Early transcriptional changes linked to naturally occurring Huntington's disease mutations in neural derivatives of human embryonic stem cells

Human Molecular Genetics

Volumn 21, Issue 17, 2012, Pages 3883-3895

  Feyeux, Maxime ^a   Bourgois Rocha, Fany ^a   Redfern, Amanda ^b   Giles, Peter ^c   Lefort, Nathalie ^a   Aubert, Sophie ^a   Bonnefond, Caroline ^a   Bugi, Aurore ^a   Ruiz, Marta ^d,e   Deglon, Nicole ^d,e   Jones, Lesley ^c   Peschanski, Marc ^a   Allen, Nicholas D ^b   Perrier, Anselme L ^a  

^a I Stem   (France)

^b CARDIFF UNIVERSITY   (United Kingdom)

^c CARDIFF UNIVERSITY   (United Kingdom)

^d DIF   (France)

^e SERVICE HOSPITALIER FRÉDÉRIC JOLIOT   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; CHCHD2 PROTEIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; HUNTINGTIN; PKIB PROTEIN; TRIM4 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BLASTOCYST; DOWN REGULATION; EMBRYO; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; GAIN OF FUNCTION MUTATION; GENE EXPRESSION; GENE MUTATION; HUMAN; HUMAN CELL; HUNTINGTON CHOREA; LOSS OF FUNCTION MUTATION; MITOCHONDRION; MOLECULAR DIAGNOSIS; PREIMPLANTATION EMBRYO; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; TRANSCRIPTOMICS; WILD TYPE;

CELL LINE; EMBRYONIC STEM CELLS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; HUNTINGTON DISEASE; MODELS, BIOLOGICAL; MUTATION; NERVE TISSUE PROTEINS; NEURAL STEM CELLS; NEURONS; REPRODUCIBILITY OF RESULTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSCRIPTION, GENETIC; TRANSCRIPTOME;

EID: 84864601973     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/dds216     Document Type: Article

References (55)

1. Maury, Y., Gauthier, M., Peschanski, M. and Martinat, C. (2012) Human pluripotent stem cells for disease modelling and drug screening. Bioessays, 34, 61-71.
2. Lee, G., Papapetrou, E.P., Kim, H., Chambers, S.M., Tomishima, M.J., Fasano, C.A., Ganat, Y.M., Menon, J., Shimizu, F., Viale, A. et al. (2009) Modelling pathogenesis and treatment of familial dysautonomia using patient-specific iPSCs. Nature, 461, 402-406.
3. Zhang, J., Lian, Q., Zhu, G., Zhou, F., Sui, L., Tan, C., Mutalif, R.A., Navasankari, R., Zhang, Y., Tse, H.F. et al. (2011) A human iPSC model of Hutchinson Gilford Progeria reveals vascular smooth muscle and mesenchymal stem cell defects. Cell Stem Cell, 8, 31-45.
4. Ebert, A.D., Yu, J., Rose, F.F. Jr, Mattis, V.B., Lorson, C.L., Thomson, J.A. and Svendsen, C.N. (2009) Induced pluripotent stem cells from a spinal muscular atrophy patient. Nature, 457, 277-280.
5. Carvajal-Vergara, X., Sevilla, A., D'Souza, S.L., Ang, Y.S., Schaniel, C., Lee, D.F., Yang, L., Kaplan, A.D., Adler, E.D., Rozov, R. et al. (2010) Patient-specific induced pluripotent stem-cell-derived models of LEOPARD syndrome. Nature, 465, 808-812.
6. Nasir, J., Floresco, S.B., O'Kusky, J.R., Diewert, V.M., Richman, J.M., Zeisler, J., Borowski, A., Marth, J.D., Phillips, A.G. and Hayden, M.R. (1995) Targeted disruption of the Huntington's disease gene results in embryonic lethality and behavioral and morphological changes in heterozygotes. Cell, 81, 811-823.
7. Godin, J.D., Colombo, K., Molina-Calavita, M., Keryer, G., Zala, D., Charrin, B.C., Dietrich, P., Volvert, M.L., Guillemot, F., Dragatsis, I. et al. (2010) Huntingtin is required for mitotic spindle orientation and mammalian neurogenesis. Neuron, 67, 392-406.
8. DiFiglia, M., Sapp, E., Chase, K., Schwarz, C., Meloni, A., Young, C., Martin, E., Vonsattel, J.P., Carraway, R., Reeves, S.A. et al. (1995) Huntingtin is a cytoplasmic protein associated with vesicles in human and rat brain neurons. Neuron, 14, 1075-1081.
9. Ross, C.A. and Tabrizi, S.J. (2011) Huntington's disease: from molecular pathogenesis to clinical treatment. Lancet Neurol., 10, 83-98.
10. Zuccato, C., Valenza, M. and Cattaneo, E. (2010) Molecular mechanisms and potential therapeutical targets in Huntington's disease. Physiol. Rev., 90, 905-981.
11. Cha, J.H. (2007) Transcriptional signatures in Huntington's disease. Prog. Neurobiol., 83, 228-248.
12. Sugars, K.L. and Rubinsztein, D.C. (2003) Transcriptional abnormalities in Huntington disease. Trends Genet., 19, 233-238.
13. Verlinsky, Y., Strelchenko, N., Kukharenko, V., Rechitsky, S., Verlinsky, O., Galat, V. and Kuliev, A. (2005) Human embryonic stem cell lines with genetic disorders. Reprod. Biomed. Online, 10, 105-110.
14. Mateizel, I., De Temmerman, N., Ullmann, U., Cauffman, G., Sermon, K., Van de Velde, H., De Rycke, M., Degreef, E., Devroey, P., Liebaers, I. et al. (2006) Derivation of human embryonic stem cell lines from embryos obtained after IVF and after PGD for monogenic disorders. Hum. Reprod., 21, 503-511.
15. Tropel, P., Tournois, J., Come, J., Varela, C., Moutou, C., Fragner, P., Cailleret, M., Laabi, Y., Peschanski, M. and Viville, S. (2010) High-efficiency derivation of human embryonic stem cell lines following pre-implantation genetic diagnosis. In Vitro Cell Dev. Biol. Anim., 46, 376-385.
16. Bradley, C.K., Scott, H.A., Chami, O., Peura, T.T., Dumevska, B., Schmidt, U. and Stojanov, T. (2011) Derivation of Huntington's disease-affected human embryonic stem cell lines. Stem Cells Dev., 20, 495-502.
17. Hodges, A., Strand, A.D., Aragaki, A.K., Kuhn, A., Sengstag, T., Hughes, G., Elliston, L.A., Hartog, C., Goldstein, D.R., Thu, D. et al. (2006) Regional and cellular gene expression changes in human Huntington's disease brain. Hum. Mol. Genet., 15, 965-977.
18. de Almeida, L.P., Ross, C.A., Zala, D., Aebischer, P. and Deglon, N. (2002) Lentiviral-mediated delivery of mutant huntingtin in the striatum of rats induces a selective neuropathology modulated by polyglutamine repeat size, huntingtin expression levels, and protein length. J. Neurosci., 22, 3473-3483.
19. Chaturvedi, R.K., Adhihetty, P., Shukla, S., Hennessy, T., Calingasan, N., Yang, L., Starkov, A., Kiaei, M., Cannella, M., Sassone, J. et al. (2009) Impaired PGC-1alpha function in muscle in Huntington's disease. Hum. Mol. Genet., 18, 3048-3065.
20. Chaturvedi, R.K., Calingasan, N.Y., Yang, L., Hennessey, T., Johri, A. and Beal, M.F. (2010) Impairment of PGC-1alpha expression, neuropathology and hepatic steatosis in a transgenic mouse model of Huntington's disease following chronic energy deprivation. Hum. Mol. Genet., 19, 3190-3205.
21. Wexler, N.S., Lorimer, J., Porter, J., Gomez, F., Moskowitz, C., Shackell, E., Marder, K., Penchaszadeh, G., Roberts, S.A., Gayan, J. et al. (2004) Venezuelan kindreds reveal that genetic and environmental factors modulate Huntington's disease age of onset. Proc. Natl Acad. Sci. USA, 101, 3498-3503.
22. Kuhn, A., Goldstein, D.R., Hodges, A., Strand, A.D., Sengstag, T., Kooperberg, C., Becanovic, K., Pouladi, M.A., Sathasivam, K., Cha, J.H. et al. (2007) Mutant huntingtin's effects on striatal gene expression in mice recapitulate changes observed in human Huntington's disease brain and do not differ with mutant huntingtin length or wild-type huntingtin dosage. Hum. Mol. Genet., 16, 1845-1861.
23. Runne, H., Kuhn, A., Wild, E.J., Pratyaksha, W., Kristiansen, M., Isaacs, J.D., Regulier, E., Delorenzi, M., Tabrizi, S.J. and Luthi-Carter, R. (2007) Analysis of potential transcriptomic biomarkers for Huntington's disease in peripheral blood. Proc. Natl Acad. Sci. USA, 104, 14424-14429.
24. Klinglmueller, F., Tuechler, T. and Posch, M. (2011) Cross-platform comparison of microarray data using order restricted inference. Bioinformatics, 27, 953-960.
25. Kuhn, A., Thu, D., Waldvogel, H.J., Faull, R.L. and Luthi-Carter, R. (2011) Population-specific expression analysis (PSEA) reveals molecular changes in diseased brain. Nat. Methods, 8, 945-947.
26. Becanovic, K., Pouladi, M.A., Lim, R.S., Kuhn, A., Pavlidis, P., Luthi-Carter, R., Hayden, M.R. and Leavitt, B.R. (2010) Transcriptional changes in Huntington disease identified using genome-wide expression profiling and cross-platform analysis. Hum. Mol. Genet, 19, 1438-1452.
27. Giles, P., Elliston, L., Higgs, G.V., Brooks, S.P., Dunnett, S.B. and Jonesa, L. (2011) Longitudinal analysis of gene expression and behaviour in the HdhQ150 mouse model of Huntington's disease. Brain Res. Bull., 88, 199-209.
28. Borovecki, F., Lovrecic, L., Zhou, J., Jeong, H., Then, F., Rosas, H.D., Hersch, S.M., Hogarth, P., Bouzou, B., Jensen, R.V. et al. (2005) Genome-wide expression profiling of human blood reveals biomarkers for Huntington's disease. Proc. Natl Acad. Sci. USA, 102, 11023-11028.
29. Runne, H., Regulier, E., Kuhn, A., Zala, D., Gokce, O., Perrin, V., Sick, B., Aebischer, P., Deglon, N. and Luthi-Carter, R. (2008) Dysregulation of gene expression in primary neuron models of Huntington's disease shows that polyglutamine-related effects on the striatal transcriptome may not be dependent on brain circuitry. J. Neurosci., 28, 9723-9731.
30. Scherzer, C.R., Eklund, A.C., Morse, L.J., Liao, Z., Locascio, J.J., Fefer, D., Schwarzschild, M.A., Schlossmacher, M.G., Hauser, M.A., Vance, J.M. et al. (2007) Molecular markers of early Parkinson's disease based on gene expression in blood. Proc. Natl Acad. Sci. USA, 104, 955-960.
31. Wyttenbach, A., Swartz, J., Kita, H., Thykjaer, T., Carmichael, J., Bradley, J., Brown, R., Maxwell, M., Schapira, A., Orntoft, T.F. et al. (2001) Polyglutamine expansions cause decreased CRE-mediated transcription and early gene expression changes prior to cell death in an inducible cell model of Huntington's disease. Hum. Mol. Genet., 10, 1829-1845.
32. Sipione, S., Rigamonti, D., Valenza, M., Zuccato, C., Conti, L., Pritchard, J., Kooperberg, C., Olson, J.M. and Cattaneo, E. (2002) Early transcriptional profiles in huntingtin-inducible striatal cells by microarray analyses. Hum. Mol. Genet., 11, 1953-1965.
33. Kita, H., Carmichael, J., Swartz, J., Muro, S., Wyttenbach, A., Matsubara, K., Rubinsztein, D.C. and Kato, K. (2002) Modulation of polyglutamine-induced cell death by genes identified by expression profiling. Hum. Mol. Genet., 11, 2279-2287.
34. Sugars, K.L., Brown, R., Cook, L.J., Swartz, J. and Rubinsztein, D.C. (2004) Decreased cAMP response element-mediated transcription: an early event in exon 1 and full-length cell models of Huntington's disease that contributes to polyglutamine pathogenesis. J. Biol. Chem., 279, 4988-4999.
35. Apostol, B.L., Illes, K., Pallos, J., Bodai, L., Wu, J., Strand, A., Schweitzer, E.S., Olson, J.M., Kazantsev, A., Marsh, J.L. et al. (2006) Mutant huntingtin alters MAPK signaling pathways in PC12 and striatal cells: ERK1/2 protects against mutant huntingtin-associated toxicity. Hum. Mol. Genet., 15, 273-285.
36. Maes, O.C., Xu, S., Yu, B., Chertkow, H.M., Wang, E. and Schipper, H.M. (2007) Transcriptional profiling of Alzheimer blood mononuclear cells by microarray. Neurobiol. Aging, 28, 1795-1809.
37. Jacobsen, J.C., Gregory, G.C., Woda, J.M., Thompson, M.N., Coser, K.R., Murthy, V., Kohane, I.S., Gusella, J.F., Seong, I.S., MacDonald, M.E. et al. (2011) HD CAG-correlated gene expression changes support a simple dominant gain of function. Hum. Mol. Genet., 20, 2846-2860.
38. Puigserver, P. and Spiegelman, B.M. (2003) Peroxisome proliferator-activated receptor-gamma coactivator 1 alpha (PGC-1 alpha): transcriptional coactivator and metabolic regulator. Endocr. Rev., 24, 78-90.
39. Cui, L., Jeong, H., Borovecki, F., Parkhurst, C.N., Tanese, N. and Krainc, D. (2006) Transcriptional repression of PGC-1alpha by mutant huntingtin leads to mitochondrial dysfunction and neurodegeneration. Cell, 127, 59-69.
40. Kaltenbach, L.S., Romero, E., Becklin, R.R., Chettier, R., Bell, R., Phansalkar, A., Strand, A., Torcassi, C., Savage, J., Hurlburt, A. et al. (2007) Huntingtin interacting proteins are genetic modifiers of neurodegeneration. PLoS Genet., 3, e82.
41. Damiano, M., Galvan, L., Deglon, N. and Brouillet, E. (2010) Mitochondria in Huntington's disease. Biochim. Biophys. Acta, 1802, 52-61.
42. Baughman, J.M., Nilsson, R., Gohil, V.M., Arlow, D.H., Gauhar, Z. and Mootha, V.K. (2009) A computational screen for regulators of oxidative phosphorylation implicates SLIRP in mitochondrial RNA homeostasis. PLoS Genet., 5, e1000590.
43. Jiang, M., Wang, J., Fu, J., Du, L., Jeong, H., West, T., Xiang, L., Peng, Q., Hou, Z., Cai, H. et al. (2012) Neuroprotective role of Sirt1 in mammalian models of Huntington's disease through activation of multiple Sirt1 targets. Nat. Med., 18, 153-158.
44. Jeong, H., Cohen, D.E., Cui, L., Supinski, A., Savas, J.N., Mazzulli, J.R., Yates, J.R. 3rd, Bordone, L., Guarente, L. and Krainc, D. (2012) Sirt1 mediates neuroprotection from mutant huntingtin by activation of the TORC1 and CREB transcriptional pathway. Nat. Med., 18, 159-165.
45. Law, I.K., Liu, L., Xu, A., Lam, K.S., Vanhoutte, P.M., Che, C.M., Leung, P.T. and Wang, Y. (2009) Identification and characterization of proteins interacting with SIRT1 and SIRT3: implications in the anti-aging and metabolic effects of sirtuins. Proteomics, 9, 2444-2456.
46. Colin, E., Regulier, E., Perrin, V., Durr, A., Brice, A., Aebischer, P., Deglon, N., Humbert, S. and Saudou, F. (2005) Akt is altered in an animal model of Huntington's disease and in patients. Eur. J. Neurosci., 21, 1478-1488.
47. Seo, M., Lee, W.H. and Suk, K. (2010) Identification of novel cell migration-promoting genes by a functional genetic screen. FASEB J., 24, 464-478.
48. Gauthier, L.R., Charrin, B.C., Borrell-Pages, M., Dompierre, J.P., Rangone, H., Cordelieres, F.P., De Mey, J., MacDonald, M.E., Lessmann, V., Humbert, S. et al. (2004) Huntingtin controls neurotrophic support and survival of neurons by enhancing BDNF vesicular transport along microtubules. Cell, 118, 127-138.
49. Yu, J., Yu, L., Chen, Z., Zheng, L., Chen, X., Wang, X., Ren, D. and Zhao, S. (2002) Protein inhibitor of neuronal nitric oxide synthase interacts with protein kinase A inhibitors. Brain Res. Mol. Brain Res., 99, 145-149.
50. Kasyapa, C., Gu, T.L., Nagarajan, L., Polakiewicz, R. and Cowell, J.K. (2009) Phosphorylation of the SSBP2 and ABL proteins by the ZNF198-FGFR1 fusion kinase seen in atypical myeloproliferative disorders as revealed by phosphopeptide-specific MS. Proteomics, 9, 3979-3988.
51. Zhai, G., Teumer, A., Stolk, L., Perry, J.R., Vandenput, L., Coviello, A.D., Koster, A., Bell, J.T., Bhasin, S., Eriksson, J. et al. (2011) Eight common genetic variants associated with serum DHEAS levels suggest a key role in ageing mechanisms. PLoS Genet., 7, e1002025.
52. Chambers, S.M., Fasano, C.A., Papapetrou, E.P., Tomishima, M., Sadelain, M. and Studer, L. (2009) Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat. Biotechnol., 27, 275-280.
53. Benchoua, A., Aubry, L. and Perrier, A.L. (2008) Method and medium for neural differentiation of pluripotent cells. doi:10.06.2010; 05.12.2008WO/2010/063848.
54. Johnson, W.E., Rabinovic, A. and Li, C. (2007) Adjusting batch effects in microarray expression data using Empirical Bayes methods. Biostatistics, 8, 118-127.
55. Perrin, V., Regulier, E., Abbas-Terki, T., Hassig, R., Brouillet, E., Aebischer, P., Luthi-Carter, R. and Déglon, N. (2007) Neuroprotection by Hsp104 and Hsp27 in lentiviral-based rat models of Huntington's disease. N. Mol. Ther., PMID: 17375066.