Modulation of stress proteins and apoptotic regulators in the anoxia tolerant turtle brain

Journal of Neurochemistry

Volumn 109, Issue 5, 2009, Pages 1413-1426

  Kesaraju, Shailaja ^a   Schmidt Kastner, Rainald ^b   Prentice, Howard M ^b   Milton, Sarah L ^a  

^a FLORIDA ATLANTIC UNIVERSITY   (United States)

^b FLORIDA ATLANTIC UNIVERSITY   (United States)

Author keywords

Anoxia; Apoptosis; Heat shock proteins; Neurons; Reoxygenation; Trachemys scripta; Turtle

Indexed keywords

APOPTOSIS REGULATORY PROTEIN; CASPASE 3; GLUCOSE REGULATED PROTEIN 78; GLUCOSE REGULATED PROTEIN 94; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 27; HEAT SHOCK PROTEIN 60; HEAT SHOCK PROTEIN 72; HEME OXYGENASE 1; PROTEIN BAX; PROTEIN BCL 2;

ANIMAL TISSUE; ANOXIA; APOPTOSIS; ARTICLE; CELL DAMAGE; CONTROLLED STUDY; DNA FRAGMENTATION; GLIA CELL; IMMUNOHISTOCHEMISTRY; NONHUMAN; PRIORITY JOURNAL; REOXYGENATION;

ANIMALS; ANOXIA; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BRAIN; GENE EXPRESSION REGULATION; HEAT-SHOCK PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; TIME FACTORS; TURTLES;

TESTUDINES; TRACHEMYS SCRIPTA;

EID: 65549125913     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2009.06068.x     Document Type: Article

References (98)

1. Abe H. Nowak Jr. T. S. (2004) Induced hippocampal neuron protection in an optimized gerbil ischemia model: insult thresholds for tolerance induction and altered gene expression defined by ischemic depolarization. J. Cereb. Blood Flow Metab. 24, 84 97. (Pubitemid 38021272)
2. Ashraf Q. M., Zanelli S. A., Mishra O. P. Delivoria-Papadopoulos M. (2001) Phosphorylation of Bcl2 and Bax proteins during hypoxia in newborn piglets. Neurochem. Res. 26, 1 9. (Pubitemid 32428806)
3. Badin R. A., Lythgoe M. F., Van der Weerd L., Thomas D. L., Gadian D. G. Latchman D. S. (2006) Neuroprotective effects of virally delivered HSPs in experimental stroke. J. Cereb. Blood Flow Metab. 26, 371 381. (Pubitemid 43297918)
4. Bando Y., Katayama T., Kasai K., Taniguchi M., Tamatani M. Tohyama M. (2003) GRP94(94 kDa glucose-regulated protein) suppresses ischemic neuronal cell death against ischemia/reperfusion injury. Eur. J. Neurosci. 18, 829 840. (Pubitemid 37059693)
5. Bechtold D. A. Brown I. R. (2000) Heat shock proteins Hsp27 and Hsp32 localize to synaptic sites in the rat cerebellum following hyperthermia. Brain Res. Mol. Brain Res. 75, 309 320. (Pubitemid 30109283)
6. Bickler P. E., Donohoe P. H. Buck L. T. (2000) Hypoxia-induced silencing of NMDA receptors in turtle neurons. J. Neurosci. 20, 3522 3528. (Pubitemid 30266213)
7. Bruey J. M., Duchase C., Bonniaud P. et al. (2000) Hsp27 negatively regulates cell death by interacting with cytochrome c. Nat. Cell Biol. 2, 645 652.
8. Cameron J. N. (1989) The Respiratory Physiology of Animals. Oxford University Press, New York, Oxford.
9. Cao G., Pei W., Lan J., Stetler R. A., Luo Y., Nagayama T., Graham S. H., Yin X. M., Simon R. P. Chen J. (2001) Caspase -activated DNase DNA fragmentation factor 40 mediates apoptotic DNA fragmentation in transient cerebral ischemia and in neuronal cultures. J. Neurosci. 21, 4678 4690. (Pubitemid 32565626)
10. Cao G., Luo Y., Nagayama T., Pei W., Stetler R. A., Graham S. H. Chen J. (2002) Cloning and characterization of rat caspase-9: implications for a role in mediating caspase-3 activation and hippocampal cell death after transient cerebral ischemia. J. Cereb. Blood Flow Metab. 22, 534 546. (Pubitemid 34477775)
11. Cao G., Clark R. S., Pei W., Yin W., Zhang F., Sun F. Y., Graham S. H. Chen J. (2003) Translocation of apoptosis-inducing factor in vulnerable neurons after transient ischemia and in neuronal cultures after oxygen-glucose deprivation. J. Cereb. Blood Flow Metab. 23, 1137 1150. (Pubitemid 37229517)
12. Chandra D., Choy G. Tang D. G. (2007) Cytosolic accumulation of HSP60 during apoptosis with or without apparent mitochondrial release: evidence that its pro-apoptotic or pro-survival functions involve differential interactions with caspase-3. J. Biol. Chem. 282, 31289 31301. (Pubitemid 350044883)
13. Chang J., Knowlton A. A. Wasser J. S. (2000) Expression of heat shock proteins in turtle and mammal hearts: relationship to anoxia tolerance. Am. J. Physiol. Regul. Integr. Comp. Physiol. 278, R209 R214. (Pubitemid 30182691)
14. Chen J., Graham S. H., Zhu R. L. Simon R. P. (1996) Stress proteins and tolerance to focal cerebral ischemia. J. Cereb. Blood Flow Metab. 16, 566 577. (Pubitemid 26227065)
15. Chen K., Gunter K. Maines M. D. (2000) Neurons overexpressing heme-oxygenase-1 resist oxidative stress-meditated cell death. J. Neurochem. 75, 304 313. (Pubitemid 30418197)
16. Clemons N. J., Buzzard K., Steel R. Anderson R. L. (2005) Hsp72 inhibits Fas-mediated apoptosis upstream of the mitochondria in type II cells. J. Biol. Chem. 280, 9005 9012. (Pubitemid 40409592)
17. Conconnaon C. G., Orrenius S. Samali A. (2001) Hsp27 inhibits cytochrome c-mediated caspase activation by sequestering both pro-caspase-3 and cytochrome c. Gene Expr. 9, 195 201. (Pubitemid 32606842)
18. Cregan S. P., Fontin A., MacLaurin J. G. et al. (2002) Apoptosis-inducing factor is involved in the regulation of caspase-independent neuronal cell death. J. Cell Biol. 158, 507 517.
19. Cserr H. F., DePasquale M. Jackson D. C. (1988) Brain and cerebrospinal fluid ion composition after long-term anoxia in diving turtles. Am. J. Physiol. 255, R338 R343. (Pubitemid 18215102)
20. Currie R. W., Ellison J. A., White R. F., Feuerstein G. Z., Wang X. Barone F. C. (2000) Benign focal ischemic preconditioning induces neuronal Hsp70 and prolonged astrogliosis with expression of Hsp27. Brain Res. 863, 169 181. (Pubitemid 30201596)
21. Feldenberg L. R., Thevananther S., del Rio M., de Leon M. Devarajan P. (1999) Partial ATP depletion induces Fas- and caspase-mediated apoptosis in MDCK cells. Am. J. Physiol. Renal Physiol. 276, F837 F846. (Pubitemid 29323557)
22. Fernandes J. A., Lutz P. L., Tannenbaum A., Todorov A. T., Liebovitch L. Vertes R. (1997) Electroencephalogram activity in the anoxic turtle brain. Am. J. Physiol. 273, R911 R919. (Pubitemid 27425638)
23. Fraser K. P., Houlihan D. F., Lutz P. L., Leone-Kabler S., Manuel L. Brechin J. G. (2001) Complete suppression of protein synthesis during anoxia with no post-anoxia protein synthesis debt in the red-eared slider turtle Trachemys scripta elegans. J. Exp. Biol. 204, 4353 4360.
24. Gabai V. L., Meriin A. B., Yaglom J. A., Wei J. Y., Mosser D. D. Sherman M. Y. (2000) Suppression of stress kinase JNK is involved in HSP72-medited protection of myogenic cells from transient energy deprivation HSP72 alleviates the stress-induced inhibition of JNK dephosphorylation. J. Biol. Chem. 275, 38088 38094. (Pubitemid 32004933)
25. Gabai V. L., Mabuchi K., Mosser D. D. Sherman M. Y. (2002) Hsp72 and stress kinase c-jun N-terminal kinase regulate the bid-dependent pathway in tumor necrosis factor induced apoptosis. Mol. Cell. Biol. 22, 3415 3424. (Pubitemid 34453981)
26. Garrido C., Bruey J. M., Fromentin A., Hammann A., Arrigo A. P. Solary E. (1999) HSP27 inhibits cytochrome c- dependent activation of procaspase-9. FASEB J. 14, 2061 2070. (Pubitemid 29517636)
27. Garrido C., Gurbuxiani S., Ravagnan L. Kroemer G. (2001) Heat shock proteins: endogenous modulators of apoptotic cell death. Biochem. Biophys. Res. Commun. 286, 433 442. (Pubitemid 32912965)
28. Geddes J. W., Pettigrew L. C., Holtz M. L., Craddock S. D. Maines M. D. (1996) Permanent focal and transient global cerebral ischemia increase glial and neuronal expression of heme oxygenase-1, but not heme oxygenase-2, protein in rat brain. Neurosci. Lett. 210, 205 208. (Pubitemid 26184522)
29. Gross A., Jockel J., Wei M. C. Korsmeyer S. J. (1998) Enforced dimerization of BAX results in its translocation, mitochondrial dysfunction and apoptosis. EMBO J. 17, 3878 3885. (Pubitemid 28333974)
30. Haddad J. J. (2007a) Discordant tissue specific expression of SAPK/MAPK(JNK)-related cofactors in hypoxia and hypoxia/reoxygenation in a model of anoxia-tolerance. Protein Pept. Lett. 14, 373 380. (Pubitemid 46570909)
31. Haddad J. J. (2007b) The role of Bax/Bcl2 and procaspase peptides in hypoxia/reperfusion-dependent regulation of MAPK (ERK): discordant proteomic effect. Protein Pept. Lett. 14, 361 371. (Pubitemid 46570908)
32. Halaby I. A., Takeda Y., Yufu K., Nowak Jr. T. S. Pulsinelli W. A. (2004) Depolarization thresholds for hippocampal damage, ischemic preconditioning, and changes in gene expression after global ischemia in the rat. Neurosci. Lett. 372, 12 16. (Pubitemid 39505219)
33. Havasi A., Li Z., Wang Z., Martin J. L., Botla V., Ruchalski K., Schwartz J. H. Borkan S. C. (2008) Hsp27 inhibits Bax activation and apoptosis via a phosphatidylinositol 3-kinase depenedant mechanism. J. Biol. Chem. 283, 12305 12313.
34. Hayashi T., Saito A., Okuno S., Ferrand-Drake M. Chan P. H. (2003) Induction of GRP78 by ischemic preconditioning reduces endoplasmic reticulum stres and prevents delayed neuronal cell death. J. Cereb. Blood Flow Metab. 8, 849 961. (Pubitemid 36959401)
35. Higashi T., Takechi H., Uemura Y., Kikuchi H. Nagata K. (1994) Differential induction of mRNA species encoding several classes of stress proteins following focal cerebral ischemia in rats. Brain Res. 650, 239 248. (Pubitemid 24207068)
36. Hwang I. K., Ahn H. C., Yoo K. Y., Lee J. Y., Suh H. W., Kwon Y. G., Cho J. H. Won M. H. (2007) Changes in immunoreactivity of HSP60 and its neuroprotective effects in the gerbil hippocampal CA1 region induced by transient ischemia. Exp. Neurol. 208, 247 256. (Pubitemid 350101502)
37. Jeon G. S., Park S. W., Kim D. W., Seo J. H., Cho J., Lim S. Y., Kim S. D. Cho S. S. (2004) Glial expression of the 90 kDA heat shock protein (HSP90) and the 94 kDA glucose regulated protein (GRP94) following an excitotoxic lesion in the mouse hippocampus. Glia 48, 250 258. (Pubitemid 39545939)
38. Kalman M., Kiss A. Majorossy K. (1994) Distribution of glial fibrillary acidic protein - immunopositive structures in the brain of the red-eared freshwater turtle (Pseudemys scripta elegans). Anat. Embryol. (Berl). 189, 421 434. (Pubitemid 24163631)
39. Kato H., Liu Y., Kogure K. Kato K. (1994) Induction of 27-kDa heat shock protein following cerebral ischemia in a rat model of ischemic tolerance. Brain Res. 634, 235 244. (Pubitemid 24025053)
40. Kato H., Kogure K., Liu X. H., Araki T., Kato K. Itoyama Y. (1995) Immunohistochemical localization of the low molecular weight stress protein HSP27 following focal cerebral ischemia in the rat. Brain Res. 679, 1 7.
41. Kim S. W., Park S., You K. H. Kwon O.-Y. (2003) Expression of the endoplasmic reticulum chaperone GRP94 gene in ischemic gerbil brain. Z. Naturforsch[C]. 58, 736 739. (Pubitemid 37224271)
42. Kim J. W., Li M. H., Jang J. H., Na H. K., Song N. Y., Lee C., Johnson J. A. Surh Y. J. (2008) 15-Deoxy-Delta(12,14)-prostaglandin J(2) rescues PC12 cells from H(2)O(2)-induced apoptosis through Nrf2-mediated upregulation of heme oxygenase-1: potential roles of Akt and ERK1/2. Biochem. Pharmacol. 76, 1577 1589.
43. Kirchoff S. R., Gupta S. Knowlton A. A. (2002) Cytosolic heat shock protein 60, apoptosis, and myocardial injury. Circulation 105, 2899 2904. (Pubitemid 34666105)
44. Kirino T. (2002) Ischemic tolerance. J. Cereb. Blood Flow Metab. 22, 1283 1296. (Pubitemid 35285085)
45. Kokubo Y., Liu J., Rajdev S., Kayama T., Sharp F. R. Weinstein P. R. (2003) Differential cerebral protein synthesis and heat shock protein 70 expression in the core and penumbra of rat brain after transient focal ischemia. Neurosurgery 53, 186 190. (Pubitemid 36801522)
46. Kudo T., Kanemoto S., Hara H., Morimoto N., Morihara T., Kimura R., Tabita T., Imaizumi K. Takeda M. (2008) A molecular chaperone inducer protects neurons from ER stress. Cell Death Differ. 15, 364 375.
47. Lanneau D., Brunet M., Frisan E., Solary E., Fontenary M. Garrido C. (2008) Heat shock proteins: essential proteins for apoptosis regulation. J. Cell Mol. Med. 12, 743 761. (Pubitemid 350159887)
48. Li C., Lee J., Ko Y., Kim J. Seo J. (2000) Heat shock protein 70 inhibits apoptosis downstream of cytochrome c release and upstream of caspase 3 activation. J. Biol. Chem. 275, 25665 25671. (Pubitemid 30662037)
49. Li F., Mao H. P., Ruchalski K. L., Wang Y. H., Choy W., Schwartz J. H. Borkan S. C. (2002) Heat stress prevents mitochondrial injury in ATP-depleted renal epithelial cells. Am. J. Physiol. Cell Physiol. 283, C917 C926.
50. Lutz P. L. Milton S. L. (2004) Negotiating brain anoxia survival in the turtle. J. Exp. Biol. 207, 3141 3147. (Pubitemid 39275288)
51. Lutz P. L., McMohan P., Rosenthal M. Sick T. J. (1984) Relationships between aerobic and anaerobic energy production in turtle brain in situ. Am. J. Physiol. 247, R740 R744. (Pubitemid 15200531)
52. Massa S. M., Swanson R. A. Sharp F. R. (1996) The stress gene response in brain. Cerebrovasc. Brain Metab. Rev. 8, 95 158. (Pubitemid 126840013)
53. Matsumori Y., Northington F. J., Hong S. M., Kayama T., Sheldon R. A., Vexler Z. S., Ferriero D. M., Weinstein P. R. Liu J. (2006) Reduction of caspase-8 and -9 cleavage is associated with increased c-FLIP and increased binding of Apaf-1 and Hsp70 after neonatal hypoxic/ischemic injury in mice overexpressing Hsp70. Stroke 37, 507 512. (Pubitemid 43732015)
54. Meeks J. P. Mennerick S. (2003) Feeding hungry neurons: astrocytes deliver food for thought. Neuron 37, 187 189. (Pubitemid 36143812)
55. Mehta S. L., Manhas N. Raghubir R. (2007) Molecular targets in cerebral ischemia for developing novel therapeutics. Brain Res. Rev. 54, 34 66. (Pubitemid 46498164)
56. Milton S. L. Prentice H. M. (2007) Beyond anoxia: the physiology of metabolic downregulation and recovery in the anoxia-tolerant turtle. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 147, 277 290. (Pubitemid 46617986)
57. Milton S. L., Thompson J. W. Lutz P. L. (2002) Mechanisms for maintaining extracellular glutamate levels in the anoxic turtle striatum. Am. J. Physiol. Regul. Integr. Comp. Physiol. 282, R1317 R1323. (Pubitemid 34664515)
58. Milton S. L., Nayak G., Kesaraju S., Kara L. Prentice H. M. (2007) Suppression of reactive oxygen species production enhances neuronal survival in vitro and in vivo in the anoxia-tolerant turtle Trachemys scripta. J. Neurochem. 101, 993 1001. (Pubitemid 46683873)
59. Milton S. L., Dirk L. J., Kara L. F. Prentice H. M. (2008) Adenosine modulates ERK1/2, PI3K/Akt, and p38MAPK activation in the brain of the anoxia-tolerant turtle Trachemys scripta. J. Cereb. Blood Flow Metab. 28, 1469 1477.
60. Mullen R. J., Buck C. R. Smith A. M. (1992) NeuN, a neuronal specific nuclear protein in vertebrates. Development 116, 201 211. (Pubitemid 23020281)
61. Nilsson G. E. Lutz P. L. (1992) Adenosine release in the turtle brain; a possible mechanism for anoxic survival. J. Exp. Biol. 162, 345 351.
62. Nishi S., Taki W., Uemura Y., Higashi T., Kikuchi H., Kudoh H., Satoh M. Nagata K. (1993) Ischemic tolerance due to the induction of HSP70 in a rat ischemic circulation model. Brain Res. 615, 281 288. (Pubitemid 23189648)
63. Nishino K. Nowak Jr. T. S. (2004) Time course and cellular distribution of hsp27 and hsp72 stress protein expression in a quantitative gerbil model of ischemic injury and tolerance: thresholds for hsp72 induction and hilar lesioning in the context of ischemic preconditioning. J. Cereb. Blood Flow Metab. 24, 167 178. (Pubitemid 38199110)
64. Obrenovitch T. P. (2008) Molecular physiology of preconditioning-induced brain tolerance to ischemia. Physiol. Rev. 88, 211 247.
65. Pamenter M. E., Richards M. D. Buck L. T. (2007) Anoxia induced changes in reactive oxygen species and cyclic nucleotides in the painted turtle. J. Comp. Physiol. 177, 473 481. (Pubitemid 46625363)
66. Panahian N., Yoshiura M. Maines M. D. (1999) Overexpression of heme oxygenase 1 in a model of permanent middle cerebral artery occlusion in transgenic mice. J. Neurochem. 72, 1187 1203. (Pubitemid 29085035)
67. Pellerin L. Magistretti P. J. (1994) Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. Proc. Natl Acad. Sci. USA 91, 10625 10629. (Pubitemid 24329051)
68. Perez Pinzon M. A., Rosenthal M., Sick T. J., Lutz P. L., Pablo J. Mash D. (1992) Downregulation of sodium channels during anoxia: a putative survival strategy of turle brain. Am. J. Physiol. 262, R712 R715.
69. Plesnila N., Zhu C., Culmsee C., Groger M., Moskowitz M. A. Blomgren K. (2004) Nuclear translocation of apoptosis-inducing factor after focal cerebral ischemia. J. Cereb. Blood Flow Metab. 24, 458 466. (Pubitemid 38452237)
70. Powers A. S. Reiner A. (1993) The distribution of cholinergic neurons in the central nervous system of turtles. Brain Behav. Evol. 41, 326 345.
71. Prentice H. M., Milton S. L., Scheurle D. Lutz P. L. (2003) Gene transcription of brain voltage-gated potassium channels is reversibly regulated by oxygen supply. Am. J. Physiol. Regul. Integr. Comp. Physiol. 285, R1317 R1321. (Pubitemid 37464390)
72. Prentice H. M., Milton S. L., Scheurle D. Lutz P. L. (2004) The upregulation of cognate and inducible heat shock proteins in the anoxic turtle brain. J. Cereb. Blood Flow Metab. 24, 826 828. (Pubitemid 38880228)
73. Ramaglia V. Buck L. T. (2004) Time-dependent expression of heat shock proteins 70 and 90 in tissues of the anoxic western painted turtle. J. Exp. Biol. 207, 3775 3784. (Pubitemid 39484195)
74. Rice M. E., Lee E. J. Choy Y. (1995) High levels of ascorbic acid, not glutathione, in the CNS of anoxia-tolerant reptiles contrasted with levels in anoxia-intolerant species. J. Neurochem. 64, 1790 1799.
75. Ruchalski K., Mao H., Li Z., Wang Z., Gillers S., Wang Y., Mosser D. D., Gabai V., Schwartz J. H. Borkan S. C. (2006) Distinct Hsp70 domains mediate apoptosis-inducing factor release and nuclear accumulation. J. Biol. Chem. 281, 7873 7880. (Pubitemid 43847403)
76. Saito A., Tominaga T. Chan P. H. (2005) Neuroprotective role of neurotrophins: relationship between nerve growth factor and apoptotic cell survival pathway after cerebral ischemia. Curr. Atheroscler. Rep. 7, 268 273. (Pubitemid 41630818)
77. Schmidt-Kastner R., Heim C. Sontag K. H. (1991) Damage of substantia nigra pars reticulata during pilocarpine-induced status epilepticus in the rat: immunohistochemical study of neurons, astrocytes and serum-protein extravasation. Exp. Brain Res. 86, 125 140.
78. Schmidt-Kastner R., Aguirre-Chen C., Saul I., Yick L., Hamasaki D., Busto R. Ginsberg M. D. (2005) Astrocytes react to oligemia in the forebrain induced by chronic bilateral common carotid artery occlusion in rats. Brain Res. 1052, 28 39. (Pubitemid 41116285)
79. Schroeder M. Kaufman R. J. (2005) The mammalian unfolded protein response. Ann. Rev. Biochem. 74, 739 789. (Pubitemid 40995523)
80. Stankiewicz A. R., Lachapelle G., Foo C. P., Radicioni S. M. Mosser D. D. (2005) Hsp70 inhibits heat-induced apoptosis upstream of mitochondria by preventing Bax translocation. J. Biol. Chem. 280, 38729 38739. (Pubitemid 43853776)
81. Storey K. B. (2006) Reptile freeze tolerance: metabolism and gene expression. Cryobiology 52, 1 16. (Pubitemid 43202189)
82. Storey K. B. (2007) Anoxia tolerance in turtles: metabolic regulation and gene expression. Comp. Biochem. Physiol. A. Mol. Integr. Physiol. 147, 263 276. (Pubitemid 46617988)
83. Susin S. A., Lorenzo H. K., ZamZami N. et al. (1999) Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397 (6718 441 446. (Pubitemid 29078912)
84. Sykova E., Mazel T. Simonova Z. (1998) Diffusion constraints and neuron-glia interaction during aging. Exp. Gerontol. 33, 837 851. (Pubitemid 29019338)
85. Tanaka H., Yokoto H., Jover T., Cappuccio I., Calderone A., Simionescu M., Bennett M. V. Zukin R. S. (2004) Ischemic preconditioning: neuronal survival in the face of caspase-3 activation. J. Neurosci. 17, 2750 2759. (Pubitemid 38380952)
86. Thompson J. W., Prentice H. M. Lutz P. L. (2007) Regulation of extracellular glutamate levels in the long term anoxic turtle striatum: coordinated activity of glutamate transporters, adenosine, K(ATP) (+) channels and GABA. J. Biomed. Sci. 14, 809 817. (Pubitemid 47573154)
87. Valentim L. M., Geyer A. B., Tavares A., Cimarosti H., Worm P. V., Rodnight R., Netto C. A. Salbego C. G. (2001) Effect of global cerebral ischemia and preconditioning on heat shock protein 27 immunocontent and phosphorylation in rat hippocampus. Neuroscience 107, 43 49. (Pubitemid 34023590)
88. Van der Weerd L., Lythgoe M. F., Badin R. A., Valentim L. M., Akbar M. T., de Belleroche J. S., Latchman D. S. Gadian D. G. (2005) Neuroprotective effects of HSP70 overexpression after cerebral ischemia-an MRI study. Exp. Neurol. 195, 257 266. (Pubitemid 41116830)
89. Vass K., Welch W. J. Nowak Jr. T. S. (1988) Localization of 70 kDa stress protein induction in gerbil brain after ischemia. Acta Neuropathol. 77, 128 135. (Pubitemid 19015549)
90. Volloch V., Gabai V. L., Rits S., Force T. Sherman M. Y. (2000) HSP72 can protect cells from heat-induced apoptosis by accelerating the inactivation of stress kinase JNK. Cell Stress Chaperones 5, 139 147.
91. Wagstaff M. J., Collaco-Moraes Y., Aspey B. S., Coffin R. S., Harrison M. J., Latchman D. S. de Belleroche J. S. (1996) Focal cerebral ischemia increases the levels of several classes of heat shock proteins and their corresponding mRNAs. Brain Res. Mol. Brain Res. 42, 236 244. (Pubitemid 27035752)
92. Wang Y. H. Borkan S. C. (1996) Prior heat stress enhances survival of renal epithelial cells after ATP depletion. Am. J. Physiol. 270, F1057 F1065. (Pubitemid 26298655)
93. Wang Y., Knowlton A. A., Christensen T. G., Shih T. Borkan S. C. (1999) Prior heat stress inhibits apoptosis in adenosine triphosphate-depleted renal tubular cells. Kidney Int. 55, 2224 2235. (Pubitemid 29256477)
94. Wang X., Yang C., Chai J., Shi Y. Xue D. (2002) Mechanisms of AIF-mediated apoptotic DNA degradation in Caenorhabditis elegans. Science 298, 1587 1592. (Pubitemid 35387191)
95. Wilmore W. G. Storey K. B. (1997) Antioxidant systems and anoxia tolerance in a freshwater turtle Trachemys scripta elegans. Mol. Cell. Biochem. 170, 177 185. (Pubitemid 27182948)
96. Wolf H. K., Buslei R., Schmidt-Kastner R., Schmidt-Kastner P. K., Pietsch T., Wiestler O. D. Blumcke I. (1995) NeuN: a useful neuronal marker for diagnostic histopathology. J. Histochem. Cytochem. 44, 1167 1171.
97. Zhang Z., Sobel R. A., Cheng D., Steinberg G. K. Yenari M. A. (2001) Mild hypothermia increases Bcl-2 protein expression following global cerebral ischemia. Brain Res. Mol. Brain Res. 95, 75 85. (Pubitemid 33000365)
98. Zhu C., Wang X., Huang Z. et al. (2007) Apoptosis-inducing factor is a major contributor to neuronal loss induced by neonatal cerebral hypoxia-ischemia. Cell Death Differ. 14, 775 784. (Pubitemid 46444515)