Exosomes-associated neurodegeneration and progression of Parkinson’s disease

American Journal of Neurodegenerative Diseases

Volumn 1, Issue 3, 2012, Pages 217-225

  Russo, Isabella ^a   Bubacco, Luigi ^a   Greggio, Elisa ^a  

^a UNIVERSITY OF PADOVA   (Italy)

Author keywords

Exosomes; LRRK2; Neuronal degeneration; Parkinson s disease; synuclein

Indexed keywords

ALPHA SYNUCLEIN; AMYLOID PRECURSOR PROTEIN; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; INTERLEUKIN 1BETA; LEUCINE RICH REPEAT KINASE 2; PATHOGEN ASSOCIATED MOLECULAR PATTERN; PATTERN RECOGNITION RECEPTOR; TUMOR NECROSIS FACTOR ALPHA;

ADRENERGIC TRANSMISSION; ANTIGEN PRESENTATION; ASTROCYTE; BIOGENESIS; CELL ACTIVATION; CELL COMMUNICATION; DOPAMINERGIC SYSTEM; EXOSOME; HUMAN; INFLAMMATION; MAJOR HISTOCOMPATIBILITY COMPLEX; MICROGLIA; NERVE DEGENERATION; NEUROPATHOLOGY; OXIDATIVE STRESS; PARKINSON DISEASE; PROTEIN AGGREGATION; PROTEIN PROTEIN INTERACTION; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM;

EID: 84980053722     PISSN: None     EISSN: 2165591X     Source Type: Journal    
DOI: None     Document Type: Review

References (82)

1. Brundin P, Li JY, Holton JL, Lindvall O and Revesz T. Research in motion: the enigma of Parkinson's disease pathology spread. Nat Rev Neurosci 2008; 9: 741-745.
2. Riess O, Kruger R and Schulz JB. Spectrum of phenotypes and genotypes in Parkinson's disease. J Neurol 2002; 249 Suppl 3: III/15-20.
3. Lees AJ, Hardy J and Revesz T. Parkinson's disease. Lancet 2009; 373: 2055-2066.
4. Forno LS. Neuropathology of Parkinson's disease. J Neuropathol Exp Neurol 1996; 55: 259- 272.
5. Ali SF, Binienda ZK and Imam SZ. Molecular aspects of dopaminergic neurodegeneration: gene-environment interaction in parkin dysfunction. Int J Environ Res Public Health 2011; 8: 4702-4713.
6. Houlden H and Singleton AB. The genetics and neuropathology of Parkinson's disease. Acta Neuropathol 2012; 124: 325-338.
7. Lee VM and Trojanowski JQ. Mechanisms of Parkinson's disease linked to pathological alpha- synuclein: new targets for drug discovery. Neuron 2006; 52: 33-38.
8. Lee HJ, Kim C and Lee SJ. Alpha-synuclein stimulation of astrocytes: Potential role for neuroinflammation and neuroprotection. Oxid Med Cell Longev 2010; 3: 283-287.
9. Kim C and Lee SJ. Controlling the mass action of alpha-synuclein in Parkinson's disease. J Neurochem 2008; 107: 303-316.
10. Giasson BI, Murray IV, Trojanowski JQ and Lee VM. A hydrophobic stretch of 12 amino acid residues in the middle of alpha-synuclein is essential for filament assembly. J Biol Chem 2001; 276: 2380-2386.
11. Hardy J, Lewis P, Revesz T, Lees A and Paisan- Ruiz C. The genetics of Parkinson's syndromes: a critical review. Curr Opin Genet Dev 2009; 19: 254-265.
12. Nalls MA, Plagnol V, Hernandez DG, Sharma M, Sheerin UM, Saad M, Simon-Sanchez J, Schulte C, Lesage S, Sveinbjornsdottir S, Stefansson K, Martinez M, Hardy J, Heutink P, Brice A, Gasser T, Singleton AB and Wood NW. Imputation of sequence variants for identification of genetic risks for Parkinson's disease: a meta-analysis of genome-wide association studies. Lancet 2011; 377: 641-649.
13. Marques O and Outeiro TF. Alpha-synuclein: from secretion to dysfunction and death. Cell Death Dis 2012; 3: e350.
14. Greggio E, Bisaglia M, Civiero L and Bubacco L. Leucine-rich repeat kinase 2 and alphasynuclein: intersecting pathways in the pathogenesis of Parkinson's disease? Mol Neurodegener 2011; 6: 6.
15. Chinta SJ and Andersen JK. Dopaminergic neurons. Int J Biochem Cell Biol 2005; 37: 942- 946.
16. Damier P, Hirsch EC, Agid Y and Graybiel AM. The substantia nigra of the human brain. II. Patterns of loss of dopamine-containing neurons in Parkinson's disease. Brain 1999; 122: 1437-1448.
17. Fearnley JM and Lees AJ. Ageing and Parkinson's disease: substantia nigra regional selectivity. Brain 1991; 114: 2283-2301.
18. Hirsch EC, Faucheux B, Damier P, Mouatt- Prigent A and Agid Y. Neuronal vulnerability in Parkinson's disease. J Neural Transm Suppl 1997; 50: 79-88.
19. Double KL, Reyes S, Werry EL and Halliday GM. Selective cell death in neurodegeneration: why are some neurons spared in vulnerable regions? Prog Neurobiol 2010; 92: 316-329.
20. Hindle JV. Ageing, neurodegeneration and Parkinson's disease. Age Ageing 2010; 39: 156- 161.
21. Korytowski W, Sarna T and Zarba M. Antioxidant action of neuromelanin: the mechanism of inhibitory effect on lipid peroxidation. Arch Biochem Biophys 1995; 319: 142-148.
22. Youdim MB, Ben-Shachar D and Riederer P. Is Parkinson's disease a progressive siderosis of substantia nigra resulting in iron and melanin induced neurodegeneration? Acta Neurol Scand Suppl 1989; 126: 47-54.
23. Bisaglia M, Mammi S and Bubacco L. Kinetic and structural analysis of the early oxidation products of dopamine: analysis of the interactions with alpha-synuclein. J Biol Chem 2007; 282: 15597-15605.
24. Conway KA, Rochet JC, Bieganski RM and Lansbury PT Jr. Kinetic stabilization of the alphasynuclein protofibril by a dopamine-alphasynuclein adduct. Science 2001; 294: 1346- 1349.
25. Lawson LJ, Perry VH, Dri P and Gordon S. Heterogeneity in the distribution and morphology of microglia in the normal adult mouse brain. Neuroscience 1990; 39: 151-170.
26. Braak H, Ghebremedhin E, Rub U, Bratzke H and Del Tredici K. Stages in the development of Parkinson's disease-related pathology. Cell Tissue Res 2004; 318: 121-134.
27. Braak H, Del Tredici K, Rub U, de Vos RA, Jansen Steur EN and Braak E. Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol Aging 2003; 24: 197-211.
28. Goedert M, Clavaguera F and Tolnay M. The propagation of prion-like protein inclusions in neurodegenerative diseases. Trends Neurosci 2010; 33: 317-325.
29. Fauvet B, Mbefo MK, Fares MB, Desobry C, Michael S, Ardah MT, Tsika E, Coune P, Prudent M, Lion N, Eliezer D, Moore DJ, Schneider B, Aebischer P, El-Agnaf OM, Masliah E and Lashuel HA. alpha-Synuclein in central nervous system and from erythrocytes, mammalian cells, and Escherichia coli exists predominantly as disordered monomer. J Biol Chem 2012; 287: 15345-15364.
30. Bartels T, Choi JG and Selkoe DJ. alpha- Synuclein occurs physiologically as a helically folded tetramer that resists aggregation. Nature 2011; 477: 107-110.
31. Wang W, Perovic I, Chittuluru J, Kaganovich A, Nguyen LT, Liao J, Auclair JR, Johnson D, Landeru A, Simorellis AK, Ju S, Cookson MR, Asturias FJ, Agar JN, Webb BN, Kang C, Ringe D, Petsko GA, Pochapsky TC and Hoang QQ. A soluble alpha-synuclein construct forms a dynamic tetramer. Proc Natl Acad Sci USA 2011; 108: 17797-17802.
32. Volpicelli-Daley LA, Luk KC, Patel TP, Tanik SA, Riddle DM, Stieber A, Meaney DF, Trojanowski JQ and Lee VM. Exogenous alpha-synuclein fibrils induce Lewy body pathology leading to synaptic dysfunction and neuron death. Neuron 2011; 72: 57-71.
33. Lesage S and Brice A. Parkinson's disease: from monogenic forms to genetic susceptibility factors. Hum Mol Genet 2009; 18: R48-59.
34. Spillantini MG, Crowther RA, Jakes R, Hasegawa M and Goedert M. alpha-Synuclein in filamentous inclusions of Lewy bodies from Parkinson's disease and dementia with lewy bodies. Proc Natl Acad Sci USA 1998; 95: 6469 -6473.
35. Ebrahimi-Fakhari D, Cantuti-Castelvetri I, Fan Z, Rockenstein E, Masliah E, Hyman BT, McLean PJ and Unni VK. Distinct roles in vivo for the ubiquitin-proteasome system and the autophagy- lysosomal pathway in the degradation of alpha-synuclein. J Neurosci 2011; 31: 14508- 14520.
36. Li JY, Englund E, Holton JL, Soulet D, Hagell P, Lees AJ, Lashley T, Quinn NP, Rehncrona S, Bjorklund A, Widner H, Revesz T, Lindvall O and Brundin P. Lewy bodies in grafted neurons in subjects with Parkinson's disease suggest hostto- graft disease propagation. Nat Med 2008; 14: 501-503.
37. Kordower JH, Chu Y, Hauser RA, Freeman TB and Olanow CW. Lewy body-like pathology in long-term embryonic nigral transplants in Parkinson's disease. Nat Med 2008; 14: 504-506.
38. Steiner JA, Angot E and Brundin P. A deadly spread: cellular mechanisms of alpha-synuclein transfer. Cell Death Differ 2011; 18: 1425- 1433.
39. Aguzzi A and Rajendran L. The transcellular spread of cytosolic amyloids, prions, and prionoids. Neuron 2009; 64: 783-790.
40. Bellingham SA, Guo BB, Coleman BM and Hill AF. Exosomes: vehicles for the transfer of toxic proteins associated with neurodegenerative diseases? Front Physiol 2012; 3: 124.
41. Schneider A and Simons M. Exosomes: vesicular carriers for intercellular communication in neurodegenerative disorders. Cell Tissue Res 2012.
42. Thery C, Amigorena S, Raposo G and Clayton A. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol 2006; Chapter 3: Unit 3 22.
43. Faure J, Lachenal G, Court M, Hirrlinger J, Chatellard-Causse C, Blot B, Grange J, Schoehn G, Goldberg Y, Boyer V, Kirchhoff F, Raposo G, Garin J and Sadoul R. Exosomes are released by cultured cortical neurones. Mol Cell Neurosci 2006; 31: 642-648.
44. Potolicchio I, Carven GJ, Xu X, Stipp C, Riese RJ, Stern LJ and Santambrogio L. Proteomic analysis of microglia-derived exosomes: metabolic role of the aminopeptidase CD13 in neuropeptide catabolism. J Immunol 2005; 175: 2237- 2243.
45. Taylor AR, Robinson MB, Gifondorwa DJ, Tytell M and Milligan CE. Regulation of heat shock protein 70 release in astrocytes: role of signaling kinases. Dev Neurobiol 2007; 67: 1815- 1829.
46. Bobrie A, Colombo M, Raposo G and Thery C. Exosome secretion: molecular mechanisms and roles in immune responses. Traffic 2011; 12: 1659-1668.
47. Simons M and Raposo G. Exosomes--vesicular carriers for intercellular communication. Curr Opin Cell Biol 2009; 21: 575-581.
48. Lee TH, D'Asti E, Magnus N, Al-Nedawi K, Meehan B and Rak J. Microvesicles as mediators of intercellular communication in cancer-- the emerging science of cellular 'debris'. Semin Immunopathol 2011; 33: 455-467.
49. Keller S, Sanderson MP, Stoeck A and Altevogt P. Exosomes: from biogenesis and secretion to biological function. Immunol Lett 2006; 107: 102-108.
50. Thery C, Boussac M, Veron P, Ricciardi-Castagnoli P, Raposo G, Garin J and Amigorena S. Proteomic analysis of dendritic cell-derived exosomes: a secreted subcellular compartment distinct from apoptotic vesicles. J Immunol 2001; 166: 7309-7318.
51. Kramer-Albers EM, Bretz N, Tenzer S, Winterstein C, Mobius W, Berger H, Nave KA, Schild H and Trotter J. Oligodendrocytes secrete exosomes containing major myelin and stressprotective proteins: Trophic support for axons? Proteomics Clin Appl 2007; 1: 1446-1461.
52. Thery C, Zitvogel L and Amigorena S. Exosomes: composition, biogenesis and function. Nat Rev Immunol 2002; 2: 569-579.
53. van Niel G, Porto-Carreiro I, Simoes S and Raposo G. Exosomes: a common pathway for a specialized function. J Biochem 2006; 140: 13- 21.
54. Dello Sbarba P and Rovida E. Transmodulation of cell surface regulatory molecules via ectodomain shedding. Biol Chem 2002; 383: 69-83.
55. Marzesco AM, Janich P, Wilsch-Brauninger M, Dubreuil V, Langenfeld K, Corbeil D and Huttner WB. Release of extracellular membrane particles carrying the stem cell marker prominin-1 (CD133) from neural progenitors and other epithelial cells. J Cell Sci 2005; 118: 2849- 2858.
56. Lachenal G, Pernet-Gallay K, Chivet M, Hemming FJ, Belly A, Bodon G, Blot B, Haase G, Goldberg Y and Sadoul R. Release of exosomes from differentiated neurons and its regulation by synaptic glutamatergic activity. Mol Cell Neurosci 2011; 46: 409-418.
57. Raposo G, Nijman HW, Stoorvogel W, Liejendekker R, Harding CV, Melief CJ and Geuze HJ. B lymphocytes secrete antigen-presenting vesicles. J Exp Med 1996; 183: 1161-1172.
58. Thery C, Ostrowski M and Segura E. Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 2009; 9: 581-593.
59. Alvarez-Erviti L, Seow Y, Schapira AH, Gardiner C, Sargent IL, Wood MJ and Cooper JM. Lysosomal dysfunction increases exosomemediated alpha-synuclein release and transmission. Neurobiol Dis 2011; 42: 360-367.
60. Emmanouilidou E, Melachroinou K, Roumeliotis T, Garbis SD, Ntzouni M, Margaritis LH, Stefanis L and Vekrellis K. Cell-produced alphasynuclein is secreted in a calcium-dependent manner by exosomes and impacts neuronal survival. J Neurosci 2010; 30: 6838-6851.
61. Desplats P, Lee HJ, Bae EJ, Patrick C, Rockenstein E, Crews L, Spencer B, Masliah E and Lee SJ. Inclusion formation and neuronal cell death through neuron-to-neuron transmission of alpha- synuclein. Proc Natl Acad Sci USA 2009; 106: 13010-13015.
62. Hansen C, Angot E, Bergstrom AL, Steiner JA, Pieri L, Paul G, Outeiro TF, Melki R, Kallunki P, Fog K, Li JY and Brundin P. alpha-Synuclein propagates from mouse brain to grafted dopaminergic neurons and seeds aggregation in cultured human cells. J Clin Invest 2011; 121: 715-725.
63. Zitvogel L, Regnault A, Lozier A, Wolfers J, Flament C, Tenza D, Ricciardi-Castagnoli P, Raposo G and Amigorena S. Eradication of established murine tumors using a novel cell-free vaccine: dendritic cell-derived exosomes. Nat Med 1998; 4: 594-600.
64. Chaput N, Flament C, Viaud S, Taieb J, Roux S, Spatz A, Andre F, LePecq JB, Boussac M, Garin J, Amigorena S, Thery C and Zitvogel L. Dendritic cell derived-exosomes: biology and clinical implementations. J Leukoc Biol 2006; 80: 471-478.
65. Bhatnagar S, Shinagawa K, Castellino FJ and Schorey JS. Exosomes released from macrophages infected with intracellular pathogens stimulate a proinflammatory response in vitro and in vivo. Blood 2007; 110: 3234-3244.
66. Lee HJ, Suk JE, Bae EJ, Lee JH, Paik SR and Lee SJ. Assembly-dependent endocytosis and clearance of extracellular alpha-synuclein. Int J Biochem Cell Biol 2008; 40: 1835-1849.
67. Lee HJ, Suk JE, Patrick C, Bae EJ, Cho JH, Rho S, Hwang D, Masliah E and Lee SJ. Direct transfer of alpha-synuclein from neuron to astroglia causes inflammatory responses in synucleinopathies. J Biol Chem 2010; 285: 9262- 9272.
68. Halliday GM and Stevens CH. Glia: initiators and progressors of pathology in Parkinson's disease. Mov Disord 2011; 26: 6-17.
69. Vekrellis K, Xilouri M, Emmanouilidou E, Rideout HJ and Stefanis L. Pathological roles of alpha-synuclein in neurological disorders. Lancet Neurol 2011; 10: 1015-1025.
70. Alvarez-Erviti L, Couch Y, Richardson J, Cooper JM and Wood MJ. Alpha-synuclein release by neurons activates the inflammatory response in a microglial cell line. Neurosci Res 2011; 69: 337-342.
71. Gao HM and Hong JS. Why neurodegenerative diseases are progressive: uncontrolled inflammation drives disease progression. Trends Immunol 2008; 29: 357-365.
72. Panaro MA and Cianciulli A. Current opinions and perspectives on the role of immune system in the pathogenesis of Parkinson's disease. Curr Pharm Des 2012; 18: 200-208.
73. Shin N, Jeong H, Kwon J, Heo HY, Kwon JJ, Yun HJ, Kim CH, Han BS, Tong Y, Shen J, Hatano T, Hattori N, Kim KS, Chang S and Seol W. LRRK2 regulates synaptic vesicle endocytosis. Exp Cell Res 2008; 314: 2055-2065.
74. Piccoli G, Condliffe SB, Bauer M, Giesert F, Boldt K, De Astis S, Meixner A, Sarioglu H, Vogt-Weisenhorn DM, Wurst W, Gloeckner CJ, Matteoli M, Sala C and Ueffing M. LRRK2 controls synaptic vesicle storage and mobilization within the recycling pool. J Neurosci 2011; 31: 2225- 2237.
75. Xiong Y, Coombes CE, Kilaru A, Li X, Gitler AD, Bowers WJ, Dawson VL, Dawson TM and Moore DJ. GTPase activity plays a key role in the pathobiology of LRRK2. PLoS Genet 2010; 6: e1000902.
76. Alegre-Abarrategui J, Christian H, Lufino MM, Mutihac R, Venda LL, Ansorge O and Wade- Martins R. LRRK2 regulates autophagic activity and localizes to specific membrane microdomains in a novel human genomic reporter cellular model. Hum Mol Genet 2009; 18: 4022- 4034.
77. Fader CM, Sanchez DG, Mestre MB and Colombo MI. TI-VAMP/VAMP7 and VAMP3/ cellubrevin: two v-SNARE proteins involved in specific steps of the autophagy/multivesicular body pathways. Biochim Biophys Acta 2009; 1793: 1901-1916.
78. Clavaguera F, Bolmont T, Crowther RA, Abramowski D, Frank S, Probst A, Fraser G, Stalder AK, Beibel M, Staufenbiel M, Jucker M, Goedert M and Tolnay M. Transmission and spreading of tauopathy in transgenic mouse brain. Nat Cell Biol 2009; 11: 909-913.
79. Edwards TL, Scott WK, Almonte C, Burt A, Powell EH, Beecham GW, Wang L, Zuchner S, Konidari I, Wang G, Singer C, Nahab F, Scott B, Stajich JM, Pericak-Vance M, Haines J, Vance JM and Martin ER. Genome-wide association study confirms SNPs in SNCA and the MAPT region as common risk factors for Parkinson disease. Ann Hum Genet 2010; 74: 97-109.
80. Satake W, Nakabayashi Y, Mizuta I, Hirota Y, Ito C, Kubo M, Kawaguchi T, Tsunoda T, Watanabe M, Takeda A, Tomiyama H, Nakashima K, Hasegawa K, Obata F, Yoshikawa T, Kawakami H, Sakoda S, Yamamoto M, Hattori N, Murata M, Nakamura Y and Toda T. Genome-wide association study identifies common variants at four loci as genetic risk factors for Parkinson's disease. Nat Genet 2009; 41: 1303-1307.
81. Giasson BI, Forman MS, Higuchi M, Golbe LI, Graves CL, Kotzbauer PT, Trojanowski JQ and Lee VM. Initiation and synergistic fibrillization of tau and alpha-synuclein. Science 2003; 300: 636-640.
82. Sullivan CP, Jay AG, Stack EC, Pakaluk M, Wadlinger E, Fine RE, Wells JM and Morin PJ. Retromer disruption promotes amyloidogenic APP processing. Neurobiol Dis 2011; 43: 338-345.