{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,3]],"date-time":"2026-07-03T03:50:39Z","timestamp":1783050639507,"version":"3.54.6"},"reference-count":62,"publisher":"Public Library of Science (PLoS)","issue":"3","license":[{"start":{"date-parts":[[2014,3,26]],"date-time":"2014-03-26T00:00:00Z","timestamp":1395792000000},"content-version":"unspecified","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/publicdomain\/zero\/1.0\/"}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"DOI":"10.1371\/journal.pone.0093274","type":"journal-article","created":{"date-parts":[[2014,3,26]],"date-time":"2014-03-26T16:53:34Z","timestamp":1395852814000},"page":"e93274","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":79,"title":["Melanopsin Ganglion Cells Are the Most Resistant Retinal Ganglion Cell Type to Axonal Injury in the Rat Retina"],"prefix":"10.1371","volume":"9","author":[{"given":"Luis","family":"P\u00e9rez de Sevilla M\u00fcller","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Allison","family":"Sargoy","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Allen R.","family":"Rodriguez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nicholas C.","family":"Brecha","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2014,3,26]]},"reference":[{"key":"ref1","doi-asserted-by":"crossref","first-page":"262","DOI":"10.1136\/bjo.2005.081224","article-title":"The number of people with glaucoma worldwide in 2010 and 2020","volume":"90","author":"HA Quigley","year":"2006","journal-title":"Br J Ophthalmol"},{"key":"ref2","doi-asserted-by":"crossref","first-page":"4368","DOI":"10.1523\/JNEUROSCI.14-07-04368.1994","article-title":"Axotomy results in delayed death and apoptosis of retinal ganglion cells in adult rats","volume":"14","author":"M Berkelaar","year":"1994","journal-title":"J Neurosci"},{"key":"ref3","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1016\/0169-328X(94)90116-3","article-title":"Immediate early gene expression in axotomized and regenerating retinal ganglion cells of the adult rat","volume":"24","author":"GA Robinson","year":"1994","journal-title":"Brain Res Mol Brain Res"},{"key":"ref4","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1523\/JNEUROSCI.08-01-00265.1988","article-title":"Influences of peripheral nerve grafts on the survival and regrowth of axotomized retinal ganglion cells in adult rats","volume":"8","author":"MP Villegas-P\u00e9rez","year":"1988","journal-title":"J Neurosci"},{"key":"ref5","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1002\/neu.480240103","article-title":"Rapid and protracted phases of retinal ganglion cell loss follow axotomy in the optic nerve of adult rats","volume":"24","author":"MP Villegas-P\u00e9rez","year":"1993","journal-title":"J Neurobiol"},{"key":"ref6","doi-asserted-by":"crossref","first-page":"1735","DOI":"10.1111\/j.1460-9568.1996.tb01317.x","article-title":"Long-term survival of retinal ganglion cells following optic nerve section in adult bcl-2 transgenic mice","volume":"8","author":"MC Cenni","year":"1996","journal-title":"Eur J Neurosci"},{"key":"ref7","doi-asserted-by":"crossref","first-page":"304","DOI":"10.1016\/0006-8993(93)90695-J","article-title":"Intravitreal injections of neurotrophic factors support the survival of axotomized retinal ganglion cells in adult rats in vivo","volume":"602","author":"J Mey","year":"1993","journal-title":"Brain Res"},{"key":"ref8","doi-asserted-by":"crossref","unstructured":"Rodriguez A, P\u00e9rez de Sevilla L, Brecha N (in press) The RNA binding protein RBPMS is a selective marker of ganglion cells in the mammalian retina. J Comp Neurol.","DOI":"10.1002\/cne.23521"},{"key":"ref9","doi-asserted-by":"crossref","first-page":"1052","DOI":"10.1167\/iovs.09-4098","article-title":"RNA binding protein with multiple splicing: a new marker for retinal ganglion cells","volume":"51","author":"JM Kwong","year":"2010","journal-title":"Invest Ophthalmol Vis Sci"},{"key":"ref10","doi-asserted-by":"crossref","first-page":"624","DOI":"10.1038\/309624a0","article-title":"Antibodies to heavy neurofilament subunit detect a subpopulation of damaged ganglion cells in retina","volume":"309","author":"UC Drager","year":"1984","journal-title":"Nature"},{"key":"ref11","first-page":"95","article-title":"The intermediate filament complement of the retina: a comparison between different mammalian species","volume":"33","author":"G Shaw","year":"1984","journal-title":"Eur J Cell Biol"},{"key":"ref12","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1016\/0006-8993(92)90325-4","article-title":"A neurofilament protein antibody selectively labels a large ganglion cell type in the human retina","volume":"582","author":"C Straznicky","year":"1992","journal-title":"Brain Res"},{"key":"ref13","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1016\/0306-4522(92)90077-F","article-title":"The neurofilament triplet is present in distinct subpopulations of neurons in the central nervous system of the guinea-pig","volume":"49","author":"JC Vickers","year":"1992","journal-title":"Neurosci"},{"key":"ref14","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1167\/iovs.02-0333","article-title":"Varicosities of intraretinal ganglion cell axons in human and nonhuman primates","volume":"44","author":"L Wang","year":"2003","journal-title":"Invest Ophthalmol Vis Sci"},{"key":"ref15","doi-asserted-by":"crossref","first-page":"483","DOI":"10.1017\/S0952523802194107","article-title":"Large-scale morphological survey of rat retinal ganglion cells","volume":"19","author":"W Sun","year":"2002","journal-title":"Vis Neurosci"},{"key":"ref16","doi-asserted-by":"crossref","first-page":"2813","DOI":"10.1016\/0306-4522(82)90104-X","article-title":"Ganglion cell death within the developing retina: a regulatory role for retinal dendrites","volume":"7","author":"R Linden","year":"1982","journal-title":"Neurosci"},{"key":"ref17","doi-asserted-by":"crossref","first-page":"683","DOI":"10.1038\/297683a0","article-title":"Evidence for dendritic competition in the developing retina","volume":"297","author":"VH Perry","year":"1982","journal-title":"Nature"},{"key":"ref18","doi-asserted-by":"crossref","first-page":"1065","DOI":"10.1126\/science.1069609","article-title":"Melanopsin-containing retinal ganglion cells: Architecture, projections, and intrinsic photosensitivity","volume":"295","author":"S Hattar","year":"2002","journal-title":"Science"},{"key":"ref19","doi-asserted-by":"crossref","first-page":"1763","DOI":"10.1111\/j.1460-9568.2008.06149.x","article-title":"Two types of melanopsin retinal ganglion cell differentially innervate the hypothalamic suprachiasmatic nucleus and the olivary pretectal nucleus","volume":"27","author":"SB Baver","year":"2008","journal-title":"Eur J Neurosci"},{"key":"ref20","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1002\/cne.22103","article-title":"Immunotoxin-induced ablation of melanopsin retinal ganglion cells in a non-murine mammalian model","volume":"516","author":"ES Ingham","year":"2009","journal-title":"J Comp Neurol"},{"key":"ref21","doi-asserted-by":"crossref","first-page":"241","DOI":"10.1089\/108076802760116160","article-title":"Brain-derived neurotrophic factor inhibits changes in soma-size of retinal ganglion cells following optic nerve axotomy in rats","volume":"18","author":"T Ota","year":"2002","journal-title":"J Ocul Pharmacol Ther"},{"key":"ref22","first-page":"285","article-title":"Ganglion cell distribution in the retina of the mouse","volume":"20","author":"UC Drager","year":"1981","journal-title":"Invest Ophthalmol Vis Sci"},{"key":"ref23","doi-asserted-by":"crossref","first-page":"4886","DOI":"10.1167\/iovs.10-5921","article-title":"Morphology and immunoreactivity of retrogradely double-labeled ganglion cells in the mouse retina","volume":"52","author":"JJ Pang","year":"2011","journal-title":"Invest Ophthalmol Vis Sci"},{"key":"ref24","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1016\/0304-3940(86)90315-0","article-title":"Displaced retinal ganglion cells in normal rats and rats with one eye enucleated at birth","volume":"67","author":"ZH Liu","year":"1986","journal-title":"Neurosci Lett"},{"key":"ref25","doi-asserted-by":"crossref","first-page":"483","DOI":"10.1007\/BF00235279","article-title":"Electroretinographic responses and retrograde changes of retinal morphology after intracranial optic nerve section: a quantitative analysis in the cat","volume":"55","author":"H Holl\u00e4nder","year":"1984","journal-title":"Exp Brain Res"},{"key":"ref26","doi-asserted-by":"crossref","first-page":"2105","DOI":"10.1523\/JNEUROSCI.13-05-02105.1993","article-title":"Number, distribution, and morphology of retinal ganglion cells with axons regenerated into peripheral nerve grafts in adult cats","volume":"13","author":"M Watanabe","year":"1993","journal-title":"J Neurosci"},{"key":"ref27","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1007\/BF01183863","article-title":"The ganglion cell response to optic nerve injury in the cat: differential responses revealed by neurofibrillar staining","volume":"23","author":"LC Silveira","year":"1994","journal-title":"J Neurocytol"},{"key":"ref28","doi-asserted-by":"crossref","first-page":"2667","DOI":"10.1016\/j.visres.2004.06.010","article-title":"Axotomized mouse retinal ganglion cells containing melanopsin show enhanced survival, but not enhanced axon regrowth into a peripheral nerve graft","volume":"44","author":"A Robinson","year":"2004","journal-title":"Vision Res"},{"key":"ref29","doi-asserted-by":"crossref","first-page":"2951","DOI":"10.1167\/iovs.05-1295","article-title":"Melanopsin-expressing retinal ganglion cells are more injury-resistant in a chronic ocular hypertension model","volume":"47","author":"RS Li","year":"2006","journal-title":"Invest Ophthalmol Vis Sci"},{"key":"ref30","first-page":"2814","article-title":"Intrinsically photosensitive retinal ganglion cells are resistant to N-methyl-D-aspartic acid excitotoxicity","volume":"18","author":"S Deparis","year":"2012","journal-title":"Mol Vis"},{"key":"ref31","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1016\/j.neuron.2010.05.023","article-title":"Melanopsin-expressing retinal ganglion-cell photoreceptors: cellular diversity and role in pattern vision","volume":"67","author":"JL Ecker","year":"2010","journal-title":"Neuron"},{"key":"ref32","first-page":"281","article-title":"Photon capture and signalling by melanopsin retinal ganglion cells","volume":"457","author":"MT Do","year":"2008","journal-title":"Nature"},{"key":"ref33","doi-asserted-by":"crossref","first-page":"371","DOI":"10.1152\/jn.00062.2008","article-title":"Intrinsic and extrinsic light responses in melanopsin-expressing ganglion cells during mouse development","volume":"100","author":"TM Schmidt","year":"2008","journal-title":"J Neurophysiol"},{"key":"ref34","doi-asserted-by":"crossref","first-page":"13608","DOI":"10.1523\/JNEUROSCI.1422-12.2012","article-title":"Form and function of the M4 cell, an intrinsically photosensitive retinal ganglion cell type contributing to geniculocortical vision","volume":"32","author":"ME Estevez","year":"2012","journal-title":"J Neurosci"},{"key":"ref35","first-page":"311","article-title":"Modulation of retinal dopaminergic cells by nitric oxide. A protective effect on NMDA-induced retinal injury","volume":"18","author":"Y Kitaoka","year":"2004","journal-title":"In Vivo"},{"key":"ref36","doi-asserted-by":"crossref","first-page":"e455","DOI":"10.1038\/cddis.2012.194","article-title":"Dopamine protects neurons against glutamate-induced excitotoxicity","volume":"4","author":"A Vaarmann","year":"2013","journal-title":"Cell Death Dis"},{"key":"ref37","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1016\/j.expneurol.2007.01.032","article-title":"Dopamine neurones form a discrete plexus with melanopsin cells in normal and degenerating retina","volume":"205","author":"AA Vugler","year":"2007","journal-title":"Exp Neurol"},{"key":"ref38","first-page":"1","article-title":"Recurrent axon collaterals of intrinsically photosensitive retinal ganglion cells","volume":"9","author":"HR Joo","year":"2013","journal-title":"Vis Neurosci"},{"key":"ref39","doi-asserted-by":"crossref","first-page":"116","DOI":"10.1038\/nn.2255","article-title":"Laminar and compartmental regulation of dendritic growth in mature cortex","volume":"12","author":"DK Chow","year":"2009","journal-title":"Nat Neurosci"},{"key":"ref40","doi-asserted-by":"crossref","first-page":"9149","DOI":"10.1073\/pnas.1119449109","article-title":"Full-length axon regeneration in the adult mouse optic nerve and partial recovery of simple visual behaviors","volume":"109","author":"S de Lima","year":"2012","journal-title":"Proc Natl Acad Sci USA"},{"key":"ref41","doi-asserted-by":"crossref","first-page":"1379","DOI":"10.1093\/carcin\/bgm052","article-title":"PTEN, more than the AKT pathway","volume":"28","author":"C Blanco-Aparicio","year":"2007","journal-title":"Carcinogenesis"},{"key":"ref42","doi-asserted-by":"crossref","first-page":"372","DOI":"10.1038\/nature10594","article-title":"Sustained axon regeneration induced by co-deletion of PTEN and SOCS3","volume":"480","author":"F Sun","year":"2011","journal-title":"Nature Letters"},{"key":"ref43","doi-asserted-by":"crossref","first-page":"338","DOI":"10.1038\/nature11861","article-title":"mTOR is a key modulator of ageing and age-related disease","volume":"493","author":"CS Johnson","year":"2013","journal-title":"Nature"},{"key":"ref44","doi-asserted-by":"crossref","first-page":"599","DOI":"10.1038\/376599a0","article-title":"Protein kinase B (c-Akt) in phosphatidylinositol-3-OH kinase signal transduction","volume":"376","author":"BM Burgering","year":"1995","journal-title":"Nature"},{"key":"ref45","doi-asserted-by":"crossref","first-page":"727","DOI":"10.1016\/0092-8674(95)90534-0","article-title":"The protein kinase encoded by the Akt proto-oncogene is a target of the PDGF-activated phosphatidylinositol 3-kinase","volume":"81","author":"TF Franke","year":"1995","journal-title":"Cell"},{"key":"ref46","doi-asserted-by":"crossref","first-page":"435","DOI":"10.1016\/S0092-8674(00)81883-8","article-title":"PI3K: downstream AKTion blocks apoptosis","volume":"88","author":"TF Franke","year":"1997","journal-title":"Cell"},{"key":"ref47","doi-asserted-by":"crossref","first-page":"294","DOI":"10.1006\/nbdi.2002.0482","article-title":"Akt phosphorylation and neuronal survival after traumatic brain injury in mice","volume":"9","author":"N Noshita","year":"2002","journal-title":"Neurobiol Dis"},{"key":"ref48","doi-asserted-by":"crossref","first-page":"1095","DOI":"10.1007\/s10571-008-9286-x","article-title":"Enhanced survival of melanopsin-expressing retinal ganglion cells after injury is associated with the PI3 K\/Akt pathway","volume":"28","author":"SY Li","year":"2008","journal-title":"Cell Mol Neurobiol"},{"key":"ref49","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1111\/j.1476-5381.2008.00020.x","article-title":"Inhibition of the phosphatase PTEN protects mice against oleic acid-induced acute lung injury","volume":"156","author":"JP Lai","year":"2009","journal-title":"Br J Pharmacol"},{"key":"ref50","doi-asserted-by":"crossref","first-page":"13765","DOI":"10.1523\/JNEUROSCI.5114-08.2008","article-title":"Leukemia inhibitory factor extends the lifespan of injured photoreceptors in vivo","volume":"28","author":"S Joly","year":"2008","journal-title":"J Neurosci"},{"key":"ref51","doi-asserted-by":"crossref","first-page":"991","DOI":"10.1016\/j.exer.2008.03.020","article-title":"STAT3 activation protects retinal ganglion cell layer neurons in response to stress","volume":"86","author":"C Zhang","year":"2008","journal-title":"Exp Eye Res"},{"key":"ref52","doi-asserted-by":"crossref","unstructured":"Rane SG, Reddy EP (2000) Janus kinases: components of multiple signaling pathways. Oncogene 19: 5662\u20135679. Review.","DOI":"10.1038\/sj.onc.1203925"},{"key":"ref53","doi-asserted-by":"crossref","first-page":"482","DOI":"10.1007\/s12031-012-9762-0","article-title":"PACAP is an endogenous protective factor-insights from PACAP-deficient mice","volume":"48","author":"D Reglodi","year":"2012","journal-title":"J Mol Neurosci"},{"key":"ref54","first-page":"4202","article-title":"Melanopsin is expressed in PACAP-containing retinal ganglion cells of the human retinohypothalamic tract. Invest Ophthalmol Vis Sci","volume":"45","author":"J Hannibal","year":"2004"},{"key":"ref55","doi-asserted-by":"crossref","unstructured":"Krysko DV, Leybaert L, Vandenabeele P, D'Herde K (2005) Gap junctions and the propagation of cell survival and cell death signals. Apoptosis. 10: 459\u2013469. Review.","DOI":"10.1007\/s10495-005-1875-2"},{"key":"ref56","doi-asserted-by":"crossref","unstructured":"Rodr\u00edguez-Sinovas A, Cabestrero A, L\u00f3pez D, Torre I, Morente M, et al. (2007) The modulatory effects of connexin 43 on cell death\/survival beyond cell coupling. Prog Biophys Mol Biol 94: 219\u2013232. Review.","DOI":"10.1016\/j.pbiomolbio.2007.03.003"},{"key":"ref57","doi-asserted-by":"crossref","first-page":"e584","DOI":"10.1038\/cddis.2013.105","article-title":"Gap junctional communication promotes apoptosis in a connexin-type-dependent manner","volume":"4","author":"P Kameritsch","year":"2013","journal-title":"Cell Death Dis"},{"key":"ref58","doi-asserted-by":"crossref","first-page":"911","DOI":"10.1002\/cne.22254","article-title":"Connexin36 is required for gap junctional coupling of most ganglion cell subtypes in the mouse retina","volume":"518","author":"F Pan","year":"2010","journal-title":"J Comp Neurol"},{"key":"ref59","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1002\/cne.20621","article-title":"Connexin45 mediates gap junctional coupling of bistratified ganglion cells in the mouse retina","volume":"490","author":"T Schubert","year":"2005","journal-title":"J Comp Neurol"},{"key":"ref60","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1017\/S0952523810000131","article-title":"Expression and modulation of connexin 30.2, a novel gap junction protein in the mouse retina","volume":"27","author":"L P\u00e9rez de Sevilla M\u00fcller","year":"2010","journal-title":"Vis Neurosci"},{"key":"ref61","doi-asserted-by":"crossref","first-page":"4813","DOI":"10.1002\/cne.22490","article-title":"Tracer coupling of intrinsically photosensitive retinal ganglion cells to amacrine cells in the mouse retina","volume":"518","author":"L P\u00e9rez de Sevilla M\u00fcller","year":"2010","journal-title":"J Comp Neurol"},{"issue":"103","key":"ref62","doi-asserted-by":"crossref","first-page":"5959","DOI":"10.1073\/pnas.0508512103","article-title":"Connexin30.2 containing gap junction channels decelerate impulse propagation through the atrioventricular node","volume":"A","author":"MM Kreuzberg","year":"2006","journal-title":"Proc Natl Acad Sci U S"}],"container-title":["PLoS ONE"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/dx.plos.org\/10.1371\/journal.pone.0093274","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2019,8,8]],"date-time":"2019-08-08T19:30:15Z","timestamp":1565292615000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0093274"}},"subtitle":[],"editor":[{"given":"Gianluca","family":"Tosini","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2014,3,26]]},"references-count":62,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2014,3,26]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0093274","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2014,3,26]]}}}