein; Biotinylation; Lewis lung carcinoma; Nucleolin

Indexed keywords

ACHARAN SULFATE; ALCIAN BLUE; BASIC FIBROBLAST GROWTH FACTOR; CELL SURFACE RECEPTOR; GLYCOSAMINOGLYCAN; HEPARIN; LIGAND; MIDKINE; NUCLEOLIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; BIOTINYLATION; CANCER CELL; CARBOHYDRATE ANALYSIS; CELL FRACTIONATION; CELL LYSATE; CELL SURFACE; CYTOTOXICITY; ELECTROSPRAY MASS SPECTROMETRY; IMMUNOFLUORESCENCE TEST; IN VITRO STUDY; INCUBATION TIME; LEWIS CARCINOMA; MOLECULAR WEIGHT; MOUSE; NONHUMAN; PERIODIC ACID SCHIFF STAIN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; SILVER STAINING; SNAIL; STAINING; TIME OF FLIGHT MASS SPECTROMETRY; TUMOR GROWTH; WESTERN BLOTTING;

AMINO ACID SEQUENCE; ANIMALS; BLOTTING, WESTERN; CELL ADHESION; CELL LINE, TUMOR; CELL MEMBRANE; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GLYCOSAMINOGLYCANS; HUMANS; MASS SPECTROMETRY; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; NEOPLASMS; PHOSPHOPROTEINS; RNA-BINDING PROTEINS;

ACHATINA FULICA; FULICA; GASTROPODA;

EID: 13444252904     PISSN: 09596658     EISSN: None     Source Type: Journal    
DOI: 10.1093/glycob/cwh132     Document Type: Article

References (43)

1. Ahrens, T., Assmann, V., Fieber, C., Termeer, C., Herrlich, P., Hofmann, M., and Simon, J.C. (2001) CD44 is the principal mediator of hyaluronic-acid-induced melanoma cell proliferation. J. Invest. Dermatol., 116, 93-101.
2. Akiyama, Y., Jung, S., Salhia, B., Lee, S., Hubbard, S., Taylor, M., Mainprize, T., Akaishi, K., van Furth, W., and Rutka, J.T. (2001) Hyaluronate receptors mediating glioma cell migration and proliferation. J. Neurooncol., 53, 115-127.
3. Alban, S. and Gastpar, R. (2001) Development of SPC-ELISA: a new assay principle for the study of sulfated polysaccharide-protein interactions. J. Biomol. Screen., 6, 393-400.
4. Asplund, T. and Heldin, P. (1994) Hyaluronan receptors are expressed on human malignant mesothelioma cells but not on normal mesothelial cells. Cancer Res., 54, 4516-4523.
5. Assmann, V., Marshall, J.F., Fieber, C., Hofmann, M., and Hart, I.R. (1998) The human hyaluronan receptor RHAMM is expressed as an intracellular protein in breast cancer cells. J. Cell Sci., 111 1685-1694.
6. Bitter, T. and Muir, H.M. (1962) A modified uronic acid carbazole reaction. Anal. Biochem., 4, 330-334.
7. Borsig, L., Wong, R., Feramisco, J., Nadeau, D.R., Varki, N.M., and Varki, A. (2001) Heparin and cancer revisited: mechanistic connections involving platelets, P-selectin, carcinoma mucins, and tumor metastasis. Proc. Natl Acad. Sci. USA, 98, 3352-3357.
8. Callebaut, C., Nisole, S., Briand, J.P., Krust, B., and Hovanessian, A.G. (2001) Inhibition of HIV infection by the cytokine midkine. Virology, 281, 248-264.
9. Capila, I. and Linhardt, R.J. (2002) Heparin-protein interactions. Angew. Chem. Int. Ed. Engl., 41, 391-412.
10. Choudhuri, R., Zhang, H.T., Donnini, S., Ziche, M., and Bicknell, R. (1997) An angiogenic role for the neurokines midkine and pleiotrophin in tumorigenesis. Cancer Res., 57, 1814-1819.
11. Christian, S., Pilch, J., Akerman, M.E., Porkka, K., Laakkonen, P., and Ruoslahti, E. (2003) Nucleolin expressed at the cell surface is a marker of endothelial cells in angiogenic blood vessels. J. Cell. Biol., 163, 871-878.
12. Cole, S.R., Ashman, L.K., and Ey, P.L. (1987) Biotinylation: an alternative to radioiodination for the identification of cell surface antigens in immunoprecipitates. Mol. Immunol., 24, 699-705.
13. Engbring, J.A., Hoffman, M.P., Karmand, A.J., and Kleinman, H.K. (2002) The B16F10 cell receptor for a metastasis-promoting site on laminin-1 is a heparan sulfate/chondroitin sulfate-containing proteoglycan. Cancer Res., 62, 3549-3554.
14. Folkman, J. and Shing, Y. (1992) Control of angiogenesis by heparin and other sulfated polysaccharides. Adv. Exp. Med. Biol., 313, 355-364.
15. Ghosh, A.K., Hirasawa, N., Lee, Y.S., Kim, Y.S., Shin, K.H., Ryu, N., and Ohuchi, K. (2002) Inhibition by acharan sulphate of angiogenesis in experimental inflammation models. Br. J. Pharmacol. 137, 441-448.
16. Goicoechea, S., Orr, A.W., Pallero, M.A., Eggleton, P., and Murphy-Ullrich, J.E. (2000) Thrombospondin mediates focal adhesion dis-assembly through interactions with cell surface calreticulin. J. Biol. Chem., 275, 36358-36368.
17. Harms, G., Kraft, R., Grelle, G., Volz, B., Dernedde, J., and Tauber, R. (2001) Identification of nucleolin as a new L-selectin ligand. Biochem. J., 360, 531-538.
18. Herrera-Gayol, A. and Jothy, S. (2001) Effects of hyaluronan on the invasive properties of human breast cancer cells in vitro. Int. J. Exp. Pathol., 82, 193-200.
19. 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., 261, 312-328.
20. Jeong, J., Toida, T., Muneta, Y., Kosiishi, I., Imanari, T., Linhardt, R.J., Choi, H.S., Wu, S.J., and Kim, Y.S. (2001) Localization and characterization of acharan sulfate in the body of the giant African snail Achatina fulica. Comp. Biochem. Physiol. B, 130, 513-519.
21. Jordan, P., Heid, H., Kinzel, V., and Kubler, D. (1994) Major cell surface-located protein substrates of an ecto-protein kinase are homologs of known nuclear proteins. Biochemistry, 33, 14696-14706.
22. Kim, Y.S., Jo, Y.Y., Chang, I.M., Toida, T., Park, Y., and Linhardt, R.J. (1996) A new glycosaminoglycan from the giant African snail Achatina fulica. J. Biol. Chem., 271, 11750-11755.
23. Kleinman, H.K., Weeks, B.S., Cannon, F.B., Sweeney, T.M., Sephel, G.C., Clement, B., Zain, M., Olson, M.O., Jucker, M., and Burrous, B.A. (1991) Identification of a 110-kDa nonintegrin cell surface laminin-binding protein which recognizes an A chain neurite-promoting peptide. Arch. Biochem. Biophys., 290, 320-325.
24. 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. USA, 84(6), 1472-1476.
25. Lee, C.H., Chang, S.C., Chen, C.J., and Chang, M.F. (1998) The nucleolin binding activity of hepatitis delta antigen is associated with nucleolus targeting. J. Biol. Chem., 273, 7650-7656.
26. Lee, Y.S., Yang, H.O., Shin, K.H., Choi, H.S., Jung, S.H., Kim, Y.M., Oh, D.K., Linhardt, R.J., and Kim, Y.S. (2003) Suppression of tumor growth by a new glycosaminoglycan isolated from the African giant snail Achatina fulica. Eur. J. Pharmacol., 465, 191-198.
27. Legrand, D., Vigie, K., Said, 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.
28. Lever, R. and Page, C.P. (2002). Novel drug development opportunities for heparin. Nat. Rev. Drug. Discov., 1, 140-148.
29. Maeda, N., Ichihara-Tanaka, K., Kimura, T., Kadomatsu, K., Muramatsu, T., and Noda, M. (1999) A receptor-like protein-tyrosine phosphatase PTPzeta/RPTPbeta binds a heparin-binding growth factor midkine. Involvement of arginine 78 of midkine in the high affinity binding to PTPzeta. J. Biol. Chem., 274, 12474-12479.
30. Muramatsu, H., Shirahama, H., Yonezawa, S., Maruta, H., and Muramatsu, T. (1993) Midkine, a retinoic acid-inducible growth/differentiation factor: immunochemical evidence for the function and distribution. Dev. Biol., 159, 392-402.
31. Orrick, L.R., Olson, M.O., and Busch, H. (1973) Comparison of nucleolar proteins of normal rat liver and Novikoff hepatoma ascites cells by two-dimensional polyacrylamide gel electrophoresis. Proc. Natl Acad. Sci. USA, 70, 1316-1320.
32. Pumphrey, C.Y., Theus, A.M., Li, S., Parrish, R.S., and Sanderson, R.D. (2002) Neoglycans, carbodiimide-modified glycosaminoglycans: a new class of anticancer agents that inhibit cancer cell proliferation and induce apoptosis. Cancer Res., 62, 3722-3728.
33. Sasisekharan, R., Shriver, Z., Venkataraman, G., and Narayanasami, U. (2002) Roles of heparan-sulphate glycosaminoglycans in cancer. Nat. Rev. Cancer, 2, 521-528.
34. Savani, R.C., Cao, G., Pooler, P.M., Zaman, A., Zhou, Z., and DeLisser, H.M. (2001) Differential involvement of the hyaluronan (HA) receptors CD44 and receptor for HA-mediated motility in endothelial cell function and angiogenesis. J. Biol. Chem., 276, 36770-36778.
35. Schmidtchen, A., Frick, I.M., and Bjorck, L. (2001) Dermatan sulphate is released by proteinases of common pathogenic bacteria and inactivates antibacterial alpha-defensin. Mol. Microbiol., 39 708-713.
36. 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.
37. Shim, J.Y., Lee, Y.S., Jung, S.H., Choi, H.S., Shin, K.H., and Kim, Y.S. (200) Pharmacological activities of a new glycosaminoglycan, acharan sulfate isolated from the giant African snail Achatina fulica. Arch. Pharm. Res., 25, 889-894.
38. 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.
39. Sumi, Y., Muramatsu, H., Takei, Y., Hata, K., Ueda, M., and Muramatsu, T. (2002) Midkine, a heparin-binding growth factor, promotes growth and glycosaminoglycan synthesis of endothelial cells through its action on smooth muscle cells in an artificial blood vessel model. J. Cell. Sci., 115, 2659-2667.
40. n. J. Biol. Chem., 279 38346-38352.
41. Wang, H., Toida, T., Kim, Y.S., Capila, I., Hileman, R.E., Bernfield, M., and Linhardt, R.J. (1997) Glycosaminoglycans can influence fibroblast growth factor-2 mitogenicity without significant growth factor binding. Biochem. Biophys. Res. Commun., 235, 369-373.
42. Westergren-Thorsson, G., Onnervik, P.O., Fransson, L.A., and Malmstrom, A. (1991) Proliferation of cultured fibroblasts is inhibited by L-iduronate-containing glycosaminoglycans. J. Cell. Physiol., 147, 523-530.
43. Wu, S.L., Amato, H., Biringer, R., Choudhary, G., Shieh, P., and Hancock, W.S. (2002) Targeted proteomics of low-level proteins in human plasma by LC/MSn: using human growth hormone as a model system. J. Proteome. Res., 1, 459-465.