Skip to main content
Log in

Adenosine receptor expression in the adult zebrafish retina

  • Original Article
  • Published:
Purinergic Signalling Aims and scope Submit manuscript

Abstract

Adenosine is an endogenous nucleoside in the central nervous system that acts on adenosine receptors. These are G protein-coupled receptors that have four known subtypes: A1, A2A, A2B, and A3 receptors. In the present study, we aimed to map the location of the adenosine receptor subtypes in adult wild-type zebrafish retina using in situ hybridization and immunohistochemistry. A1R, A2AR, and A2BR mRNA were detected in the ganglion cell layer (GCL), the inner nuclear layer (INL), the outer nuclear layer (ONL), and the outer segment (OS). A3R mRNA was detected in the GCL, ONL, and OS. A1R-immunoreactivity was expressed as puncta in the INL and in the outer plexiform layer (OPL). A1Rs were located within the cone pedicle and contiguous to horizontal cell tips in the OPL. A2AR-immunoreactivity was expressed as puncta in the GCL, inner plexiform layer (IPL), INL, and outer retina. A2AR puncta in the outer retina were situated around the ellipsoids and nuclei of cones, and weakly around the rod nuclei. A1Rs and A2ARs were clustered around ON cone bipolar cell terminals and present in the OFF lamina of the INL but were not expressed on mixed rod/cone response bipolar cell terminals. A2BR-immunoreactivity was mainly localized to the Müller cells, while A3Rs were found to be expressed in retinal ganglion cells of the GCL, INL, ONL, and OS. In summary, all four adenosine receptor subtypes were localized in the zebrafish retina and are in agreement with expression patterns shown in retinas from other species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Stella SL Jr, Bryson EJ, Cadetti L, Thoreson WB (2003) Endogenous adenosine reduces glutamatergic output from rods through activation of A2-like adenosine receptors. J Neurophysiol 90(1):165–174. https://doi.org/10.1152/jn.00671.2002

    Article  CAS  PubMed  Google Scholar 

  2. Bynoe MS, Viret C, Yan A, Kim DG (2015) Adenosine receptor signaling: a key to opening the blood-brain door. Fluids Barriers CNS 12:20. https://doi.org/10.1186/s12987-015-0017-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Kashfi S, Ghaedi K, Baharvand H, Nasr-Esfahani MH, Javan M (2017) A1 adenosine receptor activation modulates central nervous system development and repair. Mol Neurobiol 54(10):8128–8139. https://doi.org/10.1007/s12035-016-0292-6

    Article  CAS  PubMed  Google Scholar 

  4. Zhong Y, Yang Z, Huang WC, Luo X (2013) Adenosine, adenosine receptors and glaucoma: an updated overview. Biochim Biophys Acta 1830(4):2882–2890. https://doi.org/10.1016/j.bbagen.2013.01.005

    Article  CAS  PubMed  Google Scholar 

  5. Dunwiddie TV, Masino SA (2001) The role and regulation of adenosine in the central nervous system. Annu Rev Neurosci 24:31–55. https://doi.org/10.1146/annurev.neuro.24.1.31

    Article  CAS  PubMed  Google Scholar 

  6. Borea PA, Gessi S, Merighi S, Varani K (2016) Adenosine as a multi-signalling guardian angel in human diseases: when, where and how does it exert its protective effects? Trends Pharmacol Sci 37(6):419–434. https://doi.org/10.1016/j.tips.2016.02.006

    Article  CAS  PubMed  Google Scholar 

  7. Fredholm BB, AP IJ, Jacobson KA, Linden J, Muller CE (2011) International Union of Basic and Clinical Pharmacology. LXXXI. Nomenclature and classification of adenosine receptors--an update. Pharmacol Rev 63(1):1–34. https://doi.org/10.1124/pr.110.003285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Kvanta A, Seregard S, Sejersen S, Kull B, Fredholm BB (1997) Localization of adenosine receptor messenger RNAs in the rat eye. Exp Eye Res 65(5):595–602. https://doi.org/10.1006/exer.1996.0352

    Article  CAS  PubMed  Google Scholar 

  9. Li H, Zhang Z, Blackburn MR, Wang SW, Ribelayga CP, O'Brien J (2013) Adenosine and dopamine receptors coregulate photoreceptor coupling via gap junction phosphorylation in mouse retina. J Neurosci 33(7):3135–3150. https://doi.org/10.1523/JNEUROSCI.2807-12.2013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Alfinito PD, Alli R, Townes-Anderson E (2002) Adenosine A(2a) receptor-mediated inhibition of rod opsin mRNA expression in tiger salamander. J Neurochem 83(3):665–672

    Article  CAS  Google Scholar 

  11. Braas KM, Zarbin MA, Snyder SH (1987) Endogenous adenosine and adenosine receptors localized to ganglion cells of the retina. Proc Natl Acad Sci U S A 84(11):3906–3910

    Article  CAS  Google Scholar 

  12. de Carvalho RP, Braas KM, Adler R, Snyder SH (1992) Developmental regulation of adenosine A1 receptors, uptake sites and endogenous adenosine in the chick retina. Brain Res Dev Brain Res 70(1):87–95

    Article  CAS  Google Scholar 

  13. Blazynski C (1990) Discrete distributions of adenosine receptors in mammalian retina. J Neurochem 54(2):648–655

    Article  CAS  Google Scholar 

  14. Blazynski C, Perez MT (1991) Adenosine in vertebrate retina: localization, receptor characterization, and function. Cell Mol Neurobiol 11(5):463–484

    Article  CAS  Google Scholar 

  15. Nakashima KI, Iwao K, Inoue T, Haga A, Tsutsumi T, Mochita MI, Fujimoto T, Tanihara H (2018) Stimulation of the adenosine A3 receptor, not the A1 or A2 receptors, promote neurite outgrowth of retinal ganglion cells. Exp Eye Res 170:160–168. https://doi.org/10.1016/j.exer.2018.02.019

    Article  CAS  PubMed  Google Scholar 

  16. Iandiev I, Wurm A, Pannicke T, Wiedemann P, Reichenbach A, Robson SC, Zimmermann H, Bringmann A (2007) Ectonucleotidases in Muller glial cells of the rodent retina: involvement in inhibition of osmotic cell swelling. Purinergic Signal 3(4):423–433. https://doi.org/10.1007/s11302-007-9061-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Huang PC, Hsiao YT, Kao SY, Chen CF, Chen YC, Chiang CW, Lee CF, Lu JC, Chern Y, Wang CT (2014) Adenosine A(2A) receptor up-regulates retinal wave frequency via starburst amacrine cells in the developing rat retina. PLoS One 9(4):e95090. https://doi.org/10.1371/journal.pone.0095090

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Stellwagen D, Shatz CJ, Feller MB (1999) Dynamics of retinal waves are controlled by cyclic AMP. Neuron 24(3):673–685

    Article  CAS  Google Scholar 

  19. Hartwick AT, Lalonde MR, Barnes S, Baldridge WH (2004) Adenosine A1-receptor modulation of glutamate-induced calcium influx in rat retinal ganglion cells. Invest Ophthalmol Vis Sci 45(10):3740–3748. https://doi.org/10.1167/iovs.04-0214

    Article  PubMed  Google Scholar 

  20. Zhang X, Zhang M, Laties AM, Mitchell CH (2006) Balance of purines may determine life or death of retinal ganglion cells as A3 adenosine receptors prevent loss following P2X7 receptor stimulation. J Neurochem 98(2):566–575. https://doi.org/10.1111/j.1471-4159.2006.03900.x

    Article  CAS  PubMed  Google Scholar 

  21. Santos PF, Caramelo OL, Carvalho AP, Duarte CB (1999) Characterization of ATP release from cultures enriched in cholinergic amacrine-like neurons. J Neurobiol 41(3):340–348

    Article  CAS  Google Scholar 

  22. Santos PF, Caramelo OL, Carvalho AP, Duarte CB (2000) Adenosine A1 receptors inhibit Ca2+ channels coupled to the release of ACh, but not of GABA, in cultured retina cells. Brain Res 852(1):10–15

    Article  CAS  Google Scholar 

  23. Newman EA (2005) Calcium increases in retinal glial cells evoked by light-induced neuronal activity. J Neurosci 25(23):5502–5510. https://doi.org/10.1523/JNEUROSCI.1354-05.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Li Y, Holtzclaw LA, Russell JT (2001) Muller cell Ca2+ waves evoked by purinergic receptor agonists in slices of rat retina. J Neurophysiol 85(2):986–994. https://doi.org/10.1152/jn.2001.85.2.986

    Article  CAS  PubMed  Google Scholar 

  25. Collison DJ, Tovell VE, Coombes LJ, Duncan G, Sanderson J (2005) Potentiation of ATP-induced Ca2+ mobilisation in human retinal pigment epithelial cells. Exp Eye Res 80(4):465–475. https://doi.org/10.1016/j.exer.2004.09.009

    Article  CAS  PubMed  Google Scholar 

  26. Stella SL Jr, Bryson EJ, Thoreson WB (2002) A2 adenosine receptors inhibit calcium influx through L-type calcium channels in rod photoreceptors of the salamander retina. J Neurophysiol 87(1):351–360. https://doi.org/10.1152/jn.00010.2001

    Article  CAS  PubMed  Google Scholar 

  27. Stella SL Jr, Hu WD, Vila A, Brecha NC (2007) Adenosine inhibits voltage-dependent Ca2+ influx in cone photoreceptor terminals of the tiger salamander retina. J Neurosci Res 85(5):1126–1137. https://doi.org/10.1002/jnr.21210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Newman EA (2003) Glial cell inhibition of neurons by release of ATP. J Neurosci 23(5):1659–1666

    Article  CAS  Google Scholar 

  29. Newman EA (2004) Glial modulation of synaptic transmission in the retina. Glia 47(3):268–274. https://doi.org/10.1002/glia.20030

    Article  PubMed  PubMed Central  Google Scholar 

  30. Sun X, Barnes S, Baldridge WH (2002) Adenosine inhibits calcium channel currents via A1 receptors on salamander retinal ganglion cells in a mini-slice preparation. J Neurochem 81(3):550–556

    Article  CAS  Google Scholar 

  31. Li Q, Puro DG (2001) Adenosine activates ATP-sensitive K(+) currents in pericytes of rat retinal microvessels: role of A1 and A2a receptors. Brain Res 907(1–2):93–99

    Article  CAS  Google Scholar 

  32. Costenla AR, De Mendonca A, Sebastiao A, Ribeiro JA (1999) An adenosine analogue inhibits NMDA receptor-mediated responses in bipolar cells of the rat retina. Exp Eye Res 68(3):367–370

    Article  CAS  Google Scholar 

  33. Blazynski C, Woods C, Mathews GC (1992) Evidence for the action of endogenous adenosine in the rabbit retina: modulation of the light-evoked release of acetylcholine. J Neurochem 58(2):761–767

    Article  CAS  Google Scholar 

  34. Friedman Z, Hackett SF, Linden J, Campochiaro PA (1989) Human retinal pigment epithelial cells in culture possess A2-adenosine receptors. Brain Res 492(1–2):29–35

    Article  CAS  Google Scholar 

  35. Gregory CY, Abrams TA, Hall MO (1994) Stimulation of A2 adenosine receptors inhibits the ingestion of photoreceptor outer segments by retinal pigment epithelium. Invest Ophthalmol Vis Sci 35(3):819–825

    CAS  PubMed  Google Scholar 

  36. Paes-de-Carvalho R, Maia GA, Ferreira JM (2003) Adenosine regulates the survival of avian retinal neurons and photoreceptors in culture. Neurochem Res 28(10):1583–1590

    Article  CAS  Google Scholar 

  37. Rey HL, Burnside B (1999) Adenosine stimulates cone photoreceptor myoid elongation via an adenosine A2-like receptor. J Neurochem 72(6):2345–2355

    Article  CAS  Google Scholar 

  38. Uckermann O, Kutzera F, Wolf A, Pannicke T, Reichenbach A, Wiedemann P, Wolf S, Bringmann A (2005) The glucocorticoid triamcinolone acetonide inhibits osmotic swelling of retinal glial cells via stimulation of endogenous adenosine signaling. J Pharmacol Exp Ther 315(3):1036–1045. https://doi.org/10.1124/jpet.105.092353

    Article  CAS  PubMed  Google Scholar 

  39. Wurm A, Pannicke T, Wiedemann P, Reichenbach A, Bringmann A (2008) Glial cell-derived glutamate mediates autocrine cell volume regulation in the retina: activation by VEGF. J Neurochem 104(2):386–399. https://doi.org/10.1111/j.1471-4159.2007.04992.x

    Article  CAS  PubMed  Google Scholar 

  40. Yaar R, Lamperti ED, Toselli PA, Ravid K (2002) Activity of the A3 adenosine receptor gene promoter in transgenic mice: characterization of previously unidentified sites of expression. FEBS Lett 532(3):267–272

    Article  CAS  Google Scholar 

  41. Zhang M, Budak MT, Lu W, Khurana TS, Zhang X, Laties AM, Mitchell CH (2006) Identification of the A3 adenosine receptor in rat retinal ganglion cells. Mol Vis 12:937–948

    CAS  PubMed  Google Scholar 

  42. Zhang M, Hu H, Zhang X, Lu W, Lim J, Eysteinsson T, Jacobson KA, Laties AM, Mitchell CH (2010) The A3 adenosine receptor attenuates the calcium rise triggered by NMDA receptors in retinal ganglion cells. Neurochem Int 56(1):35–41. https://doi.org/10.1016/j.neuint.2009.08.011

    Article  CAS  PubMed  Google Scholar 

  43. Hu H, Lu W, Zhang M, Zhang X, Argall AJ, Patel S, Lee GE, Kim YC, Jacobson KA, Laties AM, Mitchell CH (2010) Stimulation of the P2X7 receptor kills rat retinal ganglion cells in vivo. Exp Eye Res 91(3):425–432. https://doi.org/10.1016/j.exer.2010.06.017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Richardson R, Tracey-White D, Webster A, Moosajee M (2017) The zebrafish eye-a paradigm for investigating human ocular genetics. Eye (Lond) 31(1):68–86. https://doi.org/10.1038/eye.2016.198

    Article  CAS  Google Scholar 

  45. Angueyra JM, Kindt KS (2018) Leveraging zebrafish to study retinal degenerations. Front Cell Dev Biol 6(110). https://doi.org/10.3389/fcell.2018.00110

  46. Hamblin MR, Huang YY, Heiskanen V (2018) Non-mammalian hosts and photobiomodulation: do all life-forms respond to light? Photochem Photobiol 95:126–139. https://doi.org/10.1111/php.12951

    Article  CAS  PubMed  Google Scholar 

  47. Trimarchi JM, Stadler MB, Roska B, Billings N, Sun B, Bartch B, Cepko CL (2007) Molecular heterogeneity of developing retinal ganglion and amacrine cells revealed through single cell gene expression profiling. J Comp Neurol 502(6):1047–1065. https://doi.org/10.1002/cne.21368

    Article  CAS  PubMed  Google Scholar 

  48. Larison KD, Bremiller R (1990) Early onset of phenotype and cell patterning in the embryonic zebrafish retina. Development 109(3):567–576

    CAS  PubMed  Google Scholar 

  49. Haug MF, Gesemann M, Berger M, Neuhauss SCF (2018) Phylogeny and distribution of protein kinase C variants in the zebrafish. J Comp Neurol 526(7):1097–1109. https://doi.org/10.1002/cne.24395

    Article  CAS  PubMed  Google Scholar 

  50. Klooster J, Studholme KM, Yazulla S (2001) Localization of the AMPA subunit GluR2 in the outer plexiform layer of goldfish retina. J Comp Neurol 441(2):155–167

    Article  CAS  Google Scholar 

  51. Klooster J, Yazulla S, Kamermans M (2009) Ultrastructural analysis of the glutamatergic system in the outer plexiform layer of zebrafish retina. J Chem Neuroanat 37(4):254–265. https://doi.org/10.1016/j.jchemneu.2009.02.004

    Article  CAS  PubMed  Google Scholar 

  52. Yazulla S, Studholme KM (2001) Neurochemical anatomy of the zebrafish retina as determined by immunocytochemistry. J Neurocytol 30(7):551–592

    Article  CAS  Google Scholar 

  53. Peterson RE, Fadool JM, McClintock J, Linser PJ (2001) Muller cell differentiation in the zebrafish neural retina: evidence of distinct early and late stages in cell maturation. J Comp Neurol 429(4):530–540

    Article  CAS  Google Scholar 

  54. Sherpa T, Fimbel SM, Mallory DE, Maaswinkel H, Spritzer SD, Sand JA, Li L, Hyde DR, Stenkamp DL (2008) Ganglion cell regeneration following whole-retina destruction in zebrafish. Dev Neurobiol 68(2):166–181. https://doi.org/10.1002/dneu.20568

    Article  PubMed  PubMed Central  Google Scholar 

  55. Li R, Wu F, Ruonala R, Sapkota D, Hu Z, Mu X (2014) Isl1 and Pou4f2 form a complex to regulate target genes in developing retinal ganglion cells. PLoS One 9(3):e92105. https://doi.org/10.1371/journal.pone.0092105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Grillo SL, Stella SL Jr (2018) Melanopsin retinal ganglion cells are not labeled in thy-1YFP-16 transgenic mice. Neuroreport 29(2):118–122. https://doi.org/10.1097/WNR.0000000000000918

    Article  CAS  PubMed  Google Scholar 

  57. Stella SL Jr, Vila A, Hung AY, Rome ME, Huynh U, Sheng M, Kreienkamp HJ, Brecha NC (2012) Association of shank 1A scaffolding protein with cone photoreceptor terminals in the mammalian retina. PLoS One 7(9):e43463. https://doi.org/10.1371/journal.pone.0043463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Grillo SL, Montgomery CL, Johnson HM, Koulen P (2018) Quantification of changes in visual function during disease development in a mouse model of pigmentary glaucoma. J Glaucoma 27(9):828–841. https://doi.org/10.1097/IJG.0000000000001024

    Article  PubMed  PubMed Central  Google Scholar 

  59. Grillo MA, Grillo SL, Gerdes BC, Kraus JG, Koulen P (2019) Control of neuronal ryanodine receptor-mediated calcium signaling by calsenilin. Mol Neurobiol 56(1):525–534. https://doi.org/10.1007/s12035-018-1080-2

    Article  CAS  PubMed  Google Scholar 

  60. Fredholm BB, Arslan G, Halldner L, Kull B, Schulte G, Wasserman W (2000) Structure and function of adenosine receptors and their genes. Naunyn Schmiedeberg's Arch Pharmacol 362(4–5):364–374

    Article  CAS  Google Scholar 

  61. Panula P, Chen YC, Priyadarshini M, Kudo H, Semenova S, Sundvik M, Sallinen V (2010) The comparative neuroanatomy and neurochemistry of zebrafish CNS systems of relevance to human neuropsychiatric diseases. Neurobiol Dis 40(1):46–57. https://doi.org/10.1016/j.nbd.2010.05.010

    Article  CAS  PubMed  Google Scholar 

  62. Wakisaka N, Miyasaka N, Koide T, Masuda M, Hiraki-Kajiyama T, Yoshihara Y (2017) An adenosine receptor for olfaction in fish. Curr Biol 27(10):1437–1447.e1434. https://doi.org/10.1016/j.cub.2017.04.014

    Article  CAS  PubMed  Google Scholar 

  63. Boehmler W, Petko J, Woll M, Frey C, Thisse B, Thisse C, Canfield VA, Levenson R (2009) Identification of zebrafish A2 adenosine receptors and expression in developing embryos. Gene Expr Patterns 9(3):144–151. https://doi.org/10.1016/j.gep.2008.11.006

    Article  CAS  PubMed  Google Scholar 

  64. Stella SL Jr, Hu WD, Brecha NC (2009) Adenosine suppresses exocytosis from cone terminals of the salamander retina. Neuroreport 20(10):923–929. https://doi.org/10.1097/WNR.0b013e32832ca4b0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. McIntosh HH, Blazynski C (1994) Characterization and localization of adenosine A2 receptors in bovine rod outer segments. J Neurochem 62(3):992–997

    Article  CAS  Google Scholar 

  66. Wang CT, Blankenship AG, Anishchenko A, Elstrott J, Fikhman M, Nakanishi S, Feller MB (2007) GABA(A) receptor-mediated signaling alters the structure of spontaneous activity in the developing retina. J Neurosci 27(34):9130–9140. https://doi.org/10.1523/JNEUROSCI.1293-07.2007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Jonsson G, Eysteinsson T (2017) Retinal A2A and A3 adenosine receptors modulate the components of the rat electroretinogram. Vis Neurosci 34:E001. https://doi.org/10.1017/S0952523816000171

    Article  PubMed  Google Scholar 

  68. Stone TW, Ceruti S, Abbracchio MP (2009) Adenosine receptors and neurological disease: neuroprotection and neurodegeneration. Handb Exp Pharmacol 193:535–587. https://doi.org/10.1007/978-3-540-89615-9_17

    Article  CAS  Google Scholar 

  69. Sebastiao AM, Ribeiro JA (1996) Adenosine A2 receptor-mediated excitatory actions on the nervous system. Prog Neurobiol 48(3):167–189

    Article  CAS  Google Scholar 

  70. Koscso B, Csoka B, Selmeczy Z, Himer L, Pacher P, Virag L, Hasko G (2012) Adenosine augments IL-10 production by microglial cells through an A2B adenosine receptor-mediated process. J Immunol 188(1):445–453. https://doi.org/10.4049/jimmunol.1101224

    Article  CAS  PubMed  Google Scholar 

  71. Merighi S, Borea PA, Stefanelli A, Bencivenni S, Castillo CA, Varani K, Gessi S (2015) A2a and a2b adenosine receptors affect HIF-1alpha signaling in activated primary microglial cells. Glia 63(11):1933–1952. https://doi.org/10.1002/glia.22861

    Article  PubMed  Google Scholar 

  72. Pilitsis JG, Kimelberg HK (1998) Adenosine receptor mediated stimulation of intracellular calcium in acutely isolated astrocytes. Brain Res 798(1–2):294–303

    Article  CAS  Google Scholar 

  73. Dare E, Schulte G, Karovic O, Hammarberg C, Fredholm BB (2007) Modulation of glial cell functions by adenosine receptors. Physiol Behav 92(1–2):15–20. https://doi.org/10.1016/j.physbeh.2007.05.031

    Article  CAS  PubMed  Google Scholar 

  74. Yamagata K, Hakata K, Maeda A, Mochizuki C, Matsufuji H, Chino M, Yamori Y (2007) Adenosine induces expression of glial cell line-derived neurotrophic factor (GDNF) in primary rat astrocytes. Neurosci Res 59(4):467–474. https://doi.org/10.1016/j.neures.2007.08.016

    Article  CAS  PubMed  Google Scholar 

  75. Eusemann TN, Willmroth F, Fiebich B, Biber K, van Calker D (2015) Adenosine receptors differentially regulate the expression of regulators of G-protein signalling (RGS) 2, 3 and 4 in astrocyte-like cells. PLoS One 10(8):e0134934. https://doi.org/10.1371/journal.pone.0134934

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Fusco I, Ugolini F, Lana D, Coppi E, Dettori I, Gaviano L, Nosi D, Cherchi F, Pedata F, Giovannini MG, Pugliese AM (2018) The selective antagonism of adenosine A2B receptors reduces the synaptic failure and neuronal death induced by oxygen and glucose deprivation in rat CA1 hippocampus in vitro. Front Pharmacol 9:399. https://doi.org/10.3389/fphar.2018.00399

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Trincavelli ML, Tonazzini I, Montali M, Abbracchio MP, Martini C (2008) Short-term TNF-alpha treatment induced A2B adenosine receptor desensitization in human astroglial cells. J Cell Biochem 104(1):150–161. https://doi.org/10.1002/jcb.21611

    Article  CAS  PubMed  Google Scholar 

  78. Bernascone S, Erriquez J, Ferraro M, Genazzani AA, Distasi C (2010) Novel adenosine and cAMP signalling pathways in migrating glial cells. Cell Calcium 48(1):83–90. https://doi.org/10.1016/j.ceca.2010.07.004

    Article  CAS  PubMed  Google Scholar 

  79. Dando R, Dvoryanchikov G, Pereira E, Chaudhari N, Roper SD (2012) Adenosine enhances sweet taste through A2B receptors in the taste bud. J Neurosci 32(1):322–330. https://doi.org/10.1523/JNEUROSCI.4070-11.2012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Galvao J, Elvas F, Martins T, Cordeiro MF, Ambrosio AF, Santiago AR (2015) Adenosine A3 receptor activation is neuroprotective against retinal neurodegeneration. Exp Eye Res 140:65–74. https://doi.org/10.1016/j.exer.2015.08.009

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors wish to thank Scott Chartrand for providing technical advice and James Connor for the use of his Amersham Imager 600.

Funding

This research was supported by Start-up funds provided by Penn State University, College of Medicine, and a grant from the PA Tobacco Settlement Funds (Commonwealth of Pennsylvania) to SLS.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Stephanie L. Grillo.

Ethics declarations

Conflicts of interest

Stephanie L. Grillo declares that she has no conflict of interest.

Dillon McDevitt declares that he has no conflict of interest.

Matthew G. Voas declares that he has no conflict of interest.

Amanda Khan declares that she has no conflict of interest.

Michael A. Grillo declares that he has no conflict of interest.

Salvatore L. Stella Jr declares that he has no conflict of interest.

Ethical approval

All animals were cared for according to institutional guidelines prescribed by the Penn State Hershey IACUC Committee, and the National Eye Institute.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Grillo, S.L., McDevitt, D.S., Voas, M.G. et al. Adenosine receptor expression in the adult zebrafish retina. Purinergic Signalling 15, 327–342 (2019). https://doi.org/10.1007/s11302-019-09667-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11302-019-09667-0

Keywords

Navigation