Drug delivery to macrophages: Challenges and opportunities

Journal of Controlled Release

Volumn 240, Issue , 2016, Pages 202-211

  Pei, Yihua ^a   Yeo, Yoon ^a,b  

^a PURDUE UNIVERSITY   (United States)

^b PURDUE UNIVERSITY   (United States)

Author keywords

Intracellular drug delivery; Intracellular infection; Macrophages; Targeted delivery; Tumor associated macrophages

Indexed keywords

BIOMEDICAL ENGINEERING; CONTROLLED DRUG DELIVERY;

BIODISTRIBUTIONS; CELLULAR UPTAKE; INTRACELLULAR DRUG DELIVERY; INTRACELLULAR INFECTION; INTRACELLULAR TRAFFICKING; TARGETED DELIVERY; THERAPEUTIC TARGETS; TUMOR ASSOCIATED MACROPHAGES;

MACROPHAGES;

DENDRIMER; DRUG CARRIER; LIPOSOME; NANOGEL; POLYMER; UNCLASSIFIED DRUG; DRUG;

ARTICLE; BIOLOGICAL ACTIVITY; CELL MIGRATION; DRUG DELIVERY SYSTEM; DRUG DISTRIBUTION; DRUG RELEASE; DRUG TARGETING; DRUG UPTAKE; HUMAN; MACROPHAGE; NONHUMAN; PARTICLE SIZE; PHARMACOKINETIC PARAMETERS; PRIORITY JOURNAL; SURFACE CHARGE; ANIMAL; DRUG EFFECTS; INTRACELLULAR FLUID; METABOLISM; PHYSIOLOGY; PROCEDURES; TISSUE DISTRIBUTION;

ANIMALS; DRUG DELIVERY SYSTEMS; HUMANS; INTRACELLULAR FLUID; MACROPHAGES; PARTICLE SIZE; PHARMACEUTICAL PREPARATIONS; TISSUE DISTRIBUTION;

EID: 84973653094     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2015.12.014     Document Type: Article

References (132)

1. [1] Wynn, T.A., Chawla, A., Pollard, J.W., Macrophage biology in development, homeostasis and disease. Nature 496 (2013), 445–455.
2. [2] Mosser, D.M., Edwards, J.P., Exploring the full spectrum of macrophage activation. Nat. Rev. Immunol. 8 (2008), 958–969.
3. [3] Gordon, S., Taylor, P.R., Monocyte and macrophage heterogeneity. Nat. Rev. Immunol. 5 (2005), 953–964.
4. [4] Jain, N.K., Mishra, V., Mehra, N.K., Targeted drug delivery to macrophages. Expert Opin. Drug Deliv. 10 (2013), 353–367.
5. [5] Ginhoux, F., Jung, S., Monocytes and macrophages: developmental pathways and tissue homeostasis. Nat. Rev. Immunol. 14 (2014), 392–404.
6. [6] Davies, L.C., Jenkins, S.J., Allen, J.E., Taylor, P.R., Tissue-resident macrophages. Nat. Immunol. 14 (2013), 986–995.
7. [7] Maus, U.A., Koay, M.A., Delbeck, T., Mack, M., Ermert, M., Ermert, L., Blackwell, T.S., Christman, J.W., Schlondorff, D., Seeger, W., Lohmeyer, J., Role of resident alveolar macrophages in leukocyte traffic into the alveolar air space of intact mice. Am. J. Physiol. Lung Cell Mol. Physiol. 282 (2002), L1245–L1252.
8. [8] Kohyama, M., Ise, W., Edelson, B.T., Wilker, P.R., Hildner, K., Mejia, C., Frazier, W.A., Murphy, T.L., Murphy, K.M., Role for Spi-C in the development of red pulp macrophages and splenic iron homeostasis. Nature 457 (2009), 318–321.
9. [9] Ho, V.W., Sly, L.M., Derivation and characterization of murine alternatively activated (M2) macrophages. Methods Mol. Biol. 531 (2009), 173–185.
10. [10] Chavez-Galan, L., Olleros, M.L., Vesin, D., Garcia, I., Much more than M1 and M2 macrophages, there are also CD169(+) and TCR(+) macrophages. Front. Immunol., 6, 2015.
11. [11] Siveen, K.S., Kuttan, G., Role of macrophages in tumour progression. Immunol. Lett. 123 (2009), 97–102.
12. [12] Ostuni, R., Kratochvill, F., Murray, P.J., Natoli, G., Macrophages and cancer: from mechanisms to therapeutic implications. Trends Immunol. 36 (2015), 229–239.
13. [13] Franklin, R.A., Liao, W., Sarkar, A., Kim, M.V., Bivona, M.R., Liu, K., Pamer, E.G., Li, M.O., The cellular and molecular origin of tumor-associated macrophages. Science 344 (2014), 921–925.
14. [14] Jinushi, M., Komohara, Y., Tumor-associated macrophages as an emerging target against tumors: creating a new path from bench to bedside. Biochim. Biophys. Acta 1855 (2015), 123–130.
15. [15] Gabrilovich, D.I., Ostrand-Rosenberg, S., Bronte, V., Coordinated regulation of myeloid cells by tumours. Nat. Rev. Immunol. 12 (2012), 253–268.
16. [16] Curiel, T.J., Coukos, G., Zou, L., Alvarez, X., Cheng, P., Mottram, P., Evdemon-Hogan, M., Conejo-Garcia, J.R., Zhang, L., Burow, M., Zhu, Y., Wei, S., Kryczek, I., Daniel, B., Gordon, A., Myers, L., Lackner, A., Disis, M.L., Knutson, K.L., Chen, L., Zou, W., Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat. Med. 10 (2004), 942–949.
17. [17] Kitamura, T., Qian, B.-Z., Pollard, J.W., Immune cell promotion of metastasis. Nat. Rev. Immunol. 15 (2015), 73–86.
18. [18] Casadevall, A., Evolution of intracellular pathogens. Annu. Rev. Microbiol. 62 (2008), 19–33.
19. [19] Monack, D.M., Mueller, A., Falkow, S., Persistent bacterial infections: the interface of the pathogen and the host immune system. Nat. Rev. Microbiol. 2 (2004), 747–765.
20. [20] Chappuis, F., Sundar, S., Hailu, A., Ghalib, H., Rijal, S., Peeling, R.W., Alvar, J., Boelaert, M., Visceral leishmaniasis: what are the needs for diagnosis, treatment and control?. Nat. Rev. Microbiol. 5 (2007), 873–882.
21. [21] Handman, E., Bullen, D.V.R., Interaction of Leishmania with the host macrophage. Trends Parasitol. 18 (2002), 332–334.
22. [22] Podinovskaia, M., Descoteaux, A., Leishmania and the macrophage: a multifaceted interaction. Future Microbiol 10 (2015), 111–129.
23. [23] Imbuluzqueta, E., Gamazo, C., Ariza, J., Blanco-Prieto, M.J., Drug delivery systems for potential treatment of intracellular bacterial infections. Front. Biosci. 15 (2010), 397–417.
24. [24] Jain, K., Jain, N.K., Novel therapeutic strategies for treatment of visceral leishmaniasis. Drug Discov. Today 18 (2013), 1272–1281.
25. [25] Koppensteiner, H., Brack-Werner, R., Schindler, M., Macrophages and their relevance in human immunodeficiency virus type I infection. Retrovirology 9 (2012), 1742–4690.
26. [26] Kumar, A., Herbein, G., The macrophage: a therapeutic target in HIV-1 infection. Mol. Cell Ther. 2 (2014), 1–15.
27. [27] Van Patten, S.M., Hughes, H., Huff, M.R., Piepenhagen, P.A., Waire, J., Qiu, H., Ganesa, C., Reczek, D., Ward, P.V., Kutzko, J.P., Edmunds, T., Effect of mannose chain length on targeting of glucocerebrosidase for enzyme replacement therapy of gaucher disease. Glycobiology 17 (2007), 467–478.
28. [28] Rodriguez-Lavado, J., de la Mata, M., Jimenez-Blanco, J.L., Garcia-Moreno, M.I., Benito, J.M., Diaz-Quintana, A., Sanchez-Alcazar, J.A., Higaki, K., Nanba, E., Ohno, K., Suzuki, Y., Ortiz Mellet, C., Garcia Fernandez, J.M., Targeted delivery of pharmacological chaperones for gaucher disease to macrophages by a mannosylated cyclodextrin carrier. Org. Biomol. Chem. 12 (2014), 2289–2301.
29. [29] Grabowski, G.A., Delivery of lysosomal enzymes for therapeutic use: glucocerebrosidase as an example. Expert Opin. Drug Deliv. 3 (2006), 771–782.
30. [30] Davignon, J.-L., Hayder, M., Baron, M., Boyer, J.-F., Constantin, A., Apparailly, F., Poupot, R., Cantagrel, A., Targeting monocytes/macrophages in the treatment of rheumatoid arthritis. Rheumatology (Oxford), 2012.
31. [31] Rollett, A., Reiter, T., Ohradanova-Repic, A., Machacek, C., Cavaco-Paulo, A., Stockinger, H., Guebitz, G.M., HSA nanocapsules functionalized with monoclonal antibodies for targeted drug delivery. Int. J. Pharm. 458 (2013), 1–8.
32. [32] Bilthariya, U., Jain, N., Rajoriya, V., Jain, A.K., Folate-conjugated albumin nanoparticles for rheumatoid arthritis-targeted delivery of etoricoxib. Drug Dev. Ind. Pharm. 41 (2015), 95–104.
33. [33] Duan, J., Dong, J., Zhang, T., Su, Z., Ding, J., Zhang, Y., Mao, X., Polyethyleneimine-functionalized iron oxide nanoparticles for systemic siRNA delivery in experimental arthritis. Nanomedicine (Lond.) 9 (2014), 789–801.
34. [34] Amoozgar, Z., Goldberg, M.S., Targeting myeloid cells using nanoparticles to improve cancer immunotherapy. Adv. Drug Deliv. Rev. 91 (2015), 38–51.
35. [35] Zhang, W., Zhu, X.-D., Sun, H.-C., Xiong, Y.-Q., Zhuang, P.-Y., Xu, H.-X., Kong, L.-Q., Wang, L., Wu, W.-Z., Tang, Z.-Y., Depletion of tumor-associated macrophages enhances the effect of sorafenib in metastatic liver cancer models by antimetastatic and antiangiogenic effects. Clin. Cancer Res. 16 (2010), 3420–3430.
36. [36] Allavena, P., Germano, G., Belgiovine, C., D'Incalci, M., Mantovani, A., Trabectedin: a drug from the sea that strikes tumor-associated macrophages. Oncoimmunology, 2, 2013, 16.
37. [37] Germano, G., Frapolli, R., Belgiovine, C., Anselmo, A., Pesce, S., Liguori, M., Erba, E., Uboldi, S., Zucchetti, M., Pasqualini, F., Nebuloni, M., van Rooijen, N., Mortarini, R., Beltrame, L., Marchini, S., Fuso Nerini, I., Sanfilippo, R., Casali, P.G., Pilotti, S., Galmarini, C.M., Anichini, A., Mantovani, A., D'Incalci, M., Allavena, P., Role of macrophage targeting in the antitumor activity of trabectedin. Cancer Cell 23 (2013), 249–262.
38. [38] Zhan, X., Jia, L., Niu, Y., Qi, H., Chen, X., Zhang, Q., Zhang, J., Wang, Y., Dong, L., Wang, C., Targeted depletion of tumour-associated macrophages by an alendronate-glucomannan conjugate for cancer immunotherapy. Biomaterials 35 (2014), 10046–10057.
39. [39] Rogers, T.L., Holen, I., Tumour macrophages as potential targets of bisphosphonates. J. Transl. Med. 9 (2011), 1479–5876.
40. [40] Zhu, Y., Knolhoff, B.L., Meyer, M.A., Nywening, T.M., West, B.L., Luo, J., Wang-Gillam, A., Goedegebuure, S.P., Linehan, D.C., DeNardo, D.G., CSF1/CSF1R blockade reprograms tumor-infiltrating macrophages and improves response to T-cell checkpoint immunotherapy in pancreatic cancer models. Cancer Res. 74 (2014), 5057–5069.
41. [41] Xu, M., Liu, M., Du, X., Li, S., Li, H., Li, X., Li, Y., Wang, Y., Qin, Z., Fu, Y.X., Wang, S., Intratumoral delivery of IL-21 overcomes anti-Her2/Neu resistance through shifting tumor-associated macrophages from M2 to M1 phenotype. J. Immunol. 194 (2015), 4997–5006.
42. [42] D'Incalci, M., Galmarini, C.M., A review of trabectedin (ET-743): a unique mechanism of action. Mol. Cancer Ther. 9 (2010), 2157–2163.
43. [43] Kodumudi, K.N., Woan, K., Gilvary, D.L., Sahakian, E., Wei, S., Djeu, J.Y., A novel chemoimmunomodulating property of docetaxel: suppression of myeloid-derived suppressor cells in tumor bearers. Clin. Cancer Res. 16 (2010), 4583–4594.
44. [44] Coscia, M., Quaglino, E., Iezzi, M., Curcio, C., Pantaleoni, F., Riganti, C., Holen, I., Monkkonen, H., Boccadoro, M., Forni, G., Musiani, P., Bosia, A., Cavallo, F., Massaia, M., Zoledronic acid repolarizes tumour-associated macrophages and inhibits mammary carcinogenesis by targeting the mevalonate pathway. J. Cell. Mol. Med. 14 (2010), 2803–2815.
45. [45] 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.
46. [46] Huang, W.C., Chiang, W.H., Cheng, Y.H., Lin, W.C., Yu, C.F., Yen, C.Y., Yeh, C.K., Chern, C.S., Chiang, C.S., Chiu, H.C., Tumortropic monocyte-mediated delivery of echogenic polymer bubbles and therapeutic vesicles for chemotherapy of tumor hypoxia. Biomaterials 71 (2015), 71–83.
47. [47] Anselmo, A.C., Mitragotri, S., Cell-mediated delivery of nanoparticles: taking advantage of circulatory cells to target nanoparticles. J. Control. Release 190 (2014), 531–541.
48. [48] Batrakova, E.V., Gendelman, H.E., Kabanov, A.V., Cell-mediated drug delivery. Expert Opin. Drug Deliv. 8 (2011), 415–433.
49. [49] Anselmo, A.C., Gilbert, J.B., Kumar, S., Gupta, V., Cohen, R.E., Rubner, M.F., Mitragotri, S., Monocyte-mediated delivery of polymeric backpacks to inflamed tissues: a generalized strategy to deliver drugs to treat inflammation. J. Control. Release 199 (2015), 29–36.
50. [50] Brynskikh, A.M., Zhao, Y., Mosley, R.L., Li, S., Boska, M.D., Klyachko, N.L., Kabanov, A.V., Gendelman, H.E., Batrakova, E.V., Macrophage delivery of therapeutic nanozymes in a murine model of Parkinson's disease. Nanomedicine (Lond.) 5 (2010), 379–396.
51. [51] Madsen, S.J., Baek, S.K., Makkouk, A.R., Krasieva, T., Hirschberg, H., Macrophages as cell-based delivery systems for nanoshells in photothermal therapy. Ann. Biomed. Eng. 40 (2012), 507–515.
52. [52] Madsen, S.J., Christie, C., Hong, S.J., Trinidad, A., Peng, Q., Uzal, F.A., Hirschberg, H., Nanoparticle-loaded macrophage-mediated photothermal therapy: potential for glioma treatment. Lasers Med. Sci. 30 (2015), 1357–1365.
53. [53] 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.
54. [54] Imbuluzqueta, E., Lemaire, S., Gamazo, C., Elizondo, E., Ventosa, N., Veciana, J., Van Bambeke, F., Blanco-Prieto, M.J., Cellular pharmacokinetics and intracellular activity against Listeria monocytogenes and Staphylococcus aureus of chemically modified and nanoencapsulated gentamicin. J. Antimicrob. Chemother. 67 (2012), 2158–2164.
55. [55] Imbuluzqueta, E., Gamazo, C., Lana, H., Campanero, M.Á., Salas, D., Gil, A.G., Elizondo, E., Ventosa, N., Veciana, J., Blanco-Prieto, M.J., Hydrophobic gentamicin-loaded nanoparticles are effective against Brucella melitensis infection in mice. Antimicrob. Agents Chemother. 57 (2013), 3326–3333.
56. [56] de Faria, T.J., Roman, M., de Souza, N.M., De Vecchi, R., de Assis, J.V., dos Santos, A.L.G., Bechtold, I.H., Winter, N., Soares, M.J., Silva, L.P., De Almeida, M.V., Báfica, A., An isoniazid analogue promotes Mycobacterium tuberculosis-nanoparticle interactions and enhances bacterial killing by macrophages. Antimicrob. Agents Chemother. 56 (2012), 2259–2267.
57. [57] Nahar, M., Jain, N., Preparation, characterization and evaluation of targeting potential of amphotericin B-loaded engineered PLGA nanoparticles. Pharm. Res. 26 (2009), 2588–2598.
58. [58] Zaki, N.M., Hafez, M.M., Enhanced antibacterial effect of ceftriaxone sodium-loaded chitosan nanoparticles against intracellular Salmonella typhimurium. AAPS PharmSciTech 13 (2012), 411–421.
59. [59] Gnanadhas, D.P., Ben Thomas, M., Elango, M., Raichur, A.M., Chakravortty, D., Chitosan-dextran sulphate nanocapsule drug delivery system as an effective therapeutic against intraphagosomal pathogen Salmonella. J. Antimicrob. Chemother. 68 (2013), 2576–2586.
60. [60] Ranjan, A., Pothayee, N., Seleem, M., Jain, N., Sriranganathan, N., Riffle, J.S., Kasimanickam, R., Drug delivery using novel nanoplexes against a Salmonella mouse infection model. J. Nanoparticle Res. 12 (2010), 905–914.
61. [61] Bosnjakovic, A., Mishra, M.K., Ren, W., Kurtoglu, Y.E., Shi, T., Fan, D., Kannan, R.M., Poly(amidoamine) dendrimer-erythromycin conjugates for drug delivery to macrophages involved in periprosthetic inflammation. Nanomedicine 7 (2011), 284–294.
62. [62] Jain, K., Verma, A.K., Mishra, P.R., Jain, N.K., Surface-engineered dendrimeric nanoconjugates for macrophage-targeted delivery of amphotericin B: formulation development and in vitro and in vivo evaluation. Antimicrob. Agents Chemother. 59 (2015), 2479–2487.
63. [63] Fierer, J., Hatlen, L., Lin, J.P., Estrella, D., Mihalko, P., Yau-Young, A., Successful treatment using gentamicin liposomes of Salmonella dublin infections in mice. Antimicrob. Agents Chemother. 34 (1990), 343–348.
64. [64] Vyas, S.P., Kannan, M.E., Jain, S., Mishra, V., Singh, P., Design of liposomal aerosols for improved delivery of rifampicin to alveolar macrophages. Int. J. Pharm. 269 (2004), 37–49.
65. [65] Chono, S., Tanino, T., Seki, T., Morimoto, K., Efficient drug targeting to rat alveolar macrophages by pulmonary administration of ciprofloxacin incorporated into mannosylated liposomes for treatment of respiratory intracellular parasitic infections. J. Control. Release 127 (2008), 50–58.
66. [66] Chono, S., Tanino, T., Seki, T., Morimoto, K., Efficient drug delivery to alveolar macrophages and lung epithelial lining fluid following pulmonary administration of liposomal ciprofloxacin in rats with pneumonia and estimation of its antibacterial effects. Drug Dev. Ind. Pharm. 34 (2008), 1090–1096.
67. [67] Pumerantz, A., Muppidi, K., Agnihotri, S., Guerra, C., Venketaraman, V., Wang, J., Betageri, G., Preparation of liposomal vancomycin and intracellular killing of meticillin-resistant Staphylococcus aureus (mrsa). Int. J. Antimicrob. Agents 37 (2011), 140–144.
68. [68] Schmitt, F., Lagopoulos, L., Käuper, P., Rossi, N., Busso, N., Barge, J., Wagnières, G., Laue, C., Wandrey, C., Juillerat-Jeanneret, L., Chitosan-based nanogels for selective delivery of photosensitizers to macrophages and improved retention in and therapy of articular joints. J. Control. Release 144 (2010), 242–250.
69. [69] Maya, S., Indulekha, S., Sukhithasri, V., Smitha, K.T., Nair, S.V., Jayakumar, R., Biswas, R., Efficacy of tetracycline encapsulated o-carboxymethyl chitosan nanoparticles against intracellular infections of Staphylococcus aureus. Int. J. Biol. Macromol. 51 (2012), 392–399.
70. [70] Fernandes Stefanello, T., Szarpak-Jankowska, A., Appaix, F., Louage, B., Hamard, L., De Geest, B.G., van der Sanden, B., Nakamura, C.V., Auzély-Velty, R., Thermoresponsive hyaluronic acid nanogels as hydrophobic drug carrier to macrophages. Acta Biomater. 10 (2014), 4750–4758.
71. [71] Muraoka, D., Harada, N., Hayashi, T., Tahara, Y., Momose, F., Sawada, S.-i., Mukai, S.-a., Akiyoshi, K., Shiku, H., Nanogel-based immunologically stealth vaccine targets macrophages in the medulla of lymph node and induces potent antitumor immunity. ACS Nano 8 (2014), 9209–9218.
72. [72] Kiruthika, V., Maya, S., Suresh, M.K., Anil Kumar, V., Jayakumar, R., Biswas, R., Comparative efficacy of chloramphenicol loaded chondroitin sulfate and dextran sulfate nanoparticles to treat intracellular Salmonella infections. Colloids Surf. B Biointerfaces 127 (2015), 33–40.
73. [73] Drulis-Kawa, Z., Dorotkiewicz-Jach, A., Liposomes as delivery systems for antibiotics. Int. J. Pharm. 387 (2010), 187–198.
74. [74] Kelly, C., Jefferies, C., Cryan, S.-A., Targeted liposomal drug delivery to monocytes and macrophages. J. Drug Deliv., 2011, 2011, 11.
75. [75] Rao, J.P., Geckeler, K.E., Polymer nanoparticles: preparation techniques and size-control parameters. Prog. Polym. Sci. 36 (2011), 887–913.
76. [76] Makadia, H.K., Siegel, S.J., Poly lactic-co-glycolic acid (PLGA) as biodegradable controlled drug delivery carrier. Polymers 3 (2011), 1377–1397.
77. [77] Bernkop-Schnürch, A., Dünnhaupt, S., Chitosan-based drug delivery systems. Eur. J. Pharm. Biopharm. 81 (2012), 463–469.
78. [78] Kesharwani, P., Jain, K., Jain, N.K., Dendrimer as nanocarrier for drug delivery. Prog. Polym. Sci. 39 (2014), 268–307.
79. [79] Sivaram, A.J., Rajitha, P., Maya, S., Jayakumar, R., Sabitha, M., Nanogels for delivery, imaging and therapy. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 7 (2015), 509–533.
80. [80] Semiramoth, N., Di Meo, C., Zouhiri, F., Said-Hassane, F., Valetti, S., Gorges, R., Nicolas, V., Poupaert, J.H., Chollet-Martin, S., Desmaele, D., Gref, R., Couvreur, P., Self-assembled squalenoylated penicillin bioconjugates: an original approach for the treatment of intracellular infections. ACS Nano 6 (2012), 3820–3831.
81. [81] Gupta, P.K., Jaiswal, A.K., Kumar, V., Verma, A., Dwivedi, P., Dube, A., Mishra, P.R., Covalent functionalized self-assembled lipo-polymerosome bearing amphotericin B for better management of leishmaniasis and its toxicity evaluation. Mol. Pharm. 11 (2014), 951–963.
82. [82] Gupta, P.K., Asthana, S., Jaiswal, A.K., Kumar, V., Verma, A.K., Shukla, P., Dwivedi, P., Dube, A., Mishra, P.R., Exploitation of lectinized lipo-polymerosome encapsulated amphotericin b to target macrophages for effective chemotherapy of visceral leishmaniasis. Bioconjug. Chem. 25 (2014), 1091–1102.
83. [83] Maretti, E., Rossi, T., Bondi, M., Croce, M.A., Hanuskova, M., Leo, E., Sacchetti, F., Iannuccelli, V., Inhaled solid lipid microparticles to target alveolar macrophages for tuberculosis. Int. J. Pharm. 462 (2014), 74–82.
84. [84] Niu, M., Naguib, Y.W., Aldayel, A.M., Shi, Y.C., Hursting, S.D., Hersh, M.A., Cui, Z., Biodistribution and in vivo activities of tumor-associated macrophage-targeting nanoparticles incorporated with doxorubicin. Mol. Pharm. 11 (2014), 4425–4436.
85. [85] Smith, B.R., Ghosn, E.E., Rallapalli, H., Prescher, J.A., Larson, T., Herzenberg, L.A., Gambhir, S.S., Selective uptake of single-walled carbon nanotubes by circulating monocytes for enhanced tumour delivery. Nat. Nanotechnol. 9 (2014), 481–487.
86. [86] Xie, S., Tao, Y., Pan, Y., Qu, W., Cheng, G., Huang, L., Chen, D., Wang, X., Liu, Z., Yuan, Z., Biodegradable nanoparticles for intracellular delivery of antimicrobial agents. J. Control. Release 187 (2014), 101–117.
87. [87] Ahsan, F., Rivas, I.P., Khan, M.A., Torres Suárez, A.I., Targeting to macrophages: role of physicochemical properties of particulate carriers—liposomes and microspheres—on the phagocytosis by macrophages. J. Control. Release 79 (2002), 29–40.
88. [88] Epstein-Barash, H., Gutman, D., Markovsky, E., Mishan-Eisenberg, G., Koroukhov, N., Szebeni, J., Golomb, G., Physicochemical parameters affecting liposomal bisphosphonates bioactivity for restenosis therapy: internalization, cell inhibition, activation of cytokines and complement, and mechanism of cell death. J. Control. Release 146 (2010), 182–195.
89. [89] Schwendener, R.A., Lagocki, P.A., Rahman, Y.E., The effects of charge and size on the interaction of unilamellar liposomes with macrophages. Biochim. Biophys. Acta 772 (1984), 93–101.
90. [90] Yue, H., Wei, W., Yue, Z., Lv, P., Wang, L., Ma, G., Su, Z., Particle size affects the cellular response in macrophages. Eur. J. Pharm. Sci. 41 (2010), 650–657.
91. [91] Chono, S., Tanino, T., Seki, T., Morimoto, K., Uptake characteristics of liposomes by rat alveolar macrophages: influence of particle size and surface mannose modification. J. Pharm. Pharmacol. 59 (2007), 75–80.
92. [92] Ohashi, K., Kabasawa, T., Ozeki, T., Okada, H., One-step preparation of rifampicin/poly(lactic-co-glycolic acid) nanoparticle-containing mannitol microspheres using a four-fluid nozzle spray drier for inhalation therapy of tuberculosis. J. Control. Release 135 (2009), 19–24.
93. [93] Tabata, Y., Ikada, Y., Phagocytosis of Polymer Microspheres by Macrophages, in: New Polymer Materials. 1990, Springer, Berlin Heidelberg, 107–141.
94. [94] 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.
95. [95] Champion, J.A., Mitragotri, S., Role of target geometry in phagocytosis. Proc. Natl. Acad. Sci. U. S. A. 103 (2006), 4930–4934.
96. [96] Sharma, G., Valenta, D.T., Altman, Y., Harvey, S., Xie, H., Mitragotri, S., Smith, J.W., Polymer particle shape independently influences binding and internalization by macrophages. J. Control. Release 147 (2010), 408–412.
97. [97] Martinez-Pomares, L., The mannose receptor. J. Leukoc. Biol. 92 (2012), 1177–1186.
98. [98] Guilliams, M., Bruhns, P., Saeys, Y., Hammad, H., Lambrecht, B.N., The function of Fcγ receptors in dendritic cells and macrophages. Nat. Rev. Immunol. 14 (2014), 94–108.
99. [99] 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 (2008), 120–129.
100. [100] Brown, E.J., Goodwin, J.L., Fibronectin receptors of phagocytes. Characterization of the Arg-Gly-Asp binding proteins of human monocytes and polymorphonuclear leukocytes. J. Exp. Med. 167 (1988), 777–793.
101. [101] Nahar, M., Dubey, V., Mishra, D., Mishra, P.K., Dube, A., Jain, N.K., In vitro evaluation of surface functionalized gelatin nanoparticles for macrophage targeting in the therapy of visceral leishmaniasis. J. Drug Target. 18 (2010), 93–105.
102. [102] Saraogi, G.K., Sharma, B., Joshi, B., Gupta, P., Gupta, U.D., Jain, N.K., Agrawal, G.P., Mannosylated gelatin nanoparticles bearing isoniazid for effective management of tuberculosis. J. Drug Target. 19 (2011), 219–227.
103. [103] Nimje, N., Agarwal, A., Saraogi, G.K., Lariya, N., Rai, G., Agrawal, H., Agrawal, G.P., Mannosylated nanoparticulate carriers of rifabutin for alveolar targeting. J. Drug Target. 17 (2009), 777–787.
104. [104] Wijagkanalan, W., Kawakami, S., Higuchi, Y., Yamashita, F., Hashida, M., Intratracheally instilled mannosylated cationic liposome/NFκB decoy complexes for effective prevention of LPS-induced lung inflammation. J. Control. Release 149 (2011), 42–50.
105. [105] Rathore, A., Jain, A., Gulbake, A., Shilpi, S., Khare, P., Jain, A., Jain, S.K., Mannosylated liposomes bearing amphotericin B for effective management of visceral leishmaniasis. J. Liposome Res. 21 (2011), 333–340.
106. [106] Wijagkanalan, W., Kawakami, S., Takenaga, M., Igarashi, R., Yamashita, F., Hashida, M., Efficient targeting to alveolar macrophages by intratracheal administration of mannosylated liposomes in rats. J. Control. Release 125 (2008), 121–130.
107. [107] Van Der Heijden, J.W., Oerlemans, R., Dijkmans, B.A.C., Qi, H., Laken, C.J.V.D., Lems, W.F., Jackman, A.L., Kraan, M.C., Tak, P.P., Ratnam, M., Jansen, G., Folate receptor β as a potential delivery route for novel folate antagonists to macrophages in the synovial tissue of rheumatoid arthritis patients. Arthritis Rheum. 60 (2009), 12–21.
108. [108] Paulos, C.M., Turk, M.J., Breur, G.J., Low, P.S., Folate receptor-mediated targeting of therapeutic and imaging agents to activated macrophages in rheumatoid arthritis. Adv. Drug Deliv. Rev. 56 (2004), 1205–1217.
109. [109] Nagai, T., Tanaka, M., Hasui, K., Shirahama, H., Kitajima, S., Yonezawa, S., Xu, B., Matsuyama, T., Effect of an immunotoxin to folate receptor beta on bleomycin-induced experimental pulmonary fibrosis. Clin. Exp. Immunol. 161 (2010), 348–356.
110. [110] Gabizon, A., Horowitz, A.T., Goren, D., Tzemach, D., Mandelbaum-Shavit, F., Qazen, M.M., Zalipsky, S., Targeting folate receptor with folate linked to extremities of poly(ethylene glycol)-grafted liposomes: in vitro studies. Bioconjug. Chem. 10 (1999), 289–298.
111. [111] Rollett, A., Reiter, T., Nogueira, P., Cardinale, M., Loureiro, A., Gomes, A., Cavaco-Paulo, A., Moreira, A., Carmo, A.M., Guebitz, G.M., Folic acid-functionalized human serum albumin nanocapsules for targeted drug delivery to chronically activated macrophages. Int. J. Pharm. 427 (2012), 460–466.
112. [112] Puig-Kroger, A., Sierra-Filardi, E., Dominguez-Soto, A., Samaniego, R., Corcuera, M.T., Gomez-Aguado, F., Ratnam, M., Sanchez-Mateos, P., Corbi, A.L., Folate receptor beta is expressed by tumor-associated macrophages and constitutes a marker for M2 anti-inflammatory/regulatory macrophages. Cancer Res. 69 (2009), 9395–9403.
113. [113] Turk, M.J., Waters, D.J., Low, P.S., Folate-conjugated liposomes preferentially target macrophages associated with ovarian carcinoma. Cancer Lett. 213 (2004), 165–172.
114. [114] Gupta, C.M., Haq, W., Tuftsin-bearing liposomes as antibiotic carriers in treatment of macrophage infections. Methods Enzymol. 391 (2005), 291–304.
115. [115] Jain, S., Amiji, M., Tuftsin-modified alginate nanoparticles as a noncondensing macrophage-targeted DNA delivery system. Biomacromolecules 13 (2012), 1074–1085.
116. [116] Bar-Shavit, Z., Stabinsky, Y., Fridkin, M., Goldman, R., Tuftsin-macrophage interaction: specific binding and augmentation of phagocytosis. J. Cell. Physiol. 100 (1979), 55–62.
117. [117] Cieslewicz, M., Tang, J., Yu, J.L., Cao, H., Zavaljevski, M., Motoyama, K., Lieber, A., Raines, E.W., Pun, S.H., Targeted delivery of proapoptotic peptides to tumor-associated macrophages improves survival. Proc. Natl. Acad. Sci. U. S. A. 110 (2013), 15919–15924.
118. + T cells that correlates with innate resistance to infection. J. Immunol. 177 (2006), 7146–7154.
119. [119] Steele-Mortimer, O., The Salmonella-containing vacuole — moving with the times. Curr. Opin. Microbiol. 11 (2008), 38–45.
120. [120] Celli, J., Gorvel, J.P., Organelle robbery: Brucella interactions with the endoplasmic reticulum. Curr. Opin. Microbiol. 7 (2004), 93–97.
121. [121] Dominska, M., Dykxhoorn, D.M., Breaking down the barriers: siRNA delivery and endosome escape. J. Cell Sci. 123 (2010), 1183–1189.
122. [122] Claus, V., Jahraus, A., Tjelle, T., Berg, T., Kirschke, H., Faulstich, H., Griffiths, G., Lysosomal enzyme trafficking between phagosomes, endosomes, and lysosomes in J774 macrophages. Enrichment of cathepsin H in early endosomes. J. Biol. Chem. 273 (1998), 9842–9851.
123. [123] Evans, C.J., Aguilera, R.J., DNase II: genes, enzymes and function. Gene 322 (2003), 1–15.
124. [124] Meng, F., Cheng, R., Deng, C., Zhong, Z., Intracellular drug release nanosystems. Mater. Today 15 (2012), 436–442.
125. [125] Schaible, U.E., Sturgill-Koszycki, S., Schlesinger, P.H., Russell, D.G., Cytokine activation leads to acidification and increases maturation of Mycobacterium avium-containing phagosomes in murine macrophages. J. Immunol. 160 (1998), 1290–1296.
126. [126] Vandal, O.H., Nathan, C.F., Ehrt, S., Acid resistance in Mycobacterium tuberculosis. J. Bacteriol. 191 (2009), 4714–4721.
127. [127] Prina, E., Antoine, J.C., Wiederanders, B., Kirschke, H., Localization and activity of various lysosomal proteases in Leishmania amazonensis-infected macrophages. Infect. Immun. 58 (1990), 1730–1737.
128. [128] Varkouhi, A.K., Scholte, M., Storm, G., Haisma, H.J., Endosomal escape pathways for delivery of biologicals. J. Control. Release 151 (2011), 220–228.
129. [129] Ma, D., Enhancing endosomal escape for nanoparticle mediated siRNA delivery. Nanoscale 6 (2014), 6415–6425.
130. [130] Lutwyche, P., Cordeiro, C., Wiseman, D.J., St-Louis, M., Uh, M., Hope, M.J., Webb, M.S., Finlay, B.B., Intracellular delivery and antibacterial activity of gentamicin encapsulated in pH-sensitive liposomes. Antimicrob. Agents Chemother. 42 (1998), 2511–2520.
131. [131] Ortega, R.A., Barham, W.J., Kumar, B., Tikhomirov, O., McFadden, I.D., Yull, F.E., Giorgio, T.D., Biocompatible mannosylated endosomal-escape nanoparticles enhance selective delivery of short nucleotide sequences to tumor associated macrophages. Nanoscale 7 (2015), 500–510.
132. [132] Xiong, M.-H., Bao, Y., Yang, X.-Z., Wang, Y.-C., Sun, B., Wang, J., Lipase-sensitive polymeric triple-layered nanogel for “on-demand” drug delivery. J. Am. Chem. Soc. 134 (2012), 4355–4362.