ORIGINAL RESEARCH

Effect of probenecid on astrocyte activation in vitro

Babkina II1, Mazeeva VV2, Morozova MP1, Gorbacheva LR1,2
About authors

1 Pirogov Russian National Research Medical University, Moscow, Russia

2 Lomonosov Moscow State University, Moscow, Russia

Correspondence should be addressed: Lyubov R. Gorbacheva
Ostrovitianova, 1, Moscow, 117997, Russia; ur.liam@76ibrog

About paper

Funding: The study was supported by the Russian Science Foundation, Project № 22-25-00848.

Author contribution: Babkina II, Morozova MP — obtaining and maintaining primary culture of astrocytes; collection, interpretation and statistical analysis of data, manuscript writing; Mazeeva VV — obtaining and maintaining primary culture of astrocytes, interpretation and statistical analysis of data; Gorbacheva LR — conception and design of the experiment, interpretation of data, project management, manuscript writing.

Compliance with ethical standards: the study was approved by the Ethical Committee of Pirogov Russian National Research Medical University (Protocol № 23/2021 dated December 13, 2021).

Received: 2023-12-13 Accepted: 2024-01-24 Published online: 2024-02-26
|
  1. Choi SH, Da YL, Seung UK, Byung KJ. Thrombin-induced oxidative stress contributes to the death of hippocampal neurons in vivo: Role of microglial NADPH oxidase. Journal of Neuroscience. 2005; 25: 4082–90.
  2. D’hondt C, Ponsaerts R, De Smedt H, Vinken M, De Vuyst E, De Bock M, et al. Pannexin channels in ATP release and beyond: An unexpected rendezvous at the endoplasmic reticulum. Cellular Signalling. 2011; 23: 305–16.
  3. Koval M, Cwiek A, Carr T, Good ME, Lohman AW, Isakson BE. Pannexin 1 as a driver of inflammation and ischemia–reperfusion injury. Purinergic Signalling. 2021; 17: 521–31.
  4. Galkov MD, Surin AM, Lisina OYu, Gorbacheva LR. Neurodegeneration and Neuroinflammation: The Role of Pannexin 1. Neurochemical Journal. 2023; 17: 727–39.
  5. Rusiecka OM, Tournier M, Molica F, Kwak BR. Pannexin1 channels — a potential therapeutic target in inflammation. Front Cell Dev Biol. 2022; 10: 1020826.
  6. García-Rodríguez C, Mujica P, Illanes-González J, López A, Vargas C, Sáez JC, et al. Probenecid, an Old Drug with Potential New Uses for Central Nervous System Disorders and Neuroinflammation. Biomedicines. 2023; 11.
  7. Ivanova AE, Gorbacheva LR, Strukova SM, Pinelic VG, Rajzer G. Uchastie aktivirovannogo proteina S i trombina v reguljacii funkcij astrocitov. Biol membrany. 2013; 30: 387–97.
  8. Schwartz LB, Austen KF, Wasserman SI. Immunologic Release of β-Hexosaminidase and β-Glucuronidase from Purified Rat Serosal Mast Cells. The Journal of Immunology. 1979; 123: 1445–50.
  9. Penuela S, Gehi R, Laird DW. The biochemistry and function of pannexin channels. Biochimica et Biophysica Acta — Biomembranes. 2013; 1828: 15–22.
  10. Bhaskaracharya A, Dao-Ung P, Jalilian I, Spildrejorde M, Skarratt KK, Fuller SJ, et al. Probenecid Blocks Human P2X7 ReceptorInduced Dye Uptake via a Pannexin-1 Independent Mechanism. PLoS ONE. 2014; 9: e93058.
  11. Locovei S, Wang J, Dahl G. Activation of pannexin 1 channels by ATP through P2Y receptors and by cytoplasmic calcium. FEBS Letters. 2006; 580: 239–44.
  12. Yang K, Xiao Z, He X, Weng R, Zhao X, Sun T. Mechanisms of Pannexin 1 (PANX1) Channel Mechanosensitivity and Its Pathological Roles. International Journal of Molecular Sciences. 2022; 23.
  13. Szydlowska K, Tymianski M. Calcium, ischemia and excitotoxicity. Cell Calcium. 2010; 47: 122–9.
  14. Orellana JA, Froger N, Ezan P, Jiang JX, Bennett MVL, Naus CC, et al. ATP and glutamate released via astroglial connexin 43 hemichannels mediate neuronal death through activation of pannexin 1 hemichannels. Journal of Neurochemistry. 2011; 118: 826–40.
  15. Gödecke S, Roderigo C, Rose CR, Rauch BH, Gödecke A, Schrader J. Thrombin-induced ATP release from human umbilical vein endothelial cells. Am J Physiol Cell Physiol. 2012; 302: 915–23.
  16. Chen X, Zhang H, Hao H, Zhang X, Song H, He B, et al. Thrombin induces morphological and inflammatory astrocytic responses via activation of PAR1 receptor. Cell Death Discovery. 2022; 8.
  17. Seminario-Vidal L, Kreda S, Jones L, O’Neal W, Trejo JA, Boucher RC, et al. Thrombin promotes release of ATP from lung epithelial cells through coordinated activation of Rho- and Ca2+ -dependent signaling pathways. Journal of Biological Chemistry. 2009; 284: 20638–48.
  18. Fiebich BL, Batista CRA, Saliba SW, Yousif NM, de Oliveira ACP. Role of microglia TLRs in neurodegeneration. Frontiers in Cellular Neuroscience. 2018; 12.
  19. Zhang Z, Lei Y, Yan C, Mei X, Jiang T, Ma Z, et al. Probenecid Relieves Cerebral Dysfunction of Sepsis by Inhibiting Pannexin 1-Dependent ATP Release. Inflammation. 2019; 42: 1082–92.
  20. Yu D-K, Lee B, Kwon M, Yoon N, Shin T, Kim N-G, et al. Phlorofucofuroeckol B suppresses inflammatory responses by down-regulating nuclear factor κB activation via Akt, ERK, and JNK in LPS-stimulated microglial cells. International Immunopharmacology. 2015; 28: 1068–75.
  21. Kozuka N, Itofusa R, Kudo Y, Morita M. Lipopolysaccharide and proinflammatory cytokines require different astrocyte states to induce nitric oxide production. J of Neuroscience Research. 2005; 82: 717–28.
  22. Chen Q, Liang Z, Yue Q, Wang X, Siu SWI, Pui-Man Hoi M, et al. A Neuropeptide Y/F-like Polypeptide Derived from the Transcriptome of Turbinaria peltata Suppresses LPS-Induced Astrocytic Inflammation. J Nat Prod. 2022; 85: 1569–80.
  23. Liu B, Gao H-M, Wang J-Y, Jeohn G-H, Cooper CL, Hong J-S. Role of nitric oxide in inflammation-mediated neurodegeneration. Ann N Y Acad Sci. 2002; 962: 318–31.
  24. Li T, Xu T, Zhao J, Gao H, Xie W. Depletion of iNOS-positive inflammatory cells decelerates neuronal degeneration and alleviates cerebral ischemic damage by suppressing the inflammatory response. Free Radic Biol Med. 2022; 181: 209–20.
  25. Boven LA, Vergnolle N, Henry SD, Silva C, Imai Y, Holden J, et al. Up-Regulation of Proteinase-Activated Receptor 1 Expression in Astrocytes During HIV Encephalitis. The Journal of Immunology. 2003; 170: 2638–46.
  26. Isakson BE, Thompson RJ. Pannexin-1 as a potentiator of ligandgated receptor signaling. Channels. 2014; 8: 118–23.
  27. Huang G, Bao J, Shao X, Zhou W, Wu B, Ni Z, et al. Inhibiting pannexin-1 alleviates sepsis-induced acute kidney injury via decreasing NLRP3 inflammasome activation and cell apoptosis. Life Sciences. 2020; 254.
  28. Wareham KJ, Seward EP. P2X7 receptors induce degranulation in human mast cells. Purinergic Signalling. 2016; 12: 235–46.
  29. Ponath G, Park C, Pitt D. The role of astrocytes in multiple sclerosis. Frontiers in Immunology. 2018; 9.
  30. Okada S, Nakamura M, Mikami Y, Shimazaki T, Mihara M, Ohsugi Y, et al. Blockade of interleukin-6 receptor suppresses reactive astrogliosis and ameliorates functional recovery in experimental spinal cord injury. Journal of Neuroscience Research. 2004; 76 (2): 265–76.
  31. Krasovska V, Doering LC. Regulation of IL6 secretion by astrocytes via TLR4 in the fragile X mouse model. Frontiers in Molecular Neuroscience. 2018; 11: 272.
  32. Wei L, Sheng H, Chen L, Hao B, Shi X, Chen Y. Effect of pannexin-1 on the release of glutamate and cytokines in astrocytes. Journal of Clinical Neuroscience. 2016; 23: 135–41.
  33. Shieh CH, Heinrich A, Serchov T, van Calker D, Biber K. P2X7dependent, but differentially regulated release of IL6, CCL2, and TNF-α in cultured mouse microglia. GLIA. 2014; 62: 592–607.
  34. Jian Z, Ding S, Deng H, Wang J, Yi W, Wang L, et al. Probenecid protects against oxygen–glucose deprivation injury in primary astrocytes by regulating inflammasome activity. Brain Research. 2016; 1643: 123–9.
  35. Hainz N, Wolf S, Tschernig T, Meier C. Probenecid Application Prevents Clinical Symptoms and Inflammation in Experimental Autoimmune Encephalomyelitis. Inflammation. 2016; 39: 123–8.
  36. Wang Q, Li H, Ling Z, Chen G, Wei Z-Y. Inhibition of Schwann cell pannexin 1 attenuates neuropathic pain through the suppression of inflammatory responses. J Neuroinflammation. 2022; 19: 244.