Enhancing astrocytic lysosome biogenesis facilitates Aβ clearance and attenuates amyloid plaque pathogenesis

Journal of Neuroscience

Volumn 34, Issue 29, 2014, Pages 9607-9620

  Xiao, Qingli ^a   Yan, Ping ^a   Ma, Xiucui ^a,b   Liu, Haiyan ^a   Perez, Ronaldo ^a   Zhu, Alec ^a   Gonzales, Ernesto ^a   Burchett, Jack M ^a   Schuler, Dorothy R ^a   Cirrito, John R ^a   Diwan, Abhinav ^a,b   Lee, Jin Moo ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Alzheimer's disease; Amyloid; Astrocytes; Lysosomes; TFEB

Indexed keywords

ALZHEIMER'S DISEASE; AMYLOID; ASTROCYTES; LYSOSOMES; TFEB;

AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; ANIMALS, NEWBORN; ASTROCYTES; BASIC HELIX-LOOP-HELIX LEUCINE ZIPPER TRANSCRIPTION FACTORS; CEREBRAL CORTEX; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; LYSOSOMES; MALE; MICE; MICE, TRANSGENIC; PEPTIDE FRAGMENTS; PLAQUE, AMYLOID; PRESENILIN-1; TRANSFECTION;

EID: 84904354536     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3788-13.2014     Document Type: Article

References (74)

1. Avrahami L, Farfara D, Shaham-Kol M, Vassar R, Frenkel D, Eldar-Finkelman H (2013) Inhibition of glycogen synthase kinase-3 ameliorates beta-amyloid pathology and restores lysosomal acidification and mammalian target of rapamycin activity in the Alzheimer disease mouse model: in vivo and in vitro studies. J Biol Chem 288:1295-1306. CrossRef Medline
2. Baldo G, Wu S, Howe RA, Ramamoothy M, Knutsen RH, Fang J, Mecham RP, Liu Y, Wu X, Atkinson JP, Ponder KP (2011) Pathogenesis of aortic dilatation in mucopolysaccharidosis VII mice may involve complement activation. Mol Genet Metab 104:608-619. CrossRef Medline
3. Barres BA (2008) The mystery and magic of glia: a perspective on their roles in health and disease. Neuron 60:430-440. CrossRef Medline
4. Basak JM, Verghese PB, Yoon H, Kim J, Holtzman DM (2012) Low-density lipoprotein receptor represents an apolipoprotein E-independent pathway of Abeta uptake and degradation by astrocytes. J Biol Chem 287: 13959-13971. CrossRef Medline
5. Bateman RJ, Munsell LY, Morris JC, Swarm R, Yarasheski KE, Holtzman DM (2006) Human amyloid-beta synthesis and clearance rates as measured in CSF in vivo. Nat Med 12:856-861. CrossRef Medline
6. Brenner M, Kisseberth WC, Su Y, Besnard F, Messing A (1994) GFAP promoter directs astrocyte-specific expression in transgenic mice. J Neurosci 14:1030-1037. Medline
7. Bushong EA, Martone ME, Jones YZ, Ellisman MH (2002) Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains. J Neurosci 22:183-192. Medline
8. Butler D, Hwang J, Estick C, Nishiyama A, Kumar SS, Baveghems C, Young-Oxendine HB, Wisniewski ML, Charalambides A, Bahr BA (2011) Protective effects of positive lysosomal modulation in Alzheimer's disease transgenic mouse models. PLo S One 6:e20501. CrossRef Medline
9. Cai Z, Zhao B, Li K, Zhang L, Li C, Quazi SH, Tan Y (2012) Mammalian target of rapamycin: a valid therapeutic target through the autophagy pathway for Alzheimer's disease? J Neurosci Res 90:1105-1118. CrossRef Medline
10. Callahan MJ, Lipinski WJ, Bian F, Durham RA, Pack A, Walker LC (2001) Augmented senile plaque load in aged female beta-amyloid precursor protein-transgenic mice. Am J Pathol 158:1173-1177. CrossRef Medline
11. Carter SF, Schöll M, Almkvist O, Wall A, Engler H, Långström B, Nordberg A (2012) Evidence for astrocytosis in prodromal Alzheimer disease provided by 11C-deuterium-L-deprenyl: a multitracer PET paradigm combining 11C-Pittsburgh compound B and 18F-FDG. J Nucl Med 53:37-46. CrossRef Medline
12. Castellano JM, Deane R, Gottesdiener AJ, Verghese PB, Stewart FR, West T, Paoletti AC, Kasper TR, De Mattos RB, Zlokovic BV, Holtzman DM (2012) Low-density lipoprotein receptor overexpression enhances the rate of brain-to-blood Abeta clearance in a mouse model of betaamyloidosis. Proc Natl Acad Sci U S A 109:15502-15507. CrossRef Medline
13. Cirrito JR, May PC, O'Dell MA, Taylor JW, Parsadanian M, Cramer JW, Audia JE, Nissen JS, Bales KR, Paul SM, De Mattos RB, Holtzman DM (2003) In vivo assessment of brain interstitial fluid with microdialysis reveals plaque-associated changes in amyloid-beta metabolism and halflife. J Neurosci 23:8844-8853. Medline
14. Cirrito JR, Disabato BM, Restivo JL, Verges DK, Goebel WD, Sathyan A, Hayreh D, D'Angelo G, Benzinger T, Yoon H, Kim J, Morris JC, Mintun MA, Sheline YI (2011) Serotonin signaling is associated with lower amyloid-beta levels and plaques in transgenic mice and humans. Proc Natl Acad Sci U S A 108:14968-14973. CrossRef Medline
15. Coen K, Flannagan RS, Baron S, Carraro-Lacroix LR, Wang D, Vermeire W, Michiels C, Munck S, Baert V, Sugita S, Wuytack F, Hiesinger PR, Grinstein S, Annaert W (2012) Lysosomal calcium homeostasis defects, not proton pump defects, cause endo-lysosomal dysfunction in PSENdeficient cells. J Cell Biol 198:23-35. CrossRef Medline
16. Cuervo AM, Dice JF (2000) When lysosomes get old. Exp Gerontol 35:119-131. CrossRef Medline
17. Decressac M, Mattsson B, Weikop P, Lundblad M, Jakobsson J, Björklund A (2013) TFEB-mediated autophagy rescues midbrain dopamine neurons from alpha-synuclein toxicity. Proc Natl Acad Sci U S A 110:E1817-E1826. CrossRef Medline
18. DiMalta C, Fryer JD, Settembre C, Ballabio A (2012) Astrocyte dysfunction triggers neurodegeneration in a lysosomal storage disorder. Proc Natl Acad Sci U S A 109:E2334-E2342. CrossRef Medline
19. Eroglu C, Barres BA (2010) Regulation of synaptic connectivity by glia. Nature 468:223-231. CrossRef Medline
20. Fan TC, Chang HT, Chen IW, Wang HY, Chang MD (2007) A heparan sulfate-facilitated and raft-dependent macropinocytosis of eosinophil cationic protein. Traffic 8:1778-1795. CrossRef Medline
21. Funato H, Yoshimura M, Yamazaki T, Saido TC, Ito Y, Yokofujita J, Okeda R, Ihara Y (1998) Astrocytes containing amyloid beta-protein (Abeta)-positive granules are associated with Abeta40-positive diffuse plaques in the aged human brain. Am J Pathol 152:983-992. Medline
22. Gong Y, Chang L, Viola KL, Lacor PN, Lambert MP, Finch CE, Krafft GA, Klein WL (2003) Alzheimer's disease-affected brain: presence of oligomeric A beta ligands (ADDLs) suggests a molecular basis for reversible memory loss. Proc Natl Acad Sci U S A 100:10417-10422. CrossRef Medline
23. Hardy J, Selkoe DJ (2002) The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297:353-356. CrossRef Medline
24. Hartmann T, Bieger SC, Brühl B, Tienari PJ, Ida N, Allsop D, Roberts GW, Masters CL, Dotti CG, Unsicker K, Beyreuther K (1997) Distinct sites of intracellular production for Alzheimer's disease A beta40/42 amyloid peptides. Nat Med 3:1016-1020. CrossRef Medline
25. Holmes BB, De Vos SL, Kfoury N, Li M, Jacks R, Yanamandra K, Ouidja MO, Brodsky FM, Marasa J, Bagchi DP, Kotzbauer PT, Miller TM, Papy-Garcia D, Diamond MI (2013) Heparan sulfate proteoglycans mediate internalization and propagation of specific proteopathic seeds. Proc Natl Acad Sci U S A 110:E3138-E3147. CrossRef Medline
26. Hu X, Crick SL, Bu G, Frieden C, Pappu RV, Lee JM (2009) Amyloid seeds formed by cellular uptake, concentration, and aggregation of the amyloid-beta peptide. Proc Natl Acad Sci U S A 106:20324-20329. CrossRef Medline
27. Jankowsky JL, Fadale DJ, Anderson J, Xu GM, Gonzales V, Jenkins NA, Copeland NG, Lee MK, Younkin LH, Wagner SL, Younkin SG, Borchelt DR (2004) Mutant presenilins specifically elevate the levels of the 42 residue beta-amyloid peptide in vivo: evidence for augmentation of a 42-specific gamma secretase. Hum Mol Genet 13:159-170. Medline
28. Kamenetz F, Tomita T, Hsieh H, Seabrook G, Borchelt D, Iwatsubo T, Sisodia S, Malinow R (2003) APP processing and synaptic function. Neuron 37:925-937. CrossRef Medline
29. Kanekiyo T, Zhang J, Liu Q, Liu CC, Zhang L, Bu G (2011) Heparan sulphate proteoglycan and the low-density lipoprotein receptor-related protein 1 constitute major pathways for neuronal amyloid-beta uptake. J Neurosci 31:1644-1651. CrossRef Medline
30. Kato Y, Maruyama W, Naoi M, Hashizume Y, Osawa T (1998) Immunohistochemical detection of dityrosine in lipofuscin pigments in the aged human brain. FEBS Lett 439:231-234. CrossRef Medline
31. Kim J, Castellano JM, Jiang H, Basak JM, Parsadanian M, Pham V, Mason SM, Paul SM, Holtzman DM (2009) Overexpression of low-density lipoprotein receptor in the brain markedly inhibits amyloid deposition and increases extracellular A beta clearance. Neuron 64:632-644. CrossRef Medline
32. Koistinaho M, Lin S, Wu X, Esterman M, Koger D, Hanson J, Higgs R, Liu F, Malkani S, Bales KR, Paul SM (2004) Apolipoprotein E promotes astrocyte colocalization and degradation of deposited amyloid-beta peptides. Nat Med 10:719-726. CrossRef Medline
33. Kraft AW, Hu X, Yoon H, Yan P, Xiao Q, Wang Y, Gil SC, Brown J, Wilhelmsson U, Restivo JL, Cirrito JR, Holtzman DM, Kim J, Pekny M, Lee JM (2013) Attenuating astrocyte activation accelerates plaque pathogenesis in APP/PS1 mice. FASEB J 27:187-198. CrossRef Medline
34. Lafay-Chebassier C, Paccalin M, Page G, Barc-Pain S, Perault-Pochat MC, Gil R, Pradier L, Hugon J (2005) mTOR/p70S6k signalling alteration by Abeta exposure as well as in APP-PS1 transgenic models and in patients with Alzheimer's disease. J Neurochem 94:215-225. CrossRef Medline
35. Lee JH, Yu WH, Kumar A, Lee S, Mohan PS, Peterhoff CM, Wolfe DM, Martinez-Vicente M, Massey AC, Sovak G, Uchiyama Y, Westaway D, Cuervo AM, Nixon RA (2010) Lysosomal proteolysis and autophagy require presenilin 1 and are disrupted by Alzheimer-related PS1 mutations. Cell 141:1146-1158. CrossRef Medline
36. Lomakin A, Teplow DB, Kirschner DA, Benedek GB (1997) Kinetic theory of fibrillogenesis of amyloid beta-protein. Proc Natl Acad Sci U S A 94: 7942-7947. CrossRef Medline
37. Ma X, Liu H, Foyil SR, Godar RJ, Weinheimer CJ, Hill JA, Diwan A (2012) Impaired autophagosome clearance contributes to cardiomyocyte death in ischemia/reperfusion injury. Circulation 125:3170-3181. CrossRef Medline
38. Macauley SL, Pekny M, Sands MS (2011) The role of attenuated astrocyte activation in infantile neuronal ceroid lipofuscinosis. J Neurosci 31: 15575-15585. CrossRef Medline
39. Mandrekar S, Jiang Q, Lee CY, Koenigsknecht-Talboo J, Holtzman DM, Landreth GE (2009) Microglia mediate the clearance of soluble Abeta through fluid phase macropinocytosis. J Neurosci 29:4252-4262. CrossRef Medline
40. Martina JA, Puertollano R (2013) Rag GTPases mediate amino aciddependent recruitment of TFEB and MITF to lysosomes. J Cell Biol 200: 475-491. CrossRef Medline
41. Mawuenyega KG, Sigurdson W, Ovod V, Munsell L, Kasten T, Morris JC, Yarasheski KE, Bateman RJ (2010) Decreased clearance of CNS betaamyloid in Alzheimer's disease. Science 330:1774. CrossRef Medline
42. Medina DL, Fraldi A, Bouche V, Annunziata F, Mansueto G, Spampanato C, Puri C, Pignata A, Martina JA, Sardiello M, Palmieri M, Polishchuk R, Puertollano R, Ballabio A (2011) Transcriptional activation of lysosomal exocytosis promotes cellular clearance. Dev Cell 21:421-430. CrossRef Medline
43. Menacherry S, Hubert W, Justice JB Jr (1992) In vivo calibration of microdialysis probes for exogenous compounds. Anal Chem 64:577-583. CrossRef Medline
44. Mousavi SA, Kjeken R, Berg TO, Seglen PO, Berg T, Brech A (2001) Effects of inhibitors of the vacuolar proton pump on hepatic heterophagy and autophagy. Biochim Biophys Acta 1510:243-257. CrossRef Medline
45. Mueller-Steiner S, Zhou Y, Arai H, Roberson ED, Sun B, Chen J, Wang X, Yu G, Esposito L, Mucke L, Gan L (2006) Antiamyloidogenic and neuroprotective functions of cathepsin B: implications for Alzheimer's disease. Neuron 51:703-714. CrossRef Medline
46. Nagele RG, D'Andrea MR, Lee H, Venkataraman V, Wang HY (2003) Astrocytes accumulate A beta 42 and give rise to astrocytic amyloid plaques in Alzheimer disease brains. Brain Res 971:197-209. CrossRef Medline
47. Nielsen HM, Veerhuis R, Holmqvist B, Janciauskiene S (2009) Binding and uptake of A beta1-42 by primary human astrocytes in vitro. Glia 57:978-988. CrossRef Medline
48. Nixon RA, Cataldo AM (2006) Lysosomal system pathways: genes to neurodegeneration in Alzheimer's disease. J Alzheimers Dis 9:277-289. Medline
49. Owen JB, Di Domenico F, Sultana R, Perluigi M, Cini C, Pierce WM, Butterfield DA (2009) Proteomics-determined differences in the concanavalin-Afractionated proteome of hippocampus and inferior parietal lobule in subjects with Alzheimer's disease and mild cognitive impairment: implications for progression of AD. J Proteome Res 8:471-482. CrossRef Medline
50. Palmieri M, Impey S, Kang H, di Ronza A, Pelz C, Sardiello M, Ballabio A (2011) Characterization of the CLEAR network reveals an integrated control of cellular clearance pathways. Hum Mol Genet 20:3852-3866. CrossRef Medline
51. Peña-Llopis S, Vega-Rubin-de-Celis S, Schwartz JC, Wolff NC, Tran TA, Zou L, Xie XJ, Corey DR, Brugarolas J (2011) Regulation of TFEB and V-ATPases by m TORC1. EMBO J 30:3242-3258. CrossRef Medline
52. Roczniak-Ferguson A, Petit CS, Froehlich F, Qian S, Ky J, Angarola B, Walther TC, Ferguson SM (2012) The transcription factor TFEB links m TORC1 signaling to transcriptional control of lysosome homeostasis. Sci Signal 5:ra42. CrossRef Medline
53. Roh JH, Huang Y, Bero AW, Kasten T, Stewart FR, Bateman RJ, Holtzman DM (2012) Disruption of the sleep-wake cycle and diurnal fluctuation of beta-amyloid in mice with Alzheimer's disease pathology. Sci Transl Med 4:150ra122. CrossRef Medline
54. Sardiello M, Palmieri M, di Ronza A, Medina DL, Valenza M, Gennarino VA, Di Malta C, Donaudy F, Embrione V, Polishchuk RS, Banfi S, Parenti G, Cattaneo E, Ballabio A (2009) A gene network regulating lysosomal biogenesis and function. Science 325:473-477. CrossRef Medline
55. Schipper HM, Bennett DA, Liberman A, Bienias JL, Schneider JA, Kelly J, Arvanitakis Z (2006) Glial heme oxygenase-1 expression in Alzheimer disease and mild cognitive impairment. Neurobiol Aging 27:252-261. CrossRef Medline
56. Schuur M, Ikram MA, van Swieten JC, Isaacs A, Vergeer-Drop JM, Hofman A, Oostra BA, Breteler MM, van Duijn CM (2011) Cathepsin D gene and the risk of Alzheimer's disease: a population-based study and metaanalysis. Neurobiol Aging 32:1607-1614. CrossRef Medline
57. Settembre C, Di Malta C, Polito VA, Garcia Arencibia M, Vetrini F, Erdin S, Erdin SU, Huynh T, Medina D, Colella P, Sardiello M, Rubinsztein DC, Ballabio A (2011) TFEB links autophagy to lysosomal biogenesis. Science 332:1429-1433. CrossRef Medline
58. Settembre C, Zoncu R, Medina DL, Vetrini F, Erdin S, Huynh T, Ferron M, Karsenty G, Vellard MC, Facchinetti V, Sabatini DM, Ballabio A (2012) A lysosome-to-nucleus signalling mechanism senses and regulates the lysosome viam TORand TFEB. EMBOJ 31:1095-1108. CrossRef Medline
59. Settembre C, Fraldi A, Medina DL, Ballabio A (2013a) Signals from the lysosome: a control centre for cellular clearance and energy metabolism. Nat Rev Mol Cell Biol 14:283-296. CrossRef Medline
60. Settembre C, De Cegli R, Mansueto G, Saha PK, Vetrini F, Visvikis O, Huynh T, Carissimo A, Palmer D, Klisch TJ, Wollenberg AC, Di Bernardo D, Chan L, Irazoqui JE, Ballabio A (2013b) TFEB controls cellular lipid metabolism through a starvation-induced autoregulatory loop. Nat Cell Biol 15:647-658. CrossRef Medline
61. Song W, Wang F, Lotfi P, Sardiello M, Segatori L (2014) 2-Hydroxypropylbeta-cyclodextrin promotes transcription factor EB-mediated activation of autophagy: implications for therapy. J Biol Chem 289:10211-10222. CrossRef Medline
62. Sun B, Zhou Y, Halabisky B, Lo I, Cho SH, Mueller-Steiner S, Devidze N, Wang X, Grubb A, Gan L (2008) Cystatin C-cathepsin B axis regulates amyloid beta levels and associated neuronal deficits in an animal model of Alzheimer's disease. Neuron 60:247-257. CrossRef Medline
63. Tsunemi T, Ashe TD, Morrison BE, Soriano KR, Au J, Roque RA, Lazarowski ER, Damian VA, Masliah E, La Spada AR (2012) PGC-1alpha rescues Huntington's disease proteotoxicity by preventing oxidative stress and promoting TFEB function. Sci Transl Med 4:142ra97. CrossRef Medline
64. Verges DK, Restivo JL, Goebel WD, Holtzman DM, Cirrito JR (2011) Opposing synaptic regulation of amyloid-beta metabolism by NMDAreceptors in vivo. J Neurosci 31:11328-11337. CrossRef Medline
65. Verghese PB, Castellano JM, Garai K, Wang Y, Jiang H, Shah A, Bu G, Frieden C, Holtzman DM (2013) Apo E influences amyloid-beta (Abeta) clearance despite minimal apo E/Abeta association in physiological conditions. Proc Natl Acad Sci U S A 110:E1807-1816. CrossRef Medline
66. West MJ, Slomianka L, Gundersen HJ (1991) Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231:482-497. CrossRef Medline
67. Wolfe DM, Lee JH, Kumar A, Lee S, Orenstein SJ, Nixon RA (2013) Autophagy failure in Alzheimer's disease and the role of defective lysosomal acidification. Eur J Neurosci 37:1949-1961. CrossRef Medline
68. Wyss-Coray T, Loike JD, Brionne TC, Lu E, Anankov R, Yan F, Silverstein SC, Husemann J (2003) Adult mouse astrocytes degrade amyloid-beta in vitro and in situ. Nat Med 9:453-457. CrossRef Medline
69. Xiao Q, Gil SC, Yan P, Wang Y, Han S, Gonzales E, Perez R, Cirrito JR, Lee JM (2012) Role of phosphatidylinositol clathrin assembly lymphoidmyeloid leukemia (PICALM) in intracellular amyloid precursor protein (APP) processing and amyloid plaque pathogenesis. J Biol Chem 287: 21279-21289. CrossRef Medline
70. Yamamoto A, Tagawa Y, Yoshimori T, Moriyama Y, Masaki R, Tashiro Y (1998) Bafilomycin A1 prevents maturation of autophagic vacuoles by inhibiting fusion between autophagosomes and lysosomes in rat hepatoma cell line, H-4-II-E cells. Cell Struct Funct 23:33-42. CrossRef Medline
71. Yan P, Bero AW, Cirrito JR, Xiao Q, Hu X, Wang Y, Gonzales E, Holtzman DM, Lee JM (2009) Characterizing the appearance and growth of amyloid plaques in APP/PS1 mice. J Neurosci 29:10706-10714. CrossRef Medline
72. Yang DS, Stavrides P, Mohan PS, Kaushik S, Kumar A, Ohno M, Schmidt SD, Wesson D, Bandyopadhyay U, Jiang Y, Pawlik M, Peterhoff CM, Yang AJ, Wilson DA, St George-Hyslop P, Westaway D, Mathews PM, Levy E, Cuervo AM, Nixon RA (2011) Reversal of autophagy dysfunction in the Tg CRND8 mouse model of Alzheimer's disease ameliorates amyloid pathologies and memory deficits. Brain 134:258-277. CrossRef Medline
73. Zang Y, Yu LF, Pang T, Fang LP, Feng X, Wen TQ, Nan FJ, Feng LY, Li J (2008) AICAR induces astroglial differentiation of neural stem cells via activating the JAK/STAT3 pathway independently of AMP-activated protein kinase. J Biol Chem 283:6201-6208. CrossRef Medline
74. Zoncu R, Bar-Peled L, Efeyan A, Wang S, Sancak Y, Sabatini DM (2011) m TORC1 senses lysosomal amino acids through an inside-out mechanism that requires the vacuolar H(+)-ATPase. Science 334:678-683. CrossRef Medline