Heat Shock Improves Sca-1+ Stem Cell Survival and Directs Ischemic Cardiomyocytes Toward a Prosurvival Phenotype Via Exosomal Transfer: A Critical Role for HSF1/miR-34a/HSP70 Pathway
Open accessAbstract
Stem cell-based therapy is a promising intervention for ischemic heart diseases. However, the functional integrity of stem cells is impaired in an ischemic environment. Here, we report a novel finding that heat shock significantly improves Sca-1+stem cell survival in an ischemic environment by the regulation of the triangle: heat shock factor 1 (HSF1), HSF1/miR-34a, and heat shock protein 70 (HSP70). Initially we prove that HSP70 is the key chaperone-mediating cytoprotective effect of heat shock in Sca-1+cells and then we establish miR-34a as a direct repressor of HSP70. We found that HSP70 was downregulated in heat shocked Sca-1+ stem cells (HSSca-1+ cells). Intriguingly, we demonstrate that the downregulation of miR-34a is attributed to HSF1-mediated epigenetic repression through histone H3 Lys27 trimethylation (H3K27me3) on miR-34a promoter. Moreover, we show that heat shock induces exosomal transfer of HSF1 from Sca-1+ cells, which directs ischemic cardiomyocytes toward a prosurvival phenotype by epigenetic repression of miR-34a. In addition, our in vivo study demonstrates that transplantation of HSSca-1+ cells significantly reduces apoptosis, attenuates fibrosis, and improves global heart functions in ischemic myocardium. Hence, our study provides not only novel insights into the effects of heat shock on stem cell survival and paracrine behavior but also may have therapeutic values for stem cell therapy in ischemic heart diseases. Stem Cells 2014;32:462–472
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Overexpression of heat shock protein 70 protects against age- and disease-related tissue degeneration in brain, heart, and skeletal muscle.
“Overexpression of heat shock protein 70 (HSP70), a chaperone protein that recognizes damaged proteins in CMA, also protects against age- and disease-related tissue degeneration in brain, heart and skeletal muscle90–92.”
From Stem cell aging: mechanisms, regulators and therapeutic opportunities (2014) · cites this paper as [91]
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Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET
Peinado, H., Alečković, M., Lavotshkin, S., Matei, I., Costa-Silva, B., Moreno-Bueno, G., Hergueta-Redondo, M., Williams, C., García-Santos, G., Ghajar, C. M., et al. (2012) · Nature Medicine · doi:10.1038/nm.2753 · Cited by 3,715 · see citing works
Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis
Chang, T.-C., Wentzel, E. A., Kent, O. A., Ramachandran, K., Mullendore, M., Lee, K. H., Feldmann, G., Yamakuchi, M., Ferlito, M., Lowenstein, C. J., et al. (2007) · Molecular Cell · doi:10.1016/j.molcel.2007.05.010 · Cited by 2,010 · see citing works
Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells
Mittelbrunn, M., Gutiérrez‐Vázquez, C., Villarroya‐Beltri, C., González, S., Sánchez‐Cabo, F., González, M. A., Bernad, A., & Sánchez‐Madrid, F. (2011) · Nature Communications · doi:10.1038/ncomms1285 · Cited by 1,768 · see citing works
MicroRNAs in Stress Signaling and Human Disease
Mendell, J. T., & Olson, E. N. (2012) · Cell · doi:10.1016/j.cell.2012.02.005 · Cited by 1,673 · see citing works
Transcriptional Activation of miR-34a Contributes to p53-Mediated Apoptosis
Raver-Shapira, N., Marciano, E., Meiri, E., Spector, Y., Rosenfeld, N., Moskovits, N. B.-C., Bentwich, Z., & Oren, M. (2007) · Molecular Cell · doi:10.1016/j.molcel.2007.05.017 · Cited by 1,352 · see citing works
Atheroprotective communication between endothelial cells and smooth muscle cells through miRNAs
Hergenreider, E., Heydt, S., Tréguer, K., Boettger, T., Horrevoets, A. J. G., Zeiher, A. M., Scheffer, M. P., Frangakis, A. S., Yin, X., Mayr, M., et al. (2012) · Nature Cell Biology · doi:10.1038/ncb2441 · Cited by 1,300 · see citing works
Active Wnt proteins are secreted on exosomes
Gross, J. C., Chaudhary, V., Bartscherer, K., & Boutros, M. (2012) · Nature Cell Biology · doi:10.1038/ncb2574 · Cited by 1,025 · see citing works
Heat Shock Factor 1 Is a Powerful Multifaceted Modifier of Carcinogenesis
Dai, C., Whitesell, L. J., Rogers, A. B., & Lindquist, S. L. (2007) · Cell · doi:10.1016/j.cell.2007.07.020 · Cited by 827 · see citing works
MicroRNA-34a regulates cardiac ageing and function.
Boon, R. A., Iekushi, K., Lechner, S., Seeger, T., Fischer, A., Heydt, S., Kaluza, D., Tréguer, K., Carmona, G., Bonauer, A., et al. (2013) · Nature · doi:10.1038/nature11919 · Cited by 821 · see citing works
Inactivation of miR-34a by aberrant CpG methylation in multiple types of cancer
Lodygin, D., Tarasov, V., Epanchintsev, A., Berking, C., Knyazeva, T., Koerner, H., Knyazev, P. G., Diebold, J., & Hermeking, H. (2008) · Cell Cycle · doi:10.4161/cc.7.16.6533 · Cited by 784 · see citing works
Regulation of H SF 1 Function in the Heat Stress Response: Implications in Aging and Disease
Anckar, J., & Sistonen, L. (2011) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-060809-095203 · Cited by 779 · see citing works
Mendillo, M. L., Santagata, S., Koeva, M., Bell, G. W., Hu, R., Tamimi, R. M., Fraenkel, E., Ince, T. A., Whitesell, L. J., & Lindquist, S. L. (2012) · Cell · doi:10.1016/j.cell.2012.06.031 · Cited by 696 · see citing works
Exosome mimetics: a novel class of drug delivery systems
Schiffelers, R. M., Kooijmans, S. A. A., Vader, P., van Dommelen, & van Solinge, W. W. (2012) · International Journal of Nanomedicine · doi:10.2147/ijn.s29661 · Cited by 517 · see citing works
Kajstura, J., Rota, M., Whang, B., Cascapera, S., Hosoda, T., Bearzi, C., Nurzyńska, D., Kasahara, H., Zias, E. A., Bonafè, M., et al. (2004) · Circulation Research · doi:10.1161/01.res.0000151843.79801.60 · Cited by 479 · see citing works
miR-34 miRNAs provide a barrier for somatic cell reprogramming
Choi, Y. J., Lin, C., Ho, J. J., He, X., Okada, N., Bu, P., Zhong, Y., Kim, S. Y., Bennett, M. J., Chen, C., et al. (2011) · Nature Cell Biology · doi:10.1038/ncb2366 · Cited by 381 · see citing works
A microRNA miR-34a-Regulated Bimodal Switch Targets Notch in Colon Cancer Stem Cells
Bu, P., Chen, K., Chen, J. H., Wang, L., Walters, J. N., Shin, Y. J., Goerger, J. P., Sun, J. M., Witherspoon, M., Rakhilin, N., et al. (2013) · Cell stem cell · doi:10.1016/j.stem.2013.03.002 · Cited by 355 · see citing works
Epigenetic Inactivation of the miR-124-1 in Haematological Malignancies
Wong, K. Y., So, C. C., Loong, F., Chung, L.-P., Lam, W. W. L., Liang, R. H. S., Li, G. K. H., Jin, D., & Chim, C. S. (2011) · PLoS ONE · doi:10.1371/journal.pone.0019027 · Cited by 247 · see citing works
Towards regenerative therapy for cardiac disease
Ptaszek, L. M., Mansour, M., Ruskin, J. N., & Chien, K. R. (2012) · The Lancet · doi:10.1016/s0140-6736(12)60075-0 · Cited by 242 · see citing works
Heat shock protects cultured neurons from glutamate toxicity
Rordorf, G. A., Koroshetz, W. J., & Bonventre, J. V. (1991) · Neuron · doi:10.1016/0896-6273(91)90348-4 · Cited by 195 · see citing works
The protective role of heat stress in the ischaemic and reperfused rabbit myocardium
Yellon, D. M. (1992) · Journal of Molecular and Cellular Cardiology · doi:10.1016/0022-2828(92)91102-b · Cited by 175 · see citing works
Epigenetic inactivation of the miR-34a in hematological malignancies
Chim, C. S., Wong, K. Y., Qi, Y., Loong, F., Lam, W. L., Wong, L., Jin, D., Costello, J., & Liang, R. H. S. (2010) · Carcinogenesis · doi:10.1093/carcin/bgq033 · Cited by 157 · see citing works
Regulation of survival gene hsp70
Silver, J. T., & Noble, E. G. (2011) · Cell Stress and Chaperones · doi:10.1007/s12192-011-0290-6 · Cited by 149 · see citing works
Genetic Enhancement of Stem Cell Engraftment, Survival, and Efficacy
Penn, M. S., & Mangi, A. A. (2008) · Circulation Research · doi:10.1161/circresaha.108.175174 · Cited by 146 · see citing works
McGinley, L. M., McMahon, J. M., Strappe, P., Barry, F., Murphy, M. J., O’Toole, D. P., & O’Brien, T. (2011) · Stem Cell Research & Therapy · doi:10.1186/scrt53 · Cited by 106 · see citing works
Stem Cell Engraftment and Survival in the Ischemic Heart
Wu, K. H., Mo, X. M., Han, Z., & Zhou, B. (2011) · The Annals of Thoracic Surgery · doi:10.1016/j.athoracsur.2011.07.012 · Cited by 96 · see citing works
The cardiovascular exosome: Current perspectives and potential
Cosme, J., Liu, P. P., & Gramolini, A. O. (2013) · PROTEOMICS · doi:10.1002/pmic.201200441 · Cited by 49 · see citing works
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Exosome Theranostics: Biology and Translational Medicine
He, C., Zheng, S., Luo, Y., & Wang, B. (2017) · Theranostics · doi:10.7150/thno.21945 · Cited by 1,259 · see citing works
Stem cell aging: mechanisms, regulators and therapeutic opportunities
Oh, J., Lee, Y. D., & Wagers, A. J. (2014) · Nature Medicine · doi:10.1038/nm.3651 · Cited by 796 · see citing works
IL-6R/STAT3/miR-34a feedback loop promotes EMT-mediated colorectal cancer invasion and metastasis
Rokavec, M., Öner, M. G., Li, H., Jackstadt, R., Jiang, L., Lodygin, D., Kaller, M., Horst, D., Ziegler, P. K., Schwitalla, S., et al. (2014) · Journal of Clinical Investigation · doi:10.1172/jci73531 · Cited by 753 · see citing works
Exosomal cargo-loading and synthetic exosome-mimics as potential therapeutic tools
Li, S.-P., Lin, Z., Jiang, X., & Yu, X. (2018) · Acta Pharmacologica Sinica · doi:10.1038/aps.2017.178 · Cited by 395 · see citing works
Self-citationXiao, J., Pan, Y., Li, X. H., Yang, X. Y., Feng, Y. L., Tan, H. H., Jiang, L., Feng, J., & Yu, X. Y. (2016) · Cell Death & Disease · doi:10.1038/cddis.2016.181 · Cited by 373 · see citing works
Self-citationThe p53/miR-34 axis in development and disease
Rokavec, M., Li, H., Jiang, L., & Hermeking, H. (2014) · Journal of Molecular Cell Biology · doi:10.1093/jmcb/mju003 · Cited by 354 · see citing works
Baldari, S., Rocco, G. D., Piccoli, M., Pozzobon, M., Muraca, M., & Toietta, G. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18102087 · Cited by 281 · see citing works
Extracellular Vesicles: Evolving Factors in Stem Cell Biology
Nawaz, M., Fatima, F., Vallabhaneni, K. C., Penfornis, P., Valadi, H., Ekström, K. M., Kholia, S., Whitt, J. D., Fernandes, J. D., Pochampally, R. R., et al. (2015) · Stem Cells International · doi:10.1155/2016/1073140 · Cited by 225 · see citing works
Stem Cell Therapy in Heart Diseases – Cell Types, Mechanisms and Improvement Strategies
Müller, P., Lemcke, H., & David, R. (2018) · Cellular Physiology and Biochemistry · doi:10.1159/000492704 · Cited by 218 · see citing works
Roles of heat shock factor 1 beyond the heat shock response
Barna, J., Csermely, P., & Vellai, T. (2018) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-018-2836-6 · Cited by 199 · see citing works
Wu, Q., Wang, J., Tan, W. L. W., Jiang, Y. Y., Wang, S., Li, Q., Yu, X., Tan, J., Liu, S., Zhang, P., et al. (2020) · Cell Death and Disease · doi:10.1038/s41419-020-2508-y · Cited by 191 · see citing works
Self-citationPreconditioning Stem Cells for In Vivo Delivery
Sart, S., Ma, T., & Li, Y. (2014) · BioResearch open access · doi:10.1089/biores.2014.0012 · Cited by 166 · see citing works
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Yu, H., Lü, K., Zhu, J., & Wang, J. (2017) · British Medical Bulletin · doi:10.1093/bmb/ldw059 · Cited by 157 · see citing works
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Huang, W. C., Feng, Y., Liang, J., Yu, H., Wang, C., Wang, B., Wang, M., Jiang, L., Meng, W., Cai, W., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-03019-z · Cited by 161 · see citing works
Self-citationSharma, S., Mishra, R., Bigham, G. E., Wehman, B. P., Khan, M. M., Xu, H., Saha, P., Goo, Y. A., Datla, S. R., Chen, L., et al. (2016) · Circulation Research · doi:10.1161/circresaha.116.309782 · Cited by 140 · see citing works
Stone, M. L., Zhao, Y., Smith, J. R., Weiss, M. L., Kron, I. L., Laubach, V. E., & Sharma, A. K. (2017) · Respiratory Research · doi:10.1186/s12931-017-0704-9 · Cited by 134 · see citing works
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Bagheri, F., Khori, V., Alizadeh, A. M., Khalighfard, S., Khodayari, S., & Khodayari, H. (2016) · Life Sciences · doi:10.1016/j.lfs.2016.09.013 · Cited by 127 · see citing works
Secretory microRNAs as biomarkers of cancer
Kai, K., Dittmar, R. L., & Sen, S. (2017) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2017.12.011 · Cited by 112 · see citing works
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Chen, Q., Yang, F., Guo, M., Wen, G., Zhang, C., Luong, L. A., Zhu, J., Xiao, Q., & Zhang, L. (2015) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2015.10.017 · Cited by 86 · see citing works
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Song, Y., Zhong, C., & Wang, X. (2018) · Journal of Cellular Physiology · doi:10.1002/jcp.27110 · Cited by 82 · see citing works
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Wu, R., Hu, X., & Wang, J. (2018) · Stem Cells · doi:10.1002/stem.2778 · Cited by 82 · see citing works
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Tang, Y., Ma, Y., Zhang, Z., Wang, Y., & Yang, G. (2015) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.12386 · Cited by 77 · see citing works
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Prince, T. L., Lang, B. J., Guerrero-Gimenez, M. E., Fernandez-Muñoz, J. M., Ackerman, A., & Calderwood, S. K. (2020) · Cells · doi:10.3390/cells9041046 · Cited by 67 · see citing works
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Li, L., Jin, S., & Zhang, Y. (2015) · Europe PMC (PubMed Central) · Cited by 61 · see citing works
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Patil, M., Henderson, J., Luong, H. T., Annamalai, D., Sreejit, G., & Krishnamurthy, P. (2019) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2019.00315 · Cited by 58 · see citing works
Chen, J., Huang, F., Hou, Y., Lin, X., Liang, R., Hu, X., Zhao, J. J., Wang, J., Olsen, N. J., & Zheng, S. G. (2021) · Cellular and Molecular Immunology · doi:10.1038/s41423-021-00764-y · Cited by 64 · see citing works
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Sarmah, D., Kaur, H., Saraf, J., Pravalika, K., Goswami, A., Kalia, K., Borah, A., Wang, X., Dave, K. R., Yavagal, D. R., et al. (2017) · Translational Stroke Research · doi:10.1007/s12975-017-0580-0 · Cited by 56 · see citing works
Wang, Q., Li, X., Wang, Q., Xie, J., Xie, C., & Fu, X. (2019) · Stem Cell Research & Therapy · doi:10.1186/s13287-019-1425-4 · Cited by 56 · see citing works
RetractedKahrizi, M. S., Mousavi, E., Khosravi, A., Rahnama, S., Salehi, A., Nasrabadi, N., Ebrahimzadeh, F., & Jamali, S. (2023) · Stem Cell Research & Therapy · doi:10.1186/s13287-023-03374-9 · Cited by 61 · see citing works
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Hodjat, M., Rezvanfar, M. A., & Abdollahi, M. R. (2015) · Food and Chemical Toxicology · doi:10.1016/j.fct.2015.11.002 · Cited by 49 · see citing works
He, N., Xu, Y., Du, W., Qi, X., Liang, L., Wang, Y., Feng, G., Fan, Y. L., Han, Z., Kong, D., et al. (2015) · Scientific Reports · doi:10.1038/srep10902 · Cited by 51 · see citing works
Self-citationDelphinidin suppresses breast carcinogenesis through the HOTAIR /micro RNA ‐34a axis
Han, B., Peng, X., Cheng, D., Zhu, Y., Du, J.-C., Li, J., & Yu, X. (2019) · Cancer Science · doi:10.1111/cas.14133 · Cited by 51 · see citing works
Self-citationChen, X., Wang, Q., Li, X., Wang, Q., Xie, J., & Fu, X. (2018) · Stem Cell Research & Therapy · doi:10.1186/s13287-018-0964-4 · Cited by 50 · see citing works
Mei, L., Chen, Y., Chen, P., Chen, H., He, S., Jin, C., Wang, Y., Hu, Z., Li, W., Jin, L., et al. (2022) · Redox Biology · doi:10.1016/j.redox.2022.102468 · Cited by 49 · see citing works
Self-citationLiu, X., Zhang, C., Zhang, C., Li, J., Guo, W., Yan, D., Chen, Y., Zhao, J., Xia, T., Wang, Y., et al. (2016) · In Vitro Cellular & Developmental Biology - Animal · doi:10.1007/s11626-016-0039-8 · Cited by 49 · see citing works
Self-citationSarkissian, S. D., Lévesque, T., & Noiseux, N. (2017) · World Journal of Stem Cells · doi:10.4252/wjsc.v9.i1.9 · Cited by 49 · see citing works
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Zhao, M., Fan, C., Ernst, P. J., Tang, Y., Zhu, H., Mattapally, S., Oduk, Y., Borovjagin, A. V., Zhou, L., Zhang, J. J., et al. (2018) · Cardiovascular Research · doi:10.1093/cvr/cvy207 · Cited by 45 · see citing works
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Kanda, P., Alarcon, E. I., Yeuchyk, T., Parent, S., de Kemp, R., Variola, F., Courtman, D. W., Stewart, D. J., & Davis, D. R. (2018) · ACS Nano · doi:10.1021/acsnano.7b08881 · Cited by 32 · see citing works
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Amosse, J., Martínez, M. C., & Lay, S. L. (2017) · Stem Cell Investigation · doi:10.21037/sci.2017.11.07 · Cited by 30 · see citing works
Al‐Dhamin, Z., Liu, L., Li, D., Zhang, S., Dong, S., & Nan, Y. (2020) · World Journal of Gastroenterology · doi:10.3748/wjg.v26.i47.7444 · Cited by 30 · see citing works
Zhao, C., Li, H., Zhao, X., Liu, Z., Zhou, P., Liu, Y., & Feng, M. (2016) · Neurochemical Research · doi:10.1007/s11064-015-1816-6 · Cited by 29 · see citing works
Stem Cell Therapy for the Heart: Blind Alley or Magic Bullet?
Bruyneel, A. A. N., Sehgal, A., Malandraki-Miller, S., & Carr, C. A. (2016) · Journal of Cardiovascular Translational Research · doi:10.1007/s12265-016-9708-y · Cited by 27 · see citing works
Role of Extracellular Vesicles in Compromising Cellular Resilience to Environmental Stressors
Alharbi, M. G., Lee, S. H., Abdelazim, A. M., Saadeldin, I. M., & Abomughaid, M. M. (2021) · BioMed Research International · doi:10.1155/2021/9912281 · Cited by 28 · see citing works
The potential role of exosomes in the diagnosis and therapy of ischemic diseases
Wang, W., Li, Z., & Feng, J. (2018) · Cytotherapy · doi:10.1016/j.jcyt.2018.06.012 · Cited by 27 · see citing works
Zhang, C., Liu, X., Miao, J., Wang, S., Wu, L., Yan, D., Li, J., Guo, W., Xiang, W., & Shen, A. (2017) · APOPTOSIS · doi:10.1007/s10495-017-1355-5 · Cited by 26 · see citing works
Thermotolerance in S. cerevisiae as a model to study extracellular vesicle biology
Logan, C. J., Staton, C. C., Oliver, J., Bouffard, J., Kazmirchuk, T. D. D., Magi, M., & Brett, C. L. (2024) · Journal of Extracellular Vesicles · doi:10.1002/jev2.12431 · Cited by 25 · see citing works
The mesmiRizing complexity of microRNAs for striated muscle tissue engineering
Quattrocelli, M., & Sampaolesi, M. (2015) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2015.04.011 · Cited by 24 · see citing works
Translational aspects of cardiac cell therapy
Chen, C., Sereti, K., Wu, B. M., & Ardehali, R. (2015) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.12632 · Cited by 23 · see citing works
The caspase-8 shRNA-modified mesenchymal stem cells improve the function of infarcted heart
Liang, Y., Lin, Q., Zhu, J.-N., Li, X., Fu, Y., Zou, X., Liu, X., Tan, H., Deng, C., Yu, X., et al. (2014) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-014-2165-5 · Cited by 23 · see citing works
Self-citationDai, F., Du, P., Chang, Y., Ji, E., Xu, Y., Wei, C., & Li, J. (2018) · Medical Science Monitor · doi:10.12659/msm.907441 · Cited by 23 · see citing works
Exosomal non-coding RNAs (Exo-ncRNAs) in cardiovascular health
de Giusti, C. J., Santalla, M., & Das, S. (2019) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2019.09.016 · Cited by 22 · see citing works
Sharma, S., Mishra, R., SIMPSON, D. L., Wehman, B. P., Colletti, E. J., Deshmukh, S., Datla, S. R., Balachandran, K., Guo, Y., Chen, L., et al. (2015) · Stem Cells · doi:10.1002/stem.1937 · Cited by 22 · see citing works
The Potential of Stem Cells and Stem Cell-Derived Exosomes in Treating Cardiovascular Diseases
Ni, J., Sun, Y., & Liu, Z. (2018) · Journal of Cardiovascular Translational Research · doi:10.1007/s12265-018-9799-8 · Cited by 21 · see citing works
Lin, X., Wang, Z., Lin, Y.-X., & Chen, H. H. (2021) · World Journal of Surgical Oncology · doi:10.1186/s12957-021-02381-5 · Cited by 20 · see citing works
Bioengineering Extracellular Vesicles for the Treatment of Cardiovascular Diseases
Ramasubramanian, L., Du, S., Gidda, S. S., Bahatyrevich, N., Hao, D., Kumar, P., & Wang, A. (2022) · Advanced Biology · doi:10.1002/adbi.202200087 · Cited by 20 · see citing works
Ye, X., Lin, Z.-J., Hong, G.-H., Wang, Z.-M., Dou, R.-T., Lin, J., Xie, J., & Shen, Y. (2024) · Experimental Cell Research · doi:10.1016/j.yexcr.2024.114061 · Cited by 20 · see citing works
Advances in Exosomes Derived from Different Cell Sources and Cardiovascular Diseases
Liang, B., He, X., Zhao, Y.-X., Zhang, X., & Gu, N. (2020) · BioMed Research International · doi:10.1155/2020/7298687 · Cited by 19 · see citing works
Maxwell, J. T., Trac, D. Q., Shen, M., Brown, M. E., Davis, M. E., Chao, M. S., Supapannachart, K. J., Zaladonis, C. A., Baker, E., Li, M. L., et al. (2019) · Stem Cells · doi:10.1002/stem.3088 · Cited by 18 · see citing works
Proteomics Analysis of Brain Tissue in a Rat Model of Ischemic Stroke in the Acute Phase
Zheng, F., Zhou, Y., Zeng, Y., Liu, T., Yang, Z., Tang, T., Luo, J., & Wang, Y. (2020) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2020.00027 · Cited by 18 · see citing works
Self-citationMicroRNA-34a Promotes Ischemia-Induced Cardiomyocytes Apoptosis through Targeting Notch1
Pan, J., Zhou, L., Lin, C., Xue, W., Chen, P., & Lin, J. (2022) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2022/1388415 · Cited by 17 · see citing works
Lim, K., Dayem, A. A., Choi, Y.-J., Lee, Y., An, J., Gil, M., Lee, S., Kwak, H. J., Vellingirl, B., Shin, H., et al. (2021) · Antioxidants · doi:10.3390/antiox10081292 · Cited by 14 · see citing works
Savvateeva-Popova, E. V., Zhuravlev, A. V., Brázda, V., Zakharov, G. A., Kaminskaya, A. N., Медведева, А. В., Nikitina, E. A., Tokmacheva, E. V., Dolgaya, J. F., Kulikova, D. A., et al. (2017) · Frontiers in Genetics · doi:10.3389/fgene.2017.00123 · Cited by 16 · see citing works
The Future of Direct Cardiac Reprogramming: Any GMT Cocktail Variety?
López-Muneta, L., Miranda-Arrubla, J., & Carvajal‐Vergara, X. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21217950 · Cited by 16 · see citing works
Vašíčková, K., Moráň, L., Gurín, D., & Vaňhara, P. (2018) · Cell and Tissue Research · doi:10.1007/s00441-018-2888-9 · Cited by 15 · see citing works
Strecanska, M., Sekelova, T., Csöbönyeiová, M., Danišovič, Ľ., & Čeháková, M. (2024) · Life Sciences · doi:10.1016/j.lfs.2024.122647 · Cited by 14 · see citing works
Akabane, M., Imaoka, Y., Kawashima, J., Endo, Y., Schenk, A. D., Sasaki, K., & Pawlik, T. M. (2024) · Cells · doi:10.3390/cells13191604 · Cited by 14 · see citing works
Protective role of heat shock transcription factor 1 in heart failure: A diagnostic approach
Haybar, H., Shahrabi, S., Rezaeeyan, H., Shirzad, R., & Saki, N. (2018) · Journal of Cellular Physiology · doi:10.1002/jcp.27639 · Cited by 14 · see citing works
Plasma Membrane Epichaperome–Lipid Interface: Regulating Dynamics and Trafficking
Amissah, H. A., Likhomanova, R., Opoku, G., Amissah, T. A., Balogi, Z., Török, Z., Vı́gh, L., Combs, S. E., & Shevtsov, M. A. (2025) · Cells · doi:10.3390/cells14201582 · Cited by 13 · see citing works
Wu, X., Wang, D., Qin, K., Iroegbu, C. D., Xiang, K., Zhou, Y., Guan, Q., Tang, W., Peng, J., Guo, J., et al. (2021) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2021.768873 · Cited by 12 · see citing works
YOKOYAMA, S., Ohno, Y., Egawa, T., Yasuhara, K., Nakai, A., Sugiura, T., Ohira, Y., Yoshioka, T., Okita, M., Origuchi, T., et al. (2016) · Acta Physiologica · doi:10.1111/apha.12692 · Cited by 11 · see citing works
Extracellular vesicles as next-generation therapeutics and biomarkers in amyloidosis: a new frontier
Phan, T. H., & Reed, J. H. (2024) · Frontiers in Biomaterials Science · doi:10.3389/fbiom.2023.1343658 · Cited by 10 · see citing works
Opportunities and Challenges in Stem Cell Aging
Larijani, B. A., Heravani, N. F., Alaei, S., Rezaei–Tavirani, M., Alavi-Moghadam, S., Payab, M., Goodarzi, P., Tayanloo-Beik, A., Aghayan, H. R., & Arjmand, B. (2021) · Advances in experimental medicine and biology · doi:10.1007/5584_2021_624 · Cited by 10 · see citing works
Lafuente‐Gómez, N., Martínez‐Mingo, M., Díaz‐Riascos, Z. V., García-Prats, B., de la Iglesia, I., Dhanjani, M., García‐Soriano, D., Campos, L. A., Mancilla, S., Salas, G., et al. (2025) · Journal of Controlled Release · doi:10.1016/j.jconrel.2025.113791 · Cited by 9 · see citing works
Neurogenetics and neuroepigenetics
Savvateeva-Popova, E. V., Nikitina, E. A., & Медведева, А. В. (2015) · Russian Journal of Genetics · doi:10.1134/s1022795415050075 · Cited by 14 · see citing works
Rurali, E., Vinci, M. C., Bassetti, B., Barbagallo, V., Pompilio, G., & Gambini, E. (2020) · Current Stem Cell Research & Therapy · doi:10.2174/1574888x15666200225124451 · Cited by 8 · see citing works
Xu, H., Takashi, E., Liang, J., Chen, Y., Yuan, Y., & Fan, J. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23168955 · Cited by 6 · see citing works
- Authors
- Feng, Y., Huang, W., Meng, W., Jegga, A. G., Wang, Y., Cai, W., Kim, H. W., Pasha, Z., Wen, Z., Rao, F., Modi, R. M., Yu, X., & Ashraf, M.
- Affiliations
- Guangdong General Hospital (CN)
- University of Cincinnati (US)
- Third Affiliated Hospital of Sun Yat-sen University (CN)
- Cincinnati Children's Hospital Medical Center (US)
- Nanchang University (CN)
- Medical Research Center of Guangdong General Hospital, Guangdong Academy of Medical Sciences Guangdong Provincial Cardiovascular Institute, Southern Medical University, Guangzhou, China
- Corresponding author
- Ashraf, Muhammad
- ORCID
- Venue
- Stem Cells
- Publisher
- Oxford University Press (OUP)
- Published
- 2014-01-13
- Volume
- 32
- Issue
- 2
- Pages
- 462-472
- ISSN
- 1066-5099 (ISSN-L)
- 1549-4918
- PMC
- PMC5517317
- OpenAlex
- W1835157090
- Cited by
- 121
- References
- 26
- Citations by year
- 2026: 3 · 2025: 4 · 2024: 7 · 2023: 4 · 2022: 11 · 2021: 13 · 2020: 10 · 2019: 9 · 2018: 15 · 2017: 17 · 2016: 8 · 2015: 13 · 2014: 7
- FWCI
- 4.18
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model (vor)
- Locations
- Stem Cells (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health Grants (R37-HL-074272, HL-095375, HL-087246)
- National Natural Science Foundation of China (81120108003, 81330007)
- National Key Basic Research Program of China (2012CB526602)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Heat shock proteins research
- Health Sciences › Medicine › Genetics › Mesenchymal stem cell research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Congenital heart defects research
- Keywords
- heat shock, HSF1, miR-34a, HSP70, H3K27me3, epigenetic repression, stem cell survival, paracrine signaling, ischemic heart disease, stem cell therapy, cardiomyocyte apoptosis, myocardial fibrosis
- MeSH terms
- Heat Shock Transcription Factors, Antigens, Ly, Cell Survival, DNA-Binding Proteins, Humans, Membrane Proteins, Stem Cells, Transcription Factors, Apoptosis, HSP70 Heat-Shock Proteins, Heat-Shock Response, Myocytes, Cardiac, MicroRNAs, Exosomes
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