Synchronization of endothelial Dll4-Notch dynamics switch blood vessels from branching to expansion

eLife

Volumn 5, Issue APRIL2016, 2016, Pages

  Ubezio, Benedetta ^a,b   Blanco, Raquel Agudo ^a,b   Geudens, Ilse ^c,d   Stanchi, Fabio ^c,d   Mathivet, Thomas ^c,d   Jones, Martin L ^a,b   Ragab, Anan ^a,b   Bentley, Katie ^a,e   Gerhardt, Holger ^{a,b,c,d,f,g,h}  

^a London Research Institute   (United Kingdom)

^b CRUK   (United Kingdom)

^c DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^d UNIVERSITY OF LEUVEN   (Belgium)

^e BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^f MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^g DZHK GERMAN CENTRE FOR CARDIOVASCULAR RESEARCH   (Germany)

^h BERLIN INSTITUTE OF HEALTH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

NOTCH DELTA LIKE LIGAND 4; NOTCH RECEPTOR; UNCLASSIFIED DRUG; DLL4 PROTEIN, MOUSE; MEMBRANE PROTEIN; MESSENGER RNA; SIGNAL PEPTIDE; VASCULAR ENDOTHELIAL GROWTH FACTOR A, MOUSE; VASCULOTROPIN A;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; CELL SYNCHRONIZATION; CONTROLLED STUDY; ENDOTHELIUM CELL; GENE OVEREXPRESSION; GENE SEQUENCE; GLIOBLASTOMA; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE; MATHEMATICAL ANALYSIS; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RETINOPATHY; SCANNING ELECTRON MICROSCOPY; ANGIOGENESIS; ANIMAL; BRAIN TUMOR; CANCER TRANSPLANTATION; CELL MOTION; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; MOUSE EMBRYONIC STEM CELL; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; PHYSIOLOGICAL FEEDBACK; REPORTER GENE; RETINA; SIGNAL TRANSDUCTION;

ANIMALS; BRAIN NEOPLASMS; CELL MOVEMENT; ENDOTHELIAL CELLS; FEEDBACK, PHYSIOLOGICAL; GENE EXPRESSION REGULATION; GENES, REPORTER; GLIOBLASTOMA; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; MICE; MOUSE EMBRYONIC STEM CELLS; NEOPLASM TRANSPLANTATION; NEOVASCULARIZATION, PATHOLOGIC; NEOVASCULARIZATION, PHYSIOLOGIC; RECEPTORS, NOTCH; RETINA; RNA, MESSENGER; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84975215345     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.12167     Document Type: Article

References (50)

1. Aulehla A, Wiegraebe W, Baubet V, Wahl MB, Deng C, Taketo M, Lewandoski M, PourquiéO. 2008. A beta-catenin gradient links the clock and wavefront systems in mouse embryo segmentation. Nature Cell Biology 10: 186-193. doi: 10.1038/ncb1679.
2. Beets K, Huylebroeck D, Moya IM, Umans L, Zwijsen A. 2013. Robustness in angiogenesis: Notch and BMP. shaping waves. Trends in Genetics 29: 140-149. doi: 10.1016/j.tig.2012.11.008.
3. Bentley K, Gerhardt H, Bates PA. 2008. Agent-based simulation of notch-mediated tip cell selection in angiogenic sprout initialisation. Journal of Theoretical Biology 250: 25-36. doi: 10.1016/j.jtbi.2007.09.015.
4. Bentley K, Mariggi G, Gerhardt H, Bates PA. 2009. Tipping the balance: Robustness of tip cell selection, migration and fusion in angiogenesis. PLoS Computational Biology 5:e1000549. doi: 10.1371/journal.pcbi.1000549.
5. Bentley K, Franco CA, Philippides A, Blanco R, Dierkes M, Gebala V, Stanchi F, Jones M, Aspalter IM, Cagna G, Weström S, Claesson-Welsh L, Vestweber D, Gerhardt H. 2014a. The role of differential ve-cadherin dynamics in cell rearrangement during angiogenesis. Nature Cell Biology 16: 309-321. doi: 10.1038/ncb2926.
6. Bentley K, Philippides A, Ravasz Regan E. 2014b. Do endothelial cells dream of eclectic shape? Developmental Cell 29: 146-158. doi: 10.1016/j.devcel.2014.03.019.
7. 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. 1996. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 380: 435-439. doi: 10.1038/380435a0.
8. Claxton S, Kostourou V, Jadeja S, Chambon P, Hodivala-Dilke K, Fruttiger M. 2008. Efficient, inducible cre-recombinase activation in vascular endothelium. Genesis 46: 74-80. doi: 10.1002/dvg.20367.
9. Corish P, Tyler-Smith C. 1999. Attenuation of green fluorescent protein half-life in mammalian cells. Protein Engineering Design and Selection 12: 1035-1040. doi: 10.1093/protein/12.12.1035.
10. Day RN, Davidson MW. 2009. The fluorescent protein palette: Tools for cellular imaging. Chemical Society Reviews 38: 2887-2921. doi: 10.1039/b901966a.
11. Dequéant ML, Glynn E, Gaudenz K, Wahl M, Chen J, Mushegian A, PourquiéO. 2006. A complex oscillating network of signaling genes underlies the mouse segmentation clock. Science 314: 1595-1598. doi: 10.1126/science.1133141.
12. Franco CA, Jones ML, Bernabeu MO, Geudens I, Mathivet T, Rosa A, Lopes FM, Lima AP, Ragab A, Collins RT, Phng LK, Coveney PV, Gerhardt H. 2015. Dynamic endothelial cell rearrangements drive developmental vessel regression. PLoS Biology 13:e1002125. doi: 10.1371/journal.pbio.1002125.
13. Gale NW, Dominguez MG, Noguera I, Pan L, Hughes V, Valenzuela DM, Murphy AJ, Adams NC, Lin HC, Holash J, Thurston G, Yancopoulos GD. 2004. Haploinsufficiency of delta-like 4 ligand results in embryonic lethality due to major defects in arterial and vascular development. Proceedings of the National Academy of Sciences of the United States of America 101: 15949-15954. doi: 10.1073/pnas.0407290101.
14. Gerhardt H, Golding M, Fruttiger M, Ruhrberg C, Lundkvist A, Abramsson A, Jeltsch M, Mitchell C, Alitalo K, Shima D, Betsholtz C. 2003. Vegf guides angiogenic sprouting utilizing endothelial tip cell filopodia. The Journal of Cell Biology 161: 1163-1177. doi: 10.1083/jcb.200302047.
15. Giudicelli F, Lewis J. 2004. The vertebrate segmentation clock. Current Opinion in Genetics & Development 14: 407-414. doi: 10.1016/j.gde.2004.06.014.
16. Goldbeter A, PourquiéO. 2008. Modeling the segmentation clock as a network of coupled oscillations in the notch, wnt and FGF signaling pathways. Journal of Theoretical Biology 252: 574-585. doi: 10.1016/j.jtbi.2008.01.006.
17. Hanahan D, Weinberg RA. 2011. Hallmarks of cancer: The next generation. Cell 144: 646-674. doi: 10.1016/j.cell.2011.02.013.
18. Hellström 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, Kalén M, Gerhardt H, Betsholtz C. 2007. Dll4 signalling through notch1. regulates formation of tip cells during angiogenesis. Nature 445: 776-780. doi: 10.1038/nature05571.
19. Herrgen L, Ares S, Morelli LG, Schröter C, Jülicher F, Oates AC. 2010. Intercellular coupling regulates the period of the segmentation clock. Current Biology 20: 1244-1253. doi: 10.1016/j.cub.2010.06.034.
20. Hsiao EC, Yoshinaga Y, Nguyen TD, Musone SL, Kim JE, Swinton P, Espineda I, Manalac C, deJong PJ, Conklin BR. 2008. Marking embryonic stem cells with a 2A self-cleaving peptide: A NKX2-5 emerald GFP BAC reporter. PloS One 3:e2532. doi: 10.1371/journal.pone.0002532.
21. Hubaud A, PourquiéO. 2013. Making the clock tick: Right time, right pace. Developmental Cell 24: 115-116. doi: 10.1016/j.devcel.2013.01.004.
22. Jakobsson L, Kreuger J, Holmborn K, Lundin L, Eriksson I, Kjellén L, Claesson-Welsh L. 2006. Heparan sulfate in trans potentiates vegfr-mediated angiogenesis. Developmental Cell 10: 625-634. doi: 10.1016/j.devcel.2006.03.009.
23. Jakobsson L, Kreuger J, Claesson-Welsh L. 2007. Building blood vessels-stem cell models in vascular biology. The Journal of Cell Biology 177: 751-755. doi: 10.1083/jcb.200701146.
24. 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. 2010. Endothelial cells dynamically compete for the tip cell position during angiogenic sprouting. Nature Cell Biology 12: 943-953. doi: 10.1038/ncb2103.
25. Jiang YJ, Aerne BL, Smithers L, Haddon C, Ish-Horowicz D, Lewis J. 2000. Notch signalling and the synchronization of the somite segmentation clock. Nature 408: 475-479. doi: 10.1038/35044091.
26. Joyner AL. 2000. Gene Targeting: A Practical Approach. 2nd Ed Oxford: Oxford University Press.
27. Kageyama R, Masamizu Y, Niwa Y. 2007. Oscillator mechanism of notch pathway in the segmentation clock. Developmental Dynamics 236: 1403-1409. doi: 10.1002/dvdy.21114.
28. Li X, Zhao X, Fang Y, Jiang X, Duong T, Fan C, Huang CC, Kain SR. 1998. Generation of destabilized green fluorescent protein as a transcription reporter. The Journal of Biological Chemistry 273: 34970-34975. doi: 10.1074/jbc.273.52.34970.
29. Li JL, Sainson RCA, Shi W, Leek R, Harrington LS, Preusser M, Biswas S, Turley H, Heikamp E, Hainfellner JA, Harris AL. 2007. Delta-like 4 notch ligand regulates tumor angiogenesis, improves tumor vascular function, and promotes tumor growth in vivo. Cancer Research 67: 11244-11253. doi: 10.1158/0008-5472.CAN-07-0969.
30. Lobov IB, Renard RA, Papadopoulos N, Gale NW, Thurston G, Yancopoulos GD, Wiegand SJ. 2007. Delta-like ligand 4 (dll4) is induced by VEGF as a negative regulator of angiogenic sprouting. Proceedings of the National Academy of Sciences of the United States of America 104: 3219-3224. doi: 10.1073/pnas.0611206104.
31. Mailhos C, Lewis J, Ish-Horowicz D, Modlich U, Harris A, Bicknell R. 2001. Delta4, an endothelial specific notch ligand expressed at sites of physiological and tumor angiogenesis. Differentiation 69: 135-144. doi: 10.1046/j.1432-0436.2001.690207.x.
32. Martínez-Murillo R, Martínez A. 2007. Standardization of an orthotopic mouse brain tumor model following transplantation of CT-2A astrocytoma cells. Histology and Histopathology 22: 1309-1326.
33. Masamizu Y, Ohtsuka T, Takashima Y, Nagahara H, Takenaka Y, Yoshikawa K, Okamura H, Kageyama R. 2006. Real-time imaging of the somite segmentation clock: Revelation of unstable oscillators in the individual presomitic mesoderm cells. Proceedings of the National Academy of Sciences of the United States of America 103: 1313-1318. doi: 10.1073/pnas.0508658103.
34. Miquerol L, Langille BL, Nagy A. 2000. Embryonic development is disrupted by modest increases in vascular endothelial growth factor gene expression. Development 127: 3941-3946.
35. Muzumdar MD, Tasic B, Miyamichi K, Li L, Luo L. 2007. A global double-fluorescent cre reporter mouse.. Genesis 45: 593-605. doi: 10.1002/dvg.20335.
36. Nagai T, Ibata K, Park ES, Kubota M, Mikoshiba K, Miyawaki A. 2002. A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nature Biotechnology 20: 87-90. doi: 10.1038/nbt0102-87.
37. Nagy A. 2003. Manipulating the Mouse Embryo: A Laboratory Manual. 3rd ed. Cold Spring Harbor: Cold Spring Harbor Laboratory Press.
38. Noguera-Troise I, Daly C, Papadopoulos NJ, Coetzee S, Boland P, Gale NW, Lin HC, Yancopoulos GD, Thurston G. 2006. Blockade of dll4 inhibits tumour growth by promoting non-productive angiogenesis. Nature 444: 1032-1037. doi: 10.1038/nature05355.
39. Phng LK, Gerhardt H. 2009. Angiogenesis: A team effort coordinated by notch. Developmental Cell 16: 196-208. doi: 10.1016/j.devcel.2009.01.015.
40. Potente M, Gerhardt H, Carmeliet P. 2011. Basic and therapeutic aspects of angiogenesis. Cell 146: 873-887. doi: 10.1016/j.cell.2011.08.039.
41. Ridgway J, Zhang G, Wu Y, Stawicki S, Liang WC, Chanthery Y, Kowalski J, Watts RJ, Callahan C, Kasman I, Singh M, Chien M, Tan C, Hongo JA, de Sauvage F, Plowman G, Yan M. 2006. Inhibition of dll4 signalling inhibits tumour growth by deregulating angiogenesis. Nature 444: 1083-1087. doi: 10.1038/nature05313.
42. Ruhrberg C, Gerhardt H, Golding M, Watson R, Ioannidou S, Fujisawa H, Betsholtz C, Shima DT. 2002. Spatially restricted patterning cues provided by heparin-binding VEGF-A control blood vessel branching morphogenesis. Genes & Development 16: 2684-2698. doi: 10.1101/gad.242002.
43. Ruhrberg C. 2003. Growing and shaping the vascular tree: Multiple roles for VEGF. BioEssays 25: 1052-1060. doi: 10.1002/bies.10351.
44. Smith LE, Wesolowski E, McLellan A, Kostyk SK, D’Amato R, Sullivan R, D’Amore PA. 1994. Oxygen-induced retinopathy in the mouse. Investigative Ophthalmology & Visual Science 35: 101-111.
45. Suchting S, Freitas C, le Noble F, Benedito R, Bréant C, Duarte A, Eichmann A. 2007. The notch ligand delta-like 4 negatively regulates endothelial tip cell formation and vessel branching. Proceedings of the National Academy of Sciences of the United States of America 104: 3225-3230. doi: 10.1073/pnas.0611177104.
46. Tajbakhsh S, Spörle R. 1998. Somite development: Constructing the vertebrate body. Cell 92: 9-16. doi: 10.1016/s0092-8674(00)80894-6.
47. Uyttendaele H, Ho J, Rossant J, Kitajewski J. 2001. Vascular patterning defects associated with expression of activated notch4 in embryonic endothelium. Proceedings of the National Academy of Sciences of the United States of America 98: 5643-5648. doi: 10.1073/pnas.091584598.
48. Wahl MB, Deng C, Lewandoski M, PourquiéO. 2007. Fgf signaling acts upstream of the NOTCH and WNT. signaling pathways to control segmentation clock oscillations in mouse somitogenesis. Development 134: 4033-4041. doi: 10.1242/dev.009167.
49. Webb AB, Lengyel IM, Jörg DJ, Valentin G, Jülicher F, Morelli LG, Oates AC. 2016. Persistence, period and precision of autonomous cellular oscillators from the zebrafish segmentation clock. eLife 5. doi: 10.7554/eLife.08438.
50. Yu D, Ellis HM, Lee EC, Jenkins NA, Copeland NG, Court DL. 2000. An efficient recombination system for chromosome engineering in escherichia coli. Proceedings of the National Academy of Sciences of the United States of America 97: 5978-5983. doi: 10.1073/pnas.100127597.