Nanoparticles restore lysosomal acidification defects: Implications for Parkinson and other lysosomal-related diseases

Autophagy

Volumn 12, Issue 3, 2016, Pages 472-483

  Bourdenx, Mathieu ^a,b   Daniel, Jonathan ^a   Genin, Emilie ^a   Soria, Federico N ^a,b   Blanchard Desce, Mireille ^a   Bezard, Erwan ^a,b   Dehay, Benjamin ^a,b  

^a UNIVERSITÉ DE BORDEAUX   (France)

^b INSTITUT DES MALADIES NEURODÉGÉNÉRATIVES   (France)

Author keywords

ATP13A2; GBA, lysosome; nanoparticles; neurodegeneration; Parkinson disease; XMEA

Indexed keywords

ACID PHOSPHATASE; ADENOSINE TRIPHOSPHATASE; ALPHA SYNUCLEIN; BETA N ACETYLHEXOSAMINIDASE; CHLOROQUINE; GLUCOSYLCERAMIDASE; NANOPARTICLE; 1 METHYL 4 PHENYLPYRIDINIUM; ACID; ALKALI; LACTIC ACID; POLYGLYCOLIC ACID; POLYLACTIC ACID-POLYGLYCOLIC ACID COPOLYMER;

ACIDIFICATION; ARTICLE; CELL DEATH; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; ELECTRON MICROSCOPY; FIBROBLAST; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; LYSOSOME; LYSOSOME STORAGE DISEASE; MOUSE; NONHUMAN; PARKINSON DISEASE; PH; PROTEIN DEGRADATION; TRANSMISSION ELECTRON MICROSCOPY; WESTERN BLOTTING; ANIMAL; BIOLOGICAL MODEL; CHEMISTRY; INTRACEREBROVENTRICULAR DRUG ADMINISTRATION; METABOLISM; NEOSTRIATUM; NERVE DEGENERATION; PATHOLOGY; ULTRASTRUCTURE;

1-METHYL-4-PHENYLPYRIDINIUM; ACIDS; ALKALIES; ANIMALS; CELL DEATH; DOPAMINERGIC NEURONS; HUMANS; HYDROGEN-ION CONCENTRATION; INJECTIONS, INTRAVENTRICULAR; LACTIC ACID; LYSOSOMAL STORAGE DISEASES; LYSOSOMES; MICE; MODELS, BIOLOGICAL; MODELS, GENETIC; NANOPARTICLES; NEOSTRIATUM; NERVE DEGENERATION; PARKINSON DISEASE; POLYGLYCOLIC ACID;

EID: 84962628366     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.1080/15548627.2015.1136769     Document Type: Article

References (49)

1. B.Dehay, A.Ramirez, M.Martinez-Vicente, C.Perier, M.H.Canron, E.Doudnikoff, A.Vital, M.Vila, C.Klein, E.Bezard. Loss of P-type ATPase ATP13A2/PARK9 function induces general lysosomal deficiency and leads to Parkinson disease neurodegeneration. Proc Natl Acad Sci U S A 2012; 109:9611-6; PMID:22647602; http:dx.doi.org/10.1073/pnas.1112368109
2. M.Usenovic, E.Tresse, J.R.Mazzulli, J.P.Taylor, D.Krainc. Deficiency of ATP13A2 leads to lysosomal dysfunction, α-synuclein accumulation, and neurotoxicity. J Neurosci 2012; 32:4240-6; PMID:22442086; http:dx.doi.org/10.1523/JNEUROSCI.5575-11.2012
3. A.Sanchez-Danes, Y.Richaud-Patin, I.Carballo-Carbajal, S.Jimenez-Delgado, C.Caig, S.Mora, C.Di Guglielmo, M.Ezquerra, B.Patel, A.Giralt, et al. Disease-specific phenotypes in dopamine neurons from human iPS-based models of genetic and sporadic Parkinson disease. EMBO Mol Med 2012; 4:380-95; PMID:22407749; http:dx.doi.org/10.1002/emmm.201200215
4. B.Dehay, J.Bove, N.Rodriguez-Muela, C.Perier, A.Recasens, P.Boya, M.Vila. Pathogenic lysosomal depletion in Parkinson disease. J Neurosci 2010; 30:12535-44; PMID:20844148; http:dx.doi.org/10.1523/JNEUROSCI.1920-10.2010
5. Y.Chu, H.Dodiya, P.Aebischer, C.W.Olanow, J.H.Kordower. Alterations in lysosomal and proteasomal markers in Parkinson disease: relationship to α-synuclein inclusions. Neurobiol Dis 2009; 35:385-98; PMID:19505575; http:dx.doi.org/10.1016/j.nbd.2009.05.023
6. P.Anglade, S.Vyas, F.Javoy-Agid, M.T.Herrero, P.P.Michel, J.Marquez, A.Mouatt-Prigent, M.Ruberg, E.C.Hirsch, Y.Agid. Apoptosis and autophagy in nigral neurons of patients with Parkinson disease. Histol Histopathol 1997; 12:25-31; PMID:9046040
7. L.Alvarez-Erviti, M.C.Rodriguez-Oroz, J.M.Cooper, C.Caballero, I.Ferrer, J.A.Obeso, A.H.Schapira. Chaperone-mediated autophagy markers in Parkinson disease brains. Arch Neurol 2010; 67:1464-72; PMID:20697033; http:dx.doi.org/10.1001/archneurol.2010.198
8. O.Corti, S.Lesage, A.Brice. What genetics tells us about the causes and mechanisms of Parkinson disease. Physiol Rev 2011; 91:1161-218; PMID:22013209; http:dx.doi.org/10.1152/physrev.00022.2010
9. E.Sidransky, M.A.Nalls, J.O.Aasly, J.Aharon-Peretz, G.Annesi, E.R.Barbosa, A.Bar-Shira, D.Berg, J.Bras, A.Brice, et al. Multicenter analysis of glucocerebrosidase mutations in Parkinson disease. N Engl J Med 2009; 361:1651-61; PMID:19846850; http:dx.doi.org/10.1056/NEJMoa0901281
10. A.Ramirez, A.Heimbach, J.Grundemann, B.Stiller, D.Hampshire, L.P.Cid, I.Goebel, A.F.Mubaidin, A.L.Wriekat, J.Roeper, et al. Hereditary parkinsonism with dementia is caused by mutations in ATP13A2, encoding a lysosomal type 5 P-type ATPase. Nat Genet 2006; 38:1184-91; PMID:16964263; http:dx.doi.org/10.1038/ng1884
11. B.Dehay, M.Martinez-Vicente, G.A.Caldwell, K.A.Caldwell, Z.Yue, M.R.Cookson, C.Klein, M.Vila, E.Bezard. Lysosomal impairment in Parkinson disease. Mov Disord 2013; 28:725-32; PMID:23580333; http:dx.doi.org/10.1002/mds.25462
12. M.Xilouri, O.R.Brekk, N.Landeck, P.M.Pitychoutis, T.Papasilekas, Z.Papadopoulou-Daifoti, D.Kirik, L.Stefanis. Boosting chaperone-mediated autophagy in vivo mitigates α-synuclein-induced neurodegeneration. Brain 2013; 136:2130-46; PMID:23757764; http:dx.doi.org/10.1093/brain/awt131
13. M.Decressac, B.Mattsson, P.Weikop, M.Lundblad, J.Jakobsson, A.Bjorklund. TFEB-mediated autophagy rescues midbrain dopamine neurons from α-synuclein toxicity. Proc Natl Acad Sci U S A 2013; 110:E1817-26; PMID:23610405; http:dx.doi.org/10.1073/pnas.1305623110
14. B.Spencer, R.Potkar, M.Trejo, E.Rockenstein, C.Patrick, R.Gindi, A.Adame, T.Wyss-Coray, E.Masliah. Beclin 1 gene transfer activates autophagy and ameliorates the neurodegenerative pathology in α-synuclein models of Parkinson and Lewy body diseases. J Neurosci 2009; 29:13578-88; PMID:19864570; http:dx.doi.org/10.1523/JNEUROSCI.4390-09.2009
15. Y.Diebold, M.Calonge. Applications of nanoparticles in ophthalmology. Prog Retin Eye Res 2010; 29:596-609; PMID:20826225; http:dx.doi.org/10.1016/j.preteyeres.2010.08.002
16. L.Hasadsri, J.Kreuter, H.Hattori, T.Iwasaki, J.M.George. Functional protein delivery into neurons using polymeric nanoparticles. J Biol Chem 2009; 284:6972-81; PMID:19129199; http:dx.doi.org/10.1074/jbc.M805956200
17. G.Sahay, D.Y.Alakhova, A.V.Kabanov. Endocytosis of nanomedicines. J Control Release 2010; 145:182-95; PMID:20226220; http:dx.doi.org/10.1016/j.jconrel.2010.01.036
18. G.C.Baltazar, S.Guha, W.Lu, J.Lim, K.Boesze-Battaglia, A.M.Laties, P.Tyagi, U.B.Kompella, C.H.Mitchell. Acidic nanoparticles are trafficked to lysosomes and restore an acidic lysosomal pH and degradative function to compromised ARPE-19 cells. PloS One 2012; 7:e49635; PMID:23272048; http:dx.doi.org/10.1371/journal.pone.0049635
19. J.Panyam, W.Z.Zhou, S.Prabha, S.K.Sahoo, V.Labhasetwar. Rapid endo-lysosomal escape of poly(DL-lactide-co-glycolide) nanoparticles: implications for drug and gene delivery. FASEB J 2002; 16:1217-26; PMID:12153989; http:dx.doi.org/10.1096/fj.02-0088com
20. J.Panyam, S.K.Sahoo, S.Prabha, T.Bargar, V.Labhasetwar. Fluorescence and electron microscopy probes for cellular and tissue uptake of poly(D,L-lactide-co-glycolide) nanoparticles. Int J Pharm 2003; 262:1-11; PMID:12927382; http:dx.doi.org/10.1016/S0378-5173(03)00295-3
21. P.Boya, G.Kroemer. Lysosomal membrane permeabilization in cell death. Oncogene 2008; 27:6434-51; PMID:18955971; http:dx.doi.org/10.1038/onc.2008.310
22. M.Vila, J.Bove, B.Dehay, N.Rodriguez-Muela, P.Boya. Lysosomal membrane permeabilization in Parkinson disease. Autophagy 2011; 7:98-100; PMID:21045565; http:dx.doi.org/10.4161/auto.7.1.13933
23. J.Bove, M.Martinez-Vicente, B.Dehay, C.Perier, A.Recasens, A.Bombrun, B.Antonsson, M.Vila. BAX channel activity mediates lysosomal disruption linked to Parkinson disease. Autophagy 2014; 10:889-900; PMID:24686337; http:dx.doi.org/10.4161/auto.28286
24. D.C.Wu, P.Teismann, K.Tieu, M.Vila, V.Jackson-Lewis, H.Ischiropoulos, S.Przedborski. NADPH oxidase mediates oxidative stress in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine model of Parkinson disease. Proc Natl Acad Sci U S A 2003; 100:6145-50; PMID:12721370; http:dx.doi.org/10.1073/pnas.0937239100
25. R.T.Dean. Lysosomes and protein degradation. Ciba Found Symp 1979:139-49; PMID:399886
26. E.I.Ginns, R.O.Brady, S.Pirruccello, C.Moore, S.Sorrell, F.S.Furbish, G.J.Murray, J.Tager, J.A.Barranger. Mutations of glucocerebrosidase: discrimination of neurologic and non-neurologic phenotypes of Gaucher disease. Proc Natl Acad Sci U S A 1982; 79:5607-10; PMID:6957882; http:dx.doi.org/10.1073/pnas.79.18.5607
27. M.Siebert, E.Sidransky, W.Westbroek. Glucocerebrosidase is shaking up the synucleinopathies. Brain 2014; 137:1304-22; PMID:24531622; http:dx.doi.org/10.1093/brain/awu002
28. M.Kurzawa-Akanbi, P.S.Hanson, P.G.Blain, D.J.Lett, I.G.McKeith, P.F.Chinnery, C.M.Morris. Glucocerebrosidase mutations alter the endoplasmic reticulum and lysosomes in Lewy body disease. J Neurochem 2012; 123:298-309; PMID:22803570; http:dx.doi.org/10.1111/j.1471-4159.2012.07879.x
29. J.R.Mazzulli, Y.H.Xu, Y.Sun, A.L.Knight, P.J.McLean, G.A.Caldwell, E.Sidransky, G.A.Grabowski, D.Krainc. Gaucher disease glucocerebrosidase and α-synuclein form a bidirectional pathogenic loop in synucleinopathies. Cell 2011; 146:37-52; PMID:21700325; http:dx.doi.org/10.1016/j.cell.2011.06.001
30. V.Cullen, S.P.Sardi, J.Ng, Y.H.Xu, Y.Sun, J.J.Tomlinson, P.Kolodziej, I.Kahn, P.Saftig, J.Woulfe, et al. Acid β-glucosidase mutants linked to Gaucher disease, Parkinson disease, and Lewy body dementia alter α-synuclein processing. Ann Neurol 2011; 69:940-53; PMID:21472771; http:dx.doi.org/10.1002/ana.22400
31. H.Kalimo, M.L.Savontaus, H.Lang, L.Paljarvi, V.Sonninen, P.B.Dean, K.Katevuo, A.Salminen. X-linked myopathy with excessive autophagy: a new hereditary muscle disease. Ann Neurol 1988; 23:258-65; PMID:2897824; http:dx.doi.org/10.1002/ana.410230308
32. N.Ramachandran, I.Munteanu, P.Wang, A.Ruggieri, J.J.Rilstone, N.Israelian, T.Naranian, P.Paroutis, R.Guo, Z.P.Ren, et al. VMA21 deficiency prevents vacuolar ATPase assembly and causes autophagic vacuolar myopathy. Acta Neuropathol 2013; 125:439-57; PMID:23315026; http:dx.doi.org/10.1007/s00401-012-1073-6
33. B.Dehay, M.Bourdenx, P.Gorry, S.Przedborski, M.Vila, S.Hunot, A.Singleton, C.W.Olanow, K.M.Merchant, E.Bezard, et al. Targeting α-synuclein for treatment of Parkinson disease: mechanistic and therapeutic considerations. Lancet Neurol 2015; 14(8):855-66
34. W.G.Meissner, M.Frasier, T.Gasser, C.G.Goetz, A.Lozano, P.Piccini, J.A.Obeso, O.Rascol, A.Schapira, V.Voon, et al. Priorities in Parkinson disease research. Nat Rev Drug Discov 2011; 10:377-93; PMID:21532567; http:dx.doi.org/10.1038/nrd3430
35. E.Bezard, C.Imbert, C.E.Gross. Experimental models of Parkinson disease: from the static to the dynamic. Rev Neurosci 1998; 9:71-90; PMID:9711900; http:dx.doi.org/10.1515/REVNEURO.1998.9.2.71
36. C.Settembre, R.Zoncu, D.L.Medina, F.Vetrini, S.Erdin, S.Erdin, T.Huynh, M.Ferron, G.Karsenty, M.C.Vellard, et al. A lysosome-to-nucleus signalling mechanism senses and regulates the lysosome via mTOR and TFEB. EMBO J 2012; 31:1095-108; PMID:22343943; http:dx.doi.org/10.1038/emboj.2012.32
37. M.Bourdenx, E.Bezard, B.Dehay. Lysosomes and α-synuclein form a dangerous duet leading to neuronal cell death. Front Neuroanat 2014; 8:83; PMID:25177278; http:dx.doi.org/10.3389/fnana.2014.00083
38. M.J.Clague, S.Urbe, F.Aniento, J.Gruenberg. Vacuolar ATPase activity is required for endosomal carrier vesicle formation. J Biol Chem 1994; 269:21-4; PMID:8276796
39. A.W.van Weert, K.W.Dunn, H.J.Geuze, F.R.Maxfield, W.Stoorvogel. Transport from late endosomes to lysosomes, but not sorting of integral membrane proteins in endosomes, depends on the vacuolar proton pump. J Cell Biol 1995; 130:821-34; PMID:7642700; http:dx.doi.org/10.1083/jcb.130.4.821
40. F.Danhier, E.Ansorena, J.M.Silva, R.Coco, A.Le Breton, V.Preat. PLGA-based nanoparticles: an overview of biomedical applications. J Control Release 2012; 161:505-22; PMID:22353619; http:dx.doi.org/10.1016/j.jconrel.2012.01.043
41. Y.Toyoda, C.Erkut, F.Pan-Montojo, S.Boland, M.P.Stewart, D.J.Muller, W.Wurst, A.A.Hyman, T.V.Kurzchalia. Products of the Parkinson disease-related glyoxalase DJ-1, D-lactate and glycolate, support mitochondrial membrane potential and neuronal survival. Biol Open 2014; 3:777-84; PMID:25063200; http:dx.doi.org/10.1242/bio.20149399
42. E.L.Eskelinen. Doctor Jekyll and Mister Hyde: autophagy can promote both cell survival and cell death. Cell Death Differ 2005; 12 Suppl 2:1468-72; PMID:16247492; http:dx.doi.org/10.1038/sj.cdd.4401721
43. J.H.Lee, W.H.Yu, A.Kumar, S.Lee, P.S.Mohan, C.M.Peterhoff, D.M.Wolfe, M.Martinez-Vicente, A.C.Massey, G.Sovak, et al. Lysosomal proteolysis and autophagy require presenilin 1 and are disrupted by Alzheimer-related PS1 mutations. Cell 2010; 141:1146-58; PMID:20541250; http:dx.doi.org/10.1016/j.cell.2010.05.008
44. P.Boya. Lysosomal function and dysfunction: mechanism and disease. Antioxid Redox Signal 2012; 17:766-74; PMID:22098160; http:dx.doi.org/10.1089/ars.2011.4405
45. S.Muro. New biotechnological and nanomedicine strategies for treatment of lysosomal storage disorders. Wiley Interdiscip Rev Nanomed Nanobiotechnol 2010; 2:189-204
46. C.A.Schneider, W.S.Rasband, K.W.Eliceiri. NIH Image to ImageJ: 25 years of image analysis. Nat Methods 2012; 9:671-5; PMID:22930834; http:dx.doi.org/10.1038/nmeth.2089
47. F.H.Sterky, A.F.Hoffman, D.Milenkovic, B.Bao, A.Paganelli, D.Edgar, R.Wibom, C.R.Lupica, L.Olson, N.G.Larsson. Altered dopamine metabolism and increased vulnerability to MPTP in mice with partial deficiency of mitochondrial complex I in dopamine neurons. Hum Mol Genet 2012; 21:1078-89; PMID:22090423; http:dx.doi.org/10.1093/hmg/ddr537
48. M.F.Bastide, S.Dovero, G.Charron, G.Porras, C.E.Gross, P.O.Fernagut, E.Bézard. Immediate-early gene expression in structures outside the basal ganglia is associated to l-DOPA-induced dyskinesia. Neurobiol Dis 2014; 62:179-92; PMID:24103779; http:dx.doi.org/10.1016/j.nbd.2013.09.020
49. M.Engeln, M.F.Bastide, E.Toulme, B.Dehay, M.Bourdenx, E.Doudnikoff, Q.Li, C.E.Gross, E.Boué-Grabot, A.Pisani, et al. Selective Inactivation of Striatal FosB/DeltaFosB-Expressing Neurons Alleviates L-Dopa-Induced Dyskinesia. Biol Psychiatry 2014; 79(5):338-340; PMID:25146322.