VEGF but not PlGF disturbs the barrier of retinal endothelial cells

Experimental Eye Research

Volumn 115, Issue , 2013, Pages 162-171

  Deissler, Heidrun L ^a   Deissler, Helmut ^a   Lang, Gerhard K ^a   Lang, Gabriele E ^a  

^a UNIVERSITY OF ULM   (Germany)

Author keywords

Aflibercept; BFGF; Diabetic macular edema; IGF 1; PlGF; Ranibizumab; Retinal endothelial cells; VEGF

Indexed keywords

AFLIBERCEPT; CLAUDIN 1; CLAUDIN 3; CLAUDIN 5; IMMUNOGLOBULIN F(AB) FRAGMENT; NEUROPILIN 1; PLACENTAL GROWTH FACTOR; RANIBIZUMAB; VASCULOTROPIN; VASCULOTROPIN 121; VASCULOTROPIN 165; VASCULOTROPIN A; VASCULOTROPIN E; VASCULOTROPIN RECEPTOR;

ANIMAL CELL; ARTICLE; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; DIABETIC MACULAR EDEMA; DIABETIC RETINOPATHY; DOWN REGULATION; ELECTRIC RESISTANCE; ENDOTHELIUM CELL; IMMUNOFLUORESCENCE; NONHUMAN; PRIORITY JOURNAL; WESTERN BLOTTING;

(I)BREC; (IMMORTALIZED) BOVINE RETINAL ENDOTHELIAL CELLS; AFLIBERCEPT; BASIC FIBROBLAST GROWTH FACTOR; BFGF; DIABETIC MACULAR EDEMA; DIABETIC RETINOPATHY; DME; DR; EC; ECGM; ECGS/H; ENDOTHELIAL CELL GROWTH MEDIUM; ENDOTHELIAL CELLS; ENDOTHELIAL CELLS GROWTH SUPPLEMENT/H; FCS; FETAL CALF SERUM; IGF-1; INSULIN-LIKE GROWTH FACTOR; KRN951; N-(2-CHLORO-4-((6,7-DIMETHOXY-4-QUINOLYL)OXY)PHENYL)-N′-(5-METHYL-3-ISOXAZOLYL)UREA; NEUROPILIN-1; NRP-1; PLACENTAL GROWTH FACTOR; PLGF; RANIBIZUMAB; REC; RETINAL ENDOTHELIAL CELLS; SERUM-REDUCED MEDIUM; SRM; TER; TIGHT JUNCTION; TJ; TRANSENDOTHELIAL RESISTANCE; VASCULAR ENDOTHELIAL CADHERIN; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR E; VECAD; VEGF; VEGF RECEPTOR 1; VEGF RECEPTOR 2; VEGF-E; VEGFR1; VEGFR2; ZO-1; ZONA OCCLUDENS-1;

ANIMALS; ANTIBODIES, MONOCLONAL, HUMANIZED; BIOLOGICAL TRANSPORT; BLOTTING, WESTERN; CATTLE; CELL LINE; CELL MEMBRANE PERMEABILITY; CLAUDIN-1; ELECTRIC IMPEDANCE; ENDOTHELIUM, VASCULAR; FIBROBLAST GROWTH FACTOR 2; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; INSULIN-LIKE GROWTH FACTOR I; NEUROPILIN-1; PREGNANCY PROTEINS; RECEPTORS, VASCULAR ENDOTHELIAL GROWTH FACTOR; RECOMBINANT FUSION PROTEINS; RETINAL VESSELS; TIGHT JUNCTIONS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84882800599     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2013.07.018     Document Type: Article

References (43)

1. Aiello L.P., Avery R.L., Arrigg P.G., Keyt B.A., Jampel H.D., Shah S.T., Pasquale L.R., Thieme H., Iwamoto M.A., Park J.E., Nguyen H.V., Aiello L.M., Ferrara N., King G.L. Vascular endothelial growth factor in ocular fluid of patients with diabetic retinopathy and other retinal disorders. N.Engl. J. Med. 1994, 331:1480-1487.
2. Aiello L.P., Pierce E.A., Foley E.D. Suppression of retinal neovascularization invivo by inhibition of vascular endothelial growth factor (VEGF) using soluble VEGF-receptor chimeric proteins. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:10457-10461.
3. Antonetti D.A., Barber A.J., Hollinger L.A., Wolpert E.B., Gardner T.W. Vascular endothelial growth factor induces rapid phosphorylation of tight junction proteins occludin and zonula occludens 1. J.Biol. Chem. 1999, 274:23463-23467.
4. Autiero M., Waltenberger J., Communi D., Kranz A., Moons L., Lambrechts D., Kroll J., Plaisance S., De Mol M., Bono F., Kliche S., Fellbrich G., Ballmer-Hofer K., Maglione D., Mayr-Beyrle U., Dewerchin M., Dombrowski S., Stanimirovic D., Van Hummelen P., Dehio C., Hicklin D.J., Persico G., Herbert J.M., Communi D., Shibuya M., Collen D., Conway E.M., Carmeliet P. Role of PlGF in the intra- and intermolecular cross talk between the VEGF receptors Flt1 and Flk1. Nat. Med. 2003, 7:936-943.
5. Bazzoni G. Endothelial tight junctions: permeable barriers of the vessel wall. Thromb. Haemost. 2006, 95:36-42.
6. Becker P.M., Waltenberger J., Yachechko R., Mirzapoiazova T., Sham J.S., Lee C.G., Elias J.A., Verrin A.D. Neuropilin-1 regulates vascular endothelial growth factor-mediated endothelial permeability. Circ. Res. 2005, 96:1657-1665.
7. Blume L.F., Denker M., Giesler F. Temperature corrected transepithelial electrical resistance (TEER) measurement to quantify rapid changes in paracellular permeability. Pharmazie 2010, 65:19-24.
8. Boulton M., Gregor Z., McLeod D., Charteris D., Jarvis-Evans J., Moriarty P., Khaliq A., Foreman D., Allamby D., Bardsley B. Intravitreal growth factors in proliferative diabetic retinopathy: correlation with neovascular activity and glycaemic management. Br. J. Ophthalmol. 1997, 81:228-233.
9. Brkovic A., Sirois M.G. Vascular permeability induced by VEGF family members invivo: role of endogenous PAF and NO synthesis. J.Cell. Biochem. 2007, 100:727-737.
10. Cai J., Wu L., Qi X., Shaw L., Li Calzi S., Caballero S., Jiang W.G., Vinores S.A., Antonetti D., Ahmed A., Grant M.B., Boulton M.E. Placenta growth factor-1 exerts time-dependent stabilization of adherens junctions following VEGF-induced vascular permeability. PLoS ONE 2011, 6(3):e18076. 10.1371/journal.pone.0018076.
11. Castellon R., Hamdi H.K., Sacerio I., Aoki A.M., Kenney M.C., Ljubimov A.V. Effects of angiogenic growth factor combinations on retinal endothelial cells. Exp. Eye Res. 2002, 74:523-535.
12. Deissler H.L., Deissler H., Lang G.K., Lang G.E. Generation and characterization of iBREC: novel hTERT-immortalized bovine retinal endothelial cells. Int. J. Mol. Med. 2005, 15:65-70.
13. Deissler H.L., Kuhn E.M., Lang G.E., Deissler H. Tetraspanin CD9 is involved in the migration of retinal microvascular endothelial cells. Int. J. Mol. Med. 2007, 20:643-652.
14. ®) in microvascular retinal endothelial cells. Br. J. Ophthalmol. 2008, 92:839-843.
15. 165 on tight junction protein claudin-1 and permeability in microvascular retinal endothelial cells. Invest. Ophthalmol. Vis. Sci. 2010, 51:535-542.
16. Deissler H.L., Deissler H., Lang G.E. Inhibition of VEGF is sufficient to completely restore barrier malfunction induced by growth factors in microvascular retinal endothelial cells. Br. J. Ophthalmol. 2011, 95:1151-1156.
17. Deissler H.L., Deissler H., Lang G.K., Lang G.E. Ranibizumab efficiently blocks migration but not proliferation induced by growth factor combinations including VEGF in retinal endothelial cells. Graefes Arch. Clin. Exp. Ophthalmol. 2013, 10.1007/s00417-013-2393-5.
18. Do D.V., Nguyen Q.D., Boyer D., Schmidt-Erfurth U., Brown D.M., Vitti R., Berliner A.J., Gao B., Zeitz O., Ruckert R., Schmelter T., Sandbrink R., Heier J.S. One-year outcomes of the DA VINCI study of VEGF trap-eye in eyes with diabetic macular edema. Ophthalmology 2012, 119:1658-1665. DA VINCI Study Group.
19. Ferrara N. Vascular endothelial growth factor: basic science and clinical progress. Endocr. Rev. 2004, 25:581-611.
20. Ferrara N., Damico L., Shams N., Lowman H., Kim R. Development of ranibizumab, an anti-vascular endothelial growth factor antigen binding fragment, as therapy for neovascular age-related macular degeneration. Retina 2006, 26:859-870.
21. Fujibe M., Chiba H., Kojima T., Soma T., Wada T., Yamashita T., Sawada N. Thr203 of claudin-1, a putative phosphorylation site for MAP kinase, is required to promote the barrier function of tight junctions. Exp. Cell Res. 2004, 295:36-47.
22. Harhaj N.S., Felinski E.A., Wolpert E.B., Sundstrom J.M., Gardner T.W., Antonetti D.A. VEGF activation of protein kinase C stimulates occludin phosphorylation and contributes to endothelial permeability. Invest. Ophthalmol. Vis. Sci. 2006, 47:5106-5115.
23. Haurigot V., Villacampa P., Ribera A., Llombart C., Bosch A., Nacher V., Ramos D., Ayuso E., Segovia J.C., Bueren J.A., Ruberte J., Bosch F. Increased intraocular insulin-like growth factor-I triggers blood-retinal barrier breakdown. J.Biol. Chem. 2009, 284:22961-22969.
24. Holash J., Davis S., Papadopoulos N., Croll S.D., Ho L., Russell M., Boland P., Leidich R., Hylton D., Burova E., Ioffe E., Huang T., Radziejewski C., Bailey K., Fandl J.P., Daly T., Wiegand S.J., Yancopoulos G.D., Rudge J.S. VEGF-trap: a VEGF blocker with potent antitumor effects. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:11393-11398.
25. Khaliq A., Foreman D., Ahmed A., Weich H., Gregor Z., McLeod D., Boulton M. Increased expression of placenta growth factor in proliferative diabetic retinopathy. Lab. Invest. 1998, 78:109-115.
26. Meyer M., Clauss M., Lepple-Wienhues A., Waltenberger J., Augustin H.G., Ziche M., Lanz C., Buttner M., Rziha H.J., Dehio C. Anovel endothelial growth factor encoded by Orf virus, VEGF-E, mediates angiogenesis via signaling through VEGFR-2 (KDR) but not VEGFR-1 (Flt-1) receptor kinases. EMBO J. 1999, 18:363-374.
27. Meyer-Schwickerath R., Pfeiffer A., Blum W.F., Freyberger H., Klein M., Lösche C., Röllmann R., Schatz H. Vitreous levels of the insulin-like growth factors I and II and the insulin-like growth factor binding proteins 2 and 3, increase in neovascular eye disease. J.Clin. Invest. 1993, 92:2620-2625.
28. Migdal M., Huppertz B., Tessler S., Comforti A., Shibuya M., Reich R., Baumann H., Neufeld G. Neuropilin-1 is a placenta growth factor-2 receptor. J.Biol. Chem. 1998, 273:22272-22278.
29. Mitchell P., Bandello F., Schmidt-Erfurth U., Lang G.E., Massin P., Schlingemann R.O., Sutter F., Simader C., Burian G., Gerstner O., Weichselberger A. The RESTORE study: ranibizumab monotherapy or combined with laser versus laser monotherapy for diabetic macular edema. Ophthalmology 2011, 118:615-625. RESTORE study group.
30. Nakamura K., Taguchi E., Miura T., Yamamoto A., Takahashi K., Bichat F., Guilbaud N., Hasegawa K., Kubo K., Fujiwara Y., Suzuki R., Kubo K., Shibuya M., Isae T. KRN951, a highly potent inhibitor of vascular endothelial growth factor receptor tyrosine kinases, has antitumor activities and affects functional vascular properties. Cancer Res. 2006, 66:9134-9142.
31. Nguyen Q.D., Tatlipinar S., Shah S.M., Haller J.A., Quinlan E., Sung J., Zimmer-Galler I., Do D.V., Campochiaro P.A. Vascular endothelial growth factor is a critical stimulus for diabetic macular edema. Am. J. Ophthalmol. 2006, 142:961-969.
32. Oh H., Takagi H., Otani A., Koyama S., Kemmochi S., Uemura A., Honda Y. Selective induction of neuropilin-1 by vascular endothelial growth factor (VEGF): a mechanism contributing to VEGF-induced angiogenesis. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:383-388.
33. Othman A., Ahmad S., Megyerdi S., Mussell R., Choksi K., Maddipati K.R., Elmarakby A., Rizk N., Al-Shabrawey M. 12/15-Lipoxygenase-derived lipid metabolites induce retinal endothelial cell barrier dysfunction: contribution of NADPH oxidase. PLoS ONE 2013, 8(2):e57254. 10.1371/journal.pone.0057254.
34. 165 and regulates endothelial cell migration and sprouting. J.Biol. Chem. 2007, 282:24049-24056.
35. Park J.E., Chen H.H., Winer J., Houck K.A., Ferrara N. Placenta growth factor. Potentiation of vascular endothelial growth factor bioactivity, invitro and invivo, and high affinity binding to Flt-1 but not to Flk-1/KDR. J.Biol. Chem. 1994, 269:25646-25654.
36. Qaum T., Xu Q., Joussen A.M., Clemens M.W., Qin W., Miyamoto K., Hassessian H., Wiegand S.J., Rudge J., Yancopoulos G.D., Adamis A.P. VEGF-initiated blood-retinal barrier breakdown in early diabetes. Invest. Ophthalmol. Vis. Sci. 2001, 42:2408-2413.
37. Sawano A., Takahashi T., Yamaguchi S., Aonuma M., Shibuya M. Flt-1 but not KDR/Flk-1 tyrosine kinase is a receptor for placental growth factor, which is related to vascular endothelial growth factor. Cell Growth Differ. 1996, 7:213-221.
38. Simorre-Pinatel V., Guerrin M., Chollet P., Penary M., Clamens S., Malecaze F., Plouet J. Vasculotropin-VEGF stimulates retinal capillary endothelial cells through an autocrine pathway. Invest. Ophthalmol. Vis. Sci. 1994, 35:3393-3400.
39. Stewart E.A., Samaranayake G.J., Browning A.C., Hopkinson A., Amoaku W.M. Comparison of choroidal and retinal endothelial cells: characteristics and response to VEGF-isoforms and anti-VEGF treatment. Exp. Eye Res. 2011, 93:761-766.
40. Tretiach M., van Driel D., Gillies M.C. Transendothelial electrical resistance of bovine retinal capillary endothelial cells is influenced by cell growth patterns: an ultrastructural study. Clin. Exp. Ophthalmol. 2003, 31:348-353.
41. Vogel C., Bauer A., Wiesnet M., Preissner K.T., Schaper W., Marti H.H., Fischer S. Flt-1, but not Flk-1 mediates hyperpermeability through activation of the PI3-K/Akt pathway. J.Cell. Physiol. 2007, 216:236-243.
42. Wisniewska-Kruk J., Hoeben K.A., Vogels I.M., Gaillard P.J., Van Noorden C.J., Schlingemann R.O., Klaassen I. Anovel co-culture model of the blood-retinal barrier based on primary retinal endothelial cells, pericytes and astrocytes. Exp. Eye Res. 2012, 96:181-190.
43. Yan Q., Ki Y., Hendrickson A., Sage E.H. Regulation of retinal capillary cells by basic fibroblast growth factor, vascular endothelial growth factor, and hypoxia. InVitro Cell. Dev. Biol.-animal 2001, 37:45-49.