MiR-451 ameliorates red blood cell storage damage and macrophage polarizationmediated transfusion immunity by regulating the AMPK/mTOR signalling pathway.
MiR-451 mejora el daño de almacenamiento de glóbulos rojos y la inmunidad de transfusión mediada por la polarización de macrófagos mediante la regulación de la señalización AMPK/mTOR.
Palabras clave:
micro ARN miR-451, ATF2, proteínas quinasa activadas por AMP/mTOR, eritrocitos, conservación de la sangre, macrófagos
Resumen
Los glóbulos rojos (RBC) sufren una serie de cambios estructurales y funcionales durante el almacenamiento, y miR-451a es crucial para la homeostasis de los glóbulos rojos. MiR-451 puede mantener la homeostasis de los glóbulos rojos. Los factores inflamatorios y la expresión de miR-451 en sangre completa a diferentes tiempos de almacenamiento fueron detectados por ELISA y qRT-PCR. Las células THP-1 fueron inducida a macrófagos M0, luego el miR-451 imitador y el miR-451inhibidor, junto al factor de activación de transcrpción 2 (ATF2) se transfectaron a las células, seguido de la aplicación del compuesto C. Los macrófagos son entonces polarizados a tipo M1. Los marcadores de macrófagos fueron evaluados mediante citometría de flujo y Western blot. Los niveles de proteínas de la vía de la proteína quinasa-activada por monofosfato de adenosina (AMPK)/blanco de la rapamicina en mamíferos (mTOR) fueron detectados usando Western blot. Finalmente, se construyó un modelo de shock hemorrágico traumático en ratón , y se realizó transfusión sanguínea e inyección en vena de la cola de agomir-451. Los marcadores de macrófagos tipo M1 y los niveles de factores inflamatorios fueron examinados por citometría de flujo y ELISA, respectivamente. Cuando el tiempo de almacenamiento de sangre total humana fue de 21 y 35 días, la expresión de miR-451 disminuyó y el contenido de factor pro-inflamatorio aumentó. Cuando mir-451 se superexpresa, la expresión de citocinas proinflamatorias y marcadores de macrófagos de tipo M1 en las células THP-1 disminuye, los niveles de p-AMPK aumentan y los niveles de p-mTOR disminuyen. La superexpresión de ATF2 o la aplicación del compuesto C aumenta el factor proinflamatorio y los marcadores de macrófagos de tipo M1 en las células THP-1, y la expresión de p-AMPK y p-mTOR se revierte. La sobreexpresión de miR-451 también inhibe la la polarización M1 y la inflamación en macrófagos de ratones en shock. El miR-451 inhibe el ATF2 para regular la vía AMPK/mTOR, inhibe la polarización e inflamación por los macrófagos M1 y mejora el daño de al- macenamiento de RBC.
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Deswal B, Bagchi U, Santra MK, Garg M, Kapoor S. Inhibition of STAT3 by 2-Methoxyestradiol suppresses M2 polarization and protumoral functions of macrophages in breast cancer. BMC Cancer 2024;24(1):1129. https://doi.org/10.1186/s12885-024-12871-w.
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Chen X, Xie X, Xing Y, Yang X, Yuan Z, Wei Y. MicroRNA Dysregulation Associated with Red Blood Cell Storage. Transfus Med Hemother 2018;45(6):397-402. https://doi.org/10.1159/000489321.
Sarachana T, Kulkarni S, Atreya CD. Evaluation of small noncoding RNAs in ex vivo stored human mature red blood cells: changes in noncoding RNA levels correlate with storage lesion events. Transfusion 2015;55(11):2672-2683. https://doi.org/10.1111/trf.13235.
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Lennon CS, Cao H, Hall AM, Vickers MA, Barker RN. The red blood cell as a novel regulator of human B-cell activation. Immunology 2021;163(4):436-447. https://doi.org/10.1111/imm.13327.
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An Y, Yang Q. MiR-21 modulates the polarization of macrophages and increases the effects of M2 macrophages on promoting the chemoresistance of ovarian cancer. Life Sci 2020;242:117162. https://doi.org/10.1016/j.lfs.2019.117162.
Liu Q, Yang C, Wang S, Shi D, Wei C, Song J, et al. Wnt5a-induced M2 polarization of tumor-associated macrophages via IL -10 promotes colorectal cancer progression. Cell Commun Signal 2020; 18 (1):51.https://doi.org/10.1186/s12964-020-00557-2.
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Baig MS, Liu D, Muthu K, Roy A, Saqib U, Naim A, et al.Heterotrimeric complex of p38 MAPK, PKCδ, and TIRAP is required for AP1 mediated inflammatory response. Int Immunopharmacol 2017;48:211-218. https://doi.org/10.1016/j.intimp.2017. 04.028.
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Riley BC, Stansbury LG, Hasan RA, Hess JR. Transfusion of red blood cells ≥35 days old: A narrative review of clinical outcomes. Transfusion 2023;63(11):2179-2187. https://doi.org/10.1111/trf.17536.
Zuckerman J, Coburn N, Callum J, Mahar AL, Acuña SA, Guttman MP, et al. Association of perioperative red blood cell transfusions with all-cause and cancer-specific death in patients undergoing surgery for gastrointestinal cancer: Long-term outcomes from a population-based cohort. Surgery 2021;170(3):870-879. https://doi.org/10.1016/j.surg.2021.02.003.
Mangalmurti NS, Xiong Z, Hulver M, Ranganathan M, Liu XH, Oriss T,et al. Loss of red cell chemokine scavenging promotes transfusion-related lung inflammation. Blood 2009;113(5):1158-1166. https://doi.org/10.1182/blood-2008-07-166264.
Straat M, Böing AN, Tuip-De Boer A, Nieuwland R, Juffermans NP. Extracellular Vesicles from Red Blood Cell Products Induce a Strong Proinflammatory Host Response, Dependent on Both Numbers and Storage Duration. Transfus Med He mother 2016;43(4):302-305. https://doi.org/10.1159/000442681.
Nogueira D, Rocha S, Abreu E, Costa E, Santos-Silva A. Biochemical and cellular changes in leukocyte-depleted red blood cells stored for transfusion. Transfus Med Hemother 2015;42(1):46-51. https://doi.org/10.1159/000370140.
Wang F, Ling L, Yu D. MicroRNAs in β-thalassemia. Am J Med Sci 2021;362(1):5- 12. https://doi.org/10.1016/j.amjms.2021.02.011.
Kannan M, Atreya C. Differential profiling of human red blood cells during storage for 52 selected microRNAs. Transfusion 2010;50(7):1581-1588. https://doi.org/10.1111/j.1537-2995.2010.02585.x.
Guo JU, Agarwal V, Guo H, Bartel DP. Expanded identification and characterization of mammalian circular RNAs. Genome Biol 2014;15(7):409. https://doi.org/10.1186/s13059-014-0409-z.
Listowski MA, Heger E, Bogusławska DM, Machnicka B, Kuliczkowski K, Leluk J, Sikorski AF. microRNAs: fine tuning of erythropoiesis. Cell Mol Biol Lett 2013;18(1):34-46. https://doi.org/10.2478/s11658-012-0038-z.
Fang X, Shen F, Lechauve C, Xu P, Zhao G, Itkow J, et al. miR-144/451 represses the LKB1/AMPK/mTOR pathway to promote red cell precursor survival during recovery from acute anemia. Haematologica 2018;103(3):406-416. https://doi.org/10.3324/haematol.2017.177394.
Huang H, Zhu J, Fan L, Lin Q, Fu D, Wei B, Wei S. MicroRNA Profiling of Exosomes Derived from Red Blood Cell Units: Implications in Transfusion-Related Immunomodulation. Biomed Res Int 2019. https://doi.org/10.1155/2019/2045915.
Zhao K, Wang L, Li T, Zhu M, Zhang C, Chen L, et al. The role of miR-451 in the switching between proliferation and migration in malignant glioma cells: AMPK signaling, mTOR modulation and Rac1 activation required. Int J Oncol 2017;50(6):1989-1899. https://doi.org/10.3892/ijo.2017.3973.
Peng Z, Luo R, Xie T, Zhang W, Liu H, Wang W, et al. Erythrocyte Adenosine A2B Receptor-Mediated AMPK Activation: A Missing Component Counteracting CKD by Promoting Oxygen Delivery. J Am Soc Nephrol 2019;30(8):1413-1424. https://doi.org/10.1681/ASN.2018080862.
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Simcox J, Lamming DW. The central moTOR of metabolism. Dev Cell 2022;57(6):691-706. https://doi.org/10.1016/j.devcel.2022.02.024.
D’Alessandro A, Xia Y. Erythrocyte adaptive metabolic reprogramming under physiological and pathological hypoxia. Curr Opin Hematol 2020;27(3):155-162. https://doi.org/10.1097/MOH.0000000000000574.
Karafin MS, Francis RO. Impact of G6PD status on red cell storage and transfusion outcomes. Blood Transfus 2019;17(4):289- 295. https://doi.org/10.2450/2019.0092-19.
Silic-Benussi M, Sharova E, Ciccarese F, Cavallari I, Raimondi V, Urso L, et al. mTOR inhibition downregulates glucose-6-phosphate dehydrogenase and induces ROS-dependent death in T-cell acute lymphoblastic leukemia cells. Redox Biol 2022;51:102268. https://doi.org/10.1016/j.redox.2022.102268.
Nemkov T, Stefanoni D, Bordbar A, Issaian A, Palsson BO, Dumont LJ, et al. Blood donor exposome and impact of common drugs on red blood cell metabolism. JCI Insight 2021;6(3): e146175. https://doi.org/10.1172/jci.insight.146175.
Zhang Y, Xiang J, Sheng X, Zhu N, Deng S, Chen J,et al. GM-CSF enhanced the effect of CHOP and R-CHOP on inhibiting diffuse large B-cell lymphoma progression via influencing the macrophage polarization. Cancer Cell Int 2021;21(1):141. https://doi.org/10.1186/s12935-021-01838-7.
Deswal B, Bagchi U, Santra MK, Garg M, Kapoor S. Inhibition of STAT3 by 2-Methoxyestradiol suppresses M2 polarization and protumoral functions of macrophages in breast cancer. BMC Cancer 2024;24(1):1129. https://doi.org/10.1186/s12885-024-12871-w.
Li ZZ, Wang XX, Ma L, Wang H, Xu JM, Zhou XF, et al. Influence of different erythrocyte storage times on the macrophage response in haemorrhagic shock mice. J Int Med Res 2020;48(8):300060520947872. https://doi.org/10.1177/0300060520947872.
Roussel C, Morel A, Dussiot M, Marin M, Colard M, Fricot-Monsinjon A, et al. Rapid clearance of storage-induced microerythrocytes alters transfusion recovery. Blood 2021;137(17):2285-2298. https://doi.org/10.1182/blood.2020008563.
Sut C, Tariket S, Chou ML, Garraud O, Laradi S, Hamzeh-Cognasse H, et al. Duration of red blood cell storage and inflammatory marker generation. Blood Transfus 2017;15(2):145-152. https://doi.org/10.2450/2017.0343-16.
Obrador R, Musulin S, Hansen B. Red blood cell storage lesion. J Vet Emerg Crit Care (San Antonio) 2015;25(2):187-199. https://doi.org/10.1111/vec.12252.
Chen X, Xie X, Xing Y, Yang X, Yuan Z, Wei Y. MicroRNA Dysregulation Associated with Red Blood Cell Storage. Transfus Med Hemother 2018;45(6):397-402. https://doi.org/10.1159/000489321.
Sarachana T, Kulkarni S, Atreya CD. Evaluation of small noncoding RNAs in ex vivo stored human mature red blood cells: changes in noncoding RNA levels correlate with storage lesion events. Transfusion 2015;55(11):2672-2683. https://doi.org/10.1111/trf.13235.
Mitchell A, Gray W, Rooney K, Mohamed I, Quyyumi A, Roback J, Searles C. Abstract 443: Red Blood Cell Microparticles Mediate Transfer of Functional miR-451 to Endothelial Cells in vitro. Arteriosclerosis, Thrombosis, and Vascular Biology. 2015; 35(Suppl_1). https://doi.org/10.1161/atv b.35.suppl_1.443
Zhang J, Zhang D, Zhao J, Zheng W. MiR-33a-5p in stored red blood cells regulates genes of innate immune response and promotes inflammation. Aging (Albany NY) 2024;16(12):10239-10251. https://doi.org/10.18632/aging.205925.
McFaul SJ, Corley JB, Mester CW, Nath J. Packed blood cells stored in AS-5 become proinflammatory during storage. Transfusion 2009;49(7):1451-1460. https://doi.org/10.1111/j.1537-2995.2009.02158.x.
Lennon CS, Cao H, Hall AM, Vickers MA, Barker RN. The red blood cell as a novel regulator of human B-cell activation. Immunology 2021;163(4):436-447. https://doi.org/10.1111/imm.13327.
Pradhan P, Vijayan V, Gueler F, Immenschuh S. Interplay of Heme with Macrophages in Homeostasis and Inflammation. Int J Mol Sci. 2020;21(3):740. https://doi.org/10.3390/ijms21030740
Antonelou MH, Seghatchian J. Insights into red blood cell storage lesion: Toward a new appreciation. Transfus Apher Sci 2016;55(3):292-301. https://doi.org/10.1016/j.transci.2016.10.019.
Wang F, Liu YH, Zhang T, Gao J, Xu Y, Xie GY, et al. Aging-associated changes in CD47 arrangement and interaction with thrombospondin-1 on red blood cells visualized by super-resolution imaging. Aging Cell 2020;19(10):e13224. https://doi.org/10.1111/acel.13224.
Locati M, Curtale G, Mantovani A. Diversity, Mechanisms, and Significance of Macrophage Plasticity. Annu Rev Pathol 2020;15:123-147. https://doi.org/10.1146/annurev-pathmechdis-012418-012718.
An Y, Yang Q. MiR-21 modulates the polarization of macrophages and increases the effects of M2 macrophages on promoting the chemoresistance of ovarian cancer. Life Sci 2020;242:117162. https://doi.org/10.1016/j.lfs.2019.117162.
Liu Q, Yang C, Wang S, Shi D, Wei C, Song J, et al. Wnt5a-induced M2 polarization of tumor-associated macrophages via IL -10 promotes colorectal cancer progression. Cell Commun Signal 2020; 18 (1):51.https://doi.org/10.1186/s12964-020-00557-2.
Chen L, Gao B, Zhang Y, Lu H, Li X, Pan L, et al. PAR2 promotes M1 macrophage polarization and inflammation via FOXO1 pathway. J Cell Biochem 2019;120(6):9799-9809. https://doi.org/10.1002/jcb.28260.
Salvagno GL, Sanchis-Gomar F, Picanza A, Lippi G. Red blood cell distribution width: A simple parameter with multiple clinical applications. Crit Rev Clin Lab Sci 2015;52(2):86-105. https://doi.org/10.3109/10408363.2014.992064.
Baig MS, Liu D, Muthu K, Roy A, Saqib U, Naim A, et al.Heterotrimeric complex of p38 MAPK, PKCδ, and TIRAP is required for AP1 mediated inflammatory response. Int Immunopharmacol 2017;48:211-218. https://doi.org/10.1016/j.intimp.2017. 04.028.
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Publicado
2025-08-31
Cómo citar
Wang, X., Chen, X., Zhou, H., Chen, L., Wang, H., & Qiu, H. (2025). MiR-451 ameliorates red blood cell storage damage and macrophage polarizationmediated transfusion immunity by regulating the AMPK/mTOR signalling pathway.: MiR-451 mejora el daño de almacenamiento de glóbulos rojos y la inmunidad de transfusión mediada por la polarización de macrófagos mediante la regulación de la señalización AMPK/mTOR. Investigación Clínica, 66(3), 282-300. https://doi.org/10.54817/IC.v66n3a05
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