Trimeric tau is toxic to human neuronal cells at low nanomolar concentrations

International Journal of Cell Biology

Volumn , Issue , 2013, Pages

  Tian, Huilai ^a   Davidowitz, Eliot ^b   Lopez, Patricia ^b   Emadi, Sharareh ^a   Moe, James ^b   Sierks, Michael ^a  

^a Arizona State University   (United States)

^b Oligomerix Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TAU PROTEIN;

ALZHEIMER DISEASE; ARTICLE; ATOMIC FORCE MICROSCOPY; CELL STRUCTURE; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; DISEASE COURSE; HUMAN; HUMAN CELL; NERVE CELL; NEUROBLASTOMA CELL; NEUROTOXICITY; PRIORITY JOURNAL;

EID: 84885463056     PISSN: 16878876     EISSN: 16878884     Source Type: Journal    
DOI: 10.1155/2013/260787     Document Type: Article

References (60)

1. Alzheimer's Association, 2012 Alzheimer's disease facts and figures. Alzheimer's and Dementia 2012 8 2 131 168 2-s2.0-84858225391 10.1016/j.jalz.2012.02.001
2. Alzheimer A., Über eine eigenartige Erkankung der Hirnrinde. Allgemeine Zeitschrift fur Psychiatrie und Phychish-Gerichtliche Medizin 1907 64 146 148
3. Hardy J., Selkoe D. J., The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 2002 297 5580 353 356 2-s2.0-0037135111 10.1126/science.1072994 (Pubitemid 34790756)
4. Gilman S., Koller M., Black R. S., Jenkins L., Griffith S. G., Fox N. C., Eisner L., Kirby L., Boada Rovira M., Forette F., Orgogozo J.-., Clinical effects of A β immunization (AN1792) in patients with AD in an interrupted trial. Neurology 2005 64 9 1553 1562 2-s2.0-20944448555 10.1212/01.WNL. 0000159740.16984.3C (Pubitemid 40617691)
5. Blennow K., Zetterberg H., Rinne J. O., Salloway S., Wei J., Black R., Grundman M., Liu E., Effect of immunotherapy with bapineuzumab on cerebrospinal fluid biomarker levels in patients with mild to moderate Alzheimer disease. Archives of Neurology 2012 69 8 1002 1010
6. Freeman G. B., Lin J. C., Pons J., Raha N. M., 39-week toxicity and toxicokinetic study of ponezumab (PF-04360365) in cynomolgus monkeys with 12-week recovery period. Journal of Alzheimer's Disease 2012 28 3 531 541 2-s2.0-84858047899 10.3233/JAD-2011-110869
7. Castellani R. J., Perry G., Pathogenesis and disease-modifying therapy in Alzheimer's disease: the flat line of progress. Archives of Medical Research 2012 43 8 694 698 10.1016/j.arcmed.2012.09.009
8. Braak H., Del Tredici K., The pathological process underlying Alzheimer's disease in individuals under thirty. Acta Neuropathologica 2011 121 2 171 181 2-s2.0-79451471618 10.1007/s00401-010-0789-4
9. Braak H., Braak E., Frequency of stages of Alzheimer-related lesions in different age categories. Neurobiology of Aging 1997 18 4 351 357 2-s2.0-0030805991 10.1016/S0197-4580(97)00056-0 (Pubitemid 27435070)
10. Oddo S., Vasilevko V., Caccamo A., Kitazawa M., Cribbs D. H., LaFerla F. M., Reduction of soluble A β and tau, but not soluble A β alone, ameliorates cognitive decline in transgenic mice with plaques and tangles. The Journal of Biological Chemistry 2006 281 51 39413 39423 2-s2.0-33846015514 10.1074/jbc.M608485200 (Pubitemid 46041901)
11. Weingarten M. D., Lockwood A. H., Hwo S. Y., Kirschner M. W., A protein factor essential for microtubule assembly. Proceedings of the National Academy of Sciences of the United States of America 1975 72 5 1858 1862 2-s2.0-0008538685
12. Witman G. B., Cleveland D. W., Weingarten M. D., Kirschner M. W., Tubulin requires tau for growth into microtubule initiating sites. Proceedings of the National Academy of Sciences of the United States of America 1976 73 11 4070 4074 2-s2.0-0017193352
13. Mandelkow E. M., Mandelkow E., Tau in Alzheimer's disease. Trends in Cell Biology 1998 8 11 425 427 2-s2.0-0032211829 10.1016/S0962-8924(98)01368-3 (Pubitemid 28529713)
14. Amos L. A., Microtubule structure and its stabilisation. Organic and Biomolecular Chemistry 2004 2 15 2153 2160 2-s2.0-4344572092 10.1039/b403634d
15. von Bergen M., Friedhoff P., Biernat J., Heberle J., Mandelkow E.-., Mandelkow E., Assembly of τ protein into Alzheimer paired helical filaments depends a local sequence motif (306VQIVYK311) forming β structure. Proceedings of the National Academy of Sciences of the United States of America 2000 97 10 5129 5134 2-s2.0-0034625060 10.1073/pnas.97.10.5129 (Pubitemid 30313683)
16. Thies E., Mandelkow E. M., Missorting of tau in neurons causes degeneration of synapses that can be rescued by the kinase MARK2/Par-1. Journal of Neuroscience 2007 27 11 2896 2907 2-s2.0-33947307791 10.1523/JNEUROSCI.4674- 06.2007 (Pubitemid 46438993)
17. Díaz-Hernández M., Gómez-Ramos A., Rubio A., Gómez-Villafuertes R., Naranjo J. R., Teresa Miras-Portugal M., Avila J., Tissue-nonspecific alkaline phosphatase promotes the neurotoxicity effect of extracellular tau. The Journal of Biological Chemistry 2010 285 42 32539 32548 2-s2.0-77957815617 10.1074/jbc.M110.145003
18. Pooler A. M., Phillips E. C., Lau D. H., Noble W., Hanger D. P., Physiological release of endogenous tau is stimulated by neuronal activity. EMBO Reports 2013 14 4 389 394 10.1038/embor.2013.15
19. Lasagna-Reeves C. A., Castillo-Carranza D. L., Sengupta U., Clos A. L., Jackson G. R., Kayed R., Tau oligomers impair memory and induce synaptic and mitochondrial dysfunction in wild-type mice. Molecular Neurodegeneration 2011 6 1, article 39 2-s2.0-79957913270 10.1186/1750-1326-6-39
20. Guillozet A. L., Weintraub S., Mash D. C., Mesulam M. M., Neurofibrillary tangles, amyloid, and memory in aging and mild cognitive impairment. Archives of Neurology 2003 60 5 729 736 2-s2.0-0038326624 10.1001/archneur.60.5.729 (Pubitemid 36569891)
21. Morris M., Maeda S., Vossel K., Mucke L., The many faces of tau. Neuron 2011 70 3 410 426 2-s2.0-79955670132 10.1016/j.neuron.2011.04.009
22. Haass C., Selkoe D. J., Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid β -peptide. Nature Reviews Molecular Cell Biology 2007 8 2 101 112 2-s2.0-33847662852 10.1038/nrm2101 (Pubitemid 46432529)
23. Kayed R., Head E., Thompson J. L., McIntire T. M., Milton S. C., Cotman C. W., Glabel C. G., Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 2003 300 5618 486 489 2-s2.0-0242668337 10.1126/science.1079469 (Pubitemid 36444329)
24. Lasagna-Reeves C. A., Castillo-Carranza D. L., Sengupta U., Sarmiento J., Troncoso J., Jackson G. R., Kayed R., Identification of oligomers at early stages of tau aggregation in Alzheimer's disease. The FASEB Journal 2012 26 5 1946 1959 10.1096/fj.11-199851
25. Morsch R., Simon W., Coleman P. D., Neurons may live for decades with neurofibrillary tangles. Journal of Neuropathology and Experimental Neurology 1999 58 2 188 197 2-s2.0-0033028074 (Pubitemid 29088942)
26. Kordower J. H., Chu Y., Stebbins G. T., DeKosky S. T., Cochran E. J., Bennett D., Mufson E. J., Loss and atrophy of layer II entorhinal cortex neurons in elderly people with mild cognitive impairment. Annals of Neurology 2001 49 2 202 213 (Pubitemid 32157996)
27. Brunden K. R., Trojanowski J. Q., Lee V. M., Evidence that non-fibrillar tau causes pathology linked to neurodegeneration and behavioral impairments. Journal of Alzheimer's Disease 2008 14 4 393 399 2-s2.0-49149083015
28. Santacruz K., Lewis J., Spires T., Paulson J., Kotilinek L., Ingelsson M., Guimaraes A., DeTure M., Ramsden M., McCowan E., Forster C., Yue M., Orne J., Janus C., Mariash A., Kuskowski M., Hyman B., Hutton M., Ashe K. H., Medicine: tau suppression in a neurodegenerative mouse model improves memory function. Science 2005 309 5733 476 481 2-s2.0-22344438508 10.1126/science. 1113694 (Pubitemid 40994688)
29. Andorfer C., Kress Y., Espinoza M., de Silva R., Tucker K. L., Barde Y., Duff K., Davies P., Hyperphosphorylation and aggregation of tau in mice expressing normal human tau isoforms. Journal of Neurochemistry 2003 86 3 582 590 2-s2.0-0041803006 10.1046/j.1471-4159.2003.01879.x (Pubitemid 36897439)
30. Leroy K., Bretteville A., Schindowski K., Gilissen E., Authelet M., de Decker R., Yilmaz Z., Buée L., Brion J., Early axonopathy preceding neurofibrillary tangles in mutant tau transgenic mice. The American Journal of Pathology 2007 171 3 976 992 2-s2.0-34548829896 10.2353/ajpath.2007.070345 (Pubitemid 47440995)
31. Spires T. L., Orne J. D., SantaCruz K., Pitstick R., Carlson G. A., Ashe K. H., Hyman B. T., Region-specific dissociation of neuronal loss and neurofibrillary pathology in a mouse model of tauopathy. The American Journal of Pathology 2006 168 5 1598 1607 2-s2.0-33646519920 10.2353/ajpath.2006.050840
32. Yoshiyama Y., Higuchi M., Zhang B., Huang S., Iwata N., Saido T., Maeda J., Suhara T., Trojanowski J. Q., Lee V. M.-., Synapse loss and microglial activation precede tangles in a P301S tauopathy mouse model. Neuron 2007 53 3 337 351 2-s2.0-33846538660 10.1016/j.neuron.2007.01.010 (Pubitemid 46161268)
33. Berger Z., Roder H., Hanna A., Carlson A., Rangachari V., Yue M., Wszolek Z., Ashe K., Knight J., Dickson D., Andorfer C., Rosenberry T. L., Lewis J., Hutton M., Janus C., Accumulation of pathological tau species and memory loss in a conditional model of tauopathy. Journal of Neuroscience 2007 27 14 3650 3662 2-s2.0-34147125835 10.1523/JNEUROSCI.0587-07.2007 (Pubitemid 46557687)
34. Maeda S., Sahara N., Saito Y., Murayama S., Ikai A., Takashima A., Increased levels of granular tau oligomers: an early sign of brain aging and Alzheimer's disease. Neuroscience Research 2006 54 3 197 201 2-s2.0-33244456786 10.1016/j.neures.2005.11.009 (Pubitemid 43276078)
35. Sahara N., Maeda S., Takashima A., Tau oligomerization: a role for tau aggregation intermediates linked to neurodegeneration. Current Alzheimer Research 2008 5 6 591 598 2-s2.0-58049214009 10.2174/156720508786898442
36. Ward S. M., Himmelstein D. S., Lancia J. K., Binder L. I., Tau oligomers and tau toxicity in neurodegenerative disease. Biochemical Society Transactions 2012 40 4 667 671 10.1042/BST20120134
37. Lasagna-Reeves C. A., Castillo-Carranza D. L., Sengupta U., Guerrero-Munoz M. J., Kiritoshi T., Neugebauer V., Jackson G. R., Kayed R., Alzheimer brain-derived tau oligomers propagate pathology from endogenous tau. Scientific Reports 2012 2 article 700 10.1038/srep00700
38. Genius J., Klafki H., Benninghoff J., Esselmann H., Wiltfang J., Current application of neurochemical biomarkers in the prediction and differential diagnosis of Alzheimer's disease and other neurodegenerative dementias. European Archives of Psychiatry and Clinical Neurosciences 2012 262 supplement 2 S71 S77 10.1007/s00406-012-0362-3
39. Barkhordarian H., Emadi S., Schulz P., Sierks M. R., Isolating recombinant antibodies against specific protein morphologies using atomic force microscopy and phage display technologies. Protein Engineering, Design and Selection 2006 19 11 497 502 2-s2.0-33750291199 10.1093/protein/gzl036 (Pubitemid 44627322)
40. Zameer A., Schulz P., Wang M. S., Sierks M. R., Single chain Fv antibodies against the 25-35 A β fragment inhibit aggregation and toxicity of A β 42. Biochemistry 2006 45 38 11532 11539 2-s2.0-33749034211 10.1021/bi060601o (Pubitemid 44454001)
41. Emadi S., Barkhordarian H., Wang M. S., Schulz P., Sierks M. R., Isolation of a human single chain antibody fragment against oligomeric α -synuclein that inhibits aggregation and prevents α -synuclein-induced toxicity. Journal of Molecular Biology 2007 368 4 1132 1144 2-s2.0-34147130637 10.1016/j.jmb.2007.02.089 (Pubitemid 46574670)
42. Zameer A., Kasturirangan S., Emadi S., Nimmagadda S. V., Sierks M. R., Anti-oligomeric A β single-chain variable domain antibody blocks A β -induced toxicity against human neuroblastoma cells. Journal of Molecular Biology 2008 384 4 917 928 2-s2.0-56249092747 10.1016/j.jmb.2008.09.068
43. Emadi S., Kasturirangan S., Wang M. S., Schulz P., Sierks M. R., Detecting morphologically distinct oligomeric forms of α -synuclein. The Journal of Biological Chemistry 2009 284 17 11048 11058 2-s2.0-66449097646 10.1074/jbc.M806559200
44. Wang M. S., Zameer A., Emadi S., Sierks M. R., Characterizing antibody specificity to different protein morphologies by AFM. Langmuir 2009 25 2 912 918 2-s2.0-60849137232 10.1021/la8025914
45. Pahlman S., Hoehner J. C., Nanberg E., Hedborg F., Fagerstrom S., Gestblom C., Johansson I., Larsson U., Lavenius E., Ortoft E., Soderholm H., Differentiation and survival influences of growth factors in human neuroblastoma. European Journal of Cancer A 1995 31 4 453 458 2-s2.0-0029033940 10.1016/0959-8049(95)00033-F
46. Encinas M., Iglesias M., Liu Y., Wang H., Muhaisen A., Ceña V., Gallego C., Comella J. X., Sequential treatment of SH-SY5Y cells with retinoic acid and brain-derived neurotrophic factor gives rise to fully differentiated, neurotrophic factor-dependent, human neuron-like cells. Journal of Neurochemistry 2000 75 3 991 1003 2-s2.0-0033844835 10.1046/j.1471-4159.2000. 0750991.x (Pubitemid 30660487)
47. Presgraves S. P., Ahmed T., Borwege S., Joyce J. N., Terminally differentiated SH-SY5Y cells provide a model system for studying neuroprotective effects of dopamine agonists. Neurotoxicity Research 2003 5 8 579 598 2-s2.0-2442426175 10.1007/BF03033178
48. Decker T., Lohmann-Matthes M. L., A quick and simple method for the quantitation of lactate dehydrogenase release in measurements of cellular cytotoxicity and tumor necrosis factor (TNF) activity. Journal of Immunological Methods 1988 115 1 61 69 2-s2.0-0023738916
49. Hardy J. A., Higgins G. A., Alzheimer's disease: the amyloid cascade hypothesis. Science 1992 256 5054 184 185 2-s2.0-0026597063
50. Ferreira S. T., Vieira M. N. N., de Felice F. G., Soluble protein oligomers as emerging toxins in Alzheimer's and other amyloid diseases. IUBMB Life 2007 59 4-5 332 345 2-s2.0-34248547813 10.1080/15216540701283882 (Pubitemid 46763764)
51. Varvel N. H., Bhaskar K., Patil A. R., Pimplikar S. W., Herrup K., Lamb B. T., A β oligomers induce neuronal cell cycle events in Alzheimer's disease. Journal of Neuroscience 2008 28 43 10786 10793 2-s2.0-58149151433 10.1523/JNEUROSCI.2441-08.2008
52. Kasturirangan S., Reasoner T., Schulz P., Boddapati S., Emadi S., Valla J., Sierks M. R., Isolation and characterization of antibody fragments selective for specific protein morphologies from nanogram antigen samples. Biotechnology Progress 2013 29 2 463 471 10.1002/btpr.1698
53. Sierks M. R., Chatterjee G., McGraw C., Kasturirangan S., Schulz P., Prasad S., CSF levels of oligomeric alpha-synuclein and β -amyloid as biomarkers for neurodegenerative disease. Integrative Biology 2011 3 12 1188 1196 2-s2.0-82355191922 10.1039/c1ib00018g
54. Andorfer C., Acker C. M., Kress Y., Hof P. R., Duff K., Davies P., Cell-cycle reentry and cell death in transgenic mice expressing nonmutant human tau isoforms. Journal of Neuroscience 2005 25 22 5446 5454 2-s2.0-20044367108 10.1523/JNEUROSCI.4637-04.2005 (Pubitemid 40770926)
55. Belarbi K., Schindowski K., Burnouf S., Caillierez R., Grosjean M., Demeyer D., Hamdane M., Sergeant N., Blum D., Buée L., Early tau pathology involving the septo-hippocampal pathway in a tau transgenic model: relevance to alzheimer's disease. Current Alzheimer Research 2009 6 2 152 157 2-s2.0-64549147983 10.2174/156720509787602843
56. Alonso A. D. C., Mederlyova A., Novak M., Grundke-Iqbal I., Iqbal K., Promotion of hyperphosphorylation by frontotemporal dementia tau mutations. The Journal of Biological Chemistry 2004 279 33 34873 34881 2-s2.0-4844219627 10.1074/jbc.M405131200 (Pubitemid 39318122)
57. Braak H., Rüb U., Schultz C., Del Tredici K., Vulnerability of cortical neurons to Alzheimer's and Parkinson's diseases. Journal of Alzheimer's Disease 2006 9 3, supplement 35 44 2-s2.0-33747432277 (Pubitemid 44253296)
58. Schliebs R., Arendt T., The cholinergic system in aging and neuronal degeneration. Behavioural Brain Research 2011 221 2 555 563 2-s2.0-79955727727 10.1016/j.bbr.2010.11.058
59. Wu J. W., Herman M., Liu L., Simoes S., Acker C. M., Figueroa H., Steinberg J. I., Margittai M., Kayed R., Zurzolo C., Di Paolo G., Duff K. E., Small misfolded tau species are internalized via bulk endocytosis and anterogradely and retrogradely transported in neurons. The Journal of Biological Chemistry 2013 288 3 1856 1870 10.1074/jbc.M112.394528
60. Glabe C. G., Common mechanisms of amyloid oligomer pathogenesis in degenerative disease. Neurobiology of Aging 2006 27 4 570 575 2-s2.0-33344463679 10.1016/j.neurobiolaging.2005.04.017 (Pubitemid 43290525)