Rationale for the development of 2-aminobenzamide histone deacetylase inhibitors as therapeutics for Friedreich ataxia

Journal of Child Neurology

Volumn 27, Issue 9, 2012, Pages 1164-1173

  Soragni, Elisabetta ^a   Xu, Chunping ^a   Plasterer, Heather L ^b   Jacques, Vincent ^b   Rusche, James R ^b   Gottesfeld, Joel M ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b REPLIGEN CORPORATION   (United States)

Author keywords

chromatin immunoprecipitation; Friedreich ataxia; heterochromatin; histone deacetylase inhibitor; neurodegenerative disorder

Indexed keywords

2 AMINOBENZAMIDE; 2 AMINOBENZAMIDE HISTONE DEACETYLASE INHIBITOR; COMPLEMENTARY RNA; DNA METHYLTRANSFERASE; FRATAXIN; HETEROCHROMATIN PROTEIN 1; HISTONE DEACETYLASE; HISTONE DEACETYLASE INHIBITOR; MESSENGER RNA; RNA POLYMERASE II; SILENT INFORMATION REGULATOR PROTEIN 2; TRANSCRIPTION FACTOR CTCF; UNCLASSIFIED DRUG;

CHROMATIN STRUCTURE; CHROMOSOME 9; CONFERENCE PAPER; DNA METHYLATION; DNA STRUCTURE; FRIEDREICH ATAXIA; GENE REPRESSION; GENE SILENCING; HETEROCHROMATIN; HISTONE ACETYLATION; HISTONE MODIFICATION; INTRON; NONHUMAN; POSITION EFFECT; PRIORITY JOURNAL; RNA PROCESSING; RNA SPLICING; UNTRANSLATED REGION; WILD TYPE;

ANIMALS; CLINICAL TRIALS, PHASE I AS TOPIC; DISEASE MODELS, ANIMAL; FLUORESCENT DYES; FRIEDREICH ATAXIA; GENE EXPRESSION REGULATION; HISTONE DEACETYLASE INHIBITORS; HUMANS; IRON-BINDING PROTEINS; MICE; MUTATION; ORTHO-AMINOBENZOATES; PROTEOMICS; TRINUCLEOTIDE REPEAT EXPANSION;

EID: 84865662814     PISSN: 08830738     EISSN: 17088283     Source Type: Journal    
DOI: 10.1177/0883073812448533     Document Type: Conference Paper

References (59)

1. Schmucker S, Puccio H. Understanding the molecular mechanisms of Friedreich's ataxia to develop therapeutic approaches. Hum Mol Genet. 2010 ; 19 (R1). R103 - R110
2. Saveliev A, Everett C, Sharpe T, et al. DNA triplet repeats mediate heterochromatin-protein-1-sensitive variegated gene silencing. Nature. 2003 ; 422 (6934). 909-913 (Pubitemid 36520045)
3. Herman D, Jenssen K, Burnett R, et al. Histone deacetylase inhibitors reverse gene silencing in Friedreich's ataxia. Nature Chem Biol. 2006 ; 2: 551-558 (Pubitemid 44413238)
4. Pandolfo M. Friedreich ataxia. Semin Pediatr Neurol. 2003 ; 10 (3). 163-172 (Pubitemid 37414092)
5. Delatycki MB, Williamson R, Forrest SM. Friedreich ataxia: an overview. J Med Genet. 2000 ; 37 (1). 1-8 (Pubitemid 30245868)
6. Tsou AY, Paulsen EK, Lagedrost SJ, et al. Mortality in Friedreich ataxia. J Neurol Sci. 2011 ; 307 (1-2). 46-49
7. Ye H, Rouault TA. Human iron-sulfur cluster assembly, cellular iron homeostasis, and disease. Biochemistry. 2010 ; 49 (24). 4945-4956
8. Meier T, Perlman SL, Rummey C, et al. Assessment of neurological efficacy of idebenone in pediatric patients with Friedreich's ataxia: data from a 6-month controlled study followed by a 12-month open-label extension study. J Neurol. 2012 ; 259 (2). 284-291
9. Velasco-Sanchez D, Aracil A, Montero R, et al. Combined therapy with idebenone and deferiprone in patients with Friedreich's ataxia. Cerebellum. 2011 ; 10 (1). 1-8
10. Gottesfeld JM. Small molecules affecting transcription in Friedreich ataxia. Pharmacol Ther. 2007 ; 116 (2). 236-248 (Pubitemid 47469990)
11. Sturm B, Stupphann D, Kaun C, et al. Recombinant human erythropoietin: effects on frataxin expression in vitro. Eur J Clin Invest. 2005 ; 35 (11). 711-717 (Pubitemid 41640907)
12. Acquaviva F, Castaldo I, Filla A, et al. Recombinant human erythropoietin increases frataxin protein expression without increasing mRNA expression. Cerebellum. 2008 ; 7 (3). 360-365
13. Rufini A, Fortuni S, Arcuri G, et al. Preventing the ubiquitin- proteasome-dependent degradation of frataxin, the protein defective in Friedreich's ataxia. Hum Mol Genet. 2011 ; 20 (7). 1253-1261
14. Vyas PM, Tomamichel WJ, Pride PM, et al. A TAT-Frataxin fusion protein increases lifespan and cardiac function in a conditional Friedreich's ataxia mouse model. Hum Mol Genet. 2012 ; 21 (6). 1230-1247
15. Lim F, Palomo GM, Mauritz C, et al. Functional recovery in a Friedreich's ataxia mouse model by frataxin gene transfer using an HSV-1 amplicon vector. Mol Ther. 2007 ; 15: 1072-1078 (Pubitemid 46813609)
16. Kumari D, Usdin K. Chromatin remodeling in the noncoding repeat expansion diseases. J Biol Chem. 2009 ; 284 (12). 7413-7417
17. Bidichandani SI, Ashizawa T, Patel PI. The GAA triplet-repeat expansion in Friedreich ataxia interferes with transcription and may be associated with an unusual DNA structure. Am J Hum Genet. 1998 ; 62 (1). 111-121 (Pubitemid 28093840)
18. Baralle M, Pastor T, Bussani E, Pagani F. Influence of Friedreich ataxia GAA noncoding repeat expansions on pre-mRNA processing. Am J Hum Genet. 2008 ; 83 (1). 77-88
19. Zoghbi HY, Orr HT. Trinucleotide repeat disorders. Ann Rev Neurosci. 2007 ; 30: 575-621 (Pubitemid 47218768)
20. De Biase I, Chutake YK, Rindler PM, Bidichandani SI. Epigenetic silencing in Friedreich ataxia is associated with depletion of CTCF (CCCTC-binding factor) and antisense transcription. PLoS One. 2009 ; 4 (11). e7914
21. He Y, Vogelstein B, Velculescu VE, et al. The antisense transcriptomes of human cells. Science. 2008 ; 322: 1855-1857
22. Sakamoto N, Chastain PD, Parniewski P, et al. Sticky DNA: self-association properties of long GAA.TTC repeats in R.R.Y triplex structures from Friedreich's ataxia. Mol Cell. 1999 ; 3 (4). 465-475 (Pubitemid 29292603)
23. Ohshima K, Montermini L, Wells RD, Pandolfo M. 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. 1998 ; 273 (23). 14588-14595 (Pubitemid 28319183)
24. Sakamoto N, Ohshima K, Montermini L, et al. Sticky DNA, a self-associated complex formed at long GAA*TTC repeats in intron 1 of the frataxin gene, inhibits transcription. J Biol Chem. 2001 ; 276 (29). 27171-27177
25. Grabczyk E, Usdin K. Alleviating transcript insufficiency caused by Friedreich's ataxia triplet repeats. Nucleic Acids Res. 2000 ; 28 (24). 4930-4937 (Pubitemid 32014263)
26. Grabczyk E, Usdin K. 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. 2000 ; 28 (14). 2815-2822 (Pubitemid 30488540)
27. Krasilnikova MM, Kireeva ML, Petrovic V, et al. Effects of Friedreich's ataxia (GAA)n*(TTC)n repeats on RNA synthesis and stability. Nuc Acids Res. 2007 ; 35: 1075-1084 (Pubitemid 46522963)
28. Elgin SC, Grewal SI. Heterochromatin: silence is golden. Curr Biol. 2003 ; 13 (23). R895 - R898
29. Greene E, Mahishi L, Entezam A, et al. Repeat-induced epigenetic changes in intron 1 of the frataxin gene and its consequences in Friedreich ataxia. Nucl Acids Res. 2007 ; 35: 3383-3390 (Pubitemid 47073601)
30. Kumari D, Biacsi RE, Usdin K. Repeat expansion affects both transcription initiation and elongation in Friedreich ataxia cells. J Biol Chem. 2011 ; 286 (6). 4209-4215
31. Kim E, Napierala M, Dent SY. Hyperexpansion of GAA repeats affects post-initiation steps of FXN transcription in Friedreich's ataxia. Nucleic Acids Res. 2011 ; 39 (19). 8366-8377
32. Al-Mahdawi S, Pinto RM, Ismail O, et al. The Friedreich ataxia GAA repeat expansion mutation induces comparable epigenetic changes in human and transgenic mouse brain and heart tissues. Hum Mol Genet. 2008 ; 17 (5). 735-746 (Pubitemid 351292262)
33. Rai M, Soragni E, Jenssen K, et al. HDAC inhibitors correct frataxin deficiency in a Friedreich ataxia mouse model. PLoS One. 2008 ; 3: e1958
34. Punga T, Buhler M. Long intronic GAA repeats causing Friedreich ataxia impede transcription elongation. EMBO Mol Med. 2010 ; 2 (4). 120-129
35. Castaldo I, Pinelli M, Monticelli A, et al. DNA methylation in intron 1 of the frataxin gene is related to GAA repeat length and age of onset in Friedreich ataxia patients. J Med Genet. 2008 ; 45 (12). 808-812
36. El-Osta A, Wolffe AP. DNA methylation and histone deacetylation in the control of gene expression: basic biochemistry to human development and disease. Gene Expr. 2000 ; 9: 63-75
37. Di Prospero NA, Fischbeck KH. Therapeutics development for triplet repeat expansion diseases. Nat Rev Genet. 2005 ; 6 (10). 756-765 (Pubitemid 41400833)
38. Langley B, Gensert JM, Beal MF, Ratan RR. Remodeling chromatin and stress resistance in the central nervous system: histone deacetylase inhibitors as novel and broadly effective neuroprotective agents. Curr Drug Targets CNS Neurol Disord. 2005 ; 4 (1). 41-50 (Pubitemid 41403313)
39. Kernochan LE, Russo ML, Woodling NS, et al. The role of histone acetylation in SMN gene expression. Hum Mol Genet. 2005 ; 14 (9). 1171-1182 (Pubitemid 40613906)
40. Tapscott SJ, Klesert TR, Widrow RJ, et al. Fragile-X syndrome and myotonic dystrophy: parallels and paradoxes. Curr Opin Genet Dev. 1998 ; 8 (2). 245-253 (Pubitemid 28206290)
41. Cho DH, Thienes CP, Mahoney SE, et al. Antisense transcription and heterochromatin at the DM1 CTG repeats are constrained by CTCF. Mol Cell. 2005 ; 20 (3). 483-489 (Pubitemid 41572304)
42. Kazantsev AG, Thompson LM. Therapeutic application of histone deacetylase inhibitors for central nervous system disorders. Nat Rev Drug Discov. 2008 ; 7: 854-868
43. Drummond DC, Noble CO, Kirpotin DB, et al. Clinical development of histone deacetylase inhibitors as anticancer agents. Ann Rev Pharmacol Toxicol. 2005 ; 45: 495-528 (Pubitemid 40261815)
44. Rai M, Soragni E, Chou CJ, et al. Two new pimelic diphenylamide HDAC inhibitors induce sustained frataxin upregulation in cells from Friedreich's ataxia patients and in a mouse model. PLoS One. 2010 ; 5 (1). e8825
45. Sandi C, Pinto RM, Al-Mahdawi S, et al. Prolonged treatment with pimelic o-aminobenzamide HDAC inhibitors ameliorates the disease phenotype of a Friedreich ataxia mouse model. Neurobiol Dis. 2011 ; 42 (3). 496-505
46. Soragni E, Xu C, Cooper A, Plasterer HL, et al. Evaluation of histone deacetylase inhibitors as therapeutics for neurodegenerative diseases. Methods Mol Biol. 2011 ; 793: 495-508
47. Miranda CJ, Santos MM, Ohshima K, et al. Frataxin knockin mouse. FEBS Lett. 2002 ; 512 (1-3). 291-297 (Pubitemid 34164497)
48. Chou CJ, Herman D, Gottesfeld JM. Pimelic diphenylamide 106 is a slow, tight-binding inhibitor of class I histone deacetylases. J Biol Chem. 2008 ; 283: 35402-35409
49. Beckers T, Burkhardt C, Wieland H, et al. Distinct pharmacological properties of second generation HDAC inhibitors with the benzamide or hydroxamate head group. Int J Cancer. 2007 ; 121: 1138-1148 (Pubitemid 47101654)
50. Hu E, Dul E, Sung CM, et al. Identification of novel isoform-selective inhibitors within class I histone deacetylases. J Pharmacol Exp Ther. 2003 ; 307 (2). 720-728 (Pubitemid 37310689)
51. Siliphaivanh P, Harrington P, Witter DJ, et al. Design of novel histone deacetylase inhibitors. Bioorg Med Chem Lett. 2007 ; 17 (16). 4619-4624 (Pubitemid 47058936)
52. Evans MJ, Cravatt BF. Mechanism-based profiling of enzyme families. Chem Rev. 2006 ; 106 (8). 3279-3301 (Pubitemid 44376936)
53. Hagenstein MC, Sewald N. Chemical tools for activity-based proteomics. J Biotechnol. 2006 ; 124 (1). 56-73 (Pubitemid 43816131)
54. Salisbury CM, Cravatt BF. Activity-based probes for proteomic pr ofiling of histone deacetylase complexes. Proc Natl Acad Sci U S A. 2007 ; 104 (4). 1171-1176 (Pubitemid 46183977)
55. Marks P, Rifkind RA, Richon VM, et al. Histone deacetylases and cancer: causes and therapies. Nat Rev Cancer. 2001 ; 1 (3). 194-202 (Pubitemid 33741894)
56. Xu C, Soragni E, Chou CJ, et al. Chemical probes identify a role for histone deacetylase 3 in Friedreich's ataxia gene silencing. Chem Biol. 2009 ; 16: 980-989
57. Broide RS, Redwine JM, Aftahi N, et al. Distribution of histone deacetylases 1-11 in the rat brain. J Mol Neurosci. 2007 ; 31 (1). 47-58 (Pubitemid 46588030)
58. Methot JL, Chakravarty PK, Chenard M, et al. Exploration of the internal cavity of histone deacetylase (HDAC) with selective HDAC1/HDAC2 inhibitors (SHI-1:2). Bioorg Med Chem Lett. 2008 ; 18 (3). 973-978 (Pubitemid 351179353)
59. Xu C, Soragni E, Jacques V, et al. Improved histone deacetylase inhibitors as therapeutics for the neurodegenerative disease Friedreich's ataxia: a new synthetic route. Pharmaceuticals. 2011 ; 4 (12). 1578-1590