Novel heparan mimetics potently inhibit the scrapie prion protein and its endocytosis

Biochemical and Biophysical Research Communications

Volumn 312, Issue 2, 2003, Pages 473-479

  Schonberger, Oshrat ^a   Horonchik, Lior ^a   Gabizon, Ruth ^b   Papy Garcia, Dulce ^d   Barritault, Denis ^c   Taraboulos, Albert ^a  

^a HEBREW UNIVERSITY   (Israel)

^b HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

^c UNIVERSITÉ PARIS EST CRÉTEIL   (France)

^d OTR3 Sarl ^*  (France)

Author keywords

[No Author keywords available]

Indexed keywords

AMIDE; BIOPOLYMER; DEXTRAN DERIVATIVE; GLUCOSE DERIVATIVE; HEPARAN; METHYL GROUP; PRION PROTEIN; SULFATE;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; CELL CULTURE; CHEMICAL PROCEDURES; CONTROLLED STUDY; CORRELATION ANALYSIS; ENDOCYTOSIS; MOUSE; NEUROBLASTOMA CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; SCRAPIE; SUBSTITUTION REACTION; SULFATION;

SCRAPIE PRION;

EID: 0344845037     PISSN: 0006291X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbrc.2003.10.150     Document Type: Article

References (40)

1. Caughey B.W., Dong A., Bhat K.S., Ernst D., Hayes S.F., Caughey W.S. Secondary structure analysis of the scrapie-associated protein PrP 27-30 in water by infrared spectroscopy. Biochemistry. 30:1991;7672-7680.
2. Pan K.M., Baldwin M., Nguyen J., Gasset M., Serban A., Groth D., Mehlhorn I., Huang Z., Fletterick R.J., Cohen F.E., et al. Conversion of alpha-helices into beta-sheets features in the formation of the scrapie prion proteins. Proc. Natl. Acad. Sci. USA. 90:1993;10962-10966.
3. Bolton D.C., McKinley M.P., Prusiner S.B. Identification of a protein that purifies with the scrapie prion. Science. 218:1982;1309-1311.
4. Meyer R.K., McKinley M.P., Bowman K.A., Braunfeld M.B., Barry R.A., Prusiner S.B. Separation and properties of cellular and scrapie prion proteins. Proc. Natl. Acad. Sci. USA. 83:1986;2310-2314.
5. Prusiner S.B., McKinley M.P., Bowman K.A., Bolton D.C., Bendheim P.E., Groth D.F., Glenner G.G. Scrapie prions aggregate to form amyloid-like birefringent rods. Cell. 35:1983;349-358.
6. McKinley M.P., Meyer R.K., Kenaga L., Rahbar F., Cotter R., Serban A., Prusiner S.B. Scrapie prion rod formation in vitro requires both detergent extraction and limited proteolysis. J. Virol. 65:1991;1340-1351.
7. Gabizon R., Meiner Z., Halimi M., Ben-Sasson S.A. Heparin-like molecules bind differentially to prion-proteins and change their intracellular metabolic fate. J. Cell. Physiol. 157:1993;319-325.
8. Warner R.G., Hundt C., Weiss S., Turnbull J.E. Identification of the heparan sulfate binding sites in the cellular prion protein. J. Biol. Chem. 277:2002;18421-18430.
9. Brown D.R., Qin K., Herms J.W., Madlung A., Manson J., Strome R., Fraser P.E., Kruck T., von Bohlen A., Schulz-Schaeffer W., Giese A., Westaway D., Kretzschmar H. The cellular prion protein binds copper in vivo. Nature. 390:1997;684-687.
10. Ehlers B., Diringer H. Dextran sulphate 500 delays and prevents mouse scrapie by impairment of agent replication in spleen. J. Gen. Virol. 65(Pt 8):1984;1325-1330.
11. Diringer H., Ehlers B. Chemoprophylaxis of scrapie in mice. J. Gen. Virol. 72(Pt 2):1991;457-460.
12. Ladogana A., Casaccia P., Ingrosso L., Cibati M., Salvatore M., Xi Y.G., Masullo C., Pocchiari M. Sulphate polyanions prolong the incubation period of scrapie-infected hamsters. J. Gen. Virol. 73(Pt 3):1992;661-665.
13. Caughey B., Raymond G.J. Sulfated polyanion inhibition of scrapie-associated PrP accumulation in cultured cells. J. Virol. 67:1993;643-650.
14. Kovalchuk O., Tzaban S., Tal Y., Horonchik L., Esko J.D., Vlodavsky I., Taraboulos A. Cellular heparan sulfate participates in the metabolism of prions. J. Biol. Chem. 2003.
15. Turnbull J., Powell A., Guimond S. Heparan sulfate: decoding a dynamic multifunctional cell regulator. Trends Cell Biol. 11:2001;75-82.
16. Blanquaert F., Saffar J.L., Colombier M.L., Carpentier G., Barritault D., Caruelle J.P. Heparan-like molecules induce the repair of skull defects. Bone. 17:1995;499-506.
17. Desgranges P., Barbaud C., Caruelle J.P., Barritault D., Gautron J. A substituted dextran enhances muscle fiber survival and regeneration in ischemic and denervated rat EDL muscle. FASEB J. 13:1999;761-766.
18. Yamauchi H., Desgranges P., Lecerf L., Papy-Garcia D., Tournaire M.C., Moczar M., Loisance D., Barritault D. New agents for the treatment of infarcted myocardium. FASEB J. 14:2000;2133-2134.
19. Meddahi A., Bree F., Papy-Garcia D., Gautron J., Barritault D., Caruelle J.P. Pharmacological studies of RGTA(11), a heparan sulfate mimetic polymer, efficient on muscle regeneration. J. Biomed. Mater. Res. 62:2002;525-531.
20. Ledoux D., Papy-Garcia D., Escartin Q., Sagot M.A., Cao Y., Barritault D., Courtois J., Hornebeck W., Caruelle J.P. Human plasmin enzymatic activity is inhibited by chemically modified dextrans. J. Biol. Chem. 275:2000;29383-29390.
21. Butler D.A., Scott M.R., Bockman J.M., Borchelt D.R., Taraboulos A., Hsiao K.K., Kingsbury D.T., Prusiner S.B. Scrapie-infected murine neuroblastoma cells produce protease-resistant prion proteins. J. Virol. 62:1988;1558-1564.
22. Naslavsky N., Shmeeda H., Friedlander G., Yanai A., Futerman A.H., Barenholz Y., Taraboulos A. Sphingolipid depletion increases formation of the scrapie prion protein in neuroblastoma cells infected with prions. J. Biol. Chem. 274:1999;20763-20771.
23. Naslavsky N., Stein R., Yanai A., Friedlander G., Taraboulos A. Characterization of detergent-insoluble complexes containing the cellular prion protein and its scrapie isoform. J. Biol. Chem. 272:1997;6324-6331.
24. Scott M.R., Kohler R., Foster D., Prusiner S.B. Chimeric prion protein expression in cultured cells and transgenic mice. Protein Sci. 1:1992;986-997.
25. Serban D., Taraboulos A., DeArmond S.J., Prusiner S.B. Rapid detection of Creutzfeldt-Jakob disease and scrapie prion proteins. Neurology. 40:1990;110-117.
26. Kascsak R.J., Rubenstein R., Merz P.A., Tonna-DeMasi M., Fersko R., Carp R.I., Wisniewski H.M., Diringer H. Mouse polyclonal and monoclonal antibody to scrapie-associated fibril proteins. J. Virol. 61:1987;3688-3693.
27. Taraboulos A., Scott M., Semenov A., Avrahami D., Laszlo L., Prusiner S.B., Avraham D. Cholesterol depletion and modification of COOH-terminal targeting sequence of the prion protein inhibit formation of the scrapie isoform. J. Cell Biol. 129:1995;121-132.
28. Brown D.A., Rose J.K. Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell. 68:1992;533-544.
29. Cohen E., Taraboulos A. Scrapie-like prion protein accumulates in aggresomes of cyclosporin A-treated cells. EMBO J. 22:2003;404-417.
30. Taraboulos A., Rogers M., Borchelt D.R., McKinley M.P., Scott M., Serban D., Prusiner S.B. Acquisition of protease resistance by prion proteins in scrapie-infected cells does not require asparagine-linked glycosylation. Proc. Natl. Acad. Sci. USA. 87:1990;8262-8266.
31. Caughey B., Race R.E. Potent inhibition of scrapie-associated PrP accumulation by congo red. J. Neurochem. 59:1992;768-771.
32. Borchelt D.R., Scott M., Taraboulos A., Stahl N., Prusiner S.B. Scrapie and cellular prion proteins differ in their kinetics of synthesis and topology in cultured cells. J. Cell Biol. 110:1990;743-752.
33. Vey M., Pilkuhn S., Wille H., Nixon R., DeArmond S.J., Smart E.J., Anderson R.G., Taraboulos A., Prusiner S.B. Subcellular colocalization of the cellular and scrapie prion proteins in caveolae-like membranous domains. Proc. Natl. Acad. Sci. USA. 93:1996;14945-14949.
34. Taraboulos A., Serban D., Prusiner S.B. Scrapie prion proteins accumulate in the cytoplasm of persistently infected cultured cells. J. Cell Biol. 110:1990;2117-2132.
35. McKinley M.P., Taraboulos A., Kenaga L., Serban D., Stieber A., DeArmond S.J., Prusiner S.B., Gonatas N. Ultrastructural localization of scrapie prion proteins in cytoplasmic vesicles of infected cultured cells. Lab. Invest. 65:1991;622-630.
36. Adjou K.T., Simoneau S., Sales N., Lamoury F., Dormont D., Papy-Garcia D., Barritault D., Deslys J.P., Lasmezas C.I. A novel generation of heparan sulfate mimetics for the treatment of prion diseases. J. Gen. Virol. 84:2003;2595-2603.
37. Hundt C., Peyrin J.M., Haik S., Gauczynski S., Leucht C., Rieger R., Riley M.L., Deslys J.P., Dormont D., Lasmezas C.I., Weiss S. Identification of interaction domains of the prion protein with its 37-kDa/67-kDa laminin receptor. EMBO J. 20:2001;5876-5886.
38. Rieger R., Edenhofer F., Lasmezas C.I., Weiss S. The human 37-kDa laminin receptor precursor interacts with the prion protein in eukaryotic cells. Nat. Med. 3:1997;1383-1388.
39. Stahl N., Borchelt D.R., Hsiao K., Prusiner S.B. Scrapie prion protein contains a phosphatidylinositol glycolipid. Cell. 51:1987;229-240.
40. Oesch B., Westaway D., Walchli M., McKinley M.P., Kent S.B., Aebersold R., Barry R.A., Tempst P., Teplow D.B., Hood L.E., et al. A cellular gene encodes scrapie PrP 27-30 protein. Cell. 40:1985;735-746.