Correction: Diabetes-induced superoxide anion and breakdown of the blood-retinal barrier: Role of the VEGF/uPAR pathway (PLoS ONE (2013) 8:8 (e71868) DOI: 10.1371/journal.pone.0071868);Diabetes-Induced Superoxide Anion and Breakdown of the Blood-Retinal Barrier: Role of the VEGF/uPAR Pathway

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  El Remessy, Azza B ^a,b,c   Franklin, Telina ^a   Ghaley, Nagla ^a   Yang, Jinling ^a,d   Brands, Michael W ^a   Caldwell, Ruth B ^a,c   Behzadian, Mohamed Ali ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b UNIVERSITY OF GEORGIA   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; GELATINASE B; GLYCOGEN SYNTHASE KINASE 3BETA; SUPEROXIDE; SUPEROXIDE DISMUTASE; UROKINASE; VASCULOTROPIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD RETINA BARRIER; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; DIABETES MELLITUS; DIABETIC RETINOPATHY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; MALE; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TRANSPORT; RAT; RETINA CELL; SIGNAL TRANSDUCTION;

MUS; RATTUS;

ANIMALS; ANTIOXIDANTS; BETA CATENIN; BLOOD-RETINAL BARRIER; BLOTTING, WESTERN; CAPILLARY PERMEABILITY; CATTLE; CELL MEMBRANE PERMEABILITY; CELLS, CULTURED; CYCLIC N-OXIDES; DIABETES MELLITUS, EXPERIMENTAL; ENDOTHELIAL CELLS; GLUCOSE; GLYCOGEN SYNTHASE KINASE 3; MALE; MICE; MICE, INBRED C57BL; RATS; RECEPTORS, UROKINASE PLASMINOGEN ACTIVATOR; RETINAL VESSELS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SPIN LABELS; SUPEROXIDE DISMUTASE; SUPEROXIDES; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84881345617     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0186749     Document Type: Erratum

References (48)

1. Cunha-Vaz JG, (1978) Pathophysiology of diabetic retinopathy. Br J Ophthalmol 62: 351-355. doi:10.1136/bjo.62.6.351. PubMed: 666982.
2. Gardner TW, Antonetti DA, Barber AJ, LaNoue KF, Levison SW, (2002) Diabetic retinopathy: more than meets the eye. Surv Ophthalmol 47 (Suppl 2):: S253-S262. doi:10.1016/S0039-6257(02)00387-9. PubMed: 12507627.
3. Tilton RG, (2002) Diabetic vascular dysfunction: links to glucose-induced reductive stress and VEGF. Microsc Res Tech 57: 390-407. doi:10.1002/jemt.10092. PubMed: 12112445.
4. El-Remessy AB, Behzadian MA, Abou-Mohamed G, Franklin T, Caldwell RW, et al. (2003) Experimental diabetes causes breakdown of the blood-retina barrier by a mechanism involving tyrosine nitration and increases in expression of vascular endothelial growth factor and urokinase plasminogen activator receptor. Am J Pathol 162: 1995-2004. doi:10.1016/S0002-9440(10)64332-5. PubMed: 12759255.
5. Malecaze F, Clamens S, Simorre-Pinatel V, Mathis A, Chollet P, et al. (1994) Detection of vascular endothelial growth factor messenger RNA and vascular endothelial growth factor-like activity in proliferative diabetic retinopathy. Arch Ophthalmol 112: 1476-1482. doi:10.1001/archopht.1994.01090230090028. PubMed: 7980139.
6. Murata T, Ishibashi T, Khalil A, Hata Y, Yoshikawa H, et al. (1995) Vascular endothelial growth factor plays a role in hyperpermeability of diabetic retinal vessels. Ophthal Res 27: 48-52. doi:10.1159/000267567. PubMed: 7596559.
7. Caldwell RB, Bartoli M, Behzadian MA, El-Remessy AE, Al-Shabrawey M, et al. (2005) Vascular endothelial growth factor and diabetic retinopathy: role of oxidative stress. Curr Drug Targets 6: 511-524. doi:10.2174/1389450054021981. PubMed: 16026270.
8. El-Remessy AB, Al-Shabrawey M, Khalifa Y, Tsai NT, Caldwell RB, et al. (2006) Neuroprotective and blood-retinal barrier-preserving effects of cannabidiol in experimental diabetes. Am J Pathol 168: 235-244. doi:10.2353/ajpath.2006.050500. PubMed: 16400026.
9. Platt DH, Bartoli M, El-Remessy AB, Al-Shabrawey M, Lemtalsi T, et al. (2005) Peroxynitrite increases VEGF expression in vascular endothelial cells via STAT3. Free Radic Biol Med 39: 1353-1361. doi:10.1016/j.freeradbiomed.2005.06.015. PubMed: 16257644.
10. El-Remessy AB, Abou-Mohamed G, Caldwell RW, Caldwell RB, (2003) High glucose-induced tyrosine nitration in endothelial cells: role of eNOS uncoupling and aldose reductase activation. Invest Ophthalmol Vis Sci 44: 3135-3143. doi:10.1167/iovs.02-1022. PubMed: 12824263.
11. Kowluru RA, Kowluru V, Xiong Y, Ho YS, (2006) Overexpression of mitochondrial superoxide dismutase in mice protects the retina from diabetes-induced oxidative stress. Free Radic Biol Med 41: 1191-1196. doi:10.1016/j.freeradbiomed.2006.01.012. PubMed: 17015165.
12. Goto H, Nishikawa T, Sonoda K, Kondo T, Kukidome D, et al. (2008) Endothelial MnSOD overexpression prevents retinal VEGF expression in diabetic mice. Biochem Biophys Res Commun 366: 814-820. doi:10.1016/j.bbrc.2007.12.041. PubMed: 18083119.
13. Ali TK, El-Remessy AB, (2009) Diabetic retinopathy: current management and experimental therapeutic targets. Pharmacotherapy 29: 182-192. doi:10.1592/phco.29.2.182. PubMed: 19170588.
14. Behzadian MA, Windsor LJ, Ghaly N, Liou G, Tsai NT, et al. (2003) VEGF-induced paracellular permeability in cultured endothelial cells involves urokinase and its receptor. FASEB J 17: 752-754. PubMed: 12594181.
15. Navaratna D, Menicucci G, Maestas J, Srinivasan R, McGuire P, et al. (2008) A peptide inhibitor of the urokinase/urokinase receptor system inhibits alteration of the blood-retinal barrier in diabetes. FASEB J 22: 3310-3317. doi:10.1096/fj.08-110155. PubMed: 18559877.
16. Yang J, Caldwell RB, Behzadian MA, (2012) Blockade of VEGF-induced GSK/beta-catenin signaling, uPAR expression and increased permeability by dominant negative p38alpha. Exp Eye Res 100: 101-108. doi:10.1016/j.exer.2012.03.011. PubMed: 22564969.
17. Yang J, Duh EJ, Caldwell RB, Behzadian MA, (2010) Antipermeability function of PEDF involves blockade of the MAP kinase/GSK/beta-catenin signaling pathway and uPAR expression. Invest Ophthalmol Vis Sci 51: 3273-3280. doi:10.1167/iovs.08-2878. PubMed: 20089873.
18. Pepper MS, (2001) Role of the matrix metalloproteinase and plasminogen activator-plasmin systems in angiogenesis. Arterioscler Thromb Vasc Biol 21: 1104-1117. doi:10.1161/hq0701.093685. PubMed: 11451738.
19. Ellis V, Behrendt N, Danø K, (1991) Plasminogen activation by receptor-bound urokinase. A kinetic study with both cell-associated and isolated receptor. J Biol Chem 266: 12752-12758. PubMed: 1829461.
20. Giebel SJ, Menicucci G, McGuire PG, Das A, (2005) Matrix metalloproteinases in early diabetic retinopathy and their role in alteration of the blood-retinal barrier. Lab Invest 85: 597-607. doi:10.1038/labinvest.3700251. PubMed: 15711567.
21. Dejana E, Corada M, Lampugnani MG, (1995) Endothelial cell-to-cell junctions. FASEB J 9: 910-918. PubMed: 7615160.
22. Lampugnani MG, Corada M, Caveda L, Breviario F, Ayalon O, et al. (1995) The molecular organization of endothelial cell to cell junctions: differential association of plakoglobin, beta-catenin, and alpha- catenin with vascular endothelial cadherin (VE-cadherin). J Cell Biol 129: 203-217. doi:10.1083/jcb.129.1.203. PubMed: 7698986.
23. Sadot E, Simcha I, Iwai K, Ciechanover A, Geiger B, et al. (2000) Differential interaction of plakoglobin and beta-catenin with the ubiquitin-proteasome system. Oncogene 19: 1992-2001. doi:10.1038/sj.onc.1203519. PubMed: 10803460.
24. Aberle H, Bauer A, Stappert J, Kispert A, Kemler R, (1997) beta-catenin is a target for the ubiquitin-proteasome pathway. EMBO J 16: 3797-3804. doi:10.1093/emboj/16.13.3797. PubMed: 9233789.
25. Mann B, Gelos M, Siedow A, Hanski ML, Gratchev A, et al. (1999) Target genes of beta-catenin-T cell-factor/lymphoid-enhancer-factor signaling in human colorectal carcinomas. Proc Natl Acad Sci U S A 96: 1603-1608. doi:10.1073/pnas.96.4.1603. PubMed: 9990071.
26. Behzadian MA, Wang XL, Windsor LJ, Ghaly N, Caldwell RB, (2001) TGF-beta increases retinal endothelial cell permeability by increasing MMP-9: possible role of glial cells in endothelial barrier function. Invest Ophthalmol Vis Sci 42: 853-859. PubMed: 11222550.
27. Brands MW, Bell TD, Gibson B, (2004) Nitric oxide may prevent hypertension early in diabetes by counteracting renal actions of superoxide. Hypertension 43: 57-63. PubMed: 14656952.
28. Al-Shabrawey M, Rojas M, Sanders T, Behzadian A, El-Remessy A, et al. (2008) Role of NADPH oxidase in retinal vascular inflammation. Invest Ophthalmol Vis Sci 49: 3239-3244. doi:10.1167/iovs.08-1755. PubMed: 18378574.
29. Mohamed IN, Soliman SA, Alhusban A, Matragoon S, Pillai BA, et al. (2012) Diabetes exacerbates retinal oxidative stress, inflammation, and microvascular degeneration in spontaneously hypertensive rats. Mol Vis 18: 1457-1466. PubMed: 22736937.
30. Navaratna D, McGuire PG, Menicucci G, Das A, (2007) Proteolytic degradation of VE-cadherin alters the blood-retinal barrier in diabetes. Diabetes 56: 2380-2387. doi:10.2337/db06-1694. PubMed: 17536065.
31. Zou MH, Li H, He C, Lin M, Lyons TJ, et al. (2011) Tyrosine nitration of prostacyclin synthase is associated with enhanced retinal cell apoptosis in diabetes. Am J Pathol 179: 2835-2844. doi:10.1016/j.ajpath.2011.08.041. PubMed: 22015457.
32. Byrne AM, Bouchier-Hayes DJ, Harmey JH, (2005) Angiogenic and cell survival functions of vascular endothelial growth factor (VEGF). J Cell Mol Med 9: 777-794. doi:10.1111/j.1582-4934.2005.tb00379.x. PubMed: 16364190.
33. Bartoli M, Platt D, Lemtalsi T, Gu X, Brooks SE, et al. (2003) VEGF differentially activates. Stat 3 in microvascular endothelial cells. Faseb J 17: 1562-1564.
34. Penn JS, Madan A, Caldwell RB, Bartoli M, Caldwell RW, et al. (2008) Vascular endothelial growth factor in eye disease. Prog Retin Eye Res 27: 331-371. doi:10.1016/j.preteyeres.2008.05.001. PubMed: 18653375.
35. Kowluru RA, (2010) Role of matrix metalloproteinase-9 in the development of diabetic retinopathy and its regulation by H-Ras. Invest Ophthalmol Vis Sci 51: 4320-4326. doi:10.1167/iovs.09-4851. PubMed: 20220057.
36. Kowluru RA, Mohammad G, Dos Santos JM, Zhong Q, (2011) Abrogation of MMP-9 Gene Protects Against the Development of Retinopathy in Diabetic Mice by Preventing Mitochondrial Damage. Diabetes, 60: 3023-33. PubMed: 21933988.
37. Chronopoulos A, Tang A, Beglova E, Trackman PC, Roy S, (2010) High glucose increases lysyl oxidase expression and activity in retinal endothelial cells: mechanism for compromised extracellular matrix barrier function. Diabetes 59: 3159-3166. doi:10.2337/db10-0365. PubMed: 20823103.
38. Roy S, Ha J, Trudeau K, Beglova E, (2010) Vascular basement membrane thickening in diabetic retinopathy. Curr Eye Res 35: 1045-1056. doi:10.3109/02713683.2010.514659. PubMed: 20929292.
39. Das A, McGuire PG, Eriqat C, Ober RR, DeJuan E Jr., et al. (1999) Human diabetic neovascular membranes contain high levels of urokinase and metalloproteinase enzymes. Invest Ophthalmol Vis Sci 40: 809-813. PubMed: 10067990.
40. Noda K, Ishida S, Inoue M, Obata K, Oguchi Y, et al. (2003) Production and activation of matrix metalloproteinase-2 in proliferative diabetic retinopathy. Invest Ophthalmol Vis Sci 44: 2163-2170. doi:10.1167/iovs.02-0662. PubMed: 12714657.
41. Prager GW, Breuss JM, Steurer S, Mihaly J, Binder BR, (2004) Vascular endothelial growth factor (VEGF) induces rapid prourokinase (pro-uPA) activation on the surface of endothelial cells. Blood 103: 955-962. PubMed: 14525763.
42. Mondino A, Blasi F, (2004) uPA and uPAR in fibrinolysis, immunity and pathology. Trends Immunol 25: 450-455. doi:10.1016/j.it.2004.06.004. PubMed: 15275645.
43. Elner SG, Elner VM, Kindzelskii AL, Horino K, Davis HR, et al. (2003) Human RPE cell lysis of extracellular matrix: functional urokinase plasminogen activator receptor (uPAR), collagenase and elastase. Exp Eye Res 76: 585-595. doi:10.1016/S0014-4835(03)00028-9. PubMed: 12697422.
44. Das A, Boyd N, Jones TR, Talarico N, McGuire PG, (2004) Inhibition of choroidal neovascularization by a peptide inhibitor of the urokinase plasminogen activator and receptor system in a mouse model. Arch Ophthalmol 122: 1844-1849. doi:10.1001/archopht.122.12.1844. PubMed: 15596589.
45. Rakic JM, Lambert V, Munaut C, Bajou K, Peyrollier K, et al. (2003) Mice without uPA, tPA, or plasminogen genes are resistant to experimental choroidal neovascularization. Invest Ophthalmol Vis Sci 44: 1732-1739. doi:10.1167/iovs.02-0809. PubMed: 12657615.
46. Ganesh BS, Chintala SK, (2011) Inhibition of reactive gliosis attenuates excitotoxicity-mediated death of retinal ganglion cells. PLOS ONE 6: e18305. doi:10.1371/journal.pone.0018305. PubMed: 21483783.
47. Chintala SK, (2006) The emerging role of proteases in retinal ganglion cell death. Exp Eye Res 82: 5-12. doi:10.1016/j.exer.2005.07.013. PubMed: 16185688.
48. Brown DM, Nguyen QD, Marcus DM, Boyer DS, Patel S, et al. (2013) Long-term Outcomes of Ranibizumab Therapy for Diabetic Macular Edema: The 36-Month Results from Two Phase III Trials: RISE and RIDE. Ophthalmology. PubMed: 23706949.