98
Views
0
CrossRef citations to date
0
Altmetric
REVIEW

Macrophage-Targeting DNA Nanomaterials: A Future Direction of Biological Therapy

ORCID Icon, &
Pages 3641-3655 | Received 12 Jan 2024, Accepted 28 Mar 2024, Published online: 22 Apr 2024

References

  • Figueiredo Borgognoni C, Kim JH, Zucolotto V, Fuchs H, Riehemann K. Human macrophage responses to metal-oxide nanoparticles: a review. Artif Cells Nanomed Biotechnol. 2018;46(sup2):694–703. doi:10.1080/21691401.2018.1468767
  • Zhu M, Nie G, Meng H, Xia T, Nel A, Zhao Y. Physicochemical properties determine nanomaterial cellular uptake, transport, and fate. Acc Chem Res. 2013;46(3):622–631. doi:10.1021/ar300031y
  • Elsabahy M, Wooley KL. Cytokines as biomarkers of nanoparticle immunotoxicity. Chem Soc Rev. 2013;42:5552–5576.
  • Martin KE, García AJ. Macrophage phenotypes in tissue repair and the foreign body response: implications for biomaterial-based regenerative medicine strategies. Acta Biomater. 2021;133.
  • Buechler MB, Fu W, Turley SJ. Fibroblast-macrophage reciprocal interactions in health, fibrosis, and cancer. Immunity. 2021;54:903–915.
  • Dukhinova M, Kokinos E, Kuchur P, Komissarov A, Shtro A. Macrophage-derived cytokines in pneumonia: linking cellular immunology and genetics. Cytokine Growth Factor Rev. 2021;59:46–61. doi:10.1016/j.cytogfr.2020.11.003
  • Sellner S, Kocabey S, Nekolla K, Krombach F, Liedl T, Rehberg M. DNA nanotubes as intracellular delivery vehicles in vivo. Biomaterials. 2015;53:453–463. doi:10.1016/j.biomaterials.2015.02.099
  • Maezawa T, Ohtsuki S, Hidaka K, et al. DNA density-dependent uptake of DNA origami-based two-or three-dimensional nanostructures by immune cells. Nanoscale. 2020;12(27):14818–14824. doi:10.1039/D0NR02361B
  • Steinz MM, Ezdoglian A, Khodadust F, et al. Folate Receptor Beta for Macrophage Imaging in Rheumatoid Arthritis. Front Immunol. 2022;13:819163. doi:10.3389/fimmu.2022.819163
  • Pandey RK, Prajapati VK. Molecular and immunological toxic effects of nanoparticles. Int J Biol Macromol. 2018;107:1278–1293. doi:10.1016/j.ijbiomac.2017.09.110
  • Xia K, Kong H, Cui Y, et al. Systematic Study in Mammalian Cells Showing No Adverse Response to Tetrahedral DNA Nanostructure. ACS Appl Mater Interfaces. 2018;10(18):15442–15448. doi:10.1021/acsami.8b02626
  • Mosser DM, Hamidzadeh K, Goncalves R. Macrophages and the maintenance of homeostasis. Cell Mol Immunol. 2021;18(3):579–587. doi:10.1038/s41423-020-00541-3
  • Braga TT, Moura IC, Lepique AP, Camara NOS. Editorial: macrophages Role in Integrating Tissue Signals and Biological Processes in Chronic Inflammation and Fibrosis. Front Immunol. 2017;8:845. doi:10.3389/fimmu.2017.00845
  • Sun J, Sun J, Song B, et al. Fucoidan inhibits CCL22 production through NF-κB pathway in M2 macrophages: a potential therapeutic strategy for cancer. Sci Rep. 2016;6(1):35855. doi:10.1038/srep35855
  • Chen W, Zhang F, Ju Y, Hong J, Ding Y. Gold Nanomaterial Engineering for Macrophage-Mediated Inflammation and Tumor Treatment. Adv Healthc Mater. 2021;10(5):e2000818. doi:10.1002/adhm.202000818
  • Varol C, Mildner A, Jung S. Macrophages: development and tissue specialization. Annu Rev Immunol. 2015;33:643–675.
  • Hu Q, Lyon CJ, Fletcher JK, Tang W, Wan M, Hu TY. Extracellular vesicle activities regulating macrophage- and tissue-mediated injury and repair responses. Acta Pharm Sin B. 2021;11:1493–1512.
  • Placek K, Schultze JL, Aschenbrenner AC. Epigenetic reprogramming of immune cells in injury, repair, and resolution. J Clin Invest. 2019;129(8):2994–3005. doi:10.1172/JCI124619
  • Singer BD, Chandel NS. Immunometabolism of pro-repair cells. J Clin Invest. 2019;129(7):2597–2607. doi:10.1172/JCI124613
  • Watanabe S, Alexander M, Misharin AV, Budinger GRS. The role of macrophages in the resolution of inflammation. J Clin Invest. 2019;129(7):2619–2628. doi:10.1172/JCI124615
  • Conte E. Targeting monocytes/macrophages in fibrosis and cancer diseases: therapeutic approaches. Pharmacol Ther. 2022;234:108031.
  • Yang Q, Guo N, Zhou Y, Chen J, Wei Q, Han M. The role of tumor-associated macrophages (TAMs) in tumor progression and relevant advance in targeted therapy. Acta Pharm Sin B. 2020;10(11):2156–2170. doi:10.1016/j.apsb.2020.04.004
  • D-L S, Z-M L, Shen M-N, Li X, Sun L-Y. Roles of pro- and anti-inflammatory cytokines in the pathogenesis of SLE. J Biomed Biotechnol. 2012;2012:347141.
  • Tang X, Mo C, Wang Y, Wei D, Xiao H. Anti-tumour strategies aiming to target tumour-associated macrophages. Immunology. 2013;138.
  • Kim S-J, Chang HJ, Volin MV, et al. Macrophages are the primary effector cells in IL-7-induced arthritis. Cell Mol Immunol. 2020;17(7):728–740. doi:10.1038/s41423-019-0235-z
  • Udalova IA, Mantovani A, Feldmann M. Macrophage heterogeneity in the context of rheumatoid arthritis. Nat Rev Rheumatol. 2016;12:472–485.
  • Khoury MK, Yang H, Liu B. Macrophage Biology in Cardiovascular Diseases. Arterioscler Thromb Vasc Biol. 2021;41(2):e77–e81. doi:10.1161/ATVBAHA.120.313584
  • Chen W, Schilperoort M, Cao Y, Shi J, Tabas I, Tao W. Macrophage-targeted nanomedicine for the diagnosis and treatment of atherosclerosis. Nat Rev Cardiol. 2022;19:228–249.
  • Koelwyn GJ, Corr EM, Erbay E, Moore KJ. Regulation of macrophage immunometabolism in atherosclerosis. Nat Immunol. 2018;19(6):526–537. doi:10.1038/s41590-018-0113-3
  • Wynn TA, Vannella KM. Macrophages in Tissue Repair, Regeneration, and Fibrosis. Immunity. 2016;44(3):450–462. doi:10.1016/j.immuni.2016.02.015
  • Vannella KM, Wynn TA. Mechanisms of Organ Injury and Repair by Macrophages. Annu Rev Physiol. 2017;79:593–617. doi:10.1093/nar/gkaa341
  • Krenkel O, Tacke F. Liver macrophages in tissue homeostasis and disease. Nat Rev Immunol. 2017;17(5):306–321. doi:10.1038/nri.2017.11
  • Borthwick LA, Barron L, Hart KM, et al. Macrophages are critical to the maintenance of IL-13-dependent lung inflammation and fibrosis. Mucosal Immunol. 2016;9(1):38–55. doi:10.1038/mi.2015.34
  • Henderson NC, Rieder F, Wynn TA. Fibrosis: from mechanisms to medicines. Nature. 2020;587(7835):555–566. doi:10.1038/s41586-020-2938-9
  • Ma W, Zhan Y, Zhang Y, Mao C, Xie X, Lin Y. The biological applications of DNA nanomaterials: current challenges and future directions. Signal Transduct Target Ther. 2021;6:351. doi:10.1038/s41392-021-00727-9
  • Toivari M, Nygård Y, Kumpula E-P, et al. Metabolic engineering of Saccharomyces cerevisiae for bioconversion of D-xylose to D-xylonate. Metab Eng. 2012;14(4):427–436. doi:10.1016/j.ymben.2012.03.002
  • Fu J, Liu M, Liu Y, Yan H. Spatially-interactive biomolecular networks organized by nucleic acid nanostructures. Acc Chem Res. 2012;45(8):1215–1226. doi:10.1021/ar200295q
  • Wang X, Chandrasekaran AR, Shen Z, et al. Paranemic Crossover DNA: there and Back Again. Chem Rev. 2019;119(10):6273–6289. doi:10.1021/acs.chemrev.8b00207
  • Qu Y, Shen F, Zhang Z, et al. Applications of Functional DNA Materials in Immunomodulatory Therapy. ACS Appl Mater Interfaces. 2022;14(40):45079–45095. doi:10.1021/acsami.2c13768
  • Zhang C, Su M, He Y, et al. Conformational flexibility facilitates self-assembly of complex DNA nanostructures. Proc Natl Acad Sci U S A. 2008;105(31):10665–10669. doi:10.1073/pnas.0803841105
  • Hong F, Zhang F, Liu Y, Yan H. DNA Origami: scaffolds for Creating Higher Order Structures. Chem Rev. 2017;117(20):12584–12640. doi:10.1021/acs.chemrev.6b00825
  • Goodman RP, Berry RM, Turberfield AJ. The single-step synthesis of a DNA tetrahedron. Chem Commun. 2004;1372–1373. doi:10.1039/b402293a
  • Zhang L, Zhu G, Mei L, et al. Self-Assembled DNA Immunonanoflowers as Multivalent CpG Nanoagents. ACS Appl Mater Interfaces. 2015;7(43):24069–24074. doi:10.1021/acsami.5b06987
  • Sellner S, Kocabey S, Zhang T, et al. Dexamethasone-conjugated DNA nanotubes as anti-inflammatory agents in vivo. Biomaterials. 2017;134:78–90. doi:10.1016/j.biomaterials.2017.04.031
  • Hu Y, Kahn JS, Guo W, et al. Reversible Modulation of DNA-Based Hydrogel Shapes by Internal Stress Interactions. J Am Chem Soc. 2016;138(49):16112–16119. doi:10.1021/jacs.6b10458
  • Zhang L, Tian XY, Chan CKW, et al. Promoting the Delivery of Nanoparticles to Atherosclerotic Plaques by DNA Coating. ACS Appl Mater Interfaces. 2019;11:13888–13904.
  • Li S, Jiang Q, Liu S, et al. A DNA nanorobot functions as a cancer therapeutic in response to a molecular trigger in vivo. Nat Biotechnol. 2018;36(3):258–264. doi:10.1038/nbt.4071
  • Kwon PS, Ren S, Kwon S-J, et al. Designer DNA architecture offers precise and multivalent spatial pattern-recognition for viral sensing and inhibition. Nat Chem. 2020;12(1):26–35. doi:10.1038/s41557-019-0369-8
  • Koga MM, Comberlato A, Rodríguez-Franco HJ, Bastings MMC. Strategic Insights into Engineering Parameters Affecting Cell Type-Specific Uptake of DNA-Based Nanomaterials. Biomacromolecules. 2022;23:2586–2594. doi:10.1021/acs.biomac.2c00282
  • Liang S, Li J, Zou Z, et al. Tetrahedral DNA nanostructures synergize with MnO2 to enhance antitumor immunity via promoting STING activation and M1 polarization. Acta Pharm Sin B. 2022;12(5):2494–2505. doi:10.1016/j.apsb.2021.12.010
  • Wang C, Yu Y, Irfan M, et al. Rational Design of DNA Framework-Based Hybrid Nanomaterials for Anticancer Drug Delivery. Small. 2020;16(44):e2002578. doi:10.1002/smll.202002578
  • Wang X, Yu J, Lan W, et al. Novel Stable DNA Nanoscale Material and Its Application on Specific Enrichment of DNA. ACS Appl Mater Interfaces. 2020;12(17):19834–19839. doi:10.1021/acsami.0c02242
  • Tian T, Li Y, Lin Y. Prospects and challenges of dynamic DNA nanostructures in biomedical applications. Bone Res. 2022;10(1):40. doi:10.1038/s41413-022-00212-1
  • Schipperges A, Hu Y, Moench S, et al. Formulation of DNA Nanocomposites: towards Functional Materials for Protein Expression. Polymers;2021. 13. doi:10.3390/polym14010013
  • Willem de Vries J, Schnichels S, Hurst J, et al. DNA nanoparticles for ophthalmic drug delivery. Biomaterials;2018. 157. doi:10.1016/j.biomaterials.2018.08.016
  • Hu Y, Niemeyer CM. Designer DNA-silica/carbon nanotube nanocomposites for traceable and targeted drug delivery. J Mater Chem B. 2020;8:2250–2255. doi:10.1039/C9TB02861G
  • Liang L, Li J, Li Q, et al. Single-particle tracking and modulation of cell entry pathways of a tetrahedral DNA nanostructure in live cells. Angew Chem Int Ed Engl. 2014;53(30):7745–7750. doi:10.1002/anie.201403236
  • Choi CHJ, Hao L, Narayan SP, Auyeung E, Mirkin CA. Mechanism for the endocytosis of spherical nucleic acid nanoparticle conjugates. Proc Natl Acad Sci U S A. 2013;110:7625–7630. doi:10.1073/pnas.1305804110
  • Surana S, Bhat JM, Koushika SP, Krishnan Y. An autonomous DNA nanomachine maps spatiotemporal pH changes in a multicellular living organism. Nat Commun. 2011;2(1):340. doi:10.1038/ncomms1340
  • Veetil AT, Zou J, Henderson KW, et al. DNA-based fluorescent probes of NOS2 activity in live brains. Proc Natl Acad Sci U S A. 2020;117(26):14694–14702. doi:10.1073/pnas.2003034117
  • Cui C, Chakraborty K, Tang XA, et al. A lysosome-targeted DNA nanodevice selectively targets macrophages to attenuate tumours. Nat Nanotechnol. 2021;16(12):1394–1402. doi:10.1038/s41565-021-00988-z
  • Allen RJ, Mathew B, Rice KG. PEG-Peptide Inhibition of Scavenger Receptor Uptake of Nanoparticles by the Liver. Mol Pharm. 2018;15(9):3881–3891. doi:10.1021/acs.molpharmaceut.8b00355
  • Ma Y, Lu Z, Jia B, et al. DNA Origami as a Nanomedicine for Targeted Rheumatoid Arthritis Therapy through Reactive Oxygen Species and Nitric Oxide Scavenging. ACS Nano. 2022;16(8):12520–12531. doi:10.1021/acsnano.2c03991
  • Ohtsuki S, Shiba Y, Maezawa T, et al. Folding of single-stranded circular DNA into rigid rectangular DNA accelerates its cellular uptake. Nanoscale. 2019;11(48):23416–23422. doi:10.1039/C9NR08695A
  • Mohri K, Nishikawa M, Takahashi N, et al. Design and development of nanosized DNA assemblies in polypod-like structures as efficient vehicles for immunostimulatory CpG motifs to immune cells. ACS Nano. 2012;6(7):5931–5940. doi:10.1021/nn300727j
  • Takahashi Y, Maezawa T, Araie Y, Takahashi Y, Takakura Y, Nishikawa M. In Vitro and In Vivo Stimulation of Toll-Like Receptor 9 by CpG Oligodeoxynucleotides Incorporated Into Polypod-Like DNA Nanostructures. J Pharm Sci. 2017;106:2457–2462. doi:10.1016/j.xphs.2017.03.028
  • Wang Z, Chu X, Li N, Fu L, Gu H, Zhang N. Engineered DNA nanodrugs alleviate inflammation in inflammatory arthritis. Int J Pharm. 2020;577:119047. doi:10.1016/j.ijpharm.2020.119047
  • Locati M, Curtale G. Diversity, Mechanisms, and Significance of Macrophage Plasticity. Annu Rev Pathol. 2020;15:123–147. doi:10.1146/annurev-pathmechdis-012418-012718
  • Wang W, Xiao D, Lin L, et al. Antifibrotic Effects of Tetrahedral Framework Nucleic Acids by Inhibiting Macrophage Polarization and Macrophage-Myofibroblast Transition in Bladder Remodeling. Adv Healthc Mater;2023. e2203076. doi:10.1002/adhm.202203076
  • Zhang Q, Lin S, Shi S, et al. Anti-inflammatory and Antioxidative Effects of Tetrahedral DNA Nanostructures via the Modulation of Macrophage Responses. ACS Appl Mater Interfaces. 2018;10(4):3421–3430. doi:10.1021/acsami.7b17928
  • Tan X, Sun L, Chen J, Chen ZJ. Detection of Microbial Infections Through Innate Immune Sensing of Nucleic Acids. Annu Rev Microbiol. 2018;72(1):447–478. doi:10.1146/annurev-micro-102215-095605
  • McWhirter SM, Jefferies CA. Nucleic Acid Sensors as Therapeutic Targets for Human Disease. Immunity. 2020;53(1):78–97. doi:10.1016/j.immuni.2020.04.004
  • Krieg AM. Therapeutic potential of Toll-like receptor 9 activation. Nat Rev Drug Discov. 2006;5(6):471–484. doi:10.1038/nrd2059
  • Li J, Pei H, Zhu B, et al. Self-assembled multivalent DNA nanostructures for noninvasive intracellular delivery of immunostimulatory CpG oligonucleotides. ACS Nano. 2011;5(11):8783–8789. doi:10.1021/nn202774x
  • Yang G, Koo JE, Lee HE, Shin SW, Um SH, Lee JY. Immunostimulatory activity of Y-shaped DNA nanostructures mediated through the activation of TLR9. Biomed Pharmacother. 2019;112:108657. doi:10.1016/j.biopha.2019.108657
  • Comberlato A, Koga MM, Nüssing S, Parish IA, Bastings MMC. Spatially Controlled Activation of Toll-like Receptor 9 with DNA-Based Nanomaterials. Nano Lett. 2022;22:2506–2513. doi:10.1021/acs.nanolett.2c00275
  • Woo S-R, Fuertes MB, Corrales L, et al. STING-dependent cytosolic DNA sensing mediates innate immune recognition of immunogenic tumors. Immunity. 2014;41(5):830–842. doi:10.1016/j.immuni.2014.10.017
  • Zhang X, Zhang M, Zhou M, et al. Tetrahedral-Framework Nucleic Acids Carry Small Interfering RNA to Downregulate Toll-Like Receptor 2 Gene Expression for the Treatment of Sepsis. ACS Appl Mater Interfaces. 2022;14(5):6442–6452. doi:10.1021/acsami.1c23708
  • Obuobi S, Julin K, Fredheim EGA, Johannessen M, Škalko-Basnet N. Liposomal delivery of antibiotic loaded nucleic acid nanogels with enhanced drug loading and synergistic anti-inflammatory activity against S. aureus intracellular infections. J Control Release. 2020;324:620–632. doi:10.1016/j.jconrel.2020.06.002
  • Chen Y-F, Chiou Y-H, Chen Y-C, Jiang Y-S, Lee T-Y, Jan J-S. ZnO-loaded DNA nanogels as neutrophil extracellular trap-like structures in the treatment of mouse peritonitis. Mater Sci Eng C Mater Biol Appl. 2021;131:112484. doi:10.1016/j.msec.2021.112484
  • Huang C, You Q, Xu J, et al. An mTOR siRNA-Loaded Spermidine/DNA Tetrahedron Nanoplatform with a Synergistic Anti-Inflammatory Effect on Acute Lung Injury. Adv Healthc Mater. 2022;11(11):e2200008. doi:10.1002/adhm.202200008
  • Greten FR, Grivennikov SI. Inflammation and Cancer: triggers, Mechanisms, and Consequences. Immunity. 2019;51(1):27–41. doi:10.1016/j.immuni.2019.06.025
  • Hou J, Karin M, Sun B. Targeting cancer-promoting inflammation - have anti-inflammatory therapies come of age? Nat Rev Clin Oncol. 2021;18(5):261–279. doi:10.1038/s41571-020-00459-9
  • 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
  • Xiang X, Wang J, Lu D, Xu X. Targeting tumor-associated macrophages to synergize tumor immunotherapy. Signal Transduct Target Ther. 2021;6(1):75. doi:10.1038/s41392-021-00484-9
  • Franch O, Gutiérrez-Corbo C, Domínguez-Asenjo B, et al. DNA flowerstructure co-localizes with human pathogens in infected macrophages. Nucleic Acids Res. 2020;48:6081–6091.
  • Jain S, Tran T-H, 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
  • Chen Z, Bozec A, Ramming A, Schett G. Anti-inflammatory and immune-regulatory cytokines in rheumatoid arthritis. Nat Rev Rheumatol. 2019;15.
  • Zhu J, Zhang M, Gao Y, et al. Tetrahedral framework nucleic acids promote scarless healing of cutaneous wounds via the AKT-signaling pathway. Signal Transduct Target Ther. 2020;5(1):120. doi:10.1038/s41392-020-0173-3
  • Jiang Y, Li S, Zhang T, et al. Tetrahedral Framework Nucleic Acids Inhibit Skin Fibrosis via the Pyroptosis Pathway. ACS Appl Mater Interfaces. 2022;14:15069–15079. doi:10.1021/acsami.2c02877
  • Lee J-W, Chun W, Lee HJ, et al. The Role of Macrophages in the Development of Acute and Chronic Inflammatory Lung Diseases. Cells;2021. 10. doi:10.3390/cells11010010