Lysosomal dysfunction disrupts presynaptic maintenance and restoration of presynaptic function prevents neurodegeneration in lysosomal storage diseases

EMBO Molecular Medicine

Volumn 9, Issue 1, 2017, Pages 112-132

  Sambri, Irene ^a   D'Alessio, Rosa ^a   Ezhova, Yulia ^a   Giuliano, Teresa ^a   Sorrentino, Nicolina Cristina ^a   Cacace, Vincenzo ^a   De Risi, Maria ^a,b   Cataldi, Mauro ^c   Annunziato, Lucio ^c   De Leonibus, Elvira ^a,b   Fraldi, Alessandro ^a  

^a TELETHON INSTITUTE OF GENETICS AND MEDICINE TIGEM   (Italy)

^b INSTITUTE OF GENETICS AND BIOPHYSICS ADRIANO BUZZATI TRAVERSO   (Italy)

^c UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

CSP ; lysosomal storage disorders; lysosomes; neurodegeneration; synuclein

Indexed keywords

ALPHA SYNUCLEIN; CYSTEINE STRING PROTEIN; CYSTEINE STRING PROTEIN ALPHA; PROTEASOME; SNARE PROTEIN; UNCLASSIFIED DRUG; HEAT SHOCK PROTEIN 40; MEMBRANE PROTEIN;

ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN; COMPLEX FORMATION; CONTROLLED STUDY; DISEASE SEVERITY; FEMALE; GENE OVEREXPRESSION; LYSOSOME; LYSOSOME STORAGE DISEASE; MALE; MOUSE; MUCOPOLYSACCHARIDOSIS; MUCOPOLYSACCHARIDOSIS TYPE 3A; NERVE DEGENERATION; NERVE ENDING; NEWBORN; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DEGRADATION; SYNAPSE VESICLE; ANIMAL; DEGENERATIVE DISEASE; DISEASE MODEL; METABOLISM; PATHOLOGY;

ALPHA-SYNUCLEIN; ANIMALS; DISEASE MODELS, ANIMAL; HSP40 HEAT-SHOCK PROTEINS; LYSOSOMAL STORAGE DISEASES; MEMBRANE PROTEINS; MICE; NEURODEGENERATIVE DISEASES; PRESYNAPTIC TERMINALS; PROTEOLYSIS; SNARE PROTEINS; SYNAPTIC VESICLES;

EID: 85005943353     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.15252/emmm.201606965     Document Type: Article

References (48)

1. Bhattacharyya R, Gliddon B, Beccari T, Hopwood JJ, Stanley P (2001) A novel missense mutation in lysosomal sulfamidase is the basis of MPS III A in a spontaneous mouse mutant. Glycobiology 11: 99–103
2. Bhaumik M, Muller VJ, Rozaklis T, Johnson L, Dobrenis K, Bhattacharyya R, Wurzelmann S, Finamore P, Hopwood JJ, Walkley SU et al (1999) A mouse model for mucopolysaccharidosis type III A (Sanfilippo syndrome). Glycobiology 9: 1389–1396
3. Boustany RM (2013) Lysosomal storage diseases–the horizon expands. Nat Rev Neurol 9: 583–598
4. Burgoyne RD, Morgan A (2011) Chaperoning the SNAREs: a role in preventing neurodegeneration? Nat Cell Biol 13: 8–9
5. Burre J, Sharma M, Tsetsenis T, Buchman V, Etherton MR, Sudhof TC (2010) Alpha-synuclein promotes SNARE-complex assembly in vivo and in vitro. Science 329: 1663–1667
6. Burrone J, Li Z, Murthy VN (2006) Studying vesicle cycling in presynaptic terminals using the genetically encoded probe synaptopHluorin. Nat Protoc 1: 2970–2978
7. Chandra S, Fornai F, Kwon HB, Yazdani U, Atasoy D, Liu X, Hammer RE, Battaglia G, German DC, Castillo PE et al (2004) Double-knockout mice for alpha- and beta-synucleins: effect on synaptic functions. Proc Natl Acad Sci USA 101: 14966–14971
8. Chandra S, Gallardo G, Fernandez-Chacon R, Schluter OM, Sudhof TC (2005) Alpha-synuclein cooperates with CSPalpha in preventing neurodegeneration. Cell 123: 383–396
9. Evers M, Saftig P, Schmidt P, Hafner A, McLoghlin DB, Schmahl W, Hess B, von Figura K, Peters C (1996) Targeted disruption of the arylsulfatase B gene results in mice resembling the phenotype of mucopolysaccharidosis VI. Proc Natl Acad Sci USA 93: 8214–8219
10. Fernandez-Alfonso T, Ryan TA (2006) The efficiency of the synaptic vesicle cycle at central nervous system synapses. Trends Cell Biol 16: 413–420
11. Fernandez-Chacon R, Wolfel M, Nishimune H, Tabares L, Schmitz F, Castellano-Munoz M, Rosenmund C, Montesinos ML, Sanes JR, Schneggenburger R et al (2004) The synaptic vesicle protein CSP alpha prevents presynaptic degeneration. Neuron 42: 237–251
12. Fraldi A, Hemsley K, Crawley A, Lombardi A, Lau A, Sutherland L, Auricchio A, Ballabio A, Hopwood JJ (2007) Functional correction of CNS lesions in an MPS-IIIA mouse model by intracerebral AAV-mediated delivery of sulfamidase and SUMF1 genes. Hum Mol Genet 16: 2693–2702
13. Fraldi A, Klein AD, Medina DL, Settembre C (2016) Brain disorders due to lysosomal dysfunction. Annu Rev Neurosci 39: 277–295
14. Gaffield MA, Betz WJ (2006) Imaging synaptic vesicle exocytosis and endocytosis with FM dyes. Nat Protoc 1: 2916–2921
15. Greaves J, Salaun C, Fukata Y, Fukata M, Chamberlain LH (2008) Palmitoylation and membrane interactions of the neuroprotective chaperone cysteine-string protein. J Biol Chem 283: 25014–25026
16. Greten-Harrison B, Polydoro M, Morimoto-Tomita M, Diao L, Williams AM, Nie EH, Makani S, Tian N, Castillo PE, Buchman VL et al (2010) Alphabetagamma-Synuclein triple knockout mice reveal age-dependent neuronal dysfunction. Proc Natl Acad Sci USA 107: 19573–19578
17. Hampton DW, Webber DJ, Bilican B, Goedert M, Spillantini MG, Chandran S (2010) Cell-mediated neuroprotection in a mouse model of human tauopathy. J Neurosci 30: 9973–9983
18. Hemsley KM, Hopwood JJ (2005) Development of motor deficits in a murine model of mucopolysaccharidosis type IIIA (MPS-IIIA). Behav Brain Res 158: 191–199
19. Kaech S, Banker G (2006) Culturing hippocampal neurons. Nat Protoc 1: 2406–2415
20. Kramer ML, Schulz-Schaeffer WJ (2007) Presynaptic alpha-synuclein aggregates, not Lewy bodies, cause neurodegeneration in dementia with Lewy bodies. J Neurosci 27: 1405–1410
21. Lau AA, Crawley AC, Hopwood JJ, Hemsley KM (2008) Open field locomotor activity and anxiety-related behaviors in mucopolysaccharidosis type IIIA mice. Behav Brain Res 191: 130–136
22. Lee HJ, Khoshaghideh F, Patel S, Lee SJ (2004) Clearance of alpha-synuclein oligomeric intermediates via the lysosomal degradation pathway. J Neurosci 24: 1888–1896
23. Lundblad M, Decressac M, Mattsson B, Bjorklund A (2012) Impaired neurotransmission caused by overexpression of alpha-synuclein in nigral dopamine neurons. Proc Natl Acad Sci USA 109: 3213–3219
24. Mak SK, McCormack AL, Manning-Bog AB, Cuervo AM, Di Monte DA (2010) Lysosomal degradation of alpha-synuclein in vivo. J Biol Chem 285: 13621–13629
25. Murthy VN, De Camilli P (2003) Cell biology of the presynaptic terminal. Annu Rev Neurosci 26: 701–728
26. Nemani VM, Lu W, Berge V, Nakamura K, Onoa B, Lee MK, Chaudhry FA, Nicoll RA, Edwards RH (2010) Increased expression of alpha-synuclein reduces neurotransmitter release by inhibiting synaptic vesicle reclustering after endocytosis. Neuron 65: 66–79
27. Nixon RA, Yang DS, Lee JH (2008) Neurodegenerative lysosomal disorders: a continuum from development to late age. Autophagy 4: 590–599
28. Nixon RA (2013) The role of autophagy in neurodegenerative disease. Nat Med 19: 983–997
29. Noskova L, Stranecky V, Hartmannova H, Pristoupilova A, Baresova V, Ivanek R, Hulkova H, Jahnova H, van der Zee J, Staropoli JF et al (2011) Mutations in DNAJC5, encoding cysteine-string protein alpha, cause autosomal-dominant adult-onset neuronal ceroid lipofuscinosis. Am J Hum Genet 89: 241–252
30. Platt FM, Boland B, van der Spoel AC (2012) The cell biology of disease: lysosomal storage disorders: the cellular impact of lysosomal dysfunction. J Cell Biol 199: 723–734
31. Prescott GR, Gorleku OA, Greaves J, Chamberlain LH (2009) Palmitoylation of the synaptic vesicle fusion machinery. J Neurochem 110: 1135–1149
32. Roy S (2009) The paradoxical cell biology of alpha-Synucle. Results Probl Cell Differ 48: 159–172
33. Sarkar S, Carroll B, Buganim Y, Maetzel D, Ng AH, Cassady JP, Cohen MA, Chakraborty S, Wang H, Spooner E et al (2013) Impaired autophagy in the lipid-storage disorder Niemann-Pick type C1 disease. Cell Rep 5: 1302–1315
34. Scheff SW, Price DA, Schmitt FA, DeKosky ST, Mufson EJ (2007) Synaptic alterations in CA1 in mild Alzheimer disease and mild cognitive impairment. Neurology 68: 1501–1508
35. Schultz ML, Tecedor L, Chang M, Davidson BL (2011) Clarifying lysosomal storage diseases. Trends Neurosci 34: 401–410
36. Settembre C, Annunziata I, Spampanato C, Zarcone D, Cobellis G, Nusco E, Zito E, Tacchetti C, Cosma MP, Ballabio A (2007) Systemic inflammation and neurodegeneration in a mouse model of multiple sulfatase deficiency. Proc Natl Acad Sci USA 104: 4506–4511
37. Settembre C, Fraldi A, Jahreiss L, Spampanato C, Venturi C, Medina D, de Pablo R, Tacchetti C, Rubinsztein DC, Ballabio A (2008) A block of autophagy in lysosomal storage disorders. Hum Mol Genet 17: 119–129
38. Settembre C, Fraldi A, Medina DL, Ballabio A (2013) Signals from the lysosome: a control centre for cellular clearance and energy metabolism. Nat Rev Mol Cell Biol 14: 283–296
39. Sharma M, Burre J, Sudhof TC (2011) CSPalpha promotes SNARE-complex assembly by chaperoning SNAP-25 during synaptic activity. Nat Cell Biol 13: 30–39
40. Sharma M, Burre J, Bronk P, Zhang Y, Xu W, Sudhof TC (2012a) CSPalpha knockout causes neurodegeneration by impairing SNAP-25 function. EMBO J 31: 829–841
41. Sharma M, Burre J, Sudhof TC (2012b) Proteasome inhibition alleviates SNARE-dependent neurodegeneration. Sci Transl Med 4: 147ra113
42. Sorrentino NC, D'Orsi L, Sambri I, Nusco E, Monaco C, Spampanato C, Polishchuk E, Saccone P, De Leonibus E, Ballabio A et al (2013) A highly secreted sulphamidase engineered to cross the blood-brain barrier corrects brain lesions of mice with mucopolysaccharidoses type IIIA. EMBO Mol Med 5: 675–690
43. Spillantini MG, Schmidt ML, Lee VM, Trojanowski JQ, Jakes R, Goedert M (1997) Alpha-synuclein in Lewy bodies. Nature 388: 839–840
44. Sudhof TC, Rothman JE (2009) Membrane fusion: grappling with SNARE and SM proteins. Science 323: 474–477
45. Suzuki K (2002) Lysosomal disease. In Greenfield's neuropathology, Graham DI, Lantos PL (eds), pp 653–735. London: Arnold
46. Tessitore A, Pirozzi M, Auricchio A (2009) Abnormal autophagy, ubiquitination, inflammation and apoptosis are dependent upon lysosomal storage and are useful biomarkers of mucopolysaccharidosis VI. Pathogenetics 2: 4
47. Valstar MJ, Neijs S, Bruggenwirth HT, Olmer R, Ruijter GJ, Wevers RA, van Diggelen OP, Poorthuis BJ, Halley DJ, Wijburg FA (2010) Mucopolysaccharidosis type IIIA: clinical spectrum and genotype-phenotype correlations. Ann Neurol 68: 876–887
48. Washbourne P, Thompson PM, Carta M, Costa ET, Mathews JR, Lopez-Bendito G, Molnar Z, Becher MW, Valenzuela CF, Partridge LD et al (2002) Genetic ablation of the t-SNARE SNAP-25 distinguishes mechanisms of neuroexocytosis. Nat Neurosci 5: 19–26