Поляризация макрофагов: механизмы, маркеры и факторы индукции
Автор: Федоров А.А., Ермак Н.А., Геращенко Т.С., Топольницкий Е.Б., Шефер Н.А., Родионов Е.О., Стахеева М.Н.
Журнал: Сибирский онкологический журнал @siboncoj
Рубрика: Обзоры
Статья в выпуске: 4 т.21, 2022 года.
Бесплатный доступ
Макрофаги являются ключевыми компонентами врожденной иммунной системы. Вариативность участия макрофагов в различных патологических процессах, определяемая их функциональной поляризацией, открывает широкую перспективу для модуляции их функционального профиля для использования в терапевтических целях. Цель исследования - предоставить современные данные о процессе поляризации макрофагов, механизмах его регуляции, маркерах поляризации и факторах индукции. Материал и методы. Проведен поиск доступных литературных источников, опубликованных в базах данных Web of science, scopus и др. Найдено более 160 источников, посвященных изучению процесса поляризации макрофагов, из которых 121 включен в данный обзор. Результаты. В обзоре представлены данные о молекулярных механизмах и генных сигнатурах, ассоциированных с М1- и М2-поляризацией макрофагов, информация о метаболических, фенотипических признаках и цитокиновом профиле М1- и М2-макрофагов, а также освещены данные о факторах поляризации и мишенях их воздействия. Заключение. Представленные в обзоре сведения могут послужить информационной базой для разработки экспериментальных и клинических подходов для редактирования функционального профиля макрофагов с целью управления патологическими процессами с их участием.
Макрофаги, пластичность, факторы поляризация
Короткий адрес: https://sciup.org/140295743
IDR: 140295743 | DOI: 10.21294/1814-4861-2022-21-4-124-136
Список литературы Поляризация макрофагов: механизмы, маркеры и факторы индукции
- Wynn T.A., ChawlaA., Pollard J.W. Macrophage biology in development, homeostasis and disease. Nature. 2013; 496(7446): 445-55. doi: 10.1038/nature12034.
- Ma W.-T., GaoF., Gu K, ChenD.-K. The Role of Monocytes and Macrophages in Autoimmune Diseases: A Comprehensive Review. Front Immunol. 2019; 10(1140). doi: 10.3389/fimmu.2019.01140.
- Sica A., ErreniM., Allavena P., Porta C. Macrophage polarization in pathology. Cell Mo1 Life Sci. 2015; 72(21): 4111-26. doi: 10.1007/ s00018-015-1995-y.
- Das A., Sinha M, Datta S, Abas M, Chaffee S, Sen C.K., Roy S. Monocyte and macrophage plasticity in tissue repair and regeneration. Am J Pathol. 2015; 185(10): 2596-606. doi: 10.1016/j.ajpath.2015.06.001.
- Cheng Z., Zhang D., Gong B., Wang P., Liu F. CD163 as a novel target gene of STAT3 is a potential therapeutic target for gastric cancer. Oncotarget. 2017; 8(50): 87244-62. doi: 10.18632/oncotarget.20244.
- Lan C., Huang X., Lin S., Huang H., Cai Q., Wan T., Lu J., Liu J. Expression of M2-po1arized macrophages is associated with poor prognosis for advanced epithelial ovarian cancer. Tech Cancer Res Treat. 2013; 12(3): 259-67. doi: 10.7785/tcrt.2012.500312.
- Medrek C., Ponten F., Jirstrom K., Leandersson K. The presence of tumor associated macrophages in tumor stroma as a prognostic marker for breast cancer patients. BMC cancer. 2012; 12: 306. doi: 10.1186/14712407-12-306.
- Xu L., Zhu Y., Chen L., An H., Zhang W., Wang G., Lin Z., Xu J. Prognostic value of diametrically polarized tumor-associated macrophages in renal cell carcinoma. Ann Surg Oncol. 2014; 21(9): 3142-50. doi: 10.1245/s10434-014-3601-1.
- Zhang H., Wang X., Shen Z., Xu J., Qin J., Sun Y. Infiltration of diametrically polarized macrophages predicts overall survival of patients with gastric cancer after surgical resection. Gastric Cancer. 2015; 18(4): 740-50. doi: 10.1007/s10120-014-0422-7.
- Zhang W.J., Wang X.H., Gao S.T., Chen C., Xu X.Y., Sun Q, Zhou Z.H., Wu G.Z., Yu Q., Xu G., Yao Y.Z., Guan W.X. Tumor-associated macrophages correlate with phenomenon of epithelial-mesenchymal transition and contribute to poor prognosis in triple-negative breast cancer patients. J Surg Res. 2018; 222: 93-101. doi: 10.1016/j.jss.2017.09.035.
- Wang N., Liang H., Zen K. Molecular mechanisms that influence the macrophage m1-m2 polarization balance. Front Immunol. 2014; 5: 614. doi: 10.3389/fimmu.2014.00614.
- Juhas U., Ryba-Stanistawowska M., Szargiej P., Mysliwska J. Different pathways of macrophage activation and polarization. Postepy higieny i medycyny doswiadczalnej (Online). 2015; 69: 496-502. doi: 10.5604/17322693.1150133.
- Gordon S. Alternative activation of macrophages. Nat Rev Immunol. 2003; 3(1): 23-35. doi: 10.1038/nri978.
- Szanto A., Balint B.L., Nagy Z.S., Barta E., Dezso B, Pap A., Szeles L., Poliska S., Oros M., Evans R.M., Barak Y., Schwabe J., Nagy L. STAT6 transcription factor is a facilitator of the nuclear receptor PPARy-regulated gene expression in macrophages and dendritic cells. Immunity. 2010; 33(5): 699-712. doi: 10.1016/j.immuni.2010.11.009.
- Takeda Y., Costa S., DelamarreE., Roncal C., Leite de OliveiraR., Squadrito M.L., Finisguerra V., Deschoemaeker S., Bruyère F., Wenes M., Hamm A., Serneels J., Magat J., Bhattacharyya T., Anisimov A, Jordan B.F., Alitalo K., Maxwell P., Gallez B., Zhuang Z.W., Saito Y., Simons M., De Palma M., Mazzone M. Macrophage skewing by Phd2 haplodeficiency prevents ischaemia by inducing arteriogenesis. Nature. 2011; 479(7371): 122-6. doi: 10.1038/nature10507.
- Kang K., Reilly S.M., Karabacak V., Gangl M.R., FitzgeraldK., Hatano B., Lee C.H. Adipocyte-derived Th2 cytokines and myeloid PPARdelta regulate macrophage polarization and insulin sensitivity. Cell Metab. 2008; 7(6): 485-95. doi: 10.1016/j.cmet.2008.04.002.
- Odegaard J.I., Ricardo-GonzalezR.R., GoforthM.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. 2007; 447(7148): 1116-20. doi: 10.1038/nature05894.
- 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. 2008; 7(6): 496-507. doi: 10.1016/j.cmet.2008.04.003.
- Mantovani A., Sozzani S., Locati M., Allavena P., Sica A. Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol. 2002; 23(11): 549-55. doi: 10.1016/s1471-4906(02)02302-5.
- Sica A., Bronte V. Altered macrophage differentiation and immune dysfunction in tumor development. J Clin Invest. 2007; 117(5): 1155-66. doi: 10.1172/jci31422.
- Hagemann T., Lawrence T., McNeish I., Charles K.A., Kulbe H., Thompson R.G., Robinson S.C., Balkwill F.R. «Re-educating» tumor-associated macrophages by targeting NF-kappaB. J Exp Med. 2008; 205(6): 1261-8. doi: 10.1084/jem.20080108.
- Lawrence T., Gilroy D.W. Chronic inflammation: a failure of resolution? Int J Exp Pathol. 2007; 88(2): 85-94. doi: 10.1111/j.1365-2613.2006.00507.x.
- Porta C., RimoldiM., Raes G., Brys L., Ghezzi P., Di Liberto D., Dieli F., Ghisletti S., Natoli G., De Baetselier P., Mantovani A., Sica A. Tolerance and M2 (alternative) macrophage polarization are related processes orchestrated by p50 nuclear factor kappaB. Proc Natl Acad Sci USA. 2009; 106(35): 14978-83. doi: 10.1073/pnas.0809784106.
- Italiani P., Mazza E.M., Lucchesi D., Cifola I., Gemelli C., Grande A., Battaglia C., Bicciato S., Boraschi D. Transcriptomic profiling of the development of the inflammatory response in human monocytes in vitro. PloSone. 2014; 9(2): e87680. doi: 10.1371/journal.pone.0087680.
- Raes G., De Baetselier P., Noël W., Beschin A., Brombacher F., Hassanzadeh Gh G. Differential expression of FIZZ1 and Ym1 in alternatively versus classically activated macrophages. J Leukos Biol. 2002; 71(4): 597-602.
- Netea-Maier R.T., Smit J.W.A., Netea M.G. Metabolic changes in tumor cells and tumor-associated macrophages: A mutual relationship. Cancer Lett. 2018; 413: 102-9. doi: 10.1016/j.canlet.2017.10.037.
- FreemermanA.J., JohnsonA.R., Sacks G.N., Milner J.J., KirkE.L., Troester M.A., Macintyre A.N., Goraksha-Hicks P., Rathmell J.C., Makowski L. Metabolic reprogramming of macrophages: glucose transporter 1 (GLUT1)-mediated glucose metabolism drives a proinflammatory phenotype. J Biol Chem. 2014; 289(11): 7884-96. doi: 10.1074/jbc. M113.522037.
- Viola A., Munari F., Sánchez-Rodríguez R., Scolaro T., Castegna A. The Metabolic Signature of Macrophage Responses. Front Immunol. 2019; 10: 1462. doi: 10.3389/fimmu.2019.01462.
- Palsson-McDermottE.M., CurtisA.M., Goel G., LauterbachM.A., Sheedy F.J., Gleeson L.E., van den Bosch M.W., Quinn S.R., Domingo-Fernandez R., Johnston D.G., Jiang J.K., Israelsen W.J., Keane J., Thomas C., Clish C., VanderHeidenM., XavierR.J., O'NeillL.A. Pyruvate kinase M2 regulates Hif-1a activity and IL-1ß induction and is a critical determinant of the warburg effect in LPS-activated macrophages. Cell Metab. 2015; 21(1): 65-80. doi: 10.1016/j.cmet.2014.12.005.
- XieM, Yu Y, KangR, Zhu S, Yang L, Zeng L., SunX., YangM, Billiar T.R., Wang H., Cao L., Jiang J., Tang D. PKM2-dependent glycolysis promotes NLRP3 and AIM2 inflammasome activation. Nature Commun. 2016; 7: 13280. doi: 10.1038/ncomms13280.
- Nagy C., Haschemi A. Time and Demand are Two Critical Dimensions of Immunometabolism: The Process of Macrophage Activation and the Pentose Phosphate Pathway. Front Immunol. 2015; 6: 164. doi: 10.3389/fimmu.2015.00164.
- WilliamsN.C., O'NeillL.A.J. A Role for the Krebs Cycle Intermediate Citrate in Metabolic Reprogramming in Innate Immunity and Inflammation. Front Immunol. 2018; 9: 141. doi: 10.3389/fimmu.2018.00141.
- Infantino V., Convertini P., Cucci L., PanaroM.A., Di NoiaM.A., Calvello R., Palmieri F., Iacobazzi V. The mitochondrial citrate carrier: a new player in inflammation. Biochem J. 2011; 438(3): 433-6. doi: 10.1042/bj20111275.
- Van den Bossche J., O'Neill L.A., Menon D. Macrophage Immu-nometabolism: Where Are We (Going)? Trends Immunol. 2017; 38(6): 395-406. doi: 10.1016/j.it.2017.03.001.
- Tannahill G.M., CurtisA.M., Adamik J., Palsson-McDermottE.M., McGettrick A.F., Goel G., Frezza C., Bernard N.J., Kelly B., Foley N.H., Zheng L., Gardet A., Tong Z., Jany S.S., Corr S.C., Haneklaus M., Caf-frey B.E., Pierce K., Walmsley S., Beasley F.C., Cummins E., Nizet V., WhyteM., Taylor C.T., LinH., MastersS.L., GottliebE., Kelly V.P., Clish C., AuronP.E., XavierR.J., O'NeillL.A. Succinate is an inflammatory signal that induces IL-1ß through HIF-1a. Nature. 2013; 496(7444): 238-42. doi: 10.1038/nature11986.
- Choi J., Stradmann-BellinghausenB., Yakubov E., Savaskan N.E., Régnier-Vigouroux A. Glioblastoma cells induce differential glutamatergic gene expressions in human tumor-associated microglia/macrophages and monocyte-derived macrophages. Cancer Biol Ther. 2015; 16(8): 1205-13. doi: 10.1080/15384047.2015.1056406.
- Colegio O.R., Chu N.Q., Szabo A.L., Chu T., Rhebergen A.M., Jairam V., Cyrus N., Brokowski C.E., Eisenbarth S.C., Phillips G.M., Cline G.W., PhillipsA.J., MedzhitovR. Functional polarization of tumour-associated macrophages by tumour-derived lactic acid. Nature. 2014; 513(7519): 559-63. doi: 10.1038/nature13490.
- Palmieri E.M., Menga A., Martín-Pérez R., Quinto A., Riera-Domingo C., De Tullio G., Hooper D.C., Lamers W.H., Ghesquiere B., McVicar D.W., Guarini A., Mazzone M., Castegna A. Pharmacologic or Genetic Targeting of Glutamine Synthetase Skews Macrophages toward an M1-like Phenotype and Inhibits Tumor Metastasis. Cell Rep. 2017; 20(7): 1654-66. doi: 10.1016/j.celrep.2017.07.054.
- Moon J.S., Nakahira K., Chung K.P., DeNicola G.M., Koo M.J., Pabón M.A., Rooney K.T., Yoon J.H., Ryter S.W., Stout-Delgado H., ChoiA.M. NOX4-dependent fatty acid oxidation promotes NLRP3 inflammasome activation in macrophages. Nature Med. 2016; 22(9): 1002-12. doi: 10.1038/nm.4153.
- WenH., GrisD., Lei Y., JhaS., ZhangL., HuangM.T., Brickey W.J., Ting J.P. Fatty acid-induced NLRP3-ASC inflammasome activation interferes with insulin signaling. Nature Immunol. 2011; 12(5): 408-15. doi: 10.1038/ni.2022.
- Frigerio B., Bizzoni C., Jansen G., Leamon C.P., Peters G.J., Low P.S., Matherly L.H., Figini M. Folate receptors and transporters: biological role and diagnostic/therapeutic targets in cancer and other diseases. J Exp Clin Cancer Res. 2019; 38(1): 125. doi: 10.1186/s13046-019-1123-1.
- Shen J., Hu Y., Putt K.S., Singhal S., Han H., Visscher D.W., Murphy L.M., Low P.S. Assessment of folate receptor alpha and beta expression in selection of lung and pancreatic cancer patients for receptor targeted therapies. Oncotarget. 2018; 9(4): 4485-95. doi: 10.18632/ oncotarget.23321.
- Puig-Kröger A., Sierra-Filardi E., Domínguez-Soto A., Sama-niego R., Corcuera M.T., Gómez-Aguado F., Ratnam M., Sánchez-Mateos P., Corbí A.L. Folate receptor beta is expressed by tumor-associated macrophages and constitutes a marker for M2 anti-inflammatory/regulatory macrophages. Cancer Res. 2009; 69(24): 9395-403. doi: 10.1158/0008-5472.can-09-2050.
- Samaniego R., Palacios B.S., Domiguez-Soto A., Vidal C., Salas A., Matsuyama T., Sánchez-Torres C., de la Torre I., Miranda-Carús M.E., Sánchez-Mateos P., Puig-Kröger A. Macrophage uptake and accumulation of folates are polarization-dependent in vitro and in vivo and are regulated by activin A. J Leukos Biol. 2014; 95(5): 797-808. doi: 10.1189/ jlb.0613345.
- SchmidM.C., Khan S.Q., Kaneda M.M., Pathria P., ShepardR., Louis T.L., Anand S., Woo G., Leem C., Faridi M.H., Geraghty T., Ra-jagopalan A., Gupta S., Ahmed M., Vazquez-Padron R.I., Cheresh D.A., Gupta V., Varner J.A. Integrin CD11b activation drives anti-tumor innate immunity. Nature Commun. 2018; 9(1): 5379. doi: 10.1038/s41467-018 -07387-4.
- ChistiakovD.A., KillingsworthM.C., Myasoedova VA., OrekhovA.N., Bobryshev Y.V. CD68/macrosialin: not just a histochemical marker. Lab Invest. 2017; 97(1): 4-13. doi: 10.1038/labinvest.2016.116.
- Khan S.Q., Khan I., Gupta V CD11b Activity Modulates Pathogenesis of Lupus Nephritis. Front Med. 2018; 5. doi: 10.3389/ fmed.2018.00052.
- Helm O, Held-Feindt J., Schäfer H., Sebens S. M1 and M2: there is no «good» and «bad»-How macrophages promote malignancy-associated features in tumorigenesis. Oncoimmunology. 2014; 3(7): e946818. doi: 10.4161/21624011.2014.946818.
- Ley K. M1 Means Kill; M2 Means Heal. J Immunol. 2017; 199(7): 2191-3. doi: 10.4049/jimmunol.1701135.
- Mantovani A., Biswas S.K., Galdiero M.R., Sica A., Locati M. Macrophage plasticity and polarization in tissue repair and remodelling. J Pathol. 2013; 229(2): 176-85. doi: 10.1002/path.4133.
- Tarique A.A., Logan J., Thomas E., Holt P.G., Sly P.D., Fantino E. Phenotypic, functional, and plasticity features of classical and alternatively activated human macrophages. Am J Resp Cell Mol Biol. 2015; 53(5): 676-88. doi: 10.1165/rcmb.2015-00120C.
- Saraiva D.P., Jacinto A., Borralho P., Braga S., Cabral M.G. HLA-DR in Cytotoxic T Lymphocytes Predicts Breast Cancer Patients' Response to Neoadjuvant Chemotherapy. Front Immunol. 2018; 9. doi: 10.3389/fimmu.2018.02605.
- Xue Q., Yan Y., Zhang R., Xiong H. Regulation of iNOS on Immune Cells and Its Role in Diseases. Int J Mol Sci. 2018; 19(12). doi: 10.3390/ijms19123805.
- Soskic B., Jeffery L.E., Kennedy A., Gardner D.H., Hou T.Z., Hal-liday N., Williams C., Janman D., Rowshanravan B., Hirschfield G.M., Sansom D.M. CD80 on Human T Cells Is Associated With FoxP3 Expression and Supports Treg Homeostasis. Front Immunol. 2021; 11. doi: 10.3389/fimmu.2020.577655.
- Devaraj S., Chen X., Adams-Huet B., Jialal I. Increased expression of Fc-y receptors on monocytes in patients with nascent metabolic syndrome. J Clin Endocrinol Metab. 2013; 98(9): E1510-5. doi: 10.1210/ jc.2013-2112.
- Kzhyshkowska J., Mamidi S., GratchevA., Kremmer E., Schmut-termaier C., Krusell L., Haus G., Utikal J., Schledzewski K., Scholtze J., Goerdt S. Novel stabilin-1 interacting chitinase-like protein (SI-CLP) is up-regulated in alternatively activated macrophages and secreted via lysosomal pathway. Blood. 2006; 107(8): 3221-8. doi: 10.1182/blood-2005-07-2843.
- Pouyafar A., HeydarabadM.Z., Mahboob S., Mokhtarzadeh A., Rahbarghazi R. Angiogenic potential of YKL-40 in the dynamics of tumor niche. Biomed Pharmacother. 2018; 100: 478-85. doi: 10.1016/j. biopha.2018.02.050.
- Rebelo S.P., Pinto C., Martins T.R., Harrer N., Estrada M.F., Loza-AlvarezP., Cabeçadas J., AlvesP.M., GualdaE.J., Sommergruber W., Brito C. 3D-3-culture: A tool to unveil macrophage plasticity in the tumour microenvironment. Biomaterials. 2018; 163: 185-97. doi: 10.1016/j. biomaterials.2018.02.030.
- Tedesco S., Bolego C., Toniolo A., Nassi A., Fadini G.P., Locati M., Cignarella A. Phenotypic activation and pharmacological outcomes of spontaneously differentiated human monocyte-derived macrophages. Im-munobiology. 2015; 220(5): 545-54. doi: 10.1016/j.imbio.2014.12.008.
- Wang S., Zhang J., Sui L., Xu H., Piao Q., Liu Y., Qu X., Sun Y., Song L., Li D., Peng L., Hua S., Hu G., Chen J. Antibiotics induce polarization of pleural macrophages to M2-like phenotype in patients with tuberculous pleuritis. Sci Rep. 2017; 7(1): 14982. doi: 10.1038/s41598-017-14808-9.
- Garton T., Keep R.F., Hua Y., Xi G. CD163, a Hemoglobin/Hap-toglobin Scavenger Receptor, After Intracerebral Hemorrhage: Functions in Microglia/Macrophages Versus Neurons. Transl Stroke Res. 2017; 8(6): 612-6. doi: 10.1007/s12975-017-0535-5.
- Barros M.H., Hauck F., Dreyer J.H., Kempkes B., Niedobitek G. Macrophage polarisation: an immunohistochemical approach for identifying M1 and M2 macrophages. PloSone. 2013; 8(11): e80908. doi: 10.1371/ journal.pone.0080908.
- Tsuchiya K., Suzuki Y., Yoshimura K., Yasui H., Karayama M., HozumiH., FuruhashiK., EnomotoN., Fujisawa T., Nakamura Y., InuiN., YokomuraK., Suda T. Author Correction: Macrophage Mannose Receptor CD206 Predicts Prognosis in Community-acquired Pneumonia. Sci Rep. 2020; 10(1): 3324. doi: 10.1038/s41598-020-58958-9.
- Komohara Y., Jinushi M., Takeya M. Clinical significance of macrophage heterogeneity in human malignant tumors. Cancer Sci. 2014; 105(1): 1-8. doi: 10.1111/cas.12314.
- Jing J., Yang I.V., Hui L., Patel J.A., Evans C.M., Prikeris R., Kobzik L., O'Connor B.P., Schwartz D.A. Role of macrophage receptor with collagenous structure in innate immune tolerance. J Immunol. 2013; 190(12): 6360-7. doi: 10.4049/jimmunol.1202942.
- McMillan S.J., Kearley J., Campbell J.D., ZhuX.W., Larbi K.Y., Shipley J.M., Senior R.M., Nourshargh S., Lloyd C.M. Matrix metal-loproteinase-9 deficiency results in enhanced allergen-induced airway inflammation. J Immunol. 2004; 172(4): 2586-94. doi: 10.4049/ jimmunol.172.4.2586.
- Chavez-Galan L., Olleros M.L., Vesin D., Garcia I. Much More than Ml and M2 Macrophages, There are also CD169(+) and TCR(+) Macrophages. Front Immunol. 2015; 6: 263. doi: 10.3389/ fimmu.2015.00263.
- Liu T., Larionova I., Litviakov N., Riabov V., Zavyalova M., TsyganovM., BuldakovM., Song B., Moganti K., Kazantseva P., Slonim-skayaE., KremmerE., Flatley A., KlüterH., CherdyntsevaN., Kzhyshkowska J. Tumor-associated macrophages in human breast cancer produce new monocyte attracting and pro-angiogenic factor YKL-39 indicative for increased metastasis after neoadjuvant chemotherapy. Oncoimmunology. 2018; 7(6): e1436922. doi: 10.1080/2162402x.2018.1436922.
- Wellner U., Schubert J., Burk U.C., Schmalhofer O., Zhu F., Sonntag A., Waldvogel B., Vannier C., Darling D., zur Hausen A., Brunton V.G., Morton J., Sansom O., Schüler J., Stemmler M.P., Herzberger C., Hopt U., Keck T., Brabletz S., Brabletz T. The EMT-activator ZEB1 promotes tu-morigenicity by repressing stemness-inhibiting microRNAs. Nature Cell Biol. 2009; 11(12): 1487-95. doi: 10.1038/ncb1998.
- HillL., Browne G., TulchinskyE. ZEB/miR-200 feedback loop: at the crossroads of signal transduction in cancer. Int J Cancer. 2013; 132(4): 745-54. doi: 10.1002/ijc.27708.
- StoermerK.A., Burrack A., OkoL., Montgomery S.A., BorstL.B., GillR.G., Morrison T.E. Genetic ablation of arginase 1 in macrophages and neutrophils enhances clearance of an arthritogenic alphavirus. J Immunol. 2012; 189(8): 4047-59. doi: 10.4049/jimmunol.1201240.
- Kalia N., Singh J., Kaur M. The role of dectin-1 in health and disease. Immunobiology. 2021; 226(2): 152071. doi: 10.1016/j. imbio.2021.152071.
- ArangoDuque G., DescoteauxA. Macrophage cytokines: involvement in immunity and infectious diseases. Front Immunol. 2014; 5: 491. doi: 10.3389/fimmu.2014.00491.
- Atri C., Guerfali F.Z., Laouini D. Role of Human Macrophage Polarization in Inflammation during Infectious Diseases. Int J Mol Sci. 2018; 19(6). doi: 10.3390/ijms19061801.
- ZhengX., Turkowski K., Mora J., Brüne B., Seeger W., Weigert A., Savai R. Redirecting tumor-associated macrophages to become tumoricidal effectors as a novel strategy for cancer therapy. Oncotarget. 2017; 8(29): 48436-52. doi: 10.18632/oncotarget.17061.
- Turner M.D., Nedjai B., Hurst T., Pennington D.J. Cytokines and chemokines: At the crossroads of cell signalling and inflammatory disease. Biochim Biophys Acta. 2014; 1843(11): 2563-82. doi: 10.1016/j. bbamcr.2014.05.014.
- Verreck F.A., de Boer T., Langenberg D.M., van der Zanden L., Ottenhoff T.H. Phenotypic and functional profiling of human proinflam-matory type-1 and anti-inflammatory type-2 macrophages in response to microbial antigens and IFN-gamma- and CD40L-mediated costimulation. J Leukos Biol. 2006; 79(2): 285-93. doi: 10.1189/jlb.0105015.
- Wicks I.P., Roberts A.W. Targeting GM-CSF in inflammatory diseases. Nature Rev Rheumatol. 2016; 12(1): 37-48. doi: 10.1038/ nrrheum.2015.161.
- Stanley E.R., Chitu V. CSF-1 receptor signaling in myeloid cells. Cold Spring Harb Rerspect Biol. 2014; 6(6). doi: 10.1101/cshperspect. a021857.
- Hamilton J.A. Colony-stimulating factors in inflammation and autoimmunity. Nature Rev Immunol. 2008; 8(7): 533-44. doi: 10.1038/ nri2356.
- Lacey D.C., Achuthan A., Fleetwood A.J., Dinh H., Roiniotis J., Scholz G.M., Chang M.W., Beckman S.K., Cook A.D., Hamilton J.A. Defining GM-CSF- and macrophage-CSF-dependent macrophage responses by in vitro models. J Immunol. 2012; 188(11): 5752-65. doi: 10.4049/ jimmunol.1103426.
- Ushach I., Zlotnik A. Biological role of granulocyte macrophage colony-stimulating factor (GM-CSF) and macrophage colony-stimulating factor (M-CSF) on cells of the myeloid lineage. J Leukoc Biol. 2016; 100(3): 481-9. doi: https://doi.org/10.1189/jlb.3RU0316-144R.
- Müller E., Christopoulos P.F., Halder S., Lunde A., Beraki K., Speth M., 0ynebraten I., Corthay A. Toll-Like Receptor Ligands and Interferon-y Synergize for Induction of Antitumor M1 Macrophages. Front Immunol. 2017; 8: 1383. doi: 10.3389/fimmu.2017.01383.
- Wang C.Q.F., Suarez-Farinas M., Nograles K.E., Mimoso C.A., Shrom D., Dow E.R., Heffernan M.P., Hoffman R.W., Krueger J.G. IL-17 induces inflammation-associated gene products in blood monocytes, and treatment with ixekizumab reduces their expression in psoriasis patient blood. J Invest Dermatol. 2014; 134(12): 2990-3. doi: 10.1038/ jid.2014.268.
- Netea M.G., Lewis E.C., Azam T., Joosten L.A., Jaekal J., Bae S.Y., Dinarello C.A., Kim S.H. Interleukin-32 induces the differentiation of monocytes into macrophage-like cells. Proc Natl Acad Sci USA. 2008; 105(9): 3515-20. doi: 10.1073/pnas.0712381105.
- Domschke G., Gleissner C.A. CXCL4-induced macrophages in human atherosclerosis. Cytokine. 2019; 122: 154141. doi: 10.1016/j. cyto.2017.08.021.
- Gleissner C.A., Shaked I., Little K.M., Ley K. CXC chemokine ligand 4 induces a unique transcriptome in monocyte-derived macrophages. J Immunol. 2010; 184(9): 4810-8. doi: 10.4049/jimmunol.0901368.
- Sierra-Filardi E., Nieto C., Domínguez-Soto A., Barroso R., Sánchez-Mateos P., Puig-Kroger A., López-BravoM., Joven J., Ardavín C., Rodríguez-Fernández J.L., Sánchez-Torres C., Mellado M., Corbí A.L. CCL2 shapes macrophage polarization by GM-CSF and M-CSF: identification of CCL2/CCR2-dependent gene expression profile. J Immunol. 2014; 192(8): 3858-67. doi: 10.4049/jimmunol.1302821.
- RocaH., Varsos Z.S., SudS., CraigM.J., Ying C., PientaK.J. CCL2 and interleukin-6 promote survival of human CD11b+ peripheral blood mononuclear cells and induce M2-type macrophage polarization. J Biol Chem. 2009; 284(49): 34342-54. doi: 10.1074/jbc.M109.042671.
- Farmaki E., Kaza V., Chatzistamou I., Kiaris H. CCL8 Promotes Postpartum Breast Cancer by Recruiting M2 Macrophages. iScience. 2020; 23(6): 101217. doi: 10.1016/j.isci.2020.101217.
- Fu X.L., Duan W., Su C.Y., Mao F.Y., Lv Y.P., Teng Y.S., Yu P.W., Zhuang Y., Zhao Y.L. Interleukin 6 induces M2 macrophage differentiation by STAT3 activation that correlates with gastric cancer progression. Cancer Immunol Immunother. 2017; 66(12): 1597-608. doi: 10.1007/ s00262-017-2052-5.
- Masteller E.L., Wong B.R. Targeting IL-34 in chronic inflammation. Drug Discovery Today. 2014; 19(8): 1212-6. doi: 10.1016/j. drudis.2014.05.016.
- Boulakirba S., Pfeifer A., Mhaidly R., Obba S., Goulard M., Schmitt T., Chaintreuil P., Calleja A., Furstoss N., Orange F., Lacas-Gervais S., Boyer L., Marchetti S., Verhoeyen E., Luciano F., Robert G., Auberger P., Jacquel A. IL-34 and CSF-1 display an equivalent macrophage differentiation ability but a different polarization potential. Sci Rep. 2018; 8(1): 256. doi: 10.1038/s41598-017-18433-4.
- BaghdadiM., WadaH., Nakanishi S., AbeH., HanN., Putra W.E., Endo D., Watari H., Sakuragi N., Hida Y., Kaga K., Miyagi Y., Yokose T., Takano A., Daigo Y., Seino K.I. Chemotherapy-Induced IL34 Enhances Immunosuppression by Tumor-Associated Macrophages and Mediates Survival of Chemoresistant Lung Cancer Cells. Cancer Res. 2016; 76(20): 6030-42. doi: 10.1158/0008-5472.can-16-1170.
- Oishi Y., Manabe I. Integrated regulation of the cellular metabolism and function of immune cells in adipose tissue. Clin Exp Pharmacol Physiol. 2016; 43(3): 294-303. doi: 10.1111/1440-1681.12539.
- O'Neill L.A., Kishton R.J., Rathmell J. A guide to immunome-tabolism for immunologists. Nature Rev Immunol. 2016; 16(9): 553-65. doi: 10.1038/nri.2016.70.
- Staples K.J., Sotoodehnejadnematalahi F., Pearson H., Frank-enberger M., Francescut L., Ziegler-Heitbrock L., Burke B. Monocyte-derived macrophages matured under prolonged hypoxia transcriptionally up-regulate HIF-1a mRNA. Immunobiology. 2011; 216(7): 832-9. doi: 10.1016/j.imbio.2010.12.005.
- Bonizzi G., KarinM. The two NF-kappaB activation pathways and their role in innate and adaptive immunity. Trends Immunol. 2004; 25(6): 280-8. doi: 10.1016/j.it.2004.03.008.
- HoeksemaM.A., de WintherM.P. Epigenetic Regulation of Monocyte and Macrophage Function. Antioxid Redox Signal. 2016; 25(14): 758-74. doi: 10.1089/ars.2016.6695.
- Davis F.M., Gallagher K.A. Epigenetic Mechanisms in Mono-cytes/Macrophages Regulate Inflammation in Cardiometabolic and Vascular Disease. Arterioscler Thromb Vasc Biol. 2019; 39(4): 623-34. doi: 10.1161/atvbaha.118.312135.
- Holliday R., Pugh J.E. DNA modification mechanisms and gene activity during development. Science. 1975; 187(4173): 226-32.
- Yang X., Wang X., Liu D., Yu L., Xue B., Shi H. Epigenetic regulation of macrophage polarization by DNA methyltransferase 3b. Mol Endocrinol. 2014; 28(4): 565-74. doi: 10.1210/me.2013-1293.
- Cheng C., Huang C., Ma T.T., Bian E.B., He Y., Zhang L., Li J. SOCS1 hypermethylation mediated by DNMT1 is associated with lipopol-ysaccharide-induced inflammatory cytokines in macrophages. Toxicol Lett. 2014; 225(3): 488-97. doi: 10.1016/j.toxlet.2013.12.023.
- LarionovaI., KazakovaE., PatyshevaM., Kzhyshkowska J. Transcriptional, Epigenetic and Metabolic Programming of Tumor-Associated Macrophages. Cancers. 2020; 12(6). doi: 10.3390/cancers12061411.
- Van den Bossche J., Neele A.E., Hoeksema M.A., de Winther M.P. Macrophage polarization: the epigenetic point of view. Curr Opin Lipidol. 2014; 25(5): 367-73. doi: 10.1097/mol.0000000000000109.
- KittanN.A., AllenR.M., Dhaliwal A., CavassaniK.A., SchallerM, GallagherK.A., Carson W.F.t., Mukherjee S., Grembecka J., Cierpicki T., Jarai G., Westwick J., Kunkel S.L., Hogaboam C.M. Cytokine induced phenotypic and epigenetic signatures are key to establishing specific macrophage phenotypes. PloSone. 2013; 8(10): e78045. doi: 10.1371/ journal.pone.0078045.
- Satoh T., Takeuchi O., Vandenbon A., Yasuda K., Tanaka Y., Kumagai Y., Miyake T., Matsushita K., Okazaki T., Saitoh T., Honma K., Matsuyama T., Yui K., Tsujimura T., Standley D.M., Nakanishi K., NakaiK., AkiraS. The Jmjd3-Irf4 axis regulates M2 macrophage polarization and host responses against helminth infection. Nat Immunol. 2010; 11(10): 936-44. doi: 10.1038/ni.1920.
- Feng D., Sangster-Guity N., Stone R., Korczeniewska J., Mancl M.E., Fitzgerald-Bocarsly P., Barnes B.J. Differential requirement of histone acetylase and deacetylase activities for IRF5-mediated proinflammatory cytokine expression. J Immunol. 2010; 185(10): 6003-12. doi: 10.4049/jimmunol.1000482.
- LeusN.G., ZwindermanM.R., DekkerF.J. Histone deacetylase-3 (HDAC 3) as emerging drug target in NF-KB-mediated inflammation. Curr Opin Chem Biol. 2016; 33: 160-8. doi: 10.1016/j.cbpa.2016.06.019.
- 110.MullicanS.E., GaddisC.A., AlenghatT., Nair M.G., GiacominP.R., EverettL.J., Feng D., StegerD.J., Schug J., Artis D., LazarM.A. Histone deacetylase 3 is an epigenomic brake in macrophage alternative activation. Genes Dev. 2011; 25(23): 2480-8. doi: 10.1101/gad.175950.111.
- Graff J.W., Dickson A.M., Clay G., McCaffrey A.P., Wilson M.E. Identifying functional microRNAs in macrophages with polarized phenotypes. J Biol Chem. 2012; 287(26): 21816-25. doi: 10.1074/jbc. M111.327031.
- Cai X., Yin Y., Li N., Zhu D., Zhang J., Zhang C.-Y., Zen K. Re-polarization of tumor-associated macrophages to pro-inflammatory M1 macrophages by microRNA-155. J Mol Cell Biol. 2012; 4(5): 341-3. doi: 10.1093/jmcb/mjs044.
- 113.Martinez-NunezR.T., LouafiF., Sanchez-Elsner T. The interleukin 13 (IL-13) pathway in human macrophages is modulated by microRNA-155 via direct targeting of interleukin 13 receptor alpha1 (IL13Ralpha1). J Biol Chem. 2011; 286(3): 1786-94. doi: 10.1074/jbc.M110.169367.
- Litvak V., Ramsey S.A., Rust A.G., Zak D.E., Kennedy K.A., Lampano A.E., NykterM., Shmulevich I., Aderem A. Function of C/EBP5 in a regulatory circuit that discriminates between transient and persistent TLR4-induced signals. Nat Immunol. 2009; 10(4): 437-43. doi: 10.1038/ ni.1721.
- Lu T., YangX., Huang Y., ZhaoM., Li M., Ma K., Yin J., Zhan C., Wang Q. Trends in the incidence, treatment, and survival of patients with lung cancer in the last four decades. Cancer Manag Res. 2019; 11: 943-53. doi: 10.2147/cmar. s187317.
- Millrud C.R., MehmetiM., LeanderssonK. Docetaxel promotes the generation of anti-tumorigenic human macrophages. Exp Cell Res. 2018; 362(2): 525-31. doi: 10.1016/j.yexcr.2017.12.018.
- Shree T., Olson O.C., Elie B.T., Kester J.C., GarfallA.L., Simpson K., Bell-McGuinnK.M., ZaborE.C., BrogiE., Joyce J.A. Macrophages and cathepsin proteases blunt chemotherapeutic response in breast cancer. Genes Dev. 2011; 25(23): 2465-79. doi: 10.1101/gad.180331.111.
- Bryniarski K., Szczepanik M., Ptak M., Zemelka M., Ptak W. Influence of cyclophosphamide and its metabolic products on the activity of peritoneal macrophages in mice. Pharmacol Rep. 2009; 61(3): 550-7. doi: 10.1016/s1734-1140(09)70098-2.
- Hughes R., Qian B.Z., Rowan C., Muthana M., Keklikoglou I., Olson O.C., Tazzyman S., Danson S., Addison C., ClemonsM., Gonzalez-Angulo A.M., Joyce J.A., De Palma M., Pollard J.W., Lewis C.E. Perivascular M2 Macrophages Stimulate Tumor Relapse after Chemotherapy. Cancer Res. 2015; 75(17): 3479-91. doi: 10.1158/0008-5472.can-14-3587.