Impact of Notch signaling on inflammatory responses in cardiovascular disorders

International Journal of Molecular Sciences

Volumn 14, Issue 4, 2013, Pages 6863-6888

  Quillard, Thibaut ^a   Charreau, Beatrice ^b,c,d  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b INSERM   (France)

^c NANTES UNIVERSITY HOSPITAL   (France)

^d UNIVERSITÉ DE NANTES   (France)

Author keywords

Cardiovascular diseases; Endothelial cells; Inflammation; Notch signaling; Signaling pathways; Vascular cells

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; NITRIC OXIDE; NOTCH RECEPTOR; TRANSFORMING GROWTH FACTOR BETA;

ANGIOGENESIS; APOPTOSIS; ATHEROSCLEROSIS; CARDIAC ALLOGRAFT VASCULOPATHY; CARDIOVASCULAR DISEASE; CARDIOVASCULAR INFLAMMATION; CELL ACTIVATION; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; ENDOTHELIUM CELL; HEART INFARCTION; HUMAN; HYPOXIA; IMMUNE RESPONSE; INFLAMMATION; INFLAMMATORY CELL; INNATE IMMUNITY; NONHUMAN; PATHOGENESIS; REVIEW; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; TISSUE REPAIR; VASCULITIS; ANIMAL; BIOLOGICAL MODEL; METABOLISM; PATHOLOGY;

ANIMALS; CARDIOVASCULAR DISEASES; HUMANS; INFLAMMATION; MODELS, BIOLOGICAL; RECEPTOR CROSS-TALK; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION;

EID: 84875459250     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms14046863     Document Type: Review

References (137)

1. De Celis, J.F.; Garcia-Bellido, A. Roles of the Notch gene in Drosophila wing morphogenesis. Mech. Dev. 1994, 46, 109-122.
2. Artavanis-Tsakonas, S.; Rand, M.D.; Lake, R.J. Notch signaling: Cell fate control and signal integration in development. Science 1999, 284, 770-776.
3. D'Souza, B.; Meloty-Kapella, L.; Weinmaster, G. Canonical and non-canonical Notch ligands. Curr. Top. Dev. Biol. 2010, 92, 73-129.
4. Eiraku, M.; Tohgo, A.; Ono, K.; Kaneko, M.; Fujishima, K.; Hirano, T.; Kengaku, M. DNER acts as a neuron-specific Notch ligand during Bergmann glial development. Nat. Neurosci. 2005, 8, 873-880.
5. Hu, Q.D.; Ma, Q.H.; Gennarini, G.; Xiao, Z.C. Cross-Talk between F3/contactin and Notch at axoglial interface: A role in oligodendrocyte development. Dev. Neurosci. 2006, 28, 25-33.
6. Baladron, V.; Ruiz-Hidalgo, M.J.; Nueda, M.L.; Diaz-Guerra, M.J.; Garcia-Ramirez, J.J.; Bonvini, E.; Gubina, E.; Laborda, J. dlk acts as a negative regulator of Notch1 activation through interactions with specific EGF-like repeats. Exp. Cell Res. 2005, 303, 343-359.
7. Bruckner, K.; Perez, L.; Clausen, H.; Cohen, S. Glycosyltransferase activity of Fringe modulates Notch-Delta interactions. Nature 2000, 406, 411-415.
8. Hicks, C.; Johnston, S.H.; diSibio, G.; Collazo, A.; Vogt, T.F.; Weinmaster, G. Fringe differentially modulates Jagged1 and Delta1 signalling through Notch1 and Notch2. Nat. Cell Biol. 2000, 2, 515-520.
9. Rampal, R.; Luther, K.B.; Haltiwanger, R.S. Notch signaling in normal and disease States: Possible therapies related to glycosylation. Curr. Mol. Med. 2007, 7, 427-445.
10. Van Tetering, G.; Vooijs, M. Proteolytic cleavage of Notch: "HIT and RUN". Curr. Mol. Med. 2011, 11, 255-269.
11. Nakagawa, O.; McFadden, D.G.; Nakagawa, M.; Yanagisawa, H.; Hu, T.; Srivastava, D.; Olson, E.N. Members of the HRT family of basic helix-loop-helix proteins act as transcriptional repressors downstream of Notch signaling. Proc. Natl. Acad. Sci. USA 2000, 97, 13655-13660.
12. Iso, T.; Kedes, L.; Hamamori, Y. HES and HERP families: Multiple effectors of the Notch signaling pathway. J. Cell Physiol. 2003, 194, 237-255.
13. Sprinzak, D.; Lakhanpal, A.; Lebon, L.; Santat, L.A.; Fontes, M.E.; Anderson, G.A.; Garcia-Ojalvo, J.; Elowitz, M.B. Cis-Interactions between Notch and Delta generate mutually exclusive signalling states. Nature 2010, 465, 86-90.
14. Cohen, M.; Georgiou, M.; Stevenson, N.L.; Miodownik, M.; Baum, B. Dynamic filopodia transmit intermittent Delta-Notch signaling to drive pattern refinement during lateral inhibition. Dev. Cell 2010, 19, 78-89.
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. Notch signaling is essential for vascular morphogenesis in mice. Genes Dev. 2000, 14, 1343-1352.
16. Uyttendaele, H.; Marazzi, G.; Wu, G.; Yan, Q.; Sassoon, D.; Kitajewski, J. Notch4/int-3, a mammary proto-oncogene, is an endothelial cell-specific mammalian Notch gene. Development 1996, 122, 2251-2259.
17. Shawber, C.J.; Kitajewski, J. Notch function in the vasculature: Insights from zebrafish, mouse and man. Bioessays 2004, 26, 225-234.
18. Duarte, A.; Hirashima, M.; Benedito, R.; Trindade, A.; Diniz, P.; Bekman, E.; Costa, L.; Henrique, D.; Rossant, J. Dosage-Sensitive requirement for mouse Dll4 in artery development. Genes Dev. 2004, 18, 2474-2478.
19. 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. Haploinsufficiency of delta-like 4 ligand results in embryonic lethality due to major defects in arterial and vascular development. Proc. Natl. Acad. Sci. USA 2004, 101, 15949-15954.
20. Mailhos, C.; Modlich, U.; Lewis, J.; Harris, A.; Bicknell, R.; Ish-Horowicz, D. Delta4, an endothelial specific notch ligand expressed at sites of physiological and tumor angiogenesis. Differentiation 2001, 69, 135-144.
21. Uyttendaele, H.; Ho, J.; Rossant, J.; Kitajewski, J. Vascular patterning defects associated with expression of activated Notch4 in embryonic endothelium. Proc. Natl. Acad. Sci. USA 2001, 98, 5643-5648.
22. Miele, L.; Golde, T.; Osborne, B. Notch signaling in cancer. Curr. Mol. Med. 2006, 6, 905-918.
23. Thurston, G.; Noguera-Troise, I.; Yancopoulos, G.D. The Delta paradox: DLL4 blockade leads to more tumour vessels but less tumour growth. Nat. Rev. Cancer 2007, 7, 327-331.
24. Marchant, D.J.; Boyd, J.H.; Lin, D.C.; Granville, D.J.; Garmaroudi, F.S.; McManus, B.M. Inflammation in myocardial diseases. Circ. Res. 2012, 110, 126-144.
25. Frangogiannis, N.G. The immune system and cardiac repair. Pharmacol. Res. 2008, 58, 88-111.
26. Takeshita, K.; Satoh, M.; Ii, M.; Silver, M.; Limbourg, F.P.; Mukai, Y.; Rikitake, Y.; Radtke, F.; Gridley, T.; Losordo, D.W.; et al. Critical role of endothelial Notch1 signaling in postnatal angiogenesis. Circ. Res. 2007, 100, 70-78.
27. Kratsios, P.; Catela, C.; Salimova, E.; Huth, M.; Berno, V.; Rosenthal, N.; Mourkioti, F. Distinct roles for cell-autonomous Notch signaling in cardiomyocytes of the embryonic and adult heart. Circ. Res. 2010, 106, 559-572.
28. Li, Y.; Takeshita, K.; Liu, P.Y.; Satoh, M.; Oyama, N.; Mukai, Y.; Chin, M.T.; Krebs, L.; Kotlikoff, M.I.; Radtke, F.; et al. Smooth muscle Notch1 mediates neointimal formation after vascular injury. Circulation 2009, 119, 2686-2692.
29. LaFramboise, W.A.; Bombach, K.L.; Dhir, R.J.; Muha, N.; Cullen, R.F.; Pogozelski, A.R.; Turk, D.; George, J.D.; Guthrie, R.D.; Magovern, J.A. Molecular dynamics of the compensatory response to myocardial infarct. J. Mol. Cell Cardiol. 2005, 38, 103-117.
30. Croquelois, A.; Domenighetti, A.A.; Nemir, M.; Lepore, M.; Rosenblatt-Velin, N.; Radtke, F.; Pedrazzini, T. Control of the adaptive response of the heart to stress via the Notch1 receptor pathway. J. Exp. Med. 2008, 205, 3173-3185.
31. Russell, J.L.; Goetsch, S.C.; Gaiano, N.R.; Hill, J.A.; Olson, E.N.; Schneider, J.W. A dynamic notch injury response activates epicardium and contributes to fibrosis repair. Circ. Res. 2011, 108, 51-59.
32. Li, Y.; Hiroi, Y.; Ngoy, S.; Okamoto, R.; Noma, K.; Wang, C.Y.; Wang, H.W.; Zhou, Q.; Radtke, F.; Liao, R.; et al. Notch1 in bone marrow-derived cells mediates cardiac repair after myocardial infarction. Circulation 2011, 123, 866-876.
33. Libby, P. Inflammation in atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 2012, 32, 2045-2051.
34. Fung, E.; Tang, S.M.; Canner, J.P.; Morishige, K.; Arboleda-Velasquez, J.F.; Cardoso, A.A.; Carlesso, N.; Aster, J.C.; Aikawa, M. Delta-Like 4 induces notch signaling in macrophages: Implications for inflammation. Circulation 2007, 115, 2948-2956.
35. Monsalve, E.; Perez, M.A.; Rubio, A.; Ruiz-Hidalgo, M.J.; Baladron, V.; Garcia-Ramirez, J.J.; Gomez, J.C.; Laborda, J.; Diaz-Guerra, M.J. Notch-1 up-regulation and signaling following macrophage activation modulates gene expression patterns known to affect antigen-presenting capacity and cytotoxic activity. J. Immunol. 2006, 176, 5362-5373.
36. Aoyama, T.; Takeshita, K.; Kikuchi, R.; Yamamoto, K.; Cheng, X.W.; Liao, J.K.; Murohara, T. Gamma-Secretase inhibitor reduces diet-induced atherosclerosis in apolipoprotein E-deficient mice. Biochem. Biophys. Res. Commun. 2009, 383, 216-221.
37. Fukuda, D.; Aikawa, E.; Swirski, F.K.; Novobrantseva, T.I.; Kotelianski, V.; Gorgun, C.Z.; Chudnovskiy, A.; Yamazaki, H.; Croce, K.; Weissleder, R.; et al. Notch ligand Delta-like 4 blockade attenuates atherosclerosis and metabolic disorders. Proc. Natl. Acad. Sci. USA 2012, 109, E1868-E1877.
38. Hellstrom, M.; Phng, L.K.; Hofmann, J.J.; Wallgard, E.; Coultas, L.; Lindblom, P.; Alva, J.; Nilsson, A.K.; Karlsson, L.; Gaiano, N.; et al. Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis. Nature 2007, 445, 776-780.
39. Kwon, S.M.; Alev, C.; Asahara, T. The role of notch signaling in endothelial progenitor cell biology. Trends Cardiovasc. Med. 2009, 19, 170-173.
40. Schmauss, D.; Weis, M. Cardiac allograft vasculopathy: Recent developments. Circulation 2008, 117, 2131-2141.
41. Quillard, T.; Coupel, S.; Coulon, F.; Fitau, J.; Chatelais, M.; Cuturi, M.C.; Chiffoleau, E.; Charreau, B. Impaired Notch4 activity elicits endothelial cell activation and apoptosis: Implication for transplant arteriosclerosis. Arterioscler. Thromb. Vasc. Biol. 2008, 28, 2258-2265.
42. Ando, K.; Kanazawa, S.; Tetsuka, T.; Ohta, S.; Jiang, X.; Tada, T.; Kobayashi, M.; Matsui, N.; Okamoto, T. Induction of Notch signaling by tumor necrosis factor in rheumatoid synovial fibroblasts. Oncogene 2003, 22, 7796-7803.
43. Quillard, T.; Devalliere, J.; Coupel, S.; Charreau, B. Inflammation dysregulates Notch signaling in endothelial cells: Implication of Notch2 and Notch4 to endothelial dysfunction. Biochem. Pharmacol. 2010, 80, 2032-2041.
44. Fernandez, L.; Rodriguez, S.; Huang, H.; Chora, A.; Fernandes, J.; Mumaw, C.; Cruz, E.; Pollok, K.; Cristina, F.; Price, J.E.; et al. Tumor necrosis factor-alpha and endothelial cells modulate Notch signaling in the bone marrow microenvironment during inflammation. Exp. Hematol. 2008, 36, 545-558.
45. Joutel, A.; Andreux, F.; Gaulis, S.; Domenga, V.; Cecillon, M.; Battail, N.; Piga, N.; Chapon, F.; Godfrain, C.; Tournier-Lasserve, E. The ectodomain of the Notch3 receptor accumulates within the cerebrovasculature of CADASIL patients. J. Clin. Invest. 2000, 105, 597-605.
46. Aguilera, C.; Hoya-Arias, R.; Haegeman, G.; Espinosa, L.; Bigas, A. Recruitment of IkappaBalpha to the hes1 promoter is associated with transcriptional repression. Proc. Natl. Acad. Sci. USA 2004, 101, 16537-16542.
47. Clement, N.; Gueguen, M.; Glorian, M.; Blaise, R.; Andreani, M.; Brou, C.; Bausero, P.; Limon, I. Notch3 and IL-1beta exert opposing effects on a vascular smooth muscle cell inflammatory pathway in which NF-kappaB drives crosstalk. J. Cell Sci. 2007, 120, 3352-3361.
48. Espinosa, L.; Ingles-Esteve, J.; Robert-Moreno, A.; Bigas, A. IkappaBalpha and p65 regulate the cytoplasmic shuttling of nuclear corepressors: Cross-Talk between Notch and NFkappaB pathways. Mol. Biol. Cell 2003, 14, 491-502.
49. Pucci, F.; Venneri, M.A.; Biziato, D.; Nonis, A.; Moi, D.; Sica, A.; Di Serio, C.; Naldini, L.; de Palma, M. A distinguishing gene signature shared by tumor-infiltrating Tie2-expressing monocytes, blood "resident" monocytes, and embryonic macrophages suggests common functions and developmental relationships. Blood 2009, 114, 901-914.
50. Fantin, A.; Vieira, J.M.; Gestri, G.; Denti, L.; Schwarz, Q.; Prykhozhij, S.; Peri, F.; Wilson, S.W.; Ruhrberg, C. Tissue macrophages act as cellular chaperones for vascular anastomosis downstream of VEGF-mediated endothelial tip cell induction. Blood 2010, 116, 829-840.
51. Armulik, A.; Genove, G.; Betsholtz, C. Pericytes: Developmental, physiological, and pathological perspectives, problems, and promises. Dev. Cell 2011, 21, 193-215.
52. Kim, M.Y.; Park, J.H.; Mo, J.S.; Ann, E.J.; Han, S.O.; Baek, S.H.; Kim, K.J.; Im, S.Y.; Park, J.W.; Choi, E.J.; et al. Downregulation by lipopolysaccharide of Notch signaling, via nitric oxide. J. Cell Sci. 2008, 121, 1466-1476.
53. Monsalve, E.; Ruiz-Garcia, A.; Baladron, V.; Ruiz-Hidalgo, M.J.; Sanchez-Solana, B.; Rivero, S.; Garcia-Ramirez, J.J.; Rubio, A.; Laborda, J.; Diaz-Guerra, M.J. Notch1 upregulates LPS-induced macrophage activation by increasing NF-kappaB activity. Eur. J. Immunol. 2009, 39, 2556-2570.
54. Palaga, T.; Buranaruk, C.; Rengpipat, S.; Fauq, A.H.; Golde, T.E.; Kaufmann, S.H.; Osborne, B.A. Notch signaling is activated by TLR stimulation and regulates macrophage functions. Eur. J. Immunol. 2008, 38, 174-183.
55. Mosser, D.M.; Edwards, J.P. Exploring the full spectrum of macrophage activation. Nat. Rev. Immunol. 2008, 8, 958-969.
56. Xu, H.; Zhu, J.; Smith, S.; Foldi, J.; Zhao, B.; Chung, A.Y.; Outtz, H.; Kitajewski, J.; Shi, C.; Weber, S.; et al. Notch-RBP-J signaling regulates the transcription factor IRF8 to promote inflammatory macrophage polarization. Nat. Immunol. 2012, 13, 642-650.
57. Gentle, M.E.; Rose, A.; Bugeon, L.; Dallman, M.J. Noncanonical Notch signaling modulates cytokine responses of dendritic cells to inflammatory stimuli. J. Immunol. 2012, 189, 1274-1284.
58. Kassner, N.; Krueger, M.; Yagita, H.; Dzionek, A.; Hutloff, A.; Kroczek, R.; Scheffold, A.; Rutz, S. Cutting edge: Plasmacytoid dendritic cells induce IL-10 production in T cells via the Delta-like-4/Notch axis. J. Immunol. 2010, 184, 550-554.
59. Woollard, K.J.; Geissmann, F. Monocytes in atherosclerosis: Subsets and functions. Nat. Rev. Cardiol. 2010, 7, 77-86.
60. Piggott, K.; Deng, J.; Warrington, K.; Younge, B.; Kubo, J.T.; Desai, M.; Goronzy, J.J.; Weyand, C.M. Blocking the NOTCH Pathway inhibits vascular inflammation in large-vessel vasculitis. Circulation 2011, 123, 309-318.
61. Outtz, H.H.; Wu, J.K.; Wang, X.; Kitajewski, J. Notch1 deficiency results in decreased inflammation during wound healing and regulates vascular endothelial growth factor receptor-1 and inflammatory cytokine expression in macrophages. J. Immunol. 2010, 185, 4363-4373.
62. Zen, A.A.; Oikawa, A.; Bazan-Peregrino, M.; Meloni, M.; Emanueli, C.; Madeddu, P. Inhibition of delta-like-4-mediated signaling impairs reparative angiogenesis after ischemia. Circ. Res. 2010, 107, 283-293.
63. Noseda, M.; McLean, G.; Niessen, K.; Chang, L.; Pollet, I.; Montpetit, R.; Shahidi, R.; Dorovini-Zis, K.; Li, L.; Beckstead, B.; et al. Notch activation results in phenotypic and functional changes consistent with endothelial-to-mesenchymal transformation. Circ. Res. 2004, 94, 910-917.
64. Sweeney, C.; Morrow, D.; Birney, Y.A.; Coyle, S.; Hennessy, C.; Scheller, A.; Cummins, P.M.; Walls, D.; Redmond, E.M.; Cahill, P.A. Notch 1 and 3 receptor signaling modulates vascular smooth muscle cell growth, apoptosis, and migration via a CBF-1/RBP-Jk dependent pathway. FASEB J. 2004, 18, 1421-1423.
65. Morrow, D.; Guha, S.; Sweeney, C.; Birney, Y.; Walshe, T.; O'Brien, C.; Walls, D.; Redmond, E.M.; Cahill, P.A. Notch and vascular smooth muscle cell phenotype. Circ. Res. 2008, 103, 1370-1382.
66. Proweller, A.; Pear, W.S.; Parmacek, M.S. Notch signaling represses myocardin-induced smooth muscle cell differentiation. J. Biol. Chem. 2005, 280, 8994-9004.
67. Noseda, M.; Fu, Y.; Niessen, K.; Wong, F.; Chang, L.; McLean, G.; Karsan, A. Smooth muscle alpha-actin is a direct target of Notch/CSL. Circ. Res. 2006, 98, 1468-1470.
68. Tang, Y.; Urs, S.; Liaw, L. Hairy-Related transcription factors inhibit Notch-induced smooth muscle alpha-actin expression by interfering with Notch intracellular domain/CBF-1 complex interaction with the CBF-1-binding site. Circ. Res. 2008, 102, 661-668.
69. Liu, Z.J.; Xiao, M.; Balint, K.; Soma, A.; Pinnix, C.C.; Capobianco, A.J.; Velazquez, O.C.; Herlyn, M. Inhibition of endothelial cell proliferation by Notch1 signaling is mediated by repressing MAPK and PI3K/Akt pathways and requires MAML1. FASEB J. 2006, 20, 1009-1011.
70. Noseda, M.; Chang, L.; McLean, G.; Grim, J.E.; Clurman, B.E.; Smith, L.L.; Karsan, A. Notch activation induces endothelial cell cycle arrest and participates in contact inhibition: Role of p21Cip1 repression. Mol. Cell Biol. 2004, 24, 8813-8822.
71. Benedito, R.; Trindade, A.; Hirashima, M.; Henrique, D.; da Costa, L.L.; Rossant, J.; Gill, P.S.; Duarte, A. Loss of Notch signalling induced by Dll4 causes arterial calibre reduction by increasing endothelial cell response to angiogenic stimuli. BMC Dev. Biol. 2008, 8, 117.
72. Chen, L.; Lu, W.; Wei, B.; Wang, N.; Li, T. Influence of Delta-like ligand 4/Notch signal transduction pathway upon the biological behavior of human umbilical vein endothelial cells. Zhonghua Yi Xue Za Zhi 2009, 89, 3106-3110.
73. Hanahan, D.; Folkman, J. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 1996, 86, 353-364.
74. Hobson, B.; Denekamp, J. Endothelial proliferation in tumours and normal tissues: Continuous labelling studies. Br. J. Cancer 1984, 49, 405-413.
75. Emuss, V.; Lagos, D.; Pizzey, A.; Gratrix, F.; Henderson, S.R.; Boshoff, C. KSHV manipulates Notch signaling by DLL4 and JAG1 to alter cell cycle genes in lymphatic endothelia. PLoS Pathog. 2009, 5, e1000616.
76. Campos, A.H.; Wang, W.; Pollman, M.J.; Gibbons, G.H. Determinants of Notch-3 receptor expression and signaling in vascular smooth muscle cells: Implications in cell-cycle regulation. Circ. Res. 2002, 91, 999-1006.
77. Sakata, T.; Sakaguchi, H.; Tsuda, L.; Higashitani, A.; Aigaki, T.; Matsuno, K.; Hayashi, S. Drosophila Nedd4 regulates endocytosis of notch and suppresses its ligand-independent activation. Curr. Biol. 2004, 14, 2228-2236.
78. Wang, W.; Prince, C.Z.; Hu, X.; Pollman, M.J. HRT1 modulates vascular smooth muscle cell proliferation and apoptosis. Biochem. Biophys. Res. Commun. 2003, 308, 596-601.
79. Leong, K.G.; Hu, X.; Li, L.; Noseda, M.; Larrivee, B.; Hull, C.; Hood, L.; Wong, F.; Karsan, A. Activated Notch4 inhibits angiogenesis: Role of beta 1-integrin activation. Mol. Cell Biol. 2002, 22, 2830-2841.
80. Ferran, C. Protective genes in the vessel wall: Modulators of graft survival and function. Transplantation 2006, 82, S36-S40.
81. Terraube, V.; O'Donnell, J.S.; Jenkins, P.V. Factor VIII and von Willebrand factor interaction: Biological, clinical and therapeutic importance. Haemophilia 2009, 16, 3-13.
82. MacKenzie, F.; Duriez, P.; Wong, F.; Noseda, M.; Karsan, A. Notch4 inhibits endothelial apoptosis via RBP-Jkappa-dependent and-independent pathways. J. Biol. Chem. 2004, 279, 11657-11663.
83. Quillard, T.; Devalliere, J.; Chatelais, M.; Coulon, F.; Seveno, C.; Romagnoli, M.; Nion, S.B.; Charreau, B. Notch2 signaling sensitizes endothelial cells to apoptosis by negatively regulating the key protective molecule survivin. PLoS One 2009, 4, e8244.
84. Wang, W.; Campos, A.H.; Prince, C.Z.; Mou, Y.; Pollman, M.J. Coordinate Notch3-hairy-related transcription factor pathway regulation in response to arterial injury. Mediator role of platelet-derived growth factor and ERK. J. Biol. Chem. 2002, 277, 23165-23171.
85. Heitzler, P. Biodiversity and noncanonical Notch signaling. Curr. Top. Dev. Biol. 2010, 92, 457-481.
86. Cheng, P.; Zlobin, A.; Volgina, V.; Gottipati, S.; Osborne, B.; Simel, E.J.; Miele, L.; Gabrilovich, D.I. Notch-1 regulates NF-kappaB activity in hemopoietic progenitor cells. J. Immunol. 2001, 167, 4458-4467.
87. Shin, H.M.; Minter, L.M.; Cho, O.H.; Gottipati, S.; Fauq, A.H.; Golde, T.E.; Sonenshein, G.E.; Osborne, B.A. Notch1 augments NF-kappaB activity by facilitating its nuclear retention. EMBO J. 2006, 25, 129-138.
88. Schwarzer, R.; Jundt, F. Notch and NF-kappaB signaling pathways in the biology of classical Hodgkin lymphoma. Curr. Mol. Med. 2011, 11, 236-245.
89. Wang, J.; Shelly, L.; Miele, L.; Boykins, R.; Norcross, M.A.; Guan, E. Human Notch-1 inhibits NF-kappa B activity in the nucleus through a direct interaction involving a novel domain. J. Immunol. 2001, 167, 289-295.
90. Oakley, F.; Mann, J.; Ruddell, R.G.; Pickford, J.; Weinmaster, G.; Mann, D.A. Basal expression of IkappaBalpha is controlled by the mammalian transcriptional repressor RBP-J (CBF1) and its activator Notch1. J. Biol. Chem. 2003, 278, 24359-24370.
91. Ang, H.L.; Tergaonkar, V. Notch and NFkappaB signaling pathways: Do they collaborate in normal vertebrate brain development and function? Bioessays 2007, 29, 1039-1047.
92. Johnston, D.A.; Dong, B.; Hughes, C.C. TNF induction of jagged-1 in endothelial cells is NFkappaB-dependent. Gene 2009, 435, 36-44.
93. Frantz, S.; Ertl, G.; Bauersachs, J. Mechanisms of disease: Toll-Like receptors in cardiovascular disease. Nat. Clin. Pract. Cardiovasc. Med. 2007, 4, 444-454.
94. Raymond, T.; Schaller, M.; Hogaboam, C.M.; Lukacs, N.W.; Rochford, R.; Kunkel, S.L. Toll-Like receptors, Notch ligands, and cytokines drive the chronicity of lung inflammation. Proc. Am. Thorac. Soc. 2007, 4, 635-641.
95. Henke, P.K.; Mitsuya, M.; Luke, C.E.; Elfline, M.A.; Baldwin, J.F.; Deatrick, K.B.; Diaz, J.A.; Sood, V.; Upchurch, G.R.; Wakefield, T.W.; et al. Toll-Like receptor 9 signaling is critical for early experimental deep vein thrombosis resolution. Arterioscler. Thromb. Vasc. Biol. 2011, 31, 43-49.
96. Schaller, M.A.; Neupane, R.; Rudd, B.D.; Kunkel, S.L.; Kallal, L.E.; Lincoln, P.; Lowe, J.B.; Man, Y.; Lukacs, N.W. Notch ligand Delta-like 4 regulates disease pathogenesis during respiratory viral infections by modulating Th2 cytokines. J. Exp. Med. 2007, 204, 2925-2934.
97. Ito, T.; Schaller, M.; Hogaboam, C.M.; Standiford, T.J.; Sandor, M.; Lukacs, N.W.; Chensue, S.W.; Kunkel, S.L. TLR9 regulates the mycobacteria-elicited pulmonary granulomatous immune response in mice through DC-derived Notch ligand delta-like 4. J. Clin. Invest. 2009, 119, 33-46.
98. Zhang, Q.; Wang, C.; Liu, Z.; Liu, X.; Han, C.; Cao, X.; Li, N. Notch signal suppresses Toll-like receptor-triggered inflammatory responses in macrophages by inhibiting extracellular signal-regulated kinase 1/2-mediated nuclear factor kappaB activation. J. Biol. Chem. 2012, 287, 6208-6217.
99. Gustafsson, M.V.; Zheng, X.; Pereira, T.; Gradin, K.; Jin, S.; Lundkvist, J.; Ruas, J.L.; Poellinger, L.; Lendahl, U.; Bondesson, M. Hypoxia requires notch signaling to maintain the undifferentiated cell state. Dev. Cell 2005, 9, 617-628.
100. Sahlgren, C.; Gustafsson, M.V.; Jin, S.; Poellinger, L.; Lendahl, U. Notch signaling mediates hypoxia-induced tumor cell migration and invasion. Proc. Natl. Acad. Sci. USA 2008, 105, 6392-6397.
101. Semenza, G.L. Vascular responses to hypoxia and ischemia. Arterioscler. Thromb. Vasc. Biol. 2010, 30, 648-652.
102. Hulten, L.M.; Levin, M. The role of hypoxia in atherosclerosis. Curr. Opin. Lipidol. 2009, 20, 409-414.
103. Diez, H.; Fischer, A.; Winkler, A.; Hu, C.J.; Hatzopoulos, A.K.; Breier, G.; Gessler, M. Hypoxia-Mediated activation of Dll4-Notch-Hey2 signaling in endothelial progenitor cells and adoption of arterial cell fate. Exp. Cell Res. 2007, 313, 1-9.
104. Patel, N.S.; Li, J.L.; Generali, D.; Poulsom, R.; Cranston, D.W.; Harris, A.L. Up-Regulation of delta-like 4 ligand in human tumor vasculature and the role of basal expression in endothelial cell function. Cancer Res. 2005, 65, 8690-8697.
105. Pietras, A.; von Stedingk, K.; Lindgren, D.; Pahlman, S.; Axelson, H. JAG2 induction in hypoxic tumor cells alters Notch signaling and enhances endothelial cell tube formation. Mol. Cancer Res. 2011, 9, 626-636.
106. Li, X.; Zhang, X.; Leathers, R.; Makino, A.; Huang, C.; Parsa, P.; Macias, J.; Yuan, J.X.; Jamieson, S.W.; Thistlethwaite, P.A. Notch3 signaling promotes the development of pulmonary arterial hypertension. Nat. Med. 2009, 15, 1289-1297.
107. Coleman, M.L.; Ratcliffe, P.J. Signalling cross talk of the HIF system: Involvement of the FIH protein. Curr. Pharm. Des. 2009, 15, 3904-3907.
108. Zheng, X.; Linke, S.; Dias, J.M.; Gradin, K.; Wallis, T.P.; Hamilton, B.R.; Gustafsson, M.; Ruas, J.L.; Wilkins, S.; Bilton, R.L.; et al. Interaction with factor inhibiting HIF-1 defines an additional mode of cross-coupling between the Notch and hypoxia signaling pathways. Proc. Natl. Acad. Sci. USA 2008, 105, 3368-3373.
109. Timmerman, L.A.; Grego-Bessa, J.; Raya, A.; Bertran, E.; Perez-Pomares, J.M.; Diez, J.; Aranda, S.; Palomo, S.; McCormick, F.; Izpisua-Belmonte, J.C.; et al. Notch promotes epithelial-mesenchymal transition during cardiac development and oncogenic transformation. Genes Dev. 2004, 18, 99-115.
110. Zavadil, J.; Cermak, L.; Soto-Nieves, N.; Bottinger, E.P. Integration of TGF-beta/Smad and Jagged1/Notch signalling in epithelial-to-mesenchymal transition. EMBO J. 2004, 23, 1155-1165.
111. Mount, P.F.; Kemp, B.E.; Power, D.A. Regulation of endothelial and myocardial NO synthesis by multi-site eNOS phosphorylation. J. Mol. Cell Cardiol. 2007, 42, 271-279.
112. Garg, V.; Muth, A.N.; Ransom, J.F.; Schluterman, M.K.; Barnes, R.; King, I.N.; Grossfeld, P.D.; Srivastava, D. Mutations in NOTCH1 cause aortic valve disease. Nature 2005, 437, 270-274.
113. Feng, Q.; Song, W.; Lu, X.; Hamilton, J.A.; Lei, M.; Peng, T.; Yee, S.P. Development of heart failure and congenital septal defects in mice lacking endothelial nitric oxide synthase. Circulation 2002, 106, 873-879.
114. Forstermann, U. Nitric oxide and oxidative stress in vascular disease. Pflugers Arch. 2010, 459, 923-939.
115. Chang, A.C.; Fu, Y.; Garside, V.C.; Niessen, K.; Chang, L.; Fuller, M.; Setiadi, A.; Smrz, J.; Kyle, A.; Minchinton, A.; et al. Notch initiates the endothelial-to-mesenchymal transition in the atrioventricular canal through autocrine activation of soluble guanylyl cyclase. Dev. Cell 2011, 21, 288-300.
116. Grandbarbe, L.; Michelucci, A.; Heurtaux, T.; Hemmer, K.; Morga, E.; Heuschling, P. Notch signaling modulates the activation of microglial cells. Glia 2007, 55, 1519-1530.
117. Charles, N.; Ozawa, T.; Squatrito, M.; Bleau, A.M.; Brennan, C.W.; Hambardzumyan, D.; Holland, E.C. Perivascular nitric oxide activates notch signaling and promotes stem-like character in PDGF-induced glioma cells. Cell Stem Cell 2010, 6, 141-152.
118. Ishimura, N.; Bronk, S.F.; Gores, G.J. Inducible nitric oxide synthase up-regulates Notch-1 in mouse cholangiocytes: Implications for carcinogenesis. Gastroenterology 2005, 128, 1354-1368.
119. Morga, E.; Mouad-Amazzal, L.; Felten, P.; Heurtaux, T.; Moro, M.; Michelucci, A.; Gabel, S.; Grandbarbe, L.; Heuschling, P. Jagged1 regulates the activation of astrocytes via modulation of NFkappaB and JAK/STAT/SOCS pathways. Glia 2009, 57, 1741-1753.
120. Leask, A. Potential therapeutic targets for cardiac fibrosis: TGFbeta, angiotensin, endothelin, CCN2, and PDGF, partners in fibroblast activation. Circ. Res. 2010, 106, 1675-1680.
121. Derynck, R.; Zhang, Y.E. Smad-Dependent and Smad-independent pathways in TGF-beta family signalling. Nature 2003, 425, 577-584.
122. Blokzijl, A.; Dahlqvist, C.; Reissmann, E.; Falk, A.; Moliner, A.; Lendahl, U.; Ibanez, C.F. Cross-Talk between the Notch and TGF-beta signaling pathways mediated by interaction of the Notch intracellular domain with Smad3. J. Cell Biol. 2003, 163, 723-728.
123. Itoh, F.; Itoh, S.; Goumans, M.J.; Valdimarsdottir, G.; Iso, T.; Dotto, G.P.; Hamamori, Y.; Kedes, L.; Kato, M.; ten Dijke Pt, P. Synergy and antagonism between Notch and BMP receptor signaling pathways in endothelial cells. EMBO J. 2004, 23, 541-551.
124. Fu, Y.; Chang, A.; Chang, L.; Niessen, K.; Eapen, S.; Setiadi, A.; Karsan, A. Differential regulation of transforming growth factor beta signaling pathways by Notch in human endothelial cells. J. Biol. Chem. 2009, 284, 19452-19462.
125. Tang, Y.; Urs, S.; Boucher, J.; Bernaiche, T.; Venkatesh, D.; Spicer, D.B.; Vary, C.P.; Liaw, L. Notch and transforming growth factor-beta (TGFbeta) signaling pathways cooperatively regulate vascular smooth muscle cell differentiation. J. Biol. Chem. 2010, 285, 17556-17563.
126. Kennard, S.; Liu, H.; Lilly, B. Transforming growth factor-beta (TGF-1) down-regulates Notch3 in fibroblasts to promote smooth muscle gene expression. J. Biol. Chem. 2008, 283, 1324-1333.
127. Doi, H.; Iso, T.; Shiba, Y.; Sato, H.; Yamazaki, M.; Oyama, Y.; Akiyama, H.; Tanaka, T.; Tomita, T.; Arai, M.; et al. Notch signaling regulates the differentiation of bone marrow-derived cells into smooth muscle-like cells during arterial lesion formation. Biochem. Biophys. Res. Commun. 2009, 381, 654-659.
128. Moloney, D.J.; Panin, V.M.; Johnston, S.H.; Chen, J.; Shao, L.; Wilson, R.; Wang, Y.; Stanley, P.; Irvine, K.D.; Haltiwanger, R.S.; et al. Fringe is a glycosyltransferase that modifies Notch. Nature 2000, 406, 369-375.
129. Garg, V. Molecular genetics of aortic valve disease. Curr. Opin. Cardiol. 2006, 21, 180-184.
130. McDaniell, R.; Warthen, D.M.; Sanchez-Lara, P.A.; Pai, A.; Krantz, I.D.; Piccoli, D.A.; Spinner, N.B. NOTCH2 mutations cause Alagille syndrome, a heterogeneous disorder of the notch signaling pathway. Am. J. Hum. Genet. 2006, 79, 169-173.
131. Li, L.; Krantz, I.D.; Deng, Y.; Genin, A.; Banta, A.B.; Collins, C.C.; Qi, M.; Trask, B.J.; Kuo, W.L.; Cochran, J.; et al. Alagille syndrome is caused by mutations in human Jagged1, which encodes a ligand for Notch1. Nat. Genet. 1997, 16, 243-251.
132. Peters, N.; Freilinger, T.; Opherk, C.; Pfefferkorn, T.; Dichgans, M. Enhanced L-arginine-induced vasoreactivity suggests endothelial dysfunction in CADASIL. J. Neurol. 2008, 255, 1203-1208.
133. Ridgway, J.; Zhang, G.; Wu, Y.; Stawicki, S.; Liang, W.C.; Chanthery, Y.; Kowalski, J.; Watts, R.J.; Callahan, C.; Kasman, I.; et al. Inhibition of Dll4 signalling inhibits tumour growth by deregulating angiogenesis. Nature 2006, 444, 1083-1087.
134. Scehnet, J.S.; Jiang, W.; Kumar, S.R.; Krasnoperov, V.; Trindade, A.; Benedito, R.; Djokovic, D.; Borges, C.; Ley, E.J.; Duarte, A.; et al. Inhibition of Dll4-mediated signaling induces proliferation of immature vessels and results in poor tissue perfusion. Blood 2007, 109, 4753-4760.
135. Moellering, R.E.; Cornejo, M.; Davis, T.N.; Del Bianco, C.; Aster, J.C.; Blacklow, S.C.; Kung, A.L.; Gilliland, D.G.; Verdine, G.L.; Bradner, J.E. Direct inhibition of the NOTCH transcription factor complex. Nature 2009, 462, 182-188.
136. Aste-Amezaga, M.; Zhang, N.; Lineberger, J.E.; Arnold, B.A.; Toner, T.J.; Gu, M.; Huang, L.; Vitelli, S.; Vo, K.T.; Haytko, P.; et al. Characterization of Notch1 antibodies that inhibit signaling of both normal and mutated Notch1 receptors. PLoS One 2010, 5, e9094.
137. Yan, M.; Callahan, C.A.; Beyer, J.C.; Allamneni, K.P.; Zhang, G.; Ridgway, J.B.; Niessen, K.; Plowman, G.D. Chronic DLL4 blockade induces vascular neoplasms. Nature 2010, 463, E6-E7.