The role of matrix metalloproteinases in glaucoma pathogenesis



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Abstract

Matrix metalloproteinases belong to an enzyme family, which assure a proteolysis of practically all components of the extracellular matrix of connective tissues in normal and pathological conditions. At physiological conditions, there are evidences on the impact of this enzyme group in the embryogenesis, morphogenesis, angiogenesis, and tissue involution. The activity impairment of matrix metalloproteinases and of their specific inhibitors leads to the biosynthesis misbalance and to the degradation of extracellular matrix components; it plays a role in the development of such diseases as diabetes mellitus, rheumatoid arthritis, and arteriosclerosis. Laboratory tests and clinical investigation results confirm the role of these enzymes in tissue remodeling of different eyeball structures in glaucoma (in particular, of the trabecular meshwork and the optic disc); it leads to intraocular fluid outflow impairment and to the glaucomatous optic neuropathy development. In the review, the analysis of clinical and experimental studies is performed that are dedicated to the investigation of matrix metalloproteinases role in the pathogenesis of different glaucoma types, of the possibility to use them as biomarkers, as well as therapeutic action targets in this disease.

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About the authors

Inessa Stanislavovna Beletskaya

First Pavlov State Medical University of St. Petersburg

Email: glaziki@list.ru
MD, aspirant. Ophthalmology Department

Sergey Yurievich Astakhov

First Pavlov State Medical University of St. Petersburg

Email: astakhov73@mail.ru
MD, PhD, Doc.Med.Sci., professor, head of the ophthalmology department

References

  1. Быков В. Л. Цитология и общая гистология (функциональная морфология клеток и тканей человека). СПб.: СОТИС;1998
  2. Егоров Е. А., ред. Глаукома. Национальное руководство. Гоэтар-Медиа; 2013.
  3. Каменских Т. Г., Захарова Б. Н., Колбенев И. О., Каменских И. Д., Сидельникова В. С. Исследование молекулярных механизмов регуляции апоптоза ганглиозных клеток сетчатки при первичной открытоугольной глаукоме. Клиническая офтальмология. 2013; 13 (2): 46-49
  4. Маркелова Е. В., Кириенко А. В. Состояние межклеточного матрикса у пациентов с глаукомой. Электронный научный журнал. Современные проблемы науки и образования. 2013;6. Доступен по: http://www.science-education.ru/pdf/2013/6/544.pdf
  5. Огородникова В. Ю., Егоров Е. А., Куроедов А. В., Маркитантова Ю. В., Петров А. Н. Результаты исследования апоптоза клеток дренажной зоны методом иммунохимического анализа у пациентов с продвинутыми стадиями глаукомы. Клиническая офтальмология. 2012; 13 (3): 82-85
  6. Рукина Д. А. Особенности иммунного и цитокинового статуса у больных првичной открытоугольной глаукомой. Автореф. дисс. на соиск. ст. канд. мед. наук. Владивосток; 2012.
  7. Рукина Д. А., Догадова Л. П., Маркелова Е. В., Абдуллин Е. А., Осыховский А. Л., Хохлова А. С. Иммунологические аспекты патогенеза первичной открытоугольной глаукомы. Клиническая офтальмология. 2011; 12 (4): 162-165.
  8. Серов В. В., Шехтер А. Б. Соединительная ткань. М.: Медицина; 1981.
  9. Соколов В. А., Леванова О. Н., Никифоров А. А. Матриксные металлопротеиназы -2 и -9 в слёзной жидкости у больных с первичной открытоугольной глаукомой. Глаукома. 2013; 4:21-29.
  10. Турна А. А. Матриксные металлопротеиназы в развитии деструктивных процессов при ревматоидном артрите. Научно-практическая ревматология.2010; 3: 59-64.
  11. Хасигов П. З., Подобед О. В., Кцоева С. А., Гатагонова Т. М., Грачев С. В., Шишкин С. С., Березов Т. Т. Металлопротеиназы матрикса нормальных тканей человека. Биохимия. 2001; 66 (2): 167 -179.
  12. Щербак И. Г. Биологическая химия: учебник. СПб.: Издательство СПбГМУ; 2005:388
  13. Agapova O. A., Kaufman P. L., Lucarelli M. J., Gabelt B. T., Hernandez M. R. Differential expression of matrix metalloproteinases in monkey eyes with experimental glaucoma or optic optic nerve transection. Brain Res. 2003; 967 (1-2): 132-143.
  14. Agapova O. A., Ricard C. D., Salvador-Silva M., Hernandez M. R. Expression of matrix metalloproteinases and tissue inhibitors of metalloproteinases in human optic nerve head astrocytes. Glia. 2001; 33 (3): 205-216.
  15. Agarwal R., Talati M., Lambert W., Clark A. F., Wilson S. E., Agarwal N., Wordinger R. J. Fas-activated apoptosis and apoptosis mediators in human trabecular meshwork cells. Exp Eye Res. 1999;68 (5): 583-590.
  16. Albon J., Karwatowski W. S., Avery N., Easty D. L., Duance V. C. Changes in the collagenous matrix of aging human lamina cribrosa. Brit J Ophthalmol. 1995; 79 (4): 368-375.
  17. Albon J., Karwatowsky W. S., Easty D. L., Sims T. J., Duance V. C. Age related changes in the non-collagenous components of the extracellular matrix of the human lamina cribrosa. Br J Ophthalmol. 2000; 84 (3): 311-317.
  18. Alexander J. P., Samples J. R., Van Buskirk E. M., Aсott T. S. Expression of matrix metalloproteinases and inhibitor by human trabecula meshwork. Invest Ophthalmol Vis Sci. 1991; 32 (1):172-180.
  19. An H. J., Ninonuevo M., Agilan J., Liu H., Lebrilla C. B., Alvarenga L. S., Mannis M. J. Glycomics analyses of tear fluid for the diagnostic detection of ocular rosacea. J Proteome Res. 2005; 4 (6): 1981-1987.,
  20. Antony T. L., Pierce K. L., Stamer W. D., Regan J. W. Prostaglandin F2 alpha receptors in the trabecular meshwork. Invest Ophthalmol Vis Sci. 1998; 39 (2): 315-321.
  21. Baleriola J., Garcia-Feijoo J., Martinez-de-la-Casa J. M., Fernandez-Crus A., De la Rosa E. J., Fernandez-Durango R. Apoptosis in the trabecular meshwork of glaucomatous patients. Molecular Vision. 2008; 14:1513-1516.
  22. Bellezza A. J., Rintalan C. J., Thompson H. W., Downs J. C., Hart R. T., Burgoyne C. F. Deformation of lamina cribrosa and anterior scleral canal wall in early experimental glaucoma. Invest Ophthalmol Vis Sci. 2003; 44 (2): 623-637.
  23. Bleich S., Roedl J., Von Ahsen N., Schlötzer-Schrebardt U., Reulbach U., Beck J., Kruse F. E., Naumann G. O., Kornhuber J., Jünemann A. G. Elevated homocysteine levels in aqueous humor of patients with pseudoexfoliation glaucoma. Am J Opthalmol. 2004; 138 (1):162-164.
  24. Bradley J. M., Kelley M. J., Rose A., Ascott T. S. Signaling pathways used in trabecular matrix metalloproteinase response to mechanical stretch. Invest Ophthalmol Vis Sci. 2003; 44 (12):5174-5181.
  25. Bradley J. M., Kelley M. J., Zhu X. H., Andersson A. M., Alexander J. P., Ascott T. D. Effect of mechanical stretching on trabecular matrix metalloproteinases. Invest Ophthalmol Vis Sci. 2001; 42 (7):1505-1513.
  26. Buller C., Johson D. H., Tschuper R. C. Human trabecular meshwork phagocytosis. Observation in an organ culture system. Invest Ophthalmol Vis Sci. 1990; 31 (10): 2156-2163.
  27. Burgoyne C. F., Downs J. C., Bellezza A. J. Three-dimensional reconstruction of normal and early glaucoma monkey optic nerve head connective tissues. Invest Ophthalmol Vis Sci. 2004; 45 (12): 4388-4399.
  28. Camras C. B., Chacko D. M., Schlossman A., Posner A. Posner-Schlossman syndrome. In: Prepose J. S., Holland G. N., Wilhelmus K. R., eds. Ocular infection & immunity. St. Louis: Mosby-Year Book, Inc.1996; 529-537.
  29. Chintala S. K., Zhang X., Austin J. S., Fini M. E. Deficiency in matrix metalloproteinase gelatinase B (MMP-9) protects against retinal ganglion cell death after optic nerve ligation. J Biol Chem. 2002; 277 (49): 47461-47468.]
  30. Chuang L. P., Chen N. H., Lin S. W., Chang. Y. L., Chao I. J., Pang J. H. Increased matrix metalloproteinases-9 after sleep in plasma and in monocytes of obstructive sleep apnea patients. Life Sci. 2013; 93 (5-6):220-225.
  31. Djordjević-Jocic J., Zlatanović G., Veselinović D., Jovanović P., Djordjević V., Zvezdanović L., Stanković-Babić G., Vujanović M., Cekić S., Zenkel M., Schlötzer-Schrehardt U. Transforming growth factor β1, matrimetalloproteinase-2 and its tissue inhibitor in patients with pseudoexfoliation glaucoma/syndrome. Vojnosanit Pregl. 2012; 69 (3); 231-236.
  32. Djordjević-Jocić J., Zlatanović G., Veselinović D., Stankovic-Babić G., Cekić S. Gender related differences MMP-2 activity and tissue inhibitor of matrix metalloproteinases in patients with pseudoexfoliation syndrome/glaucoma. Acta Medica Medianae. 2010; 49 (1):5-12.
  33. Downs J. C., Roberts M. D., Sigal I. A. Glaucomatous cupping of the lamina cribrosa: a review of the evidence for active progressive remodeling as a mechanism. Exp Eye Res. 2011; 93 (2): 133-140.
  34. English W. R., Puente X. S., Freije J. M. P., Knaüper V., Amour A., Merryweather A., Lopez-Otin C., Murphy G. Membrane type 4 matrix metalloproteinase (MMP-17) has tumor necrosis factor-alpha convertase activity but does not activate pro-MMP2. J Biol Chem. 2000; 275 (19): 14046-14055.
  35. Flammer J., Mozaffarieh M. What is the present pathgenetic consept of glaucomatous optic neurophathy? Surv Ophtalmol. 2007; 52 (2):162-173.
  36. Fountoulakis N., Labiris G., Aristeidu A., Katsanos A., Tentes I., Korstaris A., Kozobolis V. P. Tissue inhibitor of metalloproteinase 4 in aqueous humor of patients with primary open angle glaucoma, pseudoexfoliation syndrome and pseudoexfoliative glaucoma and its role in proteolysis imbalance. BMC Ophthalmology. 2013; Available at: http://www.biomedcentral.com/1471-2415/13/69. (accessed 23.11.2014).
  37. Fuchshofer R. The pathogenetic roleof transforming growth factor-β2 in glaucomatous damage to the optic nerve head. Exp Eye Res. 2011; 93 (2):165-169.
  38. Gabelt B. T., Kaufman P. L. Postaglandin F2 alpha increases uveoscleral outflow in the cynomolgus monkey. Exp Eye Res. 1989; 49 (3):389-402.
  39. Gartaganis S. P., Geargokopoulos C. D., Mela E. K., Exarchou A., Ziouti N., Assouti M., Vynios D. H. Matrix metalloproteinases and their inhibitors in exfoliation syndrome. Ophthalmic Res. 2002; 34 (3):165-171.
  40. Gaton D. D., Sagara T., Lindsey J. D., Weinreb R. N. Matrix metalloproteinase-1 localization in the normal human uveoscleral pathway. Invest Ophthalmol Vis Sci. 1999; 40 (2):363-369.
  41. Gold M. E., Kansara S., Nagi K. S., Bell N. P., Blieden L. S., Chuang A. Z., Baker L. A., Vankiewicz K. A., Feldman R. M. Age-related changes in trabecular meshwork imaging. HPC BioMed Research International. 2013. Available at: http://dx.doi.org/10.1155/2013/295204.
  42. Golubnitschaja O., PhD, Flammer J., MD. What are the biomarkers for glaucoma? Surv Ophthalmol.; 2007; 52 (2):155-161.
  43. Golubnitschaja O., Yeghiazaryan K., Liu R., Mönkemann H., Leppert D., Schild H., Haefliger I. O., Flammer J. Increased expression of matrix metalloproteinases in mononuclear blood cells of normal-tension glaucoma patients. Glaucoma J. 2004; 13 (1): 66-72.
  44. Guo L., Moss S. E., Alexander R. A., Ali R. R., Fitzke F. W., Cordeiro M. F. Retinal ganglion cell apoptosis in glaucoma is related to intraocular pressure and IOP-induced effects on extracellular matrix. Invest Ophthalmol Vis Sci. 2005; 46 (1):175-182.
  45. Hamid M. A. A., Fahmy I. A., Moemen L. A., El-Beltagy T. Role of matrix metalloproteinase-2 and its inhibitor and erythropoietin in the pathogenesis of pseudoexfoliative glaucoma. Aust J Basic & Appl Sci. 2008; 2 (3): 752-756.
  46. Hernandez M. R. The optic nerve head in glaucoma: role of astrocytes in tissue remodeling. Prog Retinal Eye Res. 2000; 19 (3): 297-321.
  47. Hernandez M. R., Luo X. X., Andrzejewska W., Neufeld A. H. Age-related changes in the extracellular matrix of the human optic nerve head. Am J Ophthalmol. 1989; 107 (5): 476-484.
  48. Hernandez M. R., Luo X. X., Igoe F., Neufeld A. H. Extracellular matrix of the human lamina cribrosa. Am J Ophthalmol. 1987; 104 (6): 567-576.
  49. Hernandez M. R., Wang N., Hanley N. M., Neufeld A. H. Localization of collagen I and IV mRNAs in human optic nerve head by in situ hybridization. Invest Ophthalmol Vis Sci. 1991; 32 (8): 2169-2177.
  50. Ho S. L., Dogar G. F., Wang J., Crean J., Wu Q. D., Oliver N., Weitz S., Murray A., Cleary P. E., Brien C. O. Elavated aqueous humor tissue inhibitor of matrix metalloproteinase-1 and connective tissue growth factor in pseudoexfoliation syndrome. Br J Ophthalmol. 2005; 89 (2):169-173.
  51. Honda N., Miyai T., Nejima R., Miyata K., Mimura T., Usui T., Aihara M., Araie M., Amano S. Effect of latanoprost on the expression of matrix metalloproteinases and tissue inhibitor of metalloproteinase 1 on the ocular surface. Arch Ophthalmol. 2010; 128 (4): 466-471.
  52. Hussain A. A., Lee Y., Zhang J., Marshall J. Characterization of the gelatinase system of the laminar human optic nerve, and surrounding annulus of Bruch’s membrane, choroid, and sclera. Invest Ophthalmol Vis Sci. 2014; 55 (4):2358-2364.
  53. Johnson D. H. Histologic findings after argon laser trabeculoplasty in glaucomatous eyes. Exp Eye Res. 2007; 85 (4):557-562.
  54. Johnson E. C., Morrison J. C., Farrell S., Deppmeier L., Moor C. G., McGinty M. R. The effect of chronically elevated intraocular pressure on the rat optic nerve head extracellular matrix. Exp Eye Res. 1996; 62 (6):663-674.]
  55. Johnson T. V., Fan S., Camras C. B., Toris C. B. Aqueous humor dynamics in exfoliation syndrome. Arch Ophthalmol. 2008;126 (7):914-920.
  56. Kara S., Yildirim N., Ozer A., Colak O., Sahin A. Matrix metalloproteineise-2, tissue inhibitor of matrix metalloproteineise-2, and transforming growth factor beta 1 in the aqueous humor and serum of patients with pseudoexfoliation syndrome. Clinical Ophthalmology. 2014:8. Available at: http://dx.doi.org/10.2147/OPTH.S55914. (accessed 15.12.2014)
  57. Kee C., Son S., Ahn B. H. The relationship between gelatinase A activity in aqueous humor and glaucoma. J Glaucoma. 1999; 8 (1):51-55.
  58. Kelley M. J., Rose A. Y., Song K., Chen Y., Bradley J. M., Rookhuizen D., Acott T. S. Synergism of TNF and IL-1 in the induction of matrix metalloproteinase-3 in trabecula meshwork. Invest Ophthalmol Vis Sci. 2007; 48:2634-2643.
  59. Kirwan R. P., Crean J. K., Fenetry C. H., Clark. A. А., O’Brien C. J. Effect of cyclical mechanical stretch and exogenous transforming growth factor-beta1 on matrix metalloproteinase-2 activity in lamina cribrosa cells from the human optic nerve head. J Glaucoma. 2004; 13 (4): 327-334.
  60. Knepper P. A., Goossens W., Hvizd M., Palmberg P. F. Glycosaminoglycans of the human trabecular meshwork in primary open-angle glaucoma. Invest Ophthalmol Vis Sci. 1996; 37 (7):1360-1367.
  61. Konstas A. G., Koliakos G. G., Karabatsas C. H., Liakos P., Schlötzer- Schrebardt U., Georgiadis N., Ritch R. Latanoprost therapy reduces the levels of TGF beta 1 and gelatinases in the aqueous humor of patients with exfoliative glaucoma. Exp Eye Res. 2006; 82 (2):319-322.
  62. Kouwenhoven M., Ozenci V., Gomes A., Yarilin D., Giedratis V., Press R., Link H. Multiple sclerosis: elevated expression of matrix metalloproteinases in blood monocytes. J Autoimmun. 2001; 16 (4): 463-470.
  63. Lan J., Kumar R. K., Di Giloramo N., McCluskey P., Wakefield D. Expression and distribution of matrix metalloproteinases and their inhibitors in the human iris and ciliary body. Br J Ophtalmol. 2003; 87 (2):208-211.
  64. Lindsey J. D., Kashiwagi K., Kashivagi F., Weinreb R. N. Prostaglandin action on ciliary body smooth muscle extracellular matrix metabolism: implication for uveoscleral outflow. Surv Ophthalmol. 1997;41 (2): 53-59.
  65. Liton P. B., Gonzalez P., Epstein D. L. The role of proteolytic cellular systems in trabecular meshwork homeostasis. Exp Eye Res. 2009; 88 (4):724-728.
  66. Lorenzl S., Albers D. S., Relkin N., Ngyuen T., Hilgenberg S. L., Chirichigno J., Cudkowicz M. E., Beal M. F. Increased plasma levels of matrix metalloproteinase-9 in patients with Alzheimer, s disease. Neurochem Int. 2003; 43 (3): 191-196.
  67. Määttä M., Tervahartiala T., Harju M., Airaksinen J., Autio-Harmainen H., Sorsa T. Matrix metalloproteinases and their tissue inhibitors in aqueous humor of patients with primary open-angle glaucoma, exfoliation syndrome, and exfoliation glaucoma. J Glaucoma.2005; 14 (1):64-69.
  68. Marchenko N. D., Marchenko G. N., Weinreb R. N., Lindsey J. D., Kyshtoobayeva A., Crawford H. C., Strongin A. Y. Beta-catenin regulates the gene of MMP-26, a novel metalloproteinase expressed both in carcinomas and normal epithelial cells. Int J Biochem Cell Biol. 2004; 36 (5):942-956.
  69. Marcoulli M., Papas E., Cole N., Holden B. A. The diurnal variation of matrix metalloproteinase-9 and its associated factors in human tears. Invest. Ophthalmol. Vis. Sci. 2012; 53 (3); 1479-1484.
  70. Matsuo T., Cynader M. S. Localization of prostaglandin F2 alpha and E2 binding sites in the human eye. Br J Ophthalmol.1992; 76 (4):210-213.
  71. Morrison J. C., Jerdan J. A., Dorman M. E., Quigley H. A. Structural proteins of neonatal and adult lamina cribrosa. Arch Ophthalmol. 1989; 107 (8): 1220-1224.
  72. Nagase H., Visse R., Murphy G. Structure and function of matrix metalloproteinases and TIMPs. Cardiovascular Research. 2006; 69 (3):562-573.
  73. Neufeld A. H., Hernandez M. R., Gonzalez M. Nitric oxide synthase in the human glaucomatous optic nerve head. Arch Ophthalmol. 1997; 115 (4): 497-503.
  74. Nga A. D. C., Yap S., Samsudin A., Abdul-Rahman P. S., Hashim O. H., Mumiwati Z. Matrix metalloproteinases and tissue inhibitors of metalloproteinases in the aqueous humor of patients with primary angle closure glaucoma - a quantitative study. BMC Ophthalmology. 2014; 14 (33). Available at: http://www.biomedcentral.com/1471-2415/14/33. (accessed 23.11.2014).
  75. Noske W., Hensen J., Wiederholt M. Endotelin-like immunoreactivity in aqueous humor of patients with primary open-angle glaucoma and cataract. Graefes Arch Clin Exp Ophthalmol.1997; 235 (9): 551-552.
  76. Ochuchi E., Imai K., Fujii Y., Sato H., Seiki M., Okada Y. Membrane type 1 matrix metalloproteinase digests interstitial collagens and other extracellular matrix macromolecules. J Biol Chem. 1997; 272 (4): 2446-2451.
  77. Oh D. J., Kang M. H., Ooi Y. H., Sage E. H., Rhee D. J. Overexpression of SPARC in human trabecular meshwork increases intraocular pressure and alters extracellular matrix. Invest Ophthalmol Vis Sci. 2013; 54 (5):3309-3319.
  78. Oh D-J., Martin J. L., Williams A. J., Russell P, Birk D. E., Rhee D. J. Effect of latanoprost on the expression of matrix metalloproteinases and their tissue inhibitors in human trabecula meshwork cells. Invest Ophthalmol Vis Sci. 2006; 47 (9):3887-3895.
  79. Oh D-J., Martin J. L., Williams A. J., Peck R. E., Pokorny C., Russel P., Birk D. E., Rhee D. Analysis of expression of matrix metalloproteinases and tissue inhibitors of metalloproteinases in human ciliary body after latanoprost. Invest Ophthalmol Vis Sci. 2006; 47 (3): 953-963.
  80. Osborne N. N., Ugarte M., Chao M., Chidlow G., Bae J. H., Wood J. P., Nash M. S. Neuroprotection in relation to retinal ischemia and relevance to glaucoma. Surv Ophthalmol. 1999; 43 (1): 102-128.
  81. Ovodenko B., Rostagno A., Neubert T. A., Shetty V., Thomas S., Yang A., Liebmann J., Ghiso J., Ritch R. Proteomic analysis of exfoliation deposits. Invest Ophthalmol Vis Sci. 2007; 48 (4): 1447-1457.
  82. Parshley D. E., Bradley J. M., Fisk A., Hadaegh A., Samples J. R., Van Buskirk E. M., Ascott T. S. Laser trabeculoplasty induces stromelysin expression by trabecular juxtacanalicular cells. Invest Ophthalmol Vis Sci. 1996; 37 (5):795-804.
  83. Pieragostino D., Bucci S., Agnifili L., Fasanella V., D, Aguanno S., Mastropasqua A. Et al. Differential protein expression in tears of patients with primary open angle and pseudoexfoliative glaucoma. Mol Biosyst 2012; 8 (4):1017-1028.
  84. Porter K. M., Epstein D. L., Liton P. B. Up-regulated expression of extracellular matrix remodeling genes in phagocytically challenged trabecular meshwork cells. 2012; 7 (4): e34792. Available at: www.plosone.org. (accessed 23/11/2014).
  85. Quigley H. A. Neuronal death in glaucoma. Prog Retinal Eye Res.1999; 18 (1): 39-57.
  86. Quigley H. A., Addicks E. M. Regional differences in the structure of the lamina cribrosa and their relation to the glaucomatous optic nerve damage. Arch Ophthalmol. 1981; 99 (1):137-143.
  87. Roberts M. D., Grau V., Grimm J., Reynaud J., Bellezza A. J., Burgoyne C. F., Downs C. Remodeling of the connective tissue microarchitecture of the lamina cribrosa in early experimental glaucoma. Invest Ophthalmol Vis Sci. 2009; 50 (2): 681-690.
  88. Robertson J. V., West-Mays A. S. Altered expression of transforming growth factor beta1 and matrix metalloproteinase-9 results in elevated intraocular pressure in mice. Mol Vis. 2013; 19:684-695. Available at: http://www.molvis.org/molvis/v19/684. (accessed 17.12.2014)
  89. Schachtschabel U., Lindsey J. D., Weinreb R. N. The mechanism of action of prostaglandins on uveoscleral outflow. Curr Opin Ophthalmol. 2000; 11 (2):112-115.
  90. Schlötzer-Schrebardt U., Lommatzsch J., Küchle M., Konstas A. G. P., Naumann G. O. Matrix metalloproteinases and their inhibitors in aqueous humor of patients with pseudoexfoliation syndrome/glaucoma and primary open-angle glaucoma. Invest Ophthalmol Vis Sci. 2003; 44 (3):1117-1125.
  91. Schlötzer-Schrehardt U., Zenkel M., Kuchle M., Sakai L. Y., Naumann G. O. Role of transforming growth factor-beta1 and its latent form binding protein in pseudoexfoliation syndrome. Exp Eye Res. 2001; 73 (6):765-780.
  92. Takai Y., Tanino M., Obira A. Multiple cytokine analysis of aqueous humor in eyes with primary open-angle glaucoma, exfoliation glaucoma, and cataract. Invest Ophthalmol Vis Sci. 2012; 53 (1): 241-247.
  93. Tayebjee M. H., Lip G. Y. H., Blann A. D., MacFadyen R. J. Effects of age, gender, ethnicity, diurnal variation and exercise on circulating levels of matrix metalloproteinases (MMP)-2 and -9, and their inhibitors, tissue inhibitors of matrix metalloproteinases (TIMP)-1 and -2. Thrombosis research. 2005; 115 (3): 205-210.
  94. Tektas O. Y., Lütjen-Drecoll E. Structural changes of the trabecular meshwork in different kinds of glaucoma. ExpEye Res. 2009; 88 (4):769-775.
  95. ThamY. C., Li X., Wong T. Y., Quigley H. A., Aung T., Cheng C. Y. Global prevalence of glaucoma and projections of glaucoma burden through 2040: a systematic review and meta-analysis. Ophthalmology. 2014; 121 (11):2081-2090.
  96. Toris C. B., Koepsell S. A., Yablonski M. E., Camras C. B. Aqueous humor dynamics in ocular hypertensive patients. J Glaucoma. 2002; 11 (3): 253-258.
  97. Toris C. B., Pederson J. E. Aqueous humor dynamics in experimental iridocyclitis. Invest Ophthalmol Vis Sci. 1986; 27 (3):289.
  98. Toris C. B., Yablonski M. E., Wang Y-L., Camras C. B. Aqueous humor dynamics in the aging human eye. Am J Ophthalmol. 1999; 127 (4): 407-412.
  99. Tsioufis C., Bafakis I., Kasiakogias A., Stefanadis C. The role of matrix metalloproteinases in diabetes mellitus. Curr Top Med Chem. 2012; 12 (10): 1159-1165.
  100. Van den Steen. Biochemistry and molecular biology of gelatinase B or matrix metalloproteinase-9 (MMP-9). Critical reviews in biochem. 2002; 37 (6): 375-536.
  101. Verma R. P., Hansch C. Matrix metalloproteinases (MMPs): chemical-biological functions and (Q)SARs. Bioorg Med Chem. 2007; 15 (6): 2223-2268.
  102. Visse R., Nagase H. Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ Res. 2003; 92 (8): 827-839.
  103. Wang N., Lu Q., Li J., Wang L. Prostaglandin induces the expression of matrix metalloproteinase-1in ciliary melanocytes. Chin Med J. 2008; 121 (3): 1173-1176.
  104. Weinreb R. Uveoscleral outflow: the other outflow pathway. J Glaucoma. 2000; 9 (5): 343-345.
  105. Weinreb R. N., Kashiwagi K., Kashiwagi F., Tuskahara S., Lindsey J. D. Prostaglandins increase matrix metalloproteinase release from human smooth muscle cells. Invest Ophthalmol Vis Sci. 1997; 38 (13):2772-2780.
  106. Weinstein W. L., Dietrich U. M., Sapienza J. S., Carmichael K. R., Moor P. A., Krunkovsky T. M. Identification of ocular matrix metalloproteinases present within the aqueous humor and iridocorneal drainage angle tissue of normal and glaucomatous canin eyes. Vet Ophthalmol. 2007; 10 (1): 108-116.
  107. Yan X., Tezel G., Wax M. B., Edward D. P. Matrix metalloproteinases and tumor necrosis factor alpha in glaucomatous optic nerve head. Arch Ophthalmol. 2000; 118 (5):666-673.
  108. Yang H., Downs J. C., Bellezza A., Thompson H., Burgoyne C. F. 3-D histomorphometry of the normal and early glaucomatous monkey optic nerve head: prelaminar neural tissues and cupping. Invest Ophthalmol Vis Sci. 2007; 48 (11):5068-5084.
  109. Yu A. L., Fuchshfer R., Kampik A., Welge-Lüssen U. Effects of oxidative stress in trabecular meshwork cells are reduced by prostaglandin analogues. Invest Ophthalmol Vis Sci. 2008; 49 (11):4872-4880.
  110. Yuan L., Neufeld A. H. Activated microglia in the human glaucomatous optic nerve head. J Neurosci Res. 2001; 64 (5):523-532.

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