Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2014 (2014), Article ID 239164, 9 pages
http://dx.doi.org/10.1155/2014/239164
Review Article

Heat Shock Proteins at the Crossroads between Cancer and Alzheimer’s Disease

1Department of Oncology, The Affiliated Hospital of Qingdao University, Qingdao 266003, China
2Department of Neurology, Qingdao Municipal Hospital, College of Medicine and Pharmaceutics, Ocean University of China, Qingdao 266003, China
3Department of Neurology, Qingdao Municipal Hospital, School of Medicine, Qingdao University, Qingdao 266071, China

Received 7 February 2014; Accepted 12 July 2014; Published 24 July 2014

Academic Editor: Hanna Rosenmann

Copyright © 2014 Hao Wang et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. L. A. Demetrius and D. K. Simon, “The inverse association of cancer and Alzheimer’s: a bioenergetic mechanism,” Journal of the Royal Society, Interface, vol. 10, no. 82, Article ID 20130006, 2013. View at Publisher · View at Google Scholar · View at Scopus
  2. C. M. Roe and M. I. Behrens, “AD and cancer: epidemiology makes for strange bedfellows,” Neurology, vol. 81, no. 4, pp. 310–311, 2013. View at Publisher · View at Google Scholar · View at Scopus
  3. M. Musicco, F. Adorni, S. Di Santo et al., “Inverse occurrence of cancer and Alzheimer disease: a population-based incidence study,” Neurology, vol. 81, no. 4, pp. 322–328, 2013. View at Publisher · View at Google Scholar · View at Scopus
  4. H. Plun-Favreau, P. A. Lewis, J. Hardy, L. M. Martins, and N. W. Wood, “Cancer and neurodegeneration: between the devil and the deep blue sea,” PLoS Genetics, vol. 6, no. 12, Article ID e1001257, 2010. View at Publisher · View at Google Scholar · View at Scopus
  5. N. V. Bobkova, D. G. Garbuz, I. Nesterova et al., “Therapeutic effect of exogenous hsp70 in mouse models of Alzheimer’s disease,” Journal of Alzheimer’s Disease, vol. 38, no. 2, pp. 425–435, 2014. View at Google Scholar
  6. H. H. Kampinga, J. Hageman, M. J. Vos et al., “Guidelines for the nomenclature of the human heat shock proteins,” Cell Stress and Chaperones, vol. 14, no. 1, pp. 105–111, 2009. View at Publisher · View at Google Scholar · View at Scopus
  7. D. R. Ciocca and S. K. Calderwood, “Heat shock proteins in cancer: diagnostic, prognostic, predictive, and treatment implications,” Cell Stress & Chaperones, vol. 10, no. 2, pp. 86–103, 2005. View at Publisher · View at Google Scholar · View at Scopus
  8. M. Tavaria, T. Gabriele, I. Kola, and R. L. Anderson, “A hitchhiker's guide to the human Hsp70 family,” Cell Stress and Chaperones, vol. 1, no. 1, pp. 23–28, 1996. View at Publisher · View at Google Scholar · View at Scopus
  9. K. A. Morano, “New tricks for an old dog: the evolving world of Hsp70,” Annals of the New York Academy of Sciences, vol. 1113, pp. 1–14, 2007. View at Publisher · View at Google Scholar · View at Scopus
  10. B. Chen, D. Zhong, and A. Monteiro, “Comparative genomics and evolution of the HSP90 family of genes across all kingdoms of organisms,” BMC Genomics, vol. 7, article 156, 2006. View at Publisher · View at Google Scholar · View at Scopus
  11. L. H. Pearl and C. Prodromou, “Structure and in vivo function of Hsp90,” Current Opinion in Structural Biology, vol. 10, no. 1, pp. 46–51, 2000. View at Publisher · View at Google Scholar · View at Scopus
  12. C. Prodromou and L. H. Pearl, “Structure and functional relationships of Hsp90,” Current Cancer Drug Targets, vol. 3, no. 5, pp. 301–323, 2003. View at Publisher · View at Google Scholar · View at Scopus
  13. L. H. Pearl and C. Prodromou, “Structure, function, and mechanism of the Hsp90 molecular chaperone,” Advances in Protein Chemistry, vol. 59, pp. 157–186, 2001. View at Publisher · View at Google Scholar · View at Scopus
  14. C. A. Dickey, A. Kamal, K. Lundgren et al., “The high-affinity HSP90-CHIP complex recognizes and selectively degrades phosphorylated tau client proteins,” Journal of Clinical Investigation, vol. 117, no. 3, pp. 648–658, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. H. Zhao, M. L. Michaelis, and B. S. Blagg, “Hsp90 modulation for the treatment of Alzheimer’s disease,” Advances in Pharmacology, vol. 64, pp. 1–25, 2012. View at Publisher · View at Google Scholar · View at Scopus
  16. D. R. Ciocca, A. P. Arrigo, and S. K. Calderwood, “Heat shock proteins and heat shock factor 1 in carcinogenesis and tumor development: an update,” Archives of Toxicology, vol. 87, no. 1, pp. 19–48, 2013. View at Publisher · View at Google Scholar · View at Scopus
  17. P. J. Gray Jr., T. Prince, J. Cheng, M. A. Stevenson, and S. K. Calderwood, “Targeting the oncogene and kinome chaperone CDC37,” Nature Reviews Cancer, vol. 8, no. 7, pp. 491–495, 2008. View at Publisher · View at Google Scholar · View at Scopus
  18. J. Trepel, M. Mollapour, G. Giaccone, and L. Neckers, “Targeting the dynamic HSP90 complex in cancer,” Nature Reviews Cancer, vol. 10, no. 8, pp. 537–549, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. M. A. Khaleque, A. Bharti, D. Sawyer et al., “Induction of heat shock proteins by heregulin β1 leads to protection from apoptosis and anchorage-independent growth,” Oncogene, vol. 24, no. 43, pp. 6564–6573, 2005. View at Publisher · View at Google Scholar · View at Scopus
  20. C. Garrido, M. Brunet, C. Didelot, Y. Zermati, E. Schmitt, and G. Kroemer, “Heat shock proteins 27 and 70: anti-apoptotic proteins with tumorigenic properties,” Cell Cycle, vol. 5, no. 22, pp. 2592–2601, 2006. View at Publisher · View at Google Scholar · View at Scopus
  21. V. L. Gabai, J. A. Yaglom, T. Waldman, and M. Y. Sherman, “Heat shock protein Hsp72 controls oncogene-induced senescence pathways in cancer cells,” Molecular and Cellular Biology, vol. 29, no. 2, pp. 559–569, 2009. View at Publisher · View at Google Scholar · View at Scopus
  22. C. O’Callaghan-Sunol, V. L. Gabai, and M. Y. Sherman, “Hsp27 modulates p53 signaling and suppresses cellular senescence,” Cancer Research, vol. 67, no. 24, pp. 11779–11788, 2007. View at Publisher · View at Google Scholar · View at Scopus
  23. L. Neckers and S. P. Ivy, “Heat shock protein 90,” Current Opinion in Oncology, vol. 15, no. 6, pp. 419–424, 2003. View at Publisher · View at Google Scholar · View at Scopus
  24. J. Sun and J. K. Liao, “Induction of angiogenesis by heat shock protein 90 mediated by protein kinase Akt and endothelial nitric oxide synthase,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 24, no. 12, pp. 2238–2244, 2004. View at Publisher · View at Google Scholar · View at Scopus
  25. A. Pfosser, M. Thalgott, K. Büttner et al., “Liposomal Hsp90 cDNA induces neovascularization via nitric oxide in chronic ischemia,” Cardiovascular Research, vol. 65, no. 3, pp. 728–736, 2005. View at Publisher · View at Google Scholar · View at Scopus
  26. Y. Xie, C. Chen, M. A. Stevenson, P. E. Auron, and S. K. Calderwood, “Heat shock factor 1 represses transcription of the IL-1β gene through physical interaction with the nuclear factor of interleukin 6,” The Journal of Biological Chemistry, vol. 277, no. 14, pp. 11802–11810, 2002. View at Publisher · View at Google Scholar · View at Scopus
  27. A. Mazumdar, R. A. Wang, S. K. Mishra et al., “Transcriptional repression of oestrogen receptor by metastasis-associated protein 1 corepressor,” Nature Cell Biology, vol. 3, no. 1, pp. 30–37, 2001. View at Publisher · View at Google Scholar · View at Scopus
  28. S. K. Calderwood, M. A. Khaleque, D. B. Sawyer, and D. R. Ciocca, “Heat shock proteins in cancer: chaperones of tumorigenesis,” Trends in Biochemical Sciences, vol. 31, no. 3, pp. 164–172, 2006. View at Publisher · View at Google Scholar · View at Scopus
  29. G. Jego, A. Hazoumé, R. Seigneuric, and C. Garrido, “Targeting heat shock proteins in cancer,” Cancer Letters, vol. 332, no. 2, pp. 275–285, 2013. View at Publisher · View at Google Scholar · View at Scopus
  30. C. Queitsch, T. A. Sangstert, and S. Lindquist, “Hsp90 as a capacitor of phenotypic variation,” Nature, vol. 417, no. 6889, pp. 618–624, 2002. View at Publisher · View at Google Scholar · View at Scopus
  31. S. L. Rutherford and S. Lindquist, “Hsp90 as a capacitor for morphological evolution,” Nature, vol. 396, no. 6709, pp. 336–342, 1998. View at Publisher · View at Google Scholar · View at Scopus
  32. T. A. Sangster, S. Lindquist, and C. Queitsch, “Under cover: causes, effects and implications of Hsp90-mediated genetic capacitance,” BioEssays, vol. 26, no. 4, pp. 348–362, 2004. View at Publisher · View at Google Scholar · View at Scopus
  33. M. V. Blagosklonny, “Hsp-90-associated oncoproteins: multiple targets of geldanamycin and its analogs,” Leukemia, vol. 16, no. 4, pp. 455–462, 2002. View at Publisher · View at Google Scholar · View at Scopus
  34. M. Taipale, D. F. Jarosz, and S. Lindquist, “HSP90 at the hub of protein homeostasis: emerging mechanistic insights,” Nature Reviews Molecular Cell Biology, vol. 11, no. 7, pp. 515–528, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. B. K. Eustace, T. Sakurai, J. K. Stewart et al., “Functional proteomic screens reveal an essential extracellular role for hsp90α in cancer cell invasiveness,” Nature Cell Biology, vol. 6, no. 6, pp. 507–514, 2004. View at Publisher · View at Google Scholar · View at Scopus
  36. L. Whitesell and S. L. Lindquist, “HSP90 and the chaperoning of cancer,” Nature Reviews Cancer, vol. 5, no. 10, pp. 761–772, 2005. View at Publisher · View at Google Scholar · View at Scopus
  37. P. Pandey, A. Saleh, A. Nakazawa et al., “Negative regulation of cytochrome c-mediated oligomerization of Apaf-1 and activation of procaspase-9 by heat shock protein 90,” The EMBO Journal, vol. 19, no. 16, pp. 4310–4322, 2000. View at Publisher · View at Google Scholar · View at Scopus
  38. R. Zhang, D. Luo, R. Miao et al., “Hsp90-Akt phosphorylates ASK1 and inhibits ASK1-mediated apoptosis,” Oncogene, vol. 24, no. 24, pp. 3954–3963, 2005. View at Publisher · View at Google Scholar · View at Scopus
  39. S. Fulda, L. Galluzzi, and G. Kroemer, “Targeting mitochondria for cancer therapy,” Nature Reviews Drug Discovery, vol. 9, no. 6, pp. 447–464, 2010. View at Publisher · View at Google Scholar · View at Scopus
  40. G. Garcia-Cardena, R. Fan, V. Shah et al., “Dynamic activation of endothelial nitric oxide synthase by Hsp90,” Nature, vol. 392, no. 6678, pp. 821–824, 1998. View at Publisher · View at Google Scholar
  41. M. Ziche and L. Morbidelli, “Nitric oxide and angiogenesis,” Journal of Neuro-Oncology, vol. 50, no. 1-2, pp. 139–148, 2000. View at Publisher · View at Google Scholar · View at Scopus
  42. S. Sanderson, M. Valenti, S. Gowan et al., “Benzoquinone ansamycin heat shock protein 90 inhibitors modulate multiple functions required for tumor angiogenesis,” Molecular Cancer Therapeutics, vol. 5, no. 3, pp. 522–532, 2006. View at Publisher · View at Google Scholar · View at Scopus
  43. D. R. Ciocca, G. M. Clark, A. K. Tandon, S. A. W. Fuqua, W. J. Welch, and W. L. McGuire, “Heat shock protein hsp70 in patients with axillary lymph node-negative breast cancer: prognostic implications,” Journal of the National Cancer Institute, vol. 85, no. 7, pp. 570–574, 1993. View at Publisher · View at Google Scholar · View at Scopus
  44. R. M. Elledge, G. M. Clark, S. A. W. Fuqua, Y. Yu, and D. C. Allred, “p53 protein accumulation detected by five different antibodies: relationship to prognosis and heat shock protein 70 in breast cancer,” Cancer Research, vol. 54, no. 14, pp. 3752–3757, 1994. View at Google Scholar · View at Scopus
  45. S. Mestiri, N. Bouaouina, S. B. Ahmed et al., “Genetic variation in the tumor necrosis factor-alpha promoter region and in the stress protein hsp70-2: susceptibility and prognostic implications in breast carcinoma,” Cancer, vol. 91, no. 4, pp. 672–678, 2001. View at Publisher · View at Google Scholar
  46. F. Thanner, M. W. Sütterlin, M. Kapp et al., “Heat-shock protein 70 as a prognostic marker in node-negative breast cancer,” Anticancer Research, vol. 23, no. 2A, pp. 1057–1062, 2003. View at Google Scholar · View at Scopus
  47. K. Nanbu, I. Konishi, M. Mandai et al., “Prognostic significance of heat shock proteins HSP70 and HSP90 in endometrial carcinomas,” Cancer Detection and Prevention, vol. 22, no. 6, pp. 549–555, 1998. View at Publisher · View at Google Scholar · View at Scopus
  48. B. Piura, A. Rabinovich, V. Yavelsky, and M. Wolfson, “Heat shock proteins and malignancies of the female genital tract,” Harefuah, vol. 141, no. 11, pp. 969–972, 2002. View at Google Scholar · View at Scopus
  49. K. N. Syrigos, K. J. Harrington, A. J. Karayiannakis et al., “Clinical significance of heat shock protein-70 expression in bladder cancer,” Urology, vol. 61, no. 3, pp. 677–680, 2003. View at Publisher · View at Google Scholar · View at Scopus
  50. M. M. Konstadoulakis, M. Vezeridis, E. Hatziyianni et al., “Molecular oncogene markers and their significance in cutaneous malignant melanoma,” Annals of Surgical Oncology, vol. 5, no. 3, pp. 253–260, 1998. View at Publisher · View at Google Scholar · View at Scopus
  51. N. Ricaniadis, A. Kataki, N. Agnantis, G. Androulakis, and C. P. Karakousis, “Long-term prognostic significance of HSP-70, c-myc and HLA-DR expression in patients with malignant melanoma,” European Journal of Surgical Oncology, vol. 27, no. 1, pp. 88–93, 2001. View at Publisher · View at Google Scholar · View at Scopus
  52. K. Kawanishi, H. Shiozaki, Y. Doki et al., “Prognostic significance of heat shock proteins 27 and 70 in patients with squamous cell carcinoma of the esophagus,” Cancer, vol. 85, pp. 1649–1657, 1999. View at Google Scholar
  53. M. Nakajima, H. Kuwano, T. Miyazaki, N. Masuda, and H. Kato, “Significant correlation between expression of heat shock proteins 27, 70 and lymphocyte infiltration in esophageal squamous cell carcinoma,” Cancer Letters, vol. 178, no. 1, pp. 99–106, 2002. View at Publisher · View at Google Scholar · View at Scopus
  54. T. Noguchi, S. Takeno, T. Shibata, Y. Uchida, S. Yokoyama, and W. Müller, “Expression of heat shock protein 70 in grossly resected esophageal squamous cell carcinoma,” The Annals of Thoracic Surgery, vol. 74, no. 1, pp. 222–226, 2002. View at Publisher · View at Google Scholar · View at Scopus
  55. Ö. Sagol, B. Tuna, A. Oker et al., “Immunohistochemical detection of PS2 protein and heat shock protein-70 in pancreatic adenocarcinomas. Relationship with disease extent and patient survival,” Pathology Research and Practice, vol. 198, no. 2, pp. 77–84, 2002. View at Publisher · View at Google Scholar · View at Scopus
  56. M. Santarosa, D. Favaro, M. Quaia, and E. Galligioni, “Expression of heat shock protein 72 in renal cell carcinoma: possible role and prognostic implications in cancer patients,” European Journal of Cancer Part A, vol. 33, no. 6, pp. 873–877, 1997. View at Publisher · View at Google Scholar · View at Scopus
  57. P. Athanassiadou, E. Petrakakou, V. Sakelariou et al., “Expression of p53, bcl-2 and heat shock protein (hsp72) in malignant and benign ovarian tumours,” European Journal of Cancer Prevention, vol. 7, no. 3, pp. 225–231, 1998. View at Publisher · View at Google Scholar · View at Scopus
  58. T. Ito, R. Kawabe, Y. Kurasono et al., “Expression of heat shock proteins in squamous cell carcinoma of the tongue: an immunohistochemical study,” Journal of Oral Pathology & Medicine, vol. 27, no. 1, pp. 18–22, 1998. View at Google Scholar · View at Scopus
  59. R. Gandour-Edwards, B. J. Trock, P. Gumerlock, and P. J. Donald, “Heat shock protein and p53 expression in head and neck squamous cell carcinoma,” Otolaryngology—Head and Neck Surgery, vol. 118, no. 5, pp. 610–615, 1998. View at Publisher · View at Google Scholar · View at Scopus
  60. Y. Maehara, E. Oki, T. Abe et al., “Overexpression of the heat shock protein HSP70 family and p53 protein and prognosis for patients with gastric cancer,” Oncology, vol. 58, no. 2, pp. 144–151, 2000. View at Publisher · View at Google Scholar · View at Scopus
  61. P. A. Cornford, A. R. Dodson, K. F. Parsons et al., “Heat shock protein expression independently predicts clinical outcome in prostate cancer,” Cancer Research, vol. 60, no. 24, pp. 7099–7105, 2000. View at Google Scholar · View at Scopus
  62. G. Stammler and M. Volm, “Expression of heat shock proteins, glutathione peroxidase and catalase in childhood acute lymphoblastic leukemia and nephroblastoma,” Cancer Letters, vol. 99, no. 1, pp. 35–42, 1996. View at Publisher · View at Google Scholar · View at Scopus
  63. A. Jameel, R. A. Skilton, T. A. Campbell, S. K. Chander, R. C. Coombes, and Y. A. Luqmani, “Clinical and biological significance of HSP89 alpha in human breast cancer,” International Journal of Cancer, vol. 50, no. 3, pp. 409–415, 1992. View at Publisher · View at Google Scholar · View at Scopus
  64. S. E. Conroy, P. D. Sasieni, I. Fentiman, and D. S. Latchman, “Autoantibodies to the 90 kDa heat shock protein and poor survival in breast cancer patients,” European Journal of Cancer, vol. 34, no. 6, pp. 942–943, 1998. View at Google Scholar · View at Scopus
  65. K. Nanbu, I. Konishi, T. Komatsu et al., “Expression of heat shock proteins HSP70 and HSP90 in endometrial carcinomas. Correlation with clinicopathology, sex steroid receptor status, and p53 protein expression,” Cancer, vol. 77, no. 2, pp. 330–338, 1996. View at Publisher · View at Google Scholar
  66. R. W. G. Watson, T. Lebret, and J. M. Fitzpatrick, “Heat shock proteins in the genitourinary system.,” Current Urology Reports, vol. 4, no. 1, pp. 70–76, 2003. View at Publisher · View at Google Scholar · View at Scopus
  67. J. Zou, Y. Guo, T. Guettouche, D. F. Smith, and R. Voellmy, “Repression of heat shock transcription factor HSF1 activation by HSP90 (HSP90 complex) that forms a stress-sensitive complex with HSF1,” Cell, vol. 94, no. 4, pp. 471–480, 1998. View at Publisher · View at Google Scholar · View at Scopus
  68. P. K. Sorger and H. R. B. Pelham, “Yeast heat shock factor is an essential DNA-binding protein that exhibits temperature-dependent phosphorylation,” Cell, vol. 54, no. 6, pp. 855–864, 1988. View at Publisher · View at Google Scholar · View at Scopus
  69. J. T. Westwood and C. Wu, “Activation of Drosophila heat shock factor: conformational change associated with a monomer-to-trimer transition,” Molecular and Cellular Biology, vol. 13, no. 6, pp. 3481–3486, 1993. View at Google Scholar · View at Scopus
  70. V. Hietakangas, J. K. Ahlskog, A. M. Jakobsson et al., “Phosphorylation of serine 303 is a prerequisite for the stress-inducible SUMO modification of heat shock factor 1,” Molecular and Cellular Biology, vol. 23, no. 8, pp. 2953–2968, 2003. View at Publisher · View at Google Scholar · View at Scopus
  71. S. D. Westerheide, J. Anckar, S. M. Stevens Jr., L. Sistonen, and R. I. Morimoto, “Stress-inducible regulation of heat shock factor 1 by the deacetylase SIRT,” Science, vol. 323, no. 5917, pp. 1063–1066, 2009. View at Publisher · View at Google Scholar · View at Scopus
  72. P. A. Jones and S. B. Baylin, “The fundamental role of epigenetic events in cancer,” Nature Reviews Genetics, vol. 3, no. 6, pp. 415–428, 2002. View at Google Scholar · View at Scopus
  73. U. Singh, E. Bongcam-Rudloff, and B. Westermark, “A DNA sequence directed mutual transcription regulation of HSF1 and NFIX involves novel heat sensitive protein interactions,” PLoS ONE, vol. 4, no. 4, Article ID e5050, 2009. View at Publisher · View at Google Scholar · View at Scopus
  74. I. Guzhova and B. Margulis, “Hsp70 chaperone as a survival factor in cell pathology,” International Review of Cytology, vol. 254, pp. 101–149, 2006. View at Publisher · View at Google Scholar · View at Scopus
  75. J. L. Wacker, S. Huang, A. D. Steele et al., “Loss of Hsp70 exacerbates pathogenesis but not levels of fibrillar aggregates in a mouse model of Huntington’s disease,” Journal of Neuroscience, vol. 29, no. 28, pp. 9104–9114, 2009. View at Publisher · View at Google Scholar · View at Scopus
  76. D. J. Gifondorwa, M. B. Robinson, C. D. Hayes et al., “Exogenous delivery of heat shock protein 70 increases lifespan in a mouse model of amyotrophic lateral sclerosis,” Journal of Neuroscience, vol. 27, no. 48, pp. 13173–13180, 2007. View at Publisher · View at Google Scholar · View at Scopus
  77. C. G. Evans, S. Wisén, and J. E. Gestwicki, “Heat shock proteins 70 and 90 inhibit early stages of amyloid β-(1–42) aggregation in vitro,” The Journal of Biological Chemistry, vol. 281, no. 44, pp. 33182–33191, 2006. View at Publisher · View at Google Scholar · View at Scopus
  78. T. B. Franklin, A. M. Krueger-Naug, D. B. Clarke, A.-. Arrigo, and R. W. Currie, “The role of heat shock proteins Hsp70 and Hsp27 in cellular protection of the central nervous system,” International Journal of Hyperthermia, vol. 21, no. 5, pp. 379–392, 2005. View at Publisher · View at Google Scholar · View at Scopus
  79. K. Honjo, S. E. Black, and N. P. L. G. Verhoeff, “Alzheimer’s disease, cerebrovascular disease, and the β-amyloid cascade,” The Canadian Journal of Neurological Sciences, vol. 39, no. 6, pp. 712–728, 2012. View at Google Scholar · View at Scopus
  80. G. M. Shankar, S. Li, T. H. Mehta et al., “Amyloid-beta protein dimers isolated directly from Alzheimer’s brains impair synaptic plasticity and memory,” Nature Medicine, vol. 14, no. 8, pp. 837–842, 2008. View at Google Scholar
  81. K. Herrup, “Reimagining Alzheimer’s disease—an age-based hypothesis,” The Journal of Neuroscience, vol. 30, no. 50, pp. 16755–16762, 2010. View at Publisher · View at Google Scholar · View at Scopus
  82. J. A. Hardy and G. A. Higgins, “Alzheimer’s disease: the amyloid cascade hypothesis,” Science, vol. 256, no. 5054, pp. 184–185, 1992. View at Publisher · View at Google Scholar · View at Scopus
  83. S. Oddo, A. Caccamo, J. D. Shepherd et al., “Triple-transgenic model of Alzheimer’s Disease with plaques and tangles: intracellular Aβ and synaptic dysfunction,” Neuron, vol. 39, no. 3, pp. 409–421, 2003. View at Publisher · View at Google Scholar · View at Scopus
  84. R. H. Takahashi, E. E. Nam, M. Edgar, and G. K. Gouras, “Alzheimer β-amyloid peptides: normal and abnormal localization,” Histology and Histopathology, vol. 17, no. 1, pp. 239–246, 2002. View at Google Scholar · View at Scopus
  85. J. Magrané, R. C. Smith, K. Walsh, and H. W. Querfurth, “Heat shock protein 70 participates in the neuroprotective response to intracellularly expressed β-amyloid in neurons,” Journal of Neuroscience, vol. 24, no. 7, pp. 1700–1706, 2004. View at Publisher · View at Google Scholar · View at Scopus
  86. T. Hoshino, N. Murao, T. Namba et al., “Suppression of Alzheimer’s disease-related phenotypes by expression of heat shock protein 70 in mice,” The Journal of Neuroscience, vol. 31, no. 14, pp. 5225–5234, 2011. View at Publisher · View at Google Scholar · View at Scopus
  87. S. K. Calderwood, S. S. Mambula, P. J. Gray Jr., and J. R. Theriault, “Extracellular heat shock proteins in cell signaling,” FEBS Letters, vol. 581, no. 19, pp. 3689–3694, 2007. View at Publisher · View at Google Scholar · View at Scopus
  88. P. J. Muchowski and J. L. Wacker, “Modulation of neurodegeneration by molecular chaperones,” Nature Reviews Neuroscience, vol. 6, no. 1, pp. 11–22, 2005. View at Publisher · View at Google Scholar · View at Scopus
  89. P. Kumar, R. K. Ambasta, V. Veereshwarayya et al., “CHIP and HSPs interact with β-APP in a proteasome-dependent manner and influence Aβ metabolism,” Human Molecular Genetics, vol. 16, no. 7, pp. 848–864, 2007. View at Publisher · View at Google Scholar · View at Scopus
  90. S. M. Ward, D. S. Himmelstein, J. K. Lancia, and L. I. Binder, “Tau oligomers and tau toxicity in neurodegenerative disease,” Biochemical Society Transactions, vol. 40, no. 4, pp. 667–671, 2012. View at Publisher · View at Google Scholar · View at Scopus
  91. U. K. Jinwal, J. Koren, J. C. O’Leary, J. R. Jones, J. F. Abisambra, and C. A. Dickey, “Hsp70 ATPase modulators as therapeutics for Alzheimer’s and other Neurodegenerative diseases,” Molecular and Cellular Pharmacology, vol. 2, no. 2, pp. 43–46, 2010. View at Publisher · View at Google Scholar · View at Scopus
  92. U. K. Jinwal, J. C. O’Leary III, S. I. Borysov et al., “Hsc70 rapidly engages tau after microtubule destabilization,” The Journal of Biological Chemistry, vol. 285, no. 22, pp. 16798–16805, 2010. View at Publisher · View at Google Scholar · View at Scopus
  93. K. R. Patterson, S. M. Ward, B. Combs et al., “Heat shock protein 70 prevents both tau aggregation and the inhibitory effects of preexisting tau aggregates on fast axonal transport,” Biochemistry, vol. 50, no. 47, pp. 10300–10310, 2011. View at Publisher · View at Google Scholar · View at Scopus
  94. U. K. Jinwal, Y. Miyata, J. Koren III et al., “Chemical manipulation of Hsp70 ATPase activity regulates tau stability,” Journal of Neuroscience, vol. 29, no. 39, pp. 12079–12088, 2009. View at Publisher · View at Google Scholar · View at Scopus
  95. W. Luo, W. Sun, T. Taldone, A. Rodina, and G. Chiosis, “Heat shock protein 90 in neurodegenerative diseases,” Molecular Neurodegeneration, vol. 5, no. 1, article 24, 2010. View at Publisher · View at Google Scholar · View at Scopus
  96. I. R. Brown, “Heat shock proteins and protection of the nervous system,” Annals of the New York Academy of Sciences, vol. 1113, pp. 147–158, 2007. View at Google Scholar
  97. M. Waza, H. Adachi, M. Katsuno et al., “Modulation of Hsp90 function in neurodegenerative disorders: a molecular-targeted therapy against disease-causing protein,” Journal of Molecular Medicine, vol. 84, no. 8, pp. 635–646, 2006. View at Publisher · View at Google Scholar · View at Scopus
  98. A. Salminen, J. Ojala, K. Kaarniranta, M. Hiltunen, and H. Soininen, “Hsp90 regulates tau pathology through co-chaperone complexes in Alzheimer’s disease,” Progress in Neurobiology, vol. 93, no. 1, pp. 99–110, 2011. View at Publisher · View at Google Scholar · View at Scopus
  99. P. Connell, C. A. Ballinger, J. Jiang et al., “The co-chaperone CHIP regulates protein triage decisions mediated by heat-shock proteins,” Nature Cell Biology, vol. 3, no. 1, pp. 93–96, 2001. View at Publisher · View at Google Scholar · View at Scopus
  100. H. McDonough and C. Patterson, “CHIP: a link between the chaperone and proteasome systems,” Cell Stress & Chaperones, vol. 8, no. 4, pp. 303–308, 2003. View at Google Scholar
  101. S. Murata, T. Chiba, and K. Tanaka, “CHIP: a quality-control E3 ligase collaborating with molecular chaperones,” International Journal of Biochemistry and Cell Biology, vol. 35, no. 5, pp. 572–578, 2003. View at Publisher · View at Google Scholar · View at Scopus
  102. C. A. Dickey, J. Dunmore, B. Lu et al., “HSP induction mediates selective clearance of tau phosphorylated at proline-directed Ser/Thr sites but not KXGS (MARK) sites,” The FASEB Journal, vol. 20, no. 6, pp. 753–755, 2006. View at Publisher · View at Google Scholar · View at Scopus
  103. S. Murata, Y. Minami, M. Minami, T. Chiba, and K. Tanaka, “CHIP is a chaperone-dependent E3 ligase that ubiquitylates unfolded protein,” The EMBO Reports, vol. 2, no. 12, pp. 1133–1138, 2001. View at Publisher · View at Google Scholar · View at Scopus
  104. Z. Xu, E. Kohli, K. I. Devlin, M. Bold, J. C. Nix, and S. Misra, “Interactions between the quality control ubiquitin ligase CHIP and ubiquitin conjugating enzymes,” BMC Structural Biology, vol. 8, article 26, 2008. View at Publisher · View at Google Scholar · View at Scopus
  105. C. Graf, M. Stankiewicz, R. Nikolay, and M. P. Mayer, “Insights into the conformational dynamics of the E3 ubiquitin ligase CHIP in complex with chaperones and E2 enzymes,” Biochemistry, vol. 49, no. 10, pp. 2121–2129, 2010. View at Publisher · View at Google Scholar · View at Scopus
  106. M. Zhang, M. Windheim, S. M. Roe et al., “Chaperoned ubiquitylation - Crystal structures of the CHIP U box E3 ubiquitin ligase and a CHIP-Ubc13-Uev1a complex,” Molecular Cell, vol. 20, no. 4, pp. 525–538, 2005. View at Publisher · View at Google Scholar · View at Scopus
  107. J. Kakimura, Y. Kitamura, K. Takata et al., “Microglial activation and amyloid-beta clearance induced by exogenous heat-shock proteins,” The FASEB Journal, vol. 16, no. 6, pp. 601–603, 2002. View at Google Scholar
  108. E. A. Craig, “The heat shock response,” CRC Critical Reviews in Biochemistry, vol. 18, no. 3, pp. 239–280, 1985. View at Publisher · View at Google Scholar · View at Scopus