{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,18]],"date-time":"2026-08-18T04:36:52Z","timestamp":1787027812554,"version":"build-2736575974"},"reference-count":92,"publisher":"MDPI AG","issue":"8","license":[{"start":{"date-parts":[[2023,4,14]],"date-time":"2023-04-14T00:00:00Z","timestamp":1681430400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100006769","name":"RSF","doi-asserted-by":"publisher","award":["22-25-00656"],"award-info":[{"award-number":["22-25-00656"]}],"id":[{"id":"10.13039\/501100006769","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Cells"],"abstract":"<jats:p>cAMP is a key regulatory molecule that controls many important processes in the retina, including phototransduction, cell development and death, growth of neural processes, intercellular contacts, retinomotor effects, and so forth. The total content of cAMP changes in the retina in a circadian manner following the natural light cycle, but it also shows local and even divergent changes in faster time scales in response to local and transient changes in the light environment. Changes in cAMP might also manifest or cause various pathological processes in virtually all cellular components of the retina. Here we review the current state of knowledge and understanding of the regulatory mechanisms by which cAMP influences the physiological processes that occur in various retinal cells.<\/jats:p>","DOI":"10.3390\/cells12081157","type":"journal-article","created":{"date-parts":[[2023,4,14]],"date-time":"2023-04-14T02:28:12Z","timestamp":1681439292000},"page":"1157","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":14,"title":["Multiple Roles of cAMP in Vertebrate Retina"],"prefix":"10.3390","volume":"12","author":[{"given":"Natalia","family":"Erofeeva","sequence":"first","affiliation":[{"name":"Sechenov Institute of Evolutionary Physiology and Biochemistry, Russian Academy of Sciences, 194223 St. Petersburg, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3043-1197","authenticated-orcid":false,"given":"Darya","family":"Meshalkina","sequence":"additional","affiliation":[{"name":"Sechenov Institute of Evolutionary Physiology and Biochemistry, Russian Academy of Sciences, 194223 St. Petersburg, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9395-1160","authenticated-orcid":false,"given":"Michael","family":"Firsov","sequence":"additional","affiliation":[{"name":"Sechenov Institute of Evolutionary Physiology and Biochemistry, Russian Academy of Sciences, 194223 St. Petersburg, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,4,14]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"11619","DOI":"10.1016\/S0021-9258(19)70334-2","article-title":"Cyclic GMP-specific, high affinity, noncatalytic binding sites on light-activated phosphodiesterase","volume":"255","author":"Yamazaki","year":"1980","journal-title":"J. Biol. Chem."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"184","DOI":"10.1016\/0014-5793(85)81139-X","article-title":"Light-induced conformational change in rhodopsin detected by modification of G-protein binding, GTP\u03b3S binding and cGMP phosphodiesterase activation","volume":"181","author":"Pellicone","year":"1985","journal-title":"FEBS Lett."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1016\/0014-5793(87)80530-6","article-title":"Cyclic GMP phosphodiesterase from bovine retina Amino acid sequence of the \u03b1-subunit and nucleotide sequence of the corresponding cDNA","volume":"223","author":"Ovchinnikov","year":"1987","journal-title":"FEBS Lett"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"664","DOI":"10.1007\/s11055-014-9967-5","article-title":"Cyclic AMP as a Regulator of the Phototransduction Cascade","volume":"44","author":"Astakhova","year":"2014","journal-title":"Neurosci. Behav. Physiol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"301","DOI":"10.1007\/978-3-030-27378-1_49","article-title":"cAMP and Photoreceptor Cell Death in Retinal Degeneration","volume":"1185","author":"Charish","year":"2019","journal-title":"Adv. Exp. Med. Biol."},{"key":"ref_6","first-page":"355","article-title":"Review: Role of cAMP signaling in diabetic retinopathy","volume":"26","author":"Steinle","year":"2020","journal-title":"Mol. Vis."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"663","DOI":"10.1136\/bjo.2006.093930","article-title":"Neuroglobin in normal retina and retina from eyes with advanced glaucoma","volume":"91","author":"Rajendram","year":"2007","journal-title":"Br. J. Ophthalmol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1124\/pr.116.013078","article-title":"International union of basic and clinical pharmacology. CI. Structures and small molecule modulators of mammalian adenylyl cyclases","volume":"69","author":"Dessauer","year":"2017","journal-title":"Pharmacol. Rev."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s12987-022-00322-2","article-title":"Expression and functions of adenylyl cyclases in the CNS","volume":"19","author":"Devasani","year":"2022","journal-title":"Fluids Barriers CNS"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"6075","DOI":"10.1128\/MCB.16.11.6075","article-title":"Regulation of type I adenylyl cyclase by calmodulin kinase IV in vivo","volume":"16","author":"Wayman","year":"1996","journal-title":"Mol. Cell. Biol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"16554","DOI":"10.1016\/S0021-9258(19)89424-3","article-title":"Differential activation of adenylyl cyclase by protein kinase C isoenzymes","volume":"269","author":"Kawabe","year":"1994","journal-title":"J. Biol. Chem"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"12253","DOI":"10.1016\/S0021-9258(18)31381-4","article-title":"Inhibition of cloned adenylyl cyclases by mutant-activated Gi-alpha and specific suppression of type 2 adenylyl cyclase inhibition by phorbol ester treatment","volume":"268","author":"Chen","year":"1993","journal-title":"J. Biol. Chem."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1820","DOI":"10.1167\/iovs.14-15449","article-title":"Identification of miRNAs in a Model of Retinal Degenerations","volume":"56","author":"Saxena","year":"2015","journal-title":"Investig. Ophthalmol. Vis. Sci"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1299","DOI":"10.1074\/mcp.M700054-MCP200","article-title":"The proteome of the mouse photoreceptor sensory cilium complex","volume":"6","author":"Liu","year":"2007","journal-title":"Mol. Cell. Proteom."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"5850","DOI":"10.1242\/jcs.111427","article-title":"A key phosphorylation site in AC8 mediates regulation of Ca(2+)-dependent cAMP dynamics by an AC8-AKAP79-PKA signalling complex","volume":"125","author":"Willoughby","year":"2012","journal-title":"J. Cell. Sci."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1487","DOI":"10.1093\/hmg\/ddh160","article-title":"Expression profiling of the developing and mature Nrl\u2212\/\u2212 mouse retina: Identification of retinal disease candidates and transcriptional regulatory targets of Nrl","volume":"13","author":"Yoshida","year":"2004","journal-title":"Hum. Mol. Genet."},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Nakao, T., Tsujikawa, M., Notomi, S., Ikeda, Y., and Nishida, K. (2012). The role of mislocalized phototransduction in photoreceptor cell death of retinitis pigmentosa. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0032472"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1098","DOI":"10.1167\/iovs.09-4006","article-title":"Identification of genes and pathways involved in retinal neovascularization by microarray analysis of two animal models of retinal angiogenesis","volume":"51","author":"Recchia","year":"2010","journal-title":"Investig. Ophthalmol. Vis. Sci."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"2579","DOI":"10.1016\/j.bbadis.2014.07.032","article-title":"Soluble adenylyl cyclase in the eye","volume":"1842","author":"Lee","year":"2014","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"625","DOI":"10.1126\/science.289.5479.625","article-title":"Soluble adenylyl cyclase as an evolutionarily conserved bicarbonate sensor","volume":"289","author":"Chen","year":"2000","journal-title":"Science"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"7734","DOI":"10.1523\/JNEUROSCI.5288-11.2012","article-title":"Soluble adenylyl cyclase activity is necessary for retinal ganglion cell survival and axon growth","volume":"32","author":"Corredor","year":"2012","journal-title":"J. Neurosci. Off. J. Soc. Neurosci."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"967","DOI":"10.1167\/iovs.04-0579","article-title":"Cyclic AMP prevents retraction of axon terminals in photoreceptors prepared for transplantation: An in vitro study","volume":"46","author":"Khodair","year":"2005","journal-title":"Investig. Ophthalmol. Vis. Sci."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"725","DOI":"10.1152\/physrev.1995.75.4.725","article-title":"Cyclic nucleotide phosphodiesterases: Functional implications of multiple isoforms","volume":"75","author":"Beavo","year":"1995","journal-title":"Physiol. Rev."},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Aslam, M., and Ladilov, Y. (2022). Emerging Role of cAMP\/AMPK Signaling. Cells, 11.","DOI":"10.3390\/cells11020308"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"366","DOI":"10.1016\/j.pharmthera.2005.07.003","article-title":"Cyclic nucleotide phosphodiesterase (PDE) superfamily: A new target for the development of specific therapeutic agents","volume":"109","author":"Lugnier","year":"2006","journal-title":"Pharmacol. Ther."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"781","DOI":"10.1006\/jmbi.2001.4813","article-title":"Molecular organization of bovine rod cGMP-phosphodiesterase 6","volume":"310","author":"Tcheudji","year":"2001","journal-title":"J. Mol. Biol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1007\/5584_2021_649","article-title":"Photoreceptor Phosphodiesterase (PDE6): Structure, Regulatory Mechanisms, and Implications for Treatment of Retinal Diseases","volume":"1371","author":"Cote","year":"2022","journal-title":"Adv. Exp. Med. Biol."},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Beavo, J., Francis, S.H., and Houslay, M.D. (2007). Cyclic Nucleotide Phosphodiesterases in Health and Disease, Taylor and Francis.","DOI":"10.1201\/9781420020847.ch1"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1020","DOI":"10.1002\/jnr.21009","article-title":"Gene expression and protein localization of calmodulin-dependent phosphodiesterase in adult rat retina","volume":"84","author":"Santone","year":"2006","journal-title":"J. Neurosci. Res."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1016\/0378-1119(94)90155-4","article-title":"Differential CNS expression of alternative mRNA isoforms of the mammalian genes encoding cAMP-specific phosphodiesterases","volume":"149","author":"Bolger","year":"1994","journal-title":"Gene"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1277","DOI":"10.1016\/j.neuroscience.2009.07.045","article-title":"The novel distribution of phosphodiesterase-4 subtypes within the rat retina","volume":"163","author":"Whitaker","year":"2009","journal-title":"Neuroscience"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1971","DOI":"10.1242\/jcs.114.11.1971","article-title":"Cyclic AMP signalling","volume":"114","author":"Fimia","year":"2001","journal-title":"J. Cell Sci."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1124\/molpharm.121.000315","article-title":"The Tails of Protein Kinase, A","volume":"101","author":"Taylor","year":"2022","journal-title":"Mol. Pharmacol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"E203","DOI":"10.1038\/ncb0802-e203","article-title":"Kinase-and phosphatase-anchoring proteins: Harnessing the dynamic duo","volume":"4","author":"Bauman","year":"2002","journal-title":"Nat. Cell Biol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"782041","DOI":"10.3389\/fnmol.2021.782041","article-title":"Protein Kinase A in Human Retina: Differential Localization of Cbeta, Calpha, RIIalpha, and RIIbeta in Photoreceptors Highlights Non-redundancy of Protein Kinase A Subunits","volume":"14","author":"Roa","year":"2021","journal-title":"Front. Mol. Neurosci."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"149","DOI":"10.5483\/BMBRep.2021.54.3.233","article-title":"Epac: New emerging cAMP-binding protein","volume":"54","author":"Lee","year":"2021","journal-title":"BMB Rep."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1055\/a-1657-2464","article-title":"Repercussion of cAMP and EPAC in Memory and Signaling","volume":"72","author":"Naz","year":"2022","journal-title":"Drug Res."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"955","DOI":"10.1016\/j.neuroscience.2009.10.054","article-title":"Differential distribution of exchange proteins directly activated by cyclic AMP within the adult rat retina","volume":"165","author":"Whitaker","year":"2010","journal-title":"Neuroscience"},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Rasmussen, M., Zhou, J., Schwede, F., and Ekstrom, P. (2022). Enhanced cGMP Interactor Rap Guanine Exchange Factor 4 (EPAC2) Expression and Activity in Degenerating Photoreceptors: A Neuroprotective Response?. Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms23094619"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1523","DOI":"10.1046\/j.1471-4159.1998.70041523.x","article-title":"Cyclic AMP resets the circadian clock in cultured Xenopus retinal photoreceptor layers","volume":"70","author":"Hasegawa","year":"1998","journal-title":"J. Neurochem."},{"key":"ref_41","first-page":"99","article-title":"cAMP Level in Outer Segments of Retinal Rods of the Frog, R. ridibunda","volume":"24","author":"Astakhova","year":"2010","journal-title":"Sens. Syst."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1142","DOI":"10.1111\/j.1471-4159.2006.04154.x","article-title":"Temporal coupling of cyclic AMP and Ca\/calmodulin-stimulated adenylyl cyclase to the circadian clock in chick retinal photoreceptor cells","volume":"99","author":"Chaurasia","year":"2006","journal-title":"J. Neurochem."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"109141","DOI":"10.1016\/j.exer.2022.109141","article-title":"Phosphatic metabolism in dark- and light-adapted rat retinas","volume":"221","author":"Glonek","year":"2022","journal-title":"Exp. Eye Res."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1016\/S0006-291X(78)80042-4","article-title":"Guanine nucleotide concentrations in vivo in outer segments of dark and light adapted frog retina","volume":"85","author":"Lust","year":"1978","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"731","DOI":"10.1085\/jgp.92.6.731","article-title":"Light-induced losses and dark recovery rates of guanosine 3\u2032,5\u2032-cyclic monophosphate in rod outer segments of intact amphibian photoreceptors","volume":"92","author":"Cohen","year":"1988","journal-title":"J. Gen. Physiol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"1191","DOI":"10.2741\/1612","article-title":"cGMP signaling in vertebrate retinal photoreceptor cells","volume":"10","author":"Zhang","year":"2005","journal-title":"Front. Biosci.-Landmark"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"28241","DOI":"10.1074\/jbc.M505117200","article-title":"Phosphorylation of GRK1 and GRK7 by cAMP-dependent protein kinase attenuates their enzymatic activities","volume":"280","author":"Horner","year":"2005","journal-title":"J. Biol. Chem."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"1314","DOI":"10.1111\/j.1471-4159.2008.05691.x","article-title":"Phosphorylation of GRK7 by PKA in cone photoreceptor cells is regulated by light","volume":"107","author":"Osawa","year":"2008","journal-title":"J. Neurochem."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"20923","DOI":"10.1074\/jbc.M111.230904","article-title":"Phosphorylation of G protein-coupled receptor kinase 1 (GRK1) is regulated by light but independent of phototransduction in rod photoreceptors","volume":"286","author":"Osawa","year":"2011","journal-title":"J. Biol. Chem."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"2677","DOI":"10.1096\/fj.201902535R","article-title":"Phosphorylation at Serine 21 in G protein-coupled receptor kinase 1 (GRK1) is required for normal kinetics of dark adaption in rod but not cone photoreceptors","volume":"34","author":"Kolesnikov","year":"2020","journal-title":"FASEB J."},{"key":"ref_51","doi-asserted-by":"crossref","unstructured":"Chrispell, J.D., Xiong, Y., and Weiss, E.R. (2022). Grk7 but not Grk1 undergoes cAMP-dependent phosphorylation in zebrafish cone photoreceptors and mediates cone photoresponse recovery to elevated cAMP. J. Biol. Chem., 102636.","DOI":"10.1101\/2022.06.23.497385"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"421","DOI":"10.1085\/jgp.201210811","article-title":"cAMP controls rod photoreceptor sensitivity via multiple targets in the phototransduction cascade","volume":"140","author":"Astakhova","year":"2012","journal-title":"J. Gen. Physiol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"689","DOI":"10.1085\/jgp.201611744","article-title":"Elevated cAMP improves signal-to-noise ratio in amphibian rod photoreceptors","volume":"149","author":"Astakhova","year":"2017","journal-title":"J. Gen. Physiol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"223","DOI":"10.1177\/0748730416642657","article-title":"The retina and other light-sensitive ocular clocks","volume":"31","author":"Besharse","year":"2016","journal-title":"J. Biol. Rhythm."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"26996","DOI":"10.1073\/pnas.2009164117","article-title":"Rhodopsin-mediated light-off-induced protein kinase A activation in mouse rod photoreceptor cells","volume":"117","author":"Sato","year":"2020","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1038\/s41580-019-0179-2","article-title":"Molecular mechanisms and physiological importance of circadian rhythms","volume":"21","author":"Patke","year":"2020","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"505","DOI":"10.1016\/j.ncl.2019.05.001","article-title":"Assessment of circadian rhythms","volume":"37","author":"Reid","year":"2019","journal-title":"Neurol. Clin."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/s11892-014-0507-z","article-title":"Metabolic consequences of sleep and circadian disorders","volume":"14","author":"Depner","year":"2014","journal-title":"Curr. Diabetes Rep."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1007\/978-1-0716-0381-9_18","article-title":"Light input to the mammalian circadian clock","volume":"2130","author":"Dannerfjord","year":"2021","journal-title":"Methods Mol. Biol."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1177\/0748730404263002","article-title":"Retinal circadian clocks and control of retinal physiology","volume":"19","author":"Green","year":"2004","journal-title":"J. Biol. Rhythm."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"1019","DOI":"10.1111\/j.1471-4159.2004.02571.x","article-title":"Circadian rhythms in the retina of rats with photoreceptor degeneration","volume":"90","author":"Sakamoto","year":"2004","journal-title":"J. Neurochem."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1111\/j.1469-7793.2000.0077m.x","article-title":"A circadian clock regulates the pH of the fish retina","volume":"522","author":"Dmitriev","year":"2000","journal-title":"J. Physiol."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"2897","DOI":"10.1523\/JNEUROSCI.21-08-02897.2001","article-title":"Circadian clock regulation of pH in the rabbit retina","volume":"21","author":"Dmitriev","year":"2001","journal-title":"J. Neurosci."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1016\/B978-0-12-405210-9.00006-0","article-title":"Role of melatonin and its receptors in the vertebrate retina","volume":"300","author":"Wiechmann","year":"2013","journal-title":"Int. Rev. Cell Mol. Biol."},{"key":"ref_65","first-page":"400","article-title":"The effects of dopamine and dopamine receptor agonists on the phototransduction cascade of frog rods","volume":"25","author":"Nikolaeva","year":"2019","journal-title":"Mol. Vis."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1017\/S095252381300062X","article-title":"Regulation of photoreceptor gap junction phosphorylation by adenosine in zebrafish retina","volume":"31","author":"Li","year":"2014","journal-title":"Vis. Neurosci."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"2002","DOI":"10.1016\/j.cellsig.2015.06.008","article-title":"Dopamine receptor D4 internalization requires a beta-arrestin and a visual arrestin","volume":"27","author":"Deming","year":"2015","journal-title":"Cell. Signal."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"114304","DOI":"10.1016\/j.bcp.2020.114304","article-title":"The relevance of daylight for humans","volume":"191","author":"Skene","year":"2021","journal-title":"Biochem. Pharmacol."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"107513","DOI":"10.1016\/j.pharmthera.2020.107513","article-title":"Keep an eye on adenosine: Its role in retinal inflammation","volume":"210","author":"Santiago","year":"2020","journal-title":"Pharmacol. Ther."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"4201","DOI":"10.1113\/jphysiol.2014.276220","article-title":"Adenosine modulates light responses of rat retinal ganglion cell photoreceptors througha cAMP-mediated pathway","volume":"592","author":"Sodhi","year":"2014","journal-title":"J. Physiol."},{"key":"ref_71","doi-asserted-by":"crossref","unstructured":"Liu, L., Jiang, Y., and Steinle, J.J. (2018). Epac1 protects the retina against ischemia\/reperfusion-induced neuronal and vascular damage. PLoS ONE, 13.","DOI":"10.1371\/journal.pone.0204346"},{"key":"ref_72","first-page":"1","article-title":"Epac1 agonist decreased inflammatory proteins in retinal endothelial cells, and loss of Epac1 increased inflammatory proteins in the retinal vasculature of mice","volume":"23","author":"Liu","year":"2017","journal-title":"Mol. Vis."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"108987","DOI":"10.1016\/j.exer.2022.108987","article-title":"Epac1 and PKA regulate of P2X7 and NLRP3 inflammasome proteins in the retinal vasculature","volume":"218","author":"Liu","year":"2022","journal-title":"Exp. Eye Res."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"9503","DOI":"10.1523\/JNEUROSCI.0670-21.2021","article-title":"Glycine Release Is Potentiated by cAMP via EPAC2 and Ca(2+) Stores in a Retinal Interneuron","volume":"41","author":"Meadows","year":"2021","journal-title":"J. Neurosci. Off. J. Soc. Neurosci."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"7858","DOI":"10.1007\/s12035-018-0962-7","article-title":"Dopamine Promotes Ascorbate Release from Retinal Neurons: Role of D1 Receptors and the Exchange Protein Directly Activated by cAMP type 2 (EPAC2)","volume":"55","author":"Portugal","year":"2018","journal-title":"Mol. Neurobiol."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"e20190930","DOI":"10.1084\/jem.20190930","article-title":"Neuronal Epac1 mediates retinal neurodegeneration in mouse models of ocular hypertension","volume":"217","author":"Liu","year":"2020","journal-title":"J. Exp. Med."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"6355","DOI":"10.1167\/iovs.12-10180","article-title":"Mislocalized opsin and cAMP signaling: A mechanism for sprouting by rod cells in retinal degeneration","volume":"53","author":"Wang","year":"2012","journal-title":"Invest. Ophthalmol. Vis.Sci"},{"key":"ref_78","first-page":"391","article-title":"Effects of intravitreal injection of a Rho-GTPase inhibitor (BA-210), or CNTF combined with an analogue of cAMP, on the dendritic morphology of regenerating retinal ganglion cells","volume":"32","author":"Drummond","year":"2014","journal-title":"Restor. Neurol. Neurosci."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"1742","DOI":"10.1111\/ejn.12543","article-title":"Routes to cAMP: Shaping neuronal connectivity with distinct adenylate cyclases","volume":"39","author":"Nicol","year":"2014","journal-title":"Eur. J. Neurosci."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"108220","DOI":"10.1016\/j.celrep.2020.108220","article-title":"cAMP-Dependent Co-stabilization of Axonal Arbors from Adjacent Developing Neurons","volume":"33","author":"Louail","year":"2020","journal-title":"Cell Rep."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"107828","DOI":"10.1016\/j.exer.2019.107828","article-title":"Systemic \u00df adrenergic stimulation\/sympathetic nerve system stimulation influences intraocular RAS through cAMP in the RPE","volume":"189","author":"Martins","year":"2019","journal-title":"Exp. Eye Res."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"1701","DOI":"10.1007\/s11064-021-03313-1","article-title":"Increased Retinal Ganglion Cell Survival by Exogenous IL-2 Depends on IL-10, Dopamine D1 Receptors, and Classical IL-2\/IL-2R Signaling Pathways","volume":"46","author":"Colares","year":"2021","journal-title":"Neurochem. Res."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"444","DOI":"10.1111\/jnc.12832","article-title":"CLIC1 functional expression is required for cAMP-induced neurite elongation in post-natal mouse retinal ganglion cells","volume":"131","author":"Averaimo","year":"2014","journal-title":"J. Neurochem."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"e2113751119","DOI":"10.1073\/pnas.2113751119","article-title":"Monocyte-derived SDF1 supports optic nerve regeneration and alters retinal ganglion cells\u2019 response to Pten deletion","volume":"119","author":"Xie","year":"2022","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"5466","DOI":"10.1523\/JNEUROSCI.2752-18.2019","article-title":"Regulation of Neuronal Survival and Axon Growth by a Perinuclear cAMP Compartment","volume":"39","author":"Boczek","year":"2019","journal-title":"J. Neurosci. Off. J. Soc. Neurosci."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"2054","DOI":"10.1172\/JCI125898","article-title":"Neogenin neutralization prevents photoreceptor loss in inherited retinal degeneration","volume":"130","author":"Charish","year":"2020","journal-title":"J. Clin. Invest."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"1880","DOI":"10.1016\/j.ebiom.2015.10.025","article-title":"Muscle A-kinase anchoring protein-\u03b1 is an injury-specific signaling scaffold required for neurotrophic-and cyclic adenosine monophosphate-mediated survival","volume":"2","author":"Wang","year":"2015","journal-title":"EBioMedicine"},{"key":"ref_88","doi-asserted-by":"crossref","unstructured":"Huang, P.-C., Hsiao, Y.-T., Kao, S.-Y., Chen, C.-F., Chen, Y.-C., Chiang, C.-W., Lee, C.-f., Lu, J.-C., Chern, Y., and Wang, C.-T. (2014). Adenosine A2A receptor up-regulates retinal wave frequency via starburst amacrine cells in the developing rat retina. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0095090"},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"673","DOI":"10.1016\/S0896-6273(00)81121-6","article-title":"Dynamics of retinal waves are controlled by cyclic AMP","volume":"24","author":"Stellwagen","year":"1999","journal-title":"Neuron"},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"689","DOI":"10.1016\/S0896-6273(02)00602-5","article-title":"Retinal ganglion cells do not extend axons by default: Promotion by neurotrophic signaling and electrical activity","volume":"33","author":"Goldberg","year":"2002","journal-title":"Neuron"},{"key":"ref_91","first-page":"718","article-title":"Intravitreal injection of forskolin, homotaurine, and L-carnosine affords neuroprotection to retinal ganglion cells following retinal ischemic injury","volume":"21","author":"Russo","year":"2015","journal-title":"Mol. Vis."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"1747","DOI":"10.1167\/iovs.01-0886","article-title":"Activation of MAPK and CREB by GM1 induces survival of RGCs in the retina with axotomized nerve","volume":"44","author":"Choi","year":"2003","journal-title":"Investig. Ophthalmol. Vis. Sci."}],"container-title":["Cells"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4409\/12\/8\/1157\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T19:15:40Z","timestamp":1760123740000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4409\/12\/8\/1157"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,4,14]]},"references-count":92,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2023,4]]}},"alternative-id":["cells12081157"],"URL":"https:\/\/doi.org\/10.3390\/cells12081157","relation":{},"ISSN":["2073-4409"],"issn-type":[{"value":"2073-4409","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,4,14]]}}}