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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Body mass index and the risk of Parkinson disease
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Sub-retinal drusenoid deposits in human retina: Organization and composition
Rudolf, M., Malek, G., Messinger, J. D., Clark, M. E., Wang, L., & Curcio, C. A. (2008) · Experimental Eye Research · doi:10.1016/j.exer.2008.07.010 · Cited by 201 · see citing works
Gut microbiota influences pathological angiogenesis in obesity‐driven choroidal neovascularization
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Self-citationDendritic cell physiology and function in the eye
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The spectrum of complement alternative pathway‐mediated diseases
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CRB1 mutations in inherited retinal dystrophies
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Microglia in Retinal Degeneration
Rashid, K., Akhtar‐Schäfer, I., & Langmann, T. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01975 · Cited by 354 · see citing works
“Once in the subretinal space, microglia and other mononuclear phagocytes enhance their phagocytic capacity and produce high levels of pro-inflammatory factors including IL-1β, TNF-α, IL-6, CCL2, and iNOS (100).”
BackgroundVEGFR1 signaling in retinal angiogenesis and microinflammation
Uemura, A., Fruttiger, M., D'Amore, P. A., Falco, S. D., Joussen, A. M., Sennlaub, F., Brunck, L. R., Johnson, K. T. M., Lambrou, G. N., Rittenhouse, K. D., et al. (2021) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2021.100954 · Cited by 356 · see citing works
“Both large classical drusen and reticular drusen are characterized by the accumulation of mononuclear phagocytes in the subretinal space (Combadiere et al., 2007; Eandi et al., 2016; Greferath et al., 2016; Guillonneau et al., 2017; Levy et al., 2015a; Sennlaub et al., 2013).”
BackgroundSelf-citationMettu, P. S., Allingham, M. J., & Cousins, S. W. (2021) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2020.100906 · Cited by 370 · see citing works
Microglia in the Retina: Roles in Development, Maturity, and Disease
Silverman, S. M., & Wong, W. T. (2018) · Annual Review of Vision Science · doi:10.1146/annurev-vision-091517-034425 · Cited by 351 · see citing works
Hata, M., Andriessen, E. M. M. A., Hata, M., Diaz-Marin, R., Fournier, F., Crespo‐Garcia, S., Blot, G., Juneau, R., Pilon, F., Dejda, A., et al. (2023) · Science · doi:10.1126/science.abj8894 · Cited by 192 · see citing works
Self-citationJoyal, J., Gantner, M. L., & Smith, L. E. H. (2017) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2017.11.002 · Cited by 186 · see citing works
Age-related macular degeneration: A two-level model hypothesis
Rozing, M. P., Durhuus, J. A., Nielsen, M. K., Subhi, Y., Kirkwood, T. B. L., Westendorp, R. G., & Sørensen, T. L. (2019) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2019.100825 · Cited by 183 · see citing works
Microglia versus Monocytes: Distinct Roles in Degenerative Diseases of the Retina
Chen, Y., Roubeix, C., Sennlaub, F., & Saban, D. R. (2020) · Trends in Neurosciences · doi:10.1016/j.tins.2020.03.012 · Cited by 165 · see citing works
“Advanced or ‘late’ debilitating AMD is characterized by central choroidal neovascularization (wet or ‘exudative’ AMD, late form) and ultimately a disciform scar (wet AMD end stage), or by a central, centrifugally extending lesion of the photoreceptors, RPE, and choroid that often starts parafoveally (geographic atroph…”
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 · see citing works
Self-citationLee, K. S., Lin, S., Copland, D. A., Dick, A. D., & Liu, J. (2021) · Journal of Neuroinflammation · doi:10.1186/s12974-021-02088-0 · Cited by 150 · see citing works
Reticular pseudodrusen: A critical phenotype in age-related macular degeneration
Wu, Z., Fletcher, E. L., Kumar, H., Greferath, U., & Guymer, R. H. (2021) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2021.101017 · Cited by 146 · see citing works
Schnichels, S., Paquet‐Durand, F., Löscher, M., Tsai, T., Hurst, J., Joachim, S. C., & Klettner, A. (2020) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2020.100880 · Cited by 144 · see citing works
Gagliardi, G., M’Barek, K. B., & Goureau, O. (2019) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2019.03.001 · Cited by 139 · see citing works
Modulation of three key innate immune pathways for the most common retinal degenerative diseases
Akhtar‐Schäfer, I., Wang, L., Krohne, T. U., Xu, H., & Langmann, T. (2018) · EMBO Molecular Medicine · doi:10.15252/emmm.201708259 · Cited by 127 · see citing works
“Furthermore, microglia over-express the anaphylatoxin receptors C5aR and C3aR, while complement inhibitors such as CFH and CFI are downregulated (Zipfel & Skerka, 2009; Guillonneau et al, 2017; Madeira et al, 2018).”
Retinal microglia: Functions and diseases
Fan, W., Huang, W., Chen, J., Li, N., Mao, L., & Hou, S. (2022) · Immunology · doi:10.1111/imm.13479 · Cited by 131 · see citing works
“In GA eyes, microglial infiltration was observed in the outer retinal atrophic lesions [124].”
BackgroundInnate Immune Response in Retinal Homeostasis and Inflammatory Disorders
Murakami, Y., Ishikawa, K., Nakao, S., & Sonoda, K.-H. (2020) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2019.100778 · Cited by 125 · see citing works
McMenamin, P. G., Saban, D. R., & Dando, S. J. (2019) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2018.12.002 · Cited by 115 · see citing works
“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.”
BackgroundWong, J. H. C., Jessica, Y. W., Jobling, A. I., Brandli, A. A., Greferath, U., Fletcher, E. L., & Vessey, K. A. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.1009599 · Cited by 110 · see citing works
“Indeed, RPE dysfunction and nonresolving inflammation remain two prominent hypotheses for the pathogenesis of AMD (Xu et al., 2009; Guillonneau et al., 2017).”
BackgroundRonning, K. E., Karlen, S. J., Miller, E. B., & Burns, M. E. (2019) · Scientific Reports · doi:10.1038/s41598-019-41141-0 · Cited by 88 · see citing works
Beguier, F., Housset, M., Roubeix, C., Augustin, S., Zagar, Y., Nous, C., Mathis, T., Eandi, C., Benchaboune, M., Drame-Maigné, A., et al. (2020) · Immunity · doi:10.1016/j.immuni.2020.07.021 · Cited by 87 · see citing works
Self-citationLéveillard, T., Philp, N. J., & Sennlaub, F. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20030762 · Cited by 100 · see citing works
“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].”
BackgroundInfluentialSelf-citationGeorge, S. M., Lu, F., Rao, M., Leach, L. L., & Gross, J. M. (2021) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2021.100969 · Cited by 93 · see citing works
Glaucoma: from pathogenic mechanisms to retinal glial cell response to damage
Fernández‐Albarral, J. A., Ramirez, A. I., de Hoz, R., Matamoros, J. A., Salobrar‐García, E., Elvira‐Hurtado, L., López‐Cuenca, I., Sánchez-Puebla, L., Salazar, J. J., & Ramirez, J. M. (2024) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2024.1354569 · Cited by 99 · see citing works
Ma, W., Silverman, S. M., Zhao, L., Villasmil, R., Campos, M. M., Amaral, J., & Wong, W. T. (2019) · eLife · doi:10.7554/elife.42049 · Cited by 85 · see citing works
Pâques, M., Meimon, S. C., Rossant, F., Rosenbaum, D. H., Mrejen, S., Sennlaub, F., & Grieve, K. F. (2018) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2018.07.001 · Cited by 84 · see citing works
“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
Luu, J. C., & Palczewski, K. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1721033115 · Cited by 86 · see citing works
Karlen, S. J., Miller, E. B., Wang, X., Levine, E. S., Zawadzki, R. J., & Burns, M. E. (2018) · Journal of Neuroinflammation · doi:10.1186/s12974-018-1365-4 · Cited by 77 · see citing works
“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 81 · see citing works
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 76 · see citing works
“…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 60 · see citing works
Regeneration of the zebrafish retinal pigment epithelium after widespread genetic ablation
Hanovice, N. J., Leach, L. L., Slater, K., Gabriel, A. E., Romanovicz, D. K., Shao, E., Collery, R. F., Burton, E. A., Lathrop, K. L., Link, B. A., et al. (2019) · PLoS Genetics · doi:10.1371/journal.pgen.1007939 · Cited by 57 · see citing works
“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).”
BackgroundRedefining our vision: an updated guide to the ocular immune system
Wu, M., Fletcher, E. L., Chinnery, H. R., Downie, L. E., & Mueller, S. N. (2024) · Nature reviews. Immunology · doi:10.1038/s41577-024-01064-y · Cited by 57 · see citing works
“The enriched cluster of microglia from early-stage AMD presents activation gene signatures that include APOE , TYROBP and SPP1 (ref.”
InfluentialBalser, C., Wolf, A., Herb, M., & Langmann, T. (2019) · Journal of Neuroinflammation · doi:10.1186/s12974-019-1419-2 · Cited by 55 · see citing works
“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].”
BackgroundResultInfluentialMelanophages give rise to hyperreflective foci in AMD, a disease-progression marker
Augustin, S., Lam, M., Lavalette, S., Verschueren, A., Blond, F., Forster, V., Przegralek, L., He, Z., Lewandowski, D., Bemelmans, A., et al. (2023) · Journal of Neuroinflammation · doi:10.1186/s12974-023-02699-9 · Cited by 52 · see citing works
“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].”
BackgroundResultInfluentialSelf-citationWooff, Y., Fernando, N., Wong, J. H. C., Dietrich, C. A., Aggio‐Bruce, R., Chu‐Tan, J. A., Robertson, A. A. B., Doyle, S., Man, S. M., & Natoli, R. (2020) · Scientific Reports · doi:10.1038/s41598-020-58849-z · Cited by 50 · see citing works
Pleiotropic Roles of P2X7 in the Central Nervous System
Kanellopoulos, J. M., & Delarasse, C. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00401 · Cited by 48 · see citing works
Fletcher, E. L. (2020) · Ophthalmic and Physiological Optics · doi:10.1111/opo.12671 · Cited by 48 · see citing works
“It is generally viewed that the accumulation of mononuclear phagocytes within the normally immune privileged subretinal space with age leads to deleterious inflammatory changes in the posterior eye affecting the integrity of RPE and photoreceptors.(9) Understanding how mononuclear phagocytes contribute to the differen…”
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 · see citing works
“It has also been shown that MAC recruits and activates leukocytes by coordinating inflammasome activation and endothelial cytokine signalling [196–200], which may initially preserve tissue function by rapidly suppressing danger; however, sustained production of reactive oxygen species, proteases, and inflammatory cyto…”
BackgroundPameijer, E. M., Heus, P., Damen, J. A., Spijker, R., Hooft, L., Ringens, P. J., Imhof, S. M., & van Leeuwen, R. (2022) · Acta Ophthalmologica · doi:10.1111/aos.15191 · Cited by 41 · see citing works
“Immunological factors, such as complement and oxidative stress, are important in the pathogenesis of AMD (Guillonneau et al. 2017).”
BackgroundClinical-grade production and safe delivery of human ESC derived RPE sheets in primates and rodents
M’Barek, K. B., Bertin, S., Brazhnikova, E., Jaillard, C., Habeler, W., Plancheron, A., Fovet, C.-M., Demilly, J., Jarraya, M., Bejanariu, A., et al. (2019) · Biomaterials · doi:10.1016/j.biomaterials.2019.119603 · Cited by 40 · see citing works
“AMD is a complex disease caused by the combination of genetic and environmental factors (7-10).”
BackgroundSelf-citationTouhami, S., Béguier, F., Augustin, S., Charles‐Messance, H., Vignaud, L., Nandrot, E. F., Reichman, S., Forster, V., Mathis, T., Sahel, J., et al. (2018) · Journal of Neuroinflammation · doi:10.1186/s12974-018-1106-8 · Cited by 39 · see citing works
“AMD is also associated with dysfunctional RPE: the visual cycle is slowed, evidenced by an increase of recovery time after bleach [6, 7]; the outer blood-retinal barrier is breached, illustrated by subretinal neovascularization, edema, and macrophages (Mφ) that accumulate subretinally around the RPE [2].”
InfluentialSelf-citationComplement inhibitors for age-related macular degeneration
Tzoumas, N., Riding, G., Williams, M. A., & Steel, D. H. (2023) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd009300.pub3 · Cited by 38 · see citing works
Age-Related Macular Degeneration: Cellular and Molecular Signaling Mechanisms
Jiang, F., Ma, J., Lei, C., Zhang, Y., & Zhang, M. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26136174 · Cited by 43 · see citing works
“Resident microglia, which are activated by drusen components and oxidative stress, adopt this inflammatory phenotype, releasing cytokines such as IL-1 β , IL-6, and TNF-α [51].”
Han, X., Chen, X., Chen, S., Luo, Q., Liu, X., He, A., He, S., Qiu, J., Chen, P., Wu, Y., et al. (2020) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2020.110273 · Cited by 38 · see citing works
Beaudry‐Richard, A., Nadeau‐Vallée, M., Prairie, É., Maurice, N., Heckel, É., Nezhady, M. A. M., Pundir, S., Madaan, A., Boudreault, A., Hou, X., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-30087-4 · Cited by 37 · see citing works
Hata, M., Hata, M., Andriessen, E. M. M. A., Juneau, R., Pilon, F., Crespo‐Garcia, S., Diaz-Marin, R., Guber, V., Binet, F., Fournier, F., et al. (2023) · Journal of Clinical Investigation · doi:10.1172/jci159757 · Cited by 34 · see citing works
“As a consequence, the reactivity of accumulating phagocytes is a driving force in photoreceptor demise and in disease manifestation (20), high-lighting the importance of the innate immune system as a major driver of AMD pathophysiology (16).”
Self-citationZhou, L., Xu, Z., Lu, H., Cho, H., Xie, Y., Lee, G., Ri, K., & Duh, E. J. (2024) · Journal of Neuroinflammation · doi:10.1186/s12974-024-03190-9 · Cited by 34 · see citing works
“CCL2 is known to be an important chemokine for macrophage recruitment into the retina during inflammation [51, 52].”
BackgroundDabouz, R., Cheng, C. W. H., Abram, P., Omri, S., Cagnone, G., Sawmy, K. V., Joyal, J., Desjarlais, M., Olson, D. M., Weil, A. G., et al. (2020) · Journal of Neuroinflammation · doi:10.1186/s12974-020-02032-8 · Cited by 34 · see citing works
Tzoumas, N., Hallam, D., Harris, C. L., Lako, M., Kavanagh, D., & Steel, D. H. W. (2021) · Survey of Ophthalmology · doi:10.1016/j.survophthal.2020.10.008 · Cited by 33 · see citing works
Targeting P2X7 receptors as a means for treating retinal disease
Fletcher, E. L., Wang, A. Y., Jobling, A. I., Rutar, M., Greferath, U., Gu, B. J., & Vessey, K. A. (2019) · Drug Discovery Today · doi:10.1016/j.drudis.2019.03.029 · Cited by 32 · see citing works
Demirs, J. T., Yang, J., Crowley, M. A., Twarog, M., Delgado, O., Qiu, Y., Poor, S. H., Rice, D. S., Dryja, T. P., Anderson, K., et al. (2021) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.62.7.26 · Cited by 32 · see citing works
Brandli, A. A., Vessey, K. A., & Fletcher, E. L. (2024) · Journal of Neuroinflammation · doi:10.1186/s12974-024-03055-1 · Cited by 31 · see citing works
“Impor-tantly, innate immune cells within AMD lesions, including mononuclear phagocytes and neutrophils, all express high levels of PRRs [23–31].”
BackgroundPool, F. M., Kiel, C., Serrano, L. G., & Luthert, P. J. (2020) · npj Aging and Mechanisms of Disease · doi:10.1038/s41514-019-0039-5 · Cited by 31 · see citing works
Buonfiglio, F., Korb, C. A., Stoffelns, B. M., Pfeiffer, N., & Gericke, A. (2024) · Aging and Disease · doi:10.14336/ad.2024.0124 · Cited by 31 · see citing works
“Supporting this association, serum and aqueous humor of AMD patients contain a myriad of proinflammatory cytokines, including TNF-α, IL-1β, IL-17, IL-6, and IL-8 [278, 279].”
Subhi, Y., Nielsen, M. K., Molbech, C. R., Liisborg, C., Søndergaard, H. B., Sellebjerg, F. T., & Sørensen, T. L. (2019) · Immunity & Ageing · doi:10.1186/s12979-019-0160-0 · Cited by 30 · see citing works
A role for mast cells in geographic atrophy
Ogura, S., Baldeosingh, R., Bhutto, I. A., Kambhampati, S. P., McLeod, D. S., Edwards, M. M., Rais, R., Schubert, W., & Lutty, G. A. (2020) · The FASEB Journal · doi:10.1096/fj.202000807r · Cited by 30 · see citing works
Khan, A. H., Chowers, I., & Lotery, A. J. (2023) · Cells · doi:10.3390/cells12131708 · Cited by 31 · see citing works
“• Retinal microglia SASP markers: IL-1α, IL1-β, IL-6, IL-8, IL-12, TNF-α, C3, CFB, CXCL1, TGF-β and nitric oxide [43,65].”
BackgroundInfluentialNielsen, M. K., Subhi, Y., Molbech, C. R., Falk, M. K., Nissen, M. H., & Sørensen, T. L. (2020) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.61.4.28 · Cited by 29 · see citing works
Wang, J.-H., Kumar, S., & Liu, G. (2021) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.62.14.22 · Cited by 28 · see citing works
“7,8 Moreover, elevated levels of inflammatory cytokines, such as TNF-α , IL-8, CCL2, IL-1 β , and IL-6, have been found in the vitreous fluid of patients with PDR, 9–11 suggesting increased activity of phagocytes and macrophages.”
Innate Immunity in Age-Related Macular Degeneration
Zhang, Y., & Wong, W. T. (2021) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-66014-7_5 · Cited by 27 · see citing works
Kinins and Their Receptors as Potential Therapeutic Targets in Retinal Pathologies
Othman, R., Cagnone, G., Joyal, J., Vaucher, E., & Couture, R. (2021) · Cells · doi:10.3390/cells10081913 · Cited by 45 · see citing works
Ramírez‐Pardo, I., Villarejo‐Zori, B., Jiménez‐Loygorri, J. I., Sierra‐Filardi, E., Alonso‐Gil, S., Mariño, G., de la Villa, P., Fitze, P. S., Fuentes, J. M., García‐Escudero, R., et al. (2022) · Autophagy · doi:10.1080/15548627.2022.2103307 · Cited by 27 · see citing works
“Our analysis of a publicly available RNA-seq dataset of retinal and RPE tissues from control and AMD patients revealed that genes of the autophagy initiation machinery, including AMBRA1, were markedly upregulated in the macular region of the RPE compared with the peripheral retinal region.”
BackgroundInfluentialSubhi, Y., Nielsen, M. K., Molbech, C. R., Falk, M. K., Singh, A., Hviid, T. V. F., Nissen, M. H., & Sørensen, T. L. (2019) · JAMA Ophthalmology · doi:10.1001/jamaophthalmol.2019.0010 · Cited by 26 · see citing works
Reumueller, A., Schmidt-Erfurth, U. M., Salas, M., Sacu, S., Drexler, W., Pircher, M., & Pollreisz, A. (2019) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.18-25702 · Cited by 26 · see citing works
Immunometabolic modulation of retinal inflammation by CD36 ligand
Mellal, K., Omri, S., Mulumba, M., Tahiri, H., Fortin, C. F., Dorion, M., Pham, H., García‐Ramos, Y., Zhang, J., Pundir, S., et al. (2019) · Scientific Reports · doi:10.1038/s41598-019-49472-8 · Cited by 25 · see citing works
Self-citationImmunological Aspects of Age-Related Macular Degeneration
Allingham, M. J., Loksztejn, A., Cousins, S. W., & Mettu, P. S. (2021) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-66014-7_6 · Cited by 24 · see citing works
Innate immunity dysregulation in aging eye and therapeutic interventions
Das, S., Ahmad, Z., Suryawanshi, A. S., & Kumar, A. (2022) · Ageing Research Reviews · doi:10.1016/j.arr.2022.101768 · Cited by 24 · see citing works
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 24 · see citing works
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 22 · see citing works
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 · see citing works
Cho, H.-M., Jo, Y.-D., & Choung, S. (2022) · Nutrients · doi:10.3390/nu14030401 · Cited by 22 · see citing works
“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 · see citing works
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 · see citing works
“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 · see citing works
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 · see citing works
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 20 · see citing works
“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 · see citing works
“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 · see citing works
“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., Huang, X., Avula, P. K., Caruso, E., Drysdale, C., Vessey, K. A., Ou, A., Fowler, C., Liu, T.-H., Lin, Y., et al. (2021) · Frontiers in Medicine · doi:10.3389/fmed.2021.634177 · Cited by 14 · see citing works
“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 · see citing works
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 · see citing works
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Myeloid‐resident neuropilin‐1 promotes choroidal neovascularization while mitigating inflammation
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“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 18 · see citing works
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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 · see citing works
“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 · see citing works
CD36 Deficiency Inhibits Retinal Inflammation and Retinal Degeneration in Cx3cr1 Knockout Mice
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“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.-Y., Qin, H., & Yao, K. (2024) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2024.1499719 · Cited by 17 · see citing works
“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 · see citing works
“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].”
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“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 · see citing works
“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).”
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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 16 · see citing works
“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 · see citing works
Monocyte Invasion into the Retina Restricts the Regeneration of Neurons from Müller Glia
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“…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 14 · see citing works
“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 · see citing works
“Cells were passaged every 3 days until seeding into vessels for experimentation.”
Method
- 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
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › 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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