Hyalocytes-guardians of the vitreoretinal interface.
Hyalocytes
Immunology
Vitreoretinal interface
Vitreous
Journal
Graefe's archive for clinical and experimental ophthalmology = Albrecht von Graefes Archiv fur klinische und experimentelle Ophthalmologie
ISSN: 1435-702X
Titre abrégé: Graefes Arch Clin Exp Ophthalmol
Pays: Germany
ID NLM: 8205248
Informations de publication
Date de publication:
03 Apr 2024
03 Apr 2024
Historique:
received:
03
11
2023
accepted:
08
03
2024
revised:
04
03
2024
medline:
3
4
2024
pubmed:
3
4
2024
entrez:
3
4
2024
Statut:
aheadofprint
Résumé
Originally discovered in the nineteenth century, hyalocytes are the resident macrophage cell population in the vitreous body. Despite this, a comprehensive understanding of their precise function and immunological significance has only recently emerged. In this article, we summarize recent in-depth investigations deciphering the critical role of hyalocytes in various aspects of vitreous physiology, such as the molecular biology and functions of hyalocytes during development, adult homeostasis, and disease. Hyalocytes are involved in fetal vitreous development, hyaloid vasculature regression, surveillance and metabolism of the vitreoretinal interface, synthesis and breakdown of vitreous components, and maintenance of vitreous transparency. While sharing certain resemblances with other myeloid cell populations such as retinal microglia, hyalocytes possess a distinct molecular signature and exhibit a gene expression profile tailored to the specific needs of their host tissue. In addition to inflammatory eye diseases such as uveitis, hyalocytes play important roles in conditions characterized by anomalous posterior vitreous detachment (PVD) and vitreoschisis. These can be hypercellular tractional vitreo-retinopathies, such as macular pucker, proliferative vitreo-retinopathy (PVR), and proliferative diabetic vitreo-retinopathy (PDVR), as well as paucicellular disorders such as vitreo-macular traction syndrome and macular holes. Notably, hyalocytes assume a significant role in the early pathophysiology of these disorders by promoting cell migration and proliferation, as well as subsequent membrane contraction, and vitreoretinal traction. Thus, early intervention targeting hyalocytes could potentially mitigate disease progression and prevent the development of proliferative vitreoretinal disorders altogether, by eliminating the involvement of vitreous and hyalocytes.
Identifiants
pubmed: 38568222
doi: 10.1007/s00417-024-06448-3
pii: 10.1007/s00417-024-06448-3
doi:
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024. The Author(s).
Références
Hannover A (1840) Cited in: Hamburg (1959): Some investigations on the cells of the vitreous body. Ophthalmologica 138:81–107
Virchow R (1852) Archiv für pathologische Anatomie und Physiologie und für klinische Medizin. Springer
Potiechin A (1878) Ueber die Zellen des Glaskörpers. Archiv f pathol Anat 72:157–165. https://doi.org/10.1007/BF01878762
doi: 10.1007/BF01878762
Schwalbe G (1874) Mikroskopische Anatomie des Sehnerven, der Netzhaut und des Glaskörpers. Handbuch der Allgemeinen Augenheilkunde
Lopéz Enríquez M, Costero I (1931) Sobre los carateres de la microglia retinania emigrada al humor vítreo. Bol Soc Espan Hist Nat 425–431
Szirmai JA, Balazs EA (1958) Studies on the structure of the vitreous body: III. Cells in the cortical layer. AMA Arch Ophthalmol 59:34–48
doi: 10.1001/archopht.1958.00940020058006
pubmed: 13486991
Sebag J, Niemeyer M, Koss MJ (2014) Anomalous posterior vitreous detachment and vitreoschisis. In: Sebag J (ed) Vitreous – in Health and Disease. Springer, New York. https://doi.org/10.1007/978-1-4939-1086-1_14
doi: 10.1007/978-1-4939-1086-1_14
Migacz JV, Otero-Marquez O, Zhou R et al (2022) Imaging of vitreous cortex hyalocyte dynamics using non-confocal quadrant-detection adaptive optics scanning light ophthalmoscopy in human subjects. Biomed Opt Express 13:1755–1773. https://doi.org/10.1364/BOE.449417
doi: 10.1364/BOE.449417
pubmed: 35414987
pmcid: 8973177
Wieghofer P, Engelbert M, Chui TY et al (2022) Hyalocyte origin, structure, and imaging. Expert Rev Ophthalmol 17(4):233–248. https://doi.org/10.1080/17469899.2022.2100762
doi: 10.1080/17469899.2022.2100762
pubmed: 36632192
pmcid: 9831111
Boneva SK, Wolf J, Rosmus D-D et al (2020) Transcriptional profiling uncovers human hyalocytes as a unique innate immune cell population. Front Immunol 11:567274. https://doi.org/10.3389/fimmu.2020.567274
doi: 10.3389/fimmu.2020.567274
pubmed: 33042148
pmcid: 7517040
Schlecht A, Boneva S, Salie H et al (2021) Imaging mass cytometry for high-dimensional tissue profiling in the eye. BMC Ophthalmol 21:338. https://doi.org/10.1186/s12886-021-02099-8
doi: 10.1186/s12886-021-02099-8
pubmed: 34544377
pmcid: 8454101
Laich Y, Wolf J, Hajdu RI et al (2022) Single-cell protein and transcriptional characterization of epiretinal membranes from patients with proliferative vitreoretinopathy. Invest Ophthalmol Vis Sci 63:17. https://doi.org/10.1167/iovs.63.5.17
doi: 10.1167/iovs.63.5.17
pubmed: 35579905
pmcid: 9123517
Jones CH, Gui W, Schumann RG et al (2022) Hyalocytes in proliferative vitreo-retinal diseases. Expert Rev Ophthalmol 17:263–280. https://doi.org/10.1080/17469899.2022.2100764
doi: 10.1080/17469899.2022.2100764
pubmed: 36466118
pmcid: 9718005
Boneva SK, Wolf J, Wieghofer P et al (2022) Hyalocyte functions and immunology. Expert Rev Ophthalmol 17(4):249–262. https://doi.org/10.1080/17469899.2022.2100763
doi: 10.1080/17469899.2022.2100763
Kingston Z, Provis J, Madigan MC (2004) Development and developmental disorders of vitreous. In: Sebag J (ed) Vitreous - Health Disease. Springer, New York, pp 95–112
Zhu M, Provis JM, Penfold PL (1999) The human hyaloid system: cellular phenotypes and inter-relationships. Exp Eye Res 68:553–563. https://doi.org/10.1006/exer.1998.0632
doi: 10.1006/exer.1998.0632
pubmed: 10328969
Diez-Roux G, Lang RA (1997) Macrophages induce apoptosis in normal cells in vivo. Development 124:3633–3638. https://doi.org/10.1242/dev.124.18.3633
doi: 10.1242/dev.124.18.3633
pubmed: 9342055
Lang RA, Bishop JM (1993) Macrophages are required for cell death and tissue remodeling in the developing mouse eye. Cell 74:453–462. https://doi.org/10.1016/0092-8674(93)80047-i
doi: 10.1016/0092-8674(93)80047-i
pubmed: 8348612
Lobov IB, Rao S, Carroll TJ et al (2005) WNT7b mediates macrophage-induced programmed cell death in patterning of the vasculature. Nature 437:417–421. https://doi.org/10.1038/nature03928
doi: 10.1038/nature03928
pubmed: 16163358
pmcid: 4259146
Dumas AA, Borst K, Prinz M (2021) Current tools to interrogate microglial biology. Neuron 109:2805–2819. https://doi.org/10.1016/j.neuron.2021.07.004
doi: 10.1016/j.neuron.2021.07.004
pubmed: 34390649
Wieghofer P, Knobeloch K-P, Prinz M (2015) Genetic targeting of microglia. Glia 63:1–22. https://doi.org/10.1002/glia.22727
doi: 10.1002/glia.22727
pubmed: 25132502
Gloor BP (1969) Cellular proliferation on the vitreous surface after photocoagulation. Albrecht Von Graefes Arch Klin Exp Ophthalmol 178:99–113. https://doi.org/10.1007/BF00414375
doi: 10.1007/BF00414375
pubmed: 4186406
Haddad A, André JC (1998) Hyalocyte-like cells are more numerous in the posterior chamber than they are in the vitreous of the rabbit eye. Exp Eye Res 66:709–718. https://doi.org/10.1006/exer.1997.0476
doi: 10.1006/exer.1997.0476
pubmed: 9657903
Qiao H, Hisatomi T, Sonoda K-H et al (2005) The characterisation of hyalocytes: the origin, phenotype, and turnover. Br J Ophthalmol 89:513–517. https://doi.org/10.1136/bjo.2004.050658
doi: 10.1136/bjo.2004.050658
pubmed: 15774935
pmcid: 1772586
Wieghofer P, Hagemeyer N, Sankowski R et al (2021) Mapping the origin and fate of myeloid cells in distinct compartments of the eye by single-cell profiling. EMBO J n/a:e105123. https://doi.org/10.15252/embj.2020105123
doi: 10.15252/embj.2020105123
Wolf J, Boneva S, Rosmus D-D et al (2022) Deciphering the molecular signature of human hyalocytes in relation to other innate immune cell populations. Invest Ophthalmol Vis Sci 63:9. https://doi.org/10.1167/iovs.63.3.9
doi: 10.1167/iovs.63.3.9
pubmed: 35266958
pmcid: 8934546
Sebag J (1989) Functions of the vitreous. In: Sebag J (ed) The vitreous: structure, function, and pathobiology. Springer, New York, NY, pp 59–71
doi: 10.1007/978-1-4613-8908-8_5
Ogawa K (2002) Scanning electron microscopic study of hyalocytes in the guinea pig eye. Arch Histol Cytol 65:263–268. https://doi.org/10.1679/aohc.65.263
doi: 10.1679/aohc.65.263
pubmed: 12389665
Xu Q, Wang Y, Dabdoub A et al (2004) Vascular development in the retina and inner ear: control by Norrin and Frizzled-4, a high-affinity ligand-receptor pair. Cell 116:883–895. https://doi.org/10.1016/s0092-8674(04)00216-8
doi: 10.1016/s0092-8674(04)00216-8
pubmed: 15035989
Lange CA, Luhmann UF, Mowat FM et al (2012) Von Hippel-Lindau protein in the RPE is essential for normal ocular growth and vascular development. Development. https://doi.org/10.1242/dev.070813
doi: 10.1242/dev.070813
pubmed: 22627278
pmcid: 3367444
Lutty GA, Merges C, Threlkeld AB et al (1993) Heterogeneity in localization of isoforms of TGF-beta in human retina, vitreous, and choroid. Invest Ophthalmol Vis Sci 34:477–487
pubmed: 7680639
Sukhikh GT, Panova IG, Smirnova YA et al (2010) Expression of transforming growth factor-β2in vitreous body and adjacent tissues during prenatal development of human eye. Bull Exp Biol Med 150:117–121. https://doi.org/10.1007/s10517-010-1084-z
doi: 10.1007/s10517-010-1084-z
pubmed: 21161068
Bishop P (1996) The biochemical structure of mammalian vitreous. Eye 10:664–670. https://doi.org/10.1038/eye.1996.159
doi: 10.1038/eye.1996.159
pubmed: 9091361
Sebag J (2010) Vitreous anatomy, aging, and anomalous posterior vitreous detachment encyclopedia of the eye. Elsevier, pp 307–315
Cain SA, Morgan A, Sherratt MJ et al (2006) Proteomic analysis of fibrillin-rich microfibrils. Proteomics 6:111–122. https://doi.org/10.1002/pmic.200401340
doi: 10.1002/pmic.200401340
pubmed: 16302274
Kamei A, Totani A (1982) Isolation and characterization of minor glycosaminoglycans in the rabbit vitreous body. Biochem Biophys Res Commun 109:881–887. https://doi.org/10.1016/0006-291x(82)92022-8
doi: 10.1016/0006-291x(82)92022-8
pubmed: 6818969
Miyamoto T, Inoue H, Sakamoto Y et al (2005) Identification of a novel splice site mutation of the CSPG2 gene in a Japanese family with Wagner syndrome. Invest Ophthalmol Vis Sci 46:2726–2735. https://doi.org/10.1167/iovs.05-0057
doi: 10.1167/iovs.05-0057
pubmed: 16043844
Iwanoff A (1865) Beiträge zur normalen und pathologischen Anatomie des Auges. Archiv für Opthalmologie 11:135–170. https://doi.org/10.1007/BF02720906
doi: 10.1007/BF02720906
Castanos MV, Zhou DB, Linderman RE et al (2020) Imaging of macrophage-like cells in living human retina using clinical OCT. Invest Ophthalmol Vis Sci 61:48. https://doi.org/10.1167/iovs.61.6.48
doi: 10.1167/iovs.61.6.48
pubmed: 32574351
pmcid: 7416910
Madry C, Kyrargyri V, Arancibia-Cárcamo IL et al (2018) Microglial ramification, surveillance, and interleukin-1β release are regulated by the two-pore domain K+ channel THIK-1. Neuron 97:299-312.e6. https://doi.org/10.1016/j.neuron.2017.12.002
doi: 10.1016/j.neuron.2017.12.002
pubmed: 29290552
pmcid: 5783715
Nimmerjahn A, Kirchhoff F, Helmchen F (2005) Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308:1314–1318. https://doi.org/10.1126/science.1110647
doi: 10.1126/science.1110647
pubmed: 15831717
Schlecht A, Wolf J, Boneva S et al (2022) Transcriptional and distributional profiling of microglia in retinal angiomatous proliferation. Int J Mol Sci 23:3443. https://doi.org/10.3390/ijms23073443
doi: 10.3390/ijms23073443
pubmed: 35408803
pmcid: 8998238
Haynes SE, Hollopeter G, Yang G et al (2006) The P2Y12 receptor regulates microglial activation by extracellular nucleotides. Nat Neurosci 9:1512–1519. https://doi.org/10.1038/nn1805
doi: 10.1038/nn1805
pubmed: 17115040
Ong JX, Nesper PL, Fawzi AA et al (2021) Characterization of macrophage-like cells in diabetic retinopathy using optical coherence tomography angiography. Invest Ophthalmol Vis Sci 62:1109
doi: 10.1167/iovs.62.10.2
Hamburg A (1959) Some investigations on the cells of the vitreous body. OPH 138:81–107. https://doi.org/10.1159/000303618
doi: 10.1159/000303618
Grabner G, Boltz G, Förster O (1980) Macrophage-like properaties of human hyalocytes. Invest Ophthalmol Vis Sci 19:333–340
pubmed: 7358486
Teng CC (1969) An electron microscopic study of cells in the vitreous of the rabbit eye. I. The macrophage. Eye Ear Nose Throat Mon 48:46–55
pubmed: 5763988
Gupta P, Yee KMP, Garcia P et al (2011) Vitreoschisis in macular diseases. Br J Ophthalmol 95:376–380. https://doi.org/10.1136/bjo.2009.175109
doi: 10.1136/bjo.2009.175109
pubmed: 20584710
Schetters STT, Gomez-Nicola D, Garcia-Vallejo JJ, Van Kooyk Y (2018) Neuroinflammation: microglia and T cells get ready to tango. Front Immunol 8:1905. https://doi.org/10.3389/fimmu.2017.01905
doi: 10.3389/fimmu.2017.01905
pubmed: 29422891
pmcid: 5788906
Medawar PB (1948) Immunity to homologous grafted skin; the fate of skin homografts transplanted to the brain, to subcutaneous tissue, and to the anterior chamber of the eye. Br J Exp Pathol 29:58–69
pubmed: 18865105
pmcid: 2073079
Streilein JW, Niederkorn JY (1981) Induction of anterior chamber-associated immune deviation requires an intact, functional spleen. J Exp Med 153:1058–1067. https://doi.org/10.1084/jem.153.5.1058
doi: 10.1084/jem.153.5.1058
pubmed: 6788883
Sonoda K-H, Sakamoto T, Qiao H et al (2005) The analysis of systemic tolerance elicited by antigen inoculation into the vitreous cavity: vitreous cavity-associated immune deviation. Immunology 116:390–399. https://doi.org/10.1111/j.1365-2567.2005.02239.x
doi: 10.1111/j.1365-2567.2005.02239.x
pubmed: 16236129
pmcid: 1802422
Streilein JW, Okamoto S, Hara Y et al (1997) Blood-borne signals that induce anterior chamber-associated immune deviation after intracameral injection of antigen. Invest Ophthalmol Vis Sci 38:2245–2254
pubmed: 9344347
Kohno R-i, Hata Y, Kawahara S et al (2009) Possible contribution of hyalocytes to idiopathic epiretinal membrane formation and its contraction. Br J Ophthalmol 93:1020–1026. https://doi.org/10.1136/bjo.2008.155069
doi: 10.1136/bjo.2008.155069
pubmed: 19429593
Laich Y, Wolf J, Hajdú RI et al (2022) Single-cell protein and transcriptional characterization of epiretinal membranes from patients with proliferative vitreoretinopathy. Invest Ophthalmol Vis Sci 63:17. https://doi.org/10.1167/iovs.63.5.17
doi: 10.1167/iovs.63.5.17
pubmed: 35579905
pmcid: 9123517
Rashid K, Akhtar-Schaefer I, Langmann T (2019) Microglia in retinal degeneration. Front Immunol 10:1975. https://doi.org/10.3389/fimmu.2019.01975
doi: 10.3389/fimmu.2019.01975
pubmed: 31481963
pmcid: 6710350
Zhao L, Zabel MK, Wang X et al (2015) Microglial phagocytosis of living photoreceptors contributes to inherited retinal degeneration. EMBO Mol Med 7:1179–1197. https://doi.org/10.15252/emmm.201505298
doi: 10.15252/emmm.201505298
pubmed: 26139610
pmcid: 4568951
Boeck M, Thien A, Wolf J et al (2020) Temporospatial distribution and transcriptional profile of retinal microglia in the oxygen-induced retinopathy mouse model. Glia. https://doi.org/10.1002/glia.23810
doi: 10.1002/glia.23810
pubmed: 32150307
Fischer F, Martin G, Agostini HT (2011) Activation of retinal microglia rather than microglial cell density correlates with retinal neovascularization in the mouse model of oxygen-induced retinopathy. J Neuroinflammation 8:120. https://doi.org/10.1186/1742-2094-8-120
doi: 10.1186/1742-2094-8-120
pubmed: 21943408
pmcid: 3190350
Sebag J (2020) Vitreous and vision degrading myodesopsia. Prog Retin Eye Res 79:100847. https://doi.org/10.1016/j.preteyeres.2020.100847
doi: 10.1016/j.preteyeres.2020.100847
pubmed: 32151758
Romeike A, Brügmann M, Drommer W (1998) Immunohistochemical studies in equine recurrent uveitis (ERU). Vet Pathol 35:515–526. https://doi.org/10.1177/030098589803500606
doi: 10.1177/030098589803500606
pubmed: 9823593
Vagaja NN, Chinnery HR, Binz N et al (2012) Changes in murine hyalocytes are valuable early indicators of ocular disease. Invest Ophthalmol Vis Sci 53:1445. https://doi.org/10.1167/iovs.11-8601
doi: 10.1167/iovs.11-8601
pubmed: 22297487
Joseph A, Chu CJ, Feng G et al (2020) Label-free imaging of immune cell dynamics in the living retina using adaptive optics. eLife 9:e60547. https://doi.org/10.7554/eLife.60547
doi: 10.7554/eLife.60547
pubmed: 33052099
pmcid: 7556865
Hata Y, Nakao S, Kohno R-i et al (2011) Role of tumour necrosis factor-α (TNF-α) in the functional properties of hyalocytes. Br J Ophthalmol 95:261–265. https://doi.org/10.1136/bjo.2010.190322
doi: 10.1136/bjo.2010.190322
pubmed: 21030411
Pfahler SM, Brandford AN, Glaser BM (2009) A prospective study of in-office diagnostic vitreous sampling in patients with vitreoretinal pathology. Retina 29:1032–1035. https://doi.org/10.1097/IAE.0b013e3181a2c1eb
doi: 10.1097/IAE.0b013e3181a2c1eb
pubmed: 19373124
Hickman S, Izzy S, Sen P et al (2018) Microglia in neurodegeneration. Nat Neurosci 21:1359–1369. https://doi.org/10.1038/s41593-018-0242-x
doi: 10.1038/s41593-018-0242-x
pubmed: 30258234
pmcid: 6817969
Tenbrock L, Wolf J, Boneva S et al (2021) Subretinal fibrosis in neovascular age-related macular degeneration: current concepts, therapeutic avenues, and future perspectives. Cell Tissue Res. https://doi.org/10.1007/s00441-021-03514-8
doi: 10.1007/s00441-021-03514-8
pubmed: 34477966
pmcid: 8975778
Jun Lee S, Lee CS, Jun Koh H (2009) Posterior vitreomacular adhesion and risk of exudative age-related macular degeneration: paired eye study. Am J Ophthalmol 147:621-626.e1. https://doi.org/10.1016/j.ajo.2008.10.003
doi: 10.1016/j.ajo.2008.10.003
Krebs I, Brannath W, Glittenberg C et al (2007) Posterior vitreomacular adhesion: a potential risk factor for exudative age-related macular degeneration? Am J Ophthalmol 144:741–746. https://doi.org/10.1016/j.ajo.2007.07.024
doi: 10.1016/j.ajo.2007.07.024
pubmed: 17884003
Robison CD, Krebs I, Binder S et al (2009) Vitreomacular adhesion in active and end-stage age-related macular degeneration. Am J Ophthalmol 148:79-82.e2. https://doi.org/10.1016/j.ajo.2009.01.014
doi: 10.1016/j.ajo.2009.01.014
pubmed: 19327744
Roller AB, Mahajan VB, Boldt HC et al (2010) Effects of vitrectomy on age-related macular degeneration. Ophthalmology 117:1381–1386. https://doi.org/10.1016/j.ophtha.2009.11.007
doi: 10.1016/j.ophtha.2009.11.007
pubmed: 20176401
Sebag J (2015) Vitreous in age-related macular degeneration therapy—the medium is the message. Retina 35:1715–1718. https://doi.org/10.1097/IAE.0000000000000718
doi: 10.1097/IAE.0000000000000718
pubmed: 26312447
D’Ambrosi N, Apolloni S (2020) Fibrotic scar in neurodegenerative diseases. Front Immunol 11:1394. https://doi.org/10.3389/fimmu.2020.01394
doi: 10.3389/fimmu.2020.01394
pubmed: 32922384
pmcid: 7456854
Schlecht A, Zhang P, Wolf J et al (2021) Secreted phosphoprotein 1 expression in retinal mononuclear phagocytes links murine to human choroidal neovascularization. Front Cell Dev Biol 8:618598. https://doi.org/10.3389/fcell.2020.618598
doi: 10.3389/fcell.2020.618598
pubmed: 33585455
pmcid: 7876283
Sebag J (1997) Classifying posterior vitreous detachment: A new way to look at the invisible. Br J Ophthalmol 81:521. https://doi.org/10.1136/bjo.81.7.521
Sebag J (2004) Anomalous posterior vitreous detachment: a unifying concept in vitreo-retinal disease. Graefe’s Arch Clin Exp Ophthalmol 242:690–698. https://doi.org/10.1007/s00417-004-0980-1
doi: 10.1007/s00417-004-0980-1
Gupta P, Sadun AA, Sebag J (2008) Multifocal retinal contraction in macular pucker analyzed by combined optical coherence tomography/scanning laser ophthalmoscopy. Retina 28:447–452. https://doi.org/10.1097/IAE.0b013e318160a754
doi: 10.1097/IAE.0b013e318160a754
pubmed: 18327137
Sebag J (2008) Vitreoschisis. Graefes Arch Clin Exp Ophthalmol 246:329–332. https://doi.org/10.1007/s00417-007-0743-x
doi: 10.1007/s00417-007-0743-x
pubmed: 18228032
pmcid: 2258312
van Overdam KA, van Etten PG, Accou GPBM et al (2024) Prevalence of vitreoschisis-induced vitreous cortex remnants over the peripheral retinal surface in eyes undergoing vitrectomy for primary rhegmatogenous retinal detachment. Acta Ophthalmol 102:99–106. https://doi.org/10.1111/aos.15687
doi: 10.1111/aos.15687
pubmed: 37133363
Schumann RG, Hagenau F, Guenther SR et al (2019) Premacular cell proliferation profiles in tangential traction vitreo-maculopathies suggest a key role for hyalocytes. Ophthalmologica 242:106–112. https://doi.org/10.1159/000495853
doi: 10.1159/000495853
pubmed: 30947188
Foos RY (1977) Vitreoretinal juncture; epiretinal membranes and vitreous. Invest Ophthalmol Vis Sci 16:416–422
pubmed: 852943
Appiah AP, Hirose T, Kado M (1988) A review of 324 cases of idiopathic premacular gliosis. Am J Ophthalmol 106:533–535. https://doi.org/10.1016/0002-9394(88)90581-8
doi: 10.1016/0002-9394(88)90581-8
pubmed: 3189467
Sidd RJ, Fine SL, Owens SL, Patz A (1982) Idiopathic preretinal gliosis. Am J Ophthalmol 94:44–48. https://doi.org/10.1016/0002-9394(82)90189-1
doi: 10.1016/0002-9394(82)90189-1
pubmed: 7091281
Foos RY, Wheeler NC (1982) Vitreoretinal juncture. Synchysis senilis and posterior vitreous detachment. Ophthalmology 89:1502–1512. https://doi.org/10.1016/s0161-6420(82)34610-2
doi: 10.1016/s0161-6420(82)34610-2
pubmed: 7162795
Snead DRJ, James S, Snead MP (2008) Pathological changes in the vitreoretinal junction 1: epiretinal membrane formation. Eye (Lond) 22:1310–1317. https://doi.org/10.1038/eye.2008.36
doi: 10.1038/eye.2008.36
pubmed: 18344963
Yamashita T, Uemura A, Sakamoto T (2008) Intraoperative characteristics of the posterior vitreous cortex in patients with epiretinal membrane. Graefes Arch Clin Exp Ophthalmol 246:333–337. https://doi.org/10.1007/s00417-007-0745-8
doi: 10.1007/s00417-007-0745-8
pubmed: 18193261
Vogt D, Vielmuth F, Wertheimer C et al (2018) Premacular membranes in tissue culture. Graefes Arch Clin Exp Ophthalmol 256:1589–1597. https://doi.org/10.1007/s00417-018-4033-6
doi: 10.1007/s00417-018-4033-6
pubmed: 29931427
Compera D, Entchev E, Haritoglou C et al (2015) Lamellar hole-associated epiretinal proliferation in comparison to epiretinal membranes of macular pseudoholes. Am J Ophthalmol 160:373-384.e1. https://doi.org/10.1016/j.ajo.2015.05.010
doi: 10.1016/j.ajo.2015.05.010
pubmed: 25982970
Pang CE, Spaide RF, Freund KB (2014) Epiretinal proliferation seen in association with lamellar macular holes: a distinct clinical entity. Retina 34:1513–1523. https://doi.org/10.1097/IAE.0000000000000163
doi: 10.1097/IAE.0000000000000163
pubmed: 24732699
Nguyen JH, Yee KM, Sadun AA, Sebag J (2016) Quantifying visual dysfunction and the response to surgery in macular pucker. Ophthalmology 123:1500–1510. https://doi.org/10.1016/j.ophtha.2016.03.022
doi: 10.1016/j.ophtha.2016.03.022
pubmed: 27129901
Enders P, Schick T, Schaub F et al (2017) Risk of multiple recurring retinal detachment after primary rhegmatogenous retinal detachment repair. Retina 37:930–935. https://doi.org/10.1097/IAE.0000000000001302
doi: 10.1097/IAE.0000000000001302
pubmed: 27635776
Mudhar HS (2020) A brief review of the histopathology of proliferative vitreoretinopathy (PVR). Eye (Lond) 34:246–250. https://doi.org/10.1038/s41433-019-0724-4
doi: 10.1038/s41433-019-0724-4
pubmed: 31792351
Sakamoto T, Ishibashi T (2011) Hyalocytes: essential cells of the vitreous cavity in vitreoretinal pathophysiology? Retina 31:222–228. https://doi.org/10.1097/IAE.0b013e3181facfa9
doi: 10.1097/IAE.0b013e3181facfa9
pubmed: 21240043
Hirayama K, Hata Y, Noda Y et al (2004) The involvement of the rho-kinase pathway and its regulation in cytokine-induced collagen gel contraction by hyalocytes. Invest Ophthalmol Vis Sci 45:3896–3903. https://doi.org/10.1167/iovs.03-1330
doi: 10.1167/iovs.03-1330
pubmed: 15505034
Guenther SR, Schumann RG, Hagenau F et al (2019) Comparison of surgically excised premacular membranes in eyes with macular pucker and proliferative vitreoretinopathy. Curr Eye Res 44:341–349. https://doi.org/10.1080/02713683.2018.1542006
doi: 10.1080/02713683.2018.1542006
pubmed: 30373411
van Overdam KA, Busch EM, Verdijk RM, Pennekamp CWA (2021) The role of vitreous cortex remnants in proliferative vitreoretinopathy formation demonstrated by histopathology: a case report. Am J Ophthalmol Case Rep 24:101219. https://doi.org/10.1016/j.ajoc.2021.101219
doi: 10.1016/j.ajoc.2021.101219
pubmed: 34646961
pmcid: 8501493
Song Y, Liao M, Zhao X et al (2021) Vitreous M2 macrophage-derived microparticles promote RPE cell proliferation and migration in traumatic proliferative vitreoretinopathy. Invest Ophthalmol Vis Sci 62:26. https://doi.org/10.1167/iovs.62.12.26
doi: 10.1167/iovs.62.12.26
pubmed: 34554178
pmcid: 8475283
Cheung N, Mitchell P, Wong TY (2010) Diabetic retinopathy. Lancet 376:124–136. https://doi.org/10.1016/S0140-6736(09)62124-3
doi: 10.1016/S0140-6736(09)62124-3
pubmed: 20580421
Lange CAK, Stavrakas P, Luhmann UFO et al (2011) Intraocular oxygen distribution in advanced proliferative diabetic retinopathy. Am J Ophthalmol 152:406-412.e3. https://doi.org/10.1016/j.ajo.2011.02.014
doi: 10.1016/j.ajo.2011.02.014
pubmed: 21723532
Wecker T, Ehlken C, Bühler A et al (2017) Five-year visual acuity outcomes and injection patterns in patients with pro-re-nata treatments for AMD, DME, RVO and myopic CNV. Br J Ophthalmol 101:353–359. https://doi.org/10.1136/bjophthalmol-2016-308668
doi: 10.1136/bjophthalmol-2016-308668
pubmed: 27215744
Boneva SK, Wolf J, Hajdú RI et al (2021) In-depth molecular characterization of neovascular membranes suggests a role for hyalocyte-to-myofibroblast transdifferentiation in proliferative diabetic retinopathy. Front Immunol 12:757607. https://doi.org/10.3389/fimmu.2021.757607
doi: 10.3389/fimmu.2021.757607
pubmed: 34795670
pmcid: 8593213
Zhao F, Gandorfer A, Haritoglou C et al (2013) Epiretinal cell proliferation in macular pucker and vitreomacular traction syndrome: analysis of flat-mounted internal limiting membrane specimens. Retina 33:77–88. https://doi.org/10.1097/IAE.0b013e3182602087
doi: 10.1097/IAE.0b013e3182602087
pubmed: 22914684
Little K, Llorián-Salvador M, Tang M et al (2020) Macrophage to myofibroblast transition contributes to subretinal fibrosis secondary to neovascular age-related macular degeneration. J Neuroinflammation 17:355. https://doi.org/10.1186/s12974-020-02033-7
doi: 10.1186/s12974-020-02033-7
pubmed: 33239022
pmcid: 7690191
Sebag J (2004) Seeing the invisible: the challenge of imaging vitreous. J Biomed Opt 9:38–46. https://doi.org/10.1117/1.1627339
doi: 10.1117/1.1627339
pubmed: 14715056
Schumann RG, Eibl KH, Zhao F et al (2011) Immunocytochemical and ultrastructural evidence of glial cells and hyalocytes in internal limiting membrane specimens of idiopathic macular holes. Invest Ophthalmol Vis Sci 52:7822–7834. https://doi.org/10.1167/iovs.11-7514
doi: 10.1167/iovs.11-7514
pubmed: 21900375
Schumann RG, Gandorfer A, Ziada J et al (2014) Hyalocytes in idiopathic epiretinal membranes: a correlative light and electron microscopic study. Graefes Arch Clin Exp Ophthalmol 252:1887–1894. https://doi.org/10.1007/s00417-014-2841-x
doi: 10.1007/s00417-014-2841-x
pubmed: 25377434
Sebag J, Gupta P, Rosen RR et al (2007) Macular holes and macular pucker: the role of vitreoschisis as imaged by optical coherence tomography/scanning laser ophthalmoscopy. Trans Am Ophthalmol Soc 105:121–129 (discusion 129-131)
pubmed: 18427601
pmcid: 2258095
Gandorfer A, Rohleder M, Kampik A (2002) Epiretinal pathology of vitreomacular traction syndrome. Br J Ophthalmol 86:902–909. https://doi.org/10.1136/bjo.86.8.902
doi: 10.1136/bjo.86.8.902
pubmed: 12140213
pmcid: 1771255
Sebag J (2001) Shaken not stirred. Ophthalmology 108:1177–1178. https://doi.org/10.1016/s0161-6420(01)00621-2
doi: 10.1016/s0161-6420(01)00621-2
pubmed: 11425670
Haritoglou C, Sebag J (2014) Indications and considerations for chromodissection. Retinal Physician 11:34–39
van Overdam KA, van den Bosch TPP, van Etten PG et al (2022) Novel insights into the pathophysiology of proliferative vitreoretinopathy: The role of vitreoschisis-induced vitreous cortex remnants. Acta Ophthalmol 100:e1749–e1759. https://doi.org/10.1111/aos.15197
doi: 10.1111/aos.15197
pubmed: 35673878
Kato Y, Inoue M, Hirakata A (2021) Effect of foveal vitreous cortex removal to prevent epiretinal membrane after vitrectomy for rhegmatogenous retinal detachment. Ophthalmol Retina 5:420–428. https://doi.org/10.1016/j.oret.2020.08.020
doi: 10.1016/j.oret.2020.08.020
pubmed: 32891864
Rizzo S, de Angelis L, Barca F et al (2022) Vitreoschisis and retinal detachment: new insight in proliferative vitreoretinopathy. Eur J Ophthalmol 32:2833–2839. https://doi.org/10.1177/11206721211057672
doi: 10.1177/11206721211057672
pubmed: 34779683
Wakabayashi T, Mahmoudzadeh R, Salabati M et al (2022) Utility of removal of vitreous cortex remnants during vitrectomy for primary rhegmatogenous retinal detachment repair. Curr Eye Res 47:1444–1449. https://doi.org/10.1080/02713683.2022.2103154
doi: 10.1080/02713683.2022.2103154
pubmed: 35838170
Sartini F, Menchini M, Loiudice P et al (2022) Surgical technique for removing vitreous cortex remnants using a diamond-dusted membrane scraper. Acta Ophthalmol 100:344–347. https://doi.org/10.1111/aos.14933
doi: 10.1111/aos.14933
pubmed: 34137508
Sebag J (2009) Pharmacologic vitreolysis–premise and promise of the first decade. Retina 29:871–874. https://doi.org/10.1097/IAE.0b013e3181ac7b3c
doi: 10.1097/IAE.0b013e3181ac7b3c
pubmed: 19584647
Huang Y, Xu Z, Xiong S et al (2018) Dual extra-retinal origins of microglia in the model of retinal microglia repopulation. Cell Discov 4:9. https://doi.org/10.1038/s41421-018-0011-8
doi: 10.1038/s41421-018-0011-8
pubmed: 29507754
pmcid: 5827656