NOX2 and NOX4 expression in monocytes and macrophages-extracellular vesicles in signalling and therapeutics

. 2024 ; 12 () : 1342227. [epub] 20240416

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid38690564

Extracellular vesicles (EVs) are a type of cytoplasmic vesicles secreted by a variety of cells. EVs originating from cells have been known to participate in cell communication, antigen presentation, immune cell activation, tolerance induction, etc. These EVs can also carry the active form of Nicotinamide Adenine Dinucleotide Phosphate Oxidase Hydrogen (NADPH) oxidase, which is very essential for the production of reactive oxygen species (ROS) and that can then modulate processes such as cell regeneration. The aim of this study is to characterize the EVs isolated from U-937 and THP-1 cells, identify the NADPH oxidase (NOX) isoforms, and to determine whether EVs can modulate NOX4 and NOX2 in monocytes and macrophages. In our study, isolated EVs of U-937 were characterized using dynamic light scattering (DLS) spectroscopy and immunoblotting. The results showed that the exogenous addition of differentiation agents (either phorbol 12-myristate 13-acetate (PMA) or ascorbic acid) or the supplementation of EVs used in the study did not cause any stress leading to alterations in cell proliferation and viability. In cells co-cultured with EVs for 72 h, strong suppression of NOX4 and NOX2 is evident when monocytes transform into macrophagic cells. We also observed lower levels of oxidative stress measured using immunoblotting and electron paramagnetic resonance spectroscopy under the EVs co-cultured condition, which also indicates that EVs might contribute significantly by acting as an antioxidant source, which agrees with previous studies that hypothesized the role of EVs in therapeutics. Therefore, our results provide evidence for NOX regulation by EVs in addition to its role as an antioxidant cargo.

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Ayala A., Munoz M. F., Arguelles S. (2014). Lipid peroxidation: production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxid. Med. Cell Longev. 2014, 360438. 10.1155/2014/360438 PubMed DOI PMC

Barile L., Vassalli G. (2017). Exosomes: therapy delivery tools and biomarkers of diseases. Pharmacol. Ther. 174, 63–78. 10.1016/j.pharmthera.2017.02.020 PubMed DOI

Bedard K., Krause K.-H. (2007). The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol. Rev. 87 (1), 245–313. 10.1152/physrev.00044.2005 PubMed DOI

Bermudez S., Khayrullina G., Zhao Y. J., Byrnes K. R. (2016). NADPH oxidase isoform expression is temporally regulated and may contribute to microglial/macrophage polarization after spinal cord injury. Mol. Cell. Neurosci. 77, 53–64. 10.1016/j.mcn.2016.10.001 PubMed DOI PMC

Chen H. W., Chengalvala V., Hu H. X., Sun D. X. (2021). Tumor-derived exosomes: nanovesicles made by cancer cells to promote cancer metastasis. Acta Pharm. Sin. B 11 (8), 2136–2149. 10.1016/j.apsb.2021.04.012 PubMed DOI PMC

Dalrymple A., McEwan M., Brandt M., Bielfeldt S., Bean E. J., Moga A., et al. (2022). A novel clinical method to measure skin staining reveals activation of skin damage pathways by cigarette smoke. Skin Res. Technol. 28 (1), 162–170. 10.1111/srt.13108 PubMed DOI PMC

Di Bella M. A. (2022). Overview and update on extracellular vesicles: considerations on exosomes and their application in modern medicine. Biology-Basel 11 (6), 804. 10.3390/biology11060804 PubMed DOI PMC

Doyle L. M., Wang M. Z. (2019). Overview of extracellular vesicles, their origin, composition, purpose, and methods for exosome isolation and analysis. Cells 8 (7), 727. 10.3390/cells8070727 PubMed DOI PMC

Engering A., Kuhn L., Fluitsma D., Hoefsmit E., Pieters J. (2003). Differential post-translational modification of CD63 molecules during maturation of human dendritic cells. Eur. J. Biochem. 270 (11), 2412–2420. 10.1046/j.1432-1033.2003.03609.x PubMed DOI

Gao L., Wang L., Dai T., Jin K., Zhang Z. K., Wang S., et al. (2018). Tumor-derived exosomes antagonize innate antiviral immunity. Nat. Immunol. 19 (3), 233–245. 10.1038/s41590-017-0043-5 PubMed DOI

Gao P., Li X., Du X., Liu S., Xu Y., Qi D., et al. (2021). Intermediate effects of body mass index and C-reactive protein on the serum cotinine- leukocyte telomere length association. Front. Aging Neurosci. 13, 827465. 10.3389/fnagi.2021.827465 PubMed DOI PMC

Genneback N., Hellman U., Malm L., Larsson G., Ronquist G., Waldenstrom A., et al. (2013). Growth factor stimulation of cardiomyocytes induces changes in the transcriptional contents of secreted exosomes. J. Extracell. Vesicles 2 (1). 10.3402/jev.v2i0.20167 PubMed DOI PMC

Gonzalez A., Valeiras M., Sidransky E., Tayebi N. (2014). Lysosomal integral membrane protein-2: a new player in lysosome-related pathology. Mol. Genet. Metabolism 111 (2), 84–91. 10.1016/j.ymgme.2013.12.005 PubMed DOI PMC

Hahner F., Moll F., Schroder K. (2020). NADPH oxidases in the differentiation of endothelial cells. Cardiovasc. Res. 116 (2), 262–268. 10.1093/cvr/cvz213 PubMed DOI

Hervera A., De Virgiliis F., Palmisano I., Zhou L. M., Tantardini E., Kong G. P., et al. (2018). Reactive oxygen species regulate axonal regeneration through the release of exosomal NADPH oxidase 2 complexes into injured axons. Nat. Cell Biol. 20 (3), 307–319. 10.1038/s41556-018-0039-x PubMed DOI

Johnson S. M., Banyard A., Smith C., Mironov A., McCabe M. G. (2020). Large extracellular vesicles can be characterised by multiplex labelling using imaging flow cytometry. Int. J. Mol. Sci. 21 (22), 8723. 10.3390/ijms21228723 PubMed DOI PMC

Jung K. K., Liu X. W., Chirco R., Fridman R., Kim H. R. C. (2006). Identification of CD63 as a tissue inhibitor of metalloproteinase-1 interacting cell surface protein. Embo J. 25 (17), 3934–3942. 10.1038/sj.emboj.7601281 PubMed DOI PMC

Kalluri R., LeBleu V. S. (2020). The biology, function, and biomedical applications of exosomes. Science 367 (6478), eaau6977. 10.1126/science.aau6977 PubMed DOI PMC

Kim T. H., Hong S. B., Lim C. M., Koh Y., Jang E. Y., Huh J. W. (2019). The role of exosomes in bronchoalveloar lavage from patients with acute respiratory distress syndrome. J. Clin. Med. 8 (8), 1148. 10.3390/jcm8081148 PubMed DOI PMC

Krishnamoorthy L., Chang C. J. (2018). Exosomal NADPH oxidase: delivering redox signaling for healing. Biochemistry 57 (27), 3993–3994. 10.1021/acs.biochem.8b00429 PubMed DOI PMC

Landry W. D., Cotter T. G. (2014). ROS signalling, NADPH oxidases and cancer. Biochem. Soc. Trans. 42, 934–938. 10.1042/BST20140060 PubMed DOI

Lau N. C. H., Yam J. W. P. (2023). From exosome biogenesis to absorption: key takeaways for cancer research. Cancers 15 (7), 1992. 10.3390/cancers15071992 PubMed DOI PMC

Lin T. Y., Chang T. M., Huang H. C. (2022). Extracellular vesicles derived from human umbilical cord mesenchymal stem cells attenuate mast cell activation. Antioxidants 11 (11), 2279. 10.3390/antiox11112279 PubMed DOI PMC

Manoharan R. R., Sedlářová M., Pospíšil P., Prasad A. (2023). Detection and characterization of free oxygen radicals induced protein adduct formation in differentiating macrophages. Biochimica biophysica acta. General Subj. 1867 (5), 130324. 10.1016/j.bbagen.2023.130324 PubMed DOI

Mathieu M., Nevo N., Jouve M., Valenzuela J. I., Maurin M., Verweij F. J., et al. (2021). Specificities of exosome versus small ectosome secretion revealed by live intracellular tracking of CD63 and CD9. Nat. Commun. 12 (1), 4389. 10.1038/s41467-021-24384-2 PubMed DOI PMC

Mittler R., Vanderauwera S., Suzuki N., Miller G., Tognetti V. B., Vandepoele K., et al. (2011). ROS signaling: the new wave? Trends Plant Sci. 16 (6), 300–309. 10.1016/j.tplants.2011.03.007 PubMed DOI

Muthu S., Bapat A., Jain R., Jeyaraman N., Jeyaraman M. (2021). Exosomal therapy-a new frontier in regenerative medicine. Stem Cell Investig. 8, 7. 10.21037/sci-2020-037 PubMed DOI PMC

Nederveen J. P., Warnier G., Di Carlo A., Nilsson M. I., Tarnopolsky M. A. (2021). Extracellular vesicles and exosomes: insights from exercise science. Front. Physiology 11, 604274. 10.3389/fphys.2020.604274 PubMed DOI PMC

Pospíšil P., Prasad A., Rác M. (2019). Mechanism of the formation of electronically excited species by oxidative metabolic processes: role of reactive oxygen species. Biomolecules 9 (7), 258. 10.3390/biom9070258 PubMed DOI PMC

Pou S., Ramos C. L., Gladwell T., Renks E., Centra M., Young D., et al. (1994). A kinetic approach to the selection of a sensitive spin-trapping system for the detection of hydroxyl radical. Anal. Biochem. 217 (1), 76–83. 10.1006/abio.1994.1085 PubMed DOI

Prasad A., Duchová H., Manoharan R. R., Rathi D., Pospíšil P. (2023). Imaging and characterization of oxidative protein modifications in skin. Int. J. Mol. Sci. 24 (4), 3981. 10.3390/ijms24043981 PubMed DOI PMC

Prasad A., Manoharan R. R., Sedlářová M., Pospíšil P. (2021). Free radical-mediated protein radical formation in differentiating monocytes. Int. J. Mol. Sci. 22 (18), 9963. 10.3390/ijms22189963 PubMed DOI PMC

Shelke G. V., Lasser C., Gho Y. S., Lotvall J. (2014). Importance of exosome depletion protocols to eliminate functional and RNA-containing extracellular vesicles from fetal bovine serum. J. Extracell. Vesicles 3 (1). 10.3402/jev.v3.24783 PubMed DOI PMC

Shu S. L., Allen C. L., Benjamin-Davalos S., Koroleva M., MacFarland D., Minderman H., et al. (2021). A rapid exosome isolation using ultrafiltration and size exclusion chromatography (REIUS) method for exosome isolation from melanoma cell lines. MELANOMA Methods Protoc. 2265, 289–304. 10.1007/978-1-0716-1205-7_22 PubMed DOI PMC

Song M. G., Ryoo I. G., Choi H. Y., Choi B. H., Kim S. T., Heo T. H., et al. (2015). NRF2 signaling negatively regulates phorbol-12-myristate-13-acetate (PMA)-Induced differentiation of human monocytic U937 cells into pro-inflammatory macrophages. Plos One 10 (7), e0134235. 10.1371/journal.pone.0134235 PubMed DOI PMC

Song Y. F., Wang B. C., Zhu X. L., Hu J. L., Sun J. J., Xuan J. Z., et al. (2021). Human umbilical cord blood-derived MSCs exosome attenuate myocardial injury by inhibiting ferroptosis in acute myocardial infarction mice. Cell Biol. Toxicol. 37 (1), 51–64. 10.1007/s10565-020-09530-8 PubMed DOI

Surman M., Stepien E., Hoja-Lukowicz D., Przybylo M. (2017). Deciphering the role of exosomes in cancer development and progression: focus on the proteome. Clin. Exp. Metastasis 34 (3-4), 273–289. 10.1007/s10585-017-9844-z PubMed DOI PMC

Suzuki Y. J., Carini M., Butterfield D. A. (2010). Protein carbonylation. Antioxid. Redox Signal 12 (3), 323–325. 10.1089/ars.2009.2887 PubMed DOI PMC

Takahashi A., Okada R., Nagao K., Kawamata Y., Hanyu A., Yoshimoto S., et al. (2017). Exosomes maintain cellular homeostasis by excreting harmful DNA from cells. Nat. Commun. 8, 15287. 10.1038/ncomms15287 PubMed DOI PMC

Thakur A., Parra D. C., Motallebnejad P., Brocchi M., Chen H. J. (2022). Exosomes: small vesicles with big roles in cancer, vaccine development, and therapeutics. Bioact. Mater. 10, 281–294. 10.1016/j.bioactmat.2021.08.029 PubMed DOI PMC

Tola A. J., Jaballi A., Missihoun T. D. (2021). Protein carbonylation: emerging roles in plant redox biology and future prospects. Plants-Basel 10 (7), 1451. 10.3390/plants10071451 PubMed DOI PMC

Tsikas D. (2017). Assessment of lipid peroxidation by measuring malondialdehyde (MDA) and relatives in biological samples: analytical and biological challenges. Anal. Biochem. 524, 13–30. 10.1016/j.ab.2016.10.021 PubMed DOI

van Niel G., D'Angelo G., Raposo G. (2018). Shedding light on the cell biology of extracellular vesicles. Nat. Rev. Mol. Cell Biol. 19 (4), 213–228. 10.1038/nrm.2017.125 PubMed DOI

Yan Y. M., Jiang W. Q., Tan Y. W., Zou S. Q., Zhang H. G., Mao F., et al. (2017). hucMSC exosome-derived GPX1 is required for the recovery of hepatic oxidant injury. Mol. Ther. 25 (2), 465–479. 10.1016/j.ymthe.2016.11.019 PubMed DOI PMC

Zhang M., Hu S., Liu L., Dang P., Liu Y., Sun Z., et al. (2023). Engineered exosomes from different sources for cancer-targeted therapy. Signal Transduct. Target. Ther. 8 (1), 124. 10.1038/s41392-023-01382-y PubMed DOI PMC

Zhang W. J., Liu R., Chen Y. H., Wang M. H., Du J. (2022). Crosstalk between oxidative stress and exosomes. Oxidative Med. Cell. Longev. 2022, 1–11. 10.1155/2022/3553617 PubMed DOI PMC

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