MicroRNA-17-3p protects against excessive posthypoxic autophagy in H9C2 cardiomyocytes via PTEN-Akt-mTOR signaling pathway.
autophagy
cardiomyocytes
hypoxia/reoxygenation
microRNA
rat
Journal
Cell biology international
ISSN: 1095-8355
Titre abrégé: Cell Biol Int
Pays: England
ID NLM: 9307129
Informations de publication
Date de publication:
May 2023
May 2023
Historique:
revised:
13
12
2022
received:
12
07
2022
accepted:
02
01
2023
medline:
7
4
2023
pubmed:
20
3
2023
entrez:
19
3
2023
Statut:
ppublish
Résumé
The activity of phosphatase and tensin homolog (PTEN) can be inhibited by miR-17-3p, which results in attenuating myocardial ischemia/reperfusion injury (IRI), however, the mechanism behind this phenomenon is still elusive. Suppression of PTEN leads to augmented protein kinase B (Akt)/mammalian target of rapamycin (mTOR) signaling strength and constrained autophagy activation, which might be the one mechanism for the ameliorated myocardial IRI. Thus, we tested the hypothesis that miR-17-3p attenuated hypoxia/reoxygenation (H/R)-mediated damage in cardiomyocytes by downregulating excessive autophagy via the PTEN-Akt-mTOR axis. The expression of miR-17-3p was remarkably increased after H/R treatment (6-h hypoxia followed by 6-h reoxygenation; H6/R6), which was concomitant with the increase of the release of lactic acid dehydrogenase (cell injury marker) and the enhancement LC3II/I ratio (autophagy markers) in H9C2 cardiomyocytes. Ectoexpression of miR-17-3p agomir led to remarkable augmentation of miR-17-3p expression and evidently attenuated H/R-mediated cell damage and excessive autophagy. Furthermore, an increase in miR-17-3p expression elicited constrained phosphorylation of PTEN (Ser
Substances chimiques
Proto-Oncogene Proteins c-akt
EC 2.7.11.1
MicroRNAs
0
TOR Serine-Threonine Kinases
EC 2.7.11.1
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
943-953Subventions
Organisme : Administration of Traditional Chinese Medicine of Guangdong Province
ID : 20221009
Informations de copyright
© 2023 International Federation for Cell Biology.
Références
Aoki, M., & Fujishita, T. (2017). Oncogenic roles of the PI3K/AKT/mTOR axis. Current Topics in Microbiology and Immunology, 407, 153-189.
Bai, X., Hua, S., Zhang, J., & Xu, S. (2019). The microRNA family both in normal development and in different diseases: The miR-17-92 cluster. BioMed Research International, 2019, 9450240.
Cai, Y., Ying, F., Liu, H., Ge, L., Song, E., Wang, L., Zhang, D., Hoi Ching Tang, E., Xia, Z., & Irwin, M. G. (2020). Deletion of Rap1 protects against myocardial ischemia/reperfusion injury through suppressing cell apoptosis via activation of STAT3 signaling. The FASEB Journal, 34(3), 4482-4496.
Cai, Y., Ying, F., Song, E., Wang, Y., Xu, A., Vanhoutte, P. M., & Tang, E. H. C. (2015). Mice lacking prostaglandin E receptor subtype 4 manifest disrupted lipid metabolism attributable to impaired triglyceride clearance. The FASEB Journal, 29(12), 4924-4936.
Chatterjee, A., Chattopadhyay, D., & Chakrabarti, G. (2014). miR-17-5p downregulation contributes to paclitaxel resistance of lung cancer cells through altering beclin1 expression. PLoS ONE, 9(4), e95716.
Chen, J., Huang, Z. P., Seok, H. Y., Ding, J., Kataoka, M., Zhang, Z., Hu, X., Wang, G., Lin, Z., Wang, S., Pu, W. T., Liao, R., & Wang, D. Z. (2013). mir-17-92 Cluster is required for and sufficient to induce cardiomyocyte proliferation in postnatal and adult hearts. Circulation Research, 112(12), 1557-1566.
Comincini, S., Allavena, G., Palumbo, S., Morini, M., Durando, F., Angeletti, F., Pirtoli, L., & Miracco, C. (2013). microRNA-17 regulates the expression of ATG7 and modulates the autophagy process, improving the sensitivity to temozolomide and low-dose ionizing radiation treatments in human glioblastoma cells. Cancer Biology & Therapy, 14(7), 574-586.
Davidson, S. M., Ferdinandy, P., Andreadou, I., Bøtker, H. E., Heusch, G., Ibáñez, B., Ovize, M., Schulz, R., Yellon, D. M., Hausenloy, D. J., & Garcia-Dorado, D. (2019). Multitarget strategies to reduce myocardial ischemia/reperfusion injury. Journal of the American College of Cardiology, 73(1), 89-99.
Gao, F., Kataoka, M., Liu, N., Liang, T., Huang, Z. P., Gu, F., Ding, J., Liu, J., Zhang, F., Ma, Q., Wang, Y., Zhang, M., Hu, X., Kyselovic, J., Hu, X., Pu, W. T., Wang, J., Chen, J., & Wang, D. Z. (2019). Therapeutic role of miR-19a/19b in cardiac regeneration and protection from myocardial infarction. Nature Communications, 10(1), 1802.
Ge, L., Cai, Y., Ying, F., Liu, H., Zhang, D., He, Y., Pang, L., Yan, D., Xu, A., Ma, H., & Xia, Z. (2019). miR-181c-5p exacerbates hypoxia/reoxygenation-induced cardiomyocyte apoptosis via targeting PTPN4. Oxidative Medicine and Cellular Longevity, 2019, 1957920.
Gui, L., Liu, B., & Lv, G. (2016). Hypoxia induces autophagy in cardiomyocytes via a hypoxia-inducible factor 1-dependent mechanism. Experimental and Therapeutic Medicine, 11(6), 2233-2239.
Guo, J., Mei, Y., Li, K., Huang, X., & Yang, H. (2016). Downregulation of miR-17-92a cluster promotes autophagy induction in response to celastrol treatment in prostate cancer cells. Biochemical and Biophysical Research Communications, 478(2), 804-810.
Hu, Z., Cai, H. Y., Luo, Y. Y., Xiao, J. M., Li, L., & Guo, T. (2018). Effect of varying hypoxia reoxygenation times on autophagy of cardiomyocytes. Acta cirurgica brasileira, 33(3), 223-230.
Hua, Y., Zhang, Y., Ceylan-Isik, A. F., Wold, L. E., Nunn, J. M., & Ren, J. (2011). Chronic Akt activation accentuates aging-induced cardiac hypertrophy and myocardial contractile dysfunction: Role of autophagy. Basic Research in Cardiology, 106(6), 1173-1191.
Huang, Z., Wu, S., Kong, F., Cai, X., Ye, B., Shan, P., & Huang, W. (2017). MicroRNA-21 protects against cardiac hypoxia/reoxygenation injury by inhibiting excessive autophagy in H9c2 cells via the Akt/mTOR pathway. Journal of Cellular and Molecular Medicine, 21(3), 467-474.
Keyes, K. T., Xu, J., Long, B., Zhang, C., Hu, Z., & Ye, Y. (2010). Pharmacological inhibition of PTEN limits myocardial infarct size and improves left ventricular function postinfarction. American Journal of Physiology:Heart and Circulatory Physiology, 298(4), H1198-H1208.
Maejima, Y., Chen, Y., Isobe, M., Gustafsson, Å. B., Kitsis, R. N., & Sadoshima, J. (2015). Recent progress in research on molecular mechanisms of autophagy in the heart. American Journal of Physiology: Heart and Circulatory Physiology, 308(4), H259-H268.
Maron, B. J., Roberts, W. C., Arad, M., Haas, T. S., Spirito, P., Wright, G. B., Almquist, A. K., Baffa, J. M., Saul, J. P., Ho, C. Y., Seidman, J., & Seidman, C. E. (2009). Clinical outcome and phenotypic expression in LAMP2 cardiomyopathy. JAMA, 301(12), 1253-1259.
Matsui, T., Li, L., Wu, J. C., Cook, S. A., Nagoshi, T., Picard, M. H., Liao, R., & Rosenzweig, A. (2002). Phenotypic spectrum caused by transgenic overexpression of activated Akt in the heart. Journal of Biological Chemistry, 277(25), 22896-22901.
Mialet-Perez, J., & Vindis, C. (2017). Autophagy in health and disease: Focus on the cardiovascular system. Essays in Biochemistry, 61(6), 721-732.
Olivetti, G. (1996). Acute myocardial infarction in humans is associated with activation of programmed myocyte cell death in the surviving portion of the heart. Journal of Molecular and Cellular Cardiology, 28(9), 2005-2016.
Pang, J., Fuller, N. D., Hu, N., Barton, L. A., Henion, J. M., Guo, R., Chen, Y., & Ren, J. (2016). Alcohol dehydrogenase protects against endoplasmic reticulum Stress-Induced myocardial contractile dysfunction via attenuation of oxidative stress and autophagy: Role of PTEN-Akt-mTOR signaling. PLoS ONE, 11(1), e0147322.
Pang, L., Cai, Y., Tang, E. H. C., Irwin, M. G., Ma, H., & Xia, Z. (2016). Prostaglandin E receptor subtype 4 signaling in the heart: Role in ischemia/reperfusion injury and cardiac hypertrophy. Journal of Diabetes Research, 2016, 1324347.
Pang, L., Cai, Y., Tang, E. H. C., Yan, D., Kosuru, R., Li, H., Irwin, M. G., Ma, H., & Xia, Z. (2016). Cox-2 inhibition protects against hypoxia/reoxygenation-induced cardiomyocyte apoptosis via Akt-dependent enhancement of iNOS expression. Oxidative Medicine and Cellular Longevity, 2016, 3453059.
Parajuli, N., Yuan, Y., Zheng, X., Bedja, D., & Cai, Z. P. (2012). Phosphatase PTEN is critically involved in post-myocardial infarction remodeling through the Akt/interleukin-10 signaling pathway. Basic Research in Cardiology, 107(2), 248.
Saha, S., Panigrahi, D. P., Patil, S., & Bhutia, S. K. (2018). Autophagy in health and disease: A comprehensive review. Biomedicine & Pharmacotherapy, 104, 485-495.
Saito, T., & Sadoshima, J. (2015). Molecular mechanisms of mitochondrial autophagy/mitophagy in the heart. Circulation Research, 116(8), 1477-1490.
Shi, J., Bei, Y., Kong, X., Liu, X., Lei, Z., Xu, T., Wang, H., Xuan, Q., Chen, P., Xu, J., Che, L., Liu, H., Zhong, J., Sluijter, J. P., Li, X., Rosenzweig, A., & Xiao, J. (2017). miR-17-3p contributes to exercise-induced cardiac growth and protects against myocardial ischemia-reperfusion injury. Theranostics, 7(3), 664-676.
Shi, J., Chen, C., Xu, X., & Lu, Q. (2019). miR-29a promotes pathological cardiac hypertrophy by targeting the PTEN/AKT/mTOR signalling pathway and suppressing autophagy. Acta Physiologica, 227(2), e13323.
Shirakabe, A., Ikeda, Y., Sciarretta, S., Zablocki, D. K., & Sadoshima, J. (2016). Aging and autophagy in the heart. Circulation Research, 118(10), 1563-1576.
Vergadi, E., Ieronymaki, E., Lyroni, K., Vaporidi, K., & Tsatsanis, C. (2017). Akt signaling pathway in macrophage activation and M1/M2 polarization, Journal of immunology, 198(3), 1006-1014.
Wan, G., Xie, W., Liu, Z., Xu, W., Lao, Y., Huang, N., Cui, K., Liao, M., He, J., Jiang, Y., Yang, B. B., Xu, H., Xu, N., & Zhang, Y. (2014). Hypoxia-induced MIR155 is a potent autophagy inducer by targeting multiple players in the MTOR pathway. Autophagy, 10(1), 70-79.
Wang, S., Wang, C., Yan, F., Wang, T., He, Y., Li, H., Xia, Z., & Zhang, Z. (2017). N-Acetylcysteine attenuates diabetic myocardial ischemia reperfusion injury through inhibiting excessive autophagy. Mediators of Inflammation, 2017, 9257291.
Wang, X., Chen, J., & Huang, X. (2019). Rosuvastatin attenuates myocardial ischemia-reperfusion injury via upregulating miR-17-3p-mediated autophagy. Cellular Reprogramming, 21(6), 323-330.
Xia, P., Liu, Y., & Cheng, Z. (2016). Signaling pathways in cardiac myocyte apoptosis. BioMed Research International, 2016, 9583268.
Ye, X., He, Y., Wang, S., Wong, G. T., Irwin, M. G., & Xia, Z. (2018). Heart-type fatty acid binding protein (H-FABP) as a biomarker for acute myocardial injury and long-term post-ischemic prognosis. Acta Pharmacologica Sinica, 39(7), 1155-1163.
Ying, F., Cai, Y., Cai, Y., Wang, Y., & Ching Tang, E. H. (2017). Prostaglandin E receptor subtype 4 regulates lipid droplet size and mitochondrial activity in murine subcutaneous white adipose tissue. The FASEB Journal, 31(9), 4023-4036.
Zhai, H., Fesler, A., & Ju, J. (2013). MicroRNA: A third dimension in autophagy. Cell Cycle, 12(2), 246-250.
Zhang, D., He, Y., Ye, X., Cai, Y., Xu, J., Zhang, L., Li, M., Liu, H., Wang, S., & Xia, Z. (2020). Activation of autophagy inhibits nucleotide-binding oligomerization domain-like receptor protein 3 inflammasome activation and attenuates myocardial ischemia-reperfusion injury in diabetic rats. Journal of Diabetes Investigation, 11(5), 1126-1136.
Zhang, X., Li, Y., Qi, P., & Ma, Z. (2018). Biology of miR-17-92 cluster and its progress in lung cancer. International Journal of Medical Sciences, 15(13), 1443-1448.
Zullo, A. J., Jurcic Smith, K. L., & Lee, S. (2014). Mammalian target of rapamycin inhibition and mycobacterial survival are uncoupled in murine macrophages. BMC Biochemistry, 15, 4.