{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,6]],"date-time":"2026-02-06T01:05:01Z","timestamp":1770339901956,"version":"3.49.0"},"reference-count":83,"publisher":"Wiley","issue":"1","license":[{"start":{"date-parts":[[2015,6,25]],"date-time":"2015-06-25T00:00:00Z","timestamp":1435190400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/onlinelibrary.wiley.com\/termsAndConditions#vor"}],"funder":[{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"crossref","award":["RO1 EY022030-03"],"award-info":[{"award-number":["RO1 EY022030-03"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["J of Comparative Neurology"],"published-print":{"date-parts":[[2016,1]]},"abstract":"<jats:title>ABSTRACT<\/jats:title><jats:p>Retinal progenitors in the circumferential marginal zone (CMZ) and M\u00fcller glia\u2010derived progenitors have been well described for the eyes of fish, amphibians, and birds. However, there is no information regarding a CMZ and the nature of retinal glia in species phylogenetically bridging amphibians and birds. The purpose of this study was to examine the retinal glia and investigate whether a CMZ is present in the eyes of reptilian species. We used immunohistochemical analyses to study retinal glia, neurons that could influence CMZ progenitors, the retinal margin, and the nonpigmented epithelium of ciliary body of garter snakes, queen snakes, anole lizards, snapping turtles, and painted turtles. We compare our observations on reptile eyes to the CMZ and glia of fish, amphibians, and birds. In all species, Sox9, Pax6, and the glucocorticoid receptor are expressed by M\u00fcller glia and cells at the retinal margin. However, proliferating cells were found only in the CMZ of turtles and not in the eyes of anoles and snakes. Similar to eyes of chickens, the retinal margin in turtles contains accumulations of GLP1\/glucagonergic neurites. We find that filamentous proteins, vimentin and GFAP, are expressed by M\u00fcller glia, but have different patterns of subcellular localization in the different species of reptiles. We provide evidence that the reptile retina may contain nonastrocytic inner retinal glial cells, similar to those described in the avian retina. We conclude that the retinal glia, glucagonergic neurons, and CMZ of turtles appear to be most similar to those of fish, amphibians, and birds. J. Comp. Neurol. 524:74\u201389, 2016. \u00a9 2015 Wiley Periodicals, Inc.<\/jats:p>","DOI":"10.1002\/cne.23823","type":"journal-article","created":{"date-parts":[[2015,6,6]],"date-time":"2015-06-06T09:31:15Z","timestamp":1433583075000},"page":"74-89","source":"Crossref","is-referenced-by-count":30,"title":["Comparative analysis of glucagonergic cells, glia, and the circumferential marginal zone in the reptilian retina"],"prefix":"10.1002","volume":"524","author":[{"given":"Levi","family":"Todd","sequence":"first","affiliation":[{"name":"Department of Neuroscience College of Medicine, The Ohio State University Columbus Ohio 43210"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Lilianna","family":"Suarez","sequence":"additional","affiliation":[{"name":"Department of Neuroscience College of Medicine, The Ohio State University Columbus Ohio 43210"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Natalie","family":"Squires","sequence":"additional","affiliation":[{"name":"Department of Neuroscience College of Medicine, The Ohio State University Columbus Ohio 43210"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Christopher Paul","family":"Zelinka","sequence":"additional","affiliation":[{"name":"Department of Biological Science Florida State University Tallahassee Florida 32306"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Kevin","family":"Gribbins","sequence":"additional","affiliation":[{"name":"Department of Biology University of Indianapolis Indianapolis IN 47201"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Andy J.","family":"Fischer","sequence":"additional","affiliation":[{"name":"Department of Neuroscience College of Medicine, The Ohio State University Columbus Ohio 43210"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"311","published-online":{"date-parts":[[2015,6,25]]},"reference":[{"key":"e_1_2_9_2_1","doi-asserted-by":"publisher","DOI":"10.1002\/cne.902640203"},{"key":"e_1_2_9_3_1","doi-asserted-by":"publisher","DOI":"10.1002\/dvdy.22309"},{"key":"e_1_2_9_4_1","volume-title":"Brain peptides","author":"Brecha NC","year":"1983"},{"key":"e_1_2_9_5_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00441-011-1211-9"},{"key":"e_1_2_9_6_1","doi-asserted-by":"publisher","DOI":"10.1186\/1741-7007-10-65"},{"key":"e_1_2_9_7_1","doi-asserted-by":"publisher","DOI":"10.1002\/cne.23307"},{"key":"e_1_2_9_8_1","doi-asserted-by":"publisher","DOI":"10.1098\/rsbl.2012.0331"},{"key":"e_1_2_9_9_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.76.7.3532"},{"key":"e_1_2_9_10_1","doi-asserted-by":"publisher","DOI":"10.1002\/cne.902900308"},{"key":"e_1_2_9_11_1","doi-asserted-by":"publisher","DOI":"10.1002\/cne.902390107"},{"key":"e_1_2_9_12_1","doi-asserted-by":"publisher","DOI":"10.1177\/37.8.2569003"},{"key":"e_1_2_9_13_1","doi-asserted-by":"publisher","DOI":"10.1017\/S0952523802196064"},{"key":"e_1_2_9_14_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.jchemneu.2009.10.001"},{"key":"e_1_2_9_15_1","doi-asserted-by":"publisher","DOI":"10.1111\/ede.12081"},{"key":"e_1_2_9_16_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.preteyeres.2004.07.003"},{"key":"e_1_2_9_17_1","doi-asserted-by":"publisher","DOI":"10.1007\/s12035-010-8152-2"},{"key":"e_1_2_9_18_1","doi-asserted-by":"publisher","DOI":"10.1002\/cne.20406"},{"key":"e_1_2_9_19_1","doi-asserted-by":"publisher","DOI":"10.1006\/dbio.2000.9640"},{"key":"e_1_2_9_20_1","doi-asserted-by":"publisher","DOI":"10.1038\/85090"},{"key":"e_1_2_9_21_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0012-1606(03)00178-7"},{"key":"e_1_2_9_22_1","doi-asserted-by":"publisher","DOI":"10.1038\/11167"},{"key":"e_1_2_9_23_1","doi-asserted-by":"publisher","DOI":"10.1242\/dev.129.9.2283"},{"key":"e_1_2_9_24_1","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.3247-05.2005"},{"key":"e_1_2_9_25_1","doi-asserted-by":"publisher","DOI":"10.1002\/cne.20937"},{"key":"e_1_2_9_26_1","doi-asserted-by":"publisher","DOI":"10.1002\/cne.21404"},{"key":"e_1_2_9_27_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.ydbio.2008.02.023"},{"key":"e_1_2_9_28_1","doi-asserted-by":"publisher","DOI":"10.1002\/glia.20743"},{"key":"e_1_2_9_29_1","doi-asserted-by":"publisher","DOI":"10.1002\/glia.20950"},{"key":"e_1_2_9_30_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0010774"},{"key":"e_1_2_9_31_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.exer.2013.08.018"},{"key":"e_1_2_9_32_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.exer.2013.06.019"},{"key":"e_1_2_9_33_1","doi-asserted-by":"publisher","DOI":"10.1242\/dev.109835"},{"key":"e_1_2_9_34_1","doi-asserted-by":"publisher","DOI":"10.1007\/BF01260995"},{"key":"e_1_2_9_35_1","doi-asserted-by":"publisher","DOI":"10.1006\/dbio.1997.8542"},{"key":"e_1_2_9_36_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.brainres.2007.01.105"},{"key":"e_1_2_9_37_1","doi-asserted-by":"publisher","DOI":"10.1038\/nrn3723"},{"key":"e_1_2_9_38_1","first-page":"3511","article-title":"DNA damage and repair in light\u2010induced photoreceptor degeneration","volume":"43","author":"Gordon WC","year":"2002","journal-title":"Invest Ophthalmol Vis Sci"},{"key":"e_1_2_9_39_1","doi-asserted-by":"publisher","DOI":"10.1038\/320447a0"},{"key":"e_1_2_9_40_1","doi-asserted-by":"publisher","DOI":"10.1002\/cne.20996"},{"key":"e_1_2_9_41_1","doi-asserted-by":"publisher","DOI":"10.1016\/0166-2236(92)90020-9"},{"key":"e_1_2_9_42_1","doi-asserted-by":"publisher","DOI":"10.1016\/0012-1606(68)90041-9"},{"key":"e_1_2_9_43_1","doi-asserted-by":"publisher","DOI":"10.1016\/0012-1606(71)90098-4"},{"key":"e_1_2_9_44_1","doi-asserted-by":"publisher","DOI":"10.1002\/cne.901760304"},{"key":"e_1_2_9_45_1","doi-asserted-by":"publisher","DOI":"10.1016\/0042-6989(83)90033-0"},{"key":"e_1_2_9_46_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0925-4773(97)00097-X"},{"key":"e_1_2_9_47_1","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.130.1.67"},{"key":"e_1_2_9_48_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0165-3806(01)00287-5"},{"key":"e_1_2_9_49_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0092-8674(01)00295-1"},{"key":"e_1_2_9_50_1","doi-asserted-by":"publisher","DOI":"10.1002\/ar.1091840109"},{"key":"e_1_2_9_51_1","doi-asserted-by":"publisher","DOI":"10.1097\/ICO.0b013e3181f2d578"},{"key":"e_1_2_9_52_1","first-page":"961","article-title":"The 2M6 antigen is a Muller cell\u2010specific intracellular membrane\u2010associated protein of the sarcolemmal\u2010membrane\u2010associated protein family and is also TopAP","volume":"16","author":"Ochrietor JD","year":"2010","journal-title":"Mol Vis"},{"key":"e_1_2_9_53_1","doi-asserted-by":"publisher","DOI":"10.1002\/cne.21259"},{"key":"e_1_2_9_54_1","doi-asserted-by":"publisher","DOI":"10.1006\/dbio.1998.8939"},{"key":"e_1_2_9_55_1","doi-asserted-by":"publisher","DOI":"10.1002\/cne.21746"},{"key":"e_1_2_9_56_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1460-9568.1991.tb00843.x"},{"key":"e_1_2_9_57_1","first-page":"171","article-title":"Retinal regeneration in teleost fish","volume":"160","author":"Raymond PA","year":"1991","journal-title":"Ciba Found Symp"},{"key":"e_1_2_9_58_1","first-page":"171","article-title":"Retinal regeneration: common principles but a diversity of mechanisms","volume":"72","author":"Raymond PA","year":"1997","journal-title":"Adv Neurol"},{"key":"e_1_2_9_59_1","doi-asserted-by":"publisher","DOI":"10.1186\/1471-213X-6-36"},{"key":"e_1_2_9_60_1","doi-asserted-by":"crossref","first-page":"3317","DOI":"10.1523\/JNEUROSCI.07-10-03317.1987","article-title":"Cell\u2010specific regulation of neuronal production in the larval frog retina","volume":"7","author":"Reh TA","year":"1987","journal-title":"J Neurosci"},{"key":"e_1_2_9_61_1","doi-asserted-by":"publisher","DOI":"10.1002\/(SICI)1097-4695(199808)36:2<206::AID-NEU8>3.0.CO;2-5"},{"key":"e_1_2_9_62_1","first-page":"2440","article-title":"The chicken cornea as a model of wound healing and neuronal re\u2010innervation","volume":"17","author":"Ritchey ER","year":"2011","journal-title":"Mol Vis"},{"key":"e_1_2_9_63_1","doi-asserted-by":"publisher","DOI":"10.1002\/cne.22444"},{"key":"e_1_2_9_64_1","doi-asserted-by":"publisher","DOI":"10.1002\/cne.23034"},{"key":"e_1_2_9_65_1","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.3456-09.2010"},{"key":"e_1_2_9_66_1","doi-asserted-by":"publisher","DOI":"10.1016\/0165-3806(91)90100-W"},{"key":"e_1_2_9_67_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.ydbio.2008.03.041"},{"key":"e_1_2_9_68_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.ydbio.2009.05.579"},{"key":"e_1_2_9_69_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.ydbio.2008.02.055"},{"key":"e_1_2_9_70_1","doi-asserted-by":"publisher","DOI":"10.1167\/iovs.09-4447"},{"key":"e_1_2_9_71_1","doi-asserted-by":"publisher","DOI":"10.1002\/cne.22335"},{"key":"e_1_2_9_72_1","doi-asserted-by":"publisher","DOI":"10.1002\/1096-9861(20010319)431:4<363::AID-CNE1076>3.0.CO;2-7"},{"key":"e_1_2_9_73_1","first-page":"67","article-title":"The growth of the retina in Xenopus laevis: an autoradiographic study","volume":"26","author":"Straznicky K","year":"1971","journal-title":"J Embryol Exp Morphol"},{"key":"e_1_2_9_74_1","doi-asserted-by":"publisher","DOI":"10.1002\/cne.902740106"},{"key":"e_1_2_9_75_1","doi-asserted-by":"publisher","DOI":"10.1167\/iovs.04-1026"},{"key":"e_1_2_9_76_1","doi-asserted-by":"publisher","DOI":"10.1167\/iovs.04-1027"},{"key":"e_1_2_9_77_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.ydbio.2005.02.010"},{"key":"e_1_2_9_78_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.2449732"},{"key":"e_1_2_9_79_1","doi-asserted-by":"publisher","DOI":"10.1017\/S0952523800011603"},{"key":"e_1_2_9_80_1","doi-asserted-by":"publisher","DOI":"10.1002\/cne.1401"},{"key":"e_1_2_9_81_1","doi-asserted-by":"publisher","DOI":"10.1038\/ng0195-15"},{"key":"e_1_2_9_82_1","doi-asserted-by":"publisher","DOI":"10.1007\/s001140100228"},{"key":"e_1_2_9_83_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0044477"},{"key":"e_1_2_9_84_1","doi-asserted-by":"publisher","DOI":"10.1242\/dev.00723"}],"container-title":["Journal of Comparative Neurology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.wiley.com\/onlinelibrary\/tdm\/v1\/articles\/10.1002%2Fcne.23823","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.wiley.com\/onlinelibrary\/tdm\/v1\/articles\/10.1002%2Fcne.23823","content-type":"unspecified","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1002\/cne.23823","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,10,7]],"date-time":"2023-10-07T03:19:04Z","timestamp":1696648744000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1002\/cne.23823"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2015,6,25]]},"references-count":83,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2016,1]]}},"alternative-id":["10.1002\/cne.23823"],"URL":"https:\/\/doi.org\/10.1002\/cne.23823","archive":["Portico"],"relation":{},"ISSN":["0021-9967","1096-9861"],"issn-type":[{"value":"0021-9967","type":"print"},{"value":"1096-9861","type":"electronic"}],"subject":[],"published":{"date-parts":[[2015,6,25]]}}}