Effects of extracts from goji berry (Lycium barbarum), green tea (Camellia sinensis), and persimmon (Diospyros kaki) leaves in a dry eye model of mice
Article Sidebar
Main Article Content
Abstract
This study aimed to investigate the effects of goji berry (Lycium barbarum) [GB], green tea (Camellia sinensis) [GT], and persimmon (Diospyros kaki) [DK] leaf extracts in a mouse dry eye (DE) model. Fifty-six eyes from 28 female BALB/c mice were equally divided into the following groups: control, GB, GT, and DK (left eye groups); DE, DE + GB, DE + GT, DE + DK (right eye groups). The DE model was induced in right eye groups by topical administration of 5 µL of 0.2 % benzalkonium chloride twice daily for 14 days. A 1 % extract solution of GB, GT, and DK was instilled in the DE + GB, DE + GT, and DE + DK groups between days 15 and 30, respectively. In the DE group, only 0.9 % NaCl was instilled during this period. All groups were evaluated for aqueous tear production rate, corneal fluorescein staining, and tear break-up time (TBUT). Histopathological and Western blot analyses performed after euthanasia. On day 15, aqueous tear production decreased, corneal fluorescein staining scores increased, and TBUT was shortened in right eye groups compared to left eye groups (P < 0.05). At the end of the study, no significant differences were observed among the extract-treated DE groups regarding clinical parameters (P > 0.05). However, based on histopathological and molecular analyses, the GT group demonstrated the most beneficial effect without side effects (P < 0.05). These results suggest that 0.1 % GT leaf extract may be a potential therapeutic agent for DE.
Article Details
References
Barabino S, Benítez-Del-Castillo JM. Dry eye disease pathogenesis and clinical signs: searching for correspondence in the clinical practice. European Review for Medical and Pharmacological Sciences. 2024;28(5):1881−1890. doi: 10.26355/eurrev_202403_35602.
Zhang Z, Yang WZ, Zhu ZZ, Hu QQ, Chen YF, He H, et al. Therapeutic effects of topical doxycycline in a benzalkonium chloride-induced mouse dry eye model. Investigative Ophthalmology and Visual Science. 2014;55(5):2963−2974. doi: 10.1167/iovs.13-13577.
Memarzadeh E, Luther T, Heidari-Soureshjani S. Effect and mechanisms of medicinal plants on dry eye disease: a systematic review. Journal of Clinical and Diagnostic Research. 2018;12(9):1−4. doi: 10.7860/JCDR/2018/36409.12042.
Kojima T, Dogru M, Kawashima M, Nakamura S, Tsubota K. Advances in the diagnosis and treatment of dry eye. Progress in Retinal and Eye Research. 2020;78:100842. doi: 10.1016/j.preteyeres.2020.100842.
Potterat O. Goji (Lycium barbarum and L. chinense): phytochemistry, pharmacology and safety in the perspective of traditional uses and recent popularity. Planta Medica. 2010; 76(1):7−19. doi: 10.1055/s-0029-1186218.
Chan HC, Chang RC, Koon-Ching A, Chiu K, Yuen WH, Zee SY, et al. Neuroprotective effects of Lycium barbarum Lynn on protecting retinal ganglion cells in an ocular hypertension model of glaucoma. Experimental Neurology. 2007;203(1):269−273. doi: 10.1016/j.expneurol.2006.05.031.
Bucheli P, Vidal K, Shen L, Gu Z, Zhang C, Miller LE, et al. Goji berry effects on macular characteristics and plasma antioxidant levels. Optometry and Vision Science. 2011;88(2):257−262. doi: 10.1097/OPX.0b013e318205a18f.
Masmali AM, Alanazi SA, Alotaibi AG, Fagehi R, Abusharaha A, El-Hiti GA. The acute effect of a single dose of green tea on the quality and quantity of tears in normal eye subjects. Clinical Ophthalmology. 2019;13:605−610. doi: 10.2147/OPTH.S201127.
Yoneyama S, Kawai K, Tsuno NH, Okaji Y, Asakage M, Tsuchiya T, et al. Epigallocatechin gallate affects human dendritic cell differentiation and maturation. Journal of Allergy and Clinical Immunology. 2008;121(1): 209−214. doi: 10.1016/j.jaci.2007.08.026.
Nejabat M, Reza SA, Zadmehr M, Yasemi M, Sobhani Z. Efficacy of green tea extract for treatment of dry eye and meibomian gland dysfunction; a double-blind randomized controlled clinical trial study. Journal of Clinical and Diagnostic Research. 2017;11(2):5−8. doi: 10.7860/JCDR/2017/23336.9426.
Lee HS, Chauhan SK, Okanobo A, Nallasamy N, Dana R. Therapeutic efficacy of topical epigallocatechin gallate in murine dry eye. Cornea. 2011; 30(12):1465−1840. doi: 10.1097/ICO.0b013e31821c9b5a.
Xie C, Xie Z, Xu X, Yang D. Persimmon (Diospyros kaki L.) leaves: a review on traditional uses, phytochemistry and pharmacological properties. Journal of Ethnopharmacology. 2015;163:229−240. doi: 10.1016/j.jep.2015.01.007.
Rauf A, Uddin G, Patel S, Khan A, Halim SA, Bawazeer S, et al. Diospyros, an under-utilized, multi-purpose plant genus: a review. Biomedicine and Pharmacotherapy. 2017;91:714−730. doi: 10.1016/j.biopha.2017.05.012.
Kim KA, Hyun LC, Jung SH, Jang SJ. The leaves of Diospyros kaki exert beneficial effects on a benzalkonium chloride-induced murine dry eye model. Molecular Vision. 2016;22:284−293. PMCID: PMC4818957.
Kim KA, Kang SW, Ahn HR, Song Y, Yang SJ, Jung SH. Leaves of persimmon (Diospyros kaki Thunb.) ameliorate N-methyl-N-nitrosourea (MNU)-induced retinal degeneration in Mice. Journal of Agricultural and Food Chemistry. 2015; 63(35):7750–7759. doi: 10.1021/acs.jafc.5b02578.
Kulualp K, Kiliç S, Eröksüz Y, Eröksüz H, Aslan A. Therapeutic effect of bovine amniotic fluid in murine dry eye model. Japanese Journal of Veterinary Research. 2020;68(3):171−186. doi: 10.14943/jjvr.68.3.171.
Lin Z, Liu X, Zhou T, Wang Y, Bai L, He H, et al. A mouse dry eye model induced by topical administration of benzalkonium chloride. Molecular Vision. 2011;17:257−264. PMCID: PMC3030605.
Kulualp K. Farelerde deneysel kuru göz modeli üzerine farklı terapötik ajanların etkilerinin karşılaştırılması [PHD thesis dissertation]. Türkiye: Fırat Üniversitesi, Sağlık Bilimleri Enstitüsü; 2011.
Aslan A, Gok O, Erman O, Kuloglu T. Ellagic acid impedes carbontetrachloride-induced liver damage in rats through suppression of NF-kB, Bcl-2 and regulating Nrf-2 and caspase pathway. Biomedicine and Pharmacotherapy. 2018;105:662−669. doi: 10.1016/j.biopha.2018.06.020.
Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227(5259):680−685. doi: 10.1038/227680a0.
Baudouin C, Rolando M, Benítez Del Castillo JM, Messmer EM, Figueiredo FC, Irkec M, et al. Reconsidering the central role of mucins in dry eye and ocular surface diseases. Progress in Retinal and Eye Research. 2019;71:68−87. doi: 10.1016/j.preteyeres.2018.11.007.
Suárez-Cortés T, Merino-Inda N, Benitez-del Castillo JM. Tear and ocular surface disease biomarkers: A diagnostic and clinical perspective for ocular allergies and dry eye disease. Experimental Eye Research. 2022;221:109121. doi: 10.1016/j.exer.2022.109121.
Stern ME, Gao J, Siemasko KF, Beuerman RW, Pflugfelder SC. The role of the lacrimal functional unit in the pathophysiology of dry eye. Experimental Eye Research. 2004;78(3):409−416. doi: 10.1016/j.exer.2003.09.003.
Huang W, Tourmouzis K, Perry H, Honkanen RA, Rigas B. Animal models of dry eye disease: useful, varied and evolving (Review). Experimental and Therapeutic Medicine. 2021;22(6):1394. doi: 10.3892/etm.2021.10830.
Mu N, Wang H, Chen D, Wang F, Ji L, Zhang C, Li M, Lu P. A novel rat model of dry eye induced by aerosol exposure of particulate matter. Investigative Ophthalmology and Visual Science. 2022;63(1):39. doi: 10.1167/iovs.63.1.39.
Singh S, Sharma S, Basu S. Rabbit models of dry eye disease: current understanding and unmet needs for translational research. Experimental Eye Research. 2021;206:108538. doi: 10.1016/j.exer.2021.108538.
Qin Y, Zhang Y, Liang Q, Xu X, Li Q, Pan Z, et al. Labial salivary gland transplantation for severe dry eye in a rhesus monkey model. Investigative Ophthalmology and Visual Science. 2018;59(6):2478−2486. doi: 10.1167/iovs.18-23966.
Lin N, Chen X, Liu H, Gao N, Liu Z, Li J, et al. Ectoine enhances mucin production via restoring IL-13/IFN-γ balance in a murine dry eye model. Investigative Ophthalmology and Visual Science. 2024; 65(6):39. doi: 10.1167/iovs.65.6.39.
Carpena-Torres C, Pintor J, Huete-Toral F, Martin-Gil A, Rodríguez-Pomar C, Martínez-Águila A, et al. Efficacy of artificial tears based on an extract of Artemia salina containing dinucleotides in a rabbit dry eye model. International Journal of Molecular Sciences. 2021; 22(21):11999. doi: 10.3390/ijms222111999.
Sánchez‐Ríos A, Correa‐Gallegos EY, Medina‐Espinoza JM, Navarro‐Sanchez AA, Olvera‐Montaño O, Baiza‐Durán L, Muñoz‐Villegas P. Validation of a preclinical dry eye model in New Zealand white rabbits during and following topical instillation of 1 % ophthalmic atropine sulfate. Animal Models and Experimental Medicine. 2022;5(3):266−273. doi: 10.1002/ame2.12218.
Kilic S, Kulualp K. Efficacy of several therapeutic agents in a murine model of dry eye syndrome. Comparative Medicine. 2016;66(2):112−118. PMCID: PMC4825960.
Thacker M, Sahoo A, Reddy AA, Bokara KK, Singh S, Basu S, et al. Benzalkonium chloride-induced dry eye disease animal models: current understanding and potential for translational research. Indian Journal of Ophthalmology. 2023;71(4):1256−1262. doi: 10.4103/IJO.IJO_2791_22.
Xue YL, Miyakawa T, Hayashi Y, Okatomo K, Hu F, Mitani N, et al. Isolation and tyrosinase inhibitory effects of polyphenols from the leaves of persimmon, Diospyros kaki. Journal of Agricultural and Food Chemistry. 2011;59(11): 6011−6017. doi: 10.1021/jf200940h.
Yoon KC, Ahn KY, Choi W, Li Z, Choi JS, Lee SH, et al. Tear production and ocular surface changes in experimental dry eye after elimination of desiccating stress. Investigative Ophthalmology and Visual Science. 2011;52(10):7267−7273. doi: 10.1167/iovs.11-7231.
Datta S, Baudouin C, Brignole-Baudouin F, Denoyer A, Cortopassi GA. The eye drop preservative benzalkonium chloride potently induces mitochondrial dysfunction and preferentially affects LHON mutant cells. Investigative Ophthalmology and Visual Science. 2017;58(4):2406−2412. doi: 10.1167/iovs.16-20903.
Yang Q, Zhang Y, Liu X, Wang N, Song Z, Wu K. A Comparison of the effects of benzalkonium chloride on ocular surfaces between C57BL/6 and BALB/c mice. International. Journal of Molecular Sciences. 2017;18(3):509. doi: 10.3390/ijms18030509.
Baudouin C, Denoyer A, Desbenoit N, Hamm G, Grise A. In vitro and in vivo experimental studies on trabecular meshwork degeneration induced by benzalkonium chloride (an American Ophthalmological Society thesis). Transactions of the American Ophthalmological Society. 2012;110:40–63. PMCID: PMC3671366.
Kwon YS, Park JS, Yun SH, Ku SK, Jang KH. A dog dry eye model induced by benzalkonium chloride. Investigative Ophthalmology and Visual Science. 2011;52(14):3765.
Kang SW, Kim KA, Lee CH, Yang SJ, Kang TK, Jung JH, et al. A standardized extract of Rhynchosia volubilis Lour. exerts a protective effect on benzalkonium chloride-induced mouse dry eye model. Journal of Ethnopharmacology. 2018; 215:91−100. doi: 10.1016/j.jep.2017.12.041.
Lima L, Lange RR, Turner-Giannico A, Montiani-Ferreira F. Evaluation of standardized endodontic paper point tear test in New Zealand white rabbits and comparison between corneal sensitivity followed tear tests. Veterinary Ophthalmology. 2015; 18(Suppl 1):119–124. doi: 10.1111/vop.12178.
Kim KA, Yang SJ, Kim TJ, Kang SW, Jung SH. Anti-inflammatory effects of Diospyros kaki in mouse dry eye model. Investigative Ophthalmology and Visual Science. 2016;57(12):408.
Chester T, Garg S, Johnston J, Ayers B, Gupta P. How can we best diagnose severity levels of dry eye disease: current perspectives. Clinical Ophthalmology. 2023;17:1587−1604. doi: 10.2147/OPTH.S388289.
Lee C, Kim KA, Yang S, Jung S. Protective effect of persimmon leaves (Diospyros kaki) on dry eye in an exorbital lacrimal gland excision model of mice. Investigative Ophthalmology and Visual Science. 2017;58(8):2252.
Chien KJ, Horng CT, Huang YS, Hsieh YH, Wang CJ, Yang JS, et al. Effects of Lycium barbarum (goji berry) on dry eye disease in rats. Molecular Medicine Reports. 2018;17(1):809−818. doi: 10.3892/mmr.2017.7947.
Yang C, Gao Q, Liu J, Wu Y, Hou X, Sun L, et al. M2 macrophage-derived extracellular vesicles ameliorate Benzalkonium Chloride-induced dry eye. Experimental Eye Research. 2024;247:110041. doi: 10.1016/j.exer.2024.110041.
Kim YH, Jung JC, Jung SY, Yu S, Lee KW, Park YJ. Comparison of the efficacy of fluorometholone with and without benzalkonium chloride in ocular surface disease. Cornea. 2016;35(2): 234−242. doi: 10.1097/ICO.0000000000000695.
Shanmugham V, Subban R. Capsanthin from Capsicum annum fruits exerts anti‐glaucoma, antioxidant, anti‐inflammatory activity, and corneal pro‐inflammatory cytokine gene expression in a benzalkonium chloride‐induced rat dry eye model. Journal of Food Biochemistry. 2022;46(10):e14352. doi: 10.1111/jfbc.14352.
Bates N, Edwards N. Benzalkonium chloride exposure in cats: a retrospective analysis of 245 cases reported to the Veterinary Poisons Information Service (VPIS). Veterinary Record. 2015;176(9): 229. doi: 10.1136/vr.102653.
Chen TY, Tseng CL, Lin CA, Lin HY, Venkatesan P, Lai PS. Effects of eye drops containing hyaluronic acid-nimesulide conjugates in a benzalkonium chloride-induced experimental dry eye rabbit model. Pharmaceutics. 2021;13(9):1366. doi: 10.3390/pharmaceutics13091366.
Yang SJ, Jo H, Kim KA, Ahn HR, Kang SW, Jung SH. Diospyros kaki extract inhibits alkali burn-induced corneal neovascularization. Journal of Medicinal Food. 2016;19(1):106−109. doi: 10.1089/jmf.2014.3404.
Lee HS, Jun JH, Jung EH, Koo BA, Kim YS. Epigalloccatechin-3-gallate inhibits ocular neovascularization and vascular permeability in human retinal pigment epithelial and human retinal microvascular endothelial cells via suppression of MMP-9 and VEGF activation. Molecules. 2014;19(8):12150-12172. doi: 10.3390/molecules190812150.
Li ZZ, Zou YP, Zhu H, Zeng WZ, Ding Y, Su JZ, et al. Establishment of a Beagle dog model of dry eye disease. Translational Vision Science and Technology. 2023; 12(1):2. doi: 10.1167/tvst.12.1.2.
Kundu G, Shetty R, D'Souza S, Gorimanipalli B, Koul A, Sethu S. Effect of maqui-berry extract in dry eye disease- A clinical and molecular analysis. Indian Journal of Ophthalmology. 2023;71(4):1613−1618. doi: 10.4103/IJO.IJO_2909_22.
Lan W, Petznick A, Heryati S, Rifada M, Tong L. Nuclear factor-κB: central regulator in ocular surface inflammation and diseases. The Ocular Surface. 2012;10(3):137−148. doi: 10.1016/j.jtos.2012.04.001.
Galletti JG, Gabelloni ML, Morande PE, Sabbione F, Vermeulen ME, Trevani AS, et al. Benzalkonium chloride breaks down conjunctival immunological tolerance in a murine model. Mucosal Immunology. 2013;6(1):24−34. doi: 10.1038/mi.2012.44.
Liu XF, Zhou DD, Xie T, Malik TH, Lu CB, Li HJ, et al. Nrf2, a potential therapeutic target against oxidative stress in corneal diseases. Oxidative Medicine and Cellular Longevity. 2017;2017:2326178. doi: 10.1155/2017/2326178.
Ahmed SMU, Luo L, Namani A, Wang XJ, Tang X. Nrf2 signaling pathway: Pivotal roles in inflammation. Biochimica et Biophysica Acta: Molecular Basis of Disease. 2017;1863(2):585−597. doi: 10.1016/j.bbadis.2016.11.005.
Cavet ME, Harrington KL, Vollmer TR, Ward KW, Zhang JZ. Anti-inflammatory and oxidative effects of the green tea polyphenol epigallocatechin gallate in human corneal epithelial cells. Molecular Vision. 2011;17:533−542. PMCID: PMC3044696.
Yang CC, Chien JY, Chou YY, Ciou JW, Huang SP. The effects of Lycium chinense, Cuscuta chinensis, Senna tora, Ophiopogon japonicus, and Dendrobium nobile decoction on a dry eye mouse model. Medicina (Kaunas). 2022;58(8):1134. doi: 10.3390/medicina58081134.
Qin D, Deng Y, Wang L, Yin H. Therapeutic effects of topical application of Lycium barbarum polysaccharide in a murine model of dry eye. Frontiers in Medicine. 2022;9:827594. doi: 10.3389/fmed.2022.827594.
License
Veterinaria México OA by Facultad de Medicina Veterinaria y Zootecnia - Universidad Nacional Autónoma de México is licensed under a Creative Commons Attribution 4.0 International Licence.
Based on a work at http://www.revistas.unam.mx
- All articles in Veterinaria México OA re published under the Creative Commons Attribution 4.0 Unported (CC-BY 4.0). With this license, authors retain copyright but allow any user to share, copy, distribute, transmit, adapt and make commercial use of the work, without needing to provide additional permission as long as appropriate attribution is made to the original author or source.
- By using this license, all Veterinaria México OAarticles meet or exceed all funder and institutional requirements for being considered Open Access.
- Authors cannot use copyrighted material within their article unless that material has also been made available under a similarly liberal license.