The Carbonic Anhydrase Inhibitor Dorzolamide Stimulates the Differentiation of Human Meibomian Gland Epithelial Cells

References

• Green-Church KB, Butovich I, Willcox M, Borchman D, Paulsen F, Barabino S, Glasgow BJ. The international workshop on meibomian gland dysfunction: report of the subcommittee on tear film lipids and lipid-protein interactions in health and disease. Invest Ophthalmol Vis Sci. 2011;52:1979–93.
   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, et al. TFOS DEWS II pathophysiology report. Ocul Surf. 2017;15(3):438–510. doi:10.1016/j.jtos.2017.05.011.
   PubMed Web of Science ®Google Scholar
• Knop E, Knop N, Millar T, Obata H, Sullivan DA. The international workshop on meibomian gland dysfunction: report of the subcommittee on anatomy, physiology, and pathophysiology of the meibomian gland. Invest Ophthalmol Vis Sci. 2011;52(4):1938–78. doi:10.1167/iovs.10-6997c.
   PubMed Web of Science ®Google Scholar
• Lemp MA, Crews LA, Bron AJ, Foulks GN, Sullivan BD. Distribution of aqueous-deficient and evaporative dry eye in a clinic-based patient cohort: A retrospective study. Cornea. 2012;31(5):472–78. doi:10.1097/ICO.0b013e318225415a.
   PubMed Web of Science ®Google Scholar
• Arita R, Itoh K, Maeda S, Maeda K, Furuta A, Tomidokoro A, Aihara M, Amano S. Comparison of the long-term effects of various topical antiglaucoma medications on meibomian glands. Cornea. 2012;31(11):1229–34. doi:10.1097/ICO.0b013e31823f8e7d.
   PubMed Web of Science ®Google Scholar
• Agnifili L, Fasanella V, Costagliola C, Ciabattoni C, Mastropasqua R, Frezzotti P, Mastropasqua L. In vivo confocal microscopy of meibomian glands in glaucoma. Br J Ophthalmol. 2013;97(3):343–49. doi:10.1136/bjophthalmol-2012-302597.
   PubMed Web of Science ®Google Scholar
• Uzunosmanoglu E, Mocan MC, Kocabeyoglu S, Karakaya J, Irkec M. Meibomian gland dysfunction in patients receiving long-term glaucoma medications. Cornea. 2016;35(8):1112–16. doi:10.1097/ICO.0000000000000838.
   PubMed Web of Science ®Google Scholar
• Arita R, Itoh K, Maeda S, Maeda K, Furuta A, Tomidokoro A, Aihara M, Amano S. Effects of long-term topical anti-glaucoma medications on meibomian glands. Graefes Arch Clin Exp Ophthalmol. 2012;250(8):1181–85. doi:10.1007/s00417-012-1943-6.
   PubMed Web of Science ®Google Scholar
• Fraunfelder FT, Sciubba JJ, Mathers WD. The role of medications in causing dry eye. J Ophthalmol. 2012;2012:285851. doi:10.1155/2012/285851.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Kam WR, Liu Y, Chen X, Sullivan DA. Influence of pilocarpine and timolol on human meibomian gland epithelial cells. Cornea. 2017;36(6):719–24. doi:10.1097/ICO.0000000000001181.
   PubMed Web of Science ®Google Scholar
• Chen X, Sullivan DA, Sullivan AG, Kam WR, Liu Y. Toxicity of cosmetic preservatives on human ocular surface and adnexal cells. Exp Eye Res. 2018;170:188–97. doi:10.1016/j.exer.2018.02.020.
   PubMed Web of Science ®Google Scholar
• Kam WR, Liu Y, Ding J, Sullivan DA. Do cyclosporine A, an IL-1 receptor antagonist, uridine triphosphate, rebamipide, and/or bimatoprost regulate human meibomian gland epithelial cells? Invest Ophthalmol Vis Sci. 2016;57(10):4287–94. doi:10.1167/iovs.16-19937.
   PubMed Web of Science ®Google Scholar
• Song G, Ouyang G, Bao S. The activation of AKT/PKB signaling pathway and cell survival. J Cell Mol Med. 2005;9(1):59–71. doi:10.1111/j.1582-4934.2005.tb00337.x.
   PubMed Web of Science ®Google Scholar
• Liu S, Hatton MP, Khandelwal P, Sullivan DA. Culture, immortalization, and characterization of human meibomian gland epithelial cells. Invest Ophthalmol Vis Sci. 2010;51(8):3993–4005. doi:10.1167/iovs.09-5108.
   PubMed Web of Science ®Google Scholar
• Sullivan DA, Liu Y, Kam WR, Ding J, Green KM, Shaffer SA, Hatton MP, Liu S. Serum-induced differentiation of human meibomian gland epithelial cells. Invest Ophthalmol Vis Sci. 2014;55(6):3866–77. doi:10.1167/iovs.13-13407.
   PubMed Web of Science ®Google Scholar
• Liu S, Kam WR, Ding J, Hatton MP, Sullivan DA. Effect of growth factors on the proliferation and gene expression of human meibomian gland epithelial cells. Invest Ophthalmol Vis Sci. 2013;54(4):2541–50. doi:10.1167/iovs.12-11221.
   PubMed Web of Science ®Google Scholar
• Liu Y, Kam WR, Ding J, Sullivan DA. Effect of azithromycin on lipid accumulation in immortalized human meibomian gland epithelial cells. JAMA Ophthalmol. 2014;132(2):226–28. doi:10.1001/jamaophthalmol.2013.6030.
   PubMed Web of Science ®Google Scholar
• Kadam RS, Jadhav G, Ogidigben M, Kompella UB. Ocular pharmacokinetics of dorzolamide and brinzolamide after single and multiple topical dosing: implications for effects on ocular blood flow. Drug Metab Dispos. 2011;39(9):1529–37. doi:10.1124/dmd.111.040055.
   PubMed Web of Science ®Google Scholar
• Ding J, Sullivan DA. The effects of insulin-like growth factor 1 and growth hormone on human meibomian gland epithelial cells. JAMA Ophthalmol. 2014;132(5):593–99. doi:10.1001/jamaophthalmol.2013.8295.
   PubMed Web of Science ®Google Scholar
• Ferre P, Foufelle F. Hepatic steatosis: A role for de novo lipogenesis and the transcription factor SREBP-1c. Diabetes Obes Metab. 2010;12(Suppl 2):83–92. doi:10.1111/j.1463-1326.2010.01275.x.
   PubMed Web of Science ®Google Scholar
• Eberle D, Hegarty B, Bossard P, Ferre P, Foufelle F. Srebp transcription factors: master regulators of lipid homeostasis. Biochimie. 2004;86(11):839–48. doi:10.1016/j.biochi.2004.09.018.
   PubMed Web of Science ®Google Scholar
• Horton JD, Goldstein JL, Brown MS. Srebps: activators of the complete program of cholesterol and fatty acid synthesis in the liver. J Clin Invest. 2002;109(9):1125–31. doi:10.1172/JCI0215593.
   PubMed Web of Science ®Google Scholar
• Gosmain Y, Dif N, Berbe V, Loizon E, Rieusset J, Vidal H, Lefai E. Regulation of SREBP-1 expression and transcriptional action on HKII and FAS genes during fasting and refeeding in rat tissues. J Lipid Res. 2005;46(4):697–705. doi:10.1194/jlr.M400261-JLR200.
   PubMed Web of Science ®Google Scholar
• Eskelinen EL. Roles of lamp-1 and lamp-2 in lysosome biogenesis and autophagy. Mol Aspects Med. 2006;27(5–6):495–502. doi:10.1016/j.mam.2006.08.005.
   PubMedGoogle Scholar
• Tanida I, Ueno T, Kominami E. LC3 and autophagy. Methods Mol Biol. 2008;445:77–88.
   PubMedGoogle Scholar
• Koukourakis MI, Kalamida D, Giatromanolaki A, Zois CE, Sivridis E, Pouliliou S, Mitrakas A, Gatter KC, Harris AL. Autophagosome proteins LC3A, LC3B and LC3C have distinct subcellular distribution kinetics and expression in cancer cell lines. PLoS One. 2015;10(9):e0137675. doi:10.1371/journal.pone.0137675.
   PubMed Web of Science ®Google Scholar
• Sugiura Y, Soeta S, Ichihara N, Nishita T, Murakami M, Amasaki H, Amasaki T, Asari M. Immunohistolocalization and gene expression of the carbonic anhydrase isoenzymes (CA-II and CA-VI) in glands associated with the canine lacrimal apparatus. Anat Histol Embryol. 2010;39(1):1–6. doi:10.1111/j.1439-0264.2009.00966.x.
   PubMed Web of Science ®Google Scholar
• Noda Y, Takai Y, Iwai Y, Meenaghan MA, Mori M. Immunohistochemical study of carbonic anhydrase in mixed tumours from major salivary glands and skin. Virchows Arch A Pathol Anat Histopathol. 1986;408(5):449–59. doi:10.1007/BF00705299.
   PubMedGoogle Scholar
• Wheatley VR, Hodgins LT, Coon WM. Cutaneous lipogenesis. I. Evaluation of model systems and the utilization of acetate, citrate and glucose as compared with other tissues. J Invest Dermatol. 1970;54(4):288–97. doi:10.1111/1523-1747.ep12258582.
   PubMed Web of Science ®Google Scholar
• Casini A, Antel J, Abbate F, Scozzafava A, David S, Waldeck H, Schafer S, Supuran CT. Carbonic anhydrase inhibitors: SAR and X-ray crystallographic study for the interaction of sugar sulfamates/sulfamides with isozymes I, II and IV. Bioorg Med Chem Lett. 2003;13(5):841–45. doi:10.1016/S0960-894X(03)00029-5.
   PubMed Web of Science ®Google Scholar
• Picard F, Deshaies Y, Lalonde J, Samson P, Richard D. Topiramate reduces energy and fat gains in lean (fa/?) and obese (fa/fa) zucker rats. Obes Res. 2000;8(9):656–63. doi:10.1038/oby.2000.84.
   PubMedGoogle Scholar
• De Simone G, Di Fiore A, Menchise V, Pedone C, Antel J, Casini A, Scozzafava A, Wurl M, Supuran CT. Carbonic anhydrase inhibitors. Zonisamide is an effective inhibitor of the cytosolic isozyme II and mitochondrial isozyme V: solution and x-ray crystallographic studies. Bioorg Med Chem Lett. 2005;15(9):2315–20. doi:10.1016/j.bmcl.2005.03.032.
   PubMed Web of Science ®Google Scholar
• Lynch CJ, Fox H, Hazen SA, Stanley BA, Dodgson S, Lanoue KF. Role of hepatic carbonic anhydrase in de novo lipogenesis. Biochem J. 1995;310(Pt 1):197–202. doi:10.1042/bj3100197.
   PubMed Web of Science ®Google Scholar
• Hazen SA, Waheed A, Sly WS, LaNoue KF, Lynch CJ. Differentiation-dependent expression of CA V and the role of carbonic anhydrase isozymes in pyruvate carboxylation in adipocytes. Faseb J. 1996;10(4):481–90. doi:10.1096/fasebj.10.4.8647347.
   PubMed Web of Science ®Google Scholar
• Reasor MJ, Hastings KL, Ulrich RG. Drug-induced phospholipidosis: issues and future directions. Expert Opin Drug Saf. 2006;5(4):567–83. doi:10.1517/14740338.5.4.567.
   PubMed Web of Science ®Google Scholar
• The regulatory challenges of drug-induced phospholipidosis. http://www.fda.gov/downloads/advisorycommittees/committeesmeetingmaterials/drugs/advisorycommitteeforpharmaceuticalscienceandclinicalpharmacology/ucm210798.pdf: FDA
   Google Scholar
• Lowe R, Mussa HY, Nigsch F, Glen RC, Mitchell JB. Predicting the mechanism of phospholipidosis. J Cheminform. 2012;4:2. doi:10.1186/1758-2946-4-2.
   PubMed Web of Science ®Google Scholar
• Liu Y, Kam WR, Ding J, Sullivan DA. One man’s poison is another man’s meat: using azithromycin-induced phospholipidosis to promote ocular surface health. Toxicology. 2014;320:1–5. doi:10.1016/j.tox.2014.02.014.
   PubMed Web of Science ®Google Scholar
• Liu Y, Kam WR, Fernandes P, Sullivan DA. The effect of solithromycin, a cationic amphiphilic drug, on the proliferation and differentiation of human meibomian gland epithelial cells. Curr Eye Res. 2018;43(6):683–88. doi:10.1080/02713683.2017.1418894.
   PubMed Web of Science ®Google Scholar
• Xu J, Peng Z, Li R, Dou T, Xu W, Gu G, Liu Y, Kang Z, Tao H, Zhang JH, et al. Normoxic induction of cerebral HIF-1alpha by acetazolamide in rats: role of acidosis. Neurosci Lett. 2009;451(3):274–78. doi:10.1016/j.neulet.2009.01.008.
   PubMed Web of Science ®Google Scholar
• Jewell UR, Kvietikova I, Scheid A, Bauer C, Wenger RH, Gassmann M. Induction of HIF-1alpha in response to hypoxia is instantaneous. Faseb J. 2001;15(7):1312–14. doi:10.1096/fj.00-0732fje.
   PubMed Web of Science ®Google Scholar
• Majmundar AJ, Wong WJ, Simon MC. Hypoxia-inducible factors and the response to hypoxic stress. Mol Cell. 2010;40(2):294–309. doi:10.1016/j.molcel.2010.09.022.
   PubMed Web of Science ®Google Scholar
• Liu Y, Chen D, Chen X, Kam WR, Hatton MP, Sullivan DA. Hypoxia: A breath of fresh air for the meibomian gland. Ocul Surf. 2019;17(2):310–17. doi:10.1016/j.jtos.2018.12.001.
   PubMed Web of Science ®Google Scholar
• Han X, Liu Y, Kam WR, Sullivan DA. Effect of brimonidine, an alpha2 adrenergic agonist, on human meibomian gland epithelial cells. Exp Eye Res. 2018;170:20–28. doi:10.1016/j.exer.2018.02.009.
   PubMed Web of Science ®Google Scholar
• Belkaid A, Cuperlovic-Culf M, Touaibia M, Ouellette RJ, Surette ME. Metabolic effect of estrogen receptor agonists on breast cancer cells in the presence or absence of carbonic anhydrase inhibitors. Metabolites. 2016;6(2). doi:10.3390/metabo6020016.
   PubMed Web of Science ®Google Scholar
• Reibring CG, El Shahawy M, Hallberg K, Kannius-Janson M, Nilsson J, Parkkila S, Sly WS, Waheed A, Linde A, Gritli-Linde A. Expression patterns and subcellular localization of carbonic anhydrases are developmentally regulated during tooth formation. PLoS One. 2014;9(5):e96007. doi:10.1371/journal.pone.0096007.
   PubMed Web of Science ®Google Scholar
• Mizushima N, Ohsumi Y, Yoshimori T. Autophagosome formation in mammalian cells. Cell Struct Funct. 2002;27(6):421–29. doi:10.1247/csf.27.421.
   PubMed Web of Science ®Google Scholar
• Maren TH, Conroy CW, Wynns GC, Levy NS. Ocular absorption, blood levels, and excretion of dorzolamide, a topically active carbonic anhydrase inhibitor. J Ocul Pharmacol Ther. 1997;13:23–30. doi:10.1089/jop.1997.13.23.
   PubMed Web of Science ®Google Scholar
• Biollaz J, Munafo A, Buclin T, Gervasoni JP, Magnin JL, Jaquet F, Brunner-Ferber F. Whole-blood pharmacokinetics and metabolic effects of the topical carbonic anhydrase inhibitor dorzolamide. Eur J Clin Pharmacol. 1995;47:455–60. doi:10.1007/BF00196861.
   PubMed Web of Science ®Google Scholar