Therapeutic hypothermia: Critical review of the molecular mechanisms of action

Frontiers in Neurology

Volumn FEB, Issue , 2011, Pages

  González Ibarra, Fernando Pavel ^a   Varon, Joseph ^b,c   López Meza, Elmer G ^a  

^a Internal Medicine and Neurology at Culiacan General Hospital   (Mexico)

^b UNIVERSITY OF TEXAS   (United States)

^c UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

Author keywords

Cerebral ischemia; Excitatory neurotransmitters; Mechanism of action; Neuronal acidosis; Neuronal death; Therapeutic hypothermia

Indexed keywords

EID: 79960988512     PISSN: None     EISSN: 16642295     Source Type: Journal    
DOI: 10.3389/fneur.2011.00004     Document Type: Article

References (88)

1. Aibiki, M., Maekawa, S., and Yokono, S. (2000). Moderate hypothermia improves imbalances of thromboxane A2 and prostaglandin I2 production after traumatic brain injury in humans. Crit. Care Med. 28, 3902-3906.
2. Alzaga, A. G., Cerdan, M., and Varon, J. (2006). Therapeutic hypothermia. Resuscitation 70, 369-380.
3. Baker, A. J., Zornow, M. H., Grafe, M. R., Scheller, M. S., Skilling, S. R., Smullin, D. H., and Larson, A. A. (1991). Hypothermia prevents ischemia-induced increases in hippocampal glycine concentrations in rabbits. Stroke 22, 666-673.
4. Bargonetti, J., and Manfredi, J. J. (2002). Multiple roles of the tumor suppressor p53. Curr. Opin. Oncol. 14, 86-91.
5. Beckman, J. S., Beckman, T. W., Chen, J., Marshall, P. A., and Freeman, B. A. (1990). Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc. Natl. Acad. Sci. U.S.A. 87, 1620-1624.
6. Benveniste, H., Drejer, J., Schousboe, A., and Diemer, N. H. (1984). Elevation of the extracellular concentrations of glutamate and aspartate in rat hippocampus during transient cerebral ischemia monitored by intracerebral microdialysis. J. Neurochem. 43, 1369-1374.
7. Berger, C., Schabitz, W. R., Wolf, M., Mueller, H., Sommer, C., and Schwab, S. (2004). Hypothermia and brain-derived neurotrophic factor reduce glutamate synergisti-cally in acute stroke. Exp. Neurol. 185, 305-312.
8. Bernard, S. A., Gray, T. W., Buist, M. D., Jones, B. M., Silvester, W., Gutteridge, G., and Smith, K. (2002). Treatment of comatose survivors of out-of-the hospital cardiac arrest with induced hypothermia. N. Engl. J. Med. 346, 557-563.
9. Bossenmeyer-Pourie, C., Koziel, V., and Daval, J. L. (2000). Effects of hypothermia on hypoxia-induced apoptosis in cultured neurons from developing rat forebrain: comparison with preconditioning. Pediatr. Res. 47, 385-391.
10. Bright, R., Raval, A. P., Dembner, J. M., Pérez-Pinzón M. A., Steinberg G. K., Yenari M. A., and Mochly-Rosen, D. (2004). Protein kinase C delta mediates cerebral reperfusion injury in vivo. J. Neurosci. 24, 6880-6888.
11. Brunner, T., Mogil, R. J., LaFace, D., Yoo, N. J., Mahboubi, M., Echeverri, F., Martin, S. J., Force, W. R., Lynch, D. H., Ware, C. F., and Green, D. R. (1995). Cellautonomous Fas (CD95)/Fas ligand interaction mediates activation-induced apoptosis in T-cell hybridomas. Nature 373, 441-444.
12. Carafoli, E. (1987). Intracellular calcium homeostasis. Annu. Rev. Biochem. 56, 395-433.
13. Chi, O. Z., Liu, X., and Weiss, H. R. (2001). Effects of mild hypothermia on blood - brain barrier disruption during isoflurane or pentobarbital anesthesia. Anesthesiology 95, 933-938.
14. Corry, J. J., Dhar, R., Murphy, T., and Diringer, M. N. (2008). Hypothermia for refractory status epilepticus. Neurocrit. Care 9, 189-197.
15. D'Cruz, B. J., Fertig, K. C., Filiano, A. J., Hicks, S. D., DeFranco, D. B., and Callaway, C. W. (2002). Hypothermic reperfusion after cardiac arrest augments brain-derived neurotrophic factor activation. J. Cereb. Blood Flow Metab. 22, 843-851.
16. Dietrich, W. D. III. (2009). Therapeutic hypothermia for spinal cord injury. Crit. Care Med. 37(Suppl. 7), S238-S242.
17. Dogné, J. M., Hanson, J., de Leval, X., Masereel, B., Kolh, P., and Pirotte, B. (2004). New developments on thromboxane modulators. Mini Rev. Med. Chem. 4, 649-657.
18. Foster, A. C., and Fagg, G. E. (1987). Taking apart NMDA receptors. Nature 329, 395-396.
19. Gehrmann, J., Bonnekoh, P., Miyazawa, T., Hossmann, K. A., and Kreutzberg, G. W. (1992). Immunocytochemical study of an early microglial activation in ischemia. J. Cereb. Blood Flow Metab. 12, 257-269.
20. Globus, M. Y., Alonso, O., Dietrich, W. D., Busto, R., and Ginsberg, M. D. (1995a). Glutamate release and free radical production following brain injury: effects of posttraumatic hypothermia. J. Neurochem. 65, 1704-1711.
21. Globus, M. Y., Busto, R., Lin, B., Schnippering, H., and Ginsberg, M. D. (1995b). Detection of free radical activity during transient global ischemia and recirculation: effects of intra-ischemic brain temperature modulation. J. Neurochem. 65, 1250-1256.
22. Globus, M. Y-T., Busto, R., Dietrich, W. D., Martinez, E., Valdes, I., and Ginsberg, M. D. (1988). Effect on ischemia on the in vivo release of striatal dopamine, glutamate, and gamma-aminobutyric acid studied by intracerebral microdialysis. J. Neurochem. 51, 1455-1464.
23. González, I. F. P., Martínez, F. J. I., and García, T. E. (2009). Therapeutic hypothermia in traumatic brain injury. A. S. Sin. 3, 21-26.
24. Hachimi-Idrissi, S., Van Hemelrijck, A., Michotte, A., Smolders, I., Sarre, S., Ebinger, G., Huyghens, L., and Michotte, Y. (2004). Postischemic mild hypothermia reduces neurotransmitter release and astroglial cell proliferation during reperfusion after asphyxial cardiac arrest in rats. Brain Res. 1019, 217-225.
25. Hagerdal, M., Harp, J., Nilsson, L., and Siesjo, B. K. (1975). The effect of induced hypothermia upon oxygen consumption in the rat brain. J. Neurochem. 24, 311-316.
26. Horiguchi, T., Shimizu, K., Ogino, M., Suga, S., Inamasu, J., and Kawase, T. (2003). Postischemic hypothermia inhibits the generation of hydroxyl radical following transient forebrain ischemia in rats. J. Neurotrauma 20, 511-520.
27. Huang, X. C., Xu, W., and Jiang, J. Y. (2008). Effect of resuscitation after selective cerebral ultraprofound hypothermia on expressions of nerve growth factor and glial cell line-derived neurotrophic factor in the brain of monkey. Neurosci. Bull. 24, 150-154.
28. Hypothermia after Cardiac Arrest Study Group. (2002). Mild therapeutic hypothermia to improve the neurologic outcome after cardiac arrest. N. Engl. J. Med. 346, 549-556.
29. Illievich, U. M., Zornow, M. H., Choi, K. T., Scheller, M. S., and Strnat, M. A. (1994). Effects of hypothermic metabolic suppression on hippocampal glutamate concentrations after transient global cerebral ischemia. Anesth. Analg. 78, 905-911.
30. Ji, X., Luo, Y., Ling, F., Stetler, R. A., Lan, J., Cao, G., and Chen, J. (2007). Mild hypothermia diminishes oxidative DNA damage and pro-death signaling events after cerebral ischemia: a mechanism for neuroprotection. Front. Biosci. 12, 1737-1747.
31. Jiang, J. Y., Liang, Y. M., Luo, Q. Z., and Zhu, C. (2004). Effect of mild hypothermia on brain dialysate lactate after fluid percussion brain injury in rodents. Neurosurgery 54, 713-717.
32. Johnson, J. W., and Ascher, P. (1987). Glycine potentiates the NMDA response in cultured mouse brain neurons. Nature 325, 529-531.
33. Jones, P. G., and Inouye, M. (1994). The cold-shock response: a hot topic. Mol. Microbiol. 11, 811-818.
34. Khar, A., Pardhasaradhi, B. V., Ali, A. M., and Kumari, A. L. (2003). Protection conferred by Bcl-2 expression involves reduced oxidative stress and increased glutathione production during hypothermia- induced apoptosis in AK-5 tumor cells. Free Radic. Biol. Med. 35, 949-957.
35. Kimura, A., Sakurada, S., Ohkuni, H., Todome, Y., and Kurata, K. (2002). Moderate hypothermia delays proinflammatory cytokine production of human peripheral blood mononuclear cells. Crit. Care Med. 30, 1499-1502.
36. Kimura, T., Sako, K., and Tanaka, K. (2002). Effect of mild hypothermia on energy state recovery following transient forebrain ischemia in the gerbil. Exp. Brain Res. 145, 83-90.
37. Kokaia, Z., Bengzon, J., Metsis, M., Kokaia, M., Persson, H., and Lindvall, O. (1993). Coexpression of neurotrophins and their receptors in neurons of the central nervous system. Proc. Natl. Acad. Sci. U.S.A. 90, 6711-6715.
38. Kuida, K. (2000). Caspase-9. Int. J. Biochem. Cell Biol. 32, 121-124.
39. Kvrivishvili, G. (2002). Glycine and neuroprotective effect of hypothermia in hypoxic-ischemic brain damage. Neuroreport 13, 1995-2000.
40. Lee, S. M., Zhao, H., Maier, C. M., and Steinberg, G. K. (2009). The protective effect of early hypothermia on PTEN phosphorylation correlates with free radical inhibition in rat stroke. J. Cereb. Blood Flow Metab. 29, 1589-1600.
41. Leker, R. R., and Shohami, E. (2002). Cerebral ischemia and trauma - different etiologies yet similar mechanisms: neuroprotective opportunities. Brain Res. Rev. 39, 55-73.
42. Liu, L., Kim, J. Y., Koike, M. A., Yoon, Y. J., Tang, X. N., Ma, H., Lee, H., Steinberg, G. K., Lee, J. E., and Yenari, M. A. (2008). FasL shedding is reduced by hypothermia in experimental stroke. J. Neurochem. 106, 541-550.
43. López-Hernández, F. J., Ortiz, M. A., and Piedrafita, F. J. (2006). The extrinsic and intrinsic apoptotic pathways are differentially affected by temperature upstream of mitochondrial damage. Apoptosis 11, 1339-1347.
44. Mattson, M. P., Culmsee, C., and Yu, Z. F. (2000). Apoptotic and antiapoptotic mechanisms in stroke. Cell Tissue Res. 301, 173-187.
45. McIntyre, L. A., Fergusson, D. A., and Hebert, P. C. (2003). Prolonged therapeutic hypothermia after traumatic brain injury in adults. JAMA 289, 2992-2999.
46. Merrill, J. E., and Benveniste, E. N. (1996). Cytokines in inflammatory brain lesions: helpful and harmful. Trends Neurosci. 19, 331-338.
47. Morganti-Kossmann, M. C., Lenzlinger, P. M., Hans, V., Stahel, P., Csuka, E., Ammann, E., Stocker, R., Trentz, O., and Kossmann, T. (1997). Production of cytokines following brain injury: beneficial and deleterious for the damaged tissue. Mol. Psychiatry 2, 133-136.
48. Muzio, M., Stockwell, B. R., Stennicke, H. R., Salvesen, G. S., and Dixit, V. M. (1998). An induced proximity model for caspase-8 activation. J. Biol. Chem. 273, 2926-2930.
49. Okuda, C., Saito, A., Miyazaki, M., and Kuriyama, K. (1986). Alterations of the turnover of dopamine and 5-hydroxytryptamine in rat brain associated with hypothermia. Pharmacol. Biochem. Behav. 25, 79-83.
50. Ooboshi, H., Ibayashi, S., Takano, K., Sadoshima, S., Kondo, A., Uchimura, H., and Fujishima, M. (2000). Hypothermia inhibits ischemia-induced efflux of amino acids and neuronal damage in the hippocampus of aged rats. Brain Res. 884, 23-30.
51. Pawton, T. (1995). Protein modules and signaling networks. Nature 373, 573-580.
52. Peters, O., Back, T., Lindauer, U., Busch, C., Megow, D., Dreier, J., and Dirnagl, U. (1998). Increased formation of reactive oxygen species after permanent and reversible middle cerebral artery occlusion in the rat. J. Cereb. Blood Flow Metab. 18, 196-205.
53. Raval, A. P., Dave, K. R., Prado, R., Katz, L. M., Busto, R., Sick, T. J., Ginsberg, M. D., Mochly-Rosen, D., and Pérez-Pinzón, M. A. (2005). Protein kinase C delta cleavage initiates an aberrant signal transduction pathway after cardiac arrest and oxygen glucose deprivation. J. Cereb Blood Flow Metab. 25, 730-741.
54. Reed, J. (1998). Bcl-2 family proteins. Oncogene 17, 3225-3236.
55. Rosomoff, H. L., and Holaday, D. A. (1954). Cerebral blood flow and cerebral oxygen consumption during hypothermia. Am. J. Physiol. 179, 85-88.
56. Rothman, S. M., and Olney, J. W. (1986). Glutamate and the pathophysiology of hypoxicic-ischemic brain damage. Ann. Neurol. 19, 105-111.
57. Rundgren, M., Karlsson, T., Nielsen, N., Cronberg, T., Johnsson, P., and Friberg, H. (2009). Neuron specific enolase and S-100B as predictors of outcome after cardiac arrest and induced hypothermia. Resuscitation 80, 784-789.
58. Russell, B. R., and Laverty, R. (2001). The effect of (R)-HA966 or ACEA 1021 on dexfenfluramine or (S)-MDMAinduced changes in temperature, activity, and neurotoxicity. Pharmacol. Biochem. Behav. 68, 565-574.
59. Sakurai, T., Itoh, K., Higashitsuji, H., Nonoguchi, K., Liu, Y., Watanabe, H., Nakano, T., Fukumoto, M., Chiba, T., and Fujita, J. (2006). CIRP protects against tumor necrosis factor-alphainduced apoptosis via activation of extracellular signal-regulated kinase. Biochim. Biophys. Acta 1763, 290-295.
60. Schabitz, W. R., Schwab, S., Spranger, M., and Hacke, W. (1997). Intraventricular brain-derived neurotrophic factor reduces infarct size after focal cerebral ischemia in rats. J. Cereb. Blood Flow Metab. 17, 500-506.
61. Schabitz, W. R., Sommer, C., Zoder, W., Kiessling, M., Schwaninger, M., and Schwab, S. (2000). Intravenous brainderived neurotrophic factor reduces infarct size and counterregulates Bax and Bcl-2 expression after temporary focal cerebral ischemia. Stroke 9, 2212-2217.
62. Schaeffer, H. J., and Weber, M. J. (1999). Mitogen-activated protein kinases: specific messages from ubiquitous messengers. Mol. Cell Biol. 19, 2435-2444.
63. Schmitt, K. R., Diestel, A., Lehnardt, S., Schwartlander, R., Lange, P. E., Berger, F., Ullrich, O., and Abdul-Khaliq, H. (2007). Hypothermia suppresses inflammation via ERK signaling pathway in stimulated microglial cells. J. Neuroimmunol. 189, 7-16.
64. Shi, L., Kraut, R. P., Aebersold, R., and Greenberg, A. H. (1992). A natural killer cell granule protein that induces DNA fragmentation and apoptosis. J. Exp. Med. 175, 553-566.
65. Shimohata, T., Zhao, H., and Steinberg, G. K. (2007a). Epsilon PKC may contribute to the protective effect of hypothermia in a rat focal cerebral ischemia model. Stroke 38, 375-380.
66. Shimohata, T., Zhao, H., Sung, J. H., Sun, G., Mochly-Rosen, D., and Steinberg, G. K. (2007b). Suppression of delta-PKC activation after focal cerebral ischemia contributes to the protective effect of hypothermia. J. Cereb. Blood Flow Metab. 27, 1463-1475.
67. Siesjo, B. K. (1988). Historical overview. Calcium, ischemia, and death of brain cells. Ann. N.Y. Acad. Sci. 522, 638-661.
68. Small, D. L., Morley, P., and Buchan, A. M. (1999). Biology of ischemic cerebral cell death. Prog. Cardiovasc. Dis. 42, 185-207.
69. Sopala, M., Schweizer, S., Schäfer, N., Nürnberg, E., Kreuter, J., Seiller, E., and Danysz, W. (2002). Neuroprotective activity of a nanoparticulate formulation of the glycineB site antagonist MRZ 2/576 in transient focal ischaemia in rats. Arzneimittelforschung 52, 168-174.
70. Stocchetti. N., Colombo, A., Ortolano, F., Videtta, W., Marchesi, R., Longhi, L., and Zanier, E. R. (2007). Time course of intracranial hypertension after traumatic brain injury. J. Neurotrauma 24, 1339-1346.
71. Stravitz, R. T., and Larsen, F. S. (2009). Therapeutic hypothermia for acute liver failure. Crit. Care Med. 37(Suppl. 7), S258-S264.
72. Susin, S. A., Lorenzo, H. K., Zamzami, N., Marzo, I., Snow, B. E., Brothers, G. M., Mangion, J., Jacotot, E., Costantini, P., Loeffler, M., Larochette, N., Goodlett, D. R., Aebersold, R., Siderovski, D. P., Penninger, J. M., and Kroemer, G. (1999). Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397, 441-446.
73. Taylor, C. W. (1987). Receptor regulation of calcium entry. Trends Pharmacol. Sci. 8, 79-80.
74. The Brain Trauma Foundation. (2007). The guidelines for the management of severe traumatic brain injury. J. Neurotrauma 24, S21-S25.
75. Van Harreveld, A. (1970). A mechanism for fluid shifts specific for the central nervous system. Bibl. Psychiatr. 143, 62-70.
76. Varon, J., and Acosta, P. (2008). Therapeutic hypothermia. Past, present, and future. Chest 133, 1267-1274.
77. Vespa, P. M., Nuwer, M. R., Nenov, V., Ronne-Engstrom, E., Hovda, D. A., Bergsneider, M., Kelly, D. F., Martin, N. A., and Becker, D. P. (1999). Increased incidence and impact of nonconvulsive and convulsive seizures after traumatic head injury as detected by continuous EEG in the intensive care unit. J. Neurosurg. 91, 750-760.
78. Vosler, P. S., Logue, E. S., Repine, M. J., and Callaway, C. W. (2005). Delayed hypothermia preferentially increases expression of brain-derived neurotrophic factor exon III in rat hippocampus after asphyxial cardiac arrest. Brain Res. Mol. Brain Res. 135, 21-29.
79. Xie, Y. C., Li, C. Y., Li, T., Nie, D. Y., and Ye, F. (2007). Effect of mild hypothermia on angiogenesis in rats with focal cerebral ischemia. Neurosci. Lett. 422, 87-90.
80. Xiong, M., Yang, Y., Chen, G. Q., and Zhou, W. H. (2009). Post-ischemic hypothermia for 24h in P7 rats rescues hippocampal neuron: association with decreased astrocyte activation and inflammatory cytokine expression. Brain Res. Bull. 79, 351-357.
81. Yang, D., Guo, S., Zhang, T., and Li, H. (2009). Hypothermia attenuates ischemia/reperfusion-induced endothelial cell apoptosis via alterations in apoptotic pathways and JNK signaling. FEBS Lett. 583, 2500-2506.
82. Yenari, M. A., and Hemmen, T. M. (2010). Therapeutic hypothermia for brain ischemia: where have we come and where do we go? Stroke 41(Suppl. 10), S72-S74.
83. Zhang, J., and Winoto, A. (1996). A mouse Fas-associated protein with homology to the human MORT1/FADD protein is essential for Fas-induced apoptosis. Mol. Cell Biol. 16, 2756-2763.
84. 2+ channels and their possible counter-parts in mammalian CNS neurons. Neuropharmacology 32, 1075-1088.
85. Zhao, H., Sapolsky, R. M., and Steinberg, G. K. (2006). Phosphoinositide-3-kinase/akt survival signal pathways are implicated in neuronal survival after stroke. Mol. Neurobiol. 34, 249-270.
86. Zhao, H., Shimohata, T., Wang, J. Q., Sun, G., Schaal, D. W., Sapolsky, R. M., and Steinberg, G. K. (2005). Akt contributes to neuroprotection by hypothermia against cerebral ischemia in rats. J. Neurosci. 25, 9794-9806.
87. Zhao, H., Wang, J. Q., Shimohata, T., Sun, G., Yenari, M. A., Sapolsky, R. M., and Steinberg, G. K. (2007). Conditions of protection by hypothermia and effects on apoptotic pathways in a rat model of permanent middle cerebral artery occlusion. J. Neurosurg. 107, 636-641.
88. Zhao, H., Yenari, M. A., Sapolsky, R. M., and Steinberg, G. K. (2004). Mild postischemic hypothermia prolongs the time window for gene therapy by inhibiting cytochrome C release. Stroke 35, 572-577