Drug-free mannosylated liposomes inhibit tumor growth by promoting the polarization of tumor-associated macrophages

References

• Junttila MR, de Sauvage FJ. Influence of tumour micro-environment heterogeneity on therapeutic response. Nature. 2013;501(7467):346–354. doi:10.1038/nature1262624048067
   PubMed Web of Science ®Google Scholar
• Qian BZ, Pollard JW. Macrophage diversity enhances tumor progression and metastasis. Cell. 2010;141(1):39–51. doi:10.1016/j.cell.2010.03.01420371344
   PubMed Web of Science ®Google Scholar
• Mantovani A, Schioppa T, Porta C, Allavena P, Sica A. Role of tumor-associated macrophages in tumor progression and invasion. Cancer Metastasis Rev. 2006;25(3):315–322. doi:10.1007/s10555-006-9001-716967326
   PubMed Web of Science ®Google Scholar
• Komohara Y, Fujiwara Y, Ohnishi K, Takeya M. Tumor-associated macrophages: potential therapeutic targets for anti-cancer therapy. Adv Drug Deliv Rev. 2016;99(Pt B):180–185. doi:10.1016/j.addr.2015.11.00926621196
   PubMed Web of Science ®Google Scholar
• Noy R, Pollard JW. Tumor-associated macrophages: from mechanisms to therapy. Immunity. 2014;41(1):49–61. doi:10.1016/j.immuni.2014.06.01025035953
   PubMed Web of Science ®Google Scholar
• He H, Ghosh S, Yang H. Nanomedicines for dysfunctional macrophage-associated diseases. J Control Release. 2017;247:106–126. doi:10.1016/j.jconrel.2016.12.03228057522
   PubMed Web of Science ®Google Scholar
• Zhang QW, Liu L, Gong CY, et al. Prognostic significance of tumor-associated macrophages in solid tumor: a meta-analysis of the literature. PLoS One. 2012;7(12):e50946. doi:10.1371/journal.pone.005094623284651
   PubMed Web of Science ®Google Scholar
• Bingle L, Brown NJ, Lewis CE. The role of tumour-associated macrophages in tumour progression: implications for new anticancer therapies. J Pathol. 2002;196(3):254–265. doi:10.1002/path.102711857487
   PubMed Web of Science ®Google Scholar
• Komohara Y, Jinushi M, Takeya M. Clinical significance of macrophage heterogeneity in human malignant tumors. Cancer Sci. 2014;105(1):1–8. doi:10.1111/cas.1231424168081
   PubMed Web of Science ®Google Scholar
• Heusinkveld M, van der Burg SH. Identification and manipulation of tumor associated macrophages in human cancers. J Transl Med. 2011;9:216. doi:10.1186/1479-5876-9-21622176642
   PubMed Web of Science ®Google Scholar
• Silva VL, Al-Jamal WT. Exploiting the cancer niche: tumor-associated macrophages and hypoxia as promising synergistic targets for nano-based therapy. J Control Release. 2017;253:82–96. doi:10.1016/j.jconrel.2017.03.01328285930
   PubMed Web of Science ®Google Scholar
• Liu Z, Xiong M, Gong J, et al. Legumain protease-activated TAT-liposome cargo for targeting tumours and their microenvironment. Nat Commun. 2014;5:4280.24969588
   PubMed Web of Science ®Google Scholar
• Zhang X, Tian W, Cai X, et al. Hydrazinocurcumin encapsuled nanoparticles “re-educate” tumor-associated macrophages and exhibit anti-tumor effects on breast cancer following STAT3 suppression. PLoS One. 2013;8(6):e65896. doi:10.1371/journal.pone.006589623825527
   PubMedGoogle Scholar
• Song X, Wan Z, Chen T, et al. Development of a multi-target peptide for potentiating chemotherapy by modulating tumor microenvironment. Biomaterials. 2016;108:44–56. doi:10.1016/j.biomaterials.2016.09.00127619239
   PubMed Web of Science ®Google Scholar
• Piaggio F, Kondylis V, Pastorino F, et al. A novel liposomal Clodronate depletes tumor-associated macrophages in primary and metastatic melanoma: anti-angiogenic and anti-tumor effects. J Control Release. 2016;223:165–177. doi:10.1016/j.jconrel.2015.12.03726742942
   PubMed Web of Science ®Google Scholar
• Yan Z, Wang F, Wen Z, et al. LyP-1-conjugated PEGylated liposomes: a carrier system for targeted therapy of lymphatic metastatic tumor. J Control Release. 2012;157(1):118–125. doi:10.1016/j.jconrel.2011.07.03421827801
   PubMed Web of Science ®Google Scholar
• Tian B, Liu R, Chen S, et al. Mannose-coated gadolinium liposomes for improved magnetic resonance imaging in acute pancreatitis. Int J Nanomedicine. 2017;12:1127–1141. doi:10.2147/IJN.S12329028260882
   PubMed Web of Science ®Google Scholar
• Mukherjee S, Baidoo JNE, Sampat S, et al. Liposomal TriCurin, a synergistic combination of curcumin, epicatechin gallate and resveratrol, repolarizes tumor-associated microglia/ macrophages,and eliminates glioblastoma (GBM) and GBM stem cells. Molecules. 2018;23(1). doi:10.3390/molecules23010201
   PubMed Web of Science ®Google Scholar
• Zhou S, Zhang T, Peng B, et al. Targeted delivery of epirubicin to tumor-associated macrophages by sialic acid-cholesterol conjugate modified liposomes with improved antitumor activity. Int J Pharm. 2017;523(1):203–216. doi:10.1016/j.ijpharm.2017.03.03428336455
   PubMed Web of Science ®Google Scholar
• Chellat F, Merhi Y, Moreau A, Yahia L. Therapeutic potential of nanoparticulate systems for macrophage targeting. Biomaterials. 2005;26(35):7260–7275. doi:10.1016/j.biomaterials.2005.05.04416023200
   PubMed Web of Science ®Google Scholar
• Wang D, Phan N, Isely C, Bruene L, Bratlie KM. Effect of surface modification and macrophage phenotype on particle internalization. Biomacromolecules. 2014;15(11):4102–4110. doi:10.1021/bm501138225268218
   PubMedGoogle Scholar
• Zanganeh S, Hutter G, Spitler R, et al. Iron oxide nanoparticles inhibit tumour growth by inducing pro-inflammatory macrophage polarization in tumour tissues. Nat Nanotechnol. 2016;11(11):986–994. doi:10.1038/nnano.2016.16827668795
   PubMed Web of Science ®Google Scholar
• Pal R, Chakraborty B, Nath A, et al. Noble metal nanoparticle-induced oxidative stress modulates tumor associated macrophages (TAMs) from an M2 to M1 phenotype: an in vitro approach. Int Immunopharmacol. 2016;38:332–341. doi:10.1016/j.intimp.2016.06.00627344639
   PubMed Web of Science ®Google Scholar
• Fuchs AK, Syrovets T, Haas KA, et al. Carboxyl- and amino-functionalized polystyrene nanoparticles differentially affect the polarization profile of M1 and M2 macrophage subsets. Biomaterials. 2016;85:78–87. doi:10.1016/j.biomaterials.2016.01.06426854393
   PubMed Web of Science ®Google Scholar
• Su L, Zhang W, Wu X, et al. Glycocalyx-mimicking nanoparticles for stimulation and polarization of macrophages via specific interactions. Small. 2015;11(33):4191–4200. doi:10.1002/smll.20140383825994111
   PubMed Web of Science ®Google Scholar
• Bygd HC, Forsmark KD, Bratlie KM. Altering in vivo macrophage responses with modified polymer properties. Biomaterials. 2015;56:187–197. doi:10.1016/j.biomaterials.2015.03.04225934291
   PubMed Web of Science ®Google Scholar
• Lunov O, Syrovets T, Loos C, et al. Differential uptake of functionalized polystyrene nanoparticles by human macrophages and a monocytic cell line. ACS Nano. 2011;5(3):1657–1669. doi:10.1021/nn200075621344890
   PubMed Web of Science ®Google Scholar
• Zhang C, Yu X, Gao L, et al. Noninvasive imaging of CD206-positive M2 macrophages as an early biomarker for post-chemotherapy tumor relapse and lymph node metastasis. Theranostics. 2017;7(17):4276–4288. doi:10.7150/thno.2099929158825
   PubMedGoogle Scholar
• Xu Z, Ramishetti S, Tseng YC, Guo S, Wang Y, Huang L. Multifunctional nanoparticles co-delivering Trp2 peptide and CpG adjuvant induce potent cytotoxic T-lymphocyte response against melanoma and its lung metastasis. J Control Release. 2013;172(1):259–265. doi:10.1016/j.jconrel.2013.08.02124004885
   PubMed Web of Science ®Google Scholar
• Tevis KM, Cecchi RJ, Colson YL, Grinstaff MW. Mimicking the tumor microenvironment to regulate macrophage phenotype and assessing chemotherapeutic efficacy in embedded cancer cell/macrophage spheroid models. Acta Biomater. 2017;50:271–279. doi:10.1016/j.actbio.2016.12.03728011141
   PubMed Web of Science ®Google Scholar
• Ruan GX, Chen YZ, Yao XL, et al. Macrophage mannose receptor-specific gene delivery vehicle for macrophage engineering. Acta Biomater. 2014;10(5):1847–1855. doi:10.1016/j.actbio.2014.01.01224440421
   PubMed Web of Science ®Google Scholar
• Keswani RK, Lazebnik M, Pack DW. Intracellular trafficking of hybrid gene delivery vectors. J Control Release. 2015;207:120–130. doi:10.1016/j.jconrel.2015.04.01525883029
   PubMedGoogle Scholar
• Hill AA, Reid Bolus W, Hasty AH. A decade of progress in adipose tissue macrophage biology. Immunol Rev. 2014;262(1):134–152. doi:10.1111/imr.1221625319332
   PubMedGoogle Scholar
• Bilzer M, Roggel F, Gerbes AL. Role of Kupffer cells in host defense and liver disease. Liver Int. 2006;26(10):1175–1186. doi:10.1111/j.1478-3231.2006.01342.x17105582
   PubMed Web of Science ®Google Scholar
• Stahl PD. The macrophage mannose receptor: current status. Am J Respir Cell Mol Biol. 1990;2(4):317–318. doi:10.1165/ajrcmb/2.4.3172182080
   PubMedGoogle Scholar
• Lai C, Li C, Luo X, et al. Use of dual-ligand modification in kupffer cell-targeted liposomes to examine the contribution of kupffer cells to accelerated blood clearance phenomenon. Mol Pharm. 2018;15(7):2548–2558. doi:10.1021/acs.molpharmaceut.8b0004229768009
   PubMedGoogle Scholar
• Zheng H, Li J, Wang M, et al. Exhausting tumor associated macrophages with sialic acid-polyethyleneimine-cholesterol modified liposomal doxorubicin for enhancing sarcoma chemotherapy. Int J Pharm. 2019;558:187–200. doi:10.1016/j.ijpharm.2019.01.00530654062
   PubMedGoogle Scholar
• Mantovani A, Sozzani S, Locati M, Allavena P, Sica A. Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol. 2002;23(11):549–555.12401408
   PubMed Web of Science ®Google Scholar
• Singh Y, Pawar VK, Meher JG, et al. Targeting tumor associated macrophages (TAMs) via nanocarriers. J Control Release. 2017;254:92–106. doi:10.1016/j.jconrel.2017.03.39528377038
   PubMed Web of Science ®Google Scholar
• Sabnani MK, Rajan R, Rowland B, et al. Liposome promotion of tumor growth is associated with angiogenesis and inhibition of antitumor immune responses. Nanomedicine. 2015;11(2):259–262. doi:10.1016/j.nano.2014.08.01025200609
   PubMed Web of Science ®Google Scholar
• Rajan R, Sabnani MK, Mavinkurve V, et al. Liposome-induced immunosuppression and tumor growth is mediated by macrophages and mitigated by liposome-encapsulated alendronate. J Control Release. 2018;271:139–148. doi:10.1016/j.jconrel.2017.12.02329277680
   PubMed Web of Science ®Google Scholar
• Smyth MJ, Ngiow SF, Ribas A, Teng MWL. Combination cancer immunotherapies tailored to the tumour microenvironment. Nat Rev Clin Oncol. 2015;13:143. doi:10.1038/nrclinonc.2015.20926598942
   PubMed Web of Science ®Google Scholar
• Chen D, Xie J, Fiskesund R, et al. Chloroquine modulates antitumor immune response by resetting tumor-associated macrophages toward M1 phenotype. Nat Commun. 2018;9(1):873. doi:10.1038/s41467-018-03225-929491374
   PubMed Web of Science ®Google Scholar
• Bobo D, Robinson KJ, Islam J, Thurecht KJ, Corrie SR. Nanoparticle-based medicines: a review of FDA-approved materials and clinical trials to date. Pharm Res. 2016;33(10):2373–2387. doi:10.1007/s11095-016-1958-527299311
   PubMed Web of Science ®Google Scholar
• Ngambenjawong C, Gustafson HH, Pun SH. Progress in tumor-associated macrophage (TAM)-targeted therapeutics. Adv Drug Deliv Rev. 2017;114:206–221. doi:10.1016/j.addr.2017.04.01028449873
   PubMed Web of Science ®Google Scholar
• Lunov O, Syrovets T, Röcker C, et al. Lysosomal degradation of the carboxydextran shell of coated superparamagnetic iron oxide nanoparticles and the fate of professional phagocytes. Biomaterials. 2010;31(34):9015–9022. doi:10.1016/j.biomaterials.2010.08.00320739059
   PubMed Web of Science ®Google Scholar
• Kuen J, Darowski D, Kluge T, Majety M. Pancreatic cancer cell/fibroblast co-culture induces M2 like macrophages that influence therapeutic response in a 3D model. PLoS One. 2017;12(7):e0182039. doi:10.1371/journal.pone.018203928750018
   PubMedGoogle Scholar
• Leonard F, Curtis LT, Ware MJ, et al. Macrophage polarization contributes to the anti-tumoral efficacy of mesoporous nanovectors loaded with albumin-bound paclitaxel. Front Immunol. 2017;8:693. doi:10.3389/fimmu.2017.0069328670313
   PubMedGoogle Scholar
• Gan J, Dou Y, Li Y, et al. Producing anti-inflammatory macrophages by nanoparticle-triggered clustering of mannose receptors. Biomaterials. 2018;178:95–108. doi:10.1016/j.biomaterials.2018.06.01529920405
   PubMedGoogle Scholar
• Zhang Y, Wu L, Li Z, et al. Glycocalyx-mimicking nanoparticles improve anti-PD-L1 cancer immunotherapy through reversion of tumor-associated macrophages. Biomacromolecules. 2018;19(6):2098–2108. doi:10.1021/acs.biomac.8b0030529634251
   PubMedGoogle Scholar