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Hsp90 Is a Pivotal Player in Retinal Disease and Cancer

  • Asmaa Aboelnour
  • Ahmed E. Noreldin
  • Islam M. SaadeldinEmail author
Chapter
Part of the Heat Shock Proteins book series (HESP, volume 19)

Abstract

Heat shock proteins (Hsp) are primarily protecting and maintaining cell viability during stressful conditions such as thermal and oxidative challenges through protein refolding and stabilization. Hsp play an essential role to confer eye protection from disease states particularly the diseases affecting the retina. Here, we summarize the Hsp function in normal retina, and their involvement in the pathogenesis of certain retinal diseases such cancer, glaucomatous retina, retinitis pigmentosa, and retinal neurodegeneration, as well as the age-related macular degeneration. This information would provide a better understanding of Hsp function and their involvement in ocular disease pathogenesis that could be a target for therapeutic purposes.

Keywords

Cancer Glaucomatous retina Hsp90 Inherited retinal disease Neurodegenerative disease Retina 

Abbreviations

AMD

Age-related macular degeneration

GFAP

Glial fibrillary acidic protein

Hsp

Heat shock proteins

IMPDH

Inosine-5′-monophosphate dehydrogenase

RP

Retinitis pigmentosa

RPE

Retinal pigment epithelium

Notes

Acknowledgements

We would like to thank the Deanship of Scientific Research and RSSU at King Saud University for their technical support.

References

  1. Aguila M, Bevilacqua D, McCulley C, Schwarz N, Athanasiou D, Kanuga N, Novoselov SS, Lange CA, Ali RR, Bainbridge JW, Gias C, Coffey PJ, Garriga P, Cheetham ME (2014) Hsp90 inhibition protects against inherited retinal degeneration. Hum Mol Genet 23:2164–2175PubMedCrossRefPubMedCentralGoogle Scholar
  2. Anckar J, Sistonen L (2007) Heat shock factor 1 as a coordinator of stress and developmental pathways. Adv Exp Med Biol 594:78–88PubMedCrossRefPubMedCentralGoogle Scholar
  3. Basso AD, Solit DB, Chiosis G, Giri B, Tsichlis P, Rosen N (2002) Akt forms an intracellular complex with heat shock protein 90 (Hsp90) and Cdc37 and is destabilized by inhibitors of Hsp90 function. J Biol Chem 277:39858–39866PubMedCrossRefPubMedCentralGoogle Scholar
  4. Bernstein SL, Borst DE, Neuder ME, Wong P (1996) Characterization of a human fovea cDNA library and regional differential gene expression in the human retina. Genomics 32:301–308PubMedCrossRefPubMedCentralGoogle Scholar
  5. Black JA, Waxman SG, Hildebrand C (1985) Axo-glial relations in the retina-optic nerve junction of the adult rat: freeze-fracture observations on axon membrane structure. J Neurocytol 14:887–907PubMedCrossRefPubMedCentralGoogle Scholar
  6. Bradke F, Dotti CG (1999) The role of local actin instability in axon formation. Science 283:1931–1934PubMedCrossRefPubMedCentralGoogle Scholar
  7. Brown IR (2007) Heat shock proteins and protection of the nervous system. Ann N Y Acad Sci 1113:147–158PubMedCrossRefPubMedCentralGoogle Scholar
  8. Calderwood SK, Khaleque MA, Sawyer DB, Ciocca DR (2006) Heat shock proteins in cancer: chaperones of tumorigenesis. Trends Biochem Sci 31:164–172PubMedCrossRefPubMedCentralGoogle Scholar
  9. Chatterjee S, Burns TF (2017) Targeting heat shock proteins in cancer: a promising therapeutic approach. Int J Mol Sci 18:1978PubMedCentralCrossRefGoogle Scholar
  10. Chatterjee S, Bhattacharya S, Socinski MA, Burns TF (2016) HSP90 inhibitors in lung cancer: promise still unfulfilled. Clin Adv Hematol Oncol 14:346–356PubMedPubMedCentralGoogle Scholar
  11. Chen G, Cao P, Goeddel DV (2002) TNF-induced recruitment and activation of the IKK complex require Cdc37 and Hsp90. Mol Cell 9:401–410PubMedCrossRefPubMedCentralGoogle Scholar
  12. Chen W, Zheng R, Baade PD, Zhang S, Zeng H, Bray F, Jemal A, Yu XQ, He J (2016) Cancer statistics in China, 2015. CA Cancer J Clin 66:115–132PubMedPubMedCentralCrossRefGoogle Scholar
  13. Chiosis G (2006) Targeting chaperones in transformed systems – a focus on Hsp90 and cancer. Expert Opin Ther Targets 10:37–50PubMedCrossRefPubMedCentralGoogle Scholar
  14. Chiosis G (2016) Heat shock proteins in disease–from molecular mechanisms to therapeutics. Curr Top Med Chem 16:2727PubMedPubMedCentralCrossRefGoogle Scholar
  15. Chuang J-Z, Vega C, Jun W, Sung C-H (2004) Structural and functional impairment of endocytic pathways by retinitis pigmentosa mutant rhodopsin-arrestin complexes. J Clin Invest 114:131–140PubMedPubMedCentralCrossRefGoogle Scholar
  16. Csermely P, Schnaider T, Soti C, Prohaszka Z, Nardai G (1998) The 90-kDa molecular chaperone family: structure, function, and clinical applications. A comprehensive review. Pharmacol Ther 79:129–168PubMedCrossRefPubMedCentralGoogle Scholar
  17. Czar MJ, Welsh MJ, Pratt WB (1996) Immunofluorescence localization of the 90-kDa heat-shock protein to cytoskeleton. Eur J Cell Biol 70:322–330PubMedPubMedCentralGoogle Scholar
  18. Da Silva JS, Dotti CG (2002) Breaking the neuronal sphere: regulation of the actin cytoskeleton in neuritogenesis. Nat Rev Neurosci 3:694PubMedCrossRefPubMedCentralGoogle Scholar
  19. Darimont BD (1999) The Hsp90 chaperone complex-a potential target for cancer therapy? World J Gastroenterol 5:195–198PubMedPubMedCentralCrossRefGoogle Scholar
  20. Dean DO, Tytell M (2001) Hsp25 and −90 immunoreactivity in the normal rat eye. Invest Ophthalmol Vis Sci 42:3031–3040PubMedPubMedCentralGoogle Scholar
  21. Dean DO, Kent CR, Tytell M (1999) Constitutive and inducible heat shock protein 70 immunoreactivity in the normal rat eye. Invest Ophthalmol Vis Sci 40:2952–2962PubMedPubMedCentralGoogle Scholar
  22. Decanini A, Nordgaard CL, Feng X, Ferrington DA, Olsen TW (2007) Changes in select redox proteins of the retinal pigment epithelium in age-related macular degeneration. Am J Ophthalmol 143:607–615PubMedPubMedCentralCrossRefGoogle Scholar
  23. Ellis RJ (2007) Protein misassembly. In: Csermely P, Vígh L (eds) Molecular aspects of the stress response: chaperones, membranes and networks. Springer New York, New York, pp 1–13Google Scholar
  24. Garcia-Carbonero R, Carnero A, Paz-Ares L (2013) Inhibition of HSP90 molecular chaperones: moving into the clinic. Lancet Oncol 14:e358–e369PubMedCrossRefPubMedCentralGoogle Scholar
  25. Garrido C, Brunet M, Didelot C, Zermati Y, Schmitt E, Kroemer G (2006) Heat shock proteins 27 and 70: anti-apoptotic proteins with tumorigenic properties. Cell Cycle 5:2592–2601PubMedCrossRefPubMedCentralGoogle Scholar
  26. Goedert M, Jakes R (2005) Mutations causing neurodegenerative tauopathies. Biochim Biophys Acta 1739:240–250PubMedCrossRefPubMedCentralGoogle Scholar
  27. Gyrd-Hansen M, Nylandsted J, Jäättelä M (2004) Heat shock protein 70 promotes cancer cell viability by safeguarding lysosomal integrity. Cell Cycle 3:1484–1485PubMedCrossRefPubMedCentralGoogle Scholar
  28. Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144:646–674CrossRefGoogle Scholar
  29. Harris H, Rubinsztein DC (2011) Control of autophagy as a therapy for neurodegenerative disease. Nat Rev Neurol 8:108–117PubMedCrossRefPubMedCentralGoogle Scholar
  30. He S, Zhang C, Shafi AA, Sequeira M, Acquaviva J, Friedland JC, Sang J, Smith DL, Weigel NL, Wada Y (2013) Potent activity of the Hsp90 inhibitor ganetespib in prostate cancer cells irrespective of androgen receptor status or variant receptor expression. Int J Oncol 42:35–43PubMedCrossRefPubMedCentralGoogle Scholar
  31. Honjo M, Tanihara H, Kido N, Inatani M, Okazaki K, Honda Y (2000) Expression of ciliary neurotrophic factor activated by retinal Muller cells in eyes with NMDA- and kainic acid-induced neuronal death. Invest Ophthalmol Vis Sci 41:552–560PubMedPubMedCentralGoogle Scholar
  32. Jäättelä M (1999) Escaping cell death: survival proteins in cancer. Exp Cell Res 248:30–43PubMedCrossRefPubMedCentralGoogle Scholar
  33. Jacobson C, Schnapp B, Banker GA (2006) A change in the selective translocation of the Kinesin-1 motor domain marks the initial specification of the axon. Neuron 49:797–804PubMedCrossRefPubMedCentralGoogle Scholar
  34. Jaiswal RK, Weissinger E, Kolch W, Landreth GE (1996) Nerve growth factor-mediated activation of the mitogen-activated protein (MAP) kinase cascade involves a signaling complex containing B-Raf and HSP90. J Biol Chem 271:23626–23629PubMedCrossRefPubMedCentralGoogle Scholar
  35. Jarrett SG, Boulton ME (2012) Consequences of oxidative stress in age-related macular degeneration. Mol Asp Med 33:399–417CrossRefGoogle Scholar
  36. Jego G, Hazoumé A, Seigneuric R, Garrido C (2013) Targeting heat shock proteins in cancer. Cancer Lett 332:275–285PubMedCrossRefPubMedCentralGoogle Scholar
  37. Jiang L, Liu X, Li B, He X, Jin Y, Li L, Gao F, Wang N (2008) Heat shock proteins and survivin: relationship and effects on proliferation index of retinoblastoma cells. Histol Histopathol 23:827–832PubMedPubMedCentralGoogle Scholar
  38. Johnson J, Corbisier R, Stensgard B, Toft D (1996) The involvement of p23, hsp90, and immunophilins in the assembly of progesterone receptor complexes. J Steroid Biochem Mol Biol 56:31–37PubMedCrossRefPubMedCentralGoogle Scholar
  39. Jolly C, Morimoto RI (2000) Role of the heat shock response and molecular chaperones in oncogenesis and cell death. J Natl Cancer Inst 92:1564–1572PubMedCrossRefPubMedCentralGoogle Scholar
  40. Jung T, Catalgol B, Grune T (2009) The proteasomal system. Mol Asp Med 30:191–296CrossRefGoogle Scholar
  41. Kaarniranta K, Sinha D, Blasiak J, Kauppinen A, Vereb Z, Salminen A, Boulton ME, Petrovski G (2013) Autophagy and heterophagy dysregulation leads to retinal pigment epithelium dysfunction and development of age-related macular degeneration. Autophagy 9:973–984PubMedPubMedCentralCrossRefGoogle Scholar
  42. Kanwar JR, Kamalapuram SK, Kanwar RK (2013) Survivin signaling in clinical oncology: a multifaceted dragon. Med Res Rev 33:765–789PubMedCrossRefPubMedCentralGoogle Scholar
  43. Kaplan KB, Li R (2012) A prescription for ‘stress’–the role of Hsp90 in genome stability and cellular adaptation. Trends Cell Biol 22:576–583PubMedPubMedCentralCrossRefGoogle Scholar
  44. Karagoz GE, Rudiger SG (2015) Hsp90 interaction with clients. Trends Biochem Sci 40:117–125PubMedCrossRefPubMedCentralGoogle Scholar
  45. Karunanithi S, Barclay JW, Robertson RM, Brown IR, Atwood HL (1999) Neuroprotection at Drosophila synapses conferred by prior heat shock. J Neurosci 19:4360PubMedPubMedCentralCrossRefGoogle Scholar
  46. Kauppinen A, Niskanen H, Suuronen T, Kinnunen K, Salminen A, Kaarniranta K (2012) Oxidative stress activates NLRP3 inflammasomes in ARPE-19 cells – implications for age-related macular degeneration (AMD). Immunol Lett 147:29–33PubMedCrossRefPubMedCentralGoogle Scholar
  47. Kiang JG, Tsokos GC (1998) Heat shock protein 70 kDa: molecular biology, biochemistry, and physiology. Pharmacol Ther 80:183–201PubMedCrossRefPubMedCentralGoogle Scholar
  48. Kimura E, Enns RE, Alcaraz JE, Arboleda J, Slamon DJ, Howell SB (1993) Correlation of the survival of ovarian cancer patients with mRNA expression of the 60-kD heat-shock protein HSP-60. J Clin Oncol Off J Am Soc Clin Oncol 11:891–898CrossRefGoogle Scholar
  49. Klettner A (2004) The induction of heat shock proteins as a potential strategy to treat neurodegenerative disorders. Drug News Perspect 17:299–306PubMedCrossRefPubMedCentralGoogle Scholar
  50. Kobayashi K, Kobayashi H, Ueda M, Honda Y (1998) Estrogen receptor expression in bovine and rat retinas. Invest Ophthalmol Vis Sci 39:2105–2110PubMedPubMedCentralGoogle Scholar
  51. Kojima M, Hoshimaru M, Aoki T, Takahashi JB, Ohtsuka T, Asahi M, Matsuura N, Kikuchi H (1996) Expression of heat shock proteins in the developing rat retina. Neurosci Lett 205:215–217PubMedCrossRefPubMedCentralGoogle Scholar
  52. Kosik KS, Shimura H (2005) Phosphorylated tau and the neurodegenerative foldopathies. Biochim Biophys Acta 1739:298–310PubMedCrossRefPubMedCentralGoogle Scholar
  53. Labbadia J, Cunliffe H, Weiss A, Katsyuba E, Sathasivam K, Seredenina T, Woodman B, Moussaoui S, Frentzel S, Luthi-Carter R, Paganetti P, Bates GP (2011) Altered chromatin architecture underlies progressive impairment of the heat shock response in mouse models of Huntington disease. J Clin Invest 121:3306–3319PubMedPubMedCentralCrossRefGoogle Scholar
  54. Lau LF, Schachter JB, Seymour PA, Sanner MA (2002) Tau protein phosphorylation as a therapeutic target in Alzheimer’s disease. Curr Top Med Chem 2:395–415PubMedCrossRefPubMedCentralGoogle Scholar
  55. Li J, Buchner J (2013) Structure, function and regulation of the hsp90 machinery. Biom J 36:106–117Google Scholar
  56. Li Y, Wang YS, Shen XF, Hui YN, Han J, Zhao W, Zhu J (2008) Alterations of activity and intracellular distribution of the 20S proteasome in ageing retinal pigment epithelial cells. Exp Gerontol 43:1114–1122PubMedCrossRefPubMedCentralGoogle Scholar
  57. Li Y, Zhang T, Schwartz SJ, Sun D (2009) New developments in Hsp90 inhibitors as anti-cancer therapeutics: mechanisms, clinical perspective and more potential. Drug Resist Updat 12:17–27PubMedPubMedCentralCrossRefGoogle Scholar
  58. Lin T-Y, Guo W, Long Q, Ma A, Liu Q, Zhang H, Huang Y, Chandrasekaran S, Pan C, Lam KS (2016) HSP90 inhibitor encapsulated photo-theranostic nanoparticles for synergistic combination cancer therapy. Theranostics 6:1324PubMedPubMedCentralCrossRefGoogle Scholar
  59. Lindquist S, Craig E (1988) The heat-shock proteins. Annu Rev Genet 22:631–677PubMedCrossRefPubMedCentralGoogle Scholar
  60. Luo W, Dou F, Rodina A, Chip S, Kim J, Zhao Q, Moulick K, Aguirre J, Wu N, Greengard P, Chiosis G (2007) Roles of heat-shock protein 90 in maintaining and facilitating the neurodegenerative phenotype in tauopathies. Proc Natl Acad Sci USA 104:9511–9516PubMedCrossRefPubMedCentralGoogle Scholar
  61. Luo W, Rodina A, Chiosis G (2008) Heat shock protein 90: translation from cancer to Alzheimer’s disease treatment? BMC Neurosci 9:S7–S7PubMedPubMedCentralCrossRefGoogle Scholar
  62. Martinon F (2008) Detection of immune danger signals by NALP3. J Leukoc Biol 83:507–511PubMedCrossRefPubMedCentralGoogle Scholar
  63. Mayor A, Martinon F, De Smedt T, Petrilli V, Tschopp J (2007) A crucial function of SGT1 and HSP90 in inflammasome activity links mammalian and plant innate immune responses. Nat Immunol 8:497–503PubMedCrossRefPubMedCentralGoogle Scholar
  64. Meli M, Pennati M, Curto M, Daidone MG, Plescia J, Toba S, Altieri DC, Zaffaroni N, Colombo G (2006) Small-molecule targeting of heat shock protein 90 chaperone function: rational identification of a new anticancer lead. J Med Chem 49:7721–7730PubMedCrossRefPubMedCentralGoogle Scholar
  65. Mendes HF, Cheetham ME (2008) Pharmacological manipulation of gain-of-function and dominant-negative mechanisms in rhodopsin retinitis pigmentosa. Hum Mol Genet 17:3043–3054PubMedCrossRefPubMedCentralGoogle Scholar
  66. Mimnaugh EG, Worland PJ, Whitesell L, Neckers LM (1995) Possible role for serine/threonine phosphorylation in the regulation of the heteroprotein complex between the hsp90 stress protein and the pp60v-src tyrosine kinase. J Biol Chem 270:28654–28659PubMedCrossRefPubMedCentralGoogle Scholar
  67. Mirshahi M, Nicolas C, Mirshahi A, Hecquet C, d’Hermies F, Faure JP, Agarwal MK (1996) The mineralocorticoid hormone receptor and action in the eye. Biochem Biophys Res Commun 219:150–156PubMedCrossRefPubMedCentralGoogle Scholar
  68. Miyata Y, Nakamoto H, Neckers L (2013) The therapeutic target Hsp90 and cancer hallmarks. Curr Pharm Des 19:347–365PubMedCrossRefPubMedCentralGoogle Scholar
  69. Moore SK, Kozak C, Robinson EA, Ullrich SJ, Appella E (1989) Murine 86- and 84-kDa heat shock proteins, cDNA sequences, chromosome assignments, and evolutionary origins. J Biol Chem 264:5343–5351PubMedPubMedCentralGoogle Scholar
  70. Muchowski PJ, Wacker JL (2005) Modulation of neurodegeneration by molecular chaperones. Nat Rev Neurosci 6:11–22PubMedCrossRefPubMedCentralGoogle Scholar
  71. Nathan DF, Lindquist S (1995) Mutational analysis of Hsp90 function: interactions with a steroid receptor and a protein kinase. Mol Cell Biol 15:3917–3925PubMedPubMedCentralCrossRefGoogle Scholar
  72. Nathan DF, Vos MH, Lindquist S (1997) In vivo functions of the Saccharomyces cerevisiae Hsp90 chaperone. Proc Natl Acad Sci USA 94:12949–12956PubMedCrossRefPubMedCentralGoogle Scholar
  73. Neckers L, Workman P (2012) Hsp90 molecular chaperone inhibitors: are we there yet? Clin Cancer Res 18:64–76PubMedPubMedCentralCrossRefGoogle Scholar
  74. Park JW, Moon C, Yun S, Kim SY, Bae YC, Chun M-H, Moon J-I (2007) Differential expression of heat shock protein mRNAs under in vivo glutathione depletion in the mouse retina. Neurosci Lett 413:260–264PubMedCrossRefPubMedCentralGoogle Scholar
  75. Parsell D, Lindquist S (1993) The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annu Rev Genet 27:437–496PubMedCrossRefPubMedCentralGoogle Scholar
  76. Pearl LH, Prodromou C, Workman P (2008) The Hsp90 molecular chaperone: an open and shut case for treatment. Biochem J 410:439–453PubMedCrossRefPubMedCentralGoogle Scholar
  77. Pratt WB (1997) The role of the hsp90-based chaperone system in signal transduction by nuclear receptors and receptors signaling via MAP kinase. Annu Rev Pharmacol Toxicol 37:297–326PubMedCrossRefPubMedCentralGoogle Scholar
  78. Pratt WB (1998) The hsp90-based chaperone system: involvement in signal transduction from a variety of hormone and growth factor receptors. Proc Soc Exp Biol Med 217:420–434PubMedCrossRefPubMedCentralGoogle Scholar
  79. Proia DA, Kaufmann GF (2015) Targeting heat-shock protein 90 (HSP90) as a complementary strategy to immune checkpoint blockade for cancer therapy. Cancer Immunol Res 3:583–589PubMedCrossRefPubMedCentralGoogle Scholar
  80. Qin S, Ni M, Wang X, Maurier-Mahe F, Shurland DL, Rodrigues GA (2011) Inhibition of RPE cell sterile inflammatory responses and endotoxin-induced uveitis by a cell-impermeable HSP90 inhibitor. Exp Eye Res 93:889–897PubMedCrossRefPubMedCentralGoogle Scholar
  81. Rui Z, Xiao-Yun G, Xing-Chuang X, You J, Ze-Jian H, Xiang F (2018) Progress in molecular chaperone regulation of heat shock protein 90 and cancer. Chin J Anal Chem 46:301–308CrossRefGoogle Scholar
  82. Rutherford SL, Lindquist S (1998) Hsp90 as a capacitor for morphological evolution. Nature 396:336PubMedCrossRefGoogle Scholar
  83. Saif M, Erlichman C, Dragovich T, Mendelson D, Toft D, Burrows F, Storgard C, Von Hoff D (2013) Open-label, dose-escalation, safety, pharmacokinetic, and pharmacodynamic study of intravenously administered CNF1010 (17-(allylamino)-17-demethoxygeldanamycin [17-AAG]) in patients with solid tumors. Cancer Chemother Pharmacol 71:1345–1355PubMedCrossRefPubMedCentralGoogle Scholar
  84. Sakai M, Sakai H, Nakamura Y, Fukuchi T, Sawaguchi S (2003) Immunolocalization of heat shock proteins in the retina of normal monkey eyes and monkey eyes with laser-induced glaucoma. Jpn J Ophthalmol 47:42–52PubMedCrossRefPubMedCentralGoogle Scholar
  85. Sanchez ER, Redmond T, Scherrer LC, Bresnick EH, Welsh MJ, Pratt WB (1988) Evidence that the 90-kilodalton heat shock protein is associated with tubulin-containing complexes in L cell cytosol and in intact PtK cells. Mol Endocrinol 2:756–760PubMedCrossRefPubMedCentralGoogle Scholar
  86. Santarosa M, Favaro D, Quaia M, Galligioni E (1997) Expression of heat shock protein 72 in renal cell carcinoma: possible role and prognostic implications in cancer patients. Eur J Cancer 33:873–877PubMedCrossRefPubMedCentralGoogle Scholar
  87. Sauvage F, Messaoudi S, Fattal E, Barratt G, Vergnaud-Gauduchon J (2017) Heat shock proteins and cancer: how can nanomedicine be harnessed? J Control Release 248:133–143PubMedCrossRefPubMedCentralGoogle Scholar
  88. Scheibel T, Buchner J (1998) The Hsp90 complex – a super-chaperone machine as a novel drug target. Biochem Pharmacol 56:675–682PubMedCrossRefPubMedCentralGoogle Scholar
  89. Schwamborn JC, Müller M, Becker AH, Püschel AW (2007) Retracted: ubiquitination of the GTPase Rap1B by the ubiquitin ligase Smurf2 is required for the establishment of neuronal polarity. EMBO J 26:1410–1422PubMedPubMedCentralCrossRefGoogle Scholar
  90. Shapley R, Perry VH (1986) Cat and monkey retinal ganglion cells and their visual functional roles. Trends Neurosci 9:229–235CrossRefGoogle Scholar
  91. Shi S-H, Jan LY, Jan Y-N (2003) Hippocampal neuronal polarity specified by spatially localized mPar3/mPar6 and PI 3-kinase activity. Cell 112:63–75PubMedCrossRefPubMedCentralGoogle Scholar
  92. Shi S-H, Cheng T, Jan LY, Jan Y-N (2004) APC and GSK-3β are involved in mPar3 targeting to the nascent axon and establishment of neuronal polarity. Curr Biol 14:2025–2032PubMedCrossRefPubMedCentralGoogle Scholar
  93. Singh A, Singh A, Sand JM, Bauer SJ, Hafeez BB, Meske L, Verma AK (2015) Topically applied Hsp90 inhibitor 17AAG inhibits UVR-induced cutaneous squamous cell carcinomas. J Invest Dermatol 135:1098–1107PubMedCrossRefPubMedCentralGoogle Scholar
  94. Sittler A, Lurz R, Lueder G, Priller J, Hayer-Hartl MK, Hartl FU, Lehrach H, Wanker EE (2001) Geldanamycin activates a heat shock response and inhibits huntingtin aggregation in a cell culture model of Huntington’s disease. Hum Mol Genet 10:1307–1315PubMedCrossRefPubMedCentralGoogle Scholar
  95. Sliutz G, Karlseder J, Tempfer C, Orel L, Holzer G, Simon MM (1996) Drug resistance against gemcitabine and topotecan mediated by constitutive hsp70 overexpression in vitro: implication of quercetin as sensitiser in chemotherapy. Br J Cancer 74:172–177PubMedPubMedCentralCrossRefGoogle Scholar
  96. Sudhakar J, Venkatesan N, Lakshmanan S, Khetan V, Krishnakumar S, Biswas J (2013) Hypoxic tumor microenvironment in advanced retinoblastoma. Pediatr Blood Cancer 60:1598–1601PubMedCrossRefPubMedCentralGoogle Scholar
  97. Taipale M, Jarosz DF, Lindquist S (2010) HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Nat Rev Mol Cell Biol 11:515–528PubMedCrossRefGoogle Scholar
  98. Taiyab A, Sreedhar AS, Rao CM (2009) Hsp90 inhibitors, GA and 17AAG, lead to ER stress-induced apoptosis in rat histiocytoma. Biochem Pharmacol 78:142–152PubMedCrossRefPubMedCentralGoogle Scholar
  99. Takayama S, Reed JC, Homma S (2003) Heat-shock proteins as regulators of apoptosis. Oncogene 22:9041–9047PubMedCrossRefPubMedCentralGoogle Scholar
  100. Tam LC, Kiang AS, Campbell M, Keaney J, Farrar GJ, Humphries MM, Kenna PF, Humphries P (2010) Prevention of autosomal dominant retinitis pigmentosa by systemic drug therapy targeting heat shock protein 90 (Hsp90). Hum Mol Genet 19:4421–4436PubMedPubMedCentralCrossRefGoogle Scholar
  101. Tanaka Y, Kobayashi K, Kita M, Kinoshita S, Imanishi J (1995) Messenger RNA expression of heat shock proteins (Hsp) during ocular development. Curr Eye Res 14:1125–1133PubMedCrossRefPubMedCentralGoogle Scholar
  102. Tanihara H, Hangai M, Sawaguchi S, Abe H, Kageyama M, Nakazawa F, Shirasawa E, Honda Y (1997) Up-regulation of glial fibrillary acidic protein in the retina of primate eyes with experimental glaucoma. Arch Ophthalmol 115:752–756PubMedCrossRefPubMedCentralGoogle Scholar
  103. Tapia M, Wandosell F, Garrido JJ (2010) Impaired function of HDAC6 slows down axonal growth and interferes with axon initial segment development. PLoS One 5:e12908PubMedPubMedCentralCrossRefGoogle Scholar
  104. Tarallo V, Hirano Y, Gelfand BD, Dridi S, Kerur N, Kim Y, Cho WG, Kaneko H, Fowler BJ, Bogdanovich S, Albuquerque RJ, Hauswirth WW, Chiodo VA, Kugel JF, Goodrich JA, Ponicsan SL, Chaudhuri G, Murphy MP, Dunaief JL, Ambati BK, Ogura Y, Yoo JW, Lee DK, Provost P, Hinton DR, Nunez G, Baffi JZ, Kleinman ME, Ambati J (2012) DICER1 loss and Alu RNA induce age-related macular degeneration via the NLRP3 inflammasome and MyD88. Cell 149:847–859PubMedPubMedCentralCrossRefGoogle Scholar
  105. Trabulo S, Cardoso A, Santos-Ferreira T, Cardoso A, Simoes S, Pedroso de Lima M (2011) Survivin silencing as a promising strategy to enhance the sensitivity of cancer cells to chemotherapeutic agents. Mol Pharm 8:1120–1131PubMedCrossRefPubMedCentralGoogle Scholar
  106. Tukaj S, Bieber K, Kleszczyński K, Witte M, Cames R, Kalies K, Zillikens D, Ludwig RJ, Fischer TW, Kasperkiewicz M (2017) Topically applied Hsp90 blocker 17AAG inhibits autoantibody-mediated blister-inducing cutaneous inflammation. J Investig Dermatol 137:341–349PubMedCrossRefPubMedCentralGoogle Scholar
  107. Vanden Berghe T, Kalai M, van Loo G, Declercq W, Vandenabeele P (2003) Disruption of HSP90 function reverts tumor necrosis factor-induced necrosis to apoptosis. J Biol Chem 278:5622–5629CrossRefGoogle Scholar
  108. Venkatesan N, Kanwar JR, Deepa PR, Navaneethakrishnan S, Joseph C, Krishnakumar S (2016) Targeting HSP90/Survivin using a cell permeable structure based peptido-mimetic shepherdin in retinoblastoma. Chem Biol Interact 252:141–149PubMedCrossRefPubMedCentralGoogle Scholar
  109. Wainberg ZA, Anghel A, Rogers AM, Desai AJ, Kalous O, Conklin D, Ayala R, O’Brien NA, Quadt C, Akimov M (2013) Inhibition of HSP90 with AUY922 induces synergy in HER2-amplified trastuzumab-resistant breast and gastric cancer. Mol Cancer Ther 12(4):509–519PubMedCrossRefPubMedCentralGoogle Scholar
  110. Walton-Diaz A, Khan S, Bourboulia D, Trepel JB, Neckers L, Mollapour M (2013) Contributions of co-chaperones and post-translational modifications towards Hsp90 drug sensitivity. Future Med Chem 5:1059–1071PubMedCrossRefPubMedCentralGoogle Scholar
  111. Wang YQ, Zhang XM, Wang XD, Wang BJ, Wang W (2010) 17-AAG, a Hsp90 inhibitor, attenuates the hypoxia-induced expression of SDF-1alpha and ILK in mouse RPE cells. Mol Biol Rep 37:1203–1209PubMedCrossRefPubMedCentralGoogle Scholar
  112. Wang C, Zhang Y, Guo K, Wang N, Jin H, Liu Y, Qin W (2016) Heat shock proteins in hepatocellular carcinoma: molecular mechanism and therapeutic potential. Int J Cancer 138:1824–1834PubMedCrossRefPubMedCentralGoogle Scholar
  113. Waza M, Adachi H, Katsuno M, Minamiyama M, Sang C, Tanaka F, Inukai A, Doyu M, Sobue G (2005) 17-AAG, an Hsp90 inhibitor, ameliorates polyglutamine-mediated motor neuron degeneration. Nat Med 11:1088PubMedCrossRefPubMedCentralGoogle Scholar
  114. Whitesell L, Lindquist SL (2005) HSP90 and the chaperoning of cancer. Nat Rev Cancer 5:761–772PubMedCrossRefGoogle Scholar
  115. Workman P, Burrows F, Neckers L, Rosen N (2007) Drugging the cancer chaperone HSP90. Ann N Y Acad Sci 1113:202–216PubMedCrossRefPubMedCentralGoogle Scholar
  116. Wu W-C, Kao Y-H, Hu P-S, Chen J-H (2007) Geldanamycin, a HSP90 inhibitor, attenuates the hypoxia-induced vascular endothelial growth factor expression in retinal pigment epithelium cells in vitro. Exp Eye Res 85:721–731PubMedCrossRefPubMedCentralGoogle Scholar
  117. Xu Y, Lindquist S (1993) Heat-shock protein hsp90 governs the activity of pp60v-src kinase. Proc Natl Acad Sci USA 90:7074–7078PubMedCrossRefPubMedCentralGoogle Scholar
  118. Yan D, Guo L, Wang Y (2006) Requirement of dendritic Akt degradation by the ubiquitin–proteasome system for neuronal polarity. J Cell Biol 174:415–424PubMedPubMedCentralCrossRefGoogle Scholar
  119. Ylikomi T, Wurtz JM, Syvälä H, Passinen S, Pekki A, Haverinen M, Bläuer M, Tuohimaa P, Gronemeyer H (1998) Reappraisal of the role of heat shock proteins as regulators of steroid receptor activity. Crit Rev Biochem Mol Biol 33:437–466PubMedCrossRefPubMedCentralGoogle Scholar
  120. Zou J, Guo Y, Guettouche T, Smith DF, Voellmy R (1998) Repression of heat shock transcription factor HSF1 activation by HSP90 (HSP90 complex) that forms a stress-sensitive complex with HSF1. Cell 94:471–480PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Asmaa Aboelnour
    • 1
  • Ahmed E. Noreldin
    • 1
  • Islam M. Saadeldin
    • 2
    • 3
    Email author
  1. 1.Histology and Cytology Department, Faculty of Veterinary MedicineDamanhour UniversityDamanhourEgypt
  2. 2.Department of Animal Production, College of Food and Agricultural ScienceKing Saud UniversityRiyadhSaudi Arabia
  3. 3.Department of Physiology, Faculty of Veterinary MedicineZagazig UniversityZagazigEgypt

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