Skip to main content

Advertisement

SpringerLink
Log in

HspB1 (Hsp 27) Expression and Neuroprotection in the Retina

  • Published:
Molecular Neurobiology Aims and scope Submit manuscript

Abstract

Heat shock proteins (Hsps) are highly conserved proteins that are induced in response to various physiological and environmental stressors. HspB1 (Hsp27) is a prominent member of the small Hsps family and is strongly induced during the stress response. Notably, HspB1 has powerful neuroprotective effects, increasing the survival of cells subjected to cytotoxic stimuli. This is especially relevant to the study of the retina, where cells are subject to death due to retinal disease and injury. While HspB1 shows constitutive expression in some areas of the mammalian retina, of particular interest is the upregulation of the protein in response to ischemia and oxidative stress, traumatic nerve injury, and elevated intraocular pressure and glaucoma. Several mechanisms have been proposed to account for the cytoprotective actions of HspB1, including its role as a molecular chaperone, a stabilizer of the cytoskeleton, and a regulator of apoptosis. This review will focus on the role of HspB1 in the retina, emphasizing effects on retinal ganglion cells, by analyzing the expression, induction by stressors, and mechanisms of its neuroprotective function. Finally, the potential of HspB1 as a clinical therapeutic will be examined.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Lindquist S, Craig EA (1988) The heat-shock proteins. Annu Rev Genet 22:631–677

    Article  CAS  PubMed  Google Scholar 

  2. Samali A, Orrenius S (1998) Heat shock proteins: regulators of stress response and apoptosis. Cell Stress Chaperones 3:228–236

    Article  CAS  PubMed  Google Scholar 

  3. Ehrnsperger M, Graber S, Gaestel M, Buchner J (1997) Binding of non-native protein to Hsp25 during heat shock creates a reservoir of folding intermediates for reactivation. EMBO J 16:221–229

    Article  CAS  PubMed  Google Scholar 

  4. Bova MP, McHaourab HS, Han Y, Fung BK (2000) Subunit exchange of small heat shock proteins. Analysis of oligomer formation of alphaA-crystallin and Hsp27 by fluorescence resonance energy transfer and site-directed truncations. J Biol Chem 275:1035–1042

    Article  CAS  PubMed  Google Scholar 

  5. Rogalla T, Ehrnsperger M, Preville X, Kotlyarov A, Lutsch G, Ducasse C, Paul C, Wieske M, Arrigo AP, Buchner J, Gaestel M (1999) Regulation of Hsp27 oligomerization, chaperone function, and protective activity against oxidative stress/tumor necrosis factor alpha by phosphorylation. J Biol Chem 274:18947–18956

    Article  CAS  PubMed  Google Scholar 

  6. Kato K, Hasegawa K, Goto S, Inaguma Y (1994) Dissociation as a result of phosphorylation of an aggregated form of the small stress protein, hsp27. J Biol Chem 269:11274–11278

    CAS  PubMed  Google Scholar 

  7. Kato K, Ito H, Iwamoto I, Lida K, Inaguma Y (2001) Protein kinase inhibitors can suppress stress-induced dissociation of Hsp27. Cell Stress Chaperones 6:16–20

    Article  CAS  PubMed  Google Scholar 

  8. Kostenko S, Moens U (2009) Heat shock protein 27 phosphorylation: kinases, phosphatases, functions and pathology. Cell Mol Life Sci 66:3289–3307

    Article  CAS  PubMed  Google Scholar 

  9. Landry J, Lambert H, Zhou M, Lavoie JN, Hickey E, Weber LA, Anderson CW (1992) Human HSP27 is phosphorylated at serines 78 and 82 by heat shock and mitogen-activated kinases that recognize the same amino acid motif as S6 kinase II. J Biol Chem 267:794–803

    CAS  PubMed  Google Scholar 

  10. Stokoe D, Engel K, Campbell DG, Cohen P, Gaestel M (1992) Identification of MAPKAP kinase 2 as a major enzyme responsible for the phosphorylation of the small mammalian heat shock proteins. FEBS Lett 313:307–313

    Article  CAS  PubMed  Google Scholar 

  11. Gaestel M, Schroder W, Benndorf R, Lippmann C, Buchner K, Hucho F, Erdmann VA, Bielka H (1991) Identification of the phosphorylation sites of the murine small heat shock protein hsp25. J Biol Chem 266:14721–14724

    CAS  PubMed  Google Scholar 

  12. Hawkes EL, Krueger-Naug AM, Nickerson PE, Myers TL, Currie RW, Clarke DB (2004) Expression of Hsp27 in retinal ganglion cells of the rat during postnatal development. J Comp Neurol 478:143–148

    Article  CAS  PubMed  Google Scholar 

  13. Lee J, Kim H, Lee JM, Shin T (2006) Immunohistochemical localization of heat shock protein 27 in the retina of pigs. Neurosci Lett 406:227–231

    Article  CAS  PubMed  Google Scholar 

  14. Dean DO, Tytell M (2001) Hsp25 and -90 immunoreactivity in the normal rat eye. Invest Ophthalmol Vis Sci 42:3031–3040

    CAS  PubMed  Google Scholar 

  15. Strunnikova N, Baffi J, Gonzalez A, Silk W, Cousins SW, Csaky KG (2001) Regulated heat shock protein 27 expression in human retinal pigment epithelium. Invest Ophthalmol Vis Sci 42:2130–2138

    CAS  PubMed  Google Scholar 

  16. Kalesnykas G, Tuulos T, Uusitalo H, Jolkkonen J (2008) Neurodegeneration and cellular stress in the retina and optic nerve in rat cerebral ischemia and hypoperfusion models. Neuroscience 155:937–947

    Article  CAS  PubMed  Google Scholar 

  17. Li Y, Roth S, Laser M, Ma JX, Crosson CE (2003) Retinal preconditioning and the induction of heat-shock protein 27. Invest Ophthalmol Vis Sci 44:1299–1304

    Article  PubMed  Google Scholar 

  18. Krueger-Naug AM, Emsley JG, Myers TL, Currie RW, Clarke DB (2002) Injury to retinal ganglion cells induces expression of the small heat shock protein Hsp27 in the rat visual system. Neuroscience 110:653–665

    Article  CAS  PubMed  Google Scholar 

  19. Krueger-Naug AM, Emsley JG, Myers TL, Currie RW, Clarke DB (2003) Administration of brain-derived neurotrophic factor suppresses the expression of heat shock protein 27 in rat retinal ganglion cells following axotomy. Neuroscience 116:49–58

    Article  CAS  PubMed  Google Scholar 

  20. Tezel G, Hernandez R, Wax MB (2000) Immunostaining of heat shock proteins in the retina and optic nerve head of normal and glaucomatous eyes. Arch Ophthalmol 118:511–518

    CAS  PubMed  Google Scholar 

  21. Kalesnykas G, Niittykoski M, Rantala J, Miettinen R, Salminen A, Kaarniranta K, Uusitalo H (2007) The expression of heat shock protein 27 in retinal ganglion and glial cells in a rat glaucoma model. Neuroscience 150:692–704

    Article  CAS  PubMed  Google Scholar 

  22. Salvador-Silva M, Ricard CS, Agapova OA, Yang P, Hernandez MR (2001) Expression of small heat shock proteins and intermediate filaments in the human optic nerve head astrocytes exposed to elevated hydrostatic pressure in vitro. J Neurosci Res 66:59–73

    Article  CAS  PubMed  Google Scholar 

  23. Whitlock NA, Agarwal N, Ma JX, Crosson CE (2005) Hsp27 upregulation by HIF-1 signaling offers protection against retinal ischemia in rats. Invest Ophthalmol Vis Sci 46:1092–1098

    Article  PubMed  Google Scholar 

  24. Yu AL, Fuchshofer R, Birke M, Kampik A, Bloemendal H, Welge-Lussen U (2008) Oxidative stress and TGF-beta2 increase heat shock protein 27 expression in human optic nerve head astrocytes. Invest Ophthalmol Vis Sci 49:5403–5411

    Article  PubMed  Google Scholar 

  25. Huang W, Fileta JB, Filippopoulos T, Ray A, Dobberfuhl A, Grosskreutz CL (2007) Hsp27 phosphorylation in experimental glaucoma. Invest Ophthalmol Vis Sci 48:4129–4135

    Article  PubMed  Google Scholar 

  26. Muller A, Pietri S, Villain M, Frejaville C, Bonne C, Culcas M (1997) Free radicals in rabbit retina under ocular hyperpressure and functional consequences. Exp Eye Res 64:637–643

    Article  CAS  PubMed  Google Scholar 

  27. Olney JW (1982) The toxic effects of glutamate and related compounds in the retina and the brain. Retina 2:341–359

    Article  CAS  PubMed  Google Scholar 

  28. Sucher NJ, Wong LA, Lipton SA (1990) Redox modulation of NMDA receptor-mediated Ca2+ flux in mammalian central neurons. Neuroreport 1:29–32

    Article  CAS  PubMed  Google Scholar 

  29. Whitlock NA, Lindsey K, Agarwal N, Crosson CE, Ma JX (2005) Heat shock protein 27 delays Ca2+-induced cell death in a caspase-dependent and -independent manner in rat retinal ganglion cells. Invest Ophthalmol Vis Sci 46:1085–1091

    Article  PubMed  Google Scholar 

  30. Yokoyama A, Oshitari T, Negishi H, Dezawa M, Mizota A, Adachi-Usami E (2001) Protection of retinal ganglion cells from ischemia–reperfusion injury by electrically applied Hsp27. Invest Ophthalmol Vis Sci 42:3283–3286

    CAS  PubMed  Google Scholar 

  31. Berkelaar M, Clarke DB, Wang YC, Bray GM, Aguayo AJ (1994) Axotomy results in delayed death and apoptosis of retinal ganglion cells in adult rats. J Neurosci 14:4368–4374

    CAS  PubMed  Google Scholar 

  32. Robinson GA (1994) Immediate early gene expression in axotomized and regenerating retinal ganglion cells of the adult rat. Brain Res Mol Brain Res 24:43–54

    Article  CAS  PubMed  Google Scholar 

  33. Isenmann S, Engel S, Gillardon F, Bahr M (1999) Bax antisense oligonucleotides reduce axotomy-induced retinal ganglion cell death in vivo by reduction of Bax protein expression. Cell Death Differ 6:673–682

    Article  CAS  PubMed  Google Scholar 

  34. Kermer P, Klocker N, Labes M, Thomsen S, Srinivasan A, Bahr M (1999) Activation of caspase-3 in axotomized rat retinal ganglion cells in vivo. FEBS Lett 453:361–364

    Article  CAS  PubMed  Google Scholar 

  35. Hebb MO, Myers TL, Clarke DB (2006) Enhanced expression of heat shock protein 27 is correlated with axonal regeneration in mature retinal ganglion cells. Brain Res 1073–1074:146–150

    Article  PubMed  Google Scholar 

  36. Cartwright MJ, Grajewski AL, Friedberg ML, Anderson DR, Richards DW (1992) Immune-related disease and normal-tension glaucoma. A case–control study. Arch Ophthalmol 110:500–502

    CAS  PubMed  Google Scholar 

  37. Wax MB, Barrett DA, Pestronk A (1994) Increased incidence of paraproteinemia and autoantibodies in patients with normal-pressure glaucoma. Am J Ophthalmol 117:561–568

    CAS  PubMed  Google Scholar 

  38. Tezel G, Seigel GM, Wax MB (1998) Autoantibodies to small heat shock proteins in glaucoma. Invest Ophthalmol Vis Sci 39:2277–2287

    CAS  PubMed  Google Scholar 

  39. Wax MB, Tezel G, Kawase K, Kitazawa Y (2001) Serum autoantibodies to heat shock proteins in glaucoma patients from Japan and the United States. Ophthalmology 108:296–302

    Article  CAS  PubMed  Google Scholar 

  40. Wax MB, Tezel G, Yang J, Peng G, Patil RV, Agarwal N, Sappington RM, Calkins DJ (2008) Induced autoimmunity to heat shock proteins elicits glaucomatous loss of retinal ganglion cell neurons via activated T-cell-derived fas-ligand. J Neurosci 28:12085–12096

    Article  CAS  PubMed  Google Scholar 

  41. Jakob U, Gaestel M, Engel K, Buchner J (1993) Small heat shock proteins are molecular chaperones. J Biol Chem 268:1517–1520

    CAS  PubMed  Google Scholar 

  42. Ehrnsperger M, Gaestel M, Buchner J (2000) Analysis of chaperone properties of small Hsp’s. Methods Mol Biol 99:421–429

    CAS  PubMed  Google Scholar 

  43. Nollen EA, Brunsting JF, Roelofsen H, Weber LA, Kampinga HH (1999) In vivo chaperone activity of heat shock protein 70 and thermotolerance. Mol Cell Biol 19:2069–2079

    CAS  PubMed  Google Scholar 

  44. Soldatenkov VA, Dritschilo A (1997) Apoptosis of Ewing’s sarcoma cells is accompanied by accumulation of ubiquitinated proteins. Cancer Res 57:3881–3885

    CAS  PubMed  Google Scholar 

  45. Liang P, MacRae TH (1997) Molecular chaperones and the cytoskeleton. J Cell Sci 110(Pt 13):1431–1440

    CAS  PubMed  Google Scholar 

  46. Lavoie JN, Hickey E, Weber LA, Landry J (1993) Modulation of actin microfilament dynamics and fluid phase pinocytosis by phosphorylation of heat shock protein 27. J Biol Chem 268:24210–24214

    CAS  PubMed  Google Scholar 

  47. Huot J, Lambert H, Lavoie JN, Guimond A, Houle F, Landry J (1995) Characterization of 45-kDa/54-kDa HSP27 kinase, a stress-sensitive kinase which may activate the phosphorylation-dependent protective function of mammalian 27-kDa heat-shock protein HSP27. Eur J Biochem 227:416–427

    Article  CAS  PubMed  Google Scholar 

  48. Guay J, Lambert H, Gingras-Breton G, Lavoie JN, Huot J, Landry J (1997) Regulation of actin filament dynamics by p38 map kinase-mediated phosphorylation of heat shock protein 27. J Cell Sci 110(Pt 3):357–368

    CAS  PubMed  Google Scholar 

  49. Lavoie JN, Lambert H, Hickey E, Weber LA, Landry J (1995) Modulation of cellular thermoresistance and actin filament stability accompanies phosphorylation-induced changes in the oligomeric structure of heat shock protein 27. Mol Cell Biol 15:505–516

    CAS  PubMed  Google Scholar 

  50. Pivovarova AV, Chebotareva NA, Chernik IS, Gusev NB, Levitsky DI (2007) Small heat shock protein Hsp27 prevents heat-induced aggregation of F-actin by forming soluble complexes with denatured actin. FEBS J 274:5937–5948

    Article  CAS  PubMed  Google Scholar 

  51. Benndorf R, Hayess K, Ryazantsev S, Wieske M, Behlke J, Lutsch G (1994) Phosphorylation and supramolecular organization of murine small heat shock protein HSP25 abolish its actin polymerization-inhibiting activity. J Biol Chem 269:20780–20784

    CAS  PubMed  Google Scholar 

  52. Miron T, Vancompernolle K, Vandekerckhove J, Wilchek M, Geiger B (1991) A 25-kD inhibitor of actin polymerization is a low molecular mass heat shock protein. J Cell Biol 114:255–261

    Article  CAS  PubMed  Google Scholar 

  53. Wieske M, Benndorf R, Behlke J, Dolling R, Grelle G, Bielka H, Lutsch G (2001) Defined sequence segments of the small heat shock proteins HSP25 and alphaB-crystallin inhibit actin polymerization. Eur J Biochem 268:2083–2090

    Article  CAS  PubMed  Google Scholar 

  54. Tezel G, Wax MB (2000) The mechanisms of hsp27 antibody-mediated apoptosis in retinal neuronal cells. J Neurosci 20:3552–3562

    CAS  PubMed  Google Scholar 

  55. Floyd RA (1990) Role of oxygen free radicals in carcinogenesis and brain ischemia. FASEB J 4:2587–2597

    CAS  PubMed  Google Scholar 

  56. Mehlen P, Kretz-Remy C, Preville X, Arrigo AP (1996) Human hsp27, Drosophila hsp27 and human alphaB-crystallin expression-mediated increase in glutathione is essential for the protective activity of these proteins against TNFalpha-induced cell death. EMBO J 15:2695–2706

    CAS  PubMed  Google Scholar 

  57. Preville X, Salvemini F, Giraud S, Chaufour S, Paul C, Stepien G, Ursini MV, Arrigo AP (1999) Mammalian small stress proteins protect against oxidative stress through their ability to increase glucose-6-phosphate dehydrogenase activity and by maintaining optimal cellular detoxifying machinery. Exp Cell Res 247:61–78

    Article  CAS  PubMed  Google Scholar 

  58. Arrigo AP, Virot S, Chaufour S, Firdaus W, Kretz-Remy C, Diaz-Latoud C (2005) Hsp27 consolidates intracellular redox homeostasis by upholding glutathione in its reduced form and by decreasing iron intracellular levels. Antioxid Redox Signal 7:414–422

    Article  CAS  PubMed  Google Scholar 

  59. Mehlen P, Hickey E, Weber LA, Arrigo AP (1997) Large unphosphorylated aggregates as the active form of hsp27 which controls intracellular reactive oxygen species and glutathione levels and generates a protection against TNFalpha in NIH-3T3-ras cells. Biochem Biophys Res Commun 241:187–192

    Article  CAS  PubMed  Google Scholar 

  60. Concannon CG, Gorman AM, Samali A (2003) On the role of Hsp27 in regulating apoptosis. Apoptosis 8:61–70

    Article  CAS  PubMed  Google Scholar 

  61. Li H, Zhu H, Xu CJ, Yuan J (1998) Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94:491–501

    Article  CAS  PubMed  Google Scholar 

  62. Luo X, Budihardjo I, Zou H, Slaughter C, Wang X (1998) Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 94:481–490

    Article  CAS  PubMed  Google Scholar 

  63. Ashkenazi A, Dixit VM (1998) Death receptors: signaling and modulation. Science 281:1305–1308

    Article  CAS  PubMed  Google Scholar 

  64. Charette SJ, Lavoie JN, Lambert H, Landry J (2000) Inhibition of Daxx-mediated apoptosis by heat shock protein 27. Mol Cell Biol 20:7602–7612

    Article  CAS  PubMed  Google Scholar 

  65. 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

    Article  CAS  PubMed  Google Scholar 

  66. Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M, Alnemri ES, Wang X (1997) Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91:479–489

    Article  CAS  PubMed  Google Scholar 

  67. Garrido C, Bruey JM, Fromentin A, Hammann A, Arrigo AP, Solary E (1999) HSP27 inhibits cytochrome c-dependent activation of procaspase-9. FASEB J 13:2061–2070

    CAS  PubMed  Google Scholar 

  68. Bruey JM, Ducasse C, Bonniaud P, Ravagnan L, Susin SA, Diaz-Latoud C, Gurbuxani S, Arrigo AP, Kroemer G, Solary E, Garrido C (2000) Hsp27 negatively regulates cell death by interacting with cytochrome c. Nat Cell Biol 2:645–652

    Article  CAS  PubMed  Google Scholar 

  69. Concannon CG, 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

    CAS  PubMed  Google Scholar 

  70. Samali A, Robertson JD, Peterson E, Manero F, van Zeijl L, Paul C, Cotgreave IA, Arrigo AP, Orrenius S (2001) Hsp27 protects mitochondria of thermotolerant cells against apoptotic stimuli. Cell Stress Chaperones 6:49–58

    Article  CAS  PubMed  Google Scholar 

  71. Pandey P, Farber R, Nakazawa A, Kumar S, Bharti A, Nalin C, Weichselbaum R, Kufe D, Kharbanda S (2000) Hsp27 functions as a negative regulator of cytochrome c-dependent activation of procaspase-3. Oncogene 19:1975–1981

    Article  CAS  PubMed  Google Scholar 

  72. Paul C, Manero F, Gonin S, Kretz-Remy C, Virot S, Arrigo AP (2002) Hsp27 as a negative regulator of cytochrome C release. Mol Cell Biol 22:816–834

    Article  CAS  PubMed  Google Scholar 

  73. Chauhan D, Li G, Hideshima T, Podar K, Mitsiades C, Mitsiades N, Catley L, Tai YT, Hayashi T, Shringarpure R, Burger R, Munshi N, Ohtake Y, Saxena S, Anderson KC (2003) Hsp27 inhibits release of mitochondrial protein Smac in multiple myeloma cells and confers dexamethasone resistance. Blood 102:3379–3386

    Article  CAS  PubMed  Google Scholar 

  74. Du C, Fang M, Li Y, Li L, Wang X (2000) Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell 102:33–42

    Article  CAS  PubMed  Google Scholar 

  75. Biggs WH 3rd, Meisenhelder J, Hunter T, Cavenee WK, Arden KC (1999) Protein kinase B/Akt-mediated phosphorylation promotes nuclear exclusion of the winged helix transcription factor FKHR1. Proc Natl Acad Sci U S A 96:7421–7426

    Article  CAS  PubMed  Google Scholar 

  76. Ozes ON, Mayo LD, Gustin JA, Pfeffer SR, Pfeffer LM, Donner DB (1999) NF-kappaB activation by tumour necrosis factor requires the Akt serine-threonine kinase. Nature 401:82–85

    Article  CAS  PubMed  Google Scholar 

  77. 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

    Article  CAS  PubMed  Google Scholar 

  78. Kikuchi M, Tenneti L, Lipton SA (2000) Role of p38 mitogen-activated protein kinase in axotomy-induced apoptosis of rat retinal ganglion cells. J Neurosci 20:5037–5044

    CAS  PubMed  Google Scholar 

  79. Paul C, Simon S, Gibert B, Virot S, Manero F, Arrigo AP (2010) Dynamic processes that reflect anti-apoptotic strategies set up by HspB1 (Hsp27). Exp Cell Res 316:1535–1552

    Google Scholar 

  80. Quigley HA, Broman AT (2006) The number of people with glaucoma worldwide in 2010 and 2020. Br J Ophthalmol 90:262–267

    Article  CAS  PubMed  Google Scholar 

  81. Kuehn MH, Fingert JH, Kwon YH (2005) Retinal ganglion cell death in glaucoma: mechanisms and neuroprotective strategies. Ophthalmol Clin North Am 18:383–395, vi

    Article  PubMed  Google Scholar 

  82. Wagstaff MJ, Collaco-Moraes Y, Smith J, de Belleroche JS, Coffin RS, Latchman DS (1999) Protection of neuronal cells from apoptosis by Hsp27 delivered with a herpes simplex virus-based vector. J Biol Chem 274:5061–5069

    Article  CAS  PubMed  Google Scholar 

  83. Badin RA, Lythgoe MF, van der Weerd L, Thomas DL, Gadian DG, Latchman DS (2006) Neuroprotective effects of virally delivered HSPs in experimental stroke. J Cereb Blood Flow Metab 26:371–381

    Article  CAS  PubMed  Google Scholar 

  84. 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

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Amanda O’Reilly held a Natural Sciences and Engineering Research Council Undergraduate Student Research Award. Dr. Currie’s research is funded by the Heart and Stroke Foundation of New Brunswick. Dr. Clarke’s research is funded by the Natural Sciences and Engineering Research Council and the Canadian Institutes of Health Research in partnership with Nova Scotia Health Research Foundation.

Author information

Authors and Affiliations

  1. Department of Anatomy & Neurobiology, Faculty of Medicine, Dalhousie University, Halifax, NS, B3H 1X5, Canada

    Amanda M. O’Reilly, R. William Currie & David B. Clarke

  2. Division of Neurosurgery, Department of Surgery, Faculty of Medicine, Dalhousie University, Halifax, NS, B3H 1X5, Canada

    David B. Clarke

  3. Halifax Infirmary, 1796 Summer Street, Room 3807, Halifax, NS, B3H 3A7, Canada

    David B. Clarke

Authors
  1. Amanda M. O’Reilly
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. R. William Currie
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. David B. Clarke
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to David B. Clarke.

Rights and permissions

Reprints and permissions

About this article

Cite this article

O’Reilly, A.M., Currie, R.W. & Clarke, D.B. HspB1 (Hsp 27) Expression and Neuroprotection in the Retina. Mol Neurobiol 42, 124–132 (2010). https://doi.org/10.1007/s12035-010-8143-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12035-010-8143-3

Keywords

Search

Navigation