Non-additive effects of delayed connexin hemichannel blockade and hypothermia after cerebral ischemia in near-term fetal sheep

Journal of Cerebral Blood Flow and Metabolism

Volumn 35, Issue 12, 2015, Pages 2052-2061

  Davidson, Joanne O ^a   Rout, Alexandra L ^a   Wassink, Guido ^a   Yuill, Caroline A ^a   Zhang, Frank G ^a   Green, Colin R ^a   Bennet, Laura ^a   Gunn, Alistair J ^a  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

cerebral hypothermia; cerebral ischemia; connexin hemichannel; fetal sheep; neuroprotection

Indexed keywords

CONNEXIN HEMICHANNEL BLOCKADE; NEUROPROTECTIVE AGENT; UNCLASSIFIED DRUG; GAP JUNCTION PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN ISCHEMIA; CELL SURVIVAL; CONTROLLED STUDY; ELECTROENCEPHALOGRAPHY; FETUS; INDUCED HYPOTHERMIA; MICROGLIA; NEUROPROTECTION; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; SEIZURE; ANIMAL; ANTAGONISTS AND INHIBITORS; BLOOD GAS ANALYSIS; BODY TEMPERATURE; BRAIN CIRCULATION; FEMALE; INTRACEREBROVENTRICULAR DRUG ADMINISTRATION; NERVE CELL; PATHOLOGY; PREGNANCY; SHEEP;

ANIMALS; BLOOD GAS ANALYSIS; BODY TEMPERATURE; BRAIN ISCHEMIA; CELL SURVIVAL; CEREBROVASCULAR CIRCULATION; CONNEXINS; ELECTROENCEPHALOGRAPHY; FEMALE; FETUS; HYPOTHERMIA, INDUCED; INJECTIONS, INTRAVENTRICULAR; NEURONS; NEUROPROTECTIVE AGENTS; OLIGODENDROGLIA; PREGNANCY; SHEEP;

EID: 84944772135     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2015.171     Document Type: Article

References (46)

1. Edwards AD, Brocklehurst P, Gunn AJ, Halliday H, Juszczak E, Levene M, et al. Neurological outcomes at 18 months of age after moderate hypothermia for perinatal hypoxic ischaemic encephalopathy: synthesis and meta-Analysis of trial data. BMJ. 2010; 340: c363.
2. Azzopardi D, Strohm B, Marlow N, Brocklehurst P, Deierl A, Eddama O, et al. Effects of hypothermia for perinatal asphyxia on childhood outcomes. N Engl J Med. 2014; 371: 140-149.
3. Shankaran S, Pappas A, McDonald SA, Vohr BR, Hintz SR, Yolton K, et al. Childhood outcomes after hypothermia for neonatal encephalopathy. N Engl J Med. 2012; 366: 2085-2092.
4. Guillet R, Edwards AD, Thoresen M, Ferriero DM, Gluckman PD, Whitelaw A, et al. Seven- To eight-year follow-up of the CoolCap trial of head cooling for neonatal encephalopathy. Pediatr Res. 2012; 71: 205-209.
5. Davidson JO, Wassink G, Yuill CA, Zhang FG, Bennet L, Gunn AJ. How long is too long for cerebral cooling after ischemia in fetal sheep?. J Cereb Blood Flow Metab. 2015; 35: 751-758.
6. Shankaran S, Laptook AR, Pappas A, McDonald SA, Das A, Tyson JE, et al. Effect of depth and duration of cooling on deaths in the NICU among neonates with hypoxic ischemic encephalopathy: a randomized clinical trial. JAMA. 2014; 312: 2629-2639.
7. Gunn AJ, Thoresen M. Hypothermic neuroprotection. NeuroRx. 2006; 3: 154-169.
8. Thoresen M, Tooley J, Liu X, Jary S, Fleming P, Luyt K, et al. Time is brain: starting therapeutic hypothermia within three hours after birth improves motor outcome in asphyxiated newborns. Neonatology. 2013; 104: 228-233.
9. Gluckman PD, Wyatt JS, Azzopardi D, Ballard R, Edwards AD, Ferriero DM, et al. Selective head cooling with mild systemic hypothermia after neonatal encephalopathy: multicentre randomised trial. Lancet. 2005; 365: 663-670.
10. Davidson JO, Green CR, Bennet L, Gunn AJ. Battle of the hemichannels - Connexins and Pannexins in ischemic brain injury. Int J Dev Neurosci. 2014; pii: S0736-5748(14)00209-3.
11. Nakase T, Yoshida Y, Nagata K. Enhanced connexin 43 immunoreactivity in penumbral areas in the human brain following ischemia. Glia. 2006; 54: 369-375.
12. Davidson JO, Green CR, Nicholson LF, O'Carroll SJ, Fraser M, Bennet L, et al. Connexin hemichannel blockade improves outcomes in a model of fetal ischemia. Ann Neurol. 2012; 71: 121-132.
13. Kang J, Kang N, Lovatt D, Torres A, Zhao Z, Lin J, et al. Connexin 43 hemichannels are permeable to ATP. J Neurosci. 2008; 28: 4702-4711.
14. Ye ZC, Wyeth MS, Baltan-Tekkok S, Ransom BR. Functional hemichannels in astrocytes: a novel mechanism of glutamate release. J Neurosci. 2003; 23: 3588-3596.
15. Rodriguez-Sinovas A, Cabestrero A, Lopez D, Torre I, Morente M, Abellan A, et al. The modulatory effects of connexin 43 on cell death/survival beyond cell coupling. Prog Biophys Mol Biol. 2007; 94: 219-232.
16. Quist AP, Rhee SK, Lin H, Lal R. Physiological role of gap-junctional hemichannels. Extracellular calcium-dependent isosmotic volume regulation. J Cell Biol. 2000; 148: 1063-1074.
17. Davidson JO, Green CR, Nicholson LF, Bennet L, Gunn AJ. Connexin hemichannel blockade is neuroprotective after, but not during, global cerebral ischemia in near-Term fetal sheep. Exp Neurol. 2013; 248: 301-308.
18. Davidson JO, Drury PP, Green CR, Nicholson LF, Bennet L, Gunn AJ. Connexin hemichannel blockade is neuroprotective after asphyxia in preterm fetal sheep. PLoS One. 2014; 9: e96558.
19. Robertson NJ, Faulkner S, Fleiss B, Bainbridge A, Andorka C, Price D, et al. Melatonin augments hypothermic neuroprotection in a perinatal asphyxia model. Brain. 2013; 136: 90-105.
20. Barks JD, Liu YQ, Shangguan Y, Silverstein FS. Phenobarbital augments hypothermic neuroprotection. Pediatr Res. 2010; 67: 532-537.
21. Liu Y, Barks JD, Xu G, Silverstein FS. Topiramate extends the therapeutic window for hypothermia-mediated neuroprotection after stroke in neonatal rats. Stroke. 2004; 35: 1460-1465.
22. Gunn AJ, Gunn TR, de Haan HH, Williams CE, Gluckman PD. Dramatic neuronal rescue with prolonged selective head cooling after ischemia in fetal lambs. J Clin Invest. 1997; 99: 248-256.
23. Williams CE, Gunn AJ, Mallard C, Gluckman PD. Outcome after ischemia in the developing sheep brain: an electroencephalographic and histological study. Ann Neurol. 1992; 31: 14-21.
24. Quaedackers JS, Roelfsema V, Hunter CJ, Heineman E, Gunn AJ, Bennet L. Polyuria and impaired renal blood flow after asphyxia in preterm fetal sheep. Am J Physiol Regul Integr Comp Physiol. 2004; 286: R576-R583.
25. Wibbens B, Westgate JA, Bennet L, Roelfsema V, de Haan HH, Hunter CJ, et al. Profound hypotension and associated ECG changes during prolonged cord occlusion in the near term fetal sheep. Am J Obstet Gynecol. 2005; 193: 803-810.
26. O'Carroll SJ, Alkadhi M, Nicholson LF, Green CR. Connexin 43 mimetic peptides reduce swelling, astrogliosis, and neuronal cell death after spinal cord injury. Cell Commun Adhes. 2008; 15: 27-42.
27. Davidson JO, Green CR, Nicholson LF, Bennet L, Gunn AJ. Deleterious effects of high dose connexin 43 mimetic peptide infusion after cerebral ischaemia in nearterm fetal sheep. Int J Mol Sci. 2012; 13: 6303-6319.
28. Smith DC. Effects of skin blood flow and temperature on skin-electrode impedance and offset potential: measurements at low alternating current density. J Med Eng Technol. 1992; 16: 112-116.
29. Pozo Devoto VM, Chavez JC, Fiszer de Plazas S. Acute hypoxia and programmed cell death in developing CNS: Differential vulnerability of chick optic tectum layers. Neuroscience. 2006; 142: 645-653.
30. Thornton JS, Ordidge RJ, Penrice J, Cady EB, Amess PN, Punwani S, et al. 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.
31. Gonzalez H, Hunter CJ, Bennet L, Power GG, Gunn AJ. Cerebral oxygenation during post-Asphyxial seizures in near-Term fetal sheep. J Cereb Blood Flow Metab. 2005; 25: 911-918.
32. Drury PP, Gunn ER, Bennet L, Gunn AJ. Mechanisms of hypothermic neuroprotection. Clin Perinatol. 2014; 41: 161-175.
33. van Bel F, Dorrepaal CA, Benders MJ, Zeeuwe PE, van de Bor M, Berger HM. Changes in cerebral hemodynamics and oxygenation in the first 24 hours after birth asphyxia. Pediatrics. 1993; 92: 365-372.
34. Karlsson BR, Grogaard B, Gerdin B, Steen PA. The severity of postischemic hypoperfusion increases with duration of cerebral ischemia in rats. Acta Anaesthesiol Scand. 1994; 38: 248-253.
35. Michenfelder JD, Milde JH. Postischemic canine cerebral blood flow appears to be determined by cerebral metabolic needs. J Cereb Blood Flow Metab. 1990; 10: 71-76.
36. Gold L, Lauritzen M. Neuronal deactivation explains decreased cerebellar blood flow in response to focal cerebral ischemia or suppressed neocortical function. Proc Natl Acad Sci USA. 2002; 99: 7699-7704.
37. Jensen EC, Bennet L, Hunter CJ, Power GC, Gunn AJ. Post-hypoxic hypoperfusion is associated with suppression of cerebral metabolism and increased tissue oxygenation in near-Term fetal sheep. J Physiol. 2006; 572: 131-139.
38. Gunn AJ, Gunn TR, Gunning MI, Williams CE, Gluckman PD. Neuroprotection with prolonged head cooling started before postischemic seizures in fetal sheep. Pediatrics. 1998; 102: 1098-1106.
39. Elstad M, Whitelaw A, Thoresen M. Cerebral Resistance Index is less predictive in hypothermic encephalopathic newborns. Acta Paediatr. 2011; 100: 1344-1349.
40. Laptook AR, Corbett RJ, Sterett R, Garcia D, Tollefsbol G. Quantitative relationship between brain temperature and energy utilization rate measured in vivo using 31 P and 1H magnetic resonance spectroscopy. Pediatr Res. 1995; 38: 919-925.
41. Brink PR. Gap junctions in vascular smooth muscle. Acta Physiol Scand. 1998; 164: 349-356.
42. Danesh-Meyer HV, Kerr NM, Zhang J, Eady EK, O'Carroll SJ, Nicholson LF, et al. Connexin43 mimetic peptide reduces vascular leak and retinal ganglion cell death following retinal ischaemia. Brain. 2012; 135: 506-520.
43. George SA, Bennet L, Weaver-Mikaere L, Fraser M, Bouwmans J, Mathai S, et al. White matter protection with insulin like-growth factor 1 (IGF-1) and hypothermia is not additive after severe reversible cerebral ischemia in term fetal sheep. Dev Neurosci. 2011; 33: 280-287.
44. George SA, Barrett RD, Bennet L, Mathai S, Jensen EC, Gunn AJ. Nonadditive neuroprotection with early glutamate receptor blockade and delayed hypothermia after asphyxia in preterm fetal sheep. Stroke. 2012; 43: 3114-3117.
45. Liu X, Dingley J, Scull-Brown E, Thoresen M. Adding 5 hours delayed xenon to delayed hypothermia treatment improves long term function in neonatal rats surviving to adulthood. Pediatr Res. 2015; 77: 779-783.
46. Traudt CM, McPherson RJ, Bauer LA, Richards TL, Burbacher TM, McAdams RM, et al. Concurrent erythropoietin and hypothermia treatment improve outcomes in a term nonhuman primate model of perinatal asphyxia. Dev Neurosci. 2013; 35: 491-503.