Haploinsufficiency of cathepsin D leads to lysosomal dysfunction and promotes cell-to-cell transmission of α-synuclein aggregates

Cell Death and Disease

Volumn 6, Issue 10, 2015, Pages

  Bae, E J ^a   Yang, N Y ^b,d   Lee, C ^b,c   Kim, S ^a   Lee, H J ^b,c   Lee, S J ^a  

^a Seoul National University   (South Korea)

^b Konkuk University   (South Korea)

^c Konkuk University School of Medicine   (South Korea)

^d Cook Medical Korea ^*  (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; CATHEPSIN D; ZINC FINGER NUCLEASE; CTSD PROTEIN, HUMAN; PROTEIN AGGREGATE; STOP CODON;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; HAPLOINSUFFICIENCY; HETEROZYGOTE; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; LYSOSOMAL DYSFUNCTION; LYSOSOME; LYSOSOME STORAGE DISEASE; NEUROBLASTOMA CELL LINE; NONSENSE MUTATION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN SECRETION; WILD TYPE; ENZYMOLOGY; GAUCHER DISEASE; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE; PROTEIN TRANSPORT; STOP CODON; TUMOR CELL LINE;

ALPHA-SYNUCLEIN; BASE SEQUENCE; CATHEPSIN D; CELL LINE, TUMOR; CODON, NONSENSE; GAUCHER DISEASE; HAPLOINSUFFICIENCY; HUMANS; LYSOSOMES; PROTEIN AGGREGATES; PROTEIN TRANSPORT;

EID: 84975217705     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2015.283     Document Type: Article

References (61)

1. Rujano MA, Bosveld F, Salomons FA, Dijk F, van Waarde MA, van der Want JJ et al. Polarised asymmetric inheritance of accumulated protein damage in higher eukaryotes. PLoS Biol 2006; 4: e417.
2. Taylor RC, Dillin A. Aging as an event of proteostasis collapse. Cold Spring Harb Perspect Biol 2011; 3: 5.
3. Korolchuk VI, Menzies FM, Rubinsztein DC. Mechanisms of cross-talk between the ubiquitin-proteasome and autophagy-lysosome systems. FEBS Lett 2010; 584: 1393-1398.
4. Lecker SH, Goldberg AL, Mitch WE. Protein degradation by the ubiquitin-proteasome pathway in normal and disease states. J Am Soc Nephrol 2006; 17: 1807-1819.
5. Ciechanover A. Proteolysis: from the lysosome to ubiquitin and the proteasome. Nat Rev Mol Cell Biol 2005; 6: 79-87.
6. Menzies FM, Ravikumar B, Rubinsztein DC. Protective roles for induction of autophagy in multiple proteinopathies. Autophagy 2006; 2: 224-225.
7. Matsuda N, Tanaka K. Does impairment of the ubiquitin-proteasome system or the autophagy-lysosome pathway predispose individuals to neurodegenerative disorders such as Parkinson's disease? J Alzheimers Dis 2010; 19: 1-9.
8. Pan T, Kondo S, Le W, Jankovic J. The role of autophagy-lysosome pathway in neurodegeneration associated with Parkinson's disease. Brain 2008; 131: 1969-1978.
9. Ramirez A, Heimbach A, Grundemann J, Stiller B, Hampshire D, Cid LP et al. Hereditary parkinsonism with dementia is caused by mutations in ATP13A2, encoding a lysosomal type 5P-type ATPase. Nat Genet 2006; 38: 1184-1191.
10. Sidransky E, Lopez G. The link between the GBA gene and parkinsonism. Lancet Neurol 2012; 11: 986-998.
11. Vilarino-Guell C, Wider C, Ross OA, Dachsel JC, Kachergus JM, Lincoln SJ et al. VPS35 mutations in Parkinson disease. Am J Hum Genet 2011; 89: 162-167.
12. Zimprich A, Benet-Pages A, Struhal W, Graf E, Eck SH, Offman MN et al. A mutation in VPS35, encoding a subunit of the retromer complex, causes late-onset Parkinson disease. Am J Hum Genet 2011; 89: 168-175.
13. Schymick JC, Yang Y, Andersen PM, Vonsattel JP, Greenway M, Momeni P et al. Progranulin mutations and amyotrophic lateral sclerosis or amyotrophic lateral sclerosis-frontotemporal dementia phenotypes. J Neurol Neurosurg Psychiatry 2007; 78: 754-756.
14. Talbot K, Ansorge O. Recent advances in the genetics of amyotrophic lateral sclerosis and frontotemporal dementia: common pathways in neurodegenerative disease. Hum Mol Genet 2006; 2: R182-R187.
15. Skibinski G, Parkinson NJ, Brown JM, Chakrabarti L, Lloyd SL, Hummerich H et al. Mutations in the endosomal ESCRTIII-complex subunit CHMP2B in frontotemporal dementia. Nat Genet 2005; 37: 806-808.
16. Bahr BA, Bendiske J. The neuropathogenic contributions of lysosomal dysfunction. J Neurochem 2002; 83: 481-489.
17. Brettschneider J, Del Tredici K, Lee VM, Trojanowski JQ. Spreading of pathology in neurodegenerative diseases: a focus on human studies. Nat Rev Neurosci 2015; 16: 109-120.
18. Masuda-Suzukake M, Nonaka T, Hosokawa M, Kubo M, Shimozawa A, Akiyama H et al. Pathological alpha-synuclein propagates through neural networks. Acta Neuropathol Commun 2014; 2: 88.
19. Luk KC, Kehm V, Carroll J, Zhang B, O'Brien P, Trojanowski JQ et al. Pathological alphasynuclein transmission initiates Parkinson-like neurodegeneration in nontransgenic mice. Science 2012; 338: 949-953.
20. Luk KC, Kehm VM, Zhang B, O'Brien P, Trojanowski JQ, Lee VM. Intracerebral inoculation of pathological alpha-synuclein initiates a rapidly progressive neurodegenerative alphasynucleinopathy in mice. J Exp Med 2012; 209: 975-986.
21. Masuda-Suzukake M, Nonaka T, Hosokawa M, Oikawa T, Arai T, Akiyama H et al. Prion-like spreading of pathological alpha-synuclein in brain. Brain 2013; 136: 1128-1138.
22. Kane MD, Lipinski WJ, Callahan MJ, Bian F, Durham RA, Schwarz RD et al. Evidence for seeding of beta -amyloid by intracerebral infusion of Alzheimer brain extracts in beta -amyloid precursor protein-transgenic mice. J Neurosci 2000; 20: 3606-3611.
23. Meyer-Luehmann M, Coomaraswamy J, Bolmont T, Kaeser S, Schaefer C, Kilger E et al. Exogenous induction of cerebral beta-amyloidogenesis is governed by agent and host. Science 2006; 313: 1781-1784.
24. Rosen RF, Fritz JJ, Dooyema J, Cintron AF, Hamaguchi T, Lah JJ et al. Exogenous seeding of cerebral beta-amyloid deposition in betaAPP-transgenic rats. J Neurochem 2012; 120: 660-666.
25. Stohr J, Watts JC, Mensinger ZL, Oehler A, Grillo SK, DeArmond SJ et al. Purified and synthetic Alzheimer's amyloid beta (Abeta) prions. Proc Natl Acad Sci USA 2012; 109: 11025-11030.
26. Clavaguera F, Bolmont T, Crowther RA, Abramowski D, Frank S, Probst A et al. Transmission and spreading of tauopathy in transgenic mouse brain. Nat Cell Biol 2009;11: 909-913.
27. Iba M, Guo JL, McBride JD, Zhang B, Trojanowski JQ, Lee VM. Synthetic tau fibrils mediate transmission of neurofibrillary tangles in a transgenic mouse model of Alzheimer's-like tauopathy. J Neurosci 2013; 33: 1024-1037.
28. Peeraer E, Bottelbergs A, Van Kolen K, Stancu IC, Vasconcelos B, Mahieu M et al. Intracerebral injection of preformed synthetic tau fibrils initiates widespread tauopathy and neuronal loss in the brains of tau transgenic mice. Neurobiol Dis 2015; 73: 83-95.
29. Lee SJ, Desplats P, Sigurdson C, Tsigelny I, Masliah E. Cell-to-cell transmission of non-prion protein aggregates. Nat Rev Neurol 2010; 6: 702-706.
30. Guo JL, Lee VM. Cell-to-cell transmission of pathogenic proteins in neurodegenerative diseases. Nat Med 2014; 20: 130-138.
31. Lee HJ, Bae EJ, Lee SJ. Extracellular alpha-synuclein-a novel and crucial factor in Lewy body diseases. Nat Rev Neurol 2014; 10: 92-98.
32. Lee HJ, Suk JE, Bae EJ, Lee JH, Paik SR, Lee SJ. Assembly-dependent endocytosis and clearance of extracellular alpha-synuclein. Int J Biochem Cell Biol 2008; 40: 1835-1849.
33. Desplats P, Lee HJ, Bae EJ, Patrick C, Rockenstein E, Crews L et al. Inclusion formation and neuronal cell death through neuron-to-neuron transmission of alpha-synuclein. Proc Natl Acad Sci USA 2009; 106: 13010-13015.
34. Futerman AH, van Meer G. The cell biology of lysosomal storage disorders. Nat Rev Mol Cell Biol 2004; 5: 554-565.
35. Vitner EB, Platt FM, Futerman AH. Common and uncommon pathogenic cascades in lysosomal storage diseases. J Biol Chem 2010; 285: 20423-20427.
36. Platt FM, Boland B, van der Spoel AC. The cell biology of disease: lysosomal storage disorders: the cellular impact of lysosomal dysfunction. J Cell Biol 2012; 199: 723-734.
37. Brady RO, Kanfer J, Shapiro D. The metabolism of glucocerebrosides. I. Purification and properties of a glucocerebroside-cleaving enzyme from spleen tissue. J Biol Chem 1965; 240: 39-43.
38. Rosenbloom B, Balwani M, Bronstein JM, Kolodny E, Sathe S, Gwosdow AR et al. The incidence of Parkinsonism in patients with type 1 Gaucher disease: data from the ICGG Gaucher Registry. Blood Cells Mol Dis 2011; 46: 95-102.
39. Gegg ME, Burke D, Heales SJ, Cooper JM, Hardy J, Wood NW et al. Glucocerebrosidase deficiency in substantia nigra of parkinson disease brains. Ann Neurol 2012; 72: 455-463.
40. Yang NY, Lee YN, Lee HJ, Kim YS, Lee SJ. Glucocerebrosidase, a new player changing the old rules in Lewy body diseases. Biol Chem 2013; 394: 807-818.
41. Goker-Alpan O, Stubblefield BK, Giasson BI, Sidransky E. Glucocerebrosidase is present in alpha-synuclein inclusions in Lewy body disorders. Acta Neuropathol 2010; 120: 641-649.
42. Dean RT. Lysosomes and protein degradation. Ciba Found Symp 1979; 75: 139-149.
43. Siintola E, Partanen S, Stromme P, Haapanen A, Haltia M, Maehlen J et al. Cathepsin D deficiency underlies congenital human neuronal ceroid-lipofuscinosis. Brain 2006; 129: 1438-1445.
44. Steinfeld R, Reinhardt K, Schreiber K, Hillebrand M, Kraetzner R, Bruck W et al. Cathepsin D deficiency is associated with a human neurodegenerative disorder. Am J Hum Genet 2006; 78: 988-998.
45. Qiao L, Hamamichi S, Caldwell KA, Caldwell GA, Yacoubian TA, Wilson S et al. Lysosomal enzyme cathepsin D protects against alpha-synuclein aggregation and toxicity. Mol Brain 2008; 1: 17.
46. Cullen V, Lindfors M, Ng J, Paetau A, Swinton E, Kolodziej P et al. Cathepsin D expression level affects alpha-synuclein processing, aggregation, and toxicity in vivo. Mol Brain 2009; 2: 5.
47. Cuervo AM, Dice JF. When lysosomes get old. Exp Gerontol 2000; 35: 119-131.
48. Lee HJ, Patel S, Lee SJ. Intravesicular localization and exocytosis of alpha-synuclein and its aggregates. J Neurosci 2005; 25: 6016-6024.
49. Jang A, Lee HJ, Suk JE, Jung JW, Kim KP, Lee SJ. Non-classical exocytosis of alphasynuclein is sensitive to folding states and promoted under stress conditions. J Neurochem 2010; 113: 1263-1274.
50. Bae EJ, Yang NY, Song M, Lee CS, Lee JS, Jung BC et al. Glucocerebrosidase depletion enhances cell-to-cell transmission of alpha-synuclein. Nat Commun 2014; 5: 4755.
51. Emmanouilidou E, Melachroinou K, Roumeliotis T, Garbis SD, Ntzouni M, Margaritis LH et al. Cell-produced alpha-synuclein is secreted in a calcium-dependent manner by exosomes and impacts neuronal survival. J Neurosci 2010; 30: 6838-6851.
52. Ejlerskov P, Rasmussen I, Nielsen TT, Bergstrom AL, Tohyama Y, Jensen PH et al. Tubulin polymerization-promoting protein (TPPP/p25alpha) promotes unconventional secretion of alpha-synuclein through exophagy by impairing autophagosome-lysosome fusion. J Biol Chem 2013; 288: 17313-17335.
53. Stinchcombe J, Bossi G, Griffiths GM. Linking albinism and immunity: the secrets of secretory lysosomes. Science 2004; 305: 55-59.
54. Nalls MA, Duran R, Lopez G, Kurzawa-Akanbi M, McKeith IG, Chinnery PF et al. A multicenter study of glucocerebrosidase mutations in dementia with Lewy bodies. JAMA Neurol 2013; 70: 727-735.
55. Neufeld EF. Lysosomal storage diseases. Annu Rev Biochem 1991; 60: 257-280.
56. Ballabio A, Gieselmann V. Lysosomal disorders: from storage to cellular damage. Biochim Biophys Acta 2009; 1793: 684-696.
57. Crabtree D, Boyer-Guittaut M, Ouyang X, Fineberg N, Zhang J. Dopamine and its metabolites in cathepsin D heterozygous mice before and after MPTP administration. Neurosci Lett 2013; 538: 3-8.
58. Chu Y, Dodiya H, Aebischer P, Olanow CW, Kordower JH. Alterations in lysosomal and proteasomal markers in Parkinson's disease: relationship to alpha-synuclein inclusions. Neurobiol Dis 2009; 35: 385-398.
59. Kurzawa-Akanbi M, Hanson PS, Blain PG, Lett DJ, McKeith IG, Chinnery PF et al. Glucocerebrosidase mutations alter the endoplasmic reticulum and lysosomes in Lewy body disease. J Neurochem 2012; 123: 298-309.
60. Decressac M, Mattsson B, Weikop P, Lundblad M, Jakobsson J, Bjorklund A. TFEBmediated autophagy rescues midbrain dopamine neurons from alpha-synuclein toxicity. Proc Natl Acad Sci USA 2013; 110: E1817-E1826.
61. Lee HJ, Bae EJ, Jang A, Ho DH, Cho ED, Suk JE et al. Enzyme-linked immunosorbent assays for alpha-synuclein with species and multimeric state specificities. J Neurosci Methods 2011; 199: 249-257.