Sodium Thiosulphate-Loaded Liposomes Control Hydrogen Sulphide Release and Retain Its Biological Properties in Hypoxia-like Environment
Abstract
:1. Introduction
2. Materials and Methods
2.1. Reagents and Drugs
2.2. Preparation of STS Loaded Liposomes
2.3. Liposome Characterisation: Particle Size, Polydispersity and zeta Potential
2.4. HPLC Methodology
2.5. Determination of Entrapment Efficiency
2.6. Cell Culture
2.7. Cellular Uptake of STS
2.8. Determination of H2S Release
2.9. Quantitative RT-PCR (qPCR)
2.10. ELISA
2.11. Cell Migration Assay
2.12. Capillary-Like Tube Formation Assay
2.13. Mitochondrial and Glycolytic Function
2.14. ATP Levels
2.15. Statistical Analysis
3. Results
3.1. Influence of Cholesterol and DOTAP on Liposome Characteristics
3.2. Cellular Uptake of STS
3.3. H2S Release from Liposomal Formulated and Non-Formulated STS
3.4. Formulation of STS into Liposomes Retain Pro-Angiogenic Properties of STS
3.5. Liposomal STS Promotes Mitochondrial Function under Hypoxia
3.6. Liposomal STS Promotes Cellular Metabolic Switch Favouring Mitochondrial Function in Hypoxia-Like Environment
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Timmis, A.; Vardas, P.; Townsend, N.; Torbica, A.; Katus, H.; De Smedt, D.; Gale, C.P.; Maggioni, A.P.; Petersen, S.E.; Huculeci, R.; et al. European Society of Cardiology: Cardio-vascular disease statistics 2021. Eur. Heart J. 2022, 43, 716–799. [Google Scholar] [CrossRef] [PubMed]
- Krock, B.L.; Skuli, N.; Simon, M.C. Hypoxia-Induced Angiogenesis: Good and Evil. Genes Cancer 2011, 2, 1117–1133. [Google Scholar] [CrossRef] [Green Version]
- Mitroshina, E.V.; Savyuk, M.O.; Ponimaskin, E.; Vedunova, M.V. Hypoxia-Inducible Factor (HIF) in Ischemic Stroke and Neurodegenerative Disease. Front. Cell Dev. Biol. 2021, 9, 2014. [Google Scholar] [CrossRef] [PubMed]
- Hashimoto, T.; Shibasaki, F. Hypoxia-Inducible Factor as an Angiogenic Master Switch. Front. Pediatr. 2015, 3, 33. [Google Scholar] [CrossRef] [Green Version]
- Koitabashi, N.; Kass, D.A. Reverse remodeling in heart failure—mechanisms and therapeutic opportunities. Nat. Rev. Cardiol. 2011, 9, 147–157. [Google Scholar] [CrossRef]
- Szabó, C. Hydrogen sulphide and its therapeutic potential. Nat. Rev. Drug Discov. 2007, 6, 917–935. [Google Scholar] [CrossRef] [PubMed]
- Zhao, W.; Zhang, J.; Lu, Y.; Wang, R. The vasorelaxant effect of H2S as a novel endogenous gaseous KATP channel opener. EMBO J. 2001, 20, 6008–6016. [Google Scholar] [CrossRef] [Green Version]
- Kimura, H.; Shibuya, N.; Kimura, Y. Hydrogen Sulfide Is a Signaling Molecule and a Cytoprotectant. Antioxid. Redox Signal. 2012, 17, 45–57. [Google Scholar] [CrossRef] [Green Version]
- Sanchez, L.D.; Sanchez-Aranguren, L.; Marwah, M.; Wang, K.; Spickett, C.M.; Griffiths, H.R.; Dias, I.H. Exploring mitochondrial hydrogen sulfide signalling for therapeutic interventions in vascular diseases. Adv. Redox Res. 2022, 4, 100030. [Google Scholar] [CrossRef]
- Fu, M.; Zhang, W.; Wu, L.; Yang, G.; Li, H.; Wang, R. Hydrogen sulfide (H 2 S) metabolism in mitochondria and its regulatory role in energy production. Proc. Natl. Acad. Sci. USA 2012, 109, 2943–2948. [Google Scholar] [CrossRef]
- Papapetropoulos, A.; Pyriochou, A.; Altaany, Z.; Yang, G.; Marazioti, A.; Zhou, Z.; Jeschke, M.G.; Branski, L.K.; Herndon, D.N.; Wang, R.; et al. Hydrogen sulfide is an endogenous stimulator of angiogenesis. Proc. Natl. Acad. Sci. USA 2009, 106, 21972–21977. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zanardo, R.C.O.; Brancaleone, V.; Distrutti, E.; Fiorucci, S.; Cirino, G.; Wallace, J.L. Hydrogen sulfide is an endogenous modulator of leukocyte-mediated inflammation. FASEB J. 2006, 20, 2118–2120. [Google Scholar] [CrossRef] [PubMed]
- Bos, E.M.; Wang, R.; Snijder, P.M.; Boersema, M.; Damman, J.; Fu, M.; Moser, J.; Hillebrands, J.L.; Ploeg, R.J.; Yang, G.; et al. Cystathionine γ-lyase protects against renal ische-mia/reperfusion by modulating oxidative stress. J. Am. Soc. Nephrol. 2013, 24, 759–770. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Murphy, B.; Bhattacharya, R.; Mukherjee, P. Hydrogen sulfide signaling in mitochondria and disease. FASEB J. 2019, 33, 13098–13125. [Google Scholar] [CrossRef] [Green Version]
- Szabó, G.; Veres, G.; Radovits, T.; Gero, D.; Módis, K.; Miesel-Gröschel, C.; Horkay, F.; Karck, M.; Szabó, C. Cardioprotective effects of hydrogen sulfide. Nitric Oxide 2011, 25, 201–210. [Google Scholar] [CrossRef] [Green Version]
- Liu, X.; Pan, L.; Zhuo, Y.; Gong, Q.; Rose, P.; Zhu, Y. Hypoxia-Inducible Factor-1.ALPHA. Is Involved in the Pro-angiogenic Effect of Hydrogen Sulfide under Hypoxic Stress. Biol. Pharm. Bull. 2010, 33, 1550–1554. [Google Scholar] [CrossRef] [Green Version]
- Polhemus, D.J.; Calvert, J.W.; Butler, J.; Lefer, D.J. The Cardioprotective Actions of Hydrogen Sulfide in Acute Myocardial Infarction and Heart Failure. Scientifica 2014, 2014, 768607. [Google Scholar] [CrossRef] [Green Version]
- Distrutti, E.; Sediari, L.; Mencarelli, A.; Renga, B.; Orlandi, S.; Antonelli, E.; Roviezzo, F.; Morelli, A.; Cirino, G.; Wallace, J.L.; et al. Evidence that hydrogen sulfide exerts antino-ciceptive effects in the gastrointestinal tract by activating KATP channels. J. Pharmacol. Exp. Ther. 2006, 316, 325–335. [Google Scholar] [CrossRef] [Green Version]
- Paquette, J.-M.; Rufiange, M.; Iovu Niculita, M.; Massicotte, J.; Lefebvre, M.; Colin, P.; Telmat, A.; Ranger, M. Safety, Tolerability and Pharmacokinetics of Trimebutine 3-Thiocarbamoylbenzenesulfonate (GIC-1001) in a Randomized Phase I Integrated Design Study: Single and Multiple Ascending Doses and Effect of Food in Healthy Volunteers. Clin. Ther. 2014, 36, 1650–1664. [Google Scholar] [CrossRef]
- Sen, U.; Vacek, T.P.; Hughes, W.M.; Kumar, M.; Moshal, K.S.; Tyagi, N.; Metreveli, N.; Hayden, M.R.; Tyagi, S.C. Cardioprotective Role of Sodium Thiosulfate on Chronic Heart Failure by Modulating Endogenous H2S Generation. Pharmacology 2008, 82, 201–213. [Google Scholar] [CrossRef]
- Sen, U.; Basu, P.; Abe, O.A.; Givvimani, S.; Tyagi, N.; Metreveli, N.; Shah, K.S.; Passmore, J.C.; Tyagi, S.C. Hydrogen sulfide ameliorates hyperhomocyste-inemia-associated chronic renal failure. Am. J. Physiol. Ren. Physiol. 2009, 297, F410–F419. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bijarnia, R.K.; Bachtler, M.; Chandak, P.G.; Van Goor, H.; Pasch, A. Sodium Thiosulfate Ameliorates Oxidative Stress and Preserves Renal Function in Hyperoxaluric Rats. PLoS ONE 2015, 10, e0124881. [Google Scholar] [CrossRef] [PubMed]
- Halliday, H.M.; Sutherland, C.E. Arsenical poisoning treated by sodium thiosulphate. BMJ 1925, 1, 407. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shiels, D.O. The treatment of lead poisoning by the intravenous administration of sodium thiosulphate. Med. J. Aust. 1952, 1, 879–882. [Google Scholar] [CrossRef]
- Dart, R.C. Medical Toxicology, 3rd ed.; Lippincott, Williams & Wilkins: Philadelphia, PA, USA, 2004. [Google Scholar]
- De Koning, M.S.L.; Assa, S.; Maagdenberg, C.G.; van Veldhuisen, D.J.; Pasch, A.; van Goor, H.; Lipsic, E.; van der Harst, P. Safety and Tolerability of Sodium Thiosulfate in Patients with an Acute Coronary Syndrome Undergoing Coronary Angiography: A Dose-Escalation Safety Pilot Study (SAFE-ACS). J. Interv. Cardiol. 2020, 2020, 6014915. [Google Scholar] [CrossRef]
- Nevozhay, D.; Kańska, U.; Budzyńska, R.; Boratyński, J. Current status of research on conjugates and related drug delivery systems in the treatment of cancer and other diseases. Postepy Hig. I Med. Dosw. Online 2007, 61, 350–360. [Google Scholar]
- Zhang, Y.; Wang, Z.; Gemeinhart, R.A. Progress in microRNA delivery. J. Control. Release 2013, 172, 962–974. [Google Scholar] [CrossRef] [Green Version]
- Franco, S.M.; Oliveira, C.M. Liposomes Co-encapsulating Anticancer Drugs in Synergistic Ratios as an Approach to Promote Increased Efficacy and Greater Safety. Anti Cancer Agents Med. Chem. 2019, 19, 17–28. [Google Scholar] [CrossRef]
- Northfelt, D.W.; Martin, F.J.; Working, P.; Volberding, P.A.; Russell, J.; Newman, M.; Amantea, M.A.; Kaplan, L.D. Doxorubicin Encapsulated in Liposomes Containing Surface-Bound Polyethylene Glycol: Pharmacokinetics, Tumor Localization, and Safety in Patients with AIDS-Related Kaposi’s Sarcoma. J. Clin. Pharmacol. 1996, 36, 55–63. [Google Scholar] [CrossRef]
- Batzri, S.; Korn, E.D. Single bilayer liposomes prepared without sonication. Biochim. Biophys. Acta BBA Biomembr. 1973, 298, 1015–1019. [Google Scholar] [CrossRef]
- Marwah, M.K.; Shokr, H.; Sanchez-Aranguren, L.; Badhan, R.K.S.; Wang, K.; Ahmad, S. Transdermal Delivery of a Hydrogen Sulphide Donor, ADT-OH Using Aqueous Gel Formulations for the Treatment of Impaired Vascular Function: An Ex Vivo Study. Pharm. Res. 2022, 39, 341–352. [Google Scholar] [CrossRef] [PubMed]
- Song, Y.-K.; Kim, C.-K. Topical delivery of low-molecular-weight heparin with surface-charged flexible liposomes. Biomaterials 2006, 27, 271–280. [Google Scholar] [CrossRef] [PubMed]
- Schulz, L.T.; Elder, E.J.; Jones, K.J.; Vijayan, A.; Johnson, B.D.; Medow, J.E.; Vermeulen, L. Stability of Sodium Nitroprusside and Sodium Thiosulfate 1:10 Intravenous Admixture. Hosp. Pharm. 2010, 45, 779–784. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Edgell, C.J.; McDonald, C.C.; Graham, J.B. Permanent cell line expressing human factor VIII-related antigen established by hybridization. Proc. Natl. Acad. Sci. USA 1983, 80, 3734–3737. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rana, N.K.; Singh, P.; Koch, B. CoCl2 simulated hypoxia induce cell proliferation and alter the expression pattern of hypoxia associated genes involved in angiogenesis and apoptosis. Biol. Res. 2019, 52, 12. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sanchez-Aranguren, L.C.; Ahmad, S.; Dias, I.H.K.; Alzahrani, F.A.; Rezai, H.; Wang, K.; Ahmed, A. Bioenergetic effects of hydrogen sulfide suppress soluble Flt-1 and soluble endoglin in cystathionine gamma-lyase compromised endothelial cells. Sci. Rep. 2020, 10, 15810. [Google Scholar] [CrossRef] [PubMed]
- Sanchez-Aranguren, L.C.; Espinosa-González, C.T.; González-Ortiz, L.M.; Sanabria-Barrera, S.M.; Riaño-Medina, C.E.; Nuñez, A.F.; Ahmed, A.; Vasquez-Vivar, J.; López, M. Soluble Fms-Like Tyrosine Kinase-1 Alters Cellular Metabolism and Mitochondrial Bioenergetics in Preeclampsia. Front. Physiol. 2018, 9, 83. [Google Scholar] [CrossRef] [Green Version]
- Ademowo, O.S.; Dias, I.H.K.; Diaz-Sanchez, L.; Sanchez-Aranguren, L.; Stahl, W.; Griffiths, H.R. Partial Mitigation of Oxidized Phospholipid-Mediated Mitochondrial Dysfunction in Neuronal Cells by Oxocarotenoids. J. Alzheimer’s Dis. 2020, 74, 113–126. [Google Scholar] [CrossRef] [Green Version]
- Bir, S.C.; Kolluru, G.K.; McCarthy, P.; Shen, X.; Pardue, S.; Pattillo, C.B.; Kevil, C.G. Hydrogen sulfide stimulates ischemic vascular re-modeling through nitric oxide synthase and nitrite reduction activity regulating hypoxia-inducible factor-1alpha and vascular endothelial growth factor-dependent angiogenesis. J. Am. Heart Assoc. 2012, 1, e004093. [Google Scholar] [CrossRef] [Green Version]
- Bianco, S.; Mancardi, D.; Merlino, A.; Bussolati, B.; Munaron, L. Hypoxia and hydrogen sulfide differentially affect normal and tumor-derived vascular endothelium. Redox Biol. 2017, 12, 499–504. [Google Scholar] [CrossRef]
- Gerő, D.; Torregrossa, R.; Perry, A.; Waters, A.; Le-Trionnaire, S.; Whatmore, J.L.; Wood, M.; Whiteman, M. The novel mitochondria-targeted hydrogen sulfide (H 2 S) donors AP123 and AP39 protect against hyperglycemic injury in microvascular endothelial cells in vitro. Pharmacol. Res. 2016, 113, 186–198. [Google Scholar] [CrossRef] [PubMed]
- Hu, L.F.; Lu, M.; Wu, Z.Y.; Wong, P.T.; Bian, J.S. Hydrogen sulfide inhibits rotenone-induced apoptosis via preservation of mi-tochondrial function. Mol. Pharmacol. 2009, 75, 27–34. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kashatus, D.F. The regulation of tumor cell physiology by mitochondrial dynamics. Biochem. Biophys. Res. Commun. 2018, 500, 9–16. [Google Scholar] [CrossRef] [PubMed]
- Meng, G.; Liu, J.; Liu, S.; Song, Q.; Liu, L.; Xie, L.; Han, Y.; Ji, Y. Hydrogen sulfide pretreatment improves mitochondrial function in myocardial hypertrophy via a SIRT3-dependent manner. Br. J. Pharmacol. 2018, 175, 1126–1145. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sanchez-Aranguren, L.C.; Rezai, H.; Ahmad, S.; Alzahrani, F.A.; Sparatore, A.; Wang, K.; Ahmed, A. MZe786 Rescues Cardiac Mito-chondrial Activity in High sFlt-1 and Low HO-1 Environment. Antioxidants 2020, 9, 598. [Google Scholar] [CrossRef] [PubMed]
- Robey, I.F.; Lien, A.D.; Welsh, S.J.; Baggett, B.K.; Gillies, R.J. Hypoxia-Inducible Factor-1α and the Glycolytic Phenotype in Tumors. Neoplasia 2005, 7, 324–330. [Google Scholar] [CrossRef] [Green Version]
- Kierans, S.J.; Taylor, C.T. Regulation of glycolysis by the hypoxia-inducible factor (HIF): Implications for cellular physiology. J. Physiol. 2021, 599, 23–37. [Google Scholar] [CrossRef]
- Liu, C.-X.; Tan, Y.-R.; Xiang, Y.; Liu, C.; Liu, X.-A.; Qin, X.-Q. Hydrogen Sulfide Protects against Chemical Hypoxia-Induced Injury via Attenuation of ROS-Mediated Ca2+ Overload and Mitochondrial Dysfunction in Human Bronchial Epithelial Cells. BioMed Res. Int. 2018, 2018, 2070971. [Google Scholar] [CrossRef] [Green Version]
- Calvert, J.W.; Jha, S.; Gundewar, S.; Elrod, J.W.; Ramachandran, A.; Pattillo, C.B.; Kevil, C.; Lefer, D.J. Hydrogen Sulfide Mediates Cardioprotection Through Nrf2 Signaling. Circ. Res. 2009, 105, 365–374. [Google Scholar] [CrossRef] [Green Version]
- Whiteman, M.; Le Trionnaire, S.; Chopra, M.; Fox, B.; Whatmore, J. Emerging role of hydrogen sulfide in health and disease: Critical appraisal of biomarkers and pharmacological tools. Clin. Sci. 2011, 121, 459–488. [Google Scholar] [CrossRef]
- Jiang, H.-L.; Wu, H.-C.; Li, Z.-L.; Geng, B.; Tang, C.-S. Changes of the new gaseous transmitter H2S in patients with coronary heart disease. Di Yi Jun Yi Da Xue Xue Bao Acad. J. first Med. Coll. PLA 2005, 25, 951–954. [Google Scholar]
- Liu, Y.-H.; Lu, M.; Hu, L.-F.; Wong, P.T.-H.; Webb, G.D.; Bian, J. Hydrogen Sulfide in the Mammalian Cardiovascular System. Antioxid. Redox Signal. 2012, 17, 141–185. [Google Scholar] [CrossRef] [PubMed]
- Elrod, J.W.; Calvert, J.W.; Morrison, J.; Doeller, J.E.; Kraus, D.W.; Tao, L.; Jiao, X.; Scalia, R.; Kiss, L. Hydrogen sulfide attenuates myocardial ische-mia-reperfusion injury by preservation of mitochondrial function. Proc. Natl. Acad. Sci. USA 2007, 104, 15560–15565. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hayden, M.R.; Tyagi, S.C.; Kolb, L.; Sowers, J.R.; Khanna, R. Vascular ossification-calcification in metabolic syndrome, type 2 diabetes mellitus, chronic kidney disease, and calciphylaxis-calcific uremic arteriolopathy: The emerging role of sodium thiosulfate. Cardiovasc. Diabetol. 2005, 4, 1–22. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Perridon, B.W.; Leuvenink, H.G.D.; Hillebrands, J.-L.; Van Goor, H.; Bos, E.M. The role of hydrogen sulfide in aging and age-related pathologies. Aging 2016, 8, 2264–2289. [Google Scholar] [CrossRef] [Green Version]
- Olson, K.R. The therapeutic potential of hydrogen sulfide: Separating hype from hope. Am. J. Physiol. Integr. Comp. Physiol. 2011, 301, R297–R312. [Google Scholar] [CrossRef] [Green Version]
- Kolluru, G.K.; Shen, X.; Bir, S.C.; Kevil, C.G. Hydrogen sulfide chemical biology: Pathophysiological roles and detection. Nitric Oxide 2013, 35, 5–20. [Google Scholar] [CrossRef] [Green Version]
- Zhang, M.Y.; Dugbartey, G.J.; Juriasingani, S.; Sener, A. Hydrogen Sulfide Metabolite, Sodium Thiosulfate: Clinical Applications and Underlying Molecular Mechanisms. Int. J. Mol. Sci. 2021, 22, 6452. [Google Scholar] [CrossRef]
- Olson, K.R.; DeLeon, E.R.; Gao, Y.; Hurley, K.; Sadauskas, V.; Batz, C.; Stoy, G.F. Thiosulfate: A readily accessible source of hydrogen sulfide in oxygen sensing. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2013, 305, R592–R603. [Google Scholar] [CrossRef] [Green Version]
- Shim, G.; Kim, M.-G.; Park, J.Y.; Oh, Y.-K. Application of cationic liposomes for delivery of nucleic acids. Asian J. Pharm. Sci. 2013, 8, 72–80. [Google Scholar] [CrossRef] [Green Version]
- Marwah, M.; Badhan, R.K.; Lowry, D. Development of a novel polymer-based carrier for deformable liposomes for the controlled dermal delivery of naringenin. J. Liposome Res. 2022, 32, 181–194. [Google Scholar] [CrossRef] [PubMed]
- Fu, Y.; Chen, J.; Huang, Z. Recent progress in microRNA-based delivery systems for the treatment of human disease. ExRNA 2019, 1, 24. [Google Scholar] [CrossRef]
- Saengkrit, N.; Saesoo, S.; Srinuanchai, W.; Phunpee, S.; Ruktanonchai, U.R. Influence of curcumin-loaded cationic liposome on anticancer activity for cervical cancer therapy. Colloids Surf. B Biointerfaces 2014, 114, 349–356. [Google Scholar] [CrossRef]
- Laouini, A.; Jaafar-Maalej, C.; Limayem-Blouza, I.; Sfar, S.; Charcosset, C.; Fessi, H. Preparation, Characterization and Applications of Liposomes: State of the Art. J. Colloid Sci. Biotechnol. 2012, 1, 147–168. [Google Scholar] [CrossRef]
- Petrikovics, I.; Jayanna, P.; Childress, J.; Budai, M.; Martin, S.; Kuzmitcheva, G.; Rockwood, G. Optimization of Liposomal Lipid Compo-sition for a New, Reactive Sulfur Donor, and In Vivo Efficacy Studies on Mice to Antagonize Cyanide Intoxication. J. Drug Deliv. 2011, 2011, 928626. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Socaciu, C.; Jessel, R.; Diehl, H.A. Competitive carotenoid and cholesterol incorporation into liposomes: Effects on membrane phase transition, fluidity, polarity and anisotropy. Chem. Phys. Lipids 2000, 106, 79–88. [Google Scholar] [CrossRef]
- Farzaneh, H.; Ebrahimi Nik, M.; Mashreghi, M.; Saberi, Z.; Jaafari, M.R.; Teymouri, M. A study on the role of cholesterol and phosphatidylcholine in various features of liposomal doxorubicin: From liposomal preparation to therapy. Int. J. Pharm. 2018, 551, 300–308. [Google Scholar] [CrossRef]
- Gregoriadis, G.; Davis, C. Stability of liposomes invivo and invitro is promoted by their cholesterol content and the presence of blood cells. Biochem. Biophys. Res. Commun. 1979, 89, 1287–1293. [Google Scholar] [CrossRef]
- Mohammed, A.; Weston, N.; Coombes, A.; Fitzgerald, M.; Perrie, Y. Liposome formulation of poorly water soluble drugs: Optimisation of drug loading and ESEM analysis of stability. Int. J. Pharm. 2004, 285, 23–34. [Google Scholar] [CrossRef]
- Patil, S.; Sandberg, A.; Heckert, E.; Self, W.; Seal, S. Protein adsorption and cellular uptake of cerium oxide nanoparticles as a function of zeta potential. Biomaterials 2007, 28, 4600–4607. [Google Scholar] [CrossRef] [Green Version]
- Chen, C.-C.; Tsai, T.-H.; Huang, Z.-R.; Fang, J.-Y. Effects of lipophilic emulsifiers on the oral administration of lovastatin from nanostructured lipid carriers: Physicochemical characterization and pharmacokinetics. Eur. J. Pharm. Biopharm. 2010, 74, 474–482. [Google Scholar] [CrossRef] [PubMed]
- Yu, K.O.; Grabinski, C.M.; Schrand, A.M.; Murdock, R.C.; Wang, W.; Gu, B.; Schlager, J.J.; Hussain, S.M. Toxicity of amorphous silica nanoparticles in mouse keratinocytes. J. Nanopart. Res. 2008, 11, 15–24. [Google Scholar] [CrossRef]
- Bernfield, M.; Götte, M.; Park, P.W.; Reizes, O.; Fitzgerald, M.L.; Lincecum, J.; Zako, M. Functions of Cell Surface Heparan Sulfate Proteoglycans. Annu. Rev. Biochem. 1999, 68, 729–777. [Google Scholar] [CrossRef] [PubMed]
- Mislick, K.A.; Baldeschwieler, J.D. Evidence for the role of proteoglycans in cation-mediated gene transfer. Proc. Natl. Acad. Sci. USA 1996, 93, 12349–12354. [Google Scholar] [CrossRef] [Green Version]
- Panyam, J.; Labhasetwar, V. Biodegradable nanoparticles for drug and gene delivery to cells and tissue. Adv. Drug Deliv. Rev. 2002, 55, 329–347. [Google Scholar] [CrossRef]
- Epstein-Barash, H.; Gutman, D.; Markovsky, E.; Mishan-Eisenberg, G.; Koroukhov, N.; Szebeni, J.; Golomb, G. Physicochemical pa-rameters affecting liposomal bisphosphonates bioactivity for restenosis therapy: Internalization, cell inhibition, activation of cytokines and complement, and mechanism of cell death. J. Control. Release 2010, 146, 182–195. [Google Scholar] [CrossRef]
- Takano, S.; Aramaki, Y.; Tsuchiya, S. Physicochemical properties of liposomes affecting apoptosis induced by cationic lip-osomes in macrophages. Pharm. Res. 2003, 20, 962–968. [Google Scholar] [CrossRef]
- Dabbas, S.; Kaushik, R.R.; Dandamudi, S.; Kuesters, G.M.; Campbell, R.B. Importance of the Liposomal Cationic Lipid Content and Type in Tumor Vascular Targeting: Physicochemical Characterization and In Vitro Studies Using Human Primary and Transformed Endothelial Cells. Endothelium 2008, 15, 189–201. [Google Scholar] [CrossRef]
- Jung, S.H.; Jung, S.H.; Seong, H.; Cho, S.H.; Jeong, K.-S.; Shin, B.C. Polyethylene glycol-complexed cationic liposome for enhanced cellular uptake and anticancer activity. Int. J. Pharm. 2009, 382, 254–261. [Google Scholar] [CrossRef]
- White, P.J.; Fogarty, R.D.; McKean, S.C.; Venables, D.J.; Werther, G.A.; Wraight, C.J. Oligonucleotide Uptake in Cultured Keratinocytes: Influence of Confluence, Cationic Liposomes, and Keratinocyte Cell Type. J. Investig. Dermatol. 1999, 112, 699–705. [Google Scholar] [CrossRef] [Green Version]
- Ito, A.; Fujioka, M.; Yoshida, T.; Wakamatsu, K.; Ito, S.; Yamashita, T.; Jimbow, K.; Honda, H. 4-S-Cysteaminylphenol-loaded magnetite cationic liposomes for combination therapy of hyperthermia with chemotherapy against malignant melanoma. Cancer Sci. 2007, 98, 424–430. [Google Scholar] [CrossRef] [PubMed]
- Snijder, P.M.; Frenay, A.R.; De Boer, R.A.; Pasch, A.; Hillebrands, J.L.; Leuvenink, H.G.D.; Van Goor, H. Exogenous administration of thiosulfate, a donor of hydrogen sulfide, attenuates angiotensin II-induced hypertensive heart disease in rats. Br. J. Pharmacol. 2015, 172, 1494–1504. [Google Scholar] [CrossRef] [PubMed]
- Giovinazzo, D.; Bursac, B.; Sbodio, J.I.; Nalluru, S.; Vignane, T.; Snowman, A.M.; Albacarys, L.M.; Sedlak, T.W.; Torregrossa, R.; Whiteman, M.; et al. Hydrogen sulfide is neuroprotective in Alzheimer’s disease by sulfhydrating GSK3β and inhibiting Tau hyperphosphorylation. Proc. Natl. Acad. Sci. USA 2021, 118, e2017225118. [Google Scholar] [CrossRef] [PubMed]
- Ni, X.; Zhang, L.; Peng, M.; Shen, T.-W.; Yu, X.-S.; Shan, L.-Y.; Li, L.; Si, J.-Q.; Li, X.-Z.; Ma, K.-T. Hydrogen Sulfide Attenuates Hypertensive Inflammation via Regulating Connexin Expression in Spontaneously Hypertensive Rats. Med. Sci. Monit. Int. Med. J. Exp. Clin. Res. 2018, 24, 1205–1218. [Google Scholar] [CrossRef]
- Leskova, A.; Pardue, S.; Glawe, J.D.; Kevil, C.G.; Shen, X. Role of thiosulfate in hydrogen sulfide-dependent redox signaling in endothelial cells. Am. J. Physiol. Circ. Physiol. 2017, 313, H256–H264. [Google Scholar] [CrossRef] [Green Version]
- Rezai, H.; Ahmad, S.; Alzahrani, F.A.; Sanchez-Aranguren, L.; Dias, I.H.; Agrawal, S.; Sparatore, A.; Wang, K.; Ahmed, A. MZe786, a hydrogen sulfide-releasing aspirin prevents preeclampsia in heme oxygenase-1 haplodeficient pregnancy under high soluble flt-1 environment. Redox Biol. 2020, 38, 101768. [Google Scholar] [CrossRef]
- Kondo, K.; Bhushan, S.; King, A.L.; Prabhu, S.D.; Hamid, T.; Koenig, S.; Murohara, T.; Predmore, B.L.; Gojon Sr, G.; Gojon, G., Jr.; et al. H2S protects against pressure overload-induced heart failure via upregulation of endothelial nitric oxide synthase. Circulation. Circulation 2013, 127, 1116–1127. [Google Scholar] [CrossRef] [Green Version]
- Abd Allah, E.S.H.; Ahmed, M.A.; Makboul, R.; Abd El-Rahman, M.A. Effects of hydrogen sulphide on oxidative stress, inflam-matory cytokines, and vascular remodelling in l-NAME-induced hypertension. Clin. Exp. Pharmacol. Physiol. 2020, 47, 650–659. [Google Scholar] [CrossRef]
- Goubern, M.; Andriamihaja, M.; Nübel, T.; Blachier, F.; Bouillaud, F. Sulfide, the first inorganic substrate for human cells. FASEB J. 2007, 21, 1699–1706. [Google Scholar] [CrossRef]
Formulation Number | PC | DOTAP | DSPC-PEG 2000 | Cholesterol |
---|---|---|---|---|
1 | 57.5 | 22.5 | 5 | 15 |
2 | 47.5 | 12.5 | 5 | 15 |
3 | 52.5 | 7.5 | 5 | 15 |
4 | 65 | 22.5 | 5 | 7.5 |
5 | 75 | 12.5 | 5 | 7.5 |
6 | 80 | 7.5 | 5 | 7.5 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 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
Sanchez-Aranguren, L.; Grubliauskiene, M.; Shokr, H.; Balakrishnan, P.; Wang, K.; Ahmad, S.; Marwah, M.K. Sodium Thiosulphate-Loaded Liposomes Control Hydrogen Sulphide Release and Retain Its Biological Properties in Hypoxia-like Environment. Antioxidants 2022, 11, 2092. https://doi.org/10.3390/antiox11112092
Sanchez-Aranguren L, Grubliauskiene M, Shokr H, Balakrishnan P, Wang K, Ahmad S, Marwah MK. Sodium Thiosulphate-Loaded Liposomes Control Hydrogen Sulphide Release and Retain Its Biological Properties in Hypoxia-like Environment. Antioxidants. 2022; 11(11):2092. https://doi.org/10.3390/antiox11112092
Chicago/Turabian StyleSanchez-Aranguren, Lissette, Milda Grubliauskiene, Hala Shokr, Pavanjeeth Balakrishnan, Keqing Wang, Shakil Ahmad, and Mandeep Kaur Marwah. 2022. "Sodium Thiosulphate-Loaded Liposomes Control Hydrogen Sulphide Release and Retain Its Biological Properties in Hypoxia-like Environment" Antioxidants 11, no. 11: 2092. https://doi.org/10.3390/antiox11112092
APA StyleSanchez-Aranguren, L., Grubliauskiene, M., Shokr, H., Balakrishnan, P., Wang, K., Ahmad, S., & Marwah, M. K. (2022). Sodium Thiosulphate-Loaded Liposomes Control Hydrogen Sulphide Release and Retain Its Biological Properties in Hypoxia-like Environment. Antioxidants, 11(11), 2092. https://doi.org/10.3390/antiox11112092