Table of Contents Author Guidelines Submit a Manuscript
Mediators of Inflammation
Volume 2015, Article ID 816460, 16 pages
http://dx.doi.org/10.1155/2015/816460
Review Article

Understanding the Mysterious M2 Macrophage through Activation Markers and Effector Mechanisms

Institute for Comparative Molecular Endocrinology, Center of Biomedical Research, University of Ulm, Helmholtzstrasse 8/1, 89081 Ulm, Germany

Received 12 February 2015; Accepted 30 April 2015

Academic Editor: Yona Keisari

Copyright © 2015 Tamás Rőszer. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. Z.-L. Chang, “Recent development of the mononuclear phagocyte system: in memory of Metchnikoff and Ehrlich on the 100th Anniversary of the 1908 Nobel Prize in Physiology or Medicine,” Biology of the Cell, vol. 101, no. 12, pp. 709–721, 2009. View at Publisher · View at Google Scholar · View at Scopus
  2. J. W. Pollard, “Trophic macrophages in development and disease,” Nature Reviews Immunology, vol. 9, no. 4, pp. 259–270, 2009. View at Publisher · View at Google Scholar · View at Scopus
  3. O. Osborn and J. M. Olefsky, “The cellular and signaling networks linking the immune system and metabolism in disease,” Nature Medicine, vol. 18, no. 3, pp. 363–374, 2012. View at Publisher · View at Google Scholar · View at Scopus
  4. F. O. Martinez and S. Gordon, “The M1 and M2 paradigm of macrophage activation: time for reassessment,” F1000Prime Reports, vol. 6, article 13, 2014. View at Publisher · View at Google Scholar · View at Scopus
  5. S. Colin, G. Chinetti-Gbaguidi, and B. Staels, “Macrophage phenotypes in atherosclerosis,” Immunological Reviews, vol. 262, no. 1, pp. 153–166, 2014. View at Publisher · View at Google Scholar
  6. S. J. Forbes and N. Rosenthal, “Preparing the ground for tissue regeneration: from mechanism to therapy,” Nature Medicine, vol. 20, pp. 857–869, 2014. View at Google Scholar
  7. S. Akira, T. Misawa, T. Satoh, and T. Saitoh, “Macrophages control innate inflammation,” Diabetes, Obesity and Metabolism, vol. 15, supplement 3, pp. 10–18, 2013. View at Publisher · View at Google Scholar · View at Scopus
  8. A. Sica and A. Mantovani, “Macrophage plasticity and polarization: in vivo veritas,” The Journal of Clinical Investigation, vol. 122, no. 3, pp. 787–795, 2012. View at Publisher · View at Google Scholar · View at Scopus
  9. M. L. Novak and T. J. Koh, “Macrophage phenotypes during tissue repair,” Journal of Leukocyte Biology, vol. 93, no. 6, pp. 875–881, 2013. View at Publisher · View at Google Scholar · View at Scopus
  10. P. J. Murray, J. E. Allen, S. K. Biswas et al., “Macrophage activation and polarization: nomenclature and experimental guidelines,” Immunity, vol. 41, no. 2, pp. 339–340, 2014. View at Publisher · View at Google Scholar
  11. M. Benoit, B. Desnues, and J.-L. Mege, “Macrophage polarization in bacterial infections,” The Journal of Immunology, vol. 181, no. 6, pp. 3733–3739, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. L. Fuentes, T. Röszer, and M. Ricote, “Inflammatory mediators and insulin resistance in obesity: role of nuclear receptor signaling in macrophages,” Mediators of Inflammation, vol. 2010, Article ID 219583, 10 pages, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. S. S. Bohlson, S. D. O'Conner, H. J. Hulsebus, M. M. Ho, and D. A. Fraser, “Complement, C1q, and C1q-related molecules regulate macrophage polarization,” Frontiers in Immunology, vol. 5, article 402, 2014. View at Publisher · View at Google Scholar
  14. C. J. Ferrante and S. J. Leibovich, “Regulation of macrophage polarization and wound healing,” Advances in Wound Care, vol. 1, no. 1, pp. 10–16, 2012. View at Publisher · View at Google Scholar
  15. D. L. Morris, K. Singer, and C. N. Lumeng, “Adipose tissue macrophages: phenotypic plasticity and diversity in lean and obese states,” Current Opinion in Clinical Nutrition and Metabolic Care, vol. 14, no. 4, pp. 341–346, 2011. View at Publisher · View at Google Scholar · View at Scopus
  16. E. Muraille, O. Leo, and M. Moser, “TH1/TH2 paradigm extended: macrophage polarization as an unappreciated pathogen-driven escape mechanism?” Frontiers in Immunology, vol. 5, article 603, 2014. View at Publisher · View at Google Scholar
  17. C. K. Glass and J. M. Olefsky, “Inflammation and lipid signaling in the etiology of insulin resistance,” Cell Metabolism, vol. 15, no. 5, pp. 635–645, 2012. View at Publisher · View at Google Scholar · View at Scopus
  18. E. D. Rosen and B. M. Spiegelman, “What we talk about when we talk about fat,” Cell, vol. 156, no. 1-2, pp. 20–44, 2014. View at Publisher · View at Google Scholar · View at Scopus
  19. E. Rigamonti, P. Zordan, C. Sciorati, P. Rovere-Querini, and S. Brunelli, “Macrophage plasticity in skeletal muscle repair,” BioMed Research International, vol. 2014, Article ID 560629, 9 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  20. A. Mantovani, S. Sozzani, M. Locati, P. Allavena, and A. Sica, “Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes,” Trends in Immunology, vol. 23, no. 11, pp. 549–555, 2002. View at Publisher · View at Google Scholar · View at Scopus
  21. Y. Yang, R. Zhang, F. Xia et al., “LPS converts Gr-1+CD115+ myeloid-derived suppressor cells from M2 to M1 via P38 MAPK,” Experimental Cell Research, vol. 319, no. 12, pp. 1774–1783, 2013. View at Publisher · View at Google Scholar · View at Scopus
  22. S. Bhatt, J. Qin, C. Bennett et al., “All-trans retinoic acid induces arginase-1 and inducible nitric oxide synthase-producing dendritic cells with T cell inhibitory function,” The Journal of Immunology, vol. 192, no. 11, pp. 5098–5108, 2014. View at Publisher · View at Google Scholar · View at Scopus
  23. G. Raes, P. de Baetselier, W. Noël, A. Beschin, F. Brombacher, and H. G. Gholamreza, “Differential expression of FIZZ1 and Ym1 in alternatively versus classically activated macrophages,” Journal of Leukocyte Biology, vol. 71, no. 4, pp. 597–602, 2002. View at Google Scholar · View at Scopus
  24. J. S. Welch, L. Escoubet-Lozach, D. B. Sykes, K. Liddiard, D. R. Greaves, and C. K. Glass, “TH2 cytokines and allergic challenge induce Ym1 expression in macrophages by a STAT6-dependent mechanism,” The Journal of Biological Chemistry, vol. 277, no. 45, pp. 42821–42829, 2002. View at Publisher · View at Google Scholar · View at Scopus
  25. Q. Wang, H. Ni, L. Lan, X. Wei, R. Xiang, and Y. Wang, “Fra-1 protooncogene regulates IL-6 expression in macrophages and promotes the generation of M2d macrophages,” Cell Research, vol. 20, no. 6, pp. 701–712, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. C. J. Ferrante, G. Pinhal-Enfield, G. Elson et al., “The adenosine-dependent angiogenic switch of macrophages to an M2-like phenotype is independent of interleukin-4 receptor alpha (IL-4Ralpha) signaling,” Inflammation, vol. 36, no. 4, pp. 921–931, 2013. View at Publisher · View at Google Scholar · View at Scopus
  27. F. Porcheray, S. Viaud, A.-C. Rimaniol et al., “Macrophage activation switching: an asset for the resolution of inflammation,” Clinical and Experimental Immunology, vol. 142, no. 3, pp. 481–489, 2005. View at Publisher · View at Google Scholar · View at Scopus
  28. T. Rőszer, “Phagosomal and lysosomal NO synthesis,” in The Biology of Subcellular Nitric Oxide, pp. 145–155, Springer, Dordrecht, The Netherlands, 2012. View at Publisher · View at Google Scholar
  29. T. Rőszer, “Peroxisomes: where NOS rests in peace?” in The Biology of Subcellular Nitric Oxide, chapter 11, pp. 179–185, Springer, Dordrecht, The Netherlands, 2012. View at Google Scholar
  30. A. D. Joshi, S. R. Oak, A. J. Hartigan et al., “Interleukin-33 contributes to both M1 and M2 chemokine marker expression in human macrophages,” BMC Immunology, vol. 11, article 52, 2010. View at Publisher · View at Google Scholar · View at Scopus
  31. Y. Tatano, T. Shimizu, and H. Tomioka, “Unique macrophages different from M1/M2 macrophages inhibit T cell mitogenesis while upregulating Th17 polarization,” Scientific Reports, vol. 4, article 4146, 2014. View at Publisher · View at Google Scholar
  32. C. C. Stempin, L. R. Dulgerian, V. V. Garrido, and F. M. Cerban, “Arginase in parasitic infections: macrophage activation, immunosuppression, and intracellular signals,” Journal of Biomedicine and Biotechnology, vol. 2010, Article ID 683485, 10 pages, 2010. View at Publisher · View at Google Scholar · View at Scopus
  33. J. M. Dzik, “Evolutionary roots of arginase expression and regulation,” Frontiers in Immunology, vol. 5, article 544, 2014. View at Publisher · View at Google Scholar
  34. U. Müller, W. Stenzel, G. Köhler et al., “IL-13 induces disease-promoting type 2 cytokines, alternatively activated macrophages and allergic inflammation during pulmonary infection of mice with Cryptococcus neoformans,” The Journal of Immunology, vol. 179, no. 8, pp. 5367–5377, 2007. View at Publisher · View at Google Scholar · View at Scopus
  35. M. Munder, “Arginase: an emerging key player in the mammalian immune system,” British Journal of Pharmacology, vol. 158, no. 3, pp. 638–651, 2009. View at Publisher · View at Google Scholar · View at Scopus
  36. M. Ahn, W. Yang, H. Kim, J.-K. Jin, C. Moon, and T. Shin, “Immunohistochemical study of arginase-1 in the spinal cords of Lewis rats with experimental autoimmune encephalomyelitis,” Brain Research, vol. 1453, pp. 77–86, 2012. View at Publisher · View at Google Scholar · View at Scopus
  37. B. Spittau, L. Wullkopf, X. Zhou, J. Rilka, D. Pfeifer, and K. Krieglstein, “Endogenous transforming growth factor-beta promotes quiescence of primary microglia in vitro,” Glia, vol. 61, no. 2, pp. 287–300, 2013. View at Publisher · View at Google Scholar · View at Scopus
  38. P. V. Ranganathan, C. Jayakumar, and G. Ramesh, “Netrin-1-treated macrophages protect the kidney against ischemia-reperfusion injury and suppress inflammation by inducing M2 polarization,” The American Journal of Physiology: Renal Physiology, vol. 304, no. 7, pp. F948–F957, 2013. View at Publisher · View at Google Scholar · View at Scopus
  39. B. Csóka, Z. Selmeczy, B. Koscsó et al., “Adenosine promotes alternative macrophage activation via A2Aand A2B receptors,” The FASEB Journal, vol. 26, no. 1, pp. 376–386, 2012. View at Publisher · View at Google Scholar · View at Scopus
  40. N. Kawanaka and A. W. Taylor, “Localized retinal neuropeptide regulation of macrophage and microglial cell functionality,” Journal of Neuroimmunology, vol. 232, no. 1-2, pp. 17–25, 2011. View at Publisher · View at Google Scholar · View at Scopus
  41. W. Chen, J. Liu, J. Meng et al., “Macrophage polarization induced by neuropeptide methionine enkephalin (MENK) promotes tumoricidal responses,” Cancer Immunology, Immunotherapy, vol. 61, no. 10, pp. 1755–1768, 2012. View at Publisher · View at Google Scholar · View at Scopus
  42. B. Hegyi, Z. Környei, S. Ferenczi et al., “Regulation of mouse microglia activation and effector functions by bone marrow-derived mesenchymal stem cells,” Stem Cells and Development, vol. 23, no. 21, pp. 2600–2612, 2014. View at Publisher · View at Google Scholar
  43. S. H. Jung, A. Saxena, K. Kaur et al., “The role of adipose tissue-associated macrophages and T lymphocytes in the pathogenesis of inflammatory bowel disease,” Cytokine, vol. 61, no. 2, pp. 459–468, 2013. View at Publisher · View at Google Scholar · View at Scopus
  44. M. Munder, H. Schneider, C. Luckner et al., “Suppression of T-cell functions by human granulocyte arginase,” Blood, vol. 108, no. 5, pp. 1627–1634, 2006. View at Publisher · View at Google Scholar · View at Scopus
  45. T. E. Cloke, L. Garvey, B.-S. Choi et al., “Increased level of arginase activity correlates with disease severity in HIV-seropositive patients,” Journal of Infectious Diseases, vol. 202, no. 3, pp. 374–385, 2010. View at Publisher · View at Google Scholar · View at Scopus
  46. W. Durante, F. K. Johnson, and R. A. Johnson, “Arginase: a critical regulator of nitric oxide synthesis and vascular function,” Clinical and Experimental Pharmacology and Physiology, vol. 34, no. 9, pp. 906–911, 2007. View at Publisher · View at Google Scholar · View at Scopus
  47. M. Munder, K. Eichmann, J. M. Morán, F. Centeno, G. Soler, and M. Modolell, “Th1/Th2-regulated expression of arginase isoforms in murine macrophages and dendritic cells,” Journal of Immunology, vol. 163, no. 7, pp. 3771–3777, 1999. View at Google Scholar · View at Scopus
  48. C. I. Chang, J. C. Liao, and L. Kuo, “Arginase modulates nitric oxide production in activated macrophages,” The American Journal of Physiology, vol. 274, no. 1, pp. H342–H348, 1998. View at Google Scholar · View at Scopus
  49. T. Rőszer, “Introduction,” in The Biology of Subcellular Nitric Oxide, chapter 1, pp. 3–16, Springer, Dordrecht, The Netherlands, 2012. View at Publisher · View at Google Scholar
  50. Y. Ji, S. Sun, S. Xia, L. Yang, X. Li, and L. Qi, “Short term high fat diet challenge promotes alternative macrophage polarization in adipose tissue via natural killer T cells and interleukin-4,” The Journal of Biological Chemistry, vol. 287, no. 29, pp. 24378–24386, 2012. View at Publisher · View at Google Scholar · View at Scopus
  51. R. C. Benson, K. A. Hardy, and C. R. Morris, “Arginase and arginine dysregulation in asthma,” Journal of Allergy (Cairo), vol. 2011, Article ID 736319, 12 pages, 2011. View at Publisher · View at Google Scholar
  52. L. Xu, B. Hilliard, R. J. Carmody et al., “Arginase and autoimmune inflammation in the central nervous system,” Immunology, vol. 110, no. 1, pp. 141–148, 2003. View at Publisher · View at Google Scholar · View at Scopus
  53. W. Zhang, B. Baban, M. Rojas et al., “Arginase activity mediates retinal inflammation in endotoxin-induced uveitis,” The American Journal of Pathology, vol. 175, no. 2, pp. 891–902, 2009. View at Publisher · View at Google Scholar · View at Scopus
  54. S. L. Kavalukas, A. R. Uzgare, T. J. Bivalacqua, and A. Barbul, “Arginase inhibition promotes wound healing in mice,” Surgery, vol. 151, no. 2, pp. 287–295, 2012. View at Publisher · View at Google Scholar · View at Scopus
  55. M. G. Nair, K. J. Guild, and D. Artis, “Novel effector molecules in type 2 inflammation: lessons drawn from helminth infection and allergy,” Journal of Immunology, vol. 177, no. 3, pp. 1393–1399, 2006. View at Publisher · View at Google Scholar · View at Scopus
  56. C. A. Colton, R. T. Mott, H. Sharpe, Q. Xu, W. E. Van Nostrand, and M. P. Vitek, “Expression profiles for macrophage alternative activation genes in AD and in mouse models of AD,” Journal of Neuroinflammation, vol. 3, article 27, 2006. View at Publisher · View at Google Scholar · View at Scopus
  57. J. Nio, W. Fujimoto, A. Konno, Y. Kon, M. Owhashi, and T. Iwanaga, “Cellular expression of murine Ym1 and Ym2, chitinase family proteins, as revealed by in situ hybridization and immunohistochemistry,” Histochemistry and Cell Biology, vol. 121, no. 6, pp. 473–482, 2004. View at Google Scholar · View at Scopus
  58. J. M. Ward, M. Yoon, M. R. Anver et al., “Hyalinosis and Ym1/Ym2 gene expression in the stomach and respiratory tract of 129S4/SvJae and wild-type and CYP1A2-null B6, 129 mice,” American Journal of Pathology, vol. 158, no. 1, pp. 323–332, 2001. View at Publisher · View at Google Scholar · View at Scopus
  59. M. Harbord, M. Novelli, B. Canas et al., “Ym1 is a neutrophil granule protein that crystallizes in p47phox-deficient mice,” Journal of Biological Chemistry, vol. 277, no. 7, pp. 5468–5475, 2002. View at Publisher · View at Google Scholar · View at Scopus
  60. J. Zhao, Z. Lv, F. Wang et al., “Ym1, an eosinophilic chemotactic factor, participates in the brain inflammation induced by Angiostrongylus cantonensis in mice,” Parasitology Research, vol. 112, no. 7, pp. 2689–2695, 2013. View at Publisher · View at Google Scholar · View at Scopus
  61. I. Waern, J. Jia, G. Pejler et al., “Accumulation of Ym1 and formation of intracellular crystalline bodies in alveolar macrophages lacking heparanase,” Molecular Immunology, vol. 47, no. 7-8, pp. 1467–1475, 2010. View at Publisher · View at Google Scholar · View at Scopus
  62. N.-C. A. Chang, S.-I. Hung, K.-Y. Hwa et al., “A macrophage protein, Ym1, transiently expressed during inflammation is a novel mammalian lectin,” The Journal of Biological Chemistry, vol. 276, no. 20, pp. 17497–17506, 2001. View at Publisher · View at Google Scholar · View at Scopus
  63. L. Guo, R. S. Johnson, and J. C. L. Schuh, “Biochemical characterization of endogenously formed eosinophilic crystals in the lungs of mice,” The Journal of Biological Chemistry, vol. 275, no. 11, pp. 8032–8037, 2000. View at Publisher · View at Google Scholar · View at Scopus
  64. S.-I. Hung, A. C. Chang, I. Kato, and N.-C. A. Chang, “Transient expression of Ym1, a heparin-binding lectin, during developmental hematopoiesis and inflammation,” Journal of Leukocyte Biology, vol. 72, no. 1, pp. 72–82, 2002. View at Google Scholar · View at Scopus
  65. G. Raes, R. Van Den Bergh, P. De Baetselier et al., “Arginase-1 and Ym1 are markers for murine, but not human, alternatively activated myeloid cells,” The Journal of Immunology, vol. 174, no. 11, pp. 6561–6562, 2005. View at Publisher · View at Google Scholar · View at Scopus
  66. H. Ling and A. D. Recklies, “The chitinase 3-like protein human cartilage glycoprotein 39 inhibits cellular responses to the inflammatory cytokines interleukin-1 and tumour necrosis factor-alpha,” Biochemical Journal, vol. 380, no. 3, pp. 651–659, 2004. View at Publisher · View at Google Scholar · View at Scopus
  67. S. Arora, Y. Hernandez, J. R. Erb-Downward, R. A. McDonald, G. B. Toews, and G. B. Huffnagle, “Role of IFN-gamma in regulating T2 immunity and the development of alternatively activated macrophages during allergic bronchopulmonary mycosis,” Journal of Immunology, vol. 174, no. 10, pp. 6346–6356, 2005. View at Publisher · View at Google Scholar · View at Scopus
  68. P. L. Gordts, E. M. Foley, R. Lawrence et al., “Reducing macrophage proteoglycan sulfation increases atherosclerosis and obesity through enhanced type I interferon signaling,” Cell Metabolism, vol. 20, no. 5, pp. 813–826, 2014. View at Publisher · View at Google Scholar
  69. E. Hermano, A. Meirovitz, K. Meir et al., “Macrophage polarization in pancreatic carcinoma: role of heparanase enzyme,” Journal of the National Cancer Institute, vol. 106, no. 12, pp. dju332–dju332, 2014. View at Publisher · View at Google Scholar
  70. T. E. Sutherland, N. Logan, D. Rückerl et al., “Chitinase-like proteins promote IL-17-mediated neutrophilia in a tradeoff between nematode killing and host damage,” Nature Immunology, vol. 15, no. 12, pp. 1116–1125, 2014. View at Publisher · View at Google Scholar
  71. K. J. Greenlee, D. B. Corry, D. A. Engler et al., “Proteomic identification of in vivo substrates for matrix metalloproteinases 2 and 9 reveals a mechanism for resolution of inflammation,” The Journal of Immunology, vol. 177, no. 10, pp. 7312–7321, 2006. View at Publisher · View at Google Scholar · View at Scopus
  72. M. Arora, L. Chen, M. Paglia et al., “Simvastatin promotes Th2-type responses through the induction of the chitinase family member Ym1 in dendritic cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 20, pp. 7777–7782, 2006. View at Publisher · View at Google Scholar · View at Scopus
  73. L. C. Osborne, L. A. Monticelli, T. J. Nice et al., “Virus-helminth coinfection reveals a microbiota-independent mechanism of immunomodulation,” Science, vol. 345, no. 6196, pp. 578–582, 2014. View at Publisher · View at Google Scholar
  74. I. Goren, J. Pfeilschifter, and S. Frank, “Uptake of neutrophil-derived Ym1 protein distinguishes wound macrophages in the absence of interleukin-4 signaling in murine wound healing,” The American Journal of Pathology, vol. 184, no. 12, pp. 3249–3261, 2014. View at Publisher · View at Google Scholar
  75. M. Zeyda, D. Farmer, J. Todoric et al., “Human adipose tissue macrophages are of an anti-inflammatory phenotype but capable of excessive pro-inflammatory mediator production,” International Journal of Obesity, vol. 31, no. 9, pp. 1420–1428, 2007. View at Publisher · View at Google Scholar · View at Scopus
  76. J. Aron-Wisnewsky, J. Tordjman, C. Poitou et al., “Human adipose tissue macrophages: M1 and M2 cell surface markers in subcutaneous and omental depots and after weight loss,” Journal of Clinical Endocrinology and Metabolism, vol. 94, no. 11, pp. 4619–4623, 2009. View at Publisher · View at Google Scholar · View at Scopus
  77. J. Haase, U. Weyer, K. Immig et al., “Local proliferation of macrophages in adipose tissue during obesity-induced inflammation,” Diabetologia, vol. 57, no. 3, pp. 562–571, 2014. View at Publisher · View at Google Scholar · View at Scopus
  78. E. Titos, B. Rius, A. González-Périz et al., “Resolvin D1 and its precursor docosahexaenoic acid promote resolution of adipose tissue inflammation by eliciting macrophage polarization toward an M2-like phenotype,” Journal of Immunology, vol. 187, no. 10, pp. 5408–5418, 2011. View at Publisher · View at Google Scholar · View at Scopus
  79. J. Svensson-Arvelund, R. B. Mehta, R. Lindau et al., “The human fetal placenta promotes tolerance against the semiallogeneic fetus by inducing regulatory T cells and homeostatic M2 macrophages,” The Journal of Immunology, vol. 194, no. 4, pp. 1534–1544, 2015. View at Publisher · View at Google Scholar
  80. M. Dupasquier, P. Stoitzner, H. Wan et al., “The dermal microenvironment induces the expression of the alternative activation marker CD301/mMGL in mononuclear phagocytes, independent of IL-4/IL-13 signaling,” Journal of Leukocyte Biology, vol. 80, no. 4, pp. 838–849, 2006. View at Publisher · View at Google Scholar · View at Scopus
  81. K. Kambara, W. Ohashi, K. Tomita et al., “In vivo depletion of CD206+ M2 macrophages exaggerates lung Injury in endotoxemic mice,” The American Journal of Pathology, vol. 185, no. 1, pp. 162–171, 2015. View at Publisher · View at Google Scholar
  82. S. J. Lee, S. Evers, D. Roeder et al., “Mannose receptor-mediated regulation of serum glycoprotein homeostasis,” Science, vol. 295, no. 5561, pp. 1898–1901, 2002. View at Publisher · View at Google Scholar · View at Scopus
  83. T. Bellón, V. Martínez, B. Lucendo et al., “Alternative activation of macrophages in human peritoneum: implications for peritoneal fibrosis,” Nephrology Dialysis Transplantation, vol. 26, no. 9, pp. 2995–3005, 2011. View at Publisher · View at Google Scholar · View at Scopus
  84. H. J. Medbury, V. James, J. Ngo et al., “Differing association of macrophage subsets with atherosclerotic plaque stability,” International Angiology, vol. 32, no. 1, pp. 74–84, 2013. View at Google Scholar · View at Scopus
  85. A. Rivollier, J. He, A. Kole, V. Valatas, and B. L. Kelsall, “Inflammation switches the differentiation program of Ly6chi monocytes from antiinflammatory macrophages to inflammatory dendritic cells in the colon,” The Journal of Experimental Medicine, vol. 209, no. 1, pp. 139–155, 2012. View at Publisher · View at Google Scholar · View at Scopus
  86. Z. Tang, T. Niven-Fairchild, S. Tadesse et al., “Glucocorticoids enhance CD163 expression in placental Hofbauer cells,” Endocrinology, vol. 154, no. 1, pp. 471–482, 2013. View at Publisher · View at Google Scholar · View at Scopus
  87. M. E. Shaul, G. Bennett, K. J. Strissel, A. S. Greenberg, and M. S. Obin, “Dynamic, M2-like remodeling phenotypes of CD11c+ adipose tissue macrophages during high-fat diet —induced obesity in mice,” Diabetes, vol. 59, no. 5, pp. 1171–1181, 2010. View at Publisher · View at Google Scholar · View at Scopus
  88. J. Svensson, M. C. Jenmalm, A. Matussek, R. Geffers, G. Berg, and J. Ernerudh, “Macrophages at the fetal-maternal interface express markers of alternative activation and are induced by M-CSF and IL-10,” Journal of Immunology, vol. 187, no. 7, pp. 3671–3682, 2011. View at Publisher · View at Google Scholar · View at Scopus
  89. M. Ritter, C. Buechler, T. Langmann, E. Orso, J. Klucken, and G. Schmitz, “The scavenger receptor CD163: regulation, promoter structure and genomic organization,” Pathobiology, vol. 67, no. 5-6, pp. 257–261, 2000. View at Google Scholar · View at Scopus
  90. M. M. van den Heuvel, C. P. Tensen, J. H. van As et al., “Regulation of CD163 on human macrophages: cross-linking of CD163 induces signaling and activation,” Journal of Leukocyte Biology, vol. 66, no. 5, pp. 858–866, 1999. View at Google Scholar · View at Scopus
  91. T. H. Sulahian, P. Högger, A. E. Wahner et al., “Human monocytes express CD163, which is upregulated by IL-10 and identical to p155,” Cytokine, vol. 12, no. 9, pp. 1312–1321, 2000. View at Publisher · View at Google Scholar · View at Scopus
  92. G. Zizzo, B. A. Hilliard, M. Monestier, and P. L. Cohen, “Efficient clearance of early apoptotic cells by human macrophages requires M2c polarization and MerTK induction,” Journal of Immunology, vol. 189, no. 7, pp. 3508–3520, 2012. View at Publisher · View at Google Scholar · View at Scopus
  93. Y. Komohara, K. Ohnishi, J. Kuratsu, and M. Takeya, “Possible involvement of the M2 anti-inflammatory macrophage phenotype in growth of human gliomas,” Journal of Pathology, vol. 216, no. 1, pp. 15–24, 2008. View at Publisher · View at Google Scholar · View at Scopus
  94. C. Buechler, K. Eisinger, and S. Krautbauer, “Diagnostic and prognostic potential of the macrophage specific receptor CD163 in inflammatory diseases,” Inflammation and Allergy—Drug Targets, vol. 12, no. 6, pp. 391–402, 2013. View at Publisher · View at Google Scholar · View at Scopus
  95. M. H. M. Barros, F. Hauck, J. H. Dreyer, B. Kempkes, and G. Niedobitek, “Macrophage polarisation: an immunohistochemical approach for identifying M1 and M2 macrophages,” PLoS ONE, vol. 8, no. 11, Article ID e80908, 2013. View at Publisher · View at Google Scholar · View at Scopus
  96. A. M. Stütz, L. A. Pickart, A. Trifilieff, T. Baumruker, and E. Prieschl-Strassmayr, “The Th2 cell cytokines IL-4 and IL-13 regulate found in inflammatory zone 1/resistin-like molecule α gene expression by a STAT6 and CCAAT/enhancer-binding protein-dependent mechanism,” Journal of Immunology, vol. 170, no. 4, pp. 1789–1796, 2003. View at Publisher · View at Google Scholar · View at Scopus
  97. J. T. Pesce, T. R. Ramalingam, M. S. Wilson et al., “Retnla (relmalpha/Fizz1) suppresses helminth-induced Th2- type immunity,” PLoS Pathogens, vol. 5, no. 4, Article ID e1000393, 2009. View at Publisher · View at Google Scholar · View at Scopus
  98. M. G. Nair, Y. Du, J. G. Perrigoue et al., “Alternatively activated macrophage-derived RELM-α is a negative regulator of type 2 inflammation in the lung,” Journal of Experimental Medicine, vol. 206, no. 4, pp. 937–952, 2009. View at Publisher · View at Google Scholar · View at Scopus
  99. T. Liu, H. Jin, M. Ullenbruch et al., “Regulation of found in inflammatory zone 1 expression in bleomycin-induced lung fibrosis: role of IL-4/IL-13 and mediation via STAT-6,” The Journal of Immunology, vol. 173, no. 5, pp. 3425–3431, 2004. View at Publisher · View at Google Scholar · View at Scopus
  100. K. Yamaji-Kegan, Q. Su, D. J. Angelini, A. C. Myers, C. Cheadle, and R. A. Johns, “Hypoxia-induced mitogenic factor (HIMF/FIZZ1/RELMalpha) increases lung inflammation and activates pulmonary microvascular endothelial cells via an IL-4-dependent mechanism,” Journal of Immunology, vol. 185, no. 9, pp. 5539–5548, 2010. View at Publisher · View at Google Scholar · View at Scopus
  101. I. N. Holcomb, R. C. Kabakoff, B. Chan et al., “FIZZ1, a novel cysteine-rich secreted protein associated with pulmonary inflammation, defines a new gene family,” The EMBO Journal, vol. 19, no. 15, pp. 4046–4055, 2000. View at Publisher · View at Google Scholar · View at Scopus
  102. K. Yamaji-Kegan, E. Takimoto, A. Zhang et al., “Hypoxia-induced mitogenic factor (FIZZ1/RELMα) induces endothelial cell apoptosis and subsequent interleukin-4-dependent pulmonary hypertension,” American Journal of Physiology—Lung Cellular and Molecular Physiology, vol. 306, pp. L1090–L1103, 2014. View at Google Scholar
  103. G. Pepe, G. Calderazzi, M. de Maglie, A. M. Villa, and E. Vegeto, “Heterogeneous induction of microglia M2a phenotype by central administration of interleukin-4,” Journal of Neuroinflammation, vol. 11, article 211, 2014. View at Publisher · View at Google Scholar
  104. J. K. Lee, J. Chung, G. T. Kannarkat, and M. G. Tansey, “Critical role of regulator G-protein signaling 10 (RGS10) in modulating macrophage M1/M2 activation,” PLoS ONE, vol. 8, no. 11, Article ID e81785, 2013. View at Publisher · View at Google Scholar · View at Scopus
  105. M. Relloso, A. Puig-Kröger, O. Muñiz Pello et al., “DC-SIGN (CD209) expression is IL-4 dependent and is negatively regulated by IFN, TGF-β, and anti-inflammatory agents,” Journal of Immunology, vol. 168, no. 6, pp. 2634–2643, 2002. View at Publisher · View at Google Scholar · View at Scopus
  106. M. B. Brown, M. von Chamier, A. B. Allam, and L. Reyes, “M1/M2 macrophage polarity in normal and complicated pregnancy,” Frontiers in Immunology, vol. 5, article 606, 2014. View at Publisher · View at Google Scholar
  107. U. Kämmerer, A. O. Eggert, M. Kapp et al., “Unique appearance of proliferating antigen-presenting cells expressing DC-SIGN (CD209) in the decidua of early human pregnancy,” The American Journal of Pathology, vol. 162, no. 3, pp. 887–896, 2003. View at Publisher · View at Google Scholar · View at Scopus
  108. G. C. Preza, K. Tanner, J. Elliott, O. O. Yang, P. A. Anton, and M. T. Ochoa, “Antigen-presenting cell candidates for HIV-1 transmission in human distal colonic mucosa defined by CD207 dendritic cells and CD209 macrophages,” AIDS Research and Human Retroviruses, vol. 30, no. 3, pp. 241–249, 2014. View at Publisher · View at Google Scholar
  109. S. Fujisaka, I. Usui, Y. Kanatani et al., “Telmisartan improves insulin resistance and modulates adipose tissue macrophage polarization in high-fat-fed mice,” Endocrinology, vol. 152, no. 5, pp. 1789–1799, 2011. View at Publisher · View at Google Scholar · View at Scopus
  110. B. A. Durafourt, C. S. Moore, D. A. Zammit et al., “Comparison of polarization properties of human adult microglia and blood-derived macrophages,” GLIA, vol. 60, no. 5, pp. 717–727, 2012. View at Publisher · View at Google Scholar · View at Scopus
  111. T. Zhou, Y. Chen, L. Hao, and Y. Zhang, “DC-SIGN and immunoregulation,” Cellular & Molecular Immunology, vol. 3, no. 4, pp. 279–283, 2006. View at Google Scholar · View at Scopus
  112. G. Raes, L. Brys, B. K. Dahal et al., “Macrophage galactose-type C-type lectins as novel markers for alternatively activated macrophages elicited by parasitic infections and allergic airway inflammation,” Journal of Leukocyte Biology, vol. 77, no. 3, pp. 321–327, 2005. View at Publisher · View at Google Scholar · View at Scopus
  113. Y. van Kooyk, J. M. Ilarregui, and S. J. van Vliet, “Novel insights into the immunomodulatory role of the dendritic cell and macrophage-expressed C-type lectin MGL,” Immunobiology, vol. 220, no. 2, pp. 185–192, 2015. View at Publisher · View at Google Scholar
  114. P. Allavena, M. Chieppa, G. Bianchi et al., “Engagement of the mannose receptor by tumoral mucins activates an immune suppressive phenotype in human tumor-associated macrophages,” Clinical and Developmental Immunology, vol. 2010, Article ID 547179, 10 pages, 2010. View at Publisher · View at Google Scholar · View at Scopus
  115. I. M. Dambuza and G. D. Brown, “C-type lectins in immunity: recent developments,” Current Opinion in Immunology, vol. 32, pp. 21–27, 2015. View at Publisher · View at Google Scholar
  116. L. Lefèvre, A. Galès, D. Olagnier et al., “PPARγ ligands switched high fat diet-induced macrophage m2b polarization toward m2a thereby improving intestinal candida elimination,” PLoS ONE, vol. 5, no. 9, Article ID e12828, pp. 1–12, 2010. View at Publisher · View at Google Scholar · View at Scopus
  117. Y. Okabe and R. Medzhitov, “How the immune system spots tumors,” eLife, vol. 3, Article ID e04476, 2014. View at Publisher · View at Google Scholar
  118. F. V. Loures, E. F. Araujo, C. Feriotti et al., “Dectin-1 induces M1 macrophages and prominent expansion of CD8+IL-17+ cells in pulmonary Paracoccidioidomycosis,” Journal of Infectious Diseases, vol. 210, no. 5, pp. 762–773, 2014. View at Publisher · View at Google Scholar
  119. D. M. Reid, M. Montoya, P. R. Taylor et al., “Expression of the beta-glucan receptor, Dectin-1, on murine leukocytes in situ correlates with its function in pathogen recognition and reveals potential roles in leukocyte interactions,” Journal of Leukocyte Biology, vol. 76, no. 1, pp. 86–94, 2004. View at Publisher · View at Google Scholar · View at Scopus
  120. K. D. Nguyen, Y. Qiu, X. Cui et al., “Alternatively activated macrophages produce catecholamines to sustain adaptive thermogenesis,” Nature, vol. 480, no. 7375, pp. 104–108, 2011. View at Publisher · View at Google Scholar · View at Scopus
  121. A. Blum, T. Setiawan, L. Hang, K. Stoyanoff, and J. V. Weinstock, “Interleukin-12 (IL-12) and IL-23 induction of substance P synthesis in murine T cells and macrophages is subject to IL-10 and transforming growth factor beta regulation,” Infection and Immunity, vol. 76, no. 8, pp. 3651–3656, 2008. View at Publisher · View at Google Scholar · View at Scopus
  122. J. I. Odegaard, R. R. Ricardo-Gonzalez, A. Red Eagle et al., “Alternative M2 activation of Kupffer cells by PPARdelta ameliorates obesity-induced insulin resistance,” Cell Metabolism, vol. 7, no. 6, pp. 496–507, 2008. View at Publisher · View at Google Scholar · View at Scopus
  123. S. Sakaguchi, J. Shono, T. Suzuki et al., “Implication of anti-inflammatory macrophages in regenerative moto-neuritogenesis: promotion of myoblast migration and neural chemorepellent semaphorin 3A expression in injured muscle,” The International Journal of Biochemistry & Cell Biology, vol. 54, pp. 272–285, 2014. View at Google Scholar
  124. Y. Qiu, K. D. Nguyen, J. I. Odegaard et al., “Eosinophils and type 2 cytokine signaling in macrophages orchestrate development of functional beige fat,” Cell, vol. 157, no. 6, pp. 1292–1308, 2014. View at Publisher · View at Google Scholar
  125. A. C. Bernard, E. A. Fitzpatrick, M. E. Maley et al., “Beta adrenoceptor regulation of macrophage arginase activity,” Surgery, vol. 127, no. 4, pp. 412–418, 2000. View at Publisher · View at Google Scholar · View at Scopus
  126. C. S. Boomershine, W. P. Lafuse, and B. S. Zwilling, “Beta2-adrenergic receptor stimulation inhibits nitric oxide generation by Mycobacterium avium infected macrophages,” Journal of Neuroimmunology, vol. 101, no. 1, pp. 68–75, 1999. View at Publisher · View at Google Scholar · View at Scopus
  127. N. Jetten, S. Verbruggen, M. J. Gijbels, M. J. Post, M. P. J. De Winther, and M. M. P. C. Donners, “Anti-inflammatory M2, but not pro-inflammatory M1 macrophages promote angiogenesis in vivo,” Angiogenesis, vol. 17, no. 1, pp. 109–118, 2014. View at Publisher · View at Google Scholar · View at Scopus
  128. C. V. Jones, T. M. Williams, K. A. Walker et al., “M2 macrophage polarisation is associated with alveolar formation during postnatal lung development,” Respiratory Research, vol. 14, article 41, 2013. View at Publisher · View at Google Scholar · View at Scopus
  129. C. M. V. Vendrame, M. D. T. Carvalho, A. G. Tempone, and H. Goto, “Insulin-like growth factor-I induces arginase activity in Leishmania amazonensis amastigote-infected macrophages through a cytokine-independent mechanism,” Mediators of Inflammation, vol. 2014, Article ID 475919, 13 pages, 2014. View at Publisher · View at Google Scholar
  130. C. M. van Stijn, J. Kim, A. J. Lusis, G. D. Barish, and R. K. Tangirala, “Macrophage polarization phenotype regulates adiponectin receptor expression and adiponectin anti-inflammatory response,” The FASEB Journal, vol. 29, no. 2, pp. 636–649, 2015. View at Publisher · View at Google Scholar
  131. P. Mandal, B. T. Pratt, M. Barnes, M. R. McMullen, and L. E. Nagy, “Molecular mechanism for adiponectin-dependent M2 macrophage polarization link between the metabolic and innate immune activity of full-length adiponectin,” The Journal of Biological Chemistry, vol. 286, no. 15, pp. 13460–13469, 2011. View at Publisher · View at Google Scholar · View at Scopus
  132. J. Sun, R. D. Ramnath, L. Zhi, R. Tamizhselvi, and M. Bhatia, “Substance P enhances NF-kappaB transactivation and chemokine response in murine macrophages via ERK1/2 and p38 MAPK signaling pathways,” The American Journal of Physiology—Cell Physiology, vol. 294, no. 6, pp. C1586–C1596, 2008. View at Publisher · View at Google Scholar · View at Scopus
  133. M. H. Jiang, E. Chung, G. F. Chi et al., “Substance P induces M2-type macrophages after spinal cord injury,” NeuroReport, vol. 23, no. 13, pp. 786–792, 2012. View at Publisher · View at Google Scholar · View at Scopus
  134. F. Tuluc, J. Meshki, S. Spitsin, and S. D. Douglas, “HIV infection of macrophages is enhanced in the presence of increased expression of CD163 induced by substance P,” Journal of Leukocyte Biology, vol. 96, no. 1, pp. 143–150, 2014. View at Publisher · View at Google Scholar
  135. H. S. Hong and Y. Son, “Substance P ameliorates collagen II-induced arthritis in mice via suppression of the inflammatory response,” Biochemical and Biophysical Research Communications, vol. 453, no. 1, pp. 179–184, 2014. View at Publisher · View at Google Scholar
  136. M. Delgado, J. Leceta, W. Sun, R. P. Gomariz, and D. Ganea, “VIP and PACAP induce shift to a Th2 response by upregulating B7.2 expression,” Annals of the New York Academy of Sciences, vol. 921, pp. 68–78, 2000. View at Google Scholar · View at Scopus
  137. A. Metwali, A. M. Blum, D. E. Elliott, and J. V. Weinstock, “IL-4 inhibits vasoactive intestinal peptide production by macrophages,” American Journal of Physiology—Gastrointestinal and Liver Physiology, vol. 283, no. 1, pp. G115–G121, 2002. View at Publisher · View at Google Scholar · View at Scopus
  138. L. Macia, E. Yulyaningsih, L. Pangon et al., “Neuropeptide Y1 receptor in immune cells regulates inflammation and insulin resistance associated with diet-induced obesity,” Diabetes, vol. 61, no. 12, pp. 3228–3238, 2012. View at Publisher · View at Google Scholar · View at Scopus
  139. K. Singer, D. L. Morris, K. E. Oatmen et al., “Neuropeptide Y is produced by adipose tissue macrophages and regulates obesity-induced inflammation,” PLoS ONE, vol. 8, no. 3, Article ID e57929, 2013. View at Publisher · View at Google Scholar · View at Scopus
  140. A. Sica, T. Schioppa, A. Mantovani, and P. Allavena, “Tumour-associated macrophages are a distinct M2 polarised population promoting tumour progression: potential targets of anti-cancer therapy,” European Journal of Cancer, vol. 42, no. 6, pp. 717–727, 2006. View at Publisher · View at Google Scholar · View at Scopus
  141. S. J. Kim, “Formation of lipoxins by alveolar macrophages,” Biochemical and Biophysical Research Communications, vol. 150, no. 2, pp. 870–876, 1988. View at Publisher · View at Google Scholar · View at Scopus
  142. P. Li, N. J. Spann, M. U. Kaikkonen et al., “NCoR repression of LXRs restricts macrophage biosynthesis of insulin-sensitizing omega 3 fatty acids,” Cell, vol. 155, no. 1, pp. 200–214, 2013. View at Publisher · View at Google Scholar · View at Scopus
  143. S. J. Kim, “Elevated formation of lipoxins in viral antibody-positive rat alveolar macrophages,” The American Journal of Respiratory Cell and Molecular Biology, vol. 3, no. 2, pp. 113–118, 1990. View at Publisher · View at Google Scholar · View at Scopus
  144. C. Godson, S. Mitchell, K. Harvey, N. A. Petasis, N. Hogg, and H. R. Brady, “Cutting edge: lipoxins rapidly stimulate nonphlogistic phagocytosis of apoptotic neutrophils by monocyte-derived macrophages,” Journal of Immunology, vol. 164, no. 4, pp. 1663–1667, 2000. View at Publisher · View at Google Scholar · View at Scopus
  145. Y. H. Huang, H. M. Wang, Z. Y. Cai, F. Y. Xu, and X. Y. Zhou, “Lipoxin A4 inhibits NF-kappaB activation and cell cycle progression in RAW264.7 cells,” Inflammation, vol. 37, no. 4, pp. 1084–1090, 2014. View at Publisher · View at Google Scholar · View at Scopus
  146. C. Moreno, P. Prieto, Á. Macías et al., “Modulation of voltage-dependent and inward rectifier potassium channels by 15-epi-lipoxin-A4 in activated murine macrophages: implications in innate immunity,” The Journal of Immunology, vol. 191, no. 12, pp. 6136–6146, 2013. View at Publisher · View at Google Scholar · View at Scopus
  147. E. Börgeson, F. C. McGillicuddy, K. A. Harford et al., “Lipoxin A4 attenuates adipose inflammation,” The FASEB Journal, vol. 26, no. 10, pp. 4287–4294, 2012. View at Publisher · View at Google Scholar · View at Scopus
  148. J. Hellmann, Y. Tang, M. Kosuri, A. Bhatnagar, and M. Spite, “Resolvin D1 decreases adipose tissue macrophage accumulation and improves insulin sensitivity in obese-diabetic mice,” The FASEB Journal, vol. 25, no. 7, pp. 2399–2407, 2011. View at Publisher · View at Google Scholar · View at Scopus
  149. G. M. Nassar, J. D. Morrow, L. J. Roberts II, F. G. Lakkis, and K. F. Badr, “Induction of 15-lipoxygenase by interleukin-13 in human blood monocytes,” The Journal of Biological Chemistry, vol. 269, no. 44, pp. 27631–27634, 1994. View at Google Scholar · View at Scopus
  150. J. Dalli and C. N. Serhan, “Specific lipid mediator signatures of human phagocytes: microparticles stimulate macrophage efferocytosis and pro-resolving mediators,” Blood, vol. 120, no. 15, pp. e60–e72, 2012. View at Publisher · View at Google Scholar · View at Scopus
  151. P. C. Norris and E. A. Dennis, “A lipidomic perspective on inflammatory macrophage eicosanoid signaling,” Advances in Biological Regulation, vol. 54, no. 1, pp. 99–110, 2014. View at Publisher · View at Google Scholar · View at Scopus
  152. N. Koning, M. van Eijk, W. Pouwels et al., “Expression of the inhibitory CD200 receptor is associated with alternative macrophage activation,” Journal of Innate Immunity, vol. 2, no. 2, pp. 195–200, 2010. View at Publisher · View at Google Scholar · View at Scopus
  153. K. J. Staples, T. S. C. Hinks, J. A. Ward, V. Gunn, C. Smith, and R. Djukanović, “Phenotypic characterization of lung macrophages in asthmatic patients: overexpression of CCL17,” Journal of Allergy and Clinical Immunology, vol. 130, no. 6, pp. 1404.e7–1412.e7, 2012. View at Publisher · View at Google Scholar · View at Scopus
  154. D. Vercelli, H. H. Jabara, B.-W. Lee, N. Woodland, R. S. Geha, and D. Y. M. Leung, “Human recombinant interleukin 4 induces FcεR2/CD23 on normal human monocytes,” The Journal of Experimental Medicine, vol. 167, no. 4, pp. 1406–1416, 1988. View at Publisher · View at Google Scholar · View at Scopus
  155. P. Gosset, I. Tillie-Leblond, S. Oudin et al., “Production of chemokines and proinflammatory and antiinflammatory cytokines by human alveolar macrophages activated by IgE receptors,” Journal of Allergy and Clinical Immunology, vol. 103, no. 2, pp. 289–297, 1999. View at Publisher · View at Google Scholar · View at Scopus
  156. G. Solinas, S. Schiarea, M. Liguori et al., “Tumor-conditioned macrophages secrete migration-stimulating factor: a new marker for M2-polarization, influencing tumor cell motility,” Journal of Immunology, vol. 185, no. 1, pp. 642–652, 2010. View at Publisher · View at Google Scholar · View at Scopus
  157. A. C. MacKinnon, S. L. Farnworth, P. S. Hodkinson et al., “Regulation of alternative macrophage activation by galectin-3,” The Journal of Immunology, vol. 180, no. 4, pp. 2650–2658, 2008. View at Publisher · View at Google Scholar · View at Scopus
  158. T. Rőszer, M. P. Menéndez-Gutiérrez, M. I. Lefterova et al., “Autoimmune kidney disease and impaired engulfment of apoptotic cells in mice with macrophage peroxisome proliferator-activated receptor gamma or retinoid X receptor alpha deficiency,” The Journal of Immunology, vol. 186, no. 1, pp. 621–631, 2011. View at Publisher · View at Google Scholar · View at Scopus
  159. N. A. Gonzalez, S. J. Bensinger, C. Hong et al., “Apoptotic cells promote their own clearance and immune tolerance through activation of the nuclear receptor LXR,” Immunity, vol. 31, no. 2, pp. 245–258, 2009. View at Publisher · View at Google Scholar · View at Scopus
  160. Z. Sarang, É. Garabuczi, G. Joós et al., “Macrophages engulfing apoptotic thymocytes produce retinoids to promote selection, differentiation, removal and replacement of double positive thymocytes,” Immunobiology, vol. 218, no. 11, pp. 1354–1360, 2013. View at Publisher · View at Google Scholar · View at Scopus
  161. T. Rőszer, M. P. Menéndez-Gutiérrez, M. Cedenilla, and M. Ricote, “Retinoid X receptors in macrophage biology,” Trends in Endocrinology and Metabolism, vol. 24, no. 9, pp. 460–468, 2013. View at Publisher · View at Google Scholar · View at Scopus
  162. N. A. Gonzalez and A. Hidalgo, “Nuclear receptors and clearance of apoptotic cells: stimulating the macrophage's appetite,” Frontiers in Immunology, vol. 5, article 211, 2014. View at Publisher · View at Google Scholar
  163. V. Nadella, Z. Wang, T. S. Johnson, M. Griffin, and A. Devitt, “Transglutaminase 2 interacts with syndecan-4 and CD44 at the surface of human macrophages to promote removal of apoptotic cells,” Biochimica et Biophysica Acta, vol. 1853, pp. 201–212, 2015. View at Google Scholar
  164. K. Shrivastava, P. Gonzalez, and L. Acarin, “The immune inhibitory complex CD200/CD200R is developmentally regulated in the mouse brain,” Journal of Comparative Neurology, vol. 520, no. 12, pp. 2657–2675, 2012. View at Publisher · View at Google Scholar · View at Scopus
  165. J. M. Crain, M. Nikodemova, and J. J. Watters, “Microglia express distinct M1 and M2 phenotypic markers in the postnatal and adult central nervous system in male and female mice,” Journal of Neuroscience Research, vol. 91, no. 9, pp. 1143–1151, 2013. View at Publisher · View at Google Scholar · View at Scopus
  166. H. M. Golbar, T. Izawa, F. Murai, M. Kuwamura, and J. Yamate, “Immunohistochemical analyses of the kinetics and distribution of macrophages, hepatic stellate cells and bile duct epithelia in the developing rat liver,” Experimental and Toxicologic Pathology, vol. 64, no. 1-2, pp. 1–8, 2012. View at Publisher · View at Google Scholar · View at Scopus
  167. U. U. Karniychuk and H. J. Nauwynck, “Quantitative changes of sialoadhesin and CD163 positive macrophages in the implantation sites and organs of porcine embryos/fetuses during gestation,” Placenta, vol. 30, no. 6, pp. 497–500, 2009. View at Publisher · View at Google Scholar · View at Scopus
  168. Y. Zhao and T. Mazzone, “Human umbilical cord blood-derived f-macrophages retain pluripotentiality after thrombopoietin expansion,” Experimental Cell Research, vol. 310, no. 2, pp. 311–318, 2005. View at Publisher · View at Google Scholar · View at Scopus
  169. S. Mahbub, C. R. Deburghgraeve, and E. J. Kovacs, “Advanced age impairs macrophage polarization,” Journal of Interferon and Cytokine Research, vol. 32, no. 1, pp. 18–26, 2012. View at Publisher · View at Google Scholar · View at Scopus
  170. J. Chang, T. Hisamatsu, K. Shimamura et al., “Activated hepatic stellate cells mediate the differentiation of macrophages,” Hepatology Research, vol. 43, no. 6, pp. 658–669, 2013. View at Publisher · View at Google Scholar · View at Scopus
  171. R. Rajaiah, D. J. Perkins, S. K. Polumuri, A. Zhao, A. D. Keegan, and S. N. Vogel, “Dissociation of endotoxin tolerance and differentiation of alternatively activated macrophages,” Journal of Immunology, vol. 190, no. 9, pp. 4763–4772, 2013. View at Publisher · View at Google Scholar · View at Scopus
  172. U. Müller, W. Stenzel, D. Piehler et al., “Abrogation of IL-4 receptor-alpha-dependent alternatively activated macrophages is sufficient to confer resistance against pulmonary cryptococcosis despite an ongoing th2 response,” International Immunology, vol. 25, no. 8, pp. 459–470, 2013. View at Publisher · View at Google Scholar · View at Scopus
  173. A. Nemethova, K. Michel, P. J. Gomez-Pinilla, G. E. Boeckxstaens, and M. Schemann, “Nicotine attenuates activation of tissue resident macrophages in the mouse stomach through the beta2 nicotinic acetylcholine receptor,” PLoS ONE, vol. 8, no. 11, Article ID e79264, 2013. View at Publisher · View at Google Scholar · View at Scopus
  174. Y. Tsuchida, F. Hatao, M. Fujisawa et al., “Neuronal stimulation with 5-hydroxytryptamine 4 receptor induces anti-inflammatory actions via alpha7nACh receptors on muscularis macrophages associated with postoperative ileus,” Gut, vol. 60, no. 5, pp. 638–647, 2011. View at Publisher · View at Google Scholar · View at Scopus
  175. J. Ma, T. Chen, J. Mandelin et al., “Regulation of macrophage activation,” Cellular and Molecular Life Sciences, vol. 60, no. 11, pp. 2334–2346, 2003. View at Publisher · View at Google Scholar · View at Scopus
  176. M. de la Fuente, M. Delgado, M. del Rio, C. Martinez, A. Hernanz, and R. P. Gomariz, “Stimulation by vasoactive intestinal peptide (VIP) of phagocytic function in rat macrophages. Protein kinase C involvement,” Regulatory Peptides, vol. 48, no. 3, pp. 345–353, 1993. View at Publisher · View at Google Scholar · View at Scopus
  177. Y. L. Sun, X. Y. Zhang, T. Sun et al., “The anti-inflammatory potential of neuropeptide FF in vitro and in vivo,” Peptides, vol. 47, pp. 124–132, 2013. View at Publisher · View at Google Scholar · View at Scopus
  178. G.-M. Qi, L.-X. Jia, Y.-L. Li, H.-H. Li, and J. Du, “Adiponectin suppresses angiotensin II-induced inflammation and cardiac fibrosis through activation of macrophage autophagy,” Endocrinology, vol. 155, no. 6, pp. 2254–2265, 2014. View at Publisher · View at Google Scholar · View at Scopus
  179. B. Luan, M. Goodarzi, N. Phillips et al., “Leptin-mediated increases in catecholamine signaling reduce adipose tissue inflammation via activation of macrophage HDAC4,” Cell Metabolism, vol. 19, pp. 1058–1065, 2014. View at Publisher · View at Google Scholar · View at Scopus
  180. E. M. Vasina, S. Cauwenberghs, M. A. Feijge, J. W. Heemskerk, C. Weber, and R. R. Koenen, “Microparticles from apoptotic platelets promote resident macrophage differentiation,” Cell Death & Disease, vol. 2, article e211, 2011. View at Google Scholar · View at Scopus
  181. P. Pelegrin and A. Surprenant, “Dynamics of macrophage polarization reveal new mechanism to inhibit IL-1Β release through pyrophosphates,” The EMBO Journal, vol. 28, no. 14, pp. 2114–2127, 2009. View at Publisher · View at Google Scholar · View at Scopus
  182. Y. Ueda, H. Kayama, S. G. Jeon et al., “Commensal microbiota induce LPS hyporesponsiveness in colonic macrophages via the production of IL-10,” International Immunology, vol. 22, no. 12, pp. 953–962, 2010. View at Publisher · View at Google Scholar · View at Scopus
  183. M. C. Canesso, A. T. Vieira, T. B. Castro et al., “Skin wound healing is accelerated and scarless in the absence of commensal microbiota,” The Journal of Immunology, vol. 193, no. 10, pp. 5171–5180, 2014. View at Publisher · View at Google Scholar
  184. R. Caesar, C. S. Reigstad, H. K. Bäckhed et al., “Gut-derived lipopolysaccharide augments adipose macrophage accumulation but is not essential for impaired glucose or insulin tolerance in mice,” Gut, vol. 61, no. 12, pp. 1701–1707, 2012. View at Publisher · View at Google Scholar · View at Scopus
  185. K. Aki, A. Shimizu, Y. Masuda et al., “ANG II receptor blockade enhances anti-inflammatory macrophages in anti-glomerular basement membrane glomerulonephritis,” The American Journal of Physiology—Renal Physiology, vol. 298, no. 4, pp. F870–F882, 2010. View at Publisher · View at Google Scholar · View at Scopus
  186. J. Wan, M. Benkdane, F. Teixeira-Clerc et al., “M2 Kupffer cells promote M1 Kupffer cell apoptosis: a protective mechanism against alcoholic and nonalcoholic fatty liver disease.,” Hepatology, vol. 59, no. 1, pp. 130–142, 2014. View at Publisher · View at Google Scholar · View at Scopus
  187. S. Epelman, K. J. Lavine, A. E. Beaudin et al., “Embryonic and adult-derived resident cardiac macrophages are maintained through distinct mechanisms at steady state and during inflammation,” Immunity, vol. 40, no. 1, pp. 91–104, 2014. View at Publisher · View at Google Scholar · View at Scopus
  188. E. G. Perdiguero, K. Klapproth, C. Schulz et al., “Tissue-resident macrophages originate from yolk-sac-derived erythro-myeloid progenitors,” Nature, vol. 518, no. 7540, pp. 547–551, 2014. View at Publisher · View at Google Scholar
  189. K. Molawi, Y. Wolf, P. K. Kandalla et al., “Progressive replacement of embryo-derived cardiac macrophages with age,” Journal of Experimental Medicine, vol. 211, no. 11, pp. 2151–2158, 2014. View at Publisher · View at Google Scholar
  190. C. Schulz, E. G. Perdiguero, L. Chorro et al., “A lineage of myeloid cells independent of Myb and hematopoietic stem cells,” Science, vol. 336, no. 6077, pp. 86–90, 2012. View at Publisher · View at Google Scholar · View at Scopus
  191. C. C. Bain, A. Bravo-Blas, C. L. Scott et al., “Constant replenishment from circulating monocytes maintains the macrophage pool in the intestine of adult mice,” Nature Immunology, vol. 15, pp. 929–937, 2014. View at Google Scholar
  192. C. El Chartouni, L. Schwarzfischer, and M. Rehli, “Interleukin-4 induced interferon regulatory factor (Irf) 4 participates in the regulation of alternative macrophage priming,” Immunobiology, vol. 215, no. 9-10, pp. 821–825, 2010. View at Publisher · View at Google Scholar · View at Scopus
  193. M. P. Menéndez-Gutiérrez, T. Rőszer, L. Fuentes et al., “Retinoid X receptors orchestrate osteoclast differentiation and postnatal bone remodeling,” The Journal of Clinical Investigation, vol. 125, no. 2, pp. 809–823, 2015. View at Publisher · View at Google Scholar
  194. C. I. Caescu, X. Guo, L. Tesfa et al., “Colony stimulating factor-1 receptor signaling networks inhibit mouse macrophage inflammatory responses by induction of microRNA-21,” Blood, vol. 125, no. 8, pp. e1–e13, 2015. View at Publisher · View at Google Scholar
  195. F. Steinbach, R. Stark, S. Ibrahim et al., “Molecular cloning and characterization of markers and cytokines for equid myeloid cells,” Veterinary Immunology and Immunopathology, vol. 108, no. 1-2, pp. 227–236, 2005. View at Publisher · View at Google Scholar · View at Scopus
  196. K. A. Jackson, J. L. Stott, D. W. Horohov, and J. L. Watson, “IL-4 induced CD23 (FcepsilonRII) up-regulation in equine peripheral blood mononuclear cells and pulmonary alveolar macrophages,” Veterinary Immunology and Immunopathology, vol. 101, no. 3-4, pp. 243–250, 2004. View at Publisher · View at Google Scholar · View at Scopus
  197. T. R. Pettitt, A. F. Rowley, S. E. Barrow, A. I. Mallet, and C. J. Secombes, “Synthesis of lipoxins and other lipoxygenase products by macrophages from the rainbow trout, Oncorhynchus mykiss,” The Journal of Biological Chemistry, vol. 266, no. 14, pp. 8720–8726, 1991. View at Google Scholar · View at Scopus
  198. T. Rőszer, “The invertebrate midintestinal gland (‘hepatopancreas’) is an evolutionary forerunner in the integration of immunity and metabolism,” Cell and Tissue Research, vol. 358, no. 3, pp. 685–695, 2014. View at Publisher · View at Google Scholar
  199. A. Franchini and E. Ottaviani, “Repair of molluscan tissue injury: role of PDGF and TGF-beta1,” Tissue and Cell, vol. 32, no. 4, pp. 312–321, 2000. View at Publisher · View at Google Scholar · View at Scopus
  200. J. Yang, S. C. Lin, G. Chen et al., “Adiponectin promotes monocyte-to-fibroblast transition in renal fibrosis,” Journal of the American Society of Nephrology, vol. 24, no. 10, pp. 1644–1659, 2013. View at Publisher · View at Google Scholar · View at Scopus
  201. S. Sricharoen, J. K. Jeong, S. Tunkijjanukij, and I. Söderhäll, “Exocytosis and proteomic analysis of the vesicle content of granular hemocytes from a crayfish,” Developmental and Comparative Immunology, vol. 29, no. 12, pp. 1017–1031, 2005. View at Publisher · View at Google Scholar · View at Scopus
  202. F. Badariotti, C. Lelong, M. P. Dubos, and P. Favrel, “Characterization of chitinase-like proteins (Cg-Clp1 and Cg-Clp2) involved in immune defence of the mollusc Crassostrea gigas,” The FEBS Journal, vol. 274, no. 14, pp. 3646–3654, 2007. View at Publisher · View at Google Scholar · View at Scopus
  203. R. B. Kirkpatrick, R. E. Matico, D. E. McNulty, J. E. Strickler, and M. Rosenberg, “An abundantly secreted glycoprotein from Drosophila melanogaster is related to mammalian secretory proteins produced in rheumatoid tissues and by activated macrophages,” Gene, vol. 153, no. 2, pp. 147–154, 1995. View at Publisher · View at Google Scholar · View at Scopus
  204. E. A. C. Heath-Heckman and M. J. McFall-Ngai, “The occurrence of chitin in the hemocytes of invertebrates,” Zoology (Jena), vol. 114, no. 4, pp. 191–198, 2011. View at Publisher · View at Google Scholar · View at Scopus
  205. S. Pongsomboon, S. Tang, S. Boonda et al., “Differentially expressed genes in Penaeus monodon hemocytes following infection with yellow head virus,” BMB Reports, vol. 41, no. 9, pp. 670–677, 2008. View at Publisher · View at Google Scholar
  206. S. Bunt, C. Hooley, N. Hu, C. Scahill, H. Weavers, and H. Skaer, “Hemocyte-secreted type IV collagen enhances BMP signaling to guide renal tubule morphogenesis in Drosophila,” Developmental Cell, vol. 19, no. 2, pp. 296–306, 2010. View at Publisher · View at Google Scholar · View at Scopus
  207. F. Li, L. Xu, X. Gai et al., “The involvement of PDGF/VEGF related factor in regulation of immune and neuroendocrine in Chinese mitten crab Eriocheir sinensis,” Fish and Shellfish Immunology, vol. 35, no. 4, pp. 1240–1248, 2013. View at Publisher · View at Google Scholar · View at Scopus