The small heat shock protein Hsp27 protects cortical neurons against the toxic effects of β-amyloid peptide

Journal of Neuroscience Research

Volumn 87, Issue 14, 2009, Pages 3161-3175

  King, Michael ^a   Nafar, Firoozeh ^a   Clarke, Joseph ^a   Mearow, Karen ^a  

^a MEMORIAL UNIVERSITY OF NEWFOUNDLAND   (Canada)

Author keywords

Amyloid; Cortical neurons; Heat shock protein; Hsp27; Transfection

Indexed keywords

AMYLOID BETA PROTEIN; COMPLEMENTARY DNA; ENHANCED GREEN FLUORESCENT PROTEIN; HEAT SHOCK PROTEIN 27;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN NERVE CELL; CELL SURVIVAL; CONTROLLED STUDY; DNA TRANSFECTION; DRUG EFFECT; DRUG MECHANISM; GENE OVEREXPRESSION; HEAT STRESS; NERVE CELL GROWTH; NERVE DEGENERATION; NEUROPROTECTION; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; UPREGULATION;

AMYLOID BETA-PROTEIN; ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CELLS, CULTURED; CEREBRAL CORTEX; HOT TEMPERATURE; HSP27 HEAT-SHOCK PROTEINS; IMMUNOHISTOCHEMISTRY; MICROSCOPY, CONFOCAL; MITOCHONDRIA; NEURONS; POLYMERASE CHAIN REACTION; RATS; TRANSFECTION;

EID: 70449461063     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.22145     Document Type: Article

References (63)

1. Ackerley S, James PA, Kalli A, French S, Davies KE, Talbot K. 2006. A mutation in the small heat-shock protein HSPB1 leading to distal hereditary motor neuronopathy disrupts neurofilament assembly and the axonal transport of specific cellular cargoes. Hum Mol Genet 15:347-354. (Pubitemid 43125988)
2. Akbar MT, Wells DJ, Latchman DS, de Belleroche J. 2001. Heat shock protein 27 shows a distinctive widespread spatial and temporal pattern of induction in CNS glial and neuronal cells compared with heat shock protein 70 and caspase 3 following kainate administration. Brain Res Mol Brain Res 93:148-163.
3. Akbar MT, Lundberg AM, Liu K, Vidyadaran S, Wells KE, Dolatshad H, Wynn S, Wells DJ, Latchman DS, de Belleroche J. 2003. The neuroprotective effects of heat shock protein 27 overexpression in transgenic animals against kainate-induced seizures and hippocampal cell death. J Biol Chem 278:19956-19965. (Pubitemid 36799187)
4. 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, Choi SY. 2008. Transduced human PEP-1-heat shock protein 27 efficiently protects against brain ischemic insult. FEBS J 275:1296-1308.
5. Armstrong CL, Krueger-Naug AM, Currie RW, Hawkes R. 2001. Constitutive expression of heat shock protein HSP25 in the central nervous system of the developing and adult mouse. J Comp Neurol 434:262-274. (Pubitemid 32402134)
6. Barr CS, Dokas LA. 1999. Glucocorticoids regulate the synthesis of HSP27 in rat brain slices. Brain Res 847:9-17.
7. Bechtold DA, Brown IR. 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.
8. Bechtold DA, Brown IR. 2003. Induction of Hsp27 and Hsp32 stress proteins and vimentin in glial cells of the rat hippocampus following hyperthermia. Neurochem Res 28:1163-1173.
9. Benndorf R, Welsh MJ. 2004. Shocking degeneration. Nat Genet 36:547-548.
10. Bjorkdahl C, Sjogren MJ, Zhou X, Concha H, Avila J, Winblad B, Pei JJ. 2008. Small heat shock proteins Hsp27 or alphaB-crystallin and the protein components of neurofibrillary tangles: tau and neurofilaments. J Neurosci Res 86:1343-1352. (Pubitemid 351571908)
11. Busciglio J, Lorenzo A, Yeh J, Yankner BA. 1995. Beta-amyloid fibrils induce tau phosphorylation and loss of microtubule binding. Neuron 14:879-888.
12. Carrettiero DC, Hernandez I, Neveu P, Papagiannakopoulos T, Kosik KS. 2009. The cochaperone BAG2 sweeps paired helical filament-insoluble tau from the microtubule. J Neurosci 29:2151-2161.
13. Chen S, Brown IR. 2007. Neuronal expression of constitutive heat shock proteins: implications for neurodegenerative diseases. Cell Stress Chaperones 12:51-58. (Pubitemid 47403328)
14. Costigan M, Mannion RJ, Kendall G, Lewis SE, Campagna JA, Coggeshall RE, Meridith-Middleton J, Tate S, Woolf CJ. 1998. Heat shock protein 27: developmental regulation and expression after peripheral nerve injury. J Neurosci 18:5891-5900. (Pubitemid 28341365)
15. Dierick I, Irobi J, De Jonghe P, Timmerman V. 2005. Small heat shock proteins in inherited peripheral neuropathies. Ann Med 37:413-422. (Pubitemid 41476127)
16. Evgrafov OV, Mersiyanova I, Irobi J, Van Den Bosch L, Dierick I, Leung CL, Schagina O, Verpoorten N, Van Impe K, Fedotov V, Dadali E, Auer-Grumbach M, Windpassinger C, Wagner K, Mitrovic Z, Hilton-Jones D, Talbot K, Martin JJ, Vasserman N, Tverskaya S, Polyakov A, Liem RK, Gettemans J, Robberecht W, De Jonghe P, Timmerman V. 2004. Mutant small heat-shock protein 27 causes axonal Charcot-Marie-Tooth disease and distal hereditary motor neuropathy. Nat Genet 36:602-606. (Pubitemid 38715987)
17. Franklin TB, Krueger-Naug AM, Clarke DB, Arrigo AP, Currie RW. 2005. The role of heat shock proteins Hsp70 and Hsp27 in cellular protection of the central nervous system. Int J Hyperthermia 21:379-392.
18. Grace EA, Rabiner CA, Busciglio J. 2002. Characterization of neuronal dystrophy induced by fibrillar amyloid beta: implications for Alzheimer's disease. Neuroscience 114:265-273. (Pubitemid 35247506)
19. Haass C, Selkoe DJ. 2007. Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid beta-peptide. Nat Rev 8:101-112. (Pubitemid 46432529)
20. Houlden H, Laura M, Wavrant-De Vrieze F, Blake J, Wood N, Reilly MM. 2008. Mutations in the HSP27 (HSPB1) gene cause dominant, recessive, and sporadic distal HMN/CMT type 2. Neurology 71:1660-1668.
21. Irobi J, Van Impe K, Seeman P, Jordanova A, Dierick I, Verpoorten N, Michalik A, De Vriendt E, Jacobs A, Van Gerwen V, Vennekens K, Mazanec R, Tournev I, Hilton-Jones D, Talbot K, Kremensky I, Van Den Bosch L, Robberecht W, Van Vandekerckhove J, Broeckhoven C, Gettemans J, De Jonghe P, Timmerman V. 2004. Hot-spot residue in small heat-shock protein 22 causes distal motor neuropathy. Nat Genet 36:597-601. (Pubitemid 38715986)
22. Jiang X, Tian F, Mearow K, Okagaki P, Lipsky RH, Marini AM. 2005. The excitoprotective effect of N-methyl-D-aspartate receptors is mediated by a brain-derived neurotrophic factor autocrine loop in cultured hippocampal neurons. J Neurochem 94:713-722. (Pubitemid 41098503)
23. Johnson GV, Stoothoff WH. 2004. Tau phosphorylation in neuronal cell function and dysfunction. J Cell Sci 117:5721-5729. (Pubitemid 40123939)
24. Kalwy SA, Akbar MT, Coffin RS, de Belleroche J, Latchman DS. 2003. Heat shock protein 27 delivered via a herpes simplex virus vector can protect neurons of the hippocampus against kainic-acid-induced cell loss. Brain Res Mol Brain Res 111:91-103.
25. 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)
26. Krueger-Naug AM, Hopkins DA, Armstrong JN, Plumier JC, Currie RW. 2000. Hyperthermic induction of the 27-kDa heat shock protein (Hsp27) in neuroglia and neurons of the rat central nervous system. J Comp Neurol 428:495-510.
27. 1-42 amyloidogenesis. FEBS Lett 416:117-121.
28. Latchman DS. 2005. HSP27 and cell survival in neurones. Int J Hyperthermia 21:393-402.
29. Lee S, Carson K, Rice-Ficht A, Good T. 2005. Hsp20, a novel alpha-crystallin, prevents Abeta fibril formation and toxicity. Protein Sci 14:593-601. (Pubitemid 40283897)
30. Leschik J, Welzel A, Weissmann C, Eckert A, Brandt R. 2007. Inverse and distinct modulation of tau-dependent neurodegeneration by presenilin 1 and amyloid-beta in cultured cortical neurons: evidence that tau phosphorylation is the limiting factor in amyloid-beta-induced cell death. J Neurochem 101:1303-1315. (Pubitemid 46718815)
31. Lukiw WJ. 2004. Gene expression profiling in fetal, aged, and Alzheimer hippocampus: a continuum of stress-related signaling. Neurochem Res 29:1287-1297.
32. Mearow KM, Dodge ME, Rahimtula M, Yegappan C. 2002. Stress-mediated signaling in PC12 cells - the role of the small heat shock protein, Hsp27, and Akt in protecting cells from heat stress and nerve growth factor withdrawal. J Neurochem 83:452-462. (Pubitemid 35191410)
33. Miller-Graziano CL, De A, Laudanski K, Herrmann T, Bandyopadhyay S. 2008. HSP27: an anti-inflammatory and immunomodulatory stress protein acting to dampen immune function. Novartis Found Symp 91:196-208; discussion 208-111, 221-1194
34. Mounier N, Arrigo AP. 2002. Actin cytoskeleton and small heat shock proteins: how do they interact? Cell stress Chaperones 7:167-176.
35. Pardon MC, Rattray I. 2008. What do we know about the long-term consequences of stress on ageing and the progression of age-related neurodegenerative disorders? Neurosci Biobehav Rev 32:1103-1120.
36. Perez-Olle R, Jones ST, Liem RK. 2004. Phenotypic analysis of neurofilament light gene mutations linked to Charcot-Marie-Tooth disease in cell culture models. Hum Mol Genet 13:2207-2220. (Pubitemid 39359921)
37. Perez-Olle R, Lopez-Toledano MA, Goryunov D, Cabrera-Poch N, Stefanis L, Brown K, Liem RK. 2005. Mutations in the neurofilament light gene linked to Charcot-Marie-Tooth disease cause defects in transport. J Neurochem 93:861-874. (Pubitemid 40695745)
38. Perng MD, Cairns L, van den IP, Prescott A, Hutcheson AM, Quinlan RA. 1999. Intermediate filament interactions can be altered by HSP27 and alphaB-crystallin. J Cell Sci 112:2099-2112. (Pubitemid 29355425)
39. Perrin V, Regulier E, Abbas-Terki T, Hassig R, Brouillet E, Aebischer P, Luthi-Carter R, Deglon N. 2007. Neuroprotection by Hsp104 and Hsp27 in lentiviral-based rat models of Huntington's disease. Mol Ther 15:903-911. (Pubitemid 46621648)
40. Plumier JC, 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. (Pubitemid 26377054)
41. Rane MJ, Pan Y, Singh S, Powell DW, Wu R, Cummins T, Chen Q, McLeish KR, Klein JB. 2003. Heat shock protein 27 controls apoptosis by regulating Akt activation. J Biol Chem 278:27828-27835. (Pubitemid 36899975)
42. Roy S, Zhang B, Lee VM, Trojanowski JQ. 2005. Axonal transport defects: a common theme in neurodegenerative diseases. Acta Neuropathol 109:5-13. (Pubitemid 40287785)
43. Shankar GM, Li S, Mehta TH, Garcia-Munoz A, Shepardson NE, Smith I, Brett FM, Farrell MA, Rowan MJ, Lemere CA, Regan CM, Walsh DM, Sabatini BL, Selkoe DJ. 2008. Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat Med 14:837-842.
44. Sharp P, Krishnan M, Pullar O, Navarrete R, Wells D, de Belleroche J. 2006. Heat shock protein 27 rescues motor neurons following nerve injury and preserves muscle function. Exp Neurol 198:511-518.
45. Sharp PS, Akbar MT, Bouri S, Senda A, Joshi K, Chen HJ, Latchman DS, Wells DJ, de Belleroche J. 2008. Protective effects of heat shock protein 27 in a model of ALS occur in the early stages of disease progression. Neurobiol Dis 30:42-55.
46. Shimura H, Miura-Shimura Y, Kosik KS. 2004. Binding of tau to heat shock protein 27 leads to decreased concentration of hyperphosphorylated tau and enhanced cell survival. J Biol Chem 279:17957-17962. (Pubitemid 38560564)
47. Smith RC, Rosen KM, Pola R, Magrane J. 2005. Stress proteins in Alzheimer's disease. Int J Hyperthermia 21:421-431.
48. Song MS, Rauw G, Baker GB, Kar S. 2008. Memantine protects rat cortical cultured neurons against beta-amyloid-induced toxicity by attenuating tau phosphorylation. Eur J Neurosci 28:1989-2002.
49. Stege GJ, Renkawek K, Overkamp PS, Verschuure P, van Rijk AF, Reijnen-Aalbers A, Boelens WC, Bosman GJ, de Jong WW. 1999. The molecular chaperone alphaB-crystallin enhances amyloid beta neurotoxicity. Biochem Biophys Res Commun 262:152-156. (Pubitemid 29412639)
50. Stetler RA, Cao G, Gao Y, Zhang F, Wang S, Weng Z, Vosler P, Zhang L, Signore A, Graham SH, Chen J. 2008. Hsp27 protects against ischemic brain injury via attenuation of a novel stress-response cascade upstream of mitochondrial cell death signaling. J Neurosci 28:13038-13055.
51. Tucker BA, Rahimtula M, Mearow KM. 2005. Integrin activation and neurotrophin signaling cooperate to enhance neurite outgrowth in sensory neurons. J Comp Neurol 486:267-280. (Pubitemid 40593959)
52. Tucker BA, Rahimtula M, Mearow KM. 2008. Src and FAK are key early signalling intermediates required for neurite growth in NGF-responsive adult DRG neurons. Cell Signal 20:241-257. (Pubitemid 350138385)
53. Valentim LM, Rodnight R, Geyer AB, Horn AP, Tavares A, Cimarosti H, Netto CA, Salbego CG. 2003. Changes in heat shock protein 27 phosphorylation and immunocontent in response to preconditioning to oxygen and glucose deprivation in organotypic hippocampal cultures. Neuroscience 118:379-386. (Pubitemid 36423253)
54. Villapol S, Acarin L, Faiz M, Castellano B, Gonzalez B. 2008. Survivin and heat shock protein 25/27 colocalize with cleaved caspase-3 in surviving reactive astrocytes following excitotoxicity to the immature brain. Neuroscience 153:108-119.
55. Walsh DM, Selkoe DJ. 2007. A beta oligomers - a decade of discovery. J Neurochem 101:1172-1184.
56. Wilhelmus MM, Boelens WC, Otte-Holler I, Kamps B, de Waal RM, Verbeek MM. 2006a. Small heat shock proteins inhibit amyloid-beta protein aggregation and cerebrovascular amyloid-beta protein toxicity. Brain Res 1089:67-78. (Pubitemid 43786300)
57. Wilhelmus MM, Otte-Holler I, Wesseling P, de Waal RM, Boelens WC, Verbeek MM. 2006b. Specific association of small heat shock proteins with the pathological hallmarks of Alzheimer's disease brains. Neuropathol Appl Neurobiol 32:119-130.
58. Williams KL, Rahimtula M, Mearow KM. 2005. Hsp27 and axonal growth in adult sensory neurons in vitro. BMC Neurosci 6:24. (Pubitemid 41418250)
59. Williams KL, Rahimtula M, Mearow KM. 2006. Heat shock protein 27 is involved in neurite extension and branching of dorsal root ganglion neurons in vitro. J Neurosci Res 84:716-723. (Pubitemid 44366673)
60. Wyttenbach A, Sauvageot O, Carmichael J, Diaz-Latoud C, Arrigo AP, Rubinsztein DC. 2002. Heat shock protein 27 prevents cellular polyglutamine toxicity and suppresses the increase of reactive oxygen species caused by huntingtin. Hum Mol Genet 11:1137-1151. (Pubitemid 34521094)
61. Yonekura K, Yokota S, Tanaka S, Kubota H, Fujii N, Matsumoto H, Chiba S. 2004. Prevalence of anti-heat shock protein antibodies in cerebrospinal fluids of patients with Guillain-Barre syndrome. J Neuroimmunol 156:204-209. (Pubitemid 39304201)
62. Zhai J, Lin H, Julien JP, Schlaepfer WW. 2007. Disruption of neurofilament network with aggregation of light neurofilament protein: a common pathway leading to motor neuron degeneration due to Charcot-Marie-Tooth disease-linked mutations in NFL and HSPB1. Hum Mol Genet 16:3103-3116. (Pubitemid 350131329)
63. Zourlidou A, Payne Smith MD, Latchman DS. 2004. HSP27 but not HSP70 has a potent protective effect against alpha-synuclein-induced cell death in mammalian neuronal cells. J Neurochem 88:1439-1448. (Pubitemid 38366920)