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Review

The novel target:exosoms derived from M2 macrophage

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Pages 183-196 | Received 30 Apr 2020, Accepted 19 Jul 2020, Published online: 12 Aug 2020

References

  • van Niel G, D'Angelo G, Raposo G. Shedding light on the cell biology of extracellular vesicles. Nat Rev Mol Cell Biol. 2018;19(4):213–228. doi:10.1038/nrm.2017.125.
  • Wolf FI, Wallace J, Franzini-Armstrong C, et al. Biochemical and morphological characterization of a plasma membrane-enriched fraction from bovine parathyroid cells. Arch Biochem Biophys. 1984;232(1):92–101. doi:10.1016/0003-9861(84)90524-1.
  • Harding C, Fau - Heuser J, Heuser Fau - Stahl PJ, et al. Receptor-mediated endocytosis of transferrin and recycling of the transferrin receptor in rat reticulocytes. J Cell Biol. 1983;97(2):329–339. doi:10.1083/jcb.97.2.329.
  • Pan BT, Teng K, Wu C, et al. Electron microscopic evidence for externalization of the transferrin receptor in vesicular form in sheep reticulocytes. J Cell Biol. 1985;101(3):942–948. doi:10.1083/jcb.101.3.942.
  • Johnstone Rm Fau - Adam M, et al. Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J Biol Chem. 1987; 262(19):9412–9420.
  • Tschuschke M, Kocherova I, Bryja A, et al. Inclusion biogenesis, methods of isolation and clinical application of human cellular exosomes. J Clin Med. 2020;9(2):436. doi:10.3390/jcm9020436.
  • Keerthikumar S, Chisanga D, Ariyaratne D, et al. ExoCarta: a web-based compendium of exosomal cargo. J Mol Biol. 2016;428(4):688–692. doi:10.1016/j.jmb.2015.09.019.
  • Raposo G, Nijman HW, Stoorvogel W, et al. B lymphocytes secrete antigen-presenting vesicles. J Exp Med. 1996;183(3):1162–1172.
  • Zitvogel L, Regnault A, Lozier A, et al. Eradication of established murine tumors using a novel cell-free vaccine: dendritic cell-derived exosomes. Nat Med. 1998;4(5):594–600. doi:10.1038/nm0598-594.
  • Baixauli F, López-Otín C, Mittelbrunn M. Exosomes and autophagy: coordinated mechanisms for the maintenance of cellular fitness. Front Immunol. 2014;5:403. doi:10.3389/fimmu.2014.00403.
  • Gu Y, Li M, Wang T, et al. Lactation-related microRNA expression profiles of porcine breast milk exosomes. PLoS One. 2012;7(8):e43691. doi:10.1371/journal.pone.0043691.
  • Hessvik NP, Øverbye A, Brech A, et al. PIKfyve inhibition increases exosome release and induces secretory autophagy. Cell Mol Life Sci. 2016;73(24):4717–4737. doi:10.1007/s00018-016-2309-8.
  • Simhadri VR, Reiners KS, Hansen HP, et al. Dendritic cells release HLA-B-associated transcript-3 positive exosomes to regulate natural killer function. PLoS One. 2008;3(10):e3377. doi:10.1371/journal.pone.0003377.
  • Hessvik NP, Llorente A. Current knowledge on exosome biogenesis and release. Cell Mol Life Sci. 2018;75(2):193–208. doi:10.1007/s00018-017-2595-9.
  • Becker A, Thakur BK, Weiss JM, et al. Extracellular vesicles in cancer: cell-to-cell mediators of metastasis. Cancer Cell. 2016;30(6):836–848. doi:10.1016/j.ccell.2016.10.009.
  • Rahmati S, Shojaei F, Shojaeian A, et al. An overview of current knowledge in biological functions and potential theragnostic applications of exosomes. Chem Phys Lipids. 2020;226:104836.
  • Hanson PI, Cashikar A. Multivesicular body morphogenesis. Annu Rev Cell Dev Biol. 2012;28:337–362. doi:10.1146/annurev-cellbio-092910-154152.
  • Huotari J, Helenius A. Endosome maturation. EMBO J. 2011;30(17):3481–3500. doi:10.1038/emboj.2011.286.
  • Jadli AS, Ballasy N, Edalat P, et al. Inside(sight) of tiny communicator: exosome biogenesis, secretion, and uptake. Mol Cell Biochem. 2020;467(1–2):77–94. doi:10.1007/s11010-020-03703-z.
  • Kalluri RA-OX, LeBleu VA-O. The biology, function, and biomedical applications of exosomes. Science. 2020;367(6478):eaau6977. doi:10.1126/science.aau6977.
  • Colombo M, Moita C, van Niel G, et al. Analysis of ESCRT functions in exosome biogenesis, composition and secretion highlights the heterogeneity of extracellular vesicles. J Cell Sci. 2013;126(Pt 24):5553–5565. doi:10.1242/jcs.128868.
  • Gross JC, Chaudhary V, Bartscherer K, et al. Active Wnt proteins are secreted on exosomes. Nat Cell Biol. 2012; 14(10) :1036–1045. doi:10.1038/ncb2574.
  • Tamai K, Tanaka N, Nakano T, et al. Exosome secretion of dendritic cells is regulated by Hrs, an ESCRT-0 protein. Biochem Biophys Res Commun. 2010;399(3):384–390. doi:10.1016/j.bbrc.2010.07.083.
  • Hoshino D, Kirkbride KC, Costello K, et al. Exosome secretion is enhanced by invadopodia and drives invasive behavior. Cell Rep. 2013;5(5):1159–1168. doi:10.1016/j.celrep.2013.10.050.
  • Babst M, Katzmann DJ, Snyder WB, et al. Endosome-associated complex, ESCRT-II, recruits transport machinery for protein sorting at the multivesicular body. Dev Cell. 2002;3(2):283–289. doi:10.1016/S1534-5807(02)00219-8.
  • Progida C, Malerød L, Stuffers S, et al. RILP is required for the proper morphology and function of late endosomes. J Cell Sci. 2007;120(Pt 21):3729–3737., doi:10.1242/jcs.017301.
  • Wollert T, Wunder C, Lippincott-Schwartz J, et al. Membrane scission by the ESCRT-III complex. Nature. 2009;458(7235):172–177. doi:10.1038/nature07836.
  • Baietti MF, Zhang Z, Mortier E, et al. Syndecan-syntenin-ALIX regulates the biogenesis of exosomes. Nat Cell Biol. 2012;14(7):677–685. doi:10.1038/ncb2502.
  • Friand V, David G, Zimmermann P. Syntenin and syndecan in the biogenesis of exosomes. Biol Cell. 2015;107(10):331–341. doi:10.1111/boc.201500010.
  • Trajkovic K, Hsu C, Chiantia S, et al. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science. 2008;319(5867):1244–1247. doi:10.1126/science.1153124.
  • Stuffers S, Sem Wegner C, Stenmark H, et al. Multivesicular endosome biogenesis in the absence of ESCRTs. Traffic. 2009;10(7):925–937. doi:10.1111/j.1600-0854.2009.00920.x.
  • Rana S, Zöller M. Exosome target cell selection and the importance of exosomal tetraspanins: a hypothesis. Biochem Soc Trans. 2011;39(2):559–562. doi:10.1042/BST0390559.
  • van Niel G, Charrin S, Simoes S, et al. The tetraspanin CD63 regulates ESCRT-independent and -dependent endosomal sorting during melanogenesis. Dev Cell. 2011;21(4):708–721.
  • Hurwitz SN, Nkosi D, Conlon MM, et al. CD63 regulates Epstein-Barr Virus LMP1 exosomal packaging, enhancement of vesicle production, and noncanonical NF-κB signaling. J Virol. 2017;91(5):2216–2251. doi:10.1128/JVI.02251-16.
  • Verweij FJ, van Eijndhoven MAJ, Hopmans ES, et al. LMP1 association with CD63 in endosomes and secretion via exosomes limits constitutive NF-κB activation. EMBO J. 2011;30(11):2115–2129. doi:10.1038/emboj.2011.123.
  • Chairoungdua A, Smith DL, Pochard P, et al. Exosome release of β-catenin: a novel mechanism that antagonizes Wnt signaling. J Cell Biol. 2010;190(6):1079–1091. doi:10.1083/jcb.201002049.
  • Nazarenko I, Rana S, Baumann A, et al. Cell surface tetraspanin Tspan8 contributes to molecular pathways of exosome-induced endothelial cell activation. Cancer Res. 2010;70(4):1668–1678. doi:10.1158/0008-5472.CAN-09-2470.
  • Zhu H, et al. Mutation of SIMPLE in Charcot-Marie-Tooth 1C alters production of exosomes. Mol Biol Cell. 2013;24(11):1619–1637.
  • Ghossoub R, Lembo F, Rubio A, et al. Syntenin-ALIX exosome biogenesis and budding into multivesicular bodies are controlled by ARF6 and PLD2. Nat Commun. 2014;5:3477. doi:10.1038/ncomms4477.
  • Alonso R, Rodríguez MC, Pindado J, et al. Diacylglycerol kinase alpha regulates the secretion of lethal exosomes bearing Fas ligand during activation-induced cell death of T lymphocytes. J Biol Chem. 2005;280(31):28439–28450. doi:10.1074/jbc.M501112200.
  • Zheng B, Zhou J, Wang H. Host microRNAs and exosomes that modulate influenza virus infection. Virus Res. 2020; 279:197885.
  • Primadharsini PP, Nagashima S, Takahashi M, et al. Multivesicular body sorting and the exosomal pathway are required for the release of rat hepatitis E virus from infected cells. Virus Res. 2020;278:197868.
  • Jiang W, Ma P, Deng L, et al. Hepatitis A virus structural protein pX interacts with ALIX and promotes the secretion of virions and foreign proteins through exosome-like vesicles. J Extracell Vesicles. 2020;9(1):1716513.
  • Sampey GC, Saifuddin M, Schwab A, et al. Exosomes from HIV-1-infected cells stimulate production of pro-inflammatory cytokines through trans-activating response (TAR) RNA. J Biol Chem. 2016;291(3):1251–1266. doi:10.1074/jbc.M115.662171.
  • Ye F, Wang Y, He Q, et al. Exosomes Transmit viral genetic information and immune signals may cause immunosuppression and immune tolerance in ALV-J infected HD11 cells. Int J Biol Sci. 2020;16(6):904–920. doi:10.7150/ijbs.35839.
  • Pegtel DM, Cosmopoulos K, Thorley-Lawson DA, et al. Functional delivery of viral miRNAs via exosomes. Proc Natl Acad Sci USA. 2010; 107(14) :6328–6333. doi:10.1073/pnas.0914843107.
  • Urbanelli L, Buratta S, Tancini B, et al. The role of extracellular vesicles in viral infection and transmission. Vaccines (Basel), 2019;7(3):102. doi:10.3390/vaccines7030102.
  • Chen L, Feng Z, Yuan G, et al. HIV-associated exosomes promote infection of Kaposi sarcoma-associated herpesvirus via epidermal growth factor receptor. J Virol. 2020;94(9):1719–1782. doi:10.1128/JVI.01782-19.
  • Arenaccio C, Anticoli S, Manfredi F, et al. Latent HIV-1 is activated by exosomes from cells infected with either replication-competent or defective HIV-1. Retrovirology. 2015;12:87. doi:10.1186/s12977-015-0216-y.
  • Goulielmaki E, Ioannidou A, Tsekrekou M, et al. Tissue-infiltrating macrophages mediate an exosome-based metabolic reprogramming upon DNA damage. Nat Commun. 2020;11(1):42. doi:10.1038/s41467-019-13894-9.
  • Wu J, Dong T, Chen T, et al. Hepatic exosome-derived miR-130a-3p attenuates glucose intolerance via suppressing PHLPP2 gene in adipocyte. Metab Clin Exp. 2020;103:154006. doi:10.1016/j.metabol.2019.154006.
  • Akiyama H, Ide M, Nagatsuka Y, et al. Glucocerebrosidases catalyze a transgalactosylation reaction that yields a newly-identified brain sterol metabolite, galactosylated cholesterol. J Biol Chem. 2020;295(16):5257–5277. doi:10.1074/jbc.RA119.012502.
  • Van Kampen JM, Baranowski DC, Robertson HA, et al. The progressive BSSG rat model of Parkinson's: recapitulating multiple key features of the human disease. PLoS One. 2015;10(10):e0139694. doi:10.1371/journal.pone.0139694.
  • Thomou T, Mori MA, Dreyfuss JM, et al. Adipose-derived circulating miRNAs regulate gene expression in other tissues. Nature. 2017;542(7642):450–455. doi:10.1038/nature21365.
  • Ibáñez F, Montesinos J, Ureña-Peralta JR, et al. TLR4 participates in the transmission of ethanol-induced neuroinflammation via astrocyte-derived extracellular vesicles. J Neuroinflamm. 2019;16(1):136. doi:10.1186/s12974-019-1529-x.
  • Yu H, Sun T, An J, et al. Potential roles of exosomes in Parkinson's disease: from pathogenesis, diagnosis, and treatment to prognosis. Front Cell Dev Biol. 2020;8(8):86. doi:10.3389/fcell.2020.00086.
  • Bliederhaeuser C, Grozdanov V, Speidel A, et al. Age-dependent defects of alpha-synuclein oligomer uptake in microglia and monocytes. Acta Neuropathol. 2016;131(3):379–391. doi:10.1007/s00401-015-1504-2.
  • Graziano F, Bavisotto CC, Gammazza AM, et al. Chaperonology: the third eye on brain gliomas. Brain Sci. 2018;8(6):110.
  • Paolicelli RC, Bergamini G, Rajendran L. Cell-to-cell communication by extracellular vesicles: focus on microglia. Neuroscience. 2019;405:148–157. doi:10.1016/j.neuroscience.2018.04.003.
  • Reilly P, Winston CN, Baron KR, et al. Novel human neuronal tau model exhibiting neurofibrillary tangles and transcellular propagation. Neurobiol Dis. 2017;106:222–234. doi:10.1016/j.nbd.2017.06.005.
  • Achreja A, Meurs N, Nagrath D. Quantifying metabolic transfer mediated by extracellular vesicles using Exo-MFA: an integrated empirical and computational platform. In: Nagrath D, editor. Methods in molecular biology; New York: Humana; 2020. vol. 2088, pp. 205–221.
  • Dini L, Tacconi S, Carata E, et al. Microvesicles and exosomes in metabolic diseases and inflammation. Cytokine Growth Factor Rev. 2020;51:27–39. doi:10.1016/j.cytogfr.2019.12.008.
  • Hou B-R, Jiang C, Wang Z-N, et al. Exosome-mediated crosstalk between microglia and neural stem cells in the repair of brain injury. Neural Regen Res. 2020; 15(6):1023–1024. doi:10.4103/1673-5374.270302.
  • Saeedi S, Israel S, Nagy C, et al. The emerging role of exosomes in mental disorders. Transl Psychiatry. 2019;9(1):122. doi:10.1038/s41398-019-0459-9.
  • Tian Y, Zhu P, Liu S, et al. IL-4-polarized BV2 microglia cells promote angiogenesis by secreting exosomes. Adv Clin Exp Med. 2019;28(4):421–430. doi:10.17219/acem/91826.
  • Yang D, Zhang W, Zhang H, et al. Progress, opportunity, and perspective on exosome isolation - efforts for efficient exosome-based theranostics. Theranostics 2020;10(8):3684–3707. doi:10.7150/thno.41580.
  • Ludwig NA-O, Whiteside TA-O, Reichert TE. Challenges in exosome isolation and analysis in health and disease. Int J Mol Sci. 2019;20(19):4684.
  • Konoshenko MY, Lekchnov EA, Vlassov AV, et al. Isolation of extracellular vesicles: general methodologies and latest trends. Biomed Res Int. 2018;2018:8545347. doi:10.1155/2018/8545347.
  • Yamashita T, Takahashi Y, Takakura Y. Possibility of exosome-based therapeutics and challenges in production of exosomes eligible for therapeutic application. Biol Pharm Bull. 2018;41(6):835–842. doi:10.1248/bpb.b18-00133.
  • Palviainen MA-O, Saari H, Kärkkäinen O, et al. Metabolic signature of extracellular vesicles depends on the cell culture conditions. J Extracell Vesicles. 2019;8(1):1596669.
  • Feng Y, Huang W, Wani M, et al. Ischemic preconditioning potentiates the protective effect of stem cells through secretion of exosomes by targeting Mecp2 via miR-22. PLoS One. 2014;9(2):e88685. doi:10.1371/journal.pone.0088685.
  • Shtam TA, Kovalev RA, Varfolomeeva EY, et al. Exosomes are natural carriers of exogenous siRNA to human cells in vitro. Cell Commun Signal. 2013;11(11):88. doi:10.1186/1478-811X-11-88.
  • Tauber AI. Metchnikoff and the phagocytosis theory. Nat Rev Mol Cell Biol. 2003;4(11):897–901. doi:10.1038/nrm1244.
  • Lan J, Sun L, Xu F, et al. M2 Macrophage-derived exosomes promote cell migration and invasion in colon cancer. Cancer Res. 2019;79(1):146–158. doi:10.1158/0008-5472.CAN-18-0014.
  • Yin Z, Ma T, Huang B, et al. Macrophage-derived exosomal microRNA-501-3p promotes progression of pancreatic ductal adenocarcinoma through the TGFBR3-mediated TGF-β signaling pathway. J Exp Clin Cancer Res. 2019; 38(1):310. doi:10.1186/s13046-019-1313-x.
  • Bai L, Liu Y, Guo K, et al. Ultrasound facilitates naturally equipped exosomes derived from macrophages and blood serum for orthotopic glioma treatment. ACS Appl Mater Interfaces. 2019;11(16):14576–14587. doi:10.1021/acsami.9b00893.
  • Yang F, Wang T, Du P, et al. M2 bone marrow-derived macrophage-derived exosomes shuffle microRNA-21 to accelerate immune escape of glioma by modulating PEG3. Cancer Cell Int. 2020;20:93. doi:10.1186/s12935-020-1163-9.
  • Zheng P, Luo Q, Wang W, et al. Tumor-associated macrophages-derived exosomes promote the migration of gastric cancer cells by transfer of functional Apolipoprotein E. Cell Death Dis. 2018;9(4):434. doi:10.1038/s41419-018-0465-5.
  • Zheng P, Chen L, Yuan X, et al. Exosomal transfer of tumor-associated macrophage-derived miR-21 confers cisplatin resistance in gastric cancer cells. J Exp Clin Cancer Res. 2017;36(1):53. doi:10.1186/s13046-017-0528-y.
  • Chuang H-Y, Su Y-k, Liu H-W, et al. Preclinical evidence of STAT3 inhibitor pacritinib overcoming temozolomide resistance via downregulating miR-21-enriched exosomes from M2 glioblastoma-associated macrophages. J Clin Med. 2019;8(7):959. doi:10.3390/jcm8070959.
  • Wang T, Gilkes DM, Takano N, et al. Hypoxia-inducible factors and RAB22A mediate formation of microvesicles that stimulate breast cancer invasion and metastasis. Proc Natl Acad Sci USA. 2014;111(31):3234–3242.
  • Kosaka N, Iguchi H, Hagiwara K, et al. Neutral sphingomyelinase 2 (nSMase2)-dependent exosomal transfer of angiogenic microRNAs regulate cancer cell metastasis. J Biol Chem. 2013;288(15):10849–10859. doi:10.1074/jbc.M112.446831.
  • Zhang W, Zhou X, Yao Q, et al. HIF-1-mediated production of exosomes during hypoxia is protective in renal tubular cells. Am J Physiol Renal Physiol. 2017;313(4):906–913.
  • Hackenbeck T, Huber R, Schietke R, et al. The GTPase RAB20 is a HIF target with mitochondrial localization mediating apoptosis in hypoxia. Biochim Biophys Acta. 2011;1813(1):1–13. doi:10.1016/j.bbamcr.2010.10.019.
  • Zhu X, Shen H, Yin X, et al. Macrophages derived exosomes deliver miR-223 to epithelial ovarian cancer cells to elicit a chemoresistant phenotype. J Exp Clin Cancer Res. 2019;38(1):81. doi:10.1186/s13046-019-1095-1.
  • Vila-Caballer M, González-Granado JM, Zorita V, et al. Disruption of the CCL1-CCR8 axis inhibits vascular Treg recruitment and function and promotes atherosclerosis in mice. J Mol Cell Cardiol. 2019;132:154–163. doi:10.1016/j.yjmcc.2019.05.009.
  • Yang R, Liao Y, Wang L, et al. Exosomes derived From M2b macrophages attenuate DSS-induced colitis. Front. Immunol. 2019;10:2346.
  • Kuznetsova T, Prange KHM, Glass CK, et al. Transcriptional and epigenetic regulation of macrophages in atherosclerosis. Nat Rev Cardiol. 2020;17(4):216–228. doi:10.1038/s41569-019-0265-3.
  • Wu G, Zhang J, Zhao Q, et al. Molecularly engineered macrophage-derived exosomes with inflammation tropism and intrinsic heme biosynthesis for atherosclerosis treatment. Angew Chem Int Ed Engl. 2020;59(10):4068–4074. doi:10.1002/anie.201913700.
  • Li LC, Kan LD. Traditional Chinese medicine for pulmonary fibrosis therapy: progress and future prospects. J Ethnopharmacol. 2017;198:45–63. doi:10.1016/j.jep.2016.12.042.
  • Yao M-Y, Zhang W-H, Ma W-T, et al. microRNA-328 in exosomes derived from M2 macrophages exerts a promotive effect on the progression of pulmonary fibrosis via FAM13A in a rat model. Exp Mol Med. 2019;51(6):1–16. doi:10.1038/s12276-019-0255-x.
  • Ueshima E, Fujimori M, Kodama H, et al. Macrophage-secreted TGF-β(1) contributes to fibroblast activation and ureteral stricture after ablation injury. Am J Physiol Renal Physiol. 2019;317(1):52–64.
  • Yu X, Odenthal M, Fries JW. Exosomes as miRNA carriers: formation-function-future. Int J Mol Sci. 2016;17(12):2028. doi:10.3390/ijms17122028.
  • Chen J, Zhou R, Liang Y, et al. Blockade of lncRNA-ASLNCS5088-enriched exosome generation in M2 macrophages by GW4869 dampens the effect of M2 macrophages on orchestrating fibroblast activation. FASEB J. 2019;33(11):12200–12212. doi:10.1096/fj.201901610.
  • Dai Y, Wang S, Chang S, et al. M2 macrophage-derived exosomes carry microRNA-148a to alleviate myocardial ischemia/reperfusion injury via inhibiting TXNIP and the TLR4/NF-κB/NLRP3 inflammasome signaling pathway. J Mol Cell Cardiol. 2020;142:65–79. doi:10.1016/j.yjmcc.2020.02.007.
  • Liu D, Zeng X, Li X, et al. Role of NLRP3 inflammasome in the pathogenesis of cardiovascular diseases. Basic Res Cardiol. 2018;113(1):5. doi:10.1007/s00395-017-0663-9.
  • Hamzei Taj S, Kho W, Riou A, et al. MiRNA-124 induces neuroprotection and functional improvement after focal cerebral ischemia. Biomaterials. 2016;91:151–165. doi:10.1016/j.biomaterials.2016.03.025.
  • Ponomarev ED, Veremeyko T, Barteneva N, et al. MicroRNA-124 promotes microglia quiescence and suppresses EAE by deactivating macrophages via the C/EBP-α-PU.1 pathway. Nat Med. 2011;17(1):64–70. doi:10.1038/nm.2266.
  • Zhao S-C, Ma L-S, Chu Z-H, et al. Regulation of microglial activation in stroke. Acta Pharmacol Sin. 2017;38(4):445–458. doi:10.1038/aps.2016.162.
  • Hu X, Li P, Guo Y, et al. Microglia/macrophage polarization dynamics reveal novel mechanism of injury expansion after focal cerebral ischemia. Stroke. 2012;43(11):3063–3070. doi:10.1161/STROKEAHA.112.659656.
  • Song Y, Li Z, He T, et al. M2 microglia-derived exosomes protect the mouse brain from ischemia-reperfusion injury via exosomal miR-124. Theranostics. 2019;9(10):2910–2932. doi:10.7150/thno.30879.
  • Lian S, Xie X, Lu Y, et al. Checkpoint CD47 function on tumor metastasis and immune therapy. Onco Targets Ther. 2019;12:9105–9114. doi:10.2147/OTT.S220196.
  • Liu Y, Zugazagoitia J, Ahmed FS, et al. Immune cell PD-L1 colocalizes with macrophages and is associated with outcome in PD-1 pathway blockade therapy. Clin Cancer Res. 2020;26(4):970–977. doi:10.1158/1078-0432.CCR-19-1040.
  • Villanueva MT. Macrophages get a CAR. Nat Rev Immunol. 2020;20(5):273. doi:10.1038/s41577-020-0302-9.
  • Lu M, Huang Y. Bioinspired exosome-like therapeutics and delivery nanoplatforms. Biomaterials. 2020; 242:119925. doi:10.1016/j.biomaterials.2020.119925.
  • Soularue E, Lepage P, Colombel JF, et al. Enterocolitis due to immune checkpoint inhibitors: a systematic review. Gut. 2018;67(11):2056–2067. doi:10.1136/gutjnl-2018-316948.
  • Spiller KL, Koh TJ. Macrophage-based therapeutic strategies in regenerative medicine. Adv Drug Deliv Rev. 2017;122:74–83. doi:10.1016/j.addr.2017.05.010.
  • Li F, Cheng B, Cheng J, et al. CCR5 blockade promotes M2 macrophage activation and improves locomotor recovery after spinal cord injury in mice. Inflammation. 2015;38(1):126–133. doi:10.1007/s10753-014-0014-z.
  • Döring A, Sloka S, Lau L, et al. Stimulation of monocytes, macrophages, and microglia by amphotericin B and macrophage colony-stimulating factor promotes remyelination. J Neurosci. 2015; 35(3):1136–1148.
  • Mokarram N, Merchant A, Mukhatyar V, et al. Effect of modulating macrophage phenotype on peripheral nerve repair. Biomaterials. 2012;33(34):8793–8801. doi:10.1016/j.biomaterials.2012.08.050.
  • Mirza RE, Fang MM, Weinheimer-Haus EM, et al. Sustained inflammasome activity in macrophages impairs wound healing in type 2 diabetic humans and mice. Diabetes. 2014;63(3):1103–1114. doi:10.2337/db13-0927.
  • Leigh ND, Dunlap GS, Johnson K, et al. Transcriptomic landscape of the blastema niche in regenerating adult axolotl limbs at single-cell resolution. Nat Commun. 2018;9(1):5153. doi:10.1038/s41467-018-07604-0.
  • Furukawa S, Moriyama M, Tanaka A, et al. Preferential M2 macrophages contribute to fibrosis in IgG4-related dacryoadenitis and sialoadenitis, so-called Mikulicz's disease. Clin Immunol. 2015;156(1):9–18. doi:10.1016/j.clim.2014.10.008.
  • Murray PJ, Allen JE, Biswas SK, et al. Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity. 2014;41(1):14–20. doi:10.1016/j.immuni.2014.06.008.
  • Spiller KL, Wrona EA, Romero-Torres S, et al. Differential gene expression in human, murine, and cell line-derived macrophages upon polarization. Exp Cell Res. 2016;347(1):1–13. doi:10.1016/j.yexcr.2015.10.017.
  • Martinez FO, Helming L, Milde R, et al. Genetic programs expressed in resting and IL-4 alternatively activated mouse and human macrophages: similarities and differences. Blood. 2013;121(9):e57. doi:10.1182/blood-2012-06-436212.
  • Maybruck BT, Pfannenstiel LW, Diaz-Montero M, et al. Tumor-derived exosomes induce CD8+ T cell suppressors. J Immunother Cancer. 2017;5(1):65. doi:10.1186/s40425-017-0269-7.
  • Morishita M, Takahashi Y, Matsumoto A, et al. Exosome-based tumor antigens-adjuvant co-delivery utilizing genetically engineered tumor cell-derived exosomes with immunostimulatory CpG DNA. Biomaterials. 2016;111:55–65. doi:10.1016/j.biomaterials.2016.09.031.
  • Fu W, Lei C, Liu S, et al. CAR exosomes derived from effector CAR-T cells have potent antitumour effects and low toxicity. Nat Commun. 2019;10(1):4355. doi:10.1038/s41467-019-12321-3.
  • Safari S, Malekvandfard F, Babashah S, et al. Mesenchymal stem cell-derived exosomes: a novel potential therapeutic avenue for cardiac regeneration. Cell Mol Biol (Noisy-le-grand). 2016;62(7):66–73.
  • Cosenza S, Toupet K, Maumus M, et al. Mesenchymal stem cells-derived exosomes are more immunosuppressive than microparticles in inflammatory arthritis. Theranostics. 2018;8(5):1399–1410. doi:10.7150/thno.21072.
  • Hadla M, Palazzolo S, Corona G, et al. Exosomes increase the therapeutic index of doxorubicin in breast and ovarian cancer mouse models. Nanomedicine (Lond). 2016;11(18):2431–2441. doi:10.2217/nnm-2016-0154.
  • Yang T, Fogarty B, LaForge B, et al. Delivery of small interfering RNA to inhibit vascular endothelial growth factor in zebrafish using natural brain endothelia cell-secreted exosome nanovesicles for the treatment of brain cancer. AAPS J. 2017;19(2):475–486. doi:10.1208/s12248-016-0015-y.
  • Lu M, Xing H, Xun Z, et al. Exosome-based small RNA delivery: progress and prospects. Asian J Pharm Sci. 2018;13(1):1–11. doi:10.1016/j.ajps.2017.07.008.
  • Zhang W, Yu Z-L, Wu M, et al. Magnetic and folate functionalization enables rapid isolation and enhanced tumor-targeting of cell-derived microvesicles. ACS Nano. 2017;11(1):277–290. doi:10.1021/acsnano.6b05630.
  • Pi F, Binzel DW, Lee TJ, et al. Nanoparticle orientation to control RNA loading and ligand display on extracellular vesicles for cancer regression. Nat Nanotechnol. 2018;13(1):82–89. doi:10.1038/s41565-017-0012-z.
  • Lu M, Xing H, Xun Z, et al. Functionalized extracellular vesicles as advanced therapeutic nanodelivery systems. Eur J Pharm Sci. 2018; 121:34–46. doi:10.1016/j.ejps.2018.05.001.
  • Koh E, Lee EJ, Nam G-H, et al. Exosome-SIRPα, a CD47 blockade increases cancer cell phagocytosis. Biomaterials. 2017;121:121–129. doi:10.1016/j.biomaterials.2017.01.004.
  • Kim MS, Haney MJ, Zhao Y, et al. Engineering macrophage-derived exosomes for targeted paclitaxel delivery to pulmonary metastases: in vitro and in vivo evaluations. Nanomedicine. 2018;14(1):195–204. doi:10.1016/j.nano.2017.09.011.
  • Kamerkar S, LeBleu VS, Sugimoto H, et al. Exosomes facilitate therapeutic targeting of oncogenic KRAS in pancreatic cancer. Nature. 2017;546(7659):498–503. doi:10.1038/nature22341.
  • Bellavia D, Raimondo S, Calabrese G, et al. Interleukin 3- receptor targeted exosomes inhibit in vitro and in vivo chronic myelogenous leukemia cell growth. Theranostics. 2017;7(5):1333–1345. doi:10.7150/thno.17092.
  • Besse B, Charrier M, Lapierre V, et al. Dendritic cell-derived exosomes as maintenance immunotherapy after first line chemotherapy in NSCLC. Oncoimmunology. 2016;5(4):e1071008. doi:10.1080/2162402X.2015.1071008.

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