Probenecid protects against cerebral ischemia/reperfusion injury by inhibiting lysosomal and inflammatory damage in rats

Neuroscience

Volumn 301, Issue , 2015, Pages 168-177

  Wei, R ^a   Wang, J ^b   Xu, Y ^a   Yin, B ^c   He, F ^a   Du, Y ^a   Peng, G ^a   Luo, B ^a  

^a ZHEJIANG UNIVERSITY   (China)

^b ANHUI MEDICAL UNIVERSITY   (China)

^c RENMIN HOSPITAL OF WUHAN UNIVERSITY   (China)

Author keywords

Calpain 1; Cathepsin B; Cerebral ischemia reperfusion injury; Heat shock protein 70; Inflammation; Probenecid

Indexed keywords

CALPAIN 1; CATHEPSIN B; GLIAL FIBRILLARY ACIDIC PROTEIN; HEAT SHOCK PROTEIN 70; IONIZED CALCIUM BINDING ADAPTOR MOLECULE 1; MARKER; PROBENECID; UNCLASSIFIED DRUG; ACTIN BINDING PROTEIN; CALCIUM BINDING PROTEIN; CALPONIN; NEUROPROTECTIVE AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; ASTROCYTE; BRAIN ISCHEMIA; CELLULAR DISTRIBUTION; CONTROLLED STUDY; HIPPOCAMPAL CA1 REGION; LYSOSOME; MALE; MICROGLIA; NERVE CELL NECROSIS; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RAT; SINGLE DRUG DOSE; UPREGULATION; ANIMAL; CELL DEATH; DRUG EFFECTS; ENCEPHALITIS; GLIA; METABOLISM; PYRAMIDAL NERVE CELL; REPERFUSION INJURY; SPRAGUE DAWLEY RAT;

ANIMALS; BRAIN ISCHEMIA; CA1 REGION, HIPPOCAMPAL; CALCIUM-BINDING PROTEINS; CATHEPSIN B; CELL DEATH; ENCEPHALITIS; HSP70 HEAT-SHOCK PROTEINS; LYSOSOMES; MALE; MICROFILAMENT PROTEINS; NEUROGLIA; NEUROPROTECTIVE AGENTS; PROBENECID; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY; REPERFUSION INJURY;

EID: 84931264802     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2015.05.070     Document Type: Article

References (60)

1. Amantea D., Nappi G., Bernardi G., Bagetta G., Corasaniti M.T. Post-ischemic brain damage: pathophysiology and role of inflammatory mediators. FEBS J 2009, 276:13-26.
2. Bao L., Locovei S., Dahl G. Pannexin membrane channels are mechanosensitive conduits for ATP. FEBS Lett 2004, 572:65-68.
3. Bargiotas P., Krenz A., Hormuzdi S.G., Ridder D.A., Herb A., Barakat W., Penuela S., von Engelhardt J., Monyer H., Schwaninger M. Pannexins in ischemia-induced neurodegeneration. Proc Natl Acad Sci U S A 2011, 108:20772-20777.
4. Bhaskaracharya A., Dao-Ung P., Jalilian I., Spildrejorde M., Skarratt K.K., Fuller S.J., Sluyter R., Stokes L. Probenecid blocks human P2X7 receptor-induced dye uptake via a pannexin-1 independent mechanism. PLoS One 2014, 9:e93058.
5. Billaud M., Lohman A.W., Straub A.C., Looft-Wilson R., Johnstone S.R., Araj C.A., Best A.K., Chekeni F.B., Ravichandran K.S., Penuela S., Laird D.W., Isakson B.E. Pannexin1 regulates alpha1-adrenergic receptor- mediated vasoconstriction. Circ Res 2011, 109:80-85.
6. Bruzzone R., Hormuzdi S.G., Barbe M.T., Herb A., Monyer H. Pannexins, a family of gap junction proteins expressed in brain. Proc Natl Acad Sci U S A 2003, 100:13644-13649.
7. Chao C.C., Huang C.C., Lu D.Y., Wong K.L., Chen Y.R., Cheng T.H., Leung Y.M. Ca2+ store depletion and endoplasmic reticulum stress are involved in P2X7 receptor-mediated neurotoxicity in differentiated NG108-15 cells. J Cell Biochem 2012, 113:1377-1385.
8. Chu K., Yin B., Wang J., Peng G., Liang H., Xu Z., Du Y., Fang M., Xia Q., Luo B. Inhibition of P2X7 receptor ameliorates transient global cerebral ischemia/reperfusion injury via modulating inflammatory responses in the rat hippocampus. J Neuroinflammation 2012, 9:69.
9. Cisneros-Mejorado A., Gottlieb M., Cavaliere F., Magnus T., Koch-Nolte F., Scemes E., Perez-Samartin A., Matute C. Blockade of P2X7 receptors or pannexin-1 channels similarly attenuates postischemic damage. J Cereb Blood Flow Metab 2015, 35:843-850.
10. Cisneros-Mejorado A., Perez-Samartin A., Gottlieb M., Matute C. ATP signaling in brain: release, excitotoxicity and potential therapeutic targets. Cellular Mol Neurobiol 2015, 35:1-6.
11. Colin-Gonzalez A.L., Santamaria A. Probenecid: an emerging tool for neuroprotection. CNS Neurol Disord: Drug Targets 2013, 12:1050-1065.
12. Cone A.C., Ambrosi C., Scemes E., Martone M.E., Sosinsky G.E. A comparative antibody analysis of pannexin1 expression in four rat brain regions reveals varying subcellular localizations. Front Pharmacol 2013, 4:6.
13. Cowdry R.W., Ebert M.H., van Kammen D.P., Post R.M., Goodwin F.K. Cerebrospinal fluid probenecid studies: a reinterpretation. Biol Psychiatry 1983, 18:1287-1299.
14. Dvoriantchikova G., Ivanov D., Barakat D., Grinberg A., Wen R., Slepak V.Z., Shestopalov V.I. Genetic ablation of Pannexin1 protects retinal neurons from ischemic injury. PLoS One 2012, 7:e31991.
15. Fontainhas A.M., Wang M.H., Liang K.J., Chen S., Mettu P., Damani M., Fariss R.N., Li W., Wong W.T. Microglial morphology and dynamic behavior is regulated by ionotropic glutamatergic and GABAergic neurotransmission. PLoS One 2011, 6.
16. Gulbransen B.D., Bashashati M., Hirota S.A., Gui X., Roberts J.A., MacDonald J.A., Muruve D.A., McKay D.M., Beck P.L., Mawe G.M., Thompson R.J., Sharkey K.A. Activation of neuronal P2X7 receptor-pannexin-1 mediates death of enteric neurons during colitis. Nat Med 2012, 18:600-604.
17. Hacke W., Kaste M., Bluhmki E., Brozman M., Davalos A., Guidetti D., Larrue V., Lees K.R., Medeghri Z., Machnig T., Schneider D., von Kummer R., Wahlgren N., Toni D. Thrombolysis with alteplase 3 to 4.5hours after acute ischemic stroke. New Engl J Med 2008, 359:1317-1329.
18. Hardingham G.E. Coupling of the NMDA receptor to neuroprotective and neurodestructive events. Biochem Soc T 2009, 37:1147-1160.
19. Kanneganti T.D., Lamkanfi M., Kim Y.G., Chen G., Park J.H., Franchi L., Vandenabeele P., Nunez G. Pannexin-1-mediated recognition of bacterial molecules activates the cryopyrin inflammasome independent of Toll-like receptor signaling. Immunity 2007, 26:433-443.
20. Kartzinel R., Ebert M.H., Chase T.N. Intravenous probenecid loading. Effects on plasma and cerebrospinal fluid probenecid levels and on monoamine metabolites in cerebrospinal fluid. Neurology 1976, 26:992-996.
21. Kilinc M., Gursoy-Ozdemir Y., Gurer G., Erdener S.E., Erdemli E., Can A., Dalkara T. Lysosomal rupture, necroapoptotic interactions and potential crosstalk between cysteine proteases in neurons shortly after focal ischemia. Neurobiol Dis 2010, 40:293-302.
22. Koh J.S., Lee S.J., Ryu C.W., Kim H.S. Safety and efficacy of mechanical thrombectomy with solitaire stent retrieval for acute ischemic stroke: a systematic review. Neurointervention 2012, 7:1-9.
23. Lai C.P., Bechberger J.F., Thompson R.J., MacVicar B.A., Bruzzone R., Naus C.C. Tumor-suppressive effects of pannexin 1 in C6 glioma cells. Cancer Res 2007, 67:1545-1554.
24. Li Y., Du X.F., Liu C.S., Wen Z.L., Du J.L. Reciprocal regulation between resting microglial dynamics and neuronal activity in vivo. Dev Cell 2012, 23:1189-1202.
25. Lipton P. Lysosomal membrane permeabilization as a key player in brain ischemic cell death: a "Lysosomocentric" hypothesis for ischemic brain damage. Transl Stroke Res 2013, 4:672-684.
26. Locovei S., Scemes E., Qiu F., Spray D.C., Dahl G. Pannexin1 is part of the pore forming unit of the P2X(7) receptor death complex. FEBS Lett 2007, 581:483-488.
27. Ma W., Hui H., Pelegrin P., Surprenant A. Pharmacological characterization of pannexin-1 currents expressed in mammalian cells. J Pharmacol Exp Therap 2009, 328:409-418.
28. Matute C., Cavaliere F. Neuroglial interactions mediated by purinergic signalling in the pathophysiology of CNS disorders. Semin Cell Dev Biol 2011, 22:252-259.
29. Mies G., Paschen W., Hossmann K.A. Cerebral blood flow, glucose utilization, regional glucose, and ATP content during the maturation period of delayed ischemic injury in gerbil brain. J Cereb Blood Flow Metab 1990, 10:638-645.
30. Molina C.A., Alvarez-Sabin J. Recanalization and reperfusion therapies for acute ischemic stroke. Cerebrovasc Dis 2009, 27(Suppl. 1):162-167.
31. Nozaki K., Beal M.F. Neuroprotective effects of L-kynurenine on hypoxia-ischemia and NMDA lesions in neonatal rats. J Cereb Blood Flow Metab 1992, 12:400-407.
32. Orellana J.A., Froger N., Ezan P., Jiang J.X., Bennett M.V.L., Naus C.C., Giaume C., Saez J.C. ATP and glutamate released via astroglial connexin 43 hemichannels mediate neuronal death through activation of pannexin 1 hemichannels. J Neurochem 2011, 118:826-840.
33. Pelegrin P., Surprenant A. Pannexin-1 mediates large pore formation and interleukin-1beta release by the ATP-gated P2X7 receptor. EMBO J 2006, 25:5071-5082.
34. Penuela S., Gehi R., Laird D.W. The biochemistry and function of pannexin channels. Biochim Biophys Acta 2013, 1828:15-22.
35. Prochnow N., Abdulazim A., Kurtenbach S., Wildforster V., Dvoriantchikova G., Hanske J., Petrasch-Parwez E., Shestopalov V.I., Dermietzel R., Manahan-Vaughan D., Zoidl G. Pannexin1 stabilizes synaptic plasticity and is needed for learning. PLoS One 2012, 7.
36. Reigada D., Lu W., Zhang M., Mitchell C.H. Elevated pressure triggers a physiological release of ATP from the retina: possible role for pannexin hemichannels. Neuroscience 2008, 157:396-404.
37. Robotka H., Sas K., Agoston M., Rozsa E., Szenasi G., Gigler G., Vecsei L., Toldi J. Neuroprotection achieved in the ischaemic rat cortex with L-kynurenine sulphate. Life Sci 2008, 82:915-919.
38. Sahara S., Yamashima T. Calpain-mediated Hsp70.1 cleavage in hippocampal CA1 neuronal death. Biochem Biophys Res Commun 2010, 393:806-811.
39. Santiago M.F., Veliskova J., Patel N.K., Lutz S.E., Caille D., Charollais A., Meda P., Scemes E. Targeting pannexin1 improves seizure outcome. PLoS One 2011, 6.
40. Sas K., Robotka H., Rozsa E., Agoston M., Szenasi G., Gigler G., Marosi M., Kis Z., Farkas T., Vecsei L., Toldi J. Kynurenine diminishes the ischemia-induced histological and electrophysiological deficits in the rat hippocampus. Neurobiol Dis 2008, 32:302-308.
41. Shah I.M., Macrae I.M., Di Napoli M. Neuroinflammation and neuroprotective strategies in acute ischaemic stroke - from bench to bedside. Curr Mol Med 2009, 9:336-354.
42. Shestopalov V.I., Slepak V.Z. Molecular pathways of pannexin1-mediated neurotoxicity. Front Physiol 2014, 5:23.
43. Silverman W., Locovei S., Dahl G. Probenecid, a gout remedy, inhibits pannexin 1 channels. Am J Physiol Cell Physiol 2008, 295:C761-C767.
44. Silverman W.R., de Rivero Vaccari J.P., Locovei S., Qiu F., Carlsson S.K., Scemes E., Keane R.W., Dahl G. The pannexin 1 channel activates the inflammasome in neurons and astrocytes. J Biol Chem 2009, 284:18143-18151.
45. Thompson R.J., Jackson M.F., Olah M.E., Rungta R.L., Hines D.J., Beazely M.A., MacDonald J.F., MacVicar B.A. Activation of Pannexin-1 hemichannels augments aberrant bursting in the hippocampus. Science 2008, 322:1555-1559.
46. Thompson R.J., Zhou N., MacVicar B.A. Ischemia opens neuronal gap junction hemichannels. Science 2006, 312:924-927.
47. Tsubokawa T., Solaroglu I., Yatsushige H., Cahill J., Yata K., Zhang J.H. Cathepsin and calpain inhibitor E64d attenuates matrix metalloproteinase-9 activity after focal cerebral ischemia in rats. Stroke 2006, 37:1888-1894.
48. Vamos E., Voros K., Zadori D., Vecsei L., Klivenyi P. Neuroprotective effects of probenecid in a transgenic animal model of Huntington's disease. J Neural Transm 2009, 116:1079-1086.
49. Vanden Abeele F., Bidaux G., Gordienko D., Beck B., Panchin Y.V., Baranova A.V., Ivanov D.V., Skryma R., Prevarskaya N. Functional implications of calcium permeability of the channel formed by pannexin 1. J Cell Biol 2006, 174:535-546.
50. Wang J.Y., Shen J., Gao Q., Ye Z.G., Yang S.Y., Liang H.W., Bruce I.C., Luo B.Y., Xia Q. Ischemic postconditioning protects against global cerebral ischemia/reperfusion-induced injury in rats. Stroke 2008, 39:983-990.
51. Wang J.Y., Xia Q., Chu K.T., Pan J., Sun L.N., Zeng B., Zhu Y.J., Wang Q., Wang K., Luo B.Y. Severe global cerebral ischemia-induced programmed necrosis of hippocampal CA1 neurons in rat is prevented by 3-methyladenine: a widely used inhibitor of autophagy. J Neuropathol Exp Neurol 2011, 70:314-322.
52. Weilinger N.L., Maslieieva V., Bialecki J., Sridharan S.S., Tang P.L., Thompson R.J. Ionotropic receptors and ion channels in ischemic neuronal death and dysfunction. Acta Pharmacol Sin 2013, 34:39-48.
53. Widmann R., Kuroiwa T., Bonnekoh P., Hossmann K.A. [C-14] Leucine incorporation into brain proteins in gerbils after transient ischemia - relationship to selective vulnerability of hippocampus. J Neurochem 1991, 56:789-796.
54. Windelborn J.A., Lipton P. Lysosomal release of cathepsins causes ischemic damage in the rat hippocampal slice and depends on NMDA-mediated calcium influx, arachidonic acid metabolism, and free radical production. J Neurochem 2008, 106:56-69.
55. Wonnenberg B., Tschernig T., Voss M., Bischoff M., Meier C., Schirmer S.H., Langer F., Bals R., Beisswenger C. Probenecid reduces infection and inflammation in acute Pseudomonas aeruginosa pneumonia. IJMM 2014, 304:725-729.
56. Xiong X.X., Gu L.J., Shen J., Kang X.H., Zheng Y.Y., Yue S.B., Zhu S.M. Probenecid protects against transient focal cerebral ischemic injury by inhibiting HMGB1 release and attenuating AQP4 expression in mice. Neurochem Res 2014, 39:216-224.
57. Xu M., Yang L., Rong J.G., Ni Y., Gu W.W., Luo Y., Ishidoh K., Katunuma N., Li Z.S., Zhang H.L. Inhibition of cysteine cathepsin B and L activation in astrocytes contributes to neuroprotection against cerebral ischemia via blocking the tBid-mitochondrial apoptotic signaling pathway. Glia 2014, 62:855-880.
58. Xuan A.G., Long D.H., Li J.H., Ji W.D., Hong L.P., Zhang M., Zhang W.J. Neuroprotective effects of valproic acid following transient global ischemia in rats. Life Sci 2012, 90:463-468.
59. Yamashima T. Hsp70.1 and related lysosomal factors for necrotic neuronal death. J Neurochem 2012, 120:477-494.
60. Yamashima T., Oikawa S. The role of lysosomal rupture in neuronal death. Prog Neurobiol 2009, 89:343-358.