Extracellular adenosine mediates a systemic metabolic switch during immune response
Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
25915062
PubMed Central
PMC4411001
DOI
10.1371/journal.pbio.1002135
PII: PBIOLOGY-D-14-04288
Knihovny.cz E-zdroje
- MeSH
- adenosin fyziologie MeSH
- Drosophila imunologie metabolismus parazitologie MeSH
- imunitní systém fyziologie MeSH
- interakce hostitele a parazita MeSH
- sršňovití fyziologie MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- adenosin MeSH
Immune defense is energetically costly, and thus an effective response requires metabolic adaptation of the organism to reallocate energy from storage, growth, and development towards the immune system. We employ the natural infection of Drosophila with a parasitoid wasp to study energy regulation during immune response. To combat the invasion, the host must produce specialized immune cells (lamellocytes) that destroy the parasitoid egg. We show that a significant portion of nutrients are allocated to differentiating lamellocytes when they would otherwise be used for development. This systemic metabolic switch is mediated by extracellular adenosine released from immune cells. The switch is crucial for an effective immune response. Preventing adenosine transport from immune cells or blocking adenosine receptor precludes the metabolic switch and the deceleration of development, dramatically reducing host resistance. Adenosine thus serves as a signal that the "selfish" immune cells send during infection to secure more energy at the expense of other tissues.
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Fong YM, Marano M a, Moldawer LL, Wei H, Calvano SE, Kenney JS, et al. The acute splanchnic and peripheral tissue metabolic response to endotoxin in humans. J Clin Invest. 1990;85: 1896–1904. PubMed PMC
Straub RH, Cutolo M, Buttgereit F, Pongratz G. Energy regulation and neuroendocrine-immune control in chronic inflammatory diseases. J Intern Med. 2010;267: 543–560. 10.1111/j.1365-2796.2010.02218.x PubMed DOI
Cheng S-C, Quintin J, Cramer RA, Shepardson KM, Saeed S, Kumar V, et al. mTOR- and HIF-1α–mediated aerobic glycolysis as metabolic basis for trained immunity. Science. 2014;345: 1250684 10.1126/science.1250684 PubMed DOI PMC
Delmastro-Greenwood MM, Piganelli JD. Changing the energy of an immune response. Am J Clin Exp Immunol. 2013;2: 30–54. PubMed PMC
Pfeiffer T, Schuster S, Bonhoeffer S. Cooperation and competition in the evolution of ATP-producing pathways. Science. 2001;292: 504–507. PubMed
Clark RI, Tan SWS, Péan CB, Roostalu U, Vivancos V, Bronda K, et al. MEF2 Is an In Vivo Immune-Metabolic Switch. Cell. 2013;155: 435–447. 10.1016/j.cell.2013.09.007 PubMed DOI PMC
Hartman ZC, Kiang A, Everett RS, Serra D, Yang XY, Clay TM, et al. Adenovirus infection triggers a rapid, MyD88-regulated transcriptome response critical to acute-phase and adaptive immune responses in vivo. J Virol. 2007;81: 1796–1812. PubMed PMC
Rynes J, Donohoe CD, Frommolt P, Brodesser S, Jindra M, Uhlirova M. Activating Transcription Factor 3 Regulates Immune and Metabolic Homeostasis. Mol Cell Biol. 2012;32: 3949–3962. 10.1128/MCB.00429-12 PubMed DOI PMC
Yoo J-Y, Desiderio S. Innate and acquired immunity intersect in a global view of the acute-phase response. Proc Natl Acad Sci U S A. 2003;100: 1157–1162. PubMed PMC
Calder PC. Feeding the immune system. Proc Nutr Soc. 2013;72: 299–309. 10.1017/S0029665113001286 PubMed DOI
Matarese G, La Cava A, Sanna V, Lord GM, Lechler RI, Fontana S, et al. Balancing susceptibility to infection and autoimmunity: a role for leptin? Trends Immunol. 2002;23: 182–187. PubMed
Rauw WM. Immune response from a resource allocation perspective. Front Genet. 2012;3: 267–267. 10.3389/fgene.2012.00267 PubMed DOI PMC
Arsenijevic D, Garcia I, Vesin C, Vesin D, Arsenijevic Y, Seydoux J, et al. Differential roles of tumor necrosis factor-a and interferon-g in mouse hypermetabolic and anorectic responses induced by LPS. Eur Cytokine Netw. 2000;11: 662–668. PubMed
Matarese G, La Cava A. The intricate interface between immune system and metabolism. Trends Immunol. 2004;25: 193–200. PubMed
Tracey KJ, Cerami A. Tumor Necrosis Factor and Regulation of Metabolism in Infection: Role of Systemic versus Tissue Levels. Exp Biol Med. 1992;200: 233–239. PubMed
Tsigos C, Papanicolaou DA, Kyrou I, Defensor R, Mitsiadis CS, Chrousos GP. Dose-dependent effects of recombinant human interleukin-6 on glucose regulation. J Clin Endocrinol Metab. 1997;82: 4167–4170. PubMed
Wolowczuk I, Verwaerde C, Viltart O, Delanoye A, Delacre M, Pot B, et al. Feeding our immune system: impact on metabolism. Clin Dev Immunol. 2008;2008: 639803 10.1155/2008/639803 PubMed DOI PMC
Chambers MC, Song KH, Schneider DS. Listeria monocytogenes infection causes metabolic shifts in Drosophila melanogaster. PLoS ONE. 2012;7: e50679 10.1371/journal.pone.0050679 PubMed DOI PMC
Dionne MS, Pham LN, Shirasu-Hiza M, Schneider DS. Akt and FOXO dysregulation contribute to infection-induced wasting in Drosophila. Curr Biol. 2006;16: 1977–1985. PubMed
Dionne M. Immune-metabolic interaction in Drosophila. Fly (Austin). 2014;8: 1–5. PubMed PMC
Hull-Thompson J, Muffat J, Sanchez D, Walker DW, Benzer S, Ganfornina MD, et al. Control of metabolic homeostasis by stress signaling is mediated by the lipocalin NLaz. PLoS Genet. 2009;5: e1000460 10.1371/journal.pgen.1000460 PubMed DOI PMC
Buck LT. Adenosine as a signal for ion channel arrest in anoxia-tolerant organisms. Comp Biochem Physiol Part B. 2004;139: 401–414. PubMed
Newby AC. Adenosine and the concept of “retaliatory metabolites.” Trends Biochem Sci. 1984;9: 42–44.
Bours MJL, Swennen ELR, Di Virgilio F, Cronstein BN, Dagnelie PC. Adenosine 5’-triphosphate and adenosine as endogenous signaling molecules in immunity and inflammation. Pharmacol Ther. 2006;112: 358–404. PubMed
Da Silva CG, Jarzyna R, Specht A, Kaczmarek E. Extracellular nucleotides and adenosine independently activate AMP-activated protein kinase in endothelial cells: involvement of P2 receptors and adenosine transporters. Circ Res. 2006;98: e39–47. PubMed PMC
Fishman P, Bar-Yehuda S, Barer F, Madi L, Multani AS, Pathak S. The A3 Adenosine Receptor as a New Target for Cancer Therapy and Chemoprotection. Exp Cell Res. 2001;269: 230–236. PubMed
Jinka TR, T?ien? ivind, Drew KL. Season primes the brain in an arctic hibernator to facilitate entrance into torpor mediated by adenosine A1 receptors. J Neurosci. 2011;31: 10752–10758. 10.1523/JNEUROSCI.1240-11.2011 PubMed DOI PMC
Krumschnabel G, Biasi C, Wieser W. Action of adenosine on energetics, protein synthesis and K(+) homeostasis in teleost hepatocytes. J Exp Biol. 2000;203: 2657–2665. PubMed
Pék M, Lutz PL. Role for adenosine in channel arrest in the anoxic turtle brain. J Exp Biol. 1997;200: 1913–1917. PubMed
Cortés D, Guinzberg R, Villalobos-Molina R, Piña E. Evidence that endogenous inosine and adenosine-mediated hyperglycaemia during ischaemia–reperfusion through A3 adenosine receptors. Auton Autacoid Pharmacol. 2009;29: 157–164. 10.1111/j.1474-8665.2009.00443.x PubMed DOI
Martin C, Leone M, Viviand X, Ayem ML, Guieu R. High adenosine plasma concentration as a prognostic index for outcome in patients with septic shock. Crit Care Med. 2000;28: 3198–3202. PubMed
Kumar V, Sharma A. Adenosine: an endogenous modulator of innate immune system with therapeutic potential. Eur J Pharmacol. 2009;616: 7–15. 10.1016/j.ejphar.2009.05.005 PubMed DOI
Dolezal T, Dolezelova E, Zurovec M, Bryant PJ. A role for adenosine deaminase in Drosophila larval development. PLoS Biol. 2005;3: e201 PubMed PMC
Dolezelova E, Nothacker H-P, Civelli O, Bryant PJ, Zurovec M. A Drosophila adenosine receptor activates cAMP and calcium signaling. Insect Biochem Mol Biol. 2007;37: 318–329. PubMed
Fenckova M, Hobizalova R, Fric ZF, Dolezal T. Functional characterization of ecto-5’-nucleotidases and apyrases in Drosophila melanogaster. Insect Biochem Mol Biol. 2011;41: 956–967. 10.1016/j.ibmb.2011.09.005 PubMed DOI
Knight D, Harvey PJ, Iliadi KG, Klose MK, Iliadi N, Dolezelova E, et al. Equilibrative nucleoside transporter 2 regulates associative learning and synaptic function in Drosophila. J Neurosci Off J Soc Neurosci. 2010;30: 5047–5057. PubMed PMC
Zurovec M, Dolezal T, Gazi M, Pavlova E, Bryant PJ. Adenosine deaminase-related growth factors stimulate cell proliferation in Drosophila by depleting extracellular adenosine. Proc Natl Acad Sci U S A. 2002;99: 4403–4408. PubMed PMC
Zuberova M, Fenckova M, Simek P, Janeckova L, Dolezal T. Increased extracellular adenosine in Drosophila that are deficient in adenosine deaminase activates a release of energy stores leading to wasting and death. Dis Model Mech. 2010;3: 773–784. 10.1242/dmm.005389 PubMed DOI
Novakova M, Dolezal T. Expression of Drosophila adenosine deaminase in immune cells during inflammatory response. PLoS ONE. 2011;6: e17741 10.1371/journal.pone.0017741 PubMed DOI PMC
Keebaugh ES, Schlenke TA. Insights from natural host–parasite interactions: The Drosophila model. Dev Comp Immunol. 2014;42: 111–123. 10.1016/j.dci.2013.06.001 PubMed DOI PMC
Krzemien J, Oyallon J, Crozatier M, Vincent A. Hematopoietic progenitors and hemocyte lineages in the Drosophila lymph gland. Dev Biol. 2010;346: 310–319. 10.1016/j.ydbio.2010.08.003 PubMed DOI
Kacsoh BZ, Schlenke TA. High Hemocyte Load Is Associated with Increased Resistance against Parasitoids in Drosophila suzukii, a Relative of D. melanogaster. PLoS ONE. 2012;7: e34721 10.1371/journal.pone.0034721 PubMed DOI PMC
Sorrentino RP, Melk JP, Govind S. Genetic Analysis of Contributions of Dorsal Group and JAK-Stat92E Pathway Genes to Larval Hemocyte Concentration and the Egg Encapsulation Response in Drosophila. Genetics. 2004;166: 1343–1356. PubMed PMC
Reyes-DelaTorre A, Teresa M, Rafael J. Carbohydrate Metabolism in Drosophila: Reliance on the Disaccharide Trehalose. In: Chang C-F, editor. Carbohydrates—Comprehensive Studies on Glycobiology and Glycotechnology. InTech; 2012. Available: http://www.intechopen.com/books/carbohydrates-comprehensive-studies-on-glycobiology-and-glycotechnology/carbohydrate-metabolism-in-drosophila-reliance-on-the-disaccharide-trehalose
Ayres JS, Schneider DS. The role of anorexia in resistance and tolerance to infections in Drosophila. PLoS Biol. 2009;7: e1000150–e1000150. 10.1371/journal.pbio.1000150 PubMed DOI PMC
Machado J, Abdulla P, Hanna WJB, Hilliker AJ, Coe IR. Genomic analysis of nucleoside transporters in Diptera and functional characterization of DmENT2, a Drosophila equilibrative nucleoside transporter. Physiol Genomics. 2007;28: 337–347. PubMed
Brand a H, Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Dev Camb Engl. 1993;118: 401–415. PubMed
Peters A, Schweiger U, Pellerin L, Hubold C, Oltmanns KM, Conrad M, et al. The selfish brain: competition for energy resources. Neurosci Biobehav Rev. 2004;28: 143–180. PubMed
Straub RH. Insulin resistance, selfish brain, and selfish immune system: an evolutionarily positively selected program used in chronic inflammatory diseases. Arthritis Res Ther. 2014;16: S4 10.1186/ar4688 PubMed DOI PMC
Mondal BC, Mukherjee T, Mandal L, Evans CJ, Sinenko SA, Martinez-Agosto JA, et al. Interaction between differentiating cell- and niche-derived signals in hematopoietic progenitor maintenance. Cell. 2011;147: 1589–1600. 10.1016/j.cell.2011.11.041 PubMed DOI PMC
Morin-Poulard I, Vincent A, Crozatier M. The Drosophila JAK-STAT pathway in blood cell formation and immunity. JAK-STAT. 2013;2: e25700 10.4161/jkst.25700 PubMed DOI PMC
Makki R, Meister M, Pennetier D, Ubeda J-M, Braun A, Daburon V, et al. A short receptor downregulates JAK/STAT signalling to control the Drosophila cellular immune response. PLoS Biol. 2010;8: e1000441–e1000441. 10.1371/journal.pbio.1000441 PubMed DOI PMC
Andersen S. The roles of insulin and hyperglycemia in sepsis pathogenesis. J Leukoc Biol. 2004;75: 413–421. PubMed
Faulhaber-Walter R, Jou W, Mizel D, Li L, Zhang J, Kim SM, et al. Impaired Glucose Tolerance in the Absence of Adenosine A1 Receptor Signaling. Diabetes. 2011;60: 2578–2587. 10.2337/db11-0058 PubMed DOI PMC
Figler RA, Wang G, Srinivasan S, Jung DY, Zhang Z, Pankow JS, et al. Links Between Insulin Resistance, Adenosine A2B Receptors, and Inflammatory Markers in Mice and Humans. Diabetes. 2011;60: 669–679. 10.2337/db10-1070 PubMed DOI PMC
Németh ZH, Csóka B, Wilmanski J, Xu D, Lu Q, Ledent C, et al. Adenosine A2A Receptor Inactivation Increases Survival in Polymicrobial Sepsis. J Immunol. 2006;176: 5616–5626. PubMed PMC
Sullivan GW, Fang G, Linden J, Scheld WM. A2A Adenosine Receptor Activation Improves Survival in Mouse Models of Endotoxemia and Sepsis. J Infect Dis. 2004;189: 1897–1904. PubMed
Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol. 1959;37: 911–917. PubMed
Tennessen JM, Barry W, Cox J, Thummel CS. Methods for studying metabolism in Drosophila. Methods. 2014;68: 105–115. 10.1016/j.ymeth.2014.02.034 PubMed DOI PMC
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