Emerging pathways in genetic Parkinson's disease: Autosomal-recessive genes in Parkinson's disease - A common pathway?

FEBS Journal

Volumn 275, Issue 23, 2008, Pages 5758-5766

  Fitzgerald, Julia C ^a   Plun Favreau, Helene ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Cell death; DJ 1; HtrA2; Mitochondria; Mutation; Neuron; Parkin; Parkinson's disease; PINK1; Signalling

Indexed keywords

DJ 1 PROTEIN; PARKIN; PHOSPHOTRANSFERASE; PTEN INDUCED KINASE 1; UNCLASSIFIED DRUG;

AUTOSOMAL RECESSIVE INHERITANCE; DISORDERS OF MITOCHONDRIAL FUNCTIONS; GENE MUTATION; HUMAN; MOLECULAR MECHANICS; NERVE DEGENERATION; NEUROPROTECTION; OXIDATIVE STRESS; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SHORT SURVEY; SIGNAL TRANSDUCTION; WILD TYPE;

ANIMALS; GENES, RECESSIVE; GENETIC PREDISPOSITION TO DISEASE; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; ONCOGENE PROTEINS; OXIDATIVE STRESS; PARKINSON DISEASE; PROTEIN KINASES; SIGNAL TRANSDUCTION; UBIQUITIN-PROTEIN LIGASES;

EID: 55949128232     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2008.06708.x     Document Type: Short Survey

References (96)

1. Kitada T, Asakawa S, Hattori N, Matsumine H, Yamamura Y, Minoshima S, Yokochi M, Mizuno Y Shimizu N (1998) Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 392, 605 608.
2. Lücking CB, Dürr A, Bonifati V, Vaughan J, De Michele G, Gasser T, Harhangi BS, Meco G, Denèfle P, Wood NW et al. (2000) Association between early-onset Parkinson's disease and mutations in the Parkin gene. N Engl J Med 342, 1560 1567.
3. Schapira AH (2008) Mitochondria in the aetiology and pathogenesis of Parkinson's disease. Lancet Neurol 7, 97 109.
4. Hayashi S, Wakabayashi K, Ishikawa A, Nagai H, Saito M, Maruyama M, Takahashi T, Ozawa T, Tsuji S Takahashi H (2000) An autopsy case of autosomal-recessive juvenile parsinsonism with a homozygous exon 4 deletion in the parkin gene. Mov Disord 15, 884 888.
5. Farrer M, Chan P, Chen R, Tan L, Lincoln S, Hernandez D, Forno L, Gwinn-Hardy K, Petrucelli L, Hussey J et al. (2001) Lewy bodies and parkinsonism in families with parkin mutations. Ann Neurol 50, 293 300.
6. Pramstaller PP, Schlossmacher MG, Jacques TS, Scaravelli F, Eskelson C, Pepivani I, Hedrich K, Adel S, Gonzales-McNeal M, Hilker R et al. (2005) Lewy body Parkinson's disease in a large pedigree with 77 parkin mutation carriers. Ann Neurol 58, 411 422.
7. Shimura H, Hattori N, Kubo S, Mizuno Y, Asakawa S, Minoshima S, Shimizu N, Iwai K, Chiba T, Tanaka K et al. (2000) Familial Parkinson disease gene product, Parkin, is a ubiquitin-protein ligase. Nat Genet 3, 302 305.
8. Darios F, Corti O, Lücking CB, Hampe C, Muriel MP, Abbas N, Gu WJ, Hirsch EC, Rooney T, Ruberg M et al. (2003) Parkin prevents mitochondrial swelling and cytochrome c release in mitochondria-dependent cell death. Hum Mol Genet 12, 517 526.
9. Kubo S, Kitami T, Noda S, Shimura H, Uchiyama Y, Asakawa S, Minoshima S, Shimizu N, Mizuno Y Hattori N (2001) Parkin is associated with cellular vesicles. J Neurochem 78, 42 54.
10. Wood-Kaczmar A, Gandhi S Wood NW (2006) Understanding the molecular causes of Parkinson's disease. Trends Mol Med 12, 521 528.
11. Doson MW Guo M (2007) Pink1, Parkin, DJ-1 and mitochondrial dysfunction in Parkinson's disease. Curr Opin Neurobiol 17, 331 337.
12. Valente EM, Abou-Sleiman PM, Caputo V, Muqit MM, Harvey K, Gispert S, Ali Z, Del Turco D, Bentivoglio AR, Healy DG et al. (2004) Hereditary early-onset Parkinson's disease caused by mutations in PINK1. Science 304, 1120 1122.
13. Tan E Skipper LM (2007) Pathogenic mutations in Parkinson's disease. Human Mut 28, 641 653.
14. Healey DG, Abou-Sleiman PM Wood NW (2004) PINK, PANK, or PARK? A clinicians' guide to familial parkinsonism Lancet Neurol 3, 652 662.
15. Gandhi S, Muqit MM, Stanyer L, Healy DG, Abou-Sleiman PM, Hargreaves I, Heales S, Ganguly M, Parsons L, Lees AJ et al. (2006) PINK1 protein in normal human brain and Parkinson's disease. Brain 129, 1720 1731.
16. Weihofen A, Ostaszewski B, Minami Y Selkoe DJ (2007) Pink1 Parkinson mutations, the Cdc37/Hsp90 chaperones and Parkin all influence the maturation or subcellular distribution of Pink1. Human Mol Genet 17, 602 616.
17. Haque EM, Thomas KJ, D'Souza C, Callaghan S, Kitada T, Slack RS, Fraser P, Cookson MR, Tandon A Park DS (2008) Cytoplasmic Pink1 activity protects neurons from dopaminergic neurotoxin MPTP. Proc Natl Acad Sci USA 105, 1716 1721.
18. Hague S, Rogaeva E, Hernandez D, Gulick C, Singleton A, Hanson M, Johnson J, Weiser R, Gallardo M, Ravina B et al. (2003) Early-onset Parkinson's disease caused by a compound heterozygous DJ-1 mutation. Ann Neurol 54, 271 274.
19. Abou-Sleiman PM, Healy DG, Quinn N, Lees AJ Wood NW (2003) The role of pathogenic DJ-1 mutations in Parkinson's disease. Ann Neurol 54, 283 286.
20. Hedrich K, Djarmati A, Schäfer N, Hering R, Wellenbrock C, Weiss PH, Hilker R, Vieregge P, Ozelius LJ, Heutink P et al. (2004) DJ-1 (PARK7) mutations are less frequent than Parkin (PARK2) mutations in early-onset Parkinson disease. Neurology 62, 389 394.
21. Alves da Costa C (2007) DJ-1: a newcomer in Parkinson's disease pathology. Curr Mol Med 7, 650 657.
22. Yoshida K, Sato Y, Yoshike M, Nozawa S, Ariga H Iwamoto T (2003) Immunocytochemical localisation of DJ-1 in human male reproductive tissue. Mol Reprod Dev 66, 391 397.
23. Le Naour F, Misek DE, Krause MC, Deneux L, Giordano TJ, Scholl S Hanash SM (2001) Proteomics-based identification of RS/DJ-1 as a novel circulating tumor antigen in breast cancer. Clin Cancer Res 7, 3328 3335.
24. Zhang L, Shimoji M, Thomas B, Moore DJ, Yu S, Marupudi NI, Torp R, Torgner IA, Ottersen OP, Dawson TM et al. (2005) Mitochondrial localisation of the Parkinson's disease related protein DJ-1: implications for pathogenesis. Hum Mol Genet 14, 2063 2073.
25. Bonifati V, Rizzu P, van Baren MJ, Schaap O, Breedveld GJ, Krieger E, Dekker MC, Squitieri F, Ibanez P, Joosse M et al. (2003) Mutations in the DJ-1 gene associated with autosomal recessive early-onset parkinsonism. Science 299, 256 259.
26. Canet-Avilés RM, Wilson MA, Miller DW, Ahmad R, McLendon C, Bandyopadhyay S, Baptista MJ, Ringe D, Petsko GA Cookson MR (2004) The Parkinson's disease protein DJ-1 is neuroprotective due to cysteine-sulfinic acid-driven mitochondrial localization. Proc Natl Acad Sci USA 101, 9103 9108.
27. Xu J, Zhong N, Wang H, Elias JE, Kim CY, Woldman I, Pifl C, Gygi SP, Geula C Yankner BA (2005) The Parkinson's disease-associated DJ-1 protein is a transcriptional co-activator that protects against neuronal apoptosis. Hum Mol Genet 14, 1231 1241.
28. Junn E, Taniguchi H, Jeong BS, Zhao X, Ichijo H Mouradian MM (2005) Interaction of DJ-1 with Daxx inhibits apoptosis signal-regulating kinase 1 activity and cell death. Proc Natl Acad Sci USA 102, 9691 9696.
29. Shendelman S, Jonason A, Martinat C, Leete T Abeliovich A (2004) DJ-1 is a redox-dependent molecular chaperone that inhibits alpha-synuclein aggregate formation. PLoS Biol 2, e362.
30. Olzmann JA, Brown K, Wilkinson KD, Rees HD, Huai Q, Ke H, Levey AI, Li L Chin LS (2004) Familial Parkinson's disease-associated L166P mutation disrupts DJ-1 protein folding and function. J Biol Chem 279, 8506 8515.
31. Lee SJ, Kim SJ, Kim IK, Ko J, Jeong CS, Kim GH, Park C, Kang SO, Suh PG, Lee HS et al. (2003) Crystal structures of human DJ-1 and Escherichia coli Hsp31, which share an evolutionarily conserved domain. J Biol Chem 278, 44552 44559.
32. Zhou W, Zhu M, Wilson MA, Petsko GA Fink AL (2006) The oxidation state of DJ-1 regulates its chaperone activity toward alpha-synuclein. J Mol Biol 356, 1036 1048.
33. Abeliovich A Flint Beal M (2006) Parkinsonism genes: culprits and clues. J Neurochem 99, 1062 1072.
34. Abou-Sleiman PM, Muqit MM Wood NW (2006) Expanding insights of mitochondrial dysfunction in Parkinson's disease. Nat Rev Neurosci 7, 207 219.
35. De Girolamo LA, Billett EE Hargreaves AJ (2000) Effects of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine on differentiating mouse N2a neuroblastoma cells. J Neurochem 75, 133 140.
36. + and dopamine on the human proteasome: implications for Parkinson's disease aetiology. J Neurochem 105, 225 238.
37. Davis GC, Williams AC, Markey SP, Ebert MH, Caine ED, Reichert CM Kopin IJ (1979) Chronic parkinsonism secondary to intravenous injection of meperidine analogues. Psychiat Res 1, 249 254.
38. Langston WJ, Ballard P, Tetrus JW Irwin I (1983) Chronic parkinsonism in humans due to a product of meperidine-analog synthesis. Science 219, 979 980.
39. Casarejos MJ, Menéndez J, Solano RM, Rodríguez-Navarro JA, García de Yébenes J Mena MA (2006) Susceptibility to rotenone is increased in neurons from Parkin null mice and is reduced by minocycline. J Neurochem 97, 934 946.
40. Deng H, Jankovic J, Guo Y, Xie W Le W (2005) Small interfering RNA targeting the PINK1 induces apoptosis in dopaminergic cells SH-SY5Y. Biochem Biophys Res Commun 337, 1133 1138.
41. Gautier CA, Kitada T Shen J (2008) Loss of PINK1 causes mitochondrial functional defects and increased sensitivity to oxidative stress. Proc Natl Acad Sci USA 105, 11364 11369.
42. Plun-Favreau H Hardy J (2008) Pink1 in mitochondrial function. Proc Natl Acad Sci USA 105, 11041 11042.
43. Liu F, Nguyen JL, Hulleman JD, Li L Rochet JC (2008) Mechanisms of DJ-1 neuroprotection in a cellular model of Parkinson's disease. J Neurochem 105, 2435 2453.
44. Meulener M, Whitworth AJ, Armstrong-Gold CE, Rizzu P, Heutink P, Wes PD, Pallanck LJ Bonini NM (2005) Drosophila DJ-1 mutants are selectively sensitive to environmental toxins associated with Parkinson's disease. Curr Biol 15, 1572 1577.
45. Clark IE, Dodson MW, Jiang C, Cao JH, Huh JR, Seol JH, Yoo SJ, Hay BA Guo M (2006) Drosophila pink1 is required for mitochondrial function and interacts genetically with Parkin. Nature 441, 1162 1166.
46. Park J, Lee SB, Lee S, Kim Y, Song S, Kim S, Bae E, Kim J, Shong M, Kim JM et al. (2006) Mitochondrial dysfunction in Drosophila PINK1 mutants is complemented by Parkin. Nature 441, 1157 1161.
47. Yang Y, Gehrke S, Imai Y, Huang Z, Ouyang Y, Wang JW, Yang L, Beal MF, Vogel H Lu B (2006) Mitochondrial pathology and muscle and dopaminergic neuron degeneration caused by inactivation of Drosophila Pink1 is rescued by Parkin. Proc Natl Acad Sci USA 103, 10793 10798.
48. Poole AC, Thomas RE, Andrews LA, McBride HM, Whitworth AJ Pallanck LJ (2008) The PINK1/Parkin pathway regulates mitochondrial morphology. Proc Natl Acad Sci USA 105, 1638 1643.
49. Exner N, Treske B, Paquet D, Holmström K, Schiesling C, Gispert S, Carballo-Carbajal I, Berg D, Hoepken HH, Gasser T et al. (2007) Loss-of-function of human PINK1 results in mitochondrial pathology and can be rescued by Parkin. J Neurosci 27, 12413 12418.
50. Yang Y, Ouyang Y, Yang L, Beal MF, McQuibban A, Vogel H Lu B (2008) Pink1 regulates mitochondrial dynamics through interaction with the fission/fusion machinery. Proc Natl Acad Sci USA 105, 7070 7075.
51. Yang Y, Gehrke S, Haque ME, Imai Y, Kosek J, Yang L, Beal MF, Nishimura I, Wakamatsu K, Ito S et al. (2005) Inactivation of Drosophila DJ-1 leads to impairments of oxidative stress response and phosphatidylinositol 3-kinase/Akt signaling. Proc Natl Acad Sci USA 102, 13670 13675.
52. Ekert PG Vaux DL (2005) The mitochondrial death squad: hardened killers or innocent bystanders? Curr Opin Cell Biol 17, 626 630.
53. Muqit MM, Abou-Sleiman PM, Saurin AT, Harvey K, Gandhi S, Deas E, Eaton S, Payne Smith MD, Venner K, Matilla A et al. (2006) Altered cleavage and localization of PINK1 to aggresomes in the presence of proteasomal stress. J Neurochem 98, 156 169.
54. Lin W Kang UJ (2008) PINK1 characterization of processing, stability, and subcellular localization. J Neurochem 106, 464 474.
55. Plun-Favreau H, Klupsch K, Moisoi N, Gandhi S, Kjaer S, Frith D, Harvey K, Deas E, Harvey RJ, McDonald N et al. (2007) The mitochondrial protease HtrA2 is regulated by Parkinson's disease-associated kinase PINK1. Nat Cell Biol 9, 1243 1252.
56. De Martino GN Slaughter CA (1999) The proteasome, a novel protease regulated by multiple mechanisms. J Biol Chem 274, 22123 22126.
57. Tanaka K Chiba T (1998) The proteasome: a protein-destroying machine. Genes Cells 3, 499 510.
58. Dawson TM Dawson VL (2003) Molecular pathways of neurodegeneration in Parkinson's disease. Science 302, 819 822.
59. Leroy E, Boyer R, Auburger G, Leube B, Ulm G, Mezey E, Harta G, Brownstein MJ, Jonnalagada S, Chernova T et al. (1998) The ubiquitin pathway in Parkinson's disease. Nature 395, 451 452.
60. Yokota T, Sugawara K, Ito K, Takahashi R, Ariga H Mizusawa H (2003) Down regulation of DJ-1 enhances cell death by oxidative stress, ER stress, and proteasome inhibition. Biochem Biophys Res Commun 312, 1342 1348.
61. Petrucelli L, O'Farrell C, Lockhart PJ, Baptista M, Kehoe K, Vink L, Choi P, Wolozin B, Farrer M, Hardy J et al. (2002) Parkin protects against the toxicity associated with mutant α-synuclein: proteasome dysfunction selectively affects catecholaminergic neurons. Neuron 36, 1007 1019.
62. Yang H, Zhou H, Li B, Niu G Chen S (2007) Downregulation of Parkin damages antioxidant defenses and enhances proteasome inhibition-induced toxicity in PC12 cells. J Neuroimmune Pharmacol 2, 276 283.
63. Yang W, Chen L, Ding Y, Zhuang X Kang UJ (2007) Paraquat induces dopaminergic dysfunction and proteasome impairment in DJ-1-deficient mice. Hum Mol Genet 16, 2900 2910.
64. Miller DW, Ahmad R, Hague S, Baptista MJ, Canet-Aviles R, McLendon C, Carter DM, Zhu PP, Stadler J, Chandran J et al. (2003) L166P mutant DJ-1, causative for recessive Parkinson's disease, is degraded through the ubiquitin-proteasome system. J Biol Chem 278, 36588 36595.
65. Moriwaki Y, Kim YJ, Ido Y, Misawa H, Kawashima K, Endo S Takahashi R (2008) L347P PINK1 mutant that fails to bind to Hsp90/Cdc37 chaperones is rapidly degraded in a proteasome-dependent manner. Neurosci Res 61, 43 48.
66. Choi P, Ostrerova-Golts N, Sparkman D, Cochran E, Lee JM Wolozin B (2000) Parkin is metabolized by the ubiquitin/proteasome system. NeuroReport 11, 2635 2638.
67. Hyun D, Lee M, Hattori N, Kubo S, Mizuno Y, Halliwell B Jenner P (2002) Effect of wild-type or mutant Parkin on oxidative damage, nitric oxide, antioxidant defenses, and the proteasome. J Biol Chem 277, 28572 28577.
68. Pridgeon JW, Olzmann JA, Chin LS Li L (2008) PINK1 protects against oxidative stress by phosphorylating mitochondrial chaperone TRAP1. PLoS Biol 5, 1494 1503.
69. Young JC Hartl FU (2003) A stress sensor for the bacterial periplasm. Cell 113, 1 2.
70. Moore DJ, West AB, Dikeman DA, Dawson VL Dawson TM (2008) Parkin mediates the degradation-independent ubiquitination of Hsp70. J Neurochem 105, 1806 1819.
71. Kahle PJ Haass C (2004) How does Parkin ligate ubiquitin to Parkinson's disease? EMBO Rep 5, 681 685.
72. Winklhofer KF, Henn IH, Kay-Jackson PC, Heller U Tatzelt J (2003) Inactivation of Parkin by oxidative stress and C-terminal truncations: a protective role of molecular chaperones. J Biol Chem 278, 47199 47208.
73. Anderson JK (2004) Oxidative stress in neurodegeneration: cause or consequence? Nat Rev Neurosci 10 (Suppl. S18 S25.
74. Taira T, Saito Y, Niki T, Iguchi-Ariga SM, Takahashi K Ariga H (2004) DJ-1 has a role in antioxidative stress to prevent cell death. EMBO Rep 5, 213 218.
75. Martinat C, Shendelman S, Jonason A, Leete T, Beal MF, Yang L, Floss T Abeliovich A (2004) Sensitivity to oxidative stress in DJ-1-deficient dopamine neurons: an ES-derived cell model of primary parkinsonism. PLoS Biol 2, e327.
76. Moore DJ, Zhang L, Troncoso J, Lee MK, Hattori N, Mizuno Y, Dawson TM Dawson VL (2005) Association of DJ-1 and Parkin mediated by pathogenic DJ-1 mutations and oxidative stress. Hum Mol Genet 14, 71 84.
77. Palacino JJ, Sagi D, Goldberg MS, Krauss S, Motz C, Wacker M, Klose J Shen J (2004) Mitochondrial dysfunction and oxidative damage in Parkin-deficient mice. J Biol Chem 279, 18614 18622.
78. Pesah Y, Pham T, Burgess H, Middlebrooks B, Verstreken P, Zhou Y, Harding M, Bellen H Mardon G (2004) Drosophila Parkin mutants have decreased mass and cell size and increased sensitivity to oxygen radical stress. Development 131, 2183 2194.
79. Wang D, Qian L, Xiong H, Liu J, Neckameyer WS, Oldham S, Xia K, Wang J, Bodmer R Zhang Z (2006) Antioxidants protect PINK1-dependent dopaminergic neurons in Drosophila. Proc Natl Acad Sci USA 103, 13520 13525.
80. Beilina A, Van Der Brug M, Ahmad R, Kesavapany S, Miller DW, Petsko GA Cookson MR (2005) Mutations in PTEN-induced putative kinase 1 associated with recessive Parkinsonism have differential effects on protein stability. Proc Natl Acad Sci USA 102, 5703 5708.
81. Silvestri L, Caputo V, Bellacchio E, Atorino L, Dallapiccola B, Valente EM Casari G (2005) Mitochondrial import and enzymatic activity of PINK1 mutants associated to recessive parkinsonism. Hum Mol Genet 14, 3477 3492.
82. Unoki M Nakamura Y (2001) Growth-suppressive effects of BPOZ and EGR2, two genes involved in the PTEN signaling pathway. Oncogene 20, 4457 4465.
83. Kim RH, Peters M, Jang Y, Shi W, Pintilie M, Fletcher GC, DeLuca C, Liepa J, Zhou L, Snow B et al. (2005) DJ-1, a novel regulator of the tumor suppressor PTEN. Cancer Cell 7, 263 273.
84. Fallon L, Bélanger CM, Corera AT, Kontogiannea M, Regan-Klapisz E, Moreau F, Voortman J, Haber M, Rouleau G, Thorarinsdottir T et al. (2006) A regulated interaction with the UIM protein Eps15 implicates Parkin in EGF receptor trafficking and PI(3)K-Akt signalling. Nat Cell Biol 8, 834 842.
85. Yang L, Sun M, Sun XM, Cheng GZ, Nicosia SV Cheng JQ (2007) Akt attenuation of the serine protease activity of HtrA2/Omi through phosphorylation of serine 212. J Biol Chem 282, 10981 10987.
86. Yamamoto A, Friedlein A, Imai Y, Takahashi R, Kahle PJ Haass C (2005) Parkin phosphorylation and modulation of its E3 ubiquitin ligase activity. J Biol Chem 280, 3390 3399.
87. Avraham E, Rott R, Liani E, Szargel R Engelender S (2007) Phosphorylation of Parkin by the cyclin-dependent kinase 5 at the linker region modulates its ubiquitin-ligase activity and aggregation. J Biol Chem 282, 12842 12850.
88. Tang B, Xiong H, Sun P, Zhang Y, Wang D, Hu Z, Zhu Z, Ma H, Pan Q, Xia JH et al. (2006) Association of PINK1 and DJ-1 confers digenic inheritance of early-onset Parkinson's disease. Hum Mol Genet 15, 1816 1825.
89. Strauss KM, Martins LM, Plun-Favreau H, Marx FP, Kautzmann S, Berg D, Gasser T, Wszolek Z, Müller T, Bornemann A et al. (2005) Loss of function mutations in the gene encoding Omi/HtrA2 in Parkinson's disease. Hum Mol Genet 14, 2099 2111.
90. Simón-Sánchez J Singleton AB (2008) Sequencing analysis of OMI/HTRA2 shows previously reported pathogenic mutations in neurologically normal controls. Hum Mol Genet 17, 1988 1993.
91. Bogaerts V, Nuytemans K, Reumers J, Pals P, Engelborghs S, Pickut B, Corsmit E, Peeters K, Schymkowitz J, De Deyn PP et al. (2008) Genetic variability in the mitochondrial serine protease HTRA2 contributes to risk for Parkinson disease. Hum Mutat 29, 832 840.
92. Anichtchik O, Diekmann H, Fleming A, Roach A, Goldsmith P Rubinsztein DC (2008) Loss of Pink1 function affects development and results in neurodegeneration in zebrafish. J Neurosci 28, 8199 8207.
93. Falkenburger BH Schulz JB (2006) Limitations of cellular models in Parkinson's disease research. J Neural Transm 70 (Suppl. 261 268.
94. Hyun-Park I, Arora N, Huo H, Maherali N, Ahfeldt T, Shimamura A, Lensch MW, Cowan C, Hochedlinger K Daley GQ (2008) Disease-specific induced pluripotent stem cells. Cell 134, 1 10.
95. Nishikawa S, Goldstein RA Nierras CR (2008) The promise of human induced pluripotent stem cells for research and therapy. Nat Rev Mol Cell Biol 9, 725 729.
96. Dimos JT, Rodolfa KT, Niakan KK, Weisenthal LM, Mitsumoto H, Chung W, Croft GF, Saphier G, Leibel R, Goland R et al. (2008) Induced pluripotent stem cells generated from patients with ALS can be differentiated into notor neurons. Science 321, 1218 1221.