Research progress of ferroptosis in cardiovascular diseases_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

WANG Xiaodi ,  CHEN Xin

Department of Thoracic and Cardiovascular Surgery, Nanjing First Hospital, Nanjing Medical University, Nanjing, 210006, P. R. China;

Corresponding author：

CHEN Xin, Email: stevecx@njmu.edu.cn

Keywords：

Ferroptosis; iron storage; lipid peroxidation; cardiovascular diseases

DOI：

10.7507/1007-4848.202102029

Video：

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Cardiovascular disease is a leading cause of death in Chinese population. It is of great significance to further explore the pathogenesis of cardiovascular diseases. Ferroptosis is a recently discovered iron-dependent and non-apoptotic form of regulated cell death, which exerts a regulatory role in a variety of biological events. Some studies have shown that ferroptosis plays an important role in the development of cardiovascular diseases. According to newly scientific reports, we summarized the mechanism and regulation in ferroptosis, and reviewed the results of ferroptosis in common cardiovascular diseases such as cardiac ischemia-reperfusion/myocardial infarction, cardiomyopathy, cardiac hypertrophy, atherosclerosis and abdominal aortic aneurysm.

Citation： WANG Xiaodi, CHEN Xin. Research progress of ferroptosis in cardiovascular diseases. Chinese Journal of Clinical Thoracic and Cardiovascular Surgery, 2022, 29(4): 497-501. doi: 10.7507/1007-4848.202102029 Copy

1.	中国心血管健康与疾病报告编写组. 中国心血管健康与疾病报告2019概要. 中国循环杂志, 2020, 35(9): 833-854.
2.	Stockwell BR, Jiang X, Gu W. Emerging mechanisms and disease relevance of ferroptosis. Trends Cell Biol, 2020, 30(6): 478-490.
3.	Anandhan A, Dodson M, Schmidlin CJ, et al. Breakdown of an ironclad defense system: The critical role of NRF2 in mediating ferroptosis. Cell Chem Biol, 2020, 27(4): 436-447.
4.	Dixon SJ, Lemberg KM, Lamprecht MR, et al. Ferroptosis: An iron-dependent form of nonapoptotic cell death. Cell, 2012, 149(5): 1060-1072.
5.	Chen X, Kang R, Kroemer G, et al. Broadening horizons: The role of ferroptosis in cancer. Nat Rev Clin Oncol, 2021, 18(5): 280-296.
6.	Nakamura T, Naguro I, Ichijo H. Iron homeostasis and iron-regulated ROS in cell death, senescence and human diseases. Biochim Biophys Acta Gen Subj, 2019, 1863(9): 1398-1409.
7.	Yu H, Yang C, Jian L, et al. Sulfasalazine-induced ferroptosis in breast cancer cells is reduced by the inhibitory effect of estrogen receptor on the transferrin receptor. Oncol Rep, 2019, 42(2): 826-838.
8.	Wang H, An P, Xie E, et al. Characterization of ferroptosis in murine models of hemochromatosis. Hepatology, 2017, 66(2): 449-465.
9.	Bebber CM, Müller F, Prieto Clemente L, et al. Ferroptosis in cancer cell biology. Cancers (Basel), 2020, 12(1): 164.
10.	Kagan VE, Mao G, Qu F, et al. Oxidized arachidonic and adrenic PEs navigate cells to ferroptosis. Nat Chem Biol, 2017, 13(1): 81-90.
11.	Doll S, Proneth B, Tyurina YY, et al. ACSL4 dictates ferroptosis sensitivity by shaping cellular lipid composition. Nat Chem Biol, 2017, 13(1): 91-98.
12.	Friedmann Angeli JP, Schneider M, Proneth B, et al. Inactivation of the ferroptosis regulator Gpx4 triggers acute renal failure in mice. Nat Cell Biol, 2014, 16(12): 1180-1191.
13.	Ursini F, Maiorino M. Lipid peroxidation and ferroptosis: The role of GSH and GPx4. Free Radic Biol Med, 2020, 152: 175-185.
14.	Fujii J, Homma T, Kobayashi S. Ferroptosis caused by cysteine insufficiency and oxidative insult. Free Radic Res, 2019: 1-12.
15.	Proneth B, Conrad M. Ferroptosis and necroinflammation, a yet poorly explored link. Cell Death Differ, 2019, 26(1): 14-24.
16.	Takashi Y, Tomita K, Kuwahara Y, et al. Mitochondrial dysfunction promotes aquaporin expression that controls hydrogen peroxide permeability and ferroptosis. Free Radic Biol Med, 2020, 161: 60-70.
17.	Xie LL, Shi F, Tan Z, et al. Mitochondrial network structure homeostasis and cell death. Cancer Sci, 2018, 109(12): 3686-3694.
18.	Gao M, Yi J, Zhu J, et al. Role of mitochondria in ferroptosis. Mol Cell, 2019, 73(2): 354-363.
19.	Gao M, Monian P, Quadri N, et al. Glutaminolysis and transferrin regulate ferroptosis. Mol Cell, 2015, 59(2): 298-308.
20.	Li W, Feng G, Gauthier JM, et al. Ferroptotic cell death and TLR4/Trif signaling initiate neutrophil recruitment after heart transplantation. J Clin Invest, 2019, 129(6): 2293-2304.
21.	Feng Y, Madungwe NB, Imam Aliagan AD, et al. Liproxstatin-1 protects the mouse myocardium against ischemia/reperfusion injury by decreasing VDAC1 levels and restoring GPX4 levels. Biochem Biophys Res Commun, 2019, 520(3): 606-611.
22.	Li W, Li W, Leng Y, et al. Ferroptosis is involved in diabetes myocardial ischemia/reperfusion injury through endoplasmic reticulum stress. DNA Cell Biol, 2020, 39(2): 210-225.
23.	Tang LJ, Zhou YJ, Xiong XM, et al. Ubiquitin-specific protease 7 promotes ferroptosis via activation of the p53/TfR1 pathway in the rat hearts after ischemia/reperfusion. Free Radic Biol Med, 2021, 162: 339-352.
24.	Park TJ, Park JH, Lee GS, et al. Quantitative proteomic analyses reveal that GPX4 downregulation during myocardial infarction contributes to ferroptosis in cardiomyocytes. Cell Death Dis, 2019, 10(11): 835.
25.	Nishizawa H, Matsumoto M, Shindo T, et al. Ferroptosis is controlled by the coordinated transcriptional regulation of glutathione and labile iron metabolism by the transcription factor BACH1. J Biol Chem, 2020, 295(1): 69-82.
26.	Tadokoro T, Ikeda M, Ide T, et al. Mitochondria-dependent ferroptosis plays a pivotal role in doxorubicin cardiotoxicity. JCI Insight, 2020, 5(9): e132747.
27.	Fang X, Wang H, Han D, et al. Ferroptosis as a target for protection against cardiomyopathy. Proc Natl Acad Sci U S A, 2019, 116(7): 2672-2680.
28.	Fang X, Cai Z, Wang H, et al. Loss of cardiac ferritin H facilitates cardiomyopathy via Slc7a11-mediated ferroptosis. Circ Res, 2020, 127(4): 486-501.
29.	Wang J, Deng B, Liu Q, et al. Pyroptosis and ferroptosis induced by mixed lineage kinase 3 (MLK3) signaling in cardiomyocytes are essential for myocardial fibrosis in response to pressure overload. Cell Death Dis, 2020, 11(7): 574.
30.	Yin Z, Ding G, Chen X, et al. Beclin1 haploinsufficiency rescues low ambient temperature-induced cardiac remodeling and contractile dysfunction through inhibition of ferroptosis and mitochondrial injury. Metabolism, 2020, 113: 154397.
31.	Bai T, Li M, Liu Y, et al. Inhibition of ferroptosis alleviates atherosclerosis through attenuating lipid peroxidation and endothelial dysfunction in mouse aortic endothelial cell. Free Radic Biol Med, 2020, 160: 92-102.
32.	Sawada H, Hao H, Naito Y, et al. Aortic iron overload with oxidative stress and inflammation in human and murine abdominal aortic aneurysm. Arterioscler Thromb Vasc Biol, 2015, 35(6): 1507-1514.
33.	Sampilvanjil A, Karasawa T, Yamada N, et al. Cigarette smoke extract induces ferroptosis in vascular smooth muscle cells. Am J Physiol Heart Circ Physiol, 2020, 318(3): H508-H518.

1. 中国心血管健康与疾病报告编写组. 中国心血管健康与疾病报告2019概要. 中国循环杂志, 2020, 35(9): 833-854.
2. Stockwell BR, Jiang X, Gu W. Emerging mechanisms and disease relevance of ferroptosis. Trends Cell Biol, 2020, 30(6): 478-490.
3. Anandhan A, Dodson M, Schmidlin CJ, et al. Breakdown of an ironclad defense system: The critical role of NRF2 in mediating ferroptosis. Cell Chem Biol, 2020, 27(4): 436-447.
4. Dixon SJ, Lemberg KM, Lamprecht MR, et al. Ferroptosis: An iron-dependent form of nonapoptotic cell death. Cell, 2012, 149(5): 1060-1072.
5. Chen X, Kang R, Kroemer G, et al. Broadening horizons: The role of ferroptosis in cancer. Nat Rev Clin Oncol, 2021, 18(5): 280-296.
6. Nakamura T, Naguro I, Ichijo H. Iron homeostasis and iron-regulated ROS in cell death, senescence and human diseases. Biochim Biophys Acta Gen Subj, 2019, 1863(9): 1398-1409.
7. Yu H, Yang C, Jian L, et al. Sulfasalazine-induced ferroptosis in breast cancer cells is reduced by the inhibitory effect of estrogen receptor on the transferrin receptor. Oncol Rep, 2019, 42(2): 826-838.
8. Wang H, An P, Xie E, et al. Characterization of ferroptosis in murine models of hemochromatosis. Hepatology, 2017, 66(2): 449-465.
9. Bebber CM, Müller F, Prieto Clemente L, et al. Ferroptosis in cancer cell biology. Cancers (Basel), 2020, 12(1): 164.
10. Kagan VE, Mao G, Qu F, et al. Oxidized arachidonic and adrenic PEs navigate cells to ferroptosis. Nat Chem Biol, 2017, 13(1): 81-90.
11. Doll S, Proneth B, Tyurina YY, et al. ACSL4 dictates ferroptosis sensitivity by shaping cellular lipid composition. Nat Chem Biol, 2017, 13(1): 91-98.
12. Friedmann Angeli JP, Schneider M, Proneth B, et al. Inactivation of the ferroptosis regulator Gpx4 triggers acute renal failure in mice. Nat Cell Biol, 2014, 16(12): 1180-1191.
13. Ursini F, Maiorino M. Lipid peroxidation and ferroptosis: The role of GSH and GPx4. Free Radic Biol Med, 2020, 152: 175-185.
14. Fujii J, Homma T, Kobayashi S. Ferroptosis caused by cysteine insufficiency and oxidative insult. Free Radic Res, 2019: 1-12.
15. Proneth B, Conrad M. Ferroptosis and necroinflammation, a yet poorly explored link. Cell Death Differ, 2019, 26(1): 14-24.
16. Takashi Y, Tomita K, Kuwahara Y, et al. Mitochondrial dysfunction promotes aquaporin expression that controls hydrogen peroxide permeability and ferroptosis. Free Radic Biol Med, 2020, 161: 60-70.
17. Xie LL, Shi F, Tan Z, et al. Mitochondrial network structure homeostasis and cell death. Cancer Sci, 2018, 109(12): 3686-3694.
18. Gao M, Yi J, Zhu J, et al. Role of mitochondria in ferroptosis. Mol Cell, 2019, 73(2): 354-363.
19. Gao M, Monian P, Quadri N, et al. Glutaminolysis and transferrin regulate ferroptosis. Mol Cell, 2015, 59(2): 298-308.
20. Li W, Feng G, Gauthier JM, et al. Ferroptotic cell death and TLR4/Trif signaling initiate neutrophil recruitment after heart transplantation. J Clin Invest, 2019, 129(6): 2293-2304.
21. Feng Y, Madungwe NB, Imam Aliagan AD, et al. Liproxstatin-1 protects the mouse myocardium against ischemia/reperfusion injury by decreasing VDAC1 levels and restoring GPX4 levels. Biochem Biophys Res Commun, 2019, 520(3): 606-611.
22. Li W, Li W, Leng Y, et al. Ferroptosis is involved in diabetes myocardial ischemia/reperfusion injury through endoplasmic reticulum stress. DNA Cell Biol, 2020, 39(2): 210-225.
23. Tang LJ, Zhou YJ, Xiong XM, et al. Ubiquitin-specific protease 7 promotes ferroptosis via activation of the p53/TfR1 pathway in the rat hearts after ischemia/reperfusion. Free Radic Biol Med, 2021, 162: 339-352.
24. Park TJ, Park JH, Lee GS, et al. Quantitative proteomic analyses reveal that GPX4 downregulation during myocardial infarction contributes to ferroptosis in cardiomyocytes. Cell Death Dis, 2019, 10(11): 835.
25. Nishizawa H, Matsumoto M, Shindo T, et al. Ferroptosis is controlled by the coordinated transcriptional regulation of glutathione and labile iron metabolism by the transcription factor BACH1. J Biol Chem, 2020, 295(1): 69-82.
26. Tadokoro T, Ikeda M, Ide T, et al. Mitochondria-dependent ferroptosis plays a pivotal role in doxorubicin cardiotoxicity. JCI Insight, 2020, 5(9): e132747.
27. Fang X, Wang H, Han D, et al. Ferroptosis as a target for protection against cardiomyopathy. Proc Natl Acad Sci U S A, 2019, 116(7): 2672-2680.
28. Fang X, Cai Z, Wang H, et al. Loss of cardiac ferritin H facilitates cardiomyopathy via Slc7a11-mediated ferroptosis. Circ Res, 2020, 127(4): 486-501.
29. Wang J, Deng B, Liu Q, et al. Pyroptosis and ferroptosis induced by mixed lineage kinase 3 (MLK3) signaling in cardiomyocytes are essential for myocardial fibrosis in response to pressure overload. Cell Death Dis, 2020, 11(7): 574.
30. Yin Z, Ding G, Chen X, et al. Beclin1 haploinsufficiency rescues low ambient temperature-induced cardiac remodeling and contractile dysfunction through inhibition of ferroptosis and mitochondrial injury. Metabolism, 2020, 113: 154397.
31. Bai T, Li M, Liu Y, et al. Inhibition of ferroptosis alleviates atherosclerosis through attenuating lipid peroxidation and endothelial dysfunction in mouse aortic endothelial cell. Free Radic Biol Med, 2020, 160: 92-102.
32. Sawada H, Hao H, Naito Y, et al. Aortic iron overload with oxidative stress and inflammation in human and murine abdominal aortic aneurysm. Arterioscler Thromb Vasc Biol, 2015, 35(6): 1507-1514.
33. Sampilvanjil A, Karasawa T, Yamada N, et al. Cigarette smoke extract induces ferroptosis in vascular smooth muscle cells. Am J Physiol Heart Circ Physiol, 2020, 318(3): H508-H518.

Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Research progress of ferroptosis in cardiovascular diseases

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