Protein N-homocysteinylation: From cellular toxicity to neurodegeneration

Biochimica et Biophysica Acta - General Subjects

Volumn 1850, Issue 11, 2015, Pages 2239-2245

  Sharma, Gurumayum Suraj ^a   Kumar, Tarun ^a   Dar, Tanveer Ali ^b   Singh, Laishram Rajendrakumar ^a  

^a UNIVERSITY OF DELHI   (India)

^b UNIVERSITY OF KASHMIR   (India)

Author keywords

Amyloids; Homocysteine; Homocysteine thiolactone; Homocystinuria; Neurodegenerative disease; Protein N homocysteinylation

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PROTEIN; HOMOCYSTEINE; HOMOCYSTEINE THIOLACTONE; PRION PROTEIN; PROTEIN AGGREGATE; TAU PROTEIN; AMYLOID; PRION;

ALZHEIMER DISEASE; CALCIUM TRANSPORT; CHEMICAL STRUCTURE; CORRELATIONAL STUDY; CYTOTOXICITY; ENZYME INACTIVATION; GENE CONTROL; HUMAN; LIPID PEROXIDATION; MOLECULAR DYNAMICS; NERVE DEGENERATION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DENATURATION; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN N HOMOCYSTEINYLATION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; REVIEW; UPREGULATION; ANALOGS AND DERIVATIVES; ANIMAL; CHEMISTRY; DRUG EFFECTS; METABOLISM; NERVE CELL; NEURODEGENERATIVE DISEASES; PRION;

ALZHEIMER DISEASE; AMYLOID; AMYLOID BETA-PEPTIDES; ANIMALS; HOMOCYSTEINE; HUMANS; NEURODEGENERATIVE DISEASES; NEURONS; PRIONS; PROTEIN AGGREGATES;

EID: 84940484542     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2015.08.013     Document Type: Review

References (110)

1. R.K. Chowhan, S. Mittal, T.A. Dar, M.A. Kamal, and L.R. Singh Ignored avenues in alpha-synuclein associated proteopathy CNS Neurol. Disord. Drug Targets 13 2014 1246 1257
2. C.A. Ross, and M.A. Poirier Protein aggregation and neurodegenerative disease Nat. Med. 10 2004 S10 S17 (Suppl.)
3. R.K. Chowhan, and L.R. Singh Polyamines in Modulating Protein Aggregation, Journal of Proteins & Proteomics 3 2012
4. R.K. Chowhan, M. Warepam, T.A. Dar, and L.R. Singh Recent Trends in Treating Neuronal Proteinopathies, Journal of Proteins & Proteomics 4 2013
5. M.P. Mattson, and T.B. Shea Folate and homocysteine metabolism in neural plasticity and neurodegenerative disorders Trends Neurosci. 26 2003 137 146
6. R. Obeid, and W. Herrmann Mechanisms of homocysteine neurotoxicity in neurodegenerative diseases with special reference to dementia FEBS Lett. 580 2006 2994 3005
7. S. Seshadri Elevated plasma homocysteine levels: risk factor or risk marker for the development of dementia and Alzheimer's disease? J. Alzheimers Dis. 9 2006 393 398
8. S. Schuh, D.S. Rosenblatt, B.A. Cooper, M.L. Schroeder, A.J. Bishop, L.E. Seargeant, and J.C. Haworth Homocystinuria and megaloblastic anemia responsive to vitamin B12 therapy. An inborn error of metabolism due to a defect in cobalamin metabolism N. Engl. J. Med. 310 1984 686 690
9. L. Dodds, D.B. Fell, K.C. Dooley, B.A. Armson, A.C. Allen, B.A. Nassar, S. Perkins, and K.S. Joseph Effect of homocysteine concentration in early pregnancy on gestational hypertensive disorders and other pregnancy outcomes Clin. Chem. 54 2008 326 334
10. H. Gellekink, M. den Heijer, S.G. Heil, and H.J. Blom Genetic determinants of plasma total homocysteine Semin. Vasc. Med. 5 2005 98 109
11. A.B. Lawrence de Koning, G.H. Werstuck, J. Zhou, and R.C. Austin Hyperhomocysteinemia and its role in the development of atherosclerosis Clin. Biochem. 36 2003 431 441
12. H. Refsum, P.M. Ueland, O. Nygard, and S.E. Vollset Homocysteine and cardiovascular disease Annu. Rev. Med. 49 1998 31 62
13. J.D. Spence, H. Bang, L.E. Chambless, and M.J. Stampfer Vitamin intervention for stroke prevention trial: an efficacy analysis Stroke 36 2005 2404 2409
14. A.J. Grieco Homocystinuria: pathogenetic mechanisms Am. J. Med. Sci. 273 1977 120 132
15. S.H. Mudd, F. Skovby, H.L. Levy, K.D. Pettigrew, B. Wilcken, R.E. Pyeritz, G. Andria, G.H. Boers, I.L. Bromberg, R. Cerone, and et al. The natural history of homocystinuria due to cystathionine beta-synthase deficiency Am. J. Hum. Genet. 37 1985 1 31
16. P.S. Sachdev, M. Valenzuela, X.L. Wang, J.C. Looi, and H. Brodaty Relationship between plasma homocysteine levels and brain atrophy in healthy elderly individuals Neurology 58 2002 1539 1541
17. M. van den Berg, M.S. van der Knaap, G.H. Boers, C.D. Stehouwer, J.A. Rauwerda, and J. Valk Hyperhomocysteinaemia; with reference to its neuroradiological aspects Neuroradiology 37 1995 403 411
18. K. Eto, T. Asada, K. Arima, T. Makifuchi, and H. Kimura Brain hydrogen sulfide is severely decreased in Alzheimer's disease Biochem. Biophys. Res. Commun. 293 2002 1485 1488
19. C. Isobe, T. Murata, C. Sato, and Y. Terayama Increase of total homocysteine concentration in cerebrospinal fluid in patients with Alzheimer's disease and Parkinson's disease Life Sci. 77 2005 1836 1843
20. B. Regland, L. Abrahamsson, K. Blennow, B. Grenfeldt, and C.G. Gottfries CSF-methionine is elevated in psychotic patients J. Neural Transm. 111 2004 631 640
21. B. Regland, M. Andersson, L. Abrahamsson, J. Bagby, L.E. Dyrehag, and C.G. Gottfries Increased concentrations of homocysteine in the cerebrospinal fluid in patients with fibromyalgia and chronic fatigue syndrome Scand. J. Rheumatol. 26 1997 301 307
22. Y. Yanai, T. Shibasaki, N. Kohno, T. Mitsui, and H. Nakajima Concentrations of sulfur-containing free amino acids in lumbar cerebrospinal fluid from patients with consciousness disturbances Acta Neurol. Scand. 68 1983 386 393
23. R. Obeid, H. Schorr, R. Eckert, and W. Herrmann Vitamin B12 status in the elderly as judged by available biochemical markers Clin. Chem. 50 2004 238 241
24. R. Diaz-Arrastia Homocysteine and neurologic disease Arch. Neurol. 57 2000 1422 1427
25. M.J. Morrell Guidelines for the care of women with epilepsy Neurology 51 1998 S21 S27
26. G. Ravaglia, P. Forti, F. Maioli, M. Martelli, L. Servadei, N. Brunetti, E. Porcellini, and F. Licastro Homocysteine and folate as risk factors for dementia and Alzheimer disease Am. J. Clin. Nutr. 82 2005 636 643
27. H. Jakubowski Pathophysiological consequences of homocysteine excess J. Nutr. 136 2006 1741S 1749S
28. S. Seshadri, A. Beiser, J. Selhub, P.F. Jacques, I.H. Rosenberg, R.B. D'Agostino, P.W. Wilson, and P.A. Wolf Plasma homocysteine as a risk factor for dementia and Alzheimer's disease N. Engl. J. Med. 346 2002 476 483
29. A.A. Boldyrev Why homocysteine is a risk factor of neurodegenerative diseases Neurochem. J. 1 2007 14 20
30. I.F. McDowell, and D. Lang Homocysteine and endothelial dysfunction: a link with cardiovascular disease J. Nutr. 130 2000 369S 372S
31. J. Perla-Kajan, T. Twardowski, and H. Jakubowski Mechanisms of homocysteine toxicity in humans Amino Acids 32 2007 561 572
32. C. Zhang, Y. Cai, M.T. Adachi, S. Oshiro, T. Aso, R.J. Kaufman, and S. Kitajima Homocysteine induces programmed cell death in human vascular endothelial cells through activation of the unfolded protein response J. Biol. Chem. 276 2001 35867 35874
33. J. Loscalzo The oxidant stress of hyperhomocyst(e)inemia J. Clin. Invest. 98 1996 5 7
34. K.S. McCully Homocysteine and vascular disease Nat. Med. 2 1996 386 389
35. D.W. Jacobsen Hyperhomocysteinemia and oxidative stress: time for a reality check? Arterioscler. Thromb. Vasc. Biol. 20 2000 1182 1184
36. G. Ferretti, T. Bacchetti, C. Moroni, A. Vignini, L. Nanetti, and G. Curatola Effect of homocysteinylation of low density lipoproteins on lipid peroxidation of human endothelial cells J. Cell. Biochem. 92 2004 351 360
37. P.A. Outinen, S.K. Sood, S.I. Pfeifer, S. Pamidi, T.J. Podor, J. Li, J.I. Weitz, and R.C. Austin Homocysteine-induced endoplasmic reticulum stress and growth arrest leads to specific changes in gene expression in human vascular endothelial cells Blood 94 1999 959 967
38. P.I. Ho, S.C. Collins, S. Dhitavat, D. Ortiz, D. Ashline, E. Rogers, and T.B. Shea Homocysteine potentiates beta-amyloid neurotoxicity: role of oxidative stress J. Neurochem. 78 2001 249 253
39. A.R. White, X. Huang, M.F. Jobling, C.J. Barrow, K. Beyreuther, C.L. Masters, A.I. Bush, and R. Cappai Homocysteine potentiates copper- and amyloid beta peptide-mediated toxicity in primary neuronal cultures: possible risk factors in the Alzheimer's-type neurodegenerative pathways J. Neurochem. 76 2001 1509 1520
40. G.H. Werstuck, S.R. Lentz, S. Dayal, G.S. Hossain, S.K. Sood, Y.Y. Shi, J. Zhou, N. Maeda, S.K. Krisans, M.R. Malinow, and R.C. Austin Homocysteine-induced endoplasmic reticulum stress causes dysregulation of the cholesterol and triglyceride biosynthetic pathways J. Clin. Invest. 107 2001 1263 1273
41. D.T. Rutkowski, and R.J. Kaufman A trip to the ER: coping with stress Trends Cell Biol. 14 2004 20 28
42. G.H. Doherty Homocysteine and Parkinson's disease: a complex relationship J. Neurodev. Disord. 1 2013 1 9
43. W. Herrmann, and R. Obeid Homocysteine: a biomarker in neurodegenerative diseases Clin. Chem. Lab. Med. 49 2011 435 441
44. J.M. Zhuo, H. Wang, and D. Pratico Is hyperhomocysteinemia an Alzheimer's disease (AD) risk factor, an AD marker, or neither? Trends Pharmacol. Sci. 32 2011 562 571
45. H. Jakubowski Metabolism of homocysteine thiolactone in human cell cultures. Possible mechanism for pathological consequences of elevated homocysteine levels J. Biol. Chem. 272 1997 1935 1942
46. H. Jakubowski Protein homocysteinylation: possible mechanism underlying pathological consequences of elevated homocysteine levels FASEB J. 13 1999 2277 2283
47. H. Jakubowski Calcium-dependent human serum homocysteine thiolactone hydrolase. A protective mechanism against protein N-homocysteinylation J. Biol. Chem. 275 2000 3957 3962
48. H. Jakubowski, L. Zhang, A. Bardeguez, and A. Aviv Homocysteine thiolactone and protein homocysteinylation in human endothelial cells: implications for atherosclerosis Circ. Res. 87 2000 45 51
49. H. Jakubowski, and E. Goldman Synthesis of homocysteine thiolactone by methionyl-tRNA synthetase in cultured mammalian cells FEBS Lett. 317 1993 237 240
50. H. Jakubowski Homocysteine thiolactone: metabolic origin and protein homocysteinylation in humans J. Nutr. 130 2000 377S 381S
51. A. Zinellu, E. Zinellu, S. Sotgia, M. Formato, G.M. Cherchi, L. Deiana, and C. Carru Factors affecting S-homocysteinylation of LDL apoprotein B Clin. Chem. 52 2006 2054 2059
52. D. Hubmacher, J.T. Cirulis, M. Miao, F.W. Keeley, and D.P. Reinhardt Functional consequences of homocysteinylation of the elastic fiber proteins fibrillin-1 and tropoelastin J. Biol. Chem. 285 2010 1188 1198
53. H. Jakubowski Molecular basis of homocysteine toxicity in humans Cell. Mol. Life Sci. 61 2004 470 487
54. S. Jalili, R. Yousefi, M.M. Papari, and A.A. Moosavi-Movahedi Effect of homocysteine thiolactone on structure and aggregation propensity of bovine pancreatic insulin Protein J. 30 2011 299 307
55. O. Karima, G. Riazi, S. Khodadadi, H. Aryapour, M.A. Khalili, L. Yousefi, and A.A. Moosavi-Movahedi Altered tubulin assembly dynamics with N-homocysteinylated human 4R/1N tau in vitro FEBS Lett. 586 2012 3914 3919
56. S. Khazaei, R. Yousefi, and M.M. Alavian-Mehr Aggregation and fibrillation of eye lens crystallins by homocysteinylation; implication in the eye pathological disorders Protein J. 31 2012 717 727
57. S. Khodadadi, G.H. Riazi, S. Ahmadian, E. Hoveizi, O. Karima, and H. Aryapour Effect of N-homocysteinylation on physicochemical and cytotoxic properties of amyloid beta-peptide FEBS Lett. 586 2012 127 131
58. P. Paoli, F. Sbrana, B. Tiribilli, A. Caselli, B. Pantera, P. Cirri, A. De Donatis, L. Formigli, D. Nosi, G. Manao, G. Camici, and G. Ramponi Protein N-homocysteinylation induces the formation of toxic amyloid-like protofibrils J. Mol. Biol. 400 2010 889 907
59. J. Perla-Kajan, L. Marczak, L. Kajan, P. Skowronek, T. Twardowski, and H. Jakubowski Modification by homocysteine thiolactone affects redox status of cytochrome C Biochemistry 46 2007 6225 6231
60. Y.Y. Stroylova, J.M. Chobert, V.I. Muronetz, H. Jakubowski, and T. Haertle N-homocysteinylation of ovine prion protein induces amyloid-like transformation Arch. Biochem. Biophys. 526 2012 29 37
61. Y.Y. Stroylova, J. Zimny, R. Yousefi, J.M. Chobert, H. Jakubowski, V.I. Muronetz, and T. Haertle Aggregation and structural changes of alpha(S1)-, beta- and kappa-caseins induced by homocysteinylation Biochim. Biophys. Acta 1814 2011 1234 1245
62. R. Yousefi, S. Jalili, P. Alavi, and A.A. Moosavi-Movahedi The enhancing effect of homocysteine thiolactone on insulin fibrillation and cytotoxicity of insulin fibril Int. J. Biol. Macromol. 51 2012 291 298
63. T. Zang, S. Dai, D. Chen, B.W. Lee, S. Liu, B.L. Karger, and Z.S. Zhou Chemical methods for the detection of protein N-homocysteinylation via selective reactions with aldehydes Anal. Chem. 81 2009 9065 9071
64. R. Glowacki, and H. Jakubowski Cross-talk between Cys34 and lysine residues in human serum albumin revealed by N-homocysteinylation J. Biol. Chem. 279 2004 10864 10871
65. J. Garel, and D.S. Tawfik Mechanism of hydrolysis and aminolysis of homocysteine thiolactone Chemistry 12 2006 4144 4152
66. T. Kumar, G.S. Sharma, and L.R. Singh Existence of molten globule state in homocysteine-induced protein covalent modifications PLoS One 9 2014 e113566
67. A. Undas, J. Perla, M. Lacinski, W. Trzeciak, R. Kazmierski, and H. Jakubowski Autoantibodies against N-homocysteinylated proteins in humans: implications for atherosclerosis Stroke 35 2004 1299 1304
68. H. Jakubowski The pathological hypothesis of homocysteine thiolactone-mediated vascular disease J. Physiol. Pharmacol. 59 2008 155 167
69. G.S. Sharma, T. Kumar, and L.R. Singh N-Homocysteinylation induces different structural and functional consequences on acidic and basic proteins PLoS One 9 2014 e116386
70. E. Sontag, V. Nunbhakdi-Craig, J.M. Sontag, R. Diaz-Arrastia, E. Ogris, S. Dayal, S.R. Lentz, E. Arning, and T. Bottiglieri Protein phosphatase 2A methyltransferase links homocysteine metabolism with tau and amyloid precursor protein regulation J. Neurosci. 27 2007 2751 2759
71. S.O. Loureiro, L. Heimfarth, B.A. Lacerda, L.F. Vidal, A. Soska, N.l.G. dos Santos, A.T. de Souza Wyse, and R. Pessoa-Pureur Homocysteine induces hypophosphorylation of intermediate filaments and reorganization of actin cytoskeleton in C6 glioma cells Cell. Mol. Neurobiol. 30 2010 557 568
72. S.O. Loureiro, L. Heimfarth, P.d.L. Pelaez, B.A. Lacerda, L.F. Vidal, A. Soska, N.l.G.d. Santos, C.u. Andrade, B.r. Tagliari, and E. Scherer Hyperhomocysteinemia selectively alters expression and stoichiometry of intermediate filament and induces glutamate- and calcium-mediated mechanisms in rat brain during development Int. J. Dev. Neurosci. 28 2010 21 30
73. S.O. Loureiro, L. Heimfarth, P.d.L. Pelaez, C.S. Vanzin, L. Viana, A.T.S. Wyse, and R. Pessoa-Pureur Homocysteine activates calcium-mediated cell signaling mechanisms targeting the cytoskeleton in rat hippocampus Int. J. Dev. Neurosci. 26 2008 447 455
74. H. Jakubowski Homocysteine-thiolactone and S-nitroso-homocysteine mediate incorporation of homocysteine into protein in humans Clin. Chem. Lab. Med. 41 2003 1462 1466
75. D.L. Sauls, E. Lockhart, M.E. Warren, A. Lenkowski, S.E. Wilhelm, and M. Hoffman Modification of fibrinogen by homocysteine thiolactone increases resistance to fibrinolysis: a potential mechanism of the thrombotic tendency in hyperhomocysteinemia Biochemistry 45 2006 2480 2487
76. M. Naruszewicz, E. Mirkiewicz, A.J. Olszewski, and K.S. McCully Thiolation of low-density lipoprotein by homocysteine-thiolactone causes increased aggregation and interaction with cultured macrophages Nutr. Metab. Cardiovasc. Dis. 4 1994 70 77
77. C.E. Hop, and R. Bakhtiar Homocysteine thiolactone and protein homocysteinylation: mechanistic studies with model peptides and proteins Rapid Commun. Mass Spectrom. 16 2002 1049 1053
78. Y.Y. Stroylova, P.I. Semenyuk, R.A. Asriyantz, C. Gaillard, T. Haertlé, and V.I. Muronetz Creation of catalytically active particles from enzymes crosslinked with a natural bifunctional agent-homocysteine thiolactone Biopolymers 101 2014 975 984
79. L. Hong, and W. Fast Inhibition of human dimethylarginine dimethylaminohydrolase-1 by S-nitroso-L-homocysteine and hydrogen peroxide: analysis, quantification, and implications for hyperhomocysteinemia J. Biol. Chem. 282 2007 34684 34692
80. M.C. Stühlinger, P.S. Tsao, J.-H. Her, M. Kimoto, R.F. Balint, and J.P. Cooke Homocysteine impairs the nitric oxide synthase pathway role of asymmetric dimethylarginine Circulation 104 2001 2569 2575
81. G. Topal, A. Brunet, E. Millanvoye, J. Boucher, F. Rendu, M. Devynck, and M. David-Dufilho Homocysteine induces oxidative stress by uncoupling of NO synthase activity through reduction of tetrahydrobiopterin Free Radic. Biol. Med. 36 2004 1532 1541
82. H. Jakubowski Homocysteine is a protein amino acid in humans: implications for homocysteine-linked disease J. Biol. Chem. 277 2002 30425 30428
83. E.H. Koo, P.T. Lansbury Jr., and J.W. Kelly Amyloid diseases: abnormal protein aggregation in neurodegeneration Proc. Natl. Acad. Sci. U. S. A. 96 1999 9989 9990
84. D.M. Skovronsky, V.M.Y. Lee, and J.Q. Trojanowski Neurodegenerative diseases: new concepts of pathogenesis and their therapeutic implications Annu. Rev. Pathol.: Mech. Dis. 1 2006 151 170
85. H.A. Lashuel, D. Hartley, B.M. Petre, T. Walz, and P.T. Lansbury Jr. Neurodegenerative disease: amyloid pores from pathogenic mutations Nature 418 2002 291
86. H.A. Pearson, and C. Peers Physiological roles for amyloid beta peptides J. Physiol. 575 2006 5 10
87. D.J. Selkoe Alzheimer's disease: genes, proteins, and therapy Physiol. Rev. 81 2001 741 766
88. D.J. Selkoe Soluble oligomers of the amyloid beta-protein impair synaptic plasticity and behavior Behav. Brain Res. 192 2008 106 113
89. J.M. Borreguero, B. Urbanc, N.D. Lazo, S.V. Buldyrev, D.B. Teplow, and H.E. Stanley Folding events in the 21-30 region of amyloid beta-protein (Abeta) studied in silico Proc. Natl. Acad. Sci. U. S. A. 102 2005 6015 6020
90. W.P. Esler, E.R. Stimson, J.R. Ghilardi, Y.A. Lu, A.M. Felix, H.V. Vinters, P.W. Mantyh, J.P. Lee, and J.E. Maggio Point substitution in the central hydrophobic cluster of a human beta-amyloid congener disrupts peptide folding and abolishes plaque competence Biochemistry 35 1996 13914 13921
91. A. Karsai, A. Nagy, A. Kengyel, Z. Martonfalvi, L. Grama, B. Penke, and M.S. Kellermayer Effect of lysine-28 side-chain acetylation on the nanomechanical behavior of Alzheimer amyloid beta25-35 fibrils J. Chem. Inf. Model. 45 2005 1641 1646
92. T. Luhrs, C. Ritter, M. Adrian, D. Riek-Loher, B. Bohrmann, H. Dobeli, D. Schubert, and R. Riek 3D structure of Alzheimer's amyloid-beta(1-42) fibrils Proc. Natl. Acad. Sci. U. S. A. 102 2005 17342 17347 (cc)
93. A.T. Petkova, Y. Ishii, J.J. Balbach, O.N. Antzutkin, R.D. Leapman, F. Delaglio, and R. Tycko A structural model for Alzheimer's beta-amyloid fibrils based on experimental constraints from solid state NMR Proc. Natl. Acad. Sci. U. S. A. 99 2002 16742 16747
94. J.C. Rochet, and P.T. Lansbury Jr. Amyloid fibrillogenesis: themes and variations Curr. Opin. Struct. Biol. 10 2000 60 68
95. L.O. Tjernberg, C. Lilliehook, D.J. Callaway, J. Naslund, S. Hahne, J. Thyberg, L. Terenius, and C. Nordstedt Controlling amyloid beta-peptide fibril formation with protease-stable ligands J. Biol. Chem. 272 1997 12601 12605
96. L.O. Tjernberg, J. Naslund, F. Lindqvist, J. Johansson, A.R. Karlstrom, J. Thyberg, L. Terenius, and C. Nordstedt Arrest of beta-amyloid fibril formation by a pentapeptide ligand J. Biol. Chem. 271 1996 8545 8548
97. G. Bellesia, and J.E. Shea Effect of beta-sheet propensity on peptide aggregation J. Chem. Phys. 130 2009 145103
98. R. Pellarin, E. Guarnera, and A. Caflisch Pathways and intermediates of amyloid fibril formation J. Mol. Biol. 374 2007 917 924
99. J. Hardy, and D.J. Selkoe The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics Science 297 2002 353 356
100. M.P. Lambert, A.K. Barlow, B.A. Chromy, C. Edwards, R. Freed, M. Liosatos, T.E. Morgan, I. Rozovsky, B. Trommer, K.L. Viola, P. Wals, C. Zhang, C.E. Finch, G.A. Krafft, and W.L. Klein Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins Proc. Natl. Acad. Sci. U. S. A. 95 1998 6448 6453
101. C. Haass, and D.J. Selkoe Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid beta-peptide Nat. Rev. Mol. Cell Biol. 8 2007 101 112
102. M. Goedert, M.G. Spillantini, R. Jakes, D. Rutherford, and R.A. Crowther Multiple isoforms of human microtubule-associated protein tau: sequences and localization in neurofibrillary tangles of Alzheimer's disease Neuron 3 1989 519 526
103. A. Andreadis, W.M. Brown, and K.S. Kosik Structure and novel exons of the human. tau. gene Biochemistry 31 1992 10626 10633
104. L. Buee, T. Bussiere, V. Buee-Scherrer, A. Delacourte, and P.R. Hof Tau protein isoforms, phosphorylation and role in neurodegenerative disorders Brain Res. Brain Res. Rev. 33 2000 95 130
105. E.M. Mandelkow, O. Schweers, G. Drewes, J. Biernat, N. Gustke, B. Trinczek, and E. Mandelkow Structure, microtubule interactions, and phosphorylation of tau protein Ann. N. Y. Acad. Sci. 777 1996 96 106
106. M. Hong, V. Zhukareva, V. Vogelsberg-Ragaglia, Z. Wszolek, L. Reed, B.I. Miller, D.H. Geschwind, T.D. Bird, D. McKeel, A. Goate, J.C. Morris, K.C. Wilhelmsen, G.D. Schellenberg, J.Q. Trojanowski, and V.M. Lee Mutation-specific functional impairments in distinct tau isoforms of hereditary FTDP-17 Science 282 1998 1914 1917
107. J.Q. Trojanowski, and V.M. Lee The role of tau in Alzheimer's disease Med. Clin. North Am. 86 2002 615 627
108. S.B. Prusiner Shattuck lecture - neurodegenerative diseases and prions N. Engl. J. Med. 344 2001 1516 1526
109. M. Cisse, and L. Mucke Alzheimer's disease: a prion protein connection Nature 457 2009 1090 1091
110. J. Lauren, D.A. Gimbel, H.B. Nygaard, J.W. Gilbert, and S.M. Strittmatter Cellular prion protein mediates impairment of synaptic plasticity by amyloid-beta oligomers Nature 457 2009 1128 1132