Increasing frataxin gene expression with histone deacetylase inhibitors as a therapeutic approach for Friedreich's ataxia

Journal of Neurochemistry

Volumn 126, Issue SUPPL.1, 2013, Pages 147-154

  Gottesfeld, Joel M ^a   Rusche, James R ^b   Pandolfo, Massimo ^c  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b REPLIGEN CORPORATION   (United States)

^c UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

Friedreich's ataxia; heterochromatin; histone deacetylase inhibitor; neurodegenerative disorder

Indexed keywords

2 AMINOBENZAMIDE; ADENINE; BML 210; CYTOSINE; ENTINOSTAT; FRATAXIN; GUANINE; HISTONE; HISTONE DEACETYLASE INHIBITOR; HYDROXAMIC ACID DERIVATIVE; RG 2833; THYMINE; TRICHOSTATIN A; UNCLASSIFIED DRUG; VORINOSTAT;

DRUG SAFETY; DRUG STRUCTURE; DRUG TARGETING; FRIEDREICH ATAXIA; FXN GENE; GENE; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC CODE; GENETIC TRANSCRIPTION; HETEROCHROMATIN; HUMAN; INTRON; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN PROCESSING; PROTEIN SYNTHESIS INHIBITION; REVIEW; SILENT GENE; STRUCTURE ANALYSIS; TRINUCLEOTIDE REPEAT;

FRIEDREICH'S ATAXIA; HETEROCHROMATIN; HISTONE DEACETYLASE INHIBITOR; NEURODEGENERATIVE DISORDER;

ANIMALS; CLINICAL TRIALS AS TOPIC; GENE EXPRESSION; GENE SILENCING; HETEROCHROMATIN; HISTONE DEACETYLASE INHIBITORS; HUMANS; IRON-BINDING PROTEINS; MICE; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84880354651     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12302     Document Type: Review

References (44)

1. 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.
2. Baralle M., Pastor T., Bussani E., and, Pagani F., (2008) Influence of Friedreich ataxia GAA noncoding repeat expansions on pre-mRNA processing. Am. J. Hum. Genet. 83, 77-88.
3. Beckers T., Burkhardt C., Wieland H., Gimmnich P., Ciossek T., Maier T., and, Sanders K., (2007) Distinct pharmacological properties of second generation HDAC inhibitors with the benzamide or hydroxamate head group. Int. J. Cancer 121, 1138-1148.
4. Bidichandani S. I., Ashizawa T., and, Patel P. I., (1998) The GAA triplet-repeat expansion in Friedreich ataxia interferes with transcription and may be associated with an unusual DNA structure. Am. J. Hum. Genet. 62, 111-121.
5. Bradner J. E., West N., Grachan M. L., Greenberg E. F., Haggarty S. J., Warnow T., and, Mazitschek R., (2010) Chemical phylogenetics of histone deacetylases. Nat. Chem. Biol. 6, 238-243.
6. Campuzano V., Montermini L., Moltò M. D., et al,. (1996) Friedreich's ataxia: autosomal recessive disease caused by an intronic GAA triplet repeat expansion. Science 271, 1423-1427.
7. Campuzano V., Montermini L., Lutz Y., et al,. (1997) Frataxin is reduced in Friedreich ataxia patients and is associated with mitochondrial membranes. Hum. Mol. Genet. 6, 1771-1780.
8. Chou C. J., Herman D., and, Gottesfeld J. M., (2008) Pimelic diphenylamide 106 is a slow, tight-binding inhibitor of class I histone deacetylases. J. Biol. Chem. 283, 35402-35409.
9. Cole P. A., (2008) Chemical probes for histone-modifying enzymes. Nat. Chem. Biol. 4, 590-597.
10. Cossée M., Dürr A., Schmitt M., et al,. (1999) Friedreich's ataxia: point mutations and clinical presentation of compound heterozygotes. Ann. Neurol. 45, 200-206.
11. De Biase I., Chutake Y. K., Rindler P. M., and, Bidichandani S. I., (2009) Epigenetic silencing in Friedreich ataxia is associated with depletion of CTCF (CCCTC-binding factor) and antisense transcription. PLoS ONE 4, e7914.
12. Di Prospero N. A., and, Fischbeck K. H., (2005) Therapeutics development for triplet repeat expansion diseases. Nat. Rev. Genet. 6, 756-765.
13. Festenstein R., (2006) Breaking the silence in Friedreich's ataxia. Nat. Chem. Biol. 2, 512-513.
14. Fleming J., Spinoulas A., Zheng M., Cunningham S. C., Ginn S. L., McQuilty R. C., Rowe P. B., and, Alexander I. E., (2005) Partial correction of sensitivity to oxidant stress in Friedreich ataxia patient fibroblasts by frataxin-encoding adeno-associated virus and lentivirus vectors. Hum. Gene Ther. 16, 947-956.
15. González-Cabo P., and, Palau F., (2012) Mitochondrial pathophysiology in Friedreich's ataxia. J. Neurochem. 126 (Suppl. 1), 53-64.
16. Grabczyk E., and, Usdin K., (2000a) Alleviating transcript insufficiency caused by Friedreich's ataxia triplet repeats. Nucleic Acids Res. 28, 4930-4937.
17. Grabczyk E., and, Usdin K., (2000b) The GAA*TTC triplet repeat expanded in Friedreich's ataxia impedes transcription elongation by T7 RNA polymerase in a length and supercoil dependent manner. Nucleic Acids Res. 28, 2815-2822.
18. Greene E., Mahishi L., Entezam A., Kumari D., and, Usdin K., (2007) Repeat-induced epigenetic changes in intron 1 of the frataxin gene and its consequences in Friedreich ataxia. Nucleic Acids Res. 35, 3383-3390.
19. Hebert M. D., and, Whittom A. A., (2007) Gene-based approaches toward Friedreich ataxia therapeutics. Cell. Mol. Life Sci. 64, 3034-3043.
20. 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.
21. Hu E., Dul E., Sung C.-M., et al,. (2003) Identification of novel isoform-selective inhibitors within class I histone deacetylases. J. Pharmacol. Exp. Ther. 307, 720-728.
22. Kazantsev A. G., and, Thompson L. M., (2008) Therapeutic application of histone deacetylase inhibitors for central nervous system disorders. Nat. Rev. Drug Discov. 7, 854-868.
23. Kim E., Napierala M., and, Dent S. Y. R., (2011) Hyperexpansion of GAA repeats affects post-initiation steps of FXN transcription in Friedreich's ataxia. Nucleic Acids Res. 39, 8366-8377.
24. Kumari D., Biacsi R. E., and, Usdin K., (2011) Repeat expansion affects both transcription initiation and elongation in friedreich ataxia cells. J. Biol. Chem. 286, 4209-4215.
25. Marks P. A., (2010) The clinical development of histone deacetylase inhibitors as targeted anticancer drugs. Expert Opin. Investig. Drugs 19, 1049-1066.
26. Methot J. L., Chakravarty P. K., Chenard M., et al,. (2008) Exploration of the internal cavity of histone deacetylase (HDAC) with selective HDAC1/HDAC2 inhibitors (SHI-1:2). Bioorg. Med. Chem. Lett. 18, 973-978.
27. Miranda C. J., Santos M. M., Ohshima K., et al,. (2002) Frataxin knockin mouse. FEBS Lett. 512, 291-297.
28. Ohshima K., Montermini L., Wells R. D., and, Pandolfo M., (1998) Inhibitory effects of expanded GAA.TTC triplet repeats from intron I of the Friedreich ataxia gene on transcription and replication in vivo. J. Biol. Chem. 273, 14588-14595.
29. Orr H. T., and, Zoghbi H. Y., (2007) Trinucleotide repeat disorders. Annu. Rev. Neurosci. 30, 575-621.
30. Pandolfo M., (2013) Treatment of Friedreich's ataxia. Expert Opinion on Orphan Drugs 1, 221-234.
31. Punga T., and, Bühler M., (2010) Long intronic GAA repeats causing Friedreich ataxia impede transcription elongation. EMBO Mol. Med. 2, 120-129.
32. Rai M., Soragni E., Jenssen K., Burnett R., Herman D., Coppola G., Geschwind D. H., Gottesfeld J. M., and, Pandolfo M., (2008) HDAC inhibitors correct frataxin deficiency in a Friedreich ataxia mouse model. PLoS ONE 3, e1958.
33. 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.
34. Rötig 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.
35. Rouault T. A., and, Tong W. H., (2008) Iron-sulfur cluster biogenesis and human disease. Trends Genet. 24, 398-407.
36. Sakamoto N., Chastain P. D., Parniewski P., Ohshima K., Pandolfo M., Griffith J. D., and, Wells R. D., (1999) Sticky DNA: self-association properties of long GAA.TTC repeats in R.R.Y triplex structures from Friedreich's ataxia. Mol. Cell 3, 465-475.
37. Sandi C., Pinto R. M., Al-Mahdawi S., Ezzatizadeh V., Barnes G., Jones S., Rusche J. R., Gottesfeld J. M., and, Pook M. A., (2011) Prolonged treatment with pimelic o-aminobenzamide HDAC inhibitors ameliorates the disease phenotype of a Friedreich ataxia mouse model. Neurobiol. Dis. 42, 496-505.
38. 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.
39. Siliphaivanh P., Harrington P., Witter D. J., et al,. (2007) Design of novel histone deacetylase inhibitors. Bioorg. Med. Chem. Lett. 17, 4619-4624.
40. Soragni E., Xu C., Plasterer H. L., Jacques V., Rusche J. R., and, Gottesfeld J. M., (2012) Rationale for the development of 2-aminobenzamide histone deacetylase inhibitors as therapeutics for friedreich ataxia. J. Child Neurol. 27, 1164-1173.
41. Tsai C.-L., and, Barondeau D. P., (2010) Human frataxin is an allosteric switch that activates the Fe-S cluster biosynthetic complex. Biochemistry 49, 9132-9139.
42. Vyas P. M., Tomamichel W. J., Pride P. M., Babbey C. M., Wang Q., Mercier J., Martin E. M., and, Payne R. M., (2012) A TAT-frataxin fusion protein increases lifespan and cardiac function in a conditional Friedreich's ataxia mouse model. Hum. Mol. Genet. 21, 1230-1247.
43. Wells R. D., (2008) DNA triplexes and Friedreich ataxia. FASEB J. 22, 1625-1634.
44. Xu C., Soragni E., Chou C. J., Herman D., Plasterer H. L., Rusche J. R., and, Gottesfeld J. M., (2009) Chemical probes identify a role for histone deacetylase 3 in Friedreich's ataxia gene silencing. Chem. Biol. 16, 980-989.