Knockdown of Hsc70-5/mortalin induces loss of synaptic mitochondria in a Drosophila Parkinson's disease model

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Zhu, Jun Yi ^a,b   Vereshchagina, Natalia ^a   Sreekumar, Vrinda ^a,b,c   Burbulla, Lena F ^a,c   Costa, Ana C ^d   Daub, Katharina J ^a   Woitalla, Dirk ^e   Martins, L Miguel ^d   Krüger, Rejko ^a,b,c   Rasse, Tobias M ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^d MRC TOXICOLOGY UNIT   (United Kingdom)

^e ST JOSEF HOSPITAL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; AUTOPHAGY; CELL SURVIVAL; DISEASE MODELS, ANIMAL; DOPAMINERGIC NEURONS; DROSOPHILA; FEMALE; GENE KNOCKDOWN TECHNIQUES; GENE SILENCING; GENES, ESSENTIAL; HSP70 HEAT-SHOCK PROTEINS; HUMANS; MITOCHONDRIA; NEURONS; PARKINSON DISEASE; PHENOTYPE; SYNAPSES;

EID: 84893529812     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0083714     Document Type: Article

References (55)

1. Dauer W, Przedborski S (2003) Parkinson's disease: mechanisms and models. Neuron 39: 889-909. (Pubitemid 37130207)
2. Farrer MJ (2006) Genetics of Parkinson disease: paradigm shifts and future prospects. Nat Rev Genet 7: 306-318.
3. Coelho M, Ferreira JJ (2012) Late-stage Parkinson disease. Nat Rev Neurol 8: 435-442.
4. Orsucci D, Caldarazzo Ienco E, Mancuso M, Siciliano G (2011) POLG1-related and other "mitochondrial Parkinsonisms": an overview. J Mol Neurosci 44: 17-24.
5. Rochet JC, Hay BA, Guo M (2012) Molecular insights into Parkinson's disease. Prog Mol Biol Transl Sci 107: 125-188.
6. Burbulla LF, Krebiehl G, Kruger R (2010) Balance is the challenge-the impact of mitochondrial dynamics in Parkinson's disease. Eur J Clin Invest 40: 1048-1060.
7. Deocaris CC, Kaul SC, Wadhwa R (2009) The versatile stress protein mortalin as a chaperone therapeutic agent. Protein Pept Lett 16: 517-529.
8. Deocaris CC, Kaul SC, Wadhwa R (2008) From proliferative to neurological role of an hsp70 stress chaperone, mortalin. Biogerontology 9: 391-403.
9. Craig EA, Kramer J, Kosic-Smithers J (1987) SSC1, a member of the 70-kDa heat shock protein multigene family of Saccharomyces cerevisiae, is essential for growth. Proc Natl Acad Sci U S A 84: 4156-4160. (Pubitemid 17090894)
10. Wadhwa R, Takano S, Taira K, Kaul SC (2004) Reduction in mortalin level by its antisense expression causes senescence-like growth arrest in human immortalized cells. J Gene Med 6: 439-444. (Pubitemid 40228060)
11. Yokoyama K, Fukumoto K, Murakami T, Harada S, Hosono R, et al. (2002) Extended longevity of Caenorhabditis elegans by knocking in extra copies of hsp70F, a homolog of mot-2 (mortalin)/mthsp70/Grp75. FEBS Lett 516: 53-57. (Pubitemid 34311932)
12. Kaul SC, Yaguchi T, Taira K, Reddel RR, Wadhwa R (2003) Overexpressed mortalin (mot-2)/mthsp70/GRP75 and hTERT cooperate to extend the in vitro lifespan of human fibroblasts. Exp Cell Res 286: 96-101. (Pubitemid 36506862)
13. Shi M, Jin J, Wang Y, Beyer RP, Kitsou E, et al. (2008) Mortalin: a protein associated with progression of Parkinson disease? J Neuropathol Exp Neurol 67: 117-124.
14. Chiasserini D, Tozzi A, de Iure A, Tantucci M, Susta F, et al. (2011) Mortalin inhibition in experimental Parkinson's disease. Mov Disord 26: 1639-1647.
15. De Mena L, Coto E, Sanchez-Ferrero E, Ribacoba R, Guisasola LM, et al. (2009) Mutational screening of the mortalin gene (HSPA9) in Parkinson's disease. J Neural Transm 116: 1289-1293.
16. Burbulla LF, Schelling C, Kato H, Rapaport D, Woitalla D, et al. (2010) Dissecting the role of the mitochondrial chaperone mortalin in Parkinson's disease: functional impact of disease-related variants on mitochondrial homeostasis. Hum Mol Genet 19: 4437-4452.
17. Yang H, Zhou X, Liu X, Yang L, Chen Q, et al. (2011) Mitochondrial dysfunction induced by knockdown of mortalin is rescued by Parkin. Biochem Biophys Res Commun 410: 114-120.
18. Menzies FM, Yenisetti SC, Min KT (2005) Roles of Drosophila DJ-1 in survival of dopaminergic neurons and oxidative stress. Curr Biol 15: 1578-1582. (Pubitemid 41219598)
19. Park J, Kim SY, Cha GH, Lee SB, Kim S, et al. (2005) Drosophila DJ-1 mutants show oxidative stress-sensitive locomotive dysfunction. Gene 361: 133-139. (Pubitemid 41506941)
20. Clark IE, Dodson MW, Jiang C, Cao JH, Huh JR, et al. (2006) Drosophila pink1 is required for mitochondrial function and interacts genetically with parkin. Nature 441: 1162-1166. (Pubitemid 43990738)
21. Park J, Lee SB, Lee S, Kim Y, Song S, et al. (2006) Mitochondrial dysfunction in Drosophila PINK1 mutants is complemented by parkin. Nature 441: 1157-1161. (Pubitemid 43990737)
22. Poole AC, Thomas RE, Andrews LA, McBride HM, Whitworth AJ, et al. (2008) The PINK1/Parkin pathway regulates mitochondrial morphology. Proc Natl Acad Sci U S A 105: 1638-1643. (Pubitemid 351346567)
23. Greene JC, Whitworth AJ, Kuo I, Andrews LA, Feany MB, et al. (2003) Mitochondrial pathology and apoptotic muscle degeneration in Drosophila parkin mutants. Proc Natl Acad Sci U S A 100: 4078-4083. (Pubitemid 36418160)
24. Pimenta de Castro I, Costa AC, Lam D, Tufi R, Fedele V, et al. (2012) Genetic analysis of mitochondrial protein misfolding in Drosophila melanogaster. Cell Death Differ 19: 1308-1316.
25. Dietzl G, Chen D, Schnorrer F, Su KC, Barinova Y, et al. (2007) A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448: 151-156. (Pubitemid 47067374)
26. Rasse TM, Fouquet W, Schmid A, Kittel RJ, Mertel S, et al. (2005) Glutamate receptor dynamics organizing synapse formation in vivo. Nat Neurosci 8: 898-905.
27. Schmid A, Sigrist SJ (2008) Analysis of neuromuscular junctions: histology and in vivo imaging. Methods Mol Biol 420: 239-251.
28. Kern JV, Zhang YV, Kramer S, Brenman JE, Rasse TM (2013) The Kinesin-3, Unc-104 Regulates Dendrite Morphogenesis and Synaptic Development in Drosophila. Genetics.
29. Fuger P, Behrends LB, Mertel S, Sigrist SJ, Rasse TM (2007) Live imaging of synapse development and measuring protein dynamics using two-color fluorescence recovery after photo-bleaching at Drosophila synapses. Nat Protoc 2: 3285-3298.
30. Kohler K, Brunner E, Guan XL, Boucke K, Greber UF, et al. (2009) A combined proteomic and genetic analysis identifies a role for the lipid desaturase Desat1 in starvation-induced autophagy in Drosophila. Autophagy 5: 980-990.
31. Godena VK, Romano G, Romano M, Appocher C, Klima R, et al. (2011) TDP-43 regulates Drosophila neuromuscular junctions growth by modulating Futsch/MAP1B levels and synaptic microtubules organization. PLoS ONE 6: e17808.
32. Fuger P, Sreekumar V, Schule R, Kern JV, Stanchev DT, et al. (2012) Spastic paraplegia mutation N256S in the neuronal microtubule motor KIF5A disrupts axonal transport in a Drosophila HSP model. PLoS Genet 8: e1003066.
33. Daigle JG, Lanson NA Jr, Smith RB, Casci I, Maltare A, et al. (2013) RNA-binding ability of FUS regulates neurodegeneration, cytoplasmic mislocalization and incorporation into stress granules associated with FUS carrying ALS-linked mutations. Hum Mol Genet 22: 1193-1205.
34. Yaguchi T, Aida S, Kaul SC, Wadhwa R (2007) Involvement of mortalin in cellular senescence from the perspective of its mitochondrial import, chaperone, and oxidative stress management functions. Ann N Y Acad Sci 1100: 306-311. (Pubitemid 47092666)
35. Perry RJ, Hodges JR (1996) Spectrum of memory dysfunction in degenerative disease. Curr Opin Neurol 9: 281-285. (Pubitemid 26273287)
36. Moreno E (2012) Design and Construction of "Synthetic Species". PLoS ONE 7: e39054.
37. Schnorrer F, Schonbauer C, Langer CC, Dietzl G, Novatchkova M, et al. (2010) Systematic genetic analysis of muscle morphogenesis and function in Drosophila. Nature 464: 287-291.
38. Chen J, Shi X, Padmanabhan R, Wang Q, Wu Z, et al. (2008) Identification of novel modulators of mitochondrial function by a genome-wide RNAi screen in Drosophila melanogaster. Genome Res 18: 123-136.
39. Yang Y, Gehrke S, Imai Y, Huang Z, Ouyang Y, et al. (2006) Mitochondrial pathology and muscle and dopaminergic neuron degeneration caused by inactivation of Drosophila Pink1 is rescued by Parkin. Proc Natl Acad Sci U S A 103: 10793-10798. (Pubitemid 44078055)
40. Vincent A, Briggs L, Chatwin GF, Emery E, Tomlins R, et al. (2012) parkin-induced defects in neurophysiology and locomotion are generated by metabolic dysfunction and not oxidative stress. Hum Mol Genet 21: 1760-1769.
41. Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, et al. (2012) Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 8: 445-544.
42. Rakovic A, Grunewald A, Voges L, Hofmann S, Orolicki S, et al. (2011) PINK1-Interacting Proteins: Proteomic Analysis of Overexpressed PINK1. Parkinsons Dis 2011: 153979.
43. Jin J, Li GJ, Davis J, Zhu D, Wang Y, et al. (2007) Identification of novel proteins associated with both alpha-synuclein and DJ-1. Mol Cell Proteomics 6: 845-859. (Pubitemid 46831936)
44. Davison EJ, Pennington K, Hung CC, Peng J, Rafiq R, et al. (2009) Proteomic analysis of increased Parkin expression and its interactants provides evidence for a role in modulation of mitochondrial function. Proteomics 9: 4284-4297.
45. Schneider HC, Berthold J, Bauer MF, Dietmeier K, Guiard B, et al. (1994) Mitochondrial Hsp70/MIM44 complex facilitates protein import. Nature 371: 768-774. (Pubitemid 24333863)
46. Skladal D, Halliday J, Thorburn DR (2003) Minimum birth prevalence of mitochondrial respiratory chain disorders in children. Brain 126: 1905-1912. (Pubitemid 36917349)
47. Vafai SB, Mootha VK (2012) Mitochondrial disorders as windows into an ancient organelle. Nature 491: 374-383.
48. Balaban RS, Kantor HL, Katz LA, Briggs RW (1986) Relation between work and phosphate metabolite in the in vivo paced mammalian heart. Science 232: 1121-1123. (Pubitemid 16050798)
49. Pagliarini DJ, Calvo SE, Chang B, Sheth SA, Vafai SB, et al. (2008) A mitochondrial protein compendium elucidates complex I disease biology. Cell 134: 112-123. (Pubitemid 351916708)
50. Kopin IJ (1992) Features of the dopaminergic neurotoxin MPTP. Ann N Y Acad Sci 648: 96-104.
51. Sadun A (1998) Acquired mitochondrial impairment as a cause of optic nerve disease. Trans Am Ophthalmol Soc 96: 881-923.
52. Kirkman MA, Yu-Wai-Man P, Korsten A, Leonhardt M, Dimitriadis K, et al. (2009) Gene-environment interactions in Leber hereditary optic neuropathy. Brain 132: 2317-2326.
53. Burman JL, Yu S, Poole AC, Decal RB, Pallanck L (2012) Analysis of neural subtypes reveals selective mitochondrial dysfunction in dopaminergic neurons from parkin mutants. Proc Natl Acad Sci U S A 109: 10438-10443.
54. Barzilai A, Melamed E (2003) Molecular mechanisms of selective dopaminergic neuronal death in Parkinson's disease. Trends Mol Med 9: 126-132. (Pubitemid 36433894)
55. Bolam JP, Pissadaki EK (2012) Living on the edge with too many mouths to feed: why dopamine neurons die. Mov Disord 27: 1478-1483.