Metabolism plays a key role during macrophage activation

Mediators of Inflammation

Volumn 2018, Issue , 2018, Pages

  Stunault, Marion I ^a   Bories, Gaël ^a   Guinamard, Rodolphe R ^a   Ivanov, Stoyan ^a  

^a CENTRE MÉDITERRANÉEN DE MÉDECINE MOLÉCULAIRE C3M   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; ARGININE; FATTY ACID; GLUCOSE; GLUTAMINE; ITACONIC ACID;

AMINO ACID METABOLISM; CELL METABOLISM; FATTY ACID METABOLISM; HUMAN; MACROPHAGE ACTIVATION; MACROPHAGE FUNCTION; METABOLIC REGULATION; MONOCYTE; MONONUCLEAR CELL; NONHUMAN; PHAGOCYTE; REVIEW; ANIMAL; MACROPHAGE; METABOLISM; PHAGOCYTOSIS; PHYSIOLOGY;

AMINO ACIDS; ANIMALS; FATTY ACIDS; GLUCOSE; HUMANS; MACROPHAGE ACTIVATION; MACROPHAGES; PHAGOCYTOSIS;

EID: 85060045167     PISSN: 09629351     EISSN: 14661861     Source Type: Journal    
DOI: 10.1155/2018/2426138     Document Type: Review

References (83)

1. C. Schulz, E. G. Perdiguero, L. Chorro et al., “A lineage of myeloid cells independent of Myb and hematopoietic stem cells,” Science, vol. 336, no. 6077, pp. 86-90, 2012.
2. E. Gomez Perdiguero, K. Klapproth, C. Schulz et al., “Tissue-resident macrophages originate from yolk-sac-derived erythro-myeloid progenitors,” Nature, vol. 518, no. 7540, pp. 547-551, 2015.
3. + erythro-myeloid progenitor-derived fetal monocytes give rise to adult tissue-resident macrophages,” Immunity, vol. 42, no. 4, pp. 665-678, 2015.
4. F. Ginhoux, M. Greter, M. Leboeuf et al., “Fate mapping analysis reveals that adult microglia derive from primitive macrophages,” Science, vol. 330, no. 6005, pp. 841-845, 2010.
5. S. Epelman, K. J. Lavine, A. E. Beaudin et al., “Embryonic and adult-derived resident cardiac macrophages are maintained through distinct mechanisms at steady state and during inflammation,” Immunity, vol. 40, no. 1, pp. 91-104, 2014.
6. S. Epelman, K. J. Lavine, and G. J. Randolph, “Origin and functions of tissue macrophages,” Immunity, vol. 41, no. 1, pp. 21-35, 2014.
7. C. Jakubzick, E. L. Gautier, S. L. Gibbings et al., “Minimal differentiation of classical monocytes as they survey steady-state tissues and transport antigen to lymph nodes,” Immunity, vol. 39, no. 3, pp. 599-610, 2013.
8. E. L. Gautier, T. Shay, J. Miller et al., “Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages,” Nature Immunology, vol. 13, no. 11, pp. 1118-1128, 2012.
9. E. L. Gautier, S. Ivanov, J. W. Williams et al., “Gata6 regulates aspartoacylase expression in resident peritoneal macrophages and controls their survival,” The Journal of Experimental Medicine, vol. 211, no. 8, pp. 1525-1531, 2014.
10. M. Rosas, L. C. Davies, P. J. Giles et al., “The transcription factor Gata6 links tissue macrophage phenotype and proliferative renewal,” Science, vol. 344, no. 6184, pp. 645-648, 2014.
11. Y. Okabe and R. Medzhitov, “Tissue-specific signals control reversible program of localization and functional polarization of macrophages,” Cell, vol. 157, no. 4, pp. 832-844, 2014.
12. A. Buttgereit, I. Lelios, X. Yu et al., “Sall1 is a transcriptional regulator defining microglia identity and function,” Nature Immunology, vol. 17, no. 12, pp. 1397-1406, 2016.
13. E. Mass, I. Ballesteros, M. Farlik et al., “Specification of tissue-resident macrophages during organogenesis,” Science, vol. 353, no. 6304, article aaf4238, 2016.
14. M. Kohyama, W. Ise, B. T. Edelson et al., “Role for Spi-C in the development of red pulp macrophages and splenic iron homeostasis,” Nature, vol. 457, no. 7227, pp. 318-321, 2008.
15. Y. Lavin, D. Winter, R. Blecher-Gonen et al., “Tissue-resident macrophage enhancer landscapes are shaped by the local microenvironment,” Cell, vol. 159, no. 6, pp. 1312-1326, 2014.
16. L. A. J. O'Neill and E. J. Pearce, “Immunometabolism governs dendritic cell and macrophage function,” The Journal of Experimental Medicine, vol. 213, no. 1, pp. 15-23, 2016.
17. C. V. Jakubzick, G. J. Randolph, and P. M. Henson, “Monocyte differentiation and antigen-presenting functions,” Nature Reviews. Immunology, vol. 17, no. 6, pp. 349-362, 2017.
18. C. L. Tsou, W. Peters, Y. Si et al., “Critical roles for CCR2 and MCP-3 in monocyte mobilization from bone marrow and recruitment to inflammatory sites,” The Journal of Clinical Investigation, vol. 117, no. 4, pp. 902-909, 2007.
19. N. V. Serbina and E. G. Pamer, “Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR2,” Nature Immunology, vol. 7, no. 3, pp. 311-317, 2006.
20. S. Z. Chong, M. Evrard, S. Devi et al., “CXCR4 identifies transitional bone marrow premonocytes that replenish the mature monocyte pool for peripheral responses,” The Journal of Experimental Medicine, vol. 213, no. 11, pp. 2293-2314, 2016.
21. − /− mice,” Circulation Research, vol. 118, no. 7, pp. 1062-1077, 2016.
22. + T cell metabolism,” Immunity, vol. 48, no. 5, pp. 992-1005.e8, 2018.
23. - monocytes,” Nature Immunology, vol. 12, no. 8, pp. 778-785, 2011.
24. low monocytes monitor endothelial cells and orchestrate their disposal,” Cell, vol. 153, no. 2, pp. 362-375, 2013.
25. R. N. Hanna, C. Cekic, D. Sag et al., “Patrolling monocytes control tumor metastasis to the lung,” Science, vol. 350, no. 6263, pp. 985-990, 2015.
26. F. Tacke, D. Alvarez, T. J. Kaplan et al., “Monocyte subsets differentially employ CCR2, CCR5, and CX3CR1 to accumulate within atherosclerotic plaques,” The Journal of Clinical Investigation, vol. 117, no. 1, pp. 185-194, 2007.
27. C. Varol, A. Mildner, and S. Jung, “Macrophages: development and tissue specialization,” Annual Review of Immunology, vol. 33, no. 1, pp. 643-675, 2015.
28. D. Gosselin, V. M. Link, C. E. Romanoski et al., “Environment drives selection and function of enhancers controlling tissue-specific macrophage identities,” Cell, vol. 159, no. 6, pp. 1327-1340, 2014.
29. M. N. Artyomov, A. Sergushichev, and J. D. Schilling, “Integrating immunometabolism and macrophage diversity,” Seminars in Immunology, vol. 28, no. 5, pp. 417-424, 2016.
30. + resident peritoneal and pleural macrophages rely on IRF4 for development from circulating monocytes,” The Journal of Experimental Medicine, vol. 213, no. 10, pp. 1951-1959, 2016.
31. A. J. Freemerman, A. R. Johnson, G. N. Sacks et al., “Metabolic reprogramming of macrophages: glucose transporter 1 (GLUT1)-mediated glucose metabolism drives a proinflam-matory phenotype,” The Journal of Biological Chemistry, vol. 289, no. 11, pp. 7884-7896, 2014.
32. M. Fukuzumi, H. Shinomiya, Y. Shimizu, K. Ohishi, and S. Utsumi, “Endotoxin-induced enhancement of glucose influx into murine peritoneal macrophages via GLUT1,” Infection and Immunity, vol. 64, no. 1, pp. 108-112, 1996.
33. T. Nishizawa, J. E. Kanter, F. Kramer et al., “Testing the role of myeloid cell glucose flux in inflammation and atherosclerosis,” Cell Reports, vol. 7, no. 2, pp. 356-365, 2014.
34. H. Emami, P. Singh, M. MacNabb et al., “Splenic metabolic activity predicts risk of future cardiovascular events: demonstration of a cardiosplenic axis in humans,” JACC: Cardiovascular Imaging, vol. 8, no. 2, pp. 121-130, 2015.
35. 18 F-FDG PET imaging of murine atherosclerosis: association with gene expression of key molecular markers,” PLoS One, vol. 7, no. 11, article e50908, 2012.
36. I. S. Rogers and A. Tawakol, “Imaging of coronary inflammation with FDG-PET: feasibility and clinical hurdles,” Current Cardiology Reports, vol. 13, no. 2, pp. 138-144, 2011.
37. S. Barghouthi, K. D. Everett, and D. P. Speert, “Nonopsonic phagocytosis of Pseudomonas aeruginosa requires facilitated transport of D-glucose by macrophages,” Journal of Immunology, vol. 154, no. 7, pp. 3420-3428, 1995.
38. T. M. Tucey, J. Verma, P. F. Harrison et al., “Glucose homeostasis is important for immune cell viability during Candida challenge and host survival of systemic fungal infection,” Cell Metabolism, vol. 27, no. 5, pp. 988-1006.e7, 2018.
39. L. Liu, Y. Lu, J. Martinez et al., “Proinflammatory signal suppresses proliferation and shifts macrophage metabolism from Myc-dependent to HIF1α-dependent,” Proceedings of the National Academy of Sciences of the United States of America, vol. 113, no. 6, pp. 1564-1569, 2016.
40. A. Wang, S. C. Huen, H. H. Luan et al., “Opposing effects of fasting metabolism on tissue tolerance in bacterial and viral inflammation,” Cell, vol. 166, no. 6, pp. 1512-1525.e12, 2016.
41. S. C.-C. Huang, B. Everts, Y. Ivanova et al., “Cell-intrinsic lysosomal lipolysis is essential for alternative activation of macrophages,” Nature Immunology, vol. 15, no. 9, pp. 846-855, 2014.
42. K. Kang, S. M. Reilly, V. Karabacak et al., “Adipocyte-derived Th2 cytokines and myeloid PPARδ regulate macrophage polarization and insulin sensitivity,” Cell Metabolism, vol. 7, no. 6, pp. 485-495, 2008.
43. J. I. Odegaard, R. R. Ricardo-Gonzalez, M. H. Goforth et al., “Macrophage-specific PPARγ controls alternative activation and improves insulin resistance,” Nature, vol. 447, no. 7148, pp. 1116-1120, 2007.
44. D. Vats, L. Mukundan, J. I. Odegaard et al., “Oxidative metabolism and PGC-1β attenuate macrophage-mediated inflammation,” Cell Metabolism, vol. 4, no. 1, pp. 13-24, 2006.
45. R. Zechner, P. C. Kienesberger, G. Haemmerle, R. Zimmermann, and A. Lass, “Adipose triglyceride lipase and the lipolytic catabolism of cellular fat stores,” Journal of Lipid Research, vol. 50, no. 1, pp. 3-21, 2008.
46. M. Viaud, S. Ivanov, N. Vujic et al., “Lysosomal cholesterol hydrolysis couples efferocytosis to anti-inflammatory oxy-sterol production,” Circulation Research, vol. 122, no. 10, pp. 1369-1384, 2018.
47. J. E. Kanter, F. Kramer, S. Barnhart et al., “Diabetes promotes an inflammatory macrophage phenotype and atherosclerosis through acyl-CoA synthetase 1,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 12, pp. E715-E724, 2012.
48. D. Park, C. Z. Han, M. R. Elliott et al., “Continued clearance of apoptotic cells critically depends on the phagocyte Ucp2 protein,” Nature, vol. 477, no. 7363, pp. 220-224, 2011.
49. G. J. Cannon and J. A. Swanson, “The macrophage capacity for phagocytosis,” Journal of Cell Science, vol. 101, Part 4, pp. 907-913, 1992.
50. D. Korns, S. C. Frasch, R. Fernandez-Boyanapalli, P. M. Henson, and D. L. Bratton, “Modulation of macrophage efferocytosis in inflammation,” Frontiers in Immunology, vol. 2, p. 57, 2011.
51. D. M. Schrijvers, G. R. Y. de Meyer, M. M. Kockx, A. G. Herman, and W. Martinet, “Phagocytosis of apoptotic cells by macrophages is impaired in atherosclerosis,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 25, no. 6, pp. 1256-1261, 2005.
52. M. K. Chang, C. Bergmark, A. Laurila et al., “Monoclonal antibodies against oxidized low-density lipoprotein bind to apoptotic cells and inhibit their phagocytosis by elicited macrophages: evidence that oxidation-specific epitopes mediate macrophage recognition,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 11, pp. 6353-6358, 1999.
53. E. Marsch, T. L. Theelen, J. A. F. Demandt et al., “Reversal of hypoxia in murine atherosclerosis prevents necrotic core expansion by enhancing efferocytosis,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 34, no. 12, pp. 2545-2553, 2014.
54. G. Chinetti-Gbaguidi, M. Baron, M. A. Bouhlel et al., “Human atherosclerotic plaque alternative macrophages display low cholesterol handling but high phagocytosis because of distinct activities of the PPARγ and LXRα pathways,” Circulation Research, vol. 108, no. 8, pp. 985-995, 2011.
55. A. K. Jha, S. C. C. Huang, A. Sergushichev et al., “Network integration of parallel metabolic and transcriptional data reveals metabolic modules that regulate macrophage polarization,” Immunity, vol. 42, no. 3, pp. 419-430, 2015.
56. V. Lampropoulou, A. Sergushichev, M. Bambouskova et al., “Itaconate links inhibition of succinate dehydrogenase with macrophage metabolic remodeling and regulation of inflammation,” Cell Metabolism, vol. 24, no. 1, pp. 158-166, 2016.
57. G. M. Tannahill, A. M. Curtis, J. Adamik et al., “Succinate is an inflammatory signal that induces IL-1β through HIF-1α,” Nature, vol. 496, no. 7444, pp. 238-242, 2013.
58. T. Cordes, M. Wallace, A. Michelucci et al., “Immunorespon-sive gene 1 and itaconate inhibit succinate dehydrogenase to modulate intracellular succinate levels,” The Journal of Biological Chemistry, vol. 291, no. 27, pp. 14274-14284, 2016.
59. E. L. Mills, D. G. Ryan, H. A. Prag et al., “Itaconate is an anti-inflammatory metabolite that activates Nrf2 via alkylation of KEAP1,” Nature, vol. 556, no. 7699, pp. 113-117, 2018.
60. M. Bambouskova, L. Gorvel, V. Lampropoulou et al., “Electrophilic properties of itaconate and derivatives regulate the IκBζ-ATF3 inflammatory axis,” Nature, vol. 556, no. 7702, pp. 501-504, 2018.
61. S. Nair, J. P. Huynh, V. Lampropoulou et al., “Irg1 expression in myeloid cells prevents immunopathology during M. tuberculosis infection,” The Journal of Experimental Medicine, vol. 215, no. 4, pp. 1035-1045, 2018.
62. J. M. Weiss, L. C. Davies, M. Karwan et al., “Itaconic acid mediates crosstalk between macrophage metabolism and peritoneal tumors,” The Journal of Clinical Investigation, vol. 128, no. 9, pp. 3794-3805, 2018.
63. A. E. Papathanassiu, J. H. Ko, M. Imprialou et al., “BCAT1 controls metabolic reprogramming in activated human macrophages and is associated with inflammatory diseases,” Nature Communications, vol. 8, p. 16040, 2017.
64. C. R. Green, M. Wallace, A. S. Divakaruni et al., “Branched-chain amino acid catabolism fuels adipocyte differentiation and lipogenesis,” Nature Chemical Biology, vol. 12, no. 1, pp. 15-21, 2016.
65. P. Newsholme, R. Curi, S. Gordon, and E. A. Newsholme, “Metabolism of glucose, glutamine, long-chain fatty acids and ketone bodies by murine macrophages,” The Biochemical Journal, vol. 239, no. 1, pp. 121-125, 1986.
66. P. Newsholme, S. Gordon, and E. A. Newsholme, “Rates of utilization and fates of glucose, glutamine, pyruvate, fatty acids and ketone bodies by mouse macrophages,” The Biochemical Journal, vol. 242, no. 3, pp. 631-636, 1987.
67. R. Curi, R. de Siqueira Mendes, L. A. de Campos Crispin, G. D. Norata, S. C. Sampaio, and P. Newsholme, “A past and present overview of macrophage metabolism and functional outcomes,” Clinical Science, vol. 131, no. 12, pp. 1329-1342, 2017.
68. P. S. Liu, H. Wang, X. Li et al., “α-Ketoglutarate orchestrates macrophage activation through metabolic and epigenetic reprogramming,” Nature Immunology, vol. 18, no. 9, pp. 985-994, 2017.
69. T. Satoh, O. Takeuchi, A. Vandenbon et al., “The Jmjd3-Irf4 axis regulates M2 macrophage polarization and host responses against helminth infection,” Nature Immunology, vol. 11, no. 10, pp. 936-944, 2010.
70. R. J. W. Arts, B. Novakovic, R. ter Horst et al., “Glutaminolysis and fumarate accumulation integrate immunometabolic and epigenetic programs in trained immunity,” Cell Metabolism, vol. 24, no. 6, pp. 807-819, 2016.
71. J. MacMicking, Q. W. Xie, and C. Nathan, “Nitric oxide and macrophage function,” Annual Review of Immunology, vol. 15, no. 1, pp. 323-350, 1997.
72. E. Clementi, G. C. Brown, M. Feelisch, and S. Moncada, “Persistent inhibition of cell respiration by nitric oxide: crucial role of S-nitrosylation of mitochondrial complex I and protective action of glutathione,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 13, pp. 7631-7636, 1998.
73. M. W. J. Cleeter, J. M. Cooper, V. M. Darley-Usmar, S. Moncada, and A. H. V. Schapira, “Reversible inhibition of cytochrome c oxidase, the terminal enzyme of the mitochondrial respiratory chain, by nitric oxide. Implications for neurodegen-erative diseases,” FEBS Letters, vol. 345, no. 1, pp. 50-54, 1994.
74. W. A. Baseler, L. C. Davies, L. Quigley et al., “Autocrine IL-10 functions as a rheostat for M1 macrophage glycolytic commitment by tuning nitric oxide production,” Redox Biology, vol. 10, pp. 12-23, 2016.
75. S. M. Morris Jr., “Regulation of enzymes of the urea cycle and arginine metabolism,” Annual Review of Nutrition, vol. 22, no. 1, pp. 87-105, 2002.
76. G. Wu and S. M. Morris Jr., “Arginine metabolism: nitric oxide and beyond,” The Biochemical Journal, vol. 336, no. 1, pp. 1-17, 1998.
77. J. T. Pesce, T. R. Ramalingam, M. M. Mentink-Kane et al., “Arginase-1-expressing macrophages suppress Th2 cytokine-driven inflammation and fibrosis,” PLoS Pathogens, vol. 5, no. 4, article e1000371, 2009.
78. J. Dominguez-Andres and M. G. Netea, “Long-term reprogramming of the innate immune system,” Journal of Leukocyte Biology, 2018.
79. L. B. Ivashkiv, “IFNγ: signalling, epigenetics and roles in immunity, metabolism, disease and cancer immunotherapy,” Nature Reviews. Immunology, vol. 18, no. 9, pp. 545-558, 2018.
80. G. J. Koelwyn, E. M. Corr, E. Erbay, and K. J. Moore, “Regulation of macrophage immunometabolism in atherosclerosis,” Nature Immunology, vol. 19, no. 6, pp. 526-537, 2018.
81. G. F. P. Bories and N. Leitinger, “Macrophage metabolism in atherosclerosis,” FEBS Letters, vol. 591, no. 19, pp. 3042-3060, 2017.
82. D. G. Ryan and L. A. J. O'Neill, “Krebs cycle rewired for macrophage and dendritic cell effector functions,” FEBS Letters, vol. 591, no. 19, pp. 2992-3006, 2017.
83. S. Galván-Peña and L. A. J. O'Neill, “Metabolic reprograming in macrophage polarization,” Frontiers in Immunology, vol. 5, p. 420, 2014.