Carrier–Tumor Cell Membrane Interactions for Optimized Delivery of a Promising Drug, 4(RS)-4-F4t-Neuroprostane
Abstract
:1. Introduction
1.1. Liposomes in Cancer Treatment
1.2. Targeting Strategies: Significance of Membrane Fluidity
1.3. Oxylipins and Their Potential as Chemotherapeutics
2. Materials and Methods
2.1. Synthesis of F4t-NeuroP
2.2. Liposome Preparation
2.3. Physico-Chemical Characterization of Blank and F4t-NeuroP-Loaded Liposomes
2.4. Cell Culture
2.5. Cell Viability Assay
2.6. Statistical Analysis
3. Results
3.1. Cytotoxic Effect of 12 Free Isoprostanoids
3.2. Encapsulation of F4t-NeuroP in Liposomes
3.3. Liposome Characterization
3.4. Liposome Membrane Fluidity Assessment
3.5. Cytotoxicity Effect of F4t-NeuroP Liposomes on PC-3 Prostate Tumor Cells
4. Discussion
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Anand, U.; Dey, A.; Chandel, A.K.S.; Sanyal, R.; Mishra, A.; Pandey, D.K.; De Falco, V.; Upadhyay, A.; Kandimalla, R.; Chaudhary, A.; et al. Cancer Chemotherapy and beyond: Current Status, Drug Candidates, Associated Risks and Progress in Targeted Therapeutics. Genes Dis. 2023, 10, 1367–1401. [Google Scholar] [CrossRef] [PubMed]
- Park, H.; Otte, A.; Park, K. Evolution of Drug Delivery Systems: From 1950 to 2020 and Beyond. J. Control. Release 2022, 342, 53–65. [Google Scholar] [CrossRef] [PubMed]
- Hare, J.I.; Lammers, T.; Ashford, M.B.; Puri, S.; Storm, G.; Barry, S.T. Challenges and Strategies in Anti-Cancer Nanomedicine Development: An Industry Perspective. Adv. Drug Deliv. Rev. 2017, 108, 25–38. [Google Scholar] [CrossRef] [PubMed]
- Bober, Z.; Bartusik-Aebisher, D.; Aebisher, D. Application of Dendrimers in Anticancer Diagnostics and Therapy. Molecules 2022, 27, 3237. [Google Scholar] [CrossRef] [PubMed]
- Lukyanov, A.N.; Torchilin, V.P. Micelles from Lipid Derivatives of Water-Soluble Polymers as Delivery Systems for Poorly Soluble Drugs. Adv. Drug Deliv. Rev. 2004, 56, 1273–1289. [Google Scholar] [CrossRef] [PubMed]
- Zhong, X.; Yang, J.; Liu, H.; Yang, Z.; Luo, P. Potential Lipid-Based Strategies of Amphotericin B Designed for Oral Administration in Clinical Application. Drug Deliv. 2023, 30, 2161671. [Google Scholar] [CrossRef] [PubMed]
- Mo, K.; Kim, A.; Choe, S.; Shin, M.; Yoon, H. Overview of Solid Lipid Nanoparticles in Breast Cancer Therapy. Pharmaceutics 2023, 15, 2065. [Google Scholar] [CrossRef] [PubMed]
- Metselaar, J.M.; Storm, G. Liposomes in the Treatment of Inflammatory Disorders. Expert. Opin. Drug Deliv. 2005, 2, 465–476. [Google Scholar] [CrossRef]
- Bulbake, U.; Doppalapudi, S.; Kommineni, N.; Khan, W. Liposomal Formulations in Clinical Use: An Updated Review. Pharmaceutics 2017, 9, 12. [Google Scholar] [CrossRef]
- Sharma, A.; Sharma, U.S. Liposomes in Drug Delivery: Progress and Limitations. Int. J. Pharm. 1997, 154, 123–140. [Google Scholar] [CrossRef]
- Ulrich, A.S. Biophysical Aspects of Using Liposomes as Delivery Vehicles. Biosci. Rep. 2002, 22, 129–150. [Google Scholar] [CrossRef] [PubMed]
- Mansour, A.; Hagop, K.; Tapan, K.; Farhad, R.-K.; Naval, D. CPX-351 (Vyxeos) in AML. Leuk. Lymphoma 2019, 61, 288–297. [Google Scholar]
- Liu, P.; Chen, G.; Zhang, J. A Review of Liposomes as a Drug Delivery System: Current. Molecules 2022, 27, 1372. [Google Scholar] [CrossRef] [PubMed]
- Tenchov, R.; Bird, R.; Curtze, A.E.; Zhou, Q. Lipid Nanoparticles from Liposomes to MRNA Vaccine Delivery, a Landscape of Research Diversity and Advancement. ACS Nano 2021, 15, 16982–17015. [Google Scholar] [CrossRef] [PubMed]
- Khan, A.A.; Allemailem, K.S.; Almatroodi, S.A.; Almatroudi, A.; Rahmani, A.H. Recent Strategies towards the Surface Modification of Liposomes: An Innovative Approach for Different Clinical Applications. 3 Biotech 2020, 10, 163. [Google Scholar] [CrossRef] [PubMed]
- Merino, M.; Zalba, S.; Garrido, M.J. Immunoliposomes in Clinical Oncology: State of the Art and Future Perspectives. J. Control. Release 2018, 275, 162–176. [Google Scholar] [CrossRef] [PubMed]
- Sheikh, A.; Alhakamy, N.A.; Md, S.; Kesharwani, P. Recent Progress of RGD Modified Liposomes as Multistage Rocket Against Cancer. Front. Pharmacol. 2022, 12, 803304. [Google Scholar] [CrossRef] [PubMed]
- Kumar, P.; Huo, P.; Liu, B. Formulation Strategies for Folate-Targeted Liposomes and Their Biomedical Applications. Pharmaceutics 2019, 11, 381. [Google Scholar] [CrossRef]
- Song, Z.; Lin, Y.; Zhang, X.; Feng, C.; Lu, Y.; Gao, Y.; Dong, C. Cyclic RGD Peptide-Modified Liposomal Drug Delivery System for Targeted Oral Apatinib Administration: Enhanced Cellular Uptake and Improved Therapeutic Effects. Int. J. Nanomed. 2017, 12, 1941–1958. [Google Scholar] [CrossRef]
- Deliconstantinos, G.; Kopeikina-Tsiboukidou, L.; Villiotou, V. Evaluation of Membrane Fluidity Effects and Enzyme Activities Alterations in Adriamycin Neurotoxicity. Biochem. Pharmacol. 1987, 36, 1153–1161. [Google Scholar] [CrossRef]
- Edmond, V.; Dufour, F.; Poiroux, G.; Shoji, K.; Malleter, M.; Fouqué, A.; Tauzin, S.; Rimokh, R.; Sergent, O.; Penna, A.; et al. Downregulation of Ceramide Synthase-6 during Epithelial-to-Mesenchymal Transition Reduces Plasma Membrane Fluidity and Cancer Cell Motility. Oncogene 2015, 34, 996–1005. [Google Scholar] [CrossRef] [PubMed]
- Zouaoui, J.; Trunfio-Sfarghiu, A.M.; Brizuela, L.; Piednoir, A.; Maniti, O.; Munteanu, B.; Mebarek, S.; Girard-Egrot, A.; Landoulsi, A.; Granjon, T. Multi-Scale Mechanical Characterization of Prostate Cancer Cell Lines: Relevant Biological Markers to Evaluate the Cell Metastatic Potential. Biochim. Biophys. Acta-Gen. Subj. 2017, 1861, 3109–3119. [Google Scholar] [CrossRef] [PubMed]
- Sok, M.; Schara, M.; Stare, J. Cell membrane fluidity and prognosis of lung cancer. Ann. Thorac. Surg. 2002, 73, S1567–S1571. [Google Scholar] [CrossRef] [PubMed]
- Hattori, T.; Andoh, T.; Sakai, N.; Yamada, H.; Kameyama, Y.; Ohki, K.; Nozawa, Y. Membrane Phospholipid Composition and Membrane Fluidity of Human Brain Tumour: A Spin Label Study. Neurol. Res. 1987, 9, 38–43. [Google Scholar] [CrossRef] [PubMed]
- Komizu, Y.; Ueoka, H.; Ueoka, R. Selective Accumulation and Growth Inhibition of Hybrid Liposomes to Human Hepatocellular Carcinoma Cells in Relation to Fluidity of Plasma Membranes. Biochem. Biophys. Res. Commun. 2012, 418, 81–86. [Google Scholar] [CrossRef] [PubMed]
- Bompard, J.; Rosso, A.; Brizuela, L.; Mebarek, S.; Blum, L.J.; Trunfio-Sfarghiu, A.M.; Lollo, G.; Granjon, T.; Girard-Egrot, A.; Maniti, O. Membrane Fluidity as a New Means to Selectively Target Cancer Cells with Fusogenic Lipid Carriers. Langmuir 2020, 36, 5134–5144. [Google Scholar] [CrossRef] [PubMed]
- Abawi, A.; Wang, X.; Bompard, J.; Bérot, A.; Andretto, V.; Gudimard, L.; Devillard, C.; Petiot, E.; Joseph, B.; Lollo, G.; et al. Monomethyl Auristatin e Grafted-liposomes to Target Prostate Tumor Cell Lines. Int. J. Mol. Sci. 2021, 22, 4103. [Google Scholar] [CrossRef] [PubMed]
- Gutierrez-Pajares, J.L.; Ben Hassen, C.; Oger, C.; Galano, J.M.; Durand, T.; Frank, P.G. Oxidized Products of α-Linolenic Acid Negatively Regulate Cellular Survival and Motility of Breast Cancer Cells. Biomolecules 2020, 10, 50. [Google Scholar] [CrossRef] [PubMed]
- Kinghorn, A.D.; Carcache De Blanco, E.J.; Lucas, D.M.; Rakotondraibe, H.L.; Orjala, J.; Soejarto, D.D.; Oberlies, N.H.; Pearce, C.J.; Wani, M.C.; Stockwell, B.R.; et al. Discovery of Anticancer Agents of Diverse Natural Origin. Anticancer Res. 2016, 36, 5623–5637. [Google Scholar] [CrossRef] [PubMed]
- Ahme, O.S.; Galano, J.M.; Pavlickova, T.; Revol-Cavalier, J.; Vigor, C.; Lee, J.C.Y.; Oger, C.; Durand, T. Moving Forward with Isoprostanes, Neuroprostanes and Phytoprostanes: Where Are We Now? Essays Biochem. 2020, 64, 463–484. [Google Scholar]
- Geng, X.; Galano, J.M.; Oger, C.; Sun, G.Y.; Durand, T.; Lee, J.C. Neuroprotective Effects of DHA-Derived Peroxidation Product 4(RS)-4-F4t-Neuroprostane on Microglia. Free Radic. Biol. Med. 2022, 185, 1–5. [Google Scholar] [CrossRef] [PubMed]
- Karg, K.; Dirsch, V.M.; Vollmar, A.M.; Cracowski, J.L.; Laporte, F.; Mueller, M.J. Biologically Active Oxidized Lipids (Phytoprostanes) in the Plant Diet and Parenteral Lipid Nutrition. Free Radic. Res. 2007, 41, 25–37. [Google Scholar] [CrossRef] [PubMed]
- Roy, J.; Oliveira, L.T.; Oger, C.; Galano, J.M.; Bultel-Poncé, V.; Richard, S.; Guimaraes, A.G.; Vilela, J.M.C.; Andrade, M.S.; Durand, T.; et al. Polymeric Nanocapsules Prevent Oxidation of Core-Loaded Molecules: Evidence Based on the Effects of Docosahexaenoic Acid and Neuroprostane on Breast Cancer Cells Proliferation. J. Exp. Clin. Cancer Res. 2015, 34, 155. [Google Scholar] [CrossRef] [PubMed]
- Oger, C.; Brinkmann, Y.; Bouazzaoui, S.; Durand, T.; Galano, J.M. Stereocontrolled Access to Isoprostanes via a Bicyclo[3.3.0]Octene Framework. Org. Lett. 2008, 10, 5087–5090. [Google Scholar] [CrossRef] [PubMed]
- Oger, C.; Bultel-Poncé, V.; Guy, A.; Balas, L.; Rossi, J.C.; Durand, T.; Galano, J.M. The Handy Use of Brown’s P2-Ni Catalyst for a Skipped Diyne Deuteration: Application to the Synthesis of a [D4]-Labeled F4t- Neuroprostane. Chem.-Eur. J. 2010, 16, 13976–13980. [Google Scholar] [CrossRef] [PubMed]
- Parasassi, T.; Gratton, E. Membrane Lipid Domains and Dynamics as Detected by Laurdan Fluorescence. J. Fluoresc. 1995, 5, 59–69. [Google Scholar] [CrossRef] [PubMed]
- Parasassi, T.; Krasnowska, E.K.; Bagatolli, L.; Gratton, E. Laurdan and Prodan as Polarity-Sensitive Fluorescent Membrane Probes. J. Fluoresc. 1998, 8, 365–373. [Google Scholar] [CrossRef]
- Gingrich, J.R.; Tucker, J.A.; Walther, P.J.; Day, J.W.; Poulton, S.H.M.; Webb, K.S. Establishment and Characterization of a New Human Prostatic Carcinoma Cell Line (DuPro-1). J. Urol. 1991, 146, 915–919. [Google Scholar] [CrossRef] [PubMed]
- Präbst, K.; Engelhardt, H.; Ringgeler, S.; Hübner, H. Basic Colorimetric Proliferation Assays: MTT, WST, and Resazurin. Methods Mol. Biol. 2017, 1601, 1–17. [Google Scholar] [CrossRef]
- Costa, P.; Gomes, A.T.P.C.; Braz, M.; Pereira, C.; Almeida, A. Application of the Resazurin Cell Viability Assay to Monitor Escherichia Coli and Salmonella Typhimurium Inactivation Mediated by Phages. Antibiotics 2021, 10, 974. [Google Scholar] [CrossRef]
- Chen, T.; Zhang, X.; Ding, X.; Feng, J.; Zhang, X.; Xie, D.; Wang, X. Ryanodine Receptor 2 Promotes Colorectal Cancer Metastasis by the ROS/BACH1 Axis. Mol. Oncol. 2023, 17, 695–709. [Google Scholar] [CrossRef] [PubMed]
- Morrow, J.D.; Hill, K.E.; Burk, R.F.; Nammour, T.M.; Badr, K.F.; Roberts, L.J. A Series of Prostaglandin F2-like Compounds Are Produced in Vivo in Humans by a Non-Cyclooxygenase, Free Radical-Catalyzed Mechanism. Proc. Natl. Acad. Sci. USA 1990, 87, 9383–9387. [Google Scholar] [CrossRef] [PubMed]
- Savchenko, T.; Degtyaryov, E.; Radzyukevich, Y.; Buryak, V. Therapeutic Potential of Plant Oxylipins. Int. J. Mol. Sci. 2022, 23, 14627. [Google Scholar] [CrossRef] [PubMed]
- Roberts, S.A.; Lee, C.; Singh, S.; Agrawal, N. Versatile Encapsulation and Synthesis of Potent Liposomes by Thermal Equilibration. Membranes 2022, 12, 319. [Google Scholar] [CrossRef] [PubMed]
- Roerdink, F.; Wassef, N.M.; Richardson, E.C.; Alving, C.R. Effects of Negatively Charged Lipids on Phagocytosis of Liposomes Opsonized by Complement. Cancer Res. 1983, 734, 33–39. [Google Scholar] [CrossRef] [PubMed]
- Röhrig, F.; Schulze, A. The Multifaceted Roles of Fatty Acid Synthesis in Cancer. Nat. Rev. Cancer 2016, 16, 732–749. [Google Scholar] [CrossRef] [PubMed]
- Aeffner, S.; Reusch, T.; Weinhausen, B.; Salditt, T. Energetics of Stalk Intermediates in Membrane Fusion Are Controlled by Lipid Composition. Proc. Natl. Acad. Sci. USA 2012, 109, E1609–E1618. [Google Scholar] [CrossRef] [PubMed]
- Kasson, P.M.; Pande, V.S. Control of Membrane Fusion Mechanism by Lipid Composition: Predictions from Ensemble Molecular Dynamics. PLoS Comput. Biol. 2007, 3, 2228–2238. [Google Scholar] [CrossRef]
- Butler, L.M.; Mah, C.Y.; Machiels, J.; Vincent, A.D.; Irani, S.; Mutuku, S.M.; Spotbeen, X.; Bagadi, M.; Waltregny, D.; Moldovan, M.; et al. Lipidomic Profiling of Clinical Prostate Cancer Reveals Targetable Alterations in Membrane Lipid Composition. Cancer Res. 2021, 81, 4981–4993. [Google Scholar] [CrossRef]
- Zhang, Z.; Wang, W.; Kong, P.; Feng, K.; Liu, C.; Sun, T.; Sang, Y.; Duan, X.; Tao, Z.; Liu, W. New Insights into Lipid Metabolism and Prostate Cancer (Review). Int. J. Oncol. 2023, 62, 74. [Google Scholar] [CrossRef]
Molar% | Liposome Preparation | Acyl Chain Composition | Lipid Name and Structure | Tm |
---|---|---|---|---|
Main lipid (80%) | PO | 16:0-18:1 PC | POPC 1-palmitoyl-2-oleoyl-glycero-3-phosphocholine | −4 °C |
DP | 16:0 PC | DPPC 1,2-dipalmitoyl-glycero-3-phosphocholine | 41 °C | |
Fusogenic lipid (20%) | All preparations | 18:1 (Δ9-Cis) PE | DOPE 1,2-dioleoyl-sn-glycero-3-phosphoethanolamine | −16 °C |
4(RS)-4-F4t-Neuroprostane (0.7% on total lipid mass) | In two preparations |
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. |
© 2023 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
Abawi, A.; Thomann, C.; Lollo, G.; Granjon, T.; Petiot, E.; Bérot, A.; Oger, C.; Bultel-Poncé, V.; Guy, A.; Galano, J.-M.; et al. Carrier–Tumor Cell Membrane Interactions for Optimized Delivery of a Promising Drug, 4(RS)-4-F4t-Neuroprostane. Pharmaceutics 2023, 15, 2739. https://doi.org/10.3390/pharmaceutics15122739
Abawi A, Thomann C, Lollo G, Granjon T, Petiot E, Bérot A, Oger C, Bultel-Poncé V, Guy A, Galano J-M, et al. Carrier–Tumor Cell Membrane Interactions for Optimized Delivery of a Promising Drug, 4(RS)-4-F4t-Neuroprostane. Pharmaceutics. 2023; 15(12):2739. https://doi.org/10.3390/pharmaceutics15122739
Chicago/Turabian StyleAbawi, Ariana, Céline Thomann, Giovanna Lollo, Thierry Granjon, Emma Petiot, Anna Bérot, Camille Oger, Valérie Bultel-Poncé, Alexandre Guy, Jean-Marie Galano, and et al. 2023. "Carrier–Tumor Cell Membrane Interactions for Optimized Delivery of a Promising Drug, 4(RS)-4-F4t-Neuroprostane" Pharmaceutics 15, no. 12: 2739. https://doi.org/10.3390/pharmaceutics15122739
APA StyleAbawi, A., Thomann, C., Lollo, G., Granjon, T., Petiot, E., Bérot, A., Oger, C., Bultel-Poncé, V., Guy, A., Galano, J.-M., Durand, T., Girard-Egrot, A., & Maniti, O. (2023). Carrier–Tumor Cell Membrane Interactions for Optimized Delivery of a Promising Drug, 4(RS)-4-F4t-Neuroprostane. Pharmaceutics, 15(12), 2739. https://doi.org/10.3390/pharmaceutics15122739