Modulation of Myelopoiesis Progenitors Is an Integral Component of Trained Immunity

Cell

Volumn 172, Issue 1-2, 2018, Pages 147-161.e12

  Mitroulis, Ioannis ^a   Ruppova, Klara ^a   Wang, Baomei ^b   Chen, Lan Sun ^a   Grzybek, Michal ^c,d   Grinenko, Tatyana ^a   Eugster, Anne ^e   Troullinaki, Maria ^a   Palladini, Alessandra ^a,c,d   Kourtzelis, Ioannis ^a   Chatzigeorgiou, Antonios ^a   Schlitzer, Andreas ^f   Beyer, Marc ^f,g   Joosten, Leo A B ^h   Isermann, Berend ⁱ   Lesche, Mathias ^a   Petzold, Andreas ^a   Simons, Kai ^j,k   Henry, Ian ^j   Dahl, Andreas ^a   Schultze, Joachim L ^f,g   Wielockx, Ben ^a   Zamboni, Nicola ^l   Mirtschink, Peter ^a   Coskun, Ünal ^c,d   Hajishengallis, George ^b   Netea, Mihai G ^f,h   Chavakis, Triantafyllos ^a   more..

^a DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^b UNIVERSITY OF PENNSYLVANIA SCHOOL OF DENTAL MEDICINE   (United States)

^c DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^d GERMAN CENTER FOR DIABETES RESEARCH DZD   (Germany)

^e CENTER FOR REGENERATIVE THERAPIES DRESDEN   (Germany)

^f UNIVERSITY OF BONN   (Germany)

^g GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^h RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

ⁱ OTTO VON GUERICKE UNIVERSITY   (Germany)

^j MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^k LIPOTYPE GMBH   (Germany)

^l ETH ZURICH   (Switzerland)

more..

Author keywords

cholesterol biosynthesis; glycolysis; GM CSF; inflammation; innate immune memory; interleukin 1 ; myelopoiesis; myelosuppression; trained innate immunity; glucan

Indexed keywords

GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 1BETA; BETA GLUCAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW; CELL COUNT; CELL EXPANSION; CELL LINEAGE; CELL METABOLISM; CELL SELECTION; CELL SUBPOPULATION; CHOLESTEROL METABOLISM; CONTROLLED STUDY; FLOW CYTOMETRY; GLUCOSE METABOLISM; HEMATOPOIETIC STEM CELL; INCUBATION TIME; INNATE IMMUNITY; LIPID METABOLISM; LIPIDOMICS; METABOLOMICS; MOUSE; MYELOPOIESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL; ANIMAL; C57BL MOUSE; CELL CULTURE; DRUG EFFECT; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; MALE; METABOLISM; MYELOID PROGENITOR CELL;

ANIMALS; BETA-GLUCANS; CELLS, CULTURED; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; IMMUNITY, INNATE; IMMUNOLOGIC MEMORY; INTERLEUKIN-1BETA; MALE; MICE; MICE, INBRED C57BL; MYELOID PROGENITOR CELLS; MYELOPOIESIS;

EID: 85041099114     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2017.11.034     Document Type: Article

References (66)

1. Arts, R.J.W., Carvalho, A., La Rocca, C., Palma, C., Rodrigues, F., Silvestre, R., Kleinnijenhuis, J., Lachmandas, E., Gonçalves, L.G., Belinha, A., et al. Immunometabolic pathways in BCG-induced trained immunity. Cell Rep. 17 (2016), 2562–2571.
2. 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., et al. Glutaminolysis and fumarate accumulation integrate immunometabolic and epigenetic programs in trained immunity. Cell Metab. 24 (2016), 807–819.
3. Boettcher, S., Manz, M.G., Regulation of inflammation- and infection-driven hematopoiesis. Trends Immunol. 38 (2017), 345–357.
4. Bonifacio, E., Ziegler, A.-G., Klingensmith, G., Schober, E., Bingley, P.J., Rottenkolber, M., Theil, A., Eugster, A., Puff, R., Peplow, C., et al., Pre-POINT Study Group. Effects of high-dose oral insulin on immune responses in children at high risk for type 1 diabetes: the Pre-POINT randomized clinical trial. JAMA 313 (2015), 1541–1549.
5. Chen, C., Liu, Y., Liu, Y., Zheng, P., Mammalian target of rapamycin activation underlies HSC defects in autoimmune disease and inflammation in mice. J. Clin. Invest. 120 (2010), 4091–4101.
6. 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. mTOR- and HIF-1α-mediated aerobic glycolysis as metabolic basis for trained immunity. Science, 345, 2014, 1250684.
7. Coskun, U., Simons, K., Cell membranes: the lipid perspective. Structure 19 (2011), 1543–1548.
8. Cutando, L., Busquets-Garcia, A., Puighermanal, E., Gomis-González, M., Delgado-García, J.M., Gruart, A., Maldonado, R., Ozaita, A., Microglial activation underlies cerebellar deficits produced by repeated cannabis exposure. J. Clin. Invest. 123 (2013), 2816–2831.
9. Ejsing, C.S., Sampaio, J.L., Surendranath, V., Duchoslav, E., Ekroos, K., Klemm, R.W., Simons, K., Shevchenko, A., Global analysis of the yeast lipidome by quantitative shotgun mass spectrometry. Proc. Natl. Acad. Sci. USA 106 (2009), 2136–2141.
10. Frelin, C., Herrington, R., Janmohamed, S., Barbara, M., Tran, G., Paige, C.J., Benveniste, P., Zuñiga-Pflücker, J.-C., Souabni, A., Busslinger, M., Iscove, N.N., GATA-3 regulates the self-renewal of long-term hematopoietic stem cells. Nat. Immunol. 14 (2013), 1037–1044.
11. Fuhrer, T., Heer, D., Begemann, B., Zamboni, N., High-throughput, accurate mass metabolome profiling of cellular extracts by flow injection-time-of-flight mass spectrometry. Anal. Chem. 83 (2011), 7074–7080.
12. Gekas, C., Graf, T., CD41 expression marks myeloid-biased adult hematopoietic stem cells and increases with age. Blood 121 (2013), 4463–4472.
13. Goodridge, H.S., Ahmed, S.S., Curtis, N., Kollmann, T.R., Levy, O., Netea, M.G., Pollard, A.J., van Crevel, R., Wilson, C.B., Harnessing the beneficial heterologous effects of vaccination. Nat. Rev. Immunol. 16 (2016), 392–400.
14. Herzog, R., Schwudke, D., Schuhmann, K., Sampaio, J.L., Bornstein, S.R., Schroeder, M., Shevchenko, A., A novel informatics concept for high-throughput shotgun lipidomics based on the molecular fragmentation query language. Genome Biol., 12, 2011, R8.
15. Herzog, R., Schuhmann, K., Schwudke, D., Sampaio, J.L., Bornstein, S.R., Schroeder, M., Shevchenko, A., LipidXplorer: a software for consensual cross-platform lipidomics. PLoS ONE, 7, 2012, e29851.
16. Hosoya, T., Kuroha, T., Moriguchi, T., Cummings, D., Maillard, I., Lim, K.-C., Engel, J.D., GATA-3 is required for early T lineage progenitor development. J. Exp. Med. 206 (2009), 2987–3000.
17. Ito, K., Carracedo, A., Weiss, D., Arai, F., Ala, U., Avigan, D.E., Schafer, Z.T., Evans, R.M., Suda, T., Lee, C.-H., Pandolfi, P.P., A PML–PPAR-δ pathway for fatty acid oxidation regulates hematopoietic stem cell maintenance. Nat. Med. 18 (2012), 1350–1358.
18. Jensen, K.J., Larsen, N., Biering-Sørensen, S., Andersen, A., Eriksen, H.B., Monteiro, I., Hougaard, D., Aaby, P., Netea, M.G., Flanagan, K.L., Benn, C.S., Heterologous immunological effects of early BCG vaccination in low-birth-weight infants in Guinea-Bissau: a randomized-controlled trial. J. Infect. Dis. 211 (2015), 956–967.
19. Kaul, S., Xu, H., Zabalawi, M., Maruko, E., Fulp, B.E., Bluemn, T., Brzoza-Lewis, K.L., Gerelus, M., Weerasekera, R., Kallinger, R., et al. Lipid-free apolipoprotein A-I reduces progression of atherosclerosis by mobilizing microdomain cholesterol and attenuating the number of CD131 expressing cells: monitoring cholesterol homeostasis using the cellular ester to total cholesterol ratio. J. Am. Heart Assoc., 5, 2016, e004401.
20. Liao, Y., Smyth, G.K., Shi, W., featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30 (2014), 923–930.
21. Liberzon, A., Birger, C., Thorvaldsdóttir, H., Ghandi, M., Mesirov, J.P., Tamayo, P., The Molecular Signatures Database (MSigDB) hallmark gene set collection. Cell Syst. 1 (2015), 417–425.
22. Liebisch, G., Binder, M., Schifferer, R., Langmann, T., Schulz, B., Schmitz, G., High throughput quantification of cholesterol and cholesteryl ester by electrospray ionization tandem mass spectrometry (ESI-MS/MS). Biochim. Biophys. Acta 1761 (2006), 121–128.
23. Love, M.I., Huber, W., Anders, S., Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol., 15, 2014, 550.
24. McDavid, A., Dennis, L., Danaher, P., Finak, G., Krouse, M., Wang, A., Webster, P., Beechem, J., Gottardo, R., Modeling bi-modality improves characterization of cell cycle on gene expression in single cells. PLoS Comput. Biol., 10, 2014, e1003696.
25. Mills, E.L., O'Neill, L.A., Reprogramming mitochondrial metabolism in macrophages as an anti-inflammatory signal. Eur. J. Immunol. 46 (2016), 13–21.
26. Mitroulis, I., Chen, L.-S., Singh, R.P., Kourtzelis, I., Economopoulou, M., Kajikawa, T., Troullinaki, M., Ziogas, A., Ruppova, K., Hosur, K., et al. Secreted protein Del-1 regulates myelopoiesis in the hematopoietic stem cell niche. J. Clin. Invest. 127 (2017), 3624–3639.
27. Mossadegh-Keller, N., Sarrazin, S., Kandalla, P.K., Espinosa, L., Stanley, E.R., Nutt, S.L., Moore, J., Sieweke, M.H., M-CSF instructs myeloid lineage fate in single haematopoietic stem cells. Nature 497 (2013), 239–243.
28. Murphy, A.J., Akhtari, M., Tolani, S., Pagler, T., Bijl, N., Kuo, C.-L., Wang, M., Sanson, M., Abramowicz, S., Welch, C., et al. ApoE regulates hematopoietic stem cell proliferation, monocytosis, and monocyte accumulation in atherosclerotic lesions in mice. J. Clin. Invest. 121 (2011), 4138–4149.
29. Musso, G., Mosimann, C., Panáková D., Burger, A., Zhou, Y., Zon, L.I., MacRae, C.A., Generating and evaluating a ranked candidate gene list for potential vertebrate heart field regulators. Genom. Data 6 (2015), 199–201.
30. Nagai, Y., Garrett, K.P., Ohta, S., Bahrun, U., Kouro, T., Akira, S., Takatsu, K., Kincade, P.W., Toll-like receptors on hematopoietic progenitor cells stimulate innate immune system replenishment. Immunity 24 (2006), 801–812.
31. Nakai, S., Hirai, Y., The therapeutic potential of interleukin-1 beta in the treatment of chemotherapy- or radiation-induced myelosuppression and in tumor therapy. Biotherapy 1 (1989), 339–354.
32. Netea, M.G., van Crevel, R., BCG-induced protection: effects on innate immune memory. Semin. Immunol. 26 (2014), 512–517.
33. 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., Trained immunity: A program of innate immune memory in health and disease. Science, 352, 2016, aaf1098.
34. Nimmo, R.A., May, G.E., Enver, T., Primed and ready: understanding lineage commitment through single cell analysis. Trends Cell Biol. 25 (2015), 459–467.
35. Norata, G.D., Caligiuri, G., Chavakis, T., Matarese, G., Netea, M.G., Nicoletti, A., O'Neill, L.A.J., Marelli-Berg, F.M., The cellular and molecular basis of translational immunometabolism. Immunity 43 (2015), 421–434.
36. Novershtern, N., Subramanian, A., Lawton, L.N., Mak, R.H., Haining, W.N., McConkey, M.E., Habib, N., Yosef, N., Chang, C.Y., Shay, T., et al. Densely interconnected transcriptional circuits control cell states in human hematopoiesis. Cell 144 (2011), 296–309.
37. Passegué E., Wagers, A.J., Giuriato, S., Anderson, W.C., Weissman, I.L., Global analysis of proliferation and cell cycle gene expression in the regulation of hematopoietic stem and progenitor cell fates. J. Exp. Med. 202 (2005), 1599–1611.
38. Paul, F., Arkin, Y., Giladi, A., Jaitin, D.A., Kenigsberg, E., Keren-Shaul, H., Winter, D., Lara-Astiaso, D., Gury, M., Weiner, A., et al. Transcriptional heterogeneity and lineage commitment in myeloid progenitors. Cell 163 (2015), 1663–1677.
39. Pietras, E.M., Reynaud, D., Kang, Y.-A., Carlin, D., Calero-Nieto, F.J., Leavitt, A.D., Stuart, J.M., Göttgens, B., Passegué E., Functionally distinct subsets of lineage-biased multipotent progenitors control blood production in normal and regenerative conditions. Cell Stem Cell 17 (2015), 35–46.
40. Pietras, E.M., Mirantes-Barbeito, C., Fong, S., Loeffler, D., Kovtonyuk, L.V., Zhang, S., Lakshminarasimhan, R., Chin, C.P., Techner, J.-M., Will, B., et al. Chronic interleukin-1 exposure drives haematopoietic stem cells towards precocious myeloid differentiation at the expense of self-renewal. Nat. Cell Biol. 18 (2016), 607–618.
41. Quintin, J., Saeed, S., Martens, J.H.A., Giamarellos-Bourboulis, E.J., Ifrim, D.C., Logie, C., Jacobs, L., Jansen, T., Kullberg, B.-J., Wijmenga, C., et al. Candida albicans infection affords protection against reinfection via functional reprogramming of monocytes. Cell Host Microbe 12 (2012), 223–232.
42. R Development Core Team. R: A Language and Environment for Statistical Computing. 2016, R Foundation for Statistical Computing.
43. Rosenbauer, F., Tenen, D.G., Transcription factors in myeloid development: balancing differentiation with transformation. Nat. Rev. Immunol. 7 (2007), 105–117.
44. Sampaio, J.L., Gerl, M.J., Klose, C., Ejsing, C.S., Beug, H., Simons, K., Shevchenko, A., Membrane lipidome of an epithelial cell line. Proc. Natl. Acad. Sci. USA 108 (2011), 1903–1907.
45. Sarrazin, S., Sieweke, M., Integration of cytokine and transcription factor signals in hematopoietic stem cell commitment. Semin. Immunol. 23 (2011), 326–334.
46. Sezgin, E., Levental, I., Mayor, S., Eggeling, C., The mystery of membrane organization: composition, regulation and roles of lipid rafts. Nat. Rev. Mol. Cell Biol. 18 (2017), 361–374.
47. Simsek, T., Kocabas, F., Zheng, J., Deberardinis, R.J., Mahmoud, A.I., Olson, E.N., Schneider, J.W., Zhang, C.C., Sadek, H.A., The distinct metabolic profile of hematopoietic stem cells reflects their location in a hypoxic niche. Cell Stem Cell 7 (2010), 380–390.
48. Suda, T., Takubo, K., Semenza, G.L., Metabolic regulation of hematopoietic stem cells in the hypoxic niche. Cell Stem Cell 9 (2011), 298–310.
49. Surma, M.A., Herzog, R., Vasilj, A., Klose, C., Christinat, N., Morin-Rivron, D., Simons, K., Masoodi, M., Sampaio, J.L., An automated shotgun lipidomics platform for high throughput, comprehensive, and quantitative analysis of blood plasma intact lipids. Eur. J. Lipid Sci. Technol. 117 (2015), 1540–1549.
50. Takizawa, H., Fritsch, K., Kovtonyuk, L.V., Saito, Y., Yakkala, C., Jacobs, K., Ahuja, A.K., Lopes, M., Hausmann, A., Hardt, W.-D., et al. Pathogen-induced TLR4-TRIF innate immune signaling in hematopoietic stem cells promotes proliferation but reduces competitive fitness. Cell Stem Cell 21 (2017), 225–240.e5.
51. Takubo, K., Nagamatsu, G., Kobayashi, C.I., Nakamura-Ishizu, A., Kobayashi, H., Ikeda, E., Goda, N., Rahimi, Y., Johnson, R.S., Soga, T., et al. Regulation of glycolysis by Pdk functions as a metabolic checkpoint for cell cycle quiescence in hematopoietic stem cells. Cell Stem Cell 12 (2013), 49–61.
52. Trumpp, A., Essers, M., Wilson, A., Awakening dormant haematopoietic stem cells. Nat. Rev. Immunol. 10 (2010), 201–209.
53. van der Meer, J.W., Barza, M., Wolff, S.M., Dinarello, C.A., A low dose of recombinant interleukin 1 protects granulocytopenic mice from lethal gram-negative infection. Proc. Natl. Acad. Sci. USA 85 (1988), 1620–1623.
54. Walter, D., Lier, A., Geiselhart, A., Thalheimer, F.B., Huntscha, S., Sobotta, M.C., Moehrle, B., Brocks, D., Bayindir, I., Kaschutnig, P., et al. Exit from dormancy provokes DNA-damage-induced attrition in haematopoietic stem cells. Nature 520 (2015), 549–552.
55. Wang, Y.-H., Israelsen, W.J., Lee, D., Yu, V.W.C., Jeanson, N.T., Clish, C.B., Cantley, L.C., Vander Heiden, M.G., Scadden, D.T., Cell-state-specific metabolic dependency in hematopoiesis and leukemogenesis. Cell 158 (2014), 1309–1323.
56. Wickham, H., Reshaping data with the reshape package. J. Stat. Softw. 21 (2007), 1–20.
57. Wickham, H., ggplot2: Elegant graphics for data analysis. 2009, Springer.
58. Wilson, A., Laurenti, E., Oser, G., van der Wath, R.C., Blanco-Bose, W., Jaworski, M., Offner, S., Dunant, C.F., Eshkind, L., Bockamp, E., et al. Hematopoietic stem cells reversibly switch from dormancy to self-renewal during homeostasis and repair. Cell 135 (2008), 1118–1129.
59. Winkler, I.G., Barbier, V., Nowlan, B., Jacobsen, R.N., Forristal, C.E., Patton, J.T., Magnani, J.L., Lévesque, J.-P., Vascular niche E-selectin regulates hematopoietic stem cell dormancy, self renewal and chemoresistance. Nat. Med. 18 (2012), 1651–1657.
60. Wu, T.D., Nacu, S., Fast and SNP-tolerant detection of complex variants and splicing in short reads. Bioinformatics 26 (2010), 873–881.
61. Yamada, T., Park, C.S., Lacorazza, H.D., Genetic control of quiescence in hematopoietic stem cells. Cell Cycle 12 (2013), 2376–2383.
62. Yáñez, A., Megías, J., O'Connor, J.-E., Gozalbo, D., Gil, M.L., Candida albicans induces selective development of macrophages and monocyte derived dendritic cells by a TLR2 dependent signalling. PLoS ONE, 6, 2011, e24761.
63. Yang, J., Tanaka, Y., Seay, M., Li, Z., Jin, J., Garmire, L.X., Zhu, X., Taylor, A., Li, W., Euskirchen, G., et al. Single cell transcriptomics reveals unanticipated features of early hematopoietic precursors. Nucleic Acids Res. 45 (2017), 1281–1296.
64. Yvan-Charvet, L., Pagler, T., Gautier, E.L., Avagyan, S., Siry, R.L., Han, S., Welch, C.L., Wang, N., Randolph, G.J., Snoeck, H.W., Tall, A.R., ATP-binding cassette transporters and HDL suppress hematopoietic stem cell proliferation. Science 328 (2010), 1689–1693.
65. Zhang, H., Rodriguez, S., Wang, L., Wang, S., Serezani, H., Kapur, R., Cardoso, A.A., Carlesso, N., Sepsis induces hematopoietic stem cell exhaustion and myelosuppression through distinct contributions of TRIF and MYD88. Stem Cell Reports 6 (2016), 940–956.
66. Zhao, J.L., Baltimore, D., Regulation of stress-induced hematopoiesis. Curr. Opin. Hematol. 22 (2015), 286–292.