Protective Effect of Allyl Isothiocyanate in an Experimentally Induced Rat Model for Dry Eye Syndrome

References

• Stapleton F, Alves M, Bunya VY, Jalbert I, Lekhanont K, Malet F, Na KS, Schaumberg D, Uchino M, Vehof J, et al. TFOS DEWS II epidemiology report. Ocul Surf. 2017;15(3):334–365.
   PubMed Web of Science ®Google Scholar
• Craig JP, Nichols KK, Akpek EK, Caffery B, Dua HS, Joo CK, Liu Z, Nelson JD, Nichols JJ, Tsubota K, et al. TFOS DEWS II definition and classification report. Ocul Surf. 2017;15(3):276–283.
   PubMed Web of Science ®Google Scholar
• Bron AJ, de Paiva CS, Chauhan SK, Bonini S, Gabison EE, Jain S, Knop E, Markoulli M, Ogawa Y, Perez V, Uchino Y, et al. TFOS DEWS II pathophysiology report. Ocul Surf. 2017;15(3):438–510.
   PubMed Web of Science ®Google Scholar
• Calonge M, Enriquez-de-Salamanca A, Diebold Y, Gonzalez-Garcia MJ, Reinoso R, Herreras JM, Corell A. Dry eye disease as an inflammatory disorder. Ocul Immunol Inflamm. 2010;18(4):244–253.
   PubMed Web of Science ®Google Scholar
• De Paiva CS, Corrales RM, Villarreal AL, Farley WJ, Li DQ, Stern ME, Pflugfelder SC. Corticosteroid and doxycycline suppress MMP-9 and inflammatory cytokine expression, MAPK activation in the corneal epithelium in experimental dry eye. Exp Eye Res. 2006;83(3):526–535.
   PubMed Web of Science ®Google Scholar
• Li DQ, Chen Z, Song XJ, Luo L, Pflugfelder SC. Stimulation of matrix metalloproteinases by hyperosmolarity via a JNK pathway in human corneal epithelial cells. Invest Ophthalmol Vis Sci. 2004;45(12):4302–4311.
   PubMed Web of Science ®Google Scholar
• Jones L, Downie LE, Korb D, Benitez-Del-Castillo JM, Dana R, Deng SX, Dong PN, Geerling G, Hida RY, Liu Y, et al. TFOS DEWS II management and therapy report. Ocul Surf. 2017;15(3):575–628.
   PubMed Web of Science ®Google Scholar
• Uematsu Y, Hirata K, Suzuki K, Iida K, Ueta T, Kamata K. [Determination of isothiocyanates and related compounds in mustard extract and horseradish extract used as natural food additives]. Shokuhin Eiseigaku Zasshi. 2002;43(1):10–17.
   PubMed Web of Science ®Google Scholar
• Caglayan B, Kilic E, Dalay A, Altunay S, Tuzcu M, Erten F, Orhan C, Gunal MY, Yulug B, Juturu V, et al. Allyl isothiocyanate attenuates oxidative stress and inflammation by modulating Nrf2/HO-1 and NF-κB pathways in traumatic brain injury in mice. Mol Biol Rep. 2019;46(1):241–250.
   PubMed Web of Science ®Google Scholar
• Jakubíková J, Sedlák J, Bod’o J, Bao Y. Effect of isothiocyanates on nuclear accumulation of NF-kappaB, Nrf2, and thioredoxin in caco-2 cells. J Agric Food Chem. 2006;54(5):1656–1662.
   PubMed Web of Science ®Google Scholar
• Batallé G, Cabarga L, Pol O. The inhibitory effects of slow-releasing hydrogen sulfide donors in the mechanical allodynia, grip strength deficits, and depressive-like behaviors associated with chronic osteoarthritis pain. Antioxidants (Basel). 2019;9(1):31.
   PubMedGoogle Scholar
• Danilov CA, Chandrasekaran K, Racz J, Soane L, Zielke C, Fiskum G. Sulforaphane protects astrocytes against oxidative stress and delayed death caused by oxygen and glucose deprivation. Glia. 2009;57(6):645–656.
   PubMed Web of Science ®Google Scholar
• Ernst IM, Wagner AE, Schuemann C, Storm N, Höppner W, Döring F, Stocker A, Rimbach G. Allyl-, butyl- and phenylethyl-isothiocyanate activate Nrf2 in cultured fibroblasts. Pharmacol Res. 2011;63(3):233–240.
   PubMed Web of Science ®Google Scholar
• Hasegawa K, Miwa S, Tsutsumiuchi K, Miwa J. Allyl isothiocyanate that induces GST and UGT expression confers oxidative stress resistance on C. elegans, as demonstrated by nematode biosensor. PLoS One. 2010;5(2):e9267.
   PubMed Web of Science ®Google Scholar
• Ping Z, Liu W, Kang Z, Cai J, Wang Q, Cheng N, Wang S, Wang S, Zhang JH, Sun X. Sulforaphane protects brains against hypoxic-ischemic injury through induction of Nrf2-dependent phase 2 enzyme. Brain Res. 2010;1343:178–185.
   PubMed Web of Science ®Google Scholar
• Xiang J, Alesi GN, Zhou N, Keep RF. Protective effects of isothiocyanates on blood-CSF barrier disruption induced by oxidative stress. Am J Physiol Regul Integr Comp Physiol. 2012;303(1):R1–7.
   PubMed Web of Science ®Google Scholar
• Muz OE, Orhan C, Erten F, Tuzcu M, Ozercan IH, Singh P, Morde A, Padigaru M, Rai D, Sahin K. A novel integrated active herbal formulation ameliorates dry eye syndrome by inhibiting inflammation and oxidative stress and enhancing glycosylated phosphoproteins in rats. Pharmaceuticals (Basel). 2020;13(10):295.
   PubMedGoogle Scholar
• Cohen J. Statistical power analysis for the behavioral sciences. New York: Routledge, 2013.
   Google Scholar
• Faul F, Erdfelder E, Lang A-G, Buchner A. G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods. 2007;39(2):175–191.
   PubMed Web of Science ®Google Scholar
• Guzmán M, Sabbione F, Gabelloni ML, Vanzulli S, Trevani AS, Giordano MN, Galletti JG. Restoring conjunctival tolerance by topical nuclear factor-κB inhibitors reduces preservative-facilitated allergic conjunctivitis in mice. Invest Ophthalmol Vis Sci. 2014;55(9):6116–6126.
   PubMed Web of Science ®Google Scholar
• Lin Z, Liu X, Zhou T, Wang Y, Bai L, He H, Liu Z. A mouse dry eye model induced by topical administration of benzalkonium chloride. Mol Vis. 2011;17:257–264.
   PubMed Web of Science ®Google Scholar
• Xiong C, Chen D, Liu J, Liu B, Li N, Zhou Y, Liang X, Ma P, Ye C, Ge J, et al. A rabbit dry eye model induced by topical medication of a preservative benzalkonium chloride. Invest Ophthalmol Vis Sci. 2008;49(5):1850–1856.
   PubMed Web of Science ®Google Scholar
• Baudouin C, Messmer EM, Aragona P, Geerling G, Akova YA, Benítez-del-Castillo J, Boboridis KG, Merayo-Lloves J, Rolando M, Labetoulle M. Revisiting the vicious circle of dry eye disease: a focus on the pathophysiology of meibomian gland dysfunction. Br J Ophthalmol. 2016;100(3):300–306.
   PubMed Web of Science ®Google Scholar
• Li CX, Gao JG, Wan XY, Chen Y, Xu CF, Feng ZM, Zeng H, Lin YM, Ma H, Xu P, et al. Allyl isothiocyanate ameliorates lipid accumulation and inflammation in nonalcoholic fatty liver disease via the Sirt1/AMPK and NF-κB signaling pathways. World J Gastroenterol. 2019;25(34):5120–5133.
   PubMed Web of Science ®Google Scholar
• Kim YJ, Lee DH, Ahn J, Chung WJ, Jang YJ, Seong KS, Moon JH, Ha TY, Jung CH. Pharmacokinetics, tissue distribution, and anti-lipogenic/adipogenic effects of allyl-isothiocyanate metabolites. PLoS One. 2015;10(8):e0132151.
   PubMed Web of Science ®Google Scholar
• Murata M, Yamashita N, Inoue S, Kawanishi S. Mechanism of oxidative DNA damage induced by carcinogenic allyl isothiocyanate. Free Radic Biol Med. 2000;28(5):797–805.
   PubMed Web of Science ®Google Scholar
• Agrawal R, Balne PK, Veerappan A, Au VB, Lee B, Loo E, Ghosh A, Tong L, Teoh SC, Connolly J, et al. A distinct cytokines profile in tear film of dry eye disease (DED) patients with HIV infection. Cytokine. 2016;88:77–84.
   PubMed Web of Science ®Google Scholar
• Dionne K, Redfern RL, Nichols JJ, Nichols KK. Analysis of tear inflammatory mediators: A comparison between the microarray and Luminex methods. Mol Vis. 2016;22:177–188.
   PubMed Web of Science ®Google Scholar
• Mrugacz M, Ostrowska L, Bryl A, Szulc A, Zelazowska-Rutkowska B, Mrugacz G. Pro-inflammatory cytokines associated with clinical severity of dry eye disease of patients with depression. Adv Med Sci. 2017;62(2):338–344.
   PubMed Web of Science ®Google Scholar
• Tong L, Wong TY, Cheng Y. Level of tear cytokines in population-level participants and correlation with clinical features. Cytokine. 2018;110:452–458.
   PubMed Web of Science ®Google Scholar
• VanDerMeid KR, Su SP, Ward KW, Zhang JZ. Correlation of tear inflammatory cytokines and matrix metalloproteinases with four dry eye diagnostic tests. Invest Ophthalmol Vis Sci. 2012;53(3):1512–1518.
   PubMed Web of Science ®Google Scholar
• Dogru M, Kojima T, Simsek C, Tsubota K. Potential role of oxidative stress in ocular surface inflammation and dry eye disease. Invest Ophthalmol Vis Sci. 2018;59(14):DES163–des8.
   PubMed Web of Science ®Google Scholar
• Baudouin C. The pathology of dry eye. Surv Ophthalmol. 2001;45(Suppl 2):S211–S20.
   PubMed Web of Science ®Google Scholar
• Argüeso P, Gipson IK. Epithelial mucins of the ocular surface: structure, biosynthesis and function. Exp Eye Res. 2001;73(3):281–289.
   PubMed Web of Science ®Google Scholar
• Cascio S, Zhang L, Finn OJ. MUC1 protein expression in tumor cells regulates transcription of proinflammatory cytokines by forming a complex with nuclear factor-κB p65 and binding to cytokine promoters: importance of extracellular domain. J Biol Chem. 2011;286(49):42248–42256.
   PubMed Web of Science ®Google Scholar
• Singh PK, Hollingsworth MA. Cell surface-associated mucins in signal transduction. Trends Cell Biol. 2006;16(9):467–476.
   PubMed Web of Science ®Google Scholar
• Danjo Y, Watanabe H, Tisdale AS, George M, Tsumura T, Abelson MB, Gipson IK. Alteration of mucin in human conjunctival epithelia in dry eye. Invest Ophthalmol Vis Sci. 1998;39(13):2602–2609.
   PubMed Web of Science ®Google Scholar
• Benowitz LI, Routtenberg A. GAP-43: an intrinsic determinant of neuronal development and plasticity. Trends Neurosci. 1997;20(2):84–91.
   PubMed Web of Science ®Google Scholar
• Chaudhary S, Namavari A, Yco L, Chang JH, Sonawane S, Khanolkar V, Sarkar J, Jain S. Neurotrophins and nerve regeneration-associated genes are expressed in the cornea after lamellar flap surgery. Cornea. 2012;31(12):1460–1467.
   PubMed Web of Science ®Google Scholar
• Martin RE, Bazan NG. Growth-associated protein GAP-43 and nerve cell adhesion molecule in sensory nerves of cornea. Exp Eye Res. 1992;55(2):307–314.
   PubMed Web of Science ®Google Scholar
• Uchida S, Yokoo S, Yanagi Y, Usui T, Yokota C, Mimura T, Araie M, Yamagami S, Amano S. Sphere formation and expression of neural proteins by human corneal stromal cells in vitro. Invest Ophthalmol Vis Sci. 2005;46(5):1620–1625.
   PubMed Web of Science ®Google Scholar
• Zhao G, Chen H, Song Z, Yin H, Xu Y, Chen M. Glial fibrillary acidic protein expression during HSV-1 infection in mouse cornea. APMIS. 2014;122(2):128–135.
   PubMed Web of Science ®Google Scholar
• Heiss E, Herhaus C, Klimo K, Bartsch H, Gerhäuser C. Nuclear factor kappa B is a molecular target for sulforaphane-mediated anti-inflammatory mechanisms. J Biol Chem. 2001;276(34):32008–32015.
   PubMed Web of Science ®Google Scholar
• Ritz SA, Wan J, Diaz-Sanchez D. Sulforaphane-stimulated phase II enzyme induction inhibits cytokine production by airway epithelial cells stimulated with diesel extract. Am J Physiol Lung Cell Mol Physiol. 2007;292(1):L33–39.
   PubMed Web of Science ®Google Scholar
• Talalay P, Fahey JW, Healy ZR, Wehage SL, Benedict AL, Min C, Dinkova-Kostova AT. Sulforaphane mobilizes cellular defenses that protect skin against damage by UV radiation. Proc Natl Acad Sci U S A. 2007;104(44):17500–17505.
   PubMed Web of Science ®Google Scholar
• Woo KJ, Kwon TK. Sulforaphane suppresses lipopolysaccharide-induced cyclooxygenase-2 (COX-2) expression through the modulation of multiple targets in COX-2 gene promoter. Int Immunopharmacol. 2007;7(13):1776–1783.
   PubMed Web of Science ®Google Scholar
• Wu L, Noyan Ashraf MH, Facci M, Wang R, Paterson PG, Ferrie A, Juurlink BH. Dietary approach to attenuate oxidative stress, hypertension, and inflammation in the cardiovascular system. Proc Natl Acad Sci U S A. 2004;101(18):7094–7099.
   PubMed Web of Science ®Google Scholar
• Koo JE, Park ZY, Kim ND, Lee JY. Sulforaphane inhibits the engagement of LPS with TLR4/MD2 complex by preferential binding to Cys133 in MD2. Biochem Biophys Res Commun. 2013;434(3):600–605.
   PubMed Web of Science ®Google Scholar
• Youn HS, Kim YS, Park ZY, Kim SY, Choi NY, Joung SM, Seo JA, Lim KM, Kwak MK, Hwang DH, Lee JY. Sulforaphane suppresses oligomerization of TLR4 in a thiol-dependent manner. J Immunol. 2010;184(1):411–419.
   PubMed Web of Science ®Google Scholar
• Yang G, Lee HE, Lee JY. A pharmacological inhibitor of NLRP3 inflammasome prevents non-alcoholic fatty liver disease in a mouse model induced by high fat diet. Sci Rep. 2016;6:24399.
   PubMed Web of Science ®Google Scholar
• Wagner AE, Boesch-Saadatmandi C, Dose J, Schultheiss G, Rimbach G. Anti-inflammatory potential of allyl-isothiocyanate-role of Nrf2, NF-(κ) B and microRNA-155. J Cell Mol Med. 2012;16(4):836–843.
   PubMed Web of Science ®Google Scholar
• Wagner AE, Ernst I, Iori R, Desel C, Rimbach G. Sulforaphane but not ascorbigen, indole-3-carbinole and ascorbic acid activates the transcription factor Nrf2 and induces phase-2 and antioxidant enzymes in human keratinocytes in culture. Exp Dermatol. 2010;19(2):137–144.
   PubMed Web of Science ®Google Scholar
• Brone B, Peeters PJ, Marrannes R, Mercken M, Nuydens R, Meert T, Gijsen HJ. Tear gasses CN, CR, and CS are potent activators of the human TRPA1 receptor. Toxicol Appl Pharmacol. 2008;231(2):150–156.
   PubMed Web of Science ®Google Scholar
• Everaerts W, Gees M, Alpizar YA, Farre R, Leten C, Apetrei A, Dewachter I, van Leuven F, Vennekens R, De Ridder D, et al. The capsaicin receptor TRPV1 is a crucial mediator of the noxious effects of mustard oil. Curr Biol. 2011;21(4):316–321.
   PubMed Web of Science ®Google Scholar
• Canner JP, Linsenmayer TF, Kubilus JK. Developmental regulation of trigeminal TRPA1 by the cornea. Invest Ophthalmol Vis Sci. 2014;56(1):29–36.
   PubMed Web of Science ®Google Scholar
• Mergler S, Valtink M, Takayoshi S, Okada Y, Miyajima M, Saika S, Reinach PS. Temperature-sensitive transient receptor potential channels in corneal tissue layers and cells. Ophthalmic Res. 2014;52(3):151–159.
   PubMed Web of Science ®Google Scholar
• Okada Y, Reinach PS, Shirai K, Kitano A, Miyajima M, Saika S. Trpa1 gene ablation in mice improves corneal wound healing response to injury. Invest Ophthalmol Vis Sci. 2010;51:2496–2496.
   PubMed Web of Science ®Google Scholar
• Okada Y, Reinach PS, Shirai K, Kitano-Izutani A, Miyajima M, Yamanaka O, Sumioka T, Saika S. Transient receptor potential channels and corneal stromal inflammation. Cornea. 2015;34(Suppl 11):S136–S141.
   PubMed Web of Science ®Google Scholar