Understanding macrophage diversity at the ontogenic and transcriptomic levels

Immunological Reviews

Volumn 262, Issue 1, 2014, Pages 85-95

  Gautier, Emmanuel L ^a,b,c   Yvan Charvet, Laurent ^d,e  

^a INSERM   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c Institute of Cardiometabolism and Nutrition (ICAN)   (France)

^d CENTRE MÉDITERRANÉEN DE MÉDECINE MOLÉCULAIRE C3M   (France)

^e Atip Avenir   (France)

Author keywords

Diversity; Monocyte derived macrophages; Ontogeny; Regulatory networks; Tissue macrophages

Indexed keywords

TRANSCRIPTOME;

ANIMAL; ANTIBODY SPECIFICITY; CELL DIFFERENTIATION; CLASSIFICATION; CYTOLOGY; GENE REGULATORY NETWORK; GENETICS; GENOMICS; HUMAN; IMMUNOLOGY; INFLAMMATION; LYSOSOME; MACROPHAGE; METABOLISM; MONOCYTE; PATHOLOGY; PHAGOCYTOSIS; PHENOTYPE; PHYSIOLOGY;

ANIMALS; CELL DIFFERENTIATION; GENE REGULATORY NETWORKS; GENOMICS; HUMANS; INFLAMMATION; LYSOSOMES; MACROPHAGES; MONOCYTES; ORGAN SPECIFICITY; PHAGOCYTOSIS; PHENOTYPE; TRANSCRIPTOME;

EID: 84911010946     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/imr.12231     Document Type: Article

References (81)

1. Gordon S, Taylor PR. Monocyte and macrophage heterogeneity. Nat Rev Immunol 2005;5:953-964.
2. Gautier EL, Ivanov S, Lesnik P, Randolph GJ. Local apoptosis mediates clearance of macrophages from resolving inflammation in mice. Blood 2013;122:2714-2722.
3. Khallou-Laschet J, et al. Macrophage plasticity in experimental atherosclerosis. PLoS One 2010;5:e8852.
4. Xue J, et al. Transcriptome-based network analysis reveals a spectrum model of human macrophage activation. Immunity 2014;40:274-288.
5. Takahashi K, Naito M, Takeya M. Development and heterogeneity of macrophages and their related cells through their differentiation pathways. Pathol Int 1996;46:473-485.
6. Takahashi K. Development and differentiation of macrophages and related cells: historical review and current concepts. J Clin Exp Hematop 2001;41:1-31.
7. van Furth R, Cohn ZA. The origin and kinetics of mononuclear phagocytes. J Exp Med 1968;128:415-435.
8. Ginhoux F, et al. Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science 2010;330:841-845.
9. Schulz C, et al. A lineage of myeloid cells independent of Myb and hematopoietic stem cells. Science 2012;336:86-90.
10. Epelman S, et al. Embryonic and adult-derived resident cardiac macrophages are maintained through distinct mechanisms at steady state and during inflammation. Immunity 2014;40:91-104.
11. Gautier EL, et al. Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nat Immunol 2012;13:1118-1128.
12. Guilliams M, et al. Alveolar macrophages develop from fetal monocytes that differentiate into long-lived cells in the first week of life via GM-CSF. J Exp Med 2013;210:1977-1992.
13. Samokhvalov IM, Samokhvalova NI, Nishikawa S. Cell tracing shows the contribution of the yolk sac to adult haematopoiesis. Nature 2007;446:1056-1061.
14. Yona S, et al. Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis. Immunity 2013;38:79-91.
15. Hashimoto D, et al. Tissue-resident macrophages self-maintain locally throughout adult life with minimal contribution from circulating monocytes. Immunity 2013;38:792-804.
16. Varol C, et al. Intestinal lamina propria dendritic cell subsets have different origin and functions. Immunity 2009;31:502-512.
17. Coggle JE, Tarling JD. The proliferation kinetics of pulmonary alveolar macrophages. J Leukoc Biol 1984;35:317-327.
18. Sawyer RT. The significance of local resident pulmonary alveolar macrophage proliferation to population renewal. J Leukoc Biol 1986;39:77-87.
19. Sawyer RT, Strausbauch PH, Volkman A. Resident macrophage proliferation in mice depleted of blood monocytes by strontium-89. Lab Invest 1982;46:165-170.
20. Jenkins SJ, et al. Local macrophage proliferation, rather than recruitment from the blood, is a signature of TH2 inflammation. Science 2011;332:1284-1288.
21. Aziz A, Soucie E, Sarrazin S, Sieweke MH. MafB/c-Maf deficiency enables self-renewal of differentiated functional macrophages. Science 2009;326:867-871.
22. Jenkins SJ, et al. IL-4 directly signals tissue-resident macrophages to proliferate beyond homeostatic levels controlled by CSF-1. J Exp Med 2013;210:2477-2491.
23. Davies LC, et al. Distinct bone marrow-derived and tissue-resident macrophage lineages proliferate at key stages during inflammation. Nat Commun 2013;4:1886.
24. Naito M, Hayashi S, Yoshida H, Nishikawa S, Shultz LD, Takahashi K. Abnormal differentiation of tissue macrophage populations in 'osteopetrosis' (op) mice defective in the production of macrophage colony-stimulating factor. Am J Pathol 1991;139:657-667.
25. Witmer-Pack MD, et al. Identification of macrophages and dendritic cells in the osteopetrotic (op/op) mouse. J Cell Sci 1993;104(Pt 4):1021-1029.
26. Cecchini MG, et al. Role of colony stimulating factor-1 in the establishment and regulation of tissue macrophages during postnatal development of the mouse. Development 1994;120:1357-1372.
27. Wang Y, et al. IL-34 is a tissue-restricted ligand of CSF1R required for the development of Langerhans cells and microglia. Nat Immunol 2012;13:753-760.
28. Greter M, et al. Stroma-derived interleukin-34 controls the development and maintenance of langerhans cells and the maintenance of microglia. Immunity 2012;37:1050-1060.
29. Lagasse E, Weissman IL. Enforced expression of Bcl-2 in monocytes rescues macrophages and partially reverses osteopetrosis in op/op mice. Cell 1997;89:1021-1031.
30. Otero K, et al. Macrophage colony-stimulating factor induces the proliferation and survival of macrophages via a pathway involving DAP12 and beta-catenin. Nat Immunol 2009;10:734-743.
31. Stanley ER, Chitu V. CSF-1 receptor signaling in myeloid cells. Cold Spring Harb Perspect Biol 2014;6. doi: 10.1101/cshperspect.a021857.
32. Gautier EL, et al. Gata6 regulates aspartoacylase expression in resident peritoneal macrophages and controls their survival. J Exp Med 2014;211:1525-1531.
33. Gautier EL, Jakubzick C, Randolph GJ. Regulation of the migration and survival of monocyte subsets by chemokine receptors and its relevance to atherosclerosis. Arterioscler Thromb Vasc Biol 2009;29:1412-1418.
34. Carlin LM, et al. Nr4a1-dependent Ly6C(low) monocytes monitor endothelial cells and orchestrate their disposal. Cell 2013;153:362-375.
35. Zigmond E, et al. Infiltrating monocyte-derived macrophages and resident kupffer cells display different ontogeny and functions in acute liver injury. J Immunol 2014;193:344-353.
36. Bellingan GJ, Caldwell H, Howie SE, Dransfield I, Haslett C. In vivo fate of the inflammatory macrophage during the resolution of inflammation: inflammatory macrophages do not die locally, but emigrate to the draining lymph nodes. J Immunol 1996;157:2577-2585.
37. Randolph GJ. Mechanisms that regulate macrophage burden in atherosclerosis. Circ Res 2014;114:1757-1771.
38. Jung S, Schwartz M. Non-identical twins - microglia and monocyte-derived macrophages in acute injury and autoimmune inflammation. Front Immunol 2012;3:89.
39. Shechter R, et al. Infiltrating blood-derived macrophages are vital cells playing an anti-inflammatory role in recovery from spinal cord injury in mice. PLoS Med 2009;6:e1000113.
40. Ajami B, Bennett JL, Krieger C, McNagny KM, Rossi FM. Infiltrating monocytes trigger EAE progression, but do not contribute to the resident microglia pool. Nat Neurosci 2011;14:1142-1149.
41. Gordon S, Hamann J, Lin HH, Stacey M. F4/80 and the related adhesion-GPCRs. Eur J Immunol 2011;41:2472-2476.
42. Heng TS, Painter MW. Immunological Genome Project C. The Immunological Genome Project: networks of gene expression in immune cells. Nat Immunol 2008;9:1091-1094.
43. Langlet C, et al. CD64 expression distinguishes monocyte-derived and conventional dendritic cells and reveals their distinct role during intramuscular immunization. J Immunol 2012;188:1751-1760.
44. Jakubzick C, et al. Minimal differentiation of classical monocytes as they survey steady-state tissues and transport antigen to lymph nodes. Immunity 2013;39:599-610.
45. Bogunovic M, et al. Origin of the lamina propria dendritic cell network. Immunity 2009;31:513-525.
46. Maxfield FR. Role of endosomes and lysosomes in human disease. Cold Spring Harb Perspect Biol 2014;6:a016931.
47. Boustany RM. Lysosomal storage diseases-the horizon expands. Nat Rev Neurol 2013;9:583-598.
48. Platt FM, Boland B, van der Spoel AC. The cell biology of disease: lysosomal storage disorders: the cellular impact of lysosomal dysfunction. J Cell Biol 2012;199:723-734.
49. Jerome WG. Advanced atherosclerotic foam cell formation has features of an acquired lysosomal storage disorder. Rejuvenation Res 2006;9:245-255.
50. Xu X, Grijalva A, Skowronski A, van Eijk M, Serlie MJ, Ferrante AW Jr. Obesity activates a program of lysosomal-dependent lipid metabolism in adipose tissue macrophages independently of classic activation. Cell Metab 2013;18:816-830.
51. Sardiello M, et al. A gene network regulating lysosomal biogenesis and function. Science 2009;325:473-477.
52. Palmieri M, et al. Characterization of the CLEAR network reveals an integrated control of cellular clearance pathways. Hum Mol Genet 2011;20:3852-3866.
53. Visvikis O, et al. Innate host defense requires TFEB-mediated transcription of cytoprotective and antimicrobial genes. Immunity 2014;40:896-909.
54. Medina DL, et al. Transcriptional activation of lysosomal exocytosis promotes cellular clearance. Dev Cell 2011;21:421-430.
55. Pastore N, et al. Gene transfer of master autophagy regulator TFEB results in clearance of toxic protein and correction of hepatic disease in alpha-1-anti-trypsin deficiency. EMBO Mol Med 2013;5:397-412.
56. Spampanato C, et al. Transcription factor EB (TFEB) is a new therapeutic target for Pompe disease. EMBO Mol Med 2013;5:691-706.
57. Haniffa M, et al. Human tissues contain CD141hi cross-presenting dendritic cells with functional homology to mouse CD103+ nonlymphoid dendritic cells. Immunity 2012;37:60-73.
58. Jojic V, et al. Identification of transcriptional regulators in the mouse immune system. Nat Immunol 2013;14:633-643.
59. Kohyama M, et al. Role for Spi-C in the development of red pulp macrophages and splenic iron homeostasis. Nature 2009;457:318-321.
60. Carlsson R, Hjalmarsson A, Liberg D, Persson C, Leanderson T. Genomic structure of mouse SPI-C and genomic structure and expression pattern of human SPI-C. Gene 2002;299:271-278.
61. Haldar M, et al. Heme-mediated SPI-C induction promotes monocyte differentiation into iron-recycling macrophages. Cell 2014;156:1223-1234.
62. Terpstra V, van Berkel TJ. Scavenger receptors on liver Kupffer cells mediate the in vivo uptake of oxidatively damaged red blood cells in mice. Blood 2000;95:2157-2163.
63. Willekens FL, et al. Liver Kupffer cells rapidly remove red blood cell-derived vesicles from the circulation by scavenger receptors. Blood 2005;105:2141-2145.
64. Gorgani NN, Ma Y, Clark HF. Gene signatures reflect the marked heterogeneity of tissue-resident macrophages. Immunol Cell Biol 2008;86:246-254.
65. Okabe Y, Medzhitov R. Tissue-specific signals control reversible program of localization and functional polarization of macrophages. Cell 2014;157:832-844.
66. Tontonoz P, Spiegelman BM. Fat and beyond: the diverse biology of PPARgamma. Annu Rev Biochem 2008;77:289-312.
67. Glass CK, Ogawa S. Combinatorial roles of nuclear receptors in inflammation and immunity. Nat Rev Immunol 2006;6:44-55.
68. Baker AD, et al. Targeted PPAR{gamma} deficiency in alveolar macrophages disrupts surfactant catabolism. J Lipid Res 2010;51:1325-1331.
69. Gautier EL, et al. Systemic analysis of PPARgamma in mouse macrophage populations reveals marked diversity in expression with critical roles in resolution of inflammation and airway immunity. J Immunol 2012;189:2614-2624.
70. Spann NJ, et al. Regulated accumulation of desmosterol integrates macrophage lipid metabolism and inflammatory responses. Cell 2012;151:138-152.
71. Culver DA, et al. Peroxisome proliferator-activated receptor gamma activity is deficient in alveolar macrophages in pulmonary sarcoidosis. Am J Respir Cell Mol Biol 2004;30:1-5.
72. Bonfield TL, et al. Peroxisome proliferator-activated receptor-gamma is deficient in alveolar macrophages from patients with alveolar proteinosis. Am J Respir Cell Mol Biol 2003;29:677-682.
73. Andersson C, Zaman MM, Jones AB, Freedman SD. Alterations in immune response and PPAR/LXR regulation in cystic fibrosis macrophages. J Cyst Fibros 2008;7:68-78.
74. Koutsourakis M, Langeveld A, Patient R, Beddington R, Grosveld F. The transcription factor GATA6 is essential for early extraembryonic development. Development 1999;126:723-732.
75. Duncan SA. Generation of embryos directly from embryonic stem cells by tetraploid embryo complementation reveals a role for GATA factors in organogenesis. Biochem Soc Trans 2005;33:1534-1536.
76. Whissell G, et al. The transcription factor GATA6 enables self-renewal of colon adenoma stem cells by repressing BMP gene expression. Nat Cell Biol 2014;16:695-707.
77. Sulahian R, et al. An integrative analysis reveals functional targets of GATA6 transcriptional regulation in gastric cancer. Oncogene 2013. doi: 10.1038/onc.2013.517. [Epub ahead of print].
78. Lin L, et al. Activation of GATA binding protein 6 (GATA6) sustains oncogenic lineage-survival in esophageal adenocarcinoma. Proc Natl Acad Sci USA 2012;109:4251-4256.
79. Zhuang Y, Faria TN, Chambon P, Gudas LJ. Identification and characterization of retinoic acid receptor beta2 target genes in F9 teratocarcinoma cells. Mol Cancer Res 2003;1:619-630.
80. Rosas M, et al. The transcription factor Gata6 links tissue macrophage phenotype and proliferative renewal. Science 2014;344:645-648.
81. Francis JS, Strande L, Markov V, Leone P. Aspartoacylase supports oxidative energy metabolism during myelination. J Cereb Blood Flow Metab 2012;32:1725-1736.