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

Journal of Cerebral Blood Flow and Metabolism

Volumn 24, Issue 2, 2004, Pages 167-178

  Nishino, Kazuhiko ^a,b   Nowak Jr , Thaddeus S ^a  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^b NIIGATA UNIVERSITY   (Japan)

Author keywords

Dentate hilus; Hsp27; Hsp72; Ischemia; Preconditioning; Stress protein

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; HEAT SHOCK PROTEIN 27; HEAT SHOCK PROTEIN 72; MICROTUBULE ASSOCIATED PROTEIN 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN RETRIEVAL; ARTICLE; ASTROCYTE; BRAIN ISCHEMIA; BRAIN ISCHEMIC PRECONDITIONING; BRAIN SLICE; CELL LOSS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DENTATE GYRUS; DEPOLARIZATION; DISEASE MODEL; DISEASE SEVERITY; GERBIL; HIPPOCAMPUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS;

EID: 1042278121     PISSN: 0271678X     EISSN: None     Source Type: Journal    
DOI: 10.1097/01.WCB.0000100853.67976.8B     Document Type: Article

References (83)

1. Abe H, Nowak TS Jr (1996a) Gene expression and induced ischemic tolerance following brief insults. Acta Neurobiol Exp 56:3-8
2. Abe H, Nowak TS Jr (1996b) The stress response and its role in cellular defense mechanisms after ischemia. In: Cellular and molecular mechanisms of ischemic brain damage. Advances in neurology, Vol. 71 (Siesjö BK, Wieloch T, eds), Philadelphia: Lippincott-Raven, pp 451-467
3. Abe H, Nowak TS Jr (2000) Postischemic temperature as a modulator of the stress response: dissociation of hsp72 induction from ischemic tolerance in a gerbil model. Neurosci Lett 295:54-58
4. Abe H, Nowak TS Jr (2004) Induced hippocampal neuroprotection in an optimized gerbil ischemia model: insult thresholds for tolerance induction and altered gene expression defined by ischemic depolarization. J Cereb Blood Flow Metab 24:87-97
5. Aoki M, Abe K, Kawagoe J, Nakamura S, Kogure K (1993) Acceleration of HSP70 and HSC70 heat shock gene expression following transient ischemia in the preconditioned gerbil hippocampus. J Cereb Blood Flow Metab 13:781-788
6. Baek SH, Kim JY, Choi JH, Park EM, Han MY, Kim CH, Ahn YS, Park YM (2000) Reduced glutathione oxidation ratio and 8 ohdG accumulation by mild ischemic pretreatment. Brain Res 856:28-36
7. Bigot D, Matus A, Hunt SP (1991) Reorganization of the cytoskeleton in rat neurons following stimulation with excitatory amino acids in vitro. Eur J Neurosci 3:551-558
8. ATP channel openers, adenosine agonists and elipeptic preconditioning are stress signals inducing hippocampal neuroprotection. Neuroscience 100:465-474
9. Cattoretti G, Pileri S, Parravicini C, Becker MHG, Poggi S, Bifulco C, Key G, D'Amato L, Sabattini E, Feudale E, Reynolds F, Gerdes J, Rilke F (1993) Antigen unmasking on formalin-fixed, paraffin-embedded tissue sections. J Pathol 171:83-98
10. Chen J, Graham SH, Zhu RL, Simon RP (1996) Stress proteins and tolerance to focal cerebral ischemia. J Cereb Blood Flow Metab 16:566-577
11. Chen T, Kato H, Liu X-H, Araki T, Itoyama Y, Kogure K (1994) Ischemic tolerance can be induced repeatedly in the gerbil hippocampal neurons. Neurosci Lett 177:159-161
12. Cizkova D, Vanicky I, Gottlieb M, Marsala J (1996) Ischemic damage in the hippocampus: a sliver impregnation and immunocytochemical study in the rat. Arch Ital Biol 134:279-290
13. Costigan M, Mannion RJ, Kendall G, Lewis SE, Campagna JA, Coggeshall RE, Meredith-Middleton J, Tate S, Woolf CJ (1998) Heat shock protein 27: developmental regulation and expression after peripheral nerve injury. J Neurosci 18:5891-5900
14. Furuta S, Ohta S, Hatakeyama T, Nakamura K, Sakaki S (1993) Recovery of protein synthesis in tolerance-induced hippocampal CA1 neurons after transient forebrain ischemia. Acta Neuropathol 86:329-336
15. Gilland E, Bona E, Hagberg H (1998) Temporal changes of regional glucose use, blood flow, and microtubule-associated protein 2 immunostaining after hypoxia-ischemia in the immature rat brain. J Cereb Blood Flow Metab 18:222-228
16. Glazier SS, O'Rourke DM, Graham DI, Welsh FA (1994) Induction of ischemic tolerance following brief focal ischemia in rat brain. J Cereb Blood Flow Metab 14:545-553
17. Hatakeyama T, Matsumoto M, Brengman JM, Yanagihara T (1988) Immunohistochemical investigation of ischemic and postischemic damage after bilateral carotid occlusion in gerbils. Stroke 19:1526-1534
18. Head MW, Corbin E, Goldman JE (1993) Overexpression and abnormal modification of the stress proteins aB-crystallin and HSP27 in Alexander Disease. Am J Pathol 143:1743-1753
19. 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
20. Holmin S, von Gertten C, Sandberg-Nordqvist AC, Lendahl U, Mathiesen T (2001) Induction of astrocyte nestin expression by depolarization in rats. Neurosci Lett 314:151-155
21. Imura T, Shimohama S, Sato M, Nishikawa H, Madono K, Akaike A, Kimura J (1999) Differential expression of small heat shock proteins in reactive astrocytes after focal ischemia: possible role of β-adrenergic receptor. J Neurosci 19:9768-9779
22. Irving EA, McCulloch J, Dewar D (1997) The effect of postmortem delay on the distribution of microtubule-associated proteins τ, MAP2, and MAP5 in the rat. Mol Chem Neuropathol 30:253-271
23. Iwai T, Niwa M, Hara A, Mori H, Uematsu T, Sakai N (2000) DNA fragmentation in the CA2 sector of gerbil hippocampus following transient forebrain ischemia. Brain Res 857:275-278
24. Iwai T, Niwa M, Yamada H, Nozaki K, Tsurumi K (1993) Hypothermic prevention of the hippocampal damage following ischemia in Mongolian gerbils. Comparison between intraischemic and brief postischemic hypothermia. Life Sci 52:1031-1038
25. Iwaki T, Iwaki A, Tateishi J, Sakaki Y, Goldman JE (1993) αβ-Crystallin and 27-kd heat shock protein are regulated by stress conditions in the central nervous system and accumulate in Rosenthal fibers. Am J Pathol 143:487-495
26. Jiao Y, Sun Z, Lee T, Fusco FR, Kimble TD, Meade CA, Cuthbertson S, Reiner A (1999) A simple and sensitive antigen retrieval method for free-floating and slide-mounted tissue sections. J Neurosci Methods 93:149-162
27. Johansen FF, Zimmer J, Diemer NH (1987) Early loss of somatostatin neurons in dentate hilus after cerebral ischemia in the rat precedes CA1 pyramidal loss. Acta Neuropathol (Berl) 73:110-114
28. Kanemitsu H, Kirino T, Nakagomi T, Tsujita Y, Iwamoto T, Tomich JM, Tamura A (1994) Key of induced tolerance to ischemia in gerbil hippocampal CA1 is not at transcriptional level of hsp70 gene: in situ hybridization of hsp70 mRNA. Neurol Res 16:209-212
29. Kato H, Kogure K, Araki T, Itoyama Y (1994a) Astroglial and microglial reactions in the gerbil hippocampus with induced ischemic tolerance. Brain Res 664:69-76
30. 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
31. Kato H, Liu Y, Araki T, Kogure K (1991) Temporal profile of the effects of pretreatment with brief cerebral ischemia on the neuronal damage following secondary ischemic insult in the gerbil: cumulative damage and protective effects. Brain Res 553:238-242
32. Kato H, Liu Y, Kogure K, Kato K (1994b) Induction of 27-kDa heat shock protein following cerebral ischemia in a rat model of ischemic tolerance. Brain Res 634:235-244
33. Kato K, Katoh-Semba R, Takeuchi IK, Ito H, Kamei K (1999) Responses of heat shock proteins hsp27, αβ-crystallin, and hsp70 in rat brain after kainic acid-induced seizure activity. J Neurochem 73:229-236
34. Kirino T (2002) Ischemic tolerance. J Cereb Blood Flow Metab 22:1283-1296
35. Kirino T, Sano K (1984) Selective vulnerability in the gerbil hippocampus following transient ischemia. Acta Neuropathol (Berl) 62:201-208
36. Kirino T, Tsujita Y, Tamura A (1991) Induced tolerance to ischemia in gerbil hippocampal neurons. J Cereb Blood Flow Metab 11:299-307
37. Kitagawa K, Matsumoto M, Kuwabara K, Tagaya M, Ohtsuki T, Hata R, Ueda H, Handa N, Kimura K, Kamada T (1991) 'Ischemic tolerance' phenomenon detected in various brain regions. Brain Res 561:203-211
38. Kitagawa K, Matsumoto M, Saido TC, Ohtsuki T, Kuwabara K, Yagita Y, Mabuchi T, Yanagihara T, Hori M (1999) Species differences in fodrin proteolysis in the ischemic brain. J Neurosci Res 55:643-649
39. Koistinaho J, Hökfelt T (1997) Altered gene expression in brain ischemia. Neuroreport 8(2):i-viii
40. Lewis SE, Mannion RJ, White FA, Coggeshall RE, Beggs S, Costigan M, Martin JL, Dillman WH, Woolf CJ (1999) A role for HSP27 in sensory neuron survival. J Neurosci 19:8945-8953
41. Lin RCS, Matesic DF, Marvin M, McKay RDG, Brüstle O (1995) Re-expression of the intermediate filament nestin in reactive astrocytes. Neurobiol Dis 2:79-85
42. Liu CL, Martone ME, Hu BR (2003) Ischemic preconditioning prevents protein aggregation after transient cerebral ischemia [abstract]. J Cereb Blood Flow Metab 23(suppl 1):347
43. Liu Y, Kato H, Nakata N, Kogure K (1993) Temporal profile of heat shock protein 70 synthesis in ischemic tolerance induced by preconditioning ischemia in rat hippocampus. Neuroscience 56:921-927
44. Matesic DF, Lin RCS (1994) Microtubule-associated protein 2 as an early indicator of ischemia-induced neurodegeneration in the gerbil hippocampus. J Neurochem 63:1012-1020
45. Matsuyama T, Tsuchiyama M, Nakamura H, Matsumoto M, Sugita M (1993) Hilar somatostatin neurons are more vulnerable to an ischemic insult than CA1 pyramidal neurons. J Cereb Blood Flow Metab 13:229-234
46. Morgan JM, Navabi H, Jasani B (1997) Role of calcium chelation in high-temperature antigen retrieval at different pH values. J Pathol 182:233-237
47. Nakagomi T, Kirino T, Kanemitsu H, Tsujita Y, Tamura A (1993) Early recovery of protein synthesis following ischemia in hippocampal neurons with induced tolerance in the gerbil. Acta Neuropathol 86:10-15
48. 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 recirculation model. Brain Res 615:281-288
49. Nishino K, Harrub JB, Nowak TSJ (1998) Hsp72 detection in a highly controlled gerbil ischemia model using antigen retrieval methods. Soc Neurosci Abstr 24:219
50. Nowak TS Jr, Kiessling M (1999) Reprogramming of gene expression after ischemia. In: Cerebral ischemia: molecular and cellular pathophysiology (Walz W, ed), Totowa, NJ: Humana Press, Inc.
51. Nowak TS Jr, Zhou Q, Valentine WJ, Harrub JB, Abe H (1999) Regulation of heat shock genes by ischemia. In: Stress proteins: handbook of experimental pharmacology (Latchman DS, ed), Heidelberg: Springer
52. Ohta S, Furuta S, Matsubara I, Kohno K, Kumon Y, Sakaki S (1996) Calcium movement in ischemia-tolerant hippocampal CA1 neurons after transient forebrain ischemia in gerbils. J Cereb Blood Flow Metab 16:915-922
53. Ota A, Ikeda T, Ikenoue T, Toshimori K (1997) Sequence of neuronal responses assessed by immunohistochemistry in the newborn rat brain after hypoxia-ischemia. Am J Obstet Gynecol 177:519-526
54. Park JS, Bateman MC, Goldberg MP (1996) Rapid alterations in dendrite morphology during sublethal hypoxia or glutamate receptor activation. Neurobiol Dis 3:215-227
55. Parsell DA, Lindquist S (1994) Heat shock proteins and stress tolerance. In: The biology of heat shock proteins and molecular chaperones (Morimoto R, Tissières A, Georgopoulos C, eds), Plainview, NY: Cold Spring Harbor Laboratory Press, pp 457-494
56. Paschen W, Mies G (1999) Effect of induced tolerance on biochemical disturbances in hippocampal slices from the gerbil during and after oxygen/glucose deprivation. Neuroreport 10:1417-1421
57. Petito CK, Morgello S, Felix JC, Lesser ML (1990) The two patterns of reactive astrocytosis in postischemic rat brain. J Cereb Blood Flow Metab 10:850-859
58. Plumier J-CL, Armstrong JN, Landry J, Babity JM, Robertson HA, Currie RW (1996) Expression of the 27,000 mol. wt heat shock protein following kainic acid-induced status epilepticus in the rat. Neuroscience 75:849-856
59. Plumier J-CL, Armstrong JN, Wood NI, Babity JM, Hamilton TC, Hunter AJ, Robertson HA, Currie RW (1997a) Differential expression of c-fos, Hsp70 and Hsp27 after photothrombotic injury in the rat brain. Mol Brain Res 45:239-246
60. Plumier J-CL, David J-C, Robertson HA, Currie WR (1997b) Cortical application of potassium chloride induces the low-molecular weight heat shock protein (hsp27) in astrocytes. J Cereb Blood Flow Metab 17:781-790
61. Renkawek K, Bosman GJCGM, de Jong WW (1994) Expression of small heat-shock protein hsp 27 in reactive gliosis in Alzheimer disease and other types of dementia. Acta Neuropathol 87:511-519
62. Sanz O, Acarin L, Gonzalez B, Castellano B (2001) Expression of 27 kDa heat shock protein (Hsp27) in immature rat brain after a cortical aspiration lesion. Glia 36:259-270
63. Schiffer D, Giordana MT, Migheli A, Giaccone G, Pezzotta S, Mauro A (1986) Glial fibrillary acidic protein and vimentin in the experimental glial reaction of the rat brain. Brain Res 374:110-118
64. Schmidt-Kastner R, Szymas J, Hossmann K-A (1990) Immunohistochemical study of glial reaction and serum-protein extravasation in relation to neuronal damage in rat hippocampus after ischemia. Neuroscience 38:527-540
65. Schroeter M, Schiene K, Kraemer M, Hagemann G, Weigel H, Eysel UT, Witte OW, Stoll G (1995) Astroglial responses in photochemically induced focal ischemia of the rat cortex. Exp Brain Res 106:1-6
66. Sharp FR, Massa SM, Swanson RA (1999) Heat-shock protein protection. Trends Neurosci 22:97-99
67. Shi S-R, Key ME, Kalra KL (1991) Antigen retrieval in formalin-fixed, paraffin-embedded tissues: An enhancement method for immunohistochemical staining based on microwave oven heating of tissue sections. J Histochem Cytochem 39:741-748
68. Shimazaki K, Nakamura T, Nakamura K, Oguro K, Masuzawa T, Kudo Y, Kawai N (1998) Reduced calcium elevation in hippocampal CA1 neurons of ischemia-tolerant gerbils. Neuroreport 9:1875-1878
69. Shiurba RA, Spooner ET, Ishiguro K, Takahashi M, Yoshida R, Wheelock TR, Imahori K, Cataldo AM, Nixon RA (1998) Immunocytochemistry of formalin-fixed human brain tissues: microwave irradiation of free-floating sections. Brain Res Protocols 2:109-119
70. Simon RP, Cho H, Gwinn R, Lowenstein DH (1991) The temporal profile of 72-kDa heat-shock protein expression following global ischemia. J Neurosci 11:881-889
71. Smith M-L, Auer RN, Siesjo BK (1984) The density and distribution of ischemic brain injury in the rat following 2-10 min of forebrain ischemia. Acta Neuropathol (Berl) 64:319-332
72. Sorimachi T, Abe H, Takeuchi S, Tanaka R (2002) Ischemic depolarization monitoring: evaluation of protein synthesis in the hippocampal CA1 after brief unilateral ischemia in a gerbil model. J Neurosurg 97:104-111
73. Sugimoto A, Shozuhara H, Kogure K, Onodera H (1993) Exposure to sub-lethal ischemia failed to prevent subsequent ischemic death of dentate hilar neurons, as estimated by laminin immunohistochemistry. Brain Res 629:159-162
74. Tomioka C, Nishioka K, Kogure K (1992) Absence of early destructive changes of cytoskeletal proteins after transient ischemia in the rat. Brain Res 586:352-357
75. Valentim LM, Geyer AB, Tavares A, Cimarosti H, Worm PV, Rodnight R, Netto CA, Salbego CG (2001) Effects of global cerebral ischemia and preconditioning on heat shock protein 27 immunocontent and phosphorylation in rat hippocampus. Neuroscience 107:43-49
76. Vanicky I, Balchen T, Diemer NH (1995) Alterations in MAP2 immunostaining after prolonged complete brain ischemia in the rat. Neuroreport 7:161-164
77. Vass K, Welch WJ, Nowak TS Jr (1988) Localization of 70 kDa stress protein induction in gerbil brain after ischemia. Acta Neuropathol 77:128-135
78. Yamada T, Kawamata T, Walker DG, McGeer PL (1992) Vimentin immunoreactivity in normal and pathological human brain tissue. Acta Neuropathol 84:157-162
79. Yamashita S, Miyamoto O, Janjua NA, Tomizawa K, Matsui H, Nakamura T, Nagao S, Itano T (2003) Role of the hippocampal CA2 region following postischemic hypothermia in gerbil. Mol Brain Res 111:8-16
80. Yanagihara T, Brengman JM, Mushynski WE (1990) Differential vulnerability of microtubule components in cerebral ischemia. Acta Neuropathol 80:499-505
81. Yang G, Kitagawa K, Ohtsuki T, Kuwabara K, Mabuchi T, Yagita Y, Takazawa K, Tanaka S, Yanagihara T, Hori M, Matsumoto M (2000) Regional difference of neuronal vulnerability in the murine hippocampus after transient forebrain ischemia. Brain Res 870:195-198
82. Yokota M, Saido TC, Tani E, Kawashima S, Suzuki K (1995) Three distinct phases of fodrin proteolysis induced in postischemic hippocampus. Stroke 26:1901-1907
83. Yoshimi K, Takeda M, Nishimura T, Kudo T, Nakamura Y, Tada K, Iwata N (1991) An immunohistochemical study of MAP2 and clathrin in gerbil hippocampus after cerebral ischemia. Brain Res 560:149-158