Technical advance: Visualization of bone marrow monocyte mobilization using Cx3cr1gfp/+flt3l–/– reporter mouse by multiphoton intravital microscopy

Journal of Leukocyte Biology

Volumn 97, Issue 3, 2015, Pages 611-619

  Evrard, Maximilien ^a   Chong, Shu Zhen ^a   Devi, Sapna ^a   Chew, Weng Keong ^a   Lee, Bernett ^a   Poidinger, Michael ^a   Ginhoux, Florent ^a   Tan, Suet Mien ^b   Ng, Lai Guan ^a  

^a AGENCY FOR SCIENCE   (Singapore)

^b NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

Dendritic cells; Live imaging; Macrophages; Trafficking

Indexed keywords

CHEMOKINE RECEPTOR CCR2; CHEMOKINE RECEPTOR CX3CR1; FLT3 LIGAND; GREEN FLUORESCENT PROTEIN; MAFIA PROTEIN; PROTEIN; UNCLASSIFIED DRUG; CCR2 PROTEIN, MOUSE; CHEMOKINE RECEPTOR; CX3CR1 PROTEIN, MOUSE; FLT3 LIGAND PROTEIN; LIPOPOLYSACCHARIDE; MEMBRANE PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CELL STRUCTURE; CELL SURVIVAL; CELL TRACKING; CELLULAR DISTRIBUTION; COMPARATIVE STUDY; CONTROLLED STUDY; FLOW CYTOMETRY; FLUORESCENCE ANALYSIS; GENE EXPRESSION; IMAGE ANALYSIS; IMMOBILIZED CELL; IMMUNOLOGICAL TECHNIQUE; IN VIVO STUDY; MONOCYTE; MONONUCLEAR PHAGOCYTE; MOUSE; MOUSE MODEL; MOUSE STRAIN; MULTIPHOTON INTRAVITAL MICROSCOPY; MULTIPHOTON MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SKULL RADIOGRAPHY; ANIMAL; CELL COUNT; CELL SHAPE; CYTOLOGY; DEFICIENCY; DENDRITIC CELL; DRUG EFFECTS; METABOLISM; PHENOTYPE; PROCEDURES; REPORTER GENE; SKULL;

MUS;

ANIMALS; BONE MARROW CELLS; CELL COUNT; CELL SHAPE; DENDRITIC CELLS; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; LIPOPOLYSACCHARIDES; MEMBRANE PROTEINS; MICE; MICROSCOPY, FLUORESCENCE, MULTIPHOTON; MONOCYTES; PHENOTYPE; RECEPTORS, CCR2; RECEPTORS, CHEMOKINE; SKULL;

EID: 84928767736     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.1TA0514-274R     Document Type: Article

References (34)

1. Germain, R. N., Robey, E. A., Cahalan, M. D. (2012) A decade of imaging cellular motility and interaction dynamics in the immune system. Science 336, 1676–1681.
2. Gebhardt, T., Whitney, P. G., Zaid, A., Mackay, L. K., Brooks, A. G., Heath, W. R., Carbone, F. R., Mueller, S. N. (2011) Different patterns of peripheral migration by memory CD4+ and CD8+ T cells. Nature 477, 216–219.
3. Müller, A. J., Filipe-Santos, O., Eberl, G., Aebischer, T., Späth, G. F., Bousso, P. (2012) CD4+ T cells rely on a cytokine gradient to control intracellular pathogens beyond sites of antigen presentation. Immunity 37, 147–157.
4. Moreau, H. D., Lemaˆıtre, F., Terriac, E., Azar, G., Piel, M., Lennon- Dumenil, A. M., Bousso, P. (2012) Dynamic in situ cytometry uncovers T cell receptor signaling during immunological synapses and kinapses in vivo. Immunity 37, 351–363.
5. Moran, A. E., Holzapfel, K. L., Xing, Y., Cunningham, N. R., Maltzman, J. S., Punt, J., Hogquist, K. A. (2011) T Cell receptor signal strength in Treg and iNKT cell development demonstrated by a novel fluorescent reporter mouse. J. Exp. Med. 208, 1279–1289.
6. Tal, O., Lim, H. Y., Gurevich, I., Milo, I., Shipony, Z., Ng, L. G., Angeli, V., Shakhar, G. (2011) DC mobilization from the skin requires docking to immobilized CCL21 on lymphatic endothelium and intralymphatic crawling. J. Exp. Med. 208, 2141–2153.
7. Köhler, A., De Filippo, K., Hasenberg, M., van den Brandt, C., Nye, E., Hosking, M. P., Lane, T. E., Männ, L., Ransohoff, R. M., Hauser, A. E., Winter, O., Schraven, B., Geiger, H., Hogg, N., Gunzer, M. (2011) G-CSFmediated thrombopoietin release triggers neutrophil motility and mobilization from bone marrow via induction of Cxcr2 ligands. Blood 117, 4349–4357.
8. Devi, S., Wang, Y., Chew, W. K., Lima, R., A-González, N., Mattar, C. N., Chong, S. Z., Schlitzer, A., Bakocevic, N., Chew, S., Keeble, J. L., Goh, C. C., Li, J. L., Evrard, M., Malleret, B., Larbi, A., Renia, L., Haniffa, M., Tan, S. M., Chan, J. K., Balabanian, K., Nagasawa, T., Bachelerie, F., Hidalgo, A., Ginhoux, F., Kubes, P., Ng, L. G. (2013) Neutrophil mobilization via plerixafor-mediated CXCR4 inhibition arises from lung demargination and blockade of neutrophil homing to the bone marrow. J. Exp. Med. 210, 2321–2336.
9. Mildner, A., Yona, S., Jung, S. (2013) A close encounter of the third kind: monocyte-derived cells. Adv. Immunol. 120, 69–103.
10. Ginhoux, F., Jung, S. (2014) Monocytes and macrophages: developmental pathways and tissue homeostasis. Nat. Rev. Immunol. 14, 392–404.
11. Pittet, M. J., Swirski, F. K. (2011) Monocytes link atherosclerosis and cancer. Eur. J. Immunol. 41, 2519–2522.
12. Pittet, M. J., Nahrendorf, M., Swirski, F. K. (2014) The journey from stem cell to macrophage. Ann. N. Y. Acad. Sci. 1319, 1–18.
13. Shi, C., Pamer, E. G. (2011) Monocyte recruitment during infection and inflammation. Nat. Rev. Immunol. 11, 762–774.
14. Milo, I., Sapoznikov, A., Kalchenko, V., Tal, O., Krauthgamer, R., van Rooijen, N., Dudziak, D., Jung, S., Shakhar, G. (2013) Dynamic imaging reveals promiscuous crosspresentation of blood-borne antigens to naive CD8+ T cells in the bone marrow. Blood 122, 193–208.
15. Lo Celso, C., Fleming, H. E., Wu, J. W., Zhao, C. X., Miake-Lye, S., Fujisaki, J., Cˆoté, D., Rowe, D. W., Lin, C. P., Scadden, D. T. (2009) Liveanimal tracking of individual haematopoietic stem/progenitor cells in their niche. Nature 457, 92–96.
16. Kikuta, J., Wada, Y., Kowada, T., Wang, Z., Sun-Wada, G. H., Nishiyama, I., Mizukami, S., Maiya, N., Yasuda, H., Kumanogoh, A., Kikuchi, K., Germain, R. N., Ishii, M. (2013) Dynamic visualization of RANKL and Th17-mediated osteoclast function. J. Clin. Invest. 123, 866–873.
17. Hume, D. A. (2011) Applications of myeloid-specific promoters in transgenic mice support in vivo imaging and functional genomics but do not support the concept of distinct macrophage and dendritic cell lineages or roles in immunity. J. Leukoc. Biol. 89, 525–538.
18. Iparraguirre, A., Tobias, J. W., Hensley, S. E., Masek, K. S., Cavanagh, L. L., Rendl, M., Hunter, C. A., Ertl, H. C., von Andrian, U. H., Weninger, W. (2008) Two distinct activation states of plasmacytoid dendritic cells induced by influenza virus and CpG 1826 oligonucleotide. J. Leukoc. Biol. 83, 610–620.
19. Jung, S., Aliberti, J., Graemmel, P., Sunshine, M. J., Kreutzberg, G. W., Sher, A., Littman, D. R. (2000) Analysis of fractalkine receptor CX(3) CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol. Cell. Biol. 20, 4106–4114.
20. Saederup, N., Cardona, A. E., Croft, K., Mizutani, M., Cotleur, A. C., Tsou, C. L., Ransohoff, R. M., Charo, I. F. (2010) Selective chemokine receptor usage by central nervous system myeloid cells in CCR2-red fluorescent protein knock-in mice. PLoS ONE 5, e13693.
21. Burnett, S. H., Kershen, E. J., Zhang, J., Zeng, L., Straley, S. C., Kaplan, A. M., Cohen, D. A. (2004) Conditional macrophage ablation in transgenic mice expressing a Fas-based suicide gene. J. Leukoc. Biol. 75, 612–623.
22. Landsman, L., Bar-On, L., Zernecke, A., Kim, K. W., Krauthgamer, R., Shagdarsuren, E., Lira, S. A., Weissman, I. L., Weber, C., Jung, S. (2009) CX3CR1 is required for monocyte homeostasis and atherogenesis by promoting cell survival. Blood 113, 963–972.
23. Serbina, N. V., Pamer, E. G. (2006) Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR 2. Nat. Immunol. 7, 311–317.
24. Mazo, I. B., Gutierrez-Ramos, J. C., Frenette, P. S., Hynes, R. O., Wagner, D. D., von Andrian, U. H. (1998) Hematopoietic progenitor cell rolling in bone marrow microvessels: parallel contributions by endothelial selectins and vascular cell adhesion molecule 1. J. Exp. Med. 188, 465–474.
25. Li, J. L., Goh, C. C., Keeble, J L.,Qin, J. S., Roediger, B., Jain, R.,Wang, Y, Chew, W. K.,Weninger, W., Ng, L. G. (2012) Intravital multiphoton imaging of immune responses in the mouse ear skin. Nat. Protoc. 7, 221–234.
26. Sapoznikov, A., Pewzner-Jung, Y., Kalchenko, V., Krauthgamer, R., Shachar, I., Jung, S. (2008) Perivascular clusters of dendritic cells provide critical survival signals to B cells in bone marrow niches. Nat. Immunol. 9, 388–395.
27. Jung, S., Unutmaz, D., Wong, P., Sano, G., De los Santos, K., Sparwasser, T., Wu, S., Vuthoori, S., Ko, K., Zavala, F., Pamer, E. G., Littman, D. R., Lang, R. A. (2002) In vivo depletion of CD11c+ dendritic cells abrogates priming of CD8+ T cells by exogenous cell-associated antigens. Immunity 17, 211–220.
28. Probst, H. C., Tschannen, K., Odermatt, B., Schwendener, R., Zinkernagel, R. M., Van Den Broek, M. (2005) Histological analysis of CD11c-DTR/GFP mice after in vivo depletion of dendritic cells. Clin. Exp. Immunol. 141, 398–404.
29. Tittel, A. P., Heuser, C., Ohliger, C., Llanto, C., Yona, S., Hämmerling, G. J., Engel, D. R., Garbi, N., Kurts, C. (2012) Functionally relevant neutrophilia in CD11c diphtheria toxin receptor transgenic mice. Nat. Methods 9, 385–390.
30. Merad, M., Sathe, P., Helft, J., Miller, J., Mortha, A. (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.
31. Onai, N., Obata-Onai, A., Schmid, M. A., Manz, M. G. (2007) Flt3 in regulation of type I interferon-producing cell and dendritic cell development. Ann. N. Y. Acad. Sci. 1106, 253–261.
32. Wiktor-Jedrzejczak, W., Bartocci, A., Ferrante, Jr., A. W., Ahmed-Ansari, A., Sell, K. W., Pollard, J. W., Stanley, E. R. (1990) Total absence of colony-stimulating factor 1 in the macrophage-deficient osteopetrotic (op/op) mouse. Proc. Natl. Acad. Sci. USA 87, 4828–4832.
33. Dai, X. M., Ryan, G. R., Hapel, A. J., Dominguez, M. G., Russell, R. G., Kapp, S., Sylvestre, V., Stanley, E. R. (2002) Targeted disruption of the mouse colony-stimulating factor 1 receptor gene results in osteopetrosis, mononuclear phagocyte deficiency, increased primitive progenitor cell frequencies, and reproductive defects. Blood 99, 111–120.
34. Shi, C., Jia, T., Mendez-Ferrer, S., Hohl, T. M., Serbina, N. V., Lipuma, L., Leiner, I., Li, M. O., Frenette, P. S., Pamer, E. G. (2011) Bone marrow mesenchymal stem and progenitor cells induce monocyte emigration in response to circulating Toll-like receptor ligands. Immunity 34, 590–601.