Abstract
| Original language | English |
|---|---|
| Pages (from-to) | 328-344 |
| Number of pages | 17 |
| Journal | Antioxidants and Redox Signaling |
| Volume | 27 |
| Issue number | 6 |
| DOIs | |
| Publication status | Published - 2017 |
Keywords
- aging
- Free radicals
- microRNA
- nitric oxide
- vascular
- catalase
- endothelial nitric oxide synthase
- manganese superoxide dismutase
- microRNA 200c
- sirtuin 1
- transcription factor FKHR
- aged
- animal cell
- animal experiment
- animal model
- animal tissue
- Article
- down regulation
- femoral artery
- gene targeting
- human
- human cell
- human tissue
- in vitro study
- in vivo study
- limb ischemia
- limb perfusion
- male
- mouse
- nonhuman
- oxidative stress
- priority journal
- protein acetylation
- protein interaction
- protein modification
- protein phosphorylation
- regulatory mechanism
- skin fibroblast
- transcription regulation
- upregulation
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Oxidative Stress-Induced miR-200c Disrupts the Regulatory Loop among SIRT1, FOXO1, and eNOS. / Carlomosti, F.; D'Agostino, M.; Beji, S.; Torcinaro, A.; Rizzi, R.; Zaccagnini, G.; Maimone, B.; Di Stefano, V.; De Santa, F.; Cordisco, S.; Antonini, A.; Ciarapica, R.; Dellambra, E.; Martelli, F.; Avitabile, D.; Capogrossi, M.C.; Magenta, A.
In: Antioxidants and Redox Signaling, Vol. 27, No. 6, 2017, p. 328-344.Research output: Contribution to journal › Article › peer-review
}
TY - JOUR
T1 - Oxidative Stress-Induced miR-200c Disrupts the Regulatory Loop among SIRT1, FOXO1, and eNOS
AU - Carlomosti, F.
AU - D'Agostino, M.
AU - Beji, S.
AU - Torcinaro, A.
AU - Rizzi, R.
AU - Zaccagnini, G.
AU - Maimone, B.
AU - Di Stefano, V.
AU - De Santa, F.
AU - Cordisco, S.
AU - Antonini, A.
AU - Ciarapica, R.
AU - Dellambra, E.
AU - Martelli, F.
AU - Avitabile, D.
AU - Capogrossi, M.C.
AU - Magenta, A.
N1 - Cited By :7 Export Date: 2 March 2018 CODEN: ARSIF Correspondence Address: Magenta, A.; Vascular Pathology Laboratory, Istituto Dermopatico dell'Immacolata-IRCCS, FLMM, Via dei Monti di Creta 104, Italy; email: ale.magenta@gmail.com Chemicals/CAS: catalase, 9001-05-2; endothelial nitric oxide synthase, 503473-02-7 References: Aicher, A., Heeschen, C., Mildner-Rihm, C., Urbich, C., Ihling, C., Technau-Ihling, K., Essential role of endothelial nitric oxide synthase for mobilization of stem and progenitor cells (2003) Nat Med, 9, pp. 1370-1376; Alp, N.J., Channon, K.M., Regulation of endothelial nitric oxide synthase by tetrahydrobiopterin in vascular disease (2004) Arter Thromb Vasc Biol, 24, pp. 413-420; Avitabile, D., Magenta, A., Lauri, A., Gambini, E., Spaltro, G., Vinci, M.C., Metaboloepigenetics: The emerging network in stem cell homeostasis regulation (2016) Curr Stem Cell Res Ther, 11, pp. 352-369; Avitabile, D., Ranieri, D., Nicolussi, A., D'Inzeo, S., Capriotti, A.L., Genovese, L., Peroxiredoxin 2 nuclear levels are regulated by circadian clock synchronization in human keratinocytes (2014) Int J Biochem Cell Biol, 53, pp. 24-34; Bartel, D.P., MicroRNAs: Target recognition and regulatory functions (2009) Cell, 136, pp. 215-233; Chen, Z., Shentu, T.P., Wen, L., Johnson, D.A., Shyy, J.Y., Regulation of SIRT1 by oxidative stress-responsive miRNAs and a systematic approach to identify its role in the endothelium (2013) Antioxid Redox Signal, 19, pp. 1522-1538; Choi, Y.-C., Yoon, S., Jeong, Y., Yoon, J., Baek, K., Regulation of vascular endothelial growth factor signaling by MIR-200b (2011) Mol Cells, 32, pp. 77-82; Cooper, M.E., El-Osta, A., Epigenetics: Mechanisms and implications for diabetic complications (2010) Circ Res, 107, pp. 1403-1413; Cortez, M.A., Valdecanas, D., Zhang, X., Zhan, Y., Bhardwaj, V., Calin, G.A., Therapeutic delivery of MIR-200c enhances radiosensitivity in lung cancer (2014) Mol Ther, 22, pp. 1494-1503; Couffinhal, T., Silver, M., Zheng, L.P., Kearney, M., Witzenbichler, B., Isner, J.M., Mouse model of angiogenesis (1998) Am J Pathol, 152, pp. 1667-1679; Cui, H., Kong, Y., Zhang, H., Oxidative stress, mitochondrial dysfunction, and aging (2012) J Signal Transduct, 2012, p. 646354; Dansen, T.B., Forkhead boxO transcription factors: Key players in redox signaling (2011) Antioxid Redox Signal, 14, pp. 559-561; Deanfield, J.E., Halcox, J.P., Rabelink, T.J., Endothelial function and dysfunction: Testing and clinical relevance (2007) Circulation, 115, pp. 1285-1295; Eades, G., Yao, Y., Yang, M., Zhang, Y., Chumsri, S., Zhou, Q., MIR-200a regulates SIRT1 expression and epithelial to mesenchymal transition (EMT)-like transformation in mammary epithelial cells (2011) J Biol Chem, 286, pp. 25992-26002; Fasanaro, P., D'Alessandra, Y., Di Stefano, V., Melchionna, R., Romani, S., Pompilio, G., MicroRNA-210 modulates endothelial cell response to hypoxia and inhibits the receptor tyrosine kinase ligand Ephrin-A3 (2008) J Biol Chem, 283, pp. 15878-15883; Follenzi, A., Naldini, L., HIV-based vectors (2002) Preparation and Use. 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PY - 2017
Y1 - 2017
N2 - Aims: Reactive oxygen species (ROS) play a pivotal role in different pathologic conditions, including ischemia, diabetes, and aging. We previously showed that ROS enhance miR-200c expression, causing endothelial cell (EC) apoptosis and senescence. Herein, we dissect the interaction among miR-200c and three strictly related proteins that modulate EC function and ROS production: sirtuin 1 (SIRT1), endothelial nitric oxide synthase (eNOS), and forkhead box O1 (FOXO1). Moreover, the role of miR-200c on ROS modulation was also investigated. Results: We demonstrated that miR-200c directly targets SIRT1, eNOS, and FOXO1; via this mechanism, miR-200c decreased NO and increased the acetylation of SIRT1 targets, that is, FOXO1 and p53. FOXO1 acetylation inhibited its transcriptional activity on target genes, that is, SIRT1 and the ROS scavengers, catalase and manganese superoxide dismutase. In keeping, miR-200c increased ROS production and induced p66Shc protein phosphorylation in Ser-36; this mechanism upregulated ROS and inhibited FOXO1 transcription, reinforcing this molecular circuitry. These in vitro results were validated in three in vivo models of oxidative stress, that is, human skin fibroblasts from old donors, femoral arteries from old mice, and a murine model of hindlimb ischemia. In all cases, miR-200c was higher versus control and its targets, that is, SIRT1, eNOS, and FOXO1, were downmodulated. In the mouse hindlimb ischemia model, anti-miR-200c treatment rescued these targets and improved limb perfusion. Innovation and Conclusion: miR-200c disrupts SIRT1/FOXO1/eNOS regulatory loop. This event promotes ROS production and decreases NO, contributing to endothelial dysfunction under conditions of increased oxidative stress such as aging and ischemia. © 2017, Mary Ann Liebert, Inc.
AB - Aims: Reactive oxygen species (ROS) play a pivotal role in different pathologic conditions, including ischemia, diabetes, and aging. We previously showed that ROS enhance miR-200c expression, causing endothelial cell (EC) apoptosis and senescence. Herein, we dissect the interaction among miR-200c and three strictly related proteins that modulate EC function and ROS production: sirtuin 1 (SIRT1), endothelial nitric oxide synthase (eNOS), and forkhead box O1 (FOXO1). Moreover, the role of miR-200c on ROS modulation was also investigated. Results: We demonstrated that miR-200c directly targets SIRT1, eNOS, and FOXO1; via this mechanism, miR-200c decreased NO and increased the acetylation of SIRT1 targets, that is, FOXO1 and p53. FOXO1 acetylation inhibited its transcriptional activity on target genes, that is, SIRT1 and the ROS scavengers, catalase and manganese superoxide dismutase. In keeping, miR-200c increased ROS production and induced p66Shc protein phosphorylation in Ser-36; this mechanism upregulated ROS and inhibited FOXO1 transcription, reinforcing this molecular circuitry. These in vitro results were validated in three in vivo models of oxidative stress, that is, human skin fibroblasts from old donors, femoral arteries from old mice, and a murine model of hindlimb ischemia. In all cases, miR-200c was higher versus control and its targets, that is, SIRT1, eNOS, and FOXO1, were downmodulated. In the mouse hindlimb ischemia model, anti-miR-200c treatment rescued these targets and improved limb perfusion. Innovation and Conclusion: miR-200c disrupts SIRT1/FOXO1/eNOS regulatory loop. This event promotes ROS production and decreases NO, contributing to endothelial dysfunction under conditions of increased oxidative stress such as aging and ischemia. © 2017, Mary Ann Liebert, Inc.
KW - aging
KW - Free radicals
KW - microRNA
KW - nitric oxide
KW - vascular
KW - catalase
KW - endothelial nitric oxide synthase
KW - manganese superoxide dismutase
KW - microRNA 200c
KW - sirtuin 1
KW - transcription factor FKHR
KW - aged
KW - animal cell
KW - animal experiment
KW - animal model
KW - animal tissue
KW - Article
KW - down regulation
KW - femoral artery
KW - gene targeting
KW - human
KW - human cell
KW - human tissue
KW - in vitro study
KW - in vivo study
KW - limb ischemia
KW - limb perfusion
KW - male
KW - mouse
KW - nonhuman
KW - oxidative stress
KW - priority journal
KW - protein acetylation
KW - protein interaction
KW - protein modification
KW - protein phosphorylation
KW - regulatory mechanism
KW - skin fibroblast
KW - transcription regulation
KW - upregulation
U2 - 10.1089/ars.2016.6643
DO - 10.1089/ars.2016.6643
M3 - Article
VL - 27
SP - 328
EP - 344
JO - Antioxidants and Redox Signaling
JF - Antioxidants and Redox Signaling
SN - 1523-0864
IS - 6
ER -