Microglia convert aggregated amyloid-β into neurotoxic forms through the shedding of microvesicles

Cell Death and Differentiation

Volumn 21, Issue 4, 2014, Pages 582-593

  Joshi, P ^a,b   Turola, E ^a,b   Ruiz, A ^a   Bergami, A ^c   Libera, D D ^c   Benussi, L ^d   Giussani, P ^a   Magnani, G ^c   Comi, G ^c   Legname, G ^e   Ghidoni, R ^d   Furlan, R ^c   Matteoli, M ^a,f   Verderio, C ^b,f  

^a UNIVERSITY OF MILAN   (Italy)

^b CNR   (Italy)

^c SAN RAFFAELE HOSPITAL   (Italy)

^d IRCCS Istituto Centro San Giovanni di Dio Fatebenefratelli   (Italy)

^e SISSA   (Italy)

^f HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

Author keywords

Abeta 1 42; Alzheimers disease; bioactive lipids; extracellular microvesicles; microglia; prion protein

Indexed keywords

AMYLOID BETA PROTEIN; LIPID;

ALZHEIMER DISEASE; ARTICLE; BRAIN DEGENERATION; CELL ACTIVATION; CELL MIGRATION; CELL VACUOLE; FIBER; HIPPOCAMPAL NEURONAL CULTURE; HUMAN; IN VITRO STUDY; MICROGLIA; MICROVESICLE; MILD COGNITIVE IMPAIRMENT; NERVE CELL CULTURE; NERVE FIBER; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; CELL SURVIVAL; CELLS, CULTURED; EXCITATORY AMINO ACID ANTAGONISTS; FEMALE; HUMANS; INTERLEUKIN-1BETA; MALE; MICROGLIA; NEURONS; PEPTIDE FRAGMENTS; PRPC PROTEINS; RATS; SOLUBILITY; TRANSPORT VESICLES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84903362492     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2013.180     Document Type: Article

References (64)

1. Herring A, Lewejohann L, Panzer AL, Donath A, Kroll O, Sachser N et al. Preventive and therapeutic types of environmental enrichment counteract beta amyloid pathology by different molecular mechanisms. Neurobiol Dis 2011; 42: 530-538.
2. Schilling S, Lauber T, Schaupp M, Manhart S, Scheel E, Bohm G et al. On the seeding and oligomerization of pGlu-amyloid peptides (in vitro). Biochemistry 2006; 45: 12393-12399.
3. Bieschke J, Herbst M, Wiglenda T, Friedrich RP, Boeddrich A, Schiele F et al. Small-molecule conversion of toxic oligomers to nontoxic beta-sheet-rich amyloid fibrils. Nat Chem Biol 2012; 8: 93-101.
4. Winklhofer KF, Tatzelt J, Haass C. The two faces of protein misfolding: gain- and loss-offunction in neurodegenerative diseases. EMBO J 2008; 27: 336-349.
5. Benilova I, Karran E, De Strooper B. The toxic Abeta oligomer and Alzheimer's disease: an emperor in need of clothes. Nat Neurosci 2012; 15: 349-357.
6. Lue LF, Brachova L, Civin WH, Rogers J. Inflammation, A beta deposition, and neurofibrillary tangle formation as correlates of Alzheimer's disease neurodegeneration. J Neuropathol Exp Neurol 1996; 55: 1083-1088.
7. Haass C, Mandelkow E. Fyn-tau-amyloid: a toxic triad. Cell 2010; 142: 356-358.
8. Serrano-Pozo A, Mielke ML, Gomez-Isla T, Betensky RA, Growdon JH, Frosch MP et al. Reactive glia not only associates with plaques but also parallels tangles in Alzheimer's disease. Am J Pathol 2011; 179: 1373-1384.
9. Serrano-Pozo A, Mielke ML, Muzitansky A, Gomez-Isla T, Growdon JH, Bacskai BJ et al. Stable size distribution of amyloid plaques over the course of Alzheimer disease. J Neuropathol Exp Neurol 2012; 71: 694-701.
10. Walsh DM, Selkoe DJ. A beta oligomers - a decade of discovery. J Neurochem 2007; 101: 1172-1184.
11. McLean CA, Cherny RA, Fraser FW, Fuller SJ, Smith MJ, Beyreuther K et al. Soluble pool of Abeta amyloid as a determinant of severity of neurodegeneration in Alzheimer's disease. Ann Neurol 1999; 46: 860-866.
12. Mielke MM, Haughey NJ, Bandaru VV, Weinberg DD, Darby E, Zaidi N et al. Plasma sphingomyelins are associated with cognitive progression in Alzheimer's disease. J Alzheimers Dis 2011; 27: 259-269.
13. Martins IC, Kuperstein I, Wilkinson H, Maes E, Vanbrabant M, Jonckheere W et al. Lipids revert inert Abeta amyloid fibrils to neurotoxic protofibrils that affect learning in mice. EMBO J 2008; 27: 224-233.
14. Johansson AS, Garlind A, Berglind-Dehlin F, Karlsson G, Edwards K, Gellerfors P et al. Docosahexaenoic acid stabilizes soluble amyloid-beta protofibrils and sustains amyloidbeta- induced neurotoxicity in vitro. FEBS J 2007; 274: 990-1000.
15. Snyder EM, Nong Y, Almeida CG, Paul S, Moran T, Choi EY et al. Regulation of NMDA receptor trafficking by amyloid-beta. Nat Neurosci 2005; 8: 1051-1058.
16. Lauren J, Gimbel DA, Nygaard HB, Gilbert JW, Strittmatter SM. Cellular prion protein mediates impairment of synaptic plasticity by amyloid-beta oligomers. Nature 2009; 457: 1128-1132.
17. Um JW, Nygaard HB, Heiss JK, Kostylev MA, Stagi M, Vortmeyer A et al. Alzheimer amyloid-beta oligomer bound to postsynaptic prion protein activates Fyn to impair neurons. Nat Neurosci 2012; 15: 1227-1235.
18. Verdier Y, Zarandi M, Penke B. Amyloid beta-peptide interactions with neuronal and glial cell plasma membrane: binding sites and implications for Alzheimer's disease. J Pept Sci 2004; 10: 229-248.
19. Edison P, Archer HA, Gerhard A, Hinz R, Pavese N, Turkheimer FE et al. Microglia, amyloid, and cognition in Alzheimer's disease: An [11C](R)PK11195-PET and [11C]PIB-PET study. Neurobiol Dis 2008; 32: 412-419.
20. Okello A, Edison P, Archer HA, Turkheimer FE, Kennedy J, Bullock R et al. Microglial activation and amyloid deposition in mild cognitive impairment: a PET study. Neurology 2009; 72: 56-62.
21. Hollingworth P, Harold D, Sims R, Gerrish A, Lambert JC, Carrasquillo MM et al. Common variants at ABCA7, MS4A6A/MS4A4E, EPHA1, CD33 and CD2AP are associated with Alzheimer's disease. Nat Genet 2011; 43: 429-435.
22. Guerreiro R, Wojtas A, Bras J, Carrasquillo M, Rogaeva E, Majounie E et al. TREM2 variants in Alzheimer's disease. N Engl J Med 2013; 368: 117-127.
23. Giulian D, Haverkamp LJ, Yu JH, Karshin W, Tom D, Li J et al. Specific domains of beta-amyloid from Alzheimer plaque elicit neuron killing in human microglia. J Neurosci 1996; 16: 6021-6037.
24. Fuhrmann M, Bittner T, Jung CK, Burgold S, Page RM, Mitteregger G et al. Microglial Cx3cr1 knockout prevents neuron loss in a mouse model of Alzheimer's disease. Nat Neurosci 2010; 13: 411-413.
25. Tan B, Choi RH, Chin TJ, Kaur C, Ling EA. Manipulation of microglial activity as a therapy for Alzheimer's disease. Front Biosci 2012; 4: 1402-1412.
26. Weitz TM, Town T. Microglia in Alzheimer's Disease: it's all about context. Int J Alzheimers Dis 2012; 2012: 314185.
27. Bianco F, Pravettoni E, Colombo A, Schenk U, Moller T, Matteoli M et al. induces vesicle shedding and IL-1 beta release from microglia. J Immunol 2005; 174: 7268-7277.
28. Del Conde I, Shrimpton CN, Thiagarajan P, Lopez JA. Tissue-factor-bearing microvesicles arise from lipid rafts and fuse with activated platelets to initiate coagulation. Blood 2005; 106: 1604-1611.
29. Gonnord P, Delarasse C, Auger R, Benihoud K, Prigent M, Cuif MH et al. Palmitoylation of the P2X7 receptor, an ATP-gated channel, controls its expression and association with lipid rafts. FASEB J 2009; 23: 795-805.
30. Verderio C, Muzio L, Turola E, Bergami A, Novellino L, Ruffini F et al. Myeloid microvesicles are a marker and therapeutic target for neuroinflammation. Ann Neurol 2012; 72: 610-624.
31. Colombo E, Borgiani B, Verderio C, Furlan R. Microvesicles: novel biomarkers for neurological disorders. Front Physiol 2012; 3: 63.
32. Rajendran L, Honsho M, Zahn TR, Keller P, Geiger KD, Verkade P et al. Alzheimer's disease beta-amyloid peptides are released in association with exosomes. Proc Natl Acad Sci USA 2006; 103: 11172-11177.
33. Perry VH, Nicoll JA, Holmes C. Microglia in neurodegenerative disease. Nat Rev Neurol 2010; 6: 193-201.
34. Fukunaga S, Ueno H, Yamaguchi T, Yano Y, Hoshino M, Matsuzaki K. GM1 cluster mediates formation of toxic Abeta fibrils by providing hydrophobic environments. Biochemistry 2012; 51: 8125-8131.
35. Turola E, Furlan R, Bianco F, Matteoli M, Verderio C. Microglial microvesicle secretion and intercellular signaling. Front Physiol 2012; 3: 149.
36. Jana A, Pahan K. Fibrillar amyloid-beta-activated human astroglia kill primary human neurons via neutral sphingomyelinase: implications for Alzheimer's disease. J Neurosci 2010; 30: 12676-12689.
37. Alberdi E, Sanchez-Gomez MV, Cavaliere F, Perez-Samartin A, Zugaza JL, Trullas R et al. Amyloid beta oligomers induce Ca2 dysregulation and neuronal death through activation of ionotropic glutamate receptors. Cell Calcium 2010; 47: 264-272.
38. Bianco F, Perrotta C, Novellino L, Francolini M, Riganti L, Menna E et al. Acid sphingomyelinase activity triggers microparticle release from glial cells. EMBO J 2009; 28: 1043-1054.
39. Holtzman DM. CSF biomarkers for Alzheimer's disease: current utility and potential future use. Neurobiol Aging 2011; 32(Suppl 1): S4-S9.
40. Yuyama K, Sun H, Mitsutake S, Igarashi Y. Sphingolipid-modulated exosome secretion promotes clearance of amyloid-beta by microglia. J Biol Chem 2012; 287: 10977-10989.
41. Thery C, Ostrowski M, Segura E. Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 2009; 9: 581-593.
42. Mattei V, Barenco MG, Tasciotti V, Garofalo T, Longo A, Boller K et al. Paracrine diffusion of PrP(C) and propagation of prion infectivity by plasma membrane-derived microvesicles. PLoS One 2009; 4: e5057.
43. Han X, Fagan AM, Cheng H, Morris JC, Xiong C, Holtzman DM. Cerebrospinal fluid sulfatide is decreased in subjects with incipient dementia. Ann Neurol 2003; 54: 115-119.
44. Malnar M, Kosicek M, Bene R, Tarnik IP, Pavelin S, Babic I et al. Use of cerebrospinal fluid biomarker analysis for improving Alzheimer's disease diagnosis in a non-specialized setting. Acta Neurobiol Exp 2012; 72: 264-271.
45. Ghidoni R, Paterlini A, Albertini V, Glionna M, Monti E, Schiaffonati L et al. Cystatin C is released in association with exosomes: a new tool of neuronal communication which is unbalanced in Alzheimer's disease. Neurobiol Aging 2011; 32: 1435-1442.
46. Vella LJ, Sharples RA, Nisbet RM, Cappai R, Hill AF. The role of exosomes in the processing of proteins associated with neurodegenerative diseases. Eur Biophys J 2008; 37: 323-332.
47. Vingtdeux V, Hamdane M, Begard S, Loyens A, Delacourte A, Beauvillain JC et al. Intracellular pH regulates amyloid precursor protein intracellular domain accumulation. Neurobiol Dis 2007; 25: 686-696.
48. Yamamoto M, Kiyota T, Walsh SM, Liu J, Kipnis J, Ikezu T. Cytokine-mediated inhibition of fibrillar amyloid-beta peptide degradation by human mononuclear phagocytes. J Immunol 2008; 181: 3877-3886.
49. Aguzzi A, Barres BA, Bennett ML. Microglia: scapegoat, saboteur, or something else? Science 2013; 339: 156-161.
50. Prinz M, Priller J, Sisodia SS, Ransohoff RM. Heterogeneity of CNS myeloid cells and their roles in neurodegeneration. Nat Neurosci 2011; 14: 1227-1235.
51. Paresce DM, Chung H, Maxfield FR. Slow degradation of aggregates of the Alzheimer's disease amyloid beta-protein by microglial cells. J Biol Chem 1997; 272: 29390-29397.
52. Lee CY, Landreth GE. The role of microglia in amyloid clearance from the AD brain. J Neural Transm 2010; 117: 949-960.
53. Rajendran L, Annaert W. Membrane trafficking pathways in Alzheimer's disease. Traffic 2012; 13: 759-770.
54. Ariga T, Kobayashi K, Hasegawa A, Kiso M, Ishida H, Miyatake T. Characterization of high-affinity binding between gangliosides and amyloid beta-protein. Arch Biochem Biophys 2001; 388: 225-230.
55. Kiyota T, Yamamoto M, Xiong H, Lambert MP, Klein WL, Gendelman HE et al. CCL2 accelerates microglia-mediated Abeta oligomer formation and progression of neurocognitive dysfunction. PLoS One 2009; 4: e6197.
56. Shen B, Wu N, Yang JM, Gould SJ. Protein targeting to exosomes/microvesicles by plasma membrane anchors. J Biol Chem 2011; 286: 14383-14395.
57. Sharples RA, Vella LJ, Nisbet RM, Naylor R, Perez K, Barnham KJ et al. Inhibition of gamma-secretase causes increased secretion of amyloid precursor protein C-terminal fragments in association with exosomes. FASEB J 2008; 22: 1469-1478.
58. Tamboli IY, Barth E, Christian L, Siepmann M, Kumar S, Singh S et al. Statins promote the degradation of extracellular amyloid {beta}-peptide by microglia via stimulation of exosome-associated insulin-degrading enzyme (IDE) secretion. J Biol Chem 2010; 285: 37405-37414.
59. Antonucci F, Turola E, Riganti L, Caleo M, Gabrielli M, Perrotta C et al. Microvesicles released from microglia stimulate synaptic activity via enhanced sphingolipid metabolism. EMBO J 2012; 31: 1231-1240.
60. Klein WL. Abeta toxicity in Alzheimer's disease: globular oligomers (ADDLs) as new vaccine and drug targets. Neurochem Int 2002; 41: 345-352.
61. De Felice FG, Wu D, Lambert MP, Fernandez SJ, Velasco PT, Lacor PN et al. Alzheimer's disease-type neuronal tau hyperphosphorylation induced by A beta oligomers. Neurobiol Aging 2008; 29: 1334-1347.
62. Frassoni C, Inverardi F, Coco S, Ortino B, Grumelli C, Pozzi D et al. Analysis of SNAP-25 immunoreactivity in hippocampal inhibitory neurons during development in culture and in situ. Neuroscience 2005; 131: 813-823.
63. Paluzzi S, Alloisio S, Zappettini S, Milanese M, Raiteri L, Nobile M et al. Adult astroglia is competent for Na/Ca2 exchanger-operated exocytotic glutamate release triggered by mild depolarization. J Neurochem 2007; 103: 1196-1207.
64. Albertini V, Bruno A, Paterlini A, Lista S, Benussi L, Cereda C et al. Optimization protocol for amyloid-beta peptides detection in human cerebrospinal fluid using SELDI TOF MS. Proteomics Clin Appl 2010; 4: 352-357.