Top

Published in:

01-03-2022

Exosomes: Potential Player in Endothelial Dysfunction in Cardiovascular Disease

Authors: Farahnaz Nikdoust, Mahboubeh Pazoki, Mohammadjavad Mohammadtaghizadeh, Mahsa Karimzadeh Aghaali, Mehran Amrovani

Published in: Cardiovascular Toxicology | Issue 3/2022

Abstract

Exosomes are spherical bilayer membrane vesicles with an average diameter of 40–100 nm. These particles perform a wide range of biological activities due to their contents, including proteins, nucleic acids, lipids, lncRNA, and miRNA. Exosomes are involved in inflammation induction, oxidative stress and apoptosis, which can be effective in endothelial dysfunction. Due to the induction of mentioned processes in the endothelial cells, the intercellular connections are destroyed, cell permeability increases and finally cell efficiency decreases and functional defects occur. Cardiovascular disease (CVDs) are of consequences of endothelial dysfunction. Thus by identifying the exosome signaling pathways, which induce inflammation, oxidative stress, and apoptosis, endothelial dysfunction and subsequently CVDs can be reduced; exosomes can be used for appropriate target therapy.

Jokinen, E. (2014). Obesity and cardiovascular disease. Minerva Pediatrica, 67(1), 25–32.PubMed

Foley, R. N., Parfrey, P. S., & Sarnak, M. J. (1998). Epidemiology of cardiovascular disease in chronic renal disease. Journal of the American Society of Nephrology: JASN, 9(12 Suppl), S16-23.PubMed

Carter, A. M. (2012). Complement activation: An emerging player in the pathogenesis of cardiovascular disease. Scientifica. https://doi.org/10.6064/2012/402783CrossRefPubMedPubMedCentral

Farsad, B. F., Alavi, S. M., Ghorbanian, G., Fahimi, F., Ghaemmaghami, Z., Mehr, A. Z., & Bakhshandeh, H. (2019). The therapeutic efficnecy of ranolazine in comparison with conventional therapy in diabetic individuals with ischemic heart disease; a randomized clinical trial. Journal of Renal Injury Prevention, 9(1), e04–e04.

Rahimi, N. (2017). Defenders and challengers of endothelial barrier function. Frontiers in Immunology, 8, 1847.PubMedPubMedCentralCrossRef

Zhang, J., Tecson, K. M., & McCullough, P. A. (2020). Endothelial dysfunction contributes to COVID-19-associated vascular inflammation and coagulopathy. Reviews in Cardiovascular Medicine, 21(3), 315–319.PubMedCrossRef

Zhang, Y., Murugesan, P., Huang, K., & Cai, H. (2020). NADPH oxidases and oxidase crosstalk in cardiovascular diseases: Novel therapeutic targets. Nature Reviews Cardiology, 17(3), 170–194.PubMedCrossRef

Momtaz, H. E., Tanasan, A., & Godini, M. (2020). Evaluation of urinary NGAL level in children with congenital heart disease as a possible early indicator of nephropathy. Journal of Nephropharmacology, 10(2), e14–e14.CrossRef

Ooi, B. K., Chan, K.-G., Goh, B. H., & Yap, W. H. (2018). The role of natural products in targeting cardiovascular diseases via Nrf2 pathway: Novel molecular mechanisms and therapeutic approaches. Frontiers in Pharmacology, 9, 1308.PubMedPubMedCentralCrossRef

10.

Bhattacharjee, R., Khalyfa, A., Khalyfa, A. A., Mokhlesi, B., Kheirandish-Gozal, L., Almendros, I., et al. (2018). Exosomal cargo properties, endothelial function and treatment of obesity hypoventilation syndrome: A proof of concept study. Journal of Clinical Sleep Medicine, 14(5), 797–807.PubMedPubMedCentralCrossRef

11.

Haybar, H., Shahrabi, S., Rezaeeyan, H., Jodat, H., & Saki, N. (2019). Strategies to inhibit arsenic trioxide-induced cardiotoxicity in acute promyelocytic leukemia. Journal of Cellular Physiology, 234(9), 14500–14506.CrossRef

12.

Zhang, Y., Hu, Y.-W., Zheng, L., & Wang, Q. (2017). Characteristics and roles of exosomes in cardiovascular disease. DNA and Cell Biology, 36(3), 202–211.PubMedCrossRef

13.

Terrasini, N., & Lionetti, V. (2017). Exosomes in critical illness. Critical Care Medicine, 45(6), 1054–1060.PubMedCrossRef

14.

Zadeh, F. J., Akbari, T., Samimi, A., Davari, N., & Rezaeeyan, H. (2020). The role of molecular mechanism of Ten-Eleven Translocation2 (TET2) family proteins in pathogenesis of cardiovascular diseases (CVDs). Molecular Biology Reports, 47(7), 5503–5509.PubMedCrossRef

15.

Zadeh, F. J., Ghasemi, Y., Bagheri, S., Maleknia, M., Davari, N., & Rezaeeyan, H. (2020). Do exosomes play role in cardiovascular disease development in hematological malignancy? Molecular Biology Reports. https://doi.org/10.1007/s11033-020-05453-zCrossRefPubMed

16.

Zhang, J., Li, S., Li, L., Li, M., Guo, C., Yao, J., & Mi, S. (2015). Exosome and exosomal microRNA: Trafficking, sorting, and function. Genomics, Proteomics & Bioinformatics, 13(1), 17–24.CrossRef

17.

Zhang, C., Ji, Q., Yang, Y., Li, Q., & Wang, Z. (2018). Exosome: Function and role in cancer metastasis and drug resistance. Technology in Cancer Research & Treatment, 17, 1533033818763450.CrossRef

18.

Asgarpour, K., Shojaei, Z., Amiri, F., Ai, J., Mahjoubin-Tehran, M., Ghasemi, F., et al. (2020). Exosomal microRNAs derived from mesenchymal stem cells: Cell-to-cell messages. Cell Communication and Signaling, 18(1), 1–16.CrossRef

19.

Hessvik, N. P., & Llorente, A. (2018). Current knowledge on exosome biogenesis and release. Cellular and Molecular Life Sciences, 75(2), 193–208.PubMedCrossRef

20.

Zhang, H., Wang, L., Li, C., Yu, Y., Yi, Y., Wang, J., & Chen, D. (2019). Exosome-induced regulation in inflammatory bowel disease. Frontiers in Immunology, 10, 1464.PubMedPubMedCentralCrossRef

21.

Ostrowski, M., Carmo, N. B., Krumeich, S., Fanget, I., Raposo, G., Savina, A., et al. (2010). Rab27a and Rab27b control different steps of the exosome secretion pathway. Nature Cell Biology, 12(1), 19–30.PubMedCrossRef

22.

Van Niel, G., d’Angelo, G., & Raposo, G. (2018). Shedding light on the cell biology of extracellular vesicles. Nature Reviews Molecular Cell Biology, 19(4), 213–228.PubMedCrossRef

23.

Seo, N., Akiyoshi, K., & Shiku, H. (2018). Exosome-mediated regulation of tumor immunology. Cancer Science, 109(10), 2998–3004.PubMedPubMedCentralCrossRef

24.

Bobrie, A., Colombo, M., Raposo, G., & Théry, C. (2011). Exosome secretion: Molecular mechanisms and roles in immune responses. Traffic, 12(12), 1659–1668.PubMedCrossRef

25.

Zhu, L., Sun, H.-T., Wang, S., Huang, S.-L., Zheng, Y., Wang, C.-Q., et al. (2020). Isolation and characterization of exosomes for cancer research. Journal of Hematology & Oncology, 13(1), 1–24.CrossRef

26.

Mosquera-Heredia, M. I., Morales, L. C., Vidal, O. M., Barceló, E., Silvera-Redondo, C., Vélez, J. I., & Garavito-Galofre, P. (2021). Exosomes: Potential disease biomarkers and new therapeutic targets. Biomedicines, 9(8), 1061.PubMedPubMedCentralCrossRef

27.

Li, P., Kaslan, M., Lee, S. H., Yao, J., & Gao, Z. (2017). Progress in exosome isolation techniques. Theranostics, 7(3), 789.PubMedPubMedCentralCrossRef

28.

Jiang, K., Dong, C., Yin, Z., Li, R., Mao, J., Wang, C., et al. (2020). Exosome-derived ENO1 regulates integrin α6β4 expression and promotes hepatocellular carcinoma growth and metastasis. Cell Death & Disease, 11(11), 1–20.CrossRef

29.

Zamani, P., Fereydouni, N., Butler, A. E., Navashenaq, J. G., & Sahebkar, A. (2019). The therapeutic and diagnostic role of exosomes in cardiovascular diseases. Trends in Cardiovascular Medicine, 29(6), 313–323.PubMedCrossRef

30.

Liang, B., He, X., Zhao, Y.-X., Zhang, X.-X., & Gu, N. (2020). Advances in exosomes derived from different cell sources and cardiovascular diseases. BioMed Research International. https://doi.org/10.1155/2020/7298687CrossRefPubMedPubMedCentral

31.

Yuan, Y., Du, W., Liu, J., Ma, W., Zhang, L., Du, Z., & Cai, B. (2018). Stem cell-derived exosome in cardiovascular diseases: Macro roles of micro particles. Frontiers in Pharmacology, 9, 547.PubMedPubMedCentralCrossRef

32.

Jiang, K., Yang, J., Guo, S., Zhao, G., Wu, H., & Deng, G. (2019). Peripheral circulating exosome-mediated delivery of miR-155 as a novel mechanism for acute lung inflammation. Molecular Therapy, 27(10), 1758–1771.PubMedPubMedCentralCrossRef

33.

Roohaninasab, M., Goodarzi, A., Ghassemi, M., Sadeghzadeh-Bazargan, A., Behrangi, E., & Najar Nobari, N. (2021). Systematic review of platelet-rich plasma in treating alopecia: Focusing on efficacy, safety, and therapeutic durability. Dermatologic Therapy, 34(2), e14768.PubMedCrossRef

34.

Zheng, B., Yin, W.-N., Suzuki, T., Zhang, X.-H., Zhang, Y., Song, L.-L., et al. (2017). Exosome-mediated miR-155 transfer from smooth muscle cells to endothelial cells induces endothelial injury and promotes atherosclerosis. Molecular Therapy, 25(6), 1279–1294.PubMedPubMedCentralCrossRef

35.

Kuo, Y.-C., Li, Y.-S.J., Zhou, J., Shih, Y.-R.V., Miller, M., Broide, D., et al. (2013). Human mesenchymal stem cells suppress the stretch–induced inflammatory miR-155 and cytokines in bronchial epithelial cells. PLoS ONE, 8(8), e71342.PubMedPubMedCentralCrossRef

36.

Wu, X., Li, Q., Feng, Y., & Ji, Q. (2018). Antitumor research of the active ingredients from traditional Chinese medical plant Polygonum cuspidatum. Evidence-Based Complementary and Alternative Medicine. https://doi.org/10.1155/2018/2313021CrossRefPubMedPubMedCentral

37.

Sun, H.-J., Wu, Z.-Y., Nie, X.-W., & Bian, J.-S. (2020). Role of endothelial dysfunction in cardiovascular diseases: The link between inflammation and hydrogen sulfide. Frontiers in Pharmacology, 10, 1568.PubMedPubMedCentralCrossRef

38.

Chung, H.-T., Choi, B.-M., Kwon, Y.-G., & Kim, Y.-M. (2008). Interactive relations between nitric oxide (NO) and carbon monoxide (CO): Heme oxygenase-1/CO pathway is a key modulator in NO-mediated antiapoptosis and anti-inflammation. Methods in Enzymology, 441, 329–338.PubMedCrossRef

39.

Khademi, M., Roohaninasab, M., Goodarzi, A., Seirafianpour, F., Dodangeh, M., & Khademi, A. (2021). The healing effects of facial BOTOX injection on symptoms of depression alongside its effects on beauty preservation. Journal of Cosmetic Dermatology, 20(5), 1411–1415.PubMedCrossRef

40.

Kong, L., Shen, X., Lin, L., Leitges, M., Rosario, R., Zou, Y. S., & Yan, S. F. (2013). PKCβ promotes vascular inflammation and acceleration of atherosclerosis in diabetic ApoE null mice. Arteriosclerosis, Thrombosis, and Vascular Biology, 33(8), 1779–1787.PubMedCrossRef

41.

Rahman, A., & Fazal, F. (2009). Hug tightly and say goodbye: Role of endothelial ICAM-1 in leukocyte transmigration. Antioxidants & Redox Signaling, 11(4), 823–839.CrossRef

42.

Harrell, C. R., Djonov, V., & Volarevic, V. (2021). The cross-talk between mesenchymal stem cells and immune cells in tissue repair and regeneration. International Journal of Molecular Sciences, 22(5), 2472.PubMedPubMedCentralCrossRef

43.

Mostofa, A., Punganuru, S. R., Madala, H. R., Al-Obaide, M., & Srivenugopal, K. S. (2017). The process and regulatory components of inflammation in brain oncogenesis. Biomolecules, 7(2), 34.PubMedCentralCrossRef

44.

Roohaninasab, M., Sadeghzadeh-Bazargan, A., & Goodarzi, A. (2021). Effects of laser therapy on periorbital hyperpigmentation: A systematic review on current studies. Lasers in Medical Science. https://doi.org/10.1007/s10103-020-03241-6CrossRefPubMed

45.

Melnikov, I., Kozlov, S., Saburova, O., Zubkova, E., Guseva, O., Domogatsky, S., et al. (2020). CRP is transported by monocytes and monocyte-derived exosomes in the blood of patients with coronary artery disease. Biomedicines, 8(10), 435.PubMedCentralCrossRef

46.

Cheng, C.-F., & Lian, W.-S. (2013). Prooxidant mechanisms in iron overload cardiomyopathy. BioMed Research International. https://doi.org/10.1155/2013/740573CrossRefPubMedPubMedCentral

47.

Dalvi, P., Sun, B., Tang, N., & Pulliam, L. (2017). Immune activated monocyte exosomes alter microRNAs in brain endothelial cells and initiate an inflammatory response through the TLR4/MyD88 pathway. Scientific Reports, 7(1), 1–12.CrossRef

48.

Egaña-Gorroño, L., López-Díez, R., Yepuri, G., Ramirez, L. S., Reverdatto, S., Gugger, P. F., et al. (2020). Receptor for advanced glycation end products (RAGE) and mechanisms and therapeutic opportunities in diabetes and cardiovascular disease: Insights from human subjects and animal models. Frontiers in Cardiovascular Medicine, 7, 37.PubMedPubMedCentralCrossRef

49.

Xie, Q.-B., Liang, Y., Yang, M., Yang, Y., Cen, X.-M., & Yin, G. (2017). DEPTOR-mTOR signaling is critical for lipid metabolism and inflammation homeostasis of lymphocytes in human PBMC culture. Journal of Immunology Research. https://doi.org/10.1155/2017/5252840CrossRefPubMedPubMedCentral

50.

Liu, L., Wang, W., Zhao, Z., Hu, C., Tao, L., & Zhang, X. (2019). Pholidonone, an active stilbene derivative from Pholidota cantonensis, exhibits pro-apoptotic effect via induction of endoplasmic reticulum stress in human gastric cancer. Food & Nutrition Research. https://doi.org/10.29219/fnr.v63.3553CrossRefPubMed

51.

Liu, Y., Tong, C., Xu, Y., Cong, P., Liu, Y., Shi, L., et al. (2019). CD28 deficiency ameliorates blast exposure-induced lung inflammation, oxidative stress, apoptosis, and T cell accumulation in the lungs via the PI3K/Akt/FoxO1 signaling pathway. Oxidative Medicine and Cellular Longevity. https://doi.org/10.1155/2019/4848560CrossRefPubMedPubMedCentral

52.

Dohare, P., Cheng, B., Ahmed, E., Yadala, V., Singla, P., Thomas, S., et al. (2018). Glycogen synthase kinase-3β inhibition enhances myelination in preterm newborns with intraventricular hemorrhage, but not recombinant Wnt3A. Neurobiology of Disease, 118, 22–39.PubMedPubMedCentralCrossRef

53.

Li, Y., Zhao, Y., Tan, X., Liu, J., Zhi, Y., Yi, L., et al. (2020). Isoorientin inhibits inflammation in macrophages and endotoxemia mice by regulating glycogen synthase kinase 3β. Mediators of Inflammation. https://doi.org/10.1155/2020/8704146CrossRefPubMedPubMedCentral

54.

Hong, H.-Y., Jeon, W.-K., & Kim, B.-C. (2008). Up-regulation of heme oxygenase-1 expression through the Rac1/NADPH oxidase/ROS/p38 signaling cascade mediates the anti-inflammatory effect of 15-deoxy-Δ12, 14-prostaglandin J2 in murine macrophages. FEBS Letters, 582(6), 861–868.PubMedCrossRef

55.

Kafi, F., Bolourian, A., Mojtahedi, Z., & Pouramini, A. (2021). High mobility group box 1 (HMGB1) in COVID-19. Journal of Preventive Epidemiology, 6(1), e11.CrossRef

56.

Wei, F., Liu, S. Y., Luo, L., Gu, N. N., Zeng, Y., Chen, X. Y., et al. (2017). Anti-inflammatory mechanism of ulinastatin: Inhibiting the hyperpermeability of vascular endothelial cells induced by TNF-α via the RhoA/ROCK signal pathway. International Immunopharmacology, 46, 220–227.PubMedCrossRef

57.

Wang, C. C. L., Hess, C. N., Hiatt, W. R., & Goldfine, A. B. (2016). Atherosclerotic cardiovascular disease and heart failure in type 2 diabetes–mechanisms, management, and clinical considerations. Circulation, 133(24), 2459.CrossRef

58.

Wang, X., Sun, Y., Yang, H., Lu, Y., & Li, L. (2016). Oxidized low-density lipoprotein induces apoptosis in cultured neonatal rat cardiomyocytes by modulating the TLR4/NF-κB pathway. Scientific Reports, 6(1), 1–8.

59.

Kim, S., Lee, K.-S., Choi, S., Kim, J., Lee, D.-K., Park, M., et al. (2018). NF-κB–responsive miRNA-31-5p elicits endothelial dysfunction associated with preeclampsia via down-regulation of endothelial nitric-oxide synthase. Journal of Biological Chemistry, 293(49), 18989–19000.PubMedPubMedCentralCrossRef

60.

Ko, K.-W., Yoo, Y.-I., Kim, J. Y., Choi, B., Park, S.-B., Park, W., et al. (2020). Attenuation of tumor necrosis factor-α induced inflammation by umbilical cord-mesenchymal stem cell derived exosome-mimetic nanovesicles in endothelial cells. Tissue Engineering and Regenerative Medicine, 17(2), 155–163.PubMedPubMedCentralCrossRef

61.

Song, Y., Li, H., Ren, X., Li, H., & Feng, C. (2020). SNHG9, delivered by adipocyte-derived exosomes, alleviates inflammation and apoptosis of endothelial cells through suppressing TRADD expression. European Journal of Pharmacology, 872, 172977.PubMedCrossRef

62.

Gano, L. B., Donato, A. J., Pasha, H. M., Hearon, C. M., Jr., Sindler, A. L., & Seals, D. R. (2014). The SIRT1 activator SRT1720 reverses vascular endothelial dysfunction, excessive superoxide production, and inflammation with aging in mice. American Journal of Physiology-Heart and Circulatory Physiology, 307(12), H1754–H1763.PubMedPubMedCentralCrossRef

63.

Ailawadi, S., Wang, X., Gu, H., & Fan, G.-C. (2015). Pathologic function and therapeutic potential of exosomes in cardiovascular disease. Biochimica et Biophysica Acta (BBA)-Molecular Basis of Disease, 1852(1), 1–11.CrossRef

64.

Ping, Z., Peng, Y., Lang, H., Xinyong, C., Zhiyi, Z., Xiaocheng, W., et al. (2020). Oxidative stress in radiation-induced cardiotoxicity. Oxidative Medicine and Cellular Longevity. https://doi.org/10.1155/2020/3579143CrossRefPubMedPubMedCentral

65.

Lü, J.-M., Jiang, J., Jamaluddin, M. S., Liang, Z., Yao, Q., & Chen, C. (2019). Ginsenoside Rb1 blocks ritonavir-induced oxidative stress and eNOS downregulation through activation of estrogen receptor-beta and upregulation of SOD in human endothelial cells. International Journal of Molecular Sciences, 20(2), 294.PubMedCentralCrossRef

66.

Wilkerson, B. A., & Argraves, K. M. (2014). The role of sphingosine-1-phosphate in endothelial barrier function. Biochimica et Biophysica Acta (BBA)-Molecular and Cell Biology of Lipids, 1841(10), 1403–1412.

67.

Gioscia-Ryan, R. A., LaRocca, T. J., Sindler, A. L., Zigler, M. C., Murphy, M. P., & Seals, D. R. (2014). Mitochondria-targeted antioxidant (MitoQ) ameliorates age-related arterial endothelial dysfunction in mice. The Journal of Physiology, 592(12), 2549–2561.PubMedPubMedCentralCrossRef

68.

Lee, V. V., Muravlyova, L. E., Bakirova, R. Y., Kiziltunc, A., Turkhanova, Z. Z., & Ashirbekova, B. D. (2021). Molecular patterns of oxidative stress in drug-induced nephropathy. Journal of Nephropathology, 10(3).

69.

Gurunathan, S., Kang, M.-H., Jeyaraj, M., & Kim, J.-H. (2021). Platinum nanoparticles enhance exosome release in human lung epithelial adenocarcinoma cancer cells (A549): Oxidative stress and the ceramide pathway are key players. International Journal of Nanomedicine, 16, 515.PubMedPubMedCentralCrossRef

70.

Matheus, A. S. D. M., Tannus, L. R. M., Cobas, R. A., Palma, C. C. S., Negrato, C. A., & Gomes, M. D. B. (2013). Impact of diabetes on cardiovascular disease: An update. International Journal of Hypertension, 1, 1. https://doi.org/10.1155/2013/653789CrossRef

71.

Parsaee, M., Akiash, N., Azarkeivan, A., Alizadeh Sani, Z., Amin, A., Pazoki, M., et al. (2018). The correlation between cardiac magnetic resonance T2* and left ventricular global longitudinal strain in people with β-thalassemia. Echocardiography, 35(4), 438–444.PubMedCrossRef

72.

Amiri, M. (2018). Oxidative stress and free radicals in liver and kidney diseases; an updated short-review. Journal of Nephropathology, 7(3).

73.

Kanikarla-Marie, P., & Jain, S. K. (2016). 1, 25 (OH) 2D3 inhibits oxidative stress and monocyte adhesion by mediating the upregulation of GCLC and GSH in endothelial cells treated with acetoacetate (ketosis). The Journal of Steroid Biochemistry and Molecular Biology, 159, 94–101.PubMedPubMedCentralCrossRef

74.

Touyz, R. M., Anagnostopoulou, A., Camargo, L. L., Rios, F. J., & Montezano, A. C. (2019). Vascular biology of superoxide-generating NADPH oxidase 5—implications in hypertension and cardiovascular disease. Antioxidants & Redox Signaling, 30(7), 1027–1040.CrossRef

75.

Sabbatino, F., Conti, V., Liguori, L., Polcaro, G., Corbi, G., Manzo, V., et al. (2021). Molecules and mechanisms to overcome oxidative stress inducing cardiovascular disease in cancer patients. Life, 11(2), 105.PubMedPubMedCentralCrossRef

76.

Jiao, Y., Li, W., Wang, W., Tong, X., Xia, R., Fan, J., et al. (2020). Platelet-derived exosomes promote neutrophil extracellular trap formation during septic shock. Critical Care, 24(1), 1–18.CrossRef

77.

Pei, H., Zhang, J., Nie, J., Ding, N., Hu, W., Hua, J., et al. (2017). RAC2-P38 MAPK-dependent NADPH oxidase activity is associated with the resistance of quiescent cells to ionizing radiation. Cell Cycle, 16(1), 113–122.PubMedCrossRef

78.

Boytard, L., Hadi, T., Silvestro, M., Qu, H., Kumpfbeck, A., Sleiman, R., et al. (2020). Lung-derived HMGB1 is detrimental for vascular remodeling of metabolically imbalanced arterial macrophages. Nature Communications, 11(1), 1–17.CrossRef

79.

Lang, A., Grether-Beck, S., Singh, M., Kuck, F., Jakob, S., Kefalas, A., et al. (2016). MicroRNA-15b regulates mitochondrial ROS production and the senescence-associated secretory phenotype through sirtuin 4/SIRT4. Aging (Albany NY), 8(3), 484.CrossRef

80.

Luo, G., Jian, Z., Zhu, Y., Zhu, Y., Chen, B., Ma, R., et al. (2019). Sirt1 promotes autophagy and inhibits apoptosis to protect cardiomyocytes from hypoxic stress. International Journal of Molecular Medicine, 43(5), 2033–2043.PubMedPubMedCentral

81.

Jin, Y., Guan, Z., Wang, X., Wang, Z., Zeng, R., Xu, L., & Cao, P. (2018). ALA-PDT promotes HPV-positive cervical cancer cells apoptosis and DCs maturation via miR-34a regulated HMGB1 exosomes secretion. Photodiagnosis and Photodynamic Therapy, 24, 27–35.PubMedCrossRef

82.

Seif, F., Kheirollah, A., & Babaahmadi-Rezaei, H. (2020). Efficient isolation and identification of primary endothelial cells from bovine aorta by collagenase P. Immunopathologia Persa, 6(2), e15–e15.CrossRef

83.

Zheng, P., Tang, Z., Xiong, J., Wang, B., Xu, J., Chen, L., et al. (2021). RAGE: A potential therapeutic target during FGF1 treatment of diabetes-mediated liver injury. Journal of Cellular and Molecular Medicine, 25(10), 4776–4785.PubMedPubMedCentralCrossRef

84.

Chen, J., Jing, J., Yu, S., Song, M., Tan, H., Cui, B., & Huang, L. (2016). Advanced glycation endproducts induce apoptosis of endothelial progenitor cells by activating receptor RAGE and NADPH oxidase/JNK signaling axis. American Journal of Translational Research, 8(5), 2169.PubMedPubMedCentral

85.

Chen, L., Wang, J., Wang, B., Yang, J., Gong, Z., Zhao, X., et al. (2016). MiR-126 inhibits vascular endothelial cell apoptosis through targeting PI3K/Akt signaling. Annals of Hematology, 95(3), 365–374.PubMedCrossRef

86.

Yang, S., Wu, M., Li, X., Zhao, R., Zhao, Y., Liu, L., & Wang, S. (2020). Role of endoplasmic reticulum stress in atherosclerosis and its potential as a therapeutic target. Oxidative Medicine and Cellular Longevity. https://doi.org/10.1155/2020/9270107CrossRefPubMedPubMedCentral

87.

Parodi-Rullán, R., Sone, J. Y., & Fossati, S. (2019). Endothelial mitochondrial dysfunction in cerebral amyloid angiopathy and Alzheimer’s disease. Journal of Alzheimer’s Disease, 72(4), 1019–1039.PubMedCrossRef

88.

Jayaraman, T., Paget, A., Shin, Y. S., Li, X., Mayer, J., Chaudhry, H. W., et al. (2008). TNF-α-mediated inflammation in cerebral aneurysms: A potential link to growth and rupture. Vascular Health and Risk Management, 4(4), 805.PubMedPubMedCentralCrossRef

89.

Hajsadeghi, S., Mirshafiee, S., Pazoki, M., Moradians, V., Mansouri, P., Kianmehr, N., & Iranpour, A. (2020). The relationship between global longitudinal strain and pulmonary function tests in patients with scleroderma and normal ejection fraction and pulmonary artery pressure: A case–control study. The International Journal of Cardiovascular Imaging. https://doi.org/10.1007/s10554-020-01788-7.pdfCrossRefPubMed

90.

Zhang, H., Dellsperger, K. C., & Zhang, C. (2012). The link between metabolic abnormalities and endothelial dysfunction in type 2 diabetes: An update. Basic Research in Cardiology, 107(1), 1–11.CrossRef

91.

Zuniga, F. A., Ormazabal, V., Gutierrez, N., Aguilera, V., Radojkovic, C., Veas, C., et al. (2014). Role of lectin-like oxidized low density lipoprotein-1 in fetoplacental vascular dysfunction in preeclampsia. BioMed Research International. https://doi.org/10.1155/2014/353616CrossRefPubMedPubMedCentral

92.

Frey, R. S., Ushio-Fukai, M., & Malik, A. B. (2009). NADPH oxidase-dependent signaling in endothelial cells: Role in physiology and pathophysiology. Antioxidants & redox signaling, 11(4), 791–810.CrossRef

93.

Colombo, E., Signore, A., Aicardi, S., Zekiy, A., Utyuzh, A., Benedicenti, S., & Amaroli, A. (2021). Experimental and clinical applications of red and near-infrared photobiomodulation on endothelial dysfunction: A review. Biomedicines, 9(3), 274.PubMedPubMedCentralCrossRef

94.

Veluthakal, R., Kumar, B., Mohammad, G., Kowluru, A., & Kowluru, R. A. (2015). Tiam1-Rac1 axis promotes activation of p38 MAP kinase in the development of diabetic retinopathy: Evidence for a requisite role for protein palmitoylation. Cellular Physiology and Biochemistry, 36(1), 208–220.PubMedCrossRef

95.

Liu, Y., Song, J.-W., Lin, J.-Y., Miao, R., & Zhong, J.-C. (2020). Roles of microRNA-122 in cardiovascular fibrosis and related diseases. Cardiovascular Toxicology, 20(5), 463–473.PubMedPubMedCentralCrossRef

96.

Geng, T., Song, Z.-Y., Xing, J.-X., Wang, B.-X., Dai, S.-P., & Xu, Z.-S. (2020). Exosome derived from coronary serum of patients with myocardial infarction promotes angiogenesis through the miRNA-143/IGF-IR pathway. International Journal of Nanomedicine, 15, 2647.PubMedPubMedCentralCrossRef

97.

Samiei, N., Akiash, N., Naeini, S. D., Nikpajouh, A., & Pazoki, M. (2020). The presence of patent foramen ovale in the superior type of sinus venosus atrial septal defect. The Journal of Tehran University Heart Center, 15(3), 98.PubMedPubMedCentral

98.

Ling, H., Guo, Z., Shi, Y., Zhang, L., & Song, C. (2020). Serum exosomal MicroRNA-21, MicroRNA-126, and PTEN are novel biomarkers for diagnosis of acute coronary syndrome. Frontiers in Physiology, 11, 654.PubMedPubMedCentralCrossRef

99.

Bang, C., Batkai, S., Dangwal, S., Gupta, S. K., Foinquinos, A., Holzmann, A., et al. (2014). Cardiac fibroblast–derived microRNA passenger strand-enriched exosomes mediate cardiomyocyte hypertrophy. The Journal of clinical investigation, 124(5), 2136–2146.PubMedPubMedCentralCrossRef

100.

Sun, W., Zhao, L., Song, X., Zhang, J., Xing, Y., Liu, N., et al. (2017). MicroRNA-210 modulates the cellular energy metabolism shift during H2O2-induced oxidative stress by repressing ISCU in H9c2 cardiomyocytes. Cellular Physiology and Biochemistry, 43(1), 383–394.PubMedCrossRef

101.

Wang, L., Jia, Q., Xinnong, C., Xie, Y., Yang, Y., Zhang, A., et al. (2019). Role of cardiac progenitor cell-derived exosome-mediated microRNA-210 in cardiovascular disease. Journal of Cellular and Molecular Medicine, 23(11), 7124–7131.PubMedPubMedCentralCrossRef

102.

Yang, Y., Li, Y., Chen, X., Cheng, X., Liao, Y., & Yu, X. (2016). Exosomal transfer of miR-30a between cardiomyocytes regulates autophagy after hypoxia. Journal of Molecular Medicine, 94(6), 711–724.PubMedCrossRef

103.

Aoyagi, T., & Matsui, T. (2011). Phosphoinositide-3 kinase signaling in cardiac hypertrophy and heart failure. Current Pharmaceutical Design, 17(18), 1818–1824.PubMedPubMedCentralCrossRef

104.

Ranek, M. J., Stachowski, M. J., Kirk, J. A., & Willis, M. S. (2018). The role of heat shock proteins and co-chaperones in heart failure. Philosophical Transactions of the Royal Society B: Biological Sciences, 373(1738), 20160530.CrossRef

105.

Zhang, Y., Jiang, D. S., Yan, L., Cheng, K. J., Bian, Z. Y., & Lin, G. S. (2011). HSP75 protects against cardiac hypertrophy and fibrosis. Journal of Cellular Biochemistry, 112(7), 1787–1794.PubMedCrossRef

106.

Kang, K., Ma, R., Cai, W., Huang, W., Paul, C., Liang, J., et al. (2015). Exosomes secreted from CXCR4 overexpressing mesenchymal stem cells promote cardioprotection via Akt signaling pathway following myocardial infarction. Stem Cells International. https://doi.org/10.1155/2015/659890CrossRefPubMedPubMedCentral

107.

Barile, L., Cervio, E., Lionetti, V., Milano, G., Ciullo, A., Biemmi, V., et al. (2018). Cardioprotection by cardiac progenitor cell-secreted exosomes: Role of pregnancy-associated plasma protein-A. Cardiovascular research, 114(7), 992–1005.PubMedCrossRef

108.

Guo, D., Xu, Y., Ding, J., Dong, J., Jia, N., Li, Y., & Zhang, M. (2020). Roles and clinical applications of exosomes in cardiovascular disease. BioMed Research International. https://doi.org/10.1155/2020/5424281CrossRefPubMedPubMedCentral

109.

Hu, J., Wang, S., Xiong, Z., Cheng, Z., Yang, Z., Lin, J., et al. (2018). Exosomal Mst1 transfer from cardiac microvascular endothelial cells to cardiomyocytes deteriorates diabetic cardiomyopathy. Biochimica et Biophysica Acta (BBA)-Molecular Basis of Disease, 1864(11), 3639–3649.CrossRef

110.

Hervera, A., De Virgiliis, F., Palmisano, I., Zhou, L., Tantardini, E., Kong, G., et al. (2018). Reactive oxygen species regulate axonal regeneration through the release of exosomal NADPH oxidase 2 complexes into injured axons. Nature Cell Biology, 20(3), 307–319.PubMedCrossRef

111.

Yang, T.-C., Chen, Y.-J., Chang, S.-F., Chen, C.-H., Chang, P.-Y., & Lu, S.-C. (2014). Malondialdehyde mediates oxidized LDL-induced coronary toxicity through the Akt-FGF2 pathway via DNA methylation. Journal of Biomedical Science, 21(1), 1–12.CrossRef

112.

Yao, Y., Wang, Y., Zhang, Y., & Liu, C. (2017). Klotho ameliorates oxidized low density lipoprotein (ox-LDL)-induced oxidative stress via regulating LOX-1 and PI3K/Akt/eNOS pathways. Lipids in Health and Disease, 16(1), 1–10.CrossRef

113.

Shang, X., Lin, K., Yu, R., Zhu, P., Zhang, Y., Wang, L., et al. (2019). Resveratrol protects the myocardium in sepsis by activating the phosphatidylinositol 3-kinases (PI3K)/AKT/mammalian target of rapamycin (mTOR) pathway and inhibiting the nuclear factor-κB (NF-κB) signaling pathway. Medical Science Monitor: International Medical Journal of Experimental and Clinical Research, 25, 9290.CrossRef

114.

Yan, Y., Song, D., Song, X., & Song, C. (2020). The role of lncRNA MALAT1 in cardiovascular disease. IUBMB Life, 72(3), 334–342.PubMedCrossRef

115.

Mao, Q., Liang, X.-L., Zhang, C.-L., Pang, Y.-H., & Lu, Y.-X. (2019). LncRNA KLF3-AS1 in human mesenchymal stem cell-derived exosomes ameliorates pyroptosis of cardiomyocytes and myocardial infarction through miR-138-5p/Sirt1 axis. Stem Cell Research & Therapy, 10(1), 1–14.CrossRef

116.

Arslan, F., Lai, R. C., Smeets, M. B., Akeroyd, L., Choo, A., Aguor, E. N., et al. (2013). Mesenchymal stem cell-derived exosomes increase ATP levels, decrease oxidative stress and activate PI3K/Akt pathway to enhance myocardial viability and prevent adverse remodeling after myocardial ischemia/reperfusion injury. Stem Cell Research, 10(3), 301–312.PubMedCrossRef

117.

Wang, Y., Zhang, L., Li, Y., Chen, L., Wang, X., Guo, W., et al. (2015). Exosomes/microvesicles from induced pluripotent stem cells deliver cardioprotective miRNAs and prevent cardiomyocyte apoptosis in the ischemic myocardium. International Journal of Cardiology, 192, 61–69.PubMedCrossRef

118.

Barile, L., Lionetti, V., Cervio, E., Matteucci, M., Gherghiceanu, M., Popescu, L. M., et al. (2014). Extracellular vesicles from human cardiac progenitor cells inhibit cardiomyocyte apoptosis and improve cardiac function after myocardial infarction. Cardiovascular Research, 103(4), 530–541.PubMedCrossRef

119.

Ibrahim, A.G.-E., Cheng, K., & Marbán, E. (2014). Exosomes as critical agents of cardiac regeneration triggered by cell therapy. Stem Cell Reports, 2(5), 606–619.PubMedPubMedCentralCrossRef

120.

Vicencio, J. M., Yellon, D. M., Sivaraman, V., Das, D., Boi-Doku, C., Arjun, S., et al. (2015). Plasma exosomes protect the myocardium from ischemia-reperfusion injury. Journal of the American College of Cardiology, 65(15), 1525–1536.PubMedCrossRef

121.

Zheng, L., Li, Z., Ling, W., Zhu, D., Feng, Z., & Kong, L. (2018). Exosomes derived from dendritic cells attenuate liver injury by modulating the balance of Treg and Th17 cells after ischemia reperfusion. Cellular Physiology and Biochemistry, 46(2), 740–756.PubMedCrossRef

Title: Exosomes: Potential Player in Endothelial Dysfunction in Cardiovascular Disease
Authors: Farahnaz Nikdoust
Mahboubeh Pazoki
Mohammadjavad Mohammadtaghizadeh
Mahsa Karimzadeh Aghaali
Mehran Amrovani
Publication date: 01-03-2022
Publisher: Springer US
Published in: Cardiovascular Toxicology / Issue 3/2022
Print ISSN: 1530-7905
Electronic ISSN: 1559-0259
DOI: https://doi.org/10.1007/s12012-021-09700-y

ACC 2024 Congress Coverage

Heart Failure Video

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Exosomes: Potential Player in Endothelial Dysfunction in Cardiovascular Disease

Abstract

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 3/2022

Alcohol Consumption: A New Risk Factor for Arterial Stiffness?

Oxygen Delivery Approaches to Augment Cell Survival After Myocardial Infarction: Progress and Challenges

Potential Cardiotoxic Effects of Remdesivir on Cardiovascular System: A Literature Review

Cardiac Complications: The Understudied Aspect of Cancer Cachexia

Long Non-coding RNAs: Potential Players in Cardiotoxicity Induced by Chemotherapy Drugs

Unraveling the Differentially Articulated Axes of the Century-Old Renin–Angiotensin–Aldosterone System: Potential Therapeutic Implications

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page