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Exogenous Adenosine Modulates Behaviors and Stress Response in Caenorhabditis elegans

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Abstract

Adenosine, a purine nucleoside with neuromodulatory actions, is part of the purinergic signaling system (PSS). Caenorhabditis elegans is a free-living nematode found in soil, used in biological research for its advantages as an alternative experimental model. Since there is a lack of evidence of adenosine’s direct actions and the PSS’s participation in this animal, such an investigation is necessary. In this research, we aimed to test the effects of acute and chronic adenosine at 1, 5, and 10 mM on nematode’s behaviors, morphology, survival after stress conditions, and on pathways related to the response to oxidative stress (DAF-16/FOXO and SKN-1) and genes products downstream these pathways (SOD-3, HSP-16.2, and GCS-1). Acute or chronic adenosine did not alter the worms’ morphology analyzed by the worms’ length, width, and area, nor interfered with reproductive behavior. On the other hand, acute and chronic adenosine modulated the defecation rate, pharyngeal pumping rate, and locomotion, in addition, to interacting with stress response pathways in C. elegans. Adenosine interfered in the speed and mobility of the worms analyzed. In addition, both acute and chronic adenosine presented modulatory effects on oxidative stress response signaling. Acute adenosine prevented the heat-induced-increase of DAF-16 activation and SOD-3 levels, while chronic adenosine per se induced DAF-16 activation and prevented heat-induced-increase of HSP-16.2 and SKN-1 levels. Together, these results indicate that exogenous adenosine has physiological and biochemical effects on C. elegans and describes possible purinergic signaling in worms.

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Data Availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

References

  1. Verkhratsky A, Burnstock G (2014) Biology of purinergic signalling: its ancient evolutionary roots, its omnipresence and its multiple functional significance. BioEssays 36:697–705. https://doi.org/10.1002/bies.201400024

    Article  CAS  Google Scholar 

  2. Zimmermann H (2001) Ectonucleotidases: some recent developments and a note on nomenclature. Drug Dev Res 52:44–56. https://doi.org/10.1002/ddr.1097

    Article  CAS  Google Scholar 

  3. Stone TW (1985) Classification of adenosine receptors in the central nervous system. In: Methods used in adenosine research. Springer, Boston, pp 305–316

  4. Libert F, Parmentier M, Lefort A et al (1989) Selective amplification and cloning of four new members of the G protein-coupled receptor family. Science 244:569–572. https://doi.org/10.1126/science.2541503

    Article  CAS  Google Scholar 

  5. Burnstock (1978) A basis for distinguishing two types of purinergic receptor. In: Cell Membrane Receptors for Drugs and Hormone: A Multidisciplinary Approach. pp 107–118

  6. Fredholm BB, IjzermanJacobson APKA, Klotz KN, Linden J (2001) International Union of Pharmacology. XXV. Nomenclature and classification of adenosine receptors. Pharmacol Rev 53:527–552

    CAS  Google Scholar 

  7. Gomes CV, Kaster MP, Tomé AR et al (2011) Adenosine receptors and brain diseases: neuroprotection and neurodegeneration. Biochim Biophys Acta 1808:1380–1399. https://doi.org/10.1016/j.bbamem.2010.12.001

    Article  CAS  Google Scholar 

  8. Antonioli L, Blandizzi C, Pacher P, Haskó G (2013) Immunity, inflammation and cancer: a leading role for adenosine. Nat Rev Cancer 13:842–857. https://doi.org/10.1038/nrc3613

    Article  CAS  Google Scholar 

  9. Ramkumar V, Hallam DM, Nie Z (2001) Adenosine, oxidative stress and cytoprotection. Jpn J Pharmacol 86:265–274. https://doi.org/10.1254/jjp.86.265

    Article  CAS  Google Scholar 

  10. Borea PA, Gessi S, Merighi S et al (2018) Pharmacology of adenosine receptors: the state of the art. Physiol Rev 98:1591–1625. https://doi.org/10.1152/physrev.00049.2017

    Article  CAS  Google Scholar 

  11. Rudolphi KA, Schubert P, Parkinson FE, Fredholm BB (1992) Neuroprotective role of adenosine in cerebral ischaemia. Trends Pharmacol Sci 13:439–445. https://doi.org/10.1016/0165-6147(92)90141-R

    Article  CAS  Google Scholar 

  12. Chen J-F, Huang Z, Ma J et al (1999) A(2A) Adenosine Receptor deficiency attenuates brain injury induced by transient focal ischemia in mice. J Neurosci 19:9192–9200. https://doi.org/10.1523/JNEUROSCI.19-21-09192.1999

    Article  CAS  Google Scholar 

  13. Fredholm BB, Arslan G, Kull B et al (1996) Adenosine (P1) receptor signalling. Drug Dev Res 39:262–268. https://doi.org/10.1002/(SICI)1098-2299(199611/12)39:3/4%3c262::AID-DDR5%3e3.0.CO;2-P

    Article  CAS  Google Scholar 

  14. Fredholm BB, Abbracchio MP, Burnstock G et al (1994) Nomenclature and classification of purinoceptors. Pharmacol Rev 46:143–156

    CAS  Google Scholar 

  15. Karmouty-Quintana H, Xia Y, Blackburn MR (2013) Adenosine signaling during acute and chronic disease states. J Mol Med 91:173–181. https://doi.org/10.1007/s00109-013-0997-1

    Article  CAS  Google Scholar 

  16. Zhou Y, Schneider DJ, Blackburn MR (2009) Adenosine signaling and the regulation of chronic lung disease. Pharmacol Ther 123:105–116. https://doi.org/10.1016/j.pharmthera.2009.04.003

    Article  CAS  Google Scholar 

  17. Sulston JE, Schierenberg E, White JG, Thomson JN (1983) The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol 100:64–119. https://doi.org/10.1016/0012-1606(83)90201-4

    Article  CAS  Google Scholar 

  18. Helmcke KJ, Avila DS, Aschner M (2010) Utility of Caenorhabditis elegans in high throughput neurotoxicological research. Neurotoxicol Teratol 32:62–67. https://doi.org/10.1016/j.ntt.2008.11.005

    Article  CAS  Google Scholar 

  19. Schafer JC, Winkelbauer ME, Williams CL et al (2006) IFTA-2 is a conserved cilia protein involved in pathways regulating longevity and dauer formation in Caenorhabditis elegans. J Cell Sci 119:4088–4100. https://doi.org/10.1242/jcs.03187

    Article  CAS  Google Scholar 

  20. Murphy CT (2013) Insulin/insulin-like growth factor signaling in C. elegans. WormBook 1–43. https://doi.org/10.1895/wormbook.1.164.1

  21. Robida-Stubbs S, Glover-Cutter K, Lamming DW et al (2012) TOR signaling and rapamycin influence longevity by regulating SKN-1/Nrf and DAF-16/FoxO. Cell Metab 15:713–724. https://doi.org/10.1016/j.cmet.2012.04.007

    Article  CAS  Google Scholar 

  22. Burnstock G, Verkhratsky A (2009) Evolutionary origins of the purinergic signalling system. Acta Physiol 195:415–447. https://doi.org/10.1111/j.1748-1716.2009.01957.x

    Article  CAS  Google Scholar 

  23. KelvinC A, Webb TE, Evans RJ, Ennion SJ (2004) Functional characterization of a P2X receptor from Schistosoma mansoni. J Biol Chem 279:41650–41657. https://doi.org/10.1074/jbc.M408203200

    Article  CAS  Google Scholar 

  24. Sreedharan S, Shaik JH, Olszewski PK et al (2010) Glutamate, aspartate and nucleotide transporters in the SLC17 family form four main phylogenetic clusters: evolution and tissue expression. BMC Genomics 11:17. https://doi.org/10.1186/1471-2164-11-17

    Article  CAS  Google Scholar 

  25. Hobert O (2013) The neuronal genome of Caenorhabditis elegans. WormBook 1–106 https://doi.org/10.1895/wormbook.1.161.1

  26. Xie X, Shang L, Ye S, Chen C (2020) The Protective effect of adenosine-preconditioning on paraquat-induced damage in Caenorhabditis elegans. Dose-Response 18:155932582093532. https://doi.org/10.1177/1559325820935329

    Article  CAS  Google Scholar 

  27. Machado ML, Arantes LP, Gubert P et al (2018) Ilex paraguariensis modulates fat metabolism in Caenorhabditis elegans through purinergic system (ADOR-1) and nuclear hormone receptor (NHR-49) pathways. PLoS ONE 13:e0204023. https://doi.org/10.1371/journal.pone.0204023

    Article  CAS  Google Scholar 

  28. Bridi JC, de Barros AGA, Sampaio LR et al (2015) Lifespan extension induced by caffeine in Caenorhabditis elegans is partially dependent on adenosine signaling. Front Aging Neurosci 7:220. https://doi.org/10.3389/fnagi.2015.00220

    Article  CAS  Google Scholar 

  29. Arantes LP, Machado ML, Zamberlan DC et al (2018) Mechanisms involved in anti-aging effects of guarana (Paullinia cupana) in Caenorhabditis elegans. Braz J Med Biol Res. https://doi.org/10.1590/1414-431x20187552

    Article  Google Scholar 

  30. Manalo RVM, Medina PMB (2018) Caffeine protects dopaminergic neurons from dopamine-induced neurodegeneration via synergistic adenosine-dopamine D2-like receptor interactions in transgenic Caenorhabditis elegans. Front Neurosci 12:e00137. https://doi.org/10.3389/fnins.2018.00137

    Article  Google Scholar 

  31. Polli JR, Dobbins DL, Kobet RA et al (2015) Drug-dependent behaviors and nicotinic acetylcholine receptor expressions in Caenorhabditis elegans following chronic nicotine exposure. Neurotoxicology 47:27–36. https://doi.org/10.1016/j.neuro.2014.12.005

    Article  CAS  Google Scholar 

  32. Roussel N, Sprenger J, Tappan SJ, Glaser JR (2014) Robust tracking and quantification of C. elegans body shape and locomotion through coiling, entanglement, and omega bends. Worm 3:e982437. https://doi.org/10.4161/21624054.2014.982437

    Article  Google Scholar 

  33. Gubert P, Aguiar GC, Mourão T et al (2013) Behavioral and metabolic effects of the atypical antipsychotic ziprasidone on the nematode Caenorhabditis elegans. PLoS ONE 8:e74780. https://doi.org/10.1371/journal.pone.0074780

    Article  CAS  Google Scholar 

  34. Stefanello ST, Gubert P, Puntel B et al (2015) Protective effects of novel organic selenium compounds against oxidative stress in the nematode Caenorhabditis elegans. Toxicol Rep 2:961–967. https://doi.org/10.1016/j.toxrep.2015.06.010

    Article  CAS  Google Scholar 

  35. Gill MS, Olsen A, Sampayo JN, Lithgow GJ (2003) An automated high-throughput assay for survival of the nematode Caenorhabditis elegans. Free Radic Biol Med 35:558–565. https://doi.org/10.1016/S0891-5849(03)00328-9

    Article  CAS  Google Scholar 

  36. Zamberlan DC, Arantes LP, Machado ML et al (2014) Diphenyl-diselenide suppresses amyloid-β peptide in Caenorhabditis elegans model of Alzheimer’s disease. Neuroscience 278:40–50. https://doi.org/10.1016/j.neuroscience.2014.07.068

    Article  CAS  Google Scholar 

  37. da Silveira TL, Zamberlan DC, Arantes LP et al (2018) Quinolinic acid and glutamatergic neurodegeneration in Caenorhabditis elegans. Neurotoxicology 67:94–101. https://doi.org/10.1016/j.neuro.2018.04.015

    Article  CAS  Google Scholar 

  38. Schafer WR, Sanchez BM, Kenyon CJ (1996) Genes affecting sensitivity to serotonin in Caenorhabditis elegans. Genetics 143:1219–1230. https://doi.org/10.1093/genetics/143.3.1219

    Article  CAS  Google Scholar 

  39. Duerr JS, Gaskin J, Rand JB (2001) Identified neurons in C. elegans coexpress vesicular transporters for acetylcholine and monoamines. Am J Physiol Cell Physiol 280:C1616–C1622. https://doi.org/10.1152/ajpcell.2001.280.6.C1616

    Article  CAS  Google Scholar 

  40. Fernandez RW, Wei K, Wang EY et al (2020) Cellular expression and functional roles of all 26 neurotransmitter GPCRs in the C. elegans egg-laying circuit. J Neurosci 40:7475–7488. https://doi.org/10.1523/JNEUROSCI.1357-20.2020

    Article  CAS  Google Scholar 

  41. Franks DM, Izumikawa T, Kitagawa H et al (2006) C. elegans pharyngeal morphogenesis requires both de novo synthesis of pyrimidines and synthesis of heparan sulfate proteoglycans. Dev Biol 296:409–420. https://doi.org/10.1016/j.ydbio.2006.06.008

    Article  CAS  Google Scholar 

  42. Doncaster CC (1962) Nematode feeding mechanisms. 1 observations on rhabditis and pelodera. Nematologica 8:313–320. https://doi.org/10.1163/187529262X00125

    Article  Google Scholar 

  43. Seymour MK, Wright KA, Doncaster CC (2009) The action of the anterior feeding apparatus of Caenorhabditis elegans (Nematoda: Rhabditida). J Zool 201:527–539. https://doi.org/10.1111/j.1469-7998.1983.tb05074.x

    Article  Google Scholar 

  44. Papaioannou S, Marsden D, Franks CJ et al (2005) Role of a FMRFamide-like family of neuropeptides in the pharyngeal nervous system of Caenorhabditis elegans. J Neurobiol 65:304–319. https://doi.org/10.1002/neu.20201

    Article  CAS  Google Scholar 

  45. Cunha RA, Johansson B, Fredholm BB et al (1995) Adenosine A2A receptors stimulate acetylcholine release from nerve terminals of the rat hippocampus. Neurosci Lett 196:41–44. https://doi.org/10.1016/0304-3940(95)11833-I

    Article  CAS  Google Scholar 

  46. Kurokawa M, Kirk IP, Kirkpatrick KA et al (1994) Inhibition by KF17837 of adenosine A2A receptor-mediated modulation of striatal GABA and ACh release. Br J Pharmacol 113:43–48. https://doi.org/10.1111/j.1476-5381.1994.tb16171.x

    Article  CAS  Google Scholar 

  47. Burnstock G (1996) Purinoceptors: ontogeny and phylogeny. Drug Dev Res 39:204–242. https://doi.org/10.1002/(SICI)1098-2299(199611/12)39:3/4%3c204::AID-DDR2%3e3.0.CO;2-V

    Article  CAS  Google Scholar 

  48. Dal Santo P, Logan MA, Chisholm AD, Jorgensen EM (1999) The inositol trisphosphate receptor regulates a 50-second behavioral rhythm in C. elegans. Cell 98:757–767. https://doi.org/10.1016/S0092-8674(00)81510-X

    Article  CAS  Google Scholar 

  49. Avery L, Thomas JH (1997) Feeding and defecation, chap 24. In: Riddle DL, Blumenthal T, Meyer BJ, Priess JR (eds) C. elegans II, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor (NY)

    Google Scholar 

  50. Thomas JH (1990) Genetic analysis of defecation in Caenorhabditis elegans. Genetics 124:855–872. https://doi.org/10.1093/genetics/124.4.855

    Article  CAS  Google Scholar 

  51. Mclntire SL, Jorgensen E, Kaplan J, Horvitz HR (1993) The GABAergic nervous system of Caenorhabditis elegans. Nature 364:337–341. https://doi.org/10.1038/364337a0

    Article  Google Scholar 

  52. Ségalat L, Elkes DA, Kaplan JM (1995) Modulation of serotonin-controlled behaviors by Go in Caenorhabditis elegans. Science 267:1648–1651. https://doi.org/10.1126/science.7886454

    Article  Google Scholar 

  53. Croll NA (2009) Components and patterns in the behaviour of the nematode Caenorhabditis elegans. J Zool 176:159–176. https://doi.org/10.1111/j.1469-7998.1975.tb03191.x

    Article  Google Scholar 

  54. Gray JM, Hill JJ, Bargmann CI (2005) A circuit for navigation in Caenorhabditis elegans. Proc Natl Acad Sci 102:3184–3191. https://doi.org/10.1073/pnas.0409009101

    Article  CAS  Google Scholar 

  55. Driscoll M, Kaplan J (1997) Mechanotransduction

  56. Bargmann CI, Mori I (1997) Chemotaxis and thermotaxis

  57. Schuske K, Beg AA, Jorgensen EM (2004) The GABA nervous system in C. elegans. Trends Neurosci 27:407–414. https://doi.org/10.1016/j.tins.2004.05.005

    Article  CAS  Google Scholar 

  58. Duarte-Araújo M, Nascimento C, Alexandrina Timóteo M et al (2004) Dual effects of adenosine on acetylcholine release from myenteric motoneurons are mediated by junctional facilitatory A2A and extrajunctional inhibitory A1 receptors. Br J Pharmacol 141:925–934. https://doi.org/10.1038/sj.bjp.0705697

    Article  CAS  Google Scholar 

  59. Saransaari P, Oja SS (2005) GABA release modified by adenosine receptors in mouse hippocampal slices under normal and ischemic conditions. Neurochem Res 30:467–473. https://doi.org/10.1007/s11064-005-2682-4

    Article  CAS  Google Scholar 

  60. Omura DT, Clark DA, Samuel ADT, Horvitz HR (2012) Dopamine signaling is essential for precise rates of locomotion by C. elegans. PLoS ONE 7:e38649. https://doi.org/10.1371/journal.pone.0038649

    Article  CAS  Google Scholar 

  61. Okada M, Mizuno K, Kaneko S (1996) Adenosine A1 and A2 receptors modulate extracellular dopamine levels in rat striatum. Neurosci Lett 212:53–56. https://doi.org/10.1016/0304-3940(96)12780-4

    Article  CAS  Google Scholar 

  62. Sawin ER, Ranganathan R, Horvitz HR (2000) C. elegans locomotory rate is modulated by the environment through a dopaminergic pathway and by experience through a serotonergic pathway. Neuron 26:619–631. https://doi.org/10.1016/S0896-6273(00)81199-X

    Article  CAS  Google Scholar 

  63. Selye H (1976) Forty years of stress research: principal remaining problems and misconceptions. Can Med Assoc J 115:53–56

    CAS  Google Scholar 

  64. Lithgow GJ, Walker GA (2002) Stress resistance as a determinate of C. elegans lifespan. Mech Ageing Dev 123:765–771. https://doi.org/10.1016/S0047-6374(01)00422-5

    Article  Google Scholar 

  65. Ahmad T, Suzuki YJ (2019) Juglone in oxidative stress and cell signaling. Antioxidants 8:91. https://doi.org/10.3390/antiox8040091

    Article  CAS  Google Scholar 

  66. Lin X-X, Sen I, Janssens GE et al (2018) DAF-16/FOXO and HLH-30/TFEB function as combinatorial transcription factors to promote stress resistance and longevity. Nat Commun 9:4400. https://doi.org/10.1038/s41467-018-06624-0

    Article  CAS  Google Scholar 

  67. Xu C, Li CY-T, Kong A-NT (2005) Induction of phase I, II and III drug metabolism/transport by xenobiotics. Arch Pharmacal Res 28:249–268. https://doi.org/10.1007/BF02977789

    Article  CAS  Google Scholar 

  68. Sarkadi B, Homolya L, Szakács G, Váradi A (2006) Human multidrug resistance ABCB and ABCG transporters: participation in a chemoimmunity defense system. Physiol Rev 86:1179–1236. https://doi.org/10.1152/physrev.00037.2005

    Article  CAS  Google Scholar 

  69. Jasper H (2008) SKNy worms and long life. Cell 132:915–916. https://doi.org/10.1016/j.cell.2008.03.002

    Article  CAS  Google Scholar 

  70. Tullet JMA, Green JW, Au C et al (2017) The SKN-1/Nrf2 transcription factor can protect against oxidative stress and increase lifespan in C. elegans by distinct mechanisms. Aging Cell 16:1191–1194. https://doi.org/10.1111/acel.12627

    Article  CAS  Google Scholar 

  71. An JH (2003) SKN-1 links C. elegans mesendodermal specification to a conserved oxidative stress response. Genes Dev 17:1882–1893. https://doi.org/10.1101/gad.1107803

    Article  CAS  Google Scholar 

  72. An JH, Vranas K, Lucke M et al (2005) Regulation of the Caenorhabditis elegans oxidative stress defense protein SKN-1 by glycogen synthase kinase-3. Proc Natl Acad Sci 102:16275–16280. https://doi.org/10.1073/pnas.0508105102

    Article  CAS  Google Scholar 

  73. Kenyon C (2005) The plasticity of aging: insights from long-lived mutants. Cell 120:449–460. https://doi.org/10.1016/j.cell.2005.02.002

    Article  CAS  Google Scholar 

  74. Sun X, Chen W-D, Wang Y-D (2017) DAF-16/FOXO transcription factor in aging and longevity. Front Pharmacol 8:548. https://doi.org/10.3389/fphar.2017.00548

    Article  CAS  Google Scholar 

  75. Friedman B, Corciulo C, Castro CM, Cronstein BN (2021) Adenosine A2A receptor signaling promotes FoxO associated autophagy in chondrocytes. Sci Rep 11:968. https://doi.org/10.1038/s41598-020-80244-x

    Article  CAS  Google Scholar 

  76. Choi M, Moon S, Lee S et al (2019) [Corrigendum] Adenosine induces intrinsic apoptosis via the PI3K/Akt/mTOR signaling pathway in human pharyngeal squamous carcinoma FaDu cells. Oncol Lett. https://doi.org/10.3892/ol.2019.10014

    Article  Google Scholar 

  77. Deussen A (2003) Adenosine the missing link to understanding homocysteine pathogenicity or more smoke on the horizon? Cardiovasc Res 59:259–261. https://doi.org/10.1016/S0008-6363(03)00478-4

    Article  CAS  Google Scholar 

  78. Vizán P, di Croce L, Aranda S (2021) Functional and pathological roles of AHCY. Front Cell Dev Biol 9:654344. https://doi.org/10.3389/fcell.2021.654344

    Article  Google Scholar 

  79. Clarke S, Banfield K (2001) S-adenosylmethionine-dependent methyltransferases”, in Homocysteine in Health and Disease. In: Carmel R, Jackobsen DW (eds) Homocysteine in Health and Disease, 1st edn. Cambridge University Press, Cambridge, pp 63–78

    Google Scholar 

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Funding

This work was supported by Fundação de Amparo à pesquisa do Estado do Rio Grande do Sul (FAPERGS), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Institutos Nacionais de Ciência e Tecnologia (INCT), “Programa de Apoio a Núcleos Emergentes” (PRONEM) and MCTI/CNPq [Grant numbers 472669/2011-7, 475896/2012-2]. Programa de Excelência Acadêmica (PROEX) Process number 88882.182139/2018-01.

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  1. Departamento de Bioquímica e Biologia Molecular, Programa de Pós-graduação em Ciências Biológicas: Bioquímica Toxicológica, Centro de Ciências Naturais e Exatas, Universidade Federal de Santa Maria, Av. Roraima nº 1000, Camobi, Santa Maria, RS, 97105-900, Brazil

    Thayanara Cruz da Silva, Tássia Limana da Silveira, Luiza Venturini dos Santos, Rodrigo Pereira Martins, Félix Alexandre Antunes Soares & Cristiane Lenz Dalla Corte

  2. Instituto Latino-Americano de Ciências da Vida e da Natureza, Universidade Federal da Integração Latino-Americana, Foz do Iguaçu, Paraná, 85866-000, Brazil

    Leticia Priscila Arantes

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  1. Thayanara Cruz da Silva
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All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by TCS, TLS, LVS, LPA, RPM, FAAS and CLDC. The first draft of the manuscript was written by TCS and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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da Silva, T.C., da Silveira, T.L., dos Santos, L.V. et al. Exogenous Adenosine Modulates Behaviors and Stress Response in Caenorhabditis elegans. Neurochem Res 48, 117–130 (2023). https://doi.org/10.1007/s11064-022-03727-5

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