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Current Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 0929-8673
ISSN (Online): 1875-533X

Review Article

Pathophysiological Role and Drug Modulation of Calcium Transport in Ocular Surface Cells

Author(s): Chen-Chen Chu and Shao-Zhen Zhao*

Volume 27, Issue 30, 2020

Page: [5078 - 5091] Pages: 14

DOI: 10.2174/0929867326666190619114848

Price: $65

Abstract

The ocular surface structure and extraocular accessory organs constitute the ocular surface system, which includes the cornea, conjunctiva, eyelids, lacrimal organs, and lacrimal passages. This system is composed of, and stabilized by, the corneal epithelium, conjunctival cells, conjunctival goblet cells, lacrimal acinar cells and Tenon’s fibroblasts, all of which maintain the healthy eyeball surface system. Ocular surface diseases are commonly referred to corneal and conjunctival disease and external ocular disease, resulting from damage to the ocular surface structure. A growing body of evidence has indicated that abnormal activation of the KCa3.1 channel and Ca2+/ calmodulin-dependent kinase initiates ocular injury. Signaling pathways downstream of the irregular Ca2+ influx induce cell progression and migration, and impair tight junctions, epithelial transport and secretory function. In this overview, we summarize the current knowledge regarding ocular surface disease in terms of physical and pathological alteration of the ocular system. We dissect in-depth, the mechanisms underlying disease progression, and we describe the current calcium transport therapeutics and the obstacles that remain to be solved. Finally, we summarize how to integrate the research results into clinical practice in the future.

Keywords: Calcium, ocular surface diseases, cornea, conjunctiva, lacrimal gland, ocular diseases, pathological role of calcium ion.

« Previous
[1]
Bron, A.J.; de Paiva, C.S.; Chauhan, S.K.; Bonini, S.; Gabison, E.E.; Jain, S.; Knop, E.; Markoulli, M.; Ogawa, Y.; Perez, V.; Uchino, Y.; Yokoi, N.; Zoukhri, D.; Sullivan, D.A. TFOS DEWS II pathophysiology report. Ocul. Surf., 2017, 15(3), 438-510.
[http://dx.doi.org/10.1016/j.jtos.2017.05.011] [PMID: 28736340]
[2]
Botelho, S.Y. Tears and the lacrimal gland. Sci. Am., 1964, 211, 78-86.
[http://dx.doi.org/10.1038/scientificamerican1064-78] [PMID: 14216948]
[3]
Hodges, R.R.; Dartt, D.A. Tear film mucins: front line defenders of the ocular surface; comparison with airway and gastrointestinal tract mucins. Exp. Eye Res., 2013, 117, 62-78.
[http://dx.doi.org/10.1016/j.exer.2013.07.027] [PMID: 23954166]
[4]
Nelson, J.D.; Craig, J.P.; Akpek, E.K.; Azar, D.T.; Belmonte, C.; Bron, A.J.; Clayton, J.A.; Dogru, M.; Dua, H.S.; Foulks, G.N.; Gomes, J.A.P.; Hammitt, K.M.; Holopainen, J.; Jones, L.; Joo, C.K.; Liu, Z.; Nichols, J.J.; Nichols, K.K.; Novack, G.D.; Sangwan, V.; Stapleton, F.; Tomlinson, A.; Tsubota, K.; Willcox, M.D.P.; Wolffsohn, J.S.; Sullivan, D.A. TFOS DEWS II introduction. Ocul. Surf., 2017, 15(3), 269-275.
[http://dx.doi.org/10.1016/j.jtos.2017.05.005] [PMID: 28736334]
[5]
Willcox, M.D.P.; Argüeso, P.; Georgiev, G.A.; Holopainen, J.M.; Laurie, G.W.; Millar, T.J.; Papas, E.B.; Rolland, J.P.; Schmidt, T.A.; Stahl, U.; Suarez, T.; Subbaraman, L.N.; Uçakhan, O.Ö.; Jones, L. Tfos dews ii tear film report. Ocul. Surf., 2017, 15(3), 366-403.
[http://dx.doi.org/10.1016/j.jtos.2017.03.006] [PMID: 28736338]
[6]
Chou, K.C. Structural bioinformatics and its impact to biomedical science. Curr. Med. Chem., 2004, 11(16), 2105-2134.
[http://dx.doi.org/10.2174/0929867043364667] [PMID: 15279552]
[7]
Klein, C.; Malviya, A.N. Mechanism of nuclear calcium signaling by inositol 1,4,5-trisphosphate produced in the nucleus, nuclear located protein kinase C and cyclic AMP-dependent protein kinase. Front. Biosci., 2008, 13, 1206-1226.
[http://dx.doi.org/10.2741/2756] [PMID: 17981624]
[8]
Berridge, M.J. The inositol trisphosphate/calcium signaling pathway in health and disease. Physiol. Rev., 2016, 96(4), 1261-1296.
[http://dx.doi.org/10.1152/physrev.00006.2016] [PMID: 27512009]
[9]
Berridge, M.J. Calcium signalling remodelling and disease. Biochem. Soc. Trans., 2012, 40(2), 297-309.
[http://dx.doi.org/10.1042/BST20110766] [PMID: 22435804]
[10]
Foskett, J.K.; White, C.; Cheung, K.H.; Mak, D.O. Inositol trisphosphate receptor Ca2+ release channels. Physiol. Rev., 2007, 87(2), 593-658.
[http://dx.doi.org/10.1152/physrev.00035.2006] [PMID: 17429043]
[11]
Santulli, G.; Nakashima, R.; Yuan, Q.; Marks, A.R. Intracellular calcium release channels: an update. J. Physiol., 2017, 595(10), 3041-3051.
[http://dx.doi.org/10.1113/JP272781] [PMID: 28303572]
[12]
Berridge, M.J. Calcium signalling in health and disease. Biochem. Biophys. Res. Commun., 2017, 485(1), 5.
[http://dx.doi.org/10.1016/j.bbrc.2017.01.098] [PMID: 28130105]
[13]
Mantelli, F.; Argüeso, P. Functions of ocular surface mucins in health and disease. Curr. Opin. Allergy Clin. Immunol., 2008, 8(5), 477-483.
[http://dx.doi.org/10.1097/ACI.0b013e32830e6b04] [PMID: 18769205]
[14]
Dartt, D.A.; Masli, S. Conjunctival epithelial and goblet cell function in chronic inflammation and ocular allergic inflammation. Curr. Opin. Allergy Clin. Immunol., 2014, 14(5), 464-470.
[http://dx.doi.org/10.1097/ACI.0000000000000098] [PMID: 25061855]
[15]
Hori, Y. Secreted mucins on the ocular surface. Invest. Ophthalmol. Vis. Sci., 2018, 59(14), DES151-DES156.
[http://dx.doi.org/10.1167/iovs.17-23623] [PMID: 30481820]
[16]
Dartt, D.A.; Hodges, R.R.; Li, D.; Shatos, M.A.; Lashkari, K.; Serhan, C.N. Conjunctival goblet cell secretion stimulated by leukotrienes is reduced by resolvins D1 and E1 to promote resolution of inflammation. J. Immunol., 2011, 186(7), 4455-4466.
[http://dx.doi.org/10.4049/jimmunol.1000833] [PMID: 21357260]
[17]
Ríos, J.D.; Zoukhri, D.; Rawe, I.M.; Hodges, R.R.; Zieske, J.D.; Dartt, D.A. Immunolocalization of muscarinic and VIP receptor subtypes and their role in stimulating goblet cell secretion. Invest. Ophthalmol. Vis. Sci., 1999, 40(6), 1102-1111.
[PMID: 10235543]
[18]
Hayashi, D.; Li, D.; Hayashi, C.; Shatos, M.; Hodges, R.R.; Dartt, D.A. Role of histamine and its receptor subtypes in stimulation of conjunctival goblet cell secretion. Invest. Ophthalmol. Vis. Sci., 2012, 53(6), 2993-3003.
[http://dx.doi.org/10.1167/iovs.11-8748] [PMID: 22467574]
[19]
Rivera-Ramírez, N.; Montejo-López, W.; López-Méndez, M.C.; Guerrero-Hernández, A.; Molina-Hernández, A.; García-Hernández, U.; Arias-Montaño, J.A. Histamine H3 receptor activation stimulates calcium mobilization in a subpopulation of rat striatal neurons in primary culture, but not in synaptosomes. Neurochem. Int., 2016, 101, 38-47.
[http://dx.doi.org/10.1016/j.neuint.2016.10.005] [PMID: 27744004]
[20]
Sadek, B.; Stark, H. Cherry-picked ligands at histamine receptor subtypes. Neuropharmacology, 2016, 106, 56-73.
[http://dx.doi.org/10.1016/j.neuropharm.2015.11.005] [PMID: 26581501]
[21]
Schneider, E.H.; Seifert, R. The histamine H4-receptor and the central and peripheral nervous system: a critical analysis of the literature. Neuropharmacology, 2016, 106, 116-128.
[http://dx.doi.org/10.1016/j.neuropharm.2015.05.004] [PMID: 25986697]
[22]
Li, D.; Carozza, R.B.; Shatos, M.A.; Hodges, R.R.; Dartt, D.A. Effect of histamine on Ca(2+)-dependent signaling pathways in rat conjunctival goblet cells. Invest. Ophthalmol. Vis. Sci., 2012, 53(11), 6928-6938.
[http://dx.doi.org/10.1167/iovs.12-10163] [PMID: 22956601]
[23]
He, M.; Lippestad, M.; Li, D.; Hodges, R.R.; Utheim, T.P.; Dartt, D.A. Activation of the egf receptor by histamine receptor subtypes stimulates mucin secretion in conjunctival goblet cells. Invest. Ophthalmol. Vis. Sci., 2018, 59(8), 3543-3553.
[http://dx.doi.org/10.1167/iovs.18-2476] [PMID: 30025103]
[24]
Kanno, H.; Horikawa, Y.; Hodges, R.R.; Zoukhri, D.; Shatos, M.A.; Rios, J.D.; Dartt, D.A. Cholinergic agonists transactivate EGFR and stimulate MAPK to induce goblet cell secretion. Am. J. Physiol. Cell Physiol., 2003, 284(4), C988-C998.
[http://dx.doi.org/10.1152/ajpcell.00582.2001] [PMID: 12620895]
[25]
Li, D.; Hodges, R.R.; Jiao, J.; Carozza, R.B.; Shatos, M.A.; Chiang, N.; Serhan, C.N.; Dartt, D.A. Resolvin D1 and aspirin-triggered resolvin D1 regulate histamine-stimulated conjunctival goblet cell secretion. Mucosal Immunol., 2013, 6(6), 1119-1130.
[http://dx.doi.org/10.1038/mi.2013.7] [PMID: 23462912]
[26]
English, J.T.; Norris, P.C.; Hodges, R.R.; Dartt, D.A.; Serhan, C.N. Identification and profiling of specialized pro-resolving mediators in human tears by lipid mediator metabolomics. Prostaglandins Leukot. Essent. Fatty Acids, 2017, 117, 17-27.
[http://dx.doi.org/10.1016/j.plefa.2017.01.004] [PMID: 28237084]
[27]
Hodges, R.R.; Li, D.; Shatos, M.A.; Bair, J.A.; Lippestad, M.; Serhan, C.N.; Dartt, D.A. Lipoxin A4 activates ALX/FPR2 receptor to regulate conjunctival goblet cell secretion. Mucosal Immunol., 2017, 10(1), 46-57.
[http://dx.doi.org/10.1038/mi.2016.33] [PMID: 27072607]
[28]
Dartt, D.A. Signal transduction and control of lacrimal gland protein secretion: a review. Curr. Eye Res., 1989, 8(6), 619-636.
[http://dx.doi.org/10.3109/02713688908995762] [PMID: 2545411]
[29]
Ikeda-Kurosawa, C.; Higashio, H.; Nakano, M.; Okubo, M.; Satoh, Y.; Kurosaka, D.; Saino, T. α1-Adrenoceptors relate Ca(2+) modulation and protein secretions in rat lacrimal gland. Biomed. Res., 2015, 36(6), 357-369.
[http://dx.doi.org/10.2220/biomedres.36.357] [PMID: 26700590]
[30]
Dartt, D.A. Neural regulation of lacrimal gland secretory processes: relevance in dry eye diseases. Prog. Retin. Eye Res., 2009, 28(3), 155-177.
[http://dx.doi.org/10.1016/j.preteyeres.2009.04.003] [PMID: 19376264]
[31]
Vizvári, E.; Katona, M.; Orvos, P.; Berczeli, O.; Facskó, A.; Rárosi, F.; Venglovecz, V.; Rakonczay, Z., Jr; Hegyi, P.; Ding, C.; Tóth-Molnár, E. Characterization of Na+-K+-2Cl- cotransporter activity in rabbit lacrimal gland duct cells. Invest. Ophthalmol. Vis. Sci., 2016, 57(8), 3828-3835.
[http://dx.doi.org/10.1167/iovs.15-18462] [PMID: 27438543]
[32]
Imada, T.; Nakamura, S.; Hisamura, R.; Izuta, Y.; Jin, K.; Ito, M.; Kitamura, N.; Tanaka, K.F.; Mimura, M.; Shibuya, I.; Tsubota, K. Serotonin hormonally regulates lacrimal gland secretory function via the serotonin type 3a receptor. Sci. Rep., 2017, 7(1), 6965.
[http://dx.doi.org/10.1038/s41598-017-06022-4] [PMID: 28761086]
[33]
Hodges, R.R.; Dartt, D.A. Regulatory pathways in lacrimal gland epithelium. Int. Rev. Cytol., 2003, 231, 129-196.
[http://dx.doi.org/10.1016/S0074-7696(03)31004-6] [PMID: 14713005]
[34]
Jumblatt, J.E.; Jumblatt, M.M. Regulation of ocular mucin secretion by P2Y2 nucleotide receptors in rabbit and human conjunctiva. Exp. Eye Res., 1998, 67(3), 341-346.
[http://dx.doi.org/10.1006/exer.1998.0520] [PMID: 9778415]
[35]
Xing, J.; Petranka, J.G.; Davis, F.M.; Desai, P.N.; Putney, J.W.; Bird, G.S. Role of Orai1 and store-operated calcium entry in mouse lacrimal gland signalling and function. J. Physiol., 2014, 592(5), 927-939.
[http://dx.doi.org/10.1113/jphysiol.2013.267740] [PMID: 24297846]
[36]
Gershon, M.D. 5-Hydroxytryptamine (serotonin) in the gastrointestinal tract. Curr. Opin. Endocrinol. Diabetes Obes., 2013, 20(1), 14-21.
[http://dx.doi.org/10.1097/MED.0b013e32835bc703] [PMID: 23222853]
[37]
Mauduit, P.; Jammes, H.; Rossignol, B. M3 muscarinic acetylcholine receptor coupling to PLC in rat exorbital lacrimal acinar cells. Am. J. Physiol., 1993, 264(6 Pt 1), C1550-C1560.
[http://dx.doi.org/10.1152/ajpcell.1993.264.6.C1550] [PMID: 8333505]
[38]
Chen, L.L.; Johansson, J.K.; Hodges, R.R.; Zoukhri, D.; Ghinelli, E.; Rios, J.D.; Dartt, D.A. Differential effects of the EGF family of growth factors on protein secretion, MAPK activation, and intracellular calcium concentration in rat lacrimal gland. Exp. Eye Res., 2005, 80(3), 379-389.
[http://dx.doi.org/10.1016/j.exer.2004.10.006] [PMID: 15721620]
[39]
Tepavcevic, V.; Hodges, R.R.; Zoukhri, D.; Dartt, D.A. Signal transduction pathways used by EGF to stimulate protein secretion in rat lacrimal gland. Invest. Ophthalmol. Vis. Sci., 2003, 44(3), 1075-1081.
[http://dx.doi.org/10.1167/iovs.02-0794] [PMID: 12601032]
[40]
Zoukhri, D.; Hodges, R.R.; Sergheraert, C.; Toker, A.; Dartt, D.A. Lacrimal gland PKC isoforms are differentially involved in agonist-induced protein secretion. Am. J. Physiol., 1997, 272(1 Pt 1), C263-C269.
[http://dx.doi.org/10.1152/ajpcell.1997.272.1.C263] [PMID: 9038832]
[41]
Meneray, M.A.; Fields, T.Y. Adrenergic stimulation of lacrimal protein secretion is mediated by G(q/11)alpha and G(s)alpha. Curr. Eye Res., 2000, 21(2), 602-607.
[http://dx.doi.org/10.1076/0271-3683(200008)2121-VFT602] [PMID: 11148596]
[42]
Dartt, D.A.; Dicker, D.M.; Ronco, L.V.; Kjeldsen, I.M.; Hodges, R.R.; Murphy, S.A. Lacrimal gland inositol trisphosphate isomer and inositol tetrakisphosphate production. Am. J. Physiol., 1990, 259(2 Pt 1), G274-G281.
[PMID: 2382726]
[43]
Bhattacharya, S.; García-Posadas, L.; Hodges, R.R.; Makarenkova, H.P.; Masli, S.; Dartt, D.A. Alteration in nerves and neurotransmitter stimulation of lacrimal gland secretion in the TSP-1-/- mouse model of aqueous deficiency dry eye. Mucosal Immunol., 2018, 11(4), 1138-1148.
[http://dx.doi.org/10.1038/s41385-018-0002-y] [PMID: 29445135]
[44]
Flores, A.M.; Casey, S.D.; Felix, C.M.; Phuan, P.W.; Verkman, A.S.; Levin, M.H. Small-molecule CFTR activators increase tear secretion and prevent experimental dry eye disease. FASEB J., 2016, 30(5), 1789-1797.
[http://dx.doi.org/10.1096/fj.201500180] [PMID: 26842854]
[45]
Zeng, M.; Szymczak, M.; Ahuja, M.; Zheng, C.; Yin, H.; Swaim, W.; Chiorini, J.A.; Bridges, R.J.; Muallem, S. Resto-ration of cftr activity in ducts rescues acinar cell function and reduces inflammation in pancreatic and salivary glands of mice. Gastroenterology, 2017, 153(4), 1148-1159.
[http://dx.doi.org/10.1053/j.gastro.2017.06.011] [PMID: 28634110]
[46]
Oikawa, M.; Saino, T.; Kimura, K.; Kamada, Y.; Tamagawa, Y.; Kurosaka, D.; Satoh, Y. Effects of protease-activated receptors (PARs) on intracellular calcium dynamics of acinar cells in rat lacrimal glands. Histochem. Cell Biol., 2013, 140(4), 463-476.
[http://dx.doi.org/10.1007/s00418-013-1082-0] [PMID: 23463389]
[47]
Thody, A.J.; Shuster, S. Control and function of sebaceous glands. Physiol. Rev., 1989, 69(2), 383-416.
[http://dx.doi.org/10.1152/physrev.1989.69.2.383] [PMID: 2648418]
[48]
Green-Church, K.B.; Butovich, I.; Willcox, M.; Borchman, D.; Paulsen, F.; Barabino, S.; Glasgow, B.J. 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(4), 1979-1993.
[http://dx.doi.org/10.1167/iovs.10-6997d] [PMID: 21450916]
[49]
Horwath-Winter, J.; Berghold, A.; Schmut, O.; Floegel, I.; Solhdju, V.; Bodner, E.; Schwantzer, G.; Haller-Schober, E.M. Evaluation of the clinical course of dry eye syndrome. Arch. Ophthalmol., 2003, 121(10), 1364-1368.
[http://dx.doi.org/10.1001/archopht.121.10.1364] [PMID: 14557170]
[50]
Stapleton, F.; Alves, M.; Bunya, V.Y.; Jalbert, I.; Lekhanont, K.; Malet, F.; Na, K.S.; Schaumberg, D.; Uchino, M.; Vehof, J.; Viso, E.; Vitale, S.; Jones, L. Tfos dews ii epidemiology report. Ocul. Surf., 2017, 15(3), 334-365.
[http://dx.doi.org/10.1016/j.jtos.2017.05.003] [PMID: 28736337]
[51]
Kam, W.R.; Sullivan, D.A. Neurotransmitter influence on human meibomian gland epithelial cells. Invest. Ophthalmol. Vis. Sci., 2011, 52(12), 8543-8548.
[http://dx.doi.org/10.1167/iovs.11-8113] [PMID: 21969302]
[52]
Sreedharan, S.P.; Patel, D.R.; Xia, M.; Ichikawa, S.; Goetzl, E.J. Human vasoactive intestinal peptide1 receptors expressed by stable transfectants couple to two distinct signaling pathways. Biochem. Biophys. Res. Commun., 1994, 203(1), 141-148.
[http://dx.doi.org/10.1006/bbrc.1994.2160] [PMID: 8074647]
[53]
Luo, X.; Zeng, W.; Xu, X.; Popov, S.; Davignon, I.; Wilkie, T.M.; Mumby, S.M.; Muallem, S. Alternate coupling of receptors to Gs and Gi in pancreatic and submandibular gland cells. J. Biol. Chem., 1999, 274(25), 17684-17690.
[http://dx.doi.org/10.1074/jbc.274.25.17684] [PMID: 10364208]
[54]
Yoshimura, K.; Nezu, E. Interaction between the calcium and cyclic AMP messenger systems in perifused rat parotid acinar cells. Possible mechanism for potentiation of amylase secretion. Biochem. Pharmacol., 1992, 43(5), 1031-1041.
[http://dx.doi.org/10.1016/0006-2952(92)90610-U] [PMID: 1372804]
[55]
Schröder, A.; Abrar, D.B.; Hampel, U.; Schicht, M.; Paulsen, F.; Garreis, F. In vitro effects of sex hormones in human meibomian gland epithelial cells. exp. eye res., 2016, 151, 190-202, 190-202.,
[http://dx.doi.org/10.1016/j.exer.2016.08.009] [PMID: 27569371]
[56]
Bikle, D.D.; Xie, Z.; Tu, C.L. Calcium regulation of keratinocyte differentiation. Expert Rev. Endocrinol. Metab., 2012, 7(4), 461-472.
[http://dx.doi.org/10.1586/eem.12.34] [PMID: 23144648]
[57]
Kubo-Watanabe, S.; Satoh, Y.; Saino, T. Adenosine-5′-triphosphate-induced intracellular calcium changes through gap-junctional communication in the corneal epithelium. Jpn. J. Ophthalmol., 2002, 46(5), 479-487.
[http://dx.doi.org/10.1016/S0021-5155(02)00535-X] [PMID: 12457905]
[58]
Justet, C.; Hernández, J.A.; Torriglia, A.; Chifflet, S. Fast calcium wave inhibits excessive apoptosis during epithelial wound healing. Cell Tissue Res., 2016, 365(2), 343-356.
[http://dx.doi.org/10.1007/s00441-016-2388-8] [PMID: 26987821]
[59]
Lee, A.; Derricks, K.; Minns, M.; Ji, S.; Chi, C.; Nugent, M.A.; Trinkaus-Randall, V. Hypoxia-induced changes in Ca(2+) mobilization and protein phosphorylation implicated in impaired wound healing. Am. J. Physiol. Cell Physiol., 2014, 306(10), C972-C985.
[http://dx.doi.org/10.1152/ajpcell.00110.2013] [PMID: 24671101]
[60]
Kimura, K.; Nishimura, T.; Satoh, Y. Effects of ATP and its analogues on [Ca2+]i dynamics in the rabbit corneal epithelium. Arch. Histol. Cytol., 1999, 62(2), 129-138.
[http://dx.doi.org/10.1679/aohc.62.129] [PMID: 10399537]
[61]
Berridge, M.J.; Bootman, M.D.; Lipp, P. Calcium--a life and death signal. Nature, 1998, 395(6703), 645-648.
[http://dx.doi.org/10.1038/27094] [PMID: 9790183]
[62]
Kasumu, A.W.; Liang, X.; Egorova, P.; Vorontsova, D.; Bezprozvanny, I. Chronic suppression of inositol 1,4,5-triphosphate receptor-mediated calcium signaling in cerebellar purkinje cells alleviates pathological phenotype in spinocerebellar ataxia 2 mice. J. Neurosci., 2012, 32(37), 12786-12796.
[http://dx.doi.org/10.1523/JNEUROSCI.1643-12.2012] [PMID: 22973002]
[63]
Cordeiro, J.V.; Jacinto, A. The role of transcription-independent damage signals in the initiation of epithelial wound healing. Nat. Rev. Mol. Cell Biol., 2013, 14(4), 249-262.
[http://dx.doi.org/10.1038/nrm3541] [PMID: 23443750]
[64]
Jacinto, A.; Martinez-Arias, A.; Martin, P. Mechanisms of epithelial fusion and repair. Nat. Cell Biol., 2001, 3(5), E117-E123.
[http://dx.doi.org/10.1038/35074643] [PMID: 11331897]
[65]
Stanisstreet, M. Calcium and wound healing in Xenopus early embryos. J. Embryol. Exp. Morphol., 1982, 67, 195-205.
[PMID: 6806425]
[66]
Kawai, K.; Larson, B.J.; Ishise, H.; Carre, A.L.; Nishimoto, S.; Longaker, M.; Lorenz, H.P. Calcium-based nanoparticles accelerate skin wound healing. PLoS One, 2011, 6(11), e27106.
[http://dx.doi.org/10.1371/journal.pone.0027106] [PMID: 22073267]
[67]
Ghannad-Rezaie, M.; Wang, X.; Mishra, B.; Collins, C.; Chronis, N. Microfluidic chips for in vivo imaging of cellular responses to neural injury in Drosophila larvae. PLoS One, 2012, 7(1), e29869.
[http://dx.doi.org/10.1371/journal.pone.0029869] [PMID: 22291895]
[68]
Tran, P.O.; Hinman, L.E.; Unger, G.M.; Sammak, P.J. A wound-induced [Ca2+]i increase and its transcriptional activation of immediate early genes is important in the regulation of motility. Exp. Cell Res., 1999, 246(2), 319-326.
[http://dx.doi.org/10.1006/excr.1998.4239] [PMID: 9925747]
[69]
Kim, H.J.; Kim, J.Y.; Lee, B.H.; Choi, S.H.; Rhim, H.; Kim, H.C.; Ahn, S.Y.; Jeong, S.W.; Jang, M.; Cho, I.H.; Nah, S.Y. Gintonin, an exogenous ginseng-derived LPA receptor ligand, promotes corneal wound healing. J. Vet. Sci., 2017, 18(3), 387-397.
[http://dx.doi.org/10.4142/jvs.2017.18.3.387] [PMID: 27586470]
[70]
Hwang, S.H.; Lee, B.H.; Choi, S.H.; Kim, H.J.; Jung, S.W.; Kim, H.S.; Shin, H.C.; Park, H.J.; Park, K.H.; Lee, M.K.; Nah, S.Y. Gintonin, a novel ginseng-derived lysophosphatidic acid receptor ligand, stimulates neurotransmitter release. Neurosci. Lett., 2015, 584, 356-361.
[http://dx.doi.org/10.1016/j.neulet.2014.11.007] [PMID: 25445364]
[71]
Mergler, S.; Valtink, M.; Takayoshi, S.; Okada, Y.; Miyajima, M.; Saika, S.; Reinach, P.S. Temperature-sensitive transient receptor potential channels in corneal tissue layers and cells. Ophthalmic Res., 2014, 52(3), 151-159.
[http://dx.doi.org/10.1159/000365334] [PMID: 25301091]
[72]
Zhang, F.; Yang, H.; Wang, Z.; Mergler, S.; Liu, H.; Kawakita, T.; Tachado, S.D.; Pan, Z.; Capó-Aponte, J.E.; Pleyer, U.; Koziel, H.; Kao, W.W.; Reinach, P.S. Transient receptor potential vanilloid 1 activation induces inflammatory cytokine release in corneal epithelium through MAPK signaling. J. Cell. Physiol., 2007, 213(3), 730-739.
[http://dx.doi.org/10.1002/jcp.21141] [PMID: 17508360]
[73]
Yang, Y.; Wang, Z.; Yang, H.; Wang, L.; Gillespie, S.R.; Wolosin, J.M.; Bernstein, A.M.; Reinach, P.S. TRPV1 potentiates TGFβ-induction of corneal myofibroblast development through an oxidative stress-mediated p38-SMAD2 signaling loop. PLoS One, 2013, 8(10), e77300.
[http://dx.doi.org/10.1371/journal.pone.0077300] [PMID: 24098582]
[74]
Inoue, R.; Kurahara, L.H.; Hiraishi, K. TRP channels in cardiac and intestinal fibrosis. Semin. Cell Dev. Biol., 2019, 94, 40-49.
[http://dx.doi.org/10.1016/j.semcdb.2018.11.002] [PMID: 30445149]
[75]
Feng, Q.Y.; Hu, Z.X.; Song, X.L.; Pan, H.W. Aberrant expression of genes and proteins in pterygium and their implications in the pathogenesis. Int. J. Ophthalmol., 2017, 10(6), 973-981.
[PMID: 28730091]
[76]
Buss, D.G.; Giuliano, E.A.; Sharma, A.; Mohan, R.R. Isolation and cultivation of equine corneal keratocytes, fibroblasts and myofibroblasts. Vet. Ophthalmol., 2010, 13(1), 37-42.
[http://dx.doi.org/10.1111/j.1463-5224.2009.00755.x] [PMID: 20149174]
[77]
Singh, V.; Santhiago, M.R.; Barbosa, F.L.; Agrawal, V.; Singh, N.; Ambati, B.K.; Wilson, S.E. Effect of TGFβ and PDGF-B blockade on corneal myofibroblast development in mice. Exp. Eye Res., 2011, 93(6), 810-817.
[http://dx.doi.org/10.1016/j.exer.2011.09.012] [PMID: 21978952]
[78]
Shukla, A.; Edwards, R.; Yang, Y.; Hahn, A.; Folkers, K.; Ding, J.; Padmakumar, V.C.; Cataisson, C.; Suh, K.S.; Yuspa, S.H. CLIC4 regulates TGF-β-dependent myofibroblast differentiation to produce a cancer stroma. Oncogene, 2014, 33(7), 842-850.
[http://dx.doi.org/10.1038/onc.2013.18] [PMID: 23416981]
[79]
Freise, C.; Heldwein, S.; Erben, U.; Hoyer, J.; Köhler, R.; Jöhrens, K.; Patsenker, E.; Ruehl, M.; Seehofer, D.; Stickel, F.; Somasundaram, R.k⁺ -channel inhibition reduces portal perfusion pressure in fibrotic rats and fibrosis associated characteristics of hepatic stellate cells. Liver Int., 2015, 35(4), 1244-1252.
[http://dx.doi.org/10.1111/liv.12681] [PMID: 25212242]
[80]
Roach, K.M.; Feghali-Bostwick, C.; Wulff, H.; Amrani, Y. Bradding, P. Human lung myofibroblast tgfbeta1-dependent smad2/3 signalling is ca(2+)-dependent and regulated by kca3.1 k(+) channels. Fibrogenesis Tissue Repair, 2015, 8(5)
[http://dx.doi.org/10.1186/s13069-015-0022-0] [PMID: 25829947]
[81]
Nakamura, K.; Hayashi, H.; Kubokawa, M. Proinflammatory cytokines and potassium channels in the kidney. Mediators Inflamm., 2015, 2015(362768), 362768.
[http://dx.doi.org/10.1155/2015/362768] [PMID: 26508816]
[82]
Saw, S.M.; Tan, D. Pterygium: prevalence, demography and risk factors. Ophthalmic Epidemiol., 1999, 6(3), 219-228.
[http://dx.doi.org/10.1076/opep.6.3.219.1504] [PMID: 10487976]
[83]
Garreis, F.; Schröder, A.; Reinach, P.S.; Zoll, S.; Khajavi, N.; Dhandapani, P.; Lucius, A.; Pleyer, U.; Paulsen, F.; Mergler, S. Upregulation of transient receptor potential vanil-loid type-1 channel activity and Ca2+ influx dysfunction in human pterygial cells. Invest. Ophthalmol. Vis. Sci., 2016, 57(6), 2564-2577.
[http://dx.doi.org/10.1167/iovs.16-19170] [PMID: 27163769]
[84]
Riau, A.K.; Wong, T.T.; Beuerman, R.W.; Tong, L. Calcium-binding S100 protein expression in pterygium. Mol. Vis., 2009, 15, 335-342.
[PMID: 19223989]
[85]
Réty, S.; Osterloh, D.; Arié, J.P.; Tabaries, S.; Seeman, J.; Russo-Marie, F.; Gerke, V.; Lewit-Bentley, A. Structural basis of the Ca(2+)-dependent association between S100C (S100A11) and its target, the N-terminal part of annexin I. Structure, 2000, 8(2), 175-184.
[http://dx.doi.org/10.1016/S0969-2126(00)00093-9] [PMID: 10673436]
[86]
Tong, L.; Li, J.; Chew, J.; Tan, D.; Beuerman, R. Phospholipase D in the human ocular surface and in pterygium. Cornea, 2008, 27(6), 693-698.
[http://dx.doi.org/10.1097/01.ico.0000611404.04418.6c] [PMID: 18580262]
[87]
Fang, C.; Illingworth, C.D.; Qian, L.; Wormstone, I.M. Serum deprivation can suppress receptor-mediated calcium signaling in pterygial-derived fibroblasts. Invest. Ophthalmol. Vis. Sci., 2013, 54(7), 4563-4570.
[http://dx.doi.org/10.1167/iovs.13-11604] [PMID: 23761089]
[88]
Nicola, C.; Timoshenko, A.V.; Dixon, S.J.; Lala, P.K.; Chakraborty, C. EP1 receptor-mediated migration of the first trimester human extravillous trophoblast: the role of intracellular calcium and calpain. J. Clin. Endocrinol. Metab., 2005, 90(8), 4736-4746.
[http://dx.doi.org/10.1210/jc.2005-0413] [PMID: 15886234]
[89]
Wang, L.; Eldred, J.A.; Sidaway, P.; Sanderson, J.; Smith, A.J.; Bowater, R.P.; Reddan, J.R.; Wormstone, I.M. Sigma 1 receptor stimulation protects against oxidative damage through suppression of the ER stress responses in the human lens. Mech. Ageing Dev., 2012, 133(11-12), 665-674.
[http://dx.doi.org/10.1016/j.mad.2012.09.005] [PMID: 23041531]
[90]
Anumanthan, G.; Wilson, P.J.; Tripathi, R.; Hesemann, N.P.; Mohan, R.R. Blockade of KCa3.1: a novel target to treat TGF-β1 induced conjunctival fibrosis. Exp. Eye Res., 2018, 167, 140-144.
[http://dx.doi.org/10.1016/j.exer.2017.12.003] [PMID: 29242028]
[91]
Chen, G.L.; Lei, M.; Zhou, L.P.; Zeng, B.; Zou, F. Borneol is a trpm8 agonist that increases ocular surface wetness. PLoS One, 2016, 11(7), e0158868.
[http://dx.doi.org/10.1371/journal.pone.0158868] [PMID: 27448228]
[92]
Kurose, M.; Meng, I.D. Dry eye modifies the thermal and menthol responses in rat corneal primary afferent cool cells. J. Neurophysiol., 2013, 110(2), 495-504.
[http://dx.doi.org/10.1152/jn.00222.2013] [PMID: 23636717]
[93]
Lee, S.; Phuan, P.W.; Felix, C.M.; Tan, J.A.; Levin, M.H.; Verkman, A.S. Nanomolar-potency aminophenyl-1,3,5-triazine activators of the cystic fibrosis transmembrane con-ductance regulator (cftr) chloride channel for prosecretory therapy of dry eye diseases. J. Med. Chem., 2017, 60(3), 1210-1218.
[http://dx.doi.org/10.1021/acs.jmedchem.6b01792] [PMID: 28099811]
[94]
Lippestad, M.; Hodges, R.R.; Utheim, T.P.; Serhan, C.N.; Dartt, D.A. Resolvin d1 increases mucin secretion in cultured rat conjunctival goblet cells via multiple signaling pathways. Invest. Ophthalmol. Vis. Sci., 2017, 58(11), 4530-4544.
[http://dx.doi.org/10.1167/iovs.17-21914] [PMID: 28892824]
[95]
García-Posadas, L.; Hodges, R.R.; Li, D.; Shatos, M.A.; Storr-Paulsen, T.; Diebold, Y.; Dartt, D.A. Interaction of IFN-γ with cholinergic agonists to modulate rat and human goblet cell function. Mucosal Immunol., 2016, 9(1), 206-217.
[http://dx.doi.org/10.1038/mi.2015.53] [PMID: 26129651]
[96]
Fujii, A.; Morimoto-Tochigi, A.; Walkup, R.D.; Shearer, T.R.; Azuma, M. Lacritin-induced secretion of tear proteins from cultured monkey lacrimal acinar cells. Invest. Ophthalmol. Vis. Sci., 2013, 54(4), 2533-2540.
[http://dx.doi.org/10.1167/iovs.12-10394] [PMID: 23482462]
[97]
Byun, YS; Yoo, YS; Kwon, JY; Joo, JS; Lim, SA; Whang, WJ; Mok, JW; Choi, JS; Joo, CK Diquafosol promotes corneal epithelial healing via intracellular calcium-mediated erk activation. Exp. Eye Res., 2016, 143, 89-97.
[http://dx.doi.org/10.1016/j.exer.2015.10.013] [PMID: 26505315]
[98]
Minns, M.S.; Teicher, G.; Rich, C.B.; Trinkaus-Randall, V. Purinoreceptor p2x7 regulation of Ca2+ mobilization and cytoskeletal rearrangement is required for corneal reepitheli-alization after injury. Am. J. Pathol., 2016, 186(2), 285-296.
[http://dx.doi.org/10.1016/j.ajpath.2015.10.006] [PMID: 26683661]
[99]
Nagai, N.; Ogata, F.; Kawasaki, N.; Ito, Y.; Funakami, Y.; Okamoto, N.; Shimomura, Y. Hypercalcemia leads to delayed corneal wound healing in ovariectomized rats. Biol. Pharm. Bull., 2015, 38(7), 1063-1069.
[http://dx.doi.org/10.1248/bpb.b15-00227] [PMID: 26133716]
[100]
Yang, Y.; Yang, H.; Wang, Z.; Varadaraj, K.; Kumari, S.S.; Mergler, S.; Okada, Y.; Saika, S.; Kingsley, P.J.; Marnett, L.J.; Reinach, P.S. Cannabinoid receptor 1 suppresses transient receptor potential vanilloid 1-induced inflammatory responses to corneal injury. Cell. Signal., 2013, 25(2), 501-511.
[http://dx.doi.org/10.1016/j.cellsig.2012.10.015] [PMID: 23142606]
[101]
Teranishi, S.; Kimura, K.; Nishida, T. Role of formation of an ERK-FAK-paxillin complex in migration of human corneal epithelial cells during wound closure in vitro. Invest. Ophthalmol. Vis. Sci., 2009, 50(12), 5646-5652.
[http://dx.doi.org/10.1167/iovs.08-2534] [PMID: 19494198]
[102]
Chien, J.M.; Huang, C.C.; Cheng, H.H.; Lin, K.L.; Chen, W.C.; Tseng, P.L.; Chou, C.T.; Tsai, J.Y.; Liao, W.C.; Wang, B.W.; Chang, P.M.; Jan, C.R. Econazole-evoked [Ca2+]i rise and non-Ca2+-triggered cell death in rabbit corneal epithelial cells (SIRC). J. Recept. Signal Transduct. Res., 2008, 28(6), 567-579.
[http://dx.doi.org/10.1080/10799890802517613] [PMID: 19061074]
[103]
Awasthi, B.P.; Mitra, K. In vitro leishmanicidal effects of the anti-fungal drug natamycin are mediated through disruption of calcium homeostasis and mitochondrial dysfunction. Apoptosis, 2018, 23(7-8), 420-435.
[http://dx.doi.org/10.1007/s10495-018-1468-5] [PMID: 29971703]
[104]
Pinto-Martinez, A.K.; Rodriguez-Durán, J.; Serrano-Martin, X.; Hernandez-Rodriguez, V.; Benaim, G. Mechanism of action of miltefosine on Leishmania donovani involves the im-pairment of acidocalcisome function and the activation of the sphingosine-dependent plasma membrane Ca(2+) channel. Antimicrob. Agents Chemother., 2017, 62(1), e01614-e01617.
[http://dx.doi.org/10.1128/AAC.01614-17] [PMID: 29061745]
[105]
Corral, M.J.; Benito-Peña, E.; Jiménez-Antón, M.D.; Cuevas, L.; Moreno-Bondi, M.C.; Alunda, J.M. Allicin induces calcium and mitochondrial dysregulation causing necrotic death in leishmania. PLoS Negl. Trop. Dis., 2016, 10(3), e0004525.
[http://dx.doi.org/10.1371/journal.pntd.0004525] [PMID: 27023069]
[106]
Zoukhri, D.; Hodges, R.R.; Dicker, D.M.; Dartt, D.A. Role of protein kinase C in cholinergic stimulation of lacrimal gland protein secretion. FEBS Lett., 1994, 351(1), 67-72.
[http://dx.doi.org/10.1016/0014-5793(94)00824-8] [PMID: 8076696]
[107]
Menda, S.A.; Lowry, E.A.; Porco, T.C.; Stamper, R.L.; Rubin, M.R.; Han, Y. Express outcomes using mitomycin-C, Ologen alone, Ologen with 5-fluorouracil. Int. Ophthalmol., 2015, 35(3), 357-363.
[http://dx.doi.org/10.1007/s10792-014-9955-3] [PMID: 24920197]
[108]
Chou, K.C. Impacts of bioinformatics to medicinal chemistry. Med. Chem., 2015, 11(3), 218-234.
[http://dx.doi.org/10.2174/1573406411666141229162834] [PMID: 25548930]
[109]
Xiao, X.; Min, J.L.; Lin, W.Z.; Liu, Z.; Cheng, X.; Chou, K.C. iDrug-Target: predicting the interactions between drug compounds and target proteins in cellular networking via benchmark dataset optimization approach. J. Biomol. Struct. Dyn., 2015, 33(10), 2221-2233.
[http://dx.doi.org/10.1080/07391102.2014.998710] [PMID: 25513722]
[110]
Jia, J.; Liu, Z.; Xiao, X.; Liu, B.; Chou, K.C. iPPI-Esml: an ensemble classifier for identifying the interactions of proteins by incorporating their physicochemical properties and wavelet transforms into PseAAC. J. Theor. Biol., 2015, 377, 47-56.
[http://dx.doi.org/10.1016/j.jtbi.2015.04.011] [PMID: 25908206]
[111]
Chou, K.C. Some remarks on protein attribute prediction and pseudo amino acid composition. J. Theor. Biol., 2011, 273(1), 236-247.
[http://dx.doi.org/10.1016/j.jtbi.2010.12.024] [PMID: 21168420]
[112]
Hussain, W.; Khan, Y.D.; Rasool, N.; Khan, S.A.; Chou, K.C. SPrenylC-PseAAC: A sequence-based model developed via Chou’s 5-steps rule and general PseAAC for identifying S-prenylation sites in proteins. J. Theor. Biol., 2019, 468, 1-11.
[http://dx.doi.org/10.1016/j.jtbi.2019.02.007] [PMID: 30768975]
[113]
Hussain, W.; Khan, Y.D.; Rasool, N.; Khan, S.A.; Chou, K.C. SPalmitoylC-PseAAC: A sequence-based model developed via Chou’s 5-steps rule and general PseAAC for identifying S-palmitoylation sites in proteins. Anal. Biochem., 2019, 568, 14-23.
[http://dx.doi.org/10.1016/j.ab.2018.12.019] [PMID: 30593778]

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