Decrease in VEGF expression induces intussusceptive vascular pruning

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 31, Issue 12, 2011, Pages 2836-2844

  Hlushchuk, Ruslan ^a,c   Ehrbar, Martin ^b   Reichmuth, Philipp ^a   Heinimann, Niklas ^a   Styp Rekowska, Beata ^a,c   Escher, Robert ^e   Baum, Oliver ^f   Lienemann, Philipp ^b   Makanya, Andrew ^a   Keshet, Eli ^d   Djonov, Valentin ^a,c  

^a UNIVERSITY OF FRIBOURG   (Switzerland)

^b UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^c UNIVERSITY OF BERN   (Switzerland)

^d HEBREW UNIVERSITY   (Israel)

^e UNIVERSITY OF BERN   (Switzerland)

^f NONE

Author keywords

angiogenesis; intussusceptive vascular pruning; morphogenesis; vascular biology

Indexed keywords

RECOMBINANT VASCULOTROPIN; VASCULOTROPIN; VASCULOTROPIN 165; VASCULOTROPIN A;

ANGIOGENESIS; APOPTOSIS; ARTICLE; CHORIOALLANTOIS; CONTROLLED STUDY; EMBRYO; ENZYME LINKED IMMUNOSORBENT ASSAY; HYDROGEL; IN VIVO STUDY; INTUSSUSCEPTIVE VASCULAR PRUNING; MICROSCOPY; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; VASCULARIZATION;

ANIMALS; APOPTOSIS; CHICK EMBRYO; CHORIOALLANTOIC MEMBRANE; ENDOTHELIUM, VASCULAR; GENE EXPRESSION REGULATION; MODELS, ANIMAL; NEOVASCULARIZATION, PHYSIOLOGIC; SIGNAL TRANSDUCTION; TIME FACTORS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 81755184136     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.111.231811     Document Type: Article

References (39)

1. Makanya AN, Hlushchuk R, Djonov VG. Intussusceptive angiogenesis and its role in vascular morphogenesis, patterning, and remodeling. Angiogenesis. 2009;12:113-123.
2. Franco CA, Liebner S, Gerhardt H. Vascular morphogenesis: a Wnt for every vessel? Curr Opin Genet Dev. 2009;19:476-483.
3. Rouget C. Memoire sur le developpement, la structure et les proprietes physiologiques des capillaries sanguins et lymphatiques. Arch Physiol Norm Pathol. 1873;5:603-663.
4. Ashton N. Neovascularization in ocular disease. Trans Ophthalmol Soc UK. 1961;81:145-161.
5. Ashton N. Oxygen and the growth and development of retinal vessels. In vivo and in vitro studies. The XX Francis I. Proctor Lecture. Am J Ophthalmol. 1966;62:412-435.
6. Djonov V, Baum O, Burri PH. Vascular remodeling by intussusceptive angiogenesis. Cell Tissue Res. 2003;314:107-117. (Pubitemid 37409917)
7. Risau W. Mechanisms of angiogenesis. Nature. 1997;386:671-674. (Pubitemid 27193480)
8. Ferrara N, Kerbel RS. Angiogenesis as a therapeutic target. Nature. 2005;438:967-974. (Pubitemid 43093963)
9. Gerber HP, Dixit V, Ferrara N. Vascular endothelial growth factor induces expression of the antiapoptotic proteins Bcl-2 and A1 in vascular endothelial cells. J Biol Chem. 1998;273:13313-13316. (Pubitemid 28246905)
10. Ferrara N, Gerber HP, LeCouter J. The biology of VEGF and its receptors. Nat Med. 2003;9:669-676. (Pubitemid 36749215)
11. Gerhardt H, Golding M, Fruttiger M, Ruhrberg C, Lundkvist A, Abramsson A, Jeltsch M, Mitchell C, Alitalo K, Shima D, Betsholtz C. VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J Cell Biol. 2003;161:1163-1177. (Pubitemid 36870177)
12. Carmeliet P, De SF, Loges S, Mazzone M. Branching morphogenesis and antiangiogenesis candidates: tip cells lead the way. Nat Rev Clin Oncol. 2009;6:315-326.
13. Benjamin LE, Hemo I, Keshet E. A plasticity window for blood vessel remodelling is defined by pericyte coverage of the preformed endothelial network and is regulated by PDGF-B and VEGF. Development. 1998; 125:1591-1598. (Pubitemid 28256727)
14. Hlushchuk R, Riesterer O, Baum O, Wood J, Gruber G, Pruschy M, Djonov V. Tumor recovery by angiogenic switch from sprouting to intussusceptive angiogenesis after treatment with PTK787/ZK222584 or ionizing radiation. Am J Pathol. 2008;173:1173-1185.
15. Shweiki D, Itin A, Soffer D, Keshet E. Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature. 1992;359:843-845.
16. Hlushchuk R, Baum O, Gruber G, Wood J, Djonov V. The synergistic action of a VEGF-receptor tyrosine-kinase inhibitor and a sensitizing PDGF-receptor blocker depends upon the stage of vascular maturation. Microcirculation. 2007;14:813-825. (Pubitemid 350131389)
17. Ehrbar M, Rizzi SC, Schoenmakers RG, Miguel BS, Hubbell JA, Weber FE, Lutolf MP. Biomolecular hydrogels formed and degraded via sitespecific enzymatic reactions. Biomacromolecules. 2007;8:3000-3007. (Pubitemid 350011618)
18. Djonov V, Schmid M, Tschanz SA, Burri PH. Intussusceptive angiogenesis: its role in embryonic vascular network formation. Circ Res. 2000;86:286-292. (Pubitemid 30108822)
19. Djonov VG, Kurz H, Burri PH. Optimality in the developing vascular system: branching remodeling by means of intussusception as an efficient adaptation mechanism. Dev Dyn. 2002;224:391-402. (Pubitemid 34848063)
20. Ehrbar M, Zeisberger SM, Raeber GP, Hubbell JA, Schnell C, Zisch AH. The role of actively released fibrin-conjugated VEGF for VEGF receptor 2 gene activation and the enhancement of angiogenesis. Biomaterials. 2008;29:1720-1729.
21. Augustin H. Methods in Endothelial Cell Biology. Berlin: Springer; 2004.
22. Burri PH, Hlushchuk R, Djonov V. Intussusceptive angiogenesis: its emergence, its characteristics, and its significance. Dev Dyn. 2004;231: 474-488. (Pubitemid 39410882)
23. Auerbach R, Lewis R, Shinners B, Kubai L, Akhtar N. Angiogenesis assays: a critical overview. Clin Chem. 2003;49:32-40. (Pubitemid 36078551)
24. Ehrbar M, Djonov VG, Schnell C, Tschanz SA, Martiny-Baron G, Schenk U, Wood J, Burri PH, Hubbell JA, Zisch AH. Cell-demanded liberation of VEGF121 from fibrin implants induces local and controlled blood vessel growth. Circ Res. 2004;94:1124-1132. (Pubitemid 38579708)
25. Hagedorn M, Balke M, Schmidt A, Bloch W, Kurz H, Javerzat S, Rousseau B, Wilting J, Bikfalvi A. VEGF coordinates interaction of pericytes and endothelial cells during vasculogenesis and experimental angiogenesis. Dev Dyn. 2004;230:23-33. (Pubitemid 38544070)
26. Wilting J, Birkenhager R, Eichmann A, Kurz H, Martiny-Baron G, Marme D, McCarthy JE, Christ B, Weich HA. VEGF121 induces proliferation of vascular endothelial cells and expression of flk-1 without affecting lymphatic vessels of chorioallantoic membrane. Dev Biol. 1996; 176:76-85.
27. Dor Y, Djonov V, Abramovitch R, Itin A, Fishman GI, Carmeliet P, Goelman G, Keshet E. Conditional switching of VEGF provides new insights into adult neovascularization and pro-angiogenic therapy. EMBO J. 2002; 21:1939-1947. (Pubitemid 34437191)
28. Dor Y, Porat R, Keshet E. Vascular endothelial growth factor and vascular adjustments to perturbations in oxygen homeostasis. Am J Physiol Cell Physiol. 2001;280:C1367-C1374. (Pubitemid 32553191)
29. Jain RK, Duda DG, Clark JW, Loeffler JS. Lessons from phase III clinical trials on anti-VEGF therapy for cancer. Nat Clin Pract Oncol. 2006;3: 24-40. (Pubitemid 43108832)
30. Alon T, Hemo I, Itin A, Pe'er J, Stone J, Keshet E. Vascular endothelial growth factor acts as a survival factor for newly formed retinal vessels and has implications for retinopathy of prematurity. Nat Med. 1995;1: 1024-1028.
31. Lange C, Ehlken C, Stahl A, Martin G, Hansen L, Agostini HT. Kinetics of retinal vaso-obliteration and neovascularisation in the oxygen-induced retinopathy (OIR) mouse model. Graefes Arch Clin Exp Ophthalmol. 2009;247:1205-1211.
32. Markwald RR, Krug EL, Mjaatvedt CH, Sinning AR. Endothelial formation of mesenchyme: Induction by an extracellular glycoprotein complex. In: Robertson R and Schneider MD, ed. Molecular biology of the cardiovascular system. 1990;311-319.
33. Feinberg RN, Noden DM. Experimental analysis of blood vessel development in the avian wing bud. Anat Rec. 1991;231:136-144.
34. Bergers G, Hanahan D. Modes of resistance to anti-angiogenic therapy. Nat Rev Cancer. 2008;8:592-603.
35. Furuya M, Yonemitsu Y, Aoki I, III. Angiogenesis: complexity of tumor vasculature and microenvironment. Curr Pharm Des. 2009;15: 1854-1867.
36. Willett CG, Boucher Y, di Tomaso E, Duda DG, Munn LL, Tong RT, Chung DC, Sahani DV, Kalva SP, Kozin SV, Mino M, Cohen KS, Scadden DT, Hartford AC, Fischman AJ, Clark JW, Ryan DP, Zhu AX, Blaszkowsky LS, Chen HX, Shellito PC, Lauwers GY, Jain RK. Direct evidence that the VEGF-specific antibody bevacizumab has antivascular effects in human rectal cancer. Nat Med. 2004;10:145-147. (Pubitemid 38524883)
37. Ma J, Waxman DJ. Combination of antiangiogenesis with chemotherapy for more effective cancer treatment. Mol Cancer Ther. 2008;7: 3670-3684.
38. Jain RK. Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science. 2005;307:58-62. (Pubitemid 40093472)
39. Tong RT, Boucher Y, Kozin SV, Winkler F, Hicklin DJ, Jain RK. Vascular normalization by vascular endothelial growth factor receptor 2 blockade induces a pressure gradient across the vasculature and improves drug penetration in tumors. Cancer Res. 2004;64:3731-3736. (Pubitemid 38697278)