Home LiteratureArticle Details
PMID: 22407749 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Disease-specific phenotypes in dopamine neurons from human iPS-based models of genetic and sporadic Parkinson's disease.

EMBO molecular medicine ·Vol. 4 ·No. 5 ·2012-05-00 ·Pages 380-95

Sánchez-Danés A, Richaud-Patin Y, Carballo-Carbajal I, Jiménez-Delgado S, Caig C, Mora S, Di Guglielmo C, Ezquerra M, Patel B, Giralt A, Canals JM, Memo M, Alberch J, López-Barneo J, Vila M, Cuervo AM, Tolosa E, Consiglio A, Raya A

Abstract

Induced pluripotent stem cells (iPSC) offer an unprecedented opportunity to model human disease in relevant cell types, but it is unclear whether they could successfully model age-related diseases such as Parkinson's disease (PD). Here, we generated iPSC lines from seven patients with idiopathic PD (ID-PD), four patients with familial PD associated to the G2019S mutation in the Leucine-Rich Repeat Kinase 2 (LRRK2) gene (LRRK2-PD) and four age- and sex-matched healthy individuals (Ctrl). Over long-time culture, dopaminergic neurons (DAn) differentiated from either ID-PD- or LRRK2-PD-iPSC showed morphological alterations, including reduced numbers of neurites and neurite arborization, as well as accumulation of autophagic vacuoles, which were not evident in DAn differentiated from Ctrl-iPSC. Further induction of autophagy and/or inhibition of lysosomal proteolysis greatly exacerbated the DAn morphological alterations, indicating autophagic compromise in DAn from ID-PD- and LRRK2-PD-iPSC, which we demonstrate occurs at the level of autophagosome clearance. Our study provides an iPSC-based in vitro model that captures the patients' genetic complexity and allows investigation of the pathogenesis of both sporadic and familial PD cases in a disease-relevant cell type.

MeSH Terms
Autophagy Cells, Cultured Dopamine/metabolism Humans Neurons/pathology,physiology Parkinson Disease/pathology,physiopathology Pluripotent Stem Cells/pathology,physiology Receptors, Dopamine/metabolism Vacuoles/metabolism,ultrastructure
Chemicals
Receptors, Dopamine Dopamine
Authors & Affiliations
19 authors, click to expand affiliations / ORCID
Sánchez-Danés Adriana
Institute for Biomedicine (IBUB), University of Barcelona, Barcelona, Spain.
Richaud-Patin Yvonne
Carballo-Carbajal Iria
Jiménez-Delgado Senda
Caig Carles
Mora Sergio
Di Guglielmo Claudia
Ezquerra Mario
Patel Bindiben
Giralt Albert
Canals Josep M
Memo Maurizio
Alberch Jordi
López-Barneo José
Vila Miquel
Cuervo Ana Maria
Tolosa Eduard
Consiglio Antonella
Raya Angel
References (48)
48 references, click to expand
  1. Culturing hippocampal neurons.
    Nat Protoc. 2006;1(5):2406-15 PMID: 17406484
  2. Disease-corrected haematopoietic progenitors from Fanconi anaemia induced pluripotent stem cells.
    Nature. 2009 Jul 2;460(7251):53-9 PMID: 19483674
  3. Efficient and rapid generation of induced pluripotent stem cells from human keratinocytes.
    Nat Biotechnol. 2008 Nov;26(11):1276-84 PMID: 18931654
  4. Missing pieces in the Parkinson's disease puzzle.
    Nat Med. 2010 Jun;16(6):653-61 PMID: 20495568
  5. The role of leucine-rich repeat kinase 2 (LRRK2) in Parkinson's disease.
    Nat Rev Neurosci. 2010 Dec;11(12):791-7 PMID: 21088684
  6. Leucine-rich repeat kinase 2 regulates the progression of neuropathology induced by Parkinson's-disease-related mutant alpha-synuclein.
    Neuron. 2009 Dec 24;64(6):807-27 PMID: 20064389
  7. Induction of pluripotent stem cells from adult human fibroblasts by defined factors.
    Cell. 2007 Nov 30;131(5):861-72 PMID: 18035408
  8. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing.
    EMBO J. 2000 Nov 1;19(21):5720-8 PMID: 11060023
  9. Induced pluripotent stem cell technology for the study of human disease.
    Nat Methods. 2010 Jan;7(1):25-7 PMID: 20038952
  10. Induced pluripotent stem cell lines derived from human somatic cells.
    Science. 2007 Dec 21;318(5858):1917-20 PMID: 18029452
  11. Functional neural development from human embryonic stem cells: accelerated synaptic activity via astrocyte coculture.
    J Neurosci. 2007 Mar 21;27(12):3069-77 PMID: 17376968
  12. Friedreich's ataxia induced pluripotent stem cells model intergenerational GAA⋅TTC triplet repeat instability.
    Cell Stem Cell. 2010 Nov 5;7(5):631-7 PMID: 21040903
  13. Induced pluripotent stem cells from a spinal muscular atrophy patient.
    Nature. 2009 Jan 15;457(7227):277-80 PMID: 19098894
  14. Parkinson's disease: from monogenic forms to genetic susceptibility factors.
    Hum Mol Genet. 2009 Apr 15;18(R1):R48-59 PMID: 19297401
  15. Reprogramming of human somatic cells to pluripotency with defined factors.
    Nature. 2008 Jan 10;451(7175):141-6 PMID: 18157115
  16. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors.
    Cell. 2006 Aug 25;126(4):663-76 PMID: 16904174
  17. Extensive involvement of autophagy in Alzheimer disease: an immuno-electron microscopy study.
    J Neuropathol Exp Neurol. 2005 Feb;64(2):113-22 PMID: 15751225
  18. BDNF regulation under GFAP promoter provides engineered astrocytes as a new approach for long-term protection in Huntington's disease.
    Gene Ther. 2010 Oct;17(10):1294-308 PMID: 20463759
  19. Patient-specific induced pluripotent stem-cell-derived models of LEOPARD syndrome.
    Nature. 2010 Jun 10;465(7299):808-12 PMID: 20535210
  20. Efficient generation of A9 midbrain dopaminergic neurons by lentiviral delivery of LMX1A in human embryonic stem cells and induced pluripotent stem cells.
    Hum Gene Ther. 2012 Jan;23(1):56-69 PMID: 21877920
  21. LRRK2 mutant iPSC-derived DA neurons demonstrate increased susceptibility to oxidative stress.
    Cell Stem Cell. 2011 Mar 4;8(3):267-80 PMID: 21362567
  22. Patient-specific induced pluripotent stem-cell models for long-QT syndrome.
    N Engl J Med. 2010 Oct 7;363(15):1397-409 PMID: 20660394
  23. Induced pluripotent stem cells generated from patients with ALS can be differentiated into motor neurons.
    Science. 2008 Aug 29;321(5893):1218-21 PMID: 18669821
  24. The translation factor eIF-4E promotes tumor formation and cooperates with c-Myc in lymphomagenesis.
    Nat Med. 2004 May;10(5):484-6 PMID: 15098029
  25. Protein misfolding disorders and macroautophagy.
    Curr Opin Cell Biol. 2011 Apr;23(2):190-7 PMID: 21087849
  26. Cloning of the gene containing mutations that cause PARK8-linked Parkinson's disease.
    Neuron. 2004 Nov 18;44(4):595-600 PMID: 15541308
  27. A human iPSC model of Hutchinson Gilford Progeria reveals vascular smooth muscle and mesenchymal stem cell defects.
    Cell Stem Cell. 2011 Jan 7;8(1):31-45 PMID: 21185252
  28. What features improve the accuracy of clinical diagnosis in Parkinson's disease: a clinicopathologic study.
    Neurology. 1992 Jun;42(6):1142-6 PMID: 1603339
  29. Parkinson's disease patient-derived induced pluripotent stem cells free of viral reprogramming factors.
    Cell. 2009 Mar 6;136(5):964-77 PMID: 19269371
  30. Mutations in LRRK2 cause autosomal-dominant parkinsonism with pleomorphic pathology.
    Neuron. 2004 Nov 18;44(4):601-7 PMID: 15541309
  31. Brief report: efficient generation of hematopoietic precursors and progenitors from human pluripotent stem cell lines.
    Stem Cells. 2011 Jul;29(7):1158-64 PMID: 21544903
  32. Modelling pathogenesis and treatment of familial dysautonomia using patient-specific iPSCs.
    Nature. 2009 Sep 17;461(7262):402-6 PMID: 19693009
  33. Autophagy regulates lipid metabolism.
    Nature. 2009 Apr 30;458(7242):1131-5 PMID: 19339967
  34. Studies on the mechanisms of autophagy: maturation of the autophagic vacuole.
    J Cell Biol. 1990 Jun;110(6):1935-45 PMID: 2161853
  35. Molecular and clinical prodrome of Parkinson disease: implications for treatment.
    Nat Rev Neurol. 2010 Jun;6(6):309-17 PMID: 20479780
  36. Generation of cardiomyocytes from new human embryonic stem cell lines derived from poor-quality blastocysts.
    Cold Spring Harb Symp Quant Biol. 2008;73:127-35 PMID: 19028986
  37. Generation of isogenic pluripotent stem cells differing exclusively at two early onset Parkinson point mutations.
    Cell. 2011 Jul 22;146(2):318-31 PMID: 21757228
  38. Neural differentiation of human induced pluripotent stem cells follows developmental principles but with variable potency.
    Proc Natl Acad Sci U S A. 2010 Mar 2;107(9):4335-40 PMID: 20160098
  39. Autophagy in neurite injury and neurodegeneration: in vitro and in vivo models.
    Methods Enzymol. 2009;453:217-49 PMID: 19216909
  40. Functional cardiomyocytes derived from human induced pluripotent stem cells.
    Circ Res. 2009 Feb 27;104(4):e30-41 PMID: 19213953
  41. Phosphorylation of 4E-BP by LRRK2 affects the maintenance of dopaminergic neurons in Drosophila.
    EMBO J. 2008 Sep 17;27(18):2432-43 PMID: 18701920
  42. Parkinson disease: a role for autophagy?
    Neuroscientist. 2010 Aug;16(4):335-41 PMID: 20360601
  43. Genetic animal models of Parkinson's disease.
    Neuron. 2010 Jun 10;66(5):646-61 PMID: 20547124
  44. Modeling inherited metabolic disorders of the liver using human induced pluripotent stem cells.
    J Clin Invest. 2010 Sep;120(9):3127-36 PMID: 20739751
  45. A model for neural development and treatment of Rett syndrome using human induced pluripotent stem cells.
    Cell. 2010 Nov 12;143(4):527-39 PMID: 21074045
  46. A protocol describing the genetic correction of somatic human cells and subsequent generation of iPS cells.
    Nat Protoc. 2010 Apr;5(4):647-60 PMID: 20224565
  47. Parkinson's disease.
    Lancet. 2009 Jun 13;373(9680):2055-66 PMID: 19524782
  48. Disease-specific induced pluripotent stem cells.
    Cell. 2008 Sep 5;134(5):877-86 PMID: 18691744
Article Info
Journal
EMBO molecular medicine
Abbr.
EMBO Mol Med
ISSN
1757-4684
Published
2012-05-00
Epub
2012-00-08
Pages
380-95
Language
English
Region
England
NLM ID
101487380
PMCID
PMC3403296
Subset
IM
Grants
NIA NIH HHS · P30 AG038072 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com