Metabolic Reprogramming of Immune Cells Following Vaccination: From Metabolites to Personalized Vaccinology
- Autores: Mussap M.1, Puddu M.2, Fanos V.2
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Afiliações:
- Department of Surgical Sciences, School of Medicine,, University of Cagliari
- Departmernt of Surgical Sciences, School of Medicine, University of Cagliari
- Edição: Volume 31, Nº 9 (2024)
- Páginas: 1046-1068
- Seção: Anti-Infectives and Infectious Diseases
- URL: https://permmedjournal.ru/0929-8673/article/view/645197
- DOI: https://doi.org/10.2174/0929867330666230509110108
- ID: 645197
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Resumo
Identifying metabolic signatures induced by the immune response to vaccines allows one to discriminate vaccinated from non-vaccinated subjects and decipher the molecular mechanisms associated with the host immune response. This review illustrates and discusses the results of metabolomics-based studies on the innate and adaptive immune response to vaccines, long-term functional reprogramming (immune memory), and adverse reactions. Glycolysis is not overexpressed by vaccines, suggesting that the immune cell response to vaccinations does not require rapid energy availability as necessary during an infection. Vaccines strongly impact lipids metabolism, including saturated or unsaturated fatty acids, inositol phosphate, and cholesterol. Cholesterol is strategic for synthesizing 25-hydroxycholesterol in activated macrophages and dendritic cells and stimulates the conversion of macrophages and T cells in M2 macrophage and Treg, respectively. In conclusion, the large-scale application of metabolomics enables the identification of candidate predictive biomarkers of vaccine efficacy/tolerability.
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Sobre autores
Michele Mussap
Department of Surgical Sciences, School of Medicine,, University of Cagliari
Autor responsável pela correspondência
Email: info@benthamscience.net
Melania Puddu
Departmernt of Surgical Sciences, School of Medicine, University of Cagliari
Email: info@benthamscience.net
Vassilios Fanos
Departmernt of Surgical Sciences, School of Medicine, University of Cagliari
Email: info@benthamscience.net
Bibliografia
- Domínguez-Andrés, J.; van Crevel, R.; Divangahi, M.; Netea, M.G. Designing the next generation of vaccines: Relevance for lics. MBio, 2020, 11(6), e02616-20. doi: 10.1128/mBio.02616-20 PMID: 33443120
- Mayer, A.; Balasubramanian, V.; Walczak, A.M.; Mora, T. How a well-adapting immune system remembers. Proc. Natl. Acad. Sci., 2019, 116(18), 8815-23. doi: 10.1073/pnas.1812810116
- Netea, M.G.; Domínguez-Andrés, J.; Barreiro, L.B.; Chavakis, T.; Divangahi, M.; Fuchs, E.; Joosten, L.A.B.; van der Meer, J.W.M.; Mhlanga, M.M.; Mulder, W.J.M.; Riksen, N.P.; Schlitzer, A.; Schultze, J.L.; Stabell Benn, C.; Sun, J.C.; Xavier, R.J.; Latz, E. Defining trained immunity and its role in health and disease. Nat. Rev. Immunol., 2020, 20(6), 375-388. doi: 10.1038/s41577-020-0285-6 PMID: 32132681
- Dominguez-Andres, J.; Netea, M.G. Long-term reprogramming of the innate immune system. J. Leukoc. Biol., 2019, 105(2), 329-338. doi: 10.1002/JLB.MR0318-104R PMID: 29999546
- Sánchez-Ramón, S.; Conejero, L.; Netea, M.G.; Sancho, D.; Palomares, Ó.; Subiza, J.L. Trained immunity-based vaccines: A new paradigm for the development of broad- spectrum anti-infectious formulations. Front. Immunol., 2018, 9, 2936. doi: 10.3389/fimmu.2018.02936 PMID: 30619296
- Netea, M.G.; Giamarellos-Bourboulis, E.J.; Domínguez-Andrés, J.; Curtis, N.; van Crevel, R.; van de Veerdonk, F.L.; Bonten, M. Trained immunity: A tool for reducing susceptibility to and the severity of SARS-CoV-2 infection Cell, 2020, 181(5), 969-77. doi: 10.1016/j.cell.2020.04.042
- Pinti, M.; Appay, V.; Campisi, J.; Frasca, D.; Fülöp, T.; Sauce, D.; Larbi, A.; Weinberger, B.; Cossarizza, A. Aging of the immune system: Focus on inflammation and vaccination. Eur. J. Immunol., 2016, 46(10), 2286-2301. doi: 10.1002/eji.201546178 PMID: 27595500
- Diray-Arce, J.; Conti, M.G.; Petrova, B.; Kanarek, N.; Angelidou, A.; Levy, O. Integrative metabolomics to identify molecular signatures of responses to vaccines and infections. Metabolites, 2020, 10(12), 492. doi: 10.3390/metabo10120492 PMID: 33266347
- Voss, K.; Hong, H.S.; Bader, J.E.; Sugiura, A.; Lyssiotis, C.A.; Rathmell, J.C. A guide to interrogating immunometabolism. Nat. Rev. Immunol., 2021, 21(10), 637-652. doi: 10.1038/s41577-021-00529-8 PMID: 33859379
- Mussap, M.; Noto, A.; Piras, C.; Atzori, L.; Fanos, V. Slotting metabolomics into routine precision medicine. Expert Rev. Precis. Med. Drug Dev., 2021, 6(3), 173-187. doi: 10.1080/23808993.2021.1911639
- Poland, G.A.; Ovsyannikova, I.G.; Kennedy, R.B. Personalized vaccinology: A review. Vaccine, 2018, 36(36), 5350-5357. doi: 10.1016/j.vaccine.2017.07.062 PMID: 28774561
- ONeill, L.A.J.; Kishton, R.J.; Rathmell, J. A guide to immunometabolism for immunologists. Nat. Rev. Immunol., 2016, 16(9), 553-565. doi: 10.1038/nri.2016.70 PMID: 27396447
- Sun, L.; Yang, X.; Yuan, Z.; Wang, H. Metabolic reprogramming in immune response and tissue inflammation. Arterioscler. Thromb. Vasc. Biol., 2020, 40(9), 1990-2001. doi: 10.1161/ATVBAHA.120.314037 PMID: 32698683
- Shen, W.; Gao, C.; Cueto, R.; Liu, L.; Fu, H.; Shao, Y.; Yang, W.Y.; Fang, P.; Choi, E.T.; Wu, Q.; Yang, X.; Wang, H. Homocysteine-methionine cycle is a metabolic sensor system controlling methylation-regulated pathological signaling. Redox Biol., 2020, 28, 101322. doi: 10.1016/j.redox.2019.101322 PMID: 31605963
- Cameron, A.M.; Lawless, S.J.; Pearce, E.J. Metabolism and acetylation in innate immune cell function and fate. Semin. Immunol., 2016, 28(5), 408-416. doi: 10.1016/j.smim.2016.10.003 PMID: 28340958
- Rodríguez-Prados, J.C.; Través, P.G.; Cuenca, J.; Rico, D.; Aragonés, J.; Martín-Sanz, P.; Cascante, M.; Boscá, L. Substrate fate in activated macrophages: A comparison between innate, classic, and alternative activation. J. Immunol., 2010, 185(1), 605-614. doi: 10.4049/jimmunol.0901698 PMID: 20498354
- Galván-Peña, S.; ONeill, L.A. Metabolic reprograming in macrophage polarization. Front. Immunol., 2014, 5, 420. doi: 10.3389/fimmu.2014.00420 PMID: 25228902
- 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.; ONeill, 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. Glutaminolysis and fumarate accumulation integrate immunometabolic and epigenetic programs in trained immunity. Cell Metab., 2016, 24(6), 807-819. doi: 10.1016/j.cmet.2016.10.008 PMID: 27866838
- Netea, M.G.; Joosten, L.A.B.; Latz, E.; Mills, K.H.G.; Natoli, G.; Stunnenberg, H.G.; ONeill, L.A.J.; Xavier, R.J. Trained immunity: A program of innate immune memory in health and disease. Science, 2016, 352(6284), aaf1098. doi: 10.1126/science.aaf1098 PMID: 27102489
- Riksen, N.P.; Netea, M.G. Immunometabolic control of trained immunity. Mol. Aspects Med., 2021, 77, 100897. doi: 10.1016/j.mam.2020.100897 PMID: 32891423
- Haschemi, A.; Kosma, P.; Gille, L.; Evans, C.R.; Burant, C.F.; Starkl, P.; Knapp, B.; Haas, R.; Schmid, J.A.; Jandl, C.; Amir, S.; Lubec, G.; Park, J.; Esterbauer, H.; Bilban, M.; Brizuela, L.; Pospisilik, J.A.; Otterbein, L.E.; Wagner, O. The sedoheptulose kinase CARKL directs macrophage polarization through control of glucose metabolism. Cell Metab., 2012, 15(6), 813-826. doi: 10.1016/j.cmet.2012.04.023 PMID: 22682222
- OSullivan, D.; van der Windt, G.J.W.; Huang, S.C.C.; Curtis, J.D.; Chang, C.H.; Buck, M.D.; Qiu, J.; Smith, A.M.; Lam, W.Y.; DiPlato, L.M.; Hsu, F.F.; Birnbaum, M.J.; Pearce, E.J.; Pearce, E.L. Memory CD8(+) T cells use cell-intrinsic lipolysis to support the metabolic programming necessary for development. Immunity, 2014, 41(1), 75-88. doi: 10.1016/j.immuni.2014.06.005 PMID: 25001241
- Hertz, L.; Hertz, E. Cataplerotic TCA cycle flux determined as glutamate-sustained oxygen consumption in primary cultures of astrocytes. Neurochem. Int., 2003, 43(4-5), 355-361. doi: 10.1016/S0197-0186(03)00022-6 PMID: 12742079
- Ferreira, A.V.; Domiguéz-Andrés, J.; Netea, M.G. The role of cell metabolism in innate immune memory. J. Innate Immun., 2022, 14(1), 42-50. doi: 10.1159/000512280 PMID: 33378755
- Schebb, N.H.; Kühn, H.; Kahnt, A.S.; Rund, K.M.; ODonnell, V.B.; Flamand, N.; Peters-Golden, M.; Jakobsson, P.J.; Weylandt, K.H.; Rohwer, N.; Murphy, R.C.; Geisslinger, G.; FitzGerald, G.A.; Hanson, J.; Dahlgren, C.; Alnouri, M.W.; Offermanns, S.; Steinhilber, D. Formation, signaling and occurrence of specialized pro-resolving lipid mediatorswhat is the evidence so far? Front. Pharmacol., 2022, 13, 838782. doi: 10.3389/fphar.2022.838782 PMID: 35308198
- Bosch, M.; Sánchez-Álvarez, M.; Fajardo, A.; Kapetanovic, R.; Steiner, B.; Dutra, F.; Moreira, L.; López, J.A.; Campo, R.; Marí, M.; Morales-Paytuví, F.; Tort, O.; Gubern, A.; Templin, R.M.; Curson, J.E.B.; Martel, N.; Català, C.; Lozano, F.; Tebar, F.; Enrich, C.; Vázquez, J.; Del Pozo, M.A.; Sweet, M.J.; Bozza, P.T.; Gross, S.P.; Parton, R.G.; Pol, A. Mammalian lipid droplets are innate immune hubs integrating cell metabolism and host defense. Science, 2020, 370(6514), eaay8085. doi: 10.1126/science.aay8085 PMID: 33060333
- Hagan, T.; Cortese, M.; Rouphael, N.; Boudreau, C.; Linde, C.; Maddur, M.S.; Das, J.; Wang, H.; Guthmiller, J.; Zheng, N.Y.; Huang, M.; Uphadhyay, A.A.; Gardinassi, L.; Petitdemange, C.; McCullough, M.P.; Johnson, S.J.; Gill, K.; Cervasi, B.; Zou, J.; Bretin, A.; Hahn, M.; Gewirtz, A.T.; Bosinger, S.E.; Wilson, P.C.; Li, S.; Alter, G.; Khurana, S.; Golding, H.; Pulendran, B. Antibiotics- Driven gut microbiome perturbation alters immunity to vaccines in humans. Cell, 2019, 178(6), 1313-1328.e13. doi: 10.1016/j.cell.2019.08.010 PMID: 31491384
- Goll, J.B.; Li, S.; Edwards, J.L.; Bosinger, S.E.; Jensen, T.L.; Wang, Y.; Hooper, W.F.; Gelber, C.E.; Sanders, K.L.; Anderson, E.J.; Rouphael, N.; Natrajan, M.S.; Johnson, R.A.; Sanz, P.; Hoft, D.; Mulligan, M.J. Transcriptomic and metabolic responses to a live-attenuated Francisella tularensis vaccine. Vaccines, 2020, 8(3), 412. doi: 10.3390/vaccines8030412 PMID: 32722194
- Khan, A.; Shin, O.S.; Na, J.; Kim, J.K.; Seong, R.K.; Park, M.S.; Noh, J.Y.; Song, J.Y.; Cheong, H.J.; Park, Y.H.; Kim, W.J. A systems vaccinology approach reveals the mechanisms of immunogenic responses to hantavax vaccination in humans. Sci. Rep., 2019, 9(1), 4760. doi: 10.1038/s41598-019-41205-1 PMID: 30886186
- Li, S.; Sullivan, N.L.; Rouphael, N.; Yu, T.; Banton, S.; Maddur, M.S.; McCausland, M.; Chiu, C.; Canniff, J.; Dubey, S.; Liu, K.; Tran, V.; Hagan, T.; Duraisingham, S.; Wieland, A.; Mehta, A.K.; Whitaker, J.A.; Subramaniam, S.; Jones, D.P.; Sette, A.; Vora, K.; Weinberg, A.; Mulligan, M.J.; Nakaya, H.I.; Levin, M.; Ahmed, R.; Pulendran, B. Metabolic phenotypes of response to vaccination in humans. Cell, 2017, 169(5), 862-877.e17. doi: 10.1016/j.cell.2017.04.026 PMID: 28502771
- Wang, Y.; Wang, X.; Luu, L.D.W.; Chen, S.; Jin, F.; Wang, S.; Huang, X.; Wang, L.; Zhou, X.; Chen, X.; Cui, X.; Li, J.; Tai, J.; Zhu, X. Proteomic and metabolomic signatures associated with the immune response in healthy individuals immunized with an inactivated SARS-CoV-2 vaccine. Front. Immunol., 2022, 13, 848961. doi: 10.3389/fimmu.2022.848961 PMID: 35686122
- He, M.; Huang, Y.; Wang, Y.; Liu, J.; Han, M.; Xiao, Y.; Zhang, N.; Gui, H.; Qiu, H.; Cao, L.; Jia, W.; Huang, S. Metabolomics-based investigation of SARS-CoV-2 vaccination (Sinovac) reveals an immune-dependent metabolite biomarker. Front. Immunol., 2022, 13, 954801. doi: 10.3389/fimmu.2022.954801 PMID: 36248825
- Choi, I.; Son, H.; Baek, J.H. Tricarboxylic Acid (TCA) cycle intermediates: Regulators of immune responses. Life, 2021, 11(1), 69. doi: 10.3390/life11010069 PMID: 33477822
- Williams, N.C.; ONeill, L.A.J. A role for the krebs cycle intermediate citrate in metabolic reprogramming in innate immunity and inflammation. Front. Immunol., 2018, 9, 141. doi: 10.3389/fimmu.2018.00141 PMID: 29459863
- Langston, P.K.; Shibata, M.; Horng, T. Metabolism supports macrophage activation. Front. Immunol., 2017, 8, 61. doi: 10.3389/fimmu.2017.00061 PMID: 28197151
- Hooftman, A.; ONeill, L.A.J. The immunomodulatory potential of the metabolite itaconate. Trends Immunol., 2019, 40(8), 687-698. doi: 10.1016/j.it.2019.05.007 PMID: 31178405
- Hooftman, A.; Angiari, S.; Hester, S.; Corcoran, S.E.; Runtsch, M.C.; Ling, C.; Ruzek, M.C.; Slivka, P.F.; McGettrick, A.F.; Banahan, K.; Hughes, M.M.; Irvine, A.D.; Fischer, R.; ONeill, L.A.J. The immunomodulatory metabolite itaconate modifies nlrp3 and inhibits inflammasome activation. Cell Metab., 2020, 32(3), 468-478.e7. doi: 10.1016/j.cmet.2020.07.016 PMID: 32791101
- 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.; Zheng, L.; Gardet, A.; Tong, Z.; Jany, S.S.; Corr, S.C.; Haneklaus, M.; Caffrey, B.E.; Pierce, K.; Walmsley, S.; Beasley, F.C.; Cummins, E.; Nizet, V.; Whyte, M.; Taylor, C.T.; Lin, H.; Masters, S.L.; Gottlieb, E.; Kelly, V.P.; Clish, C.; Auron, P.E.; Xavier, R.J.; ONeill, L.A.J. Succinate is an inflammatory signal that induces IL-1β through HIF-1α. Nature, 2013, 496(7444), 238-242. doi: 10.1038/nature11986 PMID: 23535595
- Liu, P.S.; Wang, H.; Li, X.; Chao, T.; Teav, T.; Christen, S.; Di Conza, G.; Cheng, W.C.; Chou, C.H.; Vavakova, M.; Muret, C.; Debackere, K.; Mazzone, M.; Huang, H.D.; Fendt, S.M.; Ivanisevic, J.; Ho, P.C. α-ketoglutarate orchestrates macrophage activation through metabolic and epigenetic reprogramming. Nat. Immunol., 2017, 18(9), 985-994. doi: 10.1038/ni.3796 PMID: 28714978
- Jha, A.K.; Huang, S.C.C.; Sergushichev, A.; Lampropoulou, V.; Ivanova, Y.; Loginicheva, E.; Chmielewski, K.; Stewart, K.M.; Ashall, J.; Everts, B.; Pearce, E.J.; Driggers, E.M.; Artyomov, M.N. Network integration of parallel metabolic and transcriptional data reveals metabolic modules that regulate macrophage polarization. Immunity, 2015, 42(3), 419-430. doi: 10.1016/j.immuni.2015.02.005 PMID: 25786174
- Mills, E.; ONeill, L.A.J. Succinate: A metabolic signal in inflammation. Trends Cell Biol., 2014, 24(5), 313-320. doi: 10.1016/j.tcb.2013.11.008 PMID: 24361092
- Domínguez-Andrés, J.; Joosten, L.A.B.; Netea, M.G. Induction of innate immune memory: The role of cellular metabolism. Curr. Opin. Immunol., 2019, 56, 10-16. doi: 10.1016/j.coi.2018.09.001 PMID: 30240964
- Wang, R.; Green, D.R. Metabolic reprogramming and metabolic dependency in T cells. Immunol. Rev., 2012, 249(1), 14-26. doi: 10.1111/j.1600-065X.2012.01155.x PMID: 22889212
- Wang, R.; Dillon, C.P.; Shi, L.Z.; Milasta, S.; Carter, R.; Finkelstein, D.; McCormick, L.L.; Fitzgerald, P.; Chi, H.; Munger, J.; Green, D.R. The transcription factor Myc controls metabolic reprogramming upon T lymphocyte activation. Immunity, 2011, 35(6), 871-882. doi: 10.1016/j.immuni.2011.09.021 PMID: 22195744
- Lochner, M.; Berod, L.; Sparwasser, T. Fatty acid metabolism in the regulation of T cell function. Trends Immunol., 2015, 36(2), 81-91. doi: 10.1016/j.it.2014.12.005 PMID: 25592731
- Miles, E.A.; Childs, C.E.; Calder, P.C. Long-Chain Polyunsaturated Fatty Acids (LCPUFAs) and the developing immune system: A narrative review. Nutrients, 2021, 13(1), 247. doi: 10.3390/nu13010247 PMID: 33467123
- Kalinski, P. Regulation of immune responses by prostaglandin E2. J. Immunol., 2012, 188(1), 21-28. doi: 10.4049/jimmunol.1101029 PMID: 22187483
- Chou, C.H.; Mohanty, S.; Kang, H.A.; Kong, L.; Avila- Pacheco, J.; Joshi, S.R.; Ueda, I.; Devine, L.; Raddassi, K.; Pierce, K.; Jeanfavre, S.; Bullock, K.; Meng, H.; Clish, C.; Santori, F.R.; Shaw, A.C.; Xavier, R.J. Metabolomic and transcriptomic signatures of influenza vaccine response in healthy young and older adults. Aging Cell, 2022, 21(9), e13682. doi: 10.1111/acel.13682 PMID: 35996998
- Maner-Smith, K.M.; Goll, J.B.; Khadka, M.; Jensen, T.L.; Colucci, J.K.; Gelber, C.E.; Albert, C.J.; Bosinger, S.E.; Franke, J.D.; Natrajan, M.; Rouphael, N.; Johnson, R.A.; Sanz, P.; Anderson, E.J.; Hoft, D.F.; Mulligan, M.J.; Ford, D.A.; Ortlund, E.A. Alterations in the human plasma lipidome in response to tularemia vaccination. Vaccines, 2020, 8(3), 414. doi: 10.3390/vaccines8030414 PMID: 32722213
- Diray-Arce, J.; Angelidou, A.; Jensen, K.J.; Conti, M.G.; Kelly, R.S.; Pettengill, M.A.; Liu, M.; van Haren, S.D.; McCulloch, S.D.; Michelloti, G.; Idoko, O.; Kollmann, T.R.; Kampmann, B.; Steen, H.; Ozonoff, A.; Lasky-Su, J.; Benn, C.S.; Levy, O. Bacille Calmette-Guérin vaccine reprograms human neonatal lipid metabolism in vivo and in vitro. Cell Rep., 2022, 39(5), 110772. doi: 10.1016/j.celrep.2022.110772 PMID: 35508141
- ODonnell, V.B.; Rossjohn, J.; Wakelam, M.J.O. Phospholipid signaling in innate immune cells. J. Clin. Invest., 2018, 128(7), 2670-2679. doi: 10.1172/JCI97944 PMID: 29683435
- Cathcart, M.K. Signal-activated phospholipase regulation of leukocyte chemotaxis. J. Lipid Res., 2009, 50(Suppl)(Suppl.), S231-S236. doi: 10.1194/jlr.R800096-JLR200 PMID: 19109234
- Tan, S.T.; Ramesh, T.; Toh, X.R.; Nguyen, L.N. Emerging roles of lysophospholipids in health and disease. Prog. Lipid Res., 2020, 80, 101068. doi: 10.1016/j.plipres.2020.101068 PMID: 33068601
- Knuplez, E.; Marsche, G. An updated review of pro- and anti-inflammatory properties of plasma lysophosphatidylcholines in the vascular system. Int. J. Mol. Sci., 2020, 21(12), 4501. doi: 10.3390/ijms21124501 PMID: 32599910
- Dagla, I.; Iliou, A.; Benaki, D.; Gikas, E.; Mikros, E.; Bagratuni, T.; Kastritis, E.; Dimopoulos, M.A.; Terpos, E.; Tsarbopoulos, A. Plasma metabolomic alterations induced by COVID-19 vaccination reveal putative biomarkers reflecting the immune response. Cells, 2022, 11(7), 1241. doi: 10.3390/cells11071241 PMID: 35406806
- Ghini, V.; Maggi, L.; Mazzoni, A.; Spinicci, M.; Zammarchi, L.; Bartoloni, A.; Annunziato, F.; Turano, P. Serum NMR profiling reveals differential alterations in the lipoproteome induced by Pfizer-BioNTech vaccine in COVID-19 recovered subjects and naïve subjects. Front. Mol. Biosci., 2022, 9, 839809. doi: 10.3389/fmolb.2022.839809 PMID: 35480886
- Maceyka, M.; Spiegel, S. Sphingolipid metabolites in inflammatory disease. Nature, 2014, 510(7503), 58-67. doi: 10.1038/nature13475 PMID: 24899305
- Spiegel, S.; Milstien, S. The outs and the ins of sphingosine-1-phosphate in immunity. Nat. Rev. Immunol., 2011, 11(6), 403-415. doi: 10.1038/nri2974 PMID: 21546914
- Hannun, Y.A.; Obeid, L.M. Sphingolipids and their metabolism in physiology and disease. Nat. Rev. Mol. Cell Biol., 2018, 19(3), 175-191. doi: 10.1038/nrm.2017.107 PMID: 29165427
- Arnon, T.I.; Horton, R.M.; Grigorova, I.L.; Cyster, J.G. Visualization of splenic marginal zone B-cell shuttling and follicular B-cell egress. Nature, 2013, 493(7434), 684-688. doi: 10.1038/nature11738 PMID: 23263181
- Walzer, T.; Chiossone, L.; Chaix, J.; Calver, A.; Carozzo, C.; Garrigue-Antar, L.; Jacques, Y.; Baratin, M.; Tomasello, E.; Vivier, E. Natural killer cell trafficking in vivo requires a dedicated sphingosine 1-phosphate receptor. Nat. Immunol., 2007, 8(12), 1337-1344. doi: 10.1038/ni1523 PMID: 17965716
- Gaggini, M.; Pingitore, A.; Vassalle, C. Plasma ceramides pathophysiology, measurements, challenges, and opportunities. Metabolites, 2021, 11(11), 719. doi: 10.3390/metabo11110719 PMID: 34822377
- Reboldi, A.; Dang, E. Cholesterol metabolism in innate and adaptive response. F1000Res, 2018, 7, 1647. doi: 10.12688/f1000research.15500.1
- Fessler, M.B. Regulation of adaptive immunity in health and disease by cholesterol metabolism. Curr. Allergy Asthma Rep., 2015, 15(8), 48. doi: 10.1007/s11882-015-0548-7 PMID: 26149587
- Aguilar-Ballester, M.; Herrero-Cervera, A.; Vinué, Á.; Martínez-Hervás, S.; González-Navarro, H. Impact of cholesterol metabolism in immune cell function and atherosclerosis. Nutrients, 2020, 12(7), 2021. doi: 10.3390/nu12072021 PMID: 32645995
- Kidani, Y.; Elsaesser, H.; Hock, M.B.; Vergnes, L.; Williams, K.J.; Argus, J.P.; Marbois, B.N.; Komisopoulou, E.; Wilson, E.B.; Osborne, T.F.; Graeber, T.G.; Reue, K.; Brooks, D.G.; Bensinger, S.J. Sterol regulatory elementbinding proteins are essential for the metabolic programming of effector T cells and adaptive immunity. Nat. Immunol., 2013, 14(5), 489-499. doi: 10.1038/ni.2570 PMID: 23563690
- Hu, X.; Wang, Y.; Hao, L.Y.; Liu, X.; Lesch, C.A.; Sanchez, B.M.; Wendling, J.M.; Morgan, R.W.; Aicher, T.D.; Carter, L.L.; Toogood, P.L.; Glick, G.D. Sterol metabolism controls TH17 differentiation by generating endogenous RORγ agonists. Nat. Chem. Biol., 2015, 11(2), 141-147. doi: 10.1038/nchembio.1714 PMID: 25558972
- Bekkering, S.; Arts, R.J.W.; Novakovic, B.; Kourtzelis, I.; van der Heijden, C.D.C.C.; Li, Y.; Popa, C.D.; ter Horst, R.; van Tuijl, J.; Netea-Maier, R.T.; van de Veerdonk, F.L.; Chavakis, T.; Joosten, L.A.B.; van der Meer, J.W.M.; Stunnenberg, H.; Riksen, N.P.; Netea, M.G. Metabolic induction of trained immunity through the mevalonate pathway. Cell, 2018, 172(1-2), 135-146.e9. doi: 10.1016/j.cell.2017.11.025 PMID: 29328908
- Griffiths, W.J.; Wang, Y. Oxysterols as lipid mediators: Their biosynthetic genes, enzymes and metabolites. Prostaglandins Other Lipid Mediat., 2020, 147, 106381. doi: 10.1016/j.prostaglandins.2019.106381 PMID: 31698146
- Mutemberezi, V.; Guillemot-Legris, O.; Muccioli, G.G. Oxysterols: From cholesterol metabolites to key mediators. Prog. Lipid Res., 2016, 64, 152-169. doi: 10.1016/j.plipres.2016.09.002 PMID: 27687912
- Reinmuth, L.; Hsiao, C.C.; Hamann, J.; Rosenkilde, M.; Mackrill, J. Multiple targets for oxysterols in their regulation of the immune system. Cells, 2021, 10(8), 2078. doi: 10.3390/cells10082078 PMID: 34440846
- Spann, N.J.; Glass, C.K. Sterols and oxysterols in immune cell function. Nat. Immunol., 2013, 14(9), 893-900. doi: 10.1038/ni.2681 PMID: 23959186
- Dang, E.V.; McDonald, J.G.; Russell, D.W.; Cyster, J.G. Oxysterol restraint of cholesterol synthesis prevents AIM2 inflammasome activation. Cell, 2017, 171(5), 1057-1071.e11. doi: 10.1016/j.cell.2017.09.029 PMID: 29033131
- Zang, R.; Case, J.B.; Yutuc, E.; Ma, X.; Shen, S.; Gomez Castro, M.F.; Liu, Z.; Zeng, Q.; Zhao, H.; Son, J. Cholesterol 25-hydroxylase suppresses SARS-CoV-2 replication by blocking membrane fusion. Proc Natl Acad Sci., 2020, 117(50), 32105-32113. doi: 10.1073/pnas.2012197117
- Wang, S.; Li, W.; Hui, H.; Tiwari, S.K.; Zhang, Q.; Croker, B.A.; Rawlings, S.; Smith, D.; Carlin, A.F.; Rana, T.M. Cholesterol 25-Hydroxylase inhibits SARS-CoV-2 and other coronaviruses by depleting membrane cholesterol. EMBO J., 2020, 39(21), e106057. doi: 10.15252/embj.2020106057 PMID: 32944968
- Kelly, B.; Pearce, E.L. Amino assets: How amino acids support immunity. Cell Metab., 2020, 32(2), 154-175. doi: 10.1016/j.cmet.2020.06.010 PMID: 32649859
- Takahara, T.; Amemiya, Y.; Sugiyama, R.; Maki, M.; Shibata, H. Amino acid-dependent control of mTORC1 signaling: A variety of regulatory modes. J. Biomed. Sci., 2020, 27(1), 87. doi: 10.1186/s12929-020-00679-2 PMID: 32799865
- Li, P.; Wu, G. Important roles of amino acids in immune responses. Br. J. Nutr., 2022, 127(3), 398-402. doi: 10.1017/S0007114521004566 PMID: 34776020
- Holeček, M. Histidine in health and disease: Metabolism, physiological importance, and use as a supplement. Nutrients, 2020, 12(3), 848. doi: 10.3390/nu12030848 PMID: 32235743
- Rath, M.; Müller, I.; Kropf, P.; Closs, E.I.; Munder, M. Metabolism via arginase or nitric oxide synthase: Two competing arginine pathways in macrophages. Front. Immunol., 2014, 5, 532. doi: 10.3389/fimmu.2014.00532 PMID: 25386178
- Sorgdrager, F.J.H.; Naudé, P.J.W.; Kema, I.P.; Nollen, E.A.; Deyn, P.P.D. Tryptophan metabolism in inflammaging: From biomarker to therapeutic target. Front. Immunol., 2019, 10(10), 2565. doi: 10.3389/fimmu.2019.02565 PMID: 31736978
- Lamas, B.; Natividad, J.M.; Sokol, H. Aryl hydrocarbon receptor and intestinal immunity. Mucosal Immunol., 2018, 11(4), 1024-1038. doi: 10.1038/s41385-018-0019-2 PMID: 29626198
- Mezrich, J.D.; Fechner, J.H.; Zhang, X.; Johnson, B.P.; Burlingham, W.J.; Bradfield, C.A. An interaction between kynurenine and the aryl hydrocarbon receptor can generate regulatory T cells. J. Immunol., 2010, 185(6), 3190-3198. doi: 10.4049/jimmunol.0903670 PMID: 20720200
- Nguyen, N.T.; Kimura, A.; Nakahama, T.; Chinen, I.; Masuda, K.; Nohara, K.; Fujii-Kuriyama, Y.; Kishimoto, T. Aryl hydrocarbon receptor negatively regulates dendritic cell immunogenicity via a kynurenine-dependent mechanism. Proc Natl Acad Sci., 2010, 107(46), 19961-6. doi: 10.1073/pnas.1014465107
- Menni, C.; Kastenmüller, G.; Petersen, A.K.; Bell, J.T.; Psatha, M.; Tsai, P.C.; Gieger, C.; Schulz, H.; Erte, I.; John, S.; Brosnan, M.J.; Wilson, S.G.; Tsaprouni, L.; Lim, E.M.; Stuckey, B.; Deloukas, P.; Mohney, R.; Suhre, K.; Spector, T.D.; Valdes, A.M. Metabolomic markers reveal novel pathways of ageing and early development in human populations. Int. J. Epidemiol., 2013, 42(4), 1111-1119. doi: 10.1093/ije/dyt094 PMID: 23838602
- Fanos, V.; Puddu, M.; Mussap, M. OMICS technologies and personalized vaccination in the COVID-19 era. J. Ped. Neo. Ind. Med. , 2022, 11(1), e110114. doi: 10.7363/110114
- Arunachalam, P.S.; Scott, M.K.D.; Hagan, T.; Li, C.; Feng, Y.; Wimmers, F.; Grigoryan, L.; Trisal, M.; Edara, V.V.; Lai, L.; Chang, S.E.; Feng, A.; Dhingra, S.; Shah, M.; Lee, A.S.; Chinthrajah, S.; Sindher, S.B.; Mallajosyula, V.; Gao, F.; Sigal, N.; Kowli, S.; Gupta, S.; Pellegrini, K.; Tharp, G.; Maysel-Auslender, S.; Hamilton, S.; Aoued, H.; Hrusovsky, K.; Roskey, M.; Bosinger, S.E.; Maecker, H.T.; Boyd, S.D.; Davis, M.M.; Utz, P.J.; Suthar, M.S.; Khatri, P.; Nadeau, K.C.; Pulendran, B. Systems vaccinology of the BNT162b2 mRNA vaccine in humans. Nature, 2021, 596(7872), 410-416. doi: 10.1038/s41586-021-03791-x PMID: 34252919
- Karagiannis, F.; Peukert, K.; Surace, L.; Michla, M.; Nikolka, F.; Fox, M.; Weiss, P.; Feuerborn, C.; Maier, P.; Schulz, S.; Al, B.; Seeliger, B.; Welte, T.; David, S.; Grondman, I.; de Nooijer, A.H.; Pickkers, P.; Kleiner, J.L.; Berger, M.M.; Brenner, T.; Putensen, C.; Abdullah, Z.; Latz, E.; Schmidt, S.; Hartmann, G.; Streeck, H.; Kümmerer, B.M.; Kato, H.; Garbi, N.; Netea, M.G.; Hiller, K.; Placek, K.; Bode, C.; Wilhelm, C. Impaired ketogenesis ties metabolism to T cell dysfunction in COVID-19. Nature, 2022, 609(7928), 801-807. doi: 10.1038/s41586-022-05128-8 PMID: 35901960
- McClenathan, B.M.; Stewart, D.A.; Spooner, C.E.; Pathmasiri, W.W.; Burgess, J.P.; McRitchie, S.L.; Choi, Y.S.; Sumner, S.C.J. Metabolites as biomarkers of adverse reactions following vaccination: A pilot study using nuclear magnetic resonance metabolomics. Vaccine, 2017, 35(9), 1238-1245. doi: 10.1016/j.vaccine.2017.01.056 PMID: 28169076
- Sasaki, E.; Kusunoki, H.; Momose, H.; Furuhata, K.; Hosoda, K.; Wakamatsu, K.; Mizukami, T.; Hamaguchi, I. Changes of urine metabolite profiles are induced by inactivated influenza vaccine inoculations in mice. Sci. Rep., 2019, 9(1), 16249. doi: 10.1038/s41598-019-52686-5 PMID: 31700085
- Koeken, V.A.C.M.; Qi, C.; Mourits, V.P.; de Bree, L.C.J.; Moorlag, S.J.C.F.M.; Sonawane, V.; Lemmers, H.; Dijkstra, H.; Joosten, L.A.B.; van Laarhoven, A.; Xu, C.J.; van Crevel, R.; Netea, M.G.; Li, Y. Plasma metabolome predicts trained immunity responses after antituberculosis BCG vaccination. PLoS Biol., 2022, 20(9), e3001765. doi: 10.1371/journal.pbio.3001765 PMID: 36094960
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