Extracellular vesicles from human plasma dampen inflammation and promote tissue repair functions in macrophages.
CREB
PGE2
exosomes
extracellular vesicles
human plasma
infection
inflammation
macrophages
resolution
tissue homeostasis
wound-healing
Journal
Journal of extracellular vesicles
ISSN: 2001-3078
Titre abrégé: J Extracell Vesicles
Pays: United States
ID NLM: 101610479
Informations de publication
Date de publication:
06 2023
06 2023
Historique:
revised:
14
04
2023
received:
31
08
2022
accepted:
04
05
2023
medline:
7
6
2023
pubmed:
5
6
2023
entrez:
5
6
2023
Statut:
ppublish
Résumé
Although inflammation is a vital defence response to infection, if left uncontrolled, it can lead to pathology. Macrophages are critical players both in driving the inflammatory response and in the subsequent events required for restoring tissue homeostasis. Extracellular vesicles (EVs) are membrane-enclosed structures released by cells that mediate intercellular communication and are present in all biological fluids, including blood. Herein, we show that extracellular vesicles from plasma (pEVs) play a relevant role in the control of inflammation by counteracting PAMP-induced macrophage activation. Indeed, pEV-treatment of macrophages simultaneously with or prior to PAMP exposure reduced the secretion of pro-inflammatory IL-6 and TNF-α and increased IL-10 response. This anti-inflammatory activity was associated with the promotion of tissue-repair functions in macrophages, characterized by augmented efferocytosis and pro-angiogenic capacity, and increased expression of VEGFa, CD300e, RGS2 and CD93, genes involved in cell growth and tissue remodelling. We also show that simultaneous stimulation of macrophages with a PAMP and pEVs promoted COX2 expression and CREB phosphorylation as well as the accumulation of higher concentrations of PGE2 in cell culture supernatants. Remarkably, the anti-inflammatory activity of pEVs was abolished if cells were treated with a pharmacological inhibitor of COX2, indicating that pEV-mediated induction of COX2 is critical for the pEV-mediated inhibition of inflammation. Finally, we show that pEVs added to monocytes prior to their M-CSF-induced differentiation to macrophages increased efferocytosis and diminished pro-inflammatory cytokine responses to PAMP stimulation. In conclusion, our results suggest that pEVs are endogenous homeostatic modulators of macrophages, activating the PGE2/CREB pathway, decreasing the production of inflammatory cytokines and promoting tissue repair functions.
Identifiants
pubmed: 37272889
doi: 10.1002/jev2.12331
pmc: PMC10241174
doi:
Substances chimiques
Dinoprostone
K7Q1JQR04M
Cyclooxygenase 2
EC 1.14.99.1
Cytokines
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e12331Subventions
Organisme : NIDA NIH HHS
ID : R01DA040385
Pays : United States
Organisme : NIH HHS
ID : U54-CA0221208
Pays : United States
Informations de copyright
© 2023 The Authors. Journal of Extracellular Vesicles published by Wiley Periodicals, LLC on behalf of the International Society for Extracellular Vesicles.
Références
Atay, S., Gercel-Taylor, C., & Taylor, D. D. (2011). Human trophoblast-derived exosomal fibronectin induces pro-inflammatory IL-1β production by macrophages. American Journal of Reproductive Immunology, 66(4), 259-269.
Baluk, P., Hirata, A., Thurston, G., Fujiwara, T., Neal, C. R., Michel, C. C., & McDonald, D. M. (1997). Endothelial gaps: Time course of formation and closure in inflamed venules of rats. American Journal of Physiology, 272(1 Pt 1), L155-L170.
Bannoud, N., García, P. A., Gambarte-Tudela, J., Sundblad, V., Cagnoni, A. J., Bach, C. A., Pérez Saez, J. M., Blidner, A. G., Maller, S. M., Mariño, K. V., Salatino, M., Cerliani, J. P., Rabinovich, G. A., & Croci, D. O. (2022). Untangling galectin-mediated circuits that control hypoxia-driven angiogenesis. Methods in Molecular Biology, 2442, 635-653. https://doi.org/10.1007/978-1-0716-2055-7_34
Barrès, C., Blanc, L., Bette-Bobillo, P., André, S., Mamoun, R., Gabius, H.-J., & Vidal, M. (2010). Galectin-5 is bound onto the surface of rat reticulocyte exosomes and modulates vesicle uptake by macrophages. Blood, 115(3), 696-705.
Basil, M. C., & Levy, B. D. (2016). Specialized pro-resolving mediators: Endogenous regulators of infection and inflammation. Nature Reviews Immunology, 16(1), 51-67.
Bei, Y., Xu, T., Lv, D., Yu, P., Xu, J., Che, L., Das, A., Tigges, J., Toxavidis, V., Ghiran, I., Shah, R., Li, Y., Zhang, Y., Das, S., & Xiao, J. (2017). Exercise-induced circulating extracellular vesicles protect against cardiac ischemia-reperfusion injury. Basic Research in Cardiology, 112(4), 38.
Bernard, M. A., Zhao, H., Yue, S. C., Anandaiah, A., Koziel, H., & Tachado, S. D. (2014). Novel HIV-1 MiRNAs stimulate TNFa release in human macrophages via TLR8 signaling pathway. PLoS ONE, 9(9), e106006.
Boilard, E. (2018). Extracellular vesicles and their content in bioactive lipid mediators: More than a sack of microRNA. Journal of Lipid Research, 59(11), 2037-2046.
Böing, A. N., Der, P. E. V., Grootemaat, A. E., a, C. F., Sturk, A., & Nieuwland, R. (2014). Single-step isolation of extracellular vesicles from plasma by size-exclusion chromatography. Int Meet ISEV Rotterdam, 3, 118.
Bonjoch, L., Casas, V., Carrascal, M., & Closa, D. (2016). Involvement of exosomes in lung inflammation associated with experimental acute pancreatitis. Journal of Pathology, 240(2), 235-245.
Brahmer, A., Neuberger, E., Esch-Heisser, L., Haller, N., Jorgensen, M. M., Baek, R., Möbius, W., Simon, P., & Krämer-Albers, E.-M. (2019). Platelets, endothelial cells and leukocytes contribute to the exercise-triggered release of extracellular vesicles into the circulation. Journal of Extracellular Vesicles, 8(1), 1615820.
Brusini, R., Varna, M., & Couvreur, P. (2020). Advanced nanomedicines for the treatment of inflammatory diseases. Advanced Drug Delivery Reviews, 15, 161-178.
Buzas, E. I., György, B., Nagy, G., Falus, A., & Gay, S. (2014). Emerging role of extracellular vesicles in inflammatory diseases. Nature Reviews Rheumatology, 10(6), 356-364. Available from: https://doi.org/10.1038/nrrheum.2014.19
Chen, L., Chen, R., Kemper, S., Cong, M., You, H., & Brigstock, D. R. (2018). Therapeutic effects of serum extracellular vesicles in liver fibrosis. Journal of Extracellular Vesicles, 7(1), 1461505.
Chettimada, S., Lorenz, D. R., Misra, V., Dillon, S. T., Reeves, R. K., Manickam, C., Morgello, S., Kirk, G. D., Mehta, S. H., & Gabuzda, D. (2018). Exosome markers associated with immune activation and oxidative stress in HIV patients on antiretroviral therapy. Scientific Reports, 8, 7227.
Cho, W., & Choe, J. (2020). Prostaglandin E2 stimulates COX-2 expression via mitogen-activated protein kinase p38 but not ERK in human follicular dendritic cell-like cells. BMC Immunology [Electronic Resource], 21(1), 20.
Colombo, M., Raposo, G., & Théry, C. (2014). Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annual Review of Cell and Developmental Biology, 30(1), 255-289.
Cooks, T., Pateras, I. S., Jenkins, L. M., Patel, K. M., Robles, A. I., Morris, J., Forshew, T., Appella, E., Gorgoulis, V. G., & Harris, C. C. (2018). Mutant p53 cancers reprogram macrophages to tumor supporting macrophages via exosomal miR-1246. Nature Communications, 9(1), 771.
Crawford, N. (1971). The presence of contractile proteins in platelet microparticles isolated from human and animal platelet-free plasma. British Journal of Haematology, 21(1), 53-69.
Dalli, J., & Serhan, C. N. (2012). Specific lipid mediator signatures of human phagocytes: Microparticles stimulate macrophage efferocytosis and pro-resolving mediators. Blood, 120(15), e60-e72.
De Boer, C., & Davies, N. H. (2022). Blood derived extracellular vesicles as regenerative medicine therapeutics. Biochimie, 196, 203-215.
Deng, Z.-B., Zhuang, X., Ju, S., Xiang, X., Mu, J., Liu, Y., Jiang, H., Zhang, L., Mobley, J., Mcclain, C., Feng, W., Grizzle, W., Yan, J., Miller, D., Kronenberg, M., & Zhang, H.-G. (2013). Exosome-like nanoparticles from intestinal mucosal cells carry prostaglandin E 2 and suppress activation of liver NKT cells. Journal of Immunology, 190(7), 3579-3589.
Donzelli, J., Proestler, E., Riedel, A., Nevermann, S., Hertel, B., Guenther, A., Gattenlöhner, S., Savai, R., Larsson, K., & Saul, M. J. (2021). Small extracellular vesicle-derived miR-574-5p regulates PGE2-biosynthesis via TLR7/8 in lung cancer. Journal of Extracellular Vesicles, 10(12), 12143.
Duchez, A.-C., Boudreau, L. H., Naika, G. S., Bollinger, J., Belleannée, C., Cloutier, N., Laffont, B., Mendoza-Villarroel, R. E., Lévesque, T., Rollet-Labelle, E., Rousseau, M., Allaeys, I., Tremblay, J. J., Poubelle, P. E., Lambeau, G., Pouliot, M., Provost, P., Soulet, D., Gelb, M. H., & Boilard, E. (2015). Platelet microparticles are internalized in neutrophils via the concerted activity of 12-lipoxygenase and secreted phospholipase A2-IIA. PNAS, 112(27), E3564-73.
Duette, G., Pereyra Gerber, P., Rubione, J., Perez, P. S., Landay, A. L., Crowe, S. M., Liao, Z., Witwer, K. W., Holgado, M. P., Salido, J., Geffner, J., Sued, O., Palmer, C. S., & Ostrowski, M. (2018). Induction of HIF-1α by HIV-1 infection in CD4+ T cells promotes viral replication and drives extracellular vesicle- mediated inflammation. MBio, 9(5), 1-21. Available from: https://doi.org/10.1128/mBio.00757-18
Escobar, C., Kao, C.-Y., Das, S., & Papoutsakis, E. T. (2020). Human megakaryocytic microparticles induce de novo platelet biogenesis in a wild-type murine model. Blood Advances, 4(5), 804-814.
Feng, D., Zhao, W.-L., Ye, Y.-Y., Bai, X.-C., Liu, R.-Q., Chang, L.-F., Zhou, Q., & Sui, S.-F. (2010). Cellular internalization of exosomes occurs through phagocytosis. Traffic (Copenhagen, Denmark), 11(5), 675-687.
Freire-De-Lima, C. G., Xiao, Yi Q., Gardai, S. J., Bratton, D. L., Schiemann, W. P., & Henson, P. M. (2006). Apoptotic cells, through transforming growth factor-β, coordinately induce anti-inflammatory and suppress pro-inflammatory eicosanoid and NO synthesis in murine macrophages. Journal of Biological Chemistry, 281(50), 38376-38384.
French, S. L., Butov, K. R., Allaeys, I., Canas, J., Morad, G., Davenport, P., Laroche, A., Trubina, N. M., Italiano, J. E., Moses, M. A., Sola-Visner, M., Boilard, E., Panteleev, M. A., & Machlus, K. R. (2020). Platelet-derived extracellular vesicles infiltrate and modify the bone marrow during inflammation. Blood Advances, 4(13), 3011-3023. https://doi.org/10.1182/bloodadvances.2020001758
Frühbeis, C., Helmig, S., Tug, S., Simon, P., & Krämer-Albers, E.-M. (2015). Physical exercise induces rapid release of small extracellular vesicles into the circulation. Journal of Extracellular Vesicles, 4(1), 28239.
Fujino, H., Salvi, S., & Regan, J. W. (2005). Differential regulation of phosphorylation of the cAMP response element-binding protein after activation of EP2 and EP4 prostanoid receptors by prostaglandin E2. Molecular Pharmacology, 68(1), 251-259.
George, J., Thoi, L., Mcmanus, L., & Reimann, T. (1982). Isolation of human platelet membrane microparticles from plasma and serum. Blood, 60(4), 834-840.
Gill, S. K., Yao, Y., Kay, L. J., Bewley, M. A., Marriott, H. M., & Peachell, P. T. (2016). The anti-inflammatory effects of PGE2on human lung macrophages are mediated by the EP4receptor. British Journal of Pharmacology, 3099-3109.
Grange, C., Tapparo, M., Bruno, S., Chatterjee, D., Quesenberry, P. J., Tetta, C., & Camussi, G. (2014). Biodistribution of mesenchymal stem cell-derived extracellular vesicles in a model of acute kidney injury monitored by optical imaging. International Journal of Molecular Medicine, 33(5), 1055-1063.
Hamidzadeh, K., Belew, A. T., El-Sayed, N. M., & Mosser, D. M. (2020). The transition of M-CSF - derived human macrophages to a growth-promoting phenotype. Blood Advances, 4(21), 5460-5472.
Hamidzadeh, K., Christensen, S. M., Dalby, E., Chandrasekaran, P., & Mosser, D. M. (2017). Macrophages and the recovery from acute and chronic inflammation. Annual Review of Physiology, 79, 567-592.
Hirata, A., Baluk, P., Fujiwara, T., & McDonald, D. M. (1995). Location of focal silver staining at endothelial gaps in inflamed venules examined by scanning electron microscopy. American Journal of Physiology, 269(3 Pt 1), L403-18.
Honda, A., Sugimoto, Y., Namba, T., Watabe, A., Irie, A., Negishi, M., Narumiya, S., & Ichikawa, A. (1993). Cloning and expression of a cDNA for mouse prostaglandin E receptor EP2 subtype. Journal of Biological Chemistry, 268(11), 7759-7762.
Hoshino, A., Kim, H. S., Bojmar, L., Gyan, K. E., Cioffi, M., Hernandez, J., Zambirinis, C. P., Rodrigues, G., Molina, H., Heissel, S., Mark, M. T., Steiner, L., Benito-Martin, A., Lucotti, S., Di Giannatale, A., Offer, K., Nakajima, M., Williams, C., Nogués, L., … Lyden, D. (2020). Extracellular vesicle and particle biomarkers define multiple human cancers. Cell, 182(4), 1044-1061.e18.
Hou, Z., Qin, X., Hu, Y., Zhang, X., Li, G., Wu, J., Li, J., Sha, J., Chen, J., Xia, J., Wang, L., & Gao, F. (2019). Longterm exercise-derived exosomal miR-342-5p: A novel exerkine for cardioprotection. Circulation Research, 124(9), 1386-1400.
Hsu, H.-H., Lin, Y.-M., Shen, C.-Y., Shibu, M., Li, S.-Y., Chang, S.-H., Lin, C.-C., Chen, R.-J., Viswanadha, V., Shih, H.-N., & Huang, C.-Y. (2017). Prostaglandin E2-induced COX-2 expressions via EP2 and EP4 signaling pathways in human LoVo colon cancer cells. International Journal of Molecular Sciences, 18(6), 1132.
Hu, Q., Lyon, C. J., Fletcher, J. K., Tang, W., Wan, M., & Hu, T. Y. (2021). Extracellular vesicle activities regulating macrophage- and tissue-mediated injury and repair responses. Acta Pharmaceutica Sinica B, 11(6), 1493-1512. https://doi.org/10.1016/j.apsb.2020.12.014
Hyenne, V., Ghoroghi, S., Collot, M., Bons, J., Follain, G., Harlepp, S., Mary, B., Bauer, J., Mercier, L., Busnelli, I., Lefebvre, O., Fekonja, N., Garcia-Leon, M. J., Machado, P., Delalande, F., López, A. A., Silva, S. G., Verweij, F. J., Van Niel, G., … Goetz, J. G. (2019). Studying the fate of tumor extracellular vesicles at high spatiotemporal resolution using the Zebrafish embryo. Developmental Cell, 48(4), 554-572.e7.
Hyvärinen, K., Holopainen, M., Skirdenko, V., Ruhanen, H., Lehenkari, P., Korhonen, M., Käkelä, R., Laitinen, S., & Kerkelä, E. (2018). Mesenchymal stromal cells and their extracellular vesicles enhance the anti-inflammatory phenotype of regulatory macrophages by downregulating the production of interleukin (IL)-23 and IL-22. Frontiers in Immunology, 9, 771.
Imai, T., Takahashi, Y., Nishikawa, M., Kato, K., Morishita, M., Yamashita, T., Matsumoto, A., Charoenviriyakul, C., & Takakura, Y. (2015). Macrophage-dependent clearance of systemically administered B16BL6-derived exosomes from the blood circulation in mice. Journal of Extracellular Vesicles, 4(1), 26238.
Just, J., Yan, Y., Farup, J., Sieljacks, P., Sloth, M., Venø, M., Gu, T., De Paoli, F. V., Nyengaard, J. R., Baek, R., Jørgensen, M. M., Kjems, J., Vissing, K., & Drasbek, K. R. (2020). Blood flow-restricted resistance exercise alters the surface profile, miRNA cargo and functional impact of circulating extracellular vesicles. Scientific Reports, 10(1), 1-13.
Kalani, M. Y. S., Alsop, E., Meechoovet, B., Beecroft, T., Agrawal, K., Whitsett, T. G., Huentelman, M. J., Spetzler, R. F., Nakaji, P., Kim, S., & Van Keuren-Jensen, K. (2020). Extracellular microRNAs in blood differentiate between ischaemic and haemorrhagic stroke subtypes. Journal of Extracellular Vesicles, 9(1), 1713540.
Kalinski, P. (2012). Regulation of immune responses by prostaglandin E2 . Journal of Immunology, 188(1), 21-28.
Karimi, N., Cvjetkovic, A., Jang, Su C., Crescitelli, R., Hosseinpour Feizi, M. A., Nieuwland, R., Lötvall, J., & Lässer, C. (2018). Detailed analysis of the plasma extracellular vesicle proteome after separation from lipoproteins. Cellular and Molecular Life Sciences, 75(15), 2873-2886.
Karimi, N., Dalirfardouei, R., Dias, T., Lötvall, J., & Lässer, C. (2022). Tetraspanins distinguish separate extracellular vesicle subpopulations in human serum and plasma-Contributions of platelet extracellular vesicles in plasma samples. Journal of Extracellular Vesicles, 11, 12213.
Khan, S., Bennit, H. F., Turay, D., Perez, M., Mirshahidi, S., Yuan, Y., & Wall, N. R. (2014). Early diagnostic value of survivin and its alternative splice variants in breast cancer. BMC Cancer, 14, 176.
Kuroda, E., & Yamashita, U. (2022). Mechanisms of enhanced macrophage-mediated prostaglandin E2 production and its suppressive role in Th1 activation in Th2-dominant BALB/c mice. Journal of Immunology, 170, 757-764.
Linton, S. S., Abraham, T., Liao, J., Clawson, G. A., Butler, P. J., Fox, T., Kester, M., & Matters, G. L. (2018). Tumor-promoting effects of pancreatic cancer cell exosomes on THP-1-derived macrophages. PLoS ONE, 13(11), 1-20.
Liu, R., Tang, A., Wang, X., Chen, X., Zhao, L., Xiao, Z., & Shen, S. (2018). Inhibition of lncRNA NEAT1 suppresses the inflammatory response in IBD by modulating the intestinal epithelial barrier and by exosome-mediated polarization of macrophages. International Journal of Molecular Medicine, 42(5), 2903-2913.
Liu, Y., Sun, D., Fan, Q., Ma, Q., Dong, Z., Tao, W., Tao, H., Liu, Z., & Wang, C. (2020). The enhanced permeability and retention effect based nanomedicine at the site of injury. Nano Research, 13(2), 564-569. https://doi.org/10.1007/s12274-020-2655-6
Locati, M., Curtale, G., & Mantovani, A. (2020). Diversity, mechanisms, and significance of macrophage plasticity. Annual Review of Pathology: Mechanisms of Disease, 15, 123-147.
Luan, B., Yoon, Y.-S., Le Lay, J., Kaestner, K. H., Hedrick, S., & Montminy, M. (2015). CREB pathway links PGE2 signaling with macrophage polarization. PNAS, 112(51), 15642-15647.
Mackenzie, K. F., Clark, K., Naqvi, S., Mcguire, V. A., Nöehren, G., Kristariyanto, Y., Van Den Bosch, M., Mudaliar, M., Mccarthy, P. C., Pattison, M. J., Pedrioli, P. G. A., Barton, G. J., Toth, R., Prescott, A., & Arthur, J. S. C. (2013). PGE(2) induces macrophage IL-10 production and a regulatory-like phenotype via a protein kinase A-SIK-CRTC3 pathway. Journal of Immunology, 190(2), 565-577.
Mastronardi, M. L., Mostefai, H. A., Meziani, F., Martínez, M. C., Asfar, P., & Andriantsitohaina, R. (2011). Circulating microparticles from septic shock patients exert differential tissue expression of enzymes related to inflammation and oxidative stress. Critical Care Medicine, 39(7), 1739-1748.
Mosser, D. M., & Edwards, J. P. (2008). Exploring the full spectrum of macrophage activation. Nature Reviews Immunology, 8(12), 958-969. https://doi.org/10.1038/nri2448
Murakami, M., Naraba, H., Tanioka, T., Semmyo, N., Nakatani, Y., Kojima, F., Ikeda, T., Fueki, M., Ueno, A., Oh-Ishi, S., & Kudo, I. (2000). Regulation of prostaglandin E2 biosynthesis by inducible membrane-associated prostaglandin E2 synthase that acts in concert with cyclooxygenase-2. Journal of Biological Chemistry, 275(42), 32783-32792.
Murray, P. J. (2017). Macrophage polarization. Annual Review of Physiology, 79, 541-566.
Na, Yi R., Jung, D., Yoon, Bo R., Lee, W. W., & Seok, S. H. (2015). Endogenous prostaglandin E2 potentiates anti-inflammatory phenotype of macrophage through the CREB-C/EBP-β cascade. European Journal of Immunology, 45(9), 2661-2671.
Nakayama, T., Mutsuga, N., Yao, L., & Tosato, G. (2006). Prostaglandin E2 promotes degranulation-independent release of MCP-1 from mast cells. Journal of Leukocyte Biology, 79(1), 95-104.
Nakazaki, M., Morita, T., Lankford, K. L., Askenase, P. W., & Kocsis, J. D. (2021). Small extracellular vesicles released by infused mesenchymal stromal cells target M2 macrophages and promote TGF-β upregulation, microvascular stabilization and functional recovery in a rodent model of severe spinal cord injury. Journal of Extracellular Vesicles, 10(1), e12137.
Nathan, C., & Ding, A. (2010). Nonresolving inflammation. Cell, 140(6), 871-882.
Oliveira, G. P., Porto, W. F., Palu, C. C., Pereira, L. M., Petriz, B., Almeida, J. A., Viana, J., Filho, N. N. A., Franco, O. L., & Pereira, R. W. (2018). Effects of acute aerobic exercise on rats serum extracellular vesicles diameter, concentration and small RNAs content. Frontiers in Physiology, 9(MAY), 1-11.
Ostalecki, C., Wittki, S., Lee, J.-H., Geist, M. M., Tibroni, N., Harrer, T., Schuler, G., Fackler, O. T., & Baur, A. S. (2016). HIV Nef- and Notch1-dependent endocytosis of ADAM17 induces vesicular TNF secretion in chronic HIV infection. EBioMedicine, 13, 294-304.
Otahal, A., Kramer, K., Kuten-Pella, O., Moser, L. B., Neubauer, M., Lacza, Z., Nehrer, S., & De Luna, A. (2021). Effects of extracellular vesicles from blood-derived products on osteoarthritic chondrocytes within an inflammation model. International Journal of Molecular Sciences, 22(13), 1-15.
Park, J. E., Dutta, B., Tse, S. W., Gupta, N., Tan, C. F., Low, J. K., Yeoh, K. W., Kon, Oi L., Tam, J. P., & Sze, S. K. (2019). Hypoxia-induced tumor exosomes promote M2-like macrophage polarization of infiltrating myeloid cells and microRNA-mediated metabolic shift. Oncogene, 38(26), 5158-5173.
Pérez, P. S., Romaniuk, M. A., Duette, G. A., Zhao, Z., Huang, Y., Martin-Jaular, L., Witwer, K. W., Théry, C., & Ostrowski, M. (2019). Extracellular vesicles and chronic inflammation during HIV infection. Journal of Extracellular Vesicles, 8(1), 1687275.
Phipps, R. P., Stein, S. H., & Roper, R. L. (1991). A new view of prostaglandin E regulation of the immune response. Immunology Today, 12(10), 349-352.
Plebanek, M. P., Angeloni, N. L., Vinokour, E., Li, J., Henkin, A., Martinez-Marin, D., Filleur, S., Bhowmick, R., Henkin, J., Miller, S. D., Ifergan, I., Lee, Y., Osman, I., Thaxton, C. S., & Volpert, O. V. (2017). Pre-metastatic cancer exosomes induce immune surveillance by patrolling monocytes at the metastatic niche. Nature Communications, 8, 1319.
Qian, M., Wang, S., Guo, X., Wang, J., Zhang, Z., Qiu, W., Gao, X., Chen, Z., Xu, J., Zhao, R., Xue, H., & Li, G. (2020). Hypoxic glioma-derived exosomes deliver microRNA-1246 to induce M2 macrophage polarization by targeting TERF2IP via the STAT3 and NF-κB pathways. Oncogene, 39(2), 428-442.
Quinn, J. F., Patel, T., Wong, D., Das, S., Freedman, J. E., Laurent, L. C., Carter, B. S., Hochberg, F., Keuren-Jensen, K. V., Huentelman, M., Spetzler, R., S Kalani, M. Y., Arango, J., Adelson, P. D., Weiner, H. L., Gandhi, R., Goilav, B., Putterman, C., & Saugstad, J. A. (2015). Extracellular RNAs: Development as biomarkers of human disease. Journal of Extracellular Vesicles, 4(1), 27495.
Rabinowits, G., Gerçel-Taylor, C., Day, J. M., Taylor, D. D., & Kloecker, G. H. (2009). Exosomal microRNA: A diagnostic marker for lung cancer. Clinical Lung Cancer, 10(1), 42-46.
Regan, J. W., Bailey, T. J., Pepperl, D. J., Pierce, K. L., Bogardus, A. M., Donello, J. E., Fairbairn, C. E., Kedzie, K. M., Woodward, D. F., & Gil, D. W. (1994). Cloning of a novel human prostaglandin receptor with characteristics of the pharmacologically defined EP2 subtype. Molecular Pharmacology, 46(2), 213-220.
Rossaint, J., Kühne, K., Skupski, J., Van Aken, H., Looney, M. R., Hidalgo, A., & Zarbock, A. (2016). Directed transport of neutrophil-derived extracellular vesicles enables platelet-mediated innate immune response. Nature Communications, 7, 13464.
Ruffell, D., Mourkioti, F., Gambardella, A., Kirstetter, P., Lopez, R. G., Rosenthal, N., & Nerlov, C. (2009). A CREB-C/EBPβ cascade induces M2 macrophage-specific gene expression and promotes muscle injury repair. PNAS, 106(41), 17475-17480.
Scher, J. U., & Pillinger, M. H. (2009). The anti-inflammatory effects of prostaglandins, The Journal of Investigative Medicine, 57(6), 703-709.
Serhan, C. N., & Levy, B. (2003). Success of prostaglandin E2 in structure-function is a challenge for structure-based therapeutics. PNAS, 100(15), 8609-8611.
Serhan, C. N., & Savill, J. (2005). Resolution of inflammation: The beginning programs the end. Nature Immunology, 6(12), 1191-1197.
Shaywitz, A. J., & Greenberg, M. E. (1999). CREB: A stimulus-induced transcription factor activated by a diverse array of extracellular signals. Annual Review of Biochemistry, 68, 821-861.
Sokolowska, M., Chen, L.-Y., Liu, Y., Martinez-Anton, A., Qi, H.-Y., Logun, C., Alsaaty, S., Park, Y. H., Kastner, D L., Chae, J. J., & Shelhamer, J. H. (2015). Prostaglandin E2 inhibits NLRP3 inflammasome activation through EP4 receptor and intracellular cyclic AMP in human macrophages. Journal of Immunology, 194(11), 5472-5487.
Subra, C., Grand, D., Laulagnier, K., Stella, A., Lambeau, G., Paillasse, M., De Medina, P., Monsarrat, B., Perret, B., Silvente-Poirot, S., Poirot, M., & Record, M. (2010). Exosomes account for vesicle-mediated transcellular transport of activatable phospholipases and prostaglandins. Journal of Lipid Research, 51(8), 2105-2120.
Suda, M., Tanaka, K., Yasoda, A., Natsui, K., Sakuma, Y., Tanaka, I., Ushikubi, F., Narumiya, S., & Nakao, K. (1998). Prostaglandin E2 (PGE2) autoamplifies its production through EP1 subtype of PGE receptor in mouse osteoblastic MC3T3-E1 cells. Calcified Tissue International, 62(4), 327-331.
Tai, H.-H., Ensor, C. M., Tong, M., Zhou, H., & Yan, F. (2002). Prostaglandin catabolizing enzymes. Prostaglandins & Other Lipid Mediators, 68-69, 483-493.
Takayama, K., Garcı́a-Cardeña, G., Sukhova, G. K., Comander, J., Gimbrone, M. A., & Libby, P. (2002). Prostaglandin E2 suppresses chemokine production in human macrophages through the EP4 receptor. Journal of Biological Chemistry, 277(46), 44147-44154.
Taylor, D. D., & Gercel-Taylor, C. (2008). MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecologic Oncology, 110(1), 13-21.
Théry, C., Ostrowski, M., & Segura, E. (2009). Membrane vesicles as conveyors of immune responses. Nature Reviews Immunology, 9(8), 581-593.
Théry, C., Witwer, K. W., Aikawa, E., Alcaraz, M. J., Anderson, J. D., Andriantsitohaina, R., Antoniou, A., Arab, T., Archer, F., Atkin-Smith, G. K., Ayre, D. C., Bach, J.-M., Bachurski, D., Baharvand, H., Balaj, L., Baldacchino, S., Bauer, N. N., Baxter, A. A., Bebawy, M., … Zuba-Surma, E. K. (2018). Minimal information for studies of extracellular vesicles 2018 (MISEV2018): A position statement of the international society for extracellular vesicles and update of the MISEV2014 guidelines. Journal of Extracellular Vesicles, 7(1), 1535750.
Tkach, M., Thalmensi, J., Timperi, E., Gueguen, P., Névo, N., Grisard, E., Sirven, P., Cocozza, F., Gouronnec, A., Martin-Jaular, L., Jouve, M., Delisle, F., Manel, N., Rookhuizen, D. C., Guerin, C. L., Soumelis, V., Romano, E., Segura, E., & Théry, C. (2022). Extracellular vesicles from triple negative breast cancer promote pro-inflammatory macrophages associated with better clinical outcome. PNAS, 119(17), 1-12.
Vacchi, E., Burrello, J., Di Silvestre, D., Burrello, A., Bolis, S., Mauri, P., Vassalli, G., Cereda, C W., Farina, C., Barile, L., Kaelin-Lang, A., & Melli, G. (2020). Immune profiling of plasma-derived extracellular vesicles identifies Parkinson disease. Neurology: Neuroimmunology and NeuroInflammation, 7(6), e866.
Van Deun, J., Mestdagh, P., Agostinis, P., Akay, Ö., Anand, S., Anckaert, J., Martinez, Z. A., Baetens, T., Beghein, E., Bertier, L., Berx, G., Boere, J., Boukouris, S., Bremer, M., Buschmann, D., Byrd, J. B., Casert, C., Cheng, L., … Hendrix, A. (2017). EV-TRACK: Transparent reporting and centralizing knowledge in extracellular vesicle research. Nature Methods, 14, 228-232.
Vannella, K. M., & Wynn, T. A. (2017). Mechanisms of organ injury and repair by macrophages. Annual Review of Physiology, 79(November), 593-617.
Verweij, F. J., Revenu, C., Arras, G., Dingli, F., Loew, D., Pegtel, D. M., Follain, G., Allio, G., Goetz, J. G., Zimmermann, P., Herbomel, P., Del Bene, F., Raposo, G., & Van Niel, G. (2019). Live tracking of inter-organ communication by endogenous exosomes in vivo. Developmental Cell, 48(4), 573-589.e4.e4.
Wang, X. S., & Lau, H. Y. A. (2006). Prostaglandin E potentiates the immunologically stimulated histamine release from human peripheral blood-derived mast cells through EP1/EP3 receptors. Allergy, 61(4), 503-506.
Weller, C. L., Collington, S. J., Hartnell, A., Conroy, D. M., Kaise, T., Barker, J. E., Wilson, M. S., Taylor, G. W., Jose, P. J., & Williams, T. J. (2007). Chemotactic action of prostaglandin E2 on mouse mast cells acting via the PGE2 receptor 3. PNAS, 104(28), 11712-11717.
Wen, A. Y., Sakamoto, K. M., & Miller, L. S. (2010). The role of the transcription factor CREB in immune function. Journal of Immunology, 185(11), 6413-6419.
Wong, W.-Y., Lee, M. M.-L., Chan, B. D., Kam, R. K.-T., Zhang, G., Lu, Ai-P., & Tai, W. C.-S. (2016). Proteomic profiling of dextran sulfate sodium induced acute ulcerative colitis mice serum exosomes and their immunomodulatory impact on macrophages. Proteomics, 16(7), 1131-1145.
Wu, J., Piao, Y., Liu, Q., & Yang, X. (2021). Platelet-rich plasma-derived extracellular vesicles: A superior alternative in regenerative medicine? Cell Proliferation, 54(12), 1-13.
Xiang, X., Poliakov, A., Liu, C., Liu, Y., Deng, Z.-B., Wang, J., Cheng, Z., Shah, S. V., Wang, G.-J., Zhang, L., Grizzle, W. E., Mobley, J., & Zhang, H.-G. (2009). Induction of myeloid-derived suppressor cells by tumor exosomes. International Journal of Cancer, 124(11), 2621-2633.
Y, Y., & Chadee, K. (1998). Prostaglandin E2 stimulates IL-8 gene expression in human colonic epithelial cells by a posttranscriptional mechanism. Journal of Immunology, 161(7), 3746-3752.
Yan, F., Zhong, Z., Wang, Y., Feng, Y., Mei, Z., Li, H., Chen, X., Cai, L., & Li, C. (2020). Exosome-based biomimetic nanoparticles targeted to inflamed joints for enhanced treatment of rheumatoid arthritis. Journal of Nanobiotechnology, 18(1), 115.
Yoshida, M., Satoh, A., Lin, J. B., Mills, K. F., Sasaki, Y., Rensing, N., Wong, M., Apte, R. S., & Imai, S.-I. (2019). Extracellular vesicle-contained eNAMPT delays aging and extends lifespan in mice. Cell Metabolism, 30(2), 329-342.e5.e5.
Yuyama, K., Sun, H., Mitsutake, S., & Igarashi, Y. (2012). Sphingolipid-modulated exosome secretion promotes clearance of amyloid-β by microglia. Journal of Biological Chemistry, 287(14), 10977-10989. https://doi.org/10.1074/jbc.M111.324616