Nrf2 regulates angiogenesis: Effect on endothelial cells, bone marrow-derived proangiogenic cells and hind limb ischemia

Antioxidants and Redox Signaling

Volumn 20, Issue 11, 2014, Pages 1693-1708

  Florczyk, Urszula ^a   Jazwa, Agnieszka ^a   Maleszewska, Monika ^a   Mendel, Mateusz ^a   Szade, Krzysztof ^a   Kozakowska, Magdalena ^a   Grochot Przeczek, Anna ^a   Viscardi, Monika ^a   Czauderna, Szymon ^a   Bukowska Strakova, Karolina ^a   Kotlinowski, Jerzy ^a   Jozkowicz, Alicja ^a   Loboda, Agnieszka ^a   Dulak, Jozef ^a  

^a JAGIELLONIAN UNIVERSITY   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; ETODOLAC; HEME OXYGENASE 1; TRANSCRIPTION FACTOR NRF2; TRANSCRIPTOME;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BLOOD FLOW; BONE MARROW CELL; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; ENDOTHELIUM CELL; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; INFLAMMATION; LIMB ISCHEMIA; MALE; MOUSE; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; OXIDATIVE STRESS; PRIORITY JOURNAL; PROANGIOGENIC CELL; PROTEIN EXPRESSION; REVASCULARIZATION;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; ANTIOXIDANTS; AORTA; BONE MARROW CELLS; CELLS, CULTURED; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; FEMALE; FEMORAL ARTERY; GENE EXPRESSION; HEME OXYGENASE-1; HINDLIMB; HUMANS; ISCHEMIA; MALE; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUSCLE, SKELETAL; NEOVASCULARIZATION, PHYSIOLOGIC; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; STEM CELLS; TRANSCRIPTOME;

EID: 84896327937     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2013.5219     Document Type: Article

References (56)

1. Ades EW, Candal FJ, Swerlick RA, George VG, Summers S, Bosse DC, and Lawley TJ. HMEC-1: establishment of an immortalized human microvascular endothelial cell line. J Invest Dermatol 99: 683-690, 1992.
2. Afonyushkin T, Oskolkova OV, Philippova M, Resink TJ, Erne P, Binder BR, and Bochkov VN. Oxidized phospho-lipids regulate expression of ATF4 and VEGF in endothelial cells via NRF2-dependent mechanism: novel point of convergence between electrophilic and unfolded protein stress pathways. Arterioscler Thromb Vasc Biol 30: 1007-1013, 2010.
3. Aicher A, Heeschen C, Mildner-Rihm C, Urbich C, Ihling C, Technau-Ihling K, Zeiher AM, and Dimmeler S. Essential role of endothelial nitric oxide synthase for mobilization of stem and progenitor cells. Nat Med 9: 1370-1376, 2003.
4. Alam J, Stewart D, Touchard C, Boinapally S, Choi AM, and Cook JL. Nrf2, a Cap'n'Collar transcription factor, regulates induction of the heme oxygenase-1 gene. J Biol Chem 274: 26071-26078, 1999.
5. Asahara T, Masuda H, Takahashi T, Kalka C, Pastore C, Silver M, Kearne M, Magner M, and Isner JM. Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neo-vascularization. Circ Res 85: 221-228, 1999.
6. Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, Witzenbichler B, Schatteman G, and Isner JM. Isolation of putative progenitor endothelial cells for angiogenesis. Science 275: 964-967, 1997.
7. Asahara T, Takahashi T, Masuda H, Kalka C, Chen D, Iwaguro H, Inai Y, Silver M, and Isner JM. VEGF contributes to postnatal neovascularization by mobilizing bone marrow-derived endothelial progenitor cells. EMBO J 18: 3964-3972, 1999.
8. Baird L and Dinkova-Kostova AT. The cytoprotective role of the Keap1-Nrf2 pathway. Arch Toxicol 85: 241-272, 2011.
9. Bradley JR. TNF-mediated inflammatory disease. J Pathol 214: 149-160, 2008.
10. Ceradini DJ, Kulkarni AR, Callaghan MJ, Tepper OM, Bas-tidas N, Kleinman ME, Capla JM, Galiano RD, Levine JP, and Gurtner GC. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat Med 10: 858-864, 2004.
11. Chen TG, Zhong ZY, Sun GF, Zhou YX, and Zhao Y. Effects of tumour necrosis factor-alpha on activity and nitric oxide synthase of endothelial progenitor cells from peripheral blood. Cell Prolif 44: 352-359, 2011.
12. Dernbach E, Urbich C, Brandes RP, Hofmann WK, Zeiher AM, and Dimmeler S. Antioxidative stress-associated genes in circulating progenitor cells: evidence for enhanced resistance against oxidative stress. Blood 104: 3591-3597, 2004.
13. Deshane J, Chen S, Caballero S, Grochot-Przeczek A, Was H, Li Calzi S, Lach R, Hock TD, Chen B, Hill-Kapturczak N, Siegal GP, Dulak J, Jozkowicz A, Grant MB, and Agarwal A. Stromal cell-derived factor 1 promotes angiogenesis via a heme oxygenase 1-dependent mechanism. J Exp Med 204: 605-618, 2007.
14. Dinkova-Kostova AT and Talalay P. NAD(P)H:quinone acceptor oxidoreductase 1 (NQO1), a multifunctional antioxi-dant enzyme and exceptionally versatile cytoprotector. Arch Biochem Biophys 501: 116-123, 2010.
15. Dulak J, Jozkowicz A, Foresti R, Kasza A, Frick M, Huk I, Green CJ, Pachinger O, Weidinger F, and Motterlini R. Heme oxygenase activity modulates vascular endothelial growth factor synthesis in vascular smooth muscle cells. Antioxid Redox Signal 4: 229-240, 2002.
16. Eliason JL and Wakefield TW. Metabolic consequences of acute limb ischemia and their clinical implications. Semin Vasc Surg 22: 29-33, 2009.
17. Florczyk U, Czauderna S, Stachurska A, Tertil M, Nowak W, Kozakowska M, Poellinger L, Jozkowicz A, Loboda A, and Dulak J. Opposite effects of HIF-1alpha and HIF-2alpha on the regulation of IL-8 expression in endothelial cells. Free Radic Biol Med 51: 1882-1892, 2011.
18. Freeman MR, Schneck FX, Gagnon ML, Corless C, Soker S, Niknejad K, Peoples GE, and Klagsbrun M. Peripheral blood T lymphocytes and lymphocytes infiltrating human cancers express vascular endothelial growth factor: a potential role for T cells in angiogenesis. Cancer Res 55: 4140-4145, 1995.
19. Galasso G, Schiekofer S, Sato K, Shibata R, Handy DE, Ouchi N, Leopold JA, Loscalzo J, and Walsh K. Impaired angio-genesis in glutathione peroxidase-1-deficient mice is associated with endothelial progenitor cell dysfunction. Circ Res 98: 254-261, 2006.
20. He T, Peterson TE, Holmuhamedov EL, Terzic A, Caplice NM, Oberley LW, and Katusic ZS. Human endothelial progenitor cells tolerate oxidative stress due to intrinsically high expression of manganese superoxide dismutase. Ar-terioscler Thromb Vasc Biol 24: 2021-2027, 2004.
21. He T, Peterson TE, and Katusic ZS. Paracrine mitogenic effect of human endothelial progenitor cells: role of interleukin-8. Am J Physiol Heart Circ Physiol 289: H968-H972, 2005.
22. Heissig B, Hattori K, Dias S, Friedrich M, Ferris B, Hackett NR, Crystal RG, Besmer P, Lyden D, Moore MA, Werb Z, and Rafii S. Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand. Cell 109: 625-637, 2002.
23. Ichihara S, Yamada Y, Liu F, Murohara T, Itoh K, Yamamoto M, and Ichihara G. Ablation of the transcription factor Nrf2 promotes ischemia-induced neovascularization by enhancing the inflammatory response. Arterioscler Thromb Vasc Biol 30: 1553-1561, 2010.
24. Imanishi T, Tsujioka H, and Akasaka T. Endothelial progenitor cells dysfunction and senescence: contribution to oxidative stress. Curr Cardiol Rev 4: 275-286, 2008.
25. Itoh K, Wakabayashi N, Katoh Y, Ishii T, Igarashi K, Engel JD, and Yamamoto M. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev 13: 76-86, 1999.
26. Jazwa A, Jozkowicz A, and Dulak J. New vectors and strategies for cardiovascular gene therapy. Curr Gene Ther 7: 7-23, 2007.
27. Jazwa A, Stepniewski J, Zamykal M, Jagodzinska J, Meloni M, Emanueli C, Jozkowicz A, and Dulak J. Pre-emptive hypoxia-regulated HO-1 gene therapy improves post-ischaemic limb perfusion and tissue regeneration in mice. Cardiovasc Res 97: 115-124, 2013.
28. Jiang M, Wang B, Wang C, He B, Fan H, Guo TB, Shao Q, Gao L, and Liu Y. Angiogenesis by transplantation of HIF-1 alpha modified EPCs into ischemic limbs. J Cell Biochem 103: 321-334, 2008.
29. Jozkowicz A, Huk I, Nigisch A, Weigel G, Dietrich W, Motterlini R, and Dulak J. Heme oxygenase and angiogenic activity of endothelial cells: stimulation by carbon monoxide and inhibition by tin protoporphyrin-IX. Antioxid Redox Signal 5: 155-162, 2003.
30. Kim TH, Hur EG, Kang SJ, Kim JA, Thapa D, Lee YM, Ku SK, Jung Y, and Kwak MK. NRF2 blockade suppresses colon tumor angiogenesis by inhibiting hypoxia-induced activation of HIF-1alpha. Cancer Res 71: 2260-2275, 2011.
31. Kozakowska M, Ciesla M, Stefanska A, Skrzypek K, Was H, Jazwa A, Grochot-Przeczek A, Kotlinowski J, Szymula A, Bartelik A, Mazan M, Yagensky O, Florczyk U, Lemke K, Zebzda A, Dyduch G, Nowak W, Szade K, Stepniewski J, Majka M, Derlacz R, Loboda A, Dulak J, and Jozkowicz A. Heme oxygenase-1 inhibits myoblast differentiation by targeting myomirs. Antioxid Redox Signal 16: 113-127, 2011.
32. Lee JM, Hanson JM, Chu WA, and Johnson JA. Phosphati-dylinositol 3-kinase, not extracellular signal-regulated ki-nase, regulates activation of the antioxidant-responsive element in IMR-32 human neuroblastoma cells. J Biol Chem 276: 20011-20016, 2001.
33. Lin HH, Chen YH, Chang PF, Lee YT, Yet SF, and Chau LY. Heme oxygenase-1 promotes neovascularization in ischemic heart by coinduction of VEGF and SDF-1. J Mol Cell Cardiol 45: 44-55, 2008.
34. Lin HH, Chen YH, Yet SF, and Chau LY. After vascular injury, heme oxygenase-1/carbon monoxide enhances reendothelialization via promoting mobilization of circulating endothelial progenitor cells. J Thromb Haemost 7: 1401-1408, 2009.
35. Loboda A, Jazwa A, Grochot-Przeczek A, Rutkowski AJ, Cisowski J, Agarwal A, Jozkowicz A, and Dulak J. Heme oxygenase-1 and the vascular bed: from molecular mechanisms to therapeutic opportunities. Antioxid Redox Signal 10: 1767-1812, 2008.
36. Loboda A, Stachurska A, Florczyk U, Rudnicka D, Jazwa A, Wegrzyn J, Kozakowska M, Stalinska K, Poellinger L, Le-vonen AL, Yla-Herttuala S, Jozkowicz A, and Dulak J. HIF-1 induction attenuates Nrf2-dependent IL-8 expression in human endothelial cells. Antioxid Redox Signal 11: 1501-1517, 2009.
37. Losordo DW and Dimmeler S. Therapeutic angiogenesis and vasculogenesis for ischemic disease: part II: cell-based therapies. Circulation 109: 2692-2697, 2004.
38. Madeddu P, Emanueli C, Spillmann F, Meloni M, Bouby N, Richer C, Alhenc-Gelas F, Van Weel V, Eefting D, Quax PH, Hu Y, Xu Q, Hemdahl AL, van Golde J, Huijberts M, de Lussanet Q, Struijker Boudier H, Couffinhal T, Duplaa C, Chimenti S, Staszewsky L, Latini R, Baumans V, and Levy BI. Murine models of myocardial and limb ischemia: diagnostic end-points and relevance to clinical problems. Vascul Pharmacol 45: 281-301, 2006.
39. Merchant AA, Singh A, Matsui W, and Biswal S. The redox-sensitive transcription factor Nrf2 regulates murine hema-topoietic stem cell survival independently of ROS levels. Blood 118: 6572-6579, 2011.
40. Motohashi H and Yamamoto M. Nrf2-Keap1 defines a physiologically important stress response mechanism. Trends Mol Med 10: 549-557, 2004.
41. Napoli C, Hayashi T, Cacciatore F, Casamassimi A, Casini C, Al-Omran M, and Ignarro LJ. Endothelial progenitor cells as therapeutic agents in the microcirculation: an update. Atherosclerosis 215: 9-22, 2011.
42. Nijmeh J, Moldobaeva A, and Wagner EM. Role of ROS in ischemia-induced lung angiogenesis. Am J Physiol Lung Cell Mol Physiol 299: L535-L541, 2010.
43. Peterson RT and Schreiber SL. Translation control: connecting mitogens and the ribosome. Curr Biol 8: R248-R250, 1998.
44. Purhonen S, Palm J, Rossi D, Kaskenpaa N, Rajantie I, Yla-Herttuala S, Alitalo K, Weissman IL, and Salven P. Bone marrow-derived circulating endothelial precursors do not contribute to vascular endothelium and are not needed for tumor growth. Proc Natl Acad Sci USA 105: 6620-6625, 2008.
45. Spinetti G, Fortunato O, Caporali A, Shantikumar S, Marchetti M, Meloni M, Floris I, Descamps B, Sangalli E, Vono R, Faglia E, Specchia C, Pintus G, Madeddu PR, and Emanueli C. MicroRNA-15a and MicroRNA-16 impair human circulating pro-angiogenic cell (PAC) functions and are increased in the PACs and serum of patients with critical limb ischemia. Circ Res 112: 335-346, 2013.
46. Takahashi T, Kalka C, Masuda H, Chen D, Silver M, Kearney M, Magner M, Isner JM, and Asahara T. Ischemia-and cytokine-induced mobilization of bone marrow-derived en-dothelial progenitor cells for neovascularization. Nat Med 5: 434-438, 1999.
47. Tongers J, Knapp JM, Korf M, Kempf T, Limbourg A, Lim-bourg FP, Li Z, Fraccarollo D, Bauersachs J, Han X, Drexler H, Fiedler B, and Wollert KC. Haeme oxygenase promotes progenitor cell mobilization, neovascularization, and functional recovery after critical hindlimb ischaemia in mice. Cardiovasc Res 78: 294-300, 2008.
48. Uno K, Prow TW, Bhutto IA, Yerrapureddy A, McLeod DS, Yamamoto M, Reddy SP, and Lutty GA. Role of Nrf2 in retinal vascular development and the vaso-obliterative phase of oxygen-induced retinopathy. Exp Eye Res 90: 493-500, 2010.
49. Valcarcel-Ares MN, Gautam T, Warrington JP, Bailey-Downs L, Sosnowska D, de Cabo R, Losonczy G, Sonntag WE, Ungvari Z, and Csiszar A. Disruption of Nrf2 signaling impairs angiogenic capacity of endothelial cells: implications for microvascular aging. J Gerontol A Biol Sci Med Sci 67:821-829, 2012.
50. Wajant H. The role of TNF in cancer. Results Probl Cell Differ 49: 1-15, 2009.
51. Wara AK, Croce K, Foo S, Sun X, Icli B, Tesmenitsky Y, Esen F, Rosenzweig A, and Feinberg MW. Bone marrow-derived CMPs and GMPs represent highly functional proangiogenic cells: implications for ischemic cardiovascular disease. Blood 118: 6461-6464, 2011.
52. Wickersheim A, Kerber M, de Miguel LS, Plate KH, and Machein MR. Endothelial progenitor cells do not contribute to tumor endothelium in primary and metastatic tumors. Int J Cancer 125: 1771-1777, 2009.
53. Yamaguchi J, Kusano KF, Masuo O, Kawamoto A, Silver M, Murasawa S, Bosch-Marce M, Masuda H, Losordo DW, Is-ner JM, and Asahara T. Stromal cell-derived factor-1 effects on ex vivo expanded endothelial progenitor cell recruitment for ischemic neovascularization. Circulation 107: 1322-1328, 2003.
54. Yao EH, Yu Y, and Fukuda N. Oxidative stress on progenitor and stem cells in cardiovascular diseases. Curr Pharm Biotechnol 7: 101-108, 2006.
55. Yu R, Chen C, Mo YY, Hebbar V, Owuor ED, Tan TH, and Kong AN. Activation of mitogen-activated protein kinase pathways induces antioxidant response element-mediated gene expression via a Nrf2-dependent mechanism. J Biol Chem 275: 39907-39913, 2000.
56. Zhang X, Chen X, Song H, Chen HZ, and Rovin BH. Activation of the Nrf2/antioxidant response pathway increases IL-8 expression. Eur J Immunol 35: 3258-3267, 2005.