Advertisement

Biochemistry (Moscow)

, Volume 84, Issue 7, pp 729–745 | Cite as

Advances and Challenges of Nanoparticle-Based Macrophage Reprogramming for Cancer Immunotherapy

  • K. S. Kapitanova
  • V. A. NaumenkoEmail author
  • A. S. Garanina
  • P. A. Melnikov
  • M. A. Abakumov
  • I. B. AlievaEmail author
Review
  • 8 Downloads

Abstract

Despite the progress of modern medicine, oncological diseases are still among the most common causes of death of adult populations in developed countries. The current therapeutic approaches are imperfect, and the high mortality of oncological patients under treatment, the lack of personalized strategies, and severe side effects arising as a result of treatment force seeking new approaches to therapy of malignant tumors. During the last decade, cancer immunotherapy, an approach that relies on activation of the host antitumor immune response, has been actively developing. Cancer immunotherapy is the most promising trend in contemporary fundamental and practical oncology, and restoration of the pathologically altered tumor microenvironment is one of its key tasks, in particular, the reprogramming of tumor macrophages from the immunosuppressive M2-phenotype into the proinflammatory M1-phenotype is pivotal for eliciting antitumor response. This review describes the current knowledge about macrophage classification, mechanisms of their polarization, their role in formation of the tumor microenvironment, and strategies for changing the functional activity of M2-macrophages, as well as problems of targeted delivery of immunostimulatory signals to tumor macrophages using nanoparticles.

Keywords

tumor microenvironment M1/M2-macrophages cancer immunotherapy nanoparticles intravital imaging 

Abbreviations

CD

cluster of differentiation

CSF

colony-stimulating factor

IFN-γ

interferon-gamma

IL

interleukin

iNOS

inducible nitric oxide synthase

IRF

interferon regulatory factor

F/M

intravital microscopy

LPS

lipopolysaccha-ride

NPs

nanoparticles

PD

programmed cell death

STAT

signal transducer and activator of transcription

TGFβ

transforming growth factor beta

TLR

Toll-like receptor

TNFα

tumor necrosis factor alpha

VEGF

vascular endothelium growth factor

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Mellman, I., Coukos, G., and Dranoff, G. (2011) Cancer immunotherapy comes of age, Nature, 480, 480–489, doi: 10.1038/naturel0673.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Mahoney, K. M., Rennert, P. D., and Freeman, G. J. (2015) Combination cancer immunotherapy and new immunomodulatory targets, Nat. Rev. Drug Discov., 14, 561–584, doi: 10.1038/nrd4591.CrossRefPubMedGoogle Scholar
  3. 3.
    Pardoll, D. M. (2012) The blockade of immune checkpoints in cancer immunotherapy, Nat. Rev. Cancer, 12, 252–264, doi: 10.1038/nrc3239.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Neelapu, S. S., Tummala, S., Kebriaei, P., Wierda, W., Gutierrez, C., Locke, F. L., Komanduri, K. V., Lin, Y., Jain, N., Daver, N., Westin, L., Gulbis, A. M., Loghin, M. E., de Groot, J. F., Adkins, S., Davis, S. E., Rezvani, K., Hwu, P., and Shpall, E. J. (2018) Chimeric antigen receptor T-cell therapy — assessment and management of toxicities, Nat. Rev. Clin. Oncol., 15, 47–62, doi: 10.1038/nrcli-nonc.2017.148.CrossRefPubMedGoogle Scholar
  5. 5.
    Romero, D. (2018) Immunotherapy: oncolytic viruses prime antitumour immunity, Nat. Rev. Clin. Oncol., 15, 135, doi: 10.1038/nrclinonc.2018.15.CrossRefPubMedGoogle Scholar
  6. 6.
    Valkenburg, K. C., de Groot, A. E., and Pienta, K. J. (2018) Targeting the tumour stroma to improve cancer therapy, Nat. Rev. Clin. Oncol., 15, 366–381, doi: 10.1038/S41571-018-0007-1.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Murdoch, C., Giannoudis, A., and Lewis, C. E. (2004) Mechanisms regulating the recruitment of macrophages into hypoxic areas of tumors and other ischemic tissues, Blood, 104, 2224–2234, doi: 10.1182/blood-2004-03-1109.CrossRefPubMedGoogle Scholar
  8. 8.
    Lewis, C. E., and Pollard, J. W. (2006) Distinct role of macrophages in different tumor microenvironments, Cancer Res., 66, 605–612, doi: 10.1158/0008-5472.can-05-4005.CrossRefPubMedGoogle Scholar
  9. 9.
    Martinez, F. O. (2011) Regulators of macrophage activation, Eur. J. Immunol., 41, 1531–1534, doi: 10.1002/eji.201141670.CrossRefPubMedGoogle Scholar
  10. 10.
    Miao, X., Leng, X., and Zhang, Q. (2017) The current state of nanoparticle-induced macrophage polarization and reprogramming research, Int. J. Mol. Sci., 18, E336, doi: 10.3390/ijmsl8020336.CrossRefPubMedGoogle Scholar
  11. 11.
    MacParland, S. A., Tsoi, K. M., Ouyang, B., Ma, X.-Z., Manuel, J., Fawaz, A., Ostrowski, M. A., Aman, B. A., Zilman, A., Chan, W. C. W., and McGilvray I. D. (2017) Phenotype determines nanoparticle uptake by human macrophages from liver and blood, ACS Nano, 11, 2428–2443, doi: 10.1021/acsnano.6b06245.CrossRefPubMedGoogle Scholar
  12. 12.
    Mills, C., and Ley, K. (2014) Ml and m2 macrophages: the chicken and the egg of immunity, J. Innate Immun., 6, 716–726, doi: 10.1159/000364945.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Zhou, D., Huang, C., Lin, Z., Zhan, S., Kong, L., Fang, C., and Li, J. (2014) Macrophage polarization and function with emphasis on the evolving roles of coordinated regulation of cellular signaling pathways, Cell. Signal., 26, 192–197, doi: 10.1016/j.cellsig.2013.11.004.CrossRefPubMedGoogle Scholar
  14. 14.
    Tripathi, C., Tewari, B. N., Kanchan, R. K., Baghel, K. S., Nautiyal, N., Shrivastava, R., Kaur, H., Bhatt, M. L. B., and Bhadauria, S. (2014) Macrophages are recruited to hypoxic tumor areas and acquire a pro-angiogenic M2-polarized phenotype via hypoxic cancer cell derived cytokines oncostatin M and eotaxin, Oncotarget, 5, 5350–5368, doi: 10.18632/oncotarget.2110.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Noy R., and Pollard, J. W. (2014) Tumor-associated macrophages: from mechanisms to therapy, Immunity, 41, 49–61, doi: 10.1016/j.immuni.2014.06.010.CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Caux, C., Ramos, R. N., Prendergast, G. C., Bendriss-Vermare, N., and Menetrier-Caux, C. (2016) A milestone review on how macrophages affect tumor growth, Cancer Res., 76, 6439–6442, doi: 10.1158/0008-5472.can-16-2631.CrossRefPubMedGoogle Scholar
  17. 17.
    Colegio, O. R., Chu, N.-Q., Szabo, A. L., Chu, T., Rhebergen, A. M., Jairam, V., Cyrus, N., Brokowski, C. E., Eisenbarth, S. C., Phillips, G. M., Cline, G. W., Phillips, A. L., and Medzhitov, R. (2014) Functional polarization of tumour-associated macrophages by tumour-derived lactic acid, Nature, 513, 559–563, doi: 10.1038/naturel3490.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Biswas, S. K., Sica, A., and Lewis, C. E. (2008) Plasticity of macrophage function during tumor progression: regulation by distinct molecular mechanisms, J. Immunol., 180, 2011–2017.CrossRefPubMedGoogle Scholar
  19. 19.
    MacGregor, H. L., and Ohashi, P. S. (2017) Molecular pathways: evaluating the potential for B7-H4 as an immunoregulatory target, Clin. CancerRes., 23, 2934–2941, doi: 10.1158/1078-0432.CCT-15-2440.CrossRefGoogle Scholar
  20. 20.
    Ruffell, B., and Coussens, L. M. (2015) Macrophages and therapeutic resistance in cancer, Cancer Cell, 27, 462–472, doi: 10.1016/j.ccell.2015.02.015.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Hughes, R., Qian, B.-Z., Rowan, C., Muthana, M., Keklikoglou, L., Olson, O. C., Tazzyman, S., Danson, S., Addison, C., Clemons, M., Gonzalez-Angulo, A. M., Joyce, J. A., De Palma, M., Pollard, J. W., and Lewis, C. E. (2015) Perivascular M2 macrophages stimulate tumor relapse after chemotherapy, Cancer Res., 75, 3479–3491, doi: 10.1158/0008-5472.can-14-3587.CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Yang, L., and Zhang, Y. (2017) Tumor-associated macrophages: from basic research to clinical application, J. Hematol. Oncol., 10, 58, doi: 10.1186/sl3045-017-0430-2.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Kim, D.-S., Dastidar, H., Zhang, C., Zemp, F. J., Lau, K., Ernst, M., Rakic, A., Sikdar, S., Rajwani, J., Naumenko, V., Balce, D. R., Ewanchuk, B. W., Tailor, P., Yates, R. M., Jenne, C., Gafuik, C., and Mahoney, D. J. (2018) Author correction: Smac mimetics and oncolytic viruses synergize in driving anticancer T-cell responses through complementary mechanisms, Nat. Commun., 9, 2109, doi: 10.1038/S41467-018-04597-8.CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Penn, C. A., Yang, K., Zong, H., Lim, J.-Y., Cole, A., Yang, D., Baker, J., Goonewardena, S. N., and Buckanovich, R. J. (2018) Therapeutic impact of nanoparticle therapy targeting tumor-associated macrophages, Mol. Cancer Ther., 17, 96–106, doi: 10.1158/1535-7163mct-17-0688.CrossRefPubMedGoogle Scholar
  25. 25.
    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, L., Sanfilippo, R., Casali, R G, Pilotti, S., Galmarini, C. M., Anichini, A., Mantovani, A., D’Incaici, M., and Allavena, R. (2013) Role of macrophage targeting in the antitumor activity of trabectedin, Cancer Cell, 23, 249–262, doi: 10.1016/j.ccr.2013.01.008.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    De Palma, M., Venneri, M. A., Galli, R., Sergi, L. S., Politi, L. S., Sampaolesi, M., and Naldini, L. (2005) Tie2 identifies a hematopoietic lineage of proangiogenic monocytes required for tumor vessel formation and a mesenchymal population of pericyte progenitors, Cancer Cell, 8, 211–226, doi: 10.1016/j.ccr.2005.08.002.CrossRefPubMedGoogle Scholar
  27. 27.
    Cassier, P. A., Italiano, A., Gomez-Roca, C. A., Le Tourneau, C., Toulmonde, M., Cannarile, M. A., Ries, C., Brillouet, A., Muller, C., Jegg, A.-M., Broske, A.-M., Dembowski, M., Bray-French, K., Freilinger, C., Meneses-Lo rente, G., Baehner, M., Harding, R., Ratnayake, L., Abiraj, K., Gass, N., Noh, K., Christen, R. D., Ukarma, L., Bompas, E., Delord, J.-P., Blay J.-Y., and Ruttinger, D. (2015) Csflr inhibition with emactuzumab in locally advanced diffuse-type tenosynovial giant cell tumours of the soft tissue: a dose-escalation and dose-expansion phase 1 study, Lancet Oncol, 16, 949–956, doi: 10.1016/sl470-2045(15)00132-l.CrossRefPubMedGoogle Scholar
  28. 28.
    Movahedi, K., Schoonooghe, S., Laoui, D., Houbracken, I., Waelput, W., Breckpot, K., Bouwens, L., Lahoutte, T, De Baetselier, P., Raes, G., Devoogdt, N., and Van Ginderachter, J. A. (2012) Nanobody-based targeting of the macrophage mannose receptor for effective in vivo imaging of tumor-associated macrophages, Cancer Res., 72, 4165–4177, doi: 10.1158/0008-5472.can-ll-2994.CrossRefPubMedGoogle Scholar
  29. 29.
    Pulaski, H. L., Spahlinger, G., Silva, I. A., McLean, K., Kueck, A. S., Reynolds, R. K., Coukos, G., Conejo-Garcia, J. R., and Buckanovich, R. J. (2009) Identifying alemtuzumab as an anti-myeloid cell antiangiogenic therapy for the treatment of ovarian cancer, J. Transi. Med., 1, 49, doi: 10.1186/1479-5876-7-49.Google Scholar
  30. 30.
    Smahel, M., Duskova, M., Polakova, I., and Musil, J. (2014) Enhancement of DNA vaccine potency against legumain, J. Immunother., 37, 293–303, doi: 10.1097/cji. 0000000000000040.CrossRefPubMedGoogle Scholar
  31. 31.
    Ahn, G.-O., Lseng, D., Liao, C.-H., Dorie, M. L., Czechowicz, A., and Brown, J. M. (2010) Inhibition of Mac-1 (CDllb/CD18) enhances tumor response to radiation by reducing myeloid cell recruitment, Proc. Natl. Acad. Sci. USA, 107, 8363–8368, doi: 10.1073/pnas.0911378107.CrossRefPubMedGoogle Scholar
  32. 32.
    Sanford, D. E., Belt, B. A., Panni, R. Z., Mayer, A., Deshpande, A. D., Carpenter, D., Mitchem, J. B., Plambeck-Suess, S. M., Worley L. A., Goetz, B. D., Wang-Gillam, A., Eberlein, L. J., Denardo, D. G., Goedegebuure, S. P., and Linehan, D. C. (2013) Inflammatory monocyte mobilization decreases patient survival in pancreatic cancer: a role for targeting the CCL2/CCR2 axis, Clin. Cancer Res., 19, 3404–3415, doi: 10.1158/1078-0432.ccr-13-0525.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Nywening, L. M., Wang-Gillam, A., Sanford, D. E., Belt, B. A., Panni, R. Z., Cusworth, B. M., Loriola, A. T., Nieman, R. K., Worley, L. A., Yano, M., Fowler, K. J., Lockhart, A. C., Suresh, R., Lan, B. R., Lim, K.-H., Fields, R. C., Strasberg, S. M., Hawkins, W. G., DeNardo, D. G., Goedegebuure, S. P., and Linehan, D. C. (2016) Largeting tumor-associated macrophages with CCR2 inhibition in combination with FOLFIRINOX in patients with borderline resectable and locally advanced pancreatic cancer: a single-centre, open-label, dose-finding, non-randomised, phase lb trial, Lancet Oncol., 17, 651–662, doi: 10.1016/S1470-2045(16)00078-4.CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Pienta, K. L., Machiels, J.-P., Schrijvers, D., Alekseev, B., Shkolnik, M., Crabb, S. L., Li, S., Seetharam, S., Puchalski, L. A., Lakimoto, C., Elsayed, Y., Dawkins, E., and de Bono, J. S. (2013) Phase 2 study of carlumab (CNLO 888), a human monoclonal antibody against CC-chemokine ligand 2 (CCL2), in metastatic castration-resistant prostate cancer, Invest. New Drug., 31, 760–768, doi: 10.1007/S10637-012-9869-8.CrossRefGoogle Scholar
  35. 35.
    Sandhu, S. K., Papadopoulos, K., Fong, P. C., Patnaik, A., Messiou, C., Olmos, D., Wang, G., Lromp, B. L., Puchalski, L. A., Balkwill, F., Berns, B., Seetharam, S., de Bono, J. S., and Lolcher, A. W. (2013) A first-in-human, first-in-class, phase I study of carlumab (CNLO 888), a human monoclonal antibody against CC-chemokine ligand 2 in patients with solid tumors, Cancer Chemother. Pharmacol., 71, 1041–1050, doi: 10.1007/s00280-013-2099-8.CrossRefPubMedGoogle Scholar
  36. 36.
    Brana, L., Calles, A., LoRusso, P. M., Yee, L. K., Puchalski, L. A., Seetharam, S., Zhong, B., de Boer, C. L., Labernero, J., and Calvo, E. (2015) Carlumab, ananti-C-C chemokine ligand 2 monoclonal antibody, in combination with four chemotherapy regimens for the treatment of patients with solid tumors: an open-label, multicenter phase lb study, Target. Oncol., 10, 111–123, doi: 10.1007/S11523-014-0320-2.CrossRefPubMedGoogle Scholar
  37. 37.
    Pyonteck, S. M., Akkari, L., Schuhmacher, A. J., Bowman, R. L., Sevenich, L., Quail, D. F., Olson, O. C., Quick, M. L., Huse, J. L., Leijeiro, V., Setty M., Leslie, C. S., Oei, Y., Pedraza, A., Zhang, J., Brennan, C. W., Sutton, J. C., Holland, E. C., Daniel, D., and Joyce, J. A. (2013) CSF-1R inhibition alters macrophage polarization and blocks glioma progression, Nat. Med., 19, 1264–1272, doi: 10.1038/nm.3337.CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Pyonteck, S. M., Gadea, B. B., Wang, H.-W., Gocheva, V., Hunter, K. E., Lang, L. H., and Joyce, J. A. (2012) Deficiency of the macrophage growth factor CSF-1 disrupts pancreatic neuroendocrine tumor development, Oncogene, 31, 1459–1467, doi: 10.1038/onc.2011.337.CrossRefPubMedGoogle Scholar
  39. 39.
    Beatty G. L., Chiorean, E. G., Fishman, M. P., Saboury B., Leitelbaum, U. R., Sun, W., Huhn, R. D., Song, W., Li, D., Sharp, L. L., Lorigian, D. A., O’Dwyer, P. J., and vonderheide, R. H. (2011) CD40 agonists alter tumor stroma and show efficacy against pancreatic carcinoma in mice and humans, Science, 331, 1612–1616, doi: 10.1126/science.ll98443.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Ruffell, B., Chang-Strachan, D., Chan, V., Rosenbusch, A., Ho, C. M. L., Pryer, N., Daniel, D., Hwang, E. S., Rugo, H. S., and Coussens, L. M. (2014) Macrophage ILIO blocks CD8+ L cell-dependent responses to chemotherapy by suppressing IL-12 expression in intratumoral dendritic cells, Cancer Cell, 26, 623–637, doi: 10.1016/j.ccell.2014.09.006.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Su, Z., Yang, R., Zhang, W., Xu, L., Zhong, Y., Yin, Y., Cen, J., DeWitt, J. P., and Wei, Q. (2015) Lhe synergistic interaction between the calcineurin B subunit and IFN-γ enhances macrophage antitumor activity, Cell Death Dis., 6, el740-el740, doi: 10.1038/cddis.2015.92.Google Scholar
  42. 42.
    Yang, L., Wang, F., Wang, L., Huang, L., Wang, J., Zhang, B., and Zhang, Y. (2015) CD163+ tumor-associated macrophage is a prognostic biomarker and is associated with therapeutic effect on malignant pleural effusion of lung cancer patients, Oncotarget, 6, 10592–10603, doi: 10.18632/oncotarget.3547.PubMedPubMedCentralGoogle Scholar
  43. 43.
    Hussain, S. F., Kong, L.-Y., Jordan, J., Conrad, C., Madden, T., Fokt, I., Priebe, W., and Heimberger, A. B. (2007) A novel small molecule inhibitor of signal transducers and activators of transcription 3 reverses immune tolerance in malignant glioma patients, Cancer Res., 67, 9630–9636, doi: 10.1158/0008-5472.can-07-1243.CrossRefPubMedGoogle Scholar
  44. 44.
    Seya, L., Shime, H., and Matsumoto, M. (2012) LAMable tumor-associated macrophages in response to innate RNA sensing, Oncoimmunology, 1, 1000–1001, doi: 10.4161/onci. 19894.CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Guiducci, C., Vicari, A. P., Sangaletti, S., Trinchieri, G., and Colombo, M. P. (2005) Redirecting in vivo elicited tumor infiltrating macrophages and dendritic cells towards tumor rejection, Cancer Res., 65, 3437–3446, doi: 10.1158/0008-5472.can-04-4262.CrossRefPubMedGoogle Scholar
  46. 46.
    Sato, T., Shimosato, T., Ueda, A., Ishigatsubo, Y., and Klinman, D. M. (2015) Intrapulmonary delivery of CpG microparticles eliminates lung tumors, Mol. Cancer Ther., 14, 2198–2205, doi: 10.1158/1535-7163.mct-15-0401.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Eriksson, F., Tsagozis, P., Lundberg, K., Parsa, R., Mangsbo, S. M., Persson, M. A. A., Harris, R. A., and Pisa, P. (2009) Tumor-specific bacteriophages induce tumor destruction through activation of tumor-associated macrophages, J. Immunol, 182, 3105–3111, doi: 10.4049/jimmunol.0800224.CrossRefPubMedGoogle Scholar
  48. 48.
    Shi, Y., Felder, M. A. R., Sondel, P. M., and Rakhmilevich, A. L. (2015) Synergy of anti-CD40, CpG and MPL in activation of mouse macrophages, Mol. Immunol., 66, 208–215, doi: 10.1016/j.molimm.2015.03.008.CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Sica, A., Saccani, A., Bottazzi, B., Polentarutti, N., Vecchi, A., Van Damme, J., and Mantovani, A. (2000) Autocrine production of IL-10 mediates defective IL-12 production and NF-KB activation in tumor-associated macrophages, J. Immunol., 164, 762–767, doi: 10.4049/jimmunol. 164.2.762.CrossRefPubMedGoogle Scholar
  50. 50.
    Chan, G., Chan, W., and Sze, D. (2009) The effects of ß-glucan on human immune and cancer cells, J. Hematol. Oncol., 2, 25, doi: 10.1186/1756-8722-2-25.CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Huang, Z., Yang, Y., Jiang, Y., Shao, J., Sun, X., Chen, J., Dong, L., and Zhang, J. (2013) Anti-tumor immune responses of tumor-associated macrophages via toll-like receptor 4 triggered by cationic polymers, Biomaterials, 34, 746–755, doi: 10.1016/j. biomaterials.2012.09.062.CrossRefPubMedGoogle Scholar
  52. 52.
    Kushner, B. H., Cheung, I. Y., Modak, S., Kramer, K., Ragupathi, G., and Cheung, N. K. V. (2014) Phase I trial of a bivalent gangliosides vaccine in combination with ß-glucan for high-risk neuroblastoma in second or later remission, Clin. Cancer Res., 20, 1375–1382, doi: 10.1158/1078-0432.CCT-13-1012.CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Segal, N. H., Gada, P., Senzer, N., Gargano, M. A., Patchen, M. L., and Saltz, L. B. (2016) A phase 2 efficacy and safety, open-label, multicenter study of imprime PGG injection in combination with cetuximab in patients with stage TV KRAS-raatar A colorectal cancer, Clin. Colorectal Cancer, 15, 222–227, doi: 10.1016/j.clcc.2016.02.013.CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Garaci, E., Pica, F., Serafino, A., Balestrieri, E., Matteucci, C., Moroni, G., Sorrentino, R., Zonfrillo, M., Pierimarchi, P., and Sinibaldi-Vallebona, P. (2012) Thymosin al and cancer: action on immune effector and tumor target cells, Ann. N. Y. Acad. Sci., 1269, 26–33, doi: 10.HH/j.1749-6632.2012.06697.x.CrossRefPubMedGoogle Scholar
  55. 55.
    Beug, S. T., Beauregard, C. E., Healy C., Sanda, T., St-Jean, M., Chabot, J., Walker, D. E., Mohan, A., Earl, N., Lun, X., Senger, D. L., Robbins, S. M., Staeheli, R., Forsyth, P. A., Alain, T., LaCasse, E. C. and Korneluk, R. G. (2018) Publisher correction: Smac mimetics synergize with immune checkpoint inhibitors to promote tumour immunity against glioblastoma, Nat. Commun., 9, 16231, doi: 10.1038/ncommsl6231.CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Gul, N., and Van Egmond, M. (2015) Antibody-dependent phagocytosis of tumor cells by macrophages: a potent effector mechanism of monoclonal antibody therapy of cancer, Cancer Res., 75, 5008–5013, doi: 10.1158/0008-5472.can-15-1330.CrossRefPubMedGoogle Scholar
  57. 57.
    Zhao, X. W., Van Beek, E. M., Schornagel, K., Van der Maaden, H., Van Houdt, M., Otten, M. A., Finetti, P., Van Egmond, M., Matozaki, T, Kraal, G., Birnbaum, D., Van Elsas, A., Kuijpers, T. W., Bertucci, F., and Van den Berg, T. K. (2011) CD47-signal regulatory protein-a (SIRP-a) interactions form a barrier for antibody-mediated tumor cell destruction, Proc. Natl. Acad. Sci. USA, 108, 18342–18347, doi: 10.1073/pnas.ll06550108.CrossRefPubMedGoogle Scholar
  58. 58.
    Wang, Y., Lin, Y.-X., Qiao, S.-L., An, H.-W., Ma, Y., Qiao, Z.-Y., Rajapaksha, R. P., and Wang, H. (2017) Polymeric nanoparticles promote macrophage reversal from M2 to Ml phenotypes in the tumor microenvironment, Biomaterials, 112, 153–163, doi: 10.1016/j.biomateri-als.2016.09.034.CrossRefPubMedGoogle Scholar
  59. 59.
    Zhu, L., Zhou, Z., Mao, H., and Yang, L. (2017) Magnetic nanoparticles for precision oncology: theranostic magnetic iron oxide nanoparticles for image-guided and targeted cancer therapy, Nanomedicine, 12, 73–87, doi: 10.2217/nnm-2016-0316.CrossRefPubMedGoogle Scholar
  60. 60.
    Shi, J., Kantoff, P. W., Wooster, R., and Farokhzad, O. C. (2017) Cancer nanomedicine: progress, challenges and opportunities, Nat. Rev. Cancer, 17, 20–37, doi: 10.1038/nrc.2016.108.CrossRefPubMedGoogle Scholar
  61. 61.
    Lee, H., Shields, A. F., Siegel, B. A., Miller, K. D., Krop, I., Ma, C. X., LoRusso, P. M., Munster, P. N., Campbell, K., Gaddy D. F., Leonard, S. C., Geretti, E., Blocker, S. L., Kirpotin, D. B., Moyo, V., Wickham, T. L., and Hendriks, B. S. (2017) 64Cu-MM-3O2 positron emission tomography quantifies variability of enhanced permeability and retention of nanoparticles in relation to treatment response in patients with metastatic breast cancer, Clin. Cancer Res., 23, 4190–4202, doi: 10.1158/1078-0432.ccr-16-3193.CrossRefPubMedGoogle Scholar
  62. 62.
    Ramanathan, R. K., Korn, R. L., Raghunand, N., Sachdev, J. C., Newbold, R. G., Jameson, G., Fetterly G. J., Prey, J., Klinz, S. G., Kim, J., Cain, J., Hendriks, B. S., Drummond, D. C., Bayever, E., and Fitzgerald, J. B. (2017) Correlation between ferumoxytol uptake in tumor lesions by MRI and response to nanoliposomal irinotecan in patients with advanced solid tumors: a pilot study, Clin. Cancer Res., 23, 3638–3648, doi: 10.1158/1078-0432.ccr-16-1990.CrossRefPubMedGoogle Scholar
  63. 63.
    Nakamura, Y., Mochida, A., Choyke, P. L., and Kobayashi, H. (2016) Nanodrug delivery: is the enhanced permeability and retention effect sufficient for curing cancer? Bioconjug. Chem., 27, 2225–2238, doi: 10.1021/acs.bioconjchem.6b00437.CrossRefPubMedGoogle Scholar
  64. 64.
    Lazarovits, J., Chen, Y. Y., Sykes, E. A., and Chan, W. C. W. (2015) Nanoparticle—blood interactions: the implications on solid tumour targeting, Chem. Commun., 51, 2756–2767, doi: 10.1039/c4cc07644c.CrossRefGoogle Scholar
  65. 65.
    Wilhelm, S., Tavares, A. J., Dai, Q., Ohta, S., Audet, J., Dvorak, H. F., and Chan, W. C. W. (2016) Analysis of nanoparticle delivery to tumours, Nat. Rev. Mater., 1, 16014, doi: 10.1038/natrevmats.2016.14.CrossRefGoogle Scholar
  66. 66.
    Miller, M. A., Gadde, S., Pfirschke, C., Engblom, C., Sprachman, M. M., Köhler, R. H., Yang, K. S., Laughney A. M., Wojtkiewicz, G., Kamaly N., Bhonagiri, S., Pittet, M. J., Farokhzad, O. C., and Weissleder, R. (2015) Predicting therapeiitic nanomedicine efficacy using a companion magnetic resonance imaging nanoparticle, Sci. Transi. Med., 7, 314ra183, doi: 10.1126/scitranslmed. aac6522.CrossRefGoogle Scholar
  67. 67.
    Miller, M. A., Zheng, Y-R., Gadde, S., Pfirschke, C., Zope, H., Engblom, C., Köhler, R. H., Iwamoto, Y., Yang, K. S., Askevold, B., Kolishetti, N., Pittet, M., Lippard, S. J., Farokhzad, O. C., and Weissleder, R. (2015) Tumour-associated macrophages act as a slow-release reservoir of nano-therapeutic Pt(IV) pro-drug, Nat. Commun., 6, 8692, doi: 10.1038/ncomms9692.CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Mikhaylov, G., Mikac, U., Magaeva, A. A., Itin, V. I., Naiden, E. P., Psakhye, I., Babes, L., Reinheckel, T, Peters, C., Zeiser, R., Bogyo, M., Turk, V., Psakhye, S. G., Turk, B., and Vasiljeva, O. (2011) Ferri-liposomes as an MRI-visible drug-delivery system for targeting tumours and their microenvironment, Nat. Nanotechnol, 6, 594–602, doi: 10.1038/nnano.2011.112.CrossRefPubMedGoogle Scholar
  69. 69.
    Daldrup-Link, H. E., Golovko, D., Ruffell, B., DeNardo, D. G., Castaneda, R., Ansari, C., Rao, J., Tikhomirov, G. A., Wendland, M. F., Corot, C., and Coussens, L. M. (2011) MRI of tumor-associated macrophages with clinically applicable iron oxide nanoparticles, Clin. Cancer Res., 17, 5695–5704, doi: 10.1158/1078-0432.ccr-10-3420.CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Ilkow, C. S., Marguerie, M., Batenchuk, C., Mayer, J., Ben Neriah, D., Cousineau, S., Falls, T, Jennings, V. A., Boileau, M., Bellamy, D., Bastin, D., de Souza, C. T., Alkayyal, A., Zhang, J., Le Boeuf, F., Arulanandam, R., Stubbert, L., Sampath, P., Thorne, S. H., Paramanthan, P., Chatterjee, A., Strieter, R. M., Burdick, M., Addison, C. L., Stojdl, D. F., Atkins, H. L., Auer, R. C., Diallo, J.-S., Lichty B. D., and Bell, J. C. (2015) Reciprocal cellular cross-talk within the tumor microenvironment promotes oncolytic virus activity, Nat. Med., 21, 530–536, doi: 10.1038/nm.3848.CrossRefPubMedGoogle Scholar
  71. 71.
    Arulanandam, R., Batenchuk, C., Angarita, F. A., Ottolino-Perry K., Cousineau, S., Mottashed, A., Burgess, E., Falls, T. J., De Silva, N., Tsang, J., Howe, G. A., Bourgeois-Daigneault, M.-C., Conrad, D. P., Daneshmand, M., Breitbach, C. J., Kirn, D. F. L., Raptis, L., Sad, S., Atkins, H., Huh, M. S., Diallo, J.-S., Lichty, B. D., Ilkow, C. S., Le Boeuf, F., Addison, C. L., McCart, J. A., and Bell, J. C. (2015) VEGF-mediated induction of PRDl-BFl/Blimpl expression sensitizes tumor vasculature to oncolytic virus infection, Cancer Cell, 28, 210–224, doi: 10.1016/j.ccell.2015.06.009.CrossRefPubMedGoogle Scholar
  72. 72.
    Hoppstadter, J., Seif, M., Dembek, A., Cavelius, C., Huwer, H., Kraegeloh, A., and Kiemer, A. K. (2015) M2 polarization enhances silica nanoparticle uptake by macrophages, Front. Pharmacol., 6, 55, doi: 10.3389/fphar.2015.00055.CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Qie, Y., Yuan, H., von Roemeling, C. A., Chen, Y., Liu, X., Shih, K. D., Knight, J. A., Tun, H. W., Wharen, R. E., Jiang, W., and Kim, B. Y S. (2016) Erratum: Corrigendum: surface modification of nanoparticles enables selective evasion of phagocytic clearance by distinct macrophage phe-notypes, Sci. Rep., 6, 26269, doi: 10.1038/srep30663.CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Jones, S. W., Roberts, R A, Robbins, G. R., Perry, J. L., Kai, M. P., Chen, K., Bo, T, Napier, M. E., Ting, J. P. Y., DeSimone, J. M., and Bear, J. E. (2013) Nanoparticle clearance is governed by Thl/Th2 immunity and strain background, J. Clin. Invest., 123, 3061–3073, doi: 10.1172/jci66895.CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Binnemars-Postma, K. A., ten Hoopen, H. W., Storm, G., and Prakash, J. (2016) Differential uptake of nanoparticles by human Ml and M2 polarized macrophages: protein corona as a critical determinant, Nanomedicine, 11, 2889–2902, doi: 10.2217/nnm-2016-0233.CrossRefPubMedGoogle Scholar
  76. 76.
    Thaiss, C. A., Zmora, N., Levy, M., and Elinav, E. (2016) The microbiome and innate immunity, Nature, 535, 65–74, doi: 10.1038/naturel8847.CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Lonez, C., Bessodes, M., Scherman, D., Vandenbranden, M., Escriou, V., and Ruysschaert, J.-M. (2014) Cationic lipid nanocarriers activate Toll-like receptor 2 and NLRP3 inflammasome pathways, Nanomedicine, 10, 775–782, doi: 10.1016/j.nano.2013.12.003.CrossRefPubMedGoogle Scholar
  78. 78.
    Lebel, M.-E., Daudelin, J.-F., Chartrand, K., Tarrab, E., Kalinke, U., Savard, P., Labrecque, N., Ledere, D., and Lamarre, A. (2014) Nanoparticle adjuvant sensing by TLR7 enhances CD8+ T cell-mediated protection from Listeria monocytogenes infection, J. Immunol., 192, 1071–1078, doi: 10.4049/jimmunol.l302030.CrossRefPubMedGoogle Scholar
  79. 79.
    Rioux, G., Carignan, D., Russell, A., Bolduc, M., Gagne, M.-E. L., Savard, P., and Ledere, D. (2016) Influence of PapMV nanoparticles on the kinetics of the antibody response to flu vaccine, J. Nanobiotechnol., 14, 43, doi: 10.1186/S12951-016-0200-2.CrossRefGoogle Scholar
  80. 80.
    Yen, H.-J., Hsu, S., and Tsai, C.-L. (2009) Cytotoxicity and immunological response of gold and silver nanoparticles of different sizes, Small, 5, 1553–1561, doi: 10.1002/smll.200900126.CrossRefPubMedGoogle Scholar
  81. 81.
    Nishanth, R. P., Jyotsna, R. G., Schlager, J. J., Hussain, S. M., and Reddanna, P. (2011) Inflammatory responses of RAW 264.7 macrophages upon exposure to nanoparticles: role of ROS-NFKB signaling pathway, Nanotoxicology, 5, 502–516, doi: 10.3109/17435390.2010.541604.CrossRefPubMedGoogle Scholar
  82. 82.
    Hashimoto, M., Toshima, H., Yonezawa, T., Kawai, K., Narushima, T, Kaga, M., and Endo, K. (2014) Responses of RAW264.7 macrophages to water-dispersible gold and silver nanoparticles stabilized by metal-carbon a-bonds, J. Biomed. Mater. Res. A, 102, 1838–1849, doi: 10.1002/jbm.a.34854.CrossRefPubMedGoogle Scholar
  83. 83.
    Bancos, S., Stevens, D. L., and Tyner, K. M. (2014) Effect of silica and gold nanoparticles on macrophage proliferation, activation markers, cytokine production, and phagocytosis in vitro, Int. J. Nanomedicine, 10, 183–206, doi: 10.2147/ijn.s72580.PubMedPubMedCentralGoogle Scholar
  84. 84.
    Zhang, Q., Hitchins, V. M., Schrand, A. M., Hussain, S. M., and Goering, P. L. (2011) Uptake of gold nanoparticles in murine macrophage cells without cytotoxicity or production of pro-inflammatory mediators, Nanotoxicology, 5, 284–295, doi: 10.3109/17435390.2010.512401.CrossRefPubMedGoogle Scholar
  85. 85.
    Giovanni, M., Yue, J., Zhang, L., Xie, J., Ong, C. N., and Leong, D. T. (2015) Pro-inflammatory responses of RAW264.7 macrophages when treated with ultralow concentrations of silver, titanium dioxide, and zinc oxide nanoparticles, J. Hazard. Mater., 191, 146–152, doi: 10.1016/j.jhazmat.2015.04.081.Google Scholar
  86. 86.
    Lucarelli, M., Gatti, A. M., Savarino, G., Quattroni, P., Martinelli, L., Monari, E., and Boraschi, D. (2004) Innate defense functions of macrophages can be biased by nano-sized ceramic and metallic particles, Eur. Cytokine Netw., 15, 339–346.PubMedGoogle Scholar
  87. 87.
    Yang, R., Sarkar, S., Yong, V. W., and Dunn, J. F. (2018) In vivo MR imaging of tumor-associated macrophages: the next frontier in cancer imaging, Magn. Resoti. Insights, 11, 1178623X1877197, doi: 10.1177/1178623x18771974.Google Scholar
  88. 88.
    Zanganeh, S., Hutter, G., Spitler, R., Lenkov, O., Mahmoudi, M., Shaw, A., Pajarinen, J. S., Nejadnik, H., Goodman, S., Moseley, M., Coussens, L. M., and Daldrup-Link, H. E. (2016) Iron oxide nanoparticles inhibit tumour growth by inducing pro-inflammatory macrophage polarization in tumour tissues, Nat. Nanotechnol., 11, 986–994, doi: 10.1038/nnano.2016. 168.CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    Laskar, A., Eilertsen, J., Li, W., and Yuan, X.-M. (2013) SPION primes THP1 derived M2 macrophages towards M1-like macrophages, Biochem. Biophys. Res. Commun., 441, 737–742, doi: 10.1016/j.bbrc.2013.10.115.CrossRefPubMedGoogle Scholar
  90. 90.
    Ma, J., Liu, R., Wang, X., Liu, Q., Chen, Y., Valle, R. P., Zuo, Y. Y., Xia, T., and Liu, S. (2015) Crucial role of lateral size for graphene oxide in activating macrophages and stimulating pro-inflammatory responses in cells and animals, ACS Nano, 9, 10498–10515, doi: 10.1021/acsnano. 5b04751.CrossRefPubMedPubMedCentralGoogle Scholar
  91. 91.
    Doshi, N., and Mitragotri, S. (2010) Macrophages recognize size and shape of their targets, PLoS One, 5, el 0051, doi: 10.1371/journal.pone.0010051.Google Scholar
  92. 92.
    Vinogradov, S., Warren, G., and Wei, X. (2014) Macrophages associated with tumors as potential targets and therapeutic intermediates, Nanomedicine, 9, 695–707, doi: 10.2217/nnm.14.13.CrossRefPubMedGoogle Scholar
  93. 93.
    Bartneck, M., Ritz, T., Keul, H. A., Wambach, M., Bornemann, J., Gbureck, U., Ehling, J., Lammers, T, Heymann, F., Gassler, N., Ludde, T., Lrautwein, C., Groll, J., and Lacke, F. (2012) Peptide-functionalized gold nanorods increase liver injury in hepatitis, ACS Nano, 6, 8767–8777, doi: 10.1021/nn302502u.CrossRefPubMedGoogle Scholar
  94. 94.
    Su, L., Zhang, W., Wu, X., Zhang, Y., Chen, X, Liu, G., Chen, G., and Jiang, M. (2015) Glycocalyx-mimicking nanoparticles for stimulation and polarization of macrophages via specific interactions, Small, 11, 4191–4200, doi: 10.1002/smll.201403838.CrossRefPubMedGoogle Scholar
  95. 95.
    Fuchs, A.-K., Syrovets, L., Haas, K. A., Loos, C., Musyanovych, A., Mailander, V., Landfester, K., and Simmet, L. (2016) Carboxyl- and amino-functionalized polystyrene nanoparticles differentially affect the polarization profile of Ml and M2 macrophage subsets, Biomaterials, 85, 78–87, doi: 10.1016/j. biomateri-als.2016.01.064.CrossRefPubMedGoogle Scholar
  96. 96.
    Wei, M., Chen, N., Li, L., Yin, M., Liang, L., He, Y., Song, H., Fan, C., and Huang, Q. (2012) Polyvalent immunos-timulatory nanoagents with self-assembled CpG oligonu-cleotide-conjugated gold nanoparticles, Angew. Chem. Int. Ed. Engl., 51, 1202–1206, doi: 10.1002/anie.201105187.CrossRefPubMedGoogle Scholar
  97. 97.
    Kim, J. H., Noh, Y-W., Heo, M. B., Cho, M. Y., and Lim, Y. L. (2012) Multifunctional hybrid nanoconjugates for efficient in vivo delivery of immunomodulating oligonucleotides and enhanced antitumor immunity, Angew. Chem. Int. Ed. Engl., 51, 9670–9673, doi: 10.1002/anie. 201204989.CrossRefPubMedGoogle Scholar
  98. 98.
    Ruiz-de-Angulo, A., Zabaleta, A., Gomez-Vallejo, V., Llop, J., and Mareque-Rivas, J. C. (2016) Microdosed lipid-coated 67Ga-magnetite enhances antigen-specific immunity by image tracked delivery of antigen and CpG to lymph nodes, ACS Nano, 10, 1602–1618, doi: 10.1021/acsnano.5b07253.CrossRefPubMedGoogle Scholar
  99. 99.
    Kim, S.-Y., Heo, M. B., Hwang, G.-S., Jung, Y., Choi, D. Y., Park, Y-M., and Lim, Y. L. (2015) Multivalent polymer nanocomplex targeting endosomal receptor of immune cells for enhanced antitumor and systemic memory response, Angew. Chem. Int. Ed. Engl., 54, 8139–8143, doi: 10.1002/anie.201501380.CrossRefPubMedGoogle Scholar
  100. 100.
    Li, A. V., Moon, J. J., Abraham, W., Suh, H., Elkhader, J., Seidman, M. A., Yen, M., Im, E.-J., Foley, M. H., Barouch, D. H., and Irvine, D. J. (2013) Generation of effector memory L cell-based mucosal and systemic immunity with pulmonary nanoparticle vaccination, Sci. Transi. Med., 5, 204ra130, doi: 10.1126/sci-translmed.3006516.Google Scholar
  101. 101.
    Ultimo, A., Gimenez, C., Bartovsky P., Aznar, E., Sancenon, F., Marcos, M. D., Amoros, R., Bernardo, A. R., Martinez-Manez, R., Jimenez-Lara, A. M., and Murguia, J. R. (2016) Largeting innate immunity with dsRNA-conjugated mesoporous silica nanoparticles promotes antitumor effects on breast cancer cells, Chem. Eur. J., 22, 1582–1586, doi: 10.1002/chem.201504629.CrossRefPubMedGoogle Scholar
  102. 102.
    Fox, C. B., Sivananthan, S. J., Duthie, M. S., Vergara, J., Guderian, J. A., Moon, E., Coblentz, D., Reed, S. G., and Carter, D. (2014) A nanoliposome delivery system to syn-ergistically trigger LLR4 and LLR7, J. Nanobiotechnol., 12, 17, doi: 10.1186/1477-3155-12-17.CrossRefGoogle Scholar
  103. 103.
    Ghoneum, M., Ghoneum, A., and Gimzewski, J. (2010) Nanodiamond and nanoplatinum liquid, DPV576, activates human monocyte-derived dendritic cells in vitro, Anticancer Res., 30, 4075–4079.PubMedGoogle Scholar
  104. 104.
    Zheng, D.-W, Chen, J.-L., Zhu, J.-Y., Rong, L., Li, B., Lei, Q., Fan, J.-X, Zou, M.-Z., Li, C., Cheng, S.-X., Xu, Z., and Zhang, X.-Z. (2016) Highly integrated nano-plat-form for breaking the barrier between chemotherapy and immunotherapy, Nano Lett., 16, 4341–4347, doi: 10.1021/acs.nanolett.6b01432.CrossRefPubMedGoogle Scholar
  105. 105.
    Manish, M., Rahi, A., Kaur, M., Bhatnagar, R., and Singh, S. (2013) A single-dose PLGA encapsulated protective antigen domain 4 nanoformulation protects mice against Bacillus anthracis spore challenge, PLoS One, 8, e61885, doi: 10.1371/journal.pone.0061885.CrossRefPubMedPubMedCentralGoogle Scholar
  106. 106.
    Guha, M. (2012) Anticancer LLR agonists on the ropes, Nat. Rev. DrugDiscov., 11, 503–505, doi: 10.1038/nrd3775.CrossRefGoogle Scholar
  107. 107.
    Lin, A. Y., Almeida, J. P., Bear, A., Liu, N., Luo, L., Foster, A. E., and Drezek, R. A. (2013) Gold nanoparticle delivery of modified CpG stimulates macrophages and inhibits tumor growth for enhanced immunotherapy, PLoS One, 8, e63550, doi: 10.1371/journal.pone.0063550.Google Scholar
  108. 108.
    Zhang, X., Wu, F., Men, K., Huang, R., Zhou, B., Zhang, R., Zou, R., and Yang, L. (2018) Modified Fe3O4 magnetic nanoparticle delivery of CpG inhibits tumor growth and spontaneous pulmonary metastases to enhance immunotherapy, Nanoscale Res. Lett., 13, 240, doi: 10.1186/S11671-018-2661-8.CrossRefPubMedPubMedCentralGoogle Scholar
  109. 109.
    Mejias, R., Perez-Yague, S., Gutierrez, L., Cabrera, L. L., Spada, R., Acedo, P., Serna, C. L., Lazaro, F. J., Villanueva, A., Morales, Mdel, P., and Barber, D. F. (2011) Dimercaptosuccinic acid-coated magnetite nanoparticles for magnetically guided in vivo delivery of interferon gamma for cancer immunotherapy, Biomaterials, 32, 2938–2952, doi: 10.1016/j.biomaterials.2011.01.008.CrossRefPubMedGoogle Scholar
  110. 110.
    Egilmez, N. K., Jong, Y. S., Sabel, M. S., Jacob, J. S., Mathiowitz, E., and Bankert, R. B. (2000) In situ tumor vaccination with interleukin-12-encapsulated biodegradable microspheres: induction of tumor regression and potent antitumor immunity, Cancer Res., 60, 3832–3837.PubMedGoogle Scholar
  111. 111.
    Song, M., Liu, T., Shi, C., Zhang, X., and Chen, X. (2016) Correction to bioconjugated manganese dioxide nanopar-ticles enhance chemotherapy response by priming tumor-associated macrophages toward M1-like phenotype and attenuating tumor hypoxia, ACS Nano, 10, 3872, doi: 10.1021/acsnano.5b06779.CrossRefPubMedPubMedCentralGoogle Scholar
  112. 112.
    Rayahin, J. E., Buhrman, J. S., Zhang, Y., Koh, T. J., and Gemeinhart, R. A. (2015) High and low molecular weight hyaluronic acid differentially influence macrophage activation, ACS Biomater. Sci. Eng., 1, 481–493, doi: 10.1021/acsbiomaterials.5b00181.CrossRefPubMedPubMedCentralGoogle Scholar
  113. 113.
    Alieva, I. B., Kireev, I. I., Garanina, A. S., Alyabyeva, N., Ruyter, A., Strelkova, O. S., Zhironkina, O. A., Cherepaninets, V. D., Majouga, A. G., Davydov, V. A., Khabashesku, V. N., Agafonov, V., and Uzbekov, R. E. (2016) Magnetocontroliability of Fe7C3@C superparamagnetic nanoparticles in living cells, J. Nanobiotechnol., 14, 67–79, doi: 10.1186/sl2951-016-0219-4.CrossRefGoogle Scholar
  114. 114.
    Hattori, Y., Yamashita, J., Sakaida, C., Kawano, K., and Yonemochi, E. (2015) Evaluation of antitumor effect of zoledronic acid entrapped in folate-linked liposome for targeting to tumor-associated macrophages, J. Liposome Res., 25, 131–140, doi: 10.3109/08982104.2014.954128.CrossRefPubMedGoogle Scholar
  115. 115.
    Shmeeda, H., Amitay Y., Tzemach, D., Gorin, J., and Gabizon, A. (2013) Liposome encapsulation of zoledronic acid results in major changes in tissue distribution and increase in toxicity, J. Control. Release, 167, 265–275, doi: 10.1016/j.jconrel.2013.02.003.CrossRefPubMedGoogle Scholar
  116. 116.
    Lang, X., Mo, C., Wang, Y., Wei, D., and Xiao, H. (2013) Anti-tumour strategies aiming to target tumour-associated macrophages, Immunology, 138, 93–104, doi: 10.1111/imm.12023.CrossRefGoogle Scholar
  117. 117.
    Zeng, Y., Ma, L., Zhan, Y., Xu, X, Zeng, Q., Liang, L., and Chen, X. (2018) Hypoxia-activated prodrugs and redox-responsive nanocarriers, Int. J. Nanomedicine, 13, 6551–6574, doi: 10.2147/ijn.sl73431.CrossRefPubMedPubMedCentralGoogle Scholar
  118. 118.
    Andon, F. L., Digifico, E., Maeda, A., Erreni, M., Mantovani, A., Alonso, M. L., and Allavena, P. (2017) Largeting tumor associated macrophages: the new challenge for nanomedicine, Semin. Immunol., 34, 103–113, doi: 10.1016/j.smim.2017.09.004.CrossRefPubMedGoogle Scholar
  119. 119.
    Downey, C. M., Aghaei, M., Schwendener, R. A., and Jirik, F. R. (2014) DMXAA causes tumor site-specific vascular disruption in murine non-small cell lung cancer, and like the endogenous non-canonical cyclic dinucleotide SLING agonist, 2’3’-cGAMR induces M2 macrophage repolarization, PLoS One, 9, e99988, doi: 10.1371/jour-nal.pone.0099988.Google Scholar
  120. 120.
    Jassar, A. S., Suzuki, E., Kapoor, V., Sun, J., Silverberg, M. B., Cheung, L., Burdick, M. D., Strieter, R. M., Ching, L.-M., Kaiser, L. R., and Albelda, S. M. (2005) Activation of tumor-associated macrophages by the vascular disrupting agent 5,6-dimethylxanthenone-4-acetic acid induces an effective CD8+ L-cell-mediated antitumor immune response in murine models of lung cancer and mesothelioma, Cancer Res., 65, 11752–11761, doi: 10.1158/0008-5472.can-05-1658.CrossRefPubMedGoogle Scholar
  121. 121.
    Conlon, L., Burdette, D. L., Sharma, S., Bhat, N., Lhompson, M., Jiang, Z., Rathinam, V. A. K., Monks, B., Jin, L., Xiao, T. S., Vogel, S. N., Vance, R. E., and Fitzgerald, K. A. (2013) Mouse, but not human SLING, binds and signals in response to the vascular disrupting agent 5,6-dimethylxanthenone-4-acetic acid, J. Immunol., 190, 5216–5225, doi: 10.4049/jimmunol.l300097.CrossRefPubMedPubMedCentralGoogle Scholar
  122. 122.
    Binnemars Postma, K., Storm, G., and Prakash, J. (2017) Nanomedicine strategies to target tumor-associated macrophages, Int. J. Mol. Sci., 18, E979, doi: 10.3390/ijmsl8050979.CrossRefPubMedGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2019

Authors and Affiliations

  • K. S. Kapitanova
    • 1
  • V. A. Naumenko
    • 2
    Email author
  • A. S. Garanina
    • 2
  • P. A. Melnikov
    • 3
  • M. A. Abakumov
    • 2
    • 4
  • I. B. Alieva
    • 5
    Email author
  1. 1.Department of Bioengineering and BioinformaticsLomonosov Moscow State UniversityMoscowRussia
  2. 2.National University of Science and Technology “MISIS”MoscowRussia
  3. 3.Serbsky Federal Medical Research Center of Psychiatry and Narcology, Department of Fundamental and Applied NeurobiologyMinistry of Health of the Russian FederationMoscowRussia
  4. 4.Department of Medical NanobiotechnologyRussian National Research Medical UniversityMoscowRussia
  5. 5.A. N. Belozersky Institute of Physico-Chemical BiologyLomonosov Moscow State UniversityMoscowRussia

Personalised recommendations