Interplay between VEGF and Nrf2 regulates angiogenesis due to intracranial venous hypertension

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Li, Liwen ^a   Pan, Hao ^a   Wang, Handong ^a   Li, Xiang ^a   Bu, Xiaomin ^a   Wang, Qiang ^a   Gao, Yongyue ^a   Wen, Guodao ^a   Zhou, Yali ^a   Cong, Zixiang ^a   Yang, Youqing ^a   Tang, Chao ^a   Liu, Zhengwei ^a  

^a NANJING UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

HEME OXYGENASE 1; HIF1A PROTEIN, RAT; HYPOXIA INDUCIBLE FACTOR 1ALPHA; NFE2L2 PROTEIN, HUMAN; TRANSCRIPTION FACTOR NRF2; VASCULOTROPIN A;

ANIMAL; BRAIN ARTERIOVENOUS MALFORMATION; BRAIN CIRCULATION; CELL CULTURE; CELL MOTION; COMPLICATION; ENDOTHELIUM CELL; HUMAN; HYPERTENSION; INSTITUTE FOR CANCER RESEARCH MOUSE; MALE; MAPK SIGNALING; METABOLISM; MICROVASCULATURE; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; CELL MOVEMENT; CELLS, CULTURED; CEREBROVASCULAR CIRCULATION; ENDOTHELIAL CELLS; HEME OXYGENASE-1; HUMANS; HYPERTENSION; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INTRACRANIAL ARTERIOVENOUS MALFORMATIONS; MALE; MAP KINASE SIGNALING SYSTEM; MICE, INBRED ICR; MICROVESSELS; NEOVASCULARIZATION, PATHOLOGIC; NF-E2-RELATED FACTOR 2; RATS, SPRAGUE-DAWLEY; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84996538407     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep37338     Document Type: Article

References (36)

1. Wedderburn, C. J., van Beijnum, J., Bhattacharya, J. J. et al. Outcome after interventional or conservative management of unruptured brain arteriovenous malformations: a prospective, population-based cohort study. The Lancet Neurology 7, 223-230 (2008).
2. Gandhi, D. et al. Intracranial dural arteriovenous fistulas: classification, imaging findings, and treatment. AJNR Am J Neuroradiol 33, 1007-1013, doi: 10.3174/ajnr.A2798 (2012).
3. Mouchtouris, N. et al. Biology of cerebral arteriovenous malformations with a focus on inflammation. J Cereb Blood Flow Metab 35, 167-175, doi: 10.1038/jcbfm.2014.179 (2015).
4. Lawton, M. T., Jacobowitz, R. & Spetzler, R. F. Redefined role of angiogenesis in the pathogenesis of dural arteriovenous malformations. J Neurosurg 87, 267-274, doi: 10.3171/jns.1997.87.2.0267 (1997).
5. Bederson, J. B. et al. Intracranial venous hypertension and the effects of venous outflow obstruction in a rat model of arteriovenous fistula. Neurosurgery 29, 341-350 (1991).
6. Herman, J. M., Spetzler, R. F., Bederson, J. B., Kurbat, J. M. & Zabramski, J. M. Genesis of a dural arteriovenous malformation in a rat model. J Neurosurg 83, 539-545, doi: 10.3171/jns.1995.83.3.0539 (1995).
7. Zhu, Y. et al. Expression of hypoxia-inducible factor-1 and vascular endothelial growth factor in response to venous hypertension. Neurosurgery 59, 687-696, discussion 687-696, doi: 10.1227/01.NEU.0000228962.68204.CF (2006).
8. Kensler, T. W., Wakabayashi, N. & Biswal, S. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu Rev Pharmacol Toxicol 47, 89-116, doi: 10.1146/annurev.pharmtox.46.120604.141046 (2007).
9. Nguyen, T., Nioi, P. & Pickett, C. B. The Nrf2-antioxidant response element signaling pathway and its activation by oxidative stress. J Biol Chem 284, 13291-13295, doi: 10.1074/jbc.R900010200 (2009).
10. Lee, J. M. & Johnson, J. A. An important role of Nrf2-ARE pathway in the cellular defense mechanism. J Biochem Mol Biol 37, 139-143 (2004).
11. Zhang, D. D. Mechanistic studies of the Nrf2-Keap1 signaling pathway. Drug Metab Rev 38, 769-789, doi: 10.1080/03602530 600971974 (2006).
12. Jin, W. et al. Erythropoietin prevents secondary brain injury induced by cortical lesion in mice: possible involvement of Nrf2 signaling pathway. An Clin Lab Sci 41, 25-32 (2011).
13. Jin, W. et al. Protective effect of tert-butylhydroquinone on cerebral inflammatory response following traumatic brain injury in mice. Injury 42, 714-718, doi: 10.1016/j.injury.2011.03.009 (2011).
14. Jin, W. et al. Effects of tert-butylhydroquinone on intestinal inflammatory response and apoptosis following traumatic brain injury in mice. Mediat Inflamm 2010, 502564, doi: 10.1155/2010/502564 (2010).
15. Lu, X. Y., Wang, H. D., Xu, J. G., Ding, K. & Li, T. Pretreatment with tert-butylhydroquinone attenuates cerebral oxidative stress in mice after traumatic brain injury. J Surg Res 188, 206-212, doi: 10.1016/j.jss.2013.11.1106 (2014).
16. Xu, J. et al. Luteolin provides neuroprotection in models of traumatic brain injury via the Nrf2-ARE pathway. Free Radical Bio Med 71, 186-195, doi: 10.1016/j.freeradbiomed.2014.03.009 (2014).
17. Uno, K. et al. Role of Nrf2 in retinal vascular development and the vaso-obliterative phase of oxygen-induced retinopathy. Exp Eye Res 90, 493-500, doi: 10.1016/j.exer.2009.12.012 (2010).
18. Ji, X. et al. Knockdown of Nrf2 suppresses glioblastoma angiogenesis by inhibiting hypoxia-induced activation of HIF-1alpha. Int J Cancer 135, 574-584, doi: 10.1002/ijc.28699 (2014).
19. Ji, X. J. et al. Knockdown of NF-E2-related factor 2 inhibits the proliferation and growth of U251MG human glioma cells in a mouse xenograft model. Oncol Rep 30, 157-164, doi: 10.3892/or.2013.2476 (2013).
20. Kim, T. H. et al. NRF2 blockade suppresses colon tumor angiogenesis by inhibiting hypoxia-induced activation of HIF-1alpha. Anticancer Res 71, 2260-2275, doi: 10.1158/0008-5472.CAN-10-3007 (2011).
21. Kweider, N. et al. Interplay between vascular endothelial growth factor (VEGF) and nuclear factor erythroid 2-related factor-2 (Nrf2): implications for preeclampsia. J Biol Chem 286, 42863-42872, doi: 10.1074/jbc.M111.286880 (2011).
22. Wei, Y. et al. Nrf2 acts cell-autonomously in endothelium to regulate tip cell formation and vascular branching. P Natl Acad Sci USA 110, E3910-E3918, doi: 10.1073/pnas.1309276110 (2013).
23. Afonyushkin, T. et al. Oxidized phospholipids regulate expression of ATF4 and VEGF in endothelial cells via NRF2-dependent mechanism: novel point of convergence between electrophilic and unfolded protein stress pathways. Arterioscl Throm VA 30, 1007-1013, doi: 10.1161/ATVBAHA.110.204354 (2010).
24. Valcarcel-Ares, M. N. et al. Disruption of Nrf2 signaling impairs angiogenic capacity of endothelial cells: implications for microvascular aging. J Gerontol A-Biol 67, 821-829, doi: 10.1093/gerona/glr229 (2012).
25. Kuang, L., Feng, J., He, G. & Jing, T. Knockdown of Nrf2 inhibits the angiogenesis of rat cardiac micro-vascular endothelial cells under hypoxic conditions. Int J Biol Sci 9, 656-665, doi: 10.7150/ijbs.5887 (2013).
26. Meng, D. et al. Arsenic promotes angiogenesis in vitro via a heme oxygenase-1-dependent mechanism. Toxicol Appl Pharm 244, 291-299, doi: 10.1016/j.taap.2010.01.004 (2010).
27. Zhang, Z. et al. Reactive oxygen species regulate FSH-induced expression of vascular endothelial growth factor via Nrf2 and HIF1alpha signaling in human epithelial ovarian cancer. Oncol Rep 29, 1429-1434, doi: 10.3892/or.2013.2278 (2013).
28. Yang, H. L. et al. Antrodia salmonea inhibits TNF-alpha-induced angiogenesis and atherogenesis in human endothelial cells through the down-regulation of NF-kappaB and up-regulation of Nrf2 signaling pathways. J Ethnopharmacol 151, 394-406, doi: 10.1016/j.jep.2013.10.052 (2014).
29. Shibuya, A. et al. Sofalcone, a gastric mucosa protective agent, increases vascular endothelial growth factor via the Nrf2-hemeoxygenase-1 dependent pathway in gastric epithelial cells. Biochem Bioph Res Co 398, 581-584, doi: 10.1016/j.bbrc.2010.06.124 (2010).
30. Gao, P. et al. Nonischemic cerebral venous hypertension promotes a pro-angiogenic stage through HIF-1 downstream genes and leukocyte-derived MMP-9. J Cerebr Blood F Met 29, 1482-1490, doi: 10.1038/jcbfm.2009.67 (2009).
31. Chen, C. H. et al. The involvement of programmed cell death 5 (PDCD5) in the regulation of apoptosis in cerebral ischemia/reperfusion injury. Cns Neurosci Ther 19, 566-576, doi: 10.1111/cns.12114 (2013).
32. Uranishi, R., Nakase, H. & Sakaki, T. Expression of angiogenic growth factors in dural arteriovenous fistula. J Neurosurg 91, 781-786, doi: 10.3171/jns.1999.91.5.0781 (1999).
33. Kojima, T. et al. The relationship between venous hypertension and expression of vascular endothelial growth factor: hemodynamic and immunohistochemical examinations in a rat venous hypertension model. Surg Neurol 68, 277-284, discussion 284, doi: 10.1016/j.surneu.2006.10.075 (2007).
34. Calabria, A. R., Weidenfeller, C., Jones, A. R., de Vries, H. E. & Shusta, E. V. Puromycin-purified rat brain microvascular endothelial cell cultures exhibit improved barrier properties in response to glucocorticoid induction. J Neurochem 97, 922-933, doi: 10.1111/j.1471-4159.2006.03793.x (2006).
35. Bustin, S. A. et al. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Biochem 55, 611-622, doi: 10.1373/clinchem.2008.112797 (2009).
36. Francescone, R. A. 3rd, Faibish, M. & Shao, R. A Matrigel-based tube formation assay to assess the vasculogenic activity of tumor cells. Journal of visualized experiments: JoVE, doi: 10.3791/3040 (2011).