Macrophage-based cell therapies: The long and winding road

Journal of Controlled Release

Volumn 240, Issue , 2016, Pages 527-540

  Lee, Simon ^a   Kivimäe, Saul ^b   Dolor, Aaron ^b   Szoka, Francis C ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cell polarization; Cell therapy; Drug delivery; Gene editing; Macrophages

Indexed keywords

ANIMALS; BLOOD VESSELS; CELLS; CYTOLOGY; DISEASE CONTROL; DRUG DELIVERY; GENES; LIPOSOMES; MACROPHAGES; PROTEINS; TUMORS;

BIODISTRIBUTIONS; CANCER CELL GROWTH; CELL BASED THERAPIES; CELL POLARIZATION; CELL THERAPY; THERAPEUTIC BENEFITS; THERAPEUTIC PROTEIN; VESSEL FORMATION;

GENE THERAPY;

DRUG VEHICLE; LIPOSOME;

ARTICLE; CELL SURVIVAL; CELL THERAPY; DRUG DELIVERY SYSTEM; EX VIVO STUDY; GENETIC ENGINEERING; HUMAN; MACROPHAGE; NANOMEDICINE; NONHUMAN; PHENOTYPE; POLARIZATION; PRIORITY JOURNAL; ANIMAL; CELL ENGINEERING; CELL POLARITY; CELL TRANSPLANTATION; CLINICAL TRIAL (TOPIC); CYTOLOGY; DISEASE MODEL; IMMUNOLOGY; NEOPLASM; PROCEDURES; TRANSPLANTATION;

ANIMALS; CELL ENGINEERING; CELL POLARITY; CELL TRANSPLANTATION; CLINICAL TRIALS AS TOPIC; DISEASE MODELS, ANIMAL; HUMANS; MACROPHAGES; NEOPLASMS;

EID: 84978906133     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2016.07.018     Document Type: Article

References (154)

1. [1] Learoyd, P., A Short History of Blood Transfusion, in. 2006, National Blood Service, Leeds Blood Centre.
2. [2] Lacerna, L.V. Jr., Stevenson, G.W., Stevenson, H.C., Adoptive cancer immunotherapy utilizing lymphokine activated killer cells and gamma interferon activated killer monocytes. Pharmacol. Ther. 38 (1988), 453–465.
3. [3] Gill, S., June, C.H., Going viral: chimeric antigen receptor T-cell therapy for hematological malignancies. Immunol. Rev. 263 (2015), 68–89.
4. [4] Fidler, I.J., Inhibition of pulmonary metastasis by intravenous injection of specifically activated macrophages. Cancer Res. 34 (1974), 1074–1078.
5. [5] Alexander, P., The role of macrophages in tumour immunity. J Clin Pathol Suppl (R Coll Pathol) 7 (1974), 77–82.
6. [6] Gordon, S., The macrophage: past, present and future. Eur. J. Immunol. 37:Suppl. 1 (2007), S9–17.
7. [7] Wynn, T.A., Chawla, A., Pollard, J.W., Macrophage biology in development, homeostasis and disease. Nature 496 (2013), 445–455.
8. [8] Franken, L., Schiwon, M., Kurts, C., Macrophages: sentinels and regulators of the immune system. Cell. Microbiol. 18:4 (2016), 475–487.
9. [9] Martin, C.J., Peters, K.N., Behar, S.M., Macrophages clean up: efferocytosis and microbial control. Curr. Opin. Microbiol. 17 (2014), 17–23.
10. [10] Soroosh, P., Doherty, T.A., Duan, W., Mehta, A.K., Choi, H., Adams, Y.F., Mikulski, Z., Khorram, N., Rosenthal, P., Broide, D.H., Croft, M., Lung-resident tissue macrophages generate Foxp3 + regulatory T cells and promote airway tolerance. J. Exp. Med. 210 (2013), 775–788.
11. [11] Mantovani, A., Sica, A., Allavena, P., Garlanda, C., Locati, M., Tumor-associated macrophages and the related myeloid-derived suppressor cells as a paradigm of the diversity of macrophage activation. Hum. Immunol. 70 (2009), 325–330.
12. [12] van Furth, R., Cohn, Z.A., The origin and kinetics of mononuclear phagocytes. J. Exp. Med. 128 (1968), 415–435.
13. [13] Varol, C., Mildner, A., Jung, S., Macrophages: development and tissue specialization. Annu. Rev. Immunol. 33 (2015), 643–675.
14. [14] Ginhoux, F., Greter, M., Leboeuf, M., Nandi, S., See, P., Gokhan, S., Mehler, M.F., Conway, S.J., Ng, L.G., Stanley, E.R., Samokhvalov, I.M., Merad, M., Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science 330 (2010), 841–845.
15. [15] Guilliams, M., De Kleer, I., Henri, S., Post, S., Vanhoutte, L., De Prijck, S., Deswarte, K., Malissen, B., Hammad, H., Lambrecht, B.N., Alveolar macrophages develop from fetal monocytes that differentiate into long-lived cells in the first week of life via GM-CSF. J. Exp. Med. 210 (2013), 1977–1992.
16. [16] Hoeffel, G., Ginhoux, F., Ontogeny of tissue-resident macrophages. Front. Immunol., 6, 2015, 486.
17. [17] Kawakami, T., Lichtnekert, J., Thompson, L.J., Karna, P., Bouabe, H., Hohl, T.M., Heinecke, J.W., Ziegler, S.F., Nelson, P.J., Duffield, J.S., Resident renal mononuclear phagocytes comprise five discrete populations with distinct phenotypes and functions. J. Immunol. 191 (2013), 3358–3372.
18. [18] Sheng, J., Ruedl, C., Karjalainen, K., Most tissue-resident macrophages except microglia are derived from fetal hematopoietic stem cells. Immunity 43 (2015), 382–393.
19. [19] Yona, S., Kim, K.W., Wolf, Y., Mildner, A., Varol, D., Breker, M., Strauss-Ayali, D., Viukov, S., Guilliams, M., Misharin, A., Hume, D.A., Perlman, H., Malissen, B., Zelzer, E., Jung, S., Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis. Immunity 38 (2013), 79–91.
20. [20] Soucie, E.L., Weng, Z., Geirsdottir, L., Molawi, K., Maurizio, J., Fenouil, R., Mossadegh-Keller, N., Gimenez, G., VanHille, L., Beniazza, M., Favret, J., Berruyer, C., Perrin, P., Hacohen, N., Andrau, J.C., Ferrier, P., Dubreuil, P., Sidow, A., Sieweke, M.H., Lineage-specific enhancers activate self-renewal genes in macrophages and embryonic stem cells. Science, 351, 2016, aad5510.
21. [21] Jenkins, S.J., Ruckerl, D., Cook, P.C., Jones, L.H., Finkelman, F.D., van Rooijen, N., MacDonald, A.S., Allen, J.E., Local macrophage proliferation, rather than recruitment from the blood, is a signature of TH2 inflammation. Science 332 (2011), 1284–1288.
22. [22] Bain, C.C., Bravo-Blas, A., Scott, C.L., Gomez Perdiguero, E., Geissmann, F., Henri, S., Malissen, B., Osborne, L.C., Artis, D., Mowat, A.M., Constant replenishment from circulating monocytes maintains the macrophage pool in the intestine of adult mice. Nat. Immunol. 15 (2014), 929–937.
23. [23] Molawi, K., Wolf, Y., Kandalla, P.K., Favret, J., Hagemeyer, N., Frenzel, K., Pinto, A.R., Klapproth, K., Henri, S., Malissen, B., Rodewald, H.R., Rosenthal, N.A., Bajenoff, M., Prinz, M., Jung, S., Sieweke, M.H., Progressive replacement of embryo-derived cardiac macrophages with age. J. Exp. Med. 211 (2014), 2151–2158.
24. [24] Tamoutounour, S., Guilliams, M., Montanana Sanchis, F., Liu, H., Terhorst, D., Malosse, C., Pollet, E., Ardouin, L., Luche, H., Sanchez, C., Dalod, M., Malissen, B., Henri, S., Origins and functional specialization of macrophages and of conventional and monocyte-derived dendritic cells in mouse skin. Immunity 39 (2013), 925–938.
25. [25] 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.
26. [26] Epelman, S., Lavine, K.J., Beaudin, A.E., Sojka, D.K., Carrero, J.A., Calderon, B., Brija, T., Gautier, E.L., Ivanov, S., Satpathy, A.T., Schilling, J.D., Schwendener, R., Sergin, I., Razani, B., Forsberg, E.C., Yokoyama, W.M., Unanue, E.R., Colonna, M., Randolph, G.J., Mann, D.L., Embryonic and adult-derived resident cardiac macrophages are maintained through distinct mechanisms at steady state and during inflammation. Immunity 40 (2014), 91–104.
27. [27] Happle, C., Lachmann, N., Skuljec, J., Wetzke, M., Ackermann, M., Brennig, S., Mucci, A., Jirmo, A.C., Groos, S., Mirenska, A., Hennig, C., Rodt, T., Bankstahl, J.P., Schwerk, N., Moritz, T., Hansen, G., Pulmonary transplantation of macrophage progenitors as effective and long-lasting therapy for hereditary pulmonary alveolar proteinosis. Sci. Transl. Med., 6, 2014, 250ra113.
28. [28] Suzuki, T., Arumugam, P., Sakagami, T., Lachmann, N., Chalk, C., Sallese, A., Abe, S., Trapnell, C., Carey, B., Moritz, T., Malik, P., Lutzko, C., Wood, R.E., Trapnell, B.C., Pulmonary macrophage transplantation therapy. Nature 514 (2014), 450–454.
29. [29] Haldar, M., Kohyama, M., So, A.Y., Kc, W., Wu, X., Briseno, C.G., Satpathy, A.T., Kretzer, N.M., Arase, H., Rajasekaran, N.S., Wang, L., Egawa, T., Igarashi, K., Baltimore, D., Murphy, T.L., Murphy, K.M., Heme-mediated SPI-C induction promotes monocyte differentiation into iron-recycling macrophages. Cell 156 (2014), 1223–1234.
30. [30] Okabe, Y., Medzhitov, R., Tissue-specific signals control reversible program of localization and functional polarization of macrophages. Cell 157 (2014), 832–844.
31. [31] Schneider, C., Nobs, S.P., Kurrer, M., Rehrauer, H., Thiele, C., Kopf, M., Induction of the nuclear receptor PPAR-gamma by the cytokine GM-CSF is critical for the differentiation of fetal monocytes into alveolar macrophages. Nat. Immunol. 15 (2014), 1026–1037.
32. [32] Glass, C.K., Genetic and genomic approaches to understanding macrophage identity and function. Arterioscler. Thromb. Vasc. Biol. 35 (2015), 755–762.
33. [33] Lavin, Y., Winter, D., Blecher-Gonen, R., David, E., Keren-Shaul, H., Merad, M., Jung, S., Amit, I., Tissue-resident macrophage enhancer landscapes are shaped by the local microenvironment. Cell 159 (2014), 1312–1326.
34. [34] Martinez, F.O., Gordon, S., The evolution of our understanding of macrophages and translation of findings toward the clinic. Expert. Rev. Clin. Immunol. 11 (2015), 5–13.
35. [35] X. Zhang, R. Goncalves, D.M. Mosser, The isolation and characterization of murine macrophages, Current Protocols in Immunology/edited by John E. Coligan … [et al.], Chapter 14 (2008) Unit 14 11.
36. [36] D.M. Mosser, X. Zhang, Activation of murine macrophages, Current Protocols in Immunology/edited by John E. Coligan … [et al.], Chapter 14 (2008) Unit 14 12.
37. [37] V. Chitu, Y.G. Yeung, W. Yu, S. Nandi, E.R. Stanley, Measurement of macrophage growth and differentiation, Current Protocols in Immunology/edited by John E. Coligan … [et al.], Chapter 14 (2011) Unit 14 11–26.
38. [38] Francke, A., Herold, J., Weinert, S., Strasser, R.H., Braun-Dullaeus, R.C., Generation of mature murine monocytes from heterogeneous bone marrow and description of their properties. J. Histochem. Cytochem. 59 (2011), 813–825.
39. [39] Redecke, V., Wu, R., Zhou, J., Finkelstein, D., Chaturvedi, V., High, A.A., Hacker, H., Hematopoietic progenitor cell lines with myeloid and lymphoid potential. Nat. Methods 10 (2013), 795–803.
40. [40] Wang, G.G., Calvo, K.R., Pasillas, M.P., Sykes, D.B., Hacker, H., Kamps, M.P., Quantitative production of macrophages or neutrophils ex vivo using conditional Hoxb8. Nat. Methods 3 (2006), 287–293.
41. [41] Gautier, E.L., Shay, T., Miller, J., Greter, M., Jakubzick, C., Ivanov, S., Helft, J., Chow, A., Elpek, K.G., Gordonov, S., Mazloom, A.R., Ma'ayan, A., Chua, W.J., Hansen, T.H., Turley, S.J., Merad, M., Randolph, G.J., Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nat. Immunol. 13 (2012), 1118–1128.
42. [42] Mills, C.D., Kincaid, K., Alt, J.M., Heilman, M.J., Hill, A.M., M-1/M-2 macrophages and the Th1/Th2 paradigm. J. Immunol. 164 (2000), 6166–6173.
43. [43] Murray, P.J., Allen, J.E., Biswas, S.K., Fisher, E.A., Gilroy, D.W., Goerdt, S., Gordon, S., Hamilton, J.A., Ivashkiv, L.B., Lawrence, T., Locati, M., Mantovani, A., Martinez, F.O., Mege, J.L., Mosser, D.M., Natoli, G., Saeij, J.P., Schultze, J.L., Shirey, K.A., Sica, A., Suttles, J., Udalova, I., van Ginderachter, J.A., Vogel, S.N., Wynn, T.A., Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity 41 (2014), 14–20.
44. [44] Lawrence, T., Natoli, G., Transcriptional regulation of macrophage polarization: enabling diversity with identity. Nat. Rev. Immunol. 11 (2011), 750–761.
45. [45] Takaoka, A., Yanai, H., Kondo, S., Duncan, G., Negishi, H., Mizutani, T., Kano, S., Honda, K., Ohba, Y., Mak, T.W., Taniguchi, T., Integral role of IRF-5 in the gene induction programme activated by Toll-like receptors. Nature 434 (2005), 243–249.
46. [46] Takeda, K., Tanaka, T., Shi, W., Matsumoto, M., Minami, M., Kashiwamura, S., Nakanishi, K., Yoshida, N., Kishimoto, T., Akira, S., Essential role of Stat6 in IL-4 signalling. Nature 380 (1996), 627–630.
47. [47] Krausgruber, T., Blazek, K., Smallie, T., Alzabin, S., Lockstone, H., Sahgal, N., Hussell, T., Feldmann, M., Udalova, I.A., IRF5 promotes inflammatory macrophage polarization and TH1-TH17 responses. Nat. Immunol. 12 (2011), 231–238.
48. [48] Ohmori, Y., Hamilton, T.A., STAT6 is required for the anti-inflammatory activity of interleukin-4 in mouse peritoneal macrophages. J. Biol. Chem. 273 (1998), 29202–29209.
49. [49] Fidler, I.J., Poste, G., Macrophage-mediated destruction of malignant tumor cells and new strategies for the therapy of metastatic disease. Springer Semin. Immunopathol. 5 (1982), 161–174.
50. [50] Fidler, I.J., Barnes, Z., Fogler, W.E., Kirsh, R., Bugelski, P., Poste, G., Involvement of macrophages in the eradication of established metastases following intravenous injection of liposomes containing macrophage activators. Cancer Res. 42 (1982), 496–501.
51. [51] Andreesen, R., Hennemann, B., Krause, S.W., Adoptive immunotherapy of cancer using monocyte-derived macrophages: rationale, current status, and perspectives. J. Leukoc. Biol. 64 (1998), 419–426.
52. [52] Faradji, A., Bohbot, A., Schmitt-Goguel, M., Siffert, J.C., Dumont, S., Wiesel, M.L., Piemont, Y., Eischen, A., Bergerat, J.P., Bartholeyns, J., et al. Large scale isolation of human blood monocytes by continuous flow centrifugation leukapheresis and counterflow centrifugation elutriation for adoptive cellular immunotherapy in cancer patients. J. Immunol. Methods 174 (1994), 297–309.
53. [53] Andreesen, R., Scheibenbogen, C., Brugger, W., Krause, S., Meerpohl, H.G., Leser, H.G., Engler, H., Lohr, G.W., Adoptive transfer of tumor cytotoxic macrophages generated in vitro from circulating blood monocytes: a new approach to cancer immunotherapy. Cancer Res. 50 (1990), 7450–7456.
54. [54] Tey, S.K., Adoptive T-cell therapy: adverse events and safety switches. Clinical & Translational Immunology, 3, 2014, e17.
55. [55] Stevenson, H.C., Keenan, A.M., Woodhouse, C., Ottow, R.T., Miller, P., Steller, E.P., Foon, K.A., Abrams, P.G., Beman, J., Larson, S.M., et al. Fate of gamma-interferon-activated killer blood monocytes adoptively transferred into the abdominal cavity of patients with peritoneal carcinomatosis. Cancer Res. 47 (1987), 6100–6103.
56. [56] Quillien, V., Moisan, A., Lesimple, T., Leberre, C., Toujas, L., Biodistribution of 111indium-labeled macrophages infused intravenously in patients with renal carcinoma. Cancer Immunol. Immunother. 50 (2001), 477–482.
57. [57] Lee, R.H., Pulin, A.A., Seo, M.J., Kota, D.J., Ylostalo, J., Larson, B.L., Semprun-Prieto, L., Delafontaine, P., Prockop, D.J., Intravenous hMSCs improve myocardial infarction in mice because cells embolized in lung are activated to secrete the anti-inflammatory protein TSG-6. Cell Stem Cell 5 (2009), 54–63.
58. [58] Eggenhofer, E., Benseler, V., Kroemer, A., Popp, F.C., Geissler, E.K., Schlitt, H.J., Baan, C.C., Dahlke, M.H., Hoogduijn, M.J., Mesenchymal stem cells are short-lived and do not migrate beyond the lungs after intravenous infusion. Front. Immunol., 3, 2012, 297.
59. [59] Karp, J.M., Leng Teo, G.S., Mesenchymal stem cell homing: the devil is in the details. Cell Stem Cell 4 (2009), 206–216.
60. [60] Faradji, A., Bohbot, A., Schmitt-Goguel, M., Roeslin, N., Dumont, S., Wiesel, M.L., Lallot, C., Eber, M., Bartholeyns, J., Poindron, P., et al. Phase I trial of intravenous infusion of ex-vivo-activated autologous blood-derived macrophages in patients with non-small-cell lung cancer: toxicity and immunomodulatory effects. Cancer Immunol. Immunother. 33 (1991), 319–326.
61. [61] Hennemann, B., Scheibenbogen, C., Schiimichen, C., Andreesen, R., Intrahepatic adoptive immunotherapy with autologous tumorcytotoxic macrophages in patients with cancer. J. Immunother. 18 (1995), 19–27.
62. [62] Faradji, A., Bohbot, A., Frost, H., Schmitt-Goguel, M., Siffert, J.C., Dufour, P., Eber, M., Lallot, C., Wiesel, M.L., Bergerat, J.P., et al. Phase I study of liposomal MTP-PE-activated autologous monocytes administered intraperitoneally to patients with peritoneal carcinomatosis. J. Clin. Oncol. 9 (1991), 1251–1260.
63. [63] Ritchie, D., Mileshkin, L., Wall, D., Bartholeyns, J., Thompson, M., Coverdale, J., Lau, E., Wong, J., Eu, P., Hicks, R.J., Prince, H.M., In vivo tracking of macrophage activated killer cells to sites of metastatic ovarian carcinoma. Cancer Immunol. Immunother. 56 (2007), 155–163.
64. [64] Burger, M., Thiounn, N., Denzinger, S., Kondas, J., Benoit, G., Chapado, M.S., Jimenz-Cruz, F.J., Kisbenedek, L., Szabo, Z., Zsolt, D., Grimm, M.O., Romics, I., Thuroff, J.W., Kiss, T., Tombal, B., Wirth, M., Munsell, M., Mills, B., Koh, T., Sherman, J., The application of adjuvant autologous antravesical macrophage cell therapy vs. BCG in non-muscle invasive bladder cancer: a multicenter, randomized trial. J. Transl. Med., 8, 2010, 54.
65. [65] Dumont, S., Hartmann, D., Poindron, P., Oberling, F., Faradji, A., Bartholeyns, J., Control of the antitumoral activity of human macrophages produced in large amounts in view of adoptive transfer. European Journal of Cancer and Clinical Oncology 24 (1988), 1691–1698.
66. [66] Okabe, Y., Medzhitov, R., Tissue biology perspective on macrophages. Nat. Immunol. 17 (2015), 9–17.
67. [67] Ruffell, B., Affara, N.I., Coussens, L.M., Differential macrophage programming in the tumor microenvironment. Trends Immunol. 33 (2012), 119–126.
68. [68] Squadrito, M.L., De Palma, M., Macrophage regulation of tumor angiogenesis: implications for cancer therapy. Mol. Asp. Med. 32 (2011), 123–145.
69. [69] Mosser, D.M., Edwards, J.P., Exploring the full spectrum of macrophage activation. Nat. Rev. Immunol. 8 (2008), 958–969.
70. [70] Bartel, R.L., Cramer, C., Ledford, K., Longcore, A., Parrish, C., Stern, T., Watling, S., Zeigler, F., The Aastrom experience. Stem Cell Research & Therapy, 3, 2012, 26.
71. [71] Ledford, K.J., Zeigler, F., Bartel, R.L., Ixmyelocel-T, an expanded multicellular therapy, contains a unique population of M2-like macrophages. Stem Cell Research & Therapy, 4, 2013, 134.
72. [72] Henry, T.D., Traverse, J.H., Hammon, B.L., East, C.A., Bruckner, B., Remmers, A.E., Recker, D., Bull, D.A., Patel, A.N., Safety and efficacy of ixmyelocel-T: an expanded, autologous multi-cellular therapy, in dilated cardiomyopathy. Circ. Res. 115 (2014), 730–737.
73. [73] Powell, R.J., Marston, W.A., Berceli, S.A., Guzman, R., Henry, T.D., Longcore, A.T., Stern, T.P., Watling, S., Bartel, R.L., Cellular therapy with Ixmyelocel-T to treat critical limb ischemia: the randomized, double-blind, placebo-controlled RESTORE-CLI trial. Mol. Ther. 20 (2012), 1280–1286.
74. [74] Eymard, J.C., Lopez, M., Cattan, A., Bouché, O., Adjizian, J.C., Bernard, J., Phase I/II trial of autologous activated macrophages in advanced colorectal cancer. Eur. J. Cancer 32 (1996), 1905–1911.
75. [75] B. Hennemann, G. Beckmann, A. Eichelmann, A. Rehm, R. Andreesen, Phase I trial of adoptive immunotherapy of cancer patients using monocyte-derived macrophages activated with interferon gamma and lipopolysaccharide, Cancer Immunol. Immunother., 45 (1998) 250–256.
76. [76] Lesimple, T., Moisan, A., Guille, F., Leberre, C., Audran, R., Drenou, B., Toujas, L., Treatment of metastatic renal cell carcinoma with activated autologous macrophages and granulocyte–macrophage colony-stimulating factor. J. Immunother. 23 (2000), 675–679.
77. [77] Baron-Bodo, V., Doceur, P., Lefebvre, M.L., Labroquere, K., Defaye, C., Cambouris, C., Prigent, D., Salcedo, M., Boyer, A., Nardin, A., Anti-tumor properties of human-activated macrophages produced in large scale for clinical application. Immunobiology 210 (2005), 267–277.
78. [78] Cao, Q., Wang, Y., Zheng, D., Sun, Y., Wang, C., Wang, X.M., Lee, V.W., Zheng, G., Tan, T.K., Wang, Y.M., Alexander, S.I., Harris, D.C., Failed renoprotection by alternatively activated bone marrow macrophages is due to a proliferation-dependent phenotype switch in vivo. Kidney Int. 85 (2014), 794–806.
79. [79] Wang, Y., Wang, Y.P., Zheng, G., Lee, V.W., Ouyang, L., Chang, D.H., Mahajan, D., Coombs, J., Wang, Y.M., Alexander, S.I., Harris, D.C., Ex vivo programmed macrophages ameliorate experimental chronic inflammatory renal disease. Kidney Int. 72 (2007), 290–299.
80. [80] Sindrilaru, A., Peters, T., Wieschalka, S., Baican, C., Baican, A., Peter, H., Hainzl, A., Schatz, S., Qi, Y., Schlecht, A., Weiss, J.M., Wlaschek, M., Sunderkotter, C., Scharffetter-Kochanek, K., An unrestrained proinflammatory M1 macrophage population induced by iron impairs wound healing in humans and mice. J. Clin. Invest. 121 (2011), 985–997.
81. [81] Leovsky, C., Fabian, C., Naaldijk, Y., Jager, C., Jang, H.J., Bohme, J., Rudolph, L., Stolzing, A., Biodistribution of in vitro-derived microglia applied intranasally and intravenously to mice: effects of aging. Cytotherapy 17 (2015), 1617–1626.
82. [82] Hanke, M.L., Heim, C.E., Angle, A., Sanderson, S.D., Kielian, T., Targeting macrophage activation for the prevention and treatment of Staphylococcus aureus biofilm infections. J. Immunol. 190 (2013), 2159–2168.
83. [83] Ilium, L., Davis, S.S., Wilson, C.G., Thomas, N.W., Frier, M., Hardy, J.G., Blood clearance and organ deposition of intravenously administered colloidal particles. The effects of particle size, nature and shape. Int. J. Pharm. 12 (1982), 135–146.
84. [84] Patel, H.M., Moghimi, S.M., Serum-mediated recognition of liposomes by phagocytic cells of the reticuloendothelial system - the concept of tissue specificity. Adv. Drug Deliv. Rev. 32 (1998), 45–60.
85. [85] Moghimi, S.M., Hunter, A.C., Murray, J.C., Long-circulating and target-specific nanoparticles: theory to practice. Pharmacol. Rev. 53 (2001), 283–318.
86. [86] Petros, R.A., DeSimone, J.M., Strategies in the design of nanoparticles for therapeutic applications. Nat. Rev. Drug Discov. 9 (2010), 615–627.
87. [87] Patel, S.K., Janjic, J.M., Macrophage targeted theranostics as personalized nanomedicine strategies for inflammatory diseases. Theranostics 5 (2015), 150–172.
88. [88] Ahsan, F., Rivas, I.P., Khan, M.A., Torres Suarez, 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.
89. [89] Champion, J.A., Katare, Y.K., Mitragotri, S., Particle shape: a new design parameter for micro- and nanoscale drug delivery carriers. J. Control. Release 121 (2007), 3–9.
90. [90] 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.
91. [91] Lee, W.H., Loo, C.Y., Traini, D., Young, P.M., Nano- and micro-based inhaled drug delivery systems for targeting alveolar macrophages. Expert Opinion on Drug Delivery 12 (2015), 1009–1026.
92. [92] Anselmo, A.C., Mitragotri, S., Impact of particle elasticity on particle-based drug delivery systems. Adv. Drug Deliv. Rev, 2016 pii: S0169-409X(16)30010-2.
93. [93] Otto, D.P., Otto, A., de Villiers, M.M., Differences in physicochemical properties to consider in the design, evaluation and choice between microparticles and nanoparticles for drug delivery. Expert Opinion on Drug Delivery 12 (2015), 763–777.
94. [94] Bareford, L.M., Swaan, P.W., Endocytic mechanisms for targeted drug delivery. Adv. Drug Deliv. Rev. 59 (2007), 748–758.
95. [95] Khalil, I.A., Kogure, K., Akita, H., Harashima, H., Uptake pathways and subsequent intracellular trafficking in nonviral gene delivery. Pharmacol. Rev. 58 (2006), 32–45.
96. [96] Rajendran, L., Knolker, H.J., Simons, K., Subcellular targeting strategies for drug design and delivery. Nat. Rev. Drug Discov. 9 (2010), 29–42.
97. [97] Batrakova, E.V., Gendelman, H.E., Kabanov, A.V., Cell-mediated drug delivery. Expert Opinion on Drug Delivery 8 (2011), 415–433.
98. [98] Haney, M.J., Zhao, Y., Harrison, E.B., Mahajan, V., Ahmed, S., He, Z., Suresh, P., Hingtgen, S.D., Klyachko, N.L., Mosley, R.L., Gendelman, H.E., Kabanov, A.V., Batrakova, E.V., Specific transfection of inflamed brain by macrophages: a new therapeutic strategy for neurodegenerative diseases. PLoS One, 8, 2013, e61852.
99. [99] Zhao, Y., Haney, M.J., Mahajan, V., Reiner, B.C., Dunaevsky, A., Mosley, R.L., Kabanov, A.V., Gendelman, H.E., Batrakova, E.V., Active targeted macrophage-mediated delivery of catalase to affected brain regions in models of Parkinson's disease. Journal of Nanomedicine & Nanotechnology, S4, 2011.
100. [100] 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 (London) 5 (2010), 379–396.
101. [101] Nowacek, A.S., Miller, R.L., McMillan, J., Kanmogne, G., Kanmogne, M., Mosley, R.L., Ma, Z., Graham, S., Chaubal, M., Werling, J., Rabinow, B., Dou, H., Gendelman, H.E., NanoART synthesis, characterization, uptake, release and toxicology for human monocyte-macrophage drug delivery. Nanomedicine (London) 4 (2009), 903–917.
102. [102] Dou, H., Grotepas, C.B., McMillan, J.M., Destache, C.J., Chaubal, M., Werling, J., Kipp, J., Rabinow, B., Gendelman, H.E., Macrophage delivery of nanoformulated antiretroviral drug to the brain in a murine model of neuroAIDS. J. Immunol. 183 (2009), 661–669.
103. [103] Batrakova, E.V., Li, S., Reynolds, A.D., Mosley, R.L., Bronich, T.K., Kabanov, A.V., Gendelman, H.E., A macrophage-nanozyme delivery system for Parkinson's disease. Bioconjug. Chem. 18 (2007), 1498–1506.
104. [104] Dou, H., Destache, C.J., Morehead, J.R., Mosley, R.L., Boska, M.D., Kingsley, J., Gorantla, S., Poluektova, L., Nelson, J.A., Chaubal, M., Werling, J., Kipp, J., Rabinow, B.E., Gendelman, H.E., Development of a macrophage-based nanoparticle platform for antiretroviral drug delivery. Blood 108 (2006), 2827–2835.
105. [105] Bressani, R.F., Nowacek, A.S., Singh, S., Balkundi, S., Rabinow, B., McMillan, J., Gendelman, H.E., Kanmogne, G.D., Pharmacotoxicology of monocyte-macrophage nanoformulated antiretroviral drug uptake and carriage. Nanotoxicology 5 (2011), 592–605.
106. [106] Choi, J., Kim, H.Y., Ju, E.J., Jung, J., Park, J., Chung, H.K., 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.
107. [107] Zhao, Y., Haney, M.J., Gupta, R., Bohnsack, J.P., He, Z., Kabanov, A.V., Batrakova, E.V., GDNF-transfected macrophages produce potent neuroprotective effects in Parkinson's disease mouse model. PLoS One, 9, 2014, e106867.
108. [108] Raposo, G., Stoorvogel, W., Extracellular vesicles: exosomes, microvesicles, and friends. J. Cell Biol. 200 (2013), 373–383.
109. [109] Haney, M.J., Klyachko, N.L., Zhao, Y., Gupta, R., Plotnikova, E.G., He, Z., Patel, T., Piroyan, A., Sokolsky, M., Kabanov, A.V., Batrakova, E.V., Exosomes as drug delivery vehicles for Parkinson's disease therapy. J. Control. Release 207 (2015), 18–30.
110. [110] Yang, T.D., Choi, W., Yoon, T.H., Lee, K.J., Lee, J.S., Joo, J.H., Lee, M.G., Yim, H.S., Choi, K.M., Kim, B., Lee, J.J., Kim, H., Lee, D.Y., Jung, K.Y., Baek, S.K., In vivo photothermal treatment by the peritumoral injection of macrophages loaded with gold nanoshells. Biomedical Optics Express 7 (2016), 185–193.
111. [111] 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.
112. [112] Choi, M.R., Bardhan, R., Stanton-Maxey, K.J., Badve, S., Nakshatri, H., Stantz, K.M., Cao, N., Halas, N.J., Clare, S.E., Delivery of nanoparticles to brain metastases of breast cancer using a cellular Trojan horse. Cancer Nanotechnology 3 (2012), 47–54.
113. [113] Burke, B., Sumner, S., Maitland, N., Lewis, C.E., Macrophages in gene therapy: cellular delivery vehicles and in vivo targets. J. Leukoc. Biol. 72 (2002), 417–428.
114. [114] Jablonska, J., Leschner, S., Westphal, K., Lienenklaus, S., Weiss, S., Neutrophils responsive to endogenous IFN-beta regulate tumor angiogenesis and growth in a mouse tumor model. J. Clin. Invest. 120 (2010), 1151–1164.
115. [115] Thomas, K.E., Galligan, C.L., Newman, R.D., Fish, E.N., Vogel, S.N., Contribution of interferon-beta to the murine macrophage response to the toll-like receptor 4 agonist, lipopolysaccharide. J. Biol. Chem. 281 (2006), 31119–31130.
116. [116] Koba, C., Haruta, M., Matsunaga, Y., Matsumura, K., Haga, E., Sasaki, Y., Ikeda, T., Takamatsu, K., Nishimura, Y., Senju, S., Therapeutic effect of human iPS-cell-derived myeloid cells expressing IFN-beta against peritoneally disseminated cancer in xenograft models. PLoS One, 8, 2013, e67567.
117. [117] Escobar, G., Moi, D., Ranghetti, A., Ozkal-Baydin, P., Squadrito, M.L., Kajaste-Rudnitski, A., Bondanza, A., Gentner, B., De Palma, M., Mazzieri, R., Naldini, L., Genetic engineering of hematopoiesis for targeted IFN-alpha delivery inhibits breast cancer progression. Sci. Transl. Med., 6, 2014, 217ra213.
118. [118] Wang, B.X., Rahbar, R., Fish, E.N., Interferon: current status and future prospects in cancer therapy. J. Interf. Cytokine Res. 31 (2011), 545–552.
119. [119] Anguille, S., Lion, E., Willemen, Y., Van Tendeloo, V.F., Berneman, Z.N., Smits, E.L., Interferon-alpha in acute myeloid leukemia: an old drug revisited. Leukemia 25 (2011), 739–748.
120. [120] Kan, O., Day, D., Iqball, S., Burke, F., Grimshaw, M.J., Naylor, S., Binley, K., Genetically modified macrophages expressing hypoxia regulated cytochrome P450 and P450 reductase for the treatment of cancer. Int. J. Mol. Med. 27 (2011), 173–180.
121. [121] Herold, J., Pipp, F., Fernandez, B., Xing, Z., Heil, M., Tillmanns, H., Braun-Dullaeus, R.C., Transplantation of monocytes: a novel strategy for in vivo augmentation of collateral vessel growth. Hum. Gene Ther. 15 (2004), 1–12.
122. [122] Basel, M.T., Balivada, S., Shrestha, T.B., Seo, G.M., Pyle, M.M., Tamura, M., Bossmann, S.H., Troyer, D.L., A cell-delivered and cell-activated SN38-dextran prodrug increases survival in a murine disseminated pancreatic cancer model. Small 8 (2012), 913–920.
123. [123] Buschmann, I.R., Hoefer, I.E., van Royen, N., Katzer, E., Braun-Dulleaus, R., Heil, M., Kostin, S., Bode, C., Schaper, W., GM-CSF: a strong arteriogenic factor acting by amplification of monocyte function. Atherosclerosis 159 (2001), 343–356.
124. [124] Rosas, M., Davies, L.C., Giles, P.J., Liao, C.T., Kharfan, B., Stone, T.C., O'Donnell, V.B., Fraser, D.J., Jones, S.A., Taylor, P.R., The transcription factor Gata6 links tissue macrophage phenotype and proliferative renewal. Science 344 (2014), 645–648.
125. [125] 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.
126. [126] Hagemann, T., Biswas, S.K., Lawrence, T., Sica, A., Lewis, C.E., Regulation of macrophage function in tumors: the multifaceted role of NF-kappaB. Blood 113 (2009), 3139–3146.
127. [127] Hagemann, T., Lawrence, T., McNeish, I., Charles, K.A., Kulbe, H., Thompson, R.G., Robinson, S.C., Balkwill, F.R., “Re-educating” tumor-associated macrophages by targeting NF-kappaB. J. Exp. Med. 205 (2008), 1261–1268.
128. [128] Li, Y., Zhao, L., Shi, B., Ma, S., Xu, Z., Ge, Y., Liu, Y., Zheng, D., Shi, J., Functions of miR-146a and miR-222 in tumor-associated macrophages in breast cancer. Sci. Report., 5, 2015, 18648.
129. [129] Dang, W., Tang, H., Cao, H., Wang, L., Zhang, X., Tian, W., Pang, X., Li, K., Chen, T., Strategy of STAT3beta cell-specific expression in macrophages exhibits antitumor effects on mouse breast cancer. Gene Ther. 22 (2015), 977–983.
130. [130] Sieweke, M.H., Allen, J.E., Beyond stem cells: self-renewal of differentiated macrophages. Science, 342, 2013, 1242974.
131. [131] Aziz, A., Soucie, E., Sarrazin, S., Sieweke, M.H., MafB/c-Maf deficiency enables self-renewal of differentiated functional macrophages. Science 326 (2009), 867–871.
132. [132] Eggenhofer, E., Luk, F., Dahlke, M.H., Hoogduijn, M.J., The life and fate of mesenchymal stem cells. Front. Immunol., 5, 2014, 148.
133. [133] Fischer, U.M., Harting, M.T., Jimenez, F., Monzon-Posadas, W.O., Xue, H., Savitz, S.I., Laine, G.A., Cox, C.S. Jr., Pulmonary passage is a major obstacle for intravenous stem cell delivery: the pulmonary first-pass effect. Stem Cells Dev. 18 (2009), 683–692.
134. [134] Barbash, I.M., Chouraqui, P., Baron, J., Feinberg, M.S., Etzion, S., Tessone, A., Miller, L., Guetta, E., Zipori, D., Kedes, L.H., Kloner, R.A., Leor, J., Systemic delivery of bone marrow-derived mesenchymal stem cells to the infarcted myocardium: feasibility, cell migration, and body distribution. Circulation 108 (2003), 863–868.
135. [135] Dubey, P., Reporter gene imaging of immune responses to cancer: progress and challenges. Theranostics 2 (2012), 355–362.
136. [136] Pajarinen, J., Lin, T.H., Sato, T., Loi, F., Yao, Z., Konttinen, Y.T., Goodman, S.B., Establishment of green fluorescent protein and firefly luciferase expressing mouse primary macrophages for in vivo bioluminescence imaging. PLoS One, 10, 2015, e0142736.
137. [137] Wang, X., Rosol, M., Ge, S., Peterson, D., McNamara, G., Pollack, H., Kohn, D.B., Nelson, M.D., Crooks, G.M., Dynamic tracking of human hematopoietic stem cell engraftment using in vivo bioluminescence imaging. Blood 102 (2003), 3478–3482.
138. [138] Park, J.S., Suryaprakash, S., Lao, Y.H., Leong, K.W., Engineering mesenchymal stem cells for regenerative medicine and drug delivery. Methods 84 (2015), 3–16.
139. [139] Corradetti, B., Ferrari, M., Nanotechnology for mesenchymal stem cell therapies. J. Control. Release 240 (2016), 242–250.
140. [140] Assis, A.C., Carvalho, J.L., Jacoby, B.A., Ferreira, R.L., Castanheira, P., Diniz, S.O., Cardoso, V.N., Goes, A.M., Ferreira, A.J., Time-dependent migration of systemically delivered bone marrow mesenchymal stem cells to the infarcted heart. Cell Transplant. 19 (2010), 219–230.
141. [141] Ge, J., Guo, L., Wang, S., Zhang, Y., Cai, T., Zhao, R.C., Wu, Y., The size of mesenchymal stem cells is a significant cause of vascular obstructions and stroke. Stem Cell Rev. 10 (2014), 295–303.
142. [142] Guilak, F., Erickson, G.R., Ting-Beall, H.P., The effects of osmotic stress on the viscoelastic and physical properties of articular chondrocytes. Biophys. J. 82 (2002), 720–727.
143. [143] Kiehl, T.R., Shen, D., Khattak, S.F., Jian Li, Z., Sharfstein, S.T., Observations of cell size dynamics under osmotic stress. Cytometry. Part A 79 (2011), 560–569.
144. [144] Elmoazzen, H.Y., Chan, C.C., Acker, J.P., Elliott, J.A., McGann, L.E., The effect of cell size distribution on predicted osmotic responses of cells. Cryo-Letters 26 (2005), 147–158.
145. [145] Burke, A.M., Quest, D.O., Chien, S., Cerri, C., The effects of mannitol on blood viscosity. J. Neurosurg. 55 (1981), 550–553.
146. [146] Janowski, M., Lyczek, A., Engels, C., Xu, J., Lukomska, B., Bulte, J.W., Walczak, P., Cell size and velocity of injection are major determinants of the safety of intracarotid stem cell transplantation. J. Cereb. Blood Flow Metab. 33 (2013), 921–927.
147. [147] Aguado, B.A., Mulyasasmita, W., Su, J., Lampe, K.J., Heilshorn, S.C., Improving viability of stem cells during syringe needle flow through the design of hydrogel cell carriers. Tissue Eng. A 18 (2012), 806–815.
148. [148] Wong Po Foo, C.T., Lee, J.S., Mulyasasmita, W., Parisi-Amon, A., Heilshorn, S.C., Two-component protein-engineered physical hydrogels for cell encapsulation. Proc. Natl. Acad. Sci. U. S. A. 106 (2009), 22067–22072.
149. [149] Parisi-Amon, A., Mulyasasmita, W., Chung, C., Heilshorn, S.C., Protein-engineered injectable hydrogel to improve retention of transplanted adipose-derived stem cells. Advanced healthcare materials 2 (2013), 428–432.
150. [150] Mulyasasmita, W., Cai, L., Dewi, R.E., Jha, A., Ullmann, S.D., Luong, R.H., Huang, N.F., Heilshorn, S.C., Avidity-controlled hydrogels for injectable co-delivery of induced pluripotent stem cell-derived endothelial cells and growth factors. J. Control. Release 191 (2014), 71–81.
151. [151] Laflamme, M.A., Chen, K.Y., Naumova, A.V., Muskheli, V., Fugate, J.A., Dupras, S.K., Reinecke, H., Xu, C., Hassanipour, M., Police, S., O'Sullivan, C., Collins, L., Chen, Y., Minami, E., Gill, E.A., Ueno, S., Yuan, C., Gold, J., Murry, C.E., Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat. Biotechnol. 25 (2007), 1015–1024.
152. [152] Covarrubias, A.J., Aksoylar, H.I., Yu, J., Snyder, N.W., Worth, A.J., Iyer, S.S., Wang, J., Ben-Sahra, I., Byles, V., Polynne-Stapornkul, T., Espinosa, E.C., Lamming, D., Manning, B.D., Zhang, Y., Blair, I.A., Horng, T., Akt-mTORC1 signaling regulates Acly to integrate metabolic input to control of macrophage activation. eLife, 5, 2016.
153. [153] Schrepfer, S., Deuse, T., Reichenspurner, H., Fischbein, M.P., Robbins, R.C., Pelletier, M.P., Stem cell transplantation: the lung barrier. Transplant. Proc. 39 (2007), 573–576.
154. [154] van Rooijen, N., Hendrikx, E., Liposomes for specific depletion of macrophages from organs and tissues. Methods Mol. Biol. 605 (2010), 189–203.