Prion Proteins pp 225-256 | Cite as

The PrP-Like Proteins Shadoo and Doppel

  • David WestawayEmail author
  • Nathalie Daude
  • Serene Wohlgemuth
  • Paul Harrison
Part of the Topics in Current Chemistry book series (TOPCURRCHEM, volume 305)


An almost unique place within protein databases, twenty-five years of study has underscored the enigmatically subtle role of PrPC in normal cell biology. It seems that PrP has evolved (and survived) to perform a function that does not have a precedent amongst transmembrane cell-surface proteins, perhaps representing a new type of plasma membrane ecosystem. In a context where we await a clarifying insight to unify a panoply of PrPC data into logical molecular framework, the GPI-anchored N-glycosylated Doppel and Sho proteins are tantalizing in that they correspond roughly to the front and back halves of PrPC itself. These molecules may be simpler – and more “understandable” – entities that can be pursued in parallel to PrPC, and could open up the biology of mammalian prion proteins from fresh directions. Dpl has a profound role in successful gametogenesis that warrants close scrutiny and a case for deeper study can be made for Sho, a recently discovered CNS-expressed protein with many parallels to established facets of PrP biochemistry. In an aerial view of biomedical research, Sho and Dpl can be considered as adjacent islands in a prion protein archipelago. As such, the coming years of molecular exploration should be extremely interesting.

Graphical Abstract


Creutzfeldt–Jakob Disease Doppel Neuroprotection Prion Shadoo 



This work was supported by the Canadian Institutes of Health Research (grants MOP36377), the Alberta Prion Research Institute, the PrionNet Network centre of Excellence and the Alberta Innovates – Health Solutions. DW is supported by the Alberta Prion Research Institute Scholar Program and a Canada Research Chair in Prion Biology. “Three Views of a Secret” and “The Lost World” with acknowledgement and apologies to Jaco Pastorius and Arthur Conan Doyle.


  1. 1.
    Bueler H, Aguzzi A, Sailer A, Greiner RA, Autenried P, Aguet M, Weissmann C (1993) Cell 73:1339CrossRefGoogle Scholar
  2. 2.
    Benestad SL, Arsac JN, Goldmann W, Noremark M (2008) Vet Res 39:19CrossRefGoogle Scholar
  3. 3.
    Sakthivelu V, Seidel RP, Winklhofer KF, Tatzelt J (2011) J Biol Chem 286:8901CrossRefGoogle Scholar
  4. 4.
    Watts JC, Drisaldi B, Ng V, Yang J, Strome B, Horne P, Sy MS, Yoong L, Young R, Mastrangelo P, Bergeron C, Fraser PE, Carlson GA, Mount HT, Schmitt-Ulms G, Westaway D (2007) EMBO J 26:4038CrossRefGoogle Scholar
  5. 5.
    Premzl M, Sangiorgio L, Strumbo B, Marshall Graves JA, Simonic T, Gready JE (2003) Gene 314:89CrossRefGoogle Scholar
  6. 6.
    Harrison PM, Khachane A, Kumar M (2010) Genomics 95:268CrossRefGoogle Scholar
  7. 7.
    Lampo E, Van Poucke M, Hugot K, Hayes H, Van Zeveren A, Peelman LJ (2007) BMC Genomics 8:138CrossRefGoogle Scholar
  8. 8.
    Uboldi C, Paulis M, Guidi E, Bertoni A, Meo GP, Perucatti A, Iannuzzi L, Raimondi E, Brunner RM, Eggen A, Ferretti L (2006) Mamm Genome 17:1130CrossRefGoogle Scholar
  9. 9.
    Le Pichon CE, Valley MT, Polymenidou M, Chesler AT, Sagdullaev BT, Aguzzi A, Firestein S (2009) Nat Neurosci 12:60CrossRefGoogle Scholar
  10. 10.
    Premzl M, Gready JE, Jermiin LS, Simonic T, Marshall Graves JA (2004) Mol Biol Evol 21:2210CrossRefGoogle Scholar
  11. 11.
    Taylor JS, Braasch I, Frickey T, Meyer A, Van de Peer Y (2003) Genome Res 13:382CrossRefGoogle Scholar
  12. 12.
    Strumbo B, Sangiorgio L, Ronchi S, Gready JE, Simonic T (2006) Fish Physiol Biochem 32:339CrossRefGoogle Scholar
  13. 13.
    Hornemann S, Christen B, von Schroetter C, Perez DR, Wuthrich K (2009) FEBS J 276:2359CrossRefGoogle Scholar
  14. 14.
    Schmitt-Ulms G, Ehsani S, Watts JC, Westaway D, Wille H (2009) PLoS One 4:e7208CrossRefGoogle Scholar
  15. 15.
    Ehsani S, Huo H, Salehzadeh A, Pocanschi CL, Watts JC, Wille H, Westaway D, Rogaeva E, St George-Hyslop PH, Schmitt-Ulms G (2010) Prog Neurobiol 93:405CrossRefGoogle Scholar
  16. 16.
    Volff JN, Brosius J (2007) Genome Dyn 3:175CrossRefGoogle Scholar
  17. 17.
    Carlson GA, Kingsbury DT, Goodman PA, Coleman S, Marshall ST, DeArmond S, Westaway D, Prusiner SB (1986) Cell 46:503CrossRefGoogle Scholar
  18. 18.
    Makrinou E, Collinge J, Antoniou M (2002) Mamm Genome 13:696CrossRefGoogle Scholar
  19. 19.
    Moore RC, Lee IY, Silverman GL, Harrison PM, Strome R, Heinrich C, Karunaratne A, Pasternak SH, Chishti MA, Liang Y, Mastrangelo P, Wang K, Smit AF, Katamine S, Carlson GA, Cohen FE, Prusiner SB, Melton DW, Tremblay P, Hood LE, Westaway D (1999) J Mol Biol 292:797CrossRefGoogle Scholar
  20. 20.
    Westaway D, Goodman PA, Mirenda CA, McKinley MP, Carlson GA, Prusiner SB (1987) Cell 51:651CrossRefGoogle Scholar
  21. 21.
    Carlson GA, Goodman PA, Lovett M, Taylor BA, Marshall ST, Peterson-Torchia M, Westaway D, Prusiner SB (1988) Mol Cell Biol 8:5528Google Scholar
  22. 22.
    Lloyd SE, Thompson SR, Beck JA, Linehan JM, Wadsworth JD, Brandner S, Collinge J, Fisher EM (2004) Mamm Genome 15:383CrossRefGoogle Scholar
  23. 23.
    Stephenson DA, Chiotti K, Ebeling C, Groth D, DeArmond SJ, Prusiner SB, Carlson GA (2000) Genomics 69:47CrossRefGoogle Scholar
  24. 24.
    Lloyd SE, Onwuazor ON, Beck JA, Mallinson G, Farrall M, Targonski P, Collinge J, Fisher EM (2001) Proc Natl Acad Sci USA 98:6279CrossRefGoogle Scholar
  25. 25.
    Lloyd SE, Uphill JB, Targonski PV, Fisher EM, Collinge J (2002) Neurogenetics 4:77CrossRefGoogle Scholar
  26. 26.
    Manolakou K, Beaton J, McConnell I, Farquar C, Manson J, Hastie ND, Bruce M, Jackson IJ (2001) Proc Natl Acad Sci USA 98:7402CrossRefGoogle Scholar
  27. 27.
    Moreno CR, Lantier F, Lantier I, Sarradin P, Elsen JM (2003) Genetics 165:2085Google Scholar
  28. 28.
    Hernandez-Sanchez J, Waddington D, Wiener P, Haley CS, Williams JL (2002) Mamm Genome 13:164CrossRefGoogle Scholar
  29. 29.
    Zhang C, De Koning DJ, Hernandez-Sanchez J, Haley CS, Williams JL, Wiener P (2004) Genetics 167:1863CrossRefGoogle Scholar
  30. 30.
    Laurent P, Schibler L, Vaiman A, Laubier J, Delcros C, Cosseddu G, Vaiman D, Cribiu EP, Yerle M (2007) Anim Genet 38:358CrossRefGoogle Scholar
  31. 31.
    Moreno CR, Moazami-Goudarzi K, Briand S, Robert C, Weisbecker JL, Laurent P, Cribiu EP, Haley CS, Andreoletti O, Bishop S, Pong-Wong R (2010) J Gen Virol 91:575CrossRefGoogle Scholar
  32. 32.
    Lloyd SE, Maytham EG, Grizenkova J, Hummerich H, Collinge J (2009) Neurogenetics 11:185Google Scholar
  33. 33.
    Lloyd SE, Maytham EG, Pota H, Grizenkova J, Molou E, Uphill J, Hummerich H, Whitfield J, Alpers MP, Mead S, Collinge J (2009) PLoS Genet 5:e1000383CrossRefGoogle Scholar
  34. 34.
    Lloyd SE, Grizenkova J, Pota H, Collinge J (2009) Mamm Genome 20:367CrossRefGoogle Scholar
  35. 35.
    Daude N, Wohlgemuth S, Rogaeva E, Farid AH, Heaton M, Westaway D (2009) PLoS One 4:e6538CrossRefGoogle Scholar
  36. 36.
    Stewart P, Shen C, Zhao D, Goldmann W (2009) J Gen Virol 90:2575CrossRefGoogle Scholar
  37. 37.
    Lampo E, Duchateau L, Schepens B, Van Poucke M, Saelens X, Erkens T, Van Zeveren A, Peelman LJ (2010) Anim Genet 41:169CrossRefGoogle Scholar
  38. 38.
    Baylis M, Goldmann W (2004) Curr Mol Med 4:385CrossRefGoogle Scholar
  39. 39.
    Beck JA, Campbell TA, Adamson G, Poulter M, Uphill JB, Molou E, Collinge J, Mead S (2008) J Med Genet 45:813CrossRefGoogle Scholar
  40. 40.
    Beck JA, Poulter M, Campbell TA, Adamson G, Uphill JB, Guerreiro R, Jackson GS, Stevens JC, Manji H, Collinge J, Mead S (2010) Hum Mutat 31:E1551CrossRefGoogle Scholar
  41. 41.
    Harris DA, Lele P, Snider WD (1993) Proc Natl Acad Sci USA 90:4309CrossRefGoogle Scholar
  42. 42.
    Miyazawa K, Manuelidis L (2010) J Neuroimmune Pharmacol 5:155CrossRefGoogle Scholar
  43. 43.
    Okiyoneda T, Barriere H, Bagdany M, Rabeh WM, Du K, Hohfeld J, Young JC, Lukacs GL (2010) Science 329:805CrossRefGoogle Scholar
  44. 44.
    Daude N, Westaway D (2011) Front Biosci 16:1505CrossRefGoogle Scholar
  45. 45.
    Zamponi GW, Stys PK (2009) Prion 3:187CrossRefGoogle Scholar
  46. 46.
    Shmerling D, Hegyi I, Fischer M, Blattler T, Brandner S, Gotz J, Rulicke T, Flechsig E, Cozzio A, von Mering C, Hangartner C, Aguzzi A, Weissmann C (1998) Cell 93:203CrossRefGoogle Scholar
  47. 47.
    Young R, Passet B, Vilotte M, Cribiu EP, Beringue V, Le Provost F, Laude H, Vilotte JL (2009) FEBS Lett 583:3296CrossRefGoogle Scholar
  48. 48.
    Essalmani R, Taourit S, Besnard N, Vilotte JL (2002) Gene 285:287CrossRefGoogle Scholar
  49. 49.
    Harrison CF, Lawson VA, Coleman BM, Kim YS, Masters CL, Cappai R, Barnham KJ, Hill AF (2010) J Biol Chem 285:20213CrossRefGoogle Scholar
  50. 50.
    Mesquita P, Batista M, Marques MR, Santos IC, Pimenta J, Silva Pereira M, Carolino I, Santos Silva F, Oliveira Sousa MC, Gama LT, Fontes CM, Horta AE, Prates JA, Pereira RM (2009) Anim Genet 41:311CrossRefGoogle Scholar
  51. 51.
    Pereira RM, Mesquita P, Batista M, Baptista MC, Barbas JP, Pimenta J, Santos IC, Marques MR, Vasques MI, Silva Pereira M, Santos Silva F, Oliveira Sousa MC, Fontes CM, Horta AE, Prates JA, Marques CC (2008) Anim Reprod Sci 114:157CrossRefGoogle Scholar
  52. 52.
    Tranulis MA, Espenes A, Comincini S, Skretting G, Harbitz I (2001) Mamm Genome 12:376CrossRefGoogle Scholar
  53. 53.
    Balbus N, Humeny A, Kashkevich K, Henz I, Fischer C, Becker CM, Schiebel K (2005) Mamm Genome 16:884CrossRefGoogle Scholar
  54. 54.
    Mead S, Beck J, Dickinson A, Fisher EM, Collinge J (2000) Neurosci Lett 290:117CrossRefGoogle Scholar
  55. 55.
    Peoc’h K, Guerin C, Brandel JP, Launay JM, Laplanche JL (2000) Neurosci Lett 286:144CrossRefGoogle Scholar
  56. 56.
    Jeong BH, Kim NH, Kim JI, Carp RI, Kim YS (2005) J Hum Genet 50:311CrossRefGoogle Scholar
  57. 57.
    Vollmert C, Windl O, Xiang W, Rosenberger A, Zerr I, Wichmann HE, Bickeboller H, Illig T, Kretzschmar HA (2006) J Med Genet 43:e53CrossRefGoogle Scholar
  58. 58.
    Schroder B, Franz B, Hempfling P, Selbert M, Jurgens T, Kretzschmar HA, Bodemer M, Poser S, Zerr I (2001) Hum Genet 109:319CrossRefGoogle Scholar
  59. 59.
    Croes EA, Alizadeh BZ, Bertoli-Avella AM, Rademaker T, Vergeer-Drop J, Dermaut B, Houwing-Duistermaat JJ, Wientjens DP, Hofman A, Van Broeckhoven C, Van Duijn CM (2004) Eur J Hum Genet 12:389CrossRefGoogle Scholar
  60. 60.
    Jeong BH, Kim NH, Choi EK, Lee C, Song YH, Kim JI, Carp RI, Kim YS (2005) Eur J Hum Genet 13:1094CrossRefGoogle Scholar
  61. 61.
    Uboldi C, Del Vecchio I, Foti MG, Azzalin A, Paulis M, Raimondi E, Vaccari G, Agrimi U, Di Guardo G, Comincini S, Ferretti L (2005) Mamm Genome 16:963CrossRefGoogle Scholar
  62. 62.
    Suzuki T, Kurokawa T, Hashimoto H, Sugiyama M (2002) Biochem Biophys Res Commun 294:912CrossRefGoogle Scholar
  63. 63.
    Oidtmann B, Simon D, Holtkamp N, Hoffmann R, Baier M (2003) FEBS Lett 538:96CrossRefGoogle Scholar
  64. 64.
    Rivera-Milla E, Oidtmann B, Panagiotidis CH, Baier M, Sklaviadis T, Hoffmann R, Zhou Y, Solis GP, Stuermer CA, Malaga-Trillo E (2006) FASEB J 20:317Google Scholar
  65. 65.
    Paltrinieri S, Comazzi S, Spagnolo V, Rondena M, Ponti W, Ceciliani F (2004) J Histochem Cytochem 52:1639CrossRefGoogle Scholar
  66. 66.
    Cordier-Dirikoc S, Zsurger N, Cazareth J, Menard B, Chabry J (2008) Eur J Immunol 38:2131CrossRefGoogle Scholar
  67. 67.
    Li YR, Li Q, Yang JM, Zhou XM, Yin XM, Zhao DM (2008) Mol Cell Probes 22:255CrossRefGoogle Scholar
  68. 68.
    Li A, Sakaguchi S, Shigematsu K, Atarashi R, Roy BC, Nakaoke R, Arima K, Okimura N, Kopacek J, Katamine S (2000) Am J Pathol 157:1447CrossRefGoogle Scholar
  69. 69.
    Ferrer I, Freixas M, Blanco R, Carmona M, Puig B (2004) Neuropathol Appl Neurobiol 30:329CrossRefGoogle Scholar
  70. 70.
    Peoc’h K, Volland H, De Gassart A, Beaudry P, Sazdovitch V, Sorgato MC, Creminon C, Laplanche JL, Lehmann S (2003) FEBS Lett 536:61CrossRefGoogle Scholar
  71. 71.
    Tuzi NL, Gall E, Melton D, Manson JC (2002) J Gen Virol 83:705Google Scholar
  72. 72.
    Comincini S, Facoetti A, Del Vecchio I, Peoc’h K, Laplanche JL, Magrassi L, Ceroni M, Ferretti L, Nano R (2004) Anticancer Res 24:1507Google Scholar
  73. 73.
    Comincini S, Chiarelli LR, Zelini P, Del Vecchio I, Azzalin A, Arias A, Ferrara V, Rognoni P, Dipoto A, Nano R, Valentini G, Ferretti L (2006) Oncol Rep 16:1325Google Scholar
  74. 74.
    Silverman GL, Qin K, Moore RC, Yang Y, Mastrangelo P, Tremblay P, Prusiner SB, Cohen FE, Westaway D (2000) J Biol Chem 275:26834Google Scholar
  75. 75.
    Rognoni P, Chiarelli LR, Comincini S, Azzalin A, Miracco C, Valentini G (2010) J Biomed Biotechnol 2010:301067CrossRefGoogle Scholar
  76. 76.
    Travaglino E, Comincini S, Benatti C, Azzalin A, Nano R, Rosti V, Ferretti L, Invernizzi R (2005) Br J Haematol 128:877CrossRefGoogle Scholar
  77. 77.
    Sbalchiero E, Azzalin A, Palumbo S, Barbieri G, Arias A, Simonelli L, Ferretti L, Comincini S (2008) Cell Oncol 30:337Google Scholar
  78. 78.
    Comincini S, Ferrara V, Arias A, Malovini A, Azzalin A, Ferretti L, Benericetti E, Cardarelli M, Gerosa M, Passarin MG, Turazzi S, Bellazzi R (2007) Oncol Rep 17:989Google Scholar
  79. 79.
    Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT (2009) Clin Chem 55:611CrossRefGoogle Scholar
  80. 80.
    Mehrpour M, Codogno P (2010) Cancer Lett 290:1CrossRefGoogle Scholar
  81. 81.
    Aguzzi A, Baumann F, Bremer J (2008) Annu Rev Neurosci 31:439CrossRefGoogle Scholar
  82. 82.
    Lu K, Wang W, Xie Z, Wong BS, Li R, Petersen RB, Sy MS, Chen SG (2000) Biochemistry 39:13575CrossRefGoogle Scholar
  83. 83.
    Peoc’h K, Serres C, Frobert Y, Martin C, Lehmann S, Chasseigneaux S, Sazdovitch V, Grassi J, Jouannet P, Launay JM, Laplanche JL (2002) J Biol Chem 277:43071CrossRefGoogle Scholar
  84. 84.
    Massimino ML, Ballarin C, Bertoli A, Casonato S, Genovesi S, Negro A, Sorgato MC (2004) Int J Biochem Cell Biol 36:2016CrossRefGoogle Scholar
  85. 85.
    Luhrs T, Riek R, Guntert P, Wuthrich K (2003) J Mol Biol 326:1549CrossRefGoogle Scholar
  86. 86.
    Mo H, Moore RC, Cohen FE, Westaway D, Prusiner SB, Wright PE, Dyson HJ (2001) Proc Natl Acad Sci USA 98:2352CrossRefGoogle Scholar
  87. 87.
    Donne DG, Viles JH, Groth D, Mehlhorn I, James TL, Cohen FE, Prusiner SB, Wright PE, Dyson HJ (1997) Proc Natl Acad Sci USA 94:13452CrossRefGoogle Scholar
  88. 88.
    Riek R, Luhrs T (2003) Clin Lab Med 23:209CrossRefGoogle Scholar
  89. 89.
    Whyte SM, Sylvester ID, Martin SR, Gill AC, Wopfner F, Schatzl HM, Dodson GG, Bayley PM (2003) Biochem J 373:485CrossRefGoogle Scholar
  90. 90.
    Zahn R, Guntert P, von Schroetter C, Wuthrich K (2003) J Mol Biol 326:225CrossRefGoogle Scholar
  91. 91.
    Knowles TP, Zahn R (2006) Biophys J 91:1494CrossRefGoogle Scholar
  92. 92.
    Hundt C, Weiss S (2004) Biochim Biophys Acta 1689:1CrossRefGoogle Scholar
  93. 93.
    Qin K, Coomaraswamy J, Mastrangelo P, Yang Y, Lugowski S, Petromilli C, Prusiner SB, Fraser PE, Goldberg JM, Chakrabartty A, Westaway D (2003) J Biol Chem 278:8888CrossRefGoogle Scholar
  94. 94.
    Cereghetti GM, Negro A, Vinck E, Massimino ML, Sorgato MC, Van Doorslaer S (2004) J Biol Chem 279:36497CrossRefGoogle Scholar
  95. 95.
    Mendola DL, Magri A, Hansson O, Bonomo RP, Rizzarelli E (2009) J Inorg Biochem 103:758Google Scholar
  96. 96.
    La Mendola D, Magri A, Campagna T, Campitiello MA, Raiola L, Isernia C, Hansson O, Bonomo RP, Rizzarelli E (2010) Chemistry 16:6212Google Scholar
  97. 97.
    Walter ED, Chattopadhyay M, Millhauser GL (2006) Biochemistry 45:13083CrossRefGoogle Scholar
  98. 98.
    Stewart RS, Harris DA (2003) J Biol Chem 278:45960CrossRefGoogle Scholar
  99. 99.
    Papadopoulos E, Oglecka K, Maler L, Jarvet J, Wright PE, Dyson HJ, Graslund A (2006) Biochemistry 45:159CrossRefGoogle Scholar
  100. 100.
    Erlich P, Cesbron JY, Lemaire-Vieille C, Curt A, Andrieu JP, Schoehn G, Jamin M, Gagnon J (2007) Biochem Biophys Res Commun 365:478Google Scholar
  101. 101.
    Shaked Y, Hijazi N, Gabizon R (2002) FEBS Lett 530:85CrossRefGoogle Scholar
  102. 102.
    Uelhoff A, Tatzelt J, Aguzzi A, Winklhofer KF, Haass C (2005) J Biol Chem 280:5137CrossRefGoogle Scholar
  103. 103.
    Caputo A, Sarnataro D, Campana V, Costanzo M, Negro A, Sorgato CM, Zurzolo C (2009) Biochem J 425:341CrossRefGoogle Scholar
  104. 104.
    Legname G, Nelken P, Guan Z, Kanyo ZF, DeArmond SJ, Prusiner SB (2002) Proc Natl Acad Sci USA 99:16285CrossRefGoogle Scholar
  105. 105.
    Benvegnu S, Franciotta D, Sussman J, Bachi A, Zardini E, Torreri P, Govaerts C, Pizzo S, Legname G (2009) PLoS One 4:e5968CrossRefGoogle Scholar
  106. 106.
    Watts JC, Huo H, Bai Y, Ehsani S, Won AH, Shi T, Daude N, Lau A, Young R, Xu L, Carlson GA, Williams D, Westaway D, Schmitt-Ulms G (2009) PLoS Pathog 5:e1000608CrossRefGoogle Scholar
  107. 107.
    Yin SM, Sy MS, Yang HY, Tien P (2004) Arch Biochem Biophys 428:165CrossRefGoogle Scholar
  108. 108.
    Azzalin A, Del Vecchio I, Ferretti L, Comincini S (2006) Anticancer Res 26:4539Google Scholar
  109. 109.
    Azzalin A, Sbalchiero E, Barbieri G, Palumbo S, Muzzini C, Comincini S (2008) Cell Oncol 30:491Google Scholar
  110. 110.
    Sakudo A, Onodera T (2010) Biochem Biophys Res Commun 404:523CrossRefGoogle Scholar
  111. 111.
    Behrens A, Aguzzi A (2002) Trends Neurosci 25:150CrossRefGoogle Scholar
  112. 112.
    Genoud N, Behrens A, Arrighi I, Aguzzi A (2003) Cytogenet Genome Res 103:285CrossRefGoogle Scholar
  113. 113.
    Genoud N, Behrens A, Miele G, Robay D, Heppner FL, Freigang S, Aguzzi A (2004) Proc Natl Acad Sci USA 101:4198CrossRefGoogle Scholar
  114. 114.
    Paisley D, Banks S, Selfridge J, McLennan NF, Ritchie AM, McEwan C, Irvine DS, Saunders PT, Manson JC, Melton DW (2004) Am J Pathol 164:2279CrossRefGoogle Scholar
  115. 115.
    Gatti JL, Metayer S, Moudjou M, Andreoletti O, Lantier F, Dacheux JL, Sarradin P (2002) Biol Reprod 67:393CrossRefGoogle Scholar
  116. 116.
    Kocer A, Gallozzi M, Renault L, Tilly G, Pinheiro I, Le Provost F, Pailhoux E, Vilotte JL (2007) Dev Dyn 236:836CrossRefGoogle Scholar
  117. 117.
    Rondena M, Ceciliani F, Comazzi S, Pocacqua V, Bazzocchi C, Luvoni C, Chigioni S, Paltrinieri S (2005) Theriogenology 63:1195CrossRefGoogle Scholar
  118. 118.
    Espenes A, Harbitz I, Skogtvedt S, Fuglestveit R, Berg KA, Dick G, Krogenaes A, Tranulis MA (2006) Int J Androl 29:400CrossRefGoogle Scholar
  119. 119.
    Serres C, Peoc’h K, Courtot AM, Lesaffre C, Jouannet P, Laplanche JL (2006) Biol Reprod 74:816CrossRefGoogle Scholar
  120. 120.
    Behrens A, Genoud N, Naumann H, Rulicke T, Janett F, Heppner FL, Ledermann B, Aguzzi A (2002) EMBO J 21:3652CrossRefGoogle Scholar
  121. 121.
    Wong BS, Liu T, Paisley D, Li R, Pan T, Chen SG, Perry G, Petersen RB, Smith MA, Melton DW, Gambetti P, Brown DR, Sy MS (2001) Mol Cell Neurosci 17:768CrossRefGoogle Scholar
  122. 122.
    Moore RC, Mastrangelo P, Bouzamondo E, Heinrich C, Legname G, Prusiner SB, Hood L, Westaway D, DeArmond SJ, Tremblay P (2001) Proc Natl Acad Sci USA 98:15288CrossRefGoogle Scholar
  123. 123.
    Massignan T, Stewart RS, Biasini E, Solomon IH, Bonetto V, Chiesa R, Harris DA (2010) J Biol Chem 285:7752CrossRefGoogle Scholar
  124. 124.
    Solomon IH, Huettner JE, Harris DA (2010) J Biol Chem 285:26719CrossRefGoogle Scholar
  125. 125.
    Sakaguchi S, Katamine S, Nishida N, Moriuchi R, Shigematsu K, Sugimoto T, Nakatani A, Kataoka Y, Houtani T, Shirabe S, Okada H, Hasegawa S, Miyamoto T, Noda T (1996) Nature 380:528CrossRefGoogle Scholar
  126. 126.
    Anderson L, Rossi D, Linehan J, Brandner S, Weissmann C (2004) Proc Natl Acad Sci USA 101:3644CrossRefGoogle Scholar
  127. 127.
    Radovanovic I, Braun N, Giger OT, Mertz K, Miele G, Prinz M, Navarro B, Aguzzi A (2005) J Neurosci 25:4879CrossRefGoogle Scholar
  128. 128.
    Al Bersaoui R, Robert I, Lutz Y, Blanc F, Sommermeyer-Leroux G, Shibaguchi H, Aunis D, Fuchs JP (2005) FEBS Lett 579:2715CrossRefGoogle Scholar
  129. 129.
    Heitz S, Grant NJ, Leschiera R, Haeberle AM, Demais V, Bombarde G, Bailly Y (2008) Brain Pathol 20:119CrossRefGoogle Scholar
  130. 130.
    Dong J, Li A, Yamaguchi N, Sakaguchi S, Harris DA (2007) Am J Pathol 171:599CrossRefGoogle Scholar
  131. 131.
    Heitz S, Lutz Y, Rodeau JL, Zanjani H, Gautheron V, Bombarde G, Richard F, Fuchs JP, Vogel MW, Mariani J, Bailly Y (2007) Dev Neurobiol 67:670CrossRefGoogle Scholar
  132. 132.
    Rossi D, Cozzio A, Flechsig E, Klein MA, Rulicke T, Aguzzi A, Weissmann C (2001) EMBO J 20:694CrossRefGoogle Scholar
  133. 133.
    Yamaguchi N, Sakaguchi S, Shigematsu K, Okimura N, Katamine S (2004) Biochem Biophys Res Commun 319:1247CrossRefGoogle Scholar
  134. 134.
    Flechsig E, Hegyi I, Leimeroth R, Zuniga A, Rossi D, Cozzio A, Schwarz P, Rulicke T, Gotz J, Aguzzi A, Weissmann C (2003) EMBO J 22:3095CrossRefGoogle Scholar
  135. 135.
    Atarashi R, Nishida N, Shigematsu K, Goto S, Kondo T, Sakaguchi S, Katamine S (2003) J Biol Chem 278:28944CrossRefGoogle Scholar
  136. 136.
    Yoshikawa D, Yamaguchi N, Ishibashi D, Yamanaka H, Okimura N, Yamaguchi Y, Mori T, Miyata H, Shigematsu K, Katamine S, Sakaguchi S (2008) J Biol Chem 283:24202CrossRefGoogle Scholar
  137. 137.
    Kim CK, Sakudo A, Taniuchi Y, Shigematsu K, Kang CB, Saeki K, Matsumoto Y, Sakaguchi S, Itohara S, Onodera T (2007) Int J Mol Med 20:169Google Scholar
  138. 138.
    Lee HP, Choi JK, Shin HY, Jeon YC, Jeong BH, Lee HG, Kim JI, Choi EK, Carp RI, Kim YS (2010) Neuroscience 167:799CrossRefGoogle Scholar
  139. 139.
    Kim CK, Hirose Y, Sakudo A, Takeyama N, Kang CB, Taniuchi Y, Matsumoto Y, Itohara S, Sakaguchi S, Onodera T (2007) Biochem Biophys Res Commun 358:469CrossRefGoogle Scholar
  140. 140.
    Watts JC, Westaway D (2007) Biochim Biophys Acta 1772:654CrossRefGoogle Scholar
  141. 141.
    Sakaguchi S (2008) Prion 2:107CrossRefGoogle Scholar
  142. 142.
    Christensen HM, Harris DA (2008) Mol Neurodegener 3:11CrossRefGoogle Scholar
  143. 143.
    Kuwahara C, Takeuchi AM, Nishimura T, Haraguchi K, Kubosaki A, Matsumoto Y, Saeki K, Yokoyama T, Itohara S, Onodera T (1999) Nature 400:225CrossRefGoogle Scholar
  144. 144.
    Sakudo A, Lee DC, Nakamura I, Taniuchi Y, Saeki K, Matsumoto Y, Itohara S, Ikuta K, Onodera T (2005) Biochem Biophys Res Commun 333:448CrossRefGoogle Scholar
  145. 145.
    Lee DC, Sakudo A, Kim CK, Nishimura T, Saeki K, Matsumoto Y, Yokoyama T, Chen SG, Itohara S, Onodera T (2006) Microbiol Immunol 50:203Google Scholar
  146. 146.
    Nishimura T, Sakudo A, Hashiyama Y, Yachi A, Saeki K, Matsumoto Y, Ogawa M, Sakaguchi S, Itohara S, Onodera T (2007) Microbiol Immunol 51:457Google Scholar
  147. 147.
    Cui T, Holme A, Sassoon J, Brown DR (2003) Mol Cell Neurosci 23:144CrossRefGoogle Scholar
  148. 148.
    Drisaldi B, Coomaraswamy J, Mastrangelo P, Strome B, Yang J, Watts JC, Chishti MA, Marvi M, Windl O, Ahrens R, Major F, Sy MS, Kretzschmar H, Fraser PE, Mount HT, Westaway D (2004) J Biol Chem 279:55443CrossRefGoogle Scholar
  149. 149.
    Xu K, Wang X, Tian C, Shi S, Wang GR, Shi Q, Li P, Zhou RM, Jiang HY, Chu YL, Dong XP (2009) Mol Biol Rep 37:2549CrossRefGoogle Scholar
  150. 150.
    Qin K, Zhao L, Tang Y, Bhatta S, Simard JM, Zhao RY (2006) Neuroscience 141:1375CrossRefGoogle Scholar
  151. 151.
    Brini M, Miuzzo M, Pierobon N, Negro A, Sorgato MC (2005) Mol Biol Cell 16:2799CrossRefGoogle Scholar
  152. 152.
    Prusiner SB, McCarty M (2006) Annu Rev Genet 40:25CrossRefGoogle Scholar
  153. 153.
    Daude N, Ng V, Watts JC, Genovesi S, Glaves JP, Wohlgemuth S, Schmitt-Ulms G, Young H, McLaurin J, Fraser PE, Westaway D (2010) J Neurochem 113:92CrossRefGoogle Scholar
  154. 154.
    Ghetti B, Piccardo P, Spillantini MG, Ichimiya Y, Porro M, Perini F, Kitamoto T, Tateishi J, Seiler C, Frangione B, Bugiani O, Giaccone G, Prelli F, Goedert M, Dlouhy SR, Tagliavini F (1996) Proc Natl Acad Sci USA 93:744CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2011

Authors and Affiliations

  • David Westaway
    • 1
    Email author
  • Nathalie Daude
    • 1
  • Serene Wohlgemuth
    • 1
  • Paul Harrison
    • 2
  1. 1.Centre for Prions and Protein Folding DiseasesUniversity of AlbertaEdmontonCanada
  2. 2.Department of BiologyMcGill UniversityMontrealCanada

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