Tissue Immunometabolism: Development, Physiology, and Pathobiology

Cell Metabolism

Volumn 25, Issue 1, 2017, Pages 11-26

  Man, Kevin ^a   Kutyavin, Vassily I ^a   Chawla, Ajay ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACCESSORY CELL; ANIMAL; BEIGE ADIPOSE TISSUE; BROWN ADIPOSE TISSUE; CELL COMMUNICATION; CELL METABOLISM; CYTOARCHITECTURE; DEVELOPMENT; HOMEOSTASIS; IMMUNITY; LIVER; METABOLIC DISORDER; NONHUMAN; PATHOLOGY; PHYSIOLOGY; PRIORITY JOURNAL; REVIEW; TISSUE METABOLISM; WHITE ADIPOSE TISSUE; ADIPOSE TISSUE; BIOLOGICAL MODEL; HUMAN; IMMUNOLOGY; METABOLISM; MORPHOGENESIS;

ADIPOSE TISSUE; ANIMALS; HUMANS; LIVER; METABOLIC DISEASES; MODELS, BIOLOGICAL; MORPHOGENESIS;

EID: 85000714857     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2016.08.016     Document Type: Review

References (166)

1. A-Gonzalez, N., Guillen, J.A., Gallardo, G., Diaz, M., de la Rosa, J.V., Hernandez, I.H., Casanova-Acebes, M., Lopez, F., Tabraue, C., Beceiro, S., et al. The nuclear receptor LXRα controls the functional specialization of splenic macrophages. Nat. Immunol. 14 (2013), 831–839.
2. Agarwal, P., Khan, S.R., Verma, S.C., Beg, M., Singh, K., Mitra, K., Gaikwad, A.N., Akhtar, M.S., Krishnan, M.Y., Mycobacterium tuberculosis persistence in various adipose depots of infected mice and the effect of anti-tubercular therapy. Microbes Infect. 16 (2014), 571–580.
3. Andrews, N.C., Forging a field: the golden age of iron biology. Blood 112 (2008), 219–230.
4. Ardawi, M.S., Newsholme, E.A., Glutamine metabolism in lymphocytes of the rat. Biochem. J. 212 (1983), 835–842.
5. Arrese, E.L., Soulages, J.L., Insect fat body: energy, metabolism, and regulation. Annu. Rev. Entomol. 55 (2010), 207–225.
6. Bapat, S.P., Myoung Suh, J., Fang, S., Liu, S., Zhang, Y., Cheng, A., Zhou, C., Liang, Y., LeBlanc, M., Liddle, C., et al. Depletion of fat-resident Treg cells prevents age-associated insulin resistance. Nature 528 (2015), 137–141.
7. Bass, J., Takahashi, J.S., Circadian integration of metabolism and energetics. Science 330 (2010), 1349–1354.
8. Benhamouche, S., Decaens, T., Godard, C., Chambrey, R., Rickman, D.S., Moinard, C., Vasseur-Cognet, M., Kuo, C.J., Kahn, A., Perret, C., Colnot, S., Apc tumor suppressor gene is the “zonation-keeper” of mouse liver. Dev. Cell 10 (2006), 759–770.
9. Berry, R., Rodeheffer, M.S., Characterization of the adipocyte cellular lineage in vivo. Nat. Cell Biol. 15 (2013), 302–308.
10. Berry, R., Jeffery, E., Rodeheffer, M.S., Weighing in on adipocyte precursors. Cell Metab. 19 (2014), 8–20.
11. Berry, D.C., Jiang, Y., Graff, J.M., Mouse strains to study cold-inducible beige progenitors and beige adipocyte formation and function. Nat. Commun., 7, 2016, 10184.
12. Brestoff, J.R., Kim, B.S., Saenz, S.A., Stine, R.R., Monticelli, L.A., Sonnenberg, G.F., Thome, J.J., Farber, D.L., Lutfy, K., Seale, P., Artis, D., Group 2 innate lymphoid cells promote beiging of white adipose tissue and limit obesity. Nature 519 (2015), 242–246.
13. Brown, M.S., Goldstein, J.L., A proteolytic pathway that controls the cholesterol content of membranes, cells, and blood. Proc. Natl. Acad. Sci. USA 96 (1999), 11041–11048.
14. Burch, H.B., Lowry, O.H., Kuhlman, A.M., Skerjance, J., Diamant, E.J., Lowry, S.R., Von Dippe, P., Changes in patterns of enzymes of carbohydrate metabolism in the developing rat liver. J. Biol. Chem. 238 (1963), 2267–2273.
15. Burzyn, D., Kuswanto, W., Kolodin, D., Shadrach, J.L., Cerletti, M., Jang, Y., Sefik, E., Tan, T.G., Wagers, A.J., Benoist, C., Mathis, D., A special population of regulatory T cells potentiates muscle repair. Cell 155 (2013), 1282–1295.
16. Cannon, B., Nedergaard, J., Brown adipose tissue: function and physiological significance. Physiol. Rev. 84 (2004), 277–359.
17. Cannon, B., Nedergaard, J., Nonshivering thermogenesis and its adequate measurement in metabolic studies. J. Exp. Biol. 214 (2011), 242–253.
18. Cayrol, C., Girard, J.P., IL-33: an alarmin cytokine with crucial roles in innate immunity, inflammation and allergy. Curr. Opin. Immunol. 31 (2014), 31–37.
19. Charroux, B., Royet, J., Elimination of plasmatocytes by targeted apoptosis reveals their role in multiple aspects of the Drosophila immune response. Proc. Natl. Acad. Sci. USA 106 (2009), 9797–9802.
20. Chawla, A., Repa, J.J., Evans, R.M., Mangelsdorf, D.J., Nuclear receptors and lipid physiology: opening the X-files. Science 294 (2001), 1866–1870.
21. Chung, S., Lee, T.J., Reader, B.F., Kim, J.Y., Lee, Y.G., Park, G.Y., Karpurapu, M., Ballinger, M.N., Qian, F., Rusu, L., et al. FoxO1 regulates allergic asthmatic inflammation through regulating polarization of the macrophage inflammatory phenotype. Oncotarget 7 (2016), 17532–17546.
22. Cipolletta, D., Feuerer, M., Li, A., Kamei, N., Lee, J., Shoelson, S.E., Benoist, C., Mathis, D., PPAR-γ is a major driver of the accumulation and phenotype of adipose tissue Treg cells. Nature 486 (2012), 549–553.
23. Cohen, P., Levy, J.D., Zhang, Y., Frontini, A., Kolodin, D.P., Svensson, K.J., Lo, J.C., Zeng, X., Ye, L., Khandekar, M.J., et al. Ablation of PRDM16 and beige adipose causes metabolic dysfunction and a subcutaneous to visceral fat switch. Cell 156 (2014), 304–316.
24. Combs, T.P., Nagajyothi, Mukherjee, S., de Almeida, C.J., Jelicks, L.A., Schubert, W., Lin, Y., Jayabalan, D.S., Zhao, D., Braunstein, V.L., et al. The adipocyte as an important target cell for Trypanosoma cruzi infection. J. Biol. Chem. 280 (2005), 24085–24094.
25. Cristancho, A.G., Lazar, M.A., Forming functional fat: a growing understanding of adipocyte differentiation. Nat. Rev. Mol. Cell Biol. 12 (2011), 722–734.
26. Damouche, A., Lazure, T., Avettand-Fènoël, V., Huot, N., Dejucq-Rainsford, N., Satie, A.P., Mélard, A., David, L., Gommet, C., Ghosn, J., et al. Adipose tissue is a neglected viral reservoir and an inflammatory site during chronic HIV and SIV infection. PLoS Pathog., 11, 2015, e1005153.
27. De Domenico, I., Ward, D.M., Kaplan, J., Hepcidin and ferroportin: the new players in iron metabolism. Semin. Liver Dis. 31 (2011), 272–279.
28. DeBerardinis, R.J., Thompson, C.B., Cellular metabolism and disease: what do metabolic outliers teach us?. Cell 148 (2012), 1132–1144.
29. DiAngelo, J.R., Bland, M.L., Bambina, S., Cherry, S., Birnbaum, M.J., The immune response attenuates growth and nutrient storage in Drosophila by reducing insulin signaling. Proc. Natl. Acad. Sci. USA 106 (2009), 20853–20858.
30. Evans, R.M., Barish, G.D., Wang, Y.-X., PPARs and the complex journey to obesity. Nat. Med. 10 (2004), 355–361.
31. Ferrandon, D., Imler, J.L., Hetru, C., Hoffmann, J.A., The Drosophila systemic immune response: sensing and signalling during bacterial and fungal infections. Nat. Rev. Immunol. 7 (2007), 862–874.
32. Ferreira, A.V., Segatto, M., Menezes, Z., Macedo, A.M., Gelape, C., de Oliveira Andrade, L., Nagajyothi, F., Scherer, P.E., Teixeira, M.M., Tanowitz, H.B., Evidence for Trypanosoma cruzi in adipose tissue in human chronic Chagas disease. Microbes Infect. 13 (2011), 1002–1005.
33. Forner, F., Kumar, C., Luber, C.A., Fromme, T., Klingenspor, M., Mann, M., Proteome differences between brown and white fat mitochondria reveal specialized metabolic functions. Cell Metab. 10 (2009), 324–335.
34. Fox, C.J., Hammerman, P.S., Thompson, C.B., Fuel feeds function: energy metabolism and the T-cell response. Nat. Rev. Immunol. 5 (2005), 844–852.
35. Franke-Fayard, B., Janse, C.J., Cunha-Rodrigues, M., Ramesar, J., Büscher, P., Que, I., Löwik, C., Voshol, P.J., den Boer, M.A., van Duinen, S.G., et al. Murine malaria parasite sequestration: CD36 is the major receptor, but cerebral pathology is unlinked to sequestration. Proc. Natl. Acad. Sci. USA 102 (2005), 11468–11473.
36. Frauwirth, K.A., Riley, J.L., Harris, M.H., Parry, R.V., Rathmell, J.C., Plas, D.R., Elstrom, R.L., June, C.H., Thompson, C.B., The CD28 signaling pathway regulates glucose metabolism. Immunity 16 (2002), 769–777.
37. Gallin, J.I., Kaye, D., O'Leary, W.M., Serum lipids in infection. N. Engl. J. Med. 281 (1969), 1081–1086.
38. Gardner, E.M., Beli, E., Clinthorne, J.F., Duriancik, D.M., Energy intake and response to infection with influenza. Annu. Rev. Nutr. 31 (2011), 353–367.
39. Gautier, E.L., Ivanov, S., Williams, J.W., Huang, S.C., Marcelin, G., Fairfax, K., Wang, P.L., Francis, J.S., Leone, P., Wilson, D.B., et al. Gata6 regulates aspartoacylase expression in resident peritoneal macrophages and controls their survival. J. Exp. Med. 211 (2014), 1525–1531.
40. Gebhardt, R., Metabolic zonation of the liver: regulation and implications for liver function. Pharmacol. Ther. 53 (1992), 275–354.
41. Gebhardt, R., Matz-Soja, M., Liver zonation: novel aspects of its regulation and its impact on homeostasis. World J. Gastroenterol. 20 (2014), 8491–8504.
42. Gebhardt, R., Baldysiak-Figiel, A., Krügel, V., Ueberham, E., Gaunitz, F., Hepatocellular expression of glutamine synthetase: an indicator of morphogen actions as master regulators of zonation in adult liver. Prog. Histochem. Cytochem. 41 (2007), 201–266.
43. 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.
44. Ghisletti, S., Barozzi, I., Mietton, F., Polletti, S., De Santa, F., Venturini, E., Gregory, L., Lonie, L., Chew, A., Wei, C.L., et al. Identification and characterization of enhancers controlling the inflammatory gene expression program in macrophages. Immunity 32 (2010), 317–328.
45. Ginhoux, F., Guilliams, M., Tissue-resident macrophage ontogeny and homeostasis. Immunity 44 (2016), 439–449.
46. Gordon, C.J., Temperature Regulation in Laboratory Rodents. 1993, Cambridge University Press.
47. Gosselin, D., Link, V.M., Romanoski, C.E., Fonseca, G.J., Eichenfield, D.Z., Spann, N.J., Stender, J.D., Chun, H.B., Garner, H., Geissmann, F., Glass, C.K., Environment drives selection and function of enhancers controlling tissue-specific macrophage identities. Cell 159 (2014), 1327–1340.
48. Haldar, M., Kohyama, M., So, A.Y., Kc, W., Wu, X., Briseño, C.G., Satpathy, A.T., Kretzer, N.M., Arase, H., Rajasekaran, N.S., et al. Heme-mediated SPI-C induction promotes monocyte differentiation into iron-recycling macrophages. Cell 156 (2014), 1223–1234.
49. Han, J., Lee, J.E., Jin, J., Lim, J.S., Oh, N., Kim, K., Chang, S.I., Shibuya, M., Kim, H., Koh, G.Y., The spatiotemporal development of adipose tissue. Development 138 (2011), 5027–5037.
50. Harms, M., Seale, P., Brown and beige fat: development, function and therapeutic potential. Nat. Med. 19 (2013), 1252–1263.
51. Harms, M.J., Ishibashi, J., Wang, W., Lim, H.W., Goyama, S., Sato, T., Kurokawa, M., Won, K.J., Seale, P., Prdm16 is required for the maintenance of brown adipocyte identity and function in adult mice. Cell Metab. 19 (2014), 593–604.
52. Harper, J., Mould, A., Andrews, R.M., Bikoff, E.K., Robertson, E.J., The transcriptional repressor Blimp1/Prdm1 regulates postnatal reprogramming of intestinal enterocytes. Proc. Natl. Acad. Sci. USA 108 (2011), 10585–10590.
53. Hausberger, F.X., Pathological changes in adipose tissue of obese mice. Anat. Rec. 154 (1966), 651–660.
54. Heinz, S., Benner, C., Spann, N., Bertolino, E., Lin, Y.C., Laslo, P., Cheng, J.X., Murre, C., Singh, H., Glass, C.K., Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 38 (2010), 576–589.
55. Heredia, J.E., Mukundan, L., Chen, F.M., Mueller, A.A., Deo, R.C., Locksley, R.M., Rando, T.A., Chawla, A., Type 2 innate signals stimulate fibro/adipogenic progenitors to facilitate muscle regeneration. Cell 153 (2013), 376–388.
56. Hijmans, B.S., Grefhorst, A., Oosterveer, M.H., Groen, A.K., Zonation of glucose and fatty acid metabolism in the liver: mechanism and metabolic consequences. Biochimie 96 (2014), 121–129.
57. Hong, K.Y., Bae, H., Park, I., Park, D.Y., Kim, K.H., Kubota, Y., Cho, E.S., Kim, H., Adams, R.H., Yoo, O.J., Koh, G.Y., Perilipin+ embryonic preadipocytes actively proliferate along growing vasculatures for adipose expansion. Development 142 (2015), 2623–2632.
58. Hotamisligil, G.S., Inflammation and metabolic disorders. Nature 444 (2006), 860–867.
59. Hotamisligil, G.S., Endoplasmic reticulum stress and the inflammatory basis of metabolic disease. Cell 140 (2010), 900–917.
60. Hotamisligil, G.S., Shargill, N.S., Spiegelman, B.M., Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science 259 (1993), 87–91.
61. Huang, J.T., Welch, J.S., Ricote, M., Binder, C.J., Willson, T.M., Kelly, C., Witztum, J.L., Funk, C.D., Conrad, D., Glass, C.K., Interleukin-4-dependent production of PPAR-gamma ligands in macrophages by 12/15-lipoxygenase. Nature 400 (1999), 378–382.
62. Hui, X., Gu, P., Zhang, J., Nie, T., Pan, Y., Wu, D., Feng, T., Zhong, C., Wang, Y., Lam, K.S., Xu, A., Adiponectin enhances cold-induced browning of subcutaneous adipose tissue via promoting M2 macrophage proliferation. Cell Metab. 22 (2015), 279–290.
63. Huttunen, R., Syrjänen, J., Obesity and the risk and outcome of infection. Int. J. Obes. 37 (2013), 333–340.
64. Jenne, C.N., Kubes, P., Immune surveillance by the liver. Nat. Immunol. 14 (2013), 996–1006.
65. Jiang, Y., Berry, D.C., Tang, W., Graff, J.M., Independent stem cell lineages regulate adipose organogenesis and adipose homeostasis. Cell Rep. 9 (2014), 1007–1022.
66. Joe, A.W., Yi, L., Even, Y., Vogl, A.W., Rossi, F.M., Depot-specific differences in adipogenic progenitor abundance and proliferative response to high-fat diet. Stem Cells 27 (2009), 2563–2570.
67. Joe, A.W., Yi, L., Natarajan, A., Le Grand, F., So, L., Wang, J., Rudnicki, M.A., Rossi, F.M., Muscle injury activates resident fibro/adipogenic progenitors that facilitate myogenesis. Nat. Cell Biol. 12 (2010), 153–163.
68. Jones, K.T., Ashrafi, K., Caenorhabditis elegans as an emerging model for studying the basic biology of obesity. Dis. Model. Mech. 2 (2009), 224–229.
69. Jungermann, K., Metabolic zonation of liver parenchyma. Semin. Liver Dis. 8 (1988), 329–341.
70. Kalaany, N.Y., Mangelsdorf, D.J., LXRS and FXR: the yin and yang of cholesterol and fat metabolism. Annu. Rev. Physiol. 68 (2006), 159–191.
71. Kang, K., Reilly, S.M., Karabacak, V., Gangl, M.R., Fitzgerald, K., Hatano, B., Lee, C.H., Adipocyte-derived Th2 cytokines and myeloid PPARdelta regulate macrophage polarization and insulin sensitivity. Cell Metab. 7 (2008), 485–495.
72. Karlsson, E.A., Beck, M.A., The burden of obesity on infectious disease. Exp. Biol. Med. (Maywood) 235 (2010), 1412–1424.
73. Katz, N., Teutsch, H.F., Jungermann, K., Sasse, D., Perinatal development of the metabolic zonation of hamster liver parenchyma. FEBS Lett. 69 (1976), 23–26.
74. Kierdorf, K., Prinz, M., Geissmann, F., Gomez Perdiguero, E., Development and function of tissue resident macrophages in mice. Semin. Immunol. 27 (2015), 369–378.
75. Kohyama, M., Ise, W., Edelson, B.T., Wilker, P.R., Hildner, K., Mejia, C., Frazier, W.A., Murphy, T.L., Murphy, K.M., Role for Spi-C in the development of red pulp macrophages and splenic iron homeostasis. Nature 457 (2009), 318–321.
76. Kolodin, D., van Panhuys, N., Li, C., Magnuson, A.M., Cipolletta, D., Miller, C.M., Wagers, A., Germain, R.N., Benoist, C., Mathis, D., Antigen- and cytokine-driven accumulation of regulatory T cells in visceral adipose tissue of lean mice. Cell Metab. 21 (2015), 543–557.
77. Kosteli, A., Sugaru, E., Haemmerle, G., Martin, J.F., Lei, J., Zechner, R., Ferrante, A.W. Jr., Weight loss and lipolysis promote a dynamic immune response in murine adipose tissue. J. Clin. Invest. 120 (2010), 3466–3479.
78. Kuswanto, W., Burzyn, D., Panduro, M., Wang, K.K., Jang, Y.C., Wagers, A.J., Benoist, C., Mathis, D., Poor repair of skeletal muscle in aging mice reflects a defect in local, interleukin-33-dependent accumulation of regulatory T cells. Immunity 44 (2016), 355–367.
79. Labialle, S., Marty, V., Bortolin-Cavaillé, M.L., Hoareau-Osman, M., Pradère, J.P., Valet, P., Martin, P.G., Cavaillé, J., The miR-379/miR-410 cluster at the imprinted Dlk1-Dio3 domain controls neonatal metabolic adaptation. EMBO J. 33 (2014), 2216–2230.
80. Lagerspetz, K., The postnatal development of homoiothermy and cold resistance in mice. Experientia 18 (1962), 282–284.
81. Lavin, Y., Winter, D., Blecher-Gonen, R., David, E., Keren-Shaul, H., Merad, M., Jung, S., Amit, I., Tissue-resident macrophage enhancer landscapes are shaped by the local microenvironment. Cell 159 (2014), 1312–1326.
82. Lavin, Y., Mortha, A., Rahman, A., Merad, M., Regulation of macrophage development and function in peripheral tissues. Nat. Rev. Immunol. 15 (2015), 731–744.
83. Lee, Y.H., Petkova, A.P., Mottillo, E.P., Granneman, J.G., In vivo identification of bipotential adipocyte progenitors recruited by β3-adrenoceptor activation and high-fat feeding. Cell Metab. 15 (2012), 480–491.
84. Lee, M.W., Odegaard, J.I., Mukundan, L., Qiu, Y., Molofsky, A.B., Nussbaum, J.C., Yun, K., Locksley, R.M., Chawla, A., Activated type 2 innate lymphoid cells regulate beige fat biogenesis. Cell 160 (2015), 74–87.
85. Lee, Y.H., Petkova, A.P., Konkar, A.A., Granneman, J.G., Cellular origins of cold-induced brown adipocytes in adult mice. FASEB J. 29 (2015), 286–299.
86. Lepper, C., Fan, C.M., Inducible lineage tracing of Pax7-descendant cells reveals embryonic origin of adult satellite cells. Genesis 48 (2010), 424–436.
87. Lin, H.V., Accili, D., Hormonal regulation of hepatic glucose production in health and disease. Cell Metab. 14 (2011), 9–19.
88. Long, J.Z., Svensson, K.J., Tsai, L., Zeng, X., Roh, H.C., Kong, X., Rao, R.R., Lou, J., Lokurkar, I., Baur, W., et al. A smooth muscle-like origin for beige adipocytes. Cell Metab. 19 (2014), 810–820.
89. Lowell, B.B., Spiegelman, B.M., Towards a molecular understanding of adaptive thermogenesis. Nature 404 (2000), 652–660.
90. Luan, B., Yoon, Y.S., Le Lay, J., Kaestner, K.H., Hedrick, S., Montminy, M., CREB pathway links PGE2 signaling with macrophage polarization. Proc. Natl. Acad. Sci. USA 112 (2015), 15642–15647.
91. Lumeng, C.N., Bodzin, J.L., Saltiel, A.R., Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J. Clin. Invest. 117 (2007), 175–184.
92. Mathis, D., Immunological goings-on in visceral adipose tissue. Cell Metab. 17 (2013), 851–859.
93. Medrikova, D., Sijmonsma, T.P., Sowodniok, K., Richards, D.M., Delacher, M., Sticht, C., Gretz, N., Schafmeier, T., Feuerer, M., Herzig, S., Brown adipose tissue harbors a distinct sub-population of regulatory T cells. PLoS ONE, 10, 2015, e0118534.
94. Melo, J.A., Ruvkun, G., Inactivation of conserved C. elegans genes engages pathogen- and xenobiotic-associated defenses. Cell 149 (2012), 452–466.
95. Molofsky, A.B., Nussbaum, J.C., Liang, H.E., Van Dyken, S.J., Cheng, L.E., Mohapatra, A., Chawla, A., Locksley, R.M., Innate lymphoid type 2 cells sustain visceral adipose tissue eosinophils and alternatively activated macrophages. J. Exp. Med. 210 (2013), 535–549.
96. Molofsky, A.B., Savage, A.K., Locksley, R.M., Interleukin-33 in tissue homeostasis, injury, and inflammation. Immunity 42 (2015), 1005–1019.
97. Mottillo, E.P., Shen, X.J., Granneman, J.G., Role of hormone-sensitive lipase in beta-adrenergic remodeling of white adipose tissue. Am. J. Physiol. Endocrinol. Metab. 293 (2007), E1188–E1197.
98. Muncan, V., Heijmans, J., Krasinski, S.D., Büller, N.V., Wildenberg, M.E., Meisner, S., Radonjic, M., Stapleton, K.A., Lamers, W.H., Biemond, I., et al. Blimp1 regulates the transition of neonatal to adult intestinal epithelium. Nat. Commun., 2, 2011, 452.
99. Naylor, C., Petri, W.A. Jr., Leptin regulation of immune responses. Trends Mol. Med. 22 (2016), 88–98.
100. Neyrolles, O., Hernández-Pando, R., Pietri-Rouxel, F., Fornès, P., Tailleux, L., Barrios Payán, J.A., Pivert, E., Bordat, Y., Aguilar, D., Prévost, M.C., et al. Is adipose tissue a place for Mycobacterium tuberculosis persistence?. PLoS ONE, 1, 2006, e43.
101. Nguyen, K.D., Qiu, Y., Cui, X., Goh, Y.P., Mwangi, J., David, T., Mukundan, L., Brombacher, F., Locksley, R.M., Chawla, A., Alternatively activated macrophages produce catecholamines to sustain adaptive thermogenesis. Nature 480 (2011), 104–108.
102. Nguyen, K.D., Fentress, S.J., Qiu, Y., Yun, K., Cox, J.S., Chawla, A., Circadian gene Bmal1 regulates diurnal oscillations of Ly6C(hi) inflammatory monocytes. Science 341 (2013), 1483–1488.
103. Nombela-Arrieta, C., Ritz, J., Silberstein, L.E., The elusive nature and function of mesenchymal stem cells. Nat. Rev. Mol. Cell Biol. 12 (2011), 126–131.
104. Nussbaum, J.C., Van Dyken, S.J., von Moltke, J., Cheng, L.E., Mohapatra, A., Molofsky, A.B., Thornton, E.E., Krummel, M.F., Chawla, A., Liang, H.E., Locksley, R.M., Type 2 innate lymphoid cells control eosinophil homeostasis. Nature 502 (2013), 245–248.
105. O'Neill, L.A., Pearce, E.J., Immunometabolism governs dendritic cell and macrophage function. J. Exp. Med. 213 (2016), 15–23.
106. Odegaard, J.I., Chawla, A., Pleiotropic actions of insulin resistance and inflammation in metabolic homeostasis. Science 339 (2013), 172–177.
107. Odegaard, J.I., Ricardo-Gonzalez, R.R., Goforth, M.H., Morel, C.R., Subramanian, V., Mukundan, L., Red Eagle, A., Vats, D., Brombacher, F., Ferrante, A.W., Chawla, A., Macrophage-specific PPARgamma controls alternative activation and improves insulin resistance. Nature 447 (2007), 1116–1120.
108. Odegaard, J.I., Ricardo-Gonzalez, R.R., Red Eagle, A., Vats, D., Morel, C.R., Goforth, M.H., Subramanian, V., Mukundan, L., Ferrante, A.W., Chawla, A., Alternative M2 activation of Kupffer cells by PPARdelta ameliorates obesity-induced insulin resistance. Cell Metab. 7 (2008), 496–507.
109. Odegaard, J.I., Lee, M.W., Sogawa, Y., Bertholet, A.M., Locksley, R.M., Weinberg, D.E., Kirichok, Y., Deo, R.C., Chawla, A., Perinatal licensing of thermogenesis by IL-33 and ST2. Cell 166 (2016), 841–854.
110. Okabe, Y., Medzhitov, R., Tissue-specific signals control reversible program of localization and functional polarization of macrophages. Cell 157 (2014), 832–844.
111. Okabe, Y., Medzhitov, R., Tissue biology perspective on macrophages. Nat. Immunol. 17 (2016), 9–17.
112. Okin, D., Medzhitov, R., The effect of sustained inflammation on hepatic mevalonate pathway results in hyperglycemia. Cell 165 (2016), 343–356.
113. Osborn, O., Olefsky, J.M., The cellular and signaling networks linking the immune system and metabolism in disease. Nat. Med. 18 (2012), 363–374.
114. Palanker, L., Tennessen, J.M., Lam, G., Thummel, C.S., Drosophila HNF4 regulates lipid mobilization and beta-oxidation. Cell Metab. 9 (2009), 228–239.
115. Pearce, E.L., Pearce, E.J., Metabolic pathways in immune cell activation and quiescence. Immunity 38 (2013), 633–643.
116. Peet, D.J., Turley, S.D., Ma, W., Janowski, B.A., Lobaccaro, J.M., Hammer, R.E., Mangelsdorf, D.J., Cholesterol and bile acid metabolism are impaired in mice lacking the nuclear oxysterol receptor LXR alpha. Cell 93 (1998), 693–704.
117. Pellegrino, M.W., Nargund, A.M., Kirienko, N.V., Gillis, R., Fiorese, C.J., Haynes, C.M., Mitochondrial UPR-regulated innate immunity provides resistance to pathogen infection. Nature 516 (2014), 414–417.
118. Qiu, Y., Nguyen, K.D., Odegaard, J.I., Cui, X., Tian, X., Locksley, R.M., Palmiter, R.D., Chawla, A., Eosinophils and type 2 cytokine signaling in macrophages orchestrate development of functional beige fat. Cell 157 (2014), 1292–1308.
119. Rajakumari, S., Wu, J., Ishibashi, J., Lim, H.W., Giang, A.H., Won, K.J., Reed, R.R., Seale, P., EBF2 determines and maintains brown adipocyte identity. Cell Metab. 17 (2013), 562–574.
120. Rao, R.R., Long, J.Z., White, J.P., Svensson, K.J., Lou, J., Lokurkar, I., Jedrychowski, M.P., Ruas, J.L., Wrann, C.D., Lo, J.C., et al. Meteorin-like is a hormone that regulates immune-adipose interactions to increase beige fat thermogenesis. Cell 157 (2014), 1279–1291.
121. Repa, J.J., Liang, G., Ou, J., Bashmakov, Y., Lobaccaro, J.M., Shimomura, I., Shan, B., Brown, M.S., Goldstein, J.L., Mangelsdorf, D.J., Regulation of mouse sterol regulatory element-binding protein-1c gene (SREBP-1c) by oxysterol receptors, LXRalpha and LXRbeta. Genes Dev. 14 (2000), 2819–2830.
122. Robinette, M.L., Fuchs, A., Cortez, V.S., Lee, J.S., Wang, Y., Durum, S.K., Gilfillan, S., Colonna, M., Immunological Genome Consortium. Transcriptional programs define molecular characteristics of innate lymphoid cell classes and subsets. Nat. Immunol. 16 (2015), 306–317.
123. Rombouts, K., Marra, F., Molecular mechanisms of hepatic fibrosis in non-alcoholic steatohepatitis. Dig. Dis. 28 (2010), 229–235.
124. Rosas, M., Davies, L.C., Giles, P.J., Liao, C.T., Kharfan, B., Stone, T.C., O'Donnell, V.B., Fraser, D.J., Jones, S.A., Taylor, P.R., The transcription factor Gata6 links tissue macrophage phenotype and proliferative renewal. Science 344 (2014), 645–648.
125. Rosen, E.D., Spiegelman, B.M., What we talk about when we talk about fat. Cell 156 (2014), 20–44.
126. Schneider, C., Nobs, S.P., Kurrer, M., Rehrauer, H., Thiele, C., Kopf, M., Induction of the nuclear receptor PPAR-γ by the cytokine GM-CSF is critical for the differentiation of fetal monocytes into alveolar macrophages. Nat. Immunol. 15 (2014), 1026–1037.
127. Schulz, T.J., Huang, T.L., Tran, T.T., Zhang, H., Townsend, K.L., Shadrach, J.L., Cerletti, M., McDougall, L.E., Giorgadze, N., Tchkonia, T., et al. Identification of inducible brown adipocyte progenitors residing in skeletal muscle and white fat. Proc. Natl. Acad. Sci. USA 108 (2011), 143–148.
128. Schwartz, D.R., Lazar, M.A., Human resistin: found in translation from mouse to man. Trends Endocrinol. Metab. 22 (2011), 259–265.
129. Seale, P., Bjork, B., Yang, W., Kajimura, S., Chin, S., Kuang, S., Scimè, A., Devarakonda, S., Conroe, H.M., Erdjument-Bromage, H., et al. PRDM16 controls a brown fat/skeletal muscle switch. Nature 454 (2008), 961–967.
130. Seale, P., Conroe, H.M., Estall, J., Kajimura, S., Frontini, A., Ishibashi, J., Cohen, P., Cinti, S., Spiegelman, B.M., Prdm16 determines the thermogenic program of subcutaneous white adipose tissue in mice. J. Clin. Invest. 121 (2011), 96–105.
131. Semple, R.K., Chatterjee, V.K., O'Rahilly, S., PPAR gamma and human metabolic disease. J. Clin. Invest. 116 (2006), 581–589.
132. Shabalina, I.G., Petrovic, N., de Jong, J.M., Kalinovich, A.V., Cannon, B., Nedergaard, J., UCP1 in brite/beige adipose tissue mitochondria is functionally thermogenic. Cell Rep. 5 (2013), 1196–1203.
133. Shaked, I., Hanna, R.N., Shaked, H., Chodaczek, G., Nowyhed, H.N., Tweet, G., Tacke, R., Basat, A.B., Mikulski, Z., Togher, S., et al. Transcription factor Nr4a1 couples sympathetic and inflammatory cues in CNS-recruited macrophages to limit neuroinflammation. Nat. Immunol. 16 (2015), 1228–1234.
134. Shivers, R.P., Youngman, M.J., Kim, D.H., Transcriptional responses to pathogens in Caenorhabditis elegans. Curr. Opin. Microbiol. 11 (2008), 251–256.
135. Si-Tayeb, K., Lemaigre, F.P., Duncan, S.A., Organogenesis and development of the liver. Dev. Cell 18 (2010), 175–189.
136. Sifri, C.D., Begun, J., Ausubel, F.M., The worm has turned—microbial virulence modeled in Caenorhabditis elegans. Trends Microbiol. 13 (2005), 119–127.
137. Stern, J.H., Rutkowski, J.M., Scherer, P.E., Adiponectin, leptin, and fatty acids in the maintenance of metabolic homeostasis through adipose tissue crosstalk. Cell Metab. 23 (2016), 770–784.
138. Suárez-Zamorano, N., Fabbiano, S., Chevalier, C., Stojanović, O., Colin, D.J., Stevanović, A., Veyrat-Durebex, C., Tarallo, V., Rigo, D., Germain, S., et al. Microbiota depletion promotes browning of white adipose tissue and reduces obesity. Nat. Med. 21 (2015), 1497–1501.
139. Swoap, S.J., Li, C., Wess, J., Parsons, A.D., Williams, T.D., Overton, J.M., Vagal tone dominates autonomic control of mouse heart rate at thermoneutrality. Am. J. Physiol. Heart Circ. Physiol. 294 (2008), H1581–H1588.
140. Tan, M.W., Shapira, M., Genetic and molecular analysis of nematode-microbe interactions. Cell. Microbiol. 13 (2011), 497–507.
141. Tang, W., Zeve, D., Suh, J.M., Bosnakovski, D., Kyba, M., Hammer, R.E., Tallquist, M.D., Graff, J.M., White fat progenitor cells reside in the adipose vasculature. Science 322 (2008), 583–586.
142. Tian, X.Y., Ganeshan, K., Hong, C., Nguyen, K.D., Qiu, Y., Kim, J., Tangirala, R.K., Tontonoz, P., Chawla, A., Thermoneutral housing accelerates metabolic inflammation to potentiate atherosclerosis but not insulin resistance. Cell Metab. 23 (2016), 165–178.
143. Timmons, J.A., Wennmalm, K., Larsson, O., Walden, T.B., Lassmann, T., Petrovic, N., Hamilton, D.L., Gimeno, R.E., Wahlestedt, C., Baar, K., et al. Myogenic gene expression signature establishes that brown and white adipocytes originate from distinct cell lineages. Proc. Natl. Acad. Sci. USA 104 (2007), 4401–4406.
144. Tontonoz, P., Hu, E., Spiegelman, B.M., Stimulation of adipogenesis in fibroblasts by PPAR gamma 2, a lipid-activated transcription factor. Cell 79 (1994), 1147–1156.
145. Trindade, S., Rijo-Ferreira, F., Carvalho, T., Pinto-Neves, D., Guegan, F., Aresta-Branco, F., Bento, F., Young, S.A., Pinto, A., Van Den Abbeele, J., et al. Trypanosoma brucei parasites occupy and functionally adapt to the adipose tissue in mice. Cell Host Microbe 19 (2016), 837–848.
146. Uezumi, A., Fukada, S., Yamamoto, N., Takeda, S., Tsuchida, K., Mesenchymal progenitors distinct from satellite cells contribute to ectopic fat cell formation in skeletal muscle. Nat. Cell Biol. 12 (2010), 143–152.
147. Umek, R.M., Friedman, A.D., McKnight, S.L., CCAAT-enhancer binding protein: a component of a differentiation switch. Science 251 (1991), 288–292.
148. Vasanthakumar, A., Moro, K., Xin, A., Liao, Y., Gloury, R., Kawamoto, S., Fagarasan, S., Mielke, L.A., Afshar-Sterle, S., Masters, S.L., et al. The transcriptional regulators IRF4, BATF and IL-33 orchestrate development and maintenance of adipose tissue-resident regulatory T cells. Nat. Immunol. 16 (2015), 276–285.
149. Vats, D., Mukundan, L., Odegaard, J.I., Zhang, L., Smith, K.L., Morel, C.R., Wagner, R.A., Greaves, D.R., Murray, P.J., Chawla, A., Oxidative metabolism and PGC-1beta attenuate macrophage-mediated inflammation. Cell Metab. 4 (2006), 13–24.
150. Vishvanath, L., MacPherson, K.A., Hepler, C., Wang, Q.A., Shao, M., Spurgin, S.B., Wang, M.Y., Kusminski, C.M., Morley, T.S., Gupta, R.K., Pdgfrβ+ mural preadipocytes contribute to adipocyte hyperplasia induced by high-fat-diet feeding and prolonged cold exposure in adult mice. Cell Metab. 23 (2016), 350–359.
151. Wan, Y.J., An, D., Cai, Y., Repa, J.J., Hung-Po Chen, T., Flores, M., Postic, C., Magnuson, M.A., Chen, J., Chien, K.R., et al. Hepatocyte-specific mutation establishes retinoid X receptor alpha as a heterodimeric integrator of multiple physiological processes in the liver. Mol. Cell. Biol. 20 (2000), 4436–4444.
152. Wang, F., Mullican, S.E., DiSpirito, J.R., Peed, L.C., Lazar, M.A., Lipoatrophy and severe metabolic disturbance in mice with fat-specific deletion of PPARγ. Proc. Natl. Acad. Sci. USA 110 (2013), 18656–18661.
153. Wang, Q.A., Tao, C., Gupta, R.K., Scherer, P.E., Tracking adipogenesis during white adipose tissue development, expansion, and regeneration. Nat. Med. 19 (2013), 1338–1344.
154. Way, J.M., Harrington, W.W., Brown, K.K., Gottschalk, W.K., Sundseth, S.S., Mansfield, T.A., Ramachandran, R.K., Willson, T.M., Kliewer, S.A., Comprehensive messenger ribonucleic acid profiling reveals that peroxisome proliferator-activated receptor gamma activation has coordinate effects on gene expression in multiple insulin-sensitive tissues. Endocrinology 142 (2001), 1269–1277.
155. Weisberg, S.P., McCann, D., Desai, M., Rosenbaum, M., Leibel, R.L., Ferrante, A.W. Jr., Obesity is associated with macrophage accumulation in adipose tissue. J. Clin. Invest. 112 (2003), 1796–1808.
156. Wernstedt Asterholm, I., Tao, C., Morley, T.S., Wang, Q.A., Delgado-Lopez, F., Wang, Z.V., Scherer, P.E., Adipocyte inflammation is essential for healthy adipose tissue expansion and remodeling. Cell Metab. 20 (2014), 103–118.
157. Williamson, R.T., On the treatment of glycosuria and diabetes mellitus with sodium salicylate. BMJ 1 (1901), 760–762.
158. Wilson-Fritch, L., Burkart, A., Bell, G., Mendelson, K., Leszyk, J., Nicoloro, S., Czech, M., Corvera, S., Mitochondrial biogenesis and remodeling during adipogenesis and in response to the insulin sensitizer rosiglitazone. Mol. Cell. Biol. 23 (2003), 1085–1094.
159. Wilson-Fritch, L., Nicoloro, S., Chouinard, M., Lazar, M.A., Chui, P.C., Leszyk, J., Straubhaar, J., Czech, M.P., Corvera, S., Mitochondrial remodeling in adipose tissue associated with obesity and treatment with rosiglitazone. J. Clin. Invest. 114 (2004), 1281–1289.
160. Wu, D., Molofsky, A.B., Liang, H.E., Ricardo-Gonzalez, R.R., Jouihan, H.A., Bando, J.K., Chawla, A., Locksley, R.M., Eosinophils sustain adipose alternatively activated macrophages associated with glucose homeostasis. Science 332 (2011), 243–247.
161. Wu, J., Boström, P., Sparks, L.M., Ye, L., Choi, J.H., Giang, A.H., Khandekar, M., Virtanen, K.A., Nuutila, P., Schaart, G., et al. Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human. Cell 150 (2012), 366–376.
162. Xu, H., Barnes, G.T., Yang, Q., Tan, G., Yang, D., Chou, C.J., Sole, J., Nichols, A., Ross, J.S., Tartaglia, L.A., Chen, H., Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J. Clin. Invest. 112 (2003), 1821–1830.
163. Xu, X., Grijalva, A., Skowronski, A., van Eijk, M., Serlie, M.J., Ferrante, A.W. Jr., Obesity activates a program of lysosomal-dependent lipid metabolism in adipose tissue macrophages independently of classic activation. Cell Metab. 18 (2013), 816–830.
164. Yamauchi, T., Kadowaki, T., Adiponectin receptor as a key player in healthy longevity and obesity-related diseases. Cell Metab. 17 (2013), 185–196.
165. Young, S.G., Zechner, R., Biochemistry and pathophysiology of intravascular and intracellular lipolysis. Genes Dev. 27 (2013), 459–484.
166. Zwezdaryk, K.J., Ferris, M.B., Strong, A.L., Morris, C.A., Bunnell, B.A., Dhurandhar, N.V., Gimble, J.M., Sullivan, D.E., Human cytomegalovirus infection of human adipose-derived stromal/stem cells restricts differentiation along the adipogenic lineage. Adipocyte 5 (2015), 53–64.