Transgenic overexpression of the alpha-synuclein interacting protein synphilin-1 leads to behavioral and neuropathological alterations in mice

Neurogenetics

Volumn 11, Issue 1, 2010, Pages 107-120

  Nuber, Silke ^a   Franck, Thomas ^a   Wolburg, Hartwig ^a   Schumann, Ulrike ^a   Casadei, Nicolas ^a   Fischer, Kristina ^a   Calaminus, Carsten ^a   Pichler, Bernd J ^a   Chanarat, Sittinan ^b   Teismann, Peter ^c   Schulz, Jörg B ^d   Luft, Andreas R ^e   Tomiuk, Jürgen ^a   Wilbertz, Johannes ^f   Bornemann, Antje ^a   Krüger, Rejko ^g   Riess, Olaf ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

^c UNIVERSITY OF ABERDEEN   (United Kingdom)

^d UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

^e UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^f STOCKHOLM UNIVERSITY   (Sweden)

^g UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Alpha synuclein; Alpha synucleinopathies; Dark cell degeneration; Mouse model; Neurotransmitter; Parkinson's disease; Purkinje cell; R621C; Synphilin 1

Indexed keywords

3,4 DIHYDROXYPHENYLACETIC ACID; 5 HYDROXYINDOLEACETIC ACID; ALPHA SYNUCLEIN; DOPAMINE; NEUROPEPTIDE; PRION PROTEIN; SEROTONIN; SYNPHILIN 1; UBIQUITIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR CHANGE; BRAIN REGION; CELL DEGENERATION; CONTROLLED STUDY; ELECTRON MICROSCOPY; GENE MUTATION; GENE OVEREXPRESSION; GENETIC VARIABILITY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; MOTOR DYSFUNCTION; MOUSE; NEUROTOXICITY; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PURKINJE CELL; TRANSGENIC MOUSE;

MUS; MUS MUSCULUS;

EID: 76549127330     PISSN: 13646745     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10048-009-0212-2     Document Type: Article

References (42)

1. C Schiesling N Kieper K Seidel R Krüger 2008 Familial Parkinson's disease-genetics, clinical phenotype and neuropathology in relation to the common sporadic form of the disease Neuropathol Appl Neurobiol 34 255 271 10.1111/j.1365-2990.2008.00952.x 1:CAS:528:DC%2BD1cXmvVShsLs%3D 18447897 (Pubitemid 351590874)
2. MG Spillantini ML Schmidt VM Lee JQ Trojanowski R Jakes M Goedert 1997 Alpha-synuclein in Lewy bodies Nature 388 839 840 10.1038/42166 1:CAS:528:DyaK2sXlslWru7o%3D 9278044 (Pubitemid 27377048)
3. E Masliah E Rockenstein I Veinbergs M Mallory M Hashimoto A Takeda Y Sagara A Sisk L Mucke 2000 Dopaminergic loss and inclusion body formation in alpha-synuclein mice: implications for neurodegenerative disorders Science 287 1265 1269 10.1126/science.287.5456.1265 1:CAS:528:DC%2BD3cXhtlOqsL4%3D 10678833 (Pubitemid 30112148)
4. PJ Kahle M Neumann L Ozmen V Muller H Jacobsen A Schindzielorz M Okochi U Leimer H van Der Putten A Probst E Kremmer HA Kretzschmar C Haass 2000 Subcellular localization of wild-type and Parkinson's disease-associated mutant alpha-synuclein in human and transgenic mouse brain J Neurosci 20 6365 6373 1:CAS:528:DC%2BD3cXmsVyhurs%3D 10964942
5. BI Giasson JE Duda SM Quinn B Zhang JQ Trojanowski VM Lee 2002 Neuronal alpha-synucleinopathy with severe movement disorder in mice expressing A53T human alpha-synuclein Neuron 34 521 533 10.1016/S0896-6273(02)00682-7 1:CAS:528:DC%2BD38XktFSmu74%3D 12062037 (Pubitemid 34628750)
6. MK Lee W Stirling Y Xu X Xu D Qui AS Mandir TM Dawson NG Copeland NA Jenkins DL Price 2002 Human alpha-synuclein-harboring familial Parkinson's disease-linked Ala-53→Thr mutation causes neurodegenerative disease with alpha-synuclein aggregation in transgenic mice Proc Natl Acad Sci U S A 99 8968 8973 10.1073/pnas.132197599 1:CAS:528:DC%2BD38XltF2htbk%3D 12084935 (Pubitemid 34693667)
7. E Rockenstein M Mallory M Hashimoto D Song CW Shults I Lang E Masliah 2002 Differential neuropathological alterations in transgenic mice expressing alpha-synuclein from the platelet-derived growth factor and Thy-1 promoters J Neurosci Res 68 568 578 10.1002/jnr.10231 1:CAS:528:DC%2BD38Xks1Kqu74%3D 12111846 (Pubitemid 34575622)
8. GK Tofaris P Garcia Reitbock T Humby SL Lambourne M O'Connell B Ghetti H Gossage PC Emson LS Wilkinson M Goedert MG Spillantini 2006 Pathological changes in dopaminergic nerve cells of the substantia nigra and olfactory bulb in mice transgenic for truncated human alpha-synuclein(1-120): implications for Lewy body disorders J Neurosci 26 3942 3950 10.1523/JNEUROSCI.4965-05.2006 1:CAS:528:DC%2BD28XktFantL8%3D 16611810 (Pubitemid 44315414)
9. S Nuber E Petrasch-Parwez B Winner J Winkler S von Hörsten T Schmidt J Boy M Kuhn HP Nguyen P Teismann JB Schulz M Neumann BJ Pichler G Reischl C Holzmann I Schmitt A Bornemann W Kuhn F Zimmermann A Servadio O Riess 2008 Neurodegeneration and motor dysfunction in a conditional model of Parkinson's disease J Neurosci 28 2471 2484 10.1523/JNEUROSCI.3040-07.2008 1:CAS:528:DC%2BD1cXjt1Ghu7s%3D 18322092 (Pubitemid 351348209)
10. PJ Kahle 2008 alpha-Synucleinopathy models and human neuropathology: similarities and differences Acta Neuropathol 115 87 95 10.1007/s00401-007-0302- x 1:CAS:528:DC%2BD2sXhtlOqtrnL 17932682 (Pubitemid 350238669)
11. MF Chesselet 2008 In vivo alpha-synuclein overexpression in rodents: a useful model of Parkinson's disease? Exp Neurol 209 22 27 10.1016/j.expneurol. 2007.08.006 1:CAS:528:DC%2BD1cXivFeitw%3D%3D 17949715
12. LJ Martin Y Pan AC Price W Sterling NG Copeland NA Jenkins DL Price MK Lee 2006 Parkinson's disease alpha-synuclein transgenic mice develop neuronal mitochondrial degeneration and cell death J Neurosci 26 41 50 10.1523/JNEUROSCI.4308-05.2006 1:CAS:528:DC%2BD28XmtV2gtw%3D%3D 16399671 (Pubitemid 43089519)
13. FP Marx C Holzmann KM Strauss L Li O Eberhardt E Gerhardt MR Cookson D Hernandez MJ Farrer J Kachergus S Engelender CA Ross K Berger L Schöls JB Schulz O Riess R Krüger 2003 Identification and functional characterization of a novel R621C mutation in the synphilin-1 gene in Parkinson's disease Hum Mol Genet 12 1223 1231 10.1093/hmg/ddg134 1:CAS:528:DC%2BD3sXkt1Wrurs%3D 12761037 (Pubitemid 36722602)
14. R Myhre H Klungland MJ Farrer JO Aasly 2008 Genetic association study of synphilin-1 in idiopathic Parkinson's disease BMC Med Genet 9 19 10.1186/1471-2350-9-19 18366718 (Pubitemid 351587047)
15. S Engelender Z Kaminsky X Guo AH Sharp RK Amaravi JJ Kleiderlein RL Margolis JC Troncoso AA Lanahan PF Worley VL Dawson TM Dawson CA Ross 1999 Synphilin-1 associates with alpha-synuclein and promotes the formation of cytosolic inclusions Nat Genet 22 110 114 10.1038/8820 1:CAS:528: DyaK1MXjtVagsLY%3D 10319874 (Pubitemid 29214817)
16. N Zaarur AB Meriin VL Gabai MY Sherman 2008 Triggering aggresome formation. Dissecting aggresome-targeting and aggregation signals in synphilin 1 J Biol Chem 283 27575 27584 10.1074/jbc.M802216200 1:CAS:528:DC%2BD1cXhtF2hsLjI 18635553
17. K Wakabayashi S Engelender M Yoshimoto S Tsuji CA Ross H Takahashi 2000 Synphilin-1 is present in Lewy bodies in Parkinson's disease Ann Neurol 47 521 523 10.1002/1531-8249(200004)47:4<521::AID-ANA18>3.0.CO;2-B 1:CAS:528:DC%2BD3cXivVyhtLo%3D 10762166 (Pubitemid 30194611)
18. KK Chung Y Zhang KL Lim Y Tanaka H Huang J Gao CA Ross VL Dawson TM Dawson 2001 Parkin ubiquitinates the alpha-synuclein-interacting protein, synphilin-1: implications for Lewy-body formation in Parkinson disease Nat Med 7 1144 1150 10.1038/nm1001-1144 1:CAS:528:DC%2BD3MXns12kurg%3D 11590439 (Pubitemid 33010024)
19. WW Smith Z Pei H Jiang VL Dawson TM Dawson CA Ross 2006 Kinase activity of mutant LRRK2 mediates neuronal toxicity Nat Neurosci 9 1231 1233 10.1038/nn1776 1:CAS:528:DC%2BD28XhtVSgu7fJ 16980962 (Pubitemid 44454261)
20. HG Jin H Yamashita T Nakamura H Fukuba T Takahashi M Hiji T Kohriyama M Matsumoto 2008 Synphilin-1 transgenic mice exhibit mild motor impairments Neurosci Lett 445 12 17 10.1016/j.neulet.2008.08.073 1:CAS:528: DC%2BD1cXhtFOgsL3L 18782602
21. U Bichelmeier T Schmidt J Hübener J Boy L Rüttiger K Häbig S Poths M Bonin M Knipper WJ Schmidt J Wilbertz H Wolburg F Laccone O Riess 2007 Nuclear localization of ataxin-3 is required for the manifestation of symptoms in SCA3: in vivo evidence J Neurosci 27 7418 7428 10.1523/JNEUROSCI. 4540-06.2007 1:CAS:528:DC%2BD2sXnvFyhur4%3D 17626202 (Pubitemid 47066563)
22. A Zhou JM Paranjape BA Hassel H Nie S Shah B Galinski RH Silverman 1998 mpact of RNase L overexpression on viral and cellular growth and death J Interferon Cytokine Res 18 953 961 1:CAS:528:DyaK1MXjtV2itg%3D%3D 9858317
23. H Braak E Braak T Ohm J Bohl 1988 Silver impregnation of Alzheimer's neurofibrillary changes counterstained for basophilic material and lipofuscin pigment Stain Technol 63 197 200 1:STN:280:DyaL1M7hsVOltg%3D%3D 2464205
24. GK Tofaris A Razzaq B Ghetti KS Lilley MG Spillantini 2003 Ubiquitination of alpha-synuclein in Lewy bodies is a pathological event not associated with impairment of proteasome function J Biol Chem 278 44405 44411 10.1074/jbc.M308041200 1:CAS:528:DC%2BD3sXoslWmur8%3D 12923179 (Pubitemid 37377190)
25. IJ Murray MA Medford HP Guan SM Rueter JQ Trojanowski VM Lee 2003 Synphilin in normal human brains and in synucleinopathies: studies with new antibodies Acta Neuropathol 105 177 184 1:CAS:528:DC%2BD3sXksVOhtw%3D%3D 12536229
26. A Eyal R Szargel E Avraham E Liani J Haskin R Rott S Engelender 2006 Synphilin-1A: an aggregation-prone isoform of synphilin-1 that causes neuronal death and is present in aggregates from alpha-synucleinopathy patients Proc Natl Acad Sci U S A 103 5917 5922 10.1073/pnas.0509707103 1:CAS:528: DC%2BD28XktFaitL0%3D 16595633
27. MM Buitrago JB Schulz J Dichgans AR Luft 2004 Short and long-term motor skill learning in an accelerated rotarod training paradigm Neurobiol Learn Mem 81 211 216 10.1016/j.nlm.2004.01.001 15082022 (Pubitemid 38479661)
28. H van der Putten KH Wiederhold A Probst S Barbieri C Mistl S Danner S Kauffmann K Hofele WP Spooren MA Ruegg S Lin P Caroni B Sommer M Tolnay G Bilbe 2000 Neuropathology in mice expressing human alpha-synuclein J Neurosci 20 6021 6029 10934251
29. C Freichel M Neumann T Ballard V Müller M Woolley L Ozmen E Borroni HA Kretzschmar C Haass W Spooren PJ Kahle 2007 Age-dependent cognitive decline and amygdala pathology in alpha-synuclein transgenic mice Neurobiol Aging 28 1421 1435 10.1016/j.neurobiolaging.2006.06.013 1:CAS:528:DC%2BD2sXotlahsLo%3D 16872721 (Pubitemid 47081234)
30. CS Ribeiro K Carneiro CA Ross JR Menezes S Engelender 2002 Synphilin-1 is developmentally localized to synaptic terminals, and its association with synaptic vesicles is modulated by alpha-synuclein J Biol Chem 277 34651 34654 10.1074/jbc.M201115200 1:CAS:528:DC%2BD38XnsVKgtbY%3D (Pubitemid 34952237)
31. M Neumann V Muller K Gorner HA Kretzschmar C Haass PJ Kahle 2004 Pathological properties of the Parkinson's disease-associated protein DJ-1 in alpha-synucleinopathies and tauopathies: relevance for multiple system atrophy and Pick's disease Acta Neuropathol (Berl) 107 489 496 10.1007/s00401-004-0834-2 1:CAS:528:DC%2BD2cXjvVKhtbs%3D (Pubitemid 38765389)
32. S Gispert D Del Turco L Garrett A Chen DJ Bernard J Hamm-Clement HW Korf T Deller H Braak G Auburger RL Nussbaum 2003 Transgenic mice expressing mutant A53T human alpha-synuclein show neuronal dysfunction in the absence of aggregate formation Mol Cell Neurosci 24 419 429 10.1016/S1044-7431(03)00198-2 1:CAS:528:DC%2BD3sXot1Grs7s%3D 14572463 (Pubitemid 37311305)
33. A Krenz BH Falkenburger E Gerhardt A Drinkut JB Schulz 2009 Aggregate formation and toxicity by wild-type and R621C synphilin-1 in the nigrostriatal system of mice using adenoviral vectors J Neurochem 108 139 146 10.1111/j.1471-4159.2008.05755.x 1:CAS:528:DC%2BD1MXns1Wqsg%3D%3D 19094062
34. M Turmaine A Raza A Mahal L Mangiarini GP Bates SW Davies 2000 Nonapoptotic neurodegeneration in a transgenic mouse model of Huntington's disease Proc Natl Acad Sci U S A 97 8093 8097 10.1073/pnas.110078997 1:CAS:528:DC%2BD3cXkvFCms7g%3D 10869421 (Pubitemid 30460778)
35. E Petrasch-Parwez HP Nguyen M Löbbecke-Schumacher HW Habbes S Wieczorek O Riess KH Andres R Dermietzel S von Hörsten 2007 Cellular and subcellular localization of Huntingtin aggregates in the brain of a rat transgenic for Huntington disease J Comp Neurol 501 716 730 10.1002/cne.21272 17299753 (Pubitemid 46319009)
36. SK Custer GA Garden N Gill U Rueb RT Libby C Schultz SJ Guyenet T Deller LE Westrum BL Sopher AR La Spada 2006 Bergmann glia expression of polyglutamine-expanded ataxin-7 produces neurodegeneration by impairing glutamate transport Nat Neurosci 9 1302 1311 10.1038/nn1750 1:CAS:528: DC%2BD28XhtVSgu7nE 16936724 (Pubitemid 44454272)
37. R Lalonde C Strazielle 2006 Spontaneous and induced mouse mutations with cerebellar dysfunctions: behavior and neurochemistry Brain Res 1140 51 74 10.1016/j.brainres.2006.01.031 16499884
38. O Hikosaka K Nakamura K Sakai H Nakahara 2002 Central mechanisms of motor skill learning Curr Opin Neurobiol 12 217 222 10.1016/S0959-4388(02)00307-0 1:CAS:528:DC%2BD38XjsFWhtLk%3D 12015240 (Pubitemid 34518343)
39. SL Senior N Ninkina R Deacon D Bannerman VL Buchman SJ Cragg R Wade-Martins 2008 Increased striatal dopamine release and hyperdopaminergic-like behaviour in mice lacking both alpha-synuclein and gamma-synuclein Eur J Neurosci 27 947 957 10.1111/j.1460-9568.2008.06055.x 18333965
40. JS Rakshi T Uema K Ito DL Bailey PK Morrish J Ashburner A Dagher IH Jenkins KJ Friston DJ Brooks 1999 Frontal, midbrain and striatal dopaminergic function in early and advanced Parkinson's disease A 3D [(18)F]dopa-PET study Brain 122 1637 1650 10.1093/brain/122.9.1637 10468504 (Pubitemid 29425668)
41. J Lotharius P Brundin 2002 Impaired dopamine storage resulting from alpha-synuclein mutations may contribute to the pathogenesis of Parkinson's disease Hum Mol Genet 11 2395 2407 10.1093/hmg/11.20.2395 1:CAS:528: DC%2BD38XnvVems7s%3D 12351575
42. Paxinos G, Franklin KB (2001) The mouse brain in stereotaxic coordinates, 2nd edn. Academic, San Diego