Exosomal cellular prion protein drives fibrillization of amyloid beta and counteracts amyloid beta-mediated neurotoxicity

Journal of Neurochemistry

Volumn 137, Issue 1, 2016, Pages 88-100

  Falker, Clemens ^a   Hartmann, Alexander ^a   Guett, Inga ^a   Dohler, Frank ^a   Altmeppen, Hermann ^a   Betzel, Christian ^b   Schubert, Robin ^b   Thurm, Dana ^a   Wegwitz, Florian ^c   Joshi, Pooja ^d   Verderio, Claudia ^d,e   Krasemann, Susanne ^a   Glatzel, Markus ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b UNIVERSITY OF HAMBURG   (Germany)

^c UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^d HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

^e CNR   (Italy)

Author keywords

Alzheimer's disease; amyloid beta; exosomes; neurodegeneration; neurotoxicity; prion protein knockout

Indexed keywords

AMYLOID BETA PROTEIN[1-42]; DIMER; OLIGOMER; PRION PROTEIN; AMYLOID; AMYLOID BETA PROTEIN; AMYLOID BETA-PROTEIN (1-42); PEPTIDE FRAGMENT; TUMOR PROTEIN;

ALZHEIMER DISEASE; ANIMAL CELL; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; EXOSOME; FIBRILLIZATION; HUMAN; HUMAN CELL; MOUSE; NERVE DEGENERATION; NEUROTOXICITY; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTECTION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN MODIFICATION; ANIMAL; GENE INACTIVATION; GENETIC TRANSFECTION; METABOLISM; NEUROBLASTOMA; PATHOLOGY; PHYSIOLOGY; SOLUBILITY; TUMOR CELL LINE;

ALZHEIMER DISEASE; AMYLOID; AMYLOID BETA-PEPTIDES; ANIMALS; CELL LINE, TUMOR; EXOSOMES; GENE KNOCKOUT TECHNIQUES; MICE; NEOPLASM PROTEINS; NEUROBLASTOMA; PEPTIDE FRAGMENTS; PRPC PROTEINS; SOLUBILITY; TRANSFECTION;

EID: 84959300206     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.13514     Document Type: Article

References (67)

1. Aad G., Abajyan T., Abbott B., et al,. (2013) Measurement of top quark polarization in top-antitop events from proton-proton collisions at radicals=7 TeV using the ATLAS detector. Phys. Rev. Lett. 111, 232002.
2. Agosta F., Dalla Libera D., Spinelli E. G., et al,. (2014) Myeloid microvesicles in cerebrospinal fluid are associated with myelin damage and neuronal loss in mild cognitive impairment and Alzheimer disease. Ann. Neurol. 76, 813-825.
3. Altmeppen H. C., Prox J., Puig B., et al,. (2011) Lack of a-disintegrin-and-metalloproteinase ADAM10 leads to intracellular accumulation and loss of shedding of the cellular prion protein in vivo. Mol. Neurodegener. 6, 36.
4. Altmeppen H. C., Prox J., Puig B., Dohler F., Falker C., Krasemann S., and, Glatzel M., (2013) Roles of endoproteolytic alpha-cleavage and shedding of the prion protein in neurodegeneration. FEBS J. 280, 4338-4347.
5. Altmeppen H. C., Prox J., Krasemann S., et al,. (2015) The sheddase ADAM10 is a potent modulator of prion disease. Elife. doi: 10.7554/eLife.04260.
6. An K., Klyubin I., Kim Y., et al,. (2013) Exosomes neutralize synaptic-plasticity-disrupting activity of Abeta assemblies in vivo. Mol. Brain 6, 47.
7. Ariga T., McDonald M. P., and, Yu R. K., (2008) Role of ganglioside metabolism in the pathogenesis of Alzheimer's disease-a review. J. Lipid Res. 49, 1157-1175.
8. Balducci C., Beeg M., Stravalaci M., et al,. (2010) Synthetic amyloid-beta oligomers impair long-term memory independently of cellular prion protein. Proc. Natl Acad. Sci. USA 107, 2295-2300.
9. Barry A. E., Klyubin I., Mc Donald J. M., Mably A. J., Farrell M. A., Scott M., Walsh D. M., and, Rowan M. J., (2011) Alzheimer's disease brain-derived amyloid-beta-mediated inhibition of LTP in vivo is prevented by immunotargeting cellular prion protein. J. Neurosci. 31, 7259-7263.
10. Bellingham S. A., Guo B. B., Coleman B. M., and, Hill A. F., (2012) Exosomes: vehicles for the transfer of toxic proteins associated with neurodegenerative diseases? Front. Physiol. 3, 124.
11. Benilova I., and, De Strooper B., (2010) Prion protein in Alzheimer's pathogenesis: a hot and controversial issue. EMBO Mol. Med. 2, 289-290.
12. Bobrie A., Colombo M., Krumeich S., Raposo G., and, Thery C., (2012) Diverse subpopulations of vesicles secreted by different intracellular mechanisms are present in exosome preparations obtained by differential ultracentrifugation. J. Extracell. Vesicles, doi: 10.3402/jev.v1i0.18397.
13. Calella A. M., Farinelli M., Nuvolone M., Mirante O., Moos R., Falsig J., Mansuy I. M., and, Aguzzi A., (2010) Prion protein and Abeta-related synaptic toxicity impairment. EMBO Mol. Med. 2, 306-314.
14. Capellari S., Parchi P., Russo C. M., Sanford J., Sy M. S., Gambetti P., and, Petersen R. B., (2000) Effect of the E200K mutation on prion protein metabolism. Comparative study of a cell model and human brain. Am. J. Pathol. 157, 613-622.
15. Cermak T., Doyle E. L., Christian M., et al,. (2011) Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Res. 39, e82.
16. Choi Y. J., Chae S., Kim J. H., Barald K. F., Park J. Y., and, Lee S. H., (2013) Neurotoxic amyloid beta oligomeric assemblies recreated in microfluidic platform with interstitial level of slow flow. Sci. Rep. 3, 1921.
17. Chung E., Ji Y., Sun Y., Kascsak R. J., Kascsak R. B., Mehta P. D., Strittmatter S. M., and, Wisniewski T., (2010) Anti-PrPC monoclonal antibody infusion as a novel treatment for cognitive deficits in an Alzheimer's disease model mouse. BMC Neurosci. 11, 130.
18. Cisse M., Duplan E., Guillot-Sestier M. V., et al,. (2011) The extracellular regulated kinase-1 (ERK1) controls regulated alpha-secretase-mediated processing, promoter transactivation, and mRNA levels of the cellular prion protein. J. Biol. Chem. 286, 29192-29206.
19. Danzer K. M., Kranich L. R., Ruf W. P., Cagsal-Getkin O., Winslow A. R., Zhu L., Vanderburg C. R., and, McLean P. J., (2012) Exosomal cell-to-cell transmission of alpha synuclein oligomers. Mol. Neurodegener. 7, 42.
20. Dinkins M. B., Dasgupta S., Wang G., Zhu G., and, Bieberich E., (2014) Exosome reduction in vivo is associated with lower amyloid plaque load in the 5XFAD mouse model of Alzheimer's disease. Neurobiol. Aging 35, 1792-1800.
21. Dohler F., Sepulveda-Falla D., Krasemann S., Altmeppen H., Schluter H., Hildebrand D., Zerr I., Matschke J., and, Glatzel M., (2014) High molecular mass assemblies of amyloid-beta oligomers bind prion protein in patients with Alzheimer's disease. Brain 137, 873-886.
22. Doyle E. L., Booher N. J., Standage D. S., Voytas D. F., Brendel V. P., Vandyk J. K., and, Bogdanove A. J., (2012) TAL Effector-Nucleotide Targeter (TALE-NT) 2.0: tools for TAL effector design and target prediction. Nucleic Acids Res. 40, W117-W122.
23. Fitzner D., Schnaars M., van Rossum D., Krishnamoorthy G., Dibaj P., Bakhti M., Regen T., Hanisch U. K., and, Simons M., (2011) Selective transfer of exosomes from oligodendrocytes to microglia by macropinocytosis. J. Cell Sci. 124, 447-458.
24. Fluharty B. R., Biasini E., Stravalaci M., et al,. (2013) An N-terminal fragment of the prion protein binds to amyloid-beta oligomers and inhibits their neurotoxicity in vivo. J. Biol. Chem. 288, 7857-7866.
25. Freir D. B., Nicoll A. J., Klyubin I., et al,. (2011) Interaction between prion protein and toxic amyloid beta assemblies can be therapeutically targeted at multiple sites. Nat. Commun. 2, 336.
26. Gimbel D. A., Nygaard H. B., Coffey E. E., Gunther E. C., Lauren J., Gimbel Z. A., and, Strittmatter S. M., (2010) Memory impairment in transgenic Alzheimer mice requires cellular prion protein. J. Neurosci. 30, 6367-6374.
27. Glatzel M., Linsenmeier L., Dohler F., Krasemann S., Puig B., and, Altmeppen H. C., (2015) Shedding light on prion disease. Prion 9, 244-256.
28. Goetzl E. J., Boxer A., Schwartz J. B., Abner E. L., Petersen R. C., Miller B. L., and, Kapogiannis D., (2015) Altered lysosomal proteins in neural-derived plasma exosomes in preclinical Alzheimer disease. Neurology 85, 40-47.
29. Hagel C., Krasemann S., Loffler J., Puschel K., Magnus T., and, Glatzel M., (2015) Upregulation of Shiga toxin receptor CD77/Gb3 and interleukin-1beta expression in the brain of EHEC patients with hemolytic uremic syndrome and neurologic symptoms. Brain Pathol. 25, 146-156.
30. Hardy J., and, Selkoe D. J., (2002) The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297, 353-356.
31. Joshi P., Turola E., Ruiz A., et al,. (2014) Microglia convert aggregated amyloid-beta into neurotoxic forms through the shedding of microvesicles. Cell Death Differ. 21, 582-593.
32. Kalani A., Tyagi A., and, Tyagi N., (2014) Exosomes: mediators of neurodegeneration, neuroprotection and therapeutics. Mol. Neurobiol. 49, 590-600.
33. Kessels H. W., Nguyen L. N., Nabavi S., and, Malinow R., (2010) The prion protein as a receptor for amyloid-beta. Nature 466, E3-E4; discussion E4-5.
34. Kuwahara C., Takeuchi A. M., Nishimura T., et al,. (1999) Prions prevent neuronal cell-line death. Nature 400, 225-226.
35. Larson M., Sherman M. A., Amar F., Nuvolone M., Schneider J. A., Bennett D. A., Aguzzi A., and, Lesne S. E., (2012) The complex PrPc-Fyn couples human oligomeric Abeta with pathological tau changes in Alzheimer's disease. J. Neurosci. 32, 16857-16871.
36. Lauren J., Gimbel D. A., Nygaard H. B., Gilbert J. W., and, Strittmatter S. M., (2009) Cellular prion protein mediates impairment of synaptic plasticity by amyloid-beta oligomers. Nature 457, 1128-1132.
37. Lesne S., Koh M. T., Kotilinek L., Kayed R., Glabe C. G., Yang A., Gallagher M., and, Ashe K. H., (2006) A specific amyloid-beta protein assembly in the brain impairs memory. Nature 440, 352-357.
38. Liu C. G., Song J., Zhang Y. Q., and, Wang P. C., (2014) MicroRNA-193b is a regulator of amyloid precursor protein in the blood and cerebrospinal fluid derived exosomal microRNA-193b is a biomarker of Alzheimer's disease. Mol. Med. Rep. 10, 2395-2400.
39. Morley J. E., Farr S. A., Banks W. A., Johnson S. N., Yamada K. A., and, Xu L., (2010) A physiological role for amyloid-beta protein:enhancement of learning and memory. J. Alzheimers Dis. 19, 441-449.
40. Moscou M. J., and, Bogdanove A. J., (2009) A simple cipher governs DNA recognition by TAL effectors. Science 326, 1501.
41. Nieznanski K., Choi J. K., Chen S., Surewicz K., and, Surewicz W. K., (2012) Soluble prion protein inhibits amyloid-beta (Abeta) fibrillization and toxicity. J. Biol. Chem. 287, 33104-33108.
42. O'Nuallain B., Freir D. B., Nicoll A. J., Risse E., Ferguson N., Herron C. E., Collinge J., and, Walsh D. M., (2010) Amyloid beta-protein dimers rapidly form stable synaptotoxic protofibrils. J. Neurosci. 30, 14411-14419.
43. Ostapchenko V. G., Beraldo F. H., Guimaraes A. L., Mishra S., Guzman M., Fan J., Martins V. R., Prado V. F., and, Prado M. A., (2013) Increased prion protein processing and expression of metabotropic glutamate receptor 1 in a mouse model of Alzheimer's disease. J. Neurochem. 127, 415-425.
44. Perera W. S., and, Hooper N. M., (2001) Ablation of the metal ion-induced endocytosis of the prion protein by disease-associated mutation of the octarepeat region. Curr. Biol. 11, 519-523.
45. Provencher S. W., (1982) A constrained regularization method for inverting data represented by linear algebraic or integral-equations. Comput. Phys. Commun. 27, 213-227.
46. Querfurth H. W., and, LaFerla F. M., (2010) Alzheimer's disease. N. Engl. J. Med. 362, 329-344.
47. Rajendran L., Honsho M., Zahn T. R., Keller P., Geiger K. D., Verkade P., and, Simons K., (2006) Alzheimer's disease beta-amyloid peptides are released in association with exosomes. Proc. Natl Acad. Sci. USA 103, 11172-11177.
48. Raposo F., Fernandez-Cegri V., De la Rubia M. A., et al,. (2011) Biochemical methane potential (BMP) of solid organic substrates: evaluation of anaerobic biodegradability using data from an international interlaboratory study. J. Chem. Technol. Biotechnol. 86, 1088-1098.
49. Renner M., Lacor P. N., Velasco P. T., Xu J., Contractor A., Klein W. L., and, Triller A., (2010) Deleterious effects of amyloid beta oligomers acting as an extracellular scaffold for mGluR5. Neuron 66, 739-754.
50. Resenberger U. K., Harmeier A., Woerner A. C., et al,. (2011) The cellular prion protein mediates neurotoxic signalling of beta-sheet-rich conformers independent of prion replication. EMBO J. 30, 2057-2070.
51. Resenberger U. K., Winklhofer K. F., and, Tatzelt J., (2012) Cellular prion protein mediates toxic signaling of amyloid beta. Neurodegener. Dis. 10, 298-300.
52. Rushworth J. V., Griffiths H. H., Watt N. T., and, Hooper N. M., (2013) Prion protein-mediated toxicity of amyloid-beta oligomers requires lipid rafts and the transmembrane LRP1. J. Biol. Chem. 288, 8935-8951.
53. Sanghera N., Correia B. E., Correia J. R., et al,. (2011) Deciphering the molecular details for the binding of the prion protein to main ganglioside GM1 of neuronal membranes. Chem. Biol. 18, 1422-1431.
54. Simons M., and, Raposo G., (2009) Exosomes-vesicular carriers for intercellular communication. Curr. Opin. Cell Biol. 21, 575-581.
55. Simpson R. J., (2008) Quantifying protein by bicinchoninic Acid. CSH Protoc. 2008, Pdb prot4722.
56. Tanzi R. E., and, Bertram L., (2005) Twenty years of the Alzheimer's disease amyloid hypothesis: a genetic perspective. Cell 120, 545-555.
57. Tauro B. J., Greening D. W., Mathias R. A., Ji H., Mathivanan S., Scott A. M., and, Simpson R. J., (2012) Comparison of ultracentrifugation, density gradient separation, and immunoaffinity capture methods for isolating human colon cancer cell line LIM1863-derived exosomes. Methods 56, 293-304.
58. Um J. W., Nygaard H. B., Heiss J. K., Kostylev M. A., Stagi M., Vortmeyer A., Wisniewski T., Gunther E. C., and, Strittmatter S. M., (2012) Alzheimer amyloid-beta oligomer bound to postsynaptic prion protein activates Fyn to impair neurons. Nat. Neurosci. 15, 1227-1235.
59. Um J. W., Kaufman A. C., Kostylev M., et al,. (2013) Metabotropic glutamate receptor 5 is a coreceptor for Alzheimer abeta oligomer bound to cellular prion protein. Neuron 79, 887-902.
60. Utsumi M., Yamaguchi Y., Sasakawa H., Yamamoto N., Yanagisawa K., and, Kato K., (2009) Up-and-down topological mode of amyloid beta-peptide lying on hydrophilic/hydrophobic interface of ganglioside clusters. Glycoconj. J. 26, 999-1006.
61. Vella L. J., Greenwood D. L., Cappai R., Scheerlinck J. P., and, Hill A. F., (2008) Enrichment of prion protein in exosomes derived from ovine cerebral spinal fluid. Vet. Immunol. Immunopathol. 124, 385-393.
62. Walsh D. M., Klyubin I., Fadeeva J. V., Cullen W. K., Anwyl R., Wolfe M. S., Rowan M. J., and, Selkoe D. J., (2002) Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416, 535-539.
63. Wik L., Klingeborn M., Willander H., and, Linne T., (2012) Separate mechanisms act concurrently to shed and release the prion protein from the cell. Prion 6, 498-509.
64. Younan N. D., Sarell C. J., Davies P., Brown D. R., and, Viles J. H., (2013) The cellular prion protein traps Alzheimer's Abeta in an oligomeric form and disassembles amyloid fibers. FASEB J. 27, 1847-1858.
65. Yuyama K., Sun H., Mitsutake S., and, Igarashi Y., (2012) Sphingolipid-modulated exosome secretion promotes clearance of amyloid-beta by microglia. J. Biol. Chem. 287, 10977-10989.
66. Yuyama K., Sun H., Sakai S., et al,. (2014) Decreased amyloid-beta pathologies by intracerebral loading of glycosphingolipid-enriched exosomes in Alzheimer model mice. J. Biol. Chem. 289, 24488-24498.
67. Yuyama K., Sun H., Usuki S., et al,. (2015) A potential function for neuronal exosomes: sequestering intracerebral amyloid-beta peptide. FEBS Lett. 589, 84-88.