MiRNA-mediated macrophage polarization and its potential role in the regulation of inflammatory response

Shock

Volumn 46, Issue 2, 2016, Pages 122-131

  Essandoh, Kobina ^a   Li, Yutian ^a   Huo, Jiuzhou ^a   Fan, Guo Chang ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

Inflammation; macrophage polarization; microRNAs; monocytes; sepsis

Indexed keywords

ADAPTOR PROTEIN; CYTOKINE; MICRORNA; MICRORNA 124; MICRORNA 125A 5P; MICRORNA 125B; MICRORNA 127; MICRORNA 132; MICRORNA 146A; MICRORNA 155; MICRORNA 223; MICRORNA 34A; MICRORNA 9; MICRORNA LET 7C; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; BIOGENESIS; CARCINOGENESIS; CELL GROWTH; CYTOKINE PRODUCTION; DISEASE COURSE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMAN; IMMUNOSUPPRESSIVE TREATMENT; INFLAMMATION; INNATE IMMUNITY; MACROPHAGE ACTIVATION; MACROPHAGE FUNCTION; MACROPHAGE POLARIZATION; MULTIPLE SCLEROSIS; NEOPLASM; NONHUMAN; OBESITY; PARASITE CLEARANCE; PHENOTYPE; POLARIZATION; PROTEIN TARGETING; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; SEPSIS; WOUND HEALING; ANIMAL; CELL POLARITY; CYTOLOGY; GENETICS; IMMUNOLOGY; MACROPHAGE; METABOLISM; MOUSE; PHYSIOLOGY;

ANIMALS; CELL POLARITY; HUMANS; INFLAMMATION; MACROPHAGE ACTIVATION; MACROPHAGES; MICE; MICRORNAS;

EID: 84960192985     PISSN: 10732322     EISSN: 15400514     Source Type: Journal    
DOI: 10.1097/SHK.0000000000000604     Document Type: Review

References (98)

1. Yang J, Zhang L, Yu C, Yang X-F, Wang H. Monocyte and macrophage differentiation: circulation inflammatory monocyte as biomarker for inflammatory diseases. Biomarker Res 2: 1, 2014
2. Epelman S, Lavine KJ, Randolph GJ. Origin and functions of tissue macrophages. Immunity 41(1): 21-35, 2014
3. Sica A, Mantovani A. Macrophage plasticity and polarization: in vivo veritas. J Clin Invest 122(3): 787-795, 2012
4. Deiuliis JA. MicroRNAs as regulators of metabolic disease: pathophysiologic significance and emerging role as biomarkers and therapeutics. Int J Obes (Lond) 40(1): 88-101, 2016
5. Liu G, Abraham E. MicroRNAs in immune response and macrophage polarization. Arterioscler Thromb Vasc Biol 33(2): 170-177, 2013
6. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 136(2): 215-233, 2009
7. Guo H, Ingolia NT, Weissman JS, Bartel DP. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 466(7308): 835-840, 2010
8. Wang X, Huang W, Yang Y, Wang Y, Peng T, Chang J, Caldwell CC, Zingarelli B, Fan GC. Loss of duplexmiR-223 (5p and 3p) aggravates myocardial depression and mortality in polymicrobial sepsis. Biochim Biophys Acta 1842(5): 701-711, 2014
9. Zhang J, Li S, Li L, Li M, Guo C, Yao J, Mi S. Exosome and exosomal microRNA: trafficking, sorting, and function. Genomics Proteomics Bioinformatics 13(1): 17-24, 2015
10. Wang X, Gu H, Qin D, Yang L, Huang W, Essandoh K, Wang Y, Caldwell CC, Peng T, Zingarelli B, et al. Exosomal miR-223 contributes to mesenchymal stem cell-elicited cardioprotection in polymicrobial sepsis. Sci Rep 5: 13721, 2015
11. Alexander M, Hu R, Runtsch MC, Kagele DA, Mosbruger TL, Tolmachova T, Seabra MC, Round JL, Ward DM, O'Connell RM. Exosome-delivered micro-RNAs modulate the inflammatory response to endotoxin. Nat Commun 6: 7321, 2015
12. Muñoz-Fernández MA, Fernández MA, Fresno M. Synergism between tumor necrosis factor-alpha and interferon-gamma on macrophage activation for the killing of intracellular Trypanosoma cruzi through a nitric oxide-dependent mechanism. Eur J Immunol 22(2): 301-307, 1992
13. Stout RD, Suttles J, Xu J, Grewal IS, Flavell RA. Impaired T cell-mediated macrophage activation in CD40 ligand-deficient mice. J Immunol 156(1): 8-11, 1996
14. Bekker LG, Freeman S, Murray PJ, Ryffel B, Kaplan G. TNF-alpha controls intracellular mycobacterial growth by both inducible nitric oxide synthasedependent and inducible nitric oxide synthase-independent pathways. J Immunol 166(11): 6728-6734, 2001
15. Ehlers S, Kutsch S, Ehlers EM, Benini J, Pfeffer K. Lethal granuloma disintegration in mycobacteria-infected TNFRp55-/-mice is dependent on T cells and IL-12. J Immunol 165(1): 483-492, 2000
16. Chávez-Galán L, Olleros ML, Vesin D, Garcia I. Much more than M1 and M2 macrophages, there are also CD169(+) and TCR(+) macrophages. Front Immunol 6: 263, 2015
17. Beutler B, Rietschel ET. Innate immune sensing and its roots: the story of endotoxin. Nat Rev Immunol 3(2): 169-176, 2003
18. Wicks IP, Roberts AW. Targeting GM-CSF in inflammatory diseases. Nat Rev Rheumatol 12(1): 37-48, 2016
19. Hao NB, LüMH, Fan YH, Cao YL, Zhang ZR, Yang SM. Macrophages in tumor microenvironments and the progression of tumors. Clin Dev Immunol 2012: 948098, 2012
20. 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 23(11): 549-555, 2002
21. Gordon S. Alternative activation of macrophages. Nat Rev Immunol 3(1): 23-35, 2003
22. Auphan N, DiDonato JA, Rosette C, Helmberg A, Karin M. Immunosuppression by glucocorticoids: inhibition of NF-kappa B activity through induction of I kappa B synthesis. Science 270(5234): 286-290, 1995
23. Herrlich P. Cross-talk between glucocorticoid receptor and AP-1. Oncogene 20(19): 2465-2475, 2001
24. Bhattacharyya S, Brown DE, Brewer JA, Vogt SK, Muglia LJ. Macrophage glucocorticoid receptors regulate Toll-like receptor 4-mediated inflammatory responses by selective inhibition of p38 MAP kinase. Blood 109(10): 4313-4319, 2007
25. Liden J, Rafter I, Truss M, Gustafsson JA, Okret S. Glucocorticoid effects on NF-kappaB binding in the transcription of the ICAM-1 gene. Biochem Biophys Res Commun 273(3): 1008-1014, 2000
26. Penton-Rol G, Cota M, Polentarutti N, Luini W, Bernasconi S, Borsatti A, Sica A, LaRosa GJ, Sozzani S, Poli G, et al. Up-regulation of CCR2 chemokine receptor expression and increased susceptibility to the multitropic HIV strain 89.6 in monocytes exposed to glucocorticoid hormones. J Immunol 163(6): 3524-3529, 1999
27. Wang Q, Ni H, Lan L, Wei X, Xiang R, Wang Y. Fra-1 protooncogene regulates IL-6 expression in macrophages and promotes the generation of M2d macrophages. Cell Res 20(6): 701-712, 2010
28. Duluc D, Delneste Y, Tan F, Moles MP, Grimaud L, Lenoir J, Preisser L, Anegon I, Catala L, Ifrah N, et al. Tumor-associated leukemia inhibitory factor and IL-6 skew monocyte differentiation into tumor-associated macrophage-like cells. Blood 110(13): 4319-4330, 2007
29. Chanmee T, Ontong P, Konno K, Itano N. Tumor-associated macrophages as major players in the tumor microenvironment. Cancers 6(3): 1670-1690, 2014
30. Jaguin M, Houlbert N, Fardel O, Lecureur V. Polarization profiles of human MCSF-generated macrophages and comparison of M1-markers in classically activated macrophages from GM-CSF and M-CSF origin. Cell Immunol 281(1): 51-61, 2013
31. Hattermann K, Sebens S, Helm O, Schmitt AD, Mentlein R, Mehdorn HM, Held-Feindt J. Chemokine expression profile of freshly isolated human glioblastoma-associated macrophages/microglia. Oncol Rep 32(1): 270-276, 2014
32. Zhang Y, Zhang M, Zhong M, Suo Q, Lv K. Expression profiles of miRNAs in polarized macrophages. Int J Mol Med 31(4): 797-802, 2013
33. Cobos Jiménez V, Bradley EJ, Willemsen AM, van Kampen AH, Baas F, Kootstra NA. Next-generation sequencing of microRNAs uncovers expression signatures in polarized macrophages. Physiol Genomics 46(3): 91-103, 2014
34. Murray PJ, Allen JE, Biswas SK, Fisher EA, Gilroy DW, Goerdt S, Gordon S, Hamilton JA, Ivashkiv LB, Lawrence T, et al. Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity 41(1): 14-20, 2014
35. Davies LC, Taylor PR. Tissue-resident macrophages: then and now. Immunology 144(4): 541-548, 2015
36. Graff JW, Dickson AM, Clay G, McCaffrey AP, Wilson ME. Identifying functional microRNAs in macrophages with polarized phenotypes. J Biol Chem 287(26): 21816-21825, 2012
37. Lawrence T, Natoli G. Transcriptional regulation of macrophage polarization: enabling diversity with identity. Nat Rev Immunol 11(11): 750-761, 2011
38. Günthner R, Anders HJ. Interferon-regulatory factors determine macrophage phenotype polarization. Mediators Inflamm 2013: 731023, 2013
39. Wang N, Liang H, Zen K: Molecularmechanisms that influence the macrophage m1-m2 polarization balance. Front Immunol 5: 614, 2014
40. Sheedy FJ. Turning 21: induction of miR-21 as a key switch in the inflammatory response. Front Immunol 6: 19, 2015
41. Caescu CI, Guo X, Tesfa L, Bhagat TD, Verma A, Zheng D, Stanley ER. Colony stimulating factor-1 receptor signaling networks inhibit mouse macrophage inflammatory responses by induction of microRNA-21. Blood 125(8): e1-e13, 2015
42. Wang Z, Brandt S, Medeiros A, Wang S, Wu H, Dent A, Serezani CH. MicroRNA 21 s a homeostatic regulator of macrophage polarization and prevents prostaglandin E2-mediated M2 generation. PLoS One 10(2): e0115855, 2015
43. Lu TX, Munitz A, Rothenberg ME. MicroRNA-21 is up-regulated in allergic airway inflammation and regulates IL-12p35 expression. J Immunol 182(8): 4994-5002, 2009
44. Thulin P, Wei T, Werngren O, Cheung L, Fisher RM, Grandér D, Corcoran M, Ehrenborg E. MicroRNA-9 regulates the expression of peroxisome proliferatoractivated receptor (in human monocytes during the inflammatory response. Int J Mol Med 31(5): 1003-1010, 2013
45. Ying H, Kang Y, Zhang H, Zhao D, Xia J, Lu Z, Wang H, Xu F, Shi L. MiR-127 modulates macrophage polarization and promotes lung inflammation and injury by activating the JNK pathway. J Immunol 194(3): 1239-1251, 2015
46. O'Connell RM, Taganov KD, Boldin MP, Cheng G, Baltimore D. MicroRNA-155 is induced during the macrophage inflammatory response. Proc Natl Acad Sci USA 104(5): 1604-1609, 2007
47. Martinez-Nunez RT, Louafi F, 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 286(3): 1786-1794, 2011
48. Arranz A, Doxaki C, Vergadi E, Martinez de la Torre Y, Vaporidi K, Lagoudaki ED, Ieronymaki E, Androulidaki A, Venihaki M, Margioris AN, et al. Akt1 and Akt2 protein kinases differentially contribute to macrophage polarization. Proc Natl Acad Sci USA 109(24): 9517-9522, 2012
49. Xu F, Kang Y, Zhang H, Piao Z, Yin H, Diao R, Xia J, Shi L. Akt1-mediated regulation of macrophage polarization in a murine model of Staphylococcus aureus pulmonary infection. J Infect Dis 208(3): 528-538, 2013
50. Chaudhuri AA, So AY, Sinha N, Gibson WS, Taganov KD, O'Connell RM, Baltimore D. MicroRNA-125b potentiates macrophage activation. J Immunol 187(10): 5062-5068, 2011
51. Sun Y, Li Q, Gui H, Xu DP, Yang YL, Su DF, Liu X. MicroRNA-124 mediates the cholinergic anti-inflammatory action through inhibiting the production of pro-inflammatory cytokines. Cell Res 23(11): 1270-1283, 2013
52. Veremeyko T, Siddiqui S, Sotnikov I, Yung A, Ponomarev ED. IL-4/IL-13-dependent and independent expression of miR-124 and its contribution to M2 phenotype of monocytic cells in normal conditions and during allergic inflammation. PLoS One 8(12): e81774, 2013
53. Chen Q, Wang H, Liu Y, Song Y, Lai L, Han Q, Cao X, Wang Q. Inducible microRNA-223 down-regulation promotes TLR-triggered IL-6 and IL-1b production in macrophages by targeting STAT3. PLoS One 7(8): e42971, 2012
54. Haneklaus M, Gerlic M, O'Neill LA, Masters SL. miR-223: infection, inflammation and cancer. J Intern Med 274(3): 215-226, 2013
55. Jiang P, Liu R, Zheng Y, Liu X, Chang L, Xiong S, Chu Y. MiR-34a inhibits lipopolysaccharide-induced inflammatory response through targeting Notch1 in murine macrophages. Exp Cell Res 318(10): 1175-1184, 2012
56. Zhang W, Liu H, Liu W, Liu Y, Xu J. Polycomb-mediated loss of microRNA let-7c determines inflammatory macrophage polarization via PAK1-dependent NF-(B pathway. Cell Death Differ 22(2): 287-297, 2015
57. Banerjee S, Xie N, Cui H, Tan Z, Yang S, Icyuz M, Abraham E, Liu G. MicroRNA let-7c regulates macrophage polarization. J Immunol 190(12): 6542-6549, 2013
58. Liu F, Li Y, Jiang R, Nie C, Zeng Z, Zhao N, Huang C, Shao Q, Ding C, Qing C, et al. miR-132 inhibits lipopolysaccharide-induced inflammation in alveolar macrophages by the cholinergic anti-inflammatory pathway. Exp Lung Res 41(5): 261-269, 2015
59. Vergadi E, Vaporidi K, Theodorakis EE, Doxaki C, Lagoudaki E, Ieronymaki E, Alexaki VI, Helms M, Kondili E, Soennichsen B, et al. Akt2 deficiency protects from acute lung injury via alternative macrophage activation and miR-146a induction in mice. J Immunol 192(1): 394-406, 2014
60. Taganov KD, Boldin MP, Chang KJ, Baltimore D. NF-kappaB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc Natl Acad Sci USA 103(33): 12481-12486, 2006
61. Banerjee S, Cui H, Xie N, Tan Z, Yang S, Icyuz M, Thannickal VJ, Abraham E. Liu G. miR-125a-5p regulates differential activation of macrophages and inflammation. J Biol Chem 288(49): 35428-35436, 2013
62. Labonte AC, Tosello-Trampont A-C, Hahn YS. The role of macrophage polarization in infectious and inflammatory diseases. Mol Cells 37(4): 275-285, 2014
63. Bashir S, Sharma Y, Elahi A, Khan F. Macrophage polarization: the link between inflammation and related diseases. Inflamm Res 65(1): 1-11, 2016
64. Biswas SK, Chittezhath M, Shalova IN, Lim JY. Macrophage polarization and plasticity in health and disease. Immunol Res 53(1-3): 11-24, 2012
65. Liu YC, Zou XB, Chai YF, Yao YM. Macrophage polarization in inflammatory diseases. Int J Biol Sci 10(5): 520-529, 2014
66. Hawiger J, Veach RA, Zienkiewicz J. New paradigms in sepsis: from prevention to protection of failing microcirculation. J Thromb Haemost 13(10): 1743-1756, 2015
67. Mayr FB, Yende S, Angus DC. Epidemiology of severe sepsis. Virulence 5(1): 4-11, 2014
68. Martin GS. Sepsis, severe sepsis and septic shock: changes in incidence, pathogens and outcomes. Expert Rev Anti Infect Ther 10(6): 701-706, 2012
69. Melamed A, Sorvillo FJ. The burden of sepsis-associated mortality in the United States from 1999 to 2005: an analysis of multiple-cause-of-death data. Crit Care 13(1): R28, 2009
70. Gentile LF, Cuenca AG, Efron PA, Ang D, Bihorac A, McKinley BA, Moldawer LL, Moore FA. Persistent inflammation and immunosuppression: a common syndrome and new horizon for surgical intensive care. J Trauma Acute Care Surg 72(6): 1491-1501, 2012
71. Essandoh K, Fan GC. Role of extracellular and intracellular microRNAs in sepsis. Biochim Biophys Acta 1842(11): 2155-2162, 2014
72. Tsujimoto H, Ono S, Efron PA, Scumpia PO, Moldawer LL, Mochizuki H. Role of Toll-like receptors in the development of sepsis. Shock 29(3): 315-321, 2008
73. Cristofaro P, Opal SM. The Toll-like receptors and their role in septic shock. Expert Opin Ther Targets 7(5): 603-612, 2003
74. Savva A, Roger T. Targeting toll-like receptors: promising therapeutic strategies for the management of sepsis-associated pathology and infectious diseases. Front Immunol 4: 387, 2013
75. Weighardt H, Holzmann B. Role of Toll-like receptor responses for sepsis pathogenesis. Immunobiology 212(9-10): 715-722, 2007
76. Foley NM, Wang J, Redmond HP, Wang JH. Current knowledge and future directions of TLR and NOD signaling in sepsis. Mil Med Res 2: 1, 2015
77. Salomão R, Martins PS, Brunialti MK, Fernandes Mda L, Martos LS, Mendes ME, Gomes NE, Rigato O. TLR signaling pathway in patients with sepsis. Shock 30(suppl 1): 73-77, 2008
78. Wang JF, Yu ML, Yu G, Bian JJ, Deng XM, Wan XJ, Zhu KM. Serum miR-146a and miR-223 as potential new biomarkers for sepsis. Biochem Biophys Res Commun 394(1): 184-188, 2010
79. Gao M, Wang X, Zhang X, Ha T, Ma H, Liu L, Kalbfleisch JH, Gao X, Kao RL, Williams DL, et al. Attenuation of cardiac dysfunction in polymicrobial sepsis by MicroRNA-146a is mediated via targeting of IRAK1 and TRAF6 expression. J Immunol 195(2): 672-682, 2015
80. Benz F, Tacke F, Luedde M, Trautwein C, Luedde T, Koch A, Roderburg C. Circulating microRNA-223 serum levels do not predict sepsis or survival in patients with critical illness. Dis Markers 2015: 384208, 2015
81. Arner P, KulytéA. MicroRNA regulatory networks in human adipose tissue and obesity. Nat Rev Endocrinol 11(5): 276-288, 2015
82. Monteiro R, Azevedo I. Chronic inflammation in obesity and the metabolic syndrome. Mediators Inflamm 2010: 289645, 2010
83. Xu H, Barnes GT, Yang Q, Tan G, Yang D, Chou CJ, Sole J, Nichols A, Ross JS, Tartaglia LA, et al. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest 112(12): 1821-1830, 2003
84. Gregor MF, Hotamisligil GS. Inflammatory mechanisms in obesity. Annu Rev Immunol 29: 415-445, 2011
85. Nishimura S, Manabe I, Nagai R. Adipose tissue inflammation in obesity and metabolic syndrome. Discov Med 8(41): 55-60, 2009
86. Bastard JP, Maachi M, Lagathu C, Kim MJ, Caron M, Vidal H, Capeau J, Feve B. Recent advances in the relationship between obesity, inflammation, and insulin resistance. Eur Cytokine Netw 17(1): 4-12, 2006
87. Moore CS, Rao VT, Durafourt BA, Bedell BJ, Ludwin SK, Bar-Or A. Antel JP. miR-155 as a multiple sclerosis-relevant regulator of myeloid cell polarization. Ann Neurol 74(5): 709-720, 2013
88. Ponomarev ED, Veremeyko T, Barteneva N, Krichevsky AM, Weiner HL. MicroRNA-124 promotes microglia quiescence and suppresses EAE by deactivating macrophages via the C/EBP-a-PU.1 pathway. Nat Med 17(1): 64-70, 2011
89. Ying W, Tseng A, Chang RC, Morin A, Brehm T, Triff K, Nair V, Zhuang G, Song H, Kanameni S, et al. MicroRNA-223 is a crucial mediator of PPARgregulated alternative macrophage activation. J Clin Invest 125(11): 4149-4159, 2015
90. Zhuang G, Meng C, Guo X, Cheruku PS, Shi L, Xu H, Li H, Wang G, Evans AR, Safe S, et al. A novel regulator of macrophage activation: miR-223 in obesityassociated adipose tissue inflammation. Circulation 125(23): 2892-2903, 2012
91. Karunakaran D, Richards L, Geoffrion M, Barrette D, Gotfrit RJ, Harper ME, Rayner KJ. Therapeutic inhibition of miR-33 promotes fatty acid oxidation but does not ameliorate metabolic dysfunction in diet-induced obesity. Arterioscler Thromb Vasc Biol 35(12): 2536-2543, 2015
92. Yang Y, Yang L, Liang X, Zhu G. MicroRNA-155 promotes atherosclerosis inflammation via targeting SOCS1. Cell Physiol Biochem 36(4): 1371-1381, 2015
93. Yang J, Zhang Z, Chen C, Liu Y, Si Q, Chuang TH, Li N, Gomez-Cabrero A, Reisfeld RA, Xiang R, et al. MicroRNA-19a-3p inhibits breast cancer progression and metastasis by inducing macrophage polarization through downregulated expression of Fra-1 proto-oncogene. Oncogene 33(23): 3014-3023, 2014
94. Jang JY, Lee JK, Jeon YK, Kim CW. Exosome derived from epigallocatechin gallate treated breast cancer cells suppresses tumor growth by inhibiting tumorassociated macrophage infiltration and M2 polarization. BMC Cancer 13: 421, 2013
95. Cai X, Yin Y, Li N, Zhu D, Zhang J, Zhang CY, Zen K. Re-polarization of tumorassociated macrophages to pro-inflammatory M1 macrophages by microRNA-155. J Mol Cell Biol 4(5): 341-343, 2012
96. Yu F, Jia X, Du F, Wang J, Wang Y, Ai W. Fan D. miR-155-deficient bone marrow promotes tumor metastasis. Mol Cancer Res 11(8): 923-936, 2013
97. Squadrito ML, Pucci F, Magri L, Moi D, Gilfillan GD, Ranghetti A, Casazza A, Mazzone M, Lyle R, Naldini L. De Palma M. miR-511-3p modulates genetic programs of tumor-associated macrophages. Cell Rep 1(2): 141-154, 2012
98. Perske C, Lahat N, Sheffy Levin S, Bitterman H, Hemmerlein B, Rahat MA. Loss of inducible nitric oxide synthase expression in the mouse renal cell carcinoma cell line RENCA is mediated by microRNA miR-146a. Am J Pathol 177(4): 2046-2054, 2010