Hibernation: A natural model of tolerance to cerebral ischemia/reperfusion

Innate Tolerance in the CNS: Translational Neuroprotection by Pre- and Post-Conditioning

Volumn , Issue , 2013, Pages 37-50

  Drew, Kelly L ^a   Zuckerman, Jeffrey A ^b   Shenk, Phillip E ^b   Bogren, Lori K ^a   Jinka, Tulasi R ^a   Moore, Jeanette T ^a  

^a UNIVERSITY OF ALASKA FAIRBANKS   (United States)

^b Radiology Consultants   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84946847391     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-1-4419-9695-4_3     Document Type: Chapter

References (67)

1. Anderson TR, Jarvis CR, Biedermann AJ, Molnar C, Andrew RD (2005) Blocking the anoxic depolarization protects without functional compromise following simulated stroke in cortical brain slices. J Neurophysiol 93:963-979
2. Barros RC, Branco LG (2000) Role of central adenosine in the respiratory and thermoregulatory responses to hypoxia. Neuroreport 11:193-197
3. Bergeron M, Gidday JM, Yu AY, Semenza GL, Ferriero DM, Sharp FR (2000) Role of hypoxia- inducible factor-1 in hypoxia-induced ischemic tolerance in neonatal rat brain. Ann Neurol 48:285-296
4. Bidder PE, Fahlman CS (2004) Moderate increases in intracellular calcium activate neuroprotective signals in hippocampal neurons. Neuroscience 127:673-683
5. Blackstone E, Roth MB (2007) Suspended animation-like state protects mice from lethal hypoxia. Shock 27:370-372
6. Blackstone E, Morrison M, Roth MB (2005) H2S induces a suspended animation-like state in mice. Science 308:518
7. Bouma HR, Kroese FG, Kok JW, Talaei F, Boerema AS, Herwig A, Draghiciu O, van Buiten A, Epema AH, van Dam A et al (2011) Low body temperature governs the decline of circulating lymphocytes during hibernation through sphingosine-1-phosphate. Proc Natl Acad Sci USA 108:2052-2057
8. Bullard RW, David G, Nichols CT (eds) (1960) The mechanisms of hypoxic tolerance in hibernating and non-hibernating mammals. In: Mammalian hibernation. Museum of Comparative Zoology at Harvard College, Cambridge, MA
9. Busto R, Dietrich WD, Globus MY, Valdes I, Scheinberg P, Ginsberg MD (1987) Small differences in intraischemic brain temperature critically determine the extent of ischemic neuronal injury. J Cereb Blood Flow Metab 7:729-738
10. Carey HV, Andrews MT, Martin SL (2003) Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature. Physiol Rev 83:1153-1181
11. Chen Y, Cantrell AR, Messing RO, Scheuer T, Catterall WA (2005) Specific modulation of Na+ channels in hippocampal neurons by protein kinase C epsilon. J Neurosci 25:507-513
12. Christian SL, Ross AP, Zhao HW, Kristenson HJ, Zhan X, Rasley BT, Bidder PE, Drew KL (2008) Arctic ground squirrel (Spermophilus parryii) hippocampal neurons tolerate prolonged oxygen-glucose deprivation and maintain baseline ERK1/2 and JNK activation despite drastic ATP loss. J Cereb Blood Flow Metab 28:1307-1319
13. Contestabile A (2009) Benefits of caloric restriction on brain aging and related pathological states: understanding mechanisms to devise novel therapies. Curr Med Chem 16:350-361
14. D'Alecy LG, Lundy EF, Kluger MJ, Harker CT, LeMay DR, Shlafer M (1990) Beta-hydroxybutyrate and response to hypoxia in the ground squirrel, Spermophilus tridecimlineatus. Comp Biochem Physiol B 96:189-193
15. Dausmann KH, Glos J, Ganzhorn JU, Heldmaier G (2004) Physiology: hibernation in a tropical primate. Nature 429:825-826
16. Dave KR, Prado R, Raval AP, Drew KL, Perez-Pinzon MA (2006) The Arctic ground squirrel brain is resistant to injury from cardiac arrest during euthermia. Stroke 37(5):1261-1265
17. Dave KR, Anthony Defazio R, Raval AP, Dashkin O, Saul I, Iceman KE, Perez-Pinzon MA, Drew KL (2009) Protein kinase C epsilon activation delays neuronal depolarization during cardiac arrest in the euthermic arctic ground squirrel. J Neurochem 110:1170-1179
18. Derwall M, Westerkamp M, Lower C, Deike-Glindemann J, Schnorrenberger NK, Coburn M, Nolte KW, Gaisa N, Weis J, Siepmann K et al (2010) Hydrogen sulfide does not increase resus- citability in a porcine model of prolonged cardiac arrest. Shock 34:190-195
19. Drew KL, Rice ME, Kuhn TB, Smith MA (2001) Neuroprotective adaptations in hibernation: therapeutic implications for ischemia-reperfusion, traumatic brain injury and neurodegenerative diseases. Free Radic Biol Med 31:563-573
20. Drew KL, Christian SL, Jinka TR, Hollen L, Dehn J (2009) "Natural" tolerance in hibernators: can we learn from physiological and preconditioning against ischemic or hypoxic brain injury? In: Schaller BJ (ed) Ischemic tolerance of the brain. Research Signpost, Trivandrum, pp 1-44
21. Dunwiddie TV, Masino SA (2001) The role and regulation of adenosine in the central nervous system. Annu Rev Neurosci 24:31-55
22. Elrod JW, Calvert JW, Morrison J, Doeller JE, Kraus DW, Tao L, Jiao X, Scalia R, Kiss L, Szabo C et al (2007) Hydrogen sulfide attenuates myocardial ischemia-reperfusion injury by preservation of mitochondrial function. Proc Natl Acad Sci USA 104:15560-15565
23. Frerichs KU, Hallenbeck JM (1998) Hibernation in ground squirrels (AGS) induces state and species-specific tolerance to hypoxia and aglycemia: an in vitro study in hippocampal slices. J Cereb Blood Flow Metab 18:168-175
24. Frerichs KU, Kennedy C, Sokoloff L, Hallenbeck JM (1994) Local cerebral blood flow during hibernation, a model of natural tolerance to "cerebral ischemia". J Cereb Blood Flow Metab 14:193-205
25. Geiser F, Ruf T (1995) Hibernation versus daily torpor in mammals and birds: physiological variables and classification of torpor patterns. Physiol Zool 68:935-966
26. Hochachka PW (1986) Defense strategies against hypoxia and hypothermia. Science 231:234-241
27. Hoffman RA, Robinson PF, Magalhaes H (eds) (1968) The Golden Hamster; its biology and use in medical research. The Iowa State University Press, Ames
28. Jackson DC (2004) Acid-base balance during hypoxic hypometabolism: selected vertebrate strategies. Respir Physiol Neurobiol 141:273-283
29. Jinka TR, Carlson ZA, Moore JT, Drew KL (2010) Altered thermoregulation via sensitization of A1 adenosine receptors in dietary restricted rats. Psychopharmacology (Berl) 209(3):217-224
30. 1 receptors. J Neurosci 31(30):10752-10758
31. Kirschner DL, Wilson AL, Drew KL, Green TK (2009) Simultaneous efflux of endogenous D-ser and L-glu from single acute hippocampus slices during oxygen glucose deprivation. J Neurosci Res 87:2812-2820
32. Kurtz CC, Lindell SL, Mangino MJ, Carey HV (2006) Hibernation confers resistance to intestinal ischemia-reperfusion injury. Am J Physiol Gastrointest Liver Physiol 291:G895-G901
33. Lechler E, Penick GD (1963) Blood clotting defect in hibernating ground squirrels (AGS) (Citellus tridecemlineatus). Am J Physiol 205:985-988
34. Lee M, Choi I, Park K (2002) Activation of stress signaling molecules in bat brain during arousal from hibernation. J Neurochem 82:867-873
35. Lee YJ, Miyake S, Wakita H, McMullen DC, Azuma Y, Auh S, Hallenbeck JM (2007) Protein SUMOylation is massively increased in hibernation torpor and is critical for the cytoprotection provided by ischemic preconditioning and hypothermia in SHSY5Y cells. J Cereb Blood Flow Metab 27:950-962
36. Lindell SL, Klahn SL, Piazza TM, Mangino MJ, Torrealba JR, Southard JH, Carey HV (2005) Natural resistance to liver cold ischemia-reperfusion injury associated with the hibernation phenotype. Am J Physiol Gastrointest Liver Physiol 288:G473-G480
37. Lipton P (1999) Ischemic cell death in brain neurons. Physiol Rev 79:1431-1568
38. Lutz PL, Milton SL (2004) Negotiating brain anoxia survival in the turtle. J Exp Biol 207:3141-3147
39. Ma YL, Zhu X, Rivera PM, Toien O, Barnes BM, LaManna JC, Smith MA, Drew KL (2005) Absence of cellular stress in brain after hypoxia induced by arousal from hibernation in Arctic ground squirrels (AGS). Am J Physiol Regul Integr Comp Physiol 289:R1297-R1306
40. Nowak G, Bakajsova D, Clifton GL (2004) Protein kinase C-epsilon modulates mitochondrial function and active Na+ transport after oxidant injury in renal cells. Am J Physiol Renal Physiol 286:F307-F316
41. Orr AL, Lohse LA, Drew KL, Hermes-Lima M (2009) Physiological oxidative stress after arousal from hibernation in Arctic ground squirrel. Comp Biochem Physiol A Mol Integr Physiol 153:213-221
42. Osborne PG, Hashimoto M (2005) Brain antioxidant levels in hamsters during hibernation, arousal and cenothermia. Behav Brain Res 175(3):147-55
43. Osborne PG, Sato J, Shuke N, Hashimoto M (2005) Sympathetic alpha-adrenergic regulation of blood flow and volume in hamsters arousing from hibernation. Am J Physiol Regul Integr Comp Physiol 289:R554-R562
44. Pivorun EB, Sinnamon WB (1981) Blood coagulation studies in normothermic, hibernating, and aroused Spermophilus franklini. Cryobiology 18:515-520
45. Prendergast BJ, Freeman DA, Zucker I, Nelson RJ (2002) Periodic arousal from hibernation is necessary for initiation of immune responses in ground squirrels (AGS). Am J Physiol Regul Integr Comp Physiol 282:R1054-R1062
46. Ross AP, Christian SL, Zhao HW, Drew KL (2006) Persistent tolerance to oxygen and nutrient deprivation and N-methyl-D-aspartate in cultured hippocampal slices from hibernating Arctic ground squirrel. J Cereb Blood Flow Metab 26:1148-1156
47. Savitz SI, Fisher M (2007a) Future of neuroprotection for acute stroke: in the aftermath of the SAINT trials. Ann Neurol 61:396-402
48. Savitz SI, Fisher M (2007b) Prophylactic neuroprotection. Curr Drug Targets 8:846-849
49. Sawe N, Steinberg G, Zhao H (2008) Dual roles of the MAPK/ERK1/2 cell signaling pathway after stroke. J Neurosci Res 86:1659-1669
50. Shiomi H, Tamura Y (2000) Pharmacological aspects of mammalian hibernation: central thermoregulation factors in hibernation cycle. Nippon Yakurigaku Zasshi (Folia Pharmacol Jpn) 116:304-312
51. Snider BJ, Tee LY, Canzoniere LM, Babcock DJ, Choi DW (2002) NMDA antagonists exacerbate neuronal death caused by proteasome inhibition in cultured cortical and striatal neurons. Eur J Neurosci 15:419-428
52. Steiner AA, Branco LG (2002) Hypoxia-induced anapyrexia: implications and putative mediators. Annu Rev Physiol 64:263-288
53. Stenzel-Poore MP, Stevens SL, Xiong Z, Lessov NS, Harrington CA, Mori M, Meller R, Rosenzweig HL, Tobar E, Shaw TE et al (2003) Effect of ischaemic preconditioning on genomic response to cerebral ischaemia: similarity to neuroprotective strategies in hibernation and hypoxia-tolerant states. Lancet 362:1028-1037
54. Stowe AM, Altay T, Freie AB, Gidday JM (2011) Repetitive hypoxia extends endogenous neurovascular protection for stroke. Ann Neurol 69:975-985
55. Swoap S, Lliff B (2011) AMP vs. Adenosine as a mediator of fasting-induced torpor. Paper presented at: metabolic responses to extreme conditions (Big Sky, Montana, Keystone Symposia on Molecular and Cellular Biology)
56. Swoap SJ, Rathvon M, Gutilla M (2007) AMP does not induce torpor. Am J Physiol Regul Integr Comp Physiol 293:R468-R473
57. Tahti H, Soivio A (1975) Blood gas concentrations, acid-base balance and blood pressure in hedgehogs in the active state and in hibernation with periodic respiration. Ann Zool Fennici 12:188-192
58. Takeda Y, Namba K, Higuchi T, Hagioka S, Takata K, Hirakawa M, Morita K (2003) Quantitative evaluation of the neuroprotective effects of hypothermia ranging from 34 degrees C to 31 degrees C on brain ischemia in gerbils and determination of the mechanism of neuroprotection. Crit Care Med 31:255-260
59. Tattersall GJ, Milsom WK (2003) Transient peripheral warming accompanies the hypoxic metabolic response in the golden-mantled ground squirrel. J Exp Biol 206:33-42
60. Toien O, Drew KL, Chao ML, Rice ME (2001) Ascorbate dynamics and oxygen consumption during arousal from hibernation in Arctic ground squirrels (AGS). Am J Physiol Regul Integr Comp Physiol 281:R572-R583
61. Toien O, Blake J, Edgar DM, Grahn DA, Heller HC, Barnes BM (2011) Hibernation in black bears: independence of metabolic suppression from body temperature. Science 331:906-909
62. Toombs CF, Insko MA, Wintner EA, Deckwerth TL, Usansky H, Jamil K, Goldstein B, Cooreman M, Szabo C (2010) Detection of exhaled hydrogen sulphide gas in healthy human volunteers during intravenous administration of sodium sulphide. Br J Clin Pharmacol 69:626-636
63. Ungvari Z, Parrado-Fernandez C, Csiszar A, de Cabo R (2008) Mechanisms underlying caloric restriction and lifespan regulation: implications for vascular aging. Circ Res 102:519-528
64. Zhang J, Kaasik K, Blackburn MR, Lee CC (2006) Constant darkness is a circadian metabolic signal in mammals. Nature 439:340-343
65. Zhao HW, Ross AP, Christian SL, Buchholz JN, Drew KL (2006) Decreased NR1 phosphorylation and decreased NMDAR function in hibernating Arctic ground squirrels (AGS). J Neurosci Res 84:291-298
66. Zhou F, Zhu X, Castellani RJ, Stimmelmayr R, Perry G, Smith MA, Drew KL (2001) Hibernation, a model of neuroprotection. Am J Pathol 158:2145-2151
67. Zhu PJ, Krnjevic K (1997) Adenosine release mediates cyanide-induced suppression of CA1 neuronal activity. J Neurosci 17:2355-2364