Role of vascular endothelial growth factor in the pathogenesis of traumatic proliferative vitreoretinopathy_Chinese Journal of Ocular Fundus Diseases

Authors：

Zhao Xiao ,  Yan Hua

Department of Ophthalmology, General Hospital of Tianjin Medical University， Tianjin 300052, China;

Corresponding author：

Yan Hua, Email: phuayan2000@163.com

Keywords：

Vitreoretinopathy, proliferative; Vascular endothelial growth factors; Receptor, platelet-derived growth factor alpha; Review

DOI：

10.3760/cma.j.issn.1005-1015.2018.02.023

Video：

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Proliferative vitreoretinopathy (PVR) is a common complication and major cause of blindness of ocular trauma. Many cytokines, including vascular endothelial growth factor (VEGF) and platelet-derived growth factor (PDGF), participate in the process of the pathogenesis of traumatic PVR. VEGF competitively inhibits binding of PDGF to its receptor (PDGFRα), enables indirect activation of PDGFRα by non-PDGF ligands, resulting in reduced p53 expression, cell proliferation and migration, which is a key point in the pathogenesis of traumatic PVR.

Citation： Zhao Xiao, Yan Hua. Role of vascular endothelial growth factor in the pathogenesis of traumatic proliferative vitreoretinopathy. Chinese Journal of Ocular Fundus Diseases, 2018, 34(2): 187-190. doi: 10.3760/cma.j.issn.1005-1015.2018.02.023 Copy

1.	Zhou Q, Xu G, Zhang X, et al. Proteomics of post-traumatic proliferative vitreoretinopathy in rabbit retina reveals alterations to a variety of functional proteins[J]. Current Eye Research, 2012, 37(4): 318-326. DOI: 10.3109/02713683.2011.635397.
2.	Colyer MH, Chun DW, Bower KS, et al. Perforating globe injuries during operation Iraqi Freedom[J]. Ophthalmology, 2008, 115(11): 2087-2093. DOI: 10.1016/j.ophtha.2008.05.013.
3.	Pastor JC, Rojas J, Pastor-Idoate S, et al. Proliferative vitreoretinopathy: a new concept of disease pathogenesis and practical consequences[J]. Prog Retin Eye Res, 2016, 51: 125-155. DOI: 10.1016/j.preteyeres.2015.07.005.
4.	Garweg JG, Tappeiner C, Halberstadt M. Pathophysiology of proliferative vitreoretinopathy in retinal detachment[J]. Surv Ophthalmol, 2013, 58(4): 321-329. DOI: 10.1016/j.survophthal.2012.12.004.
5.	Ferrara N, Gerber HP, LeCouter J.The biology of VEGF and its receptors[J]. Nat Med, 2003, 9 (6): 669-676. DOI: 10.1038/nm0603-669.
6.	Penn JS, Madan A, Caldwell RB, et al. Vascular endothelial growth factor in eye disease[J]. Prog Retin Eye Res, 2008, 27(4): 331-371. DOI: 10.1016/j.preteyeres.2008.05.001.
7.	Simons M, Gordon E, Claesson-Welsh L.Mechanisms and regulation of endothelial VEGF receptor signalling[J]. Nat Rev Mol Cell Biol, 2016, 17(10): 611-625. DOI: 10.1038/nrm.2016.87.
8.	Pereira ER, Frudd K, Awad W, et al. Endoplasmic reticulum (ER) stress and hypoxia response pathways interact to potentiate hypoxia-inducible factor 1 (HIF-1) transcriptional activity on targets like vascular endothelial growth factor (VEGF)[J]. J Biol Chem, 2014, 289(6): 3352-3364. DOI: 10.1074/jbc.M113.507194.
9.	Vempati P, Popel AS, Mac GF. Extracellular regulation of VEGF: isoforms, proteolysis, and vascular patterning[J]. Cytokine Growth Factor Rev, 2014, 25(1): 1-19. DOI: 10.1016/j.cytogfr.2013.11.002.
10.	Matsumoto K, Ema M. Roles of VEGF-A signalling in development, regeneration, and tumours[J]. J Biochem, 2014, 156(1): 1-10. DOI: 10.1093/jb/mvu031.
11.	牛彤彤, 徐艳春. VEGF与眼内血管新生[J]. 眼科新进展, 2008, 28(5): 394-398. DOI: 10.3969/j.issn.1003-5141.2008.05.025.Niu TT, Xu YC.Vascular endothelial growth factor and ocular neovascularization[J]. Rec Adv Ophthalmol, 2008, 28(5): 394-398. DOI: 10.3969/j.issn.1003-5141.2008.05.025.
12.	Moysidis SN, Thanos A, Vavvas DG. Mechanisms of inflammation in proliferative vitreoretinopathy: from bench to bedside[J/OL]. Mediators Inflamm, 2012, 2012: 815937[2012-09-25]. http://dx.doi.org/10.1155/2012/815937. DOI: 10.1155/2012/815937.
13.	Zhang J, Yuan G, Dong M, et al. Notch signaling modulates proliferative vitreoretinopathy via regulating retinal pigment epithelial-to-mesenchymal transition[J]. Histochem Cell Biol, 2017, 147(3): 367-375. DOI: 10.1007/s00418-016-1484-x.
14.	Ciprian D. The pathogeny of proliferative virtreoretinopathy [J]. Rom J Ophthalmol, 2015, 59(2): 88-92.
15.	Morescalchi F, Duse S, Gambicorti E, et al. Proliferative vitreoretinopathy after eye injuries: an overexpression of growth factors and cytokines leading to a retinal keloid[J/OL]. Mediators Inflamm, 2013, 2013: 269787[2013-09-30]. http://dx.doi.org/10.1155/2013/269787. DOI: 10.1155/2013/269787.
16.	Town CD, Krill D, Hassid AI.Vascular endothelial growth factor in aqueous humor of patients with perforative eye injuries[J]. Coll Antropol, 2008, 32 Suppl 2(3): S33-37.
17.	Citirik M, Kabatas EU, Batman C, et al. Vitreous vascular endothelial growth factor concentrations in proliferative diabetic retinopathy versus proliferative vitreoretinopathy[J]. Ophthalmic Res, 2012, 47(1): 7-12. DOI: 10.1159/000324200.
18.	Lei H, Hovland P, Velez G, et al. A potential role for PDGF-C in experimental and clinical proliferative vitreoretinopathy[J]. Invest Ophthalmol Vis Sci, 2007, 48(5): 2335-2342. DOI: 10.1167/iovs.06-0965.
19.	Cui J, Lei H, Samad A, et al. PDGF receptors are activated in human epiretinal membranes[J]. Exp Eye Res, 2009, 88(3): 438-444. DOI: 10.1016/j.exer.2008.10.020.
20.	Campochiaro PA, Hackett SF, Vinores SA, et al. Platelet-derived growth factor is an autocrine growth stimulator in retinal pigmented epithelial cells[J]. J Cell Sci, 1994, 107(Pt 9): 2459-2469.
21.	Hoch RV, Soriano P. Roles of PDGF in animal development[J]. Development, 2003, 130 (20): 4769-4784. DOI: 10.1242/dev.00721.
22.	Klinkhammer BM, Floege J, Boor P. PDGF in organ fibrosis[J/OL]. Mol Aspects Med, 2017, 2017: E1[2017-11-22]. https://doi.org/10.1016/j.mam.2017.11.008. DOI: 10.1016/j.mam.2017.11.008. [published online ahead of print].
23.	Chan CM, Chang HH, Wang VC, et al. Inhibitory effects of resveratrol on PDGF-BB-induced retinal pigment epithelial cell migration via PDGFRbeta, PI3K/Akt and MAPK pathways[J/OL].PLoS One, 2013, 8(2): 56819[2013-02-14]. https://doi.org/10.1371/journal.pone.0056819. DOI: 10.1371/journal.pone.0056819.
24.	Kumar A, Li X. PDGF-C and PDGF-D in ocular diseases[J/OL]. Mol Aspects Med, 2017, 2017: E1[2017-10-27]. https://doi.org/10.1016/j.mam.2017.10.002. DOI: 10.1016/j.mam.2017.10.002. [published online ahead of print].
25.	Pennock S, Haddock LJ, Eliott D, et al. Is neutralizing vitreal growth factors a viable strategy to prevent proliferative vitreoretinopathy?[J]. Prog Retin Eye Res, 2014, 40: 16-34. DOI: 10.1016/j.preteyeres.2013.12.006.
26.	Lei H, Rheaume MA, Cui J, et al. A novel function of p53: a gatekeeper of retinal detachment [J]. Am J Pathol, 2012, 181(3): 866-874. DOI: 10.1016/j.ajpath.2012.05.036.
27.	Velez G, Weingarden AR, Tucker BA, et al. Retinal pigment epithelium and Müller progenitor cell interaction increase Müller progenitor cell expression of PDGFRα and ability to induce proliferative vitreoretinopathy in a rabbit model[J/OL]. Stem Cells Int, 2012, 2012: 106486 [2012-08-23]. http://dx.doi.org/10.1155/2012/106486. DOI: 10.1155/2012/106486.
28.	Su CC, Chan CM, Chen HM, et al. Lutein inhibits the migration of retinal pigment epithelial cells via cytosolic and mitochondrial Akt pathways (lutein inhibits RPE cells migration)[J]. Int J Mol Sci, 2014, 15(8): 13755-13767. DOI: 10.3390/ijms150813755.
29.	Pennock S, Kazlauskas A. Vascular endothelial growth factor A competitively inhibits platelet-derived growth factor (PDGF)-dependent activation of PDGF receptor and subsequent signaling events and cellular responses[J]. Mol Cell Biol, 2012, 32(10): 1955-1966. DOI: 10.1128/MCB.06668-11.
30.	Pennock S, Kim D, Mukai S, et al. Ranibizumab is a potential prophylaxis for proliferative vitreoretinopathy, a nonangiogenic blinding disease[J]. Am J Pathol, 2013, 182(5): 1659-1670. DOI: 10.1016/j.ajpath.2013.01.052.
31.	Lei H, Velez G, Kazlauskas A. Pathological signaling via platelet-derived growth factor receptor alpha involves chronic activation of Akt and suppression of p53[J]. Mol Cell Biol, 2011, 31(9): 1788-1799. DOI: 10.1128/MCB.01321-10.
32.	Lei H, Kazlauskas A. A reactive oxygen species-mediated, self-perpetuating loop persistently activates platelet-derived growth factor receptor α[J]. Mol Cell Biol,2014,34(1): 110-122. DOI: 10.1128/MCB.00839-13.
33.	Lemos A, Leão M, Soares J, et al. Medicinal chemistry strategies to disrupt the p53-MDM2/MDMX interaction[J]. Med Res Rev, 2016, 36(5): 789-844. DOI: 10.1002/med.21393.

1. Zhou Q, Xu G, Zhang X, et al. Proteomics of post-traumatic proliferative vitreoretinopathy in rabbit retina reveals alterations to a variety of functional proteins[J]. Current Eye Research, 2012, 37(4): 318-326. DOI: 10.3109/02713683.2011.635397.
2. Colyer MH, Chun DW, Bower KS, et al. Perforating globe injuries during operation Iraqi Freedom[J]. Ophthalmology, 2008, 115(11): 2087-2093. DOI: 10.1016/j.ophtha.2008.05.013.
3. Pastor JC, Rojas J, Pastor-Idoate S, et al. Proliferative vitreoretinopathy: a new concept of disease pathogenesis and practical consequences[J]. Prog Retin Eye Res, 2016, 51: 125-155. DOI: 10.1016/j.preteyeres.2015.07.005.
4. Garweg JG, Tappeiner C, Halberstadt M. Pathophysiology of proliferative vitreoretinopathy in retinal detachment[J]. Surv Ophthalmol, 2013, 58(4): 321-329. DOI: 10.1016/j.survophthal.2012.12.004.
5. Ferrara N, Gerber HP, LeCouter J.The biology of VEGF and its receptors[J]. Nat Med, 2003, 9 (6): 669-676. DOI: 10.1038/nm0603-669.
6. Penn JS, Madan A, Caldwell RB, et al. Vascular endothelial growth factor in eye disease[J]. Prog Retin Eye Res, 2008, 27(4): 331-371. DOI: 10.1016/j.preteyeres.2008.05.001.
7. Simons M, Gordon E, Claesson-Welsh L.Mechanisms and regulation of endothelial VEGF receptor signalling[J]. Nat Rev Mol Cell Biol, 2016, 17(10): 611-625. DOI: 10.1038/nrm.2016.87.
8. Pereira ER, Frudd K, Awad W, et al. Endoplasmic reticulum (ER) stress and hypoxia response pathways interact to potentiate hypoxia-inducible factor 1 (HIF-1) transcriptional activity on targets like vascular endothelial growth factor (VEGF)[J]. J Biol Chem, 2014, 289(6): 3352-3364. DOI: 10.1074/jbc.M113.507194.
9. Vempati P, Popel AS, Mac GF. Extracellular regulation of VEGF: isoforms, proteolysis, and vascular patterning[J]. Cytokine Growth Factor Rev, 2014, 25(1): 1-19. DOI: 10.1016/j.cytogfr.2013.11.002.
10. Matsumoto K, Ema M. Roles of VEGF-A signalling in development, regeneration, and tumours[J]. J Biochem, 2014, 156(1): 1-10. DOI: 10.1093/jb/mvu031.
11. 牛彤彤, 徐艳春. VEGF与眼内血管新生[J]. 眼科新进展, 2008, 28(5): 394-398. DOI: 10.3969/j.issn.1003-5141.2008.05.025.Niu TT, Xu YC.Vascular endothelial growth factor and ocular neovascularization[J]. Rec Adv Ophthalmol, 2008, 28(5): 394-398. DOI: 10.3969/j.issn.1003-5141.2008.05.025.
12. Moysidis SN, Thanos A, Vavvas DG. Mechanisms of inflammation in proliferative vitreoretinopathy: from bench to bedside[J/OL]. Mediators Inflamm, 2012, 2012: 815937[2012-09-25]. http://dx.doi.org/10.1155/2012/815937. DOI: 10.1155/2012/815937.
13. Zhang J, Yuan G, Dong M, et al. Notch signaling modulates proliferative vitreoretinopathy via regulating retinal pigment epithelial-to-mesenchymal transition[J]. Histochem Cell Biol, 2017, 147(3): 367-375. DOI: 10.1007/s00418-016-1484-x.
14. Ciprian D. The pathogeny of proliferative virtreoretinopathy [J]. Rom J Ophthalmol, 2015, 59(2): 88-92.
15. Morescalchi F, Duse S, Gambicorti E, et al. Proliferative vitreoretinopathy after eye injuries: an overexpression of growth factors and cytokines leading to a retinal keloid[J/OL]. Mediators Inflamm, 2013, 2013: 269787[2013-09-30]. http://dx.doi.org/10.1155/2013/269787. DOI: 10.1155/2013/269787.
16. Town CD, Krill D, Hassid AI.Vascular endothelial growth factor in aqueous humor of patients with perforative eye injuries[J]. Coll Antropol, 2008, 32 Suppl 2(3): S33-37.
17. Citirik M, Kabatas EU, Batman C, et al. Vitreous vascular endothelial growth factor concentrations in proliferative diabetic retinopathy versus proliferative vitreoretinopathy[J]. Ophthalmic Res, 2012, 47(1): 7-12. DOI: 10.1159/000324200.
18. Lei H, Hovland P, Velez G, et al. A potential role for PDGF-C in experimental and clinical proliferative vitreoretinopathy[J]. Invest Ophthalmol Vis Sci, 2007, 48(5): 2335-2342. DOI: 10.1167/iovs.06-0965.
19. Cui J, Lei H, Samad A, et al. PDGF receptors are activated in human epiretinal membranes[J]. Exp Eye Res, 2009, 88(3): 438-444. DOI: 10.1016/j.exer.2008.10.020.
20. Campochiaro PA, Hackett SF, Vinores SA, et al. Platelet-derived growth factor is an autocrine growth stimulator in retinal pigmented epithelial cells[J]. J Cell Sci, 1994, 107(Pt 9): 2459-2469.
21. Hoch RV, Soriano P. Roles of PDGF in animal development[J]. Development, 2003, 130 (20): 4769-4784. DOI: 10.1242/dev.00721.
22. Klinkhammer BM, Floege J, Boor P. PDGF in organ fibrosis[J/OL]. Mol Aspects Med, 2017, 2017: E1[2017-11-22]. https://doi.org/10.1016/j.mam.2017.11.008. DOI: 10.1016/j.mam.2017.11.008. [published online ahead of print].
23. Chan CM, Chang HH, Wang VC, et al. Inhibitory effects of resveratrol on PDGF-BB-induced retinal pigment epithelial cell migration via PDGFRbeta, PI3K/Akt and MAPK pathways[J/OL].PLoS One, 2013, 8(2): 56819[2013-02-14]. https://doi.org/10.1371/journal.pone.0056819. DOI: 10.1371/journal.pone.0056819.
24. Kumar A, Li X. PDGF-C and PDGF-D in ocular diseases[J/OL]. Mol Aspects Med, 2017, 2017: E1[2017-10-27]. https://doi.org/10.1016/j.mam.2017.10.002. DOI: 10.1016/j.mam.2017.10.002. [published online ahead of print].
25. Pennock S, Haddock LJ, Eliott D, et al. Is neutralizing vitreal growth factors a viable strategy to prevent proliferative vitreoretinopathy?[J]. Prog Retin Eye Res, 2014, 40: 16-34. DOI: 10.1016/j.preteyeres.2013.12.006.
26. Lei H, Rheaume MA, Cui J, et al. A novel function of p53: a gatekeeper of retinal detachment [J]. Am J Pathol, 2012, 181(3): 866-874. DOI: 10.1016/j.ajpath.2012.05.036.
27. Velez G, Weingarden AR, Tucker BA, et al. Retinal pigment epithelium and Müller progenitor cell interaction increase Müller progenitor cell expression of PDGFRα and ability to induce proliferative vitreoretinopathy in a rabbit model[J/OL]. Stem Cells Int, 2012, 2012: 106486 [2012-08-23]. http://dx.doi.org/10.1155/2012/106486. DOI: 10.1155/2012/106486.
28. Su CC, Chan CM, Chen HM, et al. Lutein inhibits the migration of retinal pigment epithelial cells via cytosolic and mitochondrial Akt pathways (lutein inhibits RPE cells migration)[J]. Int J Mol Sci, 2014, 15(8): 13755-13767. DOI: 10.3390/ijms150813755.
29. Pennock S, Kazlauskas A. Vascular endothelial growth factor A competitively inhibits platelet-derived growth factor (PDGF)-dependent activation of PDGF receptor and subsequent signaling events and cellular responses[J]. Mol Cell Biol, 2012, 32(10): 1955-1966. DOI: 10.1128/MCB.06668-11.
30. Pennock S, Kim D, Mukai S, et al. Ranibizumab is a potential prophylaxis for proliferative vitreoretinopathy, a nonangiogenic blinding disease[J]. Am J Pathol, 2013, 182(5): 1659-1670. DOI: 10.1016/j.ajpath.2013.01.052.
31. Lei H, Velez G, Kazlauskas A. Pathological signaling via platelet-derived growth factor receptor alpha involves chronic activation of Akt and suppression of p53[J]. Mol Cell Biol, 2011, 31(9): 1788-1799. DOI: 10.1128/MCB.01321-10.
32. Lei H, Kazlauskas A. A reactive oxygen species-mediated, self-perpetuating loop persistently activates platelet-derived growth factor receptor α[J]. Mol Cell Biol,2014,34(1): 110-122. DOI: 10.1128/MCB.00839-13.
33. Lemos A, Leão M, Soares J, et al. Medicinal chemistry strategies to disrupt the p53-MDM2/MDMX interaction[J]. Med Res Rev, 2016, 36(5): 789-844. DOI: 10.1002/med.21393.

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