Tissue-Specific Role of Macrophages in Noninfectious Inflammatory Disorders
Abstract
:1. Introduction
2. Role of Macrophages in the Pathogenesis of Obesity
3. Molecular Basis of Adipose Tissue Inflammation in Individuals with Obesity
4. Specialization of Macrophages in Adipose Tissue: MMe and Mox Macrophages
5. Role of Macrophages in the Development of Endothelial Dysfunction
5.1. Macrophage Subpopulation M(Hb)
5.2. Macrophage Subpopulation Mhem
5.3. Macrophage Subpopulation M4
6. Role of Macrophages in the Neuroimmunological Intracellular Interactions of Adipose Tissue
7. The Role of Macrophages in Liver Pathologies Associated with Inflammation
8. Pathophysiological Role of Macrophages in the Development of Aseptic Inflammatory Foci in the Skin of Individuals with Metabolic Pathologies
9. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
- Obesity. Available online: https://www.who.int/westernpacific/health-topics/obesity (accessed on 25 September 2020).
- Litvinova, L.S.; Kiriyenkova, Y.V.; Aksyonova, N.N.; Gazatova, N.D.; Zatolokin, P.A. Features of cellular immunity and cytokine repertoire in patients with metabolic syndrome. Bull. Sib. Med. 2012, 11, 53–57. [Google Scholar] [CrossRef]
- Litvinova, L.S.; Vasilenko, M.A.; Zatolokin, P.A.; Aksenova, N.N.; Fattakhov, N.S. Adipokines in metabolic processes regulating during obesity treatment. Diabetes Mellit. 2014, 17, 51–59. [Google Scholar] [CrossRef] [Green Version]
- Vasilenko, M.A.; Kirienkova, E.V.; Skuratovskaia, D.A.; Zatolokin, P.A.; Mironyuk, N.I.; Litvinova, L.S. The role of adipsin and leptin production in the formation of insulin resistance in abdominal obesity patients. Acad. Sci. Rep. 2017, 475. [Google Scholar] [CrossRef]
- Skuratovskaia, D.; Litvinova, L.; Vulf, M.; Zatolokin, P.; Popadin, K.; Mazunin, I. From Normal to Obesity and Back: The Associations between Mitochondrial DNA Copy Number, Gender, and Body Mass Index. Cells 2019, 8, 430. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Litvinova, L.; Zatolokin, P.; Vulf, M.; Mazunin, I.; Skuratovskaia, D. The relationship between the mtDNA copy number in insulin-dependent tissues and markers of endothelial dysfunction and inflammation in obese patients. BMC Med. Genom. 2019, 12, 41. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Skuratovskaia, D.; Zatolokin, P.; Vulf, M.; Mazunin, I.; Litvinova, L. Interrelation of chemerin and TNF-α with mtDNA copy number in adipose tissues and blood cells in obese patients with and without type 2 diabetes. BMC Med. Genom. 2019, 12, 40. [Google Scholar] [CrossRef] [Green Version]
- Litvinova, L.; Atochin, D.; Vasilenko, M.; Fattakhov, N.; Zatolokin, P.; Vaysbeyn, I.; Kirienkova, E. Role of adiponectin and proinflammatory gene expression in adipose tissue chronic inflammation in women with metabolic syndrome. Diabetol. Metab. Syndr. 2014, 6, 137. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wynn, T.A.; Vannella, K.M. Macrophages in Tissue Repair, Regeneration, and Fibrosis. Immunity 2016, 44, 450–462. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Murray, P.J.; Wynn, T.A. Protective and pathogenic functions of macrophage subsets. Nat. Rev. Immunol. 2011, 11, 723–737. [Google Scholar] [CrossRef] [PubMed]
- Muraille, E.; Leo, O.; Moser, M. TH1/TH2 paradigm extended: Macrophage polarization as an unappreciated pathogen-driven escape mechanism? Front. Immunol. 2014, 5, 603. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rivera, A.; Siracusa, M.C.; Yap, G.S.; Gause, W.C. Innate cell communication kick-starts pathogen-specific immunity. Nat. Immunol. 2016, 17, 356–363. [Google Scholar] [CrossRef] [PubMed]
- Ziegler-Heitbrock, L.; Ancuta, P.; Crowe, S.; Dalod, M.; Grau, V.; Hart, D.N.; Leenen, P.J.M.; Liu, Y.-J.; MacPherson, G.; Randolph, G.J.; et al. Nomenclature of monocytes and dendritic cells in blood. Blood 2010, 116, e74–e80. [Google Scholar] [CrossRef] [PubMed]
- Cros, J.; Cagnard, N.; Woollard, K.; Patey, N.; Zhang, S.-Y.; Senechal, B.; Puel, A.; Biswas, S.K.; Moshous, D.; Picard, C.; et al. Human CD14dim monocytes patrol and sense nucleic acids and viruses via TLR7 and TLR8 receptors. Immunity 2010, 33, 375–386. [Google Scholar] [CrossRef] [Green Version]
- Ziegler-Heitbrock, L. Blood Monocytes and Their Subsets: Established Features and Open Questions. Front. Immunol. 2015, 6, 423. [Google Scholar] [CrossRef]
- Jakubzick, C.V.; Randolph, G.J.; Henson, P.M. Monocyte differentiation and antigen-presenting functions. Nat. Rev. Immunol. 2017, 17, 349–362. [Google Scholar] [CrossRef] [PubMed]
- Weber, C.; Shantsila, E.; Hristov, M.; Caligiuri, G.; Guzik, T.; Heine, G.H.; Hoefer, I.E.; Monaco, C.; Peter, K.; Rainger, E.; et al. Role and analysis of monocyte subsets in cardiovascular disease. Joint consensus document of the European Society of Cardiology (ESC) Working Groups “Atherosclerosis & Vascular Biology” and “Thrombosis”. Thromb. Haemost. 2016, 116, 626–637. [Google Scholar] [CrossRef] [Green Version]
- Kapellos, T.S.; Bonaguro, L.; Gemünd, I.; Reusch, N.; Saglam, A.; Hinkley, E.R.; Schultze, J.L. Human Monocyte Subsets and Phenotypes in Major Chronic Inflammatory Diseases. Front. Immunol. 2019, 10, 2035. [Google Scholar] [CrossRef] [Green Version]
- Bain, C.C.; Schridde, A. Origin, Differentiation, and Function of Intestinal Macrophages. Front. Immunol. 2018, 9. [Google Scholar] [CrossRef] [PubMed]
- Ostuni, R.; Kratochvill, F.; Murray, P.J.; Natoli, G. Macrophages and cancer: From mechanisms to therapeutic implications. Trends Immunol. 2015, 36, 229–239. [Google Scholar] [CrossRef]
- Gordon, S.; Plüddemann, A. Tissue macrophages: Heterogeneity and functions. BMC Biol. 2017, 15, 53. [Google Scholar] [CrossRef]
- Gentek, R.; Molawi, K.; Sieweke, M.H. Tissue macrophage identity and self-renewal. Immunol. Rev. 2014, 262, 56–73. [Google Scholar] [CrossRef] [PubMed]
- Kolter, J.; Kierdorf, K.; Henneke, P. Origin and Differentiation of Nerve-Associated Macrophages. J. Immunol. 2020, 204, 271–279. [Google Scholar] [CrossRef] [PubMed]
- Perdiguero, E.G.; Geissmann, F. The development and maintenance of resident macrophages. Nat. Immunol. 2016, 17, 2–8. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Snodgrass, R.G.; Boß, M.; Zezina, E.; Weigert, A.; Dehne, N.; Fleming, I.; Brüne, B.; Namgaladze, D. Hypoxia Potentiates Palmitate-induced Pro-inflammatory Activation of Primary Human Macrophages. J. Biol. Chem. 2016, 291, 413–424. [Google Scholar] [CrossRef] [Green Version]
- Bergmann, K.; Sypniewska, G. Diabetes as a complication of adipose tissue dysfunction. Is there a role for potential new biomarkers? Clin. Chem. Lab. Med. 2013, 51, 177–185. [Google Scholar] [CrossRef] [Green Version]
- Yuzefovych, L.V.; Musiyenko, S.I.; Wilson, G.L.; Rachek, L.I. Mitochondrial DNA damage and dysfunction, and oxidative stress are associated with endoplasmic reticulum stress, protein degradation and apoptosis in high fat diet-induced insulin resistance mice. PLoS ONE 2013, 8, e54059. [Google Scholar] [CrossRef]
- Litvinova, L.; Atochin, D.N.; Fattakhov, N.; Vasilenko, M.; Zatolokin, P.; Kirienkova, E. Nitric oxide and mitochondria in metabolic syndrome. Front. Physiol. 2015, 6. [Google Scholar] [CrossRef]
- Roberts, J.; Fallon, P.G.; Hams, E. The Pivotal Role of Macrophages in Metabolic Distress. In Macrophage Activation. Biology and Disease; Khalid Hussain Bhat: London, UK, 2020; pp. 1–20. [Google Scholar] [CrossRef] [Green Version]
- Yao, L.; Herlea-Pana, O.; Heuser-Baker, J.; Chen, Y.; Barlic-Dicen, J. Roles of the chemokine system in development of obesity, insulin resistance, and cardiovascular disease. J. Immunol. Res. 2014, 2014, 181450. [Google Scholar] [CrossRef] [Green Version]
- Weisberg, S.P.; Hunter, D.; Huber, R.; Lemieux, J.; Slaymaker, S.; Vaddi, K.; Charo, I.; Leibel, R.L.; Ferrante, A.W. CCR2 modulates inflammatory and metabolic effects of high-fat feeding. J. Clin. Investig. 2006, 116, 115–124. [Google Scholar] [CrossRef] [Green Version]
- Xu, Q.; Wang, J.; He, J.; Zhou, M.; Adi, J.; Webster, K.A.; Yu, H. Impaired CXCR4 expression and cell engraftment of bone marrow-derived cells from aged atherogenic mice. Atherosclerosis 2011, 219, 92–99. [Google Scholar] [CrossRef] [Green Version]
- Ogle, M.E.; Segar, C.E.; Sridhar, S.; Botchwey, E.A. Monocytes and macrophages in tissue repair: Implications for immunoregenerative biomaterial design. Exp. Biol. Med. Maywood NJ 2016, 241, 1084–1097. [Google Scholar] [CrossRef] [PubMed]
- Boyette, L.B.; Macedo, C.; Hadi, K.; Elinoff, B.D.; Walters, J.T.; Ramaswami, B.; Chalasani, G.; Taboas, J.M.; Lakkis, F.G.; Metes, D.M. Phenotype, function, and differentiation potential of human monocyte subsets. PLoS ONE 2017, 12, e0176460. [Google Scholar] [CrossRef]
- Crane, M.J.; Daley, J.M.; van Houtte, O.; Brancato, S.K.; Henry, W.L.; Albina, J.E. The Monocyte to Macrophage Transition in the Murine Sterile Wound. PLoS ONE 2014, 9. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gordon, S.; Taylor, P.R. Monocyte and macrophage heterogeneity. Nat. Rev. Immunol. 2005, 5, 953–964. [Google Scholar] [CrossRef]
- Sica, A.; Mantovani, A. Macrophage plasticity and polarization: In vivo veritas. J. Clin. Investig. 2012, 122, 787–795. [Google Scholar] [CrossRef]
- Zeyda, M.; Farmer, D.; Todoric, J.; Aszmann, O.; Speiser, M.; Györi, G.; Zlabinger, G.J.; Stulnig, T.M. Human adipose tissue macrophages are of an anti-inflammatory phenotype but capable of excessive pro-inflammatory mediator production. Int. J. Obes. 2007, 31, 1420–1428. [Google Scholar] [CrossRef] [Green Version]
- Shaul, M.E.; Bennett, G.; Strissel, K.J.; Greenberg, A.S.; Obin, M.S. Dynamic, M2-Like Remodeling Phenotypes of CD11c+ Adipose Tissue Macrophages During High-Fat Diet–Induced Obesity in Mice. Diabetes 2010, 59, 1171–1181. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kratz, M.; Coats, B.R.; Hisert, K.B.; Hagman, D.; Mutskov, V.; Peris, E.; Schoenfelt, K.Q.; Kuzma, J.N.; Larson, I.; Billing, P.S.; et al. Metabolic dysfunction drives a mechanistically distinct pro-inflammatory phenotype in adipose tissue macrophages. Cell Metab. 2014, 20, 614–625. [Google Scholar] [CrossRef] [Green Version]
- Coats, B.R.; Schoenfelt, K.Q.; Barbosa-Lorenzi, V.C.; Peris, E.; Cui, C.; Hoffman, A.; Zhou, G.; Fernandez, S.; Zhai, L.; Hall, B.A.; et al. Metabolically Activated Adipose Tissue Macrophages Perform Detrimental and Beneficial Functions during Diet-Induced Obesity. Cell Rep. 2017, 20, 3149–3161. [Google Scholar] [CrossRef] [Green Version]
- Haka, A.S.; Barbosa-Lorenzi, V.C.; Lee, H.J.; Falcone, D.J.; Hudis, C.A.; Dannenberg, A.J.; Maxfield, F.R. Exocytosis of macrophage lysosomes leads to digestion of apoptotic adipocytes and foam cell formation. J. Lipid Res. 2016, 57, 980–992. [Google Scholar] [CrossRef] [Green Version]
- Fadok, V.A.; Bratton, D.L.; Konowal, A.; Freed, P.W.; Westcott, J.Y.; Henson, P.M. Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-beta, PGE2, and PAF. J. Clin. Investig. 1998, 101, 890–898. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xu, X.; Grijalva, A.; Skowronski, A.; van Eijk, M.; Serlie, M.J.; Ferrante, A.W. Obesity Activates a Program of Lysosomal-Dependent Lipid Metabolism in Adipose Tissue Macrophages Independently of Classic Activation. Cell Metab. 2013, 18, 816–830. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hotamisligil, G.S.; Shargill, N.S.; Spiegelman, B.M. Adipose expression of tumor necrosis factor-alpha: Direct role in obesity-linked insulin resistance. Science 1993, 259, 87–91. [Google Scholar] [CrossRef] [PubMed]
- Kadl, A.; Meher, A.K.; Sharma, P.R.; Lee, M.Y.; Doran, A.C.; Johnstone, S.R.; Elliott, M.R.; Gruber, F.; Han, J.; Chen, W.; et al. Identification of a novel macrophage phenotype that develops in response to atherogenic phospholipids via Nrf2. Circ. Res. 2010, 107, 737–746. [Google Scholar] [CrossRef]
- Russo, L.; Lumeng, C.N. Properties and functions of adipose tissue macrophages in obesity. Immunology 2018, 155, 407–417. [Google Scholar] [CrossRef]
- Oh, J.Y.; Giles, N.; Landar, A.; Darley-Usmar, V. Accumulation of 15-deoxy-Δ12,14-prostaglandin J2 adduct formation with Keap1 over time: Effects on potency for intracellular antioxidant defense induction. Biochem. J. 2008, 411, 297–306. [Google Scholar] [CrossRef] [Green Version]
- Zhang, D.D. Mechanistic Studies of the Nrf2-Keap1 Signaling Pathway. Drug Metab. Rev. 2006, 38, 769–789. [Google Scholar] [CrossRef]
- Kobayashi, A.; Ohta, T.; Yamamoto, M. Unique function of the Nrf2-Keap1 pathway in the inducible expression of antioxidant and detoxifying enzymes. Methods Enzymol. 2004, 378, 273–286. [Google Scholar] [CrossRef]
- Itoh, K.; Wakabayashi, N.; Katoh, Y.; Ishii, T.; Igarashi, K.; Engel, J.D.; Yamamoto, M. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev. 1999, 13, 76–86. [Google Scholar] [CrossRef] [Green Version]
- Aleksunes, L.M.; Manautou, J.E. Emerging Role of Nrf2 in Protecting Against Hepatic and Gastrointestinal Disease. Toxicol. Pathol. 2016. [Google Scholar] [CrossRef]
- Seimon, T.; Tabas, I. Mechanisms and consequences of macrophage apoptosis in atherosclerosis. J. Lipid Res. 2009, 50, S382–S387. [Google Scholar] [CrossRef] [Green Version]
- Meng, L.-B.; Qi, R.; Xu, L.; Chen, Y.; Yu, Z.; Guo, P.; Gong, T. The more critical murderer of atherosclerosis than lipid metabolism: Chronic stress. Lipids Health Dis. 2018, 17, 143. [Google Scholar] [CrossRef] [Green Version]
- Scalia, R. The microcirculation in adipose tissue inflammation. Rev. Endocr. Metab. Disord. 2013, 14, 69–76. [Google Scholar] [CrossRef]
- Maguire, E.M.; Pearce, S.W.A.; Xiao, Q. Foam cell formation: A new target for fighting atherosclerosis and cardiovascular disease. Vascul. Pharmacol. 2019, 112, 54–71. [Google Scholar] [CrossRef]
- Rucker, A.J.; Crowley, S.D. The role of macrophages in hypertension and its complications. Pflugers Arch. 2017, 469, 419–430. [Google Scholar] [CrossRef] [Green Version]
- Nielsen, M.J.; Møller, H.J.; Moestrup, S.K. Hemoglobin and heme scavenger receptors. Antioxid. Redox Signal. 2010, 12, 261–273. [Google Scholar] [CrossRef]
- Philippidis, P.; Mason, J.C.; Evans, B.J.; Nadra, I.; Taylor, K.M.; Haskard, D.O.; Landis, R.C. Hemoglobin scavenger receptor CD163 mediates interleukin-10 release and heme oxygenase-1 synthesis: Antiinflammatory monocyte-macrophage responses in vitro, in resolving skin blisters in vivo, and after cardiopulmonary bypass surgery. Circ. Res. 2004, 94, 119–126. [Google Scholar] [CrossRef] [Green Version]
- Landis, R.C.; Philippidis, P.; Domin, J.; Boyle, J.J.; Haskard, D.O. Haptoglobin Genotype-Dependent Anti-Inflammatory Signaling in CD163(+) Macrophages. Int. J. Inflamm. 2013, 2013, 980327. [Google Scholar] [CrossRef]
- Finn, A.V.; Nakano, M.; Polavarapu, R.; Karmali, V.; Saeed, O.; Zhao, X.; Yazdani, S.; Otsuka, F.; Davis, T.; Habib, A.; et al. Hemoglobin directs macrophage differentiation and prevents foam cell formation in human atherosclerotic plaques. J. Am. Coll. Cardiol. 2012, 59, 166–177. [Google Scholar] [CrossRef] [Green Version]
- Colin, S.; Chinetti-Gbaguidi, G.; Staels, B. Macrophage phenotypes in atherosclerosis. Immunol Rev. 2014, 262, 153–166. [Google Scholar] [CrossRef]
- Chistiakov, D.A.; Bobryshev, Y.V.; Nikiforov, N.G.; Elizova, N.V.; Sobenin, I.A.; Orekhov, A.N. Macrophage phenotypic plasticity in atherosclerosis: The associated features and the peculiarities of the expression of inflammatory genes. Int. J. Cardiol. 2015, 184, 436–445. [Google Scholar] [CrossRef]
- Boyle, J.J.; Johns, M.; Kampfer, T.; Nguyen, A.T.; Game, L.; Schaer, D.J.; Mason, J.C.; Haskard, D.O. Activating transcription factor 1 directs Mhem atheroprotective macrophages through coordinated iron handling and foam cell protection. Circ. Res. 2012, 110, 20–33. [Google Scholar] [CrossRef] [Green Version]
- Bories, G.; Colin, S.; Vanhoutte, J.; Derudas, B.; Copin, C.; Fanchon, M.; Daoudi, M.; Belloy, L.; Haulon, S.; Zawadzki, C.; et al. Liver X receptor activation stimulates iron export in human alternative macrophages. Circ. Res. 2013, 113, 1196–1205. [Google Scholar] [CrossRef] [Green Version]
- Erbel, C.; Tyka, M.; Helmes, C.M.; Akhavanpoor, M.; Rupp, G.; Domschke, G.; Linden, F.; Wolf, A.; Doesch, A.; Lasitschka, F.; et al. CXCL4-induced plaque macrophages can be specifically identified by co-expression of MMP7+S100A8+ in vitro and in vivo. Innate Immun. 2015, 21, 255–265. [Google Scholar] [CrossRef] [Green Version]
- Gleissner, C.A.; Shaked, I.; Erbel, C.; Böckler, D.; Katus, H.A.; Ley, K. CXCL4 downregulates the atheroprotective hemoglobin receptor CD163 in human macrophages. Circ. Res. 2010, 106, 203–211. [Google Scholar] [CrossRef] [Green Version]
- Deng, H.; Sun, Y.; Zeng, W.; Li, H.; Guo, M.; Yang, L.; Lu, B.; Yu, B.; Fan, G.; Gao, Q.; et al. New Classification of Macrophages in Plaques: A Revolution. Curr Atheroscler Rep. 2020, 22, 31. [Google Scholar] [CrossRef]
- Liu, C.; Li, P.; Li, H.; Wang, S.; Ding, L.; Wang, H.; Ye, H.; Jin, Y.; Hou, J.; Fang, X.; et al. TREM2 regulates obesity-induced insulin resistance via adipose tissue remodeling in mice of high-fat feeding. J. Transl. Med. 2019, 17, 300. [Google Scholar] [CrossRef] [Green Version]
- Graupera, I.; Coll, M.; Pose, E.; Elia, C.; Piano, S.; Solà, E.; Blaya, D.; Huelin, P.; Solé, C.; Moreira, R.; et al. Adipocyte Fatty-Acid Binding Protein is Overexpressed in Cirrhosis and Correlates with Clinical Outcomes. Sci. Rep. 2017, 7. [Google Scholar] [CrossRef]
- Cannon, B.; Nedergaard, J. Brown adipose tissue: Function and physiological significance. Physiol. Rev. 2004, 84, 277–359. [Google Scholar] [CrossRef]
- Ryu, V.; Garretson, J.T.; Liu, Y.; Vaughan, C.H.; Bartness, T.J. Brown adipose tissue has sympathetic-sensory feedback circuits. J. Neurosci. Off. J. Soc. Neurosci. 2015, 35, 2181–2190. [Google Scholar] [CrossRef] [Green Version]
- Bartness, T.J.; Vaughan, C.H.; Song, C.K. Sympathetic and sensory innervation of brown adipose tissue. Int. J. Obes. 2005, 34 (Suppl. 1), S36–S42. [Google Scholar] [CrossRef] [Green Version]
- Klingenspor, M.; Meywirth, A.; Stöhr, S.; Heldmaier, G. Effect of unilateral surgical denervation of brown adipose tissue on uncoupling protein mRNA level and cytochrom-c-oxidase activity in the Djungarian hamster. J. Comp. Physiol. 1994, 163, 664–670. [Google Scholar] [CrossRef]
- Nguyen, K.D.; Qiu, Y.; Cui, X.; Goh, Y.P.S.; Mwangi, J.; David, T.; Mukundan, L.; Brombacher, F.; Locksley, R.M.; Chawla, A. Alternatively activated macrophages produce catecholamines to sustain adaptive thermogenesis. Nature 2011, 480, 104–108. [Google Scholar] [CrossRef] [Green Version]
- 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 2014, 157, 1292–1308. [Google Scholar] [CrossRef] [Green Version]
- Fischer, K.; Ruiz, H.H.; Jhun, K.; Finan, B.; Oberlin, D.J.; van der Heide, V.; Kalinovich, A.V.; Petrovic, N.; Wolf, Y.; Clemmensen, C.; et al. Alternatively activated macrophages do not synthesize catecholamines or contribute to adipose tissue adaptive thermogenesis. Nat. Med. 2017, 23, 623–630. [Google Scholar] [CrossRef]
- Reitman, M.L. How Does Fat Transition from White to Beige? Cell Metab. 2017, 26, 14–16. [Google Scholar] [CrossRef] [Green Version]
- Wolf, Y.; Boura-Halfon, S.; Cortese, N.; Haimon, Z.; Sar Shalom, H.; Kuperman, Y.; Kalchenko, V.; Brandis, A.; David, E.; Segal-Hayoun, Y.; et al. Brown-adipose-tissue macrophages control tissue innervation and homeostatic energy expenditure. Nat. Immunol. 2017, 18, 665–674. [Google Scholar] [CrossRef]
- Luikenhuis, S.; Giacometti, E.; Beard, C.F.; Jaenisch, R. Expression of MeCP2 in postmitotic neurons rescues Rett syndrome in mice. Proc. Natl. Acad. Sci. USA. 2004, 101, 6033–6038. [Google Scholar] [CrossRef] [Green Version]
- Pirzgalska, R.M.; Seixas, E.; Seidman, J.S.; Link, V.M.; Sánchez, N.M.; Mahú, I.; Mendes, R.; Gres, V.; Kubasova, N.; Morris, I.; et al. Sympathetic neuron-associated macrophages contribute to obesity by importing and metabolizing norepinephrine. Nat. Med. 2017, 23, 1309–1318. [Google Scholar] [CrossRef]
- Camell, C.D.; Sander, J.; Spadaro, O.; Lee, A.; Nguyen, K.Y.; Wing, A.; Goldberg, E.L.; Youm, Y.-H.; Brown, C.W.; Elsworth, J.; et al. Inflammasome-driven catecholamine catabolism in macrophages blunts lipolysis during ageing. Nature 2017, 550, 119–123. [Google Scholar] [CrossRef]
- Madden, K.S. Sympathetic neural-immune interactions regulate hematopoiesis, thermoregulation and inflammation in mammals. Dev. Comp. Immunol. 2017, 66, 92–97. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Spadaro, O.; Camell, C.D.; Bosurgi, L.; Nguyen, K.Y.; Youm, Y.-H.; Rothlin, C.V.; Dixit, V.D. IGF1 Shapes Macrophage Activation in Response to Immunometabolic Challenge. Cell Rep. 2017, 19, 225–234. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fernández, A.M.; Kim, J.K.; Yakar, S.; Dupont, J.; Hernandez-Sanchez, C.; Castle, A.L.; Filmore, J.; Shulman, G.I.; Le Roith, D. Functional inactivation of the IGF-I and insulin receptors in skeletal muscle causes type 2 diabetes. Genes Dev. 2001, 15, 1926–1934. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Moses, A.C.; Young, S.C.; Morrow, L.A.; O’Brien, M.; Clemmons, D.R. Recombinant human insulin-like growth factor I increases insulin sensitivity and improves glycemic control in type II diabetes. Diabetes 1996, 45, 91–100. [Google Scholar] [CrossRef] [PubMed]
- Thrailkill, K.M.; Quattrin, T.; Baker, L.; Kuntze, J.E.; Compton, P.G.; Martha, P.M. Cotherapy with recombinant human insulin-like growth factor I and insulin improves glycemic control in type 1 diabetes. RhIGF-I in IDDM Study Group. Diabetes Care 1999, 22, 585–592. [Google Scholar] [CrossRef] [PubMed]
- Milanski, M.; Degasperi, G.; Coope, A.; Morari, J.; Denis, R.; Cintra, D.E.; Tsukumo, D.M.L.; Anhe, G.; Amaral, M.E.; Takahashi, H.K.; et al. Saturated fatty acids produce an inflammatory response predominantly through the activation of TLR4 signaling in hypothalamus: Implications for the pathogenesis of obesity. J. Neurosci. Off. J. Soc. Neurosci. 2009, 29, 359–370. [Google Scholar] [CrossRef]
- Valdearcos, M.; Douglass, J.D.; Robblee, M.M.; Dorfman, M.D.; Stifler, D.R.; Bennett, M.L.; Gerritse, I.; Fasnacht, R.; Barres, B.A.; Thaler, J.P.; et al. Microglial Inflammatory Signaling Orchestrates the Hypothalamic Immune Response to Dietary Excess and Mediates Obesity Susceptibility. Cell Metab. 2017, 26, 185–197.e3. [Google Scholar] [CrossRef] [Green Version]
- Pongratz, G.; Straub, R.H. The sympathetic nervous response in inflammation. Arthritis Res. Ther. 2014, 16, 504. [Google Scholar] [CrossRef] [Green Version]
- Heymann, F.; Tacke, F. Immunology in the liver—From homeostasis to disease. Nat. Rev. Gastroenterol. Hepatol. 2016, 13, 88–110. [Google Scholar] [CrossRef]
- Sierro, F.; Evrard, M.; Rizzetto, S.; Melino, M.; Mitchell, A.J.; Florido, M.; Beattie, L.; Walters, S.B.; Tay, S.S.; Lu, B.; et al. A Liver Capsular Network of Monocyte-Derived Macrophages Restricts Hepatic Dissemination of Intraperitoneal Bacteria by Neutrophil Recruitment. Immunity 2017, 47, 374–388.e6. [Google Scholar] [CrossRef]
- Bonnardel, J.; T’Jonck, W.; Gaublomme, D.; Browaeys, R.; Scott, C.L.; Martens, L.; Vanneste, B.; De Prijck, S.; Nedospasov, S.A.; Kremer, A.; et al. Stellate Cells, Hepatocytes, and Endothelial Cells Imprint the Kupffer Cell Identity on Monocytes Colonizing the Liver Macrophage Niche. Immunity 2019, 51, 638–654.e9. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Theurl, I.; Hilgendorf, I.; Nairz, M.; Tymoszuk, P.; Haschka, D.; Asshoff, M.; He, S.; Gerhardt, L.M.S.; Holderried, T.A.W.; Seifert, M.; et al. On-demand erythrocyte disposal and iron recycling requires transient macrophages in the liver. Nat. Med. 2016, 22, 945–951. [Google Scholar] [CrossRef] [PubMed]
- Remmerie, A.; Scott, C.L. Macrophages and lipid metabolism. Cell. Immunol. 2018, 330, 27–42. [Google Scholar] [CrossRef] [PubMed]
- Krenkel, O.; Tacke, F. Liver macrophages in tissue homeostasis and disease. Nat. Rev. Immunol. 2017, 17, 306–321. [Google Scholar] [CrossRef] [PubMed]
- Chen, J.; Deng, X.; Liu, Y.; Tan, Q.; Huang, G.; Che, Q.; Guo, J.; Su, Z. Kupffer Cells in Non-alcoholic Fatty Liver Disease: Friend or Foe? Int. J. Biol. Sci. 2020, 16, 2367–2378. [Google Scholar] [CrossRef] [PubMed]
- Viola, A.; Munari, F.; Sánchez-Rodríguez, R.; Scolaro, T.; Castegna, A. The Metabolic Signature of Macrophage Responses. Front. Immunol. 2019, 10. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zigmond, E.; Samia-Grinberg, S.; Pasmanik-Chor, M.; Brazowski, E.; Shibolet, O.; Halpern, Z.; Varol, C. Infiltrating Monocyte-Derived Macrophages and Resident Kupffer Cells Display Different Ontogeny and Functions in Acute Liver Injury. J. Immunol. 2014, 193, 344–353. [Google Scholar] [CrossRef] [Green Version]
- Guillot, A.; Tacke, F. Liver Macrophages: Old Dogmas and New Insights. Hepatol. Commun. 2019, 3, 730–743. [Google Scholar] [CrossRef] [Green Version]
- Wang, J.; Kubes, P. A Reservoir of Mature Cavity Macrophages that Can Rapidly Invade Visceral Organs to Affect Tissue Repair. Cell 2016, 165, 668–678. [Google Scholar] [CrossRef] [Green Version]
- Rehermann, B. Mature peritoneal macrophages take an avascular route into the injured liver and promote tissue repair. Hepatology 2017, 65, 376–379. [Google Scholar] [CrossRef] [Green Version]
- Saldarriaga, O.A.; Booth, A.L.; Freiberg, B.; Burks, J.; Krishnan, S.; Rao, A.; Utay, N.; Ferguson, M.; Yi, M.; Beretta, L.; et al. Multispectral Imaging Differentiates Unique Macrophage Profiles in Patients with Distinct Chronic Liver Diseases. Hepatol. Commun. 2019, 4, 708–723. [Google Scholar] [CrossRef] [PubMed]
- Morgantini, C.; Jager, J.; Li, X.; Levi, L.; Azzimato, V.; Sulen, A.; Barreby, E.; Xu, C.; Tencerova, M.; Näslund, E.; et al. Liver macrophages regulate systemic metabolism through non-inflammatory factors. Nat. Metab. 2019, 1, 445–459. [Google Scholar] [CrossRef] [PubMed]
- Rőszer, T. Understanding the Mysterious M2 Macrophage through Activation Markers and Effector Mechanisms Mediators Inflamm. 2015, 816460. [Google Scholar] [CrossRef] [Green Version]
- Tan-Garcia, A.; Lai, F.; Yeong, J.P.S.; Irac, S.E.; Ng, P.Y.; Msallam, R.; Lim, J.C.T.; Wai, L.-E.; Tham, C.Y.L.; Choo, S.P.; et al. Liver fibrosis and CD206+ macrophage accumulation are suppressed by anti-GM-CSF therapy. JHEP Rep. 2020, 2. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dong, B.; Zhou, Y.; Wang, W.; Scott, J.; Kim, K.; Sun, Z.; Guo, Q.; Lu, Y.; Gonzales, N.M.; Wu, H.; et al. Vitamin D Receptor Activation in Liver Macrophages Ameliorates Hepatic Inflammation, Steatosis, and Insulin Resistance in Mice. Hepatology 2020, 71, 1559–1574. [Google Scholar] [CrossRef]
- Loots, M.A.; Lamme, E.N.; Zeegelaar, J.; Mekkes, J.R.; Bos, J.D.; Middelkoop, E. Differences in cellular infiltrate and extracellular matrix of chronic diabetic and venous ulcers versus acute wounds. J. Investig. Dermatol. 1998, 111, 850–857. [Google Scholar] [CrossRef] [Green Version]
- Rf, D.; Mc, E. Wound healing: An overview of acute, fibrotic and delayed healing. Front. Biosci. J. Virtual Libr. 2004, 9, 283–289. [Google Scholar] [CrossRef]
- Galkowska, H.; Olszewski, W.L.; Wojewodzka, U. Keratinocyte and dermal vascular endothelial cell capacities remain unimpaired in the margin of chronic venous ulcer. Arch. Dermatol. Res. 2005, 296, 286–295. [Google Scholar] [CrossRef]
- Ridiandries, A.; Tan, J.T.M.; Bursill, C.A. The Role of Chemokines in Wound Healing. Int. J. Mol. Sci. 2018, 19, 3217. [Google Scholar] [CrossRef] [Green Version]
- Davies, L.C.; Jenkins, S.J.; Allen, J.E.; Taylor, P.R. Tissue-resident macrophages. Nat. Immunol. 2013, 14, 986–995. [Google Scholar] [CrossRef]
- Lucas, T.; Waisman, A.; Ranjan, R.; Roes, J.; Krieg, T.; Müller, W.; Roers, A.; Eming, S.A. Differential roles of macrophages in diverse phases of skin repair. J. Immunol. 1950 2010, 184, 3964–3977. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Italiani, P.; Boraschi, D. From Monocytes to M1/M2 Macrophages: Phenotypical vs. Functional Differentiation. Front. Immunol. 2014, 5. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vågesjö, E.; Öhnstedt, E.; Mortier, A.; Lofton, H.; Huss, F.; Proost, P.; Roos, S.; Phillipson, M. Accelerated wound healing in mice by on-site production and delivery of CXCL12 by transformed lactic acid bacteria. Proc. Natl. Acad. Sci. USA 2018, 115, 1895–1900. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hesketh, M.; Sahin, K.B.; West, Z.E.; Murray, R.Z. Macrophage Phenotypes Regulate Scar Formation and Chronic Wound Healing. Int. J. Mol. Sci. 2017, 18, 1545. [Google Scholar] [CrossRef] [Green Version]
- Kiritsi, D.; Nyström, A. The role of TGFβ in wound healing pathologies. Mech. Ageing Dev. 2018, 172, 51–58. [Google Scholar] [CrossRef]
- Burgess, M.; Wicks, K.; Gardasevic, M.; Mace, K.A. Cx3CR1 Expression Identifies Distinct Macrophage Populations That Contribute Differentially to Inflammation and Repair. ImmunoHorizons 2019, 3, 262–273. [Google Scholar] [CrossRef]
- Boniakowski, A.E.; Kimball, A.S.; Jacobs, B.N.; Kunkel, S.L.; Gallagher, K.A. Macrophage-Mediated Inflammation in Normal and Diabetic Wound Healing. J. Immunol. 2017, 199, 17–24. [Google Scholar] [CrossRef] [Green Version]
- Malissen, B.; Tamoutounour, S.; Henri, S. The origins and functions of dendritic cells and macrophages in the skin. Nat. Rev. Immunol. 2014, 14, 417–428. [Google Scholar] [CrossRef]
- Barman, P.K.; Koh, T.J. Macrophage Dysregulation and Impaired Skin Wound Healing in Diabetes. Front. Cell Dev. Biol. 2020, 8, 528. [Google Scholar] [CrossRef]
- Wang, X.; Cao, Q.; Yu, L.; Shi, H.; Xue, B.; Shi, H. Epigenetic regulation of macrophage polarization and inflammation by DNA methylation in obesity. JCI Insight 2016, 1. [Google Scholar] [CrossRef] [Green Version]
- Krzyszczyk, P.; Schloss, R.; Palmer, A.; Berthiaume, F. The Role of Macrophages in Acute and Chronic Wound Healing and Interventions to Promote Pro-wound Healing Phenotypes. Front. Physiol. 2018, 9, 419. [Google Scholar] [CrossRef]
- Chen, L.; Tredget, E.E.; Wu, P.Y.G.; Wu, Y. Paracrine factors of mesenchymal stem cells recruit macrophages and endothelial lineage cells and enhance wound healing. PLoS ONE 2008, 3, e1886. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhao, W.; Lu, H.; Wang, X.; Ransohoff, R.M.; Zhou, L. CX3CR1 deficiency delays acute skeletal muscle injury repair by impairing macrophage functions. FASEB J. Off. Publ. Fed. Am. Soc. Exp. Biol. 2016, 30, 380–393. [Google Scholar] [CrossRef] [Green Version]
- den Dekker, A.; Davis, F.M.; Kunkel, S.L.; Gallagher, K.A. Targeting epigenetic mechanisms in diabetic wound healing. Transl. Res. 2019, 204, 39–50. [Google Scholar] [CrossRef]
- Wood, S.; Jayaraman, V.; Huelsmann, E.J.; Bonish, B.; Burgad, D.; Sivaramakrishnan, G.; Qin, S.; DiPietro, L.A.; Zloza, A.; Zhang, C.; et al. Pro-inflammatory chemokine CCL2 (MCP-1) promotes healing in diabetic wounds by restoring the macrophage response. PLoS ONE 2014, 9, e91574. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ochoa, O.; Torres, F.M.; Shireman, P.K. Chemokines and diabetic wound healing. Vascular 2007, 15, 350–355. [Google Scholar] [CrossRef]
- Wetzler, C.; Kämpfer, H.; Stallmeyer, B.; Pfeilschifter, J.; Frank, S. Large and sustained induction of chemokines during impaired wound healing in the genetically diabetic mouse: Prolonged persistence of neutrophils and macrophages during the late phase of repair. J. Investig. Dermatol. 2000, 115, 245–253. [Google Scholar] [CrossRef] [Green Version]
- Kimball, A.; Schaller, M.; Joshi, A.; Davis, F.M.; denDekker, A.; Boniakowski, A.; Bermick, J.; Obi, A.; Moore, B.; Henke, P.K.; et al. Ly6CHi Blood Monocyte/Macrophage Drive Chronic Inflammation and Impair Wound Healing in Diabetes Mellitus. Arterioscler. Thromb. Vasc. Biol. 2018, 38, 1102–1114. [Google Scholar] [CrossRef] [Green Version]
- Mirza, R.E.; Fang, M.M.; Novak, M.L.; Urao, N.; Sui, A.; Ennis, W.J.; Koh, T.J. Macrophage PPARγ and impaired wound healing in type 2 diabetes. J. Pathol. 2015, 236, 433–444. [Google Scholar] [CrossRef]
- Silveira, L.S.; Batatinha, H.A.P.; Castoldi, A.; Câmara, N.O.S.; Festuccia, W.T.; Souza, C.O.; Rosa Neto, J.C.; Lira, F.S. Exercise rescues the immune response fine-tuned impaired by peroxisome proliferator-activated receptors γ deletion in macrophages. J. Cell. Physiol. 2019, 234, 5241–5251. [Google Scholar] [CrossRef]
- Daryabor, G.; Atashzar, M.R.; Kabelitz, D.; Meri, S.; Kalantar, K. The Effects of Type 2 Diabetes Mellitus on Organ Metabolism and the Immune System. Front. Immunol. 2020, 11. [Google Scholar] [CrossRef]
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Skuratovskaia, D.; Vulf, M.; Khaziakhmatova, O.; Malashchenko, V.; Komar, A.; Shunkin, E.; Shupletsova, V.; Goncharov, A.; Urazova, O.; Litvinova, L. Tissue-Specific Role of Macrophages in Noninfectious Inflammatory Disorders. Biomedicines 2020, 8, 400. https://doi.org/10.3390/biomedicines8100400
Skuratovskaia D, Vulf M, Khaziakhmatova O, Malashchenko V, Komar A, Shunkin E, Shupletsova V, Goncharov A, Urazova O, Litvinova L. Tissue-Specific Role of Macrophages in Noninfectious Inflammatory Disorders. Biomedicines. 2020; 8(10):400. https://doi.org/10.3390/biomedicines8100400
Chicago/Turabian StyleSkuratovskaia, Daria, Maria Vulf, Olga Khaziakhmatova, Vladimir Malashchenko, Aleksandra Komar, Egor Shunkin, Valeriya Shupletsova, Andrei Goncharov, Olga Urazova, and Larisa Litvinova. 2020. "Tissue-Specific Role of Macrophages in Noninfectious Inflammatory Disorders" Biomedicines 8, no. 10: 400. https://doi.org/10.3390/biomedicines8100400
APA StyleSkuratovskaia, D., Vulf, M., Khaziakhmatova, O., Malashchenko, V., Komar, A., Shunkin, E., Shupletsova, V., Goncharov, A., Urazova, O., & Litvinova, L. (2020). Tissue-Specific Role of Macrophages in Noninfectious Inflammatory Disorders. Biomedicines, 8(10), 400. https://doi.org/10.3390/biomedicines8100400