Bone marrow-derived macrophages distinct from tissue-resident macrophages play a pivotal role in Concanavalin A-induced murine liver injury via CCR9 axis

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Amiya, Takeru ^a,b   Nakamoto, Nobuhiro ^a   Chu, Po Sung ^a   Teratani, Toshiaki ^a   Nakajima, Hideaki ^c   Fukuchi, Yumi ^d   Taniki, Nobuhito ^a   Yamaguchi, Akihiro ^a   Shiba, Shunsuke ^a   Miyake, Rei ^a   Katayama, Tadashi ^a   Ebinuma, Hirotoshi ^a   Kanai, Takanori ^a  

^a KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b MITSUBISHI TANABE PHARMA CORPORATION   (Japan)

^c YOKOHAMA CITY UNIVERSITY   (Japan)

^d HOSHI UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CC CHEMOKINE RECEPTOR 9; CD11B ANTIGEN; CHEMOKINE RECEPTOR CCR; CONCANAVALIN A; IMMUNOLOGIC FACTOR;

ANIMAL; CELL DIFFERENTIATION; CELL PROLIFERATION; CHEMISTRY; CLASSIFICATION; IMMUNOLOGY; LIVER; MACROPHAGE; METABOLISM; MOUSE; PATHOLOGY; TOXIC HEPATITIS;

ANIMALS; CD11B ANTIGEN; CELL DIFFERENTIATION; CELL PROLIFERATION; CHEMICAL AND DRUG INDUCED LIVER INJURY; CONCANAVALIN A; IMMUNOLOGIC FACTORS; LIVER; MACROPHAGES; MICE; RECEPTORS, CCR;

EID: 84991340916     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep35146     Document Type: Article

References (50)

1. Thomson, A. W., Knolle, P. A. Antigen-presenting cell function in the tolerogenic liver environment. Nature reviews. Immunology 10, 753-766, doi: 10.1038/nri2858 (2010).
2. Crispe, I. N. Hepatic T cells and liver tolerance. Nature reviews. Immunology 3, 51-62, doi: 10.1038/nri981 (2003).
3. Ginhoux, F., Jung, S. Monocytes and macrophages: developmental pathways and tissue homeostasis. Nature reviews. Immunology 14, 392-404, doi: 10.1038/nri3671 (2014).
4. Yona, S. et al. Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis. Immunity 38, 79-91, doi: 10.1016/j.immuni.2012.12.001 (2013).
5. Wynn, T. A., Chawla, A., Pollard, J. W. Macrophage biology in development, homeostasis and disease. Nature 496, 445-455, doi: 10.1038/nature12034 (2013).
6. Epelman, S., Lavine, K. J., Randolph, G. J. Origin and functions of tissue macrophages. Immunity 41, 21-35, doi: 10.1016/j. immuni.2014.06.013 (2014).
7. Lavin, Y., Mortha, A., Rahman, A., Merad, M. Regulation of macrophage development and function in peripheral tissues. Nature reviews. Immunology 15, 731-744, doi: 10.1038/nri3920 (2015).
8. Lavin, Y. et al. Tissue-resident macrophage enhancer landscapes are shaped by the local microenvironment. Cell 159, 1312-1326, doi: 10.1016/j.cell.2014.11.018 (2014).
9. Gomez Perdiguero, E. et al. Tissue-resident macrophages originate from yolk-sac-derived erythro-myeloid progenitors. Nature 518, 547-551, doi: 10.1038/nature13989 (2015).
10. Hashimoto, D. et al. Tissue-resident macrophages self-maintain locally throughout adult life with minimal contribution from circulating monocytes. Immunity 38, 792-804, doi: 10.1016/j.immuni.2013.04.004 (2013).
11. Jenkins, S. J. et al. Local macrophage proliferation, rather than recruitment from the blood, is a signature of TH2 inflammation. Science 332, 1284-1288, doi: 10.1126/science.1204351 (2011).
12. Ikarashi, M. et al. Distinct development and functions of resident and recruited liver Kupffer cells/macrophages. Journal of leukocyte biology 94, 1325-1336, doi: 10.1189/jlb.0313144 (2013).
13. Zigmond, E. et al. Infiltrating monocyte-derived macrophages and resident kupffer cells display different ontogeny and functions in acute liver injury. Journal of immunology 193, 344-353, doi: 10.4049/jimmunol.1400574 (2014).
14. Pellicoro, A., Ramachandran, P., Iredale, J. P., Fallowfield, J. A. Liver fibrosis and repair: immune regulation of wound healing in a solid organ. Nature reviews. Immunology 14, 181-194, doi: 10.1038/nri3623 (2014).
15. Tacke, F., Zimmermann, H. W. Macrophage heterogeneity in liver injury and fibrosis. Journal of hepatology 60, 1090-1096, doi: 10.1016/j.jhep.2013.12.025 (2014).
16. Bain, C. C. et al. Constant replenishment from circulating monocytes maintains the macrophage pool in the intestine of adult mice. Nature immunology 15, 929-937, doi: 10.1038/ni.2967 (2014).
17. Tamoutounour, S. et al. Origins and functional specialization of macrophages and of conventional and monocyte-derived dendritic cells in mouse skin. Immunity 39, 925-938, doi: 10.1016/j.immuni.2013.10.004 (2013).
18. Davies, L. C. et al. Distinct bone marrow-derived and tissue-resident macrophage lineages proliferate at key stages during inflammation. Nature communications 4, 1886, doi: 10.1038/ncomms2877 (2013).
19. Lavine, K. J. et al. Distinct macrophage lineages contribute to disparate patterns of cardiac recovery and remodeling in the neonatal and adult heart. Proceedings of the National Academy of Sciences of the United States of America 111, 16029-16034, doi: 10.1073/pnas.1406508111 (2014).
20. 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, doi: 10.1016/j.immuni.2013.11.019 (2014).
21. Bleriot, C. et al. Liver-resident macrophage necroptosis orchestrates type 1 microbicidal inflammation and type-2-mediated tissue repair during bacterial infection. Immunity 42, 145-158, doi: 10.1016/j.immuni.2014.12.020 (2015).
22. Beattie, L. et al. Bone marrow-derived and resident liver macrophages display unique transcriptomic signatures but similar biological functions. Journal of hepatology, doi: 10.1016/j.jhep.2016.05.037 (2016).
23. Scott, C. L. et al. Bone marrow-derived monocytes give rise to self-renewing and fully differentiated Kupffer cells. Nature communications 7, 10321, doi: 10.1038/ncomms10321 (2016).
24. Schumann, J. et al. Importance of Kupffer cells for T-cell-dependent liver injury in mice. The American journal of pathology 157, 1671-1683, doi: 10.1016/S0002-9440(10)64804-3 (2000).
25. Morita, A. et al. Activated Kupffer cells play an important role in intra-hepatic Th1-associated necro-inflammation in Concanavalin A-induced hepatic injury in mice. Hepatology research: the official journal of the Japan Society of Hepatology 27, 143-150 (2003).
26. Ju, C., Tacke, F. Hepatic macrophages in homeostasis and liver diseases: from pathogenesis to novel therapeutic strategies. Cellular & molecular immunology 13, 316-327, doi: 10.1038/cmi.2015.104 (2016).
27. Miller, J. C. et al. Deciphering the transcriptional network of the dendritic cell lineage. Nature immunology 13, 888-899, doi: 10.1038/ni.2370 (2012).
28. Gautier, E. L. et al. Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nature immunology 13, 1118-1128, doi: 10.1038/ni.2419 (2012).
29. Nakamoto, N. et al. CCR9+ macrophages are required for acute liver inflammation in mouse models of hepatitis. Gastroenterology 142, 366-376, doi: 10.1053/j.gastro.2011.10.039 (2012).
30. Chu, P. S. et al. C-C motif chemokine receptor 9 positive macrophages activate hepatic stellate cells and promote liver fibrosis in mice. Hepatology 58, 337-350, doi: 10.1002/hep.26351 (2013).
31. Seki, E. et al. CCR1 and CCR5 promote hepatic fibrosis in mice. Journal of Clinical Investigation, doi: 10.1172/jci37444 (2009).
32. Seki, E. et al. CCR2 promotes hepatic fibrosis in mice. Hepatology 50, 185-197, doi: 10.1002/hep.22952 (2009).
33. Heymann, F. et al. Hepatic macrophage migration and differentiation critical for liver fibrosis is mediated by the chemokine receptor C-C motif chemokine receptor 8 in mice. Hepatology 55, 898-909, doi: 10.1002/hep.24764 (2012).
34. Swirski, F. K. et al. Identification of splenic reservoir monocytes and their deployment to inflammatory sites. Science 325, 612-616, doi: 10.1126/science.1175202 (2009).
35. Davies, L. C., Jenkins, S. J., Allen, J. E., Taylor, P. R. Tissue-resident macrophages. Nature immunology 14, 986-995, doi: 10.1038/ni.2705 (2013).
36. Hettinger, J. et al. Origin of monocytes and macrophages in a committed progenitor. Nature immunology 14, 821-830, doi: 10.1038/ni.2638 (2013).
37. Rosas, M., Thomas, B., Stacey, M., Gordon, S., Taylor, P. R. The myeloid 7/4-antigen defines recently generated inflammatory macrophages and is synonymous with Ly-6B. Journal of leukocyte biology 88, 169-180, doi: 10.1189/jlb.0809548 (2010).
38. Luedde, T., Schwabe, R. F. NF-kappaB in the liver-linking injury, fibrosis and hepatocellular carcinoma. Nature reviews. Gastroenterology & hepatology 8, 108-118, doi: 10.1038/nrgastro.2010.213 (2011).
39. Marra, F., Tacke, F. Roles for chemokines in liver disease. Gastroenterology 147, 577-594 e571, doi: 10.1053/j.gastro.2014.06.043 (2014).
40. Saiman, Y., Friedman, S. L. The role of chemokines in acute liver injury. Frontiers in physiology 3, 213, doi: 10.3389/fphys.2012.00213 (2012).
41. Tacke, F. Functional role of intrahepatic monocyte subsets for the progression of liver inflammation and liver fibrosis in vivo. Fibrogenesis & tissue repair 5, S27, doi: 10.1186/1755-1536-5-S1-S27 (2012).
42. Serbina, N. V., Pamer, E. G. Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR2. Nature immunology 7, 311-317, doi: 10.1038/ni1309 (2006).
43. Gressner, A. M., Weiskirchen, R. Modern pathogenetic concepts of liver fibrosis suggest stellate cells and TGF-beta as major players and therapeutic targets. Journal of cellular and molecular medicine 10, 76-99 (2006).
44. Aoyama, T., Paik, Y. H., Seki, E. Toll-like receptor signaling and liver fibrosis. Gastroenterology research and practice 2010, doi: 10.1155/2010/192543 (2010).
45. Fujita, T. et al. Hepatic stellate cells relay inflammation signaling from sinusoids to parenchyma in mouse models of immunemediated hepatitis. Hepatology, doi: 10.1002/hep.28112 (2015).
46. Higashi, N., Senoo, H. Distribution of vitamin A-storing lipid droplets in hepatic stellate cells in liver lobules-a comparative study. The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology 271, 240-248, doi: 10.1002/ar.a.10036 (2003).
47. Lee, Y. S. et al. Blockade of Retinol Metabolism Protects T Cell-Induced Hepatitis by Increasing Migration of Regulatory T Cells. Molecules and cells 38, 998-1006, doi: 10.14348/molcells.2015.0218 (2015).
48. Iwata, M. et al. Retinoic acid imprints gut-homing specificity on T cells. Immunity 21, 527-538, doi: 10.1016/j.immuni.2004.08.011 (2004).
49. Ohoka, Y., Yokota, A., Takeuchi, H., Maeda, N., Iwata, M. Retinoic acid-induced CCR9 expression requires transient TCR stimulation and cooperativity between NFATc2 and the retinoic acid receptor/retinoid X receptor complex. Journal of immunology 186, 733-744, doi: 10.4049/jimmunol.1000913 (2011).
50. Nakamura, Y. et al. CCR2 knockout exacerbates cerulein-induced chronic pancreatitis with hyperglycemia via decreased GLP-1 receptor expression and insulin secretion. American journal of physiology. Gastrointestinal and liver physiology 304, G700-G707, doi: 10.1152/ajpgi.00318.2012 (2013).