Differential cell proliferation, apoptosis, and immune response in healthy and evaporative-type dry eye conjunctival epithelia

Investigative Ophthalmology and Visual Science

Volumn 52, Issue 7, 2011, Pages 4819-4828

  Reinoso, Roberto ^a,b   Calonge, Margarita ^a,b   Castellanos, Evangelina ^a   Martino, Mario ^a,b   Fernández, Itziar ^a,b   Stern, Michael E ^c   Corell, Alfredo ^a,b  

^a UNIVERSITY OF VALLADOLID   (Spain)

^b BIOMATERIALES Y NANOMEDICINA CIBER BBN   (Spain)

^c ALLERGAN INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTIFICIAL TEAR; CD16 ANTIGEN; CD19 ANTIGEN; CD3 ANTIGEN; CD4 ANTIGEN; CD45 ANTIGEN; CD56 ANTIGEN; CD8 ANTIGEN; DEXAFREE; DEXAMETHASONE; UNCLASSIFIED DRUG; VISCOFRESH;

ADULT; AGED; APOPTOSIS; ARTICLE; B LYMPHOCYTE; CD4 CD8 RATIO; CELL CYCLE; CELL LINEAGE; CELL PROLIFERATION; CELL VIABILITY; CLINICAL ARTICLE; CLINICAL FEATURE; CONJUNCTIVA EPITHELIUM; CONTROLLED STUDY; CYTOLOGY; DRY EYE; FEMALE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HYGIENE; IMMUNE RESPONSE; IMMUNOPHENOTYPING; LYMPHOCYTE; MALE; NATURAL KILLER T CELL; PRIORITY JOURNAL; QUESTIONNAIRE; T LYMPHOCYTE; CELLULAR IMMUNITY; COMPARATIVE STUDY; CONJUNCTIVA; EPITHELIUM CELL; FOLLOW UP; IMMUNOLOGY; MIDDLE AGED; PATHOLOGY; PROSPECTIVE STUDY;

ADULT; AGED; APOPTOSIS; CELL CYCLE; CELL PROLIFERATION; CONJUNCTIVA; DRY EYE SYNDROMES; EPITHELIAL CELLS; FEMALE; FLOW CYTOMETRY; FOLLOW-UP STUDIES; HUMANS; IMMUNITY, CELLULAR; MALE; MIDDLE AGED; PROSPECTIVE STUDIES;

EID: 80052356463     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.10-6073     Document Type: Article

References (82)

1. Stern ME, Gao J, Siemasko KF, Beuerman RW, Pflugfelder SC. The role of lacrimal functional unit in the pathophysiology of dry eye. Exp Eye Res. 2004;78:409-416.
2. Dry Eye WorkShop (DEWS). The definition and classification of dry eye disease: report of the definition and classification. Ocul Surf. 2007;5:75-92.
3. Lemp MA, Nichols KK. Blepharitis in the United States 2009: a survey-based perspective on prevalence and treatment. Ocul Surf. 2009;7(suppl):S1-S14.
4. Dry Eye WorkShop (DEWS). Methodologies to diagnose and monitor dry eye disease: report of the diagnostic methodology. Ocul Surf. 2007;5:108-152.
5. McCulley JP, Shine WE. Meibomian gland function and the tear lipid layer. Ocul Surf. 2003;1:97-106.
6. Foulks G, Bron AJ. meibomian gland dysfunction: a clinical scheme for description, diagnosis, classification, and grading. Ocul Surf. 2003;1:107-126.
7. Bron AJ, Tiffany JM. The contribution of meibomian disease to dry eye. Cornea. 2004;2:149-165.
8. Begley CG, Chalmers RL, Abetz L, et al. The relationship between habitual patient-reported symptoms and clinical signs among patients with dry eye of varying severity. Invest Ophthalmol Vis Sci. 2003;44:4753-4761.
9. Nichols KK, Nichols JJ, Mitchell GL. The lack of association between signs and symptoms in patients with dry eye disease. Cornea. 2004;23:762-770.
10. Moore JE, Graham JE, Goodall EA, et al. Concordance between common dry eye diagnostic tests. Br J Ophthalmol. 2009;93:66-72.
11. Brignole F, Pisella PJ, Goldschild M, De Saint Jean M, 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.
12. Pisella PJ, Brignole F, Debbasch C, et al. Flow cytometric analysis of conjunctival epithelium in ocular rosacea and keratoconjunctivitis sicca. Ophthalmology. 2000;107:1841-1849.
13. Baudouin C. The pathology of dry eye. Surv Ophthalmol. 2001;45:S211-S220.
14. 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.
15. Pflugfelder SC, De Paiva CS, Li DQ, Stern ME. Epithelial-immune cell interaction in dry eye. Cornea. 2008;27:S9-S11.
16. El Annan J, Chauchan 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.
17. Pflugfelder SC, Huang AJ, Feuer W, Chuchovski PT, Pereira IC, Tseng SC. Conjunctival cytologic features of primary Sjögren syndrome. Ophthalmology. 1990;97:985-991.
18. Power WJ, Mullaney P, Farrel M, Collum LM. Effect of topical cyclosporine A on conjunctival T cells in patients with secondary Sjögren's syndrome. Cornea. 1993;12:507-511.
19. Brignole F, De Saint-Jean M, Goldschild M, Becquet F, Goguel A, Baudouin C. Expression of Fas-Fas ligand antigens and apoptotic marker APO2.7 by the human conjunctival epithelium: positive correlation with class II HLA DR expression in inflammatory ocular surface disorders. Exp Eye Res. 1998;67:687-697.
20. Bourcier T, De Saint Jean M, Brignole F, Goguel A, Baudouin C. Expression of CD40 and CD40 ligand in the human conjunctival epithelium. Invest Ophthalmol Vis Sci. 2000;41:120-126.
21. 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.
22. Stern ME, Gao J, Schwalb TA, et al. Conjunctival T-cell subpopulations in Sjögren's and non-Sjögren's patients with dry eye. Invest Ophthalmol Vis Sci. 2002;43:2609-2614.
23. H2 in ocular surface disorders. J Allergy Clin Immunol. 2005;116:614-619.
24. 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.
25. Sall K, Stevenson OD, Mundorf TK, Reis BL. Two multicenter, randomized studies of the efficacy and safety of cyclosporine ophthalmic emulsion in moderate to severe dry eye disease: CsA Phase 3 Study Group. Ophthalmology. 2000;107:631-639.
26. Brignole F, Pisella PJ, De Saint Jean M, Goldschild M, Goguel A, Baudouin C. Flow cytometric analysis of inflammatory markers in KCS: 6-month treatment with topical cyclosporine A. Invest Ophthalmol Vis Sci. 2001;42:90-95.
27. Pflugfelder SC, Maskin SL, Anderson B, et al. A randomized, doublemasked, placebo-controlled, multicenter comparison of loteprednol etabonate ophthalmic suspension, 0.5%, and placebo for treatment of keratoconjunctivitis sicca in patients with delayed tear clearance. Am J Ophthalmol. 2004;138:444-457.
28. Yoo SE, Lee DC, Chang MH. The effect of low-dose doxycycline therapy in chronic meibomian gland dysfunction. Korean J Ophthalmol. 2005;19:258-263.
29. De Paiva CS, Pflugfelder SC. Rationale for anti-inflammatory therapy in dry eye syndrome. Arq Bras Oftalmol. 2008;71:89-95.
30. Gulati A, Sullivan R, Buring JE, Sullivan DA, Dana R, Schaumberg DA. Validation and repeatability of a short questionnaire for dry eye syndrome. Am J Ophthalmol. 2006;142:125-131.
31. 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.
32. Schaumberg DA, Gulati A, Mathers WD, et al. Development and validation of a short global dry eye symptom index. Ocul Surf. 2007;5:50-57.
33. McCulley JP, Dougherty JM, Deneau DG. Classification of chronic blepharitis. Ophthalmology. 1982;89:1173-1180.
34. van Bijsterveld OP. Diagnostic tests in the sicca syndrome. Arch Ophthalmol. 1969;82:10-14.
35. Lemp MA. Report of the National Eye Institute/Industry Workshop on Clinical Trials in Dry Eyes. CLAO J. 1995;21:221-232.
36. Bron AJ, Evans VE, Smith JA. Grading of corneal and conjunctival staining in the context of other dry eye tests. Cornea. 2003;22:640-650.
37. Bron AJ, Yokoi N, Gafney E, Tiffany JM. Predicted phenotypes of dry eye: proposed consequences of its natural history. Ocul Surf. 2009;7:78-92.
38. Efron N. Grading scales for contact lens complications. Ophthalmic Physiol Opt. 1998;18:182-186.
39. Oguz H, Yokoi N, Kinoshita S. The height and radius of the tear meniscus and methods for examining these parameters. Cornea. 2000;19:497-500.
40. Sakamoto R, Bennett ES, Henry VA, et al. The phenol red thread tear test: a cross-cultural study. Invest Ophthalmol Vis Sci. 1993;34:3510-3514.
41. DeLuise VP, Tabbara KF. Quantitation of tear lysozyme levels in dry-eye disorders. Arch Ophthalmol. 1983;101:634-635.
42. Fujihara T, Takeuchi T, Saito K, Kitajima Y, Kobayashi TK, Tsubota K. Evaluation of human conjunctival epithelium by a combination of brush cytology and flow cytometry: an approach to the quantitative technique. Diagn Cytopathol. 1997;17:456-460.
43. Tsubota K, Fukagawa K, Fujihara T, et al. Regulation of human leukocyte antigen expression in human conjunctival epithelium. Invest Ophthalmol Vis Sci. 1999;40:28-34.
44. Martínez-Osorio H, Calonge M, Corell A, et al. Characterization and short-term culture of cells recovered from human conjunctival epithelium by brush cytology. Mol Vis. 2009;15:2185-2195.
45. Nagata T, Suzuki H, Ishigami N, et al. Development of apoptosis and changes in lymphocyte subsets in thymus, mesenteric lymph nodes and Peyer's patches of mice orally inoculated with T-2 toxin. Exp Toxicol Pathol. 2001;53:309-315.
46. Schwarz E, Saalmüller A, Gerner W, Claus R. Intraepithelial but not lamina propria lymphocytes in the porcine gut are affected by dexamethasone treatment. Vet Immunol Immunopathol. 2005;105:125-139.
47. Jeklova E, Leva L, Jaglic Z, Faldyna M. Dexamethasone-induced immunosuppression: a rabbit model. Vet Immunol Immunopathol. 2008;122:231-240.
48. Torres KC, Antonelli LR, Souza AL, Teixeira MM, Dutra WO, Gollob KJ. Norepinephrine, dopamine and dexamethasone modulate discrete leukocyte subpopulations and cytokine profiles from human PBMC. J Neuroimmunol. 2005;166:144-157.
49. Totino PR, Riccio EK, Corte-Real S, Daniel-Ribeiro CT, Ferreira-da-Cruza MF. Dexamethasone has pro-apoptotic effects on nonactivated fresh peripheral blood mononuclear cells. Cell Biol Int. 2006;30:133-137.
50. Kunisawa J, Takahashi I, Kiyono H. Intraepithelial lymphocytes: their shared and divergent immunological behaviors in the small and large intestine. Immunol Rev. 2007;215:136-153.
51. Cheroutre H. IELs: enforcing law and order in the court of the intestinal epithelium. Immunol Rev. 2005;206:114-131.
52. Ishikawa H, Naito T, Iwanaga T, et al. Curriculum vitae of intestinal intraepithelial T cells: their developmental and behavioral characteristics. Immunol Rev. 2007;215:154-165.
53. Hingorani M, Metz D, Lightman SL. Characterisation of the normal conjunctival leukocyte population. Exp Eye Res. 1997;64:905-912.
54. Knop N, Knop E. Conjunctiva-associated lymphoid tissue in the human eye. Invest Ophthalmol Vis Sci. 2000;41:1270-1279.
55. Pflugfelder SC, Stern ME. Symposium participants: immunoregulation on the ocular surface: 2nd Cullen Symposium. Ocul Surf. 2009;7:67-77.
56. Knop E, Knop N. The role of eye-associated lymphoid tissue in corneal immune protection. J Anat. 2005;206:271-285.
57. Chang JH, Amankwah R, Robins RA, Gray T, Dua HS. Kinetics of immune cell migration at the human ocular surface. Br J Ophthalmol. 2008;92:970-975.
58. + regulatory T cells maintain a normal phenotype and suppress immune-mediated ocular surface inflammation. Invest Ophthalmol Vis Sci. 2008;49:5434-5440.
59. Chauhan SK, El Annan J, Ecoiffier T, et al. Autoimmunity in dry eye is due to resistance of Th17 to Treg suppression. J immunol. 2009;182:1247-1252.
60. Fujihara T, Takeuchi T, Saito K, Tsubota K. Flow cytometric analysis of surface antigens on human conjunctival epithelial cells. Ophthalmic Res. 1997;29:103-109.
61. Yagmur M, Ersöz C, Ersöz TR, Varinli S. Brush technique in ocular surface cytology. Diagn Cytopathol. 1997;17:88-91.
62. Avunduk AM, Avunduk MC, Varnell ED, Kaufman HE. The comparison of efficacies of topical corticosteroids and nonsteroidal anti-inflammatory drops on dry eye patients: a clinical and immunocytochemical study. Am J Ophthalmol. 2003;136:593-602.
63. Marsh P, Pflugfelder SC. Topical nonpreserved methylprednisolone therapy for keratoconjunctivitis sicca in Sjögren syndrome. Ophthalmology. 1999;106:811-816.
64. Sainz de la Maza Serra M, Simón Castellvi C, Kabbani O. Nonpreserved topical steroids and lacrimal punctal occlusion for severe keratoconjunctivitis sicca. Arch Soc Esp Oftalmol. 2000;75:751-756.
65. Niederkorn JY, Stern ME, Pflugfelder SC, et al. Desiccating stress induces T cell-mediated Sjögren's syndrome-like lacrimal keratoconjunctivitis. J Immunol. 2006;176:3950-3957.
66. 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.
67. 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.
68. Efron N, Al-Dossari M, Pritchard N. In vivo confocal microscopy of the palpebral conjunctiva and tarsal plate. Optom Vis Sci. 2009;86:E1303-E1308.
69. Efron N, Al-Dossari M, Pritchard N. In vivo confocal microscopy of the bulbar conjunctiva. Clin Exp Ophthalmol. 2009;37:335-344.
70. Gasset AR, Ishii Y, Kaufman HE, Miller T. Cytotoxicity of ophthalmic preservatives. Am J Ophthalmol. 1974;78:98-105.
71. Burstein NL. Corneal cytotoxicity of topically applied drugs, vehicles and preservatives. Surv Ophthalmol. 1980;25:15-30.
72. Pflugfelder SC, Jones D, Ji Z, Afonso A, Monroy D. Altered cytokine balance in the tear fluid and conjunctiva of patients with Sjögren's syndrome keratoconjunctivitis sicca. Curr Eye Res. 1999;19:201-211.
73. 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.
74. Fabiani C, Barabino S, Rashid S, Dana MR. Corneal epithelial proliferation and thickness in a mouse model of dry eye. Exp Eye Res. 2009;89:166-171.
75. Jones DT, Monroy D, Ji Z, Pflugfelder SC. Alterations of ocular surface gene expression in Sjögren's syndrome. Adv Exp Med Biol. 1998;438:533-536.
76. Kunert KS, Tisdale AS, Gipson IK. Goblet cell numbers and epithelial proliferation in the conjunctiva of patients with dry eye syndrome treated with cyclosporine. Arch Ophthalmol. 2002;120:330-337.
77. Walker RA, Camplejohn RS. Comparison of monocolonal antibody Ki-67 reactivity with grade and DNA flow cytometry of breast carcinomas. Br J Cancer. 1988;57:281-283.
78. Stanton KJ, Sidner RA, Miller GA, et al. Analysis of Ki-67 antigen expression, DNA proliferative fraction, and survival in resected cancer of the pancreas. Am J Surg. 2003;186:486-492.
79. Brown DC, Gatter KC. Ki67 protein: the immaculate deception? Histopathology. 2002;40:2-11.
80. Scholzen T, Gerdes J. The Ki-67 protein: from the known and the unknown. J Cell Physiol. 2002;182:311-322.
81. Johnson ME. The association between symptoms of discomfort and signs in dry eye. Ocul Surf. 2009;7:199-211.
82. Wakamatsu TH, Okada N, Kojima T, et al. Evaluation of conjunctival inflammatory status by confocal scanning laser microscopy and conjunctival brush cytology in patients with atopic keratoconjunctivitis (AKC). Mol Vis. 2009;15:1611-1619.