MicroRNA-126 overexpression rescues diabetes-induced impairment in efferocytosis of apoptotic cardiomyocytes
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Efferocytosis, a process of clearance of apoptotic cells by phagocytes, is essential for successful resolution of inflammation and maintenance of tissue homeostasis. Diabetes compromises the function of macrophages leading to adverse inflammatory response during wound healing, myocardial injury, atherosclerosis and autoimmune disorders. However, the effect of diabetes on macrophage-mediated efferocytosis of apoptotic cardiomyocytes (ACM) and the molecular mechanisms involved are not understood so far. In the present study we found that invitro efferocytosis of ACM was impaired in macrophages from db/db (diabetic) mice. Macrophages exposed to high glucose (HG) decreases microRNA-126 (miR-126) expression with a corresponding increase in ADAM9 expression. Dual-luciferase reporter assay confirms that ADAM9 3′UTR contains miR-126 target site. ADAM9 inhibition reduces HG-induced proteolytic cleavage of Mer tyrosine receptor kinase (MerTK, a proto-oncogene that plays a critical role in phagocytosis), resulting in shedding of soluble-Mer (sMER) and loss of MERTK function. Over-expression of miR-126 attenuates HG-induced impairment of efferocytosis. Furthermore, human diabetic hearts show lower miR-126 expression with a corresponding increase in ADAM9 expression vs. normal counterparts. These data suggests that diabetes impairs efferocytosis of ACM and that strategies to enhance efferocytosis might attenuate diabetes-induced impairment in inflammation resolution and cardiac repair after injury.
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miR-126 overexpression attenuates high glucose-induced impairment of efferocytosis.
“Babu et al. showed the next microRNA able to affect efferocytosis, miR-126 overexpression, attenuates high glucose-induced impairment of efferocytosis [218].”
From MicroRNAs as Regulators of Phagocytosis (2022) · cites this paper as [218]
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From Vulnerable Plaque to Vulnerable Patient
Naghavi, M., Libby, P., Falk, E., Casscells, S. W., Litovsky, S. H., Rumberger, J. A., Badimón, J. J., Stefanadis, C., Moreno, P., Pasterkamp, G., et al. (2003) · Circulation · doi:10.1161/01.cir.0000087481.55887.c9 · Cited by 2,686 · see citing works
From Vulnerable Plaque to Vulnerable Patient
Naghavi, M., Libby, P., Falk, E., Casscells, S. W., Litovsky, S. H., Rumberger, J. A., Badimón, J. J., Stefanadis, C., Moreno, P., Pasterkamp, G., et al. (2003) · Circulation · doi:10.1161/01.cir.0000087480.94275.97 · Cited by 2,270 · see citing works
The Endothelial-Specific MicroRNA miR-126 Governs Vascular Integrity and Angiogenesis
Wang, S., Aurora, A. B., Johnson, B. A., Qi, X., McAnally, J., Hill, J. A., Richardson, J. A., Bassel‐Duby, R., & Olson, E. N. (2008) · Developmental Cell · doi:10.1016/j.devcel.2008.07.002 · Cited by 1,825 · see citing works
miR-126 Regulates Angiogenic Signaling and Vascular Integrity
Fish, J. E., Santoro, M. M., Morton, S. U., Yu, S., Yeh, R.-F., Wythe, J. D., Ivey, K. N., Bruneau, B. G., Stainier, D. Y. R., & Srivastava, D. (2008) · Developmental Cell · doi:10.1016/j.devcel.2008.07.008 · Cited by 1,728 · see citing works
Plasma MicroRNA Profiling Reveals Loss of Endothelial MiR-126 and Other MicroRNAs in Type 2 Diabetes
Zampetaki, A., Kiechl, S. J., Drozdov, I. A., Willeit, P., Mayr, U., Prokopi, M., Mayr, A., Weger, S., Oberhollenzer, F., Bonora, E., et al. (2010) · Circulation Research · doi:10.1161/circresaha.110.226357 · Cited by 1,457 · see citing works
The ADAMs family of metalloproteases: multidomain proteins with multiple functionsPreprint
Seals, D. F., & Courtneidge, S. A. (2003) · Genes & Development · doi:10.1101/gad.1039703 · Cited by 1,058 · see citing works
Macrophage Dysfunction Impairs Resolution of Inflammation in the Wounds of Diabetic Mice
Khanna, S., Biswas, S., Shang, Y., Collard, E., Azad, A., Kauh, C., Bhasker, V., Gordillo, G. M., Sen, C. K., & Roy, S. (2010) · PLoS ONE · doi:10.1371/journal.pone.0009539 · Cited by 694 · see citing works
Consequences and Therapeutic Implications of Macrophage Apoptosis in Atherosclerosis
Tabas, I. A. (2005) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000184783.04864.9f · Cited by 641 · see citing works
van Amerongen, M. J., Harmsen, M. C., van Rooijen, N., Petersen, A. H., & van Luyn, M. J. A. (2007) · The American Journal of Pathology · doi:10.2353/ajpath.2007.060547 · Cited by 544 · see citing works
Krishnamurthy, P., Rajasingh, J., Lambers, E., Qin, G., Losordo, D. W., & Kishore, R. (2008) · Circulation Research · doi:10.1161/circresaha.108.188243 · Cited by 423 · see citing works
Self-citationTraverse, J. H. (2011) · JAMA · doi:10.1001/jama.2011.1670 · Cited by 404 · see citing works
Wan, E. Y., Yeap, X. Y., Dehn, S., Terry, R. L., Novak, M. L., Zhang, S., Iwata, S., Han, X., Homma, S., Drosatos, K., et al. (2013) · Circulation Research · doi:10.1161/circresaha.113.301198 · Cited by 385 · see citing works
Sather, S., Kenyon, K. D., Lefkowitz, J. B., Liang, X., Varnum, B. C., Henson, P. M., & Graham, D. K. (2006) · Blood · doi:10.1182/blood-2006-05-021634 · Cited by 333 · see citing works
Miksa, M., Komura, H., Wu, R., Shah, K. G., & Wang, P. (2009) · Journal of Immunological Methods · doi:10.1016/j.jim.2008.11.019 · Cited by 320 · see citing works
Thorp, E., Vaisar, T., Subramanian, M., Mautner, L., Blobel, C., & Tabas, I. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.263020 · Cited by 298 · see citing works
MicroRNAs in resolution of acute inflammation: identification of novel resolvin Dl‐miRNA circuits
Recchiuti, A., Krishnamoorthy, S., Fredman, G., Chiang, N., & Serhan, C. N. (2011) · The FASEB Journal · doi:10.1096/fj.10-169599 · Cited by 292 · see citing works
Role of microRNAs in diabetes and its cardiovascular complications
Shantikumar, S., Caporali, A., & Emanueli, C. (2012) · Cardiovascular Research · doi:10.1093/cvr/cvr300 · Cited by 263 · see citing works
ADAM 12 Cleaves Extracellular Matrix Proteins and Correlates with Cancer Status and Stage
Roy, R., Wewer, U. M., Zurakowski, D., Pories, S. E., & Moses, M. A. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m409565200 · Cited by 244 · see citing works
Macrophages mediate cardioprotective cellular postconditioning in acute myocardial infarction
de Couto, G., Liu, W., Tseliou, E., Sun, B., Makkar, N., Kanazawa, H., Arditi, M., & Marbán, E. (2015) · Journal of Clinical Investigation · doi:10.1172/jci81321 · Cited by 240 · see citing works
Mechanisms and consequences of efferocytosis in advanced atherosclerosis
Thorp, E., & Tabas, I. (2009) · Journal of Leukocyte Biology · doi:10.1189/jlb.0209115 · Cited by 231 · see citing works
Liu, Y., Gao, G., Yang, C., Zhou, K., Shen, B., Liang, H., & Jiang, X. (2014) · International Journal of Molecular Sciences · doi:10.3390/ijms150610567 · Cited by 193 · see citing works
Myocardial healing requires Reg3β-dependent accumulation of macrophages in the ischemic heart
Lörchner, H., Pöling, J., Gajawada, P., Hou, Y., Polyakova, V., Sawa Kostin, D., Adrian-Segarra, J. M., Boettger, T., Wietelmann, A., Warnecke, H., et al. (2015) · Nature Medicine · doi:10.1038/nm.3816 · Cited by 177 · see citing works
MiR-126 Acts as a Tumor Suppressor in Pancreatic Cancer Cells via the Regulation of ADAM9
Hamada, S., Satoh, K., Fujibuchi, W., Hirota, M., Kanno, A., Unno, J., Masamune, A., Kikuta, K., Kume, K., & Shimosegawa, T. (2011) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-11-0272 · Cited by 157 · see citing works
Tibrewal, N., Wu, Y., D’Mello, V., Akakura, R., George, T. C., Varnum, B. C., & Birge, R. B. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m706906200 · Cited by 156 · see citing works
Zhang, T., Lv, C., Li, L., Chen, S., Liu, S., Wang, C., & Su, B. (2013) · BioMed Research International · doi:10.1155/2013/761617 · Cited by 155 · see citing works
Goren, I., Müller, E., Schiefelbein, D., Christen, U., Pfeilschifter, J., Mühl, H., & Frank, S. (2007) · Journal of Investigative Dermatology · doi:10.1038/sj.jid.5700842 · Cited by 151 · see citing works
Fischer, O. M., Hart, S., Gschwind, A., Prenzel, N., & Ullrich, A. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.12.5172-5183.2004 · Cited by 151 · see citing works
Grützmann, R., Lüttges, J., Sipos, B., Ammerpohl, O., Dobrowolski, F., Alldinger, I., Kersting, S., Ockert, D., Koch, R., Kalthoff, H., et al. (2004) · British Journal of Cancer · doi:10.1038/sj.bjc.6601645 · Cited by 140 · see citing works
Hypoxia-Induced Deregulation of miR-126 and Its Regulative Effect on VEGF and MMP-9 Expression
Ye, P., Liu, J., He, F.-Y., Xu, W., & Yao, K. (2014) · International Journal of Medical Sciences · doi:10.7150/ijms.7329 · Cited by 117 · see citing works
Shedding of membrane proteins by ADAM family proteases
Moss, M. L., & Lambert, M. H. (2002) · Essays in Biochemistry · doi:10.1042/bse0380141 · Cited by 99 · see citing works
Nguyen, K.-Q. N., Tsou, W., Calarese, D. A., Kimani, S. G., Singh, S., Hsieh, S., Liu, Y., Lü, B., Wu, Y., Garforth, S., et al. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.570838 · Cited by 99 · see citing works
Oxidative Stress Induces ADAM9 Protein Expression in Human Prostate Cancer Cells
Sung, S., Kubo, H., Shigemura, K., Arnold, R. S., Logani, S., Wang, R., Konaka, H., Nakagawa, M., Mousses, S., Amin, M. B., et al. (2006) · Cancer Research · doi:10.1158/0008-5472.can-05-4375 · Cited by 99 · see citing works
MerTK-mediated engulfment of pyrenocytes by central macrophages in erythroblastic islands
Toda, S., Segawa, K., & Nagata, S. (2014) · Blood · doi:10.1182/blood-2014-01-547976 · Cited by 80 · see citing works
MicroRNA-126 inhibits invasion in bladder cancer via regulation of ADAM9
Jia, A. Y., Castillo-Martín, M., Bonal, D. M., Sänchez‐Carbayo, M., Silva, J. M., & Cordon‐Cardo, C. (2014) · British Journal of Cancer · doi:10.1038/bjc.2014.245 · Cited by 75 · see citing works
Gu, Q., Yang, X., Li, L., Li, S., Li, Q., Zhong, S., Peng, J., & Cui, Z. (2014) · Hepatology · doi:10.1002/hep.27356 · Cited by 74 · see citing works
MiR-126 regulated breast cancer cell invasion by targeting ADAM9.
Wang, C., Yuan, P., & Li, Y. (2015) · PubMed · Cited by 73 · see citing works
Enhanced Cardiac Regenerative Ability of Stem Cells After Ischemia-Reperfusion Injury
Joladarashi, D., Garikipati, V. N. S., Thandavarayan, R. A., Verma, S. K., Mackie, A. R., Khan, M., Gumpert, A. M., Bhimaraj, A., Youker, K. A., Uribe, C., et al. (2015) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2015.09.009 · Cited by 69 · see citing works
Self-citationInvolvement of ADAM9 in Multinucleated Giant Cell Formation of Blood Monocytes
Namba, K., Nishio, M., Mori, K., Miyamoto, N., Tsurudome, M., Ito, M., Kawano, M., Uchida, A., & Ito, Y. (2001) · Cellular Immunology · doi:10.1006/cimm.2001.1873 · Cited by 66 · see citing works
Singh, B., Schneider, M., Knyazev, P. G., & Ullrich, A. (2008) · International Journal of Cancer · doi:10.1002/ijc.23974 · Cited by 64 · see citing works
Krause, S., Pfeiffer, C., Strube, S., Alsadeq, A., Fedders, H., Vokuhl, C., Loges, S., Waizenegger, J. S., Batalla, I. B., Cario, G., et al. (2014) · Blood · doi:10.1182/blood-2014-06-583062 · Cited by 60 · see citing works
Poissonnier, L., Villain, G., Soncin, F., & Mattot, V. (2014) · Cardiovascular Research · doi:10.1093/cvr/cvu040 · Cited by 58 · see citing works
Xiong, Y., Kotian, S., Zeiger, M. A., Zhang, L., & Kebebew, E. (2015) · PLoS ONE · doi:10.1371/journal.pone.0130496 · Cited by 54 · see citing works
Choi, J.-Y., Park, H.-J., Lee, Y.-J., Byun, J., Youn, Y.-S., Choi, J. H., Woo, S., & Kang, J. L. (2012) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.112.199778 · Cited by 52 · see citing works
Sirtuin‐6 deficiency exacerbates diabetes‐induced impairment of wound healing
Thandavarayan, R. A., Garikipati, V. N. S., Joladarashi, D., Babu, S. S., Jeyabal, P., Verma, S. K., Mackie, A. R., Khan, M., Arumugam, S., Watanabe, K., et al. (2015) · Experimental Dermatology · doi:10.1111/exd.12762 · Cited by 52 · see citing works
Self-citationMicroRNA-126 in Atherosclerosis
Boon, R. A., & Dimmeler, S. (2014) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.114.303572 · Cited by 36 · see citing works
Liu, C.-M., Hsieh, C., He, Y.-C., Lo, S.-J., Liang, J., Hsieh, T.-F., Josson, S., Chung, L. W. K., Hung, M., & Sung, S. (2013) · PLoS ONE · doi:10.1371/journal.pone.0053795 · Cited by 33 · see citing works
Shedding Light on Impaired Efferocytosis and Nonresolving Inflammation
Novak, M. L., & Thorp, E. B. (2013) · Circulation Research · doi:10.1161/circresaha.113.301583 · Cited by 31 · see citing works
Targeting miRNAs for Pancreatic Cancer Therapy
Shi, M., DachengXie, Gaod, Y., & Xie, K. (2014) · Current Pharmaceutical Design · doi:10.2174/1381612820666140128210443 · Cited by 18 · see citing works
The Reparative Function of Cardiomyocytes in the Infarcted Myocardium
Frangogiannis, N. G. (2015) · Cell Metabolism · doi:10.1016/j.cmet.2015.05.015 · Cited by 11 · see citing works
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Doran, A. C., Yurdagul, A., & Tabas, I. (2020) · Nature Reviews Immunology · doi:10.1038/s41577-019-0240-6 · Cited by 1,066 · see citing works
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Chen, R., Zhang, H., Tang, B., Luo, Y., Yang, Y., Zhong, X., Chen, S., Xu, X., Huang, S., & Liu, C. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-024-01840-1 · Cited by 387 · see citing works
Jakubik, D., Fitas, A., Eyileten, C., Jarosz-Popek, J., Nowak, A., Czajka, P., Wicik, Z., Sourij, H., Siller-Matula, J. M., Rosa, S. D., et al. (2021) · Cardiovascular Diabetology · doi:10.1186/s12933-021-01245-2 · Cited by 99 · see citing works
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Umehara, T., Mori, R., Mace, K. A., Murase, T., Abe, Y., Yamamoto, T., & Ikematsu, K. (2018) · Diabetes · doi:10.2337/db18-0313 · Cited by 65 · see citing works
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Johnson, C., Drummer, C., Virtue, A. T., Gao, T., Wu, S., Ibáñez-Hernández, M. Á., Singh, L., Wang, H., & Yang, X. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.01297 · Cited by 45 · see citing works
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Xie, Y., Chen, H., Qu, P., Qiao, X., Guo, L., & Liu, L. (2022) · International Immunopharmacology · doi:10.1016/j.intimp.2022.109260 · Cited by 39 · see citing works
DeBerge, M., Zhang, S., Glinton, K. E., Grigoryeva, L., Hussein, I., Vorovich, E., Ho, K. J., Luo, X., & Thorp, E. B. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01428 · Cited by 37 · see citing works
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Dueñas, Á., Expósito, A., Muñoz, M. D. M., de Manuel, M. J., Cámara-Morales, A., Serrano-Osorio, F., García‐Padilla, C., Hernández‐Torres, F., Dominguez, J. N., Aránega, A. E., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-66325-x · Cited by 28 · see citing works
Immune Regulation of Tissue Repair and Regeneration via miRNAs—New Therapeutic Target
Piotto, C., Julier, Z., & Martino, M. (2018) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2018.00098 · Cited by 23 · see citing works
Gu, Y., Rampin, A., Alvino, V. V., Spinetti, G., & Madeddu, P. R. (2021) · Current Diabetes Reports · doi:10.1007/s11892-021-01378-4 · Cited by 27 · see citing works
Duan, Y., Zou, J., Mao, J., Guo, D., Wu, M., Xu, N., Zhou, J., Zhang, Y., Guo, W., & Jin, W. (2019) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2019.108761 · Cited by 25 · see citing works
MicroRNAs as Regulators of Phagocytosis
Gierlikowski, W., & Gierlikowska, B. (2022) · Cells · doi:10.3390/cells11091380 · Cited by 25 · see citing works
Leng, Q., Ding, J., Dai, M., Liu, L., Fang, Q., Wang, D. W., Wu, L., & Wang, Y. (2022) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2022.879351 · Cited by 27 · see citing works
Bravo, D. D., Shi, Y., Sheu, A., Liang, W., Lin, W., Wu, Y., Yan, M., & Wang, J. (2023) · The Journal of Immunology · doi:10.4049/jimmunol.2200597 · Cited by 25 · see citing works
Wang, X., Du, W., Li, Y., Yang, H., Zhang, Y., Akbar, R., Morgan, H., Peng, T., Chen, J., Sadayappan, S., et al. (2024) · JCI Insight · doi:10.1172/jci.insight.173832 · Cited by 24 · see citing works
Mao, Q., He, S., Hu, Q., Lu, Y., Niu, Y., Li, X., Zhang, H., Qin, L., & Su, Q. (2022) · The Journal of Immunology · doi:10.4049/jimmunol.2100695 · Cited by 23 · see citing works
Cellular mechanisms underlying the impairment of macrophage efferocytosis
Ma, Y., Kemp, S. S., Yang, X., Wu, M. H., & Yuan, S. Y. (2023) · Immunology Letters · doi:10.1016/j.imlet.2023.02.001 · Cited by 22 · see citing works
Circulating miR-126-3p is a mechanistic biomarker for knee osteoarthritis
Wilson, T. G., Baghel, M., Kaur, N., Datta, I., Loveless, I. M., Potla, P., Méndez, D., Hansen, L. M., Baker, K. C., Lynch, T. S., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-57308-5 · Cited by 22 · see citing works
Ferrière, A., Santa, P., Garreau, A., Bandopadhyay, P., Blanco, P., Ganguly, D., & Sisirak, V. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2020.624256 · Cited by 22 · see citing works
Liu, B., Wang, R. Y., & Liu, H. (2021) · BioMed Research International · doi:10.1155/2021/6622342 · Cited by 22 · see citing works
RetractedDetection of molecular signatures and pathways shared by Alzheimer’s disease and type 2 diabetes
Shu, J., Li, N., Wei, W., & Zhang, L. (2021) · Gene · doi:10.1016/j.gene.2021.146070 · Cited by 23 · see citing works
Mechanisms and Advances of Epigenetic Regulation in Cardiovascular Disease
Wang, X., Teng, X., Luo, C., & Kong, L. (2024) · Frontiers in Bioscience-Landmark · doi:10.31083/j.fbl2906205 · Cited by 22 · see citing works
Geraets, I. M. E., Chanda, D., van Tienen, F. H. J., van den Wijngaard, A., Kamps, R., Neumann, D., Liu, Y., Glatz, J. F. C., Luiken, J. J. F. P., & Nabben, M. (2017) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2017.12.025 · Cited by 21 · see citing works
Therapeutic strategies targeting mechanisms of macrophages in diabetic heart disease
Zhang, C., Shi, Y., Liu, C., Sudesh, S. M., Zhao, H., Li, P., Liu, Q., Ma, Y., Shi, A., & Cai, H. (2024) · Cardiovascular Diabetology · doi:10.1186/s12933-024-02273-4 · Cited by 22 · see citing works
Effect of diabetes on efferocytosis process
Mahmoudi, A. A., Firouzjaei, A. A., Darijani, F., Navashenaq, J. G., Taghizadeh, E., Darroudi, M., & Hayat, S. M. G. (2022) · Molecular Biology Reports · doi:10.1007/s11033-022-07725-2 · Cited by 20 · see citing works
Zhang, B., Wu, Y., Wang, Z., Gao, S., Liu, H., Lin, Y., & Yu, P. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1521554 · Cited by 17 · see citing works
High Glucose Impairs Expression and Activation of MerTK in ARPE-19 Cells
Puddu, A., Ravera, S., Panfoli, I., Bertola, N., & Maggi, D. C. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23031144 · Cited by 17 · see citing works
Liu, X., Liu, H., & Deng, Y. (2023) · Journal of Inflammation Research · doi:10.2147/jir.s418334 · Cited by 16 · see citing works
Gordillo, G. M., Guda, P. R., Singh, K., Biswas, A., Abouhashem, A. S., Rustagi, Y., Sen, A., Kumar, M., Das, A., Ghatak, S., et al. (2022) · Molecular Therapy · doi:10.1016/j.ymthe.2022.11.003 · Cited by 16 · see citing works
Metabolism Serves as a Bridge Between Cardiomyocytes and Immune Cells in Cardiovascular Diseases
Hang, L., Zhang, Y., Zhang, Z., Jiang, Y., & Xia, L. (2024) · Cardiovascular Drugs and Therapy · doi:10.1007/s10557-024-07545-5 · Cited by 15 · see citing works
Human pancreatic islet miRNA-mRNA networks of altered miRNAs due to glycemic status
Karagiannopoulos, A., Esguerra, J. L. S., Pedersen, M. G., Wendt, A., Prasad, R. B., & Eliasson, L. (2022) · iScience · doi:10.1016/j.isci.2022.103995 · Cited by 14 · see citing works
Ikeda, T., Nakamura, K., Kida, T., & Oku, H. (2021) · Graefe s Archive for Clinical and Experimental Ophthalmology · doi:10.1007/s00417-021-05342-6 · Cited by 14 · see citing works
Exploring the role of miR-126 in diabetes and its complications: a comprehensive review
Rasmi, Y., Farahani, M., Asl, E. R., Barati, S., Naseri, N., & Ghoshal, K. (2025) · Diabetology & Metabolic Syndrome · doi:10.1186/s13098-025-01897-0 · Cited by 15 · see citing works
Chen, J., Luo, M., Xing, Z., Chen, Y., Peng, C., & Li, D. (2025) · Metabolism · doi:10.1016/j.metabol.2025.156153 · Cited by 13 · see citing works
Non-Coding RNAs in Breast Cancer: Diagnostic and Therapeutic Implications
Beňačka, R., Szabóová, D., Guľašová, Z., & Hertelyová, Z. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms26010127 · Cited by 12 · see citing works
Liu, H., Sun, C., Jiang, Y., Gao, R., Ying, Q., Li, X., Liu, H., Guo, J., & Li, M. (2024) · International Immunopharmacology · doi:10.1016/j.intimp.2024.113894 · Cited by 11 · see citing works
Rong, B., Jiang, H., Zhu, W., Yang, G., Zhou, X., Lyu, Z., Li, X., & Zhang, J. (2025) · Medicine · doi:10.1097/md.0000000000041613 · Cited by 11 · see citing works
Macrophage efferocytosis promotes inflammation resolution and accelerates wound healing
Gao, J., Zhu, D., Wang, J., Khan, M. I. U., Zhang, A., Wen, X., Li, Q., Jin, P., & Shen, C. (2026) · Communications Biology · doi:10.1038/s42003-026-10107-0 · Cited by 10 · see citing works
Wang, B., Huang, Y., Ding, Y., Chen, J., Chen, Y., Zhang, H., & Tan, Q. (2025) · Food Science & Nutrition · doi:10.1002/fsn3.70688 · Cited by 9 · see citing works
MicroRNA: unveiling novel mechanistic and theranostic pathways in diabetic cardiomyopathy
De, A., Sarkar, A., Banerjee, T., Bhowmik, R., Sar, S., Shaharyar, M. A., Karmakar, S., & Ghosh, N. (2025) · Frontiers in Pharmacology · doi:10.3389/fphar.2025.1613844 · Cited by 8 · see citing works
Monocytic microRNAs—Novel targets in atherosclerosis therapy
Euler, G., & Parahuleva, M. S. (2024) · British Journal of Pharmacology · doi:10.1111/bph.16367 · Cited by 7 · see citing works
Potential Effects of Hyperglycemia on SARS-CoV-2 Entry Mechanisms in Pancreatic Beta Cells
Michaels, T. M., Essop, M. F., & Joseph, D. E. (2024) · Viruses · doi:10.3390/v16081243 · Cited by 11 · see citing works
Apoptosis and Cell Clearance in Skin Wound Healing
Cleene, H. K. L. D., Keçeli, B. N., & Maschalidi, S. (2025) · Advances in experimental medicine and biology · doi:10.1007/978-3-031-92785-0_5 · Cited by 6 · see citing works
Kang, Y., Jin, Q. K., Zhou, M., Zheng, H., Li, D. R., Wang, X., Zhou, J., Lv, J., & Wang, Y. (2025) · Frontiers in Endocrinology · doi:10.3389/fendo.2025.1652402 · Cited by 6 · see citing works
Purnama, C. A., Meiliana, A., Barliana, M. I., Lestari, K., & Wijaya, A. (2024) · Journal of Obesity · doi:10.1155/2024/1424404 · Cited by 6 · see citing works
MicroRNA-181c-5p modulates phagocytosis efficiency in bone marrow-derived macrophages
Singh, S., Henderson, J., Patil, M., Dubey, P. K., Dubey, S., Kannappan, R., Zhang, J. J., & Krishnamurthy, P. (2022) · Inflammation Research · doi:10.1007/s00011-022-01539-5 · Cited by 6 · see citing works
Self-citationMao, Q., Ran, H., Hu, Q., He, S., Lu, Y., Li, H., Chai, Y.-M., Chu, Z.-Y., Xu, Q., Ding, W., et al. (2025) · World Journal of Diabetes · doi:10.4239/wjd.v16.i5.101473 · Cited by 5 · see citing works
He, Y., Hu, J., Ma, A., Du, P., Yang, M., Xiong, X., & Deng, Y. (2026) · Journal of Inflammation Research · doi:10.2147/jir.s566523 · Cited by 5 · see citing works
Ao, J., Zhang, X., & Zhu, D. (2024) · Cardiovascular Toxicology · doi:10.1007/s12012-024-09908-8 · Cited by 5 · see citing works
Zhou, J., & Gao, T. (2025) · Frontiers in Medicine · doi:10.3389/fmed.2025.1538867 · Cited by 5 · see citing works
Athira, S. V., Bhaskar, A., Misra, P., & Sibin, M. K. (2022) · Gene Reports · doi:10.1016/j.genrep.2022.101502 · Cited by 4 · see citing works
Jin, C., Shen, D., Zhuang, Z., zhang, Q., Wu, Y., Hu, Z., Zhang, K., Li, L., Gu, Z., Hu, Y., et al. (2026) · Cell Biomaterials · doi:10.1016/j.celbio.2026.100447 · Cited by 3 · see citing works
MicroRNAs and Efferocytosis: Implications for Diagnosis and Therapy
Hayat, S. M. G., Mahmoudi, A. A., Moadab, F., Safdarian, E., Navashenaq, J. G., & Rezaee, M. (2022) · Mini-Reviews in Medicinal Chemistry · doi:10.2174/1389557522666220330150937 · Cited by 3 · see citing works
Consequence of alcohol intoxication-mediated efferocytosis impairment
Brahadeeswaran, S., & Tamizhselvi, R. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1386658 · Cited by 3 · see citing works
Nemoto, W., Yamagata, R., Nakagawasai, O., Hoshi, T., Kobayashi, R., Watanabe, M., & Tan–No, K. (2025) · Biochemical Pharmacology · doi:10.1016/j.bcp.2025.116780 · Cited by 3 · see citing works
MicroRNAs for Diabetes Management: From Natural Bioactive Compounds to Nucleotide Networks
Chen, J., Luo, M., Qin, S., Peng, C., & Li, D. (2025) · Phytotherapy Research · doi:10.1002/ptr.70084 · Cited by 3 · see citing works
Retinal Pigment Epithelium Phagocytosis and Retinal Degenerative Diseases
Du, Y., & Xia, Y. (2025) · Aging and Disease · doi:10.14336/ad.2025.0542 · Cited by 3 · see citing works
Murzina, E., Dosenko, V., Drevytska, T., Bardova, K., Vozianova, S., * Corresponding Author: Elvina Murzina, 1. K. S., & Litus, O. (2021) · Journal of Medicine and Life · doi:10.25122/jml-2021-0115 · Cited by 3 · see citing works
Azhar, G., Verma, A., Patyal, P., Zhang, W., Sharma, S., Savary, P. E., Riklon, S., Kabua, P. M., McElfish, P. A., & Wei, J. Y. (2025) · PLoS ONE · doi:10.1371/journal.pone.0329321 · Cited by 2 · see citing works
Suppression of cardiac allograft vasculopathy by a macrophage efferocytosis receptor
Shah, S., Ananthakrishnan, A., DeBerge, M., Glinton, K. E., Jones, R. T. L., Filipp, M. E., Shen, I. R., Lockhart, J., Lantz, C. W., & Thorp, E. B. (2025) · American Journal of Transplantation · doi:10.1016/j.ajt.2025.08.026 · Cited by 2 · see citing works
Efferocytosis: a therapeutic strategy for diabetes and its vascular complications
Song, Y., Yuan, J., Li, Y., Liu, Y., & Qin, G. (2025) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2025.1641748 · Cited by 2 · see citing works
Ray, D., Loomis, S. J., Venkataraghavan, S., Zhang, J., Tin, A., Yu, B., Chatterjee, N., Selvin, E., & Duggal, P. (2024) · Diabetes · doi:10.2337/db23-0318 · Cited by 2 · see citing works
Therapeutic implication of targeting mitochondrial drugs designed for efferocytosis dysfunction
Liu, W.-T., Li, C.-Q., Fu, A.-N., Yang, H., Xie, Y., Yao, H., & Yi, G. (2024) · Journal of drug targeting · doi:10.1080/1061186x.2024.2386620 · Cited by 2 · see citing works
Chatterjee, B., & Thakur, S. S. (2025) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2025.1602320 · Cited by 2 · see citing works
Salarizadeh, N., Shojai, S., Pebdeni, A. B., Nojoki, F., Zargar, S. J., & Habibi-Rezaei, M. (2023) · Elsevier eBooks · doi:10.1016/b978-0-323-90222-9.00020-0 · Cited by 1 · see citing works
ADAM9 Genetic Variants and Their Role in Modulating Enzyme Activity in Diabetes and Metabolic Traits
Drobiova, H., Al‐Mulla, F., & Al-Temaimi, R. A. (2025) · Journal of Diabetes Research · doi:10.1155/jdr/5519447 · Cited by 1 · see citing works
Role of Perturbations of Epigenetic Processes in Cardiac Hypertrophy and Fibrotic Scarring
Duvey, B. K., Sharma, D., Mittal, V., & Sharma, A. (2025) · Current Cardiology Reviews · doi:10.2174/011573403x354902250708134633 · Cited by 1 · see citing works
Ramos-Regalado, L., Schoch, L., Alcover, S., Magaldi, M., Barriuso, I., Padró, T., Borrell-Pagés, M., Badimón, L., Zaragoza, C., & Vilahur, G. (2025) · Clínica e Investigación en Arteriosclerosis (English Edition) · doi:10.1016/j.artere.2026.500842 · Cited by 1 · see citing works
Ahmed, V. A., Rahman, H. S., Raheem, M. O. M., Othman, H. H., Algarawi, M., & Ibnaouf, K. H. (2024) · Natural Product Communications · doi:10.1177/1934578x241259377 · Cited by 1 · see citing works
Circulating miR-126-3p is a mechanistic biomarker for knee osteoarthritisPreprint
Wilson, T. G., Baghel, M., Kaur, N., Datta, I., Loveless, I. M., Potla, P., Mendez, D., Hansen, L. M., Baker, K. C., Lynch, T. S., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.05.31.596603 · Cited by 1 · see citing works
Investigation of differentially methylated microRNA genes in Type 2 diabetes
Alley, P.-J. (2017) · SUNScholar (Stellenbosch University)
- Authors
- Suresh Babu, S., Thandavarayan, R. A., Joladarashi, D., Jeyabal, P., Krishnamurthy, S., Bhimaraj, A., Youker, K. A., & Krishnamurthy, P.
- Affiliations
- Houston Methodist (US)
- University of Alabama at Birmingham (US)
- Corresponding author
- Krishnamurthy, Prasanna
- ORCID
- Venue
- Scientific Reports
- Published
- 2016-11-09
- Volume
- 6
- Issue
- 1
- Pages
- 36207-36207
- ISSN
- 2045-2322 (ISSN-L)
- PMC
- PMC5101812
- OpenAlex
- W2549443412
- Cited by
- 119
- References
- 49
- Citations by year
- 2026: 12 · 2025: 23 · 2024: 19 · 2023: 8 · 2022: 18 · 2021: 17 · 2020: 5 · 2019: 8 · 2018: 4 · 2017: 5
- FWCI
- 3.44
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Scientific Reports (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- American Heart Association (25860041, 15POST25710392, 16POST30780010, GRNT25860041)
- National Institutes of Health
- National Heart, Lung, and Blood Institute (R01HL116729)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac Fibrosis and Remodeling
- Keywords
- miR-126, efferocytosis, diabetes mellitus, macrophages, ADAM9, MERTK, high glucose, db/db mice, inflammation resolution, cardiac repair, myocardial injury
- MeSH terms
- RAW 264.7 Cells, THP-1 Cells, c-Mer Tyrosine Kinase, Proto-Oncogene Mas, Animals, Diabetes Mellitus, Experimental, Gene Expression Regulation, Glucose, Humans, Macrophages, Membrane Proteins, Phagocytosis, Apoptosis, 3' Untranslated Regions, Myocytes, Cardiac, MicroRNAs, Mice, ADAM Proteins
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