Internalization of HIV-1 Tat Requires Cell Surface Heparan Sulfate Proteoglycans

Journal of Biological Chemistry

Volumn 276, Issue 5, 2001, Pages 3254-3261

  Tyagi, Mudit ^a   Rusnati, Marco ^b   Presta, Marco ^b   Giacca, Mauro ^a,c  

^a INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

^b UNIVERSITY OF BRESCIA   (Italy)

^c SCUOLA NORMALE SUPERIORE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL CULTURE; BIOASSAY; BIOCHEMISTRY; BIOSYNTHESIS; CELL MEMBRANES; CYTOLOGY; DEGRADATION; FLUORESCENCE; PHYSIOLOGY; VIRUSES;

FLOW CYTOMETRY;

PROTEINS;

CHLORAMPHENICOL ACETYLTRANSFERASE; GLUTATHIONE TRANSFERASE; GLYCOSAMINOGLYCAN; GREEN FLUORESCENT PROTEIN; PROTEOHEPARAN SULFATE; RECOMBINANT PROTEIN; TRANSACTIVATOR PROTEIN;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; CELL MUTANT; CHO CELL; CHO K1 CELL; FLOW CYTOMETRY; HELA CELL; HL3T1 CELL; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOCYTOCHEMISTRY; INTERNALIZATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; TRANSACTIVATION; ANIMAL; ENDOCYTOSIS; HAMSTER; KINETICS; METABOLISM; PHYSIOLOGY;

ANIMALIA; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; MAMMALIA; RNA VIRUSES;

ANIMALS; CHO CELLS; CRICETINAE; ENDOCYTOSIS; GENE PRODUCTS, TAT; HELA CELLS; HEPARAN SULFATE PROTEOGLYCANS; HUMANS; KINETICS; TRANS-ACTIVATION (GENETICS);

EID: 0035793619     PISSN: 00219258     EISSN: None     Source Type: Journal    
DOI: 10.1074/jbc.M006701200     Document Type: Article

References (72)

1. Berkhout, B., Silverman, R. H., and Jeang, K. T. (1989) Cell 59, 273-282
2. Benkirane, M., Chun, R. F., Xiao, H., Ogryzko, V. V., Howard, B. H., Nakatani, Y., and Jeang, K. T. (1998) J. Biol. Chem. 273, 24898-24905
3. Marzio, G., Tyagi, M., Gutierrez, M. I., and Giacca, M. (1998) Proc. Natl. Acad. Sci. U. S. A. 23, 13519-13524
4. Hottiger, M. O., and Nabel, G. J. (1998) J. Virol. 72, 8252-8256
5. Wei, P., Garber, M. E., Fang, S.-M., Fisher, W. H., and Jones, K. A. (1998) Cell 92, 451-462
6. Parada, C. A., and Roeder, R. G. (1996) Nature 384, 375-378
7. Gold, M. O., Yang, X., Herrmann, C. H., and Rice, A. P. (1998) J. Virol. 72, 4448-4453
8. Cujec, T. P., Okamoto, H., Fujinaga, K., Meyer, J., Chamberlin, H., Morgan, D. O., and Peterlin, B. M. (1997) Genes Dev. 11, 2645-2657
9. Zhu, Y., Pe'ery, T., Peng, J., Ramanathan, Y., Marshall, N., Marshall, T., Amendt, B., Mathews, M. B., and Price, D. H. (1997) Genes Dev. 11, 2622-2632
10. Lotz, M., Clark-Lewis, I., and Ganu, V. (1994) J. Cell Biol. 124, 365-371
11. Zauli, G., Davis, B. R., Re, M. C., Visani, G., Furlini, G., and La Placa, M. (1992) Blood 80, 3036-3043
12. Westendorp, M. O., Li-Weber, M., Frank, R. W., and Krammer, P. H. (1994) J. Virol. 68, 4177-4185
13. Scala, G., Ruocco, M. R., Ambrosino, C., Mallardo, M., Giordano, V., Baldassarre, F., Dragonetti, E., Quinto, I., and Venuta, S. (1994) J. Exp. Med. 179, 961-971
14. Opalenik, S. R., Shin, J. T., Wehby, J. N., Mahesh, V. K., and Thompson, J. A. (1995) J. Biol. Chem. 270, 17457-17467
15. Nabell, L. M., Raja, R. H., Sayeski, P. P., Paterson, A. and Kudlow, J. E. (1994) Cell Growth Differ. 5, 87-93
16. Puri, R. K., and Aggarwal, B. B. (1992) Cancer Res. 52, 3787-3790
17. Purvis, S. F., Georges, D. L., Williams, T. M., and Lederman, M. M. (1992) Cell. Immunol. 144,32-42
18. Pocsik, E., Higuchi, M., and Aggarwal, B. B. (1992) Lymphokine Cytokine Res. 11, 317-325
19. Ensoli, B., Buonaguro, L., Barillari, G., Fiorelli, V., Gendelman, R., Morgan, R. A., Wingfield, P., and Gallo, R. C. (1993) J. Virol. 67, 277-287
20. Zauli, G., Gibellini, D., Milani, D., Mazzoni, M., Borgatti, P., La Placa, M., and Capitani, S. (1993) Cancer Res. 53, 4481-4485
21. Ensoli, B., Barillari, G., Salahuddin, S. Z., Gallo, R. C., and Wong-Staal, F. (1990) Nature 345, 84-87
22. Lafrenie, R. M., Wahl, L. M., Epstein, J. S., Yamada, K. M., and Dhawan, S. (1997) J. Immunol. 159, 4077-4083
23. Westendorp, M. O., Frank, R., Ochsenbauer, C., Stricker, K., Dhein, J., Walczak, H., Debatin, K. M., and Krammer, P. H. (1995) Nature 375, 497-500
24. Li, C. J., Friedman, D. J., Wang, C., Metelev, V., and Pardee, A. B. (1995) Science 268, 429-431
25. Albini, A., Benelli, R., Presta, M., Rusnati, M., Ziche, M., Rubartelli, A., Paglialunga, G., F, B., and Noonan, D. (1996) Oncogene 12, 289-297
26. Albini, A., Barillari, G., Benelli, R., Gallo, R. C., and Ensoli, B. (1995) Proc. Natl. Acad. Sci. U. S. A. 92, 4838-4842
27. Corallini, A., Campioni, D., Rossi, C., Albini, A., Possati, L., Rusnati, M., Gazzanelli, G., Benelli, R., Masiello, L., Sparacciari, V., Presta, M., Mannello, F., Fontanini, G., and Barbanti-Brodano, G. (1996) AIDS 10, 701-710
28. Subramanyam, M., Gutheil, W. G., Bachovchin, W. W., and Huber, B. T. (1993) J. Immunol. 150, 2544-2553
29. Chirmule, N., Than, S., Khan, S. A., and Pahwa, S. (1995) J. Virol. 69, 492-498
30. Viscidi, R. P., Mayur, K., Lederman, H. M., and Frankel, A. D. (1989) Science 246, 1606-1608
31. Sabatier, J. M., Vives, E., Mabrouk, K., Benjouad, A., Rochat, H., Duval, A., Hue, B., and Bahraoui, E. (1991) J. Virol. 65, 961-967
32. Taylor, J. P., Cupp, C., Diaz, A., Chowdhury, M., Khalili, K., Jimenez, S. A., and Amini, S. (1992) Proc. Natl. Acad. Sci. U. S. A. 89, 9617-9621
33. Philippon, V., Vellutini, C., Gambarelli, D., Harkiss, G., Arbuthnott, G., Metzger, D., Roubin, R., and Filippi, P. (1994) Virology 205, 519-529
34. Weeks, B. S., Lieberman, D. M., Johnson, B., Roque, E., Green, M., Loewenstein, P., Oldfield, E. H., and Kleinman, H. K. (1995) J. Neurosci. Res. 42, 34-40
35. Hofman, F. M., Dohadwala, M. M., Wright, A. D., Hinton, D. R., and Walker, S. M. (1994) J. Neuroimmunol. 54, 19-28
36. Nath, A., Psooy, K., Martin, C., Knudsen, B., Magnuson, D. S., Haughey, N., and Geiger, J. D. (1996) J. Virol. 70, 1475-1480
37. Helland, D. E., Welles, J. L., Caputo, A., and Haseltine, W. A. (1991) J. Virol. 65, 4547-4549
38. Thomas, C. A., Dobkin, J., and Weinberger, O. K. (1994) J. Immunol. 153, 3831-3839
39. Chang, H. C., Samaniego, F., Nair, B. C., Buonaguro, L., and Ensoli, B. (1997) AIDS 11, 1421-1431
40. Re, M. C., Furlini, G., Vignoli, M., Ramazzotti, E., Roderigo, G., De Rosa, V., Zauli, G., Lolli, S., Capitani, S., and La Placa, M. (1995) J. Acquired Immune Deficiency Syndrome 10, 408-416
41. Albini, A., Soldi, R., Giunciuglio, D., Giraudo, E., Benelli, R., Primo, L., Noonan, D., Salio, M., Camussi, G., Rockl, W., and Bussolino, F. (1996) Nat. Med. 2, 1371-1375
42. Albini, A., Ferrini, S., Benelli, R., Sforzini, S., Giunciuglio, D., Aluigi, M. G., Proudfoot, A. E. I., Alouani, S., Wells, T. N. C., Mariani, G., Rabin, R. L., Farber, J. M., and Noonan, D. M. (1998) Proc. Natl. Acad. Sci. U. S. A. 95, 13153-13158
43. Mitola, S., Sozzani, S., Luini, W., Primo, L., Borsatti, A., Weich, H., and Bussolino, F. (1997) Blood 90, 1365-1372
44. Green, M., and Loewenstein, P. M. (1988) Cell 55, 1179-1188
45. Frankel, A. D., and Pabo, C. O. (1988) Cell 55, 1189-1193
46. Mann, D. A., and Frankel, A. D. (1991) EMBO J. 10, 1733-1739
47. Demarchi, F., Gutierrez, M. I., and Giacca, M. (1999) J. Virol. 73, 7080-7086
48. Demarchi, F., d'Adda di Fagagna, F., Falaschi, A., and Giacca, M. (1996) J. Virol. 70, 4427-4437
49. Biswas, D. K., Salas, T. R., Wang, F., Ahlers, C. M., Dezube, B. J., and Pardee, A. B. (1995) J. Virol. 69, 7437-7444
50. Westendorp, M. O., Shatrov, V. A., Schulze-Osthoff, K., Frank, R., Kraft, M., Los, M., Krammer, P. H., Droge, W., and Lehmann, V. (1995) EMBO J. 14, 546-554
51. Fawell, S., Seery, J., Daikh, Y., Moore, C., Chen, L. L., Pepinsky, B., and Barsoum, J. (1994) Proc. Natl. Acad. Sci. U. S. A. 91, 664-668
52. Nagahara, H., Vocero-Akbani, A. M., Snyder, E. L., Ho, A., Latham, D. G., Lissy, N. A., Becker-Hapak, M., Ezhevsky, S. A., and Dowdy, S. F. (1998) Nat. Med. 4, 1449-1452
53. Schwarze, S. R., Ho, A., Vocero-Akbani, A., and Dowdy, S. F. (1999) Science 285, 1569-1572
54. Rusnati, M., Coltrini, D., Oreste, P., Zoppetti, G., Albini, A., Noonan, D., d'Adda di Fagagna, F., Giacca, M., and Presta, M. (1997) J. Biol. Chem. 272, 11313-11320
55. Rusnati, M., Tulipano, G., Urbinati, C., Tanghetti, E., Giuliani, R., Giacca, M., Ciomei, M., Corallini, A., and Presta, M. (1998) J. Biol. Chem. 273, 16027-16037
56. Rusnati, M., Tulipano, G., Spillmann, D., Tanghetti, E., Oreste, P., Zoppetti, G., Giacca, M., and Presta, M. (1999) J. Biol. Chem. 274, 28198-28205
57. Rostand, K. S., and Esko, J. D. (1997) Infect. Immun. 65, 1-8
58. Esko, J. D., Elgavish, A., Prasthofer, T., Taylor, W. H., and Weinke, J. L. (1986) J. Biol. Chem. 261, 15725-15333
59. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd Ed., Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
60. Summerford, C., and Samulski, R. J. (1998) J. Virol. 72, 1438-1445
61. Ruoslahti, E. (1989) J. Biol. Chem. 264, 13369-13372
62. Esko, J. D. (1991) Curr. Opin. Cell Biol. 3, 805-816
63. Yanagishita, M., and Hascall, V. C. (1992) J. Biol. Chem. 267, 9451-9454
64. Linhardt, R. J. (1994) in Current Protocols in Molecular Biology (Janssen, K., ed) Vol. 3, pp. 17.13.17-17.13.32, John Wiley & Sons, Inc., New York, NY
65. Esko, J. D., Weinke, J. L., Taylor, W. H., Ekborg, G., Roden, L., Anantharamaiah, G., and Gawish, A. (1987) J. Biol. Chem. 262, 12189-12195
66. Esko, J. D., Stewart, T. E., and Taylor, W. H. (1985) Proc. Natl. Acad. Sci. U. S. A. 82, 3197-3201
67. Vives, E., Brodin, P., and Lebleu, B. (1997) J. Biol. Chem. 272, 16010-16017
68. Maccarana, M., Casu, B., and Lindahl, U. (1993) J. Biol. Chem. 268, 23898-23905
69. Spillmann, D., Witt, D., and Lindahl, U. (1998) J. Biol. Chem. 273, 15487-15493
70. Lyon, M., and Gallagher, J. T. (1994) Biochem. Soc. Trans. 22, 365-370
71. Lappi, D. A., Ying, W., Barthelemy, I., Martineau, D., Prieto, I., Benatti, L., Soria, M., and Baird, A. (1994) J. Biol. Chem. 269, 12552-12558
72. Sosnowski, B. A., Gonzalez, A. M., Chandler, L. A., Buechler, Y. J., Pierce, G. F., and Baird, A. (1996) J. Biol. Chem. 271, 33647-33653