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Erschienen in: Journal of Cardiovascular Translational Research 1/2019

20.03.2018

miRNA Profiling of Exosomes from Spontaneous Hypertensive Rats Using Next-Generation Sequencing

verfasst von: Xiaoyan Liu, Wen Yuan, Lei Yang, Jing Li, Jun Cai

Erschienen in: Journal of Cardiovascular Translational Research | Ausgabe 1/2019

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Abstract

The role and miRNA expression profile of exosomes in hypertension remain largely unknown. Therefore, next-generation sequencing was used to define the miRNA expression profile of plasma exosomes in spontaneously hypertensive rats (SHRs), the most widely used animal model of human essential hypertension, and their controls, normotensive Wistar-Kyoto rats (WKYs). Results revealed that percentages of miRNA in the total small RNA isolated from SHRs and WKYs were not significantly different. Twenty-seven miRNAs were significantly differentially expressed (DE) between SHR and WKY exosomes, including 23 up-regulated and four down-regulated in SHR exosomes as compared to WKY exosomes. Gene Ontology analysis and Kyoto Encyclopedia of Genes and Genomes pathway analysis of top 10 DE miRNAs identified hypertension-specific target genes/signaling pathways. In conclusion, our findings indicated the selective packing of miRNA cargo into exosomes under hypertensive status, which could facilitate the development of potential targets for the diagnosis, prevention, and treatment of hypertension.
Literatur
1.
Zurück zum Zitat Li, L., Li, C., Wang, S., Wang, Z., Jiang, J., Wang, W., et al. (2016). Exosomes derived from hypoxic oral squamous cell carcinoma cells deliver miR-21 to normoxic cells to elicit a prometastatic phenotype. Cancer Research, 76(7), 1770–1780.CrossRefPubMed Li, L., Li, C., Wang, S., Wang, Z., Jiang, J., Wang, W., et al. (2016). Exosomes derived from hypoxic oral squamous cell carcinoma cells deliver miR-21 to normoxic cells to elicit a prometastatic phenotype. Cancer Research, 76(7), 1770–1780.CrossRefPubMed
2.
Zurück zum Zitat Pierdomenico, S. D., Di Nicola, M., Esposito, A. L., Di Mascio, R., Ballone, E., Lapenna, D., et al. (2009). Prognostic value of different indices of blood pressure variability in hypertensive patients. American Journal of Hypertension, 22(8), 842–847.CrossRefPubMed Pierdomenico, S. D., Di Nicola, M., Esposito, A. L., Di Mascio, R., Ballone, E., Lapenna, D., et al. (2009). Prognostic value of different indices of blood pressure variability in hypertensive patients. American Journal of Hypertension, 22(8), 842–847.CrossRefPubMed
3.
Zurück zum Zitat Leung, A., Trac, C., Jin, W., Lanting, L., Akbany, A., Saetrom, P., et al. (2013). Novel long noncoding RNAs are regulated by angiotensin II in vascular smooth muscle cells. Circulation Research, 113(3), 266–278.CrossRefPubMedPubMedCentral Leung, A., Trac, C., Jin, W., Lanting, L., Akbany, A., Saetrom, P., et al. (2013). Novel long noncoding RNAs are regulated by angiotensin II in vascular smooth muscle cells. Circulation Research, 113(3), 266–278.CrossRefPubMedPubMedCentral
4.
Zurück zum Zitat Thery, C., Zitvogel, L., & Amigorena, S. (2002). Exosomes: Composition, biogenesis and function. Nature Reviews. Immunology, 2(8), 569–579.CrossRefPubMed Thery, C., Zitvogel, L., & Amigorena, S. (2002). Exosomes: Composition, biogenesis and function. Nature Reviews. Immunology, 2(8), 569–579.CrossRefPubMed
5.
Zurück zum Zitat Thompson, A. G., Gray, E., Heman-Ackah, S. M., Mager, I., Talbot, K., Andaloussi, S. E., et al. (2016). Extracellular vesicles in neurodegenerative disease—pathogenesis to biomarkers. Nature Reviews. Neurology, 12(6), 346–357.CrossRefPubMed Thompson, A. G., Gray, E., Heman-Ackah, S. M., Mager, I., Talbot, K., Andaloussi, S. E., et al. (2016). Extracellular vesicles in neurodegenerative disease—pathogenesis to biomarkers. Nature Reviews. Neurology, 12(6), 346–357.CrossRefPubMed
6.
Zurück zum Zitat Richards, K. E., Zeleniak, A. E., Fishel, M. L., Wu, J., Littlepage, L. E., & Hill, R. (2017). Cancer-associated fibroblast exosomes regulate survival and proliferation of pancreatic cancer cells. Oncogene, 36(13), 1770–1778.CrossRefPubMed Richards, K. E., Zeleniak, A. E., Fishel, M. L., Wu, J., Littlepage, L. E., & Hill, R. (2017). Cancer-associated fibroblast exosomes regulate survival and proliferation of pancreatic cancer cells. Oncogene, 36(13), 1770–1778.CrossRefPubMed
7.
Zurück zum Zitat Srikanthan, S., Li, W., Silverstein, R. L., & McIntyre, T. M. (2014). Exosome poly-ubiquitin inhibits platelet activation, downregulates CD36 and inhibits pro-atherothombotic cellular functions. Journal of Thrombosis and Haemostasis, 12(11), 1906–1917.CrossRefPubMed Srikanthan, S., Li, W., Silverstein, R. L., & McIntyre, T. M. (2014). Exosome poly-ubiquitin inhibits platelet activation, downregulates CD36 and inhibits pro-atherothombotic cellular functions. Journal of Thrombosis and Haemostasis, 12(11), 1906–1917.CrossRefPubMed
8.
Zurück zum Zitat Tkach, M., & Thery, C. (2016). Communication by extracellular vesicles: where we are and where we need to go. Cell, 164(6), 1226–1232.CrossRefPubMed Tkach, M., & Thery, C. (2016). Communication by extracellular vesicles: where we are and where we need to go. Cell, 164(6), 1226–1232.CrossRefPubMed
9.
Zurück zum Zitat Boulanger, C. M., Loyer, X., Rautou, P. E., & Amabile, N. (2017). Extracellular vesicles in coronary artery disease. Nature Reviews. Cardiology, 14(5), 259–272.CrossRefPubMed Boulanger, C. M., Loyer, X., Rautou, P. E., & Amabile, N. (2017). Extracellular vesicles in coronary artery disease. Nature Reviews. Cardiology, 14(5), 259–272.CrossRefPubMed
10.
Zurück zum Zitat Cocucci, E., Racchetti, G., & Meldolesi, J. (2009). Shedding microvesicles: artefacts no more. Trends in Cell Biology, 19(2), 43–51.CrossRefPubMed Cocucci, E., Racchetti, G., & Meldolesi, J. (2009). Shedding microvesicles: artefacts no more. Trends in Cell Biology, 19(2), 43–51.CrossRefPubMed
11.
Zurück zum Zitat Au, Y. C., Co, N. N., Tsuruga, T., Yeung, T. L., Kwan, S. Y., Leung, C. S., et al. (2016). Exosomal transfer of stroma-derived miR21 confers paclitaxel resistance in ovarian cancer cells through targeting APAF1. Nature Communications, 7, 11150.CrossRef Au, Y. C., Co, N. N., Tsuruga, T., Yeung, T. L., Kwan, S. Y., Leung, C. S., et al. (2016). Exosomal transfer of stroma-derived miR21 confers paclitaxel resistance in ovarian cancer cells through targeting APAF1. Nature Communications, 7, 11150.CrossRef
12.
Zurück zum Zitat Deng, Z., Rong, Y., Teng, Y., Zhuang, X., Samykutty, A., Mu, J., et al. (2017). Exosomes miR-126a released from MDSC induced by DOX treatment promotes lung metastasis. Oncogene, 36(5), 639–651.CrossRefPubMed Deng, Z., Rong, Y., Teng, Y., Zhuang, X., Samykutty, A., Mu, J., et al. (2017). Exosomes miR-126a released from MDSC induced by DOX treatment promotes lung metastasis. Oncogene, 36(5), 639–651.CrossRefPubMed
13.
Zurück zum Zitat Nguyen, M.A., Karunakaran, D., Geoffrion, M., Cheng, H.S., Tandoc, K., & Perisic, M.L., et al. (2017). Extracellular vesicles secreted by atherogenic macrophages transfer MicroRNA to inhibit cell migration. Arterioscler Thromb Vasc Biol. Nguyen, M.A., Karunakaran, D., Geoffrion, M., Cheng, H.S., Tandoc, K., & Perisic, M.L., et al. (2017). Extracellular vesicles secreted by atherogenic macrophages transfer MicroRNA to inhibit cell migration. Arterioscler Thromb Vasc Biol.
14.
Zurück zum Zitat Figueroa, J., Phillips, L.M., Shahar, T., Hossain, A., Gumin, J., & Kim, H., et al. (2017). Exosomes from glioma-associated mesenchymal stem cells increase the tumorigenicity of glioma stem-like cells via transfer of miR-1587. Cancer Res. Figueroa, J., Phillips, L.M., Shahar, T., Hossain, A., Gumin, J., & Kim, H., et al. (2017). Exosomes from glioma-associated mesenchymal stem cells increase the tumorigenicity of glioma stem-like cells via transfer of miR-1587. Cancer Res.
15.
Zurück zum Zitat Yang, V. K., Loughran, K. A., Meola, D. M., Juhr, C. M., Thane, K. E., Davis, A. M., et al. (2017). Circulating exosome microRNA associated with heart failure secondary to myxomatous mitral valve disease in a naturally occurring canine model. J Extracell Vesicles, 6(1), 1350088.CrossRefPubMedPubMedCentral Yang, V. K., Loughran, K. A., Meola, D. M., Juhr, C. M., Thane, K. E., Davis, A. M., et al. (2017). Circulating exosome microRNA associated with heart failure secondary to myxomatous mitral valve disease in a naturally occurring canine model. J Extracell Vesicles, 6(1), 1350088.CrossRefPubMedPubMedCentral
16.
Zurück zum Zitat Teng, Y., Ren, Y., Hu, X., Mu, J., Samykutty, A., Zhuang, X., et al. (2017). MVP-mediated exosomal sorting of miR-193a promotes colon cancer progression. Nature Communications, 8, 14448.CrossRefPubMedPubMedCentral Teng, Y., Ren, Y., Hu, X., Mu, J., Samykutty, A., Zhuang, X., et al. (2017). MVP-mediated exosomal sorting of miR-193a promotes colon cancer progression. Nature Communications, 8, 14448.CrossRefPubMedPubMedCentral
17.
Zurück zum Zitat Warde-Farley, D., Donaldson, S. L., Comes, O., Zuberi, K., Badrawi, R., Chao, P., et al. (2010). The GeneMANIA prediction server: biological network integration for gene prioritization and predicting gene function. Nucleic Acids Research, 38(Web Server issue), W214–W220.CrossRefPubMedPubMedCentral Warde-Farley, D., Donaldson, S. L., Comes, O., Zuberi, K., Badrawi, R., Chao, P., et al. (2010). The GeneMANIA prediction server: biological network integration for gene prioritization and predicting gene function. Nucleic Acids Research, 38(Web Server issue), W214–W220.CrossRefPubMedPubMedCentral
18.
Zurück zum Zitat von Mering, C., Huynen, M., Jaeggi, D., Schmidt, S., Bork, P., & Snel, B. (2003). STRING: a database of predicted functional associations between proteins. Nucleic Acids Research, 31(1), 258–261.CrossRef von Mering, C., Huynen, M., Jaeggi, D., Schmidt, S., Bork, P., & Snel, B. (2003). STRING: a database of predicted functional associations between proteins. Nucleic Acids Research, 31(1), 258–261.CrossRef
19.
Zurück zum Zitat Fu, S. J., Chen, J., Ji, F., Ju, W. Q., Zhao, Q., Chen, M. G., et al. (2017). MiR-486-5p negatively regulates oncogenic NEK2 in hepatocellular carcinoma. Oncotarget, 8(32), 52948–52959.PubMedPubMedCentral Fu, S. J., Chen, J., Ji, F., Ju, W. Q., Zhao, Q., Chen, M. G., et al. (2017). MiR-486-5p negatively regulates oncogenic NEK2 in hepatocellular carcinoma. Oncotarget, 8(32), 52948–52959.PubMedPubMedCentral
20.
Zurück zum Zitat Sun, Y., Su, Q., Li, L., Wang, X., Lu, Y., & Liang, J. (2017). MiR-486 regulates cardiomyocyte apoptosis by p53-mediated BCL-2 associated mitochondrial apoptotic pathway. BMC Cardiovascular Disorders, 17(1), 119.CrossRefPubMedPubMedCentral Sun, Y., Su, Q., Li, L., Wang, X., Lu, Y., & Liang, J. (2017). MiR-486 regulates cardiomyocyte apoptosis by p53-mediated BCL-2 associated mitochondrial apoptotic pathway. BMC Cardiovascular Disorders, 17(1), 119.CrossRefPubMedPubMedCentral
21.
Zurück zum Zitat Pravenec, M., Kren, V., Landa, V., Mlejnek, P., Musilova, A., Silhavy, J., et al. (2014). Recent progress in the genetics of spontaneously hypertensive rats. Physiological Research, 63(Suppl 1), S1–S8.PubMed Pravenec, M., Kren, V., Landa, V., Mlejnek, P., Musilova, A., Silhavy, J., et al. (2014). Recent progress in the genetics of spontaneously hypertensive rats. Physiological Research, 63(Suppl 1), S1–S8.PubMed
22.
Zurück zum Zitat Burke, J., Kolhe, R., Hunter, M., Isales, C., Hamrick, M., & Fulzele, S. (2016). Stem cell-derived exosomes: a potential alternative therapeutic agent in orthopaedics. Stem Cells International, 2016, 5802529.CrossRefPubMedPubMedCentral Burke, J., Kolhe, R., Hunter, M., Isales, C., Hamrick, M., & Fulzele, S. (2016). Stem cell-derived exosomes: a potential alternative therapeutic agent in orthopaedics. Stem Cells International, 2016, 5802529.CrossRefPubMedPubMedCentral
23.
Zurück zum Zitat Iraci, N., Leonardi, T., Gessler, F., Vega, B., & Pluchino, S. (2016). Focus on extracellular vesicles: physiological role and signalling properties of extracellular membrane vesicles. International Journal of Molecular Sciences, 17(2), 171.CrossRefPubMedPubMedCentral Iraci, N., Leonardi, T., Gessler, F., Vega, B., & Pluchino, S. (2016). Focus on extracellular vesicles: physiological role and signalling properties of extracellular membrane vesicles. International Journal of Molecular Sciences, 17(2), 171.CrossRefPubMedPubMedCentral
24.
Zurück zum Zitat Wu, C., Arora, P., Agha, O., Hurst, L. A., Allen, K., Nathan, D. I., et al. (2016). Novel MicroRNA regulators of atrial natriuretic peptide production. Molecular and Cellular Biology, 36(14), 1977–1987.CrossRefPubMedPubMedCentral Wu, C., Arora, P., Agha, O., Hurst, L. A., Allen, K., Nathan, D. I., et al. (2016). Novel MicroRNA regulators of atrial natriuretic peptide production. Molecular and Cellular Biology, 36(14), 1977–1987.CrossRefPubMedPubMedCentral
25.
Zurück zum Zitat Yin, J., Liu, H., Huan, L., Song, S., Han, L., Ren, F., et al. (2017). Role of miR-128 in hypertension-induced myocardial injury. Experimental and Therapeutic Medicine, 14(4), 2751–2756.CrossRefPubMedPubMedCentral Yin, J., Liu, H., Huan, L., Song, S., Han, L., Ren, F., et al. (2017). Role of miR-128 in hypertension-induced myocardial injury. Experimental and Therapeutic Medicine, 14(4), 2751–2756.CrossRefPubMedPubMedCentral
26.
Zurück zum Zitat Osada-Oka, M., Shiota, M., Izumi, Y., Nishiyama, M., Tanaka, M., Yamaguchi, T., et al. (2017). Macrophage-derived exosomes induce inflammatory factors in endothelial cells under hypertensive conditions. Hypertension Research, 40(4), 353–360.CrossRefPubMed Osada-Oka, M., Shiota, M., Izumi, Y., Nishiyama, M., Tanaka, M., Yamaguchi, T., et al. (2017). Macrophage-derived exosomes induce inflammatory factors in endothelial cells under hypertensive conditions. Hypertension Research, 40(4), 353–360.CrossRefPubMed
27.
Zurück zum Zitat Liu, X., Fortin, K., & Mourelatos, Z. (2008). MicroRNAs: biogenesis and molecular functions. Brain Pathology, 18(1), 113–121.CrossRefPubMed Liu, X., Fortin, K., & Mourelatos, Z. (2008). MicroRNAs: biogenesis and molecular functions. Brain Pathology, 18(1), 113–121.CrossRefPubMed
28.
Zurück zum Zitat Raman, M., & Cobb, M. H. (2006). TGF-beta regulation by Emilin1: new links in the etiology of hypertension. Cell, 124(5), 893–895.CrossRefPubMed Raman, M., & Cobb, M. H. (2006). TGF-beta regulation by Emilin1: new links in the etiology of hypertension. Cell, 124(5), 893–895.CrossRefPubMed
29.
Zurück zum Zitat Liu, X., Hu, C., Bao, M., Li, J., Liu, X., & Tan, X., et al. (2016). Genome wide association study identifies L3MBTL4 as a novel susceptibility gene for hypertension. Scientific Reports, 6(1), 30811. Liu, X., Hu, C., Bao, M., Li, J., Liu, X., & Tan, X., et al. (2016). Genome wide association study identifies L3MBTL4 as a novel susceptibility gene for hypertension. Scientific Reports, 6(1), 30811.
Metadaten
Titel
miRNA Profiling of Exosomes from Spontaneous Hypertensive Rats Using Next-Generation Sequencing
verfasst von
Xiaoyan Liu
Wen Yuan
Lei Yang
Jing Li
Jun Cai
Publikationsdatum
20.03.2018
Verlag
Springer US
Erschienen in
Journal of Cardiovascular Translational Research / Ausgabe 1/2019
Print ISSN: 1937-5387
Elektronische ISSN: 1937-5395
DOI
https://doi.org/10.1007/s12265-017-9784-7

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