Downregulation of MicroRNA-9 in iPSC-Derived Neurons of FTD/ALS Patients with TDP-43 Mutations

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Zhang, Zhijun ^a,g   Almeida, Sandra ^a   Lu, Yubing ^a   Nishimura, Agnes L ^b   Peng, Lingtao ^a,c   Sun, Danqiong ^d,h   Wu, Bei ^e   Karydas, Anna M ^f   Tartaglia, Maria C ^f,i   Fong, Jamie C ^f   Miller, Bruce L ^f   Farese Jr , Robert V ^d,f   Moore, Melissa J ^a,c   Shaw, Christopher E ^b   Gao, Fen Biao ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d GLADSTONE INSTITUTE OF CARDIOVASCULAR DISEASE   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g SHANGHAI JIAO TONG UNIVERSITY   (China)

^h System Biosciences   (United States)

ⁱ UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; MICRORNA 9; RNA PRECURSOR; SHORT HAIRPIN RNA; TAR DNA BINDING PROTEIN; VALINE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL LINE; CELL STRESS; CONTROLLED STUDY; CYTOPLASM; DOWN REGULATION; FRONTOTEMPORAL DEMENTIA; GENE; GENE CONTROL; GENE MUTATION; HUMAN; HUMAN CELL; MITOSIS; NERVE CELL DIFFERENTIATION; NERVE CELL LESION; NONHUMAN; PHENOTYPE; PLURIPOTENT STEM CELL; PROTEIN LOCALIZATION; TARDBP GENE;

AGED; AMYOTROPHIC LATERAL SCLEROSIS; BASE SEQUENCE; CELL DIFFERENTIATION; DNA-BINDING PROTEINS; DOWN-REGULATION; FRONTOTEMPORAL DEMENTIA; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MALE; MICRORNAS; MUTATION; NEURONS; PHENOTYPE;

EID: 84885444052     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0076055     Document Type: Article

References (59)

1. van Langenhove T, van der Zee J, van Broeckhoven C, (2012) The molecular basis of the frontotemporal lobar degeneration-amyotrophic lateral sclerosis spectrum. Ann Med 44: 817-828.
2. Watts GD, Wymer J, Kovach MJ, Mehta SG, Mumm S, et al. (2004) Inclusion body myopathy associated with Paget disease of bone and frontotemporal dementia is caused by mutant valosin containing protein. Nat Genet 36: 377-381.
3. Johnson JO, Mandrioli J, Benatar M, Abramzon Y, Van Deerlin VM, et al. (2010) Exome sequencing reveals VCP mutations as a cause of familial ALS. Neuron 68: 857-864.
4. Skibinski G, Parkinson NJ, Brown JM, Chakrabarti L, Lloyd SL, et al. (2005) Mutations in the endosomal ESCRTIII-complex subunit CHMP2B in frontotemporal dementia. Nat Genet 37: 806-808.
5. Cox LE, Ferraiuolo L, Goodall EF, Heath PR, Higginbottom A, et al. (2010) Mutations in CHMP2B in lower motor neuron predominant amyotrophic lateral sclerosis (ALS). PLoS One 5: e9872.
6. Deng HX, Chen W, Hong ST, Boycott KM, Gorrie GH, et al. (2011) Mutations in UBQLN2 cause dominant X-linked juvenile and adult-onset ALS and ALS/dementia. Nature 477: 211-215.
7. DeJesus-Hernandez M, Mackenzie IR, Boeve BF, Boxer AL, Baker M, et al. (2011) Expanded GGGGCC hexanucleotide repeat in noncoding region of C9ORF72 causes chromosome 9p-linked FTD and ALS. Neuron 72: 245-256.
8. Renton AE, Majounie E, Waite A, Simón-Sánchez J, Rollinson S, et al. (2011) A hexanucleotide repeat expansion in C9ORF72 is the cause of chromosome 9p21-linked ALS-FTD. Neuron 72: 257-268.
9. Neumann M, Sampathu DM, Kwong LK, Truax AC, Micsenyi MC, et al. (2006) Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 314: 130-133.
10. Arai T, Hasegawa M, Akiyama H, Ikeda K, Nonaka T, et al. (2006) TDP-43 is a component of ubiquitin-positive tau-negative inclusions in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Biochem Biophys Res Commun 351: 602-611.
11. Sreedharan J, Blair IP, Tripathi VB, Hu X, Vance C, et al. (2008) TDP-43 mutations in familial and sporadic amyotrophic lateral sclerosis. Science 319: 1668-1672.
12. Kwiatkowski TJ Jr, Bosco DA, Leclerc AL, Tamrazian E, Vanderburg CR, et al. (2009) Mutations in the FUS/TLS gene on chromosome 16 cause familial amyotrophic lateral sclerosis. Science 323: 1205-1208.
13. Vance C, Rogelj B, Hortobágyi T, De Vos KJ, Nishimura AL, et al. (2009) Mutations in FUS, an RNA processing protein, cause familial amyotrophic lateral sclerosis type 6. Science 323: 1208-1211.
14. Lee EB, Lee VM, Trojanowski JQ, (2011) Gains or losses: molecular mechanisms of TDP43-mediated neurodegeneration. Nat Rev Neurosci 13: 38-50.
15. Da Cruz S, Cleveland DW, (2011) Understanding the role of TDP-43 and FUS/TLS in ALS and beyond. Curr Opin Neurobiol 21: 904-919.
16. Gregory RI, Yan KP, Amuthan G, Chendrimada T, Doratotaj B, et al. (2004) The microprocessor complex mediates the genesis of microRNAs. Nature 432: 235-240.
17. Kawahara Y, Mieda-Sato A, (2012) TDP-43 promotes microRNA biogenesis as a component of the Drosha and Dicer complexes. Proc Natl Acad Sci U S A 109: 3347-3352.
18. Li Z, Lu Y, Xu XL, Gao FB, (2013) The FTD/ALS-associated RNA-binding protein TDP-43 regulates the robustness of neuronal specification through microRNA-9a in Drosophila. Hum Mol Genet 22: 218-225.
19. Ambros V, (2001) microRNAs: tiny regulators with great potential. Cell 107: 823-826.
20. Huntzinger E, Izaurralde E, (2011) Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat Rev Genet 12: 99-110.
21. Gascon E, Gao FB, (2012) Cause or effect: Misregulation of microRNA pathways in neurodegeneration. Front Neurosci 6: 48.
22. Wils H, Kleinberger G, Janssens J, Pereson S, Joris G, et al. (2010) TDP-43 transgenic mice develop spastic paralysis and neuronal inclusions characteristic of ALS and frontotemporal lobar degeneration. Proc Natl Acad Sci U S A 107: 3858-3863.
23. Ayala YM, De Conti L, Avendaño-Vázquez SE, Dhir A, Romano M, et al. (2011) TDP-43 regulates its mRNA levels through a negative feedback loop. EMBO J 30: 277-288.
24. Igaz LM, Kwong LK, Lee EB, Chen-Plotkin A, Swanson E, et al. (2011) Dysregulation of the ALS-associated gene TDP-43 leads to neuronal death and degeneration in mice. J Clin Invest 121: 726-738.
25. Polymenidou M, Lagier-Tourenne C, Hutt KR, Huelga SC, Moran J, et al. (2011) Long pre-mRNA depletion and RNA missplicing contribute to neuronal vulnerability from loss of TDP-43. Nat Neurosci 14: 459-468.
26. Kraemer BC, Schuck T, Wheeler JM, Robinson LC, Trojanowski JQ, et al. (2009) Loss of murine TDP-43 disrupts motor function and plays an essential role in embryogenesis. Acta Neuropathol 119: 409-419.
27. Wu LS, Cheng WC, Hou SC, Yan YT, Jiang ST, et al. (2010) TDP-43, a neuro-pathosignature factor, is essential for early mouse embryogenesis. Genesis 48: 56-62.
28. Sephton CF, Good SK, Atkin S, Dewey CM, Mayer P 3rd, et al. (2010) TDP-43 is a developmentally regulated protein essential for early embryonic development. J Biol Chem 285: 6826-6834.
29. Chiang PM, Ling J, Jeong YH, Price DL, Aja SM, et al. (2010) Deletion of TDP-43 down-regulates Tbc1d1, a gene linked to obesity, and alters body fat metabolism. Proc Natl Acad Sci U S A 107: 16320-16324.
30. Wu LS, Cheng WC, Shen CK, (2012) Targeted depletion of TDP-43 expression in the spinal cord motor neurons leads to the development of amyotrophic lateral sclerosis-like phenotypes in mice. J Biol Chem 287: 27335-27344.
31. Iguchi Y, Katsuno M, Niwa J, Takagi S, Ishigaki S, et al. (2013) Loss of TDP-43 causes age-dependent progressive motor neuron degeneration. Brain 136: 1371-1382.
32. Yamanaka S, (2007) Strategies and new developments in the generation of patient-specific pluripotent stem cells. Cell Stem Cell 1: 39-49.
33. Dimos JT, Rodolfa KT, Niakan KK, Niakan KK, Weisenthal LM, et al. (2008) Induced pluripotent stem cells generated from patients with ALS can be differentiated into motor neurons. Science 321: 1218-1221.
34. Nguyen HN, Byers B, Cord B, Shcheglovitov A, Byrne J, et al. (2011) LRRK2 mutant iPSC-derived DA neurons demonstrate increased susceptibility to oxidative stress. Cell Stem Cell 8: 267-280.
35. Bilican B, Serio A, Barmada SJ, Nishimura AL, Sullivan GJ, et al. (2012) Mutant induced pluripotent stem cell lines recapitulate aspects of TDP-43 proteinopathies and reveal cell-specific vulnerability. Proc Natl Acad Sci U S A 109: 5803-5808.
36. Egawa N, Kitaoka S, Tsukita K, Yamamoto T, Adachi F, et al. (2012) Drug screening for ALS using patient-specific induced pluripotent stem cells. Sci Transl Med 4: 145ra104.
37. Almeida S, Zhang Z, Copplola G, Mao W, Futai K, et al. (2012) Induced pluripotent stem cell models of progranulin-deficient frontotemporal dementia uncover specific reversible neuronal defects. Cell Rep 2: 789-798.
38. HD iPSC Consortium, (2012) Induced pluripotent stem cells from patients with Huntington's disease show CAG-repeat-expansion-associated phenotypes. Cell Stem Cell 11: 264-278.
39. Israel MA, Yuan SH, Bardy C, Reyna SM, Mu Y, et al. (2012) Probing sporadic and familial Alzheimer's disease using induced pluripotent stem cells. Nature 482: 216-220.
40. Almeida S, Gascon E, Tran H, Chou HJ, Gendron TF, et al. (2012) Modeling key pathological features of frontotemporal dementia with C9ORF72 repeat expansion in iPSC-derived human neurons. Acta Neuropathol Jul 9 [Epub ahead of print].
41. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, et al. (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131: 861-872.
42. Delaloy C, Liu L, Lee J-A, Su H, Shen F, et al. (2010) MicroRNA-9 coordinates proliferation and migration of human embryonic stem cell-derived neural progenitors. Cell Stem Cell 6: 323-335.
43. Lee JA, Liu L, Javier R, Kreitzer AC, Delaloy C, et al. (2011) ESCRT-III subunits Snf7-1 and Snf7-2 differentially regulate transmembrane cargos in hESC-derived human neurons. Mol Brain 4: 37.
44. Dewey CM, Cenik B, Sephton CF, Dries DR, Mayer P 3rd, et al. (2011) TDP-43 is directed to stress granules by sorbitol, a novel physiological osmotic and oxidative stressor. Mol Cell Biol 31: 1098-1108.
45. Colombrita C, Zennaro E, Fallini C, Weber M, Sommacal A, et al. (2009) TDP-43 is recruited to stress granules in conditions of oxidative insult. J Neurochem 111: 1051-1061.
46. Popa CV, Dumitru I, Ruta LL, Danet AF, Farcasanu IC, (2010) Exogenous oxidative stress induces Ca2+ release in the yeast Saccharomyces cerevisiae. FEBS J 277: 4027-4038.
47. Agard NJ, Mahrus S, Trinidad JC, Lynn A, Burlingame AL, et al. (2012) Global kinetic analysis of proteolysis via quantitative targeted proteomics. Proc Natl Acad Sci U S A 109: 1913-1918.
48. Neumann M, Rademakers R, Roeber S, Baker M, Kretzschmar HA, et al. (2009) A new subtype of frontotemporal lobar degeneration with FUS pathology. Brain 132: 2922-2931.
49. Yuva-Aydemir Y, Simkin A, Gascon E, Gao F-B, (2011) MicroRNA-9: functional evolution of a conserved small regulatory RNA. RNA Biol 8: 557-564.
50. Shibata M, Kurokawa D, Nakao H, Ohmura T, Aizawa S, (2008) MicroRNA-9 modulates Cajal-Retzius cell differentiation by suppressing Foxg1 expression in mouse medial pallium. J Neurosci 28: 10415-10421.
51. Xu XL, Zong R, Li Z, Biswas MH, Fang Z, et al. (2011) FXR1P but not FMRP regulates the levels of mammalian brain-specific microRNA-9 and microRNA-124. J Neurosci 13: 13705-13709.
52. Winton MJ, Van Deerlin VM, Kwong LK, Yuan W, Wood EM, et al. (2008) A90V TDP-43 variant results in the aberrant localization of TDP-43 in vitro. FEBS Lett 582: 2252-2256.
53. Chiang HH, Andersen PM, Tysnes OB, Gredal O, Christensen PB, et al. (2012) Novel TARDBP mutations in Nordic ALS patients. J Hum Genet 57: 316-319.
54. Lu Y, Ferris J, Gao FB, (2009) Frontotemporal dementia and amyotrophic lateral sclerosis-associated disease protein TDP-43 promotes dendritic branching. Mol Brain 2: 30.
55. Estes PS, Boehringer A, Zwick R, Tang JE, Grigsby B, et al. (2011) Wild-type and A315T mutant TDP-43 exert differential neurotoxicity in a Drosophila model of ALS. Hum Mol Genet 20: 2308-2321.
56. Buratti E, De Conti L, Stuani C, Romano M, Baralle M, et al. (2010) Nuclear factor TDP-43 can affect selected microRNA levels. FEBS J 277: 2268-2281.
57. Morlando M, Dini Modigliani S, Torrelli G, Rosa A, Di Carlo V, et al. (2012) FUS stimulates microRNA biogenesis by facilitating co-transcriptional Drosha recruitment. EMBO J 31: 4502-4510.
58. Sephton CF, Cenik C, Kucukural A, Dammer EB, Cenik B, et al. (2011) Identification of neuronal RNA targets of TDP-43-containing ribonucleoprotein complexes. J Biol Chem 286: 1204-1215.
59. Tollervey JR, Curk T, Rogelj B, Briese M, Cereda M, et al. (2011) Characterizing the RNA targets and position-dependent splicing regulation by TDP-43. Nat Neurosci 14: 452-458.