Surface nucleolin participates in both the binding and endocytosis of lactoferrin in target cells

European Journal of Biochemistry

Volumn 271, Issue 2, 2004, Pages 303-317

  Legrand, Dominique ^a   Vigié, Keveen ^a   Said, Elias A ^b   Elass, Elisabeth ^a   Masson, Maryse ^a   Slomianny, Marie Christine ^a   Carpentier, Mathieu ^a   Briand, Jean Paul ^c   Mazurier, Joël ^a   Hovanessian, Ara G ^b  

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

^b CNRS   (France)

^c INSTITUT DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

Cancer; HIV; Lactoferrin; Receptor binding; Surface nucleolin

Indexed keywords

CELL EXTRACT; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; LACTOFERRIN; NUCLEOLIN; PROTEOGLYCAN; PSEUDOPEPTIDE;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BINDING COMPETITION; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL NUCLEUS; CELL SURFACE; CONTROLLED STUDY; ENDOCYTOSIS; FEMALE; HAMSTER; HUMAN; HUMAN CELL; INTERNALIZATION; MOLECULAR WEIGHT; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN ISOLATION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; SURFACE PLASMON RESONANCE; TARGET CELL;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; BINDING, COMPETITIVE; BREAST NEOPLASMS; CELL DIVISION; CELL MEMBRANE; CHO CELLS; CRICETINAE; ENDOCYTOSIS; FEMALE; HEPARAN SULFATE PROTEOGLYCANS; HIV-1; HUMANS; JURKAT CELLS; LACTOFERRIN; MICROSCOPY, CONFOCAL; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PEPTIDES; PHOSPHOPROTEINS; PROTEIN CONFORMATION; PROTEINS; RNA-BINDING PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SURFACE PLASMON RESONANCE;

ANIMALIA; CRICETINAE; CYTOMEGALOVIRUS; HUMAN HERPESVIRUS 5; HUMAN IMMUNODEFICIENCY VIRUS; MAMMALIA;

EID: 9144245356     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1033.2003.03929.x     Document Type: Article

References (52)

1. Ward, P.P., Uribe-Luna, S. & Conneely, O. (2002) Lactoferrin and host defense. Biochem. Cell Biol. 80, 95-102.
2. Brock, J.H. (2002) The physiology of lactoferrin. Biochem. Cell Biol. 80, 1-6.
3. Harmsen, M.C., Swart, P.J., de Bethune, M.P., Pauwels, R., De Clercq, E., The, T.H. & Meijer, D.K. (1995) Antiviral effects of plasma and milk proteins: lactoferrin shows potent activity against both human immunodeficiency virus and human cytomegalovirus replication in vitro. J. Infect. Dis. 172, 380-388.
4. Berkhout, B., van Wamel, J.L., Beljaars, L., Meijer, D.K., Visser, S. & Floris, R. (2002) Characterization of the anti-HIV effects of native lactoferrin and other milk proteins and protein-derived peptides. Antiviral Res. 55, 341-355.
5. Moriuchi, M. & Moriuchi, H. (2001) A milk protein lactoferrin enhances human T cell leukemia virus type I and suppresses HIV-1 infection. J. Immunol. 166, 4231-4236.
6. Legrand, D., van Berkel, P.H., Salmon, V., van Veen, H.A., Slomianny, M.C., Nuijens, J.H. & Spik, G. (1997) The N-terminal Arg2, Arg3 and Arg4 of human lactoferrin interact with sulphated molecules but not with the receptor present on Jurkat human lymphoblastic T-cells. Biochem. J. 327, 841-846.
7. Damiens, E., El Yazidi, I., Mazurier, J., Elass-Rochard, E., Duthille, I., Spik, G. & Boilly-Marer, Y. (1998) Role of heparan sulphate proteoglycans in the regulation of human lactoferrin binding and activity in the MDA-MB-231 breast cancer cell line. Eur. J. Cell Biol. 77, 344-351.
8. Mazurier, J., Legrand, D., Hu, W.L., Montreuil, J. & Spik, G. (1989) Expression of human lactotransferrin receptors in phyto-hemagglutinin- stimulated human peripheral blood lymphocytes. Isolation of the receptors by antiligand-affinity chromatography. Eur. J. Biochem. 179, 481-487.
9. Leveugle, B., Mazurier, J., Legrand, D., Mazurier, C., Montreuil, J. & Spik, G. (1993) Lactotransferrin binding to its platelet receptor inhibits platelet aggregation. Eur. J. Biochem. 213, 1205-1211.
10. Suzuki, Y.A., Shin, K. & Lönnerdal, B. (2001) Molecular cloning and functional expression of a human intestinal lactoferrin receptor. Biochemistry 40, 15771-15779.
11. Huettinger, M., Retzek, H., Hermann, M. & Goldenberg, H. (1992) Lactoferrin specifically inhibits endocytosis of chylomicron remnants but not alpha-macroglobulin. J. Biol. Chem. 267, 18551-18557.
12. Dhennin-Duthille, I., Masson, M., Damiens, E., Fillebeen, C., Spik, G. & Mazurier, J. (2000) Lactoferrin upregulates the expression of CD4 antigen through the stimulation of the mitogen-activated protein kinase in the human lymphoblastic T Jurkat cell line. J. Cell Biochem. 79, 583-593.
13. Oh, S.M., Hahm, D.H., Kim, I.H. & Choi, S.Y. (2001) Human neutrophil lactoferrin trans-activates the matrix metalloproteinase 1 gene through stress-activated MAPK signaling modules. J. Biol. Chem. 276, 42575-42579.
14. Garre, C., Bianchi-Scarra, G., Sirito, M., Musso, M. & Ravazzolo, R. (1992) Lactoferrin binding sites and nuclear localization in K562 (S) cells. J. Cell. Physiol. 153, 477-482.
15. He, J. & Furmanski, P. (1995) Sequence specificity and transcriptional activation in the binding of lactoferrin to DNA. Nature 373, 721-724.
16. Damiens, E., El Yazidi, I., Mazurier, J., Duthille, I., Spik, G. & Boilly-Marer, Y. (1999) Lactoferrin inhibits G1 cyclin-dependent kinases during growth arrest of human breast carcinoma cells. J. Cell Biochem. 74, 486-498.
17. Kleinman, H.K., Weeks, B.S., Cannon, F.B., Sweeney, T.M., Sephel, G.C., Clement, B., Zain, M., Olson, M.O., Jucker, M. & 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.
18. Take, M., Tsutsui, J., Obama, H., Ozawa, M., Nakayama, T., Maruyama, I., Arima, T. & Muramatsu, T. (1994) Identification of nucleolin as a binding protein for midkine (MK) and heparin-binding growth associated molecule (HB-GAM). J. Biochem. (Tokyo) 116, 1063-1068.
19. Said, E.A., Krust, B., Nisole, S., Svab, J., Briand, J.P. & 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.
20. Larrucea, S., Gonzalez-Rubio, C., Cambronero, R., Ballou, B., Bonay, P., Lopez-Granados, E., Bouvet, P., Fontan, G., Fresno, M. & Lopez-Trascasa, M. (1998) Cellular adhesion mediated by factor J, a complement inhibitor. Evidence for nucleolin involvement. J. Biol. Chem. 273, 31718-31725.
21. Semenkovich, C.F., Ostlund, R.E., Olson, M.O. & Yang, J.W. (1990) A protein partially expressed on the surface of HepG2 cells that binds lipoproteins specifically is nucleolin. Biochemistry 29, 9708-9713.
22. Srivastava, M. & Pollard, H.B. (1999) Molecular dissection of nucleolin's role in growth and cell proliferation: new insights. FASEB J. 13, 1911-1922.
23. Hovanessian, A.G., Puvion-Dutilleul, F., Nisole, S., Svab, J., Perret, E., Deng, J.S. & Krust, B. (2000) The cell-surface-expressed nucleolin is associated with the actin cytoskeleton. Exp. Cell Res. 261, 312-328.
24. Nisole, S., Krust, B., Callebaut, C., Guichard, G., Muller, S., Briand, J.P. & Hovanessian, A.G. (1999) The anti-HIV pseudopeptide HB-19 forms a complex with the cell-surface-expressed nucleolin independent of heparan sulfate proteoglycans. J. Biol. Chem. 274, 27875-27884.
25. Nisole, S., Krust, B., Dam, E., Bianco, A., Seddiki, N., Loaec, S., Callebaut, C., Guichard, G., Muller, S., Briand, J.P. & Hovanessian, A.G. (2000) The HB-19 pseudopeptide 5[Kpsi (CH2N) PR]-TASP inhibits attachment of T lymphocyte-and macrophage-tropic HIV to permissive cells. AIDS Res. Hum. Retroviruses 16, 237-249.
26. Nisole, S., Said, E.A., Mische, C., Prevost, M.C., Krust, B., Bouvet, P., Bianco, A., Briand, J.P. & Hovanessian, A.G. (2002) The anti-HIV pentameric pseudopeptide HB-19 binds the C-terminal end of nucleolin and prevents anchorage of virus particles in the plasma membrane of target cells. J. Biol. Chem. 277, 20877-20886.
27. Esko, J.D., Rostand, K.S. & Weinke, J.L. (1988) Tumor formation dependent on proteoglycan biosynthesis. Science 241, 1092-1096.
28. Spik, G., Strecker, G., Fournet, B., Bouquelet, S., Montreuil, J., Dorland, L., van Halbeek, H. & Vliegenthart, J.F. (1982) Primary structure of the glycans from human lactotransferrin. Eur. J. Biochem. 121, 413-419.
29. Deng, J.S., Ballou, B. & Hofmeister, J.K. (1996) Internalization of anti-nucleolin antibody into viable HEp-2 cells. Mol. Biol. Report 23, 191-195.
30. Legrand, D., Mazurier, J., Aubert, J.P., Loucheux-Lefebvre, M.H., Montreuil, J. & Spik, G. (1986) Evidence for interactions between the 30 kDa N-and 50 kDa C-terminal tryptic fragments of human lactotransferrin. Biochem. J. 236, 839-844.
31. Legrand, D., Mazurier, J., Colavizza, D., Montreuil, J. & Spik, G. (1990) Properties of the iron-binding site of the N-terminal lobe of human and bovine lactotransferrins. Importance of the glycan moiety and of the non-covalent interactions between the N-and C-terminal lobes in the stability of the iron-binding site. Biochem. J. 266, 575-581.
32. Callebaut, C., Blanco, J., Benkirane, N., Krust, B., Jacotot, E., Guichard, G., Seddiki, N., Svab, J., Dam, E., Muller, S., Briand, J.P. & 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.
33. Seddiki, N., Nisole, S., Krust, B., Callebaut, C., Guichard, G., Muller, S., Briand, J.P. & Hovanessian, A.G. (1999) The V3 loop-mimicking pseudopeptide 5[Kpsi (CH2N) PR]-TASP inhibits HTV infection in primary macrophage cultures. AIDS Res. Hum. Retroviruses 15, 381-390.
34. Vercoutter-Edouart, A.S., Czeszak, X., Crépin, M., Lemoine, J., Boilly, B., Le Bourhis, X., Peyrat, J.P. & Hondermarck, H. (2001) Proteomic detection of changes in protein synthesis induced by fibroblast growth factor-2 in MCF-7 human breast cancer cells. Exp. Cell Res. 262, 59-68.
35. Callebaut, C., Nisole, S., Briand, J.P., Krust, B. & Hovanessian, A.G. (2001) Inhibition of HIV infection by the cytokine midkine. Virology 281, 248-264.
36. Lapeyre, B., Bourbon, H. & 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, 1472-1476.
37. Mann, D.M., Romm, E. & Migliorini, M. (1994) Delineation of the glycosaminoglycan-binding site in the human inflammatory response protein lactoferrin. J. Biol. Chem. 269, 23661-23667.
38. van Berkel, P.H., Geerts, M.E., van Veen, H.A., Mericskay, M., de Boer, H.A. & Nuijens, J.H. (1997) N-terminal stretch Arg2, Arg3, Arg4 and Arg5 of human lactoferrin is essential for binding to heparin, bacterial lipopolysaccharide, human lysozyme and DNA. Biochem. J. 328, 145-151.
39. Hurley, W.L., Hegarty, H.M. & Metzler, J.T. (1994) In vitro inhibition of mammary cell growth by lactoferrin: a comparative study. Life Sci. 55, 1955-1963.
40. Smart, E.J., Graf, G.A., McNiven, M.A., Sessa, W.C., Engelman, J.A., Scherer, P.E., Okamoto, T. & Lisanti, M.P. (1999) Caveolins, liquid-ordered domains, and signal transduction. Mol. Cell. Biol. 19, 7289-7304.
41. Penco, S., Scarfi, S., Giovine, M., Damonte, G., Millo, E., Villaggio, B., Passalacqua, M., Pozzolini, M., Garre, C. & Benatti, U. (2001) Identification of an import signal for, and the nuclear localization of, human lactoferrin. Biotechnol. Appl. Biochem. 34, 151-159.
42. Ghisolfi, L., Joseph, G., Amalric, F. & Erard, M. (1992) The glycine-rich domain of nucleolin has an unusual supersecondary structure responsible for its RNA-helix-destabilizing properties. J. Biol. Chem. 267, 2955-2959.
43. Hanakahi, L.A., Sun, H. & Maizels, N. (1999) High affinity interactions of nucleolin with G-G-paired rDNA. J. Biol. Chem. 274, 15908-15912.
44. Bouvet, P., Diaz, J.-J., Kindbeiter, K., Madjar, J.-J. & Amalric, F. (1998) Nucleolin interacts with several ribosomal proteins through its RGG domain. J. Biol. Chem. 273, 19025-19029.
45. Dougherty, D.A. (1996) Cation-pi interactions in chemistry and biology: a new view of benzene, Phe, Tyr, and Trp. Science 271, 163-168.
46. Yu, R.H. & Schryvers, A.B. (1993) Regions located in both the N-lobe and C-lobe of human lactoferrin participate in the binding interaction with bacterial lactoferrin receptors. Microb. Pathog. 14, 343-353.
47. Lobie, P.E., Mertani, H., Morel, G., Marales-Bustos, O., Noestedt, G. & Waters, M.J. (1994) Receptor-mediated nuclear translocation of growth hormone. J. Biol. Chem. 269, 21330-21339.
48. Rycyzyn, M.A. & Clevenger, C. (2002) The intranuclear prolactin/cyclophilin B complex as a transcriptional inducer. Proc. Natl Acad. Sci. USA 99, 6790-6795.
49. Shibata, Y., Muramatsu, T., Hirai, M., Inui, T., Kimura, T., Saito, H., McCormick, L.M., Bu, G. & Kadomatsu, K. (2002) Nuclear targeting by the growth factor midkine. Mol. Cell. Biol. 22, 6788-6796.
50. Steinfeld, R., Van Den Berghe, H. & David, G. (1996) Stimulation of fibroblast growth factor receptor-1 occupancy and signaling by cell surface-associated syndecans and glypican. J. Cell. Biol. 133, 405-416.
51. Berger, E.A. (1997) HIV entry and tropism: the chemokine receptor connection. AIDS 1, S3-S16.
52. Anderson, B.F., Baker, H.M., Dodson, E.J., Norris, G.E., Rumball, S.V., Waters, J.M. & Baker, E.N. (1987) Structure of human lactoferrin at 3.2-Å resolution. Proc. Natl Acad. Sci. USA 84, 1769-1773.