Genetic correction of a lrrk2 mutation in human iPSCs links parkinsonian neurodegeneration to ERK-dependent changes in gene expression

Cell Stem Cell

Volumn 12, Issue 3, 2013, Pages 354-367

  Reinhardt, Peter ^a   Schmid, Benjamin ^b   Burbulla, Lena F ^b   Schöndorf, David C ^b,c   Wagner, Lydia ^a   Glatza, Michael ^a   Höing, Susanne ^a   Hargus, Gunnar ^a,c   Heck, Susanna A ^b   Dhingra, Ashutosh ^b,d   Wu, Guangming ^a   Müller, Stephan ^b   Brockmann, Kathrin ^b   Kluba, Torsten ^d   Maisel, Martina ^b   Krüger, Rejko ^b   Berg, Daniela ^b   Tsytsyura, Yaroslav ^e   Thiel, Cora S ^e   Psathaki, Olympia Ekaterini ^a   Klingauf, Jürgen ^e   Kuhlmann, Tanja ^c   Klewin, Marlene ^f   Müller, Heiko ^f   Gasser, Thomas ^b   Schöler, Hans R ^a,e   Sterneckert, Jared ^a   more..

^a MAX PLANCK INSTITUTE FOR MOLECULAR BIOMEDICINE   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^d UNIVERSITY OF TÜBINGEN   (Germany)

^e UNIVERSITY OF MÜNSTER   (Germany)

^f Lead Discovery Center GmbH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

LEUCINE RICH REPEAT KINASE 2; MITOGEN ACTIVATED PROTEIN KINASE 1;

ARTICLE; CASE REPORT; CELL DIFFERENTIATION; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; GENE MUTATION; GENE SILENCING; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; HUMAN TISSUE; NERVE DEGENERATION; OUTCOME ASSESSMENT; PARKINSON DISEASE; PATHOGENESIS; PHOSPHORYLATION; PLURIPOTENT STEM CELL; POSTTRANSCRIPTIONAL GENE SILENCING; PRIORITY JOURNAL; PROTEINASE INHIBITION; TARGETED GENE REPAIR;

BENZAMIDES; CELL DIFFERENTIATION; CELLS, CULTURED; DIPHENYLAMINE; DOPAMINE; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MUTATION; NEURONS; OXIDOPAMINE; PARKINSON DISEASE; PROTEIN-SERINE-THREONINE KINASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; ROTENONE;

EID: 84875140407     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2013.01.008     Document Type: Article

References (46)

1. N. Badiola, R.M. de Oliveira, F. Herrera, C. Guardia-Laguarta, S.A. Gonçalves, M. Pera, M. Suárez-Calvet, J. Clarimon, T.F. Outeiro, and A. Lleó Tau enhances α-synuclein aggregation and toxicity in cellular models of synucleinopathy PLoS ONE 6 2011 e26609
2. D. Berg, K.J. Schweitzer, P. Leitner, A. Zimprich, P. Lichtner, P. Belcredi, T. Brüssel, C. Schulte, S. Maass, and T. Nägele Type and frequency of mutations in the LRRK2 gene in familial and sporadic Parkinson's disease Brain 128 2005 3000 3011
3. T. Botta-Orfila, M. Ezquerra, P. Pastor, R. Fernández-Santiago, C. Pont-Sunyer, Y. Compta, O. Lorenzo-Betancor, L. Samaranch, M.J. Martí, and F. Valldeoriola Age at onset in LRRK2-associated PD is modified by SNCA variants J. Mol. Neurosci. 48 2012 245 247
4. J.M. Bravo-San Pedro, M. Niso-Santano, R. Gomez-Sanchez, E. Pizarro-Estrella, A. Aiastui-Pujana, A. Gorostidi, V. Climent, R. Lopez de Maturana, R. Sanchez-Pernaute, and A. Lopez de Munain The LRRK2 G2019S mutant exacerbates basal autophagy through activation of the MEK/ERK pathway Cell. Mol. Life Sci. 70 2013 121 136
5. G.J. Brewer, J.R. Torricelli, E.K. Evege, and P.J. Price Optimized survival of hippocampal neurons in B27-supplemented Neurobasal, a new serum-free medium combination J. Neurosci. Res. 35 1993 567 576
6. I. Brunk, C. Blex, D. Speidel, N. Brose, and G. Ahnert-Hilger Ca2+-dependent activator proteins of secretion promote vesicular monoamine uptake J. Biol. Chem. 284 2009 1050 1056
7. I. Carballo-Carbajal, S. Weber-Endress, G. Rovelli, D. Chan, B. Wolozin, C.L. Klein, N. Patenge, T. Gasser, and P.J. Kahle Leucine-rich repeat kinase 2 induces alpha-synuclein expression via the extracellular signal-regulated kinase pathway Cell. Signal. 22 2010 821 827
8. S.M. Chambers, C.A. Fasano, E.P. Papapetrou, M. Tomishima, M. Sadelain, and L. Studer Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling Nat. Biotechnol. 27 2009 275 280
9. M.R. Cookson The role of leucine-rich repeat kinase 2 (LRRK2) in Parkinson's disease Nat. Rev. Neurosci. 11 2010 791 797
10. M.R. Cookson, J. Hardy, and P.A. Lewis Genetic neuropathology of Parkinson's disease Int. J. Clin. Exp. Pathol. 1 2008 217 231
11. European Brain Council (2011). Parkinson's disease Fact Sheet. http://www.europeanbraincouncil.org/pdfs/Documents/ Parkinson%27s%20fact%20sheet%20July%202011.pdf.
12. X. Fu, Y. Yang, C. Xu, Y. Niu, T. Chen, Q. Zhou, and J.J. Liu Retrolinkin cooperates with endophilin A1 to mediate BDNF-TrkB early endocytic trafficking and signaling from early endosomes Mol. Biol. Cell 22 2011 3684 3698
13. C.J. Gloeckner, N. Kinkl, A. Schumacher, R.J. Braun, E. O'Neill, T. Meitinger, W. Kolch, H. Prokisch, and M. Ueffing The Parkinson disease causing LRRK2 mutation I2020T is associated with increased kinase activity Hum. Mol. Genet. 15 2006 223 232
14. Y. Golub, D. Berg, D.B. Calne, R.F. Pfeiffer, R.J. Uitti, A.J. Stoessl, Z.K. Wszolek, M.J. Farrer, J.C. Mueller, T. Gasser, and J. Fuchs Genetic factors influencing age at onset in LRRK2-linked Parkinson disease Parkinsonism Relat. Disord. 15 2009 539 541
15. B. Greber, P. Coulon, M. Zhang, S. Moritz, S. Frank, A.J. Müller-Molina, M.J. Araúzo-Bravo, D.W. Han, H.C. Pape, and H.R. Schöler FGF signalling inhibits neural induction in human embryonic stem cells EMBO J. 30 2011 4874 4884
16. S. Hitoshi, R.M. Seaberg, C. Koscik, T. Alexson, S. Kusunoki, I. Kanazawa, S. Tsuji, and D. van der Kooy Primitive neural stem cells from the mammalian epiblast differentiate to definitive neural stem cells under the control of Notch signaling Genes Dev. 18 2004 1806 1811
17. A. Hotta, and J. Ellis Retroviral vector silencing during iPS cell induction: an epigenetic beacon that signals distinct pluripotent states J. Cell. Biochem. 105 2008 940 948
18. M. Inden, Y. Kitamura, M. Abe, A. Tamaki, K. Takata, and T. Taniguchi Parkinsonian rotenone mouse model: reevaluation of long-term administration of rotenone in C57BL/6 mice Biol. Pharm. Bull. 34 2011 92 96
19. T. Ishizawa, P. Mattila, P. Davies, D. Wang, and D.W. Dickson Colocalization of tau and alpha-synuclein epitopes in Lewy bodies J. Neuropathol. Exp. Neurol. 62 2003 389 397
20. A. Iwata, Y. Nagashima, L. Matsumoto, T. Suzuki, T. Yamanaka, H. Date, K. Deoka, N. Nukina, and S. Tsuji Intranuclear degradation of polyglutamine aggregates by the ubiquitin-proteasome system J. Biol. Chem. 284 2009 9796 9803
21. X. Li, J.C. Patel, J. Wang, M.V. Avshalumov, C. Nicholson, J.D. Buxbaum, G.A. Elder, M.E. Rice, and Z. Yue Enhanced striatal dopamine transmission and motor performance with LRRK2 overexpression in mice is eliminated by familial Parkinson's disease mutation G2019S J. Neurosci. 30 2010 1788 1797
22. X. Lin, L. Parisiadou, X.L. Gu, L. Wang, H. Shim, L. Sun, C. Xie, C.X. Long, W.J. Yang, and J. Ding Leucine-rich repeat kinase 2 regulates the progression of neuropathology induced by Parkinson's-disease-related mutant alpha-synuclein Neuron 64 2009 807 827
23. G.H. Liu, J. Qu, K. Suzuki, E. Nivet, M. Li, N. Montserrat, F. Yi, X. Xu, S. Ruiz, and W. Zhang Progressive degeneration of human neural stem cells caused by pathogenic LRRK2 Nature 491 2012 603 607
24. S.E. Lloyd, E.G. Maytham, J. Grizenkova, H. Hummerich, and J. Collinge A Copine family member, Cpne8, is a candidate quantitative trait gene for prion disease incubation time in mouse Neurogenetics 11 2010 185 191
25. D. MacLeod, J. Dowman, R. Hammond, T. Leete, K. Inoue, and A. Abeliovich The familial Parkinsonism gene LRRK2 regulates neurite process morphology Neuron 52 2006 587 593
26. H. Maldonado, E. Ortiz-Riaño, B. Krause, A. Barriga, F. Medina, M.E. Pando, C. Alberti, A.M. Kettlun, L. Collados, and L. García Microtubule proteins and their post-translational forms in the cerebrospinal fluid of patients with paraparesis associated with HTLV-I infection and in SH-SY5Y cells: an in vitro model of HTLV-I-induced disease Biol. Res. 41 2008 239 259
27. H. Maldonado, E. Ramírez, E. Utreras, M.E. Pando, A.M. Kettlun, M. Chiong, A.B. Kulkarni, L. Collados, J. Puente, L. Cartier, and M.A. Valenzuela Inhibition of cyclin-dependent kinase 5 but not of glycogen synthase kinase 3-β prevents neurite retraction and tau hyperphosphorylation caused by secretable products of human T-cell leukemia virus type I-infected lymphocytes J. Neurosci. Res. 89 2011 1489 1498
28. S. Matta, K. Van Kolen, R. da Cunha, G. van den Bogaart, W. Mandemakers, K. Miskiewicz, P.J. De Bock, V.A. Morais, S. Vilain, and D. Haddad LRRK2 controls an EndoA phosphorylation cycle in synaptic endocytosis Neuron 75 2012 1008 1021
29. A. Napolitano, P. Manini, and M. d'Ischia Oxidation chemistry of catecholamines and neuronal degeneration: an update Curr. Med. Chem. 18 2011 1832 1845
30. H.N. Nguyen, B. Byers, B. Cord, A. Shcheglovitov, J. Byrne, P. Gujar, K. Kee, B. Schüle, R.E. Dolmetsch, and W. Langston LRRK2 mutant iPSC-derived DA neurons demonstrate increased susceptibility to oxidative stress Cell Stem Cell 8 2011 267 280
31. L.J. Ozelius, G. Senthil, R. Saunders-Pullman, E. Ohmann, A. Deligtisch, M. Tagliati, A.L. Hunt, C. Klein, B. Henick, and S.M. Hailpern LRRK2 G2019S as a cause of Parkinson's disease in Ashkenazi Jews N. Engl. J. Med. 354 2006 424 425
32. C. Paisán-Ruíz, S. Jain, E.W. Evans, W.P. Gilks, J. Simón, M. van der Brug, A. López de Munain, S. Aparicio, A.M. Gil, and N. Khan Cloning of the gene containing mutations that cause PARK8-linked Parkinson's disease Neuron 44 2004 595 600
33. E.D. Plowey, S.J. Cherra 3rd, Y.J. Liu, and C.T. Chu Role of autophagy in G2019S-LRRK2-associated neurite shortening in differentiated SH-SY5Y cells J. Neurochem. 105 2008 1048 1056
34. M. Polymenidou, and D.W. Cleveland Prion-like spread of protein aggregates in neurodegeneration J. Exp. Med. 209 2012 889 893
35. M.H. Polymeropoulos, C. Lavedan, E. Leroy, S.E. Ide, A. Dehejia, A. Dutra, B. Pike, H. Root, J. Rubenstein, and R. Boyer Mutation in the alpha-synuclein gene identified in families with Parkinson's disease Science 276 1997 2045 2047
36. A. Rajput, D.W. Dickson, C.A. Robinson, O.A. Ross, J.C. Dächsel, S.J. Lincoln, S.A. Cobb, M.L. Rajput, and M.J. Farrer Parkinsonism, Lrrk2 G2019S, and tau neuropathology Neurology 67 2006 1506 1508
37. O.A. Ross, M. Toft, A.J. Whittle, J.L. Johnson, S. Papapetropoulos, D.C. Mash, I. Litvan, M.F. Gordon, Z.K. Wszolek, M.J. Farrer, and D.W. Dickson Lrrk2 and Lewy body disease Ann. Neurol. 59 2006 388 393
38. A. Sánchez-Danés, Y. Richaud-Patin, I. Carballo-Carbajal, S. Jiménez-Delgado, C. Caig, S. Mora, C. Di Guglielmo, M. Ezquerra, B. Patel, and A. Giralt Disease-specific phenotypes in dopamine neurons from human iPS-based models of genetic and sporadic Parkinson's disease EMBO Mol. Med. 4 2012 380 395
39. C. Schiesling, N. Kieper, K. Seidel, and R. Krüger Review: Familial Parkinson's disease - genetics, clinical phenotype and neuropathology in relation to the common sporadic form of the disease Neuropathol. Appl. Neurobiol. 34 2008 255 271
40. J. Simón-Sánchez, C. Schulte, J.M. Bras, M. Sharma, J.R. Gibbs, D. Berg, C. Paisan-Ruiz, P. Lichtner, S.W. Scholz, and D.G. Hernandez Genome-wide association study reveals genetic risk underlying Parkinson's disease Nat. Genet. 41 2009 1308 1312
41. M.G. Spillantini, M.L. Schmidt, V.M. Lee, J.Q. Trojanowski, R. Jakes, and M. Goedert Alpha-synuclein in Lewy bodies Nature 388 1997 839 840
42. K. Takahashi, and S. Yamanaka Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors Cell 126 2006 663 676
43. K. Takahashi, K. Tanabe, M. Ohnuki, M. Narita, T. Ichisaka, K. Tomoda, and S. Yamanaka Induction of pluripotent stem cells from adult human fibroblasts by defined factors Cell 131 2007 861 872
44. A.B. West, D.J. Moore, S. Biskup, A. Bugayenko, W.W. Smith, C.A. Ross, V.L. Dawson, and T.M. Dawson Parkinson's disease-associated mutations in leucine-rich repeat kinase 2 augment kinase activity Proc. Natl. Acad. Sci. USA 102 2005 16842 16847
45. S. Zach, S. Felk, and F. Gillardon Signal transduction protein array analysis links LRRK2 to Ste20 kinases and PKC zeta that modulate neuronal plasticity PLoS ONE 5 2010 e13191
46. A. Zimprich, S. Biskup, P. Leitner, P. Lichtner, M. Farrer, S. Lincoln, J. Kachergus, M. Hulihan, R.J. Uitti, and D.B. Calne Mutations in LRRK2 cause autosomal-dominant parkinsonism with pleomorphic pathology Neuron 44 2004 601 607