miRNAs as potential therapeutic targets for age-related macular degeneration

Future Medicinal Chemistry

Volumn 4, Issue 3, 2012, Pages 277-287

  Wang, Shusheng ^a   Koster, Kyle M ^a   He, Yuguang ^a   Zhou, Qinbo ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; MICRORNA 146A; MICRORNA 150; MICRORNA 21; MICRORNA 23; MICRORNA 23A; MICRORNA 27; MICRORNA 31; UNCLASSIFIED DRUG; UNTRANSLATED RNA;

ANGIOGENESIS; GEOGRAPHIC ATROPHY; HUMAN; IMMUNE RESPONSE; INFLAMMATION; MOLECULARLY TARGETED THERAPY; NONHUMAN; OXIDATIVE STRESS; PIGMENT EPITHELIUM; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN TARGETING; RETINA MACULA AGE RELATED DEGENERATION; REVIEW; SUBRETINAL NEOVASCULARIZATION;

ANIMALS; CHOROIDAL NEOVASCULARIZATION; DRUG DISCOVERY; HUMANS; INFLAMMATION; MACULA LUTEA; MACULAR DEGENERATION; MICRORNAS; OXIDATIVE STRESS;

EID: 84863247480     PISSN: 17568919     EISSN: 17568927     Source Type: Journal    
DOI: 10.4155/fmc.11.176     Document Type: Review

References (105)

1. Ambati J, Ambati BK, Yoo SH, Ianchulev S, Adamis AP. Age-related macular degeneration: etiology, pathogenesis and therapeutic strategies. Surv. Ophthalmol. 48(3), 257-293 (2003).
2. Friedman DS, O'Colmain BJ, Munoz B et al. Prevalence of age-related macular degeneration in the United States. Arch. Ophthalmol. 122(4), 564-572 (2004).
3. de Jong PT. Age-related macular degeneration. N. Engl. J. Med. 355(14), 1474-1485 (2006).
4. Jager RD, Mieler WF, Miller JW. Age-related macular degeneration. N. Engl. J. Med. 358(24), 2606-2617 (2008).
5. Ding X, Patel M, Chan CC. Molecular pathology of age-related macular degeneration. Prog. Retin. Eye Res. 28(1), 1-18 (2009).
6. Beatty S, Koh H, Phil M, Henson D, Boulton M. The role of oxidative stress in the pathogenesis of age-related macular degeneration. Surv. Ophthalmol. 45(2), 115-134 (2000).
7. Solberg Y, Rosner M, Belkin M. The association between cigarette smoking and ocular diseases. Surv. Ophthalmol. 42(6), 535-547 (1998).
8. Smith W, Mitchell P, Leeder SR. Smoking and age-related maculopathy. The Blue Mountains Eye Study. Arch. Ophthalmol. 114(12), 1518-1523 (1996).
9. McGeer PL, McGeer EG. Inflammation and the degenerative diseases of aging. Ann. NY Acad. Sci. 1035, 104-116 (2004).
10. Sarks JP, Sarks SH, Killingsworth MC. Evolution of geographic atrophy of the retinal pigment epithelium. Eye 2(Pt 5), 552-577 (1988).
11. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism and function. Cell 116(2), 281-297 (2004).
12. Winter J, Jung S, Keller S, Gregory RI, Diederichs S. Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat. Cell Biol. 11(3), 228-234 (2009).
13. Lanford RE, Hildebrandt-Eriksen ES, Petri A et al. Therapeutic silencing of microRNA-122 in primates with chronic hepatitis C virus infection. Science 327(5962), 198-201 (2010).
14. Krutzfeldt J, Rajewsky N, Braich R et al. Silencing of microRNAs in vivo with 'antagomirs'. Nature 438(7068), 685-689 (2005).
15. Brown DM, Kaiser PK, Michels M et al. Ranibizumab versus verteporfin for neovascular age-related macular degeneration. N. Engl. J. Med. 355(14), 1432-1444 (2006).
16. Rosenfeld PJ, Brown DM, Heier JS et al. Ranibizumab for neovascular age-related macular degeneration. N. Engl. J. Med. 355(14), 1419-1431 (2006).
17. Mitchell P. A systematic review of the efficacy and safety outcomes of anti-VEGF agents used for treating neovascular age-related macular degeneration: comparison of ranibizumab and bevacizumab. Curr. Med. Res. Opin 27(7), 1465-1475 (2011).
18. Pieramici DJ, Rabena MD. Anti-VEGF therapy: comparison of current and future agents. Eye 22(10), 1330-1336 (2008).
19. Wang S, Olson EN. AngiomiRs - key regulators of angiogenesis. Curr. Opin Genet. Dev. 19(3), 205-211 (2009).
20. Zhou Q, Gallagher R, Ufret-Vincenty R, Li X, Olson EN, Wang S. Regulation of angiogenesis and choroidal neovascularization by members of microRNA-23-27-24 clusters. Proc. Natl Acad. Sci. USA 108(20), 8287-8292 (2011). Reports that inhibition of miR-23 and miR-27 represses laser-induced choroidal neovascularization (CNV) in mice.
21. Shen J, Yang X, Xie B et al. MicroRNAs regulate ocular neovascularization. Mol. Ther. 16(7), 1208-1216 (2008). Reports that overexpression of miR-31 or miR-150 represses laser-induced CNV in mice.
22. Calin GA, Dumitru CD, Shimizu M et al. Frequent deletions and down-regulation of micro-RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc. Natl Acad. Sci. USA 99(24), 15524-15529 (2002).
23. Yamakuchi M, Lotterman CD, Bao C et al. P53-induced microRNA-107 inhibits HIF-1 and tumor angiogenesis. Proc. Natl Acad. Sci. USA 107(14), 6334-6339 (2010).
24. Dews M, Homayouni A, Yu D et al. Augmentation of tumor angiogenesis by a Myc-activated microRNA cluster. Nat. Genet. 38(9), 1060-1065 (2006).
25. Anand S, Majeti BK, Acevedo LM et al. MicroRNA-132-mediated loss of p120RasGAP activates the endothelium to facilitate pathological angiogenesis. Nat. Med. 16(8), 909-914 (2010).
26. Wurdinger T, Tannous BA, Saydam O et al. miR-296 regulates growth factor receptor overexpression in angiogenic endothelial cells. Cancer Cell 14(5), 382-393 (2008).
27. Lee DY, Deng Z, Wang CH, Yang BB. MicroRNA-378 promotes cell survival, tumor growth, and angiogenesis by targeting SuFu and Fus-1 expression. Proc. Natl Acad. Sci. USA 104(51), 20350-20355 (2007).
28. Cha ST, Chen PS, Johansson G et al. MicroRNA-519c suppresses hypoxia-inducible factor-1α expression and tumor angiogenesis. Cancer Res. 70(7), 2675-2685 (2010).
29. Liu LZ, Li C, Chen Q et al. MiR-21 induced angiogenesis through AKT and ERK activation and HIF-1α expression. PLoS ONE 6(4), e19139 (2011).
30. Fasanaro P, D'Alessandra Y, Di Stefano V et al. MicroRNA-210 modulates endothelial cell response to hypoxia and inhibits the receptor tyrosine kinase ligand Ephrin-A3. J. Biol. Chem. 283(23), 15878-15883 (2008).
31. Hua Z, Lv Q, Ye W et al. MiRNA-directed regulation of VEGF and other angiogenic factors under hypoxia. PLoS ONE 1, e116. (2006).
32. Kulshreshtha R, Ferracin M, Wojcik SE et al. A microRNA signature of hypoxia. Mol. Cell. Biol. 27(5), 1859-1867 (2007).
33. Devlin C, Greco S, Martelli F, Ivan M. miR--210: more than a silent player in hypoxia. IUBMB Life 63(2), 94-100 (2011).
34. Dentelli P, Rosso A, Orso F, Olgasi C, Taverna D, Brizzi MF. microRNA-222 controls neovascularization by regulating signal transducer and activator of transcription 5A expression. Arterioscler. Thromb. Vasc. Biol. 30(8), 1562-1568 (2010).
35. Grundmann S, Hans FP, Kinniry S et al. MicroRNA-100 regulates neovascularization by suppression of mammalian target of rapamycin in endothelial and vascular smooth muscle cells. Circulation 123(9), 999-1009 (2011).
36. Wang S, Aurora AB, Johnson BA et al. The endothelial-specific microRNA miR-126 governs vascular integrity and angiogenesis. Dev. Cell 15(2), 261-271 (2008).
37. Fish JE, Santoro MM, Morton SU et al. miR--126 regulates angiogenic signaling and vascular integrity. Dev. Cell 15(2), 272-284 (2008).
38. Kuhnert F, Mancuso MR, Hampton J et al. Attribution of vascular phenotypes of the murine Egfl7 locus to the microRNA miR-126. Development 135(24), 3989-3993 (2008).
39. van Solingen C, Seghers L, Bijkerk R et al. Antagomir-mediated silencing of endothelial cell specific microRNA-126 impairs ischemia-induced angiogenesis. J. Cell. Mol. Med. 13(8A), 1577-1585 (2009).
40. Ryan SJ. Subretinal neovascularization. Natural history of an experimental model. Arch. Ophthalmol. 100(11), 1804-1809 (1982).
41. Sabatel C, Malvaux L, Bovy N et al. MicroRNA-21 exhibits antiangiogenic function by targeting RhoB expression in endothelial cells. PLoS ONE 6(2), e16979 (2011). Reports that overexpression of miR-21 represses laser-induced CNV in mice.
42. Imamura Y, Noda S, Hashizume K et al. Drusen, choroidal neovascularization, and retinal pigment epithelium dysfunction in SOD1-deficient mice: a model of age-related macular degeneration. Proc. Natl Acad. Sci. USA 103(30), 11282-11287 (2006).
43. Justilien V, Pang JJ, Renganathan K et al. SOD2 knockdown mouse model of early AMD. Invest. Ophthalmol. Vis. Sci. 48(10), 4407-4420 (2007).
44. Lin H, Qian J, Castillo AC et al. Effect of miR-23 on oxidant-induced injury in human retinal pigment epithelial cells. Invest. Ophthalmol. Vis. Sci. 52(9), 6308-6314 (2011).
45. Hinton DR, He S, Lopez PF. Apoptosis in surgically excised choroidal neovascular membranes in age-related macular degeneration. Arch. Ophthalmol. 116(2), 203-209 (1998).
46. Dunaief JL, Dentchev T, Ying GS, Milam AH. The role of apoptosis in age-related macular degeneration. Arch. Ophthalmol. 120(11), 1435-1442 (2002).
47. Thulasingam S, Massilamany C, Gangaplara A et al. miR-27b*, an oxidative stress-responsive microRNA modulates nuclear factor-κB pathway in RAW 264.7 cells. Mol. Cell Biochem. 352(1-2), 181-188 (2011).
48. Mutharasan RK, Nagpal V, Ichikawa Y, Ardehali H. MicroRNA-210 is upregulated in hypoxic cardiomyocytes through Akt- and p53-dependent pathways and exerts cytoprotective effects. Am. J. Physiol. Heart Circ. Physiol. 301(4), H1519-H1530 (2011).
49. Chen Z, Li Y, Zhang H, Huang P, Luthra R. Hypoxia-regulated microRNA-210 modulates mitochondrial function and decreases ISCU and COX10 expression. Oncogene 29(30), 4362-4368 (2010).
50. Favaro E, Ramachandran A, McCormick R et al. MicroRNA-210 regulates mitochondrial free radical response to hypoxia and krebs cycle in cancer cells by targeting iron sulfur cluster protein ISCU. PLoS ONE 5(4), e10345 (2010).
51. Cheng Y, Liu X, Zhang S, Lin Y, Yang J, Zhang C. MicroRNA-21 protects against the H(2)O(2)-induced injury on cardiac myocytes via its target gene PDCD4. J. Mol. Cell Cardiol. 47(1), 5-14 (2009).
52. Fleissner F, Jazbutyte V, Fiedler J et al. Short communication: asymmetric dimethylarginine impairs angiogenic progenitor cell function in patients with coronary artery disease through a microRNA-21-dependent mechanism. Circ. Res. 107(1), 138-143 (2010).
53. Magenta A, Cencioni C, Fasanaro P et al. miR-200c is upregulated by oxidative stress and induces endothelial cell apoptosis and senescence via ZEB1 inhibition. Cell Death Differ. 18(10), 1628-1639 (2011).
54. Li G, Luna C, Qiu J, Epstein DL, Gonzalez P. Role of miR-204 in the regulation of apoptosis, endoplasmic reticulum stress response, and inflammation in human trabecular meshwork cells. Invest. Ophthalmol. Vis. Sci. 52(6), 2999-3007 (2011).
55. Jian X, Xiao-yan Z, Bin H et al. miR-204 regulate cardiomyocyte autophagy induced by hypoxia-reoxygenation through LC3-II. Int. J. Cardiol. 148(1), 110-112 (2011).
56. Walker JC, Harland RM. microRNA-24a is required to repress apoptosis in the developing neural retina. Genes Dev. 23(9), 1046-1051 (2009).
57. Qian L, Van Laake LW, Huang Y, Liu S, Wendland MF, Srivastava D. miR-24 inhibits apoptosis and represses Bim in mouse cardiomyocytes. J. Exp. Med. 208(3), 549-560 (2011).
58. Kim YM, Pae HO, Park JE et al. Heme oxygenase in the regulation of vascular biology: from molecular mechanisms to therapeutic opportunities. Antioxid. Redox Signal. 14(1), 137-167 (2011).
59. Synowiec E, Szaflik J, Chmielewska M et al. An association between polymorphism of the heme oxygenase-1 and -2 genes and age-related macular degeneration. Mol. Biol. Rep. 39(3), 2081-2087 (2011).
60. Chang CL, Au LC, Huang SW, Fai Kwok C, Ho LT, Juan CC. Insulin up-regulates heme oxygenase-1 expression in 3T3-L1 adipocytes via PI3-kinase- and PKC-dependent pathways and heme oxygenase-1-associated microRNA downregulation. Endocrinology 152(2), 384-393 (2011).
61. Beckman JD, Chen C, Nguyen J et al. Regulation of heme oxygenase-1 protein expression by miR-377 in combination with miR-217. J. Biol. Chem. 286(5), 3194-3202 (2011).
62. Donoso LA, Kim D, Frost A, Callahan A, Hageman G. The role of inflammation in the pathogenesis of age-related macular degeneration. Surv. Ophthalmol. 51(2), 137-152 (2006).
63. Walport MJ. Complement. Second of two parts. N. Engl. J. Med. 344(15), 1140-1144 (2001).
64. Walport MJ. Complement. First of two parts. N. Engl. J. Med. 344(14), 1058-1066 (2001).
65. Klein RJ, Zeiss C, Chew EY et al. Complement factor H polymorphism in age-related macular degeneration. Science 308(5720), 385-389 (2005).
66. Edwards AO, Ritter R 3rd, Abel KJ, Manning A, Panhuysen C, Farrer LA. Complement factor H polymorphism and age-related macular degeneration. Science 308(5720), 421-424 (2005).
67. Haines JL, Hauser MA, Schmidt S et al. Complement factor H variant increases the risk of age-related macular degeneration. Science 308(5720), 419-421 (2005).
68. 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. 38(4), 458-462 (2006).
69. Yates JR, Sepp T, Matharu BK et al. Complement C3 variant and the risk of age-related macular degeneration. N. Engl. J. Med. 357(6), 553-561 (2007).
70. Tuo J, Smith BC, Bojanowski CM et al. The involvement of sequence variation and expression of CX3CR1 in the pathogenesis of age-related macular degeneration. FASEB J. 18(11), 1297-1299 (2004).
71. Chan CC, Ross RJ, Shen D et al. Ccl2/Cx3cr1-deficient mice: an animal model for age-related macular degeneration. Ophthalmic Res. 40(3-4), 124-128 (2008).
72. Ambati J, Anand A, Fernandez S et al. An animal model of age-related macular degeneration in senescent Ccl-2- or Ccr-2-deficient mice. Nat. Med. 9(11), 1390-1397 (2003).
73. Csaky K, Baffi J, Chan CC, Byrnes GA. Clinicopathologic correlation of progressive fibrovascular proliferation associated with occult choroidal neovascularization in age-related macular degeneration. Arch. Ophthalmol. 122(4), 650-652 (2004).
74. Grossniklaus HE, Ling JX, Wallace TM et al. Macrophage and retinal pigment epithelium expression of angiogenic cytokines in choroidal neovascularization. Mol. Vis. 8, 119-126 (2002).
75. Grisanti S, Tatar O. The role of vascular endothelial growth factor and other endogenous interplayers in age-related macular degeneration. Prog. Retin. Eye Res. 27(4), 372-390 (2008).
76. Espinosa-Heidmann DG, Suner IJ, Hernandez EP, Monroy D, Csaky KG, Cousins SW. Macrophage depletion diminishes lesion size and severity in experimental choroidal neovascularization. Invest. Ophthalmol. Vis. Sci. 44(8), 3586-3592 (2003).
77. Apte RS, Richter J, Herndon J, Ferguson TA. Macrophages inhibit neovascularization in a murine model of age-related macular degeneration. PLoS Med. 3(8), e310 (2006).
78. Sakurai E, Anand A, Ambati BK, van Rooijen N, Ambati J. Macrophage depletion inhibits experimental choroidal neovascularization. Invest. Ophthalmol. Vis. Sci. 44(8), 3578-3585 (2003).
79. Sonkoly E, Stahle M, Pivarcsi A. MicroRNAs and immunity: novel players in the regulation of normal immune function and inflammation. Semin. Cancer Biol. 18(2), 131-140 (2008).
80. Moschos SA, Williams AE, Perry MM, Birrell MA, Belvisi MG, Lindsay MA. Expression profiling in vivo demonstrates rapid changes in lung microRNA levels following lipopolysaccharide-induced inflammation but not in the anti-inflammatory action of glucocorticoids. BMC Genomics 8, 240 (2007).
81. Taganov KD, Boldin MP, Chang KJ, Baltimore D. NF-κB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc. Natl Acad. Sci. USA 103(33), 12481-12486 (2006).
82. Bhaumik D, Scott GK, Schokrpur S et al. MicroRNAs miR-146a/b negatively modulate the senescence-associated inflammatory mediators IL-6 and IL-8. Aging 1(4), 402-411 (2009).
83. Perry MM, Moschos SA, Williams AE, Shepherd NJ, Larner-Svensson HM, Lindsay MA. Rapid changes in microRNA-146a expression negatively regulate the IL-1β-induced inflammatory response in human lung alveolar epithelial cells. J. Immunol. 180(8), 5689-5698 (2008).
84. Yang K, He YS, Wang XQ et al. miR-146a inhibits oxidized low-density lipoprotein-induced lipid accumulation and inflammatory response via targeting toll-like receptor 4. FEBS Lett. 585(6), 854-860 (2011).
85. Pogue AI, Li YY, Cui JG et al. Characterization of an NF-κB-regulated, miRNA-146a-mediated down-regulation of complement factor H (CFH) in metal-sulfate-stressed human brain cells. J. Inorg. Biochem. 103(11), 1591-1595 (2009).
86. Kindzelskii AL, Elner VM, Elner SG, Yang D, Hughes BA, Petty HR. Toll-like receptor 4 (TLR4) of retinal pigment epithelial cells participates in transmembrane signaling in response to photoreceptor outer segments. J. Gen. Physiol. 124(2), 139-149 (2004).
87. O'Connell RM, Taganov KD, Boldin MP, Cheng G, Baltimore D. MicroRNA-155 is induced during the macrophage inflammatory response. Proc. Natl Acad. Sci. USA 104(5), 1604-1609 (2007).
88. Huang RS, Hu GQ, Lin B, Lin ZY, Sun CC. MicroRNA-155 silencing enhances inflammatory response and lipid uptake in oxidized low-density lipoprotein-stimulated human THP-1 macrophages. J. Investig. Med. 58(8), 961-967 (2010).
89. Jennewein C, von Knethen A, Schmid T, Brune B. MicroRNA-27b contributes to lipopolysaccharide-mediated peroxisome proliferator-activated receptor gamma (PPARgamma) mRNA destabilization. J. Biol. Chem. 285(16), 11846-11853 (2010).
90. Tili E, Michaille JJ, Cimino A et al. Modulation of miR-155 and miR-125b levels following lipopolysaccharide/TNF-α stimulation and their possible roles in regulating the response to endotoxin shock. J. Immunol. 179(8), 5082-5089 (2007).
91. Gong AY, Zhou R, Hu G et al. MicroRNA-513 regulates B7-H1 translation and is involved in IFN-gamma-induced B7-H1 expression in cholangiocytes. J. Immunol. 182(3), 1325-1333 (2009).
92. Bazzoni F, Rossato M, Fabbri M et al. Induction and regulatory function of miR-9 in human monocytes and neutrophils exposed to proinflammatory signals. Proc. Natl Acad. Sci. USA 106(13), 5282-5287 (2009).
93. Niu Y, Mo D, Qin L et al. Lipopolysaccharide-induced miR-1224 negatively regulates tumour necrosis factor-α gene expression by modulating Sp1. Immunology 133(1), 8-20 (2011).
94. Ponomarev ED, Veremeyko T, Barteneva N, Krichevsky AM, Weiner HL. MicroRNA-124 promotes microglia quiescence and suppresses EAE by deactivating macrophages via the C/EBP-α-PU.1 pathway. Nat. Med. 17(1), 64-70 (2011).
95. Kumar M, Ahmad T, Sharma A et al. Let-7 microRNA-mediated regulation of IL-13 and allergic airway inflammation. J. Allergy Clin. Immunol. 128(5), 1077-1085 e1-e10 (2011).
96. Kaneko H, Dridi S, Tarallo V et al. DICER1 deficit induces Alu RNA toxicity in age-related macular degeneration. Nature 471(7338), 325-330 (2011). Reports the miRNA-independent Dicer function in processing Alu RNA and their involvement in geographic atrophy.
97. Cifuentes D, Xue H, Taylor DW et al. A novel miRNA processing pathway independent of Dicer requires Argonaute2 catalytic activity. Science 328(5986), 1694-1698 (2010).
98. Cheloufi S, Dos Santos CO, Chong MM, Hannon GJ. A Dicer-independent miRNA biogenesis pathway that requires Ago catalysis. Nature 465(7298), 584-589 (2010).
99. Bader AG, Brown D, Winkler M. The promise of microRNA replacement therapy. Cancer Res. 70(18), 7027-7030 (2010).
100. Seto AG. The road toward microRNA therapeutics. Int. J. Biochem. Cell Biol. 42(8), 1298-1305 (2010).
101. Elmen J, Lindow M, Schutz S et al. LNA-mediated microRNA silencing in non-human primates. Nature 452(7189), 896-899 (2008).
102. Ebert MS, Sharp PA. MicroRNA sponges: progress and possibilities. RNA 16(11), 2043-2050 (2010).
103. Krutzfeldt J, Kuwajima S, Braich R et al. Specificity, duplex degradation and subcellular localization of antagomirs. Nucleic Acids Res. 35(9), 2885-2892 (2007).
104. Maguire AM, High KA, Auricchio A et al. Age-dependent effects of RPE65 gene therapy for Leber's congenital amaurosis: a Phase I dose-escalation trial. Lancet 374(9701), 1597-1605 (2009).
105. Mingozzi F, High KA. Therapeutic in vivo gene transfer for genetic disease using AAV: progress and challenges. Nat. Rev. Genet. 12(5), 341-355 (2011).