Abstract
An increasing number of studies have demonstrated the existence of multiple conformational entities of tau, as have been observed for prion protein. We have developed and optimized techniques to isolate and study oligomeric tau strains both in vitro and ex vivo. Moreover, we have modified protocols that demonstrate the seeding properties of oligomeric tau strains that are capable of propagating in vivo. These methods and protocols are explained in this chapter.
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References
Colby DW, Prusiner SB (2011) Prions. Cold Spring Harb Perspect Biol 3(1):a006833. https://doi.org/10.1101/cshperspect.a006833
Prusiner SB (2013) Biology and genetics of prions causing neurodegeneration. Annu Rev Genet 47:601–623. https://doi.org/10.1146/annurev-genet-110711-155524
Morales R (2017) Prion strains in mammals: different conformations leading to disease. PLoS Pathog 13(7):e1006323. https://doi.org/10.1371/journal.ppat.1006323
Stohr J, Watts JC, Mensinger ZL, Oehler A, Grillo SK, DeArmond SJ, Prusiner SB, Giles K (2012) Purified and synthetic Alzheimer’s amyloid beta (Abeta) prions. Proc Natl Acad Sci U S A 109(27):11025–11030. https://doi.org/10.1073/pnas.1206555109
Watts JC, Condello C, Stohr J, Oehler A, Lee J, DeArmond SJ, Lannfelt L, Ingelsson M, Giles K, Prusiner SB (2014) Serial propagation of distinct strains of Abeta prions from Alzheimer's disease patients. Proc Natl Acad Sci U S A 111(28):10323–10328. https://doi.org/10.1073/pnas.1408900111
Prusiner SB, Woerman AL, Mordes DA, Watts JC, Rampersaud R, Berry DB, Patel S, Oehler A, Lowe JK, Kravitz SN, Geschwind DH, Glidden DV, Halliday GM, Middleton LT, Gentleman SM, Grinberg LT, Giles K (2015) Evidence for alpha-synuclein prions causing multiple system atrophy in humans with parkinsonism. Proc Natl Acad Sci U S A 112(38):E5308–E5317. https://doi.org/10.1073/pnas.1514475112
Goedert M, Spillantini MG (2017) Propagation of tau aggregates. Mol Brain 10(1):18. https://doi.org/10.1186/s13041-017-0298-7
Clos AL, Lasagna-Reeves CA, Castillo-Carranza DL, Sengupta U, Jackson GR, Kelly B, Beachkofsky TM, Kayed R (2011) Formation of immunoglobulin light chain amyloid oligomers in primary cutaneous nodular amyloidosis. Br J Dermatol 165(6):1349–1354. https://doi.org/10.1111/j.1365-2133.2011.10508.x
Fa M, Puzzo D, Piacentini R, Staniszewski A, Zhang H, Baltrons MA, Li Puma DD, Chatterjee I, Li J, Saeed F, Berman HL, Ripoli C, Gulisano W, Gonzalez J, Tian H, Costa JA, Lopez P, Davidowitz E, Yu WH, Haroutunian V, Brown LM, Palmeri A, Sigurdsson EM, Duff KE, Teich AF, Honig LS, Sierks M, Moe JG, D'Adamio L, Grassi C, Kanaan NM, Fraser PE, Arancio O (2016) Extracellular tau oligomers produce an immediate impairment of LTP and memory. Sci Rep 6:19393. https://doi.org/10.1038/srep19393
Ward SM, Himmelstein DS, Lancia JK, Binder LI (2012) Tau oligomers and tau toxicity in neurodegenerative disease. Biochem Soc Trans 40(4):667–671. https://doi.org/10.1042/BST20120134
Castillo-Carranza DL, Gerson JE, Sengupta U, Guerrero-Munoz MJ, Lasagna-Reeves CA, Kayed R (2014) Specific targeting of tau oligomers in Htau mice prevents cognitive impairment and tau toxicity following injection with brain-derived tau oligomeric seeds. J Alzheimers Dis 40(Suppl 1):S97–S111. https://doi.org/10.3233/JAD-132477
Lasagna-Reeves CA, Castillo-Carranza DL, Sengupta U, Guerrero-Munoz MJ, Kiritoshi T, Neugebauer V, Jackson GR, Kayed R (2012) Alzheimer brain-derived tau oligomers propagate pathology from endogenous tau. Sci Rep 2:700. https://doi.org/10.1038/srep00700
Lasagna-Reeves CA, Castillo-Carranza DL, Sengupta U, Sarmiento J, Troncoso J, Jackson GR, Kayed R (2012) Identification of oligomers at early stages of tau aggregation in Alzheimer’s disease. FASEB J 26(5):1946–1959. https://doi.org/10.1096/fj.11-199851
Gerson JE, Sengupta U, Kayed R (2017) Tau oligomers as pathogenic seeds: preparation and propagation in vitro and in vivo. In: Smet-Nocca C (ed) Tau protein: methods and protocols. Springer, New York, NY, pp 141–157. https://doi.org/10.1007/978-1-4939-6598-4_9
Kaufman SK, Thomas TL, Del Tredici K, Braak H, Diamond MI (2017) Characterization of tau prion seeding activity and strains from formaldehyde-fixed tissue. Acta Neuropathol Commun 5:41. https://doi.org/10.1186/s40478-017-0442-8
Sanders DW, Kaufman SK, DeVos SL, Sharma AM, Mirbaha H, Li A, Barker SJ, Foley A, Thorpe JR, Serpell LC, Miller TM, Grinberg LT, Seeley WW, Diamond MI (2014) Distinct tau prion strains propagate in cells and mice and define different tauopathies. Neuron 82(6):1271–1288. https://doi.org/10.1016/j.neuron.2014.04.047
Gerson JE, Sengupta U, Lasagna-Reeves CA, Guerrero-Munoz MJ, Troncoso J, Kayed R (2014) Characterization of tau oligomeric seeds in progressive supranuclear palsy. Acta Neuropathol Commun 2:73. https://doi.org/10.1186/2051-5960-2-73
Holmes BB, Furman JL, Mahan TE, Yamasaki TR, Mirbaha H, Eades WC, Belaygorod L, Cairns NJ, Holtzman DM, Diamond MI (2014) Proteopathic tau seeding predicts tauopathy in vivo. Proc Natl Acad Sci U S A 111(41):E4376–E4385. https://doi.org/10.1073/pnas.1411649111
Clavaguera F, Akatsu H, Fraser G, Crowther RA, Frank S, Hench J, Probst A, Winkler DT, Reichwald J, Staufenbiel M, Ghetti B, Goedert M, Tolnay M (2013) Brain homogenates from human tauopathies induce tau inclusions in mouse brain. Proc Natl Acad Sci 110(23):9535–9540. https://doi.org/10.1073/pnas.1301175110
Taraboulos A, Jendroska K, Serban D, Yang SL, DeArmond SJ, Prusiner SB (1992) Regional mapping of prion proteins in brain. Proc Natl Acad Sci U S A 89(16):7620–7624
Safar J, Wille H, Itri V, Groth D, Serban H, Torchia M, Cohen FE, Prusiner SB (1998) Eight prion strains have PrPSc molecules with different conformations. Nat Med 4(10):1157–1165
Choi YP, Peden AH, Gröner A, Ironside JW, Head MW (2010) Distinct stability states of disease-associated human prion protein identified by conformation-dependent immunoassay. J Virol 84(22):12030–12038. https://doi.org/10.1128/JVI.01057-10
Eenjes E, Dragich JM, Kampinga HH, Yamamoto A (2016) Distinguishing aggregate formation and aggregate clearance using cell based assays. J Cell Sci 129(6):1260–1270
Castillo-Carranza DL, Sengupta U, Guerrero-Muñoz MJ, Lasagna-Reeves CA, Gerson JE, Singh G, Estes DM, Barrett ADT, Dineley KT, Jackson GR, Kayed R (2014) Passive immunization with tau oligomer monoclonal antibody reverses tauopathy phenotypes without affecting hyperphosphorylated neurofibrillary tangles. J Neurosci 34(12):4260–4272. https://doi.org/10.1523/jneurosci.3192-13.2014
Guerrero-Munoz MJ, Castillo-Carranza DL, Sengupta U, White MA, Kayed R (2013) Design of metastable beta-sheet oligomers from natively unstructured peptide. ACS Chem Neurosci 4(12):1520–1523. https://doi.org/10.1021/cn4001395
Ramachandran G (2017) Fourier transform infrared (FTIR) spectroscopy, ultraviolet resonance raman (UVRR) spectroscopy, and atomic force microscopy (AFM) for study of the kinetics of formation and structural characterization of tau fibrils. In: Smet-Nocca C (ed) Tau protein: methods and protocols. Springer New York, New York, NY, pp 113–128. https://doi.org/10.1007/978-1-4939-6598-4_7
Nanavaty N, Lin L, Hinckley SH, Kuret J (2017) Detection and quantification methods for fibrillar products of in vitro tau aggregation assays. In: Smet-Nocca C (ed) Tau protein: methods and protocols. Springer New York, New York, pp 101–111. https://doi.org/10.1007/978-1-4939-6598-4_6
Jiménez JL, Guijarro JI, Orlova E, Zurdo J, Dobson CM, Sunde M, Saibil HR (1999) Cryo-electron microscopy structure of an SH3 amyloid fibril and model of the molecular packing. EMBO J 18(4):815–821. https://doi.org/10.1093/emboj/18.4.815
Jiménez JL, Nettleton EJ, Bouchard M, Robinson CV, Dobson CM, Saibil HR (2002) The protofilament structure of insulin amyloid fibrils. Proc Natl Acad Sci 99(14):9196–9201. https://doi.org/10.1073/pnas.142459399
Furman JL, Holmes BB, Diamond MI (2015) Sensitive detection of proteopathic seeding activity with FRET flow cytometry. J Vis Exp 106:e53205. https://doi.org/10.3791/53205
Clavaguera F, Bolmont T, Crowther RA, Abramowski D, Frank S, Probst A, Fraser G, Stalder AK, Beibel M, Staufenbiel M, Jucker M, Goedert M, Tolnay M (2009) Transmission and spreading of tauopathy in transgenic mouse brain. Nat Cell Biol 11(7):909–913. https://doi.org/10.1038/ncb1901
Golub VM, Brewer J, Wu X, Kuruba R, Short J, Manchi M, Swonke M, Younus I, Reddy DS (2015) Neurostereology protocol for unbiased quantification of neuronal injury and neurodegeneration. Front Aging Neurosci 7:196. https://doi.org/10.3389/fnagi.2015.00196
Crisostomo AC, Dang L, Digambaranath JL, Klaver AC, Loeffler DA, Payne JJ, Smith LM, Yokom AL, Finke JM (2015) Kinetic analysis of IgG antibodies to beta-amyloid oligomers with surface plasmon resonance. Anal Biochem 481:43–54. https://doi.org/10.1016/j.ab.2015.03.032
Hearty S, Leonard P, O'Kennedy R (2012) Measuring antibody-antigen binding kinetics using surface plasmon resonance. Methods Mol Biol 907:411–442. https://doi.org/10.1007/978-1-61779-974-7_24
Karlsson R, Katsamba PS, Nordin H, Pol E, Myszka DG (2006) Analyzing a kinetic titration series using affinity biosensors. Anal Biochem 349(1):136–147. https://doi.org/10.1016/j.ab.2005.09.034
Margittai M, Langen R (2004) Template-assisted filament growth by parallel stacking of tau. Proc Natl Acad Sci U S A 101(28):10278–10283. https://doi.org/10.1073/pnas.0401911101
Siddiqua A, Margittai M (2010) Three- and four-repeat tau coassemble into heterogeneous filaments: an implication for Alzheimer disease. J Biol Chem 285(48):37920–37926. https://doi.org/10.1074/jbc.M110.185728
Chai X, Wu S, Murray TK, Kinley R, Cella CV, Sims H, Buckner N, Hanmer J, Davies P, O'Neill MJ, Hutton ML, Citron M (2011) Passive immunization with anti-tau antibodies in two transgenic models: reduction of tau pathology and delay of disease progression. J Biol Chem 286(39):34457–34467. https://doi.org/10.1074/jbc.M111.229633
Combs B, Hamel C, Kanaan NM (2016) Pathological conformations involving the amino terminus of tau occur early in Alzheimer’s disease and are differentially detected by monoclonal antibodies. Neurobiol Dis 94:18–31. https://doi.org/10.1016/j.nbd.2016.05.016
Nakamura K, Greenwood A, Binder L, Bigio EH, Denial S, Nicholson L, Zhou XZ, Lu KP (2012) Proline isomer-specific antibodies reveal the early pathogenic tau conformation in Alzheimer’s disease. Cell 149(1):232–244. https://doi.org/10.1016/j.cell.2012.02.016
Petry FR, Pelletier J, Bretteville A, Morin F, Calon F, Hébert SS, Whittington RA, Planel E (2014) Specificity of anti-tau antibodies when analyzing mice models of Alzheimer’s disease: problems and solutions. PLoS One 9(5):e94251. https://doi.org/10.1371/journal.pone.0094251
Rosseels J, Van den Brande J, Violet M, Jacobs D, Grognet P, Lopez J, Huvent I, Caldara M, Swinnen E, Papegaey A, Caillierez R, Buée-Scherrer V, Engelborghs S, Lippens G, Colin M, Buée L, Galas M-C, Vanmechelen E, Winderickx J (2015) Tau monoclonal antibody generation based on humanized yeast models: impact on tau oligomerization and diagnostics. J Biol Chem 290(7):4059–4074. https://doi.org/10.1074/jbc.M114.627919
Acknowledgment
We thank Kayed lab members for their contributions in developing and optimizing the protocols and providing us with their helpful suggestions. This work was supported by grants from NIH RF1AG055771, RO1AG054025 and RO1NS094557, and The Gillson Longenbaugh Foundation.
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Sengupta, U., Carretero-Murillo, M., Kayed, R. (2018). Preparation and Characterization of Tau Oligomer Strains. In: Sigurdsson, E., Calero, M., Gasset, M. (eds) Amyloid Proteins. Methods in Molecular Biology, vol 1779. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-7816-8_9
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DOI: https://doi.org/10.1007/978-1-4939-7816-8_9
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