New age of neuroproteomics in Alzheimer's disease research

Cellular and Molecular Neurobiology

Volumn 29, Issue 6-7, 2009, Pages 799-805

  Kovacech, Branislav ^a,b   Zilka, Norbert ^a,b   Novak, Michal ^a  

^a INSTITUTE OF CHEMISTRY   (Slovakia)

^b Axon Neuroscience Forschungs und Entwicklungs GmbH   (Austria)

Author keywords

Alzheimer's disease; Hyperphosphorylation; Intrinsically disordered tau; Neuroproteomics; Truncation

Indexed keywords

AMYLOID PROTEIN; BIOLOGICAL MARKER; TAU PROTEIN;

ALZHEIMER DISEASE; ARTICLE; BIOACCUMULATION; BRAIN CELL; DISEASE COURSE; FUNCTIONAL PROTEOMICS; MEDICAL RESEARCH; NERVE DEGENERATION; NEUROFIBRILLARY TANGLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEOMICS; RAT; SENILE PLAQUE; SIGNAL TRANSDUCTION; STRUCTURAL PROTEOMICS; TAUOPATHY; TRANSGENIC RAT;

ALZHEIMER DISEASE; ANIMALS; HUMANS; PHOSPHORYLATION; PROTEOMICS; TAU PROTEINS;

RATTUS;

EID: 68149123432     PISSN: 02724340     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10571-009-9358-6     Document Type: Article

References (63)

1. R Aebersold M Mann 2003 Mass spectrometry-based proteomics Nature 422 6928 198 207 10.1038/nature01511 (Pubitemid 36362757)
2. AC Alonso T Zaidi I Grundke-Iqbal K Iqbal 1994 Role of abnormally phosphorylated tau in the breakdown of microtubules in Alzheimer disease Proc Natl Acad Sci USA 91 12 5562 5566 10.1073/pnas.91.12.5562 (Pubitemid 24174368)
3. AC Alonso I Grundke-Iqbal K Iqbal 1996 Alzheimer's disease hyperphosphorylated tau sequesters normal tau into tangles of filaments and disassembles microtubules Nat Med 2 7 783 787 10.1038/nm0796-783 (Pubitemid 26225094)
4. A Alzheimer 1907 Über eine eigenartigeErkrankung der Hirnrinde Allg Z Psychiatry Psych-Gerichtl Med 64 146 148
5. M Baker JB Kwok S Kucera R Crook M Farrer H Houlden A Isaacs S Lincoln L Onstead J Hardy L Wittenberg P Dodd S Webb N Hayward T Tannenberg A Andreadis M Hallupp P Schofield F Dark M Hutton 1997 Localization of frontotemporal dementia with parkinsonism in an Australian kindred to chromosome 17q21-22 Ann Neurol 42 5 794 798 10.1002/ana.410420516 (Pubitemid 27481552)
6. J Baudier RD Cole 1988 Interactions between the microtubule-associated tau proteins and S100b regulate tau phosphorylation by the Ca2+/calmodulin- dependent protein kinase II J Biol Chem 263 12 5876 5883
7. J Berriman LC Serpell KA Oberg AL Fink M Goedert RA Crowther 2003 Tau filaments from human brain and from in vitro assembly of recombinant protein show cross-beta structure Proc Natl Acad Sci USA 100 15 9034 9038 10.1073/pnas.1530287100 (Pubitemid 36899218)
8. LI Binder AL Guillozet-Bongaarts F Garcia-Sierra RW Berry 2005 Tau, tangles, and Alzheimer's disease Biochim Biophys Acta 1739 2-3 216 223
9. A Caceres KS Kosik 1990 Inhibition of neurite polarity by tau antisense oligonucleotides in primary cerebellar neurons Nature 343 6257 461 463 10.1038/343461a0 (Pubitemid 20065232)
10. M Cente P Filipcik M Pevalova M Novak 2006 Expression of a truncated tau protein induces oxidative stress in a rodent model of tauopathy Eur J NeuroSci 24 4 1085 1090 10.1111/j.1460-9568.2006.04986.x (Pubitemid 44268139)
11. HN Dawson A Ferreira MV Eyster N Ghoshal LI Binder MP Vitek 2001 Inhibition of neuronal maturation in primary hippocampal neurons from tau deficient mice J Cell Sci 114 Pt 6 1179 1187
12. CA Dickey A Kamal K Lundgren N Klosak RM Bailey J Dunmore P Ash S Shoraka J Zlatkovic CB Eckman C Patterson DW Dickson NS Nahman Jr M Hutton F Burrows L Petrucelli 2007 The high-affinity HSP90-CHIP complex recognizes and selectively degrades phosphorylated tau client proteins J Clin Invest 117 3 648 658 10.1172/JCI29715 (Pubitemid 46348523)
13. B Domon R Aebersold 2006 Mass spectrometry and protein analysis Science 312 5771 212 217 10.1126/science.1124619
14. J Eidenmuller T Fath T Maas M Pool E Sontag R Brandt 2001 Phosphorylation-mimicking glutamate clusters in the proline-rich region are sufficient to simulate the functional deficiencies of hyperphosphorylated tau protein Biochem J 357 Pt 3 759 767 10.1042/0264-6021:3570759 (Pubitemid 32735156)
15. B Esmaeli-Azad JH McCarty SC Feinstein 1994 Sense and antisense transfection analysis of tau function: tau influences net microtubule assembly, neurite outgrowth and neuritic stability J Cell Sci 107 Pt 4 869 879
16. CP Ferri M Prince C Brayne H Brodaty L Fratiglioni M Ganguli K Hall K Hasegawa H Hendrie Y Huang A Jorm C Mathers PR Menezes E Rimmer M Scazufca 2005 Global prevalence of dementia: a Delphi consensus study Lancet 366 9503 2112 2117 10.1016/S0140-6736(05)67889-0 (Pubitemid 41797645)
17. TC Gamblin F Chen A Zambrano A Abraha S Lagalwar AL Guillozet M Lu Y Fu F Garcia-Sierra N LaPointe R Miller RW Berry LI Binder VL Cryns 2003 Caspase cleavage of tau: linking amyloid and neurofibrillary tangles in Alzheimer's disease Proc Natl Acad Sci USA 100 17 10032 10037 10.1073/pnas.1630428100 (Pubitemid 37087063)
18. GG Glenner CW Wong 1984 Alzheimer's disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein Biochem Biophys Res Commun 120 3 885 890 10.1016/S0006-291X(84)80190-4
19. M Goedert MG Spillantini R Jakes D Rutherford RA Crowther 1989 Multiple isoforms of human microtubule-associated protein tau: sequences and localization in neurofibrillary tangles of Alzheimer's disease Neuron 3 4 519 526 10.1016/0896-6273(89)90210-9
20. M Goedert RA Crowther MG Spillantini 1998 Tau mutations cause frontotemporal dementias Neuron 21 5 955 958 10.1016/S0896-6273(00)80615-7 (Pubitemid 29018067)
21. I Grundke-Iqbal K Iqbal M Quinlan YC Tung MS Zaidi HM Wisniewski 1986 Microtubule-associated protein tau. A component of Alzheimer paired helical filaments J Biol Chem 261 13 6084 6089
22. R Hanemaaijer I Ginzburg 1991 Involvement of mature tau isoforms in the stabilization of neurites in PC12 cells J Neurosci Res 30 1 163 171 10.1002/jnr.490300117
23. DP Hanger HL Byers S Wray KY Leung MJ Saxton A Seereeram CH Reynolds MA Ward BH Anderton 2007 Novel phosphorylation sites in tau from Alzheimer brain support a role for casein kinase 1 in disease pathogenesis J Biol Chem 282 32 23645 23654 10.1074/jbc.M703269200 (Pubitemid 47311907)
24. A Harada K Oguchi S Okabe J Kuno S Terada T Ohshima R Sato-Yoshitake Y Takei T Noda N Hirokawa 1994 Altered microtubule organization in small-calibre axons of mice lacking tau protein Nature 369 6480 488 491 10.1038/369488a0 (Pubitemid 24210568)
25. T Horiguchi K Uryu BI Giasson H Ischiropoulos R LightFoot C Bellmann C Richter-Landsberg VM Lee JQ Trojanowski 2003 Nitration of tau protein is linked to neurodegeneration in tauopathies Am J Pathol 163 3 1021 1031
26. M Hrnkova N Zilka Z Minichova P Koson M Novak 2007 Neurodegeneration caused by expression of human truncated tau leads to progressive neurobehavioural impairment in transgenic rats Brain Res 1130 1 206 213 10.1016/j.brainres.2006.10.085 (Pubitemid 46053885)
27. M Hutton CL Lendon P Rizzu M Baker S Froelich H Houlden S Pickering-Brown S Chakraverty A Isaacs A Grover J Hackett J Adamson S Lincoln D Dickson P Davies RC Petersen M Stevens E de Graaff E Wauters J van Baren M Hillebrand M Joosse JM Kwon P Nowotny LK Che J Norton JC Morris LA Reed J Trojanowski H Basun L Lannfelt M Neystat S Fahn F Dark T Tannenberg PR Dodd N Hayward JB Kwok PR Schofield A Andreadis J Snowden D Craufurd D Neary F Owen BA Oostra J Hardy A Goate J van Swieten D Mann T Lynch P Heutink 1998 Association of missense and 5′-splice-site mutations in tau with the inherited dementia FTDP-17 Nature 393 6686 702 705 10.1038/31508 (Pubitemid 28289662)
28. H Inouye D Sharma WJ Goux DA Kirschner 2006 Structure of core domain of fibril-forming PHF/Tau fragments Biophys J 90 5 1774 1789 10.1529/biophysj.105. 070136
29. K Iqbal I Grundke-Iqbal 2008 Alzheimer neurofibrillary degeneration: significance, etiopathogenesis, therapeutics and prevention J Cell Mol Med 12 1 38 55 10.1111/j.1582-4934.2008.00225.x
30. K Iqbal C Alonso Adel S Chen MO Chohan E El-Akkad CX Gong S Khatoon B Li F Liu A Rahman H Tanimukai I Grundke-Iqbal 2005 Tau pathology in Alzheimer disease and other tauopathies Biochim Biophys Acta 1739 2-3 198 210
31. N Ivanovova M Handzusova J Hanes E Kontsekova M Novak 2008 High-yield purification of fetal tau preserving its structure and phosphorylation pattern J Immunol Methods 339 1 17 22 10.1016/j.jim.2008.07.014
32. PH Jensen H Hager MS Nielsen P Hojrup J Gliemann R Jakes 1999 Alpha-synuclein binds to Tau and stimulates the protein kinase A-catalyzed tau phosphorylation of serine residues 262 and 356 J Biol Chem 274 36 25481 25489 10.1074/jbc.274.36.25481 (Pubitemid 29418572)
33. M Khuebachova V Verzillo R Skrabana M Ovecka P Vaccaro S Panni A Bradbury M Novak 2002 Mapping the C terminal epitope of the Alzheimer's disease specific antibody MN423 J Immunol Methods 262 1-2 205 215 10.1016/S0022-1759(02)00006-6 (Pubitemid 34450744)
34. P Koson N Zilka A Kovac B Kovacech M Korenova P Filipcik M Novak 2008 Truncated tau expression levels determine life span of a rat model of tauopathy without causing neuronal loss or correlating with terminal neurofibrillary tangle load Eur J NeuroSci 28 2 239 246 10.1111/j.1460-9568.2008.06329.x
35. G Lee 2005 Tau and src family tyrosine kinases Biochim Biophys Acta 1739 2-3 323 330
36. J Lim KP Lu 2005 Pinning down phosphorylated tau and tauopathies Biochim Biophys Acta 1739 2-3 311 322
37. F Liu B Li EJ Tung I Grundke-Iqbal K Iqbal CX Gong 2007 Site-specific effects of tau phosphorylation on its microtubule assembly activity and self-aggregation Eur J NeuroSci 26 12 3429 3436
38. E Magnani J Fan L Gasparini M Golding M Williams G Schiavo M Goedert LA Amos MG Spillantini 2007 Interaction of tau protein with the dynactin complex EMBO J 26 21 4546 4554 10.1038/sj.emboj.7601878 (Pubitemid 350036634)
39. ER Mesco PS Timiras 1991 Tau-ubiquitin protein conjugates in a human cell line Mech Ageing Dev 61 1 1 9 10.1016/0047-6374(91)90002-H
40. M Morishima-Kawashima M Hasegawa K Takio M Suzuki K Titani Y Ihara 1993 Ubiquitin is conjugated with amino-terminally processed tau in paired helical filaments Neuron 10 6 1151 1160 10.1016/0896-6273(93)90063-W (Pubitemid 23194405)
41. MD Mukrasch M von Bergen J Biernat D Fischer C Griesinger E Mandelkow M Zweckstetter 2007 The "jaws" of the tau-microtubule interaction J Biol Chem 282 16 12230 12239 10.1074/jbc.M607159200 (Pubitemid 47100677)
42. M Novak 1994 Truncated tau protein as a new marker for Alzheimer's disease Acta Virol 38 3 173 189
43. M Novak CM Wischik P Edwards R Pannell C Milstein 1989 Characterisation of the first monoclonal antibody against the pronase resistant core of the Alzheimer PHF Prog Clin Biol Res 317 755 761
44. M Novak R Jakes PC Edwards C Milstein CM Wischik 1991 Difference between the tau protein of Alzheimer paired helical filament core and normal tau revealed by epitope analysis of monoclonal antibodies 423 and 7.51 Proc Natl Acad Sci USA 88 13 5837 5841 10.1073/pnas.88.13.5837
45. M Pevalova P Filipcik M Novak J Avila K Iqbal 2006 Post-translational modifications of tau protein Bratisl Lek Listy (Tlacene Vyd) 107 9-10 346 353
46. M Rapoport HN Dawson LI Binder MP Vitek A Ferreira 2002 Tau is essential to beta -amyloid-induced neurotoxicity Proc Natl Acad Sci USA 99 9 6364 6369 10.1073/pnas.092136199 (Pubitemid 34493317)
47. ED Roberson K Scearce-Levie JJ Palop F Yan IH Cheng T Wu H Gerstein GQ Yu L Mucke 2007 Reducing endogenous tau ameliorates amyloid beta-induced deficits in an Alzheimer's disease mouse model Science 316 5825 750 754 10.1126/science.1141736 (Pubitemid 46717684)
48. GC Ruben K Iqbal I Grundke-Iqbal HM Wisniewski TL Ciardelli JE Johnson Jr 1991 The microtubule-associated protein tau forms a triple-stranded left-hand helical polymer J Biol Chem 266 32 22019 22027
49. A Schneider J Biernat M von Bergen E Mandelkow EM Mandelkow 1999 Phosphorylation that detaches tau protein from microtubules (Ser262, Ser214) also protects it against aggregation into Alzheimer paired helical filaments Biochemistry 38 12 3549 3558 10.1021/bi981874p (Pubitemid 29149473)
50. GR Seabrook WJ Ray M Shearman M Hutton 2007 Beyond amyloid: the next generation of Alzheimer's disease therapeutics Mol Interv 7 5 261 270 10.1124/mi.7.5.8 (Pubitemid 47607486)
51. J Sevcik R Skrabana R Dvorsky N Csokova K Iqbal M Novak 2007 X-ray structure of the PHF core C-terminus: insight into the folding of the intrinsically disordered protein tau in Alzheimer's disease FEBS Lett 581 30 5872 5878 10.1016/j.febslet.2007.11.067 (Pubitemid 50009358)
52. N Siuti NL Kelleher 2007 Decoding protein modifications using top-down mass spectrometry Nat Methods 4 10 817 821 10.1038/nmeth1097 (Pubitemid 350055578)
53. R Skrabana P Kontsek A Mederlyova K Iqbal M Novak 2004 Folding of Alzheimer's core PHF subunit revealed by monoclonal antibody 423 FEBS Lett 568 1-3 178 182 10.1016/j.febslet.2004.04.098 (Pubitemid 38757978)
54. R Skrabana J Sevcik M Novak 2006 Intrinsically disordered proteins in the neurodegenerative processes: formation of tau protein paired helical filaments and their analysis Cell Mol Neurobiol 26 7-8 1085 1097 10.1007/s10571-006-9083-3 (Pubitemid 44924032)
55. ML Steinhilb D Dias-Santagata TA Fulga DL Felch MB Feany 2007 Tau phosphorylation sites work in concert to promote neurotoxicity in vivo Mol Biol Cell 18 12 5060 5068 10.1091/mbc.E07-04-0327 (Pubitemid 350246705)
56. ML Steinhilb D Dias-Santagata EE Mulkearns JM Shulman J Biernat EM Mandelkow MB Feany 2007 S/P and T/P phosphorylation is critical for tau neurotoxicity in Drosophila J Neurosci Res 85 6 1271 1278 10.1002/jnr.21232 (Pubitemid 46724370)
57. VN Uversky 2002 Natively unfolded proteins: a point where biology waits for physics Protein Sci 11 4 739 756 10.1110/ps.4210102 (Pubitemid 34241284)
58. VN Uversky CJ Oldfield AK Dunker 2008 Intrinsically disordered proteins in human diseases: introducing the D2 concept Annu Rev Biophys 37 215 246 10.1146/annurev.biophys.37.032807.125924
59. NF Visser AJ Heck 2008 Surface plasmon resonance mass spectrometry in proteomics Expert Rev Proteomics 5 3 425 433 10.1586/14789450.5.3.425 (Pubitemid 351871118)
60. DM Walsh DJ Selkoe 2004 Deciphering the molecular basis of memory failure in Alzheimer's disease Neuron 44 1 181 193 10.1016/j.neuron.2004.09.010 (Pubitemid 39348839)
61. CM Wischik M Novak PC Edwards A Klug W Tichelaar RA Crowther 1988 Structural characterization of the core of the paired helical filament of Alzheimer disease Proc Natl Acad Sci USA 85 13 4884 4888 10.1073/pnas.85.13.4884
62. CM Wischik M Novak HC Thogersen PC Edwards MJ Runswick R Jakes JE Walker C Milstein M Roth A Klug 1988 Isolation of a fragment of tau derived from the core of the paired helical filament of Alzheimer disease Proc Natl Acad Sci USA 85 12 4506 4510 10.1073/pnas.85.12.4506 (Pubitemid 18177785)
63. N Zilka P Filipcik P Koson L Fialova R Skrabana M Zilkova G Rolkova E Kontsekova M Novak 2006 Truncated tau from sporadic Alzheimer's disease suffices to drive neurofibrillary degeneration in vivo FEBS Lett 580 15 3582 3588 10.1016/j.febslet.2006.05.029 (Pubitemid 43902790)