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REVIEW

Advancements in Macrophage-Targeted Drug Delivery for Effective Disease Management

, , ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon
Pages 6915-6940 | Received 09 Aug 2023, Accepted 08 Nov 2023, Published online: 22 Nov 2023

References

  • Davies LC, Jenkins SJ, Allen JE, Taylor PR. Tissue-resident macrophages. Nat Immunol. 2013;14(10):986–995. doi:10.1038/ni.2705
  • Gordon S, Taylor PR. Monocyte and macrophage heterogeneity. Nat Rev Immunol. 2005;5(12):953–964. doi:10.1038/nri1733
  • Ginhoux F, Guilliams M. Tissue-Resident Macrophage Ontogeny and Homeostasis. Immunity. 2016;44(3):439–449. doi:10.1016/j.immuni.2016.02.024
  • Park MD, Silvin A, Ginhoux F, Merad M. Macrophages in health and disease. Cell. 2022;185(23):4259–4279. doi:10.1016/j.cell.2022.10.007
  • Wynn TA, Chawla A, Pollard JW. Macrophage biology in development, homeostasis and disease. Nature. 2013;496(7446):445–455. doi:10.1038/nature12034
  • Murray PJ, Wynn TA. Protective and pathogenic functions of macrophage subsets. Nat Rev Immunol. 2011;11(11):723–737. doi:10.1038/nri3073
  • Martinez FO, Gordon S. The M1 and M2 paradigm of macrophage activation: time for reassessment. F1000prime Rep. 2014;6:13. doi:10.12703/P6-13
  • 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. doi:10.1016/S1471-4906(02)02302-5
  • Fukui S, Iwamoto N, Takatani A, et al. M1 and M2 Monocytes in Rheumatoid Arthritis: a Contribution of Imbalance of M1/M2 Monocytes to Osteoclastogenesis. Front Immunol. 2017;8:1958. doi:10.3389/fimmu.2017.01958
  • Shields CW, Wang LL, Evans MA, Mitragotri S. Materials for Immunotherapy. Adv Mater. 2020;32(13):1901633. doi:10.1002/adma.201901633
  • Jain RK, Martin JD, Stylianopoulos T. The role of mechanical forces in tumor growth and therapy. Annu Rev Biomed Eng. 2014;16:321–346. doi:10.1146/annurev-bioeng-071813-105259
  • Papini E, Tavano R, Mancin F. Opsonins and Dysopsonins of Nanoparticles: facts, Concepts, and Methodological Guidelines. Front Immunol. 2020;11:567365. doi:10.3389/fimmu.2020.567365
  • Zhang YN, Poon W, Tavares AJ, McGilvray ID, Chan WCW. Nanoparticle–liver interactions: cellular uptake and hepatobiliary elimination. J Controlled Release. 2016;240:332–348. doi:10.1016/j.jconrel.2016.01.020
  • Wei X, Ying M, Dehaini D, et al. Nanoparticle Functionalization with Platelet Membrane Enables Multifactored Biological Targeting and Detection of Atherosclerosis. ACS Nano. 2018;12(1):109–116. doi:10.1021/acsnano.7b07720
  • Zhao Y, He Z, Gao H, et al. Fine Tuning of Core–Shell Structure of Hyaluronic Acid/Cell-Penetrating Peptides/siRNA Nanoparticles for Enhanced Gene Delivery to Macrophages in Antiatherosclerotic Therapy. Biomacromolecules. 2018;19(7):2944–2956. doi:10.1021/acs.biomac.8b00501
  • Lee GY, Kim JH, Choi KY, et al. Hyaluronic acid nanoparticles for active targeting atherosclerosis. Biomaterials. 2015;53:341–348. doi:10.1016/j.biomaterials.2015.02.089
  • Poh S, Putt KS, Low PS. Folate-Targeted Dendrimers Selectively Accumulate at Sites of Inflammation in Mouse Models of Ulcerative Colitis and Atherosclerosis. Biomacromolecules. 2017;18(10):3082–3088. doi:10.1021/acs.biomac.7b00728
  • He H, Yuan Q, Bie J, et al. Development of mannose functionalized dendrimeric nanoparticles for targeted delivery to macrophages: use of this platform to modulate atherosclerosis. Transl Res. 2018;193:13–30. doi:10.1016/j.trsl.2017.10.008
  • van Rooijen N, van Kesteren-Hendrikx E. Clodronate liposomes: perspectives in research and therapeutics. J Liposome Res. 2002;12(1–2):81–94. doi:10.1081/lpr-120004780
  • He H, Lu Y, Qi J, Zhu Q, Chen Z, Wu W. Adapting liposomes for oral drug delivery. Acta Pharm Sin B. 2019;9(1):36–48. doi:10.1016/j.apsb.2018.06.005
  • Tenzer S, Docter D, Kuharev J, et al. Rapid formation of plasma protein Corona critically affects nanoparticle pathophysiology. Nat Nanotechnol. 2013;8(10):772–781. doi:10.1038/nnano.2013.181
  • Milani S, Baldelli Bombelli F, Pitek AS, Dawson KA, Rädler J. Reversible versus Irreversible Binding of Transferrin to Polystyrene Nanoparticles: soft and Hard Corona. ACS Nano. 2012;6(3):2532–2541. doi:10.1021/nn204951s
  • Nguyen VH, Lee BJ. Protein Corona: a new approach for nanomedicine design. Int J Nanomedicine. 2017;12:3137–3151. doi:10.2147/IJN.S129300
  • Guan J, Shen Q, Zhang Z, et al. Enhanced immunocompatibility of ligand-targeted liposomes by attenuating natural IgM absorption. Nat Commun. 2018;9(1):2982. doi:10.1038/s41467-018-05384-1
  • Zabielska-Koczywąs K, Lechowski R. The Use of Liposomes and Nanoparticles as Drug Delivery Systems to Improve Cancer Treatment in Dogs and Cats. Molecules. 2017;22(12):2167. doi:10.3390/molecules22122167
  • Lamichhane N, Udayakumar T, D’Souza W, et al. Liposomes: clinical Applications and Potential for Image-Guided Drug Delivery. Molecules. 2018;23(2):288. doi:10.3390/molecules23020288
  • Shaheen SM, Shakil Ahmed FR, Hossen MN, Ahmed M, Amran MS, Ul-Islam MA. Liposome as a Carrier for Advanced Drug Delivery. Pak J Biol Sci. 2006;9(6):1181–1191. doi:10.3923/pjbs.2006.1181.1191
  • Poirier VJ, Thamm DH, Kurzman ID, et al. Liposome-Encapsulated Doxorubicin (Doxil) and Doxorubicin in the Treatment of Vaccine-Associated Sarcoma in Cats. J Vet Intern Med. 2002;16(6):726–731. doi:10.1111/j.1939-1676.2002.tb02415.x
  • Walkey CD, Olsen JB, Guo H, Emili A, Chan WCW. Nanoparticle size and surface chemistry determine serum protein adsorption and macrophage uptake. J Am Chem Soc. 2012;134(4):2139–2147. doi:10.1021/ja2084338
  • Schöttler S, Becker G, Winzen S, et al. Protein adsorption is required for stealth effect of poly(ethylene glycol)- and poly(phosphoester)-coated nanocarriers. Nat Nanotechnol. 2016;11(4):372–377. doi:10.1038/nnano.2015.330
  • Cao H, Dan Z, He X, et al. Liposomes Coated with Isolated Macrophage Membrane Can Target Lung Metastasis of Breast Cancer. ACS Nano. 2016;10(8):7738–7748. doi:10.1021/acsnano.6b03148
  • He H, Guo C, Wang J, et al. Leutusome: a Biomimetic Nanoplatform Integrating Plasma Membrane Components of Leukocytes and Tumor Cells for Remarkably Enhanced Solid Tumor Homing. Nano Lett. 2018;18(10):6164–6174. doi:10.1021/acs.nanolett.8b01892
  • Belhadj Z, He B, Deng H, et al. A combined “eat me/don’t eat me” strategy based on extracellular vesicles for anticancer nanomedicine. J Extracell Vesicles. 2020;9(1):1806444. doi:10.1080/20013078.2020.1806444
  • Tang Y, Wang X, Li J, et al. Overcoming the Reticuloendothelial System Barrier to Drug Delivery with a “Don’t-Eat-Us” Strategy. ACS Nano. 2019;13(11):13015–13026. doi:10.1021/acsnano.9b05679
  • Tsoi KM, MacParland SA, Ma XZ, et al. Mechanism of hard-nanomaterial clearance by the liver. Nat Mater. 2016;15(11):1212–1221. doi:10.1038/nmat4718
  • Cheng L, Niu MM, Yan T, et al. Bioresponsive micro-to-nano albumin-based systems for targeted drug delivery against complex fungal infections. Acta Pharm Sin B. 2021;11(10):3220–3230. doi:10.1016/j.apsb.2021.04.020
  • Wang W, Zhou X, Bian Y, et al. Dual-targeting nanoparticle vaccine elicits a therapeutic antibody response against chronic hepatitis B. Nat Nanotechnol. 2020;15(5):406–416. doi:10.1038/s41565-020-0648-y
  • Son H, Choi HS, Baek SE, et al. Shear stress induces monocyte/macrophage-mediated inflammation by upregulating cell-surface expression of heat shock proteins. Biomed Pharmacother. 2023;161:114566. doi:10.1016/j.biopha.2023.114566
  • Yazdimamaghani M, Barber ZB, Hadipour Moghaddam SP, Ghandehari H. Influence of Silica Nanoparticle Density and Flow Conditions on Sedimentation, Cell Uptake, and Cytotoxicity. Mol Pharm. 2018;15(6):2372–2383. doi:10.1021/acs.molpharmaceut.8b00213
  • Steinbach EC, Plevy SE. The Role of Macrophages and Dendritic Cells in the Initiation of Inflammation in IBD. Inflamm Bowel Dis. 2014;20(1):166–175. doi:10.1097/MIB.0b013e3182a69dca
  • Singh R, Mishra MK, Aggarwal H. Inflammation, Immunity, and Cancer. Mediators Inflamm. 2017;2017:1. doi:10.1155/2017/6027305
  • Qie Y, Yuan H, von Roemeling CA, et al. Surface modification of nanoparticles enables selective evasion of phagocytic clearance by distinct macrophage phenotypes. Sci Rep. 2016;6(1):26269. doi:10.1038/srep26269
  • Schultze JL, Schmidt SV. Molecular features of macrophage activation. Semin Immunol. 2015;27(6):416–423. doi:10.1016/j.smim.2016.03.009
  • Bonilla DL, Bhattacharya A, Sha Y, et al. Autophagy Regulates Phagocytosis by Modulating the Expression of Scavenger Receptors. Immunity. 2013;39(3):537–547. doi:10.1016/j.immuni.2013.08.026
  • Tarique AA, Logan J, Thomas E, Holt PG, Sly PD, Fantino E. Phenotypic, Functional, and Plasticity Features of Classical and Alternatively Activated Human Macrophages. Am J Respir Cell Mol Biol. 2015;53(5):676–688. doi:10.1165/rcmb.2015-0012OC
  • Verreck FAW, de Boer T, Langenberg DML, et al. Human IL-23-producing type 1 macrophages promote but IL-10-producing type 2 macrophages subvert immunity to (myco)bacteria. Proc Natl Acad Sci. 2004;101(13):4560–4565. doi:10.1073/pnas.0400983101
  • Verreck FAW, de Boer T, Langenberg DML, van der Zanden L, Ottenhoff THM. Phenotypic and functional profiling of human proinflammatory type-1 and anti-inflammatory type-2 macrophages in response to microbial antigens and IFN-γ- and CD40L-mediated costimulation. J Leukoc Biol. 2005;79(2):285–293. doi:10.1189/jlb.0105015
  • Jaguin M, Houlbert N, Fardel O, Lecureur V. Polarization profiles of human M-CSF-generated macrophages and comparison of M1-markers in classically activated macrophages from GM-CSF and M-CSF origin. Cell Immunol. 2013;281(1):51–61. doi:10.1016/j.cellimm.2013.01.010
  • Schraufstatter IU, Zhao M, Khaldoyanidi SK, DiScipio RG. The chemokine CCL18 causes maturation of cultured monocytes to macrophages in the M2 spectrum: macrophage maturation by CCL18. Immunology. 2012;135(4):287–298. doi:10.1111/j.1365-2567.2011.03541.x
  • Vogel DYS, Glim JE, Stavenuiter AWD, et al. Human macrophage polarization in vitro: maturation and activation methods compared. Immunobiology. 2014;219(9):695–703. doi:10.1016/j.imbio.2014.05.002
  • Lee A, Septiadi D, Taladriz‐Blanco P, et al. Particle Stiffness and Surface Topography Determine Macrophage‐Mediated Removal of Surface Adsorbed Particles. Adv Healthc Mater. 2021;10(6):2001667. doi:10.1002/adhm.202001667
  • Mitchell LA, Lauer FT, Burchiel SW, McDonald JD. Mechanisms for how inhaled multiwalled carbon nanotubes suppress systemic immune function in mice. Nat Nanotechnol. 2009;4(7):451–456. doi:10.1038/nnano.2009.151
  • Kelly C, Jefferies C, Cryan SA. Targeted Liposomal Drug Delivery to Monocytes and Macrophages. J Drug Deliv. 2011;2011:1–11. doi:10.1155/2011/727241
  • 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.2017.04.010
  • Tabata Y, Ikada Y. Effect of the size and surface charge of polymer microspheres on their phagocytosis by macrophage. Biomaterials. 1988;9(4):356–362. doi:10.1016/0142-9612(88)90033-6
  • Inadomi JM, Vijan S, Janz NK, et al. Adherence to colorectal cancer screening: a randomized clinical trial of competing strategies. Arch Intern Med. 2012;172(7):575–582. doi:10.1001/archinternmed.2012.332
  • 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. 2010;31(13):3657–3666. doi:10.1016/j.biomaterials.2010.01.065
  • Yue H, Wei W, Yue Z, et al. Particle size affects the cellular response in macrophages. Eur J Pharm Sci. 2010;41(5):650–657. doi:10.1016/j.ejps.2010.09.006
  • Kuhn DA, Vanhecke D, Michen B, et al. Different endocytotic uptake mechanisms for nanoparticles in epithelial cells and macrophages. Beilstein J Nanotechnol. 2014;5:1625–1636. doi:10.3762/bjnano.5.174
  • Gustafson HH, Holt-Casper D, Grainger DW, Ghandehari H. Nanoparticle uptake: the phagocyte problem. Nano Today. 2015;10(4):487–510. doi:10.1016/j.nantod.2015.06.006
  • Champion JA, Mitragotri S. Role of target geometry in phagocytosis. Proc Natl Acad Sci. 2006;103(13):4930–4934. doi:10.1073/pnas.0600997103
  • Champion JA, Walker A, Mitragotri S. Role of Particle Size in Phagocytosis of Polymeric Microspheres. Pharm Res. 2008;25(8):1815–1821. doi:10.1007/s11095-008-9562-y
  • Champion JA, Mitragotri S. Shape Induced Inhibition of Phagocytosis of Polymer Particles. Pharm Res. 2009;26(1):244–249. doi:10.1007/s11095-008-9626-z
  • Garapaty A, Champion JA. Tunable particles alter macrophage uptake based on combinatorial effects of physical properties: garapaty and Champion. Bioeng Transl Med. 2017;2(1):92–101. doi:10.1002/btm2.10047
  • Albanese A, Tang PS, Chan WCW. The Effect of Nanoparticle Size, Shape, and Surface Chemistry on Biological Systems. Annu Rev Biomed Eng. 2012;14(1):1–16. doi:10.1146/annurev-bioeng-071811-150124
  • Kinnear C, Moore TL, Rodriguez-Lorenzo L, Rothen-Rutishauser B, Petri-Fink A. Form Follows Function: nanoparticle Shape and Its Implications for Nanomedicine. Chem Rev. 2017;117(17):11476–11521. doi:10.1021/acs.chemrev.7b00194
  • Anselmo AC, Mitragotri S. Impact of particle elasticity on particle-based drug delivery systems. Adv Drug Deliv Rev. 2017;108:51–67. doi:10.1016/j.addr.2016.01.007
  • Palomba R, Palange AL, Rizzuti IF, et al. Modulating Phagocytic Cell Sequestration by Tailoring Nanoconstruct Softness. ACS Nano. 2018;12(2):1433–1444. doi:10.1021/acsnano.7b07797
  • de Castro CE, Ribeiro CAS, Alavarse AC, et al. Nanoparticle–Cell Interactions: surface Chemistry Effects on the Cellular Uptake of Biocompatible Block Copolymer Assemblies. Langmuir. 2018;34(5):2180–2188. doi:10.1021/acs.langmuir.7b04040
  • Verma A, Stellacci F. Effect of Surface Properties on Nanoparticle–Cell Interactions. Small. 2010;6(1):12–21. doi:10.1002/smll.200901158
  • Rattan R, Bhattacharjee S, Zong H, et al. Nanoparticle-macrophage interactions: a balance between clearance and cell-specific targeting. Bioorg Med Chem. 2017;25(16):4487–4496. doi:10.1016/j.bmc.2017.06.040
  • 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/nn2000756
  • Liu X, Huang N, Li H, Jin Q, Ji J. Surface and Size Effects on Cell Interaction of Gold Nanoparticles with Both Phagocytic and Nonphagocytic Cells. Langmuir. 2013;29(29):9138–9148. doi:10.1021/la401556k
  • Szolnoky G, Bata-Csörgö Z, Kenderessy AS, et al. A Mannose-Binding Receptor is Expressed on Human Keratinocytes and Mediates Killing of Candida albicans. J Invest Dermatol. 2001;117(2):205–213. doi:10.1046/j.1523-1747.2001.14071.x
  • Scodeller P, Simón-Gracia L, Kopanchuk S, et al. Precision Targeting of Tumor Macrophages with a CD206 Binding Peptide. Sci Rep. 2017;7(1):14655. doi:10.1038/s41598-017-14709-x
  • Jaynes JM, Sable R, Ronzetti M, et al. Mannose receptor (CD206) activation in tumor-associated macrophages enhances adaptive and innate antitumor immune responses. Sci Transl Med. 2020;12(530):eaax6337. doi:10.1126/scitranslmed.aax6337
  • Parker CC, Bin Salam A, Song PN, et al. Evaluation of a CD206-Targeted Peptide for PET Imaging of Macrophages in Syngeneic Mouse Models of Cancer. Mol Pharm. 2023;20(5):2415–2425. doi:10.1021/acs.molpharmaceut.2c00977
  • Zhan X, Jia L, Niu Y, et al. Targeted depletion of tumour-associated macrophages by an alendronate–glucomannan conjugate for cancer immunotherapy. Biomaterials. 2014;35(38):10046–10057. doi:10.1016/j.biomaterials.2014.09.007
  • Vyas MN, Vyas NK, Quiocho FA. Crystallographic Analysis of the Epimeric and Anomeric Specificity of the Periplasmic Transport/Chemosensory Protein Receptor for D-Glucose and D-Galactose. Biochemistry. 1994;33(16):4762–4768. doi:10.1021/bi00182a003
  • Müller C, Schibli R. Prospects in Folate Receptor-Targeted Radionuclide Therapy. Front Oncol. 2013;3. doi:10.3389/fonc.2013.00249
  • Skytthe MK, Graversen JH, Moestrup SK. Targeting of CD163+ Macrophages in Inflammatory and Malignant Diseases. Int J Mol Sci. 2020;21(15):5497. doi:10.3390/ijms21155497
  • Barclay AN. Signal regulatory protein alpha (SIRPα)/CD47 interaction and function. Curr Opin Immunol. 2009;21(1):47–52. doi:10.1016/j.coi.2009.01.008
  • Tang T, Wei Y, Kang J, et al. Tumor-specific macrophage targeting through recognition of retinoid X receptor beta. J Controlled Release. 2019;301:42–53. doi:10.1016/j.jconrel.2019.03.009
  • Ngambenjawong C, Gustafson HH, Pineda JM, Kacherovsky NA, Cieslewicz M, Pun SH. Serum Stability and Affinity Optimization of an M2 Macrophage-Targeting Peptide (M2pep). Theranostics. 2016;6(9):1403–1414. doi:10.7150/thno.15394
  • Ries CH, Hoves S, Cannarile MA, Rüttinger D. CSF-1/CSF-1R targeting agents in clinical development for cancer therapy. Curr Opin Pharmacol. 2015;23:45–51. doi:10.1016/j.coph.2015.05.008
  • Ries CH, Cannarile MA, Hoves S, et al. Targeting Tumor-Associated Macrophages with Anti-CSF-1R Antibody Reveals a Strategy for Cancer Therapy. Cancer Cell. 2014;25(6):846–859. doi:10.1016/j.ccr.2014.05.016
  • Stafford JH, Hirai T, Deng L, et al. Colony stimulating factor 1 receptor inhibition delays recurrence of glioblastoma after radiation by altering myeloid cell recruitment and polarization. Neuro-Oncol. 2016;18(6):797–806. doi:10.1093/neuonc/nov272
  • Pyonteck SM, Akkari L, Schuhmacher AJ, et al. CSF-1R inhibition alters macrophage polarization and blocks glioma progression. Nat Med. 2013;19(10):1264–1272. doi:10.1038/nm.3337
  • Cannarile MA, Weisser M, Jacob W, Jegg AM, Ries CH, Rüttinger D. Colony-stimulating factor 1 receptor (CSF1R) inhibitors in cancer therapy. J Immunother Cancer. 2017;5(1):53. doi:10.1186/s40425-017-0257-y
  • Matlung HL, Szilagyi K, Barclay NA, van den Berg TK. The CD47-SIRPα signaling axis as an innate immune checkpoint in cancer. Immunol Rev. 2017;276(1):145–164. doi:10.1111/imr.12527
  • Chao MP, Alizadeh AA, Tang C, et al. Anti-CD47 Antibody Synergizes with Rituximab to Promote Phagocytosis and Eradicate Non-Hodgkin Lymphoma. Cell. 2010;142(5):699–713. doi:10.1016/j.cell.2010.07.044
  • Weiskopf K, Ring AM, Ccm H, et al. Engineered SIRPα Variants as Immunotherapeutic Adjuvants to Anticancer Antibodies. Science. 2013;341(6141):88–91. doi:10.1126/science.1238856
  • Chen WC, Kawasaki N, Nycholat CM, et al. Antigen Delivery to Macrophages Using Liposomal Nanoparticles Targeting Sialoadhesin/CD169. PLoS One. 2012;7(6):e39039. doi:10.1371/journal.pone.0039039
  • Al Faraj A, Sultana Shaik A, Afzal S, Al Sayed B, Halwani R. MR imaging and targeting of a specific alveolar macrophage subpopulation in LPS-induced COPD animal model using antibody-conjugated magnetic nanoparticles. Int J Nanomedicine. 2014;1491. doi:10.2147/IJN.S59394
  • Ecker DM, Jones SD, Levine HL. The therapeutic monoclonal antibody market. mAbs. 2015;7(1):9–14. doi:10.4161/19420862.2015.989042
  • Nuhn L, Bolli E, Massa S, et al. Targeting Protumoral Tumor-Associated Macrophages with Nanobody-Functionalized Nanogels through Strain Promoted Azide Alkyne Cycloaddition Ligation. Bioconjug Chem. 2018;29(7):2394–2405. doi:10.1021/acs.bioconjchem.8b00319
  • De Meyer T, Muyldermans S, Depicker A. Nanobody-based products as research and diagnostic tools. Trends Biotechnol. 2014;32(5):263–270. doi:10.1016/j.tibtech.2014.03.001
  • Cieslewicz M, Tang J, Yu JL, et al. Targeted delivery of proapoptotic peptides to tumor-associated macrophages improves survival. Proc Natl Acad Sci. 2013;110(40):15919–15924. doi:10.1073/pnas.1312197110
  • Qian Y, Qiao S, Dai Y, et al. Molecular-Targeted Immunotherapeutic Strategy for Melanoma via Dual-Targeting Nanoparticles Delivering Small Interfering RNA to Tumor-Associated Macrophages. ACS Nano. 2017;11(9):9536–9549. doi:10.1021/acsnano.7b05465
  • Conde J, Bao C, Tan Y, et al. Dual Targeted Immunotherapy via In Vivo Delivery of Biohybrid RNAi-Peptide Nanoparticles to Tumor-Associated Macrophages and Cancer Cells. Adv Funct Mater. 2015;25(27):4183–4194. doi:10.1002/adfm.201501283
  • Ngambenjawong C, Cieslewicz M, Schellinger JG, Pun SH. Synthesis and evaluation of multivalent M2pep peptides for targeting alternatively activated M2 macrophages. J Control Release. 2016;224:103–111. doi:10.1016/j.jconrel.2015.12.057
  • Otvos L, Wade JD. Current challenges in peptide-based drug discovery. Front Chem. 2014;2. doi:10.3389/fchem.2014.00062
  • Song M, Liu T, Shi C, Zhang X, Chen X. Bioconjugated Manganese Dioxide Nanoparticles Enhance Chemotherapy Response by Priming Tumor-Associated Macrophages toward M1-like Phenotype and Attenuating Tumor Hypoxia. ACS Nano. 2016;10(1):633–647. doi:10.1021/acsnano.5b06779
  • Zhu S, Niu M, O’Mary H, Cui Z. Targeting of Tumor-Associated Macrophages Made Possible by PEG-Sheddable, Mannose-Modified Nanoparticles. Mol Pharm. 2013;10(9):3525–3530. doi:10.1021/mp400216r
  • Tang Y, Tang Z, Li P, et al. Precise Delivery of Nanomedicines to M2 Macrophages by Combining “Eat Me/Don’t Eat Me” Signals and Its Anticancer Application. ACS Nano. 2021;15(11):18100–18112. doi:10.1021/acsnano.1c06707
  • Irache JM, Salman HH, Gamazo C, Espuelas S. Mannose-targeted systems for the delivery of therapeutics. Expert Opin Drug Deliv. 2008;5(6):703–724. doi:10.1517/17425247.5.6.703
  • Keefe AD, Pai S, Ellington A. Aptamers as therapeutics. Nat Rev Drug Discov. 2010;9(7):537–550. doi:10.1038/nrd3141
  • Zhou J, Rossi J. Aptamers as targeted therapeutics: current potential and challenges. Nat Rev Drug Discov. 2017;16(3):181–202. doi:10.1038/nrd.2016.199
  • Sylvestre M, Saxby CP, Kacherovsky N, Gustafson H, Salipante SJ, Pun SH. Identification of a DNA Aptamer That Binds to Human Monocytes and Macrophages. Bioconjug Chem. 2020;31(8):1899–1907. doi:10.1021/acs.bioconjchem.0c00247
  • Qian H, Zhou T, Fu Y, et al. Self-assembled tetrahedral framework nucleic acid mediates tumor-associated macrophage reprogramming and restores antitumor immunity. Mol Ther Nucleic Acids. 2022;27:763–773. doi:10.1016/j.omtn.2021.12.036
  • Qian H, Fu Y, Guo M, et al. Dual-aptamer-engineered M1 macrophage with enhanced specific targeting and checkpoint blocking for solid-tumor immunotherapy. Mol Ther. 2022;30(8):2817–2827. doi:10.1016/j.ymthe.2022.04.015
  • Johnston MJW, Semple SC, Klimuk SK, Ansell S, Maurer N, Cullis PR. Characterization of the drug retention and pharmacokinetic properties of liposomal nanoparticles containing dihydrosphingomyelin. Biochim Biophys Acta BBA - Biomembr. 2007;1768(5):1121–1127. doi:10.1016/j.bbamem.2007.01.019
  • Filipczak N, Pan J, Yalamarty SSK, Torchilin VP. Recent advancements in liposome technology. Adv Drug Deliv Rev. 2020;156:4–22. doi:10.1016/j.addr.2020.06.022
  • Tang J, Rakshit M, Chua HM, et al. Liposome interaction with macrophages and foam cells for atherosclerosis treatment: effects of size, surface charge and lipid composition. Nanotechnology. 2021;32(50):505105. doi:10.1088/1361-6528/ac2810
  • Vorselen D. Dynamics of phagocytosis mediated by phosphatidylserine. Biochem Soc Trans. 2022;50(5):1281–1291. doi:10.1042/BST20211254
  • Toita R, Kang JH, Tsuchiya A. Phosphatidylserine liposome multilayers mediate the M1-to-M2 macrophage polarization to enhance bone tissue regeneration. Acta Biomater. 2022;154:583–596. doi:10.1016/j.actbio.2022.10.024
  • Kalluri R, LeBleu VS. The biology, function, and biomedical applications of exosomes. Science. 2020;367(6478):eaau6977. doi:10.1126/science.aau6977
  • Ben XY, Wang YR, Zheng HH, et al. Construction of Exosomes that Overexpress CD47 and Evaluation of Their Immune Escape. Front Bioeng Biotechnol. 2022;10:936951. doi:10.3389/fbioe.2022.936951
  • Szebeni J, Alving CR, Rosivall L, et al. Animal models of complement-mediated hypersensitivity reactions to liposomes and other lipid-based nanoparticles. J Liposome Res. 2007;17(2):107–117. doi:10.1080/08982100701375118
  • Kanlikilicer P, Bayraktar R, Denizli M, et al. Exosomal miRNA confers chemo resistance via targeting Cav1/p-gp/M2-type macrophage axis in ovarian cancer. eBioMedicine. 2018;38:100–112. doi:10.1016/j.ebiom.2018.11.004
  • Yang K, Xiao Q, Niu M, Pan X, Zhu X. Exosomes in atherosclerosis: convergence on macrophages. Int J Biol Sci. 2022;18(8):3266–3281. doi:10.7150/ijbs.71862
  • Feng Q, Ma X, Cheng K, et al. Engineered Bacterial Outer Membrane Vesicles as Controllable Two‐Way Adaptors to Activate Macrophage Phagocytosis for Improved Tumor Immunotherapy. Adv Mater. 2022;34(40):2206200. doi:10.1002/adma.202206200
  • Joralemon MJ, McRae S, Emrick T. PEGylated polymers for medicine: from conjugation to self-assembled systems. Chem Commun. 2010;46(9):1377. doi:10.1039/b920570p
  • Kolate A, Baradia D, Patil S, Vhora I, Kore G, Misra A. PEG — a versatile conjugating ligand for drugs and drug delivery systems. J Controlled Release. 2014;192:67–81. doi:10.1016/j.jconrel.2014.06.046
  • Sabzehei F, Taromchi AH, Danafar H, Rashidzadeh H, Ramazani A. In vitro Characterization of Polyethyleneimine–Oleic Acid Cationic Micelle as a Novel Protein Carrier. Adv Biomed Res. 2023;12(1):126. doi:10.4103/abr.abr_303_22
  • Hou Z, Zhou W, Guo X, et al. Poly(ϵ-Caprolactone)-Methoxypolyethylene Glycol (PCL-MPEG)-Based Micelles for Drug-Delivery: the Effect of PCL Chain Length on Blood Components, Phagocytosis, and Biodistribution. Int J Nanomedicine. 2022;17:1613–1632. doi:10.2147/IJN.S349516
  • Klein ME, Rieckmann M, Lucas H, Meister A, Loppnow H, Mäder K. Phosphatidylserine (PS) and phosphatidylglycerol (PG) enriched mixed micelles (MM): a new nano-drug delivery system with anti-inflammatory potential? Eur J Pharm Sci. 2020;152:105451. doi:10.1016/j.ejps.2020.105451
  • Sun JH, Liang X, Cai M, et al. Protein-Crowned Micelles for Targeted and Synergistic Tumor-Associated Macrophage Reprogramming to Enhance Cancer Treatment. Nano Lett. 2022;22(11):4410–4420. doi:10.1021/acs.nanolett.2c00901
  • Liu L, He H, Liang R, et al. ROS-Inducing Micelles Sensitize Tumor-Associated Macrophages to TLR3 Stimulation for Potent Immunotherapy. Biomacromolecules. 2018;19(6):2146–2155. doi:10.1021/acs.biomac.8b00239
  • Lombardo D, Kiselev MA, Caccamo MT. Smart Nanoparticles for Drug Delivery Application: development of Versatile Nanocarrier Platforms in Biotechnology and Nanomedicine. J Nanomater. 2019;2019:1–26. doi:10.1155/2019/3702518
  • Pinelli F, Perale G, Rossi F. Coating and Functionalization Strategies for Nanogels and Nanoparticles for Selective Drug Delivery. Gels. 2020;6(1):6. doi:10.3390/gels6010006
  • Chenthamara D, Subramaniam S, Ramakrishnan SG, et al. Therapeutic efficacy of nanoparticles and routes of administration. Biomater Res. 2019;23(1):20. doi:10.1186/s40824-019-0166-x
  • Fu X, Bai H, Lyu F, Liu L, Wang S. Conjugated Polymer Nanomaterials for Phototherapy of Cancer. Chem Res Chin Univ. 2020;36(2):237–242. doi:10.1007/s40242-020-0012-7
  • Li S, Wang X, Hu R, et al. Near-Infrared (NIR)-Absorbing Conjugated Polymer Dots as Highly Effective Photothermal Materials for In Vivo Cancer Therapy. Chem Mater. 2016;28(23):8669–8675. doi:10.1021/acs.chemmater.6b03738
  • Xiong Z, Timokhina I, Pereloma E. Clustering, nano-scale precipitation and strengthening of steels. Prog Mater Sci. 2021;118:100764. doi:10.1016/j.pmatsci.2020.100764
  • 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.2016.01.064
  • Huang YJ, Hung KC, Hung HS, Hsu SH. Modulation of macrophage phenotype by biodegradable polyurethane nanoparticles: the possible relation between macrophage polarization and immune response of nanoparticles. ACS Appl Mater Interfaces. 2018;10(23):19436–19448. doi:10.1021/acsami.8b04718
  • 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.2016.168
  • Jin R, Liu L, Zhu W, et al. Iron oxide nanoparticles promote macrophage autophagy and inflammatory response through activation of toll-like Receptor-4 signaling. Biomaterials. 2019;203:23–30. doi:10.1016/j.biomaterials.2019.02.026
  • Chen L, Ma X, Dang M, et al. Simultaneous T Cell Activation and Macrophage Polarization to Promote Potent Tumor Suppression by Iron Oxide‐Embedded Large‐Pore Mesoporous Organosilica Core–Shell Nanospheres. Adv Healthc Mater. 2019;8(9):1900039. doi:10.1002/adhm.201900039
  • Guo JC, An Q, Guo M, et al. Oxygen-independent free radical generation mediated by core-shell magnetic nanocomposites synergizes with immune checkpoint blockade for effective primary and metastatic tumor treatment. Nano Today. 2021;36:101024. doi:10.1016/j.nantod.2020.101024
  • Kang H, Kim S, Wong DSH, et al. Remote Manipulation of Ligand Nano-Oscillations Regulates Adhesion and Polarization of Macrophages in Vivo. Nano Lett. 2017;17(10):6415–6427. doi:10.1021/acs.nanolett.7b03405
  • Rojas JM, Sanz-Ortega L, Mulens-Arias V, Gutiérrez L, Pérez-Yagüe S, Barber DF. Superparamagnetic iron oxide nanoparticle uptake alters M2 macrophage phenotype, iron metabolism, migration and invasion. Nanomedicine Nanotechnol Biol Med. 2016;12(4):1127–1138. doi:10.1016/j.nano.2015.11.020
  • Shah A, Dobrovolskaia MA. Immunological effects of iron oxide nanoparticles and iron-based complex drug formulations: therapeutic benefits, toxicity, mechanistic insights, and translational considerations. Nanomedicine Nanotechnol Biol Med. 2018;14(3):977–990. doi:10.1016/j.nano.2018.01.014
  • Yang Y, Tian Q, Wu S, et al. Blue light-triggered Fe2+-release from monodispersed ferrihydrite nanoparticles for cancer iron therapy. Biomaterials. 2021;271:120739. doi:10.1016/j.biomaterials.2021.120739
  • Pazár B, Ea HK, Narayan S, et al. Basic Calcium Phosphate Crystals Induce Monocyte/Macrophage IL-1β Secretion through the NLRP3 Inflammasome In Vitro. J Immunol. 2011;186(4):2495–2502. doi:10.4049/jimmunol.1001284
  • He XY, Liu BY, Xu C, Zhuo RX, Cheng SX. A multi-functional macrophage and tumor targeting gene delivery system for the regulation of macrophage polarity and reversal of cancer immunoresistance. Nanoscale. 2018;10(33):15578–15587. doi:10.1039/C8NR05294H
  • Chang -C-C, Dinh TK, Lee Y-A, et al. Nanoparticle Delivery of MnO2 and Antiangiogenic Therapy to Overcome Hypoxia-Driven Tumor Escape and Suppress Hepatocellular Carcinoma. ACS Appl Mater Interfaces. 2020;12(40):44407–44419. doi:10.1021/acsami.0c08473
  • Zhang X, Tang J, Li C, Lu Y, Cheng L, Liu J. A targeting black phosphorus nanoparticle based immune cells nano-regulator for photodynamic/photothermal and photo-immunotherapy. Bioact Mater. 2021;6(2):472–489. doi:10.1016/j.bioactmat.2020.08.024
  • Yang L, Zhang Y. Tumor-associated macrophages: from basic research to clinical application. J Hematol Oncol. 2017;10(1):58. doi:10.1186/s13045-017-0430-2
  • Nirmala MJ, Kizhuveetil U, Johnson A, B G, Nagarajan R, Muthuvijayan V. Cancer nanomedicine: a review of nano-therapeutics and challenges ahead. RSC Adv. 2023;13(13):8606–8629. doi:10.1039/D2RA07863E
  • Siegel RL, Miller KD, Fuchs HE, Jemal A. Cancer statistics, 2022. CA Cancer J Clin. 2022;72(1):7–33. doi:10.3322/caac.21708
  • Mantovani A, Marchesi F, Malesci A, Laghi L, Allavena P. Tumour-associated macrophages as treatment targets in oncology. Nat Rev Clin Oncol. 2017;14(7):399–416. doi:10.1038/nrclinonc.2016.217
  • Noy R, Pollard JW. Tumor-Associated Macrophages: from Mechanisms to Therapy. Immunity. 2014;41(1):49–61. doi:10.1016/j.immuni.2014.06.010
  • Gustafson HH, Pun SH. Instructing macrophages to fight cancer. Nat Biomed Eng. 2018;2(8):559–561. doi:10.1038/s41551-018-0276-0
  • Andón FT, Digifico E, Maeda A, et al. Targeting tumor associated macrophages: the new challenge for nanomedicine. Semin Immunol. 2017;34:103–113. doi:10.1016/j.smim.2017.09.004
  • DeNardo DG, Ruffell B. Macrophages as regulators of tumour immunity and immunotherapy. Nat Rev Immunol. 2019;19(6):369–382. doi:10.1038/s41577-019-0127-6
  • Leuschner F, Courties G, Dutta P, et al. Silencing of CCR2 in myocarditis. Eur Heart J. 2015;36(23):1478–1488. doi:10.1093/eurheartj/ehu225
  • Hughes R, Qian BZ, Rowan C, et al. Perivascular M2 Macrophages Stimulate Tumor Relapse after Chemotherapy. Cancer Res. 2015;75(17):3479–3491. doi:10.1158/0008-5472.CAN-14-3587
  • Yang Z, Li H, Wang W, et al. CCL2/CCR2 Axis Promotes the Progression of Salivary Adenoid Cystic Carcinoma via Recruiting and Reprogramming the Tumor-Associated Macrophages. Front Oncol. 2019;9:231. doi:10.3389/fonc.2019.00231
  • Xu X, Li R, Dong R, et al. In vitro characterization and cellular uptake profiles of TAMs-targeted lipid calcium carbonate nanoparticles for cancer immunotherapy. Acta Mater Medica. 2022;1(3). doi:10.15212/AMM-2022-0030
  • Barclay AN, van den Berg TK. The Interaction Between Signal Regulatory Protein Alpha (SIRPα) and CD47: structure, Function, and Therapeutic Target. Annu Rev Immunol. 2014;32(1):25–50. doi:10.1146/annurev-immunol-032713-120142
  • Lin ZP, Nguyen LNM, Ouyang B, et al. Macrophages Actively Transport Nanoparticles in Tumors After Extravasation. ACS Nano. 2022;16(4):6080–6092. doi:10.1021/acsnano.1c11578
  • Shime H, Matsumoto M, Oshiumi H, et al. Toll-like receptor 3 signaling converts tumor-supporting myeloid cells to tumoricidal effectors. Proc Natl Acad Sci. 2012;109(6):2066–2071. doi:10.1073/pnas.1113099109
  • Shang Y, Lu H, Liao L, Li S, Xiong H, Yao J. Bioengineered Nanospores Selectively Blocking LC3-Associated Phagocytosis in Tumor-Associated Macrophages Potentiate Antitumor Immunity. ACS Nano. 2023;17(11):10872–10887. doi:10.1021/acsnano.3c02657
  • Pan XF, Wang L, Pan A. Epidemiology and determinants of obesity in China. Lancet Diabetes Endocrinol. 2021;9(6):373–392. doi:10.1016/S2213-8587(21)00045-0
  • Hernandez ED, Lee SJ, Kim JY, et al. A macrophage NBR1-MEKK3 complex triggers JNK-mediated adipose tissue inflammation in obesity. Cell Metab. 2014;20(3):499–511. doi:10.1016/j.cmet.2014.06.008
  • Lumeng CN, Bodzin JL, Saltiel AR. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest. 2007;117(1):175–184. doi:10.1172/JCI29881
  • Su Y, Wang W, Xiao Q, et al. Macrophage membrane-camouflaged lipoprotein nanoparticles for effective obesity treatment based on a sustainable self-reinforcement strategy. Acta Biomater. 2022;152:519–531. doi:10.1016/j.actbio.2022.08.055
  • Zou W, Rohatgi N, Brestoff JR, et al. Myeloid-specific Asxl2 deletion limits diet-induced obesity by regulating energy expenditure. J Clin Invest. 2020;130(5):2644–2656. doi:10.1172/JCI128687
  • Ma L, Liu TW, Wallig MA, et al. Efficient Targeting of Adipose Tissue Macrophages in Obesity with Polysaccharide Nanocarriers. ACS Nano. 2016;10(7):6952–6962. doi:10.1021/acsnano.6b02878
  • Soccio RE. Galectin-3 in NAFLD: therapeutic Target or Noncausal Biomarker? J Clin Endocrinol Metab. 2021;106(9):e3773–e3774. doi:10.1210/clinem/dgab363
  • Devisscher L, Verhelst X, Colle I, Van Vlierberghe H, Geerts A. The role of macrophages in obesity-driven chronic liver disease. J Leukoc Biol. 2016;99(5):693–698. doi:10.1189/jlb.5RU0116-016R
  • Paré A, Mailhot B, Lévesque SA, et al. IL-1β enables CNS access to CCR2 hi monocytes and the generation of pathogenic cells through GM-CSF released by CNS endothelial cells. Proc Natl Acad Sci. 2018;115(6). doi:10.1073/pnas.1714948115
  • Stöger JL, Gijbels MJJ, van der Velden S, et al. Distribution of macrophage polarization markers in human atherosclerosis. Atherosclerosis. 2012;225(2):461–468. doi:10.1016/j.atherosclerosis.2012.09.013
  • Jenne CN, Kubes P. Immune surveillance by the liver. Nat Immunol. 2013;14(10):996–1006. doi:10.1038/ni.2691
  • Tosello-Trampont AC, Landes SG, Nguyen V, Novobrantseva TI, Hahn YS. Kuppfer Cells Trigger Nonalcoholic Steatohepatitis Development in Diet-induced Mouse Model through Tumor Necrosis Factor-α Production. J Biol Chem. 2012;287(48):40161–40172. doi:10.1074/jbc.M112.417014
  • Ngo W, Ahmed S, Blackadar C, et al. Why nanoparticles prefer liver macrophage cell uptake in vivo. Adv Drug Deliv Rev. 2022;185:114238. doi:10.1016/j.addr.2022.114238
  • Ouyang B, Poon W, Zhang YN, et al. The dose threshold for nanoparticle tumour delivery. Nat Mater. 2020;19(12):1362–1371. doi:10.1038/s41563-020-0755-z
  • Kurniawan DW, Jajoriya AK, Dhawan G, et al. Therapeutic inhibition of spleen tyrosine kinase in inflammatory macrophages using PLGA nanoparticles for the treatment of non-alcoholic steatohepatitis. J Controlled Release. 2018;288:227–238. doi:10.1016/j.jconrel.2018.09.004
  • Maradana MR, Yekollu SK, Zeng B, et al. Immunomodulatory liposomes targeting liver macrophages arrest progression of nonalcoholic steatohepatitis. Metabolism. 2018;78:80–94. doi:10.1016/j.metabol.2017.09.002
  • Martínez–Sánchez C, Bassegoda O, Deng H, et al. Therapeutic targeting of adipose tissue macrophages ameliorates liver fibrosis in non-alcoholic fatty liver disease. JHEP Rep. 2023;5(10):100830. doi:10.1016/j.jhepr.2023.100830
  • Maeda H, Ishima Y, Saruwatari J, et al. Nitric oxide facilitates the targeting Kupffer cells of a nano-antioxidant for the treatment of NASH. J Controlled Release. 2022;341:457–474. doi:10.1016/j.jconrel.2021.11.039
  • Song M, Schuschke DA, Zhou Z, et al. Kupffer cell depletion protects against the steatosis, but not the liver damage, induced by marginal-copper, high-fructose diet in male rats. Am J Physiol-Gastrointest Liver Physiol. 2015;308(11):G934–G945. doi:10.1152/ajpgi.00285.2014
  • Traber PG, Zomer E. Therapy of Experimental NASH and Fibrosis with Galectin Inhibitors. PLoS One. 2013;8(12):e83481. doi:10.1371/journal.pone.0083481
  • Akram MS, Pery N, Butler L, et al. Challenges for biosimilars: focus on rheumatoid arthritis. Crit Rev Biotechnol. 2021;41(1):121–153. doi:10.1080/07388551.2020.1830746
  • Ye L, Wen Z, Li Y, et al. Interleukin-10 attenuation of collagen-induced arthritis is associated with suppression of interleukin-17 and retinoid-related orphan receptor γt production in macrophages and repression of classically activated macrophages. Arthritis Res Ther. 2014;16(2):R96. doi:10.1186/ar4544
  • Cutolo M, Campitiello R, Gotelli E, Soldano S. The Role of M1/M2 Macrophage Polarization in Rheumatoid Arthritis Synovitis. Front Immunol. 2022;13:867260. doi:10.3389/fimmu.2022.867260
  • Li S, Su J, Cai W, Liu JX. Nanomaterials Manipulate Macrophages for Rheumatoid Arthritis Treatment. Front Pharmacol. 2021;12:699245. doi:10.3389/fphar.2021.699245
  • Nasra S, Bhatia D, Kumar A. Recent advances in nanoparticle-based drug delivery systems for rheumatoid arthritis treatment. Nanoscale Adv. 2022;4(17):3479–3494. doi:10.1039/D2NA00229A
  • Gomez-Barrena E, Lindroos L, Ceponis A, et al. Cartilage oligomeric matrix protein (COMP) is modified by intra-articular liposomal clodronate in an experimental model of arthritis. Clin Exp Rheumatol. 2006;24(6):622–628.
  • Jain S, Tran TH, Amiji M. Macrophage repolarization with targeted alginate nanoparticles containing IL-10 plasmid DNA for the treatment of experimental arthritis. Biomaterials. 2015;61:162–177. doi:10.1016/j.biomaterials.2015.05.028
  • Yang Y, Guo L, Wang Z, et al. Targeted silver nanoparticles for rheumatoid arthritis therapy via macrophage apoptosis and Re-polarization. Biomaterials. 2021;264:120390. doi:10.1016/j.biomaterials.2020.120390
  • Lu Y, Zhou J, Wang Q, et al. Glucocorticoid-loaded pH/ROS dual-responsive nanoparticles alleviate joint destruction by downregulating the NF-κB signaling pathway. Acta Biomater. 2023;164:458–473. doi:10.1016/j.actbio.2023.04.012
  • Li H, Feng Y, Zheng X, et al. M2-type exosomes nanoparticles for rheumatoid arthritis therapy via macrophage re-polarization. J Controlled Release. 2022;341:16–30. doi:10.1016/j.jconrel.2021.11.019
  • Moore KJ, Sheedy FJ, Fisher EA. Macrophages in atherosclerosis: a dynamic balance. Nat Rev Immunol. 2013;13(10):709–721. doi:10.1038/nri3520
  • Peled M, Fisher EA. Dynamic Aspects of Macrophage Polarization during Atherosclerosis Progression and Regression. Front Immunol. 2014;5. doi:10.3389/fimmu.2014.00579
  • Wang Y, Li L, Zhao W, et al. Targeted Therapy of Atherosclerosis by a Broad-Spectrum Reactive Oxygen Species Scavenging Nanoparticle with Intrinsic Anti-inflammatory Activity. ACS Nano. 2018;12(9):8943–8960. doi:10.1021/acsnano.8b02037
  • Jiang C, Qi Z, Tang Y, et al. Rational Design of Lovastatin-Loaded Spherical Reconstituted High Density Lipoprotein for Efficient and Safe Anti-Atherosclerotic Therapy. Mol Pharm. 2019;16(7):3284–3291. doi:10.1021/acs.molpharmaceut.9b00445
  • Beldman TJ, Senders ML, Alaarg A, et al. Hyaluronan Nanoparticles Selectively Target Plaque-Associated Macrophages and Improve Plaque Stability in Atherosclerosis. ACS Nano. 2017;11(6):5785–5799. doi:10.1021/acsnano.7b01385
  • Yang Q, Jiang H, Wang Y, et al. Plaque Macrophage‐Targeting Nanosystems with Cooperative Co‐Regulation of ROS and TRAF6 for Stabilization of Atherosclerotic Plaques. Adv Funct Mater. 2023;33(28):2301053. doi:10.1002/adfm.202301053
  • Ouimet M, Ediriweera HN, Gundra UM, et al. MicroRNA-33–dependent regulation of macrophage metabolism directs immune cell polarization in atherosclerosis. J Clin Invest. 2015;125(12):4334–4348. doi:10.1172/JCI81676
  • He J, Zhang W, Zhou X, et al. Reactive oxygen species (ROS)-responsive size-reducible nanoassemblies for deeper atherosclerotic plaque penetration and enhanced macrophage-targeted drug delivery. Bioact Mater. 2023;19:115–126. doi:10.1016/j.bioactmat.2022.03.041
  • Gao C, Huang Q, Liu C, et al. Treatment of atherosclerosis by macrophage-biomimetic nanoparticles via targeted pharmacotherapy and sequestration of proinflammatory cytokines. Nat Commun. 2020;11(1):2622. doi:10.1038/s41467-020-16439-7
  • Wang Y, Zhang K, Li T, et al. Macrophage membrane functionalized biomimetic nanoparticles for targeted anti-atherosclerosis applications. Theranostics. 2021;11(1):164–180. doi:10.7150/thno.47841
  • Hu R, Dai C, Dong C, et al. Living Macrophage-Delivered Tetrapod PdH Nanoenzyme for Targeted Atherosclerosis Management by ROS Scavenging, Hydrogen Anti-inflammation, and Autophagy Activation. ACS Nano. 2022;16(10):15959–15976. doi:10.1021/acsnano.2c03422
  • Cordes T, Wallace M, Michelucci A, et al. Immunoresponsive Gene 1 and Itaconate Inhibit Succinate Dehydrogenase to Modulate Intracellular Succinate Levels. J Biol Chem. 2016;291(27):14274–14284. doi:10.1074/jbc.M115.685792
  • Na YR, Stakenborg M, Seok SH, Matteoli G. Macrophages in intestinal inflammation and resolution: a potential therapeutic target in IBD. Nat Rev Gastroenterol Hepatol. 2019;16(9):531–543. doi:10.1038/s41575-019-0172-4
  • Ma WT, Gao F, Gu K, Chen DK. The Role of Monocytes and Macrophages in Autoimmune Diseases: a Comprehensive Review. Front Immunol. 2019;10:1140. doi:10.3389/fimmu.2019.01140
  • Haribhai D, Ziegelbauer J, Jia S, et al. Alternatively Activated Macrophages Boost Induced Regulatory T and Th17 Cell Responses during Immunotherapy for Colitis. J Immunol. 2016;196(8):3305–3317. doi:10.4049/jimmunol.1501956
  • Lissner D, Schumann M, Batra A, et al. Monocyte and M1 Macrophage-induced Barrier Defect Contributes to Chronic Intestinal Inflammation in IBD. Inflamm Bowel Dis. 2015:1. doi:10.1097/MIB.0000000000000384
  • Zhu Y, Li X, Chen J, et al. The pentacyclic triterpene Lupeol switches M1 macrophages to M2 and ameliorates experimental inflammatory bowel disease. Int Immunopharmacol. 2016;30:74–84. doi:10.1016/j.intimp.2015.11.031
  • Song WJ, Li Q, Ryu MO, et al. TSG-6 Secreted by Human Adipose Tissue-derived Mesenchymal Stem Cells Ameliorates DSS-induced colitis by Inducing M2 Macrophage Polarization in Mice. Sci Rep. 2017;7(1):5187. doi:10.1038/s41598-017-04766-7
  • Seo DH, Che X, Kwak MS, et al. Interleukin-33 regulates intestinal inflammation by modulating macrophages in inflammatory bowel disease. Sci Rep. 2017;7(1):851. doi:10.1038/s41598-017-00840-2
  • Huang Z, Gan J, Jia L, et al. An orally administrated nucleotide-delivery vehicle targeting colonic macrophages for the treatment of inflammatory bowel disease. Biomaterials. 2015;48:26–36. doi:10.1016/j.biomaterials.2015.01.013
  • Tannahill GM, Curtis AM, Adamik J, et al. Succinate is an inflammatory signal that induces IL-1β through HIF-1α. Nature. 2013;496(7444):238–242. doi:10.1038/nature11986
  • Hayashi M, Sakata M, Takeda T, et al. Induction of glucose transporter 1 expression through hypoxia-inducible factor 1α under hypoxic conditions in trophoblast-derived cells. J Endocrinol. 2004;183(1):145–154. doi:10.1677/joe.1.05599
  • Herfarth H. IL-10 therapy in Crohn’s disease: at the crossroads. Gut. 2002;50(2):146–147. doi:10.1136/gut.50.2.146
  • Bae YH, Park K. Targeted drug delivery to tumors: myths, reality and possibility. J Controlled Release. 2011;153(3):198–205. doi:10.1016/j.jconrel.2011.06.001