Macrophages: Plastic solutions to environmental heterogeneity

Inflammation Research

Volumn 62, Issue 9, 2013, Pages 835-843

  Giorgio, Selma ^a  

^a UNIVERSITY OF CAMPINAS   (Brazil)

Author keywords

Macrophages; Mononuclear phagocyte; Phenotype; Plasticity; Reaction norm

Indexed keywords

ADENOSINE TRIPHOSPHATE; CD209 ANTIGEN; GAMMA INTERFERON; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INTERLEUKIN 10; INTERLEUKIN 23; INTERLEUKIN 7 RECEPTOR; TUMOR NECROSIS FACTOR ALPHA;

ANTIGEN EXPRESSION; CELL HETEROGENEITY; CELL STIMULATION; CYTOKINE PRODUCTION; ENVIRONMENTAL HETEROGENEITY; EVOLUTIONARY ADAPTATION; HUMAN; HYPOXIA; INTRACELLULAR SIGNALING; MACROPHAGE; MACROPHAGE ACTIVATION; MICROENVIRONMENT; MOLECULAR DYNAMICS; NONHUMAN; OBESITY; PHENOTYPIC PLASTICITY; PROTEIN EXPRESSION; REVIEW; TUMOR ASSOCIATED LEUKOCYTE;

EID: 84882686747     PISSN: 10233830     EISSN: 1420908X     Source Type: Journal    
DOI: 10.1007/s00011-013-0647-7     Document Type: Review

References (90)

1. Ottaviani E, Franceschi C. The invertebrate phagocytic immunocyte: clues to a common evolution of immune and neuroendocrine systems. Immunol Today. 1997;18:169-74.
2. Ottaviani E, Malagoli D, Grimaldi A, De Eguileor M. The case of the "serfdom" condition of phagocytic immune cells. Invert Surv J. 2012;9:134-8.
3. Desjardins M, Houde M, Gagnon E. Phagocytosis: the convoluted way from nutrition to adaptaive immunity. Immunol Rev. 2005;207:158-65.
4. Aderem A, Underhill DM. Mechanisms of phagocytosis in macrophages. Annu Rev Immunol. 1999;17:593-623.
5. Dale DC, Boxer L, Liles WC. The phagocytes: neutrophils and monocytes. Blood. 2008;112:935-45.
6. Metchnikoff E. Lectures on the comparative pathology of inflammation. London: Trench; 1893.
7. Silverstein AM. A history of immunology. San Diego: Academic; 1989. p. 40-56.
8. Hume DA, Ross IL, Himes SR, Sasmono RT, Wells CA, Ravasi T. The mononuclear phagocyte system revisited. J Leukoc Biol. 2002;72:621-7.
9. Habicht GS. Primordial immunity: foundations for the vertebrate immune system. In: Beck C, Habicht GS, Cooper EL, Marchalonis JJ, editors. The vertebrate immune system, New York: New York Academy of Sciences; 1994. pp. ix-xi.
10. Maurya MR, Benner C, Pradervand S, Glass C, Subramaniam S. Systems biology of macrophages. Adv Exp Med Biol. 2007;598:62-79.
11. Germain RN, Meier-Schellersheim M, Nita-Lazar A, Fraser ID. Systems biology in immunology: a computational modeling perspective. Annu Rev Immunol. 2011;29:527-85.
12. Murray PJ, Wynn TA. Protective and pathogenic functions of macrophage subsets. Nat Rev Immunol. 2011;11:723-37.
13. Halmilton JA. Therapeutic potential of targeting inflammation. Inflamm Res. 2013;62:653-65.
14. Gordon S, Martinez FO. Alternative activation of macrophages: mechanism and functions. Immunity. 2010;32:593-604.
15. Martinez FO, Helming L, Gordon S. Alternative activation of macrophages: an immunologic functional perspective. Annu Rev Immunol. 2009;27:451-83.
16. Stout RD, Watkins SK, Suttles J. Functional plasticity of macrophages: in situ reprogramming of tumor-associated macrophages. J Leukoc Biol. 2009;86:1105-9.
17. Mosser DM, Edwards JP. Exploring the full spectrum of macrophage activation. Nat Rev Immunol. 2008;8:958-69.
18. Galli SJ, Borregaard N, Wynn TA. Phenotypic and functional plasticity of cells of innate immunity: macrophages, mast cells and neutrophils. Nat Immunol. 2011;12:1035-44.
19. Weidenbusch M, Anders H-J. Tissue microenvironments define and get reinforced by macrophage phenotypes in homeostasis or during inflammation, repair and fibrosis. J Innate Immun. 2012;4:463-77.
20. Hamilton TA. Molecular basis of macrophage activation: from gene expression to phenotypic diversity. In: Burke B, Lewis CE, editors. The macrophage. New York: Oxford University Press; 2002. p. 74-102.
21. Grage-Griebenow E, Flad HD, Ernst M. Heterogeneity of human peripheral blood monocyte subsets. J Leukoc Biol. 2001;69:11-20.
22. Erwig LP, Kluth DC, Rees AJ. Macrophage heterogeneity in renal inflammation. Nephrol Dial Transplant. 2003;18:1962-5.
23. Gordon S, Taylor PR. Monocyte and macrophage heterogeneity. Nat Rev Immunol. 2005;5:953-64.
24. Kono H, Fujii H, Asakawa M, Yamamoto M, Maki A, Matsuda M, et al. Functional heterogeneity of the Kupffer cell population is involved in the mechanism of gadolinium chloride in rats administered endotoxin. J Surg Res. 2002;106:179-87.
25. He Y, Sadahiro T, Noh SI, Wang H, Todo T, Chai NN. Flow cytometric isolation and phenotypic characterization of two subsets of ED2(+) (CD163) hepatic macrophages in rats. Hepatol Res. 2009;39:1208-18.
26. Kinoshita M, Uchida T, Sato A, Nakashima M, Nakashima H, Shono S, et al. Characterization of two F4/80-positive Kupffer cell subsets by their function and phenotype in mice. J Hepatol. 2010;53:903-10.
27. Movita D, Kreefft K, Biesta P, van Oudenaren A, Leenen PJ, Janssen HL, et al. Kupffer cells express a unique combination of phenotypic and functional characteristics compared with splenic and peritoneal macrophages. J Leukoc Biol. 2012;92:723-33.
28. Kraal G. Cells in the marginal zone of the spleen. Int Rev Cytol. 1992;132:31-74.
29. den Haan JM, Kraal G. Innate immune functions of macrophage subpopulations in the spleen. J Innate Immun. 2012;4:437-45.
30. Gordon S. Innate immune functions of macrophages in different tissue environments. J Innate Immun. 2012;4:409-10.
31. Taylor PR, Martinez-Pomares L, Stacey M, Lin HH, Brown GD, Gordon S. Macrophage receptors and immune recognition. Annu Rev Immunol. 2005;23:901-44.
32. Liddiard K, Rosas M, Davies LC, Jones SA, Taylor PR. Macrophage heterogeneity and acute inflammation. Eur J Immunol. 2011;41:2503-8.
33. Hashimoto D, Miller J, Merad M. Dendritic cell and macrophage heterogeneity in vivo. Immunity. 2011;35:323-35.
34. Rutherford MS, Witsel A, Schook LB. Mechanisms generating functionally heterogeneous macrophages: chaos revisited. J Leukoc Biol. 1993;53:602-18.
35. Schust DJ, Magamatsu T. Does the classical M1/M2 dichotomy reflect the functional phenotypes of human decidual macrophages? Expert Rev Obstr Gynecol. 2011;4:377-80.
36. Porcheray F, Viaud S, Rimaniol AC, Léone C, Samah B, Dereuddre-Bosquet N, et al. Macrophage activation switching: an asset for the resolution of inflammation. Clin Exp Immunol. 2005;142:481-9.
37. Mantovani A. Macrophage diversity and polarization: in vivo veritas. Blood. 2006;108:408-9.
38. Biswas SK, Chittezhath M, Shalova IN, Lim JY. Macrophage polarization and plasticity in health and disease. Immunol Res. 2012;53:11-24.
39. Daley JM, Reichner JS, Mahoney EJ, Manfield L, Henry WL Jr, Mastrofrancesco B, et al. Modulation of macrophage phenotype by soluble product(s) released from neutrophils. J Immunol. 2005;174:2265-72.
40. Adamson S, Leitinger N. Phenotypic modulation of macrophages in response to plaque lipids. Curr Opin Lipidol. 2011;22:335-42.
41. Gleissner CA. Macrophage phenotype modulation by CXCL4 in atherosclerosis. Front Physiol. 2012;3:1.
42. Gratchev A, Schledzewski K, Guillot P, Goerdt S. Alternatively activated antigen-presenting cells: molecular repertoire, immune regulation, and healing. Skin Pharmacol Appl Skin Physiol. 2001;14:272-9.
43. Mantovani A, Sozzani S, Locati M, Allavena P, Sica A. Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol. 2002;23:549-55.
44. Stein BE, Burr D, Constantinidis C, Laurienti PJ, Alex MM, Perrault TJ, et al. Semantic confusion regarding the development of multisensory integration: a practical solution. Eur J Neurosci. 2010;31:1713-20.
45. Huang H, Fletcher A, Niu Y, Wang TY, Yu L. Characterization of lipopolysaccharide-stimulated cytokine expression in macrophages and monocytes. Inflamm Res. 2012;61:1329-38.
46. ZhangW XuW, Xiong S. Blockade of Notch1 signaling alleviates murine lupus via blunting macrophage activation and M2b polarization. J Immunol. 2010;184:6465-78.
47. Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, Locati M. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 2004;25:677-86.
48. Stout RD, Jiang C, Matta B, Tietzel I, Watkins SK, Suttles J. Macrophages sequentially change their functional phenotype in response to changes in microenvironmental influences. J Immunol. 2005;175:342-9.
49. Stout RD, Suttles J. Functional plasticity of macrophages: reversible adaptation to changing microenvironments. J Leukoc Biol. 2004;76:509-13.
50. Stout RD, Suttles J. Immunosenescence and macrophage functional plasticity: dysregulation of macrophage function by age-associated microenvironmental changes. Immunol Rev. 2005;205:60-71.
51. Stout RD. Macrophage functional phenotypes: no alternatives in dermal wound healing? J Leukoc Biol. 2010;87:19-21.
52. Mills CD, Kincaid K, Alt JM, Heilman MJ, Hill AM. M-1/M-2 macrophages and the Th1/Th2 paradigm. J Immunol. 2000;164:6166-73.
53. Meyer M, Huaux F, Gavilanes X, van den Brûle S, Lebecque P, Lore S, et al. Azithromycin reduces exaggerated cytokine production by M1 alveolar macrophages in cystic fibrosis. Am J Respir Cell Mol Biol. 2009;41:590-602.
54. Ortega MT, Xie L, Mora S, Chapes SK. Evaluation of macrophage plasticity in brown and white adipose tissue. Cell Immunol. 2011;271:124-33.
55. Empey KM, Orend JG, Peebles RS Jr, Egaña L, Norris KA, Oury TD, et al. Stimulation of immature lung macrophages with intranasal interferon gamma in a novel neonatal mouse model of respiratory syncytial virus infection. PLoS ONE. 2012;7:e40499.
56. Colhone MC, Arrais-Silva WW, Picolli C, Giorgio S. Effect of hypoxia on macrophage infection by Leishmania amazonensis. J Parasitol. 2004;90:510-5.
57. Degrosolli A, Colhone MC, Arrais-Silva WW, Giorgio S. Hypoxia modulates expression of the 70-kD heat shock protein and reduces Leishmania infection in macrophages. J Biomed Sci. 2004;11:847-54.
58. Degrossoli A, Bosetto MC, Lima CB, Giorgio S. Expression of hypoxia-inducible factor 1α in mononuclear phagocytes infected with Leishmania amazonensis. Immunol Lett. 2007;114:119-25.
59. Degrossoli A, Arrais-Silva WW, Colhone MC, Gadelha FR, Joazeiro PJ, Giorgio S. The influence of low oxygen on macrophage response to Leishmania infection. Scand J Immunol. 2011;74:165-75.
60. Murdoch C, Giannoudis A, Lewis CE. Mechanisms regulating the recruitment of macrophages into hypoxic areas of tumors and other ischemic tissues. Blood. 2004;104:2224-34.
61. Rahat MA, Bitterman H, Lahat N. Molecular mechanisms regulating macrophage response to hypoxia. Front Immunol. 2011;2:45.
62. Bosco MC, Puppo M, Blengio F, Fraone T, Cappello P, Giovarelli M, et al. Monocytes and dendritic cells in a hypoxic environment: spotlights on chemotaxis and migration. Immunobiology. 2008;213:733-49.
63. Murdoch C, Muthana M, Lewis CE. Hypoxia regulates macrophage functions in inflammation. J Immunol. 2005;175:6257-63.
64. Lahat N, Rahat MA, Ballan M, Weiss-Cerem L, Engelmayer M, Bitterman H. Hypoxia reduces CD80 expression on monocytes but enhances their LPS-stimulated TNF-alpha secretion. J Leukoc Biol. 2003;74:197-205.
65. Spear W, Chan D, Coppens I, Johnson RS, Giaccia A, Blader IJ. The host cell transcription factor hypoxia-inducible factor 1 is required for Toxoplasma gondii growth and survival at physiological oxygen levels. Cell Microbiol. 2006;8:339-52.
66. Nickel D, Busch M, Mayer D, Hagemann B, Knoll V, Stenger S. Hypoxia triggers the expression of human β defensin 2 and antimicrobial activity against Mycobacterium tuberculosis in human macrophages. J Immunol. 2012;188:4001-7.
67. Puppo M, Bosco MC, Federico M, Pastorino S, Varesio L. Hypoxia inhibits Moloney murine leukemia virus expression in activated macrophages. J Leukoc Biol. 2007;81:528-38.
68. Degrossoli A, Giorgio S. Functional alterations in macrophages after hypoxia selection. Exp Biol Med. 2007;232:88-95.
69. Leroux A, Ferrere G, Godie V, Cailleux F, Cailleux F, Renoud ML, Gaudin F, et al. Toxic lipids stored by Kupffer cells correlates with their pro-inflammatory phenotype at an early stage of steatohepatitis. J Hepatol. 2012;57:141-9.
70. Lorne E, Zmijewski JW, Zhao X, Liu G, Tsuruta Y, Park Y-J, Dupont H, Abraham E. Role of extracellular superoxide in neutrophil activation: interactions between xanthine oxidase and TLR4 induce proinflammatory cytokine production. Am J Physiol Cell Physiol. 2008;294:C985-93.
71. Nicholas SA, Coughlan K, Yasinska I, Lall GS, Gibbs BF, Calzolai L, Sumbayev VV. Dysfunctional mitochondria contain endogenous high-affinity human Toll-like receptor 4 (TLR4) ligands and induce TLR4-mediated inflammatory reactions. Int J Biochem Cell Biol. 2011;43:674-81.
72. Romagnoli M, Gomez-Cabrera MC, Perrelli MG, Biasi F, Pallardó FV, Sastre J, Poli G, Viña J. Xanthine oxidase-induced oxidative stress causes activation of NF-kappaB and inflammation in the liver of type I diabetic rats. Free Radic Biol Med. 2010;49:171-7.
73. Lewis CL, Pollard JW. Distincts roles of macrophages in different tumor microenvironments. Cancer Res;2006 pp. 605-612.
74. Pettersen JS, Fuentes-Duculan J, Suárez-Fariñas M, Pierson KC, Pitts-Kiefer A, Fan L, et al. Tumor-associated macrophages in the cutaneous SCC microenvironment are heterogeneously activated. J Invest Dermatol. 2011;131:1322-30.
75. Stofanko M, Kwon SY, Badenhorst P. Lineage tracing of lamellocytes demonstrates Drosophila macrophage plasticity. PLoS ONE. 2010;5:e14051.
76. DeWitt TJ, Scheiner SM. Phenotypic plasticity. Functional and conceptual approaches. New York: Oxford University Press; 2004.
77. Pigliucci M. Phenotypic plasticity: beyond nature and nurture. Baltimore: University Press; 2001.
78. Schlichting CD, Pigliucci M. Phenotypic evolution: a reaction norm perspective. Sunderland: Sinauer; 1998.
79. Chevin LM, Lande R, Mace GM. Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory. PLos Biol;2010 p. e1000357.
80. Svennungsen TO, Holen ØH, Leimar O. Inducible defenses: continuous reaction norms or threshold traits? Am Nat. 2011;178:397-410.
81. Fuller T. The integrative biology of phenotypic plasticity. Biol Philos. 2003;18:381-9.
82. Stearns SC. The evolutionary significance of phenotypic plasticity. Bioscience. 1989;39:436-45.
83. Dodson S. Predator-induced reaction norms. Bioscience. 1989;39:447-51.
84. Ebert D. A genome for the environment. Science. 2011;331:539-40.
85. Daley JM, Brancato SK, Thomay AA, Reichner JS, Albina JE. The phenotype of murine wound macrophages. J Leukoc Biol. 2010;87:59-67.
86. Xu W, Zhao X, Daha MR, et al. Reversible differentiation of pro- and anti-inflammatory macrophages. Mol Immunol. 2013;53:179-86.
87. Piersma T, van Gils JA. The flexible phenotype. A body-centred integration of ecology, physiology, and behavior. New York: Oxford University Press; 2011.
88. Whitman DW, Agrawal AA. What is phenotypic plasticity and why is it important? In: Whitman DW, Ananthakrishnan TN, editors. Phenotypic Plasticity of Insects: mechanisms and consequences. Enfield: Science Publishers; 2009. p. 1-63.
89. Lof ME, Reed TE, McNamara JM, Visser ME. Timing in a fluctuating environment: environmental variability and asymmetric fitness curves can lead to adaptively mismatched avian reproduction. Proc Biol Sci. 2012;279:3161-9.
90. Jenkins SJ, Ruckerl D, Cook PC, Jones LH, Finkelman FD, van Rooijen N, et al. Local macrophage proliferation, rather than recruitment from the blood, is a signature of TH2 inflammation. Science. 2011;332:1284-8.