Unique drug screening approach for prion diseases identifies tacrolimus and astemizole as antiprion agents

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 17, 2013, Pages 7044-7049

  Karapetyan, Yervand Eduard ^a,b   Sferrazza, Gian Franco ^a,c   Zhou, Minghai ^a   Ottenberg, Gregory ^a   Spicer, Timothy ^a   Chase, Peter ^a   Fallahi, Mohammad ^a   Hodder, Peter ^a   Weissmann, Charles ^a   Lasmézas, Corinne Ida ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b Oncological Dispensary Histopathology   (Azerbaijan)

^c OPKO Health Inc   (United States)

Author keywords

High throughput screening; Prion therapeutics; Protein misfolding

Indexed keywords

ASTEMIZOLE; MESSENGER RNA; PRION PROTEIN; TACROLIMUS;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; BIOTINYLATION; CELL SURFACE; CONTROLLED STUDY; DRUG EFFICACY; DRUG SCREENING; HAY FEVER; HUMAN; MOUSE; NEUROBLASTOMA CELL; NONHUMAN; PHARMACOPHORE; PRION DISEASE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SINGLE DRUG DOSE; SURVIVAL TIME;

ANIMALS; ASTEMIZOLE; AUTOPHAGY; BLOTTING, WESTERN; CELL LINE, TUMOR; DRUG DISCOVERY; DRUG EVALUATION, PRECLINICAL; FLUORESCENCE RESONANCE ENERGY TRANSFER; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; KAPLAN-MEIER ESTIMATE; MICE; MICE, INBRED C57BL; PRION DISEASES; PRIONS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TACROLIMUS;

MUS;

EID: 84876818146     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1303510110     Document Type: Article

References (57)

1. Prusiner SB (1982) Novel proteinaceous infectious particles cause scrapie. Science 216(4542):136-144.
2. Will RG, et al. (1996) A new variant of Creutzfeldt-Jakob disease in the UK. Lancet 347(9006):921-925.
3. Lasmézas CI, et al. (1996) BSE transmission to macaques. Nature 381(6585):743-744.
4. World Health Organization (2012) Variant Creutzfeldt-Jakob disease. Available at http://www.who.int/mediacentre/factsheets/fs180/en/. Accessed March 14, 2013.
5. Hewitt PE, Llewelyn CA, Mackenzie J, Will RG (2006) Creutzfeldt-Jakob disease and blood transfusion: Results of the UK Transfusion Medicine Epidemiological Review study. Vox Sang 91(3):221-230.
6. Trevitt CR, Collinge J (2006) A systematic review of prion therapeutics in experimental models. Brain 129(Pt 9):2241-2265.
7. Weissmann C, Aguzzi A (2005) Approaches to therapy of prion diseases. Annu Rev Med 56:321-344.
8. Brown P (2009) An historical perspective on efforts to treat transmissible spongiform encephalopathy. CNS Neurol Disord Drug Targets 8(5):316-322.
9. Kocisko DA, et al. (2003) New inhibitors of scrapie-associated prion protein formation in a library of 2000 drugs and natural products. J Virol 77(19):10288-10294.
10. Bertsch U, et al. (2005) Systematic identification of antiprion drugs by high-throughput screening based on scanning for intensely fluorescent targets. J Virol 79(12):7785-7791.
11. Heal W, et al. (2007) Library synthesis and screening: 2, 4-diphenylthiazoles and 2, 4-diphenyloxazoles as potential novel prion disease therapeutics. J Med Chem 50(6): 1347-1353.
12. Kimata A, et al. (2007) New series of antiprion compounds: Pyrazolone derivatives have the potent activity of inhibiting protease-resistant prion protein accumulation. J Med Chem 50(21):5053-5056.
13. Ghaemmaghami S, May BC, Renslo AR, Prusiner SB (2010) Discovery of 2-amino-thiazoles as potent antiprion compounds. J Virol 84(7):3408-3412.
14. Geissen M, et al. (2011) From high-throughput cell culture screening to mouse model: identification of new inhibitor classes against prion disease. ChemMedChem 6(10): 1928-1937.
15. Büeler H, et al. (1993) Mice devoid of PrP are resistant to scrapie. Cell 73(7):1339-1347.
16. Manson JC, Clarke AR, McBride PA, McConnell I, Hope J (1994) PrP gene dosage determines the timing but not the final intensity or distribution of lesions in scrapie pathology. Neurodegeneration 3(4):331-340.
17. Sakaguchi S, et al. (1995) Accumulation of proteinase K-resistant prion protein (PrP) is restricted by the expression level of normal PrP in mice inoculated with a mouse-adapted strain of the Creutzfeldt-Jakob disease agent. J Virol 69(12):7586-7592.
18. Mallucci G, et al. (2003) Depleting neuronal PrP in prion infection prevents disease and reverses spongiosis. Science 302(5646):871-874.
19. White MD, et al. (2008) Single treatment with RNAi against prion protein rescues early neuronal dysfunction and prolongs survival in mice with prion disease. Proc Natl Acad Sci USA 105(29):10238-10243.
20. Wuertzer CA, Sullivan MA, Qiu X, Federoff HJ (2008) CNS delivery of vectored prion-specific single-chain antibodies delays disease onset. Mol Ther 16(3):481-486.
21. Büeler H, et al. (1994) High prion and PrPSc levels but delayed onset of disease in scrapie-inoculated mice heterozygous for a disrupted PrP gene. Mol Med 1(1):19-30.
22. Tremblay P, et al. (1998) Doxycycline control of prion protein transgene expression modulates prion disease in mice. Proc Natl Acad Sci USA 95(21):12580-12585.
23. Pfeifer A, et al. (2006) Lentivector-mediated RNAi efficiently suppresses prion protein and prolongs survival of scrapie-infected mice. J Clin Invest 116(12):3204-3210.
24. Lasmézas CI (2003) Putative functions of PrP(C). Br Med Bull 66:61-70.
25. Béland M, Roucou X (2012) The prion protein unstructured N-terminal region is a broad-spectrum molecular sensor with diverse and contrasting potential functions. J Neurochem 120(6):853-868.
26. Büeler H, et al. (1992) Normal development and behaviour of mice lacking the neu-ronal cell-surface PrP protein. Nature 356(6370):577-582.
27. Manson JC, et al. (1994) 129/Ola mice carrying a null mutation in PrP that abolishes mRNA production are developmentally normal. Mol Neurobiol 8(2-3):121-127.
28. Richt JA, et al. (2007) Production of cattle lacking prion protein. Nat Biotechnol 25(1): 132-138.
29. Yu G, et al. (2009) Generation of goats lacking prion protein. Mol Reprod Dev 76(1):3.
30. Bremer J, et al. (2010) Axonal prion protein is required for peripheral myelin maintenance. Nat Neurosci 13(3):310-318.
31. Mallucci GR, et al. (2007) Targeting cellular prion protein reverses early cognitive deficits and neurophysiological dysfunction in prion-infected mice. Neuron 53(3): 325-335.
32. Vey M, et al. (1996) Subcellular colocalization of the cellular and scrapie prion proteins in caveolae-like membranous domains. Proc Natl Acad Sci USA 93(25):14945-14949.
33. Caughey B, Race RE, Ernst D, Buchmeier MJ, Chesebro B (1989) Prion protein biosynthesis in scrapie-infected and uninfected neuroblastoma cells. J Virol 63(1): 175-181.
34. Enari M, Flechsig E, Weissmann C (2001) Scrapie prion protein accumulation by scrapie-infected neuroblastoma cells abrogated by exposure to a prion protein antibody. Proc Natl Acad Sci USA 98(16):9295-9299.
35. Zhang JH, Chung TD, Oldenburg KR (1999) A simple statistical parameter for use in evaluation and validation of high throughput screening assays. J Biomol Screen 4(2): 67-73.
36. US Pharmacopeia l Convention (2005) USP Dictionary.
37. Romano S, et al. (2010) FK506 binding proteins as targets in anticancer therapy. Anticancer Agents Med Chem 10(9):651-656.
38. Aguib Y, et al. (2009) Autophagy induction by trehalose counteracts cellular prion infection. Autophagy 5(3):361-369.
39. Heiseke A, Aguib Y, Riemer C, Baier M, Schätzl HM (2009) Lithium induces clearance of protease resistant prion protein in prion-infected cells by induction of autophagy. J Neurochem 109(1):25-34.
40. Oelschlegel AM, Fallahi M, Ortiz-Umpierre S, Weissmann C (2012) The extended cell panel assay characterizes the relationship of prion strains RML, 79A, and 139A and reveals conversion of 139A to 79A-like prions in cell culture. J Virol 86(9):5297-5303.
41. Krämer BK, et al. (2012) Tacrolimus-based, steroid-free regimens in renal transplantation: 3-year follow-up of the ATLAS trial. Transplantation 94(5):492-498.
42. Imai, T, et al. (2012) Early effect of tacrolimus in improving excitation-contraction coupling in myasthenia gravis. Clin Neurophysiol 123(9):1886-1890.
43. Mukherjee A, et al. (2010) Calcineurin inhibition at the clinical phase of prion disease reduces neurodegeneration, improves behavioral alterations and increases animal survival. PLoS Pathog 6(10):e1001138.
44. Venkataramanan R, et al. (1995) Clinical pharmacokinetics of tacrolimus. Clin Phar-macokinet 29(6):404-430.
45. Richards DM, Brogden RN, Heel RC, Speight TM, Avery GS (1984) Astemizole. A review of its pharmacodynamic properties and therapeutic efficacy. Drugs 28(1):38-61.
46. Freireich EJ, Gehan EA, Rall DP, Schmidt LH, Skipper HE (1966) Quantitative comparison of toxicity of anticancer agents in mouse, rat, hamster, dog, monkey, and man. Cancer Chemother Rep 50(4):219-244.
47. Vu K, Gelli A (2010) Astemizole and an analogue promote fungicidal activity of flu-conazole against Cryptococcus neoformans var. grubii and Cryptococcus gattii. Med Mycol 48(2):255-262.
48. Chong CR, Chen X, Shi L, Liu JO, Sullivan DJ, Jr. (2006) A clinical drug library screen identifies astemizole as an antimalarial agent. Nat Chem Biol 2(8):415-416.
49. Rojo LE, Alzate-Morales J, Saavedra IN, Davies P, Maccioni RB (2010) Selective interaction of lansoprazole and astemizole with tau polymers: Potential new clinical use in diagnosis of Alzheimer's disease. J Alzheimers Dis 19(2):573-589.
50. World Health Organization (1999) Astemizole: Voluntary Withdrawal: Janssen, USA. WHO Pharmaceuticals Newsletter Nos. 7 and 8. Available at http://apps.who.int/medicinedocs/fr/d/Js2269e/5.html. Accessed March 14, 2013.
51. Janssens MM (1993) Astemizole. A nonsedating antihistamine with fast and sustained activity. Clin Rev Allergy 11(1):35-63.
52. World Health Organization (1999) Astemizole: OTC Formulation Withdrawn: UK. WHO Pharmaceuticals Newsletter Nos. 1 and 2. Available at http://apps.who.int/medicinedocs/en/d/Js2268e/6.3.html. Accessed March 14, 2013.
53. Lindquist M, Edwards IR (1997) Risks of non-sedating antihistamines. Lancet 349(9061): 1322.
54. Martinez-Vicente M, Cuervo AM (2007) Autophagy and neurodegeneration: When the cleaning crew goes on strike. Lancet Neurol 6(4):352-361.
55. Laurén J, Gimbel DA, Nygaard HB, Gilbert JW, Strittmatter SM (2009) Cellular prion protein mediates impairment of synaptic plasticity by amyloid-beta oligomers. Nature 457(7233):1128-1132.
56. Kudo W, et al. (2012) Cellular prion protein is essential for oligomeric amyloid-β-induced neuronal cell death. Hum Mol Genet 21(5):1138-1144.
57. Gimbel DA, et al. (2010) Memory impairment in transgenic Alzheimer mice requires cellular prion protein. J Neurosci 30(18):6367-6374.