Dietary Fiber Confers Protection against Flu by Shaping Ly6c− Patrolling Monocyte Hematopoiesis and CD8+ T Cell Metabolism

Immunity

Volumn 48, Issue 5, 2018, Pages 992-1005.e8

  Trompette, Aurélien ^a   Gollwitzer, Eva S ^a,c   Pattaroni, Céline ^a,d   Lopez Mejia, Isabel C ^b   Riva, Erika ^a   Pernot, Julie ^a   Ubags, Niki ^a   Fajas, Lluis ^b   Nicod, Laurent P ^a   Marsland, Benjamin J ^a,d  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

^c EPFL   (Switzerland)

^d MONASH UNIVERSITY   (Australia)

Author keywords

CD8+ T cells; fiber; hematopoiesis; influenza; metabolism; neutrophils; patrolling monocytes; SCFA

Indexed keywords

CXCL1 CHEMOKINE; SHORT CHAIN FATTY ACID; LY ANTIGEN; LY-6C ANTIGEN, MOUSE; PROTECTIVE AGENT; VOLATILE FATTY ACID;

ADAPTIVE IMMUNITY; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CD8+ T LYMPHOCYTE; CELL METABOLISM; CONTROLLED STUDY; DIETARY FIBER; EFFECTOR CELL; FEMALE; HEMATOPOIESIS; HIGH FIBER DIET; INFLUENZA; INNATE IMMUNITY; MACROPHAGE; MONOCYTE; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; ADMINISTRATION AND DOSAGE; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; DRUG EFFECT; HUMAN; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; ORTHOMYXOVIRUS INFECTION; PHARMACOLOGY;

ADAPTIVE IMMUNITY; ANIMALS; ANTIGENS, LY; CD8-POSITIVE T-LYMPHOCYTES; DIETARY FIBER; FATTY ACIDS, VOLATILE; HEMATOPOIESIS; HUMANS; IMMUNITY, INNATE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; MONOCYTES; ORTHOMYXOVIRIDAE INFECTIONS; PROTECTIVE AGENTS;

EID: 85046816552     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2018.04.022     Document Type: Article

References (55)

1. Aldridge, J.R. Jr., Moseley, C.E., Boltz, D.A., Negovetich, N.J., Reynolds, C., Franks, J., Brown, S.A., Doherty, P.C., Webster, R.G., Thomas, P.G., TNF/iNOS-producing dendritic cells are the necessary evil of lethal influenza virus infection. Proc. Natl. Acad. Sci. USA 106 (2009), 5306–5311.
2. Aoyama, M., Kotani, J., Usami, M., Butyrate and propionate induced activated or non-activated neutrophil apoptosis via HDAC inhibitor activity but without activating GPR-41/GPR-43 pathways. Nutrition 26 (2010), 653–661.
3. Arpaia, N., Campbell, C., Fan, X., Dikiy, S., van der Veeken, J., deRoos, P., Liu, H., Cross, J.R., Pfeffer, K., Coffer, P.J., Rudensky, A.Y., Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature 504 (2013), 451–455.
4. Auffray, C., Fogg, D., Garfa, M., Elain, G., Join-Lambert, O., Kayal, S., Sarnacki, S., Cumano, A., Lauvau, G., Geissmann, F., Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior. Science 317 (2007), 666–670.
5. Auffray, C., Sieweke, M.H., Geissmann, F., Blood monocytes: development, heterogeneity, and relationship with dendritic cells. Annu. Rev. Immunol. 27 (2009), 669–692.
6. Balmer, M.L., Ma, E.H., Bantug, G.R., Grählert, J., Pfister, S., Glatter, T., Jauch, A., Dimeloe, S., Slack, E., Dehio, P., et al. Memory CD8(+) T cells require increased concentrations of acetate induced by stress for optimal function. Immunity 44 (2016), 1312–1324.
7. Basu, S., Hodgson, G., Katz, M., Dunn, A.R., Evaluation of role of G-CSF in the production, survival, and release of neutrophils from bone marrow into circulation. Blood 100 (2002), 854–861.
8. Biondo, C., Mancuso, G., Midiri, A., Signorino, G., Domina, M., Lanza Cariccio, V., Mohammadi, N., Venza, M., Venza, I., Teti, G., Beninati, C., The interleukin-1β/CXCL1/2/neutrophil axis mediates host protection against group B streptococcal infection. Infect. Immun. 82 (2014), 4508–4517.
9. Blad, C.C., Tang, C., Offermanns, S., G protein-coupled receptors for energy metabolites as new therapeutic targets. Nat. Rev. Drug Discov. 11 (2012), 603–619.
10. Brandes, M., Klauschen, F., Kuchen, S., Germain, R.N., A systems analysis identifies a feedforward inflammatory circuit leading to lethal influenza infection. Cell 154 (2013), 197–212.
11. Buck, M.D., O'Sullivan, D., Pearce, E.L., T cell metabolism drives immunity. J. Exp. Med. 212 (2015), 1345–1360.
12. Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., Fierer, N., Peña, A.G., Goodrich, J.K., Gordon, J.I., et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7 (2010), 335–336.
13. Carmody, R.N., Gerber, G.K., Luevano, J.M. Jr., Gatti, D.M., Somes, L., Svenson, K.L., Turnbaugh, P.J., Diet dominates host genotype in shaping the murine gut microbiota. Cell Host Microbe 17 (2015), 72–84.
14. Cham, C.M., Driessens, G., O'Keefe, J.P., Gajewski, T.F., Glucose deprivation inhibits multiple key gene expression events and effector functions in CD8+ T cells. Eur. J. Immunol. 38 (2008), 2438–2450.
15. Chang, P.V., Hao, L., Offermanns, S., Medzhitov, R., The microbial metabolite butyrate regulates intestinal macrophage function via histone deacetylase inhibition. Proc. Natl. Acad. Sci. USA 111 (2014), 2247–2252.
16. Cummings, J.H., Short chain fatty acids in the human colon. Gut 22 (1981), 763–779.
17. Damjanovic, D., Small, C.L., Jeyanathan, M., McCormick, S., Xing, Z., Immunopathology in influenza virus infection: uncoupling the friend from foe. Clin. Immunol. 144 (2012), 57–69.
18. De Filippo, C., Cavalieri, D., Di Paola, M., Ramazzotti, M., Poullet, J.B., Massart, S., Collini, S., Pieraccini, G., Lionetti, P., Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc. Natl. Acad. Sci. USA 107 (2010), 14691–14696.
19. den Besten, G., van Eunen, K., Groen, A.K., Venema, K., Reijngoud, D.J., Bakker, B.M., The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J. Lipid Res. 54 (2013), 2325–2340.
20. DeSantis, T.Z., Hugenholtz, P., Larsen, N., Rojas, M., Brodie, E.L., Keller, K., Huber, T., Dalevi, D., Hu, P., Andersen, G.L., Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol. 72 (2006), 5069–5072.
21. Dienz, O., Rud, J.G., Eaton, S.M., Lanthier, P.A., Burg, E., Drew, A., Bunn, J., Suratt, B.T., Haynes, L., Rincon, M., Essential role of IL-6 in protection against H1N1 influenza virus by promoting neutrophil survival in the lung. Mucosal Immunol. 5 (2012), 258–266.
22. Donohoe, D.R., Garge, N., Zhang, X., Sun, W., O'Connell, T.M., Bunger, M.K., Bultman, S.J., The microbiome and butyrate regulate energy metabolism and autophagy in the mammalian colon. Cell Metab. 13 (2011), 517–526.
23. Edgar, R.C., Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26 (2010), 2460–2461.
24. Fogg, D.K., Sibon, C., Miled, C., Jung, S., Aucouturier, P., Littman, D.R., Cumano, A., Geissmann, F., A clonogenic bone marrow progenitor specific for macrophages and dendritic cells. Science 311 (2006), 83–87.
25. Geissmann, F., Manz, M.G., Jung, S., Sieweke, M.H., Merad, M., Ley, K., Development of monocytes, macrophages, and dendritic cells. Science 327 (2010), 656–661.
26. Holscher, H.D., Caporaso, J.G., Hooda, S., Brulc, J.M., Fahey, G.C. Jr., Swanson, K.S., Fiber supplementation influences phylogenetic structure and functional capacity of the human intestinal microbiome: follow-up of a randomized controlled trial. Am. J. Clin. Nutr. 101 (2015), 55–64.
27. Hu, G.X., Chen, G.R., Xu, H., Ge, R.S., Lin, J., Activation of the AMP activated protein kinase by short-chain fatty acids is the main mechanism underlying the beneficial effect of a high fiber diet on the metabolic syndrome. Med. Hypotheses 74 (2010), 123–126.
28. Jacobs, S.R., Herman, C.E., Maciver, N.J., Wofford, J.A., Wieman, H.L., Hammen, J.J., Rathmell, J.C., Glucose uptake is limiting in T cell activation and requires CD28-mediated Akt-dependent and independent pathways. J. Immunol. 180 (2008), 4476–4486.
29. Kim, C.H., Park, J., Kim, M., Gut microbiota-derived short-chain Fatty acids, T cells, and inflammation. Immune Netw. 14 (2014), 277–288.
30. Kim, M., Qie, Y., Park, J., Kim, C.H., Gut microbial metabolites fuel host antibody responses. Cell Host Microbe 20 (2016), 202–214.
31. Kruger, P., Saffarzadeh, M., Weber, A.N., Rieber, N., Radsak, M., von Bernuth, H., Benarafa, C., Roos, D., Skokowa, J., Hartl, D., Neutrophils: Between host defence, immune modulation, and tissue injury. PLoS Pathog., 11, 2015, e1004651.
32. Labonte, A.C., Tosello-Trampont, A.C., Hahn, Y.S., The role of macrophage polarization in infectious and inflammatory diseases. Mol. Cells 37 (2014), 275–285.
33. Landsman, L., Jung, S., Lung macrophages serve as obligatory intermediate between blood monocytes and alveolar macrophages. J. Immunol. 179 (2007), 3488–3494.
34. Landsman, L., Varol, C., Jung, S., Distinct differentiation potential of blood monocyte subsets in the lung. J. Immunol. 178 (2007), 2000–2007.
35. Le Poul, E., Loison, C., Struyf, S., Springael, J.Y., Lannoy, V., Decobecq, M.E., Brezillon, S., Dupriez, V., Vassart, G., Van Damme, J., et al. Functional characterization of human receptors for short chain fatty acids and their role in polymorphonuclear cell activation. J. Biol. Chem. 278 (2003), 25481–25489.
36. Marko, A.J., Miller, R.A., Kelman, A., Frauwirth, K.A., Induction of glucose metabolism in stimulated T lymphocytes is regulated by mitogen-activated protein kinase signaling. PLoS ONE, 5, 2010, e15425.
37. Martínez, I., Kim, J., Duffy, P.R., Schlegel, V.L., Walter, J., Resistant starches types 2 and 4 have differential effects on the composition of the fecal microbiota in human subjects. PLoS ONE, 5, 2010, e15046.
38. Maslowski, K.M., Vieira, A.T., Ng, A., Kranich, J., Sierro, F., Yu, D., Schilter, H.C., Rolph, M.S., Mackay, F., Artis, D., et al. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature 461 (2009), 1282–1286.
39. Millard, A.L., Mertes, P.M., Ittelet, D., Villard, F., Jeannesson, P., Bernard, J., Butyrate affects differentiation, maturation and function of human monocyte-derived dendritic cells and macrophages. Clin. Exp. Immunol. 130 (2002), 245–255.
40. Nahrendorf, M., Swirski, F.K., Aikawa, E., Stangenberg, L., Wurdinger, T., Figueiredo, J.L., Libby, P., Weissleder, R., Pittet, M.J., The healing myocardium sequentially mobilizes two monocyte subsets with divergent and complementary functions. J. Exp. Med. 204 (2007), 3037–3047.
41. Nsiah-Sefaa, A., McKenzie, M., Combined defects in oxidative phosphorylation and fatty acid β-oxidation in mitochondrial disease. Biosci. Rep., 36, 2016, 36.
42. O'Sullivan, D., Pearce, E.L., Targeting T cell metabolism for therapy. Trends Immunol. 36 (2015), 71–80.
43. Osthus, R.C., Shim, H., Kim, S., Li, Q., Reddy, R., Mukherjee, M., Xu, Y., Wonsey, D., Lee, L.A., Dang, C.V., Deregulation of glucose transporter 1 and glycolytic gene expression by c-Myc. J. Biol. Chem. 275 (2000), 21797–21800.
44. Palmer, C.S., Ostrowski, M., Balderson, B., Christian, N., Crowe, S.M., Glucose metabolism regulates T cell activation, differentiation, and functions. Front. Immunol., 6, 2015, 1.
45. Park, J., Kim, M., Kang, S.G., Jannasch, A.H., Cooper, B., Patterson, J., Kim, C.H., Short-chain fatty acids induce both effector and regulatory T cells by suppression of histone deacetylases and regulation of the mTOR-S6K pathway. Mucosal Immunol. 8 (2015), 80–93.
46. Perrone, L.A., Plowden, J.K., García-Sastre, A., Katz, J.M., Tumpey, T.M., H5N1 and 1918 pandemic influenza virus infection results in early and excessive infiltration of macrophages and neutrophils in the lungs of mice. PLoS Pathog., 4, 2008, e1000115.
47. Roy, M., Richard, J.F., Dumas, A., Vallières, L., CXCL1 can be regulated by IL-6 and promotes granulocyte adhesion to brain capillaries during bacterial toxin exposure and encephalomyelitis. J. Neuroinflammation, 9, 2012, 18.
48. Shirey, K.A., Pletneva, L.M., Puche, A.C., Keegan, A.D., Prince, G.A., Blanco, J.C., Vogel, S.N., Control of RSV-induced lung injury by alternatively activated macrophages is IL-4R alpha-, TLR4-, and IFN-beta-dependent. Mucosal Immunol. 3 (2010), 291–300.
49. Smith, P.M., Howitt, M.R., Panikov, N., Michaud, M., Gallini, C.A., Bohlooly-Y, M., Glickman, J.N., Garrett, W.S., The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 341 (2013), 569–573.
50. Trompette, A., Gollwitzer, E.S., Yadava, K., Sichelstiel, A.K., Sprenger, N., Ngom-Bru, C., Blanchard, C., Junt, T., Nicod, L.P., Harris, N.L., Marsland, B.J., Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis. Nat. Med. 20 (2014), 159–166.
51. van der Windt, G.J., Everts, B., Chang, C.H., Curtis, J.D., Freitas, T.C., Amiel, E., Pearce, E.J., Pearce, E.L., Mitochondrial respiratory capacity is a critical regulator of CD8+ T cell memory development. Immunity 36 (2012), 68–78.
52. Vinolo, M.A., Hatanaka, E., Lambertucci, R.H., Newsholme, P., Curi, R., Effects of short chain fatty acids on effector mechanisms of neutrophils. Cell Biochem. Funct. 27 (2009), 48–55.
53. Wang, N., Liang, H., Zen, K., Molecular mechanisms that influence the macrophage m1-m2 polarization balance. Front. Immunol., 5, 2014, 614.
54. Wieman, H.L., Wofford, J.A., Rathmell, J.C., Cytokine stimulation promotes glucose uptake via phosphatidylinositol-3 kinase/Akt regulation of Glut1 activity and trafficking. Mol. Biol. Cell 18 (2007), 1437–1446.
55. WorldHealthOrganization (2016). Influenza (Seasonal). http://www.who.int/mediacentre/factsheets/fs211/en/.