The Orphan Receptor Tie1 Controls Angiogenesis and Vascular Remodeling by Differentially Regulating Tie2 in Tip and Stalk Cells

Cell Reports

Volumn 12, Issue 11, 2015, Pages 1761-1773

  Savant, Soniya ^a,b,f   La Porta, Silvia ^a   Budnik, Annika ^a   Busch, Katrin ^a   Hu, Junhao ^a,g   Tisch, Nathalie ^b   Korn, Claudia ^a   Valls, Aida Freire ^a,b   Benest, Andrew V ^a,h   Terhardt, Dorothee ^a   Qu, Xianghu ^c   Adams, Ralf H ^d,e   Baldwin, H Scott ^c   Ruiz de Almodóvar, Carmen ^b   Rodewald, Hans Reimer ^a   Augustin, Hellmut G ^a,b  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d MAX PLANCK INSTITUTE FOR MOLECULAR BIOMEDICINE   (Germany)

^e UNIVERSITY OF MÜNSTER   (Germany)

^f KAROLINSKA INSTITUTE   (Sweden)

^g INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^h UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOPOIETIN 1; ANGIOPOIETIN RECEPTOR; TIE 1 RECEPTOR;

ADULT; ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL FUNCTION; CELL SURVIVAL; CELLS BY BODY ANATOMY; CONTROLLED STUDY; ENDOTHELIUM CELL; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RETINA BLOOD VESSEL; SHEAR STRESS; SIGNAL TRANSDUCTION; STALK CELL; TIP CELL; VASCULAR REMODELING; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL DIFFERENTIATION; CYTOLOGY; EMBRYONIC STEM CELL; ENZYMOLOGY; GENETICS; METABOLISM; PHYSIOLOGY;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; EMBRYONIC STEM CELLS; ENDOTHELIAL CELLS; MICE; MICE, INBRED C57BL; NEOVASCULARIZATION, PHYSIOLOGIC; RECEPTOR, TIE-1; RECEPTOR, TIE-2; RETINAL VESSELS; SIGNAL TRANSDUCTION; VASCULAR REMODELING;

EID: 84942828055     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.08.024     Document Type: Article

References (50)

1. Arima S., Nishiyama K., Ko T., Arima Y., Hakozaki Y., Sugihara K., Koseki H., Uchijima Y., Kurihara Y., Kurihara H. Angiogenic morphogenesis driven by dynamic and heterogeneous collective endothelial cell movement. Development 2011, 138:4763-4776.
2. Augustin H.G., Koh G.Y., Thurston G., Alitalo K. Control of vascular morphogenesis and homeostasis through the angiopoietin-Tie system. Nat. Rev. Mol. Cell Biol. 2009, 10:165-177.
3. Bentley K., Franco C.A., Philippides A., Blanco R., Dierkes M., Gebala V., Stanchi F., Jones M., Aspalter I.M., Cagna G., et al. The role of differential VE-cadherin dynamics in cell rearrangement during angiogenesis. Nat. Cell Biol. 2014, 16:309-321.
4. Cao Y., Sonveaux P., Liu S., Zhao Y., Mi J., Clary B.M., Li C.Y., Kontos C.D., Dewhirst M.W. Systemic overexpression of angiopoietin-2 promotes tumor microvessel regression and inhibits angiogenesis and tumor growth. Cancer Res. 2007, 67:3835-3844.
5. Chen-Konak L., Guetta-Shubin Y., Yahav H., Shay-Salit A., Zilberman M., Binah O., Resnick N. Transcriptional and post-translation regulation of the Tie1 receptor by fluid shear stress changes in vascular endothelial cells. FASEB J. 2003, 17:2121-2123.
6. D'Amico G., Korhonen E.A., Waltari M., Saharinen P., Laakkonen P., Alitalo K. Loss of endothelial Tie1 receptor impairs lymphatic vessel development-brief report. Arterioscler. Thromb. Vasc. Biol. 2010, 30:207-209.
7. D'Amico G., Korhonen E.A., Anisimov A., Zarkada G., Holopainen T., Hägerling R., Kiefer F., Eklund L., Sormunen R., Elamaa H., et al. Tie1 deletion inhibits tumor growth and improves angiopoietin antagonist therapy. J. Clin. Invest. 2014, 124:824-834.
8. Daly C., Eichten A., Castanaro C., Pasnikowski E., Adler A., Lalani A.S., Papadopoulos N., Kyle A.H., Minchinton A.I., Yancopoulos G.D., Thurston G. Angiopoietin-2 functions as a Tie2 agonist in tumor models, where it limits the effects of VEGF inhibition. Cancer Res. 2013, 73:108-118.
9. del Toro R., Prahst C., Mathivet T., Siegfried G., Kaminker J.S., Larrivee B., Breant C., Duarte A., Takakura N., Fukamizu A., et al. Identification and functional analysis of endothelial tip cell-enriched genes. Blood 2010, 116:4025-4033.
10. Dumont D.J., Gradwohl G., Fong G.H., Puri M.C., Gertsenstein M., Auerbach A., Breitman M.L. Dominant-negative and targeted null mutations in the endothelial receptor tyrosine kinase, tek, reveal a critical role in vasculogenesis of the embryo. Genes Dev. 1994, 8:1897-1909.
11. Felcht M., Luck R., Schering A., Seidel P., Srivastava K., Hu J., Bartol A., Kienast Y., Vettel C., Loos E.K., et al. Angiopoietin-2 differentially regulates angiogenesis through TIE2 and integrin signaling. J. Clin. Invest. 2012, 122:1991-2005.
12. Fukuhara S., Sako K., Minami T., Noda K., Kim H.Z., Kodama T., Shibuya M., Takakura N., Koh G.Y., Mochizuki N. Differential function of Tie2 at cell-cell contacts and cell-substratum contacts regulated by angiopoietin-1. Nat. Cell Biol. 2008, 10:513-526.
13. Gerald D., Chintharlapalli S., Augustin H.G., Benjamin L.E. Angiopoietin-2: an attractive target for improved antiangiogenic tumor therapy. Cancer Res. 2013, 73:1649-1657.
14. Gerhardt H., Betsholtz C. How do endothelial cells orientate?. EXS 2005, 2005:3-15.
15. 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.
16. Goede V., Schmidt T., Kimmina S., Kozian D., Augustin H.G. Analysis of blood vessel maturation processes during cyclic ovarian angiogenesis. Lab. Invest. 1998, 78:1385-1394.
17. Goh L.K., Sorkin A. Endocytosis of receptor tyrosine kinases. Cold Spring Harb. Perspect. Biol. 2013, 5:a017459.
18. Gustafsson E., Brakebusch C., Hietanen K., Fässler R. Tie-1-directed expression of Cre recombinase in endothelial cells of embryoid bodies and transgenic mice. J. Cell Sci. 2001, 114:671-676.
19. Hansen T.M., Singh H., Tahir T.A., Brindle N.P. Effects of angiopoietins-1 and -2 on the receptor tyrosine kinase Tie2 are differentially regulated at the endothelial cell surface. Cell. Signal. 2010, 22:527-532.
20. Hellström M., Phng L.K., Gerhardt H. VEGF and Notch signaling: the yin and yang of angiogenic sprouting. Cell Adhes. Migr. 2007, 1:133-136.
21. Herbert S.P., Stainier D.Y. Molecular control of endothelial cell behaviour during blood vessel morphogenesis. Nat. Rev. Mol. Cell Biol. 2011, 12:551-564.
22. Iljin K., Petrova T.V., Veikkola T., Kumar V., Poutanen M., Alitalo K. A fluorescent Tie1 reporter allows monitoring of vascular development and endothelial cell isolation from transgenic mouse embryos. FASEB J. 2002, 16:1764-1774.
23. Jakobsson L., Franco C.A., Bentley K., Collins R.T., Ponsioen B., Aspalter I.M., Rosewell I., Busse M., Thurston G., Medvinsky A., et al. Endothelial cells dynamically compete for the tip cell position during angiogenic sprouting. Nat. Cell Biol. 2010, 12:943-953.
24. Kontos C.D., Cha E.H., York J.D., Peters K.G. The endothelial receptor tyrosine kinase Tie1 activates phosphatidylinositol 3-kinase and Akt to inhibit apoptosis. Mol. Cell. Biol. 2002, 22:1704-1713.
25. Korhonen J., Lahtinen I., Halmekytö M., Alhonen L., Jänne J., Dumont D., Alitalo K. Endothelial-specific gene expression directed by the tie gene promoter in vivo. Blood 1995, 86:1828-1835.
26. Korn C., Augustin H.G. Mechanisms of vessel pruning and regression. Dev. Cell 2015, 34:5-17.
27. Korn C., Scholz B., Hu J., Srivastava K., Wojtarowicz J., Arnsperger T., Adams R.H., Boutros M., Augustin H.G., Augustin I. Endothelial cell-derived non-canonical Wnt ligands control vascular pruning in angiogenesis. Development 2014, 141:1757-1766.
28. Lobov I.B., Brooks P.C., Lang R.A. Angiopoietin-2 displays VEGF-dependent modulation of capillary structure and endothelial cell survival in vivo. Proc. Natl. Acad. Sci. USA 2002, 99:11205-11210.
29. Mazzone M., Dettori D., Leite de Oliveira R., Loges S., Schmidt T., Jonckx B., Tian Y.M., Lanahan A.A., Pollard P., Ruiz de Almodovar C., et al. Heterozygous deficiency of PHD2 restores tumor oxygenation and inhibits metastasis via endothelial normalization. Cell 2009, 136:839-851.
30. McCarthy M.J., Crowther M., Bell P.R., Brindle N.P. The endothelial receptor tyrosine kinase tie-1 is upregulated by hypoxia and vascular endothelial growth factor. FEBS Lett. 1998, 423:334-338.
31. Parmar K.M., Larman H.B., Dai G., Zhang Y., Wang E.T., Moorthy S.N., Kratz J.R., Lin Z., Jain M.K., Gimbrone M.A., García-Cardeña G. Integration of flow-dependent endothelial phenotypes by Kruppel-like factor 2. J. Clin. Invest. 2006, 116:49-58.
32. Phng L.K., Gerhardt H. Angiogenesis: a team effort coordinated by notch. Dev. Cell 2009, 16:196-208.
33. Porat R.M., Grunewald M., Globerman A., Itin A., Barshtein G., Alhonen L., Alitalo K., Keshet E. Specific induction of tie1 promoter by disturbed flow in atherosclerosis-prone vascular niches and flow-obstructing pathologies. Circ. Res. 2004, 94:394-401.
34. Potente M., Gerhardt H., Carmeliet P. Basic and therapeutic aspects of angiogenesis. Cell 2011, 146:873-887.
35. Puri M.C., Rossant J., Alitalo K., Bernstein A., Partanen J. The receptor tyrosine kinase TIE is required for integrity and survival of vascular endothelial cells. EMBO J. 1995, 14:5884-5891.
36. Qu X., Tompkins K., Batts L.E., Puri M., Baldwin H.S. Abnormal embryonic lymphatic vessel development in Tie1 hypomorphic mice. Development 2010, 137:1285-1295.
37. Rasmussen A.L., Okumura A., Ferris M.T., Green R., Feldmann F., Kelly S.M., Scott D.P., Safronetz D., Haddock E., LaCasse R., et al. Host genetic diversity enables Ebola hemorrhagic fever pathogenesis and resistance. Science 2014, 346:987-991.
38. Saharinen P., Kerkelä K., Ekman N., Marron M., Brindle N., Lee G.M., Augustin H., Koh G.Y., Alitalo K. Multiple angiopoietin recombinant proteins activate the Tie1 receptor tyrosine kinase and promote its interaction with Tie2. J. Cell Biol. 2005, 169:239-243.
39. Saharinen P., Eklund L., Miettinen J., Wirkkala R., Anisimov A., Winderlich M., Nottebaum A., Vestweber D., Deutsch U., Koh G.Y., et al. Angiopoietins assemble distinct Tie2 signalling complexes in endothelial cell-cell and cell-matrix contacts. Nat. Cell Biol. 2008, 10:527-537.
40. Sato T.N., Tozawa Y., Deutsch U., Wolburg-Buchholz K., Fujiwara Y., Gendron-Maguire M., Gridley T., Wolburg H., Risau W., Qin Y. Distinct roles of the receptor tyrosine kinases Tie-1 and Tie-2 in blood vessel formation. Nature 1995, 376:70-74.
41. Seegar T.C., Eller B., Tzvetkova-Robev D., Kolev M.V., Henderson S.C., Nikolov D.B., Barton W.A. Tie1-Tie2 interactions mediate functional differences between angiopoietin ligands. Mol. Cell 2010, 37:643-655.
42. Shimshek D.R., Kim J., Hübner M.R., Spergel D.J., Buchholz F., Casanova E., Stewart A.F., Seeburg P.H., Sprengel R. Codon-improved Cre recombinase (iCre) expression in the mouse. Genesis 2002, 32:19-26.
43. Singh H., Hansen T.M., Patel N., Brindle N.P. The molecular balance between receptor tyrosine kinases Tie1 and Tie2 is dynamically controlled by VEGF and TNFα and regulates angiopoietin signalling. PLoS ONE 2012, 7:e29319.
44. Srinivas S., Watanabe T., Lin C.S., William C.M., Tanabe Y., Jessell T.M., Costantini F. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev. Biol. 2001, 1:4.
45. Tsiamis A.C., Morris P.N., Marron M.B., Brindle N.P. Vascular endothelial growth factor modulates the Tie-2:Tie-1 receptor complex. Microvasc. Res. 2002, 63:149-158.
46. Wang Y., Nakayama M., Pitulescu M.E., Schmidt T.S., Bochenek M.L., Sakakibara A., Adams S., Davy A., Deutsch U., Lüthi U., et al. Ephrin-B2 controls VEGF-induced angiogenesis and lymphangiogenesis. Nature 2010, 465:483-486.
47. Woo K.V., Qu X., Babaev V.R., Linton M.F., Guzman R.J., Fazio S., Baldwin H.S. Tie1 attenuation reduces murine atherosclerosis in a dose-dependent and shear stress-specific manner. J. Clin. Invest. 2011, 121:1624-1635.
48. Yabkowitz R., Meyer S., Black T., Elliott G., Merewether L.A., Yamane H.K. Inflammatory cytokines and vascular endothelial growth factor stimulate the release of soluble tie receptor from human endothelial cells via metalloprotease activation. Blood 1999, 93:1969-1979.
49. Yuan H.T., Venkatesha S., Chan B., Deutsch U., Mammoto T., Sukhatme V.P., Woolf A.S., Karumanchi S.A. Activation of the orphan endothelial receptor Tie1 modifies Tie2-mediated intracellular signaling and cell survival. FASEB J. 2007, 21:3171-3183.
50. Yuan H.T., Khankin E.V., Karumanchi S.A., Parikh S.M. Angiopoietin 2 is a partial agonist/antagonist of Tie2 signaling in the endothelium. Mol. Cell. Biol. 2009, 29:2011-2022.