The Effects of Lipid Extracts from Microalgae Chlorococcum amblystomatis and Nannochloropsis oceanica on the Proteome of 3D-Cultured Fibroblasts Exposed to UVA Radiation
Abstract
:1. Introduction
2. Materials and Methods
2.1. Microalgae
2.2. Lipid Extraction Process
2.3. Three-Dimensional (3D) Cell Culture and the Preparation of Experimental Fibroblasts Groups
2.4. The Process of Immunoprecipitation Against Human Caspase-1 (IP Against hCasp1)
2.5. Proteomic Analysis
2.6. Protein Level Analysis
2.6.1. Western Blotting
2.6.2. Elisa Method
2.7. Lipid Peroxidation Product (4-HNE) Level Determination by GC-MS
2.8. Wound Healing Assay (In Vitro Scratch Analysis)
2.9. Statistical Analysis
3. Results
4. Discussion
4.1. Potential Cytoprotective Action of C. amblystomatis Lipid Extract: Regulation of Redox Balance and Associated Inflammatory Signaling
4.2. Potential Effects of N. oceanica Lipid Extract Treatment on the Wound Healing Process, as Indicated by Changes in the Protein Profile of Fibroblasts
4.3. Limitation of the Study
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Wei, M.; He, X.; Liu, N.; Deng, H. Role of reactive oxygen species in ultraviolet-induced photodamage of the skin. Cell Div. 2024, 19, 1. [Google Scholar] [CrossRef]
- de Jager, T.L.; Cockrell, A.E.; Du Plessis, S.S. Ultraviolet Light Induced Generation of Reactive Oxygen Species. Adv. Exp. Med. Biol. 2017, 996, 15–23. [Google Scholar] [CrossRef] [PubMed]
- Hunt, M.; Torres, M.; Bachar-Wikstrom, E.; Wikstrom, J.D. Cellular and molecular roles of reactive oxygen species in wound healing. Commun. Biol. 2024, 7, 1534. [Google Scholar] [CrossRef]
- Wang, G.; Yang, F.; Zhou, W.; Xiao, N.; Luo, M.; Tang, Z. The initiation of oxidative stress and therapeutic strategies in wound healing. Biomed. Pharmacother. 2023, 157, 114004. [Google Scholar] [CrossRef] [PubMed]
- Jakovija, A.; Chtanova, T. Skin immunity in wound healing and cancer. Front. Immunol. 2023, 14, 1060258. [Google Scholar] [CrossRef]
- Conde, T.; Neves, B.; Couto, D.; Melo, T.; Lopes, D.; Pais, R.; Batista, J.; Cardoso, H.; Silva, J.L.; Domingues, P.; et al. Polar Lipids of Marine Microalgae Nannochloropsis oceanica and Chlorococcum amblystomatis Mitigate the LPS-Induced Pro-Inflammatory Response in Macrophages. Mar. Drugs 2023, 21, 629. [Google Scholar] [CrossRef]
- 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.; Steinhoff, M. Targeting deregulated oxidative stress in skin inflammatory diseases: An update on clinical importance. Biomed. Pharmacother. 2022, 154, 113601. [Google Scholar] [CrossRef]
- Emanuelli, M.; Sartini, D.; Molinelli, E.; Campagna, R.; Pozzi, V.; Salvolini, E.; Simonetti, O.; Campanati, A.; Offidani, A. The Double-Edged Sword of Oxidative Stress in Skin Damage and Melanoma: From Physiopathology to Therapeutical Approaches. Antioxidants 2022, 11, 612. [Google Scholar] [CrossRef] [PubMed]
- Łuczaj, W.; Gęgotek, A.; Conde, T.; Domingues, M.R.; Domingues, P.; Skrzydlewska, E. Lipidomic assessment of the impact of Nannochloropsis oceanica microalga lipid extract on human skin keratinocytes exposed to chronic UVB radiation. Sci. Rep. 2023, 13, 22302. [Google Scholar] [CrossRef]
- Couto, D.; Conde, T.A.; Melo, T.; Neves, B.; Costa, M.; Cunha, P.; Guerra, I.; Correia, N.; Silva, J.T.; Pereira, H.; et al. Effects of outdoor and indoor cultivation on the polar lipid composition and antioxidant activity of Nannochloropsis oceanica and Nannochloropsis limnetica: A lipidomics perspective. Algal Res. 2022, 64, 102718. [Google Scholar] [CrossRef]
- Correia, N.; Pereira, H.; Schulze, P.S.C.; Costa, M.M.; Santo, G.E.; Guerra, I.; Trovão, M.; Barros, A.; Cardoso, H.; Silva, J.L.; et al. Heterotrophic and Photoautotrophic Media Optimization Using Response Surface Methodology for the Novel Microalga Chlorococcum amblystomatis. Appl. Sci. 2023, 13, 2089. [Google Scholar] [CrossRef]
- Miguel, S.P.; Ribeiro, M.P.; Otero, A.; Coutinho, P. Application of microalgae and microalgal bioactive compounds in skin regeneration. Algal Res. 2021, 58, 102395. [Google Scholar] [CrossRef]
- Biernacki, M.; Conde, T.; Stasiewicz, A.; Surażyński, A.; Domingues, M.R.; Domingues, P.; Skrzydlewska, E. Restorative Effect of Microalgae Nannochloropsis oceanica Lipid Extract on Phospholipid Metabolism in Keratinocytes Exposed to UVB Radiation. Int. J. Mol. Sci. 2023, 24, 14323. [Google Scholar] [CrossRef]
- Stasiewicz, A.; Conde, T.; Gęgotek, A.; Domingues, M.R.; Domingues, P.; Skrzydlewska, E. Prevention of UVB Induced Metabolic Changes in Epidermal Cells by Lipid Extract from Microalgae Nannochloropsis oceanica. Int. J. Mol. Sci. 2023, 24, 11302. [Google Scholar] [CrossRef] [PubMed]
- Regueiras, A.; Huguet, Á.; Conde, T.; Couto, D.; Domingues, P.; Domingues, M.R.; Costa, A.M.; da Silva, J.L.; Vasconcelos, V.; Urbatzka, R. 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 2022, 20, 9. [Google Scholar] [CrossRef]
- Stasiewicz, A.; Conde, T.; Domingues, M.d.R.; Domingues, P.; Biernacki, M.; Skrzydlewska, E. Comparison of the Regenerative Metabolic Efficiency of Lipid Extracts from Microalgae Nannochloropsis oceanica and Chlorococcum amblystomatis on Fibroblasts. Antioxidants 2024, 13, 276. [Google Scholar] [CrossRef]
- Ekiner, S.A.; Gęgotek, A.; Domingues, P.; Domingues, M.R.; Skrzydlewska, E. Comparison of Microalgae Nannochloropsis oceanica and Chlorococcum amblystomatis Lipid Extracts Effects on UVA-Induced Changes in Human Skin Fibroblasts Proteome. Mar. Drugs 2024, 22, 509. [Google Scholar] [CrossRef]
- Urzì, O.; Gasparro, R.; Costanzo, E.; De Luca, A.; Giavaresi, G.; Fontana, S.; Alessandro, R. Three-Dimensional Cell Cultures: The Bridge between In Vitro and In Vivo Models. Int. J. Mol. Sci. 2023, 24, 12046. [Google Scholar] [CrossRef]
- Gȩgotek, A.; Domingues, P.; Skrzydlewska, E. Natural Exogenous Antioxidant Defense against Changes in Human Skin Fibroblast Proteome Disturbed by UVA Radiation. Oxid. Med. Cell. Longev. 2020, 2020, 3216415. [Google Scholar] [CrossRef]
- Zorina, A.; Zorin, V.; Isaev, A.; Kudlay, D.; Vasileva, M.; Kopnin, P. Dermal Fibroblasts as the Main Target for Skin Anti-Age Correction Using a Combination of Regenerative Medicine Methods. Curr. Issues Mol. Biol. 2023, 45, 3829–3847. [Google Scholar] [CrossRef]
- Ramos-González, E.J.; Bitzer-Quintero, O.K.; Ortiz, G.; Hernández-Cruz, J.J.; Ramírez-Jirano, L.J. Relationship between inflammation and oxidative stress and its effect on multiple sclerosis. Neurología 2024, 39, 292–301. [Google Scholar] [CrossRef]
- Zheng, D.; Liwinski, T.; Elinav, E. Inflammasome activation and regulation: Toward a better understanding of complex mechanisms. Cell Discov. 2020, 6, 36. [Google Scholar] [CrossRef] [PubMed]
- Barros, A.; Pereira, H.; Campos, J.; Marques, A.; Varela, J.; Silva, J. Heterotrophy as a tool to overcome the long and costly autotrophic scale-up process for large scale production of microalgae. Sci. Rep. 2019, 9, 13935. [Google Scholar] [CrossRef] [PubMed]
- Folch, J.; Lees, M.; Sloane Stanley, G.H. A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 1957, 226, 497–509. [Google Scholar] [CrossRef] [PubMed]
- Godugu, C.; Singh, M. AlgiMatrixTM-Based 3D Cell Culture System as an In Vitro Tumor Model: An Important Tool in Cancer Research. Methods Mol. Biol. 2016, 1379, 117–128. [Google Scholar] [CrossRef]
- Fotakis, G.; Timbrell, J.A. In vitro cytotoxicity assays: Comparison of LDH, neutral red, MTT and protein assay in hepatoma cell lines following exposure to cadmium chloride. Toxicol. Lett. 2006, 160, 171–177. [Google Scholar] [CrossRef]
- Bradford, M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72, 248–254. [Google Scholar] [CrossRef]
- Gęgotek, A.; Domingues, P.; Wroński, A.; Wójcik, P.; Skrzydlewska, E. Proteomic plasma profile of psoriatic patients. J. Pharm. Biomed. Anal. 2018, 155, 185–193. [Google Scholar] [CrossRef]
- Cox, J.; Mann, M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 2008, 26, 1367–1372. [Google Scholar] [CrossRef]
- Eissa, S.; Seada, L.S. Quantitation of bcl-2 protein in bladder cancer tissue by enzyme immunoassay: Comparison with Western blot and immunohistochemistry. Clin. Chem. 1998, 44, 1423–1429. [Google Scholar] [CrossRef]
- Tsikas, D.; Rothmann, S.; Schneider, J.Y.; Gutzki, F.M.; Beckmann, B.; Frölich, J.C. Simultaneous GC-MS/MS measurement of malondialdehyde and 4-hydroxy-2-nonenal in human plasma: Effects of long-term L-arginine administration. Anal. Biochem. 2017, 524, 31–44. [Google Scholar] [CrossRef] [PubMed]
- Žarković, N.; Jastrząb, A.; Jarocka-Karpowicz, I.; Orehovec, B.; Baršić, B.; Tarle, M.; Kmet, M.; Lukšić, I.; Łuczaj, W.; Skrzydlewska, E. The Impact of Severe COVID-19 on Plasma Antioxidants. Molecules 2022, 27, 5323. [Google Scholar] [CrossRef] [PubMed]
- Pang, Z.; Lu, Y.; Zhou, G.; Hui, F.; Xu, L.; Viau, C.; Spigelman, A.F.; Macdonald, P.E.; Wishart, D.S.; Li, S.; et al. MetaboAnalyst 6.0: Towards a unified platform for metabolomics data processing, analysis and interpretation. Nucleic Acids Res. 2024, 52, W398–W406. [Google Scholar] [CrossRef] [PubMed]
- Lim, C.J.M.; Janhunen, S.K.; Riedel, G. Reproducibility in Preclinical in Vivo Research: Statistical Inferences. J. Integr. Neurosci. 2024, 23, 30. [Google Scholar] [CrossRef]
- Poisson, L.M.; Ghosh, D. Statistical Issues and Analyses of in vivo and in vitro Genomic Data in order to Identify Clinically Relevant Profiles. Cancer Inform. 2007, 3, 231–243. [Google Scholar] [CrossRef]
- Carragher, N.; Piccinini, F.; Tesei, A.; Trask, O.J.; Bickle, M.; Horvath, P. Concerns, challenges and promises of high-content analysis of 3D cellular models. Nat. Rev. Drug Discov. 2018, 17, 606. [Google Scholar] [CrossRef]
- Szklarczyk, D.; Franceschini, A.; Wyder, S.; Forslund, K.; Heller, D.; Huerta-Cepas, J.; Simonovic, M.; Roth, A.; Santos, A.; Tsafou, K.P.; et al. STRING v10: Protein-protein interaction networks, integrated over the tree of life. Nucleic Acids Res. 2015, 43, D447–D452. [Google Scholar] [CrossRef]
- Thomas, P.D.; Ebert, D.; Muruganujan, A.; Mushayahama, T.; Albou, L.P.; Mi, H. PANTHER: Making genome-scale phylogenetics accessible to all. Protein Sci. 2022, 31, 8–22. [Google Scholar] [CrossRef]
- Mi, H.; Muruganujan, A.; Huang, X.; Ebert, D.; Mills, C.; Guo, X.; Thomas, P.D. Protocol Update for large-scale genome and gene function analysis with the PANTHER classification system (v.14.0). Nat. Protoc. 2019, 14, 703–721. [Google Scholar] [CrossRef]
- Wickham, H. ggplot2: Elegant Graphics for Data Analysis; Springer: New York, NY, USA, 2016; pp. VIII, 213. [Google Scholar] [CrossRef]
- Wickham, H.; François, R.; Henry, L.; Müller, K.; Vaughan, D. dplyr: A Grammar of Data Manipulation. 2023. Available online: https://dplyr.tidyverse.org (accessed on 15 January 2025).
- R Core Team. R: A Language and Environment for Statistical Computing. 2021. Available online: https://www.R-project.org/ (accessed on 15 January 2025).
- Biswas, S.K. Does the Interdependence between Oxidative Stress and Inflammation Explain the Antioxidant Paradox? Oxid. Med. Cell. Longev. 2016, 2016, 5698931. [Google Scholar] [CrossRef]
- Loboda, A.; Damulewicz, M.; Pyza, E.; Jozkowicz, A.; Dulak, J. Role of Nrf2/HO-1 system in development, oxidative stress response and diseases: An evolutionarily conserved mechanism. Cell. Mol. Life Sci. 2016, 73, 3221–3247. [Google Scholar] [CrossRef] [PubMed]
- Csala, M.; Kardon, T.; Legeza, B.; Lizák, B.; Mandl, J.; Margittai, É.; Puskás, F.; Száraz, P.; Szelényi, P.; Bánhegyi, G. On the role of 4-hydroxynonenal in health and disease. Biochim. Biophys. Acta (BBA)—Mol. Basis Dis. 2015, 1852, 826–838. [Google Scholar] [CrossRef] [PubMed]
- Conde, T.A.; Couto, D.; Melo, T.; Costa, M.; Silva, J.; Domingues, M.R.; Domingues, P. Polar lipidomic profile shows Chlorococcum amblystomatis as a promising source of value-added lipids. Sci. Rep. 2021, 11, 4355. [Google Scholar] [CrossRef] [PubMed]
- Gęgotek, A.; Conde, T.; Domingues, M.R.; Domingues, P.; Skrzydlewska, E. Impact of Nannochloropsis oceanica and Chlorococcum amblystomatis Extracts on UVA-Irradiated on 3D Cultured Melanoma Cells: A Proteomic Insight. Cells 2024, 13, 1934. [Google Scholar] [CrossRef]
- Ramzan, R.; Vogt, S.; Kadenbach, B. Stress-mediated generation of deleterious ROS in healthy individuals—Role of cytochrome c oxidase. J. Mol. Med. 2020, 98, 651–657. [Google Scholar] [CrossRef]
- Pannala, V.R.; Dash, R.K. Mechanistic characterization of the thioredoxin system in the removal of hydrogen peroxide. Free Radic. Biol. Med. 2015, 78, 42–55. [Google Scholar] [CrossRef]
- Fan, Y.; Zhang, J.; Cai, L.; Wang, S.; Liu, C.; Zhang, Y.; You, L.; Fu, Y.; Shi, Z.; Yin, Z.; et al. The effect of anti-inflammatory properties of ferritin light chain on lipopolysaccharide-induced inflammatory response in murine macrophages. Biochim. Biophys. Acta (BBA)—Mol. Cell Res. 2014, 1843, 2775–2783. [Google Scholar] [CrossRef]
- de Bari, L.; Scirè, A.; Minnelli, C.; Cianfruglia, L.; Kalapos, M.P.; Armeni, T. Interplay among Oxidative Stress, Methylglyoxal Pathway and S-Glutathionylation. Antioxidants 2020, 10, 19. [Google Scholar] [CrossRef]
- Trellu, S.; Courties, A.; Jaisson, S.; Gorisse, L.; Gillery, P.; Kerdine-Römer, S.; Vaamonde-Garcia, C.; Houard, X.; Ekhirch, F.P.; Sautet, A.; et al. Impairment of glyoxalase-1, an advanced glycation end-product detoxifying enzyme, induced by inflammation in age-related osteoarthritis. Arthritis Res. Ther. 2019, 21, 18. [Google Scholar] [CrossRef]
- Wang, X.; Zhu, Z. Role of Ubiquitin-conjugating enzyme E2 (UBE2) in two immune-mediated inflammatory skin diseases: A mendelian randomization analysis. Arch. Dermatol. Res. 2024, 316, 249. [Google Scholar] [CrossRef]
- Mishra, V.; Crespo-Puig, A.; McCarthy, C.; Masonou, T.; Glegola-Madejska, I.; Dejoux, A.; Dow, G.; Eldridge, M.J.G.; Marinelli, L.H.; Meng, M.; et al. IL-1β turnover by the UBE2L3 ubiquitin conjugating enzyme and HECT E3 ligases limits inflammation. Nat. Commun. 2023, 14, 4385. [Google Scholar] [CrossRef] [PubMed]
- Mi, B.; Chen, L.; Xiong, Y.; Yan, C.; Xue, H.; Panayi, A.C.; Liu, J.; Hu, L.; Hu, Y.; Cao, F.; et al. Saliva exosomes-derived UBE2O mRNA promotes angiogenesis in cutaneous wounds by targeting SMAD6. J. Nanobiotechnol. 2020, 18, 68. [Google Scholar] [CrossRef]
- Kawahara, K.; Hohjoh, H.; Inazumi, T.; Tsuchiya, S.; Sugimoto, Y. Prostaglandin E2-induced inflammation: Relevance of prostaglandin E receptors. Biochim. Biophys. Acta 2015, 1851, 414–421. [Google Scholar] [CrossRef] [PubMed]
- Wu, G.Q.; Xu, Y.M.; Lau, A.T.Y. Recent insights into eukaryotic translation initiation factors 5A1 and 5A2 and their roles in human health and disease. Cancer Cell Int. 2020, 20, 142. [Google Scholar] [CrossRef] [PubMed]
- Kraus, F.; Roy, K.; Pucadyil, T.J.; Ryan, M.T. Function and regulation of the divisome for mitochondrial fission. Nature 2021, 590, 57–66. [Google Scholar] [CrossRef]
- Tauc, M.; Cougnon, M.; Carcy, R.; Melis, N.; Hauet, T.; Pellerin, L.; Blondeau, N.; Pisani, D.F. The eukaryotic initiation factor 5A (eIF5A1), the molecule, mechanisms and recent insights into the pathophysiological roles. Cell Biosci. 2021, 11, 219. [Google Scholar] [CrossRef]
- Miyake, T.; Pradeep, S.; Wu, S.Y.; Rupaimoole, R.; Zand, B.; Wen, Y.; Gharpure, K.M.; Nagaraja, A.S.; Hu, W.; Cho, M.S.; et al. XPO1/CRM1 Inhibition Causes Antitumor Effects by Mitochondrial Accumulation of eIF5A. Clin. Cancer Res. 2015, 21, 3286–3297. [Google Scholar] [CrossRef]
- Suzuki, K.; Dashzeveg, N.; Lu, Z.G.; Taira, N.; Miki, Y.; Yoshida, K. Programmed cell death 6, a novel p53-responsive gene, targets to the nucleus in the apoptotic response to DNA damage. Cancer Sci. 2012, 103, 1788–1794. [Google Scholar] [CrossRef]
- Lamore, S.D.; Wondrak, G.T. UVA causes dual inactivation of cathepsin B and L underlying lysosomal dysfunction in human dermal fibroblasts. J. Photochem. Photobiol. B 2013, 123, 1–12. [Google Scholar] [CrossRef]
- Espinosa-Diez, C.; Miguel, V.; Mennerich, D.; Kietzmann, T.; Sánchez-Pérez, P.; Cadenas, S.; Lamas, S. Antioxidant responses and cellular adjustments to oxidative stress. Redox Biol. 2015, 6, 183–197. [Google Scholar] [CrossRef]
- Jia, X.; He, X.; Huang, C.; Li, J.; Dong, Z.; Liu, K. Protein translation: Biological processes and therapeutic strategies for human diseases. Signal Transduct. Target. Ther. 2024, 9, 44. [Google Scholar] [CrossRef] [PubMed]
- Williams, T.D.; Rousseau, A.; Williams, D.; Rousseau, A. Translation regulation in response to stress. FEBS J. 2024, 291, 5102. [Google Scholar] [CrossRef] [PubMed]
- Meissner, F.; Molawi, K.; Zychlinsky, A. Superoxide dismutase 1 regulates caspase-1 and endotoxic shock. Nat. Immunol. 2008, 9, 866–872. [Google Scholar] [CrossRef]
- Morgan, B.P.; Harris, C.L. Complement, a target for therapy in inflammatory and degenerative diseases. Nat. Rev. Drug Discov. 2015, 14, 857–877. [Google Scholar] [CrossRef]
- Armento, A.; Ueffing, M.; Clark, S.J. The complement system in age-related macular degeneration. Cell. Mol. Life Sci. 2021, 78, 4487–4505. [Google Scholar] [CrossRef]
- Markiewski, M.M.; Lambris, J.D. The Role of Complement in Inflammatory Diseases From Behind the Scenes into the Spotlight. Am. J. Pathol. 2007, 171, 715–727. [Google Scholar] [CrossRef]
- Kandhwal, M.; Behl, T.; Singh, S.; Sharma, N.; Arora, S.; Bhatia, S.; Al-Harrasi, A.; Sachdeva, M.; Bungau, S. Role of matrix metalloproteinase in wound healing. Am. J. Transl. Res. 2022, 14, 4391–4405. [Google Scholar] [CrossRef]
- Cazander, G.; Jukema, G.N.; Nibbering, P.H. Complement Activation and Inhibition in Wound Healing. Clin. Dev. Immunol. 2012, 2012, 534291. [Google Scholar] [CrossRef] [PubMed]
- Park, D.J.; Duggan, E.; Ho, K.; Dorschner, R.A.; Dobke, M.; Nolan, J.P.; Eliceiri, B.P. Serpin-loaded extracellular vesicles promote tissue repair in a mouse model of impaired wound healing. J. Nanobiotechnol. 2022, 20, 474. [Google Scholar] [CrossRef]
- Stein, E.V.; Miller, T.W.; Ivins-O’Keefe, K.; Kaur, S.; Roberts, D.D. Secreted Thrombospondin-1 Regulates Macrophage Interleukin-1β Production and Activation through CD47. Sci. Rep. 2016, 6, 19684. [Google Scholar] [CrossRef]
- Kyriakides, T.R.; MacLauchlan, S. The role of thrombospondins in wound healing, ischemia, and the foreign body reaction. J. Cell Commun. Signal. 2009, 3, 215–225. [Google Scholar] [CrossRef] [PubMed]
- Ji, T.; Yan, D.; Huang, Y.; Luo, M.; Zhang, Y.; Xu, T.; Gao, S.; Zhang, L.; Ruan, L.; Zhang, C. 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. Gene 2024, 898, 148129. [Google Scholar] [CrossRef] [PubMed]
- Kadoya, K.; Sasaki, T.; Kostka, G.; Timpl, R.; Matsuzaki, K.; Kumagai, N.; Sakai, L.Y.; Nishiyama, T.; Amano, S. Fibulin-5 deposition in human skin: Decrease with ageing and ultraviolet B exposure and increase in solar elastosis. Br. J. Dermatol. 2005, 153, 607–612. [Google Scholar] [CrossRef]
- Raja, E.; Changarathil, G.; Oinam, L.; Tsunezumi, J.; Ngo, Y.X.; Ishii, R.; Sasaki, T.; Imanaka-Yoshida, K.; Yanagisawa, H.; Sada, A. The extracellular matrix fibulin 7 maintains epidermal stem cell heterogeneity during skin aging. EMBO Rep. 2022, 23, e55478. [Google Scholar] [CrossRef]
- Liu, S.; Zhang, R.; Zhang, L.; Yang, A.; Guo, Y.; Jiang, L.; Wang, H.; Xu, S.; Zhou, H. Oxidative stress suppresses PHB2-mediated mitophagy in β-cells via the Nrf2/PHB2 pathway. J. Diabetes Investig. 2024, 15, 559–571. [Google Scholar] [CrossRef] [PubMed]
- Wilson, Z.S.; Raya-Sandino, A.; Miranda, J.; Fan, S.; Brazil, J.C.; Quiros, M.; Garcia-Hernandez, V.; Liu, Q.; Kim, C.H.; Hankenson, K.D.; et al. Critical role of thrombospondin-1 in promoting intestinal mucosal wound repair. JCI Insight 2024, 9, e180608. [Google Scholar] [CrossRef]
- Zhang, B.; Xie, S.; Su, Z.; Song, S.; Xu, H.; Chen, G.; Cao, W.; Yin, S.; Gao, Q.; Wang, H. Heme oxygenase-1 induction attenuates imiquimod-induced psoriasiform inflammation by negative regulation of Stat3 signaling. Sci. Rep. 2016, 6, 21132. [Google Scholar] [CrossRef]
- Belvedere, R.; Novizio, N.; Morello, S.; Petrella, A. 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. 2022, 12, 11041. [Google Scholar] [CrossRef]
- Odorisio, T.; Cianfarani, F.; Failla, C.M.; Zambruno, G. The placenta growth factor in skin angiogenesis. J. Dermatol. Sci. 2006, 41, 11–19. [Google Scholar] [CrossRef]
- Bodnar, R.J. Epidermal Growth Factor and Epidermal Growth Factor Receptor: The Yin and Yang in the Treatment of Cutaneous Wounds and Cancer. Adv. Wound Care 2013, 2, 24–29. [Google Scholar] [CrossRef]
- Gilbert, R.W.D.; Vickaryous, M.K.; Viloria-Petit, A.M. Signalling by Transforming Growth Factor Beta Isoforms in Wound Healing and Tissue Regeneration. J. Dev. Biol. 2016, 4, 21. [Google Scholar] [CrossRef] [PubMed]
- Wang, Z.; Zhang, H.; Cheng, Q. PDIA4: The basic characteristics, functions and its potential connection with cancer. Biomed. Pharmacother. 2020, 122, 109688. [Google Scholar] [CrossRef]
- Farooq, M.; Khan, A.W.; Kim, M.S.; Choi, S. The Role of Fibroblast Growth Factor (FGF) Signaling in Tissue Repair and Regeneration. Cells 2021, 10, 3242. [Google Scholar] [CrossRef]
- Yasukawa, K.; Okuno, T.; Yokomizo, T. Eicosanoids in Skin Wound Healing. Int. J. Mol. Sci. 2020, 21, 8435. [Google Scholar] [CrossRef]
- Wang, Z.; Zhao, F.; Xu, C.; Zhang, Q.; Ren, H.; Huang, X.; He, C.; Ma, J.; Wang, Z. Metabolic reprogramming in skin wound healing. Burns Trauma 2024, 12, tkad047. [Google Scholar] [CrossRef] [PubMed]
- Esser-von Bieren, J. Eicosanoids in tissue repair. Immunol. Cell Biol. 2019, 97, 279–288. [Google Scholar] [CrossRef]
- D’Orazio, J.; Jarrett, S.; Amaro-Ortiz, A.; Scott, T. UV Radiation and the Skin. Int. J. Mol. Sci. 2013, 14, 12222–12248. [Google Scholar] [CrossRef] [PubMed]
- Lee, Y.B.; Lee, J.H.; Kim, Y.H.; Seo, J.M.; Yu, D.S.; Park, Y.G.; Do Han, K. Positive association between actinic keratosis and internal malignancies: A nationwide population-based cohort study. Sci. Rep. 2021, 11, 19769. [Google Scholar] [CrossRef]
- Yang, Y.M.; Jung, Y.; Abegg, D.; Adibekian, A.; Carroll, K.S.; Karbstein, K. Chaperone-directed ribosome repair after oxidative damage. Mol. Cell 2023, 83, 1527–1537.e5. [Google Scholar] [CrossRef]
- Gross, P. Ribotoxic stress drives cell death by UV. Nat. Cell Biol. 2024, 26, 1374. [Google Scholar] [CrossRef]
- Sinha, N.K.; McKenney, C.; Yeow, Z.Y.; Li, J.J.; Nam, K.H.; Yaron-Barir, T.M.; Johnson, J.L.; Huntsman, E.M.; Cantley, L.C.; Ordureau, A.; et al. The ribotoxic stress response drives UV-mediated cell death. Cell 2024, 187, 3652–3670.e40. [Google Scholar] [CrossRef]
- Kourtzelis, I.; Hajishengallis, G.; Chavakis, T. Phagocytosis of Apoptotic Cells in Resolution of Inflammation. Front. Immunol. 2020, 11, 553. [Google Scholar] [CrossRef] [PubMed]
- Laurens, N.; Koolwijk, P.; de Maat, M.P. Fibrin structure and wound healing. J. Thromb. Haemost. 2006, 4, 932–939. [Google Scholar] [CrossRef]
- Addis, R.; Cruciani, S.; Santaniello, S.; Bellu, E.; Sarais, G.; Ventura, C.; Maioli, M.; Pintore, G. Fibroblast Proliferation and Migration in Wound Healing by Phytochemicals: Evidence for a Novel Synergic Outcome. Int. J. Med. Sci. 2020, 17, 1030–1042. [Google Scholar] [CrossRef] [PubMed]
- Metzler, K.D.; Goosmann, C.; Lubojemska, A.; Zychlinsky, A.; Papayannopoulos, V. A myeloperoxidase-containing complex regulates neutrophil elastase release and actin dynamics during NETosis. Cell Rep. 2014, 8, 883–896. [Google Scholar] [CrossRef] [PubMed]
- Oh, J.M.; Venters, C.C.; Di, C.; Pinto, A.M.; Wan, L.; Younis, I.; Cai, Z.; Arai, C.; So, B.R.; Duan, J.; et al. U1 snRNP regulates cancer cell migration and invasion in vitro. Nat. Commun. 2020, 11, 1. [Google Scholar] [CrossRef]
- Keitelman, I.A.; Shiromizu, C.M.; Zgajnar, N.R.; Danielián, S.; Jancic, C.C.; Martí, M.A.; Fuentes, F.; Yancoski, J.; Aguilar, D.V.; Rosso, D.A.; et al. The interplay between serine proteases and caspase-1 regulates the autophagy-mediated secretion of Interleukin-1 beta in human neutrophils. Front. Immunol. 2022, 13, 832306. [Google Scholar] [CrossRef]
- Alayash, A.I. βCysteine 93 in human hemoglobin: A gateway to oxidative stability in health and disease. Lab. Investig. 2021, 101, 4–11. [Google Scholar] [CrossRef]
- Silveira, A.A.; Cunningham, C.; Corr, E.; Ferreira, W.A.; Costa, F.F.; Almeida, C.B.; Conran, N.; Dunne, A. Heme Induces NLRP3 Inflammasome Formation in Primary Human Macrophages and May Propagate Hemolytic Inflammatory Processes By Inducing S100A8 Expression. Blood 2016, 128, 1256. [Google Scholar] [CrossRef]
- Erdei, J.; Tóth, A.; Balogh, E.; Nyakundi, B.B.; Bányai, E.; Ryffel, B.; Paragh, G.; Cordero, M.D.; Jeney, V. Induction of NLRP3 Inflammasome Activation by Heme in Human Endothelial Cells. Oxid. Med. Cell. Longev. 2018, 2018, 4310816. [Google Scholar] [CrossRef]
- Gonçalves, N.P.; Vieira, P.; Saraiva, M.J. Interleukin-1 signaling pathway as a therapeutic target in transthyretin amyloidosis. Amyloid 2014, 21, 175–184. [Google Scholar] [CrossRef] [PubMed]
- Liu, T.; Zhang, L.; Joo, D.; Sun, S.C. NF-κB signaling in inflammation. Signal Transduct. Target. Ther. 2017, 2, 17023. [Google Scholar] [CrossRef] [PubMed]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2025 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Atalay Ekiner, S.; Gęgotek, A.; Domingues, M.R.; Domingues, P.; Skrzydlewska, E. The Effects of Lipid Extracts from Microalgae Chlorococcum amblystomatis and Nannochloropsis oceanica on the Proteome of 3D-Cultured Fibroblasts Exposed to UVA Radiation. Antioxidants 2025, 14, 545. https://doi.org/10.3390/antiox14050545
Atalay Ekiner S, Gęgotek A, Domingues MR, Domingues P, Skrzydlewska E. The Effects of Lipid Extracts from Microalgae Chlorococcum amblystomatis and Nannochloropsis oceanica on the Proteome of 3D-Cultured Fibroblasts Exposed to UVA Radiation. Antioxidants. 2025; 14(5):545. https://doi.org/10.3390/antiox14050545
Chicago/Turabian StyleAtalay Ekiner, Sinemyiz, Agnieszka Gęgotek, Maria Rosário Domingues, Pedro Domingues, and Elżbieta Skrzydlewska. 2025. "The Effects of Lipid Extracts from Microalgae Chlorococcum amblystomatis and Nannochloropsis oceanica on the Proteome of 3D-Cultured Fibroblasts Exposed to UVA Radiation" Antioxidants 14, no. 5: 545. https://doi.org/10.3390/antiox14050545
APA StyleAtalay Ekiner, S., Gęgotek, A., Domingues, M. R., Domingues, P., & Skrzydlewska, E. (2025). The Effects of Lipid Extracts from Microalgae Chlorococcum amblystomatis and Nannochloropsis oceanica on the Proteome of 3D-Cultured Fibroblasts Exposed to UVA Radiation. Antioxidants, 14(5), 545. https://doi.org/10.3390/antiox14050545