Ups and downs of guided vessel sprouting: The role of polarity

Physiology

Volumn 26, Issue 5, 2011, Pages 326-333

  Lee, Christina Y ^a   Bautch, Victoria L ^a,b  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENESIS; ANIMAL; ARTICLE; BLOOD VESSEL; CELL POLARITY; ENDOTHELIUM CELL; PHYSIOLOGY;

ANIMALS; BLOOD VESSELS; CELL POLARITY; ENDOTHELIAL CELLS; NEOVASCULARIZATION, PHYSIOLOGIC;

EID: 80054764781     PISSN: 15489213     EISSN: 15489221     Source Type: Journal    
DOI: 10.1152/physiol.00018.2011     Document Type: Article

References (83)

1. Aase K, Ernkvist M, Ebarasi L, Jakobsson L, Majumdar A, Yi C, Birot O, Ming Y, Kvanta A, Edholm D, Aspenstrom P, Kissil J, Claesson-Welsh L, Shimono A, Holmgren L. Angiomotin regulates endothelial cell migration during embryonic angiogenesis. Genes Dev 21: 2055-2068, 2007.
2. Adams RH, Alitalo K. Molecular regulation of angiogenesis and lymphangiogenesis. Nat Rev Mol Cell Biol 8: 464-478, 2007.
3. Adler PN. Planar signaling and morphogenesis in Drosophila. Dev Cell 2: 525-535, 2002.
4. Baluk P, Hashizume H, McDonald DM. Cellular abnormalities of blood vessels as targets in cancer. Curr Opin Genet Dev 15: 102-111, 2005.
5. Bayless KJ, Davis GE. Microtubule depolymerization rapidly collapses capillary tube networks in vitro and angiogenic vessels in vivo through the small GTPase Rho. J Biol Chem 279: 11686-11695, 2004.
6. Bayless KJ, Davis GE. The Cdc42 and Rac1 GTPases are required for capillary lumen formation in three-dimensional extracellular matrices. J Cell Sci 115: 1123-1136, 2002.
7. Beardsley A, Fang K, Mertz H, Castranova V, Friend S, Liu J. Loss of caveolin-1 polarity impedes endothelial cell polarization and directional movement. J Biol Chem 280: 3541-3547, 2005.
8. Bentley K, Mariggi G, Gerhardt H, Bates PA. Tipping the balance: robustness of tip cell selection, migration and fusion in angiogenesis. PLoS Comp Biol 5: e1000549, 2009.
9. Broussard JA, Webb DJ, Kaverina I. Asymmetric focal adhesion disassembly in motile cells. Curr Opin Cell Biol 20: 85-90, 2008.
10. Bryan BA, D'Amore PA. What tangled webs they weave: Rho-GTPase control of angiogenesis. Cell Mol Life Sci 64: 2053-2065, 2007.
11. Carmeliet P. Angiogenesis in life, disease and medicine. Nature 438: 932-936, 2005.
12. Carmeliet P, Ferreira V, Breier G, Pollefeyt S, Kieckens L, Gertsenstein M, Fahrig M, Vandenhoeck A, Harpal K, Eberhardt C, Declercq C, Pawling J, Moons L, Collen D, Risau W, Nagy A. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 380: 435-439, 1996.
13. Chappell JC, Bautch VL. Vascular development: genetic mechanisms and links to vascular disease. Curr Topic Dev Biol 90: 43-72, 2010.
14. Chappell JC, Taylor SM, Ferrara N, Bautch VL. Local guidance of emerging vessel sprouts requires soluble Flt-1. Dev Cell 17: 377-386, 2009.
15. Cirone P, Lin S, Griesbach HL, Zhang Y, Slusarski DC, Crews CM. A role for planar cell polarity signaling in angiogenesis. Angiogenesis 11: 347-360, 2008.
16. Coultas L, Chawengsaksophak K, Rossant J. Endothelial cells and VEGF in vascular development. Nature 438: 937-945, 2005.
17. De Smet F, Segura I, De Bock K, Hohensinner PJ, Carmeliet P. Mechanisms of vessel branching: filopodia on endothelial tip cells lead the way. Arterioscler Thromb Vasc Biol 29: 639-649, 2009.
18. del Toro R, Prahst C, Mathivet T, Siegfried G, Kaminker JS, Larrivee B, Breant C, Duarte A, Takakura N, Fukamizu A, Penninger J, Eichmann A. Identification and functional analysis of endothelial tip cell-enriched genes. Blood 116: 4025-4033, 2010.
19. Dumont DJ, Jussila L, Taipale J, Lymboussaki A, Mustonen T, Pajusola K, Breitman M, Alitalo K. Cardiovascular failure in mouse embryos deficient in VEGF receptor-3. Science 282: 946-949, 1998.
20. Estrach S, Cailleteau L, Franco CA, Gerhardt H, Stefani C, Lemichez E, Gagnoux-Palacios L, Meneguzzi G, Mettouchi A. Laminin-binding integrins induce Dll4 expression and Notch signaling in endothelial cells. Circ Res 109: 172-182, 2011.
21. Etienne-Manneville S, Hall A. Cell polarity: Par6, aPKC and cytoskeletal crosstalk. Curr Opin Cell Biol 15: 67-72, 2003.
22. Fantin A, Vieira JM, Gestri G, Denti L, Schwarz Q, Prykhozhij S, Peri F, Wilson SW, Ruhrberg C. Tissue macrophages act as cellular chaperones for vascular anastomosis downstream of VEGF-mediated endothelial tip cell induction. Blood 116: 829-840, 2010.
23. Ferrara N, Carver-Moore K, Chen H, Dowd M, Lu L, O'Shea KS, Powell-Braxton L, Hillan KJ, Moore MW. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 380: 439-442, 1996.
24. Ferrara N, Gerber HP, LeCouter J. The biology of VEGF and its receptors. Nat Med 9: 669-676, 2003.
25. Fong GH, Rossant J, Gertsenstein M, Breitman ML. Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature 376: 66-70, 1995.
26. Gardel ML, Schneider IC, Aratyn-Schaus Yvonne, Waterman CM. Mechanical integration of actin and adhesion dynamics in cell migration. Ann Rev Cell Dev Biol 26: 315-333, 2010.
27. 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 161: 1163-1177, 2003.
28. Gotlieb AI, May LM, Subrahmanyan L, Kalnins VI. Distribution of microtubule organizing centers in migrating sheets of endothelial cells. J Cell Biol 91: 589-594, 1981.
29. Gridley T. Notch signaling in vascular development and physiology. Development 134: 2709-2718, 2007.
30. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 144: 646-674, 2011.
31. Hartnett ME, Martiniuk D, Byfield G, Geisen P, Zeng G, Bautch VL. Neutralizing VEGF decreases tortuosity and alters endothelial cell division orientation in arterioles and veins in a rat model of ROP: relevance to plus disease. Invest Ophthalmol Vis Sci 49: 3107-3114, 2008.
32. Hellstrom M, Phng LK, Hofmann JJ, Wallgard E, Coultas L, Lindblom P, Alva J, Nilsson AK, Karlsson L, Gaiano N, Yoon K, Rossant J, Iruela-Arispe ML, Kalen M, Gerhardt H, Betsholtz C. 2007. Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis. Nature 445: 776-780, 2007.
33. Hiratsuka S, Minowa O, Kuno J, Noda T, Shibuya M. Flt-1 lacking the tyrosine kinase domain is sufficient for normal development and angiogenesis in mice. Proc Natl Acad Sci USA 95: 9349-9354, 1998.
34. Hofmann JJ, Iruela-Arispe ML. Notch signaling in blood vessels: who is talking to whom about what? Circ Res 100: 1556-1568, 2007.
35. Holderfield MT, Hughes CCW. Crosstalk between vascular endothelial growth factor, Notch, and transforming growth factor-beta in vascular morphogenesis. Circ Res 102: 637-652, 2008.
36. Iden S, Rehder D, August B, Suzuki A, Wolburg-Buchholz K, Wolburg H, Ohno S, Behrens J, Vestweber D, Ebnet K. A distinct PAR complex associates physically with VE-cadherin in vertebrate endothelial cells. EMBO Rpt 7: 1239-1246, 2006.
37. Iruela-Arispe ML, Davis GE. Cellular and molecular mechanisms of vascular lumen formation. Dev Cell 16: 222-231, 2009.
38. 2+ wave initiation move with caveolae to the trailing edge of migrating cells. J Cell Sci 115: 475-484, 2002.
39. Jain RK. Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science 307: 58-62, 2005.
40. Jakobsson L, Bentley K, Gerhardt H. VEGFRs and Notch: a dynamic collaboration in vascular patterning. Biochem Soc Trans 37: 1233-1236, 2009.
41. Jakobsson L, Franco CA, Bentley K, Collins RT, Ponsioen B, Aspalter IM, Rosewell I, Busse M, Thurston G, Medvinsky A, Schulte-Merker S, Gerhardt H. Endothelial cells dynamically compete for the tip cell position during angiogenic sprouting. Nat Cell Biol 12: 943-953, 2010.
42. Ju R, Cirone P, Lin S, Griesbach H, Slusarski DC, Crews CM. Activation of the planar cell polarity formin DAAM1 leads to inhibition of endothelial cell proliferation, migration, and angiogenesis. Proc Natl Acad Sci USA 107: 6906-6911, 2010.
43. Kappas NC, Zeng G, Chappell JC, Kearney JB, Hazarika S, Kallianos KG, Patterson C, Annex BH, Bautch VL. The VEGF receptor Flt-1 spatially modulates Flk-1 signaling and blood vessel branching. J Cell Biol 181: 847-858, 2008.
44. Kendall RL, Thomas KA. Inhibition of vascular endothelial cell growth factor activity by an endogenously encoded soluble receptor. Proc Natl Acad Sci USA 90: 10705-10709, 1993.
45. Kerbel RS. Tumor angiogenesis. N Engl J Med 358: 2039-2049, 2008.
46. Kiosses WB, McKee NH, Kalnins VI. The distribution of centrosomes in endothelial cells of the rat aorta and inferior vena cava. Artery 22: 251-265, 1997.
47. Koh W, Mahan RD, Davis GE. Cdc42- and Rac1- mediated endothelial lumen formation requires Pak2, Pak4 and Par3, and PKC-dependent signaling. J Cell Sci 121: 989-1001, 2008.
48. Krueger J, Liu D, Scholz K, Zimmer A, Shi Y, Klein C, Siekmann A, Schulte-Merker S, Cudmore M, Ahmed A, le Noble F. Flt1 acts as a negative regulator of tip cell formation and branching morphogenesis in the zebrafish embryo. Development 138: 2111-2120, 2011.
49. Lampugnani MG, Orsenigo F, Rudini N, Maddaluno L, Boulday G, Chapon F, Dejana E. CCM1 regulates vascular-lumen organization by inducing endothelial polarity. J Cell Sci 123: 1073-1180, 2010.
50. Lohela M, Bry M, Tammela T, Alitalo K. VEGFs and receptors involved in angiogenesis versus lymphangiogenesis. Curr Opin Cell Biol 21: 154-165, 2009.
51. Lohela M, Heloter H, Haiko P, Dumont DJ, Alitalo K. Transgenic induction of vascular endothelial growth factor-C is strongly angiogenic in mouse embryos but leads to persistent lymphatic hyperplasia in adult tissues. Am J Pathol 173: 1891-1901, 2008.
52. Marchetti V, Krohne TU, Friedlander DF, Friedlander M. Stemming vision loss with stem cells. J Clin Invest 120: 3012-3021, 2010.
53. Matsumoto T, Schiller P, Dieterich LC, Bahram F, Iribe Y, Hellman U, Wikner C, Chan G, Claesson-Welsh L, Dimberg A. Ninein is expressed in the cytoplasm of angiogenic tip-cells and regulates tubular morphogenesis of endothelial cells. Arterioscler Thromb Vasc Biol 28: 2123-2130, 2008.
54. Mazzone M, Dettori D, Leite de Olivera R, Loges S, Schmidt T, Jonckx B, Tian YM, Lanahan AA, Pollard P, Ruiz de Almodovar C, De Smet F, Vinckier S, Aragones J, Luttun A, Wyns S, JB, Pisacane A, Gallez B, Lampugnani M, Dejana E, Simons M, Ratcliffe P, Maxwell P, Carmeliet P. Heterozygous deficiency of PHD2 restores tumor oxygenation and inhibits metastasis via endothelial normalization. Cell 136: 839-851, 2009.
55. McCue S, Dajnowiec D, Xu F, Zhang M, Jackson MR, Langille BL. Shear stress regulates forward and reverse planar cell polarity of vascular endothelium in vivo and in vitro. Circ Res 98: 939-946, 2006.
56. Nemere I, Kupfer A, Singer SJ. Reorientation of the Golgi apparatus and the microtubule-organizing center inside macrophages subjected to a chemotactic gradient. Cell Motil 5: 17-29, 1985.
57. Olsson AK, Dimberg A, Kreuger J, Claesson- Welsh L. VEGF receptor signalling: in control of vascular function. Nat Rev Mol Cell Biol 7: 359-371, 2006.
58. Parat MO, Anand-Apte B, Fox PL. Differential caveolin-1 polarization in endothelial cells during migration in two and three dimensions. Mol Biol Cell 14: 3156-3168, 2003.
59. Phng LK, Gerhardt H. Angiogenesis: a team effort coordinated by notch. Dev Cell 16: 196-208, 2009.
60. Risau W. Mechanisms of angiogenesis. Nature 386: 671-674, 1997.
61. Roberts DM, Kearney JB, Johnson JH, Rosenberg MP, Kumar R, Bautch VL. The vascular endothelial growth factor (VEGF) receptor Flt-1 (VEGFR-1) modulates Flk-1 (VEGFR-2) signaling during blood vessel formation. Am J Pathol 164: 1531-1535, 2004.
62. Roca C, Adams RH. Regulation of vascular morphogenesis by Notch signaling. Genes Dev 21: 2511-2524, 2007.
63. Rogers KA, McKee NH, Kalnins VI. Preferential orientation of centrioles toward the heart in endothelial cells of major blood vessels is reestablished after reversal of a segment. Proc Natl Acad Sci USA 82: 3272-3276, 1985.
64. Ruhrberg C, Gerhardt H, Golding M, Watson R, Ioannidou S, Fujisawa H, Betsholtz C, Shima DT. Spatially restricted patterning cues provided by heparin-binding VEGF-A control blood vessel branching morphogenesis. Genes Dev 16: 2684-2698, 2002.
65. Sainson RC, Aoto J, Nakatsu MN, Holderfield M, Conn E, Koller E, Hughes CC. Cell-autonomous notch signaling regulates endothelial cell branching and proliferation during vascular tubulogenesis. FASEB J 19: 1027-1029, 2005.
66. Shalaby F, Rossant J, Yamaguchi TP, Gertsenstein M, Wu XF, Breitman ML, Schuh AC. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 376: 62-66, 1995.
67. Shawber CJ, Kitajewski J. Notch function in the vasculature: insights from zebrafish, mouse and man. Bioessays 26: 225-234, 2004.
68. Siekmann AF, Covassin L, Lawson ND. Modulation of VEGF signalling output by the Notch pathway. Bioessays 30: 303-313, 2008.
69. Simons M, Mlodzik M. Planar cell polarity signaling: from fly development to human disease. Ann Rev Genet 42: 517-540, 2008.
70. Stahl A, Krohne TU, Sapieha P, Chen J, Hellstrom A, Chew E, Holz FG, Smith LEH. Lipid metabolites in the pathogenesis and treatment of neovascular eye disease. Brit J Ophthalmol. In press.
71. Strasser GA, Kaminker JS, Tessier-Lavigne M. Microarray analysis of retinal endothelial tip cells identifies CXCR4 as a mediator of tip cell morphology and branching. Blood 115: 5102-5110, 2010.
72. Strilic B, Eglinger J, Krieg M, Zeeb M, Axnick J, Babil P, Miller DJ, Lammert E. Electrostatic cellsurface repulsion initiates lumen formation in developing blood vessels. Curr Biol 20: 2003-2009, 2010.
73. Strilic B, Kucera T, Eglinger J, Hughes MR, Mc- Nagny KM, Tsukita S, Dejana E, Ferrara N, Lammert E. The molecular basis of vascular lumen formation in the developing mouse aorta. Dev Cell 17: 505-515, 2009.
74. Suchting S, Freitas C, le Noble F, Benedito R, Breant C, Duarte A, Eichmann A. The Notch ligand delta-like 4 negatively regulates endothelial tip cell formation and vessel branching. Proc Natl Acad Sci USA 104: 3225-3230, 2007.
75. Tammela T, Zarkada G, Wallgard E, Murtomaki A, Suchting S, Wirzenius M, Waltari M, Hellstrom M, Schomber T, Peltonen R, Freitas C, Duarte A, Isoniemi H, Laakkonen P, Christofori G, Yla-Herttuala S, Shibuya M, Pytowski B, Eichmann A, Betsholtz C, Alitalo K. Blocking VEGFR-3 suppresses angiogenic sprouting and vascular network formation. Nature 454: 656-660, 2008.
76. Tzima E, Kiosses WB, del Pozo MA, Schwartz MA. Localized cdc42 activation, detected using a novel assay, mediates microtubule organizing center positioning in endothelial cells in response to fluid shear stress. J Biol Chem 278: 31020-31023, 2003.
77. Wang Y, Nathans J. 2007. Tissue/planar cell polarity in vertebrates: new insights and new questions. Development 134: 647-658, 2007.
78. Xu K, Sacharidou A, Fu S, Chong DC, Skaug B, Chen ZJ, Davis GE, Cleaver O. Blood vessel tubulogenesis requires Rasip1 regulation of GTPase signaling. Dev Cell 20: 526-539, 2011.
79. Yana I, Sagara H, Takaki S, Takatsu K, Nakamura K, Nakao K, Katsuki M, Taniguchi S, Aoki T, Sato H, Weiss SJ, Seiki M. Crosstalk between neovessels and mural cells directs the site-specific expression of MT1-MMP to endothelial tip cells. J Cell Sci 120: 1607-1614, 2007.
80. Zallen JA. Planar polarity and tissue morphogenesis. Cell 129: 1051-1063, 2007.
81. Zeng G, Taylor SM, McColm JR, Kappas NC, Kearney JB, Williams LH, Hartnett ME, Bautch VL. Orientation of endothelial cell division is regulated by VEGF signaling during blood vessel formation. Blood 109: 1345-1152, 2007.
82. Zheng Y, Vertuani S, Nystrom S, Audebert S, Meijer I, Tegnebratt T, Borg JP, Uhlen P, Majumdar A, Holmgren L. Angiomotin-like protein 1 controls endothelial polarity and junction stability during sprouting angiogenesis. Circ Res 105: 260-270, 2009.
83. Zovein AC, Luque A, Turlo KA, Hofmann JJ, Yee KM, Becker MS, Fassler R, Mellman I, Lane TF, Iruela-Arispe ML. Beta1 integrin establishes endothelial cell polarity and arteriolar lumen formation via a Par3-dependent mechanism. Dev Cell 18: 39-51, 2010.