Cellular heparan sulfate participates in the metabolism of prions

Journal of Biological Chemistry

Volumn 278, Issue 41, 2003, Pages 40041-40049

  Ben Zaken, Olga ^a   Tzaban, Salit ^b   Tal, Yuval ^b   Horonchik, Lior ^b   Esko, Jeffrey D ^c   Vlodavsky, Israel ^d   Taraboulos, Albert ^b  

^a HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

^b HEBREW UNIVERSITY   (Israel)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; DISEASES; FLOTATION; FLUORESCENCE; IMMUNOLOGY; MICROSCOPIC EXAMINATION; PROTEINS;

BIOGENESIS;

METABOLISM;

CHONDROITIN ABC LYASE; CHONDROITIN SULFATE; ESTRADIOL DERIVATIVE; GLYCOSAMINOGLYCAN; HEPARAN SULFATE; HEPARIN LYASE; PRION PROTEIN; SODIUM CHLORATE; XYLOSE;

ACIDITY; ANIMAL CELL; ARTICLE; BIOGENESIS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; IMMUNOFLUORESCENCE MICROSCOPY; MOUSE; NONHUMAN; PRION DISEASE; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN METABOLISM; SULFATION;

ANIMALS; GLYCOSAMINOGLYCANS; GLYCOSIDES; GLYCOSYLATION; HEPARIN LYASE; HEPARITIN SULFATE; MICE; MODELS, BIOLOGICAL; POLYSACCHARIDE-LYASES; PRION DISEASES; PRPC PROTEINS; PRPSC PROTEINS;

ANIMALIA;

EID: 0141994735     PISSN: 00219258     EISSN: None     Source Type: Journal    
DOI: 10.1074/jbc.M301152200     Document Type: Article

References (74)

1. Gibbs, C. J., Jr., and Gajdusek, D. C. (1969) Science 165, 1023-1025
2. Wilesmith, J. W., Wells, G. A., Cranwell, M. P., and Ryan, J. B. (1988) Vet. Rec. 123, 638-644
3. Prusiner, S. B. (1982) Science 216, 136-144
4. 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. (1993) Proc. Natl. Acad. Sci. U. S. A. 90, 10962-10966
5. Caughey, B., and Raymond, G. J. (1991) J. Biol. Chem. 266, 18217-18223
6. Prusiner, S. B. (1998) Proc. Natl. Acad. Sci. U. S. A. 95, 13363-13383
7. Come, J. H., Fraser, P. E., and Lansbury, P. T., Jr. (1993) Proc. Natl. Acad. Sci. U. S. A. 90, 5959-5963
8. Tzaban, S., Friedlander, G., Schonberger, O., Horonchik, L., Yedidia, Y., Shaked, G., Gabizon, R., and Taraboulos, A. (2002) Biochemistry 41, 12868-12875
9. Meyer, R. K., McKinley, M. P., Bowman, K. A., Braunfeld, M. B., Barry, R. A., and Prusiner, S. B. (1986) Proc. Natl. Acad. Sci. U. S. A. 83, 2310-2314
10. Borchelt, D. R., Scott, M., Taraboulos, A., Stahl, N., and Prusiner, S. B. (1990) J. Cell Biol. 110, 743-752
11. Borchelt, D. R., Taraboulos, A., and Prusiner, S. B. (1992) J. Biol. Chem. 267, 16188-16199
12. Taraboulos, A., Raeber, A. J., Borchelt, D. R., Serban, D., and Prusiner, S. B. (1992) Mol. Biol. Cell. 3, 851-863
13. Telling, G. C., Scott, M., Mastrianni, J., Gabizon, R., Torchia, M., Cohen, F. E., DeArmond, S. J., and Prusiner, S. B. (1995) Cell 83, 79-90
14. Rieger, R., Edenhofer, F., Lasmezas, C. I., and Weiss, S. (1997) Nat. Med. 3, 1383-1388
15. Graner, E., Mercadante, A. F., Zanata, S. M., Forlenza, O. V., Cabral, A. L., Veiga, S. S., Juliano, M. A., Roesler, R., Walz, R., Minetti, A., Izquierdo, I., Martins, V. R., and Brentani, R. R. (2000) Brain Res. Mol. Brain Res. 76, 85-92
16. Gauczynski, S., Peyrin, J. M., Haik, S., Leucht, C., Hundt, C., Rieger, R., Krasemann, S., Deslys, J. P., Dormont, D., Lasmezas, C. I., and Weiss, S. (2001) EMBO J. 20, 5863-5875
17. Hundt, C., Peyrin, J. M., Haik, S., Gauczynski, S., Leucht, C., Rieger, R., Riley, M. L., Deslys, J. P., Dormont, D., Lasmezas, C. I., and Weiss, S. (2001) EMBO J. 20, 5876-5886
18. Zanata, S. M., Lopes, M. H., Mercadante, A. F., Hajj, G. N., Chiarini, L. B., Nomizo, R., Freitas, A. R., Cabral, A. L., Lee, K. S., Juliano, M. A., de Oliveira, E., Jachieri, S. G., Burlingame, A., Huang, L., Linden, R., Brentani, R. R., and Martins, V. R. (2002) EMBO J. 21, 3307-3316
19. Diaz-Nido, J., Wandosell, F., and Avila, J. (2002) Peptides 23, 1323-1332
20. Snow, A. D., Kisilevsky, R., Willmer, J., Prusiner, S. B., and DeArmond, S. J. (1989) Acta Neuropathol. 77, 337-342
21. McBride, P. A., Wilson, M. I., Eikelenboom, P., Tunstall, A., and Bruce, M. E. (1998) Exp. Neurol. 149, 447-454
22. Gabizon, R., Meiner, Z, Halimi, M., and Ben-Sasson, S. A. (1993) J. Cell. Physiol. 157, 319-325
23. Ladogana, A., Casaccia, P., Ingrosso, L., Cibati, M., Salvatore, M., Xi, Y. G., Masullo, C., and Pocchiari, M. (1992) J. Gen. Virol. 73, 661-665
24. Ehlers, B., and Diringer, H. (1984) J. Gen. Virol. 65, 1325-1330
25. Caughey, B., and Raymond, G. J. (1993) J. Virol. 67, 643-650
26. Caughey, B., Brown, K., Raymond, G. J., Katzenstein, G. E., and Thresher, W. (1994) J. Virol. 68, 2135-2141
27. Warner, R. G., Hundt, C., Weiss, S., and Turnbull, J. E. (2002) J. Biol. Chem. 277, 18421-18430
28. Wong, C., Xiong, L. W., Horiuchi, M., Raymond, L., Wehrly, K., Chesebro, B., and Caughey, B. (2001) EMBO J. 20, 377-386
29. Shaked, G. M., Meiner, Z., Avraham, I., Taraboulos, A., and Gabizon, R. (2001) J. Biol. Chem. 276, 14324-14328
30. Shyng, S. L., Lehmann, S., Moulder, K. L., and Harris, D. A. (1995) J. Biol. Chem. 270, 30221-30229
31. Gilch, S., Winklhofer, K. F., Groschup, M. H., Nunziante, M., Lucassen, R., Spielhaupter, C., Muranyi, W., Riesner, D., Tatzelt, J., and Schatzl, H. M. (2001) EMBO J. 20, 3957-3966
32. Schwartz, N. B., Galligani, L., Ho, P. L., and Dorfman, A. (1974) Proc. Natl. Acad. Sci. U. S. A. 71, 4047-4051
33. Fritz, T. A., Lugemwa, F. N., Sarkar, A. K., and Esko, J. D. (1994) J. Biol. Chem. 269, 300-307
34. Lugemwa, F. N., and Esko, J. D. (1991) J. Biol. Chem. 266, 6674-6677
35. Naslavsky, N., Stein, R., Yanai, A., Friedlander, G., and Taraboulos, A. (1997) J. Biol. Chem. 272, 6324-6331
36. Kascsak, R. J., Rubenstein, R., Merz, P. A., Tonna-DeMasi, M., Fersko, R., Carp, R. I., Wisniewski, H. M., and Diringer, H. (1987) J. Virol. 61, 3688-3693
37. Birkett, C. R., Hennion, R. M., Bembridge, D. A., Clarke, M. C., Chree, A., Bruce, M. E., and Bostock, C. J. (2001) EMBO J. 20, 3351-3358
38. Vlodavsky, I. (1999) in Current Protocols in Cell Biology (Bonifacino, J. S., Dasso, M., Hartford, J. B., Lippincott-Schwartz, J., and Yamada, K. M., eds) Vol. 1, pp. 10.14.11-10.14.14, John Wiley & Sons, Inc., New York
39. Rogers, M., Serban, D., Gyuris, T., Scott, M., Torchia, T., and Prusiner, S. B. (1991) J. Immunol. 147, 3568-3574
40. Scott, M. R., Kohler, R., Foster, D., and Prusiner, S. B. (1992) Protein Sci. 1, 986-997
41. Naslavsky, N., Shmeeda, H., Friedlander, G., Yanai, A., Futerman, A. H., Barenholz, Y., and Taraboulos, A. (1999) J. Biol. Chem. 274, 20763-20771
42. Taraboulos, A., Scott, M., Semenov, A., Avrahami, D., Laszlo, L., Prusiner, S. B., and Avraham, D. (1995) J. Cell Biol. 129, 121-132
43. Vlodavsky, I., Fuks, Z., Bar-Ner, M., Ariav, Y., and Schirrmacher, V. (1983) Cancer Res. 43, 2704-2711
44. Brown, D. A., and Rose, J. K. (1992) Cell 68, 533-544
45. Yanai, A., Meiner, Z., Gahali, I., Gabizon, R., and Taraboulos, A. (1999) FEBS Lett. 460, 11-16
46. Safar, J., Wille, H., Itri, V., Groth, D., Serban, H., Torchia, M., Cohen, F. E., and Prusiner, S. B. (1998) Nat. Med. 4, 1157-1165
47. Rapraeger, A. C., Krufka, A., and Olwin, B. B. (1991) Science 252, 1705-1708
48. Yayon, A., Klagsbrun, M., Esko, J. D., Leder, P., and Ornitz, D. M. (1991) Cell 64, 841-848
49. Ornitz, D. M., Yayon, A., Flanagan, J. G., Svahn, C. M., Levi, E., and Leder, P. (1992) Mol. Cell. Biol. 12, 240-247
50. Vey, M., Pilkuhn, S., Wille, H., Nixon, R., DeArmond, S. J., Smart, E. J., Anderson, R. G., Taraboulos, A., and Prusiner, S. B. (1996) Proc. Natl. Acad. Sci. U. S. A. 93, 14945-14949
51. Harder, T., Scheiffele, P., Verkade, P., and Simons, K. (1998) J. Cell Biol. 141, 929-942
52. Mayor, S., Rothberg, K. G., and Maxfield, F. R. (1994) Science 264, 1948-1951
53. McKinley, M. P., Taraboulos, A., Kenaga, L., Serban, D., Stieber, A., DeArmond, S. J., Prusiner, S. B., and Gonatas, N. (1991) Lab. Invest. 65, 622-630
54. Baeuerle, P. A., and Huttner, W. B. (1986) Biochem. Biophys. Res. Commun. 141, 870-877
55. Keller, K. M., Brauer, P. R., and Keller, J. M. (1989) Biochemistry 28, 8100-8107
56. Prusiner, S. B., Scott, M., Foster, D., Pan, K. M., Groth, D., Mirenda, C., Torchia, M., Yang, S. L., Serban, D., Carlson, G. A., Hoppe, P. C., Westaway, D., and DeArmond, S. J. (1990) Cell 63, 673-686
57. Turnbull, J. E., Fernig, D. G., Ke, Y., Wilkinson, M. C., and Gallagher, J. T. (1992) J. Biol. Chem. 267, 10337-10341
58. Maccarana, M., Casu, B., and Lindahl, U. (1993) J. Biol. Chem. 268, 23898-23905
59. Ishai-Michaeli, R., Svahn, C. M., Weber, M., Chajek-Shaul, T., Korner, G., Ekre, H. P., and Vlodavsky, I. (1992) Biochemistry 31, 2080-2088
60. Aviezer, D., Levy, E., Safran, M., Svahn, C., Buddecke, E., Schmidt, A., David, G., Vlodavsky, I., and Yayon, A. (1994) J. Biol. Chem. 269, 114-121
61. Rogers, M., Yehiely, F., Scott, M., and Prusiner, S. B. (1993) Proc. Natl. Acad. Sci. U. S. A. 90, 3182-3186
62. Flechsig, E., Shmerling, D., Hegyi, I., Raeber, A. J., Fischer, M., Cozzio, A., von Mering, C., Aguzzi, A., and Weissmann, C. (2000) Neuron 27, 399-408
63. Cohen, F. E., Pan, K. M., Huang, Z., Baldwin, M., Fletterick, R. J., and Prusiner, S. B. (1994) Science 264, 530-531
64. Gupta-Bansal, R., Frederickson, R. C., and Brunden, K. R. (1995) J. Biol. Chem. 270, 18666-18671
65. Snow, A. D., Sekiguchi, R., Nochlin, D., Fraser, P., Kimata, K., Mizutani, A., Arai, M., Schreier, W. A., and Morgan, D. G. (1994) Neuron 12, 219-234
66. Kisilevsky, R., Lemieux, L. J., Fraser, P. E., Kong, X., Hultin, P. G., and Szarek, W. A. (1995) Nat. Med. 1, 143-148
67. Cohlberg, J. A., Li, J., Uversky, V. N., and Fink, A. L. (2002) Biochemistry 41, 1502-1511
68. Nader, H. B., Porcionatto, M. A., Tersariol, I. L., Pinhal, M. A., Oliveira, F. W., Moraes, C. T., and Dietrich, C. P. (1990) J. Biol. Chem. 265, 16807-16813
69. Yamada, S., Okada, Y., Ueno, M., Iwata, S., Deepa, S. S., Nishimura, S., Fujita, M., Van Die, I., Hirabayashi, Y., and Sugahara, K. (2002) J. Biol. Chem. 277, 31877-31886
70. Filmus, J., and Selleck, S. B. (2001) J. Clin. Invest. 108, 497-501
71. Bernfield, M., Gotte, M., Park, P. W., Reizes, O., Fitzgerald, M. L., Lincerum, J., and Zako, M. (1999) Annu. Rev. Biochem. 68, 729-777
72. Iozzo, R. V. (1998) Annu. Rev. Biochem. 67, 609-652
73. Tkachenko, E., and Simons, M. (2002) J. Biol. Chem. 277, 19946-19951
74. Turnbull, J., Powell, A., and Guimond, S. (2001) Trends Cell Biol. 11, 75-82