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Antagonism of miR-33 in mice promotes reverse cholesterol transport and regression of atherosclerosis
Open accessAbstract
Plasma HDL levels have a protective role in atherosclerosis, yet clinical therapies to raise HDL levels have remained elusive. Recent advances in the understanding of lipid metabolism have revealed that miR-33, an intronic microRNA located within the SREBF2 gene, suppresses expression of the cholesterol transporter ABC transporter A1 (ABCA1) and lowers HDL levels. Conversely, mechanisms that inhibit miR-33 increase ABCA1 and circulating HDL levels, suggesting that antagonism of miR-33 may be atheroprotective. As the regression of atherosclerosis is clinically desirable, we assessed the impact of miR-33 inhibition in mice deficient for the LDL receptor (Ldlr-/- mice), with established atherosclerotic plaques. Mice treated with anti-miR33 for 4 weeks showed an increase in circulating HDL levels and enhanced reverse cholesterol transport to the plasma, liver, and feces. Consistent with this, anti-miR33-treated mice showed reductions in plaque size and lipid content, increased markers of plaque stability, and decreased inflammatory gene expression. Notably, in addition to raising ABCA1 levels in the liver, anti-miR33 oligonucleotides directly targeted the plaque macrophages, in which they enhanced ABCA1 expression and cholesterol removal. These studies establish that raising HDL levels by anti-miR33 oligonucleotide treatment promotes reverse cholesterol transport and atherosclerosis regression and suggest that it may be a promising strategy to treat atherosclerotic vascular disease.
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“Furthermore, macrophages within the atherosclerotic lesions of these mice exhibit an anti-inflammatory phenotype characterized by enhanced cholesterol efflux, which leads to a reduction in foam cell formation.”
From Critical Role of microRNA-33a/b in Cardiovascular and Metabolic Disease: Molecular Mechanisms and Therapeutic Perspectives (2026) · cites this paper as [21]
In the citing paper
“Inhibition or genetic ablation of miR-33a has been shown to either promote the regression of atherosclerosis or prevent its formation in mouse models, such as LDL receptor-deficient or apoprotein E (ApoE)-deficient mice, conferring resistance to the disease 21 - 23) .”
From Critical Role of microRNA-33a/b in Cardiovascular and Metabolic Disease: Molecular Mechanisms and Therapeutic Perspectives (2026) · cites this paper as [21]
In the citing paper
“Moreover, the effect of miR-33 deletion in macrophages is not as simple as the shift from the M1 to M2 phenotype reported previously.19”
From MicroRNA‐33 Deficiency Reduces the Progression of Atherosclerotic Plaque in ApoE −/− Mice (2012) · cites this paper as [19]
In the citing paper
“Moreover, antisense inhibition of miR-33 resulted in a regression of the atherosclerotic plaque volume in LDL-receptor-deficient mice.19”
From MicroRNA‐33 Deficiency Reduces the Progression of Atherosclerotic Plaque in ApoE −/− Mice (2012) · cites this paper as [19]
In the citing paper
“In any case, the effect of miR-33 deletion in macrophages is not as simple as a shift from the M1 to the M2 phenotype, as described in a previous report.19”
From MicroRNA‐33 Deficiency Reduces the Progression of Atherosclerotic Plaque in ApoE −/− Mice (2012) · cites this paper as [19]
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BackgroundMicroRNAs and Lipoprotein Metabolism
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“MiR33a was also closely related to the lipid metabolism (inhibition of ABCA1 and cholesterol efflux, inhibition of HDL production) [18].”
BackgroundLDL delivery of microbial small RNAs drives atherosclerosis through macrophage TLR8
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BackgroundMicroRNAs and Cardiovascular Disease
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BackgroundAge-Related Impairments in Immune Cell Efferocytosis and Autophagy Hinder Atherosclerosis Regression
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Self-citationMicroRNAs in Macrophages: Regulators of Activation and Function
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MicroRNAs in Obesity-Associated Disorders: The Role of Exercise Training
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MicroRNA-126 participates in lipid metabolism in mammary epithelial cells
Chu, M., Zhao, Y. M., Feng, Y., Zhang, H., Liu, J., Cheng, M. Y., Li, L., Shen, W., Cao, H., Li, Q., et al. (2017) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2017.05.039 · Cited by 32
“miR-33a and miR-33b regulate cholesterol metabolism (Rayner et al., 2011; Marquart et al., 2010; Gerin et al., 2010; Horie et al., 2010; NajafiShoushtari et al., 2010); miR-27b binds to the 30-UTR of several lipid-associated genes: heparan sulfate N-deacetylase/N-sulfotransferase 1 (NDST1), angiopoietin-like 3 (ANGPTL…”
BackgroundTranscriptome Profiling in Systems Vascular Medicine
Xu, S. (2017) · Frontiers in Pharmacology · doi:10.3389/fphar.2017.00563 · Cited by 30
MicroRNAs in Cardiovascular Health: From Order to Disorder
Karunakaran, D., & Rayner, K. J. (2013) · Endocrinology · doi:10.1210/en.2013-1299 · Cited by 26
“Inhibition of miR-33 was shown to induce the expression of ABCA1 not only in the liver, where it increased circulating HDL levels but also in atherosclerotic plaque macrophages where it promoted cholesterol removal from the plaque and decreased lesion size (22).”
BackgroundSelf-citationJan, A., Karasinska, J. M., Kang, M. H., de Haan, W., Ruddle, P., Kaur, A., Connolly, C., Leavitt, B. R., Sorensen, P. H., & Hayden, M. R. (2015) · Neuroscience Letters · doi:10.1016/j.neulet.2015.05.007 · Cited by 28
Perdoncin, M., Konrad, A., Wyner, J. R., Lohana, S., Pillai, S. S., Pereira, D. G., Lakhani, H. V., & Sodhi, K. (2021) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2021.756499 · Cited by 39
Epigenetics and cardiovascular risk in childhood
Martino, F., Magenta, A., Pannarale, G., Martino, E., Zanoni, C., Perla, F. M., Puddu, P. E., & Barillà, F. (2016) · Journal of Cardiovascular Medicine · doi:10.2459/jcm.0000000000000334 · Cited by 32
Huang, S., Lv, Z., Deng, Q., Lü, L., Yang, B., Feng, J. C., Wu, T., Zhang, X., & Cheng, J. (2015) · The Tohoku Journal of Experimental Medicine · doi:10.1620/tjem.237.227 · Cited by 27
Lin, Y.-W., Liu, P.-S., Adhikari, N., Hall, J. L., & Wei, L. (2014) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2014.12.009 · Cited by 32
“Other studies showed that MiR-33 also reduces the expression of ABCA1 and ABCG1[32, 33].”
BackgroundMicroRNAs in Liver Health and Disease
Hsu, S., & Ghoshal, K. (2013) · Current Pathobiology Reports · doi:10.1007/s40139-012-0005-4 · Cited by 32
“Micromanaging” metabolic syndrome
Ramírez, C. M., Goedeke, L., & Fernandez-Hernando, C. F. (2011) · Cell Cycle · doi:10.4161/cc.10.19.17558 · Cited by 24
田中, 義., Liu, C., Feng, J., Li, J., & Fan, Z. (2020) · Experimental and Therapeutic Medicine · doi:10.3892/etm.2020.8915 · Cited by 22
High serum CRP influences myocardial miRNA profiles in ischemia-reperfusion injury of rat heart
Kim, E. N., Kim, C. J., Kim, S. R., Song, J.-A., Choe, H., Kim, K., Choi, J. S., & Oh, S. J. (2019) · PLoS ONE · doi:10.1371/journal.pone.0216610 · Cited by 27
Comparison of different chemically modified inhibitors of miR-199b in vivo
Duygu, B., Juni, R. P., Ottaviani, L., Bitsch, N. J. J. E., Wit, J. B. M., Windt, L. J. D., & Martins, P. A. D. C. (2018) · Biochemical Pharmacology · doi:10.1016/j.bcp.2018.11.013 · Cited by 28
Nguyen, M.-A., Karunakaran, D., Geoffrion, M., Cheng, H. S., Tandoc, K. V., Matic, L. P., Hedin, U., Mäegdefessel, L., Fish, J. E., & Rayner, K. J. (2017) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.117.309795 · Cited by 244
“MVBs release exosomes into the extracellular environment by directly fusing with the plasma membrane.(6,7) Microvesicles, on the other hand, are larger vesicles (with a diameter of 200 nm to 1 μm) that are produced by direct budding from the cell plasma membrane as shedding vesicles.”
Self-citationNoncoding RNAs: New Players in Pulmonary Medicine and Sarcoidosis
Salamó, O., Mortaz, E., & Mirsaeidi, M. S. (2017) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2017-0196tr · Cited by 26
Jenkins, N. T., Padilla, J., Thorne, P. K., Martin, J. S., Rector, R. S., Davis, J. W., & Laughlin, M. H. (2014) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01233.2013 · Cited by 28
“The gene Srebf2, another novel proatherogenic marker, contains an intronic region that encodes miR33, which suppresses cholesterol transport, ultimately leading to increased risk for atherosclerosis (57).”
BackgroundRadonjić, M., Wielinga, P. Y., Wopereis, S., Kelder, T., Goelela, V. S., Verschuren, L., Toet, K. H., van Duyvenvoorde, W., der Vat, B. J. C. V. D. W.-V., Stroeve, J. H. M., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0056122 · Cited by 22
“On the other hand, it is also possible that restoration of macrovascular damage is a relatively slow process which requires either more time to regress as reported [41], or pharmacotherapy [37,42].”
BackgroundmicroRNA-33 controls hunger signaling in hypothalamic AgRP neurons
Price, N. L., Fernández-Tussy, P., Varela, L., Cardelo, M. P., Shanabrough, M., Aryal, B., de Cabo, R., Suárez, Y., Horvath, T. L., & Fernández-Hernando, C. (2024) · Nature Communications · doi:10.1038/s41467-024-46427-0 · Cited by 25
“Notably, pharmacological inhibition of miR-33 elevates hepatic ABCA1 expression, thereby increasing circulating HDL-C and attenuating the progression of atherosclerosis, highlighting the therapeutic potential of miR-33 inhibitors for the treatment of cardiovascular disease 9,10 .”
BackgroundGenomic Variants and Multilevel Regulation of ABCA1, ABCG1, and SCARB1 Expression in Atherogenesis
Rozhkova, A. V., Dmitrieva, V. G., Nosova, E. V., Dergunov, A. D., Limborska, S. A., & Dergunova, L. V. (2021) · Journal of Cardiovascular Development and Disease · doi:10.3390/jcdd8120170 · Cited by 39
“An increase in circulating HDL levels and enhanced reverse cholesterol transport to the plasma, liver, and feces was detected only in some studies [216,228].”
BackgroundMicroRNAs in Cardiovascular Disease
Παπαγεωργίου, Ν., Tsalamandris, S., Giolis, A., & Tousoulis, D. (2015) · Cardiology in Review · doi:10.1097/crd.0000000000000078 · Cited by 27
“More specifically, treatment of intralesional macrophages with anti-miR-33 downregulated several proinflammatory genes, including TNFα and toll-like receptor 6 gene.(111)”
BackgroundATP-binding cassette transporter A1
Eck, M. V. (2014) · Current Opinion in Lipidology · doi:10.1097/mol.0000000000000088 · Cited by 35
“Previous studies have shown that antimiR-33 therapy promotes reverse cholesterol transport and induces rapid regression of atherosclerosis in LDL receptor knockout mice with established atherosclerotic lesions [32].”
BackgroundWalker, A. K., & Näär, A. M. (2012) · Clinical Lipidology · doi:10.2217/clp.11.67 · Cited by 25
Kim, S., Lee, W., & Cho, K. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22157791 · Cited by 24
“Endothelial dysfunction causes a lack of nitric oxide (NO), which can modulate leukocyte adhesion to the arterial walls [2].”
BackgroundPromises of Nanotherapeutics in Obesity
Ash, G. I., Kim, D., & Choudhury, M. (2019) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2019.04.004 · Cited by 33
“Whereas, administration of anti-miR-33 increases HDL-C and cholesterol efflux [70–72] while reducing atherosclerotic plaque [75, 76].”
BackgroundShao, F., Wang, X., Yu, J., Shen, K., Qi, C., & Gu, Z. (2019) · British Poultry Science · doi:10.1080/00071668.2018.1564242 · Cited by 27
“The miR-33 inhibition reduced lipid accumulation in arterial plaques and raised circulating HDL levels (Rayner et al. 2011b).”
BackgroundMicroRNAs regulating apolipoprotein B-containing lipoprotein production
Zhou, L., Irani, S., Sirwi, A., & Hussain, M. M. (2016) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2016.02.020 · Cited by 26
Strategies to Antagonize miRNA Functions In Vitro and In Vivo
Baigude, H., & Rana, T. M. (2014) · Nanomedicine · doi:10.2217/nnm.14.162 · Cited by 23
MicroRNAs and High-Density Lipoprotein Cholesterol Metabolism
Ono, K., Horie, T., Nishino, T., Baba, O., Kuwabara, Y., & Kimura, T. (2015) · International Heart Journal · doi:10.1536/ihj.15-019 · Cited by 24
MicroRNAs in brain cholesterol metabolism and their implications for Alzheimer's disease
Yoon, H., Flores, L. F., & Kim, J. (2016) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2016.04.020 · Cited by 23
van Ingen, E., Foks, A. C., Kröner, M. J., Kuiper, J., Quax, P. H. A., Bot, I., & Nossent, A. Y. (2019) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2019.09.021 · Cited by 21
Koyama, S., Horie, T., Nishino, T., Baba, O., Sowa, N., Miyasaka, Y., Kuwabara, Y., Nakao, T., Nishiga, M., Nishi, H., et al. (2019) · Journal of the American Heart Association · doi:10.1161/jaha.119.012609 · Cited by 23
“These favorable changes in serum cholesterol profile or cholesterol reverse transport reduced atherosclerotic plaque progression in mice.(11,14) These observations suggest miR-33 as a potential therapeutic target of atherosclerosis.”
BackgroundThe role of HDL in plaque stabilization and regression
Feig, J. E., Feig, J. L., & Dangas, G. (2016) · Coronary Artery Disease · doi:10.1097/mca.0000000000000408 · Cited by 25
Athyros, V., Katsiki, N., Karagiannis, A., & Mikhailidis, D. (2014) · Current pharmaceutical design · doi:10.2174/1381612820666140620115756 · Cited by 23
“Injection with anti-miR-33 antisense oligonucleotides in LDLR -/chow-fed mice showed that the levels of HDL-C and the degree of cellular cholesterol efflux increased, while atherosclerotic plaque size and macrophage content of the plaque significantly decreased vs both placebo and non-miR-33a targeting antisense oligo…”
BackgroundAdvances in miRNA research: Unraveling the complexities of gene regulation
Zheng, J., Zhang, G., & Ren, L. (2025) · Animal Models and Experimental Medicine · doi:10.1002/ame2.70076 · Cited by 23
“Furthermore, antagonism of miR-33 in mice promotes reverse cholesterol transport and regression of atherosclerosis, 109 underscoring the crucial role of miRNAs in regulating lipid transport.”
Zhao, L., Huang, J., Zhu, Y., Han, S., Qing, K. X., Wang, J., & Feng, Y. (2019) · Perfusion · doi:10.1177/0267659119850685 · Cited by 26
miR-146b Inhibits Glucose Consumption by Targeting IRS1 Gene in Porcine Primary Adipocytes
Zhu, Y., Chen, T., Xiong, J., Wu, D., Xi, Q., Luo, J., Sun, J., & Zhang, Y. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19030783 · Cited by 24
“Studies have shown that miRNAs are key regulators of the cell cycle [33], adipocyte differentiation [34,35], adipogenesis [36,37], cholesterol and lipid regulation [38,39], insulin signaling and glucose homeostasis [40].”
BackgroundSud, N., Taher, J., & Su, Q. (2015) · Drug Development Research · doi:10.1002/ddr.21269 · Cited by 25
“Short term treatment with ASOs against miR-33 that are 20 fluoro/methoxyethyl- modified increased circulation level of HDL-cholesterol by enhancing RCT to the plasma, liver, and feces, and reduced plaque size and lipid content in mice [Rayner et al., 2011b].”
BackgroundRecent Advances in Understanding of NASH: MicroRNAs as Both Biochemical Markers and Players
Vincent, R. J., & Sanyal, A. J. (2014) · Current Pathobiology Reports · doi:10.1007/s40139-014-0049-8 · Cited by 21
Vickers, K. C., & Moore, K. J. (2013) · Circulation Research · doi:10.1161/circresaha.113.302732 · Cited by 20
Self-citationMacrophages, dendritic cells, and regression of atherosclerosis
Feig, J. E., & Feig, J. L. (2012) · Frontiers in Physiology · doi:10.3389/fphys.2012.00286 · Cited by 22
miR-33 deletion in hepatocytes attenuates MASLD-MASH-HCC progression
Fernández-Tussy, P., Cardelo, M. P., Zhang, H., Sun, J., Price, N. L., Boutagy, N. E., Goedeke, L., Cadena-Sandoval, M., Xirouchaki, C. E., Brown, W., et al. (2024) · JCI Insight · doi:10.1172/jci.insight.168476 · Cited by 21
Self-citationThe role of non-coding RNA network in atherosclerosis
Yuan, Y., Xu, L., Geng, Z., Liu, J., Zhang, L., Wu, Y., He, D., & Qu, P. (2020) · Life Sciences · doi:10.1016/j.lfs.2020.118756 · Cited by 27
Vahdat‐Lasemi, F., Mahjoubin‐Tehran, M., Aghaee‐Bakhtiari, S. H., Jalili, A., Jaafari, M. R., & Sahebkar, A. (2019) · Drug Discovery Today · doi:10.1016/j.drudis.2019.04.007 · Cited by 24
MicroRNAs in Ischemic Heart Disease
Lima, J., Batty, J. A., Sinclair, H., & Kunadian, V. (2016) · Cardiology in Review · doi:10.1097/crd.0000000000000114 · Cited by 24
Aberrant expression of plasma microRNA-33a in an atherosclerosis-risk group
Kim, S. H., Kim, G. J., Umemura, T., Lee, S. G., & Cho, K. J. (2016) · Molecular Biology Reports · doi:10.1007/s11033-016-4082-z · Cited by 24
miRiaD: A Text Mining Tool for Detecting Associations of microRNAs with Diseases
Gupta, S., ROSS, K. E., Tudor, C. O., Wu, C. H., Schmidt, C. J., & Vijay‐Shanker, K. (2016) · Journal of Biomedical Semantics · doi:10.1186/s13326-015-0044-y · Cited by 22
“This category includes miR-gene targeting events, as well as regulation of processes such apoptosis [13], metastasis [14], or cholesterol transport [15] by miRs.”
BackgroundMissing link between microRNA and prostate cancer
Gill, B. S., Alex, J. M., Navgeet, & Kumar, S. (2016) · Tumor Biology · doi:10.1007/s13277-016-4900-x · Cited by 20
“9 miR-33 Inhibitor Preclinical Therapeutics [174] Tumor Biol.”
BackgroundDetection of miR-33 Expression and the Verification of Its Target Genes in the Fatty Liver of Geese
Zheng, Y., Jiang, S., Zhang, Y., Zhang, R., & Gong, D. (2015) · International Journal of Molecular Sciences · doi:10.3390/ijms160612737 · Cited by 19
“Accordingly, the HDL levels in plasma can either decrease or increase [21].”
BackgroundGanjali, S., Momtazi‐Borojeni, A. A., Banach, M., Kovanen, P. T., Gotto, A. M., & Sahebkar, A. (2017) · Drug Discovery Today · doi:10.1016/j.drudis.2017.09.014 · Cited by 21
MicroRNA-33 Inhibits Adaptive Thermogenesis and Adipose Tissue Beiging
Afonso, M. S., Verma, N., van Solingen, C., Cyr, Y., Sharma, M., Perie, L., Corr, E. M., Schlegel, M., Shanley, L. C., Peled, D., et al. (2021) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/atvbaha.120.315798 · Cited by 21
Self-citation
Metadata
- Authors
- Rayner, K. J., Sheedy, F. J., Esau, C. C., Hussain, F. N., Temel, R. E., Parathath, S., van Gils, J. M., Rayner, A. J., Chang, A. N., Suarez, Y., Fernandez-Hernando, C., Fisher, E. A., & Moore, K. J.
- Affiliations
- New York University (US)
- Regulus Therapeutics (United States) (US)
- Wake Forest University Health Sciences (US)
- Corresponding author
- Moore, Kathryn J.
- ORCID
- Venue
- Journal of Clinical Investigation
- Published
- 2011-07-01
- Volume
- 121
- Issue
- 7
- Pages
- 2921-2931
- ISSN
- 0021-9738 (ISSN-L)
- PMC
- PMC3223840
- OpenAlex
- W2168964544
- Cited by
- 690
- References
- 0
- Citations by year
- 2026: 14 · 2025: 27 · 2024: 21 · 2023: 35 · 2022: 41 · 2021: 36 · 2020: 38 · 2019: 43 · 2018: 45 · 2017: 48 · 2016: 63 · 2015: 62 · 2014: 82 · 2013: 71 · 2012: 50
- FWCI
- 70.78
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Clinical Investigation (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Leiden Repository (Leiden University) (submittedVersion)
- Funders
- National Institutes of Health (5r00hl088528-05)
- Canadian Institutes of Health Research
- National Institute on Aging (R01AG020255)
- National Heart, Lung, and Blood Institute (R01HL084312, R00-HL088528, K99HL088528, P01HL098055, R01HL108182, R01HL107953)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Cholesterol and Lipid Metabolism
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
- Life Sciences › Immunology and Microbiology › Immunology › Atherosclerosis and Cardiovascular Diseases
- Keywords
- miR-33, reverse cholesterol transport, HDL cholesterol, atherosclerosis regression, ABCA1, SREBF2, LDL receptor-deficient mice, atherosclerotic plaque, plaque macrophages, cholesterol efflux, plaque stability, inflammation
- MeSH terms
- Animals, Humans, Cholesterol, HDL, Liver, Macrophages, Mice, Inbred C57BL, Random Allocation, Receptors, LDL, Gene Expression, Mice, Knockout, ATP-Binding Cassette Transporters, MicroRNAs, Atherosclerosis, Lipid Metabolism, Mice, ATP Binding Cassette Transporter 1
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