Altered compensatory cytokine signaling underlies the discrepancy between Flt3-/- and Flt3l-/- mice

Journal of Experimental Medicine

Volumn 215, Issue 5, 2018, Pages 1417-1435

  Durai, Vivek ^a   Bagadia, Prachi ^a   Briseño, Carlos G ^a   Theisen, Derek J ^a   Iwata, Arifumi ^a   Davidson, Jesse T ^a   Gargaro, Marco ^a   Fremont, Daved H ^a   Murphy, Theresa ^a   Murphy, Kenneth M ^a  

^a WASHINGTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD135 ANTIGEN; COLONY STIMULATING FACTOR 1; FLT3 LIGAND; STEM CELL FACTOR; COLONY STIMULATING FACTOR RECEPTOR; CYTOKINE; FLT3 LIGAND PROTEIN; FLT3 PROTEIN, MOUSE; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; MEMBRANE PROTEIN; STEM CELL FACTOR RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; FEMALE; GENE DELETION; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; ANIMAL; BONE MARROW; C57BL MOUSE; CYTOLOGY; DEFICIENCY; DRUG EFFECT; GENETIC TRANSCRIPTION; METABOLISM; STEM CELL;

ANIMALS; BONE MARROW; CYTOKINES; DENDRITIC CELLS; FMS-LIKE TYROSINE KINASE 3; GENE DELETION; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; MEMBRANE PROTEINS; MICE, INBRED C57BL; PROTO-ONCOGENE PROTEINS C-KIT; RECEPTOR, MACROPHAGE COLONY-STIMULATING FACTOR; SIGNAL TRANSDUCTION; STEM CELL FACTOR; STEM CELLS; TRANSCRIPTION, GENETIC;

EID: 85046754948     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20171784     Document Type: Article

References (59)

1. Auffray, C., D.K. Fogg, E. Narni-Mancinelli, B. Senechal, C. Trouillet, N. Saederup, J. Leemput, K. Bigot, L. Campisi, M. Abitbol, et al. 2009. CX3CR1+ CD115+ CD135+ common macrophage/DC precursors and the role of CX3CR1 in their response to inflammation. J. Exp. Med. 206:595- 606. https:// doi .org/ 10 .1084/ jem .20081385
2. Brasel, K., T. De Smedt, J.L. Smith, and C.R. Maliszewski. 2000. Generation of murine dendritic cells from flt3-ligand-supplemented bone marrow cultures. Blood. 96:3029-3039.
3. Breton, G., J. Lee, Y.J. Zhou, J.J. Schreiber, T. Keler, S. Puhr, N. Anandasabapathy, S. Schlesinger, M. Caskey, K. Liu, and M.C. Nussenzweig. 2015. Circulating precursors of human CD1c+ and CD141+ dendritic cells. J. Exp. Med. 212:401-413. https:// doi .org/ 10 .1084/ jem .20141441
4. D'Amico, A., and L. Wu. 2003. The early progenitors of mouse dendritic cells and plasmacytoid predendritic cells are within the bone marrow hemopoietic precursors expressing Flt3. J. Exp. Med. 198:293-303. https:// doi .org/ 10 .1084/ jem .20030107
5. Darrah, P.A., D.T. Patel, P.M. De Luca, R.W. Lindsay, D.F. Davey, B.J. Flynn, S.T. Hoff, P. Andersen, S.G. Reed, S.L. Morris, et al. 2007. Multifunctional TH1 cells define a correlate of vaccine-mediated protection against Leishmania major. Nat. Med. 13:843-850. https:// doi .org/ 10 .1038/ nm1592
6. Dosil, M., S. Wang, and I.R. Lemischka. 1993. Mitogenic signalling and substrate specificity of the Flk2/Flt3 receptor tyrosine kinase in fibroblasts and interleukin 3-dependent hematopoietic cells. Mol. Cell. Biol. 13:6572- 6585. https:// doi .org/ 10 .1128/ MCB .13 .10 .6572
7. Enver, T., C.M. Heyworth, and T.M. Dexter. 1998. Do stem cells play dice? Blood. 92:348-351, discussion :352.
8. Fancke, B., M. Suter, H. Hochrein, and M. O'Keeffe. 2008. M-CSF: a novel plasmacytoid and conventional dendritic cell poietin. Blood. 111:150-159. https:// doi .org/ 10 .1182/ blood -2007 -05 -089292
9. Fogg, D.K., C. Sibon, C. Miled, S. Jung, P. Aucouturier, D.R. Littman, A. Cumano, and F. Geissmann. 2006. A clonogenic bone marrow progenitor specific for macrophages and dendritic cells. Science. 311:83-87. https:// doi .org/ 10 .1126/ science .1117729
10. Ginhoux, F., K. Liu, J. Helft, M. Bogunovic, M. Greter, D. Hashimoto, J. Price, N. Yin, J. Bromberg, S.A. Lira, et al. 2009. The origin and development of nonlymphoid tissue CD103+ DCs. J. Exp. Med. 206:3115-3130. https:// doi .org/ 10 .1084/ jem .20091756
11. Grajales-Reyes, G.E., A. Iwata, J. Albring, X. Wu, R. Tussiwand, W. Kc, N.M. Kretzer, C.G. Briseño, V. Durai, P. Bagadia, et al. 2015. Batf3 maintains autoactivation of Irf8 for commitment of a CD8a(+) conventional DC clonogenic progenitor. Nat. Immunol. 16:708-717. https:// doi .org/ 10 .1038/ ni .3197
12. Helft, J., F. Ginhoux, M. Bogunovic, and M. Merad. 2010. Origin and functional heterogeneity of non-lymphoid tissue dendritic cells in mice. Immunol. Rev. 234:55-75. https:// doi .org/ 10 .1111/ j .0105 -2896 .2009 .00885 .x
13. Karsunky, H., M. Merad, A. Cozzio, I.L. Weissman, and M.G. Manz. 2003. 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. https:// doi .org/ 10 .1084/ jem .20030323
14. Kingston, D., M.A. Schmid, N. Onai, A. Obata-Onai, D. Baumjohann, and M.G. Manz. 2009. The concerted action of GM-CSF and Flt3-ligand on in vivo dendritic cell homeostasis. Blood. 114:835-843. https:// doi .org/ 10 .1182/ blood -2009 -02 -206318
15. Kretzer, N.M., D.J. Theisen, R. Tussiwand, C.G. Briseño, G.E. Grajales-Reyes, X. Wu, V. Durai, J. Albring, P. Bagadia, T.L. Murphy, and K.M. Murphy. 2016. RAB43 facilitates cross-presentation of cell-associated antigens by CD8a+ dendritic cells. J. Exp. Med. 213:2871-2883. https:// doi .org/ 10 .1084/ jem .20160597
16. Lee, J., G. Breton, T.Y. Oliveira, Y.J. Zhou, A. Aljoufi, S. Puhr, M.J. Cameron, R.P. Sékaly, M.C. Nussenzweig, and K. Liu. 2015. Restricted dendritic cell and monocyte progenitors in human cord blood and bone marrow. J. Exp. Med. 212:385-399. https:// doi .org/ 10 .1084/ jem .20141442
17. Li, J., K. Chen, L. Zhu, and J.W. Pollard. 2006. Conditional deletion of the colony stimulating factor-1 receptor (c-fms proto-oncogene) in mice. Genesis. 44:328-335. https:// doi .org/ 10 .1002/ dvg .20219
18. Lieschke, G.J., D. Grail, G. Hodgson, D. Metcalf, E. Stanley, C. Cheers, K.J. Fowler, S. Basu, Y.F. Zhan, and A.R. Dunn. 1994. Mice lacking granulocyte colony-stimulating factor have chronic neutropenia, granulocyte and macrophage progenitor cell deficiency, and impaired neutrophil mobilization. Blood. 84:1737-1746.
19. Liu, K., C. Waskow, X. Liu, K. Yao, J. Hoh, and M. Nussenzweig. 2007. Origin of dendritic cells in peripheral lymphoid organs of mice. Nat. Immunol. 8:578-583. https:// doi .org/ 10 .1038/ ni1462
20. Liu, K., G.D. Victora, T.A. Schwickert, P. Guermonprez, M.M. Meredith, K. Yao, F.F. Chu, G.J. Randolph, A.Y. Rudensky, and M. Nussenzweig. 2009. In vivo analysis of dendritic cell development and homeostasis. Science. 324:392-397.
21. Lyman, S.D., L. James, T. Vanden Bos, P. de Vries, K. Brasel, B. Gliniak, L.T. Hollingsworth, K.S. Picha, H.J. McKenna, R.R. Splett, et al. 1993. Molecular cloning of a ligand for the flt3/flk-2 tyrosine kinase receptor: a proliferative factor for primitive hematopoietic cells. Cell. 75:1157-1167. https:// doi .org/ 10 .1016/ 0092 -8674(93)90325 -K
22. Mackarehtschian, K., J.D. Hardin, K.A. Moore, S. Boast, S.P. Goff, and I.R. Lemischka. 1995. Targeted disruption of the flk2/flt3 gene leads to deficiencies in primitive hematopoietic progenitors. Immunity. 3:147-161. https:// doi .org/ 10 .1016/ 1074 -7613(95)90167 -1
23. Maraskovsky, E., K. Brasel, M. Teepe, E.R. Roux, S.D. Lyman, K. Shortman, and H.J. McKenna. 1996. Dramatic increase in the numbers of functionally mature dendritic cells in Flt3 ligand-treated mice: multiple dendritic cell subpopulations identified. J. Exp. Med. 184:1953-1962. https:// doi .org/ 10 .1084/ jem .184 .5 .1953
24. Maraskovsky, E., E. Daro, E. Roux, M. Teepe, C.R. Maliszewski, J. Hoek, D. Caron, M.E. Lebsack, and H.J. McKenna. 2000. In vivo generation of human dendritic cell subsets by Flt3 ligand. Blood. 96:878-884.
25. Matthews, W., C.T. Jordan, M. Gavin, N.A. Jenkins, N.G. Copeland, and I.R. Lemischka. 1991. A receptor tyrosine kinase cDNA isolated from a population of enriched primitive hematopoietic cells and exhibiting close genetic linkage to c-kit. Proc. Natl. Acad. Sci. USA. 88:9026-9030. https:// doi .org/ 10 .1073/ pnas .88 .20 .9026
26. McKenna, H.J., K.L. Stocking, R.E. Miller, K. Brasel, T. De Smedt, E. Maraskovsky, C.R. Maliszewski, D.H. Lynch, J. Smith, B. Pulendran, et al. 2000. Mice lacking flt3 ligand have deficient hematopoiesis affecting hematopoietic progenitor cells, dendritic cells, and natural killer cells. Blood. 95:3489-3497.
27. Merad, M., P. Sathe, J. Helft, J. Miller, and A. Mortha. 2013. The dendritic cell lineage: ontogeny and function of dendritic cells and their subsets in the steady state and the inflamed setting. Annu. Rev. Immunol. 31:563-604. https:// doi .org/ 10 .1146/ annurev -immunol -020711 -074950
28. Meredith, M.M., K. Liu, G. Darrasse-Jeze, A.O. Kamphorst, H.A. Schreiber, P. Guermonprez, J. Idoyaga, C. Cheong, K.H. Yao, R.E. Niec, and M.C. Nussenzweig. 2012. Expression of the zinc finger transcription factor zDC (Zbtb46, Btbd4) defines the classical dendritic cell lineage. J. Exp. Med. 209:1153-1165. https:// doi .org/ 10 .1084/ jem .20112675
29. Metcalf, D. 1998. Lineage commitment and maturation in hematopoietic cells: the case for extrinsic regulation. Blood. 92:345-347, discussion :352.
30. Mildner, A., and S. Jung. 2014. Development and function of dendritic cell subsets. Immunity. 40:642-656. https:// doi .org/ 10 .1016/ j .immuni .2014 .04 .016
31. Miller, J.C., B.D. Brown, T. Shay, E.L. Gautier, V. Jojic, A. Cohain, G. Pandey, M. Leboeuf, K.G. Elpek, J. Helft, et al. Immunological Genome Consortium. 2012. Deciphering the transcriptional network of the dendritic cell lineage. Nat. Immunol. 13:888-899. https:// doi .org/ 10 .1038/ ni .2370
32. Moore, A.J., and M.K. Anderson. 2013. Dendritic cell development: a chooseyour- own-adventure story. Adv. Hematol. 2013:949513. https:// doi .org/ 10 .1155/ 2013/ 949513
33. Mossadegh-Keller, N., S. Sarrazin, P.K. Kandalla, L. Espinosa, E.R. Stanley, S.L. Nutt, J. Moore, and M.H. Sieweke. 2013. M-CSF instructs myeloid lineage fate in single haematopoietic stem cells. Nature. 497:239-243. https:// doi .org/ 10 .1038/ nature12026
34. Nagasawa, T. 2006. Microenvironmental niches in the bone marrow required for B-cell development. Nat. Rev. Immunol. 6:107-116. https:// doi .org/ 10 .1038/ nri1780
35. Naik, S.H., A.I. Proietto, N.S. Wilson, A. Dakic, P. Schnorrer, M. Fuchsberger, M.H. Lahoud, M. O'Keeffe, Q.X. Shao, W.F. Chen, et al. 2005. Cutting edge: generation of splenic CD8+ and CD8- dendritic cell equivalents in Fms-like tyrosine kinase 3 ligand bone marrow cultures. J. Immunol. 174:6592-6597. https:// doi .org/ 10 .4049/ jimmunol .174 .11 .6592
36. Naik, S.H., P. Sathe, H.Y. Park, D. Metcalf, A.I. Proietto, A. Dakic, S. Carotta, M. O'Keeffe, M. Bahlo, A. Papenfuss, et al. 2007. Development of plasmacytoid and conventional dendritic cell subtypes from single precursor cells derived in vitro and in vivo. Nat. Immunol. 8:1217-1226. https:// doi .org/ 10 .1038/ ni1522
37. Onai, N., A. Obata-Onai, R. Tussiwand, A. Lanzavecchia, and M.G. Manz. 2006. Activation of the Flt3 signal transduction cascade rescues and enhances type I interferon-producing and dendritic cell development. J. Exp. Med. 203:227-238. https:// doi .org/ 10 .1084/ jem .20051645
38. Onai, N., A. Obata-Onai, M.A. Schmid, T. Ohteki, D. Jarrossay, and M.G. Manz. 2007. Identification of clonogenic common Flt3+M-CSFR+ plasmacytoid and conventional dendritic cell progenitors in mouse bone marrow. Nat. Immunol. 8:1207-1216. https:// doi .org/ 10 .1038/ ni1518
39. Onai, N., K. Kurabayashi, M. Hosoi-Amaike, N. Toyama-Sorimachi, K. Matsushima, K. Inaba, and T. Ohteki. 2013. A clonogenic progenitor with prominent plasmacytoid dendritic cell developmental potential. Immunity. 38:943-957. https:// doi .org/ 10 .1016/ j .immuni .2013 .04 .006
40. Peschon, J.J., P.J. Morrissey, K.H. Grabstein, F.J. Ramsdell, E. Maraskovsky, B.C. Gliniak, L.S. Park, S.F. Ziegler, D.E. Williams, C.B. Ware, et al. 1994. Early lymphocyte expansion is severely impaired in interleukin 7 receptor- deficient mice. J. Exp. Med. 180:1955-1960. https:// doi .org/ 10 .1084/ jem .180 .5 .1955
41. Rieger, M.A., P.S. Hoppe, B.M. Smejkal, A.C. Eitelhuber, and T. Schroeder. 2009. Hematopoietic cytokines can instruct lineage choice. Science. 325:217-218. https:// doi .org/ 10 .1126/ science .1171461
42. Rottapel, R., C.W. Turck, N. Casteran, X. Liu, D. Birnbaum, T. Pawson, and P. Dubreuil. 1994. Substrate specificities and identification of a putative binding site for PI3K in the carboxy tail of the murine Flt3 receptor tyrosine kinase. Oncogene. 9:1755-1765.
43. Sathe, P., D. Vremec, L. Wu, L. Corcoran, and K. Shortman. 2013. Convergent differentiation: myeloid and lymphoid pathways to murine plasmacytoid dendritic cells. Blood. 121:11-19. https:// doi .org/ 10 .1182/ blood -2012 -02 -413336
44. Satpathy, A.T., K.M. Murphy, and W. Kc. 2011. Transcription factor networks in dendritic cell development. Semin. Immunol. 23:388-397. https:// doi .org/ 10 .1016/ j .smim .2011 .08 .009
45. Satpathy, A.T., W. Kc, J.C. Albring, B.T. Edelson, N.M. Kretzer, D. Bhattacharya, T.L. Murphy, and K.M. Murphy. 2012. Zbtb46 expression distinguishes classical dendritic cells and their committed progenitors from other immune lineages. J. Exp. Med. 209:1135-1152. https:// doi .org/ 10 .1084/ jem .20120030
46. Schlenner, S.M., V. Madan, K. Busch, A. Tietz, C. Läufle, C. Costa, C. Blum, H.J. Fehling, and H.R. Rodewald. 2010. Fate mapping reveals separate origins of T cells and myeloid lineages in the thymus. Immunity. 32:426-436. https:// doi .org/ 10 .1016/ j .immuni .2010 .03 .005
47. Schlitzer, A., V. Sivakamasundari, J. Chen, H.R. Sumatoh, J. Schreuder, J. Lum, B. Malleret, S. Zhang, A. Larbi, F. Zolezzi, et al. 2015. Identification of cDC1- and cDC2-committed DC progenitors reveals early lineage priming at the common DC progenitor stage in the bone marrow. Nat. Immunol. 16:718-728. https:// doi .org/ 10 .1038/ ni .3200
48. See, P., C.A. Dutertre, J. Chen, P. Günther, N. McGovern, S.E. Irac, M. Gunawan, M. Beyer, K. Händler, K. Duan, et al. 2017. Mapping the human DC lineage through the integration of high-dimensional techniques. Science. 356:eaag3009. https:// doi .org/ 10 .1126/ science .aag3009
49. Shooshtari, P., E.S. Fortuno III, D. Blimkie, M. Yu, A. Gupta, T.R. Kollmann, and R.R. Brinkman. 2010. Correlation analysis of intracellular and secreted cytokines via the generalized integrated mean fluorescence intensity. Cytometry A. 77A:873-880. https:// doi .org/ 10 .1002/ cyto .a .20943
50. Sitnicka, E., D. Bryder, K. Theilgaard-Mönch, N. Buza-Vidas, J. Adolfsson, and S.E. Jacobsen. 2002. Key role of flt3 ligand in regulation of the common lymphoid progenitor but not in maintenance of the hematopoietic stem cell pool. Immunity. 17:463-472. https:// doi .org/ 10 .1016/ S1074 -7613(02)00419 -3
51. Sitnicka, E., C. Brakebusch, I.L. Martensson, M. Svensson, W.W. Agace, M. Sigvardsson, N. Buza-Vidas, D. Bryder, C.M. Cilio, H. Ahlenius, et al. 2003. Complementary signaling through flt3 and interleukin-7 receptor a is indispensable for fetal and adult B cell genesis. J. Exp. Med. 198:1495- 1506. https:// doi .org/ 10 .1084/ jem .20031152
52. Tsapogas, P., L.K. Swee, A. Nusser, N. Nuber, M. Kreuzaler, G. Capoferri, H. Rolink, R. Ceredig, and A. Rolink. 2014. In vivo evidence for an instructive role of fms-like tyrosine kinase-3 (FLT3) ligand in hematopoietic development. Haematologica. 99:638-646. https:// doi .org/ 10 .3324/ haematol .2013 .089482
53. Tsapogas, P., C.J. Mooney, G. Brown, and A. Rolink. 2017. The Cytokine Flt3-Ligand in Normal and Malignant Hematopoiesis. Int. J. Mol. Sci. 18:1115. https:// doi .org/ 10 .3390/ ijms18061115
54. Ventura, A., D.G. Kirsch, M.E. McLaughlin, D.A. Tuveson, J. Grimm, L. Lintault, J. Newman, E.E. Reczek, R. Weissleder, and T. Jacks. 2007. Restoration of p53 function leads to tumour regression in vivo. Nature. 445:661-665. https:// doi .org/ 10 .1038/ nature05541
55. Verstraete, K., and S.N. Savvides. 2012. Extracellular assembly and activation principles of oncogenic class III receptor tyrosine kinases. Nat. Rev. Cancer. 12:753-766. https:// doi .org/ 10 .1038/ nrc3371
56. von Freeden-Jeffry, U., P. Vieira, L.A. Lucian, T. McNeil, S.E. Burdach, and R. Murray. 1995. Lymphopenia in interleukin (IL)-7 gene-deleted mice identifies IL-7 as a nonredundant cytokine. J. Exp. Med. 181:1519-1526. https:// doi .org/ 10 .1084/ jem .181 .4 .1519
57. Waskow, C., K. Liu, G. Darrasse-Jèze, P. Guermonprez, F. Ginhoux, M. Merad, T. Shengelia, K. Yao, and M. Nussenzweig. 2008. The receptor tyrosine kinase Flt3 is required for dendritic cell development in peripheral lymphoid tissues. Nat. Immunol. 9:676-683. https:// doi .org/ 10 .1038/ ni .1615
58. Wu, H., X. Liu, R. Jaenisch, and H.F. Lodish. 1995. Generation of committed erythroid BFU-E and CFU-E progenitors does not require erythropoietin or the erythropoietin receptor. Cell. 83:59-67. https:// doi .org/ 10 .1016/ 0092 -8674(95)90234 -1
59. Wu, X., C.G. Briseño, V. Durai, J.C. Albring, M. Haldar, P. Bagadia, K.W. Kim, G.J. Randolph, T.L. Murphy, and K.M. Murphy. 2016. Mafb lineage tracing to distinguish macrophages from other immune lineages reveals dual identity of Langerhans cells. J. Exp. Med. 213:2553-2565. https:// doi .org/ 10 .1084/ jem .20160600