Synaptic dysfunction in prion diseases: A trafficking problem?

International Journal of Cell Biology

Volumn , Issue , 2013, Pages

  Senatore, Assunta ^a   Restelli, Elena ^a   Chiesa, Roberto ^a  

^a MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84893868831     PISSN: 16878876     EISSN: 16878884     Source Type: Journal    
DOI: 10.1155/2013/543803     Document Type: Review

References (127)

1. Collinge J., Prion diseases of humans and animals: their causes and molecular basis. Annual Review of Neuroscience 2001 24 519 550 10.1146/annurev.neuro.24.1.519 (Pubitemid 32695238)
2. Watts J. C., Balachandran A., Westaway D., The expanding universe of prion diseases. PLOS Pathogens 2006 2 3 e26 10.1371/journal.ppat.0020026
3. Knight R. S., Will R. G., Prion diseases. Journal of Neurology, Neurosurgery & Psychiatry 2004 75 supplement 1 i36 i42
4. Brown P., Gibbs C. J. Jr., Rodgers-Johnson P., Asher D. M., Sulima M. P., Bacote A., Goldfarb L. G., Gajdusek D. C., Human spongiform encephalopathy: the National Institutes of Health series of 300 cases of experimentally transmitted disease. Annals of Neurology 1994 35 5 513 529 10.1002/ana.410350504 (Pubitemid 24153834)
5. Liberski P. P., Sikorska B., Brown P., Kuru: the first prion disease. Advances in Experimental Medicine and Biology 2012 724 143 153 10.1007/978-1-4614-0653-2-12
6. Brown P., Preece M., Brandel J.-P., Sato T., McShane L., Zerr I., Fletcher A., Will R. G., Pocchiari M., Cashman N. R., D'Aignaux J. H., Cervenáková L., Fradkin J., Schonberger L. B., Collins S. J., Iatrogenic Creutzfeldt-Jakob disease at the millennium. Neurology 2000 55 8 1075 1081 2-s2.0-0034711176
7. Ironside J. W., Variant Creutzfeldt-Jakob disease: an update. Folia Neuropathologica 2012 50 1 50 56 2-s2.0-84860337641
8. Prusiner S. B., Novel proteinaceous infectious particles cause scrapie. Science 1982 216 4542 136 144 2-s2.0-0020321767 (Pubitemid 12089840)
9. Westergard L., Christensen H. M., Harris D. A., The cellular prion protein (PrP C): its physiological function and role in disease. Biochimica et Biophysica Acta 2007 1772 6 629 644 2-s2.0-34249936265 10.1016/j.bbadis.2007.02. 011 (Pubitemid 46880208)
10. Chiesa R., Harris D. A., Fishing for prion protein function. PLoS Biology 2009 7 3 e75 2-s2.0-66149117047 10.1371/journal.pbio.1000075
11. Biasini E., Turnbaugh J. A., Unterberger U., Harris D. A., Prion protein at the crossroads of physiology and disease. Trends in Neurosciences 2012 35 2 92 103 2-s2.0-84856411525 10.1016/j.tins.2011.10.002
12. Campana V., Sarnataro D., Zurzolo C., The highways and byways of prion protein trafficking. Trends in Cell Biology 2005 15 2 102 111 2-s2.0-13244295520 10.1016/j.tcb.2004.12.002 (Pubitemid 40188220)
13. Pan K.-M., Baldwin M., Nguyen J., Gasset M., Serban A., Groth D., Mehlhorn I., Huang Z., Fletterick R. J., Cohen F. E., Prusiner S. B., Conversion of α -helices into β -sheets features in the formation of the scrapie prion proteins. Proceedings of the National Academy of Sciences of the United States of America 1993 90 23 10962 10966 2-s2.0-0027332116 10.1073/pnas.90.23.10962 (Pubitemid 23354348)
14. Safar J., Wille H., Itri V., Groth D., Serban H., Torchia M., Cohen F. E., Prusiner S. B., Eight prion strains have PrP(Sc) molecules with different conformations. Nature Medicine 1998 4 10 1157 1165 2-s2.0-0031720905 10.1038/2654 (Pubitemid 28468829)
15. Goold R., Rabbanian S., Sutton L., Andre R., Arora P., Moonga J., Clarke A. R., Schiavo G., Jat P., Collinge J., Tabrizi S. J., Rapid cell-surface prion protein conversion revealed using a novel cell system. Nature Communications 2011 2 1 281 2-s2.0-79955050582 10.1038/ncomms1282
16. Borchelt D. R., Taraboulos A., Prusiner S. B., Evidence for synthesis of scrapie prion proteins in the endocytic pathway. Journal of Biological Chemistry 1992 267 23 16188 16199 2-s2.0-0026775909
17. Marijanovic Z., Caputo A., Campana V., Zurzolo C., Identification of an intracellular site of prion conversion. PLoS Pathogens 2009 5 5 2-s2.0-67249099366 10.1371/journal.ppat.1000426 e1000426
18. Come J. H., Fraser P. E., Lansbury P. T. Jr., A kinetic model for amyloid formation in the prion diseases: importance of seeding. Proceedings of the National Academy of Sciences of the United States of America 1993 90 13 5959 5963 2-s2.0-0027270578 (Pubitemid 23191433)
19. Silveira J. R., Raymond G. J., Hughson A. G., Race R. E., Sim V. L., Hayes S. F., Caughey B., The most infectious prion protein particles. Nature 2005 437 7056 257 261 2-s2.0-24644448839 10.1038/nature03989 (Pubitemid 41294488)
20. Mastrianni J. A., The genetics of prion diseases. Genetics in Medicine 2010 12 4 187 195 2-s2.0-77951499689 10.1097/GIM.0b013e3181cd7374
21. Puoti G., Bizzi A., Forloni G., Safar J. G., Tagliavini F., Gambetti P., Sporadic human prion diseases: molecular insights and diagnosis. Lancet Neurology 2012 11 7 618 628 10.1016/S1474-4422(12)70063-7
22. Goldfarb L. G., Petersen R. B., Tabaton M., Brown P., LeBlanc A. C., Montagna P., Cortelli P., Julien J., Vital C., Pendelbury W. W., Haltia M., Wills P. R., Hauw J. J., McKeever P. E., Monari L., Schrank B., Swergold G. D., Autilio-Gambetti L., Carleton Gajdusek D., Fatal familial insomnia and familial Creutzfeldt-Jakob disease: disease phenotype determined by a DNA polymorphism. Science 1992 258 5083 806 808 2-s2.0-0026496257
23. Ghetti B., Piccardo P., Frangione B., Bugiani O., Giaccone G., Young K., Prelli F., Farlow M. R., Dlouhy S. R., Tagliavini F., Prion protein amyloidosis. Brain Pathology 1996 6 2 127 145 2-s2.0-15844415943 (Pubitemid 26161871)
24. Jansen C., Parchi P., Capellari S., Vermeij A. J., Corrado P., Baas F., Strammiello R., Van Gool W. A., Van Swieten J. C., Rozemuller A. J. M., Prion protein amyloidosis with divergent phenotype associated with two novel nonsense mutations in PRNP. Acta Neuropathologica 2010 119 2 189 197 2-s2.0-77449089995 10.1007/s00401-009-0609-x
25. Chiesa R., Harris D. A., Prion diseases: what is the neurotoxic molecule? Neurobiology of Disease 2001 8 5 743 763 2-s2.0-0035168351 10.1006/nbdi.2001. 0433 (Pubitemid 33055592)
26. Mallucci G. R., Prion neurodegeneration: starts and stops at the synapse. Prion 2009 3 4 195 201 2-s2.0-74249085705
27. Brown P., The phantasmagoric immunology of transmissible spongiform encephalopathy. Research Publications 1990 68 305 313 2-s2.0-0024984954
28. Berg L. J., Insights into the role of the immune system in prion diseases. Proceedings of the National Academy of Sciences of the United States of America 1994 91 2 429 432 2-s2.0-0028047285 (Pubitemid 24041414)
29. Hengartner M. O., The biochemistry of apoptosis. Nature 2000 407 6805 770 776 2-s2.0-0034641918 10.1038/35037710
30. Forloni G., Angeretti N., Chiesa R., Monzani E., Salmona M., Bugiani O., Tagliavini F., Neurotoxicity of a prion protein fragment. Nature 1993 362 6420 543 546 2-s2.0-0027483615 10.1038/362543a0 (Pubitemid 23113029)
31. Fairbairn D. W., Carnahan K. G., Thwaits R. N., Grigsby R. V., Holyoak G. R., O'Neill K. L., Detection of apoptosis induced DNA cleavage in scrapie-infected sheep brain. FEMS Microbiology Letters 1994 115 2-3 341 346 2-s2.0-0028008896
32. Giese A., Groschup M. H., Hess B., Kretzschmar H. A., Neuronal cell death in scrapie-infected mice is due to apoptosis. Brain Pathology 1995 5 3 213 221 2-s2.0-0029085515
33. Lucassen P. J., Detection of apoptosis in murine scrapie. Neuroscience Letters 1995 198 3 185 188 2-s2.0-0028867319 10.1016/0304-3940(95)11995-9
34. Lucas M., Izquierdo G., Muñoz C., Solano F., Internucleosomal breakdown of the DNA of brain cortex in human spongiform encephalopathy. Neurochemistry International 1997 31 2 241 244 2-s2.0-0030908160 10.1016/S0197-0186(96)00153-2 (Pubitemid 27267964)
35. Williams A., Lucassen P. J., Ritchie D., Bruce M., PrP deposition, microglial activation, and neuronal apoptosis in murine scrapie. Experimental Neurology 1997 144 2 433 438 2-s2.0-0031127379 10.1006/exnr.1997.6424 (Pubitemid 27224571)
36. Dorandeu A., Wingertsmann L., Chrétien F., Delisle M., Vital C., Parchi P., Montagna P., Lugaresi E., Ironside J. W., Budka H., Gambetti P., Gray F., Neuronal apoptosis in fatal familial insomnia. Brain Pathology 1998 8 3 531 537 2-s2.0-7144251862 (Pubitemid 28308852)
37. Gray F., Chrétien F., Adle-Biassette H., Dorandeu A., Ereau T., Delisle M., Kopp N., Ironside J. W., Vital C., Neuronal apoptosis in Creutzfeldt-Jakob disease. Journal of Neuropathology and Experimental Neurology 1999 58 4 321 328 2-s2.0-0345654322 (Pubitemid 29187894)
38. Jesionek-Kupnicka D., Buczyński J., Kordek R., Liberski P. P., Neuronal loss and apoptosis in experimental Creutzfeldt-Jakob disease in mice. Folia Neuropathologica 1999 37 4 283 286 2-s2.0-0033255161
39. Jamieson E., Jeffrey M., Ironside J. W., Fraser J. R., Apoptosis and dendritic dysfunction precede prion protein accumulation in 87V scrapie. NeuroReport 2001 12 10 2147 2153 2-s2.0-0035919758 (Pubitemid 32646262)
40. Jesionek-Kupnicka D., Kordek R., Buczyński J., Liberski P. P., Apoptosis in relation to neuronal loss in experimental Creutzfeldt-Jakob disease in mice. Acta Neurobiologiae Experimentalis 2001 61 1 13 19 2-s2.0-0035119377 (Pubitemid 32187883)
41. Ferrer I., Synaptic pathology and cell death in the cerebellum in Creutzfeldt-Jakob disease. Cerebellum 2002 1 3 213 222 2-s2.0-0042734442 10.1080/14734220260418448 (Pubitemid 44133831)
42. Sisó S., Puig B., Varea R., Vidal E., Acín C., Prinz M., Montrasio F., Badiola J., Aguzzi A., Pumarola M., Ferrer I., Abnormal synaptic protein expression and cell death in murine scrapie. Acta Neuropathologica 2002 103 6 615 626 2-s2.0-0036939211 10.1007/s00401-001-0512-6 (Pubitemid 36067510)
43. Serrano C., Lyahyai J., Bolea R., Varona L., Monleón E., Badiola J. J., Zaragoza P., Martín-Burriel I., Distinct spatial activation of intrinsic and extrinsic apoptosis pathways in natural scrapie: association with prion-related lesions. Veterinary Research 2009 40 5 42 2-s2.0-67650976617 10.1051/vetres/2009024
44. Kovacs G. G., Budka H., Distribution of apoptosis-related proteins in sporadic Creutzfeldt-Jakob disease. Brain Research 2010 1323 192 199 2-s2.0-77953133811 10.1016/j.brainres.2010.01.089
45. Drew S. C., Haigh C. L., Klemm H. M. J., Masters C. L., Collins S. J., Barnham K. J., Lawson V. A., Optical imaging detects apoptosis in the brain and peripheral organs of prion-infected mice. Journal of Neuropathology and Experimental Neurology 2011 70 2 143 150 2-s2.0-79251594896 10.1097/NEN. 0b013e3182084a8c
46. Chiesa R., Drisaldi B., Quaglio E., Migheli A., Piccardo P., Ghetti B., Harris D. A., Accumulation of protease-resistant prion protein (PrP) and apoptosis of cerebellar granule cells in transgenic mice expressing a PrP insertional mutation. Proceedings of the National Academy of Sciences of the United States of America 2000 97 10 5574 5579 2-s2.0-0034625069 10.1073/pnas.97.10.5574 (Pubitemid 30313760)
47. Schätzl H. M., Laszlo L., Holtzman D. M., Tatzelt J., Dearmond S. J., Weiner R. I., Mobley W. C., Prusiner S. B., A hypothalamic neuronal cell line persistently infected with scrapie prions exhibits apoptosis. Journal of Virology 1997 71 11 8821 8831 2-s2.0-0037611374 (Pubitemid 27446466)
48. Cronier S., Laude H., Peyrin J., Prions can infect primary cultured neurons and astrocytes and promote neuronal cell death. Proceedings of the National Academy of Sciences of the United States of America 2004 101 33 12271 12276 2-s2.0-4344628202 10.1073/pnas.0402725101 (Pubitemid 39145433)
49. Falsig J., Sonati T., Herrmann U. S., Saban D., Li B., Arroyo K., Ballmer B., Liberski P. P., Aguzzi A., Prion pathogenesis is faithfully reproduced in cerebellar organotypic slice cultures. PLoS Pathogens 2012 8 11 e1002985 10.1371/journal.ppat.1002985
50. Coulpier M., Messiaen S., Hamel R., Fernández de Marco M., Lilin T., Eloit M., Bax deletion does not protect neurons from BSE-induced death. Neurobiology of Disease 2006 23 3 603 611 2-s2.0-33747200829 10.1016/j.nbd.2006.05.013 (Pubitemid 44234096)
51. Steele A. D., King O. D., Jackson W. S., Hetz C. A., Borkowski A. W., Thielen P., Wollmann R., Lindquist S., Diminishing apoptosis by deletion of bax or overexpression of Bcl-2 does not protect against infectious prion toxicity in vivo. Journal of Neuroscience 2007 27 47 13022 13027 2-s2.0-36348958583 10.1523/JNEUROSCI.3290-07.2007 (Pubitemid 350159568)
52. Steele A. D., Hetz C., Yi C. H., Jackson W. S., Borkowski A. W., Yuan J., Wollmann R. H., Lindquist S., Prion pathogenesis is independent of caspase-12. Prion 2007 1 4 243 247 2-s2.0-51649103992
53. Chiesa R., Piccardo P., Dossena S., Nowoslawski L., Roth K. A., Ghetti B., Harris D. A., Bax deletion prevents neuronal loss but not neurological symptoms in a transgenic model of inherited prion disease. Proceedings of the National Academy of Sciences of the United States of America 2005 102 1 238 243 2-s2.0-11844296730 10.1073/pnas.0406173102 (Pubitemid 40094459)
54. Tooze S. A., Schiavo G., Liaisons dangereuses: autophagy, neuronal survival and neurodegeneration. Current Opinion in Neurobiology 2008 18 5 504 515 2-s2.0-56249138284 10.1016/j.conb.2008.09.015
55. Levine B., Yuan J., Autophagy in cell death: an innocent convict? Journal of Clinical Investigation 2005 115 10 2679 2688 2-s2.0-25144506835 10.1172/JCI26390 (Pubitemid 41434392)
56. Gordy C., He Y. W., The crosstalk between autophagy and apoptosis: where does this lead? Protein & Cell 2012 3 1 17 27 10.1007/s13238-011-1127-x
57. Boellaard J. W., Schlote W., Tateishi J., Neuronal autophagy in experimental Creutzfeldt-Jakob's disease. Acta Neuropathologica 1989 78 4 410 418 2-s2.0-0024328518 (Pubitemid 19200591)
58. Boellaard J. W., Kao M., Schlote W., Diringer H., Neuronal autophagy in experimental scrapie. Acta Neuropathologica 1991 82 3 225 228 2-s2.0-0025744499
59. Jeffrey M., Scott J. R., Williams A., Fraser H., Ultrastructural features of spongiform encephalopathy transmitted to mice from three species of bovidae. Acta Neuropathologica 1992 84 5 559 569 2-s2.0-0026673455 10.1007/BF00304476
60. Liberski P. P., Yanagihara R., Gibbs C. J., Gajdusek D. C., Neuronal autophagic vacuoles in experimental scrapie and Creutzfeldt-Jakob disease. Acta Neuropathologica 1992 83 2 134 139 2-s2.0-0026526705
61. Sikorska B., Liberski P. P., Giraud P., Kopp N., Brown P., Autophagy is a part of ultrastructural synaptic pathology in Creutzfeldt-Jakob disease: a brain biopsy study. International Journal of Biochemistry and Cell Biology 2004 36 12 2563 2573 2-s2.0-4344656905 10.1016/j.biocel.2004.04.014 (Pubitemid 39119767)
62. Dron M., Bailly Y., Beringue V., Haeberlé A., Griffond B., Risold P., Tovey M. G., Laude H., Dandoy-Dron F., Scrg1 is induced in TSE and brain injuries, and associated with autophagy. European Journal of Neuroscience 2005 22 1 133 146 2-s2.0-23044439752 10.1111/j.1460-9568.2005.04172.x (Pubitemid 41059979)
63. Liberski P. P., Sikorska B., Gibson P., Brown P., Autophagy contributes to widespread neuronal degeneration in hamsters infected with the echigo-1 strain of creutzfeldt-jakob disease and mice infected with the fujisaki strain of gerstmann-sträussler-scheinker (GSS) syndrome. Ultrastructural Pathology 2011 35 1 31 36 2-s2.0-79251581863 10.3109/01913123.2010.527038
64. Xu Y., Tian C., Wang S. B., Xie W. L., Guo Y., Zhang J., Shi Q., Chen C., Dong X. P., Activation of the macroautophagic system in scrapie-infected experimental animals and human genetic prion diseases. Autophagy 2012 8 11 1604 1620 10.4161/auto.21482
65. Heiseke A., Aguib Y., Riemer C., Baier M., Schätzl H. M., Lithium induces clearance of protease resistant prion protein in prion-infected cells by induction of autophagy. Journal of Neurochemistry 2009 109 1 25 34 2-s2.0-61849102412 10.1111/j.1471-4159.2009.05906.x
66. Karapetyan Y. E., Sferrazza G. F., Zhou M., Ottenberg G., Spicer T., Chase P., Fallahi M., Hodder P., Weissmann C., Lasmezas C. I., 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 2013 110 17 7044 7049 10.1073/pnas.1303510110
67. Nakagaki T., Satoh K., Ishibashi D., Fuse T., Sano K., Kamatari Y. O., Kuwata K., Shigematsu K., Iwamaru Y., Takenouchi T., Kitani H., Nishida N., Atarashi R., FK506 reduces abnormal prion protein through the activation of autolysosomal degradation and prolongs survival in prion-infected mice. Autophagy 2013 9 9 1386 1394
68. Cortes C. J., Qin K., Cook J., Solanki A., Mastrianni J. A., Rapamycin delays disease onset and prevents PrP plaque deposition in a mouse model of Gerstmann-Sträussler-Scheinker disease. Journal of Neuroscience 2012 32 36 12396 12405 10.1523/JNEUROSCI.6189-11.2012
69. Aguib Y., Heiseke A., Gilch S., Riemer C., Baier M., Schätzl H. M., Ertmer A., Autophagy induction by trehalose counteracts cellular prion infection. Autophagy 2009 5 3 361 369 2-s2.0-65249103439 10.4161/auto.5.3.7662
70. Marzo L., Marijanovic Z., Browman D., Chamoun Z., Caputo A., Zurzolo C., 4-hydroxytamoxifen leads to PrP Sc clearance by conveying both PrP C and PrP Sc to lysosomes independently of autophagy. Journal of Cell Science 2013 126 part 6 1345 1354
71. Wong E., Cuervo A. M., Autophagy gone awry in neurodegenerative diseases. Nature Neuroscience 2010 13 7 805 811 2-s2.0-77954116814 10.1038/nn.2575
72. Belichenko P. V., Brown D., Jeffrey M., Fraser J. R., Dendritic and synaptic alterations of hippocampal pyramidal neurones in scrapie-infected mice. Neuropathology and Applied Neurobiology 2000 26 2 143 149 2-s2.0-0000158060 10.1046/j.1365-2990.2000.026002143.x (Pubitemid 30251387)
73. Jeffrey M., Halliday W. G., Bell J., Johnston A. R., Macleod N. K., Ingham C., Sayers A. R., Brown D. A., Fraser J. R., Synapse loss associated with abnormal PrP precedes neuronal degeneration in the scrapie-infected murine hippocampus. Neuropathology and Applied Neurobiology 2000 26 1 41 54 2-s2.0-0034016049 10.1046/j.1365-2990.2000.00216.x (Pubitemid 30145305)
74. Brown D., Belichenko P., Sales J., Jeffrey M., Fraser J. R., Early loss of dendritic spines in murine scrapie revealed by confocal analysis. NeuroReport 2001 12 1 179 183 2-s2.0-0035931496 (Pubitemid 32099051)
75. Gray B. C., Siskova Z., Perry V. H., O'Connor V., Selective presynaptic degeneration in the synaptopathy associated with ME7-induced hippocampal pathology. Neurobiology of Disease 2009 35 1 63 74 2-s2.0-67349280983 10.1016/j.nbd.2009.04.001
76. Siskova Z., Page A., O'Connor V., Perry V. H., Degenerating synaptic boutons in prion disease: microglia activation without synaptic stripping. American Journal of Pathology 2009 175 4 1610 1621 2-s2.0-73549119497 10.2353/ajpath.2009.090372
77. Cunningham C., Deacon R., Wells H., Boche D., Waters S., Picanco Diniz C., Scott H., Rawlins J. N. P., Perry V. H., Synaptic changes characterize early behavioural signs in the ME7 model of murine prion disease. European Journal of Neuroscience 2003 17 10 2147 2155 2-s2.0-0038809966 10.1046/j.1460-9568.2003. 02662.x (Pubitemid 36713975)
78. Chiti Z., Knutsen O. M., Betmouni S., Greene J. R. T., An integrated, temporal study of the behavioural, electrophysiological and neuropathological consequences of murine prion disease. Neurobiology of Disease 2006 22 2 363 373 2-s2.0-33646136461 10.1016/j.nbd.2005.12.002
79. Mallucci G. R., White M. D., Farmer M., Dickinson A., Khatun H., Powell A. D., Brandner S., Jefferys J. G. R., Collinge J., Targeting cellular prion protein reverses early cognitive deficits and neurophysiological dysfunction in prion-infected mice. Neuron 2007 53 3 325 335 2-s2.0-33846538022 10.1016/j.neuron.2007.01.005 (Pubitemid 46161264)
80. Moreno J. A., Radford H., Peretti D., Steinert J. R., Verity N., Martin M. G., Halliday M., Morgan J., Dinsdale D., Ortori C. A., Barrett D. A., Tsaytler P., Bertolotti A., Willis A. E., Bushell M., Mallucci G. R., Sustained translational repression by eIF2alpha-P mediates prion neurodegeneration. Nature 2012 485 7399 507 511
81. Clinton J., Forsyth C., Royston M. C., Roberts G. W., Synaptic degeneration is the primary neuropathological feature in prion disease: a preliminary study. NeuroReport 1993 4 1 65 68 2-s2.0-0027394220 (Pubitemid 23066392)
82. Senatore A., Colleoni S., Verderio C., Restelli E., Morini R., Condliffe S. B., Bertani I., Mantovani S., Canovi M., Micotti E., Forloni G., Dolphin A. C., Matteoli M., Gobbi M., Chiesa R., Mutant PrP suppresses glutamatergic neurotransmission in cerebellar granule neurons by impairing membrane delivery of VGCC α 2 δ -1 subunit. Neuron 2012 74 2 300 313 2-s2.0-84860288578 10.1016/j.neuron.2012.02.027
83. Kitamoto T., Shin R.-W., Doh-ura K., Tomokane N., Miyazono M., Muramoto T., Tateishi J., Abnormal isoform of prion proteins accumulates in the synaptic structures of the central nervous system in patients with Creutzfeldt-Jakob disease. American Journal of Pathology 1992 140 6 1285 1294 2-s2.0-0026751775
84. Jeffrey M., Goodsir C., McGovern G., Barmada S. J., Medrano A. Z., Harris D. A., Prion protein with an insertional mutation accumulates on axonal and dendritic plasmalemma and is associated with distinctive ultrastructural changes. American Journal of Pathology 2009 175 3 1208 1217 2-s2.0-70349236999 10.2353/ajpath.2009.090125
85. Novitskaya V., Bocharova O. V., Bronstein I., Baskakov I. V., Amyloid fibrils of mammalian prion protein are highly toxic to cultured cells and primary neurons. Journal of Biological Chemistry 2006 281 19 13828 13836 2-s2.0-33744961169 10.1074/jbc.M511174200 (Pubitemid 43855298)
86. Simoneau S., Rezaei H., Salès N., Kaiser-Schulz G., Lefebvre-Roque M., Vidal C., Fournier J., Comte J., Wopfner F., Grosclaude J., Schätzl H., Lasmézas C. I., In vitro and in vivo neurotoxicity of prion protein oligomers. PLoS pathogens 2007 3 8 e125 2-s2.0-34548782787 10.1371/journal.ppat. 0030125 (Pubitemid 47359094)
87. Zhou M., Ottenberg G., Sferrazza G. F., Lasmeźas C. I., Highly neurotoxic monomeric α -helical prion protein. Proceedings of the National Academy of Sciences of the United States of America 2012 109 8 3113 3118 2-s2.0-84857408200 10.1073/pnas.1118090109/-/DCSupplemental
88. Lai E., Teodoro T., Volchuk A., Endoplasmic reticulum stress: signaling the unfolded protein response. Physiology 2007 22 3 193 201 2-s2.0-34447527676 10.1152/physiol.00050.2006
89. Hetz C., Glimcher L. H., Fine-tuning of the unfolded protein response: assembling the IRE1 α interactome. Molecular Cell 2009 35 5 551 561 2-s2.0-69749123786 10.1016/j.molcel.2009.08.021
90. Han J., Back S. H., Hur J., Lin Y. H., Gildersleeve R., Shan J., Yuan C. L., Krokowski D., Wang S., Hatzoglou M., Kilberg M. S., Sartor M. A., Kaufman R. J., ER-stress-induced transcriptional regulation increases protein synthesis leading to cell death. Nature Cell Biology 2013 15 481 490 10.1038/ncb2738
91. Mukherjee A., Morales-Scheihing D., Gonzalez-Romero D., Green K., Taglialatela G., Soto C., Calcineurin inhibition at the clinical phase of prion disease reduces neurodegeneration, improves behavioral alterations and increases animal survival. PLoS Pathogens 2010 6 10 2-s2.0-78449257695 10.1371/journal.ppat.1001138 e1001138
92. Chiesa R., Piccardo P., Ghetti B., Harris D. A., Neurological illness in transgenic mice expressing a prion protein with an insertional mutation. Neuron 1998 21 6 1339 1351 2-s2.0-0032427904 10.1016/S0896-6273(00)80653-4 (Pubitemid 29022536)
93. Dossena S., Imeri L., Mangieri M., Garofoli A., Ferrari L., Senatore A., Restelli E., Balducci C., Fiordaliso F., Salio M., Bianchi S., Fioriti L., Morbin M., Pincherle A., Marcon G., Villani F., Carli M., Tagliavini F., Forloni G., Chiesa R., Mutant prion protein expression causes motor and memory deficits and abnormal sleep patterns in a transgenic mouse model. Neuron 2008 60 4 598 609 2-s2.0-56349096340 10.1016/j.neuron.2008.09.008
94. Daude N., Lehmann S., Harris D. A., Identification of intermediate steps in the conversion of a mutant prion protein to a Scrapie-like form in cultured cells. Journal of Biological Chemistry 1997 272 17 11604 11612 2-s2.0-0030896803 10.1074/jbc.272.17.11604 (Pubitemid 27184173)
95. Drisaldi B., Stewart R. S., Adles C., Stewart L. R., Quaglio E., Biasini E., Fioriti L., Chiesa R., Harris D. A., Mutant PrP is delayed in its exit from the endoplasmic reticulum, but neither wild-type nor mutant PrP undergoes retrotranslocation prior to proteasomal degradation. Journal of Biological Chemistry 2003 278 24 21732 21743 2-s2.0-0038159514 10.1074/jbc.M213247200 (Pubitemid 36792576)
96. Fioriti L., Dossena S., Stewart L. R., Stewart R. S., Harris D. A., Forloni G., Chiesa R., Cytosolic prion protein (PrP) is not toxic in N2a cells and primary neurons expressing pathogenic PrP mutations. Journal of Biological Chemistry 2005 280 12 11320 11328 2-s2.0-15744395826 10.1074/jbc.M412441200 (Pubitemid 40418439)
97. Quaglio E., Restelli E., Garofoli A., Dossena S., de Luigi A., Tagliavacca L., Imperiale D., Migheli A., Salmona M., Sitia R., Forloni G., Chiesa R., Expression of mutant or cytosolic PrP in transgenic mice and cells is not associated with endoplasmic reticulum stress or proteasome dysfunction. PLoS One 2011 6 4 2-s2.0-79955781215 10.1371/journal.pone.0019339 e19339
98. Biasini E., Massignan T., Fioriti L., Rossi V., Dossena S., Salmona M., Forloni G., Bonetto V., Chiesa R., Analysis of the cerebellar proteome in a transgenic mouse model of inherited prion disease reveals preclinical alteration of calcineurin activity. Proteomics 2006 6 9 2823 2834 2-s2.0-33646728858 10.1002/pmic.200500620
99. Biasini E., Tapella L., Restelli E., Pozzoli M., Massignan T., Chiesa R., The hydrophobic core region governs mutant prion protein aggregation and intracellular retention. Biochemical Journal 2010 430 3 477 486 2-s2.0-77956705694 10.1042/BJ20100615
100. Dolphin A. C., The alpha2delta subunits of voltage-gated calcium channels. Biochim Biophys Acta 2013 1828 7 1541 1549 10.1016/j.bbamem.2012.11. 019
101. Canti C., Nieto-Rostro M., Foucault I., Heblich F., Wratten J., Richards M. W., Hendrich J., Douglas L., Page K. M., Davies A., Dolphin A. C., The metal-ion-dependent adhesion site in the Von Willebrand factor-A domain of α 2 δ subunits is key to trafficking voltage-gated Ca2+ channels. Proceedings of the National Academy of Sciences of the United States of America 2005 102 32 11230 11235 2-s2.0-23844500323 10.1073/pnas.0504183102 (Pubitemid 41153803)
102. Hoppa M. B., Lana B., Margas W., Dolphin A. C., Ryan T. A., alpha2delta expression sets presynaptic calcium channel abundance and release probability. Nature 2012 486 7401 122 125
103. Rutishauser D., Mertz K. D., Moos R., Brunner E., Rülicke T., Calella A. M., Aguzzi A., The comprehensive native interactome of a fully functional tagged prion protein. PLoS One 2009 4 2 2-s2.0-61349108262 10.1371/journal.pone.0004446 e4446
104. Traynelis S. F., Wollmuth L. P., McBain C. J., Menniti F. S., Vance K. M., Ogden K. K., Hansen K. B., Yuan H., Myers S. J., Dingledine R., Glutamate receptor ion channels: structure, regulation, and function. Pharmacological Reviews 2010 62 3 405 496 2-s2.0-77952363301 10.1124/pr.109.002451
105. Kleene R., Loers G., Langer J., Frobert Y., Buck F., Schachner M., Prion protein regulates glutamate-dependent lactate transport of astrocytes. Journal of Neuroscience 2007 27 45 12331 12340 2-s2.0-36049043710 10.1523/JNEUROSCI. 1358-07.2007 (Pubitemid 350085463)
106. Khosravani H., Zhang Y., Tsutsui S., Hameed S., Altier C., Hamid J., Chen L., Villemaire M., Ali Z., Jirik F. R., Zamponi G. W., Prion protein attenuates excitotoxicity by inhibiting NMDA receptors. Journal of Cell Biology 2008 181 3 551 555 2-s2.0-43149109488 10.1083/jcb.200711002 (Pubitemid 351645043)
107. Watt N. T., Taylor D. R., Kerrigan T. L., Griffiths H. H., Rushworth J. V., Whitehouse I. J., Hooper N. M., Prion protein facilitates uptake of zinc into neuronal cells. Nature Communications 2012 3 1134 10.1038/ncomms2135
108. You H., Tsutsui S., Hameed S., Kannanayakal T. J., Chen L., Xia P., Engbers J. D. T., Lipton S. A., Stys P. K., Zamponi G. W., A β neurotoxicity depends on interactions between copper ions, prion protein, and N-methyl-D-aspartate receptors. Proceedings of the National Academy of Sciences of the United States of America 2012 109 5 1737 1742 2-s2.0-84857127188 10.1073/pnas.1110789109
109. Hetz C., Castilla J., Soto C., Perturbation of endoplasmic reticulum homeostasis facilitates prion replication. Journal of Biological Chemistry 2007 282 17 12725 12733 2-s2.0-34250351315 10.1074/jbc.M611909200 (Pubitemid 47100587)
110. Béranger F., Mangé A., Goud B., Lehmann S., Stimulation of PrP C retrograde transport toward the endoplasmic reticulum increases accumulation of PrP Sc in prion-infected cells. Journal of Biological Chemistry 2002 277 41 38972 38977 2-s2.0-0037064026 10.1074/jbc.M205110200 (Pubitemid 35154763)
111. Torres M., Castillo K., Armisén R., Stutzin A., Soto C., Hetz C., Prion protein misfolding affects calcium homeostasis and sensitizes cells to endoplasmic reticulum stress. PLoS One 2010 5 12 2-s2.0-78650843400 10.1371/journal.pone.0015658 e15658
112. Sandberg M. K., Wallén P., Wikström M. A., Kristensson K., Scrapie-infected GT1-1 cells show impaired function of voltage-gated N-type calcium channels (CaV 2.2) which is ameliorated by quinacrine treatment. Neurobiology of Disease 2004 15 1 143 151 (Pubitemid 38134389)
113. Massignan T., Biasini E., Lauranzano E., Veglianese P., Pignataro M., Fioriti L., Harris D. A., Salmona M., Chiesa R., Bonetto V., Mutant prion protein expression is associated with an alteration of the rab GDP dissociation inhibitor α (GDI)/rab11 pathway. Molecular and Cellular Proteomics 2010 9 4 611 622 2-s2.0-77950660924 10.1074/mcp.M900271-MCP200
114. Uchiyama K., Muramatsu N., Yano M., Usui T., Miyata H., Sakaguchi S., Prions disturb post-Golgi trafficking of membrane proteins. Nature Communications 2013 4 1846 10.1038/ncomms2873
115. Unterberger U., Höftberger R., Gelpi E., Flicker H., Budka H., Voigtländer T., Endoplasmic reticulum stress features are prominent in Alzheimer disease but not in prion diseases in vivo. Journal of Neuropathology and Experimental Neurology 2006 65 4 348 357 2-s2.0-33744985455 10.1097/01.jnen.0000218445.30535.6f (Pubitemid 44264832)
116. Barclay J., Balaguero N., Mione M., Ackerman S. L., Letts V. A., Brodbeck J., Canti C., Meir A., Page K. M., Kusumi K., Perez-Reyes E., Lander E. S., Frankel W. N., Gardiner R. M., Dolphin A. C., Rees M., Ducky mouse phenotype of epilepsy and ataxia is associated with mutations in the Cacna2d2 gene and decreased calcium channel current in cerebellar Purkinje cells. Journal of Neuroscience 2001 21 16 6095 6104 2-s2.0-0035882271 (Pubitemid 32737743)
117. Ivanov S. V., Ward J. M., Tessarollo L., McAreavey D., Sachdev V., Fananapazir L., Banks M. K., Morris N., Djurickovic D., Devor-Henneman D. E., Wei M., Alvord G. W., Gao B., Richardson J. A., Minna J. D., Rogawski M. A., Lerman M. I., Cerebellar ataxia, seizures, premature death, and cardiac abnormalities in mice with targeted disruption of the Cacna2d2 gene. American Journal of Pathology 2004 165 3 1007 1018 2-s2.0-4344619176 (Pubitemid 39129306)
118. Hardingham G. E., Bading H., Synaptic versus extrasynaptic NMDA receptor signalling: implications for neurodegenerative disorders. Nature Reviews Neuroscience 2010 11 10 682 696 2-s2.0-77956917231 10.1038/nrn2911
119. Beattie M. S., Ferguson A. R., Bresnahan J. C., AMPA-receptor trafficking and injury-induced cell death. The European Journal of Neuroscience 2010 32 2 290 297 2-s2.0-78951473274
120. Biasini E., Unterberger U., Solomon I. H., Massignan T., Senatore A., Bian H., Voigtlaender T., Bowman F. P., Bonetto V., Chiesa R., Luebke J., Toselli P., Harris D. A., A mutant prion protein sensitizes neurons to glutamate-induced excitotoxicity. Journal of Neuroscience 2013 33 6 2408 2418 10.1523/JNEUROSCI.3406-12.2013
121. Linden R., Martins V. R., Prado M. A. M., Cammarota M., Izquierdo I., Brentani R. R., Physiology of the prion protein. Physiological Reviews 2008 88 2 673 728 2-s2.0-42049099020 10.1152/physrev.00007.2007 (Pubitemid 351520090)
122. Tapella L., Stravalaci M., Bastone A., Biasini E., Gobbi M., Chiesa R., Epitope scanning indicates structural differences in brain-derived monomeric and aggregated mutant prion proteins related to genetic prion diseases. Biochemical Journal 2013 454 417 425 10.1042/BJ20130563
123. Chiesa R., Piccardo P., Quaglio E., Drisaldi B., Si-Hoe S. L., Takao M., Ghetti B., Harris D. A., Molecular distinction between pathogenic and infectious properties of the prion protein. Journal of Virology 2003 77 13 7611 7622 2-s2.0-0038128629 10.1128/JVI.77.13.7611-7622.2003 (Pubitemid 36734531)
124. Sandberg M. K., Al-Doujaily H., Sharps B., Clarke A. R., Collinge J., Prion propagation and toxicity in vivo occur in two distinct mechanistic phases. Nature 2011 470 7335 540 542 2-s2.0-79952167224 10.1038/nature09768
125. Brandner S., Isenmann S., Raeber A., Fischer M., Sailer A., Kobayashi Y., Marino S., Weissmann C., Aguzzi A., Normal host prion protein necessary for scrapie-induced neurotoxicity. Nature 1996 379 6563 339 343 2-s2.0-0030054010 10.1038/379339a0 (Pubitemid 26033075)
126. Mallucci G., Dickinson A., Linehan J., Klöhn P., Brandner S., Collinge J., Depleting neuronal PrP in prion infection prevents disease and reverses spongiosis. Science 2003 302 5646 871 874 2-s2.0-0242363656 10.1126/science.1090187 (Pubitemid 37339628)
127. Chesebro B., Trifilo M., Race R., Meade-White K., Teng C., LaCasse R., Raymond L., Favara C., Baron G., Priola S., Caughey B., Masliah E., Oldstone M., Anchorless prion protein results in infectious amyloid disease without clinical scrapie. Science 2005 308 5727 1435 1439 2-s2.0-20344394154 10.1126/science.1110837 (Pubitemid 40791292)