The Heterogeneity of Ly6Chi Monocytes Controls Their Differentiation into iNOS+ Macrophages or Monocyte-Derived Dendritic Cells

Immunity

Volumn 45, Issue 6, 2016, Pages 1205-1218

  Menezes, Shinelle ^a,b   Melandri, Daisy ^a,b   Anselmi, Giorgio ^a,b   Perchet, Thibaut ^c   Loschko, Jakob ^d   Dubrot, Juan ^e   Patel, Rajen ^a,b   Gautier, Emmanuel L ^f   Hugues, Stéphanie ^e   Longhi, M Paula ^g   Henry, Jake Y ^h   Quezada, Sergio A ^h   Lauvau, Grégoire ⁱ   Lennon Duménil, Ana Maria ^j   Gutiérrez Martínez, Enrique ^a,b   Bessis, Alain ^k   Gomez Perdiguero, Elisa ^c   Jacome Galarza, Christian E ^l   Garner, Hannah ^l   Geissmann, Frederic ^l   Golub, Rachel ^c   Nussenzweig, Michel C ^d   Guermonprez, Pierre ^a,b   more..

^a KING'S COLLEGE LONDON   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c INSTITUT PASTEUR   (France)

^d ROCKEFELLER UNIVERSITY   (United States)

^e UNIVERSITY OF GENEVA   (Switzerland)

^f PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^g QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^h UNIVERSITY COLLEGE LONDON   (United Kingdom)

ⁱ ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^j INSTITUT CURIE   (France)

^k ECOLE NORMALE SUPÉRIEURE   (France)

^l MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

more..

Author keywords

GM CSF; macrophages; monocyte derived dendritic cells; monocytes; PU.1 transcription factor

Indexed keywords

CD209 ANTIGEN; CHEMOKINE RECEPTOR CCR2; FC RECEPTOR; FLT3 LIGAND; GLYCOPROTEIN P 15095; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INDUCIBLE NITRIC OXIDE SYNTHASE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; NUCLEAR RECEPTOR NUR77; PROGRAMMED DEATH 1 LIGAND 2; TRANSCRIPTION FACTOR PU 1; LY ANTIGEN; LY-6C ANTIGEN, MOUSE; NOS2 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DIFFERENTIATION; CELL FATE; CELL LINEAGE; CELL POLARITY; CONTROLLED STUDY; DENDRITIC CELL; GENE; GENETIC TRANSCRIPTION; HAPLOINSUFFICIENCY; INFLAMMATION; LISTERIA MONOCYTOGENES; MACROPHAGE; MONOCYTE; MONOCYTE DERIVED DENDRITIC CELL; MOUSE; NONHUMAN; PHAGOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SFPI1 GENE; STEM CELL; ADOPTIVE TRANSFER; ANIMAL; CELL SEPARATION; CYTOLOGY; DNA MICROARRAY; FLOW CYTOMETRY; IMMUNOLOGY; POLYMERASE CHAIN REACTION;

ADOPTIVE TRANSFER; ANIMALS; ANTIGENS, LY; CELL DIFFERENTIATION; CELL SEPARATION; DENDRITIC CELLS; FLOW CYTOMETRY; MACROPHAGES; MICE; MONOCYTES; NITRIC OXIDE SYNTHASE TYPE II; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; POLYMERASE CHAIN REACTION;

EID: 85006819029     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2016.12.001     Document Type: Article

References (62)

1. Auffray, C., Fogg, D., Garfa, M., Elain, G., Join-Lambert, O., Kayal, S., Sarnacki, S., Cumano, A., Lauvau, G., Geissmann, F., Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior. Science 317 (2007), 666–670.
2. Bain, C.C., Scott, C.L., Uronen-Hansson, H., Gudjonsson, S., Jansson, O., Grip, O., Guilliams, M., Malissen, B., Agace, W.W., Mowat, A.M., Resident and pro-inflammatory macrophages in the colon represent alternative context-dependent fates of the same Ly6Chi monocyte precursors. Mucosal Immunol. 6 (2013), 498–510.
3. Bakri, Y., Sarrazin, S., Mayer, U.P., Tillmanns, S., Nerlov, C., Boned, A., Sieweke, M.H., Balance of MafB and PU.1 specifies alternative macrophage or dendritic cell fate. Blood 105 (2005), 2707–2716.
4. Barthélémy, O., Degrell, P., Berman, E., Kerneis, M., Petroni, T., Silvain, J., Payot, L., Choussat, R., Collet, J.P., Helft, G., et al. Sex-related differences after contemporary primary percutaneous coronary intervention for ST-segment elevation myocardial infarction. Arch. Cardiovasc. Dis. 108 (2015), 428–436.
5. Brass, A.L., Zhu, A.Q., Singh, H., Assembly requirements of PU.1-Pip (IRF-4) activator complexes: inhibiting function in vivo using fused dimers. EMBO J. 18 (1999), 977–991.
6. Breton, G., Lee, J., Zhou, Y.J., Schreiber, J.J., Keler, T., Puhr, S., Anandasabapathy, N., Schlesinger, S., Caskey, M., Liu, K., Nussenzweig, M.C., Circulating precursors of human CD1c+ and CD141+ dendritic cells. J. Exp. Med. 212 (2015), 401–413.
7. Carlin, L.M., Stamatiades, E.G., Auffray, C., Hanna, R.N., Glover, L., Vizcay-Barrena, G., Hedrick, C.C., Cook, H.T., Diebold, S., Geissmann, F., Nr4a1-dependent Ly6C(low) monocytes monitor endothelial cells and orchestrate their disposal. Cell 153 (2013), 362–375.
8. Carotta, S., Dakic, A., D'Amico, A., Pang, S.H., Greig, K.T., Nutt, S.L., Wu, L., The transcription factor PU.1 controls dendritic cell development and Flt3 cytokine receptor expression in a dose-dependent manner. Immunity 32 (2010), 628–641.
9. Cheong, C., Matos, I., Choi, J.H., Dandamudi, D.B., Shrestha, E., Longhi, M.P., Jeffrey, K.L., Anthony, R.M., Kluger, C., Nchinda, G., et al. Microbial stimulation fully differentiates monocytes to DC-SIGN/CD209(+) dendritic cells for immune T cell areas. Cell 143 (2010), 416–429.
10. Dakic, A., Metcalf, D., Di Rago, L., Mifsud, S., Wu, L., Nutt, S.L., PU.1 regulates the commitment of adult hematopoietic progenitors and restricts granulopoiesis. J. Exp. Med. 201 (2005), 1487–1502.
11. Daro, E., Pulendran, B., Brasel, K., Teepe, M., Pettit, D., Lynch, D.H., Vremec, D., Robb, L., Shortman, K., McKenna, H.J., et al. Polyethylene glycol-modified GM-CSF expands CD11b(high)CD11c(high) but notCD11b(low)CD11c(high) murine dendritic cells in vivo: a comparative analysis with Flt3 ligand. J. Immunol. 165 (2000), 49–58.
12. DeKoter, R.P., Singh, H., Regulation of B lymphocyte and macrophage development by graded expression of PU.1. Science 288 (2000), 1439–1441.
13. DeKoter, R.P., Walsh, J.C., Singh, H., PU.1 regulates both cytokine-dependent proliferation and differentiation of granulocyte/macrophage progenitors. EMBO J. 17 (1998), 4456–4468.
14. Dranoff, G., Jaffee, E., Lazenby, A., Golumbek, P., Levitsky, H., Brose, K., Jackson, V., Hamada, H., Pardoll, D., Mulligan, R.C., Vaccination with irradiated tumor cells engineered to secrete murine granulocyte-macrophage colony-stimulating factor stimulates potent, specific, and long-lasting anti-tumor immunity. Proc. Natl. Acad. Sci. USA 90 (1993), 3539–3543.
15. Etzrodt, M., Cortez-Retamozo, V., Newton, A., Zhao, J., Ng, A., Wildgruber, M., Romero, P., Wurdinger, T., Xavier, R., Geissmann, F., et al. Regulation of monocyte functional heterogeneity by miR-146a and Relb. Cell Rep. 1 (2012), 317–324.
16. Fogg, D.K., Sibon, C., Miled, C., Jung, S., Aucouturier, P., Littman, D.R., Cumano, A., Geissmann, F., A clonogenic bone marrow progenitor specific for macrophages and dendritic cells. Science 311 (2006), 83–87.
17. Gao, Y., Nish, S.A., Jiang, R., Hou, L., Licona-Limón, P., Weinstein, J.S., Zhao, H., Medzhitov, R., Control of T helper 2 responses by transcription factor IRF4-dependent dendritic cells. Immunity 39 (2013), 722–732.
18. Gautier, E.L., Shay, T., Miller, J., Greter, M., Jakubzick, C., Ivanov, S., Helft, J., Chow, A., Elpek, K.G., Gordonov, S., et al., Immunological Genome Consortium. Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nat. Immunol. 13 (2012), 1118–1128.
19. Geissmann, F., Jung, S., Littman, D.R., Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 19 (2003), 71–82.
20. Ghani, S., Riemke, P., Schönheit, J., Lenze, D., Stumm, J., Hoogenkamp, M., Lagendijk, A., Heinz, S., Bonifer, C., Bakkers, J., et al. Macrophage development from HSCs requires PU.1-coordinated microRNA expression. Blood 118 (2011), 2275–2284.
21. Hanna, R.N., Shaked, I., Hubbeling, H.G., Punt, J.A., Wu, R., Herrley, E., Zaugg, C., Pei, H., Geissmann, F., Ley, K., Hedrick, C.C., NR4A1 (Nur77) deletion polarizes macrophages toward an inflammatory phenotype and increases atherosclerosis. Circ. Res. 110 (2012), 416–427.
22. Hettinger, J., Richards, D.M., Hansson, J., Barra, M.M., Joschko, A.C., Krijgsveld, J., Feuerer, M., Origin of monocytes and macrophages in a committed progenitor. Nat. Immunol. 14 (2013), 821–830.
23. Jakubzick, C., Gautier, E.L., Gibbings, S.L., Sojka, D.K., Schlitzer, A., Johnson, T.E., Ivanov, S., Duan, Q., Bala, S., Condon, T., et al. Minimal differentiation of classical monocytes as they survey steady-state tissues and transport antigen to lymph nodes. Immunity 39 (2013), 599–610.
24. Jurkin, J., Schichl, Y.M., Koeffel, R., Bauer, T., Richter, S., Konradi, S., Gesslbauer, B., Strobl, H., miR-146a is differentially expressed by myeloid dendritic cell subsets and desensitizes cells to TLR2-dependent activation. J. Immunol. 184 (2010), 4955–4965.
25. Kurotaki, D., Osato, N., Nishiyama, A., Yamamoto, M., Ban, T., Sato, H., Nakabayashi, J., Umehara, M., Miyake, N., Matsumoto, N., et al. Essential role of the IRF8-KLF4 transcription factor cascade in murine monocyte differentiation. Blood 121 (2013), 1839–1849.
26. Langlet, C., Tamoutounour, S., Henri, S., Luche, H., Ardouin, L., Grégoire, C., Malissen, B., Guilliams, M., CD64 expression distinguishes monocyte-derived and conventional dendritic cells and reveals their distinct role during intramuscular immunization. J. Immunol. 188 (2012), 1751–1760.
27. Lavin, Y., Winter, D., Blecher-Gonen, R., David, E., Keren-Shaul, H., Merad, M., Jung, S., Amit, I., Tissue-resident macrophage enhancer landscapes are shaped by the local microenvironment. Cell 159 (2014), 1312–1326.
28. Lee, J., Breton, G., Oliveira, T.Y., Zhou, Y.J., Aljoufi, A., Puhr, S., Cameron, M.J., Sékaly, R.P., Nussenzweig, M.C., Liu, K., Restricted dendritic cell and monocyte progenitors in human cord blood and bone marrow. J. Exp. Med. 212 (2015), 385–399.
29. LeibundGut-Landmann, S., Waldburger, J.M., Reis e Sousa, C., Acha-Orbea, H., Reith, W., MHC class II expression is differentially regulated in plasmacytoid and conventional dendritic cells. Nat. Immunol. 5 (2004), 899–908.
30. Lewis, K.L., Caton, M.L., Bogunovic, M., Greter, M., Grajkowska, L.T., Ng, D., Klinakis, A., Charo, I.F., Jung, S., Gommerman, J.L., et al. Notch2 receptor signaling controls functional differentiation of dendritic cells in the spleen and intestine. Immunity 35 (2011), 780–791.
31. Liu, K., Victora, G.D., Schwickert, T.A., Guermonprez, P., Meredith, M.M., Yao, K., Chu, F.F., Randolph, G.J., Rudensky, A.Y., Nussenzweig, M., In vivo analysis of dendritic cell development and homeostasis. Science 324 (2009), 392–397.
32. Loschko, J., Schreiber, H.A., Rieke, G.J., Esterházy, D., Meredith, M.M., Pedicord, V.A., Yao, K.H., Caballero, S., Pamer, E.G., Mucida, D., Nussenzweig, M.C., Absence of MHC class II on cDCs results in microbial-dependent intestinal inflammation. J. Exp. Med. 213 (2016), 517–534.
33. Mach, N., Gillessen, S., Wilson, S.B., Sheehan, C., Mihm, M., Dranoff, G., Differences in dendritic cells stimulated in vivo by tumors engineered to secrete granulocyte-macrophage colony-stimulating factor or Flt3-ligand. Cancer Res. 60 (2000), 3239–3246.
34. MacMicking, J.D., Nathan, C., Hom, G., Chartrain, N., Fletcher, D.S., Trumbauer, M., Stevens, K., Xie, Q.W., Sokol, K., Hutchinson, N., et al. Altered responses to bacterial infection and endotoxic shock in mice lacking inducible nitric oxide synthase. Cell 81 (1995), 641–650.
35. McKenna, H.J., Stocking, K.L., Miller, R.E., Brasel, K., De Smedt, T., Maraskovsky, E., Maliszewski, C.R., Lynch, D.H., Smith, J., Pulendran, B., et al. Mice lacking flt3 ligand have deficient hematopoiesis affecting hematopoietic progenitor cells, dendritic cells, and natural killer cells. Blood 95 (2000), 3489–3497.
36. McKercher, S.R., Torbett, B.E., Anderson, K.L., Henkel, G.W., Vestal, D.J., Baribault, H., Klemsz, M., Feeney, A.J., Wu, G.E., Paige, C.J., Maki, R.A., Targeted disruption of the PU.1 gene results in multiple hematopoietic abnormalities. EMBO J. 15 (1996), 5647–5658.
37. Meredith, M.M., Liu, K., Darrasse-Jeze, G., Kamphorst, A.O., Schreiber, H.A., Guermonprez, P., Idoyaga, J., Cheong, C., Yao, K.H., Niec, R.E., Nussenzweig, M.C., Expression of the zinc finger transcription factor zDC (Zbtb46, Btbd4) defines the classical dendritic cell lineage. J. Exp. Med. 209 (2012), 1153–1165.
38. Miller, J.C., Brown, B.D., Shay, T., Gautier, E.L., Jojic, V., Cohain, A., Pandey, G., Leboeuf, M., Elpek, K.G., Helft, J., et al., Immunological Genome Consortium. Deciphering the transcriptional network of the dendritic cell lineage. Nat. Immunol. 13 (2012), 888–899.
39. Naik, S.H., Sathe, P., Park, H.Y., Metcalf, D., Proietto, A.I., Dakic, A., Carotta, S., O'Keeffe, M., Bahlo, M., Papenfuss, A., et al. Development of plasmacytoid and conventional dendritic cell subtypes from single precursor cells derived in vitro and in vivo. Nat. Immunol. 8 (2007), 1217–1226.
40. Naik, S.H., Perié, L., Swart, E., Gerlach, C., van Rooij, N., de Boer, R.J., Schumacher, T.N., Diverse and heritable lineage imprinting of early haematopoietic progenitors. Nature 496 (2013), 229–232.
41. Norris, P.C., Gosselin, D., Reichart, D., Glass, C.K., Dennis, E.A., Phospholipase A2 regulates eicosanoid class switching during inflammasome activation. Proc. Natl. Acad. Sci. USA 111 (2014), 12746–12751.
42. Nussenzweig, M.C., Steinman, R.M., Gutchinov, B., Cohn, Z.A., Dendritic cells are accessory cells for the development of anti-trinitrophenyl cytotoxic T lymphocytes. J. Exp. Med. 152 (1980), 1070–1084.
43. Onai, N., Obata-Onai, A., Schmid, M.A., Ohteki, T., Jarrossay, D., Manz, M.G., Identification of clonogenic common Flt3+M-CSFR+ plasmacytoid and conventional dendritic cell progenitors in mouse bone marrow. Nat. Immunol. 8 (2007), 1207–1216.
44. Plantinga, M., Guilliams, M., Vanheerswynghels, M., Deswarte, K., Branco-Madeira, F., Toussaint, W., Vanhoutte, L., Neyt, K., Killeen, N., Malissen, B., et al. Conventional and monocyte-derived CD11b(+) dendritic cells initiate and maintain T helper 2 cell-mediated immunity to house dust mite allergen. Immunity 38 (2013), 322–335.
45. Sathe, P., Metcalf, D., Vremec, D., Naik, S.H., Langdon, W.Y., Huntington, N.D., Wu, L., Shortman, K., Lymphoid tissue and plasmacytoid dendritic cells and macrophages do not share a common macrophage-dendritic cell-restricted progenitor. Immunity 41 (2014), 104–115.
46. Satpathy, A.T., Kc, W., Albring, J.C., Edelson, B.T., Kretzer, N.M., Bhattacharya, D., Murphy, T.L., Murphy, K.M., Zbtb46 expression distinguishes classical dendritic cells and their committed progenitors from other immune lineages. J. Exp. Med. 209 (2012), 1135–1152.
47. Schlitzer, A., Sivakamasundari, V., Chen, J., Sumatoh, H.R., Schreuder, J., Lum, J., Malleret, B., Zhang, S., Larbi, A., Zolezzi, F., et al. Identification of cDC1- and cDC2-committed DC progenitors reveals early lineage priming at the common DC progenitor stage in the bone marrow. Nat. Immunol. 16 (2015), 718–728.
48. Schraml, B.U., van Blijswijk, J., Zelenay, S., Whitney, P.G., Filby, A., Acton, S.E., Rogers, N.C., Moncaut, N., Carvajal, J.J., Reis e Sousa, C., Genetic tracing via DNGR-1 expression history defines dendritic cells as a hematopoietic lineage. Cell 154 (2013), 843–858.
49. Schreiber, H.A., Loschko, J., Karssemeijer, R.A., Escolano, A., Meredith, M.M., Mucida, D., Guermonprez, P., Nussenzweig, M.C., Intestinal monocytes and macrophages are required for T cell polarization in response to Citrobacter rodentium. J. Exp. Med. 210 (2013), 2025–2039.
50. Scott, E.W., Simon, M.C., Anastasi, J., Singh, H., Requirement of transcription factor PU.1 in the development of multiple hematopoietic lineages. Science 265 (1994), 1573–1577.
51. Serbina, N.V., Pamer, E.G., Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR2. Nat. Immunol. 7 (2006), 311–317.
52. Serbina, N.V., Salazar-Mather, T.P., Biron, C.A., Kuziel, W.A., Pamer, E.G., TNF/iNOS-producing dendritic cells mediate innate immune defense against bacterial infection. Immunity 19 (2003), 59–70.
53. Steinman, R.M., Cohn, Z.A., Identification of a novel cell type in peripheral lymphoid organs of mice. I. Morphology, quantitation, tissue distribution. J. Exp. Med. 137 (1973), 1142–1162.
54. Sunderkötter, C., Nikolic, T., Dillon, M.J., Van Rooijen, N., Stehling, M., Drevets, D.A., Leenen, P.J., Subpopulations of mouse blood monocytes differ in maturation stage and inflammatory response. J. Immunol. 172 (2004), 4410–4417.
55. Tamoutounour, S., Henri, S., Lelouard, H., de Bovis, B., de Haar, C., van der Woude, C.J., Woltman, A.M., Reyal, Y., Bonnet, D., Sichien, D., 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 (2012), 3150–3166.
56. Tamura, T., Tailor, P., Yamaoka, K., Kong, H.J., Tsujimura, H., O'Shea, J.J., Singh, H., Ozato, K., IFN regulatory factor-4 and -8 govern dendritic cell subset development and their functional diversity. J. Immunol. 174 (2005), 2573–2581.
57. Tussiwand, R., Everts, B., Grajales-Reyes, G.E., Kretzer, N.M., Iwata, A., Bagaitkar, J., Wu, X., Wong, R., Anderson, D.A., Murphy, T.L., et al. Klf4 expression in conventional dendritic cells is required for T helper 2 cell responses. Immunity 42 (2015), 916–928.
58. Vander Lugt, B., Khan, A.A., Hackney, J.A., Agrawal, S., Lesch, J., Zhou, M., Lee, W.P., Park, S., Xu, M., DeVoss, J., et al. Transcriptional programming of dendritic cells for enhanced MHC class II antigen presentation. Nat. Immunol. 15 (2014), 161–167.
59. Varol, C., Landsman, L., Fogg, D.K., Greenshtein, L., Gildor, B., Margalit, R., Kalchenko, V., Geissmann, F., Jung, S., Monocytes give rise to mucosal, but not splenic, conventional dendritic cells. J. Exp. Med. 204 (2007), 171–180.
60. Waskow, C., Liu, K., Darrasse-Jèze, G., Guermonprez, P., Ginhoux, F., Merad, M., Shengelia, T., Yao, K., Nussenzweig, M., The receptor tyrosine kinase Flt3 is required for dendritic cell development in peripheral lymphoid tissues. Nat. Immunol. 9 (2008), 676–683.
61. Yona, S., Kim, K.W., Wolf, Y., Mildner, A., Varol, D., Breker, M., Strauss-Ayali, D., Viukov, S., Guilliams, M., Misharin, A., et al. Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis. Immunity 38 (2013), 79–91.
62. Zigmond, E., Varol, C., Farache, J., Elmaliah, E., Satpathy, A.T., Friedlander, G., Mack, M., Shpigel, N., Boneca, I.G., Murphy, K.M., et al. Ly6C hi monocytes in the inflamed colon give rise to proinflammatory effector cells and migratory antigen-presenting cells. Immunity 37 (2012), 1076–1090.