Conformational targeting of intracellular A' 2 oligomers demonstrates their pathological oligomerization inside the endoplasmic reticulum

Nature Communications

Volumn 5, Issue , 2014, Pages

  Meli, Giovanni ^a   Lecci, Agnese ^a   Manca, Annalisa ^a   Krako, Nina ^a,b   Albertini, Valentina ^c   Benussi, Luisa ^c   Ghidoni, Roberta ^c   Cattaneo, Antonino ^a,b  

^a EUROPEAN BRAIN RESEARCH INSTITUTE   (Italy)

^b SCUOLA NORMALE SUPERIORE   (Italy)

^c IRCCS ISTITUTO CENTRO SAN GIOVANNI DI DIO FATEBENEFRATELLI   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; AMYLOID BETA PROTEIN; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; CELL PROTEIN; CYCLOHEXIMIDE; LYSOZYME; RECOMBINANT ANTIBODY; PROTEIN BINDING; SINGLE CHAIN FRAGMENT VARIABLE ANTIBODY;

CELL ORGANELLE; HOMEOSTASIS; NERVOUS SYSTEM DISORDER; PATHOLOGY; POLYMER; PROTEIN; RECOMBINATION;

ALZHEIMER DISEASE; ARTICLE; CELL FRACTIONATION; CONFORMATIONAL SELECTIVE INTERFERENCE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MATURATION; OLIGOMERIZATION; PATHOGENESIS; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN TARGETING; SECRETORY PATHWAY; SYNAPSE; ANIMAL; BIOLOGICAL MODEL; CHEMISTRY; CHO CELL LINE; CRICETULUS; EXTRACELLULAR SPACE; GENE SILENCING; HAMSTER; INTRACELLULAR SPACE; METABOLISM; PROTEIN PROCESSING; PROTEINOSIS; RAT; WESTERN BLOTTING;

AMYLOID BETA-PEPTIDES; ANIMALS; BLOTTING, WESTERN; CHO CELLS; CRICETINAE; CRICETULUS; ENDOPLASMIC RETICULUM; EXTRACELLULAR SPACE; GENE KNOCKDOWN TECHNIQUES; HUMANS; INTRACELLULAR SPACE; MODELS, BIOLOGICAL; PROTEIN AGGREGATION, PATHOLOGICAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; RATS; SINGLE-CHAIN ANTIBODIES; SUBCELLULAR FRACTIONS;

EID: 84901502442     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms4867     Document Type: Article

References (70)

1. Selkoe, D. J. Alzheimers disease: genes, proteins, and therapy. Physiol. Rev. 81, 741-766 (2001).
2. Selkoe, D. J. Cell biology of protein misfolding: the examples of Alzheimers and Parkinsons diseases. Nat. Cell Biol. 6, 1054-1061 (2004). (Pubitemid 39468006)
3. Shankar, G. M. & Walsh, D. M. Alzheimers disease: synaptic dysfunction and Abeta. Mol. Neurodegener. 4, 48 (2009).
4. Palop, J. J. & Mucke, L. Amyloid-beta-induced neuronal dysfunction in Alzheimers disease: from synapses toward neural networks. Nat. Neurosci. 13, 812-818 (2010).
5. Lichtenthaler, S. F., Haass, C. & Steiner, H. Regulated intramembrane proteolysis-lessons from amyloid precursor protein processing. J. Neurochem. 117, 779-796 (2011).
6. Sannerud, R. & Annaert, W. Trafficking, a key player in regulated intramembrane proteolysis. Semin. Cell Dev. Biol. 20, 183-190 (2009).
7. LaFerla, F. M., Green, K. N. & Oddo, S. Intracellular amyloid-beta in Alzheimers disease. Nat. Rev. Neurosci. 8, 499-509 (2007).
8. Benilova, I., Karran, E. & De Strooper, B. The toxic A[beta] oligomer and Alzheimers disease: an emperor in need of clothes. Nat. Neurosci. 15, 349-357 (2012).
9. Haass, C. & Selkoe, D. J. Soluble protein oligomers in neurodegeneration: lessons from the Alzheimers amyloid beta-peptide. Nat. Rev. Mol. Cell Biol. 8, 101-112 (2007). (Pubitemid 46432529)
10. Glabe, C. G. Conformation-dependent antibodies target diseases of protein misfolding. Trends Biochem. Sci. 29, 542-547 (2004). (Pubitemid 39265171)
11. Biocca, S., Neuberger, M. S. & Cattaneo, A. Expression and targeting of intracellular antibodies in mammalian cells. EMBO J. 9, 101-108 (1990).
12. Biocca, S. & Cattaneo, A. Intracellular immunization: antibody targeting to subcellular compartments. Trends Cell Biol. 5, 248-252 (1995).
13. Meli, G., Visintin, M., Cannistraci, I. & Cattaneo, A. Direct in vivo intracellular selection of conformation-sensitive antibody domains targeting Alzheimers amyloid-beta oligomers. J. Mol. Biol. 387, 584-606 (2009).
14. Takahashi, R. H. et al. Oligomerization of Alzheimers beta-amyloid within processes and synapses of cultured neurons and brain. J. Neurosci. 24, 3592-3599 (2004). (Pubitemid 38481116)
15. Gouras, G. K., Tampellini, D., Takahashi, R. H. & Capetillo-Zarate, E. Intraneuronal beta-amyloid accumulation and synapse pathology in Alzheimers disease. Acta. Neuropathol. 119, 523-541 (2010).
16. Lacor, P. N. et al. Synaptic targeting by Alzheimers-related amyloid beta oligomers. J. Neurosci. 24, 10191-10200 (2004). (Pubitemid 39492046)
17. Lambert, M. P. et al. Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc. Natl Acad. Sci. USA 95, 6448-6453 (1998).
18. Matrone, C. et al. Activation of the amyloidogenic route by NGF deprivation induces apoptotic death in PC12 Cells. J. Alzheimers Dis. 13, 81-96 (2008). (Pubitemid 351365629)
19. Capsoni, S. et al. Intranasal painless human nerve growth factors slows amyloid neurodegeneration and prevents memory deficits in App X PS1 mice. PLoS ONE 7, e37555 (2012).
20. Tiveron, C. et al. ProNGF\NGF imbalance triggers learning and memory deficits, neurodegeneration and spontaneous epileptic-like discharges in transgenic mice. Cell Death Differ. 20, 1017-1030 (2013).
21. Kayed, R. et al. Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300, 486-489 (2003). (Pubitemid 36444329)
22. Munro, S. & Pelham, H. R. A C-terminal signal prevents secretion of luminal ER proteins. Cell 48, 899-907 (1987).
23. Podlisny, M. B. et al. Aggregation of secreted amyloid beta-protein into sodium dodecyl sulfate-stable oligomers in cell culture. J. Biol. Chem. 270, 9564-9570 (1995).
24. Walsh, D. M. et al. Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416, 535-539 (2002). (Pubitemid 34288854)
25. Li, S. et al. Soluble oligomers of amyloid Beta protein facilitate hippocampal long-term depression by disrupting neuronal glutamate uptake. Neuron 62, 788-801 (2009).
26. Li, S. et al. Soluble Abeta oligomers inhibit long-term potentiation through a mechanism involving excessive activation of extrasynaptic NR2B-containing NMDA receptors. J. Neurosci. 31, 6627-6638 (2011).
27. Albertini, V. et al. Optimization protocol for amyloid-beta peptides detection in human cerebrospinal fluid using SELDI TOF MS. Proteomics Clin. Appl. 4, 352-357 (2010).
28. Ghidoni, R. et al. Novel T719P AbetaPP mutation unbalances the relative proportion of amyloid-beta peptides. J. Alzheimers Dis. 18, 295-303 (2009).
29. Shearman, M. S. et al. L-685,458, an aspartyl protease transition state mimic, is a potent inhibitor of amyloid beta-protein precursor gamma-secretase activity. Biochemistry 39, 8698-8704 (2000). (Pubitemid 30602778)
30. Kayed, R. et al. Conformation dependent monoclonal antibodies distinguish different replicating strains or conformers of prefibrillar Abeta oligomers. Mol. Neurodegener. 5, 57 (2010).
31. Baulac, S. et al. Functional gamma-secretase complex assembly in Golgi/trans- Golgi network: interactions among presenilin, nicastrin, Aph1, Pen-2, and gamma-secretase substrates. Neurobiol. Dis. 14, 194-204 (2003).
32. Zheng, H. & Koo, E. H. Biology and pathophysiology of the amyloid precursor protein. Mol. Neurodegener. 6, 27 (2011).
33. State of aggregation. Nat. Neurosci. 14, 399-399 (2011).
34. Choy, R. W., Cheng, Z. & Schekman, R. Amyloid precursor protein (APP) traffics from the cell surface via endosomes for amyloid beta (Abeta) production in the trans-Golgi network. Proc. Natl Acad. Sci. USA 109, E2077-E2082 (2012).
35. Guerriero, C. J. & Brodsky, J. L. The delicate balance between secreted protein folding and endoplasmic reticulum-associated degradation in human physiology. Physiol. Rev. 92, 537-576 (2012).
36. Vecchi, L., Petris, G., Bestagno, M. & Burrone, O. R. Selective targeting of proteins within secretory pathway for endoplasmic reticulum-associated degradation. J. Biol. Chem. 287, 20007-20015 (2012).
37. Hardingham, G. E. & Bading, H. Synaptic versus extrasynaptic NMDA receptor signalling: implications for neurodegenerative disorders. Nat. Rev. Neurosci. 11, 682-696 (2010).
38. Caccamo, A., Majumder, S., Richardson, A., Strong, R. & Oddo, S. Molecular interplay between mammalian target of rapamycin (mTOR), amyloid-beta, and Tau: effects on cognitive impairments. J. Biol. Chem. 285, 13107-13120 (2010).
39. Selkoe, D. J. Resolving controversies on the path to Alzheimers therapeutics. Nat. Med. 17, 1521 (2011).
40. De Strooper, B., Vassar, R. & Golde, T. The secretases: enzymes with therapeutic potential in Alzheimer disease. Nat. Rev. Neurol. 6, 99-107 (2010).
41. Paganetti, P., Calanca, V., Galli, C., Stefani, M. & Molinari, M. beta-site specific intrabodies to decrease and prevent generation of Alzheimers Abeta peptide. J. Cell Biol. 168, 863-868 (2005). (Pubitemid 40397001)
42. Hayashi, I. et al. Single chain variable fragment against nicastrin inhibits the gamma-secretase activity. J. Biol. Chem. 284, 27838-27847 (2009).
43. Chavez-Gutierrez, L. et al. The mechanism of gamma-Secretase dysfunction in familial Alzheimer disease. EMBO J. 31, 2261-2274 (2012).
44. Kuperstein, I. et al. Neurotoxicity of Alzheimers disease Abeta peptides is induced by small changes in the Abeta42 to Abeta40 ratio. EMBO J. 29, 3408-3420 (2010).
45. Cook, D. G. et al. Alzheimers A beta(1-42) is generated in the endoplasmic reticulum/intermediate compartment of NT2N cells. Nat. Med. 3, 1021-1023 (1997). (Pubitemid 27391958)
46. Hartmann, T. et al. Distinct sites of intracellular production for Alzheimers disease A beta40/42 amyloid peptides. Nat. Med. 3, 1016-1020 (1997). (Pubitemid 27391957)
47. Stine, Jr. W. B., Dahlgren, K. N., Krafft, G. A. & LaDu, M. J. In vitro characterization of conditions for amyloid-beta peptide oligomerization and fibrillogenesis. J. Biol. Chem. 278, 11612-11622 (2003). (Pubitemid 36792723)
48. Munishkina, L. A., Cooper, E. M., Uversky, V. N. & Fink, A. L. The effect of macromolecular crowding on protein aggregation and amyloid fibril formation. J. Mol. Recognit. 17, 456-464 (2004). (Pubitemid 39218989)
49. Hoshino, T. et al. Endoplasmic reticulum chaperones inhibit the production of amyloid-beta peptides. Biochem. J. 402, 581-589 (2007). (Pubitemid 46423895)
50. Hu, X. et al. Amyloid seeds formed by cellular uptake, concentration, and aggregation of the amyloid-beta peptide. Proc. Natl Acad. Sci. USA 106, 20324-20329 (2009).
51. Alavez, S., Vantipalli, M. C., Zucker, D. J., Klang, I. M. & Lithgow, G. J. Amyloid-binding compounds maintain protein homeostasis during ageing and extend lifespan. Nature 472, 226-229 (2011).
52. Krako, N. et al. Characterization of mitochondrial dysfunction in the 7PA2 cell model of Alzheimers disease. J. Alzheimers Dis. 37, 747-758 (2013).
53. Gouras, G. K., Almeida, C. G. & Takahashi, R. H. Intraneuronal Abeta accumulation and origin of plaques in Alzheimers disease. Neurobiol. Aging. 26, 1235-1244 (2005). (Pubitemid 41338539)
54. Lazarov, O., Lee, M., Peterson, D. A. & Sisodia, S. S. Evidence that synaptically released beta-amyloid accumulates as extracellular deposits in the hippocampus of transgenic mice. J. Neurosci. 22, 9785-9793 (2002). (Pubitemid 35332862)
55. Cirrito, J. R. et al. Synaptic activity regulates interstitial fluid amyloid-beta levels in vivo. Neuron 48, 913-922 (2005). (Pubitemid 41814696)
56. Tampellini, D. & Gouras, G. K. Synapses, synaptic activity and intraneuronal Ab in Alzheimers disease. Front. Aging Neurosci. 2, 13 (2010).
57. Cattaneo, A. & Biocca, S. Intracellular Antibodies: Development and Applications (Springer-Verlag, 1997).
58. Meli, G., Krako, N., Manca, A., Lecci, A. & Cattaneo, A. Intrabodies for protein interference in Alzheimers disease. J. Biol. Regul. Homeost. Agents. 27, 89-105 (2013).
59. Lemere, C. A. & Masliah, E. Can Alzheimer disease be prevented by amyloid-beta immunotherapy? Nat. Rev. Neurol. 6, 108-119 (2010).
60. Visintin, M., Tse, E., Axelson, H., Rabbitts, T. H. & Cattaneo, A. Selection of antibodies for intracellular function using a two-hybrid in vivo system. Proc. Natl Acad. Sci. USA 96, 11723-11728 (1999). (Pubitemid 29502799)
61. Visintin, M., Meli, G. A., Cannistraci, I. & Cattaneo, A. Intracellular antibodies for proteomics. J. Immunol. Methods 290, 135-153 (2004). (Pubitemid 38917136)
62. Persic, L. et al. Targeting vectors for intracellular immunisation. Gene 187, 1-8 (1997). (Pubitemid 27110428)
63. Martineau, P., Jones, P. & Winter, G. Expression of an antibody fragment at high levels in the bacterial cytoplasm. J. Mol. Biol. 280, 117-127 (1998). (Pubitemid 28312810)
64. Reyes, J. F. et al. Alpha-synuclein transfers from neurons to oligodendrocytes. Glia 62, 387-398 (2014).
65. Foley, J. et al. Structural fingerprints and their evolution during oligomeric vs. oligomer-free amyloid fibril growth. J. Chem. Phys. 139, 121901 (2013).
66. Navarra, G., Troia, F., Militello, V. & Leone, M. Characterization of the nucleation process of lysozyme at physiological pH: Primary but not sole process. Biophys. Chem. 177-178, 24-33 (2013).
67. Xia, W. et al. Presenilin 1 regulates the processing of beta-amyloid precursor protein C-terminal fragments and the generation of amyloid beta-protein in endoplasmic reticulum and Golgi. Biochemistry 37, 16465-16471 (1998). (Pubitemid 28543904)
68. Freir, D. B. et al. Interaction between prion protein and toxic amyloid beta assemblies can be therapeutically targeted at multiple sites. Nat. Commun. 2, 336 (2011).
69. Paoletti, F. et al. Direct intracellular selection and biochemical characterization of a recombinant anti-proNGF single chain antibody fragment. Arch. Biochem. Biophys. 522, 26-36 (2012).
70. Jan, A., Hartley, D. M. & Lashuel, H. A. Preparation and characterization of toxic Abeta aggregates for structural and functional studies in Alzheimers disease research. Nat. Protoc. 5, 1186-1209 (2010).