Notch signalling in ischaemia-induced angiogenesis

Biochemical Society Transactions

Volumn 37, Issue 6, 2009, Pages 1221-1227

  Al Haj Zen, Ayman ^a   Madeddu, Paolo ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Hypoxia; Ischaemic disease; Notch intracellular domain; Notch signalling; Therapeutic angiogenesis; Vascular endothelial growth factor (VEGF)

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1; NOTCH RECEPTOR; NOTCH1 RECEPTOR; NOTCH2 RECEPTOR; NOTCH3 RECEPTOR; NOTCH4 RECEPTOR; TUMOR NECROSIS FACTOR ALPHA;

CELL DEATH; CELL DIFFERENTIATION; CELL FATE; CELL INTERACTION; CELL MIGRATION; CELL PROLIFERATION; CELL TYPE; DEVELOPMENTAL STAGE; EMBRYO DEVELOPMENT; ENDOTHELIUM CELL; GENE ACTIVATION; GENE EXPRESSION; GENE FUNCTION; GENE REPRESSION; GENE TARGETING; ISCHEMIA; LEUKOCYTE; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; PERINATAL PERIOD; PHENOTYPE; PRIORITY JOURNAL; REVIEW; SKELETAL MUSCLE; TUMOR GROWTH;

ANOXIA; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; HUMANS; ISCHEMIA; MUSCLE, SKELETAL; NEOVASCULARIZATION, PHYSIOLOGIC; RECEPTORS, NOTCH; REGENERATION; SIGNAL TRANSDUCTION;

EID: 70450160119     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST0371221     Document Type: Review

References (63)

1. Selvin, E. and Erlinger, T.P. (2004) Prevalence of and risk factors for peripheral arterial disease in the United States: results from the National Health and Nutrition Examination Survey, 1999-2000. Circulation 110, 738-743
2. Slovut, D.P. and Sullivan, T.M. (2008) Critical limb ischaemia: medical and surgical management. Vasc. Med. 13, 281-291
3. Heilmann, C., Beyersdorf, F. and Lutter, G. (2002) Collateral growth: cells arrive at the construction site. Cardiovasc. Surg. 10, 570-578
4. Emanueli, C. and Madeddu, P. (2006) Therapeutic angiogenesis: translating experimental concepts to medically relevant goals. Vasc. Pharmacol. 45, 334-339
5. Takeshita, S., Pu, L.Q., Stein, L.A., Sniderman, A.D., Bunting, S., Ferrara, N., Isner, J.M. and Symes, J.F. (1994) Intramuscular administration of vascular endothelial growth factor induces dose-dependent collateral artery augmentation in a rabbit model of chronic limb ischaemia. Circulation 90, II228-II234
6. Stone, O.A., Richer, C., Emanueli, C., van Weel, V., Quax, P.H., Katare, R., Kraenkel, N., Campagnolo, P., Barcelos, L.S., Siragusa, M. et al. (2009) Critical role of tissue kallikrein in vessel formation and maturation: implications for therapeutic revascularization. Arterioscler. Thromb. Vasc. Biol. 29, 657-664
7. Emanueli, C., Salis, M.B., Pinna, A., Graiani, G., Manni, L. and Madeddu, P. (2002) Nerve growth factor promotes angiogenesis and arteriogenesis in ischemic hindlimbs. Circulation 106, 2257-2262
8. Henry, T.D., Annex, B.H., McKendall, G.R., Azrin, M.A., Lopez, J.J., Giordano, F.J., Shah, P.K., Willerson, J.T., Benza, R.L., Berman, D.S. et al. (2003) The VIVA trial: vascular endothelial growth factor in ischaemia for vascular angiogenesis. Circulation 107, 1359-1365
9. Simons, M. and Ware, J.A. (2003) Therapeutic angiogenesis in cardiovascular disease. Nat. Rev. Drug Discov. 2, 863-871
10. Simons, M. (2005) Angiogenesis: where do we stand now? Circulation 111, 1556-1566
11. Lai, E.C. (2004) Notch signaling: control of cell communication and cell fate. Development 131, 965-973
12. Schroeter, E.H., Kisslinger, J.A. and Kopan, R. (1998) Notch-1 signalling requires ligand-induced proteolytic release of intracellular domain. Nature 393, 382-386
13. Artavanis-Tsakonas, S., Rand, M.D. and Lake, R.J. (1999) Notch signaling: cell fate control and signal integration in development. Science 284, 770-776
14. Duarte, A., Hirashima, M., Benedito, R., Trindade, A., Diniz, P., Bekman, E., Costa, L., Henrique, D. and Rossant, J. (2004) Dosage-sensitive requirement for mouse Dll4 in artery development. Genes Dev. 18, 2474-2478
15. Krebs, L.T., Xue, Y., Norton, C.R., Shutter, J.R., Maguire, M., Sundberg, J.P., Gallahan, D., Closson, V., Kitajewski, J., Callahan, R. et al. (2000) Notch signaling is essential for vascular morphogenesis in mice. Genes Dev. 14, 1343-1352
16. Roca, C. and Adams, R.H. (2007) Regulation of vascular morphogenesis by Notch signaling. Genes Dev. 21, 2511-2524
17. Phng, L.K. and Gerhardt, H. (2009) Angiogenesis: a team effort coordinated by notch. Dev. Cell 16, 196-208
18. Sato, Y., Watanabe, T., Saito, D., Takahashi, T., Yoshida, S., Kohyama, J., Ohata, E., Okano, H. and Takahashi, Y. (2008) Notch mediates the segmental specification of angioblasts in somites and their directed migration toward the dorsal aorta in avian embryos. Dev. Cell 14, 890-901
19. You, L.R., Lin, F.J., Lee, C.T., DeMayo, F.J., Tsai, M.J. and Tsai, S.Y. (2005) Suppression of Notch signalling by the COUP-TFII transcription factor regulates vein identity. Nature 435, 98-104
20. Sörensen, I., Adams, R.H. and Gossler, A. (2009) DLL1-mediated Notch activation regulates endothelial identity in mouse fetal arteries. Blood 113, 5680-5688
21. Gerhardt, H., Golding, M., Fruttiger, M., Ruhrberg, C., Lundkvist, A., Abramsson, A., Jeltsch, M., Mitchell, C., Alitalo, K., Shima, D. and Betsholtz, C. (2003) VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J. Cell Biol. 161, 1163-1177
22. Gerhardt, H., Ruhrberg, C., Abramsson, A., Fujisawa, H., Shima, D. and Betsholtz, C. (2004) Neuropilin-1 is required for endothelial tip cell guidance in the developing central nervous system. Dev. Dyn. 231, 503-509
23. Siekmann, A.F. and Lawson, N.D. (2007) Notch signalling limits angiogenic cell behaviour in developing zebrafish arteries. Nature 445, 781-784
24. Leslie, J.D., Ariza-McNaughton, L., Bermange, A.L., McAdow, R., Johnson, S.L. and Lewis, J. (2007) Endothelial signalling by the Notch ligand Delta-like 4 restricts angiogenesis. Development 134, 839-844
25. Tammela, T., Zarkada, G., Wallgard, E., Murtomäki, A., Suchting, S., Wirzenius, M., Waltari, M., Hellström, M., Schomber, T., Peltonen, R. et al. (2008) Blocking VEGFR-3 suppresses angiogenic sprouting and vascular network formation. Nature 454, 656-660
26. Hellström, M., Phng, L.K., Hofmann, J.J., Wallgard, E., Coultas, L., Lindblom, P., Alva, J., Nilsson, A.K., Karlsson, L., Gaiano, N. et al. (2007) Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis. Nature 445, 776-780
27. Sainson, R.C., Aoto, J., Nakatsu, M.N., Holderfield, M., Conn, E., Koller, E. and Hughes, C.C. (2005) Cell-autonomous notch signaling regulates endothelial cell branching and proliferation during vascular tubulogenesis. FASEB J. 19, 1027-1029
28. Liu, Z.J., Xiao, M., Balint, K., Soma, A., Pinnix, C.C., Capobianco, A.J., Velazquez, O.C. and Herlyn, M. (2006) Inhibition of endothelial cell proliferation by Notch1 signaling is mediated by repressing MAPK and PI3K/Akt pathways and requires MAML1. FASEB J. 20, 1009-1011
29. Phng, L.K., Potente, M., Leslie, J.D., Babbage, J., Nyqvist, D., Lobov, I., Ondr, J.K., Rao, S., Lang, R.A., Thuston, G. and Gerhardt, H. (2009) Nrarp coordinates endothelial Notch and Wnt signaling to control vessel density in angiogenesis. Dev. Cell 16, 70-82
30. Ridgway, J., Zhang, G., Wu, Y., Stawicki, S., Liang, W.C., Chanthery, Y., Kowalski, J., Watts, R.J., Callahan, C., Kasman, I. et al. (2006) Inhibition of Dll4 signalling inhibits tumour growth by deregulating angiogenesis. Nature 444, 1083-1087
31. Noguera-Troise, I., Daly, C., Papadopoulos, N.J., Coetzee, S., Boland, P., Gale, N.W., Lin, H.C., Yancopoulos, G.D. and Thurston, G. (2006) Blockade of Dll4 inhibits tumour growth by promoting non-productive angiogenesis. Nature 444, 1032-1037
32. Li, J.L., Sainson, R.C., Shi, W., Leek, R., Harrington, L.S., Preusser, M., Biswas, S., Turley, H., Heikamp, E., Hainfellner, J.A. and Harris, A.L. (2007) Delta-like 4 Notch ligand regulates tumor angiogenesis, improves tumor vascular function, and promotes tumor growth in vivo. Cancer Res. 67, 11244-11253
33. Sainson, R.C., Johnston, D.A., Chu, H.C., Holderfield, M.T., Nakatsu, M.N., Crampton, S.P., Davis, J., Conn, E. and Hughes, C.C. (2008) TNF primes endothelial cells for angiogenic sprouting by inducing a tip cell phenotype. Blood 111, 4997-5007
34. Johnston, D.A., Dong, B. and Hughes, C.C. (2009) TNF induction of jagged-1 in endothelial cells is NFκB-dependent. Gene 435, 36-44
35. Lindner, V., Booth, C., Prudovsky, I., Small, D., Maciag, T. and Liaw, L. (2001) Members of the Jagged/Notch gene families are expressed in injured arteries and regulate cell phenotype via alterations in cell matrix and cell-cell interaction. Am. J. Pathol. 159, 875-883
36. Semenza, G.L. (2001) HIF-1 and mechanisms of hypoxia sensing. Curr. Opin. Cell Biol. 13, 167-171
37. Gustafsson, M.V., Zheng, X., Pereira, T., Gradin, K., Jin, S., Lundkvist, J., Ruas, J.L., Poellinger, L., Lendahl, U. and Bondesson, M. (2005) Hypoxia requires notch signaling to maintain the undifferentiated cell state. Dev. Cell 9, 617-628
38. Coleman, M.L., McDonough, M.A., Hewitson, K.S., Coles, C., Mecinovic, J., Edelmann, M., Cook, K.M., Cockman, M.E., Lancaster, D.E., Kessler, B.M. et al. (2007) Asparaginyl hydroxylation of the Notch ankyrin repeat domain by factor inhibiting hypoxia-inducible factor. J. Biol. Chem. 282, 24027-24038
39. Zheng, X., Linke, S., Dias, J.M., Zheng, X., Gradin, K., Wallis, T.P., Hamilton, B.R., Gustafsson, M., Ruas, J.L., Wilkins, S. et al. (2008) Interaction with factor inhibiting HIF-1 defines an additional mode of cross-coupling between the Notch and hypoxia signaling pathways. Proc. Natl. Acad. Sci. U.S.A. 105, 3368-3373
40. Patel, N.S., Li, J.L., Generali, D., Poulsom, R., Cranston, D.W. and Harris, A.L. (2005) Up-regulation of Delta-like 4 ligand in human tumor vasculature and the role of basal expression in endothelial cell function. Cancer Res. 65, 8690-8697
41. Jogi, A., Ora, I., Nilsson, H., Lindeheim, A., Makino, Y., Poellinger, L., Axelson, A. and Pahlman, S. (2002) Hypoxia alters gene expression in human neuroblastoma cells toward an immature and neural crest-like phenotype. Proc. Natl. Acad. Sci. U.S.A. 99, 7021-7026
42. Bedogni, B., Warneke, J.A., Nickoloff, B.J., Giaccia, A.J. and Powell, M.B. (2008) Notch1 is an effector of Akt and hypoxia in melanoma development. J. Clin. Invest. 118, 3660-3670
43. Gaengel, K., Genové, G., Armulik, A. and Betsholtz, C. (2009) Endothelial-mural cell signaling in vascular development and angiogenesis. Arterioscler. Thromb. Vasc. Biol. 29, 630-638
44. High, F.A., Lu, M.M., Pear, W.S., Loomes, K.M., Kaestner, K.H. and Epstein, J.A. (2008) Endothelial expression of the Notch ligand Jagged1 is required for vascular smooth muscle development. Proc. Natl. Acad. Sci. U.S.A. 105, 1955-1959
45. Domenga, V., Fardoux, P., Lacombe, P., Monet, M., Maciazek, J., Krebs, L.T., Klonjkowski, B., Berrou, E., Mericskay, M., Li, Z. et al. (2004) Notch3 is required for arterial identity and maturation of vascular smooth muscle cells. Genes Dev. 18, 2730-2735
46. Liu, H., Kennard, S. and Lilly, B. (2009) NOTCH3 expression is induced in mural cells through an autoregulatory loop that requires endothelial-expressed JAGGED1. Circ. Res. 104, 466-475
47. Noseda, M., Fu, Y., Niessen, K., Wong, F., Chang, L., McLean, G. and Karsan, A. (2006) Smooth muscle α-actin is a direct target of Notch/CSL. Circ. Res. 98, 1468-1470
48. Doi, H., Iso, T., Sato, H., Yamazaki, M., Matsui, H., Tanaka, T., Manabe, I., Arai, M., Nagai, R. and Kurabayashi, M. (2006) Jagged1-selective notch signaling induces smooth muscle differentiation via a RBP-Jκ-dependent pathway. J. Biol. Chem. 281, 28555-28564
49. Jin, S., Hansson, E.M., Tikka, S., Lanner, F., Sahlgren, C., Farnebo, F., Baumann, M., Kalimo, H. and Lendahl, U. (2008) Notch signaling regulates platelet-derived growth factor receptor-β expression in vascular smooth muscle cells. Circ. Res. 102, 1483-1491
50. Joutel, A., Corpechot, C., Ducros, A., Vahedi, K., Chabriat, H., Mouton, P., Alamowitch, S., Domenga, V., Cécillion, M., Marechal, E. et al. (1996) Notch3 mutations in CADASIL, a hereditary adult-onset condition causing stroke and dementia. Nature 383, 707-710
51. Tang, Y., Urs, S. and Liaw, L. (2008) Hairy-related transcription factors inhibit Notch-induced smooth muscle a-actin expression by interfering with Notch intracellular domain/CBF-1 complex interaction with the CBF-1-binding site. Circ. Res. 102, 661-668
52. Limbourg, A., Ploom, M., Elligsen, D., Sörensen, I., Ziegelhoeffer, T., Gossler, A., Drexler, H. and Limbourg, F.P. (2007) Notch ligand Delta-like 1 is essential for postnatal arteriogenesis. Circ. Res. 100, 363-371
53. Charge, S.B. and Rudnicki, M.A. (2004) Cellular and molecular regulation of muscle regeneration. Physiol. Rev. 84, 209-238
54. Hawke, T.J. and Garry, D.J. (2001) Myogenic satellite cells: physiology to molecular biology. J. Appl. Physiol. 91, 534-551
55. Conboy, I.M. and Rando, T.A. (2002) The regulation of Notch signaling controls satellite cell activation and cell fate determination in postnatal myogenesis. Dev. Cell 3, 397-409
56. Vasyutina, E., Lenhard, D.C., Wende, H., Erdmann, B., Epstein, J.A. and Birchmeier, C. (2007) RBP-J (Rbpsuh) is essential to maintain muscle progenitor cells and to generate satellite cells. Proc. Natl. Acad. Sci. U.S.A. 104, 4443-4448
57. Conboy, I.M., Conboy, M.J., Smythe, G.M. and Rando, T.A. (2003) Notch-mediated restoration of regenerative potential to aged muscle. Science 302, 1575-1577
58. Sun, H., Li, L., Vercherat, C., Gulbagci, N.T., Acharjee, S., Li, J., Chung, T.K., Thin, T.H. and Taneja, R. (2007) Stra13 regulates satellite cell activation by antagonizing Notch signaling. J. Cell Biol. 177, 647-657
59. McCright, B., Gao, X., Shen, L., Lozier, J., Lan, Y., Maguire, M., Herzlinger, D., Weinmaster, G., Jiang, R. and Gridley, T. (2001) Defects in development of the kidney, heart and eye vasculature in mice homozygous for a hypomorphic Notch2 mutation. Development 128, 491-502
60. Benedito, R., Trindade, A., Hirashima, M., Henrique, D., da Costa, L.L., Rossant, J., Gill, P.S. and Duarte, A. (2008) Loss of Notch signalling induced by Dll4 causes arterial calibre reduction by increasing endothelial cell response to angiogenic stimuli. BMC Dev. Biol. 8, 117
61. Gale, N.W., Dominguez, M.G., Noguera, I., Pan, L., Hughes, V., Valenzuela, D.M., Murphy, A.J., Adams, N.C., Lin, H.C., Holash, J. et al. (2004) 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. 101, 15949-15954
62. Xue, Y., Gao, X., Lindsell, C.E., Norton, C.R., Chang, B., Hicks, C., Gendron-Maguire, M., Rand, E.B., Weinmaster, G. and Gridley, T. (1999) Embryonic lethality and vascular defects in mice lacking the Notch ligand Jagged1. Hum. Mol. Genet. 8, 723-730
63. Fischer, A., Schumacher, N., Maier, M., Sendtner, M. and Gessler, M. (2004) The Notch target genes Hey1 and Hey2 are required for embryonic vascular development. Genes Dev. 18, 901-911