HspB5/αB-Crystallin in the Brain

Chapter
Part of the Heat Shock Proteins book series (HESP, volume 8)

Abstract

Many organs including the brain exhibit powerful endogenous cytoprotective mechanisms to survive recurrent cellular stress events, i.e. the development of stress tolerance. Investigation of the molecular mechanisms underlying this neuroprotective phenomenon is of special interest since it may provide the basis to develop new therapeutic strategies for the treatment of neurological diseases. One important mechanism is the upregulation of heat shock proteins. Here, we will review the neuroprotective potential of HspB5/αB-crystallin. HspB5 is expressed in glia as well as in neurons and upregulated in certain cell types or subset of cells at pathophysiological conditions. HspB5 is found to be associated with the disease-causing pathological protein aggregates, such as amyloid plaques in Alzheimer’s disease or Rosenthal fibers in Alexander disease. One possible function of HspB5 is to counteract the aggregation process leading to increased cell survival. However, HspB5 may act additionally via its non-chaperone functions, such as anti-inflammatory, anti-apoptotic properties or association with cytoskeletal proteins influencing filament assembly. The cytoprotective activity of HspB5 is regulated by phosphorylation. Interestingly, in neurons HspB5 is recruited to axons and dendrites by phosphorylation, however, to this end little is known about the molecular targets of phosphoHspB5 in neurons. Identifying the impact of phosphorylation of HspB5 in glia and neurons and the targets of HspB5 may be useful to develop new therapeutic strategies for neurological diseases.

Keywords

HspB5 Neuroprotection Neurodegenerative diseases Stress response Phosphorylation 
This is a preview of subscription content, log in to check access.

References

  1. Alexander WS (1949) Progressive fibrinoid degeneration of fibrillary astrocytes associated with mental retardation in a hydrocephalic infant. Brain 72:373–381, 3 plPubMedCrossRefGoogle Scholar
  2. Arac A, Brownell SE, Rothbard JB, Chen C, Ko RM, Pereira MP, Albers GW, Steinman L, Steinberg GK (2011) Systemic augmentation of alphaB-crystallin provides therapeutic benefit twelve hours post-stroke onset via immune modulation. Proc Natl Acad Sci U S A 108:13287–13292PubMedCrossRefPubMedCentralGoogle Scholar
  3. Arima K, Ogawa M, Sunohara N, Nishio T, Shimomura Y, Hirai S, Eto K (1998) Immunohistochemical and ultrastructural characterization of ubiquitinated eosinophilic fibrillary neuronal inclusions in sporadic amyotrophic lateral sclerosis. Acta Neuropathol 96:75–85PubMedCrossRefGoogle Scholar
  4. Bartelt-Kirbach B, Golenhofen N (2014) Reaction of small heat shock proteins to different kinds of cellular stress in cultured rat hippocampal neurons. Cell Stress Chaperones 19:145–153PubMedCrossRefPubMedCentralGoogle Scholar
  5. Bellyei S, Szigeti A, Pozsgai E, Boronkai A, Gomori E, Hocsak E, Farkas R, Sumegi B, Gallyas F Jr (2007) Preventing apoptotic cell death by a novel small heat shock protein. Eur J Cell Biol 86:161–171PubMedCrossRefGoogle Scholar
  6. Bhat SP, Nagineni CN (1989) alpha B subunit of lens-specific protein alpha-crystallin is present in other ocular and non-ocular tissues. Biochem Biophys Res Commun 158:319–325PubMedCrossRefGoogle Scholar
  7. Bilen J, Bonini NM (2007) Genome-wide screen for modifiers of ataxin-3 neurodegeneration in Drosophila. PLoS Genet 3:1950–1964PubMedCrossRefGoogle Scholar
  8. 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 86:1343–1352PubMedCrossRefGoogle Scholar
  9. Bloemendal H (1981) Molecular and cellular biology of the eye lens. Wiley, New YorkGoogle Scholar
  10. Braak H, Del Tredici K, Sandmann-Kiel D, Rub U, Schultz C (2001) Nerve cells expressing heat-shock proteins in Parkinson’s disease. Acta Neuropathol 102:449–454PubMedGoogle Scholar
  11. Brenner M, Johnson AB, Boespflug-Tanguy O, Rodriguez D, Goldman JE, Messing A (2001) Mutations in GFAP, encoding glial fibrillary acidic protein, are associated with Alexander disease. Nat Genet 27:117–120PubMedCrossRefGoogle Scholar
  12. Bsibsi M, Holtman IR, Gerritsen WH, Eggen BJ, Boddeke E, van der Valk P, van Noort JM, Amor S (2013) Alpha-B-crystallin induces an immune-regulatory and antiviral microglial response in preactive multiple sclerosis lesions. J Neuropathol Exp Neurol 72:970–979PubMedCrossRefGoogle Scholar
  13. Che Y, Piao CS, Han PL, Lee JK (2001) Delayed induction of alpha B-crystallin in activated glia cells of hippocampus in kainic acid-treated mouse brain. J Neurosci Res 65:425–431PubMedCrossRefGoogle Scholar
  14. Dabir DV, Trojanowski JQ, Richter-Landsberg C, Lee VM, Forman MS (2004) Expression of the small heat-shock protein alphaB-crystallin in tauopathies with glial pathology. Am J Pathol 164:155–166PubMedCrossRefPubMedCentralGoogle Scholar
  15. DeArmond SJ, Prusiner SB (2003) Perspectives on prion biology, prion disease pathogenesis, and pharmacologic approaches to treatment. Clin Lab Med 23:1–41PubMedCrossRefGoogle Scholar
  16. Dehle FC, Ecroyd H, Musgrave IF, Carver JA (2010) alphaB-Crystallin inhibits the cell toxicity associated with amyloid fibril formation by kappa-casein and the amyloid-beta peptide. Cell Stress Chaperones 15:1013–1026PubMedCrossRefPubMedCentralGoogle Scholar
  17. Deng HX, Hentati A, Tainer JA, Iqbal Z, Cayabyab A, Hung WY, Getzoff ED, Hu P, Herzfeldt B, Roos RP et al (1993) Amyotrophic lateral sclerosis and structural defects in Cu, Zn superoxide dismutase. Science 261:1047–1051PubMedCrossRefGoogle Scholar
  18. Der Perng M, Su M, Wen SF, Li R, Gibbon T, Prescott AR, Brenner M, Quinlan RA (2006) The Alexander disease-causing glial fibrillary acidic protein mutant, R416W, accumulates into Rosenthal fibers by a pathway that involves filament aggregation and the association of alpha B-crystallin and HSP27. Am J Hum Genet 79:197–213CrossRefPubMedCentralGoogle Scholar
  19. Dickson DW, Yen SH, Suzuki KI, Davies P, Garcia JH, Hirano A (1986) Ballooned neurons in select neurodegenerative diseases contain phosphorylated neurofilament epitopes. Acta Neuropathol 71:216–223PubMedCrossRefGoogle Scholar
  20. Ecroyd H, Carver JA (2009) Crystallin proteins and amyloid fibrils. Cell Mol Life Sci 66:62–81PubMedCrossRefGoogle Scholar
  21. Fukushima K, Mizuno Y, Takatama M, Okamoto K (2006) Increased neuronal expression of alpha B-crystallin in human olivary hypertrophy. Neuropathology 26:196–200PubMedCrossRefGoogle Scholar
  22. Goldbaum O, Richter-Landsberg C (2001) Stress proteins in oligodendrocytes: differential effects of heat shock and oxidative stress. J Neurochem 78:1233–1242PubMedCrossRefGoogle Scholar
  23. Hagemann TL, Boelens WC, Wawrousek EF, Messing A (2009) Suppression of GFAP toxicity by alphaB-crystallin in mouse models of Alexander disease. Hum Mol Genet 18:1190–1199PubMedCrossRefPubMedCentralGoogle Scholar
  24. Head MW, Corbin E, Goldman JE (1993) Overexpression and abnormal modification of the stress proteins alpha B-crystallin and HSP27 in Alexander disease. Am J Pathol 143:1743–1753PubMedPubMedCentralGoogle Scholar
  25. Head MW, Corbin E, Goldman JE (1994) Coordinate and independent regulation of alpha B-crystallin and hsp27 expression in response to physiological stress. J Cell Physiol 159:41–50PubMedCrossRefGoogle Scholar
  26. Head MW, Hurwitz L, Goldman JE (1996) Transcription regulation of alpha B-crystallin in astrocytes: analysis of HSF and AP1 activation by different types of physiological stress. J Cell Sci 109(Pt 5):1029–1039PubMedGoogle Scholar
  27. Ito H, Okamoto K, Nakayama H, Isobe T, Kato K (1997) Phosphorylation of alphaB-crystallin in response to various types of stress. J Biol Chem 272:29934–29941PubMedCrossRefGoogle Scholar
  28. Iwaki T, Kume-Iwaki A, Liem RK, Goldman JE (1989) Alpha B-crystallin is expressed in non-lenticular tissues and accumulates in Alexander’s disease brain. Cell 57:71–78PubMedCrossRefGoogle Scholar
  29. Iwaki T, Kume-Iwaki A, Goldman JE (1990) Cellular distribution of alpha B-crystallin in non-lenticular tissues. J Histochem Cytochem 38:31–39PubMedCrossRefGoogle Scholar
  30. Iwaki T, Wisniewski T, Iwaki A, Corbin E, Tomokane N, Tateishi J, Goldman JE (1992) Accumulation of alpha B-crystallin in central nervous system glia and neurons in pathologic conditions. Am J Pathol 140:345–356PubMedPubMedCentralGoogle Scholar
  31. Iwaki T, Iwaki A, Tateishi J, Sakaki Y, Goldman JE (1993) Alpha B-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 143:487–495PubMedPubMedCentralGoogle Scholar
  32. Iwaki T, Iwaki A, Tateishi J, Goldman JE (1994) Sense and antisense modification of glial alpha B-crystallin production results in alterations of stress fiber formation and thermoresistance. J Cell Biol 125:1385–1393PubMedCrossRefGoogle Scholar
  33. Iwaki T, Iwaki A, Fukumaki Y, Tateishi J (1995) Alpha B-crystallin in C6 glioma cells supports their survival in elevated extracellular K+: the implication of a protective role of alpha B-crystallin accumulation in reactive glia. Brain Res 673:47–52PubMedCrossRefGoogle Scholar
  34. Jankovic J (2008) Parkinson’s disease: clinical features and diagnosis. J Neurol Neurosurg Psychiatry 79:368–376PubMedCrossRefGoogle Scholar
  35. Jellinger KA (2000) Cell death mechanisms in Parkinson’s disease. J Neural Transm 107:1–29PubMedCrossRefGoogle Scholar
  36. Kappe G, Franck E, Verschuure P, Boelens WC, Leunissen JA, de Jong WW (2003) The human genome encodes 10 alpha-crystallin-related small heat shock proteins: HspB1-10. Cell Stress Chaperones 8:53–61PubMedCrossRefPubMedCentralGoogle Scholar
  37. Kappe G, Boelens WC, de Jong WW (2010) Why proteins without an alpha-crystallin domain should not be included in the human small heat shock protein family HSPB. Cell Stress Chaperones 15:457–461PubMedCrossRefPubMedCentralGoogle Scholar
  38. Kato K, Shinohara H, Kurobe N, Inaguma Y, Shimizu K, Ohshima K (1991) Tissue distribution and developmental profiles of immunoreactive alpha B crystallin in the rat determined with a sensitive immunoassay system. Biochim Biophys Acta 1074:201–208PubMedCrossRefGoogle Scholar
  39. Kato S, Hirano A, Umahara T, Kato M, Herz F, Ohama E (1992a) Comparative immunohistochemical study on the expression of alpha B crystallin, ubiquitin and stress-response protein 27 in ballooned neurons in various disorders. Neuropathol Appl Neurobiol 18:335–340PubMedCrossRefGoogle Scholar
  40. Kato S, Hirano A, Umahara T, Llena JF, Herz F, Ohama E (1992b) Ultrastructural and immunohistochemical studies on ballooned cortical neurons in Creutzfeldt-Jakob disease: expression of alpha B-crystallin, ubiquitin and stress-response protein 27. Acta Neuropathol 84:443–448PubMedGoogle Scholar
  41. Kato K, Goto S, Hasegawa K, Inaguma Y (1993) Coinduction of two low-molecular-weight stress proteins, alpha B crystallin and HSP28, by heat or arsenite stress in human glioma cells. J Biochem 114:640–647PubMedGoogle Scholar
  42. Kato K, Inaguma Y, Ito H, Iida K, Iwamoto I, Kamei K, Ochi N, Ohta H, Kishikawa M (2001) Ser-59 is the major phosphorylation site in alphaB-crystallin accumulated in the brains of patients with Alexander’s disease. J Neurochem 76:730–736PubMedCrossRefGoogle Scholar
  43. Ke K, Li L, Rui Y, Zheng H, Tan X, Xu W, Cao J, Xu J, Cui G, Xu G, Cao M (2013) Increased expression of small heat shock protein alphaB-crystallin after intracerebral hemorrhage in adult rats. J Mol Neurosci 51:159–169PubMedCrossRefGoogle Scholar
  44. Kertesz A, Hillis A, Munoz DG (2003) Frontotemporal degeneration, pick’s disease, pick complex, and ravel. Ann Neurol 54(Suppl 5):S1–S2PubMedCrossRefGoogle Scholar
  45. Kim JY, Song SH, Kim HN, Kim DW, Sohn HJ, Lee EY, Cho SS, Seo JH (2012) alpha b-crystallin is expressed in myelinating oligodendrocytes of the developing and adult avian retina. Neurochem Res 37:2135–2142PubMedCrossRefGoogle Scholar
  46. Kirbach BB, Golenhofen N (2011) Differential expression and induction of small heat shock proteins in rat brain and cultured hippocampal neurons. J Neurosci Res 89:162–175PubMedCrossRefGoogle Scholar
  47. Kitagawa K (2012) Ischemic tolerance in the brain: endogenous adaptive machinery against ischemic stress. J Neurosci Res 90:1043–1054PubMedCrossRefGoogle Scholar
  48. Kitagawa K, Matsumoto M, Tagaya M, Hata R, Ueda H, Niinobe M, Handa N, Fukunaga R, Kimura K, Mikoshiba K et al (1990) ‘Ischemic tolerance’ phenomenon found in the brain. Brain Res 528:21–24PubMedCrossRefGoogle Scholar
  49. Lee VM, Goedert M, Trojanowski JQ (2001) Neurodegenerative tauopathies. Annu Rev Neurosci 24:1121–1159PubMedCrossRefGoogle Scholar
  50. Li R, Reiser G (2011) Phosphorylation of Ser45 and Ser59 of alphaB-crystallin and p38/extracellular regulated kinase activity determine alphaB-crystallin-mediated protection of rat brain astrocytes from C2-ceramide- and staurosporine-induced cell death. J Neurochem 118:354–364PubMedCrossRefGoogle Scholar
  51. Li R, Johnson AB, Salomons G, Goldman JE, Naidu S, Quinlan R, Cree B, Ruyle SZ, Banwell B, D’Hooghe M, Siebert JR, Rolf CM, Cox H, Reddy A, Gutierrez-Solana LG, Collins A, Weller RO, Messing A, van der Knaap MS, Brenner M (2005) Glial fibrillary acidic protein mutations in infantile, juvenile, and adult forms of Alexander disease. Ann Neurol 57:310–326PubMedCrossRefGoogle Scholar
  52. Lowe J, Errington DR, Lennox G, Pike I, Spendlove I, Landon M, Mayer RJ (1992) Ballooned neurons in several neurodegenerative diseases and stroke contain alpha B crystallin. Neuropathol Appl Neurobiol 18:341–350PubMedCrossRefGoogle Scholar
  53. Mao JJ, Katayama S, Watanabe C, Harada Y, Noda K, Yamamura Y, Nakamura S (2001) The relationship between alphaB-crystallin and neurofibrillary tangles in Alzheimer’s disease. Neuropathol Appl Neurobiol 27:180–188PubMedCrossRefGoogle Scholar
  54. Minami M, Mizutani T, Kawanishi R, Suzuki Y, Mori H (2003) Neuronal expression of alphaB crystallin in cerebral infarction. Acta Neuropathol 105:549–554PubMedGoogle Scholar
  55. Moncayo J, de Freitas GR, Bogousslavsky J, Altieri M, van Melle G (2000) Do transient ischemic attacks have a neuroprotective effect? Neurology 54:2089–2094PubMedCrossRefGoogle Scholar
  56. Mori H, Oda M (1997) Ballooned neurons in cortocobasal degeneneration and progressive supranuclear palsy. Neuropathology 17:248–252CrossRefGoogle Scholar
  57. Morrison LE, Hoover HE, Thuerauf DJ, Glembotski CC (2003) Mimicking phosphorylation of alphaB-crystallin on serine-59 is necessary and sufficient to provide maximal protection of cardiac myocytes from apoptosis. Circ Res 92:203–211PubMedCrossRefGoogle Scholar
  58. Muchowski PJ, Ramsden R, Nguyen Q, Arnett EE, Greiling TM, Anderson SK, Clark JI (2008) Noninvasive measurement of protein aggregation by mutant huntingtin fragments or alpha-synuclein in the lens. J Biol Chem 283:6330–6336PubMedCrossRefPubMedCentralGoogle Scholar
  59. Nicholl ID, Quinlan RA (1994) Chaperone activity of alpha-crystallins modulates intermediate filament assembly. EMBO J 13:945–953PubMedPubMedCentralGoogle Scholar
  60. Obrenovitch TP (2008) Molecular physiology of preconditioning-induced brain tolerance to ischemia. Physiol Rev 88:211–247PubMedCrossRefGoogle Scholar
  61. Ousman SS, Tomooka BH, van Noort JM, Wawrousek EF, O’Connor KC, Hafler DA, Sobel RA, Robinson WH, Steinman L (2007) Protective and therapeutic role for alphaB-crystallin in autoimmune demyelination. Nature 448:474–479PubMedCrossRefGoogle Scholar
  62. Palminiello S, Jarzabek K, Kaur K, Walus M, Rabe A, Albertini G, Golabek AA, Kida E (2009) Upregulation of phosphorylated alphaB-crystallin in the brain of children and young adults with Down syndrome. Brain Res 1268:162–173PubMedCrossRefGoogle Scholar
  63. Piao CS, Kim SW, Kim JB, Lee JK (2005) Co-induction of alphaB-crystallin and MAPKAPK-2 in astrocytes in the penumbra after transient focal cerebral ischemia. Exp Brain Res 163:421–429PubMedCrossRefGoogle Scholar
  64. Prusiner SB (1998) Prions. Proc Natl Acad Sci U S A 95:13363–13383PubMedCrossRefPubMedCentralGoogle Scholar
  65. Quach QL, Metz LM, Thomas JC, Rothbard JB, Steinman L, Ousman SS (2013) CRYAB modulates the activation of CD4+ T cells from relapsing-remitting multiple sclerosis patients. Mult Scler 19:1867–1877PubMedCrossRefGoogle Scholar
  66. Quraishe S, Asuni A, Boelens WC, O’Connor V, Wyttenbach A (2008) Expression of the small heat shock protein family in the mouse CNS: differential anatomical and biochemical compartmentalization. Neuroscience 153:483–491PubMedCrossRefGoogle Scholar
  67. Rekas A, Adda CG, Andrew Aquilina J, Barnham KJ, Sunde M, Galatis D, Williamson NA, Masters CL, Anders RF, Robinson CV, Cappai R, Carver JA (2004) Interaction of the molecular chaperone alphaB-crystallin with alpha-synuclein: effects on amyloid fibril formation and chaperone activity. J Mol Biol 340:1167–1183PubMedCrossRefGoogle Scholar
  68. Renkawek K, de Jong WW, Merck KB, Frenken CW, van Workum FP, Bosman GJ (1992) alpha B-crystallin is present in reactive glia in Creutzfeldt-Jakob disease. Acta Neuropathol 83:324–327PubMedCrossRefGoogle Scholar
  69. Renkawek K, Voorter CE, Bosman GJ, van Workum FP, de Jong WW (1994) Expression of alpha B-crystallin in Alzheimer’s disease. Acta Neuropathol 87:155–160PubMedCrossRefGoogle Scholar
  70. Renkawek K, Stege GJ, Bosman GJ (1999) Dementia, gliosis and expression of the small heat shock proteins hsp27 and alpha B-crystallin in Parkinson’s disease. Neuroreport 10:2273–2276PubMedCrossRefGoogle Scholar
  71. Robertson AL, Headey SJ, Saunders HM, Ecroyd H, Scanlon MJ, Carver JA, Bottomley SP (2010) Small heat-shock proteins interact with a flanking domain to suppress polyglutamine aggregation. Proc Natl Acad Sci U S A 107:10424–10429PubMedCrossRefPubMedCentralGoogle Scholar
  72. Rosen DR, Siddique T, Patterson D, Figlewicz DA, Sapp P, Hentati A, Donaldson D, Goto J, O’Regan JP, Deng HX et al (1993) Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 362:59–62PubMedCrossRefGoogle Scholar
  73. Schmidt T, Bartelt-Kirbach B, Golenhofen N (2012) Phosphorylation-dependent subcellular localization of the small heat shock proteins HspB1/Hsp25 and HspB5/alphaB-crystallin in cultured hippocampal neurons. Histochem Cell Biol 138:407–418PubMedCrossRefGoogle Scholar
  74. Selkoe DJ (2001) Alzheimer’s disease: genes, proteins, and therapy. Physiol Rev 81:741–766PubMedGoogle Scholar
  75. Shammas SL, Waudby CA, Wang S, Buell AK, Knowles TP, Ecroyd H, Welland ME, Carver JA, Dobson CM, Meehan S (2011) Binding of the molecular chaperone alphaB-crystallin to Abeta amyloid fibrils inhibits fibril elongation. Biophys J 101:1681–1689PubMedCrossRefPubMedCentralGoogle Scholar
  76. Shin JH, Kim SW, Lim CM, Jeong JY, Piao CS, Lee JK (2009) alphaB-crystallin suppresses oxidative stress-induced astrocyte apoptosis by inhibiting caspase-3 activation. Neurosci Res 64:355–361PubMedCrossRefGoogle Scholar
  77. 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 262:152–156PubMedCrossRefGoogle Scholar
  78. Sun Y, Makarava N, Lee CI, Laksanalamai P, Robb FT, Baskakov IV (2008) Conformational stability of PrP amyloid fibrils controls their smallest possible fragment size. J Mol Biol 376:1155–1167PubMedCrossRefPubMedCentralGoogle Scholar
  79. Tang G, Perng MD, Wilk S, Quinlan R, Goldman JE (2010) Oligomers of mutant glial fibrillary acidic protein (GFAP) Inhibit the proteasome system in Alexander disease astrocytes, and the small heat shock protein alphaB-crystallin reverses the inhibition. J Biol Chem 285:10527–10537PubMedCrossRefPubMedCentralGoogle Scholar
  80. Tolnay M, Probst A (2003) The neuropathological spectrum of neurodegenerative tauopathies. IUBMB Life 55:299–305PubMedCrossRefGoogle Scholar
  81. Tue NT, Shimaji K, Tanaka N, Yamaguchi M (2012) Effect of alphaB-crystallin on protein aggregation in Drosophila. J Biomed Biotechnol 2012:252049PubMedCrossRefPubMedCentralGoogle Scholar
  82. van Noort JM, van Sechel AC, Bajramovic JJ, el Ouagmiri M, Polman CH, Lassmann H, Ravid R (1995) The small heat-shock protein alpha B-crystallin as candidate autoantigen in multiple sclerosis. Nature 375:798–801PubMedCrossRefGoogle Scholar
  83. van Noort JM, Bsibsi M, Gerritsen WH, van der Valk P, Bajramovic JJ, Steinman L, Amor S (2010) Alphab-crystallin is a target for adaptive immune responses and a trigger of innate responses in preactive multiple sclerosis lesions. J Neuropathol Exp Neurol 69:694–703PubMedCrossRefGoogle Scholar
  84. van Noort JM, Bsibsi M, Nacken P, Gerritsen WH, Amor S (2012) The link between small heat shock proteins and the immune system. Int J Biochem Cell Biol 44:1670–1679PubMedCrossRefGoogle Scholar
  85. Vleminckx V, Van Damme P, Goffin K, Delye H, Van Den Bosch L, Robberecht W (2002) Upregulation of HSP27 in a transgenic model of ALS. J Neuropathol Exp Neurol 61:968–974PubMedGoogle Scholar
  86. Wang J, Slunt H, Gonzales V, Fromholt D, Coonfield M, Copeland NG, Jenkins NA, Borchelt DR (2003) Copper-binding-site-null SOD1 causes ALS in transgenic mice: aggregates of non-native SOD1 delineate a common feature. Hum Mol Genet 12:2753–2764PubMedCrossRefGoogle Scholar
  87. Wang C, Chou YK, Rich CM, Link JM, Afentoulis ME, van Noort JM, Wawrousek EF, Offner H, Vandenbark AA (2006) AlphaB-crystallin-reactive T cells from knockout mice are not encephalitogenic. J Neuroimmunol 176:51–62PubMedCrossRefGoogle Scholar
  88. Wang J, Martin E, Gonzales V, Borchelt DR, Lee MK (2008) Differential regulation of small heat shock proteins in transgenic mouse models of neurodegenerative diseases. Neurobiol Aging 29:586–597PubMedCrossRefPubMedCentralGoogle Scholar
  89. Wang K, Ren K, Yan YE, Wang H, Zhng BY, Liu Y, Dong XP, Zhang J (2013) Analysis of the expressions of alphaB-crystallin in the brain tissues of agent 263K-infected hamsters at terminal stage. Bing Du Xue Bao 29:192–196PubMedGoogle Scholar
  90. Waudby CA, Knowles TP, Devlin GL, Skepper JN, Ecroyd H, Carver JA, Welland ME, Christodoulou J, Dobson CM, Meehan S (2010) The interaction of alphaB-crystallin with mature alpha-synuclein amyloid fibrils inhibits their elongation. Biophys J 98:843–851PubMedCrossRefPubMedCentralGoogle Scholar
  91. 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 1089:67–78PubMedCrossRefGoogle Scholar
  92. 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 32:119–130PubMedCrossRefGoogle Scholar
  93. Wistow GJ, Piatigorsky J (1988) Lens crystallins: the evolution and expression of proteins for a highly specialized tissue. Annu Rev Biochem 57:479–504PubMedCrossRefGoogle Scholar
  94. Yerbury JJ, Gower D, Vanags L, Roberts K, Lee JA, Ecroyd H (2013) The small heat shock proteins alphaB-crystallin and Hsp27 suppress SOD1 aggregation in vitro. Cell Stress Chaperones 18:251–257PubMedCrossRefPubMedCentralGoogle Scholar
  95. Zabel C, Chamrad DC, Priller J, Woodman B, Meyer HE, Bates GP, Klose J (2002) Alterations in the mouse and human proteome caused by Huntington’s disease. Mol Cell Proteomics 1:366–375PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  1. 1.Institute of Anatomy and Cell BiologyUniversity of UlmUlmGermany

Personalised recommendations