Cis-silencing of PIP5K1B evidenced in friedreich's ataxia patient cells results in cytoskeleton anomalies

Human Molecular Genetics

Volumn 22, Issue 14, 2013, Pages 2894-2904

  Bayot, Aurélien ^a   Reichman, Sacha ^b   Lebon, Sophie ^a   Csaba, Zsolt ^a   Aubry, Laetitia ^c   Sterkers, Ghislaine ^a   Husson, Isabelle ^a   Rak, Malgorzata ^a   Rustin, Pierre ^a  

^a HÔPITAL ROBERT DEBRÉ   (France)

^b INSERM   (France)

^c I Stem   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; FRATAXIN; PHOSPHATIDYLINOSITOL 4 PHOSPHATE;

ARTICLE; CELL MEMBRANE; CLINICAL ARTICLE; CYTOSKELETON; FIBROBLAST; FRIEDREICH ATAXIA; GENE; GENE OVEREXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; LYMPHOCYTE; NATURAL KILLER CELL; PHOSPHATIDYLINOSITOL 4 PHOSPHATE 5 KINASE BETA TYPE I GENE; PRIORITY JOURNAL;

CYTOSKELETON; FIBROBLASTS; FRIEDREICH ATAXIA; GENE SILENCING; HUMANS; IRON-BINDING PROTEINS; LYMPHOCYTES; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PHOSPHATIDYLINOSITOL PHOSPHATES; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); TRINUCLEOTIDE REPEAT EXPANSION;

EID: 84880323204     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt144     Document Type: Article

References (65)

1. Harding, A.E. (1981) Friedreich's ataxia: a clinical and genetic study of 90 families with an analysis of early diagnostic criteria and intrafamilial clustering of clinical features. Brain, 104, 589-620.
2. Pandolfo, M. (2009) Friedreich ataxia: the clinical picture. J. Neurol., 256 (Suppl. 1), 3-8.
3. Campuzano, V., Montermini, L., Molto, M.D., Pianese, L., Cossee, M., Cavalcanti, F., Monros, E., Rodius, F., Duclos, F., Monticelli, A. et al. (1996) Friedreich's ataxia: autosomal recessive disease caused by an intronic GAA triplet repeat expansion. Science, 271, 1423-1427.
4. Kumari, D. and Usdin, K. (2012) Is Friedreich ataxia an epigenetic disorder? Clin. Epigenetics, 4, 2.
5. Saveliev, A., Everett, C., Sharpe, T., Webster, Z. and Festenstein, R. (2003) DNA triplet repeats mediate heterochromatin-protein-1-sensitive variegated gene silencing. Nature, 422, 909-913.
6. Evans-Galea, M.V., Carrodus, N., Rowley, S.M., Corben, L.A., Tai, G., Saffery, R., Galati, J.C., Wong, N.C., Craig, J.M., Lynch, D.R. et al. (2012) FXN methylation predicts expression and clinical outcome in Friedreich ataxia. Ann. Neurol., 71, 487-497.
7. Herman, D., Jenssen, K., Burnett, R., Soragni, E., Perlman, S.L. and Gottesfeld, J.M. (2006) Histone deacetylase inhibitors reverse gene silencing in Friedreich's ataxia. Nat. Chem. Biol., 2, 551-558.
8. Al-Mahdawi, S., Pinto, R.M., Ismail, O., Varshney, D., Lymperi, S., Sandi, C., Trabzuni, D. and Pook, M. (2008) The Friedreich ataxia GAA repeat expansion mutation induces comparable epigenetic changes in human and transgenic mouse brain and heart tissues. Hum. Mol. Genet., 17, 735-746.
9. Rai, M., Soragni, E., Chou, C.J., Barnes, G., Jones, S., Rusche, J.R., Gottesfeld, J.M. and Pandolfo, M. (2010) Two new pimelic diphenylamide HDAC inhibitors induce sustained frataxin upregulation in cells from Friedreich's ataxia patients and in a mouse model. PLoS One, 5, e8825.
10. Rotig, A., de Lonlay, P., Chretien, D., Foury, F., Koenig, M., Sidi, D., Munnich, A. and Rustin, P. (1997) Aconitase and mitochondrial iron-sulphur protein deficiency in Friedreich ataxia. Nat. Genet., 17, 215-217.
11. Gerber, J., Muhlenhoff, U. and Lill, R. (2003) An interaction between frataxin and Isu1/Nfs1 that is crucial for Fe/S cluster synthesis on Isu1. EMBO Rep., 4, 906-911.
12. Puccio, H., Simon, D., Cossee, M., Criqui-Filipe, P., Tiziano, F., Melki, J., Hindelang, C., Matyas, R., Rustin, P. and Koenig, M. (2001) Mouse models for Friedreich ataxia exhibit cardiomyopathy, sensory nerve defect and Fe-S enzyme deficiency followed by intramitochondrial iron deposits. Nat. Genet., 27, 181-186.
13. Bayot, A., Santos, R., Camadro, J.M. and Rustin, P. (2011) Friedreich's ataxia: the vicious circle hypothesis revisited. BMC Med., 9, 112.
14. Marmolino, D. (2011) Friedreich's ataxia: past, present and future. Brain Res. Rev., 67, 311-330.
15. Vaubel, R.A. and Isaya, G. (2012) Iron-sulfur cluster synthesis, iron homeostasis and oxidative stress in Friedreich ataxia. Mol. Cell Neurosci 55, 50-61.
16. Pastore, A., Tozzi, G., Gaeta, L.M., Bertini, E., Serafini, V., Di Cesare, S., Bonetto, V., Casoni, F., Carrozzo, R., Federici, G. et al. (2003) Actin glutathionylation increases in fibroblasts of patients with Friedreich's ataxia: a potential role in the pathogenesis of the disease. J. Biol. Chem., 278, 42588-42595.
17. Sparaco, M., Gaeta, L.M., Santorelli, F.M., Passarelli, C., Tozzi, G., Bertini, E., Simonati, A., Scaravilli, F., Taroni, F., Duyckaerts, C. et al. (2009) Friedreich's ataxia: oxidative stress and cytoskeletal abnormalities. J. Neurol. Sci., 287, 111-118.
18. Klesert, T.R., Otten, A.D., Bird, T.D. and Tapscott, S.J. (1997) Trinucleotide repeat expansion at the myotonic dystrophy locus reduces expression of DMAHP. Nat. Genet., 16, 402-406.
19. Thornton, C.A., Wymer, J.P., Simmons, Z., McClain, C. and Moxley, R.T., III (1997) Expansion of the myotonic dystrophy CTG repeat reduces expression of the flanking DMAHP gene. Nat. Genet., 16, 407-409.
20. van den Bout, I. and Divecha, N. (2009) PIP5K-driven PtdIns(4,5)P2 synthesis: regulation and cellular functions. J. Cell Sci., 122, 3837-3850.
21. Vicinanza, M., D'Angelo, G., Di Campli, A. and De Matteis, M.A. (2008) Function and dysfunction of the PI system in membrane trafficking. EMBO J., 27, 2457-2470.
22. Paupe, V., Dassa, E.P., Goncalves, S., Auchere, F., Lonn, M., Holmgren, A. and Rustin, P. (2009) Impaired nuclear Nrf2 translocation undermines the oxidative stress response in Friedreich ataxia. PLoS One, 4, e4253.
23. Di Paolo, G. and De Camilli, P. (2006) Phosphoinositides in cell regulation and membrane dynamics. Nature, 443, 651-657.
24. Saarikangas, J., Zhao, H. and Lappalainen, P. (2010) Regulation of the actin cytoskeleton-plasma membrane interplay by phosphoinositides. Physiol. Rev., 90, 259-289.
25. Oude Weernink, P.A., Schmidt, M. and Jakobs, K.H. (2004) Regulation and cellular roles of phosphoinositide 5-kinases. Eur. J. Pharmacol., 500, 87-99.
26. Weernink, P.A., Meletiadis, K., Hommeltenberg, S., Hinz, M., Ishihara, H., Schmidt, M. and Jakobs, K.H. (2004) Activation of type I phosphatidylinositol 4-phosphate 5-kinase isoforms by the Rho GTPases, RhoA, Rac1, and Cdc42. J. Biol. Chem., 279, 7840-7849.
27. Parsons, J.T., Horwitz, A.R. and Schwartz, M.A. (2010) Cell adhesion: integrating cytoskeletal dynamics and cellular tension. Nat. Rev. Mol. Cell Biol., 11, 633-643.
28. Zimerman, B., Volberg, T. and Geiger, B. (2004) Early molecular events in the assembly of the focal adhesion-stress fiber complex during fibroblast spreading. Cell Motil. Cytoskeleton, 58, 143-159.
29. Ling, K., Schill, N.J., Wagoner, M.P., Sun, Y. and Anderson, R.A. (2006) Movin' on up: the role of PtdIns(4,5)P(2) in cell migration. Trends Cell Biol., 16, 276-284.
30. Carvajal, J.J., Pook, M.A., dos Santos, M., Doudney, K., Hillermann, R., Minogue, S., Williamson, R., Hsuan, J.J. and Chamberlain, S. (1996) The Friedreich's ataxia gene encodes a novel phosphatidylinositol-4-phosphate 5-kinase. Nat. Genet., 14, 157-162.
31. Carvajal, J.J., Pook, M.A., Doudney, K., Hillermann, R., Wilkes, D., al-Mahdawi, S., Williamson, R. and Chamberlain, S. (1995) Friedreich's ataxia: a defect in signal transduction? Hum. Mol. Genet., 4, 1411-1419.
32. Deng, W. and Blobel, G.A. (2010) Do chromatin loops provide epigenetic gene expression states? Curr. Opin. Genet. Dev., 20, 548-554.
33. Talbert, P.B. and Henikoff, S. (2006) Spreading of silent chromatin: inaction at a distance. Nat. Rev. Genet., 7, 793-803.
34. Coon, B.G., Mukherjee, D., Hanna, C.B., Riese, D.J. II, Lowe, M. and Aguilar, R.C. (2009) Lowe syndrome patient fibroblasts display Ocrl1-specific cell migration defects that cannot be rescued by the homologous Inpp5b phosphatase. Hum. Mol. Genet., 18, 4478-4491.
35. Suchy, S.F. and Nussbaum, R.L. (2002) The deficiency of PIP2 5-phosphatase in Lowe syndrome affects actin polymerization. Am. J. Hum. Genet., 71, 1420-1427.
36. Chao, W.T., Ashcroft, F., Daquinag, A.C., Vadakkan, T., Wei, Z., Zhang, P., Dickinson, M.E. and Kunz, J. (2010) Type I phosphatidylinositol phosphate kinase beta regulates focal adhesion disassembly by promoting beta1 integrin endocytosis. Mol. Cell Biol., 30, 4463-4479.
37. Halstead, J.R., Savaskan, N.E., van den Bout, I., Van Horck, F., Hajdo-Milasinovic, A., Snell, M., Keune, W.J., Ten Klooster, J.P., Hordijk, P.L. and Divecha, N. (2010) Rac controls PIP5K localisation and PtdIns(4,5)P(2) synthesis, which modulates vinculin localisation and neurite dynamics. J. Cell Sci., 123, 3535-3546.
38. Hotulainen, P. and Lappalainen, P. (2006) Stress fibers are generated by two distinct actin assembly mechanisms in motile cells. J. Cell Biol., 173, 383-394.
39. Endlich, N., Otey, C.A., Kriz, W. and Endlich, K. (2007) Movement of stress fibers away from focal adhesions identifies focal adhesions as sites of stress fiber assembly in stationary cells. Cell Motil. Cytoskeleton, 64, 966-976.
40. Kleinjan, D.A. and van Heyningen, V. (2005) Long-range control of gene expression: emerging mechanisms and disruption in disease. Am. J. Hum. Genet., 76, 8-32.
41. Kleinjan, D.J. and Coutinho, P. (2009) Cis-ruption mechanisms: disruption of cis-regulatory control as a cause of human genetic disease. Brief Funct. Genomic Proteomic, 8, 317-332.
42. Rouault, T.A. (2012) Biogenesis of iron-sulfur clusters in mammalian cells: new insights and relevance to human disease. Dis. Models Mech., 5, 155-164.
43. Lacalle, R.A., Peregil, R.M., Albar, J.P., Merino, E., Martinez, A.C., Merida, I. and Manes, S. (2007) Type I phosphatidylinositol 4-phosphate 5-kinase controls neutrophil polarity and directional movement. J. Cell Biol., 179, 1539-1553.
44. Sasaki, J., Sasaki, T., Yamazaki, M., Matsuoka, K., Taya, C., Shitara, H., Takasuga, S., Nishio, M., Mizuno, K., Wada, T. et al. (2005) Regulation of anaphylactic responses by phosphatidylinositol phosphate kinase type I {alpha}. J. Exp. Med., 201, 859-870.
45. Draper, P., Huang, Y.S., Shapcott, D., Lemieux, B., Brennan, M., Barbeau, A. and Davignon, J. (1979) Erythrocyte membrane lipids in Friedreich's ataxia. Can. J. Neurol. Sci., 6, 291-294.
46. Filla, A., Postiglione, A., Rubba, P., Patti, L., De Michele, G., Palma, V., Brescia Morra, V. and Campanella, G. (1980) Plasma lipoprotein concentration and erythrocyte membrane lipids in patients with Friedreich's ataxia. Acta Neurol. (Napoli), 2, 382-389.
47. Coppola, G., Burnett, R., Perlman, S., Versano, R., Gao, F., Plasterer, H., Rai, M., Sacca, F., Filla, A., Lynch, D.R. et al. (2011) A gene expression phenotype in lymphocytes from Friedreich ataxia patients. Ann. Neurol., 70, 790-804.
48. Coppola, G., Marmolino, D., Lu, D., Wang, Q., Cnop, M., Rai, M., Acquaviva, F., Cocozza, S., Pandolfo, M. and Geschwind, D.H. (2009) Functional genomic analysis of frataxin deficiency reveals tissue-specific alterations and identifies the PPARgamma pathway as a therapeutic target in Friedreich's ataxia. Hum. Mol. Genet., 18, 2452-2461.
49. Navarro, J.A., Ohmann, E., Sanchez, D., Botella, J.A., Liebisch, G., Molto, M.D., Ganfornina, M.D., Schmitz, G. and Schneuwly, S. (2010) Altered lipid metabolism in a Drosophila model of Friedreich's ataxia. Hum. Mol. Genet., 19, 2828-2840.
50. Selak, M.A., Lyver, E., Micklow, E., Deutsch, E.C., Onder, O., Selamoglu, N., Yager, C., Knight, S., Carroll, M., Daldal, F. et al. (2010) Blood cells from Friedreich ataxia patients harbor frataxin deficiency without a loss of mitochondrial function. Mitochondrion, 11, 342-350.
51. Eder, K., Kish, S.J., Kirchgessner, M. and Ross, B.M. (1998) Brain phospholipids and fatty acids in Friedreich's ataxia and spinocerebellar atrophy type-1. Mov. Disord., 13, 813-819.
52. Ross, B.M., Eder, K., Moszczynska, A., Mamalias, N., Lamarche, J., Ang, L., Pandolfo, M., Rouleau, G., Kirchgessner, M. and Kish, S.J. (2000) Abnormal activity of membrane phospholipid synthetic enzymes in the brain of patients with Friedreich's ataxia and spinocerebellar atrophy type-1. Mov. Disord., 15, 294-300.
53. Volpicelli-Daley, L.A., Lucast, L., Gong, L.W., Liu, L., Sasaki, J., Sasaki, T., Abrams, C.S., Kanaho, Y. and De Camilli, P. (2010) Phosphatidylinositol-4-phosphate 5-kinases and phosphatidylinositol 4,5-bisphosphate synthesis in the brain. J. Biol. Chem., 285, 28708-28714.
54. van Horck, F.P., Lavazais, E., Eickholt, B.J., Moolenaar, W.H. and Divecha, N. (2002) Essential role of type I(alpha) phosphatidylinositol 4-phosphate 5-kinase in neurite remodeling. Curr. Biol., 12, 241-245.
55. Yamazaki, M., Miyazaki, H., Watanabe, H., Sasaki, T., Maehama, T., Frohman, M.A. and Kanaho, Y. (2002) Phosphatidylinositol 4-phosphate 5-kinase is essential for ROCK-mediated neurite remodeling. J. Biol. Chem., 277, 17226-17230.
56. Hernandez-Deviez, D.J., Roth, M.G., Casanova, J.E. and Wilson, J.M. (2004) ARNO and ARF6 regulate axonal elongation and branching through downstream activation of phosphatidylinositol 4-phosphate 5-kinase alpha. Mol. Biol. Cell, 15, 111-120.
57. Di Paolo, G., Moskowitz, H.S., Gipson, K., Wenk, M.R., Voronov, S., Obayashi, M., Flavell, R., Fitzsimonds, R.M., Ryan, T.A. and De Camilli, P. (2004) Impaired PtdIns(4,5)P2 synthesis in nerve terminals produces defects in synaptic vesicle trafficking. Nature, 431, 415-422.
58. Huang, P., Yeku, O., Zong, H., Tsang, P., Su, W., Yu, X., Teng, S., Osisami, M., Kanaho, Y., Pessin, J.E. et al. (2011) Phosphatidylinositol-4-phosphate-5-kinase alpha deficiency alters dynamics of glucose-stimulated insulin release to improve glucohomeostasis and decrease obesity in mice. Diabetes, 60, 454-463.
59. Wang, Y., Lian, L., Golden, J.A., Morrisey, E.E. and Abrams, C.S. (2007) PIP5KI gamma is required for cardiovascular and neuronal development. Proc. Natl Acad. Sci. USA, 104, 11748-11753.
60. Narkis, G., Ofir, R., Landau, D., Manor, E., Volokita, M., Hershkowitz, R., Elbedour, K. and Birk, O.S. (2007) Lethal contractural syndrome type 3 (LCCS3) is caused by a mutation in PIP5K1C, which encodes PIPKI gamma of the phophatidylinsitol pathway. Am. J. Hum. Genet., 81, 530-539.
61. Cossee, M., Durr, A., Schmitt, M., Dahl, N., Trouillas, P., Allinson, P., Kostrzewa, M., Nivelon-Chevallier, A., Gustavson, K.H., Kohlschutter, A. et al. (1999) Friedreich's ataxia: point mutations and clinical presentation of compound heterozygotes. Ann. Neurol., 45, 200-206.
62. De Michele, G., Filla, A., Cavalcanti, F., Tammaro, A., Monticelli, A., Pianese, L., Di Salle, F., Perreti, A., Santoro, L., Caruso, G. et al. (2000) Atypical Friedreich ataxia phenotype associated with a novel missense mutation in the X25 gene. Neurology, 54, 496-499.
63. Lynch, D.R., Deutsch, E.C., Wilson, R.B. and Tennekoon, G. (2012) Unanswered questions in Friedreich ataxia. J. Child Neurol., 27, 1223-1229.
64. Ku, S., Soragni, E., Campau, E., Thomas, E.A., Altun, G., Laurent, L.C., Loring, J.F., Napierala, M. and Gottesfeld, J.M. (2010) Friedreich's ataxia induced pluripotent stem cells model intergenerational GAATTC triplet repeat instability. Cell Stem Cell, 7, 631-637.
65. Wieckowski, M.R., Giorgi, C., Lebiedzinska, M., Duszynski, J. and Pinton, P. (2009) Isolation of mitochondria-associated membranes and mitochondria from animal tissues and cells. Nat. Protoc., 4, 1582-1590.