Heparan sulfate regulates VEGF165- and VEGF121- mediated vascular hyperpermeability

Journal of Biological Chemistry

Volumn 286, Issue 1, 2011, Pages 737-745

  Xu, Ding ^a   Fuster, Mark M ^b,c   Lawrence, Roger ^a   Esko, Jeffrey D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENESIS; DIRECT INTERACTIONS; HEPARAN SULFATES; IN-SITU; IN-VITRO; IN-VIVO; PHARMACOLOGICAL BLOCKADE; PROTEIN INTERACTION; RECEPTOR COMPLEX; VASCULAR PERMEABILITY; VEGFR-2;

BIOCHEMISTRY; COMPLEXATION; PHOSPHORYLATION; SELF ASSEMBLY;

ENDOTHELIAL CELLS;

HEPARAN SULFATE; VASCULOTROPIN 121; VASCULOTROPIN 165;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BIOSYNTHESIS; BLOOD VESSEL PERMEABILITY; CELL LOSS; CONTROLLED STUDY; DEACETYLATION; ENDOTHELIUM CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; SULFATION;

ANIMALS; BLOOD VESSELS; ENDOTHELIAL CELLS; HEPARITIN SULFATE; HUMANS; MICE; NEOPLASMS; PERMEABILITY; PHOSPHORYLATION; SKIN; SULFOTRANSFERASES; UREA; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 78650939979     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M110.177006     Document Type: Article

References (60)

1. Mehta, D., and Malik, A. B. (2006) Physiol. Rev. 86, 279-367
2. Marti, H. J., Bernaudin, M., Bellail, A., Schoch, H., Euler, M., Petit, E., and Risau, W. (2000) Am. J. Pathol. 156, 965-976
3. Olsson, A. K., Dimberg, A., Kreuger, J., and Claesson-Welsh, L. (2006) Nat. Rev. Mol. Cell Biol. 7, 359-371
4. Paul, R., Zhang, Z. G., Eliceiri, B. P., Jiang, Q., Boccia, A. D., Zhang, R. L., Chopp, M., and Cheresh, D. A. (2001) Nat. Med. 7, 222-227
5. Weis, S., Shintani, S., Weber, A., Kirchmair, R., Wood, M., Cravens, A., McSharry, H., Iwakura, A., Yoon, Y. S., Himes, N., Burstein, D., Doukas, J., Soll, R., Losordo, D., and Cheresh, D. (2004) J. Clin. Invest. 113, 885-894
6. Senger, D. R., Van de Water, L., Brown, L. F., Nagy, J. A., Yeo, K. T., Yeo, T. K., Berse, B., Jackman, R. W., Dvorak, A. M., and Dvorak, H. F. (1993) Cancer Metastasis Rev. 12, 303-324
7. Tong, R. T., Boucher, Y., Kozin, S. V., Winkler, F., Hicklin, D. J., and Jain, R. K. (2004) Cancer Res. 64, 3731-3736
8. Weis, S. M., and Cheresh, D. A. (2005) Nature 437, 497-504
9. Willett, C. G., Boucher, Y., di Tomaso, E., Duda, D. G., Munn, L. L., Tong, R. T., Chung, D. C., Sahani, D. V., Kalva, S. P., Kozin, S. V., Mino, M., Cohen, K. S., Scadden, D. T., Hartford, A. C., Fischman, A. J., Clark, J. W., Ryan, D. P., Zhu, A. X., Blaszkowsky, L. S., Chen, H. X., Shellito, P. C., Lauwers, G. Y., and Jain, R. K. (2004) Nat. Med. 10, 145-147
10. Criscuoli, M. L., Nguyen, M., and Eliceiri, B. P. (2005) Blood 105, 1508-1514
11. Weis, S., Cui, J., Barnes, L., and Cheresh, D. (2004) J. Cell Biol. 167, 223-229
12. Carmeliet, P., Ng, Y. S., Nuyens, D., Theilmeier, G., Brusselmans, K., Cornelissen, I., Ehler, E., Kakkar, V. V., Stalmans, I., Mattot, V., Perriard, J. C., Dewerchin, M., Flameng, W., Nagy, A., Lupu, F., Moons, L., Collen, D., D'Amore, P. A., and Shima, D. T. (1999) Nat. Med. 5, 495-502
13. Ruhrberg, C. (2003) Bioessays 25, 1052-1060
14. Tessler, S., Rockwell, P., Hicklin, D., Cohen, T., Levi, B. Z., Witte, L., Lemischka, I. R., and Neufeld, G. (1994) J. Biol. Chem. 269, 12456-12461
15. Kendall, R. L., and Thomas, K. A. (1993) Proc. Natl. Acad. Sci. U.S.A. 90, 10705-10709
16. Vander Kooi, C. W., Jusino, M. A., Perman, B., Neau, D. B., Bellamy, H. D., and Leahy, D. J. (2007) Proc. Natl. Acad. Sci. U.S.A. 104, 6152-6157
17. Mamluk, R., Gechtman, Z., Kutcher, M. E., Gasiunas, N., Gallagher, J., and Klagsbrun, M. (2002) J. Biol. Chem. 277, 24818-24825
18. Pellegrini, L., Burke, D. F., von Delft, F., Mulloy, B., and Blundell, T. L. (2000) Nature 407, 1029-1034
19. Schlessinger, J., Plotnikov, A. N., Ibrahimi, O. A., Eliseenkova, A. V., Yeh, B. K., Yayon, A., Linhardt, R. J., and Mohammadi, M. (2000) Mol. Cell 6, 743-750
20. Dementiev, A., Petitou, M., Herbert, J. M., and Gettins, P. G. (2004) Nat. Struct. Mol. Biol. 11, 863-867
21. Li, W., Johnson, D. J., Esmon, C. T., and Huntington, J. A. (2004) Nat. Struct. Mol. Biol. 11, 857-862
22. Ashikari-Hada, S., Habuchi, H., Kariya, Y., and Kimata, K. (2005) J. Biol. Chem. 280, 31508-31515
23. Fuster, M. M., Wang, L., Castagnola, J., Sikora, L., Reddi, K., Lee, P. H., Radek, K. A., Schuksz, M., Bishop, J. R., Gallo, R. L., Sriramarao, P., and Esko, J. D. (2007) J. Cell Biol. 177, 539-549
24. Jakobsson, L., Kreuger, J., Holmborn, K., Lundin, L., Eriksson, I., Kjellén, L., and Claesson-Welsh, L. (2006) Dev. Cell 10, 625-634
25. Goerges, A. L., and Nugent, M. A. (2003) J. Biol. Chem. 278, 19518-19525
26. Cohen, T., Gitay-Goren, H., Sharon, R., Shibuya, M., Halaban, R., Levi, B. Z., and Neufeld, G. (1995) J. Biol. Chem. 270, 11322-11326
27. Gitay-Goren, H., Cohen, T., Tessler, S., Soker, S., Gengrinovitch, S., Rockwell, P., Klagsbrun, M., Levi, B. Z., and Neufeld, G. (1996) J. Biol. Chem. 271, 5519-5523
28. Schuksz, M., Fuster, M. M., Brown, J. R., Crawford, B. E., Ditto, D. P., Lawrence, R., Glass, C. A., Wang, L., Tor, Y., and Esko, J. D. (2008) Proc. Natl. Acad. Sci. U.S.A. 105, 13075-13080
29. Wang, L., Fuster, M., Sriramarao, P., and Esko, J. D. (2005) Nat. Immunol. 6, 902-910
30. Inatani, M., Irie, F., Plump, A. S., Tessier-Lavigne, M., and Yamaguchi, Y. (2003) Science 302, 1044-1046
31. Constien, R., Forde, A., Liliensiek, B., Gröne, H. J., Nawroth, P., Hämmerling, G., and Arnold, B. (2001) Genesis 30, 36-44
32. Miles, A. A., and Miles, E. M. (1952) J. Physiol. 118, 228-257
33. Perrière, N., Demeuse, P., Garcia, E., Regina, A., Debray, M., Andreux, J. P., Couvreur, P., Scherrmann, J. M., Temsamani, J., Couraud, P. O., Deli, M. A., and Roux, F. (2005) J. Neurochem. 93, 279-289
34. Lawrence, R., Olson, S. K., Steele, R. E., Wang, L., Warrior, R., Cummings, R. D., and Esko, J. D. (2008) J. Biol. Chem. 283, 33674-33684
35. Holmborn, K., Ledin, J., Smeds, E., Eriksson, I., Kusche-Gullberg, M., and Kjellén, L. (2004) J. Biol. Chem. 279, 42355-42358
36. Lin, X., Wei, G., Shi, Z., Dryer, L., Esko, J. D., Wells, D. E., and Matzuk, M. M. (2000) Dev. Biol. 224, 299-311
37. Pan, Q., Chathery, Y., Wu, Y., Rathore, N., Tong, R. K., Peale, F., Bagri, A., Tessier-Lavigne, M., Koch, A. W., and Watts, R. J. (2007) J. Biol. Chem. 282, 24049-24056
38. Gille, H., Kowalski, J., Li, B., LeCouter, J., Moffat, B., Zioncheck, T. F., Pelletier, N., and Ferrara, N. (2001) J. Biol. Chem. 276, 3222-3230
39. Scheppke, L., Aguilar, E., Gariano, R. F., Jacobson, R., Hood, J., Doukas, J., Cao, J., Noronha, G., Yee, S., Weis, S., Martin, M. B., Soll, R., Cheresh, D. A., and Friedlander, M. (2008) J. Clin. Invest. 118, 2337-2346
40. Fischer, S., Clauss, M., Wiesnet, M., Renz, D., Schaper, W., and Karliczek, G. F. (1999) Am. J. Physiol. 276, C812-C820
41. Fukumura, D., Gohongi, T., Kadambi, A., Izumi, Y., Ang, J., Yun, C. O., Buerk, D. G., Huang, P. L., and Jain, R. K. (2001) Proc. Natl. Acad. Sci. U.S.A. 98, 2604-2609
42. Fulton, D., Gratton, J. P., McCabe, T. J., Fontana, J., Fujio, Y., Walsh, K., Franke, T. F., Papapetropoulos, A., and Sessa, W. C. (1999) Nature 399, 597-601
43. Park, K. W. (2004) Int. Anesthesiol. Clin. 42, 135-145
44. Söderberg, O., Gullberg, M., Jarvius, M., Ridderstråle, K., Leuchowius, K. J., Jarvius, J., Wester, K., Hydbring, P., Bahram, F., Larsson, L. G., and Landegren, U. (2006) Nat. Methods 3, 995-1000
45. Gitay-Goren, H., Soker, S., Vlodavsky, I., and Neufeld, G. (1992) J. Biol. Chem. 267, 6093-6098
46. Holmes, K., Roberts, O. L., Thomas, A. M., and Cross, M. J. (2007) Cell Signal 19, 2003-2012
47. Chiang, M. K., and Flanagan, J. G. (1995) Growth Factors 12, 1-10
48. Dougher, A. M., Wasserstrom, H., Torley, L., Shridaran, L., Westdock, P., Hileman, R. E., Fromm, J. R., Anderberg, R., Lyman, S., Linhardt, R. J., Kaplan, J., and Terman, B. I. (1997) Growth Factors 14, 257-268
49. Robinson, C. J., and Stringer, S. E. (2001) J. Cell Sci. 114, 853-865
50. Robinson, C. J., Mulloy, B., Gallagher, J. T., and Stringer, S. E. (2006) J. Biol. Chem. 281, 1731-1740
51. Park, M., and Lee, S. T. (1999) Biochem. Biophys. Res. Commun. 264, 730-734
52. Bernfield, M., Götte, M., Park, P. W., Reizes, O., Fitzgerald, M. L., Lincecum, J., and Zako, M. (1999) Annu. Rev. Biochem. 68, 729-777
53. Gengrinovitch, S., Berman, B., David, G., Witte, L., Neufeld, G., and Ron, D. (1999) J. Biol. Chem. 274, 10816-10822
54. Qiao, D., Meyer, K., Mundhenke, C., Drew, S. A., and Friedl, A. (2003) J. Biol. Chem. 278, 16045-16053
55. Stanford, K. I., Wang, L., Castagnola, J., Song, D., Bishop, J. R., Brown, J. R., Lawrence, R., Bai, X., Habuchi, H., Tanaka, M., Cardoso, W. V., Kimata, K., and Esko, J. D. (2010) J. Biol. Chem. 285, 286-294
56. Izvolsky, K. I., Lu, J., Martin, G., Albrecht, K. H., and Cardoso, W. V. (2008) Genesis 46, 8-18
57. Bishop, J. R., Schuksz, M., and Esko, J. D. (2007) Nature 446, 1030-1037
58. van Bruggen, N., Thibodeaux, H., Palmer, J. T., Lee, W. P., Fu, L., Cairns, B., Tumas, D., Gerlai, R., Williams, S. P., van Lookeren Campagne, M., and Ferrara, N. (1999) J. Clin. Invest. 104, 1613-1620
59. Kleinig, T. J., and Vink, R. (2009) Curr. Opin. Neurol. 22, 294-301
60. Wang, Q., Tang, X. N., and Yenari, M. A. (2007) J. Neuroimmunol. 184, 53-68