Advertisement

Skewed Signaling through the Receptor for Advanced Glycation End-Products Alters the Proinflammatory Profile of Tumor-Associated Macrophages

  • Armando Rojas
  • Paulina Araya
  • Jacqueline Romero
  • Fernando Delgado-López
  • Ileana Gonzalez
  • Carolina Añazco
  • Ramon Perez-Castro
Review
  • 38 Downloads

Abstract

Tumors are complex tissues composed of variable amounts of both non-cellular components (matrix proteins) and a multitude of stromal cell types, which are under an active cross-talk with tumor cells. Tumor-associated macrophages (TAMs) are the major leukocyte population among the tumor-infiltrating immune cells. Once they are infiltrated into tumor stroma they undergo a polarized activation, where the M1 and M2 phenotypes represent the two extreme of the polarization heterogeneity spectrum. It is known that TAMs acquire a specific phenotype (M2), oriented toward tumor growth, angiogenesis and immune-suppression. A growing body of evidences supports the presence of tuning mechanisms in order to skew or restraint the inflammatory response of TAMs and thus forces them to function as active tumor-promoting immune cells. The receptor of advanced glycation end-products (RAGE) is a member of the immunoglobulin protein family of cell surface molecules, being activated by several danger signals and thus signaling to promote the production of many pro-inflammatory molecules. Interestingly, this receptor is paradoxically expressed in both M1 and M2 macrophages phenotypes. This review addresses how RAGE signaling has been drifted away in M2 macrophages, and thus taking advantage of the abundance of RAGE ligands at tumor microenvironment, particularly HMGB1, to reinforce the supportive M2 macrophages strategy to support tumor growth.

Keywords

Receptor for advanced glycation end-products Tumor microenvironment Macrophage polarization Alarmins Tumor-associated macrophages 

Notes

Acknowledgments

This work was supported by grant 1130337 from Programa Fondecyt, Comisión Nacional de Ciencia y Teconología, Chile.

References

  1. 1.
    Blakwill F, Mantovani A (2001) Inflammation and cancer: back to Virchow? Lancet 237:539–545CrossRefGoogle Scholar
  2. 2.
    Mantovani A, Allavena P, Sica A, Balkwill F (2008) Cancer-related inflammation. Nature 454:436–444PubMedCrossRefGoogle Scholar
  3. 3.
    Rakoff-Nahoum S, Medzhitov R (2009) Toll-like receptors and cancer. Nat Rev Cancer 9:57–63PubMedCrossRefGoogle Scholar
  4. 4.
    H zur Hausen (2006) Infections causing human cancer. Wiley-VCH. 531 pGoogle Scholar
  5. 5.
    McNamara D, El-Omar E (2008) Helicobacter pylori infection and the pathogenesis of gastric cancer: a paradigm for host-bacterial interactions. Dig Liver Dis 40:504–509PubMedCrossRefGoogle Scholar
  6. 6.
    Mantovani A (2009) Inflaming matastasis. Nature 457:36–37PubMedCrossRefGoogle Scholar
  7. 7.
    Colotta F, Allavena P, Sica A et al (2009) Cancer-related inflammation, the seventh hallmark of cancer: links to genetic instability. Carcinogenesis 7:1073–1081CrossRefGoogle Scholar
  8. 8.
    Balkwill F, Mantovani A (2012) Cancer-related inflammation: common themes and therapeutic opportunities. Semin Cancer Biol 22:33–40PubMedCrossRefGoogle Scholar
  9. 9.
    Mantovani A, Garlanda C, Allavena P (2010) Molecular pathways and targets in cancer-related inflammation. Ann Med 42:161–170PubMedCrossRefGoogle Scholar
  10. 10.
    Sethi G, Sung B, Aggarwal BB (2008) Nuclear factor-kappaB activation: from bench to bedside. Exp Biol Med 233:21–31CrossRefGoogle Scholar
  11. 11.
    Kundu JK, Surh YJ (2008) Inflammation: gearing the journey to cancer. Mutat Res 659:15–30PubMedCrossRefGoogle Scholar
  12. 12.
    Garlanda C, Riva F, Polentarutti N et al (2004) Intestinal inflammation in mice deficient in Tir8, an inhibitory member of the IL-1 receptor family. Proc Natl Acad Sci U S A 101:3522–3526PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Yu H, Pardoll D, Jove R (2009) STATs in cancer inflammation and immunity: a leading role for STAT3. Nat Rev Cancer 9:798–809PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    Kortylewski M, Yu H (2008) Role of Stat3 in suppressing anti-tumor immunity. Curr Opin Immunol 20:228–233PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    Kortylewski M, Xin H, Kujawski M et al (2009) Regulation of the IL-23 and IL-12 balance by Stat3 signaling in the tumor microenvironment. Cancer Cell 15:114–123PubMedPubMedCentralCrossRefGoogle Scholar
  16. 16.
    Balkwill F (2009) Tumour necrosis factor and cancer. Nat Rev Cancer 9:361–371PubMedCrossRefGoogle Scholar
  17. 17.
    Charles KA, Kulbe H, Soper R et al (2009) The tumor-promoting actions of TNF-alpha involve TNFR1 and IL-17 in ovarian cancer in mice and humans. J Clin Invest 119:3011–3023PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Kulbe H, Thompson R, Wilson JL et al (2007) The inflammatory cytokine tumor necrosis factor-alpha generates an autocrine tumor-promoting network in epithelial ovarian cancer cells. Cancer Res 67:585–592PubMedPubMedCentralCrossRefGoogle Scholar
  19. 19.
    Naldini A, Filippi I, Miglietta D et al (2010) Interleukin-1beta regulates the migratory potential of MDAMB231 breast cancer cells through the hypoxia-inducible factor-1alpha. Eur J Cancer 46:3400–3408PubMedCrossRefGoogle Scholar
  20. 20.
    Dinarello CA (2006) The paradox of pro-inflammatory cytokines in cancer. Cancer Metastasis Rev 25:307–313PubMedCrossRefGoogle Scholar
  21. 21.
    Arguello F, Baggs RB, Graves BT et al (1992) Effect of IL-1 on experimental bone/bone-marrow metastases. Int J Cancer 52:802–807PubMedCrossRefGoogle Scholar
  22. 22.
    Chen CJ, Kono H, Golenbock D et al (2007) Identification of a key pathway required for the sterile inflammatory response triggered by dying cells. Nat Med 13:851–856PubMedCrossRefGoogle Scholar
  23. 23.
    Coffelt SB, Scandurro AB (2008) Tumors sound the alarmin(s). Cancer Res 68:6482–6485PubMedPubMedCentralCrossRefGoogle Scholar
  24. 24.
    Lin WW, Karin M (2007) A cytokine-mediated link between innate immunity, inflammation, and cancer. J Clin Invest 117:1175–1183PubMedPubMedCentralCrossRefGoogle Scholar
  25. 25.
    Naugler WE, Karin M (2008) The wolf in sheep’s clothing: the role of interleukin-6 in immunity, inflammation and cancer. Trends Mol Med 14:109–119PubMedCrossRefGoogle Scholar
  26. 26.
    Bollrath J, Phesse TJ, von Burstin VA et al (2009) gp130-mediated Stat3 activation in enterocytes regulates cell survival and cell-cycle progression during colitis-associated tumorigenesis. Cancer Cell 15:91–102PubMedCrossRefGoogle Scholar
  27. 27.
    Grivennikov S, Karin E, Terzic J et al (2009) IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer. Cancer Cell 15:103–113PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Allavena P, Germano G, Marchesi F et al (2011) Chemokines in cancer related inflammation. Exp Cell Res 17:664–673CrossRefGoogle Scholar
  29. 29.
    Lazennec G, Richmond A (2010) Chemokines and chemokine receptors: new insights into cancer-related inflammation. Trends Mol Med 16:133–144PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Chen G, Chen SM, Wang X et al (2012) Inhibition of chemokine (CXC motif) ligand 12/chemokine (CXC motif) receptor 4 axis (CXCL12/CXCR4)-mediated cell migration by targeting mammalian target of rapamycin (mTOR) pathway in human gastric carcinoma cells. J Biol Chem 287:12132–12141PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    Sun X, Cheng G, Hao M et al (2010) CXCL12 / CXCR4 / CXCR7 chemokine axis and cancer progression. Cancer Metastasis Rev 29:709–722PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Boldajipour B, Mahabaleshwar H, Kardash E et al (2008) Control of chemokine-guided cell migration by ligand sequestration. Cell 132:463–473PubMedCrossRefGoogle Scholar
  33. 33.
    Balkwill FR (2012) The chemockine system and cancer. J Pathol 226:148–157PubMedCrossRefGoogle Scholar
  34. 34.
    Whiteside TL (2008) The tumor microenvironment and its role in promoting tumor growth. Oncogene 27:5904–5912PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Mbeunkui F, Johann DJ Jr (2009) Cancer and the tumor microenvironment: a review of an essential relationship. Cancer Chemother Pharmacol 63:571–582PubMedCrossRefGoogle Scholar
  36. 36.
    Sautès-Fridman C, Cherfils-Vicini J, Damotte D et al (2011) Tumor microenvironment is multifaceted. Cancer Metastasis Rev 30:13–25PubMedCrossRefGoogle Scholar
  37. 37.
    Solinas G, Germano G, Mantovani A et al (2009) Tumor -associated macrophages (TAM) as major players of the cancer-related inflammation. J Leukoc Biol 86:1065–1073PubMedCrossRefGoogle Scholar
  38. 38.
    Solinas G, Marchesi F, Garlanda C et al (2010) Inflammation-mediated promotion of invasion and metastasis. Cancer Metastasis Rev 29:243–248PubMedCrossRefGoogle Scholar
  39. 39.
    Sica A (2010) Role of tumor-associated macrophages in cancer-related inflammation. Exp Oncol 32:153–158PubMedGoogle Scholar
  40. 40.
    Galon J, Costes A, Sanchez-Cabo F et al (2006) Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 313:1960–1964PubMedCrossRefGoogle Scholar
  41. 41.
    Taylor RC, Patel A, Panageas KS et al (2007) Tumor-infiltrating lymphocytes predict sentinel lymph node positivity in patients with cutaneous melanoma. J Clin Oncol 25:869–875PubMedCrossRefGoogle Scholar
  42. 42.
    Qian B, Deng Y, Im JH et al (2009) A distinct macrophage population mediates metastatic breast cancer cell extravasation, establishment and growth. PLoS One 4:e6562PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Chen J, Yao Y, Gong C et al (2011) CCL18 from tumor-associated macrophages promotes breast cancer metastasis via PITPNM3. Cancer Cell 19:541–555PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Kurahara H, Shinchi H, Mataki Y et al (2011) Significance of M2-polarized tumor-associated macrophage in pancreatic cancer. J Surg Res 167:e211–e219PubMedCrossRefGoogle Scholar
  45. 45.
    Das A, Sinha M, Datta S et al (2015) Monocyte and macrophage plasticity in tissue repair and regeneration. Am J Pathol 185:2596–2606PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Locati M, Mantovani A, Sica A (2013) Macrophage activation and polarization as an adaptive component of innate immunity. Adv Immunol 120:163–184PubMedCrossRefGoogle Scholar
  47. 47.
    Giorgio S (2013) Macrophages: plastic solutions to environmental heterogeneity. Inflamm Res 62:835–843PubMedCrossRefGoogle Scholar
  48. 48.
    Gordon S, Martinez F (2010) Alternative activation of macrophages: mechanism and functions. Immunity 32:593–604PubMedCrossRefGoogle Scholar
  49. 49.
    Jetten N, Verbruggen S (2014) Anti-inflammatory M2, but not pro-inflammatory M1 macrophages promote angiogenesis in vivo. Angiogenesis 1:109–118CrossRefGoogle Scholar
  50. 50.
    Mantovani A, Sozzani S, Locati M et al (2002) Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol 23:549–555PubMedCrossRefGoogle Scholar
  51. 51.
    Sica A, Bronte V (2007) Altered macrophage differentiation and immune dysfunction in tumor development. J Clin Invest 117:1155–1166PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Porta C, Rimoldi M, Raes G et al (2009) Tolerance and M2 (alternative) macrophage polarization are related processes orchestrated by p50 nuclear factor kappaB. Proc Natl Acad Sci U S A 106:14978–14983PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Fujimoto M, Naka T (2003) Regulation of cytokine signaling by SOCS family molecules. Trends Immunol 24:659–666PubMedCrossRefGoogle Scholar
  54. 54.
    Yoshimura A, Naka T, Kubo M (2007) SOCS proteins, cytokine signalling and immune regulation. Nat Rev Immunol 7:454–465PubMedCrossRefGoogle Scholar
  55. 55.
    Liu Y, Stewart KN, Bishop E et al (2008) Unique expression of suppressor of cytokine signaling 3 is essential for classical macrophage activation in rodents in vitro and in vivo. J Immunol 180:6270–6278PubMedCrossRefGoogle Scholar
  56. 56.
    Whyte CS, Bishop ET, Rückerl D et al (2011) Suppressor of cytokine signaling (SOCS)1 is a key determinant of differential macrophage activation and function. J Leukoc Biol 90:845–854PubMedCrossRefGoogle Scholar
  57. 57.
    Ozato K, Tailor P, Kubota T (2007) The interferon regulatory factor family in host defense: mechanism of action. J Biol Chem 282:20065–20069PubMedCrossRefGoogle Scholar
  58. 58.
    Krausgruber T, Blazek K, Smallie T et al (2011) IRF5 promotes inflammatory macrophage polarization and TH1-TH17 responses. Nat Immunol 12:231–238PubMedCrossRefGoogle Scholar
  59. 59.
    Satoh T, Takeuchi O, Vandenbon A et al (2010) The Jmjd3-Irf4 axis regulates M2 macrophage polarization and host responses against helminth infection. Nat Immunol 11:936–944PubMedCrossRefGoogle Scholar
  60. 60.
    Capece D, Fischietti M, Verzella D et al (2013) The inflammatory microenvironment in hepatocellular carcinoma: a pivotal role for tumor-associated macrophages. Biomed Res Int 2013:187204PubMedCrossRefGoogle Scholar
  61. 61.
    Yuan F, Fu X, Shi H et al (2014) Induction of murine macrophage M2 polarization by cigarette smoke extract via the JAK2/STAT3 pathway. PLoS One 8(9):e107063CrossRefGoogle Scholar
  62. 62.
    González I, Romero J, Rodríguez BL et al (2013) The immunobiology of the receptor of advanced glycation end-products: trends and challenges. Immunobiology 218:790–797PubMedCrossRefGoogle Scholar
  63. 63.
    Rojas A, Pérez-Castro R, González I et al (2014) The emerging role of the receptor for advanced glycation end products on innate immunity. Int Rev Immunol 33:67–80PubMedCrossRefGoogle Scholar
  64. 64.
    Raucci A, Cugusi S, Antonelli A et al (2008) A soluble form of the receptor for advanced glycation endproducts (RAGE) is produced by proteolytic cleavage of the membrane-bound form by the sheddase a disintegrin and metalloprotease 10 (ADAM10). FASEB J 22:3716–3727PubMedCrossRefGoogle Scholar
  65. 65.
    Zhang L, Bukulin M, Kojro E et al (2008) Receptor for advanced glycation end products is subjected to protein ectodomain shedding by metalloproteinases. J Biol Chem 283:35507–35516PubMedCrossRefGoogle Scholar
  66. 66.
    Santilli F, Vazzana N, Bucciarelli LG et al (2009) Soluble forms of RAGE in human diseases: clinical and therapeutical implications. Curr Med Chem 16:940–952PubMedCrossRefGoogle Scholar
  67. 67.
    Kislinger T, Fu C, Huber B et al (1999) N(epsilon)-(carboxymethyl)lysine adducts of proteins are ligands for receptor for advanced glycation end products that activate cell signaling pathways and modulate gene expression. J Biol Chem 274:31740–31749PubMedCrossRefGoogle Scholar
  68. 68.
    Cho SJ, Roman G, Yeboah F et al (2007) The road to advanced glycation end products: a mechanistic perspective. Curr Med Chem 14:1653–1671PubMedCrossRefGoogle Scholar
  69. 69.
    van Heijst JW, Niessen HW, Hoekman K et al (2005) Advanced glycation end products in human cancer tissues: detection of N-epsilon-(carboxymethyl)lysine and argpyrimidine. Ann N Y Acad Sci 1043:725–733PubMedCrossRefGoogle Scholar
  70. 70.
    Marenholz I, Heizmann CW, Fritz G (2004) S100 proteins in mouse and man: from evolution to function and pathology (including an update of the nomenclature). Biochem Biophys Res Commun 322:1111–1122PubMedCrossRefGoogle Scholar
  71. 71.
    Lotze MT, Tracey KJ (2005) High mobility group box-1 protein (HMGB1): nuclear weapon in damage-associated molecular pattern the immune arsenal. Nat Rev Immunol 5:331–342PubMedCrossRefGoogle Scholar
  72. 72.
    Salama I, Malone PS, Mihaimeed F et al (2008) A review of the S100 proteins in cancer. Eur J Surg Oncol 34:357–364PubMedCrossRefGoogle Scholar
  73. 73.
    Campana L, Bosurgi L, Rovere-Querini P (2008) HMGB1: a two-headed signal regulating tumor progression and immunity. Curr Opin Immunol 20:518–523PubMedCrossRefGoogle Scholar
  74. 74.
    van Beijnum JR, Buurman WA, Griffioen AW (2008) Convergence and amplification of toll-like receptor (TLR) and receptor for advanced glycation end products (RAGE) signaling pathways via high mobility group B1 (HMGB1). Angiogenesis 11:91–99PubMedCrossRefGoogle Scholar
  75. 75.
    Sakaguchi M, Murata H, Yamamoto K et al (2011) TIRAP, an adaptor protein for TLR2/4, transduces a signal from RAGE phosphorylated upon ligand binding. PLoS One 6:e23132PubMedPubMedCentralCrossRefGoogle Scholar
  76. 76.
    Rojas A, Figueroa H, Morales E (2010) Fueling inflammation at tumor microenvironment: the role of multiligand/RAGE axis. Carcinogenesis 31:334–341PubMedCrossRefGoogle Scholar
  77. 77.
    Vlassara H, Brownlee M, Manogue KR et al (1988) Cachectin/TNF and IL-1 induced by glucose-modified proteins: role in normal tissue remodeling. Science 240:1546–1548PubMedCrossRefGoogle Scholar
  78. 78.
    Rojas A, Caveda L, Romay C et al (1996) Effect of advanced glycosylation end products on the induction of nitric oxide synthase in murine macrophages. Biochem Biophys Res Commun 225:358–362PubMedCrossRefGoogle Scholar
  79. 79.
    Wautier MP, Chappey O, Corda S et al (2001) Activation of NADPH oxidase by AGE links oxidant stress to altered gene expression via RAGE. Am J Physiol Endocrinol Metab 280:E685–E694PubMedCrossRefGoogle Scholar
  80. 80.
    Wu CH, Huang CM, Lin CH et al (2002) Advanced glycosylation end products induce NF-kappaB dependent iNOS expression in RAW 264.7 cells. Mol Cell Endocrinol 194:9–17PubMedCrossRefGoogle Scholar
  81. 81.
    Kokkola R, Andersson A, Mullins G et al (2005) RAGE is the major receptor for the proinflammatory activity of HMGB1 in rodent macrophages. Scand J Immunol 61:1–9PubMedCrossRefGoogle Scholar
  82. 82.
    Rashid G, Korzets Z, Bernheim J (2006) Advanced glycation end products stimulate tumor necrosis factor-alpha and interleukin-1 beta secretion by peritoneal macrophages in patients on continuous ambulatory peritoneal dialysis. Isr Med Assoc J 8:36–39PubMedGoogle Scholar
  83. 83.
    Hama S, Takeichi O, Saito I et al (2007) Involvement of inducible nitric oxide synthase and receptor for advanced glycation end products in periapical granulomas. J Endod 33:137–141PubMedCrossRefGoogle Scholar
  84. 84.
    Berbaum K, Shanmugam K, Stuchbury G et al (2008) Induction of novel cytokines and chemokines by advanced glycation end-products determined with a cytometric bead array. Cytokine 41:198–203PubMedCrossRefGoogle Scholar
  85. 85.
    Wang Y, Wang H, Piper MG et al (2010) sRAGE induces human monocyte survival and differentiation. J Immunol 185:1822–1835PubMedPubMedCentralCrossRefGoogle Scholar
  86. 86.
    Allavena P, Chieppa M, Bianchi G et al (2010) Engagement of the mannose receptor by tumoral mucins activates an immune suppressive phenotype in human tumor-associated macrophages. Clin Dev Immunol 54:71–79Google Scholar
  87. 87.
    Soria G, Ben-Baruch A (2008) The inflammatory chemokines CCL2 and CCL5 in breast cancer. Cancer Lett 267:271–285PubMedCrossRefGoogle Scholar
  88. 88.
    Zhang J, Patel L, Pienta KJ (2010) Targeting chemokine (C-C motif) ligand 2 (CCL2) as an example of translation of cancer molecular biology to the clinic. Prog Mol Biol Transl Sci 95:31–53PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    Hayakawa E, Yoshimoto T, Sekizawa N et al (2012) Overexpression of receptor for advanced glycation end-products induces monocyte chemoattractant protein-1 expression in rat vascular smooth muscle cell line. J Atheroscler Thromb 19:13–22PubMedCrossRefGoogle Scholar
  90. 90.
    Caillou B, Talbot M, Weyemi U et al (2011) Tumor-associated macrophages (TAMs) form an interconnected cellular supportive network in anaplastic thyroid carcinoma. PLoS One 6:e22567PubMedPubMedCentralCrossRefGoogle Scholar
  91. 91.
    Corzo CA, Cotter MJ, Cheng P et al (2009) Mechanism regulating reactive oxygen species in tumor-induced myeloid-derived suppressor cells. J Immunol 182:5693–5701PubMedPubMedCentralCrossRefGoogle Scholar
  92. 92.
    Yamaguchi H, Pixley F, Condeelis J (2006) Invadopodia and podosomes in tumor invasion. Eur J Cell Biol 85:213–218PubMedCrossRefGoogle Scholar
  93. 93.
    Domínguez PM, Ardavín C (2010) Differentiation and function of mouse monocyte-derived dendritic cells in steady state and inflammation. Immunol Rev 234:90–104PubMedCrossRefGoogle Scholar
  94. 94.
    Ivashkiv LB (2011) Inflammatory signaling in macrophages: transitions from acute to tolerant and alternative activation states. Eur J Immunol 41:2477–2481PubMedPubMedCentralCrossRefGoogle Scholar
  95. 95.
    Pena OM, Pistolic J, Raj D et al (2011) Endotoxin tolerance represents a distinctive state of alternative polarization (M2) in human mononuclear cells. J Immunol 186:7243–7254PubMedCrossRefGoogle Scholar
  96. 96.
    West MA, Heagy W (2002) Endotoxin tolerance: a review. Crit Care Med 30:S64–S73CrossRefPubMedGoogle Scholar
  97. 97.
    Foster SL, Medzhitov R (2009) Gene-specific control of the TLR-induced inflammatory response. Clin Immunol 130:7–15PubMedCrossRefGoogle Scholar
  98. 98.
    Chen J, Ivashkiv LB (2010) IFN-γ abrogates endotoxin tolerance by facilitating toll-like receptor-induced chromatin remodeling. Proc Natl Acad Sci U S A 107:19438–19443PubMedPubMedCentralCrossRefGoogle Scholar
  99. 99.
    Kouzarides T (2007) Chromatin modifications and their functions. Cell 128:693–705PubMedCrossRefGoogle Scholar
  100. 100.
    Mohtat D, Susztak K (2010) Fine tuning gene expression: the epigenome. Semin Nephrol 30:468–476PubMedPubMedCentralCrossRefGoogle Scholar
  101. 101.
    Ishii M, Wen H, Corsa CA et al (2009) Epigenetic regulation of the alternatively activated macrophage phenotype. Blood 114:3244–3254PubMedPubMedCentralCrossRefGoogle Scholar
  102. 102.
    Banerjee S, Halder K, Bose A et al (2011) TLR signaling-mediated differential histone modification at IL-10 and IL-12 promoter region leads to functional impairments in tumor-associated macrophages. Carcinogenesis 32:1789–1797PubMedCrossRefGoogle Scholar
  103. 103.
    Perrone L, Devi TS, Hosoya K et al (2009) Thioredoxin interacting protein (TXNIP) induces inflammation through chromatin modification in retinal capillary endothelial cells under diabetic conditions. J Cell Physiol 221:262–272PubMedCrossRefGoogle Scholar
  104. 104.
    Alam MM, O'Neill LA (2011) MicroRNAs and the resolution phase of inflammation in macrophages. Eur J Immunol 41:2482–2485PubMedCrossRefGoogle Scholar
  105. 105.
    He M, Xu Z, Ding T et al (2009) MicroRNA-155 regulates inflammatory cytokine production in tumor-associated macrophages via targeting C/EBPbeta. Cell Mol Immunol 6:343–352PubMedPubMedCentralCrossRefGoogle Scholar
  106. 106.
    Martinez-Nunez RT, Louafi F, Sanchez-Elsner T (2011) 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 286:1786–1794PubMedCrossRefGoogle Scholar
  107. 107.
    McCoy CE, Sheedy FJ, Qualls JE et al (2010) IL-10 inhibits miR-155 induction by toll-like receptors. J Biol Chem 285:20492–20498PubMedPubMedCentralCrossRefGoogle Scholar
  108. 108.
    Krausgruber T, Blazek K, Smallie T et al (2011) RF5 promotes inflammatory macrophage polarization and TH1-TH17 responses. Nat Immunol 12:231–238PubMedCrossRefGoogle Scholar
  109. 109.
    Quinn SR, O'Neill LA (2011) A trio of microRNAs that control toll-like receptor signalling. Int Immunol 23:421–425PubMedCrossRefGoogle Scholar
  110. 110.
    Perry MM, Moschos SA, Williams AE et al (2008) Rapid changes in microRNA-146a expression negatively regulate the IL-1beta-induced inflammatory response in human lung alveolar epithelial cells. J Immunol 15(180):5689–5698CrossRefGoogle Scholar
  111. 111.
    Bhaumik D, Scott GK, Schokrpur S et al (2009) MicroRNAs miR-146a/b negatively modulate the senescence-associated inflammatory mediators IL-6 and IL-8. Aging 1:402–411PubMedPubMedCentralCrossRefGoogle Scholar
  112. 112.
    Nahid MA, Pauley KM, Satoh M et al (2009) miR-146a is critical for endotoxin-induced tolerance: Implication in innate immunity. J Biol Chem 284:34590–34599PubMedPubMedCentralCrossRefGoogle Scholar
  113. 113.
    Sheedy FJ, Palsson-McDermott E, Hennessy EJ et al (2010) Negative regulation of TLR4 via targeting of the proinflammatory tumor suppressor PDCD4 by the microRNA miR-21. Nat Immunol 11:141–147PubMedCrossRefGoogle Scholar
  114. 114.
    Rojas A, Delgado-López F, Perez-Castro R et al (2016) HMGB1 enhances the protumoral activities of M2 macrophages by a RAGE-dependent mechanism. Tumour Biol 37(3):3321–3329PubMedCrossRefGoogle Scholar
  115. 115.
    Huber R, Meier B, Otsuka A et al (2016) Tumour hypoxia promotes melanoma growth and metastasis via High Mobility Group Box-1 and M2-like macrophages. Sci Report 18(6):29914.  https://doi.org/10.1038/srep29914 CrossRefGoogle Scholar
  116. 116.
    Rojas A, Araya P, Romero J, et al (2016) HMGB1-mediated RAGE activation mechanism in M2 macrophages. In: Proceedings of the 107th Annual Meeting of the American Association for Cancer Research; 2016 Apr 16-20; New Orleans, LA. Philadelphia (PA): AACR; Cancer Res. 76 (14 Suppl):Abstract nr 725Google Scholar
  117. 117.
    De Palma M, Lewis CE (2013) Macrophage regulation of tumor responses to anticancer therapies. Cancer Cell 23:277–286PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Biomedical Research Labs., Medicine FacultyCatholic University of MauleTalcaChile

Personalised recommendations