nach oben

Angiogenesis

Erschienen in:

01.12.2008 | Original Paper

A role for planar cell polarity signaling in angiogenesis

verfasst von: Pasquale Cirone, Shengda Lin, Hilary L. Griesbach, Yi Zhang, Diane C. Slusarski, Craig M. Crews

Erschienen in: Angiogenesis | Ausgabe 4/2008

Einloggen, um Zugang zu erhalten

Abstract

The planar cell polarity (PCP) pathway is a highly conserved signaling cascade that coordinates both epithelial and axonal morphogenic movements during development. Angiogenesis also involves the growth and migration of polarized cells, although the mechanisms underlying their intercellular communication are poorly understood. Here, using cell culture assays, we demonstrate that inhibition of PCP signaling disrupts endothelial cell growth, polarity, and migration, all of which can be rescued through downstream activation of this pathway by expression of either Daam-1, Diversin or Inversin. Silencing of either Dvl2 or Prickle suppressed endothelial cell proliferation. Moreover, loss of p53 rescues endothelial cell growth arrest but not the migration inhibition caused by PCP disruption. In addition, we show that the zebrafish Wnt5 mutant (pipetail (ppt)), which has impaired PCP signaling, displays vascular developmental defects. These findings reveal a potential role for PCP signaling in the coordinated assembly of endothelial cells into vascular structures and have important implications for vascular remodeling in development and disease.

Nur mit Berechtigung zugänglich

Liebner S, Cavallaro U, Dejana E (2006) The multiple languages of endothelial cell-to-cell communication. Arterioscler Thromb Vasc Biol 26:1431–1438. doi:10.1161/01.ATV.0000218510.04541.5e PubMedCrossRef

Fanto M, McNeill H (2004) Planar polarity from flies to vertebrates. J Cell Sci 117:527–533. doi:10.1242/jcs.00973 PubMedCrossRef

Gong Y, Mo C, Fraser SE (2004) Planar cell polarity signalling controls cell division orientation during zebrafish gastrulation. Nature 430:689–693. doi:10.1038/nature02796 PubMedCrossRef

Heisenberg CP, Tada M, Rauch GJ, Saude L, Concha ML, Geisler R et al (2000) Silberblick/Wnt11 mediates convergent extension movements during zebrafish gastrulation. Nature 405:76–81. doi:10.1038/35011068 PubMedCrossRef

Myers DC, Sepich DS, Solnica-Krezel L (2002) Convergence and extension in vertebrate gastrulae: cell movements according to or in search of identity? Trends Genet 18:447–455. doi:10.1016/S0168-9525(02)02725-7 PubMedCrossRef

Wallingford JB, Vogeli KM, Harland RM (2001) Regulation of convergent extension in Xenopus by Wnt5a and Frizzled-8 is independent of the canonical Wnt pathway. Int J Dev Biol 45:225–227PubMed

Arevalo JC, Chao MV (2005) Axonal growth: where neurotrophins meet Wnts. Curr Opin Cell Biol 17:112–115. doi:10.1016/j.ceb.2005.01.004 PubMedCrossRef

Rosso SB, Sussman D, Wynshaw-Boris A, Salinas PC (2005) Wnt signaling through Dishevelled, Rac and JNK regulates dendritic development. Nat Neurosci 8:34–42. doi:10.1038/nn1374 PubMedCrossRef

Malbon CC, Wang HY (2006) Dishevelled: a mobile scaffold catalyzing development. Curr Top Dev Biol 72:153–166. doi:10.1016/S0070-2153(05)72002-0 PubMedCrossRef

10.

Habas R, Kato Y, He X (2001) Wnt/Frizzled activation of Rho regulates vertebrate gastrulation and requires a novel Formin homology protein Daam1. Cell 107:843–854. doi:10.1016/S0092-8674(01)00614-6 PubMedCrossRef

11.

Marlow F, Topczewski J, Sepich D, Solnica-Krezel L (2002) Zebrafish Rho kinase 2 acts downstream of Wnt11 to mediate cell polarity and effective convergence and extension movements. Curr Biol 12:876–884. doi:10.1016/S0960-9822(02)00864-3 PubMedCrossRef

12.

Yamanaka H, Moriguchi T, Masuyama N, Kusakabe M, Hanafusa H, Takada R et al (2002) JNK functions in the non-canonical Wnt pathway to regulate convergent extension movements in vertebrates. EMBO Rep 3:69–75. doi:10.1093/embo-reports/kvf008 PubMedCrossRef

13.

Wright M, Aikawa M, Szeto W, Papkoff J (1999) Identification of a Wnt-responsive signal transduction pathway in primary endothelial cells. Biochem Biophys Res Commun 263:384–388. doi:10.1006/bbrc.1999.1344 PubMedCrossRef

14.

Masckauchan TN, Agalliu D, Vorontchikhina M, Ahn A, Parmalee NL, Li CM et al (2006) Wnt5a signaling induces proliferation and survival of endothelial cells in vitro and expression of MMP-1 and Tie-2. Mol Biol Cell 17:5163–5172. doi:10.1091/mbc.E06-04-0320 PubMedCrossRef

15.

Cheng CW, Yeh JC, Fan TP, Smith SK, Charnock-Jones DS (2008) Wnt5a-mediated non-canonical Wnt signalling regulates human endothelial cell proliferation and migration. Biochem Biophys Res Commun 365:285–290PubMedCrossRef

16.

Zhang Y, Yeh JR, Mara A, Ju R, Hines JF, Cirone P et al (2006) A chemical and genetic approach to the mode of action of fumagillin. Chem Biol 13:1001–1009. doi:10.1016/j.chembiol.2006.07.010 PubMedCrossRef

17.

Yeh JR, Ju R, Brdlik CM, Zhang W, Zhang Y, Matyskiela ME et al (2006) Targeted gene disruption of methionine aminopeptidase 2 results in an embryonic gastrulation defect and endothelial cell growth arrest. Proc Natl Acad Sci USA 103:10379–10384. doi:10.1073/pnas.0511313103 PubMedCrossRef

18.

Zhang Y, Neo SY, Han J, Lin SC (2000) Dimerization choices control the ability of axin and dishevelled to activate c-Jun N-terminal kinase/stress-activated protein kinase. J Biol Chem 275:25008–25014. doi:10.1074/jbc.M002491200 PubMedCrossRef

19.

Yeh JR, Mohan R, Crews CM (2000) The antiangiogenic agent TNP-470 requires p53 and p21CIP/WAF for endothelial cell growth arrest. Proc Natl Acad Sci USA 97:12782–12787. doi:10.1073/pnas.97.23.12782 PubMedCrossRef

20.

Beardsley A, Fang K, Mertz H, Castranova V, Friend S, Liu J (2005) Loss of caveolin-1 polarity impedes endothelial cell polarization and directional movement. J Biol Chem 280:3541–3547. doi:10.1074/jbc.M409040200 PubMedCrossRef

21.

Zicha D, Dunn GA, Brown AF (1991) A new direct-viewing chemotaxis chamber. J Cell Sci 99(Pt 4):769–775PubMed

22.

Rousseau S, Houle F, Kotanides H, Witte L, Waltenberger J, Landry J et al (2000) Vascular endothelial growth factor (VEGF)-driven actin-based motility is mediated by VEGFR2 and requires concerted activation of stress-activated protein kinase 2 (SAPK2/p38) and geldanamycin-sensitive phosphorylation of focal adhesion kinase. J Biol Chem 275:10661–10672. doi:10.1074/jbc.275.14.10661 PubMedCrossRef

23.

Yamaguchi N, Anand-Apte B, Lee M, Sasaki T, Fukai N, Shapiro R et al (1999) Endostatin inhibits VEGF-induced endothelial cell migration and tumor growth independently of zinc binding. EMBO J 18:4414–4423. doi:10.1093/emboj/18.16.4414 PubMedCrossRef

24.

Nicosia RF, Ottinetti A (1990) Modulation of microvascular growth and morphogenesis by reconstituted basement membrane gel in three-dimensional cultures of rat aorta: a comparative study of angiogenesis in matrigel, collagen, fibrin, and plasma clot. In Vitro Cell Dev Biol 26:119–128. doi:10.1007/BF02624102 PubMedCrossRef

25.

Borodovsky A, Ovaa H, Kolli N, Gan-Erdene T, Wilkinson KD, Ploegh HL et al (2002) Chemistry-based functional proteomics reveals novel members of the deubiquitinating enzyme family. Chem Biol 9:1149–1159. doi:10.1016/S1074-5521(02)00248-X PubMedCrossRef

26.

Yoshida A, Anand-Apte B, Zetter BR (1996) Differential endothelial migration and proliferation to basic fibroblast growth factor and vascular endothelial growth factor. Growth Factors 13:57–64. doi:10.3109/08977199609034566 PubMedCrossRef

27.

Grande-Garcia A, Echarri A, de Rooij J, Alderson NB, Waterman-Storer CM, Valdivielso JM et al (2007) Caveolin-1 regulates cell polarization and directional migration through Src kinase and Rho GTPases. J Cell Biol 177:683–694. doi:10.1083/jcb.200701006 PubMedCrossRef

28.

Parat MO, Anand-Apte B, Fox PL (2003) Differential caveolin-1 polarization in endothelial cells during migration in two and three dimensions. Mol Biol Cell 14:3156–3168. doi:10.1091/mbc.E02-11-0761 PubMedCrossRef

29.

Sheldahl LC, Slusarski DC, Pandur P, Miller JR, Kuhl M, Moon RT (2003) Dishevelled activates Ca²⁺flux, PKC, and CamKII in vertebrate embryos. J Cell Biol 161:769–777. doi:10.1083/jcb.200211094 PubMedCrossRef

30.

Boutros M, Paricio N, Strutt DI, Mlodzik M (1998) Dishevelled activates JNK and discriminates between JNK pathways in planar polarity and wingless signaling. Cell 94:109–118. doi:10.1016/S0092-8674(00)81226-X PubMedCrossRef

31.

Tada M, Smith JC (2000) Xwnt11 is a target of Xenopus Brachyury: regulation of gastrulation movements via Dishevelled, but not through the canonical Wnt pathway. Development 127:2227–2238PubMed

32.

Kusaka M, Sudo K, Fujita T, Marui S, Itoh F, Ingber D et al (1991) Potent anti-angiogenic action of AGM-1470: comparison to the fumagillin parent. Biochem Biophys Res Commun 174:1070–1076. doi:10.1016/0006-291X(91)91529-L PubMedCrossRef

33.

Kishida S, Yamamoto H, Hino S, Ikeda S, Kishida M, Kikuchi A (1999) DIX domains of Dvl and axin are necessary for protein interactions and their ability to regulate beta-catenin stability. Mol Cell Biol 19:4414–4422PubMed

34.

Li L, Yuan H, Xie W, Mao J, Caruso AM, McMahon A et al (1999) Dishevelled proteins lead to two signaling pathways. Regulation of LEF-1 and c-Jun N-terminal kinase in mammalian cells. J Biol Chem 274:129–134. doi:10.1074/jbc.274.1.129 PubMedCrossRef

35.

Moriguchi T, Kawachi K, Kamakura S, Masuyama N, Yamanaka H, Matsumoto K et al (1999) Distinct domains of mouse dishevelled are responsible for the c-Jun N-terminal kinase/stress-activated protein kinase activation and the axis formation in vertebrates. J Biol Chem 274:30957–30962. doi:10.1074/jbc.274.43.30957 PubMedCrossRef

36.

Park TJ, Gray RS, Sato A, Habas R, Wallingford JB (2005) Subcellular localization and signaling properties of dishevelled in developing vertebrate embryos. Curr Biol 15:1039–1044. doi:10.1016/j.cub.2005.04.062 PubMedCrossRef

37.

Pan WJ, Pang SZ, Huang T, Guo HY, Wu D, Li L (2004) Characterization of function of three domains in dishevelled-1: DEP domain is responsible for membrane translocation of dishevelled-1. Cell Res 14:324–330. doi:10.1038/sj.cr.7290232 PubMedCrossRef

38.

Farinelle S, Malonne H, Chaboteaux C, Decaestecker C, Dedecker R, Gras T et al (2000) Characterization of TNP-470-induced modifications to cell functions in HUVEC and cancer cells. J Pharmacol Toxicol Methods 43:15–24. doi:10.1016/S1056-8719(00)00080-0 PubMedCrossRef

39.

Schwarz-Romond T, Asbrand C, Bakkers J, Kuhl M, Schaeffer HJ, Huelsken J et al (2002) The ankyrin repeat protein Diversin recruits Casein kinase Iepsilon to the beta-catenin degradation complex and acts in both canonical Wnt and Wnt/JNK signaling. Genes Dev 16:2073–2084. doi:10.1101/gad.230402 PubMedCrossRef

40.

Tissir F, Bar I, Goffinet AM, Lambert De Rouvroit C (2002) Expression of the ankyrin repeat domain 6 gene (Ankrd6) during mouse brain development. Dev Dyn 224:465–469. doi:10.1002/dvdy.10126 PubMedCrossRef

41.

Simons M, Gloy J, Ganner A, Bullerkotte A, Bashkurov M, Kronig C et al (2005) Inversin, the gene product mutated in nephronophthisis type II, functions as a molecular switch between Wnt signaling pathways. Nat Genet 37:537–543. doi:10.1038/ng1552 PubMedCrossRef

42.

Moeller H, Jenny A, Schaeffer HJ, Schwarz-Romond T, Mlodzik M, Hammerschmidt M et al (2006) Diversin regulates heart formation and gastrulation movements in development. Proc Natl Acad Sci USA 103:15900–15905. doi:10.1073/pnas.0603808103 PubMedCrossRef

43.

De Calisto J, Araya C, Marchant L, Riaz CF, Mayor R (2005) Essential role of non-canonical Wnt signalling in neural crest migration. Development 132:2587–2597. doi:10.1242/dev.01857 PubMedCrossRef

44.

Park M, Moon RT (2002) The planar cell-polarity gene stbm regulates cell behaviour and cell fate in vertebrate embryos. Nat Cell Biol 4:20–25. doi:10.1038/ncb716 PubMedCrossRef

45.

Habas R, Dawid IB, He X (2003) Coactivation of Rac and Rho by Wnt/Frizzled signaling is required for vertebrate gastrulation. Genes Dev 17:295–309. doi:10.1101/gad.1022203 PubMedCrossRef

46.

Kilian B, Mansukoski H, Barbosa FC, Ulrich F, Tada M, Heisenberg CP (2003) The role of Ppt/Wnt5 in regulating cell shape and movement during zebrafish gastrulation. Mech Dev 120:467–476. doi:10.1016/S0925-4773(03)00004-2 PubMedCrossRef

47.

Moon RT, Campbell RM, Christian JL, McGrew LL, Shih J, Fraser S (1993) Xwnt-5A: a maternal Wnt that affects morphogenetic movements after overexpression in embryos of Xenopus laevis. Development 119:97–111PubMed

48.

Liao G, Tao Q, Kofron M, Chen JS, Schloemer A, Davis RJ et al (2006) Jun NH2-terminal kinase (JNK) prevents nuclear {beta}-catenin accumulation and regulates axis formation in Xenopus embryos. Proc Natl Acad Sci USA 103:16313–16318. doi:10.1073/pnas.0602557103 PubMedCrossRef

49.

Kragh M, Hjarnaa PJ, Bramm E, Binderup L (2004) A versatile in vivo chamber angiogenesis assay for measuring anti-angiogenic activity in mice. Oncol Rep 11:303–307PubMed

50.

Goto T, Davidson L, Asashima M, Keller R (2005) Planar cell polarity genes regulate polarized extracellular matrix deposition during frog gastrulation. Curr Biol 15:787–793. doi:10.1016/j.cub.2005.03.040 PubMedCrossRef

51.

Na J, Lykke-Andersen K, Torres Padilla ME, Zernicka-Goetz M (2007) Dishevelled proteins regulate cell adhesion in mouse blastocyst and serve to monitor changes in Wnt signaling. Dev Biol 302:40–49. doi:10.1016/j.ydbio.2006.08.036 PubMedCrossRef

52.

Witzel S, Zimyanin V, Carreira-Barbosa F, Tada M, Heisenberg CP (2006) Wnt11 controls cell contact persistence by local accumulation of Frizzled 7 at the plasma membrane. J Cell Biol 175:791–802. doi:10.1083/jcb.200606017 PubMedCrossRef

53.

Keller R, Shih J, Sater AK, Moreno C (1992) Planar induction of convergence and extension of the neural plate by the organizer of Xenopus. Dev Dyn 193:218–234PubMed

54.

Hamblet NS, Lijam N, Ruiz-Lozano P, Wang J, Yang Y, Luo Z et al (2002) Dishevelled 2 is essential for cardiac outflow tract development, somite segmentation and neural tube closure. Development 129:5827–5838. doi:10.1242/dev.00164 PubMedCrossRef

55.

Lawson ND, Weinstein BM (2002) In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev Biol 248:307–318. doi:10.1006/dbio.2002.0711 PubMedCrossRef

56.

Rauch GJ, Hammerschmidt M, Blader P, Schauerte HE, Strahle U, Ingham PW et al (1997) Wnt5 is required for tail formation in the zebrafish embryo. Cold Spring Harb Symp Quant Biol 62:227–234PubMed

57.

Isogai S, Horiguchi M, Weinstein BM (2001) The vascular anatomy of the developing zebrafish: an atlas of embryonic and early larval development. Dev Biol 230:278–301. doi:10.1006/dbio.2000.9995 PubMedCrossRef

58.

Shaw KM, Castranova DA, Pham VN, Kamei M, Kidd KR, Lo BD et al (2006) Fused-somites-like mutants exhibit defects in trunk vessel patterning. Dev Dyn 235:1753–1760. doi:10.1002/dvdy.20814 PubMedCrossRef

59.

Blankesteijn WM, van Gijn ME, Essers-Janssen YP, Daemen MJ, Smits JF (2000) Beta-catenin, an inducer of uncontrolled cell proliferation and migration in malignancies, is localized in the cytoplasm of vascular endothelium during neovascularization after myocardial infarction. Am J Pathol 157:877–883PubMed

60.

Goodwin AM, D’Amore PA (2002) Wnt signaling in the vasculature. Angiogenesis 5:1–9. doi:10.1023/A:1021563510866 PubMedCrossRef

61.

Goodwin AM, Sullivan KM, D’Amore PA (2006) Cultured endothelial cells display endogenous activation of the canonical Wnt signaling pathway and express multiple ligands, receptors, and secreted modulators of Wnt signaling. Dev Dyn 235:3110–3120. doi:10.1002/dvdy.20939 PubMedCrossRef

62.

Hanai J, Gloy J, Karumanchi SA, Kale S, Tang J, Hu G et al (2002) Endostatin is a potential inhibitor of Wnt signaling. J Cell Biol 158:529–539. doi:10.1083/jcb.200203064 PubMedCrossRef

63.

Masckauchan TN, Shawber CJ, Funahashi Y, Li CM, Kitajewski J (2005) Wnt/beta-catenin signaling induces proliferation, survival and interleukin-8 in human endothelial cells. Angiogenesis 8:43–51. doi:10.1007/s10456-005-5612-9 PubMedCrossRef

64.

Yano H, Hara A, Takenaka K, Nakatani K, Shinoda J, Shimokawa K et al (2000) Differential expression of beta-catenin in human glioblastoma multiforme and normal brain tissue. Neurol Res 22:650–656PubMed

65.

Ishikawa T, Tamai Y, Zorn AM, Yoshida H, Seldin MF, Nishikawa S et al (2001) Mouse Wnt receptor gene Fzd5 is essential for yolk sac and placental angiogenesis. Development 128:25–33PubMed

66.

Qian D, Jones C, Rzadzinska A, Mark S, Zhang X, Steel KP et al (2007) Wnt5a functions in planar cell polarity regulation in mice. Dev Biol 306:121–133. doi:10.1016/j.ydbio.2007.03.011 PubMedCrossRef

67.

Yamaguchi TP, Bradley A, McMahon AP, Jones S (1999) A Wnt5a pathway underlies outgrowth of multiple structures in the vertebrate embryo. Development 126:1211–1223PubMed

68.

Huang S, Chen CS, Ingber DE (1998) Control of cyclin D1, p27(Kip1), and cell cycle progression in human capillary endothelial cells by cell shape and cytoskeletal tension. Mol Biol Cell 9:3179–3193PubMed

69.

Mammoto A, Huang S, Moore K, Oh P, Ingber DE (2004) Role of RhoA, mDia, and ROCK in cell shape-dependent control of the Skp2–p27kip1 pathway and the G1/S transition. J Biol Chem 279:26323–26330. doi:10.1074/jbc.M402725200 PubMedCrossRef

70.

Zhang Y, Griffith EC, Sage J, Jacks T, Liu JO (2000) Cell cycle inhibition by the anti-angiogenic agent TNP-470 is mediated by p53 and p21WAF1/CIP1. Proc Natl Acad Sci USA 97:6427–6432. doi:10.1073/pnas.97.12.6427 PubMedCrossRef

71.

Witmer AN, Vrensen GF, Van Noorden CJ, Schlingemann RO (2003) Vascular endothelial growth factors and angiogenesis in eye disease. Prog Retin Eye Res 22:1–29. doi:10.1016/S1350-9462(02)00043-5 PubMedCrossRef

72.

Carmeliet P (2005) Angiogenesis in life, disease and medicine. Nature 438:932–936. doi:10.1038/nature04478 PubMedCrossRef

73.

Ferrara N, Kerbel RS (2005) Angiogenesis as a therapeutic target. Nature 438:967–974. doi:10.1038/nature04483 PubMedCrossRef

74.

Folkman J (2006) Angiogenesis. Annu Rev Med 57:1–18. doi:10.1146/annurev.med.57.121304.131306 PubMedCrossRef

Titel: A role for planar cell polarity signaling in angiogenesis
verfasst von: Pasquale Cirone
Shengda Lin
Hilary L. Griesbach
Yi Zhang
Diane C. Slusarski
Craig M. Crews
Publikationsdatum: 01.12.2008
Verlag: Springer Netherlands
Erschienen in: Angiogenesis / Ausgabe 4/2008
Print ISSN: 0969-6970
Elektronische ISSN: 1573-7209
DOI: https://doi.org/10.1007/s10456-008-9116-2

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

^{Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag}

Kostenlos registrieren

Neu im Fachgebiet Innere Medizin

Echinokokkose medikamentös behandeln oder operieren?

06.05.2024 DCK 2024 Kongressbericht

Die Therapie von Echinokokkosen sollte immer in spezialisierten Zentren erfolgen. Eine symptomlose Echinokokkose kann – egal ob von Hunde- oder Fuchsbandwurm ausgelöst – konservativ erfolgen. Wenn eine Op. nötig ist, kann es sinnvoll sein, vorher Zysten zu leeren und zu desinfizieren.

Umsetzung der POMGAT-Leitlinie läuft

03.05.2024 DCK 2024 Kongressbericht

Seit November 2023 gibt es evidenzbasierte Empfehlungen zum perioperativen Management bei gastrointestinalen Tumoren (POMGAT) auf S3-Niveau. Vieles wird schon entsprechend der Empfehlungen durchgeführt. Wo es im Alltag noch hapert, zeigt eine Umfrage in einem Klinikverbund.

Proximale Humerusfraktur: Auch 100-Jährige operieren?

01.05.2024 DCK 2024 Kongressbericht

Mit dem demographischen Wandel versorgt auch die Chirurgie immer mehr betagte Menschen. Von Entwicklungen wie Fast-Track können auch ältere Menschen profitieren und bei proximaler Humerusfraktur können selbst manche 100-Jährige noch sicher operiert werden.

Die „Zehn Gebote“ des Endokarditis-Managements

30.04.2024 Endokarditis Leitlinie kompakt

Worauf kommt es beim Management von Personen mit infektiöser Endokarditis an? Eine Kardiologin und ein Kardiologe fassen die zehn wichtigsten Punkte der neuen ESC-Leitlinie zusammen.

Update Innere Medizin

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.

Newsletter bestellen

Springer Medizin

Abstract

Bitte loggen Sie sich ein, um Zugang zu diesem Inhalt zu erhalten

Weitere Artikel der Ausgabe 4/2008

The chick embryo chorioallantoic membrane as a model to study tumor metastasis

Circulating and imaging markers for angiogenesis

A nuclease-resistant RNA aptamer specifically inhibits angiopoietin-1-mediated Tie2 activation and function

PPARγ ligands, rosiglitazone and pioglitazone, inhibit bFGF- and VEGF-mediated angiogenesis

Angiogenic response to extracorporeal shock wave treatment in murine skin isografts