Endorepellin, the angiostatic module of perlecan, interacts with both the α2β1 integrin and vascular endothelial growth factor receptor 2 (VEGFR2): A dual receptor antagonism

Journal of Biological Chemistry

Volumn 286, Issue 29, 2011, Pages 25947-25962

  Goyal, Atul ^a   Pal, Nutan ^a   Concannon, Matthew ^a   Paul, Matthew ^a   Doran, Mike ^a   Poluzzi, Chiara ^a   Sekiguchi, Kiyotoshi ^b   Whitelock, John M ^c   Neill, Thomas ^a   Iozzo, Renato V ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b OSAKA UNIVERSITY   (Japan)

^c UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN CYTOSKELETON; ANGIOGENESIS; ANGIOSTATIC ACTIVITIES; ANTIANGIOGENIC; C-TERMINAL DOMAINS; DOWN-REGULATION; ENDOREPELLIN; HIGH AFFINITY; INTEGRINS; PERLECAN; SIGNALING CASCADES; TYROSINE PHOSPHATASE; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR; VEGFR-2;

AMINO ACIDS; PROTEINS;

ENDOTHELIAL CELLS;

ENDOREPELLIN; FIBROBLAST GROWTH FACTOR 2; PERLECAN; PLACENTAL GROWTH FACTOR; PROTEIN TYROSINE PHOSPHATASE SHP 1; RECOMBINANT PLACENTAL GROWTH FACTOR; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2; VERY LATE ACTIVATION ANTIGEN 2;

ANIMAL CELL; ANTIANGIOGENIC ACTIVITY; ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIUM CELL; ENZYME ACTIVATION; HUMAN; HUMAN CELL; INTERNALIZATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RECEPTOR BLOCKING; TRANSCRIPTION REGULATION;

ANGIOSTATIC PROTEINS; ANIMALS; CELL LINE; DOWN-REGULATION; ENDOTHELIAL CELLS; HEPARAN SULFATE PROTEOGLYCANS; HUMANS; INTEGRIN ALPHA2BETA1; PEPTIDE FRAGMENTS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 6; RATS; TRANSCRIPTION, GENETIC; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

SUS;

EID: 79960400832     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.243626     Document Type: Article

References (111)

1. Olsson, A. K., Dimberg, A., Kreuger, J., and Claesson-Welsh, L. (2006) Nat. Rev. Mol. Cell Biol. 7, 359-371
2. Senger, D. R. (2010) Mol. Biol. Cell 21, 377-379
3. Iozzo, R. V. (2005) Nat. Rev. Mol. Cell Biol. 6, 646-656
4. Ferrara, N., Gerber, H. P., and LeCouter, J. (2003) Nat. Med. 9, 669-676
5. Byzova, T. V., Goldman, C. K., Pampori, N., Thomas, K. A., Bett, A., Shattil, S. J., and Plow, E. F. (2000) Mol. Cell 6, 851-860
6. Humphries, M. J., Travis, M. A., Clark, K., and Mould, A. P. (2004) Biochem. Soc. Trans. 32, 822-825
7. Soldi, R., Mitola, S., Strasly, M., Defilippi, P., Tarone, G., and Bussolino, F. (1999) EMBO J. 18, 882-892
8. Borges, E., Jan, Y., and Ruoslahti, E. (2000) J. Biol. Chem. 275, 39867-39873
9. De, S., Razorenova, O., McCabe, N. P., O'Toole, T., Qin, J., and Byzova, T. V. (2005) Proc. Natl. Acad. Sci. U.S.A. 102, 7589-7594
10. Mahabeleshwar, G. H., Chen, J., Feng, W., Somanath, P. R., Razorenova, O. V., and Byzova, T. V. (2008) Cell Cycle 7, 335-347
11. Mahabeleshwar, G. H., Feng, W., Phillips, D. R., and Byzova, T. V. (2006) J. Exp. Med. 203, 2495-2507
12. Somanath, P. R., Malinin, N. L., and Byzova, T. V. (2009) Angiogenesis 12, 177-185
13. Senger, D. R., Claffey, K. P., Benes, J. E., Perruzzi, C. A., Sergiou, A. P., and Detmar, M. (1997) Proc. Natl. Acad. Sci. U.S.A. 94, 13612-13617
14. Senger, D. R., Perruzzi, C. A., Streit, M., Koteliansky, V. E., de Fougerolles, A. R., and Detmar, M. (2002) Am. J. Pathol. 160, 195-204
15. Sweeney, S. M., DiLullo, G., Slater, S. J., Martinez, J., Iozzo, R. V., Lauer-Fields, J. L., Fields, G. B., and San Antonio, J. D. (2003) J. Biol. Chem. 278, 30516-30524
16. Davis, G. E., and Senger, D. R. (2008) Curr. Opin. Hematol. 15, 197-203
17. Vlahakis, N. E., Young, B. A., Atakilit, A., Hawkridge, A. E., Issaka, R. B., Boudreau, N., and Sheppard, D. (2007) J. Biol. Chem. 282, 15187-15196
18. Oommen, S., Gupta, S. K., and Vlahakis, N. E. (2011) J. Biol. Chem. 286, 1083-1092
19. Mattila, E., Auvinen, K., Salmi, M., and Ivaska, J. (2008) J. Cell Sci. 121, 3570-3580
20. Borza, C. M., Chen, X., Mathew, S., Mont, S., Sanders, C. R., Zent, R., and Pozzi, A. (2010) J. Biol. Chem. 285, 40114-40124
21. Jinnin, M., Medici, D., Park, L., Limaye, N., Liu, Y., Boscolo, E., Bischoff, J., Vikkula, M., Boye, E., and Olsen, B. R. (2008) Nature Med. 14, 1236-1246
22. Chen, T. T., Luque, A., Lee, S., Anderson, S. M., Segura, T., and Iruela-Arispe, M. L. (2010) J. Cell Biol. 188, 595-609
23. Zhang, X., Kazerounian, S., Duquette, M., Perruzzi, C., Nagy, J. A., Dvorak, H. F., Parangi, S., and Lawler, J. (2009) FASEB J. 23, 3368-3376
24. Bishop, J. R., Schuksz, M., and Esko, J. D. (2007) Nature 446, 1030-1037
25. 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
26. Jakobsson, L., Kreuger, J., Holmborn, K., Lundin, L., Eriksson, I., Kjellén, L., and Claesson-Welsh, L. (2006) Dev. Cell 10, 625-634
27. Hayashi, K., Madri, J. A., and Yurchenco, P. D. (1992) J. Cell Biol. 119, 945-959
28. Yurchenco, P. D., Amenta, P. S., and Patton, B. L. (2004) Matrix Biol. 22, 521-538
29. Iozzo, R. V. (1984) J. Cell Biol. 99, 403-417
30. Iozzo, R. V., Cohen, I. R., Grässel, S., and Murdoch, A. D. (1994) Biochem. J. 302, 625-639
31. Iozzo, R. V., and San Antonio, J. D. (2001) J. Clin. Invest. 108, 349-355
32. Whitelock, J. M., Melrose, J., and Iozzo, R. V. (2008) Biochemistry 47, 11174-11183
33. Iozzo, R. V., and Sanderson, R. D. (2011) J. Cell Mol. Med. 15, 1013-1031
34. Cohen, I. R., Grässel, S., Murdoch, A. D., and Iozzo, R. V. (1993) Proc. Natl. Acad. Sci. U.S.A. 90, 10404-10408
35. Dodge, G. R., Kovalszky, I., Hassell, J. R., and Iozzo, R. V. (1990) J. Biol. Chem. 265, 18023-18029
36. Iozzo, R. V., Pillarisetti, J., Sharma, B., Murdoch, A. D., Danielson, K. G., Uitto, J., and Mauviel, A. (1997) J. Biol. Chem. 272, 5219-5228
37. Baker, A. B., Ettenson, D. S., Jonas, M., Nugent, M. A., Iozzo, R. V., and Edelman, E. R. (2008) Circ. Res. 103, 289-297
38. Sharma, B., and Iozzo, R. V. (1998) J. Biol. Chem. 273, 4642-4646
39. Cohen, I. R., Murdoch, A. D., Naso, M. F., Marchetti, D., Berd, D., and Iozzo, R. V. (1994) Cancer Res. 54, 5771-5774
40. Iozzo, R. V., and Cohen, I. (1993) Cell Mol. Life Sci. 49, 447-455
41. Zhou, Z., Wang, J., Cao, R., Morita, H., Soininen, R., Chan, K. M., Liu, B., Cao, Y., and Tryggvason, K. (2004) Cancer Res. 64, 4699-4702
42. Iozzo, R. V. (1998) Annu. Rev. Biochem. 67, 609-652
43. Fuki, I. V., Iozzo, R. V., and Williams, K. J. (2000) J. Biol. Chem. 275, 25742-25750
44. Nugent, M. A., Nugent, H. M., Iozzo, R. V., Sanchack, K., and Edelman, E. R. (2000) Proc. Natl. Acad. Sci. U.S.A. 97, 6722-6727
45. Kinsella, M. G., Tran, P. K., Weiser-Evans, M. C., Reidy, M., Majack, R. A., and Wight, T. N. (2003) Arterioscler. Thromb. Vasc. Biol. 23, 608-614
46. Tran, P. K., Tran-Lundmark, K., Soininen, R., Tryggvason, K., Thyberg, J., and Hedin, U. (2004) Circ. Res. 94, 550-558
47. Tran-Lundmark, K., Tran, P. K., Paulsson-Berne, G., Fridén, V., Soininen, R., Tryggvason, K., Wight, T. N., Kinsella, M. G., Borén, J., and Hedin, U. (2008) Circ. Res. 103, 43-52
48. Whitelock, J. M., and Iozzo, R. V. (2005) Chem. Rev. 105, 2745-2764
49. Whitelock, J. M., Murdoch, A. D., Iozzo, R. V., and Underwood, P. A. (1996) J. Biol. Chem. 271, 10079-10086
50. Xu, D., Fuster, M. M., Lawrence, R., and Esko, J. D. (2011) J. Biol. Chem. 286, 737-745
51. Kaji, T., Yamamoto, C., Oh-i, M., Fujiwara, Y., Yamazaki, Y., Morita, T., Plaas, A. H., and Wight, T. N. (2006) Biochim. Biophys. Acta 1760, 1465-1474
52. Kadenhe-Chiweshe, A., Papa, J., McCrudden, K. W., Frischer, J., Bae, J. O., Huang, J., Fisher, J., Lefkowitch, J. H., Feirt, N., Rudge, J., Holash, J., Yancopoulos, G. D., Kandel, J. J., and Yamashiro, D. J. (2008) Mol. Cancer Res. 6, 1-9
53. Aviezer, D., Iozzo, R. V., Noonan, D. M., and Yayon, A. (1997) Mol. Cell Biol. 17, 1938-1946
54. Sharma, B., Handler, M., Eichstetter, I., Whitelock, J. M., Nugent, M. A., and Iozzo, R. V. (1998) J. Clin. Invest. 102, 1599-1608
55. Savorè, C., Zhang, C., Muir, C., Liu, R., Wyrwa, J., Shu, J., Zhau, H. E., Chung, L. W., Carson, D. D., and Farach-Carson, M. C. (2005) Clin. Exp. Metastasis 22, 377-390
56. Mathiak, M., Yenisey, C., Grant, D. S., Sharma, B., and Iozzo, R. V. (1997) Cancer Res. 57, 2130-2136
57. Mongiat, M., Sweeney, S. M., San Antonio, J. D., Fu, J., and Iozzo, R. V. (2003) J. Biol. Chem. 278, 4238-4249
58. Bix, G., Fu, J., Gonzalez, E. M., Macro, L., Barker, A., Campbell, S., Zutter, M. M., Santoro, S. A., Kim, J. K., Höök, M., Reed, C. C., and Iozzo, R. V. (2004) J. Cell Biol. 166, 97-109
59. Bix, G., Castello, R., Burrows, M., Zoeller, J. J., Weech, M., Iozzo, R. A., Cardi, C., Thakur, M. L., Barker, C. A., Camphausen, K., and Iozzo, R. V. (2006) J. Natl. Cancer Inst. 98, 1634-1646
60. Bix, G., Iozzo, R. A., Woodall, B., Burrows, M., McQuillan, A., Campbell, S., Fields, G. B., and Iozzo, R. V. (2007) Blood 109, 3745-3748
61. Nyström, A., Shaik, Z. P., Gullberg, D., Krieg, T., Eckes, B., Zent, R., Pozzi, A., and Iozzo, R. V. (2009) Blood 114, 4897-4906
62. Zoeller, J. J., McQuillan, A., Whitelock, J., Ho, S. Y., and Iozzo, R. V. (2008) J. Cell Biol. 181, 381-394
63. San Antonio, J. D., Zoeller, J. J., Habursky, K., Turner, K., Pimtong, W., Burrows, M., Choi, S., Basra, S., Bennett, J. S., DeGrado, W. F., and Iozzo, R. V. (2009) Am. J. Pathol. 175, 1338-1347
64. Zoeller, J. J., Whitelock, J. M., and Iozzo, R. V. (2009) Matrix Biol. 28, 284-291
65. Waltenberger, J., Claesson-Welsh, L., Siegbahn, A., Shibuya, M., and Heldin, C. H. (1994) J. Biol. Chem. 269, 26988-26995
66. Ito, N., and Claesson-Welsh, L. (1999) Angiogenesis 3, 159-166
67. Li, S., Shimono, C., Norioka, N., Nakano, I., Okubo, T., Yagi, Y., Hayashi, M., Sato, Y., Fujisaki, H., Hattori, S., Sugiura, N., Kimata, K., and Sekiguchi, K. (2010) J. Biol. Chem. 285, 36645-36655
68. Chuang, C. Y., Lord, M. S., Melrose, J., Rees, M. D., Knox, S. M., Freeman, C., Iozzo, R. V., and Whitelock, J. M. (2010) Biochemistry 49, 5524-5532
69. Murdoch, A. D., Liu, B., Schwarting, R., Tuan, R. S., and Iozzo, R. V. (1994) J. Histochem. Cytochem. 42, 239-249
70. Whitelock, J. M., Graham, L. D., Melrose, J., Murdoch, A. D., Iozzo, R. V., and Underwood, P. A. (1999) Matrix Biol. 18, 163-178
71. Gonzalez, E. M., Mongiat, M., Slater, S. J., Baffa, R., and Iozzo, R. V. (2003) J. Biol. Chem. 278, 38113-38116
72. Buraschi, S., Pal, N., Tyler-Rubinstein, N., Owens, R. T., Neill, T., and Iozzo, R. V. (2010) J. Biol. Chem. 285, 42075-42085
73. Woodall, B. P., Nyström, A., Iozzo, R. A., Eble, J. A., Niland, S., Krieg, T., Eckes, B., Pozzi, A., and Iozzo, R. V. (2008) J. Biol. Chem. 283, 2335-2343
74. Gonzalez, E. M., Reed, C. C., Bix, G., Fu, J., Zhang, Y., Gopalakrishnan, B., Greenspan, D. S., and Iozzo, R. V. (2005) J. Biol. Chem. 280, 7080-7087
75. Mukhopadhyay, D., Knebelmann, B., Cohen, H. T., Ananth, S., and Sukhatme, V. P. (1997) Mol. Cell Biol. 17, 5629-5639
76. Chen, L., Sung, S. S., Yip, M. L., Lawrence, H. R., Ren, Y., Guida, W. C., Sebti, S. M., Lawrence, N. J., and Wu, J. (2006) Mol. Pharmacol. 70, 562-570
77. Yurchenco, P. D., Cheng, Y. S., and Ruben, G. C. (1987) J. Biol. Chem. 262, 17668-17676
78. Ogawa, S., Oku, A., Sawano, A., Yamaguchi, S., Yazaki, Y., and Shibuya, M. (1998) J. Biol. Chem. 273, 31273-32282
79. Park, J. E., Chen, H. H., Winer, J., Houck, K. A., and Ferrara, N. (1994) J. Biol. Chem. 269, 25646-25654
80. Christinger, H. W., Fuh, G., de Vos, A. M., and Wiesmann, C. (2004) J. Biol. Chem. 279, 10382-10388
81. Fong, T. A., Shawver, L. K., Sun, L., Tang, C., App, H., Powell, T. J., Kim, Y. H., Schreck, R., Wang, X., Risau, W., Ullrich, A., Hirth, K. P., and McMahon, G. (1999) Cancer Res. 59, 99-106
82. Kroll, J., and Waltenberger, J. (1997) J. Biol. Chem. 272, 32521-32527
83. Gluzman-Poltorak, Z., Cohen, T., Shibuya, M., and Neufeld, G. (2001) J. Biol. Chem. 276, 18688-18694
84. Mongiat, M., Taylor, K., Otto, J., Aho, S., Uitto, J., Whitelock, J. M., and Iozzo, R. V. (2000) J. Biol. Chem. 275, 7095-7100
85. Mongiat, M., Otto, J., Oldershaw, R., Ferrer, F., Sato, J. D., and Iozzo, R. V. (2001) J. Biol. Chem. 276, 10263-10271
86. Mongiat, M., Fu, J., Oldershaw, R., Greenhalgh, R., Gown, A. M., and Iozzo, R. V. (2003) J. Biol. Chem. 278, 17491-17499
87. Iozzo, R. V. (1994) Matrix Biol. 14, 203-208
88. Iozzo, R. V., Zoeller, J. J., and Nyström, A. (2009) Mol. Cells 27, 503-513
89. Seo, D. W., Li, H., Guedez, L., Wingfield, P. T., Diaz, T., Salloum, R., Wei, B. Y., and Stetler-Stevenson, W. G. (2003) Cell 114, 171-180
90. Seo, D. W., Li, H., Qu, C. K., Oh, J., Kim, Y. S., Diaz, T., Wei, B., Han, J. W., and Stetler-Stevenson, W. G. (2006) J. Biol. Chem. 281, 3711-3721
91. Lee, S. J., Tsang, P. S., Diaz, T. M., Wei, B. Y., and Stetler-Stevenson, W. G. (2010) Lab. Invest. 90, 374-382
92. Costell, M., Carmona, R., Gustafsson, E., González-Iriarte, M., Fässler, R., and Muñoz-Chápuli, R. (2002) Circ. Res. 91, 158-164
93. Nasevicius, A., Larson, J., and Ekker, S. C. (2000) Yeast 17, 294-301
94. Lawson, N. D., Mugford, J. W., Diamond, B. A., and Weinstein, B. M. (2003) Genes Dev. 17, 1346-1351
95. Muthusamy, A., Cooper, C. R., and Gomes, R. R., Jr. (2010) BMC Biochemistry 11, 43
96. Bhattacharya, R., Kwon, J., Wang, E., Mukherjee, P., and Mukhopadhyay, D. (2008) J. Mol. Signal. 3, 8
97. Poole, A. W., and Jones, M. L. (2005) Cell Signalling 17, 1323-1332
98. Chiang, M. K., and Flanagan, J. G. (1995) Growth Factors 12, 1-10
99. 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
100. Wiesmann, C., Fuh, G., Christinger, H. W., Eigenbrot, C., Wells, J. A., and de Vos, A. M. (1997) Cell 91, 695-704
101. Ruch, C., Skiniotis, G., Steinmetz, M. O., Walz, T., and Ballmer-Hofer, K. (2007) Nat. Struct. Mol. Biol. 14, 249-250
102. Yang, Y., Xie, P., Opatowsky, Y., and Schlessinger, J. (2010) Proc. Natl. Acad. Sci. U.S.A. 107, 1906-1911
103. Tvorogov, D., Anisimov, A., Zheng, W., Leppänen, V. M., Tammela, T., Laurinavicius, S., Holnthoner, W., Heloterä, H., Holopainen, T., Jeltsch, M., Kalkkinen, N., Lankinen, H., Ojala, P. M., and Alitalo, K. (2010) Cancer Cell 18, 630-640
104. Kendrew, J., Eberlein, C., Hedberg, B., McDaid, K., Smith, N. R., Weir, H. M., Wedge, S. R., Blakely, D. C., Foltz, I., Zhou, J., Kang, J. S., and Barry, S. T. (2011) Mol. Cancer Ther. 10, 770-784
105. Bix, G., and Iozzo, R. V. (2005) Trends Cell Biol. 15, 52-60
106. Zhang, Z., Ramirez, N. E., Yankeelov, T. E., Li, Z., Ford, L. E., Qi, Y., Pozzi, A., and Zutter, M. M. (2008) Blood 111, 1980-1988
107. Grenache, D. G., Zhang, Z., Wells, L. E., Santoro, S. A., Davidson, J. M., and Zutter, M. M. (2007) J. Invest. Dermatol. 127, 455-466
108. Zweers, M. C., Davidson, J. M., Pozzi, A., Hallinger, R., Janz, K., Quondamatteo, F., Leutgeb, B., Krieg, T., and Eckes, B. (2007) J. Invest. Dermatol. 127, 467-478
109. Cailhier, J. F., Sirois, I., Laplante, P., Lepage, S., Raymond, M. A., Brassard, N., Prat, A., Iozzo, R. V., Pshezhetsky, A. V., and Hébert, M. J. (2008) J. Biol. Chem. 283, 27220-27229
110. Grønborg, M., Kristiansen, T. Z., Iwahori, A., Chang, R., Reddy, R., Sato, N., Molina, H., Jensen, O. N., Hruban, R. H., Goggins, M. G., Maitra, A., and Pandey, A. (2006) Mol. Cell Proteom. 5, 157-171
111. Chang, J. W., Kang, U. B., Kim, D. H., Yi, J. K., Lee, J. W., Noh, D. Y., Lee, C., and Yu, M. H. (2008) Proteomics Clin. Appl. 2, 23-32