Pannexin channels and ischaemia

Journal of Physiology

Volumn 593, Issue 16, 2015, Pages 3463-3470

  Thompson, Roger J ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; GLUTAMIC ACID; ION CHANNEL; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; OXYGEN; PANNEXIN 1; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG; GAP JUNCTION PROTEIN; NERVE PROTEIN; PANX1 PROTEIN, HUMAN;

ACIDIFICATION; ALLOSTERISM; ANOXIA; BRAIN BLOOD FLOW; BRAIN ISCHEMIA; BRAIN SLICE; CARBOXY TERMINAL SEQUENCE; ENZYME ACTIVATION; EXCITOTOXICITY; HIPPOCAMPUS; HUMAN; HYPERCAPNIA; ION TRANSPORT; MEMBRANE DEPOLARIZATION; NERVE CELL NECROSIS; NEUROPATHOLOGY; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; REVIEW; SIGNAL TRANSDUCTION; SPREADING CORTICAL DEPRESSION; ANIMAL; CELL DEATH; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; BRAIN ISCHEMIA; CELL DEATH; CONNEXINS; NERVE TISSUE PROTEINS; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 84938985874     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2014.282426     Document Type: Review

References (65)

1. Aarts M, Iihara K, Wei W-L, Xiong Z-G, Arundine M, Cerwinski W, MacDonald JF & Tymianski M (2003). A key role for TRPM7 channels in anoxic neuronal death. Cell 115, 863-877.
2. Aarts M, Liu Y, Liu L, Besshoh S, Arundine M, Gurd JW, Wang Y-T, Salter MW & Tymianski M (2002). Treatment of ischemic brain damage by perturbing NMDA receptor-PSD-95 protein interactions. Science 298, 846-850.
3. Alim I, Teves L, Li R, Mori Y & Tymianski M (2013). Modulation of NMDAR subunit expression by TRPM2 channels regulates neuronal vulnerability to ischemic cell death. J Neurosci 33, 17264-17277.
4. Balestrino M (1995). Pathophysiology of anoxic depolarization: new findings and a working hypothesis. J Neurosci Methods 59, 99-103.
5. Baranova A, Ivanov D, Petrash N, Pestova A, Skoblov M, Kelmanson I, Shagin D, Nazarenko S, Geraymovych E, Litvin O et al. (2004). The mammalian pannexin family is homologous to the invertebrate innexin gap junction proteins. Genomics 83, 706-716.
6. Bargiotas P, Krenz A, Hormuzdi SG, Ridder DA, Herb A, Barakat W, Penuela S, von Engelhardt J, Monyer H & Schwaninger M (2011). Pannexins in ischemia-induced neurodegeneration. Proc Natl Acad Sci U S A 108, 20772-20777.
7. Bargiotas P, Krenz A, Monyer H & Schwaninger M (2012). Functional outcome of pannexin-deficient mice after cerebral ischemia. Channels (Austin) 6, 453-456.
8. Bond SR, Lau A, Penuela S, Sampaio AV, Underhill TM, Laird DW & Naus CC (2011). Pannexin 3 is a novel target for Runx2, expressed by osteoblasts and mature growth plate chondrocytes. J Bone Miner Res 26, 2911-2922.
9. Brisson CD & Andrew RD (2012). A neuronal population in hypothalamus that dramatically resists acute ischemic injury compared to neocortex. J Neurophysiol 108, 419-430.
10. Bruzzone R, Hormuzdi SG, Barbe MT, Herb A & Monyer H (2003). Pannexins, a family of gap junction proteins expressed in brain. Proc Natl Acad Sci U S A 100, 13644-13649.
11. Bunse S, Schmidt M, Prochnow N, Zoidl G & Dermietzel R (2010). Intracellular cysteine 346 is essentially involved in regulating Panx1 channel activity. J Biol Chem 285, 38444-38452.
12. Chekeni FB, Elliott MR, Sandilos JK, Walk SF, Kinchen JM, Lazarowski ER, Armstrong AJ, Penuela S, Laird DW, Salvesen GS et al. (2010). Pannexin 1 channels mediate "find-me" signal release and membrane permeability during apoptosis. Nature 467, 863-867.
13. Cook DJ, Teves L & Tymianski M (2012). Treatment of stroke with a PSD-95 inhibitor in the gyrencephalic primate brain. Nature 483, 213-217.
14. Dijkhuizen RM, Beekwilder JP, van der Worp HB, Berkelbach van der Sprenkel JW, Tulleken KA & Nicolay K (1999). Correlation between tissue depolarizations and damage in focal ischemic rat brain. Brain Res 840, 194-205.
15. Gao J, Duan B, Wang D-G, Deng X-H, Zhang G-Y, Xu L & Xu T-L (2005). Coupling between NMDA receptor and acid-sensing ion channel contributes to ischemic neuronal death. Neuron 48, 635-646.
16. Gladding CM & Raymond LA (2011). Mechanisms underlying NMDA receptor synaptic/extrasynaptic distribution and function. Mol Cell Neurosci 48, 308-320.
17. Hansen AJ (1977). Extracellular potassium concentration in juvenile and adult rat brain cortex during anoxia. Acta Physiol Scand 99, 412-420.
18. Hansen AJ (1978). The extracellular potassium concentration in brain cortex following ischemia in hypo- and hyperglycemic rats. Acta Physiol Scand 102, 324-329.
19. Hardingham GE (2006). Pro-survival signalling from the NMDA receptor. Biochem Soc Trans 34, 936-938.
20. Hardingham GE & Bading H (2010). Synaptic versus extrasynaptic NMDA receptor signalling: implications for neurodegenerative disorders. Nat Rev Neurosci 11, 682-696.
21. Hill MD, Martin RH, Mikulis D, Wong JH, Silver FL, Terbrugge KG, Milot G, Clark WM, Macdonald RL, Kelly ME et al. (2012). Safety and efficacy of NA-1 in patients with iatrogenic stroke after endovascular aneurysm repair (ENACT): a phase 2, randomised, double-blind, placebo-controlled trial. Lancet Neurol 11, 942-950.
22. Hoyte L, Barber PA, Buchan AM & Hill MD (2004). The rise and fall of NMDA antagonists for ischemic stroke. Curr Mol Med 4, 131-136.
23. Leao A (1944). Spreading depression of activity in the cerebral cortex. J Neurophysiol 7, 359-390.
24. Leao A (1947). Further observations on the spreading depression of activity in the cerebral cortex. J Neurophysiol 10, 409-414.
25. Lemasters JJ, Theruvath TP, Zhong Z & Nieminen A-L (2009). Mitochondrial calcium and the permeability transition in cell death. Biochim Biophys Acta 1787, 1395-1401.
26. Lipton P (1999). Ischemic cell death in brain neurons. Physiol Rev 79, 1431-1568.
27. Liu Y, Wong TP, Aarts M, Rooyakkers A, Liu L, Lai TW, Wu DC, Lu J, Tymianski M, Craig AM & Wang YT (2007). NMDA receptor subunits have differential roles in mediating excitotoxic neuronal death both in vitro and in vivo. J Neurosci 27, 2846-2857.
28. 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.
29. Lohman AW, Billaud M, Straub AC, Johnstone SR, Best AK, Lee M, Barr K, Penuela S, Laird DW & Isakson BE (2012a). Expression of pannexin isoforms in the systemic murine arterial network. J Vasc Res 49, 405-416.
30. Lohman AW, Weaver JL, Billaud M, Sandilos JK, Griffiths R, Straub AC, Penuela S, Leitinger N, Laird DW, Bayliss DA & Isakson BE (2012b). S-nitrosylation inhibits pannexin 1 channel function. J Biol Chem 287, 39602-39612.
31. Madry C, Haglerød C & Attwell D (2010). The role of pannexin hemichannels in the anoxic depolarization of hippocampal pyramidal cells. Brain 133, 3755-3763.
32. Martel M-A, Ryan TJ, Bell KFS, Fowler JH, McMahon A, Al-Mubarak B, Komiyama NH, Horsburgh K, Kind PC, Grant SGN et al. (2012). The subtype of GluN2 C-terminal domain determines the response to excitotoxic insults. Neuron 74, 543-556.
33. 2+ of NMDA responses in spinal cord neurones. Nature 309, 261-263.
34. Naga KK, Sullivan PG & Geddes JW (2007). High cyclophilin D content of synaptic mitochondria results in increased vulnerability to permeability transition. J Neurosci 27, 7469-7475.
35. Nakamura T, Tu S, Akhtar MW, Sunico CR, Okamoto S-I & Lipton SA (2013). Aberrant protein S-nitrosylation in neurodegenerative diseases. Neuron 78, 596-614.
36. Nedergaard M (1987). Neuronal injury in the infarct border: a neuropathological study in the rat. Acta Neuropathol 73, 267-274.
37. 14C]2-deoxyglucose phosphorylation. J Cereb Blood Flow Metab 6, 607-615.
38. Papouin T, Ladépêche L, Ruel J, Sacchi S, Labasque M, Hanini M, Groc L, Pollegioni L, Mothet J-P & Oliet SHR (2012). Synaptic and extrasynaptic NMDA receptors are gated by different endogenous coagonists. Cell 150, 633-646.
39. Penuela S, Harland L, Simek J & Laird DW (2014a). Pannexin channels and their links to human disease. Biochem J 461, 371-381.
40. Penuela S, Simek J & Thompson RJ (2014b). Regulation of pannexin channels by post-translational modifications. FEBS Lett 588, 1411-1415.
41. Pillon NJ, Li YE, Fink LN, Brozinick JT, Nikolayev A, Kuo M-S, Bilan PJ & Klip A (2014). Nucleotides released from palmitate challenged muscle cells through pannexin-3 attract monocytes. Diabetes 63, 3815-3826.
42. Rader RK & Lanthorn TH (1989). Experimental ischemia induces a persistent depolarization blocked by decreased calcium and NMDA antagonists. Neurosci Lett 99, 125-130.
43. Risher WC, Lee MR, Fomitcheva IV, Hess DC & Kirov SA (2011). Dibucaine mitigates spreading depolarization in human neocortical slices and prevents acute dendritic injury in the ischemic rodent neocortex. PLoS One 6, e22351.
44. Rothman S (1984). Synaptic release of excitatory amino acid neurotransmitter mediates anoxic neuronal death. J Neurosci 4, 1884-1891.
45. Salter MW & Kalia LV (2004). Src kinases: a hub for NMDA receptor regulation. Nat Rev Neurosci 5, 317-328.
46. Sandilos JK, Chiu Y-H, Chekeni FB, Armstrong AJ, Walk SF, Ravichandran KS & Bayliss DA (2012). Pannexin 1, an ATP release channel, is activated by caspase cleavage of its pore-associated C-terminal autoinhibitory region. J Biol Chem 287, 11303-11311.
47. Sosinsky GE, Boassa D, Dermietzel R, Duffy HS, Laird DW, MacVicar B, Naus CC, Penuela S, Scemes E, Spray DC et al. (2011). Pannexin channels are not gap junction hemichannels. Channels (Austin) 5, 193-197.
48. 2+ exchanger. J Neurosci 12, 430-439.
49. Takano T, Tian G-F, Peng W, Lou N, Lovatt D, Hansen AJ, Kasischke KA & Nedergaard M (2007). Cortical spreading depression causes and coincides with tissue hypoxia. Nat Neurosci 10, 754-762.
50. Tekkök SB, Ye Z & Ransom BR (2007). Excitotoxic mechanisms of ischemic injury in myelinated white matter. J Cereb Blood Flow Metab 27, 1540-1552.
51. Thompson RJ, Jackson MF, Olah ME, Rungta RL, Hines DJ, Beazely MA, MacDonald JF & MacVicar BA (2008). Activation of pannexin-1 hemichannels augments aberrant bursting in the hippocampus. Science 322, 1555-1559.
52. Thompson RJ & Macvicar BA (2008). Connexin and pannexin hemichannels of neurons and astrocytes. Channels (Austin) 2, 81-86.
53. Thompson RJ, Zhou N & MacVicar BA (2006). Ischemia opens neuronal gap junction hemichannels. Science 312, 924-927.
54. Tovar KR, McGinley MJ & Westbrook GL (2013). Triheteromeric NMDA receptors at hippocampal synapses. J Neurosci 33, 9150-9160.
55. Traynelis SF, Wollmuth LP, McBain CJ, Menniti FS, Vance KM, Ogden KK, Hansen KB, Yuan H, Myers SJ & Dingledine R (2010). Glutamate receptor ion channels: structure, regulation, and function. Pharmacol Rev 62, 405-496.
56. Tymianski M (2011). Emerging mechanisms of disrupted cellular signaling in brain ischemia. Nat Neurosci 14, 1369-1373.
57. Tymianski M, Charlton MP, Carlen PL & Tator CH (1993). Source specificity of early calcium neurotoxicity in cultured embryonic spinal neurons. J Neurosci 13, 2085-2104.
58. Van Harreveld A & Hawes RC (1946). Asphyxial depolarisation in the spinal cord. Am J Physiol 147, 669-684.
59. Vergun O, Keelan J, Khodorov BI & Duchen MR (1999). Glutamate-induced mitochondrial depolarisation and perturbation of calcium homeostasis in cultured rat hippocampal neurones. J Physiol 519, 451-466.
60. Wang J, Ma M, Locovei S, Keane RW & Dahl G (2007). Modulation of membrane channel currents by gap junction protein mimetic peptides: size matters. Am J Physiol Cell Physiol 293, C1112-C1119.
61. Weilinger NL, Maslieieva V, Bialecki J, Sridharan SS, Tang PL & Thompson RJ (2012a). Ionotropic receptors and ion channels in ischemic neuronal death and dysfunction. Acta Pharmacol Sin 34, 39-34.
62. Weilinger NL, Tang PL & Thompson RJ (2012b). Anoxia-induced NMDA receptor activation opens pannexin channels via SRC family kinases. J Neurosci 32, 12579-12588.
63. Wicki-Stordeur LE, Boyce AKJ & Swayne LA (2013). Analysis of a pannexin 2-pannexin 1 chimeric protein supports divergent roles for pannexin C-termini in cellular localization. Cell Commun Adhes 20, 73-79.
64. Xie Y, Zacharias E, Hoff P & Tegtmeier F (1995). Ion channel involvement in anoxic depolarization induced by cardiac arrest in rat brain. J Cereb Blood Flow Metab 15, 587-594.
65. Zhang L, Deng T, Sun Y, Liu K, Yang Y & Zheng X (2008). Role for nitric oxide in permeability of hippocampal neuronal hemichannels during oxygen glucose deprivation. J Neurosci Res 86, 2281-2291.