Comparison of choroidal and retinal endothelial cells: Characteristics and response to VEGF isoforms and anti-VEGF treatments

Experimental Eye Research

Volumn 93, Issue 5, 2011, Pages 761-766

  Stewart, Elizabeth A ^a   Samaranayake, Govindi J ^a   Browning, Andrew C ^a   Hopkinson, Andrew ^a   Amoaku, Winfried M ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

Age related macular degeneration; Bevacizumab; Choroid; Endothelial cell; Ocular neovascularisation; Pegaptanib; Ranibizumab; Retina

Indexed keywords

BEVACIZUMAB; CD31 ANTIGEN; CD34 ANTIGEN; PEGAPTANIB; RANIBIZUMAB; VASCULOTROPIN 121; VASCULOTROPIN 165; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2; VON WILLEBRAND FACTOR;

ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CELL PROLIFERATION; CHOROID; CHOROID ENDOTHELIAL CELL; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOTOXICITY; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; NONHUMAN; PRIORITY JOURNAL; RETINA BLOOD VESSEL; RETINA CELL; RETINA ENDOTHELIAL CELL; TREATMENT RESPONSE;

ANGIOGENESIS INHIBITORS; ANTIBODIES, MONOCLONAL, HUMANIZED; ANTIGENS, CD31; ANTIGENS, CD34; APTAMERS, NUCLEOTIDE; BIOLOGICAL MARKERS; CELL PROLIFERATION; CELLS, CULTURED; CHOROID; ENDOTHELIUM, VASCULAR; HUMANS; PROTEIN ISOFORMS; RETINAL VESSELS; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2; VON WILLEBRAND FACTOR;

EID: 81355127555     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2011.09.010     Document Type: Article

References (39)

1. Adamis A.P., Shima D.T., Tolentino M.J., Gragoudas E.S., Ferrara N., Folkman J., D'Amore P.A., Miller J.W. Inhibition of vascular endothelial growth factor prevents retinal ischemia-associated iris neovascularization in a nonhuman primate. Arch. Ophthalmol. 1996, 114:66-71.
2. Aird W.C. Endothelial cell heterogeneity. Crit. Care Med. 2003, 31:S221-S230.
3. Ancelin M., Buteau-Lozano H., Meduri G., Osborne-Pellegrin M., Sordello S., Plouet J., Perrot-Applanat M. A dynamic shift of VEGF isoforms with a transient and selective progesterone-induced expression of VEGF189 regulates angiogenesis and vascular permeability in human uterus. Proc. Natl. Acad. Sci. U S A 2002, 99:6023-6028.
4. Bakri S.J., Snyder M.R., Reid J.M., Pulido J.S., Ezzat M.K., Singh R.J. Pharmacokinetics of intravitreal ranibizumab (Lucentis). Ophthalmology 2007, 114:2179.
5. Barzelay A., Lowenstein A., George J., Barak A. Influence of non-toxic doses of bevacizumab and ranibizumab on endothelial functions and inhibition of angiogenesis. Curr. Eye Res. 2010, 35:835-841.
6. Bhisitkul R.B. Vascular endothelial growth factor biology: clinical implications for ocular treatments. Br. J. Ophthalmol. 2006, 90:1542-1547.
7. Brown D.M., Campochiaro P.A., Singh R.P., Li Z., Gray S., Saroj N., Rundle A.C., Rubio R.G., Murahashi W.Y. Ranibizumab for macular edema following central retinal vein occlusion: six-month primary end point results of a phase III study. Ophthalmology 2010, 117:1124-1133. e1121.
8. Browning A.C., Dua H.S., Amoaku W.M. The effects of growth factors on the proliferation and in vitro angiogenesis of human macular inner choroidal endothelial cells. Br. J. Ophthalmol. 2008, 92:1003-1008.
9. Browning A.C., Gray T., Amoaku W.M. Isolation, culture, and characterisation of human macular inner choroidal microvascular endothelial cells. Br. J. Ophthalmol. 2005, 89:1343-1347.
10. Browning, A.C., Halligan, E.P., Stewart, E.A., Swan, D.C., Samaranayake, G.J., Amoaku, W.M. Comparative gene expression profiling of HUVEC and ocular vascular endothelial cells. Br. J. Ophthalmol., in press.
11. Brylla E., Tscheudschilsuren G., Santos A.N., Nieber K., Spanel-Borowski K., Aust G. Differences between retinal and choroidal microvascular endothelial cells (MVECs) under normal and hypoxic conditions. Exp. Eye Res. 2003, 77:527-535.
12. Campochiaro P.A. Ocular versus extraocular neovascularization: mirror images or vague resemblances. Invest. Ophthalmol. Vis. Sci. 2006, 47:462-474.
13. Carneiro A., Falcao M., Pirraco A., Milheiro-Oliveira P., Falcao-Reis F., Soares R. Comparative effects of bevacizumab, ranibizumab and pegaptanib at intravitreal dose range on endothelial cells. Exp. Eye Res. 2009, 88:522-527.
14. Costa R., Carneiro A., Rocha A., Pirraco A., Falcao M., Vasques L., Soares R. Bevacizumab and ranibizumab on microvascular endothelial cells: a comparative study. J. Cell Biochem. 2009, 108:1410-1417.
15. Craig L.E., Spelman J.P., Strandberg J.D., Zink M.C. Endothelial cells from diverse tissues exhibit differences in growth and morphology. Microvasc. Res. 1998, 55:65-76.
16. Das A., McGuire P.G. Retinal and choroidal angiogenesis: pathophysiology and strategies for inhibition. Prog. Retin. Eye Res. 2003, 22:721.
17. Dejana E., Orsenigo F., Lampugnani M.G. The role of adherens junctions and VE-cadherin in the control of vascular permeability. J. Cell Sci. 2008, 121:2115-2122.
18. Fajardo L.F. The complexity of endothelial cells. A review. Am. J. Clin. Pathol. 1989, 92:241-250.
19. Friedman D.S., O'Colmain B.J., Munoz B., Tomany S.C., McCarty C., de Jong P.T., Nemesure B., Mitchell P., Kempen J. Prevalence of age-related macular degeneration in the United States. Arch. Ophthalmol. 2004, 122:564-572.
20. Hopkinson A., McIntosh R.S., Shanmuganathan V., Tighe P.J., Dua H.S. Proteomic analysis of amniotic membrane prepared for human transplantation: characterization of proteins and clinical implications. J. Proteome Res. 2006, 5:2226-2235.
21. Huang J.C., Liu D.Y., Dawood M.Y. The expression of vascular endothelial growth factor isoforms in cultured human endometrial stromal cells and its regulation by 17beta-oestradiol. Mol. Hum. Reprod. 1998, 4:603-607.
22. Imegwu O.J., Entersz I., Graham A.M., Nackman G.B. Heterotypic smooth muscle cell/endothelial cell interactions differ between species. J. Surg. Res. 2001, 98:85-88.
23. Ishida S., Usui T., Yamashiro K., Kaji Y., Amano S., Ogura Y., Hida T., Oguchi Y., Ambati J., Miller J.W., Gragoudas E.S., Ng Y.S., D'Amore P.A., Shima D.T., Adamis A.P. VEGF164-mediated inflammation is required for pathological, but not physiological, ischemia-induced retinal neovascularization. J. Exp. Med. 2003, 198:483-489.
24. Keyt B.A., Berleau L.T., Nguyen H.V., Chen H., Heinsohn H., Vandlen R., Ferrara N. The carboxyl-terminal domain (111-165) of vascular endothelial growth factor is critical for its mitogenic potency. J. Biol. Chem. 1996, 271:7788-7795.
25. Lowe J., Araujo J., Yang J., Reich M., Oldendorp A., Shiu V., Quarmby V., Lowman H., Lien S., Gaudreault J., Maia M. Ranibizumab inhibits multiple forms of biologically active vascular endothelial growth factor in vitro and in vivo. Exp. Eye Res. 2007, 85:425.
26. 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.
27. Muller A.M., Hermanns M.I., Skrzynski C., Nesslinger M., Muller K.M., Kirkpatrick C.J. Expression of the endothelial markers PECAM-1, vWf, and CD34 in vivo and in vitro. Exp. Mol. Pathol. 2002, 72:221-229.
28. Rakic J.M., Lambert V., Devy L., Luttun A., Carmeliet P., Claes C., Nguyen L., Foidart J.M., Noel A., Munaut C. Placental growth factor, a member of the VEGF family, contributes to the development of choroidal neovascularization. Invest. Ophthalmol. Vis. Sci. 2003, 44:3186-3193.
29. Robinson C.J., Stringer S.E. The splice variants of vascular endothelial growth factor (VEGF) and their receptors. J. Cell Sci. 2001, 114:853-865.
30. Saint-Geniez M., Maldonado A.E., D'Amore P.A. VEGF expression and receptor activation in the choroid during development and in the adult. Invest. Ophthalmol. Vis. Sci. 2006, 47:3135-3142.
31. Schmidt-Erfurth U.M., Pruente C. Management of neovascular age-related macular degeneration. Prog. Retin. Eye Res. 2007, 26:437-451.
32. Soker S., Takashima S., Miao H.Q., Neufeld G., Klagsbrun M. Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor. Cell 1998, 92:735-745.
33. Spitzer M.S., Yoeruek E., Sierra A., Wallenfels-Thilo B., Schraermeyer U., Spitzer B., Bartz-Schmidt K.U., Szurman P. Comparative antiproliferative and cytotoxic profile of bevacizumab (Avastin), pegaptanib (Macugen) and ranibizumab (Lucentis) on different ocular cells. Graefes Arch. Clin. Exp. Ophthalmol. 2007.
34. Sultan M.B., Zhou D., Loftus J., Dombi T., Ice K.S. A phase 2/3, multicenter, randomized, double-masked, 2-year trial of pegaptanib sodium for the treatment of diabetic macular edema. Ophthalmology 2011, 118:1107-1118.
35. Usui T., Ishida S., Yamashiro K., Kaji Y., Poulaki V., Moore J., Moore T., Amano S., Horikawa Y., Dartt D., Golding M., Shima D.T., Adamis A.P. VEGF164(165) as the pathological isoform: differential leukocyte and endothelial responses through VEGFR1 and VEGFR2. Invest. Ophthalmol. Vis. Sci. 2004, 45:368-374.
36. Wroblewski J.J., Wells J.A., Gonzales C.R. Pegaptanib sodium for macular edema secondary to branch retinal vein occlusion. Am. J. Ophthalmol. 2010, 149:147-154.
37. Yonekura H., Sakurai S., Liu X., Migita H., Wang H., Yamagishi S., Nomura M., Abedin M.J., Unoki H., Yamamoto Y., Yamamoto H. Placenta growth factor and vascular endothelial growth factor B and C expression in microvascular endothelial cells and pericytes. Implication in autocrine and paracrine regulation of angiogenesis. J. Biol. Chem. 1999, 274:35172-35178.
38. Zamora D.O., Riviere M., Choi D., Pan Y., Planck S.R., Rosenbaum J.T., David L.L., Smith J.R. Proteomic profiling of human retinal and choroidal endothelial cells reveals molecular heterogeneity related to tissue of origin. Mol. Vis. 2007, 13:2058-2065.
39. Zhu Q., Ziemssen F., Henke-Fahle S., Tatar O., Szurman P., Aisenbrey S., Schneiderhan-Marra N., Xu X., Grisanti S. Vitreous levels of bevacizumab and vascular endothelial growth factor-A in patients with choroidal neovascularization. Ophthalmology 2008, 115:1750-1755. 1755 e1751.