Generic placeholder image

Current Pharmaceutical Design

Editor-in-Chief

ISSN (Print): 1381-6128
ISSN (Online): 1873-4286

Review Article

Exosomes in Sepsis and Inflammatory Tissue Injury

Author(s): Eun J. Park*, Michael G. Appiah, Phyoe K. Myint, Arong Gaowa, Eiji Kawamoto and Motomu Shimaoka*

Volume 25, Issue 42, 2019

Page: [4486 - 4495] Pages: 10

DOI: 10.2174/1381612825666191116125525

Price: $65

Abstract

Sepsis is the leading cause of death in medical intensive care units, and thus represents a serious healthcare problem worldwide. Sepsis is often caused by the aberrant host responses to infection, which induce dysregulated inflammation that leads to life-threatening multiple organ failures. Mediators such as proinflammatory cytokines that drive the sepsis pathogenesis have been extensively studied. Exosomes, biological lipid bilayer nanoparticles secreted via the endosomal pathway of cells, have recently emerged as important cargos that carry multiple mediators critical for the pathogenesis of sepsis-associated organ dysfunctions. Here we will review current knowledge on the exosomes in sepsis and relevant inflammatory tissue injuries.

Keywords: Sepsis, septic shock, inflammatory tissue injury, exosome, extracellular vesicle, integrin, miRNA

[1]
Raposo G, Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol 2013; 200(4): 373-83.
[http://dx.doi.org/10.1083/jcb.201211138] [PMID: 23420871]
[2]
Hessvik NP, Llorente A. Current knowledge on exosome biogenesis and release. Cell Mol Life Sci 2018; 75(2): 193-208.
[http://dx.doi.org/10.1007/s00018-017-2595-9] [PMID: 28733901]
[3]
Valadi H, Ekström K, Bossios A, Sjöstrand M, Lee JJ, Lötvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 2007; 9(6): 654-9.
[http://dx.doi.org/10.1038/ncb1596] [PMID: 17486113]
[4]
Sun Z, Shi K, Yang S, et al. Effect of exosomal miRNA on cancer biology and clinical applications. Mol Cancer 2018; 17(1): 147.
[http://dx.doi.org/10.1186/s12943-018-0897-7] [PMID: 30309355]
[5]
Villarroya-Beltri C, Gutiérrez-Vázquez C, Sánchez-Cabo F, et al. Sumoylated hnRNPA2B1 controls the sorting of miRNAs into exosomes through binding to specific motifs. Nat Commun 2013; 4: 2980.
[http://dx.doi.org/10.1038/ncomms3980] [PMID: 24356509]
[6]
Villarroya-Beltri C, Baixauli F, Gutiérrez-Vázquez C, Sánchez-Madrid F, Mittelbrunn M. Sorting it out: regulation of exosome loading. Semin Cancer Biol 2014; 28: 3-13.
[http://dx.doi.org/10.1016/j.semcancer.2014.04.009] [PMID: 24769058]
[7]
Guo D, Chen Y, Wang S, et al. Exosomes from heat-stressed tumour cells inhibit tumour growth by converting regulatory T cells to Th17 cells via IL-6. Immunology 2018; 154(1): 132-43.
[http://dx.doi.org/10.1111/imm.12874] [PMID: 29197065]
[8]
Burger D, Viñas JL, Akbari S, et al. Human endothelial colony-forming cells protect against acute kidney injury: role of exosomes. Am J Pathol 2015; 185(8): 2309-23.
[http://dx.doi.org/10.1016/j.ajpath.2015.04.010] [PMID: 26073035]
[9]
Takahashi K, Yan IK, Haga H, Patel T. Modulation of hypoxia-signaling pathways by extracellular linc-RoR. J Cell Sci 2014; 127(Pt 7): 1585-94.
[http://dx.doi.org/10.1242/jcs.141069] [PMID: 24463816]
[10]
Gutwein P, Stoeck A, Riedle S, et al. Cleavage of L1 in exosomes and apoptotic membrane vesicles released from ovarian carcinoma cells. Clin Cancer Res 2005; 11(7): 2492-501.
[http://dx.doi.org/10.1158/1078-0432.CCR-04-1688] [PMID: 15814625]
[11]
Zhang L, Zhang S, Yao J, et al. Microenvironment-induced PTEN loss by exosomal microRNA primes brain metastasis outgrowth. Nature 2015; 527(7576): 100-4.
[http://dx.doi.org/10.1038/nature15376] [PMID: 26479035]
[12]
Costa-Silva B, Aiello NM, Ocean AJ, et al. Pancreatic cancer exosomes initiate pre-metastatic niche formation in the liver. Nat Cell Biol 2015; 17(6): 816-26.
[http://dx.doi.org/10.1038/ncb3169] [PMID: 25985394]
[13]
Lobb RJ, Lima LG, Möller A. Exosomes: key mediators of metastasis and pre-metastatic niche formation. Semin Cell Dev Biol 2017; 67: 3-10.
[http://dx.doi.org/10.1016/j.semcdb.2017.01.004] [PMID: 28077297]
[14]
Liu Y, Cao X. Organotropic metastasis: role of tumor exosomes. Cell Res 2016; 26(2): 149-50.
[http://dx.doi.org/10.1038/cr.2015.153] [PMID: 26704450]
[15]
Fong MY, Zhou W, Liu L, et al. Breast-cancer-secreted miR-122 reprograms glucose metabolism in premetastatic niche to promote metastasis. Nat Cell Biol 2015; 17(2): 183-94.
[http://dx.doi.org/10.1038/ncb3094] [PMID: 25621950]
[16]
Fang T, Lv H, Lv G, et al. Tumor-derived exosomal miR-1247-3p induces cancer-associated fibroblast activation to foster lung metastasis of liver cancer. Nat Commun 2018; 9(1): 191.
[http://dx.doi.org/10.1038/s41467-017-02583-0] [PMID: 29335551]
[17]
Zeng Z, Li Y, Pan Y, et al. Cancer-derived exosomal miR-25-3p promotes pre-metastatic niche formation by inducing vascular permeability and angiogenesis. Nat Commun 2018; 9(1): 5395.
[http://dx.doi.org/10.1038/s41467-018-07810-w] [PMID: 30568162]
[18]
Plebanek MP, Angeloni NL, Vinokour E, et al. Pre-metastatic cancer exosomes induce immune surveillance by patrolling monocytes at the metastatic niche. Nat Commun 2017; 8(1): 1319.
[http://dx.doi.org/10.1038/s41467-017-01433-3] [PMID: 29105655]
[19]
Gao K, Jin J, Huang C, et al. Exosomes derived from septic mouse serum modulate immune responses via exosome-associated cytokines. Front Immunol 2019; 10: 1560.
[http://dx.doi.org/10.3389/fimmu.2019.01560] [PMID: 31354717]
[20]
Kojima M, Gimenes-Junior JA, Chan TW, et al. Exosomes in postshock mesenteric lymph are key mediators of acute lung injury triggering the macrophage activation via Toll-like receptor 4. FASEB J 2018; 32(1): 97-110.
[http://dx.doi.org/10.1096/fj.201700488R] [PMID: 28855278]
[21]
Ulloa L, Brunner M, Ramos L, Deitch EA. Scientific and clinical challenges in sepsis. Curr Pharm Des 2009; 15(16): 1918-35.
[http://dx.doi.org/10.2174/138161209788453248] [PMID: 19519432]
[22]
Mayr FB, Yende S, Angus DC. Epidemiology of severe sepsis. Virulence 2014; 5(1): 4-11.
[http://dx.doi.org/10.4161/viru.27372] [PMID: 24335434]
[23]
Vincent JL, Marshall JC, Namendys-Silva SA, et al. Assessment of the worldwide burden of critical illness: the intensive care over nations (ICON) audit. Lancet Respir Med 2014; 2(5): 380-6.
[http://dx.doi.org/10.1016/S2213-2600(14)70061-X] [PMID: 24740011]
[24]
Bone RC, Balk RA, Cerra FB, et al. The ACCP/SCCM Consensus Conference Committee. American College of Chest Physicians/Society of Critical Care Medicine. Definitions for sepsis and organ failure and guidelines for the use of innovative therapies in sepsis. Chest 1992; 101(6): 1644-55.
[http://dx.doi.org/10.1378/chest.101.6.1644] [PMID: 1303622]
[25]
Shimaoka M, Park EJ. Advances in understanding sepsis. Eur J Anaesthesiol Suppl 2008; 42: 146-53.
[http://dx.doi.org/10.1017/S0265021507003389] [PMID: 18289433]
[26]
Singer M, Deutschman CS, Seymour CW, et al. The Third International Consensus definitions for sepsis and septic shock (sepsis-3). JAMA 2016; 315(8): 801-10.
[http://dx.doi.org/10.1001/jama.2016.0287] [PMID: 26903338]
[27]
Jiao Y, Li Z, Loughran PA, et al. Frontline science: macrophage-derived exosomes promote neutrophil necroptosis following hemorrhagic shock. J Leukoc Biol 2018; 103(2): 175-83.
[PMID: 28801344]
[28]
Merx MW, Weber C. Sepsis and the heart. Circulation 2007; 116(7): 793-802.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.106.678359] [PMID: 17698745]
[29]
Azevedo LC, Janiszewski M, Pontieri V, et al. Platelet-derived exosomes from septic shock patients induce myocardial dysfunction. Crit Care 2007; 11(6): R120.
[http://dx.doi.org/10.1186/cc6176] [PMID: 17996049]
[30]
Gambim MH, do Carmo Ade O, Marti L, Veríssimo-Filho S, Lopes LR, Janiszewski M. Platelet-derived exosomes induce endothelial cell apoptosis through peroxynitrite generation: experimental evidence for a novel mechanism of septic vascular dysfunction. Crit Care 2007; 11(5): R107.
[http://dx.doi.org/10.1186/cc6133] [PMID: 17894858]
[31]
Essandoh K, Yang L, Wang X, et al. Blockade of exosome generation with GW4869 dampens the sepsis-induced inflammation and cardiac dysfunction. Biochim Biophys Acta 2015; 1852(11): 2362-71.
[http://dx.doi.org/10.1016/j.bbadis.2015.08.010] [PMID: 26300484]
[32]
Wang X, Gu H, Qin D, et al. Exosomal miR-223 contributes to mesenchymal stem cell-elicited cardioprotection in polymicrobial sepsis. Sci Rep 2015; 5: 13721.
[http://dx.doi.org/10.1038/srep13721] [PMID: 26348153]
[33]
Englert JA, Bobba C, Baron RM. Integrating molecular pathogenesis and clinical translation in sepsis-induced acute respiratory distress syndrome. JCI Insight 2019; 4(2): 4.
[http://dx.doi.org/10.1172/jci.insight.124061] [PMID: 30674720]
[34]
Zhou Y, Li P, Goodwin AJ, et al. Exosomes from endothelial progenitor cells improve the outcome of a murine model of sepsis. Mol Ther 2018; 26(5): 1375-84.
[http://dx.doi.org/10.1016/j.ymthe.2018.02.020] [PMID: 29599080]
[35]
Chu M, Qin S, Wu R, et al. Role of MiR-126a-3p in endothelial injury in endotoxic mice. Crit Care Med 2016; 44(8): e639-50.
[http://dx.doi.org/10.1097/CCM.0000000000001629] [PMID: 26968021]
[36]
Tang ST, Wang F, Shao M, Wang Y, Zhu HQ. MicroRNA-126 suppresses inflammation in endothelial cells under hyperglycemic condition by targeting HMGB1. Vascul Pharmacol 2017; 88: 48-55.
[http://dx.doi.org/10.1016/j.vph.2016.12.002] [PMID: 27993686]
[37]
Zhou Y, Li P, Goodwin AJ, et al. Exosomes from endothelial progenitor cells improve outcomes of the lipopolysaccharide-induced acute lung injury. Crit Care 2019; 23(1): 44.
[http://dx.doi.org/10.1186/s13054-019-2339-3] [PMID: 30760290]
[38]
Wu X, Liu Z, Hu L, Gu W, Zhu L. Exosomes derived from endothelial progenitor cells ameliorate acute lung injury by transferring miR-126. Exp Cell Res 2018; 370(1): 13-23.
[http://dx.doi.org/10.1016/j.yexcr.2018.06.003] [PMID: 29883714]
[39]
Moon HG, Cao Y, Yang J, Lee JH, Choi HS, Jin Y. Lung epithelial cell-derived extracellular vesicles activate macrophage-mediated inflammatory responses via ROCK1 pathway. Cell Death Dis 2015; 6 e2016
[http://dx.doi.org/10.1038/cddis.2015.282] [PMID: 26658190]
[40]
Li ZG, Scott MJ, Brzóska T, et al. Lung epithelial cell-derived IL-25 negatively regulates LPS-induced exosome release from macrophages. Mil Med Res 2018; 5(1): 24.
[http://dx.doi.org/10.1186/s40779-018-0173-6] [PMID: 30056803]
[41]
Heijnen HF, Schiel AE, Fijnheer R, Geuze HJ, Sixma JJ. Activated platelets release two types of membrane vesicles: microvesicles by surface shedding and exosomes derived from exocytosis of multivesicular bodies and alpha-granules. Blood 1999; 94(11): 3791-9.
[http://dx.doi.org/10.1182/blood.V94.11.3791] [PMID: 10572093]
[42]
Zhu YG, Feng XM, Abbott J, et al. Human mesenchymal stem cell microvesicles for treatment of Escherichia coli endotoxin-induced acute lung injury in mice. Stem Cells 2014; 32(1): 116-25.
[http://dx.doi.org/10.1002/stem.1504] [PMID: 23939814]
[43]
Monsel A, Zhu YG, Gennai S, et al. Therapeutic effects of human mesenchymal stem cell-derived microvesicles in severe pneumonia in mice. Am J Respir Crit Care Med 2015; 192(3): 324-36.
[http://dx.doi.org/10.1164/rccm.201410-1765OC] [PMID: 26067592]
[44]
Genschmer KR, Russell DW, Lal C, et al. Activated PMN exosomes: pathogenic entities causing matrix destruction and disease in the lung cell 2019; 176: 113-126.e15.
[45]
Chang CL, Sung PH, Chen KH, et al. Adipose-derived mesenchymal stem cell-derived exosomes alleviate overwhelming systemic inflammatory reaction and organ damage and improve outcome in rat sepsis syndrome. Am J Transl Res 2018; 10(4): 1053-70.
[PMID: 29736200]
[46]
Jia P, Wu X, Dai Y, et al. MicroRNA-21 is required for local and remote ischemic preconditioning in multiple organ protection against sepsis. Crit Care Med 2017; 45(7): e703-10.
[http://dx.doi.org/10.1097/CCM.0000000000002363] [PMID: 28437377]
[47]
Pan T, Jia P, Chen N, et al. Delayed remote ischemic preconditioning confersrenoprotection against septic acute kidney injury via exosomal miR-21. Theranostics 2019; 9(2): 405-23.
[http://dx.doi.org/10.7150/thno.29832] [PMID: 30809283]
[48]
Balusu S, Van Wonterghem E, De Rycke R, et al. Identification of a novel mechanism of blood-brain communication during peripheral inflammation via choroid plexus-derived extracellular vesicles. EMBO Mol Med 2016; 8(10): 1162-83.
[http://dx.doi.org/10.15252/emmm.201606271] [PMID: 27596437]
[49]
Li JJ, Wang B, Kodali MC, et al. In vivo evidence for the contribution of peripheral circulating inflammatory exosomes to neuroinflammation. J Neuroinflammation 2018; 15(1): 8.
[http://dx.doi.org/10.1186/s12974-017-1038-8] [PMID: 29310666]
[50]
Zhao S, Wehner R, Bornhäuser M, Wassmuth R, Bachmann M, Schmitz M. Immunomodulatory properties of mesenchymal stromal cells and their therapeutic consequences for immune-mediated disorders. Stem Cells Dev 2010; 19(5): 607-14.
[http://dx.doi.org/10.1089/scd.2009.0345] [PMID: 19824807]
[51]
Singer NG, Caplan AI. Mesenchymal stem cells: mechanisms of inflammation. Annu Rev Pathol 2011; 6: 457-78.
[http://dx.doi.org/10.1146/annurev-pathol-011110-130230] [PMID: 21073342]
[52]
Russell KC, Phinney DG, Lacey MR, Barrilleaux BL, Meyertholen KE, O’Connor KC. In vitro high-capacity assay to quantify the clonal heterogeneity in trilineage potential of mesenchymal stem cells reveals a complex hierarchy of lineage commitment. Stem Cells 2010; 28(4): 788-98.
[http://dx.doi.org/10.1002/stem.312] [PMID: 20127798]
[53]
Tamura R, Uemoto S, Tabata Y. Immunosuppressive effect of mesenchymal stem cell-derived exosomes on a concanavalin A-induced liver injury model. Inflamm Regen 2016; 36: 26.
[http://dx.doi.org/10.1186/s41232-016-0030-5] [PMID: 29259699]
[54]
Eguchi A, Franz N, Kobayashi Y, et al. Circulating extracellular vesicles and their mir “barcode” differentiate alcohol drinkers with liver injury and those without liver injury in severe trauma patients. Front Med (Lausanne) 2019; 6: 30.
[http://dx.doi.org/10.3389/fmed.2019.00030] [PMID: 30859103]
[55]
Bonjoch L, Casas V, Carrascal M, Closa D. Involvement of exosomes in lung inflammation associated with experimental acute pancreatitis. J Pathol 2016; 240(2): 235-45.
[http://dx.doi.org/10.1002/path.4771] [PMID: 27447723]
[56]
Park KS, Lee J, Lee C, et al. Sepsis-like systemic inflammation induced by nano-sized extracellular vesicles from feces. Front Microbiol 2018; 9: 1735.
[http://dx.doi.org/10.3389/fmicb.2018.01735] [PMID: 30131776]
[57]
Real JM, Ferreira LRP, Esteves GH, et al. Exosomes from patients with septic shock convey miRNAs related to inflammation and cell cycle regulation: new signaling pathways in sepsis? Crit Care 2018; 22(1): 68.
[http://dx.doi.org/10.1186/s13054-018-2003-3] [PMID: 29540208]
[58]
Zarbock A, Kellum JA. Remote ischemic preconditioning and protection of the kidney-a novel therapeutic option. Crit Care Med 2016; 44(3): 607-16.
[http://dx.doi.org/10.1097/CCM.0000000000001381] [PMID: 26496454]
[59]
Song Y, Dou H, Li X, et al. Exosomal miR-146a contributes to the enhanced therapeutic efficacy of interleukin-1β-primed mesenchymal stem cells against sepsis. Stem Cells 2017; 35(5): 1208-21.
[http://dx.doi.org/10.1002/stem.2564] [PMID: 28090688]
[60]
Alexander M, Hu R, Runtsch MC, et al. Exosome-delivered microRNAs modulate the inflammatory response to endotoxin. Nat Commun 2015; 6: 7321.
[http://dx.doi.org/10.1038/ncomms8321] [PMID: 26084661]
[61]
Alexander M, Ramstead AG, Bauer KM, et al. Rab27-dependent exosome production inhibits chronic inflammation and enables acute responses to inflammatory stimuli. J Immunol 2017; 199(10): 3559-70.
[http://dx.doi.org/10.4049/jimmunol.1700904] [PMID: 28978688]
[62]
Ostrowski M, Carmo NB, Krumeich S, et al. Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat Cell Biol 2010; 12(1): 9-30. 1-13
[http://dx.doi.org/10.1038/ncb2000]
[63]
Hanayama R, Tanaka M, Miwa K, Shinohara A, Iwamatsu A, Nagata S. Identification of a factor that links apoptotic cells to phagocytes. Nature 2002; 417(6885): 182-7.
[http://dx.doi.org/10.1038/417182a] [PMID: 12000961]
[64]
Miksa M, Wu R, Dong W, et al. Immature dendritic cell-derived exosomes rescue septic animals via milk fat globule epidermal growth factor-factor VIII. J Immunol 2009; 183(9): 5983-90.
[http://dx.doi.org/10.4049/jimmunol.0802994] [PMID: 19812188]
[65]
Miksa M, Wu R, Dong W, Das P, Yang D, Wang P. Dendritic cell-derived exosomes containing milk fat globule epidermal growth factor-factor VIII attenuate proinflammatory responses in sepsis. Shock 2006; 25(6): 586-93.
[http://dx.doi.org/10.1097/01.shk.0000209533.22941.d0] [PMID: 16721266]
[66]
Komura H, Miksa M, Wu R, Goyert SM, Wang P. Milk fat globule epidermal growth factor-factor VIII is down-regulated in sepsis via the lipopolysaccharide-CD14 pathway. J Immunol 2009; 182(1): 581-7.
[http://dx.doi.org/10.4049/jimmunol.182.1.581] [PMID: 19109191]
[67]
Goodwin AJ, Guo C, Cook JA, Wolf B, Halushka PV, Fan H. Plasma levels of microRNA are altered with the development of shock in human sepsis: an observational study. Crit Care 2015; 19: 440.
[http://dx.doi.org/10.1186/s13054-015-1162-8] [PMID: 26683209]
[68]
Xu Y, Ku X, Wu C, Cai C, Tang J, Yan W. Exosomal proteome analysis of human plasma to monitor sepsis progression. Biochem Biophys Res Commun 2018; 499(4): 856-61.
[http://dx.doi.org/10.1016/j.bbrc.2018.04.006] [PMID: 29625113]
[69]
Reithmair M, Buschmann D, Märte M, et al. Cellular and extracellular miRNAs are blood-compartment-specific diagnostic targets in sepsis. J Cell Mol Med 2017; 21(10): 2403-11.
[http://dx.doi.org/10.1111/jcmm.13162] [PMID: 28382754]
[70]
Wu SC, Yang JC, Rau CS, et al. Profiling circulating microRNA expression in experimental sepsis using cecal ligation and puncture. PLoS One 2013; 8(10) e77936
[http://dx.doi.org/10.1371/journal.pone.0077936] [PMID: 24205035]
[71]
Gómez H, Kellum JA. Sepsis-induced acute kidney injury. Curr Opin Crit Care 2016; 22(6): 546-53.
[http://dx.doi.org/10.1097/MCC.0000000000000356] [PMID: 27661757]
[72]
Panich T, Chancharoenthana W, Somparn P, Issara-Amphorn J, Hirankarn N, Leelahavanichkul A. Urinary exosomal activating transcriptional factor 3 as the early diagnostic biomarker for sepsis-induced acute kidney injury. BMC Nephrol 2017; 18(1): 10.
[http://dx.doi.org/10.1186/s12882-016-0415-3] [PMID: 28061889]
[73]
Park EJ, Yuki Y, Kiyono H, Shimaoka M. Structural basis of blocking integrin activation and deactivation for anti-inflammation. J Biomed Sci 2015; 22: 51.
[http://dx.doi.org/10.1186/s12929-015-0159-6] [PMID: 26152212]
[74]
Hoshino A, Costa-Silva B, Shen TL, et al. Tumour exosome integrins determine organotropic metastasis. Nature 2015; 527(7578): 329-35.
[http://dx.doi.org/10.1038/nature15756] [PMID: 26524530]
[75]
Kawamoto E, Masui-Ito A, Eguchi A, et al. Integrin and PD-1 ligand expression on circulating extracellular vesicles in systemic inflammatory response syndrome and sepsis. Shock 2018; 52(1): 13-22.
[PMID: 30036273]
[76]
Ventimiglia LN, Alonso MA. Biogenesis and function of T cell-derived exosomes. Front Cell Dev Biol 2016; 4: 84.
[http://dx.doi.org/10.3389/fcell.2016.00084] [PMID: 27583248]
[77]
Lu J, Wu J, Tian J, Wang S. Role of T cell-derived exosomes in immunoregulation. Immunol Res 2018; 66(3): 313-22.
[http://dx.doi.org/10.1007/s12026-018-9000-0] [PMID: 29804198]
[78]
Xie Y, Zhang H, Li W, et al. Dendritic cells recruit T cell exosomes via exosomal LFA-1 leading to inhibition of CD8+ CTL responses through downregulation of peptide/MHC class I and Fas ligand-mediated cytotoxicity. J Immunol 2010; 185(9): 5268-78.
[http://dx.doi.org/10.4049/jimmunol.1000386] [PMID: 20881190]
[79]
Shimaoka M, Kawamoto E, Gaowa A, Okamoto T, Park EJ. Connexins and integrins in exosomes. Cancers (Basel) 2019; 11(1): 11.
[http://dx.doi.org/10.3390/cancers11010106] [PMID: 30658425]
[80]
Park EJ, Prajuabjinda O, Soe ZY, et al. Exosomal regulation of lymphocyte homing to the gut. Blood Adv 2019; 3(1): 1-11.
[http://dx.doi.org/10.1182/bloodadvances.2018024877] [PMID: 30591532]
[81]
Moser M, Legate KR, Zent R, Fässler R. The tail of integrins, talin, and kindlins. Science 2009; 324(5929): 895-9.
[http://dx.doi.org/10.1126/science.1163865] [PMID: 19443776]
[82]
Tadokoro S, Shattil SJ, Eto K, et al. Talin binding to integrin beta tails: a final common step in integrin activation. Science 2003; 302(5642): 103-6.
[http://dx.doi.org/10.1126/science.1086652] [PMID: 14526080]
[83]
Soe ZY, Prajuabjinda O, Myint PK, et al. Talin-2 regulates integrin functions in exosomes. Biochem Biophys Res Commun 2019; 512(3): 429-34.
[http://dx.doi.org/10.1016/j.bbrc.2019.03.027] [PMID: 30879762]
[84]
Leoni G, Neumann PA, Kamaly N, et al. Annexin A1-containing extracellular vesicles and polymeric nanoparticles promote epithelial wound repair. J Clin Invest 2015; 125(3): 1215-27.
[http://dx.doi.org/10.1172/JCI76693] [PMID: 25664854]
[85]
Borges FT, Melo SA, Özdemir BC, et al. TGF-β1-containing exosomes from injured epithelial cells activate fibroblasts to initiate tissue regenerative responses and fibrosis. J Am Soc Nephrol 2013; 24(3): 385-92.
[http://dx.doi.org/10.1681/ASN.2012101031] [PMID: 23274427]
[86]
Park SJ, Kim JM, Kim J, et al. Molecular mechanisms of biogenesis of apoptotic exosome-like vesicles and their roles as damage-associated molecular patterns. Proc Natl Acad Sci USA 2018; 115(50): E11721-30.
[http://dx.doi.org/10.1073/pnas.1811432115] [PMID: 30463946]
[87]
Vicencio JM, Yellon DM, Sivaraman V, et al. Plasma exosomes protect the myocardium from ischemia-reperfusion injury. J Am Coll Cardiol 2015; 65(15): 1525-36.
[http://dx.doi.org/10.1016/j.jacc.2015.02.026] [PMID: 25881934]
[88]
Jin CY, Lee JD, Park C, Choi YH, Kim GY. Curcumin attenuates the release of pro-inflammatory cytokines in lipopolysaccharide-stimulated BV2 microglia. Acta Pharmacol Sin 2007; 28(10): 1645-51.
[http://dx.doi.org/10.1111/j.1745-7254.2007.00651.x] [PMID: 17883952]
[89]
Menon VP, Sudheer AR. Antioxidant and anti-inflammatory properties of curcumin. Adv Exp Med Biol 2007; 595: 105-25.
[http://dx.doi.org/10.1007/978-0-387-46401-5_3] [PMID: 17569207]
[90]
Jurenka JS. Anti-inflammatory properties of curcumin, a major constituent of Curcuma longa: a review of preclinical and clinical research. Altern Med Rev 2009; 14(2): 141-53.
[PMID: 19594223]
[91]
Sun D, Zhuang X, Xiang X, et al. A novel nanoparticle drug delivery system: the anti-inflammatory activity of curcumin is enhanced when encapsulated in exosomes. Mol Ther 2010; 18(9): 1606-14.
[http://dx.doi.org/10.1038/mt.2010.105] [PMID: 20571541]
[92]
Zhuang X, Xiang X, Grizzle W, et al. Treatment of brain inflammatory diseases by delivering exosome encapsulated anti-inflammatory drugs from the nasal region to the brain. Mol Ther 2011; 19(10): 1769-79.
[http://dx.doi.org/10.1038/mt.2011.164] [PMID: 21915101]
[93]
Fuhrmann G, Chandrawati R, Parmar PA, et al. Engineering extracellular vesicles with the tools of enzyme prodrug therapy. Adv Mater 2018; 30(15) e1706616
[http://dx.doi.org/10.1002/adma.201706616] [PMID: 29473230]
[94]
Willis GR, Mitsialis SA, Kourembanas S. “Good things come in small packages”: application of exosome-based therapeutics in neonatal lung injury. Pediatr Res 2018; 83(1-2): 298-307.
[http://dx.doi.org/10.1038/pr.2017.256] [PMID: 28985201]
[95]
Peer D, Park EJ, Morishita Y, Carman CV, Shimaoka M. Systemic leukocyte-directed siRNA delivery revealing cyclin D1 as an anti-inflammatory target. Science 2008; 319(5863): 627-30.
[http://dx.doi.org/10.1126/science.1149859] [PMID: 18239128]
[96]
Maheshwari R, Tekade M, Gondaliya P, Kalia K, D’Emanuele A, Tekade RK. Recent advances in exosome-based nanovehicles as RNA interference therapeutic carriers. Nanomedicine (Lond) 2017; 12(21): 2653-75.
[http://dx.doi.org/10.2217/nnm-2017-0210] [PMID: 28960165]
[97]
Shtam TA, Kovalev RA, Varfolomeeva EY, Makarov EM, Kil YV, Filatov MV. Exosomes are natural carriers of exogenous siRNA to human cells in vitro. Cell Commun Signal 2013; 11: 88.
[http://dx.doi.org/10.1186/1478-811X-11-88] [PMID: 24245560]
[98]
Alvarez-Erviti L, Seow Y, Yin H, Betts C, Lakhal S, Wood MJ. Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. Nat Biotechnol 2011; 29(4): 341-5.
[http://dx.doi.org/10.1038/nbt.1807] [PMID: 21423189]
[99]
Miller RR III, Lopansri BK, Burke JP, et al. Validation of a host response assay, SeptiCyte LAB, for discriminating sepsis from systemic inflammatory response syndrome in the ICU. Am J Respir Crit Care Med 2018; 198(7): 903-13.
[http://dx.doi.org/10.1164/rccm.201712-2472OC] [PMID: 29624409]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy