Self-renewing resident arterial macrophages arise from embryonic CX3CR1 + precursors and circulating monocytes immediately after birth

Nature Immunology

Volumn 17, Issue 2, 2016, Pages 159-168

  Ensan, Sherine ^a   Li, Angela ^a   Besla, Rickvinder ^a   Degousee, Norbert ^b   Cosme, Jake ^b   Roufaiel, Mark ^b   Shikatani, Eric A ^a   El Maklizi, Mahmoud ^a   Williams, Jesse W ^c   Robins, Lauren ^b   Li, Cedric ^b   Lewis, Bonnie ^b   Yun, Tae Jin ^d   Lee, Jun Seong ^d   Wieghofer, Peter ^e   Khattar, Ramzi ^b   Farrokhi, Kaveh ^a   Byrne, John ^b,i   Ouzounian, Maral ^b,i   Zavitz, Caleb C J ^b   Levy, Gary A ^a,b   Bauer, Carla M T ^f   Libby, Peter ^g   Husain, Mansoor ^a,b,i   Swirski, Filip K ^h   Cheong, Cheolho ^d   Prinz, Marco ^e   Hilgendorf, Ingo ^e   Randolph, Gwendalyn J ^c   Epelman, Slava ^a,b,i   Gramolini, Anthony O ^a,b,i   Cybulsky, Myron I ^a,b,i   Rubin, Barry B ^b,i   Robbins, Clinton S ^a,b,i   more..

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY HEALTH NETWORK   (Canada)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

^e UNIVERSITY OF FREIBURG   (Germany)

^f HOFFMANN LA ROCHE INC   (United States)

^g BRIGHAM AND WOMEN S HOSPITAL   (United States)

^h MASSACHUSETTS GENERAL HOSPITAL   (United States)

ⁱ UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CX3CR1; FRACTALKINE; PROTEIN PRECURSOR; CHEMOKINE RECEPTOR; CX3CR1 PROTEIN, MOUSE; PROTEIN BINDING; TRANSCRIPTOME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; BONE MARROW DERIVED MONOCYTE; CELL SELF-RENEWAL; CELL SURVIVAL; CONTROLLED STUDY; EMBRYO; GENE EXPRESSION PROFILING; HOMEOSTASIS; MACROPHAGE; MONOCYTE; MOUSE; NEWBORN; NONHUMAN; PERINATAL PERIOD; PHENOTYPE; PRIORITY JOURNAL; SEPSIS; STEADY STATE; ANIMAL; CLUSTER ANALYSIS; CYTOLOGY; EMBRYONIC STEM CELL; FEMALE; IMMUNOLOGY; IMMUNOPHENOTYPING; MALE; METABOLISM; MICROBIOLOGY; STEM CELL NICHE; TRANSGENIC MOUSE;

ANIMALS; CELL SELF RENEWAL; CELL SURVIVAL; CHEMOKINE CX3CL1; CLUSTER ANALYSIS; EMBRYONIC STEM CELLS; FEMALE; GENE EXPRESSION PROFILING; IMMUNOPHENOTYPING; MACROPHAGES; MALE; MICE; MICE, TRANSGENIC; MONOCYTES; PHENOTYPE; PROTEIN BINDING; RECEPTORS, CHEMOKINE; STEM CELL NICHE; TRANSCRIPTOME;

EID: 84955129407     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.3343     Document Type: Article

References (49)

1. Akazaki, K. A concept of reticuloendothelial system. Tohoku J. Exp. Med. 76, 107-118 (1962).
2. Naito, M., Yamamura, F., Nishikawa, S. & Takahashi, K. Development, differentiation, and maturation of fetal mouse yolk sac macrophages in cultures. J. Leukoc. Biol. 46, 1-10 (1989).
3. van Furth, R. & Cohn, Z. A. The origin and kinetics of mononuclear phagocytes. J. Exp. Med. 128, 415-435 (1968).
4. Samokhvalov, I. M., Samokhvalova, N. I. & Nishikawa, S. Cell tracing shows the contribution of the yolk sac to adult haematopoiesis. Nature 446, 1056-1061 (2007).
5. Ginhoux, F. et al. Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science 330, 841-845 (2010).
6. Schulz, C. et al. A lineage of myeloid cells independent of Myb and hematopoietic stem cells. Science 336, 86-90 (2012).
7. Hoeffel, G. et al. Adult Langerhans cells derive predominantly from embryonic fetal liver monocytes with a minor contribution of yolk sac-derived macrophages. J. Exp. Med. 209, 1167-1181 (2012).
8. Epelman, S. et al. Embryonic and adult-derived resident cardiac macrophages are maintained through distinct mechanisms at steady state and during inflammation. Immunity 40, 91-104 (2014).
9. Molawi, K. et al. Progressive replacement of embryo-derived cardiac macrophages with age. J. Exp. Med. 211, 2151-2158 (2014).
10. Hoeffel, G. et al. C-myb+ erythro-myeloid progenitor-derived fetal monocytes give rise to adult tissue-resident macrophages. Immunity 42, 665-678 (2015).
11. Gomez Perdiguero, E. et al. Tissue-resident macrophages originate from yolk-sac-derived erythro-myeloid progenitors. Nature 518, 547-551 (2015).
12. Hashimoto, D. et al. Tissue-resident macrophages self-maintain locally throughout adult life with minimal contribution from circulating monocytes. Immunity 38, 792-804 (2013).
13. Yona, S. et al. Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis. Immunity 38, 79-91 (2013).
14. Gautier, E. L. et al. Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nat. Immunol. 13, 1118-1128 (2012).
15. Majesky, M. W., Dong, X. R., Hoglund, V., Mahoney, W. M. J. & Daum, G. The adventitia: A dynamic interface containing resident progenitor cells. Arterioscler. Thromb. Vasc. Biol. 31, 1530-1539 (2011).
16. Jakubzick, C. et al. Minimal differentiation of classical monocytes as they survey steady-state tissues and transport antigen to lymph nodes. Immunity 39, 599-610 (2013).
17. Meredith, M. M. et al. Expression of the zinc finger transcription factor zDC (Zbtb46, Btbd4) defines the classical dendritic cell lineage. J. Exp. Med. 209, 1153-1165 (2012).
18. Satpathy, A. T. et al. Zbtb46 expression distinguishes classical dendritic cells and their committed progenitors from other immune lineages. J. Exp. Med. 209, 1135-1152 (2012).
19. McGovern, N. et al. Human dermal CD14+ cells are a transient population of monocyte-derived macrophages. Immunity 41, 465-477 (2014).
20. Galkina, E. et al. Lymphocyte recruitment into the aortic wall before and during development of atherosclerosis is partially l-selectin dependent. J. Exp. Med. 203, 1273-1282 (2006).
21. Choi, J. H. et al. Identification of antigen-presenting dendritic cells in mouse aorta and cardiac valves. J. Exp. Med. 206, 497-505 (2009).
22. Choi, J. H. et al. Flt3 signaling-dependent dendritic cells protect against atherosclerosis. Immunity 35, 819-831 (2011).
23. 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. 210, 1977-1992 (2013).
24. Medvinsky, A. & Dzierzak, E. Definitive hematopoiesis is autonomously initiated by the AGM region. Cell 86, 897-906 (1996).
25. Parkhurst, C. N. et al. Microglia promote learning-dependent synapse formation through brain-derived neurotrophic factor. Cell 155, 1596-1609 (2013).
26. Prinz, M. & Priller, J. Microglia and brain macrophages in the molecular age: from origin to neuropsychiatric disease. Nat. Rev. Neurosci. 15, 300-312 (2014).
27. Karsunky, H., Merad, M., Cozzio, A., Weissman, I. L. & Manz, M. G. Flt3 ligand regulates dendritic cell development from Flt3+ lymphoid and myeloid-committed progenitors to Flt3+ dendritic cells in vivo. J. Exp. Med. 198, 305-313 (2003).
28. Bain, C. C. et al. Constant replenishment from circulating monocytes maintains the macrophage pool in the intestine of adult mice. Nat. Immunol. 15, 929-937 (2014).
29. Davies, L. C., Jenkins, S. J., Allen, J. E. & Taylor, P. R. Tissue-resident macrophages. Nat. Immunol. 14, 986-995 (2013).
30. Ginhoux, F. & Jung, S. Monocytes and macrophages: developmental pathways and tissue homeostasis. Nat. Rev. Immunol. 14, 392-404 (2014).
31. Kim, K. W. et al. In vivo structure/function and expression analysis of the CX3C chemokine fractalkine. Blood 118, e156-e167 (2011).
32. Serbina, N. V. & Pamer, E G. Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR2. Nat. Immunol. 7, 311-317 (2006).
33. Robbins, C. S. et al. Local proliferation dominates lesional macrophage accumulation in atherosclerosis. Nat. Med. 19, 1166-1172 (2013).
34. Goldmann, T. et al. A new type of microglia gene targeting shows TAK1 to be pivotal in CNS autoimmune inflammation. Nat. Neurosci. 16, 1618-1626 (2013).
35. Foudi, A. et al. Analysis of histone 2B-GFP retention reveals slowly cycling hematopoietic stem cells. Nat. Biotechnol. 27, 84-90 (2009).
36. Mildner, A. et al. Microglia in the adult brain arise from Ly-6ChiCCR2+ monocytes only under defined host conditions. Nat. Neurosci. 10, 1544-1553 (2007).
37. Ajami, B., Bennett, J. L., Krieger, C., Tetzlaff, W. & Rossi, F. M. Local self-renewal can sustain CNS microglia maintenance and function throughout adult life. Nat. Neurosci. 10, 1538-1543 (2007).
38. Sieweke, M. H. & Allen, J. E. Beyond stem cells: self-renewal of differentiated macrophages. Science 342, 1242974 (2013).
39. Barth, M. W., Hendrzak, J. A., Melnicoff, M. J. & Morahan, P. S. Review of the macrophage disappearance reaction. J. Leukoc. Biol. 57, 361-367 (1995).
40. Kierdorf, K. et al. Microglia emerge from erythromyeloid precursors via Pu. 1-and Irf8-dependent pathways. Nat. Neurosci. 16, 273-280 (2013).
41. Chorro, L. et al. Langerhans cell (LC) proliferation mediates neonatal development, homeostasis, and inflammation-associated expansion of the epidermal LC network. J. Exp. Med. 206, 3089-3100 (2009).
42. Boehme, S. A., Lio, F. M., Maciejewski-Lenoir, D., Bacon, K. B. & Conlon, P. J. The chemokine fractalkine inhibits Fas-mediated cell death of brain microglia. J. Immunol. 165, 397-403 (2000).
43. Lionakis, M. S. et al. CX3CR1-dependent renal macrophage survival promotes Candida control and host survival. J. Clin. Invest. 123, 5035-5051 (2013).
44. Zheng, J. et al. Chemokine receptor CX3CR1 contributes to macrophage survival in tumor metastasis. Mol. Cancer 12, 141 (2013).
45. Landsman, L. et al. CX3CR1 is required for monocyte homeostasis and atherogenesis by promoting cell survival. Blood 113, 963-972 (2009).
46. Gautier, E. L. et al. Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nat. Immunol. 13, 1118-1128 (2012).
47. Jongstra-Bilen, J. et al. Low-grade chronic inflammation in regions of the normal mouse arterial intima predisposed to atherosclerosis. J. Exp. Med. 203, 2073-2083 (2006).
48. Paulson, K. E. et al. Resident intimal dendritic cells accumulate lipid and contribute to the initiation of atherosclerosis. Circ. Res. 106, 383-390 (2010).
49. Carvalho, B. S. & Irizarry, R. A. A framework for oligonucleotide microarray preprocessing. Bioinformatics 26, 2363-2367 (2010).