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REVIEW

Long non-coding RNAs: A trained immunity perspective

Bikesh Kumar Nirala1 ,  Gauri Shishodia2 ,  Praveen Kumar3 ,  Ravi Shankar Singh4*
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1 Department of Pediatrics, School of Medicine, Emory University, Atlanta, Georgia, United States of America
2 Department of Biochemistry, UT Southwestern Medical Centre, Dallas, Texas, United States of America
3 Department of Neurology, UT Southwestern Medical Centre, Dallas, Texas, United States of America
4 Department of Pathology, Division of Microbiology and Immunology University of Utah, Emma Eccles Jones Medical Research Building, Salt Lake City, Utah, United States of America
GPD 2024, 3(2), 2791 https://doi.org/10.36922/gpd.2791
Submitted: 20 January 2024 | Accepted: 29 April 2024 | Published: 4 June 2024
© 2024 by the Author(s). This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution 4.0 International License ( https://creativecommons.org/licenses/by/4.0/ )
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Abstract

The conventional understanding of immunological memory within adaptive immunity has faced recent challenges, paving the way for a novel concept known as “trained immunity.” This phenomenon revolves around the epigenetic and metabolic reprogramming of cells as its central components. A growing body of evidence suggests that long non-coding RNAs (lncRNAs) play a crucial role in regulating immune cell development, function, and response to various diseases. Through intricate protein-protein interactions and interactions with DNA and RNA, lncRNAs significantly contribute to the modulation of immune processes. However, our comprehension of the involvement of lncRNAs in trained immunity is still in its early stages. This review delves into the recent advancements in lncRNA research, focusing on their diverse functions in immune cell development, host-pathogen interactions, potential processes, and their biological significance in trained immunity. Special attention is given to the role of lncRNAs in altering chromatin structure, orchestrating chromosomal looping, and driving metabolic reprogramming within cells.

Keywords
Long non-coding RNA
Trained immunity
Metabolic reprogramming
Epigenetics
Funding
None.
Conflict of interest
The authors declare that they have no competing interests.
References
  1. Ma L, Bajic VB, Zhang Z. On the classification of long non-coding RNAs. RNA Biol. 2013;10(6):925-33. doi: 10.4161/rna.24604

 

  1. Van Bakel H, Nislow C, Blencowe BJ, Hughes TR. Most “dark matter” transcripts are associated with known genes. PLoS Biol. 2010;8(5):e1000371. doi: 10.1371/journal.pbio.1000371

 

  1. Kazimierczyk M, Wrzesinski J. Long Non-Coding RNA Epigenetics. Int J Mol Sci. 2021;22(11):6166. doi: 10.3390/ijms22116166

 

  1. Jain S, Thakkar N, Chhatai J, Pal Bhadra M, Bhadra U. Long non-coding RNA: Functional agent for disease traits. RNA Biol. 2017;14(5):522-535. doi: 10.1080/15476286.2016.1172756

 

  1. Zhang Y, Cao X. Long noncoding RNAs in innate immunity. Cell Mol Immunol. 2016;13(2):138-147. doi: 10.1038/cmi.2015.68

 

  1. St Laurent G, Wahlestedt C, Kapranov P. The Landscape of long noncoding RNA classification. Trends Genet. 2015;31:239-251. doi: 10.1016/j.tig.2015.03.007

 

  1. Iyer MK, Niknafs YS, Malik R, et al. The landscape of long noncoding RNAs in the human transcriptome. Nat Genet. 2015;47(3):199-208. doi: 10.1038/ng.3192

 

  1. Ahmad I, Valverde A, Ahmad F, Naqvi AR. Long noncoding RNA in myeloid and lymphoid cell differentiation, polarization and function. Cells. 2020;9(2):269. doi: 10.3390/cells9020269

 

  1. Matsui M, Corey DR. Non-coding RNAs as drug targets. Nat Rev Drug Discov. 2017;16(3):167-179. doi: 10.1038/nrd.2016.117

 

  1. Yi K, Zhang Y, Wang Y, et al. Long noncoding RNA and its role in virus infection and pathogenesis. Front Biosci (Landmark Ed). 2019;24:777-789. doi: 10.2741/4750

 

  1. Ponjavic J, Ponting CP, Lunter G. Functionality or transcriptional noise? Evidence for selection within long noncoding RNAs. Genome Res. 2007;17(5):556-565. doi: 10.1101/gr.6036807

 

  1. Pegueroles C, Iraola-Guzman S, Chorostecki U, Ksiezopolska E, Saus E, Gabaldon T. Transcriptomic analyses reveal groups of co-expressed, syntenic lncRNAs in four species of the genus Caenorhabditis. RNA Biol. 2019;16(3):320-329. doi: 10.1080/15476286.2019.1572438

 

  1. Hadjicharalambous MR, Lindsay MA. Long Non-coding RNAs and the innate immune response. Noncoding RNA. 2019;5(2):34. doi: 10.3390/ncrna5020034

 

  1. Wang Z, Zheng Y. lncRNAs regulate innate immune responses and their roles in macrophage polarization. Mediators Inflamm. 2018;2018:8050956. doi: 10.1155/2018/8050956

 

  1. Feng S, Ji G, Ma J, Wang Z, Zhao Y, Tao C. Long noncoding RNA GAS5 does not regulate HBV replication. J Med Virol. 2019;91(11):1949-1959. doi: 10.1002/jmv.25547

 

  1. Fanucchi S, Fok ET, Dalla E, et al. Publisher Correction: Immune genes are primed for robust transcription by proximal long noncoding RNAs located in nuclear compartments. Nat Genet. 2019;51(2):364. doi: 10.1038/s41588-018-0341-3

 

  1. Han P, Chang CP. Long non-coding RNA and chromatin remodeling. RNA Biol. 2015;12(10):1094-1098. doi: 10.1080/15476286.2015.1063770

 

  1. Netea MG, Joosten LA, Latz E, et al. Trained immunity: A program of innate immune memory in health and disease. Science. 2016;352(6284):aaf1098. doi: 10.1126/science.aaf1098

 

  1. Cheng SC, Quintin J, Cramer RA, et al. mTOR-and HIF- 1alpha-mediated aerobic glycolysis as metabolic basis for trained immunity. Science. 2014;345(6204):1250684. doi: 10.1126/science.1250684

 

  1. Quintin J, Saeed S, Martens JH, et al. Candida albicans infection affords protection against reinfection via functional reprogramming of monocytes. Cell Host Microbe. 2012;12(2):223-232. doi: 10.1016/j.chom.2012.06.006

 

  1. Rosenthal SR, Loewinsohn E, Graham ML, Liveright D, Thorne MG, Johnson V. BCG vaccination in tuberculous households. Am Rev Respir Dis. 1961;84:690-704. doi: 10.1164/arrd.1961.84.5P1.690

 

  1. Chedid L, Parant M, Parant F, Lefrancher P, Choay J, Lederer E. Enhancement of nonspecific immunity to Klebsiella pneumoniae infection by a synthetic immunoadjuvant (N-acetylmuramyl-L-alanyl-D-isoglutamine) and several analogs. Proc Natl Acad Sci U S A. 1977;74(5):2089-2093. doi: 10.1073/pnas.74.5.2089

 

  1. Flanagan KL, Van Crevel R, Curtis N, Shann F, Levy O, Optimmunize Network. Heterologous (“nonspecific”) and sex-differential effects of vaccines: Epidemiology, clinical trials, and emerging immunologic mechanisms. Clin Infect Dis. 2013;57(2):283-289. doi: 10.1093/cid/cit209

 

  1. Geckin B, Konstantin Fohse F, Dominguez-Andres J, Netea MG. Trained immunity: Implications for vaccination. Curr Opin Immunol. 2022;77:102190. doi: 10.1016/j.coi.2022.102190

 

  1. Uthaya Kumar DB, Williams A. Long non-coding RNAs in immune regulation and their potential as therapeutic targets. Int Immunopharmacol. 2020;81:106279. doi: 10.1016/j.intimp.2020.106279

 

  1. Kotzin JJ, Spencer SP, McCright SJ, et al. The long non-coding RNA Morrbid regulates Bim and short-lived myeloid cell lifespan. Nature. 2016;537(7619):239-243. doi: 10.1038/nature19346

 

  1. Yang CA, Li JP, Yen JC, et al. lncRNA NTT/PBOV1 axis promotes monocyte differentiation and is elevated in rheumatoid arthritis. Int J Mol Sci. 2018;19(9):2806. doi: 10.3390/ijms19092806

 

  1. Krawczyk M, Emerson BM. p50-associated COX-2 extragenic RNA (PACER) activates COX-2 gene expression by occluding repressive NF-κB complexes. Elife. 2014;3:e01776. doi: 10.7554/eLife.01776

 

  1. Chen MT, Lin HS, Shen C, et al. PU.1-regulated long noncoding RNA lnc-MC controls human monocyte/ macrophage differentiation through interaction with MicroRNA 199a-5p. Mol Cell Biol. 2015;35(18):3212-3224. doi: 10.1128/MCB.00429-15

 

  1. Huang Z, Luo Q, Yao F, et al. Identification of differentially expressed long non-coding RNAs in polarized macrophages. Sci Rep. 2016;6:19705. doi: 10.1038/srep19705

 

  1. Obaid M, Udden SM, Deb P, Shihabeddin N, Zaki MH, Mandal SS. LncRNA HOTAIR regulates lipopolysaccharide-induced cytokine expression and inflammatory response in macrophages. Sci Rep. 2018;8(1):15670. doi: 10.1038/s41598-018-33722-2

 

  1. Wang P, Xue Y, Han Y, et al. The STAT3-binding long noncoding RNA lnc-DC controls human dendritic cell differentiation. Science. 2014;344(6181):310-313. doi: 10.1126/science.1251456

 

  1. Xin J, Li J, Feng Y, Wang L, Zhang Y, Yang R. Downregulation of long noncoding RNA HOTAIRM1 promotes monocyte/ dendritic cell differentiation through competitively binding to endogenous miR-3960. Onco Targets Ther. 2017;10:1307-1315. doi: 10.2147/OTT.S124201

 

  1. Zhang M, Zheng Y, Sun Y, et al. Knockdown of NEAT1 induces tolerogenic phenotype in dendritic cells by inhibiting activation of NLRP3 inflammasome. Theranostics. 2019;9(12):3425-3442. doi: 10.7150/thno.33178

 

  1. Wu J, Li S, Zheng Y, et al. Silencing of lncRNA NEAT1 induces tolerogenic dendritic cells and immune tolerance in heart transplantation. J. Immunol. 2017;198(1_ Supplement):82.27-82.27. doi: 10.4049/jimmunol.198.Supp.82.27

 

  1. Wu J, Zhang H, Zheng Y, et al. The long noncoding RNA MALAT1 induces tolerogenic dendritic cells and regulatory T cells via miR155/dendritic cell-specific intercellular adhesion molecule-3 grabbing nonintegrin/IL10 axis. Front Immunol. 2018;9:1847. doi: 10.3389/fimmu.2018.01847

 

  1. Cai Z, Zhang C, Kotzin JJ, Williams A, Henao-Mejia J, Kapur R. Role of lncRNA Morrbid in PTPN11(Shp2)E76K-driven juvenile myelomonocytic leukemia. Blood Adv. 2020;4(14):3246-3251. doi: 10.1182/bloodadvances.2020002123

 

  1. Ye Y, Xu Y, Lai Y, et al. Long non-coding RNA cox-2 prevents immune evasion and metastasis of hepatocellular carcinoma by altering M1/M2 macrophage polarization. J Cell Biochem. 2018;119(3):2951-2963. doi: 10.1002/jcb.26509

 

  1. Tian X, Wu Y, Yang Y, et al. Long noncoding RNA LINC00662 promotes M2 macrophage polarization and hepatocellular carcinoma progression via activating Wnt/β- catenin signaling. Mol Oncol. 2020;14(2):462-483. doi: 10.1002/1878-0261.12606

 

  1. Liang Y, Song X, Li Y, et al. LncRNA BCRT1 promotes breast cancer progression by targeting miR-1303/PTBP3 axis. Mol Cancer. 2020;19(1):85. doi: 10.1186/s12943-020-01206-5

 

  1. Liu D, Wei Y, Liu Y, Wu T, Hu J, Lu H. The Long non-coding RNA NEAT1/miR-224-5p/IL-33 axis modulates macrophage M2a polarization and A1 astrocyte activation. Mol Neurobiol. 2021;58(9):4506-4519. doi: 10.1007/s12035-021-02405-x

 

  1. Cao J, Dong R, Jiang L, et al. LncRNA-MM2P identified as a Res. 2019;7(2):292-305. doi: 10.1158/2326-6066.CIR-18-0145

 

  1. Yang C, Shen C, Feng T, Li H. Noncoding RNA in NK cells. J Leukoc Biol. 2019;105(1):63-71. doi: 10.1002/JLB.1RU0518-197RR

 

  1. Sun JC, Madera S, Bezman NA, Beilke JN, Kaplan MH, Lanier LL. Proinflammatory cytokine signaling required for the generation of natural killer cell memory. J Exp Med. 2012;209(5):947-954. doi: 10.1084/jem.20111760

 

  1. O’Leary JG, Goodarzi M, Drayton DL, Von Andrian UH. T cell-and B cell-independent adaptive immunity mediated by natural killer cells. Nat Immunol. 2006;7(5):507-516. doi: 10.1038/ni1332

 

  1. Sun JC, Beilke JN, Lanier LL. Adaptive immune features of natural killer cells. Nature. 2009;457(7229):557-561. doi: 10.1038/nature07665

 

  1. Mowel WK, McCright SJ, Kotzin JJ, et al. Group 1 innate lymphoid cell lineage identity is determined by a cis-regulatory element marked by a long non-coding RNA. Immunity. 2017;47(3):435-449.e8. doi: 10.1016/j.immuni.2017.08.012

 

  1. Fang P, Xiang L, Chen W, et al. LncRNA GAS5 enhanced the killing effect of NK cell on liver cancer through regulating miR-544/RUNX3. Innate Immun. 2019;25(2):99-109. doi: 10.1177/1753425919827632

 

  1. Guttman M, Amit I, Garber M, et al. Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature. 2009;458(7235):223-227. doi: 10.1038/nature07672

 

  1. Carpenter S, Aiello D, Atianand MK, et al. A long noncoding RNA mediates both activation and repression of immune response genes. Science. 2013;341(6147):789-92. doi: 10.1126/science.1240925

 

  1. Morchikh M, Cribier A, Raffel R, et al. HEXIM1 and NEAT1 Long non-coding RNA form a multi-subunit complex that regulates dna-mediated innate immune response. Mol Cell. 2017;67(3):387-399.e5. doi: 10.1016/j.molcel.2017.06.020

 

  1. Wang Y, Wang P, Zhang Y, et al. Decreased expression of the host long-noncoding RNA-GM facilitates viral escape by inhibiting the kinase activity TBK1 via S-glutathionylation. Immunity. 2020;53(6):1168-1181.e7. doi: 10.1016/j.immuni.2020.11.010

 

  1. Biswas S, Thomas AA, Chen S, et al. MALAT1: An epigenetic regulator of inflammation in diabetic retinopathy. Sci Rep. 2018;8(1):6526. doi: 10.1038/s41598-018-24907-w

 

  1. Yuan J, Zhu Q, Zhang X, et al. Ezh2 competes with p53 to license lncRNA Neat1 transcription for inflammasome activation. Cell Death Differ. 2022;29(10):2009-2023. doi: 10.1038/s41418-022-00992-3

 

  1. Tang L, Wei X, Li T, et al. Emerging perspectives of RNA N6-methyladenosine (m6A) modification on immunity and autoimmune diseases. Front Immunol. 2021;12:630358. doi: 10.3389/fimmu.2021.630358

 

  1. Zhou KI, Parisien M, Dai Q, et al. N(6)-methyladenosine modification in a long noncoding RNA hairpin predisposes its conformation to protein binding. J Mol Biol. 2016;428(5 Pt A):822-833. doi: 10.1016/j.jmb.2015.08.021

 

  1. Chang YZ, Chai RC, Pang B, et al. Corrigendum to “METTL3 enhances the stability of MALAT1 with the assistance of HuR via m6A modification and activates NF-κB to promote the malignant progression of IDH-wildtype glioma” [Canc. Lett. 511 (2021) 36-46. Cancer Lett. 2023;569:216309. doi: 10.1016/j.canlet.2023.216309

 

  1. Jiang M, Zhang S, Yang Z, et al. Self-recognition of an inducible host lncRNA by RIG-I feedback restricts innate immune response. Cell. 2018;173(4):906-919.e13. doi: 10.1016/j.cell.2018.03.064

 

  1. Hamada A, Torre C, Drancourt M, Ghigo E. Trained immunity carried by non-immune cells. Front Microbiol. 2018;9:3225. doi: 10.3389/fmicb.2018.03225

 

  1. Wei JW, Huang K, Yang C, Kang CS. Non-coding RNAs as regulators in epigenetics (Review). Oncol Rep. 2017;37(1): 3-9. doi: 10.3892/or.2016.5236

 

  1. Foster SL, Hargreaves DC, Medzhitov R. Gene-specific control of inflammation by TLR-induced chromatin modifications. Nature. 2007;447(7147):972-978. doi: 10.1038/nature05836

 

  1. Chen F, Wu W, Millman A, et al. Neutrophils prime a long-lived effector macrophage phenotype that mediates accelerated helminth expulsion. Nat Immunol. 2014;15(10):938-946. doi: 10.1038/ni.2984

 

  1. Barton ES, White DW, Cathelyn JS, et al. Herpesvirus latency confers symbiotic protection from bacterial infection. Nature. 2007;447(7142):326-329. doi: 10.1038/nature05762

 

  1. Yona S, Kim KW, Wolf Y, et al. Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis. Immunity. 2013;38(1):79-91. doi: 10.1016/j.immuni.2012.12.001

 

  1. Kleinnijenhuis J, Quintin J, Preijers F, et al. Bacille calmette-guerin induces NOD2-dependent nonspecific protection from reinfection via epigenetic reprogramming of monocytes. Proc Natl Acad Sci U S A. 2012;109(43): 17537-17542. doi: 10.1073/pnas.1202870109

 

  1. Ostuni R, Piccolo V, Barozzi I, et al. Latent enhancers activated by stimulation in differentiated cells. Cell. 2013;152(1-2):157-171. doi: 10.1016/j.cell.2012.12.018

 

  1. Kaikkonen MU, Spann NJ, Heinz S, et al. Remodeling of the enhancer landscape during macrophage activation is coupled to enhancer transcription. Mol Cell. 2013;51(3): 310-325. doi: 10.1016/j.molcel.2013.07.010

 

  1. Kamada R, Yang W, Zhang Y, et al. Interferon stimulation creates chromatin marks and establishes transcriptional memory. Proc Natl Acad Sci U S A. 2018;115(39):E9162-E9171. doi: 10.1073/pnas.1720930115

 

  1. Lee J, Zhang T, Hwang I, et al. Epigenetic modification and antibody-dependent expansion of memory-like NK cells in human cytomegalovirus-infected individuals. Immunity. 2015;42(3):431-442. doi: 10.1016/j.immuni.2015.02.013

 

  1. Hanly DJ, Esteller M, Berdasco M. Interplay between long non-coding RNAs and epigenetic machinery: Emerging targets in cancer? Philos Trans R Soc Lond B Biol Sci. 2018;373(1748):20170074. doi: 10.1098/rstb.2017.0074

 

  1. Wu X, Wan Q, Wang J, et al. Epigenetic activation of lncRNA MIR155HG mediated by promoter hypomethylation and SP1 is correlated with immune infiltration in Glioma. Onco Targets Ther. 2022;15:219-235. doi: 10.2147/OTT.S349078

 

  1. Guo B, Jiang T, Wu F, et al. LncRNA RP5-998N21.4 promotes immune defense through upregulation of IFIT2 and IFIT3 in schizophrenia. Schizophrenia (Heidelb). 2022;8(1):11. doi: 10.1038/s41537-021-00195-8

 

  1. Bah I, Youssef D, Yao ZQ, McCall CE, El Gazzar M. Inhibiting KDM6A demethylase represses long non-coding RNA hotairm1 transcription in MDSC during sepsis. Front Immunol. 2022;13:823660. doi: 10.3389/fimmu.2022.823660

 

  1. Morlando M, Fatica A. Alteration of epigenetic regulation by long noncoding RNAs in cancer. Int J Mol Sci. 2018;19(2):570. doi: 10.3390/ijms19020570

 

  1. Kanbar JN, Ma S, Kim ES, et al. The long noncoding RNA Malat1 regulates CD8+ T cell differentiation by mediating epigenetic repression. J Exp Med. 2022;219(6):e20211756. doi: 10.1084/jem.20211756

 

  1. Fok ET, Davignon L, Fanucchi S, Mhlanga MM. The lncRNA connection between cellular metabolism and epigenetics in trained immunity. Front Immunol. 2018;9:3184. doi: 10.3389/fimmu.2018.03184

 

  1. Fanucchi S, Dominguez-Andres J, Joosten LA, Netea MG, Mhlanga MM. The Intersection of epigenetics and metabolism in trained immunity. Immunity. 2021;54(1): 32-43. doi: 10.1016/j.immuni.2020.10.011

 

  1. Fernandes JC, Acuna SM, Aoki JI, Floeter-Winter LM, Muxel SM. Long Non-Coding RNAs in the regulation of gene expression: Physiology and disease. Noncoding RNA. 2019;5(1):17. doi: 10.3390/ncrna5010017

 

  1. Zhang T, Cooper S, Brockdorff N. The interplay of histone modifications-writers that read. EMBO Rep. 2015;16(11):1467-1481. doi: 10.15252/embr.201540945

 

  1. Bohmdorfer G, Wierzbicki AT. Control of chromatin structure by long noncoding RNA. Trends Cell Biol. 2015;25(10):623-632. doi: 10.1016/j.tcb.2015.07.002

 

  1. Fanucchi S, Fok ET, Dalla E, et al. Immune genes are primed for robust transcription by proximal long noncoding RNAs located in nuclear compartments. Nat Genet. 2019;51(1): 138-150. doi: 10.1038/s41588-018-0298-2

 

  1. Fanucchi S, Mhlanga MM. Lnc-ing trained immunity to chromatin architecture. Front Cell Dev Biol. 2019;7:2. doi: 10.3389/fcell.2019.00002

 

  1. Kim TK, Hemberg M, Gray JM. Enhancer RNAs: A class of long noncoding RNAs synthesized at enhancers. Cold Spring Harb Perspect Biol. 2015;7(1):a018622. doi: 10.1101/cshperspect.a018622

 

  1. Wang KC, Yang YW, Liu B, et al. A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression. Nature. 2011;472(7341):120-124. doi: 10.1038/nature09819

 

  1. Gomez JA, Wapinski OL, Yang YW, et al. The NeST long ncRNA controls microbial susceptibility and epigenetic activation of the interferon-γ locus. Cell. 2013;152(4):743-754. doi: 10.1016/j.cell.2013.01.015

 

  1. Murphy MB, Medvedev AE. Long noncoding RNAs as regulators of Toll-like receptor signaling and innate immunity. J Leukoc Biol. 2016;99(6):839-850. doi: 10.1189/jlb.2RU1215-575R

 

  1. Carpenter S. Long noncoding RNA: Novel links between gene expression and innate immunity. Virus Res. 2016;212:137-145. doi: 10.1016/j.virusres.2015.08.019

 

  1. Du M, Yuan L, Tan X, et al. The LPS-inducible lncRNA Mirt2 is a negative regulator of inflammation. Nat Commun. 2017;8(1):2049. doi: 10.1038/s41467-017-02229-1

 

  1. Lu W, Cao F, Wang S, Sheng X, Ma J. LncRNAs: The regulator of glucose and lipid metabolism in tumor cells. Front Oncol. 2019;9:1099. doi: 10.3389/fonc.2019.01099

 

  1. Hong J, Guo F, Lu SY, et al. F. nucleatum targets lncRNA ENO1-IT1 to promote glycolysis and oncogenesis in colorectal cancer. Gut. 2021;70(11):2123-2137. doi: 10.1136/gutjnl-2020-322780

 

  1. Sohrabi Y, Godfrey R, Findeisen HM. Altered cellular metabolism drives trained immunity. Trends Endocrinol Metab. 2018;29(9):602-605. doi: 10.1016/j.tem.2018.03.012

 

  1. Arts RJ, Carvalho A, La Rocca C, et al. Immunometabolic pathways in BCG-induced trained immunity. Cell Rep. 2016;17(10):2562-2571. doi: 10.1016/j.celrep.2016.11.011

 

  1. Sohrabi Y, Dos Santos JC, Dorenkamp M, et al. Trained immunity as a novel approach against COVID-19 with a focus on Bacillus Calmette-Guérin vaccine: Mechanisms, challenges and perspectives. Clin Transl Immunol. 2020;9(12):e1228. doi: 10.1002/cti2.1228
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