Connexin hemichannel blockade is neuroprotective after, but not during, global cerebral ischemia in near-term fetal sheep

Experimental Neurology

Volumn 248, Issue , 2013, Pages 301-308

  Davidson, J O ^a   Green, C R ^a   Nicholson, L F B ^a   Bennet, L ^a   Gunn, A J ^a  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

Cerebral ischemia; Fetal sheep; Hemichannel; Hypoxic ischemic encephalopathy; Neuroprotection

Indexed keywords

CONNEXIN 43; PROTEIN INHIBITOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN ISCHEMIA; BRAIN NERVE CELL; CELL COUNT; CONNEXIN 43 HEMICHANNEL BLOCKING; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; FETUS; GESTATIONAL AGE; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; HIPPOCAMPUS; LATERAL BRAIN VENTRICLE; NEUROPROTECTION; NONHUMAN; OLIGODENDROGLIA; PHARMACOLOGICAL BLOCKING; PRIORITY JOURNAL; PROTEIN FUNCTION; SHEEP; WHITE MATTER;

CEREBRAL ISCHEMIA; FETAL SHEEP; HEMICHANNEL; HYPOXIC-ISCHEMIC ENCEPHALOPATHY; NEUROPROTECTION;

ANIMALS; BRAIN; BRAIN ISCHEMIA; CONNEXIN 43; FEMALE; FETUS; GAP JUNCTIONS; HYPOXIA-ISCHEMIA, BRAIN; NEUROPROTECTIVE AGENTS; OLIGOPEPTIDES; SHEEP;

EID: 84880618839     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2013.06.026     Document Type: Article

References (37)

1. Baroja-Mazo A., Barbera-Cremades M., Pelegrin P. The participation of plasma membrane hemichannels to purinergic signaling. Biochim. Biophys. Acta 2013, 1828:79-93.
2. Belluardo N., Mudo G., Trovato-Salinaro A., Le Gurun S., Charollais A., Serre-Beinier V., Amato G., Haefliger J.A., Meda P., Condorelli D.F. Expression of connexin36 in the adult and developing rat brain. Brain Res. 2000, 865:121-138.
3. Bennett M.V., Garre J.M., Orellana J.A., Bukauskas F.F., Nedergaard M., Saez J.C. Connexin and pannexin hemichannels in inflammatory responses of glia and neurons. Brain Res. 2012, 1487:3-15.
4. Contreras J.E., Sanchez H.A., Eugenin E.A., Speidel D., Theis M., Willecke K., Bukauskas F.F., Bennett M.V., Saez J.C. Metabolic inhibition induces opening of unapposed connexin 43 gap junction hemichannels and reduces gap junctional communication in cortical astrocytes in culture. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:495-500.
5. Cotrina M.L., Lin J.H., Alves-Rodrigues A., Liu S., Li J., Azmi-Ghadimi H., Kang J., Naus C.C., Nedergaard M. Connexins regulate calcium signaling by controlling ATP release. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:15735-15740.
6. Danesh-Meyer H.V., Kerr N.M., Zhang J., Eady E.K., O'Carroll S.J., Nicholson L.F., Johnson C.S., Green C.R. Connexin43 mimetic peptide reduces vascular leak and retinal ganglion cell death following retinal ischaemia. Brain 2012, 135:506-520.
7. Davidson J.O., Green C.R., Nicholson L.F., Bennet L., Gunn A.J. Deleterious effects of high dose connexin 43 mimetic peptide infusion after cerebral ischaemia in near-term fetal sheep. Int. J. Mol. Sci. 2012, 13:6303-6319.
8. Davidson J.O., Green C.R., Nicholson L.F., O'Carroll S.J., Fraser M., Bennet L., Gunn A.J. Connexin hemichannel blockade improves outcomes in a model of fetal ischemia. Ann. Neurol. 2012, 71:121-132.
9. Deans M.R., Gibson J.R., Sellitto C., Connors B.W., Paul D.L. Synchronous activity of inhibitory networks in neocortex requires electrical synapses containing connexin36. Neuron 2001, 31:477-485.
10. Decrock E., De Vuyst E., Vinken M., Van Moorhem M., Vranckx K., Wang N., Van Laeken L., De Bock M., D'Herde K., Lai C.P., Rogiers V., Evans W.H., Naus C.C., Leybaert L. Connexin 43 hemichannels contribute to the propagation of apoptotic cell death in a rat C6 glioma cell model. Cell Death Differ. 2009, 16:151-163.
11. Dobbing J., Sands J. Timing of neuroblast multiplication in developing human brain. Nature 1970, 226:639-640.
12. Faigle M., Seessle J., Zug S., El Kasmi K.C., Eltzschig H.K. ATP release from vascular endothelia occurs across Cx43 hemichannels and is attenuated during hypoxia. PLoS One 2008, 3:e2801.
13. Gunn A.J., Gunn T.R., de Haan H.H., Williams C.E., Gluckman P.D. Dramatic neuronal rescue with prolonged selective head cooling after ischemia in fetal lambs. J. Clin. Invest. 1997, 99:248-256.
14. Haupt C., Witte O.W., Frahm C. Up-regulation of Connexin43 in the glial scar following photothrombotic ischemic injury. Mol. Cell. Neurosci. 2007, 35:89-99.
15. Hossmann K.A. Pathophysiology and therapy of experimental stroke. Cell. Mol. Neurobiol. 2006, 26:1057-1083.
16. Jakovcevski I., Filipovic R., Mo Z., Rakic S., Zecevic N. Oligodendrocyte development and the onset of myelination in the human fetal brain. Front. Neuroanat. 2009, 3:5.
17. Kang J., Kang N., Lovatt D., Torres A., Zhao Z., Lin J., Nedergaard M. Connexin 43 hemichannels are permeable to ATP. J. Neurosci. 2008, 28:4702-4711.
18. Kondo R.P., Wang S.Y., John S.A., Weiss J.N., Goldhaber J.I. Metabolic inhibition activates a non-selective current through connexin hemichannels in isolated ventricular myocytes. J. Mol. Cell. Cardiol. 2000, 32:1859-1872.
19. Lauf U., Giepmans B.N., Lopez P., Braconnot S., Chen S.C., Falk M.M. Dynamic trafficking and delivery of connexons to the plasma membrane and accretion to gap junctions in living cells. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:10446-10451.
20. Li H., Liu T.F., Lazrak A., Peracchia C., Goldberg G.S., Lampe P.D., Johnson R.G. Properties and regulation of gap junctional hemichannels in the plasma membranes of cultured cells. J. Cell Biol. 1996, 134:1019-1030.
21. McIntosh G.H., Baghurst K.I., Potter B.J., Hetzel B.S. Foetal brain development in the sheep. Neuropathol. Appl. Neurobiol. 1979, 5:103-114.
22. Nakase T., Yoshida Y., Nagata K. Enhanced connexin 43 immunoreactivity in penumbral areas in the human brain following ischemia. Glia 2006, 54:369-375.
23. O'Carroll S.J., Alkadhi M., Nicholson L.F., Green C.R. Connexin 43 mimetic peptides reduce swelling, astrogliosis, and neuronal cell death after spinal cord injury. Cell Commun. Adhes. 2008, 15:27-42.
24. Orellana J.A., Hernandez D.E., Ezan P., Velarde V., Bennett M.V., Giaume C., Saez J.C. Hypoxia in high glucose followed by reoxygenation in normal glucose reduces the viability of cortical astrocytes through increased permeability of connexin 43 hemichannels. Glia 2010, 58:329-343.
25. Orellana J.A., Froger N., Ezan P., Jiang J.X., Bennett M.V., 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.
26. Peng W., Cotrina M.L., Han X., Yu H., Bekar L., Blum L., Takano T., Tian G.F., Goldman S.A., Nedergaard M. Systemic administration of an antagonist of the ATP-sensitive receptor P2X7 improves recovery after spinal cord injury. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:12489-12493.
27. Quist A.P., Rhee S.K., Lin H., Lal R. Physiological role of gap-junctional hemichannels. Extracellular calcium-dependent isosmotic volume regulation. J. Cell Biol. 2000, 148:1063-1074.
28. Rami A., Volkmann T., Winckler J. Effective reduction of neuronal death by inhibiting gap junctional intercellular communication in a rodent model of global transient cerebral ischemia. Exp. Neurol. 2001, 170:297-304.
29. Rodriguez-Sinovas A., Cabestrero A., Lopez D., Torre I., Morente M., Abellan A., Miro E., Ruiz-Meana M., Garcia-Dorado D. The modulatory effects of connexin 43 on cell death/survival beyond cell coupling. Prog. Biophys. Mol. Biol. 2007, 94:219-232.
30. Stangland K.J., Milde J.H., Michenfelder J.D. Canine cerebral function and blood flow after complete cerebral ischemia: effect of head position. Anesthesiology 1986, 64:430-434.
31. Stout C.E., Costantin J.L., Naus C.C., Charles A.C. Intercellular calcium signaling in astrocytes via ATP release through connexin hemichannels. J. Biol. Chem. 2002, 277:10482-10488.
32. Thompson R.J., Zhou N., MacVicar B.A. Ischemia opens neuronal gap junction hemichannels. Science 2006, 312:924-927.
33. Thornton J.S., Ordidge R.J., Penrice J., Cady E.B., Amess P.N., Punwani S., Clemence M., Wyatt J.S. Temporal and anatomical variations of brain water apparent diffusion coefficient in perinatal cerebral hypoxic-ischemic injury: relationships to cerebral energy metabolism. Magn. Reson. Med. 1998, 39:920-927.
34. Wibbens B., Westgate J.A., Bennet L., Roelfsema V., de Haan H.H., Hunter C.J., Gunn A.J. Profound hypotension and associated ECG changes during prolonged cord occlusion in the near term fetal sheep. Am. J. Obstet. Gynecol. 2005, 193:803-810.
35. Williams C.E., Gunn A., Gluckman P.D. Time course of intracellular edema and epileptiform activity following prenatal cerebral ischemia in sheep. Stroke 1991, 22:516-521.
36. Williams C.E., Gunn A.J., Mallard C., Gluckman P.D. Outcome after ischemia in the developing sheep brain: an electroencephalographic and histological study. Ann. Neurol. 1992, 31:14-21.
37. Ye Z.C., Wyeth M.S., Baltan-Tekkok S., Ransom B.R. Functional hemichannels in astrocytes: a novel mechanism of glutamate release. J. Neurosci. 2003, 23:3588-3596.