Endostatin binds biglycan and LDL and interferes with LDL retention to the subendothelial matrix during atherosclerosis

Journal of Lipid Research

Volumn 46, Issue 9, 2005, Pages 1849-1859

  Zeng, Xiaokun ^a   Chen, Joshua ^a   Miller, Yury I ^b   Javaherian, Kashi ^a   Moulton, Karen S ^a,c  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Collagen XVIII; Extracellular matrix; Low density lipoprotein; Proteoglycans; Vascular basement membrane

Indexed keywords

BIGLYCAN; COLLAGEN TYPE 18; ENDOSTATIN; LOW DENSITY LIPOPROTEIN;

ARTICLE; ATHEROMA; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; BASEMENT MEMBRANE; BLOOD VESSEL PERMEABILITY; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENDOTHELIUM; HUMAN; HUMAN CELL; HUMAN TISSUE; LIPID COMPOSITION; NEOVASCULARIZATION (PATHOLOGY); PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN LIPID INTERACTION; VASCULAR ENDOTHELIUM;

ANIMALS; AORTA; ARTERIOSCLEROSIS; BASEMENT MEMBRANE; BINDING SITES; BINDING, COMPETITIVE; COLLAGEN TYPE XVIII; ENDOSTATINS; ENDOTHELIUM; EXTRACELLULAR MATRIX PROTEINS; GLYCOSAMINOGLYCANS; HUMANS; LIPOPROTEINS; LIPOPROTEINS, LDL; MACROPHAGES; MACROPHAGES, PERITONEAL; MICE; MICE, INBRED C57BL; PROTEOGLYCANS; RECOMBINANT PROTEINS; UMBILICAL VEINS;

EID: 24344507690     PISSN: 00222275     EISSN: None     Source Type: Journal    
DOI: 10.1194/jlr.M500241-JLR200     Document Type: Article

References (39)

1. Williams, K. J., and I. Tabas. 1998. The response-to-retention hypothesis of atherogenesis reinforced. Curr. Opin. Lipidol. 9: 471-474.
2. Williams, K. J., and I. Tabas. 1995. The response-to-retention hypothesis of early atherogenesis. Arterioscler. Thromb. Vasc. Biol. 15: 551-561.
3. Srinivasan, S. R., B. Radhakrishnamurthy, P. Vijayagopal, and G. S. Berenson. 1991. Proteoglycans, lipoproteins, and atherosclerosis. Adv. Exp. Med. Biol. 285: 373-381.
4. O'Brien, K. D., K. L. Olin, C. E. Alpers, W. Chiu, M. Ferguson, K. Hudkins, T. N. Wight, and A. Chait. 1998. Comparison of apolipoprotein and proteoglycan deposits in human coronary atherosclerotic plaques: colocalization of biglycan with apolipoproteins. Circulation. 98: 519-527.
5. Kunjathoor, V. V., D. S. Chiu, K. D. O'Brien, and R. C. LeBoeuf. 2002. Accumulation of biglycan and perlecan, but not versican, in lesions of murine models of atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 22: 462-468.
6. Olin, K. L., S. Potter-Perigo, P. H. Barrett, T. N. Wight, and A. Chait. 2001. Biglycan, a vascular proteoglycan, binds differently to HDL2 and HDL3: role of apoE. Arterioscler. Thromb. Vasc. Biol. 21: 129-135.
7. Hurt-Camejo, E., G. Camejo, B. Rosengren, F. Lopez, C. Ahlstrom, G. Fager, and G. Bondjers. 1992. Effect of arterial proteoglycans and glycosaminoglycans on low density lipoprotein oxidation and its uptake by human macrophages and arterial smooth muscle cells. Arterioscler. Thromb. 12: 569-583.
8. Hurt, E., G. Bondjers, and G. Camejo. 1990. Interaction of LDL with human arterial proteoglycans stimulates its uptake by human monocyte-derived macrophages. J. Lipid Res. 31: 443-454.
9. Skalen, K., M. Gustafsson, E. K. Rydberg, L. M. Hulten, O. Wiklund, T. L. Innerarity, and J. Boren. 2002. Subendothelial retention of atherogenic lipoproteins in early atherosclerosis. Nature. 417: 750-754.
10. Boren, J., K. Olin, I. Lee, A. Chait, T. N. Wight, and T. L. Innerarity. 1998. Identification of the principal proteoglycan-binding site in LDL. A single-point mutation in apo-B100 severely affects proteoglycan interaction without affecting LDL receptor binding. J. Clin. Invest. 101: 2658-2664.
11. Pillarisetti, S., L. Paka, J. C. Obunike, L. Berglund, and I. J. Goldberg. 1997. Subendothelial retention of lipoprotein (a). Evidence that reduced heparan sulfate promotes lipoprotein binding to subendothelial matrix. J. Clin. Invest. 100: 867-874.
12. Halfter, W., S. Dong, B. Schurer, and G. J. Cole. 1998. Collagen XVIII is a basement membrane heparan sulfate proteoglycan. J. Biol. Chem. 273: 25404-25412.
13. Miosge, N., T. Sasaki, and R. Timpl. 1999. Angiogenesis inhibitor endostatin is a distinct component of elastic fibers in vessel walls. FASEB J. 13: 1743-1750.
14. O'Reilly, M. S., T. Boehm, Y. Shing, N. Fukai, G. Vasios, W. S. Lane, E. Flynn, J. R. Birkhead, B. R. Olsen, and J. Folkman. 1997. Endostatin: an endogenous inhibitor of angiogenesis and tumor growth. Cell. 88: 277-285.
15. Moulton, K. S., E. Heller, M. A. Konerding, E. Flynn, W. Palinski, and J. Folkman. 1999. Angiogenesis inhibitors endostatin or TNP-470 reduce intimal neovascularization and plaque growth in apolipoprotein E-deficient mice. Circulation. 99: 1726-1732.
16. Dong, S., G. J. Cole, and W. Halfter. 2003. Expression of collagen XVIII and localization of its glycosaminoglycan attachment sites. J. Biol. Chem. 278: 1700-1707.
17. Marneros, A. G., D. R. Keene, U. Hansen, N. Fukai, K. Moulton, P. L. Goletz, G. Moiseyev, B. S. Pawlyk, W. Halfter, S. Dong, et al. 2004. Collagen XVIII/endostatin is essential for vision and retinal pigment epithelial function. EMBO J. 23: 89-99.
18. Ferreras, M., U. Felbor, T. Lenhard, B. R. Olsen, and J. Delaisse. 2000. Generation and degradation of human endostatin proteins by various proteinases. FEBS Lett. 486: 247-251.
19. Moulton, K. S., B. R. Olsen, S. Sonn, N. Fukai, D. Zurakowski, and X. Zeng. 2004. Loss of collagen XVIII enhances neovascularization and vascular permeability in atherosclerosis. Circulation. 110: 1330-1336.
20. Javaherian, K., S. Y. Park, W. F. Pickl, K. R. LaMontagne, R. T. Sjin, S. Gillies, and K. M. Lo. 2002. Laminin modulates morphogenic properties of the collagen XVIII endostatin domain. J. Biol. Chem. 277: 45211-45218.
21. Sasaki, T., H. Larsson, J. Kreuger, M. Salmivirta, L. Claesson-Welsh, U. Lindahl, E. Hohenester, and R. Timpl. 1999. Structural basis and potential role of heparin/heparan sulfate binding to the angiogenesis inhibitor endostatin. EMBO J. 18: 6240-6248.
22. Fisher, L. W., J. T. Stubbs 3rd, and M. F. Young. 1995. Antisera and cDNA probes to human and certain animal model bone matrix noncollagenous proteins. Acta Orthop. Scand. Suppl. 266: 61-65.
23. Tjin Tham Sjin, R. M., R. Satchi-Fainaro, A. E. Birsner, V. M. Ramanujam, J. Folkman, and K. Javaherian. 2005. A 27-amino-acid synthetic peptide corresponding to the NH2-terminal zinc-binding domain of endostatin is responsible for its antitumor activity. Cancer Res. 65: 3656-3663.
24. Ding, Y. H., K. Javaherian, K. M. Lo, R. Chopra, T. Boehm, J. Lanciotti, B. A. Harris, Y. Li, R. Shapiro, E. Hohenester, R. Timpl, et al. 1998. Zinc-dependent dimers observed in crystals of human endostatin. Proc. Natl. Acad. Sci. USA. 95: 10443-10448.
25. Goldstein, J. L., S. K. Basu, and M. S. Brown. 1983. Receptor-mediated endocytosis of low density lipoprotein in cultured cells. Methods Enzymol. 98: 241-260.
26. Miller, Y. I., S. Viriyakosol, C. J. Binder, J. R. Feramisco, T. N. Kirkland, and J. L. Witztum. 2003. Minimally modified LDL binds to CD14, induces macrophage spreading via TLR4/MD-2, and inhibits phagocytosis of apoptotic cells. J. Biol. Chem. 278: 1561-1568.
27. Miller, Y. I., D. S. Worrall, C. D. Funk, J. R. Feramisco, and J. L. Witztum. 2003. Actin polymerization in macrophages in response to oxidized LDL and apoptotic cells: role of 12/15-lipoxygenase and phosphoinositide 3-kinase. Mol. Biol. Cell. 14: 4196-4206.
28. Lim, Y. C., G. Garcia-Cardena, J. R. Allport, M. Zervoglos, A. J. Connolly, M. A. Gimbrone, Jr., and F. W. Luscinskas. 2002. Heterogeneity of endothelial cells from different organ sites in T-cell subset recruitment. Am. J. Pathol. 162: 1591-1601.
29. Ricard-Blum, S., O. Feraud, H. Lortat-Jacob, A. Rencurosi, N. Fukai, F. Dkhissi, D. Vittet, A. Imberty, B. R. Olsen, and M. van der Rest. 2004. Characterization of endostatin binding to heparin and heparan sulfate by surface plasmon resonance and molecular modeling: role of divalent cations. J. Biol. Chem. 279: 2927-2936.
30. Sasaki, T., H. Larsson, D. Tisi, L. Claesson-Welsh, E. Hohenester, and R. Timpl. 2000. Endostatins derived from collagens XV and XVIII differ in structural and binding properties, tissue distribution and anti-angiogenic activity. J. Mol. Biol. 301: 1179-1190.
31. Hohenester, E., T. Sasaki, B. R. Olsen, and R. Timpl. 1998. Crystal structure of the angiogenesis inhibitor endostatin at 1.5 A resolution. EMBO J. 17: 1656-1664.
32. O'Brien, K. D., K. Lewis, J. W. Fischer, P. Johnson, J. Y. Hwang, E. A. Knopp, M. G. Kinsella, P. H. Barrett, A. Chait, and T. N. Wight. 2004. Smooth muscle cell biglycan overexpression results in increased lipoprotein retention on extracellular matrix: implications for the retention of lipoproteins in atherosclerosis. Atherosclerosis. 177: 29-35.
33. Hurt, E., and G. Camejo. 1987. Effect of arterial proteoglycans on the interaction of LDL with human monocyte-derived macrophages. Atherosclerosis. 67: 115-126.
34. Williams, K. J. 2001. Arterial wall chondroitin sulfate proteoglycans: diverse molecules with distinct roles in lipoprotein retention and atherogenesis. Curr. Opin. Lipidol. 12: 477-487.
35. Oorni, K., M. O. Pentikainen, M. Ala-Korpela, and P. T. Kovanen. 2000. Aggregation, fusion, and vesicle formation of modified low density lipoprotein particles: molecular mechanisms and effects on matrix interactions. J. Lipid Res. 41: 1703-1714.
36. Wight, T. N. 1989. Cell biology of arterial proteoglycans. Arteriosclerosis. 9: 1-20.
37. Ren, B., Y. Wang, X. Rabasseda, and Y. Z. Wang. 2002. Recombinant human endostatin is beneficial to endothelial cell growth exposed to mildly oxidized low-density lipoproteins. Methods Find. Exp. Clin. Pharmacol. 24: 195-199.
38. Yang, D. J., K. D. Kim, N. R. Schechter, D. F. Yu, P. Wu, A. Azhdarinia, J. S. Roach, S. K. Kalimi, K. Ozaki, W. E. Fogler, et al. 2002. Assessment of antiangiogenic effect using 99mTc-EC-endostatin. Cancer Biother. Radiopharm. 17: 233-245.
39. Citrin, D., A. K. Lee, T. Scott, M. Sproull, C. Menard, P. J. Tofilon, and K. Camphausen. 2004. In vivo tumor imaging in mice with near-infrared labeled endostatin. Mol. Cancer Ther. 3: 481-488.