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Contrast Media & Molecular Imaging
Volume 2017, Article ID 3127908, 8 pages
https://doi.org/10.1155/2017/3127908
Research Article

Fibered Confocal Fluorescence Microscopy for the Noninvasive Imaging of Langerhans Cells in Macaques

1CEA, Université Paris Sud 11, INSERM U1184, Immunology of Viral Infections and Autoimmune Diseases Research Center, IDMIT Infrastructure, 92265 Fontenay-aux-Roses, France
2Vaccine Research Institute (VRI), Créteil, France
3CEA, Institute of Biomedical Imaging (I2BM), DSV/I2BM/SHFJ/INSERM U1023, CEA, Orsay, France

Correspondence should be addressed to Catherine Chapon; rf.aec@nopahc.enirehtac

Received 24 February 2017; Revised 28 April 2017; Accepted 8 May 2017; Published 7 June 2017

Academic Editor: Fijs W. B. Van Leeuwen

Copyright © 2017 Biliana Todorova et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. N. Romani, B. E. Clausen, and P. Stoitzner, “Langerhans cells and more: langerin-expressing dendritic cell subsets in the skin,” Immunological Reviews, vol. 234, no. 1, pp. 120–141, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. J. Seneschal, R. A. Clark, A. Gehad, C. M. Baecher-Allan, and T. S. Kupper, “Human epidermal Langerhans cells maintain immune homeostasis in skin by activating skin resident regulatory T cells,” Immunity, vol. 36, no. 5, pp. 873–884, 2012. View at Publisher · View at Google Scholar · View at Scopus
  3. A. Bobr, I. Olvera-Gomez, B. Z. Igyarto, K. M. Haley, K. A. Hogquist, and D. H. Kaplan, “Acute ablation of Langerhans cells enhances skin immune responses,” Journal of Immunology, vol. 185, no. 8, pp. 4724–4728, 2010. View at Publisher · View at Google Scholar · View at Scopus
  4. C. Liard, S. Munier, A. Joulin-Giet et al., “Intradermal immunization triggers epidermal langerhans cell mobilization required for CD8 T-cell immune responses,” Journal of Investigative Dermatology, vol. 132, no. 3, pp. 615–625, 2012. View at Publisher · View at Google Scholar · View at Scopus
  5. T. Rattanapak, J. C. Birchall, K. Young et al., “Dynamic visualization of dendritic cell-antigen interactions in the skin following transcutaneous immunization,” PLoS ONE, vol. 9, no. 2, Article ID e89503, 2014. View at Publisher · View at Google Scholar · View at Scopus
  6. M. Kreutz, S. Karrer, P. Hoffmann et al., “Whole-body UVB irradiation during allogeneic hematopoietic cell transplantation is safe and decreases acute graft-versus-host disease,” Journal of Investigative Dermatology, vol. 132, no. 1, pp. 179–187, 2012. View at Publisher · View at Google Scholar · View at Scopus
  7. M. Merad, P. Hoffmann, E. Ranheim et al., “Depletion of host Langerhans cells before transplantation of donor alloreactive T cells prevents skin graft-versus-host disease,” Nature Medicine, vol. 10, pp. 510–517, 2004. View at Publisher · View at Google Scholar
  8. P. Stoitzner, L. K. Green, J. Y. Jung et al., “Tumor immunotherapy by epicutaneous immunization requires langerhans cells,” The Journal of Immunology, vol. 180, pp. 1991–1998. View at Publisher · View at Google Scholar
  9. F. L. Shaw, M. Cumberbatch, C. E. Kleyn et al., “Langerhans cell mobilization distinguishes between early-onset and late-onset psoriasis,” Journal of Investigative Dermatology, vol. 130, no. 7, pp. 1940–1942, 2010. View at Publisher · View at Google Scholar · View at Scopus
  10. K. Kautz-Neu, M. Noordegraaf, S. Dinges et al., “Langerhans cells are negative regulators of the anti-Leishmania response,” The Journal of Experimental Medicine, vol. 208, no. 5, pp. 885–891, 2011. View at Publisher · View at Google Scholar · View at Scopus
  11. J. Helft, F. Ginhoux, M. Bogunovic, and M. Merad, “Origin and functional heterogeneity of non-lymphoid tissue dendritic cells in mice,” Immunological Reviews, vol. 234, no. 1, pp. 55–75, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. R. L. Lindquist, G. Shakhar, D. Dudziak et al., “Visualizing dendritic cell networks in vivo,” Nature Immunology, vol. 5, pp. 1243–1250, 2004. View at Publisher · View at Google Scholar
  13. A. Kissenpfennig and B. Malissen, “Langerhans cells - Revisiting the paradigm using genetically engineered mice,” Trends in Immunology, vol. 27, no. 3, pp. 132–139, 2006. View at Publisher · View at Google Scholar · View at Scopus
  14. D. Sen, L. Forrest, T. B. Kepler, I. Parker, and M. D. Cahalan, “Selective and site-specific mobilization of dermal dendritic cells and Langerhans cells by Th1- and Th2-polarizing adjuvants,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 18, pp. 8334–8339, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. S. Celli, M. L. Albert, and P. Bousso, “Visualizing the innate and adaptive immune responses underlying allograft rejection by two-photon microscopy,” Nature Medicine, vol. 17, no. 6, pp. 744–749, 2011. View at Publisher · View at Google Scholar · View at Scopus
  16. M. Derieppe, A. Yudina, M. Lepetit-Coiffé, B. D. De Senneville, C. Bos, and C. Moonen, “Real-time assessment of ultrasound-mediated drug delivery using fibered confocal fluorescence microscopy,” Molecular Imaging and Biology, vol. 15, no. 1, pp. 3–11, 2013. View at Publisher · View at Google Scholar · View at Scopus
  17. B. Mahe, A. Vogt, C. Liard et al., “Nanoparticle-based targeting of vaccine compounds to skin antigen-presenting cells by hair follicles and their transport in mice,” Journal of Investigative Dermatology, vol. 129, no. 5, pp. 1156–1164, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. J. Bai, J. T. Wang, K. Mei et al., “Real-time monitoring of magnetic drug targeting using fibered confocal fluorescence microscopy,” Journal of Controlled Release, 2016. View at Publisher · View at Google Scholar
  19. V. Fitoussi, N. Faye, F. Chamming's, O. Clement, C.-A. Cuenod, and L. S. Fournier, “In vivo imaging of tumor angiogenesis using fluorescence confocal videomicroscopy,” Journal of Visualized Experiments, no. 79, Article ID e50347, 2013. View at Publisher · View at Google Scholar · View at Scopus
  20. K. H. Al-Gubory, “Fibered confocal fluorescence microscopy for imaging apoptotic DNA fragmentation at the single-cell level in vivo,” Experimental Cell Research, vol. 310, no. 2, pp. 474–481, 2005. View at Publisher · View at Google Scholar · View at Scopus
  21. S. Eser, M. Messer, P. Eser et al., “In vivo diagnosis of murine pancreatic intraepithelial neoplasia and early-stage pancreatic cancer by molecular imaging,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 24, pp. 9945–9950, 2011. View at Publisher · View at Google Scholar · View at Scopus
  22. H. Morisse, L. Heyman, M. Salaün et al., “In vivo molecular microimaging of pulmonary aspergillosis,” Medical Mycology, vol. 51, no. 4, pp. 352–360, 2013. View at Publisher · View at Google Scholar · View at Scopus
  23. S. F. Elahi, Z. Liu, K. E. Luker, R. S. Kwon, G. D. Luker, and T. D. Wang, “Longitudinal molecular imaging with single cell resolution of disseminated ovarian cancer in mice with a LED-based confocal microendoscope,” Molecular Imaging and Biology, vol. 13, no. 6, pp. 1157–1162, 2011. View at Publisher · View at Google Scholar · View at Scopus
  24. L. D. Swindle, S. G. Thomas, M. Freeman, and P. M. Delaney, “View of Normal Human Skin In Vivo as Observed Using Fluorescent Fiber-Optic Confocal Microscopic Imaging,” Journal of Investigative Dermatology, vol. 121, no. 4, pp. 706–712, 2003. View at Publisher · View at Google Scholar · View at Scopus
  25. C. Suihko and J. Serup, “Fluorescent fibre-optic confocal imaging of lesional and non-lesional psoriatic skin compared with normal skin in vivo,” Skin Research and Technology, vol. 18, no. 4, pp. 397–404, 2012. View at Publisher · View at Google Scholar · View at Scopus
  26. J. Tan, M. A. Quinn, J. M. Pyman, P. M. Delaney, and W. J. McLaren, “Detection of cervical intraepithelial neoplasia in vivo using confocal endomicroscopy,” BJOG: An International Journal of Obstetrics and Gynaecology, vol. 116, no. 12, pp. 1663–1670, 2009. View at Publisher · View at Google Scholar · View at Scopus
  27. A. L. Polglase, W. J. McLaren, S. A. Skinner, R. Kiesslich, M. F. Neurath, and P. M. Delaney, “A fluorescence confocal endomicroscope for in vivo microscopy of the upper- and the lower-GI tract,” Gastrointestinal Endoscopy, vol. 62, no. 5, pp. 686–695, 2005. View at Publisher · View at Google Scholar · View at Scopus
  28. R. Atreya, H. Neumann, C. Neufert et al., “In vivo imaging using fluorescent antibodies to tumor necrosis factor predicts therapeutic response in Crohn's disease,” Nature Medicine, vol. 20, no. 3, pp. 313–318, 2014. View at Publisher · View at Google Scholar · View at Scopus
  29. O. Epaulard, L. Adam, C. Poux et al., “Macrophage-and neutrophil-derived TNF-α instructs skin Langerhans cells to prime antiviral immune responses,” Journal of Immunology, vol. 193, no. 5, pp. 2416–2426, 2014. View at Publisher · View at Google Scholar · View at Scopus
  30. L. Adam, P. Rosenbaum, A. Cosma, R. Le Grand, and F. Martinon, “Identification of skin immune cells in non-human primates,” Journal of Immunological Methods, vol. 426, pp. 42–49, 2015. View at Publisher · View at Google Scholar · View at Scopus
  31. M. Vishwanath, A. Nishibu, S. Saeland et al., “Development of intravital intermittent confocal imaging system for studying Langerhans cell turnover,” Journal of Investigative Dermatology, vol. 126, no. 11, pp. 2452–2457, 2006. View at Publisher · View at Google Scholar · View at Scopus
  32. A. Kissenpfennig, S. Henri, B. Dubois et al., “Dynamics and function of Langerhans cells in vivo: dermal dendritic cells colonize lymph node areas distinct from slower migrating Langerhans cells,” Immunity 22, pp. 643–654, 2005. View at Publisher · View at Google Scholar
  33. L. Eidsmo, R. Allan, I. Caminschi, N. Van Rooijen, W. R. Heath, and F. R. Carbone, “Differential migration of epidermal and dermal dendritic cells during skin infection,” Journal of Immunology, vol. 182, no. 5, pp. 3165–3172, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. K. Furmanov, M. Elnekave, D. Lehmann, B. E. Clausen, D. N. Kotton, and A.-H. Hovav, “The role of skin-derived dendritic cells in CD8+ T cell priming following immunization with lentivectors,” Journal of Immunology, vol. 184, no. 9, pp. 4889–4897, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. M. J. Miller, A. S. Hejazi, S. H. Wei, M. D. Cahalan, and I. Parker, “T cell repertoire scanning is promoted by dynamic dendritic cell behavior and random T cell motility in the lymph node,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 4, pp. 998–1003, 2004. View at Publisher · View at Google Scholar · View at Scopus
  36. D. Sen, T. J. Deerinck, M. H. Ellisman, I. Parker, and M. D. Cahalan, “Quantum dots for tracking dendritic cells and priming an immune response in vibtro and in vivo,” PLoS ONE, vol. 3, no. 9, Article ID e3290, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. G. Romain, E. van Gulck, O. Epaulard et al., “CD34-derived dendritic cells transfected ex vivo with HIV-Gag mRNA induce polyfunctional T-cell responses in nonhuman primates,” European Journal of Immunology, vol. 42, no. 8, pp. 2019–2030, 2012. View at Publisher · View at Google Scholar · View at Scopus
  38. N. A. Monteiro-Riviere, D. G. Bristol, T. O. Manning, R. A. Rogers, and J. E. Riviere, “Interspecies and interregional analysis of the comparative histologic thickness and laser Doppler blood flow measurements at five cutaneous sites in nine species,” Journal of Investigative Dermatology, vol. 95, no. 5, pp. 582–586, 1990. View at Publisher · View at Google Scholar · View at Scopus
  39. K. Robertson and J. L. Rees, “Variation in epidermal morphology in human skin at different body sites as measured by reflectance confocal microscopy,” Acta Dermato-Venereologica, vol. 90, no. 4, pp. 368–373, 2010. View at Publisher · View at Google Scholar · View at Scopus
  40. D. Hanau, M. Fabre, D. A. Schmitt et al., “Human epidermal Langerhans cells cointernalize by receptor-mediated endocytosis 'nonclassical' major histocompatibility complex class I molecules (T6 antigens) and class II molecules (HLA-DR antigens),” Proceedings of the National Academy of Sciences of the United States of America, vol. 84, no. 9, pp. 2901–2905, 1987. View at Publisher · View at Google Scholar · View at Scopus
  41. V. Flacher, C. H. Tripp, P. Stoitzner et al., “Epidermal langerhans cells rapidly capture and present antigens from C-type lectin-targeting antibodies deposited in the dermis,” Journal of Investigative Dermatology, vol. 130, no. 3, pp. 755–762, 2010. View at Publisher · View at Google Scholar · View at Scopus
  42. N. Salabert, B. Todorova, F. Martinon et al., “Intradermal injection of an anti-Langerin-HIVGag fusion vaccine targets epidermal Langerhans cells in nonhuman primates and can be tracked in vivo,” European Journal of Immunology, vol. 46, no. 3, pp. 689–700, 2016. View at Publisher · View at Google Scholar · View at Scopus
  43. H. D. Moreau, F. Lemaître, E. Terriac et al., “Dynamic in situ cytometry uncovers T cell receptor signaling during immunological synapses and kinapses in vivo,” Immunity, vol. 37, no. 2, pp. 351–363, 2012. View at Publisher · View at Google Scholar · View at Scopus
  44. Z. Garcia, F. Lemaître, N. van Rooijen et al., “Subcapsular sinus macrophages promote NK cell accumulation and activation in response to lymph-borne viral particles,” Blood, vol. 120, no. 24, pp. 4744–4750, 2012. View at Publisher · View at Google Scholar · View at Scopus
  45. F. Progatzky, M. J. Dallman, and C. L. Celso, “From seeing to believing: Labelling strategies for in vivo cell-tracking experiments,” Interface Focus, vol. 3, no. 3, 2013. View at Publisher · View at Google Scholar · View at Scopus