Nrf2 acts cell-autonomously in endothelium to regulate tip cell formation and vascular branching

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 41, 2013, Pages

  Wei, Yanhong ^a   Gong, Junsong ^a   Thimmulappa, Rajesh K ^b   Kosmider, Beata ^c   Biswal, Shyam ^b   Duh, Elia J ^a  

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

^b Johns Hopkins University   (United States)

^c DEPARTMENT OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 2ALPHA; NOTCH RECEPTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SMOOTH MUSCLE ACTIN; TRANSCRIPTION FACTOR NRF2; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; DOWN REGULATION; ENDOTHELIUM; GENE DELETION; GENE EXPRESSION; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SPROUTING; UPREGULATION;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BLOTTING, WESTERN; BROMODEOXYURIDINE; CRYOULTRAMICROTOMY; ENDOTHELIAL CELLS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LASER CAPTURE MICRODISSECTION; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; NEOVASCULARIZATION, PHYSIOLOGIC; NF-E2-RELATED FACTOR 2; PHOSPHATIDYLINOSITOL 3-KINASES; RECEPTORS, NOTCH; RETINA; RETINAL VESSELS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84885339373     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1309276110     Document Type: Article

References (44)

1. Carmeliet P (2005) Angiogenesis in life, disease and medicine. Nature 438(7070): 932-936.
2. Gerhardt H, et al. (2003) VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J Cell Biol 161(6):1163-1177.
3. Eilken HM, Adams RH (2010) Dynamics of endothelial cell behavior in sprouting angiogenesis. Curr Opin Cell Biol 22(5):617-625.
4. Kim J, Oh WJ, Gaiano N, Yoshida Y, Gu C (2011) Semaphorin 3E-Plexin-D1 signaling regulates VEGF function in developmental angiogenesis via a feedback mechanism. Genes Dev 25(13):1399-1411.
5. Kensler TW, Wakabayashi N, Biswal S (2007) Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu Rev Pharmacol Toxicol 47:89-116.
6. DeNicola GM, et al. (2011) Oncogene-induced Nrf2 transcription promotes ROS detoxification and tumorigenesis. Nature 475(7354):106-109.
7. Mitsuishi Y, et al. (2012) Nrf2 redirects glucose and glutamine into anabolic pathways in metabolic reprogramming. Cancer Cell 22(1):66-79.
8. Tsai JJ, et al. (2013) Nrf2 regulates haematopoietic stem cell function. Nat Cell Biol 15(3):309-316.
9. Kim TH, et al. (2011) NRF2 blockade suppresses colon tumor angiogenesis by inhibiting hypoxia-induced activation of HIF-1α. Cancer Res 71(6):2260-2275.
10. Nijmeh J, Moldobaeva A, Wagner EM (2010) Role of ROS in ischemia-induced lung angiogenesis. Am J Physiol Lung Cell Mol Physiol 299(4):L535-L541.
11. Ichihara S, et al. (2010) Ablation of the transcription factor Nrf2 promotes ischemiainduced neovascularization by enhancing the inflammatory response. Arterioscler Thromb Vasc Biol 30(8):1553-1561.
12. Economopoulou M, et al. (2009) Histone H2AX is integral to hypoxia-driven neovascularization. Nat Med 15(5):553-558.
13. Furuta Y, Lagutin O, Hogan BL, Oliver GC (2000) Retina-and ventral forebrain-specific Cre recombinase activity in transgenic mice. Genesis 26(2):130-132.
14. Muzumdar MD, Tasic B, Miyamichi K, Li L, Luo L (2007) A global double-fluorescent Cre reporter mouse. Genesis 45(9):593-605.
15. Hellström M, et al. (2007) Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis. Nature 445(7129):776-780.
16. Skuli N, et al. (2012) Endothelial HIF-2α regulates murine pathological angiogenesis and revascularization processes. J Clin Invest 122(4):1427-1443.
17. Takeshita K, et al. (2007) Critical role of endothelial Notch1 signaling in postnatal angiogenesis. Circ Res 100(1):70-78.
18. Hayashi H, Kume T (2008) Foxc transcription factors directly regulate Dll4 and Hey2 expression by interacting with the VEGF-Notch signaling pathways in endothelial cells. PLoS ONE 3(6):e2401.
19. Zhang J, et al. (2011) Angiopoietin-1/Tie2 signal augments basal Notch signal controlling vascular quiescence by inducing delta-like 4 expression through AKT-mediated activation of beta-catenin. J Biol Chem 286(10):8055-8066.
20. Zhang Z, et al. (2013) Reactive oxygen species regulate FSH-induced expression of vascular endothelial growth factor via Nrf2 and HIF1α signaling in human epithelial ovarian cancer. Oncol Rep 29(4):1429-1434.
21. Uno K, et al. (2010) Role of Nrf2 in retinal vascular development and the vasoobliterative phase of oxygen-induced retinopathy. Exp Eye Res 90(4):493-500.
22. Fruttiger M (2007) Development of the retinal vasculature. Angiogenesis 10(2):77-88.
23. Valcarcel-Ares MN, et al. (2012) Disruption of Nrf2 signaling impairs angiogenic capacity of endothelial cells: implications for microvascular aging. J Gerontol A Biol Sci Med Sci 67(8):821-829.
24. Suchting S, et al. (2007) The Notch ligand Delta-like 4 negatively regulates endothelial tip cell formation and vessel branching. Proc Natl Acad Sci USA 104(9):3225-3230.
25. Lobov IB, et al. (2007) Delta-like ligand 4 (Dll4) is induced by VEGF as a negative regulator of angiogenic sprouting. Proc Natl Acad Sci USA 104(9):3219-3224.
26. Caolo V, et al. (2010) Feed-forward signaling by membrane-bound ligand receptor circuit: the case of NOTCH DELTA-like 4 ligand in endothelial cells. J Biol Chem 285(52):40681-40689.
27. Wakabayashi N, et al. (2010) Regulation of notch1 signaling by nrf2: implications for tissue regeneration. Sci Signal 3(130):ra52.
28. Phng LK, Gerhardt H (2009) Angiogenesis: A team effort coordinated by notch. Dev Cell 16(2):196-208.
29. Jeong WS, Jun M, Kong AN (2006) Nrf2: A potential molecular target for cancer chemoprevention by natural compounds. Antioxid Redox Signal 8(1-2):99-106.
30. Deeb D, Gao X, Dulchavsky SA, Gautam SC (2007) CDDO-me induces apoptosis and inhibits Akt, mTOR and NF-kappaB signaling proteins in prostate cancer cells. Anticancer Res 27(5A):3035-3044.
31. Ling X, et al. (2007) The novel triterpenoid C-28 methyl ester of 2-cyano-3, 12-dioxoolen-1, 9-dien-28-oic acid inhibits metastatic murine breast tumor growth through inactivation of STAT3 signaling. Cancer Res 67(9):4210-4218.
32. Liu Y, Gao X, Deeb D, Gautam SC (2012) Oleanane triterpenoid CDDO-Me inhibits Akt activity without affecting PDK1 kinase or PP2A phosphatase activity in cancer cells. Biochem Biophys Res Commun 417(1):570-575.
33. Kulkarni AA, et al. (2011) PPAR-γ ligands repress TGFβ-induced myofibroblast differentiation by targeting the PI3K/Akt pathway: Implications for therapy of fibrosis. PLoS ONE 6(1):e15909.
34. Wei Y, et al. (2011) Nrf2 has a protective role against neuronal and capillary degeneration in retinal ischemia-reperfusion injury. Free Radic Biol Med 51(1):216-224.
35. Kong X, et al. (2011) Enhancing Nrf2 pathway by disruption of Keap1 in myeloid leukocytes protects against sepsis. Am J Respir Crit Care Med 184(8):928-938.
36. Xu Z, et al. (2012) MEF2C ablation in endothelial cells reduces retinal vessel loss and suppresses pathologic retinal neovascularization in oxygen-induced retinopathy. Am J Pathol 180(6):2548-2560.
37. Benedito R, et al. (2009) The notch ligands Dll4 and Jagged1 have opposing effects on angiogenesis. Cell 137(6):1124-1135.
38. Stenzel D, et al. (2011) Endothelial basement membrane limits tip cell formation by inducing Dll4/Notch signalling in vivo. EMBO Rep 12(11):1135-1143.
39. Benedito R, et al. (2012) Notch-dependent VEGFR3 upregulation allows angiogenesis without VEGF-VEGFR2 signalling. Nature 484(7392):110-114.
40. Joyal JS, et al. (2011) Ischemic neurons prevent vascular regeneration of neural tissue by secreting semaphorin 3A. Blood 117(22):6024-6035.
41. Soucy KG, et al. (2010) Single exposure to radiation produces early anti-angiogenic effects in mouse aorta. Radiat Environ Biophys 49(3):397-404.
42. Kosmider B, et al. (2012) Nrf2 protects human alveolar epithelial cells against injury induced by influenza A virus. Respir Res 13:43.
43. Yoshida T, Gong J, Xu Z, Wei Y, Duh EJ (2012) Inhibition of pathological retinal angiogenesis by the integrin αvβ3 antagonist tetraiodothyroacetic acid (tetrac). Exp Eye Res 94(1):41-48.
44. Chen J, et al. (2011) Wnt signaling mediates pathological vascular growth in proliferative retinopathy. Circulation 124(17):1871-1881.