Extracellular matrix-bound angiopoietin-like 4 inhibits endothelial cell adhesion, migration, and sprouting and alters actin cytoskeleton

Circulation Research

Volumn 99, Issue 11, 2006, Pages 1207-1215

  Cazes, Aurélie ^a   Galaup, Ariane ^a   Chomel, Clémence ^a   Bignon, Marine ^a   Bréchot, Nicolas ^a   Jan, Sébastien Le ^a   Weber, Holger ^b   Corvol, Pierre ^a   Muller, Laurent ^a   Germain, Stéphane ^a,c   Monnot, Catherine ^a  

^a INSERM   (France)

^b TUMOR BIOLOGY CENTER   (Germany)

^c HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

Author keywords

Angiogenesis; Endothelial cells; Extracellular matrix; Hypoxia

Indexed keywords

ACTIN; ANGIOPOIETIN; ANGIOPOIETIN 4; HEPARAN SULFATE; HEPARIN; PROTEOGLYCAN; UNCLASSIFIED DRUG;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOCRINE EFFECT; BINDING ASSAY; CELL ADHESION; CELL MIGRATION; CELL MOTILITY; CELL STRAIN HEK293; CONTROLLED STUDY; CYTOSKELETON; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; HYPOXIA; ISCHEMIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN SECRETION;

ACTINS; ANIMALS; ANOXIA; BIOLOGICAL AVAILABILITY; BLOOD PROTEINS; CELL ADHESION; CELL MOVEMENT; CELLS, CULTURED; CYTOSKELETON; ENDOTHELIAL CELLS; EXTRACELLULAR MATRIX; HEPARIN; HINDLIMB; ISCHEMIA; MICE; MICE, INBRED C57BL; NEOVASCULARIZATION, PHYSIOLOGIC; PROTEOGLYCANS;

EID: 33751341522     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.0000250758.63358.91     Document Type: Article

References (32)

1. Carmeliet P. Angiogenesis in health and disease. Nat Med. 2003;9:653-660.
2. Le Jan S, Amy C, Cazes A, Monnot C, Lamande N, Favier J, Philippe J, Sibony M, Gasc JM, Corvol P, Germain S. Angiopoietin-like 4 is a proangiogenic factor produced during ischemia and in conventional renal cell carcinoma. Am J Pathol. 2003;162:1521-1528.
3. Kim I, Kim HG, Kim H, Kim HH, Park SK, Uhm CS, Lee ZH, Koh GY. Hepatic expression, synthesis and secretion of a novel fibrinogen/angiopoietin-related protein that prevents endothelial-cell apoptosis. Biochem J. 2000;346:603-610.
4. Ge H, Yang G, Huang L, Motola DL, Pourbahrami T, Li C. Oligomerization and regulated proteolytic processing of angiopoietin-like protein 4. J Biol Chem. 2004;279:2038-2045.
5. Suri C, Jones PF, Patan S, Bartunkova S, Maisonpierre PC, Davis S, Sato TN, Yancopoulos GD. Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell. 1996;87:1171-1180.
6. Maisonpierre PC, Suri C, Jones PF, Bartunkova S, Wiegand SJ, Radziejewski C, Compton D, McClain J, Aldrich TH, Papadopoulos N, Daly TJ, Davis S, Sato TN, Yancopoulos GD. Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis. Science. 1997;277:55-60.
7. Dhanabal M, LaRochelle WJ, Jeffers M, Herrmann J, Rastelli L, McDonald WF, Chillakuru RA, Yang M, Boldog FL, Padigaru M, McQueeney KD, Wu F, Minskoff SA, Shimkets RA, Lichenstein HS. Angioarrestin: an antiangiogenic protein with tumor-inhibiting properties. Cancer Res. 2002;62:3834-3841.
8. Kubota Y, Oike Y, Satoh S, Tabata Y, Niikura Y, Morisada T, Akao M, Urano T, Ito Y, Miyamoto T, Nagai N, Koh GY, Watanabe S, Suda T. Cooperative interaction of Angiopoietin-like proteins 1 and 2 in zebrafish vascular development. Proc Natl Acad Sci U S A. 2005;102:13502-13507.
9. Kim I, Moon SO, Koh KN, Kim H, Uhm CS, Kwak HJ, Kim NG, Koh GY. Molecular cloning, expression, and characterization of angiopoietin-related protein. Angiopoietin-related protein induces endothelial cell sprouting. J Biol Chem. 1999;274:26523-26528.
10. Camenisch G, Pisabarro MT, Sherman D, Kowalski J, Nagel M, Hass P, Xie MH, Gurney A, Bodary S, Liang XH, Clark K, Beresini M, Ferrara N, Gerber HP. ANGPTL3 stimulates endothelial cell adhesion and migration via integrin alpha vbeta 3 and induces blood vessel formation in vivo. J Biol Chem. 2002;277:17281-17290.
11. Ito Y, Oike Y, Yasunaga K, Hamada K, Miyata K, Matsumoto S, Sugano S, Tanihara H, Masuho Y, Suda T. Inhibition of angiogenesis and vascular leakiness by angiopoietin-related protein 4. Cancer Res. 2003;63:6651-6657.
12. Hermann LM, Pinkerton M, Jennings K, Yang L, Grom A, Sowders D, Kersten S, Witte DP, Hirsch R, Thornton S. Angiopoietin-like-4 is a potential angiogenic mediator in arthritis. Clin Immunol. 2005;115:93-101.
13. Yoon JC, Chickering TW, Rosen ED, Dussault B, Qin Y, Soukas A, Friedman JM, Holmes WE, Spiegelman BM. Peroxisome proliferator-activated receptor gamma target gene encoding a novel angiopoietin-related protein associated with adipose differentiation. Mol Cell Biol. 2000;20:5343-5349.
14. Kersten S, Mandard S, Tan NS, Escher P, Metzger D, Chambon P, Gonzalez FJ, Desvergne B, Wahli W. Characterization of the fasting-induced adipose factor FIAF, a novel peroxisome proliferator-activated receptor target gene. J Biol Chem. 2000;275:28488-28493.
15. Yoshida K, Shimizugawa T, Ono M, Furukawa H. Angiopoietin-like protein 4 is a potent hyperlipidemia-inducing factor in mice and inhibitor of lipoprotein lipase. J Lipid Res. 2002;43:1770-1772.
16. Xu A, Lam MC, Chan KW, Wang Y, Zhang J, Hoo RL, Xu JY, Chen B, Chow WS, Tso AW, Lam KS. Angiopoietin-like protein 4 decreases blood glucose and improves glucose tolerance but induces hyperlipidemia and hepatic steatosis in mice. Proc Natl Acad Sci U S A. 2005;102:6086-6091.
17. Yu X, Burgess SC, Ge H, Wong KK, Nassem RH, Garry DJ, Sherry AD, Malloy CR, Berger JP, Li C. Inhibition of cardiac lipoprotein utilization by transgenic overexpression of Angptl4 in the heart. Proc Natl Acad Sci U S A. 2005;102:1767-1772.
18. Davis GE, Senger DR. Endothelial extracellular matrix: biosynthesis, remodeling, and functions during vascular morphogenesis and neovessel stabilization. Circ Res. 2005;97:1093-1107.
19. Xu Y, Yu Q. Angiopoietin-1, unlike angiopoietin-2, is incorporated into the extracellular matrix via its linker peptide region. J Biol Chem. 2001;276:34990-34998.
20. Hutchings H, Ortega N, Plouet J. Extracellular matrix-bound vascular endothelial growth factor promotes endothelial cell adhesion, migration, and survival through integrin ligation. FASEB J. 2003;17:1520-1522.
21. Owensby DA, Morton PA, Schwartz AL. Interactions between tissue-type plasminogen activator and extracellular matrix-associated plasminogen activator inhibitor type 1 in the human hepatoma cell line HepG2. J Biol Chem. 1989;264:18180-18187.
22. Couffinhal T, Silver M, Zheng LP, Kearney M, Witzenbichler B, Isner JM. Mouse model of angiogenesis. Am J Pathol. 1998;152:1667-1679.
23. Le Jan S, Le Meur N, Cazes A, Philippe J, Le Cunff M, Leger J, Corvol P, Germain S. Characterization of the expression of the hypoxia-induced genes neuritin, TXNIP and IGFBP3 in cancer. FEBS Lett. 2006;580:3395-3400.
24. Korff T, Augustin HG. Tensional forces in fibrillar extracellular matrices control directional capillary sprouting. J Cell Sci. 1999;112:3249-3258.
25. Brigstock DR. The connective tissue growth factor/cysteine-rich 61/nephroblastoma overexpressed (CCN) family. Endocr Rev. 1999;20:189-206.
26. Mandard S, Zandbergen F, Tan NS, Escher P, Patsouris D, Koenig W, Kleemann R, Bakker A, Veenman F, Wahli W, Muller M, Kersten S. The direct peroxisome proliferator-activated receptor target fasting-induced adipose factor (FIAF/PGAR/ANGPTL4) is present in blood plasma as a truncated protein that is increased by fenofibrate treatment. J Biol Chem. 2004;279:34411-34420.
27. Kireeva ML, Latinkic BV, Kolesnikova TV, Chen CC, Yang GP, Abler AS, Lau LF. Cyr61 and Fisp12 are both ECM-associated signaling molecules: activities, metabolism, and localization during development. Exp Cell Res. 1997;233:63-77.
28. Belanger AJ, Lu H, Date T, Liu LX, Vincent KA, Akita GY, Cheng SH, Gregory RJ, Jiang C. Hypoxia up-regulates expression of peroxisome proliferator-activated receptor gamma angiopoietin-related gene (PGAR) in cardiomyocytes: role of hypoxia inducible factor 1α. J Mol Cell Cardiol. 2002;34:765-774.
29. Ono M, Shimizugawa T, Shimamura M, Yoshida K, Noji-Sakikawa C, Ando Y, Koishi R, Furukawa H. Protein region important for regulation of lipid metabolism in angiopoietin-like 3 (ANGPTL3): ANGPTL3 is cleaved and activated in vivo. J Biol Chem. 2003;278:41804-41809.
30. Murphy-Ullrich JE. The de-adhesive activity of matricellular proteins: is intermediate cell adhesion an adaptive state? J Clin Invest. 2001;107:785-790.
31. Bornstein P, Sage EH. Matricellular proteins: extracellular modulators of cell function. Curr Opin Cell Biol. 2002;14:608-616.
32. Carlson TR, Feng Y, Maisonpierre PC, Mrksich M, Morla AO. Direct cell adhesion to the angiopoietins mediated by integrins. J Biol Chem. 2001;276:26516-26525.