Hsp70 alters tau function and aggregation in an isoform specific manner

Biochemistry

Volumn 51, Issue 4, 2012, Pages 888-898

  Voss, Kellen ^a   Combs, Benjamin ^a   Patterson, Kristina R ^b   Binder, Lester I ^b   Gamblin, T Chris ^a  

^a UNIVERSITY OF KANSAS   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALZHEIMER'S DISEASE; HEAT SHOCK PROTEIN 70; ISOFORMS; MICROTUBULE ASSEMBLY; MICROTUBULE ASSOCIATED PROTEIN; MICROTUBULES; MOLECULAR CHAPERONES; NATIVE CONFORMATION; NORMAL FUNCTION; PRIMARY SEQUENCES; REFOLDING; TAUOPATHIES;

HYDROPHOBICITY; NEURODEGENERATIVE DISEASES; OLIGOMERS;

PROTEINS;

HEAT SHOCK PROTEIN 70; ISOPROTEIN; TAU PROTEIN; TAU PROTEIN 0N3R; TAU PROTEIN 0N4R; TAU PROTEIN 1N3R; TAU PROTEIN 1N4R; TAU PROTEIN 2N3R; TAU PROTEIN 2N4R; UNCLASSIFIED DRUG;

ARTICLE; MICROTUBULE ASSEMBLY; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN FUNCTION; PROTEIN TARGETING; TAUOPATHY;

ADENOSINE TRIPHOSPHATE; ALTERNATIVE SPLICING; AMYLOID; ARACHIDONIC ACID; HSP70 HEAT-SHOCK PROTEINS; HUMANS; KINETICS; MICROSCOPY, ELECTRON, TRANSMISSION; MICROTUBULES; MOLECULAR TARGETED THERAPY; NEUROFIBRILLARY TANGLES; OSMOLAR CONCENTRATION; PROTEIN ISOFORMS; PROTEIN STABILITY; RECOMBINANT PROTEINS; REPETITIVE SEQUENCES, AMINO ACID; SOLUBILITY; TAU PROTEINS; TAUOPATHIES;

EID: 84856477398     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi2018078     Document Type: Article

References (71)

1. Himmler, A. (1989) Structure of the bovine tau gene: alternatively spliced transcripts generate a protein family Mol. Cell. Biol. 9, 1389-1396 (Pubitemid 19095178)
2. Himmler, A., Drechsel, D., Kirschner, M. W., and Martin, D. W., Jr. (1989) Tau consists of a set of proteins with repeated C-terminal microtubule-binding domains and variable N-terminal domains Mol. Cell. Biol. 9, 1381-1388 (Pubitemid 19095177)
3. Hernandez, F. and Avila, J. (2007) Tauopathies Cell. Mol. Life Sci. 64, 2219-2233 (Pubitemid 47347961)
4. Lee, V. M., Goedert, M., and Trojanowski, J. Q. (2001) Neurodegenerative tauopathies Annu. Rev. Neurosci. 24, 1121-1159 (Pubitemid 32695256)
5. Boutajangout, A., Boom, A., Leroy, K., and Brion, J. P. (2004) Expression of tau mRNA and soluble tau isoforms in affected and non-affected brain areas in Alzheimer's disease FEBS Lett. 576, 183-189 (Pubitemid 39330481)
6. Chambers, C. B., Lee, J. M., Troncoso, J. C., Reich, S., and Muma, N. A. (1999) Overexpression of four-repeat tau mRNA isoforms in progressive supranuclear palsy but not in Alzheimer's disease Ann. Neurol. 46, 325-332 (Pubitemid 29416270)
7. Connell, J. W., Rodriguez-Martin, T., Gibb, G. M., Kahn, N. M., Grierson, A. J., Hanger, D. P., Revesz, T., Lantos, P. L., Anderton, B. H., and Gallo, J. M. (2005) Quantitative analysis of tau isoform transcripts in sporadic tauopathies Brain Res. Mol. Brain Res. 137, 104-109 (Pubitemid 40798892)
8. Goedert, M., Spillantini, M. G., Jakes, R., Rutherford, D., and Crowther, R. A. (1989) Multiple isoforms of human microtubule-associated protein tau: sequences and localization in neurofibrillary tangles of Alzheimer's disease Neuron 3, 519-526
9. Goedert, M., Spillantini, M. G., Potier, M. C., Ulrich, J., and Crowther, R. A. (1989) Cloning and sequencing of the cDNA encoding an isoform of microtubule-associated protein tau containing four tandem repeats: differential expression of tau protein mRNAs in human brain EMBO J. 8, 393-399 (Pubitemid 19274956)
10. Ingelsson, M., Ramasamy, K., Cantuti-Castelvetri, I., Skoglund, L., Matsui, T., Orne, J., Kowa, H., Raju, S., Vanderburg, C. R., Augustinack, J. C., de Silva, R., Lees, A. J., Lannfelt, L., Growdon, J. H., Frosch, M. P., Standaert, D. G., Irizarry, M. C., and Hyman, B. T. (2006) No alteration in tau exon 10 alternative splicing in tangle-bearing neurons of the Alzheimer's disease brain Acta Neuropathol. 112, 439-449 (Pubitemid 44469164)
11. Espinoza, M., de Silva, R., Dickson, D. W., and Davies, P. (2008) Differential incorporation of tau isoforms in Alzheimer's disease J. Alzheimer's Dis. 14, 1-16 (Pubitemid 352039016)
12. Glatz, D. C., Rujescu, D., Tang, Y., Berendt, F. J., Hartmann, A. M., Faltraco, F., Rosenberg, C., Hulette, C., Jellinger, K., Hampel, H., Riederer, P., Moller, H. J., Andreadis, A., Henkel, K., and Stamm, S. (2006) The alternative splicing of tau exon 10 and its regulatory proteins CLK2 and TRA2-BETA1 changes in sporadic Alzheimer's disease J. Neurochem. 96, 635-644
13. Lace, G., Savva, G. M., Forster, G., de Silva, R., Brayne, C., Matthews, F. E., Barclay, J. J., Dakin, L., Ince, P. G., and Wharton, S. B. (2009) Hippocampal tau pathology is related to neuroanatomical connections: an ageing population-based study Brain 132, 1324-1334
14. Shi, J., Qian, W., Yin, X., Iqbal, K., Grundke-Iqbal, I., Gu, X., Ding, F., Gong, C. X., and Liu, F. (2011) Cyclic AMP-dependent protein kinase regulates the alternative splicing of tau exon 10: a mechanism involved in tau pathology of Alzheimer disease J. Biol. Chem. 286, 14639-14648
15. Umeda, Y., Taniguchi, S., Arima, K., Piao, Y. S., Takahashi, H., Iwatsubo, T., Mann, D., and Hasegawa, M. (2004) Alterations in human tau transcripts correlate with those of neurofilament in sporadic tauopathies Neurosci. Lett. 359, 151-154 (Pubitemid 38446660)
16. Yasojima, K., McGeer, E. G., and McGeer, P. L. (1999) Tangled areas of Alzheimer brain have upregulated levels of exon 10 containing tau mRNA Brain Res. 831, 301-305 (Pubitemid 29336215)
17. Voss, K. and Gamblin, T. C. (2009) GSK-3beta phosphorylation of functionally distinct tau isoforms has differential, but mild effects Mol. Neurodegener. 4, 18
18. Koren, J., III, Jinwal, U. K., Lee, D. C., Jones, J. R., Shults, C. L., Johnson, A. G., Anderson, L. J., and Dickey, C. A. (2009) Chaperone signalling complexes in Alzheimer's disease J. Cell. Mol. Med. 13, 619-630
19. Hartl, F. U. and Hayer-Hartl, M. (2002) Molecular chaperones in the cytosol: from nascent chain to folded protein Science 295, 1852-1858 (Pubitemid 34214115)
20. Brown, I. R. (2007) Heat shock proteins and protection of the nervous system Ann. N.Y. Acad. Sci. 1113, 147-158 (Pubitemid 350015026)
21. Young, J. C. (2010) Mechanisms of the Hsp70 chaperone system Biochem. Cell Biol. 88, 291-300
22. Chen, X., Li, Y., Huang, J., Cao, D., Yang, G., Liu, W., Lu, H., and Guo, A. (2007) Study of tauopathies by comparing Drosophila and human tau in Drosophila Cell Tissue Res. 329, 169-178 (Pubitemid 46686106)
23. Dou, F., Netzer, W. J., Tanemura, K., Li, F., Hartl, F. U., Takashima, A., Gouras, G. K., Greengard, P., and Xu, H. (2003) Chaperones Increase Association of Tau Protein with Microtubules Proc. Natl. Acad. Sci. U. S. A. 100, 721-726 (Pubitemid 36126119)
24. Sahara, N., Maeda, S., Yoshiike, Y., Mizoroki, T., Yamashita, S., Murayama, M., Park, J.-M., Saito, Y., Murayama, S., and Takashima, A. (2007) Molecular Chaperone-Mediated Tau Protein Metabolism Counteracts the Formation of Granular Tau Oligomers in Human Brain J. Neurosci. Res. 85, 3098-3108 (Pubitemid 350057365)
25. Petrucelli, L., Dickson, D., Kehoe, K., Taylor, J., Snyder, H., Grover, A., De Lucia, M., McGowan, E., Lewis, J., Prihar, G., Kim, J., Dillmann, W. H., Browne, S. E., Hall, A., Voellmy, R., Tsuboi, Y., Dawson, T. M., Wolozin, B., Hardy, J., and Hutton, M. (2004) CHIP and Hsp70 Regulate Tau Ubiquitination, degredation, and aggregation Hum. Mol. Genet. 13, 703-714 (Pubitemid 38455958)
26. Sarkar, M., Kuret, J., and Lee, G. (2008) Two Motifs Within the Tau Microtubule-binding Domain Mediate Its Association With the Hsc70 Molecular Chaperone J. Neurosci. Res. 86, 2763-2772
27. Jinwal, U. K., Miyata, Y., Koren, J., III, Jones, J. R., Trotter, J. H., Chang, L., O'Leary, J., Morgan, D., Lee, D. C., Shults, C. L., Rousaki, A., Weeber, E. J., Zuiderweg, E. R. P., Gestwicki, J. E., and Dickey, C. A. (2009) Chemical Manipulation of Hsp70 ATPase Activity Regulates Tau Stability J. Neurosci. 29, 12079-12088
28. Jinwal, U. K., O'Leary, J. C., III, Borysov, S. I., Jones, J. R., Li, Q., Koren, J., III, Abisambra, J. F., Vestal, G. D., Lawson, L. Y., Johnson, A. G., Blair, L. J., Jin, Y., Miyata, Y., Gestwicki, J. E., and Dickey, C. A. (2010) Hsc70 rapidly engages tau after microtubule destabilization J. Biol. Chem. 285, 16798-16805
29. Evans, C. G., Chang, L., and Gestwicki, J. E. (2010) Heat shock protein 70 (hsp70) as an emerging drug target J. Med. Chem. 53, 4585-4602
30. Patterson, K. R., Ward, S. M., Combs, B., Voss, K., Kanaan, N. M., Morfini, G., Brady, S. T., Gamblin, T. C., and Binder, L. I. (2011) Heat Shock Protein 70 Prevents both Tau Aggregation and the Inhibitory Effects of Preexisting Tau Aggregates on Fast Axonal Transport Biochemistry 50, 10300-10310
31. Andreadis, A. (2011) Tau splicing and the intricacies of dementia J. Cell Physiol. 227, 1220-1225
32. Brandt, R., Hundelt, M., and Shahani, N. (2005) Tau alteration and neuronal degeneration in tauopathies: mechanisms and models Biochim. Biophys. Acta 1739, 331-354 (Pubitemid 40018549)
33. D'Souza, I. and Schellenberg, G. D. (2005) Regulation of tau isoform expression and dementia Biochim. Biophys. Acta 1739, 104-115 (Pubitemid 40021805)
34. Friedhoff, P., von Bergen, M., Mandelkow, E. M., and Mandelkow, E. (2000) Structure of tau protein and assembly into paired helical filaments Biochim. Biophys. Acta 1502, 122-132 (Pubitemid 30433861)
35. Liu, F. and Gong, C. X. (2008) Tau exon 10 alternative splicing and tauopathies Mol. Neurodegener. 3, 8
36. Sergeant, N., Delacourte, A., and Buee, L. (2005) Tau protein as a differential biomarker of tauopathies Biochim. Biophys. Acta 1739, 179-197 (Pubitemid 40018537)
37. von Bergen, M., Barghorn, S., Biernat, J., Mandelkow, E. M., and Mandelkow, E. (2005) Tau aggregation is driven by a transition from random coil to beta sheet structure Biochim. Biophys. Acta 1739, 158-166 (Pubitemid 40018535)
38. Butner, K. A. and Kirschner, M. W. (1991) Tau protein binds to microtubules through a flexible array of distributed weak sites J. Cell Biol. 115, 717-730 (Pubitemid 21909925)
39. Goode, B. L., Chau, M., Denis, P. E., and Feinstein, S. C. (2000) Structural and functional differences between 3-repeat and 4-repeat tau isoforms. Implications for normal tau function and the onset of neurodegenerative disease J. Biol. Chem. 275, 38182-38189 (Pubitemid 32009136)
40. Goode, B. L. and Feinstein, S. C. (1994) Identification of a novel microtubule binding and assembly domain in the developmentally regulated inter-repeat region of tau J. Cell Biol. 124, 769-782
41. von Bergen, M., Barghorn, S., Li, L., Marx, A., Biernat, J., Mandelkow, E. M., and Mandelkow, E. (2001) Mutations of tau protein in frontotemporal dementia promote aggregation of paired helical filaments by enhancing local beta-structure J. Biol. Chem. 276, 48165-48174
42. von Bergen, M., Friedhoff, P., Biernat, J., Heberle, J., and Mandelkow, E. (2000) Assembly of tau protein into Alzheimer paired helical filaments depends on a local sequence motif (306VQIVYK311) forming beta structure Proc. Natl. Acad. Sci. U. S. A. 97, 5129-5134 (Pubitemid 30313683)
43. Carmel, G., Mager, E. M., Binder, L. I., and Kuret, J. (1996) The structural basis of monoclonal antibody Alz50's selectivity for Alzheimer's disease pathology J. Biol. Chem. 271, 32789-32795 (Pubitemid 27008707)
44. Carlson, S. W., Branden, M., Voss, K., Sun, Q., Rankin, C. A., and Gamblin, T. C. (2007) A complex mechanism for inducer mediated tau polymerization Biochemistry 46, 8838-8849 (Pubitemid 47204449)
45. Chirita, C. N., Congdon, E. E., Yin, H., and Kuret, J. (2005) Triggers of full-length tau aggregation: a role for partially folded intermediates Biochemistry 44, 5862-5872 (Pubitemid 40525123)
46. Rankin, C. A., Sun, Q., and Gamblin, T. C. (2007) Tau phosphorylation by GSK-3beta promotes tangle-like filament morphology Mol. Neurodegener. 2, 12
47. Rankin, C. A., Sun, Q., and Gamblin, T. C. (2008) Pre-assembled tau filaments phosphorylated by GSK-3b form large tangle-like structures Neurobiol Dis 31, 368-377
48. Sarthy, J. and Gamblin, T. C. (2006) A light scattering assay for arachidonic acid-induced tau fibrillization without interfering micellization Anal. Biochem. 353, 150-152 (Pubitemid 43668935)
49. Sun, Q. and Gamblin, T. C. (2009) Pseudohyperphosphorylation causing AD-like changes in tau has significant effects on its polymerization Biochemistry 48, 6002-6011
50. Bandyopadhyay, B., Li, G., Yin, H., and Kuret, J. (2007) Tau aggregation and toxicity in a cell culture model of tauopathy J. Biol. Chem. 282, 16454-16464 (Pubitemid 47100356)
51. DeTure, M., Granger, B., Grover, A., Hutton, M., and Yen, S. H. (2006) Evidence for independent mechanisms and a multiple-hit model of tau assembly Biochem. Biophys. Res. Commun. 339, 858-864 (Pubitemid 41772893)
52. King, M. E., Gamblin, T. C., Kuret, J., and Binder, L. I. (2000) Differential assembly of human tau isoforms in the presence of arachidonic acid J. Neurochem. 74, 1749-1757 (Pubitemid 30163998)
53. Benaroudj, N., Triniolles, F., and Ladjimi, M. M. (1996) Effect of nucleotides, peptides, and unfolded proteins on the self-association of the molecular chaperone HSC70 J. Biol. Chem. 271, 18471-18476 (Pubitemid 26322704)
54. Heuser, J. and Steer, C. J. (1989) Trimeric binding of the 70-kD uncoating ATPase to the vertices of clathrin triskelia: a candidate intermediate in the vesicle uncoating reaction J. Cell Biol. 109, 1457-1466 (Pubitemid 19251203)
55. Necula, M. and Kuret, J. (2004) Electron microscopy as a quantitative method for investigating tau fibrillization Anal. Biochem. 329, 238-246 (Pubitemid 38680504)
56. Barron, D. M., Chatterjee, S. K., Ravindra, R., Roof, R., Baloglu, E., Kingston, D. G., and Bane, S. (2003) A fluorescence-based high-throughput assay for antimicrotubule drugs Anal. Biochem. 315, 49-56 (Pubitemid 36379105)
57. Bonne, D., Heusele, C., Simon, C., and Pantaloni, D. (1985) 4′,6-Diamidino-2-phenylindole, a fluorescent probe for tubulin and microtubules J. Biol. Chem. 260, 2819-2825 (Pubitemid 15141425)
58. Necula, M. and Kuret, J. (2004) A static laser light scattering assay for surfactant-induced tau fibrillization Anal. Biochem. 333, 205-215 (Pubitemid 39278041)
59. Winsor, C. (1932) The Gompertz Curve as a Growth Curve Proc. Natl. Acad. Sci. U. S. A. 18, 1-8
60. Wilson, D. M. and Binder, L. I. (1997) Free fatty acids stimulate the polymerization of tau and amyloid beta peptides. In vitro evidence for a common effector of pathogenesis in Alzheimer's disease Am. J. Pathol. 150, 2181-2195 (Pubitemid 27233088)
61. Goedert, M., Jakes, R., Spillantini, M. G., Hasegawa, M., Smith, M. J., and Crowther, R. A. (1996) Assembly of microtubule-associated protein tau into Alzheimer-like filaments induced by sulphated glycosaminoglycans Nature 383, 550-553 (Pubitemid 26346185)
62. Voss, K. and Gamblin, T. C. (2009) GSK-3β phosphorylation of functionally distinct tau isoforms has differential, but mild effects Mol. Neurodegener. 4, 1-12
63. Akiyama, H., Barger, S., Barnum, S., Bradt, B., Bauer, J., Cole, G. M., Cooper, N. R., Eikelenboom, P., Emmerling, M., Fiebich, B. L., Finch, C. E., Frautschy, S., Griffin, W. S., Hampel, H., Hull, M., Landreth, G., Lue, L., Mrak, R., Mackenzie, I. R., McGeer, P. L., O'Banion, M. K., Pachter, J., Pasinetti, G., Plata-Salaman, C., Rogers, J., Rydel, R., Shen, Y., Streit, W., Strohmeyer, R., Tooyoma, I., Van Muiswinkel, F. L., Veerhuis, R., Walker, D., Webster, S., Wegrzyniak, B., Wenk, G., and Wyss-Coray, T. (2000) Inflammation and Alzheimer's disease Neurobiol. Aging 21, 383-421 (Pubitemid 30349107)
64. Markesbery, W. R. and Carney, J. M. (1999) Oxidative alterations in Alzheimer's disease Brain Pathol. 9, 133-146 (Pubitemid 29056524)
65. McGeer, E. G. and McGeer, P. L. (1998) The importance of inflammatory mechanisms in Alzheimer disease Exp. Gerontol. 33, 371-378 (Pubitemid 28354931)
66. Ray, W. J., Ashall, F., and Goate, A. M. (1998) Molecular pathogenesis of sporadic and familial forms of Alzheimer's disease Mol. Med. Today 4, 151-157 (Pubitemid 28207730)
67. Aksenov, M. Y., Aksenova, M. V., Butterfield, D. A., Geddes, J. W., and Markesbery, W. R. (2001) Protein oxidation in the brain in Alzheimer's disease Neuroscience 103, 373-383 (Pubitemid 32201924)
68. Patterson, K. R., Remmers, C., Fu, Y., Brooker, S., Kanaan, N. M., Vana, L., Ward, S., Reyes, J. F., Philibert, K., Glucksman, M. J., and Binder, L. I. (2011) Characterization of prefibrillar Tau oligomers in vitro and in Alzheimer disease J. Biol. Chem. 286, 23063-23076
69. Jeganathan, S., von Bergen, M., Brutlach, H., Steinhoff, H. J., and Mandelkow, E. (2006) Global hairpin folding of tau in solution Biochemistry 45, 2283-2293 (Pubitemid 43271328)
70. Santos, R. X., Correia, S. C., Wang, X., Perry, G., Smith, M. A., Moreira, P. I., and Zhu, X. (2010) Alzheimer's disease: diverse aspects of mitochondrial malfunctioning Int. J. Clin. Exp. Pathol. 3, 570-581
71. Amniai, L., Barbier, P., Sillen, A., Wieruszeski, J. M., Peyrot, V., Lippens, G., and Landrieu, I. (2008) Alzheimer disease specific phosphoepitopes of Tau interfere with assembly of tubulin but not binding to microtubules FASEB J. 23, 1146-1152