Embryonic nutritional hyperglycemia decreases cell proliferation in the zebrafish retina.
Cell proliferation
Diabetic retinopathy
Hyperglycemia
Mitosis
Retina
Zebrafish
Journal
Histochemistry and cell biology
ISSN: 1432-119X
Titre abrégé: Histochem Cell Biol
Pays: Germany
ID NLM: 9506663
Informations de publication
Date de publication:
Oct 2022
Oct 2022
Historique:
accepted:
10
06
2022
pubmed:
3
7
2022
medline:
28
9
2022
entrez:
2
7
2022
Statut:
ppublish
Résumé
Diabetic retinopathy (DR) is one of the leading causes of blindness in the world. While there is a major focus on the study of juvenile/adult DR, the effects of hyperglycemia during early retinal development are less well studied. Recent studies in embryonic zebrafish models of nutritional hyperglycemia (high-glucose exposure) have revealed that hyperglycemia leads to decreased cell numbers of mature retinal cell types, which has been related to a modest increase in apoptotic cell death and altered cell differentiation. However, how embryonic hyperglycemia impacts cell proliferation in developing retinas still remains unknown. Here, we exposed zebrafish embryos to 50 mM glucose from 10 h postfertilization (hpf) to 5 days postfertilization (dpf). First, we confirmed that hyperglycemia increases apoptotic death and decreases the rod and Müller glia population in the retina of 5-dpf zebrafish. Interestingly, the increase in cell death was mainly observed in the ciliary marginal zone (CMZ), where most of the proliferating cells are located. To analyze the impact of hyperglycemia in cell proliferation, mitotic activity was first quantified using pH3 immunolabeling, which revealed a significant decrease in mitotic cells in the retina (mainly in the CMZ) at 5 dpf. A significant decrease in cell proliferation in the outer nuclear and ganglion cell layers of the central retina in hyperglycemic animals was also detected using the proliferation marker PCNA. Overall, our results show that nutritional hyperglycemia decreases cellular proliferation in the developing retina, which could significantly contribute to the decline in the number of mature retinal cells.
Identifiants
pubmed: 35779079
doi: 10.1007/s00418-022-02127-8
pii: 10.1007/s00418-022-02127-8
doi:
Substances chimiques
Proliferating Cell Nuclear Antigen
0
Glucose
IY9XDZ35W2
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
401-409Subventions
Organisme : Xunta de Galicia
ID : ED481A-2019/120
Organisme : Xunta de Galicia
ID : ED431C 2021/18
Organisme : Agencia Estatal de Investigación
ID : PID2020-115121GB-I00
Organisme : Agencia Estatal de Investigación
ID : PID2020-113881RB-I00
Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Ali Z, Zang J, Lagali N, Schmitner N, Salvenmoser W, Mukwaya A, Neuhauss S, Jensen LD, Kimmel RA (2020) Photoreceptor degeneration accompanies vascular changes in a zebrafish model of diabetic retinopathy. Investig Ophthalmol vis Sci 61:43. https://doi.org/10.1167/iovs.61.2.43
doi: 10.1167/iovs.61.2.43
Alvarez Y, Chen K, Reynolds AL, Waghorne N, O’Connor JJ, Kennedy BN (2010) Predominant cone photoreceptor dysfunction in a hyperglycaemic model of non-proliferative diabetic retinopathy. Dis Model Mech 3:236–245. https://doi.org/10.1242/dmm.003772
doi: 10.1242/dmm.003772
pubmed: 20142328
Amini R, Labudina AA, Norden C (2019) Stochastic single cell migration leads to robust horizontal cell layer formation in the vertebrate retina. Development 146:dev173450. https://doi.org/10.1242/dev.173450
doi: 10.1242/dev.173450
pubmed: 31126979
Bejarano-Escobar R, Blasco M, DeGrip WJ, Martín-Partido G, Francisco-Morcillo J (2009) Cell differentiation in the retina of an epibenthonic teleost, the Tench (Tinca tinca, Linneo 1758). Exp Eye Res 89:398–415
doi: 10.1016/j.exer.2009.04.007
Bejarano-Escobar R, Blasco M, Durán AC, Rodríguez C, Martín-Partido G, Francisco-Morcillo J (2012) Retinal histogenesis and cell differentiation in an elasmobranch species, the small-spotted catshark Scyliorhinus canicula. J Anat 220:318–335. https://doi.org/10.1111/j.1469-7580.2012.01480.x
doi: 10.1111/j.1469-7580.2012.01480.x
pubmed: 22332849
pmcid: 3375769
Bringmann A, Pannicke T, Grosche J, Francke M, Wiedemann P, Skatchkov SN, Osborne NN, Reichenbach A (2006) Müller cells in the healthy and diseased retina. Prog Retin Eye Res 25:397–424. https://doi.org/10.1016/j.preteyeres.2006.05.003
doi: 10.1016/j.preteyeres.2006.05.003
pubmed: 16839797
Cai X, McGinnis JF (2016) Diabetic Retinopathy: animal models, therapies, and perspectives. J Diabetes Res 2016:3789217. https://doi.org/10.1155/2016/3789217
doi: 10.1155/2016/3789217
pubmed: 26881246
pmcid: 4736804
Candal E, Anadón R, DeGrip WJ, Rodríguez-Moldes I (2005) Patterns of cell proliferation and cell death in the developing retina and optic tectum of the brown trout. Brain Res Dev 154:101–119. https://doi.org/10.1016/j.devbrainres.2004.10.008
doi: 10.1016/j.devbrainres.2004.10.008
Cid E, Velasco A, Ciudad J, Orfao A, Aijón J, Lara JM (2002) Quantitative evaluation of the distribution of proliferating cells in the adult retina in three cyprinid species. Cell Tissue Res 308(1):47–59. https://doi.org/10.1007/s00441-002-0529-8
Easter SS Jr, Nicola GN (1996) The development of vision in the zebrafish (Danio rerio). Dev Biol 180:646–663. https://doi.org/10.1006/dbio.1996.0335
doi: 10.1006/dbio.1996.0335
pubmed: 8954734
Fernández-López B, Barreiro-Iglesias A, Rodicio MC (2014) Confocal microscopy used for the semiautomatic quantification of the changes in aminoacidergic fibers during spinal cord regeneration. In: Bakota L., Brandt R. (eds) Laser Scanning Microscopy and Quantitative Image Analysis of Neuronal Tissue. Neuromethods, vol 87. Humana Press, New York, NY https://doi.org/10.1007/978-1-4939-0381-8_11
Ferreiro-Galve S, Rodríguez-Moldes I, Anadón R, Candal E (2010a) Patterns of cell proliferation and rod photoreceptor differentiation in shark retinas. J Chem Neuroanat 39:1–14. https://doi.org/10.1016/j.jchemneu.2009.10.001
doi: 10.1016/j.jchemneu.2009.10.001
pubmed: 19822206
Ferreiro-Galve S, Rodríguez-Moldes I, Candal E (2010b) Calretinin immunoreactivity in the developing retina of sharks: comparison with cell proliferation and GABAergic system markers. Exp Eye Res 91:378–386. https://doi.org/10.1016/j.exer.2010.06.011
doi: 10.1016/j.exer.2010.06.011
pubmed: 20599967
Ferreiro-Galve S, Rodríguez-Moldes I, Candal E (2012) Pax6 expression during retinogenesis in sharks: comparison with markers of cell proliferation and neuronal differentiation. J Exp Zool B Mol Dev Evol 318:91–108. https://doi.org/10.1002/jezb.21448
doi: 10.1002/jezb.21448
pubmed: 22532472
Gilbert JS, Banek CT, Babcock SA, Dreyer HC (2013) Diabetes in early pregnancy: getting to the heart of the matter. Diabetes 62:27–28. https://doi.org/10.2337/db12-1117
doi: 10.2337/db12-1117
pubmed: 23258908
Gleeson M, Connaughton V, Arneson LS (2007) Induction of hyperglycaemia in zebrafish (Danio rerio) leads to morphological changes in the retina. Acta Diabetol 44:157–163. https://doi.org/10.1007/s00592-007-0257-3
doi: 10.1007/s00592-007-0257-3
pubmed: 17721755
Godinho L, Williams PR, Claassen Y, Provost E, Leach SD, Kamermans M, Wong RO (2007) Nonapical symmetric divisions underlie horizontal cell layer formation in the developing retina in vivo. Neuron 56:597–603. https://doi.org/10.1016/j.neuron.2007.09.036
doi: 10.1016/j.neuron.2007.09.036
pubmed: 18031679
Hernández-Núñez I, Quelle-Regaldie A, Sánchez L, Adrio F, Candal E, Barreiro-Iglesias A (2021a) Decline in constitutive proliferative activity in the zebrafish retina with ageing. Int J Mol Sci 22:11715. https://doi.org/10.3390/ijms222111715
doi: 10.3390/ijms222111715
pubmed: 34769146
pmcid: 8583983
Hernández-Núñez I, Robledo D, Mayeur H, Mazan S, Sánchez L, Adrio F, Barreiro-Iglesias A, Candal E (2021b) Loss of active neurogenesis in the adult shark retina. Front Cell Dev Biol 9:628721. https://doi.org/10.3389/fcell.2021.628721
doi: 10.3389/fcell.2021.628721
pubmed: 33644067
pmcid: 7905061
Jensen AM, Walker C, Westerfield M (2001) Mosaic eyes: a zebrafish gene required in pigmented epithelium for apical localization of retinal cell division and lamination. Development 128:95–105. https://doi.org/10.1242/dev.128.1.95
doi: 10.1242/dev.128.1.95
pubmed: 11092815
Jung SH, Kim YS, Lee YR, Kim JS (2016) High glucose-induced changes in hyaloid-retinal vessels during early ocular development of zebrafish: a short-term animal model of diabetic retinopathy. Br J Pharmacol 173:15–26. https://doi.org/10.1111/bph.13279
doi: 10.1111/bph.13279
pubmed: 26276677
Kua KL, Hu S, Wang C, Yao J, Dang D, Sawatzke AB, Segar JL, Wang K, Norris AW (2019) Fetal hyperglycemia acutely induces persistent insulin resistance in skeletal muscle. J Endocrinol 242:M1–M15. https://doi.org/10.1530/JOE-18-0455
doi: 10.1530/JOE-18-0455
pubmed: 30444716
pmcid: 6494731
Landau K, Bajka JD, Kirchschläger BM (1998) Topless optic disks in children of mothers with type I diabetes mellitus. Am J Ophthalmol 125:605–611: https://doi.org/10.1016/s0002-9394(98)00016-6
Leasher JL, Bourne RR, Flaxman SR, Jonas JB, Keeffe J, Naidoo K, Pesudovs K, Price H, White RA, Wong TY, Resnikoff S, Taylor HR, Vision Loss Expert Group of the Global Burden of Disease Study (2016) Global estimates on the number of people blind or visually impaired by diabetic retinopathy: a meta-analysis from 1990 to 2010. Diabetes care 39:1643–1649. https://doi.org/10.2337/dc15-2171
doi: 10.2337/dc15-2171
pubmed: 27555623
Lee Y, Yang J (2021) Development of a zebrafish screening model for diabetic retinopathy induced by hyperglycemia: reproducibility verification in animal model. Biomed 135:111201. https://doi.org/10.1016/j.biopha.2020.111201
doi: 10.1016/j.biopha.2020.111201
Mack AF, Germer A, Janke C, Reichenbach A (1998) Müller (glial) cells in the teleost retina: consequences of continuous growth. Glia 22:306–313
doi: 10.1002/(SICI)1098-1136(199803)22:3<306::AID-GLIA9>3.0.CO;2-2
Malicki J, Neuhauss SC, Schier AF, Solnica-Krezel L, Stemple DL, Stainier DY, Abdelilah S, Zwartkruis F, Rangini Z, Driever W (1996) Mutations affecting development of the zebrafish retina. Development 123:263–273. https://doi.org/10.1242/dev.123.1.263
doi: 10.1242/dev.123.1.263
pubmed: 9007246
McCarthy E, Rowe CJ, Crowley-Perry M, Connaughton VP (2021) Alternate immersion in glucose to produce prolonged hyperglycemia in zebrafish. J vis Exp 5:171. https://doi.org/10.3791/61935
doi: 10.3791/61935
Meier A, Nelson R, Connaughton VP (2018) Color processing in zebrafish retina. Front Cell Neurosci 12:327. https://doi.org/10.3389/fncel.2018.00327
doi: 10.3389/fncel.2018.00327
pubmed: 30337857
pmcid: 6178926
Meléndez-Ferro M, Villar-Cheda B, Abalo XM, Pérez-Costas E, Rodríguez-Muñoz R, Degrip WJ, Yáñez J, Rodicio MC, Anadón R (2002) Early development of the retina and pineal complex in the sea lamprey: comparative immunocytochemical study. J Comp Neurol 442:250–265. https://doi.org/10.1002/cne.10090
doi: 10.1002/cne.10090
pubmed: 11774340
Ogurtsova K, da Rocha Fernandes JD, Huang Y, Linnenkamp U, Guariguata L, Cho NH, Cavan D, Shaw JE, Makaroff LE (2017) IDF diabetes atlas: global estimates for the prevalence of diabetes for 2015 and 2040. Diabetes Res Clin Pract 128:40–50
doi: 10.1016/j.diabres.2017.03.024
Pan WW, Lin F, Fort PE (2021) The innate immune system in diabetic retinopathy. Prog Retin Eye Res 84:100940. https://doi.org/10.1016/j.preteyeres.2021.100940
doi: 10.1016/j.preteyeres.2021.100940
pubmed: 33429059
pmcid: 8263813
Peterson RE, Fadool JM, McClintock J, Linser PJ (2001) Müller cell differentiation in the zebrafish neural retina: evidence of distinct early and late stages in cell maturation. J Comp Neurol 429:530–540. https://doi.org/10.1002/1096-9861(20010122)429:4%3c530::aid-cne2%3e3.0.co;2-c
doi: 10.1002/1096-9861(20010122)429:4<530::aid-cne2>3.0.co;2-c
pubmed: 11135233
Romaus-Sanjurjo D, Valle-Maroto SM, Barreiro-Iglesias A, Fernández-López B, Rodicio MC (2018) Anatomical recovery of the GABAergic system after a complete spinal cord injury in lampreys. Neuropharmacology 131:389–402. https://doi.org/10.1016/j.neuropharm.2018.01.006
doi: 10.1016/j.neuropharm.2018.01.006
pubmed: 29317225
Sánchez-Farías N, Candal E (2015) Doublecortin widely expressed in the developing and adult retina of sharks. Exp Eye Res 134:90–100. https://doi.org/10.1016/j.exer.2015.04.002
doi: 10.1016/j.exer.2015.04.002
pubmed: 25849205
Sánchez-Farías N, Candal E (2016) Identification of radial glia progenitors in the developing and adult retina of sharks. Front Neuroanat 10:65. https://doi.org/10.3389/fnana.2016.00065
doi: 10.3389/fnana.2016.00065
pubmed: 27378863
pmcid: 4913098
Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, Tinevez JY, White DJ, Hartenstein V, Eliceiri K, Tomancak P, Cardona A (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9:676–682. https://doi.org/10.1038/nmeth.2019
doi: 10.1038/nmeth.2019
pubmed: 22743772
Schmitner N, Recheis C, Thönig J, Kimmel RA (2021) Differential responses of neural retina progenitor populations to chronic hyperglycemia. Cell 10:3265. https://doi.org/10.3390/cells10113265
doi: 10.3390/cells10113265
Scott-Drechsel DE, Rugonyi S, Marks DL, Thornburg KL, Hinds MT (2013) Hyperglycemia slows embryonic growth and suppresses cell cycle via cyclin D1 and p21. Diabetes 62:234–242. https://doi.org/10.2337/db12-0161
doi: 10.2337/db12-0161
pubmed: 23193186
Simó R, Stitt AW, Gardner TW (2018) Neurodegeneration in diabetic retinopathy: does it really matter? Diabetologia 61:1902–1912. https://doi.org/10.1007/s00125-018-4692-1
doi: 10.1007/s00125-018-4692-1
pubmed: 30030554
pmcid: 6096638
Singh A, Castillo HA, Brown J, Kaslin J, Dwyer KM, Gibert Y (2019) High glucose levels affect retinal patterning during zebrafish embryogenesis. Sci Rep 9:4121. https://doi.org/10.1038/s41598-019-41009-3
doi: 10.1038/s41598-019-41009-3
pubmed: 30858575
pmcid: 6411978
Tanvir Z, Nelson RF, DeCicco-Skinner K, Connaughton VP (2018) One month of hyperglycemia alters spectral responses of the zebrafish photopic electroretinogram. Dis Model Mech 11:dmm035220. https://doi.org/10.1242/dmm.035220
doi: 10.1242/dmm.035220
pubmed: 30158110
pmcid: 6215424
Tariq YM, Samarawickrama C, Li H, Huynh SC, Burlutsky G, Mitchell P (2010) Retinal thickness in the offspring of diabetic pregnancies. Am J Ophthalmol 150:883–887. https://doi.org/10.1016/j.ajo.2010.06.036
doi: 10.1016/j.ajo.2010.06.036
pubmed: 20951974
Thummel R, Kassen SC, Enright JM, Nelson CM, Montgomery JE, Hyde DR (2008) Characterization of Müller glia and neuronal progenitors during adult zebrafish retinal regeneration. Exp Eye Res 87:433–444. https://doi.org/10.1016/j.exer.2008.07.009
doi: 10.1016/j.exer.2008.07.009
pubmed: 18718467
pmcid: 2586672
Titialii-Torres KF, Morris AC (2022) Embryonic hyperglycemia perturbs the development of specific retinal cell types, including photoreceptors. J Cell Sci 135:jcs259187. https://doi.org/10.1242/jcs.259187
doi: 10.1242/jcs.259187
pubmed: 34851372
Villar-Cheda B, Abalo XM, Villar-Cerviño V, Barreiro-Iglesias A, Anadón R, Rodicio MC (2008) Late proliferation and photoreceptor differentiation in the transforming lamprey retina. Brain Res 1201:60–67
doi: 10.1016/j.brainres.2008.01.077
Wang S, Du S, Wang W, Zhang F (2020) Therapeutic investigation of quercetin nanomedicine in a zebrafish model of diabetic retinopathy. Biomed 130:110573. https://doi.org/10.1016/j.biopha.2020.110573
doi: 10.1016/j.biopha.2020.110573
Weber IP, Ramos AP, Strzyz PJ, Leung LC, Young S, Norden C (2014) Mitotic position and morphology of committed precursor cells in the zebrafish retina adapt to architectural changes upon tissue maturation. Cell Rep 7:386–397. https://doi.org/10.1016/j.celrep.2014.03.014
doi: 10.1016/j.celrep.2014.03.014
pubmed: 24703843
Wiggenhauser LM, Qi H, Stoll SJ, Metzger L, Bennewitz K, Poschet G, Krenning G, Hillebrands JL, Hammes HP, Kroll J (2020) Activation of retinal angiogenesis in hyperglycemic pdx1-/- zebrafish mutants. Diabetes 69:1020–1031. https://doi.org/10.2337/db19-0873
doi: 10.2337/db19-0873
pubmed: 32139597