New mechanism for Notch signaling to endothelium at a distance by delta-like 4 incorporation into exosomes

Blood

Volumn 116, Issue 13, 2010, Pages 2385-2394

  Sheldon, Helen ^a   Heikamp, Emily ^b   Turley, Helen ^a   Dragovic, Rebecca ^c   Thomas, Peter ^a   Oon, Chern Ein ^a   Leek, Russell ^a   Edelmann, Mariola ^d   Kessler, Benedikt ^d   Sainson, Richard C A ^a   Sargent, Ian ^c   Li, Ji Liang ^a   Harris, Adrian L ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

NOTCH RECEPTOR; NOTCH1 RECEPTOR; PROTEIN; PROTEIN DELTA LIKE 4; UNCLASSIFIED DRUG;

ANGIOGENESIS; ANIMAL CELL; ARTICLE; BIOTINYLATION; CELL COMMUNICATION; CELL MEMBRANE; CELL PROLIFERATION; COMPETITIVE INHIBITION; CONTROLLED STUDY; ENDOTHELIUM CELL; EXOSOME; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TUMOR CELL; UPREGULATION; WESTERN BLOTTING;

EID: 77957708340     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2009-08-239228     Document Type: Article

References (42)

1. Artavanis-Tsakonas S, Rand MD, Lake RJ. Notch signaling: cell fate control and signal integration in development. Science. 1999;284(5415):770-776. (Pubitemid 29291335)
2. Phng LK, Gerhardt H. Angiogenesis: a team effort coordinated by notch. Dev Cell. 2009;16(2):196-208.
3. Gale NW, Dominguez MG, Noguera I, et al. Haploinsufficiency of delta-like 4 ligand results in embryonic lethality due to major defects in arterial and vascular development. Proc Natl Acad Sci U S A. 2004;101(45):15949-15954.
4. Le Borgne R. Regulation of Notch signalling by endocytosis and endosomal sorting. Curr Opin Cell Biol. 2006;18(2):213-222. (Pubitemid 43375891)
5. Wang W, Struhl G. Drosophila Epsin mediates a select endocytic pathway that DSL ligands must enter to activate Notch. Development. 2004;131(21):5367- 5380.
6. Hicks C, Ladi E, Lindsell C, et al. A secreted Delta1-Fc fusion protein functions both as an activator and inhibitor of Notch1 signaling. J Neurosci Res. 2002;68(6):655-667.
7. Kooh PJ, Fehon RG, Muskavitch MA. Implications of dynamic patterns of Delta and Notch expression for cellular interactions during Drosophila development. Development. 1993;117(2):493-507.
8. Le Borgne R, Schweisguth F. Notch signaling: endocytosis makes delta signal better. Curr Biol. 2003;13(7):R273-R275.
9. Keller S, Sanderson MP, Stoeck A, Altevogt P. Exosomes: from biogenesis and secretion to biological function. Immunol Lett. 2006;107(2):102-108. (Pubitemid 44779821)
10. Schorey JS, Bhatnagar S. Exosome function: from tumor immunology to pathogen biology. Traffic. 2008;9(6):871-881. (Pubitemid 351639493)
11. Simons M, Raposo G. Exosomes: vesicular carriers for intercellular communication. Curr Opin Cell Biol. 2009;21(4):575-581.
12. Mishra-Gorur K, Rand MD, Perez-Villamil B, Artavanis-Tsakonas S. Down-regulation of Delta by proteolytic processing. J Cell Biol. 2002;159(2):313-324.
13. Li JL, Sainson RC, Shi W, et al. Delta-like 4 Notch ligand regulates tumor angiogenesis, improves tumor vascular function, and promotes tumor growth in vivo. Cancer Res. 2007;67(23):11244-11253.
14. Harrington LS, Sainson RC, Williams CK, et al. Regulation of multiple angiogenic pathways by Dll4 and Notch in human umbilical vein endothelial cells. Microvasc Res. 2008;75(2):144-154.
15. Wessel D, Flugge UI. A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal Biochem. 1984;138(1):141-143. (Pubitemid 14146660)
16. Batycka M, Inglis NF, Cook K, et al. Ultra-fast tandem mass spectrometry scanning combined with monolithic column liquid chromatography increases throughput in proteomic analysis. Rapid Commun Mass Spectrom. 2006;20(14):2074-2080.
17. Xu D, Suenaga N, Edelmann MJ, Fridman R, Muschel RJ, Kessler BM. Novel MMP-9 substrates in cancer cells revealed by a label-free quantitative proteomics approach. Mol Cell Proteomics. 2008;7(11):2215-2228.
18. Kolowos W, Gaipl US, Sheriff A, et al. Microparticles shed from different antigen-presenting cells display an individual pattern of surface molecules and a distinct potential of allogeneic T-cell activation. Scand J Immunol. 2005;61(3):226-233.
19. Thery C, Amigorena S, Raposo G, Clayton A. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol. 2006;chapter 3:unit 3.22.
20. Fevrier B, Raposo G. Exosomes: endosomal-derived vesicles shipping extracellular messages. Curr Opin Cell Biol. 2004;16(4):415-421. (Pubitemid 38903148)
21. Simpson RJ, Jensen SS, Lim JW. Proteomic profiling of exosomes: current perspectives. Proteomics. 2008;8(19):4083-4099.
22. Munoz-Chapuli R, Quesada AR, Angel Medina M. Angiogenesis and signal transduction in endothelial cells. Cell Mol Life Sci. 2004;61(17):2224-2243.
23. Six EM, Ndiaye D, Sauer G, et al. The notch ligand Delta1 recruits Dlg1 at cell-cell contacts and regulates cell migration. J Biol Chem. 2004;279(53):55818-55826. (Pubitemid 40066589)
24. Hood JL, Pan H, Lanza GM, Wickline SA. Paracrine induction of endothelium by tumor exosomes. Lab Invest. 2009;89(11):1317-1328.
25. Noguera-Troise I, Daly C, Papadopoulos NJ, et al. Blockade of Dll4 inhibits tumour growth by promoting non-productive angiogenesis. Nature. 2006;444(7122):1032-1037.
26. Kanno T, Yamada T, Iwabuki H, et al. Size distribution measurement of vesicles by atomic force microscopy. Anal Biochem. 2002;309(2):196-199. (Pubitemid 35387309)
27. Denzer K, Kleijmeer MJ, Heijnen HF, StoorvogelW, Geuze HJ. Exosome: from internal vesicle of the multivesicular body to intercellular signaling device. J Cell Sci. 2000;113(pt 19):3365-3374.
28. Al-Nedawi K, Meehan B, Micallef J, et al. Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat Cell Biol. 2008;10(5):619-624.
29. Skog J, Wurdinger T, van Rijn S, et al. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol. 2008;10(12):1470-1476.
30. Millimaggi D, Mari M, D'Ascenzo S, et al. Tumor vesicle-associated CD147 modulates the angiogenic capability of endothelial cells. Neoplasia. 2007;9(4):349-357.
31. Jubb AM, Turley H, Moeller HC, et al. Expression of delta-like ligand 4 (Dll4) and markers of hypoxia in colon cancer. Br J Cancer. 2009;101(10):1749- 1757.
32. Suchting S, Freitas C, le Noble F, et al. The Notch ligand Delta-like 4 negatively regulates endothelial tip cell formation and vessel branching. Proc Natl Acad Sci U S A. 2007;104(9):3225-3230. (Pubitemid 46364141)
33. Lobov IB, Renard RA, Papadopoulos N, et al. Delta-like ligand 4 (Dll4) is induced by VEGF as a negative regulator of angiogenic sprouting. Proc Natl Acad Sci U S A. 2007;104(9):3219-3224.
34. Sakamoto K, Ohara O, Takagi M, Takeda S, Katsube K. Intracellular cell-autonomous association of Notch and its ligands: a novel mechanism of Notch signal modification. Dev Biol. 2002;241(2):313-326. (Pubitemid 34098695)
35. Jacobsen TL, Brennan K, Arias AM, Muskavitch MA. Cis-interactions between Delta and Notch modulate neurogenic signalling in Drosophila. Development. 1998;125(22):4531-4540. (Pubitemid 28564296)
36. Glittenberg M, Pitsouli C, Garvey C, Delidakis C, Bray S. Role of conserved intracellular motifs in Serrate signalling, cis-inhibition and endocytosis. EMBO J. 2006;25(20):4697-4706. (Pubitemid 44607016)
37. Ladi E, Nichols JT, Ge W, et al. The divergent DSL ligand Dll3 does not activate Notch signaling but cell autonomously attenuates signaling induced by other DSL ligands. J Cell Biol. 2005;170(6):983-992.
38. Parks AL, Stout JR, Shepard SB, et al. Structure-function analysis of delta trafficking, receptor binding and signaling in Drosophila. Genetics. 2006;174(4):1947-1961.
39. Klueg KM, Muskavitch MA. Ligand-receptor interactions and trans-endocytosis of Delta, Serrate and Notch: members of the Notch signalling pathway in Drosophila. J Cell Sci. 1999;112(pt 19):3289-3297.
40. Fehon RG, Kooh PJ, Rebay I, et al. Molecular interactions between the protein products of the neurogenic loci Notch and Delta, two EGF-homologous genes in Drosophila. Cell. 1990;61(3):523-534. (Pubitemid 20169007)
41. Hellstrom M, Phng LK, Hofmann JJ, et al. Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis. Nature. 2007;445(7129):776-780.
42. Parks AL, Klueg KM, Stout JR, Muskavitch MA. Ligand endocytosis drives receptor dissociation and activation in the Notch pathway. Development. 2000;127(7):1373-1385. (Pubitemid 30232589)