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Nanocarriers and Immune Cells

  • Lorna Moll
  • Volker MailänderEmail author
Chapter
Part of the NanoScience and Technology book series (NANO)

Abstract

Nanocarriers (NCs) have a high potential as target-specific drug-delivery system. Especially immune cells are a prime target in the nanoparticle-cell interaction. Uptake into the correct subtype of immune cells is crucial. Therefore uptake processes as well as intracellular processing is of utmost importance. The so-called protein corona heavily affects the interaction with immune cells which can decide the fate of the NC for degradation. On a wider perspective also nanoparticles which were not intentionally made for the transport of drugs get in contact with immune cells e.g. in the lungs. These immune cells are then trying to degrade these foreign materials.

References

  1. 1.
    Boraschi, D., Costantino, L., Italiani, P.: Interaction of nanoparticles with immunocompetent cells: nanosafety considerations. Nanomedicine (Lond.) 7(1), 121–131 (2012)CrossRefGoogle Scholar
  2. 2.
    Walkey, C.D., Chan, W.C.: Understanding and controlling the interaction of nanomaterials with proteins in a physiological environment. Chem. Soc. Rev. 41(7), 2780–2799 (2012)CrossRefGoogle Scholar
  3. 3.
    Hellstrand, E., Lynch, I., Andersson, A., Drakenberg, T., Dahlback, B., Dawson, K.A., et al.: Complete high-density lipoproteins in nanoparticle corona. FEBS J. 276(12), 3372–3381 (2009)CrossRefGoogle Scholar
  4. 4.
    Milani, S., Bombelli, F.B., Pitek, A.S., Dawson, K.A., Radler, J.: Reversible versus irreversible binding of transferrin to polystyrene nanoparticles: soft and hard corona. ACS Nano 6(3), 2532–2541 (2012)CrossRefGoogle Scholar
  5. 5.
    Cedervall, T., Lynch, I., Lindman, S., Berggard, T., Thulin, E., Nilsson, H., et al.: Understanding the nanoparticle-protein corona using methods to quantify exchange rates and affinities of proteins for nanoparticles. Proc. Natl. Acad. Sci. U.S.A. 104(7), 2050–2055 (2007)CrossRefADSGoogle Scholar
  6. 6.
    Lundqvist, M., Stigler, J., Elia, G., Lynch, I., Cedervall, T., Dawson, K.A.: Nanoparticle size and surface properties determine the protein corona with possible implications for biological impacts. Proc. Natl. Acad. Sci. U.S.A. 105(38), 14265–14270 (2008)CrossRefADSGoogle Scholar
  7. 7.
    Maiorano, G., Sabella, S., Sorce, B., Brunetti, V., Malvindi, M.A., Cingolani, R., et al.: Effects of cell culture media on the dynamic formation of protein-nanoparticle complexes and influence on the cellular response. ACS Nano 4(12), 7481–7491 (2010)CrossRefGoogle Scholar
  8. 8.
    Ghavami, M., Rezaei, M., Ejtehadi, R., Lotfi, M., Shokrgozar, M.A., Abd Emamy, B., et al.: Physiological temperature has a crucial role in amyloid beta in the absence and presence of hydrophobic and hydrophilic nanoparticles. ACS Chem. Neurosci. 4(3), 375–378 (2013)CrossRefGoogle Scholar
  9. 9.
    Mahmoudi, M., Abdelmonem, A.M., Behzadi, S., Clement, J.H., Dutz, S., Ejtehadi, M.R., et al.: Temperature: the “ignored” factor at the NanoBio interface. ACS Nano 7(8), 6555–6562 (2013)CrossRefGoogle Scholar
  10. 10.
    Limbach, L.K., Wick, P., Manser, P., Grass, R.N., Bruinink, A., Stark, W.J.: Exposure of engineered nanoparticles to human lung epithelial cells: influence of chemical composition and catalytic activity on oxidative stress. Environ. Sci. Technol. 41(11), 4158–4163 (2007)CrossRefADSGoogle Scholar
  11. 11.
    Byrne, B., Donohoe, G.G., O’Kennedy, R.: Sialic acids: carbohydrate moieties that influence the biological and physical properties of biopharmaceutical proteins and living cells. Drug Discov. Today. 12(7–8), 319–326 (2007)CrossRefGoogle Scholar
  12. 12.
    Kah, J.C., Wong, K.Y., Neoh, K.G., Song, J.H., Fu, J.W., Mhaisalkar, S., et al.: Critical parameters in the pegylation of gold nanoshells for biomedical applications: an in vitro macrophage study. J. Drug Target. 17(3), 181–193 (2009)CrossRefGoogle Scholar
  13. 13.
    Lin, S.Y., Hsu, W.H., Lo, J.M., Tsai, H.C., Hsiue, G.H.: Novel geometry type of nanocarriers mitigated the phagocytosis for drug delivery. J. Control. Release 154(1), 84–92 (2011)CrossRefGoogle Scholar
  14. 14.
    Janeway Jr., C.A., Medzhitov, R.: Innate immune recognition. Annu. Rev. Immunol. 20, 197–216 (2002)CrossRefGoogle Scholar
  15. 15.
    Steinman, R.M., Banchereau, J.: Taking dendritic cells into medicine. Nature 449(7161), 419–426 (2007)CrossRefADSGoogle Scholar
  16. 16.
    Janeway, C.A.: How the immune system works to protect the host from infection: a personal view. Proc. Natl. Acad. Sci. U.S.A. 98(13), 7461–7468 (2001)CrossRefADSGoogle Scholar
  17. 17.
    Dranoff, G.: Cytokines in cancer pathogenesis and cancer therapy. Nat. Rev. Cancer 4(1), 11–22 (2004)CrossRefGoogle Scholar
  18. 18.
    Zinkernagel, R.M.: On natural and artificial vaccinations. Annu. Rev. Immunol. 21, 515–546 (2003)CrossRefGoogle Scholar
  19. 19.
    Jenne, C.N., Liao, S., Singh, B.: Neutrophils: multitasking first responders of immunity and tissue homeostasis. Cell Tissue Res. (2018)Google Scholar
  20. 20.
    Mayadas, T.N., Cullere, X., Lowell, C.A.: The multifaceted functions of neutrophils. Annu. Rev. Pathol. 9, 181–218 (2014)CrossRefGoogle Scholar
  21. 21.
    Lin, A., Lore, K.: Granulocytes: new members of the antigen-presenting cell family. Front. Immunol. 8, 1781 (2017)CrossRefGoogle Scholar
  22. 22.
    Siracusa, M.C., Kim, B.S., Spergel, J.M., Artis, D.: Basophils and allergic inflammation. J. Allergy Clin. Immunol. 132(4), 789–801; quiz 788 (2013)Google Scholar
  23. 23.
    Guilliams, M., Ginhoux, F., Jakubzick, C., Naik, S.H., Onai, N., Schraml, B.U., et al.: Dendritic cells, monocytes and macrophages: a unified nomenclature based on ontogeny. Nat. Rev. Immunol. 14(8), 571–578 (2014)CrossRefGoogle Scholar
  24. 24.
    Geissmann, F., Manz, M.G., Jung, S., Sieweke, M.H., Merad, M., Ley, K.: Development of monocytes, macrophages, and dendritic cells. Science 327(5966), 656–661 (2010)CrossRefADSGoogle Scholar
  25. 25.
    Mosser, D.M., Edwards, J.P.: Exploring the full spectrum of macrophage activation. Nat. Rev. Immunol. 8(12), 958–969 (2008)CrossRefGoogle Scholar
  26. 26.
    Verreck, F.A., de Boer, T., Langenberg, D.M., Hoeve, M.A., Kramer, M., Vaisberg, E., et al.: Human IL-23-producing type 1 macrophages promote but IL-10-producing type 2 macrophages subvert immunity to (myco)bacteria. Proc. Natl. Acad. Sci. U.S.A. 101(13), 4560–4565 (2004)CrossRefADSGoogle Scholar
  27. 27.
    Murray, P.J., Allen, J.E., Biswas, S.K., Fisher, E.A., Gilroy, D.W., Goerdt, S., et al.: Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity 41(1), 14–20 (2014)CrossRefGoogle Scholar
  28. 28.
    Murray, P.J., Wynn, T.A.: Protective and pathogenic functions of macrophage subsets. Nat. Rev. Immunol. 11(11), 723–737 (2011)CrossRefGoogle Scholar
  29. 29.
    Buckwalter, M.R., Albert, M.L.: Orchestration of the immune response by dendritic cells. Curr. Biol. 19(9), R355–R361 (2009)CrossRefGoogle Scholar
  30. 30.
    Villadangos, J.A., Schnorrer, P.: Intrinsic and cooperative antigen-presenting functions of dendritic-cell subsets in vivo. Nat. Rev. Immunol. 7(7), 543–555 (2007)CrossRefGoogle Scholar
  31. 31.
    Heath, W.R., Belz, G.T., Behrens, G.M., Smith, C.M., Forehan, S.P., Parish, I.A., et al.: Cross-presentation, dendritic cell subsets, and the generation of immunity to cellular antigens. Immunol. Rev. 199, 9–26 (2004)CrossRefGoogle Scholar
  32. 32.
    Niess, J.H., Brand, S., Gu, X., Landsman, L., Jung, S., McCormick, B.A., et al.: CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science 307(5707), 254–258 (2005)CrossRefADSGoogle Scholar
  33. 33.
    Cyster, J.G.: Chemokines and the homing of dendritic cells to the T cell areas of lymphoid organs. J. Exp. Med. 189(3), 447–450 (1999)CrossRefGoogle Scholar
  34. 34.
    Itano, A.A., Jenkins, M.K.: Antigen presentation to naive CD4 T cells in the lymph node. Nat. Immunol. 4(8), 733–739 (2003)CrossRefGoogle Scholar
  35. 35.
    Randolph, G.J., Angeli, V., Swartz, M.A.: Dendritic-cell trafficking to lymph nodes through lymphatic vessels. Nat. Rev. Immunol. 5(8), 617–628 (2005)CrossRefGoogle Scholar
  36. 36.
    Gordon, J.R., Ma, Y., Churchman, L., Gordon, S.A., Dawicki, W.: Regulatory dendritic cells for immunotherapy in immunologic diseases. Front. Immunol. 5, 7 (2014)CrossRefGoogle Scholar
  37. 37.
    Kaisho, T., Akira, S.: Regulation of dendritic cell function through Toll-like receptors. Curr. Mol. Med. 3(4), 373–385 (2003)CrossRefGoogle Scholar
  38. 38.
    Krieg, A.M.: CpG motifs in bacterial DNA and their immune effects. Annu. Rev. Immunol. 20, 709–760 (2002)CrossRefGoogle Scholar
  39. 39.
    Verthelyi, D., Zeuner, R.A.: Differential signaling by CpG DNA in DCs and B cells: not just TLR9. Trends Immunol. 24(10), 519–522 (2003)CrossRefGoogle Scholar
  40. 40.
    Manzotti, C.N., Liu, M.K., Burke, F., Dussably, L., Zheng, Y., Sansom, D.M.: Integration of CD28 and CTLA-4 function results in differential responses of T cells to CD80 and CD86. Eur. J. Immunol. 36(6), 1413–1422 (2006)CrossRefGoogle Scholar
  41. 41.
    Odobasic, D., Kitching, A.R., Tipping, P.G., Holdsworth, S.R.: CD80 and CD86 costimulatory molecules regulate crescentic glomerulonephritis by different mechanisms. Kidney Int. 68(2), 584–594 (2005)CrossRefGoogle Scholar
  42. 42.
    Lenschow, D.J., Ho, S.C., Sattar, H., Rhee, L., Gray, G., Nabavi, N., et al.: Differential effects of anti-B7-1 and anti-B7-2 monoclonal antibody treatment on the development of diabetes in the nonobese diabetic mouse. J. Exp. Med. 181(3), 1145–1155 (1995)CrossRefGoogle Scholar
  43. 43.
    Xiang, J., Gu, X., Qian, S., Chen, Z.: Graded function of CD80 and CD86 in initiation of T-cell immune response and cardiac allograft survival. Transpl. Int. 21(2), 163–168 (2008)Google Scholar
  44. 44.
    Probst, H.C., McCoy, K., Okazaki, T., Honjo, T., van den Broek, M.: Resting dendritic cells induce peripheral CD8 + T cell tolerance through PD-1 and CTLA-4. Nat. Immunol. 6(3), 280–286 (2005)CrossRefGoogle Scholar
  45. 45.
    Hawiger, D., Inaba, K., Dorsett, Y., Guo, M., Mahnke, K., Rivera, M., et al.: Dendritic cells induce peripheral T cell unresponsiveness under steady state conditions in vivo. J. Exp. Med. 194(6), 769–779 (2001)CrossRefGoogle Scholar
  46. 46.
    Luo, X., Tarbell, K.V., Yang, H., Pothoven, K., Bailey, S.L., Ding, R., et al.: Dendritic cells with TGF-beta1 differentiate naive CD4+ CD25 T cells into islet-protective Foxp3+ regulatory T cells. Proc Natl Acad Sci U S A. 104(8), 2821–2826 (2007)CrossRefADSGoogle Scholar
  47. 47.
    Pulendran, B., Smith, J.L., Caspary, G., Brasel, K., Pettit, D., Maraskovsky, E., et al.: Distinct dendritic cell subsets differentially regulate the class of immune response in vivo. Proc. Natl. Acad. Sci. U.S.A. 96(3), 1036–1041 (1999)CrossRefADSGoogle Scholar
  48. 48.
    Maldonado-Lopez, R., De Smedt, T., Michel, P., Godfroid, J., Pajak, B., Heirman, C., et al.: CD8 alpha(+) and CD8 alpha(−) subclasses of dendritic cells direct the development of distinct T helper cells in vivo. J. Exp. Med. 189(3), 587–592 (1999)CrossRefGoogle Scholar
  49. 49.
    Napolitani, G., Rinaldi, A., Bertoni, F., Sallusto, F., Lanzavecchia, A.: Selected Toll-like receptor agonist combinations synergistically trigger a T helper type 1-polarizing program in dendritic cells. Nat. Immunol. 6(8), 769–776 (2005)CrossRefGoogle Scholar
  50. 50.
    Seder, R.A., Paul, W.E., Davis, M.M., Fazekas de St Groth, B.: The presence of interleukin 4 during in vitro priming determines the lymphokine-producing potential of CD4+ T cells from T cell receptor transgenic mice. J. Exp. Med. 176(4), 1091–1098 (1992)Google Scholar
  51. 51.
    LeibundGut-Landmann, S., Gross, O., Robinson, M.J., Osorio, F., Slack, E.C., Tsoni, S.V., et al.: Syk- and CARD9-dependent coupling of innate immunity to the induction of T helper cells that produce interleukin 17. Nat. Immunol. 8(6), 630–638 (2007)CrossRefGoogle Scholar
  52. 52.
    Jonuleit, H., Schmitt, E., Schuler, G., Knop, J., Enk, A.H.: Induction of interleukin 10-producing, nonproliferating CD4(+) T cells with regulatory properties by repetitive stimulation with allogeneic immature human dendritic cells. J. Exp. Med. 192(9), 1213–1222 (2000)CrossRefGoogle Scholar
  53. 53.
    Badovinac, V.P., Messingham, K.A.N., Jabbari, A., Haring, J.S., Harty, J.T.: Accelerated CD8(+) T-cell memory and prime-boost response after dendritic-cell vaccination. Nat. Med. 11(7), 748–756 (2005)CrossRefGoogle Scholar
  54. 54.
    Trumpfheller, C., Finke, J.S., Lopez, C.B., Moran, T.M., Moltedo, B., Soares, H., et al.: Intensified and protective CD4+ T cell immunity in mice with anti-dendritic cell HIV gag fusion antibody vaccine. J. Exp. Med. 203(3), 607–617 (2006)CrossRefGoogle Scholar
  55. 55.
    Amer, M.G., Mazen, N.F., Mohamed, A.M.: Caffeine intake decreases oxidative stress and inflammatory biomarkers in experimental liver diseases induced by thioacetamide: biochemical and histological study. Int. J. Immunopathol. Pharmacol. 30(1), 13–24 (2017)CrossRefGoogle Scholar
  56. 56.
    Lunin, S.M., Khrenov, M.O., Glushkova, O.V., Vinogradova, E.V., Yashin, V.A., Fesenko, E.E., et al.: Extrathymic production of thymulin induced by oxidative stress, heat shock, apoptosis, or necrosis. Int. J. Immunopathol. Pharmacol. 30(1), 58–69 (2017)CrossRefGoogle Scholar
  57. 57.
    Fleshner, M., Crane, C.R.: Exosomes, DAMPs and miRNA: features of stress physiology and immune homeostasis. Trends Immunol. 38(10), 768–776 (2017)CrossRefGoogle Scholar
  58. 58.
    Fleshner, M.: Stress-evoked sterile inflammation, danger associated molecular patterns (DAMPs), microbial associated molecular patterns (MAMPs) and the inflammasome. Brain Behav. Immun. 27, 1–7 (2013)CrossRefGoogle Scholar
  59. 59.
    Rock, K.L., Latz, E., Ontiveros, F., Kono, H.: The sterile inflammatory response. Annu. Rev. Immunol. 28, 321–342 (2010)CrossRefGoogle Scholar
  60. 60.
    Fleshner, M., Nguyen, K.T., Cotter, C.S., Watkins, L.R., Maier, S.F.: Acute stressor exposure both suppresses acquired immunity and potentiates innate immunity. Am. J. Physiol. 275(3 Pt 2), R870–R878 (1998)Google Scholar
  61. 61.
    Campisi, J., Fleshner, M.: Role of extracellular HSP72 in acute stress-induced potentiation of innate immunity in active rats. J. Appl. Physiol. (1985) 94(1):43–52 (2003)Google Scholar
  62. 62.
    Maslanik, T., Mahaffey, L., Tannura, K., Beninson, L., Greenwood, B.N., Fleshner, M.: The inflammasome and danger associated molecular patterns (DAMPs) are implicated in cytokine and chemokine responses following stressor exposure. Brain Behav. Immun. 28, 54–62 (2013)CrossRefGoogle Scholar
  63. 63.
    Beninson, L.A., Brown, P.N., Loughridge, A.B., Saludes, J.P., Maslanik, T., Hills, A.K., et al.: Acute stressor exposure modifies plasma exosome-associated heat shock protein 72 (Hsp72) and microRNA (miR-142-5p and miR-203). PLoS ONE 9(9), e108748 (2014)CrossRefADSGoogle Scholar
  64. 64.
    Rock, K.L., Lai, J.J., Kono, H.: Innate and adaptive immune responses to cell death. Immunol. Rev. 243(1), 191–205 (2011)CrossRefGoogle Scholar
  65. 65.
    Chen, G.Y., Nunez, G.: Sterile inflammation: sensing and reacting to damage. Nat. Rev. Immunol. 10(12), 826–837 (2010)CrossRefGoogle Scholar
  66. 66.
    Hernandez, C., Huebener, P., Schwabe, R.F.: Damage-associated molecular patterns in cancer: a double-edged sword. Oncogene 35(46), 5931–5941 (2016)CrossRefGoogle Scholar
  67. 67.
    Gallo, P.M., Gallucci, S.: The dendritic cell response to classic, emerging, and homeostatic danger signals. Implications for autoimmunity. Front Immunol. 4, 138 (2013)CrossRefGoogle Scholar
  68. 68.
    Dwivedi, P.D., Misra, A., Shanker, R., Das, M.: Are nanomaterials a threat to the immune system? Nanotoxicology 3(1), 19–26 (2009)CrossRefGoogle Scholar
  69. 69.
    Dobrovolskaia, M.A., McNeil, S.E.: Immunological properties of engineered nanomaterials. Nat. Nanotechnol. 2(8), 469–478 (2007)CrossRefGoogle Scholar
  70. 70.
    Thiele, L., Rothen-Rutishauser, B., Jilek, S., Wunderli-Allenspach, H., Merkle, H.P., Walter, E.: Evaluation of particle uptake in human blood monocyte-derived cells in vitro. Does phagocytosis activity of dendritic cells measure up with macrophages? J. Control. Release 76(1–2), 59–71 (2001)Google Scholar
  71. 71.
    Foged, C., Brodin, B., Frokjaer, S., Sundblad, A.: Particle size and surface charge affect particle uptake by human dendritic cells in an in vitro model. Int. J. Pharm. 298(2), 315–322 (2005)CrossRefGoogle Scholar
  72. 72.
    Thiele, L., Merkle, H.P., Walter, E.: Phagocytosis and phagosomal fate of surface-modified microparticles in dendritic cells and macrophages. Pharm. Res. 20(2), 221–228 (2003)CrossRefGoogle Scholar
  73. 73.
    Thiele, L., Diederichs, J.E., Reszka, R., Merkle, H.P., Walter, E.: Competitive adsorption of serum proteins at microparticles affects phagocytosis by dendritic cells. Biomaterials 24(8), 1409–1418 (2003)CrossRefGoogle Scholar
  74. 74.
    Muller, C., Schibli, R.: Prospects in folate receptor-targeted radionuclide therapy. Front Oncol. 3, 249 (2013)CrossRefGoogle Scholar
  75. 75.
    Yameen, B., Choi, W.I., Vilos, C., Swami, A., Shi, J.J., Farokhzad, O.C.: Insight into nanoparticle cellular uptake and intracellular targeting. J. Control. Release 190, 485–499 (2014)CrossRefGoogle Scholar
  76. 76.
    Low, P.S., Kularatne, S.A.: Folate-targeted therapeutic and imaging agents for cancer. Curr. Opin. Chem. Biol. 13(3), 256–262 (2009)CrossRefGoogle Scholar
  77. 77.
    Xia, W., Hilgenbrink, A.R., Matteson, E.L., Lockwood, M.B., Cheng, J.X., Low, P.S.: A functional folate receptor is induced during macrophage activation and can be used to target drugs to activated macrophages. Blood 113(2), 438–446 (2009)CrossRefGoogle Scholar
  78. 78.
    Ross, J.F., Wang, H., Behm, F.G., Mathew, P., Wu, M., Booth, R., et al.: Folate receptor type beta is a neutrophilic lineage marker and is differentially expressed in myeloid leukemia. Cancer 85(2), 348–357 (1999)CrossRefGoogle Scholar
  79. 79.
    Low, P.S., Henne, W.A., Doorneweerd, D.D.: Discovery and development of folic-acid-based receptor targeting for imaging and therapy of cancer and inflammatory diseases. Acc. Chem. Res. 41(1), 120–129 (2008)CrossRefGoogle Scholar
  80. 80.
    Lu, Y., Sega, E., Leamon, C.P., Low, P.S.: Folate receptor-targeted immunotherapy of cancer: mechanism and therapeutic potential. Adv. Drug Deliv. Rev. 56(8), 1161–1176 (2004)CrossRefGoogle Scholar
  81. 81.
    Danhier, F., Feron, O., Preat, V.: To exploit the tumor microenvironment: Passive and active tumor targeting of nanocarriers for anti-cancer drug delivery. J. Control. Release. 148(2), 135–146 (2010)CrossRefGoogle Scholar
  82. 82.
    van der Meel, R., Vehmeijer, L.J., Kok, R.J., Storm, G., van Gaal, E.V.: Ligand-targeted particulate nanomedicines undergoing clinical evaluation: current status. Adv. Drug Deliv. Rev. 65(10), 1284–1298 (2013)CrossRefGoogle Scholar
  83. 83.
    Lurje, G., Lenz, H.J.: EGFR signaling and drug discovery. Oncology 77(6), 400–410 (2009)CrossRefGoogle Scholar
  84. 84.
    Xia, T., Kovochich, M., Liong, M., Zink, J.I., Nel, A.E.: Cationic polystyrene nanosphere toxicity depends on cell-specific endocytic and mitochondrial injury pathways. ACS Nano 2(1), 85–96 (2008)CrossRefGoogle Scholar
  85. 85.
    Loos, C., Syrovets, T., Musyanovych, A., Mailander, V., Landfester, K., Nienhaus, G.U., et al.: Functionalized polystyrene nanoparticles as a platform for studying bio-nano interactions. Beilstein J. Nanotechnol. 5, 2403–2412 (2014)CrossRefGoogle Scholar
  86. 86.
    Sohaebuddin, S.K., Thevenot, P.T., Baker, D., Eaton, J.W., Tang, L.: Nanomaterial cytotoxicity is composition, size, and cell type dependent. Part Fibre Toxicol. 7, 22 (2010)CrossRefGoogle Scholar
  87. 87.
    Lanone, S., Rogerieux, F., Geys, J., Dupont, A., Maillot-Marechal, E., Boczkowski, J., et al.: Comparative toxicity of 24 manufactured nanoparticles in human alveolar epithelial and macrophage cell lines. Part Fibre Toxicol. 6, 14 (2009)CrossRefGoogle Scholar
  88. 88.
    Loh, M.L.: Recent advances in the pathogenesis and treatment of juvenile myelomonocytic leukaemia. Br. J. Haematol. 152(6), 677–687 (2011)CrossRefGoogle Scholar
  89. 89.
    Kohro, T., Tanaka, T., Murakami, T., Wada, Y., Aburatani, H., Hamakubo, T., et al.: A comparison of differences in the gene expression profiles of phorbol 12-myristate 13-acetate differentiated THP-1 cells and human monocyte-derived macrophage. J. Atheroscler. Thromb. 11(2), 88–97 (2004)CrossRefGoogle Scholar
  90. 90.
    Park, E.K., Jung, H.S., Yang, H.I., Yoo, M.C., Kim, C., Kim, K.S.: Optimized THP-1 differentiation is required for the detection of responses to weak stimuli. Inflamm. Res. 56(1), 45–50 (2007)CrossRefGoogle Scholar
  91. 91.
    Schottler, S., Becker, G., Winzen, S., Steinbach, T., Mohr, K., Landfester, K., et al.: Protein adsorption is required for stealth effect of poly(ethylene glycol)- and poly(phosphoester)-coated nanocarriers. Nat. Nanotechnol. 11(4), 372–377 (2016)CrossRefADSGoogle Scholar
  92. 92.
    Schottler, S., Klein, K., Landfester, K., Mailander, V.: Protein source and choice of anticoagulant decisively affect nanoparticle protein corona and cellular uptake. Nanoscale 8(10), 5526–5536 (2016)CrossRefADSGoogle Scholar
  93. 93.
    Gillis, S., Watson, J.: Biochemical and biological characterization of lymphocyte regulatory molecules. V. Identification of an interleukin 2-producing human leukemia T cell line. J. Exp. Med. 152(6), 1709–1719 (1980)Google Scholar
  94. 94.
    Abraham, R.T., Weiss, A.: Jurkat T cells and development of the T-cell receptor signalling paradigm. Nat. Rev. Immunol. 4(4), 301–308 (2004)CrossRefGoogle Scholar
  95. 95.
    Astoul, E., Edmunds, C., Cantrell, D.A., Ward, S.G.: PI 3-K and T-cell activation: limitations of T-leukemic cell lines as signaling models. Trends Immunol. 22(9), 490–496 (2001)CrossRefGoogle Scholar
  96. 96.
    Shan, X., Czar, M.J., Bunnell, S.C., Liu, P., Liu, Y., Schwartzberg, P.L., et al.: Deficiency of PTEN in Jurkat T cells causes constitutive localization of Itk to the plasma membrane and hyperresponsiveness to CD3 stimulation. Mol. Cell. Biol. 20(18), 6945–6957 (2000)CrossRefGoogle Scholar
  97. 97.
    Wang, X., Gjorloff-Wingren, A., Saxena, M., Pathan, N., Reed, J.C., Mustelin, T.: The tumor suppressor PTEN regulates T cell survival and antigen receptor signaling by acting as a phosphatidylinositol 3-phosphatase. J. Immunol. 164(4), 1934–1939 (2000)CrossRefGoogle Scholar
  98. 98.
    Seminario, M.C., Wange, R.L.: Signaling pathways of D3-phosphoinositide-binding kinases in T cells and their regulation by PTEN. Semin. Immunol. 14(1), 27–36 (2002)CrossRefGoogle Scholar
  99. 99.
    Mohr, K., Sommer, M., Baier, G., Schöttler, S., Okwieka, P., Tenzer, S., et al.: Aggregation behavior of polystyrene-nanoparticles in human blood serum and its impact on the in vivo distribution in mice. J. Nanomed. Nanotech. 5, 193 (2014)CrossRefGoogle Scholar
  100. 100.
    Schmid, D., Park, C.G., Hartl, C.A., Subedi, N., Cartwright, A.N., Puerto, R.B., et al.: T cell-targeting nanoparticles focus delivery of immunotherapy to improve antitumor immunity. Nat. Commun. 8(1), 1747 (2017)CrossRefADSGoogle Scholar
  101. 101.
    Gros, A., Robbins, P.F., Yao, X., Li, Y.F., Turcotte, S., Tran, E., et al.: PD-1 identifies the patient-specific CD8(+) tumor-reactive repertoire infiltrating human tumors. J. Clin. Invest. 124(5), 2246–2259 (2014)CrossRefGoogle Scholar
  102. 102.
    Gros, A., Parkhurst, M.R., Tran, E., Pasetto, A., Robbins, P.F., Ilyas, S., et al.: Prospective identification of neoantigen-specific lymphocytes in the peripheral blood of melanoma patients. Nat. Med. 22(4), 433–438 (2016)CrossRefGoogle Scholar
  103. 103.
    Zolnik, B.S., Gonzalez-Fernandez, A., Sadrieh, N., Dobrovolskaia, M.A.: Nanoparticles and the immune system. Endocrinology 151(2), 458–465 (2010)CrossRefGoogle Scholar
  104. 104.
    Muller, L.K., Simon, J., Schottler, S., Landfester, K., Mailander, V., Mohr, K.: Pre-coating with protein fractions inhibits nano-carrier aggregation in human blood plasma. RSC Adv. 6(99), 96495–96509 (2016)CrossRefGoogle Scholar
  105. 105.
    Ahmed, T.A., Aljaeid, B.M.: Preparation, characterization, and potential application of chitosan, chitosan derivatives, and chitosan metal nanoparticles in pharmaceutical drug delivery. Drug Des. Dev. Ther. 10, 483–507 (2016)CrossRefGoogle Scholar
  106. 106.
    Owens, D.E., Peppas, N.A.: Opsonization, biodistribution, and pharmacokinetics of polymeric nanoparticles. Int. J. Pharm. 307(1), 93–102 (2006)CrossRefGoogle Scholar
  107. 107.
    Andersson, L.I., Hellman, P., Eriksson, H.: Receptor-mediated endocytosis of particles by peripheral dendritic cells. Hum. Immunol. 69(10), 625–633 (2008)CrossRefGoogle Scholar
  108. 108.
    Tabata, Y., Ikada, Y.: Macrophage phagocytosis of biodegradable microspheres composed of L-lactic acid/glycolic acid homo- and copolymers. J. Biomed. Mater. Res. 22(10), 837–858 (1988)CrossRefGoogle Scholar
  109. 109.
    Guo, S.T., Huang, L.: Nanoparticles escaping RES and endosome: challenges for siRNA delivery for cancer therapy. J. Nanomater. (2011)Google Scholar
  110. 110.
    Wei, W., Ma, G.H., Wang, L.Y., Wu, J., Su, Z.G.: Hollow quaternized chitosan microspheres increase the therapeutic effect of orally administered insulin. Acta Biomater. 6(1), 205–209 (2010)CrossRefGoogle Scholar
  111. 111.
    Nagamoto, T., Hattori, Y., Takayama, K., Maitani, Y.: Novel chitosan particles and chitosan-coated emulsions inducing immune response via intranasal vaccine delivery. Pharm. Res. 21(4), 671–674 (2004)CrossRefGoogle Scholar
  112. 112.
    Jiang, H.L., Kang, M.L., Quan, J.S., Kang, S.G., Akaike, T., Yoo, H.S., et al.: The potential of mannosylated chitosan microspheres to target macrophage mannose receptors in an adjuvant-delivery system for intranasal immunization. Biomaterials 29(12), 1931–1939 (2008)CrossRefGoogle Scholar
  113. 113.
    Kang, M.L., Jiang, H.L., Kang, S.G., Guo, D.D., Lee, D.Y., Cho, C.S., et al.: Pluronic F127 enhances the effect as an adjuvant of chitosan microspheres in the intranasal delivery of Bordetella bronchiseptica antigens containing dermonecrotoxin. Vaccine 25(23), 4602–4610 (2007)CrossRefGoogle Scholar
  114. 114.
    Ferin, J., Oberdorster, G., Soderholm, S.C., Gelein, R.: Pulmonary tissue access of ultrafine particles. J. Aerosol. Med. 4(1), 57–68 (1991)CrossRefGoogle Scholar
  115. 115.
    Huang, Y.C., Vieira, A., Huang, K.L., Yeh, M.K., Chiang, C.H.: Pulmonary inflammation caused by chitosan microparticles. J. Biomed. Mater. Res. A 75(2), 283–287 (2005)CrossRefGoogle Scholar
  116. 116.
    Donaldson, K., Poland, C.A., Schins, R.P.: Possible genotoxic mechanisms of nanoparticles: criteria for improved test strategies. Nanotoxicology 4, 414–420 (2010)CrossRefGoogle Scholar
  117. 117.
    Przybytkowski, E., Behrendt, M., Dubois, D., Maysinger, D.: Nanoparticles can induce changes in the intracellular metabolism of lipids without compromising cellular viability. FEBS J. 276(21), 6204–6217 (2009)CrossRefGoogle Scholar
  118. 118.
    Saptarshi, S.R., Feltis, B.N., Wright, P.F.A., Lopata, A.L.: Investigating the immunomodulatory nature of zinc oxide nanoparticles at sub-cytotoxic levels in vitro and after intranasal instillation in vivo. J. Nanobiotechnol. 13 (2015)Google Scholar
  119. 119.
    Kawata, K., Osawa, M., Okabe, S.: In vitro toxicity of silver nanoparticles at noncytotoxic doses to HepG2 human hepatoma cells. Environ. Sci. Technol. 43(15), 6046–6051 (2009)CrossRefADSGoogle Scholar
  120. 120.
    Dworak, N., Wnuk, M., Zebrowski, J., Bartosz, G., Lewinska, A.: Genotoxic and mutagenic activity of diamond nanoparticles in human peripheral lymphocytes in vitro. Carbon 68, 763–776 (2014)CrossRefGoogle Scholar
  121. 121.
    Smith, M.J., Brown, J.M., Zamboni, W.C., Walker, N.J.: From immunotoxicity to nanotherapy: the effects of nanomaterials on the immune system. Toxicol. Sci. 138(2), 249–255 (2014)CrossRefGoogle Scholar
  122. 122.
    Baumann, D., Hofmann, D., Nullmeier, S., Panther, P., Dietze, C., Musyanovych, A., et al.: Complex encounters: nanoparticles in whole blood and their uptake into different types of white blood cells. Nanomedicine (Lond.) 8(5), 699–713 (2013)CrossRefGoogle Scholar
  123. 123.
    Lunov, O., Syrovets, T., Loos, C., Beil, J., Delacher, M., Tron, K., et al.: Differential uptake of functionalized polystyrene nanoparticles by human macrophages and a monocytic cell line. ACS Nano 5(3), 1657–1669 (2011)CrossRefGoogle Scholar
  124. 124.
    Clift, M.J., Gehr, P., Rothen-Rutishauser, B.: Nanotoxicology: a perspective and discussion of whether or not in vitro testing is a valid alternative. Arch. Toxicol. 85(7), 723–731 (2011)CrossRefGoogle Scholar
  125. 125.
    Tonigold, M., Mailander, V.: Endocytosis and intracellular processing of nanoparticles in dendritic cells: routes to effective immunonanomedicines. Nanomedicine (Lond.) 11(20), 2625–2630 (2016)CrossRefGoogle Scholar
  126. 126.
    Harush-Frenkel, O., Debotton, N., Benita, S., Altschuler, Y.: Targeting of nanoparticles to the clathrin-mediated endocytic pathway. Biochem. Biophys. Res. Commun. 353(1), 26–32 (2007)CrossRefGoogle Scholar
  127. 127.
    Vasir, J.K., Labhasetwar, V.: Quantification of the force of nanoparticle-cell membrane interactions and its influence on intracellular trafficking of nanoparticles. Biomaterials 29(31), 4244–4252 (2008)CrossRefGoogle Scholar
  128. 128.
    Garaiova, Z., Strand, S.P., Reitan, N.K., Lelu, S., Storset, S.O., Berg, K., et al.: Cellular uptake of DNA-chitosan nanoparticles: the role of clathrin- and caveolae-mediated pathways. Int. J. Biol. Macromol. 51(5), 1043–1051 (2012)CrossRefGoogle Scholar
  129. 129.
    Parton, R.G., Simons, K.: The multiple faces of caveolae. Nat. Rev. Mol. Cell Biol. 8(3), 185–194 (2007)CrossRefGoogle Scholar
  130. 130.
    Sahay, G., Alakhova, D.Y., Kabanov, A.V.: Endocytosis of nanomedicines. J. Control. Release. 145(3), 182–195 (2010)CrossRefGoogle Scholar
  131. 131.
    Liu, Y., Huang, R., Han, L., Ke, W., Shao, K., Ye, L., et al.: Brain-targeting gene delivery and cellular internalization mechanisms for modified rabies virus glycoprotein RVG29 nanoparticles. Biomaterials 30(25), 4195–4202 (2009)CrossRefGoogle Scholar
  132. 132.
    Falcone, S., Cocucci, E., Podini, P., Kirchhausen, T., Clementi, E., Meldolesi, J.: Macropinocytosis: regulated coordination of endocytic and exocytic membrane traffic events. J. Cell Sci. 119(Pt 22), 4758–4769 (2006)CrossRefGoogle Scholar
  133. 133.
    Mercer, J., Helenius, A.: Virus entry by macropinocytosis. Nat. Cell Biol. 11(5), 510–520 (2009)CrossRefGoogle Scholar
  134. 134.
    Kolb-Maurer, A., Wilhelm, M., Weissinger, F., Brocker, E.B., Goebel, W.: Interaction of human hematopoietic stem cells with bacterial pathogens. Blood 100(10), 3703–3709 (2002)CrossRefGoogle Scholar
  135. 135.
    Fiorentini, C., Falzano, L., Fabbri, A., Stringaro, A., Logozzi, M., Travaglione, S., et al.: Activation of rho GTPases by cytotoxic necrotizing factor 1 induces macropinocytosis and scavenging activity in epithelial cells. Mol. Biol. Cell 12(7), 2061–2073 (2001)CrossRefGoogle Scholar
  136. 136.
    Steinman, R.M., Swanson, J.: The endocytic activity of dendritic cells. J. Exp. Med. 182(2), 283–288 (1995)CrossRefGoogle Scholar
  137. 137.
    Sallusto, F., Cella, M., Danieli, C., Lanzavecchia, A.: Dendritic cells use macropinocytosis and the mannose receptor to concentrate macromolecules in the major histocompatibility complex class II compartment: downregulation by cytokines and bacterial products. J. Exp. Med. 182(2), 389–400 (1995)CrossRefGoogle Scholar
  138. 138.
    Zhang, L., Zhang, S., Ruan, S.B., Zhang, Q.Y., He, Q., Gao, H.L.: Lapatinib-incorporated lipoprotein-like nanoparticles: preparation and a proposed breast cancer-targeting mechanism. Acta Pharmacol. Sin. 35(6), 846–852 (2014)CrossRefGoogle Scholar
  139. 139.
    Gupta, A.K., Gupta, M.: Cytotoxicity suppression and cellular uptake enhancement of surface modified magnetic nanoparticles. Biomaterials 26(13), 1565–1573 (2005)CrossRefGoogle Scholar
  140. 140.
    Zhang, J., Chen, X.G., Huang, L., Han, J.T., Zhang, X.F.: Self-assembled polymeric nanoparticles based on oleic acid-grafted chitosan oligosaccharide: biocompatibility, protein adsorption and cellular uptake. J. Mater. Sci. Mater. Med. 23(7), 1775–1783 (2012)CrossRefGoogle Scholar
  141. 141.
    Wadhwa, S., Rea, C., O’Hare, P., Mathur, A., Roy, S.S., Dunlop, P.S., et al.: Comparative in vitro cytotoxicity study of carbon nanotubes and titania nanostructures on human lung epithelial cells. J. Hazard. Mater. 191(1–3), 56–61 (2011)CrossRefGoogle Scholar
  142. 142.
    Panariti, A., Miserocchi, G., Rivolta, I.: The effect of nanoparticle uptake on cellular behavior: disrupting or enabling functions? Nanotechnol. Sci Appl. 5, 87–100 (2012)Google Scholar
  143. 143.
    Ahamed, M.: Toxic response of nickel nanoparticles in human lung epithelial A549 cells. Toxicol. In Vitro 25(4), 930–936 (2011)CrossRefGoogle Scholar
  144. 144.
    Gourlay, C.W., Ayscough, K.R.: The actin cytoskeleton: a key regulator of apoptosis and ageing? Nat. Rev. Mol. Cell Biol. 6(7), 583–589 (2005)CrossRefGoogle Scholar
  145. 145.
    Buyukhatipoglu, K., Clyne, A.M.: Superparamagnetic iron oxide nanoparticles change endothelial cell morphology and mechanics via reactive oxygen species formation. J. Biomed. Mater. Res. A 96(1), 186–195 (2011)CrossRefGoogle Scholar
  146. 146.
    Scherbart, A.M., Langer, J., Bushmelev, A., van Berlo, D., Haberzettl, P., van Schooten, F.J., et al.: Contrasting macrophage activation by fine and ultrafine titanium dioxide particles is associated with different uptake mechanisms. Part Fibre Toxicol. 8, 31 (2011)CrossRefGoogle Scholar
  147. 147.
    Wang, H.J., Growcock, A.C., Tang, T.H., O’Hara, J., Huang, Y.W., Aronstam, R.S.: Zinc oxide nanoparticle disruption of store-operated calcium entry in a muscarinic receptor signaling pathway. Toxicol. In Vitro 24(7), 1953–1961 (2010)CrossRefGoogle Scholar
  148. 148.
    Horie, M., Nishio, K., Kato, H., Fujita, K., Endoh, S., Nakamura, A., et al.: Cellular responses induced by cerium oxide nanoparticles: induction of intracellular calcium level and oxidative stress on culture cells. J. Biochem. 150(4), 461–471 (2011)CrossRefGoogle Scholar
  149. 149.
    McCarthy, J., Gong, X., Nahirney, D., Duszyk, M., Radomski, M.: Polystyrene nanoparticles activate ion transport in human airway epithelial cells. Int. J. Nanomed. 6, 1343–1356 (2011)CrossRefGoogle Scholar
  150. 150.
    Garrett, W.S., Chen, L.M., Kroschewski, R., Ebersold, M., Turley, S., Trombetta, S., et al.: Developmental control of endocytosis in dendritic cells by Cdc42. Cell 102(3), 325–334 (2000)CrossRefGoogle Scholar
  151. 151.
    Zhang, L.W., Baumer, W., Monteiro-Riviere, N.A.: Cellular uptake mechanisms and toxicity of quantum dots in dendritic cells. Nanomedicine (Lond.) 6(5), 777–791 (2011)CrossRefGoogle Scholar
  152. 152.
    Le Roux, D., Le Bon, A., Dumas, A., Taleb, K., Sachse, M., Sikora, R., et al.: Antigen stored in dendritic cells after macropinocytosis is released unprocessed from late endosomes to target B cells. Blood 119(1), 95–105 (2012)CrossRefGoogle Scholar
  153. 153.
    Platt, C.D., Ma, J.K., Chalouni, C., Ebersold, M., Bou-Reslan, H., Carano, R.A., et al.: Mature dendritic cells use endocytic receptors to capture and present antigens. Proc. Natl. Acad. Sci. U.S.A. 107(9), 4287–4292 (2010)CrossRefADSGoogle Scholar
  154. 154.
    Rodriguez, A., Regnault, A., Kleijmeer, M., Ricciardi-Castagnoli, P., Amigorena, S.: Selective transport of internalized antigens to the cytosol for MHC class I presentation in dendritic cells. Nat. Cell Biol. 1(6), 362–368 (1999)CrossRefGoogle Scholar
  155. 155.
    Harding, C.V., Song, R.: Phagocytic processing of exogenous particulate antigens by macrophages for presentation by class I MHC molecules. J. Immunol. 153(11), 4925–4933 (1994)Google Scholar
  156. 156.
    Joffre, O.P., Segura, E., Savina, A., Amigorena, S.: Cross-presentation by dendritic cells. Nat. Rev. Immunol. 12(8), 557–569 (2012)CrossRefGoogle Scholar
  157. 157.
    Guermonprez, P., Saveanu, L., Kleijmeer, M., Davoust, J., Van Endert, P., Amigorena, S.: ER-phagosome fusion defines an MHC class I cross-presentation compartment in dendritic cells. Nature 425(6956), 397–402 (2003)CrossRefADSGoogle Scholar
  158. 158.
    Silva, A.L., Rosalia, R.A., Varypataki, E., Sibuea, S., Ossendorp, F., Jiskoot, W.: Poly-(lactic-co-glycolic-acid)-based particulate vaccines: particle uptake by dendritic cells is a key parameter for immune activation. Vaccine 33(7), 847–854 (2015)CrossRefGoogle Scholar
  159. 159.
    Shen, H., Ackerman, A.L., Cody, V., Giodini, A., Hinson, E.R., Cresswell, P., et al.: Enhanced and prolonged cross-presentation following endosomal escape of exogenous antigens encapsulated in biodegradable nanoparticles. Immunology 117(1), 78–88 (2006)CrossRefGoogle Scholar
  160. 160.
    Sneh-Edri, H., Likhtenshtein, D., Stepensky, D.: Intracellular targeting of PLGA nanoparticles encapsulating antigenic peptide to the endoplasmic reticulum of dendritic cells and its effect on antigen cross-presentation in vitro. Mol. Pharm. 8(4), 1266–1275 (2011)CrossRefGoogle Scholar
  161. 161.
    Jiskoot, W., van Schie, R.M., Carstens, M.G., Schellekens, H.: Immunological risk of injectable drug delivery systems. Pharm. Res. 26(6), 1303–1314 (2009)CrossRefGoogle Scholar
  162. 162.
    Fuchs, A.K., Syrovets, T., Haas, K.A., Loos, C., Musyanovych, A., Mailander, V., et al.: Carboxyl- and amino-functionalized polystyrene nanoparticles differentially affect the polarization profile of M1 and M2 macrophage subsets. Biomaterials 85, 78–87 (2016)CrossRefGoogle Scholar
  163. 163.
    Andersen, A.J., Hashemi, S.H., Andresen, T.L., Hunter, A.C., Moghimi, S.M.: Complement: alive and kicking nanomedicines. J. Biomed. Nanotechnol. 5(4), 364–372 (2009)CrossRefGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of DermatologyUniversity Medical Center of the Johannes Gutenberg-University MainzMainzGermany
  2. 2.Max-Planck-Institute for Polymer ResearchMainzGermany

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