Tissue-specific differentiation of colonic macrophages requires TGFβ receptor-mediated signaling

Mucosal Immunology

Volumn 10, Issue 6, 2017, Pages 1387-1399

  Schridde, A ^a,b,c   Bain, C C ^a   Mayer, J U ^a   Montgomery, J ^a   Pollet, E ^d   Denecke, B ^c   Milling, S W F ^a   Jenkins, S J ^e   Dalod, M ^d   Henri, S ^d   Malissen, B ^d   Pabst, O ^b,c   McL Mowat, A ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b HANNOVER MEDICAL SCHOOL   (Germany)

^c RWTH AACHEN UNIVERSITY   (Germany)

^d CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

^e UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 10; LY ANTIGEN; LY-6C ANTIGEN, MOUSE; TRANSCRIPTOME; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR;

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; FEMALE; GENE; GENE FUNCTION; GENETIC ANALYSIS; GENETIC IDENTIFICATION; INTESTINE MUCOSA; MACROPHAGE; MALE; MONOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TGFBR GENE; TGFBR1 GENE; TGFBR2 GENE; TISSUE DIFFERENTIATION; UPREGULATION; ANIMAL; ANTIBODY SPECIFICITY; C57BL MOUSE; CELL CULTURE; COLON; GENE EXPRESSION PROFILING; GENETICS; HOMEOSTASIS; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; TUMOR MICROENVIRONMENT;

ANIMALS; ANTIGENS, LY; CELL DIFFERENTIATION; CELLS, CULTURED; CELLULAR MICROENVIRONMENT; COLON; FEMALE; GENE EXPRESSION PROFILING; HOMEOSTASIS; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MONOCYTES; ORGAN SPECIFICITY; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SIGNAL TRANSDUCTION; TRANSCRIPTOME; TRANSFORMING GROWTH FACTOR BETA;

EID: 85020925080     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2016.142     Document Type: Article

References (64)

1. Perdiguero, E. G. & Geissmann, F. The development and maintenance of resident macrophages. Nat. Immunol. 17, 2-8 (2015).
2. Okabe, Y. & Medzhitov, R. Tissue biology perspective on macrophages. Nat. Immunol. 17, 9-17 (2016).
3. Ginhoux, F. & Guilliams, M. Tissue-resident macrophage ontogeny and homeostasis. Immunity 44, 439-449 (2016).
4. Gomez Perdiguero, E. et al. Tissue-resident macrophages originate from yolk-sac-derived erythro-myeloid progenitors. Nature 518, 547-551 (2015).
5. Hoeffel, G. et al. C-Myb() erythro-myeloid progenitor-derived fetal monocytes give rise to adult tissue-resident macrophages. Immunity 42, 665-678 (2015).
6. Sheng, J., Ruedl, C. & Karjalainen, K. Most tissue-resident macrophages except microglia are derived from fetal hematopoietic stem cells. Immunity 43, 382-393 (2015).
7. 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).
8. Bain, C. C. et al. Resident and pro-inflammatory macrophages in the colon represent alternative context-dependent fates of the same Ly6Chi monocyte precursors. Mucosal Immunol. 6, 498-510 (2013).
9. Bain, C. C. et al. Constant replenishment from circulating monocytes maintains themacrophage pool in the intestine of adult mice.Nat. Immunol. 15, 929-937 (2014).
10. 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 (2013).
11. 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).
12. Molawi, K. et al. Progressive replacement of embryo-derived cardiac macrophages with age. J. Exp. Med. 211, 2151-2158 (2014).
13. Heidt, T. et al. Differential contribution ofmonocytes to heartmacrophages in steady-stateandaftermyocardial infarction. Circ. Res. 115, 284-295 (2014).
14. Bain, C. C. et al. Long-lived self-renewing bone marrow-derived macrophages displace embryo-derived cells to inhabit adult serous cavities. Nat. Commun. 7, ncomms11852 (2016).
15. Lavin, Y. et al. Tissue-resident macrophage enhancer landscapes are shaped by the local microenvironment. Cell 159, 1312-1326 (2014).
16. van de Laar, L. et al. Yolk sac macrophages, fetal liver, and adultmonocytes can colonize an empty niche and develop into functional tissue-resident macrophages. Immunity 44, 755-768 (2016).
17. Lee, S. H., Starkey, P. M. & Gordon, S. Quantitative analysis of total macrophage content in adult mouse tissues. Immunochemical studieswithmonoclonal antibody F4/80. J. Exp.Med. 161, 475-489 (1985).
18. Tamoutounour, S. et al. CD64 distinguishes macrophages from dendritic cells in the gut and reveals the Th1-inducing role of mesenteric lymph node macrophages during colitis. Eur. J. Immunol. 42, 3150-3166 (2012).
19. Smythies, L. E. et al. Inflammation anergy in human intestinal macrophages is due to Smad-induced IkappaBalpha expression and NF-kappaB inactivation. J. Biol. Chem. 285, 19593-19604 (2010).
20. Platt, A. M., Bain, C. C., Bordon, Y., Sester, D. P. & Mowat, A. M. An independent subset of TLR expressing CCR2-dependent macrophages promotes colonic inflammation. J. Immunol. 184, 6843-6854 (2010).
21. Zigmond, E. et al. Ly6C hi monocytes in the inflamed colon give rise to proinflammatory effector cells and migratory antigen-presenting cells. Immunity 37, 1076-1090 (2012).
22. Okabe, Y. & Medzhitov, R. Tissue-specific signals control reversible program of localization and functional polarization of macrophages. Cell 157, 832-844 (2014).
23. Schneider, C. et al. Induction of the nuclear receptor PPAR-g by the cytokine GM-CSF is critical for the differentiation of fetal monocytes into alveolar macrophages. Nat. Immunol. 15, 1026-1037 (2014).
24. 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).
25. Asano, K. et al. Intestinal CD169() macrophages initiate mucosal inflammation by secreting CCL8 that recruits inflammatory monocytes. Nat. Commun. 6, 7802 (2015).
26. Butovsky, O. et al. Identification of a unique TGF-b-dependent molecular and functional signature in microglia. Nat. Neurosci. 17, 131-143 (2014).
27. Rivollier, A., He, J., Kole, A., Valatas, V. & Kelsall, B. L. Inflammation switches the differentiation program of Ly6Chi monocytes from antiinflammatory macrophages to inflammatory dendritic cells in the colon. J. Exp. Med. 209, 139-155 (2012).
28. Zigmond, E. et al. Macrophage-restricted interleukin-10 receptor deficiency, but not IL-10 deficiency, causes severe spontaneous colitis. Immunity 40, 720-733 (2014).
29. Shouval, D. S. et al. Interleukin-10 receptor signaling in innate immune cells regulates mucosal immune tolerance and anti-inflammatory macrophage function. Immunity 40, 706-719 (2014).
30. Hoshi,N. et al. MyD88 signalling in colonic mononuclear phagocytes drives colitis in IL-10-deficient mice. Nat. Commun. 3, 1120 (2012).
31. Girard-Madoux, M. J. H. et al. IL-10 control of CD11c myeloid cells is essential to maintain immune homeostasis in the small and large intestine. Oncotarget 7, 32015-32030 (2016).
32. Maheshwari, A. et al. TGF-beta2 suppresses macrophage cytokine production and mucosal inflammatory responses in the developing intestine. Gastroenterology 140, 242-253 (2011).
33. 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).
34. Ruggiero, L., Connor, M. P., Chen, J., Langen, R. & Finnemann, S. C. Diurnal, localized exposure of phosphatidylserine by rod outer segment tips in wild-type but not Itgb5-/- or Mfge8-/- mouse retina. Proc. Natl. Acad. Sci. USA 109, 8145-8148 (2012).
35. Lacy-Hulbert, A. et al. Ulcerative colitis and autoimmunity induced by loss of myeloid alphav integrins. Proc. Natl. Acad. Sci. USA 104, 15823-15828 (2007).
36. Bauer, T. et al. Identification of Axl as a downstream effector of TGF-b1 during Langerhans cell differentiation and epidermal homeostasis. J. Exp. Med. 209, 2033-2047 (2012).
37. Morton, P. E. et al. TNFa promotes CAR-dependent migration of leukocytes across epithelial monolayers. Sci. Rep. 6, 26321 (2016).
38. Niess, J. H. et al. CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science 307, 254-258 (2005).
39. Chieppa, M., Rescigno, M., Huang, A. Y. & Germain, R. N. Dynamic imaging of dendritic cell extension into the small bowel lumen in response to epithelial cell TLR engagement. J. Exp. Med. 203, 2841-2852 (2006).
40. Garlanda, C., Riva, F., Bonavita, E. & Mantovani, A. Negative regulatory receptors of the IL-1 family. Semin. Immunol. 25, 408-415 (2013).
41. Huber, S. et al. IL-22BP is regulated by the inflammasome and modulates tumorigenesis in the intestine. Nature 491, 259-263 (2012).
42. Dinarello,C. A., Novick, D.,Kim,S. & Kaplanski, G. Interleukin-18 and IL-18 binding protein. Front. Immunol. 4, 289 (2013).
43. Yang, J. et al. The novel costimulatory programmed death ligand 1/B7.1 pathway is functional in inhibiting alloimmune responses in vivo. J. Immunol. 187, 1113-1119 (2011).
44. Varol, C. et al. Intestinal lamina propria dendritic cell subsets have different origin and functions. Immunity 31, 502-512 (2009).
45. Jarry, A., Bossard, C., Sarrabayrouse, G., Mosnier, J.-F. & Laboisse, C. L. Loss of interleukin-10 or transforming growth factor b signaling in the human colon initiates a T-helper 1 response via distinct pathways. Gastroenterology 141, 1887-96.e1-2 (2011).
46. Rosas, M. et al. The transcription factor Gata6 links tissue macrophage phenotype and proliferative renewal. Science 344, 645-648 (2014).
47. Gautier, E. L. et al. Gata6 regulates aspartoacylase expression in resident peritoneal macrophages and controls their survival. J. Exp. Med 211, 1525-1531 (2014).
48. A-Gonzalez, N. et al. The nuclear receptor LXRa controls the functional specialization of splenic macrophages. Nat. Immunol. 14, 831-839 (2013).
49. Lavin, Y., Mortha, A., Rahman, A. & Merad, M. Regulation of macrophage development and function in peripheral tissues. Nat. Rev. 15, 731-744 (2015).
50. Fainaru, O. et al. Runx3 regulates mouse TGF-beta-mediated dendritic cell function and its absence results in airway inflammation. EMBO J. 23, 969-979 (2004).
51. Brenner, O. et al. Loss of Runx3 function in leukocytes is associated with spontaneously developed colitis and gastric mucosal hyperplasia. Proc. Natl. Acad. Sci. USA 101, 16016-16021 (2004).
52. Chopin, M. et al. Langerhans cells are generated by two distinct PU.1-dependent transcriptional networks. J. Exp. Med. 210, 2967-2980 (2013).
53. Schlitzer, A. et al. IRF4 transcription factor-dependent CD11b dendritic cells in human and mouse control mucosal IL-17 cytokine responses. Immunity 38, 970-983 (2013).
54. Ishifune, C. et al. Differentiation of CD11c CX3CR1 cells in the small intestine requires Notch signaling. Proc. Natl. Acad. Sci. USA 111, 5986-5991 (2014).
55. Klebanoff, C. A. et al. Retinoic acid controls the homeostasis of pre-cDCderived splenic and intestinal dendritic cells. J. Exp. Med. 210, 1961-1976 (2013).
56. Ueda, Y. et al. Commensal microbiota induce LPS hyporesponsiveness in colonic macrophages via the production of IL-10. Int. Immunol. 22, 953-962 (2010).
57. Jung, S. et al. Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol. Cell Biol. 20, 4106-4114 (2000).
58. Kel, J. M.,Girard-Madoux, M. J. H., Reizis, B. & Clausen, B. E. TGF-beta is required to maintain the pool of immature Langerhans cells in the epidermis. J. Immunol. 185, 3248-3255 (2010).
59. Caton, M. L., Smith-Raska, M. R. & Reizis, B. Notch-RBP-J signaling controls the homeostasis of CD8-dendritic cells in the spleen. J. Exp. Med. 204, 1653-1664 (2007).
60. Larsson, J. et al. Abnormal angiogenesis but intact hematopoietic potential in TGF-beta type I receptor-deficient mice. EMBO J. 20, 1663-1673 (2001).
61. Boring, L. et al. Impaired monocyte migration and reduced type 1 (Th1) cytokine responses in C-C chemokine receptor 2 knockout mice. J. Clin. Invest. 100, 2552-2561 (1997).
62. Bain, C. C. & Mowat, A. M. CD200 receptor and macrophage function in the intestine. Immunobiology 217, 643-651 (2011).
63. Henri, S. et al. CD207 CD103 dermal dendritic cells cross-present keratinocyte-derived antigens irrespective of the presence of Langerhans cells. J. Exp. Med. 207, 189-206 (2010).
64. Wang, J., Duncan, D., Shi, Z. & Zhang, B. WEB-based GEne SeT AnaLysis Toolkit (WebGestalt): update 2013. Nucleic Acids Res. 41,W77-W83 (2013).