Skip to main content

Unraveling the Role of Peptidyl-Prolyl Isomerases in Neurodegeneration

Molecular Neurobiology volume 44, pages 13–27 (2011)Cite this article

Abstract

Immunophilins are a family of highly conserved proteins with a peptidyl-prolyl isomerase activity that binds immunosuppressive drugs such as FK506, cyclosporin A, and rapamycin. Immunophilins can be divided into two subfamilies, the cyclophilins, and the FK506 binding proteins (FKBPs). Next to the immunophilins, a third group of peptidyl-prolyl isomerases exist, the parvulins, which do not influence the immune system. The beneficial role of immunophilin ligands in neurodegenerative disease models has been known for more than a decade but remains largely unexplained in terms of molecular mechanisms. In this review, we summarize reported effects of parvulins, immunophilins, and their ligands in the context of neurodegeneration. We focus on the role of FKBP12 in Parkinson’s disease and propose it as a novel drug target for therapy of Parkinson’s disease.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Uversky VN (2003) J Biomol Struct Dyn 21:211–234

    PubMed  CAS  Google Scholar 

  2. Uversky VN, Oldfield CJ, Dunker AK (2008) Annu Rev Biophys 37:215–246

    PubMed  CAS  Article  Google Scholar 

  3. Kino T, Hatanaka H, Miyata S, Inamura N, Nishiyama M, Yajima T, Goto T, Okuhara M, Kohsaka M, Aoki H et al (1987) J Antibiot (Tokyo) 40:1256–1265

    CAS  Google Scholar 

  4. Kino T, Hatanaka H, Hashimoto M, Nishiyama M, Goto T, Okuhara M, Kohsaka M, Aoki H, Imanaka H (1987) J Antibiot (Tokyo) 40:1249–1255

    CAS  Google Scholar 

  5. Parsons WH, Sigal NH, Wyvratt MJ (1993) Ann N Y Acad Sci 685:22–36

    PubMed  CAS  Article  Google Scholar 

  6. Rulten SL, Kinloch RA, Tateossian H, Robinson C, Gettins L, Kay JE (2006) Mamm Genome 17:322–331

    PubMed  CAS  Article  Google Scholar 

  7. Harding MW, Galat A, Uehling DE, Schreiber SL (1989) Nature 341:758–760

    PubMed  CAS  Article  Google Scholar 

  8. Rosen MK, Standaert RF, Galat A, Nakatsuka M, Schreiber SL (1990) Science 248:863–866

    PubMed  CAS  Article  Google Scholar 

  9. Heitman J, Movva NR, Hiestand PC, Hall MN (1991) Proc Natl Acad Sci U S A 88:1948–1952

    PubMed  CAS  Article  Google Scholar 

  10. Blatch GL, Lassle M (1999) Bioessays 21:932–939

    PubMed  CAS  Article  Google Scholar 

  11. Valdivia C, Vaughan D, Potter BV, Coronado R (1992) Biophys J 61:1184–1193

    PubMed  CAS  Article  Google Scholar 

  12. Sutko JL, Airey JA (1996) Physiol Rev 76:1027–1071

    PubMed  CAS  Google Scholar 

  13. Collins JH (1991) Biochem Biophys Res Commun 178:1288–1290

    PubMed  CAS  Article  Google Scholar 

  14. Valdivia HH (1998) Trends Pharmacol Sci 19:479–482

    PubMed  CAS  Article  Google Scholar 

  15. Marx SO, Reiken S, Hisamatsu Y, Jayaraman T, Burkhoff D, Rosemblit N, Marks AR (2000) Cell 101:365–376

    PubMed  CAS  Article  Google Scholar 

  16. Van AK, Bultynck G, Rossi D, Sorrentino V, Boens N, Missiaen L, De SH, Parys JB, Callewaert G (2004) J Cell Sci 117:1129–1137

    Article  CAS  Google Scholar 

  17. Xiao RP, Valdivia HH, Bogdanov K, Valdivia C, Lakatta EG, Cheng H (1997) J Physiol 500(Pt 2):343–354

    PubMed  CAS  Google Scholar 

  18. Carmody M, Mackrill JJ, Sorrentino V, O'Neill C (2001) FEBS Lett 505:97–102

    PubMed  CAS  Article  Google Scholar 

  19. Wang YX, Zheng YM, Mei QB, Wang QS, Collier ML, Fleischer S, Xin HB, Kotlikoff MI (2004) Am J Physiol Cell Physiol 286:C538–C546

    PubMed  CAS  Article  Google Scholar 

  20. Zheng YM, Mei QB, Wang QS, Abdullaev I, Lai FA, Xin HB, Kotlikoff MI, Wang YX (2004) Cell Calcium 35:345–355

    PubMed  CAS  Article  Google Scholar 

  21. MacMillan D, Currie S, Bradley KN, Muir TC, McCarron JG (2005) J Cell Sci 118:5443–5451

    PubMed  CAS  Article  Google Scholar 

  22. MacMillan D, McCarron JG (2009) Br J Pharmacol 158:1112–1120

    PubMed  CAS  Article  Google Scholar 

  23. Bultynck G, De Smet P, Rossi D, Callewaert G, Missiaen L, Sorrentino V, De Smedt H, Parys JB (2001) Biochem J 354:413–422

    PubMed  CAS  Article  Google Scholar 

  24. Fruman DA, Klee CB, Bierer BE, Burakoff SJ (1992) Proc Natl Acad Sci U S A 89:3686–3690

    PubMed  CAS  Article  Google Scholar 

  25. Liu J, Albers MW, Wandless TJ, Luan S, Alberg DG, Belshaw PJ, Cohen P, MacKintosh C, Klee CB, Schreiber SL (1992) Biochemistry 31:3896–3901

    PubMed  CAS  Article  Google Scholar 

  26. Liu J, Farmer JD Jr, Lane WS, Friedman J, Weissman I, Schreiber SL (1991) Cell 66:807–815

    PubMed  CAS  Article  Google Scholar 

  27. Vezina C, Kudelski A, Sehgal SN (1975) J Antibiot (Tokyo) 28:721–726

    CAS  Google Scholar 

  28. Dumont FJ, Staruch MJ, Koprak SL, Siekierka JJ, Lin CS, Harrison R, Sewell T, Kindt VM, Beattie TR, Wyvratt M et al (1992) J Exp Med 176:751–760

    PubMed  CAS  Article  Google Scholar 

  29. Brown EJ, Beal PA, Keith CT, Chen J, Shin TB, Schreiber SL (1995) Nature 377:441–446

    PubMed  CAS  Article  Google Scholar 

  30. Sabatini DM, Erdjument-Bromage H, Lui M, Tempst P, Snyder SH (1994) Cell 78:35–43

    PubMed  CAS  Article  Google Scholar 

  31. Bai X, Ma D, Liu A, Shen X, Wang QJ, Liu Y, Jiang Y (2007) Science 318:977–980

    PubMed  CAS  Article  Google Scholar 

  32. Uhlenbrock K, Weiwad M, Wetzker R, Fischer G, Wittinghofer A, Rubio I (2009) FEBS Lett 583:965–970

    PubMed  CAS  Article  Google Scholar 

  33. Wang X, Fonseca BD, Tang H, Liu R, Elia A, Clemens MJ, Bommer UA, Proud CG (2008) J Biol Chem 283:30482–30492

    PubMed  CAS  Article  Google Scholar 

  34. Lorenzen S, Peters B, Goede A, Preissner R, Frommel C (2005) Proteins 58:589–595

    PubMed  CAS  Article  Google Scholar 

  35. Bachinger HP (1987) J Biol Chem 262:17144–17148

    PubMed  CAS  Google Scholar 

  36. Tropschug M, Wachter E, Mayer S, Schonbrunner ER, Schmid FX (1990) Nature 346:674–677

    PubMed  CAS  Article  Google Scholar 

  37. Lang K, Schmid FX, Fischer G (1987) Nature 329:268–270

    PubMed  CAS  Article  Google Scholar 

  38. Dowling RJ, Topisirovic I, Fonseca BD, Sonenberg N (2010) Biochim Biophys Acta 1804:433–439

    PubMed  CAS  Google Scholar 

  39. Pei H, Li L, Fridley BL, Jenkins GD, Kalari KR, Lingle W, Petersen G, Lou Z, Wang L (2009) Cancer Cell 16:259–266

    PubMed  CAS  Article  Google Scholar 

  40. Periyasamy S, Warrier M, Tillekeratne MP, Shou W, Sanchez ER (2007) Endocrinology 148:4716–4726

    PubMed  CAS  Article  Google Scholar 

  41. Chen Z, Li Z, Wei B, Yin W, Xu T, Kotlikoff MI, Ji G (2010) FASEB J 24:357–363

    PubMed  CAS  Article  Google Scholar 

  42. Gkika D, Topala CN, Hoenderop JG, Bindels RJ (2006) Am J Physiol Renal Physiol 290:F1253–F1259

    PubMed  CAS  Article  Google Scholar 

  43. Ni L, Yang CS, Gioeli D, Frierson H, Toft DO, Paschal BM (2010) Mol Cell Biol 30:1243–1253

    PubMed  CAS  Article  Google Scholar 

  44. Banerjee A, Periyasamy S, Wolf IM, Hinds TD Jr, Yong W, Shou W, Sanchez ER (2008) Biochemistry 47:10471–10480

    PubMed  CAS  Article  Google Scholar 

  45. Hirota Y, Tranguch S, Daikoku T, Hasegawa A, Osuga Y, Taketani Y, Dey SK (2008) Am J Pathol 173:1747–1757

    PubMed  CAS  Article  Google Scholar 

  46. Riggs DL, Cox MB, Tardif HL, Hessling M, Buchner J, Smith DF (2007) Mol Cell Biol 27:8658–8669

    PubMed  CAS  Article  Google Scholar 

  47. Tatro ET, Everall IP, Kaul M, Achim CL (2009) Brain Res 1286:1–12

    PubMed  CAS  Article  Google Scholar 

  48. Cook LG, Chiasson VL, Long C, Wu GY, Mitchell BM (2009) Kidney Int 75:719–726

    PubMed  CAS  Article  Google Scholar 

  49. Okamoto T, Omori H, Kaname Y, Abe T, Nishimura Y, Suzuki T, Miyamura T, Yoshimori T, Moriishi K, Matsuura Y (2008) J Virol 82:3480–3489

    PubMed  CAS  Article  Google Scholar 

  50. Handschumacher RE, Harding MW, Rice J, Drugge RJ, Speicher DW (1984) Science 226:544–547

    PubMed  CAS  Article  Google Scholar 

  51. Shaw LM (1989) Clin Chem 35:1299–1308

    PubMed  CAS  Google Scholar 

  52. Galat A, Bua J (2010) Cell Mol Life Sci 67:3467–3488

    PubMed  CAS  Article  Google Scholar 

  53. Galat A (2003) Curr Top Med Chem 3:1315–1347

    PubMed  CAS  Article  Google Scholar 

  54. Halestrap AP, Clarke SJ, Javadov SA (2004) Cardiovasc Res 61:372–385

    PubMed  CAS  Article  Google Scholar 

  55. Ferreira PA, Nakayama TA, Pak WL, Travis GH (1996) Nature 383:637–640

    PubMed  CAS  Article  Google Scholar 

  56. Stamnes MA, Shieh BH, Chuman L, Harris GL, Zuker CS (1991) Cell 65:219–227

    PubMed  CAS  Article  Google Scholar 

  57. Horowitz DS, Lee EJ, Mabon SA, Misteli T (2002) EMBO J 21:470–480

    PubMed  CAS  Article  Google Scholar 

  58. Jang LK, Lee ZH, Kim HH, Hill JM, Kim JD, Kwon BS (2001) Mol Cells 12:304–312

    PubMed  CAS  Google Scholar 

  59. Scholz C, Rahfeld J, Fischer G, Schmid FX (1997) J Mol Biol 273:752–762

    PubMed  CAS  Article  Google Scholar 

  60. Ranganathan R, Lu KP, Hunter T, Noel JP (1997) Cell 89:875–886

    PubMed  CAS  Article  Google Scholar 

  61. Yaffe MB, Schutkowski M, Shen M, Zhou XZ, Stukenberg PT, Rahfeld JU, Xu J, Kuang J, Kirschner MW, Fischer G, Cantley LC, Lu KP (1997) Science 278:1957–1960

    PubMed  CAS  Article  Google Scholar 

  62. Lu KP, Zhou XZ (2007) Nat Rev Mol Cell Biol 8:904–916

    PubMed  CAS  Article  Google Scholar 

  63. Lu KP, Finn G, Lee TH, Nicholson LK (2007) Nat Chem Biol 3:619–629

    PubMed  CAS  Article  Google Scholar 

  64. Lippens G, Landrieu I, Smet C (2007) FEBS J 274:5211–5222

    PubMed  CAS  Article  Google Scholar 

  65. Spillantini MG, Crowther RA, Jakes R, Hasegawa M, Goedert M (1998) Proc Natl Acad Sci U S A 95:6469–6473

    PubMed  CAS  Article  Google Scholar 

  66. Ohama E, Ikuta F (1976) Acta Neuropathol (Berl) 34:311–319

    CAS  Article  Google Scholar 

  67. Spillantini MG, Schmidt ML, Lee VM, Trojanowski JQ, Jakes R, Goedert M (1997) Nature 388:839–840

    PubMed  CAS  Article  Google Scholar 

  68. Gelb DJ, Oliver E, Gilman S (1999) Arch Neurol 56:33–39

    PubMed  CAS  Article  Google Scholar 

  69. Gasser T (2009) Expert Rev Mol Med 11:e22

    PubMed  Article  Google Scholar 

  70. Mizuno Y, Hattori N, Kubo S, Sato S, Nishioka K, Hatano T, Tomiyama H, Funayama M, Machida Y, Mochizuki H (2008) Philos Trans R Soc Lond B Biol Sci 363:2215–2227

    PubMed  CAS  Article  Google Scholar 

  71. Olanow CW, Tatton WG (1999) Annu Rev Neurosci 22:123–144

    PubMed  CAS  Article  Google Scholar 

  72. Mori F, Tanji K, Yoshimoto M, Takahashi H, Wakabayashi K (2002) Exp Neurol 176:98–104

    PubMed  CAS  Article  Google Scholar 

  73. Maroteaux L, Campanelli JT, Scheller RH (1988) J Neurosci 8:2804–2815

    PubMed  CAS  Google Scholar 

  74. George JM, Jin H, Woods WS, Clayton DF (1995) Neuron 15:361–372

    PubMed  CAS  Article  Google Scholar 

  75. George JM (2002) Genome Biol 3:3002.1–3002.6

    Google Scholar 

  76. Polymeropoulos MH, Lavedan C, Leroy E, Ide SE, Dehejia A, Dutra A, Pike B, Root H, Rubenstein J, Boyer R, Stenroos ES, Chandrasekharappa S, Athanassiadou A, Papapetropoulos T, Johnson WG, Lazzarini AM, Duvoisin RC, Di Iorio G, Golbe LI, Nussbaum RL (1997) Science 276:2045–2047

    PubMed  CAS  Article  Google Scholar 

  77. Jellinger KA (2003) Mov Disord 18(Suppl 6):S2–S12

    PubMed  Article  Google Scholar 

  78. Kruger R, Kuhn W, Muller T, Woitalla D, Graeber M, Kosel S, Przuntek H, Epplen JT, Schols L, Riess O (1998) Nat Genet 18:106–108

    PubMed  CAS  Article  Google Scholar 

  79. Zarranz JJ, Alegre J, Gomez-Esteban JC, Lezcano E, Ros R, Ampuero I, Vidal L, Hoenicka J, Rodriguez O, Atares B, Llorens V, Gomez TE, del Ser T, Munoz DG, de Yebenes JG (2004) Ann Neurol 55:164–173

    PubMed  CAS  Article  Google Scholar 

  80. Li J, Uversky VN, Fink AL (2001) Biochemistry 40:11604–11613

    PubMed  CAS  Article  Google Scholar 

  81. Fredenburg RA, Rospigliosi C, Meray RK, Kessler JC, Lashuel HA, Eliezer D, Lansbury PT Jr (2007) Biochemistry 46:7107–7118

    PubMed  CAS  Article  Google Scholar 

  82. Choi W, Zibaee S, Jakes R, Serpell LC, Davletov B, Crowther RA, Goedert M (2004) FEBS Lett 576:363–368

    PubMed  CAS  Article  Google Scholar 

  83. Conway KA, Harper JD, Lansbury PT (1998) Nat Med 4:1318–1320

    PubMed  CAS  Article  Google Scholar 

  84. Conway KA, Lee SJ, Rochet JC, Ding TT, Williamson RE, Lansbury PT Jr (2000) Proc Natl Acad Sci U S A 97:571–576

    PubMed  CAS  Article  Google Scholar 

  85. Li J, Uversky VN, Fink AL (2002) Neurotoxicology 23:553–567

    PubMed  CAS  Article  Google Scholar 

  86. Uversky VN, Fink AL (2002) FEBS Lett 522:9–13

    PubMed  CAS  Article  Google Scholar 

  87. Chartier-Harlin MC, Kachergus J, Roumier C, Mouroux V, Douay X, Lincoln S, Levecque C, Larvor L, Andrieux J, Hulihan M, Waucquier N, Defebvre L, Amouyel P, Farrer M, Destee A (2004) Lancet 364:1167–1169

    PubMed  CAS  Article  Google Scholar 

  88. Ibanez P, Bonnet AM, Debarges B, Lohmann E, Tison F, Pollak P, Agid Y, Durr A, Brice A (2004) Lancet 364:1169–1171

    PubMed  CAS  Article  Google Scholar 

  89. Singleton AB, Farrer M, Johnson J, Singleton A, Hague S, Kachergus J, Hulihan M, Peuralinna T, Dutra A, Nussbaum R, Lincoln S, Crawley A, Hanson M, Maraganore D, Adler C, Cookson MR, Muenter M, Baptista M, Miller D, Blancato J, Hardy J, Gwinn-Hardy K (2003) Science 302:841

    PubMed  CAS  Article  Google Scholar 

  90. Chiba-Falek O, Nussbaum RL (2001) Hum Mol Genet 10:3101–3109

    PubMed  CAS  Article  Google Scholar 

  91. Farrer M, Maraganore DM, Lockhart P, Singleton A, Lesnick TG, de AM, West A, de SR, Hardy J, Hernandez D (2001) Hum Mol Genet 10:1847–1851

    PubMed  CAS  Article  Google Scholar 

  92. Kruger R, Vieira-Saecker AM, Kuhn W, Berg D, Muller T, Kuhnl N, Fuchs GA, Storch A, Hungs M, Woitalla D, Przuntek H, Epplen JT, Schols L, Riess O (1999) Ann Neurol 45:611–617

    PubMed  CAS  Article  Google Scholar 

  93. Tan EK, Matsuura T, Nagamitsu S, Khajavi M, Jankovic J, Ashizawa T (2000) Neurology 54:1195–1198

    PubMed  CAS  Google Scholar 

  94. Feany MB, Bender WW (2000) Nature 404:394–398

    PubMed  CAS  Article  Google Scholar 

  95. Dawson TM, Ko HS, Dawson VL (2010) Neuron 66:646–661

    PubMed  CAS  Article  Google Scholar 

  96. Eslamboli A, Romero-Ramos M, Burger C, Bjorklund T, Muzyczka N, Mandel RJ, Baker H, Ridley RM, Kirik D (2007) Brain 130:799–815

    PubMed  Article  Google Scholar 

  97. Kahle PJ (2008) Acta Neuropathol 115:87–95

    PubMed  CAS  Article  Google Scholar 

  98. Uversky VN, Oldfield CJ, Dunker AK (2005) J Mol Recognit 18:343–384

    PubMed  CAS  Article  Google Scholar 

  99. Hoyer W, Cherny D, Subramaniam V, Jovin TM (2004) Biochemistry 43:16233–16242

    PubMed  CAS  Article  Google Scholar 

  100. McLean PJ, Hyman BT (2002) Neurosci Lett 323:219–223

    PubMed  CAS  Article  Google Scholar 

  101. Steiner JP, Dawson TM, Fotuhi M, Glatt CE, Snowman AM, Cohen N, Snyder SH (1992) Nature 358:584–587

    PubMed  CAS  Article  Google Scholar 

  102. Avramut M, Zeevi A, Achim CL (2001) Brain Res Dev Brain Res 132:151–157

    PubMed  CAS  Article  Google Scholar 

  103. Gold BG, Katoh K, Storm-Dickerson T (1995) J Neurosci 15:7509–7516

    PubMed  CAS  Google Scholar 

  104. Gold BG (1999) Drug Metab Rev 31:649–663

    PubMed  CAS  Article  Google Scholar 

  105. Jost SC, Doolabh VB, Mackinnon SE, Lee M, Hunter D (2000) Restor Neurol Neurosci 17:39–44

    PubMed  CAS  Google Scholar 

  106. Pardo R, Colin E, Regulier E, Aebischer P, Deglon N, Humbert S, Saudou F (2006) J Neurosci 26:1635–1645

    PubMed  CAS  Article  Google Scholar 

  107. Edlich F, Weiwad M, Wildemann D, Jarczowski F, Kilka S, Moutty MC, Jahreis G, Lucke C, Schmidt W, Striggow F, Fischer G (2006) J Biol Chem 281:14961–14970

    PubMed  CAS  Article  Google Scholar 

  108. Gold BG, Zeleny-Pooley M, Wang MS, Chaturvedi P, Armistead DM (1997) Exp Neurol 147:269–278

    PubMed  CAS  Article  Google Scholar 

  109. Guo X, Dawson VL, Dawson TM (2001) Eur J Neurosci 13:1683–1693

    PubMed  CAS  Article  Google Scholar 

  110. Steiner JP, Hamilton GS, Ross DT, Valentine HL, Guo H, Connolly MA, Liang S, Ramsey C, Li JH, Huang W, Howorth P, Soni R, Fuller M, Sauer H, Nowotnik AC, Suzdak PD (1997) Proc Natl Acad Sci U S A 94:2019–2024

    PubMed  CAS  Article  Google Scholar 

  111. Gold BG, Udina E, Bourdette D, Navarro X (2004) Neurol Res 26:371–380

    PubMed  CAS  Article  Google Scholar 

  112. Pong K, Zaleska MM (2003) Curr Drug Targets CNS Neurol Disord 2:349–356

    PubMed  CAS  Article  Google Scholar 

  113. Charters AR, Kobayashi M, Butcher SP (1994) Biochem Soc Trans 22:412S

    PubMed  CAS  Google Scholar 

  114. Charters AR, Kobayashi M, Butcher SP (1994) Biochem Soc Trans 22:411S

    PubMed  CAS  Google Scholar 

  115. Coss MC, Stephens RM, Morrison DK, Winterstein D, Smith LM, Simek SL (1998) Cell Growth Differ 9:41–48

    PubMed  CAS  Google Scholar 

  116. Avramut M, Achim CL (2002) Physiol Behav 77:463–468

    PubMed  CAS  Article  Google Scholar 

  117. Labrande C, Velly L, Canolle B, Guillet B, Masmejean F, Nieoullon A, Pisano P (2006) Neuroscience 137:231–239

    PubMed  CAS  Article  Google Scholar 

  118. Kato H, Oikawa T, Otsuka K, Takahashi A, Itoyama Y (2000) Brain Res Mol Brain Res 84:58–66

    PubMed  CAS  Article  Google Scholar 

  119. Brecht S, Schwarze K, Waetzig V, Christner C, Heiland S, Fischer G, Sartor K, Herdegen T (2003) Neuroscience 120:1037–1048

    PubMed  CAS  Article  Google Scholar 

  120. Sugata H, Matsuo K, Nakagawa T, Takahashi M, Mukai H, Ono Y, Maeda K, Akiyama H, Kawamata T (2009) Neurosci Lett 459:96–99

    PubMed  CAS  Article  Google Scholar 

  121. Gerard M, Debyser Z, Desender L, Kahle PJ, Baert J, Baekelandt V, Engelborghs Y (2006) FASEB J 20:524–526

    PubMed  CAS  Google Scholar 

  122. Gerard M, Debyser Z, Desender L, Baert J, Brandt I, Baekelandt V, Engelborghs Y (2008) J Neurochem 106:121–133

    PubMed  CAS  Article  Google Scholar 

  123. Gerard M, Deleersnijder A, Daniels V, Schreurs S, Munck S, Reumers V, Pottel H, Engelborghs Y, Van den HC, Taymans JM, Debyser Z, Baekelandt V (2010) J Neurosci 30:2454–2463

    PubMed  CAS  Article  Google Scholar 

  124. Deleersnijder A, Desender L, Pottel H, Buee L, Debyser Z, Baekelandt V, Gerard M (2010) in revision

  125. Thibault O, Gant JC, Landfield PW (2007) Aging Cell 6:307–317

    PubMed  CAS  Article  Google Scholar 

  126. Caporello E, Nath A, Slevin J, Galey D, Hamilton G, Williams L, Steiner JP, Haughey NJ (2006) J Neurochem 98:146–155

    PubMed  CAS  Article  Google Scholar 

  127. Bultynck G, De SP, Weidema AF, Ver HM, Maes K, Callewaert G, Missiaen L, Parys JB, De SH (2000) J Physiol 525(Pt 3):681–693

    PubMed  CAS  Article  Google Scholar 

  128. Shirane M, Nakayama KI (2003) Nat Cell Biol 5:28–37

    PubMed  CAS  Article  Google Scholar 

  129. Edlich F, Weiwad M, Erdmann F, Fanghanel J, Jarczowski F, Rahfeld JU, Fischer G (2005) EMBO J 24:2688–2699

    PubMed  CAS  Article  Google Scholar 

  130. Gold BG, Densmore V, Shou W, Matzuk MM, Gordon HS (1999) J Pharmacol Exp Ther 289:1202–1210

    PubMed  CAS  Google Scholar 

  131. Baughman G, Wiederrecht GJ, Campbell NF, Martin MM, Bourgeois S (1995) Mol Cell Biol 15:4395–4402

    PubMed  CAS  Google Scholar 

  132. Yong W, Yang Z, Periyasamy S, Chen H, Yucel S, Li W, Lin LY, Wolf IM, Cohn MJ, Baskin LS, Sanchez ER, Shou W (2007) J Biol Chem 282:5026–5036

    PubMed  CAS  Article  Google Scholar 

  133. Sanokawa-Akakura R, Dai H, Akakura S, Weinstein D, Fajardo JE, Lang SE, Wadsworth S, Siekierka J, Birge RB (2004) J Biol Chem 279:27845–27848

    PubMed  CAS  Article  Google Scholar 

  134. Chambraud B, Sardin E, Giustiniani J, Dounane O, Schumacher M, Goedert M, Baulieu EE (2010) Proc Natl Acad Sci U S A 107:2658–2663

    PubMed  CAS  Article  Google Scholar 

  135. Jinwal UK, Koren J III, Borysov SI, Schmid AB, Abisambra JF, Blair LJ, Johnson AG, Jones JR, Shults CL, O'Leary JC III, Jin Y, Buchner J, Cox MB, Dickey CA (2010) J Neurosci 30:591–599

    PubMed  CAS  Article  Google Scholar 

  136. Wang GX, Poo MM (2005) Nature 434:898–904

    PubMed  CAS  Article  Google Scholar 

  137. Miniero R, Tardivo I, Curtoni ES, Segoloni GP, La RE, Nino A, Todeschini P, Tregnaghi C, Rosati A, Zanelli P, Dall'Omo AM (2002) J Nephrol 15:626–632

    PubMed  Google Scholar 

  138. Patterson CE, Schaub T, Coleman EJ, Davis EC (2000) Mol Biol Cell 11:3925–3935

    PubMed  CAS  Google Scholar 

  139. Zeng B, MacDonald JR, Bann JG, Beck K, Gambee JE, Boswell BA, Bachinger HP (1998) Biochem J 330(Pt 1):109–114

    PubMed  CAS  Google Scholar 

  140. Davis EC, Broekelmann TJ, Ozawa Y, Mecham RP (1998) J Cell Biol 140:295–303

    PubMed  CAS  Article  Google Scholar 

  141. Baker CA, Manuelidis L (2003) Proc Natl Acad Sci U S A 100:675–679

    PubMed  CAS  Article  Google Scholar 

  142. Klettner A, Herdegen T (2003) Br J Pharmacol 138:1004–1012

    PubMed  CAS  Article  Google Scholar 

  143. Domanska-Janik K, Buzanska L, Dluzniewska J, Kozlowska H, Sarnowska A, Zablocka B (2004) Brain Res Mol Brain Res 121:50–59

    PubMed  CAS  Article  Google Scholar 

  144. Mbye LH, Singh IN, Carrico KM, Saatman KE, Hall ED (2008) J Cereb Blood Flow Metab 29:87–97

    PubMed  Article  CAS  Google Scholar 

  145. Sinigaglia-Coimbra R, Cavalheiro EA, Coimbra C (2002) J Neurol Sci 203–204:273–276

    PubMed  Article  Google Scholar 

  146. Baines CP, Kaiser RA, Purcell NH, Blair NS, Osinska H, Hambleton MA, Brunskill EW, Sayen MR, Gottlieb RA, Dorn GW, Robbins J, Molkentin JD (2005) Nature 434:658–662

    PubMed  CAS  Article  Google Scholar 

  147. Marzo I, Brenner C, Zamzami N, Susin SA, Beutner G, Brdiczka D, Remy R, Xie ZH, Reed JC, Kroemer G (1998) J Exp Med 187:1261–1271

    PubMed  CAS  Article  Google Scholar 

  148. Schinzel AC, Takeuchi O, Huang Z, Fisher JK, Zhou Z, Rubens J, Hetz C, Danial NN, Moskowitz MA, Korsmeyer SJ (2005) Proc Natl Acad Sci U S A 102:12005–12010

    PubMed  CAS  Article  Google Scholar 

  149. Du H, Guo L, Fang F, Chen D, Sosunov AA, McKhann GM, Yan Y, Wang C, Zhang H, Molkentin JD, Gunn-Moore FJ, Vonsattel JP, Arancio O, Chen JX, Yan SD (2008) Nat Med 14:1097–1105

    PubMed  CAS  Article  Google Scholar 

  150. Cohen E, Taraboulos A (2003) EMBO J 22:404–417

    PubMed  CAS  Article  Google Scholar 

  151. Lu PJ, Wulf G, Zhou XZ, Davies P, Lu KP (1999) Nature 399:784–788

    PubMed  CAS  Article  Google Scholar 

  152. Pastorino L, Sun A, Lu PJ, Zhou XZ, Balastik M, Finn G, Wulf G, Lim J, Li SH, Li X, Xia W, Nicholson LK, Lu KP (2006) Nature 440:528–534

    PubMed  CAS  Article  Google Scholar 

  153. Sultana R, Boyd-Kimball D, Poon HF, Cai J, Pierce WM, Klein JB, Markesbery WR, Zhou XZ, Lu KP, Butterfield DA (2006) Neurobiol Aging 27:918–925

    PubMed  CAS  Article  Google Scholar 

  154. Ryo A, Togo T, Nakai T, Hirai A, Nishi M, Yamaguchi A, Suzuki K, Hirayasu Y, Kobayashi H, Perrem K, Liou YC, Aoki I (2006) J Biol Chem 281:4117–4125

    PubMed  CAS  Article  Google Scholar 

  155. Poulter MO, Payne KB, Steiner JP (2004) Neuroscience 128:1–6

    PubMed  CAS  Article  Google Scholar 

  156. Sommer DB, Stacy MA (2008) Expert Rev Neurother 8:1829–1839

    PubMed  CAS  Article  Google Scholar 

  157. Gasser T (2009) Neurology 72:S27–S31

    PubMed  CAS  Article  Google Scholar 

  158. Tolosa E, Gaig C, Santamaria J, Compta Y (2009) Neurology 72:S12–S20

    PubMed  Article  Google Scholar 

  159. Marshall VL, Grosset DG (2004) Curr Opin Investig Drugs 5:107–112

    PubMed  CAS  Google Scholar 

  160. Kupina NC, Detloff MR, Dutta S, Hall ED (2002) J Cereb Blood Flow Metab 22:1212–1221

    PubMed  CAS  Article  Google Scholar 

  161. Griffith JP, Kim JL, Kim EE, Sintchak MD, Thomson JA, Fitzgibbon MJ, Fleming MA, Caron PR, Hsiao K, Navia MA (1995) Cell 82:507–522

    PubMed  CAS  Article  Google Scholar 

  162. Ochocka AM, Kampanis P, Nicol S, Lende-Vega N, Cox M, Marcar L, Milne D, Fuller-Pace F, Meek D (2009) FEBS Lett 583:621–626

    PubMed  CAS  Article  Google Scholar 

  163. Viklund IM, Aspenstrom P, Meas-Yedid V, Zhang B, Kopec J, Agren D, Schneider G, D'Amato M, Olivo-Marin JC, Sansonetti P, Van Nhieu GT, Pettersson S (2009) Exp Cell Res 315:1040–1052

    PubMed  CAS  Article  Google Scholar 

  164. Jarczowski F, Jahreis G, Erdmann F, Schierhorn A, Fischer G, Edlich F (2009) J Biol Chem 284:766–773

    PubMed  CAS  Article  Google Scholar 

  165. Jarczowski F, Fischer G, Edlich F (2008) Biochemistry 47:6946–6952

    PubMed  CAS  Article  Google Scholar 

  166. Ma Q, Whitlock JP Jr (1997) J Biol Chem 272:8878–8884

    PubMed  CAS  Article  Google Scholar 

  167. Kashuba E, Kashuba V, Pokrovskaja K, Klein G, Szekely L (2000) Oncogene 19:1801–1806

    PubMed  CAS  Article  Google Scholar 

  168. Davies TH, Ning YM, Sanchez ER (2005) Biochemistry 44:2030–2038

    PubMed  CAS  Article  Google Scholar 

  169. Quinta HR, Maschi D, Gomez-Sanchez C, Piwien-Pilipuk G, Galigniana MD (2010) J Neurochem 115:716–734

    PubMed  CAS  Article  Google Scholar 

  170. Li L, Lou Z, Wang L (2010) Br. J. Cancer

  171. Shim S, Yuan JP, Kim JY, Zeng W, Huang G, Milshteyn A, Kern D, Muallem S, Ming GL, Worley PF (2009) Neuron 64:471–483

    PubMed  CAS  Article  Google Scholar 

  172. Neye H, Verspohl EJ (2004) BMC Pharmacol 4:19

    PubMed  Article  CAS  Google Scholar 

  173. Padilla PI, Chang MJ, Pacheco-Rodriguez G, Adamik R, Moss J, Vaughan M (2003) Proc Natl Acad Sci U S A 100:2322–2327

    PubMed  CAS  Article  Google Scholar 

  174. Halatsch ME, Low S, Hielscher T, Schmidt U, Unterberg A, Vougioukas VI (2008) Anticancer Res 28:3725–3728

    PubMed  Google Scholar 

  175. Zhang X, Wang Y, Li H, Zhang W, Wu D, Mi H (2004) FEBS Lett 559:57–60

    PubMed  CAS  Article  Google Scholar 

  176. Shadidy M, Caubit X, Olsen R, Seternes OM, Moens U, Krauss S (1999) Biochim Biophys Acta 1446:295–307

    PubMed  CAS  Google Scholar 

  177. Alanay Y, Avaygan H, Camacho N, Utine GE, Boduroglu K, Aktas D, Alikasifoglu M, Tuncbilek E, Orhan D, Bakar FT, Zabel B, Superti-Furga A, Bruckner-Tuderman L, Curry CJ, Pyott S, Byers PH, Eyre DR, Baldridge D, Lee B, Merrill AE, Davis EC, Cohn DH, Akarsu N, Krakow D (2010) Am J Hum Genet 87:572–573

    CAS  Article  Google Scholar 

  178. Ishikawa Y, Vranka J, Wirz J, Nagata K, Bachinger HP (2008) J Biol Chem 283:31584–31590

    PubMed  CAS  Article  Google Scholar 

  179. Baum N, Schiene-Fischer C, Frost M, Schumann M, Sabapathy K, Ohlenschlager O, Grosse F, Schlott B (2009) Oncogene 28:3915–3925

    PubMed  CAS  Article  Google Scholar 

  180. Pan H, Luo C, Li R, Qiao A, Zhang L, Mines M, Nyanda AM, Zhang J, Fan GH (2008) J Biol Chem 283:623–637

    PubMed  CAS  Article  Google Scholar 

  181. Braaten D, Luban J (2001) EMBO J 20:1300–1309

    PubMed  CAS  Article  Google Scholar 

  182. Fernandes F, Ansari IU, Striker R (2010) PLoS ONE 5:e9815

    PubMed  Article  CAS  Google Scholar 

  183. Meza-Zepeda LA, Forus A, Lygren B, Dahlberg AB, Godager LH, South AP, Marenholz I, Lioumi M, Florenes VA, Maelandsmo GM, Serra M, Mischke D, Nizetic D, Ragoussis J, Tarkkanen M, Nesland JM, Knuutila S, Myklebost O (2002) Oncogene 21:2261–2269

    PubMed  CAS  Article  Google Scholar 

  184. Kuhn AN, van Santen MA, Schwienhorst A, Urlaub H, Luhrmann R (2009) RNA 15:153–175

    PubMed  CAS  Article  Google Scholar 

  185. Obama K, Kato T, Hasegawa S, Satoh S, Nakamura Y, Furukawa Y (2006) Clin Cancer Res 12:70–76

    PubMed  CAS  Article  Google Scholar 

  186. Galat A, Bouet F (1994) FEBS Lett 347:31–36

    PubMed  CAS  Article  Google Scholar 

  187. Stumpf T, Zhang Q, Hirnet D, Lewandrowski U, Sickmann A, Wissenbach U, Dorr J, Lohr C, Deitmer JW, Fecher-Trost C (2008) J Biol Chem 283:18086–18098

    PubMed  CAS  Article  Google Scholar 

  188. Schneider H, Charara N, Schmitz R, Wehrli S, Mikol V, Zurini MG, Quesniaux VF, Movva NR (1994) Biochemistry 33:8218–8224

    PubMed  CAS  Article  Google Scholar 

  189. Chiara F, Castellaro D, Marin O, Petronilli V, Brusilow WS, Juhaszova M, Sollott SJ, Forte M, Bernardi P, Rasola A (2008) PLoS ONE 3:e1852

    PubMed  Article  CAS  Google Scholar 

  190. Millay DP, Sargent MA, Osinska H, Baines CP, Barton ER, Vuagniaux G, Sweeney HL, Robbins J, Molkentin JD (2008) Nat Med 14:442–447

    PubMed  CAS  Article  Google Scholar 

  191. Mi H, Kops O, Zimmermann E, Jaschke A, Tropschug M (1996) FEBS Lett 398:201–205

    PubMed  CAS  Article  Google Scholar 

  192. Gudbjartsson DF, Walters GB, Thorleifsson G, Stefansson H, Halldorsson BV, Zusmanovich P, Sulem P, Thorlacius S, Gylfason A, Steinberg S, Helgadottir A, Ingason A, Steinthorsdottir V, Olafsdottir EJ, Olafsdottir GH, Jonsson T, Borch-Johnsen K, Hansen T, Andersen G, Jorgensen T, Pedersen O, Aben KK, Witjes JA, Swinkels DW, den HM, Franke B, Verbeek AL, Becker DM, Yanek LR, Becker LC, Tryggvadottir L, Rafnar T, Gulcher J, Kiemeney LA, Kong A, Thorsteinsdottir U, Stefansson K (2008) Nat Genet 40:609–615

    PubMed  CAS  Article  Google Scholar 

  193. Carrello A, Allan RK, Morgan SL, Owen BA, Mok D, Ward BK, Minchin RF, Toft DO, Ratajczak T (2004) Cell Stress Chaperones 9:167–181

    PubMed  CAS  Article  Google Scholar 

  194. Peyrl A, Krapfenbauer K, Slavc I, Yang JW, Strobel T, Lubec G (2003) Proteomics 3:1781–1800

    PubMed  CAS  Article  Google Scholar 

  195. Olsen JV, Blagoev B, Gnad F, Macek B, Kumar C, Mortensen P, Mann M (2006) Cell 127:635–648

    PubMed  CAS  Article  Google Scholar 

  196. Dubourg B, Kamphausen T, Weiwad M, Jahreis G, Feunteun J, Fischer G, Modjtahedi N (2004) J Biol Chem 279:22322–22330

    PubMed  CAS  Article  Google Scholar 

  197. Sakashita E, Tatsumi S, Werner D, Endo H, Mayeda A (2004) Mol Cell Biol 24:1174–1187

    PubMed  CAS  Article  Google Scholar 

  198. Dawlaty MM, Malureanu L, Jeganathan KB, Kao E, Sustmann C, Tahk S, Shuai K, Grosschedl R, van Deursen JM (2008) Cell 133:103–115

    PubMed  CAS  Article  Google Scholar 

  199. Rundle NT, Nelson J, Flory MR, Joseph J, Th'ng J, Aebersold R, Dasso M, Andersen RJ, Roberge M (2006) ACS Chem Biol 1:443–450

    PubMed  CAS  Article  Google Scholar 

  200. Winkler KE, Swenson KI, Kornbluth S, Means AR (2000) Science 287:1644–1647

    PubMed  CAS  Article  Google Scholar 

  201. Lu KP, Hanes SD, Hunter T (1996) Nature 380:544–547

    PubMed  CAS  Article  Google Scholar 

  202. Wulf GM, Ryo A, Wulf GG, Lee SW, Niu T, Petkova V, Lu KP (2001) EMBO J 20:3459–3472

    PubMed  CAS  Article  Google Scholar 

  203. Fujiyama-Nakamura S, Yoshikawa H, Homma K, Hayano T, Tsujimura-Takahashi T, Izumikawa K, Ishikawa H, Miyazawa N, Yanagida M, Miura Y, Shinkawa T, Yamauchi Y, Isobe T, Takahashi N (2009) Mol Cell Proteomics 8:1552–1565

    PubMed  CAS  Article  Google Scholar 

  204. Reimer T, Weiwad M, Schierhorn A, Ruecknagel PK, Rahfeld JU, Bayer P, Fischer G (2003) J Mol Biol 330:955–966

    PubMed  CAS  Article  Google Scholar 

  205. Surmacz TA, Bayer E, Rahfeld JU, Fischer G, Bayer P (2002) J Mol Biol 321:235–247

    PubMed  CAS  Article  Google Scholar 

  206. Mueller JW, Kessler D, Neumann D, Stratmann T, Papatheodorou P, Hartmann-Fatu C, Bayer P (2006) BMC Mol Biol 7:9

    PubMed  Article  CAS  Google Scholar 

Download references

Author information

Affiliations

  1. Laboratory of Biochemistry, IRC, K.U. Leuven-Kortrijk, Etienne Sabbelaan 53, 8500, Kortrijk, Flanders, Belgium

    Melanie Gerard, Angélique Deleersnijder & Zeger Debyser

  2. Laboratory of Molecular Virology and Gene Therapy, K.U. Leuven, Kapucijnenvoer 33, 3000, Leuven, Flanders, Belgium

    Jonas Demeulemeester & Zeger Debyser

  3. Laboratory of Neurobiology and Gene Therapy, K. U. Leuven, Kapucijnenvoer 33, 3000, Leuven, Flanders, Belgium

    Melanie Gerard, Angélique Deleersnijder & Veerle Baekelandt

Authors
  1. Melanie Gerard
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Angélique Deleersnijder
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jonas Demeulemeester
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zeger Debyser
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Veerle Baekelandt
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Veerle Baekelandt.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Gerard, M., Deleersnijder, A., Demeulemeester, J. et al. Unraveling the Role of Peptidyl-Prolyl Isomerases in Neurodegeneration. Mol Neurobiol 44, 13–27 (2011). https://doi.org/10.1007/s12035-011-8184-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12035-011-8184-2

Keywords

  • FK506 binding proteins
  • Immunophilins
  • Immunophilin ligands
  • Parvulins
  • Cyclophilins
  • Neurodegeneration
  • Parkinson’s disease