Skip to main content

Advertisement

Log in

Long Noncoding RNAs Involved in Cardiomyocyte Apoptosis Triggered by Different Stressors

  • Review
  • Published:
Journal of Cardiovascular Translational Research Aims and scope Submit manuscript

Abstract

Cardiomyocytes are essential to maintain the normal cardiac function. Ischemia, hypoxia, and drug stimulation can induce pathological apoptosis of cardiomyocytes which eventually leads to heart failure, arrhythmia, and other cardiovascular diseases. Understanding the molecular mechanisms that regulate cardiomyocyte apoptosis is of great significance for the prevention and treatment of cardiovascular diseases. In recent years, more and more evidences reveal that long noncoding RNAs (lncRNAs) play important regulatory roles in myocardial cell apoptosis. They can modulate the expression of apoptosis-related genes at post-transcriptional level by altering the translation efficacy of target mRNAs or functioning as a precursor for miRNAs or competing for miRNA-mediated inhibition. Moreover, reversing the abnormal expression of lncRNAs can attenuate and even reverse the pathological apoptosis of cardiomyocytes. Therefore, apoptosis-related lncRNAs may become a potential new field for studying cardiomyocyte apoptosis and provide new ideas for the treatment of cardiovascular diseases.

Graphical abstract

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Portt, L., Norman, G., Clapp, C., et al. (2011). Anti-apoptosis and cell survival: A review. Biochimica et Biophysica Acta, 1813, 238–259.

    Article  CAS  PubMed  Google Scholar 

  2. Elmore, S. (2007). Apoptosis: A review of programmed cell death. Toxicologic Pathology, 35, 495–516.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Olivetti, G., Abbi, R., Quaini, F., et al. (1997). Apoptosis in the failing human heart. New England Journal of Medicine, 336, 1131–1141.

    Article  CAS  PubMed  Google Scholar 

  4. Fujita, T., & Ishikawa, Y. (2011). Apoptosis in heart failure -The role of the beta-adrenergic receptor-mediated signaling pathway and p53-mediated signaling pathway in the apoptosis of cardiomyocytes. CIRC Journal, 75, 1811–8.

    Article  CAS  Google Scholar 

  5. Mignone, J. L., Kreutziger, K. L., Paige, S. L., et al. (2010). Cardiogenesis from human embryonic stem cells. Circulation Journal, 74, 2517–2526.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Hosoda, T., Kajstura, J., Leri, A., et al. (2010). Mechanisms of myocardial regeneration. CIRC Journal, 74, 13–17.

    Article  CAS  Google Scholar 

  7. Djebali, S., Davis, C. A., Merkel, A., et al. (2012). Landscape of transcription in human cells. Nature, 489, 101–108.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Carninci, P., Kasukawa, T., Katayama, S., et al. (2005). The transcriptional landscape of the mammalian genome. Science, 309, 1559–1563.

    Article  CAS  PubMed  Google Scholar 

  9. Kumar, M. M., & Goyal, R. (2017). LncRNA as a therapeutic target for angiogenesis. Current Topics in Medicinal Chemistry, 17, 1750–1757.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Guttman, M., Amit, I., Garber, M., et al. (2009). Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature, 458, 223–227.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Kung, J. T., Colognori, D., & Lee, J. T. (2013). Long noncoding RNAs: Past, present, and future. Genetics, 193, 651–669.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Li, L., & Chang, H. Y. (2014). Physiological roles of long noncoding RNAs: Insight from knockout mice. Trends in Cell Biology, 24, 594–602.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Grote, P., Wittler, L., Hendrix, D., et al. (2013). The tissue-specific lncRNA Fendrr is an essential regulator of heart and body wall development in the mouse. Developmental Cell, 24, 206–214.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Tsoi, L. C., Iyer, M. K., Stuart, P. E., et al. (2015). Analysis of long non-coding RNAs highlights tissue-specific expression patterns and epigenetic profiles in normal and psoriatic skin. Genome Biology, 16, 24.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Gibb, E. A., Vucic, E. A., Enfield, K. S., et al. (2011). Human cancer long non-coding RNA transcriptomes. PLOS ONE, 6, e25915.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Derrien, T., Johnson, R., Bussotti, G., et al. (2012). The GENCODE v7 catalog of human long noncoding RNAs: Analysis of their gene structure, evolution, and expression. Genome Research, 22, 1775–1789.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Rinn, J. L., & Chang, H. Y. (2012). Genome regulation by long noncoding RNAs. Annual Review of Biochemistry, 81, 145–166.

    Article  CAS  PubMed  Google Scholar 

  18. Wang, K. C., & Chang, H. Y. (2011). Molecular mechanisms of long noncoding RNAs. Molecular Cell, 43, 904–914.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Jathar, S., Kumar, V., Srivastava, J., et al. (2017). Technological developments in lncRNA biology. Advances in Experimental Medicine and Biology, 1008, 283–323.

    Article  CAS  PubMed  Google Scholar 

  20. Elahi, M. M., Kong, Y. X., & Matata, B. M. (2009). Oxidative stress as a mediator of cardiovascular disease. Oxidative Medicine and Cellular Longevity, 2, 259–269.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Becker, L. B. (2004). New concepts in reactive oxygen species and cardiovascular reperfusion physiology. Cardiovascular Research, 61, 461–470.

    Article  CAS  PubMed  Google Scholar 

  22. Zou, L., Ma, X., Lin, S., et al. (2019). Long noncoding RNA-MEG3 contributes to myocardial ischemia-reperfusion injury through suppression of miR-7–5p expression. Bioscience Reports, 39.

  23. Li, B., Li, R., Zhang, C., et al. (2014). MicroRNA-7a/b protects against cardiac myocyte injury in ischemia/reperfusion by targeting poly (ADP-ribose) polymerase. PLOS ONE, 9, e90096.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Li, X., Luo, S., Zhang, J., et al. (2019). lncRNA H19 alleviated myocardial I/RI via suppressing miR-877-3p/Bcl-2-mediated mitochondrial apoptosis. Molecular Therapy--Nucleic Acids, 17, 297–309.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Wu, H. J., Tang, G. M., Shao, P. Y., et al. (2019). Long non-coding RNA NEAT1 modulates hypoxia/reoxygenation-induced cardiomyocyte injury via targeting microRNA-520a. Experimental and Therapeutic Medicine, 18, 2199–2206.

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Yan, H., Liang, H., Liu, L., et al. (2019). Long noncoding RNA NEAT1 sponges miR125a5p to suppress cardiomyocyte apoptosis via BCL2L12. Molecular Medicine Reports, 19, 4468–4474.

    CAS  PubMed  Google Scholar 

  27. Zhao, Z. H., Hao, W., Meng, Q. T., et al. (2017). Long non-coding RNA MALAT1 functions as a mediator in cardioprotective effects of fentanyl in myocardial ischemia-reperfusion injury. Cell Biology International, 41, 62–70.

    Article  CAS  PubMed  Google Scholar 

  28. Lu, H., He, Y., Lin, L., et al. (2016). Long non-coding RNA MALAT1 modulates radiosensitivity of HR-HPV+ cervical cancer via sponging miR-145. Tumour Biology, 37, 1683–1691.

    Article  CAS  PubMed  Google Scholar 

  29. Diwan, A., Krenz, M., Syed, F. M., et al. (2007). Inhibition of ischemic cardiomyocyte apoptosis through targeted ablation of Bnip3 restrains postinfarction remodeling in mice. The Journal of Clinical Investigation, 117, 2825–2833.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Li, R., Yan, G., Li, Q., et al. (2012). MicroRNA-145 protects cardiomyocytes against hydrogen peroxide (H(2)O(2))-induced apoptosis through targeting the mitochondria apoptotic pathway. PLOS ONE, 7, e44907.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Kubli, D. A., Quinsay, M. N., Huang, C., et al. (2008). Bnip3 functions as a mitochondrial sensor of oxidative stress during myocardial ischemia and reperfusion. American Journal of Physiology. Heart and Circulatory Physiology, 295, H2025–H2031.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Hamacher-Brady, A., Brady, N. R., Logue, S. E., et al. (2007). Response to myocardial ischemia/reperfusion injury involves Bnip3 and autophagy. Cell Death and Differentiation, 14, 146–157.

    Article  CAS  PubMed  Google Scholar 

  33. Gross, E. R., Hsu, A. K., & Gross, G. J. (2006). The JAK/STAT pathway is essential for opioid-induced cardioprotection: JAK2 as a mediator of STAT3, Akt, and GSK-3 beta. American Journal of Physiology. Heart and Circulatory Physiology, 291, H827–H834.

    Article  CAS  PubMed  Google Scholar 

  34. Sun, T., Cheng, Y. T., Yan, L. X., et al. (2019). LncRNA MALAT1 knockdown alleviates myocardial apoptosis in rats with myocardial ischemia-reperfusion through activating PI3K/AKT signaling pathway. European Review for Medical and Pharmacological Sciences, 23, 10523–10531.

    CAS  PubMed  Google Scholar 

  35. Morkedal, B., Vatten, L. J., Romundstad, P. R., et al. (2014). Risk of myocardial infarction and heart failure among metabolically healthy but obese individuals: HUNT (Nord-Trondelag Health Study), Norway. Journal of the American College of Cardiology, 63, 1071–1078.

    Article  PubMed  Google Scholar 

  36. Ding, L., Gong, C., Zhao, J., et al. (2019). Noncoding transcribed ultraconserved region (T-UCR) UC.48+ is a novel regulator of high-fat diet induced myocardial ischemia/reperfusion injury. Journal of Cellular Physiology, 234, 9849–61.

    Article  CAS  PubMed  Google Scholar 

  37. Garcia-Huerta, P., Diaz-Hernandez, M., Delicado, E. G., et al. (2012). The specificity protein factor Sp1 mediates transcriptional regulation of P2X7 receptors in the nervous system. Journal of Biological Chemistry, 287, 44628–44644.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Chen, Z., He, L., Li, L., et al. (2018). The P2X7 purinergic receptor: An emerging therapeutic target in cardiovascular diseases. Clinica Chimica Acta, 479, 196–207.

    Article  CAS  Google Scholar 

  39. Wu, H., Zhu, H., Zhuang, Y., et al. (2020). LncRNA ACART protects cardiomyocytes from apoptosis by activating PPAR-gamma/Bcl-2 pathway. Journal of Cellular and Molecular Medicine, 24, 737–746.

    Article  CAS  PubMed  Google Scholar 

  40. Ren, Y., Sun, C., Sun, Y., et al. (2009). PPAR gamma protects cardiomyocytes against oxidative stress and apoptosis via Bcl-2 upregulation. Vascular Pharmacology, 51, 169–174.

    Article  CAS  PubMed  Google Scholar 

  41. Ye, Y., Hu, Z., Lin, Y., et al. (2010). Downregulation of microRNA-29 by antisense inhibitors and a PPAR-gamma agonist protects against myocardial ischaemia-reperfusion injury. Cardiovascular Research, 87, 535–544.

    Article  CAS  PubMed  Google Scholar 

  42. Zhan, L. F., Zhang, Q., Zhao, L., et al. (2021). LncRNA-6395 promotes myocardial ischemia-reperfusion injury in mice through increasing p53 pathway. Acta Pharmacologica Sinica.

  43. Yao, Y., Fan, X., Yu, B., et al. (2019). Knockdown of long noncoding RNA Malat1 aggravates hypoxia-induced cardiomyocyte injury by targeting miR-217. Advances in Clinical and Experimental Medicine, 28, 719–728.

    Article  PubMed  Google Scholar 

  44. Guarani, V., Deflorian, G., Franco, C. A., et al. (2011). Acetylation-dependent regulation of endothelial Notch signalling by the SIRT1 deacetylase. Nature, 473, 234–238.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Li, W., Du, D., Wang, H., et al. (2015). Silent information regulator 1 (SIRT1) promotes the migration and proliferation of endothelial progenitor cells through the PI3K/Akt/eNOS signaling pathway. International Journal of Clinical and Experimental Pathology, 8, 2274–2287.

    PubMed  PubMed Central  Google Scholar 

  46. Gong, L., Chang, H., & Xu, H. (2019). LncRNA MALAT1 knockdown alleviates oxygen-glucose deprivation and reperfusion induced cardiomyocyte apoptotic death by regulating miR-122. Experimental and Molecular Pathology, 111, 104325.

    Article  CAS  PubMed  Google Scholar 

  47. Zhang, Z., Li, H., Chen, S., et al. (2017). Knockdown of MicroRNA-122 protects H9c2 cardiomyocytes from hypoxia-induced apoptosis and promotes autophagy. Medical Science Monitor, 23, 4284–4290.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Dai, P., Mao, Y., Sun, X., et al. (2017). Attenuation of oxidative stress-induced osteoblast apoptosis by curcumin is associated with preservation of mitochondrial functions and increased Akt-GSK3beta signaling. Cellular Physiology and Biochemistry, 41, 661–677.

    Article  CAS  PubMed  Google Scholar 

  49. He, H., Li, X., & He, Y. (2019). Hyperbaric oxygen therapy attenuates neuronal apoptosis induced by traumatic brain injury via Akt/GSK3beta/beta-catenin pathway. Neuropsychiatric Disease and Treatment, 15, 369–374.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Li, X., Zhao, J., Geng, J., et al. (2019). Long non-coding RNA MEG3 knockdown attenuates endoplasmic reticulum stress-mediated apoptosis by targeting p53 following myocardial infarction. Journal of Cellular and Molecular Medicine, 23, 8369–8380.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Zhao, L. Y., Li, X., Gao, L., et al. (2019). LncRNA MEG3 accelerates apoptosis of hypoxic myocardial cells via FoxO1 signaling pathway. European Review for Medical and Pharmacological Sciences, 23, 334–340.

    PubMed  Google Scholar 

  52. Gong, G., Yang, X. X., Li, Y., et al. (2017). LncRNA260-specific siRNA targeting IL28RA gene inhibit cardiomyocytes hypoxic/reoxygenation injury. Journal of Thoracic Disease, 9, 2447–2460.

    Article  PubMed  PubMed Central  Google Scholar 

  53. Li, X., Ni, L., Wang, W., et al. (2020). LncRNA Fendrr inhibits hypoxia/reoxygenation-induced cardiomyocyte apoptosis by downregulating p53 expression. Journal of Pharmacy and Pharmacology, 72, 1211–1220.

    Article  CAS  PubMed  Google Scholar 

  54. Ka, W. H., Cho, S. K., Chun, B. N., et al. (2018). The ubiquitin ligase COP1 regulates cell cycle and apoptosis by affecting p53 function in human breast cancer cell lines. Breast Cancer, 25, 529–538.

    Article  PubMed  Google Scholar 

  55. Chen, M., Guo, Y., Sun, Z., et al. (2021). Long non-coding RNA SENCR alleviates hypoxia/reoxygenation-induced cardiomyocyte apoptosis and inflammatory response by sponging miR-1. Cardiovascular Diagnosis and Therapy, 11, 707–715.

    Article  PubMed  PubMed Central  Google Scholar 

  56. Abbate, A., & Narula, J. (2012). Role of apoptosis in adverse ventricular remodeling. Heart Failure Clinics, 8, 79–86.

    Article  PubMed  Google Scholar 

  57. Jiao, L., Li, M., Shao, Y., et al. (2019). lncRNA-ZFAS1 induces mitochondria-mediated apoptosis by causing cytosolic Ca(2+) overload in myocardial infarction mice model. Cell Death & Disease, 10, 942.

    Article  CAS  Google Scholar 

  58. Wu, T., Wu, D., Wu, Q., et al. (2017). Knockdown of long non-coding RNA-ZFAS1 protects cardiomyocytes against acute myocardial infarction via anti-apoptosis by regulating miR-150/CRP. Journal of Cellular Biochemistry, 118, 3281–3289.

    Article  CAS  PubMed  Google Scholar 

  59. Hao, S., Liu, X., Sui, X., et al. (2018). Long non-coding RNA GAS5 reduces cardiomyocyte apoptosis induced by MI through sema3a. International Journal of Biological Macromolecules, 120, 371–377.

    Article  CAS  PubMed  Google Scholar 

  60. Zhao, C., Liu, J., Zhang, M., et al. (2016). Semaphorin 3A deficiency improves hypoxia-induced myocardial injury via resisting inflammation and cardiomyocytes apoptosis. Cellular and Molecular Biology (Noisy-le-grand), 62, 8–14.

    CAS  Google Scholar 

  61. Li, X., Hou, L., Cheng, Z., et al. (2019). Overexpression of GAS5 inhibits abnormal activation of Wnt/beta-catenin signaling pathway in myocardial tissues of rats with coronary artery disease. Journal of Cellular Physiology, 234, 11348–11359.

    Article  CAS  PubMed  Google Scholar 

  62. Takahashi-Yanaga, F., & Sasaguri, T. (2007). The Wnt/beta-catenin signaling pathway as a target in drug discovery. Journal of Pharmacological Sciences, 104, 293–302.

    Article  CAS  PubMed  Google Scholar 

  63. Zhang, Y., Hou, Y. M., Gao, F., et al. (2019). lncRNA GAS5 regulates myocardial infarction by targeting the miR-525-5p/CALM2 axis. Journal of Cellular Biochemistry, 120, 18678–18688.

    Article  CAS  PubMed  Google Scholar 

  64. Zhang, B. F., Jiang, H., Chen, J., et al. (2020). LncRNA H19 ameliorates myocardial infarction-induced myocardial injury and maladaptive cardiac remodelling by regulating KDM3A. Journal of Cellular and Molecular Medicine, 24, 1099–1115.

    Article  CAS  PubMed  Google Scholar 

  65. Chen, J., Zhang, J., Yang, J., et al. (2017). Histone demethylase KDM3a, a novel regulator of vascular smooth muscle cells, controls vascular neointimal hyperplasia in diabetic rats. Atherosclerosis, 257, 152–163.

    Article  CAS  PubMed  Google Scholar 

  66. Zhan, Y., Brown, C., Maynard, E., et al. (2005). Ets-1 is a critical regulator of Ang II-mediated vascular inflammation and remodeling. The Journal of Clinical Investigation, 115, 2508–2516.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Bian, C., Xu, T., Zhu, H., et al. (2015). Luteolin inhibits ischemia/reperfusion-induced myocardial injury in rats via downregulation of microRNA-208b-3p. PLOS ONE, 10, e144877.

    Google Scholar 

  68. Shi, H. J., Wang, M. W., Sun, J. T., et al. (2019). A novel long noncoding RNA FAF inhibits apoptosis via upregulating FGF9 through PI3K/AKT signaling pathway in ischemia-hypoxia cardiomyocytes. Journal of Cellular Physiology, 234, 21973–21987.

    Article  CAS  PubMed  Google Scholar 

  69. Liu, Y., Wang, T., Zhang, M., et al. (2019). Down-regulation of myocardial infarction associated transcript 1 improves myocardial ischemia-reperfusion injury in aged diabetic rats by inhibition of activation of NF-kappaB signaling pathway. Chemico-Biological Interactions, 300, 111–122.

    Article  CAS  PubMed  Google Scholar 

  70. Li, X., Zhou, J., & Huang, K. (2017). Inhibition of the lncRNA Mirt1 attenuates acute myocardial infarction by suppressing NF-kappaB activation. Cellular Physiology and Biochemistry, 42, 1153–1164.

    Article  CAS  PubMed  Google Scholar 

  71. Yu, J., & Zhang, L. (2008). PUMA, a potent killer with or without p53. Oncogene, 27(Suppl 1), S71-83.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Sun, J., Knickelbein, K., He, K., et al. (2014). Aurora kinase inhibition induces PUMA via NF-kappaB to kill colon cancer cells. Molecular Cancer Therapeutics, 13, 1298–1308.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Zhang, B., Song, C., Feng, B., et al. (2016). Neuroprotection by triptolide against cerebral ischemia/reperfusion injury through the inhibition of NF-kappaB/PUMA signal in rats. Therapeutics and Clinical Risk Management, 12, 817–824.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Chen, L., Zhang, D., Yu, L., et al. (2019). Targeting MIAT reduces apoptosis of cardiomyocytes after ischemia/reperfusion injury. Bioengineered, 10, 121–132.

    Article  PubMed  PubMed Central  Google Scholar 

  75. Cao, X., Ma, Q., Wang, B., et al. (2021). Silencing long non-coding RNA MIAT ameliorates myocardial dysfunction induced by myocardial infarction via MIAT/miR-10a-5p/EGR2 axis. Aging (Albany NY), 13, 11188–11206.

    Article  CAS  Google Scholar 

  76. He, Z., Zeng, X., Zhou, D., et al. (2021). LncRNA Chaer prevents cardiomyocyte apoptosis from acute myocardial infarction through AMPK activation. Frontiers in Pharmacology, 12, 649398.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Bairwa, S. C., Parajuli, N., & Dyck, J. R. (2016). The role of AMPK in cardiomyocyte health and survival. Biochimica et Biophysica Acta, 1862, 2199–2210.

    Article  CAS  PubMed  Google Scholar 

  78. Zhuo, X. Z., Wu, Y., Ni, Y. J., et al. (2013). Isoproterenol instigates cardiomyocyte apoptosis and heart failure via AMPK inactivation-mediated endoplasmic reticulum stress. Apoptosis, 18, 800–810.

    Article  CAS  PubMed  Google Scholar 

  79. Zhou, L., Sun, C. B., Liu, C., et al. (2015). Upregulation of arginase activity contributes to intracellular ROS production induced by high glucose in H9c2 cells. International Journal of Clinical and Experimental Pathology, 8, 2728–2736.

    PubMed  PubMed Central  Google Scholar 

  80. Huynh, K., Bernardo, B. C., McMullen, J. R., et al. (2014). Diabetic cardiomyopathy: Mechanisms and new treatment strategies targeting antioxidant signaling pathways. Pharmacology & Therapeutics, 142, 375–415.

    Article  CAS  Google Scholar 

  81. Zou, G., Zhong, W., Wu, F., et al. (2019). Catalpol attenuates cardiomyocyte apoptosis in diabetic cardiomyopathy via Neat1/miR-140-5p/HDAC4 axis. Biochimie, 165, 90–99.

    Article  CAS  PubMed  Google Scholar 

  82. Zhou, X., Zhang, W., Jin, M., et al. (2017). lncRNA MIAT functions as a competing endogenous RNA to upregulate DAPK2 by sponging miR-22–3p in diabetic cardiomyopathy. Cell Death & Disease, 8, e2929.

    Article  CAS  Google Scholar 

  83. Britschgi, A., Trinh, E., Rizzi, M., et al. (2008). DAPK2 is a novel E2F1/KLF6 target gene involved in their proapoptotic function. Oncogene, 27, 5706–5716.

    Article  CAS  PubMed  Google Scholar 

  84. Schlegel, C. R., Fonseca, A. V., Stocker, S., et al. (2014). DAPK2 is a novel modulator of TRAIL-induced apoptosis. Cell Death and Differentiation, 21, 1780–1791.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Gao, W. L., Liu, M., Yang, Y., et al. (2012). The imprinted H19 gene regulates human placental trophoblast cell proliferation via encoding miR-675 that targets Nodal Modulator 1 (NOMO1). RNA Biology, 9, 1002–1010.

    Article  CAS  PubMed  Google Scholar 

  86. Dey, B. K., Pfeifer, K., & Dutta, A. (2014). The H19 long noncoding RNA gives rise to microRNAs miR-675-3p and miR-675-5p to promote skeletal muscle differentiation and regeneration. Genes & Development, 28, 491–501.

    Article  Google Scholar 

  87. Li, X., Wang, H., Yao, B., et al. (2016). lncRNA H19/miR-675 axis regulates cardiomyocyte apoptosis by targeting VDAC1 in diabetic cardiomyopathy. Science and Reports, 6, 36340.

    Article  CAS  Google Scholar 

  88. Shoshan-Barmatz, V., Mizrachi, D., & Keinan, N. (2013). Oligomerization of the mitochondrial protein VDAC1: From structure to function and cancer therapy. Progress in Molecular Biology and Translational Science, 117, 303–334.

    Article  CAS  PubMed  Google Scholar 

  89. Shoshan-Barmatz, V., & Golan, M. (2012). Mitochondrial VDAC1: Function in cell life and death and a target for cancer therapy. Current Medicinal Chemistry, 19, 714–735.

    Article  CAS  PubMed  Google Scholar 

  90. Shimizu, S., Matsuoka, Y., Shinohara, Y., et al. (2001). Essential role of voltage-dependent anion channel in various forms of apoptosis in mammalian cells. Journal of Cell Biology, 152, 237–250.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Yu, F. R., Xia, Y. W., Wang, S. B., et al. (2021). Long noncoding RNA PVT1 facilitates high glucose-induced cardiomyocyte death through the miR-23a-3p/CASP10 axis. Cell Biology International, 45, 154–163.

    Article  PubMed  CAS  Google Scholar 

  92. Milhas, D., Cuvillier, O., Therville, N., et al. (2005). Caspase-10 triggers Bid cleavage and caspase cascade activation in FasL-induced apoptosis. Journal of Biological Chemistry, 280, 19836–19842.

    Article  CAS  PubMed  Google Scholar 

  93. Wang, C., Liu, G., Yang, H., et al. (2021). MALAT1-mediated recruitment of the histone methyltransferase EZH2 to the microRNA-22 promoter leads to cardiomyocyte apoptosis in diabetic cardiomyopathy. The Science of the Total Environment, 766, 142191.

    Article  CAS  PubMed  Google Scholar 

  94. Zhao, S. F., Ye, Y. X., Xu, J. D., et al. (2021). Long non-coding RNA KCNQ1OT1 increases the expression of PDCD4 by targeting miR-181a-5p, contributing to cardiomyocyte apoptosis in diabetic cardiomyopathy. Acta Diabetologica, 58, 1251–1267.

    Article  CAS  PubMed  Google Scholar 

  95. Octavia, Y., Tocchetti, C. G., Gabrielson, K. L., et al. (2012). Doxorubicin-induced cardiomyopathy: From molecular mechanisms to therapeutic strategies. Journal of Molecular and Cellular Cardiology, 52, 1213–1225.

    Article  CAS  PubMed  Google Scholar 

  96. Zhan, J., Hu, P., & Wang, Y. (2020). lncRNA PVT1 aggravates doxorubicin-induced cardiomyocyte apoptosis by targeting the miR-187–3p/AGO1 axis. Molecular and Cellular Probes, 49, 101490.

    Article  CAS  PubMed  Google Scholar 

  97. Mondal, T., Bag, I., Sncvl, P., et al. (2018). Two way controls of apoptotic regulators consign DmArgonaute-1 a better clasp on it. PLOS ONE, 13, e190548.

    Article  CAS  Google Scholar 

  98. Parisi, C., Giorgi, C., Batassa, E. M., et al. (2011). Ago1 and Ago2 differentially affect cell proliferation, motility and apoptosis when overexpressed in SH-SY5Y neuroblastoma cells. FEBS Letters, 585, 2965–2971.

    Article  CAS  PubMed  Google Scholar 

  99. Li, J., Li, L., Li, X., et al. (2018). Long noncoding RNA LINC00339 aggravates doxorubicin-induced cardiomyocyte apoptosis by targeting MiR-484. Biochemical and Biophysical Research Communications, 503, 3038–3043.

    Article  CAS  PubMed  Google Scholar 

  100. Wang, K., Long, B., Jiao, J. Q., et al. (2012). miR-484 regulates mitochondrial network through targeting Fis1. Nature Communications, 3, 781.

    Article  PubMed  CAS  Google Scholar 

  101. Abdelwahid, E., Li, H., Wu, J., et al. (2016). Endoplasmic reticulum (ER) stress triggers Hax1-dependent mitochondrial apoptotic events in cardiac cells. Apoptosis, 21, 1227–1239.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Grzybowska, E. A., Zayat, V., Konopinski, R., et al. (2013). HAX-1 is a nucleocytoplasmic shuttling protein with a possible role in mRNA processing. FEBS Journal, 280, 256–272.

    Article  CAS  PubMed  Google Scholar 

  103. Jans, D. A., Martin, A. J., & Wagstaff, K. M. (2019). Inhibitors of nuclear transport. Current Opinion in Cell Biology, 58, 50–60.

    Article  CAS  PubMed  Google Scholar 

  104. Liu, Y., Duan, C., Liu, W., et al. (2019). Upregulation of let-7f-2-3p by long noncoding RNA NEAT1 inhibits XPO1-mediated HAX-1 nuclear export in both in vitro and in vivo rodent models of doxorubicin-induced cardiotoxicity. Archives of Toxicology, 93, 3261–3276.

    Article  CAS  PubMed  Google Scholar 

  105. Zhang, Y., Zhang, M., Xu, W., et al. (2017). The long non-coding RNA H19 promotes cardiomyocyte apoptosis in dilated cardiomyopathy. Oncotarget, 8, 28588–28594.

    Article  PubMed  PubMed Central  Google Scholar 

  106. Figeac, N., Serralbo, O., Marcelle, C., et al. (2014). ErbB3 binding protein-1 (Ebp1) controls proliferation and myogenic differentiation of muscle stem cells. Developmental Biology, 386, 135–151.

    Article  CAS  PubMed  Google Scholar 

  107. Okada, M., Jang, S. W., & Ye, K. (2007). Ebp1 association with nucleophosmin/B23 is essential for regulating cell proliferation and suppressing apoptosis. Journal of Biological Chemistry, 282, 36744–36754.

    Article  CAS  PubMed  Google Scholar 

  108. Lai, L., Xu, Y., Kang, L., et al. (2020). LncRNA KCNQ1OT1 contributes to cardiomyocyte apoptosis by targeting FUS in heart failure. Experimental and Molecular Pathology, 115, 104480.

    Article  CAS  PubMed  Google Scholar 

  109. Deng, J., Yang, M., Chen, Y., et al. (2015). FUS interacts with HSP60 to promote mitochondrial damage. PLOS Genet, 11, e1005357.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  110. Wang, H., Lin, X., Li, J., et al. (2021). Long noncoding RNA SOX2-OT Aggravates doxorubicin-induced apoptosis of cardiomyocyte by targeting miR-942-5p/DP5. Drug Design, Development and Therapy, 15, 481–492.

    Article  PubMed  PubMed Central  Google Scholar 

  111. Chen, S., Lee, J. M., Zeng, C., et al. (2006). Amyloid beta peptide increases DP5 expression via activation of neutral sphingomyelinase and JNK in oligodendrocytes. Journal of Neurochemistry, 97, 631–640.

    Article  CAS  PubMed  Google Scholar 

  112. Kumarswamy, R., Bauters, C., Volkmann, I., et al. (2014). Circulating long noncoding RNA, LIPCAR, predicts survival in patients with heart failure. Circulation Research, 114, 1569–1575.

    Article  CAS  PubMed  Google Scholar 

  113. Yang, Y., Cai, Y., Wu, G., et al. (2015). Plasma long non-coding RNA, CoroMarker, a novel biomarker for diagnosis of coronary artery disease. Clinical Science (London, England), 129, 675–685.

    Article  CAS  Google Scholar 

  114. Lorenzen, J. M., Schauerte, C., Kielstein, J. T., et al. (2015). Circulating long noncoding RNATapSaki is a predictor of mortality in critically ill patients with acute kidney injury. Clinical Chemistry, 61, 191–201.

    Article  CAS  PubMed  Google Scholar 

  115. Bai, Z., Li, Y., Li, Y., et al. (2020). Long noncoding RNA and messenger RNA abnormalities in pediatric sepsis: A preliminary study. BMC Medical Genomics, 13, 36.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Fotuhi, S. N., Khalaj-Kondori, M., Hoseinpour, F. M., et al. (2019). Long non-coding RNA BACE1-AS May Serve as an Alzheimer’s Disease Blood-Based Biomarker. Journal of Molecular Neuroscience, 69, 351–359.

    Article  CAS  PubMed  Google Scholar 

  117. Cui, X., Sun, X., Niu, W., et al. (2016). Long non-coding RNA: Potential diagnostic and therapeutic biomarker for major depressive disorder. Medical Science Monitor, 22, 5240–5248.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Liang, Z., Zhu, B., Meng, D., et al. (2019). Down-regulation of lncRNA-NEF indicates poor prognosis in intrahepatic cholangiocarcinoma. Bioscience Reports, 39.

  119. Bayarmaa, B., Wu, Z., Peng, J., et al. (2019). Association of LncRNA MEG3 polymorphisms with efficacy of neoadjuvant chemotherapy in breast cancer. BMC Cancer, 19, 877.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  120. Yin, Q., Shen, X., Cui, X., et al. (2019). Elevated serum lncRNA TUG1 levels are a potential diagnostic biomarker of multiple myeloma. Experimental Hematology, 79, 47–55.

    Article  CAS  PubMed  Google Scholar 

  121. Schlosser, K., Hanson, J., Villeneuve, P. J., et al. (2016). Assessment of circulating LncRNAs under physiologic and pathologic conditions in humans reveals potential limitations as biomarkers. Science and Reports, 6, 36596.

    Article  CAS  Google Scholar 

Download references

Funding

This study was funded by the National Natural Sciences Foundation of China (grant number 81874410).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Chenglong Wang.

Ethics declarations

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Conflict of Interest

The authors declare no competing interests.

Additional information

Associate Editor Junjie Xiao oversaw the review of this article.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sun, J., Wang, R., Chao, T. et al. Long Noncoding RNAs Involved in Cardiomyocyte Apoptosis Triggered by Different Stressors. J. of Cardiovasc. Trans. Res. 15, 588–603 (2022). https://doi.org/10.1007/s12265-021-10186-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12265-021-10186-w

Keywords

Navigation