Cis phosphorylated tau as the earliest detectable pathogenic conformation in Alzheimer disease, offering novel diagnostic and therapeutic strategies

References

• Blume-Jensen P, Hunter T. Oncogenic kinase signalling. Nature 2001; 411:355 - 65; http://dx.doi.org/10.1038/35077225; PMID: 11357143
   PubMed Web of Science ®Google Scholar
• Lu KP, Finn G, Lee TH, Nicholson LK. Prolyl cis-trans isomerization as a molecular timer. Nat Chem Biol 2007; 3:619 - 29; http://dx.doi.org/10.1038/nchembio.2007.35; PMID: 17876319
   PubMed Web of Science ®Google Scholar
• Lee TH, Pastorino L, Lu KP. Peptidyl-prolyl cis-trans isomerase Pin1 in ageing, cancer and Alzheimer disease. Expert Rev Mol Med 2011; 13:e21; http://dx.doi.org/10.1017/S1462399411001906; PMID: 21682951
   PubMed Web of Science ®Google Scholar
• Eckert B, Martin A, Balbach J, Schmid FX. Prolyl isomerization as a molecular timer in phage infection. Nat Struct Mol Biol 2005; 12:619 - 23; http://dx.doi.org/10.1038/nsmb946; PMID: 15937494
   PubMed Web of Science ®Google Scholar
• Sarkar P, Reichman C, Saleh T, Birge RB, Kalodimos CG. Proline cis-trans isomerization controls autoinhibition of a signaling protein. Mol Cell 2007; 25:413 - 26; http://dx.doi.org/10.1016/j.molcel.2007.01.004; PMID: 17289588
   PubMed Web of Science ®Google Scholar
• Sarkar P, Saleh T, Tzeng SR, Birge RB, Kalodimos CG. Structural basis for regulation of the Crk signaling protein by a proline switch. Nat Chem Biol 2011; 7:51 - 7; http://dx.doi.org/10.1038/nchembio.494; PMID: 21131971
   PubMed Web of Science ®Google Scholar
• Wang L, Yang F, Zhang D, Chen Z, Xu RM, Nierhaus KH, et al. A conserved proline switch on the ribosome facilitates the recruitment and binding of trGTPases. Nat Struct Mol Biol 2012; 19:403 - 10; http://dx.doi.org/10.1038/nsmb.2254; PMID: 22407015
   PubMed Web of Science ®Google Scholar
• Lummis SC, Beene DL, Lee LW, Lester HA, Broadhurst RW, Dougherty DA. Cis-trans isomerization at a proline opens the pore of a neurotransmitter-gated ion channel. Nature 2005; 438:248 - 52; http://dx.doi.org/10.1038/nature04130; PMID: 16281040
   PubMed Web of Science ®Google Scholar
• Nakamura K, Greenwood A, Binder L, Bigio EH, Denial S, Nicholson L, et al. Proline isomer-specific antibodies reveal the early pathogenic tau conformation in Alzheimer’s disease. Cell 2012; 149:232 - 44; http://dx.doi.org/10.1016/j.cell.2012.02.016; PMID: 22464332
   PubMed Web of Science ®Google Scholar
• Lu PJ, Wulf G, Zhou XZ, Davies P, Lu KP. The prolyl isomerase Pin1 restores the function of Alzheimer-associated phosphorylated tau protein. Nature 1999; 399:784 - 8; http://dx.doi.org/10.1038/21650; PMID: 10391244
   PubMed Web of Science ®Google Scholar
• Liou YC, Sun A, Ryo A, Zhou XZ, Yu ZX, Huang HK, et al. Role of the prolyl isomerase Pin1 in protecting against age-dependent neurodegeneration. Nature 2003; 424:556 - 61; http://dx.doi.org/10.1038/nature01832; PMID: 12891359
   PubMed Web of Science ®Google Scholar
• Zhou XZ, Kops O, Werner A, Lu PJ, Shen M, Stoller G, et al. Pin1-dependent prolyl isomerization regulates dephosphorylation of Cdc25C and tau proteins. Mol Cell 2000; 6:873 - 83; http://dx.doi.org/10.1016/S1097-2765(05)00083-3; PMID: 11090625
   PubMed Web of Science ®Google Scholar
• Lim J, Balastik M, Lee TH, Nakamura K, Liou YC, Sun A, et al. Pin1 has opposite effects on wild-type and P301L tau stability and tauopathy. J Clin Invest 2008; 118:1877 - 89; PMID: 18431510
   PubMed Web of Science ®Google Scholar
• Augustinack JC, Schneider A, Mandelkow EM, Hyman BT. Specific tau phosphorylation sites correlate with severity of neuronal cytopathology in Alzheimer’s disease. Acta Neuropathol 2002; 103:26 - 35; http://dx.doi.org/10.1007/s004010100423; PMID: 11837744
   PubMed Web of Science ®Google Scholar
• Luna-Muñoz J, Chávez-Macías L, García-Sierra F, Mena R. Earliest stages of tau conformational changes are related to the appearance of a sequence of specific phospho-dependent tau epitopes in Alzheimer’s disease. J Alzheimers Dis 2007; 12:365 - 75; PMID: 18198423
   PubMed Web of Science ®Google Scholar
• Luna-Muñoz J, García-Sierra F, Falcón V, Menéndez I, Chávez-Macías L, Mena R. Regional conformational change involving phosphorylation of tau protein at the Thr231, precedes the structural change detected by Alz-50 antibody in Alzheimer’s disease. J Alzheimers Dis 2005; 8:29 - 41; PMID: 16155347
   PubMed Web of Science ®Google Scholar
• Pal D, Chakrabarti P. Cis peptide bonds in proteins: residues involved, their conformations, interactions and locations. J Mol Biol 1999; 294:271 - 88; http://dx.doi.org/10.1006/jmbi.1999.3217; PMID: 10556045
   PubMed Web of Science ®Google Scholar
• Schutkowski M, Bernhardt A, Zhou XZ, Shen M, Reimer U, Rahfeld JU, et al. Role of phosphorylation in determining the backbone dynamics of the serine/threonine-proline motif and Pin1 substrate recognition. Biochemistry 1998; 37:5566 - 75; http://dx.doi.org/10.1021/bi973060z; PMID: 9548941
   PubMed Web of Science ®Google Scholar
• Stewart DE, Sarkar A, Wampler JE. Occurrence and role of cis peptide bonds in protein structures. J Mol Biol 1990; 214:253 - 60; http://dx.doi.org/10.1016/0022-2836(90)90159-J; PMID: 2370664
   PubMed Web of Science ®Google Scholar
• Davies CA, Mann DM, Sumpter PQ, Yates PO. A quantitative morphometric analysis of the neuronal and synaptic content of the frontal and temporal cortex in patients with Alzheimer’s disease. J Neurol Sci 1987; 78:151 - 64; http://dx.doi.org/10.1016/0022-510X(87)90057-8; PMID: 3572454
   PubMed Web of Science ®Google Scholar
• DeKosky ST, Scheff SW. Synapse loss in frontal cortex biopsies in Alzheimer’s disease: correlation with cognitive severity. Ann Neurol 1990; 27:457 - 64; http://dx.doi.org/10.1002/ana.410270502; PMID: 2360787
   PubMed Web of Science ®Google Scholar
• Scheff SW, DeKosky ST, Price DA. Quantitative assessment of cortical synaptic density in Alzheimer’s disease. Neurobiol Aging 1990; 11:29 - 37; http://dx.doi.org/10.1016/0197-4580(90)90059-9; PMID: 2325814
   PubMed Web of Science ®Google Scholar
• Orlicky S, Tang X, Willems A, Tyers M, Sicheri F. Structural basis for phosphodependent substrate selection and orientation by the SCFCdc4 ubiquitin ligase. Cell 2003; 112:243 - 56; http://dx.doi.org/10.1016/S0092-8674(03)00034-5; PMID: 12553912
   PubMed Web of Science ®Google Scholar
• Segat L, Pontillo A, Annoni G, Trabattoni D, Vergani C, Clerici M, et al. PIN1 promoter polymorphisms are associated with Alzheimer’s disease. Neurobiol Aging 2007; 28:69 - 74; http://dx.doi.org/10.1016/j.neurobiolaging.2005.11.009; PMID: 16384626
   PubMed Web of Science ®Google Scholar
• Sultana R, Boyd-Kimball D, Poon HF, Cai J, Pierce WM, Klein JB, et al. Oxidative modification and down-regulation of Pin1 in Alzheimer’s disease hippocampus: A redox proteomics analysis. Neurobiol Aging 2006; 27:918 - 25; http://dx.doi.org/10.1016/j.neurobiolaging.2005.05.005; PMID: 15950321
   PubMed Web of Science ®Google Scholar
• Ma SL, Tang NL, Tam CW, Lui VW, Lam LC, Chiu HF, et al. A PIN1 polymorphism that prevents its suppression by AP4 associates with delayed onset of Alzheimer’s disease. Neurobiol Aging 2012; 33:804 - 13; http://dx.doi.org/10.1016/j.neurobiolaging.2010.05.018; PMID: 20580132
   PubMed Web of Science ®Google Scholar
• Clavaguera F, Bolmont T, Crowther RA, Abramowski D, Frank S, Probst A, et al. Transmission and spreading of tauopathy in transgenic mouse brain. Nat Cell Biol 2009; 11:909 - 13; http://dx.doi.org/10.1038/ncb1901; PMID: 19503072
   PubMed Web of Science ®Google Scholar
• Asuni AA, Boutajangout A, Quartermain D, Sigurdsson EM. Immunotherapy targeting pathological tau conformers in a tangle mouse model reduces brain pathology with associated functional improvements. J Neurosci 2007; 27:9115 - 29; http://dx.doi.org/10.1523/JNEUROSCI.2361-07.2007; PMID: 17715348
   PubMed Web of Science ®Google Scholar
• Chai X, Wu S, Murray TK, Kinley R, Cella CV, Sims H, et al. Passive immunization with anti-Tau antibodies in two transgenic models: reduction of Tau pathology and delay of disease progression. J Biol Chem 2011; 286:34457 - 67; http://dx.doi.org/10.1074/jbc.M111.229633; PMID: 21841002
   PubMed Web of Science ®Google Scholar
• Spires-Jones TL, Kopeikina KJ, Koffie RM, de Calignon A, Hyman BT. Are tangles as toxic as they look?. J Mol Neurosci 2011; 45:438 - 44; http://dx.doi.org/10.1007/s12031-011-9566-7; PMID: 21638071
   PubMed Web of Science ®Google Scholar