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On phagocytes and macular degeneration
Open accessAbstract
Age related macular degeneration (AMD) is a complex multifactorial disease caused by the interplay of age and genetic and environmental risk factors. A common feature observed in early and both forms of late AMD is the breakdown of the physiologically immunosuppressive subretinal environment and the protracted accumulation of mononuclear phagocytes (MP). We here discuss the origin and nature of subretinal MPs, the mechanisms that lead to their accumulation, the inflammatory mediators they produce as well as the consequences of their chronic presence on photoreceptors, retinal pigment epithelium and choroid. Recent advances highlight how both genetic and environmental risk factors directly promote subretinal inflammation and tip the balance from a beneficial inflammation that helps control debris accumulation to detrimental chronic inflammation and destructive late AMD. Finally, we discuss how changes in life style or pharmacological intervention can help to break the vicious cycle of inflammation and degeneration, restore the immunosuppressive properties of the subretinal space, and reestablish homeostasis.
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BackgroundInfluentialSelf-citationIL-1β induces rod degeneration through the disruption of retinal glutamate homeostasis
Charles‐Messance, H., Blot, G., Couturier, A., Vignaud, L., Touhami, S., Béguier, F., Siqueiros‐Márquez, L., Forster, V., Barmo, N., Augustin, S., et al. (2020) · Journal of Neuroinflammation · doi:10.1186/s12974-019-1655-5 · Cited by 154
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Retinal microglia: Functions and diseases
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“This topic has recently been reviewed in this journal (Guillonneau et al., 2017) and once again highlights the importance of our emerging understanding of the immune cells in the choroid.”
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“Indeed, RPE dysfunction and nonresolving inflammation remain two prominent hypotheses for the pathogenesis of AMD (Xu et al., 2009; Guillonneau et al., 2017).”
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“Choroidal involution, non-resolving low-grade inflammation, and RPE dysfunction and resulting defective photoreceptor outer segment renewal are the prominent proposed hypotheses for its pathogenesis [30].”
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Glaucoma: from pathogenic mechanisms to retinal glial cell response to damage
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“The dominant paradigm states that AMD results from cumulative damage affecting the interaction between the photoreceptors and the RPE cells related to genetically determined low grade subretinal inflammation (Guillonneau et al., 2017).”
Self-citationHuman aging and disease: Lessons from age-related macular degeneration
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“This is consistent with other models of neurodegeneration that have shown Ly6C classical monocytes, and inflammatory monocytes can infiltrate tissue and differentiate into pro-inflammatory macrophages and dendritic cells ([43, 44] for review).”
ResultBrinks, J., van Dijk, E. H. C., Klaassen, I., Schlingemann, R. O., Kiełbasa, S. M., Emri, E., Quax, P. H. A., Bergen, A. A. B., Meijer, O. C., & Boon, C. J. F. (2021) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2021.100994 · Cited by 82
Single-cell analysis reveals inflammatory interactions driving macular degeneration
Kuchroo, M. R., DiStasio, M., Song, E., Calapkulu, E., Zhang, L., Ige, M., Sheth, A. H., Majdoubi, A., Menon, M., Tong, A., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-37025-7 · Cited by 78
“…origin into circulating macrophages, tissue resident macrophages, and microglia remains challenging, it is believed that the mononuclear phagocytes found at the apical side of the RPE in the vicinity of drusen, which induce activation of the in fl ammasome, come from all three populations 56 .”
Jabbehdari, S., & Handa, J. T. (2020) · Survey of Ophthalmology · doi:10.1016/j.survophthal.2020.09.002 · Cited by 61
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“While the specific causes of AMD remain unclear, data strongly support that RPE dysfunction and degeneration precede PR loss, and that chronic RPE inflammation contributes to RPE and PR death (55).”
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InfluentialBalser, C., Wolf, A., Herb, M., & Langmann, T. (2019) · Journal of Neuroinflammation · doi:10.1186/s12974-019-1419-2 · Cited by 62
“However, by producing pro-angiogenic cytokines and growth factors including VEGF and placental growth factor (PGF), mononuclear phagocytes may also play a role in neovascularization [6].”
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“Their accumulation has been shown to play an important role in the pathogenesis of many chronic, age-related diseases [13, 14], including late AMD [3, 10] where they have been shown to play a critical role in neovascularization and photoreceptor degeneration [3].”
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InfluentialHammadi, S., Tzoumas, N., Ferrara, M., Meschede, I. P., Lo, K., Harris, C., Lako, M., & Steel, D. H. (2023) · Journal of Clinical Medicine · doi:10.3390/jcm12082870 · Cited by 44
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Myeloid cells in retinal and brain degeneration
Guo, M., Schwartz, T. D., Dunaief, J. L., & Cui, Q. N. (2021) · FEBS Journal · doi:10.1111/febs.16177 · Cited by 25
Vascular Inflammation Risk Factors in Retinal Disease
Soto, I., Krebs, M. P., Reagan, A. M., & Howell, G. R. (2019) · Annual Review of Vision Science · doi:10.1146/annurev-vision-091517-034416 · Cited by 24
Peripheral Monocyte Count and Age-Related Macular Degeneration. The Tongren Health Care Study
Xue, C. C., Cui, J., Gao, L. Q., Zhang, C., Dou, H. L., Chen, D. N., Wang, Y. X., & Jonas, J. B. (2021) · American Journal of Ophthalmology · doi:10.1016/j.ajo.2021.03.010 · Cited by 22
Cho, H.-M., Jo, Y.-D., & Choung, S. (2022) · Nutrients · doi:10.3390/nu14030401 · Cited by 24
“To correlate with in vitro study, we investigated expressions of inflammation-related genes (TNF-α, CXCL-2, IL-1β, IL-6, and MCP-1) and angiogenesis-related genes (MMP-2, MMP-9, and VEGF-A) in mice retina (Figure 5A).”
BackgroundInfluentialTan, Y., Jianguo, H., Li, D., Zou, C., Liu, D., & Qin, B. (2023) · Ageing Research Reviews · doi:10.1016/j.arr.2023.102030 · Cited by 22
Blot, G., Karadayi, R., Przegralek, L., Sartoris, T.-M., Charles‐Messance, H., Augustin, S., Négrier, P., Blond, F., Muñiz-Ruvalcaba, F. P., la Parra, D. R.-D., et al. (2023) · Journal of Clinical Investigation · doi:10.1172/jci161348 · Cited by 22
“In contrast, subretinal MPs in exudative age-related macular degeneration show proangiogenic activity (58, 59).”
Self-citationNew concepts in macrophage ontogeny in the adult neural retina
Saban, D. R. (2018) · Cellular Immunology · doi:10.1016/j.cellimm.2018.04.008 · Cited by 22
Age-related pro-inflammatory and pro-angiogenic changes in human aqueous humor
Yan, Z., Rao, Y., Li, J.-K., Huang, Y., Zhao, P., & Li, J. (2018) · International Journal of Ophthalmology · doi:10.18240/ijo.2018.02.03 · Cited by 21
Autophagy in drusen biogenesis secondary to age‐related macular degeneration
Hyttinen, J. M. T., Koskela, A. K. J., Błasiak, J., & Kaarniranta, K. (2024) · Acta Ophthalmologica · doi:10.1111/aos.16744 · Cited by 22
“The presence of drusen maintains chronic inflammation as well (Fletcher, 2020; Guillonneau et al., 2017).”
Label-Free Imaging of Inflammation at the Level of Single Cells in the Living Human Eye
Rui, Y., Zhang, M., Lee, D. M. W., Snyder, V. C., Raghuraman, R., Gofas-Salas, E., Mecê, P., Yadav, S., Tiruveedhula, P. K., Grieve, K. F., et al. (2024) · Ophthalmology Science · doi:10.1016/j.xops.2024.100475 · Cited by 20
“31 More work is still needed to re fi ne this tool for clinical use, but we have demonstrated here that the technological improvements afforded through simultaneous multioffset detection using a FB are a major step forward, reducing the acquisition time substantially and allowing for fi ne-scale…”
Self-citationKlipfel, L., Cordonnier, M., Thiébault, L., Clérin, E., Blond, F., Millet-Puel, G., Mohand‐Saïd, S., Goureau, O., Sahel, J., Nandrot, E. F., et al. (2021) · Cells · doi:10.3390/cells10010179 · Cited by 20
“One of the prominent accepted hypotheses proposes that degeneration results from an initial defect in photoreceptor outer segment processing by the retinal pigment epithelium (RPE) [1].”
BackgroundSelf-citationGu, B. J., Huang, X., Avula, P. K., Caruso, E., Drysdale, C., Vessey, K. A., Ou, A., Fowler, C. J., Liu, T.-H., Lin, Y. Q., et al. (2021) · Frontiers in Medicine · doi:10.3389/fmed.2021.634177 · Cited by 20
“Notably, mononuclear phagocytes that includes peripheral blood monocytes, macrophages and retinal microglia, accumulate within and around drusen, RPD, and also in zones of atrophy (11).”
BackgroundLazzara, F., Conti, F., Eandi, C. M., Eandi, C. M., Drago, F., & Bucolo, C. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.778165 · Cited by 19
Self-citationInsulin inhibits inflammation-induced cone death in retinal detachment
Conart, J., Blot, G., Augustin, S., Millet-Puel, G., Roubeix, C., Béguier, F., Charles‐Messance, H., Touhami, S., Sahel, J., Berrod, J., et al. (2020) · Journal of Neuroinflammation · doi:10.1186/s12974-020-02039-1 · Cited by 19
Self-citationOtsuki, Y., Ito, E., Mukai, A., Ueno, M., Yamawaki, T., Sotozono, C., Kinoshita, S., & Hamuro, J. (2021) · Experimental Eye Research · doi:10.1016/j.exer.2021.108496 · Cited by 19
Myeloid‐resident neuropilin‐1 promotes choroidal neovascularization while mitigating inflammation
Andriessen, E. M. M. A., Binet, F., Fournier, F., Hata, M., Dejda, A., Mawambo, G., Crespo‐Garcia, S., Pilon, F., Buscarlet, M., Beauchemin, K., et al. (2021) · EMBO Molecular Medicine · doi:10.15252/emmm.201911754 · Cited by 17
“Inade-quate clearance of these deposits can trigger a pathologic inflammatory response and ensuing tissue damage (Guillonneau et al, 2017; Handa et al, 2017).”
Self-citationP2X7-dependent immune pathways in retinal diseases
Déchelle-Marquet, P.-A., Guillonneau, X., Sennlaub, F., & Delarasse, C. (2022) · Neuropharmacology · doi:10.1016/j.neuropharm.2022.109332 · Cited by 20
Self-citationTerauchi, R., Kohno, H., Watanabe, S., Saitô, S., Watanabe, A., & Nakano, T. (2021) · PLoS ONE · doi:10.1371/journal.pone.0239108 · Cited by 18
Krueger, K., Boehme, E., Klettner, A., & Zille, M. (2021) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2021.1915242 · Cited by 18
“TNF can be observed in neovascular tissue and may interfere with RPE function (Oh et al. 1999; Guillonneau et al. 2017).”
BackgroundInfluentialLiisborg, C., Skov, V., Kjær, L., Hasselbalch, H. C., & Sørensen, T. L. (2021) · EClinicalMedicine · doi:10.1016/j.eclinm.2021.101248 · Cited by 18
CD36 Deficiency Inhibits Retinal Inflammation and Retinal Degeneration in Cx3cr1 Knockout Mice
Lavalette, S., Conart, J., Touhami, S., Roubeix, C., Houssier, M., Augustin, S., Raoul, W., Combadière, C., Febbraio, M., Ong, H., et al. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2019.03032 · Cited by 18
“This is likely due to APOE-induced cholesterol extraction from the lipid rafts of MPs, which lifts the physiological separation of CD14 (located in the lipid raft) from TLR2 (located in non-lipid raft membrane) and triggers NFκB activation and cytokine secretion in the absence of TLR ligands, as previously demonstrate…”
BackgroundSelf-citationTraversing the epigenetic landscape: DNA methylation from retina to brain in development and disease
Xu, C., Fu, X., Qin, H., & Yao, K. (2024) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2024.1499719 · Cited by 17
“As the disease progresses, central choroidal neovascularization develops, ultimately leading to the formation of a disciform scar, that significantly impairs visual function (Guillonneau et al., 2017; Figure 4A).”
Liisborg, C., Nielsen, M. K., Hasselbalch, H. C., & Sørensen, T. L. (2020) · EClinicalMedicine · doi:10.1016/j.eclinm.2020.100526 · Cited by 17
“The chronic pro-inflammatory environment in patients with MPNs could also contribute to the overactivation of microglia by promoting blood-derived inflammatory mononuclear phagocytes with characteristics that lead to resisted elimination and excessive recruitment in the subretinal space [54].”
BackgroundShu, X., Hu, Y., Huang, C., & Wei, N. (2021) · Saudi Journal of Biological Sciences · doi:10.1016/j.sjbs.2021.06.039 · Cited by 18
“Numerous mechanisms are participated in the development of DR like pro-inflammatory mediators, microvascular injury, and oxidative stress (Guzman et al., 2016).”
BackgroundRe-programming immunosurveillance in persistent non-infectious ocular inflammation
Epps, S. J., Boldison, J., Stimpson, M. L., Khera, T. K., Lait, P. J. P., Copland, D. A., Dick, A. D., & Nicholson, L. B. (2018) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2018.03.001 · Cited by 17
“Under these circumstance there may be movement of the microglia and recruited macrophages to the subretinal space, where they are retained rather than being cleared by normal homeostatic processes (Guillonneau et al., 2017).”
BackgroundDu, X., Peñalva, R. G., Little, K., Kissenpfennig, A., Chen, M., & Xu, H. (2021) · Molecular Neurodegeneration · doi:10.1186/s13024-021-00432-9 · Cited by 16
Liu, W., Jiang, X., Li, X., Sun, K., Yang, Y., Yang, M., Li, S., & Zhu, X. (2022) · Journal of Cell Science · doi:10.1242/jcs.259468 · Cited by 16
Shedding light on eye disease in obesity: A review
Lam, S., Lindsey, J. L., Leon, B. G. C., & Takkouche, S. K. (2023) · Clinical Obesity · doi:10.1111/cob.12616 · Cited by 20
“25 Analyses of patients with AMD revealed higher levels of aqueous humour cytokines such as CRP, IL-6, and several subtypes of amyloid.”
BackgroundPhase 2 Trial Evaluating Minocycline for Geographic Atrophy in Age-Related Macular Degeneration
Keenan, T. D. L., Bailey, C., Abraham, M., Orndahl, C. M., Menezes, S. M., Bellur, S., Arunachalam, T., Kangale-Whitney, C., Srinivas, S., Karamat, A., et al. (2024) · JAMA Ophthalmology · doi:10.1001/jamaophthalmol.2024.0118 · Cited by 16
Monocyte Invasion into the Retina Restricts the Regeneration of Neurons from Müller Glia
Blasdel, N., Bhattacharya, S., Donaldson, P. C., Reh, T. A., & Todd, L. J. (2024) · Journal of Neuroscience · doi:10.1523/jneurosci.0938-24.2024 · Cited by 15
Mathis, T., Baudin, F., Mariet, A., Augustin, S., Bricout, M., Przegralek, L., Roubeix, C., Benzenine, É., Blot, G., Nous, C., et al. (2024) · Journal of Clinical Investigation · doi:10.1172/jci174199 · Cited by 14
“…cells (red; Figure 1C), prepared after an additional 7 days of continued treatment, demonstrated that the number of subretinal infiltrating MPs, a driving force of CNV development (6), was not affected by either the MPTP-induced nigrostriatal lesion or the l-DOPA/benser-azide treatment (Figure 1D).”
Self-citationApolipoprotein ε in Brain and Retinal Neurodegenerative Diseases
Abyadeh, M., Gupta, V., Paulo, J. A., Sheriff, S., Shadfar, S., Fitzhenry, M. J., Amirkhani, A., Gupta, V. B., Salekdeh, G. H., Haynes, P. A., et al. (2023) · Aging and Disease · doi:10.14336/ad.2023.0312-1 · Cited by 15
“This was followed by subretinal inflammation, photoreceptor degeneration and CNV formation [79, 80].”
Twarog, M., Schustak, J., Xu, Y., Coble, M., Dolan, K., Esterberg, R., Huang, Q., Saint‐Geniez, M., & Bao, Y. (2023) · Scientific Reports · doi:10.1038/s41598-023-41610-7 · Cited by 15
“Cells were passaged every 3 days until seeding into vessels for experimentation.”
Method
Metadata
- Authors
- Guillonneau, X., Eandi, C. M., Paques, M., Sahel, J.-A., Sapieha, P., & Sennlaub, F.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- University of Turin (IT)
- Hôpital Maisonneuve-Rosemont (CA)
- Corresponding author
- Sennlaub, Florian
- Venue
- Progress in Retinal and Eye Research
- Publisher
- Elsevier BV
- Published
- 2017-11
- Volume
- 61
- Pages
- 98-128
- ISSN
- 1350-9462 (ISSN-L)
- OpenAlex
- W2622806731
- Cited by
- 185
- References
- 399
- Citations by year
- 2026: 13 · 2025: 15 · 2024: 31 · 2023: 16 · 2022: 19 · 2021: 33 · 2020: 20 · 2019: 19 · 2018: 18 · 2017: 1
- FWCI
- 2.91
- Type
- journal article
- Language
- en
- Open access
- Licence
- Locations
- Progress in Retinal and Eye Research (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion, other-oa)
- Institutional Research Information System University of Turin (University of Turin) (submittedVersion)
- Funders
- INSERM
- ANR Geno 2009 (R09099DS)
- ANR MACLEAR (ANR-15-CE14-0015-01)
- LABEX LIFESENSES (ANR-10-LABX-65)
- ANR (Investissements d'Avenir programme (ANR-11-IDEX-0004-02)
- Carnot
- ERC (ERC-2007 St.G. 210345)
- Association de Prévoyance Santé de ALLIANZ
- Topics
- Health Sciences › Medicine › Ophthalmology › Retinal Diseases and Treatments
- Health Sciences › Medicine › Ophthalmology › Ocular Diseases and Behçet’s Syndrome
- Health Sciences › Medicine › Ophthalmology › Retinal Development and Disorders
- Keywords
- age-related macular degeneration, mononuclear phagocytes, chronic inflammation, retinal pigment epithelium, photoreceptors, choroid, genetic risk factors, environmental risk factors, immunosuppression, lifestyle modification
- MeSH terms
- Choroid, Humans, Life Style, Macular Degeneration, Macular Edema, Phagocytes, Photoreceptor Cells, Retinal Pigment Epithelium
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