Stimulating the release of exosomes increases the intercellular transfer of prions

Journal of Biological Chemistry

Volumn 291, Issue 10, 2016, Pages 5128-5137

  Guo, Belinda B ^a,b   Bellingham, Shayne A ^a,b   Hill, Andrew F ^a,b,c  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c LA TROBE UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; CYTOLOGY; IONOPHORES; NUCLEIC ACIDS; PROTEINS; YARN;

ALZHEIMER DISEASE; CELL-CELL CONTACT; CELLULAR PRION PROTEINS; CONFORMATIONAL STABILITIES; INTERCELLULAR COMMUNICATIONS; NUCLEIC ACID CONTENTS; PRION INFECTIVITY; SPHINGOMYELINASE;

NEURODEGENERATIVE DISEASES;

3,3' (1,4 PHENYLENE)BIS[N [4 (4,5 DIHYDRO 1H IMIDAZOL 2 YL)PHENYL]ACRYLAMIDE]; IONOPHORE; MONENSIN; PRION PROTEIN; PROTEINASE K; SPHINGOMYELIN PHOSPHODIESTERASE; ANILINE DERIVATIVE; BENZYLIDENE DERIVATIVE; PRION;

ANIMAL CELL; ARTICLE; CELL ASSAY; CELL CONTACT; CELLULAR DISTRIBUTION; CELLULAR PARAMETERS; CONTROLLED STUDY; EXOSOME RELEASE; FILTERS AND MEMBRANES; IN VITRO STUDY; INTERCELLULAR SPACE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DETERMINATION; PROTEIN LOCALIZATION; PROTEIN SECRETION; PROTEIN STABILITY; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; ANIMAL; CELL LINE; CELL MEMBRANE; CHEMISTRY; DRUG EFFECTS; EXOSOME; METABOLISM; PRION; RABBIT;

ANILINE COMPOUNDS; ANIMALS; BENZYLIDENE COMPOUNDS; CELL LINE; CELL MEMBRANE; EXOSOMES; MICE; MONENSIN; PRIONS; PROTEIN STABILITY; PROTEIN TRANSPORT; RABBITS;

EID: 84964665924     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.684258     Document Type: Article

References (52)

1. Zitvogel, L., Regnault, A., Lozier, A., Wolfers, J., Flament, C., Tenza, D., Ricciardi-Castagnoli, P., Raposo, G., and Amigorena, S. (1998) Eradication of established murine tumors using a novel cell-free vaccine: dendritic cell-derived exosomes. Nat. Med. 4, 594-600
2. Izquierdo-Useros, N., Naranjo-Gómez, M., Archer, J., Hatch, S. C., Erkizia, I., Blanco, J., Borràs, F. E., Puertas, M. C., Connor, J. H., Fernández-Figueras, M. T., Moore, L., Clotet, B., Gummuluru, S., and Martinez-Picado, J. (2009) Capture and transfer of HIV-1 particles by mature dendritic cells converges with the exosome-dissemination pathway. Blood 113, 2732-2741
3. Bellingham, S. A., and Guo., B. B., Coleman, B. M., and Hill, A. F. (2012) Exosomes: vehicles for the transfer of toxic proteins associated with neurode-generative diseases? Front. Physiol. 3, 124
4. Caby, M. P., Lankar, D., Vincendeau-Scherrer, C., Raposo, G., and Bonnerot, C. (2005) Exosomal-like vesicles are present in human blood plasma. Int. Immunol. 17, 879-887
5. Pisitkun, T., and Shen., R. F., and Knepper, M. A. (2004) Identification and proteomic profiling of exosomes in human urine. Proc. Natl. Acad. Sci. U.S.A. 101, 13368-13373
6. Raposo, G., and Nijman., H. W., Stoorvogel, W., Liejendekker, R., Harding, C. V., and Melief., C. J., and Geuze, H. J. (1996) B lymphocytes secrete antigen-presenting vesicles. J. Exp. Med. 183, 1161-1172
7. O'Neill, H. C., and Quah, B. J. (2008) Exosomes secreted by bacterially infected macrophages are proinflammatory. Sci. Signal. 1, e8
8. Valadi, H., Ekström, K., Bossios, A., Sjöstrand, M., Lee, J. J., and Lötvall, J. O. (2007) Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol. 9, 654-659
9. Bellingham, S. A., and Coleman., B. M., and Hill, A. F. (2012) Small RNA deep sequencing reveals a distinct miRNA signature released in exosomes from prion-infected neuronal cells. Nucleic Acids Res. 40, 10937-10949
10. Fevrier, B., Vilette, D., Archer, F., Loew, D., Faigle, W., Vidal, M., Laude, H., and Raposo, G. (2004) Cells release prions in association with exosomes. Proc. Natl. Acad. Sci. U.S.A. 101, 9683-9688
11. Vella, L.J., Sharples, R. A., and Lawson., V. A., Masters, C. L., Cappai, R., and Hill, A. F. (2007) Packaging of prions into exosomes is associated with a novel pathway of PrP processing. J. Pathol. 211, 582-590
12. Rajendran, L., Honsho, M., Zahn, T. R., Keller, P., and Geiger., K. D., Verkade, P., and Simons, K. (2006) Alzheimer's disease β-amyloid peptides are released in association with exosomes. Proc. Natl. Acad. Sci. U.S.A. 103, 11172-11177
13. Sharples, R. A., and Vella., L. J., Nisbet, R. M., Naylor, R., Perez, K., and Barnham., K. J., Masters, C. L., and Hill, A. F. (2008) Inhibition of γ-secretase causes increased secretion of amyloid precursor protein C-terminal fragments in association with exosomes. FASEB J. 22, 1469-1478
14. Alvarez-Erviti, L., Seow, Y., and Schapira., A. H., Gardiner, C., Sargent, I. L., and Wood., M. J., and Cooper, J. M. (2011) Lysosomal dysfunction increases exosome-mediated α-synuclein release and transmission. Neurobiol. Dis. 42, 360-367
15. Gomes, C, Keller, S., Altevogt, P., and Costa, J. (2007) Evidence for secretion of Cu, Zn superoxide dismutase via exosomes from a cell model of amyotrophic lateral sclerosis. Neurosci. Lett. 428, 43-46
16. Vilette, D., Laulagnier, K., Huor, A., Alais, S., Simoes, S., Maryse, R., Provansal, M., Lehmann, S., Andreoletti, O., Schaeffer, L., Raposo, G., and Leblanc, P. (2015) Efficient inhibition of infectious prions multiplication and release by targeting the exosomal pathway. Cell. Mol. Life Sci. 72, 4409-4427
17. Prusiner, S.B. (1998) Prions. Proc. Natl. Acad. Sci. U.S.A. 95, 13363-13383
18. Kanu, N, Imokawa, Y., Drechsel, D. N, Williamson, R. A., and Birkett., C. R., Bostock, C. J., and Brockes, J. P. (2002) Transfer of scrapie prion infectivity by cell contact in culture. Curr. Biol. 12, 523-530
19. Gousset, K., Schiff, E., Langevin, C, Marijanovic, Z., Caputo, A., Browman, D. T., Chenouard, N., de Chaumont, F., Martino, A., Enninga, J., Olivo-Marin, J. C, Männel, D., and Zurzolo, C. (2009) Prions hijack tunnelling nanotubes for intercellular spread. Nat. Cell Biol. 11, 328-336
20. Deleault, N. R., and Lucassen., R. W., and Supattapone, S. (2003) RNA molecules stimulate prion protein conversion. Nature 425, 717-720
21. Deleault, N. R., and Piro., J. R., Walsh, D. J., Wang, F., Ma, J., Geoghegan, J. C, and Supattapone, S. (2012) Isolation of phosphatidylethanolamine as a solitary cofactor for prion formation in the absence of nucleic acids. Proc. Natl. Acad. Sci. U.S.A. 109, 8546-8551
22. Deleault, N. R., and Walsh., D. J., Piro, J. R., Wang, F., Wang, X., Ma, J., Rees, J. R., and Supattapone, S. (2012) Cofactor molecules maintain infectious conformation and restrict strain properties in purified prions. Proc. Natl. Acad. Sci. U.S.A. 109, E1938-1946
23. Wang, F., Wang, X., Yuan, C. G., and Ma, J. (2010) Generating a prion with bacterially expressed recombinant prion protein. Science 327, 1132-1135
24. Lawson, V. A., and Vella., L. J., Stewart, J. D., Sharples, R. A., Klemm, H., and Machalek., D. M., Masters, C. L., Cappai, R., Collins, S. J., and Hill, A. F. (2008) Mouse-adapted sporadic human Creutzfeldt-Jakob disease prions propagate in cell culture. Int. J. Biochem. Cell Biol. 40, 2793-2801
25. Guo, B. B., and Bellingham., S. A., and Hill, A. F. (2015) The neutral sphingomyelinase pathway regulates packaging of the prion protein into exosomes. J. Biol. Chem. 290, 3455-3467
26. Coleman, B. M., Hanssen, E., Lawson, V. A., and Hill, A. F. (2012) Prion-infected cells regulate the release of exosomes with distinct ultrastructural features. FASEB J. 26, 4160-4173
27. Ellman, G. L., and Courtney., K. D., Andres, V., Jr., and Feather-Stone, R. M. (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem. Pharmacol. 7, 88-95
28. Cantin, R., Diou, J., Bélanger, D., Tremblay, A. M., and Gilbert, C. (2008) Discrimination between exosomes and HIV-1: purification of both vesicles from cell-free supernatants. J. Immunol. Methods 338, 21-30
29. Rabesandratana, H., and Toutant., J. P., Reggio, H., and Vidal, M. (1998) Decay-accelerating factor (CD55) and membrane inhibitor of reactive lysis (CD59) are released within exosomes during in vitro maturation of reticulocytes. Blood 91, 2573-2580
30. Harrison, C F., Lawson, V. A., Coleman, B. M., Kim, Y.-S., Masters, C. L., Cappai, R., Barnham, K.J., and Hill, A. F. (2010) Conservation of aglycinerich region in the prion protein is required for uptake of prion infectivity. J. Biol. Chem. 285, 20213-20223
31. Rasband, W.S. (1997) ImageJ, National Institutes of Health, Bethesda, MD
32. Schätzl, H. M., Laszlo, L., Holtzman, D. M., Tatzelt, J., and DeArmond., S. J., Weiner, R. I., Mobley, W. C, and Prusiner, S. B. (1997) A hypothalamic neuronal cell line persistently infected with scrapie prions exhibits apoptosis. J. Virol. 71, 8821-8831
33. Mellon, P. L., and Windle., J. J., Goldsmith, P. C, Padula, C A., Roberts, J. L., and Weiner, R. I. (1990) Immortalization of hypothalamic GnRH neurons by genetically targeted tumorigenesis. Neuron 5, 1-10
34. Savina, A., Furlán, M., Vidal, M., and Colombo, M. I. (2003) Exosome release is regulated by a calcium-dependent mechanism in K562 cells. J. Biol. Chem. 278, 20083-20090
35. Trajkovic, K., Hsu, C, Chiantia, S., Rajendran, L., Wenzel, D., Wieland, F., Schwille, P., Brügger, B., and Simons, M. (2008) Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 319, 1244-1247
36. Saborio, G. P., Permanne, B., and Soto, C. (2001) Sensitive detection of pathological prion protein by cyclic amplification of protein misfolding. Nature 411, 810-813
37. Mollenhauer, H. H., and Morre., D. J., and Rowe, L. D. (1990) Alteration of intracellular traffic by monensin; mechanism, specificity and relationship to toxicity. Biochim. Biophys. Acta 7, 225-246
38. LeBlanc, A. C, and Goodyer, C. G. (1999) Role of endoplasmic reticulum, endosomal-lysosomal compartments, and microtubules in amyloid precursor protein metabolism of human neurons. J. Neurochem. 72, 1832-1842
39. Bäck, N, and Soinila, S. (1996) Effect of monensin on secretory granules and basal β-endorphin secretion in the melanotroph of the rat pituitary. Histochem. J. 28, 591-597
40. Kuismanen, E., Saraste, J., and Pettersson, R. F. (1985) Effect of monensin on the assembly of Uukuniemi virus in the Golgi complex. J. Virol. 55, 813-822
41. Cancellotti, E., and Mahal., S. P., Somerville, R., Diack, A., Brown, D., Piccardo, P., Weissmann, C, and Manson, J. C. (2013) Post-translational changes to PrP alter transmissible spongiform encephalopathy strain properties. EMBO J. 32, 756-769
42. Collinge, J., Sidle, K. C, Meads, J., Ironside, J., and Hill, A. F. (1996) Molecular analysis of prion strain variation and the aetiology of "new variant" CJD. Nature 383, 685-690
43. DeArmond, S. J., Sánchez, H., Yehiely, F., Qiu, Y., Ninchak-Casey, A., Daggett, V., and Camerino., A. P., Cayetano, J., Rogers, M., Groth, D., Torchia, M., Tremblay, P., Scott, M. R., and Cohen., F. E., and Prusiner, S. B. (1997) Selective neuronal targeting in prion disease. Neuron 19, 1337-1348
44. Cancellotti, E., and Bradford., B. M., Tuzi, N. L., Hickey, R. D., Brown, D., and Brown., K. L., Barron, R. M., Kisielewski, D., Piccardo, P., and Manson, J. C. (2010) Glycosylation of PrPC determines timing of neuroinvasion and targeting in the brain following transmissible spongiform encephalopathy infection by a peripheral route. J. Virol. 84, 3464-3475
45. Taraboulos, A., and Raeber., A. J., Borchelt, D. R., Serban, D., and Prusiner, S. B. (1992) Synthesis and trafficking of prion proteins in cultured cells. Mol. Biol. Cell 3, 851-863
46. Yuyama, K., Sun, H., Mitsutake, S., and Igarashi, Y. (2012) Sphingolipid-modulated exosome secretion promotes clearance of amyloid-β by microglia. J. Biol. Chem. 287, 10977-10989
47. Lehmann, S., and Harris, D. A. (1997) Blockade of glycosylation promotes acquisition of scrapie-like properties by the prion protein in cultured cells. J. Biol. Chem. 272, 21479-21487
48. Nitrini, R., Rosemberg, S., Passos-Bueno, M. R., da Silva, L. S., Iughetti, P., Papadopoulos, M., Carrilho, P. M., Caramelli, P., Albrecht, S., Zatz, M., and LeBlanc, A. (1997) Familial spongiform encephalopathy associated with a novel prion protein gene mutation. Ann. Neurol. 42, 138-146
49. Barron, R. M., and Campbell., S. L., King, D., Bellon, A., Chapman, K. E., and Williamson., R. A., and Manson, J. C. (2007) High titers of transmissible spongiform encephalopathy infectivity associated with extremely low levels of PrPSc in vivo. J. Biol. Chem. 282, 35878-35886
50. Lasmézas, C. I., Deslys, J. P., Robain, O., Jaegly, A., Beringue, V., Peyrin, J. M., and Fournier., J. G., Hauw, J. J., Rossier, J., and Dormont, D. (1997) Transmission of the BSE agent to mice in the absence of detectable abnormal prion protein. Science 275, 402-405
51. Manson, J. C., Jamieson, E., Baybutt, H., Tuzi, N. L., Barron, R., McConnell, I., Somerville, R., Ironside, J., Will, R., Sy, M. S., and Melton., D. W., Hope, J., and Bostock, C. (1999) A single amino acid alteration (101L) introduced into murine PrP dramatically alters incubation time of transmissible spongiform encephalopathy. EMBO J. 18, 6855-6864
52. Bessen, R. A., and Marsh, R. F. (1992) Biochemical and physical properties of the prion protein from two strains of the transmissible mink encephalopathy agent. J. Virol. 66, 2096-2101