The quantification of zebrafish ocular-associated proteins provides hints for sex-biased visual impairments and perception
Status PubMed-not-MEDLINE Language English Country England, Great Britain Media electronic-ecollection
Document type Journal Article
PubMed
38994070
PubMed Central
PMC11238053
DOI
10.1016/j.heliyon.2024.e33057
PII: S2405-8440(24)09088-1
Knihovny.cz E-resources
- Keywords
- Eye, Protein, Proteomics, Sexual dimorphism,
- Publication type
- Journal Article MeSH
Biochemical differences between sexes can also be seen in non-sexual organs and may affect organ functions and susceptibility to diseases. It has been shown that there are sex-biased visual perceptions and impairments. Abundance differences of eye proteins could provide explanations for some of these. Exploration of the ocular proteome was performed to find sex-based protein abundance differences in zebrafish Danio rerio. A label-free protein quantification workflow using high-resolution mass spectrometry was employed to find proteins with significant differences between the sexes. In total, 3740 unique master proteins were identified and quantified, and 49 proteins showed significant abundance differences between the eyes of male and female zebrafish. Those proteins belong to lipoproteins, immune system, blood coagulation, antioxidants, iron and heme-binding proteins, ion channels, pumps and exchangers, neuronal and photoreceptor proteins, and the cytoskeleton. An extensive literature review provided clues for the possible links between the sex-biased level of proteins and visual perception and impairments. In conclusion, sexual dimorphism at the protein level was discovered for the first time in the eye of zebrafish and should be accounted for in ophthalmological studies. Data are available via ProteomeXchange with identifier PXD033338.
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Niksirat H., Siino V., Steinbach C., Levander F. High-resolution proteomic profiling shows sexual dimorphism in zebrafish heart-associated proteins. J. Proteome Res. 2021;20:4075–4088. doi: 10.1021/acs.jproteome.1c00387. PubMed DOI
Gianazza E., Miller I., Guerrini U., Palazzolo L., Parravicini C., Eberini I. Gender proteomics I. Which proteins in non-sexual organs. J. Proteonomics. 2018;178:7–17. doi: 10.1016/j.jprot.2017.10.002. PubMed DOI
Hajipour M.J., Aghaverdi H., Serpooshan V., Vali H., Sheibani S., Mahmoudi M. Sex as an important factor in nanomedicine. Nat. Commun. 2021;12:2984. doi: 10.1038/s41467-021-23230-9. PubMed DOI PMC
Zetterberg M., Celojevic D. Gender and cataract - the role of estrogen. Curr. Eye Res. 2015;40:176–190. doi: 10.3109/02713683.2014.898774. PubMed DOI
Klein R., Klein B.E.K., Knudtson M.D., Meuer S.M., Swift M., Gangnon R.E. Fifteen-year cumulative incidence of age-related macular degeneration. Ophthalmology. 2007;114:253–262. doi: 10.1016/j.ophtha.2006.10.040. PubMed DOI
Abramov I., Gordon J., Feldman O., Chavarga A. Sex & vision I: spatio-temporal resolution. Biol. Sex Differ. 2012;3:20. doi: 10.1186/2042-6410-3-20. PubMed DOI PMC
Abramov I., Gordon J., Feldman O., Chavarga A. Sex and vision II: color appearance of monochromatic lights. Biol. Sex Differ. 2012;3:21. doi: 10.1186/2042-6410-3-21. PubMed DOI PMC
Howe K., Clark M.D., Torroja C.F., Torrance J., Berthelot C., Muffato M., Collins J.E., Humphray S., McLaren K., Matthews L., et al. The zebrafish reference genome sequence and its relationship to the human genome. Nature. 2013;496:498–503. doi: 10.1038/nature12111. PubMed DOI PMC
Richardson R., Tracey-White D., Webster A., Moosajee M. The zebrafish eye-a paradigm for investigating human ocular genetics. Eye. 2017;31:68–86. doi: 10.1038/eye.2016.198. PubMed DOI PMC
Blanco-Sanchez B., Clement A., Phillips J.B., Westerfield M. Zebrafish models of human eye and inner ear diseases. Methods Cell Biol. 2017;138:415–467. doi: 10.1016/bs.mcb.2016.10.006. PubMed DOI
Eastlake K., Heywood W.E., Tracey-White D., Aquino E., Bliss E., Vasta G.R., Mills K., Khaw P.T., Moosajee M., Limb G.A. Comparison of proteomic profiles in the zebrafish retina during experimental degeneration and regeneration. Sci Rep-Uk. 2017;7 doi: 10.1038/srep44601. ARTN 44601. PubMed DOI PMC
Niksirat H., James P., Andersson L., Kouba A., Kozak P. Label-free protein quantification in freshly ejaculated versus post-mating spermatophores of the noble crayfish Astacus astacus. J. Proteonomics. 2015;123:70–77. doi: 10.1016/j.jprot.2015.04.004. PubMed DOI
Chambers M.C., Maclean B., Burke R., Amodei D., Ruderman D.L., Neumann S., Gatto L., Fischer B., Pratt B., Egertson J., et al. A cross-platform toolkit for mass spectrometry and proteomics. Nat. Biotechnol. 2012;30:918–920. doi: 10.1038/nbt.2377. PubMed DOI PMC
Teleman J., Chawade A., Sandin M., Levander F., Malmstrom J. Dinosaur: a refined open-source peptide ms feature detector. J. Proteome Res. 2016;15:2143–2151. doi: 10.1021/acs.jproteome.6b00016. PubMed DOI PMC
Hakkinen J., Vincic G., Mansson O., Warell K., Levander F. The Proteios software environment: an extensible multiuser platform for management and analysis of proteomics data. J. Proteome Res. 2009;8:3037–3043. doi: 10.1021/pr900189c. PubMed DOI
Kim S., Pevzner P.A. MS-GF plus makes progress towards a universal database search tool for proteomics. Nat. Commun. 2014;5 doi: 10.1038/ncomms6277. PubMed DOI PMC
Craig R., Beavis R.C. TANDEM: matching proteins with tandem mass spectra. Bioinformatics. 2004;20:1466–1467. doi: 10.1093/bioinformatics/bth092. PubMed DOI
Sandin M., Ali A., Hansson K., Mansson O., Andreasson E., Resjo S., Levander F. An adaptive alignment algorithm for quality-controlled label-free LC-MS. Mol. Cell. Proteomics. 2013;12:1407–1420. doi: 10.1074/mcp.O112.021907. PubMed DOI PMC
Willforss J., Chawade A., Levander F. NormalyzerDE: online tool for improved normalization of omics expression data and high-sensitivity differential expression analysis. J. Proteome Res. 2019;18:732–740. doi: 10.1021/acs.jproteome.8b00523. PubMed DOI
Karpievitch Y., Stanley J., Taverner T., Huang J., Adkins J.N., Ansong C., Heffron F., Metz T.O., Qian W.J., Yoon H., et al. A statistical framework for protein quantitation in bottom-up MS-based proteomics. Bioinformatics. 2009;25:2028–2034. doi: 10.1093/bioinformatics/btp362. PubMed DOI PMC
Ritchie M.E., Phipson B., Wu D., Hu Y.F., Law C.W., Shi W., Smyth G.K. Limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 2015;43 doi: 10.1093/nar/gkv007. PubMed DOI PMC
Willforss J., Siino V., Levander F. OmicLoupe: facilitating biological discovery by interactive exploration of multiple omic datasets and statistical comparisons. BMC Bioinf. 2021;22:1–19. PubMed PMC
Szklarczyk D., Gable A.L., Lyon D., Junge A., Wyder S., Huerta-Cepas J., Simonovic M., Doncheva N.T., Morris J.H., Bork P., et al. STRING v11: protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res. 2019;47:D607–D613. doi: 10.1093/nar/gky1131. PubMed DOI PMC
Niksirat H., Levander F., Kouba A., James P. Proteomic changes after fertilization and before first cleavage in rainbow trout Oncorhynchus mykiss. Aquaculture. 2020;520 doi: 10.1016/j.aquaculture.2020.734951. DOI
Baker M.E. Is vitellogenin an ancestor of apolipoprotein-B-100 of human low-density lipoprotein and human lipoprotein-lipase. Biochem. J. 1988;255:1057–1060. PubMed PMC
Yamada Y., Tian J., Yang Y., Cutler R.G., Wu T., Telljohann R.S., Mattson M.P., Handa J.T. Oxidized low density lipoproteins induce a pathologic response by retinal pigmented epithelial cells. J. Neurochem. 2008;105:1187–1197. doi: 10.1111/j.1471-4159.2008.05211.x. PubMed DOI
Xu S.S., Xie F.J., Tian L., Fallah S., Babaei F., Manno S.H.C., Manno F.A.M., Zhu L.N., Wong K.F., Liang Y.M., et al. Estrogen accelerates heart regeneration by promoting the inflammatory response in zebrafish. J. Endocrinol. 2020;245:39–51. doi: 10.1530/Joe-19-0413. PubMed DOI PMC
Colijn J.M., den Hollander A.I., Demirkan A., Cougnard-Gregoire A., Verzijden T., Kersten E., Meester-Smoor M.A., Merle B.M.J., Papageorgiou G., Ahmad S., et al. Increased high-density lipoprotein levels associated with age-related macular degeneration: evidence from the EYE-RISK and European eye epidemiology consortia. Ophthalmology. 2019;126:393–406. doi: 10.1016/j.ophtha.2018.09.045. PubMed DOI
Nordestgaard L.T., Tybjaerg-Hansen A., Frikke-Schmidt R., Nordestgaard B.G. Elevated apolipoprotein A1 and HDL cholesterol associated with age-related macular degeneration: 2 population cohorts. J. Clin. Endocrinol. Metab. 2021;106:e2749–e2758. doi: 10.1210/clinem/dgab095. PubMed DOI
Li C.X., Tan X.F., Lim T.K., Lin Q.S., Gong Z.Y. Comprehensive and quantitative proteomic analyses of zebrafish plasma reveals conserved protein profiles between genders and between zebrafish and human. Sci Rep-Uk. 2016;6 doi: 10.1038/srep24329. PubMed DOI PMC
Pradhan A., Olsson P.E. Germ cell depletion in zebrafish leads to incomplete masculinization of the brain. Gen. Comp. Endocrinol. 2018;265:15–21. doi: 10.1016/j.ygcen.2018.02.001. PubMed DOI
Klaver C.C., Kliffen M., van Duijn C.M., Hofman A., Cruts M., Grobbee D.E., van Broeckhoven C., de Jong P.T. Genetic association of apolipoprotein E with age-related macular degeneration. Am. J. Hum. Genet. 1998;63:200–206. doi: 10.1086/301901. PubMed DOI PMC
Johnson L.V., Forest D.L., Banna C.D., Radeke C.M., Maloney M.A., Hu J., Spencer C.N., Walker A.M., Tsie M.S., Bok D., et al. Cell culture model that mimics drusen formation and triggers complement activation associated with age-related macular degeneration. P Natl Acad Sci USA. 2011;108:18277–18282. doi: 10.1073/pnas.1109703108. PubMed DOI PMC
Ling C.N.Y., Lim S.C., Jonas J.B., Sabanayagam C. Obesity and risk of age-related eye diseases: a systematic review of prospective population-based studies. Int. J. Obes. 2021;45:1863–1885. doi: 10.1038/s41366-021-00829-y. PubMed DOI
Finucane M.M., Stevens G.A., Cowan M.J., Danaei G., Lin J.K., Paciorek C.J., Singh G.M., Gutierrez H.R., Lu Y.A., Bahalim A.N., et al. National, regional, and global trends in body-mass index since 1980: systematic analysis of health examination surveys and epidemiological studies with 960 country-years and 9.1 million participants. Lancet. 2011;377:557–567. doi: 10.1016/S0140-6736(10)62037-5. PubMed DOI PMC
Garawi F., Devries K., Thorogood N., Uauy R. Global differences between women and men in the prevalence of obesity: is there an association with gender inequality? Eur. J. Clin. Nutr. 2014;68:1101–1106. doi: 10.1038/ejcn.2014.86. PubMed DOI
Toomey C.B., Kelly U., Saban D.R., Rickman C.B. Regulation of age-related macular degeneration-like pathology by complement factor H. P Natl Acad Sci USA. 2015;112:E3040–E3049. doi: 10.1073/pnas.1424391112. PubMed DOI PMC
Hageman G.S., Anderson D.H., Johnson L.V., Hancox L.S., Taiber A.J., Hardisty L.I., Hageman J.L., Stockman H.A., Borchardt J.D., Gehrs K.M., et al. A common haplotype in the complement regulatory gene factor H (HF1/CFH) predisposes individuals to age-related macular degeneration. P Natl Acad Sci USA. 2005;102:7227–7232. doi: 10.1073/pnas.0501536102. PubMed DOI PMC
Thompson R.B., Reffatto V., Bundy J.G., Kortvely E., Flinn J.M., Lanzirotti A., Jones E.A., McPhail D.S., Fearn S., Boldt K., et al. Identification of hydroxyapatite spherules provides new insight into subretinal pigment epithelial deposit formation in the aging eye. P Natl Acad Sci USA. 2015;112:1565–1570. doi: 10.1073/pnas.1413347112. PubMed DOI PMC
Toomey C.B., Johnson L.V., Rickman C.B. Complement factor H in AMD: bridging genetic associations and pathobiology. Prog. Retin. Eye Res. 2018;62:38–57. doi: 10.1016/j.preteyeres.2017.09.001. PubMed DOI PMC
Armento A., Honisch S., Panagiotakopoulou V., Sonntag I., Jacob A., Bolz S., Kilger E., Deleidi M., Clark S., Ueffing M. Loss of Complement Factor H impairs antioxidant capacity and energy metabolism of human RPE cells. Sci Rep-Uk. 2020;10 doi: 10.1038/s41598-020-67292-z. PubMed DOI PMC
Matthews K.W., Mueller-Ortiz S.L., Wetsel R.A. Carboxypeptidase N: a pleiotropic regulator of inflammation. Mol. Immunol. 2004;40:785–793. PubMed
Skidgel R.A., Erdos E.G. Structure and function of human plasma carboxypeptidase N, the anaphylatoxin inactivator. Int. Immunopharm. 2007;7:1888–1899. doi: 10.1016/j.intimp.2007.07.014. PubMed DOI PMC
Fabregat A., Jupe S., Matthews L., Sidiropoulos K., Gillespie M., Garapati P., Haw R., Jassal B., Korninger F., May B., et al. The reactome pathway knowledgebase. Nucleic Acids Res. 2018;46:D649–D655. doi: 10.1093/nar/gkx1132. PubMed DOI PMC
Deboer J.P., Creasey A.A., Chang A., Abbink J.J., Roem D., Eerenberg A.J.M., Hack C.E., Taylor F.B. Alpha-2-Macroglobulin functions as an inhibitor of fibrinolytic, clotting, and neutrophilic proteinases in sepsis - studies using a baboon model. Infect. Immun. 1993;61:5035–5043. doi: 10.1128/Iai.61.12.5035-5043.1993. PubMed DOI PMC
Ollivier F.J., Gilger B.C., Barrie K.P., Kallberg M.E., Plummer C.E., O'Reilly S., Gelatt K.N., Brooks D.E. Proteinases of the cornea and preocular tear film. Vet. Ophthalmol. 2007;10:199–206. doi: 10.1111/j.1463-5224.2007.00546.x. PubMed DOI
Shi Z.H., Rudzinski M., Meerovitch K., Lebrun-Julien F., Birman E., Di Polo A., Saragovi H.U. Alpha 2-macroglobulin is a mediator of retinal ganglion cell death in glaucoma. J. Biol. Chem. 2008;283:29156–29165. doi: 10.1074/jbc.M802365200. PubMed DOI PMC
Bai Y.J., Sivori D., Woo S.B., Neet K.E., Lerner S.F., Saragovi H.U. During glaucoma, alpha 2-macroglobulin accumulates in aqueous humor and binds to nerve growth factor, neutralizing neuroprotection. Invest. Ophthalmol. Vis. Sci. 2011;52:5260–5265. doi: 10.1167/iovs.10-6691. PubMed DOI
Bost F., Diarra-Mehrpour M., Martin J.P. Inter-alpha-trypsin inhibitor proteoglycan family - a group of proteins binding and stabilizing the extracellular matrix. Eur. J. Biochem. 1998;252:339–346. doi: 10.1046/j.1432-1327.1998.2520339.x. PubMed DOI
Lord M.S., Melrose J., Day A.J., Whitelock J.M. The inter-alpha-trypsin inhibitor family: versatile molecules in biology and pathology. J. Histochem. Cytochem. 2020;68:907–927. doi: 10.1369/0022155420940067. PubMed DOI PMC
Petaja J. Inflammation and coagulation. An overview. Thromb. Res. 2011;127:S34–S37. doi: 10.1016/S0049-3848(10)70153-5. PubMed DOI
Mullins R.F., Russell S.R., Anderson D.H., Hageman G.S. Drusen associated with aging and age-related macular degeneration contain proteins common to extracellular deposits associated with atherosclerosis, elastosis, amyloidosis, and dense deposit disease. Faseb. J. 2000;14:835–846. doi: 10.1096/fasebj.14.7.835. PubMed DOI
Rodrigues E.B. Inflammation in dry age-related macular degeneration. Ophthalmologica. 2007;221:143–152. doi: 10.1159/000099293. PubMed DOI
Johnson L.V., Leitner W.P., Staples M.K., Anderson D.H. Complement activation and inflammatory processes in drusen formation and age related macular degeneration. Exp. Eye Res. 2001;73:887–896. doi: 10.1006/exer.2001.1094. PubMed DOI
Caillard A., Sadoune M., Cescau A., Meddour M., Gandon M., Polidano E., Delcayre C., Da Silva K., Manivet P., Gomez A.M., et al. QS0X1, a novel actor of cardiac protection upon acute stress in mice. J. Mol. Cell. Cardiol. 2018;119:75–86. doi: 10.1016/j.yjmcc.2018.04.014. PubMed DOI
Coppock D.L., Thorpe C. Multidomain flavin-dependent sulfhydryl oxidases. Antioxidants Redox Signal. 2006;8:300–311. doi: 10.1089/ars.2006.8.300. PubMed DOI
Zhao J., Liu Y., Wei X., Yuan C., Yuan X.R., Xiao X.Z. A novel WD-40 repeat protein WDR26 suppresses H2O2-induced cell death in neural cells. Neurosci. Lett. 2009;460:66–71. doi: 10.1016/j.neulet.2009.05.024. PubMed DOI
Chen W.H., Lu H.S., Dutt K., Smith A., Hunt D.M., Hunt R.C. Expression of the protective proteins hemopexin and haptoglobin by cells of the neural retina. Exp. Eye Res. 1998;67:83–93. doi: 10.1006/exer.1998.0494. PubMed DOI
He X.N., Hahn P., Iacovelli J., Wong R., King C., Bhisitkul R., Massaro-Giordano M., Dunaief J.L. Iron homeostasis and toxicity in retinal degeneration. Prog. Retin. Eye Res. 2007;26:649–673. doi: 10.1016/j.preteyeres.2007.07.004. PubMed DOI PMC
Weinberg E.D. Iron availability and infection. Bba-Gen Subjects. 2009;1790:600–605. doi: 10.1016/j.bbagen.2008.07.002. PubMed DOI
Lin T., Sammy F., Yang H., Thundivalappil S., Hellman J., Tracey K.J., Warren H.S. Identification of hemopexin as an anti-inflammatory factor that inhibits synergy of hemoglobin with HMGB1 in sterile and infectious inflammation. J. Immunol. 2012;189:2017–2022. doi: 10.4049/jimmunol.1103623. PubMed DOI PMC
Yefimova M.G., Jeanny J.C., Guillonneau X., Keller N., Nguyen-Legros J., Sergeant C., Guillou F., Courtois Y. Iron, ferritin, transferrin, and transferrin receptor in the adult rat retina. Invest. Ophthalmol. Vis. Sci. 2000;41:2343–2351. PubMed
Chowers I., Wong R., Dentchev T., Farkas R.H., Iacovelli J., Gunatilaka T.L., Medeiros N.E., Presley J.B., Campochiaro P.A., Curcio C.A., et al. The iron carrier transferrin is upregulated in retinas from patients with age-related macular degeneration. Invest. Ophthalmol. Vis. Sci. 2006;47:2135–2140. PubMed
Daruich A., Le Rouzic Q., Jonet L., Naud M.C., Kowalczuk L., Pournaras J.A., Boatright J.H., Thomas A., Turck N., Moulin A., et al. Iron is neurotoxic in retinal detachment and transferrin confers neuroprotection. Sci. Adv. 2019;5:9940. doi: 10.1126/sciadv.aau9940. PubMed DOI PMC
Goralska M., Ferrell J., Harned J., Lall M., Nagar S., Fleisher L.N., McGahan M.C. Iron metabolism in the eye: a review. Exp. Eye Res. 2009;88:204–215. doi: 10.1016/j.exer.2008.10.026. PubMed DOI PMC
Young M.A., Tunstall M.J., Kistler J., Donaldson P.J. Blocking chloride channels in the rat lens: localized changes in tissue hydration support the existence of a circulating chloride flux. Invest. Ophthalmol. Vis. Sci. 2000;41:3049–3055. PubMed
Cao L., Zhang X.D., Liu X.B., Chen T.Y., Zhao M. Chloride channels and transporters in human corneal epithelium. Exp. Eye Res. 2010;90:771–779. doi: 10.1016/j.exer.2010.03.013. PubMed DOI PMC
Li L., Jiao X.D., D'Atri I., Ono F., Nelson R., Chan C.C., Nakaya N., Ma Z.W., Ma Y., Cai X.Y., et al. Mutation in the intracellular chloride channel CLCC1 associated with autosomal recessive retinitis pigmentosa. PLoS Genet. 2018;14 doi: 10.1371/journal.pgen.1007504. PubMed DOI PMC
Gerke V., Moss S.E. Annexins: from structure to function. Physiol. Rev. 2002;82:331–371. doi: 10.1152/physrev.00030.2001. PubMed DOI
Huang B., Blanco G., Mercer R.W., Fleming T., Pepose J.S. Human corneal endothelial cell expression of Na+,K+-adenosine triphosphatase isoforms. Arch. Ophthalmol. 2003;121:840–845. doi: 10.1001/archopht.121.6.840. PubMed DOI
Delamere N.A., Tamiya S. Expression, regulation and function of Na,K-ATPase in the lens. Prog. Retin. Eye Res. 2004;23:593–615. doi: 10.1016/j.preteyeres.2004.06.003. PubMed DOI
Wetzel R.K., Arystarkhova E., Sweadner K.J. Cellular and subcellular specification of Na,K-ATPase alpha and beta isoforms in the postnatal development of mouse retina. J. Neurosci. 1999;19:9878–9889. PubMed PMC
Delamere N.A., Tamiya S. Lens ion transport: from basic concepts to regulation of Na,K-ATPase activity. Exp. Eye Res. 2009;88:140–143. doi: 10.1016/j.exer.2008.05.005. PubMed DOI PMC
Blaustein M.P., Lederer W.J. Sodium calcium exchange: its physiological implications. Physiol. Rev. 1999;79:763–854. doi: 10.1152/physrev.1999.79.3.763. PubMed DOI
Hassan M.T., Lytton J. Potassium-dependent sodium-calcium exchanger (NCKX) isoforms and neuronal function. Cell Calcium. 2020;86 doi: 10.1016/j.ceca.2019.102135. PubMed DOI
Vinberg F., Wang T., Molday R.S., Chen J., Kefalov V.J. A new mouse model for stationary night blindness with mutant Slc24a1 explains the pathophysiology of the associated human disease. Hum. Mol. Genet. 2015;24:5915–5929. doi: 10.1093/hmg/ddv319. PubMed DOI PMC
Vinberg F., Wang T., De Maria A., Zhao H.Q., Bassnett S., Chen J., Kefalov V.J. The Na+/Ca2+, K+ exchanger NCKX4 is required for efficient cone-mediated vision. Elife. 2017;6 doi: 10.7554/eLife.24550. PubMed DOI PMC
Gao J.Y., Minogue P.J., Beyer E.C., Mathias R.T., Berthoud V.M. Disruption of the lens circulation causes calcium accumulation and precipitates in connexin mutant mice. Am J Physiol-Cell Ph. 2018;314:C492–C503. doi: 10.1152/ajpcell.00277.2017. PubMed DOI PMC
Umapathy N.S., Dun Y., Martin P.M., Duplantier J.N., Roon P., Prasad P., Smith S.B., Ganapathy V. Expression and function of system N glutamine transporters (SN1/SN2 or SNAT3/SNAT5) in retinal ganglion cells. Invest. Ophthalmol. Vis. Sci. 2008;49:5151–5160. doi: 10.1167/iovs.08-2245. PubMed DOI PMC
Gaudet P., Livstone M.S., Lewis S.E., Thomas P.D. Phylogenetic-based propagation of functional annotations within the Gene Ontology consortium. Briefings Bioinf. 2011;12:449–462. doi: 10.1093/bib/bbr042. PubMed DOI PMC
Langhauser M., Ustinova J., Rivera-Milla E., Ivannikov D., Seidl C., Slomka C., Finne J., Yoshihara Y., Bastmeyer M., Bentrop J. Ncam1a and Ncam1b: two carriers of polysialic acid with different functions in the developing zebrafish nervous system. Glycobiology. 2012;22:196–209. doi: 10.1093/glycob/cwr129. PubMed DOI
Montenegro-Venegas C., Tortosa E., Rosso S., Peretti D., Bollati F., Bisbal M., Jausoro I., Avila J., Caceres A., Gonzalez-Billault C. MAP1B regulates axonal development by modulating rho-GTPase Rac1 activity. Mol. Biol. Cell. 2010;21:3518–3528. doi: 10.1091/mbc.E09-08-0709. PubMed DOI PMC
Kustermann S., Hildebrandt H., Bolz S., Dengler K., Kohler K. Genesis of rods in the zebrafish retina occurs in a microenvironment provided by polysialic acid-expressing muller glia. J. Comp. Neurol. 2010;518:636–646. doi: 10.1002/cne.22232. PubMed DOI
Ooto S., Hangai M., Tomidokoro A., Saito H., Araie M., Otani T., Kishi S., Matsushita K., Maeda N., Shirakashi M., et al. Effects of age, sex, and axial length on the three-dimensional profile of normal macular layer structures. Invest. Ophthalmol. Vis. Sci. 2011;52:8769–8779. doi: 10.1167/iovs.11-8388. PubMed DOI
Ucuncu E., Rajamani K., Wilson M.S.C., Medina-Cano D., Altin N., David P., Barcia G., Lefort N., Banal C., Vasilache-Dangles M.T., et al. MINPP1 prevents intracellular accumulation of the chelator inositol hexakisphosphate and is mutated in Pontocerebellar Hypoplasia. Nat. Commun. 2020;11:6087. doi: 10.1038/s41467-020-19919-y. PubMed DOI PMC
Kilaparty S.P., Agarwal R., Singh P., Kannan K., Ali N. Endoplasmic reticulum stress-induced apoptosis accompanies enhanced expression of multiple inositol polyphosphate phosphatase 1 (Minpp1): a possible role for Minpp1 in cellular stress response. Cell Stress Chaperones. 2016;21:593–608. doi: 10.1007/s12192-016-0684-6. PubMed DOI PMC
Barsacchi D., Cappiello M., Tozzi M.G., Delcorso A., Peccatori M., Camici M., Ipata P.L., Mura U. Purine nucleoside phosphorylase from bovine lens - purification and properties. Biochim. Biophys. Acta. 1992;1160:163–170. doi: 10.1016/0167-4838(92)90003-V. PubMed DOI
Pena-Altamira L.E., Polazzi E., Giuliani P., Beraudi A., Massenzio F., Mengoni I., Poli A., Zuccarini M., Ciccarelli R., Di Iorio P., et al. Release of soluble and vesicular purine nucleoside phosphorylase from rat astrocytes and microglia induced by pro-inflammatory stimulation with extracellular ATP via P2X(7) receptors. Neurochem. Int. 2018;115:37–49. PubMed
Curran K., Lister J.A., Kunkel G.R., Prendergast A., Parichy D.M., Raible D.W. Interplay between Foxd3 and Mitf regulates cell fate plasticity in the zebrafish neural crest. Dev. Biol. 2010;344:107–118. doi: 10.1016/j.ydbio.2010.04.023. PubMed DOI PMC
Sanderson J., Dartt D.A., Trinkaus-Randall V., Pintor J., Civan M.M., Delamere N.A., Fletcher E.L., Salt T.E., Grosche A., Mitchell C.H. Purines in the eye: recent evidence for the physiological and pathological role of purines in the RPE, retinal neurons, astrocytes, Muller cells, lens, trabecular meshwork, cornea and lacrimal gland. Exp. Eye Res. 2014;127:270–279. doi: 10.1016/j.exer.2014.08.009. PubMed DOI PMC
Hu M.J., Bai Y., Zhang C.X., Liu F., Cui Z.B., Chen J., Peng J.R. Liver-enriched gene 1, a glycosylated secretory protein, binds to FGFR and mediates an anti-stress pathway to protect liver development in zebrafish. PLoS Genet. 2016;12 doi: 10.1371/journal.pgen.1005881. PubMed DOI PMC
Dang Y.N., Wang J.Y., Chen L., Kun Z., Peng J.R., Jin H. Evolutionary and molecular characterization of liver-enriched gene 1. Sci Rep-Uk. 2020;10 PubMed PMC
Wright F.A., Bonzerato C.G., Sliter D.A., Wojcikiewicz R.J.H. The erlin2 T65I mutation inhibits erlin1/2 complex-mediated inositol 1,4,5-trisphosphate receptor ubiquitination and phosphatidylinositol 3-phosphate binding. J. Biol. Chem. 2018;293:15706–15714. doi: 10.1074/jbc.RA118.004547. PubMed DOI PMC
Huber M.D., Vesely P.W., Datta K., Gerace L. Erlins restrict SREBP activation in the ER and regulate cellular cholesterol homeostasis. J. Cell Biol. 2013;203:427–436. doi: 10.1083/jcb.201305076. PubMed DOI PMC
Laver C.R.J., Taylor J.S. RT-qPCR reveals opsin gene upregulation associated with age and sex in guppies (Poecilia reticulata)-a species with color-based sexual selection and 11 visual-opsin genes. BMC Evol. Biol. 2011;11:81. doi: 10.1186/1471-2148-11-81. PubMed DOI PMC
Perez-Riverol Y., Bai J.W., Bandla C., Garcia-Seisdedos D., Hewapathirana S., Kamatchinathan S., Kundu D.J., Prakash A., Frericks-Zipper A., Eisenacher M., et al. The PRIDE database resources in 2022: a hub for mass spectrometry-based proteomics evidences. Nucleic Acids Res. 2022;50:D543–D552. doi: 10.1093/nar/gkab1038. PubMed DOI PMC