Impact of Nannochloropsis oceanica and Chlorococcum amblystomatis Extracts on UVA-Irradiated on 3D Cultured Melanoma Cells: A Proteomic Insight
Abstract
:1. Introduction
2. Materials and Methods
2.1. Microalgal Material
2.2. Microalgae Lipid Extracts
2.3. Cell Culturing and Treatment
2.4. MTT Test
2.5. SDS-PAGE-Based Profiling
2.6. Protein Digestion and Peptide Analysis
2.7. Protein Identification and Label-Free Quantification
2.8. Statistical Analysis
3. Results
4. Discussion
4.1. The Effect of UVA on Melanoma Cell Proteome and Released Factors
4.2. The Effect of Microalgae Extracts on Melanoma Cells
4.3. The Effect of Microalgae Extracts on UVA-Irradiated Melanoma Cells
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- World Health Organization. Malignant Skin Melanoma. Available online: https://platform.who.int/mortality/themes/theme-details/topics/indicator-groups/indicators/indicator-details/MDB/a-malignant-skin-melanoma (accessed on 29 September 2023).
- Beroukhim, K.; Pourang, A.; Eisen, D.B. Risk of Second Primary Cutaneous and Noncutaneous Melanoma after Cutaneous Melanoma Diagnosis: A Population-Based Study. J. Am. Acad. Dermatol. 2020, 82, 683–689. [Google Scholar] [CrossRef]
- Schadendorf, D.; van Akkooi, A.C.J.; Berking, C.; Griewank, K.G.; Gutzmer, R.; Hauschild, A.; Stang, A.; Roesch, A.; Ugurel, S. Melanoma. Lancet 2018, 392, 971–984. [Google Scholar] [CrossRef]
- Schadendorf, D.; Fisher, D.E.; Garbe, C.; Gershenwald, J.E.; Grob, J.-J.; Halpern, A.; Herlyn, M.; Marchetti, M.A.; McArthur, G.; Ribas, A.; et al. Melanoma. Nat. Rev. Dis. Primers 2015, 1, 15003. [Google Scholar] [CrossRef]
- Denat, L.; Kadekaro, A.L.; Marrot, L.; Leachman, S.A.; Abdel-Malek, Z.A. Melanocytes as Instigators and Victims of Oxidative Stress. J. Investig. Dermatol. 2014, 134, 1512–1518. [Google Scholar] [CrossRef]
- Cannavò, S.P.; Tonacci, A.; Bertino, L.; Casciaro, M.; Borgia, F.; Gangemi, S. The Role of Oxidative Stress in the Biology of Melanoma: A Systematic Review. Pathol. Res. Pract. 2019, 215, 21–28. [Google Scholar] [CrossRef]
- Meierjohann, S. Oxidative Stress in Melanocyte Senescence and Melanoma Transformation. Eur. J. Cell Biol. 2014, 93, 36–41. [Google Scholar] [CrossRef]
- Uchida, K. Lipid Peroxidation and Redox-Sensitive Signaling Pathways. Curr. Atheroscler. Rep. 2007, 9, 216–221. [Google Scholar] [CrossRef]
- Nedelcu, R.I.; Turcu, G.; Ion, D.A.; Brinzea, A. Immune Mediated Mechanisms Against Cutaneous Melanocytes in Melanoma. In Interdisciplinary Cancer Research; Springer International Publishing: Cham, Switzerland, 2022; pp. 1–8. [Google Scholar]
- Centeno, P.P.; Pavet, V.; Marais, R. The Journey from Melanocytes to Melanoma. Nat. Rev. Cancer 2023, 23, 372–390. [Google Scholar] [CrossRef] [PubMed]
- Balsamo, M.; Scordamaglia, F.; Pietra, G.; Manzini, C.; Cantoni, C.; Boitano, M.; Queirolo, P.; Vermi, W.; Facchetti, F.; Moretta, A.; et al. Melanoma-Associated Fibroblasts Modulate NK Cell Phenotype and Antitumor Cytotoxicity. Proc. Natl. Acad. Sci. USA 2009, 106, 20847–20852. [Google Scholar] [CrossRef] [PubMed]
- Kodet, O.; Lacina, L.; Krejčí, E.; Dvořánková, B.; Grim, M.; Štork, J.; Kodetová, D.; Vlček, Č.; Šáchová, J.; Kolář, M.; et al. Melanoma Cells Influence the Differentiation Pattern of Human Epidermal Keratinocytes. Mol. Cancer 2015, 14, 1. [Google Scholar] [CrossRef] [PubMed]
- Dadachova, E.; Nosanchuk, J.D.; Shi, L.; Schweitzer, A.D.; Frenkel, A.; Nosanchuk, J.S.; Casadevall, A. Dead Cells in Melanoma Tumors Provide Abundant Antigen for Targeted Delivery of Ionizing Radiation by a mAb to Melanin. Proc. Natl. Acad. Sci. USA 2004, 101, 14865–14870. [Google Scholar] [CrossRef]
- Mellado, M.; de Ana, A.M.; Moreno, M.C.; Martínez-A, C.; Rodríguez-Frade, J.M. A Potential Immune Escape Mechanism by Melanoma Cells through the Activation of Chemokine-Induced T Cell Death. Curr. Biol. 2001, 11, 691–696. [Google Scholar] [CrossRef]
- He, S.; Huang, Q.; Cheng, J. The Unfolding Story of Dying Tumor Cells during Cancer Treatment. Front. Immunol. 2023, 14, 1073561. [Google Scholar] [CrossRef]
- Zhuang, D.; He, N.; Khoo, K.S.; Ng, E.-P.; Chew, K.W.; Ling, T.C. Application Progress of Bioactive Compounds in Microalgae on Pharmaceutical and Cosmetics. Chemosphere 2022, 291, 132932. [Google Scholar] [CrossRef] [PubMed]
- Wang, H.-M.D.; Li, X.-C.; Lee, D.-J.; Chang, J.-S. Potential Biomedical Applications of Marine Algae. Bioresour. Technol. 2017, 244, 1407–1415. [Google Scholar] [CrossRef] [PubMed]
- Conde, T.A.; Zabetakis, I.; Tsoupras, A.; Medina, I.; Costa, M.; Silva, J.; Neves, B.; Domingues, P.; Domingues, M.R. Microalgal Lipid Extracts Have Potential to Modulate the Inflammatory Response: A Critical Review. Int. J. Mol. Sci. 2021, 22, 9825. [Google Scholar] [CrossRef] [PubMed]
- Robertson, R.C.; Guihéneuf, F.; Bahar, B.; Schmid, M.; Stengel, D.B.; Fitzgerald, G.F.; Ross, R.P.; Stanton, C. The Anti-Inflammatory Effect of Algae-Derived Lipid Extracts on Lipopolysaccharide (LPS)-Stimulated Human THP-1 Macrophages. Mar. Drugs 2015, 13, 5402–5424. [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]
- Montuori, E.; Capalbo, A.; Lauritano, C. Marine Compounds for Melanoma Treatment and Prevention. Int. J. Mol. Sci. 2022, 23, 10284. [Google Scholar] [CrossRef] [PubMed]
- Baudelet, P.-H.; Gagez, A.-L.; Bérard, J.-B.; Juin, C.; Bridiau, N.; Kaas, R.; Thiéry, V.; Cadoret, J.-P.; Picot, L. Antiproliferative Activity of Cyanophora Paradoxa Pigments in Melanoma, Breast and Lung Cancer Cells. Mar. Drugs 2013, 11, 4390–4406. [Google Scholar] [CrossRef]
- Tavares-Carreón, F.; la Torre-Zavala, S.D.; Arocha-Garza, H.F.; Souza, V.; Galán-Wong, L.J.; Avilés-Arnaut, H. In Vitro Anticancer Activity of Methanolic Extract of Granulocystopsis Sp., a Microalgae from an Oligotrophic Oasis in the Chihuahuan Desert. PeerJ 2020, 8, e8686. [Google Scholar] [CrossRef]
- Gonçalves de Oliveira-Júnior, R.; Grougnet, R.; Bodet, P.-E.; Bonnet, A.; Nicolau, E.; Jebali, A.; Rumin, J.; Picot, L. Updated Pigment Composition of Tisochrysis Lutea and Purification of Fucoxanthin Using Centrifugal Partition Chromatography Coupled to Flash Chromatography for the Chemosensitization of Melanoma Cells. Algal Res. 2020, 51, 102035. [Google Scholar] [CrossRef]
- Zhong, D.; Du, Z.; Zhou, M. Algae: A Natural Active Material for Biomedical Applications. View 2021, 2, 20200189. [Google Scholar] [CrossRef]
- Mourelle, M.L.; Gómez, C.P.; Legido, J.L. The Potential Use of Marine Microalgae and Cyanobacteria in Cosmetics and Thalassotherapy. Cosmetics 2017, 4, 46. [Google Scholar] [CrossRef]
- Pereira, L. Seaweeds as Source of Bioactive Substances and Skin Care Therapy—Cosmeceuticals, Algotheraphy, and Thalassotherapy. Cosmetics 2018, 5, 68. [Google Scholar] [CrossRef]
- Choo, W.-T.; Teoh, M.-L.; Phang, S.-M.; Convey, P.; Yap, W.-H.; Goh, B.-H.; Beardall, J. Microalgae as Potential Anti-Inflammatory Natural Product Against Human Inflammatory Skin Diseases. Front. Pharmacol. 2020, 11, 1086. [Google Scholar] [CrossRef]
- Marconi, A.; Quadri, M.; Farnetani, F.; Ciardo, S.; Palazzo, E.; Lotti, R.; Cesinaro, A.M.; Fabbiani, L.; Vaschieri, C.; Puviani, M.; et al. In Vivo Melanoma Cell Morphology Reflects Molecular Signature and Tumor Aggressiveness. J. Investig. Dermatol. 2022, 142, 2205–2216.e6. [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]
- 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]
- 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] [PubMed]
- 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] [PubMed]
- 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]
- Medzihradszky, K.F. In-Solution Digestion of Proteins for Mass Spectrometry. In Methods in Enzymology; Mass Spectrometry: Modified Proteins and Glycoconjugates; Academic Press: Cambridge, MA, USA, 2005; Volume 405, pp. 50–65. [Google Scholar]
- Gęgotek, A.; Domingues, P.; Wroński, A.; Skrzydlewska, E. Changes in Proteome of Fibroblasts Isolated from Psoriatic Skin Lesions. Int. J. Mol. Sci. 2020, 21, 5363. [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]
- Tyanova, S.; Temu, T.; Cox, J. The MaxQuant Computational Platform for Mass Spectrometry-Based Shotgun Proteomics. Nat. Protoc. 2016, 11, 2301–2319. [Google Scholar] [CrossRef]
- Creasy, D.M.; Cottrell, J.S. Unimod: Protein Modifications for Mass Spectrometry. Proteomics 2004, 4, 1534–1536. [Google Scholar] [CrossRef] [PubMed]
- Domingues, M.R.; Fedorova, M.; Domingues, P. Mass Spectrometry Detection of Protein Modification by Cross-Reaction with Lipid Peroxidation Products. React. Oxyg. Species Lipid Peroxid. Protein Oxid. 2015, 3, 61–86. [Google Scholar]
- Karpievitch, Y.V.; Nikolic, S.B.; Wilson, R.; Sharman, J.E.; Edwards, L.M. Metabolomics Data Normalization with EigenMS. PLoS ONE 2014, 9, e116221. [Google Scholar] [CrossRef]
- Kronthaler, F.; Zöllner, S. Data Analysis with RStudio: An Easygoing Introduction; Springer: Berlin/Heidelberg, Germany, 2021. [Google Scholar]
- Gęgotek, A.; Bielawska, K.; Biernacki, M.; Dobrzyńska, I.; Skrzydlewska, E. Time-Dependent Effect of Rutin on Skin Fibroblasts Membrane Disruption Following UV Radiation. Redox Biol. 2017, 12, 733–744. [Google Scholar] [CrossRef]
- Chong, J.; Wishart, D.S.; Xia, J. Using MetaboAnalyst 4.0 for Comprehensive and Integrative Metabolomics Data Analysis. Curr. Protoc. Bioinform. 2019, 68, e86. [Google Scholar] [CrossRef] [PubMed]
- 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] [PubMed]
- Hanash, S.M.; Pitteri, S.J.; Faca, V.M. Mining the Plasma Proteome for Cancer Biomarkers. Nature 2008, 452, 571–579. [Google Scholar] [CrossRef] [PubMed]
- Ilkovitch, D.; Lopez, D.M. Immune Modulation by Melanoma-Derived Factors. Exp. Dermatol. 2008, 17, 977–985. [Google Scholar] [CrossRef]
- Wang, S.Q.; Setlow, R.; Berwick, M.; Polsky, D.; Marghoob, A.A.; Kopf, A.W.; Bart, R.S. Ultraviolet A and Melanoma: A Review. J. Am. Acad. Dermatol. 2001, 44, 837–846. [Google Scholar] [CrossRef]
- Khan, A.Q.; Travers, J.B.; Kemp, M.G. Roles of UVA Radiation and DNA Damage Responses in Melanoma Pathogenesis. Environ. Mol. Mutagen. 2018, 59, 438–460. [Google Scholar] [CrossRef]
- Mechanisms and Prevention of UV-Induced Melanoma-Sample-2018-Photodermatology, Photoimmunology & Photomedicine-Wiley Online Library. Available online: https://onlinelibrary.wiley.com/doi/full/10.1111/phpp.12329 (accessed on 24 October 2023).
- Gęgotek, A.; Domingues, P.; Skrzydlewska, E. Proteins Involved in the Antioxidant and Inflammatory Response in Rutin-Treated Human Skin Fibroblasts Exposed to UVA or UVB Irradiation. J. Dermatol. Sci. 2018, 90, 241–252. [Google Scholar] [CrossRef]
- Gęgotek, A.; Biernacki, M.; Ambrożewicz, E.; Surażyński, A.; Wroński, A.; Skrzydlewska, E. The Cross-Talk between Electrophiles, Antioxidant Defence and the Endocannabinoid System in Fibroblasts and Keratinocytes after UVA and UVB Irradiation. J. Dermatol. Sci. 2016, 81, 107–117. [Google Scholar] [CrossRef]
- IJMS|Free Full-Text|Changes in Phospholipid/Ceramide Profiles and Eicosanoid Levels in the Plasma of Rats Irradiated with UV Rays and Treated Topically with Cannabidiol. Available online: https://www.mdpi.com/1422-0067/22/16/8700 (accessed on 24 October 2023).
- Tse, B.C.Y.; Byrne, S.N. Lipids in Ultraviolet Radiation-Induced Immune Modulation. Photochem. Photobiol. Sci. 2020, 19, 870–878. [Google Scholar] [CrossRef]
- Busse, A.; Keilholz, U. Role of TGF-β in Melanoma. Curr. Pharm. Biotechnol. 2011, 12, 2165–2175. [Google Scholar] [CrossRef]
- Van Belle, P.; Rodeck, U.; Nuamah, I.; Halpern, A.C.; Elder, D.E. Melanoma-Associated Expression of Transforming Growth Factor-Beta Isoforms. Am. J. Pathol. 1996, 148, 1887–1894. [Google Scholar] [PubMed]
- Sabourin, C.L.K.; Kusewitt, D.F.; Applegate, L.A.; Budge, C.L.; Ley, R.D. Expression of Fibroblast Growth Factors in Ultraviolet Radiation—Induced Corneal Tumors and Corneal Tumor Cell Lines from Monodelphis Domestica. Mol. Carcinog. 1993, 7, 197–205. [Google Scholar] [CrossRef] [PubMed]
- Scott, G.; Jacobs, S.; Leopardi, S.; Anthony, F.A.; Learn, D.; Malaviya, R.; Pentland, A. Effects of PGF2α on Human Melanocytes and Regulation of the FP Receptor by Ultraviolet Radiation. Exp. Cell Res. 2005, 304, 407–416. [Google Scholar] [CrossRef]
- Ke, Y.; Wang, X.-J. TGFβ Signaling in Photoaging and UV-Induced Skin Cancer. J. Investig. Dermatol. 2021, 141, 1104–1110. [Google Scholar] [CrossRef] [PubMed]
- Li, Y.; Bi, Z.; Yan, B.; Wan, Y. UVB Radiation Induces Expression of HIF-1α and VEGF through the EGFR/PI3K/DEC1 Pathway. Int. J. Mol. Med. 2006, 18, 713–719. [Google Scholar] [CrossRef]
- Schwarz, T. UV Light Affects Cell Membrane and Cytoplasmic Targets. J. Photochem. Photobiol. B Biol. 1998, 44, 91–96. [Google Scholar] [CrossRef]
- Dwivedi, S.; Sharma, A.; Patrick, B.; Sharma, R.; Awasthi, Y.C. Role of 4-Hydroxynonenal and Its Metabolites in Signaling. Redox Rep. 2007, 12, 4–10. [Google Scholar] [CrossRef]
- Nikitakis, N.G.; Siavash, H.; Hebert, C.; Reynolds, M.A.; Hamburger, A.W.; Sauk, J.J. 15-PGJ2, but Not Thiazolidinediones, Inhibits Cell Growth, Induces Apoptosis, and Causes Downregulation of Stat3 in Human Oral SCCa Cells. Br. J. Cancer 2002, 87, 1396–1403. [Google Scholar] [CrossRef]
- Bie, Q.; Dong, H.; Jin, C.; Zhang, H.; Zhang, B. 15d-PGJ2 Is a New Hope for Controlling Tumor Growth. Am. J. Transl. Res. 2018, 10, 648–658. [Google Scholar]
- Łuczaj, W.; Gęgotek, A.; Skrzydlewska, E. Antioxidants and HNE in Redox Homeostasis. Free Radic. Biol. Med. 2017, 111, 87–101. [Google Scholar] [CrossRef]
- Simiczyjew, A.; Dratkiewicz, E.; Mazurkiewicz, J.; Ziętek, M.; Matkowski, R.; Nowak, D. The Influence of Tumor Microenvironment on Immune Escape of Melanoma. Int. J. Mol. Sci. 2020, 21, 8359. [Google Scholar] [CrossRef]
- 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]
- da Silva Vaz, B.; Moreira, J.B.; de Morais, M.G.; Costa, J.A.V. Microalgae as a New Source of Bioactive Compounds in Food Supplements. Curr. Opin. Food Sci. 2016, 7, 73–77. [Google Scholar] [CrossRef]
- Kim, H.-M.; Jung, J.H.; Kim, J.Y.; Heo, J.; Cho, D.-H.; Kim, H.-S.; An, S.; An, I.-S.; Bae, S. The Protective Effect of Violaxanthin from Nannochloropsis Oceanica against Ultraviolet B-Induced Damage in Normal Human Dermal Fibroblasts. Photochem. Photobiol. 2019, 95, 595–604. [Google Scholar] [CrossRef]
- Berg, J.; Seyedsadjadi, N.; Grant, R. Saturated Fatty Acid Intake Is Associated With Increased Inflammation, Conversion of Kynurenine to Tryptophan, and Delta-9 Desaturase Activity in Healthy Humans. Int. J. Tryptophan Res. 2020, 13, 1178646920981946. [Google Scholar] [CrossRef]
- Pellerin, L.; Carrié, L.; Dufau, C.; Nieto, L.; Ségui, B.; Levade, T.; Riond, J.; Andrieu-Abadie, N. Lipid Metabolic Reprogramming: Role in Melanoma Progression and Therapeutic Perspectives. Cancers 2020, 12, 3147. [Google Scholar] [CrossRef] [PubMed]
- Aloia, A.; Müllhaupt, D.; Chabbert, C.D.; Eberhart, T.; Flückiger-Mangual, S.; Vukolic, A.; Eichhoff, O.; Irmisch, A.; Alexander, L.T.; Scibona, E.; et al. A Fatty Acid Oxidation-Dependent Metabolic Shift Regulates the Adaptation of BRAF-Mutated Melanoma to MAPK Inhibitors. Clin. Cancer Res. 2019, 25, 6852–6867. [Google Scholar] [CrossRef]
- Mutch, D.M.; O’Maille, G.; Wikoff, W.R.; Wiedmer, T.; Sims, P.J.; Siuzdak, G. Mobilization of Pro-Inflammatory Lipids in Obese Plscr3-Deficient Mice. Genome Biol. 2007, 8, R38. [Google Scholar] [CrossRef] [PubMed]
- Harvey, K.A.; Walker, C.L.; Pavlina, T.M.; Xu, Z.; Zaloga, G.P.; Siddiqui, R.A. Long-Chain Saturated Fatty Acids Induce pro-Inflammatory Responses and Impact Endothelial Cell Growth. Clin. Nutr. 2010, 29, 492–500. [Google Scholar] [CrossRef] [PubMed]
- Qu, X.; Tang, Y.; Hua, S. Immunological Approaches Towards Cancer and Inflammation: A Cross Talk. Front. Immunol. 2018, 9, 563. [Google Scholar] [CrossRef]
- Gęgotek, A.; Skrzydlewska, E. Biological Effect of Protein Modifications by Lipid Peroxidation Products. Chem. Phys. Lipids 2019, 221, 46–52. [Google Scholar] [CrossRef] [PubMed]
- Maier, N.K.; Leppla, S.H.; Moayeri, M. The Cyclopentenone Prostaglandin 15d-PGJ2 Inhibits the NLRP1 and NLRP3 Inflammasomes. J. Immunol. 2015, 194, 2776–2785. [Google Scholar] [CrossRef] [PubMed]
- Yamamoto, Y.; Takase, K.; Kishino, J.; Fujita, M.; Okamura, N.; Sakaeda, T.; Fujimoto, M.; Yagami, T. Proteomic Identification of Protein Targets for 15-Deoxy-Δ12,14-Prostaglandin J2 in Neuronal Plasma Membrane. PLoS ONE 2011, 6, e17552. [Google Scholar] [CrossRef]
- Oh, J.Y.; Giles, N.; Landar, A.; Darley-Usmar, V. Accumulation of 15-Deoxy-Δ12,14-Prostaglandin J2 Adduct Formation with Keap1 over Time: Effects on Potency for Intracellular Antioxidant Defence Induction. Biochem. J. 2008, 411, 297–306. [Google Scholar] [CrossRef]
- Nilsson, L.; Palm, F.; Nørregaard, R. 15-Deoxy-Δ12,14-Prostaglandin J2 Exerts Antioxidant Effects While Exacerbating Inflammation in Mice Subjected to Ureteral Obstruction. Mediat. Inflamm. 2017, 2017, e3924912. [Google Scholar] [CrossRef]
- D’Arcy, M.S. Cell Death: A Review of the Major Forms of Apoptosis, Necrosis and Autophagy. Cell Biol. Int. 2019, 43, 582–592. [Google Scholar] [CrossRef]
- Adyns, L.; Proost, P.; Struyf, S. Role of Defensins in Tumor Biology. Int. J. Mol. Sci. 2023, 24, 5268. [Google Scholar] [CrossRef] [PubMed]
- Takeshita, F.; Ishii, K.J.; Kobiyama, K.; Kojima, Y.; Coban, C.; Sasaki, S.; Ishii, N.; Klinman, D.M.; Okuda, K.; Akira, S.; et al. TRAF4 Acts as a Silencer in TLR-Mediated Signaling through the Association with TRAF6 and TRIF. Eur. J. Immunol. 2005, 35, 2477–2485. [Google Scholar] [CrossRef]
- Chung, E.Y.; Kim, S.J.; Ma, X.J. Regulation of Cytokine Production during Phagocytosis of Apoptotic Cells. Cell Res. 2006, 16, 154–161. [Google Scholar] [CrossRef]
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. |
© 2024 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
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. https://doi.org/10.3390/cells13231934
Gęgotek A, Conde T, Domingues MR, 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(23):1934. https://doi.org/10.3390/cells13231934
Chicago/Turabian StyleGęgotek, Agnieszka, Tiago Conde, Maria Rosário Domingues, Pedro Domingues, and Elżbieta Skrzydlewska. 2024. "Impact of Nannochloropsis oceanica and Chlorococcum amblystomatis Extracts on UVA-Irradiated on 3D Cultured Melanoma Cells: A Proteomic Insight" Cells 13, no. 23: 1934. https://doi.org/10.3390/cells13231934
APA StyleGęgotek, A., Conde, T., Domingues, M. R., Domingues, P., & Skrzydlewska, E. (2024). Impact of Nannochloropsis oceanica and Chlorococcum amblystomatis Extracts on UVA-Irradiated on 3D Cultured Melanoma Cells: A Proteomic Insight. Cells, 13(23), 1934. https://doi.org/10.3390/cells13231934