Review Article

Age-related Macular Degeneration: Current Knowledge of Zinc Metalloproteinases Involvement

Author(s): Francesca Liva, Doretta Cuffaro, Elisa Nuti, Susanna Nencetti, Elisabetta Orlandini, Giovanni Vozzi and Armando Rossello*

Volume 20, Issue 9, 2019

Page: [903 - 918] Pages: 16

DOI: 10.2174/1389450120666190122114857

Price: $65

Abstract

Background: Advanced age-related macular degeneration (AMD) is the leading cause of blindness in the elderly with limited therapeutic options. The disease is characterized by photoreceptor loss in the macula and reduced Retinal Pigment Epithelium (RPE) function, associated with matrix degradation, cell proliferation, neovascularization and inflammation. Matrix metalloproteinases (MMPs), a disintegrin and metalloproteinases (ADAMs) and a disintegrin and metalloproteinase with thrombospondin motifs (ADAMTSs) play a critical role in the physiology of extracellular matrix (ECM) turnover and, in turn, in ECM pathologies, such as AMD. A balance between the activities of MMPs and Tissue Inhibitors of Metalloproteinase (TIMPs) is crucial for the integrity of the ECM components; indeed, a dysregulation in the ratio of these factors produces profound changes in the ECM, including thickening and deposit formation, which eventually might lead to AMD development.

Objective: This article reviews the relevance and impact of zinc metalloproteinases on the development of AMD and their roles as biomarkers and/or therapeutic targets. We illustrate some studies on several inhibitors of MMPs currently used to dissect physiological properties of MMPs. Moreover, all molecules or technologies used to control MMP and ADAM activity in AMD are analyzed.

Conclusion: This study underlines the changes in the activity of MMPs expressed by RPE cells, highlights the functions of already used MMP inhibitors and consequently suggests their application as therapeutic agents for the treatment of AMD.

Keywords: AMD, RPE, MMPs, ADAMs, ADAMTSs, MMP inhibitors.

Graphical Abstract
[1]
Curcio CA, Presley JB, Malek G, Medeiros NE, Avery DV, Kruth HS. Esterified and unesterified cholesterol in drusen and basal deposits of eyes with age-related maculopathy. Exp Eye Res 2005; 81(6): 731-41.
[http://dx.doi.org/10.1016/j.exer.2005.04.012] [PMID: 16005869]
[2]
Hogan MJ. Role of the retinal pigment epithelium in macular disease. Trans Am Acad Ophthalmol Otolaryngol 1972; 76(1): 64-80.
[PMID: 5024602]
[3]
Murphy G. The ADAMs: signalling scissors in the tumour microenvironment. Nat Rev Cancer 2008; 8(12): 929-41.
[http://dx.doi.org/10.1038/nrc2459] [PMID: 19005493]
[4]
Jager RD, Mieler WF, Miller JW. Age-related macular degeneration. N Engl J Med 2008; 358(24): 2606-17.
[http://dx.doi.org/ 10.1056/NEJMra0801537] [PMID: 18550876]
[5]
Lim LS, Mitchell P, Seddon JM, Holz FG, Wong TY. Age-related macular degeneration. Lancet 2012; 379(9827): 1728-38.
[http://dx.doi.org/10.1016/S0140-6736(12)60282-7] [PMID: 22559899]
[6]
Fritsche LG, Igl W, Bailey JN, et al. A large genome-wide association study of age-related macular degeneration highlights contributions of rare and common variants. Nat Genet 2016; 48(2): 134-43.
[http://dx.doi.org/10.1038/ng.3448] [PMID: 26691988]
[7]
Vingerling JR, Dielemans I, Bots ML, Hofman A, Grobbee DE, de Jong PT. Age-related macular degeneration is associated with atherosclerosis. The Rotterdam Study. Am J Epidemiol 1995; 142(4): 404-9.
[http://dx.doi.org/10.1093/oxfordjournals.aje.a117648] [PMID: 7625405]
[8]
Seddon JM, Ajani UA, Sperduto RD, et al. Dietary carotenoids, vitamins A, C, and E, and advanced age-related macular degeneration. JAMA 1994; 272(18): 1413-20.
[http://dx.doi.org/10.1001/jama.1994.03520180037032] [PMID: 7933422]
[9]
Friedman DS, O’Colmain BJ, Muñoz B, et al. Prevalence of age-related macular degeneration in the United States. Arch Ophthalmol 2004; 122(4): 564-72.
[http://dx.doi.org/10.1001/archopht.1941.00870100042005] [PMID: 15078675]
[10]
Chang MA, Bressler SB, Munoz B, West SK. Racial differences and other risk factors for incidence and progression of age-related macular degeneration: Salisbury Eye Evaluation (SEE) Project. Invest Ophthalmol Vis Sci 2008; 49(6): 2395-402.
[http://dx.doi.org/ 10.1167/iovs.07-1584] [PMID: 18263809]
[11]
Nano ME, Lansingh VC, Pighin MS, et al. Risk factors of age-related macular degeneration in Argentina. Arq Bras Oftalmol 2013; 76(2): 80-4.
[http://dx.doi.org/10.1590/S0004-27492013000 200005] [PMID: 23828466]
[12]
McCarty CA, Mukesh BN, Fu CL, Mitchell P, Wang JJ, Taylor HR. Risk factors for age-related maculopathy: the Visual Impairment Project. Arch Ophthalmol 2001; 119(10): 1455-62.
[http://dx.doi.org/10.1001/archopht.119.10.1455] [PMID: 11594944]
[13]
Rowan S, Jiang S, Korem T, et al. Involvement of a gut-retina axis in protection against dietary glycemia-induced age-related macular degeneration. Proc Natl Acad Sci USA 2017; 114(22): E4472-81.
[http://dx.doi.org/10.1073/pnas.1702302114] [PMID: 28507131]
[14]
Armstrong RA, Mousavi M. Overview of risk factors for Age-Related Macular Degeneration (AMD). J Stem Cells 2015; 10(3): 171-91.
[PMID: 27125062]
[15]
Chakravarthy U, Evans J, Rosenfeld PJ. Age related macular degeneration. BMJ 2010; 340: c981.
[http://dx.doi.org/10.1136/bmj.c981] [PMID: 20189972]
[16]
Johnson LV, Leitner WP, Staples MK, Anderson DH. Complement activation and inflammatory processes in Drusen formation and age related macular degeneration. Exp Eye Res 2001; 73(6): 887-96.
[http://dx.doi.org/10.1006/exer.2001.1094] [PMID: 11846519]
[17]
Edwards AO, Ritter R III, Abel KJ, Manning A, Panhuysen C, Farrer LA. Complement factor H polymorphism and age-related macular degeneration. Science 2005; 308(5720): 421-4.
[http://dx.doi.org/10.1126/science.1110189] [PMID: 15761121]
[18]
Gold B, Merriam JE, Zernant J, et al. Variation in factor B (BF) and complement component 2 (C2) genes is associated with age-related macular degeneration. Nat Genet 2006; 38(4): 458-62.
[http://dx.doi.org/10.1038/ng1750] [PMID: 16518403]
[19]
Jager RD, Mieler WF, Miller JW. Age-related macular degeneration. N Engl J Med 2008; 358(24): 2606-17.
[http://dx.doi.org/10.1056/NEJMra0801537] [PMID: 18550876]
[20]
Molins B, Romero-Vázquez S, Fuentes-Prior P, Adan A, Dick AD. C-Reactive Protein as a Therapeutic Target in Age-Related Macular Degeneration. Front Immunol 2018; 9: 808.
[http://dx.doi.org/10.3389/fimmu.2018.00808] [PMID: 29725335]
[21]
Nita M, Strzałka-Mrozik B, Grzybowski A, Mazurek U, Romaniuk W. Age-related macular degeneration and changes in the extracellular matrix. Med Sci Monit 2014; 20: 1003-16.
[http://dx.doi.org/10.12659/MSM.889887] [PMID: 24938626]
[22]
Kutty RK, Samuel W, Boyce K, et al. Proinflammatory cytokines decrease the expression of genes critical for RPE function. Mol Vis 2016; 22: 1156-68.
[PMID: 27733811]
[23]
Ferris FL, Davis MD, Clemons TE, et al. A simplified severity scale for age-related macular degeneration: AREDS Report No. 18. Arch Ophthalmol 2005; 123(11): 1570-4.
[http://dx.doi.org/ 10.1001/archopht.123.11.1570] [PMID: 16286620]
[24]
Wong WL, Su X, Li X, et al. Global prevalence of age-related macular degeneration and disease burden projection for 2020 and 2040: a systematic review and meta-analysis. Lancet Glob Health 2014; 2(2): e106-16.
[http://dx.doi.org/10.1016/S2214-109X(13) 70145-1] [PMID: 25104651]
[25]
A randomized, placebo-controlled, clinical trial of high-dose supplementation with vitamins C and E, beta carotene, and zinc for age-related macular degeneration and vision loss: AREDS report no. 8. Arch Ophthalmol 2001; 119(10): 1417-36.
[http://dx.doi.org/ 10.1001/archopht.119.10.1417] [PMID: 11594942]
[26]
Parmet S, Lynm C, Glass RM. JAMA patient page. Age-related macular degeneration. JAMA 2002; 288(18): 2358.
[http://dx.doi.org/10.1001/jama.288.18.2358] [PMID: 12448423]
[27]
Al-Zamil WM, Yassin SA. Recent developments in age-related macular degeneration: a review. Clin Interv Aging 2017; 12: 1313-30.
[http://dx.doi.org/10.2147/CIA.S143508] [PMID: 28860733]
[28]
Bennett N, John L, Likhar N, Agrawal R, Amoaku WM. Clinical Efficacy and Safety of Current Interventions for Choroidal Neovascularization Associated with Rare Diseases: A Systematic Literature Review. Adv Ther 2018; 35(5): 591-603.
[http://dx.doi.org/ 10.1007/s12325-018-0698-9] [PMID: 29687336]
[29]
Fritsche LG, Fariss RN, Stambolian D, Abecasis GR, Curcio CA, Swaroop A. Age-related macular degeneration: genetics and biology coming together. Annu Rev Genomics Hum Genet 2014; 15: 151-71.
[http://dx.doi.org/10.1146/annurev-genom-090413-025610] [PMID: 24773320]
[30]
Chong NH, Keonin J, Luthert PJ, et al. Decreased thickness and integrity of the macular elastic layer of Bruch’s membrane correspond to the distribution of lesions associated with age-related macular degeneration. Am J Pathol 2005; 166(1): 241-51.
[http://dx.doi.org/10.1016/S0002-9440(10)62248-1] [PMID: 15632016]
[31]
Saint-Geniez M, Kurihara T, Sekiyama E, Maldonado AE, D’Amore PA. An essential role for RPE-derived soluble VEGF in the maintenance of the choriocapillaris. Proc Natl Acad Sci USA 2009; 106(44): 18751-6.
[http://dx.doi.org/10.1073/pnas.090501 0106] [PMID: 19841260]
[32]
Mullins RF, Sohn EH. Bruch’s Membrane: The Critical Boundary in Macular Degeneration. In: Ying GS, ed. Age Related Macular Degeneration. Rec Adv Basic Res Clin Care 2012; 3: 300.
[33]
Nita M, Strzałka-Mrozik B, Grzybowski A, Mazurek U, Romaniuk W. Age-related macular degeneration and changes in the extracellular matrix. Med Sci Monit 2014; 20: 1003-16.
[http://dx.doi.org/10.12659/MSM.889887] [PMID: 24938626]
[34]
Sparrow JR, Hicks D, Hamel CP. The retinal pigment epithelium in health and disease. Curr Mol Med 2010; 10(9): 802-23.
[http://dx.doi.org/10.2174/156652410793937813] [PMID: 21091424]
[35]
Alcazar O, Cousins SW, Striker GE, Marin-Castano ME. (Pro)renin receptor is expressed in human retinal pigment epithelium and participates in extracellular matrix remodeling. Exp Eye Res 2009; 89(5): 638-47.
[http://dx.doi.org/10.1016/j.exer. 2009.06.014] [PMID: 19580809]
[36]
Brew K, Nagase H. The tissue inhibitors of metalloproteinases (TIMPs): an ancient family with structural and functional diversity. Biochim Biophys Acta 2010; 1803(1): 55-71.
[http://dx.doi.org/ 10.1016/j.bbamcr.2010.01.003] [PMID: 20080133]
[37]
Alexander JP, Bradley JM, Gabourel JD, Acott TS. Expression of matrix metalloproteinases and inhibitor by human retinal pigment epithelium. Invest Ophthalmol Vis Sci 1990; 31(12): 2520-8.
[PMID: 2176183]
[38]
Rhoades W, Dickson D, Do DV. Potential role of lampalizumab for treatment of geographic atrophy. Clin Ophthalmol 2015; 9: 1049-56.
[PMID: 26089637]
[39]
ahttps://clinicaltrials.gov/ct2/show/NCT022474792017.https://clinicaltrials.gov/ct2/show/NCT02247531bHolz FG, Sadda SR, Busbee B, et al. Efficacy and safety of lampalizumab for geographic atrophy due to age-related macular degeneration: Chroma and spectri phase 3 randomized clinical trials. JAMA Ophthalmol 2018; 136(6): 666-77.
[http://dx.doi.org/10.1001/jamaophthalmol.2018.1544] [PMID: 29801123]
[40]
Clinical study to evaluate treatment with Oracea® for geo-graphic atrophy (TOGA). https://clinicaltrials.gov/ct2/show/NCT01782989 NLM identifier: NCT01782989 [Accessed on December 17, 2018.];
[41]
Szeto HH, Birk AV. Serendipity and the discovery of novel compounds that restore mitochondrial plasticity. Clin Pharmacol Ther 2014; 96(6): 672-83.
[http://dx.doi.org/10.1038/clpt.2014.174] [PMID: 25188726]
[42]
A study of MTP-131 topical ophthalmic solution in subjects with diabetic macular edema and non-exudative intermediate age-related macular degeneration (SPIOC-101). https://clinicaltrials.gov/ct2/show/NCT02314299?termNLM identifier: NCT02314299 [Accessed on December 17, 2018.];
[43]
Gragoudas ES, Adamis AP, Cunningham ET Jr, Feinsod M, Guyer DR. Pegaptanib for neovascular age-related macular degeneration. N Engl J Med 2004; 351(27): 2805-16.
[http://dx.doi.org/ 10.1056/NEJMoa042760] [PMID: 15625332]
[44]
Yonekawa Y, Miller JW, Kim IK. Age-related macular degeneration: advances in management and diagnosis. J Clin Med 2015; 4(2): 343-59.
[http://dx.doi.org/10.3390/jcm4020343] [PMID: 26239130]
[45]
Stewart MW. Aflibercept (VEGF Trap-eye): the newest anti-VEGF drug. Br J Ophthalmol 2012; 96(9): 1157-8.
[http://dx.doi.org/10. 1136/bjophthalmol-2011-300654] [PMID: 22446028]
[46]
A phase 1, safety, tolerability and pharmacokinetic profile of intravitreous injections of E10030 (anti-PDGF pegylated ap-tamer) in subjects with neovascular age-related macular de-generation. https://clinicaltrials.gov/show/NCT00569140 NLM identifier: NCT00569140 [Accessed on December 17, 2018.];
[47]
A safety and efficacy study of E10030 (antiPDGF pegylated aptamer) plus lucentis for neovascular age-related macular degeneration. https://clinicaltrials.gov/ct2/show/NLM identifier: NCT 01089517 [Accessed on December 17, 2018.];
[48]
Singh M, Tyagi SC. Metalloproteinases as mediators of inflammation and the eyes: molecular genetic underpinnings governing ocular pathophysiology. Int J Ophthalmol 2017; 10(8): 1308-18.
[PMID: 28861360]
[49]
Guo L, Hussain AA, Limb GA, Marshall J. Age-dependent variation in metalloproteinase activity of isolated human Bruch’s membrane and choroid. Invest Ophthalmol Vis Sci 1999; 40(11): 2676-82.
[PMID: 10509665]
[50]
Hussain AA, Starita C, Marshall J. Molecular weight size exclusion limit and diffusional status of aging human Bruch’s membrane. IOVS 1999; 40: S973.
[51]
Liutkeviciene R, Sinkunaite-Marsalkiene G, Asmoniene V, Zaliuniene D. An impact of mutation on MMP-2, -3 and -9 activity regulation and influence on age-related macular degeneration development: literature review. Biologija (Vilnius) 2014; 60: 107-16.
[http://dx.doi.org/10.6001/biologija.v60i2.2910]
[52]
Eichler W, Friedrichs U, Thies A, Tratz C, Wiedemann P. Modulation of matrix metalloproteinase and TIMP-1 expression by cytokines in human RPE cells. Invest Ophthalmol Vis Sci 2002; 43(8): 2767-73.
[PMID: 12147614]
[53]
Plantner JJ, Jiang C, Smine A. Increase in interphotoreceptor matrix gelatinase A (MMP-2) associated with age-related macular degeneration. Exp Eye Res 1998; 67(6): 637-45.
[http://dx.doi.org/ 10.1006/exer.1998.0552] [PMID: 9990329]
[54]
Kamei M, Hollyfield JG. TIMP-3 in Bruch’s membrane: changes during aging and in age-related macular degeneration. Invest Ophthalmol Vis Sci 1999; 40(10): 2367-75.
[PMID: 10476804]
[55]
Hussain AA, Lee Y, Zhang JJ, Marshall J. Disturbed matrix metalloproteinase activity of Bruch’s membrane in age-related macular degeneration. Invest Ophthalmol Vis Sci 2011; 52(7): 4459-66.
[http://dx.doi.org/10.1167/iovs.10-6678] [PMID: 21498613]
[56]
Hiscott P, Sheridan C, Magee RM, Grierson I. Matrix and the retinal pigment epithelium in proliferative retinal disease. Prog Retin Eye Res 1999; 18(2): 167-90.
[http://dx.doi.org/10.1016/S1350-9462(98)00024-X] [PMID: 9932282]
[57]
Mousa SA, Lorelli W, Campochiaro PA. Role of hypoxia and extracellular matrix-integrin binding in the modulation of angiogenic growth factors secretion by retinal pigmented epithelial cells. J Cell Biochem 1999; 74(1): 135-43.
[http://dx.doi.org/10.1002/(SICI)1097-4644(19990701)74:1<135: AID-JCB15>3.0.CO;2-#] [PMID: 10381270]
[58]
Steen B, Sejersen S, Berglin L, Seregard S, Kvanta A. Matrix metalloproteinases and metalloproteinase inhibitors in choroidal neovascular membranes. Invest Ophthalmol Vis Sci 1998; 39(11): 2194-200.
[PMID: 9761302]
[59]
Hollborn M, Stathopoulos C, Steffen A, Wiedemann P, Kohen L, Bringmann A. Positive feedback regulation between MMP-9 and VEGF in human RPE cells. Invest Ophthalmol Vis Sci 2007; 48(9): 4360-7.
[http://dx.doi.org/10.1167/iovs.06-1234] [PMID: 17724228]
[60]
Hunt RC, Fox A, al Pakalnis V, et al. Cytokines cause cultured retinal pigment epithelial cells to secrete metalloproteinases and to contract collagen gels. Invest Ophthalmol Vis Sci 1993; 34(11): 3179-86.
[PMID: 8407227]
[61]
Hoffmann S, He S, Ehren M, Ryan SJ, Wiedemann P, Hinton DR. MMP-2 and MMP-9 secretion by rpe is stimulated by angiogenic molecules found in choroidal neovascular membranes. Retina 2006; 26(4): 454-61.
[PMID: 16603966]
[62]
Fiotti N, Pedio M, Battaglia Parodi M, et al. MMP-9 microsatellite polymorphism and susceptibility to exudative form of age-related macular degeneration. Genet Med 2005; 7(4): 272-7.
[http://dx.doi.org/10.1097/01.GIM.0000159903.69597.73] [PMID: 15834245]
[63]
Liutkeviciene R, Lesauskaite V, Sinkunaite-Marsalkiene G, et al. The role of matrix metalloproteinases polymorphisms in age-related macular degeneration. Ophthalmic Genet 2015; 36(2): 149-55.
[http://dx.doi.org/10.3109/13816810.2013.838274] [PMID: 24079541]
[64]
Marin-Castaño ME, Csaky KG, Cousins SW. Nonlethal oxidant injury to human retinal pigment epithelium cells causes cell membrane blebbing but decreased MMP-2 activity. Invest Ophthalmol Vis Sci 2005; 46(9): 3331-40.
[http://dx.doi.org/10.1167/iovs.04-1224] [PMID: 16123437]
[65]
Ahir A, Guo L, Hussain AA, Marshall J. Expression of metalloproteinases from human retinal pigment epithelial cells and their effects on the hydraulic conductivity of Bruch’s membrane. Invest Ophthalmol Vis Sci 2002; 43(2): 458-65.
[PMID: 11818391]
[66]
Elliot S, Catanuto P, Stetler-Stevenson W, Cousins SW. Retinal pigment epithelium protection from oxidant-mediated loss of MMP-2 activation requires both MMP-14 and TIMP-2. Invest Ophthalmol Vis Sci 2006; 47(4): 1696-702.
[http://dx.doi.org/ 10.1167/iovs.05-1258] [PMID: 16565411]
[67]
Or C, Wang J, Kojic L, Cui Z, Matsubara JA. Expression of ADAMs (A Disintegrin and Metalloproteinase) 10 and 17 in human eyes and in experimental models of age related macular degeneration (AMD). IOVS 2014; 55: 3460.
[68]
Park GB, Kim D, Kim YS, et al. Regulation of ADAM10 and ADAM17 by sorafenib inhibits epithelial-to-mesenchymal transition in epstein-barr virus-infected retinal pigment epithelial cells. Invest Ophthalmol Vis Sci 2015; 56(9): 5162-73.
[http://dx.doi.org/10.1167/iovs.14-16058] [PMID: 26244291]
[69]
Saftig P, Reiss K. The “A Disintegrin And Metalloproteases” ADAM10 and ADAM17: novel drug targets with therapeutic potential? Eur J Cell Biol 2011; 90(6-7): 527-35.
[http://dx.doi.org/ 10.1016/j.ejcb.2010.11.005] [PMID: 21194787]
[70]
Sahin U, Weskamp G, Kelly K, et al. Distinct roles for ADAM10 and ADAM17 in ectodomain shedding of six EGFR ligands. J Cell Biol 2004; 164(5): 769-79.
[http://dx.doi.org/10.1083/jcb.200307137] [PMID: 14993236]
[71]
Lim JM, Lee JH, Wee WR, Joo CK. Downregulated expression of ADAM9 in anterior polar cataracts. J Cataract Refract Surg 2002; 28(4): 697-702.
[http://dx.doi.org/10.1016/S0886-3350(01)01236-6] [PMID: 11955914]
[72]
Swendeman S, Mendelson K, Weskamp G, et al. VEGF-A stimulates ADAM17-dependent shedding of VEGFR2 and crosstalk between VEGFR2 and ERK signaling. Circ Res 2008; 103(9): 916-8.
[http://dx.doi.org/10.1161/CIRCRESAHA.108.184416] [PMID: 18818406]
[73]
Weber S, Niessen MT, Prox J, et al. The disintegrin/metalloproteinase Adam10 is essential for epidermal integrity and Notch-mediated signaling. Development 2011; 138(3): 495-505.
[http://dx.doi.org/10.1242/dev.055210] [PMID: 21205794]
[74]
Murthy A, Shao YW, Narala SR, Molyneux SD, Zúñiga-Pflücker JC, Khokha R. Notch activation by the metalloproteinase ADAM17 regulates myeloproliferation and atopic barrier immunity by suppressing epithelial cytokine synthesis. Immunity 2012; 36(1): 105-19.
[http://dx.doi.org/10.1016/j.immuni.2012.01.005] [PMID: 22284418]
[75]
Parry DA, Toomes C, Bida L, et al. Loss of the metalloprotease ADAM9 leads to cone-rod dystrophy in humans and retinal degeneration in mice. Am J Hum Genet 2009; 84(5): 683-91.
[http://dx.doi.org/10.1016/j.ajhg.2009.04.005] [PMID: 19409519]
[76]
Majka S, McGuire PG, Das A. Regulation of matrix metalloproteinase expression by tumor necrosis factor in a murine model of retinal neovascularization. Invest Ophthalmol Vis Sci 2002; 43(1): 260-6.
[PMID: 11773040]
[77]
Jin M, He S, Wörpel V, Ryan SJ, Hinton DR. Promotion of adhesion and migration of RPE cells to provisional extracellular matrices by TNF-alpha. Invest Ophthalmol Vis Sci 2000; 41(13): 4324-32.
[PMID: 11095634]
[78]
Bevitt DJ, Mohamed J, Catterall JB, et al. Expression of ADAMTS metalloproteinases in the retinal pigment epithelium derived cell line ARPE-19: transcriptional regulation by TNFalpha. Biochim Biophys Acta 2003; 1626(1-3): 83-91.
[http://dx.doi.org/10.1016/S0167-4781(03)00047-2] [PMID: 12697333]
[79]
Das A, McGuire PG. Retinal and choroidal angiogenesis: pathophysiology and strategies for inhibition. Prog Retin Eye Res 2003; 22(6): 721-48.
[http://dx.doi.org/10.1016/j.preteyeres.2003.08.001] [PMID: 14575722]
[80]
Hackett SF, Campochiaro PA. Modulation of plasminogen activator inhibitor-1 and urokinase in retinal pigmented epithelial cells. Invest Ophthalmol Vis Sci 1993; 34(6): 2055-61.
[PMID: 8491554]
[81]
Kvanta A, Shen WY, Sarman S, Seregard S, Steen B, Rakoczy E. Matrix metalloproteinase (MMP) expression in experimental choroidal neovascularization. Curr Eye Res 2000; 21(3): 684-90.
[http://dx.doi.org/10.1076/0271-3683(200009)2131-RFT684] [PMID: 11120556]
[82]
Lambert V, Munaut C, Jost M, et al. Matrix metalloproteinase-9 contributes to choroidal neovascularization. Am J Pathol 2002; 161(4): 1247-53.
[http://dx.doi.org/10.1016/S0002-9440(10)64401-X] [PMID: 12368198]
[83]
Lambert V, Wielockx B, Munaut C, et al. MMP-2 and MMP-9 synergize in promoting choroidal neovascularization. FASEB J 2003; 17(15): 2290-2.
[http://dx.doi.org/10.1096/fj.03-0113fje] [PMID: 14563686]
[84]
Das A, McLamore A, Song W, McGuire PG. Retinal neovascularization is suppressed with a matrix metalloproteinase inhibitor. Arch Ophthalmol 1999; 117(4): 498-503.
[http://dx.doi.org/10.1001/archopht.117.4.498] [PMID: 10206578]
[85]
Berglin L, Sarman S, van der Ploeg I, et al. Reduced choroidal neovascular membrane formation in matrix metalloproteinase-2-deficient mice. Invest Ophthalmol Vis Sci 2003; 44(1): 403-8.
[http://dx.doi.org/10.1167/iovs.02-0180] [PMID: 12506102]
[86]
Zeng R, Wen F, Zhang X, Su Y. Serum levels of matrix metalloproteinase 2 and matrix metalloproteinase 9 elevated in polypoidal choroidal vasculopathy but not in age-related macular degeneration. Mol Vis 2013; 19: 729-36.
[PMID: 23559867]
[87]
Chau KY, Sivaprasad S, Patel N, Donaldson TA, Luthert PJ, Chong NV. Plasma levels of matrix metalloproteinase-2 and -9 (MMP-2 and MMP-9) in age-related macular degeneration. Eye (Lond) 2008; 22(6): 855-9.
[http://dx.doi.org/10.1038/sj.eye. 6702722x] [PMID: 18597988]
[88]
Tatar O, Adam A, Shinoda K, et al. Matrix metalloproteinases in human choroidal neovascular membranes excised following verteporfin photodynamic therapy. Br J Ophthalmol 2007; 91(9): 1183-9.
[http://dx.doi.org/10.1136/bjo.2007.114769] [PMID: 17475706]
[89]
Jonas JB, Jonas RA, Neumaier M, Findeisen P. Cytokine concentration in aqueous humor of eyes with diabetic macular edema. Retina 2012; 32(10): 2150-7.
[http://dx.doi.org/10.1097/IAE.0b013 e3182576d07] [PMID: 22617833]
[90]
Kwon JW, Choi JA, Jee D. Matrix Metalloproteinase-1 and Matrix Metalloproteinase-9 in the Aqueous Humor of Diabetic Macular Edema Patients. PLoS One 2016; 11(7): e0159720.
[http://dx.doi.org/ 10.1371/journal.pone.0159720] [PMID: 27467659]
[91]
Wang F, Rendahl KG, Manning WC, Quiroz D, Coyne M, Miller SS. AAV-mediated expression of vascular endothelial growth factor induces choroidal neovascularization in rat. Invest Ophthalmol Vis Sci 2003; 44(2): 781-90.
[http://dx.doi.org/10.1167/iovs.02-0281] [PMID: 12556414]
[92]
Witmer AN, Vrensen GF, Van Noorden CJ, Schlingemann RO. Vascular endothelial growth factors and angiogenesis in eye disease. Prog Retin Eye Res 2003; 22(1): 1-29.
[http://dx.doi.org/10.1016/S1350-9462(02)00043-5] [PMID: 12597922]
[93]
Lee S, Jilani SM, Nikolova GV, Carpizo D, Iruela-Arispe ML. Processing of VEGF-A by matrix metalloproteinases regulates bioavailability and vascular patterning in tumors. J Cell Biol 2005; 169(4): 681-91.
[http://dx.doi.org/10.1083/jcb.200409115] [PMID: 15911882]
[94]
Barbolina MV, Stack MSN. Membrane type 1-matrix metalloproteinase: substrate diversity in pericellular proteolysis. Semin Cell Dev Biol 2008; 19(1): 24-33.
[http://dx.doi.org/10.1016/j.semcdb. 2007.06.008] [PMID: 17702616]
[95]
Itoh Y, Ito N, Nagase H, Evans RD, Bird SA, Seiki M. Cell surface collagenolysis requires homodimerization of the membrane-bound collagenase MT1-MMP. Mol Biol Cell 2006; 17(12): 5390-9.
[http://dx.doi.org/10.1091/mbc.e06-08-0740] [PMID: 17050733]
[96]
Camodeca C, Cuffaro D, Nuti E, Rossello A. ADAM metalloproteinases as potential drug targets. Curr Med Chem 2018; 25: 1-26.
[http://dx.doi.org/10.2174/0929867325666180326164104] [PMID: 29589526]
[97]
Edwards DR, Handsley MM, Pennington CJ. The ADAM metalloproteinases. Mol Aspects Med 2008; 29(5): 258-89.
[http://dx.doi.org/10.1016/j.mam.2008.08.001] [PMID: 18762209]
[98]
White JM. ADAMs: modulators of cell-cell and cell-matrix interactions. Curr Opin Cell Biol 2003; 15(5): 598-606.
[http://dx.doi.org/ 10.1016/j.ceb.2003.08.001] [PMID: 14519395]
[99]
Yan X, Lin J, Rolfs A, Luo J. Differential expression of the ADAMs in developing chicken retina. Dev Growth Differ 2011; 53(5): 726-39.
[http://dx.doi.org/10.1111/j.1440-169X.2011.01282.x] [PMID: 21671920]
[100]
Rossello A, Nuti E, Ferrini S, Fabbi M. Targeting ADAM17 Sheddase Activity in Cancer. Curr Drug Targets 2016; 17(16): 1908-27.
[http://dx.doi.org/10.2174/1389450117666160727143618] [PMID: 27469341]
[101]
Maretzky T, Scholz F, Köten B, Proksch E, Saftig P, Reiss K. ADAM10-mediated E-cadherin release is regulated by proinflammatory cytokines and modulates keratinocyte cohesion in eczematous dermatitis. J Invest Dermatol 2008; 128(7): 1737-46.
[http://dx.doi.org/10.1038/sj.jid.5701242] [PMID: 18200054]
[102]
Kelwick R, Desanlis I, Wheeler GN, Edwards DR. The ADAMTS (A Disintegrin and Metalloproteinase with Thrombospondin motifs) family. Genome Biol 2015; 16: 113.
[http://dx.doi.org/ 10.1186/s13059-015-0676-3] [PMID: 26025392]
[103]
Hollyfield JG, Rayborn ME, Midura RJ, Shadrach KG, Acharya S. Chondroitin sulfate proteoglycan core proteins in the interphotoreceptor matrix: a comparative study using biochemical and immunohistochemical analysis. Exp Eye Res 1999; 69(3): 311-22.
[http://dx.doi.org/10.1006/exer.1999.0707] [PMID: 10471339]
[104]
Colige A, Li SW, Sieron AL, Nusgens BV, Prockop DJ, Lapière CM. cDNA cloning and expression of bovine procollagen I N-proteinase: a new member of the superfamily of zinc-metalloproteinases with binding sites for cells and other matrix components. Proc Natl Acad Sci USA 1997; 94(6): 2374-9.
[http://dx.doi.org/10.1073/pnas.94.6.2374] [PMID: 9122202]
[105]
Fernandes RJ, Hirohata S, Engle JM, et al. Procollagen II amino propeptide processing by ADAMTS-3. Insights on dermatosparaxis. J Biol Chem 2001; 276(34): 31502-9.
[http://dx.doi.org/ 10.1074/jbc.M103466200] [PMID: 11408482]
[106]
Wang YS, Friedrichs U, Eichler W, Hoffmann S, Wiedemann P. Inhibitory effects of triamcinolone acetonide on bFGF-induced migration and tube formation in choroidal microvascular endothelial cells. Graefes Arch Clin Exp Ophthalmol 2002; 240(1): 42-8.
[http://dx.doi.org/10.1007/s00417-001-0398-y] [PMID: 11954780]
[107]
Webb AH, Gao BT, Goldsmith ZK, et al. Inhibition of MMP-2 and MMP-9 decreases cellular migration, and angiogenesis in in vitro models of retinoblastoma. BMC Cancer 2017; 17(1): 434.
[http://dx.doi.org/10.1186/s12885-017-3418-y] [PMID: 28633655]
[108]
Becerra EM, Morescalchi F, Gandolfo F, et al. Clinical evidence of intravitreal triamcinolone acetonide in the management of age-related macular degeneration. Curr Drug Targets 2011; 12(2): 149-72.
[http://dx.doi.org/10.2174/138945011794182746] [PMID: 20887246]
[109]
Samtani S, Amaral J, Campos MM, Fariss RN, Becerra SP. Doxycycline-mediated inhibition of choroidal neovascularization. Invest Ophthalmol Vis Sci 2009; 50(11): 5098-106.
[http://dx.doi.org/10.1167/iovs.08-3174] [PMID: 19516001]
[110]
Kim D, Ko HS, Park GB, Hur DY, Kim YS, Yang JW. Vandetanib and ADAM inhibitors synergistically attenuate the pathological migration of EBV-infected retinal pigment epithelial cells by regulating the VEGF-mediated MAPK pathway. Exp Ther Med 2017; 13(4): 1415-25.
[http://dx.doi.org/10.3892/etm.2017.4110] [PMID: 28413487]
[111]
Griffioen AW. AG-3340 (Agouron Pharmaceuticals Inc). IDrugs 2000; 3(3): 336-45.
[PMID: 16103944]
[112]
El Bradey M, Cheng L, Bartsch DU, et al. Preventive versus treatment effect of AG3340, a potent matrix metalloproteinase inhibitor in a rat model of choroidal neovascularization. J Ocul Pharmacol Ther 2004; 20(3): 217-36.
[http://dx.doi.org/10.1089/1080768041223657] [PMID: 15279727]
[113]
Kohri T, Moriwaki M, Nakajima M, Tabuchi H, Shiraki K. Reduction of experimental laser-induced choroidal neovascularization by orally administered BPHA, a selective metalloproteinase inhibitor. Graefes Arch Clin Exp Ophthalmol 2003; 241(11): 943-52.
[http://dx.doi.org/10.1007/s00417-003-0761-2] [PMID: 14586590]
[114]
Das A, McLamore A, Song W, McGuire PG. Retinal neovascularization is suppressed with a matrix metalloproteinase inhibitor. Arch Ophthalmol 1999; 117(4): 498-503.
[http://dx.doi.org/10.1001/archopht.117.4.498] [PMID: 10206578]
[115]
Garcia C, Bartsch DU, Rivero ME, et al. Efficacy of Prinomastat) (AG3340), a matrix metalloprotease inhibitor, in treatment of retinal neovascularization. Curr Eye Res 2002; 24(1): 33-8.
[http://dx.doi.org/10.1076/ceyr.24.1.33.5429] [PMID: 12187492]
[116]
Pasquale TR, Tan JS. Update on antimicrobial agents: new indications of older agents. Expert Opin Pharmacother 2005; 6(10): 1681-91.
[http://dx.doi.org/10.1517/14656566.6.10.1681] [PMID: 16086654]
[117]
Cox CA, Amaral J, Salloum R, et al. Doxycycline’s effect on ocular angiogenesis: an in vivo analysis. Ophthalmology 2010; 117(9): 1782-91.
[http://dx.doi.org/10.1016/j.ophtha.2010.01.037] [PMID: 20605212]
[118]
Su W, Li Z, Lin M, et al. The effect of doxycycline temperature-sensitive hydrogel on inhibiting the corneal neovascularization induced by BFGF in rats. Graefes Arch Clin Exp Ophthalmol 2011; 249(3): 421-7.
[http://dx.doi.org/10.1007/s00417-010-1539-y] [PMID: 20953876]
[119]
Su W, Li Z, Li Y, et al. Doxycycline enhances the inhibitory effects of bevacizumab on corneal neovascularization and prevents its side effects. Invest Ophthalmol Vis Sci 2011; 52(12): 9108-15.
[http://dx.doi.org/10.1167/iovs.11-7255] [PMID: 22039247]
[120]
Su W, Li Z, Li F, Chen X, Wan Q, Liang D. Doxycycline-mediated inhibition of corneal angiogenesis: an MMP-independent mechanism. Invest Ophthalmol Vis Sci 2013; 54(1): 783-8.
[http://dx.doi.org/10.1167/iovs.12-10323] [PMID: 23249709]
[121]
García RA, Pantazatos DP, Gessner CR, Go KV, Woods VL Jr, Villarreal FJ. Molecular interactions between matrilysin and the matrix metalloproteinase inhibitor doxycycline investigated by deuterium exchange mass spectrometry. Mol Pharmacol 2005; 67(4): 1128-36.
[http://dx.doi.org/10.1124/mol.104.006346] [PMID: 15665254]
[122]
Inoue K, Torimura T, Nakamura T, et al. Vandetanib, an inhibitor of VEGF receptor-2 and EGF receptor, suppresses tumor development and improves prognosis of liver cancer in mice. Clin Cancer Res 2012; 18(14): 3924-33.
[http://dx.doi.org/10.1158/1078-0432.CCR-11-2041] [PMID: 22611027]
[123]
Bressler NM. Photodynamic therapy of subfoveal choroidal neovascularization in age-related macular degeneration with verteporfin: two-year results of 2 randomized clinical trials-tap report 2. Arch Ophthalmol 2001; 119(2): 198-207.
[PMID: 11176980]
[124]
Verteporfin therapy of subfoveal choroidal neovascularization in age-related macular degeneration: two-year results of a randomized clinical trial including lesions with occult with no classic choroidal neovascularization--verteporfin in photodynamic therapy report 2. Am J Ophthalmol 2001; 131(5): 541-60.
[http://dx.doi.org/10.1016/S0002-9394(01)00967-9] [PMID: 11336929]
[125]
Tatar O, Adam A, Shinoda K, et al. Matrix metalloproteinases in human choroidal neovascular membranes excised following verteporfin photodynamic therapy. Br J Ophthalmol 2007; 91(9): 1183-9.
[http://dx.doi.org/10.1136/bjo.2007.114769] [PMID: 17475706]
[126]
Zhu WH, Guo X, Villaschi S, Francesco Nicosia R. Regulation of vascular growth and regression by matrix metalloproteinases in the rat aorta model of angiogenesis. Lab Invest 2000; 80(4): 545-55.
[http://dx.doi.org/10.1038/labinvest.3780060] [PMID: 10780671]
[127]
Zhang JJ, Sun Y, Hussain AA, Marshall J. Laser-mediated activation of human retinal pigment epithelial cells and concomitant release of matrix metalloproteinases. Invest Ophthalmol Vis Sci 2012; 53(6): 2928-37.
[http://dx.doi.org/10.1167/iovs.11-8585] [PMID: 22447861]

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