Treatment of Niemann-Pick Type C Disease by Histone Deacetylase Inhibitors

Neurotherapeutics

Volumn 10, Issue 4, 2013, Pages 688-697

  Helquist, Paul ^a   Maxfield, Frederick R ^b   Wiech, Norbert L ^c   Wiest, Olaf ^a,d  

^a UNIVERSITY OF NOTRE DAME   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c Lysomics LLC   (United States)

^d PEKING UNIVERSITY   (China)

Author keywords

Cholesterol; Histone deacetylase inhibitors; Lipids; Lysosomes; Proteostasis

Indexed keywords

BENZAMIDE; CHOLESTEROL; GM 05659; GM 18443; GM 18445; HISTONE DEACETYLASE INHIBITOR; MANNOSE 6 PHOSPHATE; MEMBRANE PROTEIN; PANOBINOSTAT; PCI 34051; PCI 343051; ROMIDEPSIN; SOMATOMEDIN B RECEPTOR; TACEDINALINE; THIOPHENE; THIOPHENE BENZAMIDE; TRICHOSTATIN A; UNCLASSIFIED DRUG; VALPROIC ACID; VORINOSTAT;

CHOLESTEROL ESTERIFICATION; CHOLESTEROL TRANSPORT; CUTANEOUS T CELL LYMPHOMA; DEATH; DISEASE ASSOCIATION; DISEASE COURSE; DISEASE SEVERITY; DRUG APPROVAL; ENDOPLASMIC RETICULUM; ENDOSOME; FIBROBLAST; FOOD AND DRUG ADMINISTRATION; GENE MUTATION; HUMAN; INCIDENCE; LIPID STORAGE; MISSENSE MUTATION; MUTATION; NEUROPATHOLOGY; NIEMANN PICK DISEASE; NONHUMAN; PALLIATIVE THERAPY; POINT MUTATION; PRIORITY JOURNAL; RARE DISEASE; REVIEW;

CHOLESTEROL; ENDOSOMES; FIBROBLASTS; HISTONE DEACETYLASE INHIBITORS; HUMANS; LYSOSOMES; NIEMANN-PICK DISEASE, TYPE C;

EID: 84886303330     PISSN: 19337213     EISSN: 18787479     Source Type: Journal    
DOI: 10.1007/s13311-013-0217-2     Document Type: Review

References (112)

1. Vanier MT. Niemann-Pick disease type C. Orphanet J Rare Dis 2010;5: 16.
2. Walkley SU, Vanier MT. Secondary lipid accumulation in lysosomal disease. Biochim Biophys Acta 2009;1793: 726-36.
3. Niemann A. Ein unbekanntes Krankheitsbild. Jahrbuch für Kinderheilkunde 1914;79: 1-10.
4. Pick L. Der Morbus Gaucher und die ihm ähnlichen Krankheiten (die lipoidzellige Splenohepatomegalie Typus Niemann und die diabetische Lipoidzellenhypoplasie der Milz. Ergebnisse der Inneren Medizin und Kinderheilkunde, Berlin 1926;29: 519-627.
5. Crocker AC, Farber S. Niemann-Pick disease: a review of eighteen patients. Medicine 1958;37: 1-95.
6. Kruth HS, Comly M, Butler JD, et al. Type C Niemann-Pick disease. Abnormal metabolism of low density lipoprotein in homozygous and heterozygous fibroblasts. J Biol Chem 1986;261: 9290-8.
7. Pentchev PG, Kruth HS, Comly ME, et al. Type C Niemann-Pick disease. A parallel loss of regulatory responses in both the uptake and esterification of low density lipoprotein-derived cholesterol in cultured fibroblasts. J Biol Chem 1986;261: 16775-80.
8. Carstea ED, Morris JA, Coleman KG, et al. Niemann-Pick C1 disease gene: homology to mediators of cholesterol homeostasis. Science 1997;277: 228-31.
9. Stampfer M, Theiss S, Amraoui Y, et al. Niemann-Pick disease type C clinical database: cognitive and coordination deficits are early disease indicators. Orphanet J Rare Dis 2013;8: 35.
10. Kluenemann H-H, Santosh PJ, Sedel F. Treatable metabolic psychoses that go undetected: What Niemann-Pick type C can teach us. Int J Psych Clin Pract 2010;16: 162-9.
11. Bauer P, Balding DJ, Klunemann HH, et al. Genetic screening for Niemann-Pick disease type C in adults with neurological and psychiatric symptoms: findings from the ZOOM study. Hum Mol Genet 2013 Jun 26.
12. Yanjanin NM, Velez JI, Gropman A, et al. Linear clinical progression, independent of age of onset, in Niemann-Pick disease, type C. Am J Med Genet B Neuropsychiatr Genet 2010;153B(1): 132-40.
13. Trendelenburg G, Vanier MT, Maza S, et al. Niemann-Pick type C disease in a 68-year-old patient. J Neurol Neurosurg Psychiatry 2006;77: 997-8.
14. Salsano E, Umeh C, Rufa A, Pareyson D, Zee DS. Vertical supranuclear gaze palsy in Niemann-Pick type C disease. Neur Sci. 2012;33: 1225-32.
15. Walkley SU, Suzuki K. Consequences of NPC1 and NPC2 loss of function in mammalian neurons. Biochim Biophys Acta 2004;1685: 48-62.
16. Liou HL, Dixit SS, Xu S, Tint GS, Stock AM, Lobel P. NPC2, the protein deficient in Niemann-Pick C2 disease, consists of multiple glycoforms that bind a variety of sterols. J Biol Chem 2006;281: 36710-23.
17. Infante RE, Abi-Mosleh L, Radhakrishnan A, Dale JD, Brown MS, Goldstein JL. Purified NPC1 protein. I. Binding of cholesterol and oxysterols to a 1278-amino acid membrane protein. J Biol Chem 2008;283: 1052-63.
18. Kwon HJ, Abi-Mosleh L, Wang ML, et al. Structure of N-terminal domain of NPC1 reveals distinct subdomains for binding and transfer of cholesterol. Cell 2009;137: 1213-24.
19. Wang ML, Motamed M, Infante RE, et al. Identification of surface residues on Niemann-Pick C2 essential for hydrophobic handoff of cholesterol to NPC1 in lysosomes. Cell Metab 2010;12: 166-73.
20. Xu S, Benoff B, Liou HL, Lobel P, Stock AM. Structural basis of sterol binding by NPC2, a lysosomal protein deficient in Niemann-Pick type C2 disease. J Biol Chem 2007;282: 23525-31.
21. Deffieu MS, Pfeffer SR. Niemann-Pick type C 1 function requires lumenal domain residues that mediate cholesterol-dependent NPC2 binding. Proc Natl Acad Sci U S A 2011;108: 18932-6.
22. Kobayashi T, Beuchat MH, Lindsay M, et al. Late endosomal membranes rich in lysobisphosphatidic acid regulate cholesterol transport. Nat Cell Biol 1999;1: 113-8.
23. Mesmin B, Maxfield FR. Intracellular sterol dynamics. Biochim Biophys Acta 2009;1791: 636-45.
24. Devlin C, Pipalia NH, Liao X, Schuchman EH, Maxfield FR, Tabas I. Improvement in lipid and protein trafficking in Niemann-Pick C1 cells by correction of a secondary enzyme defect. Traffic 2011;11: 601-15.
25. Wraith JE, Vecchio D, Jacklin E, et al. Miglustat in adult and juvenile patients with Niemann-Pick disease type C: long-term data from a clinical trial. Mol Genet Metab 2010;99: 351-7.
26. Gelsthorpe ME, Baumann N, Millard E, et al. Niemann-Pick type C1 I1061T mutant encodes a functional protein that is selected for endoplasmic reticulum-associated degradation due to protein misfolding. J Biol Chem 2008;283: 8229-36.
27. Helquist P, Wiest O. Current status of drug therapy development for Niemann-Pick type C disease. Drugs Future 2009;34: 315-31.
28. Patterson MC, Di Bisceglie AM, Higgins JJ, et al. The effect of cholesterol-lowering agents on hepatic and plasma cholesterol in Niemann-Pick disease type C. Neurology 1993;43: 61-4.
29. Sylvain M, Arnold DL, Scriver CR, Schreiber R, Shevell MI. Magnetic resonance spectroscopy in Niemann-Pick disease type C: correlation with diagnosis and clinical response to cholestyramine and lovastatin. Pediatr Neurol 1994;10: 228-32.
30. Cheung NS, Koh CH, Bay BH, et al. Chronic exposure to U18666A induces apoptosis in cultured murine cortical neurons. Biochem Biophys Res Commun 2004;315: 408-17.
31. Reid PC, Lin S, Vanier MT, et al. Partial blockage of sterol biosynthesis with a squalene synthase inhibitor in early postnatal Niemann-Pick type C npcnih null mice brains reduces neuronal cholesterol accumulation, abrogates astrogliosis, but may inhibit myelin maturation. J Neurosci Methods 2008;168: 15-25.
32. Beltroy EP, Liu B, Dietschy JM, Turley SD. Lysosomal unesterified cholesterol content correlates with liver cell death in murine Niemann-Pick type C disease. J Lipid Res 2007;48: 869-81.
33. Schedin S, Pentchev P, Dallner G. Reduced cholesterol accumulation and improved deficient peroxisomal functions in a murine model of Niemann-Pick type C disease upon treatment with peroxisomal proliferators. Biochem Pharmacol 1998;56: 1195-9.
34. Beheregaray AP, Souza FT, Coelho JC. Effect of a peroxysomal proliferator agent on intracellular cholesterol accumulation in cultured fibroblasts from Niemann-Pick type C disease patients. Clin Chim Acta 2003;336: 137-42.
35. Griffin LD, Gong W, Verot L, Mellon SH. Niemann-Pick type C disease involves disrupted neurosteroidogenesis and responds to allopregnanolone. Nat Med 2004;10: 704-11.
36. Langmade SJ, Gale SE, Frolov A, et al. Pregnane X receptor (PXR) activation: a mechanism for neuroprotection in a mouse model of Niemann-Pick C disease. Proc Natl Acad Sci U S A 2006;103: 13807-12.
37. Lange Y, Ye J, Rigney M, Steck T. Cholesterol movement in Niemann-Pick type C cells and in cells treated with amphiphiles. J Biol Chem 2000;275: 17468-75.
38. Frolov A, Zielinski SE, Crowley JR, Dudley-Rucker N, Schaffer JE, Ory DS. NPC1 and NPC2 regulate cellular cholesterol homeostasis through generation of low density lipoprotein cholesterol-derived oxysterols. J Biol Chem 2003;278: 25517-25.
39. Chen G, Li HM, Chen YR, Gu XS, Duan S. Decreased estradiol release from astrocytes contributes to the neurodegeneration in a mouse model of Niemann-Pick disease type C. Glia 2007;55: 1509-18.
40. Ory DS. The Niemann-Pick disease genes; regulators of cellular cholesterol homeostasis. Trends Cardiovasc Med 2004;14: 66-72.
41. Repa JJ, Li H, Frank-Cannon TC, et al. Liver X receptor activation enhances cholesterol loss from the brain, decreases neuroinflammation, and increases survival of the NPC1 mouse. J Neurosci 2007;27: 14470-80.
42. Boadu E, Choi HY, Lee DW, et al. Correction of apolipoprotein A-I-mediated lipid efflux and high density lipoprotein particle formation in human Niemann-Pick type C disease fibroblasts. J Biol Chem 2006;281: 37081-90.
43. Lalloyer F, Fievet C, Lestavel S, et al. The RXR agonist bexarotene improves cholesterol homeostasis and inhibits atherosclerosis progression in a mouse model of mixed dyslipidemia. Arterioscler Thromb Vasc Biol 2006;26: 2731-7.
44. Patterson MC, Vecchio D, Prady H, Abel L, Wraith JE. Miglustat for treatment of Niemann-Pick C disease: a randomised controlled study. Lancet Neurol 2007;6: 765-72.
45. Zervas M, Somers KL, Thrall MA, Walkley SU. Critical role for glycosphingolipids in Niemann-Pick disease type C. Curr Biol 2001;11: 1283-7.
46. Patterson MC, Platt F. Therapy of Niemann-Pick disease, type C. Biochim Biophys Acta 2004;1685: 77-82.
47. Lloyd-Evans E, Morgan AJ, He X, et al. Niemann-Pick disease type C1 is a sphingosine storage disease that causes deregulation of lysosomal calcium. Nat Med 2008;14: 1247-55.
48. Fu S, Kurzrock R. Development of curcumin as an epigenetic agent. Cancer 2010;116: 4670-6.
49. Borbon IA, Hillman Z, Duran E, Jr, Kiela PR, Frautschy SA, Erickson RP. Lack of efficacy of curcumin on neurodegeneration in the mouse model of Niemann-Pick C1. Pharmacol Biochem Behav 2012;101: 125-31.
50. Alvarez AR, Klein A, Castro J, et al. Imatinib therapy blocks cerebellar apoptosis and improves neurological symptoms in a mouse model of Niemann-Pick type C disease. FASEB J 2008;22: 3617-27.
51. Erickson RP, Bernard O. Studies on neuronal death in the mouse model of Niemann-Pick C disease. J Neurosci Res 2002;68: 738-44.
52. Kim SJ, Lim MS, Kang SK, Lee YS, Kang KS. Impaired functions of neural stem cells by abnormal nitric oxide-mediated signaling in an in vitro model of Niemann-Pick type C disease. Cell Res 2008;18: 686-94.
53. Bascunan-Castillo EC, Erickson RP, Howison CM, et al. Tamoxifen and vitamin E treatments delay symptoms in the mouse model of Niemann-Pick C. J Appl Genet 2004;45: 461-7.
54. Ulatowski L, Parker R, Davidson C, et al. Altered vitamin E status in Niemann-Pick type C disease. J Lipid Res 2011;52: 1400-10.
55. Liscum L, Arnio E, Anthony M, Howley A, Sturley SL, Agler M. Identification of a pharmaceutical compound that partially corrects the Niemann-Pick C phenotype in cultured cells. J Lipid Res 2002;43: 1708-17.
56. Pipalia NH, Huang A, Ralph H, Rujoi M, Maxfield FR. Automated microscopy screening for compounds that partially revert cholesterol accumulation in Niemann-Pick C cells. J Lipid Res 2006;47: 284-301.
57. Rujoi M, Pipalia NH, Maxfield FR. Cholesterol pathways affected by small molecules that decrease sterol levels in Niemann-Pick type C mutant cells. PLoS One 2010;5: e12788.
58. Cosner CC, Markiewicz JT, Bourbon P, et al. Investigation of N-aryl-3-alkylidenepyrrolinones as potential Niemann-Pick type C disease therapeutics. J Med Chem 2009;52: 6494-8.
59. Rosenbaum AI, Cosner CC, Mariani CJ, Maxfield FR, Wiest O, Helquist P. Thiadiazole carbamates: potent inhibitors of lysosomal acid lipase and potential Niemann-Pick type C disease therapeutics. J Med Chem 2010;53: 5281-9.
60. Somers KL, Brown DE, Fulton R, et al. Effects of dietary cholesterol restriction in a feline model of Niemann-Pick type C disease. J Inherit Metab Dis 2001;24: 427-36.
61. Walterfang M, Chien YH, Imrie J, Rushton D, Schubiger D, Patterson MC. Dysphagia as a risk factor for mortality in Niemann-Pick disease type C: systematic literature review and evidence from studies with miglustat. Orphanet J Rare Dis 2012;7: 76.
62. Kuter DJ, Mehta A, Hollak CE, et al. Miglustat therapy in type 1 Gaucher disease: clinical and safety outcomes in a multicenter retrospective cohort study. Blood Cells Mol Dis 2013;51: 116-24.
63. Ramirez CM, Liu B, Taylor AM, et al. Weekly cyclodextrin administration normalizes cholesterol metabolism in nearly every organ of the Niemann-Pick type C1 mouse and markedly prolongs life. Pediatr Res 2010;68: 309-15.
64. Fan M, Sidhu R, Fujiwara H, et al. Identification of Niemann-Pick C1 (NPC1) disease biomarkers through sphingolipid profiling. J Lipid Res 2013 Jul 23.
65. ClinicalTrials. gov. Hydroxypropyl beta cyclodextrin for Niemann-Pick Type C1 disease. Available at: http://clinicaltrials. gov/ct2/show/NCT01747135. Accessed 10 Sept 2013.
66. Crumling MA, Liu L, Thomas PV, et al. Hearing loss and hair cell death in mice given the cholesterol-chelating agent hydroxypropyl-beta-cyclodextrin. PLoS One 2012;7: e53280.
67. Pipalia NH, Cosner CC, Huang A, et al. Histone deacetylase inhibitor treatment dramatically reduces cholesterol accumulation in Niemann-Pick type C1 mutant human fibroblasts. Proc Natl Acad Sci U S A 2011;108: 5620-5.
68. Yang C, Rahimpour S, Lu J, et al. Histone deacetylase inhibitors increase glucocerebrosidase activity in Gaucher disease by modulation of molecular chaperones. Proc Natl Acad Sci U S A 2013;110: 966-71.
69. Kim SJ, Lee BH, Lee YS, Kang KS. Defective cholesterol traffic and neuronal differentiation in neural stem cells of Niemann-Pick type C disease improved by valproic acid, a histone deacetylase inhibitor. Biochem Biophys Res Commun 2007;360: 593-9.
70. Shafaati M, O'Driscoll R, Bjorkhem I, Meaney S. Transcriptional regulation of cholesterol 24-hydroxylase by histone deacetylase inhibitors. Biochem Biophys Res Commun 2009;378(4): 689-94.
71. Wagner FF, Weyi{cyrillic}wer M, Lewis MC, Holson, EB. Small Molecule Inhibitors of Zinc-Dependent Histone Deacetylases (HDACs). Neurotherapeutics 2013. doi: 10. 1007/s13311-013-0226-1.
72. Pipalia NH, Maxfield FR. Investigating the therapeutic potential of HDAC Inhibitors for the treatment of Niemann Pick type C1 Disease. Mol Biol Cell 2011;22: abstract #1642.
73. Munkacsi AB, Chen FW, Brinkman MA, et al. An "exacerbate-reverse" strategy in yeast identifies histone deacetylase inhibition as a correction for cholesterol and sphingolipid transport defects in human Niemann-Pick type C disease. J Biol Chem 2011;286: 23842-51.
74. Wehrmann ZT, Hulett TW, Huegel KL, et al. Quantitative comparison of the efficacy of various compounds in lowering intracellular cholesterol levels in Niemann-Pick type C fibroblasts. PLoS One 2012;7: e48561.
75. Grant S, Easley C, Kirkpatrick P. Vorinostat. Nat Rev Drug Discov 2007;6(1): 21-2.
76. Tiffon C, Adams J, van der Fits L, et al. The histone deacetylase inhibitors vorinostat and romidepsin downmodulate IL-10 expression in cutaneous T-cell lymphoma cells. Br J Pharmacol 2011;162: 1590-602.
77. Wiech NL, Fisher JF, Helquist P, Wiest O. Inhibition of histone deacetylases: a pharmacological approach to the treatment of non-cancer disorders. Curr Top Med Chem 2009;9: 257-71.
78. Marini JC, Lanpher BC, Scaglia F, et al. Phenylbutyrate improves nitrogen disposal via an alternative pathway without eliciting an increase in protein breakdown and catabolism in control and ornithine transcarbamylase-deficient patients. Am J Clin Nutr 2011;93: 1248-54.
79. Batshaw ML, MacArthur RB, Tuchman M. Alternative pathway therapy for urea cycle disorders: twenty years later. J Pediatr 2001;138(1 Suppl.): S46-54.
80. Collins AF, Pearson HA, Giardina P, McDonagh KT, Brusilow SW, Dover GJ. Oral sodium phenylbutyrate therapy in homozygous beta thalassemia: a clinical trial. Blood 1995;85: 43-9.
81. Dover GJ, Brusilow S, Charache S. Induction of fetal hemoglobin production in subjects with sickle cell anemia by oral sodium phenylbutyrate. Blood 1994;8: 339-43.
82. Rubenstein RC, Egan ME, Zeitlin PL. In vitro pharmacologic restoration of CFTR-mediated chloride transport with sodium 4-phenylbutyrate in cystic fibrosis epithelial cells containing delta F508-CFTR. J Clin Invest 1997;100: 2457-65.
83. Smith W, Diaz GA, Lichter-Konecki U, et al. Ammonia control in children ages 2 months through 5 years with urea cycle disorders: comparison of sodium phenylbutyrate and glycerol phenylbutyrate. J Pediatr. 2013;162: 1228-34, 34 e1.
84. Perucca E. Pharmacological and therapeutic properties of valproate: a summary after 35 years of clinical experience. CNS Drugs 2002;16: 695-714.
85. Peedicayil J. Epigenetic drugs in cognitive disorders. Curr Pharm Des 2013 Jul 19.
86. Graff J, Tsai LH. The potential of HDAC inhibitors as cognitive enhancers. Annu Rev Pharmacol Toxicol 2013;53: 311-30.
87. Levenson JM, O'Riordan KJ, Brown KD, Trinh MA, Molfese DL, Sweatt JD. Regulation of histone acetylation during memory formation in the hippocampus. J Biol Chem 2004;279: 40545-59.
88. Stilling RM, Fischer A. The role of histone acetylation in age-associated memory impairment and Alzheimer's disease. Neurobiol Learn Mem 2011;96: 19-26.
89. Kelly WK, O'Connor OA, Krug LM, et al. Phase I study of an oral histone deacetylase inhibitor, suberoylanilide hydroxamic acid, in patients with advanced cancer. J Clin Oncol 2005;23: 3923-31.
90. Kelly WK, Richon VM, O'Connor O, et al. Phase I clinical trial of histone deacetylase inhibitor: suberoylanilide hydroxamic acid administered intravenously. Clin Cancer Res 2003;9: 3578-88.
91. O'Connor OA, Heaney ML, Schwartz L, et al. Clinical experience with intravenous and oral formulations of the novel histone deacetylase inhibitor suberoylanilide hydroxamic acid in patients with advanced hematologic malignancies. J Clin Oncol 2006;24: 166-73.
92. Parise RA, Holleran JL, Beumer JH, Ramalingam S, Egorin MJ. A liquid chromatography-electrospray ionization tandem mass spectrometric assay for quantitation of the histone deacetylase inhibitor, vorinostat (suberoylanilide hydroxamicacid, SAHA), and its metabolites in human serum. J Chromatogr B Analyt Technol Biomed Life Sci 2006;840: 108-15.
93. Iwamoto M, Friedman EJ, Sandhu P, Agrawal NG, Rubin EH, Wagner JA. Clinical pharmacology profile of vorinostat, a histone deacetylase inhibitor. Cancer Chemother Pharmacol 2013;72: 493-508.
94. Maue RA, Burgess RW, Wang B, et al. A novel mouse model of Niemann-Pick type C disease carrying a D1005G-Npc1 mutation comparable to commonly observed human mutations. Hum Mol Genet 2012;21: 730-50.
95. Bagel JH, Sikora TU, Prociuk M, et al. Electrodiagnostic testing and histopathologic changes confirm peripheral nervous system myelin abnormalities in the feline model of Niemann-Pick disease type C. J Neuropathol Exp Neurol 2013;72: 256-62.
96. Yin D, Ong JM, Hu J, et al. Suberoylanilide hydroxamic acid, a histone deacetylase inhibitor: effects on gene expression and growth of glioma cells in vitro and in vivo. Clin Cancer Res 2007;13: 1045-52.
97. Palmieri D, Lockman PR, Thomas FC, et al. Vorinostat inhibits brain metastatic colonization in a model of triple-negative breast cancer and induces DNA double-strand breaks. Clin Cancer Res 2009;15: 6148-57.
98. Hockly E, Richon VM, Woodman B, et al. Suberoylanilide hydroxamic acid, a histone deacetylase inhibitor, ameliorates motor deficits in a mouse model of Huntington's disease. Proc Natl Acad Sci U S A 2003;100: 2041-6.
99. Guan JS, Haggarty SJ, Giacometti E, et al. HDAC2 negatively regulates memory formation and synaptic plasticity. Nature 2009;459: 55-60.
100. Galanis E, Jaeckle KA, Maurer MJ, et al. Phase II trial of vorinostat in recurrent glioblastoma multiforme: a north central cancer treatment group study. J Clin Oncol 2009;27: 2052-8.
101. Kazantsev AG, Thompson LM. Therapeutic application of histone deacetylase inhibitors for central nervous system disorders. Nat Rev Drug Discov 2008;7: 854-68.
102. Leoni F, Zaliani A, Bertolini G, et al. The antitumor histone deacetylase inhibitor suberoylanilide hydroxamic acid exhibits antiinflammatory properties via suppression of cytokines. Proc Natl Acad Sci U S A 2002;99: 2995-3000.
103. Fouladi M, Park JR, Stewart CF, et al. Pediatric phase I trial and pharmacokinetic study of vorinostat: a Children's Oncology Group phase I consortium report. J Clin Oncol 2010;28: 3623-9.
104. Hummel TR, Wagner L, Ahern C, et al. A pediatric phase 1 trial of vorinostat and temozolomide in relapsed or refractory primary brain or spinal cord tumors: A children's oncology group phase 1 consortium study. Pediatr Blood Cancer 2013;60: 1452-7.
105. Muscal JA, Thompson PA, Horton TM, et al. A phase I trial of vorinostat and bortezomib in children with refractory or recurrent solid tumors: a Children's Oncology Group phase I consortium study (ADVL0916). Pediatr Blood Cancer 2013;60: 390-5.
106. Witt O, Milde T, Deubzer HE, et al. Phase I/II intra-patient dose escalation study of vorinostat in children with relapsed solid tumor, lymphoma or leukemia. Klin Padiatr 2012;224: 398-403.
107. Marks PA. Discovery and development of SAHA as an anticancer agent. Oncogene 2007;26: 1351-6.
108. Siegel D, Hussein M, Belani C, et al. Vorinostat in solid and hematologic malignancies. J Hematol Oncol 2009;2: 31.
109. Riva L, Blaney SM, Dauser R, et al. Pharmacokinetics and cerebrospinal fluid penetration of CI-994 (N-acetyldinaline) in the nonhuman primate. Clin Cancer Res 2000;6: 994-7.
110. Fass DM, Reis SA, Ghosh B, et al. Crebinostat: a novel cognitive enhancer that inhibits histone deacetylase activity and modulates chromatin-mediated neuroplasticity. Neuropharmacology 2013;64: 81-96.
111. Schroeder FA, Chonde DB, Riley MM, et al. FDG-PET imaging reveals local brain glucose utilization is altered by class I histone deacetylase inhibitors. Neurosci Lett 2013;550: 119-24.
112. Wang Y, Zhang YL, Hennig K, et al. Class I HDAC imaging using [(3) H]CI-994 autoradiography. Epigenetics 2013 Jun 11.