Nanoparticle–liver interactions: Cellular uptake and hepatobiliary elimination

Journal of Controlled Release

Volumn 240, Issue , 2016, Pages 332-348

  Zhang, Yi Nan ^a,b   Poon, Wilson ^a,b   Tavares, Anthony J ^a,b   McGilvray, Ian D ^c   Chan, Warren C W ^a,b,d  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY HEALTH NETWORK   (Canada)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

Hepatobiliary clearance; Liver; Macrophage; Nanoparticle

Indexed keywords

DIAGNOSIS; LIVER; MACROPHAGES;

CELLULAR INTERACTION; CELLULAR LEVELS; CELLULAR UPTAKE; CLINICAL TRANSLATION; DISEASED TISSUES; HEPATIC CELLS; HEPATOBILIARY;

NANOPARTICLES;

NANOCARRIER; NANOPARTICLE;

ARTICLE; BILIARY CLEARANCE; BILIARY EXCRETION; CELL INTERACTION; CIRCULATION; DRUG DELIVERY SYSTEM; ENDOTHELIUM CELL; HEPATOBILIARY SYSTEM; HEPATOCELLULAR CARCINOMA CELL LINE; HUMAN; KUPFFER CELL; LIVER CELL; LIVER FUNCTION; LIVER STRUCTURE; MACROPHAGE; NANOTECHNOLOGY; NONHUMAN; PHAGOCYTE; PRIORITY JOURNAL; STELLATE CELL; SURFACE PROPERTY; ANIMAL; CHEMISTRY; DRUG EFFECTS; LIVER; METABOLISM;

ANIMALS; BILIARY TRACT; HEPATOBILIARY ELIMINATION; HUMANS; KUPFFER CELLS; LIVER; NANOPARTICLES; SURFACE PROPERTIES;

EID: 84958581834     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2016.01.020     Document Type: Article

References (184)

1. [1] Chou, L.Y., Ming, K., Chan, W.C., Strategies for the intracellular delivery of nanoparticles. Chem. Soc. Rev. 40 (2011), 233–245.
2. [2] Sun, T., Zhang, Y.S., Pang, B., Hyun, D.C., Yang, M., Xia, Y., Engineered nanoparticles for drug delivery in cancer therapy. Angew. Chem. Int. Ed. 53 (2014), 12320–12364.
3. [3] Poon, W., Zhang, X., Nadeau, J., Nanoparticle drug formulations for cancer diagnosis and treatment. Crit. Rev. Oncog. 19 (2014), 223–245.
4. [4] Yu, M., Zheng, J., Clearance pathways and tumor targeting of imaging nanoparticles. ACS Nano 9 (2015), 6655–6674.
5. [5] Abdel-Misih, S.R.Z., Bloomston, M., Liver anatomy. Surg. Clin. North Am. 90 (2010), 643–653.
6. [6] Hoekstra, L.T., de Graaf, W., Nibourg, G.A.A., Heger, M., Bennink, R.J., Stieger, B., van Gulik, T.M., Physiological and biochemical basis of clinical liver function tests. Ann. Surg. 257 (2013), 27–36.
7. [7] Ghibellini, G., Leslie, E.M., Brouwer, K.L.R., Methods to evaluate biliary excretion of drugs in humans: an updated review. Mol. Pharm. 3 (2006), 198–211.
8. [8] Pond, S.M., Tozer, T.N., First-pass elimination basic concepts and clinical consequences. Clin. Pharmacokinet. 9 (1984), 1–25.
9. [9] Wang, H., Thorling, C.A., Liang, X., Bridle, K.R., Grice, J.E., Zhu, Y., Crawford, D.H.G., Xu, Z.P., Liu, X., Roberts, M.S., Diagnostic imaging and therapeutic application of nanoparticles targeting the liver. J. Mater. Chem. B 3 (2015), 939–958.
10. [10] Racanelli, V., Rehermann, B., The liver as an immunological organ. Hepatology 43 (2006), S54–S62.
11. [11] Bertrand, N., Leroux, J.-C., The journey of a drug-carrier in the body: an anatomo-physiological perspective. J. Control. Release 161 (2012), 152–163.
12. [12] Friedman, S.L., Hepatic stellate cells: protean, multifunctional, and enigmatic cells of the liver. Physiol. Rev. 88 (2008), 125–172.
13. [13] Li, L., Wang, H., Ong, Z.Y., Xu, K., Ee, P.L.R., Zheng, S., Hedrick, J.L., Yang, Y.-Y., Polymer- and lipid-based nanoparticle therapeutics for the treatment of liver diseases. Nano Today 5 (2010), 296–312.
14. [14] Reddy, L.H., Couvreur, P., Nanotechnology for therapy and imaging of liver diseases. J. Hepatol. 55 (2011), 1461–1466.
15. [15] Mishra, N., Yadav, N.P., Rai, V.K., Sinha, P., Yadav, K.S., Jain, S., Arora, S., Efficient hepatic delivery of drugs: novel strategies and their significance. Biomed. Res. Int., 2013, 2013, 382184.
16. [16] Janeway, C.A., Travers, P., Walport, M., Shlomchik, M.J., The Front Line of Host Defense. 2001, Garland Science.
17. [17] Doble, B.W., Woodgett, J.R., GSK-3: tricks of the trade for a multi-tasking kinase. J. Cell Sci. 116 (2003), 1175–1186.
18. [18] Davies, L.C., Jenkins, S.J., Allen, J.E., Taylor, P.R., Tissue-resident macrophages. Nat. Immunol. 14 (2013), 986–995.
19. [19] Aderem, A., Underhill, D.M., Mechanisms of phagocytosis in macrophages. Annu. Rev. Immunol. 17 (1999), 593–623.
20. [20] Walkey, C.D., Olsen, J.B., Guo, H., Emili, A., Chan, W.C.W., Nanoparticle size and surface chemistry determine serum protein adsorption and macrophage uptake. J. Am. Chem. Soc. 134 (2012), 2139–2147.
21. [21] Fischer, H.C., Hauck, T.S., Gómez-Aristizábal, A., Chan, W.C.W., Exploring primary liver macrophages for studying quantum dot interactions with biological systems. Adv. Mater. 22 (2010), 2520–2524.
22. [22] Dobrovolskaia, M.A., McNeil, S.E., Immunological properties of engineered nanomaterials. Nat. Nanotechnol. 2 (2007), 469–478.
23. [23] Lunov, O., Zablotskii, V., Syrovets, T., Röcker, C., Tron, K., Nienhaus, G.U., Simmet, T., Modeling receptor-mediated endocytosis of polymer-functionalized iron oxide nanoparticles by human macrophages. Biomaterials 32 (2011), 547–555.
24. [24] Thurman, R.G., Mechanisms of hepatic toxicity II. Alcoholic liver injury involves activation of Kupffer cells by endotoxin. Am. J. Phys. 275 (1998), G605–G611.
25. [25] Gershwin, M.E., Vierling, J.M., Manns, M.P., Liver Immunology. Principles and Practice. 2014, Springer International Publishing.
26. [26] Smedsrød, B., Clearance function of scavenger endothelial cells. Comp. Hepatol., 3, 2004, S22.
27. [27] Kamps, J.A.A.M., Morselt, H., Swart, P.J., Keijer, D., Scherphof, G.L., Massive targeting of liposomes, surface-modified with anionized albumins, to hepatic endothelial cells. Proc. Natl. Acad. Sci. U. S. A. 94 (1997), 11681–11685.
28. [28] Popielarski, S.R., Hu-Lieskovan, S., French, S.W., Triche, T.J., Davis, M.E., A nanoparticle-based model delivery system to guide the rational design of gene delivery to the liver. 2. In vitro and in vivo uptake results. Bioconjug. Chem. 16 (2005), 1071–1080.
29. [29] Yin, C., Evason, K.J., Asahina, K., Stainier, D.Y.R., Hepatic stellate cells in liver development, regeneration, and cancer. J. Clin. Invest. 123 (2013), 1902–1910.
30. [30] Beljaars, L., Molema, G., Schuppan, D., Geerts, A., Bleser, P.J., Weert, B., Meijer, D.K.F., Poelstra, K., Successful targeting to rat hepatic stellate cells using albumin modified with cyclic peptides that recognize the collagen type VI receptor. J. Biol. Chem. 275 (2000), 12743–12751.
31. [31] Du, S.-L., Pan, H., Lu, W.-Y., Wang, J., Wu, J., Wang, J.-Y., Cyclic Arg–Gly–Asp peptide-labeled liposomes for targeting drug therapy of hepatic fibrosis in rats. J. Pharmacol. Exp. Ther. 322 (2007), 560–568.
32. [32] Duong, H.T.T., Dong, Z., Su, L., Boyer, C., George, J., Davis, T.P., Wang, J., The use of nanoparticles to deliver nitric oxide to hepatic stellate cells for treating liver fibrosis and portal hypertension. Small 11 (2015), 2291–2304.
33. [33] Fallon, R.J., Schwartz, A.L., Receptor-mediated delivery of drugs to hepatocytes. Adv. Drug Deliv. Rev. 4 (1989), 49–63.
34. [34] Romero, E.L., Morilla, M.-J., Regts, J., Koning, G.A., Scherphof, G.L., On the mechanism of hepatic transendothelial passage of large liposomes. FEBS Lett. 448 (1999), 193–196.
35. [35] Qi, W.-W., Yu, H.-Y., Guo, H., Lou, J., Wang, Z.-M., Liu, P., Sapin-Minet, A., Maincent, P., Hong, X.-C., Hu, X.-M., Xiao, Y.-L., Doxorubicin-loaded glycyrrhetinic acid modified recombinant human serum albumin nanoparticles for targeting liver tumor chemotherapy. Mol. Pharm. 12 (2015), 675–683.
36. [36] Tian, Q., Zhang, C.-N., Wang, X.-H., Wang, W., Huang, W., Cha, R.-T., Wang, C.-H., Yuan, Z., Liu, M., Wan, H.-Y., Tang, H., Glycyrrhetinic acid-modified chitosan/poly(ethylene glycol) nanoparticles for liver-targeted delivery. Biomaterials 31 (2010), 4748–4756.
37. [37] Negishi, M., Irie, A., Nagata, N., Ichikawa, A., Specific binding of glycyrrhetinic acid to the rat liver membrane. Biochim. Biophys. Acta Biomembr. 1066 (1991), 77–82.
38. [38] Lin, A., Liu, Y., Huang, Y., Sun, J., Wu, Z., Zhang, X., Ping, Q., Glycyrrhizin surface-modified chitosan nanoparticles for hepatocyte-targeted delivery. Int. J. Pharm. 359 (2008), 247–253.
39. [39] Wu, F., Wuensc, S.A., Azadniv, M., Ebrahimkhani, M.R., Crispe, I.N., Galactosylated LDL nanoparticles: a novel targeting delivery system to deliver antigen to macrophages and enhance antigen specific T cell responses. Mol. Pharm. 6 (2009), 1506–1517.
40. [40] Opanasopit, P., Sakai, M., Nishikawa, M., Kawakami, S., Yamashita, F., Hashida, M., Inhibition of liver metastasis by targeting of immunomodulators using mannosylated liposome carriers. J. Control. Release 80 (2002), 283–294.
41. [41] Higuchi, Y., Kawakami, S., Oka, M., Yabe, Y., Yamashita, F., Hashida, M., Intravenous administration of mannosylated cationic liposome/NFkB decoy complexes effectively prevent LPS-induced cytokine production in a murine liver failure model. FEBS Lett. 580 (2006), 3706–3714.
42. [42] Akhter, A., Hayashi, Y., Sakurai, Y., Ohga, N., Hida, K., Harashima, H., Ligand density at the surface of a nanoparticle and different uptake mechanism: two important factors for successful siRNA delivery to liver endothelial cells. Int. J. Pharm. 475 (2014), 227–237.
43. [43] Kren, B.T., Unger, G.M., Sjeklocha, L., Trossen, A.A., Korman, V., Diethelm-Okita, B.M., Reding, M.T., Steer, C.J., Nanocapsule-delivered sleeping beauty mediates therapeutic factor VIII expression in liver sinusoidal endothelial cells of hemophilia A mice. J. Clin. Invest. 119 (2009), 2086–2099.
44. [44] Lee, M.-Y., Yang, J.-A., Jung, H.S., Beack, S., Choi, J.E., Hur, W., Koo, H., Kim, K., Yoon, S.K., Hahn, S.K., Hyaluronic acid–gold nanoparticle/interferon α complex for targeted treatment of hepatitis C virus infection. ACS Nano 6 (2012), 9522–9531.
45. [45] Adrian, J.E., Kamps, J.A.A.M., Poelstra, K., Scherphof, G.L., Meijer, D.K.F., Kaneda, Y., Delivery of viral vectors to hepatic stellate cells in fibrotic livers using HVJ envelopes fused with targeted liposomes. J. Drug Target. 15 (2007), 75–82.
46. [46] Li, F.-Q., Su, H., Chen, X., Qin, X.-J., Liu, J.-Y., Zhu, Q.-G., Hu, J.-H., Mannose 6-phosphate-modified bovine serum albumin nanoparticles for controlled and targeted delivery of sodium ferulate for treatment of hepatic fibrosis. J. Pharm. Pharmacol. 61 (2009), 1155–1161.
47. [47] Patel, G., Kher, G., Misra, A., Preparation and evaluation of hepatic stellate cell selective, surface conjugated, peroxisome proliferator-activated receptor-gamma ligand loaded liposomes. J. Drug Target. 20 (2012), 155–165.
48. [48] Adrian, J.E., Poelstra, K., Scherphof, G.L., Meijer, D.K.F., van Loenen-Weemaes, A.-M., Reker-Smit, C., Morselt, H.W.M., Zwiers, P., Kamps, J.A.A.M., Effects of a new bioactive lipid-based drug carrier on cultured hepatic stellate cells and liver fibrosis in bile duct-ligated rats. J. Pharmacol. Exp. Ther. 321 (2007), 536–543.
49. [49] Li, F., Li, Q.-h., Wang, L.-y., Zhan, C.-y., Xie, C., Liu, W.-y., Effects of interferon-gamma liposomes targeted to platelet-derived growth factor receptor–beta on hepatic fibrosis in rats. J. Control. Release 159 (2012), 261–270.
50. [50] Mezghrani, O., Tang, Y., Ke, X., Chen, Y., Hu, D., Tu, J., Zhao, L., Bourkaib, N., Hepatocellular carcinoma dually-targeted nanoparticles for reduction triggered intracellular delivery of doxorubicin. Int. J. Pharm. 478 (2015), 553–568.
51. [51] Sato, Y., Murase, K., Kato, J., Kobune, M., Sato, T., Kawano, Y., Takimoto, R., Takada, K., Miyanishi, K., Matsunaga, T., Takayama, T., Niitsu, Y., Resolution of liver cirrhosis using vitamin A-coupled liposomes to deliver siRNA against a collagen-specific chaperone. Nat. Biotechnol. 26 (2008), 431–442.
52. [52] Zhang, Z., Wang, C., Zha, Y., Hu, W., Gao, Z., Zang, Y., Chen, J., Zhang, J., Dong, L., Corona-directed nucleic acid delivery into hepatic stellate cells for liver fibrosis therapy. ACS Nano 9 (2015), 2405–2419.
53. [53] Wang, Q.-B., Han, Y., Jiang, T.-T., Chai, W.-M., Chen, K.-M., Liu, B.-Y., Wang, L.-F., Zhang, C., Wang, D.-B., MR imaging of activated hepatic stellate cells in liver injured by CCl4 of rats with integrin-targeted ultrasmall superparamagnetic iron oxide. Eur. J. Radiol. 21 (2011), 1016–1025.
54. [54] Selim, K.M., Ha, Y.-S., Kim, S.-J., Chang, Y., Kim, T.-J., Ho Lee, G., Kang, I.-K., Surface modification of magnetite nanoparticles using lactobionic acid and their interaction with hepatocytes. Biomaterials 28 (2007), 710–716.
55. [55] Lee, C.-M., Jeong, H.-J., Kim, E.-M., Kim, D.W., Lim, S.T., Kim, H.T., Park, I.-K., Jeong, Y.Y., Kim, J.W., Sohn, M.-H., Superparamagnetic iron oxide nanoparticles as a dual imaging probe for targeting hepatocytes in vivo. Magn. Reson. Med. 62 (2009), 1440–1446.
56. [56] Peng, J., Wang, K., Tan, W., He, X., He, C., Wu, P., Liu, F., Identification of live liver cancer cells in a mixed cell system using galactose-conjugated fluorescent nanoparticles. Talanta 71 (2007), 833–840.
57. [57] Xu, Z., Chen, L., Gu, W., Gao, Y., Lin, L., Zhang, Z., Xi, Y., Li, Y., The performance of docetaxel-loaded solid lipid nanoparticles targeted to hepatocellular carcinoma. Biomaterials 30 (2009), 226–232.
58. [58] Yang, Y., Yuan, S.-X., Zhao, L.-H., Wang, C., Ni, J.-S., Wang, Z.-G., Lin, C., Wu, M.-C., Zhou, W.-P., Ligand-directed stearic acid grafted chitosan micelles to increase therapeutic efficacy in hepatic cancer. Mol. Pharm. 12 (2015), 644–652.
59. [59] Yang, K.W., Li, X.R., Yang, Z.L., Li, P.Z., Wang, F., Liu, Y., Novel polyion complex micelles for liver-targeted delivery of diammonium glycyrrhizinate: in vitro and in vivo characterization. J. Biomed. Mater. Res. A 88 (2008), 140–148.
60. [60] Wu, J., Sun, T.-M., Yang, X.-Z., Zhu, J., Du, X.-J., Yao, Y.-D., Xiong, M.-H., Wang, H.-X., Wang, Y.-C., Wang, J., Enhanced drug delivery to hepatocellular carcinoma with a galactosylated core–shell polyphosphoester nanogel. Biomater. Sci., 1, 2013, 1143.
61. [61] Yu, F., Jiang, T., Zhang, J., Cheng, L., Wang, S., Galactosylated liposomes as oligodeoxynucleotides carrier for hepatocyte-selective targeting. Pharmazie, 62, 2007.
62. [62] Jiang, N., Zhang, X., Zheng, X., Chen, D., Zhang, Y., Siu, L.K.S., Xin, H.-B., Li, R., Zhao, H., Riordan, N., Ichim, T.E., Quan, D., Jevnikar, A.M., Chen, G., Min, W., Targeted gene silencing of TLR4 using liposomal nanoparticles for preventing liver ischemia reperfusion injury. Am. J. Transplant. 11 (2011), 1835–1844.
63. [63] Jiang, N., Zhang, X., Zheng, X., Chen, D., Siu, K., Wang, H., Ichim, T.E., Quan, D., McAlister, V., Chen, G., Min, W.-P., A novel in vivo siRNA delivery system specifically targeting liver cells for protection of ConA-induced fulminant hepatitis. PLoS One, 7, 2012, e44138.
64. [64] Gupta, S., Agarwal, A., Gupta, N.K., Saraogi, G., Agrawal, H., Agrawal, G.P., Galactose decorated PLGA nanoparticles for hepatic delivery of acyclovir. Drug Dev. Ind. Pharm. 39 (2013), 1866–1873.
65. [65] Cheng, M., He, B., Wan, T., Zhu, W., Han, J., Zha, B., Chen, H., Yang, F., Li, Q., Wang, W., Xu, H., Ye, T., 5-Fluorouracil nanoparticles inhibit hepatocellular carcinoma via activation of the p53 pathway in the orthotopic transplant mouse model. PLoS One, 7, 2012, e47115.
66. [66] Zheng, D., Duan, C., Zhang, D., Jia, L., Liu, G., Liu, Y., Wang, F., Li, C., Guo, H., Zhang, Q., Galactosylated chitosan nanoparticles for hepatocyte-targeted delivery of oridonin. Int. J. Pharm. 436 (2012), 379–386.
67. [67] Liang, H.-F., Chen, S.-C., Chen, M.-C., Lee, P.-W., Chen, C.-T., Sung, H.-W., Paclitaxel-loaded poly(gamma-glutamic acid)-poly(lactide) nanoparticles as a targeted drug delivery system against cultured HepG2 cells. Bioconjug. Chem. 17 (2006), 291–299.
68. [68] Liang, H.-F., Chen, C.-T., Sung-Ching, C., Kulkarni, A.R., Chiu, Y.-L., Chen, M.-C., Sung, H.-W., Paclitaxel-loaded poly(gamma-glutamic acid)-poly(lactide) nanoparticles as a targeted drug delivery system for the treatment of liver cancer. Biomaterials 27 (2006), 2051–2059.
69. [69] Wang, S.-N., Deng, Y.-H., Xu, H., Wu, H.-B., Qiu, Y.-K., Chen, D.-W., Synthesis of a novel galactosylated lipid and its application to the hepatocyte-selective targeting of liposomal doxorubicin. Eur. J. Pharm. Biopharm. 62 (2006), 32–38.
70. [70] Guhagarkar, S.A., Gaikwad, R.V., Samad, A., Malshe, V.C., Devarajan, P.V., Polyethylene sebacate-doxorubicin nanoparticles for hepatic targeting. Int. J. Pharm. 401 (2010), 113–122.
71. [71] Qi, X.-R., Yan, W.-W., Shi, J., Hepatocytes targeting of cationic liposomes modified with soybean sterylglucoside and polyethylene glycol. World J. Gastroenterol. 11 (2005), 4947–4952.
72. [72] Cheng, M., Gao, X., Wang, Y., Chen, H., He, B., Xu, H., Li, Y., Han, J., Zhang, Z., Synthesis of glycyrrhetinic acid-modified chitosan 5-fluorouracil nanoparticles and its inhibition of liver cancer characteristics in vitro and in vivo. Mar. Drugs 11 (2013), 3517–3536.
73. [73] Tian, Q., Wang, X.-H., Wang, W., Zhang, C.-N., Wang, P., Yuan, Z., Self-assembly and liver targeting of sulfated chitosan nanoparticles functionalized with glycyrrhetinic acid. Nanomedicine 8 (2012), 870–879.
74. [74] Shi, L., Tang, C., Yin, C., Glycyrrhizin-modified O-carboxymethyl chitosan nanoparticles as drug vehicles targeting hepatocellular carcinoma. Biomaterials 33 (2012), 7594–7604.
75. [75] Huang, W., Wang, W., Wang, P., Tian, Q., Zhang, C., Wang, C., Yuan, Z., Liu, M., Wan, H., Tang, H., Glycyrrhetinic acid-modified poly(ethylene glycol)-b-poly(gamma-benzyl l-glutamate) micelles for liver targeting therapy. Acta Biomater. 6 (2010), 3927–3935.
76. [76] Zhang, C., Wang, W., Liu, T., Wu, Y., Guo, H., Wang, P., Tian, Q., Wang, Y., Yuan, Z., Doxorubicin-loaded glycyrrhetinic acid-modified alginate nanoparticles for liver tumor chemotherapy. Biomaterials 33 (2012), 2187–2196.
77. [77] Guo, H., Lai, Q., Wang, W., Wu, Y., Zhang, C., Liu, Y., Yuan, Z., Functional alginate nanoparticles for efficient intracellular release of doxorubicin and hepatoma carcinoma cell targeting therapy. Int. J. Pharm. 451 (2013), 1–11.
78. [78] Cheong, S.-J., Lee, C.-M., Kim, S.-L., Jeong, H.-J., Kim, E.-M., Park, E.-H., Kim, D.W., Lim, S.T., Sohn, M.-H., Superparamagnetic iron oxide nanoparticles-loaded chitosan-linoleic acid nanoparticles as an effective hepatocyte-targeted gene delivery system. Int. J. Pharm. 372 (2009), 169–176.
79. [79] Longmuir, K.J., Haynes, S.M., Baratta, J.L., Kasabwalla, N., Robertson, R.T., Liposomal delivery of doxorubicin to hepatocytes in vivo by targeting heparan sulfate. Int. J. Pharm. 382 (2009), 222–233.
80. [80] Gao, D.-Y., Lin, T.-T., Sung, Y.-C., Liu, Y.C., Chiang, W.-H., Chang, C.-C., Liu, J.-Y., Chen, Y., CXCR4-targeted lipid-coated PLGA nanoparticles deliver sorafenib and overcome acquired drug resistance in liver cancer. Biomaterials 67 (2015), 194–203.
81. [81] Zhang, X., Zhang, Q., Peng, Q., Zhou, J., Liao, L., Sun, X., Zhang, L., Gong, T., Hepatitis B virus preS1-derived lipopeptide functionalized liposomes for targeting of hepatic cells. Biomaterials 35 (2014), 6130–6141.
82. [82] Rui, M., Guo, W., Ding, Q., Wei, X., Xu, J., Xu, Y., Recombinant high-density lipoprotein nanoparticles containing gadolinium-labeled cholesterol for morphologic and functional magnetic resonance imaging of the liver. Int. J. Nanomedicine 7 (2012), 3751–3768.
83. [83] Skajaa, T., Cormode, D.P., Jarzyna, P.A., Delshad, A., Blachford, C., Barazza, A., Fisher, E.A., Gordon, R.E., Fayad, Z.A., Mulder, W.J.M., The biological properties of iron oxide core high-density lipoprotein in experimental atherosclerosis. Biomaterials 32 (2011), 206–213.
84. [84] Kim, S.I., Shin, D., Choi, T.H., Lee, J.C., Cheon, G.-J., Kim, K.-Y., Park, M., Kim, M., Systemic and specific delivery of small interfering RNAs to the liver mediated by apolipoprotein A-I. Mol. Ther. 15 (2007), 1145–1152.
85. [85] Renaud, G., Hamilton, R.L., Havel, R.J., Hepatic metabolism of colloidal gold-low-density lipoprotein complexes in the rat: evidence for bulk excretion of lysosomal contents into bile. Hepatology 9 (1989), 380–392.
86. [86] Moghimi, S.M., Hunter, A.C., Murray, J.C., Long-circulating and target-specific nanoparticles: theory to practice. Pharmacol. Rev. 53 (2001), 283–318.
87. [87] Longmire, M., Choyke, P.L., Kobayashi, H., Clearance properties of nano-sized particles and molecules as imaging agents: considerations and caveats. Nanomedicine 3 (2008), 703–717.
88. [88] He, C., Hu, Y., Yin, L., Tang, C., Yin, C., Effects of particle size and surface charge on cellular uptake and biodistribution of polymeric nanoparticles. Biomaterials 31 (2010), 3657–3666.
89. [89] Ogawara, K.-i., Yoshida, M., Higaki, K., Kimura, T., Shiraishi, K., Nishikawa, M., Takakura, Y., Hashida, M., Hepatic uptake of polystyrene microshperes in rats: effect of particle size on intrahepatic distribution. J. Control. Release 59 (1999), 15–22.
90. [90] Takakura, Y., Mahato, R.I., Hashida, M., Extravasation of macromolecules. Adv. Drug Deliv. Rev. 34 (1998), 93–108.
91. [91] Gaumet, M., Vargas, A., Gurny, R., Delie, F., Nanoparticles for drug delivery: the need for precision in reporting particle size parameters. Eur. J. Pharm. Biopharm. 69 (2008), 1–9.
92. [92] Poelstra, K., Prakash, J., Beljaars, L., Drug targeting to the diseased liver. J. Control. Release 161 (2012), 188–197.
93. [93] Bartsch, M., Meijer, D.K.F., Weeke-Klimp, A.H., Scherphof, G.L., Kamps, J.A.A.M., Massive and selective delivery of lipid-coated cationic lipoplexes of oligonucleotides targeted in vivo to hepatic endothelial cells. Pharm. Res., 19, 2002.
94. [94] Chevallier, P., Walter, A., Garofalo, A., Veksler, I., Lagueux, J., Bégin-Colin, S., Felder-Flesch, D., Fortin, M.-A., Tailored biological retention and efficient clearance of pegylated ultra-small MnO nanoparticles as positive MRI contrast agents for molecular imaging. J. Mater. Chem. B, 2, 2014, 1779.
95. [95] Yang, L., Lee, Y.-C., Kim, M.I., Park, H.G., Huh, Y.S., Shao, Y., Han, H.-K., Biodistribution and clearance of aminoclay nanoparticles: implication for in vivo applicability as a tailor-made drug delivery carrier. J. Mater. Chem. B 2 (2014), 7567–7574.
96. [96] Chen, Z., Chen, H., Meng, H., Xing, G., Gao, X., Sun, B., Shi, X., Yuan, H., Zhang, C., Liu, R., Zhao, F., Zhao, Y., Fang, X., Bio-distribution and metabolic paths of silica coated CdSeS quantum dots. Toxicol. Appl. Pharmacol. 230 (2008), 364–371.
97. [97] Bourrinet, P., Bengele, H.H., Bonnemain, B., Dencausse, A., Idee, J.-M., Jacobs, P.M., Lewis, J.M., Preclinical safety and pharmacokinetic profile of ferumoxtran-10, an ultrasmall superparamagnetic iron oxide magnetic resonance contrast agent. Investig. Radiol. 41 (2006), 313–324.
98. [98] Kumar, R., Roy, I., Ohulchanskky, T.Y., Vathy, L.A., Bergey, E.J., Sajjad, M., Prasad, P.N., In vivo biodistribution and clearance studies using multimodal organically modified silica nanoparticles. ACS Nano 4 (2010), 699–708.
99. [99] Lu, J., Liong, M., Li, Z., Zink, J.I., Tamanoi, F., Biocompatibility, biodistribution, and drug-delivery efficiency of mesoporous silica nanoparticles for cancer therapy in animals. Small 6 (2010), 1794–1805.
100. [100] Ye, S., Marston, G., McLaughlan, J.R., Sigle, D.O., Ingram, N., Freear, S., Baumberg, J.J., Bushby, R.J., Markham, A.F., Critchley, K., Coletta, P.L., Evans, S.D., Engineering gold nanotubes with controlled length and near-infrared absorption for theranostic applications. Adv. Funct. Mater. 25 (2015), 2117–2127.
101. [101] Semmler-Behnke, M., Kreyling, W.G., Lipka, J., Fertsch, S., Wenk, A., Takenaka, S., Schmid, G., Brandau, W., Biodistribution of 1.4- and 18-nm gold particles in rats. Small 4 (2008), 2108–2111.
102. [102] Hirn, S., Semmler-Behnke, M., Schleh, C., Wenk, A., Lipka, J., Schäffler, M., Takenaka, S., Möller, W., Schmid, G., Simon, U., Kreyling, W.G., Particle size-dependent and surface charge-dependent biodistribution of gold nanoparticles after intravenous administration. Eur. J. Pharm. Biopharm. 77 (2011), 407–416.
103. [103] Wang, L., Li, Y.-F., Zhou, L., Liu, Y., Meng, L., Zhang, K., Wu, X., Zhang, L., Li, B., Chen, C., Characterization of gold nanorods in vivo by integrated analytical techniques: their uptake, retention, and chemical forms. Anal. Bioanal. Chem. 396 (2010), 1105–1114.
104. [104] Sadauskas, E., Danscher, G., Stoltenberg, M., Vogel, U., Larsen, A., Wallin, H., Protracted elimination of gold nanoparticles from mouse liver. Nanomedicine 5 (2009), 162–169.
105. [105] Balasubramanian, S.K., Jittiwat, J., Manikandan, J., Ong, C.-N., Yu, L.E., Ong, W.-Y., Biodistribution of gold nanoparticles and gene expression changes in the liver and spleen after intravenous administration in rats. Biomaterials 31 (2010), 2034–2042.
106. [106] Jain, T.K., Reddy, M.K., Morales, M.A., Leslie-Pelecky, D.L., Labhasetwar, V., Biodistribution, clearance, and biocompatibility of iron oxide magnetic nanoparticles in rats. Mol. Pharm. 5 (2008), 316–327.
107. [107] Sykes, E.A., Dai, Q., Tsoi, K.M., Hwang, D.M., Chan, W.C.W., Nanoparticle exposure in animals can be visualized in the skin and analysed via skin biopsy. Nat. Commun., 5, 2014, 3796.
108. [108] Huang, X., Li, L., Liu, T., Hao, N., Liu, H., Chen, D., Tang, F., The shape effect of mesoporous silica nanoparticles on biodistribution, clearance, and biocompatibility in vivo. ACS Nano 5 (2011), 5390–5399.
109. [109] Cho, M., Cho, W.-S., Choi, M., Kim, S.J., Han, B.S., Kim, S.H., Kim, H.O., Sheen, Y.Y., Jeong, J., The impact of size on tissue distribution and elimination by single intravenous injection of silica nanoparticles. Toxicol. Lett. 189 (2009), 177–183.
110. [110] Souris, J.S., Lee, C.-H., Cheng, S.-H., Chen, C.-T., Yang, C.-S., Ho, J.-a.A., Mou, C.-Y., Lo, L.-W., Surface charge-mediated rapid hepatobiliary excretion of mesoporous silica nanoparticles. Biomaterials 31 (2010), 5564–5574.
111. [111] Fu, C., Liu, T., Li, L., Liu, H., Chen, D., Tang, F., The absorption, distribution, excretion and toxicity of mesoporous silica nanoparticles in mice following different exposure routes. Biomaterials 34 (2013), 2565–2575.
112. [112] Yu, T., Hubbard, D., Ray, A., Ghandehari, H., In vivo biodistribution and pharmacokinetics of silica nanoparticles as a function of geometry, porosity and surface characteristics. J. Control. Release 163 (2012), 46–54.
113. [113] Bulte, J.W.M., Schmieder, A.H., Keupp, J., Caruthers, S.D., Wickline, S.A., Lanza, G.M., MR cholangiography demonstrates unsuspected rapid biliary clearance of nanoparticles in rodents: implications for clinical translation. Nanomedicine 10 (2014), 1385–1388.
114. [114] Lipka, J., Semmler-Behnke, M., Sperling, R.A., Wenk, A., Takenaka, S., Schleh, C., Kissel, T., Parak, W.J., Kreyling, W.G., Biodistribution of PEG-modified gold nanoparticles following intratracheal instillation and intravenous injection. Biomaterials 31 (2010), 6574–6581.
115. [115] Xiao, J., Tian, X.M., Yang, C., Liu, P., Luo, N.Q., Liang, Y., Li, H.B., Chen, D.H., Wang, C.X., Li, L., Yang, G.W., Ultrahigh relaxivity and safe probes of manganese oxide nanoparticles for in vivo imaging. Sci. Rep., 3, 2013.
116. [116] Park, K., Park, E.-J., Chun, I.K., Choi, K., Lee, S.H., Yoon, J., Lee, B.C., Bioavailability and toxicokinetics of citrate-coated silver nanoparticles in rats. Arch. Pharm. Res. 34 (2011), 153–158.
117. [117] Watson, C.Y., Molina, R.M., Louzada, A., Murdaugh, K.M., Donaghey, T.C., Brain, J.D., Effects of zinc oxide nanoparticles on Kupffer cell phagosomal motility, bacterial clearance, and liver function. Int. J. Nanomedicine 10 (2015), 4173–4184.
118. [118] Liu, C., Gao, Z., Zeng, J., Hou, Y., Fang, F., Li, Y., Qiao, R., Shen, L., Lei, H., Yang, W., Gao, M., Magnetic/upconversion fluorescent NaGdF4:Yb,Er nanoparticle-based dual-modal molecular probes for imaging tiny tumors in vivo. ACS Nano 7 (2013), 7227–7240.
119. [119] Amoozgar, Z., Yeo, Y., Recent advances in stealth coating of nanoparticle drug delivery systems. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 4 (2012), 219–233.
120. [120] Karmali, P.P., Simberg, D., Interactions of nanoparticles with plasma proteins: implication on clearance and toxicity of drug delivery systems. Expert Opin. Drug Deliv. 8 (2011), 343–357.
121. [121] Desai, N., Challenges in development of nanoparticle-based therapeutics. AAPS J. 14 (2012), 282–295.
122. [122] Choi, H.S., Liu, W., Misra, P., Tanaka, E., Zimmer, J.P., Itty Ipe, B., Bawendi, M.G., Frangioni, J.V., Renal clearance of quantum dots. Nat. Biotechnol. 25 (2007), 1165–1170.
123. [123] Elsabahy, M., Wooley, K.L., Design of polymeric nanoparticles for biomedical delivery applications. Chem. Soc. Rev. 41 (2012), 2545–2561.
124. [124] Lacava, L.M., Garcia, V., Kuchelhaus, S., Azevedo, R.B., Sadeghiani, N., Buske, N., Morais, P.C., Lacava, Z.G.M., Long-term retention of dextran-coated magnetite nanoparticles in the liver and spleen. J. Magn. Magn. Mater. 272–276 (2004), 2434–2435.
125. [125] Kolosnjaj-Tabi, J., Javed, Y., Lartigue, L., Volatron, J., Elgrabli, D., Marangon, I., Pugliese, G., Caron, B., Figuerola, A., Luciani, N., Pellegrino, T., Alloyeau, D., Gazeau, F., The one year fate of iron oxide coated gold nanoparticles in mice. ACS Nano 9 (2015), 7925–7939.
126. [126] Pan, Y., Neuss, S., Leifert, A., Fischler, M., Wen, F., Simon, U., Schmid, G., Brandau, W., Jahnen-Dechent, W., Size-dependent cytotoxicity of gold nanoparticles. Small 3 (2007), 1941–1949.
127. [127] Xia, T., Kovochich, M., Liong, M., Mädler, L., Gilbert, B., Shi, H., Yeh, J.I., Zink, J.I., Nel, A.E., Comparison of the mechanism of toxicity of zinc oxide and cerium oxide nanoparticles based on dissolution and oxidative stress properties. ACS Nano 2 (2008), 2121–2134.
128. [128] George, S., Pokhrel, S., Xia, T., Gilbert, B., Ji, Z., Schowalter, M., Rosenauer, A., Damoiseaux, R., Bradley, K.A., Mädler, L., Nel, A.E., Use of a rapid cytotoxicity screening approach to engineer a safer zinc oxide nanoparticle through iron doping. ACS Nano 4 (2010), 15–29.
129. [129] Paek, H.-J., Lee, Y.-J., Chung, H.-E., Yoo, N.-H., Lee, J.-A., Kim, M.-K., Lee, J.K., Jeong, J., Choi, S.-J., Modulation of the pharmacokinetics of zinc oxide nanoparticles and their fates in vivo. Nanoscale 5 (2013), 11416–11427.
130. [130] Krebs, N.F., Hambidge, K.M., Zinc metabolism and homeostasis: the application of tracer techniques to human zinc physiology. Biometals 14 (2001), 397–412.
131. [131] Martinez-Finley, E.J., Chakraborty, S., J.B., F., Aschner, M., Cellular transport and homeostasis of essential and nonessential metals. Metallomics 4 (2012), 593–605.
132. [132] Hower, V., Mendes, P., Torti, F.M., Laubenbacher, R., Akman, S., Shulaev, V., Torti, S.V., A general map of iron metabolism and tissue-specific subnetworks. Mol. BioSyst. 5 (2009), 422–443.
133. [133] Papanikolaou, G., Pantopoulos, K., Iron metabolism and toxicity. Toxicol. Appl. Pharmacol. 202 (2005), 199–211.
134. [134] Briley-Saebo, K., Ahlstrom, H., Bjørnerud, A., Berg, T., Grant, D., Kindberg, G.M., Hepatic cellular distribution and degradation of iron oxide nanoparticles following single intravenous injection in rats: implications for magnetic resonance imaging. Cell Tissue Res. 316 (2004), 315–323.
135. [135] Levy, M., Luciani, N., Alloyeau, D., Elgrabli, D., Deveaux, V., Pechoux, C., Chat, S., Wang, G., Vats, N., Gendron, F., Factor, C., Lotersztajn, S., Luciani, A., Wilhelm, C., Gazeau, F., Long term in vivo biotransformation of iron oxide nanoparticles. Biomaterials 32 (2011), 3988–3999.
136. [136] King, E.J., Mcgeorge, M., The biochemistry of silicic acid. Biochem. J. 32 (1938), 426–433.
137. [137] He, Q., Zhang, Z., Gao, Y., Shi, J., Li, Y., Intracellular localization and cytotoxicity of spherical mesoporous silica nano- and microparticles. Small 5 (2009), 2722–2729.
138. [138] Park, J.-H., Gu, L., von Maltzahn, G., Ruoslahti, E., Bhatia, S.N., Sailor, M.J., Biodegradable luminescent porous silicon nanoparticles for in vivo applications. Nat. Mater. 8 (2009), 331–336.
139. [139] He, X., Nie, H., Wang, K., Tan, W., Wu, X., Zhang, P., In vivo study of biodistribution and urinary excretion of surface-modified silica nanoparticles. Anal. Chem. 80 (2008), 9597–9603.
140. [140] Chen, F., Goel, S., Valdovinos, H.F., Luo, H., Hernandez, R., Barnhart, T.E., Cai, W., In vivo integrity and biological fate of chelator-free zirconium-89-labeled mesoporous silica nanoparticles. ACS Nano 9 (2015), 7950–7959.
141. [141] D'Souza, A.A., Devarajan, P.V., Asialoglycoprotein receptor mediated hepatocyte targeting — strategies and applications. J. Control. Release 203 (2015), 126–139.
142. [142] Bergen, J.M., von Recum, H.A., Goodman, T.T., Massey, A.P., Pun, S.H., Gold nanoparticles as a versatile platform for optimizing physicochemical parameters for targeted drug delivery. Macromol. Biosci. 6 (2006), 506–516.
143. [143] Yamada, T., Iwasaki, Y., Tada, H., Iwabuki, H., Chuah, M.K., VandenDriessche, T., Fukuda, H., Kondo, A., Ueda, M., Seno, M., Tanizawa, K., Kuroda, S., Nanoparticles for the delivery of genes and drugs to human hepatocytes. Nat. Biotechnol. 21 (2003), 885–890.
144. [144] Cheng, S.-H., Li, F.-C., Souris, J.S., Yang, C.-S., Tseng, F.-G., Lee, H.-S., Chen, C.-T., Dong, C.-Y., Lo, L.-W., Visualizing dynamics of sub-hepatic distribution of nanoparticles using intravital multiphoton fluorescence microscopy. ACS Nano 6 (2012), 4122–4131.
145. [145] Eberle, D., Clarke, R., Kaplowitz, N., Rapid oxidation in vitro of endogenous and exogenous glutathione in bile of rats. J. Biol. Chem. 256 (1980), 2115–2117.
146. 1H NMR spectroscopy. Magn. Reson. Med. 53 (2005), 1441–1446.
147. [147] Walter, A., Garofalo, A., Parat, A., Jouhannaud, J., Pourroy, G., Voirin, E., Laurent, S., Bonazza, P., Taleb, J., Billotey, C., Vander Elst, L., Muller, R.N., Begin-Colin, S., Felder-Flesch, D., Validation of a dendron concept to tune colloidal stability, MRI relaxivity and bioelimination of functional nanoparticles. J. Mater. Chem. B 3 (2015), 1484–1494.
148. [148] Lamanna, G., Kueny-Stotz, M., Mamlouk-Chaouachi, H., Ghobril, C., Basly, B., Bertin, A., Miladi, I., Billotey, C., Pourroy, G., Begin-Colin, S., Felder-Flesch, D., Dendronized iron oxide nanoparticles for multimodal imaging. Biomaterials 32 (2011), 8562–8573.
149. [149] Lin, C.-J., Kang, N., Lee, J.-Y., Lee, H.-S., Dong, C.-Y., Visualizing and quantifying difference in cytoplasmic and nuclear metabolism in the hepatobiliary system in vivo. J. Biomed. Opt., 20, 2015, 16020.
150. [150] Geng, Y., Dalhaimer, P., Cai, S., Tsai, R., Tewari, M., Minko, T., Discher, D.E., Shape effects of filaments versus spherical particles in flow and drug delivery. Nat. Nanotechnol. 2 (2007), 249–255.
151. [151] 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 (2011), 84–92.
152. [152] Arnida, M.M., Janát-Amsbury, A., Ray, C.M., Peterson, H., Ghandehari, geometry and surface characteristics of gold nanoparticles influence their biodistribution and uptake by macrophages. Eur. J. Pharm. Biopharm. 77 (2011), 417–423.
153. [153] Decuzzi, P., Godin, B., Tanaka, T., Lee, S.-Y., Chiappini, C., Liu, X., Ferrari, M., Size and shape effects in the biodistribution of intravascularly injected particles. J. Control. Release 141 (2010), 320–327.
154. [154] Champion, J.A., Mitragotri, S., Shape induced inhibition of phagocytosis of polymer particles. Pharm. Res. 26 (2009), 244–249.
155. [155] Musyanovych, A., Dausend, J., Dass, M., Walther, P., Mailänder, V., Landfester, K., Criteria impacting the cellular uptake of nanoparticles: a study emphasizing polymer type and surfactant effects. Acta Biomater. 7 (2011), 4160–4168.
156. [156] Beningo, K.A., Wang, Y.-L., Fc-receptor-mediated phagocytosis is regulated by mechanical properties of the target. J. Cell Sci. 115 (2002), 849–856.
157. [157] Merkel, T.J., Jones, S.W., Herlihy, K.P., Kersey, F.R., Shields, A.R., Napier, M., Luft, J.C., Wu, H., Zamboni, W.C., Wang, A.Z., Bear, J.E., DeSimone, J.M., Using mechanobiological mimicry of red blood cells to extend circulation times of hydrogel microparticles. Proc. Natl. Acad. Sci. U. S. A. 108 (2011), 586–591.
158. [158] Gabizon, A.A., Liposome circulation time and tumor targeting: implications for cancer chemotherapy. Adv. Drug Deliv. Rev. 16 (1995), 285–294.
159. [159] Dai, Q., Walkey, C., Chan, W.C.W., Polyethylene glycol backfilling mitigates the negative impact of the protein corona on nanoparticle cell targeting. Angew. Chem. Int. Ed. 53 (2014), 5093–5096.
160. [160] Bartneck, M., Keul, H.A., Singh, S., Czaja, K., Bornemann, J., Bockstaller, M., Moeller, M., Zwadlo-Klarwasser, G., Groll, J., Rapid uptake of gold nanorods by primary human blood phagocytes and immunomodulatory effects of surface chemistry. ACS Nano 4 (2010), 3073–3086.
161. [161] Keefe, A.J., Jiang, S., Poly(zwitterionic)protein conjugates offer increased stability without sacrificing binding affinity or bioactivity. Nat. Chem. 4 (2012), 59–63.
162. [162] Schlenoff, J.B., Zwitteration: coating surfaces with zwitterionic functionality to reduce nonspecific adsorption. Langmuir 30 (2014), 9625–9636.
163. [163] Jiang, S., Cao, Z., Ultralow-fouling, functionalizable, and hydrolyzable zwitterionic materials and their derivatives for biological applications. Adv. Mater. 22 (2010), 920–932.
164. [164] Liu, T., Choi, H., Zhou, R., Chen, I.-W., RES blockade: a strategy for boosting efficiency of nanoparticle drug. Nano Today 10 (2015), 11–21.
165. [165] Torchilin, V.P., Recent advances with liposomes as pharmaceutical carriers. Nat. Rev. Drug Discov. 4 (2005), 145–160.
166. [166] van Rooijen, N., Sanders, A., Liposome mediated depletion of macrophage, mechanism of action, preparation of liposomes and applications. J. Immunol. Methods 174 (1994), 83–93.
167. [167] van Rooijen, N., Liposomes for targeting of antigens and drugs: immunoadjuvant activity and liposome-mediated depletion of macrophages. J. Drug Target. 16 (2008), 529–534.
168. [168] Lehenkari, P.P., Kellinsalmi, M., Näpänkangas, J.P., Ylitalo, K.V., Mönkkönen, J., Rogers, M.J., Azhayev, A., Väänänen, H.K., Hassinen, I.E., Further insight into mechanism of action of clodronate: inhibition of mitochondrial ADP/ATP translocase by a nonhydrolyzable, adenine-containing metabolite. Mol. Pharmacol. 62 (2002), 1255–1262.
169. [169] Kirby, A.C., Beattie, L., Maroof, A., van Rooijen, N., Kaye, P.M., SIGNR1-negative red pulp macrophages protect against acute streptococcal sepsis after Leishmania donovani-induced loss of marginal zone macrophages. Am. J. Pathol. 175 (2009), 1107–1115.
170. [170] Hu, Q., van Rooijen, N., Liu, D., Effect of macrophage elimination using liposome-encapsulated dichloromethylene diphosphonate on tissue distribution of liposomes. J. Lipid Res. 6 (1996), 681–698.
171. [171] Ohara, Y., Oda, T., Yamada, K., Hashimoto, S., Akashi, Y., Miyamoto, R., Kobayashi, A., Fukunaga, K., Sasaki, R., Ohkohchi, N., Effective delivery of chemotherapeutic nanoparticles by depleting host Kupffer cells. Int. J. Cancer 131 (2012), 2402–2410.
172. [172] Simberg, D., Duza, T., Park, J.H., Essler, M., Pilch, J., Zhang, L., Derfus, A.M., Yang, M., Hoffman, R.M., Bhatia, S., Sailor, M.J., Ruoslahti, E., Biomimetic amplification of nanoparticle homing to tumors. Proc. Natl. Acad. Sci. U. S. A. 104 (2007), 932–936.
173. 125mTe/ZnS nanoparticles in vivo. Nucl. Med. Biol. 35 (2008), 501–514.
174. [174] Ruttinger, D., Vollmar, B., Wanner, G.A., Messmer, K., In vivo assessment of hepatic alterations following gadolinium chloride-induced Kupffer cell blockade. J. Hepatol. 25 (1996), 960–967.
175. [175] Husztik, E., Lazar, G., Parducz, A., Electron microscopic study of Kupffer-cell phagocytosis blockade induced by gadolinium chloride. Br. J. Exp. Pathol. 61 (1980), 624–630.
176. [176] Hardonk, M.J., Dijkhuis, F., Hulstaert, C.E., Koudstaal, J., Heterogeneity of rat liver and spleen macrophages in Gadolinium chloride-induced elimination and repopulation. J. Leukoc. Biol. 52 (1992), 296–302.
177. [177] Diagaradjane, P., Deorukhkar, A., Gelovani, J.G., Maru, D.M., Krishnan, S., Gadolinium chloride augments tumor-specific imaging of targeted quantum dots in vivo. ACS Nano 4 (2010), 4131–4141.
178. [178] Yoo, J.-W., Irvine, D.J., Discher, D.E., Mitragotri, S., Bio-inspired, bioengineered and biomimetic drug delivery carriers. Nat. Rev. Drug Discov. 10 (2011), 521–535.
179. [179] Anselmo, A.C., Gupta, V., Zern, B.J., Pan, D., Zakrewsky, M., Muzykantov, V., Mitragotri, S., Delivering nanoparticles to lungs while avoiding liver and spleen through adsorption on red blood cells. ACS Nano 7 (2013), 11129–11137.
180. [180] Parodi, A., Quattrocchi, N., van de Ven, A.L., Chiappini, C., Evangelopoulos, M., Martinez, J.O., Brown, B.S., Khaled, S.Z., Yazdi, I.K., Enzo, M.V., Isenhart, L., Ferrari, M., Tasciotti, E., Synthetic nanoparticles functionalized with biomimetic leukocyte membranes possess cell-like functions. Nat. Nanotechnol. 8 (2013), 61–68.
181. [181] Choi, M.-R., Stanton-Maxey, K.J., Stanley, J.K., Levin, C.S., Bardhan, R., Akin, D., Badve, S., Sturgis, J., Robinson, J.P., Bashir, R., Halas, N.J., Clare, S.E., A cellular Trojan Horse for delivery of therapeutic nanoparticles into tumors. Nano Lett. 7 (2007), 3759–3765.
182. [182] Choi, J., Kim, H.-Y., Ju, E.J., Jung, J., Park, J., Chung, H.-K., Lee, J.S., Lee, J.S., Park, H.J., Song, S.Y., Jeong, S.-Y., Choi, E.K., Use of macrophages to deliver therapeutic and imaging contrast agents to tumors. Biomaterials 33 (2012), 4195–4203.
183. [183] Doshi, N., Zahr, A.S., Bhaskar, S., Lahann, J., Mitragotri, S., Red blood cell-mimicking synthetic biomaterial particles. Proc. Natl. Acad. Sci. U. S. A. 106 (2009), 21495–21499.
184. [184] Hu, C.-M.J., Fang, R.H., Copp, J., Luk, B.T., Zhang, L., A biomimetic nanosponge that absorbs pore-forming toxins. Nat. Nanotechnol. 8 (2013), 336–340.