The roles of macrophage polarization in the host immune response to sepsis

Singer, 2016, The third international consensus definitions for sepsis and septic shock (Sepsis-3), JAMA, 315, 801, 10.1001/jama.2016.0287 Seymour, 2017, Time to Treatment and Mortality during Mandated Emergency Care for Sepsis, N. Engl. J. Med., 376, 2235, 10.1056/NEJMoa1703058 Kyriacou, 2019, Government Regulation of Sepsis Care, JAMA, J. Am. Med. Assoc., 322, 250, 10.1001/jama.2019.9230 Delano, 2016, The immune system's role in sepsis progression, resolution, and long-term outcome, Immunol. Rev., 274, 330, 10.1111/imr.12499 Hotchkiss, 2013, Immunosuppression in sepsis: a novel understanding of the disorder and a new therapeutic approach, Lancet Infect. Dis., 13, 260, 10.1016/S1473-3099(13)70001-X Chousterman, 2017, Cytokine storm and sepsis disease pathogenesis, Seminars Immunopathol., 39, 517, 10.1007/s00281-017-0639-8 Davies, 2013, Tissue-resident macrophages, Nat. Immunol., 14, 986, 10.1038/ni.2705 Funes, 2018, Implications of macrophage polarization in autoimmunity, Immunology, 154, 186, 10.1111/imm.12910 Paula, 2020, Crosstalk between hypoxia and ER stress response: A key regulator of macrophage polarization, Front. Immunol., 10, 2951, 10.3389/fimmu.2019.02951 Murray, 2014, Macrophage activation and polarization: nomenclature and experimental guidelines - ScienceDirect, Immunity, 41, 14, 10.1016/j.immuni.2014.06.008 Liu, 2014, Macrophage polarization in inflammatory diseases, Int. J. Biol. Sci., 10, 520, 10.7150/ijbs.8879 Biswas, 2012, Macrophage polarization and plasticity in health and disease, Immunol. Res., 53, 11, 10.1007/s12026-012-8291-9 Moghaddam, 2018, Macrophage plasticity, polarization, and function in health and disease, J. Cell. Physiol., 233, 6425, 10.1002/jcp.26429 Patel, 2017, Macrophage polarization in response to epigenetic modifiers during infection and inflammation, Drug Discovery Today, 22, 186, 10.1016/j.drudis.2016.08.006 Murray, 2011, Protective and pathogenic functions of macrophage subsets, Nat. Rev. Immunol., 11, 723, 10.1038/nri3073 Feng, 2014, Pentamethoxyflavanone regulates macrophage polarization and ameliorates sepsis in mice, Biochem. Pharmacol., 89, 109, 10.1016/j.bcp.2014.02.016 Xu, 2019, Inhibition of PTP1B promotes M2 polarization via MicroRNA-26a/MKP1 signaling pathway in murine macrophages, Front. Immunol., 10, 1930, 10.3389/fimmu.2019.01930 Cheng, 2018, Park 7: A Novel therapeutic target for macrophages in sepsis-induced immunosuppression, Front. Immunol., 9, 2632, 10.3389/fimmu.2018.02632 Sica, 2015, Macrophage polarization in pathology, Cell. Mol. Life Sci. Cmls, 72, 4111, 10.1007/s00018-015-1995-y Igor, 2015, Current concept and update of the macrophage plasticity concept: intracellular mechanisms of reprogramming and M3 macrophage “Switch” phenotype, Biomed Res. Int., 2015 Labonte, 2014, The role of macrophage polarization in infectious and inflammatory diseases, Mol. Cells, 37, 275, 10.14348/molcells.2014.2374 Arora, 2018, Macrophages: Their role, activation and polarization in pulmonary diseases, Immunobiology, 223, 383, 10.1016/j.imbio.2017.11.001 Shivshankar, 2014, Caveolin-1 deletion exacerbates cardiac interstitial fibrosis by promoting M2 macrophage activation in mice after myocardial infarction, J. Mol. Cell. Cardiol., 76, 84, 10.1016/j.yjmcc.2014.07.020 Tits, 2011, Oxidized LDL enhances pro-inflammatory responses of alternatively activated M2 macrophages: A crucial role for Krüppel-like factor 2, Atherosclerosis, 214, 345, 10.1016/j.atherosclerosis.2010.11.018 Chiraz, 2018, Role of Human Macrophage Polarization in Inflammation during Infectious Diseases, Int. J. Mol. Sci., 19, 1801, 10.3390/ijms19061801 Vogel, 2014, Human macrophage polarization in vitro: maturation and activation methods compared, Immunobiology, 219, 695, 10.1016/j.imbio.2014.05.002 Paola, 2014, Transcriptomic profiling of the development of the inflammatory response in human monocytes in vitro, PLoS ONE, 9 Porta, 2015, Molecular and epigenetic basis of macrophage polarized activation, Semin. Immunol., 27, 237, 10.1016/j.smim.2015.10.003 Chistiakov, 2015, Macrophage phenotypic plasticity in atherosclerosis: The associated features and the peculiarities of the expression of inflammatory genes, Int. J. Cardiol., 184, 436, 10.1016/j.ijcard.2015.03.055 Kadl, 2010, Identification of a novel macrophage phenotype that develops in response to atherogenic phospholipids via Nrf2, Circ. Res., 107, 737, 10.1161/CIRCRESAHA.109.215715 Gleissner, 2010, CXC chemokine ligand 4 induces a unique transcriptome in monocyte-derived macrophages, J. Immunol., 184, 4810, 10.4049/jimmunol.0901368 Boyle, 2009, Coronary Intraplaque Hemorrhage Evokes a Novel Atheroprotective Macrophage Phenotype, Am. J. Pathol., 174, 1097, 10.2353/ajpath.2009.080431 Yang, 2020, Macrophage Polarization in Atherosclerosis, Clin. Chim. Acta, 501, 142, 10.1016/j.cca.2019.10.034 Chen, 2019, PAR2 promotes M1 macrophage polarization and inflammation via FOXO1 pathway, J. Cell. Biochem., 120, 9799, 10.1002/jcb.28260 Im, 2020, FGF2 alters macrophage polarization, tumour immunity and growth and can be targeted during radiotherapy, Nat. Commun., 11, 4064, 10.1038/s41467-020-17914-x Davis, 2019, Epigenetic Mechanisms in Monocytes/Macrophages Regulate Inflammation in Cardiometabolic and Vascular Disease, Arterioscler. Thromb. Vasc. Biol., 39, 623, 10.1161/ATVBAHA.118.312135 O'Neill, 2016, A guide to immunometabolism for immunologists, Nat. Rev. Immunol., 16, 553, 10.1038/nri.2016.70 Wang, 2019, M1 and M2 macrophage polarization and potentially therapeutic naturally occurring compounds, Int. Immunopharmacol., 70, 459, 10.1016/j.intimp.2019.02.050 Sica, 2012, Macrophage plasticity and polarization: in vivo veritas, J. Clin. Investig., 122, 787, 10.1172/JCI59643 Date, 2014, Kruppel-like Transcription Factor 6 Regulates Inflammatory Macrophage Polarization, J. Biol. Chem., 289, 10318, 10.1074/jbc.M113.526749 Ghoreschi, 2009, Janus kinases in immune cell signaling, Immunol. Rev., 228, 273, 10.1111/j.1600-065X.2008.00754.x Zhao, 2016, Protective effect of suppressing STAT3 activity in LPS-induced acute lung injury, Am. J. Physiol. Lung Cell. Mol. Physiol., 311, L868, 10.1152/ajplung.00281.2016 Zhou, 2014, Macrophage polarization and function with emphasis on the evolving roles of coordinated regulation of cellular signaling pathways, Cell. Signal., 26, 192, 10.1016/j.cellsig.2013.11.004 Wilson, 2014, SOCS Proteins in Macrophage Polarization and Function, Front. Immunol., 5, 357, 10.3389/fimmu.2014.00357 Chen, 2020, Macrophage polarization and its role in the pathogenesis of acute lung injury/acute respiratory distress syndrome, Agents Actions, 69, 883 Amanda, 2015, PPARγ and the Innate Immune System Mediate the Resolution of Inflammation, PPAR Res., 2015 Odegaard, 2007, Macrophage-specific PPARγ controls alternative activation and improves insulin resistance, Nature, 447, 1116, 10.1038/nature05894 Liao, 2011, Kruppel-like factor 4 regulates macrophage polarization, J. Clin. Investig., 121, 2736, 10.1172/JCI45444 Pello, 2012, Role of c-MYC in alternative activation of human macrophages and tumor-associated macrophage biology, Blood, 119, 411, 10.1182/blood-2011-02-339911 Hao, 2017, Involvement of JNK signaling in IL4-induced M2 macrophage polarization, Exp. Cell Res., 357, 155, 10.1016/j.yexcr.2017.05.010 Tawakol, 2015, HIF-1α and PFKFB3 Mediate a Tight Relationship Between Proinflammatory Activation and Anerobic Metabolism in Atherosclerotic Macrophages, Arterioscler. Thromb. Vasc. Biol., 35, 1463, 10.1161/ATVBAHA.115.305551 Takeda, 2010, Differential activation and antagonistic function of HIF-{alpha} isoforms in macrophages are essential for NO homeostasis, Genes Dev., 24, 491, 10.1101/gad.1881410 Ruse, 2006, New players in TLR-mediated innate immunity: PI3K and small Rho GTPases, Immunol. Res., 34, 33, 10.1385/IR:34:1:33 Arranz, 2012, Akt1 and Akt2 protein kinases differentially contribute to macrophage polarization, Proc. Natl. Acad. Sci. U S A, 109, 9517, 10.1073/pnas.1119038109 Arranz, 2012, Akt1 and Akt2 protein kinases differentially contribute to macrophage polarization, Proc. Natl. Acad. Sci., 109, 9517, 10.1073/pnas.1119038109 B.M. Moradi-Chaleshtori, N. Heidari, S. Mohammadi-Yeganeh, S. Mahmoud Hashemi, Exosome-mediated miR-33 transfer induces M1 polarization in mouse macrophages and exerts antitumor effect in 4T1 breast cancer cell line, International Immunopharmacology 90 (2021) 107198. Thulin, 2013, MicroRNA-9 regulates the expression of peroxisome proliferator-activated receptor δ in human monocytes during the inflammatory response, Int. J. Mol. Med., 31, 1003, 10.3892/ijmm.2013.1311 Zhuo, 2015, MicroRNA 21 Is a Homeostatic Regulator of Macrophage Polarization and Prevents Prostaglandin E2-Mediated M2 Generation, PLoS ONE, 10 Kabesch, 2012, Epigenetics in asthma and COPD, Biochimie, 94, 2231, 10.1016/j.biochi.2012.07.017 X. Chen, I. Barozzi, A. Termanini, E. Prosperini, A. Recchiuti, Requirement for the histone deacetylase Hdac3 for the inflammatory gene expression program in macrophages, Proc. Natl. Acad. Sci. 109(42) (2012) E2865-E2874. Chaudhuri, 2011, MicroRNA-125b Potentiates Macrophage Activation, J. Immunol., 187, 5062, 10.4049/jimmunol.1102001 Ying, 2015, MiR-127 modulates macrophage polarization and promotes lung inflammation and injury by activating the JNK pathway, J. Immunol., 194, 1239, 10.4049/jimmunol.1402088 O'Connell, 2007, MicroRNA-155 is induced during the macrophage inflammatory response, Proc. Nat. Acad. Sci. USA, 104, 1604, 10.1073/pnas.0610731104 Feng, 2013, Akt1-mediated regulation of macrophage polarization in a murine model of Staphylococcus aureus pulmonary infection, J. Infect. Dis., 208, 528, 10.1093/infdis/jit177 Caescu, 2015, Colony stimulating factor-1 receptor signaling networks inhibit mouse macrophage inflammatory responses by induction of microRNA-21, Blood, 125, e1, 10.1182/blood-2014-10-608000 Yang, 2013, MicroRNA-124 mediates the cholinergic anti-inflammatory action through inhibiting the production of pro-inflammatory cytokines, Cell Res., 23, 1270, 10.1038/cr.2013.116 H.B. Wang, Y. Wang, C. Wang, H. Zhang, J. Xue, X. Wang, T. Niu, Z. Niu, Y. Chen, Mesenchymal stem cell–secreted extracellular vesicles carrying TGF‐β1 up‐regulate miR‐132 and promote mouse M2 macrophage polarization, J. Cell. Mol. Med. 24(21) (2020) 12750-12764. Xu-Ren, 2020, miR-34a carried by adipocyte exosomes inhibits the polarization of M1 macrophages in mouse osteolysis model, J. Biomed. Mater. Res. Part A, 10 Zhang, 2020, Upregulated MELK leads to doxorubicin chemoresistance and M2 macrophage polarization via the miR-34a/JAK2/STAT3 pathway in uterine leiomyosarcoma, Front. Oncol., 10, 453, 10.3389/fonc.2020.00453 Cui Banerjee, Xie Hc, Yang Tan, Icyuz Sz, Vj Thannickal, miR-125a-5p regulates differential activation of macrophages and inflammation, J. Biol. Chem. 288(49) (2013) 35428-35436. Seeley, 2018, Induction of innate immune memory via microRNA targeting of chromatin remodelling factors, Nature, 559, 114, 10.1038/s41586-018-0253-5 Chen, 2012, Inducible MicroRNA-223 down-regulation promotes TLR-Triggered IL-6 and IL-1β production in macrophages by targeting STAT3, PLoS ONE, 7, 10.1371/journal.pone.0042971 Gou, 2018, MiR-223/Pknox1 axis protects mice from CVB3-induced viral myocarditis by modulating macrophage polarization, Exp. Cell Res., 366, 41, 10.1016/j.yexcr.2018.03.004 Thangavel, 2015, Epigenetic modifiers reduce inflammation and modulate macrophage phenotype during endotoxemia-induced acute lung injury, J. Cell Sci., 128, 3094 Cokus, 2008, Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning, Nature, 452, 215, 10.1038/nature06745 Satoh, 2010, The Jmjd3-Irf4 axis regulates M2 macrophage polarization and host responses against helminth infection, Nat. Immunol., 11, 936, 10.1038/ni.1920 Zhang, 2015, Polycomb-mediated loss of microRNA let-7c determines inflammatory macrophage polarization via PAK1-dependent NF-κB pathway, Cell Death Differ., 22, 287, 10.1038/cdd.2014.142 Banerjee, 2013, MicroRNA let-7c regulates macrophage polarization, J. Immunol., 190, 6542, 10.4049/jimmunol.1202496 Xu, 2015, Histone methyltransferase Smyd2 is a negative regulator of macrophage activation by suppressing IL-6 and TNF-α production, J. Biol. Chem., 290, 5414, 10.1074/jbc.M114.610345 Tsou, 2007, Critical roles for CCR2 and MCP-3 in monocyte mobilization from bone marrow and recruitment to inflammatory sites, J. Clin. Investig., 117, 902, 10.1172/JCI29919 Chen, 2014, Effects of low-level laser therapy on M1-related cytokine expression in monocytes via histone modification, Mediators Inflamm., 2014, 10.1155/2014/625048 Ahmad, 2020, Long Non-coding RNAs RN7SK and GAS5 Regulate Macrophage Polarization and Innate Immune Responses, Front. Immunol., 11, 10.3389/fimmu.2020.604981 Du, 2017, The LPS-inducible lncRNA Mirt2 is a negative regulator of inflammation, Nat. Commun., 8, 2049, 10.1038/s41467-017-02229-1 Rong Cao, Jiang Dong, Gong Yanling, Yuan Meng, You Jieqiong, LncRNA-MM2P identified as a Modulator of Macrophage M2 Polarization, Cancer Immunol. Res. 7(2) (2019) 292-305. Chen, 2020, Lnc-M2 controls M2 macrophage differentiation via the PKA/CREB pathway, Mol. Immunol., 124, 142, 10.1016/j.molimm.2020.06.006 Z.Y. Li, Pei W, LncRNA Dnmt3aos regulates Dnmt3a expression leading to aberrant DNA methylation in macrophage polarization, The FASEB J. 34(4) (2020) 5077-5091. Munteanu, 2020, Long non-coding RNA FENDRR regulates IFNγ-induced M1 phenotype in macrophages, Sci. Rep., 10, 13672, 10.1038/s41598-020-70633-7 Zhang, 2020, Circular RNA circPPM1F modulates M1 macrophage activation and pancreatic islet inflammation in type 1 diabetes mellitus, Theranostics, 10, 10908, 10.7150/thno.48264 Wu, 2010, Active DNA demethylation: many roads lead to Rome, Nat. Rev. Mol. Cell Biol., 11, 607, 10.1038/nrm2950 Xiaosong, 2014, Epigenetic regulation of macrophage polarization by DNA methyltransferase 3b, Mol. Endocrinol., 28, 565, 10.1210/me.2013-1293 Nadal, 2018, Synthetic post-translational modification of histones, Curr. Opin. Chem. Biol., 45, 35, 10.1016/j.cbpa.2018.02.004 Bossche, 2014, Macrophage polarization: the epigenetic point of view, Curr. Opin. Lipidol., 25, 367, 10.1097/MOL.0000000000000109 Chen, 2020, Epigenetic regulation of macrophages: from homeostasis maintenance to host defense, Cell. Mol. Immunol., 17, 36, 10.1038/s41423-019-0315-0 Loftus, 2016, Immunometabolism: cellular metabolism turns immune regulator, J. Biol. Chem., 291, 1, 10.1074/jbc.R115.693903 Liu, 2020, Research progress of metabolism reprogramming in regulating macrophage polarization, Zhonghua Wei Zhong Bing Ji Jiu Yi Xue, 32, 765 Mills, 2017, Mitochondria are the powerhouses of immunity, Nat. Immunol., 18, 488, 10.1038/ni.3704 Freemerman, 2014, Metabolic reprogramming of macrophages: glucose transporter 1 (GLUT1)-mediated glucose metabolism drives a proinflammatory phenotype, J. Biol. Chem., 289, 7884, 10.1074/jbc.M113.522037 Geeraerts, 2017, Macrophage metabolism as therapeutic target for cancer, atherosclerosis, and obesity, Front. Immunol., 8, 289, 10.3389/fimmu.2017.00289 Mills, 2016, Succinate dehydrogenase supports metabolic repurposing of mitochondria to drive inflammatory macrophages, Cell, 167, 457, 10.1016/j.cell.2016.08.064 Tannahill, 2013, Succinate is an inflammatory signal that induces IL-1β through HIF-1α, Nature, 496, 238, 10.1038/nature11986 Moon, 2015, UCP2-induced fatty acid synthase promotes NLRP3 inflammasome activation during sepsis, J. Clin. Invest., 125, 665, 10.1172/JCI78253 Wang, 2017, Diosgenin glucoside provides neuroprotection by regulating microglial M1 polarization, Int. Immunopharmacol., 50, 22, 10.1016/j.intimp.2017.06.008 Zhu, 2016, The pentacyclic triterpene Lupeol switches M1 macrophages to M2 and ameliorates experimental inflammatory bowel disease, Int. Immunopharmacol., 30, 74, 10.1016/j.intimp.2015.11.031 Li, 2018, Crocin alleviates coronary atherosclerosis via inhibiting lipid synthesis and inducing M2 macrophage polarization, Int. Immunopharmacol., 55, 120, 10.1016/j.intimp.2017.11.037 Tan, 2015, Src/STAT3-dependent heme oxygenase-1 induction mediates chemoresistance of breast cancer cells to doxorubicin by promoting autophagy, Cancer Sci., 106, 1023, 10.1111/cas.12712 Iwanowycz, 2016, Emodin bidirectionally modulates macrophage polarization and epigenetically regulates macrophage memory, J. Biol. Chem., 291, 11491, 10.1074/jbc.M115.702092 Wang, 2021, Isobavachalcone prevents osteoporosis by suppressing activation of ERK and NF-κB pathways and M1 polarization of macrophages, Int. Immunopharmacol., 94, 10.1016/j.intimp.2021.107370 Liu, 2018, Berberine inhibits macrophage M1 polarization via AKT1/SOCS1/NF-κB signaling pathway to protect against DSS-induced colitis, Int. Immunopharmacol., 57, 121, 10.1016/j.intimp.2018.01.049 Zhao, 2020, Salvianolic acid B regulates macrophage polarization in ischemic/reperfused hearts by inhibiting mTORC1-induced glycolysis, Eur. J. Pharmacol., 871, 10.1016/j.ejphar.2020.172916 Nyiramana, 2020, Sea hare hydrolysate-induced reduction of human non-small cell lung cancer cell growth through regulation of macrophage polarization and non-apoptotic regulated cell death pathways, Cancers (Basel), 12, 726, 10.3390/cancers12030726 Feng, 2020, TLR-2-mediated metabolic reprogramming participates in polyene phosphatidylcholine-mediated inhibition of M1 macrophage polarization, Immunol. Res., 68, 28, 10.1007/s12026-020-09125-9 Wang, 2020, Effect of (R)-salbutamol on the switch of phenotype and metabolic pattern in LPS-induced macrophage cells, J. Cell Mol. Med., 24, 722, 10.1111/jcmm.14780 Ariyoshi, 2017, Mechanisms involved in enhancement of matrix metalloproteinase-9 expression in macrophages by interleukin-33, J. Cell. Physiol., 232, 3481, 10.1002/jcp.25809 Tong, 2021, The HIV protease inhibitor Saquinavir attenuates sepsis-induced acute lung injury and promotes M2 macrophage polarization via targeting matrix metalloproteinase-9, Cell Death Dis., 12, 67, 10.1038/s41419-020-03320-0 L.D. Zhuo Y, Cui L, Li C, Zhang S, Zhang Q, Zhang L, Wang X, Yang L, Treatment with 3,4-dihydroxyphenylethyl alcohol glycoside ameliorates sepsis-induced ALI in mice by reducing inflammation and regulating M1 polarization - ScienceDirect, Biomedicine & Pharmacotherapy 116 (2019) 109012. Y. Zhang, T. Huang, L. Jiang, J. Gao, D. Yu, Y. Ge, S. Lin, MCP-induced protein 1 attenuates sepsis-induced acute lung injury by modulating macrophage polarization via the JNK/c-Myc pathway, Int. Immunopharmacol. 75 (2019) 105741. Zhang, 2020, The anti-inflammatory mediator Resolvin E1 protects mice against lipopolysaccharide-induced heart injury, Front. Pharmacol., 11, 203, 10.3389/fphar.2020.00203 Shu, 2018, Blockade of CD38 diminishes lipopolysaccharide-induced macrophage classical activation and acute kidney injury involving NF-κB signaling suppression, Cell. Signal., 42, 249, 10.1016/j.cellsig.2017.10.014 Bai, 2020, Extracellular vesicles from adipose tissue-derived stem cells affect Notch-miR148a-3p Axis to regulate polarization of macrophages and alleviate sepsis in mice, Front. Immunol., 11, 1391, 10.3389/fimmu.2020.01391 Tang, 2017, Soluble egg antigen activates M2 macrophages via the STAT6 and PI3K pathways, and Schistosoma Japonicum alternatively activates macrophage polarization to improve the survival rate of septic mice, J. Cell. Biochem., 118, 4230, 10.1002/jcb.26073 Deng, 2020, Bone marrow mesenchymal stem cell-derived exosomes attenuate LPS-induced ARDS by modulating macrophage polarization through inhibiting glycolysis in macrophages, Shock, 54, 828, 10.1097/SHK.0000000000001549 M. Yao, B. Cui, W. Zhang, W. Ma, G. Zhao, L. Xing, Exosomal miR-21 secreted by IL-1β-primed-mesenchymal stem cells induces macrophage M2 polarization and ameliorates sepsis - ScienceDirect, Life Sci. 264 (2021) 118658. Zhou, 2020, Extracellular CIRP induces macrophage endotoxin tolerance through IL-6R-mediated STAT3 activation, JCI Insight, 5, 10.1172/jci.insight.133715 Wang, 2019, M2b macrophage polarization and its roles in diseases, J. Leukoc. Biol., 106, 345, 10.1002/JLB.3RU1018-378RR Nishiguchi, 2017, Macrophage polarization and MRSA infection in burned mice, Immunol. Cell Biol., 95, 198, 10.1038/icb.2016.84 Ito, 2016, The polarization of M2b monocytes in cultures of burn patient peripheral CD14 cells treated with a selected human CCL1 antisense oligodeoxynucleotide, Nucleic Acid Ther., 26, 269, 10.1089/nat.2016.0617 Kobayashi, 2012, Role of M2b macrophages in the acceleration of bacterial translocation and subsequent sepsis in mice exposed to whole body [137Cs] γ-irradiation, J. Immunol., 189, 296, 10.4049/jimmunol.1200350 Yao, 2020, Constitutively expressed MHC class Ib molecules regulate macrophage M2b polarization and sepsis severity in irradiated mice, J. Leukoc. Biol., 107, 445, 10.1002/JLB.1AB1219-125RR Shigematsu, 2009, Enterococcus faecalis translocation in mice with severe burn injury: a pathogenic role of CCL2 and alternatively activated macrophages (M2aMphi and M2cMphi), J. Leukoc. Biol., 86, 999, 10.1189/jlb.0409235 Wakeley, 2020, Check point inhibitors and their role in immunosuppression in sepsis, Crit. Care Clin., 36, 69, 10.1016/j.ccc.2019.08.006 Wolf, 2020, TIM3 comes of age as an inhibitory receptor, Nat. Rev. Immunol., 20, 173, 10.1038/s41577-019-0224-6 Yang, 2013, T cell Ig Mucin-3 promotes homeostasis of sepsis by negatively regulating the TLR response, J. Immunol., 190, 2068, 10.4049/jimmunol.1202661 L.A. van Vught, P.M.C. Klein Klouwenberg, C. Spitoni, B.P. Scicluna, M.A. Wiewel, J. Horn, M.J. Schultz, P. Nürnberg, M.J.M. Bonten, O.L. Cremer, T. van der Poll, M. Consortium, Incidence, risk factors, and attributable mortality of secondary infections in the intensive care unit after admission for sepsis, JAMA 315(14) (2016) 1469–1479. McBride, 2020, The metabolic basis of immune dysfunction following sepsis and Trauma, Front. Immunol., 11, 1043, 10.3389/fimmu.2020.01043 Rackov, 2016, p21 mediates macrophage reprogramming through regulation of p50–p50 NF-κB and IFN-β, J. Clin. Invest., 126, 3089, 10.1172/JCI83404 Cui, 2019, Trichostatin A modulates the macrophage phenotype by enhancing autophagy to reduce inflammation during polymicrobial sepsis, Int. Immunopharmacol., 77, 10.1016/j.intimp.2019.105973 Li, 2020, Csf2 attenuated sepsis-induced acute kidney injury by promoting alternative macrophage transition, Front. Immunol., 11, 1415, 10.3389/fimmu.2020.01415 L. Guo, M. Meng, Y. Wei, F. Lin, Y. Jiang, X. Cui, G. Wang, C. Wang, X. Guo, B. Subtilis, Protective effects of live combined and in polymicrobial sepsis through modulating activation and transformation of macrophages and mast cells, Front. Pharmacol. 9 (2018) 1506. Shimizu, 2018, Synbiotics modulate gut microbiota and reduce enteritis and ventilator-associated pneumonia in patients with sepsis: a randomized controlled trial, Crit. Care, 22, 239, 10.1186/s13054-018-2167-x Wang, 2016, Therapeutic potential of recombinant cystatin from Schistosoma japonicum in TNBS-induced experimental colitis of mice, Parasit Vectors, 9, 6, 10.1186/s13071-015-1288-1 Xie, 2021, Schistosoma japonicum cystatin alleviates sepsis through activating regulatory macrophages, Front. Cell Infect. Microbiol., 11, 10.3389/fcimb.2021.617461 Fallon, 2017, Program cell death receptor-1-mediated invariant natural killer T-cell control of peritoneal macrophage modulates survival in neonatal sepsis, Front. Immunol., 8, 1469, 10.3389/fimmu.2017.01469 Condotta, 2015, Polymicrobial sepsis increases susceptibility to chronic viral infection and exacerbates CD8+ T cell exhaustion, J. Immunol., 195, 116, 10.4049/jimmunol.1402473 Wei, 2021, PD-L1 induces macrophage polarization toward the M2 phenotype via Erk/Akt/mTOR, Exp. Cell Res., 402, 10.1016/j.yexcr.2021.112575 Hotchkiss, 2019, Immune checkpoint inhibition in sepsis: a Phase 1b randomized study to evaluate the safety, tolerability, pharmacokinetics, and pharmacodynamics of nivolumab, Intensive Care Med., 45, 1360, 10.1007/s00134-019-05704-z Hotchkiss, 2019, Immune checkpoint inhibition in sepsis: A phase 1b randomized, placebo-controlled, single ascending dose study of antiprogrammed cell death-ligand 1 antibody (BMS-936559), Crit. Care Med., 47, 632, 10.1097/CCM.0000000000003685 Ingersoll, 2011, Monocyte trafficking in acute and chronic inflammation, Trends Immunol., 32, 470, 10.1016/j.it.2011.05.001 E.L. Soucie, W. Ziming, G. Laufey, M. Kaaweh, M. Julien, F. Romain, M.K. Noushine, G. Gregory, V.H. Laurent, B. Meryam, Lineage-specific enhancers activate self-renewal genes in macrophages and embryonic stem cells, Science (New York, N.Y.) 351(6274) (2016) aad5510.