Small stress proteins in the central nervous system: From neurodegeneration to neuroprotection

Small Stress Proteins and Human Diseases

Volumn , Issue , 2010, Pages 117-146

  Wyttenbach, Andreas ^a   Hands, Sarah ^a   O'Connor, Vincent ^a  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84963732609     PISSN: None     EISSN: None     Source Type: Book    
DOI: None     Document Type: Chapter

References (133)

1. Quraishe S, Asuni A, Boelens WC, O'Connor V and Wyttenbach A. Expression of the small heat shock protein family in the mouse CNS: differential anatomical and biochemical compartmentalization. Neuroscience, 2008; 153: 483-491.
2. Hampel H, Teipel SJ, Alexander GE, Pogarell O, Rapoport SI and Möller H. In vivo imaging of region and cell type specific neocortical neurodegeneration in Alzheimer's disease. Perspectives of MRI derived corpus callosum measurement for mapping disease progression and effects of therapy. Evidence from studies with MRI, EEG and PET. J Neural Transm. 2002; 109: 837-855.
3. Cowan CM and Raymond LA. Selective neuronal degeneration in Huntington's disease. Curr Top Dev Biol. 2006; 75: 25-71.
4. Orr HT and Zoghbi HY. Trinucleotide Repeat Disorders. Annual Review of Neuroscience, 2007; 30: 575-621.
5. Gasser T. Mendelian forms of Parkinson's disease. Biochim Biophys Acta, 2009; 1792: 587-596.
6. Liberski PP and Ironside JW. An outline of the neuropathology of transmissible spongiform encephalopathies (prion diseases). Folia Neuropathol. 2004; 42 Suppl B: 39-58
7. Cunningham C, Deacon R, Wells H, Boche D, Waters S, Diniz CP, Scott H, Rawlins JN and Perry VH. Synaptic changes characterize early behavioural signs in the ME7 model of murine prion disease. Eur J Neurosci. 2003; 17: 2147-2155.
8. Thind K and Sabbagh MN. Pathological correlates of cognitive decline in Alzheimer's disease. Panminerva Med. 2007; 49: 191-195.
9. Goldbaum O and Richter-Landsberg C. Stress proteins in oligodendrocytes: differential effects of heat shock and oxidative stress. J Neurochem. 2001; 78: 1233-1242.
10. van Noort JM. Stress proteins in CNS inflammation. J Pathol. 2008; 214: 267-275.
11. Haslbeck M, Franzmann T, Weinfurtner D and Buchner J. Some like it hot: the structure and function of small heat-shock proteins. Nat Struct Mol Biol. 2005; 12: 842-846.
12. Der Perng M and Quinlan R. Neuronal diseases: small heat shock proteins calm your nerves. Curr Biol. 2004; 14: R625-626.
13. Aizenstein H, Nebes R, Saxton J, Price J, Mathis C, Tsopelas N, Ziolko S, James J, Snitz B, Houck P, Bi W, Cohen A, Lopresti B, DeKosky S, Halligan E and Klunk W. Frequent amyloid deposition without significant cognitive impairment among the elderly. Arch Neurol. 2008; 65: 1509-1517.
14. Shankar G, Li S, Mehta T, Garcia-Munoz A, Shepardson N, Smith I, Brett F, Farrell M, Rowan M, Lemere C, Regan C, Walsh D, Sabatini B and Selkoe D. Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat Med. 2008; 14: 837-842.
15. Ohyagi Y. Intracellular Amyloid ß-Protein As a Therapeutic Target for Treating Alzheimer's Disease Current Alzheimer Research, 2008; 5: 555-561
16. Adalbert, Gilley J and Coleman M. Abeta, tau and ApoE4 in Alzheimer's disease: the axonal connection. Trends Mol Med. 2007; 13: 135-142.
17. Shinohara H, Inaguma Y, Goto S, Inagaki T and K. K. Alpha B crystallin and HSP28 are enhanced in the cerebral cortex of patients with Alzheimer's disease. J Neurol Sci. 1993; 119: 203-208
18. Lowe J, McDermott H, Pike I, Spendlove I, Landon M and Mayer RJ. alpha B crystallin expression in non-lenticular tissues and selective presence in ubiquitinated inclusion bodies in human disease. J Pathol. 1992; 166
19. Renkawek K, Voorter CE, Bosman GJ, van Workum FP and de Jong WW. Expression of alpha B-crystallin in Alzheimer's disease. Acta Neuropathol. (Berl). 1994; 87: 155
20. Wilhelmus MM, Otte-Höller I, Wesseling P, de Waal RM, Boelens WC and MM V. Specific association of small heat shock proteins with the pathological hallmarks of Alzheimer's disease brains. Neuropathol Appl Neurobiol. 2006; 32: 119-130
21. Raman B, Ban T, Sakai M, Pasta SY, Ramakrishna T, Naiki H, Goto Y and ChM. R. AlphaB-crystallin, a small heat-shock protein, prevents the amyloid fibril growth of an amyloid beta-peptide and beta2-microglobulin. Biochem J. 2005; 392
22. Sherman M and G. M. Heat shock proteins in cancer. Ann N Y Acad Sci. 2007; 1113: 192-201.
23. Ousman SS, Tomooka BH, van Noort JM, Wawrousek EF, O'Connor KC, Hafler DA, Sobel RA, Robinson WH and L. S. Protective and therapeutic role for alphaB-crystallin in autoimmune demyelination. Nature,. 2007; 448: 474-479
24. Iwaki T, Wisniewski T, Iwaki A, Corbin E, Tomokane N, Tateishi J and Goldman JE. Accumulation of alpha B-crystallin in central nervous system glia and neurons in pathologic conditions. Am J Pathol. 1992; 140: 345-356
25. Dabir DV, Trojanowski JQ, Richter-Landsberg C, Lee VM and Forman MS. Expression of the small heat-shock protein alphaB-crystallin in tauopathies with glial pathology. Am.J.Pathol. 2004; 164: 155
26. Wilhelmus MM, Boelens WC, Otte-Holler I, Kamps B, de Waal RM and Verbeek MM. Small heat shock proteins inhibit amyloid-beta protein aggregation and cerebrovascular amyloid-beta protein toxicity. Brain Res. 2006; 1089: 67
27. Le Pichon CE, Valley MT, Polymenidou M, Chesler AT, Sagdullaev BT, Aguzzi A and Firestein S. Olfactory behavior and physiology are disrupted in prion protein knockout mice. Nature Neruoscience, 2009; 12: 60-69
28. Ironside JW. Pathology of variant Creutzfeldt-Jakob disease. Arch Virol Suppl. 2000; 16
29. Silveira JR, Raymond GJ, Hughson AG, Race RE, Sim VL, Hayes SF and Caughey B. The most infectious prion protein particles. Nature, 2005; 437: 257-261
30. Tatzelt J, Voellmy R and Welch W. Abnormalities in stress proteins in prion diseases. Cell Mol Neurobiol. 1998; 18: 721-729
31. Renkawek K, De Jong WW, Merck KB, Frenken CW, Van Workum FP and Bosman GJ. alpha B-crystallin is present in reactive glia in Creutzfeldt-Jakob disease. Acta Neuropathol. 1992; 83: 324-327.
32. Hwang D, Lee IY, Yoo H, Gehlenborg N, Cho JH, Petritis B, Baxter D, Pitstick R, Young R, Spicer D, Price ND, Hohmann JG, Dearmond SJ, Carlson GA and Hood LE. A systems approach to prion disease. Mol Syst Biol. 2009; 5: 252.
33. O'Connor V, Quraishe S, Asuni A, Lunnon K, Baxter M, Brown J, Perry VH and Wyttenbach A. A co-ordinated and selective small heat shock protein response is associated with the ME7 model of prion disease. Neuroprion Conference. 2008; Madrid.
34. Robinson PA. Protein stability and aggregation in Parkinson's disease. Biochem J. 2008; 413: 1-13.
35. Spillantini MG, Schmidt ML, Lee VM, Trojanowski JQ, Jakes R and Goedert M. Alpha-synuclein in Lewy bodies. Nature, 1997; 388: 839-840
36. Henchcliffe C and Beal MF. Mitochondrial biology and oxidative stress in Parkinson disease pathogenesis. Nat Clin Pract Neurol. 2008; 4: 600-609
37. Zhang Y, James M, Middleton FA and Davis RL. Transcriptional analysis of multiple brain regions in Parkinson's disease supports the involvement of specific protein processing, energy metabolism, and signaling pathways, and suggests novel disease mechanisms. Am J Med Genet B Neuropsychiatr Genet. 2005; 137B: 5-16.
38. Renkawek K, Stege GJ and Bosman GJ. Dementia, gliosis and expression of the small heat shock proteins hsp27 and alpha B-crystallin in Parkinson's disease. Neuroreport. 1999; 10: 2273-2276
39. Outeiro TF, Klucken J, Strathearn KE, Liu F, Nguyen P, Rochet J-C, Hyman BT and McLean PJ. Small heat shock proteins protect against [alpha]-synuclein-induced toxicity and aggregation. Biochemical and Biophysical Research Communications, 2006; 351: 631-638
40. Mirza B, Hadberg H, Thomsen P and Moos T. The absence of reactive astrocytosis is indicative of a unique inflammatory process in Parkinson's disease. Neuroscience, 2000; 95: 425-432
41. Braak H, Del Tredici K, Sandmann-Kiel D, Rüb U and Schultz C. Nerve cells expressing heat-shock proteins in Parkinson's disease. Acta Neuropathol. (Berl). 2001; 102: 449-454
42. Rekas A, Adda CG, Andrew Aquilina J, Barnham KJ, Sunde M, Galatis D, Williamson NA, Masters CL, Anders RF, Robinson CV, Cappai R and Carver JA. Interaction of the molecular chaperone alphaB-crystallin with alpha-synuclein: effects on amyloid fibril formation and chaperone activity. J Mol Biol. 2004; 340: 1167-1183
43. Wang J, Martin E, Gonzales V, Borchelt DR and Lee MK. Differential regulation of small heat shock proteins in transgenic mouse models of neurodegenerative diseases. Neurobiology of Ageing, 2008; 29: 586-597.
44. Hands S, Sinadinos C and Wyttenbach A. Polyglutamine gene function and dysfunction in the ageing brain. Biochimica et Biophysica Acta (BBA) -Gene Regulatory Mechanisms, 2008; 1779: 507-521
45. Wyttenbach A. Role of Heat Shock Proteins During Polyglutamine Neurodegeneration: Mechanisms and Hypothesis. Journal of Molecular Neuroscience. 2004; 23: 69-96.
46. Wyttenbach A, Arrigo AP and Richter-Landsberg C. (2006) Role of Heat Shock Proteins during Neurodegeneration in Alzheimer's, Parkinson's and Huntington's Disease. In Heat Shock Proteins in Neural Cells, Eurekah.com.
47. Tsai HF, Lin SJ, Li C and Hsieh M. Decreased expression of Hsp27 and Hsp70 in transformed lymphoblastoid cells from patients with spinocerebellar ataxia type 7. Biochem Biophys Res Commun. 2005; 334: 1279-1286.
48. Chang WH, Cemal CK, Hsu YH, Kuo CL, Nukina N, Chang MH, Hu HT, Li C and Hsieh M. Dynamic expression of Hsp27 in the presence of mutant ataxin-3. Biochem Biophys Res Commun. 2005; 336: 258-267
49. Hay DG, Sathasivam K, Tobaben S, Stahl B, Marber M, Mestril R, Mahal A, Smith DL, Woodman B and Bates GP. Progressive decrease in chaperone protein levels in a mouse model of Huntington's disease and induction of stress proteins as a therapeutic approach. Hum.Mol.Genet. 2004; 13: 1389
50. Zabel C, Chamrad DC, Priller J, Woodman B, Meyer HE, Bates GP and Klose J. Alterations in the mouse and human proteome caused by Huntington's disease. Mol.Cell Proteomics, 2002; 1: 366
51. Wang J, Martin E, Gonzales V, Borchelt DR and Lee MK. Differential regulation of small heat shock proteins in transgenic mouse models of neurodegenerative diseases. Neurobiol Aging, 2008; 29: 586-597
52. Friedman MJ, Shah AG, Fang ZH, Ward EG, Warren ST, Li S and Li XJ. Polyglutamine domain modulates the TBP-TFIIB interaction: implications for its normal function and neurodegeneration. Nat Neurosci. 2007; 10: 1519-1528.
53. Wyttenbach A, Sauvageot O, Carmichael J, Diaz-Latoud C, Arrigo AP and Rubinsztein DC. Heat shock protein 27 prevents cellular polyglutamine toxicity and suppresses the increase of reactive oxygen species caused by huntingtin. Human Molecular Genetics, 2002; 11: 1137-1151
54. Laity JH and Andrews GK. Understanding the mechanisms of zinc-sensing by metalresponse element binding transcription factor-1 (MTF-1). Archives of Biochemistry and Biophysics, 2007; 463: 201-210.
55. Hidalgo J, Aschner M, Zatta P and Vasák M. Roles of the metallothionein family of proteins in the central nervous system. Brain Research Bulletin, 2001; 55: 133-145
56. Hidalgo J, Penkowa M, Espejo C, Martinez-Caceres EM, Carrasco J, Quintana A, Molinero A, Florit S, Giralt M and Ortega-Aznar A. Expression of Metallothionein-I, -II, and -III in Alzheimer Disease and Animal Models of Neuroinflammation. Experimental Biology and Medicine, 2006; 231: 1450-1458.
57. Zambenedetti P, Giordano R and Zatta P. Metallothioneins are highly expressed in astrocytes and microcapillaries in Alzheimer's disease. Journal of Chemical Neuroanatomy, 1998; 15: 21-26.
58. Miyazaki I, Asanuma M, Higashi Y, Sogawa CA, Tanaka K-i and Ogawa N. Agerelated changes in expression of metallothionein-III in rat brain. Neuroscience Research, 2002; 43: 323-333
59. Yu WH, Lukiw WJ, Bergeron C, Niznik HB and Fraser PE. Metallothionein III is reduced in Alzheimer's disease. Brain Research, 2001; 894: 37-45
60. Colangelo V, Schurr J, Ball MJ, Pelaez RP, Bazan NG and Lukiw WJ. Gene expression profiling of 12633 genes in Alzheimer hippocampal CA1: Transcription and neurotrophic factor down-regulation and up-regulation of apoptotic and proinflammatory signaling. Journal Of Neuroscience Research, 2002; 70: 462-473
61. Tsuji S, Kobayashi H, Uchida Y, Ihara Y and Miyatake T. Molecular cloning of human growth inhibitory factor cDNA and its down-regulation in Alzheimer's disease. EMBO J. 1992; 11: 4843-4850
62. Shiraga H, Pfeiffer RF and Ebadi M. The effects of 6-hydroxydopamine and oxidative stress on the level of brain metallothionein. Neurochem Int. 1993; 23: 561-566
63. Rojas P, Hidalgo J, Ebadi M and Rios C. Changes of Metallothionein I + II Proteins in the Brain after 1-Methyl-4-Phenylpyridinium Administration in Mice. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 2000; 24: 143-154
64. Hodges A, Strand AD, Aragaki AK, Kuhn A, Sengstag T, Hughes G, Elliston LA, Hartog C, Goldstein DR, Thu D, Hollingsworth ZR, Collin F, Synek B, Holmans PA, Young AB, Wexler NS, Delorenzi M, Kooperberg C, Augood SJ, Faull RLM, Olson JM, Jones L and Luthi-Carter R. Regional and cellular gene expression changes in human Huntington's disease brain. Hum. Mol. Genet. 2006; 15: 965-977.
65. Wyttenbach A, Swartz J, Kita H, Thykjaer T, Carmichael J, Bradley J, Brown R, Maxwell M, Schapira A, Orntoft TF, Kato K and Rubinsztein DC. Polyglutamine expansions cause decreased CRE-mediated transcription and early gene expression changes prior to cell death in an inducible cell model of Huntington's disease. Human Molecular Genetics, 2001; 10: 1829-1845.
66. Duguid JR, Bohmont CW, Liu NG and Tourtellotte WW. Changes in brain gene expression shared by scrapie and Alzheimer disease. Proc Natl Acad Sci U S A. 1989; 86: 7260-7264
67. Hanlon J, Monks E, Hughes C, Weavers E and Rogers M. Metallothionein in Bovine Spongiform Encephalopathy. Journal of Comparative Pathology, 2002; 127: 280-289
68. Kawashima T, Doh-ura K, Torisu M, Uchida Y, Furuta A and Iwaki T. Differential Expression of Metallothioneins in Human Prion Diseases. Dement Geriatr Cogn Disord. 2000; 11: 251-262.
69. Halliwell B. Oxidative stress and neurodegeneration: where are we now? Journal of Neurochemistry, 2006; 97: 1634-1658
70. Erickson JC, Sewell AK, Jensen LT, Winge DR and Palmiter RD. Enhanced neurotrophic activity in Alzheimer's disease cortex is not associated with downregulation of metallothionein-III (GIF). Brain Research, 1994; 649: 297-304
71. Meloni G, Sonois V, Delaine T, Guilloreau L, Gillet A, Teissie J, Faller P and Vasak M. Metal swap between Zn7-metallothionein-3 and amyloid-[beta]-Cu protects against amyloid-[beta] toxicity. Nat Chem Biol. 2008; 4: 366-372
72. Tortosa R, Vidal E, Costa C, Alamillo E, Torres JM, Ferrer I and Pumarola M. Stress response in the central nervous system of a transgenic mouse model of bovine spongiform encephalopathy. The Veterinary Journal, 2008; 178: 126-129.
73. Vidal E, Tortosa R, Márquez M, Serafin A, Hidalgo J and Pumarola M. Infection of metallothionein 1 + 2 knockout mice with Rocky Mountain Laboratory scrapie. Brain Research, 2008; 1196: 140-150
74. Ebadi M, Brown-Borg H, El Refaey H, Singh BB, Garrett S, Shavali S and Sharma SK. Metallothionein-mediated neuroprotection in genetically engineered mouse models of Parkinson's disease. Molecular Brain Research, 2005; 134: 67-75
75. Sharma SK and Ebadi M. Metallothionein Attenuates 3-Morpholinosydnonimine (SIN-1)-Induced Oxidative Stress in Dopaminergic Neurons. Antioxidants & Redox Signaling, 2003; 5: 251-264
76. Ebadi M and Sharma S. Metallothioneins 1 and 2 Attenuate Peroxynitrite-Induced Oxidative Stress in Parkinson Disease. Experimental Biology and Medicine, 2006; 231: 1576-1583
77. Hwang YP, Kim HG, Han EH and Jeong HG. Metallothionein-III protects against 6-hydroxydopamine-induced oxidative stress by increasing expression of heme oxygenase-1 in a PI3K and ERK/Nrf2-dependent manner. Toxicology and Applied Pharmacology, 2008; 231: 318-327
78. Chung RS, Penkowa M, Dittmann J, King CE, Bartlett C, Asmussen JW, Hidalgo J, Carrasco J, Leung YKJ, Walker AK, Fung SJ, Dunlop SA, Fitzgerald M, Beazley LD, Chuah MI, Vickers JC and West AK. Redefining the Role of Metallothionein within the Injured Brain: Extracellular metallothioneins play an important role in the astroctyteneuron response to injury. J. Biol. Chem. 2008; 283: 15349-15358
79. Gauthier MA, Eibl JK, Crispo JA and Ross GM. Covalent arylation of metallothionein by oxidized dopamine products: a possible mechanism for zinc-mediated enhancement of dopaminergic neuron survival. Neurotox Res. 2008; 14: 317-328
80. Chung RS, Vickers JC, Chuah MI and West AK. Metallothionein-IIA Promotes Initial Neurite Elongation and Postinjury Reactive Neurite Growth and Facilitates Healing after Focal Cortical Brain Injury. J. Neurosci. 2003; 23: 3336-3342
81. Køhler LB, Berezin V, Bock E and Penkowa M. The role of metallothionein II in neuronal differentiation and survival. Brain Research, 2003; 992: 128-136
82. Uchida Y and Ihara Y. The N-terminal Portion of Growth Inhibitory Factor Is Sufficient for Biological Activity. J. Biol. Chem. 1995; 270: 3365-3369
83. Bush A and Tanzi RE. Therapeutics for Alzheimer's disease based on the metal hypothesis. Neurotherapeutics, 2008; 5: 421-432
84. Hyman M. Schipper WS, Hillel Zukor, Jacob R. Hascalovici, David Zeligman,. Heme Oxygenase-1 and Neurodegeneration: Expanding Frontiers of Engagement. Journal of Neurochemistry,. 2009; 9999
85. Dennery PA. Regulation and role of heme oxygenase in oxidative injury. Curr Top Cell Regul. 2000; 36: 181-199
86. Smith MA, Kutty RK, Richey PL, Yan SD, Stern D, Chader GJ, Wiggert B, Petersen RB and Perry G. Heme oxygenase-1 is associated with the neurofibrillary pathology of Alzheimer's disease. Am J Pathol. 1994; 145: 42-47
87. Schipper HM, Cissé S and Stopa EG. Expression of heme oxygenase-1 in the senescent and Alzheimer-diseased brain. Ann Neurol. 1995; 37: 758-768
88. Smith M, Keisuke Hirai, Karen Hsiao, Miguel A. Pappolla, Peggy L. R. Harris, Sandra L. Siedlak, Massimo Tabaton and George Perry. Amyloid-beta Deposition in Alzheimer Transgenic Mice Is Associated with Oxidative Stress. Journal of Neurochemistry. 1998; 70: 2212-2215
89. Song W, Patel A, Dong H, Paudel HK and Schipper HM. Heme oxygenase-1 promotes proteosomal degradation of tau and a-synuclein in human neuroblastoma cells. Alz Demen. 2008; 4: T410
90. Takahashi M, Doré S, Ferris CD, Tomita T, Sawa A, Wolosker H, Borchelt DR, Iwatsubo T, Kim S-H, Thinakaran G, Sisodia SS and Snyder SH. Amyloid Precursor Proteins Inhibit Heme Oxygenase Activity and Augment Neurotoxicity in Alzheimer's Disease. Neuron. 2000; 28: 461-473.
91. Rizzardini M, Chiesa R, Angeretti N, Lucca E, Salmona M and Forloni G. Prion Protein Fragment 106-126 Differentially Induces Heme Oxygenase-1 mRNA in Cultured Neurons and Astroglial Cells. Journal of Neurochemistry, 1997; 68: 715-720
92. Yun S-W, Gerlach M, Riederer P and Klein MA. Oxidative stress in the brain at early preclinical stages of mouse scrapie. Experimental Neurology, 2006; 201: 90-98
93. Choi Y-G, Kim J-I, Lee H-P, Jin J-K, Choi E-K, Carp RI and Kim Y-S. Induction of heme oxygenase-1 in the brains of scrapie-infected mice. Neuroscience Letters, 2000; 289: 173-176.
94. Guentchev M, Voigtländer T, Haberler C, Groschup MH and Budka H. Evidence for Oxidative Stress in Experimental Prion Disease. Neurobiology Of Disease, 2000; 7: 270-273.
95. Petersen R, Siedlak S, Lee H-g, Kim Y-S, Nunomura A, Tagliavini F, Ghetti B, Cras P, Moreira P, Castellani R, Guentchev M, Budka H, Ironside J, Gambetti P, Smith M and Perry G. Redox metals and oxidative abnormalities in human prion diseases. Acta Neuropathologica, 2005; 110: 232-238.
96. Schipper HM, Liberman A and Stopa EG. Neural Heme Oxygenase-1 Expression in Idiopathic Parkinson's Disease. Experimental Neurology, 1998; 150: 60-68
97. Hung S-Y, Liou H-C, Kang K-H, Wu R-M, Wen C-C and Fu W-M. Overexpression of Heme Oxygenase-1 Protects Dopaminergic Neurons against 1-Methyl-4-Phenylpyridinium-Induced Neurotoxicity. Mol Pharmacol. 2008; 74: 1564-1575.
98. Song W, Patel A, Qureshi HY, Han D, Schipper HM and Paudel HK. The Parkinson disease-associated A30P mutation stabilizes alpha-synuclein against proteasomal degradation triggered by heme oxygenase-1 over-expression in human neuroblastoma cells. Journal of Neurochemistry. 2009; May 13 Epub ahead of print.
99. Dwyer BE, Nishimura RN and Lu S-Y. Differential expression of heme oxygenase-1 in cultured cortical neurons and astrocytes determined by the aid of a new heme oxygenase antibody. Response to oxidative stress. Molecular Brain Research, 1995; 30: 37-47.
100. Hirose W, Ikematsu K and Tsuda R. Age-associated increases in heme oxygenase-1 and ferritin immunoreactivity in the autopsied brain. Legal Medicine, 2003; 5: S360-S366.
101. Kadoya C, Domino EF, Yang G-Y, Stern JD and Betz AL. Preischemic But Not Postischemic Zinc Protoporphyrin Treatment Reduces Infarct Size and Edema Accumulation After Temporary Focal Cerebral Ischemia in Rats. Stroke, 1995; 26: 1035-1038.
102. Koeppen AH, Dickson AC and Smith J. Heme oxygenase in experimental intracerebral hemorrhage: the benefit of tin-mesoporphyrin. J Neuropathol Exp Neurol. 2004; 63: 587-597
103. Lee DW, Gelein RM and Opanashuk LA. Heme-Oxygenase-1 Promotes Polychlorinated Biphenyl Mixture Aroclor 1254-Induced Oxidative Stress and Dopaminergic Cell Injury. Toxicol. Sci. 2006; 90: 159-167.
104. Murray CJ and Lopez A. Mortality by cause for eight regions of the world: Global Burden of Disease Study. LANCET, 1997; 349: 1269-1276.
105. Durukan A and Tatlisumak T. Acute ischemic stroke: overview of major experimental rodent models, pathophysiology, and therapy of focal cerebral ischemia. Pharmacol Biochem Behav. 2007; 87: 179-197.
106. Dienel GA, Kiessling M, Jacewicz M and Pulsinelli WA. Synthesis of heat shock proteins in rat brain cortex after transient ischemia. J Cereb Blood Flow Metab. 1986; 6: 505-510.
107. Minami M, Mizutani T, Kawanishi R, Suzuki Y and Mori H. Neuronal expression of alphaB crystallin in cerebral infarction. Acta Neuropathol. (Berl). 2003; 105: 549-554
108. Piao CS, Kim SW, Kim JB and Lee JK. Co-induction of alphaB-crystallin and MAPKAPK-2 in astrocytes in the penumbra after transient focal cerebral ischemia. Exp Brain Res. 2005; 163: 421-429.
109. Kato H, Kogure K, Liu XH, Araki T, Kato K and Y. I. Immunohistochemical localization of the low molecular weight stress protein HSP27 following focal cerebral ischemia in the rat. Brain Res. 1995; 679
110. Currie RW, Ellison JA, White RF, Feuerstein GZ, Wang X and Barone FC. Benign focal ischemic preconditioning induces neuronal Hsp70 and prolonged astrogliosis with expression of Hsp27. Brain Res. 2000; 863: 169-168
111. Villapol S, Acarin L, Faiz M, Castellano B and Gonzalez B. Survivin and heat shock protein 25/27 colocalize with cleaved caspase-3 in surviving reactive astrocytes following excitotoxicity to the immature brain. Neuroscience, 2008; 153: 108-119
112. Valentim LM, Rodnight R, Geyer AB, Horn AP, Tavares A, Cimarosti H, Netto CA and Salbego CG. Changes in heat shock protein 27 phosphorylation and immunocontent in response to preconditioning to oxygen and glucose deprivation in organotypic hippocampal cultures. Neuroscience, 2003; 118: 379-378.
113. Acarin L, Paris J, González B and Castellano B. Glial expression of small heat shock proteins following an excitotoxic lesion in the immature rat brain. Glia. 2002; 38: 1-14
114. Sanz O, Acarin L, González B and Castellano B. Expression of 27 kDa heat shock protein (Hsp27) in immature rat brain after a cortical aspiration lesion. Glia. 2001; 36: 259-270.
115. Niwa M, Hara A, Taguchi A, Aoki H, Kozawa O and Mori H. Spatiotemporal expression of Hsp20 and its phosphorylation in hippocampal CA1 pyramidal neurons after transient forebrain ischemia. Neurol Res. 2008.
116. Lu A, Ran R, Parmentier-Batteur S, Nee A and Sharp FR. Geldanamycin induces heat shock proteins in brain and protects against focal cerebral ischemia. J Neurochem. 2002; 81: 355-364.
117. Lu A, Ran RQ, Clark J, Reilly M, Nee A and Sharp FR. 17-beta-estradiol induces heat shock proteins in brain arteries and potentiates ischemic heat shock protein induction in glia and neurons. J Cereb Blood Flow Metab. 2002; 22: 183-195.
118. Badin RA, Modo M, Cheetham M, Thomas DL, Gadian DG, Latchman DS and Lythgoe MF. Protective effect of post-ischaemic viral delivery of heat shock proteins in vivo. J Cereb Blood Flow Metab. 2009; 29: 254-263.
119. Reynolds LP and Allen GV. A review of heat shock protein induction following cerebellar injury. Cerebellum, 2003; 2: 171-177
120. Akbar MT, Lundberg AM, Liu K, Vidyadaran S, Wells KE, Dolatshad H, Wynn S, Wells DJ, Latchman DS and de Belleroche J. The neuroprotective effects of heat shock protein 27 overexpression in transgenic animals against kainate-induced seizures and hippocampal cell death. J Biol Chem. 2003; 278: 19956-19965.
121. Stetler RA, Cao G, Gao Y, Zhang F, Wang S, Weng Z, Vosler P, Zhang L, Signore A, Graham SH and Chen J. Hsp27 protects against ischemic brain injury via attenuation of a novel stress-response cascade upstream of mitochondrial cell death signaling. J Neurosci. 2008; 28: 13038-13055.
122. An JJ, Lee YP, Kim SY, Lee SH, Lee MJ, Jeong MS, Kim DW, Jang SH, Yoo KY, Won MH, Kang TC, Kwon OS, Cho SW, Lee KS, Park J, Eum WS and Choi SY. Transduced human PEP-1-heat shock protein 27 efficiently protects against brain ischemic insult. FEBS Journal, 2008; 275: 1296-1308.
123. Willis D, Li KW, Zheng JQ, Chang JH, Smit A, Kelly T, Merianda TT, Sylvester J, van Minnen J and Twiss JL. Differential transport and local translation of cytoskeletal, injury-response, and neurodegeneration protein mRNAs in axons. J Neurosci. 2005; 25: 778-791
124. Neal JW, Singhrao SK, Jasani B and Newman GR. Immunocytochemically detectable metallothionein is expressed by astrocytes in the ischaemic human brain. Neuropathol Appl Neurobiol. 1996; 22: 243-247.
125. Yousuf S, Atif F, Ahmad M, Hoda N, Ishrat T, Khan B and Islam F. Resveratrol exerts its neuroprotective effect by modulating mitochondrial dysfunctions and associated cell death during cerebral ischemia. Brain Res. 2009; 1250: 242-253
126. Wakida K, Shimazawa M, Hozumi I, Satoh M, Nagase H, Inuzuka T and Hara H. Neuroprotective effect of erythropoietin, and role of metallothionein-1 and -2, in permanent focal cerebral ischemia. Neuroscience, 2007; 148: 105-114
127. Fukuda K, Panter SS, Sharp FR and Noble LJ. Induction of heme oxygenase-1 (HO-1) after traumatic brain injury in the rat. Neurosci Lett. 1995; 199: 127-130
128. Beschorner R, Adjodah D, Schwab JM, Mittelbronn M, Pedal I, Mattern R, Schluesener HJ and Meyermann R. Long-term expression of heme oxygenase-1 (HO-1, HSP-32) following focal cerebral infarctions and traumatic brain injury in humans. Acta Neuropathol. 2000; 100: 377-384
129. Panahian N, Yoshiura M and Maines MD. Overexpression of heme oxygenase-1 is neuroprotective in a model of permanent middle cerebral artery occlusion in transgenic mice. J Neurochem. 1999; 72: 1187-1203
130. Yang C, Zhang X, Fan H and Liu Y. Curcumin upregulates transcription factor Nrf2, HO-1 expression and protects rat brains against focal ischemia. Brain Res. 2009; May 13 Epub ahead of print
131. Saleem S, Zhuang H, Biswal S, Christen Y and Doré S. Ginkgo biloba extract neuroprotective action is dependent on heme oxygenase 1 in ischemic reperfusion brain injury. Stroke, 2008; 39: 3389-3396
132. Nakaso K, Kitayama M, Fukuda H, Kimura K, Yanagawa T, Ishii T, Nakashima K and Yamada K. Oxidative stress-related proteins A170 and heme oxygenase-1 are differently induced in the rat cerebellum under kainate-mediated excitotoxicity. Neurosci Lett. 2000; 282: 57-60.
133. Imuta N, Hori O, Kitao Y, Tabata Y, Yoshimoto T, Matsuyama T and Ogawa S. Hypoxia-mediated induction of heme oxygenase type I and carbon monoxide release from astrocytes protects nearby cerebral neurons from hypoxia-mediated apoptosis. Antioxid Redox Signal, 2007; 9: 543-552.