- 1. Department of Clinical Epidemiology and Evidence-based Medicine, The First Affiliated Hospital of China Medical University, Shenyang, 110032, P.R.China;
- 2. Department of Cardiology, The Fourth Affiliated Hospital of China Medical University, Shenyang, 110032, P.R.China;
SHI Jingpu,
Email: sjp562013@126.com
Hypoxia inducible factor-1 (HIF-1) is the main transcription factor and the core regulator for cells to adapt to hypoxia, and oxygen homeostasis is achieved by controlling and utilizing oxygen delivery. Autophagy and apoptosis play an important role in determining cell fate and maintaining cell homeostasis. In recent years, it has been found that the dynamic change of HIF-1 expression plays a key role in the hypoxic adaptive response of cardiomyocytes. The regulation of HIF-1 on autophagy and apoptosis of hypoxic cardiomyocytes determines the survival of cardiomyocytes, which is of great significance for the prognosis of ischemic heart disease.
Citation： ZHANG Xiaohong, SHI Jingpu. Progress of hypoxia inducible factor-1 regulating autophagy and apoptosis in cardiomyocytes under hypoxia. Chinese Journal of Clinical Thoracic and Cardiovascular Surgery, 2020, 27(9): 1087-1093. doi: 10.7507/1007-4848.201912062 Copy
| 1. | Semenza GL. Perspectives on oxygen sensing. Cell, 1999, 98(3): 281-284. |
| 2. | Chanmee T, Ontong P, Izumikawa T, <italic>et al</italic>. Hyaluronan production regulates metabolic and cancer stem-like properties of breast cancer cells via hexosamine biosynthetic pathway-coupled HIF-1 signaling. J Biol Chem, 2016, 291(46): 24105-24120. |
| 3. | Zhang W, Zhou X, Yao Q, <italic>et al</italic>. HIF-1-mediated production of exosomes during hypoxia is protective in renal tubular cells. Am J Physiol Renal Physiol, 2017, 313(4): F906-F913. |
| 4. | Wang QL, Huang WX, Zhang PJ, <italic>et al</italic>. Colorimetric determination of the early biomarker hypoxia-inducible factor-1 alpha (HIF-1α) in circulating exosomes by using a gold seed-coated with aptamer-functionalized Au@Au core-shell peroxidase mimic. Mikrochim Acta, 2019, 187(1): 61. |
| 5. | Su M, Mei Y, Sinha S. Role of the crosstalk between autophagy and apoptosis in cancer. J Oncol, 2013, 2013: 102735. |
| 6. | Byun S, Lee E, Lee KW. Therapeutic implications of autophagy inducers in immunological disorders, infection, and cancer. Int J Mol Sci, 2017, 18(9): E1959. |
| 7. | Thompson CB. Apoptosis in the pathogenesis and treatment of disease. Science, 1995, 267(5203): 1456-1462. |
| 8. | Kang PM, lzumo S. Apoptosis in heart: basic mechanisms and implications in cardiovascular diseases. Trends Mol Med, 2003, 9(4): 177-182. |
| 9. | Bhutia SK, Kegelman TP, Das SK, <italic>et al</italic>. Astrocyte elevated gene-1 induces protective autophagy. Proc Natl Acad Sci USA, 2010, 107: 22243-22248. |
| 10. | Huang Y, Hickey RP, Yeh JL, <italic>et al</italic>. Cardiac myocyte-specific HIF-1 alpha deletion alters vascularization, energy availability, calcium flux, and contractility in the normoxic heart. FASEB J, 2004, 18(10): 1138-1140. |
| 11. | Majmundar AJ, Wong WJ, Simon MC. Hypoxia-inducible factors and the response to hypoxic stress. Mol Cell, 2010, 40(2): 294-309. |
| 12. | Greijer AE, van der Groep P, Kemming D, <italic>et al</italic>. Up-regulation of gene expression by hypoxia is mediated predominantly by hypoxia-inducible factor 1 (HIF-1). J Pathol, 2005, 206(3): 291-304. |
| 13. | Lee SH, Wolf PL, Escudero R, <italic>et al</italic>. Early expression of angiogenesis factors in acute myocardial ischemia and infarction. N Engl J Med, 2000, 342(9): 626-633. |
| 14. | Iyer NV, Kotch LE, Agani F, <italic>et al</italic>. Cellular and developmental control of O<sub>2</sub> homeostasis by hypoxia-inducible factor 1 alpha. Genes Dev, 1998, 12(2): 149-162. |
| 15. | Kim JW, Tchernyshyov I, Semenza GL, <italic>et al</italic>. HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab, 2006, 3(3): 177-185. |
| 16. | Semenza GL. Regulation of oxygen homeostasis by hypoxia-inducible factor 1. Physiology (Bethesda), 2009, 24: 97-106. |
| 17. | Fisher JW. Erythropoietin: physiology and pharmacology update. Exp Biol Med (Maywood), 2003, 228(1): 1-14. |
| 18. | Bogoyevitch MA. An update on the cardiac effects of erythropoietin cardioprotection by erythropoietin and the lessons learnt from studies in neuroprotection. Cardiovasc Res, 2004, 63(2): 208-216. |
| 19. | Shyu KG, Wang MT, Wang BW, <italic>et al</italic>. Intramyocardial injection of naked DNA encoding HIF-1alpha/VP16 hybrid to enhance angiogenesis in an acute myocardial infarction model in the rat. Cardiovasc Res, 2002, 54(3): 576-583. |
| 20. | Kido M, Du L, Sullivan CC, <italic>et al</italic>. Hypoxia-inducible factor 1-alpha reduces infarction and attenuates progression of cardiac dysfunction after myocardial infarction in the mouse. J Am Coll Cardiol, 2005, 46(11): 2116-2124. |
| 21. | Yet SF, Tian R, Layne MD, <italic>et al</italic>. Cardiac-specific expression of heme oxygenase-1 protects against ischemia and reperfusion injury in transgenic mice. Circ Res, 2001, 89(2): 166-173. |
| 22. | Robador PA, San José G, Rodríguez C, <italic>et al</italic>. HIF-1-mediated up-regulation of cardiotrophin-1 is involved in the survival response of cardiomyocytes to hypoxia. Cardiovasc Res, 2011, 92(2): 247-255. |
| 23. | Blanco Pampín J, García Rivero SA, Otero Cepeda XL, <italic>et al</italic>. Immunohistochemical expression of HIF-1alpha in response to early myocardial ischemia. J Forensic Sci, 2006, 51(1): 120-124. |
| 24. | Date T, Mochizuki S, Belanger AJ, <italic>et al</italic>. Expression of constitutively stable hybrid hypoxia-inducible factor-1alpha protects cultured rat cardiomyocytes against simulated ischemia-reperfusion injury. Am J Physiol Cell Physiol, 2005, 288(2): C314-C320. |
| 25. | Murry CE, Jennings RB, Reimer KA. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation, 1986, 74(5): 1124-1136. |
| 26. | Zhao HX, Wang XL, Wang YH, <italic>et al</italic>. Attenuation of myocardial injury by postconditioning: role of hypoxia inducible factor-1alpha. Basic Res Cardiol, 2010, 105(1): 109-118. |
| 27. | Czibik G, Gravning J, Martinov V, <italic>et al</italic>. Gene therapy with hypoxia-inducible factor 1 alpha in skeletal muscle is cardioprotective in vivo. Life Sci, 2011, 88(11-12): 543-550. |
| 28. | Lei L, Mason S, Liu D, <italic>et al</italic>. Hypoxia-inducible factor-dependent degeneration, failure, and malignant transformation of the heart in the absence of the von Hippel-Lindau protein. Mol Cell Biol, 2008, 28(11): 3790-3803. |
| 29. | Bekeredjian R, Walton CB, MacCannell KA, <italic>et al</italic>. Conditional HIF-1alpha expression produces a reversible cardiomyopathy. PLoS One, 2010, 5(7): e11693. |
| 30. | Shyu KG, Liou JY, Wang BW, <italic>et al</italic>. Carvedilol prevents cardiac hypertrophy and overexpression of hypoxia-inducible factor-1alpha and vascular endothelial growth factor in pressure-overloaded rat heart. J Biomed Sci, 2005, 12(2): 409-420. |
| 31. | Bohuslavová R, Kolář F, Kuthanová L, <italic>et al</italic>. Gene expression profiling of sex differences in HIF1-dependent adaptive cardiac responses to chronic hypoxia. J Appl Physiol (1985), 2010, 109(4): 195-202. |
| 32. | Kaluz S, Kaluzová M, Stanbridge EJ. Regulation of gene expression by hypoxia: integration of the HIF-transduced hypoxic signal at the hypoxia responsive element. Clin Chim Acta, 2008, 395: 6-13. |
| 33. | De Meyer GR, Grootaert MO, Michiels CF, <italic>et al</italic>. Autophagy in vascular disease. Circ Res, 2015, 116(3): 468-479. |
| 34. | Mines MA, Beurel E, Jope RS. Regulation of cell survival mechanisms in Alzheimer’s disease by glycogen synthase kinase-3. Int J Alzheimers Dis, 2011, 2011: 861072. |
| 35. | Mizushima N. Autophagy: Process and function. Genes Dev, 2007, 21(22): 2861-2873. |
| 36. | Gatica D, Chiong M, Lavandero S, <italic>et al</italic>. Molecular mechanisms of autophagy in the cardiovascular system. Circ Res, 2015, 116(3): 456-67. |
| 37. | 杨贵芳, 柴湘平, 彭文, 等. PKD1 基因对主动脉平滑肌细胞自噬的影响. 中国胸心血管外科临床杂志, 2106, 23(7): 724-727. |
| 38. | Matsui Y1, Takagi H, Qu X, <italic>et al</italic>. Distinct roles of autophagy in the heart during ischemia and reperfusion: roles of AMP-activated protein kinase and Beclin 1 in mediating autophagy. Circ Res, 2007, 100(6): 914-922. |
| 39. | Loos B, Genade S, Ellis B, <italic>et al</italic>. At the core of survival: Autophagy delays the onset of both apoptotic and necrotic cell death in a model of ischemic cell injury. Exp Cell Res, 2011, 317(10): 1437-1453. |
| 40. | Mellor KM, Bell JR, Young MJ, <italic>et al</italic>. Myocardial autophagy activation and suppressed survival signaling is associated with insulin resistance in fructose-fed mice. J Mol Cell Cardiol, 2011, 50(6): 1035-1043. |
| 41. | Lavandero S, Troncoso R, Rothermel BA, <italic>et al</italic>. Cardiovascular autophagy: concepts, controversies, and perspectives. Autophagy, 2013, 9(10): 1455-1466. |
| 42. | Mazure NM, Pouysségur J. Hypoxia-induced autophagy: cell death or cell survival? Curr Opin Cell Biol, 2010, 22(2): 177-180. |
| 43. | Dong Y, Chen H, Gao J, <italic>et al</italic>. Molecular machinery and interplay of apoptosis and autophagy in coronary heart disease. J Mol Cell Cardiol, 2019, 136: 27-41. |
| 44. | Bellot G, Garcia-Medina R, Gounon P, <italic>et al</italic>. Hypoxia-induced autophagy is mediated through hypoxia-inducible factor induction of BNIP3 and BNIP3L via their BH3 domains. Mol Cell Biol, 2009, 29(10): 2570-2581. |
| 45. | Yang Y, Li Y, Chen X, <italic>et al</italic>. Exosomal transfer of miR-30a between cardiomyocytes regulates autophagy after hypoxia. J Mol Med, 2016, 94(6): 711-724. |
| 46. | Gui L, Liu B, Lv G. Hypoxia induces autophagy in cardiomyocytes via a hypoxia-inducible factor 1-dependent mechanism. Exp Ther Med, 2016, 11(6): 2233-2239. |
| 47. | Lu N, Li X, Tan R, <italic>et al</italic>. HIF-1α/beclin1-mediated autophagy is involved in neuroprotection induced by hypoxic preconditioning. J Mol Neurosci, 2018, 66(2): 238-250. |
| 48. | Brill A, Torchinsky A, Carp H, <italic>et al</italic>. The role of apoptosis in normal and abnormal embryonic development. J Assist Reprod Genet, 1999, 16(10): 512-519. |
| 49. | Cotter TG. Apoptosis and cancer: the genesis of a research field. Nat Rev Cancer, 2009, 9(7): 501-507. |
| 50. | Saraste A, Pulkki K, Kallajoki M, <italic>et al</italic>. Apoptosis in human acute myocardial infarction. Circulation, 1997, 95(2): 320-323. |
| 51. | Abbate A, Melfi R, Patti G, <italic>et al</italic>. Apoptosis in recent myocardial infarction. Clin Ter, 2000, 151(4): 247-251. |
| 52. | Baldi A, Abbate A, Bussani R, <italic>et al</italic>. Apoptosis and post-infarction left ventricular remodeling. J Mol Cell Cardiol, 2002, 34(2): 165-174. |
| 53. | Abbate A, Salloum FN, Vecile E, <italic>et al</italic>. Anakinra, a recombinant human interleukin-1 receptor antagonist, inhibits apoptosis in experimental acute myocardial infarction. Circulation, 2008, 117(20): 2670-2683. |
| 54. | Griffiths EJ, Halestrap AP. Mitochondrial non-specific pores remain closed during cardiac ischaemia, but open upon reperfusion. Biochem J, 1995, 307(1): 93-98. |
| 55. | Hausenloy DJ, Yellon DM. The mitochondrial permeability transition pore: its fundamental role in mediating cell death during ischaemia and reperfusion. J Mol Cell Cardiol, 2003, 35(4): 339-341. |
| 56. | Gurel E, Smeele KM, Eerbeek O, <italic>et al</italic>. Ischemic preconditioning affects hexokinase activity and HKⅡ in different subcellular compartments throughout cardiac ischemia-reperfusion. J Appl Physiol, 2009, 106(6): 1909-1916. |
| 57. | Ong SG, Lee WH, Theodorou L, <italic>et al</italic>. HIF-1 reduces ischaemia-reperfusion injury in the heart by targeting the mitochondrial permeability transition pore. Cardiovasc Res, 2014, 104(1): 24-36. |
| 58. | Li DF, Tian J, Guo X, <italic>et al</italic>. Induction of microRNA-24 by HIF-1 protects against ischemic injury in rat cardiomyocytes. Physiol Res, 2012, 61(6): 555-565. |
| 59. | Yang B, He K, Zheng F, <italic>et al</italic>. Over-expression of hypoxia-inducible factor-1 alpha in vitro protects the cardiac fibroblasts from hypoxia-induced apoptosis. J Cardio Vas Med (Hagerstown), 2014, 15(7): 579-586. |
| 60. | Holscher M, Schafer K, Krull S, <italic>et al</italic>. Unfavourable consequences of chronic cardiac HIF-1alpha stabilization. Cardiovasc Res, 2012, 94(1): 77-86. |
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- 1. Semenza GL. Perspectives on oxygen sensing. Cell, 1999, 98(3): 281-284.
- 2. Chanmee T, Ontong P, Izumikawa T, <italic>et al</italic>. Hyaluronan production regulates metabolic and cancer stem-like properties of breast cancer cells via hexosamine biosynthetic pathway-coupled HIF-1 signaling. J Biol Chem, 2016, 291(46): 24105-24120.
- 3. Zhang W, Zhou X, Yao Q, <italic>et al</italic>. HIF-1-mediated production of exosomes during hypoxia is protective in renal tubular cells. Am J Physiol Renal Physiol, 2017, 313(4): F906-F913.
- 4. Wang QL, Huang WX, Zhang PJ, <italic>et al</italic>. Colorimetric determination of the early biomarker hypoxia-inducible factor-1 alpha (HIF-1α) in circulating exosomes by using a gold seed-coated with aptamer-functionalized Au@Au core-shell peroxidase mimic. Mikrochim Acta, 2019, 187(1): 61.
- 5. Su M, Mei Y, Sinha S. Role of the crosstalk between autophagy and apoptosis in cancer. J Oncol, 2013, 2013: 102735.
- 6. Byun S, Lee E, Lee KW. Therapeutic implications of autophagy inducers in immunological disorders, infection, and cancer. Int J Mol Sci, 2017, 18(9): E1959.
- 7. Thompson CB. Apoptosis in the pathogenesis and treatment of disease. Science, 1995, 267(5203): 1456-1462.
- 8. Kang PM, lzumo S. Apoptosis in heart: basic mechanisms and implications in cardiovascular diseases. Trends Mol Med, 2003, 9(4): 177-182.
- 9. Bhutia SK, Kegelman TP, Das SK, <italic>et al</italic>. Astrocyte elevated gene-1 induces protective autophagy. Proc Natl Acad Sci USA, 2010, 107: 22243-22248.
- 10. Huang Y, Hickey RP, Yeh JL, <italic>et al</italic>. Cardiac myocyte-specific HIF-1 alpha deletion alters vascularization, energy availability, calcium flux, and contractility in the normoxic heart. FASEB J, 2004, 18(10): 1138-1140.
- 11. Majmundar AJ, Wong WJ, Simon MC. Hypoxia-inducible factors and the response to hypoxic stress. Mol Cell, 2010, 40(2): 294-309.
- 12. Greijer AE, van der Groep P, Kemming D, <italic>et al</italic>. Up-regulation of gene expression by hypoxia is mediated predominantly by hypoxia-inducible factor 1 (HIF-1). J Pathol, 2005, 206(3): 291-304.
- 13. Lee SH, Wolf PL, Escudero R, <italic>et al</italic>. Early expression of angiogenesis factors in acute myocardial ischemia and infarction. N Engl J Med, 2000, 342(9): 626-633.
- 14. Iyer NV, Kotch LE, Agani F, <italic>et al</italic>. Cellular and developmental control of O<sub>2</sub> homeostasis by hypoxia-inducible factor 1 alpha. Genes Dev, 1998, 12(2): 149-162.
- 15. Kim JW, Tchernyshyov I, Semenza GL, <italic>et al</italic>. HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab, 2006, 3(3): 177-185.
- 16. Semenza GL. Regulation of oxygen homeostasis by hypoxia-inducible factor 1. Physiology (Bethesda), 2009, 24: 97-106.
- 17. Fisher JW. Erythropoietin: physiology and pharmacology update. Exp Biol Med (Maywood), 2003, 228(1): 1-14.
- 18. Bogoyevitch MA. An update on the cardiac effects of erythropoietin cardioprotection by erythropoietin and the lessons learnt from studies in neuroprotection. Cardiovasc Res, 2004, 63(2): 208-216.
- 19. Shyu KG, Wang MT, Wang BW, <italic>et al</italic>. Intramyocardial injection of naked DNA encoding HIF-1alpha/VP16 hybrid to enhance angiogenesis in an acute myocardial infarction model in the rat. Cardiovasc Res, 2002, 54(3): 576-583.
- 20. Kido M, Du L, Sullivan CC, <italic>et al</italic>. Hypoxia-inducible factor 1-alpha reduces infarction and attenuates progression of cardiac dysfunction after myocardial infarction in the mouse. J Am Coll Cardiol, 2005, 46(11): 2116-2124.
- 21. Yet SF, Tian R, Layne MD, <italic>et al</italic>. Cardiac-specific expression of heme oxygenase-1 protects against ischemia and reperfusion injury in transgenic mice. Circ Res, 2001, 89(2): 166-173.
- 22. Robador PA, San José G, Rodríguez C, <italic>et al</italic>. HIF-1-mediated up-regulation of cardiotrophin-1 is involved in the survival response of cardiomyocytes to hypoxia. Cardiovasc Res, 2011, 92(2): 247-255.
- 23. Blanco Pampín J, García Rivero SA, Otero Cepeda XL, <italic>et al</italic>. Immunohistochemical expression of HIF-1alpha in response to early myocardial ischemia. J Forensic Sci, 2006, 51(1): 120-124.
- 24. Date T, Mochizuki S, Belanger AJ, <italic>et al</italic>. Expression of constitutively stable hybrid hypoxia-inducible factor-1alpha protects cultured rat cardiomyocytes against simulated ischemia-reperfusion injury. Am J Physiol Cell Physiol, 2005, 288(2): C314-C320.
- 25. Murry CE, Jennings RB, Reimer KA. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation, 1986, 74(5): 1124-1136.
- 26. Zhao HX, Wang XL, Wang YH, <italic>et al</italic>. Attenuation of myocardial injury by postconditioning: role of hypoxia inducible factor-1alpha. Basic Res Cardiol, 2010, 105(1): 109-118.
- 27. Czibik G, Gravning J, Martinov V, <italic>et al</italic>. Gene therapy with hypoxia-inducible factor 1 alpha in skeletal muscle is cardioprotective in vivo. Life Sci, 2011, 88(11-12): 543-550.
- 28. Lei L, Mason S, Liu D, <italic>et al</italic>. Hypoxia-inducible factor-dependent degeneration, failure, and malignant transformation of the heart in the absence of the von Hippel-Lindau protein. Mol Cell Biol, 2008, 28(11): 3790-3803.
- 29. Bekeredjian R, Walton CB, MacCannell KA, <italic>et al</italic>. Conditional HIF-1alpha expression produces a reversible cardiomyopathy. PLoS One, 2010, 5(7): e11693.
- 30. Shyu KG, Liou JY, Wang BW, <italic>et al</italic>. Carvedilol prevents cardiac hypertrophy and overexpression of hypoxia-inducible factor-1alpha and vascular endothelial growth factor in pressure-overloaded rat heart. J Biomed Sci, 2005, 12(2): 409-420.
- 31. Bohuslavová R, Kolář F, Kuthanová L, <italic>et al</italic>. Gene expression profiling of sex differences in HIF1-dependent adaptive cardiac responses to chronic hypoxia. J Appl Physiol (1985), 2010, 109(4): 195-202.
- 32. Kaluz S, Kaluzová M, Stanbridge EJ. Regulation of gene expression by hypoxia: integration of the HIF-transduced hypoxic signal at the hypoxia responsive element. Clin Chim Acta, 2008, 395: 6-13.
- 33. De Meyer GR, Grootaert MO, Michiels CF, <italic>et al</italic>. Autophagy in vascular disease. Circ Res, 2015, 116(3): 468-479.
- 34. Mines MA, Beurel E, Jope RS. Regulation of cell survival mechanisms in Alzheimer’s disease by glycogen synthase kinase-3. Int J Alzheimers Dis, 2011, 2011: 861072.
- 35. Mizushima N. Autophagy: Process and function. Genes Dev, 2007, 21(22): 2861-2873.
- 36. Gatica D, Chiong M, Lavandero S, <italic>et al</italic>. Molecular mechanisms of autophagy in the cardiovascular system. Circ Res, 2015, 116(3): 456-67.
- 37. 杨贵芳, 柴湘平, 彭文, 等. PKD1 基因对主动脉平滑肌细胞自噬的影响. 中国胸心血管外科临床杂志, 2106, 23(7): 724-727.
- 38. Matsui Y1, Takagi H, Qu X, <italic>et al</italic>. Distinct roles of autophagy in the heart during ischemia and reperfusion: roles of AMP-activated protein kinase and Beclin 1 in mediating autophagy. Circ Res, 2007, 100(6): 914-922.
- 39. Loos B, Genade S, Ellis B, <italic>et al</italic>. At the core of survival: Autophagy delays the onset of both apoptotic and necrotic cell death in a model of ischemic cell injury. Exp Cell Res, 2011, 317(10): 1437-1453.
- 40. Mellor KM, Bell JR, Young MJ, <italic>et al</italic>. Myocardial autophagy activation and suppressed survival signaling is associated with insulin resistance in fructose-fed mice. J Mol Cell Cardiol, 2011, 50(6): 1035-1043.
- 41. Lavandero S, Troncoso R, Rothermel BA, <italic>et al</italic>. Cardiovascular autophagy: concepts, controversies, and perspectives. Autophagy, 2013, 9(10): 1455-1466.
- 42. Mazure NM, Pouysségur J. Hypoxia-induced autophagy: cell death or cell survival? Curr Opin Cell Biol, 2010, 22(2): 177-180.
- 43. Dong Y, Chen H, Gao J, <italic>et al</italic>. Molecular machinery and interplay of apoptosis and autophagy in coronary heart disease. J Mol Cell Cardiol, 2019, 136: 27-41.
- 44. Bellot G, Garcia-Medina R, Gounon P, <italic>et al</italic>. Hypoxia-induced autophagy is mediated through hypoxia-inducible factor induction of BNIP3 and BNIP3L via their BH3 domains. Mol Cell Biol, 2009, 29(10): 2570-2581.
- 45. Yang Y, Li Y, Chen X, <italic>et al</italic>. Exosomal transfer of miR-30a between cardiomyocytes regulates autophagy after hypoxia. J Mol Med, 2016, 94(6): 711-724.
- 46. Gui L, Liu B, Lv G. Hypoxia induces autophagy in cardiomyocytes via a hypoxia-inducible factor 1-dependent mechanism. Exp Ther Med, 2016, 11(6): 2233-2239.
- 47. Lu N, Li X, Tan R, <italic>et al</italic>. HIF-1α/beclin1-mediated autophagy is involved in neuroprotection induced by hypoxic preconditioning. J Mol Neurosci, 2018, 66(2): 238-250.
- 48. Brill A, Torchinsky A, Carp H, <italic>et al</italic>. The role of apoptosis in normal and abnormal embryonic development. J Assist Reprod Genet, 1999, 16(10): 512-519.
- 49. Cotter TG. Apoptosis and cancer: the genesis of a research field. Nat Rev Cancer, 2009, 9(7): 501-507.
- 50. Saraste A, Pulkki K, Kallajoki M, <italic>et al</italic>. Apoptosis in human acute myocardial infarction. Circulation, 1997, 95(2): 320-323.
- 51. Abbate A, Melfi R, Patti G, <italic>et al</italic>. Apoptosis in recent myocardial infarction. Clin Ter, 2000, 151(4): 247-251.
- 52. Baldi A, Abbate A, Bussani R, <italic>et al</italic>. Apoptosis and post-infarction left ventricular remodeling. J Mol Cell Cardiol, 2002, 34(2): 165-174.
- 53. Abbate A, Salloum FN, Vecile E, <italic>et al</italic>. Anakinra, a recombinant human interleukin-1 receptor antagonist, inhibits apoptosis in experimental acute myocardial infarction. Circulation, 2008, 117(20): 2670-2683.
- 54. Griffiths EJ, Halestrap AP. Mitochondrial non-specific pores remain closed during cardiac ischaemia, but open upon reperfusion. Biochem J, 1995, 307(1): 93-98.
- 55. Hausenloy DJ, Yellon DM. The mitochondrial permeability transition pore: its fundamental role in mediating cell death during ischaemia and reperfusion. J Mol Cell Cardiol, 2003, 35(4): 339-341.
- 56. Gurel E, Smeele KM, Eerbeek O, <italic>et al</italic>. Ischemic preconditioning affects hexokinase activity and HKⅡ in different subcellular compartments throughout cardiac ischemia-reperfusion. J Appl Physiol, 2009, 106(6): 1909-1916.
- 57. Ong SG, Lee WH, Theodorou L, <italic>et al</italic>. HIF-1 reduces ischaemia-reperfusion injury in the heart by targeting the mitochondrial permeability transition pore. Cardiovasc Res, 2014, 104(1): 24-36.
- 58. Li DF, Tian J, Guo X, <italic>et al</italic>. Induction of microRNA-24 by HIF-1 protects against ischemic injury in rat cardiomyocytes. Physiol Res, 2012, 61(6): 555-565.
- 59. Yang B, He K, Zheng F, <italic>et al</italic>. Over-expression of hypoxia-inducible factor-1 alpha in vitro protects the cardiac fibroblasts from hypoxia-induced apoptosis. J Cardio Vas Med (Hagerstown), 2014, 15(7): 579-586.
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