419
Views
41
CrossRef citations to date
0
Altmetric
Research Article

The Beneficial Effects of Doxycycline, An Inhibitor of Matrix Metalloproteinases, on Sulfur Mustard-Induced Ocular Pathologies Depend on the Injury Stage

, , , , , , , , , & show all
Pages 803-812 | Received 11 Aug 2013, Accepted 08 Dec 2013, Published online: 06 Feb 2014

References

  • Kadar T, Turetz J, Fishbine E, Sahar R, Chapman S, Amir A. Characterization of acute and delayed ocular lesions induced by sulfur mustard in rabbits. Curr Eye Res 2001;22:42–53
  • Kadar T, Dachir S, Cohen L, Sahar R, Fishbine E, Cohen M, et al. Ocular injuries following sulfur mustard exposure – pathological mechanism and potential therapy. Toxicology 2009;263:59–69
  • Kadar T, Horwitz V, Sahar R, Cohen M, Cohen L, Gez R, et al. Delayed loss of corneal epithelial stem cells in a chemical injury model associated with limbal stem cell deficiency in rabbits. Curr Eye Res 2011;36:1098–1107
  • Kadar T, Dachir S, Cohen M, Gutman H, Cohen L, Brandeis R, et al. Prolonged impairment of corneal innervation after exposure to sulfur mustard and its relation to the development of delayed limbal stem cell deficiency. Cornea 2013;32:44–50
  • Kadar T, Cohen M, Cohen L, Fishbine E, Sahar R, Brandeis R, et al. Endothelial cell damage following sulfur mustard exposure in rabbits and its association with the delayed-onset ocular lesions. Cutan Ocul Toxicol 2013;32:115–123
  • Javadi MA, Jafarinasab MR, Feizi S, Karimian F, Negahban K. Management of mustard gas-induced limbal stem cell deficiency and keratitis. Ophthalmology 2011;118:1272–1281
  • McNutt P, Hamilton T, Nelson M, Adkins A, Swartz A, Lawrence R, et al. Pathogenesis of acute and delayed corneal lesions after ocular exposure to sulfur mustard vapor. Cornea 2012;31:280–290
  • Milhorn D, Hamilton T, Nelson M, McNutt P. Progression of ocular sulfur mustard injury: development of a model system. Ann N Y Acad Sci 2010;1194:72–80
  • Petrali JP, Dick EJ, Brozetti JJ, Hamilton TA, Finger AV. Acute ocular effects of mustard gas: ultrastructural pathology and immunohistopathology of exposed rabbit cornea. J Appl Toxicol 2000;20:S173–S175
  • Safarinejad MR, Moosavi SA, Montazeri B. Ocular injuries caused by mustard gas: diagnosis, treatment, and medical defense. Mil Med 2001;166:67–70
  • Shohrati M, Peyman M, Peyman A, Davoudi M, Ghanei M. Cutaneous and ocular late complications of sulfur mustard in Iranian veterans. Cutan Ocul Toxicol 2007;26:73–81
  • Amir A, Turetz J, Chapman S, Fishbeine E, Meshulam J, Sahar R, et al. Beneficial effects of topical anti-inflammatory drugs against sulfur mustard-induced ocular lesions in rabbits. J Appl Toxicol 2000;20:S109–S114
  • Chang JH, Gabison EE, Kato T, Azar DT. Corneal neovascularization. Curr Opin Ophthalmol 2001;12:242–249
  • Fujikawa LS, Foster CS, Gipson IK, Colvin RB. Basement membrane components in healing rabbit corneal epithelial wounds: immunofluorescence and ultrastructural studies. J Cell Biol 1984;98:128–138
  • Kurpakus Wheater M, Kernacki KA, Hazlett LD. Corneal cell proteins and ocular surface pathology. Biotech Histochem 1999;74:146–159
  • Li DQ, Pflugfelder SC. Matrix metalloproteinases in corneal inflammation. Ocul Surf 2005;3:S198–S202
  • Fini ME, Girard MT. Expression of collagenolytic/gelatinolytic metalloproteinases by normal cornea. Invest Ophthalmol Vis Sci 1990;31:1779–1788
  • Powell WC, Matrisian LM. Complex roles of matrix metalloproteinases in tumor progression. Curr Top Microbiol Immunol 1996;213:1–21
  • Fini ME, Cook JR, Mohan R. Proteolytic mechanisms in corneal ulceration and repair. Arch Dermatol Res 1998;290:S12–S23
  • Matsubara M, Girard MT, Kublin CL, Cintron C, Fini ME. Differential roles for two gelatinolytic enzymes of the matrix metalloproteinase family in the remodelling cornea. Dev Biol 1991;147:425–439
  • Fini ME, Stramer BM. How the cornea heals: cornea-specific repair mechanisms affecting surgical outcomes. Cornea 2005;24:S2–S11
  • Mohan R, Chintala SK, Jung JC, Villar WV, McCabe F, Russo LA, et al. Matrix metalloproteinase gelatinase B (MMP-9) coordinates and effects epithelial regeneration. J Biol Chem 2002;277:2065–2072
  • Kvanta A, Sarman S, Fagerholm P, Seregard S, Steen B. Expression of matrix metalloproteinase-2 (MMP-2) and vascular endothelial growth factor (VEGF) in inflammation-associated corneal neovascularization. Exp Eye Res 2000;70:419–428
  • Ma DH, Chen JK, Kim WS, Hao YX, Wu HC, Tsai RJ, et al. Expression of matrix metalloproteinases 2 and 9 and tissue inhibitors of metalloproteinase 1 and 2 in inflammation-induced corneal neovascularization. Ophthalmic Res 2001;33:353–362
  • Samolov B, Steen B, Seregard S, van der Ploeg I, Montan P, Kvanta A. Delayed inflammation-associated corneal neovascularization in MMP-2-deficient mice. Exp Eye Res 2005;80:159–166
  • Sivak JM, Fini ME. MMPs in the eye: emerging roles for matrix metalloproteinases in ocular physiology. Prog.Retin Eye Res 2002;21:1–14
  • Su W, Li Z, Lin M, Li Y, He Z, Wu C, et al. The effect of doxycycline temperature-sensitive hydrogel on inhibiting the corneal neovascularization induced by BFGF in rats. Graefes Arch Clin Exp Ophthalmol 2010;249:421–427
  • Zhang H, Li C, Baciu PC. Expression of integrins and MMPs during alkaline-burn-induced corneal angiogenesis. Invest Ophthalmol Vis Sci 2002;43:955–962
  • Ollivier FJ, Gilger BC, Barrie KP, Kallberg ME, Plummer CE, O'Reilly S, et al. Proteinases of the cornea and preocular tear film. Vet. Ophthalmol 2007;10:199–206
  • De Paiva CS, Corrales RM, Villarreal AL, Farley WJ, Li DQ, Stern ME, 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 2006b;83:526–535
  • Pflugfelder SC, Farley W, Luo L, Chen LZ, de Paiva CS, Olmos LC, et al. Matrix metalloproteinase-9 knockout confers resistance to corneal epithelial barrier disruption in experimental dry eye. Am J Pathol 2005;166:61–71
  • Sobrin L, Liu Z, Monroy DC, Solomon A, Selzer MG, Lokeshwar BL, et al. Regulation of MMP-9 activity in human tear fluid and corneal epithelial culture supernatant. Invest Ophthalmol Vis Sci 2000;41:1703–1709
  • Ollivier FJ, Brooks DE, Kallberg ME, Komaromy AM, Lassaline ME, Andrew AE, et al. Evaluation of various compounds to inhibit activity of matrix metalloproteinases in the tear film of horses with ulcerative keratitis. Am J Vet Res 2003;64:1081–1087
  • Golub LM. Introduction and background. Pharmacol Res 2011;63:99–101
  • Griffin MO, Ceballos G, Villarreal FJ. Tetracycline compounds with non-antimicrobial organ protective properties: possible mechanisms of action. Pharmacol Res 2011;63:102–107
  • Stechmiller J, Cowan L, Schultz G. The role of doxycycline as a matrix metalloproteinase inhibitor for the treatment of chronic wounds. Biol Res Nurs 2010;11:336–344
  • Hanemaaijer R, Visser H, Koolwijk P, Sorsa T, Salo T, Golub LM, et al. Inhibition of MMP synthesis by doxycycline and chemically modified tetracyclines (CMTs) in human endothelial cells. Adv Dent Res 1998;12:114–118
  • Ralph RA. Tetracyclines and the treatment of corneal stromal ulceration: a review. Cornea 2000;19:274–277
  • Dursun D, Kim MC, Solomon A, Pflugfelder SC. Treatment of recalcitrant recurrent corneal erosions with inhibitors of matrix metalloproteinase-9, doxycycline and corticosteroids. Am J Ophthalmol 2001;132:8–13
  • Solomon A, Rosenblatt M, Li DQ, Liu Z, Monroy D, Ji Z, et al. Doxycycline inhibition of interleukin-1 in the corneal epithelium. Invest Ophthalmol Vis Sci 2000;41:2544–2557
  • Ren S, Guo LL, Yang J, Liu DS, Wang T, Chen L, et al. Doxycycline attenuates acrolein-induced mucin production, in part by inhibiting MMP-9. Eur J Pharmacol 2011;650:418–423
  • Uitto VJ, Firth JD, Nip L, Golub LM. Doxycycline and chemically modified tetracyclines inhibit gelatinase A (MMP-2) gene expression in human skin keratinocytes. Ann NY Acad Sci 1994;732:140–151
  • Burns FR, Stack MS, Gray RD, Paterson CA. Inhibition of purified collagenase from alkali-burned rabbit corneas. Invest Ophthalmol Vis Sci 1989;30:1569–1575
  • Anumolu SS, DeSantis AS, Menjoge AR, Hahn RA, Beloni JA, Gordon MK, et al. Doxycycline loaded poly(ethylene glycol) hydrogels for healing vesicant-induced ocular wounds. Biomaterials 2010;31:964–974
  • Gordon MK, Desantis A, Deshmukh M, Lacey CJ, Hahn RA, Beloni J, et al. Doxycycline hydrogels as a potential therapy for ocular vesicant injury. J Ocul Pharmacol Ther 2010;26:407–419
  • Aydin E, Kivilcim M, Peyman GA, Esfahani MR, Kazi AA, Sanders DR. Inhibition of experimental angiogenesis of cornea by various doses of doxycycline and combination of triamcinolone acetonide with low-molecular-weight heparin and doxycycline. Cornea 2008;27:446–453
  • Riazi-Esfahani M, Peyman GA, Aydin E, Kazi AA, Kivilcim M, Sanders DR. Prevention of corneal neovascularization: evaluation of various commercially available compounds in an experimental rat model. Cornea 2006;25:801–805
  • Peyman GA, Kazi AA, Riazi-Esfahani M, Aydin E, Kivilcim M, Sanders DR. The effect of combinations of flurbiprofen, low molecular weight heparin, and doxycycline on the inhibition of corneal neovascularization. Cornea 2006;25:582–585
  • Javadi MA, Yazdani S, Sajjadi H, Jadidi K, Karimian F, Einollahi B, et al. Chronic and delayed-onset mustard gas keratitis: report of 48 patients and review of literature. Ophthalmology 2005;112:617–625
  • Solberg Y, Alcalay M, Belkin M. Ocular injury by mustard gas. Surv Ophthalmol 1997;41:461–466
  • Carter RT, Kambampati R, Murphy CJ, Bentley E. Expression of matrix metalloproteinase 2 and 9 in experimentally wounded canine corneas and spontaneous chronic corneal epithelial defects. Cornea 2007;26:1213–1219
  • Daniels JT, Geerling G, Alexander RA, Murphy G, Khaw PT, Saarialho-Kere U. Temporal and spatial expression of matrix metalloproteinases during wound healing of human corneal tissue. Exp Eye Res 2003;77:653–664
  • Ye HQ, Azar DT. Expression of gelatinases A and B, and TIMPs 1 and 2 during corneal wound healing. Invest Ophthalmol Vis Sci 1998;39:913–921
  • Fini ME, Parks WC, Rinehart WB, Girard MT, Matsubara M, Cook JR, et al. Role of matrix metalloproteinases in failure to re-epithelialize after corneal injury. Am J Pathol 1996;149:1287–1302
  • Kuo IC. Corneal wound healing. Curr Opin Ophthalmol 2004;15:311–315
  • Brooks PC, Strömblad S, Sanders LC, von Schalscha TL, Aimes RT, Stetler-Stevenson WG, et al. Localization of matrix metalloproteinase MMP-2 to the surface of invasive cells by interaction with integrin alpha v beta 3. Cell 1996;85:683–693
  • Silletti S, Kessler T, Goldberg J, Boger DL, Cheresh DA. Disruption of matrix metalloproteinase 2 binding to integrin alpha vbeta 3 by an organic molecule inhibits angiogenesis and tumor growth in vivo. Proc Natl Acad Sci USA 2001;98:119–124
  • Mohan R, Sivak J, Ashton P, Russo LA, Pham BQ, Kasahara N, et al. Curcuminoids inhibit the angiogenic response stimulated by fibroblast growth factor-2, including expression of matrix metalloproteinase gelatinase B. J Biol Chem 2000;275:10405–10412
  • McNutt P, Lyman M, Swartz A, Tuznik K, Kniffin D, et al. Arcitectural and biochemical expressions of mustard gas keratopathy: preclinical indicators and pathogenic mechanisms. PLoS ONE 2012;7:e42837
  • Ghasemi H, Ghazanfari T, Babaei M, Soroush MR, Yaraee R, Ghassemi-Broumand M, et al. Long-term ocular complications of sulfur mustard in the civilian victims of Sardasht, Iran. Cutan Ocul Toxicol 2008;27:317–326

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.