{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,12,24]],"date-time":"2025-12-24T21:37:20Z","timestamp":1766612240422,"version":"build-2065373602"},"reference-count":105,"publisher":"MDPI AG","issue":"5","license":[{"start":{"date-parts":[[2025,4,30]],"date-time":"2025-04-30T00:00:00Z","timestamp":1745971200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100004281","name":"National Science Center in Poland (Narodowe Centrum Nauki, NCN)","doi-asserted-by":"publisher","award":["2024\/08\/X\/NZ7\/00029"],"award-info":[{"award-number":["2024\/08\/X\/NZ7\/00029"]}],"id":[{"id":"10.13039\/501100004281","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Antioxidants"],"abstract":"<jats:p>Nannochloropsis oceanica and Chlorococcum amblystomatis exhibit significant potential for protecting skin cells from oxidative stress-induced metabolic dysfunctions, owing to their high bioactive lipid content. This study aimed to evaluate their cytoprotective effects on the ultraviolet A (UVA)-perturbed proteome of 3D-cultured skin fibroblasts, using high-throughput proteomics. Chlorococcum amblystomatis lipid extract promoted a reduction in UVA-induced cytochrome c oxidase subunit 4 isoform 1 and cell death protein 6 levels, alongside the restoration of ferritin light chain expression diminished by UVA. It downregulated the expression of ubiquitin-conjugating enzyme E2 and lactoylglutathione lyase, which were upregulated by UVA. Furthermore, the elevated superoxide dismutase [Mn] mitochondrial levels in the caspase-1 interactome emphasized the lipid extract\u2019s role in mitigating oxidative stress-associated chronic inflammation by regulating caspase-1 activity. In addition to this notable redox balance-regulating and cytoprotective activity, conversely, the protein inflammation signaling mediated by UVA was regulated in terms of wound healing potential in the case of Nannochloropsis oceanica lipid extract. Following UVA radiation, it promoted the upregulation of complement component B, thrombospondin-1, MMP1, and fibulin-1. The results revealed that both lipid extracts effectively reversed the UVA-perturbed proteomic profile of fibroblasts, highlighting their therapeutic potential in protecting the skin from UV radiation.<\/jats:p>","DOI":"10.3390\/antiox14050545","type":"journal-article","created":{"date-parts":[[2025,5,2]],"date-time":"2025-05-02T08:28:11Z","timestamp":1746174491000},"page":"545","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":1,"title":["The Effects of Lipid Extracts from Microalgae Chlorococcum amblystomatis and Nannochloropsis oceanica on the Proteome of 3D-Cultured Fibroblasts Exposed to UVA Radiation"],"prefix":"10.3390","volume":"14","author":[{"given":"Sinemyiz","family":"Atalay Ekiner","sequence":"first","affiliation":[{"name":"Department of Analytical Chemistry, Medical University of Bialystok, Mickiewicza 2D, 15-222 Bialystok, Poland"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5240-1346","authenticated-orcid":false,"given":"Agnieszka","family":"G\u0119gotek","sequence":"additional","affiliation":[{"name":"Department of Analytical Chemistry, Medical University of Bialystok, Mickiewicza 2D, 15-222 Bialystok, Poland"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5357-3601","authenticated-orcid":false,"given":"Maria Ros\u00e1rio","family":"Domingues","sequence":"additional","affiliation":[{"name":"Mass Spectrometry Centre, LAQV-REQUIMTE, Department of Chemistry, University of Aveiro, Santiago University Campus, 3810-193 Aveiro, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8060-7675","authenticated-orcid":false,"given":"Pedro","family":"Domingues","sequence":"additional","affiliation":[{"name":"Mass Spectrometry Centre, LAQV-REQUIMTE, Department of Chemistry, University of Aveiro, Santiago University Campus, 3810-193 Aveiro, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5397-7139","authenticated-orcid":false,"given":"El\u017cbieta","family":"Skrzydlewska","sequence":"additional","affiliation":[{"name":"Department of Analytical Chemistry, Medical University of Bialystok, Mickiewicza 2D, 15-222 Bialystok, Poland"}]}],"member":"1968","published-online":{"date-parts":[[2025,4,30]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s13008-024-00107-z","article-title":"Role of reactive oxygen species in ultraviolet-induced photodamage of the skin","volume":"19","author":"Wei","year":"2024","journal-title":"Cell Div."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1007\/978-3-319-56017-5_2","article-title":"Ultraviolet Light Induced Generation of Reactive Oxygen Species","volume":"996","author":"Cockrell","year":"2017","journal-title":"Adv. Exp. Med. Biol."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Hunt, M., Torres, M., Bachar-Wikstrom, E., and Wikstrom, J.D. (2024). Cellular and molecular roles of reactive oxygen species in wound healing. Commun. Biol., 7.","DOI":"10.1038\/s42003-024-07219-w"},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Wang, G., Yang, F., Zhou, W., Xiao, N., Luo, M., and Tang, Z. (2023). The initiation of oxidative stress and therapeutic strategies in wound healing. Biomed. Pharmacother., 157.","DOI":"10.1016\/j.biopha.2022.114004"},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Jakovija, A., and Chtanova, T. (2023). Skin immunity in wound healing and cancer. Front. Immunol., 14.","DOI":"10.3389\/fimmu.2023.1060258"},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Conde, T., Neves, B., Couto, D., Melo, T., Lopes, D., Pais, R., Batista, J., Cardoso, H., Silva, J.L., and Domingues, P. (2023). Polar Lipids of Marine Microalgae Nannochloropsis oceanica and Chlorococcum amblystomatis Mitigate the LPS-Induced Pro-Inflammatory Response in Macrophages. Mar. Drugs, 21.","DOI":"10.3390\/md21120629"},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Khan, A.Q., Agha, M.V., Sheikhan, K.S.A.M., Younis, S.M., Al Tamimi, M., Alam, M., Ahmad, A., Uddin, S., Buddenkotte, J., and Steinhoff, M. (2022). Targeting deregulated oxidative stress in skin inflammatory diseases: An update on clinical importance. Biomed. Pharmacother., 154.","DOI":"10.1016\/j.biopha.2022.113601"},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Emanuelli, M., Sartini, D., Molinelli, E., Campagna, R., Pozzi, V., Salvolini, E., Simonetti, O., Campanati, A., and Offidani, A. (2022). The Double-Edged Sword of Oxidative Stress in Skin Damage and Melanoma: From Physiopathology to Therapeutical Approaches. Antioxidants, 11.","DOI":"10.3390\/antiox11040612"},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"\u0141uczaj, W., G\u0119gotek, A., Conde, T., Domingues, M.R., Domingues, P., and Skrzydlewska, E. (2023). Lipidomic assessment of the impact of Nannochloropsis oceanica microalga lipid extract on human skin keratinocytes exposed to chronic UVB radiation. Sci. Rep., 13.","DOI":"10.1038\/s41598-023-49827-2"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"102718","DOI":"10.1016\/j.algal.2022.102718","article-title":"Effects of outdoor and indoor cultivation on the polar lipid composition and antioxidant activity of Nannochloropsis oceanica and Nannochloropsis limnetica: A lipidomics perspective","volume":"64","author":"Couto","year":"2022","journal-title":"Algal Res."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Correia, N., Pereira, H., Schulze, P.S.C., Costa, M.M., Santo, G.E., Guerra, I., Trov\u00e3o, M., Barros, A., Cardoso, H., and Silva, J.L. (2023). Heterotrophic and Photoautotrophic Media Optimization Using Response Surface Methodology for the Novel Microalga Chlorococcum amblystomatis. Appl. Sci., 13.","DOI":"10.3390\/app13042089"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"102395","DOI":"10.1016\/j.algal.2021.102395","article-title":"Application of microalgae and microalgal bioactive compounds in skin regeneration","volume":"58","author":"Miguel","year":"2021","journal-title":"Algal Res."},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Biernacki, M., Conde, T., Stasiewicz, A., Sura\u017cy\u0144ski, A., Domingues, M.R., Domingues, P., and Skrzydlewska, E. (2023). Restorative Effect of Microalgae Nannochloropsis oceanica Lipid Extract on Phospholipid Metabolism in Keratinocytes Exposed to UVB Radiation. Int. J. Mol. Sci., 24.","DOI":"10.3390\/ijms241814323"},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Stasiewicz, A., Conde, T., G\u0119gotek, A., Domingues, M.R., Domingues, P., and Skrzydlewska, E. (2023). Prevention of UVB Induced Metabolic Changes in Epidermal Cells by Lipid Extract from Microalgae Nannochloropsis oceanica. Int. J. Mol. Sci., 24.","DOI":"10.3390\/ijms241411302"},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Regueiras, A., Huguet, \u00c1., Conde, T., Couto, D., Domingues, P., Domingues, M.R., Costa, A.M., da Silva, J.L., Vasconcelos, V., and Urbatzka, R. (2022). Potential anti-obesity, anti-steatosis, and anti-inflammatory properties of extracts from the microalgae chlorella vulgaris and Chlorococcum amblystomatis under different growth conditions. Mar. Drugs, 20.","DOI":"10.3390\/md20010009"},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Stasiewicz, A., Conde, T., Domingues, M.d.R., Domingues, P., Biernacki, M., and Skrzydlewska, E. (2024). Comparison of the Regenerative Metabolic Efficiency of Lipid Extracts from Microalgae Nannochloropsis oceanica and Chlorococcum amblystomatis on Fibroblasts. Antioxidants, 13.","DOI":"10.3390\/antiox13030276"},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Ekiner, S.A., G\u0119gotek, A., Domingues, P., Domingues, M.R., and Skrzydlewska, E. (2024). Comparison of Microalgae Nannochloropsis oceanica and Chlorococcum amblystomatis Lipid Extracts Effects on UVA-Induced Changes in Human Skin Fibroblasts Proteome. Mar. Drugs, 22.","DOI":"10.3390\/md22110509"},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Urz\u00ec, O., Gasparro, R., Costanzo, E., De Luca, A., Giavaresi, G., Fontana, S., and Alessandro, R. (2023). Three-Dimensional Cell Cultures: The Bridge between In Vitro and In Vivo Models. Int. J. Mol. Sci., 24.","DOI":"10.3390\/ijms241512046"},{"key":"ref_19","first-page":"3216415","article-title":"Natural Exogenous Antioxidant Defense against Changes in Human Skin Fibroblast Proteome Disturbed by UVA Radiation","volume":"2020","author":"Domingues","year":"2020","journal-title":"Oxid. Med. Cell. Longev."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"3829","DOI":"10.3390\/cimb45050247","article-title":"Dermal Fibroblasts as the Main Target for Skin Anti-Age Correction Using a Combination of Regenerative Medicine Methods","volume":"45","author":"Zorina","year":"2023","journal-title":"Curr. Issues Mol. Biol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"292","DOI":"10.1016\/j.nrl.2021.10.003","article-title":"Relationship between inflammation and oxidative stress and its effect on multiple sclerosis","volume":"39","author":"Ortiz","year":"2024","journal-title":"Neurolog\u00eda"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"36","DOI":"10.1038\/s41421-020-0167-x","article-title":"Inflammasome activation and regulation: Toward a better understanding of complex mechanisms","volume":"6","author":"Zheng","year":"2020","journal-title":"Cell Discov."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Barros, A., Pereira, H., Campos, J., Marques, A., Varela, J., and Silva, J. (2019). Heterotrophy as a tool to overcome the long and costly autotrophic scale-up process for large scale production of microalgae. Sci. Rep., 9.","DOI":"10.1038\/s41598-019-50206-z"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"497","DOI":"10.1016\/S0021-9258(18)64849-5","article-title":"A simple method for the isolation and purification of total lipides from animal tissues","volume":"226","author":"Folch","year":"1957","journal-title":"J. Biol. Chem."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1007\/978-1-4939-3191-0_11","article-title":"AlgiMatrixTM-Based 3D Cell Culture System as an In Vitro Tumor Model: An Important Tool in Cancer Research","volume":"1379","author":"Godugu","year":"2016","journal-title":"Methods Mol. Biol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1016\/j.toxlet.2005.07.001","article-title":"In vitro cytotoxicity assays: Comparison of LDH, neutral red, MTT and protein assay in hepatoma cell lines following exposure to cadmium chloride","volume":"160","author":"Fotakis","year":"2006","journal-title":"Toxicol. Lett."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"248","DOI":"10.1016\/0003-2697(76)90527-3","article-title":"A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding","volume":"72","author":"Bradford","year":"1976","journal-title":"Anal. Biochem."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1016\/j.jpba.2018.03.068","article-title":"Proteomic plasma profile of psoriatic patients","volume":"155","author":"Domingues","year":"2018","journal-title":"J. Pharm. Biomed. Anal."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1367","DOI":"10.1038\/nbt.1511","article-title":"MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification","volume":"26","author":"Cox","year":"2008","journal-title":"Nat. Biotechnol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1423","DOI":"10.1093\/clinchem\/44.7.1423","article-title":"Quantitation of bcl-2 protein in bladder cancer tissue by enzyme immunoassay: Comparison with Western blot and immunohistochemistry","volume":"44","author":"Eissa","year":"1998","journal-title":"Clin. Chem."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1016\/j.ab.2016.08.009","article-title":"Simultaneous GC-MS\/MS measurement of malondialdehyde and 4-hydroxy-2-nonenal in human plasma: Effects of long-term L-arginine administration","volume":"524","author":"Tsikas","year":"2017","journal-title":"Anal. Biochem."},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"\u017darkovi\u0107, N., Jastrz\u0105b, A., Jarocka-Karpowicz, I., Orehovec, B., Bar\u0161i\u0107, B., Tarle, M., Kmet, M., Luk\u0161i\u0107, I., \u0141uczaj, W., and Skrzydlewska, E. (2022). The Impact of Severe COVID-19 on Plasma Antioxidants. Molecules, 27.","DOI":"10.3390\/molecules27165323"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"W398","DOI":"10.1093\/nar\/gkae253","article-title":"MetaboAnalyst 6.0: Towards a unified platform for metabolomics data processing, analysis and interpretation","volume":"52","author":"Pang","year":"2024","journal-title":"Nucleic Acids Res."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"30","DOI":"10.31083\/j.jin2302030","article-title":"Reproducibility in Preclinical in Vivo Research: Statistical Inferences","volume":"23","author":"Lim","year":"2024","journal-title":"J. Integr. Neurosci."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"231","DOI":"10.1177\/117693510700300008","article-title":"Statistical Issues and Analyses of in vivo and in vitro Genomic Data in order to Identify Clinically Relevant Profiles","volume":"3","author":"Poisson","year":"2007","journal-title":"Cancer Inform."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"606","DOI":"10.1038\/nrd.2018.99","article-title":"Concerns, challenges and promises of high-content analysis of 3D cellular models","volume":"17","author":"Carragher","year":"2018","journal-title":"Nat. Rev. Drug Discov."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"D447","DOI":"10.1093\/nar\/gku1003","article-title":"STRING v10: Protein-protein interaction networks, integrated over the tree of life","volume":"43","author":"Szklarczyk","year":"2015","journal-title":"Nucleic Acids Res."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"8","DOI":"10.1002\/pro.4218","article-title":"PANTHER: Making genome-scale phylogenetics accessible to all","volume":"31","author":"Thomas","year":"2022","journal-title":"Protein Sci."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"703","DOI":"10.1038\/s41596-019-0128-8","article-title":"Protocol Update for large-scale genome and gene function analysis with the PANTHER classification system (v.14.0)","volume":"14","author":"Mi","year":"2019","journal-title":"Nat. Protoc."},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Wickham, H. (2016). ggplot2: Elegant Graphics for Data Analysis, Springer.","DOI":"10.1007\/978-3-319-24277-4_9"},{"key":"ref_41","unstructured":"Wickham, H., Fran\u00e7ois, R., Henry, L., M\u00fcller, K., and Vaughan, D. (2025, January 15). dplyr: A Grammar of Data Manipulation. Available online: https:\/\/dplyr.tidyverse.org."},{"key":"ref_42","unstructured":"R Core Team (2025, January 15). R: A Language and Environment for Statistical Computing. Available online: https:\/\/www.R-project.org\/."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"5698931","DOI":"10.1155\/2016\/5698931","article-title":"Does the Interdependence between Oxidative Stress and Inflammation Explain the Antioxidant Paradox?","volume":"2016","author":"Biswas","year":"2016","journal-title":"Oxid. Med. Cell. Longev."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"3221","DOI":"10.1007\/s00018-016-2223-0","article-title":"Role of Nrf2\/HO-1 system in development, oxidative stress response and diseases: An evolutionarily conserved mechanism","volume":"73","author":"Loboda","year":"2016","journal-title":"Cell. Mol. Life Sci."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"826","DOI":"10.1016\/j.bbadis.2015.01.015","article-title":"On the role of 4-hydroxynonenal in health and disease","volume":"1852","author":"Csala","year":"2015","journal-title":"Biochim. Biophys. Acta (BBA)\u2014Mol. Basis Dis."},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Conde, T.A., Couto, D., Melo, T., Costa, M., Silva, J., Domingues, M.R., and Domingues, P. (2021). Polar lipidomic profile shows Chlorococcum amblystomatis as a promising source of value-added lipids. Sci. Rep., 11.","DOI":"10.1038\/s41598-021-83455-y"},{"key":"ref_47","doi-asserted-by":"crossref","unstructured":"G\u0119gotek, A., Conde, T., Domingues, M.R., Domingues, P., and Skrzydlewska, E. (2024). Impact of Nannochloropsis oceanica and Chlorococcum amblystomatis Extracts on UVA-Irradiated on 3D Cultured Melanoma Cells: A Proteomic Insight. Cells, 13.","DOI":"10.3390\/cells13231934"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"651","DOI":"10.1007\/s00109-020-01905-y","article-title":"Stress-mediated generation of deleterious ROS in healthy individuals\u2014Role of cytochrome c oxidase","volume":"98","author":"Ramzan","year":"2020","journal-title":"J. Mol. Med."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1016\/j.freeradbiomed.2014.10.508","article-title":"Mechanistic characterization of the thioredoxin system in the removal of hydrogen peroxide","volume":"78","author":"Pannala","year":"2015","journal-title":"Free Radic. Biol. Med."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"2775","DOI":"10.1016\/j.bbamcr.2014.06.015","article-title":"The effect of anti-inflammatory properties of ferritin light chain on lipopolysaccharide-induced inflammatory response in murine macrophages","volume":"1843","author":"Fan","year":"2014","journal-title":"Biochim. Biophys. Acta (BBA)\u2014Mol. Cell Res."},{"key":"ref_51","doi-asserted-by":"crossref","unstructured":"de Bari, L., Scir\u00e8, A., Minnelli, C., Cianfruglia, L., Kalapos, M.P., and Armeni, T. (2020). Interplay among Oxidative Stress, Methylglyoxal Pathway and S-Glutathionylation. Antioxidants, 10.","DOI":"10.3390\/antiox10010019"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1186\/s13075-018-1801-y","article-title":"Impairment of glyoxalase-1, an advanced glycation end-product detoxifying enzyme, induced by inflammation in age-related osteoarthritis","volume":"21","author":"Trellu","year":"2019","journal-title":"Arthritis Res. Ther."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1007\/s00403-024-02976-4","article-title":"Role of Ubiquitin-conjugating enzyme E2 (UBE2) in two immune-mediated inflammatory skin diseases: A mendelian randomization analysis","volume":"316","author":"Wang","year":"2024","journal-title":"Arch. Dermatol. Res."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"4385","DOI":"10.1038\/s41467-023-40054-x","article-title":"IL-1\u03b2 turnover by the UBE2L3 ubiquitin conjugating enzyme and HECT E3 ligases limits inflammation","volume":"14","author":"Mishra","year":"2023","journal-title":"Nat. Commun."},{"key":"ref_55","doi-asserted-by":"crossref","unstructured":"Mi, B., Chen, L., Xiong, Y., Yan, C., Xue, H., Panayi, A.C., Liu, J., Hu, L., Hu, Y., and Cao, F. (2020). Saliva exosomes-derived UBE2O mRNA promotes angiogenesis in cutaneous wounds by targeting SMAD6. J. Nanobiotechnol., 18.","DOI":"10.1186\/s12951-020-00624-3"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"414","DOI":"10.1016\/j.bbalip.2014.07.008","article-title":"Prostaglandin E2-induced inflammation: Relevance of prostaglandin E receptors","volume":"1851","author":"Kawahara","year":"2015","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"142","DOI":"10.1186\/s12935-020-01226-7","article-title":"Recent insights into eukaryotic translation initiation factors 5A1 and 5A2 and their roles in human health and disease","volume":"20","author":"Wu","year":"2020","journal-title":"Cancer Cell Int."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1038\/s41586-021-03214-x","article-title":"Function and regulation of the divisome for mitochondrial fission","volume":"590","author":"Kraus","year":"2021","journal-title":"Nature"},{"key":"ref_59","doi-asserted-by":"crossref","unstructured":"Tauc, M., Cougnon, M., Carcy, R., Melis, N., Hauet, T., Pellerin, L., Blondeau, N., and Pisani, D.F. (2021). The eukaryotic initiation factor 5A (eIF5A1), the molecule, mechanisms and recent insights into the pathophysiological roles. Cell Biosci., 11.","DOI":"10.1186\/s13578-021-00733-y"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"3286","DOI":"10.1158\/1078-0432.CCR-14-1953","article-title":"XPO1\/CRM1 Inhibition Causes Antitumor Effects by Mitochondrial Accumulation of eIF5A","volume":"21","author":"Miyake","year":"2015","journal-title":"Clin. Cancer Res."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"1788","DOI":"10.1111\/j.1349-7006.2012.02362.x","article-title":"Programmed cell death 6, a novel p53-responsive gene, targets to the nucleus in the apoptotic response to DNA damage","volume":"103","author":"Suzuki","year":"2012","journal-title":"Cancer Sci."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.jphotobiol.2013.03.007","article-title":"UVA causes dual inactivation of cathepsin B and L underlying lysosomal dysfunction in human dermal fibroblasts","volume":"123","author":"Lamore","year":"2013","journal-title":"J. Photochem. Photobiol. B"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1016\/j.redox.2015.07.008","article-title":"Antioxidant responses and cellular adjustments to oxidative stress","volume":"6","author":"Miguel","year":"2015","journal-title":"Redox Biol."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1038\/s41392-024-01749-9","article-title":"Protein translation: Biological processes and therapeutic strategies for human diseases","volume":"9","author":"Jia","year":"2024","journal-title":"Signal Transduct. Target. Ther."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"5102","DOI":"10.1111\/febs.17076","article-title":"Translation regulation in response to stress","volume":"291","author":"Williams","year":"2024","journal-title":"FEBS J."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"866","DOI":"10.1038\/ni.1633","article-title":"Superoxide dismutase 1 regulates caspase-1 and endotoxic shock","volume":"9","author":"Meissner","year":"2008","journal-title":"Nat. Immunol."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"857","DOI":"10.1038\/nrd4657","article-title":"Complement, a target for therapy in inflammatory and degenerative diseases","volume":"14","author":"Morgan","year":"2015","journal-title":"Nat. Rev. Drug Discov."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"4487","DOI":"10.1007\/s00018-021-03796-9","article-title":"The complement system in age-related macular degeneration","volume":"78","author":"Armento","year":"2021","journal-title":"Cell. Mol. Life Sci."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"715","DOI":"10.2353\/ajpath.2007.070166","article-title":"The Role of Complement in Inflammatory Diseases From Behind the Scenes into the Spotlight","volume":"171","author":"Markiewski","year":"2007","journal-title":"Am. J. Pathol."},{"key":"ref_70","first-page":"4391","article-title":"Role of matrix metalloproteinase in wound healing","volume":"14","author":"Kandhwal","year":"2022","journal-title":"Am. J. Transl. Res."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"534291","DOI":"10.1155\/2012\/534291","article-title":"Complement Activation and Inhibition in Wound Healing","volume":"2012","author":"Cazander","year":"2012","journal-title":"Clin. Dev. Immunol."},{"key":"ref_72","doi-asserted-by":"crossref","unstructured":"Park, D.J., Duggan, E., Ho, K., Dorschner, R.A., Dobke, M., Nolan, J.P., and Eliceiri, B.P. (2022). Serpin-loaded extracellular vesicles promote tissue repair in a mouse model of impaired wound healing. J. Nanobiotechnol., 20.","DOI":"10.1186\/s12951-022-01656-7"},{"key":"ref_73","doi-asserted-by":"crossref","unstructured":"Stein, E.V., Miller, T.W., Ivins-O\u2019Keefe, K., Kaur, S., and Roberts, D.D. (2016). Secreted Thrombospondin-1 Regulates Macrophage Interleukin-1\u03b2 Production and Activation through CD47. Sci. Rep., 6.","DOI":"10.1038\/srep19684"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1007\/s12079-009-0077-z","article-title":"The role of thrombospondins in wound healing, ischemia, and the foreign body reaction","volume":"3","author":"Kyriakides","year":"2009","journal-title":"J. Cell Commun. Signal."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"148129","DOI":"10.1016\/j.gene.2024.148129","article-title":"Fibulin 1, targeted by microRNA-24-3p, promotes cell proliferation and migration in vascular smooth muscle cells, contributing to the development of atherosclerosis in APOE-\/- mice","volume":"898","author":"Ji","year":"2024","journal-title":"Gene"},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"607","DOI":"10.1111\/j.1365-2133.2005.06716.x","article-title":"Fibulin-5 deposition in human skin: Decrease with ageing and ultraviolet B exposure and increase in solar elastosis","volume":"153","author":"Kadoya","year":"2005","journal-title":"Br. J. Dermatol."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"e55478","DOI":"10.15252\/embr.202255478","article-title":"The extracellular matrix fibulin 7 maintains epidermal stem cell heterogeneity during skin aging","volume":"23","author":"Raja","year":"2022","journal-title":"EMBO Rep."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"559","DOI":"10.1111\/jdi.14147","article-title":"Oxidative stress suppresses PHB2-mediated mitophagy in \u03b2-cells via the Nrf2\/PHB2 pathway","volume":"15","author":"Liu","year":"2024","journal-title":"J. Diabetes Investig."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"e180608","DOI":"10.1172\/jci.insight.180608","article-title":"Critical role of thrombospondin-1 in promoting intestinal mucosal wound repair","volume":"9","author":"Wilson","year":"2024","journal-title":"JCI Insight"},{"key":"ref_80","doi-asserted-by":"crossref","unstructured":"Zhang, B., Xie, S., Su, Z., Song, S., Xu, H., Chen, G., Cao, W., Yin, S., Gao, Q., and Wang, H. (2016). Heme oxygenase-1 induction attenuates imiquimod-induced psoriasiform inflammation by negative regulation of Stat3 signaling. Sci. Rep., 6.","DOI":"10.1038\/srep21132"},{"key":"ref_81","doi-asserted-by":"crossref","unstructured":"Belvedere, R., Novizio, N., Morello, S., and Petrella, A. (2022). The combination of mesoglycan and VEGF promotes skin wound repair by enhancing the activation of endothelial cells and fibroblasts and their cross-talk. Sci. Rep., 12.","DOI":"10.1038\/s41598-022-15227-1"},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1016\/j.jdermsci.2005.08.008","article-title":"The placenta growth factor in skin angiogenesis","volume":"41","author":"Odorisio","year":"2006","journal-title":"J. Dermatol. Sci."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1089\/wound.2011.0326","article-title":"Epidermal Growth Factor and Epidermal Growth Factor Receptor: The Yin and Yang in the Treatment of Cutaneous Wounds and Cancer","volume":"2","author":"Bodnar","year":"2013","journal-title":"Adv. Wound Care"},{"key":"ref_84","doi-asserted-by":"crossref","unstructured":"Gilbert, R.W.D., Vickaryous, M.K., and Viloria-Petit, A.M. (2016). Signalling by Transforming Growth Factor Beta Isoforms in Wound Healing and Tissue Regeneration. J. Dev. Biol., 4.","DOI":"10.3390\/jdb4020021"},{"key":"ref_85","doi-asserted-by":"crossref","unstructured":"Wang, Z., Zhang, H., and Cheng, Q. (2020). PDIA4: The basic characteristics, functions and its potential connection with cancer. Biomed. Pharmacother., 122.","DOI":"10.1016\/j.biopha.2019.109688"},{"key":"ref_86","doi-asserted-by":"crossref","unstructured":"Farooq, M., Khan, A.W., Kim, M.S., and Choi, S. (2021). The Role of Fibroblast Growth Factor (FGF) Signaling in Tissue Repair and Regeneration. Cells, 10.","DOI":"10.3390\/cells10113242"},{"key":"ref_87","doi-asserted-by":"crossref","unstructured":"Yasukawa, K., Okuno, T., and Yokomizo, T. (2020). Eicosanoids in Skin Wound Healing. Int. J. Mol. Sci., 21.","DOI":"10.3390\/ijms21228435"},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"tkad047","DOI":"10.1093\/burnst\/tkad047","article-title":"Metabolic reprogramming in skin wound healing","volume":"12","author":"Wang","year":"2024","journal-title":"Burns Trauma"},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"279","DOI":"10.1111\/imcb.12226","article-title":"Eicosanoids in tissue repair","volume":"97","year":"2019","journal-title":"Immunol. Cell Biol."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"12222","DOI":"10.3390\/ijms140612222","article-title":"UV Radiation and the Skin","volume":"14","author":"Jarrett","year":"2013","journal-title":"Int. J. Mol. Sci."},{"key":"ref_91","doi-asserted-by":"crossref","unstructured":"Lee, Y.B., Lee, J.H., Kim, Y.H., Seo, J.M., Yu, D.S., Park, Y.G., and Do Han, K. (2021). Positive association between actinic keratosis and internal malignancies: A nationwide population-based cohort study. Sci. Rep., 11.","DOI":"10.1038\/s41598-021-99225-9"},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"1527","DOI":"10.1016\/j.molcel.2023.03.030","article-title":"Chaperone-directed ribosome repair after oxidative damage","volume":"83","author":"Yang","year":"2023","journal-title":"Mol. Cell"},{"key":"ref_93","doi-asserted-by":"crossref","unstructured":"Gross, P. (2024). Ribotoxic stress drives cell death by UV. Nat. Cell Biol., 26.","DOI":"10.1038\/s41556-024-01506-8"},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"3652","DOI":"10.1016\/j.cell.2024.05.018","article-title":"The ribotoxic stress response drives UV-mediated cell death","volume":"187","author":"Sinha","year":"2024","journal-title":"Cell"},{"key":"ref_95","doi-asserted-by":"crossref","unstructured":"Kourtzelis, I., Hajishengallis, G., and Chavakis, T. (2020). Phagocytosis of Apoptotic Cells in Resolution of Inflammation. Front. Immunol., 11.","DOI":"10.3389\/fimmu.2020.00553"},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"932","DOI":"10.1111\/j.1538-7836.2006.01861.x","article-title":"Fibrin structure and wound healing","volume":"4","author":"Laurens","year":"2006","journal-title":"J. Thromb. Haemost."},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"1030","DOI":"10.7150\/ijms.43986","article-title":"Fibroblast Proliferation and Migration in Wound Healing by Phytochemicals: Evidence for a Novel Synergic Outcome","volume":"17","author":"Addis","year":"2020","journal-title":"Int. J. Med. Sci."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"883","DOI":"10.1016\/j.celrep.2014.06.044","article-title":"A myeloperoxidase-containing complex regulates neutrophil elastase release and actin dynamics during NETosis","volume":"8","author":"Metzler","year":"2014","journal-title":"Cell Rep."},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41467-019-13993-7","article-title":"U1 snRNP regulates cancer cell migration and invasion in vitro","volume":"11","author":"Oh","year":"2020","journal-title":"Nat. Commun."},{"key":"ref_100","doi-asserted-by":"crossref","unstructured":"Keitelman, I.A., Shiromizu, C.M., Zgajnar, N.R., Danieli\u00e1n, S., Jancic, C.C., Mart\u00ed, M.A., Fuentes, F., Yancoski, J., Aguilar, D.V., and Rosso, D.A. (2022). The interplay between serine proteases and caspase-1 regulates the autophagy-mediated secretion of Interleukin-1 beta in human neutrophils. Front. Immunol., 13.","DOI":"10.3389\/fimmu.2022.832306"},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1038\/s41374-020-00492-3","article-title":"\u03b2Cysteine 93 in human hemoglobin: A gateway to oxidative stability in health and disease","volume":"101","author":"Alayash","year":"2021","journal-title":"Lab. Investig."},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"1256","DOI":"10.1182\/blood.V128.22.1256.1256","article-title":"Heme Induces NLRP3 Inflammasome Formation in Primary Human Macrophages and May Propagate Hemolytic Inflammatory Processes By Inducing S100A8 Expression","volume":"128","author":"Silveira","year":"2016","journal-title":"Blood"},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"4310816","DOI":"10.1155\/2018\/4310816","article-title":"Induction of NLRP3 Inflammasome Activation by Heme in Human Endothelial Cells","volume":"2018","author":"Erdei","year":"2018","journal-title":"Oxid. Med. Cell. Longev."},{"key":"ref_104","doi-asserted-by":"crossref","first-page":"175","DOI":"10.3109\/13506129.2014.927759","article-title":"Interleukin-1 signaling pathway as a therapeutic target in transthyretin amyloidosis","volume":"21","author":"Vieira","year":"2014","journal-title":"Amyloid"},{"key":"ref_105","doi-asserted-by":"crossref","first-page":"17023","DOI":"10.1038\/sigtrans.2017.23","article-title":"NF-\u03baB signaling in inflammation","volume":"2","author":"Liu","year":"2017","journal-title":"Signal Transduct. Target. Ther."}],"container-title":["Antioxidants"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-3921\/14\/5\/545\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,9]],"date-time":"2025-10-09T17:25:25Z","timestamp":1760030725000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-3921\/14\/5\/545"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,4,30]]},"references-count":105,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2025,5]]}},"alternative-id":["antiox14050545"],"URL":"https:\/\/doi.org\/10.3390\/antiox14050545","relation":{},"ISSN":["2076-3921"],"issn-type":[{"type":"electronic","value":"2076-3921"}],"subject":[],"published":{"date-parts":[[2025,4,30]]}}}