Neovascular Progression and Retinal Dysfunction in the Laser-Induced Choroidal Neovascularization Mouse Model
Abstract
1. Introduction
2. Materials and Methods
2.1. Animals
2.2. Laser Photocoagulation
2.3. Multimodal Imaging and Focal Electroretinography Recording
2.4. Retinal Pigment Epithelium, Choroid, and Sclera Flat-Mounts
2.5. Real-Time PCR
2.6. Histology and Immunohistochemistry
2.7. Exclusion Criteria
2.8. Statistics
3. Results
3.1. LI-CNV Lesion Size Stabilized from Day 7 Post-Induction
3.2. The LI-CNV Mouse Model Presents a Retinal Dysfunction in Lesioned Areas
3.3. Neovascular Areas Are Maximal at 7 Days Post-Laser
3.4. Laser Photocoagulation Induces a Pro-Inflammatory but Not a Pro-Angiogenic Response
3.5. Inflammation and Fibrosis Are Present in the LI-CNV Lesions
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Colijn, J.M.; Buitendijk, G.H.S.; Prokofyeva, E.; Alves, D.; Cachulo, M.L.; Khawaja, A.P.; Cougnard-Gregoire, A.; Merle, B.M.J.; Korb, C.; Erke, M.G.; et al. Prevalence of Age-Related Macular Degeneration in Europe: The Past and the Future. Ophthalmology 2017, 124, 1753–1763. [Google Scholar] [CrossRef] [PubMed]
- Mitchell, P.; Liew, G.; Gopinath, B.; Wong, T.Y. Age-related macular degeneration. Lancet 2018, 392, 1147–1159. [Google Scholar] [CrossRef]
- Jonas, J.B.; Cheung, C.M.G.; Panda-Jonas, S. Updates on the epidemiology of age-related macular degeneration. Asia-Pacific J. Ophthalmol. 2017, 6, 493–497. [Google Scholar]
- Wong, W.L.; Su, X.; Li, X.; Cheung, C.M.G.; Klein, R.; Cheng, C.Y.; Wong, T.Y. Global prevalence of age-related macular degeneration and disease burden projection for 2020 and 2040: A systematic review and meta-analysis. Lancet Glob. Health 2014, 2, e106–e116. [Google Scholar] [CrossRef] [PubMed]
- Fleckenstein, M.; Keenan, T.D.L.; Guymer, R.H.; Chakravarthy, U.; Schmitz-Valckenberg, S.; Klaver, C.C.; Wong, W.T.; Chew, E.Y. Age-related macular degeneration. Nat. Rev. Dis. Prim. 2021, 7, 31. [Google Scholar] [CrossRef]
- Coleman, H.R.; Chan, C.C.; Ferris, F.L.; Chew, E.Y. Age-related macular degeneration. Lancet 2008, 372, 1835–1845. [Google Scholar] [CrossRef]
- Sacconi, R.; Fragiotta, S.; Sarraf, D.; Sadda, S.V.R.; Freund, K.B.; Parravano, M.; Corradetti, G.; Cabral, D.; Capuano, V.; Miere, A.; et al. Towards a better understanding of non-exudative choroidal and macular neovascularization. Prog. Retin. Eye Res. 2023, 92, 101113. [Google Scholar] [CrossRef]
- Campochiaro, P.A. Molecular Pathogenesis of Retinal and Choroidal Vascular Diseases. Prog. Retin. Eye Res. 2015, 49, 67. [Google Scholar] [CrossRef]
- Bhutto, I.; Lutty, G. Understanding age-related macular degeneration (AMD): Relationships between the photoreceptor/retinal pigment epithelium/Bruch’s membrane/choriocapillaris complex. Mol. Aspects Med. 2012, 33, 295–317. [Google Scholar] [CrossRef]
- Apte, R.S.; Chen, D.S.; Ferrara, N. VEGF in Signaling and Disease: Beyond Discovery and Development. Cell 2019, 176, 1248–1264. [Google Scholar] [CrossRef]
- Forooghian, F.; Razavi, R.; Timms, L. Hypoxia-inducible factor expression in human RPE cells. Br. J. Ophthalmol. 2007, 91, 1406–1410. [Google Scholar] [CrossRef] [PubMed]
- Khachigian, L.M.; Liew, G.; Teo, K.Y.C.; Wong, T.Y.; Mitchell, P. Emerging therapeutic strategies for unmet need in neovascular age-related macular degeneration. J. Transl. Med. 2023, 21, 133. [Google Scholar] [CrossRef] [PubMed]
- Vishwakarma, S.; Kaur, I. Molecular Mediators and Regulators of Retinal Angiogenesis. Semin. Ophthalmol. 2023, 38, 124–133. [Google Scholar] [CrossRef]
- Daniel, E.; Pan, W.; Ying, G.S.; Kim, B.J.; Grunwald, J.E.; Ferris, F.L.; Jaffe, G.J.; Toth, C.A.; Martin, D.F.; Fine, S.L.; et al. Development and Course of Scars in the Comparison of Age-Related Macular Degeneration Treatments Trials. Ophthalmology 2018, 125, 1037–1046. [Google Scholar] [CrossRef]
- Daniel, E.; Toth, C.A.; Grunwald, J.E.; Jaffe, G.J.; Martin, D.F.; Fine, S.L.; Huang, J.; Ying, G.S.; Hagstrom, S.A.; Winter, K.; et al. Risk of scar in the comparison of Age-related Macular Degeneration Treatments Trials. Ophthalmology 2014, 121, 656–666. [Google Scholar] [CrossRef]
- Grossniklaus, H.E.; Martinez, J.A.; Brown, V.B.; Lambert, H.M.; Sternberg, P.; Capone, A.; Aaberg, T.M.; Lopez, P.F. Immunohistochemical and histochemical properties of surgically excised subretinal neovascular membranes in age-related macular degeneration. Am. J. Ophthalmol. 1992, 114, 464–472. [Google Scholar] [CrossRef]
- Schlecht, A.; Boneva, S.; Gruber, M.; Zhang, P.; Horres, R.; Bucher, F.; Auw-Haedrich, C.; Hansen, L.; Stahl, A.; Hilgendorf, I.; et al. Transcriptomic Characterization of Human Choroidal Neovascular Membranes Identifies Calprotectin as a Novel Biomarker for Patients with Age-Related Macular Degeneration. Am. J. Pathol. 2020, 190, 1632–1642. [Google Scholar] [CrossRef] [PubMed]
- Little, K.; Llorián-Salvador, M.; Tang, M.; Du, X.; Marry, S.; Chen, M.; Xu, H. Macrophage to myofibroblast transition contributes to subretinal fibrosis secondary to neovascular age-related macular degeneration. J. Neuroinflammation 2020, 17, 355. [Google Scholar] [CrossRef]
- Brandli, A.; Khong, F.L.; Kong, R.C.K.; Kelly, D.J.; Fletcher, E.L. Transcriptomic analysis of choroidal neovascularization reveals dysregulation of immune and fibrosis pathways that are attenuated by a novel anti-fibrotic treatment. Sci. Rep. 2022, 12, 859. [Google Scholar] [CrossRef]
- Grossniklaus, H.E.; Kang, S.J.; Berglin, L. Animal models of choroidal and retinal neovascularization. Prog. Retin. Eye Res. 2010, 29, 500–519. [Google Scholar] [CrossRef]
- Ryan, S.J. The development of an experimental model of subretinal neovascularization in disciform macular degeneration. Trans. Am. Ophthalmol. Soc. 1979, 77, 707–745. [Google Scholar]
- Miller, H.; Miller, B.; Ryan, S.J. The role of retinal pigment epithelium in the involution of subretinal neovascularization. Investig. Ophthalmol. Vis. Sci. 1986, 27, 1644–1652. [Google Scholar]
- Criswell, M.H.; Ciulla, T.A.; Hill, T.E.; Small, W.; Danis, R.P.; Snyder, W.J.; Lowseth, L.A.; Carson, D.L. The Squirrel Monkey: Characterization of a New-World Primate Model of Experimental Choroidal Neovascularization and Comparison with the Macaque. Investig. Ophthalmol. Vis. Sci. 2004, 45, 625–634. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Tobe, T.; Ortega, S.; Luna, J.D.; Ozaki, H.; Okamoto, N.; Derevjanik, N.L.; Vinores, S.A.; Basilico, C.; Campochiaro, P.A. Targeted disruption of the FGF2 gene does not prevent choroidal neovascularization in a murine model. Am. J. Pathol. 1998, 153, 1641–1646. [Google Scholar] [CrossRef] [PubMed]
- Seo, M.S.; Kwak, N.; Ozaki, H.; Yamada, H.; Okamoto, N.; Yamada, E.; Fabbro, D.; Hofmann, F.; Wood, J.M.; Campochiaro, P.A. Dramatic inhibition of retinal and choroidal neovascularization by oral administration of a kinase inhibitor. Am. J. Pathol. 1999, 154, 1743–1753. [Google Scholar] [CrossRef]
- Dobi, E.T.; Puliafito, C.A.; Destro, M. A New Model of Experimental Choroidal Neovascularization in the Rat. Arch. Ophthalmol. 1989, 107, 264–269. [Google Scholar] [CrossRef]
- Frank, R.N.; Das, A.; Weber, M.L. A model of subretinal neovascularization in the pigmented rat. Curr. Eye Res. 1989, 8, 239–247. [Google Scholar] [CrossRef]
- Kimura, H.; Sakamoto, T.; Hinton, D.R.; Spee, C.; Ogura, Y.; Tabata, Y.; Ikada, Y.; Ryan, S.J. A new model of subretinal neovascularization in the rabbit. Investig. Ophthalmol. Vis. Sci. 1995, 36, 2110–2119. [Google Scholar]
- Saishin, Y.; Silva, R.L.; Saishin, Y.; Callahan, K.; Schoch, C.; Ahlheim, M.; Lai, H.; Kane, F.; Brazzell, R.K.; Bodmer, D.; et al. Periocular Injection of Microspheres Containing PKC412 Inhibits Choroidal Neovascularization in a Porcine Model. Investig. Ophthalmol. Vis. Sci. 2003, 44, 4989–4993. [Google Scholar] [CrossRef]
- Kiilgaard, J.F.; Andersen, M.V.N.; Wiencke, A.K.; Scherfig, E.; la Cour, M.; Tezel, T.H.; Prause, J.U. A new animal model of choroidal neovascularization. Acta Ophthalmol. Scand. 2005, 83, 697–704. [Google Scholar] [CrossRef]
- Spilsbury, K.; Garrett, K.L.; Shen, W.Y.; Constable, I.J.; Rakoczy, P.E. Overexpression of vascular endothelial growth factor (VEGF) in the retinal pigment epithelium leads to the development of choroidal neovascularization. Am. J. Pathol. 2000, 157, 135–144. [Google Scholar] [CrossRef]
- Rastoin, O.; Pagès, G.; Dufies, M. Experimental models in neovascular age related macular degeneration. Int. J. Mol. Sci. 2020, 21, 4627. [Google Scholar] [CrossRef] [PubMed]
- Zhu, Y.; Lu, Q.; Shen, J.; Zhang, L.; Gao, Y.; Shen, X.; Xie, B. Improvement and optimization of standards for a preclinical animal test model of laser induced choroidal neovascularization. PLoS ONE 2014, 9, e94743. [Google Scholar] [CrossRef]
- Poor, S.H.; Qiu, Y.; Fassbender, E.S.; Shen, S.; Woolfenden, A.; Delpero, A.; Kim, Y.; Buchanan, N.; Gebuhr, T.C.; Hanks, S.M.; et al. Reliability of the mouse model of choroidal neovascularization induced by laser photocoagulation. Investig. Ophthalmol. Vis. Sci. 2014, 55, 6525–6534. [Google Scholar] [CrossRef] [PubMed]
- Espinosa-Heidmann, D.G.; Marin-Castano, M.E.; Pereira-Simon, S.; Hernandez, E.P.; Elliot, S.; Cousins, S.W. Gender and estrogen supplementation increases severity of experimental choroidal neovascularization. Exp. Eye Res. 2005, 80, 413–423. [Google Scholar] [CrossRef]
- Schnabolk, G.; Stauffer, K.; O’Quinn, E.; Coughlin, B.; Kunchithapautham, K.; Rohrer, B. A comparative analysis of C57BL/6J and 6N substrains; chemokine/cytokine expression and susceptibility to laser-induced choroidal neovascularization. Exp. Eye Res. 2014, 129, 18–23. [Google Scholar] [CrossRef] [PubMed]
- Espinosa-Heidmann, D.G.; Suner, I.; Hernandez, E.P.; Frazier, W.D.; Csaky, K.G.; Cousins, S.W. Age as an Independent Risk Factor for Severity of Experimental Choroidal Neovascularization | IOVS | ARVO Journals. Investig. Ophthalmol. Vis. Sci. 2002, 43, 1567–1573. [Google Scholar]
- Edelman, J.L.; Castro, M.R. Quantitative image analysis of laser-induced choroidal neovascularization in rat. Exp. Eye Res. 2000, 71, 523–533. [Google Scholar] [CrossRef]
- Giani, A.; Thanos, A.; Roh, M.I.; Connolly, E.; Trichonas, G.; Kim, I.; Gragoudas, E.; Vavvas, D.; Miller, J.W. In Vivo Evaluation of Laser-Induced Choroidal Neovascularization Using Spectral-Domain Optical Coherence Tomography. Investig. Ophthalmol. Vis. Sci. 2011, 52, 3880. [Google Scholar] [CrossRef]
- Espinosa-Heidmann, D.G.; Suner, I.J.; Hernandez, E.P.; Monroy, D.; Csaky, K.G.; Cousins, S.W. Macrophage depletion diminishes lesion size and severity in experimental choroidal neovascularization. Investig. Ophthalmol. Vis. Sci. 2003, 44, 3586–3592. [Google Scholar] [CrossRef]
- Grossniklaus, H.E.; Ling, J.X.; Wallace, T.M.; Dithmar, S.; Lawson, D.H.; Cohen, C.; Elner, V.M.; Elner, S.G.; Sternberg, P., Jr. Macrophage and retinal pigment epithelium expression of angiogenic cytokines in choroidal neovascularization-PubMed. Mol. Vis. 2002, 8, 119–126. [Google Scholar] [PubMed]
- Fabian-Jessing, B.K.; Jakobsen, T.S.; Jensen, E.G.; Alsing, S.; Hansen, S.; Aagaard, L.; Askou, A.L.; Bek, T.; Corydon, T.J. Animal Models of Choroidal Neovascularization: A Systematic Review. Investig. Ophthalmol. Vis. Sci. 2022, 63, 11. [Google Scholar] [CrossRef]
- Pennesi, M.E.; Neuringer, M.; Courtney, R.J. Animal models of age related macular degeneration. Mol. Aspects Med. 2012, 33, 487–509. [Google Scholar] [CrossRef]
- Badia, A.; Duarri, A.; Salas, A.; Rosell, J.; Ramis, J.; Gusta, M.F.; Casals, E.; Zapata, M.A.; Puntes, V.; García-Arumí, J. Repeated Topical Administration of 3 nm Cerium Oxide Nanoparticles Reverts Disease Atrophic Phenotype and Arrests Neovascular Degeneration in AMD Mouse Models. ACS Nano 2023, 17, 910–926. [Google Scholar] [CrossRef]
- Ragauskas, S.; Kielczewski, E.; Vance, J.; Kaja, S.; Kalesnykas, G. In vivo multimodal imaging and analysis of mouse laser-induced choroidal neovascularization model. J. Vis. Exp. 2018, 2018, 56173. [Google Scholar] [CrossRef]
- Zhao, M.; Xie, W.; Hein, T.W.; Kuo, L.; Rosa, R.H. Laser-Induced Choroidal Neovascularization in Rats. In Methods in Molecular Biology; Humana Press Inc.: Totowa, NJ, USA, 2021; Volume 2319, pp. 77–85. [Google Scholar]
- Shah, R.S.; Soetikno, B.T.; Lajko, M.; Fawzi, A.A. A Mouse Model for Laser-induced Choroidal Neovascularization. J. Vis. Exp 2015, 106, 53502. [Google Scholar] [CrossRef]
- Lambert, V.; Lecomte, J.; Hansen, S.; Blacher, S.; Gonzalez, M.L.A.; Struman, I.; Sounni, N.E.; Rozet, E.; De Tullio, P.; Foidart, J.M.; et al. Laser-induced choroidal neovascularization model to study age-related macular degeneration in mice. Nat. Protoc. 2013, 8, 2197–2211. [Google Scholar] [CrossRef]
- Schneider, C.A.; Rasband, W.S.; Eliceiri, K.W. NIH Image to ImageJ: 25 years of Image Analysis. Nat. Methods 2012, 9, 671. [Google Scholar] [CrossRef] [PubMed]
- Badia, A.; Salas, A.; Duarri, A.; Ferreira-de-Souza, B.; Zapata, M.Á.; Fontrodona, L.; García-Arumí, J. Transcriptomics analysis of Ccl2/Cx3cr1/Crb1rd8 deficient mice provides new insights into the pathophysiology of progressive retinal degeneration. Exp. Eye Res. 2021, 203, 108424. [Google Scholar] [CrossRef]
- Gong, Y.; Li, J.; Sun, Y.; Fu, Z.; Liu, C.H.; Evans, L.; Tian, K.; Saba, N.; Fredrick, T.; Morss, P.; et al. Optimization of an image-guided laser-induced choroidal neovascularization model in mice. PLoS ONE 2015, 10, e0132643. [Google Scholar] [CrossRef]
- Congdon, N. Causes and Prevalence of Visual Impairment among Adults in the United States. Arch. Ophthalmol. 2004, 122, 477–485. [Google Scholar] [CrossRef] [PubMed]
- Lim, L.S.; Mitchell, P.; Seddon, J.M.; Holz, F.G.; Wong, T.Y. Age-related macular degeneration. Lancet 2012, 379, 1728–1738. [Google Scholar] [CrossRef] [PubMed]
- Mattapallil, M.J.; Wawrousek, E.F.; Chan, C.C.; Zhao, H.; Roychoudhury, J.; Ferguson, T.A.; Caspi, R.R. The Rd8 mutation of the Crb1 gene is present in vendor lines of C57BL/6N mice and embryonic stem cells, and confounds ocular induced mutant phenotypes. Investig. Ophthalmol. Vis. Sci. 2012, 53, 2921–2927. [Google Scholar] [CrossRef]
- Aredo, B.; Zhang, K.; Chen, X.; Wang, C.X.Z.; Li, T.; Ufret-Vincenty, R.L. Differences in the distribution, phenotype and gene expression of subretinal microglia/macrophages in C57BL/6N (Crb1rd8/rd8) versus C57BL6/J (Crb1wt/wt) mice. J. Neuroinflamm. 2015, 12, 6. [Google Scholar] [CrossRef]
- Jawad, S.; Liu, B.; Li, Z.; Katamay, R.; Campos, M.; Wei, L.; Sen, H.N.; Ling, D.; Estrada, F.M.; Amaral, J.; et al. The role of macrophage class a scavenger receptors in a laser-induced murine choroidal neovascularization model. Investig. Ophthalmol. Vis. Sci. 2013, 54, 5959–5970. [Google Scholar] [CrossRef]
- Caicedo, A.; Espinosa-Heidmann, D.G.; Hamasaki, D.; Piña, Y.; Cousins, S.W. Photoreceptor synapses degenerate early in experimental choroidal neovascularization. J. Comp. Neurol. 2005, 483, 263–277. [Google Scholar] [CrossRef] [PubMed]
- Hoerster, R.; Muether, P.S.; Vierkotten, S.; Schröder, S.; Kirchhof, B.; Fauser, S. In-vivo and ex-vivo characterization of laser-induced choroidal neovascularization variability in mice. Graefe’s Arch. Clin. Exp. Ophthalmol. 2012, 250, 1579–1586. [Google Scholar] [CrossRef]
- Shansky, R.M. Sex differences in mechanisms of disease. Genes Brain Behav. 2020, 19, e12646. [Google Scholar] [CrossRef]
- Ramsey, D.J.; Ripps, H.; Qian, H. An electrophysiological study of retinal function in the diabetic female rat. Investig. Ophthalmol. Vis. Sci. 2006, 47, 5116–5124. [Google Scholar] [CrossRef]
- Toker, E.; Yenice, Ö.; Akpinar, I.; Aribal, E.; Kazokoglu, H. The influence of sex hormones on ocular blood flow in women. Acta Ophthalmol. Scand. 2003, 81, 617–624. [Google Scholar] [CrossRef]
- Sulaiman, R.S.; Quigley, J.; Qi, X.; O’Hare, M.N.; Grant, M.B.; Boulton, M.E.; Corson, T.W. A simple optical coherence tomography quantification method for choroidal neovascularization. J. Ocul. Pharmacol. Ther. 2015, 31, 447–454. [Google Scholar] [CrossRef] [PubMed]
- André, H.; Tunik, S.; Aronsson, M.; Kvanta, A. Hypoxia-inducible factor-1α Is associated with sprouting angiogenesis in the murine laser-induced Choroidal neovascularization model. Investig. Ophthalmol. Vis. Sci. 2015, 56, 6591–6604. [Google Scholar] [CrossRef] [PubMed]
- Zhou, Y.; Yoshida, S.; Kubo, Y.; Yoshimura, T.; Kobayashi, Y.; Nakama, T.; Yamaguchi, M.; Ishikawa, K.; Oshima, Y.; Ishibashi, T. Different distributions of M1 and M2 macrophages in a mouse model of laser-induced choroidal neovascularization. Mol. Med. Rep. 2017, 15, 3949–3956. [Google Scholar] [CrossRef]
- Yang, C.; Tang, D. Patient-Specific Carotid Plaque Progression Simulation. C. Model. Eng. Sci. 2000, 1, 119–131. [Google Scholar] [CrossRef]
- Wang, H.; Han, X.; Wittchen, E.S.; Hartnett, M.E. TNF-α mediates choroidal neovascularization by upregulating VEGF expression in RPE through ROS-dependent β-catenin activation. Mol. Vis. 2016, 22, 116–128. [Google Scholar]
- Xu, J.; Zhu, D.; Sonoda, S.; He, S.; Spee, C.; Ryan, S.J.; Hinton, D.R. Over-expression of BMP4 inhibits experimental choroidal neovascularization by modulating VEGF and MMP-9. Angiogenesis 2012, 15, 213–227. [Google Scholar] [CrossRef]
- Bora, P.S.; Sohn, J.-H.; Cruz, J.M.C.; Jha, P.; Nishihori, H.; Wang, Y.; Kaliappan, S.; Kaplan, H.J.; Bora, N.S. Role of Complement and Complement Membrane Attack Complex in Laser-Induced Choroidal Neovascularization. J. Immunol. 2005, 174, 491–497. [Google Scholar] [CrossRef]
- Yanai, R.; Chen, S.; Uchi, S.H.; Nanri, T.; Connor, K.M.; Kimura, K. Attenuation of choroidal neovascularization by dietary intake of ω-3 long-chain polyunsaturated fatty acids and lutein in mice. PLoS ONE 2018, 13, e0196037. [Google Scholar] [CrossRef]
- Hasegawa, E.; Inafuku, S.; Mulki, L.; Okunuki, Y.; Yanai, R.; Smith, K.E.; Kim, C.B.; Klokman, G.; Bielenberg, D.R.; Puli, N.; et al. Cytochrome P450 monooxygenase lipid metabolites are significant second messengers in the resolution of choroidal neovascularization. Proc. Natl. Acad. Sci. USA 2017, 114, E7545–E7553. [Google Scholar] [CrossRef]
- Jeong, J.H.; Ojha, U.; Lee, Y.M. Pathological angiogenesis and inflammation in tissues. Arch. Pharm. Res. 2021, 44, 1. [Google Scholar] [CrossRef] [PubMed]
- Nguyen, D.D.; Luo, L.J.; Yang, C.J.; Lai, J.Y. Highly Retina-Permeating and Long-Acting Resveratrol/Metformin Nanotherapeutics for Enhanced Treatment of Macular Degeneration. ACS Nano 2023, 17, 168–183. [Google Scholar] [CrossRef] [PubMed]
- Li, L.; Cao, X.; Huang, L.; Huang, X.; Gu, J.; Yu, X.; Zhu, Y.; Zhou, Y.; Song, Y.; Zhu, M. Lycopene inhibits endothelial-to-mesenchymal transition of choroidal vascular endothelial cells in laser-induced mouse choroidal neovascularization. J. Cell. Mol. Med. 2023, 27, 1327–1340. [Google Scholar] [CrossRef] [PubMed]
- Liang, I.C.; Ko, W.C.; Hsu, Y.J.; Lin, Y.R.; Chang, Y.H.; Zong, X.H.; Lai, P.C.; Chang, D.C.; Hung, C.F. The anti-inflammatory effect of hydrogen gas inhalation and its influence on laser-induced choroidal neovascularization in a mouse model of neovascular age-related macular degeneration. Int. J. Mol. Sci. 2021, 22, 2049. [Google Scholar] [CrossRef]
- Wang, Y.; Xie, L.; Zhu, M.; Guo, Y.; Tu, Y.; Zhou, Y.; Zeng, J.; Zhu, L.; Du, S.; Wang, Z.; et al. Shikonin alleviates choroidal neovascularization by inhibiting proangiogenic factor production from infiltrating macrophages. Exp. Eye Res. 2021, 213, 108823. [Google Scholar] [CrossRef] [PubMed]
- Do, J.Y.; Kim, J.; Kim, M.J.; Lee, J.Y.; Park, S.Y.; Yanai, R.; Lee, I.K.; Park, S.; Park, D.H. Fursultiamine alleviates choroidal neovascularization by suppressing inflammation and metabolic reprogramming. Investig. Ophthalmol. Vis. Sci. 2020, 61, 24. [Google Scholar] [CrossRef] [PubMed]
- Cui, K.; Liu, J.; Huang, L.; Qin, B.; Yang, X.; Li, L.; Liu, Y.; Gu, J.; Wu, W.; Yu, Y.; et al. Andrographolide attenuates choroidal neovascularization by inhibiting the HIF-1α/VEGF signaling pathway. Biochem. Biophys. Res. Commun. 2020, 530, 60–66. [Google Scholar] [CrossRef]
- Narendran, S.; Pereira, F.; Yerramothu, P.; Apicella, I.; Wang, S.B.; Varshney, A.; Baker, K.L.; Marion, K.M.; Ambati, M.; Ambati, V.L.; et al. A clinical metabolite of azidothymidine inhibits experimental choroidal neovascularization and retinal pigmented epithelium degeneration. Investig. Ophthalmol. Vis. Sci. 2020, 61, 4. [Google Scholar] [CrossRef]
- Bao, Y.; Huang, L.; Huang, X.; Gao, C.; Chen, Y.; Wu, L.; Zhu, S.; Song, Y. Pirfenidone ameliorates the formation of choroidal neovascularization in mice. Mol. Med. Rep. 2020, 21, 2162–2170. [Google Scholar] [CrossRef]
- Heloterä, H.; Kaarniranta, K. A Linkage between Angiogenesis and Inflammation in Neovascular Age-Related Macular Degeneration. Cells 2022, 11, 3453. [Google Scholar] [CrossRef]
- Wang, Y.; Wang, V.M.; Chan, C.C. The role of anti-inflammatory agents in age-related macular degeneration (AMD) treatment. Eye 2011, 25, 127–139. [Google Scholar] [CrossRef]
- Kuppermann, B.D.; Goldstein, M.; Maturi, R.K.; Pollack, A.; Singer, M.; Tufail, A.; Weinberger, D.; Li, X.Y.; Liu, C.C.; Lou, J.; et al. Dexamethasone Intravitreal Implant as Adjunctive Therapy to Ranibizumab in Neovascular Age-Related Macular Degeneration: A Multicenter Randomized Controlled Trial. Ophthalmologica 2015, 234, 40–54. [Google Scholar] [CrossRef] [PubMed]
- Becerra, E.M.; Morescalchi, F.; Gandolfo, F.; Danzi, P.; Nascimbeni, G.; Arcidiacono, B.; Semeraro, F. Clinical evidence of intravitreal triamcinolone acetonide in the management of age-related macular degeneration. Curr. Drug Targets 2011, 12, 149–172. [Google Scholar] [CrossRef]
- Ando, R.; Hirooka, K.; Saito, M.; Kase, S.; Noda, K.; Ishida, S. Two-year clinical outcomes of triple therapy with photodynamic therapy, anti-vascular endothelial growth factor agent, and triamcinolone acetonide for neovascular age-related macular degeneration. Jpn. J. Ophthalmol. 2023, 67, 50–58. [Google Scholar] [CrossRef] [PubMed]
- Forte, R.; Bonavolontà, P.; Benayoun, Y.; Adenis, J.P.; Robert, P.Y. Intravitreal ranibizumab and bevacizumab in combination with full-fluence verteporfin therapy and dexamethasone for exudative age-related macular degeneration. Ophthalmic Res. 2011, 45, 129–134. [Google Scholar] [CrossRef] [PubMed]
- Frimpong-Boateng, A.; Bunse, A.; Rüfer, F.; Roider, J. Photodynamic therapy with intravitreal application of triamcinolone acetonide in age-related macular degeneration: Functional results in 54 patients. Acta Ophthalmol. 2009, 87, 183–187. [Google Scholar] [CrossRef]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Salas, A.; Badia, A.; Fontrodona, L.; Zapata, M.; García-Arumí, J.; Duarri, A. Neovascular Progression and Retinal Dysfunction in the Laser-Induced Choroidal Neovascularization Mouse Model. Biomedicines 2023, 11, 2445. https://doi.org/10.3390/biomedicines11092445
Salas A, Badia A, Fontrodona L, Zapata M, García-Arumí J, Duarri A. Neovascular Progression and Retinal Dysfunction in the Laser-Induced Choroidal Neovascularization Mouse Model. Biomedicines. 2023; 11(9):2445. https://doi.org/10.3390/biomedicines11092445
Chicago/Turabian StyleSalas, Anna, Anna Badia, Laura Fontrodona, Miguel Zapata, José García-Arumí, and Anna Duarri. 2023. "Neovascular Progression and Retinal Dysfunction in the Laser-Induced Choroidal Neovascularization Mouse Model" Biomedicines 11, no. 9: 2445. https://doi.org/10.3390/biomedicines11092445
APA StyleSalas, A., Badia, A., Fontrodona, L., Zapata, M., García-Arumí, J., & Duarri, A. (2023). Neovascular Progression and Retinal Dysfunction in the Laser-Induced Choroidal Neovascularization Mouse Model. Biomedicines, 11(9), 2445. https://doi.org/10.3390/biomedicines11092445