Impact of lysosome status on extracellular vesicle content and release

Ageing Research Reviews

Volumn 32, Issue , 2016, Pages 65-74

  Eitan, Erez ^a   Suire, Caitlin ^a   Zhang, Shi ^a   Mattson, Mark P ^a  

^a NATIONAL INSTITUTE ON AGING   (United States)

Author keywords

Alzheimer's disease; HIV AIDS; Niemann pick disease; Parkinson's disease

Indexed keywords

DRUG;

ANALYTICAL PARAMETERS; CELL FUNCTION; CELL MIGRATION; CELLULAR SECRETION; DEGENERATIVE DISEASE; EXOSOME; EXTRACELLULAR VESICLE CONTENT; EXTRACELLULAR VESICLE RELEASE; HUMAN; LYSOSOME; LYSOSOME STORAGE DISEASE; ORGANELLE BIOGENESIS; PATHOGENESIS; RECIPIENT; REGULATORY MECHANISM; REVIEW; VIRUS; AGING; AUTOPHAGY; CELL MEMBRANE; METABOLISM; MULTIVESICULAR BODY; PHYSIOLOGY; PROTEIN TRANSPORT;

AGING; AUTOPHAGY; CELL MEMBRANE; EXOSOMES; HUMANS; LYSOSOMES; MULTIVESICULAR BODIES; NEURODEGENERATIVE DISEASES; PROTEIN TRANSPORT;

EID: 84973570803     PISSN: 15681637     EISSN: 18729649     Source Type: Journal    
DOI: 10.1016/j.arr.2016.05.001     Document Type: Review

References (122)

1. Abrami, L., Brandi, L., Moayeri, M., Brown, M.J., Krantz, B.A., Leppla, S.H., van der Goot, F.G., Hijacking multivesicular bodies enables long-term and exosome-mediated long-distance action of anthrax toxin. Cell Rep. 5:4 (2013), 986–996.
2. Alvarez-Erviti, L., Seow, Y., Schapira, A.H., Gardiner, C., Sargent, I.L., Wood, M.J., Cooper, J.M., Lysosomal dysfunction increases exosome-mediated alpha-synuclein release and transmission. Neurobiol. Dis. 42:3 (2011), 360–367.
3. An, Q., van Bel, A.J., Huckelhoven, R., Do plant cells secrete exosomes derived from multivesicular bodies?. Plant Signal. Behav. 2:1 (2007), 4–7.
4. Andreu, Z., Yanez-Mo, M., Tetraspanins in extracellular vesicle formation and function. Front. Immunol., 5, 2014, 442.
5. Azmi, A.S., Bao, B., Sarkar, F.H., Exosomes in cancer development, metastasis, and drug resistance: a comprehensive review. Cancer Metastasis Rev. 32:3–4 (2013), 623–642.
6. Baietti, M.F., Zhang, Z., Mortier, E., Melchior, A., Degeest, G., Geeraerts, A., Ivarsson, Y., Depoortere, F., Coomans, C., Vermeiren, E., Zimmermann, P., David, G., Syndecan-syntenin-ALIX regulates the biogenesis of exosomes. Nat. Cell Biol. 14:7 (2012), 677–685.
7. Baixauli, F., Lopez-Otin, C., Mittelbrunn, M., Exosomes and autophagy: coordinated mechanisms for the maintenance of cellular fitness. Front. Immunol., 5, 2014, 403.
8. Bari, R., Guo, Q., Xia, B., Zhang, Y.H., Giesert, E.E., Levy, S., Zheng, J.J., Zhang, X.A., Tetraspanins regulate the protrusive activities of cell membrane. Biochem. Biophys. Res. Commun. 415:4 (2011), 619–626.
9. Beckett, K., Monier, S., Palmer, L., Alexandre, C., Green, H., Bonneil, E., Raposo, G., Thibault, P., Le Borgne, R., Vincent, J.P., Drosophila S2 cells secrete wingless on exosome-like vesicles but the wingless gradient forms independently of exosomes. Traffic 14:1 (2013), 82–96.
10. Bellingham, S.A., Guo, B., Hill, A.F., The secret life of extracellular vesicles in metal homeostasis and neurodegeneration. Biol. Cell. 107:11 (2015), 389–418.
11. Bhattacharya, S., Pal, K., Sharma, A.K., Dutta, S.K., Lau, J.S., Yan, I.K., Wang, E., Elkhanany, A., Alkharfy, K.M., Sanyal, A., Patel, T.C., Chari, S.T., Spaller, M.R., Mukhopadhyay, D., GAIP interacting protein C-terminus regulates autophagy and exosome biogenesis of pancreatic cancer through metabolic pathways. PLoS One, 9(12), 2014, e114409.
12. Bianchi, E., Doe, B., Goulding, D., Wright, G.J., Juno is the egg Izumo receptor and is essential for mammalian fertilization. Nature 508:7497 (2014), 483–487.
13. Biffi, A., Gene therapy for lysosomal storage disorders: a good start. Hum. Mol. Genet. 25:R1 (2015), R65–R75.
14. Brinton, L.T., Sloane, H.S., Kester, M., Kelly, K.A., Formation and role of exosomes in cancer. Cell. Mol. Life Sci. 72:4 (2015), 659–671.
15. Challagundla, K.B., Wise, P.M., Neviani, P., Chava, H., Murtadha, M., Xu, T., Kennedy, R., Ivan, C., Zhang, X., Vannini, I., Fanini, F., Amadori, D., Calin, G.A., Hadjidaniel, M., Shimada, H., Jong, A., Seeger, R.C., Asgharzadeh, S., Goldkorn, A., Fabbri, M., Exosome-mediated transfer of microRNAs within the tumor microenvironment and neuroblastoma resistance to chemotherapy. J. Natl. Cancer Inst., 107(7), 2015.
16. Chen, F.W., Li, C., Ioannou, Y.A., Cyclodextrin induces calcium-dependent lysosomal exocytosis. PLoS One, 5(11), 2010, e15054.
17. Chen, X., Qiu, W., Ye, J., Han, L., Gu, X., Zhang, H., Demographic characteristics and distribution of lysosomal storage disorder subtypes in Eastern China. J. Hum. Genet., 2016.
18. Chiba, M., Watanabe, N., Watanabe, M., Sakamoto, M., Sato, A., Fujisaki, M., Kubota, S., Monzen, S., Maruyama, A., Nanashima, N., Kashiwakura, I., Nakamura, T., Exosomes derived from SW480 colorectal cancer cells promote cell migration in HepG2 hepatocellular cancer cells via the mitogen-activated protein kinase pathway. Int. J. Oncol. 48:1 (2016), 305–312.
19. Colombo, M., Moita, C., van Niel, G., Kowal, J., Vigneron, J., Benaroch, P., Manel, N., Moita, L.F., Thery, C., Raposo, G., Analysis of ESCRT functions in exosome biogenesis, composition and secretion highlights the heterogeneity of extracellular vesicles. J. Cell Sci. 126:Pt. 24 (2013), 5553–5565.
20. Colombo, M., Raposo, G., Thery, C., Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu. Rev. Cell Dev. Biol. 30 (2014), 255–289.
21. Danzer, K.M., Kranich, L.R., Ruf, W.P., Cagsal-Getkin, O., Winslow, A.R., Zhu, L., Vanderburg, C.R., McLean, P.J., Exosomal cell-to-cell transmission of alpha synuclein oligomers. Mol. Neurodegener., 7, 2012, 42.
22. Davis, C.H., Kim, K.Y., Bushong, E.A., Mills, E.A., Boassa, D., Shih, T., Kinebuchi, M., Phan, S., Zhou, Y., Bihlmeyer, N.A., Nguyen, J.V., Jin, Y., Ellisman, M.H., Marsh-Armstrong, N., Transcellular degradation of axonal mitochondria. Proc. Natl. Acad. Sci. U. S. A. 111:26 (2014), 9633–9638.
23. Denzer, K., Kleijmeer, M.J., Heijnen, H.F., Stoorvogel, W., Geuze, H.J., Exosome: from internal vesicle of the multivesicular body to intercellular signaling device. J. Cell. Sci. 113:Pt. 19 (2000), 3365–3374.
24. Ditaranto, K., Tekirian, T.L., Yang, A.J., Lysosomal membrane damage in soluble Abeta-mediated cell death in Alzheimer's disease. Neurobiol. Dis. 8:1 (2001), 19–31.
25. Eitan, E., Zhang, S., Witwer, K.W., Mattson, M.P., Extracellular vesicle-depleted fetal bovine and human sera have reduced capacity to support cell growth. J. Extracell. Vesicles, 4, 2015, 26373.
26. Emmanouilidou, E., Melachroinou, K., Roumeliotis, T., Garbis, S.D., Ntzouni, M., Margaritis, L.H., Stefanis, L., Vekrellis, K., Cell-produced alpha-synuclein is secreted in a calcium-dependent manner by exosomes and impacts neuronal survival. J. Neurosci. 30:20 (2010), 6838–6851.
27. Escudero, C.A., Lazo, O.M., Galleguillos, C., Parraguez, J.I., Lopez-Verrilli, M.A., Cabeza, C., Leon, L., Saeed, U., Retamal, C., Gonzalez, A., Marzolo, M.P., Carter, B.D., Court, F.A., Bronfman, F.C., The p75 neurotrophin receptor evades the endolysosomal route in neuronal cells, favouring multivesicular bodies specialised for exosomal release. J. Cell Sci. 127:Pt. 9 (2014), 1966–1979.
28. Fabbri, M., Paone, A., Calore, F., Galli, R., Gaudio, E., Santhanam, R., Lovat, F., Fadda, P., Mao, C., Nuovo, G.J., Zanesi, N., Crawford, M., Ozer, G.H., Wernicke, D., Alder, H., Caligiuri, M.A., Nana-Sinkam, P., Perrotti, D., Croce, C.M., MicroRNAs bind to toll-like receptors to induce prometastatic inflammatory response. Proc. Natl. Acad. Sci. U. S. A. 109:31 (2012), E2110–E2116.
29. Fader, C.M., Sanchez, D.G., Mestre, M.B., Colombo, M.I., TI-VAMP/VAMP7 and VAMP3/cellubrevin: two v-SNARE proteins involved in specific steps of the autophagy/multivesicular body pathways. Biochim. Biophys. Acta 1793:12 (2009), 1901–1916.
30. Faigle, W., Raposo, G., Tenza, D., Pinet, V., Vogt, A.B., Kropshofer, H., Fischer, A., de Saint-Basile, G., Amigorena, S., Deficient peptide loading and MHC class II endosomal sorting in a human genetic immunodeficiency disease: the Chediak–Higashi syndrome. J. Cell. Biol. 141:5 (1998), 1121–1134.
31. Federici, C., Petrucci, F., Caimi, S., Cesolini, A., Logozzi, M., Borghi, M., D'Ilio, S., Lugini, L., Violante, N., Azzarito, T., Majorani, C., Brambilla, D., Fais, S., Exosome release and low pH belong to a framework of resistance of human melanoma cells to cisplatin. PLoS One, 9(2), 2014, e88193.
32. Fevrier, B., Raposo, G., Exosomes: endosomal-derived vesicles shipping extracellular messages. Curr. Opin. Cell Biol. 16:4 (2004), 415–421.
33. Fevrier, B., Vilette, D., Archer, F., Loew, D., Faigle, W., Vidal, M., Laude, H., Raposo, G., Cells release prions in association with exosomes. Proc. Natl. Acad. Sci. U. S. A. 101:26 (2004), 9683–9688.
34. Fiandaca, M.S., Kapogiannis, D., Mapstone, M., Boxer, A., Eitan, E., Schwartz, J.B., Abner, E.L., Petersen, R.C., Federoff, H.J., Miller, B.L., Goetzl, E.J., Identification of preclinical Alzheimer's disease by a profile of pathogenic proteins in neurally derived blood exosomes: a case-control study. Alzheimers Dement, 607, 2015, e601.
35. Fruhbeis, C., Frohlich, D., Kramer-Albers, E.M., Emerging roles of exosomes in neuron-glia communication. Front. Physiol., 3, 2012, 119.
36. Gould, S.J., Booth, A.M., Hildreth, J.E., The trojan exosome hypothesis. Proc. Natl. Acad. Sci. U. S. A. 100:19 (2003), 10592–10597.
37. Grad, L.I., Yerbury, J.J., Turner, B.J., Guest, W.C., Pokrishevsky, E., O'Neill, M.A., Yanai, A., Silverman, J.M., Zeineddine, R., Corcoran, L., Kumita, J.R., Luheshi, L.M., Yousefi, M., Coleman, B.M., Hill, A.F., Plotkin, S.S., Mackenzie, I.R., Cashman, N.R., Intercellular propagated misfolding of wild-type Cu/Zn superoxide dismutase occurs via exosome-dependent and -independent mechanisms. Proc. Natl. Acad. Sci. U. S. A. 111:9 (2014), 3620–3625.
38. Hanson, P.I., Cashikar, A., Multivesicular body morphogenesis. Annu. Rev. Cell Dev. Biol. 28 (2012), 337–362.
39. Hasegawa, T., Konno, M., Baba, T., Sugeno, N., Kikuchi, A., Kobayashi, M., Miura, E., Tanaka, N., Tamai, K., Furukawa, K., Arai, H., Mori, F., Wakabayashi, K., Aoki, M., Itoyama, Y., Takeda, A., The AAA-ATPase VPS4 regulates extracellular secretion and lysosomal targeting of alpha-synuclein. PLoS One, 6(12), 2011, e29460.
40. Ho, D.H., Yi, S., Seo, H., Son, I., Seol, W., Increased DJ-1 in urine exosome of Korean males with Parkinson's disease. Biomed. Res. Int., 2014, 2014, 704678.
41. Hoshino, A., Costa-Silva, B., Shen, T.L., Rodrigues, G., Hashimoto, A., Tesic Mark, M., Molina, H., Kohsaka, S., Di Giannatale, A., Ceder, S., Singh, S., Williams, C., Soplop, N., Uryu, K., Pharmer, L., King, T., Bojmar, L., Davies, A.E., Ararso, Y., Zhang, T., Zhang, H., Hernandez, J., Weiss, J.M., Dumont-Cole, V.D., Kramer, K., Wexler, L.H., Narendran, A., Schwartz, G.K., Healey, J.H., Sandstrom, P., Jorgen Labori, K., Kure, E.H., Grandgenett, P.M., Hollingsworth, M.A., de Sousa, M., Kaur, S., Jain, M., Mallya, K., Batra, S.K., Jarnagin, W.R., Brady, M.S., Fodstad, O., Muller, V., Pantel, K., Minn, A.J., Bissell, M.J., Garcia, B.A., Kang, Y., Rajasekhar, V.K., Ghajar, C.M., Matei, I., Peinado, H., Bromberg, J., Lyden, D., Tumour exosome integrins determine organotropic metastasis. Nature 527:7578 (2015), 329–335.
42. Hosseini, H.M., Fooladi, A.A., Nourani, M.R., Ghanezadeh, F., The role of exosomes in infectious diseases. Inflamm. Allergy Drug Targets 12:1 (2013), 29–37.
43. Hsu, C., Morohashi, Y., Yoshimura, S., Manrique-Hoyos, N., Jung, S., Lauterbach, M.A., Bakhti, M., Gronborg, M., Mobius, W., Rhee, J., Barr, F.A., Simons, M., Regulation of exosome secretion by Rab35 and its GTPase-activating proteins TBC1D10A-C. J. Cell Biol. 189:2 (2010), 223–232.
44. Huang, L.S., Berdyshev, E.V., Tran, J.T., Xie, L., Chen, J., Ebenezer, D.L., Mathew, B., Gorshkova, I., Zhang, W., Reddy, S.P., Harijith, A., Wang, G., Feghali-Bostwick, C., Noth, I., Ma, S.F., Zhou, T., Ma, W., Garcia, J.G., Natarajan, V., Sphingosine-1-phosphate lyase is an endogenous suppressor of pulmonary fibrosis: role of S1P signalling and autophagy. Thorax 70:12 (2015), 1138–1148.
45. Huizing, M., Gahl, W.A., Disorders of vesicles of lysosomal lineage: the Hermansky-Pudlak syndromes. Curr. Mol. Med. 2:5 (2002), 451–467.
46. Huizing, M., Anikster, Y., Gahl, W.A., Hermansky-Pudlak syndrome and Chediak-Higashi syndrome: disorders of vesicle formation and trafficking. Thromb. Haemost. 86:1 (2001), 233–245.
47. Huotari, J., Helenius, A., Endosome maturation. EMBO J. 30:17 (2011), 3481–3500.
48. Hurley, J.H., ESCRTs are everywhere. EMBO J. 34:19 (2015), 2398–2407.
49. Iglesias, D.M., El-Kares, R., Taranta, A., Bellomo, F., Emma, F., Besouw, M., Levtchenko, E., Toelen, J., van den Heuvel, L., Chu, L., Zhao, J., Young, Y.K., Eliopoulos, N., Goodyer, P., Stem cell microvesicles transfer cystinosin to human cystinotic cells and reduce cystine accumulation in vitro. PLoS One, 7(8), 2012, e42840.
50. Johnstone, R.M., Mathew, A., Mason, A.B., Teng, K., Exosome formation during maturation of mammalian and avian reticulocytes: evidence that exosome release is a major route for externalization of obsolete membrane proteins. J. Cell. Physiol. 147:1 (1991), 27–36.
51. Kajimoto, T., Okada, T., Miya, S., Zhang, L., Nakamura, S., Ongoing activation of sphingosine 1-phosphate receptors mediates maturation of exosomal multivesicular endosomes. Nat. Commun., 4, 2013, 2712.
52. Kaparakis-Liaskos, M., Ferrero, R.L., Immune modulation by bacterial outer membrane vesicles. Nat. Rev. Immunol. 15:6 (2015), 375–387.
53. Kapogiannis, D., Boxer, A., Schwartz, J.B., Abner, E.L., Biragyn, A., Masharani, U., Frassetto, L., Petersen, R.C., Miller, B.L., Goetzl, E.J., Dysfunctionally phosphorylated type 1 insulin receptor substrate in neural-derived blood exosomes of preclinical Alzheimer's disease. FASEB J. 29:2 (2015), 589–596.
54. Kaushik, S., Cuervo, A.M., Proteostasis and aging. Nat. Med. 21:12 (2015), 1406–1415.
55. Koch, R., Aung, T., Vogel, D., Chapuy, B., Wenzel, D., Becker, S., Sinzig, U., Venkataramani, V., von Mach, T., Jacob, R., Truemper, L., Wulf, G.G., Nuclear trapping through inhibition of exosomal export by indomethacin increases cytostatic efficacy of doxorubicin and pixantrone. Clin. Cancer Res., 2015.
56. Kong, S.M., Chan, B.K., Park, J.S., Hill, K.J., Aitken, J.B., Cottle, L., Farghaian, H., Cole, A.R., Lay, P.A., Sue, C.M., Cooper, A.A., Parkinson's disease-linked human PARK9/ATP13A2 maintains zinc homeostasis and promotes alpha-Synuclein externalization via exosomes. Hum. Mol. Genet. 23:11 (2014), 2816–2833.
57. Kulkarni, H.M., Jagannadham, M.V., Biogenesis and multifaceted roles of outer membrane vesicles from gram-negative bacteria. Microbiology 160:Pt. 10 (2014), 2109–2121.
58. Lai, R.C., Yeo, R.W., Lim, S.K., Mesenchymal stem cell exosomes. Semin. Cell Dev. Biol. 40 (2015), 82–88.
59. Lee, H.D., Kim, Y.H., Kim, D.S., Exosomes derived from human macrophages suppress endothelial cell migration by controlling integrin trafficking. Eur. J. Immunol. 44:4 (2014), 1156–1169.
60. Liegeois, S., Benedetto, A., Garnier, J.M., Schwab, Y., Labouesse, M., The V0-ATPase mediates apical secretion of exosomes containing hedgehog-related proteins in Caenorhabditis elegans. J. Cell Biol. 173:6 (2006), 949–961.
61. Liscum, L., A role for NPC1 and NPC2 in intestinal cholesterol absorption–the hypothesis gutted. Biochem. J. 408:1 (2007), e1–3.
62. Lotvall, J., Hill, A.F., Hochberg, F., Buzas, E.I., Di Vizio, D., Gardiner, C., Gho, Y.S., Kurochkin, I.V., Mathivanan, S., Quesenberry, P., Sahoo, S., Tahara, H., Wauben, M.H., Witwer, K.W., Thery, C., Minimal experimental requirements for definition of extracellular vesicles and their functions: a position statement from the International Society for Extracellular Vesicles. J. Extracell. Vesicles, 3, 2014, 26913.
63. Luzio, J.P., Hackmann, Y., Dieckmann, N.M., Griffiths, G.M., The biogenesis of lysosomes and lysosome-related organelles. Cold Spring Harbour Perspect. Biol., 6(9), 2014, a016840.
64. Maguire, C.A., Balaj, L., Sivaraman, S., Crommentuijn, M.H., Ericsson, M., Mincheva-Nilsson, L., Baranov, V., Gianni, D., Tannous, B.A., Sena-Esteves, M., Breakefield, X.O., Skog, J., Microvesicle-associated AAV vector as a novel gene delivery system. Mol. Ther. 20:5 (2012), 960–971.
65. Mantel, P.Y., Marti, M., The role of extracellular vesicles in Plasmodium and other protozoan parasites. Cell. Microbiol. 16:3 (2014), 344–354.
66. Marchesano, V., Hernandez, Y., Salvenmoser, W., Ambrosone, A., Tino, A., Hobmayer, B., de la Fuente, J.M., Tortiglione, C., Imaging inward and outward trafficking of gold nanoparticles in whole animals. ACS Nano 7:3 (2013), 2431–2442.
67. Mattson, M.P., Degenerative and protective signaling mechanisms in the neurofibrillary pathology of AD. Neurobiol. Aging 16:3 (1995), 447–457 Discussion 458–463.
68. Mazzulli, J.R., Xu, Y.H., Sun, Y., Knight, A.L., McLean, P.J., Caldwell, G.A., Sidransky, E., Grabowski, G.A., Krainc, D., Gaucher disease glucocerebrosidase and alpha-synuclein form a bidirectional pathogenic loop in synucleinopathies. Cell 146:1 (2011), 37–52.
69. Miao, Y., Li, G., Zhang, X., Xu, H., Abraham, S.N., A TRP channel senses lysosome neutralization by pathogens to trigger their expulsion. Cell 161:6 (2015), 1306–1319.
70. Milane, L., Singh, A., Mattheolabakis, G., Suresh, M., Amiji, M.M., Exosome mediated communication within the tumor microenvironment. J. Control. Release 219 (2015), 278–294.
71. Milbank, E., Martinez, M.C., Andriantsitohaina, R., Extracellular vesicles: pharmacological modulators of the peripheral and central signals governing obesity. Pharmacol. Ther. 157 (2016), 65–83.
72. Mu, J., Zhuang, X., Wang, Q., Jiang, H., Deng, Z.B., Wang, B., Zhang, L., Kakar, S., Jun, Y., Miller, D., Zhang, H.G., Interspecies communication between plant and mouse gut host cells through edible plant derived exosome-like nanoparticles. Mol. Nutr. Food Res. 58:7 (2014), 1561–1573.
73. Mulcahy, L.A., Pink, R.C., Carter, D.R., Routes and mechanisms of extracellular vesicle uptake. J. Extracell. Vesicles, 2014, 3.
74. Murrow, L., Malhotra, R., Debnath, J., ATG12-ATG3 interacts with Alix to promote basal autophagic flux and late endosome function. Nat. Cell Biol. 17:3 (2015), 300–310.
75. Nixon, R.A., The role of autophagy in neurodegenerative disease. Nat. Med. 19:8 (2013), 983–997.
76. Nour, A.M., Modis, Y., Endosomal vesicles as vehicles for viral genomes. Trends Cell Biol. 24:8 (2014), 449–454.
77. Ochieng, J., Pratap, S., Khatua, A.K., Sakwe, A.M., Anchorage-independent growth of breast carcinoma cells is mediated by serum exosomes. Exp. Cell Res. 315:11 (2009), 1875–1888.
78. Ostrowski, M., Carmo, N.B., Krumeich, S., Fanget, I., Raposo, G., Savina, A., Moita, C.F., Schauer, K., Hume, A.N., Freitas, R.P., Goud, B., Benaroch, P., Hacohen, N., Fukuda, M., Desnos, C., Seabra, M.C., Darchen, F., Amigorena, S., Moita, L.F., Thery, C., Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat. Cell Biol. 12:1 (2010), 11–13 19–30, sup.
79. Perez-Gonzalez, R., Gauthier, S.A., Kumar, A., Levy, E., The exosome secretory pathway transports amyloid precursor protein carboxyl-terminal fragments from the cell into the brain extracellular space. J. Biol. Chem. 287:51 (2012), 43108–43115.
80. Piccin, A., Murphy, W.G., Smith, O.P., Circulating microparticles: pathophysiology and clinical implications. Blood Rev. 21:3 (2007), 157–171.
81. Poehler, A.M., Xiang, W., Spitzer, P., May, V.E., Meixner, H., Rockenstein, E., Chutna, O., Outeiro, T.F., Winkler, J., Masliah, E., Klucken, J., Autophagy modulates SNCA/alpha-synuclein release, thereby generating a hostile microenvironment. Autophagy 10:12 (2014), 2171–2192.
82. Rajendran, L., Honsho, M., Zahn, T.R., Keller, P., Geiger, K.D., Verkade, P., Simons, K., Alzheimer's disease beta-amyloid peptides are released in association with exosomes. Proc. Natl. Acad. Sci. U. S. A. 103:30 (2006), 11172–11177.
83. Ramakrishnaiah, V., Thumann, C., Fofana, I., Habersetzer, F., Pan, Q., de Ruiter, P.E., Willemsen, R., Demmers, J.A., Stalin Raj, V., Jenster, G., Kwekkeboom, J., Tilanus, H.W., Haagmans, B.L., Baumert, T.F., van der Laan, L.J., Exosome-mediated transmission of hepatitis C virus between human hepatoma Huh7.5 cells. Proc. Natl. Acad. Sci. U. S. A. 110:32 (2013), 13109–13113.
84. Robbins, P.D., Morelli, A.E., Regulation of immune responses by extracellular vesicles. Nat. Rev. Immunol. 14:3 (2014), 195–208.
85. Robertson, C., Booth, S.A., Beniac, D.R., Coulthart, M.B., Booth, T.F., McNicol, A., Cellular prion protein is released on exosomes from activated platelets. Blood 107:10 (2006), 3907–3911.
86. Rusten, T.E., Simonsen, A., ESCRT functions in autophagy and associated disease. Cell Cycle 7:9 (2008), 1166–1172.
87. Safaei, R., Larson, B.J., Cheng, T.C., Gibson, M.A., Otani, S., Naerdemann, W., Howell, S.B., Abnormal lysosomal trafficking and enhanced exosomal export of cisplatin in drug-resistant human ovarian carcinoma cells. Mol. Cancer Ther. 4:10 (2005), 1595–1604.
88. Saman, S., Kim, W., Raya, M., Visnick, Y., Miro, S., Saman, S., Jackson, B., McKee, A.C., Alvarez, V.E., Lee, N.C., Hall, G.F., Exosome-associated tau is secreted in tauopathy models and is selectively phosphorylated in cerebrospinal fluid in early Alzheimer disease. J. Biol. Chem. 287:6 (2012), 3842–3849.
89. Sampey, G.C., Saifuddin, M., Schwab, A., Barclay, R., Punya, S., Chung, M.C., Hakami, R.M., Asad Zadeh, M., Lepene, B., Klase, Z.A., El-Hage, N., Young, M., Iordanskiy, S., Kashanchi, F., Exosomes from HIV-1 infected cells stimulate production of pro-inflammatory cytokines through TAR RNA. J. Biol. Chem., 2015.
90. Samuel, M., Bleackley, M., Anderson, M., Mathivanan, S., Extracellular vesicles including exosomes in cross kingdom regulation: a viewpoint from plant-fungal interactions. Front. Plant Sci., 6, 2015, 766.
91. Savina, A., Vidal, M., Colombo, M.I., The exosome pathway in K562 cells is regulated by Rab11. J. Cell Sci. 115:Pt. 12 (2002), 2505–2515.
92. Savina, A., Furlan, M., Vidal, M., Colombo, M.I., Exosome release is regulated by a calcium-dependent mechanism in K562 cells. J. Biol. Chem. 278:22 (2003), 20083–20090.
93. Schwab, A., Meyering, S.S., Lepene, B., Iordanskiy, S., van Hoek, M.L., Hakami, R.M., Kashanchi, F., Extracellular vesicles from infected cells: potential for direct pathogenesis. Front. Microbiol., 6, 2015, 1132.
94. Shelke, G.V., Lasser, C., Gho, Y.S., Lotvall, J., Importance of exosome depletion protocols to eliminate functional and RNA-containing extracellular vesicles from fetal bovine serum. J. Extracell. Vesicles, 2014, 3.
95. Shen, B., Wu, N., Yang, J.M., Gould, S.J., Protein targeting to exosomes/microvesicles by plasma membrane anchors. J. Biol. Chem. 286:16 (2011), 14383–14395.
96. Shi, M., Liu, C., Cook, T.J., Bullock, K.M., Zhao, Y., Ginghina, C., Li, Y., Aro, P., Dator, R., He, C., Hipp, M.J., Zabetian, C.P., Peskind, E.R., Hu, S.C., Quinn, J.F., Galasko, D.R., Banks, W.A., Zhang, J., Plasma exosomal alpha-synuclein is likely CNS-derived and increased in Parkinson's disease. Acta Neuropathol. 128:5 (2014), 639–650.
97. Shin, H.Y., Oh, J.M., Kim, Y.S., The functional role of prion protein (PrPC) on autophagy. Pathogens 2:3 (2013), 436–445.
98. Shrivastava, S., Devhare, P., Sujijantarat, N., Steele, R., Kwon, Y.C., Ray, R., Ray, R.B., Knockdown of autophagy inhibits infectious hepatitis C virus release by exosomal pathway. J. Virol., 2015.
99. Simon, D., Garcia-Garcia, E., Royo, F., Falcon-Perez, J.M., Avila, J., Proteostasis of tau. Tau overexpression results in its secretion via membrane vesicles. FEBS Lett. 586:1 (2012), 47–54.
100. Squadrito, M.L., Baer, C., Burdet, F., Maderna, C., Gilfillan, G.D., Lyle, R., Ibberson, M., De Palma, M., Endogenous RNAs modulate microRNA sorting to exosomes and transfer to acceptor cells. Cell Rep. 8:5 (2014), 1432–1446.
101. Steele, S., Brunton, J., Kawula, T., The role of autophagy in intracellular pathogen nutrient acquisition. Front. Cell. Infect. Microbiol., 5, 2015, 51.
102. Strauss, J.F. 3rd, Liu, P., Christenson, L.K., Watari, H., Sterols and intracellular vesicular trafficking: lessons from the study of NPC1. Steroids 67:12 (2002), 947–951.
103. Strauss, K., Goebel, C., Runz, H., Mobius, W., Weiss, S., Feussner, I., Simons, M., Schneider, A., Exosome secretion ameliorates lysosomal storage of cholesterol in Niemann-Pick type C disease. J. Biol. Chem. 285:34 (2010), 26279–26288.
104. Sullivan, R., Saez, F., Girouard, J., Frenette, G., Role of exosomes in sperm maturation during the transit along the male reproductive tract. Blood Cells Mol. Dis. 35:1 (2005), 1–10.
105. Szatmari, Z., Sass, M., The autophagic roles of Rab small GTPases and their upstream regulators: a review. Autophagy 10:7 (2014), 1154–1166.
106. Szatmari, Z., Kis, V., Lippai, M., Hegedus, K., Farago, T., Lorincz, P., Tanaka, T., Juhasz, G., Sass, M., Rab11 facilitates cross-talk between autophagy and endosomal pathway through regulation of Hook localization. Mol. Biol. Cell 25:4 (2014), 522–531.
107. Tamai, K., Shiina, M., Tanaka, N., Nakano, T., Yamamoto, A., Kondo, Y., Kakazu, E., Inoue, J., Fukushima, K., Sano, K., Ueno, Y., Shimosegawa, T., Sugamura, K., Regulation of hepatitis C virus secretion by the Hrs-dependent exosomal pathway. Virology 422:2 (2012), 377–385.
108. Tian, T., Wang, Y., Wang, H., Zhu, Z., Xiao, Z., Visualizing of the cellular uptake and intracellular trafficking of exosomes by live-cell microscopy. J. Cell. Biochem. 111:2 (2010), 488–496.
109. Tian, T., Zhu, Y.L., Hu, F.H., Wang, Y.Y., Huang, N.P., Xiao, Z.D., Dynamics of exosome internalization and trafficking. J. Cell. Physiol. 228:7 (2013), 1487–1495.
110. Tomlinson, P.R., Zheng, Y., Fischer, R., Heidasch, R., Gardiner, C., Evetts, S., Hu, M., Wade-Martins, R., Turner, M.R., Morris, J., Talbot, K., Kessler, B.M., Tofaris, G.K., Identification of distinct circulating exosomes in Parkinson's disease. Ann. Clin. Transl. Neurol. 2:4 (2015), 353–361.
111. Trajkovic, K., Hsu, C., Chiantia, S., Rajendran, L., Wenzel, D., Wieland, F., Schwille, P., Brugger, B., Simons, M., Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 319:5867 (2008), 1244–1247.
112. Tsunemi, T., Hamada, K., Krainc, D., ATP13A2/PARK9 regulates secretion of exosomes and alpha-synuclein. J. Neurosci. 34:46 (2014), 15281–15287.
113. Van Giau, V., An, S.S., Emergence of exosomal miRNAs as a diagnostic biomarker for Alzheimer's disease. J. Neurol. Sci. 360 (2016), 141–152.
114. Veith, N.M., Plattner, H., Stuermer, C.A., Schulz-Schaeffer, W.J., Burkle, A., Immunolocalisation of PrPSc in scrapie-infected N2a mouse neuroblastoma cells by light and electron microscopy. Eur. J. Cell Biol. 88:1 (2009), 45–63.
115. Vingtdeux, V., Hamdane, M., Loyens, A., Gele, P., Drobeck, H., Begard, S., Galas, M.C., Delacourte, A., Beauvillain, J.C., Buee, L., Sergeant, N., Alkalizing drugs induce accumulation of amyloid precursor protein by-products in luminal vesicles of multivesicular bodies. J. Biol. Chem. 282:25 (2007), 18197–18205.
116. Walker, L.C., Levine, H. 3rd, Mattson, M.P., Jucker, M., Inducible proteopathies. Trends Neurosci. 29:8 (2006), 438–443.
117. Wren, M.C., Zhao, J., Liu, C.C., Murray, M.E., Atagi, Y., Davis, M.D., Fu, Y., Okano, H.J., Ogaki, K., Strongosky, A.J., Tacik, P., Rademakers, R., Ross, O.A., Dickson, D.W., Wszolek, Z.K., Kanekiyo, T., Bu, G., Frontotemporal dementia-associated N279K tau mutant disrupts subcellular vesicle trafficking and induces cellular stress in iPSC-derived neural stem cells. Mol. Neurodegener., 10, 2015, 46.
118. Yanez-Mo, M., Siljander, P.R., Andreu, Z., Zavec, A.B., Borras, F.E., Buzas, E.I., Buzas, K., Casal, E., Cappello, F., Carvalho, J., Colas, E., Cordeiro-da Silva, A., Fais, S., Falcon-Perez, J.M., Ghobrial, I.M., Giebel, B., Gimona, M., Graner, M., Gursel, I., Gursel, M., Heegaard, N.H., Hendrix, A., Kierulf, P., Kokubun, K., Kosanovic, M., Kralj-Iglic, V., Kramer-Albers, E.M., Laitinen, S., Lasser, C., Lener, T., Ligeti, E., Line, A., Lipps, G., Llorente, A., Lotvall, J., Mancek-Keber, M., Marcilla, A., Mittelbrunn, M., Nazarenko, I., Nolte Hoen, E.N., Nyman, T.A., O'Driscoll, L., Olivan, M., Oliveira, C., Pallinger, E., Del Portillo, H.A., Reventos, J., Rigau, M., Rohde, E., Sammar, M., Sanchez-Madrid, F., Santarem, N., Schallmoser, K., Ostenfeld, M.S., Stoorvogel, W., Stukelj, R., Van der Grein, S.G., Vasconcelos, M.H., Wauben, M.H., De Wever, O., Biological properties of extracellular vesicles and their physiological functions. J. Extracell. Vesicles, 4, 2015, 27066.
119. Yang, J.M., Gould, S.J., The cis-acting signals that target proteins to exosomes and microvesicles. Biochem. Soc. Trans. 41:1 (2013), 277–282.
120. Yao, H., Zhao, D., Khan, S.H., Yang, L., Role of autophagy in prion protein-induced neurodegenerative diseases. Acta Biochim. Biophys. Sin. (Shanghai) 45:6 (2013), 494–502.
121. Yuyama, K., Yamamoto, N., Yanagisawa, K., Accelerated release of exosome-associated GM1 ganglioside (GM1) by endocytic pathway abnormality: another putative pathway for GM1-induced amyloid fibril formation. J. Neurochem. 105:1 (2008), 217–224.
122. Yuyama, K., Sun, H., Mitsutake, S., Igarashi, Y., Sphingolipid-modulated exosome secretion promotes clearance of amyloid-beta by microglia. J. Biol. Chem. 287:14 (2012), 10977–10989.