Skip to main content
SpringerLink
Log in

P2X7 receptors and pannexin1 hemichannels shape presynaptic transmission

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

Abstract

Over the last decades, since the discovery of ATP as a transmitter, accumulating evidence has been reported about the role of this nucleotide and purinergic receptors, in particular P2X7 receptors, in the modulation of synaptic strength and plasticity. Purinergic signaling has emerged as a crucial player in orchestrating the molecular interaction between the components of the tripartite synapse, and much progress has been made in how this neuron-glia interaction impacts neuronal physiology under basal and pathological conditions. On the other hand, pannexin1 hemichannels, which are functionally linked to P2X7 receptors, have appeared more recently as important modulators of excitatory synaptic function and plasticity under diverse contexts. In this review, we will discuss the contribution of ATP, P2X7 receptors, and pannexin hemichannels to the modulation of presynaptic strength and its impact on motor function, sensory processing, synaptic plasticity, and neuroglial communication, with special focus on the P2X7 receptor/pannexin hemichannel interplay. We also address major hypotheses about the role of this interaction in physiological and pathological circumstances.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

Data availability

Not applicable.

References

  1. Burnstock G (1976) Purinergic receptors. J Theor Biol 62:491–503. https://doi.org/10.1016/0022-5193(76)90133-8

    Article  CAS  PubMed  Google Scholar 

  2. Burnstock G, Satchell DG, Smythe A (1972) A comparison of the excitatory and inhibitory effects of non-adrenergic, non-cholinergic nerve stimulation and exogenously applied ATP on a variety of smooth muscle preparations from different vertebrate species. Br J Pharmacol 46:234–242. https://doi.org/10.1111/j.1476-5381.1972.tb06868.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Burnstock G (2007) Physiology and pathophysiology of purinergic neurotransmission. Physiol Rev 87:659–797. https://doi.org/10.1152/physrev.00043.2006

    Article  CAS  PubMed  Google Scholar 

  4. Mori M, Heuss C, Gähwiler BH, Gerber U (2001) Fast synaptic transmission mediated by P2X receptors in CA3 pyramidal cells of rat hippocampal slice cultures. J Physiol 535:115–123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. North R, a, (2002) Molecular physiology of P2X receptors. Physiol Rev 82:1013–1067. https://doi.org/10.1152/physrev.00015.2002

    Article  CAS  PubMed  Google Scholar 

  6. North RA, Verkhratsky A (2006) Purinergic transmission in the central nervous system. Eur J Physiol 452:479–485. https://doi.org/10.1007/s00424-006-0060-y

    Article  CAS  Google Scholar 

  7. Cunha RA, Vizi ES, Ribeiro JA, Sebastião AM (1996) Preferential release of ATP and its extracellular catabolism as a source of adenosine upon high- but not low-frequency stimulation of rat hippocampal Slices. J Neurochem 67:2180–2187. https://doi.org/10.1046/j.1471-4159.1996.67052180.x

    Article  CAS  PubMed  Google Scholar 

  8. Wieraszko A, Goldsmith G, Seyfried TN (1989) Stimulation-dependent release of adenosine triphosphate from hippocampal slices. Brain Res 485:244–250. https://doi.org/10.1016/0006-8993(89)90567-2

    Article  CAS  PubMed  Google Scholar 

  9. Kang J, Kang N, Lovatt D et al (2008) Connexin 43 hemichannels are permeable to ATP. J Neurosci 28:4702–4711. https://doi.org/10.1523/jneurosci.5048-07.2008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Dahl G (2015) ATP release through pannexon channels. Phil Trans R Soc B 370. https://doi.org/10.1098/rstb.2014.0191

  11. Burnstock G, Cocks T, Crowe R (1978) Evidence for purinergic innervation of the anococcygeus muscle. Br J Pharmacol 64:13–20. https://doi.org/10.1111/j.1476-5381.1978.tb08635.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. North RA, Barnard EA (1997) Nucleotide receptors. Curr Opin Neurobiol 7:346–357. https://doi.org/10.1016/s0959-4388(97)80062-1

    Article  CAS  PubMed  Google Scholar 

  13. Jarvis MF, Khakh BS (2009) Neuropharmacology ATP-gated P2X cation-channels. Neuropharmacology 56:208–215. https://doi.org/10.1016/j.neuropharm.2008.06.067

    Article  CAS  PubMed  Google Scholar 

  14. Martínez-cuesta MÁ, Blanch-ruiz MA, Ortega-luna R et al (2020) Structural and functional basis for understanding the biological significance of P2X7 receptor. Int J Mol Sci 21:1–23. https://doi.org/10.3390/ijms21228454

    Article  CAS  Google Scholar 

  15. Sperlágh B, Vizi ES, Wirkner K, Illes P (2006) P2X7 receptors in the nervous system. Prog Neurobiol 78:327–346. https://doi.org/10.1016/j.pneurobio.2006.03.007

    Article  CAS  PubMed  Google Scholar 

  16. Sluyter R (2017) The P2X7 Receptor. Adv Exp Med Biol 1051:17–53. https://doi.org/10.1007/5584_2017_59

    Article  CAS  PubMed  Google Scholar 

  17. Surprenant A, Kawashima E, Rassendren F et al (1996) The cytolytic P2z receptor for extracellular ATP identified as a P2x receptor (P2X7). Science 272(80):735–738. https://doi.org/10.1126/science.272.5262.735

    Article  CAS  PubMed  Google Scholar 

  18. Sperlágh B, Illes P (2014) P2X7 receptor : an emerging target in central nervous system diseases. Trends Pharmacol Sci 35:537–547. https://doi.org/10.1016/j.tips.2014.08.002

    Article  CAS  PubMed  Google Scholar 

  19. Tewari M, Seth P (2015) Emerging role of P2X7 receptors in CNS health and disease. Ageing Res Rev 24:328–342. https://doi.org/10.1016/j.arr.2015.10.001

    Article  CAS  PubMed  Google Scholar 

  20. Khakh BS, Lester HA (1999) Dynamic selectivity filters in ion channels. Neuron 23:653–658. https://doi.org/10.1016/S0896-6273(01)80025-8

    Article  CAS  PubMed  Google Scholar 

  21. Virginio C, Mackenzie A, Rassendren FA et al (1999) Pore dilation of neuronal P2X receptor channels. Nat Neurosci 2:315–321. https://doi.org/10.1038/7225

    Article  CAS  PubMed  Google Scholar 

  22. Virginio C, Mackenzie A, North RA et al (1999) Kinetics of cell lysis, dye uptake and permeability changes in cells expressing the rat P2XÝ receptor. J Physiol 519:335–346. https://doi.org/10.1111/j.1469-7793.1999.0335m.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Hibell AD, Kidd EJ, Chessell IP et al (2000) Apparent species differences in the kinetic properties of P2X 7 receptors. Br J Pharmacol 130:167–173. https://doi.org/10.1038/sj.bjp.0703302

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Pelegrin P, Surprenant A (2006) Pannexin-1 mediates large pore formation and interleukin-1 release by the ATP-gated P2X7 receptor. EMBO J 25:5071–5082. https://doi.org/10.1038/sj.emboj.7601378

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Di Virgilio F, Schmalzing G, Markwardt F (2018) The elusive P2X7 macropore. Trends Cell Biol 28:392–404. https://doi.org/10.1016/j.tcb.2018.01.005

    Article  CAS  PubMed  Google Scholar 

  26. Ugur M, Ugur Ö (2019) A mechanism-based approach to P2X7 receptor action. Mol Pharmacol 95:442–450. https://doi.org/10.1124/mol.118.115022

    Article  CAS  PubMed  Google Scholar 

  27. Di Virgilio F, Giuliani AL, Vultaggio-Poma V et al (2018) Non-nucleotide agonists triggering P2X7 receptor activation and pore formation. Front Pharmacol 9:1–10. https://doi.org/10.3389/fphar.2018.00039

    Article  CAS  Google Scholar 

  28. Di Virgilio F, Dal Ben D, Sarti AC et al (2017) The P2X7 receptor in infection and inflammation. Immunity 47:15–31. https://doi.org/10.1016/j.immuni.2017.06.020

    Article  CAS  PubMed  Google Scholar 

  29. Ferrari D, Pizzirani C, Adinolfi E et al (2004) The antibiotic polymyxin B modulates P2X7 receptor function. J Immunol 173:4652–4660. https://doi.org/10.4049/jimmunol.173.7.4652

    Article  CAS  PubMed  Google Scholar 

  30. Karasawa A, Michalski K, Mikhelzon P, Kawate T (2017) The P2X7 receptor forms a dye-permeable pore independent of its intracellular domain but dependent on membrane lipid composition. Elife 6:1–22. https://doi.org/10.7554/eLife.31186

    Article  Google Scholar 

  31. Duan S, Neary J (2006) P2X7 receptors: properties and relevance to CNS function. Glia 54:738–746. https://doi.org/10.1002/glia

    Article  PubMed  Google Scholar 

  32. Kim M, Jiang L, Wilson HL et al (2001) Proteomic and functional evidence for a P2X7 receptor signalling complex. EMBO J 20:6347–6358. https://doi.org/10.1093/emboj/20.22.6347

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Denlinger LC, Fisette PL, Sommer JA et al (2001) Cutting Edge: The nucleotide receptor P2X7 contains multiple protein- and lipid-interaction motifs including a potential binding site for bacterial lipopolysaccharide. J Immunol 164:1871–1876. https://doi.org/10.4049/jimmunol.167.4.1871

    Article  Google Scholar 

  34. Armstrong JN, Brust TB, Lewis RG, MacVicar B a (2002) Activation of presynaptic P2X7-like receptors depresses mossy fiber-CA3 synaptic transmission through p38 mitogen-activated protein kinase. J Neurosci 22:5938–5945 20026618

  35. Panchin Y, Kelmanson I, Matz M et al (2000) A ubiquitous family of putative gap junction molecules. Curr Biol 10:473–474. https://doi.org/10.1016/s0960-9822(00)00576-5

    Article  Google Scholar 

  36. Bruzzone R, Hormuzdi SG, Barbe MT et al (2003) Pannexins, a family of gap junction proteins expressed in brain. Proc Natl Acad Sci 100:13644–13649. https://doi.org/10.1073/pnas.2233464100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Panchin YV (2005) Evolution of gap junction proteins – the pannexin alternative. J Exp Biol 208:1415–1419. https://doi.org/10.1242/jeb.01547

    Article  CAS  PubMed  Google Scholar 

  38. Baranova A, Ivanov D, Petrash N et al (2004) The mammalian pannexin family is homologous to the invertebrate innexin gap junction proteins. Genomics 83:706–716. https://doi.org/10.1016/j.ygeno.2003.09.025

    Article  CAS  PubMed  Google Scholar 

  39. Ray A, Zoidl G, Weickert S et al (2005) Site-specific and developmental expression of pannexin1 in the mouse nervous system. Eur J Neurosci 21:3277–3290. https://doi.org/10.1111/j.1460-9568.2005.04139.x

    Article  PubMed  Google Scholar 

  40. Vogt A, Hormuzdi SG, Monyer H (2005) Pannexin1 and pannexin2 expression in the developing and mature rat brain. Mol Brain Res 141:113–120. https://doi.org/10.1016/j.molbrainres.2005.08.002

    Article  CAS  PubMed  Google Scholar 

  41. Yeung AK, Patil CS, Jackson MF (2020) Pannexin-1 in the CNS: emerging concepts in health and disease. J Neurochem 154:468–485. https://doi.org/10.1111/jnc.15004

    Article  CAS  PubMed  Google Scholar 

  42. Zoidl G, Petrasch-Parwez E, Ray A et al (2007) Localization of the pannexin1 protein at postsynaptic sites in the cerebral cortex and hippocampus. Neuroscience 146:9–16. https://doi.org/10.1016/j.neuroscience.2007.01.061

    Article  CAS  PubMed  Google Scholar 

  43. Locovei S, Bao L, Dahl G (2006) Pannexin 1 in erythrocytes: function without a gap. Proc Natl Acad Sci U S A 103:7655–7659. https://doi.org/10.1073/pnas.0601037103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Ambrosi C, Gassmann O, Pranskevich JN et al (2010) Pannexin1 and pannexin2 channels show quaternary similarities to connexons and different oligomerization numbers from each other. J Biol Chem 285:24420–24431. https://doi.org/10.1074/jbc.M110.115444

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Michalski K, Syrjanen JL, Henze E et al (2020) The Cryo-EM structure of a pannexin 1 reveals unique motifs for ion selection and inhibition. Elife 9:1–14. https://doi.org/10.7554/eLife.54670

    Article  Google Scholar 

  46. Deng Z, He Z, Maksaev G et al (2020) Cryo-EM structures of the ATP release channel pannexin 1. Nat Struct Mol Biol 27:373–381. https://doi.org/10.1038/s41594-020-0401-0

    Article  CAS  PubMed  Google Scholar 

  47. Qu R, Dong L, Zhang J et al (2020) Cryo-EM structure of human heptameric pannexin 1 channel. Cell Res 30:446–448. https://doi.org/10.1038/s41422-020-0298-5

    Article  PubMed  PubMed Central  Google Scholar 

  48. Ruan Z, Orozco IJ, Du J (2020) Structures of human pannexin 1 reveal ion pathways and mechanism of gating. Nature 584:646–651. https://doi.org/10.1038/s41586-020-2357-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Dahl G, Locovei S (2006) Pannexin: to gap or not to gap, is that a question? IUBMB Life 58:409–419. https://doi.org/10.1080/15216540600794526

    Article  CAS  PubMed  Google Scholar 

  50. Chiu Y, Ravichandran KS, Bayliss DA (2015) Intrinsic properties and regulation of pannexin 1 channel. Channels 8:1–7. https://doi.org/10.4161/chan.27545

    Article  CAS  Google Scholar 

  51. Bao L, Locovei S, Dahl G (2004) Pannexin membrane channels are mechanosensitive conduits for ATP. FEBS Lett 572:65–68. https://doi.org/10.1016/j.febslet.2004.07.009

    Article  CAS  PubMed  Google Scholar 

  52. Thompson RJ, Zhou N, Mac Vicar BA (2006) Ischemia opens neuronal gap junction hemichannels. Science (80- ) 312:924–927. https://doi.org/10.1126/science.1126241

    Article  CAS  Google Scholar 

  53. Iglesias R, Dahl G, Qiu F et al (2009) Pannexin 1: the molecular substrate of astrocyte “hemichannels.” J Neurosci 29:7092–7097. https://doi.org/10.1523/jneurosci.6062-08.2009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Suadicani SO, Iglesias R, Wang J et al (2012) ATP signaling is deficient in cultured pannexin1-null mouse astrocytes. Glia 60:1106–1116. https://doi.org/10.1002/glia.22338

    Article  PubMed  PubMed Central  Google Scholar 

  55. Chiu YH, Schappe MS, Desai BN, Bayliss DA (2018) Revisiting multimodal activation and channel properties of pannexin 1. J Gen Physiol 150:19–39. https://doi.org/10.1085/jgp.201711888

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Ma W, Compan V, Zheng W et al (2012) Pannexin 1 forms an anion-selective channel. Pflugers Arch Eur J Physiol 463:585–592. https://doi.org/10.1007/s00424-012-1077-z

    Article  CAS  Google Scholar 

  57. Romanov RA, Bystrova MF, Rogachevskaya OA et al (2012) The ATP permeability of pannexin 1 channels in a heterologous system and in mammalian taste cells is dispensable. J Cell Sci 125:5514–5523. https://doi.org/10.1242/jcs.111062

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Garré JM, Bukauskas FF, Bennett MVL (2022) Single channel properties of pannexin-1 and connexin-43 hemichannels and P2X7 receptors in astrocytes cultured from rodent spinal cords. Glia 70:2260–2275. https://doi.org/10.1002/glia.24250

    Article  CAS  PubMed  Google Scholar 

  59. Chiu Y, Jin X, Medina CB et al (2017) A quantized mechanism for activation of pannexin channels. Nat Commun. https://doi.org/10.1038/ncomms14324

    Article  PubMed  PubMed Central  Google Scholar 

  60. Dahl G (2018) The Pannexin1 membrane channel: distinct conformations and functions. FEBS Lett 592:3201–3209. https://doi.org/10.1002/1873-3468.13115

    Article  CAS  PubMed  Google Scholar 

  61. Dahl G, Keane RW (2012) Pannexin : from discovery to bedside in 11 4 years ? Brain Res 1487:150–159. https://doi.org/10.1016/j.brainres.2012.04.058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Cheung G, Chever O, Rouach N (2014) Connexons and pannexons: newcomers in neurophysiology. Front Cell Neurosci 8:1–19. https://doi.org/10.3389/fncel.2014.00348

    Article  Google Scholar 

  63. Abudara V, Retamal MA, Del Rio R, Orellana JA (2018) Synaptic functions of hemichannels and pannexons: a double-edged sword. Front Mol Neurosci 11:1–24. https://doi.org/10.3389/fnmol.2018.00435

    Article  CAS  Google Scholar 

  64. Barbe MT, Monyer H, Bruzzone R (2006) Cell-cell communication beyond connexins: the pannexin channels. Physiology 21:103–114. https://doi.org/10.1152/physiol.00048.2005

    Article  CAS  PubMed  Google Scholar 

  65. Sandilos JK, Bayliss DA (2012) Physiological mechanisms for the modulation of pannexin 1 channel activity. J Physiol 590:6257–6266. https://doi.org/10.1113/jphysiol.2012.240911

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Isakson BE, Thompson RJ (2014) Pannexin-1 as a potentiator of ligand-gated receptor signaling. Channels 8:118–123. https://doi.org/10.4161/chan.27978

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Whyte-fagundes P, Zoidl G (2017) Mechanisms of pannexin1 channel gating and regulation. BBA - Biomembr 1860:65–71. https://doi.org/10.1016/j.bbamem.2017.07.009

    Article  CAS  Google Scholar 

  68. Thompson RJ, Jackson MF, Olah ME et al (2008) Activation of pannexin-1 hemichannels augments aberrant bursting in the hippocampus. Science 322:1555–1559. https://doi.org/10.1126/science.1165209

    Article  CAS  PubMed  Google Scholar 

  69. Garré JM, Retamal MA, Cassina P et al (2010) FGF-1 induces ATP release from spinal astrocytes in culture and opens pannexin and connexin hemichannels. Proc Natl Acad Sci U S A 107:22659–22664. https://doi.org/10.1073/pnas.1013793107

    Article  PubMed  PubMed Central  Google Scholar 

  70. Billaud M, Lohman AW, Straub AC et al (2011) Pannexin1 regulates alpha1-adrenergic receptor– mediated vasoconstriction. Circ Res 109:80–85. https://doi.org/10.1161/CIRCRESAHA.110.237594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Orellana JA, Figueroa XF, Sanchez HA et al (2011) Hemichannels in the neurovascular unit and white matter under normal and inflamed conditions. CNS Neurol Disord - Drug Targets 10:404–414. https://doi.org/10.2174/187152711794653869

    Article  CAS  PubMed  Google Scholar 

  72. Locovei S, Scemes E, Qiu F et al (2007) Pannexin1 is part of the pore forming unit of the P2X7 receptor death complex. FEBS Lett 581:483–488. https://doi.org/10.1016/j.biotechadv.2011.08.021.Secreted

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Locovei S, Wang J, Dahl G (2006) Activation of pannexin 1 channels by ATP through P2Y receptors and by cytoplasmic calcium. FEBS Lett 580:239–244. https://doi.org/10.1016/j.febslet.2005.12.004

    Article  CAS  PubMed  Google Scholar 

  74. Boyce AKJ, Kim MS, Wicki-Stordeur LE, Swayne LA (2015) ATP stimulates pannexin 1 internalization to endosomal compartments. Biochem J 470:319–330. https://doi.org/10.1042/BJ20141551

    Article  CAS  PubMed  Google Scholar 

  75. Boyce AKJ, Swayne LA (2017) P2X7 receptor crosstalk regulates ATP-induced pannexin 1 internalization Andrew. Biochem J 474:2133–2144. https://doi.org/10.1042/BCJ20170257

    Article  CAS  PubMed  Google Scholar 

  76. Qiu F, Dahl G (2009) A permeant regulating its permeation pore: inhibition of pannexin 1 channels by ATP. Am J Physiol - Cell Physiol 296:250–255. https://doi.org/10.1152/ajpcell.00433.2008

    Article  CAS  Google Scholar 

  77. Flores-Muñoz C, García-Rojas F, Pérez MA et al (2022) The long-term pannexin 1 ablation produces structural and functional modifications in hippocampal neurons. Cells 11:1–31. https://doi.org/10.3390/cells11223646

    Article  CAS  Google Scholar 

  78. Lai CPK, Bechberger JF, Thompson RJ et al (2007) Tumor-suppressive effects of pannexin 1 in C6 glioma cells. Cancer Res 67:1545–1554. https://doi.org/10.1158/0008-5472.CAN-06-1396

    Article  CAS  PubMed  Google Scholar 

  79. Vanden Abeele F, Bidaux G, Gordienko D et al (2006) Functional implications of calcium permeability of the channel formed by pannexin 1. J Cell Biol 174:535–546. https://doi.org/10.1083/jcb.200601115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Boassa D, Ambrosi C, Qiu F et al (2007) Pannexin1 channels contain a glycosylation site that targets the hexamer to the plasma membrane. J Biol Chem 282:31733–31743. https://doi.org/10.1074/jbc.M702422200

    Article  CAS  PubMed  Google Scholar 

  81. Sosinsky GE, Boassa D, Dermietzel R et al (2011) Pannexin channels are not gap junction hemichannels. Channels 5:193–197. https://doi.org/10.4161/chan.5.3.15765

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Penuela S, Simek J, Thompson RJ (2014) Regulation of pannexin channels by post-translational modifications. In: FEBS Letters 1411–1415. https://doi.org/10.1016/j.febslet.2014.01.028

  83. Sahu G, Sukumaran S, Bera AK (2014) Pannexins form gap junctions with electrophysiological and pharmacological properties distinct from connexins. Sci Rep 4:1–9. https://doi.org/10.1038/srep04955

    Article  CAS  Google Scholar 

  84. Palacios-Prado N, Soto PA, Lopez X et al (2022) Endogenous pannexin1 channels form functional intercellular cell-cell channels with characteristic voltage-dependent properties. Proc Natl Acad Sci U S A 119:1–11. https://doi.org/10.1073/pnas.2202104119

    Article  CAS  Google Scholar 

  85. Suadicani SO, Brosnan CF, Scemes E (2006) P2X7 Receptors mediate ATP release and amplification of astrocytic intercellular Ca2+ signaling. J Neurosci 26:1378–1385. https://doi.org/10.1523/JNEUROSCI.3902-05.2006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Yan Z, Li S, Liang Z et al (2008) The P2X 7 receptor channel pore dilates under physiological ion conditions. J Gen Physiol 132:563–573. https://doi.org/10.1085/jgp.200810059

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Rigato C, Swinnen N, Buckinx R et al (2012) Microglia proliferation is controlled by P2X7 receptors in a pannexin-1-independent manner during early embryonic spinal cord invasion. J Neurosci 32:11559–11573. https://doi.org/10.1523/JNEUROSCI.1042-12.2012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. De Vuyst E, Decrock E, De Bock M et al (2007) Connexin hemichannels and gap junction channels are differentially influenced by lipopolysaccharide and basic fibroblast growth factor. Mol Biol Cell 18:34–36. https://doi.org/10.1091/mbc.E06

    Article  PubMed  PubMed Central  Google Scholar 

  89. Anselmi F, Hernandez VH, Crispino G et al (2008) ATP release through connexin hemichannels and gap junction transfer of second messengers propagate Ca2+ signals across the inner ear. Proc Natl Acad Sci 105:18770–18775. https://doi.org/10.1073/pnas.0800793105

    Article  PubMed  PubMed Central  Google Scholar 

  90. Sorge RE, Trang T, Dorfman R et al (2012) Genetically determined P2X7 receptor pore formation regulates variability in chronic pain sensitivity. Nat Med 18:595–599. https://doi.org/10.1038/nm.2710

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Purohit R, Bera AK (2021) Pannexin 1 plays a pro-survival role by attenuating P2X7 receptor-mediated Ca2+ influx. Cell Calcium 99:102458. https://doi.org/10.1016/j.ceca.2021.102458

    Article  CAS  PubMed  Google Scholar 

  92. Purohit R, Bera AK (2023) Carboxyl terminus of pannexin-1 plays a crucial role in P2X7 receptor-mediated signaling. Biochem Biophys Res Commun 664:20–26. https://doi.org/10.1016/j.bbrc.2023.04.081

    Article  CAS  PubMed  Google Scholar 

  93. Deuchars SA, Atkinson L, Brooke RE, et al (2001) Neuronal P2X7 receptors are targeted to presynaptic terminals in the central and peripheral nervous systems. J Neurosci 21:7143–7152 21/18/7143 [pii]

  94. Sperlagh B, Kofalvi A, Deuchars J et al (2002) Involvement of P2X7 receptors in the regulation of neurotransmitter release in the rat hippocampus. J Neurochem 81:1196–1211. https://doi.org/10.1046/j.1471-4159.2002.00920.x

    Article  CAS  PubMed  Google Scholar 

  95. Atkinson L, Batten TFC, Moores TS et al (2004) Differential co-localisation of the P2X7 receptor subunit with vesicular glutamate transporters VGLUT1 and VGLUT2 in rat CNS. Neuroscience 123:761–768. https://doi.org/10.1016/j.neuroscience.2003.08.065

    Article  CAS  PubMed  Google Scholar 

  96. Cho J, Choi I, Jang I (2010) P2X7 receptors enhance glutamate release in hippocampal hilar neurons. Cell Mol Dev Neurosci 21:865–870. https://doi.org/10.1097/WNR.0b013e32833d9142

    Article  CAS  Google Scholar 

  97. Zhang PA, Xu QY, Xue L et al (2017) Neonatal maternal deprivation enhances presynaptic p2x7 receptor transmission in insular cortex in an adult rat model of visceral hypersensitivity. CNS Neurosci Ther 23:145–154. https://doi.org/10.1111/cns.12663

    Article  CAS  PubMed  Google Scholar 

  98. Miras-Portugal MT, Ortega F, Gómez-Villafuertes R, et al (2021) P2X7 receptors in the central nervous system. Biochem Pharmacol 187. https://doi.org/10.1016/j.bcp.2021.114472

  99. Rafael A, Cairus A, Tizzoni M et al (2020) Glial ATP and large pore channels modulate synaptic strength in response to chronic inactivity. Mol Neurobiol 57:2856–2869. https://doi.org/10.1007/s12035-020-01919-0

    Article  CAS  PubMed  Google Scholar 

  100. Alloisio S, Cervetto C, Passalacqua M et al (2008) Functional evidence for presynaptic P2X7 receptors in adult rat cerebrocortical nerve terminals. FEBS Lett 582:3948–3953. https://doi.org/10.1016/j.febslet.2008.10.041

    Article  CAS  PubMed  Google Scholar 

  101. Marcoli M, Cervetto C, Paluzzi P et al (2008) P2X7 pre-synaptic receptors in adult rat cerebrocortical nerve terminals: a role in ATP-induced glutamate release. J Neurochem 105:2330–2342. https://doi.org/10.1111/j.1471-4159.2008.05322.x

    Article  CAS  PubMed  Google Scholar 

  102. León D, Sánchez-Nogueiro J, Marín-García P, Miras-Portugal MT (2008) Glutamate release and synapsin-I phosphorylation induced by P2X7receptors activation in cerebellar granule neurons. Neurochem Int 52:1148–1159. https://doi.org/10.1016/j.neuint.2007.12.004

    Article  CAS  PubMed  Google Scholar 

  103. Miras-Portugal MT, Díaz-Hernández M, Giráldez L et al (2003) P2X7 receptors in rat brain: presence in synaptic terminals and granule cells. Neurochem Res 28:1597–1605. https://doi.org/10.1023/A:1025690913206

    Article  CAS  PubMed  Google Scholar 

  104. Egan TM, Samways DSK, Li Z (2006) Biophysics of P2X receptors. Pflugers Arch Eur J Physiol 452:501–512. https://doi.org/10.1007/s00424-006-0078-1

    Article  CAS  Google Scholar 

  105. Lundy PM, Hamilton MG, Mi L et al (2002) Stimulation of Ca 2+ influx through ATP receptors on rat brain synaptosomes: identification of functional P2X 7 receptor subtypes. Br J Pharmacol 135:1616–1626. https://doi.org/10.1038/sj.bjp.0704624

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Ireland MF, Noakes PG, Bellingham MC (2004) P2X 7-like receptor subunits enhance excitatory synaptic transmission at central synapses by presynaptic mechanisms. Neuroscience 128:269–280. https://doi.org/10.1016/j.neuroscience.2004.06.014

    Article  CAS  PubMed  Google Scholar 

  107. Miteva AS, Gaydukov AE, Shestopalov VI, Balezina OP (2018) Mechanism of P2X7 receptor-dependent enhancement of neuromuscular transmission in pannexin 1 knockout mice. Purinergic Signal 14:459–469. https://doi.org/10.1007/s11302-018-9630-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Miteva A, Gaydukov A, Balezina O (2020) Interaction between calcium chelators and the activity of P2X7 receptors in mouse motor synapses. Int J Mol Sci 21. https://doi.org/10.3390/ijms21062034

  109. Ardiles AO, Flores-Muñoz C, Toro-Ayala G et al (2014) Pannexin 1 regulates bidirectional hippocampal synaptic plasticity in adult mice. Front Cell Neurosci 8:1–11. https://doi.org/10.3389/fncel.2014.00326

    Article  Google Scholar 

  110. Kurtenbach S, Prochnow N, Kurtenbach S et al (2013) Pannexin1 channel proteins in the zebrafish retina Have shared and unique properties. PLoS One 8:e77722. https://doi.org/10.1371/journal.pone.0077722

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. García-Rojas F, Flores-Muñoz C, Santander O et al (2023) Pannexin-1 modulates inhibitory transmission and hippocampal synaptic plasticity. Biomolecules 13:1–17. https://doi.org/10.3390/biom13060887

    Article  CAS  Google Scholar 

  112. Santos DA, Salgado AI, Cunha RA (2003) ATP is released from nerve terminals and from activated muscle fibres on stimulation of the rat phrenic nerve. Neurosci Lett 338:225–228. https://doi.org/10.1016/S0304-3940(02)01419-2

    Article  CAS  PubMed  Google Scholar 

  113. Miteva AS, Gaydukov AE, Shestopalov VI, Balezina OP (2017) The role of pannexin 1 in the purinergic regulation of synaptic transmission in mouse motor synapses. Biochem Suppl Ser A Membr Cell Biol 11:311–320. https://doi.org/10.1134/S1990747817040067

    Article  Google Scholar 

  114. Cunha RA, Ribeiro JA (2000) ATP as a presynaptic modulator. Life Sci 68:119–137. https://doi.org/10.1016/S0024-3205(00)00923-1

    Article  CAS  PubMed  Google Scholar 

  115. Ribeiro JA, Walker J (1975) The effects of adenosine triphosphate and adenosine diphosphate on transmission at the rat and frog neuromuscular junctions. Br J Pharmacol 54:213–218. https://doi.org/10.1111/j.1476-5381.1975.tb06931.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Momboisse F, Olivares MJ, Báez-Matus X et al (2014) Pannexin 1 channels: new actors in the regulation of catecholamine release from adrenal chromaffin cells. Front Cell Neurosci 8:1–12. https://doi.org/10.3389/fncel.2014.00270

    Article  Google Scholar 

  117. Maldifassi MC, Momboisse F, Guerra MJ et al (2021) The interplay between α7 nicotinic acetylcholine receptors, pannexin-1 channels and P2X7 receptors elicit exocytosis in chromaffin cells. J Neurochem 157:1789–1808. https://doi.org/10.1111/jnc.15186

    Article  CAS  PubMed  Google Scholar 

  118. Sokolova E, Nistri A, Giniatullin R (2001) Negative cross talk between anionic GABA A and cationic P2X ionotropic receptors of rat dorsal root ganglion neurons. J Neurosci 21:4958–4968. https://doi.org/10.1523/JNEUROSCI.21-14-04958.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Dvoriantchikova G, Ivanov D, Panchin Y, Shestopalov VI (2006) Expression of pannexin family of proteins in the retina. FEBS Lett 580:2178–2182. https://doi.org/10.1016/j.febslet.2006.03.026

    Article  CAS  PubMed  Google Scholar 

  120. Riquelme MA, Cea LA, Vega JL et al (2013) The ATP required for potentiation of skeletal muscle contraction is released via pannexin hemichannels. Neuropharmacology 75:594–603. https://doi.org/10.1016/j.neuropharm.2013.03.022

    Article  CAS  PubMed  Google Scholar 

  121. Sokolova E, Grishin S, Shakirzyanova A et al (2003) Distinct receptors and different transduction mechanisms for ATP and adenosine at the frog motor nerve endings. Eur J Neurosci 18:1254–1264. https://doi.org/10.1046/j.1460-9568.2003.02835.x

    Article  CAS  PubMed  Google Scholar 

  122. Li Q, Barres BA (2018) Microglia and macrophages in brain homeostasis and disease. Nat Publ Gr 18:225–242. https://doi.org/10.1038/nri.2017.125

    Article  CAS  Google Scholar 

  123. Liddelow SA, Guttenplan KA, Clarke LE et al (2017) Neurotoxic reactive astrocytes are induced by activated microglia. Nature 541:481–487. https://doi.org/10.1038/nature21029

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Barres BA (2008) The mystery and magic of glia: A perspective on their roles in health and disease. Neuron 60:430–440. https://doi.org/10.1016/j.neuron.2008.10.013

    Article  CAS  PubMed  Google Scholar 

  125. Araque A, Navarrete M (2010) Glial cells in neuronal network function. Philos Trans R Soc B Biol Sci 365:2375–2381. https://doi.org/10.1098/rstb.2009.0313

    Article  Google Scholar 

  126. Durkee CA, Araque A (2019) Diversity and specificity of astrocyte–neuron communication. Neuroscience 396:73–78. https://doi.org/10.1016/j.neuroscience.2018.11.010

    Article  CAS  PubMed  Google Scholar 

  127. Araque A, Parpura V, Sanzgiri RP, Haydon PG (1999) Tripartite synapses: glia, the unacknowledged partner. Trends Neurosci 22:208–215. https://doi.org/10.1016/s0166-2236(98)01349-6

    Article  CAS  PubMed  Google Scholar 

  128. Perea G, Navarrete M, Araque A (2009) Tripartite synapses: astrocytes process and control synaptic information. Trends Neurosci 32:421–431. https://doi.org/10.1016/j.tins.2009.05.001

    Article  CAS  PubMed  Google Scholar 

  129. Stevens ER, Esguerra M, Kim PM et al (2003) D-serine and serine racemase are present in the vertebrate retina and contribute to the physiological activation of NMDA receptors. Proc Natl Acad Sci 100:6789–6794

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Wolosker H, Blackshaw S, Snyder SH (1999) Serine racemase: a glial enzyme synthesizing D-serine to regulate glutamate-N-methyl-D-aspartate neurotransmission. Proc Natl Acad Sci 96:13409–13414. https://doi.org/10.1073/pnas.96.23.13409

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Yang Y, Ge W, Chen Y et al (2003) Contribution of astrocytes to hippocampal long-term potentiation through release of D-serine. Proc Natl Acad Sci 100:15194–15199. https://doi.org/10.1073/pnas.2431073100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Yang S, Qiao H, Wen L et al (2005) D-Serine enhances impaired long-term potentiation in CA1 subfield of hippocampal slices from aged senescence-accelerated mouse prone/8. Neurosci Lett 379:7–12. https://doi.org/10.1016/j.neulet.2004.12.033

    Article  CAS  PubMed  Google Scholar 

  133. Panatier A, Gentles SJ, Bourque CW, Oliet SHR (2006) Activity-dependent synaptic plasticity in the supraoptic nucleus of the rat hypothalamus. J Physiol 573:711–721. https://doi.org/10.1113/jphysiol.2006.109447

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Henneberger C, Papouin T, Oliet SHR, Rusakov DA (2010) Long-term potentiation depends on release of d-serine from astrocytes. Nature 463:232–236. https://doi.org/10.1038/nature08673

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Martineau M, Parpura V, Mothet JP (2014) Cell-type specific mechanisms of D-serine uptake and release in the brain. Front. Synaptic Neurosci. 6:1–9. https://doi.org/10.3389/fnsyn.2014.00012

  136. Sherwood MW, Oliet SHR, Panatier A (2021) NMDARs, coincidence detectors of astrocytic and neuronal activities. Int J Mol Sci 22:1–23. https://doi.org/10.3390/ijms22147258

    Article  CAS  Google Scholar 

  137. Pan HC, Chou YC, Sun SH (2015) P2X7R-mediated Ca2+-independent d-serine release via pannexin-1 of the P2X7R-pannexin-1 complex in astrocytes. Glia 63:877–893. https://doi.org/10.1002/glia.22790

    Article  PubMed  Google Scholar 

  138. Bademosi AT, Lauwers E, Padmanabhan P et al (2017) In vivo single-molecule imaging of syntaxin1A reveals polyphosphoinositide- and activity-dependent trapping in presynaptic nanoclusters. Nat Commun 7:13660. https://doi.org/10.1038/ncomms13660

    Article  CAS  Google Scholar 

  139. Mothet JP, Pollegioni L, Ouanounou G et al (2005) Glutamate receptor activation triggers a calcium-dependent and SNARE protein-dependent release of the gliotransmitter D-serine. Proc Natl Acad Sci 102:5606–5611. https://doi.org/10.1073/pnas.0408483102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Li YH, Han TZ (2007) Glycine binding sites of presynaptic NMDA receptors may tonically regulate glutamate release in the rat visual cortex. J Neurophysiol 97:817–823. https://doi.org/10.1152/jn.00980.2006

    Article  CAS  PubMed  Google Scholar 

  141. Ohi Y, Kimura S, Haji A (2015) Modulation of glutamatergic transmission by presynaptic N-methyl-d-aspartate mechanisms in second-order neurons of the rat nucleus tractus solitarius. Neurosci Lett 587:62–67. https://doi.org/10.1016/j.neulet.2014.12.031

    Article  CAS  PubMed  Google Scholar 

  142. Lench A, Massey P V, Pollegioni L, et al (2014) Neuropharmacology Astroglial D -serine is the endogenous co-agonist at the presynaptic NMDA receptor in rat entorhinal cortex. Neuropharmacology 1–9. https://doi.org/10.1016/j.neuropharm.2014.04.004

  143. Kandel ER, Schwartz JH, Jessell TM (2000) Principles of neural science (4th ed). McGraw Hill, Health Professions Division, New York

  144. Amir R, Devor M (2003) Electrical excitability of the soma of sensory neurons is required for spike invasion of the soma, but not for through-conduction. Biophys J 84:2181–2191. https://doi.org/10.1016/S0006-3495(03)75024-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Hanani M (2005) Satellite glial cells in sensory ganglia: from form to function. Brain Res Rev 48:457–476. https://doi.org/10.1016/j.brainresrev.2004.09.001

    Article  CAS  PubMed  Google Scholar 

  146. Pannese E (1981) The satellite cells of the sensory ganglia. Adv Anat Embryol Cell Biol 65:1–111. https://doi.org/10.1007/978-3-642-67750-2

    Article  CAS  PubMed  Google Scholar 

  147. Zhang X, Chen Y, Wang C, Huang LYM (2007) Neuronal somatic ATP release triggers neuron-satellite glial cell communication in dorsal root ganglia. Proc Natl Acad Sci 104:9864–9869. https://doi.org/10.1073/pnas.0611048104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. Gu Y, Chen Y, Zhang X et al (2010) Neuronal soma-satellite glial cell interactions in sensory ganglia and the participation of purinergic receptors. Neuron Glia Biol. 6:53–62. https://doi.org/10.1017/S1740925X10000116

    Article  PubMed  PubMed Central  Google Scholar 

  149. Retamal MA, Alcayaga J, Verdugo CA et al (2014) Opening of pannexin- and connexin-based channels increases the excitability of nodose ganglion sensory neurons. Front Cell Neurosci 8:1–12. https://doi.org/10.3389/fncel.2014.00158

    Article  CAS  Google Scholar 

  150. Chen Y, Zhang X, Wang C et al (2008) Activation of P2X7 receptors in glial satellite cells reduces pain through downregulation of P2X3 receptors in nociceptive neurons. Proc Natl Acad Sci 105:16773–16778. https://doi.org/10.1073/pnas.0801793105

    Article  PubMed  PubMed Central  Google Scholar 

  151. Hanstein R, Hanani M, Scemes E, Spray DC (2016) Glial pannexin1 contributes to tactile hypersensitivity in a mouse model of orofacial pain. Sci Rep 6:1–10. https://doi.org/10.1038/srep38266

    Article  CAS  Google Scholar 

  152. Hanani M, Spray DC (2020) Emerging importance of satellite glia in nervous system function and dysfunction. Nat Rev Neurosci 21:485–498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  153. Chen Z, Zhang C, Song X et al (2022) Bzatp activates satellite glial cells and increases the excitability of dorsal root ganglia neurons in vivo. Cells 11:1–17. https://doi.org/10.3390/cells11152280

    Article  CAS  Google Scholar 

  154. Hanstein R, Negoro H, Patel NK et al (2013) Promises and pitfalls of a Pannexin1 transgenic mouse line. Front Pharmacol 4:1–10. https://doi.org/10.3389/fphar.2013.00061

    Article  Google Scholar 

  155. Feldman-Goriachnik R, Belzer V, Hanani M (2015) Systemic inflammation activates satellite glial cells in the mouse nodose ganglion and alters their functions. Glia 63:2121–2132. https://doi.org/10.1002/glia.22881

    Article  PubMed  Google Scholar 

  156. Zhang Y, Laumet G, Chen SR et al (2015) Pannexin-1 up-regulation in the dorsal root ganglion contributes to neuropathic pain development. J Biol Chem 290:14647–14655. https://doi.org/10.1074/jbc.M115.650218

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  157. Zhang XF, Han P, Faltynek CR et al (2005) Functional expression of P2X7 receptors in non-neuronal cells of rat dorsal root ganglia. Brain Res 1052:63–70. https://doi.org/10.1016/j.brainres.2005.06.022

    Article  CAS  PubMed  Google Scholar 

  158. Chen Y, Li G, Huang LYM (2012) P2X7 receptors in satellite glial cells mediate high functional expression of P2X3 receptors in immature dorsal root ganglion neurons. Mol Pain 8:1–9. https://doi.org/10.1186/1744-8069-8-9

    Article  CAS  Google Scholar 

  159. Turrigiano GG (2008) The self-tuning neuron: synaptic scaling of excitatory synapses. Cell 135:422–435. https://doi.org/10.1016/j.cell.2008.10.008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  160. Pozo K, Goda Y (2010) Unraveling mechanisms of homeostatic synaptic plasticity. Neuron 66:337–351. https://doi.org/10.1016/j.neuron.2010.04.028

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  161. Vitureira N, Goda Y (2013) The interplay between Hebbian and homeostatic synaptic plasticity. J Cell Biol 203:175–186. https://doi.org/10.1083/jcb.201306030

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  162. Stellwagen D, Malenka RC (2006) Synaptic scaling mediated by glial TNF-α. Nature 440:1054–1059. https://doi.org/10.1038/nature04671

    Article  CAS  PubMed  Google Scholar 

  163. Beattie EC, Stellwagen D, Morishita W et al (2002) Control of synaptic strength by glial TNF alpha. Science (80- ) 295:2282–2285. https://doi.org/10.1126/science.1067859

    Article  CAS  Google Scholar 

  164. Vlachos A, Ikenberg B, Lenz M et al (2013) Synaptopodin regulates denervation-induced homeostatic synaptic plasticity. Proc Natl Acad Sci 110:8242–8247. https://doi.org/10.1073/pnas.121367711010.1073/pnas.1213677110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  165. Becker D, Zahn N, Deller T, Vlachos A (2013) Tumor necrosis factor alpha maintains denervation-induced homeostatic synaptic plasticity of mouse dentate granule cells. Front Cell Neurosci 7:1–10. https://doi.org/10.3389/fncel.2013.00257

    Article  CAS  Google Scholar 

  166. Heir R, Stellwagen D (2020) TNF-mediated homeostatic synaptic plasticity: from in vitro to in vivo models. Front Cell Neurosci 14:1–12. https://doi.org/10.3389/fncel.2020.565841

    Article  CAS  Google Scholar 

  167. Pankratov Y, Lalo U, Krishtal OA, Verkhratsky A (2009) P2X receptors and synaptic plasticity. Neuroscience 158:137–148. https://doi.org/10.1016/j.neuroscience.2008.03.076

    Article  CAS  PubMed  Google Scholar 

  168. Khakh BS (2001) Molecular physiology of P2X receptors and ATP signalling at synapses. Nat Rev Neurosci 2:165–174. https://doi.org/10.1038/35058521

    Article  CAS  PubMed  Google Scholar 

  169. Zhao CJ, Dreosti E, Lagnado L (2011) Homeostatic synaptic plasticity through changes in presynaptic calcium influx. J Neurosci 31:7492–7496. https://doi.org/10.1523/JNEUROSCI.6636-10.2011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  170. Lazarevic V, Schöne C, Heine M et al (2011) Extensive remodeling of the presynaptic cytomatrix upon homeostatic adaptation to network activity silencing. J Neurosci 31:10189–10200. https://doi.org/10.1523/JNEUROSCI.2088-11.2011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  171. Rátkai A, Tárnok K, El AH et al (2021) Homeostatic plasticity and burst activity are mediated by hyperpolarization-activated cation currents and T-type calcium channels in neuronal cultures. Sci Rep 11:1–17. https://doi.org/10.1038/s41598-021-82775-3

    Article  CAS  Google Scholar 

Download references

Acknowledgements

A.R. received a PhD Fellowship from the Agencia Nacional de Investigación e Innovación (ANII-MEC).

Funding

This work was supported by grants to N.V., V.A. and AR by the Comisión Sectorial de Investigación Científica (CSIC-UdelaR, Uruguay, grant number: 22520220100095UD, 22520220100243UD and 22320200200227UD, respectively) and by the Programa de Desarrollo de las Ciencias Básicas (PEDECIBA, Uruguay).

Author information

Authors and Affiliations

  1. Departamento de Fisiología, Facultad de Medicina, Universidad de la República, Montevideo, Uruguay

    Nathalia Vitureira, Alberto Rafael & Verónica Abudara

Authors
  1. Nathalia Vitureira
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alberto Rafael
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Verónica Abudara
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to the manuscript conception and design. The manuscript was written by both NV and VA and all authors reviewed the manuscript. AR prepared the figure. All authors read and approved the manuscript.

Corresponding authors

Correspondence to Nathalia Vitureira or Verónica Abudara.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Additional information

Publisher's Note

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

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vitureira, N., Rafael, A. & Abudara, V. P2X7 receptors and pannexin1 hemichannels shape presynaptic transmission. Purinergic Signalling (2023). https://doi.org/10.1007/s11302-023-09965-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11302-023-09965-8

Keywords

Search

Navigation