Post-hypoxic hypothermia is protective in human NT2-N neurons regardless of oxygen concentration during reoxygenation

Brain Research

Volumn 1259, Issue , 2009, Pages 80-89

  Dalen, Marit Lunde ^a   Frøyland, Elisabeth ^a   Saugstad, Ola Didrik ^a   Mollnes, Tom Eirik ^a   Rootwelt, Terje ^a  

^a OSLO UNIVERSITY HOSPITAL   (Norway)

Author keywords

Hyperoxia; Hypothermia; Hypoxia; In vitro; Inflammation; Neuron

Indexed keywords

BASIC FIBROBLAST GROWTH FACTOR; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GLUCOSE; HYPOXANTHINE; INTERLEUKIN 8; MONOCYTE CHEMOTACTIC PROTEIN 1;

ARTICLE; BODY TEMPERATURE; BRAIN NERVE CELL; CELL ASSAY; CELL ENERGY; CELL VIABILITY; CONTROLLED STUDY; HUMAN; HUMAN CELL; HYPOTHERMIA; HYPOXIA; INFLAMMATION; OXYGEN CONCENTRATION; PRIORITY JOURNAL; REOXYGENATION;

ANOXIA; CELL LINE; CELL SURVIVAL; CHEMOKINE CCL2; CHEMOKINE CXCL10; FIBROBLAST GROWTH FACTOR 2; GLUCOSE; HUMANS; HYPOTHERMIA, INDUCED; HYPOXANTHINE; HYPOXIA, BRAIN; INTERLEUKIN-8; NEURONS; OXYGEN; TEMPERATURE;

EID: 61549138112     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2008.12.055     Document Type: Article

References (66)

1. Almaas R., Saugstad O.D., Pleasure D., and Rootwelt T. Effect of barbiturates on hydroxyl radicals, lipid peroxidation, and hypoxic cell death in human NT2-N neurons. Anesthesiology 92 (2000) 764-774
2. Almaas R., Saugstad O.D., Pleasure D., and Rootwelt T. Neuronal formation of free radicals plays a minor role in hypoxic cell death in human NT2-N neurons. Pediatr. Res. 51 2 (2002) 136-143
3. Almaas R., Pytte M., Lindstad J.K., Wright M., Saugstad O.D., Pleasure D., and Rootwelt T. Acidosis has opposite effects on neuronal survival during hypoxia and reoxygenation. J. Neurochem. 84 5 (2003) 1018-1027
4. Bernard S.A., Gray T.W., Buist M.D., Jones B.M., Silvester W., Gutteridge G., and Smith K. Treatment of comatose survivors of out-of-hospital cardiac arrest with induced hypothermia. N. Engl. J. Med. 346 (2002) 557-563
5. Bruno V.M., Goldberg M.P., Dugan L.L., Giffard R.G., and Choi D.W. Neuroprotective effect of hypothermia in cortical cultures exposed to oxygen-glucose deprivation or excitatory amino acids. J. Neurochem. 63 (1994) 1398-1406
6. Colton C.A., Pagan F., Snell J., Colton J.S., Cummins A., and Gilbert D.L. Protection from oxidation enhances the survival of cultured mesencephalic neurons. Exp. Neurol. 132 (1995) 54-61
7. Deng H., Han H.S., Cheng D., Sun G.H., and Yenari M.A. Mild hypothermia inhibits inflammation after experimental stroke and brain inflammation. Stroke 34 (2003) 2495-2501
8. Enokido Y., and Hatanaka H. Apoptotic cell death occurs in hippocampal neurons cultured in a high oxygen atmosphere. Neuroscience 57 (1993) 965-972
9. Feet B.A., Yu X.Q., Rootwelt T., Oyasaeter S., and Saugstad O.D. Effects of hypoxemia and reoxygenation with 21% or 100% oxygen in newborn piglets: extracellular hypoxanthine in cerebral cortex and femoral muscle. Crit. Care Med. 25 (1997) 1384-1391
10. Feiner J.R., Bickler P.E., Estrada S., Donohoe P.H., Fahlman C.S., and Schuyler J.A. Mild hypothermia, but not propofol, is neuroprotective in organotypic hippocampal cultures. Anesth. Analg. 100 (2005) 215-225
11. Felderhoff-Mueser U., Bittigau P., Sifringer M., Jarosz B., Korobowicz E., Mahler L., Piening T., Moysich A., Grune T., Thor F., Heumann R., Buhrer C., and Ikonomidou C. Oxygen causes cell death in the developing brain. Neurobiol. Dis. 17 (2004) 273-282
12. Felderhoff-Mueser U., Sifringer M., Polley O., Dzietko M., Leineweber B., Mahler L., Baier M., Bittigau P., Obladen M., Ikonomidou C., and Buhrer C. Caspase-1-processed interleukins in hyperoxia-induced cell death in the developing brain. Ann. Neurol. 57 (2005) 50-59
13. Froyland E., Wibrand F., Almaas R., Dalen I., Lindstad J.K., and Rootwelt T. Acidosis during reoxygenation has an early detrimental effect on neuronal metabolic activity. Pediatr. Res. 57 4 (2005) 488-493
14. Froyland E., Didenko P.E., Kvissel A.K., Almaas R., Pharo A., Skalhegg B.S., Mollnes T.E., and Rootwelt T. Effect of acidosis on IL-8 and MCP-1 during hypoxia and reoxygenation in human NT2-N neurons. Brain Res. 1113 (2006) 64-73
15. Froyland E., Skjaeret C., Wright M.S., Dalen M.L., Cvancarova M., Kasi C., and Rootwelt T. Inflammatory receptors and pathways in human NT2-N neurons during hypoxia and reoxygenation. Impact of acidosis. Brain Res. 1217 (2008) 37-49
16. Fukui O., Kinugasa Y., Fukuda A., Fukuda H., Tskitishvili E., Hayashi S., Song M., Kanagawa T., Hosono T., Shimoya K., and Murata Y. Post-ischemic hypothermia reduced IL-18 expression and suppressed microglial activation in the immature brain. Brain Res. 1121 (2006) 35-45
17. Gluckman P.D., Wyatt J.S., Azzopardi D., Ballard R., Edwards A.D., Ferriero D.M., Polin R.A., Robertson C.M., Thoresen M., Whitelaw A., and Gunn A.J. Selective head cooling with mild systemic hypothermia after neonatal encephalopathy: multicentre randomised trial. Lancet 365 (2005) 663-670
18. Gunn A.J., and Thoresen M. Hypothermic neuroprotection. NeuroRx 3 (2006) 154-169
19. Gunn A.J., Gunn T.R., de Haan H.H., Williams C.E., and Gluckman P.D. Dramatic neuronal rescue with prolonged selective head cooling after ischemia in fetal lambs. J. Clin. Invest. 99 (1997) 248-256
20. Guo Q., Sebastian L., Sopher B.L., Miller M.W., Glazner G.W., Ware C.B., Martin G.M., and Mattson M.P. Neurotrophic factors [activity-dependent neurotrophic factor (ADNF) and basic fibroblast growth factor (bFGF)] interrupt excitotoxic neurodegenerative cascades promoted by a PS1 mutation. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 4125-4130
21. Han H.S., Karabiyikoglu M., Kelly S., Sobel R.A., and Yenari M.A. Mild hypothermia inhibits nuclear factor-kappaB translocation in experimental stroke. J. Cereb. Blood Flow Metab. 23 (2003) 589-598
22. Hedtjarn M., Mallard C., and Hagberg H. Inflammatory gene profiling in the developing mouse brain after hypoxia-ischemia. J. Cereb. Blood Flow Metab. 24 (2004) 1333-1351
23. Horiguchi T., Shimizu K., Ogino M., Suga S., Inamasu J., and Kawase T. Postischemic hypothermia inhibits the generation of hydroxyl radical following transient forebrain ischemia in rats. J. Neurotrauma 20 (2003) 511-520
24. Jacobs S., Hunt R., Tarnow-Mordi W., Inder T., and Davis P. Cooling for newborns with hypoxic ischaemic encephalopathy,. Cochrane Database Syst. Rev. (2007). http://doi:10.1002/14651858.CD003311.pub2 Issue 4. Art. No.: CD003311. doi:10.1002/14651858.CD003311.pub2
25. Kadhim H., Tabarki B., Verellen G., De P.C., Rona A.M., and Sebire G. Inflammatory cytokines in the pathogenesis of periventricular leukomalacia. Neurology 56 (2001) 1278-1284
26. Kaplan F.S., Brighton C.T., Boytim M.J., Selzer M.E., Lee V., Spindler K., Silberberg D., and Black J. Enhanced survival of rat neonatal cerebral cortical neurons at subatmospheric oxygen tensions in vitro. Brain Res. 384 (1986) 199-203
27. Khanna S., Roy S., Maurer M., Ratan R.R., and Sen C.K. Oxygen-sensitive reset of hypoxia-inducible factor transactivation response: prolyl hydroxylases tune the biological normoxic set point. Free Radic. Biol. Med. 40 (2006) 2147-2154
28. Koch J.D., Miles D.K., Gilley J.A., Yang C.P., and Kernie S.G. Brief exposure to hyperoxia depletes the glial progenitor pool and impairs functional recovery after hypoxic-ischemic brain injury. J. Cereb. Blood Flow Metab. 28 (2008) 1294-1306
29. Laptook A.R., Corbett R.J., Sterett R., Burns D.K., Garcia D., and Tollefsbol G. Modest hypothermia provides partial neuroprotection when used for immediate resuscitation after brain ischemia. Pediatr. Res. 42 (1997) 17-23
30. Lawrence E.J., Dentcheva E., Curtis K.M., Roberts V.L., Siman R., and Neumar R.W. Neuroprotection with delayed initiation of prolonged hypothermia after in vitro transient global brain ischemia. Resuscitation 64 (2005) 383-388
31. Lin T.N., Te J., Lee M., Sun G.Y., and Hsu C.Y. Induction of basic fibroblast growth factor (bFGF) expression following focal cerebral ischemia. Brain Res. Mol. Brain Res. 49 (1997) 255-265
32. Ma D., Hossain M., Chow A., Arshad M., Battson R.M., Sanders R.D., Mehmet H., Edwards A.D., Franks N.P., and Maze M. Xenon and hypothermia combine to provide neuroprotection from neonatal asphyxia. Ann. Neurol. 58 (2005) 182-193
33. Markus T., Hansson S., mer-Wahlin I., Hellstrom-Westas L., Saugstad O.D., and Ley D. Cerebral inflammatory response after fetal asphyxia and hyperoxic resuscitation in newborn sheep. Pediatr. Res. 62 (2007) 71-77
34. McGuire W. Perinatal asphyxia. Clin. Evid. (2006) 511-519
35. Munir M., Lu L., and Mcgonigle P. Excitotoxic cell death and delayed rescue in human neurons derived from NT2 cells. J. Neurosci. 15 (1995) 7847-7860
36. Munkeby B.H., Borke W.B., Bjornland K., Sikkeland L.I., Borge G.I., Halvorsen B., and Saugstad O.D. Resuscitation with 100% O2 increases cerebral injury in hypoxemic piglets. Pediatr. Res. 56 5 (2004) 783-790
37. Munkeby B.H., Borke W.B., Bjornland K., Sikkeland L.I., Borge G.I., Lomo J., Rivera S., Khrestchatisky M., Halvorsen B., and Saugstad O.D. Resuscitation of hypoxic piglets with 100% O2 increases pulmonary metalloproteinases and IL-8. Pediatr. Res. 58 3 (2005) 542-548
38. Nakamura T., Miyamoto O., Kawai N., Negi T., Itano T., and Nagao S. Long-term activation of the glutamatergic system associated with N-methyl-D-aspartate receptors after postischemic hypothermia in gerbils. Neurosurgery 49 (2001) 706-713
39. Oillet J., Koziel V., Vert P., and Daval J.L. Influence of post-hypoxia reoxygenation conditions on energy metabolism and superoxide production in cultured neurons from the rat forebrain. Pediatr. Res. 39 (1996) 598-603
40. Pleasure S.J., Page C., and Lee V.M. Pure, postmitotic, polarized human neurons derived from NTera 2 cells provide a system for expressing exogenous proteins in terminally differentiated neurons. J. Neurosci. 12 (1992) 1802-1815
41. Popovic R., Liniger R., and Bickler P.E. Anesthetics and mild hypothermia similarly prevent hippocampal neuron death in an in vitro model of cerebral ischemia. Anesthesiology 92 (2000) 1343-1349
42. Ramani R. Hypothermia for brain protection and resuscitation. Curr. Opin. Anaesthesiol. 19 (2006) 487-491
43. Ramji S., Ahuja S., Thirupuram S., Rootwelt T., Rooth G., and Saugstad O.D. Resuscitation of asphyxic newborn infants with room air or 100% oxygen. Pediatr. Res. 34 (1993) 809-812
44. Rootwelt T., Odden J.P., Hall C., Ganes T., and Saugstad O.D. Cerebral blood flow and evoked potentials during reoxygenation with 21 or 100% O2 in newborn pigs. J. Appl. Physiol. 75 (1993) 2054-2060
45. Rootwelt T., Dunn M., Yudkoff M., Itoh T., Almaas R., and Pleasure D. Hypoxic cell death in human NT2-N neurons: involvement of NMDA and non-NMDA glutamate receptors. J. Neurochem. 71 4 (1998) 1544-1553
46. Roth S.C., Baudin J., Cady E., Johal K., Townsend J.P., Wyatt J.S., Reynolds E.O., and Stewart A.L. Relation of deranged neonatal cerebral oxidative metabolism with neurodevelopmental outcome and head circumference at 4 years. Dev. Med. Child Neurol. 39 (1997) 718-725
47. Saliba E., and Henrot A. Inflammatory mediators and neonatal brain damage. Biol. Neonate 79 (2001) 224-227
48. Saugstad O.D. Hypoxanthine as a measurement of hypoxia. Pediatr. Res. 9 (1975) 158-161
49. Saugstad O.D. Hypoxanthine as an indicator of hypoxia: its role in health and disease through free radical production. Pediatr. Res. 23 (1988) 143-150
50. Saugstad O.D., Rootwelt T., and Aalen O. Resuscitation of asphyxiated newborn infants with room air or oxygen: an international controlled trial: the Resair 2 study. Pediatrics 102 (1998) e1
51. Saugstad O.D., Ramji S., Soll R.F., and Vento M. Resuscitation of newborn infants with 21% or 100% oxygen: an updated systematic review and meta-analysis. Neonatology. 94 (2008) 176-182
52. Saxena M., Andrews P.J., and Cheng A. Modest cooling therapies (35 degrees C to 37.5 degrees C) for traumatic brain injury, Cochrane. Database Syst. Rev. (2008). http://doi:10.1002/14651858.CD006811.pub2 Issue 3. Art. No.: CD006811. doi:10.1002/14651858.CD006811.pub2
53. Shankaran S., Laptook A.R., Ehrenkranz R.A., Tyson J.E., McDonald S.A., Donovan E.F., Fanaroff A.A., Poole W.K., Wright L.L., Higgins R.D., Finer N.N., Carlo W.A., Duara S., Oh W., Cotten C.M., Stevenson D.K., Stoll B.J., Lemons J.A., Guillet R., and Jobe A.H. Whole-body hypothermia for neonates with hypoxic-ischemic encephalopathy. N. Engl. J. Med. 353 (2005) 1574-1584
54. Si Q.S., Nakamura Y., and Kataoka K. Hypothermic suppression of microglial activation in culture: inhibition of cell proliferation and production of nitric oxide and superoxide. Neuroscience 81 (1997) 223-229
55. Solberg R., Andresen J.H., Escrig R., Vento M., and Saugstad O.D. Resuscitation of hypoxic newborn piglets with oxygen induces a dose-dependent increase in markers of oxidation. Pediatr. Res. 62 (2007) 559-563
56. Tamatani M., Ogawa S., and Tohyama M. Roles of Bcl-2 and caspases in hypoxia-induced neuronal cell death: a possible neuroprotective mechanism of peptide growth factors. Brain Res. Mol. Brain Res. 58 (1998) 27-39
57. The Hypothermia After Cardiac Arrest Study Group. Mild therapeutic hypothermia to improve the neurologic outcome after cardiac arrest. N. Engl. J. Med. 346 (2002) 549-556
58. Thoresen M., Penrice J., Lorek A., Cady E.B., Wylezinska M., Kirkbride V., Cooper C.E., Brown G.C., Edwards A.D., and Wyatt J.S. Mild hypothermia after severe transient hypoxia-ischemia ameliorates delayed cerebral energy failure in the newborn piglet. Pediatr. Res. 37 5 (1995) 667-670
59. Thoresen M., Satas S., Puka-Sundvall M., Whitelaw A., Hallstrom A., Loberg E.M., Ungerstedt U., Steen P.A., and Hagberg H. Post-hypoxic hypothermia reduces cerebrocortical release of NO and excitotoxins. NeuroReport 8 15 (1997) 3359-3362
60. Tooley J.R., Satas S., Porter H., Silver I.A., and Thoresen M. Head cooling with mild systemic hypothermia in anesthetized piglets is neuroprotective. Ann. Neurol. 53 (2003) 65-72
61. Vannucci S.J., and Hagberg H. Hypoxia-ischemia in the immature brain. J. Exp. Biol. 207 (2004) 3149-3154
62. Vento M., Asensi M., Sastre J., Lloret A., Garcia-Sala F., and Vina J. Oxidative stress in asphyxiated term infants resuscitated with 100% oxygen. J. Pediatr. 142 (2003) 240-246
63. Vento M., Sastre J., Asensi M.A., and Vina J. Room-air resuscitation causes less damage to heart and kidney than 100% oxygen. Am. J. Respir. Crit. Care Med. 172 (2005) 1393-1398
64. Wyatt J.S., Gluckman P.D., Liu P.Y., Azzopardi D., Ballard R., Edwards A.D., Ferriero D.M., Polin R.A., Robertson C.M., Thoresen M., Whitelaw A., and Gunn A.J. Determinants of outcomes after head cooling for neonatal encephalopathy. Pediatrics 119 (2007) 912-921
65. Xu L., Yenari M.A., Steinberg G.K., and Giffard R.G. Mild hypothermia reduces apoptosis of mouse neurons in vitro early in the cascade. J. Cereb. Blood Flow Metab. 22 (2002) 21-28
66. Yenari M.A., and Han H.S. Influence of hypothermia on post-ischemic inflammation: role of nuclear factor kappa B (NFkappaB). Neurochem. Int. 49 (2006) 164-169