Lysyl oxidase-like protein-2 regulates sprouting angiogenesis and type IV collagen assembly in the endothelial basement membrane

Blood

Volumn 118, Issue 14, 2011, Pages 3979-3989

  Bignon, Marine ^a,b,c   Pichol Thievend, Cathy ^a,b,c   Hardouin, Julie ^d   Malbouyres, Marilyne ^e   Bréchot, Nicolas ^a,b,c   Nasciutti, Luiz ^a,b,c   Barret, Alain ^a,b,c   Teillon, Jérémie ^a,b,c   Guillon, Emilie ^e   Etienne, Eric ^a,b,c   Caron, Michel ^d   Joubert Caron, Raymonde ^d   Monnot, Catherine ^a,b,c   Ruggiero, Florence ^e   Muller, Laurent ^a,b,c   Germain, Stéphane ^a,b,c  

^a PSL RESEARCH UNIVERSITY   (France)

^b CNRS   (France)

^c INSERM   (France)

^d UNIVERSITÉ PARIS 13   (France)

^e UNIVERSITÉ DE LYON   (France)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 4; LYSYLOXIDASE LILE PROTEIN 2; PROTEIN LYSINE 6 OXIDASE; UNCLASSIFIED DRUG;

ANGIOGENESIS; ANIMAL TISSUE; ARTICLE; BASEMENT MEMBRANE; CELL MIGRATION; CELL PROLIFERATION; EMBRYO; ENDOTHELIUM CELL; ENZYME RELEASE; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; HYPOXIA; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEOMICS; UPREGULATION;

EID: 80053648630     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2010-10-313296     Document Type: Article

References (45)

1. Germain S, Monnot C, Muller L, Eichmann A. Hypoxia-driven angiogenesis: role of tip cells and extracellular matrix scaffolding. Curr Opin Hematol. 2010;17(3):245-251.
2. Gerhardt H, Golding M, Fruttiger M, et al. VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J Cell Biol. 2003;161(6):1163-1177. (Pubitemid 36870177)
3. West H, Richardson WD, Fruttiger M. Stabilization of the retinal vascular network by reciprocal feedback between blood vessels and astrocytes. Development. 2005;132(8):1855-1862. (Pubitemid 40691775)
4. Iruela-Arispe ML, Davis GE. Cellular and molecular mechanisms of vascular lumen formation. Dev Cell. 2009;16(2):222-231.
5. Davis GE, Senger DR. Endothelial extracellular matrix: biosynthesis, remodeling, and functions during vascular morphogenesis and neovessel stabilization. Circ Res. 2005;97(11):1093-1107.
6. Maki JM. Lysyl oxidases in mammalian development and certain pathological conditions. Histol Histopathol. 2009;24(5):651-660.
7. Rodriguez HM, Vaysberg M, Mikels A, et al. Modulation of lysyl oxidase-like 2 enzymatic activity by an allosteric antibody inhibitor. J Biol Chem. 2010;285(27):20964-20974.
8. Maki JM, Rasanen J, Tikkanen H, et al. Inactivation of the lysyl oxidase gene Lox leads to aortic aneurysms, cardiovascular dysfunction, and perinatal death in mice. Circulation. 2002;106(19):2503-2509. (Pubitemid 35278809)
9. Liu X, Zhao Y, Gao J, et al. Elastic fiber homeostasis requires lysyl oxidase-like 1 protein. Nat Genet. 2004;36(2):178-182. (Pubitemid 38174378)
10. Barry-Hamilton V, Spangler R, Marshall D, et al. Allosteric inhibition of lysyl oxidase-like-2 impedes the development of a pathologic microenvironment. Nat Med. 2010;16(9):1009-1017.
11. Brekhman V, Lugassie J, Zaffryar-Eilot S, et al. Receptor activity modifying protein-3 mediates the protumorigenic activity of lysyl oxidase-like protein-2. Faseb J. 2011;25(1):55-65.
12. Higgins DF, Kimura K, Bernhardt WM, et al. Hypoxia promotes fibrogenesis in vivo via HIF-1 stimulation of epithelial-to-mesenchymal transition. J Clin Invest. 2007;117(12):3810-3820. (Pubitemid 350224091)
13. Peinado H, Del Carmen Iglesias-de la Cruz M, Olmeda D, et al. A molecular role for lysyl oxidase-like 2 enzyme in snail regulation and tumor progression. EMBO J. 2005;24(19):3446-3458. (Pubitemid 41486782)
14. Lelievre E, Hinek A, Lupu F, Buquet C, Soncin F, Mattot V. VE-statin/egfl7 regulates vascular elastogenesis by interacting with lysyl oxidases. EMBO J. 2008;27(12):1658-1670.
15. Kumar S, Weaver VM. Mechanics, malignancy, and metastasis: the force journey of a tumor cell. Cancer Metastasis Rev. 2009;28(1-2):113-127.
16. Chomel C, Cazes A, Faye C, et al. Interaction of the coiled-coil domain with glycosaminoglycans protects angiopoietin-like 4 from proteolysis and regulates its antiangiogenic activity. Faseb J. 2009;23(3):940-949.
17. Brechot N, Gomez E, Bignon M, et al. Modulation of macrophage activation state protects tissue from necrosis during critical limb ischemia in thrombospondin-1-deficient mice. PLoS ONE. 2008;3(12):e3950.
18. del Toro R, Prahst C, Mathivet T, et al. Identification and functional analysis of endothelial tip cell-enriched genes. Blood. 2010;116(19):4025-33.
19. Le Jan S, Amy C, Cazes A, et al. Angiopoietin-like 4 is a proangiogenic factor produced during ischemia and in conventional renal cell carcinoma. Am J Pathol. 2003;162(5):1521-1528. (Pubitemid 36512834)
20. Cazes A, Galaup A, Chomel C, et al. Extracellular matrix-bound angiopoietin-like 4 inhibits endothelial cell adhesion, migration, and sprouting and alters actin cytoskeleton. Circ Res. 2006;99(11):1207-1215. (Pubitemid 44808657)
21. Palamakumbura AH, Trackman PC. A fluorometric assay for detection of lysyl oxidase enzyme activity in biological samples. Anal Biochem. 2002;300(2):245-251. (Pubitemid 34093700)
22. Nakatsu MN, Sainson RC, Aoto JN, et al. Angiogenic sprouting and capillary lumen formation modeled by human umbilical vein endothelial cells (HUVEC) in fibrin gels: the role of fibroblasts and angiopoietin-1. Microvasc Res. 2003;66(2):102-112. (Pubitemid 36962872)
23. Faye C, Inforzato A, Bignon M, et al. Transglutaminase- 2: a new endostatin partner in the extracellular matrix of endothelial cells. Biochem J. 2010;427(3):467-475.
24. Le Jan S, Le Meur N, Cazes A, et al. Characterization of the expression of the hypoxia-induced genes neuritin, TXNIP and IGFBP3 in cancer. FEBS Lett. 2006;580(14):3395-3400. (Pubitemid 43795919)
25. Manalo DJ, Rowan A, Lavoie T, et al. Transcriptional regulation of vascular endothelial cell responses to hypoxia by HIF-1. Blood. 2005;105(2):659-669. (Pubitemid 40070750)
26. Couffinhal T, Silver M, Zheng LP, Kearney M, Witzenbichler B, Isner JM. Mouse model of angiogenesis. Am J Pathol. 1998;152(6):1667-1679. (Pubitemid 28275025)
27. Gansner JM, Mendelsohn BA, Hultman KA, Johnson SL, Gitlin JD. Essential role of lysyl oxidases in notochord development. Dev Biol. 2007;307(2):202-213. (Pubitemid 47001354)
28. Isogai S, Lawson ND, Torrealday S, Horiguchi M, Weinstein BM. Angiogenic network formation in the developing vertebrate trunk. Development. 2003;130(21):5281-5290. (Pubitemid 37369685)
29. Reynaud C, Baas D, Gleyzal C, Le Guellec D, Sommer P. Morpholino knockdown of lysyl oxidase impairs zebrafish development, and reflects some aspects of copper metabolism disorders. Matrix Biol. 2008;27(6):547-560.
30. Levental KR, Yu H, Kass L, et al. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell. 2009;139(5):891-906.
31. Rhodes JM, Simons M. The extracellular matrix and blood vessel formation: not just a scaffold. J Cell Mol Med. 2007;11(2):176-205. (Pubitemid 46695692)
32. Scheurer SB, Rybak JN, Rosli C, Neri D, Elia G. Modulation of gene expression by hypoxia in human umbilical cord vein endothelial cells: a transcriptomic and proteomic study. Proteomics. 2004;4(6):1737-1760. (Pubitemid 38738330)
33. Fujimoto E, Tajima S. Reciprocal regulation of LOX and LOXL2 expression during cell adhesion and terminal differentiation in epidermal keratinocytes. J Dermatol Sci. 2009;55(2):91-98.
34. Hein S, Yamamoto SY, Okazaki K, Jourdan-LeSaux C, Csiszar K, Bryant-Greenwood GD. Lysyl oxidases: expression in the fetal membranes and placenta. Placenta. 2001;22(1):49-57. (Pubitemid 32124096)
35. Reiser K, McCormick RJ, Rucker RB. Enzymatic and nonenzymatic cross-linking of collagen and elastin. Faseb J. 1992;6(7):2439-2449.
36. Maki JM, Sormunen R, Lippo S, Kaarteenaho-Wiik R, Soininen R, Myllyharju J. Lysyl oxidase is essential for normal development and function of the respiratory system and for the integrity of elastic and collagen fibers in various tissues. Am J Pathol. 2005;167(4):927-936. (Pubitemid 41416246)
37. Siekmann AF, Lawson ND. Notch signalling and the regulation of angiogenesis. Cell Adh Migr. 2007;1(2):104-106.
38. Payne SL, Fogelgren B, Hess AR, et al. Lysyl oxidase regulates breast cancer cell migration and adhesion through a hydrogen peroxide-mediated mechanism. Cancer Res. 2005;65(24):11429-11436. (Pubitemid 41821700)
39. Hollosi P, Yakushiji JK, Fong KS, Csiszar K, Fong SF. Lysyl oxidase-like 2 promotes migration in noninvasive breast cancer cells but not in normal breast epithelial cells. Int J Cancer. 2009;125(2):318-327.
40. Lucero HA, Ravid K, Grimsby JL, et al. Lysyl oxidase oxidizes cell membrane proteins and enhances the chemotactic response of vascular smooth muscle cells. J Biol Chem. 2008;283(35):24103-24117.
41. Poschl E, Schlotzer-Schrehardt U, Brachvogel B, Saito K, Ninomiya Y, Mayer U. Collagen IV is essential for basement membrane stability but dispensable for initiation of its assembly during early development. Development. 2004;131(7):1619-1628. (Pubitemid 38559288)
42. Kucera T, Strilic B, Regener K, Schubert M, Laudet V, Lammert E. Ancestral vascular lumen formation via basal cell surfaces. PLoS One. 2009;4(1):e4132.
43. Sacharidou A, Koh W, Stratman AN, Mayo AM, Fisher KE, Davis GE. Endothelial lumen signaling complexes control 3D matrix-specific tubulogenesis through interdependent Cdc42- and MT1-MMP-mediated events. Blood. 2010;115(25):5259-5269.
44. Stratman AN, Malotte KM, Mahan RD, Davis MJ, Davis GE. Pericyte recruitment during vasculogenic tube assembly stimulates endothelial basement membrane matrix formation. Blood. 2009;114(24):5091-5101.
45. Zovein AC, Luque A, Turlo KA, et al. Beta1 integrin establishes endothelial cell polarity and arteriolar lumen formation via a Par3-dependent mechanism. Dev Cell. 2010;18(1):39-51.