Calcineurin inhibition at the clinical phase of prion disease reduces neurodegeneration, improves behavioral alterations and increases animal survival

PLoS Pathogens

Volumn 6, Issue 10, 2010, Pages

  Mukherjee, Abhisek ^a,b   Morales Scheihing, Diego ^a   Gonzalez Romero, Dennisse ^a,b   Green, Kristi ^b   Taglialatela, Giulio ^b   Soto, Claudio ^a,b  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b University of Texas Medical Branch School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCINEURIN; RAPAMYCIN; TACROLIMUS;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME INHIBITION; NERVE CELL; NERVE DEGENERATION; NEUROTOXICITY; NONHUMAN; PRION DISEASE; SURVIVAL; SURVIVAL TIME;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN; CALCINEURIN; CALCIUM SIGNALING; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; INJECTIONS, INTRAPERITONEAL; MICE; MICE, INBRED C57BL; NERVE DEGENERATION; PRION DISEASES; SURVIVAL ANALYSIS; TACROLIMUS;

ANIMALIA; MUS;

EID: 78449257695     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1001138     Document Type: Article

References (65)

1. Aguzzi A, Calella AM (2009) Prions: protein aggregation and infectious diseases. Physiol Rev 89: 1105-1152.
2. Collinge J (2001) Prion diseases of humans and animals: their causes and molecular basis. Annu Rev Neurosci 24: 519-550.
3. Bruce ME, Will RG, Ironside JW, McConnell I, Drummond D, et al. (1997) Transmissions to mice indicate that 'new variant' CJD is caused by the BSE agent. Nature 389: 498-501.
4. Collinge J, Sidle KC, Meads J, Ironside J, Hill AF (1996) Molecular analysis of prion strain variation and the aetiology of 'new variant' CJD. Nature 383: 685-690.
5. Aguzzi A, Glatzel M (2004) vCJD tissue distribution and transmission by transfusion-a worst-case scenario coming true? Lancet 363: 411-412.
6. Llewellyn CA, Hewitt P, Knight RS, Amar K, Cousens S, et al. (2004) Possible transmission of variant Creutzfeldt-Jakob disease by blood transfusion. Lancet 363: 417-421.
7. Peden AH, Head MW, Ritchie DL, Bell JE, Ironside JW (2004) Preclinical vCJD after blood transfusion in a PRNP codon 129 heterozygous patient. Lancet 364: 527-529.
8. Trevitt CR, Collinge J (2006) A systematic review of prion therapeutics in experimental models. Brain 129: 2241-2265.
9. Weissmann C, Aguzzi A (2005) Approaches to Therapy of Prion Diseases. Annu Rev Med 56: 321-344.
10. Cashman NR, Caughey B (2004) Prion diseases - close to effective therapy? Nat Rev Drug Discov 3: 874-884.
11. Hetz C, Russelakis-Carneiro M, Maundrell K, Castilla J, Soto C (2003) Caspase-12 and endoplasmic reticulum stress mediate neurotoxicity of pathological prion protein. EMBO J 22: 5435-5445.
12. Hetz CA, Soto C (2006) Stressing Out the ER: A Role of the Unfolded Protein Response in Prion-Related Disorders. Curr Mol Med 6: 37-43.
13. Yoo BC, Krapfenbauer K, Cairns N, Belay G, Bajo M, et al. (2002) Overexpressed protein disulfide isomerase in brains of patients with sporadic Creutzfeldt-Jakob disease. Neurosci Lett 334: 196-200.
14. Hetz C, Russelakis-Carneiro M, Walchli S, Carboni S, Vial-Knecht E, et al. (2005) The disulfide isomerase Grp58 is a protective factor against prion neurotoxicity. J Neurosci 25: 2793-2802.
15. Mansuy IM (2003) Calcineurin in memory and bidirectional plasticity. Biochem Biophys Res Commun 311: 1195-1208.
16. Goto S, Matsukado Y, Mihara Y, Inoue N, Miyamoto E (1986) The distribution of calcineurin in rat brain by light and electron microscopic immunohistochemistry and enzyme-immunoassay. Brain Res 397: 161-172.
17. Goto S, Matsukado Y, Mihara Y, Inoue N, Miyamoto E (1986) Calcineurin in human brain and its relation to extrapyramidal system. Immunohistochemical study on postmortem human brains. Acta Neuropathol 72: 150-156.
18. Wang HG, Pathan N, Ethell IM, Krajewski S, Yamaguchi Y, et al. (1999) Ca2+- induced apoptosis through calcineurin dephosphorylation of BAD. Science 284: 339-343.
19. Groth RD, Dunbar RL, Mermelstein PG (2003) Calcineurin regulation of neuronal plasticity. Biochem Biophys Res Commun 311: 1159-1171.
20. Scott LJ, McKeage K, Keam SJ, Plosker GL (2003) Tacrolimus: a further update of its use in the management of organ transplantation. Drugs 63: 1247-1297.
21. Liu J, Farmer JD, Jr., Lane WS, Friedman J, Weissman I, et al. (1991) Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes. Cell 66: 807-815.
22. Rogers TB, Inesi G, Wade R, Lederer WJ (1995) Use of thapsigargin to study Ca2+ homeostasis in cardiac cells. Biosci Rep 15: 341-349.
23. Guenther K, Deacon RM, Perry VH, Rawlins JN (2001) Early behavioural changes in scrapie-affected mice and the influence of dapsone. Eur J Neurosci 14: 401-409.
24. Betmouni S, Clements J, Perry VH (1999) Vacuolation in murine prion disease: an informative artifact. Curr Biol 9: R677-R679.
25. Siskova Z, Page A, O'Connor V, Perry VH (2009) Degenerating synaptic boutons in prion disease: microglia activation without synaptic stripping. Am J Pathol 175: 1610-1621.
26. Perry VH, Cunningham C, Boche D (2002) Atypical inflammation in the central nervous system in prion disease. Curr Opin Neurol 15: 349-354.
27. Aramburu J, Heitman J, Crabtree GR (2004) Calcineurin: a central controller of signalling in eukaryotes. EMBO Rep 5: 343-348.
28. Mullen RJ, Buck CR, Smith AM (1992) NeuN, a neuronal specific nuclear protein in vertebrates. Development 116: 201-211.
29. Schmued LC, Hopkins KJ (2000) Fluoro-Jade: novel fluorochromes for detecting toxicant-induced neuronal degeneration. Toxicol Pathol 28: 91-99.
30. Soto C (2004) Diagnosing prion diseases: needs, challenges and hopes. Nat Rev Microbiol 2: 809-819.
31. Sim VL, Caughey B (2009) Recent advances in prion chemotherapeutics. Infect Disord Drug Targets 9: 81-91.
32. Doh-Ura K, Iwaki T, Caughey B (2000) Lysosomotropic agents and cysteine protease inhibitors inhibit scrapie-associated prion protein accumulation. J Virol 74: 4894-4897.
33. Korth C, May BC, Cohen FE, Prusiner SB (2001) Acridine and phenothiazine derivatives as pharmacotherapeutics for prion disease. Proc Natl Acad Sci U S A 98: 9836-9841.
34. Barret A, Tagliavini F, Forloni G, Bate C, Salmona M, et al. (2003) Evaluation of quinacrine treatment for prion diseases. J Virol 77: 8462-8469.
35. Doh-Ura K, Ishikawa K, Murakami-Kubo I, Sasaki K, Mohri S, et al. (2004) Treatment of transmissible spongiform encephalopathy by intraventricular drug infusion in animal models. J Virol 78: 4999-5006.
36. Nakajima M, Yamada T, Kusuhara T, Furukawa H, Takahashi M, et al. (2004) Results of quinacrine administration to patients with Creutzfeldt-Jakob disease. Dement Geriatr Cogn Disord 17: 158-163.
37. Collinge J, Gorham M, Hudson F, Kennedy A, Keogh G, et al. (2009) Safety and efficacy of quinacrine in human prion disease (PRION-1 study): a patientpreference trial. Lancet Neurol 8: 334-344.
38. Mange A, Nishida N, Milhavet O, McMahon HE, Casanova D, et al. (2000) Amphotericin B inhibits the generation of the scrapie isoform of the prion protein in infected cultures. J Virol 74: 3135-3140.
39. Adjou KT, Privat N, Demart S, Deslys JP, Seman M, et al. (2000) MS-8209, an amphotericin B analogue, delays the appearance of spongiosis, astrogliosis and PrPres accumulation in the brain of scrapie-infected hamsters. J Comp Pathol 122: 3-8.
40. McKenzie D, Kaczkowski J, Marsh R, Aiken J (1994) Amphotericin B delays both scrapie agent replication and PrP-res accumulation early in infection. J Virol 68: 7534-7536.
41. Masullo C, Macchi G, Xi YG, Pocchiari M (1992) Failure to ameliorate Creutzfeldt-Jakob disease with amphotericin B therapy. J Infect Dis 165: 784-785.
42. Caughey B, Raymond GJ (1993) Sulfated polyanion inhibition of scrapieassociated PrP accumulation in cultured cells. J Virol 67: 643-650.
43. Diringer H, Ehlers B (1991) Chemoprophylaxis of scrapie in mice. J Gen Virol 72: 457-460.
44. Ladogana A, Casaccia P, Ingrosso L, Cibati M, Salvatore M, et al. (1992) Sulphate polyanions prolong the incubation period of scrapie-infected hamsters. J Gen Virol 73: 661-665.
45. Bone I, Belton L, Walker AS, Darbyshire J (2008) Intraventricular pentosan polysulphate in human prion diseases: an observational study in the UK. Eur J Neurol 15: 458-464.
46. Terada T, Tsuboi Y, Obi T, Doh-Ura K, Murayama S, et al. (2009) Less protease-resistant PrP in a patient with sporadic CJD treated with intraventricular pentosan polysulphate. Acta Neurol Scand 121: 127-130.
47. Tsuboi Y, Doh-Ura K, Yamada T (2009) Continuous intraventricular infusion of pentosan polysulfate: clinical trial against prion diseases. Neuropathology 29: 632-636.
48. Whittle IR, Knight RS, Will RG (2006) Unsuccessful intraventricular pentosan polysulphate treatment of variant Creutzfeldt-Jakob disease. Acta Neurochir (Wien) 148: 677-679.
49. Mansuy IM (2003) Calcineurin in memory and bidirectional plasticity. Biochem Biophys Res Commun 311: 1195-1208.
50. Pritchard DI (2005) Sourcing a chemical succession for cyclosporin from parasites and human pathogens. Drug Discov Today 10: 688-691.
51. Saunders RN, Metcalfe MS, Nicholson ML (2001) Rapamycin in transplantation: a review of the evidence. Kidney Int 59: 3-16.
52. Matus S, Lisbona F, Torres M, Leon C, Thielen P, et al. (2008) The stress rheostat: an interplay between the unfolded protein response (UPR) and autophagy in neurodegeneration. Curr Mol Med 8: 157-172.
53. Reese LC, Zhang W, Dineley KT, Kayed R, Taglialatela G (2008) Selective induction of calcineurin activity and signaling by oligomeric amyloid beta. Aging Cell 7: 824-835.
54. Ghribi O (2006) The role of the endoplasmic reticulum in the accumulation of beta-amyloid peptide in Alzheimer's disease. Curr Mol Med 6: 119-133.
55. Rao RV, Bredesen DE (2004) Misfolded proteins, endoplasmic reticulum stress and neurodegeneration. Curr Opin Cell Biol 16: 653-662.
56. Abdul HM, Sama MA, Furman JL, Mathis DM, Beckett TL, et al. (2009) Cognitive decline in Alzheimer's disease is associated with selective changes in calcineurin/NFAT signaling. J Neurosci 29: 12957-12969.
57. Dineley KT, Hogan D, Zhang WR, Taglialatela G (2007) Acute inhibition of calcineurin restores associative learning and memory in Tg2576 APP transgenic mice. Neurobiol Learn Mem 88: 217-224.
58. Taglialatela G, Hogan D, Zhang WR, Dineley KT (2009) Intermediate- and long-term recognition memory deficits in Tg2576 mice are reversed with acute calcineurin inhibition. Behav Brain Res 200: 95-99.
59. Chen QS, Wei WZ, Shimahara T, Xie CW (2002) Alzheimer amyloid betapeptide inhibits the late phase of long-term potentiation through calcineurindependent mechanisms in the hippocampal dentate gyrus. Neurobiol Learn Mem 77: 354-371.
60. Banks WA, Robinson SM, Diaz-Espinoza R, Urayama A, Soto C (2009) Transport of prion protein across the blood-brain barrier. Exp Neurol 218: 162-167.
61. Kimberlin RH (1976) Experimental Scrapie in Mouse - Review of An Important Model Disease. Science Progress 63: 461-481.
62. Castilla J, Morales R, Saa P, Barria M, Gambetti P, et al. (2008) Cell-free propagation of prion strains. EMBO J 27: 2557-2566.
63. Castilla J, Saá P, Hetz C, Soto C (2005) In vitro generation of infectious scrapie prions. Cell 121: 195-206.
64. Deininger MH, Weinschenk T, Meyermann R, Schluesener HJ (2003) The allograft inflammatory factor-1 in Creutzfeldt-Jakob disease brains. Neuropathol Appl Neurobiol 29: 389-399.
65. Liu F, Schafer DP, McCullough LD (2009) TTC, Fluoro-Jade B and NeuN staining confirm evolving phases of infarction induced by middle cerebral artery occlusion. J Neurosci Methods 179: 1-8.