Peritoneal tissue-resident macrophages are metabolically poised to engage microbes using tissue-niche fuels

Nature Communications

Volumn 8, Issue 1, 2017, Pages

  Davies, Luke C ^a,b   Rice, Christopher M ^b   Palmieri, Erika M ^b   Taylor, Philip R ^a   Kuhns, Douglas B ^c   McVicar, Daniel W ^b  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b NATIONAL CANCER INSTITUTE   (United States)

^c FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARACHIDIC ACID; ASPARAGINE; ASPARTIC ACID; CYSTINE; GLUCOSE; GLUTAMIC ACID; GLUTAMINE; INTERLEUKIN 1BETA; LINOLEIC ACID; MESSENGER RNA; N ACETYLASPARTIC ACID; NITRIC OXIDE SYNTHASE; OLEIC ACID; PALMITIC ACID; PROTEIN KINASE C; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; SOTRASTAURIN; STEARIC ACID; TUMOR NECROSIS FACTOR; UBIQUINOL CYTOCHROME C REDUCTASE; ZYMOSAN; SUCCINATE DEHYDROGENASE (UBIQUINONE);

CELLS AND CELL COMPONENTS; ENZYME ACTIVITY; IMMUNE SYSTEM; METABOLISM; MICROORGANISM; MITOCHONDRION; OXYGEN; PHYSIOLOGICAL RESPONSE; PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; BONE MARROW DERIVED MACROPHAGE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; EFFECTOR CELL; ENZYME ACTIVITY; GENE EXPRESSION; HUMAN; HUMAN CELL; MASS FRAGMENTOGRAPHY; MICROORGANISM; MONOCYTE; MOUSE; NONHUMAN; OXYGEN CONSUMPTION; PERITONEUM MACROPHAGE; PHAGOCYTOSIS; PHAGOLYSOSOME; PHAGOSOME; RESPIRATORY BURST; ANIMAL; C57BL MOUSE; CYTOLOGY; FEMALE; IMMUNOLOGY; INFLAMMATION; MALE; METABOLISM; MICROBIOLOGY; MITOCHONDRION; PERITONEUM; PRIMARY CELL CULTURE; STEM CELL NICHE;

ANIMALS; ELECTRON TRANSPORT COMPLEX II; FEMALE; GLUTAMIC ACID; INFLAMMATION; MACROPHAGES, PERITONEAL; MALE; MICE; MICE, INBRED C57BL; MITOCHONDRIA; PERITONEUM; PHAGOCYTOSIS; PHAGOSOMES; PRIMARY CELL CULTURE; PROTEIN KINASE C; REACTIVE OXYGEN SPECIES; RESPIRATORY BURST; STEM CELL NICHE;

EID: 85037739168     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/s41467-017-02092-0     Document Type: Article

References (72)

1. Liddiard, K., Rosas, M., Davies, L. C., Jones, S. A. & Taylor, P. R. Macrophage heterogeneity and acute inflammation. Eur. J. Immunol. 41, 2503-2508 (2011).
2. Davies, L. C. & Taylor, P. R. Tissue-resident macrophages: then and now. Immunology 144, 541-548 (2015).
3. Davies, L. C. et al. A quantifiable proliferative burst of tissue macrophages restores homeostatic macrophage populations after acute inflammation. Eur. J. Immunol. 41, 2155-2164 (2011).
4. Hashimoto, D. et al. Tissue resident macrophages self-maintain locally throughout adult life with minimal contribution from circulating monocytes. Immunity 38, 792-804 (2013).
5. Yona, S. et al. Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis. Immunity 38, 79-91 (2012).
6. Bain, C. C. et al. Long-lived self-renewing bone marrow-derived macrophages displace embryo-derived cells to inhabit adult serous cavities. Nat. Commun. 7, ncomms11852 (2016).
7. Murray Peter, J. et al. Macrophage activation and polarization: Nomenclature and experimental guidelines. Immunity 41, 14-20 (2014).
8. Gosselin, D. et al. Environment drives selection and function of enhancers controlling tissue-specific macrophage identities. Cell 159, 1327-1340 (2014).
9. Lavin, Y. et al. Tissue-resident macrophage enhancer landscapes are shaped by the local microenvironment. Cell 159, 1312-1326 (2014).
10. Okabe, Y. & Medzhitov, R. Tissue-specific signals control reversible program of localization and functional polarization of macrophages. Cell 157, 832-844 (2014).
11. Rosas, M. et al. The transcription factor Gata6 links tissue macrophage phenotype and proliferative renewal. Science 344, 645-648 (2014).
12. Gautier, E. L. et al. Gata6 regulates aspartoacylase expression in resident peritoneal macrophages and controls their survival. J. Exp. Med. 211, 1525-1531 (2014).
13. Ganeshan, K. & Chawla, A. Metabolic regulation of immune responses. Annu. Rev. Immunol. 32, 609-634 (2014).
14. Pearce, E. L. & Pearce, E. J. Metabolic pathways in immune cell activation and quiescence. Immunity 38, 633-643 (2013).
15. Galvan-Pena, S. & O'Neill, L. A. Metabolic reprograming in macrophage polarization. Front. Immunol. 5, 420 (2014).
16. Jha, A. K. et al. Network integration of parallel metabolic and transcriptional data reveals metabolic modules that regulate macrophage polarization. Immunity 42, 419-430 (2015).
17. Namgaladze, D. & Brune, B. Fatty acid oxidation is dispensable for human macrophage IL-4-induced polarization. Biochim. Biophys. Acta 1841, 1329-1335 (2014).
18. Nomura, M. et al. Fatty acid oxidation in macrophage polarization. Nat. Immunol. 17, 216-217 (2016).
19. Wang, J. & Kubes, P. A reservoir of mature cavity macrophages that can rapidly invade visceral organs to affect tissue repair. Cell 165, 668-678 (2016).
20. Iles, K. E. & Forman, H. J. Macrophage signaling and respiratory burst. Immunol. Res. 26, 95-105 (2002).
21. Brown, G. D. et al. Dectin-1 is a major beta-glucan receptor on macrophages. J. Exp. Med. 196, 407-412 (2002).
22. Cathcart, M. K. Regulation of superoxide anion production by NADPH oxidase in monocytes/macrophages: contributions to atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 24, 23-28 (2004).
23. Westermann, B. Bioenergetic role of mitochondrial fusion and fission. Biochim. Biophys. Acta 1817, 1833-1838 (2012).
24. Newsholme, P., Gordon, S. & Newsholme, E. A. Rates of utilization and fates of glucose, glutamine, pyruvate, fatty acids and ketone bodies by mouse macrophages. Biochem. J. 242, 631-636 (1987).
25. Azevedo, E. P. et al. A metabolic shift toward pentose phosphate pathway is necessary for amyloid fibril-and phorbol 12-myristate 13-acetate-induced neutrophil extracellular trap (NET) formation. J. Biol. Chem. 290, 22174-22183 (2015).
26. Horgan, K., Cooke, E., Hallett, M. B. & Mansel, R. E. Inhibition of protein kinase C mediated signal transduction by tamoxifen. Importance for antitumour activity. Biochem. Pharmacol. 35, 4463-4465 (1986).
27. Clark, R. A. Activation of the neutrophil respiratory burst oxidase. J. Infect. Dis. 179, S309-S317 (1999).
28. Holmes, B., Page, A. R. & Good, R. A. Studies of the metabolic activity of leukocytes from patients with a genetic abnormality of phagocytic function. J. Clin. Invest. 46, 1422-1432 (1967).
29. Maianski, N. A. et al. Functional characterization of mitochondria in neutrophils: a role restricted to apoptosis. Cell Death Differ. 11, 143-153 (2004).
30. Daiber, A. Redox signaling (cross-talk) from and to mitochondria involves mitochondrial pores and reactive oxygen species. Biochim. Biophys. Acta 1797, 897-906 (2010).
31. Bleier, L. & Drose, S. Superoxide generation by complex III: from mechanistic rationales to functional consequences. Biochim. Biophys. Acta 1827, 1320-1331 (2013).
32. Muller, F. L., Liu, Y. & Van Remmen, H. Complex III releases superoxide to both sides of the inner mitochondrial membrane. J. Biol. Chem. 279, 49064-49073 (2004).
33. Tannahill, G. M. et al. Succinate is an inflammatory signal that induces IL-1beta through HIF-1alpha. Nature 496, 238-242 (2013).
34. Garaude, J. et al. Mitochondrial respiratory-chain adaptations in macrophages contribute to antibacterial host defense. Nat. Immunol. 17, 1037-1045 (2016).
35. Baseler, W. A. et al. Autocrine IL-10 functions as a rheostat for M1 macrophage glycolytic commitment by tuning nitric oxide production. Redox Biol. 10, 12-23 (2016).
36. Taylor, P. R. et al. Dectin-1 is required for beta-glucan recognition and control of fungal infection. Nat. Immunol. 8, 31-38 (2007).
37. Strasser, D. et al. Syk kinase-coupled C-type lectin receptors engage protein kinase C-sigma to elicit Card9 adaptor-mediated innate immunity. Immunity 36, 32-42 (2012).
38. Mindell, J. A. Lysosomal acidification mechanisms. Annu. Rev. Physiol. 74, 69-86 (2012).
39. Geng, J. et al. Kinases Mst1 and Mst2 positively regulate phagocytic induction of reactive oxygen species and bactericidal activity. Nat. Immunol. 16, 1142-1152 (2015).
40. Fernandez-Boyanapalli, R. F. et al. Pioglitazone restores phagocyte mitochondrial oxidants and bactericidal capacity in chronic granulomatous disease. J. Allergy Clin. Immunol. 135, 517-527 e512 (2015).
41. Furukawa, S. et al. Supplemental glutamine augments phagocytosis and reactive oxygen intermediate production by neutrophils and monocytes from postoperative patients in vitro. Nutrition 16, 323-329 (2000).
42. Yassad, A., Lavoinne, A., Bion, A., Daveau, M. & Husson, A. Glutamine accelerates interleukin-6 production by rat peritoneal macrophages in culture. FEBS Lett. 413, 81-84 (1997).
43. Wallace, C. & Keast, D. Glutamine and macrophage function. Metabolism 41, 1016-1020 (1992).
44. Newsholme, P., Curi, R., Gordon, S. & Newsholme, E. A. Metabolism of glucose, glutamine, long-chain fatty acids and ketone bodies by murine macrophages. Biochem. J. 239, 121-125 (1986).
45. Mitra, K. Mitochondrial fission-fusion as an emerging key regulator of cell proliferation and differentiation. Bioessays 35, 955-964 (2013).
46. Mazzoli, R. & Pessione, E. The neuro-endocrinological role of microbial glutamate and GABA signaling. Front. Microbiol. 7, 1934 (2016).
47. Dillon, S. et al. Yeast zymosan, a stimulus for TLR2 and dectin-1, induces regulatory antigen-presenting cells and immunological tolerance. J. Clin. Invest. 116, 916-928 (2006).
48. Thaiss, C. A., Zmora, N., Levy, M. & Elinav, E. The microbiome and innate immunity. Nature 535, 65-74 (2016).
49. Dikalov, S. Cross talk between mitochondria and NADPH oxidases. Free Radic. Biol. Med. 51, 1289-1301 (2011).
50. Green, S. P., Hamilton, J. A., Uhlinger, D. J. & Phillips, W. A. Expression of p47-phox and p67-phox proteins in murine bone marrow-derived macrophages: enhancement by lipopolysaccharide and tumor necrosis factor alpha but not colony stimulating factor 1. J. Leukoc. Biol. 55, 530-535 (1994).
51. Dusi, S. et al. Mechanisms of expression of NADPH oxidase components in human cultured monocytes: role of cytokines and transcriptional regulators involved. Eur. J. Immunol. 31, 929-938 (2001).
52. Wallace, D. C. Mitochondria and cancer. Nat. Rev. Cancer 12, 685-698 (2012).
53. Palmieri, E. M. et al. Acetylation of human mitochondrial citrate carrier modulates mitochondrial citrate/malate exchange activity to sustain NADPH production during macrophage activation. Biochim. Biophys. Acta 1847, 729-738 (2015).
54. Mills, E. L. et al. Succinate dehydrogenase supports metabolic repurposing of mitochondria to drive inflammatory macrophages. Cell 167, 457-470 e413 (2016).
55. Palmieri, F. The mitochondrial transporter family SLC25: identification, properties and physiopathology. Mol. Asp. Med. 34, 465-484 (2013).
56. Pardee, A. B. & Potter, V. R. Malonate inhibition of oxidations in the Krebs tricarboxylic acid cycle. J. Biol. Chem. 178, 241-250 (1949).
57. Naik, E. & Dixit, V. M. Mitochondrial reactive oxygen species drive proinflammatory cytokine production. J. Exp. Med. 208, 417-420 (2011).
58. Clementi, E., Brown, G. C., Feelisch, M. & Moncada, S. Persistent inhibition of cell respiration by nitric oxide: crucial role of S-nitrosylation of mitochondrial complex I and protective action of glutathione. Proc. Natl Acad. Sci. USA 95, 7631-7636 (1998).
59. Chang, C. I., Liao, J. C. & Kuo, L. Arginase modulates nitric oxide production in activated macrophages. Am. J. Physiol. 274, H342-H348 (1998).
60. Soubannier, V. et al. A vesicular transport pathway shuttles cargo from mitochondria to lysosomes. Curr. Biol. 22, 135-141 (2012).
61. Segal, A. W. How neutrophils kill microbes. Annu. Rev. Immunol. 23, 197-223 (2005).
62. Jackson, S. H., Gallin, J. I. & Holland, S. M. The p47phox mouse knock-out model of chronic granulomatous disease. J. Exp. Med. 182, 751-758 (1995).
63. Laubach, V. E., Shesely, E. G., Smithies, O. & Sherman, P. A. Mice lacking inducible nitric oxide synthase are not resistant to lipopolysaccharide-induced death. Proc. Natl Acad. Sci. USA 92, 10688-10692 (1995).
64. Adachi, O. et al. Targeted disruption of the MyD88 gene results in loss of IL-1-and IL-18-mediated function. Immunity 9, 143-150 (1998).
65. Akazawa, T. et al. Antitumor NK activation induced by the Toll-like receptor 3-TICAM-1 (TRIF) pathway in myeloid dendritic cells. Proc. Natl Acad. Sci. USA 104, 252-257 (2007).
66. Turnbull, I. R. et al. Cutting edge: TREM-2 attenuates macrophage activation. J. Immunol. 177, 3520-3524 (2006).
67. Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15-21 (2013).
68. Robinson, M. D. & Oshlack, A. A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol. 11, R25 (2010).
69. Law, C. W., Chen, Y., Shi, W. & Smyth, G. K. voom: Precision weights unlock linear model analysis tools for RNA-seq read counts. Genome Biol. 15, R29 (2014).
70. Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676-682 (2012).
71. Bolte, S. & Cordelieres, F. P. A guided tour into subcellular colocalization analysis in light microscopy. J. Microsc. 224, 213-232 (2006).
72. Edgar, R., Domrachev, M. & Lash, A. E. Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 30, 207-210 (2002).