The DOI matches its Crossref record; 42 of the 42 references it cites were found in a registry or an index.
Glutaminolysis and Fumarate Accumulation Integrate Immunometabolic and Epigenetic Programs in Trained Immunity
Open accessAbstract
Induction of trained immunity (innate immune memory) is mediated by activation of immune and metabolic pathways that result in epigenetic rewiring of cellular functional programs. Through network-level integration of transcriptomics and metabolomics data, we identify glycolysis, glutaminolysis, and the cholesterol synthesis pathway as indispensable for the induction of trained immunity by β-glucan in monocytes. Accumulation of fumarate, due to glutamine replenishment of the TCA cycle, integrates immune and metabolic circuits to induce monocyte epigenetic reprogramming by inhibiting KDM5 histone demethylases. Furthermore, fumarate itself induced an epigenetic program similar to β-glucan-induced trained immunity. In line with this, inhibition of glutaminolysis and cholesterol synthesis in mice reduced the induction of trained immunity by β-glucan. Identification of the metabolic pathways leading to induction of trained immunity contributes to our understanding of innate immune memory and opens new therapeutic avenues.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“Fumarate was shown to cause succination of the mitochondrial aconitase, ACO2, leading to an additional truncation of the TCA cycle86”
From Coupling Krebs cycle metabolites to signalling in immunity and cancer (2018) · cites this paper as [86]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Succinate is an inflammatory signal that induces IL-1β through HIF-1α
Tannahill, G. M., Curtis, A. M., Adamik, J., Palsson-McDermott, E. M., McGettrick, A. F., Goel, G., Frezza, C., Bernard, N. J., Kelly, B., Foley, N. H., et al. (2013) · Nature · doi:10.1038/nature11986 · Cited by 4,176 · cited 1×
“Citric acid cycle metabolites (e.g., fumarate and succinate) have previously been reported to regulate HIF1a stabilization by inhibiting hydroxylation and therefore stabilizing HIF1a (Koi- vunen et al., 2007; Tannahill et al., 2013).”
BackgroundSelf-citationCaspi, R., Billington, R., Ferrer, L., Foerster, H., Fulcher, C. A., Keseler, I. M., Kothari, A., Krummenacker, M., Latendresse, M., Mueller, L. A., et al. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkv1164 · Cited by 3,395
Trained immunity: A program of innate immune memory in health and– disease
Netea, M. G., Joosten, L. A. B., Latz, E., Mills, K. H. G., Natoli, G., Stunnenberg, H. G., O’Neill, L. A. J., & Xavier, R. J. (2016) · Science · doi:10.1126/science.aaf1098 · Cited by 2,768
Self-citationMetaboAnalyst 3.0—making metabolomics more meaningful
Xia, J., Sinelnikov, I. V., Han, B., & Wishart, D. S. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv380 · Cited by 2,680
mTOR- and HIF-1α–mediated aerobic glycolysis as metabolic basis for trained immunity
Cheng, S.-C., Quintin, J., Cramer, R. A., Shepardson, K. M., Saeed, S., Kumar, V., Giamarellos-Bourboulis, E. J., Martens, J. H. A., Rao, N. A., Aghajanirefah, A., et al. (2014) · Science · doi:10.1126/science.1250684 · Cited by 2,224
Self-citationIDH mutation impairs histone demethylation and results in a block to cell differentiation
Lu, C., Ward, P. S., Kapoor, G. S., Rohle, D., Turcan, S., Abdel-Wahab, O., Edwards, C. R., Khanin, R., Figueroa, M. E., Melnick, A., et al. (2012) · Nature · doi:10.1038/nature10860 · Cited by 1,985
Epigenetic programming of monocyte-to-macrophage differentiation and trained innate immunity
Saeed, S., Quintin, J., Kerstens, H. H. D., Rao, N. A., Aghajanirefah, A., Matarese, F., Cheng, S.-C., Ratter, J., Berentsen, K., van der Ent, M. A., et al. (2014) · Science · doi:10.1126/science.1251086 · Cited by 1,761
Self-citationTrained Immunity: A Memory for Innate Host Defense
Netea, M. G., Quintin, J., & van der Meer, J. W. M. (2011) · Cell Host & Microbe · doi:10.1016/j.chom.2011.04.006 · Cited by 1,760
Self-citationKleinnijenhuis, J., Quintin, J., Preijers, F., Joosten, L. A. B., Ifrim, D. C., Saeed, S., Jacobs, C., van Loenhout, J., de Jong, D., Stunnenberg, H. G., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1202870109 · Cited by 1,728
Self-citationHypoxia-Inducible Factor-1 (HIF-1)
Ke, Q., & Costa, M. (2006) · Molecular Pharmacology · doi:10.1124/mol.106.027029 · Cited by 1,690
Flagged first, then by citations
Cited by
Sorted by citations
Items 501–600 of 927
Lin, D. L., Magnaye, K. M., Porsche, C. E., Levan, S., Rackaityte, E., Özçam, M., & Lynch, S. V. (2024) · Journal of Immunology Research · doi:10.1155/2024/2506586 · Cited by 16
Smokelin, I. S., Mizzoni, C., Erndt‐Marino, J. D., Kaplan, D. L., & Georgakoudi, I. (2020) · Journal of Biomedical Optics · doi:10.1117/1.jbo.25.1.014512 · Cited by 17
Emerging roles of microRNAs in the metabolic control of immune cells
Yao, Q., Song, Z., Wang, B., & Zhang, J. (2018) · Cancer Letters · doi:10.1016/j.canlet.2018.06.024 · Cited by 17
Dysregulation of Host–Pathogen Interactions in Sepsis: Host-Related Factors
Joosten, S. C. M., Wiersinga, W. J., & van der Poll, T. (2024) · Seminars in Respiratory and Critical Care Medicine · doi:10.1055/s-0044-1787554 · Cited by 16
Migliaccio, G., Morikka, J., del Giudice, G., Vaani, M., Möbus, L., Serra, A., Federico, A., & Greco, D. (2024) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2024.08.018 · Cited by 16
Investigating endogenous immune-mediated monocyte memory in rheumatoid arthritis
Marzeda, A. M., Schwenzer, A., Didov, B. S., Woolcock, K., Richard, J.-B., Jennings, L. K., Julé, A. M., Yang, N., Davidson, S., Sansom, S. C., et al. (2025) · Annals of the Rheumatic Diseases · doi:10.1016/j.ard.2025.03.016 · Cited by 15
Potential effects of PFAS exposure on trained immunity: From mechanisms to health risks
Qiu, J., Huo, X., Dai, Y., Huang, Y., & Xu, X. (2025) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2025.118757 · Cited by 15
Trained immunity modulators: A new frontier in immunoregulation and disease intervention
Chen, J., Wang, C., Chen, S., Cai, H., Wang, M., Chang, J., Cai, X., Yang, J., & Cao, P. (2025) · Journal of Advanced Research · doi:10.1016/j.jare.2025.09.029 · Cited by 15
Unraveling effects of anti-aging drugs on C. elegans using liposomes
Zhang, A., Hsiung, K. C., Kern, C. C., Wang, Y., Girtle, A., Xu, N., & Gems, D. (2023) · GeroScience · doi:10.1007/s11357-023-00800-x · Cited by 17
Helicobacter pylori induces a novel form of innate immune memory via accumulation of NF-кB proteins
Frauenlob, T., Neuper, T., Regl, C., Schäpertöns, V., Unger, M. S., Oswald, A., Dang, H.-H., Huber, C. G., Aberger, F., Weßler, S., et al. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1290833 · Cited by 16
Sarcoidosis immunopathogenesis – a new concept of maladaptive trained immunity
Robert, M., Yatim, N., Sacré, K., & Duffy, D. (2024) · Trends in Immunology · doi:10.1016/j.it.2024.04.013 · Cited by 15
Trained Immunity and Trained Tolerance: The Case of Helicobacter pylori Infection
Dore, M. P., & Pes, G. M. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25115856 · Cited by 15
Song, X., Lei, T., Cui, N., Jin, X., Huang, Y. K., Shi, Y., & Zhao, Z. (2024) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2024.110035 · Cited by 15
Glutamine metabolism in adipocytes: a bona fide epigenetic modulator of inflammation
Lecoutre, S., Maqdasy, S., Petrus, P., Ludzki, A. C., Couchet, M., Mejhert, N., & Rydén, M. (2020) · Adipocyte · doi:10.1080/21623945.2020.1831825 · Cited by 16
Macrophage Metabolic Signaling during Ischemic Injury and Cardiac Repair
Thorp, E. B. (2021) · Immunometabolism · doi:10.20900/immunometab20210018 · Cited by 15
Denstaedt, S. J., Bustamante, A. C., Newstead, M. W., Moore, B. B., Standiford, T. J., Zemans, R. L., & Singer, B. H. (2021) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00123.2021 · Cited by 16
Targeting immunometabolism in host-directed therapies to fungal disease
Gonçalves, S. M., Ferreira, A. V., Cunha, C., & Carvalho, A. (2021) · Clinical & Experimental Immunology · doi:10.1093/cei/uxab014 · Cited by 15
Self-citationTherapeutic Potentials of Immunometabolomic Modulations Induced by Tuberculosis Vaccination
Rawat, B. S., Kumar, D., Soni, V., & Rosenn, E. H. (2022) · Vaccines · doi:10.3390/vaccines10122127 · Cited by 15
Quinteros, S. L., von Krusenstiern, E. V., Snyder, N. W., Tanaka, A., O’Brien, B. A., & Donnelly, S. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1018076 · Cited by 15
Trained immunity: novel perspectives in diabetes and associated complications
Liu, Y., Lei, Y., Dai, Z., Luo, C., Gong, Q., Li, Y., Xu, Y., & Huang, W. G. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1613602 · Cited by 14
Trained Immunity in Health and Disease
Yao, M., Zhou, J., Mei, J., Gao, C., Ding, P., Li, G., Zhang, C., Li, Z., & Gao, J. (2025) · MedComm · doi:10.1002/mco2.70461 · Cited by 16
Trained Immunity and Cardiovascular Risk: An Immunological Perspective
Boden, K. A., Chai, J., Kufazvinei, T. T. J., & Choudhury, R. P. (2026) · Immunological Reviews · doi:10.1111/imr.70095 · Cited by 15
Cellular Metabolism at a Glance
Mesquita, I., & Rodrigues, F. J. S. (2018) · Experientia supplementum · doi:10.1007/978-3-319-74932-7_1 · Cited by 14
Self-citationStifel, U., Caratti, G., & Tuckermann, J. P. (2022) · FEBS Letters · doi:10.1002/1873-3468.14474 · Cited by 14
The Role of NLRP3 Inflammasomes in Trained Immunity
Lee, G., Ahn, H., Lee, G., & Lee, G. (2023) · Frontiers in Bioscience-Landmark · doi:10.31083/j.fbl2809210 · Cited by 14
Chen, H., Song, J., Zeng, L., Zha, J., Zha, J., Chen, A., Liu, Y., Dong, Z., & Chen, G. (2024) · Biochemical Pharmacology · doi:10.1016/j.bcp.2024.116505 · Cited by 14
Mucosal Inflammatory Memory in Chronic Rhinosinusitis
Koo, M., Moon, S., & Rha, M. (2024) · Cells · doi:10.3390/cells13231947 · Cited by 14
Hematopoietic stem cell a reservoir of innate immune memory
Ruffinatto, L., Groult, Y., Iacono, J., Sarrazin, S., & de Laval, B. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1491729 · Cited by 14
Epigenetic Regulation of Innate and Adaptive Immune Cells in Salt-Sensitive Hypertension
Mutchler, A. P., Haynes, A. P., Saleem, M., Jamison, S., Khan, M. M., Ertuğlu, L. A., & Kirabo, A. (2025) · Circulation Research · doi:10.1161/circresaha.124.325439 · Cited by 14
Pathogenesis of ANCA-associated vasculitis: an emerging role for immunometabolism
Leacy, E. J., Brady, G., & Little, M. A. (2020) · Rheumatology · doi:10.1093/rheumatology/keaa023 · Cited by 14
Filippi, M. (2021) · Experimental Hematology · doi:10.1016/j.exphem.2021.01.006 · Cited by 15
Trained Innate Immunity in Hematopoietic Stem Cell and Solid Organ Transplantation
Cunningham, K. T., & Mills, K. H. G. (2021) · Transplantation · doi:10.1097/tp.0000000000003673 · Cited by 14
Maasfeh, L., Härtlová, A., Isaksson, S., Sundin, J., Mavroudis, G., Savolainen, O. I., Strid, H., Öhman, L., & Magnusson, M. K. (2021) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2021.06.004 · Cited by 14
Clinical Characteristics of Molecularly Defined Renal Cell Carcinomas
Hu, X., Tan, C., & Zhu, G. (2023) · Current Issues in Molecular Biology · doi:10.3390/cimb45060303 · Cited by 14
Metabolic dysregulation of trained immunity in immune aging and the impact of dietary patterns
Grigorescu, A., Riza, A., Streață, I., & Netea, M. G. (2025) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00153.2025 · Cited by 16
Self-citationMacrophages in chronic infections: regulation and remodeling
Cui, H., Wang, M., Jiao, S., Tian, S., Liu, H., & Luo, B. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1594988 · Cited by 13
Acevedo, N., Lozano, A. M., Zakzuk, J., Llinás-Caballero, K., Brodin, D., Nejsum, P. L., Williams, A. R., & Caraballo, L. R. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1328401 · Cited by 13
From metabolic to epigenetic: Insight into trained macrophages in atherosclerosis (Review)
Li, T., Feng, W., Yan, W., & Wang, T. (2024) · Molecular Medicine Reports · doi:10.3892/mmr.2024.13269 · Cited by 13
Innate immune response in acute critical illness: a narrative review
Stiel, L., Gaudet, A., Thietart, S., Vallet, H., Bastard, P., Voiriot, G., Oualha, M., Sarton, B., Kallel, H., Bréchot, N., et al. (2024) · Annals of Intensive Care · doi:10.1186/s13613-024-01355-6 · Cited by 13
Epigenetic and Transcriptional Regulation of Innate Immunity in Cancer
Chen, C., Man, N., Liu, F., Martín, G. M., Itonaga, H., Sun, J., & Nimer, S. D. (2022) · Cancer Research · doi:10.1158/0008-5472.can-21-3503 · Cited by 13
Innate Immune Training of Human Macrophages by Cathelicidin Analogs
van Dijk, A. I. J. M., Anten, J., Bakker, A., Evers, N., Hoekstra, A. T., Chang, J., Scheenstra, M. R., Veldhuizen, E. J. A., Netea, M. G., Berkers, C. R., et al. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.777530 · Cited by 13
Self-citationTrained immunity: a cutting edge approach for designing novel vaccines against parasitic diseases?
Zhu, J., Liu, J., Yan, C., Wang, D., & Pan, W. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1252554 · Cited by 13
Mahon, R. N., & Hafner, R. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00688 · Cited by 13
Arginine metabolism supports metabolic reprogramming in trained immunity
Pich, L. M. M., Ziogas, A., Ferreira, A. V., Sumpter, N. A., Sarlea, A. S., Kostidis, S., Joosten, L. A. B., & Netea, M. G. (2025) · Journal of Leukocyte Biology · doi:10.1093/jleuko/qiaf080 · Cited by 12
Self-citationReversing inflammatory diseases via trained immunity: mechanisms, challenges, and prospects
Xu, W., Guo, Z., Xu, T., Chen, J., Chen, L., & Xu, W. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1666233 · Cited by 14
The role of immunomodulatory metabolites in shaping the inflammatory response of macrophages
Park, D., Lim, G., Yoon, S., Yi, H., & Choi, D. W. (2022) · BMB Reports · doi:10.5483/bmbrep.2022.55.11.128 · Cited by 12
Huang, Z. (2023) · Journal of Alzheimer s Disease · doi:10.3233/jad-221042 · Cited by 12
Harnessing traditional Chinese medicine polysaccharides for combatting COVID-19
Xiao, Z., Guo, Y., Li, J., Jiang, X., Wu, F., Wang, Y., Zhang, Y., & Zhou, W. (2024) · Carbohydrate Polymers · doi:10.1016/j.carbpol.2024.122605 · Cited by 12
Trained immunity in diabetes: emerging targets for cardiovascular complications
Bai, Y., Wu, J., & Jian, W. (2025) · Frontiers in Endocrinology · doi:10.3389/fendo.2025.1533620 · Cited by 12
BCG and SARS-CoV-2—What Have We Learned?
Kulesza, J., Kulesza, E., Koziński, P., Karpik, W., Broncel, M., & Fol, M. (2022) · Vaccines · doi:10.3390/vaccines10101641 · Cited by 12
Dietary schizophyllan reduces mitochondrial damage by activating SIRT3 in mice
Lee, D., Kim, Y.-R., Js, K., Kim, D.-G., Kim, S., Kim, S., Jang, K., Lee, J.-D., & Yang, C. (2020) · Archives of Pharmacal Research · doi:10.1007/s12272-020-01231-4 · Cited by 12
TIDB: a comprehensive database of trained immunity
Cao, Y., Dong, Q., Wang, D., Liu, Y., Zhang, P., Yu, X., & Niu, C. (2021) · Database · doi:10.1093/database/baab041 · Cited by 12
Bacillus Calmette–Guérin in Immuno-Regulation of Alzheimer’s Disease
Klein, B., Greenblatt, C. L., Gofrit, O. N., & Bercovier, H. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.861956 · Cited by 12
Takahashi, K., Drolet, J., Liu, J., Jackson, J. R., Thiruppathi, M., Fang, M. M., Rogers, J., Davis, I. D., Fantuzzi, G., Benevolenskaya, E. V., et al. (2025) · The Journal of Immunology · doi:10.1093/jimmun/vkaf156 · Cited by 13
Integration and Intersection of Cancer Metabolism with Epigenetic Pathways in Gliomas
Natarajan, S. K., Pun, M. J., Haggerty-Skeans, J., & Venneti, S. (2025) · Annual Review of Pathology Mechanisms of Disease · doi:10.1146/annurev-pathmechdis-111523-023424 · Cited by 13
Mitochondrial Factors in the Cell Nucleus
González‐Arzola, K., & Dı́az-Quintana, A. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241713656 · Cited by 12
Skin innate immune response against fungal infections and the potential role of trained immunity
Bombassaro, A., Figueiredo, J., Taborda, C. P., Joosten, L. A. B., Vicente, V. A., Queiroz‐Telles, F., Meis, J. F. G. M., & Kischkel, B. (2024) · Mycoses · doi:10.1111/myc.13682 · Cited by 11
Self-citationCapriotti, Z., & Klase, Z. A. (2024) · Journal of NeuroVirology · doi:10.1007/s13365-024-01239-2 · Cited by 11
Guo, C., Xu, P., Luo, W., Zhang, J., Sun, X., Hoang, H., Ma, D., Wu, D., Zhong, J., & Miao, C. (2025) · Journal of Inflammation Research · doi:10.2147/jir.s482213 · Cited by 11
Cross-kingdom mechanisms of trained immunity in plant systemic acquired resistance
Conrath, U. (2025) · Nature Plants · doi:10.1038/s41477-025-02119-1 · Cited by 11
Metabolic–Epigenetic Crosstalk in Macrophage Activation: An Updated View
Verberk, S. G. S., de Goede, K. E., & den Bossche, J. V. (2019) · Epigenomics · doi:10.2217/epi-2019-0073 · Cited by 11
Hackett, E. E., & Sheedy, F. J. (2020) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2020.00446 · Cited by 11
Al‐Obaidy, K. I., Alruwaii, Z. I., Williamson, S. R., & Liang Cheng, C. (2022) · Histopathology · doi:10.1111/his.14641 · Cited by 11
Glycolytic metabolism supports microglia training during age-related neurodegeneration
Camacho‐Morales, A. (2022) · Pharmacological Reports · doi:10.1007/s43440-022-00363-2 · Cited by 11
The Burgeoning World of Immunometabolites: Th17 Cells Take Center Stage
Bantug, G. R., & Hess, C. (2017) · Cell Metabolism · doi:10.1016/j.cmet.2017.09.014 · Cited by 11
Shen, W., Nie, Z., Wang, M., Zhang, H., Liu, Y., Zhu, H., Zhou, W., Zhang, L., Zhao, M., Zeng, H., et al. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2501704122 · Cited by 10
Self-citationTrained innate immunity modulates osteoblast and osteoclast differentiation
Rahmani, N. R., Belluomo, R., Kruyt, M. C., Gawlitta, D., Joosten, L. A. B., Weinans, H., & Croes, M. (2024) · Stem Cell Reviews and Reports · doi:10.1007/s12015-024-10711-9 · Cited by 10
Self-citationLiu, J., Liu, S., Zheng, H., Lee, J., Gurung, R. L., Chan, C., Lee, L. S., Ang, K., Ching, J., Kovalik, J., et al. (2024) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgae199 · Cited by 11
Álvarez-González, E., & Sierra, L. M. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25169054 · Cited by 10
McBride, M. A., Burelbach, K. R., Patil, T. K., Owen, A. M., Luan, L., Bohannon, J. K., Hernandez, A., Stothers, C. L., Trenary, I. A., Rahim, M., et al. (2024) · Journal of Leukocyte Biology · doi:10.1093/jleuko/qiae198 · Cited by 10
Immune Memory: A New Frontier in Treating Recurrent Inflammatory Skin Diseases
Yin, H., Chen, J., & Li, C. (2025) · Clinical Reviews in Allergy & Immunology · doi:10.1007/s12016-025-09039-0 · Cited by 10
Trained immunity-based Adjuvated vaccines (TIbAV) approach: β-glucans as example
Angulo, M., Ramos‐Vega, A., & Angulo, C. (2025) · Vaccine · doi:10.1016/j.vaccine.2025.127240 · Cited by 10
Targeting innate immune memory: a new paradigm for gout treatment
Gaal, O. I., Joosten, L. A. B., & Crișan, T. O. (2025) · Exploration of Musculoskeletal Diseases · doi:10.37349/emd.2025.1007103 · Cited by 10
Self-citationWang, X., Ma, L., Chen, C., Ma, L., Qu, X., Ren, A., Zhou, Y., & Cheng, H. (2025) · Carbohydrate Polymers · doi:10.1016/j.carbpol.2025.124554 · Cited by 11
Wang, X., Zhao, Z., Song, C., Su, Z., Li, M., Wu, Y., Jin, B. R., & Deng, M. (2022) · Insect Science · doi:10.1111/1744-7917.13114 · Cited by 10
Temporary consumption of western diet trains the immune system to reduce future gut inflammation
Wu, D., Wang, X., Yang, X., Gu, L., McGeachy, M. J., & Liu, X. (2023) · iScience · doi:10.1016/j.isci.2023.106915 · Cited by 11
BCG-Induced Immune Training: Interplay between Trained Immunity and Emergency Granulopoiesis
Henok, A., Hollams, E. M., Kollmann, T. R., & Amenyogbe, N. (2023) · Journal of Molecular Biology · doi:10.1016/j.jmb.2023.168169 · Cited by 10
Nitric oxide is an epigenetic regulator of histone post-translational modifications in cancer
Palczewski, M. B., Kuschman, H. P., & Thomas, D. D. (2019) · Current Opinion in Physiology · doi:10.1016/j.cophys.2019.05.006 · Cited by 10
Krebs Cycle Rewired: Driver of Atherosclerosis Progression?
Liang, Y., Chen, Y., Lü, L., Zhang, S., Xiao, J., & Wei, D. (2021) · Current Medicinal Chemistry · doi:10.2174/0929867328666210806105246 · Cited by 11
Heme induces innate immune memoryPreprint
Jentho, E., Novakovic, B., Ruiz-Moreno, C., Kourtzelis, I., Martins, R., Chavakis, T., Soares, M. P., Kalafati, L., Guerra, J., Röstel, F., et al. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2019.12.12.874578 · Cited by 10
Self-citationCui, M., Tang, G., Yan, F., Wang, S., Wang, X., Yao, J., & Xu, X. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1119747 · Cited by 9
Self-citationSilva, R. C. M. C., Ramos, I., Travassos, L. H., Mendez, A. P. G., & Gomes, F. M. (2024) · Journal of Comparative Physiology B · doi:10.1007/s00360-024-01549-1 · Cited by 9
Engineering immunity using metabolically active polymeric nanoparticles
Griffin, K. V., Saunders, M. N., Lyssiotis, C. A., & Shea, L. D. (2024) · Trends in biotechnology · doi:10.1016/j.tibtech.2024.11.016 · Cited by 9
Bioengineering approaches to trained immunity: Physiologic targets and therapeutic strategies
Knight, H. R., Kim, M., Kannan, N., Taylor, H. B., Main, H., Azcue, E., & Esser-Kahn, A. P. (2025) · eLife · doi:10.7554/elife.106339 · Cited by 9
Glucose Metabolic Reprogramming of Macrophages Against Mycobacterium tuberculosis Infection
Liu, T., Yang, Z., Tong, J., Gao, M., & Pang, Y. (2025) · ImmunoTargets and Therapy · doi:10.2147/itt.s552746 · Cited by 9
Trained Immunity: RoadMap for drug discovery and development
van Puffelen, J. H., Campbell, C., Gander-Meisterernst, I., Holldack, J., & Lukey, P. T. (2025) · eLife · doi:10.7554/elife.108465 · Cited by 9
A CLOCK-targeting lncRNA induces trained immunity against tuberculosis
Yu, S., Chai, Q., Lu, Z., Qiu, C., Zhong, Y., Wang, Y., Lei, Z., Qiang, L., Fang, Y., Zhang, X., et al. (2025) · Cell Host & Microbe · doi:10.1016/j.chom.2025.12.002 · Cited by 9
Høgh, R. I., Droujinine, A., Møller, S. H., Jepsen, S. D., Mellergaard, M., Andresen, L. O., & Skov, S. (2020) · The Journal of Immunology · doi:10.4049/jimmunol.1900740 · Cited by 9
Transcriptomic Remodelling of Fetal Endothelial Cells During Establishment of Inflammatory Memory
Weiß, E., Vlahos, A., Kim, B., Wijegunasekara, S., Shanmuganathan, D., Aitken, T., Joo, J. E., Imran, S., Shepherd, R., Craig, J. M., et al. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.757393 · Cited by 9
Self-citationHypoxia signalling in the regulation of innate immune training
Eades, L., Drozd, M., & Cubbon, R. M. (2021) · Biochemical Society Transactions · doi:10.1042/bst20210857 · Cited by 9
Trained immunity from the perspective of Plasmodium infection
Li, J., Liu, L., Chen, D., Yin, W., & Huang, J. (2023) · European Journal of Immunology · doi:10.1002/eji.202250268 · Cited by 9
Cox, J. H., McCain, R. S., Tran, E., Swaminathan, S., Smith, H. H., Piroli, G. G., Shtutman, M. S., Walla, M. D., Cotham, W. E., & Frizzell, N. (2024) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00354.2023 · Cited by 9
Silva-Gomes, R., Caldeira, I., Fernandes, R., Cunha, C., & Carvalho, A. (2024) · Journal of Leukocyte Biology · doi:10.1093/jleuko/qiae045 · Cited by 9
Self-citationThe Heterologous Effects of Bacillus Calmette-Guérin (BCG) Vaccine and Trained Innate Immunity
Novakovic, B., Messina, N. L., & Curtis, N. C. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-814603-3.00006-9 · Cited by 9
Self-citationTrained immunity as a possible newcomer in autoinflammatory and autoimmune diseases pathophysiology
Beignon, A., Galeotti, C., Ménager, M. M., & Schvartz, A. (2023) · Frontiers in Medicine · doi:10.3389/fmed.2022.1085339 · Cited by 9
KDM4 Regulates the Glycolysis of Hemocytes in the Immune Priming of Eriocheir sinensis
Zhao, X., Qiao, X., Yu, S., Jin, Y., Niu, J., Li, J., Ying-mei, X., Yang, Y., Wang, L., & Song, L. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms252313174 · Cited by 9
González-Pérez, M., Baranda, J., Pérez‐Rodríguez, L., Conde, P., de la Calle‐Fabregat, C., Berges-Buxeda, M. J., Dimitrov, A., Arranz, J., Rius‐Rocabert, S., Zotta, A., et al. (2025) · Cell Reports · doi:10.1016/j.celrep.2025.116202 · Cited by 8
Self-citationMonocyte/macrophage-mediated trained immunity in disease prevention and immunotherapy
Zhang, X., Wang, X., Xu, M., Yuan, J., & Liu, Y. (2026) · Bioactive Materials · doi:10.1016/j.bioactmat.2025.12.044 · Cited by 8
Trained innate immunity and diseases: Bane with the boon
Mishra, S., Arsh, A. M., & Rathore, J. S. (2022) · Clinical Immunology Communications · doi:10.1016/j.clicom.2022.08.004 · Cited by 9
Innate sensing and cellular metabolism: role in fine tuning antiviral immune responses
Ahmed, D., Daraawi, M. A., & Cassol, E. (2023) · Journal of Leukocyte Biology · doi:10.1093/jleuko/qiac011 · Cited by 8
Metadata
- Authors
- Arts, R. J. W., Novakovic, B., ter Horst, R., Carvalho, A., Bekkering, S., Lachmandas, E., Rodrigues, F., Silvestre, R., Cheng, S.-C., Wang, S.-Y., Habibi, E., Gonçalves, L. G., Mesquita, I., Cunha, C., van Laarhoven, A., van de Veerdonk, F. L., Williams, D. L., van der Meer, J. W. M., Logie, C., O'Neill, L. A., Dinarello, C. A., Riksen, N. P., van Crevel, R., Clish, C., Notebaart, R. A., Joosten, L. A. B., Stunnenberg, H. G., Xavier, R. J., & Netea, M. G.
- Affiliations
- Radboud University Medical Center (NL)
- Radboud University Nijmegen (NL)
- University of Minho (PT)
- National Tsing Hua University (TW)
- Instituto de Tecnologia Química e Biológica António Xavier (PT)
- East Tennessee State University (US)
- Trinity College Dublin (IE)
- Broad Institute (US)
- Corresponding author
- Arts, Rob J.W.
- ORCID
- Arts, Rob J.W.
- Novakovic, Boris
- Carvalho, Agostinho
- Bekkering, Siroon
- Rodrigues, Fernando
- Silvestre, Ricardo
- Cheng, Shih-Chin
- Wang, Shuang-Yin
- Habibi, Ehsan
- Gonçalves, Luís G.
- Mesquita, Inês
- Cunha, Cristina
- Williams, David L.
- Logie, Colin
- O'Neill, Luke A.
- Dinarello, Charles A.
- Riksen, Niels P.
- Clish, Clary
- Notebaart, Richard A.
- Joosten, Leo A.B.
- Stunnenberg, Hendrik G.
- Xavier, Ramnik J.
- Netea, Mihai G.
- Venue
- Cell Metabolism
- Publisher
- Elsevier BV
- Published
- 2016-12
- Volume
- 24
- Issue
- 6
- Pages
- 807-819
- ISSN
- 1550-4131 (ISSN-L)
- PMC
- PMC5742541
- OpenAlex
- W2557169014
- Cited by
- 930
- References
- 42
- Citations by year
- 2026: 134 · 2025: 120 · 2024: 101 · 2023: 81 · 2022: 118 · 2021: 111 · 2020: 108 · 2019: 66 · 2018: 62 · 2017: 28 · 2016: 1
- FWCI
- 31.71
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Cell Metabolism (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Socio-Environmental Systems Modeling (acceptedVersion, cc-by-nc-nd)
- Digital Commons - East Tennessee State University (East Tennessee State University) (submittedVersion, cc-by-nc-nd)
- Portuguese National Funding Agency for Science, Research and Technology (RCAAP Project by FCT) (submittedVersion, cc-by-nc-nd)
- Radboud Repository (Radboud University) (submittedVersion)
- Radboud Repository (Radboud University) (submittedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion, cc-by-nc-nd)
- Funders
- ERC Consolidator (310372)
- Spinoza
- Netherlands Organization for Scientific Research
- NHMRC
- CJ Martin Early Career Fellowship
- Dr. Dekker
- Netherlands Heart Foundation (2012T051)
- H2020
- European Union (667837)
- Fundação para a Ciência e Tecnologia (IF/00735/2014, IF/00021/2014, RECI/BBB-BQB/0230/2012, SFRH/BPD/96176/2013)
- FCT (RECI/BBB-BQB/0230/2012)
- Programa Operacional Regional do Norte (ON.2—O Novo Norte)
- Quadro de Referência Estratégico Nacional
- Fundo Europeu de Desenvolvimento Regional
- Projeto Estratégico (LA 26 – 2013–2014 (PEst-C/SAU/LA0026/2013)
- NIH (DK43351, DK097485, GM53522, GM083016, GM119197, C06RR0306551)
- Helmsley Trust
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Immune responses and vaccinations
- Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
- Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
- Keywords
- trained immunity, glutaminolysis, fumarate accumulation, monocytes, β-glucan, epigenetic reprogramming, cholesterol biosynthesis, glycolysis, TCA cycle, immunometabolism, epigenetic rewiring
- MeSH terms
- Cholesterol, Fumarates, Glucose, Glutamine, Glycolysis, Humans, Immune Tolerance, Immunity, Innate, Macrophages, Models, Biological, Pentose Phosphate Pathway, Epigenesis, Genetic, Hypoxia-Inducible Factor 1, alpha Subunit, Proteolysis
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
