Inhibition of the striatal specific phosphodiesterase PDE10A ameliorates striatal and cortical pathology in R6/2 mouse model of Huntington's disease

PLoS ONE

Volumn 5, Issue 10, 2010, Pages

  Giampà, Carmela ^a   Laurenti, Daunia ^a   Anzilotti, Serenella ^a   Bernardi, Giorgio ^a,b   Menniti, Frank S ^c   Fusco, Francesca Romana ^a  

^a IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^b UNIVERSITY OF ROME TOR VERGATA   (Italy)

^c Mnemosyne Pharmaceuticals Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CYCLIC AMP; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; HUNTINGTIN; PHOSPHODIESTERASE; PHOSPHODIESTERASE INHIBITOR; PHOSPHODIESTERASE XA; PHOSPHODIESTERASE XA INHIBITOR; TP 10; UNCLASSIFIED DRUG; 2 (4 (PYRIDIN 4 YL 1 (2,2,2 TRIFLUOROETHYL) 1H PYRAZOL 3 YL)PHENOXYMETHYL)QUINOLINE SUCCINIC ACID; 2-(4-(PYRIDIN-4-YL-1-(2,2,2-TRIFLUOROETHYL)-1H-PYRAZOL-3-YL)PHENOXYMETHYL)QUINOLINE SUCCINIC ACID; PDE10A PROTEIN, MOUSE; PYRAZOLE DERIVATIVE; QUINOLINE DERIVATIVE;

ANIMAL CELL; ANIMAL EUTHANASIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; BRAIN CORTEX; BRAIN FUNCTION; CELL ACTIVATION; CELL LOSS; CELL NUCLEUS INCLUSION BODY; CONTROLLED STUDY; DISEASE MODEL; DRUG BLOOD LEVEL; DRUG BRAIN LEVEL; DRUG TARGETING; ENZYME INHIBITION; HINDLIMB; HUNTINGTON CHOREA; LOCOMOTION; MICROGLIA; MOUSE; NONHUMAN; OPEN FIELD TEST; PROTEIN PHOSPHORYLATION; RIGHTING REFLEX; ROTAROD TEST; SIGNAL TRANSDUCTION; STRIATE CORTEX; TASK PERFORMANCE; TREATMENT DURATION; ANIMAL; CORPUS STRIATUM; DRUG EFFECT; ENZYMOLOGY; IMMUNOHISTOCHEMISTRY; METABOLISM; PATHOLOGY;

MUS;

ANIMALS; CORPUS STRIATUM; DISEASE MODELS, ANIMAL; HUNTINGTON DISEASE; IMMUNOHISTOCHEMISTRY; MICE; PHOSPHODIESTERASE INHIBITORS; PHOSPHORIC DIESTER HYDROLASES; PYRAZOLES; QUINOLINES;

EID: 78149452347     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0013417     Document Type: Article

References (56)

1. Walker FO (2007) Huntington's disease. Lancet 369: 218-228.
2. The Huntington's Disease Collaborative Research Group (1993) A novel gene containing a trinucleotide repeat is expanded and unstable on Huntington's disease chromosomes. Cell 72: 971-983.
3. Mangiarini L, Sathasivam K, Seller M, Cozens B, Harper A, et al. (1996) Exon 1 of the HD gene with an expanded CAG repeat is sufficient to cause a progressive neurological phenotype in transgenic mice. Cell 87: 493-506.
4. Andrew SE, Goldberg YP, Kremer B, Telenius H, Theilmann J, et al. (1993) The relationship between trinucleotide (CAG) repeat length and clinical features of Huntington's disease. Nature Genetics 4: 398-403.
5. Vonsattel JP, Myers RH, Stevens TJ, Ferrante RJ, Bird ED, et al. (1985) Neuropathological classification of Huntington's disease. J Neuropathol Exp Neurol 44: 559-577.
6. de la Monte SM, Vonsattel JP, Richardson EP, Jr. (1988) Morphometric demonstration of atrophic changes in the cerebral cortex, white matter, and neostriatum in Huntington's disease. J Neuropathol Exp Neurol 47: 516-525.
7. DiFiglia M, Sapp E, Chase KO, Davies SW, Bates GP, et al. (1997) Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science 277: 1990-1993.
8. Bates G (2003) Huntingtin aggregation and toxicity in Huntington's disease. Lancet 361: 1642-1644.
9. Kuemmerle S, Gutekunst CA, Klein AM, Li XJ, Li SH, et al. (1999) Huntington aggregates may not predict neuronal death in Huntington's disease. Annals of Neurology 46: 842-849.
10. Stack EC, Ferrante RJ (2007) Huntington's disease: progress and potential in the field. Expert Opin Investig Drugs 16: 1933-1953.
11. Imarisio S, Carmichael J, Korolchuk V, Chen CW, Saiki S, et al. (2008) Huntington's disease: from pathology and genetics to potential therapies. Biochemical Journal 412: 191-209.
12. Gines S, Seong IS, Fossale E, Ivanova E, Trettel F, et al. (2003) Specific progressive cAMP reduction implicates energy deficit in presymptomatic Huntington's disease knock-in mice. Human Molecular Genetics 12: 497-508.
13. Sugars KL, Rubinsztein DC (2003) Transcriptional abnormalities in Huntington disease. Trends in Genetics 19: 233-238.
14. Sugars KL, Brown R, Cook LJ, Swartz J, Rubinsztein DC (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.
15. Jiang H, Nucifora FC, Jr., Ross CA, DeFranco DB (2003) Cell death triggered by polyglutamine-expanded huntingtin in a neuronal cell line is associated with degradation of CREB-binding protein. Human Molecular Genetics 12: 1-12.
16. Nucifora FC, Jr., Sasaki M, Peters MF, Huang H, Cooper JK (2001) Interference by huntingtin and atrophin-1 with cbp-mediated transcription leading to cellular toxicity. Science 291: 2423-2428.
17. Steffan JS, Kazantsev A, Spasic-Boskovic O, Greenwald M, Zhu YZ (2000) The Huntington's disease protein interacts with p53 and CREB-binding protein and represses transcription. Proc Natl Acad Sci U S A 97: 6763-6768.
18. Steffan JS, Bodai L, Pallos J, Poelman M, McCampbell A (2001) Histone deacetylase inhibitors arrest polyglutamine-dependent neurodegeneration in Drosophila. Nature 413: 739-743.
19. Luthi-Carter R, Strand A, Peters NL, Solano SM, Hollingsworth ZR (2000) Decreased expression of striatal signaling genes in a mouse model of Huntington's disease. Human Molecular Genetics 9: 1259-1271.
20. Wyttenbach A, Swartz J, Kita H, Thykjaer T, Carmichael J (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. Human Molecular Genetics 10: 1829-1845.
21. Houslay MD, Adams DR (2003) PDE4 cAMP phosphodiesterases: modular enzymes that orchestrate signalling cross-talk, desensitization and compartmentalization. Biochem J 370: 1-18.
22. Conti M, Beavo J (2007) Biochemistry and Physiology of Cyclic Nucleotide Phosphodiesterases: Essential Components in Cyclic Nucleotide Signaling. Annual Review of Biochemistry 76: 481-511.
23. Menniti FS, Faraci WS, Schmidt CJ (2006) Phosphodiesterases in the CNS: targets for drug development. Nat Rev Drug Discov 5: 660-670.
24. MacKenzie SJ, Houslay MD (2000) Action of rolipram on specific PDE4 cAMP phosphodiesterase isoforms and on the phosphorylation of cAMP-responseelement- binding protein (CREB) and p38 mitogen-activated protein (MAP) kinase in U937 monocytic cells. Biochemical Journal 347: 571-578.
25. Carlezon WA, Jr., Duman RS, Nestler EJ (2005) The many faces of CREB. Trends Neurosci 28: 436-445.
26. DeMarch Z, Giampa C, Patassini S, Martorana A, Bernardi G (2007) Beneficial effects of rolipram in a quinolinic acid model of striatal excitotoxicity. Neurobiology of Disease 25: 266-273.
27. DeMarch Z, Giampa C, Patassini S, Bernardi G, Fusco FR (2008) Beneficial effects of rolipram in the R6/2 mouse model of Huntington's disease. Neurobiology of Disease 30: 375-387.
28. Coskran TM, Morton D, Menniti FS, Adamowicz WO, Kleiman RJ, et al. (2006) Immunohistochemical Localization of Phosphodiesterase 10A in Multiple Mammalian Species. J Histochem Cytochem 54: 1205-1213.
29. Seeger TF, Bartlett B, Coskran TM, Culp JS, James LC, et al. (2003) Immunohistochemical localization of PDE10A in the rat brain. Brain Research 985: 113-126.
30. Xie Z, Adamowicz WO, Eldred WD, Jakowski AB, Kleiman RJ, et al. (2006) Cellular and subcellular localization of PDE10A, a striatum-enriched phosphodiesterase. Neuroscience 139: 597-607.
31. Siuciak JA, Chapin DS, Harms JF, Lebel LA, McCarthy SA, et al. (2006) Inhibition of the striatum-enriched phosphodiesterase PDE10A: A novel approach to the treatment of psychosis. Neuropharmacology 51: 386-396.
32. Siuciak JA, McCarthy SA, Chapin DS, Fujiwara RA, James LC, et al. (2006) Genetic deletion of the striatum-enriched phosphodiesterase PDE10A: Evidence for altered striatal function. Neuropharmacology 51: 374-385.
33. Schmidt CJ, Chapin DS, Cianfrogna J, Corman ML, Hajos M, et al. (2008) Preclinical Characterization of Selective Phosphodiesterase 10A Inhibitors: A New Therapeutic Approach to the Treatment of Schizophrenia. J Pharmacol Exp Ther 325: 681-690.
34. Giampà C, Patassini S, Borreca A, Laurenti D, Marullo F, et al. (2009) Phosphodiesterase 10 inhibition reduces striatal excitotoxicity in the quinolinic acid model of Huntington's disease. Neurobiology of Disease In press.
35. Hansson O, Nylandsted J, Castilho RF, Leist M, Jaattela M, et al. (2003) Overexpression of heat shock protein 70 in R6/2 Huntington's disease mice has only modest effects on disease progression. Brain Research 970: 47-57.
36. Hersch SM, Ferrante RJ (2004) Translating therapies for Huntington's disease from genetic animal models to clinical trials. NeuroRX 1: 298-306.
37. Ma TC, Buescher JL, Oatis B, Funk JA, Nash AJ, et al. (2007) Metformin therapy in a transgenic mouse model of Huntington's disease. Neuroscience Letters 411: 98-103.
38. Hockly E, Cordery PM, Woodman B, Mahal A, van Dellen A, et al. (2002) Environmental enrichment slows disease progression in R6/2 Huntington's disease mice. Annals of Neurology 51: 235-242.
39. Stack EC, Smith KM, Ryu H, Cormier K, Chen M, et al. (2006) Combination therapy using minocycline and coenzyme Q10 in R6/2 transgenic Huntington's disease mice. Biochim Biophys Acta 1762: 373-380.
40. Gutekunst CA, Li SH, Yi H, Mulroy JS, Kuemmerle S, et al. (1999) Nuclear and neuropil aggregates in Huntington's disease: relationship to neuropathology. Journal of Neuroscience 19: 2522-2534.
41. Sano H, Nagai Y, Miyakawa T, Shigemoto R, Yokoi M (2008) Increased social interaction in mice deficient of the striatal medium spiny neuron-specific phosphodiesterase 10A2. Journal of Neurochemistry 105: 546-556.
42. Strick CA, James LC, Fox CB, Seeger TF, Menniti FS, et al. (2010) Alterations in gene regulation following inhibition of the striatum-enriched phosphodiesterase, PDE10A. Neuropharmacology 58: 444-451.
43. Kleiman RJ, Kimmel LH, Bove SE, Lanz TA, Harms JF, et al. (2010) Chronic suppression of PDE10A alters striatal expression of genes responsible for neurotransmitter synthesis, neurotransmission and signaling pathways implicated in Huntington's Disease. Journal of Pharmacology and Experimental Theraputics. In press.
44. Cramer H, Warter JM, Renaud B (1984) Analysis of neurotransmitter metabolites and adenosine 39,59-monophosphate in the CSF of patients with extrapyramidal motor disorders. Adv Neurol 40: 431-435.
45. Zuccato C, Marullo M, Conforti P, MacDonald ME, Tartari M, et al. (2008) Systematic assessment of BDNF and its receptor levels in human cortices affected by Huntington's disease. Brain Pathol 18: 225-238.
46. Zuccato C, Ciammola A, Rigamonti D, Leavitt BR, Goffredo D, et al. (2001) Loss of huntingtin-mediated BDNF gene transcription in Huntington's disease. Science 293: 493-498.
47. Gharami K, Xie Y, An JJ, Tonegawa S, Xu B (2008) Brain-derived neurotrophic factor over-expression in the forebrain ameliorates Huntington's disease phenotypes in mice. Journal of Neurochemistry 105: 369-379.
48. Zuccato C, Cattaneo E (2007) Role of brain-derived neurotrophic factor in Huntington's disease. Progress in Neurobiology 81: 294-330.
49. Chappie TA, Humphrey JM, Menniti FS, Schmidt CJ (2009) PDE10A Inhibitors: An Assessment of the Current CNS Drug Discovery Landscape. Current Opinion in Investigational Drugs 12: 458-467.
50. Kehler J, Kilburn JP (2009) Patented PDE10A inhibitors: novel compounds since 2007. Expert Opin Ther Pat 19: 1715-1725.
51. Verhoest PR, Chapin DS, Corman M, Fonseca K, Harms JF, et al. (2009) Discovery of a Novel Class of Phosphodiesterase 10A Inhibitors and Identification of Clinical Candidate 2-[4-(1-Methyl-4-pyridin-4-yl-1H-pyrazol- 3-yl)-phenoxymethyl]-quinoline (PF-2545920) for the Treatment of Schizophrenia. J Med Chem 52: 7946-7949.
52. Fusco FR, Chen Q, Lamoreaux WJ, Figueredo-Cardenas G, Jiao Y, et al. (1999) Cellular localization of huntingtin in striatal and cortical neurons in rats: lack of correlation with neuronal vulnerability in Huntington's disease. Journal of Neuroscience 19: 1189-1202.
53. Giampa C, DeMarch Z, D'Angelo V, Morello M, Martorana A (2006) Striatal modulation of cAMP-response-element-binding protein CREB. after excitotoxic lesions, implications with neuronal vulnerability in Huntington's disease. Eur J Neurosci 23: 11-20.
54. Fusco FR, Zuccato, C, Tartari, M, Martorana, A, De March, Z, et al. (2003) Colocalization of brain-derived neurotrophic factor (BDNF) and wild-type huntingtin in normal and quinolinic acid-lesioned rat brain. Eur J Neurosci 18: 1093-1102.
55. Perrin V, Dufour, N, Raoul, C, Hassig, R, Brouillet, E, et al. (2009) Implication of the JNK pathway in a rat model of Huntington's disease. Exp Neurol 215: 191-200.
56. Kaplan EL, Meier P (1958) Nonparametric estimation from incomplete observations. Journal of the American Statistical Association 53: 457-481.