The phagocytosis of gas-filled microbubbles by human and murine antigen-presenting cells

Biomaterials

Volumn 33, Issue 1, 2012, Pages 333-342

  Bioley, Gilles ^a   Bussat, Philippe ^b   Lassus, Anne ^b   Schneider, Michel ^b   Terrettaz, Jacques ^b   Corthésy, Blaise ^a  

^a LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^b Bracco Suisse SA   (Switzerland)

Author keywords

Antigen presenting cells; Cellular uptake; Dendritic cells; Gas filled microbubbles; Microparticles

Indexed keywords

ANTIGEN PRESENTING CELLS; CELLULAR UPTAKE; DENDRITIC CELLS; MICRO-PARTICLES; MICROBUBBLES;

ANTIGEN-ANTIBODY REACTIONS; ANTIGENS; BIOLOGICAL MEMBRANES; BODY FLUIDS; CONFOCAL MICROSCOPY; CYTOLOGY; MAMMALS; MONOCLONAL ANTIBODIES;

CELLS;

CD11 ANTIGEN;

ANIMAL CELL; ANIMAL TISSUE; ANTIGEN PRESENTING CELL; ARTICLE; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; CYTOPLASM; DENDRITIC CELL; FEMALE; HUMAN; IN VITRO STUDY; MICROBUBBLE; MONOCYTE; MOUSE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; ULTRASOUND;

ANIMALS; ANTIGEN-PRESENTING CELLS; CELL LINE; CELL LINE, TUMOR; DENDRITIC CELLS; GASES; HUMANS; MICE; MICROBUBBLES; PHAGOCYTOSIS;

MURINAE; MUS;

EID: 82855172090     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2011.09.045     Document Type: Article

References (60)

1. Ueno H., Klechevsky E., Morita R., Aspord C., Cao T., Matsui T., et al. Dendritic cell subsets in health and disease. Immunol Rev 2007, 219:118-142.
2. Raychaudhuri S., Rock K.L. Fully mobilizing host defense: building better vaccines. Nat Biotechnol 1998, 16:1025-1031.
3. Kovacsovics-Bankowski M., Clark K., Benacerraf B., Rock K.L. Efficient major histocompatibility complex class I presentation of exogenous antigen upon phagocytosis by macrophages. Proc Natl Acad Sci U S A 1993, 90:4942-4946.
4. Falo L.D., Kovacsovics-Bankowski M., Thompson K., Rock K.L. Targeting antigen into the phagocytic pathway in vivo induces protective tumour immunity. Nat Med 1995, 1:649-653.
5. Shen Z., Reznikoff G., Dranoff G., Rock K.L. Cloned dendritic cells can present exogenous antigens on both MHC class I and class II molecules. J Immunol 1997, 158:2723-2730.
6. Burgdorf S., Kurts C. Endocytosis mechanisms and the cell biology of antigen presentation. Curr Opin Immunol 2008, 20:89-95.
7. Kumari S., Mg S., Mayor S. Endocytosis unplugged: multiple ways to enter the cell. Cell Res 2010, 20:256-275.
8. Copland M.J., Rades T., Davies N.M., Baird M.A. Lipid based particulate formulations for the delivery of antigen. Immunol Cell Biol 2005, 83:97-105.
9. Reddy S.T., Swartz M.A., Hubbell J.A. Targeting dendritic cells with biomaterials: developing the next generation of vaccines. Trends Immunol 2006, 27:573-579.
10. Jilek S., Walter E., Merkle H.P., Corthesy B. Modulation of allergic responses in mice by using biodegradable poly(lactide-co-glycolide) microspheres. J Allergy Clin Immunol 2004, 114:943-950.
11. Vordermeier H.M., Coombes A.G., Jenkins P., McGee J.P., O'Hagan D.T., Davis S.S., et al. Synthetic delivery system for tuberculosis vaccines: immunological evaluation of the M. tuberculosis 38 kDa protein entrapped in biodegradable PLG microparticles. Vaccine 1995, 13:1576-1582.
12. O'Hagan D., Singh M., Ugozzoli M., Wild C., Barnett S., Chen M., et al. Induction of potent immune responses by cationic microparticles with adsorbed human immunodeficiency virus DNA vaccines. J Virol 2001, 75:9037-9043.
13. Chong C.S., Cao M., Wong W.W., Fischer K.P., Addison W.R., Kwon G.S., et al. Enhancement of T helper type 1 immune responses against hepatitis B virus core antigen by PLGA nanoparticle vaccine delivery. J Control Release 2005, 102:85-99.
14. Feng L., Qi X.R., Zhou X.J., Maitani Y., Wang S.C., Jiang Y., et al. Pharmaceutical and immunological evaluation of a single-dose hepatitis B vaccine using PLGA microspheres. J Control Release 2006, 112:35-42.
15. Taneichi M., Ishida H., Kajino K., Ogasawara K., Tanaka Y., Kasai M., et al. Antigen chemically coupled to the surface of liposomes are cross-presented to CD8+ T cells and induce potent antitumor immunity. J Immunol 2006, 177:2324-2330.
16. Perrie Y., Frederik P.M., Gregoriadis G. Liposome-mediated DNA vaccination: the effect of vesicle composition. Vaccine 2001, 19:3301-3310.
17. Cui Z., Huang L. Liposome-polycation-DNA (LPD) particle as a carrier and adjuvant for protein-based vaccines: therapeutic effect against cervical cancer. Cancer Immunol Immunother 2005, 54:1180-1190.
18. Kamath A.T., Rochat A.F., Christensen D., Agger E.M., Andersen P., Lambert P.H., et al. A liposome-based mycobacterial vaccine induces potent adult and neonatal multifunctional T cells through the exquisite targeting of dendritic cells. PLoS One 2009, 4:e5771.
19. Collins D.S., Findlay K., Harding C.V. Processing of exogenous liposome-encapsulated antigens in vivo generates class I MHC-restricted T cell responses. J Immunol 1992, 148:3336-3341.
20. Jilek S., Ulrich M., Merkle H.P., Walter E. Composition and surface charge of DNA-loaded microparticles determine maturation and cytokine secretion in human dendritic cells. Pharm Res 2004, 21:1240-1247.
21. Phillips N.C., Gagne L., Ivanoff N., Riveau G. Influence of phospholipid composition on antibody responses to liposome encapsulated protein and peptide antigens. Vaccine 1996, 14:898-904.
22. Vangasseri D.P., Cui Z., Chen W., Hokey D.A., Falo L.D., Huang L. Immunostimulation of dendritic cells by cationic liposomes. Mol Membr Biol 2006, 23:385-395.
23. Lindner J.R. Microbubbles in medical imaging: current applications and future directions. Nat Rev Drug Discov 2004, 3:527-532.
24. Keller M.W., Feinstein S.B., Watson D.D. Successful left ventricular opacification following peripheral venous injection of sonicated contrast agent: an experimental evaluation. Am Heart J 1987, 114:570-575.
25. Coley B.D., Trambert M.A., Mattrey R.F. Perfluorocarbon-enhanced sonography: value in detecting acute venous thrombosis in rabbits. AJR Am J Roentgenol 1994, 163:961-964.
26. Schneider M., Arditi M., Barrau M.B., Brochot J., Broillet A., Ventrone R., et al. BR1: a new ultrasonographic contrast agent based on sulfur hexafluoride-filled microbubbles. Invest Radiol 1995, 30:451-457.
27. Hernot S., Klibanov A.L. Microbubbles in ultrasound-triggered drug and gene delivery. Adv Drug Deliv Rev 2008, 60:1153-1166.
28. Tinkov S., Bekeredjian R., Winter G., Coester C. Microbubbles as ultrasound triggered drug carriers. J Pharm Sci 2009, 98:1935-1961.
29. Miller D.L. Overview of experimental studies of biological effects of medical ultrasound caused by gas body activation and inertial cavitation. Prog Biophys Mol Biol 2007, 93:314-330.
30. Miller D.L., Quddus J. Sonoporation of monolayer cells by diagnostic ultrasound activation of contrast-agent gas bodies. Ultrasound Med Biol 2000, 26:661-667.
31. Anwer K., Kao G., Proctor B., Anscombe I., Florack V., Earls R., et al. Ultrasound enhancement of cationic lipid-mediated gene transfer to primary tumors following systemic administration. Gene Ther 2000, 7:1833-1839.
32. Takahashi M., Kido K., Aoi A., Furukawa H., Ono M., Kodama T. Spinal gene transfer using ultrasound and microbubbles. J Control Release 2007, 117:267-272.
33. Sallusto F., Lanzavecchia A. Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha. J Exp Med 1994, 179:1109-1118.
34. Lee H., Terry E., Zong M., Arrowsmith N., Perrier S., Thurecht K.J., et al. Successful dispersion polymerization in supercritical CO2 using polyvinylalkylate hydrocarbon surfactants synthesized and anchored via RAFT. J Am Chem Soc 2008, 130:12242-12243.
35. Newman C.M., Bettinger T. Gene therapy progress and prospects: ultrasound for gene transfer. Gene Ther 2007, 14:465-475.
36. Schlicher R.K., Radhakrishna H., Tolentino T.P., Apkarian R.P., Zarnitsyn V., Prausnitz M.R. Mechanism of intracellular delivery by acoustic cavitation. Ultrasound Med Biol 2006, 32:915-924.
37. Lanzavecchia A., Sallusto F. Regulation of T cell immunity by dendritic cells. Cell 2001, 106:263-266.
38. Lemmon J.C., McFarland R.J., Rybicka J.M., Balce D.R., McKeown K.R., Krohn R.M., et al. In vitro and in vivo transfection of primary phagocytes via microbubble-mediated intraphagosomal sonoporation. J Immunol Methods 2011, 371:152-158.
39. Lindner J.R., Dayton P.A., Coggins M.P., Ley K., Song J., Ferrara K., et al. Noninvasive imaging of inflammation by ultrasound detection of phagocytosed microbubbles. Circulation 2000, 102:531-538.
40. Lindner J.R., Coggins M.P., Kaul S., Klibanov A.L., Brandenburger G.H., Ley K. Microbubble persistence in the microcirculation during ischemia/reperfusion and inflammation is caused by integrin- and complement-mediated adherence to activated leukocytes. Circulation 2000, 101:668-675.
41. Yanagisawa K., Moriyasu F., Miyahara T., Yuki M., Iijima H. Phagocytosis of ultrasound contrast agent microbubbles by Kupffer cells. Ultrasound Med Biol 2007, 33:318-325.
42. Takeuchi H., Ohmori K., Kondo I., Shinomiya K., Oshita A., Takagi Y., et al. Interaction with leukocytes: phospholipid-stabilized versus albumin-shell microbubbles. Radiology 2004, 230:735-742.
43. Wischke C., Borchert H.H., Zimmermann J., Siebenbrodt I., Lorenzen D.R. Stable cationic microparticles for enhanced model antigen delivery to dendritic cells. J Control Release 2006, 114:359-368.
44. Christensen D., Agger E.M., Andreasen L.V., Kirby D., Andersen P., Perrie Y. Liposome-based cationic adjuvant formulations (CAF): past, present, and future. J Liposome Res 2009, 19:2-11.
45. Manolova V., Flace A., Bauer M., Schwarz K., Saudan P., Bachmann M.F. Nanoparticles target distinct dendritic cell populations according to their size. Eur J Immunol 2008, 38:1404-1413.
46. Reddy S.T., Rehor A., Schmoekel H.G., Hubbell J.A., Swartz M.A. In vivo targeting of dendritic cells in lymph nodes with poly(propylene sulfide) nanoparticles. J Control Release 2006, 112:26-34.
47. Itano A.A., McSorley S.J., Reinhardt R.L., Ehst B.D., Ingulli E., Rudensky A.Y., et al. Distinct dendritic cell populations sequentially present antigen to CD4 T cells and stimulate different aspects of cell-mediated immunity. Immunity 2003, 19:47-57.
48. Allan R.S., Waithman J., Bedoui S., Jones C.M., Villadangos J.A., Zhan Y., et al. Migratory dendritic cells transfer antigen to a lymph node-resident dendritic cell population for efficient CTL priming. Immunity 2006, 25:153-162.
49. Kamath A.T., Henri S., Battye F., Tough D.F., Shortman K. Developmental kinetics and lifespan of dendritic cells in mouse lymphoid organs. Blood 2002, 100:1734-1741.
50. Randolph G.J., Inaba K., Robbiani D.F., Steinman R.M., Muller W.A. Differentiation of phagocytic monocytes into lymph node dendritic cells in vivo. Immunity 1999, 11:753-761.
51. Goldberg B.B., Merton D.A., Liu J.B., Murphy G., Forsberg F. Contrast-enhanced sonographic imaging of lymphatic channels and sentinel lymph nodes. J Ultrasound Med 2005, 24:953-965.
52. Wisner E.R., Ferrara K.W., Short R.E., Ottoboni T.B., Gabe J.D., Patel D. Sentinel node detection using contrast-enhanced power Doppler ultrasound lymphography. Invest Radiol 2003, 38:358-365.
53. Wang Y., Wang W., Li J., Tang J. Gray-scale contrast-enhanced ultrasonography of sentinel lymph nodes in a metastatic breast cancer model. Acad Radiol 2009, 16:957-962.
54. Nielsen K.R., Grossjohann H.S., Hansen C.P., Nielsen M.B. Use of contrast-enhanced ultrasound imaging to detect the first draining lymph node (FDLN) in a swine model: correlation of imaging findings with the distance from the injection site to the FDLN. J Ultrasound Med 2008, 27:1203-1209.
55. Rue Nielsen K., Klyver H., Hougaard Chakera A., Nedergaard L., Hesse B., Bachmann Nielsen M. Sentinel node detection in melanomas using contrast-enhanced ultrasound. Acta Radiol 2009, 50:412-417.
56. Swartz M.A., Hubbell J.A., Reddy S.T. Lymphatic drainage function and its immunological implications: from dendritic cell homing to vaccine design. Semin Immunol 2008, 20:147-156.
57. Kadowaki N. The divergence and interplay between pDC and mDC in humans. Front Biosci 2009, 14:808-817.
58. Heurtault B., Frisch B., Pons F. Liposomes as delivery systems for nasal vaccination: strategies and outcomes. Expert Opin Drug Deliv 2010, 7:829-844.
59. Fenske D.B., Cullis P.R. Liposomal nanomedicines. Expert Opin Drug Deliv 2008, 5:25-44.
60. Samad A., Sultana Y., Aqil M. Liposomal drug delivery systems: an update review. Curr Drug Deliv 2007, 4:297-305.