Suppression of NLRP3/Caspase-1/GSDMD Mediated Corneal Epithelium Pyroptosis Using Melatonin-Loaded Liposomes to Inhibit Benzalkonium Chloride-Induced Dry Eye Disease

References

• Merchel Piovesan Pereira B, Tagkopoulos I. Benzalkonium chlorides: Uses, regulatory status, and microbial resistance. Appl Environ Microbiol. 2019;85:e00377–19.
   PubMed Web of Science ®Google Scholar
• Ittoop SM, Seibold LK, Kahook MY. Ocular surface disease and the role of preservatives in glaucoma medications. In: Shaarawy TM, Sherwood MB, Hitchings RA, Crowston JG, editors. Glaucoma. 2nd ed. Philadelphia, PA: Elsevier, Saunders WB; 2015:593–597.
   Google Scholar
• Goldstein MH, Silva FQ, Blender N, Tran T, Vantipalli S. Ocular benzalkonium chloride exposure: Problems and solutions. Eye. 2022;36:361–368.
   PubMed Web of Science ®Google Scholar
• Zhang R, Park M, Richardson A, et al. Dose-dependent benzalkonium chloride toxicity imparts ocular surface epithelial changes with features of dry eye disease. Ocul Surf. 2020;18:158–169.
   PubMed Web of Science ®Google Scholar
• Schaumberg DA, Sullivan DA, Dana MR. Epidemiology of dry eye syndrome. Adv Exp Med Biol Biol. 2002;506:989–998.
   PubMed Web of Science ®Google Scholar
• Stapleton F, Alves M, Bunya VY, et al. TFOS DEWS II epidemiology report. Ocul Surf. 2017;15:334–365.
   PubMed Web of Science ®Google Scholar
• Tsubota K, Yokoi N, Shimazaki J, et al. New perspectives on dry eye definition and diagnosis: A consensus report by the Asia dry eye society. Ocul Surf. 2017;15:65–76.
   PubMed Web of Science ®Google Scholar
• Li S, Lu Z, Huang Y, et al. Anti-oxidative and anti-Inflammatory micelles: Break the dry eye vicious cycle. Adv Sci. 2022;9:e2200435.
   Web of Science ®Google Scholar
• Zheng Q, Ren Y, Reinach PS, et al. Reactive oxygen species activated NLRP3 inflammasomes prime environment-induced murine dry eye. Exp Eye Res. 2014;125:1–8.
   PubMed Web of Science ®Google Scholar
• Swanson KV, Deng M, Ting JPY. The NLRP3 inflammasome: molecular activation and regulation to therapeutics. Nat Rev Immunol. 2019;19:477–489.
   PubMed Web of Science ®Google Scholar
• Paik S, Kim JK, Silwal P, Sasakawa C, Jo EK. An update on the regulatory mechanisms of NLRP3 inflammasome activation. Cell Mol Immunol. 2021;18:1141–1160.
   PubMed Web of Science ®Google Scholar
• Tang TT, Lang XT, Xu CF, et al. CLICs-dependent chloride efflux is an essential and proximal upstream event for NLRP3 inflammasome activation. Nat Commun. 2017;8:202.
   PubMed Web of Science ®Google Scholar
• Domingo-Fernandez R, Coll RC, Kearney J, Breit S, O’Neill LAJ. The intracellular chloride channel proteins CLIC1 and CLIC4 induce IL-1 beta transcription and activate the NLRP3 inflammasome. J Biol Chem. 2017;292:12077–12087.
   PubMed Web of Science ®Google Scholar
• Zhang J, Dai Y, Yang Y, Xu J. Calcitriol alleviates hyperosmotic stress-induced corneal epithelial cell damage via inhibiting the NLRP3-ASC-Caspase-1-GSDMD pyroptosis pathway in dry eye disease. J Inflamm Res. 2021;14:2955–2962.
   PubMed Web of Science ®Google Scholar
• Evavold CL, Hafner-Bratkovic I, Devant P, et al. Control of gasdermin D oligomerization and pyroptosis by the Ragulator-Rag-mTORC1 pathway. Cell. 2021;184:4495–4511 e19.
   PubMed Web of Science ®Google Scholar
• Kayagaki N, Stowe IB, Lee BL, et al. Caspase-11 cleaves gasdermin D for non-canonical inflammasome signalling. Nature. 2015;526:666–671.
   PubMed Web of Science ®Google Scholar
• Tsai TY, Chen TC, Wang IJ, et al. The effect of resveratrol on protecting corneal epithelial cells from cytotoxicity caused by moxifloxacin and benzalkonium chloride. Invest. Ophth. Vis Sci. 2015;56:1575–1584.
   Google Scholar
• Reiter RJ, Mayo JC, Tan DX, Sainz RM, Alatorre-Jimenez M, Qin L. Melatonin as an antioxidant: Under promises but over delivers. J Pineal Res. 2016;61:253–278.
   PubMed Web of Science ®Google Scholar
• Manchester LC, Coto-Montes A, Boga JA, et al. Melatonin: An ancient molecule that makes oxygen metabolically tolerable. J Pineal Res. 2015;59:403–419.
   PubMed Web of Science ®Google Scholar
• Reiter RJ, Tan D, Mayo JC, Sainz RM, Leon J, Czarnocki Z. Melatonin as an antioxidant: Biochemical mechanisms and pathophysiological implications in humans. Acta Biochim Pol. 2003;50:1129–1146.
   PubMed Web of Science ®Google Scholar
• Reiter RJ, Rosales-Corral S, Tan DX, Jou MJ, Galano A, Xu B. Melatonin as a mitochondria-targeted antioxidant: One of evolution’s best ideas. Cell Mol Life Sci. 2017;74:3863–3881.
   PubMed Web of Science ®Google Scholar
• Jou MJ, Peng TI, Reiter RJ, Jou SB, Wu HY, Wen ST. Visualization of the antioxidative effects of melatonin at the mitochondrial level during oxidative stress-induced apoptosis of rat brain astrocytes. J Pineal Res. 2004;37:55–70.
   PubMed Web of Science ®Google Scholar
• Rastmanesh R. Potential of melatonin to treat or prevent age-related macular degeneration through stimulation of telomerase activity. Med Hypotheses. 2011;76:79–85.
   PubMed Web of Science ®Google Scholar
• Blasiak J, Reiter RJ, Kaarniranta K. Melatonin in retinal physiology and pathology: The case of age-related macular degeneration. Oxid Med Cell Longev. 2016;2016:6819736.
   PubMed Web of Science ®Google Scholar
• Wang B, Zuo X, Peng L, et al. Melatonin ameliorates oxidative stress-mediated injuries through induction of HO-1 and restores autophagic flux in dry eye. Exp Eye Res. 2021;205:108491.
   PubMed Web of Science ®Google Scholar
• Jin K, Ge Y, Ye Z, et al. Anti-oxidative and mucin-compensating dual-functional nano eye drops for synergistic treatment of dry eye disease. Appl Mater Today. 2022;27:101411.
   Web of Science ®Google Scholar
• Ashrafizadeh M, Najafi M, Kavyiani N, Mohammadinejad R, Farkhondeh T, Samarghandian S. Anti-inflammatory activity of melatonin: a focus on the role of NLRP3 inflammasome. Inflammation. 2021;44:1207–1222.
   PubMed Web of Science ®Google Scholar
• Che H, Li H, Li Y, et al. Melatonin exerts neuroprotective effects by inhibiting neuronal pyroptosis and autophagy in STZ-induced diabetic mice. FASEB J. 2020;34:14042–14054.
   PubMed Web of Science ®Google Scholar
• Liu QJ, Su LY, Sun CL, et al. Melatonin alleviates morphine analgesic tolerance in mice by decreasing NLRP3 inflammasome activation. Redox Biol. 2020;34:101560.
   PubMed Web of Science ®Google Scholar
• Rowe-Rendleman CL, Durazo SA, Kompella UB, et al. Drug and gene delivery to the back of the eye: from bench to bedside. Invest Ophthalmol Vis Sci. 2014;55:2714–2730.
   PubMed Web of Science ®Google Scholar
• Park CG, Kim YK, Kim MJ, et al. Mucoadhesive microparticles with a nanostructured surface for enhanced bioavailability of glaucoma drug. J Control Release. 2015;220:180–188.
   PubMed Web of Science ®Google Scholar
• Lin S, Ge C, Wang D, et al. Overcoming the anatomical and physiological barriers in topical eye surface medication using a peptide-decorated polymeric micelle. ACS Appl Mater Interf. 2019;11:39603–39612.
   PubMed Web of Science ®Google Scholar
• Zheng Q, Li L, Liu M, et al. In situ scavenging of mitochondrial ROS by antioxidative MitoQ/hyaluronic acid nanoparticles for environment-induced dry eye disease therapy. Chem Eng J. 2020;398:125621.
   Web of Science ®Google Scholar
• Nguyen D, Lai J. Synthesis, bioactive properties, and biomedical applications of intrinsically therapeutic nanoparticles for disease treatment. Chem Eng J. 2022;435:134970.
   Web of Science ®Google Scholar
• Assanhou A, Li W, Zhang L, et al. Reversal of multidrug resistance by co-delivery of paclitaxel and lonidamine using a TPGS and hyaluronic acid dual functionalized liposome for cancer treatment. Biomaterials. 2015;73:284–295.
   PubMed Web of Science ®Google Scholar
• Sang R, Stratton B, Engel A, Deng W. Liposome technologies towards colorectal cancer therapeutics. Acta Biomater. 2021;127:24–40.
   PubMed Web of Science ®Google Scholar
• Janagam DR, Wu L, Lowe TL. Nanoparticles for drug delivery to the anterior segment of the eye. Adv Drug Deliv Rev. 2017;122:31–64.
   PubMed Web of Science ®Google Scholar
• Zhang P. Monteiro da Silva G, Deatherage C, Burd C, DiMaio D. Cell-penetrating peptide mediates intracellular membrane passage of human papillomavirus L2 protein to trigger retrograde trafficking. Cell. 2018;174:1465–1476 e13.
   PubMed Web of Science ®Google Scholar
• Zou L, Peng Q, Wang P, Zhou B. Progress in research and application of HIV-1 TAT-derived cell-penetrating peptide. J Membr Biol. 2017;250::115–122.
   PubMed Web of Science ®Google Scholar
• Nguyen D, Luo L, Yang C, Lai J. Highly retina-permeating and long-acting resveratrol/metformin nanotherapeutics for enhanced treatment of macular degeneration. ACS Nano. 2023;17:168–183.
   PubMed Web of Science ®Google Scholar
• Yadavar-Nikravesh M-S, Ahmadi S, Milani A, et al. Construction and characterization of a novel Tenofovir-loaded PEGylated niosome conjugated with TAT peptide for evaluation of its cytotoxicity and anti-HIV effects. Adv Powder Technol. 2021;32:3161–3173.
   Web of Science ®Google Scholar
• Zhang H. Thin-film hydration followed by extrusion method for liposome preparation. Methods Mol Biol. 2017;1522:17–22.
   PubMedGoogle Scholar
• Jose J, Kanniyappan H, Muthuvijayan V. A novel, rapid and cost-effective method for separating drug-loaded liposomes prepared from egg yolk phospholipids. Process Biochem. 2022;115:80–91.
   Web of Science ®Google Scholar
• Yi H, Lu W, Liu F, et al. ROS-responsive liposomes with NIR light-triggered doxorubicin release for combinatorial therapy of breast cancer. J Nanobiotechnol. 2021;19:134.
   PubMed Web of Science ®Google Scholar
• Agarwal P, Huang D, Thakur SS, Rupenthal ID. Nanotechnology for ocular drug delivery. In: Grumezescu AM, editor. Design of Nanostructures for Versatile Therapeutic Applications. 2018:137–188.
   Google Scholar
• Lin Z, Liu X, Zhou T, et al. A mouse dry eye model induced by topical administration of benzalkonium chloride. Mol Vis. 2011;17:257–264.
   PubMed Web of Science ®Google Scholar
• Lin S, Gao W, Zhu C, et al. Efficiently suppress of ferroptosis using deferoxamine nanoparticles as a new method for retinal ganglion cell protection after traumatic optic neuropathy. Biomater Adv. 2022;138:212936.
   PubMedGoogle Scholar
• Huang B, Li X, Tu X, et al. OTX1 regulates cell cycle progression of neural progenitors in the developing cerebral cortex. J Biol Chem. 2018;293:2137–2148.
   PubMed Web of Science ®Google Scholar
• Wu B, Li M, Li K, et al. Cell penetrating peptide TAT-functionalized liposomes for efficient ophthalmic delivery of flurbiprofen: penetration and its underlying mechanism, retention, anti-inflammation and biocompatibility. Int J Pharm. 2021;598:120405.
   PubMedGoogle Scholar
• Yu C, Chen P, Xu J, et al. Corneal epithelium-derived netrin-1 alleviates dry eye disease via regulating dendritic cell activation. Invest Ophthalmol Vis Sci. 2022;63:1.
   PubMed Web of Science ®Google Scholar
• Swamynathan SK, Wells A. Conjunctival goblet cells: Ocular surface functions, disorders that affect them, and the potential for their regeneration. Ocul Surf. 2020;18:19–26.
   PubMed Web of Science ®Google Scholar
• Ock CY, Kim EH, Choi DJ, Lee HJ, Hahm KB, Chung MH. 8-Hydroxydeoxyguanosine: not mere biomarker for oxidative stress, but remedy for oxidative stress-implicated gastrointestinal diseases. World J Gastroenterol. 2012;18:302–308.
   PubMed Web of Science ®Google Scholar
• Zheng Q, Ren Y, Reinach PS, et al. Chen, Reactive oxygen species activated NLRP3 inflammasomes initiate inflammation in hyperosmolarity stressed human corneal epithelial cells and environment-induced dry eye patients. Exp Eye Res. 2015;134:133–140.
   PubMed Web of Science ®Google Scholar
• Zheng Q, Tan Q, Ren Y, et al. Hyperosmotic stress-induced TRPM2 channel activation stimulates NLRP3 inflammasome activity in primary human corneal epithelial cells. Invest Ophthalmol Vis Sci. 2018;59:3259–3268.
   PubMed Web of Science ®Google Scholar
• Li S, Sun Y, Song M, et al. NLRP3/caspase-1/GSDMD-mediated pyroptosis exerts a crucial role in astrocyte pathological injury in mouse model of depression. JCI Insight. 2021;6:e146852.
   PubMed Web of Science ®Google Scholar
• Lian H, Fang X, Li Q, et al. NLRP3 inflammasome-mediated pyroptosis pathway contributes to the pathogenesis of candida albicans keratitis. Front Med. 2022;9:845129.
   Web of Science ®Google Scholar
• Ibrahim MM, Maria DN, Mishra SR, Guragain D, Wang X, Jablonski MM. Once daily pregabalin eye drops for management of glaucoma. ACS Nano. 2019;13:13728–13744.
   PubMed Web of Science ®Google Scholar
• De Saint Jean M, Brignole F, Bringuier AF, Bauchet A, Feldmann G, Baudouin C. Effects of benzalkonium chloride on growth and survival of chang conjunctival cells. Invest Ophthalmol Vis Sci. 1999;40:619–630.
   PubMed Web of Science ®Google Scholar
• Noecker R. Effects of common ophthalmic preservatives on ocular health. Adv Ther. 2001;18:205–215.
   PubMed Web of Science ®Google Scholar
• Kanno S, Hirano S, Kato H, Fukuta M, Mukai T, Aoki Y. Benzalkonium chloride and cetylpyridinium chloride induce apoptosis in human lung epithelial cells and alter surface activity of pulmonary surfactant monolayers. Chem -Biol Interact. 2020;317:108962.
   PubMed Web of Science ®Google Scholar
• Green JP, Yu S, Martin-Sanchez F, et al. Chloride regulates dynamic NLRP3-dependent ASC oligomerization and inflammasome priming. Proc Natl Acad Sci USA. 2018;115:E9371–E9380.
   PubMed Web of Science ®Google Scholar
• Li S, Li H, Zhang YL, et al. SFTSV infection induces BAK/BAX-dependent mitochondrial DNA release to trigger NLRP3 inflammasome activation. Cell Rep. 2020;30:4370–4385 e7.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Jiao Y, Li X, et al. Pyroptosis: A new insight into eye disease therapy. Front Pharmacol. 2021;12:797110.
   PubMed Web of Science ®Google Scholar
• Chen H, Gan X, Li Y, et al. NLRP12- and NLRC4-mediated corneal epithelial pyroptosis is driven by GSDMD cleavage accompanied by IL-33 processing in dry eye. Ocul Surf. 2020;18:783–794.
   PubMed Web of Science ®Google Scholar
• Luo L, Nguyen D, Huang C, Lai J. Therapeutic hydrogel sheets programmed with multistage drug delivery for effective treatment of corneal abrasion. Chem Eng J. 2022;429:132409.
   Web of Science ®Google Scholar
• Luo L, Nguyen D, Lai J. Long-acting mucoadhesive thermogels for improving topical treatments of dry eye disease. Mater Sci Eng C Mater Biol Appl. 2020;115:111095.
   PubMed Web of Science ®Google Scholar
• Nguyen D, Luo L, Lai J. Thermogels containing sulfated hyaluronan as novel topical therapeutics for treatment of ocular surface inflammation. Mater Today Bio. 2022;13:100183.
   PubMedGoogle Scholar
• Lin P, Jian H, Li Y, et al. Alleviation of dry eye syndrome with one dose of antioxidant, anti-inflammatory, and mucoadhesive lysine-carbonized nanogels. Acta Biomater. 2022;141:140–150.
   PubMed Web of Science ®Google Scholar