Characterization of the Peroxisomal Proteome and Redox Balance in Human Prostate Cancer Cell Lines
Abstract
:1. Introduction
2. Materials and Methods
2.1. Cell Lines, Tissue Culture, and Treatment
2.2. Proteomics Analysis
2.3. Plasmids and Electroporation
2.4. SDS-PAGE and Immunoblotting
2.5. Antibodies
2.6. Catalase Activity
2.7. Subcellular Fractionation
2.8. Fluorescence Microscopy and Immunofluorescence
2.9. Proliferation and Sulforhodamine B Assays
2.10. Knockdown of Catalase Expression
2.11. Statistical Analysis
3. Results
3.1. Comparative Analysis of the Peroxisomal, Mitochondrial, and Cytosolic Redox Profiles in Prostate Cell Lines
3.2. Unbiased Proteomics Reveals Differential Peroxisomal and Redox Proteomes in Benign and Malignant Prostate Cell Lines
3.3. Expression, Activity, and Localization of Catalase in Prostate Cancer Cell Lines
3.4. Chemical Inhibition of Catalase Activity Reduces LNCaP Cell Proliferation
3.5. Knockdown of Catalase Expression Stimulates the Proliferation of LNCaP and 22Rv1 Cells
3.6. Androgen Receptor Activation by R1881 Alters Peroxisomal Redox State
3.7. R1881 Modulates the Peroxisomal and Antioxidant Enzyme Proteome
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Global Cancer Observatory: Cancer Today (Version 1.1); International Agency for Research on Cancer: Lyon, France. Available online: https://gco.iarc.who.int/today (accessed on 9 September 2024).
- Claessens, F.; Helsen, C.; Prekovic, S.; Van den Broeck, T.; Spans, L.; Van Poppel, H.; Joniau, S. Emerging mechanisms of enzalutamide resistance in prostate cancer. Nat. Rev. Urol. 2014, 11, 712–776. [Google Scholar] [CrossRef] [PubMed]
- Formaggio, N.; Rubin, M.A.; Theurillat, J.P. Loss and revival of androgen receptor signaling in advanced prostate cancer. Oncogene 2021, 40, 1205–1216. [Google Scholar] [CrossRef] [PubMed]
- Wu, K.; El Zowalaty, A.E.; Sayin, V.I.; Papagiannakopoulos, T. The pleiotropic functions of reactive oxygen species in cancer. Nat. Cancer 2024, 5, 384–399. [Google Scholar] [CrossRef] [PubMed]
- Battisti, V.; Maders, L.D.; Bagatini, M.D.; Reetz, L.G.; Chiesa, J.; Battisti, I.E.; Gonçalves, J.F.; Duarte, M.M.; Schetinger, M.R.; Morsch, V.M. Oxidative stress and antioxidant status in prostate cancer patients: Relation to Gleason score, treatment and bone metastasis. Biomed. Pharmacother. 2011, 65, 516–524. [Google Scholar] [CrossRef] [PubMed]
- Kalinina, E.V.; Gavriliuk, L.A.; Pokrovsky, V.S. Oxidative stress and redox-dependent signaling in prostate cancer. Biochemistry 2022, 87, 413–424. [Google Scholar] [CrossRef] [PubMed]
- Frohlich, D.A.; McCabe, M.T.; Arnold, R.S.; Day, M.L. The role of Nrf2 in increased reactive oxygen species and DNA damage in prostate tumorigenesis. Oncogene 2008, 27, 4353–4362. [Google Scholar] [CrossRef] [PubMed]
- Lee, W.H.; Morton, R.A.; Epstein, J.I.; Brooks, J.D.; Campbell, P.A.; Bova, G.S.; Hsieh, W.S.; Isaacs, W.B.; Nelson, W.G. Cytidine methylation of regulatory sequences near the pi-class glutathione S-transferase gene accompanies human prostatic carcinogenesis. Proc. Natl. Acad. Sci. USA 1994, 91, 11733–11737. [Google Scholar] [CrossRef]
- Lim, S.D.; Sun, C.; Lambeth, J.D.; Marshall, F.; Amin, M.; Chung, L.; Petros, J.A.; Arnold, R.S. Increased Nox1 and hydrogen peroxide in prostate cancer. Prostate 2005, 62, 200–207. [Google Scholar] [CrossRef]
- Miar, A.; Hevia, D.; Muñoz-Cimadevilla, H.; Astudillo, A.; Velasco, J.; Sainz, R.M.; Mayo, J.C. Manganese superoxide dismutase (SOD2/MnSOD)/catalase and SOD2/GPx1 ratios as biomarkers for tumor progression and metastasis in prostate, colon, and lung cancer. Free Radic. Biol. Med. 2015, 85, 45–55. [Google Scholar] [CrossRef]
- Wanders, R.J.A.; Baes, M.; Ribeiro, D.; Ferdinandusse, S.; Waterham, H.R. The physiological functions of human peroxisomes. Physiol. Rev. 2023, 103, 957–1024. [Google Scholar] [CrossRef]
- Fransen, M.; Lismont, C. Peroxisomal hydrogen peroxide signaling: A new chapter in intracellular communication research. Curr. Opin. Chem. Biol. 2024, 78, 102426. [Google Scholar] [CrossRef] [PubMed]
- Lismont, C.; Revenco, I.; Fransen, M. Peroxisomal hydrogen peroxide metabolism and signaling in health and disease. Int. J. Mol. Sci. 2019, 20, 3673. [Google Scholar] [CrossRef] [PubMed]
- Yifrach, E.; Fischer, S.; Oeljeklaus, S.; Schuldiner, M.; Zalckvar, E.; Warscheid, B. Defining the mammalian peroxisomal proteome. Subcell. Biochem. 2018, 89, 47–66. [Google Scholar] [CrossRef] [PubMed]
- Rixen, S.; Indorf, P.M.; Kubitza, C.; Struwe, M.A.; Klopp, C.; Scheidig, A.J.; Kunze, T.; Clement, B. Reduction of hydrogen peroxide by human mitochondrial amidoxime reducing component enzymes. Molecules 2023, 28, 6384. [Google Scholar] [CrossRef] [PubMed]
- Boveris, A.; Oshino, N.; Chance, B. The cellular production of hydrogen peroxide. Biochem. J. 1972, 128, 617–630. [Google Scholar] [CrossRef] [PubMed]
- Karpenko, I.L.; Valuev-Elliston, V.T.; Ivanova, O.N.; Smirnova, O.A.; Ivanov, A.V. Peroxiredoxins—The underrated actors during virus-induced oxidative stress. Antioxidants 2021, 10, 977. [Google Scholar] [CrossRef]
- Walton, P.A.; Brees, C.; Lismont, C.; Apanasets, O.; Fransen, M. The peroxisomal import receptor PEX5 functions as a stress sensor, retaining catalase in the cytosol in times of oxidative stress. Biochim. Biophys. Acta Mol. Cell Res. 2017, 1864, 1833–1843. [Google Scholar] [CrossRef]
- Sies, H.; Jones, D.P. Reactive oxygen species (ROS) as pleiotropic physiological signalling agents. Nat. Rev. Mol. Cell Biol. 2020, 21, 363–383. [Google Scholar] [CrossRef]
- Baker, A.M.; Oberley, L.W.; Cohen, M.B. Expression of antioxidant enzymes in human prostatic adenocarcinoma. Prostate 1997, 32, 229–233. [Google Scholar] [CrossRef]
- Bostwick, D.G.; Alexander, E.E.; Singh, R.; Shan, A.; Qian, J.; Santella, R.M.; Oberley, L.W.; Yan, T.; Zhong, W.; Jiang, X.; et al. Antioxidant enzyme expression and reactive oxygen species damage in prostatic intraepithelial neoplasia and cancer. Cancer 2000, 89, 123–134. [Google Scholar] [CrossRef]
- Oberley, T.D.; Zhong, W.; Szweda, L.I.; Oberley, L.W. Localization of antioxidant enzymes and oxidative damage products in normal and malignant prostate epithelium. Prostate 2000, 44, 144–155. [Google Scholar] [CrossRef] [PubMed]
- Ahn, J.; Nowell, S.; McCann, S.E.; Yu, J.; Carter, L.; Lang, N.P.; Kadlubar, F.F.; Ratnasinghe, L.D.; Ambrosone, C.B. Associations between catalase phenotype and genotype: Modification by epidemiologic factors. Cancer Epidemiol. Biomarkers Prev. 2006, 15, 1217–1222. [Google Scholar] [CrossRef] [PubMed]
- Shen, Y.; Li, D.; Tian, P.; Shen, K.; Zhu, J.; Feng, M.; Wan, C.; Yang, T.; Chen, L.; Wen, F. The catalase C-262T gene polymorphism and cancer risk: A systematic review and meta-analysis. Medicine 2015, 94, e679. [Google Scholar] [CrossRef]
- Wang, C.D.; Sun, Y.; Chen, N.; Huang, L.; Huang, J.W.; Zhu, M.; Wang, T.; Ji, Y.L. The role of catalase C262T gene polymorphism in the susceptibility and survival of cancers. Sci. Rep. 2016, 6, 26973. [Google Scholar] [CrossRef] [PubMed]
- Valença, I.; Pértega-Gomes, N.; Vizcaino, J.R.; Henrique, R.M.; Lopes, C.; Baltazar, F.; Ribeiro, D. Localization of MCT2 at peroxisomes is associated with malignant transformation in prostate cancer. J. Cell. Mol. Med. 2015, 19, 723–733. [Google Scholar] [CrossRef]
- Valença, I.; Ferreira, A.R.; Correia, M.; Kühl, S.; van Roermund, C.; Waterham, H.R.; Máximo, V.; Islinger, M.; Ribeiro, D. Prostate cancer proliferation is affected by the subcellular localization of MCT2 and accompanied by significant peroxisomal alterations. Cancers 2020, 12, 3152. [Google Scholar] [CrossRef] [PubMed]
- Mah, C.Y.; Nguyen, A.D.T.; Niijima, T.; Helm, M.; Dehairs, J.; Ryan, F.J.; Ryan, N.; Quek, L.E.; Hoy, A.J.; Don, A.S.; et al. Peroxisomal β-oxidation enzyme, DECR2, regulates lipid metabolism and promotes treatment resistance in advanced prostate cancer. Br. J. Cancer 2024, 130, 741–754. [Google Scholar] [CrossRef] [PubMed]
- Zha, S.; Ferdinandusse, S.; Hicks, J.L.; Denis, S.; Dunn, T.A.; Wanders, R.J.; Luo, J.; De Marzo, A.M.; Isaacs, W.B. Peroxisomal branched chain fatty acid beta-oxidation pathway is upregulated in prostate cancer. Prostate 2005, 63, 316–323. [Google Scholar] [CrossRef]
- Kushwaha, P.P.; Verma, S.S.; Shankar, E.; Lin, S.; Gupta, S. Role of solute carrier transporters SLC25A17 and SLC27A6 in acquired resistance to enzalutamide in castration-resistant prostate cancer. Mol. Carcinog. 2022, 61, 397–407. [Google Scholar] [CrossRef]
- Demichev, V.; Messner, C.B.; Vernardis, S.I.; Lilley, K.S.; Ralser, M. DIA-NN: Neural networks and interference correction enable deep proteome coverage in high throughput. Nat. Methods 2020, 17, 41–44. [Google Scholar] [CrossRef]
- Ivashchenko, O.; Van Veldhoven, P.P.; Brees, C.; Ho, Y.S.; Terlecky, S.R.; Fransen, M. Intraperoxisomal redox balance in mammalian cells: Oxidative stress and interorganellar cross-talk. Mol. Biol. Cell 2011, 22, 1440–1451. [Google Scholar] [CrossRef] [PubMed]
- Lismont, C.; Nordgren, M.; Brees, C.; Knoops, B.; Van Veldhoven, P.P.; Fransen, M. Peroxisomes as modulators of cellular protein thiol oxidation: A new model system. Antioxid. Redox Signal. 2019, 30, 22–39. [Google Scholar] [CrossRef] [PubMed]
- Brees, C.; Fransen, M. A cost-effective approach to microporate mammalian cells with the Neon Transfection System. Anal. Biochem. 2014, 466, 49–50. [Google Scholar] [CrossRef] [PubMed]
- Fransen, M.; Wylin, T.; Brees, C.; Mannaerts, G.P.; Van Veldhoven, P.P. Human Pex19p binds peroxisomal integral membrane proteins at regions distinct from their sorting sequences. Mol. Cell. Biol. 2001, 21, 4413–4424. [Google Scholar] [CrossRef]
- Amery, L.; Fransen, M.; De Nys, K.; Mannaerts, G.P.; Van Veldhoven, P.P. Mitochondrial and peroxisomal targeting of 2-methylacyl-CoA racemase in humans. J. Lipid Res. 2000, 41, 1752–1759. [Google Scholar] [CrossRef]
- Van Veldhoven, P.P.; de Schryver, E.; Young, S.G.; Zwijsen, A.; Fransen, M.; Espeel, M.; Baes, M.; Van Ael, E. Slc25a17 gene trapped mice: PMP34 plays a role in the peroxisomal degradation of phytanic and pristanic acid. Front. Cell Dev. Biol. 2020, 8, 144. [Google Scholar] [CrossRef]
- Goemaere, J.; Knoops, B. Peroxiredoxin distribution in the mouse brain with emphasis on neuronal populations affected in neurodegenerative disorders. J. Comp. Neurol. 2012, 520, 258–280. [Google Scholar] [CrossRef] [PubMed]
- Baudhuin, P.; Beaufay, H.; Rahman-Li, Y.; Sellinger, O.Z.; Wattiaux, R.; Jacques, P.; De Duve, C. Tissue fractionation studies. 17. Intracellular distribution of monoamine oxidase, aspartate aminotransferase, alanine aminotransferase, D-amino acid oxidase and catalase in rat-liver tissue. Biochem. J. 1964, 92, 179–184. [Google Scholar] [CrossRef]
- Huybrechts, S.J.; Van Veldhoven, P.P.; Brees, C.; Mannaerts, G.P.; Los, G.V.; Fransen, M. Peroxisome dynamics in cultured mammalian cells. Traffic 2009, 10, 1722–1733. [Google Scholar] [CrossRef]
- Ramazani, Y.; Knops, N.; Berlingerio, S.P.; Adebayo, O.C.; Lismont, C.; Kuypers, D.J.; Levtchenko, E.; van den Heuvel, L.P.; Fransen, M. Therapeutic concentrations of calcineurin inhibitors do not deregulate glutathione redox balance in human renal proximal tubule cells. PLoS ONE 2021, 16, e0250996. [Google Scholar] [CrossRef]
- Begara-Morales, J.C.; Sánchez-Calvo, B.; Chaki, M.; Valderrama, R.; Mata-Pérez, C.; Padilla, M.N.; Corpas, F.J.; Barroso, J.B. Antioxidant systems are regulated by nitric oxide-mediated post-translational modifications (NO-PTMs). Front. Plant Sci. 2016, 7, 152. [Google Scholar] [CrossRef] [PubMed]
- Rhee, S.G.; Woo, H.A.; Kang, D. The role of peroxiredoxins in the transduction of H2O2 signals. Antioxid. Redox Signal. 2018, 28, 537–557. [Google Scholar] [CrossRef] [PubMed]
- Joly-Pharaboz, M.O.; Soave, M.C.; Nicolas, B.; Mebarki, F.; Renaud, M.; Foury, O.; Morel, Y.; Andre, J.G. Androgens inhibit the proliferation of a variant of the human prostate cancer cell line LNCaP. J. Steroid Biochem. Mol. Biol. 1995, 55, 67–76. [Google Scholar] [CrossRef] [PubMed]
- Esquenet, M.; Swinnen, J.V.; Heyns, W.; Verhoeven, G. LNCaP prostatic adenocarcinoma cells derived from low and high passage numbers display divergent responses not only to androgens but also to retinoids. J. Steroid Biochem. Mol. Biol. 1997, 62, 391–399. [Google Scholar] [CrossRef]
- Ripple, M.O.; Henry, W.F.; Rago, R.P.; Wilding, G. Prooxidant-antioxidant shift induced by androgen treatment of human prostate carcinoma cells. J. Natl. Cancer Inst. 1997, 89, 40–48. [Google Scholar] [CrossRef] [PubMed]
- Handle, F.; Prekovic, S.; Helsen, C.; Van den Broeck, T.; Smeets, E.; Moris, L.; Eerlings, R.; Kharraz, S.E.; Urbanucci, A.; Mills, I.G.; et al. Drivers of AR indifferent anti-androgen resistance in prostate cancer cells. Sci. Rep. 2019, 9, 13786. [Google Scholar] [CrossRef]
- Sedelaar, J.P.; Isaacs, J.T. Tissue culture media supplemented with 10% fetal calf serum contains a castrate level of testosterone. Prostate 2009, 69, 1724–1749. [Google Scholar] [CrossRef] [PubMed]
- Chaiswing, L.; Zhong, W.; Oberley, T.D. Distinct redox profiles of selected human prostate carcinoma cell lines: Implications for rational design of redox therapy. Cancers 2011, 3, 3557–3584. [Google Scholar] [CrossRef]
- Jung, K.; Seidel, B.; Rudolph, B.; Lein, M.; Cronauer, M.V.; Henke, W.; Hampel, G.; Schnorr, D.; Loening, S.A. Antioxidant enzymes in malignant prostate cell lines and in primary cultured prostatic cells. Free Radic. Biol. Med. 1997, 23, 127–133. [Google Scholar] [CrossRef]
- Glorieux, C.; Zamocky, M.; Sandoval, J.M.; Verrax, J.; Calderon, P.B. Regulation of catalase expression in healthy and cancerous cells. Free Radic. Biol. Med. 2015, 87, 84–97. [Google Scholar] [CrossRef]
- Tao, Y.; Liu, S.; Lu, J.; Fu, S.; Li, L.; Zhang, J.; Wang, Z.; Hong, M. FOXO3a-ROS pathway is involved in androgen-induced proliferation of prostate cancer cell. BMC Urol. 2022, 22, 70. [Google Scholar] [CrossRef] [PubMed]
- Cancer Genome Atlas Research Network. The molecular taxonomy of primary prostate cancer. Cell 2015, 163, 1011–1025. [Google Scholar] [CrossRef] [PubMed]
- Krönig, M.; Walter, M.; Drendel, V.; Werner, M.; Jilg, C.A.; Richter, A.S.; Backofen, R.; McGarry, D.; Follo, M.; Schultze-Seemann, W.; et al. Cell type specific gene expression analysis of prostate needle biopsies resolves tumor tissue heterogeneity. Oncotarget 2015, 6, 1302–1314. [Google Scholar] [CrossRef] [PubMed]
- Chandrashekar, D.S.; Karthikeyan, S.K.; Korla, P.K.; Patel, H.; Shovon, A.R.; Athar, M.; Netto, G.J.; Qin, Z.S.; Kumar, S.; Manne, U.; et al. UALCAN: An update to the integrated cancer data analysis platform. Neoplasia 2022, 25, 18–27. [Google Scholar] [CrossRef] [PubMed]
- Uhlen, M.; Oksvold, P.; Fagerberg, L.; Lundberg, E.; Jonasson, K.; Forsberg, M.; Zwahlen, M.; Kampf, C.; Wester, K.; Hober, S.; et al. Towards a knowledge-based Human Protein Atlas. Nat. Biotechnol. 2010, 28, 1248–1250. [Google Scholar] [CrossRef]
- Giginis, F.; Wang, J.; Chavez, A.; Martins-Green, M. Catalase as a novel drug target for metastatic castration-resistant prostate cancer. Am. J. Cancer Res. 2023, 13, 2644–2656. [Google Scholar]
- Casteels, M.; Croes, K.; Van Veldhoven, P.P.; Mannaerts, G.P. Aminotriazole is a potent inhibitor of alpha-oxidation of 3-methyl-substituted fatty acids in rat liver. Biochem. Pharmacol. 1994, 48, 1973–1975. [Google Scholar] [CrossRef] [PubMed]
- Tephly, T.R.; Hasegawa, E.; Baron, J. Effect of drugs on heme synthesis in the liver. Metabolism 1971, 20, 200–214. [Google Scholar] [CrossRef]
- Koop, D.R. Inhibition of ethanol-inducible cytochrome P450IIE1 by 3-amino-1,2,4-triazole. Chem. Res. Toxicol. 1990, 3, 377–383. [Google Scholar] [CrossRef]
- Sen, S.; Kawahara, B.; Chaudhuri, G. Maintenance of higher H2O2 levels, and its mechanism of action to induce growth in breast cancer cells: Important roles of bioactive catalase and PP2A. Free Radic. Biol. Med. 2012, 53, 1541–1551. [Google Scholar] [CrossRef]
- Onumah, O.E.; Jules, G.E.; Zhao, Y.; Zhou, L.; Yang, H.; Guo, Z. Overexpression of catalase delays G0/G1- to S-phase transition during cell cycle progression in mouse aortic endothelial cells. Free Radic. Biol. Med. 2009, 46, 1658–1667. [Google Scholar] [CrossRef] [PubMed]
- Pinthus, J.H.; Bryskin, I.; Trachtenberg, J.; Lu, J.P.; Singh, G.; Fridman, E.; Wilson, B.C. Androgen induces adaptation to oxidative stress in prostate cancer: Implications for treatment with radiation therapy. Neoplasia 2007, 9, 68–80. [Google Scholar] [CrossRef] [PubMed]
- Shiota, M.; Ushijima, M.; Tsukahara, S.; Nagakawa, S.; Okada, T.; Tanegashima, T.; Kobayashi, S.; Matsumoto, T.; Eto, M. Oxidative stress in peroxisomes induced by AR inhibition through peroxisome proliferator-activated receptor promotes enzalutamide resistance in PCa. Free Radic. Biol. Med. 2024, 221, 81–88. [Google Scholar] [CrossRef] [PubMed]
- Feng, Y.; Zhang, Y.; Li, H.; Wang, T.; Lu, F.; Liu, R.; Xie, G.; Song, L.; Huang, B.; Li, X.; et al. Enzalutamide inhibits PEX10 function and sensitizes prostate cancer cells to ROS activators. Cell Death Dis. 2024, 15, 559. [Google Scholar] [CrossRef] [PubMed]
- Lazniewska, J.; Li, K.L.; Johnson, I.R.D.; Sorvina, A.; Logan, J.M.; Martini, C.; Moore, C.; Ung, B.S.; Karageorgos, L.; Hickey, S.M.; et al. Dynamic interplay between sortilin and syndecan-1 contributes to prostate cancer progression. Sci. Rep. 2023, 13, 13489. [Google Scholar] [CrossRef] [PubMed]
- Safi, R.; Wardell, S.E.; Watkinson, P.; Qin, X.; Lee, M.; Park, S.; Krebs, T.; Dolan, E.L.; Blattler, A.; Tsuji, T.; et al. Androgen receptor monomers and dimers regulate opposing biological processes in prostate cancer cells. Nat. Commun. 2024, 15, 7675. [Google Scholar] [CrossRef] [PubMed]
- Helminen, L.; Huttunen, J.; Tulonen, M.; Aaltonen, N.; Niskanen, E.A.; Palvimo, J.J.; Paakinaho, V. Chromatin accessibility and pioneer factor FOXA1 restrict glucocorticoid receptor action in prostate cancer. Nucleic Acids Res. 2024, 52, 625–642. [Google Scholar] [CrossRef]
- Bui, A.T.; Huang, M.E.; Havard, M.; Laurent-Tchenio, F.; Dautry, F.; Tchenio, T. Transient exposure to androgens induces a remarkable self-sustained quiescent state in dispersed prostate cancer cells. Cell Cycle 2017, 16, 879–893. [Google Scholar] [CrossRef]
- Kumar, R.; Sena, L.A.; Denmeade, S.R.; Kachhap, S. The testosterone paradox of advanced prostate cancer: Mechanistic insights and clinical implications. Nat. Rev. Urol. 2023, 20, 265–278. [Google Scholar] [CrossRef]
- Cao, Y.Y.; Chen, Y.Y.; Wang, M.S.; Tong, J.J.; Xu, M.; Zhao, C.; Lin, H.Y.; Mei, L.C.; Dong, J.; Zhang, W.L.; et al. A catalase inhibitor: Targeting the NADPH-binding site for castration-resistant prostate cancer therapy. Redox Biol. 2023, 63, 102751. [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
Hussein, M.A.F.; Lismont, C.; Costa, C.F.; Li, H.; Claessens, F.; Fransen, M. Characterization of the Peroxisomal Proteome and Redox Balance in Human Prostate Cancer Cell Lines. Antioxidants 2024, 13, 1340. https://doi.org/10.3390/antiox13111340
Hussein MAF, Lismont C, Costa CF, Li H, Claessens F, Fransen M. Characterization of the Peroxisomal Proteome and Redox Balance in Human Prostate Cancer Cell Lines. Antioxidants. 2024; 13(11):1340. https://doi.org/10.3390/antiox13111340
Chicago/Turabian StyleHussein, Mohamed A. F., Celien Lismont, Cláudio F. Costa, Hongli Li, Frank Claessens, and Marc Fransen. 2024. "Characterization of the Peroxisomal Proteome and Redox Balance in Human Prostate Cancer Cell Lines" Antioxidants 13, no. 11: 1340. https://doi.org/10.3390/antiox13111340
APA StyleHussein, M. A. F., Lismont, C., Costa, C. F., Li, H., Claessens, F., & Fransen, M. (2024). Characterization of the Peroxisomal Proteome and Redox Balance in Human Prostate Cancer Cell Lines. Antioxidants, 13(11), 1340. https://doi.org/10.3390/antiox13111340