Dry eye disease as an inflammatory disorder

Ocular Immunology and Inflammation

Volumn 18, Issue 4, 2010, Pages 244-253

  Calonge, Margarita ^a   Enríquez De Salamanca, Amalia ^a   Diebold, Yolanda ^a   González Garca, María J ^a   Reinoso, Roberto ^a   Herreras, José M ^a   Corell, Alfredo ^a  

^a UNIVERSITY OF VALLADOLID   (Spain)

Author keywords

Cytokines; Dry eye disease; Inflammation; Lacrimal functional unit; Lymphocytes

Indexed keywords

CD23 ANTIGEN; CD40 ANTIGEN; CD40 LIGAND; CHEMOKINE RECEPTOR CCR5; HLA DR ANTIGEN; INTERCELLULAR ADHESION MOLECULE 1; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1;

CD3+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL INFILTRATION; CONJUNCTIVA; DISEASE ASSOCIATION; DISEASE CLASSIFICATION; DRY EYE; HUMAN; IMMUNOPATHOLOGY; INFLAMMATORY CELL; INFLAMMATORY DISEASE; LACRIMAL GLAND FUNCTION; LYMPHOCYTE COUNT; NONHUMAN; REVIEW; SCHIRMER TEST; SJOEGREN SYNDROME; STAINING;

ANIMALS; CATS; CHRONIC DISEASE; CONJUNCTIVA; CYTOKINES; DISEASE MODELS, ANIMAL; DOGS; DRY EYE SYNDROMES; EYE; FEMALE; HUMANS; INFLAMMATION; MALE; RABBITS; TEARS;

EID: 77954940219     PISSN: 09273948     EISSN: 17445078     Source Type: Journal    
DOI: 10.3109/09273941003721926     Document Type: Review

References (107)

1. The epidemiology of dry eye disease: report of the Epidemiology Subcommittee of the International Dry Eye WorkShop (2007). Ocul Surf. 2007;5:93-107.
2. McCarty CA, Bansal AK, Livingston PM, Stanislavsky YL, Taylor HR. The epidemiology of dry eye in Melbourne, Australia. Ophthalmology. 1998;105:1114-1119.
3. Schaumberg DA, Sullivan DA, Buring JE, Dana MR. Prevalence of dry eye syndrome among US women. Am J Ophthalmol. 2003;136:318-326.
4. Schaumberg DA, Dana R, Buring JE, Sullivan DA. Prevalence of dry eye disease among US men: estimates from the Physicians' Health Studies. Arch Ophthalmol. 2009;127:763-768.
5. Sjögren H, Bloch KJ. Keratoconjunctivitis sicca and the Sjögren syndrome. Surv Ophthalmol. 1971;16:145-159.
6. Tseng SC, Tsubota K. Important concepts for treating ocular surface and tear disorders. Am J Ophthalmol. 1997;124:825-835.
7. Behrens A, Doyle JJ, Stern L et al. Dysfunctional tear syndrome: a Delphi approach to treatment recommendations. Cornea. 2006;25:900-907.
8. Niederkorn JY, Stern ME, Pflugfelder SC et al. Desiccating stress induces T cell-mediated Sjogren's Syndrome-like lacrimal keratoconjunctivitis. J Immunol. 2006;176:3950-3957.
9. Yoon KC, De Paiva CS, Qi H, et al. Desiccating environmental stress exacerbates autoimmune lacrimal keratoconjunctivitis in non-obese diabetic mice. J Autoimmun. 2008;30:212-221.
10. Holly FJ, Lemp MA. Tear physiology and dry eyes. Surv Ophthalmol. 1977;22:69-87.
11. Dilly PN. Structure and function of the tear film. Adv Exp Med Biol. 1994;350:239-247.
12. Lemp MA. Report of the National Eye Institute/Industry workshop on Clinical Trials in Dry Eyes. CLAO J. 1995;21:221-232.
13. The definition and classification of dry eye disease: report of the Definition and Classification Subcommittee of the International Dry Eye WorkShop (2007). Ocul Surf. 2007;5:75-92.
14. Methodologies to diagnose and monitor dry eye disease: report of the Diagnostic Methodology Subcommittee of the Internacional Dry Eye WorkShop (2007). Ocul Surf. 2007;5:108-152.
15. Driver PJ, Lemp MA. Meibomian gland dysfunction. Surv Ophthalmol. 1996;40:343-367.
16. Herreras JM, Perez S, Perez H, Calonge M, Pastor JC. Influence of topical anesthesia on tests diagnostic of blepharitis- associated dry eye syndrome. Ocul Immunol Inflamm. 1997;5:33-41.
17. Shimazaki J, Goto E, Ono M, Shimmura S, Tsubota K. Meibomian gland dysfunction in patients with Sjogren syndrome. Ophthalmology. 1998;105:1485-1488.
18. Thoft RA, Friend J. Biochemical transformation of regenerating ocular surface epithelium. Invest Ophthalmol Vis Sci. 1977;16:14-20.
19. Stern ME, Beuerman RW, Fox RI, Gao J, Mircheff AK, Pflugfelder SC. The pathology of dry eye: the interaction between the ocular surface and lacrimal glands. Cornea. 1998;17:584-589.
20. Pflugfelder S, Stern ME, Beuerman RW. Dysfunction of the lacrimal functional unit and its impact on tear film stability and composition. In: Pflugfelder SC, Beuerman RW, Stern ME (eds), Dry Eye and Ocular Surface Disorders. New York: Marcel Dekker; 2004:63-68.
21. Barabino S, Dana MR. Animal models of dry eye: a critical assessment of opportunities and limitations. Invest Ophthalmol Vis Sci. 2004;45:1641-1646. (Pubitemid 38868954)
22. Schrader S, Mircheff AK, Geerling G. Animal models of dry eye. Dev Ophthalmol. 2008;41:298-312.
23. Gao J, Schwalb TA, Addeo JV, Ghosn CR, Stern ME. The role of apoptosis in the pathogenesis of canine keratoconjunctivitis sicca: the effect of topical Cyclosporin A therapy. Cornea. 1998;17:654-663.
24. Hicks SJ, Corfield AP, Kaswan RL, et al. Biochemical analysis of ocular surface mucin abnormalities in dry eye: the canine model. Exp Eye Res. 1998;67:709-718.
25. Kaswan RL, Salisbury MA, Ward DA. Spontaneous canine keratoconjunctivitis sicca: a useful model for human keratoconjunctivitis sicca: treatment with cyclosporine eye drops. Arch Ophthalmol. 1989;107:1210-1216.
26. Moore CP, McHugh JB, Thorne JG, Phillips TE. Effect of cyclosporine on conjunctival mucin in a canine keratoconjunctivitis sicca model. Invest Ophthalmol Vis Sci. 2001;42:653-659.
27. Zhu Z, Stevenson D, Schechter JE, Mircheff AK, Atkinson R, Trousdale MD. Lacrimal histopathology and ocular surface disease in a rabbit model of autoimmune dacryoadenitis. Cornea. 2003;22:25-32.
28. Toshida H, Nguyen DH, Beuerman RW, Murakami A. Evaluation of novel dry eye model: preganglionic parasympathetic denervation in rabbit. Invest Ophthalmol Vis Sci. 2007;48:4468-4475.
29. Toshida H, Nguyen DH, Beuerman RW, Murakami A. Neurologic evaluation of acute lacrimomimetic effect of cyclosporine in an experimental rabbit dry eye model. Invest Ophthalmol Vis Sci. 2009;50:2736-2741.
30. Dartt DA. Regulation of mucin and fluid secretion by conjunctival epithelial cells. Prog Retin Eye Res. 2002;21:555-576.
31. Choy EP, Cho P, Benzie IF, Choy CK. Dry eye and blink rate simulation with a pig eye model. Optom Vis Sci. 2008;85:129-134.
32. Choy EP, Cho P, Benzie IF, Choy CK, To TS. A novel porcine dry eye model system (pDEM) with simulated lacrimation/blinking system: preliminary findings on system variability and effect of corneal drying. Curr Eye Res. 2004;28:319-325.
33. Fujihara T, Murakami T, Fujita H, Nakamura M, Nakata K. Improvement of corneal barrier function by the P2Y(2) agonist INS365 in a rat dry eye model. Invest Ophthalmol Vis Sci. 2001;42:96-100.
34. Nakamura S, Shibuya M, Saito Y, et al. Protective effect of d-beta- hydroxybutyrate on corneal epithelia in dry eye conditions through suppression of apoptosis. Invest Ophthalmol Vis Sci. 2003;44:4682-4688.
35. Nakamura S, Shibuya M, Nakashima H, Imagawa T, Uehara M, Tsubota K. D- Beta-hydroxybutyrate protects against corneal epithelial disorders in a rat dry eye model with jogging board. Invest Ophthalmol Vis Sci. 2005;46:2379-2387.
36. Higuchi A, Ueno R, Shimmura S, Suematsu M, Dogru M, Tsubota K. Albumin rescues ocular epithelial cells from cell death in dry eye. Curr Eye Res. 2007;32:83-88.
37. Chen W, Zhao K, Li X, Yoshitomi T. Keratoconjunctivitis sicca modifies epithelial stem cell proliferation kinetics in conjunctiva. Cornea. 2007;26:1101-1106.
38. Viau S, Maire MA, Pasquis B, et al. Time course of ocular surface and lacrimal gland changes in a new scopolamineinduced dry eye model. Graefes Arch Clin Exp Ophthalmol. 2008;246:857-867.
39. Nakamura S, Shibuya M, Nakashima H, et al. Involvement of oxidative stress on corneal epithelial alterations in a blink-suppressed dry eye. Invest Ophthalmol Vis Sci. 2007;48:1552-1558.
40. Jabs DA, Alexander EL, Green WR. Ocular inflammation in autoimmune MRL/Mp mice. Invest Ophthalmol Vis Sci. 1985;26:1223-1229.
41. Haneji N, Nakamura T, Takio K, et al. Identification of alpha-fodrin as a candidate autoantigen in primary Sjogren's syndrome. Science. 1997;276:604-607.
42. Hu Y, Nakagawa Y, Purushotham KR, Humphreys-Beher MG. Functional changes in salivary glands of autoimmune disease-prone NOD mice. Am J Physiol. 1992;263: E607-E614.
43. Dursun D, Wang M, Monroy D, et al. A mouse model of keratoconjunctivitis sicca. Invest Ophthalmol Vis Sci. 2002;43:632-638.
44. Barabino S, Shen L, Chen L, Rashid S, Rolando M, Dana MR. The controlled- environment chamber: a new mouse model of dry eye. Invest Ophthalmol Vis Sci. 2005;46: 2766-2771.
45. Chen W, Zhang X, Zhang J, et al. A murine model of dry eye induced by an intelligently controlled environmental system. Invest Ophthalmol Vis Sci. 2008;49:1386-1391.
46. González-García MJ, González-Sáiz A, de la Fuente B, et al. Exposure to a controlled adverse environment impairs the ocular surface of subjects with minimally symptomatic dry eye. Invest Ophthalmol Vis Sci. 2007;48:4026-4032.
47. Yeh S, Song XJ, Farley W, Li DQ, Stern ME, Pflugfelder SC. Apoptosis of ocular surface cells in experimentally induced dry eye. Invest Ophthalmol Vis Sci. 2003;44:124-129.
48. Corrales RM, Stern ME, De Paiva CS, Welch J, Li DQ, Pflugfelder SC. Desiccating stress stimulates expression of matrix metalloproteinases by the corneal epithelium. Invest Ophthalmol Vis Sci. 2006;47:3293-3302.
49. De Paiva CS, Corrales RM, Villarreal AL, et al. Apical corneal barrier disruption in experimental murine dry eye is abrogated by methylprednisolone and doxycycline. Invest Ophthalmol Vis Sci. 2006;47:2847-2856.
50. Luo L, Li DQ, Doshi A, Farley W, Corrales RM, Pflugfelder SC. Experimental dry eye stimulates production of inflammatory cytokines and MMP-9 and activates MAPK signaling pathways on the ocular surface. Invest Ophthalmol Vis Sci. 2004;45:4293-4301.
51. Strong B, Farley W, Stern ME, Pflugfelder SC. Topical cyclosporine inhibits conjunctival epithelial apoptosis in experimental murine keratoconjunctivitis sicca. Cornea. 2005;24:80-85.
52. Corrales RM, Villarreal A, Farley W, Stern ME, Li DQ, Pflugfelder SC. Strain- related cytokine profiles on the murine ocular surface in response to desiccating stress. Cornea. 2007;26:579-584.
53. De Paiva CS, Corrales RM, Villarreal AL, et al. Corticosteroid and doxycycline suppress MMP-9 and inflammatory cytokine expression, MAPK activation in the corneal epithelium in experimental dry eye. Exp Eye Res. 2006;83:526-535.
54. De Paiva CS, Villarreal AL, Corrales RM, et al. Dry eyeinduced conjunctival epithelial squamous metaplasia is modulated by interferon-gamma. Invest Ophthalmol Vis Sci. 2007;48:2553-2560.
55. Barabino S, Rolando M, Chen L, Dana MR. Exposure to a dry environment induces strain-specific responses in mice. Exp Eye Res. 2007;84:973-977.
56. Narayanan S, Corrales RM, Farley W, McDermott AM, Pflugfelder SC. Interleukin-1 receptor-1-deficient mice show attenuated production of ocular surface inflammatory cytokines in experimental dry eye. Cornea. 2008;27: 811-817.
57. Beardsley RM, De Paiva CS, Power DF, Pflugfelder SC. Desiccating stress decreases apical corneal epithelial cell size-modulation by the metalloproteinase inhibitor doxycycline. Cornea. 2008;27:935-940.
58. Ecoiffier T, El AJ, Rashid S, Schaumberg D, Dana R. Modulation of integrin alpha4beta1 (VLA-4) in dry eye disease. Arch Ophthalmol. 2008;126:1695-1699.
59. Siemasko KF, Gao J, Calder VL, et al. In vitro expanded CD4+CD25+Foxp3+ regulatory T cells maintain a normal phenotype and suppress immune-mediated ocular surface inflammation. Invest Ophthalmol Vis Sci. 2008;49:5434-5440.
60. De Paiva CS, Chotikavanich S, Pangelinan SB, et al. IL-17 disrupts corneal barrier following desiccating stress. Mucosal Immunol. 2009;2:243-253.
61. El Annan J., Chauhan SK, Ecoiffier T, Zhang Q, Saban DR, Dana R. Characterization of effector T cells in dry eye disease. Invest Ophthalmol Vis Sci. 2009;50:3802-3807.
62. Chauhan SK, El AJ, Ecoiffier T ,et al. Autoimmunity in dry eye is due to resistance of Th17 to Treg suppression. J Immunol. 2009;182:1247-1252.
63. Rashid S, Jin Y, Ecoiffier T, Barabino S, Schaumberg DA, Dana MR. Topical omega-3 and omega-6 fatty acids for treatment of dry eye. Arch Ophthalmol. 2008;126: 219-225.
64. Goyal S, Chauhan SK, Zhang Q, Dana R. Amelioration of murine dry eye disease by topical antagonist to chemokine receptor 2. Arch Ophthalmol. 2009;127:882-887.
65. Nyunt AK, Ishida Y, Yu Y, Shimada S. Topical apolipoprotein A-1 may have a beneficial effect on the corneal epithelium in a mouse model of dry eye: a pilot study. Eye Contact Lens. 2008;34:287-292.
66. Lekhanont K, Leyngold IM, Suwan-Apichon O, Rangsin R, Chuck RS. Comparison of topical dry eye medications for the treatment of keratoconjunctivitis sicca in a botulinum toxin B-induced mouse model. Cornea. 2007;26:84-89. (Pubitemid 46041569)
67. Park CY, Zhuang W, Lekhanont K, et al. Lacrimal gland inflammatory cytokine gene expression in the botulinum toxin B-induced murine dry eye model. Mol Vis. 2007;13:2222-2232.
68. Hongyok T, Chae JJ, Shin YJ, Na D, Li L, Chuck RS. Effect of chitosan-N- acetylcysteine conjugate in a mouse model of botulinum toxin B-induced dry eye. Arch Ophthalmol. 2009;127:525-532.
69. Zhu L, Shen J, Zhang C, et al. Inflammatory cytokine expression on the ocular surface in the Botulium toxin B induced murine dry eye model. Mol Vis. 2009;15:250-258.
70. Williamson J, Gibson AA, Wilson T, Forrester JV, Whaley K, Dick WC. Histology of the lacrimal gland in keratoconjunctivitis sicca. Br J Ophthalmol. 1973;57:852-858.
71. Pflugfelder SC, Huang AJ, Feuer W, Chuchovski PT, Pereira IC, Tseng SC. Conjunctival cytologic features of primary Sjogren's syndrome. Ophthalmology. 1990;97: 985-991.
72. Power WJ, Mullaney P, Farrell M, Collum LM. Effect of topical cyclosporin A on conjunctival T cells in patients with secondary Sjogren's syndrome. Cornea. 1993;12: 507-511.
73. Tsubota K, Fujihara T, Saito K, Takeuchi T. Conjunctival epithelium expression of HLA-DR in dry eye patients. Ophthalmologica. 1999;213:16-19.
74. Kunert KS, Tisdale AS, Stern ME, Smith JA, Gipson IK. Analysis of topical cyclosporine treatment of patients with dry eye syndrome: effect on conjunctival lymphocytes. Arch Ophthalmol. 2000;118:1489-1496.
75. Brignole F, Pisella PJ, Goldschild M, De Saint JM, Goguel A, Baudouin C. Flow cytometric analysis of inflammatory markers in conjunctival epithelial cells of patients with dry eyes. Invest Ophthalmol Vis Sci. 2000;41:1356-1363.
76. Albietz JM. Dry eye: an update on clinical diagnosis, management and promising new treatments. Clin Exp Optom. 2001;84:4-18.
77. Stern ME, Gao J, Schwalb TA, et al. Conjunctival T-cell subpopulations in Sjogren's and non-Sjogren's patients with dry eye. Invest Ophthalmol Vis Sci. 2002;43:2609-2614.
78. Baudouin C, Liang H, Bremond-Gignac D, et al. CCR 4 and CCR 5 expression in conjunctival specimens as differential markers of T(H)1/ T(H)2 in ocular surface disorders. J Allergy Clin Immunol. 2005;116:614-619.
79. Rolando M, Barabino S, Mingari C, Moretti S, Giuffrida S, Calabria G. Distribution of conjunctival HLA-DR expression and the pathogenesis of damage in early dry eyes. Cornea. 2005;24:951-954.
80. Gulati A, Sacchetti M, Bonini S, Dana R. Chemokine receptor CCR5 expression in conjunctival epithelium of patients with dry eye syndrome. Arch Ophthalmol. 2006;124:710-716.
81. Sullivan DA, Wickham LA, Rocha EM et al. Androgens and dry eye in Sjogren's syndrome. Ann N Y Acad Sci. 1999;876:312-324.
82. Stern ME, Beuerman RW, Fox RI, Gao J, Mircheff AK, Pflugfelder SC. A unified theory of the role of the ocular surface in dry eye. Adv Exp Med Biol. 1998;438:643-651.
83. Stern ME, Gao J, Siemasko KF, Beuerman RW, Pflugfelder SC. The role of the lacrimal functional unit in the pathophysiology of dry eye. Exp Eye Res. 2004;78:409-416.
84. Baudouin C. The pathology of dry eye. Surv Ophthalmol. 2001;45 (Suppl 2):S211-S220.
85. Baudouin C, Liang H. Amplifying factors in ocular surface diseases: apoptosis. Ocul Surf. 2005;3:S194-S197.
86. Beuerman RW, Stern ME. Neurogenic inflammation: a first line of defense for the ocular surface. Ocul Surf. 2005;3:S203-S206.
87. Bron AJ. Diagnosis of dry eye. Surv Ophthalmol. 2001;45 (Suppl 2):S221-S226.
88. Calonge M. The treatment of dry eye. Surv Ophthalmol. 2001;45 (Suppl 2):S227-S239.
89. De Paiva CS, Pflugfelder SC. Rationale for anti-inflammatory therapy in dry eye syndrome. Arq Bras Oftalmol. 2008;71:89-95.
90. Gumus K, Cavanagh DH. The role of inflammation and antiinflammation therapies in keratoconjunctivitis sicca. Clin Ophthalmol. 2009;3:57-67.
91. Latkany R. Dry eyes: etiology and management. Curr Opin Ophthalmol. 2008;19:287-291.
92. Lemp MA. Advances in understanding and managing dry eye disease. Am J Ophthalmol. 2008;146:350-356.
93. Pflugfelder SC, De Paiva CS, Tong L, Luo L, Stern ME, Li DQ. Stress-activated protein kinase signaling pathways in dry eye and ocular surface disease. Ocul Surf. 2005;3:S154-S157.
94. Pflugfelder SC, De Paiva CS, Li DQ, Stern ME. Epithelialimmune cell interaction in dry eye. Cornea. 2008;27(Suppl 1):S9-S11.
95. Martinez-Osorio H, Calonge M, Corell A, et al. Characterization and short-term culture of cells recovered from human conjunctival epithelium by minimally invasive means. Mol Vis. 2009;15:2185-2195.
96. Dinarello CA. Historical insights into cytokines. Eur J Immunol. 2007;37(Suppl 1):S34-S45.
97. Enríquez-de-Salamanca A, Calonge M. Cytokines and chemokines in immune- based ocular surface inflammation. Expert Rev Clin Immunol. 2008;4:457-467.
98. Enriquez-de-Salamanca A, Calder V, Gao J, et al. Cytokine responses by conjunctival epithelial cells: an in vitro model of ocular inflammation. Cytokine. 2008;44: 160-167.
99. Zhan H, Towler HM, Calder VL. The immunomodulatory role of human conjunctival epithelial cells. Invest Ophthalmol Vis Sci. 2003;44:3906-3910.
100. Mitsias DI, Kapsogeorgou EK, Moutsopoulos HM. The role of epithelial cells in the initiation and perpetuation of autoimmune lesions: lessons from Sjogren's syndrome (autoimmune epithelitis). Lupus. 2006;15:255-261.
101. Tishler M, Yaron I, Geyer O, Shirazi I, Naftaliev E, Yaron M. Elevated tear interleukin-6 levels in patients with Sjogren syndrome. Ophthalmology. 1998;105:2327-2329. (Pubitemid 30191679)
102. Pflugfelder SC, Jones D, Ji Z, Afonso A, Monroy D. Altered cytokine balance in the tear fluid and conjunctiva of patients with Sjogren's syndrome keratoconjunctivitis sicca. Curr Eye Res. 1999;19:201-211.
103. Solomon A, Dursun D, Liu Z, Xie Y, Macri A, Pflugfelder SC. Pro- and anti- inflammatory forms of interleukin-1 in the tear fluid and conjunctiva of patients with dry-eye disease. Invest Ophthalmol Vis Sci. 2001;42:2283-2292.
104. Yoon KC, Jeong IY, Park YG, Yang SY. Interleukin-6 and tumor necrosis factor-alpha levels in tears of patients with dry eye syndrome. Cornea. 2007;26:431-437.
105. Lam H, Bleiden L, De Paiva CS, Farley W, Stern ME, Pflugfelder SC. Tear cytokine profiles in dysfunctional tear syndrome. Am J Ophthalmol. 2009;147:198-205.
106. Chotikavanich S, De Paiva CS, Li dQ, et al. Production and activity of matrix metalloproteinase-9 on the ocular surface increase in dysfunctional tear syndrome. Invest Ophthalmol Vis Sci. 2009;50:3203-3209.
107. Chen D, Wei Y, Li X, Epstein S, Wolosin JM, Asbell P. sPLA2-IIa is an inflammatory mediator when the ocular surface is compromised. Exp Eye Res. 2009;88:880-888.